The cyclin-dependent kinase inhibitor p16INK4a physically interacts with transcription factor Sp1 and cyclin-dependent kinase 4 to Transactivate MicroRNA-141 and MicroRNA-146b-5p spontaneously and in response to ultraviolet light-induced DNA Damage

Journal of Biological Chemistry

Volumn 288, Issue 49, 2013, Pages 35511-35525

  Al Khalaf, Huda H ^a,b   Mohideen, Peer ^a   Nallar, Shreeram C ^c   Kalvakolanu, Dhananjaya V ^c   Aboussekhra, Abdelilah ^a  

^a KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^b KING ABDULAZIZ CITY FOR SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN-DEPENDENT KINASE; CYCLIN-DEPENDENT KINASE INHIBITORS; DNA DAMAGES; LIGHT-INDUCED; MICRORNAS; P16INK4A; TRANSCRIPTIONAL ACTIVITY; UP-REGULATION;

ENZYME INHIBITION; TRANSCRIPTION FACTORS;

RNA;

ANKYRIN; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE INHIBITOR 2A; MESSENGER RNA; MICRORNA; MICRORNA 141; MICRORNA 146B; PROTEIN P16; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CYCLE REGULATION; COMPLEX FORMATION; CONTROLLED STUDY; DNA DAMAGE; EXPRESSED SEQUENCE TAG; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENOTOXICITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR MECHANICS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; RADIATION INJURY; REGULATORY MECHANISM; RNA TRANSCRIPTION; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ULTRAVIOLET RADIATION; UPREGULATION;

PROTEIN COMPLEXES; PROTEIN-DNA INTERACTION; SHRNA; SIGNALING; TUMOR SUPPRESSOR GENE;

BASE SEQUENCE; CELL CYCLE; CELL LINE; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA DAMAGE; HUMANS; MICRORNAS; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA STABILITY; SP1 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION; ULTRAVIOLET RAYS;

EID: 84890296289     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.512640     Document Type: Article

References (51)

1. Koh, J., Enders, G. H., Dynlacht, B. D., and Harlow, E. (1995) Tumourderived p16 alleles encoding proteins defective in cell-cycle inhibition. Nature 375, 506-510
2. Lukas, J., Parry, D., Aagaard, L., Mann, D. J., Bartkova, J., Strauss, M., Peters, G., and Bartek, J. (1995) Retinoblastoma-protein-dependent cellcycle inhibition by the tumour suppressor p16. Nature 375, 503-506
3. Sherr, C. J. (2001) The INK4a/ARF network in tumour suppression. Nat. Rev. Mol. Cell Biol. 2, 731-737
4. Serrano, M., Hannon, G. J., and Beach, D. (1993)Anew regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 366, 704-707
5. Giacinti, C., and Giordano, A. (2006) RB and cell cycle progression. Oncogene 25, 5220-5227
6. Shapiro, G. I., Edwards, C. D., Ewen, M. E., and Rollins, B. J. (1998) p16ink4a participates in a G1 arrest checkpoint in response to DNA damage. Mol. Cell. Biol. 18, 378-387
7. Alcorta, D. A., Xiong, Y., Phelps, D., Hannon, G., Beach, D., and Barrett, J. C. (1996) Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 93, 13742-13747
8. Di Micco, R., Fumagalli, M., Cicalese, A., Piccinin, S., Gasparini, P., Luise, C., Schurra, C., Garre', M., Nuciforo, P. G., Bensimon, A., Maestro, R., Pelicci, P. G., and d'Adda di Fagagna, F. (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444, 638-642
9. Chavey, C., Bibeau, F., Gourgou-Bourgade, S., Burlinchon, S., Boissière, F., Laune, D., Roques, S., and Lazennec, G. (2007) Oestrogen receptor negative breast cancers exhibit high cytokine content. Breast Cancer Res. 9, R15
10. Al-Mohanna, M. A., Manogaran, P. S., Al-Mukhalafi, Z.,AAl-Hussein, K., and Aboussekhra, A. (2004) The tumor suppressor p16(INK4a) gene is a regulator of apoptosis induced by ultraviolet light and cisplatin. Oncogene 23, 201-212
11. Ruas, M., and Peters, G. (1998) The p16INK4a/CDKN2A tumor suppressor and its relatives. Biochim. Biophys. Acta 1378, F115-F177
12. Rocco, J. W., and Sidransky, D. (2001) p16(MTS-1/CDKN2/INK4a) in cancer progression. Exp. Cell Res. 264, 42-55
13. Romagosa, C., Simonetti, S., López-Vicente, L., Mazo, A., Lleonart, M. E., Castellvi, J., and Ramon y Cajal, S. (2011) p16(Ink4a) overexpression in cancer: a tumor suppressor gene associated with senescence and highgrade tumors. Oncogene 30, 2087-2097
14. Witkiewicz, A. K., Knudsen, K. E., Dicker, A. P., and Knudsen, E. S. (2011) The meaning of p16(ink4a) expression in tumors: functional significance, clinical associations and future developments. Cell Cycle 10, 2497-2503
15. Souza-Rodrígues, E., Estanyol, J. M., Friedrich-Heineken, E., Olmedo, E., Vera, J., Canela, N., Brun, S., Agell, N., Hübscher, U., Bachs, O., and Jaumot, M. (2007) Proteomic analysis of p16ink4a-binding proteins. Proteomics 7, 4102-4111
16. Sun, P., Nallar, S. C., Raha, A., Kalakonda, S., Velalar, C. N., Reddy, S. P., and Kalvakolanu, D. V. (2010) GRIM-19 and p16(INK4a) synergistically regulate cell cycle progression and E2F1-responsive gene expression. J. Biol. Chem. 285, 27545-27552
17. Vernell, R., Helin, K., and Müller, H. (2003) Identification of target genes of the p16INK4A-pRB-E2F pathway. J. Biol. Chem. 278, 46124-46137
18. Al-Khalaf, H. H., Colak, D., Al-Saif, M., Al-Bakheet, A., Hendrayani, S. F., Al-Yousef, N., Kaya, N., Khabar, K. S., and Aboussekhra, A. (2011) p16(INK4a) positively regulates cyclin D1 and E2F1 through negative control of AUF1. PLoS One 6, e21111
19. Chien, W. W., Domenech, C., Catallo, R., Kaddar, T., Magaud, J. P., Salles, G., and Ffrench, M. (2011) Cyclin-dependent kinase 1 expression is inhibited by p16(INK4a) at the post-transcriptional level through the microRNA pathway. Oncogene 30, 1880-1891
20. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
21. Koturbash, I., Zemp, F. J., Pogribny, I., and Kovalchuk, O. (2011) Small molecules with big effects: the role of the microRNAome in cancer and carcinogenesis. Mutat. Res. 722, 94-105
22. Farazi, T. A., Spitzer, J. I., Morozov, P., and Tuschl, T. (2011) miRNAs in human cancer. J. Pathol. 223, 102-115
23. Lovat, F., Valeri, N., and Croce, C. M. (2011) MicroRNAs in the pathogenesis of cancer. Semin. Oncol. 38, 724-733
24. McConnell, B. B., Gregory, F. J., Stott, F. J., Hara, E., and Peters, G. (1999) Induced expression of p16(INK4a) inhibits both CDK4- and CDK2-associated kinase activity by reassortment of cyclin-CDK-inhibitor complexes. Mol. Cell. Biol. 19, 1981-1989
25. Taganov, K. D., Boldin, M. P., Chang, K. J., and Baltimore, D. (2006) NF-B-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U.S.A. 103, 12481-12486
26. Al-Mohanna, M. A., Al-Khalaf, H. H., Al-Yousef, N., and Aboussekhra, A. (2007) The p16INK4a tumor suppressor controls p21WAF1 induction in response to ultraviolet light. Nucleic Acids Res. 35, 223-233
27. Bond, J. A., Haughton, M. F., Rowson, J. M., Smith, P. J., Gire, V., Wynford- Thomas, D., and Wyllie, F. S. (1999) Control of replicative life span in human cells: barriers to clonal expansion intermediate betweenM1senescence and M2 crisis. Mol. Cell. Biol. 19, 3103-3114
28. Al-Khalaf, H. H., and Aboussekhra, A. (2013) p16(INK4A) Positively regulates p21(WAF1) expression by suppressing AUF1-dependent mRNA decay. PLoS One 8, e70133
29. Oleaga, C., Welten, S., Belloc, A., Solé, A., Rodriguez, L., Mencia, N., Selga, E., Tapias, A., Noé, V., and Ciudad, C. J. (2012) Identification of novel Sp1 targets involved in proliferation and cancer by functional genomics. Biochem. Pharmacol. 84, 1581-1591
30. Tapias, A., Ciudad, C. J., Roninson, I. B., and Noé, V. (2008) Regulation of Sp1 by cell cycle related proteins. Cell Cycle 7, 2856-2867
31. Xu, Z., Xiao, S. B., Xu, P., Xie, Q., Cao, L., Wang, D., Luo, R., Zhong, Y., Chen, H. C., and Fang, L. R. (2011) miR-365, a novel negative regulator of interleukin-6 gene expression, is cooperatively regulated by Sp1 and NF-B. J. Biol. Chem. 286, 21401-21412
32. Wouters, M. D., van Gent, D. C., Hoeijmakers, J. H., and Pothof, J. (2011) MicroRNAs, the DNA damage response and cancer. Mutat. Res. 717, 54-66
33. Al-Khalaf, H. H., Hendrayani, S. F., and Aboussekhra, A. (2011) The Atr protein kinase controls UV-dependent up-regulation of p16INK4A through inhibition of Skp2-related polyubiquitination/degradation. Mol. Cancer Res. 9, 311-319
34. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., and Brabletz, T. (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582-589
35. Katakowski, M., Zheng, X., Jiang, F., Rogers, T., Szalad, A., and Chopp, M. (2010) MiR-146b-5p suppresses EGFR expression and reduces in vitro migration and invasion of glioma. Cancer Invest. 28, 1024-1030
36. Zhao, J. L., Rao, D. S., Boldin, M. P., Taganov, K. D., O'Connell, R. M., and Baltimore, D. (2011) NF-B dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc. Natl. Acad. Sci. U.S.A. 108, 9184-9189
37. Hurst, D. R., Edmonds, M. D., Scott, G. K., Benz, C. C., Vaidya, K. S., and Welch, D. R. (2009) Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res. 69, 1279-1283
38. Mansilla, S., and Portugal, J. (2008) Sp1 transcription factor as a target for anthracyclines: effects on gene transcription. Biochimie 90, 976-987
39. Foti, D., Iuliano, R., Chiefari, E., and Brunetti, A. (2003) A nucleoprotein complex containing Sp1, C/EBP-, and HMGI-Y controls human insulin receptor gene transcription. Mol. Cell. Biol. 23, 2720-2732
40. Ortega, S., Malumbres, M., and Barbacid, M. (2002) Cyclin D-dependent kinases, INK4 inhibitors and cancer. Biochim. Biophys. Acta 1602, 73-87
41. Li, L., and Davie, J. R. (2010) The role of Sp1 and Sp3 in normal and cancer cell biology. Ann. Anat. 192, 275-283
42. Hsu, T. I., Wang, M. C., Chen, S. Y., Yeh, Y. M., Su, W. C., Chang, W. C., and Hung, J. J. (2012) Sp1 expression regulates lung tumor progression. Oncogene 31, 3973-3988
43. Arslan, A. A., Silvera, D., Arju, R., Giashuddin, S., Belitskaya-Levy, I., Formenti, S. C., and Schneider, R. J. (2012) Atypical ezrin localization as a marker of locally advanced breast cancer. Breast Cancer Res. Treat. 134, 981-988
44. Sabir, M., Baig, R. M., Mahjabeen, I., and Kayani, M. A. (2012) Novel germline CDK4 mutations in patients with head and neck cancer. Hered. Cancer Clin. Pract. 10, 11
45. Negrini, M., Nicoloso, M. S., and Calin, G. A. (2009) MicroRNAs and cancer-new paradigms in molecular oncology. Curr. Opin. Cell Biol. 21, 470-479
46. Bhaumik, D., Scott, G. K., Schokrpur, S., Patil, C. K., Campisi, J., and Benz, C. C. (2008) Expression of microRNA-146 suppresses NF-B activity with reduction of metastatic potential in breast cancer cells. Oncogene 27, 5643-5647
47. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., Vadas, M. A., Khew-Goodall, Y., and Goodall, G. J. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593-601
48. Pothof, J., Verkaik, N. S., van IJcken, W., Wiemer, E. A., Ta, V. T., van der Horst, G. T., Jaspers, N. G., van Gent, D. C., Hoeijmakers, J. H., and Persengiev, S. P. (2009) MicroRNA-mediated gene silencing modulates the UV light-induced DNA-damage response. EMBO J. 28, 2090-2099
49. Tan, G., Shi, Y., and Wu, Z. H. (2012) MicroRNA-22 promotes cell survival uponUVradiation by repressing PTEN. Biochem. Biophys. Res. Commun. 417, 546-551
50. Zhou, X., Wang, G., and Zhang, W. (2007) UV-B responsive microRNA genes in Arabidopsis thaliana. Mol. Syst. Biol. 3, 103
51. Tan, G., Niu, J., Shi, Y., Ouyang, H., and Wu, Z. H. (2012) NF-B-dependent microRNA-125b up-regulation promotes cell survival by targeting p38- upon ultraviolet radiation. J. Biol. Chem. 287, 33036-33047