Necdin promotes ubiquitin-dependent degradation of PIAS1 SUMO E3 ligase

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Gur, Ibrahim ^a   Fujiwara, Kazushiro ^a   Hasegawa, Koichi ^a   Yoshikawa, Kazuaki ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NECDIN; PROTEIN CBX4; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN MAGED1; PROTEIN MAGEF1; PROTEIN MAGEL2; PROTEIN NSMCE2; PROTEIN PIAS1; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; MELANOMA ANTIGEN; NERVE PROTEIN; NUCLEAR PROTEIN; PROTEASOME; PROTEIN BINDING; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS MATRIX; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; UBIQUITINATION; ANIMAL; CELL LINE; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; METABOLISM; PROTEIN DEGRADATION; PROTEIN DOMAIN; SUMOYLATION;

ANIMALS; CELL LINE; HUMANS; MELANOMA-SPECIFIC ANTIGENS; MICE; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEOLYSIS; SUBSTRATE SPECIFICITY; SUMOYLATION; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84902590389     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099503     Document Type: Article

References (71)

1. Maruyama K, Usami M, Aizawa T, Yoshikawa K (1991) A novel brain-specific mRNA encoding nuclear protein (necdin) expressed in neurally differentiated embryonal carcinoma cells. Biochem Biophys Res Commun 178: 291-296.
2. Aizawa T, Maruyama K, Kondo H, Yoshikawa K (1992) Expression of necdin, an embryonal carcinoma-derived nuclear protein, in developing mouse brain. Brain Res Dev Brain Res 68: 265-274.
3. Uetsuki T, Takagi K, Sugiura H, Yoshikawa K (1996) Structure and expression of the mouse necdin gene. Identification of a postmitotic neuron-restrictive core promoter. J Biol Chem 271: 918-924.
4. Kuwajima T, Taniura H, Nishimura I, Yoshikawa K (2004) Necdin interacts with the Msx2 homeodomain protein via MAGE-D1 to promote myogenic differentiation of C2C12 cells. J Biol Chem 279: 40484-40493. (Pubitemid 39287639)
5. Huang Z, Fujiwara K, Minamide R, Hasegawa K, Yoshikawa K (2013) Necdin controls proliferation and apoptosis of embryonic neural stem cells in an oxygen tension-dependent manner. J Neurosci 33: 10362-10373.
6. Minamide R, Fujiwara K, Hasegawa K, Yoshikawa K (2014) Antagonistic interplay between necdin and Bmi1 controls proliferation of neural precursor cells in the embryonic mouse neocortex. PLoS One 9: e84460.
7. Taniura H, Taniguchi N, Hara M, Yoshikawa K (1998) Necdin, a postmitotic neuron-specific growth suppressor, interacts with viral transforming proteins and cellular transcription factor E2F1. J Biol Chem 273: 720-728. (Pubitemid 28049158)
8. Taniura H, Matsumoto K, Yoshikawa K (1999) Physical and functional interactions of neuronal growth suppressor necdin with p53. J Biol Chem 274: 16242-16248.
9. Kobayashi M, Taniura H, Yoshikawa K (2002) Ectopic expression of necdin induces differentiation of mouse neuroblastoma cells. J Biol Chem 277: 42128-42135. (Pubitemid 35257529)
10. Kurita M, Kuwajima T, Nishimura I, Yoshikawa K (2006) Necdin downregulates cdc2 expression to attenuate neuronal apoptosis. J Neurosci 26: 12003-12013. (Pubitemid 44772111)
11. Hasegawa K, Yoshikawa K (2008) Necdin regulates p53 acetylation via Sirtuin1 to modulate DNA damage response in cortical neurons. J Neurosci 28: 8772-8784.
12. Kuwako K, Hosokawa A, Nishimura I, Uetsuki T, Yamada M, et al. (2005) Disruption of the paternal necdin gene diminishes TrkA signaling for sensory neuron survival. J Neurosci 25: 7090-7099. (Pubitemid 41077018)
13. Aebischer J, Sturny R, Andrieu D, Rieusset A, Schaller F, et al. (2011) Necdin protects embryonic motoneurons from programmed cell death. PLoS One 6: e23764.
14. Chomez P, De Backer O, Bertrand M, De Plaen E, Boon T, et al. (2001) An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res 61: 5544-5551. (Pubitemid 32694940)
15. Barker PA, Salehi A (2002) The MAGE proteins: Emerging roles in cell cycle progression, apoptosis, and neurogenetic disease. J Neurosci Res 67: 705-712. (Pubitemid 34226281)
16. Pold M, Zhou J, Chen GL, Hall JM, Vescio RA, et al. (1999) Identification of a new, unorthodox member of the MAGE gene family. Genomics 59: 161-167. (Pubitemid 29365346)
17. Bischof JM, Ekker M, Wevrick R (2003) A MAGE/NDN-like gene in zebrafish. Dev Dyn 228: 475-479. (Pubitemid 37372768)
18. Lopez-Sanchez N, Gonzalez-Fernandez Z, Niinobe M, Yoshikawa K, Frade JM (2007) Single mage gene in the chicken genome encodes CMage, a protein with functional similarities to mammalian type II Mage proteins. Physiol Genomics 30: 156-171. (Pubitemid 47173279)
19. Pebernard S, McDonald WH, Pavlova Y, Yates JR 3rd, Boddy MN (2004) Nse1, Nse2, and a novel subunit of the Smc5-Smc6 complex, Nse3, play a crucial role in meiosis. Mol Biol Cell 15: 4866-4876. (Pubitemid 39392203)
20. Sergeant J, Taylor E, Palecek J, Fousteri M, Andrews EA, et al. (2005) Composition and architecture of the Schizosaccharomyces pombe Rad18 (Smc5-6) complex. Mol Cell Biol 25: 172-184. (Pubitemid 40039809)
21. Kegel A, Sjogren C (2010) The Smc5/6 complex: more than repair? Cold Spring Harb Symp Quant Biol 75: 179-187.
22. Katsura Y, Satta Y (2011) Evolutionary history of the cancer immunity antigen MAGE gene family. PLoS One 6: e20365.
23. Zhao Q, Caballero OL, Simpson AJ, Strausberg RL (2012) Differential evolution of MAGE genes based on expression pattern and selection pressure. PLoS One 7: e48240.
24. Nishimura I, Shimizu S, Sakoda JY, Yoshikawa K (2007) Expression of Drosophila MAGE gene encoding a necdin homologous protein in postembryonic neurogenesis. Gene Expr Patterns 7: 244-251. (Pubitemid 44835283)
25. Nishimura I, Sakoda JY, Yoshikawa K (2008) Drosophila MAGE controls neural precursor proliferation in postembryonic neurogenesis. Neuroscience 154: 572-581.
26. van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, et al. (1991) A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254: 1643-1647. (Pubitemid 21917508)
27. Lee S, Kozlov S, Hernandez L, Chamberlain SJ, Brannan CI, et al. (2000) Expression and imprinting of MAGEL2 suggest a role in prader-willi syndrome and the homologous murine imprinting phenotype. Hum Mol Genet 9: 1813-1819. (Pubitemid 30608615)
28. Chibuk TK, Bischof JM, Wevrick R (2001) A necdin/MAGE-like gene in the chromosome 15 autism susceptibility region: expression, imprinting, and mapping of the human and mouse orthologues. BMC Genet 2: 22.
29. Jay P, Rougeulle C, Massacrier A, Moncla A, Mattei MG, et al. (1997) The human necdin gene, NDN, is maternally imprinted and located in the Prader-Willi syndrome chromosomal region. Nat Genet 17: 357-361. (Pubitemid 27476006)
30. MacDonald HR, Wevrick R (1997) The necdin gene is deleted in Prader-Willi syndrome and is imprinted in human and mouse. Hum Mol Genet 6: 1873-1878. (Pubitemid 27460362)
31. Nakada Y, Taniura H, Uetsuki T, Inazawa J, Yoshikawa K (1998) The human chromosomal gene for necdin, a neuronal growth suppressor, in the Prader-Willi syndrome deletion region. Gene 213: 65-72. (Pubitemid 28284724)
32. Kozlov SV, Bogenpohl JW, Howell MP, Wevrick R, Panda S, et al. (2007) The imprinted gene Magel2 regulates normal circadian output. Nat Genet 39: 1266-1272. (Pubitemid 47482682)
33. Gerard M, Hernandez L, Wevrick R, Stewart CL (1999) Disruption of the mouse necdin gene results in early post-natal lethality. Nat Genet 23: 199-202. (Pubitemid 29455393)
34. Muscatelli F, Abrous DN, Massacrier A, Boccaccio I, Le Moal M, et al. (2000) Disruption of the mouse Necdin gene results in hypothalamic and behavioral alterations reminiscent of the human Prader-Willi syndrome. Hum Mol Genet 9: 3101-3110. (Pubitemid 32000784)
35. Geiss-Friedlander R, Melchior F (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8: 947-956. (Pubitemid 350176509)
36. Gill G (2004) SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev 18: 2046-2059.
37. Denuc A, Marfany G (2010) SUMO and ubiquitin paths converge. Biochem Soc Trans 38: 34-39.
38. Doyle JM, Gao J, Wang J, Yang M, Potts PR (2010) MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Molecular Cell 39: 963-974.
39. Yang B, O'Herrin SM, Wu J, Reagan-Shaw S, Ma Y, et al. (2007) MAGE-A, mMage-b, and MAGE-C proteins form complexes with KAP1 and suppress p53-dependent apoptosis in MAGE-positive cell lines. Cancer Res 67: 9954-9962. (Pubitemid 47621245)
40. Perry JJ, Tainer JA, Boddy MN (2008) A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem Sci 33: 201-208.
41. Liu B, Liao J, Rao X, Kushner SA, Chung CD, et al. (1998) Inhibition of Stat1-mediated gene activation by PIAS1. Proc Natl Acad Sci U S A 95: 10626-10631. (Pubitemid 28413118)
42. Kagey MH, Melhuish TA, Wotton D (2003) The polycomb protein Pc2 is a SUMO E3. Cell 113: 127-137. (Pubitemid 36411965)
43. Zhao X, Blobel G (2005) A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc Natl Acad Sci U S A 102: 4777-4782. (Pubitemid 40471530)
44. Andrews EA, Palecek J, Sergeant J, Taylor E, Lehmann AR, et al. (2005) Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol Cell Biol 25: 185-196. (Pubitemid 40039810)
45. Pichler A, Gast A, Seeler JS, Dejean A, Melchior F (2002) The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108: 109-120. (Pubitemid 34137016)
46. Shuai K, Liu B (2005) Regulation of gene-activation pathways by PIAS proteins in the immune system. Nat Rev Immunol 5: 593-605. (Pubitemid 41113191)
47. Rytinki MM, Kaikkonen S, Pehkonen P, Jaaskelainen T, Palvimo JJ (2009) PIAS proteins: pleiotropic interactors associated with SUMO. Cell Mol Life Sci 66: 3029-3041.
48. Taniura H, Kobayashi M, Yoshikawa K (2005) Functional domains of necdin for protein-protein interaction, nuclear matrix targeting, and cell growth suppression. J Cell Biochem 94: 804-815. (Pubitemid 41420277)
49. Hudson JJ, Bednarova K, Kozakova L, Liao C, Guerineau M, et al. (2011) Interactions between the Nse3 and Nse4 components of the SMC5-6 complex identify evolutionarily conserved interactions between MAGE and EID families. PLoS One 6: e17270.
50. Liang M, Melchior F, Feng XH, Lin X (2004) Regulation of Smad4 sumoylation and transforming growth factor-beta signaling by protein inhibitor of activated STAT1. J Biol Chem 279: 22857-22865. (Pubitemid 38685586)
51. Rabellino A, Carter B, Konstantinidou G, Wu SY, Rimessi A, et al. (2012) The SUMO E3-ligase PIAS1 regulates the tumor suppressor PML and its oncogenic counterpart PML-RARA. Cancer Res 72: 2275-2284.
52. Sudharsan R, Azuma Y (2012) The SUMO ligase PIAS1 regulates UV-induced apoptosis by recruiting Daxx to SUMOylated foci. J Cell Sci 125: 5819-5829.
53. Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, et al. (2001) PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 15: 3088-3103. (Pubitemid 33115674)
54. Taniura H, Yoshikawa K (2002) Necdin interacts with the ribonucleoprotein hnRNP U in the nuclear matrix. J Cell Biochem 84: 545-555.
55. Taylor EM, Copsey AC, Hudson JJ, Vidot S, Lehmann AR (2008) Identification of the proteins, including MAGEG1, that make up the human SMC5-6 protein complex. Mol Cell Biol 28: 1197-1206. (Pubitemid 351214123)
56. Kuwako K, Taniura H, Yoshikawa K (2004) Necdin-related MAGE proteins differentially interact with the E2F1 transcription factor and the p75 neurotrophin receptor. J Biol Chem 279: 1703-1712. (Pubitemid 38084437)
57. Depaux A, Regnier-Ricard F, Germani A, Varin-Blank N (2007) A crosstalk between hSiah2 and Pias E3-ligases modulates Pias-dependent activation. Oncogene 26: 6665-6676. (Pubitemid 47573683)
58. Francois S, D'Orlando C, Fatone T, Touvier T, Pessina P, et al. (2012) Necdin enhances myoblasts survival by facilitating the degradation of the mediator of apoptosis CCAR1/CARP1. PLoS One 7: e43335.
59. Lallemand-Breitenbach V, Jeanne M, Benhenda S, Nasr R, Lei M, et al. (2008) Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ ubiquitin-mediated pathway. Nat Cell Biol 10: 547-555. (Pubitemid 351627374)
60. Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, et al. (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10: 538-546. (Pubitemid 351627373)
61. Regad T, Bellodi C, Nicotera P, Salomoni P (2009) The tumor suppressor Pml regulates cell fate in the developing neocortex. Nat Neurosci 12: 132-140.
62. Duval D, Duval G, Kedinger C, Poch O, Boeuf H (2003) The 'PINIT' motif, of a newly identified conserved domain of the PIAS protein family, is essential for nuclear retention of PIAS3L. FEBS Lett 554: 111-118. (Pubitemid 37324824)
63. Hochstrasser M (2001) SP-RING for SUMO: new functions bloom for a ubiquitin-like protein. Cell 107: 5-8.
64. Takazaki R, Nishimura I, Yoshikawa K (2002) Necdin is required for terminal differentiation and survival of primary dorsal root ganglion neurons. Exp Cell Res 277: 220-232. (Pubitemid 34757103)
65. Liu B, Shuai K (2001) Induction of apoptosis by protein inhibitor of activated Stat1 through c-Jun NH2-terminal kinase activation. J Biol Chem 276: 36624-36631.
66. Yang N, Zhao B, Rasul A, Qin H, Li J, et al. (2013) PIAS1-modulated Smad2/4 complex activation is involved in zinc-induced cancer cell apoptosis. Cell Death Dis 4: e811.
67. Hasegawa K, Kawahara T, Fujiwara K, Shimpuku M, Sasaki T, et al. (2012) Necdin controls FoxO1 acetylation in hypothalamic arcuate neurons to modulate the thyroid axis. J Neurosci 32: 5562-5572.
68. Niinobe M, Koyama K, Yoshikawa K (2000) Cellular and subcellular localization of necdin in fetal and adult mouse brain. Dev Neurosci 22: 310-319.
69. He DC, Nickerson JA, Penman S (1990) Core filaments of the nuclear matrix. J Cell Biol 110: 569-580.
70. Fujiwara K, Hasegawa K, Ohkumo T, Miyoshi H, Tseng YH, et al. (2012) Necdin controls proliferation of white adipocyte progenitor cells. PLoS One 7: e30948.
71. Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM (1998) Development of a self-inactivating lentivirus vector. J Virol 72: 8150-8157.