Mechanism of apoptosis with the involvement of calpain and caspase cascades in human malignant neuroblastoma SH-SY5Y cells exposed to flavonoids

International Journal of Cancer

Volumn 119, Issue 11, 2006, Pages 2575-2585

  Das, Arabinda ^a   Banik, Naren L ^a   Ray, Swapan K ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Apoptosis; Calpain; Caspase; Flavonoids; Neuroblastoma

Indexed keywords

APIGENIN; CALCIUM; CALPAIN; CALPEPTIN; CASPASE; CASPASE 12; CASPASE 3; CASPASE 3 INHIBITOR; CASPASE 8; CASPASE 8 INHIBITOR; CASPASE 9; CASPASE 9 INHIBITOR; CYTOCHROME C; DEOXYRIBONUCLEASE; EPIGALLOCATECHIN; EPIGALLOCATECHIN GALLATE; FLAVONOID; GENISTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEINASE;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; NEUROBLASTOMA; PRIORITY JOURNAL; PROTEIN DEGRADATION;

APOPTOSIS; CALPAIN; CASPASES; CELL LINE, TUMOR; COLORIMETRY; FLAVONOIDS; HUMANS; NEUROBLASTOMA;

EID: 33750612111     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22228     Document Type: Article

References (70)

1. Brodeur GM. Meeting summary for advances in neuroblastoma research-2000. Med Pediatr Oncol 2000;35:727-8.
2. Kuroda Y, Hara Y. Anti-mutagenic and anti-carcinogenic activity of tea polyphenols. Mutat Res 1999;436:69-97.
3. Prasad KN, Cole WC, Hovland AR, Prasad KC, Nahreini P, Kumar B, Edwards-Prasad J, Andreatta CP. Multiple antioxidants in the prevention and treatment of neurodegenerative disease: analysis of biologic rationale. Curr Opin Neurol 1999;12:761-70.
4. Prasad KN, Kumar B, Yan XD, Hanson AJ, Cole WC. α-tocopheryl succinate, the most effective form of vitamin E, for adjuvant cancer treatment: a review. J Am Coll Nutr 2003;22:108-17.
5. Cohrs RJ, Torelli S, Prasad KN, Edwards-Prasad J, Sharma OK. Effect of vitamin E succinate and a cAMP-stimulating agent on the expression of c-myc and N-myc and H-ras in murine neuroblastoma cells. Int J Dev Neurosci 1991;9:187-94.
6. Cole WC, Prasad KN. Contrasting effects of vitamins as modulators of apoptosis in cancer cells and normal cells: a review. Nutr Cancer 1997;29:97-103.
7. Gunawardena K, Murray DK, Meikle AW. Testosterone is a potential augmentor of antioxidant-induced apoptosis in human prostate cancer cells. Cancer Detect Prev 2002;26:105-13.
8. McKinney M, Pfenning M, Richelson E. Effect of the anti-tumor drug caracemide on the neurochemistry of murine neuroblastoma cells (clone N1E-115). Biochem Pharmacol 1986;35:2615-22.
9. Nargi JL, Ratan RR, Griffin DE. p53-independent inhibition of proliferation and p21 (WAF1/Cip1)-modulated induction of cell death by the antioxidants N-acetylcysteine and vitamin E. Neoplasia 1999;1:544-56.
10. Kumar B, Jha MN, Cole WC, Bedford JS, Prasad KN. D-α-tocopheryl succinate (vitamin E) enhances radiation-induced chromosomal damage levels in human cancer cells, but reduces it in normal cells. J Am Coll Nutr 2002;21:339-43.
11. Formica JV, Regelson W. Review of the biology of quercetin and related bioflavonoids. Food Chem Toxicol 1995;33:1061-80.
12. Ahmad N, Feyes DK, Nieminen AL, Agarwal R, Mukhtar H. Green tea constituent epigallocatechin-3-gallate and induction of apoptosis and cell cycle arrest in human carcinoma cells. J Natl Cancer Inst 1997;89:1881-6.
13. Gupta S, Afaq F, Mukhtar H. Involvement of nuclear factor κ B, Bax and Bcl-2 in induction of cell cycle arrest and apoptosis by apigenin in human prostate carcinoma cells. Oncogene 2002;21:3727-38.
14. Gupta S, Hussain T, Mukhtar H. Molecular pathway for (-)- epigallocatechin-3-gallate-induced cell cycle arrest and apoptosis of human prostate carcinoma cells. Arch Biochem Biophys 2003;410:177-85.
15. Hayakawa S, Saeki K, Sazuka M, Suzuki Y, Shoji Y, Ohta T, Kaji K, Yuo A, Isemura M. Apoptosis induction by epigallocatechin gallate involves its binding to Fas. Biochem Biophys Res Commun 2001;285:1102-6.
16. Saeki K, Kobayashi N, Inazawa Y, Zhang H, Nishitoh H, Ichijo H, Isemura M, Yuo A. Oxidation-triggered c-Jun N-terminal kinase (JNK) and p38 mitogen-activated protein (MAP) kinase pathways for apoptosis in human leukaemic cells stimulated by epigallocatechin-3-gallate (EGCG): a distinct pathway from those of chemically induced and receptor-mediated apoptosis. Biochem J 2002;368.705-20.
17. Paillart C, Carlier E, Guedin D, Dargent B, Couraud F. Direct block of voltage-sensitive sodium channels by genistein, a tyrosine kinase inhibitor. J Pharmacol Exp Ther 1997;280:521-6.
18. Brown A, Jolly P, Wei H. Genistein modulates neuroblastoma cell proliferation and differentiation through induction of apoptosis and regulation of tyrosine kinase activity and N-myc expression. Carcinogenesis 1998;19:991-7.
19. Suzuki K, Koike H, Matsui H, Ono Y, Hasumi M, Nakazato H, Okugi H, Sekine Y, Oki K, Ito K, Yamamoto T, Fukabori Y, et al. Genistein, a soy isoflavone, induces glutathione peroxidase in the human prostate cancer cell lines LNCaP and PC-3. Int J Cancer 2002;9:846-52.
20. Constantinou A, Huberman E. Genistein as an inducer of tumor cell differentiation: possible mechanisms of action. Proc Soc Exp Biol Med 1995;208:109-15.
21. Srinivasan A, Li F, Wong A, Kodandapani L, Smidt R, Jr, Krebs JF, Fritz LC, Wu JC, Tomaselli KJ. Bcl-xL functions downstream of caspase-8 to inhibit Fas- and tumor necrosis factor receptor 1-induced apoptosis of MCF-7 breast carcinoma cells. J Biol Chem 1998;273:4523-9.
22. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998;281:1309-12.
23. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med 2000;6:513-19.
24. Martin AG, Nguyen J, Wells JA, Fearnhead HO. Apo cytochrome c inhibits caspases by preventing apoptosome formation. Biochem Biophys Res Commun 2004;319:944-50.
25. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl-2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998;94:481-90.
26. Daniel PT, Schulze-Osthoff K, Belka C, Güner D. Guardians of cell death: the Bcl-2 family proteins. Essays Biochem 2003;39:73-88.
27. Eskes R, Desagher S, Antonsson B, Martinou JC. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 2000;20:929-35.
28. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature 2000;403:98-103.
29. Nakagawa T, Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 2000;150:887-94.
30. Suzuki K. Calcium-activated neutral protease and its endogenous inhibitor. Activation at the cell membrane and biological function. FEBS Lett 1987;220:271-7.
31. Liu X, Li P, Widlak P, Zou H, Luo X, Garrard WT, Wang X. The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis. Proc Natl Acad Sci USA 1998;95:8461-6.
32. Sakahira H, Enari M, Nagata S. Functional differences of two forms of the inhibitor of caspase-activated DNase, ICAD-L, and ICAD-S. J Biol Chem 1999;274:15740-4.
33. Biedler JL, Helson L, Spengler BA. Morphology, growth, tumorigenicity and cytogenetics of human neuroblastoma cells in continuous culture. Cancer Res 1973;33:2643-9.
34. Martin H, Lambert MP, Barber K, Hinton S, Klein WL. Alzheimer's- associated phospho-tau epitope in human neuroblastoma cell cultures: upregulation by fibronectin and laminin. Neuroscience 1995;66:769-79.
35. Ward RV, Davis JB, Gray CW, Barton AJ, Bresciani LG, Caivano M, Murphy VF, Duff K, Hutton M, Hardy J, Roberts GW, Karran EH. Presenilin-1 is processed into two major cleavage products in neuronal cell lines. Neurodegeneration 1996;5:293-8.
36. Das A, Sribnick EA, Wingrave JM, Del Re AM, Woodward JJ, Appel SH, Banik NL, Ray SK. Calpain activation in apoptosis of ventral spinal cord 4.1 (VSC4.1) motoneurons exposed to glutamate: calpain inhibition provides functional neuroprotection. J Neurosci Res 2005;81:551-62.
37. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985;260:3440-50.
38. Hansen CA, Monck JR, Williamson JR. Measurement of intracellular free calcium to investigate receptor-mediated calcium signaling. Methods Enzymol 1990;191:691-706.
39. Nudson WA, Rovnak J, Buechner M, Quackenbush SL. Walleye dermal sarcoma virus Orf C is targeted to the mitochondria. J Gen Virol 2003;84:375-81.
40. Pique M, Barragan M, Dalmau M, Bellosillo B, Pons G, Gil J. Aspirin induces apoptosis through mitochondrial cytochrome c release. FEBS Lett 2000;480:193-6.
41. Kang D, Nishida J, Iyama A, Nakabeppu Y, Furuichi M, Fujiwara T, Sekiguchi M, Takeshige K. Intracellular localization of 8-oxo-dGTPase in human cells, with special reference to the role of the enzyme in mitochondria. J Biol Chem 1995;270:14659-65.
42. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, Maundrell K, Antonsson B, Martinou JC. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 1999;144:891-901.
43. Nath R, Raser KJ, Stafford D, Hajimohammadreza I, Posner A, Allen H, Talanian RV, Yuen P, Gilbertsen RB, Wang KK. Non-erythroid aspectrin breakdown by calpain and interleukin-1β-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem J 1996;319:683-90.
44. Wang KK, Posmantur R, Nath R, McGinnis K, Whitton M, Talanian RV, Glantz SB, Morrowl JS. Simultaneous degradation of all- and βII-spectrin by caspase 3 (CPP32) in apoptotic cells. J Biol Chem 1998;273:22490-7.
45. Tan X, Hu D, Li S, Han Y, Zhang Y, Zhou D. Differences of four catechins in cell cycle arrest and induction of apoptosis in LoVo cells. Cancer Lett 2000;158:1-6.
46. Saeki K, Sano M, Miyase T, Nakamura Y, Hara Y, Aoyagi Y, Isemura M. Apoptosis-inducing activity of polyphenol compounds derived from tea catechins in human histiolytic lymphoma U937 cells. Biosci Biotechnol Biochem 1999;63:585-7.
47. Islam S, Islam N, Kermode T, Johnstone B, Mukhtar H, Moskowitz RW, Goldberg VM, Malemud CJ, Haqqi TM. Involvement of caspase-3 in epigallocatechin-3-gallate-mediated apoptosis of human chondrosarcoma cells. Biochem Biophys Res Commun 2000;270:793-7.
48. Hayes RL, Kampfl A, Posmantur RM. The contribution of calpain proteolysis to neuronal death following traumatic brain injury. In: Wang KK, Yuen P, eds. Calpain: pharmacology and toxicology of calcium-dependent protease. Philadelphia: Taylor and Francis, 1999. 191-210.
49. Varghese J, Radhika G, Sarin A. The role of calpain in caspase activation during etoposide induced apoptosis in T cells. Eur J Immunol 2001;31:2035-41.
50. 2+ influx upregulate calpain and induce apoptosis in PC12 cells. Brain Res 2000;852:326-34.
51. Waters SL, Sarang SS, Wang KK, Schnellmann RG. Calpains mediate calcium and chloride influx during the late phase of cell injury. J Pharmacol Exp Ther 1997;283:1177-84.
52. Yanagisawa K, Sato S, Amaya N, Miyatake T. Degradation of myelin basic protein by calcium-activated neutral protease in human brain and inhibition by E-64 analogue. Neurochem Res 1983;8:1285-93.
53. Buki A, Okonkwo DO, Wang KK, Povlishock JT. Cytochrome c release and caspase activation in traumatic axonal injury. J Neurosci 2000;20:2825-34.
54. Levin ER. Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol Endocrinol 2003;17:309-17.
55. Sergeev IN, Norman AW. Calcium as a mediator of apoptosis in bovine oocytes and preimplantation embryos. Endocrine 2003;22:169-75.
56. 2+-mediated, calpain/caspase-12-dependent apoptosis in breast cancer cells. Biochem Biophys Res Commun 2004;321:462-7.
57. Roy M, Chakrabarty S, Sinha D, Bhattacharya RK, Siddiqi M. Anti-clastogenic, anti-genotoxic and apoptotic activity of epigallocatechin gallate: a green tea polyphenol. Mutat Res 2003;523/524:33-41.
58. Hastak K, Gupta S, Ahmad N, Agarwal MK, Agarwal ML, Mukhtar H. Role of p53 and NFκB in epigallocatechin-3-gallate-induced apoptosis of LNCaP cells. Oncogene 2003;22:4851-9.
59. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of Bid by caspase-8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998;94:491-501.
60. Olson M, Kornbluth S. Mitochondria in apoptosis and human disease. Curr Mol Med 2001;1:91-122.
61. Reed JC, Jurgensmeier JM, Matsuyama S. Bcl-2 family proteins and mitochondria. Biochim Biophys Acta 1998;1366:127-37.
62. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997;275:1132-6.
63. Ray SK, Matzelle DD, Wilford GG, Hogan EL, Banik NL. Cell death in spinal cord injury (SCI) requires de novo protein synthesis: calpain inhibitor E-64-d provides neuroprotection in SCI lesion and penumbra. Ann N Y Acad Sci 2001;939:436-49.
64. Shimizu S, Narita M, Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 1999;399:483-7.
65. Scarlett JL, Sheard PW, Hughes G, Ledgerwood EC, Ku HH, Murphy MP. Changes in mitochondrial membrane potential during staurosporine-induced apoptosis in Jurkat cells. FEBS Lett 2000;475:267-72.
66. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 1999;144:281-92.
67. Mitamura S, Ikawa H, Mizuno N, Kaziro Y, Itoh H. Cytosolic nuclease activated by caspase-3 and inhibited by DFF-45. Biochem Biophys Res Commun 1998;243:480-4.
68. Sakahira H, Enari M, Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 1998;391:96-9.
69. Enari M, Sakahira H, Yokoyama H, Okawa K, Iwamatsu A, Nagata S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 1998;391:43-50.
70. Kuo PL, Lin CC. Green tea constituent (-)-epigallocatechin-3-gallate inhibits HepG2 cell proliferation and induces apoptosis through p53-dependent and Fas-mediated pathways. J Biomed Sci 2003;10:219-27.