Expression of apoptosis inhibitor protein Mcl1 linked to neuroprotection in CNS neurons

Cell Death and Differentiation

Volumn 11, Issue 11, 2004, Pages 1223-1233

  Mori, M ^a,c   Burgess, D L ^a   Gefrides, L A ^a   Foreman, P J ^a   Opferman, J T ^b   Korsmeyer, S J ^b   Cavalheiro, E A ^c   Naffah Mazzacoratti, Md G ^c   Noebels, J L ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Genetics; Hippocampus; Mcl1; Modifier genes; Neuronal cell death; Neuroprotection; Seizure

Indexed keywords

APOPTOSIS INHIBITOR; CASPASE; MESSENGER RNA; PROTEIN MCL 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DIFFERENTIAL DISPLAY; DNA DAMAGE; GENE IDENTIFICATION; GENETIC SCREENING; GENETIC SUSCEPTIBILITY; GENETIC TRANSCRIPTION; HIPPOCAMPUS; MOUSE; MOUSE STRAIN; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SEIZURE; SEIZURE THRESHOLD; STRAIN DIFFERENCE; TRANSCRIPTION INITIATION; UPREGULATION;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL DEATH; CENTRAL NERVOUS SYSTEM; DNA DAMAGE; GENE EXPRESSION PROFILING; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASM PROTEINS; NEURONS; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEASES; RNA, MESSENGER; UP-REGULATION;

EID: 4644246284     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401483     Document Type: Article

References (56)

1. Xiang H, Kinoshita Y, Knudson CM, Korsmeyer SJ, Schwartzkroin PA and Morrison RS (1998) Bax involvement in p53-mediated neuronal cell death. J. Neurosci. 18: 1363-1373
2. Faherty CJ, Xanthoudakis S and Smeyne RJ (1999) Caspase-3-dependent neuronal death in the hippocampus following kainic acid treatment Brain. Res. Mol. Brain Res. 70: 159-163
3. Holcik M, Thompson CS, Yaraghi Z, Lefebvre CA, MacKenzie AE and Korneluk RG (2000) The hippocampal neurons of neuronal apoptosis inhibitory protein 1 (NAIP1)-deleted mice display increased vulnerability to kainic acid-induced injury. Proc. Natl. Acad. Sci. USA 97: 2286-2290
4. Viswanath V, Wu Z, Fonck C, Wei Q, Boonplueang R and Andersen JK (2000) Transgenic mice neuronally expressing baculoviral p35 are resistant to diverse types of induced apoptosis, including seizure-associated neurodegeneration. Proc. Natl. Acad. Sci. USA 97: 2270-2275
5. Korhonen L, Belluardo N and Lindholm D (2001) Regulation of X-chromosome-linked inhibitor of apoptosis protein in kainic acid-induced neuronal death in the rat hippocampus. Mol. Cell. Neurosci. 17: 364-372
6. Shuttleworth CWR and Connor JA (2001) Strain-dependent differences in calcium signaling predict excitotoxicity in murine hippocampal neurons. J. Neurosci. 21: 4225-4236
7. Morrison RS, Wenzel HJ, Kinoshita Y, Robbins CA, Donehower LA and Schwartzkroin PA (1996) Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J. Neurosci. 16: 1337-1345
8. Schauwecker PE and Steward O (1997) Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sci. USA 94: 4103-4108
9. Roy N, Mahadevan MS, McLean M, Shutler G, Yaraghi Z, Farahani R, Baird S, Besner-Johnston A, Lefebvre C, Kang X, Salih M, Aubry H, Tamay K, Guan X, Ioannou P, Crawford TO, de Jong PJ, Suhr L, Ikeda J-E, Korneluk RG and MacKenzie A (1995) The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80: 167-178
10. Li H and Yuan J (1999) Deciphering the pathways of life and death. Curr. Opin. Cell Biol. 11: 261-266
11. Mullauer L, Gruber P, Sebinger D, Buch J, Wohlfart S and Chott A (2001) Mutations in apoptosis genes: a pathogenetic factor for human disease. Mutat. Res. 488: 211-231
12. Turski WA, Cavalheiro EA, Bortolotto ZA, Mello LM, Schwarz M and Turski L (1984) Seizures produced by pilocarpine in mice: a behavioral, electroencephalographic and morphological analysis. Brain Res. 321: 237-253
13. Kozopas KM, Yang T, Buchan HL, Zhou P and Craig RW (1993) Mcl1, a gene expressed in programmed myeloid cell differentiation has sequence similarity to BCL-2. Proc. Natl. Acad. Sci. USA 90: 3516-3520
14. Hockenbery D, Nunez G, Minniman C, Schreiber RD and Korsmeyer SJ (1990) Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348: 334-336
15. Garcia I, Martinou I, Tsujimoto Y and Martinou J (1992) Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene. Science 258: 302-304
16. Hsu SY and Hsueh AJ (2000) Tissue-specific Bcl-2 protein partners in apoptosis: an ovarian paradigm. Physiol. Rev. 80: 593-614
17. Krajewski S, Bodrug S, Krajewska M, Shabaik A, Gascoyne R, Berean K and Reed JC (1995) Immunohistochemical analysis of Mcl-1 protein in human tissues. Differential regulation of Mcl-1 and Bcl-2 protein production suggests a unique role for Mcl-1 in control of programmed cell death in vivo. Am. J. Pathol. 146: 1309-1319
18. Krajewski S, Krajewska M, Ehrmann J, Sikorska M, Lach B, Chatten J and Reed JC (11997) Immunohistochemical analysis of Bcl-2, Bcl-X, Mcl-1, and Bax in tumors of central and peripheral nervous system origin. Am. J. Pathol. 150: 805-814
19. Cavalheiro EA, Santos NF and Priel MR (1996) The pilocarpine model of epilepsy in mice. Epilepsia 37: 1015-1019
20. Bae J, Leo CP, Hsu SY and Hsueh AJ (2000) MCL-1S, a splicing variant of the antiapoptotic BCL-2 family member MCL-1, encodes a proapoptotic protein possessing only the BH3 domain. J. Biol. Chem. 275: 25255-25261
21. Bingle CD, Craig RW, Swales BM, Singleton V, Zhou P and Whyte MK (2000) Exon skipping in Mcl-1 results in a bcl-2 homology domain 3 only gene product that promotes cell death. J. Biol. Chem. 275: 22136-22146
22. Krajewski S, Bodrug S, Gascoyne R, Berean K, Krajewska M and Reed JC (1994) Immunohistochemical analysis of Mcl-1 and Bcl-2 proteins in normal and neoplastic lymph nodes. Am. J. Pathol. 145: 515-525
23. Yang T, Kozopas KM and Craig RW (1995) The intracellular distribution and pattern of expression of Mcl-1 overlap with but are not identical to, those of Bcl-2. J. Cell Biol. 28: 1173-1184
24. Akgul C, Moulding DA, White MR and Edwards SW (2000) In vivo localization and stability of human Mcl-1 using green fluorescent protein (GFP) fusion proteins. FEBS Lett. 478: 72-76
25. Rinkenberger JL, Horning S, Klocke B, Roth K and Korsmeyer SJ (2000) Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev. 14: 23-27
26. Gross A, McDonnell JM and Korsmeyer SJ (1999) BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13: 1899-1911
27. Huang DC and Strasser A (2000) BH3-only proteins - essential initiators of apoptotic cell death. Cell 103: 839-842
28. Bae J, Hsu SY, Leo CP, Zell K and Hsueh AJ (2001) Underphosphorylated BAD interacts with diverse antiapoptotic Bcl-2 family proteins to regulate apoptosis. Apoptosis 6: 319-330
29. Putcha GV, Moulder KL, Golden JP, Bouillet P, Adams JA, Strasser A and Johnson EM (2001) Induction of BIM, a proapoptotic BH3-only BCL-2 family member, is critical for neuronal apoptosis. Neuron 29: 615-628
30. Whitfield J, Neame SJ, Paquet L, Bernard O and Ham J (2001) Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 29: 629-643
31. Merry DE and Korsmeyer SJ (1997) Bcl-2 gene family in the nervous system. Annu. Rev. Neurosci. 20: 245-267
32. Yuan J and Yankner BA (2000) Apoptosis in the nervous system. Nature 407: 802-809
33. Oppenheim RW, Flavell RA, Vinsant S, Prevette D, Kuan CY and Rakic P (2001) Programmed cell death of developing mammalian neurons after genetic deletion of caspases. J. Neurosci. 21: 4752-4760
34. Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, Du F and Wang X (2003) Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 17: 1475-1486
35. Moulding DA, Giles RV, Spiller DG, White MR, Tidd DM and Edwards SW (2000) Apoptosis is rapidly triggered by antisense depletion of MCL-1 in differentiating U937 cells. Blood 96: 1756-1763
36. Derenne S, Monia B, Dean NM, TaylorJK, Rapp MJ, Harousseau JL, Bataille R and Amiot M (2002) Antisense strategy shows that Mcl-1 rather than Bcl-2 or Bcl-x(L) is an essential survival protein of human myeloma cells. Blood 100: 194-199
37. Zhou P, Levy NB, Xie H, Qian L, Lee CY, Gascoyne RD and Craig RW (2001) Mcl1 transgenic mice exhibit a high incidence of B-cell lymphoma manifested as a spectrum of histologic subtypes. Blood 97: 3902-3909
38. Deininger MH, Weller M, Streffer J and Meyermann R (1999) Antiapoptotic Bcl-2 family protein expression increases with progression of oligodendroglioma. Cancer 86: 1832-1839
39. Ranger AM, Malynn BA and Korsmeyer SJ (2001) Mouse models of cell death. Nat. Genet. 28: 113-118
40. Brunet A and Datta SR (2001) Greenberg ME transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11: 297-305
41. Henshall DC, Clark RS, Adelson PD, Chen M, Watkins SC and Simon RP (2000) Alterations in bcl-2 and caspase gene family protein expression in human temporal lobe epilepsy. Neurology 55: 250-257
42. Henshall DC, Bonislawski DP, Skradski SL, Lan JQ, Meller R and Simon RP (2001) Cleavage of bid may amplify caspase-8-induced neuronal death following focally evoked limbic seizures. Neurobiol. Dis. 8: 568-580
43. Puthier D, Bataille R and Amiot M (1999) IL-6 up-regulates mcl-1 in human myeloma cells through JAK/STAT rather than ras/MAP kinase pathway. Eur. J. Immunol. 29: 3945-3950
44. Puthier D, Thabard W, Rapp M, Etrillard M, Harousseau J, Bataille R and Amiot M (2001) Interferon alpha extends the survival of human myeloma cells through an upregulation of the Mcl-1 anti-apoptotic molecule. Br. J. Haematol. 112: 358-363
45. Jee SH, Shen SC, Chiu HC, Tsai WL and Kuo ML (2001) Overexpression of interleukin-6 in human basal cell carcinoma cell lines increases anti-apoptotic activity and tumorigenic potency. Oncogene 20: 198-208
46. Epling-Burnette PK, Zhong B, Bai F, Jiang K, Bailey RD, Garcia R, Jove R, Djeu JY, Loughran Jr TP and Wei S (2001) Cooperative regulation of Mcl-1 by Janus kinase/stat and phosphatidylinositol 3-kinase contribute to granulocyte-macrophage colony-stimulating factor-delayed apoptosis in human neutrophils. J. Immunol. 166: 7486-7495
47. Fukuchi Y, Kizaki M, Yamato K, Kawamura C, Umezawa A, Hata J, Nishihara T and Ikeda Y (2001) Mcl-1, an early-induction molecule, modulates activin A-induced apoptosis and differentiation of CML cells. Oncogene 20: 704-713
48. Schubert KM and Duronio V (2001) Distinct roles for extracellular-signal-regulated protein kinase (ERK) mitogen-activated protein kinases and phosphatidylinositol 3-kinase in the regulation of Mcl-1 synthesis. Biochem. J. 356: 473-480
49. Garrido YC, Sanabria ER, Funke MG, Cavalheiro EA and Naffah-Mazzacoratti MG (1998) Mitogen-activated protein kinase is increased in the limbic structures of the rat brain during the early stages of status epilepticus. Brain Res. Bull. 47: 223-229
50. De Simoni MG, Perego C, Ravizza T, Moneta D, Conti M, Marchesi F, De Luigi A, Garattini S and Vezzani A (2000) Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic Status epilepticus. Eur. J. Neurosci. 12: 2623-2633
51. Justicia C, Gabriel C and Planes AM (2000) Activation of the JAK/STAT pathway following transient focal cerebral ischemia: signaling through Jak1 and Stat3 in astrocytes. Glia 30: 253-270
52. Liu H, Perlman H, Pagliari LJ and Pope RM (2001) Constitutively activated Akt1 is vital for the survival of human monocyte-differentiated macrophages Role of Mcl-1, independent of nuclear factor (NF)-kappaB, Bad, or caspase activation. J. Exp. Med. 194: 113-126
53. Clark RS, Kochanek PM, Watkins SC, Chen M, Dixon CE, Seidberg NA, Melick J, Loeffert JE, Nathaniel PD, Jin KL and Graham SH (2000) Caspase-3 mediated neuronal death after traumatic brain injury in rats. J. Neurochem. 74: 740-753
54. Didier M, Bursztajn S, Adamec E, Passani L, Nixon RA, Coyle JT, Wei JY and Berman SA (1996) DNA strand breaks induced by sustained glutamate excitotoxicity in primary neuronal cultures. J. Neurosci. 16: 2238-2250
55. Liang P, Zhu W, Zhang X, Guoo Z, O'Connell RP, Averboukh L, Wang F and Pardee AB (1994) Differential display using one-base anchored oligo-dT primers. Nucleic Acids Res. 22: 5763-5764
56. Burgess DL, Biddlecome GH, McDonough SI, Diaz ME, Zilinski CA, Bean BP, Campbell KP and Noebels JL (1999) beta subunit reshuffling modifies N- and P/Q-type Ca2+ channel subunit compositions in lethargic mouse brain. Mol. Cell Neurosci. 13: 293-311