NPHP4 is necessary for normal photoreceptor ribbon synapse maintenance and outer segment formation, and for sperm development

Human Molecular Genetics

Volumn 20, Issue 3, 2011, Pages 482-496

  Won, Jungyeon ^a   de Evsikova, Caralina Marín ^a   Smith, Richard S ^a   Hicks, Wanda L ^a   Edwards, Malia M ^a   Longo Guess, Chantal ^a   Li, Tiansen ^b   Naggert, Jürgen K ^a   Nishina, Patsy M ^a  

^a JACKSON LABORATORY   (United States)

^b MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P14;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; EXON; GENE; GENE MUTATION; KIDNEY DYSFUNCTION; MALE; MOUSE; MUCOCILIARY TRANSPORT; NEPHRONOPHTHISIS; NEPHRONOPHTHISIS 4 GENE; NONHUMAN; PHENOTYPE; PHOTORECEPTOR INNER SEGMENT; PHOTORECEPTOR OUTER SEGMENT; PRIORITY JOURNAL; PROTEIN DEGRADATION; RETINA CONE; RETINA ROD; SPERMATOGENESIS; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; SYNAPSE;

ANIMALS; BLOTTING, WESTERN; CHROMOSOME MAPPING; CILIA; CODON, NONSENSE; ELECTRORETINOGRAPHY; INFERTILITY, MALE; KIDNEY DISEASES, CYSTIC; MALE; MICE; MICE, INBRED BALB C; MUTATION; NITROSOUREA COMPOUNDS; PHENOTYPE; PHOTORECEPTOR CELLS, VERTEBRATE; PROTEINS; RETINA; RETINAL DEGENERATION; SEQUENCE ANALYSIS, DNA; SPERM MATURATION; SPERM MOTILITY; SYNAPSES;

MUS;

EID: 78651078413     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq494     Document Type: Article

References (53)

1. Hildebrandt, F. and Otto, E. (2000) Molecular genetics of nephronophthisis and medullary cystic kidney disease. J. Am. Soc. Nephrol., 11, 1753-1761.
2. Saunier, S., Salomon, R. and Antignac, C. (2005) Nephronophthisis. Curr. Opin. Genet. Dev., 15, 324-331.
3. Krishnan, R., Eley, L. and Sayer, J.A. (2008) Urinary concentration defects and mechanisms underlying nephronophthisis. Kidney Blood Press Res., 31, 152-162.
4. Hildebrandt, F. and Omram, H. (2001) New insights: nephronophthisismedullary cystic kidney disease. Pediatr. Nephrol., 16, 168-176.
5. Mollet, G., Salomon, R., Gribouval, O., Silbermann, F., Bacq, D., Landthaler, G., Milford, D., Nayir, A., Rizzoni, G., Antignac, C. et al. (2002) The gene mutated in juvenile nephronophthisis type 4 encodes a novel protein that interacts with nephrocystin. Nat. Genet., 32, 300-305.
6. Roepman, R., Letteboer, S.J., Arts, H.H., van Beersum, S.E., Lu, X., Krieger, E., Ferreira, P.A. and Cremers, F.P. (2005) Interaction of nephrocystin-4 and RPGRIP1 is disrupted by nephronophthisis or Leber congenital amaurosis-associated mutations. Proc. Natl Acad. Sci. USA, 102, 18520-18525.
7. Delous, M., Baala, L., Salomon, R., Laclef, C., Vierkotten, J., Tory, K., Golzio, C., Lacoste, T., Besse, L., Ozilou, C. et al. (2007) The ciliary gene RPGRIP1L is mutated in cerebello-oculo-renal syndrome (Joubert syndrome type B) and Meckel syndrome. Nat. Genet., 39, 875-881.
8. Murga-Zamalloa, C.A., Desai, N.J., Hildebrandt, F. and Khanna, H. (2010) Interaction of ciliary disease protein retinitis pigmentosa GTPase regulator with nephronophthisis-associated proteins in mammalian retinas. Mol. Vis., 16, 1373-1381.
9. Mollet, G., Silbermann, F., Delous, M., Salomon, R., Antignac, C. and Saunier, S. (2005) Characterization of the nephrocystin/nephrocystin-4 complex and subcellular localization of nephrocystin-4 to primary cilia and centrosomes. Hum. Mol. Genet., 14, 645-656.
10. Otto, E., Hoefele, J., Ruf, R., Mueller, A.M., Hiller, K.S., Wolf, M.T., Schuermann, M.J., Becker, A., Birkenhäger, R., Sudbrak, R. et al. (2002) A gene mutated in nephronophthisis and retinitis pigmentosa encodes a novel protein, nephroretinin, conserved in evolution. Am. J. Hum. Genet., 71, 1161-1167.
11. May-Simera, H.L., Ross, A., Rix, S., Forge, A., Beales, P.L. and Jagger, D.J. (2009) Patterns of expression of Bardet-Biedl syndrome proteins in the mammalian cochlea suggest noncentrosomal functions. J. Comp. Neurol., 514, 174-188.
12. Liu, X.Z.,Walsh, J.,Mburu, P.,Kendrick-Jones, J.,Cope,M.J., Steel,K.P. and Brown, S.D. (1997) Mutations in the myosin VIIA gene cause non-syndromic recessive deafness. Nat. Genet., 16, 188-190.
13. Walton, J.P., Barsz, K. and Wilson, W.W. (2008) Sensorineural hearing loss and neural correlates of temporal acuity in the inferior colliculus of the C57BL/6 mouse. J. Assoc. Res. Otolaryngol., 9, 90-101.
14. Danciger, M., Lyon, J., Worrill, D., Hoffman, S., Lem, J., Reme, C.E., Wenzel, A. and Grimm, C. (2004) New retinal light damage QTL in mice with the light-sensitive RPE65 LEU variant. Mamm. Genome, 15, 277-283.
15. Won, J., Gifford, E., Smith, R.S., Yi, H., Ferreira, P.A., Hicks, W.L., Li, T., Naggert, J.K. and Nishina, P.M. (2009) RPGRIP1 is essential for normal rod photoreceptor outer segment elaboration and morphogenesis. Hum. Mol. Genet., 18, 4329-4339.
16. Morrow, E.M., Furukawa, T., Raviola, E. and Cepko, C.L. (2005) Synaptogenesis and outer segment formation are perturbed in the neural retina of Crx mutant mice. BMC Neurosci., 6, 5.
17. tom Dieck, S. and Brandstätter, J.H. (2006) Ribbon synapses of the retina. Cell Tissue Res., 326, 339-346.
18. Regus-Leidig, H., tomDieck, S., Specht, D.,Meyer, L. and Brandstätter, J.H. (2009) Early steps in the assembly of photoreceptor ribbon synapses in the mouse retina: the involvement of precursor spheres. J. Comp. Neurol., 512, 814-824.
19. Marc, R.E., Jones, B.W., Anderson, J.R., Kinard, K., Marshak, D.W., Wilson, J.H., Wensel, T. and Lucas, R.J. (2007) Neural reprogramming in retinal degeneration. Invest. Ophthalmol. Vis. Sci., 48, 3364-3371.
20. Jones, B.W., Watt, C.B., Frederick, J.M., Baehr, W., Chen, C.K., Levine, E.M., Milam, A.H., Lavail, M.M. and Marc, R.E. (2003) Retinal remodeling triggered by photoreceptor degenerations. J. Comp. Neurol., 464, 1-16.
21. Sakamoto, K., McCluskey, M., Wensel, T.G., Naggert, J.K. and Nishina, P.M. (2009) New mouse models for recessive retinitis pigmentosa caused by mutations in the Pde6a gene. Hum. Mol. Genet., 18, 178-192.
22. Won, J., Smith, R.S., Peachey, N.S., Wu, J., Hicks, W.L., Naggert, J.K. and Nishina, P.M. (2008) Membrane frizzled-related protein is necessary for the normal development and maintenance of photoreceptor outer segments. Vis. Neurosci., 25, 563-574.
23. Bisgrove, B.W. and Yost, H.J. (2006) The roles of cilia in developmental disorders and disease. Development, 133, 4131-4143.
24. Katsanis, N., Beales, P.L., Woods, M.O., Lewis, R.A., Green, J.S., Parfrey, P.S., Ansley, S.J., Davidson, W.S. and Lupski, J.R. (2000) Mutations in MKKS cause obesity, retinal dystrophy and renal malformations associated with Bardet-Biedl syndrome. Nat. Genet., 26, 67-70.
25. Collin, G.B., Marshall, J.D., Ikeda, A., So, W.V., Russell-Eggitt, I., Maffei, P., Beck, S., Boerkoel, C.F., Sicolo, N., Martin, M. et al. (2002) Mutations in ALMS1 cause obesity, type 2 diabetes and neurosensory degeneration in Alström syndrome. Nat. Genet., 31, 74-78.
26. Nauli, S.M., Alenghat, F.J., Luo, Y., Williams, E., Vassilev, P., Li, X., Elia, A.E., Lu, W., Brown, E.M., Quinn, S.J. et al. (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet., 33, 129-137.
27. Jauregui, A.R. and Barr, M.M. (2005) Functional characterization of the C. elegans nephrocystins NPHP-1 and NPHP-4 and their role in cilia and male sensory behaviors. Exp. Cell Res., 305, 333-342.
28. Wolf, M.T., Lee, J., Panther, F., Otto, E.A., Guan, K.L. and Hildebrandt, F. (2005) Expression and phenotype analysis of the nephrocystin-1 and nephrocystin-4 homologs in Caenorhabditis elegans. J. Am. Soc. Nephrol., 16, 676-687.
29. Wiik, A.C., Wade, C., Biagi, T., Ropstad, E.O., Bjerkas, E., Lindblad-Toh, K. and Lingaas, F. (2008) A deletion in nephronophthisis 4 (NPHP4) is associated with recessive cone-rod dystrophy in standard wire-haired dachshund. Genome Res., 18, 1415-1421.
30. Jiang, S.T., Chiou, Y.Y., Wang, E., Lin, H.K., Lee, S.P., Lu, H.Y., Wang, C.K., Tang, M.J. and Li, H. (2008) Targeted disruption of Nphp1 causes male infertility due to defects in the later steps of sperm morphogenesis in mice. Hum. Mol. Genet., 17, 3368-3379.
31. Chang, B., Khanna, H., Hawes, N., Jimeno, D., He, S., Lillo, C., Parapuram, S.K., Cheng, H., Scott, A., Hurd, R.E. et al. (2006) In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum. Mol. Genet., 15, 1847-1857.
32. Cook, S.A.,Collin,G.B.,Bronson,R.T.,Naggert, J.K., Liu,D.P.,Akeson,E.C. and Davisson, M.T. (2009) A mouse model for Meckel syndrome type 3. J. Am. Soc. Nephrol., 20, 753-764.
33. 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.
34. Collin, G.B., Cyr, E., Bronson, R., Marshall, J.D., Gifford, E.J., Hicks, W., Murray, S.A., Zheng, Q.Y., Smith, R.S., Nishina, P.M. et al. (2005) Alms1-disrupted mice recapitulate human Alström syndrome. Hum. Mol. Genet., 14, 2323-2333.
35. Davis, R.E., Swiderski, R.E., Rahmouni, K., Nishimura, D.Y., Mullins, R.F., Agassandian, K., Philp, A.R., Searby, C.C., Andrews, M.P., Thompson, S. et al. (2007) A knockin mouse model of the Bardet-Biedl syndrome 1 M390R mutation has cilia defects, ventriculomegaly, retinopathy, and obesity. Proc. Natl Acad. Sci. USA, 104, 19422-19427.
36. Zhao, Y., Hong, D.H., Pawlyk, B., Yue, G., Adamian, M., Grynberg, M., Godzik, A. and Li, T. (2003) The retinitis pigmentosa GTPase regulator (RPGR)-interacting protein: subserving RPGR function and participating in disk morphogenesis. Proc. Natl Acad. Sci. USA, 100, 3965-3970.
37. Arts, H.H., Doherty, D., van Beersum, S.E., Parisi, M.A., Letteboer, S.J., Gorden, N.T., Peters, T.A., Märker, T., Voesenek, K., Kartono, A. et al. (2007) Mutations in the gene encoding the basal body protein RPGRIP1L,a nephrocystin-4 interactor, cause Joubert syndrome. Nat. Genet., 39, 882-888.
38. Libby, R.T., Lavallee,C.R.,Balkema,G.W., Brunken, W.J. andHunter, D.D. (1999) Disruption of laminin beta2 chain production causes alterations in morphology and function in the CNS. J. Neurosci., 19, 9399-9411.
39. Libby, R.T., Lillo, C., Kitamoto, J., Williams, D.S. and Steel, K.P. (2004) Myosin Va is required for normal photoreceptor synaptic activity. J. Cell Sci., 117, 4509-4515.
40. Muresan, V., Lyass, A. and Schnapp, B.J. (1999) The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors. J. Neurosci., 19, 1027-1037.
41. Dick, O., tom Dieck, S., Altrock, W.D., Ammermüller, J., Weiler, R., Garner, C.C., Gundelfinger, E.D. and Brandstätter, J.H. (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron, 37, 775-786.
42. 2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat. Neurosci., 7, 1079-1087.
43. Chang, B., Heckenlively, J.R., Bayley, P.R., Brecha, N.C., Davisson, M.T., Hawes, N.L., Hirano, A.A., Hurd, R.E., Ikeda, A., Johnson, B.A. et al. (2006) The nob2 mouse, a null mutation in Cacna1f: anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses. Vis. Neurosci., 23, 11-24.
44. Johnson, K.R., Longo-Guess, C., Gagnon, L.H., Yu, H. and Zheng, Q.Y. (2008) A locus on distal chromosome 11 (ahl8) and its interaction with Cdh23 ahl underlie the early onset, age-related hearing loss of DBA/2J mice. Genomics, 92, 219-225.
45. Miller, S.A., Dykes, D.D. and Polesky, H.F. (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res., 16, 1215.
46. Taylor, B.A. and Phillips, S.J. (1996) Detection of obesity QTLs on mouse chromosomes 1 and 7 by selective DNA pooling. Genomics, 34, 389-398.
47. Ikeda, A., Naggert, J.K. and Nishina, P.M. (2002) Genetic modification of retinal degeneration in tubby mice. Exp. Eye Res., 74, 455-461.
48. LaVail, M.M., Gorrin, G.M., Repaci, M.A., Thomas, L.A. and Ginsberg, H.M. (1987) Genetic regulation of light damage to photoreceptors. Invest. Ophthalmol. Vis. Sci., 28, 1043-1048.
49. Hong, D.H., Pawlyk, B.S., Shang, J., Sandberg, M.A., Berson, E.L. and Li, T. (2000) A retinitis pigmentosa GTPase regulator (RPGR)-deficient mouse model for X-linked retinitis pigmentosa (RP3). Proc. Natl Acad. Sci. USA, 97, 3649-3654.
50. Bavister, B.D. and Andrews, J.C. (1988) A rapid sperm motility bioassay procedure for quality-control testing of water and culture media. J. In Vitro Fert. Embryo Transf., 5, 67-75.
51. Reed, M.L. and Petters, R.M. (1991) An evaluation of hamster, rat, and mouse sperm-cell motility in media formulated with water of different qualities. J. In Vitro Fert. Embryo Transf., 8, 41-47.
52. Eppig, J.J. and O'Brien, M.J. (1996) Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod., 54, 197-207.
53. Marín Bivens, C.L., Grøndahl, C., Murray, A., Blume, T., Su, Y.Q. and Eppig, J.J. (2004) Meiosis-activating sterol promotes the metaphase I to metaphase II transition and preimplantation developmental competence of mouse oocytes maturing in vitro. Biol. Reprod., 70, 1458-1464.