The role of Zi2 during neural tube and neural crest development


The role of Zi2 during neural tube and neural crest development


Gerald Muça*

Department of Morfofunctional Modules, Faculty of Veterinary Medicine, Agricultural University of Tirana, Koder Kamez, 2021 Tirana-Albania


Global Journal of Molecular Biology

The transcription factor Zic2 is member of Zic family, at early stages it has been involved in several processes during embryonic development and later on in morphogenesis and organogenesis. An important role has been attributed to Zic2 during the development of the neural system. It has been involved in neural tube and neural crest formation. Both process structures will form the central and peripheral neural system. Mutation of Zic2 provokes holoprosencephaly in humans and in mouse also spina bifida. To date, there is not well elaborated the specific mechanisms under which Zic2 affect neural tube formation and the differences may exist between mouse and human phenotype. Almost the same ambiguity is for the specific role of Zic2 during neural crest development. Here is given are resumed latest studies and are given new insight about the role of Zic2 in these two processes and its new target genes.


Keywords: Zic2; neural tube; neural crest; cell proliferation; development

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How to cite this article:
Gerald Muça.The role of Zi2 during neural tube and neural crest development. Global Journal of Molecular Biology, 2019, 2:6. DOI: 10.28933/gjmb-2019-01-1605


References:
1. Abdul-Aziz, N.M., Turmaine, M., Greene, N.D.E., and Copp, A.J. (2009). EphrinA-EphA receptor interactions in mouse spinal neurulation: Implications for neural fold fusion. Int. J. Dev. Biol. 53, 559–568.
2. Abdullah, N.L., Mohd-Zin, S.W., Ahmad-Annuar, A., and Abdul-Aziz, N.M. (2017). A Novel Occulta-Type Spina Bifida Mediated by Murine Double Heterozygotes EphA2 and EphA4 Receptor Tyrosine Kinases. Front. Cell Dev. Biol. 5.
3. Ali, R.G., Bellchambers, H.M., and Arkell, R.M. (2012). Zinc fingers of the cerebellum (Zic): Transcription factors and co-factors. Int. J. Biochem. Cell Biol. 44, 2065–2068.
4. Alles, A.J., and Sulik, K.K. (1990). Retinoic acid-induced spina bifida: evidence for a pathogenetic mechanism. Dev. Camb. Engl. 108, 73–81.
5. Aruga, J., Nagai, T., Tokuyama, T., Hayashizaki, Y., Okazaki, Y., Chapman, V.M., and Mikoshiba, K. (1996). The Mouse Zic Gene Family: HOMOLOGUES OF THE DROSOPHILA PAIR-RULE GENE odd-paired. J. Biol. Chem. 271, 1043–1047.
6. Aruga, J., Inoue, T., Hoshino, J., and Mikoshiba, K. (2002). Zic2 controls cerebellar development in cooperation with Zic1. J. Neurosci. Off. J. Soc. Neurosci. 22, 218–225.
7. Bartholin, L., Powers, S.E., Melhuish, T.A., Lasse, S., Weinstein, M., and Wotton, D. (2006). TGIF Inhibits Retinoid Signaling. Mol. Cell. Biol. 26, 990–1001.
8. Brewster, R., Lee, J., and Ruiz i Altaba, a (1998). Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 393, 579–583.
9. Briscoe, J., Pierani, A., Jessell, T.M., and Ericson, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101, 435–445.
10. Brown, L.Y., Odent, S., David, V., Blayau, M., Dubourg, C., Apacik, C., Delgado, M.A., Hall, B.D., Reynolds, J.F., Sommer, A., et al. (2001). Holoprosencephaly due to mutations in ZIC2: alanine tract expansion mutations may be caused by parental somatic recombination. Hum. Mol. Genet. 10, 791–796.
11. Brown, S.A., Warburton, D., Brown, L.Y., Yu, C., Roeder, E.R., Stengel-rutkowski, S., Hennekam, R.C.M., and Muenke, M. (1998). Holoprosencephaly due to mutations in ZIC2 , a homologue of Drosophila odd-paired. 20, 3–6.
12. Burstyn-Cohen, T. (2004). Canonical Wnt activity regulates trunk neural crest delamination linking BMP/noggin signaling with G1/S transition. Development 131, 5327–5339.
13. Chen, G., Pei, L.-J., Huang, J., Song, X.-M., Lin, L.-M., Gu, X., Wu, J.-X., Wang, F., Wu, J.-L., Chen, J.-P., et al. (2009). Unusual Patterns of Neural Tube Defects in a High Risk Region of Northern China. Biomed. Environ. Sci. 22, 340–344.
14. Chiang, C., Litingtung, Y., Lee, E., Young, K.E., Corden, J.L., Westphal, H., and Beachy, P. a (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407–413.
15. Cohen, M.M., and Shiota, K. (2002). Teratogenesis of holoprosencephaly. Am. J. Med. Genet. 109, 1–15.
16. Copp, A.J., and Greene, N.D.E. (2013). Neural tube defects-disorders of neurulation and related embryonic processes. Wiley Interdiscip. Rev. Dev. Biol. 2, 213–227.
17. Copp, A.J., Greene, N.D.E., and Murdoch, J.N. (2003). The genetic basis of mammalian neurulation. Nat. Rev. Genet.
18. Drummond, D.L., Cheng, C.S., Selland, L.G., Hocking, J.C., Prichard, L.B., and Waskiewicz, A.J. (2013). The role of Zic transcription factors in regulating hindbrain retinoic acid signaling. BMC Dev. Biol. 13, 31–31.
19. Edison, R., and Muenke, M. (2003). The interplay of genetic and environmental factors in craniofacial morphogenesis: holoprosencephaly and the role of cholesterol. Congenit. Anom. 43, 1–21.
20. Elms, P., Siggers, P., Napper, D., Greenfield, A., and Arkell, R. (2003). Zic2 is required for neural crest formation and hindbrain patterning during mouse development. Dev. Biol. 264, 391–406.
21. Elms, P., Scurry, A., Davies, J., Willoughby, C., Hacker, T., Bogani, D., and Arkell, R. (2004). Overlapping and distinct expression domains of Zic2 and Zic3 during mouse gastrulation. Gene Expr. Patterns 4, 505–511.
22. Escalante, A., Murillo, B., Morenilla-Palao, C., Klar, A., and Herrera, E. (2013). Zic2-dependent axon midline avoidance controls the formation of major ipsilateral tracts in the CNS. Neuron 80, 1392–1406.
23. Franco, P.G., Paganelli, A.R., López, S.L., and Carrasco, A.E. (1999). Functional association of retinoic acid and hedgehog signaling in Xenopus primary neurogenesis. Dev. Camb. Engl. 126, 4257–4265.
24. Furushima, K., Murata, T., Matsuo, I., and Aizawa, S. (2000). A new murine zinc finger gene, Opr. Mech. Dev. 98, 161–164.
25. Galea, G.L., Cho, Y.-J., Galea, G., Molè, M.A., Rolo, A., Savery, D., Moulding, D., Culshaw, L.H., Nikolopoulou, E., Greene, N.D.E., et al. (2017). Biomechanical coupling facilitates spinal neural tube closure in mouse embryos. Proc. Natl. Acad. Sci. 201700934.
26. García-Frigola, C., Carreres, M.I., Vegar, C., Mason, C., and Herrera, E. (2008). Zic2 promotes axonal divergence at the optic chiasm midline by EphB1-dependent and -independent mechanisms. Dev. Camb. Engl. 135, 1833–1841.
27. Grinberg, I., and Millen, K.J. (2005). The ZIC gene family in development and disease. Clin. Genet. 67, 290–296.
28. Gripp, K.W., Wotton, D., Edwards, M.C., Roessler, E., Ades, L., Meinecke, P., Richieri-Costa, A., Zackai, E.H., Massagué, J., Muenke, M., et al. (2000). Mutations in TGIF cause holoprosencephaly and link NODAL signalling to human neural axis determination. Nat. Genet. 25, 205–208.
29. Hari, L., Brault, V., Kléber, M., Lee, H.Y., Ille, F., Leimeroth, R., Paratore, C., Suter, U., Kemler, R., and Sommer, L. (2002). Lineage-specific requirements of β-catenin in neural crest development. J. Cell Biol.
30. Helms, A.W., and Johnson, J.E. (2003). Specification of dorsal spinal cord interneurons. Curr. Opin. Neurobiol. 13, 42–49.
31. Herrera, E., Brown, L., Aruga, J., Rachel, R. a, Dolen, G., Mikoshiba, K., Brown, S., and Mason, C. a (2003). Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 114, 545–557.
32. Houtmeyers, R., Souopgui, J., Tejpar, S., and Arkell, R. (2013). The ZIC gene family encodes multi-functional proteins essential for patterning and morphogenesis. Cell. Mol. Life Sci. CMLS.
33. Houtmeyers, R., Tchouate Gainkam, O., Glanville-Jones, H.A., Van den Bosch, B., Chappell, A., Barratt, K.S., Souopgui, J., Tejpar, S., and Arkell, R.M. (2016). Zic2 mutation causes holoprosencephaly via disruption of NODAL signalling. Hum. Mol. Genet. 25, 3946–3959.
34. Inoue, T., Hatayama, M., Tohmonda, T., Itohara, S., Aruga, J., and Mikoshiba, K. (2004). Mouse Zic5 deficiency results in neural tube defects and hypoplasia of cephalic neural crest derivatives. Dev. Biol. 270, 146–162.
35. Inoue, T., Ota, M., Mikoshiba, K., and Aruga, J. (2007). Zic2 and Zic3 synergistically control neurulation and segmentation of paraxial mesoderm in mouse embryo. Dev. Biol. 306, 669–684.
36. Ishiguro, A., Hatayama, M., Otsuka, M.I., and Aruga, J. (2018). Link between the causative genes of holoprosencephaly: Zic2 directly regulates Tgif1 expression. Sci. Rep. 8.
37. Janesick, A., Abbey, R., Chung, C., Liu, S., Taketani, M., and Blumberg, B. (2013). ERF and ETV3L are retinoic acid-inducible repressors required for primary neurogenesis. Development 140, 3095–3106.
38. Kalcheim, C. (2018). Neural crest emigration: From start to stop. Genesis 56, e23090.
39. Klootwijk, R., Groenen, P., Schijvenaars, M., Hol, F., Hamel, B., Straatman, H., Steegers-Theunissen, R., Mariman, E., and Franke, B. (2004). Genetic variants inZIC1,ZIC2, andZIC3 are not major risk factors for neural tube defects in humans. Am. J. Med. Genet. 124A, 40–47.
40. Koyabu, Y., Nakata, K., Mizugishi, K., Aruga, J., and Mikoshiba, K. (2001). Physical and Functional Interactions between Zic and Gli Proteins. J. Biol. Chem. 276, 6889–6892.
41. Kumar, M., and Chapman, S.C. (2012). Cloning and expression analysis of Fgf5, 6 and 7 during early chick development. Gene Expr. Patterns 12, 245–253.
42. Laussu, J., Audouard, C., Kischel, A., Assis-Nascimento, P., Escalas, N., Liebl, D.J., Soula, C., and Davy, A. (2017). Eph/Ephrin Signaling Controls Progenitor Identities In The Ventral Spinal Cord. Neural Develop. 12.
43. Le Douarin, N.M., and Kalcheim, C. (1999). The Neural Crest.
44. Lee, K.J., Mendelsohn, M., and Jessell, T.M. (1998). Neuronal patterning by BMPs: a requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord. Genes Dev. 12, 3394–3407.
45. Lee, R., Petros, T.J., and Mason, C.A. (2008). Zic2 Regulates Retinal Ganglion Cell Axon Avoidance of ephrinB2 through Inducing Expression of the Guidance Receptor EphB1. J. Neurosci. 28, 5910–5919.
46. Li, J.Y.H., and Joyner, A.L. Otx2 and Gbx2 in mid-hindbrain patterning. 13.
47. Liao, Y., Wang, J., Li, X., Guo, Y., and Zheng, X. (2009). Identifying environmental risk factors for human neural tube defects before and after folic acid supplementation. BMC Public Health 9.
48. Life, T., and Project, C.N. (1997). Xenopus Zic 3 , a primary regulator both in neural and neural. 94, 11980–11985.
49. Lu, S.-X., Zhang, C.Z., Luo, R.-Z., Wang, C.-H., Liu, L.-L., Fu, J., Zhang, L., Wang, H., Xie, D., and Yun, J.-P. (2017). Zic2 promotes tumor growth and metastasis via PAK4 in hepatocellular carcinoma. Cancer Lett. 402, 71–80.
50. Luo, Z., Gao, X., Lin, C., Smith, E.R., Marshall, S.A., Swanson, S.K., Florens, L., Washburn, M.P., and Shilatifard, A. (2015). Zic2 is an enhancer-binding factor required for embryonic stem cell specification. Mol. Cell 57, 685–694.
51. Maden, M. (2006). Retinoids and spinal cord development. J. Neurobiol. 66, 726–738.
52. Matsuda, K., Mikami, T., Oki, S., Iida, H., Andrabi, M., Boss, J.M., Yamaguchi, K., Shigenobu, S., and Kondoh, H. (2017). ChIP-seq analysis of genomic binding regions of five major transcription factors highlights a central role for ZIC2 in the mouse epiblast stem cell gene regulatory network. Development 144, 1948–1958.
53. McGeachie, A.B., Koishi, K., Imamura, T., McLennan, I.S., and Department of Anatomy and Structural Biology, University of Otago, Dunedin, New Zealand (2001). Fibroblast growth factor-5 is expressed in Schwann cells and is not essential for motoneurone survival. Neuroscience 104, 891–899.
54. McMahon, A.R., and Merzdorf, C.S. (2010). Expression of the zic1, zic2, zic3, and zic4 genes in early chick embryos. BMC Res. Notes.
55. McMahon, J.A., Takada, S., Zimmerman, L.B., Fan, C.-M., Harland, R.M., and McMahon, A.P. (1998). Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12, 1438–1452.
56. Melloy, P.., Ewart, J.., Cohen, M.., Desmond, M.., Kuehn, M.., and Lo, C.. (1998). No turning,a Mouse Mutation Causing Left–Right and Axial Patterning Defects. Dev. Biol. 193, 77–89.
57. Murillo, B., Ruiz-Reig, N., Herrera, M., Fairen, a., and Herrera, E. (2015). Zic2 Controls the Migration of Specific Neuronal Populations in the Developing Forebrain. J. Neurosci. 35, 11266–11280.
58. Nagai, T., Aruga, J., Takada, S., Gu, T., Spo, R., Schughart, K., and Mikoshiba, K. (1997). Gene Suggests an Essential Role for Zic Genes in Body Pattern Formation. 313, 299–313.
59. Nagai, T., Aruga, J., Minowa, O., Sugimoto, T., Ohno, Y., Noda, T., and Mikoshiba, K. (2000). Zic2 regulates the kinetics of neurulation. In Proceedings of the National Academy of Sciences of the United States of America, pp. 1618–1623.
60. Nakata, K., Nagai, T., Aruga, J., and Mikoshiba, K. (1998). Xenopus Zic family and its role in neural and neural crest development.
61. Nakata, K., Koyabu, Y., Aruga, J., and Mikoshiba, K. (2000). A novel member of the Xenopus Zic family, Zic5, mediates neural crest development. Mech. Dev. 99, 83–91.
62. Niederreither, K., Vermot, J., Schuhbaur, B., Chambon, P., and Dollé, P. (2000). Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Dev. Camb. Engl. 127, 75–85.
63. Nitzan, E., Avraham, O., Kahane, N., Ofek, S., Kumar, D., and Kalcheim, C. (2016). Dynamics of BMP and Hes1/Hairy1 signaling in the dorsal neural tube underlies the transition from neural crest to definitive roof plate. BMC Biol. 14.
64. Nyholm, M.K., Wu, S.-F., Dorsky, R.I., and Grinblat, Y. (2007). The zebrafish zic2a-zic5 gene pair acts downstream of canonical Wnt signaling to control cell proliferation in the developing tectum. Dev. Camb. Engl. 134, 735–746.
65. Nyholm, M.K., Abdelilah-Seyfried, S., and Grinblat, Y. (2009). A novel genetic mechanism regulates dorsolateral hinge-point formation during zebrafish cranial neurulation. J. Cell Sci. 122, 2137–2148.
66. Pourebrahim, R., Houtmeyers, R., Ghogomu, S., Janssens, S., Thelie, A., Tran, H.T., Langenberg, T., Vleminckx, K., Bellefroid, E., Cassiman, J.J., et al. (2011). Transcription factor Zic2 inhibits Wnt/??-catenin protein signaling. J. Biol. Chem. 286, 37732–37740.
67. Saeger, B.M., Suhm, M., and Neubu, A. (2011). Ephrin / ephrin Receptor Expression During Early Stages of Mouse Inner Ear Development.
68. Sanek, N.A., and Grinblat, Y. (2008). A novel role for zebrafish zic2a during forebrain development. Dev. Biol. 317, 325–335.
69. Santiago, A., and Erickson, C.A. (2002). Ephrin-B ligands play a dual role in the control of neural crest cell migration. Development 129, 3621–3632.
70. Sato, T., Sasai, N., and Sasai, Y. (2005). Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 132, 2355–2363.
71. Sela-Donenfeld, D., and Kalcheim, C. (2000). Inhibition of noggin expression in the dorsal neural tube by somitogenesis: a mechanism for coordinating the timing of neural crest emigration. Dev. Camb. Engl. 127, 4845–4854.
72. Smith, a, Robinson, V., Patel, K., and Wilkinson, D.G. (1997). The EphA4 and EphB1 receptor tyrosine kinases and ephrin-B2 ligand regulate targeted migration of branchial neural crest cells. Curr. Biol. CB 7, 561–570.
73. Taniguchi, K., Anderson, A.E., Sutherland, A.E., and Wotton, D. (2012). of Tgif Function Causes HoloprosenceLoss phaly by Disrupting the Shh Signaling Pathway. PLoS Genet. 8, e1002524.
74. Taniguchi, K., Anderson, A.E., Melhuish, T.A., Carlton, A.L., Manukyan, A., Sutherland, A.E., and Wotton, D. (2017). Genetic and Molecular Analyses indicate independent effects of TGIFs on Nodal and Gli3 in neural tube patterning. Eur. J. Hum. Genet. 25, 208–215.
75. TeSlaa, J.J., Keller, A.N., Nyholm, M.K., and Grinblat, Y. (2013). Zebrafish Zic2a and Zic2b regulate neural crest and craniofacial development. Dev. Biol. 380, 73–86.
76. Thomas, A.J., and Erickson, C. a (2009). FOXD3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Dev. Camb. Engl. 136, 1849–1858.
77. Thomas, S., Thomas, M., Wincker, P., Babarit, C., Xu, P., Speer, M.C., Munnich, A., Lyonnet, S., Vekemans, M., and Etchevers, H.C. (2008). Human neural crest cells display molecular and phenotypic hallmarks of stem cells. Hum. Mol. Genet. 17, 3411–3425.
78. Warr, N., Powles-Glover, N., Chappell, A., Robson, J., Norris, D., and Arkell, R.M. (2008). Zic2-associated holoprosencephaly is caused by a transient defect in the organizer region during gastrulation. Hum. Mol. Genet. 17, 2986–2996.
79. Wilson, L., Gale, E., Chambers, D., and Maden, M. (2004). Retinoic acid and the control of dorsoventral patterning in the avian spinal cord. Dev. Biol. 269, 433–446.
80. Wilson, S., Rydström, A., Trimborn, T., Willert, K., Nusse, R., Jessell, T.M., and Edlund, T. (2001). The status of Wnt signalling regulates neural and epidermal fates in the chick embryo. Nature 411, 325–330.
81. Wotton, D., Lo, R.S., Lee, S., and Massagué, J. (1999). A Smad Transcriptional Corepressor. Cell 97, 29–39.
82. Ybot-Gonzalez, P., Cogram, P., Gerrelli, D., and Copp, A.J. (2002). Sonic hedgehog and the molecular regulation of mouse neural tube closure. Dev. Camb. Engl. 129, 2507–2517.
83. Ybot-Gonzalez, P., Gaston-Massuet, C., Girdler, G., Klingensmith, J., Arkell, R., Greene, N.D.E., and Copp, A.J. (2007). Neural plate morphogenesis during mouse neurulation is regulated by antagonism of Bmp signalling. Development 134, 3203–3211.
84. Zohn, I.E., and Sarkar, A.A. (2008). Modeling neural tube defects in the mouse. Curr. Top. Dev. Biol. 84, 1–35.