Role of Monocytes in the Pathogenesis of Dengue

  • Jorge Andrés Castillo
  • Juan Sebastián Naranjo
  • Mauricio Rojas
  • Diana Castaño
  • Paula Andrea VelillaEmail author


Diseases caused by dengue virus (DENV) are a major public health problem worldwide, considered one of the infections with more prevalence in tropical and subtropical zones of the world. Despite the intense research in the pathogenesis of DENV, this feature is not well understood. One of the main target cells for DENV infection is monocytes; these phagocytes can play a dual role, since they are essential to control viremia, but they also participate in the induction of tissue damage during DENV infection. Monocytes produce different pro-inflammatory cytokines and chemokines in response to infection, and also mediate endothelial damage. In peripheral blood, monocytes can be divided into three different subpopulations, namely classical, intermediate and non-classical, which differ in frequency, cytokine production, among others. Studies in the last years suggest that non-classical monocytes have higher affinity for microvasculature endothelium compared to other type of monocytes, which implies that they could be more involved in the increase of endothelial permeability observed during DENV infection. This review provides a general view of the role of monocytes and their subpopulations in DENV pathogenesis and its effect in viral replication. Finally, the potential contribution of these phagocytes in the alterations of endothelial permeability is discussed.


Dengue virus Monocytes Monocyte subpopulations Endothelial permeability Dengue virus pathogenesis 



This work was supported by COLCIENCIAS (111556933247) and by Universidad de Antioquia (Sostenibilidad). The authors wish to thank Anne-Lise Haenni for her constructive comments.


  1. Adikari TN, Gomes L, Wickramasinghe N et al (2016) Dengue NS1 antigen contributes to disease severity by inducing interleukin (IL)-10 by monocytes. Clin Exp Immunol 184:90–100Google Scholar
  2. Amorim JH, Alves RP dos Boscardin S SB et al (2014) The dengue virus non-structural 1 protein: Risks and benefits. Virus Res 181:53–60Google Scholar
  3. Ancuta P, Rao R, Moses A et al (2003) Fractalkine preferentially mediates arrest and migration of CD16+ monocytes. J Exp Med 197:1701–1707Google Scholar
  4. Anderson KB, Chunsuttiwat S, Nisalak A et al (2007) Burden of symptomatic dengue infection in children at primary school in Thailand: a prospective study. Lancet 369:1452–1459Google Scholar
  5. Appanna R, Wang SM, Ponnampalavanar S et al (2012) Cytokine factors present in dengue patient sera induces alterations of junctional proteins in human endothelial cells. Am J Trop Med Hyg 87:936–942Google Scholar
  6. Arias J, Valero N, Mosquera J et al (2014) Increased expression of cytokines, soluble cytokine receptors, soluble apoptosis ligand and apoptosis in dengue. Virology 452–453:42–51Google Scholar
  7. Aye KS, Charngkaew K, Win N et al (2014) Pathologic highlights of dengue hemorrhagic fever in 13 autopsy cases from Myanmar. Hum Pathol 45:1221–1233Google Scholar
  8. Azeredo EL, Neves-Souza PC, Alvarenga AR et al (2010) Differential regulation of toll-like receptor-2, toll-like receptor-4, CD16 and human leucocyte antigen-DR on peripheral blood monocytes during mild and severe dengue fever. Immunology 130:202–216Google Scholar
  9. Balakrishnan T, Bela-Ong DB, Toh YX et al (2011) Dengue virus activates polyreactive, natural IgG B cells after primary and secondary infection. PLoS One 6:e29430Google Scholar
  10. Balsitis SJ, Coloma J, Castro G et al (2009) Tropism of dengue virus in mice and humans defined by viral nonstructural protein 3-specific immunostaining. Am J Trop Med Hyg 80:416–424Google Scholar
  11. Balsitis SJ, Williams KL, Lachica R et al (2010) Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6:e1000790Google Scholar
  12. Beatty PR, Puerta-Guardo H, Killingbeck SS et al (2015) Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination. Sci Transl Med 7:304ra141Google Scholar
  13. Beltrán D, López-Vergès S (2014) NK cells during dengue disease and their recognition of dengue virus-infected cells. Front Immunol 5:192Google Scholar
  14. Bhatt S, Gething PW, Brady OJ et al (2013) The global distribution and burden of dengue. Nature 496:504–507Google Scholar
  15. Bosch I, Xhaja K, Estevez L et al (2002) Increased production of interleukin-8 in primary human monocytes and in human epithelial and endothelial cell lines after dengue virus challenge. J Virol 76:5588–5597Google Scholar
  16. Bozza FA, Cruz OG, Zagne SM et al (2008) Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity. BMC Infect Dis 8:86Google Scholar
  17. Burbano C, Villar-Vesga J, Orejuela J et al (2018) Potential involvement of platelet-derived microparticles and microparticles forming immune complexes during monocyte activation in patients with systemic lupus erythematosus. Front Immunol 9:322Google Scholar
  18. Burke-Gaffney A, Keenan AK (1993) Modulation of human endothelial cell permeability by combinations of the cytokines interleukin-1 alpha/beta, tumor necrosis factor-alpha and interferon-gamma. Immunopharmacology 25:1–9Google Scholar
  19. Chakravarti A, Kumaria R (2006) Circulating levels of tumour necrosis factor-α and interferon-γ in patients with dengue and dengue haemorrhagic fever during an outbreak. Indian J Med Res 123:25–30Google Scholar
  20. Chareonsirisuthigul T, Kalayanarooj S, Ubol S (2007) Dengue virus (DENV) antibody-dependent enhancement of infection upregulates the production of anti-inflammatory cytokines, but suppresses anti-DENV free radical and pro-inflammatory cytokine production, in THP-1 cells. J Gen Virol 88(Pt 2):365–375Google Scholar
  21. Chau TNB, Hieu NT, Anders KL et al (2009) Dengue virus infections and maternal antibody decay in a prospective birth cohort study of Vietnamese infants. J Infect Dis 200:1893–1900Google Scholar
  22. Chen YC, Wang SY (2002) Activation of terminally differentiated human monocytes / macrophages by dengue virus: productive infection, hierarchical production of innate cytokines and chemokines, and the synergistic effect of lipopolysaccharide. J Virol 76:9877–9887Google Scholar
  23. Chen YC, Wang SY, King CC (1999) Bacterial lipopolysaccharide inhibits dengue virus infection of primary human monocytes/macrophages by blockade of virus entry via a CD14-dependent mechanism. J Virol 73:2650–2657Google Scholar
  24. Chen J, Ng MM, Chu JJ (2015) Activation of TLR2 and TLR6 by dengue NS1 protein and its implications in the immunopathogenesis of dengue virus infection. PLoS Pathog 11:e1005053Google Scholar
  25. Chousterman BG, Boissonnas A, Poupel L et al (2016) Ly6Chigh monocytes protect against kidney damage during sepsis via a CX3CR1-dependent adhesion mechanism. J Am Soc Nephrol 27:792–803Google Scholar
  26. Clark KB, Noisakran S, Onlamoon N et al (2012) Multiploid CD61+ cells are the pre-dominant cell lineage infected during acute dengue virus infection in bone marrow. PLoS One 7:e52902Google Scholar
  27. Collison JL, Carlin LM, Eichmann M et al (2015) Heterogeneity in the locomotory behavior of human monocyte subsets over human vascular endothelium in vitro. J Immunol 195:1162–1170Google Scholar
  28. Cros J, Cagnard N, Woollard K et al (2010) Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 33:375–386Google Scholar
  29. Cruz-Oliveira C, Freire JM, Conceição TM et al (2015) Receptors and routes of dengue virus entry into the host cells. FEMS Microbiol Rev 39:155–170Google Scholar
  30. da Silva Voorham JM, Rodenhuis-Zybert IA, Ayala Nuñez NV et al (2012) Antibodies against the envelope glycoprotein promote infectivity of immature dengue virus serotype 2. PLoS One 7:e29957Google Scholar
  31. Dalrymple NA, Mackow ER (2012) Endothelial cells elicit immune-enhancing responses to dengue virus infection. J Virol 86:6408–6415Google Scholar
  32. Dejnirattisai W, Jumnainsong A, Onsirisakul N et al (2010) Cross-reacting antibodies enhance dengue virus infection in humans. Science 328:745–748Google Scholar
  33. Devignot S, Sapet C, Duong V et al (2010) Genome-wide expression profiling deciphers host responses altered during dengue shock syndrome and reveals the role of innate immunity in severe dengue. PLoS One 5:e11671Google Scholar
  34. Dewi BE, Takasaki T, Kurane I (2004) In vitro assessment of human endothelial cell permeability: effects of inflammatory cytokines and dengue virus infection. J Virol Methods 121:171–180Google Scholar
  35. Diamond MS, Edgil D, Roberts TG et al (2000) Infection of human cells by dengue virus is modulated by different cell types and viral strains. J Virol 74:7814–7823Google Scholar
  36. Duong V, Ly S, Try P et al (2011) Clinical and virological factors influencing the performance of a ns1 antigen-capture assay and potential use as a marker of dengue disease severity. PLoS Negl Trop Dis 5:e1244Google Scholar
  37. Durbin AP, Vargas MJ, Wanionek K et al (2008) Phenotyping of peripheral blood mononuclear cells during acute dengue illness demonstrates infection and increased activation of monocytes in severe cases compared to classic dengue fever. Virology 376:429–435Google Scholar
  38. Espina LM, Valero NJ, Hernández JM et al (2003) Increased apoptosis and expression of tumor necrosis factor-alpha caused by infection of cultured human monocytes with dengue virus. Am J Trop Med Hyg 68:48–53Google Scholar
  39. Falconar AK (1997) The dengue virus nonstructural-1 protein (NS1) generates antibodies to common epitopes on human blood clotting, integrin/adhesin proteins and binds to human endothelial cells: potential implications in haemorrhagic fever pathogenesis. Arch Virol 142:897–916Google Scholar
  40. Garcia-Bates TM, Cordeiro MT, Nascimento EJ et al (2013) Association between magnitude of the virus-specific plasmablast response and disease severity in dengue patients. J Immunol 190:80–87Google Scholar
  41. Geissmann F, Jung S, Littman DR (2003) Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:71–82Google Scholar
  42. Goncalvez AP, Engle RE, St Claire MS et al (2007) Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. Proc Natl Acad Sci USA 104:9422–9427Google Scholar
  43. Guzman M, Kouri G, Bravo J et al (2002) Effect of age on outcome of secondary dengue 2 infections. Int J Infect Dis 6:118–124Google Scholar
  44. Halstead SB (1979) In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J Infect Dis 140:527–533Google Scholar
  45. Halstead SB (2007) Dengue. Lancet 370:1644–1652Google Scholar
  46. Halstead SB (2008) Pathogenesis: risk factors prior to infection. In: Halstead SB (ed) Dengue. Imperial College Press, London, pp 219–256Google Scholar
  47. Halstead SB, O’Rourke EJ (1977) Dengue viruses and mononuclear phagocytes. Infection enhancement by non-neutralizing antibody. J Exp Med 146:201–217Google Scholar
  48. Halstead SB, Marchette N, Sung Chow J et al (1976) Dengue virus replication enhancement in peripheral blood leukocytes from immune human beings. Proc Soc Exp Biol Med 151:136–139Google Scholar
  49. Halstead SB, O´Rourke EJ, Allison AC (1977) Dengue viruses and mononuclear phagocytes II: identity of blood and tissue leukocytes supporting in vitro infection. J Exp Med 146:218–229Google Scholar
  50. Halstead SB, Mahalingam S, Marovich MA et al (2010) Intrinsic antibody-dependent enhancement of microbial infection in macrophages: disease regulation by immune complexes. Lancet Infect Dis 10:712–722Google Scholar
  51. Jessie K, Fong MY, Devi S et al (2004) Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J Infect Dis 189:1411–1418Google Scholar
  52. Kanlaya R, Pattanakitsakul S, Sinchaikul S et al (2009) Alterations in actin cytoskeletal assembly and junctional protein complexes in human endothelial cells induced by dengue virus infection and mimicry of leukocyte transendothelial migration. J Proteome Res 8:2551–2562Google Scholar
  53. Kelley JF, Kaufusi PH, Nerurkar VR (2012) Dengue hemorrhagic fever-associated immunomediators induced via maturation of dengue virus nonstructural 4B protein in monocytes modulate endothelial cell adhesion molecules and human microvascular endothelial cells permeability. Virology 422:326–337Google Scholar
  54. Klomporn P, Panyasrivanit M, Wikan N et al (2011) Dengue infection of monocytic cells activates ER stress pathways, but apoptosis is induced through both extrinsic and intrinsic pathways. Virology 409:189–197Google Scholar
  55. Kou Z, Quinn M, Chen H et al (2008) Monocytes, but not T or B cells, are the principal target cells for dengue virus (DV) Infection among human peripheral blood mononuclear cells. J Med Virol 80:134–146Google Scholar
  56. Kumar Y, Liang C, Bo Z et al (2012) Serum proteome and cytokine analysis in a longitudinal cohort of adults with primary dengue infection reveals predictive markers of DHF. PLoS Negl Trop Dis 6:e1887Google Scholar
  57. Kwissa M, Nakaya HI, Onlamoon N et al (2014) Dengue virus infection induces expansion of a CD14(+)CD16(+) monocyte population that stimulates plasmablast differentiation. Cell Host Microbe 16:115–127Google Scholar
  58. Lech M, Avila-Ferrufino A, Skuginna V et al (2010) Quantitative expression of RIG-like helicase, NOD-like receptor and inflammasome-related mRNAs in humans and mice. Int Immunol 22:717–728Google Scholar
  59. Lee YR, Liu MT, Lei HY et al (2006) MCP1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol 87(Pt 12):3623–3630Google Scholar
  60. Libraty DH, Young PR, Pickering D et al (2002) High circulating levels of the dengue virus nonstructural protein NS1 early in dengue illness correlate with the development of dengue hemorrhagic fever. J Infect Dis 186:1165–1168Google Scholar
  61. Lin C, Lei H, Liu C et al (2001) Generation of IgM anti-platelet autoantibody in dengue patients. J Med Virol 63:143–149Google Scholar
  62. Lin CF, Lei HY, Shiau AL et al (2003) Antibodies from dengue patient sera cross-react with endothelial cells and induce damage. J Med Virol 69:82–90Google Scholar
  63. Malavige GN, Ogg GS (2017) Pathogenesis of vascular leak in dengue virus infection. Immunology 151:261–269Google Scholar
  64. Martina BE, Koraka P, Osterhaus AD (2009) Dengue virus pathogenesis: an integrated view. Clin Microbiol Rev 22:564–581Google Scholar
  65. Martínez Gómez JM, Ong LC, Lam JH et al (2016) Maternal antibody-mediated disease enhancement in type I interferon-deficient mice leads to lethal disease associated with liver damage. PLoS Negl Trop Dis 10:e0004536Google Scholar
  66. Méndez Á, González G (2006) Manifestaciones clínicas inusuales del dengue hemorrágico en niños Abnormal clinical manifestations of dengue hemorrhagic fever in children. Biomedica 26:61–70Google Scholar
  67. Mikołajczyk TP, Osmenda G, Batko B et al (2016) Heterogeneity of peripheral blood monocytes, endothelial dysfunction and subclinical atherosclerosis in patients with systemic lupus erythematosus. Lupus 25:18–27Google Scholar
  68. Miller JL, de Wet BJ, Martinez-Pomares L et al (2008) The mannose receptor mediates dengue virus infection of macrophages. PLoS Pathog 4:e17Google Scholar
  69. Modhiran N, Watterson D, Muller DA et al (2015) Dengue virus NS1 protein activates cells via Toll-like receptor 4 and disrupts endothelial cell monolayer integrity. Sci Transl Med 7:304ra142Google Scholar
  70. Mongkolsapaya J, Dejnirattisai W, Xu XN et al (2003) Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 9:921–927Google Scholar
  71. Mukhopadhyay S, Kuhn RJ, Rossmann MG (2005) A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 3:13–22Google Scholar
  72. Nasirudeen AM, Wong HH, Thien P et al (2011) RIG-I, MDA5 and TLR3 synergistically play an important role in restriction of dengue virus infection. PLoS Negl Trop Dis 5:e926Google Scholar
  73. Navarro-Sánchez E, Desprès P, Cedillo-Barrón L (2005) Innate immune responses to dengue virus. Arch Med Res 36:425–435Google Scholar
  74. Neves-Souza PC, Azeredo EL, Zagne SM et al (2005) Inducible nitric oxide synthase (iNOS) expression in monocytes during acute dengue Fever in patients and during in vitro infection. BMC Infect Dis 5:64Google Scholar
  75. Ng JK, Zhang SL, Tan HC et al (2014) First experimental in vivo model of enhanced dengue disease severity through maternally acquired heterotypic dengue antibodies. PLoS Pathog 10:1004031Google Scholar
  76. Nguyen TH, Lei HY, Nguyen TL et al (2004) Dengue hemorrhagic fever in infants: a study of clinical and cytokine profiles. J Infect Dis 189:221–232Google Scholar
  77. Nguyen TH, Nguyen TL, Lei HY et al (2005) Association between sex, nutritional status, severity of dengue hemorrhagic fever, and immune status in infants with dengue hemorrhagic fever. Am J Trop Med Hyg 72:370–374Google Scholar
  78. Pang T, Cardosa MJ, Guzman MG (2006) Of cascades and perfect storms: the immunopathogenesis of dengue haemorrhagic fever-dengue shock syndrome (DHF/DSS). Immunol Cell Biol 85:43–45Google Scholar
  79. Pérez AB, García G, Sierra B et al (2004) IL-10 levels in dengue patients: some findings from the exceptional epidemiological conditions in Cuba. J Med Virol 73:230–234Google Scholar
  80. Puerta-Guardo H, Raya-Sandino A, González-Mariscal L et al (2013) The cytokine response of U937-derived macrophages infected through antibody-dependent enhancement of dengue virus disrupts cell apical-junction complexes and increases vascular permeability. J Virol 87:7486–7501Google Scholar
  81. Puerta-Guardo H, Glasner DR, Harris E (2016) Dengue virus NS1 disrupts the endothelial glycocalyx, leading to hyperpermeability. PLoS Pathog 12:e1005738Google Scholar
  82. Qin CF, Zhao H, Liu ZY et al (2011) Retinoic acid inducible gene-I and melanoma differentiation-associated gene 5 are induced but not essential for dengue virus induced type I interferon response. Mol Biol Rep 38:3867–3873Google Scholar
  83. Restrepo BN, Isaza DM, Salazar CL et al (2008) Serum levels of interleukin-6, tumor necrosis factor-alpha and interferon-gama in infants with and without dengue Níveis séricos de interleucina-6, fator de necrose tumoral-alfa e interferon-gama em crianças menores de um ano com e sem dengue. Rev Soc Bras Med Trop 41:6–10Google Scholar
  84. Reyes-del Valle J, Salas-Benito J, Soto-Acosta R et al (2014) Dengue virus cellular receptors and tropism. Curr Trop Med Rep 1:36–43Google Scholar
  85. Rodenhuis-Zybert IA, van der Schaar HM, da Silva Voorham JM et al (2010) Immature dengue virus: a veiled pathogen? PLoS Pathog 6:e1000718Google Scholar
  86. Saha P, Geissmann F (2011) Toward a functional characterization of blood monocytes. Immunol Cell Biol 89:2–4Google Scholar
  87. Saito M, Oishi K, Inoue S et al (2004) Association of increased platelet-associated immunoglobulins with thrombocytopenia and the severity of disease in secondary dengue virus infections. Clin Exp Immunol 138:299–303Google Scholar
  88. Schneberger D, Aharonson-Raz K, Singh B (2011) Monocyte and macrophage heterogeneity and Toll-like receptors in the lung. Cell Tissue Res 343:97–106Google Scholar
  89. Simmons CP, Chau TN, Thuy TT et al (2007) Maternal antibody and viral factors in the pathogenesis of dengue virus in infants. J Infect Dis 196:416–424Google Scholar
  90. Simmons CP, Farrar JJ, Nguyen VV et al (2012) Dengue. N Engl J Med 366:1423–1432Google Scholar
  91. Skrzeczyñska J, Kobylarz K, Hartwich Z et al (2002) CD14+ CD16+ monocytes in the course of sepsis in neonates and small children: monitoring and functional studies. Scand J Immunol 55:629–638Google Scholar
  92. Srikiatkhachorn A, Mathew A, Rothman AL (2017) Immune-mediated cytokine storm and its role in severe dengue. Semin Immunopathol 39:563–574Google Scholar
  93. Sun P, Kochel TJ (2013) The battle between infection and host immune responses of dengue virus and its implication in dengue disease pathogenesis. Sci World J 2013:843469Google Scholar
  94. Sun P, Bauza K, Pal S et al (2011) Infection and activation of human peripheral blood monocytes by dengue viruses through the mechanism of antibody-dependent enhancement. Virology 421:245–252Google Scholar
  95. Tan TY, Chu JJH (2013) Dengue virus-infected human monocytes trigger late activation of caspase-1, which mediates pro-inflammatory IL-1β secretion and pyroptosis. J Gen Virol 94(Pt 10):2215–2220Google Scholar
  96. Torrentes-Carvalho A, Azeredo EL, Reis SR et al (2009) Dengue-2 infection and the induction of apoptosis in human primary monocytes. Mem Inst Oswaldo Cruz 104:1091–1099Google Scholar
  97. Tsai TT, Chuang YJ, Lin YS et al (2014) Antibody-dependent enhancement infection facilitates dengue virus-regulated signaling of IL-10 production in monocytes. PLoS Negl Trop Dis 8(11):e3320Google Scholar
  98. Ubol S, Phuklia W, Kalayanarooj S et al (2010) Mechanisms of immune evasion induced by a complex of dengue virus and preexisting enhancing antibodies. J Infect Dis 201:923–935Google Scholar
  99. Urcuqui-Inchima S, Patiño C, Torres S et al (2010) Recent developments in understanding dengue virus replication. Adv Virus Res 77:1–39Google Scholar
  100. Wan SW, Lin CF, Yeh TM et al (2013) Autoimmunity in dengue pathogenesis. J Formos Med Assoc 112:3–11Google Scholar
  101. Weiskopf D, Angelo MA, de Azeredo EL et al (2013) Comprehensive analysis of dengue virus-specific responses supports an HLA-linked protective role for CD8+ T cells. Proc Natl Acad Sci 110:E2046–E2053Google Scholar
  102. Whitehead SS, Blaney JE, Durbin AP et al (2007) Prospects for a dengue virus vaccine. Nat Rev Microbiol 5:518–528Google Scholar
  103. Whitehorn J, Yacoub S, Anders KL et al (2014) Dengue therapeutics, chemoprophylaxis, and allied tools: state of the art and future directions. PLoS Negl Trop Dis 8:e3025Google Scholar
  104. Wong KL, Tai JJ, Wong W et al (2011) Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood 118:e16–e31Google Scholar
  105. Wong KL, Chen W, Balakrishnan T et al (2012a) Susceptibility and response of human blood monocyte subsets to primary dengue virus infection. PLoS One 7:e36435Google Scholar
  106. Wong KL, Yeap WH, Tai JJ et al (2012b) The three human monocyte subsets: implications for health and disease. Immunol Res 53:41–57Google Scholar
  107. World Health Organization (2009) Dengue. Guidelines for diagnosis, treatment, prevention and control. New edition 2009. WHO Press, GenevaGoogle Scholar
  108. Yoshimoto S, Nakatani K, Iwano M et al (2007) Elevated levels of fractalkine expression and accumulation of CD16+ monocytes in glomeruli of active lupus nephritis. Am J Kidney Dis 50:47–58Google Scholar
  109. Ziegler-Heitbrock HW (2000) Definition of human blood monocytes. J Leukoc Biol 67:603–606Google Scholar
  110. Ziegler-Heitbrock L, Hofer TP (2013) Toward a refined definition of monocyte subsets. Front Immunol 4:23Google Scholar

Copyright information

© L. Hirszfeld Institute of Immunology and Experimental Therapy, Wroclaw, Poland 2018

Authors and Affiliations

  • Jorge Andrés Castillo
    • 1
  • Juan Sebastián Naranjo
    • 2
  • Mauricio Rojas
    • 2
    • 3
  • Diana Castaño
    • 2
  • Paula Andrea Velilla
    • 1
    Email author
  1. 1.Grupo de Inmunovirología. Departamento de Microbiología y Parasitología, Facultad de MedicinaUniversidad de Antioquia UdeAMedellínColombia
  2. 2.Grupo de Inmunología Celular e Inmunogenética (GICIG). Instituto de Investigaciones Médicas, Facultad de MedicinaUniversidad de Antioquia UdeAMedellínColombia
  3. 3.Unidad de Citometría, Facultad de Medicina, Sede de Investigación UniversitariaUniversidad de Antioquia UdeAMedellínColombia

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