Dysfunction of brain pericytes in chronic neuroinflammation

Journal of Cerebral Blood Flow and Metabolism

Volumn 36, Issue 4, 2015, Pages 794-807

  Persidsky, Yuri ^a   Hill, Jeremy ^a   Zhang, Ming ^a   Dykstra, Holly ^a   Winfield, Malika ^a   Reichenbach, Nancy L ^a   Potula, Raghava ^a   Mukherjee, Abir ^a   Ramirez, Servio H ^a   Rom, Slava ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

blood brain barrier; HIV 1; monocyte; neuroinflammation; Pericyte

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ALPHA1 INTEGRIN; ANGIOPOIETIN 1; ANTIRETROVIRUS AGENT; CELL ADHESION MOLECULE; INTERLEUKIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; CHEMOKINE; CYTOKINE;

ADULT; ANIMAL CELL; ANTIVIRAL THERAPY; ARTICLE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BRAIN DYSFUNCTION; BRAIN PERICYTE; CELL ADHESION; CHRONIC INFLAMMATION; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; IN VITRO STUDY; MALE; MONOCYTE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; WESTERN BLOTTING; BIOSYNTHESIS; BRAIN; CHRONIC DISEASE; GENETICS; METABOLISM; MIDDLE AGED; NEURITIS; PATHOLOGY; PERICYTE; PRIMARY CELL CULTURE;

ADULT; BASEMENT MEMBRANE; BLOOD-BRAIN BARRIER; BRAIN; CELL ADHESION; CHEMOKINES; CHRONIC DISEASE; CYTOKINES; ENDOTHELIAL CELLS; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; MALE; MIDDLE AGED; MONOCYTES; NEURITIS; PERICYTES; PRIMARY CELL CULTURE; RNA, MESSENGER;

EID: 84962439520     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1177/0271678X15606149     Document Type: Article

References (40)

1. Letendre SL, Zheng JC, Kaul M, et al. Chemokines in cerebrospinal fluid correlate with cerebral metabolite patterns in HIV-infected individuals. J Neurovirol 2011; 17: 63-69.
2. Andras IE, Pu H, Tian J, et al. Signaling mechanisms of HIV-1 Tat-induced alterations of claudin-5 expression in brain endothelial cells. J Cereb Blood Flow Metab 2005; 25: 1159-1170.
3. Persidsky Y, Ramirez SH, Haorah J, et al. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 2006; 1: 223-236.
4. Armulik A, Genove G, Mae M, et al. Pericytes regulate the blood-brain barrier. Nature 2010; 468: 557-561.
5. Bell RD, Winkler EA, Sagare AP, et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 2010; 68: 409-427.
6. Aguilera KY and Brekken RA. Recruitment and retention: factors that affect pericyte migration. Cell Mol Life Sci 2013; 71: 299-309.
7. Hall CN, Reynell C, Gesslein B, et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 2014; 508: 55-60.
8. Winkler EA, Bell RD and Zlokovic BV. Central nervous system pericytes in health and disease. Nat Neurosci 2011; 14: 1398-1405.
9. Wang S, Cao C, Chen Z, et al. Pericytes regulate vascular basement membrane remodeling and govern neutrophil extravasation during inflammation. PLoS ONE 2012; 7: e45499.
10. Stark K, Eckart A, Haidari S, et al. Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct' them with pattern-recognition and motility programs. Nat Immunol 2013; 14: 41-51.
11. Nehme A and Edelman J. Dexamethasone inhibits high glucose-, TNF-alpha-, and IL-1beta-induced secretion of inflammatory and angiogenic mediators from retinal microvascular pericytes. Invest Ophthalmol Vis Sci 2008; 49: 2030-2038.
12. Tigges U, Boroujerdi A, Welser-Alves JV, et al. TNFalpha promotes cerebral pericyte remodeling in vitro, via a switch from alpha1 to alpha2 integrins. J Neuroinflammation 2013; 10: 33.
13. Hill J, Rom S, Ramirez SH, et al. Emerging roles of pericytes in the regulation of the neurovascular unit in health and disease. J Neuroimmune Pharmacol 2014; 9: 591-605.
14. Sengillo JD, Winkler EA, Walker CT, et al. Deficiency in mural vascular cells coincides with blood-brain barrier disruption in Alzheimer's disease. Brain Pathol 2012; 23: 303-310.
15. Winkler EA, Sengillo JD, Sullivan JS, et al. Blood-spinal cord barrier breakdown and pericyte reductions in amyotrophic lateral sclerosis. Acta Neuropathol 2013; 125: 111-120.
16. Vates GE, Takano T, Zlokovic B, et al. Pericyte constriction after stroke: the jury is still out. Nat Med 2010; 16: 959author reply 960.
17. Rom S, Zuluaga-Ramirez V, Dykstra H, et al. Poly(ADP-ribose) polymerase-1 inhibition in brain endothelium protects the blood-brain barrier under physiologic and neuroinflammatory conditions. J Cerebr Blood Flow Metabol 2015; 35: 28-36.
18. Vermeire J, Naessens E, Vanderstraeten H, et al. Quantification of reverse transcriptase activity by real-time PCR as a fast and accurate method for titration of HIV, lenti- and retroviral vectors. PLoS ONE 2012; 7: e50859.
19. Guijarro-Munoz I, Cuesta AM, Alvarez-Cienfuegos A, et al. The axonal repellent Slit2 inhibits pericyte migration: potential implications in angiogenesis. Exp Cell Res 2012; 318: 371-378.
20. Rom S, Fan S, Reichenbach N, et al. Glycogen synthase kinase 3beta inhibition prevents monocyte migration across brain endothelial cells via Rac1-GTPase suppression and down-regulation of active integrin conformation. Am J Pathol 2012; 181: 1414-1425.
21. Krueger M and Bechmann I. CNS pericytes: concepts, misconceptions, and a way out. Glia 2010; 58: 1-10.
22. Niu F, Yao H, ZhangW, et al. 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.
23. Daneman R, Zhou L, Kebede AA, et al. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 2010; 468: 562-566.
24. Ayres-Sander CE, Lauridsen H, Maier CL, et al. Transendothelial migration enables subsequent transmigration of neutrophils through underlying pericytes. PLoS ONE 2013; 8: e60025.
25. Balabanov R, Beaumont T and Dore-Duffy P. Role of central nervous system microvascular pericytes in activation of antigen-primed splenic T-lymphocytes. J Neurosci Res 1999; 55: 578-587.
26. Verbeek MM, Westphal JR, Ruiter DJ, et al. T lymphocyte adhesion to human brain pericytes is mediated via very late antigen-4/vascular cell adhesion molecule-1 interactions. J Immunol 1995; 154: 5876-5884.
27. Bonkowski D, Katyshev V, Balabanov RD, et al. The CNS microvascular pericyte: pericyte-astrocyte crosstalk in the regulation of tissue survival. Fluids Barriers CNS 2011; 8: 8.
28. Nakagawa S, Castro V and 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.
29. Dohgu S and 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.
30. Zhong Y, Zhang B, Eum SY, et al. HIV-1 Tat triggers nuclear localization of ZO-1 via Rho signaling and cAMP response element-binding protein activation. J Neurosci 2012; 32: 143-150.
31. Murakami M. Signaling required for blood vessel maintenance: molecular basis and pathological manifestations. Int J Vasc Med 2012; 2012: 293641.
32. Thanabalasundaram G, Schneidewind J, Pieper C, et al. The impact of pericytes on the blood-brain barrier integrity depends critically on the pericyte differentiation stage. Int J Biochem Cell Biol 2011; 43: 1284-1293.
33. Hill RA, Tong L, Yuan P, et al. Regional blood flow in the normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron 2015; 87: 95-110.
34. Gaengel K, Genove G, Armulik A, et al. Endothelialmural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol 2009; 29: 630-638.
35. Quaegebeur A, Lange C and Carmeliet P. The neurovascular link in health and disease: molecular mechanisms and therapeutic implications. Neuron 2011; 71: 406-424.
36. Abraham S, Kogata N, Fassler R, et al. Integrin beta1 subunit controls mural cell adhesion, spreading, and blood vessel wall stability. Circ Res 2008; 102: 562-570.
37. Towgood KJ, Pitkanen M, Kulasegaram R, et al. Regional cerebral blood flow and FDG uptake in asymptomatic HIV-1 men. Hum Brain Mapp 2013; 34: 2484-2493.
38. Graham SM, Rajwans N, Tapia KA, et al. 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.
39. Fiedler U and Augustin HG. Angiopoietins: a link between angiogenesis and inflammation. Trends Immunol 2006; 27: 552-528.
40. Yao H, Bethel-Brown C, Niu F, et al. Yin and Yang of PDGF-mediated signaling pathway in the context of HIV infection and drug abuse. J Neuroimmune Pharmacol 2013; 9: 161-167.