The RCC1 superfamily: From genes, to function, to disease

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1783, Issue 8, 2008, Pages 1467-1479

  Hadjebi, Ouadah ^a   Casas Terradellas, Eduard ^a   Garcia Gonzalo, Francesc R ^a   Rosa, Jose Luis ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

GEF; GRF; HERC; RCBTB; RCC1; RLD

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; POLYCYSTIN 1; PROTEIN RCC1; REGULATOR PROTEIN;

AMINO ACID SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; CARBOXY TERMINAL SEQUENCE; CELL CYCLE REGULATION; CELLULAR DISTRIBUTION; ENZYME INHIBITION; GENE EXPRESSION; GENE MUTATION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; KIDNEY POLYCYSTIC DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN STRUCTURE; REVIEW; WILLIAMS BEUREN SYNDROME;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; GENETIC DISEASES, INBORN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PHYLOGENY; SEQUENCE ALIGNMENT; TISSUE DISTRIBUTION;

EID: 45049086435     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2008.03.015     Document Type: Review

References (160)

1. Nishimoto T., Eilen E., and Basilico C. Premature of chromosome condensation in a ts DNA-mutant of BHK cells. Cell 15 (1978) 475-483
2. Ohtsubo M., Kai R., Furuno N., Sekiguchi T., Sekiguchi M., Hayashida H., Kuma K., Miyata T., Fukushige S., Murotsu T., et al. Isolation and characterization of the active cDNA of the human cell cycle gene (RCC1) involved in the regulation of onset of chromosome condensation. Genes Dev. 1 (1987) 585-593
3. Nishitani H., Ohtsubo M., Yamashita K., Iida H., Pines J., Yasudo H., Shibata Y., Hunter T., and Nishimoto T. Loss of RCC1, a nuclear DNA-binding protein, uncouples the completion of DNA replication from the activation of cdc2 protein kinase and mitosis. EMBO J. 10 (1991) 1555-1564
4. Rosa J.L., Casaroli-Marano R.P., Buckler A.J., Vilaro S., and Barbacid M. p619, a giant protein related to the chromosome condensation regulator RCC1, stimulates guanine nucleotide exchange on ARF1 and Rab proteins. EMBO J. 15 (1996) 4262-4273
5. Garcia-Gonzalo F.R., and Rosa J.L. The HERC proteins: functional and evolutionary insights. Cell. Mol. Life Sci. 62 (2005) 1826-1838
6. Hood F.E., and Clarke P.R. RCC1 isoforms differ in their affinity for chromatin, molecular interactions and regulation by phosphorylation. J. Cell Sci. 120 (2007) 3436-3445
7. Hochrainer K., Mayer H., Baranyi U., Binder B., Lipp J., and Kroismayr R. The human HERC family of ubiquitin ligases: novel members, genomic organization, expression profiling, and evolutionary aspects. Genomics 85 (2005) 153-164
8. Uhlmann J., Wiemann S., and Ponstingl H. DelGEF, an RCC1-related protein encoded by a gene on chromosome 11p14 critical for two forms of hereditary deafness. FEBS Lett. 460 (1999) 153-160
9. Shu X., Black G.C., Rice J.M., Hart-Holden N., Jones A., O'Grady A., Ramsden S., and Wright A.F. RPGR mutation analysis and disease: an update. Human Mutat. 28 (2007) 322-328
10. Santos T.M., Han S., Bowser M., Sazani K., Beauchamp R.L., Murthy V., Bhide P.G., and Ramesh V. Alternative splicing in protein associated with Myc (Pam) influences its binding to c-Myc. J. Neurosci. Res. 83 (2006) 222-232
11. Neidhardt J., Glaus E., Barthelmes D., Zeitz C., Fleischhauer J., and Berger W. Identification and characterization of a novel RPGR isoform in human retina. Human Mutat. 28 (2007) 797-807
12. Kirschner R., Rosenberg T., Schultz-Heienbrok R., Lenzner S., Feil S., Roepman R., Cremers F.P., Ropers H.H., and Berger W. RPGR transcription studies in mouse and human tissues reveal a retina-specific isoform that is disrupted in a patient with X-linked retinitis pigmentosa. Hum. Mol. Genet. 8 (1999) 1571-1578
13. Hubbard T.J., Aken B.L., Beal K., Ballester B., Caccamo M., Chen Y., Clarke L., Coates G., Cunningham F., Cutts T., Down T., Dyer S.C., Fitzgerald S., Fernandez-Banet J., Graf S., Haider S., Hammond M., Herrero J., Holland R., Howe K., Howe K., Johnson N., Kahari A., Keefe D., Kokocinski F., Kulesha E., Lawson D., Longden I., Melsopp C., Megy K., Meidl P., Ouverdin B., Parker A., Prlic A., Rice S., Rios D., Schuster M., Sealy I., Severin J., Slater G., Smedley D., Spudich G., Trevanion S., Vilella A., Vogel J., White S., Wood M., Cox T., Curwen V., Durbin R., Fernandez-Suarez X.M., Flicek P., Kasprzyk A., Proctor G., Searle S., Smith J., Ureta-Vidal A., and Birney E. Ensembl 2007. Nucleic Acids Res. 35 (2007) D610-D617
14. Mulder N.J., Apweiler R., Attwood T.K., Bairoch A., Bateman A., Binns D., Bork P., Buillard V., Cerutti L., Copley R., Courcelle E., Das U., Daugherty L., Dibley M., Finn R., Fleischmann W., Gough J., Haft D., Hulo N., Hunter S., Kahn D., Kanapin A., Kejariwal A., Labarga A., Langendijk-Genevaux P.S., Lonsdale D., Lopez R., Letunic I., Madera M., Maslen J., McAnulla C., McDowall J., Mistry J., Mitchell A., Nikolskaya A.N., Orchard S., Orengo C., Petryszak R., Selengut J.D., Sigrist C.J., Thomas P.D., Valentin F., Wilson D., Wu C.H., and Yeats C. New developments in the InterPro database. Nucleic Acids Res. 35 (2007) D224-D228
15. Renault L., Nassar N., Vetter I., Becker J., Klebe C., Roth M., and Wittinghofer A. The 1.7 A crystal structure of the regulator of chromosome condensation (RCC1) reveals a seven-bladed propeller. Nature 392 (1998) 97-101
16. Hulo N., Bairoch A., Bulliard V., Cerutti L., Cuche B.A., de Castro E., Lachaize C., Langendijk-Genevaux P.S., and Sigrist C.J. The 20 years of PROSITE. Nucleic Acids Res. 36 (2008) D245-D249
17. Stevens T.J., and Paoli M. RCC1-like repeat proteins: a pangenomic, structurally diverse new superfamily of beta-propeller domains. Proteins 70 (2008) 378-387
18. Bateman A., Birney E., Cerruti L., Durbin R., Etwiller L., Eddy S.R., Griffiths-Jones S., Howe K.L., Marshall M., and Sonnhammer E.L. The Pfam protein families database. Nucleic Acids Res. 30 (2002) 276-280
19. Bateman A., Birney E., Durbin R., Eddy S.R., Howe K.L., and Sonnhammer E.L. The Pfam protein families database. Nucleic Acids Res. 28 (2000) 263-266
20. Ochman H., Lawrence J.G., and Groisman E.A. Lateral gene transfer and the nature of bacterial innovation. Nature 405 (2000) 299-304
21. Lim D., Park H.U., De Castro L., Kang S.G., Lee H.S., Jensen S., Lee K.J., and Strynadka N.C. Crystal structure and kinetic analysis of beta-lactamase inhibitor protein-II in complex with TEM-1 beta-lactamase. Nat. Struct. Biol. 8 (2001) 848-852
22. Renault L., Nassar N., Wittinghofer A., Roth M., and Vetter I.R. Crystallization and preliminary X-ray analysis of human RCC1, the regulator of chromosome condensation. Acta Crystallogr., D Biol. Crystallogr. 55 (1999) 272-275
23. Chen T., Muratore T.L., Schaner-Tooley C.E., Shabanowitz J., Hunt D.F., and Macara I.G. N-terminal alpha-methylation of RCC1 is necessary for stable chromatin association and normal mitosis. Nat. Cell Biol. 9 (2007) 596-603
24. Hutchins J.R., Moore W.J., Hood F.E., Wilson J.S., Andrews P.D., Swedlow J.R., and Clarke P.R. Phosphorylation regulates the dynamic interaction of RCC1 with chromosomes during mitosis. Curr. Biol. 14 (2004) 1099-1104
25. Li H.Y., and Zheng Y. Phosphorylation of RCC1 in mitosis is essential for producing a high RanGTP concentration on chromosomes and for spindle assembly in mammalian cells. Genes Dev. 18 (2004) 512-527
26. Friedrich B., Quensel C., Sommer T., Hartmann E., and Kohler M. Nuclear localization signal and protein context both mediate importin alpha specificity of nuclear import substrates. Mol. Cell. Biol. 26 (2006) 8697-8709
27. Seino H., Hisamoto N., Uzawa S., Sekiguchi T., and Nishimoto T. DNA-binding domain of RCC1 protein is not essential for coupling mitosis with DNA replication. J. Cell Sci. 102 Pt 3 (1992) 393-400
28. Mollinari C., Reynaud C., Martineau-Thuillier S., Monier S., Kieffer S., Garin J., Andreassen P.R., Boulet A., Goud B., Kleman J.P., and Margolis R.L. The mammalian passenger protein TD-60 is an RCC1 family member with an essential role in prometaphase to metaphase progression. Dev. Cell 5 (2003) 295-307
29. Moore W., Zhang C., and Clarke P.R. Targeting of RCC1 to chromosomes is required for proper mitotic spindle assembly in human cells. Curr. Biol. 12 (2002) 1442-1447
30. Martineau-Thuillier S., Andreassen P.R., and Margolis R.L. Colocalization of TD-60 and INCENP throughout G2 and mitosis: evidence for their possible interaction in signalling cytokinesis. Chromosoma 107 (1998) 461-470
31. Nemergut M.E., Mizzen C.A., Stukenberg T., Allis C.D., and Macara I.G. Chromatin docking and exchange activity enhancement of RCC1 by histones H2A and H2B. Science 292 (2001) 1540-1543
32. Sjolinder M., Uhlmann J., and Ponstingl H. Characterisation of an evolutionary conserved protein interacting with the putative guanine nucleotide exchange factor DelGEF and modulating secretion. Exp. Cell Res. 294 (2004) 68-76
33. Sjolinder M., Uhlmann J., and Ponstingl H. DelGEF, a homologue of the Ran guanine nucleotide exchange factor RanGEF, binds to the exocyst component Sec5 and modulates secretion. FEBS Lett. 532 (2002) 211-215
34. Lehman A.L., Nakatsu Y., Ching A., Bronson R.T., Oakey R.J., Keiper-Hrynko N., Finger J.N., Durham-Pierre D., Horton D.B., Newton J.M., Lyon M.F., and Brilliant M.H. A very large protein with diverse functional motifs is deficient in rjs (runty, jerky, sterile) mice. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 9436-9441
35. Davies W., Smith R.J., Kelsey G., and Wilkinson L.S. Expression patterns of the novel imprinted genes Nap1l5 and Peg13 and their non-imprinted host genes in the adult mouse brain. Gene Expr. Patterns 4 (2004) 741-747
36. Mitsui K., Nakanishi M., Ohtsuka S., Norwood T.H., Okabayashi K., Miyamoto C., Tanaka K., Yoshimura A., and Ohtsubo M. A novel human gene encoding HECT domain and RCC1-like repeats interacts with cyclins and is potentially regulated by the tumor suppressor proteins. Biochem. Biophys. Res. Commun. 266 (1999) 115-122
37. Kroismayr R., Baranyi U., Stehlik C., Dorfleutner A., Binder B.R., and Lipp J. HERC5, a HECT E3 ubiquitin ligase tightly regulated in LPS activated endothelial cells. J. Cell Sci. 117 (2004) 4749-4756
38. Dastur A., Beaudenon S., Kelley M., Krug R.M., and Huibregtse J.M. Herc5, an interferon-induced HECT E3 enzyme, is required for conjugation of ISG15 in human cells. J. Biol. Chem. 281 (2006) 4334-4338
39. Wong J.J., Pung Y.F., Sze N.S., and Chin K.C. HERC5 is an IFN-induced HECT-type E3 protein ligase that mediates type I IFN-induced ISGylation of protein targets. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 10735-10740
40. Takeuchi T., Inoue S., and Yokosawa H. Identification and Herc5-mediated ISGylation of novel target proteins. Biochem. Biophys. Res. Commun. 348 (2006) 473-477
41. Cruz C., Ventura F., Bartrons R., and Rosa J.L. HERC3 binding to and regulation by ubiquitin. FEBS Lett. 488 (2001) 74-80
42. Garcia-Gonzalo F.R., Bartrons R., Ventura F., and Rosa J.L. Requirement of phosphatidylinositol-4,5-bisphosphate for HERC1-mediated guanine nucleotide release from ARF proteins. FEBS Lett. 579 (2005) 343-348
43. Garcia-Gonzalo F.R., Munoz P., Gonzalez E., Casaroli-Marano R.P., Vilaro S., Bartrons R., Ventura F., and Rosa J.L. The giant protein HERC1 is recruited to aluminum fluoride-induced actin-rich surface protrusions in HeLa cells. FEBS Lett. 559 (2004) 77-83
44. Rosa J.L., and Barbacid M. A giant protein that stimulates guanine nucleotide exchange on ARF1 and Rab proteins forms a cytosolic ternary complex with clathrin and Hsp70. Oncogene 15 (1997) 1-6
45. Rodriguez C.I., and Stewart C.L. Disruption of the ubiquitin ligase HERC4 causes defects in spermatozoon maturation and impaired fertility. Dev. Biol. 312 (2007) 501-508
46. Liu S., Lu W., Obara T., Kuida S., Lehoczky J., Dewar K., Drummond I.A., and Beier D.R. A defect in a novel Nek-family kinase causes cystic kidney disease in the mouse and in zebrafish. Development 129 (2002) 5839-5846
47. Tan B.C., and Lee S.C. Nek9, a novel FACT-associated protein, modulates interphase progression. J. Biol. Chem. 279 (2004) 9321-9330
48. Roig J., Mikhailov A., Belham C., and Avruch J. Nercc1, a mammalian NIMA-family kinase, binds the Ran GTPase and regulates mitotic progression. Genes Dev. 16 (2002) 1640-1658
49. Pelka P., Scime A., Mandalfino C., Joch M., Abdulla P., and Whyte P. Adenovirus E1A proteins direct subcellular redistribution of Nek9, a NimA-related kinase. J. Cell. Physiol. 212 (2007) 13-25
50. Holland P.M., Milne A., Garka K., Johnson R.S., Willis C., Sims J.E., Rauch C.T., Bird T.A., and Virca G.D. Purification, cloning, and characterization of Nek8, a novel NIMA-related kinase, and its candidate substrate Bicd2. J. Biol. Chem. 277 (2002) 16229-16240
51. Mahjoub M.R., Trapp M.L., and Quarmby L.M. NIMA-related kinases defective in murine models of polycystic kidney diseases localize to primary cilia and centrosomes. J. Am. Soc. Nephrol. 16 (2005) 3485-3489
52. Liu W., Quinto I., Chen X., Palmieri C., Rabin R.L., Schwartz O.M., Nelson D.L., and Scala G. Direct inhibition of Bruton's tyrosine kinase by IBtk, a Btk-binding protein. Nat. Immunol. 2 (2001) 939-946
53. Shu X., Fry A.M., Tulloch B., Manson F.D., Crabb J.W., Khanna H., Faragher A.J., Lennon A., He S., Trojan P., Giessl A., Wolfrum U., Vervoort R., Swaroop A., and Wright A.F. RPGR ORF15 isoform co-localizes with RPGRIP1 at centrioles and basal bodies and interacts with nucleophosmin. Hum. Mol. Genet. 14 (2005) 1183-1197
54. Hong D.H., Pawlyk B., Sokolov M., Strissel K.J., Yang J., Tulloch B., Wright A.F., Arshavsky V.Y., and Li T. RPGR isoforms in photoreceptor connecting cilia and the transitional zone of motile cilia. Investig. Ophthalmol. Vis. Sci. 44 (2003) 2413-2421
55. Khanna H., Hurd T.W., Lillo C., Shu X., Parapuram S.K., He S., Akimoto M., Wright A.F., Margolis B., Williams D.S., and Swaroop A. RPGR-ORF15, which is mutated in retinitis pigmentosa, associates with SMC1, SMC3, and microtubule transport proteins. J. Biol. Chem. 280 (2005) 33580-33587
56. Zhao Y., Hong D.H., Pawlyk B., Yue G., Adamian M., Grynberg M., Godzik A., and Li T. The retinitis pigmentosa GTPase regulator (RPGR)-interacting protein: subserving RPGR function and participating in disk morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 3965-3970
57. Yamanaka K., Vande Velde C., Eymard-Pierre E., Bertini E., Boespflug-Tanguy O., and Cleveland D.W. Unstable mutants in the peripheral endosomal membrane component ALS2 cause early-onset motor neuron disease. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 16041-16046
58. Topp J.D., Gray N.W., Gerard R.D., and Horazdovsky B.F. Alsin is a Rab5 and Rac1 guanine nucleotide exchange factor. J. Biol. Chem. 279 (2004) 24612-24623
59. Kunita R., Otomo A., Mizumura H., Suzuki-Utsunomiya K., Hadano S., and Ikeda J.E. The Rab5 activator ALS2/alsin acts as a novel Rac1 effector through Rac1-activated endocytosis. J. Biol. Chem. 282 (2007) 16599-16611
60. Guo Q., Xie J., Dang C.V., Liu E.T., and Bishop J.M. Identification of a large Myc-binding protein that contains RCC1-like repeats. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 9172-9177
61. Yang H., Scholich K., Poser S., Storm D.R., Patel T.B., and Goldowitz D. Developmental expression of PAM (protein associated with MYC) in the rodent brain. Brain Res. 136 (2002) 35-42
62. Lewcock J.W., Genoud N., Lettieri K., and Pfaff S.L. The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56 (2007) 604-620
63. Murthy V., Han S., Beauchamp R.L., Smith N., Haddad L.A., Ito N., and Ramesh V. Pam and its ortholog highwire interact with and may negatively regulate the TSC1.TSC2 complex. J. Biol. Chem. 279 (2004) 1351-1358
64. Bos J.L., Rehmann H., and Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 129 (2007) 865-877
65. Riddick G., and Macara I.G. A systems analysis of importin-{alpha}-{beta} mediated nuclear protein import. J. Cell Biol. 168 (2005) 1027-1038
66. Ohtsubo M., Okazaki H., and Nishimoto T. The RCC1 protein, a regulator for the onset of chromosome condensation locates in the nucleus and binds to DNA. J. Cell Biol. 109 (1989) 1389-1397
67. Bamba C., Bobinnec Y., Fukuda M., and Nishida E. The GTPase Ran regulates chromosome positioning and nuclear envelope assembly in vivo. Curr. Biol. 12 (2002) 503-507
68. Askjaer P., Galy V., Hannak E., and Mattaj I.W. Ran GTPase cycle and importins alpha and beta are essential for spindle formation and nuclear envelope assembly in living Caenorhabditis elegans embryos. Mol. Biol. Cell 13 (2002) 4355-4370
69. Aebi M., Clark M.W., Vijayraghavan U., and Abelson J. A yeast mutant, PRP20, altered in mRNA metabolism and maintenance of the nuclear structure, is defective in a gene homologous to the human gene RCC1 which is involved in the control of chromosome condensation. Mol. Gen. Genet. 224 (1990) 72-80
70. Ohtsubo M., Yoshida T., Seino H., Nishitani H., Clark K.L., Sprague Jr. G.F., Frasch M., and Nishimoto T. Mutation of the hamster cell cycle gene RCC1 is complemented by the homologous genes of Drosophila and S. cerevisiae. EMBO J. 10 (1991) 1265-1273
71. Schlenstedt G., Saavedra C., Loeb J.D., Cole C.N., and Silver P.A. The GTP-bound form of the yeast Ran/TC4 homologue blocks nuclear protein import and appearance of poly(A)+ RNA in the cytoplasm. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 225-229
72. Ryan K.J., McCaffery J.M., and Wente S.R. The Ran GTPase cycle is required for yeast nuclear pore complex assembly. J. Cell Biol. 160 (2003) 1041-1053
73. Clement M., Deshaies F., de Repentigny L., and Belhumeur P. The nuclear GTPase Gsp1p can affect proper telomeric function through the Sir4 protein in Saccharomyces cerevisiae. Mol. Microbiol. 62 (2006) 453-468
74. Hirose E., Mukai M., Shimada A., Nishitani H., Shibata Y., and Nishimoto T. Loss of RanGEF/Pim1 activity abolishes the orchestration of Ran-mediated mitotic cellular events in S. pombe. Genes Cells 11 (2006) 29-46
75. Matsumoto T., and Beach D. Premature initiation of mitosis in yeast lacking RCC1 or an interacting GTPase. Cell 66 (1991) 347-360
76. Dilworth D.J., Tackett A.J., Rogers R.S., Yi E.C., Christmas R.H., Smith J.J., Siegel A.F., Chait B.T., Wozniak R.W., and Aitchison J.D. The mobile nucleoporin Nup2p and chromatin-bound Prp20p function in endogenous NPC-mediated transcriptional control. J. Cell Biol. 171 (2005) 955-965
77. Rosasco-Nitcher S.E., Lan W., Khorasanizadeh S., and Stukenberg P.T. Centromeric Aurora-B activation requires TD-60, microtubules, and substrate priming phosphorylation. Science 319 (2008) 469-472
78. Scheffner M., and Staub O. HECT E3s and human disease. BMC Biochem. 8 Suppl 1 (2007) S6
79. Chong-Kopera H., Inoki K., Li Y., Zhu T., Garcia-Gonzalo F.R., Rosa J.L., and Guan K.L. TSC1 stabilizes TSC2 by inhibiting the interaction between TSC2 and the HERC1 ubiquitin ligase. J. Biol. Chem. 281 (2006) 8313-8316
80. Schwarz S.E., Rosa J.L., and Scheffner M. Characterization of human hect domain family members and their interaction with UbcH5 and UbcH7. J. Biol. Chem. 273 (1998) 12148-12154
81. Belham C., Roig J., Caldwell J.A., Aoyama Y., Kemp B.E., Comb M., and Avruch J. A mitotic cascade of NIMA family kinases. Nercc1/Nek9 activates the Nek6 and Nek7 kinases. J. Biol. Chem. 278 (2003) 34897-34909
82. O'Connell M.J., Krien M.J., and Hunter T. Never say never. The NIMA-related protein kinases in mitotic control. Trends Cell Biol. 13 (2003) 221-228
83. Nigg E.A. Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev., Mol. Cell Biol. 2 (2001) 21-32
84. Smith L.A., Bukanov N.O., Husson H., Russo R.J., Barry T.C., Taylor A.L., Beier D.R., and Ibraghimov-Beskrovnaya O. Development of polycystic kidney disease in juvenile cystic kidney mice: insights into pathogenesis, ciliary abnormalities, and common features with human disease. J. Am. Soc. Nephrol. 17 (2006) 2821-2831
85. Sohara E., Luo Y., Zhang J., Manning D.K., Beier D.R., and Zhou J. Nek8 regulates the expression and localization of polycystin-1 and polycystin-2. J. Am. Soc. Nephrol. 19 (2008) 469-476
86. Hoogenraad C.C., Wulf P., Schiefermeier N., Stepanova T., Galjart N., Small J.V., Grosveld F., de Zeeuw C.I., and Akhmanova A. Bicaudal D induces selective dynein-mediated microtubule minus end-directed transport. EMBO J. 22 (2003) 6004-6015
87. Hadano S., Benn S.C., Kakuta S., Otomo A., Sudo K., Kunita R., Suzuki-Utsunomiya K., Mizumura H., Shefner J.M., Cox G.A., Iwakura Y., Brown Jr. R.H., and Ikeda J.E. Mice deficient in the Rab5 guanine nucleotide exchange factor ALS2/alsin exhibit age-dependent neurological deficits and altered endosome trafficking. Hum. Mol. Genet. 15 (2006) 233-250
88. Devon R.S., Orban P.C., Gerrow K., Barbieri M.A., Schwab C., Cao L.P., Helm J.R., Bissada N., Cruz-Aguado R., Davidson T.L., Witmer J., Metzler M., Lam C.K., Tetzlaff W., Simpson E.M., McCaffery J.M., El-Husseini A.E., Leavitt B.R., and Hayden M.R. Als2-deficient mice exhibit disturbances in endosome trafficking associated with motor behavioral abnormalities. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 9595-9600
89. Lai C., Xie C., McCormack S.G., Chiang H.C., Michalak M.K., Lin X., Chandran J., Shim H., Shimoji M., Cookson M.R., Huganir R.L., Rothstein J.D., Price D.L., Wong P.C., Martin L.J., Zhu J.J., and Cai H. Amyotrophic lateral sclerosis 2-deficiency leads to neuronal degeneration in amyotrophic lateral sclerosis through altered AMPA receptor trafficking. J. Neurosci. 26 (2006) 11798-11806
90. Boylan J.P., and Wright A.F. Identification of a novel protein interacting with RPGR. Hum. Mol. Genet. 9 (2000) 2085-2093
91. Roepman R., Bernoud-Hubac N., Schick D.E., Maugeri A., Berger W., Ropers H.H., Cremers F.P., and Ferreira P.A. The retinitis pigmentosa GTPase regulator (RPGR) interacts with novel transport-like proteins in the outer segments of rod photoreceptors. Hum. Mol. Genet. 9 (2000) 2095-2105
92. Hong D.H., Yue G., Adamian M., and Li T. Retinitis pigmentosa GTPase regulator (RPGRr)-interacting protein is stably associated with the photoreceptor ciliary axoneme and anchors RPGR to the connecting cilium. J. Biol. Chem. 276 (2001) 12091-12099
93. Hong D.H., Pawlyk B.S., Shang J., Sandberg M.A., Berson E.L., and Li T. A retinitis pigmentosa GTPase regulator (RPGR)-deficient mouse model for X-linked retinitis pigmentosa (RP3). Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 3649-3654
94. Linari M., Ueffing M., Manson F., Wright A., Meitinger T., and Becker J. The retinitis pigmentosa GTPase regulator, RPGR, interacts with the delta subunit of rod cyclic GMP phosphodiesterase. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 1315-1320
95. Semov A., Marcotte R., Semova N., Ye X., and Wang E. Microarray analysis of E-box binding-related gene expression in young and replicatively senescent human fibroblasts. Anal. Biochem. 302 (2002) 38-51
96. Scholich K., Pierre S., and Patel T.B. Protein associated with Myc (PAM) is a potent inhibitor of adenylyl cyclases. J. Biol. Chem. 276 (2001) 47583-47589
97. Pierre S.C., Hausler J., Birod K., Geisslinger G., and Scholich K. PAM mediates sustained inhibition of cAMP signaling by sphingosine-1-phosphate. EMBO J. 23 (2004) 3031-3040
98. Gao X., and Patel T.B. Histidine residues 912 and 913 in protein associated with Myc are necessary for the inhibition of adenylyl cyclase activity. Mol. Pharmacol. 67 (2005) 42-49
99. Jiao X., Trifillis P., and Kiledjian M. Identification of target messenger RNA substrates for the murine deleted in azoospermia-like RNA-binding protein. Biol. Reprod. 66 (2002) 475-485
100. Collier B., Gorgoni B., Loveridge C., Cooke H.J., and Gray N.K. The DAZL family proteins are PABP-binding proteins that regulate translation in germ cells. EMBO J. 24 (2005) 2656-2666
101. Fulga T.A., and Van Vactor D. Synapses and growth cones on two sides of a highwire. Neuron 57 (2008) 339-344
102. Ehnert C., Tegeder I., Pierre S., Birod K., Nguyen H.V., Schmidtko A., Geisslinger G., and Scholich K. Protein associated with Myc (PAM) is involved in spinal nociceptive processing. J. Neurochem. 88 (2004) 948-957
103. Burgess R.W., Peterson K.A., Johnson M.J., Roix J.J., Welsh I.C., and O'Brien T.P. Evidence for a conserved function in synapse formation reveals Phr1 as a candidate gene for respiratory failure in newborn mice. Mol. Cell. Biol. 24 (2004) 1096-1105
104. D'Souza J., Hendricks M., Le Guyader S., Subburaju S., Grunewald B., Scholich K., and Jesuthasan S. Formation of the retinotectal projection requires Esrom, an ortholog of PAM (protein associated with Myc). Development 132 (2005) 247-256
105. Le Guyader S., Maier J., and Jesuthasan S. Esrom, an ortholog of PAM (protein associated with c-myc), regulates pteridine synthesis in the zebrafish. Dev. Biol. 277 (2005) 378-386
106. Wan H.I., DiAntonio A., Fetter R.D., Bergstrom K., Strauss R., and Goodman C.S. Highwire regulates synaptic growth in Drosophila. Neuron 26 (2000) 313-329
107. Wu C., Wairkar Y.P., Collins C.A., and DiAntonio A. Highwire function at the Drosophila neuromuscular junction: spatial, structural, and temporal requirements. J. Neurosci. 25 (2005) 9557-9566
108. Zhen M., Huang X., Bamber B., and Jin Y. Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26 (2000) 331-343
109. Schaefer A.M., Hadwiger G.D., and Nonet M.L. rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26 (2000) 345-356
110. DiAntonio A., Haghighi A.P., Portman S.L., Lee J.D., Amaranto A.M., and Goodman C.S. Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412 (2001) 449-452
111. Abrams B., Grill B., Huang X., and Jin Y. Cellular and molecular determinants targeting the Caenorhabditis elegans PHR protein RPM-1 to perisynaptic regions. Dev. Dyn. 237 (2008) 630-639
112. Collins C.A., Wairkar Y.P., Johnson S.L., and DiAntonio A. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51 (2006) 57-69
113. Wu C., Daniels R.W., and Diantonio A. DFsn collaborates with Highwire to down-regulate the Wallenda/DLK kinase and restrain synaptic terminal growth. Neural Develop. 2 (2007) 16
114. Liao E.H., Hung W., Abrams B., and Zhen M. An SCF-like ubiquitin ligase complex that controls presynaptic differentiation. Nature 430 (2004) 345-350
115. Nakata K., Abrams B., Grill B., Goncharov A., Huang X., Chisholm A.D., and Jin Y. Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120 (2005) 407-420
116. Grill B., Bienvenut W.V., Brown H.M., Ackley B.D., Quadroni M., and Jin Y. C. elegans RPM-1 regulates axon termination and synaptogenesis through the Rab GEF GLO-4 and the Rab GTPase GLO-1. Neuron 55 (2007) 587-601
117. McCabe B.D., Hom S., Aberle H., Fetter R.D., Marques G., Haerry T.E., Wan H., O'Connor M.B., Goodman C.S., and Haghighi A.P. Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron 41 (2004) 891-905
118. Hermann G.J., Schroeder L.K., Hieb C.A., Kershner A.M., Rabbitts B.M., Fonarev P., Grant B.D., and Priess J.R. Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol. Biol. Cell 16 (2005) 3273-3288
119. Ma J., Plesken H., Treisman J.E., Edelman-Novemsky I., and Ren M. Lightoid and Claret: a rab GTPase and its putative guanine nucleotide exchange factor in biogenesis of Drosophila eye pigment granules. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 11652-11657
120. Heras B., and Drobak B.K. PARF-1: an Arabidopsis thaliana FYVE-domain protein displaying a novel eukaryotic domain structure and phosphoinositide affinity. J. Exp. Bot. 53 (2002) 565-567
121. Kliebenstein D.J., Lim J.E., Landry L.G., and Last R.L. Arabidopsis UVR8 regulates ultraviolet-B signal transduction and tolerance and contains sequence similarity to human regulator of chromatin condensation 1. Plant Physiol. 130 (2002) 234-243
122. Brown B.A., Cloix C., Jiang G.H., Kaiserli E., Herzyk P., Kliebenstein D.J., and Jenkins G.I. A UV-B-specific signaling component orchestrates plant UV protection. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 18225-18230
123. Kaiserli E., and Jenkins G.I. UV-B promotes rapid nuclear translocation of the Arabidopsis UV-B specific signaling component UVR8 and activates its function in the nucleus. Plant Cell (2007)
124. Gogendeau D., Keller A.M., Yanagi A., Cohen J., and Koll F. Nd6p, a novel protein with RCC1-like domains involved in exocytosis in Paramecium tetraurelia. Eukaryot. Cell 4 (2005) 2129-2139
125. Hadano S., Hand C.K., Osuga H., Yanagisawa Y., Otomo A., Devon R.S., Miyamoto N., Showguchi-Miyata J., Okada Y., Singaraja R., Figlewicz D.A., Kwiatkowski T., Hosler B.A., Sagie T., Skaug J., Nasir J., Brown Jr. R.H., Scherer S.W., Rouleau G.A., Hayden M.R., and Ikeda J.E. A gene encoding a putative GTPase regulator is mutated in familial amyotrophic lateral sclerosis 2. Nat. Genet. 29 (2001) 166-173
126. Yang Y., Hentati A., Deng H.X., Dabbagh O., Sasaki T., Hirano M., Hung W.Y., Ouahchi K., Yan J., Azim A.C., Cole N., Gascon G., Yagmour A., Ben-Hamida M., Pericak-Vance M., Hentati F., and Siddique T. The gene encoding alsin, a protein with three guanine-nucleotide exchange factor domains, is mutated in a form of recessive amyotrophic lateral sclerosis. Nat. Genet. 29 (2001) 160-165
127. Gros-Louis F., Gaspar C., and Rouleau G.A. Genetics of familial and sporadic amyotrophic lateral sclerosis. Biochim. Biophys. Acta 1762 (2006) 956-972
128. Chandran J., Ding J., and Cai H. Alsin and the molecular pathways of amyotrophic lateral sclerosis. Mol. Neurobiol. 36 (2007) 224-231
129. Cai H., Lin X., Xie C., Laird F.M., Lai C., Wen H., Chiang H.C., Shim H., Farah M.H., Hoke A., Price D.L., and Wong P.C. Loss of ALS2 function is insufficient to trigger motor neuron degeneration in knock-out mice but predisposes neurons to oxidative stress. J. Neurosci. 25 (2005) 7567-7574
130. Deng H.X., Zhai H., Fu R., Shi Y., Gorrie G.H., Yang Y., Liu E., Dal Canto M.C., Mugnaini E., and Siddique T. Distal axonopathy in an alsin-deficient mouse model. Hum. Mol. Genet. 16 (2007) 2911-2920
131. Kanekura K., Hashimoto Y., Niikura T., Aiso S., Matsuoka M., and Nishimoto I. Alsin, the product of ALS2 gene, suppresses SOD1 mutant neurotoxicity through RhoGEF domain by interacting with SOD1 mutants. J. Biol. Chem. 279 (2004) 19247-19256
132. Kanekura K., Hashimoto Y., Kita Y., Sasabe J., Aiso S., Nishimoto I., and Matsuoka M. A Rac1/phosphatidylinositol 3-kinase/Akt3 anti-apoptotic pathway, triggered by AlsinLF, the product of the ALS2 gene, antagonizes Cu/Zn-superoxide dismutase (SOD1) mutant-induced motoneuronal cell death. J. Biol. Chem. 280 (2005) 4532-4543
133. Erie E.A., Shim H., Smith A.L., Lin X., Keyvanfar K., Xie C., Chen J., and Cai H. Mice deficient in the ALS2 gene exhibit lymphopenia and abnormal hematopietic function. J. Neuroimmunol. 182 (2007) 226-231
134. Provinciali L., Laurenzi M.A., Vesprini L., Giovagnoli A.R., Bartocci C., Montroni M., Bagnarelli P., Clementi M., and Varaldo P.E. Immunity assessment in the early stages of amyotrophic lateral sclerosis: a study of virus antibodies and lymphocyte subsets. Acta Neurol. Scand. 78 (1988) 449-454
135. Bowers A.J., and Boylan J.F. Nek8, a NIMA family kinase member, is overexpressed in primary human breast tumors. Gene 328 (2004) 135-142
136. Torres V.E., and Harris P.C. Mechanisms of disease: autosomal dominant and recessive polycystic kidney diseases. Nat. Clin. Prac. 2 (2006) 40-55 (quiz 55)
137. Trapp M.L., Galtseva A., Manning D.K., Beier D.R., Rosenblum N.D., and Quarmby L.M. Defects in ciliary localization of Nek8 is associated with cystogenesis. Pediatr. Nephrol. (Berlin, Germany) 23 (2008) 377-387
138. Natoli T.A., Gareski T.C., Dackowski W.R., Smith L., Bukanov N.O., Russo R.J., Husson H., Matthews D., Piepenhagen P., and Ibraghimov-Beskrovnaya O. Pkd1 and Nek8 mutations affect cell-cell adhesion and cilia in cysts formed in kidney organ cultures. Am. J. Physiol. 294 (2008) F73-F83
139. Otto E.A., Trapp M.L., Schultheiss U.T., Helou J., Quarmby L.M., and Hildebrandt F. NEK8 mutations affect ciliary and centrosomal localization and may cause nephronophthisis. J. Am. Soc. Nephrol. 19 (2008) 587-592
140. Cai Y., and Somlo S. Too much of a good thing: does Nek8 link polycystic kidney disease and nephronophthisis?. J. Am. Soc. Nephrol. 19 (2008) 418-420
141. Walkowicz M., Ji Y., Ren X., Horsthemke B., Russell L.B., Johnson D., Rinchik E.M., Nicholls R.D., and Stubbs L. Molecular characterization of radiation- and chemically induced mutations associated with neuromuscular tremors, runting, juvenile lethality, and sperm defects in jdf2 mice. Mamm. Genome 10 (1999) 870-878
142. Ji Y., Walkowicz M.J., Buiting K., Johnson D.K., Tarvin R.E., Rinchik E.M., Horsthemke B., Stubbs L., and Nicholls R.D. The ancestral gene for transcribed, low-copy repeats in the Prader-Willi/Angelman region encodes a large protein implicated in protein trafficking, which is deficient in mice with neuromuscular and spermiogenic abnormalities. Hum. Mol. Genet. 8 (1999) 533-542
143. Ji Y., Rebert N.A., Joslin J.M., Higgins M.J., Schultz R.A., and Nicholls R.D. Structure of the highly conserved HERC2 gene and of multiple partially duplicated paralogs in human. Genome Res. 10 (2000) 319-329
144. Amos-Landgraf J.M., Ji Y., Gottlieb W., Depinet T., Wandstrat A.E., Cassidy S.B., Driscoll D.J., Rogan P.K., Schwartz S., and Nicholls R.D. Chromosome breakage in the Prader-Willi and Angelman syndromes involves recombination between large, transcribed repeats at proximal and distal breakpoints. Am. J. Hum. Genet. 65 (1999) 370-386
145. Nicholls R.D., and Knepper J.L. Genome organization, function, and imprinting in Prader-Willi and Angelman syndromes. Annu. Rev. Genomics Hum. Genet. 2 (2001) 153-175
146. Sturm R.A., Duffy D.L., Zhao Z.Z., Leite F.P., Stark M.S., Hayward N.K., Martin N.G., and Montgomery G.W. A single SNP in an evolutionary conserved region within intron 86 of the HERC2 gene determines human blue-brown eye color. Am. J. Hum. Genet. 82 (2008) 424-431
147. Kayser M., Liu F., Janssens A.C., Rivadeneira F., Lao O., van Duijn K., Vermeulen M., Arp P., Jhamai M.M., van Ijcken W.F., den Dunnen J.T., Heath S., Zelenika D., Despriet D.D., Klaver C.C., Vingerling J.R., de Jong P.T., Hofman A., Aulchenko Y.S., Uitterlinden A.G., Oostra B.A., and van Duijn C.M. Three genome-wide association studies and a linkage analysis identify HERC2 as a human iris color gene. Am. J. Hum. Genet. 82 (2008) 411-423
148. Eiberg H., Troelsen J., Nielsen M., Mikkelsen A., Mengel-From J., Kjaer K.W., and Hansen L. Blue eye color in humans may be caused by a perfectly associated founder mutation in a regulatory element located within the HERC2 gene inhibiting OCA2 expression. Hum. Genet. 123 (2008) 177-187
149. Yuan W., and Krug R.M. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 20 (2001) 362-371
150. Krug R.M., Yuan W., Noah D.L., and Latham A.G. Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 309 (2003) 181-189
151. Wang X.F., Wang D., Zhu W., Delrahim K.K., Dolnak D., and Rapaport M.H. Studies characterizing 60 kDa autoantibodies in subjects with schizophrenia. Biol. Psychiatry 53 (2003) 361-375
152. Merla G., Ucla C., Guipponi M., and Reymond A. Identification of additional transcripts in the Williams-Beuren syndrome critical region. Hum. Genet. 110 (2002) 429-438
153. Ouyang X.M., Xia X.J., Verpy E., Du L.L., Pandya A., Petit C., Balkany T., Nance W.E., and Liu X.Z. Mutations in the alternatively spliced exons of USH1C cause non-syndromic recessive deafness. Hum. Genet. 111 (2002) 26-30
154. Mabuchi H., Fujii H., Calin G., Alder H., Negrini M., Rassenti L., Kipps T.J., Bullrich F., and Croce C.M. Cloning and characterization of CLLD6, CLLD7, and CLLD8, novel candidate genes for leukemogenesis at chromosome 13q14, a region commonly deleted in B-cell chronic lymphocytic leukemia. Cancer Res. 61 (2001) 2870-2877
155. Mertens D., Wolf S., Schroeter P., Schaffner C., Dohner H., Stilgenbauer S., and Lichter P. Down-regulation of candidate tumor suppressor genes within chromosome band 13q14.3 is independent of the DNA methylation pattern in B-cell chronic lymphocytic leukemia. Blood 99 (2002) 4116-4121
156. Solomou E.E., Sfikakis P.P., Kotsi P., Papaioannou M., Karali V., Vervessou E., Hoffbrand A.V., and Panayiotidis P. 13q deletion in chronic lymphocytic leukemia: characterization of E4.5, a novel chromosome condensation regulator-like guanine nucleotide exchange factor. Leuk. Lymphoma 44 (2003) 1579-1585
157. Latil A., Chene L., Mangin P., Fournier G., Berthon P., and Cussenot O. Extensive analysis of the 13q14 region in human prostate tumors: DNA analysis and quantitative expression of genes lying in the interval of deletion. Prostate 57 (2003) 39-50
158. Clamp M., Cuff J., Searle S.M., and Barton G.J. The Jalview Java alignment editor. Bioinformatics 20 (2004) 426-427
159. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
160. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882