Repression of the antiapoptotic molecule galectin-3 by homeodomain- interacting protein kinase 2-activated p53 is required for p53-induced apoptosis

Molecular and Cellular Biology

Volumn 26, Issue 12, 2006, Pages 4746-4757

  Cecchinelli, Barbara ^a   Lavra, Luca ^b,f   Rinaldo, Cinzia ^a   Iacovelli, Stefano ^a   Gurtner, Aymone ^a   Gasbarri, Alessandra ^c   Ulivieri, Alessandra ^b,f   Del Prete, Fabrizio ^c   Trovato, Maria ^d   Piaggio, Giulia ^a   Bartolazzi, Armando ^c,e   Soddu, Silvia ^a   Sciacchitano, Salvatore ^b,f,g  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b FATEBENEFRATELLI HOSPITAL   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF MESSINA   (Italy)

^e KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

^g CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GALAPTIN; GALECTIN 3; HOMEODOMAIN INTERACTING PROTEIN KINASE 2; PROTEIN P53; SERINE;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR GROWTH;

ANIMALS; APOPTOSIS; BASE SEQUENCE; CARRIER PROTEINS; CELL LINE; DNA, COMPLEMENTARY; GALECTIN 3; GALECTINS; HUMANS; MICE; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT PROTEINS; SERINE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 33745020886     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00959-05     Document Type: Article

References (61)

1. Akahani, S., P. Nangia-Makker, H. Inohara, H.-R. Kim, and A. Raz. 1997. Galectin-3: a novel antiapoptotic molecule with a functional BH1 (NWGR) domain of Bcl-2 family. Cancer Res. 57:5272-5276.
2. Appella, E., and C. W. Anderson. 2000. Signaling to p53: breaking the post-translational modification code. Pathol. Biol. 48:227-245.
3. Ashcroft, M., M. H. Kubbutat, and K. H. Vousden. 1999. Regulation of p53 function and stability by phosphorylation. Mol. Cell. Biol. 19:1751-1758.
4. Bacchetti, S., and F. Graham. 1993. Inhibition of cell proliferation by an adenovirus vector expressing the human wild type p53 protein. Int. J. Oncol. 3:781-788.
5. Barondes, S. H., V. Castronovo, D. N. Cooper, R. D. Cummings, K. Drickamer, T. Feizi, M. A. Gitt, J. Hirabayashi, C. Hughes, K. Kasai, et al. 1994. Galectins: a family of animal beta-galactoside-binding lectins. Cell 76:597-598.
6. Bartolazzi, A., A. Gasbarri, M. Papotti, G. Bussolati, T. Lucante, A. Khan, H. Inohara, F. Marandino, F. Orlandi, A. Vecchione, R. Tecce, and O. Larsson. 2001. Application of an immunodiagnostic method for improving the preoperative diagnosis of nodular thyroid lesions. Lancet 357:1644-1650.
7. Boyd, K. E., J. Wells, J. Gutman, S. M. Bartley, and P. J. Farnham. 1998. c-Myc target gene specificity is determined by a post-DNA-binding mechanism. Proc. Natl. Acad. Sci. USA 95:13887-13892.
8. Brummelkamp, T. R., R. Bernards, and R. Agami. 2002. A system for stable expression of short interfering RNAs in mammalian cells. Science 296:550-553.
9. Bulavin, D. V., S. Saito, M. C. Hollander, C. W. Anderson, E. Appella, and A. J. Fornace, Jr. 1999. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J. 18:6845-6854.
10. Bunz, F., A. Dutriaux, C. Lengauer, T. Waldman, S. Zhou, J. P. Brown, J. M. Sedivy, K. W. Kinzler, and B. Vogelstein. 1998. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282:1497-1501.
11. Capponcelli, S., S. Fontanesi, E. Pedrini, M. A. Cerone, V. Corti, M. Alessio, A. Bachi, S. Soddu, D. Ribatti, P. Picci, L. J. Helman, G. Cantelli-Forti, and L. Sangiorgi. 2005. Evaluation of the molecular mechanisms involved in the gain of function of a Li-Fraumeni TP53 mutation. Hum. Mut. 26:94-103.
12. Cecchinelli, B., A. Porrello, C. Lazzari, A. Gradi, G. Bossi, M. D'Angelo, A. Sacchi, S. Soddu. Ser58 of mouse p53 is the homologue of human Ser46 and is phosphorylated by HIPK2 in apoptosis. Cell Death Differ., in press.
13. Choi, C. Y., Y. O. Kim, H. J. Kwon, and Y. Kim. 1999. The homeodomain protein NK-3 recruits Groucho and a histone deacetylase complex to repress transcription. J. Biol. Chem. 274:33194-33197.
14. Dagher, S. F., J. L. Wang, and R. J. Patterson. 1995. Identification of galectin-3 as a factor in pre-mRNA splicing. Proc. Natl. Acad. Sci. USA 92:1213-1217.
15. Di Stefano, V., G. Blandino, A. Sacchi, S. Soddu, and G. D'Orazi. 2004. HIPK2 neutralizes MDM2 inhibition rescuing p53 transcriptional activity and apoptotic function. Oncogene 23:5185-5192.
16. Di Stefano, V., C. Rinaldo, A. Sacchi, S. Soddu, and G. D'Orazi. 2004. Homeodomain-interacting protein kinase-2 activity and p53 phosphorylation are critical events for cisplatin-mediated apoptosis. Exp. Cell Res. 293:311-320.
17. Di Stefano, V., S. Soddu, A. Sacchi, and G. D'Orazi. 2005. HIPK2 contributes to PCAF-mediated p53 acetylation and selective transactivation of p21(Wafl) after nonapoptotic DNA damage. Oncogene 24:5431-5442.
18. D'Orazi, G., B. Cecchinelli, T. Bruno, I. Manni, Y. Higashimoto, S. Saito, M. Gostissa, S. Coen, A. Maschetti, G. Del Sal, G. Piaggio, M. Fanciulli, E. Appella, and S. Soddu. 2002. Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat. Cell Biol. 4:11-19.
19. el-Deiry, W. S. 1998. Regulation of p53 downstream genes. Semin. Cancer Biol. 8:345-357.
20. Frasca, F., V. Vella, A. Aloisi, A. Mandarine, E. Mazzon, R. Vigneri, and P. Vigneri. 2003. p73 tumor-suppressor activity is impaired in human thyroid cancer. Cancer Res. 63:5829-5837.
21. Gaudin, J. C., M. Monsigny, and A. Legrand. 1997. Modulation of the expression of the rabbit galectin-3 gene by p53 and c-Ha-ras proteins and PMA. Glycobiology 7:1089-1098.
22. Germain, M., E. B. Affar, D. D'Amours, V. M. Dixit, G. S. Salvesen, and G. G. Poirier. 1999. Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J. Biol. Chem. 274:28379-28384.
23. Gong, H. C., Y. Honjo, P. Nangia-Makker, V. Hogan, N. Mazurak, R. S. Bresalier, and A. Raz. 1999. The NH2 terminus of galectin-3 governs cellular compartmentalization and functions in cancer cells. Cancer Res. 59:6239-6245.
24. 23a. Guittant, M., S. Charpentier, T. Normand, M. Dubois, J. Raimond, and A. Legrand. 2001. Identification of an integral gene to the human galectin-3 gene with two different overlapping reading frames that do not encode galectin-3. J. Biol. Chem. 276:2652-2657.
25. Hainaut, P., and M. Hollstein. 2000. p53 and human cancer: the first ten thousand mutations. Adv. Cancer Res. 77:81-137.
26. Ho, J., and S. Benchimol. 2003. Transcriptional repression mediated by the p53 tumour suppressor. Cell Death Differ. 4:404-408.
27. Hofmann, T. G., A. Moller, H. Sirma, H. Zentgraf, Y. Taya, W. Droge, H. Will, and M. L. Schmitz. 2002. Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat. Cell Biol. 4:1-10.
28. Hsu, D. K., R. Y. Yang, Z. Pan, L. Yu, D. R. Salomon, W. P. Fung-Leung, and F. T. Liu. 2000. Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses. Am. J. Pathol. 156:1073-1083.
29. 2/M promoters. Mol. Cell. Biol. 25:3737-3751.
30. Ito, T., T. Seyama, T. Mizuno, N. Tsuyama, T. Hayashi, Y. Hayashi, K. Dohi, N. Namamura, and M. Akiyama. 1992. Unique association of p53 mutations with undifferentiated but not with differentiated carcinomas of the thyroid gland. Cancer Res. 52:1369-1371.
31. Kadrofske, M., K. P. Openo, and J. L. Wang. 1998. The human LGALS3 (galectin-3) gene: determination of the gene structure and functional characterization of the promoter. Arch. Biochem. Biophys. 349:7-20.
32. Kannan, K., N. Amariglio, G. Rechavi, J. Jakob-Hirsch, I. Kela, N. Kaminski, G. Getz, E. Domany, and D. Givol. 2001a. DNA microarrays identification of primary and secondary target genes regulated by p53. Oncogene 20:2225-2234.
33. Kannan, K., N. Kaminski, G. Rechavi, J. Jakob-Hirsch, N. Amariglio, D. Givol. 2001b. DNA microarray analysis of genes involved in p53 mediated apoptosis: activation of Apaf-1. Oncogene 20:3449-3455.
34. Kim, E.-J., J.-S. Park, and S.-J. Um. 2002. Identification and characterization of HIPK2 interacting with p73 and modulating functions of the p53 family in vivo. J. Biol. Chem. 277:32020-32028.
35. Kim, H. R., H. M. Lin, H. Bilirian, and A. Raz. 1999. Cell cycle arrest and inhibition of anoikis by galectin-3 in human breast epithelial cells. Cancer Res. 59:4148-4154.
36. Kim, Y. H., C. Y. Choi, S. J. Lee, M. A. Conti, and Y. Kim. 1998. Homeodomain-interacting protein kinases, a novel family of co-repressors for homeodomain transcription factors. J. Biol. Chem. 273:25875-25879.
37. Kuwabara, I., and F. T. Liu. 1996. Galectin-3 promotes adhesion of human neutrophils to laminin. J. Immunol. 156:3939-3944.
38. Liu, F. T., R. J. Patterson, J. L. Wang. 2002. Intracellular functions of galectins. Biochim. Biophys. Acta 1572:263-273.
39. Liu, F. T., and G. A. Rabinovich. 2005. Galectins as modulators of tumour progression. Nat. Rev. Cancer 5:29-41.
40. Lloyd, R. V. 2001. Distinguishing benign from malignant thyroid lesions: galectin-3 as the latest candidate. Endrocr. Pathol. 12:255-257.
41. Marchetti, A., F. Barassi, C. Martella, A. Chella, S. Salvatore, A. Castrataro, F. Mucilli, R. Sacco, and F. Buttitta. 2004. Down-regulation of high in normal-1 (HIN-1) is a frequent event in stage I non-small cell lung cancer and correlates with poor clinical outcome. Clin. Cancer Res. 10:1338-1344.
42. Michalovitz, D., O. Halevy, and M. Oren. 1990. Conditional inhibition of transformation and of cell proliferation by a temperature-sensitive mutant of p53. Cell 62:671-680.
43. Moller, A., H. Sirma, T. G. Hofmann, S. Rueffer, E. Klimczak, W. Droge, H. Will, and M. L. Schmitz. 2003. PML is required for homeodomain-interacting protein kinase 2 (HIPK2)-mediated p53 phosphorylation and cell cycle arrest but is dispensable for the formation of HIPK domains. Cancer Res. 63:4310-4314.
44. Oda, K., H. Arakawa, T. Tanaka, K. Matsuda, C. Tanikawa, T. Mori, H. Nishimori, K. Tamai, T. Tokino, Y. Nakamura, and Y. Taya. 2000. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102:849-862.
45. Pierantoni, G. M., A. Bulfone, F. Pentimalli, M. Fedele, R. Iuliano, M. Santoro, L. Chiariotti, A. Ballabio, and A. Fusco. 2002. The homeodomain-interacting protein kinase 2 gene is expressed late in embryogenesis and preferentially in retina, muscle, and neural tissues. Biochem. Biophys. Res. Commun. 290:942-947.
46. Porrello, A., M. A. Cerone, S. Coen, A. Gurtner, G. Fontemaggi, L. Cimino, G. Piaggio, A. Sacchi, and S. Soddu. 2000. p53 regulates myogenesis by triggering the differentiation activity of pRb. J. Cell Biol. 151:1295-1303.
47. Raimond, J., F. Rouleux, M. Monsigny, and A. Legrand. 1995. The second intron of the human galectin-3 gene has a strong promoter activity down-regulated by p53. FEES Lett. 363:165-169.
48. Saito, S., A. A. Goodarzi, Y. Higashimoto, Y. Noda, S. P. Lees-Miller, E. Appella, and C. W. Anderson. 2002. ATM mediates phosphorylation at multiple p53 sites, including Ser(46), in response to ionizing radiation. J. Biol. Chem. 277:12491-12494.
49. Schmitt, C. A., J. S. Fridman, M. Yang, E. Baranov, R. M. Hoffman, and S. W. Lowe. 2002. Dissecting p53 tumor suppressor functions in vivo. Cancer Cell 1:289.
50. Sciacchitano, S., A. Orecchio, L. Lavra, S. Misiti, A. Giacchini, M. Zani, D. Danese, A. Gurtner, S. Soddu, U. Di Mario, and M. Andreoli. 2002. Cloning of the mouse insulin receptor substrate-3 (mIRS-3) promoter, and its regulation by p53. Mol. Endocrinol. 16:1577-1589.
51. Takenaka, Y., T. Fukumori, T. Yoshii, N. Oka, H. Inohara, H. R. Kim, R. S. Bresalier, and A. Raz. 2004. Nuclear export of phosphorylated galectin-3 regulates its antiapoptotic activity in response to chemotherapeutic drugs. Mol. Cell. Biol. 24:4395-4406.
52. Vousden, K. H. 2000. p53: death star. Cell 103:691-694.
53. Wang, Y., K. M. Debatin, and H. Hug. 2001. H1PK2 overexpression leads to stabilization of p53 protein and increased p53 transcriptional activity by decreasing Mdm2 protein levels. BMC Mol. Biol. 2:8-16.
54. Yang, R. Y., D. K. Hsu, and F. T. Liu. 1996. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc. Natl. Acad. Sci. USA 93:6737-6742.
55. Yang, R. Y., and F. T. Liu. 2003. Galectins in cell growth and apoptosis. Cell. Mol. Life Sci. 60:267-276.
56. Yano, Y., N. Uematsu, T. Yashiro, H. Hara, E. Ueno, M. Miwa, G. Tsujimoto, Y. Aiyoshi, and K. Uchida. 2004. Gene expression profiling identifies platelet-derived growth factor as a diagnostic molecular marker for papillary thyroid carcinoma. Clin. Cancer Res. 10:2035-2043.
57. Yoshii, T., T. Fukumori, Y. Honjo, H. Inohara, H. R. Kim, and A. Raz. 2002. Galectin-3 phosphorylation is required for its anti-apoptotic function and cell cycle arrest. J. Biol. Chem. 277:6852-6857.
58. Yoshii, T., H. Inohara, Y. Takenaka, Y. Honjo, S. Akahani, T. Nomura, A. Raz, and T. Kubo. 2001. Galectin-3 maintains the transformed phenotype of thyroid papillary carcinoma cells. Int. J. Oncol. 18:787-792.
59. Yu, F., R. L. Finley, Jr., A. Raz, and H.-R. Kim. 2002. Galectin-3 translocates to the perinuclear membranes and inhibits cytochrome c release from the mitochondria. J. Biol. Chem. 277:15819-15827.
60. Zhang, Q., Y. Yoshimatsu, J. Hildebrand, S. M. Frisch, and R. H. Goodman. 2003. Homeodomain interacting protein kinase 2 promotes apoptosis by down-regulating the transcriptional corepressor CtBP. Cell 115:177-186.
61. Zhao, R., G. Kurt, M. Murphy, Y. Yin, D. Notterman, W. H. Hoffman, E. Tom, D. H. Mack, and A. J. Levine. 2000. Analysis of p53-regulated gene expression patterns using oligonucleotide arrays. Genes Dev. 14:981-993.