What drives intense apoptosis resistance and propensity for necrosis in glioblastoma? A role for Bcl2L12 as a multifunctional cell death regulator

Cell Cycle

Volumn 7, Issue 18, 2008, Pages 2833-2839

  Stegh, Alexander H ^a   Chin, Lynda ^a,b   Louis, David N ^b   DePinho, Ronald A ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; Bcl2L12; Caspase 3 and caspase 7; Glioblastoma; Necrosis; B crystallin

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 3; CASPASE 7; CRYSTALLIN; EMBELIN; HEPATOMA DERIVED GROWTH FACTOR; HIGH MOBILITY GROUP B1 PROTEIN; ONCOPROTEIN BCL 2 LIKE 2; PROTEIN BCL 2; PROTEIN INHIBITOR; SMALL HEAT SHOCK PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ADAPTATION; APOPTOSIS; BREAST CARCINOMA; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CARCINOGENESIS; CELL DEATH; CELL TYPE; COLORECTAL CANCER; ENERGY CONSERVATION; ENZYME ACTIVATION; ENZYME INHIBITION; ESOPHAGUS CARCINOMA; GENETICS; GLIA CELL; GLIOBLASTOMA; GLIOMA; HUMAN; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; LUNG NON SMALL CELL CANCER; MELANOMA; MITOCHONDRIAL MEMBRANE; MOLECULAR DYNAMICS; MOUTH CARCINOMA; NONHUMAN; PANCREAS CANCER; PANCREATITIS; POINT MUTATION; PROGNOSIS; PROSTATE CANCER; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR NECROSIS; UPREGULATION;

EID: 51849083426     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.7.18.6759     Document Type: Review

References (81)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (eds). World Health Organization Histological Classification of Tumours of the Central Nervous System. Lyon: International Agency for Research on Cancer, 2007.
2. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, Hahn WC, Ligon KL, Louis DN, Brennan C, Chin L, DePinho RA and Cavenee WK. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007; 21:2683-710.
3. Brat DJ and Van Meir EG. Vaso-occlusive and prothrombotic mechanisms associated with tumor hypoxia, necrosis and accelerated growth in glioblastoma. Lab Invest 2004; 84:397-405.
4. Chernova O and Cowell JK. Molecular definition of chromosome translocations involving 10q24 and 19q13 in human malignant glioma cells. Cancer Genet Cytogenet 1998; 105:60-8.
5. Magnani I, Chiariello E, Conti AM and Finocchiaro G. A recurrent 19q11-12 breakpoint suggested by cytogenetic and fluorescence in situ hybridization analysis of three glioblastoma cell lines. Cancer Genet Cytogenet 1999; 110:82-6.
6. Stegh AH, Kim H, Bachoo RM, Forloney KL, Zhang J, Schulze H, Park K, Hannon GJ, Yuan J, Louis DN, DePinho RA and Chin L. Bcl2L12 inhibits post-mitochondrial apoptosis signaling in glioblastoma. Genes Dev 2007; 21:98-111.
7. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL, Studholme DJ, Yeats C and Eddy SR. The Pfam protein families database. Nucleic Acids Res 2004; 32:138-41.
8. Youle RJ and Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008; 9:47-59.
9. Hanahan D and Weinberg RA. The hallmarks of cancer. Cell 2000; 100:57-70.
10. Roth W, Isenmann S, Nakamura M, Platten M, Wick W, Kleihues P, Bahr M, Ohgaki H, Ashkenazi A and Weller M. Soluble decoy receptor 3 is expressed by malignant gliomas and suppresses CD95 ligand-induced apoptosis and chemotaxis. Cancer Res 2001; 61:2759-65.
11. Roth W, Wagenknecht B, Klumpp A, Naumann U, Hahne M, Tschopp J and Weller M. APRIL, a new member of the tumor necrosis factor family, modulates death ligand-induced apoptosis. Cell Death Differ 2001; 8:403-10.
12. Louis DN. The p53 gene and protein in human brain tumors. J Neuropathol Exp Neurol 1994; 53:11-21.
13. Strik H, Deininger M, Streffer J, Grote E, Wickboldt J, Dichgans J, Weller M and Meyermann R. BCL-2 family protein expression in initial and recurrent glioblastomas: modulation by radiochemotherapy. J Neurol Neurosurg Psychiatry 1999; 67:763-8.
14. Julien T, Frankel B, Longo S, Kyle M, Gibson S, Shillitoe E and Ryken T. Antisense-mediated inhibition of the bcl-2 gene induces apoptosis in human malignant glioma. Surg Neurol 2000; 53:360-8.
15. McDonald FE, Ironside JW, Gregor A, Wyatt B, Stewart M, Rye R, Adams J and Potts HW. The prognostic influence of bcl-2 in malignant glioma. Br J Cancer 2002; 86:1899-904.
16. Nagane M, Pan G, Weddle JJ, Dixit VM, Cavenee WK and Huang HJ. Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor-related apoptosis-inducing ligand in vitro and in vivo. Cancer Res 2000; 60:847-53.
17. Stegh AH, Kesari S, Mahoney JE, Jenq HT, Forloney KL, Protopopov A, Louis DN, Chin L and Depinho RA. Bcl2L12-mediated inhibition of effector caspase-3 and caspase-7 via distinct mechanisms in glioblastoma. Proc Natl Acad Sci USA 2008.
18. Eckelman BP, Salvesen GS and Scott FL. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep 2006; 7:988-94.
19. Chen Z, Naito M, Hori S, Mashima T, Yamori T and Tsuruo T. A human IAP-family gene, apollon, expressed in human brain cancer cells. Biochem Biophys Res Commun 1999; 264:847-54.
20. Wagenknecht B, Glaser T, Naumann U, Kugler S, Isenmann S, Bahr M, Korneluk R, Liston P and Weller M. Expression and biological activity of X-linked inhibitor of apoptosis (XIAP) in human malignant glioma. Cell Death Differ 1999; 6:370-6.
21. Chakravarti A, Zhai GG, Zhang M, Malhotra R, Latham DE, Delaney MA, Robe P, Nestler U, Song Q and Loeffler J. Survivin enhances radiation resistance in primary human glioblastoma cells via caspase-independent mechanisms. Oncogene 2004; 23:7494-506.
22. Schimmer AD, Welsh K, Pinilla C, Wang Z, Krajewska M, Bonneau MJ, Pedersen IM, Kitada S, Scott FL, Bailly-Maitre B, Glinsky G, Scudiero D, Sausville E, Salvesen G, Nefzi A, Ostresh JM, Houghten RA and Reed JC. Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity. Cancer Cell 2004; 5:25-35.
23. Fulda S, Wick W, Weller M and Debatin KM. Smac agonists sensitize for Apo2L/TRAILor anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002; 8:808-15.
24. Arrigo AP, Simon S, Gibert B, Kretz-Remy C, Nivon M, Czekalla A, Guillet D, Moulin M, Diaz-Latoud C and Vicart P. Hsp27 (HspB1) and alphaB-crystallin (HspB5) as therapeutic targets. FEBS Lett 2007.
25. Clark JI and Muchowski PJ. Small heat-shock proteins and their potential role in human disease. Curr Opin Struct Biol 2000; 10:52-9.
26. Takashi M, Katsuno S, Sakata T, Ohshima S and Kato K. Different concentrations of two small stress proteins, alphaB crystallin and HSP27 in human urological tumor tissues. Urol Res 1998; 26:395-9.
27. Lo WY, Tsai MH, Tsai Y, Hua CH, Tsai FJ, Huang SY, Tsai CH and Lai CC. Identification of overexpressed proteins in oral squamous cell carcinoma (OSCC) patients by clinical proteomic analysis. Clin Chim Acta 2007; 376:101-7.
28. Holcakova J, Hernychova L, Bouchal P, Brozkova K, Zaloudik J, Valik D, Nenutil R and Vojtesek B. Identification of alphaB-crystallin, a biomarker of renal cell carcinoma by SELDI-TOF MS. Int J Biol Markers 2008; 23:48-53.
29. Sitterding SM, Wiseman WR, Schiller CL, Luan C, Chen F, Moyano JV, Watkin WG, Wiley EL, Cryns VL and Diaz LK. AlphaB-crystallin: a novel marker of invasive basal-like and metaplastic breast carcinomas. Ann Diagn Pathol 2008; 12:33-40.
30. Aoyama A, Frohli E, Schafer R and Klemenz R. AlphaB-crystallin expression in mouse NIH 3T3 fibroblasts: glucocorticoid responsiveness and involvement in thermal protection. Mol Cell Biol 1993; 13:1824-35.
31. Hitotsumatsu T, Iwaki T, Fukui M and Tateishi J. Distinctive immunohistochemical profiles of small heat shock proteins (heat shock protein 27 and alphaB-crystallin) in human brain tumors. Cancer 1996; 77:352-61.
32. Kato S, Hirano A, Kato M, Herz F and Ohama E. Comparative study on the expression of stress-response protein (srp) 72, srp 27, alphaB-crystallin and ubiquitin in brain tumours. An immunohistochemical investigation. Neuropathol Appl Neurobiol 1993; 19:436-42.
33. Moyano JV, Evans JR, Chen F, Lu M, Werner ME, Yehiely F, Diaz LK, Turbin D, Karaca G, Wiley E, Nielsen TO, Perou CM and Cryns VL. AlphaB-crystallin is a novel oncoprotein that predicts poor clinical outcome in breast cancer. J Clin Invest 2006; 116:261-70.
34. Kamradt MC, Chen F, Sam S and Cryns VL. The small heat shock protein alphaB-crystallin negatively regulates apoptosis during myogenic differentiation by inhibiting caspase-3 activation. J Biol Chem 2002; 277:38731-6.
35. 2-induced apoptosis through downregulation of the alphaB-crystallin gene. J Biol Chem 2001; 276:43435-45.
36. Chai J, Shiozaki E, Srinivasula SM, Wu Q, Datta P, Alnemri ES and Shi Y. Structural basis of caspase-7 inhibition by XIAP. Cell 2001; 104:769-80.
37. Huang Y, Park YC, Rich RL, Segal D, Myszka DG and Wu H. Structural basis of caspase inhibition by XIAP: differential roles of the linker versus the BIR domain. Cell 2001; 104:781-90.
38. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW, Liddington RC and Salvesen GS. Structural basis for the inhibition of caspase-3 by XIAP. Cell 2001; 104:791-800.
39. Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, Klein-Szanto AJ, Rustgi A, Fuchs SY and Diehl JA. Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex. Mol Cell 2006; 24:355-66.
40. Huang H, Joazeiro CA, Bonfoco E, Kamada S, Leverson JD and Hunter T. The inhibitor of apoptosis, cIAP2, functions as a ubiquitin-protein ligase and promotes in vitro monoubiquitination of caspases 3 and 7. J Biol Chem 2000; 275:26661-4.
41. Suzuki Y, Nakabayashi Y, Nakata K, Reed JC and Takahashi R. X-linked inhibitor of apoptosis protein (XIAP) inhibits caspase-3 and -7 in distinct modes. J Biol Chem 2001; 276:27058-63.
42. Kato K, Ito H, Kamei K, Inaguma Y, Iwamoto I and Saga S. Phosphorylation of alphaB-crystallin in mitotic cells and identification of enzymatic activities responsible for phosphorylation. J Biol Chem 1998; 273:28346-54.
43. Chautan M, Chazal G, Cecconi F, Gruss P and Golstein P. Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr Biol 1999; 9:967-70.
44. Leist M, Single B, Castoldi AF, Kuhnle S and Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 1997; 185:1481-6.
45. Nicotera P, Leist M and Ferrando-May E. Apoptosis and necrosis: different execution of the same death. Biochem Soc Symp 1999; 66:69-73.
46. Reed JC and Pellecchia M. Apoptosis-based therapies for hematologic malignancies. Blood 2005; 106:408-18.
47. Mareninova OA, Sung KF, Hong P, Lugea A, Pandol SJ, Gukovsky I and Gukovskaya AS. Cell death in pancreatitis: caspases protect from necrotizing pancreatitis. J Biol Chem 2006; 281:3370-81.
48. Chan FK, Shisler J, Bixby JG, Felices M, Zheng L, Appel M, Orenstein J, Moss B and Lenardo MJ. A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J Biol Chem 2003; 278:51613-21.
49. Holler N, Zaru R, Micheau O, Thome M, Attinger A, Valitutti S, Bodmer JL, Schneider P, Seed B and Tschopp J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 2000; 1:489-95.
50. Ditsworth D, Zong WX and Thompson CB. Activation of poly(ADP)-ribose polymerase (PARP-1) induces release of the pro-inflammatory mediator HMGB1 from the nucleus. J Biol Chem 2007; 282:17845-54.
51. Zong WX, Ditsworth D, Bauer DE, Wang ZQ and Thompson CB. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 2004; 18:1272-82.
52. + exchanger in excitotoxicity. Cell 2005; 120:275-85.
53. Wang KK. Calpain and caspase: can you tell the difference? Trends Neurosci 2000; 23:20-6.
54. 2+-dependent proteases in ischemic neuronal death: a conserved 'calpaincathepsin cascade' from nematodes to primates. Cell Calcium 2004; 36:285-93.
55. Kagedal K, Zhao M, Svensson I and Brunk UT. Sphingosine-induced apoptosis is dependent on lysosomal proteases. Biochem J 2001; 359:335-43.
56. Perez-Morga D, Vanhollebeke B, Paturiaux-Hanocq F, Nolan DP, Lins L, Homble F, Vanhamme L, Tebabi P, Pays A, Poelvoorde P, Jacquet A, Brasseur R and Pays E. Apolipoprotein L-I promotes trypanosome lysis by forming pores in lysosomal membranes. Science 2005; 309:469-72.
57. Boise LH and Collins CM. Salmonella-induced cell death: apoptosis, necrosis or programmed cell death? Trends Microbiol 2001; 9:64-7.
58. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J and Molkentin JD. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005; 434:658-62.
59. Nakagawa T, Shimizu S, Watanabe T, Yamaguchi O, Otsu K, Yamagata H, Inohara H, Kubo T and Tsujimoto Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005; 434:652-8.
60. Brat DJ, Castellano-Sanchez AA, Hunter SB, Pecot M, Cohen C, Hammond EH, Devi SN, Kaur B and Van Meir EG. Pseudopalisades in glioblastoma are hypoxic, express extracellular matrix proteases, and are formed by an actively migrating cell population. Cancer Res 2004; 64:920-7.
61. Golstein P and Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 2007; 32:37-43.
62. Zong WX and Thompson CB. Necrotic death as a cell fate. Genes Dev 2006; 20:1-15.
63. Dong S, Nutt CL, Betensky RA, Stemmer-Rachamimov AO, Denko NC, Ligon KL, Rowitch DH and Louis DN. Histology-based expression profiling yields novel prognostic markers in human glioblastoma. J Neuropathol Exp Neurol 2005; 64:948-55.
64. Tachibana O, Lampe J, Kleihues P and Ohgaki H. Preferential expression of Fas/APO1 (CD95) and apoptotic cell death in perinecrotic cells of glioblastoma multiforme. Acta Neuropathol 1996; 92:431-4.
65. Tachibana O, Nakazawa H, Lampe J, Watanabe K, Kleihues P and Ohgaki H. Expression of Fas/APO-1 during the progression of astrocytomas. Cancer Res 1995; 55:5528-30.
66. Daumas-Duport C, Scheithauer B, O'Fallon J and Kelly P. Grading of astrocytomas. A simple and reproducible method. Cancer 1988; 62:2152-65.
67. Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D and Sawaya R. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 2001; 95:190-8.
68. Flannery T, McQuaid S, McGoohan C, McConnell RS, McGregor G, Mirakhur M, Hamilton P, Diamond J, Cran G, Walker B, Scott C, Martin L, Ellison D, Patel C, Nicholson C, Mendelow D, McCormick D and Johnston PG. Cathepsin S expression: An independent prognostic factor in glioblastoma tumours - A pilot study. Int J Cancer 2006; 119:854-60.
69. Keerthivasan S, Keerthivasan G, Mittal S and Chauhan SS. Transcriptional upregulation of human cathepsin L by VEGF in glioblastoma cells. Gene 2007; 399:129-36.
70. Zeh HJ, 3rd and Lotze MT. Addicted to death: invasive cancer and the immune response to unscheduled cell death. J Immunother 2005; 28:1-9.
71. Logsdon CD, Fuentes MK, Huang EH and Arumugam T. RAGE and RAGE ligands in cancer. Curr Mol Med 2007; 7:777-89.
72. Chang KC, Tai MH, Lin JW, Wang CC, Huang CC, Hung CH, Chen CH, Lu SN, Lee CM, Changchien CS and Hu TH. Hepatoma-derived growth factor is a novel prognostic factor for gastrointestinal stromal tumors. Int J Cancer 2007; 121:1059-65.
73. Yamamoto S, Tomita Y, Hoshida Y, Takiguchi S, Fujiwara Y, Yasuda T, Doki Y, Yoshida K, Aozasa K, Nakamura H and Monden M. Expression of hepatoma-derived growth factor is correlated with lymph node metastasis and prognosis of gastric carcinoma. Clin Cancer Res 2006; 12:117-22.
74. Uyama H, Tomita Y, Nakamura H, Nakamori S, Zhang B, Hoshida Y, Enomoto H, Okuda Y, Sakon M, Aozasa K, Kawase I, Hayashi N and Monden M. Hepatoma-derived growth factor is a novel prognostic factor for patients with pancreatic cancer. Clin Cancer Res 2006; 12:6043-8.
75. Yoshida K, Tomita Y, Okuda Y, Yamamoto S, Enomoto H, Uyama H, Ito H, Hoshida Y, Aozasa K, Nagano H, Sakon M, Kawase I, Monden M and Nakamura H. Hepatoma-derived growth factor is a novel prognostic factor for hepatocellular carcinoma. Ann Surg Oncol 2006; 13:159-67.
76. Ren H, Tang X, Lee JJ, Feng L, Everett AD, Hong WK, Khuri FR and Mao L. Expression of hepatoma-derived growth factor is a strong prognostic predictor for patients with early-stage non-small-cell lung cancer. J Clin Oncol 2004; 22:3230-7.
77. Lepourcelet M, Tou L, Cai L, Sawada J, Lazar AJ, Glickman JN, Williamson JA, Everett AD, Redston M, Fox EA, Nakatani Y and Shivdasani RA. Insights into developmental mechanisms and cancers in the mammalian intestine derived from serial analysis of gene expression and study of the hepatoma-derived growth factor (HDGF). Development 2005; 132:415-27.
78. Bernard K, Litman E, Fitzpatrick JL, Shellman YG, Argast G, Polvinen K, Everett AD, Fukasawa K, Norris DA, Ahn NG and Resing KA. Functional proteomic analysis of melanoma progression. Cancer Res 2003; 63:6716-25.
79. Okuda Y, Nakamura H, Yoshida K, Enomoto H, Uyama H, Hirotani T, Funamoto M, Ito H, Everett AD, Hada T and Kawase I. Hepatoma-derived growth factor induces tumorigenesis in vivo through both direct angiogenic activity and induction of vascular endothelial growth factor. Cancer Sci 2003; 94:1034-41.
80. Zhang J, Ren H, Yuan P, Lang W, Zhang L and Mao L. Downregulation of hepatoma-derived growth factor inhibits anchorage-independent growth and invasion of non-small cell lung cancer cells. Cancer Res 2006; 66:18-23.
81. Gilbertson RJ and Rich JN. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer 2007; 7:733-6.