Neuroprotection resulting from insufficiency of RANBP2 is associated with the modulation of protein and lipid homeostasis of functionally diverse but linked pathways in response to oxidative stress

DMM Disease Models and Mechanisms

Volumn 3, Issue 9-10, 2010, Pages 595-604

  Cho, Kyoung In ^a   Yi, Haiqing ^a   Tserentsoodol, Nomingerel ^a   Searle, Kelly ^a   Ferreira, Paulo A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 1; CHOLESTEROL; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EXPORTIN 5; FATTY ACID; LIPID; ORPHAN NUCLEAR RECEPTOR; PROTEIN; PROTEIN UBC9;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENOTYPE; HOMEOSTASIS; IN VIVO STUDY; LIPOPHILICITY; MOUSE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA; UPREGULATION;

ANIMALS; CHOLESTEROL; COUP TRANSCRIPTION FACTOR I; CYTOPROTECTION; FATTY ACIDS; HAPLOINSUFFICIENCY; HOMEOSTASIS; LIGHT; LIPID METABOLISM; MICE; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; NUCLEAR PORE COMPLEX PROTEINS; OXIDATIVE STRESS; PROTEIN BINDING; PROTEIN ISOFORMS; RETINAL NEURONS; RETINAL PIGMENT EPITHELIUM; SIGNAL TRANSDUCTION; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATED PROTEINS;

EID: 77956553887     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.004648     Document Type: Article

References (79)

1. Alkuraya, F. S., Saadi, I., Lund, J. J., Turbe-Doan, A., Morton, C. C. and Maas, R. L. (2006). SUMO1 haploinsufficiency leads to cleft lip and palate. Science 313, 1751.
2. Andersen, J. K. (2004). Oxidative stress in neurodegeneration: cause or consequence? Nat. Med. 10, S18-S25. (Pubitemid 38901863)
3. Aslanukov, A., Bhowmick, R., Guruju, M., Oswald, J., Raz, D., Bush, R. A., Sieving, P. A., Lu, X., Bock, C. B. and Ferreira, P. A. (2006). RanBP2 modulates Cox11 and Hexokinase I activities and haploinsufficiency of RanBP2 causes deficits in glucose metabolism. PLoS Genet. 2, e177.
4. Ayaydin, F. and Dasso, M. (2004). Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol. Biol. Cell 15, 5208-5218. (Pubitemid 39564718)
5. Bazan, N. G. (2006). Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors. Trends Neurosci. 29, 263-271.
6. Bermingham-McDonogh, O., McCabe, K. L. and Reh, T. A. (1996). Effects of GGF/neuregulins on neuronal survival and neurite outgrowth correlate with erbB2/neu expression in developing rat retina. Development 122, 1427-1438.
7. Bernad, R., van der Velde, H., Fornerod, M. and Pickersgill, H. (2004). Nup358/RanBP2 attaches to the nuclear pore complex via association with Nup88 and Nup214/CAN and plays a supporting role in CRM1-mediated nuclear protein export. Mol. Cell. Biol. 24, 2373-2384. (Pubitemid 38325994)
8. Bossis, G. and Melchior, F. (2006). Regulation of SUMOylation by reversible oxidation of SUMO conjugating enzymes. Mol. Cell 21, 349-357. (Pubitemid 43163530)
9. Breusing, N. and Grune, T. (2008). Regulation of proteasome-mediated protein degradation during oxidative stress and aging. Biol. Chem. 389, 203-209. (Pubitemid 351329027)
10. Cai, Y., Singh, B. B., Aslanukov, A., Zhao, H. and Ferreira, P. A. (2001). The docking of kinesins, KIF5B and KIF5C, to Ran-binding protein 2 (RanBP2) is mediated via a novel RanBP2 domain. J. Biol. Chem. 276, 41594-41602.
11. Campisi, J. (2005). Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 120, 513-522.
12. Casanova, M., Portales, P., Blaineau, C., Crobu, L., Bastien, P. and Pages, M. (2008). Inhibition of active nuclear transport is an intrinsic trigger of programmed cell death in trypanosomatids. Cell Death Differ. 15, 1910-1920.
13. Chakrabarti, S. R., Sood, R., Ganguly, S., Bohlander, S., Shen, Z. and Nucifora, G. (1999). Modulation of TEL transcription activity by interaction with the ubiquitin-conjugating enzyme UBC9. Proc. Natl. Acad. Sci. USA 96, 7467-7472. (Pubitemid 29299685)
14. Chi, N. C., Adam, E. J., Visser, G. D. and Adam, S. A. (1996). RanBP1 stabilizes the interaction of Ran with p97 nuclear protein import. J. Cell Biol. 135, 559-569.
15. Cho, K. I., Cai, Y., Yi, H., Yeh, A., Aslanukov, A. and Ferreira, P. A. (2007). Association of the kinesin-binding domain of RanBP2 to KIF5B and KIF5C determines mitochondria localization and function. Traffic 8, 1722-1735.
16. Cho, K. I., Yi, H., Desai, R., Hand, A. R., Haas, A. L. and Ferreira, P. A. (2009a). RANBP2 is an allosteric activator of the conventional kinesin-1 motor protein, KIF5B, in a minimal cell-free system. EMBO Rep. 10, 480-486.
17. Cho, K. I., Yi, H., Yeh, A., Tserentsoodol, N., Cuadrado, L., Searle, K., Hao, Y. and Ferreira, P. A. (2009b). Haploinsufficiency of RanBP2 is neuroprotective against light-elicited and age-dependent degeneration of photoreceptor neurons. Cell Death Differ. 16, 287-297.
18. Crampton, N., Kodiha, M., Shrivastava, S., Umar, R. and Stochaj, U. (2009). Oxidative stress inhibits nuclear protein export by multiple mechanisms that target FG nucleoporins and Crm1. Mol. Biol. Cell 20, 5106-5116.
19. D'Angelo, M. A., Raices, M., Panowski, S. H. and Hetzer, M. W. (2009). Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 136, 284-295.
20. Dawlaty, M. M., Malureanu, L., Jeganathan, K. B., Kao, E., Sustmann, C., Tahk, S., Shuai, K., Grosschedl, R. and van Deursen, J. M. (2008). Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIalpha. Cell 133, 103-115.
21. Delphin, C., Guan, T., Melchior, F. and Gerace, L. (1997). RanGTP targets p97 to RanBP2, a filamentous protein localized at the cytoplasmic periphery of the nuclear pore complex. Mol. Biol. Cell 8, 2379-2390. (Pubitemid 27528208)
22. Engelsma, D., Bernad, R., Calafat, J. and Fornerod, M. (2004). Supraphysiological nuclear export signals bind CRM1 independently of RanGTP and arrest at Nup358. EMBO J. 23, 3643-3652. (Pubitemid 39336286)
23. Ethen, C. M., Hussong, S. A., Reilly, C., Feng, X., Olsen, T. W. and Ferrington, D. A. (2007). Transformation of the proteasome with age-related macular degeneration. FEBS Lett. 581, 885-890.
24. Evdokimov, E., Sharma, P., Lockett, S. J., Lualdi, M. and Kuehn, M. R. (2008). Loss of SUMO1 in mice affects RanGAP1 localization and formation of PML nuclear bodies, but is not lethal as it can be compensated by SUMO2 or SUMO3. J. Cell Sci. 121, 4106-4113.
25. Ferreira, P. A. (2000). Characterization of RanBP2-associated molecular components in neuroretina. Methods Enzymol. 315, 455-468.
26. Ferreira, P. A., Hom, J. T. and Pak, W. L. (1995). Retina-specifically expressed novel subtypes of bovine cyclophilin. J. Biol. Chem. 270, 23179-23188.
27. Ferreira, P. A., Nakayama, T. A., Pak, W. L. and Travis, G. H. (1996). Cyclophilin-related protein RanBP2 acts as chaperone for red/green opsin. Nature 383, 637-640.
28. Ferreira, P. A., Nakayama, T. A. and Travis, G. H. (1997). Interconversion of red opsin isoforms by the cyclophilin-related chaperone protein Ran-binding protein 2. Proc. Natl. Acad. Sci. USA 94, 1556-1561.
29. Ferreira, P. A., Yunfei, C., Schick, D. and Roepman, R. (1998). The cyclophilin-like domain mediates the association of Ran-binding protein 2 with subunits of the 19 S regulatory complex of the proteasome. J. Biol. Chem. 273, 24676-24682. (Pubitemid 28454967)
30. Forler, D., Rabut, G., Ciccarelli, F. D., Herold, A., Kocher, T., Niggeweg, R., Bork, P., Ellenberg, J. and Izaurralde, E. (2004). RanBP2/Nup358 provides a major binding site for NXF1-p15 dimers at the nuclear pore complex and functions in nuclear mRNA export. Mol. Cell. Biol. 24, 1155-1167. (Pubitemid 38112178)
31. Gao, L., Wang, J., Sekhar, K. R., Yin, H., Yared, N. F., Schneider, S. N., Sasi, S., Dalton, T. P., Anderson, M. E., Chan, J. Y. et al. (2007). Novel n-3 fatty acid oxidation products activate Nrf2 by destabilizing the association between Keap1 and Cullin3. J. Biol. Chem. 282, 2529-2537. (Pubitemid 47076775)
32. Gika, A. D., Rich, P., Gupta, S., Neilson, D. E. and Clarke, A. (2009). Recurrent acute necrotizing encephalopathy following influenza A in a genetically predisposed family. Dev. Med. Child Neurol. 52, 99-102.
33. Giri, D. K., Ali-Seyed, M., Li, L. Y., Lee, D. F., Ling, P., Bartholomeusz, G., Wang, S. C. and Hung, M. C. (2005). Endosomal transport of ErbB-2: mechanism for nuclear entry of the cell surface receptor. Mol. Cell. Biol. 25, 11005-11018.
34. Greenstein, J. P. (1954). Biochemistry of Cancer. New York: Academic Press.
35. Heo, J. (2008). Redox regulation of Ran GTPase. Biochem. Biophys. Res. Commun. 376, 568-572.
36. Hirano, M., Furiya, Y., Asai, H., Yasui, A. and Ueno, S. (2006). ALADINI482S causes selective failure of nuclear protein import and hypersensitivity to oxidative stress in triple A syndrome. Proc. Natl. Acad. Sci. USA 103, 2298-2303. (Pubitemid 43271664)
37. Hollyfield, J. G., Bonilha, V. L., Rayborn, M. E., Yang, X., Shadrach, K. G., Lu, L., Ufret, R. L., Salomon, R. G. and Perez, V. L. (2008). Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat. Med. 14, 194-198.
38. Imamura, Y., Noda, S., Hashizume, K., Shinoda, K., Yamaguchi, M., Uchiyama, S., Shimizu, T., Mizushima, Y., Shirasawa, T. and Tsubota, K. (2006). Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in SOD1-deficient mice: a model of age-related macular degeneration. Proc. Natl. Acad. Sci. USA 103, 11282-11287. (Pubitemid 44156510)
39. Jansen, M. S., Nagel, S. C., Miranda, P. J., Lobenhofer, E. K., Afshari, C. A. and McDonnell, D. P. (2004). Short-chain fatty acids enhance nuclear receptor activity through mitogen-activated protein kinase activation and histone deacetylase inhibition. Proc. Natl. Acad. Sci. USA 101, 7199-7204.
40. Johnstone, R. W., Ruefli, A. A. and Lowe, S. W. (2002). Apoptosis: a link between cancer genetics and chemotherapy. Cell 108, 153-164.
41. Kapphahn, R. J., Bigelow, E. J. and Ferrington, D. A. (2007). Age-dependent inhibition of proteasome chymotrypsin-like activity in the retina. Exp. Eye Res. 84, 646-654.
42. Klein, J. A., Longo-Guess, C. M., Rossmann, M. P., Seburn, K. L., Hurd, R. E., Frankel, W. N., Bronson, R. T. and Ackerman, S. L. (2002). The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419, 367-374.
43. Kobayashi, S., Shibata, H., Kurihara, I., Yokota, K., Suda, N., Saito, I. and Saruta, T. (2004). Ubc9 interacts with chicken ovalbumin upstream promoter-transcription factor I and represses receptor-dependent transcription. J. Mol. Endocrinol. 32, 69-86. (Pubitemid 38312622)
44. Kodiha, M., Chu, A., Matusiewicz, N. and Stochaj, U. (2004). Multiple mechanisms promote the inhibition of classical nuclear import upon exposure to severe oxidative stress. Cell Death Differ. 11, 862-874. (Pubitemid 39139745)
45. Kurihara, I., Shibata, H., Kobayashi, S., Suda, N., Ikeda, Y., Yokota, K., Murai, A., Saito, I., Rainey, W. E. and Saruta, T. (2005). Ubc9 and protein inhibitor of activated STAT 1 activate chicken ovalbumin upstream promoter-transcription factor I-mediated human CYP11B2 gene transcription. J. Biol. Chem. 280, 6721-6730. (Pubitemid 40341227)
46. Kurtzman, A. L. and Schechter, N. (2001). Ubc9 interacts with a nuclear localization signal and mediates nuclear localization of the paired-like homeobox protein Vsx-1 independent of SUMO-1 modification. Proc. Natl. Acad. Sci. USA 98, 5602-5607.
47. Lee, G. W., Melchior, F., Matunis, M. J., Mahajan, R., Tian, Q. and Anderson, P. (1998). Modification of Ran GTPase-activating protein by the small ubiquitin-related modifier SUMO-1 requires Ubc9, an E2-type ubiquitin- conjugating enzyme homologue. J. Biol. Chem. 273, 6503-6507. (Pubitemid 28144747)
48. Lipton, S. A. and Bossy-Wetzel, E. (2002). Dueling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 111, 147-150.
49. Mahajan, R., Delphin, C., Guan, T., Gerace, L. and Melchior, F. (1997). A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 88, 97-107. (Pubitemid 27180334)
50. Mahajan, R., Gerace, L. and Melchior, F. (1998). Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J. Cell Biol. 140, 259-270. (Pubitemid 28078390)
51. Matunis, M. J., Coutavas, E. and Blobel, G. (1996). A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J. Cell Biol. 135, 1457-1470. (Pubitemid 26427644)
52. Mavlyutov, T. A., Cai, Y. and Ferreira, P. A. (2002). Identification of RanBP2- and kinesin-mediated transport pathways with restricted neuronal and subcellular localization. Traffic 3, 630-640.
53. Medes, G., Thomas, A. and Weinhouse, S. (1953). Metabolism of neoplastic tissue. IV. A study of lipid synthesis in neoplastic tissue slices in vitro. Cancer Res. 13, 27-29.
54. Melchior, F. (2000). SUMO-nonclassical ubiquitin. Annu. Rev. Cell Dev. Biol. 16, 591-626.
55. Mimnaugh, E. G., Chavany, C. and Neckers, L. (1996). Polyubiquitination and proteasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J. Biol. Chem. 271, 22796-22801. (Pubitemid 26304727)
56. Nacerddine, K., Lehembre, F., Bhaumik, M., Artus, J., Cohen-Tannoudji, M., Babinet, C., Pandolfi, P. P. and Dejean, A. (2005). The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev. Cell 9, 769-779. (Pubitemid 41724105)
57. Neilson, D. E., Adams, M. D., Orr, C. M., Schelling, D. K., Eiben, R. M., Kerr, D. S., Anderson, J., Bassuk, A. G., Bye, A. M., Childs, A. M. et al. (2009). Infection-triggered familial or recurrent cases of acute necrotizing encephalopathy caused by mutations in a component of the nuclear pore, RANBP2. Am. J. Hum. Genet. 84, 44-51.
58. Noell, W. K., Walker, V. S., Kang, B. S. and Berman, S. (1966). Retinal damage by light in rats. Invest. Ophthalmol. 5, 450-473.
59. Nowak, M. and Hammerschmidt, M. (2006). Ubc9 regulates mitosis and cell survival during zebrafish development. Mol. Biol. Cell 17, 5324-5336. (Pubitemid 44907372)
60. Poukka, H., Aarnisalo, P., Karvonen, U., Palvimo, J. J. and Janne, O. A. (1999). Ubc9 interacts with the androgen receptor and activates receptor-dependent transcription. J. Biol. Chem. 274, 19441-19446.
61. Reinheckel, T., Sitte, N., Ullrich, O., Kuckelkorn, U., Davies, K. J. and Grune, T. (1998). Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem. J. 335, 637-642.
62. Reme, C. E. (2005). The dark side of light: rhodopsin and the silent death of vision the proctor lecture. Invest. Ophthalmol. Vis. Sci. 46, 2671-2682.
63. Seeler, J. S. and Dejean, A. (2003). Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell Biol. 4, 690-699.
64. Seufert, W., Futcher, B. and Jentsch, S. (1995). Role of a ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins. Nature 373, 78-81.
65. Singh, B. B., Patel, H. H., Roepman, R., Schick, D. and Ferreira, P. A. (1999). The zinc finger cluster domain of RanBP2 is a specific docking site for the nuclear export factor, exportin-1. J. Biol. Chem. 274, 37370-37378.
66. Suri, M. (2009). Genetic basis for acute necrotizing encephalopathy of childhood. Dev. Med. Child Neurol. 52, 4-5.
67. Swinnen, J. V., Brusselmans, K. and Verhoeven, G. (2006). Increased lipogenesis in cancer cells: new players, novel targets. Curr. Opin. Clin. Nutr. Metab. Care 9, 358-365. (Pubitemid 44101970)
68. Szatmari, I. and Nagy, L. (2008). Nuclear receptor signalling in dendritic cells connects lipids, the genome and immune function. EMBO J. 27, 2353-2362.
69. Vetter, I. R., Nowak, C., Nishimoto, T., Kuhlmann, J. and Wittinghofer, A. (1999). Structure of a Ran-binding domain complexed with Ran bound to a GTP analogue: implications for nuclear transport. Nature 398, 39-46.
70. Vigouroux, S., Briand, M. and Briand, Y. (2004). Linkage between the proteasome pathway and neurodegenerative diseases and aging. Mol. Neurobiol. 30, 201-221. (Pubitemid 41271216)
71. Wong, C. H., Chan, H., Ho, C. Y., Lai, S. K., Chan, K. S., Koh, C. G. and Li, H. Y. (2009). Apoptotic histone modification inhibits nuclear transport by regulating RCC1. Nat. Cell Biol. 11, 36-45.
72. Wu, J., Matunis, M. J., Kraemer, D., Blobel, G. and Coutavas, E. (1995). Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leucine-rich region. J. Biol. Chem. 270, 14209-14213.
73. Yamashita, H., Horie, K., Yamamoto, T., Nagano, T. and Hirano, T. (1992). Lightinduced retinal damage in mice. Hydrogen peroxide production and superoxide dismutase activity in retina. Retina 12, 59-66.
74. Yasuda, Y., Miyamoto, Y., Saiwaki, T. and Yoneda, Y. (2006). Mechanism of the stressinduced collapse of the Ran distribution. Exp. Cell Res. 312, 512-520. (Pubitemid 41804115)
75. Yi, H., Friedman, J. L. and Ferreira, P. A. (2007). The cyclophilin-like domain of Ranbinding protein-2 modulates selectively the activity of the ubiquitin-proteasome system and protein biogenesis. J. Biol. Chem. 282, 34770-34778.
76. Yokoyama, N., Hayashi, N., Seki, T., Pante, N., Ohba, T., Nishii, K., Kuma, K., Hayashida, T., Miyata, T., Aebi, U. et al. (1995). A giant nucleopore protein that binds Ran/TC4. Nature 376, 184-188.
77. Young, R. W. and Bok, D. (1969). Participation of the retinal pigment epithelium in the rod outer segment renewal process. J. Cell Biol. 42, 392-403.
78. Zelcer, N. and Tontonoz, P. (2006). Liver X receptors as integrators of metabolic and inflammatory signaling. J. Clin. Invest. 116, 607-614. (Pubitemid 43326865)
79. Zhang, F. P., Mikkonen, L., Toppari, J., Palvimo, J. J., Thesleff, I. and Janne, O. A. (2008). Sumo-1 function is dispensable in normal mouse development. Mol. Cell. Biol. 28, 5381-5390.