Interaction with the Bardet-Biedl gene product TRIM32/BBS11 modifies the half-life and localization of Glis2/NPHP7

Journal of Biological Chemistry

Volumn 289, Issue 12, 2014, Pages 8390-8401

  Ramachandran, Haribaskar ^a   Schäfer, Tobias ^a   Kim, Yunhee ^a,b   Herfurth, Konstantin ^a,c   Hoff, Sylvia ^a,b   Lienkamp, Soeren S ^a   Kramer Zucker, Albrecht ^a   Walz, Gerd ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINS;

CILIARY LOCALIZATION; CLINICAL MANIFESTATION; FUNCTIONAL INTERACTION; GENETIC INTERACTION; MUSCULAR DYSTROPHY; SUBNUCLEAR LOCALIZATION; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL REPRESSORS;

GENES;

GLIS2 PROTEIN; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; GENE INTERACTION; GENE MUTATION; GENE PRODUCT; GENETIC ANALYSIS; GENETIC LINKAGE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PRONEPHROS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TRIM32 GENE; UBIQUITINATION; ZEBRA FISH;

BARDET-BIEDL SYNDROME; CILIOPATHIES; GENETIC DISEASES; NEPHRONOPHTHISIS; PROTEIN DEGRADATION; PROTEIN STABILITY; TRANSCRIPTION REGULATION; UBIQUITYLATION;

ANIMALS; BARDET-BIEDL SYNDROME; HEK293 CELLS; HUMANS; KIDNEY DISEASES, CYSTIC; KRUPPEL-LIKE TRANSCRIPTION FACTORS; PROTEIN INTERACTION MAPS; PROTEIN TRANSPORT; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; ZEBRAFISH;

EID: 84896957360     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.534024     Document Type: Article

References (51)

1. Hildebrandt, F., Benzing, T., and Katsanis, N. (2011) Ciliopathies. N. Engl. J. Med. 364, 1533-1543
2. Wolf, M. T., and Hildebrandt, F. (2011) Nephronophthisis. Pediatr. Nephrol. 26, 181-194
3. Jauregui, A. R., Nguyen, K. C., Hall, D. H., and Barr, M. M. (2008) The Caenorhabditis elegans nephrocystins act as global modifiers of cilium structure. J. Cell Biol. 180, 973-988 (Pubitemid 351398423)
4. Williams, C. L., Masyukova, S. V., and Yoder, B. K. (2010) Normal ciliogenesis requires synergy between the cystic kidney disease genes MKS-3 and NPHP-4. J. Am. Soc. Nephrol. 21, 782-793
5. Williams, C. L., Li, C., Kida, K., Inglis, P. N., Mohan, S., Semenec, L., Bialas, N. J., Stupay, R. M., Chen, N., Blacque, O. E., Yoder, B. K., and Leroux, M. R. (2011) MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J. Cell Biol. 192, 1023-1041
6. Sang, L., Miller, J. J., Corbit, K. C., Giles, R. H., Brauer, M. J., Otto, E. A., Baye, L. M., Wen, X., Scales, S. J., Kwong, M., Huntzicker, E. G., Sfakianos, M. K., Sandoval, W., Bazan, J. F., Kulkarni, P., Garcia-Gonzalo, F. R., Seol, A. D., O'Toole, J. F., Held, S., Reutter, H. M., Lane, W. S., Rafiq, M. A., Noor, A., Ansar, M., Devi, A. R., Sheffield, V. C., Slusarski, D. C., Vincent, J. B., Doherty, D. A., Hildebrandt, F., Reiter, J. F., and Jackson, P. K. (2011) Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 145, 513-528
7. Zaghloul, N. A., and Katsanis, N. (2009) Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy. J. Clin. Invest. 119, 428-437
8. Attanasio, M., Uhlenhaut, N. H., Sousa, V. H., O'Toole, J. F., Otto, E., Anlag, K., Klugmann, C., Treier, A. C., Helou, J., Sayer, J. A., Seelow, D., Nürnberg, G., Becker, C., Chudley, A. E., Nürnberg, P., Hildebrandt, F., and Treier, M. (2007) Loss of GLIS2 causes nephronophthisis in humans and mice by increased apoptosis and fibrosis. Nat. Genet. 39, 1018-1024 (Pubitemid 47185176)
9. Halbritter, J., Porath, J. D., Diaz, K. A., Braun, D. A., Kohl, S., Chaki, M., Allen, S. J., Soliman, N. A., Hildebrandt, F., and Otto, E. A. (2013) Identification of 99 novel mutations in a worldwide cohort of 1,056 patients with a nephronophthisis-related ciliopathy. Hum. Genet. 132, 865-884
10. Zhang, F., and Jetten, A. M. (2001) Genomic structure of the gene encoding the human GLI-related, Kruppel-like zinc finger protein GLIS2. Gene 280, 49-57 (Pubitemid 34014883)
11. Zhang, F., Nakanishi, G., Kurebayashi, S., Yoshino, K., Perantoni, A., Kim, Y. S., and Jetten, A. M. (2002) Characterization of Glis2, a novel gene encoding a Gli-related, Kruppel-like transcription factor with transactivation and repressor functions. Roles in kidney development and neurogenesis. J. Biol. Chem. 277, 10139-10149 (Pubitemid 34968126)
12. Kim, S. C., Kim, Y. S., and Jetten, A. M. (2005) Kruppel-like zinc finger protein Gli-similar 2 (Glis2) represses transcription through interaction with C-terminal binding protein 1 (CtBP1). Nucleic Acids Res. 33, 6805-6815
13. Kim, Y. S., Kang, H. S., and Jetten, A. M. (2007) The Kruppel-like zinc finger protein Glis2 functions as a negative modulator of the Wnt/betacatenin signaling pathway. FEBS Lett. 581, 858-864
14. Li, B., Rauhauser, A. A., Dai, J., Sakthivel, R., Igarashi, P., Jetten, A. M., and Attanasio, M. (2011) Increased hedgehog signaling in postnatal kidney results in aberrant activation of nephron developmental programs. Hum. Mol. Genet 20, 4155-4166
15. Gruber, T. A., Larson Gedman, A., Zhang, J., Koss, C. S., Marada, S., Ta, H. Q., Chen, S. C., Su, X., Ogden, S. K., Dang, J., Wu, G., Gupta, V., Andersson, A. K., Pounds, S., Shi, L., Easton, J., Barbato, M. I., Mulder, H. L., Manne, J., Wang, J., Rusch, M., Ranade, S., Ganti, R., Parker, M., Ma, J., Radtke, I., Ding, L., Cazzaniga, G., Biondi, A., Kornblau, S. M., Ravandi, F., Kantarjian, H., Nimer, S. D., Döhner, K., Döhner, H., Ley, T. J., Ballerini, P., Shurtleff, S., Tomizawa, D., Adachi, S., Hayashi, Y., Tawa, A., Shih, L. Y., Liang, D. C., Rubnitz, J. E., Pui, C. H., Mardis, E. R., Wilson, R. K., and Downing, J. R. (2012) An Inv(16)(p13.3q24.3)-encoded CBFA2T3-GLIS2 fusion protein defines an aggressive subtype of pediatric acute megakaryoblastic leukemia. Cancer Cell 22, 683-697
16. Masetti, R., Pigazzi, M., Togni, M., Astolfi, A., Indio, V., Manara, E., Casadio, R., Pession, A., Basso, G., and Locatelli, F. (2013) CBFA2T3-GLIS2 fusion transcript is a novel common feature in pediatric, cytogenetically normal AML, not restricted to FAB M7 subtype. Blood 121, 3469-3472
17. Kim, Y. S., Kang, H. S., Herbert, R., Beak, J. Y., Collins, J. B., Grissom, S. F., and Jetten, A. M. (2008) Kruppel-like zinc finger protein Glis2 is essential for the maintenance of normal renal functions. Mol. Cell Biol. 28, 2358-2367 (Pubitemid 351429981)
18. Vasanth, S., ZeRuth, G., Kang, H. S., and Jetten, A. M. (2011) Identification of nuclear localization, DNA binding, and transactivating mechanisms of Kruppel-like zinc finger protein Gli-similar 2 (Glis2). J. Biol. Chem. 286, 4749-4759
19. Hosking, C. R., Ulloa, F., Hogan, C., Ferber, E. C., Figueroa, A., Gevaert, K., Birchmeier, W., Briscoe, J., and Fujita, Y. (2007) The transcriptional repressor Glis2 is a novel binding partner for p120 catenin. Mol. Biol. Cell 18, 1918-1927 (Pubitemid 46717571)
20. Kang, H. S., Beak, J. Y., Kim, Y. S., Herbert, R., and Jetten, A. M. (2009) Glis3 is associated with primary cilia and Wwtr1/TAZ and implicated in polycystic kidney disease. Mol. Cell Biol. 29, 2556-2569
21. Kang, H. S., ZeRuth, G., Lichti-Kaiser, K., Vasanth, S., Yin, Z., Kim, Y. S., and Jetten, A. M. (2010) Gli-similar (Glis) Kruppel-like zinc finger proteins. Insights into their physiological functions and critical roles in neonatal diabetes and cystic renal disease. Histol. Histopathol. 25, 1481-1496
22. Chiang, A. P., Beck, J. S., Yen, H. J., Tayeh, M. K., Scheetz, T. E., Swiderski, R. E., Nishimura, D. Y., Braun, T. A., Kim, K. Y., Huang, J., Elbedour, K., Carmi, R., Slusarski, D. C., Casavant, T. L., Stone, E. M., and Sheffield, V. C. (2006) Homozygosity mapping with SNP arrays identifies TRIM32, an E3 ubiquitin ligase, as a Bardet-Biedl syndrome gene (BBS11). Proc. Natl. Acad. Sci. U.S.A. 103, 6287-6292
23. Micale, L., Chaignat, E., Fusco, C., Reymond, A., and Merla, G. (2012) The tripartite motif. Structure and function. Adv. Exp. Med. Biol. 770, 11-25
24. Ozato, K., Shin, D. M., Chang, T. H., and Morse, H. C., 3rd. (2008) TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 8, 849-860
25. Cammas, F., Khetchoumian, K., Chambon, P., and Losson, R. (2012) TRIM involvement in transcriptional regulation. Adv. Exp. Med. Biol. 770, 59-76
26. LaBeau-DiMenna, E. M., Clark, K. A., Bauman, K. D., Parker, D. S., Cripps, R. M., and Geisbrecht, E. R. (2012) Thin, a Trim32 ortholog, is essential for myofibril stability and is required for the integrity of the costamere in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 109, 17983-17988
27. Hatakeyama, S. (2011) TRIM proteins and cancer. Nat. Rev. Cancer 11, 792-804
28. Frosk, P., Weiler, T., Nylen, E., Sudha, T., Greenberg, C. R., Morgan, K., Fujiwara, T. M., and Wrogemann, K. (2002) Limb-girdle muscular dystrophy type 2H associated with mutation in TRIM32, a putative E3-ubiquitin-ligase gene. Am. J. Hum. Genet. 70, 663-672 (Pubitemid 34177921)
29. Cossée, M., Lagier-Tourenne, C., Seguela, C., Mohr, M., Leturcq, F., Gundesli, H., Chelly, J., Tranchant, C., Koenig, M., and Mandel, J. L. (2009) Use of SNP array analysis to identify a novel TRIM32 mutation in limbgirdle muscular dystrophy type 2H. Neuromuscul. Disord. 19, 255-260
30. Kudryashova, E., Wu, J., Havton, L. A., and Spencer, M. J. (2009) Deficiency of the E3 ubiquitin ligase TRIM32 in mice leads to a myopathy with a neurogenic component. Hum. Mol. Genet 18, 1353-1367
31. Kudryashova, E., Struyk, A., Mokhonova, E., Cannon, S. C., and Spencer, M. J. (2011) The common missense mutation D489N in TRIM32 causing limb girdle muscular dystrophy 2H leads to loss of the mutated protein in knock-in mice resulting in a Trim32-null phenotype. Hum. Mol. Genet 20, 3925-3932
32. Kudryashova, E., Kudryashov, D., Kramerova, I., and Spencer, M. J. (2005) Trim32 is a ubiquitin ligase mutated in limb girdle muscular dystrophy type 2H that binds to skeletal muscle myosin and ubiquitinates actin. J. Mol. Biol. 354, 413-424 (Pubitemid 41579855)
33. Albor, A., El-Hizawi, S., Horn, E. J., Laederich, M., Frosk, P., Wrogemann, K., and Kulesz-Martin, M. (2006) The interaction of Piasy with Trim32, an E3-ubiquitin ligase mutated in limb-girdle muscular dystrophy type 2H, promotes Piasy degradation and regulates UVB-induced keratinocyte apoptosis through NFκB. J. Biol. Chem. 281, 25850-25866 (Pubitemid 44401973)
34. Kano, S., Miyajima, N., Fukuda, S., and Hatakeyama, S. (2008) Tripartite motif protein 32 facilitates cell growth and migration via degradation of Abl-interactor 2. Cancer Res. 68, 5572-5580
35. Locke, M., Tinsley, C. L., Benson, M. A., and Blake, D. J. (2009) TRIM32 is an E3 ubiquitin ligase for dysbindin. Hum. Mol. Genet 18, 2344-2358
36. Ryu, Y. S., Lee, Y., Lee, K. W., Hwang, C. Y., Maeng, J. S., Kim, J. H., Seo, Y. S., You, K. H., Song, B., and Kwon, K. S. (2011) TRIM32 protein sensitizes cells to tumor necrosis factor (TNFα)-induced apoptosis via its RING domain-dependent E3 ligase activity against X-linked inhibitor of apoptosis (XIAP). J. Biol. Chem. 286, 25729-25738
37. Gonzalez-Cano, L., Hillje, A. L., Fuertes-Alvarez, S., Marques, M. M., Blanch, A., Ian, R. W., Irwin, M. S., Schwamborn, J. C., and Marín, M. C. (2013) Regulatory feedback loop between TP73 and TRIM32. Cell Death Dis. 4, e704
38. Cohen, S., Zhai, B., Gygi, S. P., and Goldberg, A. L. (2012) Ubiquitylation by Trim32 causes coupled loss of desmin, Z-bands, and thin filaments in muscle atrophy. J. Cell Biol. 198, 575-589
39. Schäfer, T., Pütz, M., Lienkamp, S., Ganner, A., Bergbreiter, A., Ramachandran, H., Gieloff, V., Gerner, M., Mattonet, C., Czarnecki, P. G., Sayer, J. A., Otto, E. A., Hildebrandt, F., Kramer-Zucker, A., and Walz, G. (2008) Genetic and physical interaction between the NPHP5 and NPHP6 gene products. Hum. Mol. Genet 17, 3655-3662
40. Haribaskar, R., Pütz, M., Schupp, B., Skouloudaki, K., Bietenbeck, A., Walz, G., and Schäfer, T. (2009) The planar cell polarity (PCP) protein Diversin translocates to the nucleus to interact with the transcription factor AF9. Biochem. Biophys. Res. Commun. 387, 212-217
41. Kim, Y. H., Epting, D., Slanchev, K., Engel, C., Walz, G., and Kramer-Zucker, A. (2013) A complex of BBS1 and NPHP7 is required for cilia motility in zebrafish. PLoS One 8, e72549
42. Perner, B., Englert, C., and Bollig, F. (2007) The Wilms tumor genes wt1a and wt1b control different steps during formation of the zebrafish pronephros. Dev. Biol. 309, 87-96 (Pubitemid 47302449)
43. Mund, T., and Pelham, H. R. (2010) Regulation of PTEN/Akt and MAP kinase signaling pathways by the ubiquitin ligase activators Ndfip1 and Ndfip2. Proc. Natl. Acad. Sci. U.S.A. 107, 11429-11434
44. Aguilar, R. C., and Wendland, B. (2003) Ubiquitin. Not just for proteasomes anymore. Curr. Opin. Cell Biol. 15, 184-190 (Pubitemid 36332193)
45. Chen, Z. J., and Sun, L. J. (2009) Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 33, 275-286
46. Zhang, J., Hu, M. M., Wang, Y. Y., and Shu, H. B. (2012) TRIM32 protein modulates type I interferon induction and cellular antiviral response by targeting MITA/STING protein for K63-linked ubiquitination. J. Biol. Chem. 287, 28646-28655
47. Nachury, M. V., Seeley, E. S., and Jin, H. (2010) Trafficking to the ciliary membrane. How to get across the periciliary diffusion barrier? Annu. Rev. Cell Dev. Biol. 26, 59-87
48. Thiollier, C., Lopez, C. K., Gerby, B., Ignacimouttou, C., Poglio, S., Duffourd, Y., Guégan, J., Rivera-Munoz, P., Bluteau, O., Mabialah, V., Diop, M., Wen, Q., Petit, A., Bauchet, A. L., Reinhardt, D., Bornhauser, B., Gautheret, D., Lecluse, Y., Landman-Parker, J., Radford, I., Vainchenker, W., Dastugue, N., de Botton, S., Dessen, P., Bourquin, J. P., Crispino, J. D., Ballerini, P., Bernard, O. A., Pflumio, F., and Mercher, T. (2012) Characterization of novel genomic alterations and therapeutic approaches using acute megakaryoblastic leukemia xenograft models. J. Exp. Med. 209, 2017-2031
49. Muller, J., Stoetzel, C., Vincent, M. C., Leitch, C. C., Laurier, V., Danse, J. M., Hellé, S., Marion, V., Bennouna-Greene, V., Vicaire, S., Megarbane, A., Kaplan, J., Drouin-Garraud, V., Hamdani, M., Sigaudy, S., Francannet, C., Roume, J., Bitoun, P., Goldenberg, A., Philip, N., Odent, S., Green, J., Cossée, M., Davis, E. E., Katsanis, N., Bonneau, D., Verloes, A., Poch, O., Mandel, J. L., and Dollfus, H. (2010) Identification of 28 novel mutations in the Bardet-Biedl syndrome genes. The burden of private mutations in an extensively heterogeneous disease. Hum. Genet. 127, 583-593
50. Katsanis, N., Ansley, S. J., Badano, J. L., Eichers, E. R., Lewis, R. A., Hoskins, B. E., Scambler, P. J., Davidson, W. S., Beales, P. L., and Lupski, J. R. (2001) Triallelic inheritance in Bardet-Biedl syndrome, a Mendelian recessive disorder. Science 293, 2256-2259 (Pubitemid 32900235)
51. Badano, J. L., Kim, J. C., Hoskins, B. E., Lewis, R. A., Ansley, S. J., Cutler, D. J., Castellan, C., Beales, P. L., Leroux, M. R., and Katsanis, N. (2003) Heterozygous mutations in BBS1, BBS2 and BBS6 have a potential epistatic effect on Bardet-Biedl patients with two mutations at a second BBS locus. Hum. Mol. Genet 12, 1651-1659 (Pubitemid 36896658)