Negative and positive auto-regulation of BMP expression in early eye development

Developmental Biology

Volumn 407, Issue 2, 2015, Pages 256-264

  Huang, Jie ^a   Liu, Ying ^a   Filas, Benjamen ^a   Gunhaga, Lena ^b   Beebe, David C ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Auto regulation; BMP; Coloboma; Development; Lens; Specification

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; OSTEOGENIC PROTEIN 1; SECRETED FRIZZLED RELATED PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTOR;

ANIMAL TISSUE; ARTICLE; AUTOREGULATION; BMP GENE; BMP2 GENE; BMP4 GENE; BMP7 GENE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EXPLANT; EYE DEVELOPMENT; GENE EXPRESSION REGULATION; IN VITRO STUDY; INTRACELLULAR SIGNALING; LEGHORN CHICKEN; LENS; MOUSE; NONHUMAN; OPTIC DISK CUP; PRIORITY JOURNAL; PROTEIN EXPRESSION; SFRP2 GENE; TRANSCRIPTION REGULATION; ANIMAL; CHICK EMBRYO; CHO CELL LINE; COLOBOMA; CRICETULUS; ECTODERM; EMBRYOLOGY; EYE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; HAMSTER; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEINS; CHICK EMBRYO; CHO CELLS; COLOBOMA; CRICETINAE; CRICETULUS; ECTODERM; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; LENS, CRYSTALLINE; MICE, TRANSGENIC;

EID: 84952861473     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2015.09.009     Document Type: Article

References (42)

1. Ashery-Padan R., Marquardt T., Zhou X., Gruss P. Pax6 activity in the lens primordium is required for lens formation and for correct placement of single retina in the eye. Genes Dev. 2000, 14:2701-2711.
2. Bailey A.P., Bhattacharyya S., Bronner-Fraser M., Streit A. Lens specification is the ground state of all sensory placodes, from which FGF promotes olfactory identity. Dev. Cell 2006, 11:505-517.
3. Beebe D.C., Piatigorsky J. Translational regulation of delta-crystallin synthesis during lens development in the chicken embryo. Dev. Biol. 1981, 84:96-101.
4. Beebe D.C., Garcia C., Wang X., Rajagopal R., Feldmeier M., Kim J.Y., Chytil A., Moses H., Ashery-Padan R., Rauchman M. Contributions by members of the TGFbeta superfamily to lens development. Int. J. Dev. Biol. 2004, 48:845-856.
5. Beites C.L., Hollenbeck P.L.W., Kim J., Lovell-Badge R., Lander A.D., Calof A.L. Follistatin modulates a BMP autoregulatory loop to control the size and patterning of sensory domains in the developing tongue. Development 2009, 136:2187-2197.
6. Belecky-Adams T.L., Adler R., Beebe D.C. Bone morphogenetic protein signaling and the initiation of lens fiber cell differentiation. Dev. (Camb., Engl.) 2002, 129:3795-3802.
7. Bhattacharyya S., Bailey A.P., Bronner-Fraser M., Streit A. Segregation of lens and olfactory precursors from a common territory: cell sorting and reciprocity of Dlx5 and Pax6 expression. Dev. Biol. 2004, 271:403-414.
8. Chanut F., Heberlein U. Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 1997, 124:559-567.
9. Chapman S.C., Schubert F.R., Schoenwolf G.C., Lumsden A. Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. Dev. Biol. 2002, 245:187-199.
10. Dudley A., Robertson E.J. Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev. Dyn. 1997, 208:349-362.
11. Faber S.C., Robinson M.L., Makarenkova H.P., Lang R. BMP signaling is required for development of primary lens fiber cells. Development 2002, 129:3727-3737.
12. Faure S., de Santa Barbara P., Roberts D.J., Whitman M. Endogenous patterns of BMP signaling during early chick development. Dev. Biol. 2002, 244:44-65.
13. French C.R., Erickson T., French D.V., Pilgrim D.B., Waskiewicz A.J. Gdf6a is required for the initiation of dorsal-ventral retinal patterning and lens development. Dev. Biol. 2009, 333:37-47.
14. Furuta Y., Hogan B.L.M. BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 1998, 12:3764-3775.
15. Ghosh-Choudhury N., Ghosh Choudhury G., Harris M.A., Wozney J., Mundy G.R., Abboud S.L., Harris S.E. Autoregulation of mouse BMP-2 gene transcription is directed by the proximal promoter element. Biochem. Biophys. Res. Commun. 2001, 286:101-108.
16. Grainger R.M., Henry J.J., Saha M.S., Servetnick M. Recent progress on the mechanisms of embryonic lens formation. Eye 1992, 6:117-122.
17. Grainger R.M., Mannion J.E., Cook T.L., Zygar C.A. Defining intermediate stages in cell determination: acquisition of a lens-forming bias in head ectoderm during lens determination. Dev. Genet. 1997, 20:246-257.
18. Hendrix R.W., Zwaan J. Changes in the glycoprotein concentration of the extracellular matrix between lens and optic vesicle associated with early lens differentiation. Differentiation 1974, 2:357-362.
19. Hendrix R.W., Zwaan J. The matrix of the optic vesicle-presumptive lens interface during induction of the lens in the chicken embryo. J. Embryol. Morphol. 1975, 33:1023-1049.
20. Holly V.L., Widen S.A., Famulski J.K., Waskiewicz A.J. Sfrp1a and Sfrp5 function as positive regulators of Wnt and BMP signaling during early retinal development. Dev. Biol. 2014, 388:192-204.
21. Huang J., Rajagopal R., Liu Y., Dattilo L.K., Shaham O., Ashery-Padan R., Beebe D.C. The mechanism of lens placode formation: a case of matrix-mediated morphogenesis. Dev. Biol. 2011, 355:32-42.
22. Huang J., Liu Y., Oltean A., Beebe D.C. BMP4 from the optic vesicle specifies murine retina formation. Dev. Biol. 2015, 402:119-126.
23. Hyer J., Mima T., Mikawa T. FGF1 patterns the optic vesicle by directing the placement of the neural retina domain. Development 1998, 125:869-877.
24. Hyer J., Kuhlman J., Afif E., Mikawa T. Optic cup morphogenesis requires pre-lens ectoderm but not lens differentiation. Dev. Biol. 2003, 259:351-363.
25. Lamb T., Knecht A., Smith W., Stachel S., Economides A., Stahl N., Yancopolous G., Harland R. Neural induction by the secreted polypeptide noggin. Science 1993, 262:713-718.
26. Liu C., Nathans J. An essential role for frizzled 5 in mammalian ocular development. Development 2008, 135:3567-3576.
27. Morcillo J., Martinez-Morales J.R., Trousse F., Fermin Y., Sowden J.C., Bovolenta P. Proper patterning of the optic fissure requires the sequential activity of BMP7 and SHH. Development 2006, 133:3179-3190.
28. Murali D., Yoshikawa S., Corrigan R.R., Plas D.J., Crair M.C., Oliver G., Lyons K.M., Mishina Y., Furuta Y. Distinct developmental programs require different levels of Bmp signaling during mouse retinal development. Development 2005, 132:913-923.
29. Pandit T., Jidigam V.K., Gunhaga L. BMP-induced L-Maf regulates subsequent BMP-independent differentiation of primary lens fibre cells. Dev. Dyn. 2011, 240:1917-1928.
30. Pandit T., Jidigam V.K., Patthey C., Gunhaga L. Neural retina identity is specified by lens-derived BMP signals. Development 2015, 142:1850-1859.
31. Patthey C., Edlund T., Gunhaga L. Wnt-regulated temporal control of BMP exposure directs the choice between neural plate border and epidermal fate. Development 2009, 136:73-83.
32. Rajagopal R., Huang J., Dattilo L.K., Kaartinen V., Mishina Y., Deng C.X., Umans L., Zwijsen A., Roberts A.B., Beebe D.C. The type I BMP receptors, Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Dev. Biol. 2009, 335:305-316.
33. Sanyanusin P., Schimmenti L.A., McNoe L.A., Ward T.A., Pierpont M.E.M., Sullivan M.J., Dobyns W.B., Eccles M.R. Mutation of the PAX2 gene in a family with optic nerve colobomas, renal anomalies and vesicoureteral reflux. Nat. Genet. 1995, 9:358-364.
34. Sjödal M., Edlund T., Gunhaga L. Time of exposure to BMP signals plays a key role in the specification of the olfactory and lens placodes ex vivo. Dev. Cell 2007, 13:141-149.
35. Sullivan C.H., Braunstein L., Hazard-Leonards R.M., Holen A.L., Samaha F., Stephens L., Grainger R.M. A re-examination of lens induction in chicken embryos: in vitro studies of early tissue interactions. Int. J. Dev. Biol. 2004, 48:771-782.
36. Torres M., Gomez-Pardo E., Gruss P. Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 1996, 122:3381-3391.
37. Wawersik S., Purcell P., Rauchman M., Dudley A.T., Robertson E.J., Maas R. BMP7 acts in murine lens placode development. Dev. Biol. 1999, 207:176-188.
38. Viringipurampeer I.A., Ferreira T., DeMaria S., Yoon J.J., Shan X., Moosajee M., Gregory-Evans K., Ngai J., Gregory-Evans C.Y. Pax2 regulates a fadd-dependent molecular switch that drives tissue fusion during eye development. Hum. Mol. Genet. 2012, 21:2357-2369.
39. Zhang R., Huang H., Cao P., Wang Z., Chen Y., Pan Y. Sma- and Mad-related protein 7 (Smad 7) is required for embryonic eye development in the mouse. J. Biol. Chem. 2013, 288:10275-10285.
40. Zhao L., Saitsu H., Sun X., Shiota K., Ishibashi M. Sonic hedgehog is involved in formation of the ventral optic cup by limiting Bmp4 expression to the dorsal domain. Mech. Dev. 2010, 127:62-72.
41. Zhou C.-J., Molotkov A., Song L., Li Y., Pleasure D.E., Pleasure S.J., Wang Y.-Z. Ocular coloboma and dorsoventral neuroretinal patterning defects in Lrp6 mutant eyes. Dev. Dyn. 2008, 237:3681-3689.
42. Zwaan J., Webster E.H. Histochemical analysis of extracellular matrix material during embryonic mouse lens morphogenesis in an aphakic strain of mice. Dev. Biol. 1984, 104:380-389.