H2S protects hippocampal neurons from anoxia-reoxygenation through cAMP-mediated PI3K/Akt/p70S6K cell-survival signaling pathways

Journal of Molecular Neuroscience

Volumn 43, Issue 3, 2011, Pages 453-460

  Shao, Jian Lin ^a   Wan, Xiao Hong ^a   Chen, Yan ^a   Bi, Chun ^a   Chen, Hong Mei ^b   Zhong, Ying ^a   Heng, Xin Hua ^a   Qian, Jin Qiao ^a  

^a KUNMING MEDICAL UNIVERSITY   (China)

^b Kunming Tongren Hospital   (China)

Author keywords

Akt; cAMP; H2S; OGD R; P70S6k; PI3K

Indexed keywords

CYCLIC AMP; CYCLIC AMP BINDING PROTEIN; HYDROGEN SULFIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P70; RAPAMYCIN; S6 KINASE; TRICIRIBINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL HYPOXIA; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; HIPPOCAMPUS; NERVE INJURY; NEUROPROTECTION; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; RAT; REOXYGENATION; SIGNAL TRANSDUCTION; AIR POLLUTANT; ANIMAL; ANOXIA; CELL CULTURE; CYTOLOGY; METABOLISM; NERVE CELL; REPERFUSION INJURY; WISTAR RAT;

RATTUS;

AIR POLLUTANTS; ANIMALS; ANIMALS, NEWBORN; ANOXIA; CELL SURVIVAL; CELLS, CULTURED; CYCLIC AMP; HIPPOCAMPUS; HYDROGEN SULFIDE; NEURONS; PHOSPHATIDYLINOSITOL 3-KINASE; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; REPERFUSION INJURY; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION;

EID: 79955662370     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-010-9464-4     Document Type: Article

References (58)

1. Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066-1071 (Pubitemid 26140863)
2. Bruer U, Weih MK, Isaev NK, Meisel A, Ruscher K, Bergk A, Trendelenburg G, Wiegand F, Victorov IV, Dirnagl U (1997) Induction of tolerance in rat cortical neurons: hypoxic preconditioning. FEBS Lett 414:117-121 (Pubitemid 27380366)
3. Cass LA, Summers SA, Prendergast GV, Backer JM, Birnbaum MJ, Meinkoth JL (1999) Protein kinase A-dependent and -independent signaling pathways contribute to cyclic AMP-stimulated proliferation. Mol Cell Biol 19:5882-5891 (Pubitemid 29399293)
4. Chan PH (2004) Future targets and cascades for neuroprotective strategies. Stroke 35:2748-2750
5. Chen Y, Zheng Y, Foster DA (2003) Phospholipase D confers rapamycin resistance in human breast cancer cells. Oncogene 22:3937-3942 (Pubitemid 36819667)
6. del Zoppo G, Ginis I, Hallenbeck JM, Iadecola C, Wang X, Feuerstein GZ (2000) Inflammation and stroke: putative role for cytokines, adhesion molecules and iNOS in brain response to ischemia. Brain Pathol 10:95-112 (Pubitemid 30056398)
7. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391-397 (Pubitemid 29453643)
8. Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen J (2001) Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294:1942-1945 (Pubitemid 33101594)
9. Ferrer I, Soriano MA, Vidal A, Planas AM (1995) Survival of parvalbumin-immunoreactive neurons in the gerbil hippocampus following transient forebrain ischemia does not depend on HSP-70 protein induction. Brain Res 692:41-46
10. Freund TF, Buzsaki G, Leon A, Baimbridge KG, Somogyi P (1990) Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia. Exp Brain Res 83:55-66
11. Goodwin LR, Francom D, Dieken FP, Taylor JD, Warenycia MW, Reiffenstein RJ, Dowling G (1989) Determination of sulfide in brain tissue by gas dialysis/ion chromatography: postmortem studies and two case reports. J Anal Toxicol 13:105-109 (Pubitemid 19084165)
12. Gwag BJ, Lobner D, Koh JY, Wie MB, Choi DW (1995) Blockade of glutamate receptors unmasks neuronal apoptosis after oxygen-glucose deprivation in vitro. Neuroscience 68:615-619
13. Han Y, Qin J, Chang X, Yang Z, Bu D, Du J (2005) Modulating effect of hydrogen sulfide on gamma-aminobutyric acid B receptor in recurrent febrile seizures in rats. Neurosci Res 53:216-219 (Pubitemid 41219539)
14. Harada H, Andersen JS, Mann M, Terada N, Korsmeyer SJ (2001) p70S6 kinase signals cell survival as well as growth, inactivating the pro-apoptotic molecule BAD. Proc Natl Acad Sci USA 98:9666-9670 (Pubitemid 32769360)
15. Heinonen H, Nieminen A, Saarela M, Kallioniemi A, Klefstrom J, Hautaniemi S, Monni O (2008) Deciphering downstream gene targets of PI3K/mTOR/p70S6K pathway in breast cancer. BMC Genomics 9:348
16. Hennessy BT, Smith DL, Ram PT, Lu Y, Mills GB (2005) Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat Rev Drug Discov 4:988-1004
17. Hillion JA, Li Y, Maric D, Takanohashi A, Klimanis D, Barker JL, Hallenbeck JM (2006) Involvement of Akt in preconditioning-induced tolerance to ischemia in PC12 cells. J Cereb Blood Flow Metab 26:1323-1331 (Pubitemid 44435246)
18. Horn AP, Gerhardt D, Geyer AB, Valentim L, Cimarosti H, Tavares A, Horn F, Lenz G, Salbego C (2005) Cellular death in hippocampus in response to PI3K pathway inhibition and oxygen and glucose deprivation. Neurochem Res 30:355-361 (Pubitemid 40880811)
19. Hosoi H, Dilling MB, Shikata T, Liu LN, Shu L, Ashmun RA, Germain GS, Abraham RT, Houghton PJ (1999) Rapamycin causes poorly reversible inhibition of mTOR and induces p53-independent apoptosis in human rhabdomyosarcoma cells. Cancer Res 59:886-894 (Pubitemid 29086744)
20. Hosoki R, Matsuki N, Kimura H (1997) The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem Biophys Res Commun 237:527-531 (Pubitemid 27434718)
21. Howard S, Bottino C, Brooke S, Cheng E, Giffard RG, Sapolsky R (2002) Neuroprotective effects of bcl-2 overexpression in hippocampal cultures: interactions with pathways of oxidative damage. J Neurochem 83:914-923 (Pubitemid 35316042)
22. Jiang X, Mu D, Manabat C, Koshy AA, Christen S, Tauber MG, Vexler ZS, Ferriero DM (2004) Differential vulnerability of immature murine neurons to oxygen-glucose deprivation. Exp Neurol 190:224-232 (Pubitemid 39335721)
23. Kimura H (2000) Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem Biophys Res Commun 267:129-133
24. Kimura Y, Kimura H (2004) Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18:1165-1167 (Pubitemid 39561558)
25. Kimura Y, Dargusch R, Schubert D, Kimura H (2006) Hydrogen sulfide protects HT22 neuronal cells from oxidative stress. Antioxid Redox Signal 8:661-670 (Pubitemid 43741334)
26. Kirino T, Sano K (1984) Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta Neuropathol 62:201-208 (Pubitemid 14178596)
27. Kirino T, Tamura A, Sano K (1985) Selective vulnerability of the hippocampus to ischemia - reversible and irreversible types of ischemic cell damage. Prog Brain Res 63:39-58 (Pubitemid 18069472)
28. Lawlor MA, Alessi DR (2001) PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J Cell Sci 114:2903-2910
29. Lee JM, Grabb MC, Zipfel GJ, Choi DW (2000) Brain tissue responses to ischemia. J Clin Invest 106:723-731
30. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431-1568
31. Lowicka E, Beltowski J (2007) Hydrogen sulfide (H2S) - the third gas of interest for pharmacologists. Pharmacol Rep 59:4-24 (Pubitemid 46522698)
32. Malhotra S, Savitz SI, Ocava L, Rosenbaum DM (2006) Ischemic preconditioning is mediated by erythropoietin through PI-3 kinase signaling in an animal model of transient ischemic attack. J Neurosci Res 83:19-27 (Pubitemid 43062006)
33. Mason J, Cardin CJ, Dennehy A (1978) The role of sulphide and sulphide oxidation in the copper molybdenum antagonism in rats and guinea pigs. Res Vet Sci 24:104-108 (Pubitemid 8265034)
34. Mattson MP, Culmsee C, Yu ZF (2000) Apoptotic and antiapoptotic mechanisms in stroke. Cell Tissue Res 301:173-187 (Pubitemid 30459864)
35. Montagne J, Stewart MJ, Stocker H, Hafen E, Kozma SC, Thomas G (1999) Drosophila S6 kinase: a regulator of cell size. Science 285:2126-2129 (Pubitemid 29451430)
36. Nagai Y, Tsugane M, Oka J, Kimura H (2004) Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 18:557-559
37. Noraberg J, Poulsen FR, Blaabjerg M, Kristensen BW, Bonde C, Montero M, Meyer M, Gramsbergen JB, Zimmer J (2005) Organotypic hippocampal slice cultures for studies of brain damage, neuroprotection and neurorepair. Curr Drug Targets CNS Neurol Disord 4:435-452 (Pubitemid 41086760)
38. Park IH, Bachmann R, Shirazi H, Chen J (2002) Regulation of ribosomal S6 kinase 2 by mammalian target of rapamycin. J Biol Chem 277:31423-31429 (Pubitemid 34968942)
39. Prass K, Ruscher K, Karsch M, Isaev N, Megow D, Priller J, Scharff A, Dirnagl U, Meisel A (2002) Desferrioxamine induces delayed tolerance against cerebral ischemia in vivo and in vitro. J Cereb Blood Flow Metab 22:520-525 (Pubitemid 34477773)
40. Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491-498 (Pubitemid 12158810)
41. Qu K, Lee SW, Bian JS, Low CM, Wong PT (2008) Hydrogen sulfide: neurochemistry and neurobiology. Neurochem Int 52:155-165 (Pubitemid 350235691)
42. Ray AM, Benham CD, Roberts JC, Gill CH, Lanneau C, Gitterman DP, Harries M, Davis JB, Davies CH (2003) Capsazepine protects against neuronal injury caused by oxygen glucose deprivation by inhibiting I(h). J Neurosci 23:10146-10153 (Pubitemid 37392563)
43. Reiffenstein RJ, Hulbert WC, Roth SH (1992) Toxicology of hydrogen sulfide. Annu Rev Pharmacol Toxicol 32:109-134
44. Roberson ED, Sweatt JD (1996) Transient activation of cyclic AMP-dependent protein kinase during hippocampal long-term potentiation. J Biol Chem 271:30436-30441 (Pubitemid 26404048)
45. Savage JC, Gould DH (1990) Determination of sulfide in brain tissue and rumen fluid by ion-interaction reversed-phase high-performance liquid chromatography. J Chromatogr 526:540-545
46. Tingley WG, Ehlers MD, Kameyama K, Doherty C, Ptak JB, Riley CT, Huganir RL (1997) Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J Biol Chem 272:5157-5166 (Pubitemid 27090073)
47. Vivanco I, Sawyers CL (2002) The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2:489-501 (Pubitemid 37328931)
48. Warenycia MW, Goodwin LR, Benishin CG, Reiffenstein RJ, Francom DM, Taylor JD, Dieken FP (1989) Acute hydrogen sulfide poisoning. Demonstration of selective uptake of sulfide by the brainstem by measurement of brain sulfide levels. Biochem Pharmacol 38:973-981
49. Weih M, Bergk A, Isaev NK, Ruscher K, Megow D, Riepe M, Meisel A, Victorov IV, Dirnagl U (1999) Induction of ischemic tolerance in rat cortical neurons by 3-nitropropionic acid: chemical preconditioning. Neurosci Lett 272:207-210 (Pubitemid 29412979)
50. Whiteman M, Armstrong JS, Chu SH, Jia-Ling S, Wong BS, Cheung NS, Halliwell B, Moore PK (2004) The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J Neurochem 90:765-768
51. Whiteman M, Cheung NS, Zhu YZ, Chu SH, Siau JL, Wong BS, Armstrong JS, Moore PK (2005) Hydrogen sulphide: a novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem Biophys Res Commun 326:794-798
52. Workman P (2004) Inhibiting the phosphoinositide 3-kinase pathway for cancer treatment. Biochem Soc Trans 32:393-396
53. Wu X, Reiter CE, Antonetti DA, Kimball SR, Jefferson LS, Gardner TW (2004) Insulin promotes rat retinal neuronal cell survival in a p70S6K-dependent manner. J Biol Chem 279:9167-9175 (Pubitemid 38295980)
54. Yang L, Dan HC, Sun M, Liu Q, Sun XM, Feldman RI, Hamilton AD, Polokoff M, Nicosia SV, Herlyn M, Sebti SM, Cheng JQ (2004) Akt/protein kinase B signaling inhibitor-2, a selective small molecule inhibitor of Akt signaling with antitumor activity in cancer cells overexpressing Akt. Cancer Res 64:4394-4399 (Pubitemid 38856907)
55. Yong QC, Pan TT, Hu LF, Bian JS (2008) Negative regulation of beta-adrenergic function by hydrogen sulphide in the rat hearts. J Mol Cell Cardiol 44:701-710
56. Zhang L, Qu Y, Yang C, Tang J, Zhang X, Mao M, Mu D, Ferriero D (2009) Signaling pathway involved in hypoxia-inducible factor-1alpha regulation in hypoxic-ischemic cortical neurons in vitro. Neurosci Lett 461:1-6
57. Zhao W, Zhang J, Lu Y, Wang R (2001) The vasorelaxant effect of H (2)S as a novel endogenous gaseous K(ATP) channel opener. EMBO J 20:6008-6016 (Pubitemid 33049276)
58. Zhao H, Shimohata T, Wang JQ, Sun G, Schaal DW, Sapolsky RM, Steinberg GK (2005) Akt contributes to neuroprotection by hypothermia against cerebral ischemia in rats. J Neurosci 25:9794-9806 (Pubitemid 41510919)