CD133+ liver cancer stem cells from methionine adenosyl transferase 1A-deficient mice demonstrate resistance to transforming growth factor (TGF)-β-induced apoptosis

Hepatology

Volumn 49, Issue 4, 2009, Pages 1277-1286

  Ding, Wei ^a   Mouzaki, Marialena ^a   You, Hanning ^a   Laird, Joshua C ^a   Mato, Jose ^b   Lu, Shelly C ^c   Rountree, C Bart ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CD33 ANTIGEN; METHIONINE ADENOSYLTRANSFERASE; METHIONINE ADENOSYLTRANSFERASE 1A; MITOGEN ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CD133 ANTIGEN; CELL CYCLE PROTEIN; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; MAT1A PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CANCER STEM CELL; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL GROWTH; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EXPERIMENTAL NEOPLASM; GROWTH INHIBITION; LIVER CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; CELL LINE; DRUG ANTAGONISM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; LIVER; LIVER TUMOR; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; XENOGRAFT;

ANIMALS; ANTIGENS, CD; APOPTOSIS; CELL CYCLE PROTEINS; CELL LINE; CELL PROLIFERATION; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; LIVER; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; MAP KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; METHIONINE ADENOSYLTRANSFERASE; MICE; MICE, KNOCKOUT; NEOPLASTIC STEM CELLS; PEPTIDES; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION, HETEROLOGOUS;

EID: 65449138684     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.22743     Document Type: Article

References (41)

1. El-Serag HB. Hepatocellular carcinoma: An epidemiologic view. J Clin Gastroenterol 2002;35:S72-S78.
2. Llovet JM, Fuster J, Bruix J. Prognosis of hepatocellular carcinoma. Hepatogastroenterology 2002;49:7-11.
3. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007;445:111-115.
4. Gou S, Liu T, Wang C, Yin T, Li K, Yang M, et al. Establishment of clonal colony-forming assay for propagation of pancreatic cancer cells with stem cell properties. Pancreas 2007;34:429-435.
5. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63:5821-5828.
6. Miki J, Furusato B, Li H, Gu Y, Takahashi H, Egawa S, et al. Identification of putative stem cell markers, CD133 and CXCR4, in hTERT-immortalized primary nonmalignant and malignant tumor-derived human prostate epithelial cell lines and in prostate cancer specimens. Cancer Res 2007;67: 3153-3161.
7. Ma S, Lee TK, Zheng BJ, Chan KW, Guan XY. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008;27:1749-1758.
8. Sell S, Dunsford HA. Evidence for the stem cell origin of hepatocellular carcinoma and cholangiocarcinoma. Am J Pathol 1989;134:1347-1363.
9. Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, Iwama A, et al. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. HEPATOLOGY2006;44:240-251.
10. Lee JS, Heo J, Libbrecht L, Chu IS, Kaposi-Novak P, Calvisi DF, et al. A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 2006;12:410-416.
11. Rountree CB, Senadheera S, Mato JM, Crooks GM, Lu SC. Expansion of liver cancer stem cells during aging in methionine adenosyltransferase 1Adeficient mice. HEPATOLOGY2008;47:1288-1297.
12. Mato JM, Lu SC. Role of S-adenosyl-L-methionine in liver health and injury. HEPATOLOGY2007;45:1306-1312.
13. Avila MA, Berasain C, Torres L, Martin-Duce A, Corrales FJ, Yang H, et al. Reduced mRNA abundance of the main enzymes involved in methionine metabolism in human liver cirrhosis and hepatocellular carcinoma. J Hepatol 2000;33:907-914.
14. Lu SC, Alvarez L, Huang ZZ, Chen L, An W, Corrales FJ, et al. Methionine adenosyltransferase 1A knockout mice are predisposed to liver injury and exhibit increased expression of genes involved in proliferation. Proc Natl Acad Sci U S A 2001;98:5560-5565.
15. Coulouarn C, Factor VM, Thorgeirsson SS. Transforming growth factorbeta gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer. HEPATOLOGY2008;47:2059-2067.
16. Kitisin K, Ganesan N, Tang Y, Jogunoori W, Volpe EA, Kim SS, et al. Disruption of transforming growth factor-beta signaling through betaspectrin ELF leads to hepatocellular cancer through cyclin D1 activation. Oncogene 2007;26:7103-7110.
17. Massague J, Andres J, Attisano L, Cheifetz S, Lopez-Casillas F, Ohtsuki M, et al. TGF-beta receptors. Mol Reprod Dev 1992;32:99-104.
18. Massague J, Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 2000;19:1745-1754.
19. Nguyen LN, Furuya MH, Wolfraim LA, Nguyen AP, Holdren MS, Campbell JS, et al. Transforming growth factor-beta differentially regulates oval cell and hepatocyte proliferation. HEPATOLOGY2007;45:31-41.
20. Siegel PM, Massague J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 2003;3:807-821.
21. Gressner AM, Lahme B, Mannherz HG, Polzar B. TGF-beta-mediated hepatocellular apoptosis by rat and human hepatoma cells and primary rat hepatocytes. J Hepatol 1997;26:1079-1092.
22. Rountree CB, Barsky L, Ge S, Zhu J, Senadheera S, Crooks GM. A CD133-expressing murine liver oval cell population with bilineage potential. Stem Cells 2007;25:2419-2429.
23. Ilangovan U, Ding W, Zhong Y, Wilson CL, Groppe JC, Trbovich JT, et al. Structure and dynamics of the homodimeric dynein light chain km23. J Mol Biol 2005;352:338-354.
24. Rountree CB, Senadheera S, Mato JM, Crooks GM, Lu SC. Expansion of liver cancer stem cells during aging in methionine adenosyltransferase 1Adeficient mice. HEPATOLOGY2008;47:1288-1297.
25. Nelson-Degrave VL, Wickenheisser JK, Hendricks KL, Asano T, Fujishiro M, Legro RS, et al. Alterations in mitogen-activated protein kinase kinase and extracellular regulated kinase signaling in theca cells contribute to excessive androgen production in polycystic ovary syndrome. Mol Endocrinol 2005;19:379-390.
26. Nagy P, Bisgaard HC, Thorgeirsson SS. Expression of hepatic transcription factors during liver development and oval cell differentiation. J Cell Biol 1994;126:223-233.
27. Inagaki M, Moustakas A, Lin HY, Lodish HF, Carr BI. Growth inhibition by transforming growth factor beta (TGF-beta) type I is restored in TGFbeta-resistant hepatoma cells after expression of TGF-beta receptor type II cDNA. Proc Natl Acad Sci U S A 1993;90:5359-5363.
28. Zhang H, Ozaki I, Mizuta T, Yoshimura T, Matsuhashi S, Eguchi Y, et al. Transforming growth factor-beta 1-induced apoptosis is blocked by beta 1-integrin-mediated mitogen-activated protein kinase activation in human hepatoma cells. Cancer Sci 2004;95:878-886.
29. Mansour SJ, Matten WT, Hermann AS, Candia JM, Rong S, Fukasawa K, et al. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 1994;265:966-970.
30. Chan HL, Sung JJ. Hepatocellular carcinoma and hepatitis B virus. Semin Liver Dis 2006;26:153-161.
31. Grasl-Kraupp B, Rossmanith W, Ruttkay-Nedecky B, Mullauer L, Kammerer B, Bursch W, et al. Levels of transforming growth factor beta and transforming growth factor beta receptors in rat liver during growth, regression by apoptosis and neoplasia. HEPATOLOGY1998;28:717-726.
32. Clark JB, Rice L, Sadiq T, Brittain E, Song L, Wang J, et al. Hepatic progenitor cell resistance to TGF-beta1's proliferative and apoptotic effects. Biochem Biophys Res Commun 2005;329:337-344.
33. Sanchez A, Alvarez AM, Lopez Pedrosa JM, Roncero C, Benito M, Fabregat I. Apoptotic response to TGF-beta in fetal hepatocytes depends upon their state of differentiation. Exp Cell Res 1999;252:281-291.
34. Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng IO, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007;132:2542-2556.
35. McGinnis KM, Gnegy ME, Park YH, Mukerjee N, Wang KK. Procaspase-3 and poly(ADP)ribose polymerase (PARP) are calpain substrates. Biochem Biophys Res Commun 1999;263:94-99.
36. Huynh H, Nguyen TT, Chow KH, Tan PH, Soo KC, Tran E. Overexpression of the mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK in hepatocellular carcinoma: Its role in tumor progression and apoptosis. BMC Gastroenterol 2003;3:19.
37. Hayashi J, Aoki H, Kajino K, Moriyama M, Arakawa Y, Hino O. Hepatitis C virus core protein activates the MAPK/ERK cascade synergistically with tumor promoter TPA, but not with epidermal growth factor or transforming growth factor alpha. HEPATOLOGY2000;32:958-961.
38. Ding Q, Xia W, Liu JC, Yang JY, Lee DF, Xia J, et al. Erk associates with and primes GSK-3beta for its inactivation resulting in upregulation of beta-catenin. Mol Cell 2005;19:159-170.
39. Martinez-Chantar ML, Corrales FJ, Martinez-Cruz LA, Garcia-Trevijano ER, Huang ZZ, Chen L, et al. Spontaneous oxidative stress and liver tumors in mice lacking methionine adenosyltransferase 1A. FASEB J 2002; 16:1292-1294.
40. Wiesenauer CA, Yip-Schneider MT, Wang Y, Schmidt CM. Multiple anticancer effects of blocking MEK-ERK signaling in hepatocellular carcinoma. J Am Coll Surg 2004;198:410-421.
41. Shepherd CJ, Rizzo S, Ledaki I, Davies M, Brewer D, Attard G, et al. Expression profiling of CD133+ and CD133- epithelial cells from human prostate. Prostate 2008;68:1007-1024.