Neuronal intracellular pH directly mediates nitric oxide-induced programmed cell death

Journal of Neurobiology

Volumn 40, Issue 2, 1999, Pages 171-184

  Vincent, Andrea M ^a   TenBroeke, Michelle ^a   Maiese, Kenneth ^a  

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

Author keywords

Apoptosis; Endonuclease; Intracellular pH; Nitric oxide; Primary hippocampal culture

Indexed keywords

ENDONUCLEASE; NITRIC OXIDE;

ACIDIFICATION; ANIMAL CELL; ARTICLE; CELL PH; CONTROLLED STUDY; DNA DEGRADATION; EMBRYO; ENZYME ACTIVITY; ENZYME ANALYSIS; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; APOPTOSIS; CASPASES; DNA FRAGMENTATION; ENDONUCLEASES; FLUORESCEINS; FLUORESCENT DYES; HIPPOCAMPUS; HYDRAZINES; HYDROGEN-ION CONCENTRATION; INTRACELLULAR FLUID; MOLSIDOMINE; NERVE TISSUE PROTEINS; NEURONS; NITRIC ACID; NITRIC OXIDE DONORS; NITROPRUSSIDE; NITROSO COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; RATS; RATS, SPRAGUE-DAWLEY; TRIAZENES;

EID: 0032864715     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199908)40:2<171::AID-NEU4>3.0.CO;2-F     Document Type: Article

References (47)

1. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, Yuan J. 1996. Human ICE/ CED-3 protease nomenclature. Cell 87:171.
2. + antiporter. J Cell Biochem 67:231-240.
3. Chen Q, Benson RS, Whetton AD, Brant SR, Donowitz M, Montrose MH, Dive C, Watson AJ. 1997. Role of acid/ base homeostasis in the suppression of apoptosis in haemopoietic cells by v-Abl protein tyrosine kinase. J Cell Sci 110:379-387.
4. 2+ buffering, a cell property that in some neurons markedly decreases during aging, has a protective effect against NMDA/nitric oxide-induced excitotoxicity. Life Sci 59:389-397.
5. Collins MK, Furlong IJ, Malde P, Ascaso R, Oliver J, Lopez Rivas A. 1996. An apoptotic endonuclease activated either by decreasing pH or by increasing calcium. J Cell Sci 109:2393-2399.
6. Deng G, Wu R. 1983. Terminal transferase: use of the tailing of DNA and for in vitro mutagenesis. Methods Enzymol 100:96-116.
7. Didier M, Bursztajn S, Adamec E, Passani L, Nixon RA, Coyle JT, Wei JY, Berman S. 1996. DNA strand breaks induced by sustained glutamate excitotoxicity in primary neuronal cultures. J Neurosci 16:2238-2250.
8. Ellis HM, Horvitz HR. 1986. Genetic control of programmed cell death in the nematode C. elegans. Cell 44:817-829.
9. Endoh M, Maiese K, Wagner J. 1994. Expression of the inducible form of nitric oxide synthase by reactive astrocytes after transient global ischemia. Brain Res 651:92-100.
10. Furlong IJ, Ascaso R, Lopez Rivas A, Collins MK. 1997. Intracellular acidification induces apoptosis by stimulating ICE-like protease activity. J Cell Sci 110:653-661.
11. Gonzalez RG, Haxo RS, Schleich T. 1980. Mechanism of action of polymeric aurintricarboxylic acid, a potent inhibitor of protein-nucleic acid interactions. Biochemistry 19:4299-4303.
12. Goodwin JL, Uemura E, Cunnick JE. 1995. Microglial release of nitric oxide by the synergistic action of beta-amyloid and IFN-gamma. Brain Res 692:207-214.
13. Gottlieb RA, Nordberg J, Skowronski E, Babior BM. 1996. Apoptosis induced in Jurkat cells by several agents is preceded by intracellular acidification. Proc Natl Acad Sci USA 93:654-658.
14. Gunzel D, Durry S, Schlue WR. 1997. Intracellular alkalinization causes Mg2+ release from intracellular binding sites in leech Retzius neurons. Pflugers Arch 435:65-73.
15. Hara A, Yoshimi N, Hirose Y, Ino N, Tanaka T, Mori H. 1995. DNA fragmentation in granular cells of human cerebellum following global ischemia. Brain Res 697: 247-250.
16. Hunot S, Boissiere F, Faucheux B, Brugg B, Mouatt-Prigent A, Agid Y, Hirsch EC. 1996. Nitric oxide synthase and neuronal vulnerability in Parkinson's disease. Neuroscience 72:355-363.
17. Jenner P, Olanow CW. 1996. Oxidative stress and the pathogenesis of Parkinson's disease. Neurology 47(Suppl 3):S161-S170.
18. Kerr JF, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239-257.
19. Kimura C, Zhao QL, Kondo T, Amatsu M, Fujiwara Y. 1998. Mechanism of UV-induced apoptosis in human leukemia cells: roles of calcium/magnesium-dependent endonuclease, caspase-3, and stress-activated protein kinases. Exp Cell Res 239:411-422.
20. 2+-independent. Blood 91:4350-4360.
21. Madaio MP, Fabbi M, Tiso M, Daga A, Puccetti A. 1996. Spontaneously produced anti-DNA/DNase I autoantibodies modulate nuclear apoptosis in living cells. Eur J Immunol 26:3035-3041.
22. Maiese K. 1998a. Cellular mechanisms of neuronal protec-tion by metabotropic glutamate receptors. In: Robertson JT, Nowak TS, editors. Frontiers in cerebrovascular disease: mechanisms, diagnosis, and treatment. Armonk, NY: Futura. p 281-297.
23. Maiese K. 1998b. From the bench to the bedside: the molecular management of cerebral ischemia. Clin Neuropharmacol 21:1-7.
24. Maiese K, Boccone L. 1995. Neuroprotection by peptide growth factors against anoxia and nitric oxide toxicity requires modulation of protein kinase C. J Cereb Blood Flow Metab 15:440-449.
25. Maiese K, Boniece I, DeMeo D, Wagner JA. 1993a. Peptide growth factors protect against ischemia in culture by preventing nitric oxide toxicity. J Neurosci 13:3034-3040.
26. Maiese K, Boniece IR, Skurat K, Wagner JA. 1993b. Protein kinases modulate the sensitivity of hippocampal neurons to nitric oxide toxicity and anoxia. J Neurosci Res 36:77-87.
27. Maiese K, Vincent AM. 1999. Group I metabotropic receptors down-regulate nitric oxide induced CPP32 activity in rat hippocampal neurons. Neurosci Lett (in press).
28. Maiese K, Wagner J, Boccone L. 1994. Nitric oxide: a downstream mediator of calcium toxicity in the ischemic cascade. Neurosci Lett 166:43-47.
29. Nakashima MN, Yamashita K, Kataoka Y, Yamashita YS, Niwa M. 1995. Time course of nitric oxide synthase activity in neuronal, glial, and endothelial cells of rat striatum following focal cerebral ischemia. Cell Mol Neurobiol 15:341-349.
30. Nishio E, Watanabe Y. 1998. NO induced apoptosis accompanying the change of oncoprotein expression. Life Sci 62:239-245.
31. Pandey S, Walker PR, Sikorska M. 1997. Identification of a novel 97 kDa endonuclease capable of internucleosomal DNA cleavage. Biochemistry 36:711-720.
32. Park HJ, Makepeace CM, Lyons JC, Song CW. 1996. Effect of intracellular acidity and ionomycin on apoptosis in HL-60 cells. Eur J Cancer 3:540-546.
33. Ritucci NA, Dean JB, Putnam RW. 1997. Intracellular pH response to hypercapnia in neurons from chemosensitive areas of the medulla. Am J Physiol 273:R433-R441.
34. Roberts E Jr, Chih CP. 1997. The influence of age of pH regulation in hippocampal slices before, during and after anoxia. J Cereb Blood Flow Metab 17:560-566.
35. Shen H, Chan J, Kass IS, Bergold PJ. 1995. Transient acidosis induces delayed neurotoxicity in cultured hippocampal slices. Neurosci Lett 185:115-118.
36. Takasu T, Lyons JC, Park HJ, Song CW. 1998. Apoptosis and perturbation of cell cycle progression in an acidic environment after hyperthermia. Cancer Res 58:2504-2508.
37. Thomas RC. 1984. Experimental displacement of intracellular pH and the mechanism of its subsequent recovery. J Physiol 354:3P-22P.
38. Toku K, Tanaka J, Yano H, Desaki J, Zhang B, Yang L, Ishihara K, Sakanaka M, Maeda N. 1998. Microglial cells prevent nitric oxide-induced neuronal apoptosis in vitro. J Neurosci Res 53:415-425.
39. Torriglia A, Chaudun E, Chany-Fournier F, Jeanny JC, Courtois Y, Counis MF. 1995. Involvement of DNase II in nuclear degeneration during lens cell differentiation. J Biol Chem 270:28579-28585.
40. Tsao N, Lei HY. 1996. Activation of the Na(+)/H(+) antiporter, Na+/HCO3(-)/CO3(2-) cotransporter, or Cl(-)/HCO3(-) exchanger in spontaneous thymocyte apoptosis. J Immunol 157:1107-1116.
41. Vincent AM, Maiese K. 1999. Nitric oxide induction of neuronal endonuclease activity in programmed cell death. Exp Cell Res 246:290-300.
42. Vincent AM, Mohammad Y, Ahmad I, Greenberg R, Maiese K. 1997. Metabotropic glutamate receptors prevent nitric oxide induced programmed cell death. J Neurosci Res 50:549-564.
43. Vincent AM, TenBroeke M, Maiese K. 1999. Metabotropic glutamate receptors prevent programmed cell death through the modulation of neuronal endonuclease activity and intracellular pH. Exp Neurol 155:79-94.
44. Wyllie AH, Beattie GJ, Hargreaves AD. 1981. Chromatin changes in apoptosis. Histochem J 13:681-692.
45. Xie Z, Schendel S, Matsuyama S, Reed JC. 1998. Acidic pH promotes dimerization of Bcl-2 family proteins. Biochemistry 37:6410-6418.
46. Zanke BW, Lee C, Arab S, Tannock IF. 1998. Death of tumor cells after intracellular acidification is dependent on stress-activated protein kinases (SAPK/JNK) pathway activation and cannot be inhibited by Bcl-2 expression or interleukin 1beta-converting enzyme inhibition. Cancer Res 58:2801-2808.
47. Zhan RZ, Fujiwara N, Yamakura T, Taga K, Fukuda S, Endoh H, Shimoji K. 1997. NMDA induces a biphasic change in intracellular pH in rat hippocampal slices. Brain Res 760:179-186.