Identification of a novel phosphorylation site of acyl-CoA binding protein (ACBP) in nodularin-induced apoptotic hepatocytes

Experimental Cell Research

Volumn 314, Issue 10, 2008, Pages 2141-2149

  Solstad, Therese ^a,b   Fismen, Lise ^a   Garberg, Hilde ^a   Fladmark, Kari E ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

ACBP; Algal toxin; Apoptosis; MALDI ToF; Mass spectrometry; Nodularin; Phosphopeptide; Phosphorylation; Phosphorylation site; Translocation

Indexed keywords

AMINO ACID; CALPAIN; DIAZEPAM BINDING INHIBITOR; LIVER PROTEIN; LONG CHAIN FATTY ACID; NODULARIN; PEPTIDE; PHOSPHATASE; PHOSPHOPROTEIN; SERYLGLUTAMINYLALANYLASPARTYLPHENYLALANYLASPARTYLLYSYLALANYLALANYL GLUTAMYLGLUTAMYLVALYLLYSYLARGINYLLEUCYLLYSINE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MEMBRANE; LIVER CELL; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ALGAE; NODULARIA SPUMIGENA; RATTUS;

EID: 44749092646     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.03.014     Document Type: Article

References (40)

1. Fladmark K.E., Brustugun O.T., Hovland R., Boe R., Gjertsen B.T., Zhivotovsky B., and Doskeland S.O. Ultrarapid caspase-3 dependent apoptosis induction by serine/threonine phosphatase inhibitors. Cell Death Differ 6 (1999) 1099-1108
2. Runnegar M.T., Jackson A.R., and Falconer I.R. Toxicity of the cyanobacterium Nodularia spumigena Mertens. Toxicon 26 (1988) 143-151
3. Honkanen R.E., Dukelow M., Zwiller J., Moore R.E., Khatra B.S., and Boynton A.L. Cyanobacterial nodularin is a potent inhibitor of type 1 and type 2A protein phosphatases. Mol. Pharmacol. 40 (1991) 577-583
4. Bright J., and Khar A. Apoptosis: programmed cell death in health and disease. Biosci. Rep. 14 (1994) 67-81
5. Solstad T., and Fladmark K.E. Algal toxins as guidance to identify phosphoproteins with key roles in apoptotic cell death. Curr. Pharm. Biotechnol. 7 (2006) 209-215
6. Knudsen J., Hojrup P., Hansen H.O., Hansen H.F., and Roepstorff P. Acyl-CoA-binding protein in the rat. Purification, binding characteristics, tissue concentrations and amino acid sequence. Biochem. J. 262 (1989) 513-519
7. Mikkelsen J., and Knudsen J. Acyl-CoA-binding protein from cow. Binding characteristics and cellular and tissue distribution. Biochem. J. 248 (1987) 709-714
8. Van Loo G., Demol H., van Gurp M., Hoorelbeke B., Schotte P., Beyaert R., Zhivotovsky B., Gevaert K., Declercq W., Vandekerckhove J., and Vandenabeele P. A matrix-assisted laser desorption ionization post-source decay (MALDI-PSD) analysis of proteins released from isolated liver mitochondria treated with recombinant truncated Bid. Cell Death Differ. 9 (2002) 301-308
9. Elholm M., Garras A., Neve S., Tornehave D., Lund T.B., Skorve J., Flatmark T., Kristiansen K., and Berge R.K. Long-chain acyl-CoA esters and acyl-CoA binding protein are present in the nucleus of rat liver cells. J. Lipid Res. 41 (2000) 538-545
10. Hansen J.S., Faergeman N.J., Kagelund B.B., and Knudsen J. Acyl-CoA binding protein (ACBP) localizes to ER and Golgi in a ligand dependent manner in mammalian cells. Biochem. J. (2007)
11. Rasmussen J.T., Rosendal J., and Knudsen J. Interaction of acyl-CoA binding protein (ACBP) on processes for which acyl-CoA is a substrate, product or inhibitor. Biochem. J. 292 Pt 3 (1993) 907-913
12. Guidotti A., Forchetti C.M., Corda M.G., Konkel D., Bennett C.D., and Costa E. Isolation, characterization, and purification to homogeneity of an endogenous polypeptide with agonistic action on benzodiazepine receptors. Proc. Natl. Acad. Sci. U. S. A. 80 (1983) 3531-3535
13. Gray P.W., Glaister D., Seeburg P.H., Guidotti A., and Costa E. Cloning and expression of cDNA for human diazepam binding inhibitor, a natural ligand of an allosteric regulatory site of the gamma-aminobutyric acid type A receptor. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 7547-7551
14. Papadopoulos V., Berkovich A., Krueger K.E., Costa E., and Guidotti A. Diazepam binding inhibitor and its processing products stimulate mitochondrial steroid biosynthesis via an interaction with mitochondrial benzodiazepine receptors. Endocrinology 129 (1991) 1481-1488
15. Sjoholm A., Funakoshi A., Efendic S., Ostenson C.G., and Hellerstrom C. Long term inhibitory effects of pancreastatin and diazepam binding inhibitor on pancreatic beta-cell deoxyribonucleic acid replication, polyamine content, and insulin secretion. Endocrinology 128 (1991) 3277-3282
16. Borboni P., Condorelli L., De Stefanis P., Sesti G., and Lauro R. Modulation of insulin secretion by diazepam binding inhibitor and its processing products. Neuropharmacology 30 (1991) 1399-1403
17. Faergeman N.J., and Knudsen J. Acyl-CoA binding protein is an essential protein in mammalian cell lines. Biochem. J. 368 (2002) 679-682
18. Huang H., Atshaves B.P., Frolov A., Kier A.B., and Schroeder F. Acyl-coenzyme A binding protein expression alters liver fatty acyl-coenzyme A metabolism. Biochemistry 44 (2005) 10282-10297
19. Shulga N., and Pastorino J.G. Acyl coenzyme A-binding protein augments bid-induced mitochondrial damage and cell death by activating mu-calpain. J. Biol. Chem. 281 (2006) 30824-30833
20. Gossett R.E., Frolov A.A., Roths J.B., Behnke W.D., Kier A.B., and Schroeder F. Acyl-CoA binding proteins: multiplicity and function. Lipids 31 (1996) 895-918
21. Rasmussen J.T., Borchers T., and Knudsen J. Comparison of the binding affinities of acyl-CoA-binding protein and fatty-acid-binding protein for long-chain acyl-CoA esters. Biochem. J. 265 (1990) 849-855
22. Rosendal J., Ertbjerg P., and Knudsen J. Characterization of ligand binding to acyl-CoA-binding protein. Biochem. J. 290 Pt 2 (1993) 321-326
23. Jenkins C.M., Yan W., Mancuso D.J., and Gross R.W. Highly selective hydrolysis of fatty acyl-CoAs by calcium-independent phospholipase A2beta. Enzyme autoacylation and acyl-CoA-mediated reversal of calmodulin inhibition of phospholipase A2 activity. J. Biol. Chem. 281 (2006) 15615-15624
24. de Pablo M.A., Susin S.A., Jacotot E., Larochette N., Costantini P., Ravagnan L., Zamzami N., and Kroemer G. Palmitate induces apoptosis via a direct effect on mitochondria. Apoptosis 4 (1999) 81-87
25. Paumen M.B., Ishida Y., Muramatsu M., Yamamoto M., and Honjo T. Inhibition of carnitine palmitoyltransferase I augments sphingolipid synthesis and palmitate-induced apoptosis. J. Biol. Chem. 272 (1997) 3324-3329
26. Runnegar M.T., Gerdes R.G., and Falconer I.R. The uptake of the cyanobacterial hepatotoxin microcystin by isolated rat hepatocytes. Toxicon 29 (1991) 43-51
27. Mellgren G., Vintermyr O.K., and Doskeland S.O. Okadaic acid, cAMP, and selected nutrients inhibit hepatocyte proliferation at different stages in G1: modulation of the cAMP effect by phosphatase inhibitors and nutrients. J. Cell. Physiol. 163 (1995) 232-240
28. Seglen P.O. Preparation of isolated rat liver cells. Methods Cell Biol. 13 (1976) 29-83
29. Larsen M.R., Thingholm T.E., Jensen O.N., Roepstorff P., and Jorgensen T.J. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell Proteomics 4 (2005) 873-886
30. DeGnore J.P., and Qin J. Fragmentation of phosphopeptides in an ion trap mass spectrometer. J. Am. Soc. Mass Spectrom. 9 (1998) 1175-1188
31. Pontremoli S., Melloni E., Michetti M., Salamino F., Sparatore B., and Horecker B.L. An endogenous activator of the Ca2+-dependent proteinase of human neutrophils that increases its affinity for Ca2+. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 1740-1743
32. Ding W.X., Shen H.M., and Ong C.N. Calpain activation after mitochondrial permeability transition in microcystin-induced cell death in rat hepatocytes. Biochem. Biophys. Res. Commun. 291 (2002) 321-331
33. Furuno T., Kanno T., Arita K., Asami M., Utsumi T., Doi Y., Inoue M., and Utsumi K. Roles of long chain fatty acids and carnitine in mitochondrial membrane permeability transition. Biochem. Pharmacol. 62 (2001) 1037-1046
34. Wieckowski M.R., Brdiczka D., and Wojtczak L. Long-chain fatty acids promote opening of the reconstituted mitochondrial permeability transition pore. FEBS Lett. 484 (2000) 61-64
35. Knudsen J. Acyl-CoA-binding protein (ACBP) and its relation to fatty acid-binding protein (FABP): an overview. Mol. Cell. Biochem. 98 (1990) 217-223
36. Chao H., Martin G.G., Russell W.K., Waghela S.D., Russell D.H., Schroeder F., and Kier A.B. Membrane charge and curvature determine interaction with acyl-CoA binding protein (ACBP) and fatty acyl-CoA targeting. Biochemistry 41 (2002) 10540-10553
37. Fisher E., Nitz I., Gieger C., Grallert H., Gohlke H., Lindner I., Dahm S., Boeing H., Burwinkel B., Rathmann W., Wichmann H.E., Schrezenmeir J., Illig T., and Doring F. Association of acyl-CoA-binding protein (ACBP) single nucleotide polymorphisms and type 2 diabetes in two German study populations. Mol. Nutr Food Res. 51 (2007) 178-184
38. Knudsen J., Jensen M.V., Hansen J.K., Faergeman N.J., Neergaard T.B., and Gaigg B. Role of acylCoA binding protein in acylCoA transport, metabolism and cell signaling. Mol. Cell. Biochem. 192 (1999) 95-103
39. Faergeman N.J., and Knudsen J. Role of long-chain fatty acyl-CoA esters in the regulation of metabolism and in cell signalling. Biochem. J. 323 Pt 1 (1997) 1-12
40. Neely J.R., and Feuvray D. Metabolic products and myocardial ischemia. Am. J. Pathol. 102 (1981) 282-291