Stem cell factor and c-kit are involved in hepatic recovery after acetaminophen-induced liver injury in mice

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 295, Issue 1, 2008, Pages

  Hu, Bin ^a   Colletti, Lisa M ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b 2210A Taubmen Center ^*  (United States)

Author keywords

Apoptosis; Cytokines; Hepatocyte proliferation; Liver regeneration

Indexed keywords

BROXURIDINE; MESSENGER RNA; PARACETAMOL; PROTEIN BCL 2; PROTEIN BCL XL; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; HYDROGEN PEROXIDE; NONSTEROID ANTIINFLAMMATORY AGENT;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; LIVER CELL; LIVER FUNCTION; LIVER INJURY; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BLOOD; C57BL MOUSE; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; LIVER; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; TIME; TOXIC HEPATITIS;

ACETAMINOPHEN; ALANINE TRANSAMINASE; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASPARTATE AMINOTRANSFERASES; CELL PROLIFERATION; GENE DELETION; GENE EXPRESSION REGULATION; HEPATITIS, TOXIC; HEPATOCYTES; HYDROGEN PEROXIDE; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-KIT; STEM CELL FACTOR; TIME FACTORS;

EID: 51149120023     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00024.2008     Document Type: Article

References (44)

1. Bauman U, Crosby HA, Ramani P, Kelly DA, Strain AJ. Expression of the stem cell factor receptor c-kit in normal and diseased pediatric liver: identification of a human hepatic progenitor cell? Hepatology 30: 112-117, 1999.
2. Boulares AH, Zoltoski AJ, Stoica BA, Cuvillier O, Smulson ME. Acetaminopeh induces a caspase-dependent and Bcl-XL sensitive apoptosis in human hepatoma cells and lymphocytes. Pharmacol Toxicol 90: 38-50, 2000.
3. Christensen JG, Romach EH, Healy LN, Gonzales AJ, Anderson SP, Malarkey DE, Corton JC, Fox TR, Cattley RC, Coldsworthy TL. Altered bcl-2 family expression during non-genotoxic carcinogenesis in mice. Carcinogenesis 20: 1583-1590.
4. Dahlin DC, Miwa GT, Lu AY, Nelson SD. N-acetyl-p-benzoquinone imine: a cytochrome P-450-mediated oxidation product of acetaminophen. Proc Natl Acad Sci USA 81: 1327-1331, 1984.
5. deCastro CM, Denning SM, Langdon S, Vandenbark GR, Kurtzber J, Scearce R, Haynes BF, Kaufman RE. The c-kit proto-oncogene receptor is expressed on a subset of human CD3-CD4-CD8- (triple-negative) thymocytes. Exp Hematol 22: 1025-1033, 1994.
6. Dhandapani KM, Wade FM, Wakade C, Mahesh VB, Brann DW. Neuroprotection by stem cell factor in rat cortical neurons involves AKT and NFkappa B. J Neurochem 95: 9-19, 2005.
7. Domen J, Weissman IL. Hematopoietic stem cells need two signals to prevent apoptosis; BCL-2 can provide one of these, Kitl/c-Kit signaling the other. J Exp Med 192: 1707-1718, 2000.
8. El-Hassan H, Anwar K, Macanas-Pirard P, Crabtree M, Chow SC, Johnson VL, Lee PD, Hinton RH, Price SC, Kass GE. Involvement of mitochondria in acetaminophen-induced apoptosis and hepatic injury: role of cytochrome c, Bax, Bid, and caspases. Toxicol Appl Pharmacol 191: 118-129, 2003.
9. Escribano L, Ocqueteau M, Almeida J, Orfao A, San Miguel JF. Expression of the c-kit (CD117) molecule in normal and malignant hematopoiesis. Leuk Lymphoma 30: 459-466, 1998.
10. Fleming WH, Alpern EJ, Uchida N, Ikuta K, Weissman IL. Steel factor influences the distribution and activity of murine hematopoietic stem cells in vivo. Proc Natl Acad Sci USA 90: 3760-3764, 1993.
11. Fujio K, Evarts RP, Hu Z, Marsden ER, Thorgeirsson SS. Expression of stem cell factor and its receptor, c-kit, during liver regeneration from putative stem cells in adult rat. Lab Invest 70: 511-516, 1994.
12. Fujio K, Hu Z, Evarts RP, Marsden ER, Niu CH, Thorgeirsson SS. Coexpression of stem cell factor and c-kit in embryonic and adult liver. Exp Cell Res 224: 243-250, 1996.
13. Gujral JS, Knight TR, Farhood A, Bajt ML, Jaeschke H. Mode of cell death after acetaminophen overdose in mice: apoptosis or oncotic necrosis? Toxicol Sci 67: 322-328, 2002.
14. Haldar S, Jena N, Croce CM. Inactivation of Bcl-2 by phosphorylation. Proc Natl Acad Sci USA 92: 4507-4511, 1995.
15. Hart SG, Cartun RW, Wyand DS, Khairallah EA, Cohen SD. Immunohistochemical localization of acetaminophen in target tissues of the CD-1 mouse: correspondence of covalent binding with toxicity. Fundam Appl Toxicol 24: 260-274, 1995.
16. Heinemann A, Sturm GJ, Ofner M, Sturm EM, Weller C, Peskar BA, Hartnell A. Stem cell factor stimulates the chemotaxis, integrin upregulation, and survival of human basophils. J Allergy Clin Immunol 116: 820-826, 2005.
17. Jin X, Han CS, Yu FQ, Wei P, Hu ZY, Liu YX. Anti-apoptotic action of stem cell factor on oocytes in primordial follicles and its signal transduction. Mol Reprod Dev 70: 82-90, 2005.
18. Johnson BW, Cepero E, Boise LH. Bcl-Xl inhibits cytochrome c release but not mitochondrial depolarization during the activation of multiple death pathways by tumor necrosis factor-alpha. J Biol Chem 275: 31546-31553, 2000.
19. Kim R, Emi M, Tanabe K. Caspase-dependent and -independent cell death pathways after DNA damage. Oncol Rep 14: 595-599, 2005.
20. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136, 1997.
21. Kofman Morgan G Kirschenbaum A Osbeck J Hussain M Swenson S Theise ND AV. Dose- and time-dependent oval cell reaction in acetaminophen-induced murine liver injury. Hepatology 41: 1252-1261, 2005.
22. Kon K, Kim JS, Jaeschke H, Lemasters JJ. Mitochondrial permeability transition in acetaminophen-induced necrosis and apoptosis of cultured mouse hepatocytes. Hepatology 40: 1170-1179, 2004.
23. Kovalovich K, Li W, DeAngelis R, Greenbaum LE, Ciliberto G, Taub R. Interleukin-6 protects again fas-mediated death by establishing a critical level of anti-apoptotic hepatic proteins FLIP, Bcl-2, and Bcl-xL. J Biol Chem 276: 26605-26613, 2001.
24. Larson AM, Polson J, Fontana RJ, Davern TJ, Lalani E, Hynan LS, Reisch JS, Schiodt FV, Ostapowicz G, Shakil AO, Lee WM. Acute Liver Failure Study Group. Acetaminophen-induced acute liver failure: results of a United States multicenter, prospective study. Hepatology 42: 1364-1372, 2005.
25. Leary AG, Zeng HQ, Clark SC, Ogawa M. Growth factor requirements for survival in G0 and entry into the cell cycle of primitive human hemopoietic progenitors. Proc Natl Acad Sci USA 89: 4013-4017, 1992.
26. Levesque JP, Leavesley DI, Nuitta S, Vadas M, Simmons PJ. Cytokines increase human hemopoietic cell adhesiveness by activation of very late antigen (VLA)-4 and VLA-5 integrins. J Exp Med 181: 1805-1815, 1995.
27. Lorz C, Justo P, Sanz AB, Egido J, Ortiz A. Role of Bcl-xL in paracetamol-induced tubular epithelial cell death. Kidney Int 67: 595-601, 2005.
28. Nicotera P, Leist M, Ferrando-May E. Apoptosis and necrosis: different execution of the same death. Biochem Soc Symp 66: 69-73, 1999.
29. Nicotera P, Melino G. Regulation of the apoptosis-necrosis switch. Oncogene 23: 2757-2765, 2004.
30. Nishio M, Oda A, Koizumi K, Satoh I, Sato Y, Endoh T, Tsutsumi A, Fujihara M, Ikebuchi K, Ikeda H, Koike T, Sawada KI. Stem cell factor prevents Fas-mediated apoptosis of human erythoid precursor cells with Src-family kinase dependency. Exp Hematol 29: 19-29, 2001.
31. Okumoto K, Saito T, Onodera M, Sakamoto A, Tanaka M, Hattori E, Haga H, Ito JO, Sugahara K, Saito K, Togashi H, Kawata S. Serum levels of stem cell factor and thrombopoietin are markedly decreased in fulminant hepatic failure patients with a poor prognosis. J Gastroenterol Hepatol 22: 1265-1270, 2007.
32. Omori M, Omori N, Evarts RP, Teramoto T, Thorgeirsson SS. Coexpression of flt-3 ligand/flt and SCF/c-kit signal transduction system in bile duct-ligated Sl and W mice. Am J Pathol 150: 1179-1187, 1997.
33. Pierce RH, Franklin CC, Campbell JS, Tonge RP, Chen W, Fausto N, Nelson SD, Bruschi SA. Cell culture model for acetaminophen-induced hepatocyte death in vivo. Biochem Pharmacol 64: 413-424, 2002.
34. Ray SD, Jena N. A hepatotoxic dose of acetaminophen modulates expression of BCL-2, BCL-X(L), and BCL-X(S) during apoptotic and necrotic death of mouse liver cells in vivo. Arch Toxicol 73: 594-606, 2000.
35. Ray SD, Mumaw VR, Raje RR, Fariss MW. Protection of acetaminophen-induced hepatocellular apoptosis and necrosis by cholesteryl hemisuccinate pretreatment. J Pharmacol Exp Ther 279: 1470-1483, 1996.
36. Ray SD, Parikh H, Hickey E, Bagchi M, Bagchi D. Differential effects of IH636 grape seed proanthocyanidin extract and a DNA repair modulator 4-aminobenzamide on liver microsomal cytochrome 4502E1-dependent aniline hydroxylation. Mol Cell Biochem 218: 27-33, 2001.
37. Ren X, Hogaboam C, Carpenter A, Colletti L. Stem cell factor restores hepatocyte proliferation in IL-6 knockout mice following 70% hepatectomy. J Clin Invest 112: 1407-1418, 2003.
38. Roskoski R Jr. Structure and regulation of Kit protein-tyrosine kinase. The stem cell receptor. Biochem Biophys Res Commun 338: 1307-1315, 2005.
39. Simpson K, Hogaboam CH, Kunkel SL, Harrison DJ, Bone-Larson C, Lukacs NW. Stem cell factor attenuates liver damage in a murine model of acetaminophen-induced hepatic injury. Lab Invest 83: 199-206, 2003.
40. Tzung SP, Fausto N, Hockenbery DM. Expression of Bcl-2 family during lier regeneration and identification of Bcl-x as a delayed early response gene. Am J Pathol 150: 1985-1995, 1997.
41. Wang CH, Verma S, Hsieh IC, Hung A, Cheng TT, Wang Sy Liu YC, Stanford WL, Weisel RD, Li RK, Cherng WJ. Stem cell factor attenuates vascular smooth muscle apoptosis and increases intimal hyperplasia after vascular injury. Arterioscler Thromb Vasc Biol 27: 540-547, 2007.
42. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng Ti Jones DP, Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondrial blocked. Science 275: 1129-1132, 1997.
43. Yang Y, Zhang GM, Feigenbaum L, Zhang YE. Smad3 reduces susceptibility to hepatocarcinoma by sensitizing hepatocytes to apoptosis through downregulation of Bcl-2. Cancer Cell 9: 445-457, 2006.
44. Zeuner A, Pedini F, Signore M, Testa U, Pelosi E, Peschle C, De Maria R. Stem cell factor protects erythroid precursor cells from chemotherapeutic agents via upregulation of BCL-2 family proteins. Blood 102: 87-93, 2003.