Rapamycin inhibits transforming growth factor β-induced peritoneal angiogenesis by blocking the secondary hypoxic response

Journal of Cellular and Molecular Medicine

Volumn 16, Issue 8, 2012, Pages 1934-1945

  Sekiguchi, Yoshimi ^a,b   Zhang, Jing ^a   Patterson, Sarah ^a   Liu, Limin ^a   Hamada, Chieko ^b   Tomino, Yasuhiko ^b   Margetts, Peter J ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b JUNTENDO UNIVERSITY   (Japan)

Author keywords

Adenovirus; Angiogenesis; Hypoxia inducible factor; MTOR; Rapamycin; Smad; Transforming growth factor; Vascular endothelial growth factor

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; RAPAMYCIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN A;

ANIMAL; ARTICLE; C57BL MOUSE; CELL CULTURE; CELL HYPOXIA; DRUG EFFECT; EPITHELIUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PERITONEAL FIBROSIS; PERITONEUM; RAT; VASCULARIZATION;

ANIMALS; CELL HYPOXIA; CELLS, CULTURED; EPITHELIUM; GENE EXPRESSION REGULATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; PERITONEAL FIBROSIS; PERITONEUM; RATS; SIROLIMUS; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ADENOVIRIDAE; MUS;

EID: 84864390258     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2011.01493.x     Document Type: Article

References (55)

1. Davies SJ, Bryan J, Phillips L, et al Longitudinal changes in peritoneal kinetics: the effects of peritoneal dialysis and peritonitis. Nephrol Dial Transplant. 1996; 11: 498-506.
2. Flessner MF. The effect of fibrosis on peritoneal transport. Contrib Nephrol. 2006; 150: 174-80.
3. Brimble KS, Walker M, Margetts PJ, et al Meta-analysis: peritoneal membrane transport, mortality, and technique failure in peritoneal dialysis. J Am Soc Nephrol. 2006; 17: 2591-8.
4. Honda K, Hamada C, Nakayama M, et al Impact of uremia, diabetes, and peritoneal dialysis itself on the pathogenesis of peritoneal sclerosis: a quantitative study of peritoneal membrane morphology. Clin J Am Soc Nephrol. 2008; 3: 720-8.
5. Combet S, Ferrier ML, Van LM, et al Chronic uremia induces permeability changes, increased nitric oxide synthase expression, and structural modifications in the peritoneum. J Am Soc Nephrol. 2001; 12: 2146-57.
6. Moona SJ, Hana SH, Kim DK, et al Risk factors for adverse outcomes after peritonitis-related technique failure. Perit Dial Int. 2008; 28: 352-60.
7. Cho JH, Hur IK, Kim CD, et al Impact of systemic and local peritoneal inflammation on peritoneal solute transport rate in new peritoneal dialysis patients: a 1-year prospective study. Nephrol Dial Transplant. 2010; 25: 1964-73.
8. Lai KN, Lai KB, Szeto CC, et al Growth factors in continuous ambulatory peritoneal dialysis effluent. Their relation with peritoneal transport of small solutes. Am J Nephrol. 1999; 19: 416-22.
9. Gangji AS, Brimble KS, Margetts PJ. Association between markers of inflammation, fibrosis and hypervolemia in peritoneal dialysis patients. Blood Purif. 2009; 28: 354-8.
10. Margetts PJ, Kolb M, Galt T, et al Gene transfer of transforming growth factor-beta1 to the rat peritoneum: effects on membrane function. J Am Soc Nephrol. 2001; 12: 2029-39.
11. Yanez-Mo M, Lara-Pezzi E, Selgas R, et al Peritoneal dialysis and epithelial-to-mesenchymal transition of mesothelial cells. N Engl J Med. 2003; 348: 403-13.
12. Margetts PJ, Bonniaud P, Liu L, et al Transient overexpression of TGF-{beta}1 induces epithelial mesenchymal transition in the rodent peritoneum. J Am Soc Nephrol. 2005; 16: 425-36.
13. Liao D, Johnson RS. Hypoxia: a key regulator of angiogenesis in cancer. Cancer Metastasis Rev. 2007; 26: 281-90.
14. Fine LG, Norman JT. Chronic hypoxia as a mechanism of progression of chronic kidney diseases: from hypothesis to novel therapeutics. Kidney Int. 2008; 74: 867-72.
15. Higgins DF, Kimura K, Bernhardt WM, et al Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest. 2007; 117: 3810-20.
16. Maxwell P. HIF-1: an oxygen response system with special relevance to the kidney. J Am Soc Nephrol. 2003; 14: 2712-22.
17. Corpechot C, Barbu V, Wendum D, et al Hypoxia-induced VEGF and collagen I expressions are associated with angiogenesis and fibrogenesis in experimental cirrhosis. Hepatology. 2002; 35: 1010-21.
18. Cosgrove GP, Brown KK, Schiemann WP, et al Pigment epithelium-derived factor in idiopathic pulmonary fibrosis: a role in aberrant angiogenesis. Am J Respir Crit Care Med. 2004; 170: 242-51.
19. Manotham K, Tanaka T, Matsumoto M, et al Evidence of tubular hypoxia in the early phase in the remnant kidney model. J Am Soc Nephrol. 2004; 15: 1277-88.
20. Nakagawa T, Lan HY, Zhu HJ, et al Differential regulation of VEGF by TGF-beta and hypoxia in rat proximal tubular cells. Am J Physiol Renal Physiol. 2004; 287: F658-64.
21. Zhou G, Dada LA, Wu M, et al Hypoxia-induced alveolar epithelial-mesenchymal transition requires mitochondrial ROS and hypoxia-inducible factor 1. Am J Physiol Lung Cell Mol Physiol. 2009; 297: L1120-30.
22. Moon JO, Welch TP, Gonzalez FJ, et al Reduced liver fibrosis in hypoxia-inducible factor-1alpha-deficient mice. Am J Physiol Gastrointest Liver Physiol. 2009; 296: G582-92.
23. Lundgren K, Nordenskjold B, Landberg G. Hypoxia, Snail and incomplete epithelial-mesenchymal transition in breast cancer. Br J Cancer. 2009; 101: 1769-81.
24. Huang CH, Yang WH, Chang SY, et al Regulation of membrane-type 4 matrix metalloproteinase by SLUG contributes to hypoxia-mediated metastasis. Neoplasia. 2009; 11: 1371-82.
25. Sun S, Ning X, Zhang Y, et al Hypoxia-inducible factor-1alpha induces Twist expression in tubular epithelial cells subjected to hypoxia, leading to epithelial-to-mesenchymal transition. Kidney Int. 2009; 75: 1278-87.
26. Hudson CC, Liu M, Chiang GG, et al Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin. Mol Cell Biol. 2002; 22: 7004-14.
27. Guba M, von Breitenbuch P, Steinbauer M, et al Rapamycin inhibits primary and metastatic tumour growth by antiangiogenesis: involvement of vascular endothelial growth factor. Nat Med. 2002; 8: 128-35.
28. Lloberas N, Cruzado JM, Franquesa M, et al Mammalian target of rapamycin pathway blockade slows progression of diabetic kidney disease in rats. J Am Soc Nephrol. 2006; 17: 1395-404.
29. Wu MJ, Wen MC, Chiu YT, et al Rapamycin attenuates unilateral ureteral obstruction-induced renal fibrosis. Kidney Int. 2006; 69: 2029-36.
30. Zhu J, Wu J, Frizell E, et al Rapamycin inhibits hepatic stellate cell proliferation in vitro and limits fibrogenesis in an in vivo model of liver fibrosis. Gastroenterology. 1999; 117: 1198-204.
31. Yoshizaki A, Yanaba K, Yoshizaki A, et al Treatment with rapamycin prevents fibrosis in tight-skin and bleomycin-induced mouse models of systemic sclerosis. Arthritis Rheum. 2010; 62: 2476-87.
32. Duman S, Bozkurt D, Sipahi S, et al Effects of everolimus as an antiproliferative agent on regression of encapsulating peritoneal sclerosis in a rat model. Adv Perit Dial. 2008; 24: 104-10.
33. Aguilera A, Aroeira LS, Ramirez-Huesca M, et al Effects of rapamycin on the epithelial-to-mesenchymal transition of human peritoneal mesothelial cells. Int J Artif Organs. 2005; 28: 164-9.
34. Patel P, West-Mays J, Kolb M, et al Platelet derived growth factor B and epithelial mesenchymal transition of peritoneal mesothelial cells. Matrix Biol. 2010; 29: 97-106.
35. Cina DP, Xu H, Liu L, et al Renal tubular angiogenic dysregulation in anti-Thy1.1 glomerulonephritis. Am J Physiol Renal Physiol. 2011; 300: F488-98.
36. Sime PJ, Xing Z, Graham FL, et al Adenovector-mediated gene transfer of active transforming growth factor-beta1 induces prolonged severe fibrosis in rat lung. J Clin Invest. 1997; 100: 768-76.
37. Kelly BD, Hackett SF, Hirota K, et al Cell type-specific regulation of angiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1. Circ Res. 2003; 93: 1074-81.
38. Bonniaud P, Margetts PJ, Kolb M, et al Adenoviral gene transfer of connective tissue growth factor in the lung induces transient fibrosis. Am J Respir Crit Care Med. 2003; 168: 770-8.
39. Yang X, Letterio JJ, Lechleider RJ, et al Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-beta. EMBO J. 1999; 18: 1280-91.
40. Rosenberger C, Rosen S, Paliege A, et al Pimonidazole adduct immunohistochemistry in the rat kidney: detection of tissue hypoxia. Methods Mol Biol. 2009; 466: 161-74.
41. Farkas L, Farkas D, Ask K, et al VEGF ameliorates pulmonary hypertension through inhibition of endothelial apoptosis in experimental lung fibrosis in rats. J Clin Invest. 2009; 119: 1298-311.
42. McMahon S, Charbonneau M, Grandmont S, et al Transforming growth factor beta1 induces hypoxia-inducible factor-1 stabilization through selective inhibition of PHD2 expression. J Biol Chem. 2006; 281: 24171-81.
43. Basu RK, Hubchak SC, Hayashida T, et al Interdependence of HIF-1{alpha} and TGF-{beta}/Smad3 signaling in normoxic and hypoxic renal epithelial cell collagen expression. Am J Physiol Renal Physiol. 2011; 300: F898-905.
44. Copple BL, Bustamante JJ, Welch TP, et al Hypoxia-inducible factor-dependent production of profibrotic mediators by hypoxic hepatocytes. Liver Int. 2009; 29: 1010-21.
45. Suzuki A, Kusakai G, Shimojo Y, et al Involvement of transforming growth factor-beta 1 signaling in hypoxia-induced tolerance to glucose starvation. J Biol Chem. 2005; 280: 31557-63.
46. Chen CP, Yang YC, Su TH, et al Hypoxia and transforming growth factor-beta 1 act independently to increase extracellular matrix production by placental fibroblasts. J Clin Endocrinol Metab. 2005; 90: 1083-90.
47. Patel P, Sekiguchi Y, Oh KH, et al Smad3-dependent and -independent pathways are involved in peritoneal membrane injury. Kidney Int. 2010; 77: 319-28.
48. Dong J, Peng J, Zhang H, et al Role of glycogen synthase kinase 3beta in rapamycin-mediated cell cycle regulation and chemosensitivity. Cancer Res. 2005; 65: 1961-72.
49. Wang S, Wilkes MC, Leof EB, et al Noncanonical TGF-beta pathways, mTORC1 and Abl, in renal interstitial fibrogenesis. Am J Physiol Renal Physiol. 2010; 298: F142-9.
50. Kramer S, Wang-Rosenke Y, Scholl V, et al Low-dose mTOR inhibition by rapamycin attenuates progression in anti-thy1-induced chronic glomerulosclerosis of the rat. Am J Physiol Renal Physiol. 2008; 294: F440-9.
51. Lamouille S, Derynck R. Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J Cell Biol. 2007; 178: 437-51.
52. Yoshizaki A, Yanaba K, Yoshizaki A, et al Treatment with rapamycin prevents fibrosis in tight-skin and bleomycin-induced mouse models of systemic sclerosis. Arthritis Rheum. 2010; 62: 2476-87.
53. Poulalhon N, Farge D, Roos N, et al Modulation of collagen and MMP-1 gene expression in fibroblasts by the immunosuppressive drug rapamycin. A direct role as an antifibrotic agent?J Biol Chem. 2006; 281: 33045-52.
54. Neef M, Ledermann M, Saegesser H, et al Low-dose oral rapamycin treatment reduces fibrogenesis, improves liver function, and prolongs survival in rats with established liver cirrhosis. J Hepatol. 2006; 45: 786-96.
55. Lock HR, Sacks SH, Robson MG. Rapamycin at subimmunosuppressive levels inhibits mesangial cell proliferation and extracellular matrix production. Am J Physiol Renal Physiol. 2007; 292: F76-81.