Setdb2 controls convergence and extension movements during zebrafish gastrulation by transcriptional regulation of dvr1

Developmental Biology

Volumn 392, Issue 2, 2014, Pages 233-244

  Du, Ting Ting ^a   Xu, Peng Fei ^c   Dong, Zhi Wei ^b   Fan, Hong Bo ^b   Jin, Yi ^a   Dong, Mei ^b   Chen, Yi ^a   Pan, Wei Jun ^b   Ren, Rui Bao ^a   Liu, Ting Xi ^a,b   Deng, Min ^b   Huang, Qiu Hua ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Chinese Academy of Sciences   (China)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Convergence and extension; Dvr1; Histone methylation; Setdb2; TGF superfamily; Zebrafish

Indexed keywords

HISTONE; PROTEIN SETDB2; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL MIGRATION; CELL MOTION; CELL POLARITY; DEVELOPMENTAL STAGE; DVR1 GENE; GASTRULATION; GENE; GENE TARGETING; MESODERM; NONHUMAN; NOTOCHORD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RHOMBENCEPHALON; SETDB2 GENE; SOMITE; TRANSCRIPTION REGULATION; UPREGULATION;

DANIO RERIO;

CONVERGENCE AND EXTENSION; DVR1; HISTONE METHYLATION; SETDB2; TGF-Β SUPERFAMILY; ZEBRAFISH;

ANIMALS; BLOTTING, WESTERN; CELL MOVEMENT; FLUORESCENT ANTIBODY TECHNIQUE; GASTRULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; HISTONE-LYSINE N-METHYLTRANSFERASE; IN SITU HYBRIDIZATION; MICROARRAY ANALYSIS; MORPHOLINOS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSFORMING GROWTH FACTOR BETA; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84904384193     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.05.022     Document Type: Article

References (64)

1. Andersen I.S., Ostrup O., Lindeman L.C., Aanes H., Reiner A.H., Mathavan S., Alestrom P., Collas P. Epigenetic complexity during the zebrafish mid-blastula transition. Biochem. Biophys. Res. Commun. 2012, 417:1139-1144.
2. Andersson O., Bertolino P., Ibanez C.F. Distinct and cooperative roles of mammalian Vg1 homologs GDF1 and GDF3 during early embryonic development. Dev. Biol. 2007, 311:500-511.
3. Ataliotis P., Symes K., Chou M.M., Ho L., Mercola M. PDGF signalling is required for gastrulation of Xenopus laevis. Development 1995, 121:3099-3110.
4. Bakkers J., Kramer C., Pothof J., Quaedvlieg N.E., Spaink H.P., Hammerschmidt M. Has2 is required upstream of Rac1 to govern dorsal migration of lateral cells during zebrafish gastrulation. Development 2004, 131:525-537.
5. Birsoy B., Kofron M., Schaible K., Wylie C., Heasman J. Vg 1 is an essential signaling molecule in Xenopus development. Development 2006, 133:15-20.
6. Chan J., Mably J.D., Serluca F.C., Chen J.N., Goldstein N.B., Thomas M.C., Cleary J.A., Brennan C., Fishman M.C., Roberts T.M. Morphogenesis of prechordal plate and notochord requires intact Eph/ephrin B signaling. Dev. Biol. 2001, 234:470-482.
7. Chen Q., Takada R., Takada S. Loss of Porcupine impairs convergent extension during gastrulation in zebrafish. J. Cell. Sci. 2012, 125:2224-2234.
8. Cheng S.K., Olale F., Bennett J.T., Brivanlou A.H., Schier A.F. EGF-CFC proteins are essential coreceptors for the TGF-beta signals Vg1 and GDF1. Genes Dev. 2003, 17:31-36.
9. Coyle R.C., Latimer A., Jessen J.R. Membrane-type 1 matrix metalloproteinase regulates cell migration during zebrafish gastrulation: evidence for an interaction with non-canonical Wnt signaling. Exp. Cell Res. 2008, 314:2150-2162.
10. Dohrmann C.E., Kessler D.S., Melton D.A. Induction of axial mesoderm by zDVR-1, the zebrafish orthologue of Xenopus Vg1. Dev. Biol. 1996, 175:108-117.
11. Fu Y.F., Du T.T., Dong M., Zhu K.Y., Jing C.B., Zhang Y., Wang L., Fan H.B., Chen Y., Jin Y., Yue G.P., Chen S.J., Chen Z., Huang Q.H., Jing Q., Deng M., Liu T.X. Mir-144 selectively regulates embryonic alpha-hemoglobin synthesis during primitive erythropoiesis. Blood 2009, 113:1340-1349.
12. Ghil J.S., Chung H.M. Evidence that platelet derived growth factor (PDGF) action is required for mesoderm patterning in early amphibian (Xenopus laevis) embryogenesis. Int. J. Dev. Biol. 1999, 43:329-334.
13. Glickman N.S., Kimmel C.B., Jones M.A., Adams R.J. Shaping the zebrafish notochord. Development 2003, 130:873-887.
14. Hammerschmidt M., Pelegri F., Mullins M.C., Kane D.A., Brand M., van Eeden F.J., Furutani-Seiki M., Granato M., Haffter P., Heisenberg C.P., Jiang Y.J., Kelsh R.N., Odenthal J., Warga R.M., Nusslein-Volhard C. Mutations affecting morphogenesis during gastrulation and tail formation in the zebrafish, Danio rerio. Development 1996, 123:143-151.
15. Hatta K., Tsujii H., Omura T. Cell tracking using a photoconvertible fluorescent protein. Nat. Protoc. 2006, 1:960-967.
16. Heisenberg C.P., Tada M., Rauch G.J., Saude L., Concha M.L., Geisler R., Stemple D.L., Smith J.C., Wilson S.W. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 2000, 405:76-81.
17. Hyatt B.A., Lohr J.L., Yost H.J. Initiation of vertebrate left-right axis formation by maternal Vg1. Nature 1996, 384:62-65.
18. Jessen J.R., Topczewski J., Bingham S., Sepich D.S., Marlow F., Chandrasekhar A., Solnica-Krezel L. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell Biol. 2002, 4:610-615.
19. Jones T.L., Chong L.D., Kim J., Xu R.H., Kung H.F., Daar I.O. Loss of cell adhesion in Xenopus laevis embryos mediated by the cytoplasmic domain of XLerk, an erythropoietin-producing hepatocellular ligand. Proc. Natl. Acad. Sci. USA 1998, 95:576-581.
20. Kaasinen E., Aittomaki K., Eronen M., Vahteristo P., Karhu A., Mecklin J.P., Kajantie E., Aaltonen L.A., Lehtonen R. Recessively inherited right atrial isomerism caused by mutations in growth/differentiation factor 1 (GDF1). Hum. Mol. Genet. 2010, 19:2747-2753.
21. Keller R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 2002, 298:1950-1954.
22. Kilian B., Mansukoski H., Barbosa F.C., Ulrich F., Tada M., Heisenberg C.P. The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech. Dev. 2003, 120:467-476.
23. Kim S.H., Yamamoto A., Bouwmeester T., Agius E., Robertis E.M. The role of paraxial protocadherin in selective adhesion and cell movements of the mesoderm during Xenopus gastrulation. Development 1998, 125:4681-4690.
24. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
25. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
26. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 2002, 3:662-673.
27. Li X., Ma Y., Li D., Gao X., Li P., Bai N., Luo M., Tan X., Lu C., Ma X. Arsenic impairs embryo development via down-regulating Dvr1 expression in zebrafish. Toxicol. Lett. 2012, 212:161-168.
28. Lindeman L.C., Andersen I.S., Reiner A.H., Li N., Aanes H., Ostrup O., Winata C., Mathavan S., Muller F., Alestrom P., Collas P. Prepatterning of developmental gene expression by modified histones before zygotic genome activation. Dev Cell. 2011, 21:993-1004.
29. Lindeman L.C., Winata C.L., Aanes H., Mathavan S., Alestrom P., Collas P. Chromatin states of developmentally-regulated genes revealed by DNA and histone methylation patterns in zebrafish embryos. Int. J. Dev. Biol. 2010, 54:803-813.
30. Matsui T., Bessho Y. Left-right asymmetry in zebrafish. Cell. Mol. Life Sci. 2012, 69:3069-3077.
31. Matsui T., Raya A., Kawakami Y., Callol-Massot C., Capdevila J., Rodriguez-Esteban C., Izpisua Belmonte J.C. Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev. 2005, 19:164-175.
32. Miyagi C., Yamashita S., Ohba Y., Yoshizaki H., Matsuda M., Hirano T. STAT3 noncell-autonomously controls planar cell polarity during zebrafish convergence and extension. J. Cell Biol. 2004, 166:975-981.
33. Myers D.C., Sepich D.S., Solnica-Krezel L. Bmp activity gradient regulates convergent extension during zebrafish gastrulation. Dev. Biol. 2002, 243:81-98.
34. Myers D.C., Sepich D.S., Solnica-Krezel L. Convergence and extension in vertebrate gastrulae: cell movements according to or in search of identity?. Trends Genet. 2002, 18:447-455.
35. Oates A.C., Lackmann M., Power M.A., Brennan C., Down L.M., Do C., Evans B., Holder N., Boyd A.W. An early developmental role for eph-ephrin interaction during vertebrate gastrulation. Mech. Dev. 1999, 83:77-94.
36. Oishi I., Kawakami Y., Raya A., Callol-Massot C., Izpisua Belmonte J.C. Regulation of primary cilia formation and left-right patterning in zebrafish by a noncanonical Wnt signaling mediator, duboraya. Nat. Genet. 2006, 38:1316-1322.
37. Peterson A.G., Wang X., Joseph Yost H. Dvr1 transfers left-right asymmetric signals from Kupffer's vesicle to lateral plate mesoderm in zebrafish. Dev. Biol. 2013, 382:198-208.
38. Rankin C.T., Bunton T., Lawler A.M., Lee S.J. Regulation of left-right patterning in mice by growth/differentiation factor-1. Nat. Genet. 2000, 24:262-265.
39. Rauch G.J., Hammerschmidt M., Blader P., Schauerte H.E., Strahle U., Ingham P.W., McMahon A.P., Haffter P. Wnt5 is required for tail formation in the zebrafish embryo. Cold Spring Harb. Symp. Quant. Biol. 1997, 62:227-234.
40. Robu M.E., Larson J.D., Nasevicius A., Beiraghi S., Brenner C., Farber S.A., Ekker S.C. p53 activation by knockdown technologies. PLoS Genet. 2007, 3:e78.
41. Roszko I., Sawada A., Solnica-Krezel L. Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway. Semin. Cell Dev. Biol. 2009, 20:986-997.
42. Schier A.F., Talbot W.S. Molecular genetics of axis formation in zebrafish. Annu. Rev. Genet. 2005, 39:561-613.
43. Sepich D.S., Myers D.C., Short R., Topczewski J., Marlow F., Solnica-Krezel L. Role of the zebrafish trilobite locus in gastrulation movements of convergence and extension. Genesis 2000, 27:159-173.
44. Solnica-Krezel L. Gastrulation in zebrafish - all just about adhesion?. Curr. Opin. Genet. Dev. 2006, 16:433-441.
45. Solnica-Krezel L., Driever W. The role of the homeodomain protein Bozozok in zebrafish axis formation. Int. J. Dev. Biol. 2001, 45:299-310.
46. Stickney H.L., Imai Y., Draper B., Moens C., Talbot W.S. Zebrafish bmp4 functions during late gastrulation to specify ventroposterior cell fates. Dev. Biol. 2007, 310:71-84.
47. Sumanas S., Kim H.J., Hermanson S., Ekker S.C. Zebrafish frizzled-2 morphant displays defects in body axis elongation. Genesis 2001, 30:114-118.
48. Thisse C., Thisse B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 2008, 3:59-69.
49. Topczewski J., Sepich D.S., Myers D.C., Walker C., Amores A., Lele Z., Hammerschmidt M., Postlethwait J., Solnica-Krezel L. The zebrafish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev. Cell. 2001, 1:251-264.
50. Tsai Y.J., Pan H., Hung C.M., Hou P.T., Li Y.C., Lee Y.J., Shen Y.T., Wu T.T., Li C. The predominant protein arginine methyltransferase PRMT1 is critical for zebrafish convergence and extension during gastrulation. FEBS J. 2011, 278:905-917.
51. Ulrich F., Concha M.L., Heid P.J., Voss E., Witzel S., Roehl H., Tada M., Wilson S.W., Adams R.J., Soll D.R., Heisenberg C.P. Slb/Wnt11 controls hypoblast cell migration and morphogenesis at the onset of zebrafish gastrulation. Development 2003, 130:5375-5384.
52. Ungar A.R., Kelly G.M., Moon R.T. Wnt4 affects morphogenesis when misexpressed in the zebrafish embryo. Mech Dev. 1995, 52:153-164.
53. van Eekelen M., Runtuwene V., Overvoorde J., den Hertog J. RPTPalpha and PTPepsilon signaling via Fyn/Yes and RhoA is essential for zebrafish convergence and extension cell movements during gastrulation. Dev. Biol. 2010, 340:626-639.
54. von der Hardt S., Bakkers J., Inbal A., Carvalho L., Solnica-Krezel L., Heisenberg C.P., Hammerschmidt M. The Bmp gradient of the zebrafish gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr. Biol. 2007, 17:475-487.
55. Wall N.A., Craig E.J., Labosky P.A., Kessler D.S. Mesendoderm induction and reversal of left-right pattern by mouse Gdf1, a Vg1-related gene. Dev. Biol. 2000, 227:495-509.
56. Warga R.M., Kimmel C.B. Cell movements during epiboly and gastrulation in zebrafish. Development 1990, 108:569-580.
57. Williams B.B., Cantrell V.A., Mundell N.A., Bennett A.C., Quick R.E., Jessen J.R. VANGL2 regulates membrane trafficking of MMP14 to control cell polarity and migration. J. Cell Sci. 2012, 125:2141-2147.
58. Wu M.Y., Hill C.S. Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev. Cell. 2009, 16:329-343.
59. Xu P.F., Zhu K.Y., Jin Y., Chen Y., Sun X.J., Deng M., Chen S.J., Chen Z., Liu T.X. Setdb2 restricts dorsal organizer territory and regulates left-right asymmetry through suppressing fgf8 activity. Proc. Natl. Acad. Sci. USA 2010, 107:2521-2526.
60. Xu X., Shuen W.H., Chen C., Goudevenou K., Jones P., Sablitzky F. Swap70b is required for convergent and extension cell movement during zebrafish gastrulation linking Wnt11 signalling and RhoA effector function. Dev. Biol. 2013, 386:191-203.
61. Yamamoto A., Amacher S.L., Kim S.H., Geissert D., Kimmel C.B., De Robertis E.M. Zebrafish paraxial protocadherin is a downstream target of spadetail involved in morphogenesis of gastrula mesoderm. Development 1998, 125:3389-3397.
62. Yamashita S., Miyagi C., Carmany-Rampey A., Shimizu T., Fujii R., Schier A.F., Hirano T. Stat3 controls cell movements during zebrafish gastrulation. Dev. Cell. 2002, 2:363-375.
63. Yamashita S., Miyagi C., Fukada T., Kagara N., Che Y.S., Hirano T. Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer. Nature 2004, 429:298-302.
64. Yin C., Kiskowski M., Pouille P.A., Farge E., Solnica-Krezel L. Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J. Cell Biol. 2008, 180:221-232.