Viral infection and pulmonary hypertension: Is there an association?

Expert Review of Respiratory Medicine

Volumn 5, Issue 2, 2011, Pages 207-216

  Cool, Carlyne D ^a,b   Voelkel, Norbert F ^c   Bull, Todd ^b  

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

^b UNIVERSITY OF COLORADO   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

angioproliferation; HHV 8; HIV; idiopathic pulmonary arterial hypertension; immune dysregulation; pulmonary arterial hypertension

Indexed keywords

VIRUS PROTEIN;

ANGIOPROLIFERATION; APOPTOSIS; CELL GROWTH; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; GENETIC PREDISPOSITION; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HERPES VIRUS INFECTION; HUMAN; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE STATUS; IMMUNOPATHOLOGY; NONHUMAN; PATHOGENESIS; PHENOTYPE; PULMONARY HYPERTENSION; REVIEW; SURVIVAL RATE; T LYMPHOCYTE; VIRUS INFECTION;

EID: 79955404241     PISSN: 17476348     EISSN: 17476356     Source Type: Journal    
DOI: 10.1586/ers.11.17     Document Type: Review

References (114)

1. Simonneau G, Robbins IM, Beghetti M et al. Updated clinical classification of pulmonary hypertension. J. Am. Coll. Cardiol. 54, S43-S54 (2009).
2. Aldred MA, Vijayakrishnan J, James V et al. BMPR2 gene rearrangements account for a significant proportion of mutations in familial and idiopathic pulmonary arterial hypertension. Hum. Mutat. 27, 212-213 (2006).
3. Nana-Sinkam P, Oyer RJ, Stearman RS et al. Prostacyclin synthase promoter regulation and familial pulmonary arterial hypertension. Chest 128, 612S (2005). (Pubitemid 43054156)
4. Cogan JD, Pauciulo MW, Batchman AP et al. High frequency of BMPRT2 exonic deleteions/duplications in familial pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 174, 590-598 (2006). (Pubitemid 44330553)
5. Hatano S, Strasser T. Primary Pulmonary Hypertension: Report on a WHO Meeting. October 15-17, 1973. World Health Organization, Geneva, Switzerland (1975).
6. Simonneau G, Galiè N, Rubin LJ et al. Clinical classification of pulmonary hypertension. J. Am. Coll. Cardiol. 43, 5S-12S (2004). (Pubitemid 38759712)
7. Cool CD, Stewart JS, Werahera P et al. Three-dimensional reconstruction of pulmonary arteries in plexiform pulmonary hypertension using cell-specific markers. Evidence for a dynamic and heterogeneous process of pulmonary endothelial cell growth. Am. J. Pathol. 155,411-419 (1999). (Pubitemid 29370391)
8. Sitbon O, Humbert M, Xavier J et al. Long-term response to calcium channel blockers in idiopathic pulmonary arterial hypertension. Circulation 111, 3105-3111 (2005). (Pubitemid 40847788)
9. Barst RJ, Maislin G, Fishman AP. Vasodilator therapy for primary pulmonary hypertension in children. Circulation 99, 1197-1208 (1999).
10. Yung D, Widlitz AC, Rosenzweig EB et al. Outcomes in children with idiopathic pulmonary arterial hypertension. Circulation 110, 660-665. (2004). (Pubitemid 39056263)
11. Beghetti M, Galiè N. Eisenmenger syndrome. A clinical perspective in a new therapeutic era of pulmonary arterial hypertension. J. Am. Coll. Cardiol. 53, 733-740 (2009).
12. Sakao S, Tatsumi K, Voelkel NF. Endothelial cells and pulmonary arterial hypertension: apoptosis, proliferation, interaction and transdifferentiation. Respir. Res. 10, 95-103 (2009).
13. Tuder RM, Groves B, Badesch DB et al. Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension. Am. J. Pathol. 144, 275-285 (1994). (Pubitemid 24165948)
14. Tuder RM, Chacon M, Alger L et al. Expression of angiogenesis-related molecules in plexiform lesions in severe pulmonary hypertension: evidence for a process of disordered angiogenesis. J. Pathol. 195, 367-374 (2001).
15. Du L, Sullivan CC, Chu D et al. Signaling molecules in nonfamilial pulmonary hypertension. N. Engl. J. Med. 348, 500-509 (2003). (Pubitemid 36159885)
16. Mason NA, Springall DR, Burke M et al. High expression of endothelial nitric oxide synthase in plexiform lesions of pulmonary hypertension. J. Pathol. 185, 313-318 (1998). (Pubitemid 28320054)
17. Xue C, Johns RA. Upregulation of nitric oxide synthase correlates temporally with onset of pulmonary vascular remodeling in the hypoxic rat. Hypertension 28, 743-753 (1996). (Pubitemid 26365513)
18. Giaid A, Yanagisawa M, Langleben D et al. Expression of endothelin-1 in the lungs of patients with pulmonary hypertension. N. Engl. J. Med. 328, 1732-1739 (1993). (Pubitemid 23170122)
19. Golpon HA, Geraci MW, Moore MD et al. HOX genes in human lung: altered expression in primary pulmonary hypertension and emphysema Am. J. Pathol. 158, 955-966 (2001). (Pubitemid 32221787)
20. Dorfmuller P, Zarka V, Durand-Gasselin I et al. Chemokine RANTES in severe pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 165, 534-539 (2002). (Pubitemid 34165478)
21. Cool CD, Groshong SD, Oakey J, Voelkel NF. Pulmonary hypertension: cellular and molecular mechanisms. Chest 128, 565S-571S (2005). (Pubitemid 43054120)
22. Wright L, Tuder RM, Wang J et al. 5-lipoxygenase and 5-lipoxygenase activating protein (FLAP) immunoreactivity in lungs from patients with primary pulmonary hypertension. Am. J. Respir. Crit. Care Med. 157, 219-229 (1998). (Pubitemid 28071286)
23. Tuder RM, Cool CD, Geraci MW et al. Prostacyclin synthase expression is decreased in lungs from patients with severe pulmonary hypertension. Am. J. Respir. Crit. Care Med. 159, 1925-1932 (1999). (Pubitemid 29275065)
24. Achcar R, Yoshiki D, Rai PR et al. Loss of caveolin and heme oxygenase expression in severe pulmonary hypertension. Chest 129, 696-705 (2006).
25. Ameshima S, Golpon H, Cool CD et al. Peroxisome proliferator-activated receptor g (PPARg) expression is decreased in pulmonary hypertension and affects endothelial cell growth. Circ. Res. 92, 1162-1169 (2003). (Pubitemid 36665863)
26. Rai PR, Cool CD, King JA et al. The cancer paradigm of severe pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 178, 558-564 (2008).
27. Lee SD, Shroyer KR, Markham NE et al. Monoclonal endothelial cell proliferation is present in primary but not secondary pulmonary hypertension. J. Clin. Invest. 101, 927-934 (1998). (Pubitemid 28125268)
28. Yeager ME, Halley GR, Golpon HA et al. Microsatellite instability of endothelial cell growth and apoptosis genes within plexiform lesions in primary pulmonary hypertension. Circ. Res. 88, e8-e11 (2001).
29. Richter A, Yeager ME, Zaiman A et al. Impaired transforming growth factor-b signaling in idiopathic pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 170, 1340-1348 (2004). (Pubitemid 39657199)
30. Masri FA, Xu W, Comhair SA et al. Hyperproliferative apoptosis-resistant endothelial cells in idiopathic pulmonary arterial hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L548-L554 (2007). (Pubitemid 47358814)
31. Taraseviciene-Stewart L, Kasahara Y, Alger L et al. Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death-dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension. FASEB J. 15, 427-438 (2001). (Pubitemid 32141434)
32. Taraseviciene-Stewart L, Scerbavicius R, Stewart JM et al. Treatment of severe pulmonary hypertension: a bradykinin receptor 2 agonist B9972 causes reduction of pulmonary artery pressure and right ventricular hypertrophy. Peptides 26, 1292-1300, (2005). (Pubitemid 41021462)
33. Chang, Y, Cesarman MS, Pess F et al. Identification of herpesviruslike DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266, 1865-1869 (1994).
34. Memar OM, Rady PL, Tyring SK. Human herpesvirus-8: detection of novel herpesvirus-like DNA sequences in Kaposi's sarcoma and other lesions. J. Mol. Med. 73, 603-609 (1995). (Pubitemid 26018552)
35. Whitby D, Howard MR, Tenant-Flowers M et al. Detection of Kaposi sarcoma associated herpesvirus in peripheral blood of HIV-infected individuals and progression to Kaposi's sarcoma. Lancet 346, 799-802 (1995).
36. Chang Y, Antman K. Kaposi's Sarcoma. N. Engl. J. Med. 342, 1027-1038 (2000). (Pubitemid 30180651)
37. Jenner RG, Boshoff C. The molecular pathology of Kaposi's sarcoma-associated herpesvirus. Biochim. Biophys. Acta 1602, 1-22 (2002). (Pubitemid 34311897)
38. Ensoli B, Sgadari C, Barillari G, Sirianni MC, Sturzl M, Monini P. Biology of Kaposi's sarcoma. Eur. J. Cancer 37, 1251-1269 (2001). (Pubitemid 32553770)
39. Jensen KK, Manfra DJ, Grisotto MG et al. The human herpes virus 8-encoded chemokine receptor is required for angioproliferation in a murine model of Kaposi's sarcoma. J. Immunol. 174, 3686-3694 (2005). (Pubitemid 40354079)
40. Bais C, Santomasso B, Coso O et al. G-protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator. Nature 391, 86 (1998).
41. Pati S, Cavrois M, Guo HG et al. Activation of NF-kB by the human herpesvirus 8 chemokinereceptor ORF74: evidence for a paracrine model of Kaposi's sarcoma pathogenesis. J. Virol. 7, 8660 (2001).
42. Polson AG, Wang D, DeRisi J, Ganem D. Modulation of host gene expression by the constitutively active G protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus. Cancer Res. 62, 4525 (2002).
43. Schwarz M, Murphy PM. Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor constitutively activates NF-kB and induces proinflammatory cytokine and chemokine production via a C-terminal signaling determinant. J. Immunol. 167, 505 (2001).
44. Yang TY, Chen SC, Leach MW et al. Transgenic expression of the chemokine receptor encoded by human herpesvirus 8 induces an angioproliferative disease resembling Kaposi's sarcoma. J. Exp. Med. 191, 445-454 (2000).
45. Montaner S, Sodhi A, Molinolo A et al. Endothelial infection with KSHV genes in vivo reveals that vGPCR initiates Kaposi's sarcomagenesis and can promote the tumorigenic potential of viral latent genes. Cancer Cell 3, 23-36 (2003). (Pubitemid 37443889)
46. Flore O, Rafii S, Ely S et al. Transformation of primary human endothelial cells by Kaposi's sarcoma-associated herpesvirus. Nature 394, 588-592 (1998). (Pubitemid 28366835)
47. Dupin N, Fisher C, Kellam P et al. Distribution of human herpesvirus-8 latently infected cells in Kaposi's sarcoma, multicentric Castleman's disease, and primary effusion lymphoma. Proc. Natl Acad. Sci. USA 96, 4546-4551 (1999). (Pubitemid 29190373)
48. Cesarman E, Mesri EA, Gershengorn MC. Viral G protein-coupled receptor and Kaposi's sarcoma: a model of paracrine neoplasia? J. Exp. Med. 191, 417-422 (2000).
49. Grisotto MG, Garin A, Martin AP et al. The human herpesvirus 8 chemokine receptor vGPCR triggers autonomous proliferation of endothelial cells. J. Clin. Invest. 116, 1264-1273 (2006).
50. Calore EE. Herpes simplex 2 pneumonia. Braz. J. Infect. Dis. 6, 305-308 (2002).
51. Smith FB, Arias JH, Elmquist TH, Mazzara JT. Microvascular cytomegalovirus endothelialitis of the lung: a possible cause of secondary pulmonary hypertension. Chest 114, 337-340 (1998). (Pubitemid 28337408)
52. Marecki JC, Cool CD, Parr JE et al. HIV-1 Nef is associated with complex pulmonary vascular lesions in SHIV-Nef-infected macaques. Am. J. Respir. Crit. Care Med. 174, 437-445 (2006). (Pubitemid 44223125)
53. Graziani A, Galimi F, Medico E et al. The HIV-1 Nef protein interferes with phosphatidylinositol 3-kinase activation 1. J. Biol. Chem. 271, 6590-6593 (1996). (Pubitemid 26104084)
54. Linnemann T, Zheng YH, Mandic R et al. Interaction between Nef and phosphatidylinositol-3-kinase leads to activation of p21-activated kinase and increased production of HIV. Virology 294, 246-255 (2002). (Pubitemid 34920523)
55. He JC, Husain M, Sunamoto M et al. Nef stimulates proliferation of glomerular podocytes through activation of Src-dependent Stat3 and MAPK1,2 pathways. J. Clin. Invest. 114, 643-651 (2004). (Pubitemid 39578754)
56. Krautkramer E, Giese SI, Gasteier JE et al. Human immunodeficiency virus type 1 Nef activates p21-activated kinase via recruitment into lipid rafts. J. Virol. 78, 4085-4097 (2004). (Pubitemid 38437215)
57. Olivetta E, Percario Z, Fiorucci G et al. HIV-1 Nef induces the release of inflammatory factors from human monocyte/macrophages: involvement of Nef endocytotic signals and NF-k B activation. J. Immunol. 170, 1716-1727 (2003). (Pubitemid 36197386)
58. Pellicelli AM, Barbaro G, Palmieri F et al. Primary pulmonary hypertension in HIV patients: a systematic review. Angiology 52, 31-41 (2001). (Pubitemid 32113205)
59. Hughes JD, Rubin LJ. Primary pulmonary hypertension an analysis of 28 cases and a review of the literature. Medicine 65, 56-72 (1986). (Pubitemid 16160818)
60. Speich R, Jenni R, Opravil M, Pfab M, Russi EW. Primary pulmonary hypertension in HIV infection, Chest 100 1268-1271 (1991).
61. Kim KK, Factor SM. Membranoproliferative glomerulonephritis and plexogenic pulmonary arteriopathy in a homosexual man with acquired immunodeficiency syndrome. Hum. Pathol. 18, 293-296 (1987).
62. Kanmogne GD, Kennedy RC, Grammas P. Is HIV involved in the pathogenesis of non-infectious pulmonary complications in infected patients? Curr. HIV Res. 4, 385-393 (2003).
63. Mette SA, Palevsky HI, Pietra GG et al. 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. 145, 1196-1200 (1992).
64. Opravil M, Pechere M, Speich R et al. HIV-associated primary pulmonary hypertension. A case control study. Swiss HIV cohort study. Am. J. Respir. Crit. Care Med. 155, 990-995 (1997). (Pubitemid 27133414)
65. Kirchhoff F, Greenough TC, Brettler DB, Sullivan JL, Desrosiers RC. Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N. Engl. J. Med. 332, 228-232 (1995).
66. Kestler HW 3rd, Ringler DJ, Mori K et al. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65, 651-662 (1991).
67. James CO, Huang MB, Khan M, Garcia-Barrio M, Powell MD, Bond VC. Extracellular Nef protein targets CD4R T cells for apoptosis by interacting with CXCR4 surface receptors. J. Virol. 78, 3099-3109 (2004). (Pubitemid 38314368)
68. Huang MB, Jin LL, James CO, Khan M, Powell MD, Bond VC. Characterization of Nef-CXCR4 interactions important for apoptosis induction. J. Virol. 78, 11084-11096 (2004). (Pubitemid 39299649)
69. Kanmogne GD, Primeaux C, Grammas P. Induction of apoptosis and endothelin-1 secretion in primary human lung endothelial cells by HV-1 gp120 proteins. Biochem. Biophys. Res. Comm. 333, 1107-1115 (2005). (Pubitemid 40910118)
70. Fagan KA, McMurtry IF, Rodman DM. Role of endothelin-1 in lung disease. Respir. Res. 2, 90-101 (2001). (Pubitemid 34187913)
71. Filippatos GS, Gangopadhyay N, Lalude O et al. Regulation of apoptosis by vasoactive peptides. Am. J. Physiol. Lung Cell. Mol. Physiol. 281, L749-L761 (2001).
72. Hofman FM, Wright AD, Dohadwala MM, Wong-Staal F, Walker SM. Exogenous Tat protein activates human endothelial cells. Blood 82, 2774-2780 (1993). (Pubitemid 23318084)
73. Humbert M, Monti G, Brenot F et al. Increased interleukin-1 and interleukin-6 serum concentrations in severe primary pulmonary hypertension. Am. J. Respir. Crit. Care Med. 151, 1628-31 (1995).
74. Bull TM, Cool CD, Serls AE et al. Primary pulmonary hypertension, Castleman's disease and human herpesvirus-8. Eur. Respir. J. 22, 403-407 (2003). (Pubitemid 37098918)
75. Winter SS, Howard TA, Ritchey AK, Keller FG, Ware RE. Elevated levels of tumor necrosis factor-b, g-interferon, and IL-6 mRNA in Castleman's disease. Med. Pediatr. Oncol. 26, 48-53 (1996). (Pubitemid 126507801)
76. Nishi J, Maruyama I. Increased expression of vascular endothelial growth factor (VEGF) in Castleman's disease: proposed pathomechanism of vascular proliferation in the affected lymph node. Leuk. Lymphoma. 38, 387-394 (2000). (Pubitemid 30303673)
77. Moore PS, Boshoff C, Weiss RA, Chang Y. Molecular mimicry of human cytokine and cytokine response pathway genes by KSHV. Science 274, 1739 (1996).
78. Neipel F, Albrecht JC, Ensser A et al. Human herpesvirus 8 encodes a homolog of interleukin-6. J. Virol. 71, 839 (1997).
79. Nicholas J, Ruvolo VR, Burns WH et al. Kaposi's sarcoma associated human herpesvirus-8 encodes homologues of macrophage inflammatory protein-1 and interleukin-6. Nat. Med. 3, 287 (1997).
80. Burger R, Neipel F, Fleckenstein B et al. Human herpesvirus type 8 interleukin-6 homologue is functionally active on human myeloma cells. Blood 91, 1858-1863 (1998). (Pubitemid 28185485)
81. Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ. Interleukin 6 induces the expression of vascular endothelial growth factor. J. Biol. Chem. 271, 736 (1996).
82. Cool CD, Rai PR, Yeager ME et al. Expression of human herpesvirus 8 in primary pulmonary hypertension. N. Engl. J. Med. 349, 1113-1122 (2003). (Pubitemid 37122323)
83. Henke-Gendo C, Mengel M, Hoeper MM, Alkharsah K, Schulz TF. Absence of Kaposi's sarcoma-associated herpesvirus in patients with pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 172, 1581-1585 (2005). (Pubitemid 43076549)
84. Nicastri E. Human herpesvirus 8 and pulmonary hypertension. Emerg. Infect. Dis. 11, 480-482 (2005).
85. Laney AS, De Marco T, Peters JS et al. Kaposi sarcoma-associated herpesvirus and primary and secondary pulmonary hypertension. Chest 127, 762-767 (2005). (Pubitemid 40775503)
86. Montani D, Achouh L, Marcelin AG et al. Reversibility of pulmonary arterial hypertension in HIV/HHV8-associated Castleman's disease. Eur. Respir. J. 26, 969-972 (2005). (Pubitemid 41632055)
87. Opravil M, Sereni D. Natural history of HIV-associated pulmonary arterial hypertension: trends in the HAART era. AIDS 3, 35-40 (2008).
88. Bélec L, Mohamed AS, Authier FJ et al. Human herpesvirus 8 infection in patients with POEMS syndrome-associated multicentric Castleman's disease. Blood 9, 3643-3653 (1999). (Pubitemid 29249810)
89. Lesprit P, Godeau B, Authier FJ et al. Pulmonary hypertension in POEMS syndrome: a new feature mediated by cytokines. Am. J. Respir. Crit. Care Med. 157, 907-911 (1998).
90. Bull TM, Meadows CA, Coldren CD et al. Human herpesvirus-8 infection of pulmonary microvascular endothelial cells. Am. J. Respir. Cell Mol. Biol. 39, 706-716 (2008).
91. Humbert M, Morrell NW, Archer SL et al. Cellular and molecular pathobiology of pulmonary arterial hypertension. J. Am. Coll. Cardiol. 43, 13S-24S (2004). (Pubitemid 38759713)
92. Voelkel NF, Cool C, Taraceviene-Stewart L et al. Janus face of vascular endothelial growth factor: the obligatory survival factor for lung vascular endothelium controls precapillary artery remodeling in severe pulmonary hypertension. Crit. Care Med. 30, S251-S256 (2002). (Pubitemid 34507999)
93. Durrington HJ, Upton PD, Hoer S et al. Identification of a lysosomal pathway regulating degradation of the bone morphogenetic protein receptor II. J. Biol. Chem. 285, 37641-37649 (2010).
94. Dias Batista M, Ferreira S, Sauer MM et al. High human herpesvirus 8 (HHV-8) prevalence, clinical correlates and high incidence among recently HIV-1-infected subjects in Sao Paulo, Brazil. PloS ONE 4(5), e5613 (2009).
95. Young RH, Mark GJ. Pulmonary vascular changes in scleroderma. Am. J. Med. 64, 998-1004 (1978). (Pubitemid 8358593)
96. Kcomt W, Nahavandi AA, Myaing M, Alkhalil C, Stein D. Hepatitis C and the heart: to beat or not to beat. Int. J. Cardiol. 96, 147-149 (2003). (Pubitemid 38979892)
97. Moorman J, Saad M, Kosseifi S, Krishnaswamy G. Hepatitis C virus and the lung: implications for therapy. Chest 128, 2882-2892 (2005). (Pubitemid 41507650)
98. Feitelson MA, Duan LX. Hepatitis B virus X antigen in the pathogenesis of chronic infections and the development of hepatocellular carcinoma. Am. J. Pathol. 150, 1141-1157 (1997). (Pubitemid 27152632)
99. Su Q, Schroder CH, Hofmann WJ, Otto G, Pichlmayr R, Bannasch P. Expression of hepatitis B virus X protein in HBV-infected human livers and hepatocellular carcinomas. Hepatology 27, 1109-1120 (1998). (Pubitemid 28160498)
100. Kandemir O, Polat A, Kaya A. Inducible nitric oxide synthase expression in chronic viral hepatitis. J. Clin. Invest. 101, 1343-1352 (1998).
101. Yoo YD, Ueda H, Park K et al. Regulation of transforming growth factor-b1 expression by the hepatitis B virus (HBV) X transactivator. J. Clin. Invest. 97, 388-395 (1996).
102. Moon EJ, Jeon CH, Kim KR et al. Hepatitis B virus X protein induces angiogenesis by stabilizing hypoxia-inducible factor-1a. FASEB J. 18, 382-384 (2004).
103. Suzuki T. Primary pulmonary hypertension in association with human T-cell lymphotropic virus type I in a hemophiliac. Ann. Intern. Med. 123, 394 (1995).
104. 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. 28, 434-442 (1997). (Pubitemid 27175084)
105. Hachulla E, Gressin V, Guillevin L et al. Early detection of pulmonary arterial hypertension in systemic sclerosis: a French nationwide prospective multicenter study. Arthritis Rheum. 52, 3792-3800 (2005). (Pubitemid 41798217)
106. Mukerjee D, St George D, Coleiro B et al. Prevalence and outcome in systemic sclerosis associated pulmonary arterial hypertension: application of a registry approach. Ann. Rheum. Dis. 62, 1088-1093 (2003). (Pubitemid 37323574)
107. Tanaka E, Harigai M, Tanaka M, Kawaguchi Y, Hara M, Kamatani N. Pulmonary hypertension in systemic lupus erythematosus: evaluation of clinical characteristics and response to immunosuppressive treatment. J. Rheumatol. 29, 282-287 (2002). (Pubitemid 34118774)
108. Asherson RA, Higenbottam TW, Dinh Xuan AT, Khamashta MA, Huges GR. Pulmonary hypertension in a lupus clinic: experience with twenty-four patients. J. Rheumatol. 17, 1292-1298 (1990). (Pubitemid 20382853)
109. Burdt MA, Hoffman RW, Deutscher SL, Wang GS, Johnson JC, Sharp GC. Long-term outcome in mixed connective tissue disease: longitudinal clinical and serologic findings. Arthritis Rheum. 42, 899-909 (1999). (Pubitemid 29215000)
110. Jais X, Launay D, Yaici A et al. Immunosuppressive therapy in lupus-and mixed connective tissue disease-associated pulmonary arterial hypertension: a retrospective analysis of twenty-three cases. Arthritis Rheum. 58, 521-531 (2008). (Pubitemid 351294886)
111. Taraseviciene-Stewart L, Scerbavicius DK, Burns N, Cool CD, Nicolls MR, Voelkel NF. The protective role of T-lymphocytes in pulmonary vascular remodeling. Chest 128, S571-S572 (2005).
112. Tamosiuniene R, Long C, Ambler K et al. Immune reconstitution prevents autoimmune inflammation and right ventricular remodeling in immunodeficiency- associated pulmonary hypertension. Circulation 120, S1135 (2009).
113. Hamamdzic D, Kasman LM, LeRoy EC. The role of infectious agents in the pathogenesis of systemic sclerosis. Curr. Opin. Rheumatol. 14, 694-698 (2002) (Pubitemid 35191558)
114. Harel L, Straussberg R, Rudich H, Cohen AH, Amir J. Raynaud's phenomenon as a manifestation of parvovirus B19 infection: case reports and review of parvovirus B19 infection: case reports and review of parvovirus B19 rheumatic and vasculitic syndromes. Clin. Infect. Dis. 30, 500-503 (2000). (Pubitemid 30205295)