Hypoxia regulates bone morphogenetic protein signaling through C-terminal-binding protein 1

Circulation Research

Volumn 99, Issue 3, 2006, Pages 240-247

  Wu, Xinqi ^a   Chang, Mun Seog ^a   Mitsialis, S Alex ^a   Kourembanas, Stella ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Bone morphogenetic protein; C terminal binding protein 1; Histone deacetylases; Hypoxia; Inhibitor of differentiation 1; Pulmonary hypertension

Indexed keywords

BINDING PROTEIN; BONE MORPHOGENETIC PROTEIN; CARBOXY TERMINAL BINDING PROTEIN 1; HISTONE DEACETYLASE; INHIBITOR OF DIFFERENTIATION 1; NICOTINAMIDE ADENINE DINUCLEOTIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTERY MUSCLE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY; SMOOTH MUSCLE FIBER; STIMULATION;

ALCOHOL OXIDOREDUCTASES; ANOXIA; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELLS, CULTURED; DNA-BINDING PROTEINS; HUMANS; HYPERTENSION, PULMONARY; INHIBITOR OF DIFFERENTIATION PROTEIN 1; MYOCYTES, SMOOTH MUSCLE; NAD; PHOSPHOPROTEINS; PULMONARY ARTERY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 33746801074     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000237021.65103.24     Document Type: Article

References (60)

1. Reddi AH. BMPs: actions in flesh and bone. Nat Med. 1997;3:837-839.
2. Balemans W, Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev Biol. 2002;250:231-250.
3. Dorai H, Vukicevic S, Sampath TK. Bone morphogenetic protein-7 (OP-1) inhibits smooth muscle cell proliferation and stimulates the expression of markers that are characteristic of SMC phenotype in vitro. J Cell Physiol. 2000;184:37-45.
4. Nakaoka T, Gonda K, Ogita T, Otawara-Hamamoto Y, Okabe F, Kira Y, Harii K, Miyazono K, Takuwa Y, Fujita T. Inhibition of rat vascular smooth muscle proliferation in vitro and in vivo by bone morphogenetic protein-2. J Clin Invest. 1997;100:2824-2832.
5. Rosenzweig BL, Immamura T, Okadome T, Cox GN. Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc Natl Acad Sci U S A. 1995;92:7632-7636.
6. Takeda K, Oida S, Ichijo H, Iimura T, Maruoka Y, Amagasa T, Sasaki S. Molecular cloning of rat bone morphogenetic protein (BMP) type IA receptor and its expression during ectopic bone formation induced by BMP. Biochem Biophys Res Commun. 1994:204;203-209.
7. Mishina Y, Suzuki A, Gilbert DJ, Copeland NG, Jenkins NA, Ueno N, Behringer RR. Genomic organization and chromosomal location of the mouse type I BMP-2/4 receptor. Biochem Biophys Res Commun. 1995:206;310-317.
8. Nishitoh H, Ichijo H, Kimura M, Matsumoto T, Makishima F, Yamaguchi A, Yamashita H, Enomoto S, Miyazono K. Identification of type I and type II serine/threonine kinase receptors for growth/differentiation factor-5. J Biol Chem. 1996;271:21345-21352.
9. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell. 2003;113:685-700.
10. Attisano L, Wrana JL. Signal transduction by the TGF-beta superfamily. Science. 2002;296:1646-1647.
11. Itoh F, Asao H, Sugamura K, Heldin CH, ten Dijke P, Itoh S. Promoting bone morphogenetic protein signaling through negative regulation of inhibitory Smads. EMBO J. 2001;20:4132-4142.
12. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, Miyazono K. Smad6 inhibits signalling by the TGF-β superfamily. Nature. 1997;389:622-626.
13. Ishisaki A, Yamato K, Hashimoto S, Nakao A, Tamaki K, Nonaka K, ten Dijke P, Sugino H, Nishihara T. Differential inhibition of Smad6 and Smad7 on bone morphogenetic protein- and activin-mediated growth arrest and apoptosis in B cells. J Biol Chem. 1999;274:13637-13642.
14. Lin X, Liang YY, Sun B, Liang M, Shi Y, Brunicardi FC, Shi Y, Feng XH. Smad6 recruits transcription corepressor CtBP to repress bone morphogenetic protein-induced transcription. Mol Cell Biol. 2003;23:9081-9093.
15. Wotton D, Knoepfler PS, Laherty CD, Eisenman RN, Massague J. The Smad transcriptional corepressor TGIF recruits mSin3. Cell Growth Differ. 2001;12:457-463.
16. Wotton D, Lo RS, Lee S, Massague J. A Smad transcriptional corepressor. Cell. 1999;97:29-39.
17. Long J, Matsuura I, He D, Wang G, Shuai K, Liu F. Repression of Smad transcriptional activity by PIASy, an inhibitor of activated STAT. Proc Natl Acad Sci U S A. 2003;100:9791-9796.
18. Postigo AA, Dean DC. ZEB represses transcription through interaction with the corepressor CtBP. Proc Natl Acad Sci U S A. 1999;96:6683-6688.
19. Postigo AA. Opposing functions of ZEB proteins in the regulation of the TGFbeta/BMP signaling pathway. EMBO J. 2003;22:2443-2452.
20. Postigo AA, Depp JL, Taylor JJ, Kroll KL. Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins. EMBO J. 2003;22:2453-2462.
21. Kim DW, Lassar AB. Smad-dependent recruitment of a histone deacetylase/Sin3A complex modulates the bone morphogenetic protein-dependent transcriptional repressor activity of Nkx3.2. Mol Cell Biol. 2003;23:8704-8717.
22. Shi Y, Sawada J, Sui G, Affar B, Whetstine JR, Lan F, Ogawa H, Luke MP, Nakatani Y, Shi Y. Coordinated histone modifications mediated by a CtBP corepressor complex. Nature. 2003;422:735-738.
23. Chinnadurai G. CtBP family proteins: more than transcriptional corepressors. Bioessays. 2003;25:9-12.
24. Chinnadurai G. CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol Cell. 2000;9:213-224.
25. Zhang Q, Piston DW, Goodman RH. Regulation of corepressor function by nuclear NADH. Science. 2002;295:1895-1897.
26. Balasubramanian P, Zhao LJ, Chinnadurai G. Nicotinamide adenine dinucleotide stimulates oligomerization, interaction with adenovirus E1A and an intrinsic dehydrogenase activity of CtBP. FEBS Lett. 2003;537:157-160.
27. Kumar V, Carlson JE, Ohgi KA, Edwards TA, Rose DW, Escalante CR, Rosenfeld MG, Aggarwal AK. Transcription corepressor CtBP is an NAD(+)-regulated dehydrogenase. Mol Cell. 2002;10:857-869.
28. Fjeld CC, Birdsong WT, Goodman RH. Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor. Proc Natl Acad Sci U S A. 2003;100:9202-9207.
29. 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. 2000;67:737-744.
30. 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. Nat Genet. 2000;26:81-84.
31. Thomson JR, Machado RD, Pauciulo MW, Morgan NV, Humbert M, Elliott GC, Ward K, Yacoub M, Mikhail G, Rogers P, Newman J, Wheeler L, Higenbottam T, Gibbs JS, Egan J, Crozier A, Peacock A, Allcock R, Corris P, Loyd JE, Trembath RC, Nichols WC. Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-beta family. J Med Genet. 2000;37:741-745.
32. Machado RD, Pauciulo MW, Thomson JR, Lane KB, Morgan NV, Wheeler L, Phillips JA 3rd, Newman J, Williams D, Galie N, Manes A, McNeil K, Yacoub M, Mikhail G, Rogers P, Corris P, Humbert M, Donnai D, Martensson G, Tranebjaerg L, Loyd JE, Trembath RC, Nichols WC. BMPR2 haploinsufficiency as the inherited molecular mechanism for primary pulmonary hypertension. Am J Hum Genet. 2001;68:92-102.
33. Nishihara A, Watabe T, Imamura T, Miyazono K. Functional heterogeneity of bone morphogenetic protein receptor-II mutants found in patients with primary pulmonary hypertension. Mol Biol Cell. 2002;13:3055-3063.
34. Rudarakanchana N, Flanagan JA, Chen H, Upton PD, Machado R, Patel D, Trembath RC, Morrell NW. Functional analysis of bone morphogenetic protein type II receptor mutations underlying primary pulmonary hypertension. Hum Mol Genet. 2002;11:1517-1525.
35. 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. 2002;105:1672-16788.
36. Kourembanas S. Hypoxia and carbon monoxide in the vasculature. Antioxid Redox Signal. 2002;4:291-299.
37. 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.
38. Yet SF, Perrella MA, Layne MD, Hsieh CM, Maemura K, Kobzik L, Wiesel P, Christou H, Kourembanas S, Lee ME. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest. 1999;103:R23-R29.
39. Christou H, Yoshida A, Arthur V, Morita T, Kourembanas S. Increased vascular endothelial growth factor production in the lungs of rats with hypoxia-induced pulmonary hypertension. Am J Respir Cell Mol Biol. 1998;18:768-776.
40. Arrigoni FI, Vallance P, Haworth SG, Leiper JM. Metabolism of asymmetric dimethylarginines is regulated in the lung developmentally and with pulmonary hypertension induced by hypobaric hypoxia. Circulation. 2003;107:1195-1201.
41. Miyazono K, Miyazawa K. Id: A target of BMP signaling. Sci STKE. 2002;2002:PE40.
42. Ruzinova MB, Benezra R. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 2003;13:410-418.
43. Sikder HA, Devlin MK, Dunlap S, Ryu B, Alani RM. Id proteins in cell growth and tumorigenesis. Cancer Cell. 2003;3:525-530.
44. Yokota Y, Mori S. Role of Id family proteins in growth control. J Cell Physiol. 2002;190:21-28.
45. Norton JD. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci. 2002;113:3897-3905.
46. Norton JD, Deed RW, Craggs G, Sablitzky F. Id helix-loop-helix proteins in cell growth and differentiation. Trends Cell Biol. 2003;8:58-65.
47. Katagiri T, Imada M, Yanai T, Suda T, Takahashi N, Kamijo P. Identification of a BMP-responsive element in Id1, the gene for inhibition of myogenesis. Genes Cells. 2002;7:949-960.
48. Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A. 1998;95:11715-11720.
49. Wozney O, Benezra R, Noda M. Bone morphogenetic protein 2 transiently enhances expression of a gene, Id (inhibitor of differentiation), encoding a helix-loop-helix molecule in osteoblast-like cells. Proc Natl Acad Sci U S A. 1993;90:9219-9222.
50. Korchynskyi O, ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem. 2002;277:4883-4891.
51. López-Rovira T, Chalaux E, Massagué J, Rosa JL, Ventura F. Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J Biol Chem. 2002;277:3176-3185.
52. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Giallongo A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem. 1996;271:32529-32537.
53. Archer SL, Hung J, Henry T, Peterson D, Weir EK. A redox-based O2 sensor in rat pulmonary vasculature. Circ Res. 1993;73:1100-1112.
54. Shigemori K, Ishizaki T, Matsukawa S, Sakai A, Nakai T, Miyabo S. Adenine nucleotides via activation of ATP-sensitive K+ channels modulate hypoxic response in rat pulmonary artery. Am J Physiol Lung Cell Mol Physiol. 1996;270:L803-L809.
55. Wilson HL, Dipp M, Thomas JM, Lad C, Galione A, Evans AM. ADP-ribosyl cyclase and cyclic ADP-ribose hydrolase act as a redox sensor. A primary role for cyclic ADP-ribose in hypoxic pulmonary vasoconstriction. J Biol Chem. 2001;276:11180-11188.
56. Mirnezami AH, Campbell SJ, Darley M, Primrose JN, Johnson PW, Blaydes JP. Hdm2 recruits a hypoxia-sensitive corepressor to negatively regulate p53-dependent transcription. Curr Biol. 2003;13:1234-1239.
57. West J, Fagan K, Steudel W, Fouty B, Lane K, Harral J, Hoedt-Miller M, Tada Y, Ozimek J, Tuder R, Rodman DM. Pulmonary hypertension in transgenic mice expressing a dominant-negative BMPRII gene in smooth muscle. Circ Res. 2004;94:1109-1114.
58. Sheares KK, Jeffery TK, Long L, Yang X, Morrell NW. Differential effects of TGF-beta1 and BMP-4 on the hypoxic induction of cyclooxygenase-2 in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2004;287:L919-L927.
59. Frank BD, Abtahi A, Yamaguchi DJ, Manning S, Shyr Y, Pozzi A, Baldwin HS, Johnson JE, de Caestecker MP. Bone morphogenetic protein 4 promotes pulmonary vascular remodeling in hypoxic pulmonary hypertension. Circ Res. 2005;97:496-504.
60. Semenza GL. Perspectives on oxygen sensing. Cell. 1999;98:281-284.