Ocular abnormalities in mice lacking the immunoglobulin superfamily member Cdo

FEBS Journal

Volumn 276, Issue 20, 2009, Pages 5998-6010

  Zhang, Wei ^a   Mulieri, Philip J ^a   Gaio, Ursula ^a   Bae, Gyu Un ^b   Krauss, Robert S ^a   Kang, Jong Sun ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Sungkyunkwan University   (South Korea)

Author keywords

Cdo; Coloboma; Congenital eye defect; Eye development; Lens

Indexed keywords

CADHERIN; CELL SURFACE IMMUNOGLOBULIN; NETRIN; PROTEIN CDO; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; COLOBOMA; CONTROLLED STUDY; ENZYME REGULATION; EYE DEVELOPMENT; MICROPHTHALMIA; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION MOLECULES; EYE; EYE PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; MALE; MICE; MICE, MUTANT STRAINS; PAIRED BOX TRANSCRIPTION FACTORS; PAX2 TRANSCRIPTION FACTOR; REPRESSOR PROTEINS; T-BOX DOMAIN PROTEINS;

ERINACEIDAE; MUS; VERTEBRATA;

EID: 70349487744     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07310.x     Document Type: Article

References (67)

1. Hero I (1989) The optic fissure in the normal and microphthalmic mouse. Exp Eye Res 49, 229 239.
2. Hero I, Farjah M Scholtz CL (1991) The prenatal development of the optic fissure in colobomatous microphthalmia. Invest Ophthalmol Vis Sci 32, 2622 2635.
3. Otteson DC, Shelden E, Jones JM, Kameoka J Hitchcock PF (1998) Pax2 expression and retinal morphogenesis in the normal and Krd mouse. Dev Biol 193, 209 224.
4. Morrison D, FitzPatrick D, Hanson I, Williamson K, van Heyningen V, Fleck B, Jones I, Chalmers J Campbell H (2002) National study of microphthalmia, anophthalmia, and coloboma (MAC) in Scotland: investigation of genetic aetiology. J Med Genet 39, 16 22.
5. Fitzpatrick DR van Heyningen V (2005) Developmental eye disorders. Curr Opin Genet Dev 15, 348 353.
6. Graw J (1996) Genetic aspects of embryonic eye development in vertebrates. Dev Genet 18, 181 197.
7. Jean D, Ewan K Gruss P (1998) Molecular regulators involved in vertebrate eye development. Mech Dev 76, 3 18.
8. Chow RL Lang RA (2001) Early eye development in vertebrates. Annu Rev Cell Dev Biol 17, 255 296.
9. Hyer J, Kuhlman J, Afif E Mikawa T (2003) Optic cup morphogenesis requires pre-lens ectoderm but not lens differentiation. Dev Biol 259, 351 363.
10. 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.
11. Ashery-Padan R Gruss P (2001) Pax6 lights-up the way for eye development. Curr Opin Cell Biol 13, 706 714.
12. 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.
13. Saha MS, Servetnick M Grainger RM (1992) Vertebrate eye development. Curr Opin Genet Dev 2, 582 588.
14. Huh S, Hatini V, Marcus RC, Li SC Lai E (1999) Dorsal-ventral patterning defects in the eye of BF-1 deficient mice associated with a restricted loss of Shh expression. Dev Biol 211, 53 63.
15. Ekker SC, Ungar AR, Greenstein P, von Kessler DP, Porter JA, Moon RT Beachy PA (1995) Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr Biol 5, 944 955.
16. Macdonald R, Barth KA, Xu Q, Holder N, Mikkola I Wilson SW (1995) Midline signalling is required for Pax gene regulation and patterning of the eyes. Development 121, 3267 3278.
17. Oliver G Gruss P (1997) Current views on eye development. Trends Neurosci 20, 415 421.
18. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H Beachy PA (1996) Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407 413.
19. Schimmenti L, de la Cruz J, Lewis R, Karkera J, Manligas G, Roessler E Muenke M (2003) Novel mutation in sonic hedgehog in non-syndromic colobomatous microphthalmia. Am J Med Genet A 116, 215 221.
20. Schwarz M, Cecconi F, Bernier G, Andrejewski N, Kammandel B, Wagner M Gruss P (2000) Spatial specification of mammalian eye territories by reciprocal transcriptional repression of Pax2 and Pax6. Development 127, 4325 4334.
21. Zhang XM Yang XJ (2001) Temporal and spatial effects of Sonic hedgehog signaling in chick eye morphogenesis. Dev Biol 233, 271 290.
22. Torres M, Gomez-Pardo E Gruss P (1996) Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122, 3381 3391.
23. Baumer N, Marquardt T, Stoykova A, Spieler D, Treichel D, Ashery-Padan R Gruss P (2003) Retinal pigmented epithelium determination requires the redundant activities of Pax2 and Pax6. Development 130, 2903 2915.
24. Hogan BL, Horsburgh G, Cohen J, Hetherington CM, Fisher G Lyon MF (1986) Small eyes (Sey): a homozygous lethal mutation on chromosome 2 which affects the differentiation of both lens and nasal placodes in the mouse. J Embryol Exp Morphol 97, 95 110.
25. Hill RE, Favor J, Hogan BL, Ton CC, Saunders GF, Hanson IM, Prosser J, Jordan T, Hastie ND van Heyningen V (1991) Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 354, 522 525.
26. Hanson IM, Seawright A, Hardman K, Hodgson S, Zaletayev D, Fekete G van Heyningen V (1993) PAX6 mutations in aniridia. Hum Mol Genet 2, 915 920.
27. Matsuo T, Osumi-Yamashita N, Noji S, Ohuchi H, Koyama E, Myokai F, Matsuo N, Taniguchi S, Doi H, Iseki S et al. (1993) A mutation in the Pax-6 gene in rat small eye is associated with impaired migration of midbrain crest cells. Nat Genet 3, 299 304.
28. Chalepakis G, Stoykova A, Wijnholds J, Tremblay P Gruss P (1993) Pax: gene regulators in the developing nervous system. J Neurobiol 24, 1367 1384.
29. Hanson IM, Fletcher JM, Jordan T, Brown A, Taylor D, Adams RJ, Punnett HH van Heyningen V (1994) Mutations at the PAX6 locus are found in heterogeneous anterior segment malformations including Peters' anomaly. Nat Genet 6, 168 173.
30. Glaser T, Jepeal L, Edwards JG, Young SR, Favor J Maas RL (1994) PAX6 gene dosage effect in a family with congenital cataracts, aniridia, anophthalmia and central nervous system defects. Nat Genet 7, 463 471. (Pubitemid 24308331)
31. Grindley JC, Davidson DR Hill RE (1995) The role of Pax-6 in eye and nasal development. Development 121, 1433 1442.
32. Quinn JC, West JD Hill RE (1996) Multiple functions for Pax6 in mouse eye and nasal development. Genes Dev 10, 435 446.
33. Hanson IM (2003) PAX6 and congenital eye malformations. Pediatr Res 54, 791 796.
34. Gibson-Brown JJ, Agulnik SI, Silver LM Papaioannou VE (1998) Expression of T-box genes Tbx2-Tbx5 during chick organogenesis. Mech Dev 74, 165 169.
35. Koshiba-Takeuchi K, Takeuchi JK, Matsumoto K, Momose T, Uno K, Hoepker V, Ogura K, Takahashi N, Nakamura H, Yasuda K et al. (2000) Tbx5 and the retinotectum projection. Science 287, 134 137.
36. Leconte L, Lecoin L, Martin P Saule S (2004) Pax6 interacts with cVax and Tbx5 to establish the dorsoventral boundary of the developing eye. J Biol Chem 279, 47272 47277.
37. Barbieri AM, Lupo G, Bulfone A, Andreazzoli M, Mariani M, Fougerousse F, Consalez GG, Borsani G, Beckmann JS, Barsacchi G et al. (1999) A homeobox gene, vax2, controls the patterning of the eye dorsoventral axis. Proc Natl Acad Sci USA 96, 10729 10734.
38. Bertuzzi S, Hindges R, Mui SH, O'Leary DD Lemke G (1999) The homeodomain protein vax1 is required for axon guidance and major tract formation in the developing forebrain. Genes Dev 13, 3092 3105.
39. Hallonet M, Hollemann T, Pieler T Gruss P (1999) Vax1, a novel homeobox-containing gene, directs development of the basal forebrain and visual system. Genes Dev 13, 3106 3114.
40. Mui SH, Kim JW, Lemke G Bertuzzi S (2005) Vax genes ventralize the embryonic eye. Genes Dev 19, 1249 1259.
41. Kang JS, Gao M, Feinlein JL, Cotter PD, Guadagno SN Krauss RS (1997) CDO: an oncogene-, serum-, and anchorage-regulated member of the Ig/fibronectin type III repeat family. J Cell Biol 138, 203 213.
42. Kang JS, Mulieri PJ, Miller C, Sassoon DA Krauss RS (1998) CDO, a Robo-related cell surface protein that mediates myogenic differentiation. J Cell Biol 143, 403 413.
43. Mulieri PJ, Okada A, Sassoon DA, McConnell SK Krauss RS (2000) Developmental expression pattern of the cdo gene. Dev Dyn 219, 40 49.
44. Cole F, Zhang W, Geyra A, Kang JS Krauss RS (2004) Positive regulation of myogenic bHLH factors and skeletal muscle development by the cell surface receptor CDO. Dev Cell 7, 843 854.
45. Kang JS, Mulieri PJ, Hu Y, Taliana L Krauss RS (2002) BOC, an Ig superfamily member, associates with CDO to positively regulate myogenic differentiation. EMBO J 21, 114 124.
46. Kang JS, Feinleib JL, Knox S, Ketteringham MA Krauss RS (2003) Pro-myogenic members of the Ig and cadherin families associate to positively regulate differentiation. Proc Natl Acad Sci USA 7, 3989 3994.
47. Kang JS, Yi MJ, Zhang W, Feinleib JL, Cole F Krauss RS (2004) Netrins and neogenin promote myotube formation. J Cell Biol 167, 493 504.
48. Kang JS, Bae GU, Yi MJ, Yang YJ, Oh JE, Takaesu G, Zhou YT, Low BC Krauss RS (2008) A Cdo/Bnip-2/Cdc42 signaling pathway regulates p38a/b MAPK activity and myogenic differentiation. J Cell Biol 182, 497 507.
49. Oh JE, Bae GU, Yang YJ, Yi MJ, Lee HJ, Kim BK, Krauss RS Kang JS (2009) Cdo promotes neuronal differentiation via activation of the p38MAPK pathway. FASEB J 23, 2088 2099.
50. Tenzen T, Allen BL, Cole F, Kang JS, Krauss RS McMahon AP (2006) The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev Cell 10, 647 656.
51. Cole F Krauss RS (2003) Microform of holoprosencephaly in mice that lack the Ig superfamily member Cdon. Curr Biol 13, 411 415.
52. Zhang W, Kang JS, Cole F, Yi MJ Krauss RS (2006) Cdo functions at multiple points in the Sonic Hedgehog pathway, and Cdo-deficient mice accurately model human holoprosencephaly. Dev Cell 10, 657 665.
53. Zhang W, Yi MJ, Chen X, Cole F, Krauss RS Kang JS (2006) Cortical thinning and hydrocephalus in mice lacking the immunoglobulin superfamily member CDO. Mol Cell Biol 26, 3764 3772.
54. Muenke M Beachy PA (2000) Genetics of ventral forebrain development and holoprosencephaly. Curr Opin Genet Dev 10, 262 269.
55. Chang B, Smith RS, Peters M, Savinova OV, Hawes NL, Zabaleta A, Nusinowitz S, Martin JE, Davisson ML, Cepko CL et al. (2001) Haploinsufficient Bmp4 ocular phenotypes include anterior segment dysgenesis with elevated intraocular pressure. BMC Genet 2, 18.
56. Murali D, Yoshikawa S, Corrigan RR, Plas DJ, Crair MC, Oliver G, Lyons KM, Mishina Y Furuta Y (2005) Distinct developmental programs require different levels of Bmp signaling during mouse retinal development. Development 132, 913 923.
57. Schedl A, Ross A, Lee M, Engelkamp D, Rashbass P, van Heyningen V Hastie ND (1996) Influence of PAX6 gene dosage on development: overexpression causes severe eye abnormalities. Cell 86, 71 82.
58. van Raamsdonk CD Tilghman SM (2000) Dosage requirement and allelic expression of PAX6 during lens placode formation. Development 127, 5439 5448.
59. Lang RA (2004) Pathways regulating lens induction in the mouse. Int J Dev Biol 48, 783 791.
60. Mikkola I, Bruun JA, Bjorkoy G, Holm T Johansen T (1999) Phosphorylation of the transactivation domain of Pax6 by extracellular signal-regulated kinase and p38 mitogen-activated protein kinase. J Biol Chem 274, 15115 15126.
61. Takaesu G, Kang JS, Bae GU, Yi MJ, Lee CM, Reddy EP Krauss RS (2006) Activation of p38alpha/beta MAPK in myogenesis via binding of the scaffold protein JLP to the cell surface protein Cdo. J Cell Biol 175, 383 388.
62. Miller GL, Somani S, Nowaczyk MJ, Feigenbaum A, Davidson RG, Costa T Levin AV (2006) The ocular manifestations of Jacobsen syndrome: a report of four cases and a review of the literature. Ophthalmic Genet 27, 1 7.
63. Pivnick EK, Velagaleti GV, Wilroy RS, Smith ME, Rose SR, Tipton RE Tharapel AT (1996) Jacobsen syndrome: report of a patient with severe eye anomalies, growth hormone deficiency, and hypothyroidism associated with deletion 11 (q23q25) and review of 52 cases. J Med Genet 33, 772 778.
64. Unique (2005). 11q deletion disorder: Jacobsen syndrome. Available at: http://www.rarechromo.org/INFO/FILES/11qTerminalDeletionSyndromeLeaflet.pdf (accessed 3 April 2006).
65. Stone DL, Kenyon KR, Green WR Ryan SJ (1976) Congenital central corneal leukoma (Peter's anomaly). Am J Ophthalmol 81, 173 193.
66. Churchill AJ, Booth AP, Anwar R Markham AF (1998) PAX 6 is normal in most cases of Peters' anomaly. Eye 12, 299 303.
67. Mulieri PJ, Kang JS, Sassoon DA Krauss RS (2002) Expression of the boc gene during murine embryogenesis. Dev Dyn 223, 379 388.