Histone deacetylase inhibitor Trichostatin A induces neural tube defects and promotes neural crest specification in the chicken neural tube

Differentiation

Volumn 85, Issue 1-2, 2013, Pages 55-66

  Murko, Christina ^a   Lagger, Sabine ^b,c   Steiner, Marianne ^a   Seiser, Christian ^b   Schoefer, Christian ^a   Pusch, Oliver ^a  

^a Medical University of Vienna   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Chick; Histone deacetylase; Neural crest; Neural tube defect; Trichostatin A

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CADHERIN; HISTONE DEACETYLASE; NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR SOX9; TRICHOSTATIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CHICKEN; EMBRYO; ENZYME ACTIVITY; NEURAL CREST; NEURAL TUBE DEFECT; NEUROEPITHELIUM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION;

ANIMALS; APOPTOSIS; BONE MORPHOGENETIC PROTEIN 4; CADHERINS; CHICK EMBRYO; HISTONE DEACETYLASE INHIBITORS; HYDROXAMIC ACIDS; NEURAL CREST; NEURAL TUBE; NEURAL TUBE DEFECTS; NEUROEPITHELIAL CELLS; TRANSCRIPTION FACTORS;

SPONDIAS PURPUREA; VERTEBRATA;

EID: 84872370840     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2012.12.001     Document Type: Article

References (60)

1. Bantscheff M., Hopf C., Savitski M.M., Dittmann A., Grandi P., Michon A.M., Schlegl J., Abraham Y., Becher I., Bergamini G., Boesche M., Delling M., Dümpelfeld B., Eberhard D., Huthmacher C., Mathieson T., Poeckel D., Reader V., Strunk K., Sweetman G., Kruse U., Neubauer G., Ramsden N.G., Drewes G. Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nature Biotechnology 2011, 29:255-265.
2. Bartl S., Taplick J., Lagger G., Khier H., Kuchler K., Seiser C. Identification of mouse histone deacetylase 1 as a growth factor-inducible gene. Molecular and Cellular Biology 1997, 17:5033-5043.
3. Basch M.L., Bronner-Fraser M., García-Castro M.I. Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 2006, 441:218-222.
4. Betancur P., Bronner-Fraser M., Sauka-Spengler T. Assembling neural crest regulatory circuits into a gene regulatory network. Annual Review of Cell and Developmental Biology 2010, 26:581-603.
5. Bhaskara S., Knutson S.K., Jiang G., Chandrasekharan M.B., Wilson A.J., Zheng S., Yenamandra A., Locke K., Yuan J.L., Bonine-Summers A.R., Wells C.E., Kaiser J.F., Washington M.K., Zhao Z., Wagner F.F., Sun Z.W., Xia F., Holson E.B., Khabele D., Hiebert S.W. Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell 2010, 18:436-447.
6. Brunmeir R., Lagger S., Seiser C. Histone deacetylase HDAC1/2-controlled embryonic development and cell differentiation. International Journal of Developmental Biology 2009, 53:275-289.
7. Coles E.G., Taneyhill L.A., Bronner-Fraser M. A critical role for Cadherin 6B in regulating avian neural crest emigration. Developmental Biology 2007, 312:533-544.
8. Copp A.J., Greene N.D., Murdoch J.N. The genetic basis of mammalian neurulation. Nature Reviews Genetics 2003, 4:784-793.
9. Damjanovski S., Sachs L.M., Shi Y.B. Multiple stage-dependent roles for histone deacetylases during amphibian embryogenesis: implications for the involvement of extracellular matrix remodeling. International Journal of Developmental Biology 2000, 44:769-776.
10. del Barrio M.G., Nieto M.A. Overexpression of snail family members highlights their ability to promote chick neural crest formation. Development 2002, 129:1583-1593.
11. Di Renzo F., Broccia M.L., Giavini E., Menegola E. Relationship between embryonic histonic hyperacetylation and axial skeletal defects in mouse exposed to the three HDAC inhibitors apicidin, MS-275, and sodium butyrate. Toxicological Sciences 2007, 98:582-588.
12. Eot-Houllier G., Fulcrand G., Magnaghi-Jaulin L., Jaulin C. Histone deacetylase inhibitors and genomic stability. Cancer Letters 2009, 274:169-176.
13. Epstein D.J., Vekemans M., Gros P. Splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax-3. Cell 1991, 67:767-774.
14. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heyningen V., Jessell T.M., Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 1997, 90:169-180.
15. Gregoretti I.V., Lee Y.M., Goodson H.V. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. Journal of Molecular Biology 2004, 338:17-31.
16. Haberland M., Montgomery R.L., Olson E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nature Reviews Genetics 2009, 10:32-42.
17. Haberland M., Mokalled M.H., Montgomery R.L., Olson E.N. Epigenetic control of skull morphogenesis by histone deacetylase 8. Genes & Development 2009, 23:1625-1630.
18. Haldin C.E., LaBonne C. SoxE factors as multifunctional neural crest regulatory factors. International Journal of Biochemistry & Cell Biology 2010, 42:441-444.
19. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. Developmental Dynamics 1992, 195:231-272.
20. Henion P.D., Blyss G.K., Luo R., An M., Maynard T.M., Cole G.J., Weston J.A. Avian transitin expression mirrors glia cell fate restrictions during neural crest development. Developmental Dynamics 2000, 218:150-159.
21. Henrique D., Adam J., Myat A., Chitnis A., Lewis J., Ish-Horowicz D. Expression of a Delta homolog in prospective neurons in the chick. Nature 1995, 375:787-790.
22. Ichi S., Costa F.F., Bischof J.M., Nakazaki H., Shen Y.W., Boshnjaku V., Sharma S., Mania-Farnell B., McLone D.G., Tomita T., Soares M.B., Mayanil C.S. Folic acid remodels chromatin on Hes1 and Neurog2 promoters during caudal neural tube development. Journal of Biological Chemistry 2010, 285:36922-36932.
23. Krispin S., Nitzan E., Kalcheim C. The dorsal neural tube: a dynamic setting for cell fate decisions. Developmental Neurobiology 2010, 70:796-812.
24. Lai I.L., Lin T.P., Yao Y.L., Lin C.Y., Hsieh M.J., Yang W.M. Histone deacetylase 10 relieves repression on the melanogenic program by maintaining the deacetylation status of repressors. Journal of Biological Chemistry 2010, 285:7187-7196.
25. Le Douarin N. The Neural Crest 1982, Cambridge University Press, New York.
26. Liu J.P., Jessell T.M. A role for rhoB in the delamination of neural crest cells from the dorsal neural tube. Development 1998, 125:5055-5067.
27. Ma Y., Cai S., Lu Q., Lu X., Jiang Q., Zhou J., Zhang C. Inhibition of protein deacetylation by trichostatin A impairs microtubule-kinetochore attachment. Cellular and Molecular Life Sciences 2008, 65:3100-3109.
28. Martínez-Morales P.L., Diez del Corral R., Olivera-Martínez I., Quiroga A.C., Das R.M., Barbas J.A., Storey K.G., Morales A.V. FGF and retinoic acid activity gradients control the timing of neural crest cell emigration in the trunk. Journal of Cell Biology 2011, 194:489-503.
29. Mayanil C.S., Pool A., Nakazaki H., Reddy A.C., Mania-Farnell B., Yun B., George D., McLone D.G., Bremer E.G. Regulation of murine TGFbeta2 by Pax3 during early embryonic development. Journal of Biological Chemistry 2006, 281:24544-24552.
30. Menegola E., Di Renzo F., Broccia M.L., Prudenziati M., Minucci S., Massa V., Giavini E. Inhibition of histone deacetylase activity on specific embryonic tissues as a new mechanism for teratogenicity. Birth Defects Research Part B: Developmental and ReproductiveToxicology 2005, 74:392-398.
31. Meulemans D., Bronner-Fraser M. Gene-regulatory interactions in neural crest evolution and development. Developmental Cell 2004, 7:291-299.
32. Miller C.P., Singh M.M., Rivera-Del Valle N., Manton C.A., Chandra J. Therapeutic strategies to enhance the anticancer efficacy of histone deacetylase inhibitors. Journal of Biomedicine and Biotechnology 2011, 2011:514261.
33. Murko C., Lagger S., Steiner M., Seiser C., Schoefer C., Pusch O. Expression of class I histone deacetylases during chick and mouse development. International Journal of Developmental Biology 2010, 54:1527-1537.
34. Nakazaki H., Reddy A.C., Mania- Farnell B.L., Shen Y.W., Ichi S., McCabe C., George D., McLone D.G., Tomita T., Mayanil C.S. Key basic helix-loop helix transcription factor genes Hes1 and Ngn2 are regulated by Pax3 during mouse embryonic development. Developmental Biology 2008, 316:510-523.
35. Nau H., Hauck R.S., Ehlers K. Valporic acid-induced neural tube defects in mouse and human: aspects of chirality, alternative drug development, pharmacokinetics and possible mechanisms. Pharmacology and Toxicology 1991, 69:310-321.
36. Noh E.J., Lee J.S. Functional interplay between modulation of histone deacetylase activity and its regulatory role in G2-M transition. Biochemical and Biophysical Research Communications 2003, 310:267-273.
37. Park K.S., Gumbiner B.M. Cadherin 6B induces BMP signaling and de-epithelialization during the epithelial mesenchymal transition of the neural crest. Development 2010, 137:2691-2701.
38. Reichert N., Choukrallah M.A., Matthias P. Multiple roles of class I HDACs in proliferation, differentiation and development. Cellular and Molecular Life Sciences 2012, 10.1007/s00018-012-0921-9.
39. Robbins A.R., Jablonski S.A., Yen T.J., Yoda K., Robey R., Bates S.E., Sackett D.L. Inhibitors of histone deacetylases alter kinetochore assembly by disrupting pericentromeric heterochromatin. Cell Cycle 2005, 4:717-726.
40. Robert T., Vanoli F., Chiolo I., Shubassi G., Bernstein K.A., Rothstein R., Botrugno O.A., Parazzoli D., Oldani A., Minucci S., Foiani M. HDACs link the DNA damage response, processing of double-strand breaks and autophagy. Nature 2011, 471:74-79.
41. Sauka-Spengler T., Bronner-Fraser M. A gene regulatory network orchestrates neural crest formation. Nature Reviews Molecular Cell Biology 2008, 9:557-568.
42. Schuettengruber B., Simboeck E., Khier H., Seiser C. Autoregulation of mouse histone deacetylase 1 expression. Molecular and Cellular Biology 2003, 23:6993-7004.
43. Sela-Donenfeld D., Kalcheim C. Regulation of the onset of neural crest migration by coordinated activity of BMP4 and Noggin in the dorsal neural tube. Development 1999, 126:4749-4762.
44. Shakéd M., Weissmüller K., Svoboda H., Hortschansky P., Nishino N., Wölfl S., Tucker K.L. Histone deacetylases control neurogenesis in embryonic brain by inhibition of BMP2/4 signaling. PLoS One 2008, 3:e2668.
45. Shin H.J., Baek K.H., Jeon A.H., Kim S.J., Jang K.L., Sung Y.C., Kim C.M., Lee C.W. Inhibition of histone deacetylase activity increases chromosomal instability by the aberrant regulation of mitotic checkpoint activation. Oncogene 2003, 22:3853-3858.
46. Shookhoff J.M., Gallicano G.I. A new perspective on neural tube defects: folic acid and microRNA missexpression. Genesis 2010, 48:282-294.
47. Singh N., Trivedi C.M., Lu M., Mullican S.E., Lazar M.A., Epstein J.A. Histone deacetylase 3 regulates smooth muscle differentiation in neural crest cells and development of the cardiac outflow tract. Circulation Research 2011, 109:1240-1249.
48. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
49. Strobl-Mazzulla P.H., Sauka-Spengler T., Bronner-Fraser M. Histone demethylase JmjD2A regulates neural crest specification. Developmental Cell 2010, 19:460-468.
50. Ververis K., Karagiannis T.C. Potential non-oncological applications of histone deacetylase inhibitors. American Journal of Translational Research 2011, 3:454-467.
51. Vincent M., Duband J.L., Thiery J.P. A cell surface determinant expressed early on migrating avian neural crest cells. Brain Research 1983, 285:235-238.
52. Wallingford J.B. Neural tube closure and neural tube defects: studies in animal models reveal known knowns and known unknowns. American Journal of Medical Genetics Part C: Seminars in Medical Genetics 2005, 135C:59-68.
53. Wang Z., Zang C., Cui K., Schones D.E., Barski A., Peng W., Zhao K. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009, 138:1019-1031.
54. Werner T., Hammer A., Wahlbuhl M., Bösl M.R., Wegner M. Multiple conserved regulatory elements with overlapping functions determine Sox10 expression in mouse embryogenesis. Nucleic Acids Research 2007, 35:6526-6538.
55. Yang X.J., Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nature Reviews Molecular Cell Biology 2008, 9:206-218.
56. Yoshida M., Kijima M., Akita M., Beppu T. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. Journal of Biological Chemistry 1990, 265:17174-17179.
57. Zhang Y., Kwon S., Yamaguchi T., Cubizolles F., Rousseaux S., Kneissel M., Cao C., Li N., Cheng H.L., Chua K., Lombard D., Mizeracki A., Matthias G., Alt F.W., Khochbin S., Matthias P. Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Molecular and Cellular Biology 2008, 28:1688-1701.
58. Zhao W., Dai F., Bonafede A., Schafer S., Jung M., Yusuf F., Gamel A.J., Wang J., Brand-Saberi B. Histone deaceteylase inhibitor, trichostatin A, affects gene expression patterns during morphogenesis of chicken limb buds in vivo. Cells Tissues Organs 2009, 190:121-134.
59. Zilberman Y., Ballestrem C., Carramusa L., Mazitschek R., Khochbin S., Bershadsky A. Regulation of microtubule dynamics by inhibition of the tubulin deacetylase HDAC6. Journal of Cell Science 2009, 122:3531-3541.
60. Zupkovitz G., Tischler J., Posch M., Sadzak I., Ramsauer K., Egger G., Grausenburger R., Schweifer N., Chiocca S., Decker T., Seiser C. Negative and positive regulation of gene expression by mouse histone deacetylase 1. Molecular and Cellular Biology 2006, 26:7913-7928.