Micro-RNA 21 inhibition of SMAD7 enhances fibrogenesis via leptin-mediated NADPH oxidase in experimental and human nonalcoholic steatohepatitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 308, Issue 4, 2015, Pages G298-G312

  Dattaroy, Diptadip ^a   Pourhoseini, Sahar ^a   Das, Suvarthi ^a   Alhasson, Firas ^a   Seth, Ratanesh Kumar ^a   Nagarkatti, Mitzi ^b   Michelotti, Gregory A ^c   Diehl, Anna Mae ^c   Chatterjee, Saurabh ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

NF kB; Nonalcoholic fatty liver disease; Ob ob; SMAD2 3 colocalization; SMAD7; Transforming growth factor

Indexed keywords

3 NITROTYROSINE; ALPHA SMOOTH MUSCLE ACTIN; BROMODICHLOROMETHANE; COLLAGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LEPTIN; MICRORNA 21; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; CYBB PROTEIN, HUMAN; CYBB PROTEIN, MOUSE; MEMBRANE PROTEIN; MICRORNA; NEUTROPHIL CYTOSOLIC FACTOR 1; PEROXYNITROUS ACID; RECEPTOR REGULATED SMAD PROTEIN; SMAD4 PROTEIN, MOUSE; SMAD7 PROTEIN, HUMAN; SMAD7 PROTEIN, MOUSE; TRIHALOMETHANE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL DIFFERENTIATION; CONTROLLED STUDY; DIET INDUCED OBESITY; DNA BINDING; EXPERIMENTAL LIVER FIBROSIS; FIBROBLAST; FIBROGENESIS; HEPATITIS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; KUPFFER CELL; LIVER HOMOGENATE; LIVER INJURY; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; STELLATE CELL; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CASE CONTROL STUDY; CELL NUCLEUS; DEFICIENCY; DISEASE MODEL; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; LIPID DIET; LIVER; METABOLISM; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; CASE-CONTROL STUDIES; CELL NUCLEUS; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; HUMANS; LEPTIN; LIVER; MALE; MEMBRANE GLYCOPROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; NADPH OXIDASE; NF-KAPPA B; NON-ALCOHOLIC FATTY LIVER DISEASE; OXIDATIVE STRESS; PEROXYNITROUS ACID; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMAD PROTEINS, RECEPTOR-REGULATED; SMAD4 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRIHALOMETHANES;

EID: 84922876430     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00346.2014     Document Type: Article

References (44)

1. Aschner Y, Khalifah AP, Briones N, Yamashita C, Dolgonos L, Young SK, Campbell MN, Riches DW, Redente EF, Janssen WJ, Henson PM, Sap J, Vacaresse N, Kapus A, McCulloch CA, Zemans RL, Downey GP. Protein tyrosine phosphatase alpha mediates profibrotic signaling in lung fibroblasts through TGF-beta responsiveness. Am J Pathol 184: 1489-1502, 2014.
2. Bataller R, Schwabe RF, Choi YH, Yang L, Paik YH, Lindquist J, Qian T, Schoonhoven R, Hagedorn CH, Lemasters JJ, Brenner DA. NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J Clin Invest 112: 1383-1394, 2003.
3. Chatterjee S, Ganini D, Tokar EJ, Kumar A, Das S, Corbett J, Kadiiska M, Waalkes M, Diehl AM, Mason RP. Leptin is key to peroxynitrite-mediated oxidative stress and Kupffer cell activation in experimental nonalcoholic steatohepatitis. J Hepatol 58: 778-7784, 2013.
4. Cheung O, Sanyal AJ. Role of microRNAs in non-alcoholic steatohepatitis. Curr Pharm Des 16: 1952-1957, 2010.
5. Choi SS, Syn WK, Karaca GF, Omenetti A, Moylan CA, Witek RP, Agboola KM, Jung Y, Michelotti GA, Diehl AM. Leptin promotes the myofibroblastic phenotype in hepatic stellate cells by activating the hedgehog pathway. J Biol Chem 285: 36551-36560, 2010.
6. Chung AC, Dong Y, Yang W, Zhong X, Li R, Lan HY. Smad7 suppresses renal fibrosis via altering expression of TGF-beta/Smad3-regulated microRNAs. Mol Ther 21: 388-398, 2013.
7. Copaci I, Micu L, Voiculescu M. The role of cytokines in non-alcoholic steatohepatitis. A review. J Gastrointest Liver Dis 15: 363-373, 2006.
8. De Minicis S, Seki E, Oesterreicher C, Schnabl B, Schwabe RF, Brenner DA. Reduced nicotinamide adenine dinucleotide phosphate oxidase mediates fibrotic and inflammatory effects of leptin on hepatic stellate cells. Hepatology 48: 2016-2026, 2008.
9. De Minicis S, Svegliati-Baroni G. Fibrogenesis in nonalcoholic steatohepatitis. Exp Rev Gastroenterol Hepatol 5: 179-187, 2011.
10. Dooley S, ten Dijke P. TGF-beta in progression of liver disease. Cell Tissue Res 347: 245-256, 2012.
11. Honda H, Ikejima K, Hirose M, Yoshikawa M, Lang T, Enomoto N, Kitamura T, Takei Y, Sato N. Leptin is required for fibrogenic responses induced by thioacetamide in the murine liver. Hepatology 36: 12-21, 2002.
12. Ikejima K, Okumura K, Kon K, Takei Y, Sato N. Role of adipocyto-kines in hepatic fibrogenesis. J Gastroenterol Hepatol 22, Suppl 1: S87-S92, 2007.
13. Ikejima K, Okumura K, Lang T, Honda H, Abe W, Yamashina S, Enomoto N, Takei Y, Sato N. The role of leptin in progression of non-alcoholic fatty liver disease. Hepatol Res 33: 151-154, 2005.
14. Kamada Y, Takehara T, Hayashi N. Adipocytokines and liver disease. J Gastroenterol 43: 811-822, 2008.
15. Kohan M, Muro AF, White ES, Berkman N. EDA-containing cellular fibronectin induces fibroblast differentiation through binding to a4|37 integrin receptor and MAPK/Erk 1/2-dependent signaling. FASEB J 24: 4503-4512, 2010.
16. Lin Y, Liu X, Cheng Y, Yang J, Huo Y, Zhang C. Involvement of microRNAs in hydrogen peroxide-mediated gene regulation and cellular injury response in vascular smooth muscle cells. J Biol Chem 284: 7903-7913, 2009.
17. Liu G, Friggeri A, Yang Y, Milosevic J, Ding Q, Thannickal VJ, Kaminski N, Abraham E. miR-21 mediates fibrogenic activation of pulmonary fibroblasts and lung fibrosis. J Exp Med 207: 1589-1597, 2010.
18. Liu Y, Liu H, Meyer C, Li J, Nadalin S, Konigsrainer A, Weng H, Dooley S, ten Dijke P. Transforming growth factor-beta (TGF-beta)-mediated connective tissue growth factor (CTGF) expression in hepatic stellate cells requires Stat3 signaling activation. J Biol Chem 288: 30708-30719, 2013.
19. Marra F, Aleffi S, Bertolani C, Petrai I, Vizzutti F. Adipokines and liver fibrosis. Eur Rev Med Pharmacol Sci 9: 279-284, 2005.
20. Medici V, Ali MR, Seo S, Aoki CA, Rossaro L, Kim K, Fuller WD, Vidovszky TJ, Smith W, Jiang JX, Maganti K, Havel PJ, Kamboj A, Ramsamooj R, Torok NJ. Increased soluble leptin receptor levels in morbidly obese patients with insulin resistance and nonalcoholic fatty liver disease. Obesity (Silver Spring) 18: 2268-2273, 2010.
21. Michelotti GA, Machado MV, Diehl AM. NAFLD, NASH and liver cancer. Nat Rev Gastroenterol Hepatol 10: 656-665, 2013.
22. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin NE, Heldin CH, ten Dijke P. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 389: 631-635, 1997.
23. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, ten Dijke P. TGF-beta receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16: 5353-5362, 1997.
24. Nakao A, Roijer E, Imamura T, Souchelnytskyi S, Stenman G, Heldin CH, ten Dijke P. Identification of Smad2, a human Mad-related protein in the transforming growth factor beta signaling pathway. J Biol Chem 272: 2896-2900, 1997.
25. Noetel A, Kwiecinski M, Elfimova N, Huang J, Odenthal M. mi-croRNA are Central Players in Anti- and Profibrotic Gene Regulation during Liver Fibrosis. Front Physiol 3: 49, 2012.
26. Paik YH, Brenner DA. NADPH oxidase mediated oxidative stress in hepatic fibrogenesis. Kor J Hepatol 17: 251-257, 2011.
27. Paik YH, Kim J, Aoyama T, De Minicis S, Bataller R, Brenner DA. Role of NADPH oxidases in liver fibrosis. Antioxid Redox Signal 20: 2854-2872, 2014.
28. Patel V, Noureddine L. MicroRNAs and fibrosis. Curr Opin Nephrol Hypertens 21: 410-416, 2012.
29. Pirola CJ, Fernandez Gianotti T, Castano GO, Mallardi P, San Martino J, Mora Gonzalez Lopez Ledesma M, Flichman D, Mirshahi F, Sanyal AJ, Sookoian S. Circulating microRNA signature in nonalcoholic fatty liver disease: from serum non-coding RNAs to liver histology and disease pathogenesis. Gut. In press.
30. Procaccini C, Galgani M, De Rosa V, Carbone F, La Rocca C, Ranucci G, Iorio R, Matarese G. Leptin: the prototypic adipocytokine and its role in NAFLD. Curr Pharm Des 16: 1902-1912, 2010.
31. Quinn SR, O’Neill LA. A trio of microRNAs that control Toll-like receptor signalling. Int Immunol 23: 421-425, 2011.
32. Ruan Q, Wang T, Kameswaran V, Wei Q, Johnson DS, Matschinsky F, Shi W, Chen YH. The microRNA-21-PDCD4 axis prevents type 1 diabetes by blocking pancreatic beta cell death. Proc Natl Acad Sci USA 108: 12030-12035, 2011.
33. Saxena NK, Saliba G, Floyd JJ, Anania FA. Leptin induces increased alpha2(I) collagen gene expression in cultured rat hepatic stellate cells. J Cell Biochem 89: 311-320, 2003.
34. Schuppan D, Schattenberg JM. Non-alcoholic steatohepatitis: pathogenesis and novel therapeutic approaches. J Gastroenterol Hepatol 28, Suppl 1: 68-76, 2013.
35. Seth RK, Das S, Kumar A, Chanda A, Kadiiska MB, Michelotti G, Manautou J, Diehl AM, Chatterjee S. CYP2E1-dependent and leptin-mediated hepatic CD57 expression on CD8+ T cells aid progression of environment-linked nonalcoholic steatohepatitis. Toxicol Appl Pharmacol 274: 42-54, 2014.
36. Seth RK, Kumar A, Das S, Kadiiska MB, Michelotti G, Diehl AM, Chatterjee S. Environmental toxin-linked nonalcoholic steatohepatitis and hepatic metabolic reprogramming in obese mice. Toxicol Sci 134: 291-303, 2013.
37. Sheedy FJ, Palsson-McDermott E, Hennessy EJ, Martin C, O’Leary JJ, Ruan Q, Johnson DS, Chen Y, ÓNeill LA. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol 11: 141-147, 2010.
38. Singh S, Allen AM, Wang Z, Prokop LJ, Murad MH, Loomba R. Fibrosis progression in nonalcoholic fatty liver vs nonalcoholic steatohepatitis: a systematic review and meta-analysis of paired-biopsy studies. Clin Gastroenterol Hepatol. In press.
39. Tang M, Potter JJ, Mezey E. Leptin enhances the effect of transforming growth factor beta in increasing type I collagen formation. Biochem Biophys Res Commun 297: 906-911, 2002.
40. Wang J, Leclercq I, Brymora JM, Xu N, Ramezani-Moghadam M, London RM, Brigstock D, George J. Kupffer cells mediate leptin-induced liver fibrosis. Gastroenterology 137: 713-723, 2009.
41. Yang L, Roh YS, Song J, Zhang B, Liu C, Loomba R, Seki E. Transforming growth factor beta signaling in hepatocytes participates in steatohepatitis through regulation of cell death and lipid metabolism in mice. Hepatology 59: 483–495, 2014.
42. Yao H, Yang SR, Kode A, Rajendrasozhan S, Caito S, Adenuga D, Henry R, Edirisinghe I, Rahman I. Redox regulation of lung inflammation: role of NADPH oxidase and NF-kappaB signalling. Biochem Soc Trans 35: 1151–1155, 2007.
43. Yilmaz Y, Younossi ZM. Obesity-associated nonalcoholic fatty liver disease. Clin Liver Dis 18: 19–31, 2014.
44. Zhang Z, Gao Z, Hu W, Yin S, Wang C, Zang Y, Chen J, Zhang J, Dong L. 3,3=-Diindolylmethane ameliorates experimental hepatic fi-brosis via inhibiting miR-21 expression. Br J Pharmacol 170: 649–660, 2013.