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The role of polymorphonuclear neutrophils during HIV-1 infection

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Abstract

It is well-recognized that human immunodeficiency virus type-1 (HIV-1) mainly targets CD4+ T cells and macrophages. Nonetheless, during the past three decades, a huge number of studies have reported that HIV-1 can directly or indirectly target other cellular components of the immune system including CD8+ T cells, B cells, dendritic cells, natural killer cells, and polymorphonuclear neutrophils (PMNs), among others. PMNs are the most abundant leukocytes in the human circulation, and are known to play principal roles in the elimination of invading pathogens, regulating different immune responses, healing of injured tissues, and maintaining mucosal homeostasis. Until recently, little was known about the impact of HIV-1 infection on PMNs as well as the impact of PMNs on HIV-1 disease progression. This is because early studies focused on neutropenia and recurrent microbial infections, particularly, during advanced disease. However, recent studies have extended the investigation area to cover new aspects of the interactions between HIV-1 and PMNs. This review aims to summarize these advances and address the impact of HIV-1 infection on PMNs as well as the impact of PMNs on HIV-1 disease progression to better understand the pathophysiology of HIV-1 infection.

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References

  1. Moir S, Ho J, Malaspina A (2008) Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med 205:1797–1805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Moir S, Malaspina A, Ogwaro KM, Donoghue ET, Hallahan CW, Ehler LA, Liu S, Adelsberger J, Lapointe R, Hwu P, Baseler M, Orenstein JM, Chun TW, Mican JA, Fauci AS (2001) HIV-1 induces phenotypic and functional perturbations of B cells in chronically infectedindividuals. Proc Natl Acad Sci USA 98:10362–10367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Mureithi MW, Cohen K, Moodley R, Poole D, Mncube Z, Kasmar A, Moody DB, Goulder PJ, Walker BD, Altfeld M, Ndung’u T (2011) Impairment of CD1d-restricted natural killer T cells in chronic HIV type 1 clade C infection. AIDS Res Hum Retrovir 27:50150–50159

    Google Scholar 

  4. Cella M, Presti R, Vermi W, Lavender K, Turnbull E, Ochsenbauer-Jambor C, Kappes JC, Ferrari G, Kessels L, Williams I, McMichael AJ, Haynes BF, Borrow P, Colonna M, CHAVI Clinical Core B, NIAID Center for HIV, AIDS Vaccine Immunology (2010) Loss of DNAM-1 contributes to CD8+ T-cell exhaustion in chronic HIV-1 infection. Eur J Immunol 40:949–954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Sachdeva M, Sharma A, Arora SK (2015) Functional impairment of myeloid dendritic cells during advanced stage of HIV-1 infection: role of factors regulating cytokine signaling. PLoS One 10:e0140852

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Cardone M, Ikeda KN, Varano B, Gessani S, Conti L (2015) HIV-1-induced impairment of dendritic cell cross talk with γδ T lymphocytes. J Virol 89:4798–4808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Fischer-Smith T, Tedaldi EM, Rappaport J (2008) CD163/CD16 coexpression by circulating monocytes/macrophages in HIV: potential biomarkers for HIV infection and AIDS progression. AIDS Res Hum Retrovir 24:417–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Pan X, Baldauf HM, Keppler OT, Fackler OT (2013) Restrictions to HIV-1 replication in resting CD4+ T lymphocytes. Cell Res 23:876–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zerbato JM, Serrao E, Lenzi G, Kim B, Ambrose Z, Watkins SC, Engelman AN, Sluis-Cremer N (2016) Establishment and reversal of HIV-1 latency in naive and central memory CD4+ T cells in vitro. J Virol 90:8059–8073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Koppensteiner H, Brack-Werner R, Schindler M (2012) Macrophages and their relevance in human immunodeficiency virus type I infection. Retrovirology 9:82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Honeycutt JB, Wahl A, Baker C, Spagnuolo RA, Foster J, Zakharova O, Wietgrefe S, Caro-Vegas C, Madden V, Sharpe G, Haase AT, Eron JJ, Garcia JV (2016) Macrophages sustain HIV replication in vivo independently of T cells. J Clin Invest 126:1353–1366

    Article  PubMed  PubMed Central  Google Scholar 

  12. Kumar A, Herbein G (2014) The macrophage: a therapeutic target in HIV-1 infection. Mol Cell Ther 2:10

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kumar A, Abbas W, Herbein G (2014) HIV-1 latency in monocytes/macrophages. Viruses 6:1837–1860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Araínga M, Edagwa B, Mosley RL, Poluektova LY, Gorantla S, Gendelman HE (2017) A mature macrophage is a principal HIV-1 cellular reservoir in humanized mice after treatment with long acting antiretroviral therapy. Retrovirology 14:17

    Article  PubMed  PubMed Central  Google Scholar 

  15. Honeycutt JB, Thayer WO, Baker CE, Ribeiro RM, Lada SM, Cao Y, Cleary RA, Hudgens MG, Richman DD, Garcia JV (2017) HIV persistence in tissue macrophages of humanized myeloid-only mice during antiretroviral therapy. Nat Med 23:638–643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Rinaldo CR (2013) HIV-1 trans infection of CD4(+) T cells by professional antigen presenting cells. Scientifica (Cairo) 2013:164203

    Google Scholar 

  17. Peressin M, Proust A, Schmidt S, Su B, Lambotin M, Biedma ME, Laumond G, Decoville T, Holl V, Moog C (2014) Efficient transfer of HIV-1 in trans and in cis from Langerhans dendritic cells and macrophages to autologous T lymphocytes. AIDS 28:667–677

    Article  CAS  PubMed  Google Scholar 

  18. Crowe S, Zhu T, Muller WA (2003) The contribution of monocyte infection and trafficking to viral persistence, and maintenance of the viral reservoir in HIV infection. J Leukoc Biol 74:635–641

    Article  CAS  PubMed  Google Scholar 

  19. McIlroy D, Autran B, Cheynier R, Wain-Hobson S, Clauvel JP, Oksenhendler E, Debré P, Hosmalin A (1995) Infection frequency of dendritic cells and CD4+ T lymphocytes in spleens of human immunodeficiency virus-positive patients. J Virol 69:4737–4745

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Wonderlich ER, Barratt-Boyes SM (2012) A dendrite in every pie: myeloid dendritic cells in HIV and SIV infection. Virulence 3:647–653

    Article  PubMed  PubMed Central  Google Scholar 

  21. Alqudah MAY, Yaseen MMM, Yaseen MSM (2016) HIV-1 strategies to overcome the immune system by evading and invading innate immune system. HIV AIDS Rev 15:1–12

    Article  Google Scholar 

  22. Pillay J, den Braber I, Vrisekoop N, Kwast LM, de Boer RJ, Borghans JA, Tesselaar K, Koenderman L (2010) In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 116:625–627

    Article  CAS  PubMed  Google Scholar 

  23. Saitoh T, Komano J, Saitoh Y, Misawa T, Takahama M, Kozaki T, Uehata T, Iwasaki H, Omori H, Yamaoka S, Yamamoto N, Akira S (2012) Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 12:109–116

    Article  CAS  PubMed  Google Scholar 

  24. Drescher B, Bai F (2013) Neutrophil in viral infections, friend or foe? Virus Res 171:1–7

    Article  CAS  PubMed  Google Scholar 

  25. Kolaczkowska E, Kubes P (2013) Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13:159–175

    Article  CAS  PubMed  Google Scholar 

  26. Rot A, von Andrian UH (2004) Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol 22:891–928

    Article  CAS  PubMed  Google Scholar 

  27. Charo IF, Ransohoff RM (2006) The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354:610–621

    Article  CAS  PubMed  Google Scholar 

  28. Hayashi F, Means TK, Luster AD (2003) Toll-like receptors stimulate human neutrophil function. Blood 102:2660–2669

    Article  CAS  PubMed  Google Scholar 

  29. Kennedy AD, Willment JA, Dorward DW, Williams DL, Brown GD, DeLeo FR (2007) Dectin-1 promotes fungicidal activity of human neutrophils. Eur J Immunol 37:467–478

    Article  CAS  PubMed  Google Scholar 

  30. Ekman AK, Cardell LO (2010) The expression and function of Nod-like receptors in neutrophils. Immunology 130:55–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. van Kessel KP, Bestebroer J, van Strijp JA (2014) Neutrophil-mediated phagocytosis of Staphylococcus aureus. Front Immunol 5:467

    PubMed  PubMed Central  Google Scholar 

  32. Witko-Sarsat V, Rieu P, Descamps-Latscha B, Lesavre P, Halbwachs-Mecarelli L (2000) Neutrophils: molecules, functions and pathophysiological aspects. Lab Invest 80:617–653

    Article  CAS  PubMed  Google Scholar 

  33. Nimmerjahn F, Ravetch JV (2006) Fc receptors: old friends and new family members. Immunity 24:19–28

    Article  CAS  PubMed  Google Scholar 

  34. Repp R, Valerius T, Sendler A, Gramatzki M, Iro H, Kalden JR, Platzer E (1991) Neutrophils express the high affinity receptor for IgG (Fc γ RI, CD64) after in vivo application of recombinant human granulocyte colony-stimulating factor. Blood 78:885–889

    CAS  PubMed  Google Scholar 

  35. Thomas CJ, Schroder K (2013) Pattern recognition receptor function in neutrophils. Trends Immunol 34:317–328

    Article  CAS  PubMed  Google Scholar 

  36. Futosi K, Fodor S, Mócsai A (2013) Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int Immunopharmacol 17:638–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hochreiter-Hufford A, Ravichandran KS (2013) Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol 5:a008748

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Smalls-Mantey A, Connors M, Sattentau QJ (2013) Comparative efficiency of HIV-1-infected T cell killing by NK cells, monocytes and neutrophils. PLoS One 8:e74858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A (2007) Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176:231–241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Johansson A, Jesaitis AJ, Lundqvist H, Magnusson KE, Sjölin C, Karlsson A, Dahlgren C (1995) Different subcellular localization of cytochrome b and the dormant NADPH-oxidase in neutrophils and macrophages: effect on the production of reactive oxygen species during phagocytosis. Cell Immunol 161:61–71

    Article  CAS  PubMed  Google Scholar 

  41. Karlsson A, Dahlgren C (2002) Assembly and activation of the neutrophil NADPH oxidase in granule membranes. Antioxid Redox Signal 4:49–60

    Article  CAS  PubMed  Google Scholar 

  42. Sips M, Krykbaeva M, Diefenbach TJ, Ghebremichael M, Bowman BA, Dugast AS, Boesch AW, Streeck H, Kwon DS, Ackerman ME, Suscovich TJ, Brouckaert P, Schacker TW, Alter G (2016) Fc receptor-mediated phagocytosis in tissues as a potent mechanism for preventive and therapeutic HIV vaccine strategies. Mucosal Immunol 9:1584–1595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Segal AW, Dorling J, Coade S (1980) Kinetics of fusion of the cytoplasmic granules with phagocytic vacuoles in human polymorphonuclear leukocytes. Biochemical and morphological studies. J Cell Biol 85:42–59

    Article  CAS  PubMed  Google Scholar 

  44. Henry RM, Hoppe AD, Joshi N, Swanson JA (2004) The uniformity of phagosome maturation in macrophages. J Cell Biol 164:185–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303:1532–1535

    Article  CAS  PubMed  Google Scholar 

  46. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 5:e1000639

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Desai J, Mulay SR, Nakazawa D, Anders HJ (2016) Matters of life and death. How neutrophils die or survive along NET release and is “NETosis” = necroptosis? Cell Mol Life Sci 73:2211–2219

    Article  CAS  PubMed  Google Scholar 

  48. Bennouna S, Denkers EY (2005) Microbial antigen triggers rapid mobilization of TNF-alpha to the surface of mouse neutrophils transforming them into inducers of high-level dendritic cell TNF-alpha production. J Immunol 174:4845–4851

    Article  CAS  PubMed  Google Scholar 

  49. van Gisbergen KP, Ludwig IS, Geijtenbeek TB, van Kooyk Y (2005) Interactions of DC-SIGN with Mac-1 and CEACAM1 regulate contact between dendritic cells and neutrophils. FEBS Lett 579:6159–6168

    Article  PubMed  CAS  Google Scholar 

  50. van Gisbergen KP, Sanchez-Hernandez M, Geijtenbeek TB, van Kooyk Y (2005) Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J Exp Med 201:1281–1292

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Micheletti A, Costantini C, Calzetti F, Camuesco D, Costa S, Tamassia N, Cassatella MA (2013) Neutrophils promote 6-sulfo LacNAc+ dendritic cell (slanDC) survival. J Leukoc Biol 94:705–710

    Article  CAS  PubMed  Google Scholar 

  52. Yang D, de la Rosa G, Tewary P, Oppenheim JJ (2009) Alarmins link neutrophils and dendritic cells. Trends Immunol 30:531–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Megiovanni AM, Sanchez F, Robledo-Sarmiento M, Morel C, Gluckman JC, Boudaly S (2006) Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J Leukoc Biol 79:977–988

    Article  CAS  PubMed  Google Scholar 

  54. Maffia PC, Zittermann SE, Scimone ML, Tateosian N, Amiano N, Guerrieri D, Lutzky V, Rosso D, Romeo HE, Garcia VE, Issekutz AC, Chuluyan HE (2007) Neutrophil elastase converts human immature dendritic cells into transforming growth factor-beta1-secreting cells and reduces allostimulatory ability. Am J Pathol 171:928–937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Eken C, Gasser O, Zenhaeusern G, Oehri I, Hess C, Schifferli JA (2008) Polymorphonuclear neutrophil-derived ectosomes interfere with the maturation of monocyte-derived dendritic cells. J Immunol 180:817–824

    Article  CAS  PubMed  Google Scholar 

  56. Kasama T, Streiter RM, Standiford TJ, Burdick MD, Kunkel SL (1993) Expression and regulation of human neutrophil-derived macrophage inflammatory protein 1-α. J Exp Med 78:63–72

    Article  Google Scholar 

  57. Kumar V, Sharma A (2010) Neutrophils: Cinderella of innate immune system. Int Immunopharmacol 10:1325–1334

    Article  CAS  PubMed  Google Scholar 

  58. Kasama T, Streiter RM, Lukacs NW, Burdick MD, Kunkel SL (1994) Regulation of neutrophil-derived chemokine expression by IL-10. J Immunol 152:3559–3569

    CAS  PubMed  Google Scholar 

  59. Silva MT (2010) When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J Leukoc Biol 87:93–106

    Article  CAS  PubMed  Google Scholar 

  60. Horckmans M, Ring L, Duchene J, Santovito D, Schloss MJ, Drechsler M, Weber C, Soehnlein O, Steffens S (2017) Neutrophils orchestrate post-myocardial infarction healing by polarizing macrophages towards a reparative phenotype. Eur Heart J 38:187–197

    PubMed  Google Scholar 

  61. Zahran N, Sayed A, William I, Mahmoud O, Sabry O, Rafaat M (2013) Neutrophil apoptosis: impact of granulocyte macrophage colony stimulating factor on cell survival and viability in chronic kidney disease and hemodialysis patients. Arch Med Sci 9:984–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Mathias B, Szpila BE, Moore FA, Efron PA, Moldawer LL (2015) A review of GM-CSF therapy in sepsis. Medicine (Baltimore) 94:e2044

    Article  CAS  Google Scholar 

  63. Nakazawa D, Shida H, Kusunoki Y, Miyoshi A, Nishio S, Tomaru U, Atsumi T, Ishizu A (2016) The responses of macrophages in interaction with neutrophils that undergo NETosis. J Autoimmun 67:19–28

    Article  CAS  PubMed  Google Scholar 

  64. Spörri R, Joller N, Hilbi H, Oxenius A (2008) A novel role for neutrophils as critical activators of NK cells. J Immunol 181:7121–7130

    Article  PubMed  Google Scholar 

  65. Jaeger BN, Donadieu J, Cognet C, Bernat C, Ordoñez-Rueda D, Barlogis V, Mahlaoui N, Fenis A, Narni-Mancinelli E, Beaupain B, Bellanné-Chantelot C, Bajénoff M, Malissen B, Malissen M, Vivier E, Ugolini S (2012) Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J Exp Med 209:565–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Degli-Esposti MA, Smyth MJ (2005) Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat Rev Immunol 5:112

    Article  CAS  PubMed  Google Scholar 

  67. Costantini C, Micheletti A, Calzetti F, Perbellini O, Pizzolo G, Cassatella MA (2010) Neutrophil activation and survival are modulated by interaction with NK cells. Int Immunol 22:827–838

    Article  CAS  PubMed  Google Scholar 

  68. Costantini C, Cassatella MA (2011) The defensive alliance between neutrophils and NK cells as a novel arm of innate immunity. J Leukoc Biol 89:221–233

    Article  CAS  PubMed  Google Scholar 

  69. Bangani N, Nakiwala J, Martineau AR, Wilkinson RJ, Wilkinson KA, Lowe DM (2016) Brief report: HIV-1 infection impairs CD16 and CD35 mediated opsonophagocytosis of Mycobacterium tuberculosis by human neutrophils. J Acquir Immune Defic Syndr 73:263–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kuritzkes DR (2000) Neutropenia, neutrophil dysfunction, and bacterial infection in patients with human immunodeficiency virus disease: the role of granulocyte colony-stimulating factor. Clin Infect Dis 30:256–260

    Article  CAS  PubMed  Google Scholar 

  71. Cloke T, Munder M, Bergin P, Herath S, Modolell M, Taylor G, Müller I, Kropf P (2013) Phenotypic alteration of neutrophils in the blood of HIV seropositive patients. PLoS One 8:e72034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Shi X, Sims MD, Hanna MM, Xie M, Gulick PG, Zheng YH, Basson MD, Zhang P (2014) Neutropenia during HIV infection: adverse consequences and remedies. Int Rev Immunol 33:511–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Keiser P, Higgs E, Smith J (1996) Neutropenia is associated with bacteremia in patients infected with the human immunodeficiency virus. Am J Med Sci 312:118–122

    Article  CAS  PubMed  Google Scholar 

  74. Babadoko AA, Aminu SM, Suleiman AN (2008) Neutropenia and human immunodeficiency virus-1 infection: analysis of 43 cases. Niger J Med 17:57–60

    Article  CAS  PubMed  Google Scholar 

  75. Levine AM, Karim R, Mack W, Gravink DJ, Anastos K, Young M, Cohen M, Newman M, Augenbraun M, Gange S, Watts DH (2006) Neutropenia in human immunodeficiency virus infection: data from the women’s interagency HIV study. Arch Intern Med 166:405–410

    PubMed  Google Scholar 

  76. Leroi C, Balestre E, Messou E, Minga A, Sawadogo A, Drabo J, Maiga M, Zannou M, Seydi M, Dabis F, Jaquet A, IeDEA West Africa collaboration (2017) Incidence of severe neutropenia in HIV-infected people starting antiretroviral therapy in West Africa. PLoS One 12:e0170753

    Article  PubMed  PubMed Central  Google Scholar 

  77. Rezvani K, Flanagan AM, Sarma U, Constantinovici N, Bain BJ (2001) Investigation of ethnic neutropenia by assessment of bone marrow colony-forming cells. Acta Haematol 105:32–37

    Article  CAS  PubMed  Google Scholar 

  78. Reich D, Nalls MA, Kao WH, Akylbekova EL, Tandon A, Patterson N, Mullikin J, Hsueh WC, Cheng CY, Coresh J, Boerwinkle E, Li M, Waliszewska A, Neubauer J, Li R, Leak TS, Ekunwe L, Files JC, Hardy CL, Zmuda JM, Taylor HA, Ziv E, Harris TB, Wilson JG (2009) Reduced neutrophil count in people of African descent is due to a regulatory variant in the Duffy antigen receptor for chemokines gene. PLoS Genet 5:e1000360

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Kourtis AP, Hudgens MG, Kayira D, BAN Study Team (2012) Neutrophil count in African mothers and newborns and HIV transmission risk. N Engl J Med 367:2260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Jan MS, Huang YH, Shieh B, Teng RH, Yan YP, Lee YT, Liao KK, Li C (2006) CC chemokines induce neutrophils to chemotaxis, degranulation, and alpha-defensin release. J Acquir Immune Defic Syndr 41:6–16

    Article  CAS  PubMed  Google Scholar 

  81. Gabrilovich DI, Vassilev V, Nosikov VV, Serebrovskaya LV, Ivanova LA, Pokrovsky VV (1993) Clinical significance of HIV DNA in polymorphonuclear neutrophils from patients with HIV infection. J Acquir Immune Defic Syndr 6:587–591

    CAS  PubMed  Google Scholar 

  82. Biswas P, Mantelli B, Sica A, Malnati M, Panzeri C, Saccani A, Hasson H, Vecchi A, Saniabadi A, Lusso P, Lazzarin A, Beretta A (2003) Expression of CD4 on human peripheral blood neutrophils. Blood 101:4452–4456

    Article  CAS  PubMed  Google Scholar 

  83. Jouve M, Sol-Foulon N, Watson S, Schwartz O, Benaroch P (2007) HIV-1 buds and accumulates in “nonacidic” endosomes of macrophages. Cell Host Microbe 2:85–95

    Article  CAS  PubMed  Google Scholar 

  84. Mazzolini J, Herit F, Bouchet J, Benmerah A, Benichou S, Niedergang F (2010) Inhibition of phagocytosis in HIV-1-infected macrophages relies on Nef-dependent alteration of focal delivery of recycling compartments. Blood 115:4226–4236

    Article  CAS  PubMed  Google Scholar 

  85. Pitrak DL, Tsai HC, Mullane KM, Sutton SH, Stevens P (1996) Accelerated neutrophil apoptosis in the acquired immunodeficiency syndrome. J Clin Invest 98:2714–2719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Baldelli F, Preziosi R, Francisci D, Tascini C, Bistoni F, Nicoletti I (2004) Programmed granulocyte neutrophil death in patients at different stages of HIV infection. AIDS 14:1067–1069

    Article  Google Scholar 

  87. Salmen S, Terán G, Borges L, Goncalves L, Albarrán B, Urdaneta H, Montes H, Berrueta L (2004) Increased Fas-mediated apoptosis in polymorphonuclear cells from HIV-infected patients. Clin Exp Immunol 137:166–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Salmen S, Montes H, Soyano A, Hernández D, Berrueta L (2007) Mechanisms of neutrophil death in human immunodeficiency virus-infected patients: role of reactive oxygen species, caspases and map kinase pathways. Clin Exp Immunol 150:539–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Elbim C, Monceaux V, François S, Hurtrel B, Gougerot-Pocidalo MA, Estaquier J (2009) Increased neutrophil apoptosis in chronically SIV-infected macaques. Retrovirology 6:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Casulli S, Elbim C (2014) Interactions between human immunodeficiency virus type1 and polymorphonuclear neutrophils. J Innate Immun 6:13–20

    Article  CAS  PubMed  Google Scholar 

  91. Hadad N, Levy R, Schlaeffer F, Riesenberg K (2007) Direct effect of human immunodeficiency virus protease inhibitors on neutrophil function and apoptosis via calpain inhibition. Clin Vaccine Immunol 14:1515–1521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Busch M, Beckstead J, Gantz D, Vyas G (1986) Detection of human immunodeficiency virus infection of myeloid precursors in bone marrow samples from AIDS patients (abstract). Blood 68:122a

    Google Scholar 

  93. Zauli G, Furlini G, Vitale M, Re MC, Gibellini D, Zamai L, Visani G, Borgatti P, Capitani S, La Placa M (1994) A subset of human CD34+ hematopoietic progenitors express low levels of CD4, the high-affinity receptor for human immunodeficiency virus-type 1. Blood 84:1896–1905

    CAS  PubMed  Google Scholar 

  94. Aiuti A, Turchetto L, Cota M, Cipponi A, Brambilla A, Arcelloni C, Paroni R, Vicenzi E, Bordignon C, Poli G (1999) Human CD34(+) cells express CXCR4 and its ligand stromal cell-derived factor-1. Implications for infection by T-cell tropic human immunodeficiency virus. Blood 94:62–73

    CAS  PubMed  Google Scholar 

  95. Lee B, Ratajczak J, Doms RW, Gewirtz AM, Ratajczak MZ (1999) Coreceptor/chemokine receptor expression on human hematopoietic cells: biological implications for human immunodeficiency virus-type 1 infection. Blood 93:1145–1156

    CAS  PubMed  Google Scholar 

  96. Deichmann M, Kronenwett R, Haas R (1997) Expression of the human immunodeficiency virus type-1 coreceptors CXCR-4 (fusin, LESTR) and CKR-5 in CD34+ hematopoietic progenitor cells. Blood 89:3522–3528

    CAS  PubMed  Google Scholar 

  97. Redd AD, Avalos A, Essex M (2007) Infection of hematopoietic progenitor cells by HIV-1 subtype C, and its association with anemia in southern Africa. Blood 110:3143–3149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Alexaki A, Wigdahl B (2008) HIV-1 infection of bone marrow hematopoietic progenitor cells and their role in trafficking and viral dissemination. PLoS Pathog 4:e1000215

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Carter CC, Onafuwa-Nuga A, McNamara LA, Riddell J 4th, Bixby D, Savona MR, Collins KL (2010) HIV-1 infects multipotent progenitor cells causing cell death and establishing latent cellular reservoirs. Nat Med 16:446–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Zauli G, Vitale M, Gibellini D, Capitani S (1996) Inhibition of purified CD34+ hematopoietic progenitor cells by human immunodeficiency virus 1 or gp120 mediated by endogenous transforming growth factor beta 1. J Exp Med 183:99–108

    Article  CAS  PubMed  Google Scholar 

  101. Banda NK, Tomczak JA, Shpall EJ, Sipple J, Akkina RK, Steimer KS, Hami L, Curiel TJ, Singer Harrison G (1997) HIV-gp120 induced cell death in hematopoietic progenitor CD34+ cells. Apoptosis 2:61–68

    Article  CAS  PubMed  Google Scholar 

  102. Calenda V, Graber P, Delamarter JF, Chermann JC (1994) Involvement of HIV nef protein in abnormal hematopoiesis in AIDS: in vitro study on bone marrow progenitor cells. Eur J Haematol 52:103–107

    Article  CAS  PubMed  Google Scholar 

  103. Prost S, Le Dantec M, Augé S, Le Grand R, Derdouch S, Auregan G, Déglon N, Relouzat F, Aubertin AM, Maillere B, Dusanter-Fourt I, Kirszenbaum M (2008) Human and simian immunodeficiency viruses deregulate early hematopoiesis through a Nef/PPARgamma/STAT5 signaling pathway in macaques. J Clin Invest 118:1765–7175

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Prakash O, Zhang P, Xie M, Ali M, Zhou P, Coleman R, Stoltz DA, Bagby GJ, Shellito JE, Nelson S (1998) The human immunodeficiency virus type I Tat protein potentiates ethanol-induced neutrophil functional impairment in transgenic mice. Alcohol Clin Exp Res 22:2043–2049

    CAS  PubMed  Google Scholar 

  105. Gibellini D, Clò A, Morini S, Miserocchi A, Ponti C, Re MC (2013) Effects of human immunodeficiency virus on the erythrocyte and megakaryocyte lineages. World J Virol 2:91–101

    Article  PubMed  PubMed Central  Google Scholar 

  106. Isgrò A, Aiuti A, Mezzaroma I, Addesso M, Riva E, Giovannetti A, Mazzetta F, Alario C, Mazzone A, Ruco L, Aiuti F (2002) Improvement of interleukin 2 production, clonogenic capability and restoration of stromal cell function in human immunodeficiency virus-type-1 patients after highly active antiretroviral therapy. Br J Haematol 118:864–874

    Article  PubMed  Google Scholar 

  107. Isgrò A, Aiuti A, Leti W, Gramiccioni C, Esposito A, Mezzaroma I, Aiuti F (2005) Immunodysregulation of HIV disease at bone marrow level. Autoimmun Rev 4:486–490

    Article  PubMed  Google Scholar 

  108. Isgrò A, Leti W, De Santis W, Marziali M, Esposito A, Fimiani C, Luzi G, Pinti M, Cossarizza A, Aiuti F, Mezzaroma I (2008) Altered clonogenic capability and stromal cell function characterize bone marrow of HIV-infected subjects with low CD4+ T cell counts despite viral suppression during HAART. Clin Infect Dis 46:1902–1910

    Article  PubMed  Google Scholar 

  109. Gill V, Shattock RJ, Freeman AR, Robinson G, Griffin GE, Gordon-Smith EC, Gibson FM (1996) Macrophages are the major target cell for HIV infection in long-term marrow culture and demonstrate dual susceptibility to lymphocytotropic and monocytotropic strains of HIV-1. Br J Haematol 93:30–37

    Article  CAS  PubMed  Google Scholar 

  110. Canque B, Marandin A, Rosenzwajg M, Louache F, Vainchenker W, Gluckman JC (1995) Susceptibility of human bone marrow stromal cells to human immunodeficiency virus (HIV). Virology 208:779–783

    Article  CAS  PubMed  Google Scholar 

  111. Chelucci C, Federico M, Guerriero R, Mattia G, Casella I, Pelosi E, Testa U, Mariani G, Hassan HJ, Peschle C (1998) Productive human immunodeficiency virus-1 infection of purified megakaryocytic progenitors/precursors and maturing megakaryocytes. Blood 91:1225–1234

    CAS  PubMed  Google Scholar 

  112. Jaresko GS (1999) Etiology of neutropenia in HIV-infected patients. Am J Health Syst Pharm 5:S5–S8

    Google Scholar 

  113. Volberding PA, Baker KR, Levine AM (2003) Human immunodeficiency virus hematology. Hematol Am Soc Hematol Educ Program 2003:294–313

    Google Scholar 

  114. Jacobs JL, Gold JW, Murray HW, Roberts RB, Armstrong D (1985) Salmonella infections in patients with the acquired immunodeficiency syndrome. Ann Intern Med 102:186–188

    Article  CAS  PubMed  Google Scholar 

  115. Puthucheary SD, Ng KP, Hafeez A, Raja NS, Hassan HH (2004) Salmonellosis in persons infected with human immunodeficiency virus: a report of seven cases from Malaysia. Southeast Asian J Trop Med Public Health 35:361–365

    CAS  PubMed  Google Scholar 

  116. Casado JL, Navas E, Frutos B, Moreno A, Martín P, Hermida JM, Guerrero A (1997) Salmonella lung involvement in patients with HIV infection. Chest 112:1197–1201

    Article  CAS  PubMed  Google Scholar 

  117. Wain J, Pham VB, Ha V, Nguyen NM, To SD, Walsh AL, Parry CM, Hasserjian RP, HoHo VA, Tran TH, Farrar J, White NJ, Day NP (2001) Quantitation of bacteria in bone marrow from patients with typhoid fever: relationship between counts and clinical features. J Clin Microbiol 39:1571–1576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Hakawi AM, Alrajhi AA (2006) Tuberculosis of the bone marrow: clinico-pathological study of 22 cases from Saudi Arabia. Int J Tuberc Lung Dis 10:1041–1044

    CAS  PubMed  Google Scholar 

  119. Khandekar MM, Deshmukh SD, Holla VV, Rane SR, Kakrani AL, Sangale SA, Habbu AA, Pandit DP, Bhore AV, Sastry J, Phadke MA, Bollinger RC (2005) Profile of bone marrow examination in HIV/AIDS patients to detect opportunistic infections, especially tuberculosis. Indian J Pathol Microbiol 48:7–12

    CAS  PubMed  Google Scholar 

  120. Getahun H, Gunneberg C, Granich R, Nunn P (2010) HIV infection-associated tuberculosis: The epidemiology and the response. Clin Infect Dis 50:S201–S207

    Article  PubMed  Google Scholar 

  121. Burke M, Yust I, Katlama C, Vardinon N, Clumeck N, Pinching AJ, Ledergerber B, Gatell JM, Chiesi A, Barton SE, Lundgren JD, Pedersen C (1997) Cytomegalovirus retinitis in patients with AIDS in Europe. AIDS in Europe Study Group. Eur J Clin Microbiol Infect Dis 16:876–882

    Article  CAS  PubMed  Google Scholar 

  122. Sing GK, Ruscetti FW (1995) The role of human cytomegalovirus in haematological diseases. Baillieres Clin Haematol 8:149–163

    Article  CAS  PubMed  Google Scholar 

  123. Pantanowitz L, Omar T, Sonnendecker H, Karstaedt AS (2000) Bone marrow cryptococcal infection in the acquired immunodeficiency syndrome. J Infect 41:92–94

    Article  CAS  PubMed  Google Scholar 

  124. Calore EE, Tanaka PY, Perez NM, de Almeida LV (2004) Bone marrow pathology in AIDS. Pathol Res Pract 200:591–597

    Article  PubMed  Google Scholar 

  125. Folkvord JM, McCarter MD, Ryder J, Meditz AL, Forster JE, Connick E (2006) Alpha-defensins 1, 2, and 3 are expressed by granulocytes in lymphoid tissues of HIV-1-seropositive and seronegative individuals. J Acquir Immune Defic Syndr 42:529–536

    Article  CAS  PubMed  Google Scholar 

  126. Allers K, Fehr M, Conrad K, Epple HJ, Schürmann D, Geelhaar-Karsch A, Schinnerling K, Moos V, Schneider T (2014) Macrophages accumulate in the gut mucosa of untreated HIV-infected patients. J Infect Dis 209:739–748

    Article  CAS  PubMed  Google Scholar 

  127. Aseffa A, Dietrich MA, Shannon EJ (1997) Effect of thalidomide on apoptosis of lymphocytes and neutrophils. Immunopharmacol Immunotoxicol 19:313–326

    Article  CAS  PubMed  Google Scholar 

  128. Israel DS, Plaisance KI (1991) Neutropenia in patients infected with human immunodeficiency virus. Clin Pharm 10:268–279

    CAS  PubMed  Google Scholar 

  129. Toure S, Gabillard D, Inwoley A, Seyler C, Gourvellec G, Anglaret X (2006) Incidence of neutropenia in HIV-infected African adults receiving co-trimoxazole prophylaxis: a 6-year cohort study in Abidjan, Côte d’Ivoire. Trans R Soc Trop Med Hyg 100:785–790

    Article  CAS  PubMed  Google Scholar 

  130. Dryden-Peterson S, Jayeoba O, Hughes MD, Jibril H, McIntosh K, Modise TA, Asmelash A, Powis KM, Essex M, Shapiro RL, Lockman S (2013) Cotrimoxazole prophylaxis and risk of severe anemia or severe neutropenia in HAART-exposed. HIV-uninfected infants. PLoS One 8:e74171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Smith C, Forster JE, Levin MJ, Davies J, Pappas J, Kinzie K, Barr E, Paul S, McFarland EJ, Weinberg A (2015) Serious adverse events are uncommon with combination neonatal antiretroviral prophylaxis: a retrospective case review. PLoS One 10:e0127062

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. Richman DD, Fischl MA, Grieco MH, Gottlieb MS, Volberding PA, Laskin OL, Leedom JM, Groopman JE, Mildvan D, Hirsch MS et al (1987) The toxicity of azidothymidine (AZT) in the treatment of patients with AIDS and AIDS-related complex. A double-blind, placebo-controlled trial. N Engl J Med 317:192–197

    Article  CAS  PubMed  Google Scholar 

  133. Moh R, Danel C, Sorho S, Sauvageot D, Anzian A, Minga A, Gomis OB, Konga C, Inwoley A, Gabillard D, Bissagnene E, Salamon R, Anglaret X (2005) Haematological changes in adults receiving a zidovudine-containing HAART regimen in combination with cotrimoxazole in Côte d’Ivoire. Antivir Ther 10:615–624

    CAS  PubMed  Google Scholar 

  134. Moyle G, Sawyer W, Law M, Amin J, Hill A (2004) Changes in hematologic parameters and efficacy of thymidine analogue-based, highly active antiretroviral therapy: a meta-analysis of six prospective, randomized, comparative studies. Clin Ther 26:92–97

    Article  CAS  PubMed  Google Scholar 

  135. Bower M, McCall-Peat N, Ryan N, Davies L, Young AM, Gupta S, Nelson M, Gazzard B, Stebbing J (2004) Protease inhibitors potentiate chemotherapy-induced neutropenia. Blood 104:2943–2946

    Article  CAS  PubMed  Google Scholar 

  136. Zon LI, Arkin C, Groopman JE (1987) Haematologic manifestations of the human immune deficiency virus (HIV). Br J Haematol 66:251

    Article  CAS  PubMed  Google Scholar 

  137. Kuritzkes DR, Parenti D, Ward DJ, Rachlis A, Wong RJ, Mallon KP, Rich WJ, Jacobson MA (1998) Filgrastim prevents severe neutropenia and reduces infective morbidity in patients with advanced HIV infection: results of a randomized, multicenter, controlled trial. G-CSF 930101 Study Group. AIDS 12:65–74

    Article  CAS  PubMed  Google Scholar 

  138. Frumkin LR (1997) Role of granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor in the treatment of patients with HIV infection. Curr Opin Hematol 4:200–206

    Article  CAS  PubMed  Google Scholar 

  139. Hermans P, Rozenbaum W, Jou A, Castelli F, Borleffs J, Gray S, Ward N, Gori A, De Bona A, Ferré C, Loncà M, Lang JM, Ammassari A, Clumeck N (1996) Filgrastim to treat neutropenia and support myelosuppressive medication dosing in HIV infection. G-CSF 92105 Study Group. AIDS 10:1627–1633

    Article  CAS  PubMed  Google Scholar 

  140. Keiser P, Rademacher S, Smith JW, Skiest D, Vadde V (1998) Granulocyte colony-stimulating factor use is associated with decreased bacteremia and increased survival in neutropenic HIV-infected patients. Am J Med 104:48–55

    Article  CAS  PubMed  Google Scholar 

  141. Nielsen SD, Sørensen TU, Aladdin H, Ersbøll AK, Mathiesen L, Ullum H, Gerstoft J, Nielsen JO, Pedersen BK (2000) The effect of long-term treatment with granulocyte colony-stimulating factor on hematopoiesis in HIV-infected individuals. Scand J Immunol 52:298–303

    Article  CAS  PubMed  Google Scholar 

  142. Barbaro G, Di Lorenzo G, Grisorio B, Soldini M, Barbarini G (1997) Effect of recombinant human granulocyte-macrophage colony-stimulating factor on HIV-related leukopenia: a randomized, controlled clinical study. AIDS 11:1453–1461

    Article  CAS  PubMed  Google Scholar 

  143. Angel JB, High K, Rhame F, Brand D, Whitmore JB, Agosti JM, Gilbert MJ, Deresinski S (2000) Phase III study of granulocyte-macrophage colony-stimulating factor in advanced HIV disease: effect on infections, CD4 cell counts and HIV suppression. Leukine/HIV Study Group. AIDS 14:387–395

    Article  CAS  PubMed  Google Scholar 

  144. Mastroianni CM, d’Ettorre G, Forcina G, Lichtner M, Mengoni F, D’Agostino C, Corpolongo A, Massetti AP, Vullo V (2000) Interleukin-15 enhances neutrophil functional activity in patients with human immunodeficiency virus infection. Blood 96:1979–1984

    CAS  PubMed  Google Scholar 

  145. Swaminathan S, Qiu J, Rupert AW, Hu Z, Higgins J, Dewar RL, Stevens R, Rehm CA, Metcalf JA, Sherman BT, Baseler MW, Lane HC, Imamichi T (2016) Interleukin-15 (IL-15) strongly correlates with increasing HIV-1 viremia and markers of inflammation. PLoS One 11:e0167091

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  146. Bowers NL, Helton ES, Huijbregts RP, Goepfert PA, Heath SL, Hel Z (2014) Immune suppression by neutrophils in HIV-1 infection: role of PD-L1/PD-1 pathway. PLoS Pathog 10:e1003993

    Article  PubMed  PubMed Central  Google Scholar 

  147. Kubes P, Heit B, van Marle G, Johnston JB, Knight D, Khan A, Power C (2003) In vivo impairment of neutrophil recruitment during lentivirus infection. J Immunol 171:4801–4808

    Article  CAS  PubMed  Google Scholar 

  148. Heit B, Jones G, Knight D, Antony JM, Gill MJ, Brown C, Power C, Kubes P (2006) HIV and other lentiviral infections cause defects in neutrophil chemotaxis, recruitment, and cell structure: immunorestorative effects of granulocyte-macrophage colony-stimulating factor. J Immunol 177:6405–6414

    Article  CAS  PubMed  Google Scholar 

  149. Debaisieux S, Lachambre S, Gross A, Mettling C, Besteiro S, Yezid H, Henaff D, Chopard C, Mesnard JM, Beaumelle B (2015) HIV-1 Tat inhibits phagocytosis by preventing the recruitment of Cdc42 to the phagocytic cup. Nat Commun 6:6211

    Article  PubMed  CAS  Google Scholar 

  150. Michailidis C, Giannopoulos G, Vigklis V, Armenis K, Tsakris A, Gargalianos P (2012) Impaired phagocytosis among patients infected by the human immunodeficiency virus: implication for a role of highly active anti-retroviral therapy. Clin Exp Immunol 167:499–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Roilides E, Mertins S, Eddy J, Walsh TJ, Pizzo PA, Rubin M (1990) Impairment of neutrophil chemotactic and bactericidal function in children infected with human immunodeficiency virus type 1 and partial reversal after in vitro exposure to granulocyte-macrophage colony-stimulating factor. J Pediatr 117:531–540

    Article  CAS  PubMed  Google Scholar 

  152. Roilides E, Walsh TJ, Pizzo PA, Rubin M (1991) Granulocyte colony-stimulating factor enhances the phagocytic and bactericidal activity of normal and defective human neutrophils. J Infect Dis 163:579–583

    Article  CAS  PubMed  Google Scholar 

  153. Schaumann R, Krosing J, Shah PM (1998) Phagocytosis of Escherichia coli and Staphylococcus aureus by neutrophils of human immunodeficiency virus-infected patients. Eur J Med Res 3:546–548

    CAS  PubMed  Google Scholar 

  154. Roilides E, Holmes A, Blake C, Pizzo PA, Walsh TJ (1993) Impairment of neutrophil antifungal activity against hyphae of Aspergillus fumigatus in children infected with human immunodeficiency virus. J Infect Dis 167:905–911

    Article  CAS  PubMed  Google Scholar 

  155. Coffey MJ, Phare SM, George S, Peters-Golden M, Kazanjian PH (1998) Granulocyte colony-stimulating factor administration to HIV-infected subjects augments reduced leukotriene synthesis and anticryptococcal activity in neutrophils. J Clin Invest 102:663–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Moore DA, Henderson D, Gazzard BG (1998) Neutrophil adhesion molecules in HIV disease. Clin Exp Immunol 114:73–77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Meddows-Taylor S, Kuhn L, Meyers TM, Tiemessen CT (2001) Altered expression of L-selectin (CD62L) on polymorphonuclear neutrophils of children vertically infected with human immunodeficiency virus type 1. J Clin Immunol 21:286–292

    Article  CAS  PubMed  Google Scholar 

  158. Meddows-Taylor S, Martin DJ, Tiemessen CT (1999) Impaired interleukin-8-induced degranulation of polymorphonuclear neutrophils from human immunodeficiency virus type 1-infected individuals. Clin Diagn Lab Immunol 6:345–351

    CAS  PubMed  PubMed Central  Google Scholar 

  159. Vecchiarelli A, Monari C, Palazzetti B, Bistoni F, Casadevall A (2000) Dysregulation in IL-12 secretion by neutrophils from HIV-infected patients. Clin Exp Immunol 121:311–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Meddows-Taylor S, Kuhn L, Meyers TM, Sherman G, Tiemessen CT (2001) Defective neutrophil degranulation induced by interleukin-8 and complement 5a and down-regulation of associated receptors in children vertically infected with human immunodeficiency virus type 1. Clin Diagn Lab Immunol 8:21–30

    CAS  PubMed  PubMed Central  Google Scholar 

  161. Schwartz R, Lu Y, Villines D, Sroussi HY (2010) Effect of human immunodeficiency virus infection on S100A8/A9 inhibition of peripheral neutrophils oxidative metabolism. Biomed Pharmacother 64:572–575

    Article  CAS  PubMed  Google Scholar 

  162. Boros P, Gardos E, Bekesi GJ, Unkeless JC (1990) Change in expression of Fc gamma RIII (CD16) on neutrophils from human immunodeficiency virus-infected individuals. Clin Immunol Immunopathol 54:281–289

    Article  CAS  PubMed  Google Scholar 

  163. Meddows-Taylor S, Martin DJ, Tiemessen CT (1997) Altered expression of Fc gamma RIII (CD16) on polymorphonuclear neutrophils from individuals with human immunodeficiency virus type 1 disease and pulmonary tuberculosis. Clin Diagn Lab Immunol 4:789–791

    CAS  PubMed  PubMed Central  Google Scholar 

  164. Muñoz JF, Salmen S, Berrueta LR, Carlos MP, Cova JA, Donis JH, Hernández MR, Torres JV (1999) Effect of human immunodeficiency virus type 1 on intracellular activation and superoxide production by neutrophils. J Infect Dis 180:206–210

    Article  PubMed  Google Scholar 

  165. Chen TP, Roberts RL, Wu KG, Ank BJ, Stiehm ER (1993) Decreased superoxide anion and hydrogen peroxide production by neutrophils and monocytes in human immunodeficiency virus-infected children and adults. Pediatr Res 34:544–550

    Article  CAS  PubMed  Google Scholar 

  166. Olinger GG, Saifuddin M, Spear GT (2000) CD4-Negative cells bind human immunodeficiency virus type 1 and efficiently transfer virus to T cells. J Virol 74:8550–8557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Gabali AM, Anzinger JJ, Spear GT, Thomas LL (2004) Activation by inflammatory stimuli increases neutrophil binding of human immunodeficiencyvirus type 1 and subsequent infection of lymphocytes. J Virol 78:10833–10836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Yoshida T, Jones VC, Kobayashi M, Li XD, Pollard RB, Suzuki F (2007) Acceleration of R5 HIV replication by polymorphonuclear neutrophils in cultures of macrophages. Immunol Cell Biol 85:215–219

    CAS  PubMed  Google Scholar 

  169. Yoshida T, Kobayashi M, Li XD, Pollard RB, Suzuki F (2009) Inhibitory effect of glycyrrhizin on the neutrophil-dependent increase of R5 HIV replication in cultures of macrophages. Immunol Cell Biol 87:554–558

    Article  CAS  PubMed  Google Scholar 

  170. Fu J, Sha BE, Thomas LL (2011) HIV-1-infected peripheral blood mononuclear cells enhance neutrophil survival and HLA-DR expression via increased production of GM-CSF: implications for HIV-1 infection. J Acquir Immune Defic Syndr 56:16–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Prodger JL, Gray RH, Shannon B, Shahabi K, Kong X, Grabowski K, Kigozi G, Nalugoda F, Serwadda D, Wawer MJ, Reynolds SJ, Liu CM, Tobian AA, Kaul R (2016) Chemokine levels in the penile coronal sulcus correlate with HIV-1 acquisition and are reduced by male circumcision in Rakai, Uganda. PLoS Pathog 12:e1006025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  172. Rajasuriar R, Khoury G, Kamarulzaman A, French MA, Cameron PU, Lewin SR (2013) Persistent immune activation in chronic HIV infection: do any interventions work? AIDS 27:1199–1208

    Article  PubMed  PubMed Central  Google Scholar 

  173. D’Agostino C, Lichtner M, Mastroianni CM, Ceccarelli G, Iannetta M, Antonucci S, Vullo V, Massetti AP (2009) In vivo release of alpha-defensins in plasma, neutrophils and CD8 T-lymphocytes of patients with HIV infection. Curr HIV Res 7:650–655

    Article  PubMed  Google Scholar 

  174. Day CL, Kaufmann DE, Kiepiela P, Brown JA, Moodley ES, Reddy S, Mackey EW, Miller JD, Leslie AJ, DePierres C, Mncube Z, Duraiswamy J, Zhu B, Eichbaum Q, Altfeld M, Wherry EJ, Coovadia HM, Goulder PJ, Klenerman P, Ahmed R, Freeman GJ, Walker BD (2006) PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443:350–354

    Article  CAS  PubMed  Google Scholar 

  175. Rosignoli G, Cranage A, Burton C, Nelson M, Steel A, Gazzard B, Gotch F, Imami N (2007) Expression of PD-L1, a marker of disease status, is not reduced by HAART in aviraemic patients. AIDS 21:1379–1381

    Article  CAS  PubMed  Google Scholar 

  176. Velu V, Titanji K, Zhu B, Husain S, Pladevega A, Lai L, Vanderford TH, Chennareddi L, Silvestri G, Freeman GJ, Ahmed R, Amara RR (2009) Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 458:206–210

    Article  CAS  PubMed  Google Scholar 

  177. Dyavar Shetty R, Velu V, Titanji K, Bosinger SE, Freeman GJ, Silvestri G, Amara RR (2012) PD-1 blockade during chronic SIV infection reduces hyperimmune activation and microbial translocation in rhesus macaques. J Clin Invest 122:1712–1716

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  178. Hunt PW, Brenchley J, Sinclair E, McCune JM, Roland M, Page-Shafer K, Hsue P, Emu B, Krone M, Lampiris H, Douek D, Martin JN, Deeks SG (2008) Relationship between T cell activation and CD4+ T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis 197:126–133

    Article  PubMed  PubMed Central  Google Scholar 

  179. Campillo-Gimenez L, Casulli S, Dudoit Y, Seang S, Carcelain G, Lambert-Niclot S, Appay V, Autran B, Tubiana R, Elbim C (2014) Neutrophils in antiretroviral therapy-controlled HIV demonstrate hyperactivation associated with a specific IL-17/IL-22 environment. J Allergy Clin Immunol 134:1142–1152

    Article  CAS  PubMed  Google Scholar 

  180. Torre D, Gennero L, Baccino F, Speranza F, Biondi G, Pugliese A (2002) Impaired macrophage phagocytosis of apoptotic neutrophils in patients with human immunodeficiency virus type 1 infection. Clin Vaccine Immunol 9:983

    Article  Google Scholar 

  181. Morquin D, Tuaillon E, Makinson A, Bendriss S, Le Moing V, Reynes J (2016) Impact of T cell activation, HIV replication and hepatitis C virus infection on neutrophil CD64 expression. Cytom B Clin Cytom. doi:10.1002/cyto.b.21385

    Google Scholar 

  182. Mitsumoto-Kaseida F, Murata M, Ura K, Takayama K, Hiramine S, Shimizu M, Toyoda K, Ogawa E, Furusyo N (2017) The expression level of neutrophil CD64 is a useful marker of systemic inflammation associated with HIV infection. AIDS Res Hum Retrovir 33:147–156

    Article  CAS  PubMed  Google Scholar 

  183. Giraldo DM, Hernandez JC, Velilla P, Urcuqui-Inchima S (2016) HIV-1-neutrophil interactions trigger neutrophil activation and Toll-like receptor expression. Immunol Res 64:93–103

    Article  CAS  PubMed  Google Scholar 

  184. Giraldo DM, Hernandez JC, Urcuqui-Inchima S (2016) HIV-1-derived single-stranded RNA acts as activator of human neutrophils. Immunol Res 64:1185–1194

    Article  CAS  PubMed  Google Scholar 

  185. Salmen S, Colmenares M, Peterson DL, Reyes E, Rosales JD, Berrueta L (2010) HIV-1 Nef associates with p22-phox, a component of the NADPH oxidase protein complex. Cell Immunol 263:166–171

    Article  CAS  PubMed  Google Scholar 

  186. Kavoosi G, Ardestani SK, Kariminia A (2009) The involvement of TLR2 in cytokine and reactive oxygen species (ROS) production by PBMCs in response to Leishmania major phosphoglycans (PGs). Parasitology 136:1193–1199

    Article  CAS  PubMed  Google Scholar 

  187. Prince LR, Whyte MK, Sabroe I, Parker LC (2011) The role of TLRs in neutrophil activation. Curr Opin Pharmacol 11:397–403

    Article  CAS  PubMed  Google Scholar 

  188. Jenne CN, Kubes P (2012) NETs tangle with HIV. Cell Host Microbe 12:5–7

    Article  CAS  PubMed  Google Scholar 

  189. Hooper LV (2015) Epithelial cell contributions to intestinal immunity. Adv Immunol 126:129–172

    Article  PubMed  Google Scholar 

  190. Fournier BM, Parkos CA (2012) The role of neutrophils during intestinal inflammation. Mucosal Immunol 5:354–366

    Article  CAS  PubMed  Google Scholar 

  191. Colgan SP (2015) Neutrophils and inflammatory resolution in the mucosa. Semin Immunol 27:177–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Zindl CL, Lai JF, Lee YK, Maynard CL, Harbour SN, Ouyang W, Chaplin DD, Weaver CT (2013) IL-22-producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. Proc Natl Acad Sci USA 110:12768–12773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Hooper LV, Macpherson AJ (2010) Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10:159–169

    Article  CAS  PubMed  Google Scholar 

  194. Peterson LW, Artis D (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14:141–153

    Article  CAS  PubMed  Google Scholar 

  195. Obata Y, Takahashi D, Ebisawa M, Kakiguchi K, Yonemura S, Jinnohara T, Kanaya T, Fujimura Y, Ohmae M, Hase K, Ohno H (2012) Epithelial cell-intrinsic Notch signaling plays an essential role in the maintenance of gut immune homeostasis. J Immunol 188:2427–2436

    Article  CAS  PubMed  Google Scholar 

  196. Pastorelli L, De Salvo C, Mercado JR, Vecchi M, Pizarro TT (2013) Central role of the gut epithelial barrier in the pathogenesis of chronic intestinal inflammation: lessons learned from animal models and human genetics. Front Immunol 4:280

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  197. Hoffmanová I, Sánchez D, Hábová V, Anděl M, Tučková L, Tlaskalová-Hogenová H (2015) Serological markers of enterocyte damage and apoptosis in patients with celiac disease, autoimmune diabetes mellitus and diabetes mellitus type 2. Physiol Res 64:537–546

    PubMed  Google Scholar 

  198. Cenit MC, Olivares M, Codoñer-Franch P, Sanz Y (2015) Intestinal microbiota and celiac disease: cause, consequence or co-evolution? Nutrients 7:6900–6923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Timmons T, Shen C, Aldrovandi G, Rollie A, Gupta SK, Stein JH, Dubé MP (2014) Microbial translocation and metabolic and body composition measures in treated and untreated HIV infection. AIDS Res Hum Retrovir 30:272–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Louis P, Hold GL, Flint HJ (2014) The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12:661–672

    Article  CAS  PubMed  Google Scholar 

  201. Peterson CT, Sharma V, Elmén L, Peterson SN (2015) Immune homeostasis, dysbiosis and therapeutic modulation of the gut microbiota. Clin Exp Immunol 179:363–377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Tojo R, Suárez A, Clemente MG, de los Reyes-Gavilán CG, Margolles A, Gueimonde M, Ruas-Madiedo P (2014) Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis. Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis. World J Gastroenterol 20:15163–15176

    Article  PubMed  PubMed Central  Google Scholar 

  203. Rai R, Saraswat VA, Dhiman RK (2015) Gut microbiota: its role in hepatic encephalopathy. J Clin Exp Hepatol 5:S29–S36

    Article  PubMed  Google Scholar 

  204. Festi D, Schiumerini R, Eusebi LH, Marasco G, Taddia M, Colecchia A (2014) Gut microbiota and metabolic syndrome. World J Gastroenterol 20:16079–16094

    Article  PubMed  PubMed Central  Google Scholar 

  205. Bjerknes M, Cheng H (2005) Gastrointestinal stem cells. II. Intestinal stem cells. Am J Physiol Gastrointest Liver Physiol 289:G381–G387

    Article  CAS  PubMed  Google Scholar 

  206. Crosnier C, Stamataki D, Lewis J (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 7:349–359

    Article  CAS  PubMed  Google Scholar 

  207. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:262–265

    Article  CAS  PubMed  Google Scholar 

  208. Barker N (2014) Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat Rev Mol Cell Biol 15:19–33

    Article  CAS  PubMed  Google Scholar 

  209. Lee SH (2015) Intestinal permeability regulation by tight junction: implication on inflammatory bowel diseases. Intest Res 13:11–18

    Article  PubMed  PubMed Central  Google Scholar 

  210. Mowat A, Viney J (1997) The anatomical basis of intestinal immunity. Immunol Rev 156:145–166

    Article  CAS  PubMed  Google Scholar 

  211. Carter LW (1994) Bacterial translocation: nursing implications in the care of patients with neutropenia. Oncol Nurs Forum 21:857–865

    CAS  PubMed  Google Scholar 

  212. Koh AY, Priebe GP, Pier GB (2005) Virulence of Pseudomonas aeruginosa in a murine model of gastrointestinal colonization and dissemination in neutropenia. Infect Immun 73:2262–2272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Koh AY, Köhler JR, Coggshall KT, Van Rooijen N, Pier GB (2008) Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog 4:e35

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  214. Faber J, van Limpt K, Kegler D, Luiking Y, Garssen J, van Helvoort A, Vos AP, Knol J (2011) Bacterial translocation is reduced by a specific nutritional combination in mice with chemotherapy-induced neutropenia. J Nutr 141:1292–1298

    Article  CAS  PubMed  Google Scholar 

  215. Green SI, Ajami NJ, Ma L, Poole NM, Price RE, Petrosino JF, Maresso AW (2015) Murine model of chemotherapy-induced extraintestinal pathogenic Escherichia coli translocation. Infect Immun 83:3243–3256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Colgan SP, Ehrentraut SF, Glover LE, Kominsky DJ, Campbell EL (2013) Contributions of neutrophils to resolution of mucosal inflammation. Immunol Res 55:75–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  217. Kolls JK, McCray PB Jr, Chan YR (2008) Cytokine-mediated regulation of antimicrobial proteins. Nat Rev Immunol 8:829–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Valeri M, Raffatellu M (2016) Cytokines IL-17 and IL-22 in the host response to infection. Pathog Dis 74. doi:10.1093/femspd/ftw111

  219. Kim CJ, Nazli A, Rojas OL, Chege D, Alidina Z, Huibner S, Mujib S, Benko E, Kovacs C, Shin LY, Grin A, Kandel G, Loutfy M, Ostrowski M, Gommerman JL, Kaushic C, Kaul R (2012) A role for mucosal IL-22 production and Th22 cells in HIV-associated mucosal immunopathogenesis. Mucosal Immunol 5:670–680

    Article  CAS  PubMed  Google Scholar 

  220. Abi Abdallah DS, Egan CE, Butcher BA, Denkers EY (2011) Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int Immunol 23:317–326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. Hansen JJ (2015) Immune responses to intestinal microbes in inflammatory bowel diseases. Curr Allergy Asthma Rep 15:61

    Article  PubMed  CAS  Google Scholar 

  222. Zhang YZ, Li YY (2014) Inflammatory bowel disease: pathogenesis. World J Gastroenterol 20:91–99

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  223. Vrakas S, Mountzouris KC, Michalopoulos G, Karamanolis G, Papatheodoridis G, Tzathas C, Gazouli M (2017) Intestinal bacteria composition and translocation of bacteria in inflammatory bowel disease. PLoS One 12:e0170034

    Article  PubMed  PubMed Central  Google Scholar 

  224. Sartor RB, Mazmanian SK (2012) Intestinal microbes in inflammatory bowel diseases. Am J Gastroenterol 1:15–21

    Article  CAS  Google Scholar 

  225. Levine AP, Segal AW (2013) What is wrong with granulocytes in inflammatory bowel diseases? Dig Dis 31:321–327

    Article  PubMed  PubMed Central  Google Scholar 

  226. Somasundaram R, Nuij VJ, van der Woude CJ, Kuipers EJ, Peppelenbosch MP, Fuhler GM (2013) Peripheral neutrophil functions and cell signalling in Crohn’s disease. PLoS One 8:e84521

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  227. Koelink PJ, Overbeek SA, Braber S, Morgan ME, Henricks PA, Abdul Roda M, Verspaget HW, Wolfkamp SC, te Velde AA, Jones CW, Jackson PL, Blalock JE, Sparidans RW, Kruijtzer JA, Garssen J, Folkerts G, Kraneveld AD (2014) Collagen degradation and neutrophilic infiltration: a vicious circle in inflammatory bowel disease. Gut 63:578–587

    Article  CAS  PubMed  Google Scholar 

  228. Yamada T, Grisham MB (1991) Role of neutrophil-derived oxidants in the pathogenesis of intestinal inflammation. Klin Wochenschr 69:988–994

    Article  CAS  PubMed  Google Scholar 

  229. Kristjánsson G, Venge P, Wanders A, Lööf L, Hällgren R (2004) Clinical and subclinical intestinal inflammation assessed by the mucosal patch technique: studies of mucosal neutrophil and eosinophil activation in inflammatory bowel diseases and irritable bowel syndrome. Gut 53:1806–1812

    Article  PubMed  PubMed Central  Google Scholar 

  230. Al-Sadi R, Ye D, Boivin M, Guo S, Hashimi M, Ereifej L, Ma TY (2014) Interleukin-6 modulation of intestinal epithelial tight junction permeability is mediated by JNK pathway activation of claudin-2 gene. PLoS One 9:e85345

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  231. Al-Sadi R, Guo S, Ye D, Ma TY (2013) TNF-α modulation of intestinal epithelial tight junction barrier is regulated by ERK1/2 activation of Elk-1. Am J Pathol 183:1871–1884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Hirao LA, Grishina I, Bourry O, Hu WK, Somrit M, Sankaran-Walters S, Gaulke CA, Fenton AN, Li JA, Crawford RW, Chuang F, Tarara R, Marco ML, Bäumler AJ, Cheng H, Dandekar S (2014) Early mucosal sensing of SIV infection by paneth cells induces IL-1β production and initiates gut epithelial disruption. PLoS Pathog 10:e1004311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  233. Takac B, Mihaljević S, Stefanić M, Glavas-Obrovac L, Kibel A, Samardzija M (2014) Importance of interleukin 6 in pathogenesis of inflammatory bowel disease. Coll Antropol 38:659–664

    PubMed  Google Scholar 

  234. Bank S, Andersen PS, Burisch J, Pedersen N, Roug S, Galsgaard J, Turino SY, Brodersen JB, Rashid S, Rasmussen BK, Avlund S, Olesen TB, Hoffmann HJ, Thomsen MK, Thomsen V, Frydenberg M, Nexø BA, Sode J, Vogel U, Andersen V (2014) Associations between functional polymorphisms in the NFκB signaling pathway and response to anti-TNF treatment in Danish patients with inflammatory bowel disease. Pharmacogenom J 14:526–534

    Article  CAS  Google Scholar 

  235. Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM (2004) TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 286:G367–G376

    Article  CAS  PubMed  Google Scholar 

  236. Ye D, Ma I, Ma TY (2006) Molecular mechanism of tumor necrosis factor-alpha modulation of intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol 290:G496–G504

    Article  CAS  PubMed  Google Scholar 

  237. Graham WV, Wang F, Clayburgh DR, Cheng JX, Yoon B, Wang Y, Lin A, Turner JR (2006) Tumor necrosis factor-induced long myosin light chain kinase transcription is regulated by differentiation-dependent signaling events. Characterization of the human long myosin light chain kinase promoter. J Biol Chem 281:26205–26215

    Article  CAS  PubMed  Google Scholar 

  238. Sankaran S, George MD, Reay E, Guadalupe M, Flamm J, Prindiville T, Dandekar S (2008) Rapid onset of intestinal epithelial barrier dysfunction in primary human immunodeficiency virus infection is driven by an imbalance between immune response and mucosal repair and regeneration. J Virol 82:538–545

    Article  CAS  PubMed  Google Scholar 

  239. Batman PA, Kapembwa MS, Belmonte L, Tudor G, Kotler DP, Potten CS, Booth C, Cahn P, Griffin GE (2014) HIV enteropathy: HAART reduces HIV-induced stem cell hyperproliferation and crypt hypertrophy to normal in jejunal mucosa. Clin Pathol 67:14–18

    Article  Google Scholar 

  240. Circu ML, Aw TY (2012) Intestinal redox biology and oxidative stress. Semin Cell Dev Biol 23:729–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  241. Sumagin R, Parkos CA (2015) Epithelial adhesion molecules and the regulation of intestinal homeostasis during neutrophil transepithelial migration. Tissue Barriers 3:e969100

    Article  PubMed  CAS  Google Scholar 

  242. Hatano H, Somsouk M, Sinclair E, Harvill K, Gilman L, Cohen M, Hoh R, Hunt PW, Martin JN, Wong JK, Deeks SG, Yukl SA (2013) Comparison of HIV DNA and RNA in gut-associated lymphoid tissue of HIV-infected controllers and noncontrollers. AIDS 27:2255–2260

    Article  PubMed  PubMed Central  Google Scholar 

  243. Mehandru S, Poles MA, Tenner-Racz K, Horowitz A, Hurley A, Hogan C, Boden D, Racz P, Markowitz M (2004) Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 200:761–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  244. Guadalupe M, Reay E, Sankaran S, Prindiville T, Flamm J, McNeil A, Dandekar S (2003) Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J Virol 77:11708–11717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  245. Steele AK, Lee EJ, Manuzak JA, Dillon SM, Beckham JD, McCarter MD, Santiago ML, Wilson CC (2014) Microbial exposure alters HIV-1-induced mucosal CD4+ T cell death pathways ex vivo. Retrovirology 11:14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  246. Dillon SM, Lee EJ, Donovan AM, Guo K, Harper MS, Frank DN, McCarter MD, Santiago ML, Wilson CC (2016) Enhancement of HIV-1 infection and intestinal CD4+ T cell depletion ex vivo by gut microbes altered during chronic HIV-1 infection. Retrovirology 13:5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  247. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M (2005) Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 434:1093–1097

    Article  CAS  PubMed  Google Scholar 

  248. George MD, Sankaran S, Reay E, Gelli AC, Dandekar S (2003) High-throughput gene expression profiling indicates dysregulation of intestinal cell cycle mediators and growth factors during primary simian immunodeficiency virus infection. Virology 312:84–94

    Article  CAS  PubMed  Google Scholar 

  249. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, Nguyen PL, Khoruts A, Larson M, Haase AT, Douek DC (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200:749–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Page EE, Greathead L, Metcalf R, Clark SA, Hart M, Fuchs D, Pantelidis P, Gotch F, Pozniak A, Nelson M, Boasso A, Gazzard B, Kelleher P (2014) Loss of Th22 cells is associated with increased immune activation and IDO-1 activity in HIV-1 infection. J Acquir Immune Defic Syndr 67:227–235

    Article  CAS  PubMed  Google Scholar 

  251. Ullrich R, Zeitz M, Heise W, L’age M, Höffken G, Riecken EO (1989) Small intestinal structure and function in patients infected with human immunodeficiency virus (HIV): evidence for HIV-induced enteropathy. Ann Intern Med 111:15–21

    Article  CAS  PubMed  Google Scholar 

  252. Batman PA, Kapembwa MS, Miller AR, Sedgwick PM, Lucas S, Sewankambo NK, Serwadda D, Pudney J, Moody A, Harris JR, Griffin GE (1998) HIV enteropathy: comparative morphometry of the jejunal mucosa of HIV infected patients resident in the United Kingdom and Uganda. Gut 43:350–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  253. Epple HJ, Schneider T, Troeger H, Kunkel D, Allers K, Moos V, Amasheh M, Loddenkemper C, Fromm M, Zeitz M, Schulzke JD (2009) Impairment of the intestinal barrier is evident in untreated but absent in suppressively treated HIV-infected patients. Gut 58:220–227

    Article  CAS  PubMed  Google Scholar 

  254. Nazli A, Chan O, Dobson-Belaire WN, Ouellet M, Tremblay MJ, Gray-Owen SD, Arsenault AL, Kaushic C (2010) Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 6:e1000852

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  255. Delézay O, Yahi N, Tamalet C, Baghdiguian S, Boudier JA, Fantini J (1997) Direct effect of type 1 human immunodeficiency virus (HIV-1) on intestinal epithelial cell differentiation: relationship to HIV-1 enteropathy. Virology 238:231–242

    Article  PubMed  Google Scholar 

  256. Phillips DM, Bourinbaiar AS (1992) Mechanism of HIV spread from lymphocytes to epithelia. Virology 186:261–273

    Article  CAS  PubMed  Google Scholar 

  257. Asmuth DM, Hammer SM, Wanke CA (1994) Physiological effects of HIV infection on human intestinal epithelial cells: an in vitro model for HIV enteropathy. AIDS 8:205–211

    Article  CAS  PubMed  Google Scholar 

  258. Liu R, Huang L, Li J, Zhou X, Zhang H, Zhang T, Lei Y, Wang K, Xie N, Zheng Y, Wang F, Nice EC, Rong L, Huang C, Wei Y (2013) HIV Infection in gastric epithelial cells. J Infect Dis 208:1221–1230

    Article  CAS  PubMed  Google Scholar 

  259. Horejsh D, Ruckwardt TJ, David Pauza C (2002) CXCR4-dependent HIV-1 infection of differentiated epithelial cells. Virus Res 90:275–286

    Article  CAS  PubMed  Google Scholar 

  260. Tang Y, George A, Nouvet F, Sweet S, Emeagwali N, Taylor HE, Simmons G, Hildreth JE (2014) Infection of female primary lower genital tract epithelial cells after natural pseudotyping of HIV 1: possible implications for sexual transmission of HIV-1. PLoS One 9:e101367

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  261. Kohli A, Islam A, Moyes DL, Murciano C, Shen C, Challacombe SJ, Naglik JR (2014) Oral and vaginal epithelial cell lines bind and transfer cell-free infectious HIV-1 to permissive cells but are not productively infected. PLoS One 9:e98077

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  262. Taborda NA, Gonzalez SM, Correa LA, Montoya CJ, Rugeles MT (2015) Spontaneous HIV controllers exhibit preserved immune parameters in peripheral blood and gastrointestinal mucosa. J Acquir Immune Defic Syndr 70:115–121

    Article  CAS  PubMed  Google Scholar 

  263. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, Blazar BR, Rodriguez B, Teixeira-Johnson L, Landay A, Martin JN, Hecht FM, Picker LJ, Lederman MM, Deeks SG, Douek DC (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12:1365–1371

    Article  CAS  PubMed  Google Scholar 

  264. Estes JD, Harris LD, Klatt NR, Tabb B, Pittaluga S, Paiardini M, Barclay GR, Smedley J, Pung R, Oliveira KM, Hirsch VM, Silvestri G, Douek DC, Miller CJ, Haase AT, Lifson J, Brenchley JM (2010) Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog 6:e1001052

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  265. Stockmann M, Schmitz H, Fromm M, Schmidt W, Pauli G, Scholz P, Riecken EO, Schulzke JD (2000) Mechanisms of epithelial barrier impairment in HIV infection. Ann N Y Acad Sci 915:293–303

    Article  CAS  PubMed  Google Scholar 

  266. Puerta-Arias JD, Pino-Tamayo PA, Arango JC, González Á (2016) Depletion of neutrophils promotes the resolution of pulmonary inflammation and fibrosis in mice infected with Paracoccidioides brasiliensis. PLoS One 11:e0163985

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  267. Nusbaum RJ, Calderon VE, Huante MB, Sutjita P, Vijayakumar S, Lancaster KL, Hunter RL, Actor JK, Cirillo JD, Aronson J, Gelman BB, Lisinicchia JG, Valbuena G, Endsley J (2016) Pulmonary tuberculosis in humanized mice infected with HIV-1. Sci Rep 6:21522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  268. Cassol E, Rossouw T, Malfeld S, Mahasha P, Slavik T, Seebregts C, Bond du Plessis J, Janssen C, Roskams T, Nevens F, Alfano M, Poli G, van der Merwe SW (2015) CD14(+) macrophages that accumulate in the colon of African AIDS patients express pro-inflammatory cytokines and are responsive to lipopolysaccharide. BMC Infect Dis 15:430

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  269. Somsouk M, Estes JD, Deleage C, Dunham RM, Albright R, Inadomi JM, Martin JN, Deeks SG, McCune JM, Hunt PW (2015) Gut epithelial barrier and systemic inflammation during chronic HIV infection. AIDS 29:43–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  270. Paiva CN, Bozza MT (2014) Are reactive oxygen species always detrimental to pathogens? Antioxid Redox Signal 20:1000–1037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  271. Cunningham KE, Turner JR (2012) Myosin light chain kinase: pulling the strings of epithelial tight junction function. Ann N Y Acad Sci 1258:34–42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  272. Fujioka S, Niu J, Schmidt C, Sclabas GM, Peng B, Uwagawa T, Li Z, Evans DB, Abbruzzese JL, Chiao PJ (2004) NF-kappaB and AP-1 connection: mechanism of NF-kappaB-dependent regulation of AP-1 activity. Mol Cell Biol 24:7806–7819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  273. Shen L, Black ED, Witkowski ED, Lencer WI, Guerriero V, Schneeberger EE, Turner JR (2006) Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci 119:2095–2106

    Article  CAS  PubMed  Google Scholar 

  274. Luettig J, Rosenthal R, Barmeyer C, Schulzke JD (2015) Claudin-2 as a mediator of leaky gut barrier during intestinal inflammation. Tissue Barriers 3:e977176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was funded by Jordan University of Science and Technology.

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Authors and Affiliations

  1. Medical Laboratory Sciences, College of Applied Medical Sciences, Jordan University of Science and Technology, Irbid, 22110, Jordan

    Mahmoud Mohammad Yaseen

  2. Applied Biological Sciences, College of Science and Arts, Jordan University of Science and Technology, Irbid, 22110, Jordan

    Nizar Mohammad Abuharfeil

  3. Public Health, College of Medicine, Jordan University of Science and Technology, Irbid, 22110, Jordan

    Mohammad Mahmoud Yaseen

  4. Chemical Sciences, College of Science and Arts, Jordan University of Science and Technology, Irbid, 22110, Jordan

    Barakat Mohammad Shabsoug

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  1. Mahmoud Mohammad Yaseen
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Yaseen, M.M., Abuharfeil, N.M., Yaseen, M.M. et al. The role of polymorphonuclear neutrophils during HIV-1 infection. Arch Virol 163, 1–21 (2018). https://doi.org/10.1007/s00705-017-3569-9

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