Insulin blocks cytochrome c release in the reperfused brain through PI3-K signaling and by promoting Bax/Bcl-XL binding

Journal of Neurochemistry

Volumn 106, Issue 3, 2008, Pages 1248-1258

  Sanderson, Thomas H ^a   Kumar, Rita ^a   Sullivan, Jonathon M ^a   Krause, Gary S ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bax; Cytochrome c; Hippocampus; Insulin; Ischemia; Neuroprotection

Indexed keywords

CYTOCHROME C; INSULIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BCL XL; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN PERFUSION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME RELEASE; HORMONE ACTION; MALE; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RAT; REPERFUSION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; BRAIN ISCHEMIA; CYTOCHROMES C; INSULIN; MALE; PROTEIN BINDING; RATS; RATS, LONG-EVANS; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 48249135491     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05473.x     Document Type: Article

References (46)

1. Adachi M., Higuchi H., Miura S., Azuma T., Inokuchi S., Saito H., Kato S. Ishii H. (2004) Bax interacts with the voltage-dependent anion channel and mediates ethanol-induced apoptosis in rat hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G695 G705.
2. Basu A. Haldar S. (2003) Identification of a novel Bcl-xL phosphorylation site regulating the sensitivity of taxol- or 2-methoxyestradiol-induced apoptosis. FEBS Lett. 538, 41 47.
3. Brunet A., Bonni A., Zigmond M. J., Lin M. Z., Juo P., Hu L. S., Anderson M. J., Arden K. C., Blenis J. Greenberg M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857 868.
4. Cao G., Minami M., Pei W., Yan C., Chen D., O'Horo C., Graham S. H. Chen J. (2001) Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death. J. Cereb. Blood Flow Metab. 21, 321 333.
5. Cao G., Luo Y., Nagayama T., Pei W., Stetler R. A., Graham S. H. Chen J. (2002) Cloning and characterization of rat caspase-9; implications for a role in mediating caspase-3 activation and hippocampal cell death after transient cerebral ischemia. J. Cereb. Blood Flow Metab. 22, 534 546.
6. Cao G., Xiao M., Sun F., Xiao X., Pei W., Li J., Graham S. H., Simon R. P. Chen J. (2004) Cloning of a novel Apaf-1-interacting protein: a potent suppressor of apoptosis and ischemic neuronal cell death. J. Neurosci. 24, 6189 6201.
7. Cardone M. H., Roy N., Stennicke H. R., Salvesen G. S., Franks T. F., Stanbridge E., Frisch S. Reed J. C. (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282, 1318 1321.
8. Chiesa R., Piccardo P., Dossena S., Nowoslawski L., Roth K. A., Ghetti B. Harris D. A. (2005) Bax deletion prevents neuronal loss but not neurological symptoms in a transgenic model of inherited prion disease. Proc. Natl Acad. Sci. USA 102, 238 243.
9. Claeys I., Simonet G., Poels J., Loy T. V., Vercammen L., Loof A. D. Broeck J. V. (2002) Insulin-related peptides and their conserved signal transduction pathway. Peptides 23, 807 816.
10. Del Peso L., Gonzalez-Garcia M., Page C., Herrera R. Nunez G. (1997) Interleukin-3 induced phosphorylation of BAD through the protein kinase Akt. Science 278, 687 689.
11. Dudek H., Datta S. R., Franke T. F., Birnbaum M. J., Yao R., Cooper G. M., Segal R. A., Kaplan D. R. Greenberg M. E. (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275, 661 665.
12. Fujimura M., Morita-Fujimura Y., Murakami K., Kawase M. Chan P. H. (1998) Cytosolic redistribution of cytochrome c after transient focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 18, 1239 1247.
13. Fukuoka S., Yeh H., Mandybur T. I. Tew J. M. Jr (1989) Effects of insulin on acute experimental cerebral ischemia in gerbils. Stroke 20, 396 399.
14. Gardai S. J., Hildeman D. A., Frankel S. K., Whitlock B. B., Frasch S. C., Borregaard N., Marrack P., Bratton D. L. Henson P. M. (2004) Phosphorylation of Bax ser184 by Akt regulates its activity and apoptosis in neutrophils. J. Biol. Chem. 279, 21085 21095.
15. Goldstein J. C., Waterhouse N. J., Juin P., Evan G. I. Green D. R. (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nat. Cell Biol. 2, 156 162.
16. Goodner C. J., Hom F. G. Berrie M. A. (1980) Investigation of the effect of insulin upon regional brain glucose metabolism in the rat in vivo. Endocrinology 107, 1827 1832.
17. Heiskanen K. M., Bhat M. B., Wang H. W., Ma J. Nieminen A. L. (1999) Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells. J. Biol. Chem. 274, 5654 5658.
18. Hetz C., Vitte P., Bombran A. et al. (2005) Bax channel inhibitors prevent mitochondrial-mediated apoptosis and protect neurons in a model of global brain ischemia. J. Biol. Chem. 280, 42960 42970.
19. Jenkins L. W., Povlishock J. T., Lewelt W., Miller J. D. Becker D. P. (1981) The role of postischemic recirculation in the development of ischemic neuronal injury following complete cerebral ischemia. Acta Neuropathol. 5, 205 220.
20. 125I] insulin receptor binding sites in developing and adult rat brain. J. Comp. Neurol. 333, 375 397.
21. Kawano T., Fukunaga K., Takeuchi Y., Morioka M., Yano S., Hamada J., Ushio Y. Miyamoto E. (2001) Neuroprotective effect of sodium orthovanadate on delayed neuronal death after transient forebrain ischemia in gerbil hippocampus. J. Cereb. Blood Flow Metab. 21, 1268 1280.
22. Kennedy S. G., Kandel E. S., Cross T. K. Hay N. (1999) Akt/protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria. Mol. Cell. Biol. 19, 5800 5810.
23. Kirino T. Sano K. (1984) Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta Neuropathol. 62, 201 208.
24. Knudsen G. M., Hasselbalch S. G., Hertz M. M. Paulson O. B. (1999) High dose insulin does not increase glucose transfer across the blood-brain barrier in humans: a re-evaluation. Eur. J. Clin. Invest. 29, 687 691.
25. Kumar K., Goosman M., Krause G. S., Nayini N. R., Estrada R., Hoehner T. J., White B. C. Koestner A. (1987) Ultrastructural and ionic changes in global ischemic dog brain. Acta Neuropathol. 73, 393 399.
26. Kuwana T. Newmeyer D. D. (2003) Bcl-2 family proteins and the role of mitochondria in apoptosis. Curr. Opin. Cell Biol. 15, 691 699.
27. Lalier L., Cartron P. F., Juin P., Nedelkina S., Manon S., Bechinger B. Vallette F. M. (2007) Bax activation and mitochondrial insertion during apoptosis. Apoptosis 12, 887 896.
28. LeMay D. R., Gehua L., Zelenock G. B. D'Alacy L. G. (1988) Insulin administration protects neurologic function in cerebral ischemia in rats. Stroke 19, 1411 1419.
29. Lipton P. (1999) Ischemic cell death in brain neurons. Physiol. Rev. 79, 1431 1568.
30. Lo E. H., Moskowitz M. A. Jacobs T. P. (2005) Exciting, radical, suicidal: how brain cells die after stroke. Stroke 36, 189 192.
31. Ouyang Y. B., Tan Y., Comb M., Liu C. L., Martone M. E., Siesjo B. K. Hu B. R. (1999) Survival- and death-promoting events after transient cerebral ischemia: phosphorylation of Akt, release of cytochrome c and activation of caspase-like proteases. J. Cereb. Blood Flow Metab. 19, 1126 1135.
32. Page A. B., Owen C. R., Kumar R., Miller J. M., Rafols J. A., White B. C., DeGracia D. J. Krause G. S. (2003) Persistent eIF2α (P) is colocalized with cytoplasmic cytochrome c in vulnerable hippocampal neurons after 4 hours of reperfusion following 10-minute complete brain ischemia. Acta Neuropathol. 106, 8 16.
33. Pulsinelli W. A., Jacewicz M., Levy D. E., Petito C. K. Plum F. (1997) Ischemic brain injury and the therapeutic window. Ann. NY Acad. Sci. 835, 187 193.
34. Putcha G. V., Harris C. A., Moulder K. L., Easton R. M., Thompson C. B. Johnson E. M. Jr (2002) Intrinsic and extrinsic pathway signaling during neuronal apoptosis: lessons from the analysis of mutant mice. J. Cell Biol. 57, 441 453.
35. Rizk N. N., Rafols J. Dunbar J. C. (2005) Cerebral ischemia induced apoptosis and necrosis in normal and diabetic rats. Brain Res. 1053, 1 9.
36. Schroeter H., Boyd C. S., Ahmed R., Spencer J. P., Duncan R. F., Rice-Evans C. Cadenas E. (2003) c-Jun N-terminal kinase (JNK)-mediated modulation of brain mitochondria function: new target proteins for JNK signalling in mitochondrion-dependent apoptosis. Biochem. J. 372, 359 369.
37. Shepherd P. R., Withers D. J. Siddle K. (1998) Phosphoinositide 3-kinase: the key switch mechanism in insulin signaling. Biochem. J. 333, 471 490.
38. Smith M. L., Bendek G., Dahlgren N., Rosen I., Wieloch T. Siesjo B. K. (1984) Models for studying long-term recovery following forebrain ischemia in rat. A 2-vessel occlusion model. Acta Neurol. Scand. 69, 385 401.
39. Strong A. J., Fairfield J. E., Monteiro E., Kirby M., Hogg A. R., Snape M. Ross-Field L. (1990) Insulin protects cognitive function in experimental stroke. J. Neurol. Neurosurg. Psych. 53, 847 857.
40. Sugawara T., Fujimura M., Morita-Fujimura Y., Kawase M. Chan P. H. (1999) Mitochondrial release of cytochrome c corresponds to the selective vulnerability of hippocampal CA1 neurons in rats after transient global cerebral ischemia. J. Neurosci. 19, RC39 RC45.
41. Sugawara T., Kawase M., Lewen A., Noshita N., Gasche Y., Fujimura M. Chan P. (2000) Effects of hypotension severity on hippocampal CA1 neurons in a rat global ischemia model. Brain Res. 77, 281 287.
42. Sullivan J. M., Alousi S. S., Hikade K. R., Rafols J. A., Krause G. S. White B. C. (1999) Insulin induces dephosphorylation of eukaryotic initiation factor 2alpha and restores protein synthesis in vulnerable hippocampal neurons after transient brain ischemia. J. Cereb. Blood Flow Metab. 19, 1010 1019.
43. Voll C. L. Auer R. N. (1991) Insulin attenuates ischemic brain damage independent of its hypoglycemic effect. J. Cereb. Blood Flow Metab. 11, 1006 1014.
44. White F. A., Keller-Peck C. R., Knudson C. M., Korsmeyer S. J. Snider W. D. (1998) Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J. Neurosci. 8, 428 439.
45. Willis S. N., Fletcher J. I., Kaufmann T. et al. (2007) Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315, 856 859.
46. Zhan R. Z., Wu C., Fujiwara H., Taga K., Qi S., Naito M. Shimoji K. (2001) Both caspase-dependent and caspase-independent pathways may be involved in hippocampal CA1 neuronal death because of loss of cytochrome c from mitochondria in a rat forebrain ischemia model. J. Cereb. Blood Flow Metab. 21, 529 540.