Binding of Par-4 to the actin cytoskeleton is essential for Par-4/Dlk-mediated apoptosis

Experimental Cell Research

Volumn 305, Issue 2, 2005, Pages 392-408

  Vetterkind, Susanne ^a   Illenberger, Susanne ^b   Kubicek, Jan ^c   Boosen, Meike ^a   Appel, Sarah ^a   Naim, Hassan Y ^d   Scheidtmann, Karl Heinz ^a   Preuss, Ute ^a  

^a UNIVERSITY OF BONN   (Germany)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

Actin; Apoptosis; Cytoskeleton; Dlk; Par 4

Indexed keywords

ACTIN BINDING PROTEIN; AMINO ACID; DEATH ASSOCIATED PROTEIN KINASE; F ACTIN; LEUCINE ZIPPER PROTEIN; MEMBRANE PROTEIN; PROSTATE APOPTOSIS RESPONSE 4 PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFOCAL FLUORESCENCE MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; ENZYME MECHANISM; FIBROBLAST; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE; GENE FUNCTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE BINDING; MICROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROSTATE APOPTOSIS RESPONSE 4 GENE; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SEDIMENTATION; STRESS FIBER;

EID: 16244415838     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2005.01.012     Document Type: Article

References (61)

1. C. Benoist, and D. Mathis Cell death mediators in autoimmune diabetes-no shortage of suspects Cell 89 1997 1 3
2. M.K. Hellerstein, and J.M. McCune T cell turnover in HIV-1 disease Immunity 7 1997 583 589
3. C.B. Thompson Apoptosis in the pathogenesis and treatment of disease Science 267 1995 1456 1462
4. M. Barradas, A. Monjas, M.T. Diaz-Meco, M. Serrano, and J. Moscat The downregulation of the pro-apoptotic protein Par-4 is critical for Ras-induced survival and tumor progression EMBO J. 18 1999 6362 6369
5. J. Cook, S. Krishnan, S. Ananth, S.F. Sells, Y. Shi, M.M. Walther, W.M. Linehan, V.P. Sukhatme, M.H. Weinstein, and V.M. Rangnekar Decreased expression of the pro-apoptotic protein Par-4 in renal cell carcinoma Oncogene 18 1999 1205 1208
6. T. Lucas, B. Pratscher, S. Krishnan, D. Fink, P. Gunsberg, M. Wolschek, V. Wacheck, T. Muster, I. Romirer, K. Wolff, H. Pehamberger, H.G. Eichler, V.M. Rangnekar, and B. Jansen Differential expression levels of Par-4 in melanoma Melanoma Res. 11 2001 379 383
7. G. Qiu, M. Ahmed, S.F. Sells, M. Mohiuddin, M.H. Weinstein, and V.M. Rangnekar Mutually exclusive expression patterns of Bcl-2 and Par-4 in human prostate tumors consistent with down-regulation of Bcl-2 by Par-4 Oncogene 18 1999 623 631
8. S.G. Qiu, S. Krishnan, N. El-Guendy, and V.M. Rangnekar Negative regulation of Par-4 by oncogenic Ras is essential for cellular transformation Oncogene 18 1999 7115 7123
9. C. Culmsee, Y. Zhu, J. Krieglstein, and M.P. Mattson Evidence for the involvement of Par-4 in ischemic neuron cell death J. Cereb. Blood Flow Metab. 21 2001 334 343
10. W. Duan, Z. Zhang, D.M. Gash, and M.P. Mattson Participation of prostate apoptosis response-4 in degeneration of dopaminergic neurons in models of Parkinson's disease Ann. Neurol. 46 1999 587 597
11. W. Duan, V.M. Rangnekar, and M.P. Mattson Prostate apoptosis response-4 production in synaptic compartments following apoptotic and excitotoxic insults: evidence for a pivotal role in mitochondrial dysfunction and neuronal degeneration J. Neurochem. 72 1999 2312 2322
12. Q. Guo, W. Fu, J. Xie, H. Luo, S.F. Sells, J.W. Geddes, V. Bondada, V.M. Rangnekar, and M.P. Mattson Par-4 is a mediator of neuronal degeneration associated with the pathogenesis of Alzheimer disease Nat. Med. 4 1998 957 962
13. W.A. Pedersen, H. Luo, I. Kruman, E. Kasarskis, and M.P. Mattson The prostate apoptosis response-4 protein participates in motor neuron degeneration in amyotrophic lateral sclerosis FASEB J. 14 2000 913 924
14. J. Xie, X. Chang, X. Zhang, and Q. Guo Aberrant induction of Par-4 is involved in apoptosis of hippocampal neurons in presenilin-1 M146V mutant knock-in mice Brain Res. 915 2001 1 10
15. M.P. Mattson, W. Duan, S.L. Chan, and S. Camandola Par-4: an emerging pivotal player in neuronal apoptosis and neurodegenerative disorders J. Mol. Neurosci. 13 1999 17 30
16. S.F. Sells, D.P. Wood Jr., S.S. Joshi-Barve, S. Muthukumar, R.J. Jacob, S.A. Crist, S. Humphreys, and V.M. Rangnekar Commonality of the gene programs induced by effectors of apoptosis in androgen-dependent and -independent prostate cells Cell Growth Differ. 5 1994 457 466
17. N. El-Guendy, Y. Zhao, S. Gurumurthy, R. Burikhanov, and V.M. Rangnekar Identification of a unique core domain of par-4 sufficient for selective apoptosis induction in cancer cells Mol. Cell. Biol. 23 2003 5516 5525
18. S. Bang, E.J. Jeong, I.K. Kim, Y.K. Jung, and K.S. Kim Fas- and tumor necrosis factor-mediated apoptosis uses the same binding surface of FADD to trigger signal transduction. A typical model for convergent signal transduction J. Biol. Chem. 275 2000 36217 36222
19. M.T. Diaz-Meco, M.M. Municio, S. Frutos, P. Sanchez, J. Lozano, L. Sanz, and J. Moscat The product of par-4, a gene induced during apoptosis, interacts selectively with the atypical isoforms of protein kinase C Cell 86 1996 777 786
20. R.W. Johnstone, R.H. See, S.F. Sells, J. Wang, S. Muthukkumar, C. Englert, D.A. Haber, J.D. Licht, S.P. Sugrue, T. Roberts, V.M. Rangnekar, and Y. Shi A novel repressor, par-4, modulates transcription and growth suppression functions of the Wilms' tumor suppressor WT1 Mol. Cell. Biol. 16 1996 6945 6956
21. V.M. Rangnekar Apoptosis mediated by a novel leucine zipper protein Par-4 Apoptosis 3 1998 61 66
22. S.F. Sells, S.S. Han, S. Muthukkumar, N. Maddiwar, R. Johnstone, E. Boghaert, D. Gillis, G. Liu, P. Nair, S. Monnig, P. Collini, M.P. Mattson, V.P. Sukhatme, S.G. Zimmer, D.P. Wood Jr., J.W. McRoberts, Y. Shi, and V.M. Rangnekar Expression and function of the leucine zipper protein Par-4 in apoptosis Mol. Cell. Biol. 17 1997 3823 3832
23. T.W. Hai, F. Liu, W.J. Coukos, and M.R. Green Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers Genes Dev. 3 1989 2083 2090
24. T. Kouzarides, and E. Ziff The role of the leucine zipper in the fos-jun interaction Nature 336 1988 646 651
25. E.M. Blackwood, and R.N. Eisenman Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc Science 251 1991 1211 1217
26. D.J. Richard, V. Schumacher, B. Royer-Pokora, and S.G. Roberts Par4 is a coactivator for a splice isoform-specific transcriptional activation domain in WT1 Genes Dev. 15 2001 328 339
27. E.R. Boghaert, S.F. Sells, A.J. Walid, P. Malone, N.M. Williams, M.H. Weinstein, R. Strange, and V.M. Rangnekar Immunohistochemical analysis of the proapoptotic protein Par-4 in normal rat tissues Cell Growth Differ. 8 1997 881 890
28. J. Anrather, V. Csizmadia, M.P. Soares, and H. Winkler Regulation of NF-kappaB RelA phosphorylation and transcriptional activity by p21(ras) and protein kinase Czeta in primary endothelial cells J. Biol. Chem. 274 1999 13594 13603
29. G. Guo, Y. Yan-Sanders, B.D. Lyn-Cook, T. Wang, D. Tamae, J. Ogi, A. Khaletskiy, Z. Li, C. Weydert, J.A. Longmate, T.T. Huang, D.R. Spitz, L.W. Oberley, and J.J. Li Manganese superoxide dismutase-mediated gene expression in radiation-induced adaptive responses Mol. Cell. Biol. 23 2003 2362 2378
30. L.K. Miller An exegesis of IAPs: salvation and surprises from BIR motifs Trends Cell Biol. 9 1999 323 328
31. S. Boehrer, K.U. Chow, F. Beske, N. Kukoc-Zivojnov, E. Puccetti, M. Ruthardt, C. Baum, V.M. Rangnekar, D. Hoelzer, P.S. Mitrou, and E. Weidmann In lymphatic cells par-4 sensitizes to apoptosis by down-regulating bcl-2 and promoting disruption of mitochondrial membrane potential and caspase activation Cancer Res. 62 2002 1768 1775
32. S. Camandola, and M.P. Mattson Pro-apoptotic action of PAR-4 involves inhibition of NF-kappaB activity and suppression of BCL-2 expression J. Neurosci. Res. 61 2000 134 139
33. G. Page, D. Kögel, V. Rangnekar, and K.H. Scheidtmann Interaction partners of Dlk/ZIP kinase: co-expression of Dlk/ZIP kinase and Par-4 results in cytoplasmic retention and apoptosis Oncogene 18 1999 7265 7273
34. D. Kögel, O. Plöttner, G. Landsberg, S. Christian, and K.H. Scheidtmann Cloning and characterization of Dlk, a novel serine/threonine kinase that is tightly associated with chromatin and phosphorylates core histones. PG Oncogene 17 1998 2645 2654
35. O. Cohen, E. Feinstein, and A. Kimchi DAP-kinase is a Ca2+/calmodulin-dependent, cytoskeletal-associated protein kinase, with cell death-inducing functions that depend on its catalytic activity EMBO J. 16 1997 998 1008
36. N. Suarez-Huerta, R. Mosselmans, J.E. Dumont, and B. Robaye Actin depolymerization and polymerization are required during apoptosis in endothelial cells J. Cell. Physiol. 184 2000 239 245
37. M.G. Levee, M.I. Dabrowska, J.L. Lelli Jr., and D.B. Hinshaw Actin polymerization and depolymerization during apoptosis in HL-60 cells Am. J. Physiol. 271 1996 C1981 C1992
38. J.Y. Rao, Y.S. Jin, Q. Zheng, J. Cheng, J. Tai, and G.P. Hemstreet III Alterations of the actin polymerization status as an apoptotic morphological effector in HL-60 cells J. Cell. Biochem. 75 1999 686 697
39. J.A. Kim, K. Mitsukawa, M.K. Yamada, N. Nishiyama, N. Matsuki, and Y. Ikegaya Cytoskeleton disruption causes apoptotic degeneration of dentate granule cells in hippocampal slice cultures Neuropharmacology 42 2002 1109 1118
40. H. Suria, L.A. Chau, E. Negrou, D.J. Kelvin, and J. Madrenas Cytoskeletal disruption induces T cell apoptosis by a caspase-3 mediated mechanism Life Sci. 65 1999 2697 2707
41. S.R. White, P. Williams, K.R. Wojcik, S. Sun, P.S. Hiemstra, K.F. Rabe, and D.R. Dorscheid Initiation of apoptosis by actin cytoskeletal derangement in human airway epithelial cells Am. J. Respir. Cell Mol. Biol. 24 2001 282 294
42. S. Vetterkind, M. Boosen, K.H. Scheidtmann, and U. Preuss Ectopic expression of Par-4 leads to apoptosis induction in CNS tumor cell lines Int. J. Oncol. 26 2005 159 168
43. R. Jacob, M. Heine, M. Alfalah, and H.Y. Naim Distinct cytoskeletal tracks direct individual vesicle populations to the apical membrane of epithelial cells Curr. Biol. 13 2003 607 612
44. E. Müller, and K.H. Scheidtmann Purification and characterization of a protein kinase which is activated by SV40 large T-antigen and phosphorylates the tumor suppressor protein p53 Oncogene 10 1995 1175 1185
45. T.M. Olson, S. Illenberger, N.Y. Kishimoto, S. Huttelmaier, M.T. Keating, and B.M. Jockusch Metavinculin mutations alter actin interaction in dilated cardiomyopathy Circulation 105 2002 431 437
46. J.A. Spudich, and S. Watt The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin J. Biol. Chem. 246 1971 4866 4871
47. M.M. Bradford A rapid and sensitive method for quantification of microgram quantities of protein utilizing the prinziple of protein-dye binding Anal. Biochem. 72 1976 248 254
48. R. Pollack, M. Osborn, and K. Weber Patterns of organization of actin and myosin in normal and transformed cultured cells Proc. Natl. Acad. Sci. U. S. A. 72 1975 994 998
49. S.C. Hsu, F. Kirschenbaum, J. Miller, B. Cordell, and J.V. McCarthy Structural and functional characterization of the upstream regulatory region of the human gene encoding prostate apoptosis response factor-4 Gene 295 2002 109 116
50. D. Kulms, H. Dussmann, B. Poppelmann, S. Stander, A. Schwarz, and T. Schwarz Apoptosis induced by disruption of the actin cytoskeleton is mediated via activation of CD95 (Fas/APO-1) Cell Death Differ. 9 2002 598 608
51. M. Bando, Y. Miyake, M. Shiina, M. Wachi, K. Nagai, and T. Kataoka Actin cytoskeleton is required for early apoptosis signaling induced by anti-Fas antibody but not Fas ligand in murine B lymphoma A20 cells. PG- Biochem. Biophys. Res. Commun. 290 2002 268 274
52. M. Chakraborty, S.G. Qiu, K.M. Vasudevan, and V.M. Rangnekar Par-4 drives trafficking and activation of Fas and Fasl to induce prostate cancer cell apoptosis and tumor regression Cancer Res. 61 2001 7255 7263
53. M. Bergmann, N. Kukoc-Zivojnov, K.U. Chow, B. Trepohl, D. Hoelzer, E. Weidmann, P.S. Mitrou, and S. Boehrer Prostate apoptosis response gene-4 sensitizes neoplastic lymphocytes to CD95-induced apoptosis Ann. Hematol. 83 2004 646 653
54. J.C. Mills, N.L. Stone, J. Erhardt, and R.N. Pittman Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation J. Cell Biol. 140 1998 627 636
55. M. Murata-Hori, F. Suizu, T. Iwasaki, A. Kikuchi, and H. Hosoya ZIP kinase identified as a novel myosin regulatory light chain kinase in HeLa cells FEBS Lett. 451 1999 81 84
56. J.C. Kuo, J.R. Lin, J.M. Staddon, H. Hosoya, and R.H. Chen Uncoordinated regulation of stress fibers and focal adhesions by DAP kinase J. Cell Sci. 116 2003 4777 4790
57. S. Komatsu, and M. Ikebe ZIP kinase is responsible for the phosphorylation of myosin II and necessary for cell motility in mammalian fibroblasts J. Cell Biol. 165 2004 243 254
58. M.L. Coleman, E.A. Sahai, M. Yeo, M. Bosch, A. Dewar, and M.F. Olson Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I Nat. Cell Biol. 3 2001 339 345
59. I. Petrache, K. Birukov, A.L. Zaiman, M.T. Crow, H. Deng, R. Wadgaonkar, L.H. Romer, and J.G. Garcia Caspase-dependent cleavage of myosin light chain kinase (MLCK) is involved in TNF-alpha-mediated bovine pulmonary endothelial cell apoptosis FASEB J. 17 2003 407 416
60. M. Sebbagh, C. Renvoize, J. Hamelin, N. Riche, J. Bertoglio, and J. Breard Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing Nat. Cell Biol. 3 2001 346 352
61. R.S. Fredricksen, and C.A. Swenson Relationship between stability and function for isolated domains of troponin C Biochemistry 35 1996 14012 14026