The DNA damage checkpoint protein ATM promotes hepatocellular apoptosis and fibrosis in a mouse model of non-alcoholic fatty liver disease

Cell Cycle

Volumn 11, Issue 10, 2012, Pages 1918-1928

  Daugherity, Erin K ^a   Balmus, Gabriel ^a   Al Saei, Ahmed ^a   Moore, Elizabeth S ^a   Abi Abdallah, Delbert ^a   Rogers, Arlin B ^b   Weiss, Robert S ^a   Maurer, Kirk J ^a  

^a Department of Obstetrics Gynecology   (United States)

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

Author keywords

ATM; Hepatic fibrosis; Nonalcoholic fatty liver disease; Oxidative stress; Steatoapoptosis

Indexed keywords

ATM PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DNA DAMAGE CHECKPOINT; FEEDING; FEMALE; LIPID DIET; LIPID STORAGE; LIVER CELL DAMAGE; LIVER FIBROSIS; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PREVALENCE; PROTEIN EXPRESSION; PUMA;

ATAXIA TELANGIECTASIA; MUS;

EID: 84861413262     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.20259     Document Type: Article

References (52)

1. Cohen JC, Horton JD, Hobbs HH. Human fatty liver disease: old questions and new insights. Science 2011; 332:1519-23; PMID:21700865; http://dx.doi.org/ 10.1126/science.1204265.
2. Starley BQ, Calcagno CJ, Harrison SA. Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology 2010; 51:1820-32; PMID:20432259; http://dx.doi.org/10.1002/hep.23594.
3. Williams CD, Stengel J, Asike MI, Torres DM, Shaw J, Contreras M, et al. Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology 2011; 140:124-31; PMID:20858492; http://dx.doi.org/10.1053/j.gastro.2010.09.038.
4. Hardwick RN, Fisher CD, Canet MJ, Lake AD, Cherrington NJ. Diversity in antioxidant response enzymes in progressive stages of human nonalcoholic fatty liver disease. Drug Metab Dispos 2010; 38:2293-301; PMID:20805291; http://dx.doi.org/10.1124/dmd.110.035006.
5. Caldwell S, Park SH. The epidemiology of hepatocellular cancer: from the perspectives of public health problem to tumor biology. J Gastroenterol 2009; 44:96-101; PMID:19148801; http://dx.doi.org/10.1007/s00535-008-2258-6.
6. Mehta K, Van Thiel DH, Shah N, Mobarhan S. Nonalcoholic fatty liver disease: pathogenesis and the role of antioxidants. Nutr Rev 2002; 60:289-93; PMID:12296456; http://dx.doi.org/10.1301/002966402320387224.
7. Ong J, Younossi ZM, Reddy V, Price LL, Gramlich T, Mayes J, et al. Cryptogenic cirrhosis and post-transplantation nonalcoholic fatty liver disease. Liver Transpl 2001; 7:797-801; PMID:11552214; http:// dx.doi.org/10.1053/jlts. 2001.24644.
8. Kusminski CM, Shetty S, Orci L, Unger RH, Scherer PE. Diabetes and apoptosis: lipotoxicity. Apoptosis 2009; 14:1484-95; PMID:19421860; http://dx.doi.org/10.1007/s10495-009-0352-8.
9. Cazanave SC, Elmi NA, Akazawa Y, Bronk SF, Mott JL, Gores GJ. CHOP and AP-1 cooperatively mediate PUMA expression during lipoapoptosis. Am J Physiol Gastrointest Liver Physiol 2010; 299:236-43; PMID:20430872; http://dx.doi.org/ 10.1152/ajpgi.00091.2010.
10. Feldstein A, Gores GJ. Steatohepatitis and apoptosis: therapeutic implications. Am J Gastroenterol 2004; 99:1718-9; PMID:15330908; http://dx.doi.org/10.1111/j.1572-0241.2004.40573.x.
11. Feldstein AE, Gores GJ. Apoptosis in alcoholic and non-alcoholic steatohepatitis. Front Biosci 2005; 10:3093-9; PMID:15970563; http://dx.doi.org/10.2741/1765.
12. Machado MV, Cortez-Pinto H. Cell death and non-alcoholic steatohepatitis: where is ballooning relevant? Expert Rev Gastroenterol Hepatol 2011; 5:213-22; PMID:21476916; http://dx.doi.org/10.1586/egh.11.16.
13. Noguchi Y, Young JD, Aleman JO, Hansen ME, Kelleher JK, Stephanopoulos G. Tracking cellular metabolomics in lipoapoptosis- and steatosis-developing liver cells. Mol Biosyst 2011; 7:1409-19; PMID:21327189; http://dx.doi.org/10.1039/ c0mb00309c.
14. Sunny NE, Parks EJ, Browning JD, Burgess SC. Excessive hepatic mitochondrial TCA cycle and gluconeogenesis in humans with nonalcoholic fatty liver disease. Cell Metab 2011; 14:804-10; PMID:22152305; http://dx.doi.org/10. 1016/j.cmet.2011.11.004.
15. McKinnon PJ. ATM and the molecular pathogenesis of ataxia telangiectasia. Annu Rev Pathol 2012; 7:303-21; PMID:22035194; http://dx.doi.org/10.1146/ annurev-pathol-011811-132509.
16. Armata HL, Golebiowski D, Jung DY, Ko HJ, Kim JK, Sluss HK. Requirement of the ATM/p53 tumor suppressor pathway for glucose homeostasis. Mol Cell Biol 2010; 30:5787-94; PMID:20956556; http://dx.doi.org/10.1128/MCB.00347-10.
17. Ditch S, Paull TT. The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem Sci 2012; 37:15-22; PMID:22079189; http://dx.doi.org/10.1016/j.tibs.2011.10.002.
18. Guo Z, Kozlov S, Lavin MF, Person MD, Paull TT. ATM activation by oxidative stress. Science 2010; 330:517-21; PMID:20966255; http://dx.doi.org/10. 1126/science.1192912.
19. Barzilai A, Yamamoto K. DNA damage responses to oxidative stress. DNA Repair (Amst) 2004; 3:1109-15; PMID:15279799; http://dx.doi.org/10.1016/j. dnarep.2004.03.002.
20. Gao D, Wei C, Chen L, Huang J, Yang S, Diehl AM. Oxidative DNA damage and DNA repair enzyme expression are inversely related in murine models of fatty liver disease. Am J Physiol Gastrointest Liver Physiol 2004; 287:1070-7; PMID:15231485; http:// dx.doi.org/10.1152/ajpgi.00228.2004.
21. Matsuzawa N, Takamura T, Kurita S, Misu H, Ota T, Ando H, et al. Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 2007; 46:1392-403; PMID:17929294; http://dx.doi.org/10.1002/ hep.21874.
22. Barzilai A, Rotman G, Shiloh Y. ATM deficiency and oxidative stress: a new dimension of defective response to DNA damage. DNA Repair (Amst) 2002; 1:3-25; PMID:12509294; http://dx.doi.org/10.1016/S1568-7864(01)00007-6.
23. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506; PMID:12556884; http://dx.doi.org/10.1038/nature01368.
24. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, et al. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 1996; 86:159-71; PMID:8689683; http://dx.doi.org/10.1016/S0092-8674(00)80086-0.
25. Elson A, Wang Y, Daugherty CJ, Morton CC, Zhou F, Campos-Torres J, et al. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc Natl Acad Sci USA 1996; 93:13084-9; PMID:8917548; http:// dx.doi.org/10.1073/pnas.93. 23.13084.
26. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects and thymic lymphoma. Genes Dev 1996; 10:2411-22; PMID:8843194; http:// dx.doi.org/10.1101/gad.10.19.2411.
27. Kinner A, Wu W, Staudt C, Iliakis G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 2008; 36:5678-94; PMID:18772227; http://dx.doi. org/10.1093/nar/gkn550.
28. Yu J, Zhang L. PUMA, a potent killer with or without p53. Oncogene 2008; 27:71-83; PMID:19641508; http://dx.doi.org/10.1038/onc.2009.45.
29. Krizhanovsky V, Yon M, Dickins RA, Hearn S, Simon J, Miething C, et al. Senescence of activated stellate cells limits liver fibrosis. Cell 2008; 134:657-67; PMID:18724938; http://dx.doi.org/10.1016/j.cell.2008.06.049.
30. Povero D, Busletta C, Novo E, di Bonzo LV, Cannito S, Paternostro C, et al. Liver fibrosis: a dynamic and potentially reversible process. Histol Histopathol 2010; 25:1075-91; PMID:20552556.
31. Zhan SS, Jiang JX, Wu J, Halsted C, Friedman SL, Zern MA, et al. Phagocytosis of apoptotic bodies by hepatic stellate cells induces NADPH oxidase and is associated with liver fibrosis in vivo. Hepatology 2006; 43:435-43; PMID:16496318; http://dx.doi.org/10.1002/hep.21093.
32. Canbay A, Friedman S, Gores GJ. Apoptosis: the nexus of liver injury and fibrosis. Hepatology 2004; 39:273-8; PMID:14767974; http://dx.doi.org/10.1002/ hep.20051.
33. Villunger A, Michalak EM, Coultas L, Müllauer F, Böck G, Ausserlechner MJ, et al. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003; 302:1036- 8; PMID:14500851; http://dx.doi.org/10.1126/science.1090072.
34. Cazanave SC, Mott JL, Elmi NA, Bronk SF, Werneburg NW, Akazawa Y, et al. JNK1-dependent PUMA expression contributes to hepatocyte lipoapoptosis. J Biol Chem 2009; 284:26591-602; PMID:19638343; http://dx.doi.org/10.1074/jbc.M109. 022491.
35. Michalak EM, Jansen ES, Happo L, Cragg MS, Tai L, Smyth GK, et al. Puma and to a lesser extent Noxa are suppressors of Myc-induced lymphomagenesis. Cell Death Differ 2009; 16:684-96; PMID:19148184; http://dx.doi.org/10.1038/cdd. 2008.195.
36. Michalak EM, Villunger A, Adams JM, Strasser A. In several cell types tumour suppressor p53 induces apoptosis largely via Puma but Noxa can contribute. Cell Death Differ 2008; 15:1019-29; PMID:18259198; http://dx.doi.org/10.1038/cdd.2008.16.
37. Farinati F, Cardin R, Bortolami M, Grottola A, Manno M, Colantoni A, et al. Estrogens receptors and oxidative damage in the liver. Mol Cell Endocrinol 2002; 193:85-8; PMID:12161006; http://dx.doi.org/10.1016/S0303-7207(02)00100-4.
38. Lu S, Shen KC, Wang Y, Brooks SC, Wang YA. Impaired hepatocyte survival and liver regeneration in Atm-deficient mice. Hum Mol Genet 2005; 14:3019-25; PMID:16141284; http://dx.doi.org/10.1093/hmg/ddi333.
39. Nunomura A, Perry G, Pappolla MA, Wade R, Hirai K, Chiba S, et al. RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease. J Neurosci 1999; 19:1959-64; PMID:10066249.
40. Woodbine L, Brunton H, Goodarzi AA, Shibata A, Jeggo PA. Endogenously induced DNA double strand breaks arise in heterochromatic DNA regions and require ataxia telangiectasia mutated and Artemis for their repair. Nucleic Acids Res 2011; 39:6986-97; PMID:21596788; http://dx.doi.org/10.1093/nar/gkr331.
41. El-Serag HB. Hepatocellular carcinoma. N Engl J Med 2011; 365:1118-27; PMID:21992124; http://dx.doi. org/10.1056/NEJMra1001683.
42. Yasui K, Hashimoto E, Komorizono Y, Koike K, Arii S, Imai Y, et al.; Japan NASH Study Group, Ministry of Health, Labour and Welfare of Japan. Characteristics of patients with nonalcoholic steatohepatitis who develop hepatocellular carcinoma. Clin Gastroenterol Hepatol 2011; 9:428-33; PMID:21320639; http://dx.doi.org/10.1016/j.cgh.2011.01.023.
43. Tang D, Lotze MT, Kang R, Zeh HJ. Apoptosis promotes early tumorigenesis. Oncogene 2011; 30:1851-4; PMID:21151175; http://dx.doi.org/10.1038/onc.2010. 573.
44. Dowman JK, Armstrong MJ, Tomlinson JW, Newsome PN. Current therapeutic strategies in non-alcoholic fatty liver disease. Diabetes Obes Metab 2011; 13:692-702; PMID:21449949; http://dx.doi.org/10.1111/j.1463-326.2011.01403.x.
45. Foster T, Budoff MJ, Saab S, Ahmadi N, Gordon C, Guerci AD. Atorvastatin and antioxidants for the treatment of nonalcoholic fatty liver disease: the St. Francis Heart Study randomized clinical trial. Am J Gastroenterol 2011; 106:71-7; PMID:20842109; http://dx.doi.org/10.1038/ajg.2010.299.
46. Reliene R, Schiestl RH. Antioxidants suppress lymphoma and increase longevity in Atm-deficient mice. J Nutr 2007; 137:229-32; PMID:17182831.
47. Reliene R, Schiestl RH. Experimental antioxidant therapy in ataxia telangiectasia. Clin Med Oncol 2008; 2:431-6; PMID:21892312.
48. Schubert R, Erker L, Barlow C, Yakushiji H, Larson D, Russo A, et al. Cancer chemoprevention by the antioxidant tempol in Atm-deficient mice. Hum Mol Genet 2004; 13:1793-802; PMID:15213104; http:// dx.doi.org/10.1093/hmg/ddh189.
49. Rogers AB, Boutin SR, Whary MT, Sundina N, Ge Z, Cormier K, et al. Progression of chronic hepatitis and preneoplasia in Helicobacter hepaticus-infected A/JCr mice. Toxicol Pathol 2004; 32:668-77; PMID:15513910; http://dx.doi.org/10.1080/01926230490524247.
50. Maurer KJ, Rao VP, Ge Z, Rogers AB, Oura TJ, Carey MC, et al. T-cell function is critical for murine cholesterol gallstone formation. Gastroenterology 2007; 133:1304-15; PMID:17919501; http://dx.doi.org/10.1053/j. gastro.2007.07.005.
51. Sobreira C, Davidson M, King MP, Miranda AF. Dihydrorhodamine 123 identifies impaired mitochondrial respiratory chain function in cultured cells harboring mitochondrial DNA mutations. J Histochem Cytochem 1996; 44:571-9; PMID:8666742; http:// dx.doi.org/10.1177/44.6.8666742.
52. Harlow E, Lane D. Lysing Tissue-Culture Cells for Immunoprecipitation. Cold Spring Harbor Protocols 2006; 2006:4531; http://dx.doi.org/10.1101/pdb. prot4531.