Inhibition of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) reverses experimental pulmonary hypertension

Journal of Experimental Medicine

Volumn 209, Issue 11, 2012, Pages 1919-1935

  Hameed, Abdul G ^a   Arnold, Nadine D ^a,b   Chamberlain, Janet ^a   Pickworth, Josephine A ^a,b   Paiva, Claudia ^a   Dawson, Sarah ^a   Cross, Simon ^a   Long, Lu ^c   Zhao, Lan ^d   Morrell, Nicholas W ^c   Crossman, David C ^a,b,e   Newman, Christopher M H ^a   Kiely, David G ^b,f   Francis, Sheila E ^a   Lawrie, Allan ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b National Institute for Health Research Cardiovascular Biomedical Research Unit ^*  (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^f ROYAL HALLAMSHIRE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; MESSENGER RNA; TUMOR NECROSIS FACTOR ANTIBODY; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW TRANSPLANTATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; ECHOCARDIOGRAPHY; GENE DELETION; HEMODYNAMICS; HUMAN; HUMAN CELL; HYPOXIA; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PHARMACOLOGICAL BLOCKING; POST TREATMENT SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RAT; REMISSION; UPREGULATION;

ADULT; ANIMALS; ANOXIA; ANTIBODIES; APOLIPOPROTEINS E; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; GENE EXPRESSION; HUMANS; HYPERTENSION, PULMONARY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PULMONARY ARTERY; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; YOUNG ADULT;

EID: 84870279242     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20112716     Document Type: Article

References (89)

1. Ashkenazi, A., and V.M. Dixit. 1998. Death receptors: signaling and modulation. Science. 281:1305-1308. http://dx.doi.org/10.1126/science.281.5381.1305
2. Benisty, J.I., V.V. McLaughlin, M.J. Landzberg, J.D. Rich, J.W. Newburger, S. Rich, and J. Folkman. 2004. Elevated basic fibroblast growth factor levels in patients with pulmonary arterial hypertension. Chest. 126:1255-1261. http://dx.doi.org/10.1378/chest.126.4.1255
3. Bräutigam, K., J. Biernath-Wüpping, D.O. Bauerschlag, C.S. von Kaisenberg, W. Jonat, N. Maass, N. Arnold, and I. Meinhold-Heerlein. 2011. Combined treatment with TRAIL and PPARγ ligands overcomes chemoresistance of ovarian cancer cell lines. J. Cancer Res. Clin. Oncol. 137:875-886. http://dx.doi.org/10.1007/s00432-010-0952-2
4. Chamberlain, J., D. Evans, A. King, R. Dewberry, S. Dower, D. Crossman, and S. Francis. 2006. Interleukin-1beta and signaling of interleukin-1 in vascular wall and circulating cells modulates the extent of neointima formation in mice. Am. J. Pathol. 168:1396-1403. http://dx.doi.org/10.2353/ajpath.2006.051054
5. Chan, J., L. Prado-Lourenco, L.M. Khachigian, M.R. Bennett, B.A. Di Bartolo, and M.M. Kavurma. 2010. TRAIL promotes VSMC proliferation and neointima formation in a FGF-2-, Sp1 phosphorylation-, and NFkappaB-dependent manner. Circ. Res. 106:1061-1071. http://dx.doi.org/10.1161/CIRCRESAHA.109.206029
6. Chapman, H.A., R.J. Riese, and G.P. Shi. 1997. Emerging roles for cysteine proteases in human biology. Annu. Rev. Physiol. 59:63-88. http://dx.doi.org/10.1146/annurev.physiol.59.1.63
7. Chemla, D., V. Castelain, M. Humbert, J.-L. Hébert, G. Simonneau, Y. Lecarpentier, and P. Hervé. 2004. New formula for predicting mean pulmonary artery pressure using systolic pulmonary artery pressure. Chest. 126:1313-1317. http://dx.doi.org/10.1378/chest.126.4.1313
8. Chin, K.M., N.H.S. Kim, and L.J. Rubin. 2005. The right ventricle in pulmonary hypertension. Coron. Artery Dis. 16:13-18. http://dx.doi.org/10.1097/00019501-200502000-00003
9. Cretney, E., K. Takeda, H. Yagita, M. Glaccum, J.J. Peschon, and M.J. Smyth. 2002. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J. Immunol. 168: 1356-1361.
10. de Man, F.S., M.L. Handoko, J.J.M. van Ballegoij, I. Schalij, S.J.P. Bogaards, P.E. Postmus, J. van der Velden, N. Westerhof, W.J. Paulus, and A. VonkNoordegraaf. 2012. Bisoprolol delays progression towards right heart failure in experimental pulmonary hypertension. Circ. Heart Fail. 5:97-105. http://dx.doi.org/10.1161/Circheartfailure.111.964494
11. De Toni, E.N., S.E. Thieme, A. Herbst, A. Behrens, P. Stieber, A. Jung, H. Blum, B. Göke, and F.T. Kolligs. 2008. OPG is regulated by beta-catenin and mediates resistance to TRAIL-induced apoptosis in colon cancer. Clin. Cancer Res. 14:4713-4718. http://dx.doi.org/10.1158/1078-0432.CCR-07-5019
12. Degli-Esposti, M.A., W.C. Dougall, P.J. Smolak, J.Y. Waugh, C.A. Smith, and R.G. Goodwin. 1997a. The novel receptor TRAIL-R4 induces NF-kappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. Immunity. 7:813-820. http://dx.doi.org/10.1016/S1074-7613(00)80399-4
13. Degli-Esposti, M.A., P.J. Smolak, H. Walczak, J. Waugh, C.P. Huang, R.F. DuBose, R.G. Goodwin, and C.A. Smith. 1997b. Cloning and characterization of TRAIL-R3, a novel member of the emerging TRAIL receptor family. J. Exp. Med. 186:1165-1170. http://dx.doi.org/10.1084/jem.186.7.1165
14. Dickinson, M.G., B. Bartelds, G. Molema, M.A. Borgdorff, B. Boersma, J. Takens, M. Weij, P. Wichers, H. Sietsma, and R.M.F. Berger. 2011. Egr-1 expression during neointimal development in flow-associated pulmonary hypertension. Am. J. Pathol. 179:2199-2209. http://dx.doi.org/10.1016/j.ajpath.2011.07.030
15. Droin, N.M., M.J. Pinkoski, E. Dejardin, and D.R. Green. 2003. Egr family members regulate nonlymphoid expression of Fas ligand, TRAIL, and tumor necrosis factor during immune responses. Mol. Cell. Biol. 23:7638-7647. http://dx.doi.org/10.1128/MCB.23.21.7638-7647.2003
16. Emery, J.G., P. McDonnell, M.B. Burke, K.C. Deen, S. Lyn, C. Silverman, E. Dul, E.R. Appelbaum, C. Eichman, R. DiPrinzio, et al. 1998. Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL. J. Biol. Chem. 273:14363-14367. http://dx.doi.org/10.1074/jbc.273.23.14363
17. Falschlehner, C., U. Schaefer, and H. Walczak. 2009. Following TRAIL's path in the immune system. Immunology. 127:145-154. http://dx.doi.org/10.1111/j.1365-2567.2009.03058.x
18. Fionda, C., F. Nappi, M. Piccoli, L. Frati, A. Santoni, and M. Cippitelli. 2007. Inhibition of trail gene expression by cyclopentenonic prostaglandin 15-deoxy-delta12,14-prostaglandin J2 in T lymphocytes. Mol. Pharmacol. 72:1246-1257. http://dx.doi.org/10.1124/mol.107.038042
19. Fu, M., X. Zhu, J. Zhang, J. Liang, Y. Lin, L. Zhao, M.U. Ehrengruber, and Y.E. Chen. 2003. Egr-1 target genes in human endothelial cells identified by microarray analysis. Gene. 315:33-41. http://dx.doi.org/10.1016/S0378-1119(03)00730-3
20. Ghofrani, H.A., R.J. Barst, R.L. Benza, H.C. Champion, K.A. Fagan, F. Grimminger, M. Humbert, G. Simonneau, D.J. Stewart, C. Ventura, and L.J. Rubin. 2009. Future perspectives for the treatment of pulmonary arterial hypertension. J. Am. Coll. Cardiol. 54:S108-S117. http://dx.doi.org/10.1016/j.jacc.2009.04.014
21. Ghofrani, H.A., N.W. Morrell, M.M. Hoeper, H. Olschewski, A.J. Peacock, R.J. Barst, S. Shapiro, H. Golpon, M. Toshner, F. Grimminger, and S. Pascoe. 2010. Imatinib in pulmonary arterial hypertension patients with inadequate response to established therapy. Am. J. Respir. Crit. Care Med. 182:1171-1177. http://dx.doi.org/10.1164/rccm.201001-0123OC
22. Gochuico, B.R., J. Zhang, B.Y. Ma, A. Marshak-Rothstein, and A. Fine. 2000. TRAIL expression in vascular smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:L1045-L1050.
23. Guignabert, C., C.M. Alvira, T.-P. Alastalo, H. Sawada, G. Hansmann, M. Zhao, L. Wang, N. El-Bizri, and M. Rabinovitch. 2009. Tie2-mediated loss of peroxisome proliferator-activated receptor-gamma in mice causes PDGF receptor-beta-dependent pulmonary arterial muscularization. Am. J. Physiol. Lung Cell. Mol. Physiol. 297:L1082-L1090. http://dx.doi.org/10.1152/ajplung.00199.2009
24. Hagen, M., K. Fagan, W. Steudel, M. Carr, K. Lane, D.M. Rodman, and J. West. 2007. Interaction of interleukin-6 and the BMP pathway in pulmonary smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 292:L1473-L1479. http://dx.doi.org/10.1152/ajplung.00197.2006
25. Hansmann, G., R.A. Wagner, S. Schellong, V.A. Perez, T. Urashima, L. Wang, A.Y. Sheikh, R.S. Suen, D.J. Stewart, and M. Rabinovitch. 2007. Pulmonary arterial hypertension is linked to insulin resistance and reversed by peroxisome proliferator-activated receptor-gamma activation. Circulation. 115:1275-1284.
26. Hansmann, G., V.A. de Jesus Perez, T.-P. Alastalo, C.M. Alvira, C. Guignabert, J.M. Bekker, S. Schellong, T. Urashima, L. Wang, N.W. Morrell, and M. Rabinovitch. 2008. An antiproliferative BMP-2/PPARgamma/apoE axis in human and murine SMCs and its role in pulmonary hypertension. J. Clin. Invest. 118:1846-1857. http://dx.doi.org/10.1172/JCI32503
27. Hemnes, A.R., and H.C. Champion. 2008. Right heart function and haemodynamics in pulmonary hypertension. Int. J. Clin. Pract. Suppl. 62:11-19. http://dx.doi.org/10.1111/j.1742-1241.2008.01812.x
28. Ho, T.C., S.L. Chen, S.C. Shih, S.J. Chang, S.L. Yang, J.W. Hsieh, H.C. Cheng, L.J. Chen, and Y.P. Tsao. 2011. Pigment epithelium-derived factor (PEDF) promotes tumor cell death by inducing macrophage membrane tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J. Biol. Chem. 286:35943-35954. http://dx.doi.org/10.1074/jbc.M111.266064
29. Holen, I., and C.M. Shipman. 2006. Role of osteoprotegerin (OPG) in cancer. Clin. Sci. 110:279-291. http://dx.doi.org/10.1042/CS20050175
30. Hopkins-Donaldson, S., A. Ziegler, S. Kurtz, C. Bigosch, D. Kandioler, C. Ludwig, U. Zangemeister-Wittke, and R. Stahel. 2003. Silencing of death receptor and caspase-8 expression in small cell lung carcinoma cell lines and tumors by DNA methylation. Cell Death Differ. 10:356-364. http://dx.doi.org/10.1038/sj.cdd.4401157
31. Hübner, R.-H., W. Gitter, N.E. El Mokhtari, M. Mathiak, M. Both, H. Bolte, S. Freitag-Wolf, and B. Bewig. 2008. Standardized quantification of pulmonary fibrosis in histological samples. Biotechniques. 44:507-511: 514-517. http://dx.doi.org/10.2144/000112729
32. Humbert, M. 2008. Update in pulmonary arterial hypertension 2007. Am. J. Respir. Crit. Care Med. 177:574-579. http://dx.doi.org/10.1164/rccm.200801-029UP
33. Humbert, M., and V.V. McLaughlin. 2009. The 4th World Symposium on Pulmonary Hypertension. Introduction. J. Am. Coll. Cardiol. 54:S1-S2. http://dx.doi.org/10.1016/j.jacc.2009.04.013
34. Humbert, M., G. Monti, F. Brenot, O. Sitbon, A. Portier, L. Grangeot-Keros, P. Duroux, P. Galanaud, G. Simonneau, and D. Emilie. 1995. Increased interleukin-1 and interleukin-6 serum concentrations in severe primary pulmonary hypertension. Am. J. Respir. Crit. Care Med. 151:1628-1631.
35. Humbert, M., O. Sitbon, and G. Simonneau. 2004. Treatment of pulmonary arterial hypertension. N. Engl. J. Med. 351:1425-1436. http://dx.doi.org/10.1056/NEJMra040291
36. Ikeda, T., S. Hirata, S. Fukushima, Y. Matsunaga, T. Ito, M. Uchino, Y. Nishimura, and S. Senju. 2010. Dual effects of TRAIL in suppression of autoimmunity: the inhibition of Th1 cells and the promotion of regulatory T cells. J. Immunol. 185:5259-5267. http://dx.doi.org/10.4049/jimmunol.0902797
37. International PPH Consortium, Lane, K.B., R.D. Machado, M.W. Pauciulo, J.R. Thomson, J.A. Phillips III, J.E. Loyd, W.C. Nichols, and R.C. Trembath. 2000. Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. Nat. Genet. 26:81-84. http://dx.doi.org/10.1038/79226
38. Izikki, M., C. Guignabert, E. Fadel, M. Humbert, L. Tu, P. Zadigue, P. Dartevelle, G. Simonneau, S. Adnot, B. Maitre, et al. 2009. Endothelialderived FGF2 contributes to the progression of pulmonary hypertension in humans and rodents. J. Clin. Invest. 119:512-523. http://dx.doi.org/10.1172/JCI35070
39. Kavurma, M.M., M. Schoppet, Y.V. Bobryshev, L.M. Khachigian, and M.R. Bennett. 2008. TRAIL stimulates proliferation of vascular smooth muscle cells via activation of NF-kappaB and induction of insulin-like growth factor-1 receptor. J. Biol. Chem. 283:7754-7762. http://dx.doi.org/10.1074/jbc.M706927200
40. Lawrie, A., E. Spiekerkoetter, E.C. Martinez, N. Ambartsumian, W.J. Sheward, M.R. MacLean, A.J. Harmar, A.-M. Schmidt, E. Lukanidin, and M. Rabinovitch. 2005. Interdependent serotonin transporter and receptor pathways regulate S100A4/Mts1, a gene associated with pulmonary vascular disease. Circ. Res. 97:227-235. http://dx.doi.org/10.1161/01.RES.0000176025.57706.1e
41. Lawrie, A., E. Waterman, M. Southwood, D. Evans, J. Suntharalingam, S. Francis, D.C. Crossman, P. Croucher, N.W. Morrell, and C. Newman. 2008. Evidence of a role for osteoprotegerin in the pathogenesis of pulmonary arterial hypertension. Am. J. Pathol. 172:256-264. http://dx.doi.org/10.2353/ajpath.2008.070395
42. Lawrie, A., A.G. Hameed, J. Chamberlain, N. Arnold, A. Kennerley, K. Hopkinson, J. Pickworth, D.G. Kiely, D.C. Crossman, and S.E. Francis. 2011. Paigen diet-fed apolipoprotein E knockout mice develop severe pulmonary hypertension in an interleukin-1-dependent manner. Am. J. Pathol. 179:1693-1705. http://dx.doi.org/10.1016/j.ajpath.2011.06.037
43. LeBlanc, H.N., and A. Ashkenazi. 2003. Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ. 10:66-75. http://dx.doi.org/10.1038/sj.cdd.4401187
44. Lee, S.L., W.W. Wang, G.A. Finlay, and B.L. Fanburg. 1999. Serotonin stimulates mitogen-activated protein kinase activity through the formation of superoxide anion. Am. J. Physiol. 277:L282-L291.
45. Leung, W.C.Y., A. Lawrie, S. Demaries, H. Massaeli, A. Burry, S. Yablonsky, J.M. Sarjeant, E. Fera, E. Rassart, J.G. Pickering, and M. Rabinovitch. 2004. Apolipoprotein D and platelet-derived growth factor-BB synergism mediates vascular smooth muscle cell migration. Circ. Res. 95:179-186. http://dx.doi.org/10.1161/01.RES.0000135482.74178.14
46. Li, J.H., N.C. Kirkiles-Smith, J.M. McNiff, and J.S. Pober. 2003. TRAIL induces apoptosis and inflammatory gene expression in human endothelial cells. J. Immunol. 171:1526-1533.
47. Long, L., M.R. MacLean, T.K. Jeffery, I. Morecroft, X. Yang, N. Rudarakanchana, M. Southwood, V. James, R.C. Trembath, and N.W. Morrell. 2006. Serotonin increases susceptibility to pulmonary hypertension in BMPR2-deficient mice. Circ. Res. 98:818-827. http://dx.doi.org/10.1161/01.RES.0000215809.47923.fd
48. Lu, M., T. Kwan, C. Yu, F. Chen, B. Freedman, J.M. Schafer, E.-J. Lee, J.L. Jameson, V.C. Jordan, and V.L. Cryns. 2005. Peroxisome proliferatoractivated receptor gamma agonists promote TRAIL-induced apoptosis by reducing survivin levels via cyclin D3 repression and cell cycle arrest. J. Biol. Chem. 280:6742-6751. http://dx.doi.org/10.1074/jbc.M411519200
49. Ma, W., W. Han, P.A. Greer, R.M. Tuder, H.A. Toque, K.K.W. Wang, R.W. Caldwell, and Y. Su. 2011. Calpain mediates pulmonary vascular remodeling in rodent models of pulmonary hypertension, and its inhibition attenuates pathologic features of disease. J. Clin. Invest. 121:4548-4566. http://dx.doi.org/10.1172/JCI57734
50. MacFarlane, M., M. Ahmad, S.M. Srinivasula, T. Fernandes-Alnemri, G.M. Cohen, and E.S. Alnemri. 1997. Identification and molecular cloning of two novel receptors for the cytotoxic ligand TRAIL. J. Biol. Chem. 272:25417-25420. http://dx.doi.org/10.1074/jbc.272.41.25417
51. Malyankar, U.M., M. Scatena, K.L. Suchland, T.J. Yun, E.A. Clark, and C.M. Giachelli. 2000. Osteoprotegerin is an alpha vbeta 3-induced, NF-kappa B-dependent survival factor for endothelial cells. J. Biol. Chem. 275:20959-20962. http://dx.doi.org/10.1074/jbc.C000290200
52. Mariani, S.M., and P.H. Krammer. 1998. Differential regulation of TRAIL and CD95 ligand in transformed cells of the T and B lymphocyte lineage. Eur. J. Immunol. 28:973-982. http://dx.doi.org/10.1002/(SICI)15214141(199803)28:03<973::AID-IMMU973>3.0.CO;2-T
53. Marsters, S.A., J.P. Sheridan, R.M. Pitti, A. Huang, M. Skubatch, D. Baldwin, J. Yuan, A. Gurney, A.D. Goddard, P. Godowski, and A. Ashkenazi. 1997. A novel receptor for Apo2L/TRAIL contains a truncated death domain. Curr. Biol. 7:1003-1006. http://dx.doi.org/10.1016/S0960-9822(06)00422-2
54. McGrath, E.E., H.M. Marriott, A. Lawrie, S.E. Francis, I. Sabroe, S.A. Renshaw, D.H. Dockrell, and M.K.B. Whyte. 2011. TNF-related apoptosis-inducing ligand (TRAIL) regulates inflammatory neutrophil apoptosis and enhances resolution of inflammation. J. Leukoc. Biol. 90:855-865. http://dx.doi.org/10.1189/jlb.0211062
55. McMurtry, M.S., S.L. Archer, D.C. Altieri, S. Bonnet, A. Haromy, G. Harry, S. Bonnet, L. Puttagunta, and E.D. Michelakis. 2005. Gene therapy targeting survivin selectively induces pulmonary vascular apoptosis and reverses pulmonary arterial hypertension. J. Clin. Invest. 115:1479-1491. http://dx.doi.org/10.1172/JCI23203
56. Merklinger, S.L., P.L. Jones, E.C. Martinez, and M. Rabinovitch. 2005. Epidermal growth factor receptor blockade mediates smooth muscle cell apoptosis and improves survival in rats with pulmonary hypertension. Circulation. 112:423-431. http://dx.doi.org/10.1161/CIRCULATIONAHA.105.540542
57. Miyashita, T., A. Kawakami, T. Nakashima, S. Yamasaki, M. Tamai, F. Tanaka, M. Kamachi, H. Ida, K. Migita, T. Origuchi, et al. 2004. Osteoprotegerin (OPG) acts as an endogenous decoy receptor in tumour necrosis factorrelated apoptosis-inducing ligand (TRAIL)-mediated apoptosis of fibroblast-like synovial cells. Clin. Exp. Immunol. 137:430-436. http://dx.doi.org/10.1111/j.1365-2249.2004.02534.x
58. Morrell, N.W., S. Adnot, S.L. Archer, J. Dupuis, P.L. Jones, M.R. MacLean, I.F. McMurtry, K.R. Stenmark, P.A. Thistlethwaite, N. Weissmann, et al. 2009. Cellular and molecular basis of pulmonary arterial hypertension. J. Am. Coll. Cardiol. 54:S20-S31. http://dx.doi.org/10.1016/j.jacc.2009.04.018
59. Nguyen, K.Q., P. Olesen, T. Ledet, and L.M. Rasmussen. 2007. Bone morphogenetic proteins regulate osteoprotegerin and its ligands in human vascular smooth muscle cells. Endocrine. 32:52-58. http://dx.doi.org/10.1007/s12020-007-9007-0
60. Nisbet, R.E., J.M. Bland, D.J. Kleinhenz, P.O. Mitchell, E.R. Walp, R.L. Sutliff, and C.M. Hart. 2010. Rosiglitazone attenuates chronic hypoxia-induced pulmonary hypertension in a mouse model. Am. J. Respir. Cell Mol. Biol. 42:482-490. http://dx.doi.org/10.1165/rcmb.2008-0132OC
61. Pai, S.I., G.S. Wu, N. Ozören, L. Wu, J. Jen, D. Sidransky, and W.S. ElDeiry. 1998. Rare loss-of-function mutation of a death receptor gene in head and neck cancer. Cancer Res. 58:3513-3518.
62. Pan, G., J. Ni, Y.F. Wei, G. Yu, R. Gentz, and V.M. Dixit. 1997a. An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science. 277:815-818. http://dx.doi.org/10.1126/science.277.5327.815
63. Pan, G., K. O'Rourke, A.M. Chinnaiyan, R. Gentz, R. Ebner, J. Ni, and V.M. Dixit. 1997b. The receptor for the cytotoxic ligand TRAIL. Science. 276:111-113. http://dx.doi.org/10.1126/science.276.5309.111
64. Pan, G., J. Ni, G. Yu, Y.F. Wei, and V.M. Dixit. 1998. TRUNDD, a new member of the TRAIL receptor family that antagonizes TRAIL signalling. FEBS Lett. 424:41-45. http://dx.doi.org/10.1016/S0014-5793(98)00135-5
65. Perros, F., D. Montani, P. Dorfmüller, I. Durand-Gasselin, C. Tcherakian, J. Le Pavec, M. Mazmanian, E. Fadel, S. Mussot, O. Mercier, et al. 2008. Platelet-derived growth factor expression and function in idiopathic pulmonary arterial hypertension. Am. J. Respir. Crit. Care Med. 178:81-88. http://dx.doi.org/10.1164/rccm.200707-1037OC
66. Pitti, R.M., S.A. Marsters, S. Ruppert, C.J. Donahue, A. Moore, and A. Ashkenazi. 1996. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271:12687-12690. http://dx.doi.org/10.1074/jbc.271.22.12687
67. Rabinovitch, M. 2010. PPARgamma and the pathobiology of pulmonary arterial hypertension. Adv. Exp. Med. Biol. 661:447-458. http://dx.doi.org/10.1007/978-1-60761-500-2_29
68. Schermuly, R.T., E. Dony, H.A. Ghofrani, S. Pullamsetti, R. Savai, M. Roth, A. Sydykov, Y.J. Lai, N. Weissmann, W. Seeger, and F. Grimminger. 2005. Reversal of experimental pulmonary hypertension by PDGF inhibition. J. Clin. Invest. 115:2811-2821. http://dx.doi.org/10.1172/JCI24838
69. Screaton, G.R., J. Mongkolsapaya, X.N. Xu, A.E. Cowper, A.J. McMichael, and J.I. Bell. 1997. TRICK2, a new alternatively spliced receptor that transduces the cytotoxic signal from TRAIL. Curr. Biol. 7:693-696. http://dx.doi.org/10.1016/S0960-9822(06)00297-1
70. Secchiero, P., A. Gonelli, E. Carnevale, D. Milani, A. Pandolfi, D. Zella, and G. Zauli. 2003. TRAIL promotes the survival and proliferation of primary human vascular endothelial cells by activating the Akt and ERK pathways. Circulation. 107:2250-2256. http://dx.doi.org/10.1161/01.CIR.0000062702.60708.C4
71. Secchiero, P., C. Zerbinati, E. Rimondi, F. Corallini, D. Milani, V. Grill, G. Forti, S. Capitani, and G. Zauli. 2004. TRAIL promotes the survival, migration and proliferation of vascular smooth muscle cells. Cell. Mol. Life Sci. 61:1965-1974. http://dx.doi.org/10.1007/s00018004-4197-6
72. Secchiero, P., E. Melloni, F. Corallini, A.P. Beltrami, F. Alviano, D. Milani, F. D'Aurizio, M.G. di Iasio, D. Cesselli, G.P. Bagnara, and G. Zauli. 2008. Tumor necrosis factor-related apoptosis-inducing ligand promotes migration of human bone marrow multipotent stromal cells. Stem Cells. 26:2955-2963. http://dx.doi.org/10.1634/stemcells.2008-0512
73. Simoncini, S., M.-S. Njock, S. Robert, L. Camoin-Jau, J. Sampol, J.-R. Harlé, C. Nguyen, F. Dignat-George, and F. Anfosso. 2009. TRAIL/Apo2L mediates the release of procoagulant endothelial microparticles induced by thrombin in vitro: a potential mechanism linking inflammation and coagulation. Circ. Res. 104:943-951. http://dx.doi.org/10.1161/CIRCRESAHA.108.183285
74. Song, S., K. Choi, S.-W. Ryu, S.W. Kang, and C. Choi. 2011. TRAIL promotes caspase-dependent pro-inflammatory responses via PKCδ activation by vascular smooth muscle cells. Cell Death Dis. 2:e223. http://dx.doi.org/10.1038/cddis.2011.103
75. Spiekerkoetter, E., C. Guignabert, V. de Jesus Perez, T.-P. Alastalo, J.M. Powers, L. Wang, A. Lawrie, N. Ambartsumian, A.-M. Schmidt, M. Berryman, et al. 2009. S100A4 and bone morphogenetic protein-2 codependently induce vascular smooth muscle cell migration via phospho-extracellular signalregulated kinase and chloride intracellular channel 4. Circ. Res. 105:639-647: 13: 647. http://dx.doi.org/10.1161/CIRCRESAHA.109.205120
76. Steiner, M.K., O.L. Syrkina, N. Kolliputi, E.J. Mark, C.A. Hales, and A.B. Waxman. 2009. Interleukin-6 overexpression induces pulmonary hypertension. Circ. Res. 104:236-244: 28p: 244. http://dx.doi.org/10.1161/CIRCRESAHA.108.182014
77. Tang, W., W. Wang, Y. Zhang, S. Liu, Y. Liu, and D. Zheng. 2009. TRAIL receptor mediates inflammatory cytokine release in an NF-kappaBdependent manner. Cell Res. 19:758-767. http://dx.doi.org/10.1038/cr.2009.57
78. Tu, L., L. Dewachter, B. Gore, E. Fadel, P. Dartevelle, G. Simonneau, M. Humbert, S. Eddahibi, and C. Guignabert. 2011. Autocrine fibroblast growth factor-2 signaling contributes to altered endothelial phenotype in pulmonary hypertension. Am. J. Respir. Cell Mol. Biol. 45:311-322. http://dx.doi.org/10.1165/rcmb.2010-0317OC
79. Wagner, M., K. Schmelz, B. Dörken, and I. Tamm. 2008. Transcriptional regulation of human survivin by early growth response (Egr)-1 transcription factor. Int. J. Cancer. 122:1278-1287. http://dx.doi.org/10.1002/ijc.23183
80. Walczak, H., M.A. Degli-Esposti, R.S. Johnson, P.J. Smolak, J.Y. Waugh, N. Boiani, M.S. Timour, M.J. Gerhart, K.A. Schooley, C.A. Smith, et al. 1997. TRAIL-R2: a novel apoptosis-mediating receptor for TRAIL. EMBO J. 16:5386-5397. http://dx.doi.org/10.1093/emboj/16.17.5386
81. Wang, P., Y. Lu, C. Li, N. Li, P. Yu, and D. Ma. 2011. Novel transcript variants of TRAIL show different activities in activation of NF-κB and apoptosis. Life Sci. 89:839-846. http://dx.doi.org/10.1016/j.lfs.2011.09.003
82. Watt, V., J. Chamberlain, T. Steiner, S. Francis, and D. Crossman. 2011. TRAIL attenuates the development of atherosclerosis in apolipoprotein E deficient mice. Atherosclerosis. 215:348-354. http://dx.doi.org/10.1016/j.atherosclerosis.2011.01.010
83. Wiley, S.R., K. Schooley, P.J. Smolak, W.S. Din, C.P. Huang, J.K. Nicholl, G.R. Sutherland, T.D. Smith, C. Rauch, C.A. Smith, et al. 1995. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity. 3:673-682. http://dx.doi.org/10.1016/1074-7613(95)90057-8
84. Wu, G.S. 2009. TRAIL as a target in anti-cancer therapy. Cancer Lett. 285:1-5. http://dx.doi.org/10.1016/j.canlet.2009.02.029
85. Wu, G.S., T.F. Burns, Y. Zhan, E.S. Alnemri, and W.S. El-Deiry. 1999. Molecular cloning and functional analysis of the mouse homologue of the KILLER/DR5 tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor. Cancer Res. 59:2770-2775.
86. Xu, Y., F. Toure, W. Qu, L. Lin, F. Song, X. Shen, R. Rosario, J. Garcia, A.-M. Schmidt, and S.-F. Yan. 2010. Advanced glycation end product (AGE)receptor for AGE (RAGE) signaling and up-regulation of Egr-1 in hypoxic macrophages. J. Biol. Chem. 285:23233-23240. http://dx.doi.org/10.1074/jbc.M110.117457
87. Yang, X., L. Long, M. Southwood, N. Rudarakanchana, P.D. Upton, T.K. Jeffery, C. Atkinson, H. Chen, R.C. Trembath, and N.W. Morrell. 2005. Dysfunctional Smad signaling contributes to abnormal smooth muscle cell proliferation in familial pulmonary arterial hypertension. Circ. Res. 96:1053-1063. http://dx.doi.org/10.1161/01.RES.0000166926.54293.68
88. Zauli, G., and P. Secchiero. 2006. The role of the TRAIL/TRAIL receptors system in hematopoiesis and endothelial cell biology. Cytokine Growth Factor Rev. 17:245-257. http://dx.doi.org/10.1016/j.cytogfr.2006.04.002
89. Zou, W., X. Liu, P. Yue, F.R. Khuri, and S.-Y. Sun. 2007. PPARgamma ligands enhance TRAIL-induced apoptosis through DR5 upregulation and c-FLIP downregulation in human lung cancer cells. Cancer Biol. Ther. 6:99-106. http://dx.doi.org/10.4161/cbt.6.1.3555