Distinct gene expression profiles and reduced JNK signaling in retinitis pigmentosa caused by RP1 mutations

Human Molecular Genetics

Volumn 14, Issue 19, 2005, Pages 2945-2958

  Liu, Jiewu ^a   Huang, Qian ^a   Higdon, Jason ^a   Liu, Wei ^a   Xie, Tao ^a   Yamashita, Tetsuji ^a   Cheon, Kyeogmi ^a   Cheng, Cheng ^a   Zuo, Jian ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; COMPLEMENTARY DNA; DOUBLECORTIN; GENE PRODUCT; MICROTUBULE ASSOCIATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN C JUN; PROTEIN RP1; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; URACIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; FEMALE; GENE CLUSTER; GENE DISRUPTION; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC IDENTIFICATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERMETHOD COMPARISON; MALE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RETINA; RETINITIS PIGMENTOSA; SERIAL ANALYSIS OF GENE EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; DOWN-REGULATION; EYE PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MICE, MUTANT STRAINS; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORIC DIESTER HYDROLASES; RETINITIS PIGMENTOSA; ROD OUTER SEGMENTS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS;

EID: 26444501080     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddi325     Document Type: Article

References (76)

1. Jacobson, S.G., Cideciyan, A.V., Iannaccone, A., Weleber, R.G., Fishman, G.A., Maguire, A.M., Affatigato, L.M., Bennett, J., Pierce, E.A., Danciger, M., Farber, D.B. and Stone, E.M. (2000) Disease expression of RP1 mutations causing autosomal dominant retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci., 41, 1898-1908.
2. Guillonneau, X., Piriev, N.I., Danciger, M., Kozak, C.A., Cideciyan, A.V., Jacobson, S.G. and Farber, D.B.(1999) A nonsense mutation in a novel gene is associated with retinitis pigmentosa in a family linked to the RP1 locus. Hum. Mol. Genet., 8, 1541-1546.
3. Pierce, E.A., Quinn, T., Meehan, T., McGee, T.L., Berson, E.L. and Dryja, T.P. (1999) Mutations in a gene encoding a new oxygen-regulated photoreceptor protein cause dominant retinitis pigmentosa. Nat. Genet., 22, 248-254.
4. Sullivan, L.S., Heckenlively, J.R., Bowne, S.J., Zuo, J., Hide, W.A., Gal, A., Denton, M., Inglehearn, C.F., Blanton, S.H. and Daiger, S.P. (1999) Mutations in a novel retina-specific gene cause autosomal dominant retinitis pigmentosa. Nat. Genet., 22, 255-259.
5. Gleeson, J.G., Lin, P.T., Flanagan, L.A. and Walsh, C.A. (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23, 257-271.
6. des Portes, V., Pinard, J.M., Billuart, P., Vinet, M.C., Koulakoff, A., Carrie, A., Gelot, A., Dupuis, E., Motte, J., Berwald-Netter, Y. et al. (1998) A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell, 92, 51-61.
7. Hong, D.H., Pawlyk, B., Sokolov, M., Strissel, K.J., Yang, J., Tulloch, B., Wright, A.F., Arshavsky, V.Y. and Li, T. (2003) RPGR isoforms in photoreceptor connecting cilia and the transitional zone of motile cilia. Invest. Ophthalmol. Vis. Sci., 44, 2413-2421.
8. Liu, Q., Zhou, J., Daiger, S.P., Farber, D.B., Heckenlively, J.R., Smith, J.E., Sullivan, L.S., Zuo, J., Milam, A.H. and Pierce, E.A. (2002) Identification and subcellular localization of the RP1 protein in human and mouse photoreceptors. Invest. Ophthalmol. Vis. Sci., 43, 22-32.
9. Gao, J., Cheon, K., Nusinowitz, S., Liu, Q., Bei, D., Atkins, K., Azimi, A., Daiger, S.P., Farber, D.B., Heckenlively, J.R. et al. (2002) Progressive photoreceptor degeneration, outer segment dysplasia, and rhodopsin mislocalization in mice with targeted disruption of the retinitis pigmentosa-1 (Rp1) gene. Proc. Natl Acad. Sci. USA 99, 5698-5703.
10. Liu, Q., Lyubarskv, A., Skalet, J.H., Pugh, E.N., Jr and Pierce, E.A. (2003) RP1 is required for the correct stacking of outer segment discs. Invest. Ophthalmol. Vis. Sci., 44, 4171-4183.
11. Liu, Q., Zuo, J. and Pierce, E.A. (2004) The retinitis pigmentosa 1 protein is a photoreceptor microtubule-associated protein. J. Neurosci., 24, 6427-6436.
12. Reiner, O., Gdalyahu, A., Ghosh, I., Levy, T., Sapoznik, S., Nir, R. and Sapir, T. (2004) DCX's phosphorylation by not just another kinase (JNK). Cell Cycle, 3, 747-757.
13. Xia, Y. and Karin, M. (2004) The control of cell motility and epithelial morphogenesis by Jun kinases. Trends Cell Biol., 14, 94-101.
14. Davis, R.J. (2000) Signal transduction by the JNK group of MAP kinases. Cell, 103, 239-252.
15. Weston, C.R. and Davis, R.J. (2002) The JNK signal transduction pathway. Curr. Opin. Genet. Dev., 12, 14-21.
16. Dufour, E.M., Nandrot, E., Marchant, D., Van Den, B.L., Gadin, S., Issilame, M., Dufier, J.L., Marsac, C., Carper, D., Menasche, M. and Abitbol, M. (2003) Identification of novel genes and altered signaling pathways in the retinal pigment epithelium during the Royal College of Surgeons rat retinal degeneration. Neurobiol. Dis., 14, 166-180.
17. Roth, S., Shaikh, A.R., Hennelly, M.M., Li, Q., Bindokas, V. and Graham, C.E. (2003) Mitogen-activated protein kinases and retinal ischemia. Invest. Ophthalmol. Vis. Sci., 44, 5383-5395.
18. Tezel, G., Chauhan, B.C., LeBlanc, R.P. and Wax, M.B. (2003) Immunohistochemical assessment of the glial mitogen-activated protein kinase activation in glaucoma. Invest. Ophthalmol. Vis. Sci., 44, 3025-3033.
19. Tezel, G., Yang, X., Yang, J. and Wax, MB. (2004) Role of tumor necrosis factor receptor-1 in the death of retinal ganglion cells following optic nerve crush injury in mice. Brain Res., 996, 202-212.
20. Yoshida, K., Behrens, A., Le Niculescu, H., Wagner, E.F., Harada, T., Imaki, J., Ohno, S. and Karin, M. (2002) Amino-terminal phosphorylation of c-Jun regulates apoptosis in the retinal ganglion cells by optic nerve transection. Invest. Ophthalmol. Vis. Sci., 43, 1631-1635.
21. Rich, K.A., Zhan, Y. and Blanks, J.C. (1997) Aberrant expression of c-Fos accompanies photoreceptor cell death in the rd mouse. J. Neurobiol., 32, 593-612.
22. Dorrell, M.I., Aguilar, E., Weber, C. and Friedlander, M. (2004) Global gene expression analysis of the developing postnatal mouse retina. Invest. Ophthalmol. Vis. Sci., 45, 1009-1019.
23. Cheng, C., Pounds, S.B., Boyett, I.M., Pei, D., Kuo, M.L. and Roussel, M.F. (2004) Statistical significance threshold criteria for analysis of microarray gene expression data. Stat. Appl. Genet. Mol. Biol., 3, Article 36, URL: http//www.bepress.com/sagmb/vol3/iss1/art36.
24. Blackshaw, S., Fraioli, R.E., Furukawa, T. and Cepko, C.L. (2001) Comprehensive analysis of photoreceptor gene expression and the identification of candidate retinal disease genes. Cell, 107 579-589.
25. Chowers, I., Liu, D., Farkas, R.H., Gunatilaka, T.L., Hackam, A.S., Bernstein, S.L., Campochiaro, P.A., Parmigiani, G. and Zack, D.J. (2003) Gene expression variation in the adult human retina. Hum. Mol. Genet. 12, 2881-2893.
26. Hackam, A.S., Strom, R., Liu, D., Qian, J., Wang. C., Otteson, D., Gunatilaka, T., Farkas, R.H., Chowers, L, Kageyama, M. et al. (2004) Identification of gene expression changes associated with the progression of retinal degeneration in the rd1 mouse. Invest. Ophthalmol. Vis. Sci., 45, 2929-2942.
27. Hosack, D.A., Dennis, G., Jr, Sherman, B.T., Lane, H.C. and Lempicki, R.A. (2003) Identifying biological themes within lists of genes with EASE. Genome Biol., 4, R70.
28. Yoshida, S., Mears, A.J., Friedman, J.S., Carter, T., He, S., Oh, E., Jing, Y., Farjo. R., Fleury, G., Barlow, C., Hero, A.O. and Swaroop, A. (2004) Expression profiling of the developing and mature Nrl-/- mouse retina: Identification of retinal disease candidates and transcriptional regulatory targets of Nrl. Hum. Mol. Genet., 13, 1487-1503.
29. Furukawa, T., Morrow, E.M., Li, T., Davis, F.C. and Cepko, C.L. (1999) Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat. Genet., 23, 466-470.
30. Mears, A.J., Kondo, M., Swain, P.K., Takada, Y., Bush, R.A., Saunders, T.L., Sieving, P.A. and Swaroop, A. (2001) Nrl is required for rod photoreceptor development. Nat. Genet., 29, 447-452.
31. Malik, S., Wallberg, A.E., Kang, Y.K. and Roeder, R.G. (2002) TRAP/SMCC/ mediator-dependent transcriptional activation from DNA and chromatin templates by orphan nuclear receptor hepatocyte nuclear factor 4. Mol. Cell. Biol., 22, 5626-5637.
32. Oster, S.K., Ho, C.S., Soucie, E.L. and Penn, L.Z. (2002) The myc oncogene: MarvelouslY complex. Adv. Cancer Res., 84, 81-154.
33. Wilson, H.L., Wilson, S.A., Surprenant, A. and North, R.A. (2002) Epithelial membrane proteins induce membrane blebbing and interact with the P2X7 receptor C terminus. J. Biol. Chem., 277, 34017-34023.
34. Naik, M.U., Mousa, S.A., Parkos, C.A. and Naik, U.P. (2003) Signaling through JAM-1 and alphavbeta3 is required for the angiogenic action of bFGF: Dissociation of the JAM-1 and alphavbeta3 complex. Blood, 102, 2108-2114.
35. Zhou, Q., Ruiz-Lozano, P., Martone, M.E. and Chen, J. (1999) Cypher, a striated muscle-restricted PDZ and LIM domain-containing protein, binds to alpha-actinin-2 and protein kinase C. J. Biol. Chem., 274 19807-19813.
36. Cao, M.Y., Shinjo, F., Heinrichs, S., Soh, J.W., Jongstra-Bilen, J. and Jongstra, J. (2001) Inhibition of anti-IgM-induced translocation of protein kinase C beta 1 inhibits ERK2 activation and increases apoptosis. J. Biol. Chem., 276, 24506-24510.
37. Zhang, G. and Ghosh, S. (2002) Negative regulation of toll-like receptor-mediated signaling by Tollip. J. Biol. Chem., 277, 7059-7065.
38. Xu, W., Shy, M., Kamholz, J., Elferink, L., Xu, G., Lilien, J. and Balsamo, J. (2001) Mutations in the cytoplasmic domain of P0 reveal a role for PKC-mediated phosphorylation in adhesion and myelination. J. Cell Biol., 155, 439-446.
39. Tucker, R.P. and Matus, A.I. (1988) Microtubule-associated proteins characteristic of embryonic brain are found in the adult mammalian retina. Dev. Biol., 130, 423-434.
40. Berling, B., Wille, H., Roll, B., Mandelkow, E.M., Garner, C. and Mandelkow, E. (1994) Phosphorylation of microtubule-associated proteins MAP2a,b and MAP2c at Ser136 by proline-directed kinases in vivo and in vitro. Eur. J. Cell Biol., 64, 120-130.
41. Chang, L., Jones, Y., Ellisman, M.H., Goldstein, L.S. and Karin, M. (2003) JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev. Cell, 4, 521-533.
42. Chang, B., Hawes, N.L., Hurd, R.E., Davisson, M.T., Nusinowitz, S. and Heckenlively, J.R. (2002) Retinal degeneration mutants in the mouse. Vision Res., 42, 517-525.
43. Lem, J., Krasnoperova, N.V., Calvert, P.D., Kosaras, B., Cameron, D.A., Nicolo, M., Makino, C.L. and Sidman, R.L. (1999) Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc. Natl Acad. Sci. USA, 96, 736-741.
44. Humphries, M.M., Rancourt, D., Farrar, G.J., Kenna, P., Hazel, M., Bush, RA., Sieving, P.A., Sheils, D.M., McNally, N., Creighton, P. et al. (1997) Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat. Genet., 15, 216-219.
45. Akhmedov, N.B., Piriev, N.I., Chang, B., Rapoport, A.L., Hawes, N.L., Nishina, P.M., Nusinowitz, S., Heckenlively, J.R., Roderick, T.H., Kozak, C.A. et al. (2000) A deletion in a photoreceptor-specific nuclear receptor mRNA causes retinal degeneration in the rd7 mouse. Proc. Natl Acad. Sci. USA, 97, 5551-5556.
46. Clarke, G., Goldberg, A.F., Vidgen, D., Collins, L., Ploder, L., Schwarz, L., Molday, L.L., Rossant, J., Szel, A., Molday, R.S., Birch, D.G. and McInnes, R.R. (2000) Rom-1 is required for rod photoreceptor viability and the regulation of disk morphogenesis. Nat. Genet., 25, 67-73.
47. Sanyal, S., De Ruiter, A. and Hawkins, R.K. (1980) Development and degeneration of retina in rds mutant mice: Light microscopy. J. Comp. Neurol., 194, 193-207.
48. Fernandez-Gonzalez, A., La Spada, A.R., Treadaway, J., Higdon, J.C., Harris, B.S., Sidman, R.L., Morgan, J.I. and Zuo, J. (2002) Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science, 295, 1904-1906.
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. Liu, X., Udovichenko, I.P., Brown, S.D., Steel, K.P. and Williams, D.S. (1999) Myosin VIIa participates in opsin transport through the photoreceptor cilium. J. Neurosci., 19, 6267-6274.
51. Ikeda, S., Shiva, N., Ikeda, A., Smith, R.S., Nusinowitz, S., Yan, G., Lin, T.R., Chu, S., Heckenlively, J.R., North, M.A. et al. (2000) Retinal degeneration but not obesity is observed in null mutants of the tubby-like protein 1 gene. Hum. Mol. Genet., 9, 155-163.
52. Willingham, S., Outeiro, T.F., DeVit, M.J., Lindquist, S.L. and Muchowski, P.J. (2003) Yeast genes that enhance the toxicity of a mutant huntingtin fragment or alpha-synuclein. Science, 302, 1769-1772.
53. Cheok, M.H., Yang, W., Pui, C.H., Downing, J.R., Cheng, C., Naeve, C.W., Relling, M.V. and Evans, W.E. (2003) Treatment-specific changes in gene expression discriminate in vivo drug response in human leukemia cells. Nat. Genet., 34, 85-90.
54. Ip, Y.T. and Davis. R.J. (1998) Signal transduction by the c-Jun N-terminal kinase (JNK) - from inflammation to development. Curr. Opin. Cell Biol., 10, 205-219.
55. Gallo, K.A. and Johnson, G.L. (2002) Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat. Rev. Mol. Cell Biol., 3, 663-672.
56. Tafolla, E., Wang, S., Wong, B., Leong, J. and Kapila, Y.L. (2005) JNK1 and JNK2 oppositely regulate p53 in signaling linked to apoptosis triggered by an altered fibronectin matrix: JNK links FAK and p53. J. Biol. Chem., 280, 19992-19999.
57. Davis, R.J. (2000) Signal transduction by the JNK group of MAP kinases. Cell, 103, 239-252.
58. Balasubramanian, N. and Slepak, V.Z. (2003) Light-mediated activation of Rac-1 in photoreceptor outer segments. Curr. Biol., 13, 1306-1310.
59. Ridley, A.J. (2001) Rho family proteins: Coordinating cell responses. Trends Cell Biol., 11, 471-477.
60. Deretic, D., Huber, L.A., Ransom, N., Mancini, M., Simons, K. and Papermaster, D.S. (1995) rab8 in retinal photoreceptors may participate in rhodopsin transport and in rod outer segment disk morphogenesis. J. Cell Sci., 108, 215-224.
61. Moritz, O.L., Tam, B.M., Hurd, L.L., Peranen, J., Deretic, D. and Papermaster, D.S. (2001) Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol. Biol. Cell, 12, 2341-2351.
62. Keyse, S.M. (2000) Protein phosphatases and the regulation of mitogen-activated protein kinase signalling. Curr. Opin. Cell Biol. 12, 186-192.
63. Marszalek, J.R., Liu, X., Roberts, E.A., Chui, D., Marth, J.D., Williams, D.S. and Goldstein, L.S. (2000) Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell, 102, 175-187.
64. Gdalyahu, A., Ghosh, I., Levy, T., Sapir, T., Sapoznik, S., Fishler, Y., Azoulai, D. and Reiner, O. (2004) DCX, a new mediator of the JNK pathway. EMBO J., 23, 823-832.
65. Schaar, B.T., Kinoshita, K. and McConnell, S.K. (2004) Doublecortin microtubule affinity is regulated by a balance of kinase and phosphatase activity at the leading edge of migrating neurons. Neuron, 41 203-213.
66. Tanaka, T., Serneo, F.F., Tseng, H.C., Kulkarni, A.B., Tsai, L.H. and Gleeson, J.G. (2004) Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron, 41, 215-227.
67. Songyang, Z., Lu, K.P., Kwon, Y.T., Tsai, L.H., Filhol, O., Cochet, C., Brickey, D.A., Soderling, T.R., Bartleson, C., Graves, D.J. et al. (1996) A structural basis for substrate specificities of protein Ser/Thr kinases: Primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and Erk1. Mol. Cell. Biol., 16, 6486-6493.
68. Morrison, D.K. and Davis, R.J. (2003) Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu. Rev. Cell Dev. Biol. 19, 91-118.
69. Kuan, C.Y., Yang, D.D., Samanta Roy, D.R., Davis, R.J., Rakic, P. and Flavell, R.A. (1999) The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 22, 667-676.
70. Sabapathy, K., Jochum, W., Hochedlinger, K., Chang, L., Karin, M. and Wagner, E.F. (1999) Defective neural tube morphogenesis and altered apoptosis in the absence of both JNK1 and JNK2.Mech. Dev., 89 115-124.
71. Yang, D.D., Kuan, C.Y., Whitmarsh, A.J., Rincon, M., Zheng, T.S., Davis, R.J., Rakic, P. and Flavell, R.A. (1997) Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature, 389, 865-870.
72. Behrens, A., Sibilia, M. and Wagner, E.F. (1999) Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet., 21, 326-329.
73. Ito, T., Deng, X., Carr, B. and May, W.S. (1997) Bcl-2 phosphorylation required for anti-apoptosis function. J. Biol. Chem., 272, 11671-11673.
74. Yamamoto, K., Ichijo, H. and Korsmeyer, S.J. (1999) BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol., 19, 8469-8478.
75. Chang, H.Y. and Ready, D.F. (2000) Rescue of photoreceptor degeneration in rhodopsin-null Drosophila mutants by activated Rac1. Science 290, 1978-1980.
76. Liberman, M.C., Gao, J., He. D.Z., Wu, X., Jia, S. and Zuo, J. (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature, 419, 300-304.