ID2: A negative transcription factor regulating oligodendroglia differentiation

Journal of Neuroscience Research

Volumn 90, Issue 5, 2012, Pages 925-932

  Chen, Xing Shu ^a   Zhang, Yu Hang ^a   Cai, Qi Yan ^a   Yao, Zhong Xiang ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Differentiation; ID2; Oligodendrogenesis; OPC; Pathway

Indexed keywords

BONE MORPHOGENETIC PROTEIN; G PROTEIN COUPLED RECEPTOR; HISTONE DEACETYLASE; INHIBITOR OF DIFFERENTIATION 2; TUMOR SUPPRESSOR PROTEIN; WNT PROTEIN;

CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CYTOPLASM; DEMYELINATION; OLIGODENDROGENESIS; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REMYELINIZATION; RETINOBLASTOMA; SHORT SURVEY;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; DEMYELINATING DISEASES; GENE EXPRESSION REGULATION; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 2; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84862799108     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22826     Document Type: Short Survey

References (72)

1. Adams PD. 2001. Regulation of the retinoblastoma tumor suppressor protein by cyclin/cdks. Biochim Biophys Acta 1471: M123-133.
2. Andres-Barquin PJ, Hernandez MC, Israel MA. 2000. ID genes in nervous system development. Histol Histopathol 15: 603-618.
3. Belletti B, Prisco M, Morrione A, Valentinis B, Navarro M, Baserga R. 2001. Regulation of ID2 gene expression by the insulin-like growth factor I receptor requires signaling by phosphatidylinositol 3-kinase. J Biol Chem 276: 13867-13874.
4. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. 1990. The protein ID: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61: 49-59.
5. Buzzard JJ, Wreford NG, Morrison JR. 2003. Thyroid hormone, retinoic acid, and testosterone suppress proliferation and induce markers of differentiation in cultured rat sertoli cells. Endocrinology 144: 3722-3731.
6. Cai J, Qi Y, Hu X, Tan M, Liu Z, Zhang J, Li Q, Sander M, Qiu M. 2005. Generation of oligodendrocyte precursor cells from mouse dorsal spinal cord independent of Nkx6 regulation and Shh signaling. Neuron 45: 41-53.
7. Cate HS, Sabo JK, Merlo D, Kemper D, Aumann TD, Robinson J, Merson TD, Emery B, Perreau VM, Kilpatrick TJ. 2010. Modulation of bone morphogenic protein signalling alters numbers of astrocytes and oligodendroglia in the subventricular zone during cuprizone-induced demyelination. J Neurochem 115: 11-22.
8. Chen XS, Zhou DS, Yao ZX. 2007. The inhibitor of DNA binding 2 is mainly expressed in oligodendrocyte lineage cells in adult rat brain. Neurosc Lett 428: 93-98.
9. Chen Y, Wu H, Wang SZ, Koito H, Li JR, Ye F, Hoang J, Escobar SS, Gow A, Arnett HA, Trapp BD, Karandikar NJ, Hsieh J, Lu QR. 2009. The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat Neurosci 12: 1398-1406.
10. Chen Y, Wang H, Yoon SO, Xu X, Hottiger MO, Svaren J, Nave KA, Kim HA, Olson EN, Lu QR. 2011. HDAC-mediated deacetylation of NF-kappaB is critical for Schwann cell myelination. Nat Neurosci 14: 437-441.
11. Cheng X, Wang Y, He Q, Qiu M, Whittemore SR, Cao Q. 2007. Bone morphogenetic protein signaling and olig1/2 interact to regulate the differentiation and maturation of adult oligodendrocyte precursor cells. Stem Cells 25: 3204-3214.
12. Colombo N, Schroeder J, Cabrele C. 2006. A short ID2 protein fragment containing the nuclear export signal forms amyloid-like fibrils. Biochem Biophys Res Commun 346: 182-187.
13. Dizon ML, Maa T, Kessler JA. 2011. The bone morphogenetic protein antagonist noggin protects white matter after perinatal hypoxia-ischemia. Neurobiol Dis 42: 318-326.
14. Emery B. 2011. Regulation of oligodendrocyte differentiation and myelination. Science 330: 779-782.
15. Fajerman I, Schwartz AL, Ciechanover A. 2004. Degradation of the ID2 developmental regulator: targeting via N-terminal ubiquitination. Biochem Biophys Res Commun 314: 505-512.
16. Fancy SP, Baranzini SE, Zhao C, Yuk DI, Irvine KA, Kaing S, Sanai N, Franklin RJ, Rowitch DH. 2009. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 23: 1571-1585.
17. Fancy SP, Kotter MR, Harrington EP, Huang JK, Zhao C, Rowitch DH, Franklin RJ. 2010. Overcoming remyelination failure in multiple sclerosis and other myelin disorders. Exp Neurol 225: 18-23.
18. Feigenson K, Reid M, See J, Crenshaw Iii EB, Grinspan JB. 2011. Canonical Wnt signaling requires the BMP pathway to inhibit oligodendrocyte maturation. ASN Neuro (in press).
19. Frank CL, Tsai LH. 2009. Alternative functions of core cell cycle regulators in neuronal migration, neuronal maturation, and synaptic plasticity. Neuron 62: 312-326.
20. Fu H, Qi Y, Tan M, Cai J, Takebayashi H, Nakafuku M, Richardson W, Qiu M. 2002. Dual origin of spinal oligodendrocyte progenitors and evidence for the cooperative role of Olig2 and Nkx2.2 in the control of oligodendrocyte differentiation. Development 129: 681-693.
21. Gokhan S, Marin-Husstege M, Yung SY, Fontanez D, Casaccia-Bonnefil P, Mehler MF. 2005. Combinatorial profiles of oligodendrocyte-selective classes of transcriptional regulators differentially modulate myelin basic protein gene expression. J Neurosci 25: 8311-8321.
22. Gonzalez-Perez O, Alvarez-Buylla A. 2011. Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res Rev 67: 147-156.
23. Hara E, Hall M, Peters G. 1997. Cdk2-dependent phosphorylation of ID2 modulates activity of E2A-related transcription factors. EMBO J 16: 332-342.
24. He Y, Dupree J, Wang J, Sandoval J, Li JD, Liu HF, Shi Y, Nave KA, Casaccia-Bonnefil P. 2007. The transcription factor Yin Yang 1 is essential for oligodendrocyte progenitor differentiation. Neuron 55: 217-230.
25. Jacob C, Christen CN, Pereira JA, Somandin C, Baggiolini A, Lotscher P, Ozcelik M, Tricaud N, Meijer D, Yamaguchi T, Matthias P, Suter U. 2011. HDAC1 and HDAC2 control the transcriptional program of myelination and the survival of Schwann cells. Nat Neurosci 14: 429-436.
26. Jessen KR, Mirsky R. 2008. Negative regulation of myelination: relevance for development, injury, and demyelinating disease. Glia 56: 1552-1565.
27. Kabos P, Kabosova A, Neuman T. 2002. Neuronal injury affects expression of helix-loop-helix transcription factors. Neuroreport 13: 2385-2388.
28. Karaya K, Mori S, Kimoto H, Shima Y, Tsuji Y, Kurooka H, Akira S, Yokota Y. 2005. Regulation of ID2 expression by CCAAT/enhancer binding protein beta. Nucleic Acids Res 33: 1924-1934.
29. Kondo T, Raff M. 2000. The Id4 HLH protein and the timing of oligodendrocyte differentiation. EMBO J 19: 1998-2007.
30. Kotter MR, Stadelmann C, Hartung HP. 2011. Enhancing remyelination in disease-can we wrap it up? Brain 134: 1882-1900.
31. Kremer D, Aktas O, Hartung HP, Kury P. 2011. The complex world of oligodendroglial differentiation inhibitors. Ann Neurol 69: 602-618.
32. Kurisaki K, Kurisaki A, Valcourt U, Terentiev AA, Pardali K, Ten Dijke P, Heldin CH, Ericsson J, Moustakas A. 2003. Nuclear factor YY1 inhibits transforming growth factor beta- and bone morphogenetic protein-induced cell differentiation. Mol Cell Biol 23: 4494-4510.
33. Kurooka H, Yokota Y. 2005. Nucleo-cytoplasmic shuttling of ID2, a negative regulator of basic helix-loop-helix transcription factors. J Biol Chem 280: 4313-4320.
34. Lasorella A, Noseda M, Beyna M, Yokota Y, Iavarone A. 2000. ID2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 407: 592-598.
35. Lasorella A, Stegmuller J, Guardavaccaro D, Liu GC, Carro MS, Rothschild G, de la Torre-Ubieta L, Pagano M, Bonni A, Iavarone A. 2006. Degradation of ID2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442: 471-474.
36. Le N, Nagarajan R, Wang JY, Araki T, Schmidt RE, Milbrandt J. 2005. Analysis of congenital hypomyelinating Egr2Lo/Lo nerves identifies Sox2 as an inhibitor of Schwann cell differentiation and myelination. Proc Natl Acad Sci U S A 102: 2596-2601.
37. Lee DK, George SR, Evans JF, Lynch KR, O'Dowd BF. 2001. Orphan G protein-coupled receptors in the CNS. Curr Opin Pharmacol 1: 31-39.
38. Lee KH, Evans S, Ruan TY, Lassar AB. 2004. SMAD-mediated modulation of YY1 activity regulates the BMP response and cardiac-specific expression of a GATA4/5/6-dependent chick Nkx2.5 enhancer. Development (Cambridge, England) 131: 4709-4723.
39. Leung JY, Kolligs FT, Wu R, Zhai Y, Kuick R, Hanash S, Cho KR, Fearon ER. 2002. Activation of AXIN2 expression by beta-catenin-T cell factor. A feedback repressor pathway regulating Wnt signaling. J Biol Chem 277: 21657-21665.
40. Li H, He Y, Richardson WD, Casaccia P. 2009. Two-tier transcriptional control of oligodendrocyte differentiation. Curr Opin Neurobiol 19: 479-485.
41. Lofstedt T, Jogi A, Sigvardsson M, Gradin K, Poellinger L, Pahlman S, Axelson H. 2004. Induction of ID2 expression by hypoxia-inducible factor-1-a role in dedifferentiation of hypoxic neuroblastoma cells. J Biol Chem 279: 39223-39231.
42. Lu HZ, Wang YX, Zou J, Li Y, Fu SL, Jin JQ, Hu JG, Lu PH. 2011. Differentiation of neural precursor cell-derived oligodendrocyte progenitor cells following transplantation into normal and injured spinal cords. Differ Res Biol Divers 80: 228-240.
43. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, McMahon AP, Stiles CD, Rowitch DH. 2000. Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25: 317-329.
44. Mariconti L, Pellegrini B, Cantoni R, Stevens R, Bergounioux C, Cella R, Albani D. 2002. The E2F family of transcription factors from Arabidopsis thaliana. Novel and conserved components of the retinoblastoma/E2F pathway in plants. J Biol Chem 277: 9911-9919.
45. Marin-Husstege M, He Y, Li J, Kondo T, Sablitzky F, Casaccia-Bonnefil P. 2006. Multiple roles of ID4 in developmental myelination: predicted outcomes and unexpected findings. Glia 54: 285-296.
46. Mekki-Dauriac S, Agius E, Kan P, Cochard P. 2002. Bone morphogenetic proteins negatively control oligodendrocyte precursor specification in the chick spinal cord. Development 129: 5117-5130.
47. Memezawa A, Takada I, Takeyama K, Igarashi M, Ito S, Aiba S, Kato S, Kouzmenko AP. 2007. ID2 gene-targeted crosstalk between Wnt and retinoid signaling regulates proliferation in human keratinocytes. Oncogene 26: 5038-5045.
48. Miller RH. 2011. Unwrapping HDAC1 and HDAC2 functions in Schwann cell myelination. Nat Neurosci 14: 401-403.
49. Miyazono K, ten Dijke P, Heldin CH. 2000. TGF-beta signaling by Smad proteins. Adv Immunol 75: 115-157.
50. Miyazono K, Maeda S, Imamura T. 2005. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev 16: 251-263.
51. Morgan DO. 1997. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 13: 261-291.
52. Nakahara J, Aiso S, Suzuki N. 2009. Factors that retard remyelination in multiple sclerosis with a focus on TIP30: a novel therapeutic target. Expert Opin Ther Targets 13: 1375-1386.
53. Nishimori H, Sasaki Y, Yoshida K, Irifune H, Zembutsu H, Tanaka T, Aoyama T, Hosaka T, Kawaguchi S, Wada T, Hata J-I, Toguchida J, Nakamura Y, Tokino T. 2002. The ID2 gene is a novel target of transcriptional activation by EWS-ETS fusion proteins in Ewing family tumors. Oncogene 21: 8302-8309.
54. Parras CM, Galli R, Britz O, Soares S, Galichet C, Battiste J, Johnson JE, Nakafuku M, Vescovi A, Guillemot F. 2004. Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J 23: 4495-4505.
55. Patel JR, Klein RS. 2011. Mediators of oligodendrocyte differentiation during remyelination. FEBS Lett (in press).
56. Roberts EC, Deed RW, Inoue T, Norton JD, Sharrocks AD. 2001. Id helix-loop-helix proteins antagonize pax transcription factor activity by inhibiting DNA binding. Mol Cell Biol 21: 524-533.
57. Ruzinova MB, Benezra R. 2003. ID proteins in development, cell cycle and cancer. Trends Cell Biol 13: 410-418.
58. Samanta J, Kessler JA. 2004. Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131: 4131-4142.
59. Shen S, Sandoval J, Swiss VA, Li J, Dupree J, Franklin RJ, Casaccia-Bonnefil P. 2008. Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat Neurosci 11: 1024-1034.
60. Sikder HA, Devlin MK, Dunlap S, Ryu B, Alani RM. 2003. ID proteins in cell growth and tumorigenesis. Cancer Cell 3: 525-530.
61. Sun XH, Copeland NG, Jenkins NA, Baltimore D. 1991. ID proteins ID1 and ID2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol Cell Biol 11: 5603-5611.
62. Takebayashi H, Yoshida S, Sugimori M, Kosako H, Kominami R, Nakafuku M, Nabeshima Y. 2000. Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech Dev 99: 143-148.
63. Tekki-Kessaris N, Woodruff R, Hall AC, Gaffield W, Kimura S, Stiles CD, Rowitch DH, Richardson WD. 2001. Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development 128: 2545-2554.
64. Toma JG, El-Bizri H, Barnabe-Heider F, Aloyz R, Miller FD. 2000. Evidence that helix-loop-helix proteins collaborate with retinoblastoma tumor suppressor protein to regulate cortical neurogenesis. J Neurosci 20: 7648-7656.
65. Tzeng SF. 2003. Inhibitors of DNA binding in neural cell proliferation and differentiation. Neurochem Res 28: 45-52.
66. Tzeng SF, Bresnahan JC, Beattie MS, de Vellis J. 2001. Upregulation of the HLH ID gene family in neural progenitors and glial cells of the rat spinal cord following contusion injury. J Neurosci Res 66: 1161-1172.
67. Voumvourakis KI, Antonelou RC, Kitsos DK, Stamboulis E, Tsiodras S. 2011. TGF-beta/BMP: crucial crossroad in neural autoimmune disorders. Neurochem Int (in press).
68. Wang S, Sdrulla A, Johnson JE, Yokota Y, Barres BA. 2001. A role for the helix-loop-helix protein ID2 in the control of oligodendrocyte development. Neuron 29: 603-614.
69. Wang Y, Cheng X, He Q, Zheng Y, Kim DH, Whittemore SR, Cao QL. 2011. Astrocytes from the contused spinal cord inhibit oligodendrocyte differentiation of adult oligodendrocyte precursor cells by increasing the expression of bone morphogenetic proteins. J Neurosci 31: 6053-6058.
70. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, Hu T, Taketo MM, van Es JH, Clevers H, Hsieh J, Bassel-Duby R, Olson EN, Lu QR. 2009. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12: 829-838.
71. Yokota Y. 2001. ID and development. Oncogene 20: 8290-8298.
72. Zhou Q, Wang S, Anderson DJ. 2000. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25: 331-343.