Targeting androgen receptor in bone marrow mesenchymal stem cells leads to better transplantation therapy efficacy in liver cirrhosis

Hepatology

Volumn 57, Issue 4, 2013, Pages 1550-1563

  Huang, Chiung Kuei ^a   Lee, Soo Ok ^a   Lai, Kuo Pao ^a   Ma, Wen Lung ^a,b   Lin, Tzu Hua ^a   Tsai, Meng Yin ^c   Luo, Jie ^a   Chang, Chawnshang ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; ASC J 9; CARBON TETRACHLORIDE; EPIDERMAL GROWTH FACTOR RECEPTOR; GELATINASE B; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MISCELLANEOUS DRUGS AND AGENTS; SMALL INTERFERING RNA; THIOACETAMIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL MIGRATION; CELL RENEWAL; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; GENE SILENCING; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOMODULATION; INTRACELLULAR SIGNALING; LIVER CIRRHOSIS; LIVER REGENERATION; MACROPHAGE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION; STELLATE CELL; THERAPY EFFECT; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; CARBON TETRACHLORIDE; DISEASE MODELS, ANIMAL; FEMALE; LIVER CIRRHOSIS; MALE; MATRIX METALLOPROTEINASE 9; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MICE, KNOCKOUT; PHENOTYPE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, ANDROGEN; RECEPTORS, INTERLEUKIN-1; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THIOACETAMIDE; TREATMENT OUTCOME;

EID: 84876148888     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26135     Document Type: Article

References (40)

1. Heron M, Hoyert DL, Murphy SL, Xu J, Kochanek KD, Tejada-Vera B. Deaths: final data for 2006. Natl Vital Stat Rep 2009; 57: 1-134.
2. Sorensen HT, Thulstrup AM, Mellemkjar L, Jepsen P, Christensen E, Olsen JH, Vilstrup H. Long-term survival and cause-specific mortality in patients with cirrhosis of the liver: a nationwide cohort study in Denmark. J Clin Epidemiol 2003; 56: 88-93.
3. Yu MW, Hsu FC, Sheen IS, Chu CM, Lin DY, Chen CJ, Liaw YF. Prospective study of hepatocellular carcinoma and liver cirrhosis in asymptomatic chronic hepatitis B virus carriers. Am J Epidemiol 1997; 145: 1039-1047.
4. Seton M, Pless M, Fishman JA, Caruso PA, Hedley-Whyte ET. Case records of the Massachusetts General Hospital. Case 18-2008. A 68-year-old man with headache and visual changes after liver transplantation. N Engl J Med 2008; 358: 2619-2628.
5. Shimizu T, Kasahara M, Tanaka K. Living-donor liver transplantation for chronic hepatic graft-versus-host disease. N Engl J Med 2006; 354: 1536-1537.
6. Kobayashi N, Ito M, Nakamura J, Cai J, Hammel JM, Fox IJ. Hepatocyte transplantation improves liver function and prolongs survival in rats with decompensated liver cirrhosis. Transplant Proc 1999; 31: 428-429.
7. Liu F, Liu ZD, Wu N, Cong X, Fei R, Chen HS, Wei L. Transplanted endothelial progenitor cells ameliorate carbon tetrachloride-induced liver cirrhosis in rats. Liver Transpl 2009; 15: 1092-1100.
8. Nakamura T, Torimura T, Sakamoto M, Hashimoto O, Taniguchi E, Inoue K, et al. Significance and therapeutic potential of endothelial progenitor cell transplantation in a cirrhotic liver rat model. Gastroenterology 2007; 133: 91-107.e101.
9. Chang YJ, Liu JW, Lin PC, Sun LY, Peng CW, Luo GH, et al. Mesenchymal stem cells facilitate recovery from chemically induced liver damage and decrease liver fibrosis. Life Sci 2009; 85: 517-525.
10. Mohamadnejad M, Namiri M, Bagheri M, Hashemi SM, Ghanaati H, Zare Mehrjardi N, et al. Phase 1 human trial of autologous bone marrow-hematopoietic stem cell transplantation in patients with decompensated cirrhosis. World J Gastroenterol 2007; 13: 3359-3363.
11. Houlihan DD, Newsome PN. Critical review of clinical trials of bone marrow stem cells in liver disease. Gastroenterology 2008; 135: 438-450.
12. Toma C, Wagner WR, Bowry S, Schwartz A, Villanueva F. Fate of culture-expanded mesenchymal stem cells in the microvasculature: in vivo observations of cell kinetics. Circ Res 2009; 104: 398-402.
13. Crisostomo PR, Markel TA, Wang M, Lahm T, Lillemoe KD, Meldrum DR. In the adult mesenchymal stem cell population, source gender is a biologically relevant aspect of protective power. Surgery 2007; 142: 215-221.
14. Lee HJ, Teixeira J. Evidence of a role for androgens in embryonic stem cell function and differentiation. Endocrinology 2008; 149: 3-4.
15. Miyahara Y, Nagaya N, Kataoka M, Yanagawa B, Tanaka K, Hao H, et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 2006; 12: 459-465.
16. Seki E, De Minicis S, Osterreicher CH, Kluwe J, Osawa Y, Brenner DA, Schwabe RF. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 2007; 13: 1324-1332.
17. Hardjo M, Miyazaki M, Sakaguchi M, Masaka T, Ibrahim S, Kataoka K, Huh NH. Suppression of carbon tetrachloride-induced liver fibrosis by transplantation of a clonal mesenchymal stem cell line derived from rat bone marrow. Cell Transplant 2009; 18: 89-99.
18. Friedman SL. Mechanisms of hepatic fibrogenesis. Gastroenterology 2008; 134: 1655-1669.
19. Tilg H, Wilmer A, Vogel W, Herold M, Nolchen B, Judmaier G, Huber C. Serum levels of cytokines in chronic liver diseases. Gastroenterology 1992; 103: 264-274.
20. Zimmermann HW, Seidler S, Nattermann J, Gassler N, Hellerbrand C, Zernecke A, et al. Functional contribution of elevated circulating and hepatic non-classical CD14CD16 monocytes to inflammation and human liver fibrosis. PLoS One 2010; 5: e11049.
21. Ortiz LA, Dutreil M, Fattman C, Pandey AC, Torres G, Go K, Phinney DG. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci U S A 2007; 104: 11002-11007.
22. Oyagi S, Hirose M, Kojima M, Okuyama M, Kawase M, Nakamura T, et al. Therapeutic effect of transplanting HGF-treated bone marrow mesenchymal cells into CCl4-injured rats. J Hepatol 2006; 44: 742-748.
23. Sakaida I, Terai S, Yamamoto N, Aoyama K, Ishikawa T, Nishina H, Okita K. Transplantation of bone marrow cells reduces CCl4-induced liver fibrosis in mice. HEPATOLOGY 2004; 40: 1304-1311.
24. Preaux AM, Mallat A, Nhieu JT, D'Ortho MP, Hembry RM, Mavier P. Matrix metalloproteinase-2 activation in human hepatic fibrosis regulation by cell-matrix interactions. HEPATOLOGY 1999; 30: 944-950.
25. Chung TW, Kim JR, Suh JI, Lee YC, Chang YC, Chung TH, Kim CH. Correlation between plasma levels of matrix metalloproteinase (MMP)-9/MMP-2 ratio and alpha-fetoproteins in chronic hepatitis carrying hepatitis B virus. J Gastroenterol Hepatol 2004; 19: 565-571.
26. Lin H, Xu R, Zhang Z, Chen L, Shi M, Wang FS. Implications of the immunoregulatory functions of mesenchymal stem cells in the treatment of human liver diseases. Cell Mol Immunol 2011; 8: 19-22.
27. Deuse T, Peter C, Fedak PW, Doyle T, Reichenspurner H, Zimmermann WH, et al. Hepatocyte growth factor or vascular endothelial growth factor gene transfer maximizes mesenchymal stem cell-based myocardial salvage after acute myocardial infarction. Circulation 2009; 120: S247-254.
28. Tang J, Wang J, Guo L, Kong X, Yang J, Zheng F, et al. Mesenchymal stem cells modified with stromal cell-derived factor 1 alpha improve cardiac remodeling via paracrine activation of hepatocyte growth factor in a rat model of myocardial infarction. Mol Cells 2010; 29: 9-19.
29. Bonyadi M, Waldman SD, Liu D, Aubin JE, Grynpas MD, Stanford WL. Mesenchymal progenitor self-renewal deficiency leads to age-dependent osteoporosis in Sca-1/Ly-6A null mice. Proc Natl Acad Sci U S A 2003; 100: 5840-5845.
30. Han YP, Zhou L, Wang J, Xiong S, Garner WL, French SW, Tsukamoto H. Essential role of matrix metalloproteinases in interleukin-1-induced myofibroblastic activation of hepatic stellate cell in collagen. J Biol Chem 2004; 279: 4820-4828.
31. Koda K, Niitsu Y, Bunya M, Ito N, Sasagawa Y, Owada M, et al. Increased production of interleukin-1 by macrophage from the patients with chronic liver disease and its implication for liver fibrosis. [Article in Japanese]. Nihon Shokakibyo Gakkai Zasshi 1985; 82: 1527-1532.
32. Stienstra R, Saudale F, Duval C, Keshtkar S, Groener JE, van Rooijen N, et al. Kupffer cells promote hepatic steatosis via interleukin-1beta-dependent suppression of peroxisome proliferator-activated receptor alpha activity. HEPATOLOGY 2010; 51: 511-522.
33. Friedman SL, Arthur MJ. Activation of cultured rat hepatic lipocytes by Kupffer cell conditioned medium. Direct enhancement of matrix synthesis and stimulation of cell proliferation via induction of platelet-derived growth factor receptors. J Clin Invest 1989; 84: 1780-1785.
34. Ma WL, Hsu CL, Wu MH, Wu CT, Wu CC, Lai JJ, et al. Androgen receptor is a new potential therapeutic target for the treatment of hepatocellular carcinoma. Gastroenterology 2008; 135: 947-955, 955.e941-945.
35. Singh R, Artaza JN, Taylor WE, Gonzalez-Cadavid NF, Bhasin S. Androgens stimulate myogenic differentiation and inhibit adipogenesis in C3H 10T1/2 pluripotent cells through an androgen receptor-mediated pathway. Endocrinology 2003; 144: 5081-5088.
36. Isaacs JT. Prostate stem cells and benign prostatic hyperplasia. Prostate 2008; 68: 1025-1034.
37. Kang HY, Shyr CR, Huang CK, Tsai MY, Orimo H, Lin PC, et al. Altered TNSALP expression and phosphate regulation contribute to reduced mineralization in mice lacking androgen receptor. Mol Cell Biol 2008; 28: 7354-7367.
38. Chang CY, Hsuuw YD, Huang FJ, Shyr CR, Chang SY, Huang CK, et al. Androgenic and antiandrogenic effects and expression of androgen receptor in mouse embryonic stem cells. Fertil Steril 2006; 85( Suppl 1): 1195-1203.
39. Goulmy E, Schipper R, Pool J, Blokland E, Falkenburg JH, Vossen J, et al. Mismatches of minor histocompatibility antigens between HLA-identical donors and recipients and the development of graft-versus-host disease after bone marrow transplantation. N Engl J Med 1996; 334: 281-285.
40. Burt RK, Loh Y, Pearce W, Beohar N, Barr WG, Craig R, et al. Clinical applications of blood-derived and marrow-derived stem cells for nonmalignant diseases. JAMA 2008; 299: 925-936.