Nitric oxide augments mesenchymal stem cell ability to repair liver fibrosis

Journal of Translational Medicine

Volumn 10, Issue 1, 2012, Pages

  Ali, Gibran ^a   Mohsin, Sadia ^a   Khan, Mohsin ^a   Nasir, Ghazanfar A ^a   Shams, Sulaiman ^a   Khan, Shaheen N ^a   Riazuddin, Sheikh ^a  

^a UNIVERSITY OF THE PUNJAB   (Pakistan)

Author keywords

Hepatic stellate cells (HSCs); Liver fibrosis; Mesenchymal stem cells (MSCS); Nitric oxide

Indexed keywords

ALBUMIN; ALKALINE PHOSPHATASE; ALPHA SMOOTH MUSCLE ACTIN; BILIRUBIN; COLLAGEN TYPE 1; CYTOKERATIN 18; ENDOTHELIAL NITRIC OXIDE SYNTHASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITROPRUSSIDE SODIUM; TISSUE INHIBITOR OF METALLOPROTEINASE; COLLAGEN; NITRIC OXIDE;

ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BILIRUBIN BLOOD LEVEL; CELL HOMING; CELL SURVIVAL; CELL TRANSPLANTATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIVER FIBROSIS; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL LINEAGE; CELL MOTION; CONVALESCENCE; CYTOLOGY; DRUG EFFECT; GENETICS; LIVER; LIVER CIRRHOSIS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; TUMOR MICROENVIRONMENT; WOUND HEALING;

ANIMALS; CELL LINEAGE; CELL MOVEMENT; CELLULAR MICROENVIRONMENT; COLLAGEN; FEMALE; GENE EXPRESSION PROFILING; LIVER; LIVER CIRRHOSIS; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; NITRIC OXIDE; NITROPRUSSIDE; RECOVERY OF FUNCTION; WOUND HEALING;

EID: 84862174243     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-10-75     Document Type: Article

References (50)

1. Elsharkawy AM, Oakley F, Mann DA. The role and regulation of hepatic stellate cell apoptosis in reversal of liver fibrosis. Apoptosis 2005, 10:927-939. 10.1007/s10495-005-1055-4, 16151628.
2. Moreira RK. Hepatic stellate cells and liver fibrosis. Arch Pathol Lab Med 2007, 131:1728-1734.
3. Wu J, Kuncio GS, Zern MA. Human liver growth in fibrosis and cirrhosis. Liver Growth and Repair 1998, 558-76. Chapman and Hall, London, Strain AJ, Diehl AM.
4. Carvalho AB, Quintanilha LF, Dias JV, Paredes BD, Mannheimer EG, Carvalho FG. Bone marrow multipotent mesenchymal stromal cells do not reduce fibrosis or improve function in a rat model of severe chronic liver injury. Stem Cells 2008, 26(5):1307-1314. 10.1634/stemcells.2007-0941, 18308943.
5. Zhao DC, Lei JX, Yu W, Zhang X, Li S, Xiang P. Bone marrow derived mesenchymal stem cells protect against experimental liver fibrosis in rats. World J Gastroenterol 2005, 11:3431-3440.
6. Yamamoto Y, Banas A, Murata S, Ishikawa M, Lim CR, Teratani T, Hatada I, Matsubara K, Kato T, Ochiya T. A comparative analysis of the transcriptome and signal pathways in hepatic differentiation of human adipose mesenchymal stem cells. FEBS J 2008, 275:1260-1273. 10.1111/j.1742-4658.2008.06287.x, 18318837.
7. Kuo TK, Hung SP, Chuang CH, Chen CT, Shih YR, Fang SC. Stem cell therapy for liver disease: parameters governing the success of using bone marrow mesenchymal stem cells. Gastroenterology 2008, 134:2111-2121. 10.1053/j.gastro.2008.03.015, 3086672, 18455168.
8. Liang L, Ma T, Chen W, Hu J, Bai X. Therapeutic potential and related signal pathway of adipose-derived stem cell transplantation for rat liver injury. Hepatol Res 2009, 39(8):822-32. 10.1111/j.1872-034X.2009.00506.x, 19473439.
9. Song H, Kwon K, Lim S, Kang SM, Ko YG, Xu Z, Chung JH, Kim BS, Lee H, Joung B, Park S, Choi D, Jang Y, Chung NS, Yoo KJ, Hwang KC. Transfection of mesenchymal stem cells with the FGF-2 gene improves their survival under hypoxic conditions. Mol Cells 2005, 19(3):402-407.
10. Friedman SL. Hepatic stellate cells. Prog Liver Dis 1996, 14:101-130.
11. Friedman SL. Hepatic fibrosis-Overview. Toxicology 2008, 254:120-129. 10.1016/j.tox.2008.06.013, 18662740.
12. Bataller R, Brenner D. Liver fibrosis. J Clin Invest 2005, 115:209-218. 546435, 15690074.
13. Jiang F, Parsons CJ, Stefanovic B. Gene expression profile of quiescent and activated rat hepatic stellate cells implicates Wnt signaling pathway in activation. J Hepatol 2006, 45:401-409. 10.1016/j.jhep.2006.03.016, 16780995.
14. Jiang F, Stefanovic B. Homeobox Gene Prx1 is expressed in activated hepatic stellate cells and transactivates Collagen α1 (I) promoter. Exp Biol Med 2008, 233:286-296.
15. Nishikawa Y, Ohi N, Yagisawa A, Doi Y, Yamamoto Y, Yoshida M, Tokairin T, Yoshioka T, Omori Y, Enomoto K. Suppressive effect of orthovanadate on hepatic stellate cell activation and liver fibrosis in rats. Am J Path 2009, 174:881-890. 10.2353/ajpath.2009.080261, 2665748, 19164509.
16. Hagens WI, Olinga P, Meijer DKF, Groothuis GMM, Beljaars L, Poelstra K. Gliotoxin non-selectively induces apoptosis in fibrotic and normal livers. Liver Int 2006, 26:232-239. 10.1111/j.1478-3231.2005.01212.x, 16448462.
17. Hayashi S, Itoh A, Isoda K, Kondoh M, Kawase M, Yagi K. Fucoidan partly prevents CCl4-induced liver fibrosis. Eur J Pharmacol 2008, 580(3):380-384. 10.1016/j.ejphar.2007.11.015, 2258315, 18068155.
18. Langer DA, Das A, Semela D, Kang-Decker N, Hendrickson H, Bronk SF, Katusic ZS, Gores GJ, Shah VH. Nitric oxide promotes caspase-independent hepatic stellate cell apoptosis through the generation of reactive oxygen species. Hepatology 2008, 47:1983-1993. 10.1002/hep.22285, 2562502, 18459124.
19. Dai L, Hui J, Xiang-wen K, Yi-hua Z. Antifibrotic effects of ZK14, a novel nitric oxidedonating biphenyldicarboxylate derivative, on rat HSC-T6 cells and CCl4-induced hepatic fibrosis. Acta Pharmacologica Sinica 2010, 31:27-34. 10.1038/aps.2009.170, 19966836.
20. Leung TM, Fung ML, Liong EC, Lau TYH, Nanji AA, Tipoe GL. Role of nitric oxide in the regulation of fibrogenic factors in experimental liver fibrosis in mice. Histol Histopathol 2011, 26:201-211.
21. Khan M, Mohsin S, Khan SN, Riazuddin S. Repair of the senescent myocardium by mesenchymal stem cells is dependent on the age of donor mice. J Cell Mol Med 2011, 15:1515-1527. 10.1111/j.1582-4934.2009.00998.x, 20041970.
22. Mohsin S, Shams S, Nasir GA, Khan M, Awan SJ, Khan SN, Riazuddin S. Enhanced hepatic differentiation of mesenchymal stem cells after pretreatment with injured liver tissue. Differentiation 2011, 81:42-48. 10.1016/j.diff.2010.08.005, 20943307.
23. Leung TM, Tipoe GL, Liong EC, Lau TYH, Fung ML, Nanji AA. Endothelial nitric oxide synthase is a critical factor in experimental liver fibrosis. Int J Exp Path 2008, 89:241-250.
24. Wu J, Zern MA. Hepatic stellate cells: a target for the treatment of liver fibrosis. J Gastroenterol 2000, 35:665-672. 10.1007/s005350070045, 11023037.
25. Guimaraes EL, Franceschi MF, Grivicich I. Relationship between oxidative stress levels and activation state on hepatic stellate cell line. Liver Int 2006, 26:477-485. 10.1111/j.1478-3231.2006.01245.x, 16629652.
26. Murphy FR, Issa R, Zhou X, Ratnarajah S, Nagase H, Arthur MJP, Benyon C, Iredale JP. Inhibition of apoptosis of activated hepatic stellate cells by tissue inhibitor of metalloproteinase-1 is mediated via effects on matrix metalloproteinase inhibition. J Biol Chem 2002, 277:11069-11076. 10.1074/jbc.M111490200, 11796725.
27. Kisseleva T, Brenner DA. Hepatic stellate cells and the reversal of fibrosis. J Gastroenterol Hepatol 2006, 21:84-87. 10.1111/j.1440-1746.2005.04155.x, 16706817.
28. Houlihan DD, Newsome PN. Critical review of clinical trials of bone marrow stem cells in liver disease. Gastroenterology 2008, 135:438-50. 10.1053/j.gastro.2008.05.040, 18585384.
29. Alison MR, Islam S, Lim S. Stem cells in liver regeneration, fibrosis and cancer: the good, the bad and the ugly. J Pathol 2009, 217:282-98. 10.1002/path.2453, 18991329.
30. Moreno M, Gonzalo T, Kok RJ, Sancho-Bru P, Beuge MV, Swart J, Prakash J, Temming K, Fondevila C, Beljaars L, Lacombe M, Hoeven PVD, Arroyo V, Poelstra K, Brenner DA, Gines P, Bataller R. Reduction of advanced liver fibrosis by short-term targeted delivery of an angiotensin receptor blocker to hepatic stellate cells in rats. Hepatology 2010, 51:1-11. 10.1002/hep.23235, 19827164.
31. Krizhanovsky V, Yon M, Dickins RA, Hearn S, Simon J, Miething C, Yee H, Zender L, Lowe SW. Senescence of activated stellate cells limits liver fibrosis. Cell 2008, 134:657-667. 10.1016/j.cell.2008.06.049, 3073300, 18724938.
32. Lysy PA, Smets F, Najimi M, Sokal EM. Leukemia inhibitory factor contributes to hepatocyte-like differentiation of human bone marrow mesenchymal stem cells. Differentiation 2008, 76:1057-1067. 10.1111/j.1432-0436.2008.00287.x, 18557762.
33. Cho KA, Lim GW, Joo SY, Woo SY, Seoh JY, Cho SJ, Han HS, Ryu KH. Transplantation of bone marrow cells reduces CCl4-induced liver fibrosis in mice. Liver Int 2010, 31:1478-3223.
34. Patella S, Phillips DJ, Tchongue J, Kretser DM, Sievert W. Follistatin attenuates early liver fibrosis: effects on hepatic stellate cell activation and hepatocyte apoptosis. Am J Physiol Gastrointest Liver Physiol 2006, 290:G137-G144.
35. Balakirev MY, Khramtsov VV, Zimmer G. Modulation of the mitochondrial permeability transition by nitric oxide. Eur J Biochem 1997, 246:710-718. 10.1111/j.1432-1033.1997.00710.x, 9219530.
36. Hortelano S, Dallaporta B, Zamzami N. Nitric oxide induces apoptosis via triggering mitochondrial permeability transition. FEBS Lett 1997, 410:373-377. 10.1016/S0014-5793(97)00623-6, 9237665.
37. Lee JS, Decker N, Chatterjee S, Yao J, Friedman S, Shah V. Mechanisms of nitric oxide interplay with Rho GTPase family members in modulation of actin membrane dynamics in pericytes and fibroblasts. Am J Pathol 2005, 166:1861-70. 10.1016/S0002-9440(10)62495-9, 1602419, 15920170.
38. Perri RE, Langer DA, Chatterjee S, Gibbons SJ, Gadgil J, Cao S. Defects in cGMP-PKG pathway contribute to impaired NO-dependent responses in hepatic stellate cells upon activation. Am J Physiol Gastrointest Liver Physiol 2006, 290:G535-G542. 10.1152/ajpgi.00297.2005, 16269521.
39. Sato Y, Araki H, Kato J. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 2005, 106:756-63. 10.1182/blood-2005-02-0572, 15817682.
40. Oyagi S, Hirose M, Kojima M, Okuyama M, Kawase M, Nakamura T, Ohgushi H, Yagi K. Therapeutic effect of transplanting HGF-treated bone marrow mesenchymal cells into CCl4-injured rats. J Hepatol 2006, 44:742-748. 10.1016/j.jhep.2005.10.026, 16469408.
41. Van Poll D, Parekkadan B, Cho CH, Berthiaume F, Nahmias Y, Tilles AW, Yarmush ML. Mesenchymal stem cell-derived molecules directly modulate hepatocellular death and regeneration in vitro and in vivo. Hepatology 2008, 47:1634-1643. 10.1002/hep.22236, 18395843.
42. Vig P, Russo FP, Edwards RJ, Tadrous PJ, Wright NA, Thomas HC, Alison MR, Forbes SJ. The sources of parenchymal regeneration after chronic hepatocellular liver injury in mice. Hepatology 2006, 43:316-324. 10.1002/hep.21018, 16440343.
43. Popp FC, Slowik P, Eggenhofer E, Renner P, Lang SA, Stoeltzing O, Geissler EK, Piso P, Schlitt HJ, Dahlke MH. No contribution of multipotent mesenchymal stromal cells to liver regeneration in a rat model of prolonged hepatic injury. Stem Cells 2007, 25:639-645.
44. Ishikawa T, Terai S, Urata Y, Marumoto Y, Aoyama K, Murata K, Mizunaga Y, Yamamoto N, Nishina H, Shinoda K, Sakaida K. Administration of fibroblast growth factor 2 in combination with bone marrow transplantation synergistically improves carbon-tetrachloride-induced liver fibrosis in mice. Cell Tissue Res 2007, 327:463-470. 10.1007/s00441-006-0334-x, 17093919.
45. Pinzani M, Rombouts K. Liver fibrosis: from the bench to clinical targets. Dig Liver Dis 2004, 36:231-242. 10.1016/j.dld.2004.01.003, 15115333.
46. Zhang J, You H, Wang T, Wang B, Jia J, Katayama H, Maeda S, Wang R, Asano G, Ishiwata T, Naito Z, Yokoyama M. Triple staining to identify apoptosis of hepatic cells in situ. J Nippon Med Sch 2000, 67(4):280-283.
47. Eng FJ, Friedman SL. Fibrogenesis I. New insights into hepatic stellate cell activation: the simple becomes complex. Am J Physiol Gastrointest Liver Physiol 2000, 279:G7-G11.
48. Maher JJ. Interactions between hepatic stellate cells and the immune system. Semin Liver Dis 2001, 21:417-426. 10.1055/s-2001-17555, 11586469.
49. Lee M, Song SU, Ryu JK, Suh JK. Sp1-dependent regulation of the tissue inhibitor of metalloproteinases-1 promoter. J Cell Biochem 2004, 91:1260-1268. 10.1002/jcb.20021, 15048879.
50. Hu AB, He XS, Zheng QC, Cai JY. Curative effects of transplantation of hepatocytes differentiated from embryonic stem cells on treatment of fulminant hepatic failure: experiment with mice. Zhonghua Yi Xue Za Zhi 2006, 86:3280-3284.