Nitric oxide and carbon monoxide antagonize TGF-β through ligandindependent internalization of TβR1/ALK5

American Journal of Physiology - Renal Physiology

Volumn 307, Issue 6, 2014, Pages F727-F735

  Hovater, Michael B ^b   Ying, Wei Zhong ^b   Agarwal, Anupam ^a,b,c,d,e   Sanders, Paul W ^a,b,c,e  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

Activin receptor like kinase 5; Carbon monoxide; Dynamin 2; Nitric oxide; Transforming growth factor ; Vascular smooth muscle

Indexed keywords

CARBON MONOXIDE; DYNAMIN II; NITRIC OXIDE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; NERVE PROTEIN; PROTEIN SERINE THREONINE KINASE; T BOX TRANSCRIPTION FACTOR; TBR-1 PROTEIN, RAT; TGF-BETA TYPE I RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; INTERNALIZATION; INTRACELLULAR SIGNALING; NONHUMAN; PRIMARY CULTURE; PROTEIN EXPRESSION; RAT; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VASCULARIZATION; ANIMAL; MALE; METABOLISM; POLYMERIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; CARBON MONOXIDE; DYNAMIN II; MALE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NERVE TISSUE PROTEINS; NITRIC OXIDE; POLYMERIZATION; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; T-BOX DOMAIN PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84907143739     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00353.2014     Document Type: Article

References (62)

1. Bolognesi M, Sacerdoti D, Piva A, Di Pascoli M, Zampieri F, Quarta S, Motterlini R, Angeli P, Merkel C, Gatta A. Carbon monoxidemediated activation of large-conductance calcium-activated potassium channels contributes to mesenteric vasodilatation in cirrhotic rats. J Pharmacol Exp Ther 321: 187–194, 2007.
2. Brouard S, Otterbein LE, Anrather J, Tobiasch E, Bach FH, Choi AM, Soares MP. Carbon monoxide generated by heme oxygenase 1 suppresses endothelial cell apoptosis. J Exp Med 192: 1015–1026, 2000.
3. Brown KA, Pietenpol JA, Moses HL. A tale of two proteins: differential roles and regulation of Smad2 and Smad3 in TGF-β signaling. J Cell Biochem 101: 9–33, 2007.
4. Cao S, Yao J, McCabe TJ, Yao Q, Katusic ZS, Sessa WC, Shah V. Direct interaction between endothelial nitric-oxide synthase and dynamin- 2. Implications for nitric-oxide synthase function. J Biol Chem 276: 14249–14256, 2001.
5. Cepinskas G, Katada K, Bihari A, Potter RF. Carbon monoxide liberated from carbon monoxide-releasing molecule CORM-2 attenuates inflammation in the liver of septic mice. Am J Physiol Gastrointest Liver Physiol 294: G184–G191, 2008.
6. Chen CL, Hou WH, Liu IH, Hsiao G, Huang SS, Huang JS. Inhibitors of clathrin-dependent endocytosis enhance TGFβ signaling and responses. J Cell Sci 122: 1863–1871, 2009.
7. Christodoulides N, Durante W, Kroll MH, Schafer AI. Vascular smooth muscle cell heme oxygenases generate guanylyl cyclase-stimulatory carbon monoxide. Circulation 91: 2306–2309, 1995.
8. Davidge KS, Motterlini R, Mann BE, Wilson JL, Poole RK. Carbon monoxide in biology and microbiology: surprising roles for the “Detroit perfume”. Adv Microb Physiol 56: 85–167, 2009.
9. Dulak J, Deshane J, Jozkowicz A, Agarwal A. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis. Circulation 117: 231–241, 2008.
10. Frolik CA, Wakefield LM, Smith DM, Sporn MB. Characterization of a membrane receptor for transforming growth factor-beta in normal rat kidney fibroblasts. J Biol Chem 259: 10995–11000, 1984.
11. Guillen MI, Megias J, Clerigues V, Gomar F, Alcaraz MJ. The CO-releasing molecule CORM-2 is a novel regulator of the inflammatory process in osteoarthritic chondrocytes. Rheumatology (Oxford) 47: 1323-1328, 2008.
12. Gvaramia D, Blaauboer ME, Hanemaaijer R, Everts V. Role of caveolin-1 in fibrotic diseases. Matrix Biol 32: 307–315, 2013.
13. Hartung R, Parapuram SK, Ganti R, Hunt DM, Chalam KV, Hunt RC. Vitreous induces heme oxygenase-1 expression mediated by transforming growth factor-β and reactive oxygen species generation in human retinal pigment epithelial cells. Mol Vis 13: 66–78, 2007.
14. Hayes S, Chawla A, Corvera S. TGFβ receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2. J Cell Biol 158: 1239–1249, 2002.
15. Hill-Kapturczak N, Chang SH, Agarwal A. Heme oxygenase and the kidney. DNA Cell Biol 21: 307–321, 2002.
16. Hill-Kapturczak N, Truong L, Thamilselvan V, Visner GA, Nick HS, Agarwal A. Smad7-dependent regulation of heme oxygenase-1 by transforming growth factor-beta in human renal epithelial cells. J Biol Chem 275: 40904–40909, 2000.
17. Hovater MB, Sanders PW. Effect of dietary salt on regulation of TGF-β in the kidney. Semin Nephrol 32: 269–276, 2012.
18. Hyndman KA, Musall JB, Xue J, Pollock JS. Dynamin activates NO production in rat renal inner medullary collecting ducts via protein-protein interaction with NOS1. Am J Physiol Renal Physiol 301: F118–F124, 2011.
19. Inoue N, Venema RC, Sayegh HS, Ohara Y, Murphy TJ, Harrison DG. Molecular regulation of the bovine endothelial cell nitric oxide synthase by transforming growth factor-β 1. Arterioscler Thromb Vasc Biol 15: 1255–1261, 1995.
20. Islam MS, Ohkuma H, Kimura M, Suzuki S. In vitro effects of new generation fungal derived nitric oxide donors on rabbit basilar artery. Neurol Med Chir (Tokyo) 43: 175–180, 2003.
21. Kanbay M, Chen Y, Solak Y, Sanders PW. Mechanisms and consequences of salt sensitivity and dietary salt intake. Curr Opin Nephrol Hypertens 20: 37–43, 2011.
22. Kang-Decker N, Cao S, Chatterjee S, Yao J, Egan LJ, Semela D, Mukhopadhyay D, Shah V. Nitric oxide promotes endothelial cell survival signaling through S-nitrosylation and activation of dynamin-2. J Cell Sci 120: 492–501, 2007.
23. Kim SI, Na HJ, Ding Y, Wang Z, Lee SJ, Choi ME. Autophagy promotes intracellular degradation of type I collagen induced by transforming growth factor (TGF)-β1. J Biol Chem 287: 11677–11688, 2012.
24. Kita Y, Hirasawa Y, Maeda K, Nishio M, Yoshida K. Spontaneous nitric oxide release accounts for the potent pharmacological actions of FK409. Eur J Pharmacol 257: 123–130, 1994.
25. Kutty RK, Nagineni CN, Kutty G, Hooks JJ, Chader GJ, Wiggert B. Increased expression of heme oxygenase-1 in human retinal pigment epithelial cells by transforming growth factor- β. J Cell Physiol 159: 371–378, 1994.
26. Lan TH, Huang XQ, Tan HM. Vascular fibrosis in atherosclerosis. Cardiovasc Pathol 22: 401–407, 2013.
27. Leffler CW, Parfenova H, Jaggar JH. Carbon monoxide as an endogenous vascular modulator. Am J Physiol Heart Circ Physiol 301: H1–H11, 2011.
28. Litteri G, Carnevale D, D’Urso A, Cifelli G, Braghetta P, Damato A, Bizzotto D, Landolfi A, Ros FD, Sabatelli P, Facchinello N, Maffei A, Volpin D, Colombatti A, Bressan GM, Lembo G. Vascular smooth muscle emilin-1 is a regulator of arteriolar myogenic response and blood pressure. Arterioscler Thromb Vasc Biol 32: 2178–2184, 2012.
29. Loboda A, Jazwa A, Grochot-Przeczek A, Rutkowski AJ, Cisowski J, Agarwal A, Jozkowicz A, Dulak J. Heme oxygenase-1 and the vascular bed: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 10: 1767–1812, 2008.
30. Lu J, Katano T, Uta D, Furue H, Ito S. Rapid S-nitrosylation of actin by NO-generating donors and in inflammatory pain model mice. Mol Pain 7: 101, 2011.
31. Massague J, Attisano L, Wrana JL. The TGF-β family and its composite receptors. Trends Cell Biol 4: 172–178, 1994.
32. Megias J, Busserolles J, Alcaraz MJ. The carbon monoxide-releasing molecule CORM-2 inhibits the inflammatory response induced by cytokines in Caco-2 cells. Br J Pharmacol 150: 977–986, 2007.
33. Meyer C, Godoy P, Bachmann A, Liu Y, Barzan D, Ilkavets I, Maier P, Herskind C, Hengstler JG, Dooley S. Distinct role of endocytosis for Smad and non-Smad TGF-β signaling regulation in hepatocytes. J Hepatol 55: 369–378, 2011.
34. Morita T, Mitsialis SA, Koike H, Liu Y, Kourembanas S. Carbon monoxide controls the proliferation of hypoxic vascular smooth muscle cells. J Biol Chem 272: 32804–32809, 1997.
35. Motterlini R, Clark JE, Foresti R, Sarathchandra P, Mann BE, Green CJ. Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ Res 90: E17–24, 2002.
36. 2+ oscillation in pancreatic acini. Nitric Oxide 24: 139–150, 2011.
37. Moustakas A, Heldin CH. Non-Smad TGF-β signals. J Cell Sci 118: 3573–3584, 2005.
38. Moustakas A, Heldin CH. The regulation of TGFβ signal transduction. Development 136: 3699–3714, 2009.
39. Nakamura T, Matsushima M, Hayashi Y, Shibasaki M, Imaizumi K, Hashimoto N, Shimokata K, Hasegawa Y, Kawabe T. Attenuation of transforming growth factor-β-stimulated collagen production in fibroblasts by quercetin-induced heme oxygenase-1. Am J Respir Cell Mol Biol 44: 614–620, 2011.
40. Ramos KS, Lin H, McGrath JJ. Modulation of cyclic guanosine monophosphate levels in cultured aortic smooth muscle cells by carbon monoxide. Biochem Pharmacol 38: 1368–1370, 1989.
41. Ryan ST, Koteliansky VE, Gotwals PJ, Lindner V. Transforming growth factor-β-dependent events in vascular remodeling following arterial injury. J Vasc Res 40: 37–46, 2003.
42. Ryter SW, Otterbein LE. Carbon monoxide in biology and medicine. Bioessays 26: 270–280, 2004.
43. Sanders PW. Vascular consequences of dietary salt intake. Am J Physiol Renal Physiol 297: F237–F243, 2009.
44. Sarzani R, Brecher P, Chobanian AV. Growth factor expression in aorta of normotensive and hypertensive rats. J Clin Invest 83: 1404–1408, 1989.
45. Schwer CI, Stoll P, Rospert S, Fitzke E, Schallner N, Burkle H, Schmidt R, Humar M. Carbon monoxide releasing molecule-2 CORM-2 represses global protein synthesis by inhibition of eukaryotic elongation factor eEF2. Int J Biochem Cell Biol 45: 201–212, 2013.
46. Seki J, Nishio M, Kato Y, Motoyama Y, Yoshida K. FK409, a new nitric-oxide donor, suppresses smooth muscle proliferation in the rat model of balloon angioplasty. Atherosclerosis 117: 97–106, 1995.
47. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61: 748–755, 1968.
48. Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase. Characterization of the enzyme. J Biol Chem 244: 6388–6394, 1969.
49. Tracz MJ, Alam J, Nath KA. Physiology and pathophysiology of heme: implications for kidney disease. J Am Soc Nephrol 18: 414–420, 2007.
50. Wang G, Moniri NH, Ozawa K, Stamler JS, Daaka Y. Nitric oxide regulates endocytosis by S-nitrosylation of dynamin. Proc Natl Acad Sci USA 103: 1295–1300, 2006.
51. Wang Z, Humphrey C, Frilot N, Wang G, Nie Z, Moniri NH, Daaka Y. Dynamin2- and endothelial nitric oxide synthase-regulated invasion of bladder epithelial cells by uropathogenic Escherichia coli. J Cell Biol 192: 101–110, 2011.
52. 2+-dependent big-conductance K channels in the cortical collecting duct. Am J Physiol Renal Physiol 304: F543–F552, 2013.
53. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J. Mechanism of activation of the TGF-β receptor. Nature 370: 341–347, 1994.
54. Ying WZ, Aaron KJ, Sanders PW. Transforming growth factor-β regulates endothelial function during high salt intake in rats. Hypertension 62: 951–956, 2013.
55. Ying WZ, Sanders PW. Dietary salt enhances glomerular endothelial nitric oxide synthase through TGF-β1. Am J Physiol Renal Physiol 275: F18–F24, 1998.
56. Ying WZ, Sanders PW. Dietary salt increases endothelial nitric oxide synthase and TGF-β1 in rat aortic endothelium. Am J Physiol Heart Circ Physiol 277: H1293–H1298, 1999.
57. Ying WZ, Sanders PW. Enhanced expression of EGF receptor in a model of salt-sensitive hypertension. Am J Physiol Renal Physiol 289: F314–F321, 2005.
58. Ying WZ, Sanders PW. The interrelationship between TGF-β1 and nitric oxide is altered in salt-sensitive hypertension. Am J Physiol Renal Physiol 285: F902–F908, 2003.
59. Zarjou A, Agarwal A. Heme oxygenase-1 as a target for TGF-β in kidney disease. Semin Nephrol 32: 277–286, 2012.
60. Zhang YE. Non-Smad pathways in TGF-β signaling. Cell Res 19: 128–139, 2009.
61. Zhu L, Herrera GA, White CR, Sanders PW. Immunoglobulin light chain alters mesangial cell calcium homeostasis. Am J Physiol Renal Physiol 272: F319–F324, 1997.
62. Zrelli H, Wu CW, Zghonda N, Shimizu H, Miyazaki H. Combined treatment of hydroxytyrosol with carbon monoxide-releasing molecule-2 prevents TNFκ-induced vascular endothelial cell dysfunction through NO production with subsequent NF B inactivation. Biomed Res Int 2013: 912431, 2013.