Hyperproliferative apoptosis-resistant endothelial cells in idiopathic pulmonary arterial hypertension

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 293, Issue 3, 2007, Pages

  Masri, Fares A ^a,b   Xu, Weiling ^a   Comhair, Suzy A A ^a   Asosingh, Kewal ^a   Koo, Michelle ^a   Vasanji, Amit ^a   Drazba, Judith ^a   Anand Apte, Bela ^a   Erzurum, Serpil C ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; STAT3

Indexed keywords

BROXURIDINE; CASPASE 3; JANUS KINASE INHIBITOR; KI 67 ANTIGEN; PROTEIN MCL 1; STAT3 PROTEIN;

ADULT; ANGIOGENESIS; APOPTOSIS; ARTICLE; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; NICK END LABELING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION;

ADULT; APOPTOSIS; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; FEMALE; HUMANS; HYPERTENSION, PULMONARY; INTERLEUKIN-15; MALE; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; PULMONARY ARTERY; STAT3 TRANSCRIPTION FACTOR;

EID: 34548433880     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00428.2006     Document Type: Article

References (37)

1. Aaronson DS, Horvath CM. A road map for those who don't know JAK-STAT. Science 296: 1653-1655, 2002.
2. Ameshima S, Golpon H, Cool CD, Chan D, Vandivier RW, Gardai SJ, Wick M, Nemenoff RA, Geraci MW, Voelkel NF. Peroxisome proliferator-activated receptor gamma (PPARgamma) expression is decreased in pulmonary hypertension and affects endothelial cell growth. Circ Res 92: 1162-1169, 2003.
3. Angiolillo AL, Kanegane H, Sgadari C, Reaman GH, Tosato G. Interleukin-15 promotes angiogenesis in vivo. Biochem Biophys Res Commun 233: 231-237, 1997.
4. Atkinson C, Stewart S, Upton PD, Machado R, Thomson JR, Trembath RC, Morrell NW. Primary pulmonary hypertension is associated with reduced pulmonary vascular expression of type II bone morphogenetic protein receptor. Circulation 105: 1672-1678, 2002.
5. Bartoli M, Gu X, Tsai NT, Venema RC, Brooks SE, Marrero MB, Caldwell RB. Vascular endothelial growth factor activates STAT proteins in aortic endothelial cells. J Biol Chem 275: 33189-33192, 2000.
6. Benekli M, Baer MR, Baumann H, Wetzler M. Signal transducer and activator of transcription proteins in leukemias. Blood 101: 2940-2954, 2003.
7. Bulfone-Paus S, Ungureanu D, Pohl T, Lindner G, Paus R, Ruckert R, Krause H, Kunzendorf U. Interleukin-15 protects from lethal apoptosis in vivo. Nat Med 3: 1124-1128, 1997.
8. 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.
9. Cool CD, Stewart JS, Werahera P, Miller GJ, Williams RL, Voelkel NF, Tuder RM. 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.
10. Darnell JE Jr. STATs and gene regulation. Science 277: 1630-1635, 1997.
11. Deng Z, Morse JH, Slager SL, Cuervo N, Moore KJ, Venetos G, Kalachikov S, Cayanis E, Fischer SG, Barst RJ, Hodge SE, Knowles JA. Familial primary pulmonary hypertension (gene PPH1) is caused by mutations in the bone morphogenetic protein receptor-II gene. Am J Hum Genet 67: 737-744, 2000.
12. Geraci MW, Moore M, Gesell T, Yeager ME, Alger L, Golpon H, Gao B, Loyd JE, Tuder RM, Voelkel NF. Gene expression patterns in the lungs of patients with primary pulmonary hypertension: a gene microarray analysis. Circ Res 88: 555-562, 2001.
13. Gerber HP, Dixit V, Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J Biol Chem 273: 13313-13316, 1998.
14. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273: 30336-30343, 1998.
15. Girard D, Paquet ME, Paquin R, Beaulieu AD. Differential effects of interleukin-15 (IL-15) and IL-2 on human neutrophils: modulation of phagocytosis, cytoskeleton rearrangement, gene expression, and apoptosis by IL-15. Blood 88: 3176-3184, 1996.
16. Giron-Michel J, Caignard A, Fogli M, Brouty-Boye D, Briard D, van Dijk M, Meazza R, Ferrini S, Lebousse-Kerdiles C, Clay D, Bompais H, Chouaib S, Peault B, Azzarone B. Differential STAT3, STAT5, and NF-kappaB activation in human hematopoietic progenitors by endogenous interleukin-15: implications in the expression of functional molecules. Blood 102: 109-117, 2003.
17. Grabstein KH, Eisenman J, Shanebeck K, Rauch C, Srinivasan S, Fung V, Beers C, Richardson J, Schoenborn MA, Ahdieh M, Johnson L, Alderson MR, Watson JD, Anderson DM, Giri JG. Cloning of a T cell growth factor that interacts with the beta chain of the interleukin-2 receptor. Science 264: 965-968, 1994.
18. Kawamura C, Kizaki M, Yamato K, Uchida H, Fukuchi Y, Hattori Y, Koseki T, Nishihara T, Ikeda Y. Bone morphogenetic protein-2 induces apoptosis in human myeloma cells with modulation of STAT3. Blood 96: 2005-2011, 2000.
19. Lane KB, Machado RD, Pauciulo MW, Thomson JR, Phillips JA 3rd, Loyd JE, Nichols WC, Trembath RC. Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. The International PPH Consortium. Nat Genet 26: 81-84, 2000.
20. Lee PC, Salyapongse AN, Bragdon GA, Shears LL 2nd, Watkins SC, Edington HD, Billiar TR. Impaired wound healing and angiogenesis in eNOS-deficient mice. Am J Physiol Heart Circ Physiol 277: H1600-H1608, 1999.
21. Lee SD, Shroyer KR, Markham NE, Cool CD, Voelkel NF, Tuder RM. Monoclonal endothelial cell proliferation is present in primary but not secondary pulmonary hypertension. J Clin Invest 101: 927-934, 1998.
22. Liu H, Ma Y, Cole SM, Zander C, Chen KH, Karras J, Pope RM. Serine phosphorylation of STAT3 is essential for Mcl-1 expression and macrophage survival. Blood 102: 344-352, 2003.
23. Niu G, Wright KL, Huang M, Song L, Haura E, Turkson J, Zhang S, Wang T, Sinibaldi D, Coppola D, Heller R, Ellis LM, Karras J, Bromberg J, Pardoll D, Jove R, Yu H. Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene 21: 2000-2008, 2002.
24. Pelletier M, Ratthe C, Girard D. Mechanisms involved in interleukin-15-induced suppression of human neutrophil apoptosis: role of the antiapoptotic Mcl-1 protein and several kinases including Janus kinase-2, p38 mitogen-activated protein kinase and extracellular signal-regulated kinases-1/2. FEBS Lett 532: 164-170, 2002.
25. Pepper MS. Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev 8: 21-43, 1997.
26. Rich S. Primary pulmonary hypertension. Prog Cardiovasc Dis 31: 205-238, 1988.
27. Rubin LJ. Primary pulmonary hypertension. N Engl J Med 336: 111-117, 1997.
28. Sakao S, Taraseviciene-Stewart L, Lee JD, Wood K, Cool CD, Voelkel NF. Initial apoptosis is followed by increased proliferation of apoptosis-resistant endothelial cells. FASEB J 19: 1178-1180, 2005.
29. Shibata R, Kai H, Seki Y, Kato S, Wada Y, Hanakawa Y, Hashimoto K, Yoshimura A, Imaizumi T. Inhibition of STAT3 prevents neointima formation by inhibiting proliferation and promoting apoptosis of neointimal smooth muscle cells. Hum Gene Ther 14: 601-610, 2003.
30. 29a. Simonneau G, Galie N, Rubin LJ, Langleben D, Seeger W, Domenighetti G, Gibbs S, Lebrec D, Speich R, Beghetti M, Rich S, Fishman A. Clinical classification of pulmonary hypertension. J Am Coll Cardiol 43: 5S-12S, 2004.
31. Taraseviciene-Stewart L, Kasahara Y, Alger L, Hirth P, Mc Mahon G, Waltenberger J, Voelkel NF, Tuder RM. 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.
32. 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 144: 275-285, 1994.
33. Xu W, Comhair SA, Zheng S, Chu SC, Marks-Konczalik J, Moss J, Haque SJ, Erzurum SC. STAT-1 and c-Fos interaction in nitric oxide synthase-2 gene activation. Am J Physiol Lung Cell Mol Physiol 285: L137-L148, 2003.
34. Xu W, Kaneko FT, Zheng S, Comhair SA, Janocha AJ, Goggans T, Thunnissen FB, Farver C, Hazen SL, Jennings C, Dweik RA, Arroliga AC, Erzurum SC. Increased arginase II and decreased NO synthesis in endothelial cells of patients with pulmonary arterial hypertension. FASEB J 18: 1746-1748, 2004.
35. Yahata Y, Shirakata Y, Tokumaru S, Yamasaki K, Sayama K, Hanakawa Y, Detmar M, Hashimoto K. Nuclear translocation of phosphorylated STAT3 is essential for vascular endothelial growth factor-induced human dermal microvascular endothelial cell migration and tube formation. J Biol Chem 278: 40026-40031, 2003.
36. Zamo A, Chiarle R, Piva R, Howes J, Fan Y, Chilosi M, Levy DE, Inghirami G. Anaplastic lymphoma kinase (ALK) activates Stat3 and protects hematopoietic cells from cell death. Oncogene 21: 1038-1047, 2002.
37. Zhou P, Levy NB, Xie H, Qian L, Lee CY, Gascoyne RD, Craig RW. MCL1 transgenic mice exhibit a high incidence of B-cell lymphoma manifested as a spectrum of histologic subtypes. Blood 97: 3902-3909, 2001.