Gliotoxin induces caspase-dependent neurite degeneration and calpain-mediated general cytotoxicity in differentiated human neuroblastoma SH-SY5Y cells

Biochemical and Biophysical Research Communications

Volumn 345, Issue 3, 2006, Pages 1068-1074

  Axelsson, V ^a   Holback, S ^a   Sjogren M ^a   Gustafsson, H ^a   Forsby, A ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Calpain; Caspase; Cytotoxicity; Gliotoxin; Mycotoxin; Neurite degeneration; SH SY5Y cells

Indexed keywords

BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CALCIUM; CALPAIN; CALPEPTIN; CASPASE; CASPASE INHIBITOR; CELL PROTEIN; FODRIN; GLIOTOXIN; PROTEINASE;

ARTICLE; ATTENUATION; CALCIUM CELL LEVEL; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG INHIBITION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; NERVE CELL DEGENERATION; NEURITE; NEUROBLASTOMA CELL; PRIORITY JOURNAL; WESTERN BLOTTING;

AMINO ACID CHLOROMETHYL KETONES; CALCIUM; CALPAIN; CASPASES; CELL DIFFERENTIATION; CELL LINE, TUMOR; ENZYME INHIBITORS; GLIOTOXIN; HUMANS; IMMUNOSUPPRESSIVE AGENTS; NEURITES; NEUROBLASTOMA; SPECTRIN;

EID: 33646848562     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.05.019     Document Type: Article

References (50)

1. Richard J.L., Debey M.C., Chermette R., Pier A.C., Hasegawa A., Lund A., Bratberg A.M., Padhye A.A., and Connole M.D. Advances in veterinary mycology. J. Med. Vet. Mycol. 32 Suppl. 1 (1994) 169-187
2. Scudamore K.A., and Livesey C.Y. Occurence and significance of mycotoxins in forage crops and silage: a review. J. Sci. Food Agric. 77 (1998) 1-17
3. Waring P., Eichner R.D., Müllbacher A., and Sjaarda A. Gliotoxin induces apoptosis in macrophages unrelated to its antiphagocytic properties. J. Biol. Chem. 263 (1988) 18493-18499
4. Sutton P., Newcombe N.R., Waring P., and Müllbacher A. In vivo immunosuppressive activity of gliotoxin, a metabolite produced by human pathogenic fungi. Infect. Immun. 62 (1994) 1192-1198
5. Waring P., and Beaver J. Gliotoxin and related epipolythiodioxopiperazines. Gen. Pharmacol. 27 (1996) 1311-1316
6. Richard J.L., Dvorak T.J., and Ross P.F. Natural occurrence of gliotoxin in turkeys infected with Aspergillus fumigatus, Fresenius. Mycopathologia 134 (1996) 167-170
7. Bauer J., Gareis M., Bott A., and Gedek B. Isolation of a mycotoxin (gliotoxin) from a bovine udder infected with Aspergillus fumigatus. J. Med. Vet. Mycol. 27 (1989) 45-50
8. Wenehed V., Solyakov A., Thylin I., Häggblom P., and Forsby A. Cytotoxic response of Aspergillus fumigatus-produced mycotoxins on growth medium, maize and commercial animal feed substrates. Food Chem. Toxicol. 41 (2003) 395-403
9. Axelsson V., Pikkarainen K., and Forsby A. Glutathione intensifies gliotoxin-induced cytotoxicity in human neuroblastoma SH-SY5Y cells. Cell Biol. Toxicol. 22 (2006) 127-136
10. LoPachin Jr. R.M., and Lehning E.J. Acrylamide-induced distal axon degeneration: a proposed mechanism of action. Neurotoxicology 15 (1994) 247-260
11. Nordin-Andersson M., Walum E., Kjellstrand P., and Forsby A. Acrylamide-induced effects on general and neurospecific cellular functions during exposure and recovery. Cell Biol. Toxicol. 19 (2003) 43-51
12. 2+ release from intact rat liver mitochondria. Biochemistry 33 (1994) 13401-13405
13. Green D., Pace S.M., Hurne A.M., Waring P., Hart J.D., and Dulhunty A.F. Skeletal muscle ryanodine receptor channels are activated by the fungal metabolite, gliotoxin. J. Membr. Biol. 175 (2000) 223-233
14. Hurne A.M., Chai C.L., Moerman K., and Waring P. Influx of calcium through a redox-sensitive plasma membrane channel in thymocytes causes early necrotic cell death induced by the epipolythiodioxopiperazine toxins. J. Biol. Chem. 277 (2002) 31631-31638
15. Grynspan F., Griffin W.B., Mohan P.S., Shea T.B., and Nixon R.A. Calpains and calpastatin in SH-SY5Y neuroblastoma cells during retinoic acid-induced differentiation and neurite outgrowth: comparison with the human brain calpain system. J. Neurosci. Res. 48 (1997) 181-191
16. Murray S.S., Grisanti M.S., Bentley G.V., Kahn A.J., Urist M.R., and Brochmann Murray E.J. The calpain-calpastatin system and cellular proliferation and differentiation in rodent osteoblastic cells. Exp. Cell Res. 233 (1997) 297-309
17. Goll D.E., Thompson V.F., Li H., Wei W., and Cong J. The calpain system. Physiol. Rev. 83 (2003) 731-801
18. Carafoli E., and Molinari M. Calpain: a protease in search of a function?. Biochem. Biophys. Res. Commun. 247 (1998) 193-203
19. Chan S.L., and Mattson M.P. Caspase and calpain substrates: roles in synaptic plasticity and cell death. J. Neurosci. Res. 58 (1999) 167-190
20. Bizat N., Hermel J.M., Humbert S., Jacquard C., Creminon C., Escartin C., Saudou F., Krajewski S., Hantraye P., and Brouillet E. In vivo calpain/caspase cross-talk during 3-nitropropionic acid-induced striatal degeneration: implication of a calpain-mediated cleavage of active caspase-3. J. Biol. Chem. 278 (2003) 43245-43253
21. Blomgren K., Zhu C., Wang X., Karlsson J.O., Leverin A.L., Bahr B.A., Mallard C., and Hagberg H. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis"?. J. Biol. Chem. 276 (2001) 10191-10198
22. Biedler J.L., Helson L., and Spengler B.A. Morphology and growth, tumorigenicity, and cytogenetics of human neuroblastoma cells in continuous culture. Cancer Res. 33 (1973) 2643-2652
23. Bottenstein J.E., and Sato G.H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. USA 76 (1979) 514-517
24. Påhlman S., Ruusala A.I., Abrahamsson L., Mattsson M.E., and Esscher T. Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation. Cell Differ. 14 (1984) 135-144
25. Banik N.L., Matzelle D., Gantt-Wilford G., and Hogan E.L. Role of calpain and its inhibitors in tissue degeneration and neuroprotection in spinal cord injury. Ann. NY Acad. Sci. 825 (1997) 120-127
26. Forsby A., Pilli F., Bianchi V., and Walum E. Determination of critical cellular neurotoxic concentrations in human neuroblastoma (SH-SY5Y) cell cultures. Altern. Lab. Anim. 23 (1995) 800-811
27. 2+ and inositol 1,4,5-trisphosphate mass in a human neuroblastoma cell line, SH-SY5Y. Biochem. J. 265 (1990) 555-562
28. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
29. Nordin-Andersson M., Forsby A., Heldring N., DeJongh J., Kjellstrand P., and Walum E. Neurite degeneration in differentiated human neuroblastoma cells. Toxicol. In Vitro 12 (1998) 557-560
30. Ciccarone V., Spengler B.A., Meyers M.B., Biedler J.L., and Ross R.A. Phenotypic diversification in human neuroblastoma cells: expression of distinct neural crest lineages. Cancer Res. 49 (1989) 219-225
31. McGinnis K.M., Wang K.K., and Gnegy M.E. Alterations of extracellular calcium elicit selective modes of cell death and protease activation in SH-SY5Y human neuroblastoma cells. J. Neurochem. 72 (1999) 1853-1863
32. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
33. Zhou X., Zhao A., Goping G., and Hirszel P. Gliotoxin-induced cytotoxicity proceeds via apoptosis and is mediated by caspases and reactive oxygen species in LLC-PK1 cells. Toxicol. Sci. 54 (2000) 194-202
34. Suen Y.K., Fung K.P., Lee C.Y., and Kong S.K. Gliotoxin induces apoptosis in cultured macrophages via production of reactive oxygen species and cytochrome c release without mitochondrial depolarization. Free Radic. Res. 35 (2001) 1-10
35. Kweon Y.-O., Paik Y.-H., Schnabl B., Qian T., Lemasters J.J., and Brenner D.A. Gliotoxin-mediated apoptosis of activated human hepatic stellate cells. J. Hepatol. 39 (2003) 38-46
36. Müllbacher A., Waring P., Tiwari-Palni U., and Eichner R.D. Structural relationship of epipolythiodioxopiperazines and their immunomodulating activity. Mol. Immunol. 23 (1986) 231-235
37. Kampfl A., Posmantur R., Nixon R., Grynspan F., Zhao X., Liu S.J., Newcomb J.K., Clifton G.L., and Hayes R.L. μ-calpain activation and calpain-mediated cytoskeletal proteolysis following traumatic brain injury. J. Neurochem. 67 (1996) 1575-1583
38. Posmantur R., Kampfl A., Siman R., Liu S.J., Zhao X., Clifton G.L., and Hayes R.L. A calpain inhibitor attenuates cortical cytoskeletal protein loss after experimental traumatic brain injury in the rat. Neuroscience 77 (1997) 875-888
39. Rami A., Ferger D., and Krieglstein J. Blockade of calpain proteolytic activity rescues neurons from glutamate excitotoxicity. Neurosci. Res. 27 (1997) 93-97
40. Crocker S.J., Smith P.D., Jackson-Lewis V., Lamba W.R., Hayley S.P., Grimm E., Callaghan S.M., Slack R.S., Melloni E., Przedborski S., Robertson G.S., Anisman H., Merali Z., and Park D.S. Inhibition of calpains prevents neuronal and behavioral deficits in an MPTP mouse model of Parkinson's disease. J. Neurosci. 23 (2003) 4081-4091
41. Lee M.S., Kwon Y.T., Li M., Peng J., Friedlander R.M., and Tsai L.H. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405 (2000) 360-364
42. Wang M.S., Davis A.A., Culver D.G., Wang Q., Powers J.C., and Glass J.D. Calpain inhibition protects against Taxol-induced sensory neuropathy. Brain 127 (2004) 671-679
43. Schumacher P.A., Siman R.G., and Fehlings M.G. Pretreatment with calpain inhibitor CEP-4143 inhibits calpain I activation and cytoskeletal degradation, improves neurological function, and enhances axonal survival after traumatic spinal cord injury. J. Neurochem. 74 (2000) 1646-1655
44. Wang K.K., Posmantur R., Nath R., McGinnis K., Whitton M., Talanian R.V., Glantz S.B., and Morrow J.S. Simultaneous degradation of alphaII- and betaII-spectrin by caspase 3 (CPP32) in apoptotic cells. J. Biol. Chem. 273 (1998) 22490-22497
45. Rotter B., Kroviarski Y., Nicolas G., Dhermy D., and Lecomte M.C. AlphaII-spectrin is an in vitro target for caspase-2, and its cleavage is regulated by calmodulin binding. Biochem. J. 378 (2004) 161-168
46. Ivins K.J., Bui E.T., and Cotman C.W. Beta-amyloid induces local neurite degeneration in cultured hippocampal neurons: evidence for neuritic apoptosis. Neurobiol. Dis. 5 (1998) 365-378
47. Chung C.W., Song Y.H., Kim I.K., Yoon W.J., Ryu B.R., Jo D.G., Woo H.N., Kwon Y.K., Kim H.H., Gwag B.J., Mook-Jung I.H., and Jung Y.K. Proapoptotic effects of tau cleavage product generated by caspase-3. Neurobiol. Dis. 8 (2001) 162-172
48. Guo H., Albrecht S., Bourdeau M., Petzke T., Bergeron C., and LeBlanc A.C. Active caspase-6 and caspase-6-cleaved tau in neuropil threads, neuritic plaques, and neurofibrillary tangles of Alzheimer's disease. Am. J. Pathol. 165 (2004) 523-531
49. Land C.J., Hult K., Fuchs R., Hagelberg S., and Lundstrom H. Tremorgenic mycotoxins from Aspergillus fumigatus as a possible occupational health problem in sawmills. Appl. Environ. Microbiol. 53 (1987) 787-790
50. Gordon K.E., Masotti R.E., and Waddell W.R. Tremorgenic encephalopathy: a role of mycotoxins in the production of CNS disease in humans?. Can. J. Neurol. Sci. 20 (1993) 237-239