BMP-induced L-Maf regulates subsequent BMP-independent differentiation of primary lens fibre cells

Developmental Dynamics

Volumn 240, Issue 8, 2011, Pages 1917-1928

  Pandit, Tanushree ^a   Jidigam, Vijay K ^a   Gunhaga, Lena ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

crystallin; BMP; Chick; Development; Differentiation; L Maf; Lens; Lens fibre cells

Indexed keywords

BONE MORPHOGENETIC PROTEIN; DELTA CRYSTALLIN; L MAF PROTEIN; TRANSCRIPTION FACTOR MAF; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; EXPLANT; GAIN OF FUNCTION MUTATION; LENS EPITHELIUM; LENS FIBER; LOSS OF FUNCTION MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CHICK EMBRYO; DELTA-CRYSTALLINS; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; KERATINS; LENS, CRYSTALLINE; MAF TRANSCRIPTION FACTORS; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SOXB1 TRANSCRIPTION FACTORS;

EID: 79960359883     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22692     Document Type: Article

References (55)

1. Andersson E, Tryggvason U, Deng Q, Friling S, Alekseenko Z, Robert B, Perlmann T, Ericson J. 2006. Identification of intrinsic determinants of midbrain dopamine neurons. Cell 124: 393-405.
2. Artner I, Le Lay J, Hang Y, Elghazi L, Schisler JC, Henderson E, Sosa-Pineda B, Stein R. 2006. MafB: an activator of the glucagon gene expressed in developing islet alpha- and beta-cells. Diabetes 55: 297-304.
3. Ashery-Padan R, Marquardt T, Zhou X, Gruss P. 2000. Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev 14: 2701-2711.
4. Beebe DC, Piatigorsky J. 1981. Translational regulation of delta-crystallin synthesis during lens development in the chicken embryo. Dev Biol 84: 96-101.
5. Beebe D, Garcia C, Wang X, Rajagopal R, Feldmeier M, Kim JY, Chytil A, Moses H, Ashery-Padan R, Rauchman M. 2004. Contributions by members of the TGFbeta superfamily to lens development. Int J Dev Biol 48: 845-856.
6. Belecky-Adams TL, Adler R, Beebe DC. 2002. Bone morphogenetic protein signaling and the initiation of lens fibre cell differentiation. Development 129: 3795-3802.
7. Bhattacharyya S, Bailey AP, Bronner-Fraser M, Streit A. 2004. Segregation of lens and olfactory precursors from a common territory: cell sorting and reciprocity of Dlx5 and Pax6 expression. Dev Biol 271: 403-414.
8. Bower DJ, Errington LH, Pollock BJ, Morris S, Clayton RM. 1983. The pattern of expression of chick delta-crystallin genes in lens differentiation and in trans-differentiating cultured tissues. EMBO J 2: 333-338.
9. Chapman SC, Schubert FR, Schoenwolf GC, Lumsden A. 2002. Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. Dev Biol 245: 187-199.
10. Chizhikov VV, Millen KJ. 2004. Control of roof plate formation by Lmx1a in the developing spinal cord. Development 131: 2693-2705.
11. Couly GF, Le Douarin NM. 1985. Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev Biol 110: 422-439.
12. Donner AL, Episkopou V, Maas RL. 2007. Sox2 and Pou2f1 interact to control lens and olfactory placode development. Dev Biol 303: 784-799.
13. Dudley AT, Robertson EJ. 1997. Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev Dyn 208: 349-362.
14. Dutta S, Dietrich JE, Aspock G, Burdine RD, Schier A, Westerfield M, Varga ZM. 2005. pitx3 defines an equivalence domain for lens and anterior pituitary placode. Development 132: 1579-1590.
15. Faber SC, Robinson ML, Makarenkova HP, Lang RA. 2002. Bmp signaling is required for development of primary lens fibre cells. Development 129: 3727-3737.
16. Faure S, de Santa Barbara P, Roberts DJ, Whitman M. 2002. Endogenous patterns of BMP signaling during early chick development. Dev Biol 244: 44-65.
17. Francis PH, Richardson MK, Brickell PM, Tickle C. 1994. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. Development 120: 209-218.
18. French CR, Erickson T, French DV, Pilgrim DB, Waskiewicz AJ. 2009. Gdf6a is required for the initiation of dorsal-ventral retinal patterning and lens development. Dev Biol 333: 37-47.
19. Furuta Y, Hogan BL. 1998. BMP4 is essential for lens induction in the mouse embryo. Genes Dev 12: 3764-3775.
20. Hamburger V, Hamilton HL. 1951. Series of embryonic chicken growth. J Morphol 88: 49-92.
21. Hiramatsu Y, Suto A, Kashiwakuma D, Kanari H, Kagami S, Ikeda K, Hirose K, Watanabe N, Grusby MJ, Iwamoto I, Nakajima H. 2010. c-Maf activates the promoter and enhancer of the IL-21 gene, and TGF-beta inhibits c-Maf-induced IL-21 production in CD4+ T cells. J Leukoc Biol 87: 703-712.
22. Ho IC, Hodge MR, Rooney JW, Glimcher LH. 1996. The proto-oncogene c-maf is responsible for tissue-specific expression of interleukin-4. Cell 85: 973-983.
23. Kamachi Y, Uchikawa M, Tanouchi A, Sekido R, Kondoh H. 2001. Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes Dev 15: 1272-1286.
24. Kataoka K, Han SI, Shioda S, Hirai M, Nishizawa M, Handa H. 2002. MafA is a glucose-regulated and pancreatic beta-cell-specific transcriptional activator for the insulin gene. J Biol Chem 277: 49903-49910.
25. Kataoka K, Noda M, Nishizawa M. 1994. Maf nuclear oncoprotein recognizes sequences related to an AP-1 site and forms heterodimers with both Fos and Jun. Mol Cell Biol 14: 700-712.
26. Kawauchi S, Takahashi S, Nakajima O, Ogino H, Morita M, Nishizawa M, Yasuda K, Yamamoto M. 1999. Regulation of lens fibre cell differentiation by transcription factor c-Maf. J Biol Chem 274: 19254-19260.
27. Kerppola TK, Curran T. 1994. A conserved region adjacent to the basic domain is required for recognition of an extended DNA binding site by Maf/Nrl family proteins. Oncogene 9: 3149-3158.
28. Lamb TM, Knecht AK, Smith WC, Stachel SE, Economides AN, Stahl N, Yancopolous GD, Harland RM. 1993. Neural induction by the secreted polypeptide noggin. Science 262: 713-718.
29. Lovicu FJ, McAvoy JW. 2005. Growth factor regulation of lens development. Dev Biol 280: 1-14.
30. Manzanares M, Cordes S, Ariza-McNaughton L, Sadl V, Maruthainar K, Barsh G, Krumlauf R. 1999. Conserved and distinct roles of kreisler in regulation of the paralogous Hoxa3 and Hoxb3 genes. Development 126: 759-769.
31. Muta M, Kamachi Y, Yoshimoto A, Higashi Y, Kondoh H. 2002. Distinct roles of SOX2, Pax6 and Maf transcription factors in the regulation of lens-specific delta1-crystallin enhancer. Genes Cells 7: 791-805.
32. Nishimura W, Kondo T, Salameh T, El Khattabi I, Dodge R, Bonner-Weir S, Sharma A. 2006. A switch from MafB to MafA expression accompanies differentiation to pancreatic beta-cells. Dev Biol 293: 526-539.
33. Ogino H, Yasuda K. 1998. Induction of lens differentiation by activation of a bZIP transcription factor, L-Maf. Science 280: 115-118.
34. Olbrot M, Rud J, Moss LG, Sharma A. 2002. Identification of beta-cell-specific insulin gene transcription factor RIPE3b1 as mammalian MafA. Proc Natl Acad Sci U S A 99: 6737-6742.
35. Panganiban G, Sebring A, Nagy L, Carroll S. 1995. The development of crustacean limbs and the evolution of arthropods. Science 270: 1363-1366.
36. Patthey C, Edlund T, Gunhaga L. 2009. Wnt-regulated temporal control of BMP exposure directs the choice between neural plate border and epidermal fate. Development 136: 73-83.
37. Pevny LH, Sockanathan S, Placzek M, Lovell-Badge R. 1998. A role for SOX1 in neural determination. Development 125: 1967-1978.
38. Rajagopal R, Huang J, Dattilo LK, Kaartinen V, Mishina Y, Deng CX, Umans L, Zwijsen A, Roberts AB, Beebe DC. 2009. The type I BMP receptors, Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Dev Biol 335: 305-316.
39. Reza HM, Ogino H, Yasuda K. 2002. L-Maf, a downstream target of Pax6, is essential for chick lens development. Mech Dev 116: 61-73.
40. Reza HM, Yasuda K. 2004a. The involvement of neural retina pax6 in lens fibre differentiation. Dev Neurosci 26: 318-327.
41. Reza HM, Yasuda K. 2004b. Lens differentiation and crystallin regulation: a chick model. Int J Dev Biol 48: 805-817.
42. Reza HM, Nishi H, Kataoka K, Takahashi Y, Yasuda K. 2007. L-Maf regulates p27kip1 expression during chick lens fibre differentiation. Differentiation 75: 737-744.
43. Roberts C, Platt N, Streit A, Schachner M, Stern CD. 1991. The L5 epitope: an early marker for neural induction in the chick embryo and its involvement in inductive interactions. Development 112: 959-970.
44. Robinson ML. 2006. An essential role for FGF receptor signaling in lens development. Semin Cell Dev Biol 17: 726-740.
45. Shimada N, Aya-Murata T, Reza HM, Yasuda K. 2003. Cooperative action between L-Maf and Sox2 on delta-crystallin gene expression during chick lens development. Mech Dev 120: 455-465.
46. Shinohara T, Piatigorsky J. 1976. Quantitation of delta-crystallin messenger RNA during lens induction in chick embryos. Proc Natl Acad Sci U S A 73: 2808-2812.
47. Sjodal M, Edlund T, Gunhaga L. 2007. Time of exposure to BMP signals plays a key role in the specification of the olfactory and lens placodes ex vivo. Dev Cell 13: 141-149.
48. Streit A, Lee KJ, Woo I, Roberts C, Jessell TM, Stern CD. 1998. Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development 125: 507-519.
49. Takeuchi T, Kudo T, Ogata K, Hamada M, Nakamura M, Kito K, Abe Y, Ueda N, Yamamoto M, Engel JD, Takahashi S. 2009. Neither MafA/L-Maf nor MafB is essential for lens development in mice. Genes Cells 14: 941-947.
50. Timmer JR, Wang C, Niswander L. 2002. BMP signaling patterns the dorsal and intermediate neural tube via regulation of homeobox and helix-loop-helix transcription factors. Development 129: 2459-2472.
51. Tsuchiya M, Maeda A, Suzuki A, Yasuda K, Yoshida T, Nitta K, Tsuchiya K. 2009. Suppression of MafA mRNA with siRNA prevents adipose cell differentiation in 3T3-L1 cells. Int J Mol Med 23: 725-732.
52. Wawersik S, Purcell P, Rauchman M, Dudley AT, Robertson EJ, Maas R. 1999. BMP7 acts in murine lens placode development. Dev Biol 207: 176-188.
53. Wilkinson DG, Nieto MA. 1993. Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. Methods Enzymol 225: 361-373.
54. Xu J, Yang Y, Qiu G, Lal G, Wu Z, Levy DE, Ochando JC, Bromberg JS, Ding Y. 2009. c-Maf regulates IL-10 expression during Th17 polarization. J Immunol 182: 6226-6236.
55. Yoshida T, Yasuda K. 2002. Characterization of the chicken L-Maf, MafB and c-Maf in crystallin gene regulation and lens differentiation. Genes Cells 7: 693-706.