Selective inactivation of Otx2 mRNA isoforms reveals isoform-specific requirement for visceral endoderm anteriorization and head morphogenesis and highlights cell diversity in the visceral endoderm

Mechanisms of Development

Volumn 126, Issue 10, 2009, Pages 882-897

  Acampora, Dario ^a,c   Di Giovannantonio, Luca Giovanni ^a   Di Salvio, Michela ^a   Mancuso, Pietro ^a   Simeone, Antonio ^a,b,c  

^a CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^b European School of Molecular Medicine SEMM   (Italy)

^c INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

A P axis conversion; Dkk1; Forebrain; Gastrulation; Head morphogenesis; Lefty1; Midbrain; Otx2; Visceral endoderm

Indexed keywords

DICKKOPF 1 PROTEIN; GENE PRODUCT; ISOPROTEIN; MESSENGER RNA; PROTEIN LEFTY1; TRANSCRIPTION FACTOR OTX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; EMBRYO DEVELOPMENT; ENDODERM; FOREBRAIN; GASTRULATION; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENETIC VARIABILITY; MESENCEPHALON; MORPHOGENESIS; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; ENDODERM; GENE EXPRESSION PROFILING; HEAD; IMMUNOHISTOCHEMISTRY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LEFT-RIGHT DETERMINATION FACTORS; MESENCEPHALON; MICE; MORPHOGENESIS; OTX TRANSCRIPTION FACTORS; PROSENCEPHALON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VISCERA;

EID: 70349512750     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2009.07.003     Document Type: Article

References (44)

1. Acampora D., Annino A., Puelles E., Alfano I., Tuorto F., and Simeone A. OTX1 compensates for OTX2 requirement in regionalisation of anterior neuroectoderm. Gene Expr. Patterns 3 (2003) 497-501
2. Acampora D., Avantaggiato V., Tuorto F., Briata P., Corte G., and Simeone A. Visceral endoderm-restricted translation of Otx1 mediates recovery of Otx2 requirements for specification of anterior neural plate and normal gastrulation. Development 125 (1998) 5091-5104
3. Acampora D., Mazan S., Lallemand Y., Avantaggiato V., Maury M., Simeone A., and Brûlet P. Forebrain and midbrain regions are deleted in Otx2-/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 121 (1995) 279-290
4. Acampora D., Pilo Boyl P., Signore M., Martinez-Barbera J.P., Ilengo C., Puelles E., Annino A., Reichert H., Corte G., and Simeone A. OTD/OTX2 functional equivalence depends on 5′ and 3′ UTR-mediated control of Otx2 mRNA for nucleo-cytoplasmic export and epiblast-restricted translation. Development 128 (2001) 4801-4813
5. Ang S.L., Jin O., Rhinn M., Daigle N., Stevenson L., and Rossant J. A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development 122 (1996) 243-252
6. Beddington R.S., and Robertson E.J. Axis development and early asymmetry in mammals. Cell 96 (1999) 195-209
7. Bertocchini F., and Stern C.D. The hypoblast of the chick embryo positions the primitive streak by antagonizing nodal signaling. Dev. Cell 3 (2002) 735-744
8. Courtois V., Chatelain G., Han Z.Y., Le Novère N., Brun G., and Lamonerie T. New Otx2 mRNA isoforms expressed in the mouse brain. J. Neurochem. 84 (2003) 840-853
9. Dufort D., Schwartz L., Harpal K., and Rossant J. The transcription factor HNF3beta is required in visceral endoderm for normal primitive streak morphogenesis. Development 125 (1998) 3015-3025
10. Filosa S., Rivera-Pérez J.A., Gómez A.P., Gansmuller A., Sasaki H., Behringer R.R., and Ang S.L. Goosecoid and HNF-3beta genetically interact to regulate neural tube patterning during mouse embryogenesis. Development 124 (1997) 2843-2854
11. Foley A.C., Skromne I., and Stern C.D. Reconciling different models of forebrain induction and patterning: a dual role for the hypoblast. Development 127 (2000) 3839-3854
12. Fossat N., Courtois V., Chatelain G., Brun G., and Lamonerie T. Alternative usage of Otx2 promoters during mouse development. Dev. Dyn. 233 (2005) 154-160
13. Glinka A., Wu W., Delius H., Monaghan A.P., Blumenstock C., and Niehrs C. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391 (1998) 357-362
14. Kimura C., Yoshinaga K., Tian E., Suzuki M., Aizawa S., and Matsuo I. Visceral endoderm mediates forebrain development by suppressing posteriorizing signals. Dev. Biol. 225 (2000) 304-321
15. Kimura W., Yasugi S., Stern C.D., and Fukuda K. Fate and plasticity of the endoderm in the early chick embryo. Dev. Biol. 289 (2006) 283-295
16. Kimura-Yoshida C., Nakano H., Okamura D., Nakao K., Yonemura S., Belo J.A., Aizawa S., Matsui Y., and Matsuo I. Canonical Wnt signaling and its antagonist regulate anterior-posterior axis polarization by guiding cell migration in mouse visceral endoderm. Dev. Cell 9 (2005) 639-650
17. Kwon G.S., Viotti M., and Hadjantonakis A.K. The endoderm of the mouse embryo arises by dynamic widespread intercalation of embryonic and extraembryonic lineages. Dev. Cell 15 (2008) 509-520
18. Lewis S.L., Khoo P.L., De Young R.A., Steiner K., Wilcock C., Mukhopadhyay M., Westphal H., Jamieson R.V., Robb L., and Tam P.P. Dkk1 and Wnt3 interact to control head morphogenesis in the mouse. Development 135 (2008) 1791-1801
19. Mallamaci A., Di Blas E., Briata P., Boncinelli E., and Corte G. OTX2 homeoprotein in the developing central nervous system and migratory cells of the olfactory area. Mech. Dev. 58 (1996) 165-178
20. Martinez-Barbera J.P., Signore M., Pilo Boyl P., Puelles E., Acampora D., Gogoi R., Schubert F., Lumsden A., and Simeone A. Regionalisation of anterior neuroectoderm and its competence in responding to forebrain and midbrain inducing activities depend on mutual antagonism between OTX2 and GBX2. Development 128 (2001) 4789-4800
21. Matsuo I., Kuratani S., Kimura C., Takeda N., and Aizawa S. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 9 (1995) 2646-2658
22. Meno C., Ito Y., Saijoh Y., Matsuda Y., Tashiro K., Kuhara S., and Hamada H. Two closely-related left-right asymmetrically expressed genes, lefty-1 and lefty-2: their distinctexpression domains, chromosomal linkage and direct neuralizing activity in Xenopus embryos. Genes Cells 2 (1997) 513-524
23. Morgan R., Hooiveld M.H., Pannese M., Dati G., Broders F., Delarue M., Thiery J.P., Boncinelli E., and Durston A.J. Calponin modulates the exclusion of Otx-expressing cells from convergence extension movements. Nat. Cell Biol. 1 (1999) 404-408
24. Mukhopadhyay M., Shtrom S., Rodriguez-Esteban C., Chen L., Tsukui T., Gomer L., Dorward D.W., Glinka A., Grinberg A., Huang S.P., Niehrs C., Belmonte J.C., and Westphal H. Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev. Cell 1 (2001) 423-434
25. Nagy A., Gertsenstein M., Vintersten K., and Behringer R. Manipulating the Mouse Embryo: A Laboratory Manual. third ed. (2003), Cold Spring Harbor Press, Cold Spring Harbor, NY
26. Perea-Gomez A., Lawson K.A., Rhinn M., Zakin L., Brûlet P., Mazan S., and Ang S.L. Otx2 is required for visceral endoderm movement and for the restriction of posterior signals in the epiblast of the mouse embryo. Development 128 (2001) 753-765
27. Perea-Gomez A., Vella F.D., Shawlot W., Oulad-Abdelghani M., Chazaud C., Meno C., Pfister V., Chen L., Robertson E., Hamada H., Behringer R.R., and Ang S.L. Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks. Dev. Cell 3 (2002) 745-756
28. Pilo Boyl P., Signore M., Acampora D., Martinez-Barbera J.P., Ilengo C., Annino A., Corte G., and Simeone A. Forebrain and midbrain development requires epiblast-restricted Otx2 translational control mediated by its 3′ UTR. Development 128 (2001) 2989-3000
29. Rhinn M., Dierich A., Shawlot W., Behringer R.R., Le Meur M., and Ang S.L. Sequential roles for Otx2 in visceral endoderm and neuroectoderm for forebrain and midbrain induction and specification. Development 125 (1998) 845-856
30. Rivera-Pérez J.A., Mager J., and Magnuson T. Dynamic morphogenetic events characterize the mouse visceral endoderm. Dev. Biol. 261 (2003) 470-487
31. Rodriguez T.A., Srinivas S., Clements M.P., Smith J.C., and Beddington R.S. Induction and migration of the anterior visceral endoderm is regulated by the extra-embryonic ectoderm. Development 132 (2005) 2513-2520
32. Shawlot W., Wakamiya M., Kwan K.M., Kania A., Jessell T.M., and Behringer R.R. Lim1 is required in both primitive streak-derived tissues and visceral endoderm for head formation in the mouse. Development 126 (1999) 4925-4932
33. Simeone, A., 1999. Detection of mRNA in tissue sections with radiolabelled riboprobes. In situ hybridization, second ed. In: Wilkinson, D.G. (Ed.), A Practical Approach, Oxford University Press, Oxford, IRL, pp. 69-86.
34. Simeone A. Role of Otx2 during gastrulation. In: Stern C.D. (Ed). Gastrulation: From Cells to Embryo (2004), Cold Spring Harbor Press, New York 553-561
35. Srinivas S. The anterior visceral endoderm-turning heads. Genesis 44 (2006) 565-572
36. Srinivas S., Rodriguez T., Clements M., Smith J.C., and Beddington R.S. Active cell migration drives the unilateral movements of the anterior visceral endoderm. Development 131 (2004) 1157-1164
37. Stern C.D. Initial patterning of the central nervous system: how many organizers?. Nat. Rev. Neurosci. 2 (2001) 92-98
38. Stern C.D. Neural induction. In: Stern C.D. (Ed). Gastrulation: From Cells to Embryo (2004), Cold Spring Harbor Press, New York 419-432
39. Stern C.D. Aptly named visceral endoderm. Dev. Cell 15 (2008) 493-494
40. Tam P.P.L., and Gad J.L. Gastrulation in the mouse embryo. In: Stern C.D. (Ed). Gastrulation: From Cells to Embryo (2004), Cold Spring Harbor Press 233-262
41. Tam P.P., and Steiner K.A. Anterior patterning by synergistic activity of the early gastrula organizer and the anterior germ layer tissues of the mouse embryo. Development 126 (1999) 5171-5179
42. Varlet I., Collignon J., and Robertson E.J. Nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 124 (1997) 1033-1044
43. Yamamoto M., Saijoh Y., Perea-Gomez A., Shawlot W., Behringer R.R., Ang S.L., Hamada H., and Meno C. Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428 (2004) 387-392
44. Zakin L., Reversade B., Virlon B., Rusniok C., Glaser P., Elalouf J.M., and Brulet P. Gene expression profiles in normal and Otx2-/- early gastrulating mouse embryos. Proc. Natl. Acad. Sci. USA 97 (2000) 14388-14393