Pericentrin, a centrosomal protein related to microcephalic primordial dwarfism, is required for olfactory cilia assembly in mice

FASEB Journal

Volumn 23, Issue 10, 2009, Pages 3289-3297

  Miyoshi, Ko ^a   Kasahara, Kyosuke ^a   Miyazaki, Ikuko ^a   Shimizu, Shoko ^b   Taniguchi, Manabu ^b   Matsuzaki, Shinsuke ^b   Tohyama, Masaya ^b   Asanuma, Masato ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Ciliogenesis; Kendrin; Olfaction

Indexed keywords

GENOMIC DNA; PERICENTRIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CILIARY MOTILITY; CONTROLLED STUDY; DWARFISM; GENE MUTATION; GENOTYPE; IMMUNOFLUORESCENCE; MICROCEPHALIC PRIMORDIAL DWARFISM; MOUSE; NONHUMAN; NORTHERN BLOTTING; NOSE MUCOSA; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PRIORITY JOURNAL; PROTEIN FUNCTION; SENSORY NERVE CELL;

ANIMALS; ANTIGENS; CENTROSOME; CILIA; DWARFISM; MICE; MICE, MUTANT STRAINS; MICROCEPHALY; OLFACTORY BULB; TRANSCRIPTION, GENETIC;

ANIMALIA; MAMMALIA; MUS;

EID: 70349663509     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-124420     Document Type: Article

References (39)

1. Doxsey, S. J., Stein, P., Evans, L., Calarco, P. D., and Kirschner, M. (1994) Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76, 639-650 (Pubitemid 24070649)
2. Takahashi, M., Shibata, H., Shimakawa, M., Miyamoto, M., Mukai, H., and Ono, Y. (1999) Characterization of a novel giant scaffolding protein, CG-NAP, that anchors multiple signaling enzymes to centrosome and the golgi apparatus. J. Biol. Chem. 274, 17267-17274 (Pubitemid 129519063)
3. Flory, M. R., Moser, M. J., Monnat, R.J., Jr., and Davis, T. N. (2000) Identification of a human centrosomal calmodulinbinding protein that shares homology with pericentrin. Proc. Natl. Acad. Sci. U. S. A. 97, 5919-5923
4. Li, Q., Hansen, D., Killilea, A., Joshi, H. C., Palazzo, R. E., and Balczon, R. (2001) Kendrin/pericentrin-B, a centrosome protein with homology to pericentrin that complexes with PCM-1. J. Cell Sci. 114, 797-809 (Pubitemid 32237152)
5. Gillingham, A. K., and Munro, S. (2000) The PACT domain, a conserved centrosomal targeting motif in the coiled-coil proteins AKAP450 and pericentrin. EMBO Rep. 1, 524-529
6. Dictenberg, J. B., Zimmerman, W., Sparks, C. A., Young, A., Vidair, C., Zheng, Y., Carrington, W., Fay, F. S., and Doxsey, S. J. (1998) Pericentrin and gamma-tubulin form a protein complex and are organized into a novel lattice at the centrosome. J. Cell Biol. 141, 163-174 (Pubitemid 28182649)
7. Takahashi, M., Yamagiwa, A., Nishimura, T., Mukai, H., and Ono, Y. (2002) Centrosomal proteins CG-NAP and kendrin provide microtubule nucleation sites by anchoring γ-tubulin ring complex. Mol. Biol. Cell 13, 3235-3245 (Pubitemid 35034258)
8. Zimmerman, W. C., Sillibourne, J., Rosa, J., and Doxsey, S. J. (2004) Mitosis-specific anchoring of γ tubulin complexes by pericentrin controls spindle organization and mitotic entry. Mol. Biol. Cell 15, 3642-3657 (Pubitemid 38989703)
9. Martinez-Campos, M., Basto, R., Baker, J., Kernan, M., and Raff, J. W. (2004) The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J. Cell Biol. 165, 673-683 (Pubitemid 38765769)
10. Kawaguchi, S., and Zheng, Y. (2004) Characterization of a Drosophila centrosome protein CP309 that shares homology with Kendrin and CG-NAP. Mol. Biol. Cell 15, 37-45 (Pubitemid 38044941)
11. Bakalyar, H. A., and Reed, R. R. (1990) Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science 250, 1403-1406
12. Brunet, L. J., Gold, G. H., and Ngai, J. (1996) General anosmia caused by a targeted disruption of the mouse olfactory cyclic nucleotide-gated cation channel. Neuron 17, 681-693
13. Belluscio, L., Gold, G. H., Nemes, A., and Axel, R. (1998) Mice deficient in G(olf) are anosmic. Neuron 20, 69-81 (Pubitemid 28078350)
14. Wong, S. T., Trinh, K., Hacker, B., Chan, G. C., Lowe, G., Gaggar, A., Xia, Z., Gold, G. H., and Storm, D. R. (2000) Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27, 487-497 (Pubitemid 30951851)
15. Miyoshi, K., Onishi, K., Asanuma, M., Miyazaki, I., Diaz-Corrales, F. J., and Ogawa, N. (2006) Embryonic expression of pericentrin suggests universal roles in ciliogenesis. Dev. Genes Evol. 216, 537-542 (Pubitemid 44304960)
16. Jurczyk, A., Gromley, A., Redick, S., San Agustin, J., Witman, G., Pazour, G. J., Peters, D. J., and Doxsey, S. (2004) Pericentrin forms a complex with intraflagellar transport proteins and polycystin-2 and is required for primary cilia assembly. J. Cell Biol. 166, 637-643 (Pubitemid 39181001)
17. Griffith, E., Walker, S., Martin, C. A., Vagnarelli, P., Stiff, T., Vernay, B., Al Sanna, N., Saggar, A., Hamel, B., Earnshaw, W. C., Jeggo, P. A., Jackson, A. P., and O'Driscoll, M. (2008) Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat. Genet. 40, 232-236 (Pubitemid 351171398)
18. Rauch, A., Thiel, C. T., Schindler, D., Wick, U., Crow, Y. J., Ekici, A. B., van Essen, A. J., Goecke, T. O., Al-Gazali, L., Chrzanowska, K. H., Zweier, C., Brunner, H. G., Becker, K., Curry, C. J., Dallapiccola, B., Devriendt, K., Dörfler, A., Kinning, E., Megarbane, A., Meinecke, P., Semple, R. K., Spranger, S., Toutain, A., Trembath, R. C., Voss, E., Wilson, L., Hennekam, R., de Zegher, F., Dörr, H. G., and Reis, A. (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319, 816-819 (Pubitemid 351225872)
19. Araki, K., Imaizumi, T., Sekimoto, T., Yoshinobu, K., Yoshimuta, J., Akizuki, M., Miura, K., Araki, M., and Yamamura, K. (1999) Exchangeable gene trap using the Cre/mutated lox system. Cell. Mol. Biol. (Noisy-le-grand). 45, 737-750
20. Taniwaki, T., Haruna, K., Nakamura, H., Sekimoto, T., Oike, Y., Imaizumi, T., Saito, F., Muta, M., Soejima, Y., Utoh, A., Nakagata, N., Araki, M., Yamamura, K., and Araki, K. (2005) Characterization of an exchangeable gene trap using pU-17 carrying a stop codon-beta geo cassette. Dev. Growth Differ. 47, 163-172 (Pubitemid 40676938)
21. Yamamura, K., and Araki, K. (2008) Gene trap mutagenesis in mice: new perspectives and tools in cancer. Res. Cancer Sci. 99, 1-6 (Pubitemid 350239024)
22. Flory, M. R., and Davis, T. N. (2003) The centrosomal proteins pericentrin and kendrin are encoded by alternatively spliced products of one gene. Genomics 82, 401-405
23. Miyoshi, K., Asanuma, M., Miyazaki, I., Matsuzaki, S., Tohyama, M., and Ogawa, N. (2006) Characterization of pericentrin isoforms in vivo. Biochem. Biophys. Res. Commun. 351, 745-749
24. Rosenbaum, J. L., and Witman, G. B. (2002) Intraflagellar transport. Nat. Rev. Mol. Cell. Biol. 3, 813-825
25. Pan, J., Wang, Q., and Snell, W. J. (2005) Cilium-generated signaling and cilia-related disorders. Lab. Invest. 85, 452-463
26. Miura, K., Yoshinobu, K., Imaizumi, T., Haruna, K., Miyamoto, Y., Yoneda, Y., Nakagata, N., Araki, M., Miyakawa, T., Yamamura, K., and Araki, K. (2006) Impaired expression of importin/ karyopherin beta1 leads to post-implantation lethality. Biochem. Biophys. Res. Commun. 341, 132-138 (Pubitemid 43117396)
27. Moyer, J. H., Lee-Tischler, M. J., Kwon, H. Y., Schrick, J. J., Avner, E. D., Sweeney, W. E., Godfrey, V. L., Cacheiro, N. L., Wilkinson, J. E., and Woychik, R. P. (1994) Candidate gene associated with a mutation causing recessive polycystic kidney disease in mice. Science 264, 1329-1333
28. Pazour, G. J., Dickert, B. L., Vucica, Y., Seeley, E. S., Rosenbaum, J. L., Witman, G. B., and Cole, D. G. (2000) Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151, 709-718 (Pubitemid 30828148)
29. Taulman, P. D., Haycraft, C. J., Balkovetz, D. F., and Yoder, B. K. (2001) Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol. Biol. Cell 12, 589-599
30. Cano, D. A., Murcia, N. S., Pazour, G. J., and Hebrok, M. (2004) Orpk mouse model of polycystic kidney disease reveals essential role of primary cilia in pancreatic tissue organization. Development 131, 3457-3467
31. Zhang, Q., Davenport, J. R., Croyle, M. J., Haycraft, C. J., and Yoder, B. K. (2005) Disruption of IFT results in both exocrine and endocrine abnormalities in the pancreas of Tg737(orpk) mutant mice. Lab. Invest. 85, 45-64 (Pubitemid 40128040)
32. Kulaga, H. M., Leitch, C. C., Eichers, E. R., Badano, J. L., Lesemann, A., Hoskins, B. E., Lupski, J. R., Beales, P. L., Reed, R. R., and Katsanis, N. (2004) Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat. Genet. 36, 994-998 (Pubitemid 39167497)
33. Nishimura, D. Y., Fath, M., Mullins, R. F., Searby, C., Andrews, M., Davis, R., Andorf, J. L., Mykytyn, K., Swiderski, R. E., Yang, B., Carmi, R., Stone, E. M., and Sheffield, V. C. (2004) Bbs2-null mice have neurosensory deficits, a defect in social dominance, and retinopathy associated with mislocalization of rhodopsin. Proc. Natl. Acad. Sci. U. S. A. 101, 16588-16593 (Pubitemid 39557757)
34. Ross, A. J., May-Simera, H., Eichers, E. R., Kai, M., Hill, J., Jagger, D. J., Leitch, C. C., Chapple, J. P., Munro, P. M., Fisher, S., Tan, P. L., Phillips, H. M., Leroux, M. R., Henderson, D. J., Murdoch, J. N., Copp, A. J., Eliot, M. M., Lupski, J. R., Kemp, D. T., Dollfus, H., Tada, M., Katsanis, N., Forge, A., and Beales, P. L. (2005) Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet. 37, 1135-1140 (Pubitemid 41486669)
35. Mykytyn, K., Mullins, R. F., Andrews, M., Chiang, A. P., Swiderski, R. E., Yang, B., Braun, T., Casavant, T., Stone, E. M., and Sheffield, V. C. (2004) Bardet-Biedl syndrome type 4 (BBS4)- null mice implicate Bbs4 in flagella formation but not global cilia assembly. Proc. Natl. Acad. Sci. U. S. A. 101, 8664-8669 (Pubitemid 38745828)
36. Nachury, M. V., Loktev, A. V., Zhang, Q., Westlake, C. J., Peränen, J., Merdes, A., Slusarski, D. C., Scheller, R. H., Bazan, J. F., Sheffield, V. C., and Jackson, P. K. (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129, 1201-1213 (Pubitemid 46891037)
37. Kubo, A., and Tsukita, S. (2003) Non-membranous granular organelle consisting of PCM-1: subcellular distribution and cellcycle- dependent assembly/disassembly. J. Cell Sci. 116, 919-928 (Pubitemid 36367641)
38. Kim, J., Krishnaswami, S. R., and Gleeson, J. G. (2008) CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum. Mol. Genet. 17, 3796-3805
39. Marshall, W. F. (2008) The cell biological basis of ciliary disease. J. Cell Biol. 180, 17-21