Synergistic effect of cAMP and palmitate in promoting altered mitochondrial function and cell death in HepG2 cells

Experimental Cell Research

Volumn 316, Issue 5, 2010, Pages 716-727

  Zhang, Linxia ^a   Seitz, Linsey C ^a   Abramczyk, Amy M ^a   Chan, Christina ^a  

^a Michigan State University   (United States)

Author keywords

Apoptosis; cAMP; Mitochondria; Necrosis; Palmitate

Indexed keywords

CASPASE; CYCLIC AMP; PALMITIC ACID; REACTIVE OXYGEN METABOLITE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE;

ARTICLE; BIOGENESIS; CELL DEATH; CELL STRAIN HEPG2; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LIVER MITOCHONDRION; MITOCHONDRIAL RESPIRATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN SECRETION;

EID: 76749101133     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.12.008     Document Type: Article

References (45)

1. Eitel K., Staiger H., Brendel M.D., Brandhorst D., Bretzel R.G., Haring H.U., and Kellerer M. Different role of saturated and unsaturated fatty acids in beta-cell apoptosis. Biochem. Biophys. Res. Commun. 299 (2002) 853-856
2. Morgan N.G., Dhayal S., Diakogiannaki E., and Welters H.J. The cytoprotective actions of long-chain mono-unsaturated fatty acids in pancreatic beta-cells. Biochem. Soc. Trans. 36 (2008) 905-908
3. Kong J.Y., and Rabkin S.W. Palmitate-induced apoptosis in cardiomyocytes is mediated through alterations in mitochondria: prevention by cyclosporin A. Biochim. Biophys. Acta 1485 (2000) 45-55
4. Ostrander D.B., Sparagna G.C., Amoscato A.A., McMillin J.B., and Dowhan W. Decreased cardiolipin synthesis corresponds with cytochrome c release in palmitate-induced cardiomyocyte apoptosis. J. Biol. Chem. 276 (2001) 38061-38067
5. Wei Y., Wang D., Topczewski F., and Pagliassotti M.J. Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am. J. Physiol. Endocrinol. Metab. 291 (2006) E275-281
6. Srivastava S., and Chan C. Hydrogen peroxide and hydroxyl radicals mediate palmitate-induced cytotoxicity to hepatoma cells: relation to mitochondrial permeability transition. Free Radic. Res. 41 (2007) 38-49
7. Feldstein A.E., Werneburg N.W., Canbay A., Guicciardi M.E., Bronk S.F., Rydzewski R., Burgart L.J., and Gores G.J. Free fatty acids promote hepatic lipotoxicity by stimulating TNF-alpha expression via a lysosomal pathway. Hepatology 40 (2004) 185-194
8. Ji J., Zhang L., Wang P., Mu Y.M., Zhu X.Y., Wu Y.Y., Yu H., Zhang B., Chen S.M., and Sun X.Z. Saturated free fatty acid, palmitic acid, induces apoptosis in fetal hepatocytes in culture. Exp. Toxicol. Pathol. 56 (2005) 369-376
9. Malhi H., Bronk S.F., Werneburg N.W., and Gores G.J. Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J. Biol. Chem. 281 (2006) 12093-12101
10. Kwon G., Pappan K.L., Marshall C.A., Schaffer J.E., and McDaniel M.L. cAMP dose-dependently prevents palmitate-induced apoptosis by both protein kinase A- and cAMP-guanine nucleotide exchange factor-dependent pathways in beta-cells. J. Biol. Chem. 279 (2004) 8938-8945
11. Welters H.J., Diakogiannaki E., Mordue J.M., Tadayyon M., Smith S.A., and Morgan N.G. Differential protective effects of palmitoleic acid and cAMP on caspase activation and cell viability in pancreatic beta-cells exposed to palmitate. Apoptosis 11 (2006) 1231-1238
12. Webster C.R., and Anwer M.S. Cyclic adenosine monophosphate-mediated protection against bile acid-induced apoptosis in cultured rat hepatocytes. Hepatology 27 (1998) 1324-1331
13. Cullen K.A., McCool J., Anwer M.S., and Webster C.R. Activation of cAMP-guanine exchange factor confers PKA-independent protection from hepatocyte apoptosis. Am. J. Physiol. Gastrointest. Liver Physiol. 287 (2004) G334-343
14. Fladmark K.E., Gjertsen B.T., Doskeland S.O., and Vintermyr O.K. Fas/APO-1(CD95)-induced apoptosis of primary hepatocytes is inhibited by cAMP. Biochem. Biophys. Res. Commun. 232 (1997) 20-25
15. Li J., Yang S., and Billiar T.R. Cyclic nucleotides suppress tumor necrosis factor alpha-mediated apoptosis by inhibiting caspase activation and cytochrome c release in primary hepatocytes via a mechanism independent of Akt activation. J. Biol. Chem. 275 (2000) 13026-13034
16. Srivastava S., Zhang L., Jin R., and Chan C. A novel method incorporating gene ontology information for unsupervised clustering and feature selection. PLoS ONE 3 (2008) e3860
17. Furman B., Pyne N., Flatt P., and O'Harte F. Targeting beta-cell cyclic 3′5′ adenosine monophosphate for the development of novel drugs for treating type 2 diabetes mellitus. A review. J. Pharm. Pharmacol. 56 (2004) 1477-1492
18. Woerle H.J., Popa E., Dostou J., Welle S., Gerich J., and Meyer C. Exogenous insulin replacement in type 2 diabetes reverses excessive hepatic glucose release, but not excessive renal glucose release and impaired free fatty acid clearance. Metabolism 51 (2002) 1494-1500
19. Boden G., Chen X., Capulong E., and Mozzoli M. Effects of free fatty acids on gluconeogenesis and autoregulation of glucose production in type 2 diabetes. Diabetes 50 (2001) 810-816
20. Skowronski R., Hollenbeck C.B., Varasteh B.B., Chen Y.D., and Reaven G.M. Regulation of non-esterified fatty acid and glycerol concentration by insulin in normal individuals and patients with type 2 diabetes. Diabet. Med. 8 (1991) 330-333
21. Goldenthal M.J., and Marin-Garcia J. Mitochondrial signaling pathways: a receiver/integrator organelle. Mol. Cell. Biochem. 262 (2004) 1-16
22. Newmeyer D.D., and Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112 (2003) 481-490
23. Saelens X., Festjens N., Vande Walle L., van Gurp M., van Loo G., and Vandenabeele P. Toxic proteins released from mitochondria in cell death. Oncogene 23 (2004) 2861-2874
24. Cereghetti G.M., and Scorrano L. The many shapes of mitochondrial death. Oncogene 25 (2006) 4717-4724
25. Perfettini J.L., Roumier T., and Kroemer G. Mitochondrial fusion and fission in the control of apoptosis. Trends Cell Biol. 15 (2005) 179-183
26. Golstein P., and Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci. 32 (2007) 37-43
27. Zong W.X., and Thompson C.B. Necrotic death as a cell fate. Genes Dev. 20 (2006) 1-15
28. Orrenius S., Gogvadze V., and Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu. Rev. Pharmacol. Toxicol. 47 (2007) 143-183
29. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 552 (2003) 335-344
30. Darzynkiewicz Z., Juan G., Li X., Gorczyca W., Murakami T., and Traganos F. Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 27 (1997) 1-20
31. Garrett R.H., and Grisham C.M. Biochemistry (1999), Brooks/Cole-Thomson Learning, Pacific Grove, CA
32. Listenberger L.L., Han X., Lewis S.E., Cases S., Farese Jr. R.V., Ory D.S., and Schaffer J.E. Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 3077-3082
33. Srivastava S., and Chan C. Application of metabolic flux analysis to identify the mechanisms of free fatty acid toxicity to human hepatoma cell line. Biotechnol. Bioeng. 99 (2008) 399-410
34. Green D.R., and Reed J.C. Mitochondria and apoptosis. Science 281 (1998) 1309-1312
35. Cory S., and Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2 (2002) 647-656
36. Srivastava S., Li Z., Yang X., Yedwabnick M., Shaw S., and Chan C. Identification of genes that regulate multiple cellular processes/responses in the context of lipotoxicity to hepatoma cells. BMC Genomics 8 (2007) 364
37. Hock M.B., and Kralli A. Transcriptional control of mitochondrial biogenesis and function. Annu. Rev. Physiol. 71 (2009) 177-203
38. Perez-de-Arce K., Foncea R., and Leighton F. Reactive oxygen species mediates homocysteine-induced mitochondrial biogenesis in human endothelial cells: modulation by antioxidants. Biochem. Biophys. Res. Commun. 338 (2005) 1103-1109
39. Miranda S., Foncea R., Guerrero J., and Leighton F. Oxidative stress and upregulation of mitochondrial biogenesis genes in mitochondrial DNA-depleted HeLa cells. Biochem. Biophys. Res. Commun. 258 (1999) 44-49
40. Yu T., Robotham J.L., and Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 2653-2658
41. Shen X., Zheng S., Thongboonkerd V., Xu M., Pierce Jr. W.M., Klein J.B., and Epstein P.N. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am. J. Physiol. 287 (2004) E896-905
42. Deniaud A., Sharaf el dein O., Maillier E., Poncet D., Kroemer G., Lemaire C., and Brenner C. Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene 27 (2008) 285-299
43. Rusnak F., and Mertz P. Calcineurin: form and function. Physiol. Rev. 80 (2000) 1483-1521
44. Cribbs J.T., and Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8 (2007) 939-944
45. Karaskov E., Scott C., Zhang L., Teodoro T., Ravazzola M., and Volchuk A. Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 147 (2006) 3398-3407