αB-crystallin is elevated in highly infiltrative apoptosis-resistant glioblastoma cells

American Journal of Pathology

Volumn 177, Issue 4, 2010, Pages 1618-1628

  Goplen, Dorota ^a,b   Bougnaud, Sébastien ^d   Rajcevic, Uroš ^d   Bøe, Stig O ^a   Skaftnesmo, Kai O ^a   Voges, Juergen ^c   Enger, Per O Ø ^a,b   Wang, Jian ^a   Tysnes, Berit B ^a   Laerum, Ole D ^a   Niclou, Simone ^d   Bjerkvig, Rolf ^a,d  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BASIC CRYSTALLIN; ALPHA CRYSTALLIN; DACTINOMYCIN; HEAT SHOCK PROTEIN; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INFILTRATION; CELL MIGRATION; CELL PROTECTION; CONTROLLED STUDY; GENE OVEREXPRESSION; GLIOBLASTOMA; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; MASS SPECTROMETRY; NONHUMAN; NUDE RAT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ELECTROPHORESIS; RAT; WESTERN BLOTTING; XENOTRANSPLANTATION;

EID: 77957366358     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090063     Document Type: Article

References (56)

1. Norden AD, Wen PY: Glioma therapy in adults. Neurologist 2006, 12:279-292
2. Giese A, Westphal M: Glioma invasion in the central nervous system. Neurosurgery 1996, 39:235-250; discussion 250-232
3. Giese A, Bjerkvig R, Berens ME, Westphal M: Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 2003, 21:1624-1636
4. Rempel SA, Ge S, Gutierrez JA: SPARC: a potential diagnostic marker of invasive meningiomas. Clin Cancer Res 1999, 5:237-241
5. Tysnes BB, Mahesparan R: Biological mechanisms of glioma invasion and potential therapeutic targets. J Neurooncol 2001, 53:129-147
6. Gunther W, Skaftnesmo KO, Arnold H, Terzis AJ: Molecular approaches to brain tumour invasion. Acta Neurochir (Wien) 2003, 145:1029-1036
7. Bjerkvig R, Tonnesen A, Laerum OD, Backlund EO: Multicellular tumor spheroids from human gliomas maintained in organ culture. J Neurosurg 1990, 72:463-475
8. Engebraaten O, Bjerkvig R, Lund-Johansen M, Wester K, Pedersen PH, Mork S, Backlund EO, Laerum OD: Interaction between human brain tumour biopsies and fetal rat brain tissue in vitro. Acta Neuropathol (Berl) 1990, 81:130-140
9. Sakariassen PO, Prestegarden L, Wang J, Skaftnesmo KO, Mahesparan R, Molthoff C, Sminia P, Sundlisaeter E, Misra A, Tysnes BB, Chekenya M, Peters H, Lende G, Kalland KH, Oyan AM, Petersen K, Jonassen I, van der Kogel A, Feuerstein BG, Terzis AJ, Bjerkvig R, Enger PO: Angiogenesis-independent tumor growth mediated by stem-like cancer cells. Proc Natl Acad Sci USA 2006, 103:16466-16471
10. Klemenz R, Frohli E, Steiger RH, Schafer R, Aoyama A: Alpha Bcrystallin is a small heat shock protein. Proc Natl Acad Sci USA 1991, 88:3652-3656 (Pubitemid 21916681)
11. Aoyama A, Frohli E, Schafer R, Klemenz R: Alpha B-crystallin expression in mouse NIH 3T3 fibroblasts: glucocorticoid responsiveness and involvement in thermal protection. Mol Cell Biol 1993, 13:1824-1835 (Pubitemid 23068121)
12. Horwitz J: Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 1992, 89:10449-10453
13. Kantorow M, Piatigorsky J: Alpha-crystallin/small heat shock protein has autokinase activity. Proc Natl Acad Sci USA 1994, 91:3112-3116 (Pubitemid 24130185)
14. Iwaki T, Wisniewski T, Iwaki A, Corbin E, Tomokane N, Tateishi J, Goldman JE: Accumulation of alpha B-crystallin in central nervous system glia and neurons in pathologic conditions. Am J Pathol 1992, 140:345-356
15. Nicholl ID, Quinlan RA: Chaperone activity of alpha-crystallins modulates intermediate filament assembly. EMBO J 1994, 13:945-953 (Pubitemid 2032569)
16. Perng MD, Cairns L, van den IP, Prescott A, Hutcheson AM, Quinlan RA: Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin. J Cell Sci 1999, 112:2099-2112 (Pubitemid 29355425)
17. Wisniewski T, Goldman JE: Alpha B-crystallin is associated with intermediate filaments in astrocytoma cells. Neurochem Res 1998, 23:385-392 (Pubitemid 28109884)
18. Iwaki T, Iwaki A, Miyazono M, Goldman JE: Preferential expression of alpha B-crystallin in astrocytic elements of neuroectodermal tumors. Cancer 1991, 68:2230-2240
19. Hitotsumatsu T, Iwaki T, Fukui M, Tateishi J: Distinctive immunohistochemical profiles of small heat shock proteins (heat shock protein 27 and alpha B-crystallin) in human brain tumors. Cancer 1996, 77:352-361 (Pubitemid 26023355)
20. de Ridder LI, Laerum OD, Mork SJ, Bigner DD: Invasiveness of human glioma cell lines in vitro: relation to tumorigenicity in athymic mice. Acta Neuropathol (Berl) 1987, 72:207-213
21. Engebraaten O, Hjortland GO, Hirschberg H, Fodstad O: Growth of precultured human glioma specimens in nude rat brain. J Neurosurg 1999, 90:125-132 (Pubitemid 29024749)
22. Thorsen F, Ersland L, Nordli H, Enger PO, Huszthy PC, Lundervold A, Standnes T, Bjerkvig R, Lund-Johansen M: Imaging of experimental rat gliomas using a clinical MR scanner. J Neurooncol 2003, 63:225-231 (Pubitemid 36880723)
23. Enger PO, Thorsen F, Lonning PE, Bjerkvig R, Hoover F: Adeno-associated viral vectors penetrate human solid tumor tissue in vivo more effectively than adenoviral vectors. Hum Gene Ther 2002, 13:1115-1125 (Pubitemid 34721325)
24. Goplen D, Wang J, Enger PO, Tysnes BB, Terzis AJ, Laerum OD, Bjerkvig R: Protein disulfide isomerase expression is related to the invasive properties of malignant glioma. Cancer Res 2006, 66:9895-9902
25. Balgley BM, Laudeman T, Yang L, Song T, Lee CS: Comparative evaluation of tandem MS search algorithms using a target-decoy search strategy. Mol Cell Proteomics 2007, 6:1599-1608
26. Voges J, Schroder R, Treuer H, Pastyr O, Schlegel W, Lorenz WJ, Sturm V: CT-guided and computer assisted stereotactic biopsy. Technique, results, indications. Acta Neurochir (Wien) 1993, 125:142-149
27. Jul-Larsen A, Visted T, Karlsen BO, Rinaldo CH, Bjerkvig R, Lonning PE, Boe SO: PML-nuclear bodies accumulate DNA in response to polyomavirus BK and simian virus 40 replication. Exp Cell Res 2004, 298:58-73
28. Ruitenberg MJ, Plant GW, Christensen CL, Blits B, Niclou SP, Harvey AR, Boer GJ, Verhaagen J: Viral vector-mediated gene expression in olfactory ensheathing glia implants in the lesioned rat spinal cord. Gene Ther 2002, 9:135-146
29. Lefranc F, Brotchi J, Kiss R: Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J Clin Oncol 2005, 23:2411-2422
30. Uhm JH, Dooley NP, Kyritsis AP, Rao JS, Gladson CL: Vitronectin, a glioma-derived extracellular matrix protein, protects tumor cells from apoptotic death. Clin Cancer Res 1999, 5:1587-1594
31. Aoyama A, Steiger RH, Frohli E, Schafer R, von Deimling A, Wiestler OD, Klemenz R: Expression of alpha B-crystallin in human brain tumors. Int J Cancer 1993, 55:760-764
32. Odreman F, Vindigni M, Gonzales ML, Niccolini B, Candiano G, Zanotti B, Skrap M, Pizzolitto S, Stanta G, Vindigni A: Proteomic studies on low- and high-grade human brain astrocytomas. J Proteome Res 2005, 4:698-708
33. Mariani L, Beaudry C, McDonough WS, Hoelzinger DB, Demuth T, Ross KR, Berens T, Coons SW, Watts G, Trent JM, Wei JS, Giese A, Berens ME: Glioma cell motility is associated with reduced transcription of proapoptotic and proliferation genes: a cDNA microarray analysis. J Neurooncol 2001, 53:161-176
34. Chelouche-Lev D, Kluger HM, Berger AJ, Rimm DL, Price JE: alphaB-crystallin as a marker of lymph node involvement in breast carcinoma. Cancer 2004, 100:2543-2548
35. Moyano JV, Evans JR, Chen F, Lu M, Werner ME, Yehiely F, Diaz LK, Turbin D, Karaca G, Wiley E, Nielsen TO, Perou CM, Cryns VL: AlphaB-crystallin is a novel oncoprotein that predicts poor clinical outcome in breast cancer. J Clin Invest 2006, 116:261-270
36. Cicek M, Samant RS, Kinter M, Welch DR, Casey G: Identification of metastasis-associated proteins through protein analysis of metastatic MDA-MB-435 and metastasis-suppressed BRMS1 transfected-MDA-MB-435 cells. Clin Exp Metastasis 2004, 21:149-157
37. Gruvberger-Saal SK, Parsons R: Is the small heat shock protein alphaB-crystallin an oncogene?. J Clin Invest 2006, 116:30-32
38. Kamradt MC, Chen F, Cryns VL: The small heat shock protein alpha B-crystallin negatively regulates cytochrome c- and caspase-8-dependent activation of caspase-3 by inhibiting its autoproteolytic maturation. J Biol Chem 2001, 276:16059-16063
39. Liu B, Bhat M, Nagaraj RH: AlphaB-crystallin inhibits glucose-induced apoptosis in vascular endothelial cells. Biochem Biophys Res Commun 2004, 321:254-258 (Pubitemid 39055632)
40. Kamradt MC, Lu M, Werner ME, Kwan T, Chen F, Strohecker A, Oshita S, Wilkinson JC, Yu C, Oliver PG, Duckett CS, Buchsbaum DJ, LoBuglio AF, Jordan VC, Cryns VL: The small heat shock protein alpha B-crystallin is a novel inhibitor of TRAIL-induced apoptosis that suppresses the activation of caspase-3. J Biol Chem 2005, 280:11059-11066
41. Stegh AH, Chin L, Louis DN, DePinho RA: What drives intense apoptosis resistance and propensity for necrosis in glioblastoma? A role for Bcl2L12 as a multifunctional cell death regulator. Cell Cycle 2008, 7:2833-2839
42. Ikeda R, Yoshida K, Ushiyama M, Yamaguchi T, Iwashita K, Futagawa T, Shibayama Y, Oiso S, Takeda Y, Kariyazono H, Furukawa T, Nakamura K, Akiyama S, Inoue I, Yamada K: The small heat shock protein alphaB-crystallin inhibits differentiation-induced caspase 3 activation and myogenic differentiation. Biol Pharm Bull 2006, 29:1815-1819
43. Wilkins MR, Gasteiger E, Sanchez JC, Bairoch A, Hochstrasser DF: Two-dimensional gel electrophoresis for proteome projects: the effects of protein hydrophobicity and copy number. Electrophoresis 1998, 19:1501-1505 (Pubitemid 28310866)
44. Chambers G, Lawrie L, Cash P, Murray GI: Proteomics: a new approach to the study of disease. J Pathol 2000, 192:280-288
45. Simon S, Fontaine JM, Martin JL, Sun X, Hoppe AD, Welsh MJ, Benndorf R, Vicart P: Myopathy-associated alphaB-crystallin mutants: abnormal phosphorylation, intracellular location, and interactions with other small heat shock proteins. J Biol Chem 2007, 282:34276-34287 (Pubitemid 350159493)
46. Sun Y, MacRae TH: Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 2005, 62:2460-2476 (Pubitemid 41801099)
47. Gangalum RK, Schibler MJ, Bhat SP: Small heat shock protein alphaB-crystallin is part of cell cycle-dependent Golgi reorganization. J Biol Chem 2004, 279:43374-43377
48. Bhat SP, Hale IL, Matsumoto B, Elghanayan D: Ectopic expression of alpha B-crystallin in Chinese hamster ovary cells suggests a nuclear role for this protein. Eur J Cell Biol 1999, 78:143-150 (Pubitemid 29112476)
49. van Rijk AE, Stege GJ, Bennink EJ, May A, Bloemendal H: Nuclear staining for the small heat shock protein alphaB-crystallin colocalizes with splicing factor SC35. Eur J Cell Biol 2003, 82:361-368 (Pubitemid 36944165)
50. Maddala R, Rao VP: alpha-Crystallin localizes to the leading edges of migrating lens epithelial cells. Exp Cell Res 2005, 306:203-215 (Pubitemid 40692784)
51. Goldbaum O, Riedel M, Stahnke T, Richter-Landsberg C: The small heat shock protein HSP25 protects astrocytes against stress induced by proteasomal inhibition. Glia 2009, 57:1566-1577
52. Stegh AH, Kesari S, Mahoney JE, Jenq HT, Forloney KL, Protopopov A, Louis DN, Chin L, DePinho RA: Bcl2L12-mediated inhibition of effector caspase-3 and caspase-7 via distinct mechanisms in glioblastoma. Proc Natl Acad Sci USA 2008, 105:10703-10708
53. Schauff AK, Kim EL, Leppert J, Nadrowitz R, Wuestenberg R, Brockmann MA, Giese A: Inhibition of invasion-associated thromboxane synthase sensitizes experimental gliomas to gamma-radiation, J Neurooncol 2009, 91:241-249
54. Nakada M, Nakada S, Demuth T, Tran NL, Hoelzinger DB, Berens ME: Molecular targets of glioma invasion. Cell Mol Life Sci 2007, 64:458-478
55. Wick W, Wagner S, Kerkau S, Dichgans J, Tonn JC, Weller M: BCL-2 promotes migration and invasiveness of human glioma cells. FEBS Lett 1998, 440:419-424 (Pubitemid 29052326)
56. Bowers DC, Fan S, Walter KA, Abounader R, Williams JA, Rosen EM, Laterra J: Scatter factor/hepatocyte growth factor protects against cytotoxic death in human glioblastoma via phosphatidylinositol 3-kinase- and AKT-dependent pathways. Cancer Res 2000, 60:4277-4283 (Pubitemid 30636617)