Calcineurin mediates acetylcholinesterase expression during calcium ionophore A23187-induced HeLa cell apoptosis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1773, Issue 4, 2007, Pages 593-602

  Zhu, Hui ^a   Gao, Wei ^a   Jiang, Hua ^a   Wu, Jun ^a   Shi, Yu fang ^b   Zhang, Xue Jun ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b University of Medicine and Dentistry   (United States)

Author keywords

Acetylcholinesterase; Apoptosis; Calcineurin; Calpain; NFAT

Indexed keywords

ACETYLCHOLINESTERASE; CALCIMYCIN; CALCINEURIN; CALPAIN; CALPEPTIN; CYCLOSPORIN A; MESSENGER RNA; NUCLEAR FACTOR OF ACTIVATED T CELL 3; NUCLEAR FACTOR OF ACTIVATED T CELL 4; TACROLIMUS; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION;

ACETYLCHOLINESTERASE; APOPTOSIS; CALCIMYCIN; CALCINEURIN; CALCIUM; CALPAIN; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITORS; HELA CELLS; HUMANS; IONOPHORES; NFATC TRANSCRIPTION FACTORS; PROMOTER REGIONS (GENETICS); PROTEIN TRANSPORT;

EID: 33947408116     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2007.01.008     Document Type: Article

References (59)

1. Taylor P., and Radic Z. The cholinesterases: from genes to proteins. Annu. Rev. Pharmacol. Toxicol. 34 (1994) 281-320
2. Soreq H., and Seidman S. Acetylcholinesterase-New roles for an old actor. Nat. Rev., Neurosci. 2 (2001) 294-302
3. Small D.H., Michaelson S., and Sberna G. Non-classical actions of cholinesterases: role in cellular differentiation, tumorigenesis and Alzheimer's disease. Neurochem. Int. 28 (1996) 453-483
4. Tung E.K., Choi R.C., Siow N.L., Jiang J.X., Ling K.K., Simon J., Barnard E.A., and Tsim K.W. P2Y2 receptor activation regulates the expression of acetylcholinesterase and acetylcholine receptor genes at vertebrate neuromuscular junctions. Mol. Pharmacol. 66 (2004) 794-806
5. Angus L.M., Chan R.Y., and Jasmin B.J. Role of intronic E- and N-box motifs in the transcriptional induction of the acetylcholinesterase gene during myogenic differentiation. J. Biol. Chem. 276 (2001) 17603-17609
6. Luo Z., Fuentes M.E., and Taylor P. Regulation of acetylcholinesterase mRNA stability by calcium during differentiation from myoblasts to myotubes. J. Biol. Chem. 269 (1994) 27216-27223
7. Stephenson J., Czepulkowski B., Hirst W., and Mufti G.J. Deletion of the acetylcholinesterase locus at 7q22 associated with myelodysplastic syndromes (MDS) and acute myeloid leukaemia (AML). Leuk. Res. 20 (1996) 235-241
8. Zhang X.J., Yang L., Zhao Q., Caen J.P., He H.Y., Jin Q.H., Guo L.H., Alemany M., Zhang L.Y., and Shi Y.F. Induction of acetylcholinesterase expression during apoptosis in various cell types. Cell Death Differ. 9 (2002) 790-800
9. Zhu H., Gao W., Jiang H., Jin Q.H., Shi Y.F., Tsim K.W., and Zhang X.J. Regulation of acetylcholinesterase expression by calcium signaling during calcium ionophore A23187- and thapsigargin-induced apoptosis. Int. J. Biochem. Cell. Biol. 39 (2007) 93-108
10. Orrenius S., Zhivotovsky B., and Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat. Rev., Mol Cell Biol. 4 (2003) 552-565
11. Kim M.J., Jo D.G., Hong G.S., Kim B.J., Lai M., Cho D.H., Kim K.W., Bandyopadhyay A., Hong Y.M., Kim do H., Cho C., Liu J.O., Snyder S.H., and Jung Y.K. Calpain-dependent cleavage of cain/cabin1 activates calcineurin to mediate calcium-triggered cell death. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 9870-9875
12. Ishihara I., Minami Y., Nishizaki T., Matsuoka T., and Yamamura H. Activation of calpain precedes morphological alterations during hydrogen peroxide-induced apoptosis in neuronally differentiated mouse embryonal carcinoma P19 cell line. Neurosci. Lett. 279 (2000) 97-100
13. Nakagawa T., and Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150 (2000) 887-894
14. Kusakawa G., Saito T., Onuki R., Ishiguro K., Kishimoto T., and Hisanaga S. Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J. Biol. Chem. 275 (2000) 17166-17172
15. Goll D.E., Thompson V.F., Li H., Wei W., and Cong J. The calpain system. Physiol. Rev. 83 (2003) 731-801
16. Klee C.B., Crouch T.H., and Krinks M.H. Calcineurin: a calcium- and calmodulin-binding protein of the nervous system. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 6270-6273
17. Wu H.Y., Tomizawa K., Oda Y., Wei F.Y., Lu Y.F., Matsushita M., Li S.T., Moriwaki A., and Matsui H. Critical role of calpain-mediated cleavage of calcineurin in excitotoxic neurodegeneration. J. Biol. Chem. 279 (2004) 4929-4940
18. Lakshmikuttyamma A., Selvakumar P., Sharma A.R., Anderson D.H., and Sharma R.K. In vitro proteolytic degradation of bovine brain calcineurin by m-calpain. Neurochem. Res. 29 (2004) 1913-1921
19. Wang K.K., Roufogalis B.D., and Villalobo A. Characterization of the fragmented forms of calcineurin produced by calpain I. Biochem. Cell. Biol. 67 (1989) 703-711
20. Cohen P. The structure and regulation of protein phosphatases. Annu. Rev. Biochem. 58 (1989) 453-508
21. Shou Y., Li L., Prabhakaran K., Borowitz J.L., and Isom G.E. Calcineurin-mediated Bad translocation regulates cyanide-induced neuronal apoptosis. Biochem. J. 379 (2004) 805-813
22. Berthier A., Lemaire-Ewing S., Prunet C., Monier S., Athias A., Bessede G., Pais de Barros J.P., Laubriet A., Gambert P., Lizard G., and Neel D. Involvement of a calcium-dependent dephosphorylation of BAD associated with the localization of Trpc-1 within lipid rafts in 7-ketocholesterol-induced THP-1 cell apoptosis. Cell Death Differ. 11 (2004) 897-905
23. Agostinho P., and Oliveira C.R. Involvement of calcineurin in the neurotoxic effects induced by amyloid-beta and prion peptides. Eur. J. Neurosci. 17 (2003) 1189-1196
24. Wang H.G., Pathan N., Ethell I.M., Krajewski S., Yamaguchi Y., Shibasaki F., McKeon F., Bobo T., Franke T.F., and Reed J.C. Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284 (1999) 339-343
25. Asai A., Qiu J., Narita Y., Chi S., Saito N., Shinoura N., Hamada H., Kuchino Y., and Kirino T. High level calcineurin activity predisposes neuronal cells to apoptosis. J. Biol. Chem. 274 (1999) 34450-34458
26. Luo Z.D., Wang Y., Werlen G., Camp S., Chien K.R., and Taylor P. Calcineurin enhances acetylcholinesterase mRNA stability during C2-C12 muscle cell differentiation. Mol. Pharmacol. 56 (1999) 886-894
27. Rao A., Luo C., and Hogan P.G. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15 (1997) 707-747
28. Hogan P.G., Chen L., Nardone J., and Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17 (2003) 2205-2232
29. Timmerman L.A., Clipstone N.A., Ho S.N., Northrop J.P., and Crabtree G.R. Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature 383 (1996) 837-840
30. Shibasaki F., Price E.R., Milan D., and McKeon F. Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382 (1996) 370-373
31. Crabtree G.R., and Olson E.N. NFAT signaling: choreographing the social lives of cells. Cell 109 (2002) S67-S79 (Suppl.)
32. Cohen T.V., and Randall W.R. NFATc1 activates the acetylcholinesterase promoter in rat muscle. J. Neurochem. 90 (2004) 1059-1067
33. Ben Aziz-Aloya R., Seidman S., Timberg R., Sternfeld M., Zakut H., and Soreq H. Expression of a human acetylcholinesterase promoter-reporter construct in developing neuromuscular junctions of Xenopus embryos. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 2471-2475
34. Wan D.C., Choi R.C., Siow N.L., and Tsim K.W. The promoter of human acetylcholinesterase is activated by a cyclic adenosine 3′,5′-monophosphate-dependent pathway in cultured NG108-15 neuroblastoma cells. Neurosci. Lett. 288 (2000) 81-85
35. Ray S.K., Fidan M., Nowak M.W., Wilford G.G., Hogan E.L., and Banik N.L. Oxidative stress and Ca2+ influx upregulate calpain and induce apoptosis in PC12 cells. Brain Res. 852 (2000) 326-334
36. Michetti M., Salamino F., Tedesco I., Averna M., Minafra R., Melloni E., and Pontremoli S. Autolysis of human erythrocyte calpain produces two active enzyme forms with different cell localization. FEBS Lett. 392 (1996) 11-15
37. Shibasaki F., and McKeon F. Calcineurin functions in Ca(2+)-activated cell death in mammalian cells. J. Cell Biol. 131 (1995) 735-743
38. Yang T.T., and Chow C.W. Transcription cooperation by NFAT. C/EBP composite enhancer complex. J. Biol. Chem. 278 (2003) 15874-15885
39. Chow C.W., Rincon M., and Davis R.J. Requirement for transcription factor NFAT in interleukin-2 expression. Mol. Cell. Biol. 19 (1999) 2300-2307
40. Yang T.T., Xiong Q., Enslen H., Davis R.J., and Chow C.W. Phosphorylation of NFATc4 by p38 mitogen-activated protein kinases. Mol. Cell. Biol. 22 (2002) 3892-3904
41. Park S.E., Kim N.D., and Yoo Y.H. Acetylcholinesterase plays a pivotal role in apoptosome formation. Cancer Res. 64 (2004) 2652-2655
42. Fadeel B., Orrenius S., and Zhivotovsky B. Apoptosis in human disease: a new skin for the old ceremony?. Biochem. Biophys. Res. Commun. 266 (1999) 699-717
43. Mandic A., Viktorsson K., Strandberg L., Heiden T., Hansson J., Linder S., and Shoshan M.C. Calpain-mediated Bid cleavage and calpain-independent Bak modulation: two separate pathways in cisplatin-induced apoptosis. Mol. Cell. Biol. 22 (2002) 3003-3013
44. Choi W.S., Lee E.H., Chung C.W., Jung Y.K., Jin B.K., Kim S.U., Oh T.H., Saido T.C., and Oh Y.J. Cleavage of Bax is mediated by caspase-dependent or-independent calpain activation in dopaminergic neuronal cells: protective role of Bcl-2. J. Neurochem. 77 (2001) 1531-1541
45. Groenendyk J., Lynch J., and Michalak M. Calreticulin, Ca2+, and calcineurin-signaling from the endoplasmic reticulum. Mol. Cells 17 (2004) 383-389
46. Tantral L., Malathi K., Kohyama S., Silane M., Berenstein A., and Jayaraman T. Intracellular calcium release is required for caspase-3 and-9 activation. Cell Biochem. Funct. 22 (2004) 35-40
47. Li C., Fox C.J., Master S.R., Bindokas V.P., Chodosh L.A., and Thompson C.B. Bcl-X(L) affects Ca(2+) homeostasis by altering expression of inositol 1,4,5-trisphosphate receptors. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 9830-9835
48. Aramburu J., Heitman J., and Crabtree G.R. Calcineurin: a central controller of signalling in eukaryotes. EMBO Rep. 5 (2004) 343-348
49. Bittinger M.A., McWhinnie E., Meltzer J., Iourgenko V., Latario B., Liu X., Chen C.H., Song C., Garza D., and Labow M. Activation of cAMP response element-mediated gene expression by regulated nuclear transport of TORC proteins. Curr. Biol. 14 (2004) 2156-2161
50. Gomez del Arco P., Martinez-Martinez S., Maldonado J.L., Ortega-Perez I., and Redondo J.M. A role for the p38 MAP kinase pathway in the nuclear shuttling of NFATp. J. Biol. Chem. 275 (2000) 13872-13878
51. Su J.H., Deng G., and Cotman C.W. Bax protein expression is increased in Alzheimer's brain: correlations with DNA damage, Bcl-2 expression, and brain pathology. J. Neuropathol. Exp. Neurol. 56 (1997) 86-93
52. Li W.P., Chan W.Y., Lai H.W., and Yew D.T. Terminal dUTP nick end labeling (TUNEL) positive cells in the different regions of the brain in normal aging and Alzheimer patients. J. Mol. Neurosci. 8 (1997) 75-82
53. LaFerla F.M. Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nat. Rev., Neurosci. 3 (2002) 862-872
54. Hata R., Masumura M., Akatsu H., Li F., Fujita H., Nagai Y., Yamamoto T., Okada H., Kosaka K., Sakanaka M., and Sawada T. Up-regulation of calcineurin Abeta mRNA in the Alzheimer's disease brain: assessment by cDNA microarray. Biochem. Biophys. Res. Commun. 284 (2001) 310-316
55. Veeranna, Kaji T., Boland B., Odrljin T., Mohan P., Basavarajappa B.S., Peterhoff C., Cataldo A., Rudnicki A., Amin N., Li B.S., Pant H.C., Hungund B.L., Arancio O., and Nixon R.A. Calpain mediates calcium-induced activation of the erk1,2 MAPK pathway and cytoskeletal phosphorylation in neurons: relevance to Alzheimer's disease. Am. J. Pathol. 165 (2004) 795-805
56. Saito K., Elce J.S., Hamos J.E., and Nixon R.A. Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 2628-2632
57. Liu F., Grundke-Iqbal I., Iqbal K., Oda Y., Tomizawa K., and Gong C.X. Truncation and activation of calcineurin A by calpain I in Alzheimer disease brain. J. Biol. Chem. 280 (2005) 37755-37762
58. Moran M.A., Mufson E.J., and Gomez-Ramos P. Colocalization of cholinesterases with beta amyloid protein in aged and Alzheimer's brains. Acta Neuropathol. (Berl.) 85 (1993) 362-369
59. Ulrich J., Meier-Ruge W., Probst A., Meier E., and Ipsen S. Senile plaques: staining for acetylcholinesterase and A4 protein: a comparative study in the hippocampus and entorhinal cortex. Acta Neuropathol. (Berl.) 80 (1990) 624-628