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Deciphering Endothelial Dysfunction in the HIV-Infected Population

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Reviews on Biomarker Studies of Metabolic and Metabolism-Related Disorders

Part of the book series: Advances in Experimental Medicine and Biology ((PMISB,volume 1134))

Abstract

Cardiovascular disease (CVD), as a possible consequence of endothelial dysfunction, is prevalent among HIV-infected patients despite successful administration of antiretroviral drugs. This warrants the routine clinical assessment of endothelial function in HIV-positive patients to circumvent potential CVD events. Several different non-invasive strategies have been employed to assess endothelial function in clinical research studies yielding inconsistencies among these reports. This review summarises the different techniques used for assessing endothelial function, with a focus on proposed blood-based biomarkers, such as endothelial leukocyte adhesion molecule-1 (E-selectin), soluble intercellular adhesion molecule-1 (sICAM-1), soluble vascular cell adhesion molecule-1 (sVCAM-1), von Willebrand factor (vWF), TNF-α, interleukin 6 (IL6) and soluble thrombomodulin (sTM). The identification of suitable blood-based biomarkers, especially those that can be measured using a point-of-care device, would be more applicable in under-resourced countries where the prevalence of HIV is high.

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References

  1. UNAIDS (2017) Global AIDS Monitoring. Geneva: UNAIDS. http://www.unaids.org/sites/default/files/media_asset/2017-Global-AIDS-Monitoring_en.pdf

  2. Chow FC, Regan S, Feske S, Meigs JB, Grinspoon SK, Triant VA (2012) Comparison of ischemic stroke incidence in HIV-infected and non-HIV-infected patients in a US health care system. J Acquir Immune Defic Syndr 60:351–358

    Article  PubMed  PubMed Central  Google Scholar 

  3. Freiberg MS, Chang CC, Kuller LH, Skanderson M, Lowy E, Kraemer KL et al (2013) HIV infection and the risk of acute myocardial infarction. JAMA Intern Med 173:614–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Wang T, Yi R, Green LA, Chelvanambi S, Seimetz M, Clauss M (2015) Increased cardiovascular disease risk in the HIV-positive population on ART: potential role of HIV-Nef and Tat. Cardiovasc Pathol 24:279–282

    Article  PubMed  PubMed Central  Google Scholar 

  5. Stein JH (2006) Cardiovascular risk in patients with human immunodeficiency virus infection: incomplete data. J Am Coll Cardiol 47:1124–1125

    Article  PubMed  Google Scholar 

  6. Zheng M, Kimura S, Nio-Kobayashi J, Iwanaga T (2016) The selective distribution of LYVE-1-expressing endothelial cells and reticular cells in the reticulo-endothelial system (RES). Biomed Res 37:187–198

    Article  PubMed  Google Scholar 

  7. Verma S, Anderson TJ (2002) Fundamentals of endothelial function for the clinical cardiologist. Circulation 105:546–549

    Article  CAS  PubMed  Google Scholar 

  8. Davignon J, Ganz P (2004) Role of endothelial dysfunction in atherosclerosis. Circulation 109(23 Suppl 1):III27–III32

    PubMed  Google Scholar 

  9. Vanhoutte PM (1997) Endothelial dysfunction and atherosclerosis. Eur Heart J 18:19–29

    Article  Google Scholar 

  10. Brevetti G, Schiano V, Chiariello M (2008) Endothelial dysfunction: a key to the pathophysiology and natural history of peripheral arterial disease? Atherosclerosis 197:1–11

    Article  CAS  PubMed  Google Scholar 

  11. Ludmer PL, Selwyn AP, Shook TL, Wayne RR, Mudge GH, Alexander RW et al (1986) Paradoxical vasoconstriction induced by acetylcholine in atherosclerotic coronary arteries. N Engl J Med 315:1046–1051

    Article  CAS  PubMed  Google Scholar 

  12. Planès R, Serrero M, Leghmari K, BenMohamed L, Bahraoui E (2018) HIV-1 envelope glycoproteins induce the production of TNF-α and IL-10 in human monocytes by activating calcium pathway. Sci Rep 8:17215. https://doi.org/10.1038/s41598-018-35478-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hansson GK, Libby P (2006) The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 6:508–519

    Article  CAS  PubMed  Google Scholar 

  14. Gimbrone MA Jr, Nagel T, Topper JN (1997) Biomechanical activation: an emerging paradigm in endothelial adhesion biology. J Clin Invest 99:1809–1813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bruyndonckx L, Hoymans VY, Van Craenenbroeck AH, Vissers DK, Vrints CJ, Ramet J et al (2013) Assessment of endothelial dysfunction in childhood obesity and clinical use. Oxidative Med Cell Longev 2013:174782. https://doi.org/10.1155/2013/174782

    Article  Google Scholar 

  16. Liao JK (2013) Linking endothelial dysfunction with endothelial cell activation. J Clin Invest 123:540–541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399:601–605

    Article  CAS  PubMed  Google Scholar 

  18. Furchgott RF, Zawadzki JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288:373–376

    Article  CAS  PubMed  Google Scholar 

  19. Virdis A, Ghiadoni L, Taddei S (2010) Human endothelial dysfunction: EDCFs. Pflugers Arch 459:1015–1023

    Article  CAS  PubMed  Google Scholar 

  20. Flammer AJ, Luscher TF (2010) Human endothelial dysfunction: EDRFs. Pflugers Arch 459:1005–1013

    Article  CAS  PubMed  Google Scholar 

  21. Hong YM (2010) Atherosclerotic cardiovascular disease beginning in childhood. Korean Circ J 40:1–9

    Article  PubMed  PubMed Central  Google Scholar 

  22. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr et al (1995) A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 92:1355–1374

    Article  CAS  PubMed  Google Scholar 

  23. Skaug EA, Aspenes ST, Oldervoll L, Mørkedal B, Vatten L, Wisløff U et al (2013) Age and gender differences of endothelial function in 4739 healthy adults: the HUNT3 Fitness Study. Eur J Prev Cardiol 20:531–540

    Article  PubMed  Google Scholar 

  24. Goldfine AB, Beckman JA, Betensky RA, Devlin H, Hurley S, Varo N et al (2006) Family history of diabetes is a major determinant of endothelial function. J Am Coll Cardiol 47:2456–2461

    Article  CAS  PubMed  Google Scholar 

  25. Siasos G, Chrysohoou C, Tousoulis D, Oikonomou E, Panagiotakos D, Zaromitidou M et al (2013) The impact of physical activity on endothelial function in middle-aged and elderly subjects: the Ikaria study. Hell J Cardiol 54:94–101

    Google Scholar 

  26. Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G, Baron AD (1996) Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J Clin Invest 97:2601–2610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mäkimattila S, Virkamäki A, Groop PH, Cockcroft J, Utriainen T, Fagerudd J et al (1996) Chronic hyperglycemia impairs endothelial function and insulin sensitivity via different mechanisms in insulin-dependent diabetes mellitus. Circulation 94:1276–1282

    Article  PubMed  Google Scholar 

  28. Celermajer DS, Sorensen KE, Georgakopoulos D, Bull C, Thomas O, Robinson J et al (1993) Cigarette smoking is associated with dose-related and potentially reversible impairment of endothelium-dependent dilation in healthy young adults. Circulation 88:2149–2155

    Article  CAS  PubMed  Google Scholar 

  29. Romero-Corral A, Sert-Kuniyoshi FH, Sierra-Johnson J, Orban M, Gami A, Davison D et al (2010) Modest visceral fat gain causes endothelial dysfunction in healthy humans. J Am Coll Cardiol 56:662–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Virdis A, Ghiadoni L, Cardinal H, Favilla S, Duranti P, Birindelli R et al (2001) Mechanisms responsible for endothelial dysfunction induced by fasting hyperhomocystinemia in normotensive subjects and patients with essential hypertension. J Am Coll Cardiol 38:1106–1115

    Article  CAS  PubMed  Google Scholar 

  31. Masiá M, Padilla S, García N, Jarrin I, Bernal E, López N et al (2010) Endothelial function is impaired in HIV-infected patients with lipodystrophy. Antivir Ther 15:101–110

    Article  PubMed  CAS  Google Scholar 

  32. Grunfeld C, Delaney JA, Wanke C, Currier JS, Scherzer R, Biggs ML et al (2009) Preclinical atherosclerosis due to HIV infection: carotid intima-medial thickness measurements from the FRAM study. AIDS 23:1841–1849

    Article  PubMed  Google Scholar 

  33. Solages A, Vita JA, Thornton DJ, Murray J, Heeren T, Craven DE et al (2006) Endothelial function in HIV-infected persons. Clin Infect Dis 42:1325–1332

    Article  PubMed  Google Scholar 

  34. McLenachan JM, Vita J, Fish DR, Treasure CB, Cox DA, Ganz P et al (1990) Early evidence of endothelial vasodilator dysfunction at coronary branch points. Circulation 82:1169–1173

    Article  CAS  PubMed  Google Scholar 

  35. Blann AD, Woywodt A, Bertolini F, Bull TM, Buyon JP, Clancy RM et al (2005) Circulating endothelial cells. Thromb Haemost 93:228–235

    Article  CAS  PubMed  Google Scholar 

  36. Wassmann S, Werner N, Czech T, Nickenig G (2006) Improvement of endothelial function by systemic transfusion of vascular progenitor cells. Circ Res 99:E74–E83

    Article  CAS  PubMed  Google Scholar 

  37. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T et al (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–966

    Article  CAS  PubMed  Google Scholar 

  38. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K et al (2003) Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 9:1370–1376

    Article  CAS  PubMed  Google Scholar 

  39. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR et al (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109:625–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Georgescu A, Alexandru N, Andrei E, Dragan E, Cochior D, Dias S (2016) Effects of transplanted circulating endothelial progenitor cells and platelet microparticles in atherosclerosis development. Biol Cell 108:219–243

    Article  CAS  PubMed  Google Scholar 

  41. Wang T, Green LA, Gupta SK, Kim C, Wang L, Almodovar S et al (2014) Transfer of intracellular HIV Nef to endothelium causes endothelial dysfunction. PLoS One 9:e91063. https://doi.org/10.1371/journal.pone.0091063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Matzen K, Dirkx AE, oude Egbrink MG, Speth C, Götte M, Ascherl G et al (2004) HIV-1 Tat increases the adhesion of monocytes and T-cells to the endothelium in vitro and in vivo: implications for AIDS-associated vasculopathy. Virus Res 104:145–155

    Article  CAS  PubMed  Google Scholar 

  43. Jiang J, Fu W, Wang X, Lin PH, Yao Q, Chen C (2010) HIV gp120 induces endothelial dysfunction in tumour necrosis factor-alpha-activated porcine and human endothelial cells. Cardiovasc Res 87:366–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Dhawan S, Puri RK, Kumar A, Duplan H, Masson JM, Aggarwal BB (1997) Human immunodeficiency virus-1–tat protein induces the cell surface expression of endothelial leukocyte adhesion molecule-1, vascular cell adhesion molecule-1, and intercellular adhesion molecule-1 in human endothelial cells. Blood 90:1535–1544

    CAS  PubMed  Google Scholar 

  45. Arildsen H, Sørensen KE, Ingerslev JM, Østergaard LJ, Laursen AL (2013) Endothelial dysfunction, increased inflammation, and activated coagulation in HIV-infected patients improve after initiation of highly active antiretroviral therapy. HIV Med 14:1–9

    Article  CAS  PubMed  Google Scholar 

  46. Fourie C, van Rooyen J, Pieters M, Conradie K, Hoekstra T, Schutte A (2011) Is HIV-1 infection associated with endothelial dysfunction in a population of African ancestry in South Africa? Cardiovasc J Afr 22:134–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Deeks SG, Tracy R, Douek DC (2013) Systemic effects of inflammation on health during chronic HIV infection. Immunity 39:633–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Walker NF, Scriven J, Meintjes G, Wilkinson RJ (2015) Immune reconstitution inflammatory syndrome in HIV-infected patients. HIV AIDS (Auckl) 7:49–64

    Google Scholar 

  49. Flammer AJ, Anderson T, Celermajer DS, Creager MA, Deanfield J, Ganz P et al (2012) The assessment of endothelial function: from research into clinical practice. Circulation 126:753–767

    Article  PubMed  PubMed Central  Google Scholar 

  50. Verma S, Buchanan MR, Anderson TJ (2003) Endothelial function testing as a biomarker of vascular disease. Circulation 108:2054–2059

    Article  PubMed  Google Scholar 

  51. da Silva EF, Fonseca FA, França CN, Ferreira PR, Izar MC, Salomão R et al (2011) Imbalance between endothelial progenitors cells and microparticles in HIV-infected patients naive for antiretroviral therapy. AIDS 25:1595–1601

    Article  PubMed  Google Scholar 

  52. Yoder MC (2009) Defining human endothelial progenitor cells. J Thromb Haemost 7:49–52

    Article  CAS  PubMed  Google Scholar 

  53. Masouleh BK, Baraniskin A, Schmiegel W, Schroers R (2010) Quantification of circulating endothelial progenitor cells in human peripheral blood: establishing a reliable flow cytometry protocol. J Immunol Methods 357:38–42

    Article  CAS  PubMed  Google Scholar 

  54. Boulanger CM, Amabile N, Tedgui A (2006) Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease. Hypertension 48:180–186

    Article  CAS  PubMed  Google Scholar 

  55. Sun D, Wu Y, Yuan Y, Wang Y, Liu W, Yang J (2015) Is the atherosclerotic process accentuated under conditions of HIV infection, antiretroviral therapy, and protease inhibitor exposure? Meta-analysis of the markers of arterial structure and function. Atherosclerosis 242:109–116

    Article  CAS  PubMed  Google Scholar 

  56. Kuvin JT, Patel AR, Sliney KA, Pandian NG, Sheffy J, Schnall RP et al (2003) Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J 146:168–174

    Article  PubMed  Google Scholar 

  57. Lavie P, Schnall RP, Sheffy J, Shlitner A (2000) Peripheral vasoconstriction during REM sleep detected by a new plethysmographic method. Nat Med 6:606

    Article  CAS  PubMed  Google Scholar 

  58. Hamburg NM, Palmisano J, Larson MG, Sullivan LM, Lehman BT, Vasan RS et al (2011) Relation of brachial and digital measures of vascular function in the community: the Framingham heart study. Hypertension 57:390–396

    Article  CAS  PubMed  Google Scholar 

  59. Schnabel RB, Schulz A, Wild PS, Sinning CR, Wilde S, Eleftheriadis M et al (2011) Noninvasive vascular function measurement in the community: cross-sectional relations and comparison of methods. Circ Cardiovasc Imaging 4:371–380

    Article  PubMed  Google Scholar 

  60. Den Ruijter HM, Peters SA, Anderson TJ, Britton AR, Dekker JM, Eijkemans MJ et al (2012) Common carotid intima-media thickness measurements in cardiovascular risk prediction: a meta-analysis. JAMA 308:796–803

    Article  Google Scholar 

  61. Owolabi MO, Agunloye AM, Umeh EO, Akpa OM (2015) Can common carotid intima media thickness serve as an indicator of both cardiovascular phenotype and risk among black Africans? Eur J Prev Cardiol 22:1442–1451

    Article  CAS  PubMed  Google Scholar 

  62. Falcão Mda C, Zírpoli JC, Albuquerque VM, Markman Filho B, Araújo NA, Falcão CA et al (2012) Association of biomarkers with atherosclerosis and risk for coronary artery disease in patients with HIV. Arq Bras Cardiol 99:971–978

    Article  PubMed  Google Scholar 

  63. Hileman CO, Longenecker CT, Carman TL, McComsey GA (2014) C-reactive protein predicts 96-week carotid intima media thickness progression in HIV-infected adults naive to antiretroviral therapy. J Acquir Immune Defic Syndr 65:340–344

    Article  CAS  PubMed  Google Scholar 

  64. Witkowska AM, Borawska MH (2004) Soluble intercellular adhesion molecule-1 (sICAM-1): an overview. Eur Cytokine Netw 15:91–98

    CAS  PubMed  Google Scholar 

  65. Worm SW, Hsue P (2010) Role of biomarkers in predicting CVD risk in the setting of HIV infection? Curr Opin HIV AIDS 5:467–472

    Article  PubMed  Google Scholar 

  66. Fonsatti E, Altomonte M, Coral S, Cattarossi I, Nicotra MR, Gasparollo A et al (1997) Tumour-derived interleukin 1alpha (IL-1alpha) up-regulates the release of soluble intercellular adhesion molecule-1 (sICAM-1) by endothelial cells. Br J Cancer 76:1255–1261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Garton KJ, Gough PJ, Philalay J, Wille PT, Blobel CP, Whitehead RH et al (2003) Stimulated shedding of vascular cell adhesion molecule 1 (VCAM-1) is mediated by tumor necrosis factor-alpha-converting enzyme (ADAM 17). J Biol Chem 278:37459–37464

    Article  CAS  PubMed  Google Scholar 

  68. Teppo AM, von Willebrand E, Honkanen E, Ahonen J, Grönhagen-Riska C (2001) Soluble intercellular adhesion molecule-1 (sICAM-1) after kidney transplantation: the origin and role of urinary sICAM-1? Transplantation 71:1113–1119

    Article  CAS  PubMed  Google Scholar 

  69. Huo Y1, Hafezi-Moghadam A, Ley K (2000) Role of vascular cell adhesion molecule-1 and fibronectin connecting segment-1 in monocyte rolling and adhesion on early atherosclerotic lesions. Circ Res 87:15315–15319

    Article  Google Scholar 

  70. Wung BS, Ni CW, Wang DL (2005) ICAM-1 induction by TNFα and IL-6 is mediated by distinct pathways via Rac in endothelial cells. J Biomed Sci 12:91–101

    Article  CAS  PubMed  Google Scholar 

  71. Roy J, Audette M, Tremblay MJ (2001) Intercellular adhesion molecule-1 (ICAM-1) gene expression in human T cells is regulated by phosphotyrosyl phosphatase activity. Involvement of NF-kappaB, Ets, and palindromic interferon-gamma-responsive element-binding sites. J Biol Chem 276:14553–14561

    Article  CAS  PubMed  Google Scholar 

  72. Miller TL, Somarriba G, Orav EJ, Mendez AJ, Neri D, Schaefer N et al (2010) Biomarkers of vascular dysfunction in children infected with human immunodeficiency virus-1. J Acquir Immune Defic Syndr 55:182–188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Newton K, Dixit VM (2012) Signaling in innate immunity and inflammation. Cold Spring Harb Perspect Biol 4(3):pii: a006049. https://doi.org/10.1101/cshperspect.a006049

    Article  CAS  Google Scholar 

  74. Greve JM, Davis G, Meyer AM, Forte CP, Yost SC, Marlor CW (1989) The major human rhinovirus receptor is ICAM-1. Cell 56:839–847

    Article  CAS  PubMed  Google Scholar 

  75. Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD, Springer TA (1989) A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56:849–853

    Article  CAS  PubMed  Google Scholar 

  76. Berendt AR, McDowall A, Craig AG, Bates PA, Sternberg MJ, Marsh K et al (1992) The binding site on ICAM-1 for Plasmodium falciparum-infected erythrocytes overlaps, but is distinct from, the LFA-1-binding site. Cell 68:71–81

    Article  CAS  PubMed  Google Scholar 

  77. Ockenhouse CF, Betageri R, Springer TA, Staunton DE (1992) Plasmodium falciparum-infected erythrocytes bind ICAM-1 at a site distinct from LFA-1, Mac-1, and human rhinovirus. Cell 68:63–69

    Article  CAS  PubMed  Google Scholar 

  78. Cybulsky MI, Iiyama K, Li H, Zhu S, Chen M, Iiyama M et al (2001) A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest 107:1255–1262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Mason JC, Kapahi P, Haskard DO (1993) Detection of increased levels of circulating intercellular adhesion molecule 1 in some patients with rheumatoid arthritis but not in patients with systemic lupus erythematosus. Lack of correlation with levels of circulating vascular cell adhesion molecule 1. Arthritis Rheum 36:519–527

    Article  CAS  PubMed  Google Scholar 

  80. Nagel T, Resnick N, Atkinson WJ, Dewey CF Jr, Gimbrone MA Jr (1994) Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J Clin Invest 94:885–891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Chappell DC, Varner SE, Nerem RM, Medford RM, Alexander RW (1998) Oscillatory shear stress stimulates adhesion molecule expression in cultured human endothelium. Circ Res 82:532–539

    Article  CAS  PubMed  Google Scholar 

  82. Chiu JJ, Chen LJ, Lee PL, Lee CI, Lo LW, Usami S et al (2003) Shear stress inhibits adhesion molecule expression in vascular endothelial cells induced by coculture with smooth muscle cells. Blood 101:2667–2674

    Article  CAS  PubMed  Google Scholar 

  83. Walpola PL, Gotlieb AI, Cybulsky MI, Langille B (1995) Expression of ICAM-1 and VCAM-1 and monocyte adherence in arteries exposed to altered shear stress. Arterioscler Thromb Vasc Biol 15:2–10

    Article  CAS  PubMed  Google Scholar 

  84. Sampath R, Kukielka GL, Smith CW, Eskin SG, McIntire LV (1995) Shear stress-mediated changes in the expression of leukocyte adhesion receptors on human umbilical vein endothelial cells in vitro. Ann Biomed Eng 23:247–256

    Article  CAS  PubMed  Google Scholar 

  85. Shimizu Y, Shaw S, Graber N, Gopal TV, Horgan KJ, Van Seventer GA et al (1991) Activation-independent binding of human memory T cells to adhesion molecule ELAM-1. Nature 349:799–802

    Article  CAS  PubMed  Google Scholar 

  86. Chiu JJ, Chen LJ, Lee CI, Lee PL, Lee DY, Tsai MC et al (2007) Mechanisms of induction of endothelial cell E-selectin expression by smooth muscle cells and its inhibition by shear stress. Blood 110:519–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Tsukada N, Matsuda M, Miyagi K, Yanagisawa N (1993) Increased levels of intercellular adhesion molecule-1 (ICAM-1) and tumor necrosis factor receptor in the cerebrospinal fluid of patients with multiple sclerosis. Neurology 43:2679–2682

    Article  CAS  PubMed  Google Scholar 

  88. Liu CM, Sheen TS, Ko JY, Shun CT (1999) Circulating intercellular adhesion molecule 1 (ICAM-1), E-selectin and vascular cell adhesion molecule 1 (VCAM-1) in head and neck cancer. Br J Cancer 79:360–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Pizzolo G, Vinante F, Nadali G, Ricetti MM, Morosato L, Marrocchella R et al (1993) ICAM-1 tissue overexpression associated with increased serum levels of its soluble form in Hodgkin’s disease. Br J Haematol 84:161–162

    Article  CAS  PubMed  Google Scholar 

  90. Miller MA, Sagnella GA, Kerry SM, Strazzullo P, Cook DG, Cappuccio FP (2003) Ethnic differences in circulating soluble adhesion molecules: the Wandsworth Heart and Stroke Study. Clin Sci (Lond) 104:591–598

    Article  CAS  Google Scholar 

  91. Nofer JR, Kehrel B, Fobker M, Levkau B, Assmann G, von Eckardstein A (2002) HDL and arteriosclerosis: beyond reverse cholesterol transport. Atherosclerosis 161:1–16

    Article  CAS  PubMed  Google Scholar 

  92. Toth PP (2010) Activation of intracellular signaling systems by high-density lipoproteins. J Clin Lipidol 4:376–381

    Article  PubMed  Google Scholar 

  93. Sadler JE (1998) Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 67:395–424

    Article  CAS  PubMed  Google Scholar 

  94. Jaffe EA, Hoyer LW, Nachman RL (1974) Synthesis of von Willebrand factor by cultured human endothelial cells. Proc Natl Acad Sci U S A 71:1906–1909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Nachman R, Levine R, Jaffe EA (1977) Synthesis of factor VIII antigen by cultured Guinea pig megakaryocytes. J Clin Invest 60:914–921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Felmeden DC, Blann AD, Spencer CG, Beevers DG, Lip GY (2003) A comparison of flow-mediated dilatation and von Willebrand factor as markers of endothelial cell function in health and in hypertension: relationship to cardiovascular risk and effects of treatment: a substudy of the Anglo-Scandinavian Cardiac Outcomes Trial. Blood Coagul Fibrinolysis 14:425–431

    Article  CAS  PubMed  Google Scholar 

  97. Freestone B, Chong AY, Nuttall S, Lip GY (2008) Impaired flow mediated dilatation as evidence of endothelial dysfunction in chronic atrial fibrillation: relationship to plasma von Willebrand factor and soluble E-selectin levels. Thromb Res 122:85–90

    Article  CAS  PubMed  Google Scholar 

  98. Meyer AA, Kundt G, Steiner M, Schuff-Werner P, Kienast W (2006) Impaired flow-mediated vasodilation, carotid artery intima-media thickening, and elevated endothelial plasma markers in obese children: the impact of cardiovascular risk factors. Pediatrics 117:1560–1567

    Article  PubMed  Google Scholar 

  99. Seigneur M, Constans J, Blann A, Renard M, Pellegrin JL, Amiral J et al (1997) Soluble adhesion molecules and endothelial cell damage in HIV infected patients. Thromb Haemost 77:646–649

    Article  CAS  PubMed  Google Scholar 

  100. Sadler JE (1997) Thrombomodulin structure and function. Thromb Haemost 78:392–395

    Article  CAS  PubMed  Google Scholar 

  101. Boffa MC, Karochkine M, Bérard M (1991) Plasma thrombomodulin as a marker of endothelium damage. Nouv Rev Fr Hematol 33:529–530

    CAS  PubMed  Google Scholar 

  102. Ishii H, Uchiyama H, Kazama M (1991) Soluble thrombomodulin antigen in conditioned medium is increased by damage of endothelial cells. Thromb Haemost 65:618–623

    Article  CAS  PubMed  Google Scholar 

  103. Ileri M, Hisar I, Yetkin E, Koşar F, Cehreli S, Korkmaz S et al (2001) Increased levels of plasma thrombomodulin in patients with acute myocardial infarction who had thrombolytic therapy and achieved successful reperfusion. Clin Cardiol 24:377–379

    Article  CAS  PubMed  Google Scholar 

  104. Ware LB, Fang X, Matthay MA (2003) Protein C and thrombomodulin in human acute lung injury. Am J Physiol Lung Cell Mol Physiol 285:L514–L521

    Article  CAS  PubMed  Google Scholar 

  105. Strijbos MH, Rao C, Schmitz PI, Kraan J, Lamers CH, Sleijfer S et al (2008) Correlation between circulating endothelial cell counts and plasma thrombomodulin levels as markers for endothelial damage. Thromb Haemost 100:642–647

    Article  CAS  PubMed  Google Scholar 

  106. Nilsson TK, Hellsten G, Amiral J (1993) Plasma thrombomodulin concentrations in relation to cardiovascular risk factors in a population sample. Blood Coagul Fibrinolysis 4:455–458

    Article  CAS  PubMed  Google Scholar 

  107. Pepys MB, Hirschfield GM (2003) C-reactive protein: a critical update. J Clin Invest 111:1805–1812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Black S, Kushner I, Samols D (2004) C-reactive protein. J Biol Chem 279:48487–48490

    Article  CAS  PubMed  Google Scholar 

  109. Burke AP, Tracy RP, Kolodgie F, Malcom GT, Zieske A, Kutys R et al (2002) Elevated C-reactive protein values and atherosclerosis in sudden coronary death: association with different pathologies. Circulation 105:2019–2023

    Article  CAS  PubMed  Google Scholar 

  110. Jialal I, Devaraj S, Venugopal SK (2004) C-reactive protein: risk marker or mediator in atherothrombosis? Hypertension 44:6–11

    Article  CAS  PubMed  Google Scholar 

  111. Kushner I, Jiang SL, Zhang D, Lozanski G, Samols D (1995) Do post-transcriptional mechanisms participate in induction of C-reactive protein and Serum Amyloid A by IL-6 and IL-1? Ann N Y Acad Sci 762:102–107

    Article  CAS  PubMed  Google Scholar 

  112. Fichtlscherer S, Rosenberger G, Walter DH, Breuer S, Dimmeler S, Zeiher AM (2000) Elevated C-reactive protein levels and impaired endothelial vasoreactivity in patients with coronary artery disease. Circulation 102:1000–1006

    Article  CAS  PubMed  Google Scholar 

  113. Ridker PM, Hennekens CH, Buring JE, Rifai N (2000) C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med 342:836–843

    Article  CAS  PubMed  Google Scholar 

  114. Shikuma CM, Ribaudo HJ (2009) 96-week effects of suppressive efavirenz containing ART, abacavir, and sex on high-sensitivity C-reactive protein: ACTG A5095 [Abstract 736]. Presented at: 16th conference on retroviruses and opportunistic infections. February 8–11, 2009; Montreal, Canada

    Google Scholar 

  115. Neuhaus J, Jacobs DR Jr, Baker JV, Calmy A, Duprez D, La Rosa A et al (2010) Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. J Infect Dis 201:1788–1795

    Article  CAS  PubMed  Google Scholar 

  116. Deshmane SL, Kremlev S, Amini S, Sawaya BE (2009) Monocyte Chemoattractant protein-1 (MCP-1): an overview. J Interf Cytokine Res 29:313–326

    Article  CAS  Google Scholar 

  117. Wang CH, Li SH, Weisel RD, Fedak PW, Dumont AS, Szmitko P et al (2003) C-reactive protein upregulates angiotensin type 1 receptors in vascular smooth muscle. Circulation 107:1783–1790

    Article  CAS  PubMed  Google Scholar 

  118. Febbraio MA, Pedersen BK (2005) Contraction-induced myokine production and release: is skeletal muscle an endocrine organ? Exerc Sport Sci Rev 33:114–119

    Article  PubMed  Google Scholar 

  119. Sprague AH, Khalil RA (2009) Inflammatory cytokines in vascular dysfunction and vascular disease. Biochem Pharmacol 78:539–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Mathew M, Tay E, Cusi K (2010) Elevated plasma free fatty acids increase cardiovascular risk by inducing plasma biomarkers of endothelial activation, myeloperoxidase and PAI-1 in healthy subjects. Cardiovasc Diabetol 9:9. https://doi.org/10.1186/1475-2840-9-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Baker RG, Hayden MS, Ghosh S (2011) NF-κB, inflammation, and metabolic disease. Cell Metab 13:11–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Hedges JC, Singer CA, Gerthoffer WT (2000) Mitogen-activated protein kinases regulate cytokine gene expression in human airway myocytes. Am J Respir Cell Mol Biol 23:86–94

    Article  CAS  PubMed  Google Scholar 

  123. Chu WM (2013) Tumor necrosis factor. Cancer Lett 328:222–225

    Article  CAS  PubMed  Google Scholar 

  124. Signorelli SS, Mazzarino MC, Di Pino L, Malaponte G, Porto C, Pennisi G et al (2003) High circulating levels of cytokines (IL-6 and TNFalpha), adhesion molecules (VCAM-1 and ICAM-1) and selectins in patients with peripheral arterial disease at rest and after a treadmill test. Vasc Med 8:15–19

    Article  PubMed  Google Scholar 

  125. Wang Y, Wang L, Ai X, Zhao J, Hao X, Lu Y et al (2004) Nicotine could augment adhesion molecule expression in human endothelial cells through macrophages secreting TNF-alpha, IL-1beta. Int Immunopharmacol 4:1675–1686

    Article  CAS  PubMed  Google Scholar 

  126. López M, Vispo E, San Román J, Herrero D, Peris A, Corral A et al (2012) Short communication high risk of endothelial dysfunction in HIV individuals may result from deregulation of circulating endothelial cells and endothelial progenitor cells. AIDS Res Hum Retrovir 28:656–659

    Article  PubMed  Google Scholar 

  127. Teofili L, Iachininoto MG, Capodimonti S, Ucciferri C, Nuzzolo ER, Martini M et al (2010) Endothelial progenitor cell trafficking in human immunodeficiency virus-infected persons. AIDS 24:2443–2450

    Article  CAS  PubMed  Google Scholar 

  128. Papasavvas E, Hsue P, Reynolds G, Pistilli M, Hancock A, Martin JN et al (2012) Increased CD34+/KDR+ cells are not associated with carotid artery intima-media thickness progression in chronic HIV-positive subjects. Antivir Ther 17:557–563

    Article  PubMed  Google Scholar 

  129. Costiniuk CT, Hibbert BM, Filion LG, Kovacs CM, Benko E, O'Brien ER et al (2012) Circulating endothelial progenitor cell levels are not reduced in HIV-infected men. J Infect Dis 205:713–717

    Article  CAS  PubMed  Google Scholar 

  130. Heiss C, Keymel S, Niesler U, Ziemann J, Kelm M, Kalka C (2005) Impaired progenitor cell activity in age-related endothelial dysfunction. J Am Coll Cardiol 45:1441–1448

    Article  CAS  PubMed  Google Scholar 

  131. Van Craenenbroeck EM, Beckers PJ, Possemiers NM, Wuyts K, Frederix G, Hoymans VY et al (2010) Exercise acutely reverses dysfunction of circulating angiogenic cells in chronic heart failure. Eur Heart J 31:1924–1934

    Article  PubMed  CAS  Google Scholar 

  132. Makin AJ, Blann AD, Chung NA, Silverman SH, Lip GY (2004) Assessment of endothelial damage in atherosclerotic vascular disease by quantification of circulating endothelial cells. Relationship with von Willebrand factor and tissue factor. Eur Heart J 25:371–376

    Article  CAS  PubMed  Google Scholar 

  133. Chong AY, Blann AD, Patel J, Freestone B, Hughes E, Lip GY (2004) Endothelial dysfunction and damage in congestive heart failure: relation of flow-mediated dilation to circulating endothelial cells, plasma indexes of endothelial damage, and brain natriuretic peptide. Circulation 110:1794–1798

    Article  PubMed  Google Scholar 

  134. Helmke SM, Duncan MW (2007) Measurement of the NO metabolites, nitrite and nitrate, in human biological fluids by GC–MS. J Chromatogr B Analyt Technol Biomed Life Sci 851:83–92

    Article  CAS  PubMed  Google Scholar 

  135. Kelm M, Schrader J (1990) Control of coronary vascular tone by nitric oxide. Circ Res 66:1561–1575

    Article  CAS  PubMed  Google Scholar 

  136. Lomelí O, Pérez-Torres I, Márquez R, Críales S, Mejía AM, Chiney C et al (2018) The evaluation of flow-mediated vasodilation in the brachial artery correlates with endothelial dysfunction evaluated by nitric oxide synthase metabolites in Marfan syndrome patients. Front Physiol 9:965–965

    Article  PubMed  PubMed Central  Google Scholar 

  137. Olson E, Torres R, Levene MJ (2013) Integrated fluorescence correlation spectroscopy device for point-of-care clinical applications. Biomed Opt Express 4:1074–1082

    Article  PubMed  PubMed Central  Google Scholar 

  138. Pandey CM, Augustine S, Kumar S, Kumar S, Nara S, Srivastava S et al (2018) Microfluidics based point-of-care diagnostics. Biotechnol J 13. https://doi.org/10.1002/biot.201700047

  139. Aymong ED, Curtis MJ, Youssef M, Graham MM, Shewchuk L, Leschuk W et al (2002) Abciximab attenuates coronary microvascular endothelial dysfunction after coronary stenting. Circulation 105:2981–2985

    Article  CAS  PubMed  Google Scholar 

  140. Zeiher AM, Drexler H, Wollschläger H, Just H (1991) Endothelial dysfunction of the coronary microvasculature is associated with coronary blood flow regulation in patients with early atherosclerosis. Circulation 84:1984–1992

    Article  CAS  PubMed  Google Scholar 

  141. Mather KJ, Verma S, Anderson TJ (2001) Improved endothelial function with metformin in type 2 diabetes mellitus. J Am Coll Cardiol 37:1344–1350

    Article  CAS  PubMed  Google Scholar 

  142. Verma S, Raj SR, Shewchuk L, Mather KJ, Anderson TJ (2001) Cyclooxygenase-2 blockade does not impair endothelial vasodilator function in healthy volunteers: randomized evaluation of rofecoxib versus naproxen on endothelium-dependent vasodilatation. Circulation 104:2879–2882

    Article  CAS  PubMed  Google Scholar 

  143. Thijssen DH, Black MA, Pyke KE, Padilla J, Atkinson G, Harris RA et al (2011) Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol 300:H2–12

    Article  CAS  PubMed  Google Scholar 

  144. Costa-Hong V, Katayama KY, Consolim-Colombo FM (2018) Methods to investigate endothelial function in humans. In: Endothelium and cardiovascular diseases: vascular biology and clinical syndromes, 1st edn. ISBN-10: 0128123486. Academic Press. https://doi.org/10.1016/B978-0-12-812348-5.00016-7

  145. Fourie CM, Schutte AE, Smith W, Kruger A, van Rooyen JM (2015) Endothelial activation and cardiometabolic profiles of treated and never-treated HIV infected Africans. Atherosclerosis 240:154–160

    Article  CAS  PubMed  Google Scholar 

  146. De Pablo-Bernal RS, Ruiz-Mateos E, Rosado I, Dominguez-Molina B, Alvarez-Ríos AI, Carrillo-Vico A et al (2014) TNF-alpha levels in HIV-infected patients after long-term suppressive cART persist as high as in elderly, HIV-uninfected subjects. J Antimicrob Chemother 69:3041–3046

    Article  PubMed  CAS  Google Scholar 

  147. Sinha A, Ma Y, Scherzer R, Hur S, Li D, Ganz P et al (2016) Role of T-cell dysfunction, inflammation, and coagulation in microvascular disease in HIV. J Am Heart Assoc 5(12). pii: e004243. https://doi.org/10.1161/JAHA.116.004243

  148. Giuliano Ide C, de Freitas SF, de Souza M, Caramelli B (2008) Subclinic atherosclerosis and cardiovascular risk factors in HIV-infected children: PERI study. Coron Artery Dis 19:167–172

    Article  PubMed  Google Scholar 

  149. Mosepele M, Mohammed T, Mupfumi L, Moyo S, Bennett K, Lockman S et al (2018) HIV disease is associated with increased biomarkers of endothelial dysfunction despite viral suppression on long–term antiretroviral therapy in Botswana. Cardiovasc J Afr 29:155–161

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by a Postgraduate Training Fellowship from the Organization for Women in Science for the Developing World (OWSD) and the Swedish International Development Cooperation Agency (SIDA).

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Mezoh, G., Crowther, N.J. (2019). Deciphering Endothelial Dysfunction in the HIV-Infected Population. In: Guest, P. (eds) Reviews on Biomarker Studies of Metabolic and Metabolism-Related Disorders. Advances in Experimental Medicine and Biology(), vol 1134. Springer, Cham. https://doi.org/10.1007/978-3-030-12668-1_11

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