Hypoxia-inducible factor-1 α/platelet derived growth factor axis in HIV-associated pulmonary vascular remodeling

Respiratory Research

Volumn 12, Issue , 2011, Pages

  Mermis, Joel ^a   Gu, Haihua ^a   Xue, Bing ^a   Li, Fang ^a,d   Tawfik, Ossama ^a   Buch, Shilpa ^b   Bartolome, Sonja ^c   O'Brien Ladner, Amy ^a   Dhillon, Navneet K ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^c Department of Medicine ^*  (United States)

^d AFFILIATED HOSPITAL OF NINGXIA MEDICAL UNIVERSITY   (China)

Author keywords

Endothelial cells; Gp 120; Lungs; Oxidative stress

Indexed keywords

ANTIOXIDANT; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BB; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HIF1A PROTEIN, HUMAN; HIF1A PROTEIN, RAT; PLATELET-DERIVED GROWTH FACTOR BB;

ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL WALL THICKENING; ARTERY ENDOTHELIUM; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; GENETIC TRANSFECTION; HEART LEFT VENTRICLE; HEART RIGHT VENTRICLE; HEART VENTRICLE SEPTUM; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; LUNG BLOOD VESSEL; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RAT; TRANSGENIC RAT; UPREGULATION; WESTERN BLOTTING; WILD TYPE; ANIMAL; CELL CULTURE; DISEASE MODEL; DRUG EFFECT; ENZYMOLOGY; GENETICS; HEART RIGHT VENTRICLE HYPERTROPHY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LUNG; METABOLISM; MICROVASCULATURE; PATHOGENICITY; PULMONARY ARTERY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TIME; VASCULARIZATION; VIROLOGY;

ANIMALS; ANTIOXIDANTS; BLOTTING, WESTERN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HIV-1; HUMANS; HYPERTENSION, PULMONARY; HYPERTROPHY, RIGHT VENTRICULAR; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUNG; MICROVESSELS; OXIDATIVE STRESS; PLATELET-DERIVED GROWTH FACTOR; PULMONARY ARTERY; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, MESSENGER; SIGNAL TRANSDUCTION; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TIME FACTORS; TRANSFECTION; UP-REGULATION;

EID: 79961110896     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-12-103     Document Type: Article

References (64)

1. Humbert M, Montani D, Perros F, Dorfmuller P, Adnot S, Eddahibi S. Endothelial cell dysfunction and cross talk between endothelium and smooth muscle cells in pulmonary arterial hypertension. Vascul Pharmacol 2008, 49(4-6):113-118. 10.1016/j.vph.2008.06.003, 18606248.
2. Humbert M. Mediators involved in HIV-related pulmonary arterial hypertension. Aids 2008, 22(Suppl 3):S41-47. 10.1097/01.aids.0000327515.55041.da, 19033754.
3. Degano B, Guillaume M, Savale L, Montani D, Jais X, Yaici A, Le Pavec J, Humbert M, Simonneau G, Sitbon O. HIV-associated pulmonary arterial hypertension: survival and prognostic factors in the modern therapeutic era. Aids 24(1):67-75.
4. Mette SA, Palevsky HI, Pietra GG, Williams TM, Bruder E, Prestipino AJ, Patrick AM, Wirth JA. Primary pulmonary hypertension in association with human immunodeficiency virus infection. A possible viral etiology for some forms of hypertensive pulmonary arteriopathy. Am Rev Respir Dis 1992, 145(5):1196-1200.
5. Kanmogne GD, Kennedy RC, Grammas P. Analysis of human lung endothelial cells for susceptibility to HIV type 1 infection, coreceptor expression, and cytotoxicity of gp120 protein. AIDS Res Hum Retroviruses 2001, 17(1):45-53. 10.1089/088922201750056771, 11177382.
6. Klings ES, Farber HW. The pathogenesis of HIV-associated pulmonary hypertension. Adv Cardiol 2003, 40:71-82.
7. Pellicelli AM, D'Ambrosio C, Vizza CD, Borgia MC, Tanzi P, Pino P, Zachara E, Soccorsi F. HIV-related pulmonary hypertension. From pathogenesis to clinical aspects. Acta Cardiol 2004, 59(3):323-330. 10.2143/AC.59.3.2005190, 15255466.
8. Marecki JC, Cool CD, Parr JE, Beckey VE, Luciw PA, Tarantal AF, Carville A, Shannon RP, Cota-Gomez A, Tuder RM, et al. HIV-1 Nef is associated with complex pulmonary vascular lesions in SHIV-nef-infected macaques. Am J Respir Crit Care Med 2006, 174(4):437-445. 10.1164/rccm.200601-005OC, 2648120, 16728715.
9. Kanmogne GD, Primeaux C, Grammas P. Induction of apoptosis and endothelin-1 secretion in primary human lung endothelial cells by HIV-1 gp120 proteins. Biochem Biophys Res Commun 2005, 333(4):1107-1115. 10.1016/j.bbrc.2005.05.198, 15979050.
10. Pellicelli AM, Palmieri F, Cicalini S, Petrosillo N. Pathogenesis of HIV-related pulmonary hypertension. AnnNYAcadSci 2001, 946:82-94.
11. Humbert M, Monti G, Brenot F, Sitbon O, Portier A, Grangeot-Keros L, Duroux P, Galanaud P, Simonneau G, Emilie D. Increased interleukin-1 and interleukin-6 serum concentrations in severe primary pulmonary hypertension. Am J Respir Crit Care Med 1995, 151(5):1628-1631.
12. Humbert M, Monti G, Fartoukh M, Magnan A, Brenot F, Rain B, Capron F, Galanaud P, Duroux P, Simonneau G, et al. Platelet-derived growth factor expression in primary pulmonary hypertension: comparison of HIV seropositive and HIV seronegative patients. EurRespirJ 1998, 11(3):554-559.
13. Perros F, Montani D, Dorfmuller P, Durand-Gasselin I, Tcherakian C, Le Pavec J, Mazmanian M, Fadel E, Mussot S, Mercier O, et al. Platelet-derived growth factor expression and function in idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med 2008, 178(1):81-88. 10.1164/rccm.200707-1037OC, 18420966.
14. Balabanian K, Foussat A, Dorfmuller P, Durand-Gasselin I, Capel F, Bouchet-Delbos L, Portier A, Marfaing-Koka A, Krzysiek R, Rimaniol AC, et al. CX(3)C chemokine fractalkine in pulmonary arterial hypertension. Am J Respir Crit Care Med 2002, 165(10):1419-1425. 10.1164/rccm.2106007, 12016106.
15. Dorfmuller P, Zarka V, Durand-Gasselin I, Monti G, Balabanian K, Garcia G, Capron F, Coulomb-Lhermine A, Marfaing-Koka A, Simonneau G, et al. Chemokine RANTES in severe pulmonary arterial hypertension. Am J Respir Crit Care Med 2002, 165(4):534-539.
16. Dhillon NK, Sui Y, Pinson D, Li S, Dhillon S, Tawfik O, Callen S, Nemon O, Narayan O, Buch S. Upregulation of expression of platelet-derived growth factor and its receptor in pneumonia associated with SHIV-infected macaques. AIDS 2007, 21(3):307-316. 10.1097/QAD.0b013e328012c35a, 17255737.
17. Park IW, Ullrich CK, Schoenberger E, Ganju RK, Groopman JE. HIV-1 Tat induces microvascular endothelial apoptosis through caspase activation. J Immunol 2001, 167(5):2766-2771.
18. Voelkel NF, Cool CD, Flores S. From viral infection to pulmonary arterial hypertension: a role for viral proteins?. Aids 2008, 22(Suppl 3):S49-53. 10.1097/01.aids.0000327516.55041.01, 18845922.
19. Balasubramaniam V, Le Cras TD, Ivy DD, Grover TR, Kinsella JP, Abman SH. Role of platelet-derived growth factor in vascular remodeling during pulmonary hypertension in the ovine fetus. Am J Physiol Lung Cell Mol Physiol 2003, 284(5):L826-833.
20. Fukuda N, Kishioka H, Satoh C, Nakayama T, Watanabe Y, Soma M, Izumi Y, Kanmatsuse K. Role of long-form PDGF A-chain in the growth of vascular smooth muscle cells from spontaneously hypertensive rats. Am J Hypertens 1997, 10(10 Pt 1):1117-1124.
21. Ghofrani HA, Seeger W, Grimminger F. Imatinib for the treatment of pulmonary arterial hypertension. N Engl J Med 2005, 353(13):1412-1413. 10.1056/NEJMc051946, 16192491.
22. Patterson KC, Weissmann A, Ahmadi T, Farber HW. Imatinib mesylate in the treatment of refractory idiopathic pulmonary arterial hypertension. Ann Intern Med 2006, 145(2):152-153.
23. Souza R, Sitbon O, Parent F, Simonneau G, Humbert M. Long term imatinib treatment in pulmonary arterial hypertension. Thorax 2006, 61(8):736. 2104679, 16877696.
24. Ghofrani HA, Morrell NW, Hoeper MM, Olschewski H, Peacock AJ, Barst RJ, Shapiro S, Golpon H, Toshner M, Grimminger F, et al. Imatinib in pulmonary arterial hypertension patients with inadequate response to established therapy. Am J Respir Crit Care Med 2010, 182(9):1171-1177. 10.1164/rccm.201001-0123OC, 3001259, 20581169.
25. Potula R, Dhillion N, Sui Y, Zien CA, Funa K, Pinson D, Mayo MS, Singh DK, Narayan O, Buch S. Association of platelet-derived growth factor-B chain with simian human immunodeficiency virus encephalitis. AmJPathol 2004, 165(3):815-824.
26. Dhillon NK, Li F, Xue B, Tawfik O, Morgello S, Buch S, O'Brien Ladner A. Effect of Cocaine on HIV-mediated Pulmonary Endothelial and Smooth Muscle Dysfunction. Am J Respir Cell Mol Biol 2010,
27. Price TO, Ercal N, Nakaoke R, Banks WA. HIV-1 viral proteins gp120 and Tat induce oxidative stress in brain endothelial cells. Brain Res 2005, 1045(12):57-63.
28. Price TO, Uras F, Banks WA, Ercal N. A novel antioxidant N-acetylcysteine amide prevents gp120- and Tat-induced oxidative stress in brain endothelial cells. Exp Neurol 2006, 201(1):193-202. 10.1016/j.expneurol.2006.03.030, 16750528.
29. Hanze J, Weissmann N, Grimminger F, Seeger W, Rose F. Cellular and molecular mechanisms of hypoxia-inducible factor driven vascular remodeling. Thromb Haemost 2007, 97(5):774-787.
30. Kuwabara K, Ogawa S, Matsumoto M, Koga S, Clauss M, Pinsky DJ, Lyn P, Leavy J, Witte L, Joseph-Silverstein J, et al. Hypoxia-mediated induction of acidic/basic fibroblast growth factor and platelet-derived growth factor in mononuclear phagocytes stimulates growth of hypoxic endothelial cells. Proc Natl Acad Sci USA 1995, 92(10):4606-4610. 10.1073/pnas.92.10.4606, 41993, 7538678.
31. Li H, Chen SJ, Chen YF, Meng QC, Durand J, Oparil S, Elton TS. Enhanced endothelin-1 and endothelin receptor gene expression in chronic hypoxia. J Appl Physiol 1994, 77(3):1451-1459.
32. Kline ER, Kleinhenz DJ, Liang B, Dikalov S, Guidot DM, Hart CM, Jones DP, Sutliff RL. Vascular oxidative stress and nitric oxide depletion in HIV-1 transgenic rats are reversed by glutathione restoration. Am J Physiol Heart Circ Physiol 2008, 294(6):H2792-2804. 10.1152/ajpheart.91447.2007, 2586125, 18456725.
33. Lassiter C, Fan X, Joshi PC, Jacob BA, Sutliff RL, Jones DP, Koval M, Guidot DM. HIV-1 transgene expression in rats causes oxidant stress and alveolar epithelial barrier dysfunction. AIDS Res Ther 2009, 6:1. 10.1186/1742-6405-6-1, 2644707, 19193217.
34. Reid W, Sadowska M, Denaro F, Rao S, Foulke J, Hayes N, Jones O, Doodnauth D, Davis H, Sill A, et al. An HIV-1 transgenic rat that develops HIV-related pathology and immunologic dysfunction. Proc Natl Acad Sci USA 2001, 98(16):9271-9276. 10.1073/pnas.161290298, 55410, 11481487.
35. White RJ, Meoli DF, Swarthout RF, Kallop DY, Galaria II, Harvey JL, Miller CM, Blaxall BC, Hall CM, Pierce RA, et al. Plexiform-like lesions and increased tissue factor expression in a rat model of severe pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol 2007, 293(3):L583-590. 10.1152/ajplung.00321.2006, 17586694.
36. Rabinovitch M. Molecular pathogenesis of pulmonary arterial hypertension. J Clin Invest 2008, 118(7):2372-2379. 10.1172/JCI33452, 2439479, 18596905.
37. Rubin LJ. Primary pulmonary hypertension. N Engl J Med 1997, 336(2):111-117. 10.1056/NEJM199701093360207, 8988890.
38. Fulton RM, Hutchinson EC, Jones AM. Ventricular weight in cardiac hypertrophy. Br Heart J 1952, 14(3):413-420. 10.1136/hrt.14.3.413, 479473, 14944734.
39. Gillespie MN, Hartsfield CL, O'Connor WN, Cohen DA. Pulmonary hypertension in a murine model of the acquired immunodeficiency syndrome. Am J Respir Crit Care Med 1994, 150(1):194-199.
40. Williams R, Yao H, Peng F, Yang Y, Bethel-Brown C, Buch S. Cooperative induction of CXCL10 involves NADPH oxidase: Implications for HIV dementia. Glia 58(5):611-621.
41. Helland DE, Welles JL, Caputo A, Haseltine WA. Transcellular transactivation by the human immunodeficiency virus type 1 tat protein. J Virol 1991, 65(8):4547-4549. 248903, 2072464.
42. Marcuzzi A, Weinberger J, Weinberger OK. Transcellular activation of the human immunodeficiency virus type 1 long terminal repeat in cocultured lymphocytes. J Virol 1992, 66(7):4228-4232. 241226, 1602543.
43. Ensoli B, Buonaguro L, Barillari G, Fiorelli V, Gendelman R, Morgan RA, Wingfield P, Gallo RC. Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J Virol 1993, 67(1):277-287. 237361, 8416373.
44. Toborek M, Lee YW, Pu H, Malecki A, Flora G, Garrido R, Hennig B, Bauer HC, Nath A. HIV-Tat protein induces oxidative and inflammatory pathways in brain endothelium. J Neurochem 2003, 84(1):169-179.
45. Dewhirst MW. Relationships between cycling hypoxia, HIF-1, angiogenesis and oxidative stress. Radiat Res 2009, 172(6):653-665. 10.1667/RR1926.1, 2790140, 19929412.
46. Tuder RM, Groves B, Badesch DB, Voelkel NF. Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension. Am J Pathol 1994, 144(2):275-285. 1887146, 7508683.
47. Cool CD, Kennedy D, Voelkel NF, Tuder RM. Pathogenesis and evolution of plexiform lesions in pulmonary hypertension associated with scleroderma and human immunodeficiency virus infection. Hum Pathol 1997, 28(4):434-442. 10.1016/S0046-8177(97)90032-0, 9104943.
48. Chi D, Henry J, Kelley J, Thorpe R, Smith JK, Krishnaswamy G. The effects of HIV infection on endothelial function. Endothelium 2000, 7(4):223-242.
49. Kourembanas S, Hannan RL, Faller DV. Oxygen tension regulates the expression of the platelet-derived growth factor-B chain gene in human endothelial cells. J Clin Invest 1990, 86(2):670-674. 10.1172/JCI114759, 296775, 2384608.
50. Ambalavanan N, Bulger A, Philips IJ. Hypoxia-induced release of peptide growth factors from neonatal porcine pulmonary artery smooth muscle cells. Biol Neonate 1999, 76(5):311-319. 10.1159/000014173, 10516398.
51. Kim J, Shao Y, Kim SY, Kim S, Song HK, Jeon JH, Suh HW, Chung JW, Yoon SR, Kim YS, et al. Hypoxia-induced IL-18 increases hypoxia-inducible factor-1alpha expression through a Rac1-dependent NF-kappaB pathway. Mol Biol Cell 2008, 19(2):433-444. 2230593, 18003981.
52. Irwin DC, McCord JM, Nozik-Grayck E, Beckly G, Foreman B, Sullivan T, White M, T Crossno J J, Bailey D, Flores SC, et al. A potential role for reactive oxygen species and the HIF-1alpha-VEGF pathway in hypoxia-induced pulmonary vascular leak. Free Radic Biol Med 2009, 47(1):55-61. 10.1016/j.freeradbiomed.2009.03.027, 2689923, 19358884.
53. Yu AY, Shimoda LA, Iyer NV, Huso DL, Sun X, McWilliams R, Beaty T, Sham JS, Wiener CM, Sylvester JT, et al. Impaired physiological responses to chronic hypoxia in mice partially deficient for hypoxia-inducible factor 1alpha. J Clin Invest 1999, 103(5):691-696. 10.1172/JCI5912, 408131, 10074486.
54. Rosenberg HC, Rabinovitch M. Endothelial injury and vascular reactivity in monocrotaline pulmonary hypertension. Am J Physiol 1988, 255(6 Pt 2):H1484-1491.
55. Kline ER, Sutliff RL. The roles of HIV-1 proteins and antiretroviral drug therapy in HIV-1-associated endothelial dysfunction. J Investig Med 2008, 56(5):752-769. 2586126, 18525451.
56. Deshmane SL, Mukerjee R, Fan S, Del Valle L, Michiels C, Sweet T, Rom I, Khalili K, Rappaport J, Amini S, et al. Activation of the oxidative stress pathway by HIV-1 Vpr leads to induction of hypoxia-inducible factor 1alpha expression. J Biol Chem 2009, 284(17):11364-11373. 2670142, 19204000.
57. Gleadle JM, Ebert BL, Firth JD, Ratcliffe PJ. Regulation of angiogenic growth factor expression by hypoxia, transition metals, and chelating agents. Am J Physiol 1995, 268(6 Pt 1):C1362-1368.
58. Stenmark KR, Mecham RP. Cellular and molecular mechanisms of pulmonary vascular remodeling. Annu Rev Physiol 1997, 59:89-144. 10.1146/annurev.physiol.59.1.89, 9074758.
59. Ulleras E, Wilcock A, Miller SJ, Franklin GC. The sequential activation and repression of the human PDGF-B gene during chronic hypoxia reveals antagonistic roles for the depletion of oxygen and glucose. Growth Factors 2001, 19(4):233-245. 10.3109/08977190109001089, 11811779.
60. Huang MB, Hunter M, Bond VC. Effect of extracellular human immunodeficiency virus type 1 glycoprotein 120 on primary human vascular endothelial cell cultures. AIDS Res Hum Retroviruses 1999, 15(14):1265-1277. 10.1089/088922299310160, 10505675.
61. Knox KS, Vinton C, Hage CA, Kohli LM, Twigg HL, Klatt NR, Zwickl B, Waltz J, Goldman M, Douek DC, et al. Reconstitution of CD4 T cells in bronchoalveolar lavage fluid after initiation of highly active antiretroviral therapy. J Virol 2010, 84(18):9010-9018. 10.1128/JVI.01138-10, 2937631, 20610726.
62. Chalifoux LV, Simon MA, Pauley DR, MacKey JJ, Wyand MS, Ringler DJ. Arteriopathy in macaques infected with simian immunodeficiency virus. Lab Invest 1992, 67(3):338-349.
63. Douek DC, Picker LJ, Koup RA. T cell dynamics in HIV-1 infection. Annu Rev Immunol 2003, 21:265-304. 10.1146/annurev.immunol.21.120601.141053, 12524385.
64. Cicala C, Arthos J, Martinelli E, Censoplano N, Cruz CC, Chung E, Selig SM, Van Ryk D, Yang J, Jagannatha S, et al. R5 and X4 HIV envelopes induce distinct gene expression profiles in primary peripheral blood mononuclear cells. Proc Natl Acad Sci USA 2006, 103(10):3746-3751. 10.1073/pnas.0511237103, 1533779, 16505369.