Structural and functional interactions of the prostate cancer suppressor protein NKX3.1 with topoisomerase I

Biochemical Journal

Volumn 453, Issue 1, 2013, Pages 125-136

  Song, Liang Nian ^a   Bowen, Cai ^a   Gelmann, Edward P ^a  

^a Columbia University ^*  (United States)

Author keywords

Camptothecin (CPT); DNA repair; Homeodomain; NK3 homeobox 1 (NKX3.1); Prostate cancer; Topoisomerase I

Indexed keywords

CAMPTOTHECIN; HOMEODOMAIN PROTEIN; TUMOR SUPPRESSOR PROTEIN;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; ATAXIA TELANGIECTASIA; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVE SITE; ENZYME RECONSTITUTION; HOMEOBOX; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE;

APOPTOSIS; CAMPTOTHECIN; CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; DNA TOPOISOMERASES, TYPE I; HOMEODOMAIN PROTEINS; HUMANS; MALE; PROSTATIC NEOPLASMS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 84879014958     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130012     Document Type: Article

References (40)

1. Bhatia-Gaur, R., Donjacour, A. A., Sciavolino, P. J., Kim, M., Desai, N., Norton, C. R., Gridley, T., Cardiff, R. D., Cunha, G. R., Abate-Shen, C. and Shen, M. M. (1999) Roles for Nkx3.1 in prostate development and cancer. Genes Dev. 13, 966-977 (Pubitemid 29200980)
2. Bowen, C., Bubendorf, L., Voeller, H. J., Slack, R., Willi, N., Sauter, G., Gasser, T. C., Koivisto, P., Lack, E. E., Kononen, J. et al. (2000) Loss of NKX3.1 expression in human prostate cancers correlates with tumor progression. Cancer Res. 60, 6111-6115
3. Asatiani, E., Huang, W. X., Wang, A., Rodriguez, O. E., Cavalli, L. R., Haddad, B. R. and Gelmann, E. P. (2005) Deletion, methylation, and expression of the NKX3.1 suppressor gene in primary human prostate cancer. Cancer Res. 65, 1164-1173 (Pubitemid 40270140)
4. Bethel, C. R., Faith, D., Li, X., Guan, B., Hicks, J. L., Lan, F., Jenkins, R. B., Bieberich, C. J. and De Marzo, A. M. (2006) Decreased NKX3.1 protein expression in focal prostatic atrophy, prostatic intraepithelial neoplasia, and adenocarcinoma: association with gleason score and chromosome 8p deletion. Cancer Res. 66, 10683-10690 (Pubitemid 44876963)
5. Kim, M. J., Bhatia-Gaur, R., Banach-Petrosky, W. A., Desai, N., Wang, Y., Hayward, S. W., Cunha, G. R., Cardiff, R. D., Shen, M. M. and Abate-Shen, C. (2002) Nkx3.1 mutant mice recapitulate early stages of prostate carcinogenesis. Cancer Res. 62, 2999-3004 (Pubitemid 34602384)
6. Bowen, C. and Gelmann, E. P. (2010) NKX3.1 activates cellular response to DNA damage. Cancer Res. 70, 3089-3097
7. Bowen, C., Stuart, A., Ju, J. H., Tuan, J., Blonder, J., Conrads, T. P., Veenstra, T. D. and Gelmann, E. P. (2007) NKX3.1 homeodomain protein binds to topoisomerase I and enhances its activity. Cancer Res. 67, 455-464 (Pubitemid 46192181)
8. Champoux, J. J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369-413
9. Koster, D. A., Croquette, V., Dekker, C., Shuman, S. and Dekker, N. H. (2005) Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature 434, 671-674 (Pubitemid 40488562)
10. Kingma, P. S. and Osheroff, N. (1998) The response of eukaryotic topoisomerases to DNA damage. Biochim. Biophys. Acta 1400, 223-232 (Pubitemid 28475106)
11. Simmons, D. T., Roy, R., Chen, L., Gai, D. and Trowbridge, P. W. (1998) The activity of topoisomerase I is modulated by large T antigen during unwinding of the SV40 origin. J. Biol. Chem. 273, 20390-20396 (Pubitemid 28377605)
12. Gai, D., Roy, R., Wu, C. and Simmons, D. T. (2000) Topoisomerase I associates specifically with simian virus 40 large-T-antigen double hexamer-origin complexes. J. Virol. 74, 5224-5232 (Pubitemid 30313863)
13. Pommier, Y. (2009) DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem. Rev. 109, 2894-2902
14. Andoh, T., Ishii, K., Suzuki, Y., Ikegami, Y., Kusunoki, Y., Takemoto, Y. and Okada, K. (1987) Characterization of a mammalian mutant with a camptothecin-resistant DNA topoisomerase I. Proc. Natl. Acad. Sci. U.S.A. 84, 5565-5569
15. Beidler, D. R. and Cheng, Y. C. (1995) Camptothecin induction of a time- and concentration-dependent decrease of topoisomerase I and its implication in camptothecin activity. Mol. Pharmacol. 47, 907-914
16. Fiorani, P., Bruselles, A., Falconi, M., Chillemi, G., Desideri, A. and Benedetti, P. (2003) Single mutation in the linker domain confers protein flexibility and camptothecin resistance to human topoisomerase I. J. Biol. Chem. 278, 43268-43275 (Pubitemid 37345947)
17. 729 in human topoisomerase I modulates anti-cancer drug resistance by altering protein domain communications as suggested by molecular dynamics simulations. Nucleic Acids Res. 36, 5645-5651
18. Frangioni, J. V. and Neel, B. G. (1993) Solubilization and purification of enzymatically active glutathione S -transferase (pGEX) fusion proteins. Anal. Biochem. 210,179-187 (Pubitemid 23147952)
19. Stewart, L., Ireton, G. C. and Champoux, J. J. (1997) Reconstitution of human topoisomerase I by fragment complementation. J. Mol. Biol. 269, 355-372 (Pubitemid 27267758)
20. Zheng, S. L., Ju, J. H., Chang, B. L., Ortner, E., Sun, J., Isaacs, S. D., Sun, J., Wiley, K. E., Liu, W., Zemedkun, M. et al. (2006) Germ-line mutation of NKX3.1 cosegregates with hereditary prostate cancer and alters the homeodomain structure and function. Cancer Res. 66, 69-77 (Pubitemid 43166011)
21. Gelmann, E. P., Steadman, D. J., Ma, J., Ahronovitz, N., Voeller, H. J., Swope, S., Abbaszadegan, M., Brown, K. M., Strand, K., Hayes, R. B. and Stampfer, M. J. (2002) Occurrence of NKX3.1 C154T polymorphism in men with and without prostate cancer and studies of its effect on protein function. Cancer Res. 62, 2654-2659 (Pubitemid 34462749)
22. Weiler, S., Gruschus, J. M., Tsao, D. H., Yu, L., Wang, L. H., Nirenberg, M. and Ferretti, J. A. (1998) Site-directed mutations in the vnd/NK-2 homeodomain. Basis of variations in structure and sequence-specific DNA binding. J. Biol. Chem. 273, 10994-11000 (Pubitemid 28204940)
23. Yang, Z. and Champoux, J. J. (2002) Reconstitution of enzymatic activity by the association of the cap and catalytic domains of human topoisomerase I. J. Biol. Chem. 277, 30815-30823 (Pubitemid 34970780)
24. Redinbo, M. R., Stewart, L., Kuhn, P., Champoux, J. J. and Hol, W. G. (1998) Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279, 1504-1513 (Pubitemid 28217069)
25. Laco, G. S., Collins, J. R., Luke, B. T., Kroth, H., Sayer, J. M., Jerina, D. M. and Pommier, Y. (2002) Human topoisomerase I inhibition: docking camptothecin and derivatives into a structure-based active site model. Biochemistry 41, 1428-1435 (Pubitemid 34112730)
26. Miao, Z. H., Player, A., Shankavaram, U., Wang, Y. H., Zimonjic, D. B., Lorenzi, P. L., Liao, Z. Y., Liu, H., Shimura, T., Zhang, H. L. et al. (2007) Nonclassic functions of human topoisomerase I: genome-wide and pharmacologic analyses. Cancer Res. 67,8752-8761 (Pubitemid 47437451)
27. Pommier, Y., Pourquier, P., Fan, Y. and Strumberg, D. (1998) Mechanism of action of eukaryotic DNA topoisomerase I and drugs targeted to the enzyme. Biochim. Biophys. Acta 1400, 83-105
28. Gilmour, D. S., Pflugfelder, G., Wang, J. C. and Lis, J. T. (1986) Topoisomerase I interacts with transcribed regions in Drosophila cells. Cell 44, 401-407 (Pubitemid 16043331)
29. Subramanian, D., Rosenstein, B. S. and Muller, M. T. (1998) Ultraviolet-induced DNA damage stimulates topoisomerase I-DNA complex formation in vivo: possible relationship with DNA repair. Cancer Res. 58, 976-984 (Pubitemid 28182467)
30. Wang, J. C. (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3, 430-440
31. Bieberich, C. J., Fujita, K., He, W. W. and Jay, G. (1996) Prostate-specific and androgen-dependent expression of a novel homeobox gene. J. Biol. Chem. 271,31779-31782 (Pubitemid 26422192)
32. Kos, L., Chiang, C. and Mahon, K. A. (1998) Mediolateral patterning of somites: multiple axial signals, including Sonic hedgehog, regulate Nkx-3.1 expression. Mech. Dev. 70,25-34 (Pubitemid 28116480)
33. Mao, Y., Okada, S., Chang, L. S. and Muller, M. T. (2000) p53 dependence of topoisomerase I recruitment in vivo. Cancer Res. 60, 4538-4543 (Pubitemid 32103637)
34. Karayan, L., Riou, J. F., Seite, P., Migeon, J., Cantereau, A. and Larsen, C. J. (2001) Human ARF protein interacts with topoisomerase I and stimulates its activity. Oncogene 20, 836-848 (Pubitemid 32198177)
35. Boothman, D. A., Trask, D. K. and Pardee, A. B. (1989) Inhibition of potentially lethal DNA damage repair in human tumor cells by β -lapachone, an activator of topoisomerase I. Cancer Res. 49, 605-612 (Pubitemid 19050323)
36. Mao, Y. and Muller, M. T. (2003) Down modulation of topoisomerase I affects DNA repair efficiency. DNA Repair 2, 1115-1126 (Pubitemid 39662826)
37. Lebedeva, N. A., Rechkunova, N. I., Agama, K., Pommier, Y. and Lavrik, O. I. (2009) Interaction of DNA topoisomerase 1 with DNA intermediates and proteins of base excision repair. Biochemistry 74, 1278-1284
38. Steadman, D. J., Giuffrida, D. and Gelmann, E. P. (2000) DNA-binding sequence of the human prostate-specific homeodomain protein NKX3.1. Nucleic Acids Res. 28,2389-2395 (Pubitemid 30349045)
39. Ju, J. H., Maeng, J. S., Zemedkun, M., Ahronovitz, N., Mack, J. W., Ferretti, J. A., Gelmann, E. P. and Gruschus, J. M. (2006) Physical and functional interactions between the prostate suppressor homeoprotein NKX3.1 and serum response factor. J. Mol. Biol. 360, 989-999 (Pubitemid 44062515)
40. Carson, J. A., Fillmore, R. A., Schwartz, R. J. and Zimmer, W. E. (2000) The smooth muscle γ -actin gene promoter is a molecular target for the mouse bagpipe homologue, mNkx3-1, and serum response factor. J. Biol. Chem. 275,39061-39072 (Pubitemid 32058920)