Endothelial indoleamine 2,3-dioxygenase protects against development of pulmonary hypertension

American Journal of Respiratory and Critical Care Medicine

Volumn 188, Issue 4, 2013, Pages 482-491

  Xiao, Yongguang ^a   Christou, Helen ^a,b   Liu, Li ^b   Visner, Gary ^a   Mitsialis, S Alex ^a   Kourembanas, Stella ^a,b   Liu, Hanzhong ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Gene therapy; Smooth muscle cells; Vascular remodeling

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; MONOCROTALINE; MYOCARDIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; DNA SEQUENCE; DOWN REGULATION; ENDOTHELIUM; ENDOTHELIUM CELL; ENZYME SYNTHESIS; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; HEART RIGHT VENTRICLE HYPERTROPHY; HYPOXIA; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; SMOOTH MUSCLE FIBER; THERAPY EFFECT; TRANSGENE; VASCULAR SMOOTH MUSCLE;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; DNA TRANSPOSABLE ELEMENTS; ENDOTHELIUM, VASCULAR; ETS-DOMAIN PROTEIN ELK-1; HYPERTENSION, PULMONARY; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LUNG; MICE; MYOCYTES, SMOOTH MUSCLE; RATS; UP-REGULATION;

EID: 84882730241     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201304-0700OC     Document Type: Article

References (42)

1. Schermuly RT, Ghofrani HA, Wilkins MR, Grimminger F. Mechanisms of disease: pulmonary arterial hypertension. Nat Rev Cardiol 2011;8:443-455.
2. Wang J, Weigand L, Lu W, Sylvester JT, Semenza GL, Shimoda LA. Hypoxia inducible factor 1 mediates hypoxia-induced TRPC expression and elevated intracellular Ca21 in pulmonary arterial smooth muscle cells. Circ Res 2006;98:1528-1537.
3. Rios EJ, Fallon M, Wang J, Shimoda LA. Chronic hypoxia elevates intracellular pH and activates Na1/H1 exchange in pulmonary arterial smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2005;289:L867-L874.
4. Tian X, Vroom C, Ghofrani HA, Weissmann N, Bieniek E, Grimminger F, Seeger W, Schermuly RT, Pullamsetti SS. Phosphodiesterase 10A upregulation contributes to pulmonary vascular remodeling. PLoS ONE 2011;6:e18136.
5. Courboulin A, Tremblay VL, Barrier M, Meloche J, JacobMH, ChapolardM, Bisserier M, Paulin R, Lambert C, Provencher S, et al. Krüppel-like factor 5 contributes to pulmonary artery smooth muscle proliferation and resistance to apoptosis in human pulmonary arterial hypertension. Respir Res 2011;12:128.
6. Courboulin A, Paulin R, Giguère NJ, Saksouk N, Perreault T, Meloche J, Paquet ER, Biardel S, Provencher S, Côté J, et al. Role for miR-204 in human pulmonary arterial hypertension. J Exp Med 2011;208:535-548.
7. Li X, Zhang X, Leathers R, Makino A, Huang C, Parsa P, Macias J, Yuan JX, Jamieson SW, Thistlethwaite PA. Notch3 signaling promotes the development of pulmonary arterial hypertension. Nat Med 2009;15:1289-1297.
8. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 2004;84:767-801.
9. Hayashi T, Beck L, Rossetto C, Gong X, Takikawa O, Takabayashi K, Broide DH, Carson DA, Raz E. Inhibition of experimental asthma by indoleamine 2,3-dioxygenase. J Clin Invest 2004;114:270-279.
10. Iannitti RG, Carvalho A, Cunha C, De Luca A, Giovannini G, Casagrande A, Zelante T, Vacca C, Fallarino F, Puccetti P, et al. Th17/Treg imbalance in murine cystic fibrosis is linked to indoleamine 2,3-dioxygenase deficiency but corrected by kynurenines. Am J Respir Crit Care Med 2013;187:609-620.
11. Katz JB, Muller AJ, Prendergast GC. Indoleamine 2,3-dioxygenase in T-cell tolerance and tumoral immune escape. Immunol Rev 2008; 222:206-221.
12. Liu H, Liu L, Fletcher BS, Visner GA. Sleeping Beauty-based gene therapy with indoleamine 2,3-dioxygenase inhibits lung allograft fibrosis. FASEB J 2006;20:2384-2386.
13. Liu H, Liu L, Fletcher BS, Visner GA. Novel action of indoleamine 2,3- dioxygenase attenuating acute lung allograft injury. Am J Respir Crit Care Med 2006;173:566-572.
14. Wang Y, Liu H, McKenzie G, Witting PK, Stasch JP, Hahn M, Changsirivathanathamrong D, Wu BJ, Ball HJ, Thomas SR, et al. Kynurenine is an endothelium-derived relaxing factor produced during inflammation. Nat Med 2010;16:279-285.
15. Zhou W, Negash S, Liu J, Raj JU. Modulation of pulmonary vascular smooth muscle cell phenotype in hypoxia: role of cGMP-dependent protein kinase and myocardin. Am J Physiol Lung Cell Mol Physiol 2009;296:L780-L789.
16. Lockman K, Taylor JM, Mack CP. The histone demethylase, Jmjd1a, interacts with the myocardin factors to regulate SMC differentiation marker gene expression. Circ Res 2007;101:e115-e123.
17. Wang Z, Wang DZ, Hockemeyer D, McAnally J, Nordheim A, Olson EN. Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature 2004;428: 185-189.
18. Liu H, Liu L, Liu K, Bizargity P, Hancock WW, Visner GA. Reduced cytotoxic function of effector CD81 T cells is responsible for indoleamine 2,3-dioxygenase-dependent immune suppression. J Immunol 2009;183:1022-1031.
19. Dromparis P, Sutendra G, Michelakis ED. The role of mitochondria in pulmonary vascular remodeling. J Mol Med (Berl) 2010;88:1003-1010.
20. Liu H, Visner GA. Applications of Sleeping Beauty transposons for nonviral gene therapy. IUBMB Life 2007;59:374-379.
21. Iken K, Liu K, Liu H, Bizargity P, Wang L, Hancock WW, Visner GA. Indoleamine 2,3-dioxygenase and metabolites protect murine lung allografts and impair the calcium mobilization of T cells. Am J Respir Cell Mol Biol 2012;47:405-416.
22. Mellor AL, Baban B, Chandler P, Marshall B, Jhaver K, Hansen A, Koni PA, Iwashima M, Munn DH. Cutting edge: induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J Immunol 2003;171:1652-1655.
23. Vergadi E, Chang MS, Lee C, Liang OD, Liu X, Fernandez-Gonzalez A, Mitsialis SA, Kourembanas S. Early macrophage recruitment and alternative activation are critical for the later development of hypoxiainduced pulmonary hypertension. Circulation 2011;123:1986-1995.
24. Christou H, Morita T, Hsieh CM, Koike H, Arkonac B, Perrella MA, Kourembanas S. Prevention of hypoxia-induced pulmonary hypertension by enhancement of endogenous heme oxygenase-1 in the rat. Circ Res 2000;86:1224-1229.
25. Zhou H, Liu H, Porvasnik SL, Terada N, Agarwal A, Cheng Y, Visner GA. Heme oxygenase-1 mediates the protective effects of rapamycin in monocrotaline-induced pulmonary hypertension. Lab Invest 2006;86:62-71.
26. Liu L, Liu H, Visner G, Fletcher BS. Sleeping Beauty-mediated eNOS gene therapy attenuates monocrotaline-induced pulmonary hypertension in rats. FASEB J 2006;20:2594-2596.
27. Liu L, Sanz S, Heggestad AD, Antharam V, Notterpek L, Fletcher BS. Endothelial targeting of the Sleeping Beauty transposon within lung. Mol Ther 2004;10:97-105.
28. Liu H, Liu L, Visner GA. Nonviral gene delivery with indoleamine 2,3- dioxygenase targeting pulmonary endothelium protects against ischemiareperfusion injury. Am J Transplant 2007;7:2291-2300.
29. Majka S, Burnham E, Stenmark KR. Cell-based therapies in pulmonary hypertension: who, what, and when? Am J Physiol Lung Cell Mol Physiol 2011;301:L9-L11.
30. Archer SL, Weir EK, Wilkins MR. Basic science of pulmonary arterial hypertension for clinicians: new concepts and experimental therapies. Circulation 2010;121:2045-2066.
31. Michelakis ED, McMurtry MS, Wu XC, Dyck JR, Moudgil R, Hopkins TA, Lopaschuk GD, Puttagunta L, Waite R, Archer SL. Dichloroacetate, a metabolic modulator, prevents and reverses chronic hypoxic pulmonary hypertension in rats: role of increased expression and activity of voltage-gated potassium channels. Circulation 2002;105: 244-250.
32. Bonnet S, Rochefort G, Sutendra G, Archer SL, Haromy A, Webster L, Hashimoto K, Bonnet SN, Michelakis ED. The nuclear factor of activated T cells in pulmonary arterial hypertension can be therapeutically targeted. Proc Natl Acad Sci USA 2007;104:11418-11423.
33. Schermuly RT, Dony E, Ghofrani HA, Pullamsetti S, Savai R, Roth M, Sydykov A, Lai YJ, Weissmann N, Seeger W, et al. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest 2005;115:2811-2821.
34. Alastalo TP, Li M, Perez VdeJ, Pham D, Sawada H, Wang JK, Koskenvuo M, Wang L, Freeman BA, Chang HY, et al. Disruption of PPARg/b-catenin-mediated regulation of apelin impairs BMPinduced mouse and human pulmonary arterial EC survival. J Clin Invest 2011;121:3735-3746.
35. Uyttenhove C, Pilotte L, Théate I, Stroobant V, Colau D, Parmentier N, Boon T, Van den Eynde BJ. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3- dioxygenase. Nat Med 2003;9:1269-1274.
36. Zuckerbraun BS, Chin BY, Wegiel B, Billiar TR, Czsimadia E, Rao J, Shimoda L, Ifedigbo E, Kanno S, Otterbein LE. Carbon monoxide reverses established pulmonary hypertension. J Exp Med 2006;203: 2109-2119.
37. Tuder RM, Abman SH, Braun T, Capron F, Stevens T, Thistlethwaite PA, Haworth SG. Development and pathology of pulmonary hypertension. J Am Coll Cardiol 2009; 54(1, Suppl)S3-S9.
38. Masri FA, Xu W, Comhair SA, Asosingh K, Koo M, Vasanji A, Drazba J, Anand-Apte B, Erzurum SC. Hyperproliferative apoptosis-resistant endothelial cells in idiopathic pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol 2007;293:L548-L554.
39. McMurtry MS, Archer SL, Altieri DC, Bonnet S, Haromy A, Harry G, Bonnet S, Puttagunta L,Michelakis ED.Gene therapy targeting survivin selectively induces pulmonary vascular apoptosis and reverses pulmonary arterial hypertension. J Clin Invest 2005;115:1479-1491.
40. Ma W, Han W, Greer PA, Tuder RM, Toque HA, Wang KK, Caldwell RW, Su Y. Calpain mediates pulmonary vascular remodeling in rodent models of pulmonary hypertension, and its inhibition attenuates pathologic features of disease. J Clin Invest 2011;121:4548-4566.
41. Liu L, Liu H, Mah C, Fletcher BS. Indoleamine 2,3-dioxygenase attenuates inhibitor development in gene-therapy-treated hemophilia A mice. Gene Ther 2009;16:724-733.
42. Williams DA. Sleeping beauty vector system moves toward human trials in the United States. Mol Ther 2008;16:1515-1516.