Diverse roles of GADD45α in stress signaling

Current Protein and Peptide Science

Volumn 10, Issue 4, 2009, Pages 388-394

  Gao, Ming ^a   Guo, Ning ^a   Huang, Chuanshu ^b   Song, Lun ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

GADD45 ; Stress; Tumor progression; Tumor suppressor

Indexed keywords

GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45ALPHA; UNCLASSIFIED DRUG; SIGNAL PEPTIDE;

APOPTOSIS; CANCER INHIBITION; CARCINOGENESIS; CELL STRESS; CELL SURVIVAL; DNA REPAIR; GENETIC STABILITY; HUMAN; NONHUMAN; PROGNOSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TUMOR GROWTH; ANIMAL; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY;

MAMMALIA;

ANIMALS; CELL SURVIVAL; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASMS; SIGNAL TRANSDUCTION;

EID: 70349508867     PISSN: 13892037     EISSN: None     Source Type: Journal    
DOI: 10.2174/138920309788922216     Document Type: Review

References (55)

1. Lal, A.; Gorospe, M. Egad, more forms of gene regulation: the GADD45a story. Cell Cycle., 2006, 5, 1422-1425.
2. Hildesheim, J.; Fomace, A. J., Jr. Gadd45a: an elusive yet attractive candidate gene in pancreatic cancer. Clin. Cancer Res., 2002, 8, 2475-2479.
3. Zhan, Q. Gadd45a, a p53- and BRCA1 -regulated stress protein, in cellular response to DNA damage. Mutat. Res., 2005, 569, 133-143.
4. Hildesheim, J.; Bulavin, D. V.; Anver, M. R.; Alvord, W. G.; Hollander, M. C.; Vardanian, L.; Fornace, A. J., Jr. Gadd45a protects against UV irradiation-induced skin tumors, and promotes apoptosis and stress signaling via MAPK and p53. Cancer Res., 2002, 62, 7305-7315.
5. Yamasawa, K.; Nio, Y.; Dong, M.; Yamaguchi, K.; Itakura, M. Clinicopathological significance of abnormalities in Gadd45 expression and its relationship to p53 in human pancreatic cancer. Clin. Cancer Res., 2002, 8, 2563-2569.
6. Kettenhofen, R.; Hoppe, J.; Eberhard, G.; Seul, C.; Ko, Y.; Sachinidis, A. Regulation of Gadd45a mRNA expression in vascular smooth muscle under growth and stress conditions. Cell Signal., 2001, 13, 787-799.
7. Xiao, G.; Chicas, A.; Olivier, M.; Taya, Y.; Tyagi, S.; Kramer, F. R.; Bargonetti, J. A DNA damage signal is required for p53 to activate GADD45. Cancer Res., 2000, 60, 1711-1719.
8. Fan, W.; Jin, S.; Tong, T.; Zhao, H.; Fan, F.; Antinorc, M. J.; Rajasekamn, B.; Wu, M.; Zhan, Q. BRCA1 regulates GADD45 through its interactions with the OCT-1 and CAAT motifs. J. Biol. Chem., 2002, 277, 8061-8067.
9. Zhang, Y.; Bhatia, D.; Xia, H.; Castranova, V.; Shi, X.; Chen, F. Nucleolin links to arsenic-induced stabilization of GADD45 alpha mRNA. Nucleic Acids Res., 2006, 34, 485-495.
10. Jiang, H. Y.; Jiang, L.; Wek, R. C. The eukaryotic initiation factor-2 kinase pathway facilitates differential GADD45a expression in response to environmental stress. J. Biol. Chem., 2007, 282, 3755-3765.
11. Zhan, Q.; Antinore, M. J.; Wang, X. W.; Carrier, F.; Smith, M. L.; Harris, C. C.; Fornace, A. J., Jr. Association with Cdc2 and inhibition of Cdc2/Cyclin B1 kinase activity by the p53-regulated protein Gadd45. Oncogene, 1999, 18, 2892-2900.
12. Vairapandi, M.; Azam, N.; Balliet, A. G.; Hoffman, B.; Liebermann, D. A. Characterization of MyD118, Gadd45, and proliferating cell nuclear antigen (PCNA) interacting domains. PCNA impedes MyD118 AND Gadd45-mediated negative growth control. J. Biol. Chem., 2000, 275, 16810-16819.
13. Zhao, H.; Jin, S.; Antinore, M. J.; Lung, F. D.; Fan, F.; Blanck, P.; Roller, P.; Fornace, A. J.; Jr.; Zhan, Q. The central region of Gadd45 is required for its interaction with p21/WAF1. Exp. Cell Res., 2000, 258, 92-100.
14. Miyake, Z.; Takekawa, M.; Ge, Q.; Saito, H. Activation of MTK1/MEKK4 by GADD45 through induced N-C dissociation and dimerization-mediated trans autophosphorylation of the MTK1 kinase domain. Mol. Cell. Biol., 2007, 27, 2765-2776.
15. Kovalsky, O.; Lung, F. D.; Roller, P. P.; Fornace, A. J.; Jr. Oligomerization of human Gadd45a protein. J. Biol. Chem., 2001, 276, 39330-39339.
16. Hollander, M. C.; Sheikh, M. S.; Bulavin, D. V.; Lundgren, K.; Augeri-Henmueller, L.; Shehee, R.; Molinaro, T. A.; Kim, K. E.; Tolosa, E.; Ashwell, J. D.; Rosenberg, M. P.; Zhan, Q.; Fernandez-Salgnero, P. M.; Morgan, W. F.; Deng, C. X.; Fornace, A. J.; Jr. Genomic instability in Gadd45a-deficient mice. Nat. Genet., 1999, 23, 176-184.
17. Tront, J. S.; Hoffman, B.; Liebermann, D. A. Gadd45a suppresses Ras-driven mammary tumorigenesis by activation of c-Jun NH2-terminal kinase and p38 stress signaling resulting in apoptosis and senescence. Cancer Res., 2006, 66, 8448-8454.
18. Wang, X. W.; Zhan, Q.; Coursen, J. D.; Khan, M. A.; Kontny, H. U.; Yu, L.; Hollander, M. C.; O'Connor, P. M.; Fornace, A. J.; Jr.; Harris, C. C. GADD45 induction of a: G2/M cell cycle checkpoint. Proc. Natl. Acad. Sci. USA, 1999, 96, 3706-3711.
19. Song, L.; Li, J.; Zhang, D.; Liu, Z. G.; Ye, J.; Zhan, Q.; Shen, H. M.; Whiteman, M.; Huang, C. IKKbeta programs to turn on the GADD45alpha-MKK4-JNK apoptotic cascade specifically via p50 NF-kappaB in arsenite response. J. Cell Biol., 2006, 175, 607-617.
20. pHildesheim, J.; Salvador, J. M.; Hollander, M. C.; Fornace, A. J.; Jr. Casein kinase 2- and protein kinase A-regulated adenomatous polyposis coli and beta-catenin cellular localization is dependent on P38 MAPK. J. Biol. Chem., 2005, 280, 17221-17226.
21. Ji, J.; Liu, R.; Tong, T.; Song, Y.; Jin, S.; Wu, M.; Zhan, Q. Gadd45a regulates beta-catenin distribution and maintains cell-cell adhesion/ contact. Oncogene, 2007, 26, 6396-6405.
22. Gupta, M.; Gupta, S. K.; Hoffman, B.; Liebermann, D. A. Gadd45a and Gadd45b protect hematopoiotic cells from UV-induced apoptosis via distinct signaling pathways, including p38 activation and JNK inhibition. J. Biol. Chem., 2006, 281, 17552-17558.
23. Smith, G. B.; Mocarski, E. S. Contribution of GADD45 family members to cell death suppression by cellular Bcl-xL and cytomegalovirus vMIA. J. Virol., 2005, 79, 14923-14932.
24. Rai, K.; Huggins, I. J.; James, S. R.; Karpf, A. R.; Jones, D. A.; Cairns, B. R. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and GADD45. Cell, 2008, 135, 1201-1212.
25. Barreto, G.; Schafer, A.; Marhold, J.; Stach, D.; Swaminathan, S. K.; Handa, V.; Doderlein, G.; Maltry, N.; Wit, W., Lyko, F.; Niehrs, C. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature, 2007, 445, 671-675.
26. Schmitz, K. M.; Schmitt, N.; Hoffmann-Rohrer, U.; Schafer, A.; Grurrunt, I.; Mayer, C. TAF12 recruits Gadd45a and the nucleotide excision repair complex to the promoter of rRNA genes leading to active DNA demethylation. Mol. Cell, 2009, 33, 344-353.
27. Engel, N.; Tront, J. S.; Erinle, T.; Nguyen, N.; Latham, K. E.; Sapienza, C.; Hoffman, B.; Liebermann, D. A. Conserved DNA methylation in Gadd45a(-/-) mice. Epigenelics, 2009, 4, 2.
28. Jin, S. G.; Guo, C.; Pfeifer, G. P. GADD45A does not promote DNA demethylation. PLoS Genet., 2008, 4, e1000013.
29. Zhan, Q.; Chen, I. T.; Antinore, M. J.; Fornace, A. J.; Jr. Tumor suppressor p53 can participate in transcriptional induction of the GADD45 promoter in the absence of direct DNA binding. Mol. Cell Biol., 1998, 18, 2768-2778.
30. Thyss, R.; Virolle, V.; Imbert, V.; Peyron, J. F.; Aberdam, D.; Virolle, T. NF-kappaB/Egr-1/Gadd45 are sequentially activated upon UVB irradiation to mediate epidermal cell death. EMBO J., 2005, 24, 128-137.
31. Tran, H.; Brunet, A.; Grenier, J. M.; Datta, S. R.; Fornace, A. J.; Jr.; DiStefano, P. S.; Chiang, L. W.; Greenberg, M. E. DNA repair pathway stimulated by the foikhead transcription factor FOX03a through the Gadd45 protein. Science, 2002, 296, 530-534.
32. Daino, K.; Ichimura, S.; Nenoi, M. Both the basal transcriptional activity of the GADD45A gene and its enhancement after ionizing irradiation are mediated by AP-1 element. Biochim. Biophys. Acta, 2006, 1759, 458-469.
33. Zhang, D.; Song, L.; Li, J.; Wu, K.; Huang, C. Coordination of JNK1 and JNK2 is critical for GADD45alpha induction and its mediated cell apoptosis in arsenite responses. J. Biol. Chem., 2006, 281, 34113-34123.
34. Barsyte-Lovejoy, D.; Mao, D. Y.; Penn, L. Z. c-Myc represses the proximal promoters of GADD45a and GADD153 by a post-RNA polymerase II recruitment mechanism. Oncogene, 2004, 23, 3481-3486.
35. Yun, J.; Lee, W. H. Degradation of transcription repressor ZBRK1 through the ubiquitin-proteasome pathway relieves repression of Gadd45a upon DNA damage. Mol. Cell Biol., 2003, 23, 7305-7314.
36. Li, X.; Lee, Y. K.; Jeng, J. C.; Yen, Y.; Schultz, D. C.; Shih, H. M.; Ann, D. K. Role for KAP1 serine 824 phosphorylation and sumoylation/ desumoylation switch in regulating KAP1-mediated transcriptional repression. J. Biol. Chem., 2007, 282, 36177-36189.
37. Zhu, Q. S.; Ren, W.; Korchin, B.; Lahat, G.; Dicker, A.; Lu, Y.; Mills, G.; Pollock, R. E.; Lev, D. Soft tissue sarcoma cells are highly sensitive to AKT blockade: a role for p53-independent up-regulation of GADD45 alpha. Cancer Res., 2008, 68, 2895-2903.
38. Wang, W.; Huper, G.; Guo, Y.; Murphy, S. K.; Olson, J. A.; Jr.; Marks, J. R. Analysis of methylation-sensitive transcriptome identifies GADD45a as a frequently methylated gene in breast cancer. Oncogene, 2005, 24, 2705-2714.
39. Al-Romaih, K.; Sadikovic, B.; Yoshimoto, M.; Wang, Y.; Zielenska, M.; Squire, J. A. Decitabine-induced demethylation of 5′ CpG island in GADD45A leads to apoptosis in osteosarcoma cells. Neoplasia, 2008, 10, 471-480.
40. Lal, A.; Abdelmohsen, K.; Pullmann, R.; Kawai, T.; Galban, S.; Yang, X.; Brewer, G.; Gorospe, M. Posttranscriptional derepression of GADD45alpha by genotoxic stress. Mol. Cell, 2006, 22, 117-128.
41. Chang, Q.; Bhatia, D.; Zhang, Y.; Meighan, T.; Castranova, V.; Shi, X.; Chen, F. Incorporation of an internal ribosome entry site-dependent mechanism in arsenic-induced GADD45 alpha expression. Cancer Res., 2007, 67, 6146-6154.
42. Song, L.; Li, J.; Hu, M.; Huang, C. Both IKKalpha and IKKbeta are implicated in the arsenite-induced AP-1 transactivation correlating with cell apoptosis through NF-kappaB activity-independent manner. Exp. Cell Res., 2008, 314, 2187-2198.
43. Gao, H.; Jin, S.; Song, Y.; Fu, M.; Wang, M.; Liu, Z.; Wu, M.; Zhan, Q. B23 regulates GADD45a nuclear translocation and contributes to GADD45a-induced cell cycle G2-M arrest. J. Biol. Chem., 2005, 280, 10988-10996.
44. Hollander, M. C.; Fornace, A. J.; Jr. Genomic instability, centrosome amplification, cell cycle checkpoints and Gadd45a. Oncogene, 2002, 21, 6228-6233.
45. Shao, S.; Wang, Y.; Jin, S.; Song, Y.; Wang, X.; Fan, W.; Zhao, Z.; Fu, M.; Tong, T.; Dong, L.; Fan, F.; Xu, N.; Zhan, Q. Gadd45a interacts with aurora-A and inhibits its kinase activity. J. Biol. Chem., 2006, 281, 28943-28950.
46. Wang, X.; Wang, R. H.; Li, W.; Xu, X.; Hollander, M. C.; Fornace, A. J.; Jr.; Deng, C. X. Genetic interactions between Brca1 and Gadd45a in centrosome duplication, genetic stability, and neural tube closure. J. Biol. Chem., 2004, 279, 29606-29614.
47. Hollander, M. C.; Kovalsky, O.; Salvador, J. M.; Kim, K. E.; Patterson, A. D.; Haines, D. C.; Fornace, A. J.; Jr. Dimethylbenzanthracene carcinogenesis in Gadd45a-null mice is associated with decreased DNA repair and increased mutation frequency. Cancer Res., 2001, 61, 2487-2491.
48. Jackson, J. G.; Pereira-Smith, O. M. p53 is preferentially recruited to the promoters of growth arrest genes p21 and GADD45 during replicative senescence of normal human fibroblasts. Cancer Res., 2006, 66, 8356-8360.
49. Bulavin, D. V.; Kovalsky, O.; Hollander, M. C.; Fornace, A. J.; Jr. Loss of oncogenic H-ras-induced cell cycle arrest and p38 mitogen-activated protein kinase activation by disruption of Gadd45a. Mol. Cell Biol., 2003, 23, 3859-3871.
50. Jin, S.; Mazzacurati, L.; Zhu, X.; Tong, T.; Song, Y.; Shujuan, S.; Petrik, K. L.; Rajasekaran, B.; Wu, M.; Zhan, Q. Gadd45a contributes to p53 stabilization in response to DNA damage. Oncogene, 2003, 22, 8536-8540.
51. Tong, T.; Ji, J.; Jin, S.; Li, X.; Fan, W.; Song, Y.; Wang, M.; Liu, Z.; Wu, M.; Zhan, Q. Gadd45a expression induces Bim dissociation from the cytoskeleton and translocation to mitochondria. Mol. Cell Biol., 2005, 25,4488-4500.
52. Fayolle, C.; Pourchet, J.; de Fromentel, C. C.; Puisieux, A.; Dore, J. F.; Voeltzel, T. Gadd45a activation protects melanoma cells from ultraviolet B-induced apoptosis. J. Invest. Dermatol., 2008, 128, 196-202.
53. Klopp, A. H.; Jhingran, A.; Ramdas, L.; Story, M. D.; Broadus, R. R.; Lu, K. H.; Eifel, P. J.; Buchholz, T. A. Gene expression changes in cervical squamous cell carcinoma ffter initiation of chemoradiation and correlation with clinical outcome. Int. J. Radiat. Oncol. Biol. Phys., 2008, 71, 226-236.
54. Higashi, H.; Vallbohmer, D.; Warnecke-Eberz, U.; Hokita, S.; Xi, H.; Brabender, J.; Metzger, R.; Baldus, S. E.; Natsugoe, S.; Aikou, T.; Holscher, A. H.; Schneider, P. M. Down-regulation of Gadd45 expression is associated with tumor differentiation in non-small cell lung cancer. Anticancer Res., 2006, 26, 2143-2147.
55. Levine, A. J.; Hu, W.; Feng, Z. The P53 pathway: what questions remain to be explored? Cell Death Differ., 2006, 13, 1027-1036.