CtBP2 downregulation during neural crest specification induces expression of Mitf and REST, resulting in melanocyte differentiation and sympathoadrenal lineage suppression

Molecular and Cellular Biology

Volumn 31, Issue 5, 2011, Pages 955-970

  Liang, Hongzi ^a   Fekete, Donna M ^b   Andrisani, Ourania M ^a  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CARBOXY TERMINAL BINDING PROTEIN 2; CYCLIC AMP; HOMEODOMAIN INTERACTING PROTEIN KINASE 2; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; PROTEASOME; UNCLASSIFIED DRUG; WNT PROTEIN;

ADRENERGIC SYSTEM; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; GENE EXPRESSION; MELANOCYTE; NERVE CELL; NEURAL CREST; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; RECEPTOR DOWN REGULATION; ZEBRA FISH;

ANIMALS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOWN-REGULATION; MELANOCYTES; MICE; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; NEURAL CREST; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; SYMPATHETIC NERVOUS SYSTEM; TRANSCRIPTION, GENETIC; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 79952256249     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01062-10     Document Type: Article

References (84)

1. 1-S progression in melanoma cells. Cancer Res. 70:2891-2900.
2. Anderson, D. J. 1993. Molecular control of cell fate in the neural crest: the sympathoadrenal lineage. Annu. Rev. Neurosci. 16:129-158.
3. Bergman, L. M., C. N. Birts, M. Darley, B. Gabrielli, and J. P. Blaydes. 2009. CtBPs promote cell survival through the maintenance of mitotic fidelity. Mol. Cell. Biol. 29:4539-4551.
4. Bertolotto, C., et al. 1998. Microphthalmia gene product as a signal transducer in cAMP-induced differentiation of melanocytes. J. Cell Biol. 142:827-835. (Pubitemid 28381498)
5. Bertolotto, C., et al. 1998. Different cis-acting elements are involved in the regulation of TRP1 and TRP2 promoter activities by cyclic AMP: pivotal role of M boxes (GTCATGTGCT) and of microphthalmia. Mol. Cell. Biol. 18:694-702.
6. Bertolotto, C., K. Bille, J. P. Ortonne, and R. Ballotti. 1996. Regulation of tyrosinase gene expression by cAMP in B16 melanoma cells involves two CATGTG motifs surrounding the TATA box: implication of the microphthalmia gene product. J. Cell Biol. 134:747-755. (Pubitemid 26269144)
7. Bilodeau, M. L., M. Ji, M. Paris, and O. M. Andrisani. 2005. Adenosine signaling promotes neuronal, catecholaminergic differentiation of primary neural crest cells and CNS-derived CAD cells. Mol. Cell Neurosci. 29:394-404.
8. Bilodeau, M. L., et al. 2001. BMP-2 stimulates tyrosinase gene expression and melanogenesis in differentiated melanocytes. Pigment Cell Res. 14:328-336. (Pubitemid 32956358)
9. Bilodeau, M. L., T. Boulineau, R. L. Hullinger, and O. M. Andrisani. 2000. Cyclic AMP signaling functions as a bimodal switch in sympathoadrenal cell development in cultured primary neural crest cells. Mol. Cell. Biol. 20:3004-3014.
10. Bitomsky, N., and T. G. Hofmann. 2009. Apoptosis and autophagy: regulation of apoptosis by DNA damage signalling - roles of p53, p73 and HIPK2. FEBS J. 276:6074-6083.
11. Brand, M., M. Granato, and C. Nüsslein-Volhard. 2002. Keeping and raising zebrafish, p. 7-37. In C. Nüsslein-Volhard and R. Dahm (ed.), Zebrafish: a practical approach. Oxford University Press, Oxford, United Kingdom.
12. Brannon, M., J. D. Brown, R. Bates, D. Kimelman, and R. T. Moon. 1999. XCtBP is a XTcf-3 co-repressor with roles throughout Xenopus development. Development 126:3159-3170.
13. Calzado, M. A., F. Renner, A. Roscic, and M. L. Schmitz. 2007. HIPK2: a versatile switchboard regulating the transcription machinery and cell death. Cell Cycle 6:139-143.
14. Chen, S., M. Ji, M. Paris, R. L. Hullinger, and O. M. Andrisani. 2005. The cAMP pathway regulates both transcription and activity of the paired homeobox transcription factor Phox2a required for development of neural crest-derived and central nervous system-derived catecholaminergic neurons. J. Biol. Chem. 280:41025-41036.
15. Chinnadurai, G. 2009. The transcriptional corepressor CtBP: a foe of multiple tumor suppressors. Cancer Res. 69:731-734.
16. Chinnadurai, G. 2002. CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol. Cell 9:213-224. (Pubitemid 34195548)
17. Chong, J. A., et al. 1995. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80:949-957.
18. Cuilliere-Dartigues, P., et al. 2006. TCF-4 isoforms absent in TCF-4 mutated MSI-H colorectal cancer cells colocalize with nuclear CtBP and repress TCF-4-mediated transcription. Oncogene 25:4441-4448. (Pubitemid 44141632)
19. Curran, K., D. W. Raible, and J. A. Lister. 2009. Foxd3 controls melanophore specification in the zebrafish neural crest by regulation of Mitf. Dev. Biol. 332:408-417.
20. Curran, K., et al. 2010. Interplay between Foxd3 and Mitf regulates cell fate plasticity in the zebrafish neural crest. Dev. Biol. 344:107-118.
21. D'Orazi, G., et al. 2002. Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat. Cell Biol. 4:11-19.
22. Dorsky, R. I., D. W. Raible, and R. T. Moon. 2000. Direct regulation of nacre, a zebrafish MITF homolog required for pigment cell formation, by the Wnt pathway. Genes Dev. 14:158-162.
23. Dorsky, R. I., R. T. Moon, and D. W. Raible. 1998. Control of neural crest cell fate by the Wnt signalling pathway. Nature 396:370-373.
24. Dunn, K. J., et al. 2005. WNT1 and WNT3a promote expansion of melanocytes through distinct modes of action. Pigment Cell Res. 18:167-180. (Pubitemid 40733335)
25. Dunn, K. J., B. O. Williams, Y. Li, and W. J. Pavan. 2000. Neural crest-directed gene transfer demonstrates Wnt1 role in melanocyte expansion and differentiation during mouse development. Proc. Natl. Acad. Sci. U. S. A. 97:10050-10055.
26. Dupin, E., M. Maus, and M. Fauquet. 1993. Regulation of the quail tyrosine hydroxylase gene in neural crest cells by cAMP and beta-adrenergic ligands. Dev. Biol. 159:75-86.
27. Fang, M., et al. 2006. C-terminal-binding protein directly activates and represses Wnt transcriptional targets in Drosophila. EMBO J. 25:2735-2745. (Pubitemid 43980381)
28. Goding, C. R. 2000. Mitf from neural crest to melanoma: signal transduction and transcription in the melanocyte lineage. Genes Dev. 14:1712-1728. (Pubitemid 30602990)
29. Hamada, F., and M. Bienz. 2004. The APC tumor suppressor binds to C-terminal binding protein to divert nuclear beta-catenin from TCF. Dev. Cell 7:677-685. (Pubitemid 39462688)
30. Hari, L., et al. 2002. Lineage-specific requirements of beta-catenin in neural crest development. J. Cell Biol. 159:867-880. (Pubitemid 36008368)
31. Hildebrand, J. D., and P. Soriano. 2002. Overlapping and unique roles for C-terminal binding protein 1 (CtBP1) and CtBP2 during mouse development. Mol. Cell. Biol. 22:5296-5307.
32. Hino, S., C. Tanji, K. I. Nakayama, and A. Kikuchi. 2005. Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase stabilizes beta-catenin through inhibition of its ubiquitination. Mol. Cell. Biol. 25:9063-9072.
33. Hirsch, M. R., M. C. Tiveron, F. Guillemot, J. F. Brunet, and C. Goridis. 1998. Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development 125:599-608. (Pubitemid 28108085)
34. Hofmann, T. G., E. Jaffray, N. Stollberg, R. T. Hay, and H. Will. 2005. Regulation of homeodomain-interacting protein kinase 2 (HIPK2) effector function through dynamic small ubiquitin-related modifier-1 (SUMO-1) modification. J. Biol. Chem. 280:29224-29232.
35. Hou, L., J. J. Panthier, and H. Arnheiter. 2000. Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF. Development 127:5379-5389. (Pubitemid 32049193)
36. Ikeya, M., S. M. Lee, J. E. Johnson, A. P. McMahon, and S. Takada. 1997. Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389:966-970.
37. Ji, M., and O. M. Andrisani. 2005. High-level activation of cyclic AMP signaling attenuates bone morphogenetic protein 2-induced sympathoadrenal lineage development and promotes melanogenesis in neural crest cultures. Mol. Cell. Biol. 25:5134-5145.
38. Jin, E. J., C. A. Erickson, S. Takada, and L. W. Burrus. 2001. Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo. Dev. Biol. 233:22-37.
39. Kim, H. S., C. Yang, and K. S. Kim. 1998. The cell-specific silencer region of the human dopamine beta-hydroxylase gene contains several negative regulatory elements. J. Neurochem. 71:41-50.
40. Kim, S. M., et al. 2006. Regulation of human tyrosine hydroxylase gene by neuron-restrictive silencer factor. Biochem. Biophys. Res. Commun. 346:426-435.
41. Kim, Y. H., C. Y. Choi, and Y. Kim. 1999. Covalent modification of the homeodomain-interacting protein kinase 2 (HIPK2) by the ubiquitin-like protein SUMO-1. Proc. Natl. Acad. Sci. U. S. A. 96:12350-12355.
42. Kloosterman, W. P., A. K. Lagendijk, R. F. Ketting, J. D. Moulton, and R. H. Plasterk. 2007. Targeted inhibition of miRNA maturation with morpholinos reveals a role for mirR-375 in pancreatic islet development. PLoS Biol. 5:e203.
43. Kos, R., M. V. Reedy, R. L. Johnson, and C. A. Erickson. 2001. The winged-helix transcription factor FoxD3 is important for establishing the neural crest lineage and repressing melanogenesis in avian embryos. Development 128:1467-1479.
44. Le Douarin, N. M., S. Creuzet, G. Couly, and E. Dupin. 2004. Neural crest cell plasticity and its limits. Development 131:4637-4650. (Pubitemid 39433452)
45. Le Douarin, N. M., and C. Kalcheim. 1999. The neural crest. Developmental and cell biology series, 2nd ed. Cambridge University Press, Cambridge, United Kingdom.
46. Lee, W., S. Swarup, J. Chen, T. Ishitani, and E. M. Verheyen. 2009. Homeodomain-interacting protein kinases (Hipks) promote Wnt/Wg signaling through stabilization of beta-catenin/Arm and stimulation of target gene expression. Development 136:241-251.
47. Lewis, J. L., et al. 2004. Reiterated Wnt signaling during zebrafish neural crest development. Development 131:1299-1308. (Pubitemid 38443884)
48. Li, H., W. Kloosterman, and D. M. Fekete. 2010. MicroRNA-183 family members regulate sensorineural fates in the inner ear. J. Neurosci. 30:3254-3263.
49. Li, M., et al. 2000. Cyclic AMP promotes neuronal survival by phosphorylation of glycogen synthase kinase 3beta. Mol. Cell. Biol. 20:9356-9363.
50. Lister, J. A., C. P. Robertson, T. Lepage, S. L. Johnson, and D. W. Raible. 1999. nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126:3757-3767.
51. Lo, L., X. Morin, J. F. Brunet, and D. J. Anderson. 1999. Specification of neurotransmitter identity by Phox2 proteins in neural crest stem cells. Neuron 22:693-705.
52. Lo, L., M. C. Tiveron, and D. J. Anderson. 1998. MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development 125:609-620.
53. Maxwell, G. D., and M. E. Forbes. 1990. Stimulation of adrenergic development in neural crest cultures by a reconstituted basement membrane-like matrix is inhibited by agents that elevate cAMP. J. Neurosci. Res. 25:172-179.
54. Nataf, V., P. Mercier, C. Ziller, and N. Le Douarin. 1993. Novel markers of melanocyte differentiation in the avian embryo. Exp. Cell Res. 207:171-182.
55. Nishihara, S., L. Tsuda, and T. Ogura. 2003. The canonical Wnt pathway directly regulates NRSF/REST expression in chick spinal cord. Biochem. Biophys. Res. Commun. 311:55-63.
56. Opdecamp, K., et al. 1997. Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix- zipper transcription factor. Development 124:2377-2386. (Pubitemid 27309737)
57. Otto, S. J., et al. 2007. A new binding motif for the transcriptional repressor REST uncovers large gene networks devoted to neuronal functions. J. Neurosci. 27:6729-6739. (Pubitemid 46983428)
58. Paliwal, S., et al. 2006. Targeting of C-terminal binding protein (CtBP) by ARF results in p53-independent apoptosis. Mol. Cell. Biol. 26:2360-2372.
59. Paris, M., W. H. Wang, M. H. Shin, D. S. Franklin, and O. M. Andrisani. 2006. Homeodomain transcription factor Phox2a, via cyclic AMP-mediated activation, induces p27Kip1 transcription, coordinating neural progenitor cell cycle exit and differentiation. Mol. Cell. Biol. 26:8826-8839.
60. Price, E. R., et al. 1998. Alpha-melanocyte-stimulating hormone signaling regulates expression of microphthalmia, a gene deficient in Waardenburg syndrome. J. Biol. Chem. 273:33042-33047.
61. Raible, D. W. 2006. Development of the neural crest: achieving specificity in regulatory pathways. Curr. Opin. Cell Biol. 18:698-703.
62. Rinaldo, C., A. Prodosmo, F. Siepi, and S. Soddu. 2007. HIPK2: a multi-talented partner for transcription factors in DNA damage response and development. Biochem. Cell Biol. 85:411-418.
63. Satoh, M., and H. Ide. 1987. Melanocyte-stimulating hormone affects melanogenic differentiation of quail neural crest cells in vitro. Dev. Biol. 119:579-586.
64. Sauka-Spengler, T., and M. Bronner-Fraser. 2006. Development and evolution of the migratory neural crest: a gene regulatory perspective. Curr. Opin. Genet. Dev. 16:360-366.
65. Schoenherr, C. J., and D. J. Anderson. 1995. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267:1360-1363.
66. Kip1 transcription. Mol. Cell. Biol. 29:4878-4890.
67. Stanke, M., et al. 1999. The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. Development 126:4087-4094. (Pubitemid 29481565)
68. Steingrimsson, E., N. G. Copeland, and N. A. Jenkins. 2004. Melanocytes and the microphthalmia transcription factor network. Annu. Rev. Genet. 38:365-411.
69. Suzuki, A., et al. 2008. PTH/cAMP/PKA signaling facilitates canonical Wnt signaling via inactivation of glycogen synthase kinase-3beta in osteoblastic Saos-2 cells. J. Cell Biochem. 104:304-317.
70. Takeda, K., et al. 2000. Induction of melanocyte-specific microphthalmia-associated transcription factor by Wnt-3a. J. Biol. Chem. 275:14013-14016.
71. Thomas, A. J., and C. A. Erickson. 2008. The making of a melanocyte: the specification of melanoblasts from the neural crest. Pigment Cell Melanoma Res. 21:598-610.
72. Thomas, A. J., and C. A. Erickson. 2009. FOXD3 regulates the lineage switch between neural crest derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Development 136:1849-1858.
73. Turner, J., and M. Crossley. 2001. The CtBP family: enigmatic and enzymatic transcriptional co-repressors. Bioessays 23:683-690. (Pubitemid 32792512)
74. Valenta, T., J. Lukas, and V. Korinek. 2003. HMG box transcription factor TCF-4's interaction with CtBP1 controls the expression of the Wnt target Axin2/Conductin in human embryonic kidney cells. Nucleic Acids Res. 31: 2369-2380. (Pubitemid 37442105)
75. Vance, K. W., and C. R. Goding. 2004. The transcription network regulating melanocyte development and melanoma. Pigment Cell Res. 17:318-325.
76. Van Hateren, N., T. Shenton, and A. G. Borycki. 2006. Expression of avian C-terminal binding proteins (Ctbp1 and Ctbp2) during embryonic development. Dev. Dyn. 235:490-495.
77. Wang, S. Y., M. Iordanov, and Q. Zhang. 2006. c-Jun NH2-terminal kinase promotes apoptosis by down-regulating the transcriptional co-repressor CtBP. J. Biol. Chem. 281:34810-34815.
78. Westbrook, T. F., et al. 2005. A genetic screen for candidate tumor suppressors identifies REST. Cell 121:837-848. (Pubitemid 40806416)
79. Westerfield, M. 1994. The zebrafish book: a guide for the laboratory use of zebrafish (Brachydanio rerio), ed. 2.1. University of Oregon, Eugene, OR.
80. Widlund, H. R., and D. E. Fisher. 2003. Microphthalamia-associated transcription factor: a critical regulator of pigment cell development and survival. Oncogene 22:3035-3041.
81. Willert, J., M. Epping, J. R. Pollack, P. O. Brown, and R. Nusse. 2002. A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC. Dev. Biol. 2:8.
82. Yasumoto, K., et al. 2002. Microphthalmia-associated transcription factor interacts with LEF-1, a mediator of Wnt signaling. EMBO J. 21:2703-2714. (Pubitemid 34619386)
83. Zhang, Q., A. Nottke, and R. H. Goodman. 2005. Homeodomain-interacting protein kinase-2 mediates CtBP phosphorylation and degradation in UV-triggered apoptosis. Proc. Natl. Acad. Sci. U. S. A. 102:2802-2807.
84. Zhang, Q., Y. Yoshimatsu, J. Hildebrand, S. M. Frisch, and R. H. Goodman. 2003. Homeodomain interacting protein kinase 2 promotes apoptosis by downregulating the transcriptional corepressor CtBP. Cell 115:177-186.