1887

Journal of General Virology header logo

Volume 102, Issue 8

The emerging role of perivascular cells (pericytes) in viral pathogenesis Open Access

Abstract

Viruses may exploit the cardiovascular system to facilitate transmission or within-host dissemination, and the symptoms of many viral diseases stem at least in part from a loss of vascular integrity. The microvascular architecture is comprised of an endothelial cell barrier ensheathed by perivascular cells (pericytes). Pericytes are antigen-presenting cells (APCs) and play crucial roles in angiogenesis and the maintenance of microvascular integrity through complex reciprocal contact-mediated and paracrine crosstalk with endothelial cells. We here review the emerging ways that viruses interact with pericytes and pay consideration to how these interactions influence microvascular function and viral pathogenesis. Major outcomes of virus-pericyte interactions include vascular leakage or haemorrhage, organ tropism facilitated by barrier disruption, including viral penetration of the blood-brain barrier and placenta, as well as inflammatory, neurological, cognitive and developmental sequelae. The underlying pathogenic mechanisms may include direct infection of pericytes, pericyte modulation by secreted viral gene products and/or the dysregulation of paracrine signalling from or to pericytes. Viruses we cover include the herpesvirus human cytomegalovirus (HCMV, ), the retrovirus human immunodeficiency virus (HIV; causative agent of acquired immunodeficiency syndrome, AIDS, and HIV-associated neurocognitive disorder, HAND), the flaviviruses dengue virus (DENV), Japanese encephalitis virus (JEV) and Zika virus (ZIKV), and the coronavirus severe acute respiratory syndrome-related coronavirus 2 (SARS-CoV-2; causative agent of coronavirus disease 2019, COVID-19). We touch on promising pericyte-focussed therapies for treating the diseases caused by these important human pathogens, many of which are emerging viruses or are causing new or long-standing global pandemics.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): blood-brain barrier , COVID-19 , dengue haemorrhage , HIV/AIDS , pericyte and SARS-CoV-2
Funding
This study was supported by the:
  • university global partnership network (ugpn)
    • Principle Award Recipient: PaolaCampagnolo
  • global challenges research fund (gcrf)
    • Principle Award Recipient: PaolaCampagnolo
  • biotechnology and biological sciences research council (Award BBS/E/I/00007034)
    • Principle Award Recipient: KevinMaringer
  • biotechnology and biological sciences research council (Award BBS/E/I/00007030)
    • Principle Award Recipient: KevinMaringer
  • department for international development (Award MR/R010315/1)
    • Principle Award Recipient: KevinMaringer
  • medical research council (Award MR/R010315/1)
    • Principle Award Recipient: KevinMaringer
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001634
2021-08-23
2024-05-08
Loading full text...

Full text loading...

/deliver/fulltext/jgv/102/8/jgv001634.html?itemId=/content/journal/jgv/10.1099/jgv.0.001634&mimeType=html&fmt=ahah

References

  1. Seeherman S, Suzuki YJ. Viral infection and cardiovascular disease: Implications for the molecular basis of COVID-19 pathogenesis. Int J Mol Sci 2021; 22:1659 [View Article] [PubMed]
     [Google Scholar]
  2. Lapenna A, Palma MD, Lewis CE. Perivascular macrophages in health and disease. Nat Rev Immunol 2018; 18:689–702 [View Article] [PubMed]
     [Google Scholar]
  3. Koizumi T, Kerkhofs D, Mizuno T, Steinbusch HWM, Foulquier S. Vessel-associated immune cells in cerebrovascular diseases: From perivascular macrophages to vessel-associated microglia. Front Neurosci 2019; 13:1291 [View Article]
     [Google Scholar]
  4. Crisan M, Yap S, Casteilla L, Chen C-W, Corselli M et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3:301–313 [View Article] [PubMed]
     [Google Scholar]
  5. Hirschi KK, D’Amore PA. Pericytes in the microvasculature. Cardiovasc Res 1996; 32:687–698 [View Article] [PubMed]
     [Google Scholar]
  6. Steinberg BE, Goldenberg NM, Lee WL. Do viral infections mimic bacterial sepsis? The role of microvascular permeability: A review of mechanisms and methods. Antiviral Res 2012; 93:2–15 [View Article] [PubMed]
     [Google Scholar]
  7. Vanlandewijck M, He L, Mäe MA, Andrae J, Ando K. A molecular atlas of cell types and zonation in the brain vasculature. Nature 2018; 554:475–480 [View Article] [PubMed]
     [Google Scholar]
  8. Gaceb A, Paul G. Pericyte biology - novel concepts. Adv Exp Med Biol 2018; 1109:139–163
     [Google Scholar]
  9. Alarcon-Martinez L, Yilmaz-Ozcan S, Yemisci M, Schallek J, Kılıç K et al. Retinal ischemia induces α-SMA-mediated capillary pericyte contraction coincident with perivascular glycogen depletion. Acta Neuropathol Commun 2019; 7:134 [View Article]
     [Google Scholar]
  10. Rustenhoven J, Jansson D, Smyth LC, Dragunow M. Brain pericytes as mediators of neuroinflammation. Trends Pharmacol Sci 2017; 38:291–304 [View Article] [PubMed]
     [Google Scholar]
  11. Avolio E, Alvino VV, Ghorbel MT, Campagnolo P. Perivascular cells and tissue engineering: Current applications and untapped potential. Pharmacology & Therapeutics 2017; 171:83–92 [View Article]
     [Google Scholar]
  12. Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 2011; 21:193–215 [View Article] [PubMed]
     [Google Scholar]
  13. Risau W. Development and differentiation of endothelium. Kidney Int 1998; 54:S3–S6 [View Article]
     [Google Scholar]
  14. Hill J, Rom S, Ramirez SH, Persidsky Y. Emerging Roles of Pericytes in the Regulation of the Neurovascular Unit in Health and Disease. J Neuroimmune Pharmacol 2014; 9:591–605 [View Article]
     [Google Scholar]
  15. Kostallari E, Shah VH. Pericytes in the liver. Adv Exp Med Biol 2019; 1122:153–167 [View Article] [PubMed]
     [Google Scholar]
  16. He L, Vanlandewijck M, Mäe MA, Andrae J, Ando K. Single-cell RNA sequencing of mouse brain and lung vascular and vessel-associated cell types. Sci Data 2018; 5:180160 [View Article] [PubMed]
     [Google Scholar]
  17. Chavkin NW, Hirschi KK. Single cell analysis in vascular biology. Front Cardiovasc Med 2020; 7:42 [View Article]
     [Google Scholar]
  18. Dias Moura Prazeres PH, Sena IFG, Borges I da T, de Azevedo PO, Andreotti JP et al. Pericytes are heterogeneous in their origin within the same tissue. Dev Biol 2017; 427:6–11 [View Article] [PubMed]
     [Google Scholar]
  19. Wang Y, Xu J, Chang L, Meyers CA, Zhang L. Relative contributions of adipose-resident CD146+ pericytes and CD34+ adventitial progenitor cells in bone tissue engineering. npj Regen Med 2019; 4:1 [View Article]
     [Google Scholar]
  20. Bergers G, Song S. The role of pericytes in blood-vessel formation and maintenance. Neuro-oncology 2005; 7:452–464 [View Article] [PubMed]
     [Google Scholar]
  21. Hammes H-P. Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res 2005; 37 Suppl 1:39–43 [PubMed]
     [Google Scholar]
  22. Griffiths P, Baraniak I, Reeves M. The pathogenesis of human cytomegalovirus. J Pathol 2015; 235:288–297 [View Article]
     [Google Scholar]
  23. Alcendor DJ, Charest AM, Zhu WQ, Vigil HE, Knobel SM. Infection and upregulation of proinflammatory cytokines in human brain vascular pericytes by human cytomegalovirus. J Neuroinflamm 2012; 9:95 [View Article]
     [Google Scholar]
  24. Wilkerson I, Laban J, Mitchell JM, Sheibani N, Alcendor DJ. Retinal pericytes and cytomegalovirus infectivity: implications for HCMV-induced retinopathy and congenital ocular disease. J Neuroinflammation 2015; 12:2 [View Article]
     [Google Scholar]
  25. Aronoff DM, Correa H, Rogers LM, Arav‐Boger R, Alcendor DJ. Placental pericytes and cytomegalovirus infectivity: Implications for HCMV placental pathology and congenital disease. Am J Reprod Immunol 2017; 78: [View Article] [PubMed]
     [Google Scholar]
  26. Soland MA, Keyes LR, Bayne R, Moon J, Porada CD. Perivascular stromal cells as a potential reservoir of human cytomegalovirus. Am J Transplant 2014; 14:820–830 [View Article] [PubMed]
     [Google Scholar]
  27. Popik W, Correa H, Khatua A, Aronoff DM, Alcendor DJ. Mesangial cells, specialized renal pericytes and cytomegalovirus infectivity: Implications for HCMV pathology in the glomerular vascular unit and post- transplant renal disease. J Transl Sci 2018; 5: [View Article] [PubMed]
     [Google Scholar]
  28. Sharp PM, Hahn BH. Origins of HIV and the AIDS Pandemic. Csh Perspect Med 2011; 1:a006841
     [Google Scholar]
  29. Clifford DB, Ances BM. HIV-associated neurocognitive disorder. Lancet Infect Dis 2013; 13:976–986 [View Article] [PubMed]
     [Google Scholar]
  30. Illanes-Álvarez F, Márquez-Ruiz D, Márquez-Coello M, Cuesta-Sancho S, Girón-González JA. Similarities and differences between HIV and SARS-CoV-2. Int J Med Sci 2021; 18:846–851 [View Article] [PubMed]
     [Google Scholar]
  31. Persidsky Y, Hill J, Zhang M, Dykstra H, Winfield M et al. Dysfunction of brain pericytes in chronic neuroinflammation. J Cereb Blood Flow Metabolism 2015; 36:794–807
     [Google Scholar]
  32. Rom S, Gajghate S, Winfield M, Reichenbach NL, Persidsky Y. Combination of HIV-1 and diabetes enhances blood brain barrier injury via effects on brain endothelium and pericytes. Int J Mol Sci 2020; 21:4663 [View Article]
     [Google Scholar]
  33. Bohannon DG, Ko A, Filipowicz AR, Kuroda MJ, Kim WK. Dysregulation of sonic hedgehog pathway and pericytes in the brain after lentiviral infection. J Neuroinflammation 2019; 16:86 [View Article]
     [Google Scholar]
  34. Niu F, Yao H, Zhang W, Sutliff RL, Buch S. Tat 101-mediated enhancement of brain pericyte migration involves platelet-derived growth factor subunit B homodimer: Implications for human immunodeficiency virus-associated neurocognitive disorders. J Neurosci 2014; 34:11812–11825 [View Article] [PubMed]
     [Google Scholar]
  35. Cho HJ, Kuo AM-S, Bertrand L, Toborek M. HIV alters gap junction-mediated intercellular communication in human brain pericytes. Front Mol Neurosci 2017; 10:410 [View Article] [PubMed]
     [Google Scholar]
  36. Torices S, Roberts SA, Park M, Malhotra A, Toborek M. Occludin, caveolin‐1, and Alix form a multi‐protein complex and regulate HIV‐1 infection of brain pericytes. Faseb J 2020; 34:16319–16332 [View Article] [PubMed]
     [Google Scholar]
  37. Nakagawa S, Castro V, Toborek M. Infection of human pericytes by HIV‐1 disrupts the integrity of the blood–brain barrier. J Cell Mol Med 2012; 16:2950–2957 [View Article] [PubMed]
     [Google Scholar]
  38. Castro V, Bertrand L, Luethen M, Dabrowski S, Lombardi J. Occludin controls HIV transcription in brain pericytes via regulation of SIRT‐1 activation. Faseb J 2016; 30:1234–1246 [View Article] [PubMed]
     [Google Scholar]
  39. Dohgu S, Banks WA. Brain pericytes increase the lipopolysaccharide-enhanced transcytosis of HIV-1 free virus across the in vitro blood–brain barrier: evidence for cytokine-mediated pericyte-endothelial cell crosstalk. Fluids Barriers Cns 2013; 10:23 [View Article] [PubMed]
     [Google Scholar]
  40. Banks WA, Freed EO, Wolf KM, Robinson SM, Franko M et al. Transport of human immunodeficiency virus type 1 pseudoviruses across the blood-brain barrier: Role of envelope proteins and adsorptive endocytosis. J Virol 2001; 75:4681–4691 [View Article] [PubMed]
     [Google Scholar]
  41. Persidsky Y, Stins M, Way D, Witte MH, Weinand M et al. A model for monocyte migration through the blood-brain barrier during HIV-1 encephalitis. J Immunol Baltim Md 1950 1997; 158:3499–3510
     [Google Scholar]
  42. Nottet HS, Persidsky Y, Sasseville VG, Nukuna AN, Bock P et al. Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. J Immunol Baltim Md 1950 1996; 156:1284–1295
     [Google Scholar]
  43. Stephenson SE, Wilson CL, Bond NG, Kaur A, Alvarez X et al. Pericytes as novel targets for HIV/SIV infection in the lung. Am J Physiol-lung C 2020; 319:L848–L853 [View Article]
     [Google Scholar]
  44. Weaver SC, Charlier C, Vasilakis N, Zika LM. Chikungunya, and other emerging vector-borne viral diseases. Annu Rev Med 2017; 69:395–408 [View Article] [PubMed]
     [Google Scholar]
  45. Gatherer D, Kohl A. Zika virus: a previously slow pandemic spreads rapidly through the Americas. J Gen Virol 2016; 97:269–273 [View Article] [PubMed]
     [Google Scholar]
  46. Kim J, Alejandro B, Hetman M, Hattab EM, Joiner J et al. Zika virus infects pericytes in the choroid plexus and enters the central nervous system through the blood-cerebrospinal fluid barrier. Plos Pathog 2020; 16:e1008204
     [Google Scholar]
  47. Roach T, Alcendor DJ. Zika virus infection of cellular components of the blood-retinal barriers: implications for viral associated congenital ocular disease. J Neuroinflammation 2017; 14:43 [View Article]
     [Google Scholar]
  48. Kumar A, Sharma P, Shukla KK, Misra S, Nyati KK. Japanese encephalitis virus: Associated immune response and recent progress in vaccine development. Microbial Pathogenesis 2019; 136:103678 [View Article]
     [Google Scholar]
  49. Chang C-Y, Li J-R, Ou Y-C, Lin S-Y, Wang Y-Y et al. Interplay of inflammatory gene expression in pericytes following Japanese encephalitis virus infection. Brain Behav Immun 2017; 66:230–243 [View Article] [PubMed]
     [Google Scholar]
  50. Zhou M, Wang S, Guo J, Liu Y, Cao J et al. RNAI screening reveals requirement for pdgfrβ in JEV infection. Antimicrob Agents Ch 2021 [View Article]
     [Google Scholar]
  51. Zhou P, Yang X-L, Wang X-G, Hu B, Zhang L et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 2020; 579:270–273 [View Article] [PubMed]
     [Google Scholar]
  52. Guzik TJ, Mohiddin SA, Dimarco A, Patel V, Savvatis K. COVID-19 and the cardiovascular system: implications for risk assessment, diagnosis, and treatment options. Cardiovasc Res 2020; 116:1666–1687 [View Article] [PubMed]
     [Google Scholar]
  53. Brann DH, Tsukahara T, Weinreb C, Lipovsek M, den BK. Non-neuronal expression of SARS-CoV-2 entry genes in the olfaory system suggests mechanisms underlying COVID-19-associated anosmia. Sci Adv 2020; 6:eabc5801 [View Article] [PubMed]
     [Google Scholar]
  54. Chen L, Li X, Chen M, Feng Y, Xiong C. The ACE2 expression in human heart indicates new potential mechanism of heart injury among patients infected with SARS-CoV-2. Cardiovasc Res 2020; 116:1097–1100 [View Article] [PubMed]
     [Google Scholar]
  55. Nicin L, Abplanalp WT, Mellentin H, Kattih B, Tombor L. Cell type-specific expression of the putative SARS-CoV-2 receptor ACE2 in human hearts. Eur Heart J 2020; 41:1804–1806 [View Article] [PubMed]
     [Google Scholar]
  56. Tucker NR, Chaffin M, Bedi KC, Papangeli I, Akkad A-D et al. Myocyte-specific upregulation of ACE2 in cardiovascular disease: Implications for SARS-CoV-2-mediated myocarditis. Circulation 2020; 142:708–710 [View Article] [PubMed]
     [Google Scholar]
  57. Avolio E, Gamez M, Gupta K, Foster R, Berger I et al. The SARS-CoV-2 spike protein disrupts the cooperative function of human cardiac pericytes - endothelial cells through CD147 receptor-mediated signalling: a potential non-infective mechanism of COVID-19 microvascular disease. Biorxiv 2020; 2020:12.21.423721
     [Google Scholar]
  58. Cardot-Leccia N, Hubiche T, Dellamonica J, Burel-Vandenbos F, Passeron T. Pericyte alteration sheds light on micro-vasculopathy in COVID-19 infection. Intensive Care Med 2020; 46:1777–1778 [View Article]
     [Google Scholar]
  59. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW. The global distribution and burden of dengue. Nature 2013; 496:504–507 [View Article] [PubMed]
     [Google Scholar]
  60. Rastogi M, Sharma N, Singh SK. Flavivirus NS1: a multifaceted enigmatic viral protein. Virol J 2016; 13:131 [View Article] [PubMed]
     [Google Scholar]
  61. Malavige GN, Ogg GS. Pathogenesis of vascular leak in dengue virus infection. Immunology 2017; 151:261–269 [View Article] [PubMed]
     [Google Scholar]
  62. Beatty PR, Puerta-Guardo H, Killingbeck SS, Glasner DR, Hopkins K et al. Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination. Sci Transl Med 2015; 7:304ra141 [View Article] [PubMed]
     [Google Scholar]
  63. Puerta-Guardo H, Glasner DR, Espinosa DA, Biering SB, Patana M et al. Flavivirus NS1 triggers tissue-specific vascular endothelial dysfunction reflecting disease tropism. Cell Rep 2019; 26:1598–1613 [View Article] [PubMed]
     [Google Scholar]
  64. Cheung YP, Mastrullo V, Maselli D, Butsabong T, Madeddu P et al. A critical role for perivascular cells in amplifying vascular leakage induced by dengue virus nonstructural protein 1. mSphere 2020; 5:e00258-20 [View Article] [PubMed]
     [Google Scholar]
  65. Yu X, Ye F. Role of angiopoietins in development of cancer and neoplasia associated with viral infection. Cells 2020; 9:457 [View Article]
     [Google Scholar]
  66. Ruszczak Zb, Silva A-D, Orfanos CE. Kaposi’s sarcoma in AIDS. Am J Dermatopathol 1987; 9:388–398
     [Google Scholar]
  67. Carotti S, Morini S, Corradini SG, Burza MA, Molinaro A. Glial fibrillary acidic protein as an early marker of hepatic stellate cell activation in chronic and posttransplant recurrent hepatitis C. Liver Transpl 2008; 14:806–814 [View Article]
     [Google Scholar]
  68. Mapalagamage M, Handunnetti SM, Wickremasinghe AR, Premawansa G, Thillainathan S et al. High levels of serum angiopoietin 2 and angiopoietin 2/1 ratio at the critical stage of dengue hemorrhagic fever in patients and association with clinical and biochemical parameters. J Clin Microbiol 2020; 58:e00436-19 [View Article] [PubMed]
     [Google Scholar]
  69. Michels M, van der Ven AJAM, Djamiatun K, Fijnheer R, de Groot PG et al. Imbalance of angiopoietin-1 and angiopoetin-2 in severe dengue and relationship with thrombocytopenia, endothelial activation, and vascular stability. Am J Trop Med Hyg 2012; 87:943–946 [View Article]
     [Google Scholar]
  70. Mariko R, Darwin E, Yanwirasti Y, Hadinegoro SR. The difference of angiopoietin-2 levels between dengue hemorrhagic fever patients with shock and without shock. Open Access Maced J Med Sci 2019; 7:2119–2122
     [Google Scholar]
  71. Ong SP, ML N, JJH C. Differential regulation of angiopoietin 1 and angiopoietin 2 during dengue virus infection of human umbilical vein endothelial cells: implications for endothelial hyperpermeability. Med Microbiol Immunol 2013; 202:437–452 [View Article]
     [Google Scholar]
  72. Singh S, Anupriya MG, Modak A, Sreekumar E. Dengue virus or NS1 protein induces trans-endothelial cell permeability associated with VE-Cadherin and RhoA phosphorylation in HMEC-1 cells preventable by Angiopoietin-1. J Gen Virol 2018; 99:1658–1670 [View Article] [PubMed]
     [Google Scholar]
  73. Her Z, Kam YW, Gan VC, Lee B, Thein TL et al. Severity of plasma leakage is associated with high levels of interferon γ-inducible protein 10, hepatocyte growth factor, Matrix Metalloproteinase 2 (MMP-2), and MMP-9 during dengue virus infection. J Infect Dis 2017; 215:42–51 [PubMed]
     [Google Scholar]
  74. Lum F-M, Lye DCB, Tan JJL, Lee B, Chia P-Y et al. Longitudinal study of cellular and systemic cytokine signatures to define the dynamics of a balanced immune environment during disease manifestation in zika virus-infected patients. J Infect Dis 2018; 218:814–824 [View Article] [PubMed]
     [Google Scholar]
  75. Dhillon NK, Li F, Xue B, Tawfik O, Morgello S et al. Effect of cocaine on human immunodeficiency virus-mediated pulmonary endothelial and smooth muscle dysfunction. Am J Respir Cell Mol Biol 2011; 45:40–52 [View Article]
     [Google Scholar]
  76. Graham SM, Rajwans N, Tapia KA, Jaoko W, Estambale BB. A prospective study of endothelial activation biomarkers, including plasma angiopoietin-1 and angiopoietin-2, in Kenyan women initiating antiretroviral therapy. Bmc Infect Dis 2013; 13:263 [View Article] [PubMed]
     [Google Scholar]
  77. Gulhati V, Soo J, Ransy DG, Brophy J, Kakkar F et al. Brief report: Higher levels of angiopoietin-1 are associated with early and sustained viral suppression in children living with vertically acquired HIV. Jaids J Acquir Immune Defic Syndromes 2019; 80:590–595 [View Article]
     [Google Scholar]
  78. Gustafsson RKL, Jeffery HC, Yaiw K-C, Wilhelmi V, Kostopoulou ON et al. Direct infection of primary endothelial cells with human cytomegalovirus prevents angiogenesis and migration. J Gen Virol 2015; 96:3598–3612 [View Article] [PubMed]
     [Google Scholar]
  79. Reinhardt B, Mertens T, Mayr-Beyrle U, Frank H, Lüske A. HCMV infection of human vascular smooth muscle cells leads to enhanced expression of functionally intact PDGF β-receptor. Cardiovasc Res 2005; 67:151–160 [View Article] [PubMed]
     [Google Scholar]
  80. Teuwen LA, Geldhof V, Pasut A, Carmeliet P. Covid-19: The vasculature unleashed. Nat Rev Immunol 2020; 20:389–391 [View Article] [PubMed]
     [Google Scholar]
  81. Smadja DM, Guerin CL, Chocron R, Yatim N, Boussier J. Angiopoietin-2 as a marker of endothelial activation is a good predictor factor for intensive care unit admission of COVID-19 patients. Angiogenesis 2020; 23:611–620 [View Article] [PubMed]
     [Google Scholar]
  82. Fosse JH, Haraldsen G, Falk K, Edelmann R. Endothelial cells in emerging viral infections. Front Cardiovasc Med 2021; 8:619690 [View Article]
     [Google Scholar]
  83. Malik S, Khalique H, Buch S, Seth P. A growth factor attenuates HIV-1 tat and morphine induced damage to human neurons: Implication in hiv/aids-drug abuse cases. PLoS One 2011; 6:e18116 [View Article] [PubMed]
     [Google Scholar]
  84. Yao H, Duan M, Yang L, Buch S. Platelet-derived growth factor-BB restores human immunodeficiency virus Tat-cocaine-mediated impairment of neurogenesis: role of TRPC1 channels. J Neurosci 2012; 32:9835–9847 [View Article] [PubMed]
     [Google Scholar]
  85. Peng F, Dhillon NK, Yao H, Zhu X, Williams R. Mechanisms of platelet‐derived growth factor‐mediated neuroprotection – implications in HIV dementia. Eur J Neurosci 2008; 28:1255–1264 [View Article] [PubMed]
     [Google Scholar]
  86. Peng F, Dhillon N, Callen S, Yao H, Bokhari S. Platelet-derived growth factor protects neurons against gp120-mediated toxicity. J Neurovirol 2008; 14:62–72 [View Article] [PubMed]
     [Google Scholar]
  87. Yang L, Chen X, Hu G, Cai Y, Liao K et al. Mechanisms of platelet-derived Growth Factor-bb in restoring HIV tat-cocaine-mediated impairment of neuronal differentiation. Mol Neurobiol 2016; 53:6377–6387 [View Article] [PubMed]
     [Google Scholar]
  88. Chao J, Yang L, Yao H, Buch S. Platelet-Derived growth Factor-BB restores HIV tat -mediated impairment of neurogenesis: role of GSK-3β/β-Catenin. J Neuroimmune Pharmacol 2014; 9:259–268 [View Article]
     [Google Scholar]
  89. Bayer P, Kraft M, Ejchart A, Westendorp M, Frank R. Structural studies of HIV-1 tat protein. J Mol Biol 1995; 247:529–535 [View Article] [PubMed]
     [Google Scholar]
  90. Sehnal D, Rose AS, Koca J, Burley SK, Velankar S. Mol*: Towards a common library and tools for web molecular graphics. EuroVis Proceedings 2018 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001634
Loading
The emerging role of perivascular cells (pericytes) in viral pathogenesis
J. Gen. Virol. 102, 001634 (2021); https://doi.org/10.1099/jgv.0.001634
/content/journal/jgv/10.1099/jgv.0.001634
/content/journal/jgv/10.1099/jgv.0.001634
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error