Etiology of craniofacial malformations in mouse models of blepharophimosis, ptosis and epicanthus inversus syndrome

Human Molecular Genetics

Volumn 24, Issue 6, 2015, Pages 1670-1681

  Heude, Églantine ^a   Bellessort, Brice ^a   Fontaine, Anastasia ^a   Hamazaki, Manatsu ^b   Treier, Anna Corina ^c   Treier, Mathias ^c   Levi, Giovanni ^a   Narboux Nême, Nicolas ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b UNIVERSITY OF TOKYO   (Japan)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; DESMIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXL2; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXL2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; BLEPHAROPHIMOSIS PTOSIS EPICANTHUS INVERSUS SYNDROME; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; CRANIAL MESODERMAL CELL; CRANIAL NEURAL CREST CELL; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MALFORMATION; DISEASE ASSOCIATION; EXTRAOCULAR MUSCLE; EYE MOVEMENT; EYELID CLOSURE; EYELID DISEASE; GENE DELETION; GENE EXPRESSION; GENETIC DISORDER; HEAD; HYPOPLASIA; INFERIOR OBLIQUE MUSCLE; MESODERMAL CELL; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; NEURAL CREST CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SKELETAL MUSCLE; ANIMAL; BLEPHAROPHIMOSIS; CONGENITAL MALFORMATION; CRANIOFACIAL ABNORMALITIES; EMBRYOLOGY; EYELID; GENETICS; SKIN ABNORMALITIES; UROGENITAL ABNORMALITIES;

MUS;

ANIMALS; BLEPHAROPHIMOSIS; CRANIOFACIAL ABNORMALITIES; EYELIDS; FORKHEAD TRANSCRIPTION FACTORS; GENE DELETION; GENE EXPRESSION; MICE; OCULOMOTOR MUSCLES; SKIN ABNORMALITIES; UROGENITAL ABNORMALITIES;

EID: 84934765375     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu579     Document Type: Article

References (53)

1. Vignes, N.I. (1889) Epicanthus hereditaire. Rev. Gen. Ophtal., 8, 438.
2. Decock, C.E., De Baere, E.E., Bauters, W., Shah, A.D., Delaey, C., Forsyth, R., Leroy, B.P., Kestelyn, P. and Claerhout, I. (2011) Insights into levator muscle dysfunction in a cohort of patients with molecularly confirmed blepharophimosis-ptosis-epicanthus inversus syndrome using high-resolution imaging, anatomic examination, and histopathologic examination. Arch. Ophthalmol., 129, 1564-1569.
3. Dollfus, H., Stoetzel, C., Riehm, S., Lahlou Boukoffa, W., Bediard Boulaneb, F., Quillet, R., Abu-Eid, M., Speeg-Schatz, C., Francfort, J.J., Flament, J. et al. (2003) Sporadic and familial blepharophimosis-ptosis-epicanthus inversus syndrome: FOXL2 mutation screen and MRI study of the superior levator eyelid muscle. Clin. Genet., 63, 117-120.
4. Chawla, B., Bhadange, Y., Dada, R., Kumar, M., Sharma, S., Bajaj, M.S., Pushker, N., Chandra, M. and Ghose, S. (2013) Clinical, radiologic, and genetic features in blepharophimosis, ptosis, and epicanthus inversus syndrome in the Indian population. Invest. Ophthalmol. Vis. Sci., 54, 2985-2991.
5. Zlotogora, J., Sagi, M. and Cohen, T. (1983) The blepharophimosis, ptosis, and epicanthus inversus syndrome: delineation of two types. Am. J. Hum. Genet., 35, 1020-1027.
6. Crisponi, L., Deiana, M., Loi, A., Chiappe, F., Uda, M., Amati, P., Bisceglia, L., Zelante, L., Nagaraja, R., Porcu, S. et al. (2001) The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat. Genet., 27, 159-166.
7. De Baere, E., Dixon, M.J., Small, K.W., Jabs, E.W., Leroy, B.P., Devriendt, K., Gillerot, Y., Mortier, G., Meire, F., Van Maldergem, L. et al. (2001) Spectrum of FOXL2 gene mutations in blepharophimosis-ptosis-epicanthus inversus (BPES) families demonstrates a genotype-phenotype correlation. Hum. Mol. Genet., 10, 1591-1600.
8. Beysen, D., De Paepe, A. and De Baere, E. (2009) FOXL2 mutations and genomic rearrangements in BPES. Hum. Mutat., 30, 158-169.
9. Beysen, D., Raes, J., Leroy, B.P., Lucassen, A., Yates, J.R., Clayton-Smith, J., Ilyina, H., Brooks, S.S., Christin-Maitre, S., Fellous, M. et al. (2005) Deletions involving long-range conserved nongenic sequences upstream and downstream of FOXL2 as a novel disease-causing mechanism in blepharophimosis syndrome. Am. J. Hum. Genet., 77, 205-218.
10. D'Haene, B., Attanasio, C., Beysen, D., Dostie, J., Lemire, E., Bouchard, P., Field, M., Jones, K., Lorenz, B., Menten, B. et al. (2009) Disease-causing 7.4 kb cis-regulatory deletion disrupting conserved non-coding sequences and their interaction with the FOXL2 promotor: implications for mutation screening. PLoS Genet., 5, e1000522.
11. Oley, C. and Baraitser, M. (1988) Blepharophimosis, ptosis, epicanthus inversus syndrome (BPES syndrome). J. Med. Genet., 25, 47-51.
12. Beaconsfield, M., Walker, J.W. and Collin, J.R. (1991) Visual development in the blepharophimosis syndrome. Br. J. Ophthalmol., 75, 746-748.
13. Vincent, A.L., Watkins, W.J., Sloan, B.H. and Shelling, A.N. (2005) Blepharophimosis and bilateral Duane syndrome associated with a FOXL2 mutation. Clin. Genet., 68, 520-523.
14. Shah, B.M., Dada, T., Panda, A., Tanwar, M., Bhartiya, S. and Dada, R. (2013) Novel occurrence of axenfeld: Rieger syndrome in a patient with blepharophimosis ptosis epicanthus inversus syndrome. Indian J. Ophthalmol., 63, 358-360.
15. Ng, J.K., Stout, A.U., Aaby, A.A. and Ng, J.D. (2014) Blepharophimosis syndrome with absent tear production. Ophthal. Plast. Reconstr. Surg. (Epub ahead of print).
16. Cocquet, J., Pailhoux, E., Jaubert, F., Servel, N., Xia, X., Pannetier, M., De Baere, E., Messiaen, L., Cotinot, C., Fellous, M. et al. (2002) Evolution and expression of FOXL2. J. Med. Genet., 39, 916-921.
17. Pisarska, M.D., Bae, J., Klein, C. and Hsueh, A.J. (2004) Forkhead l2 is expressed in the ovary and represses the promoter activity of the steroidogenic acute regulatory gene. Endocrinology, 145, 3424-3433.
18. Shi, F., Ding, S., Zhao, S., Han, M., Zhuang, Y., Xu, T. and Wu, X. (2014) A piggyBac insertion disrupts Foxl2 expression that mimics BPES syndrome in mice. Hum. Mol. Genet., 23, 3792-3800.
19. Schmidt, D., Ovitt, C.E., Anlag, K., Fehsenfeld, S., Gredsted, L., Treier, A.C. and Treier, M. (2004) The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development, 131, 933-942.
20. Couly, G., Grapin-Botton, A., Coltey, P., Ruhin, B. and Le Douarin, N.M. (1998) Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development, 125, 3445-3459.
21. LeLievre. (1978) Participation of neural crest derived cells in the genesis of the skull in birds. J. Embryol. Exp. Morphol., 47, 17-37.
22. McBratney-Owen, B., Iseki, S., Bamforth, S.D., Olsen, B.R. and Morriss-Kay, G.M. (2008) Development and tissue origins of the mammalian cranial base. Dev. Biol., 322, 121-132.
23. Noden, D.M. (1983) The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Am. J. Anat., 168, 257-276.
24. Trainor, P.A., Tan, S.S. and Tam, P.P. (1994) Cranial paraxial mesoderm: regionalisation of cell fate and impact on craniofacial development in mouse embryos. Development, 120, 2397-2408.
25. Yoshida, T., Vivatbutsiri, P., Morriss-Kay, G., Saga, Y. and Iseki, S. (2008) Cell lineage in mammalian craniofacial mesenchyme. Mech. Dev., 125, 797-808.
26. Trainor, P.A. (2013) Neural Crest Cells: Evolution, Development and Disease. Academic Press, Oxford, UK.
27. Ellsworth, B.S., Egashira, N., Haller, J.L., Butts, D.L., Cocquet, J., Clay, C.M., Osamura, R.Y. and Camper, S.A. (2006) FOXL2 in the pituitary: molecular, genetic, and developmental analysis. Mol. Endocrinol., 20, 2796-2805.
28. Uhlenhaut, N.H., Jakob, S., Anlag, K., Eisenberger, T., Sekido, R., Kress, J., Treier, A.C., Klugmann, C., Klasen, C., Holter, N. I. et al. (2009) Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell, 139, 1130-1142.
29. Uda, M., Ottolenghi, C., Crisponi, L., Garcia, J.E., Deiana, M., Kimber, W., Forabosco, A., Cao, A., Schlessinger, D. and Pilia, G. (2004) Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum. Mol. Genet., 13, 1171-1181.
30. Zhang, Y., Kao, W.W., Pelosi, E., Schlessinger, D. and Liu, C.Y. (2011) Notch gain of function in mouse periocular mesenchyme downregulates FoxL2 and impairs eyelid levator muscle formation, leading to congenital blepharophimosis. J. Cell Sci., 124, 2561-2572.
31. Tan, S.S. and Morriss-Kay, G.M. (1986) Analysis of cranial neural crest cell migration and early fates in postimplantation rat chimaeras. J. Embryol. Exp. Morphol., 98, 21-58.
32. Noden, D.M. and Trainor, P.A. (2005) Relations and interactions between cranial mesoderm and neural crest populations. J. Anat., 207, 575-601.
33. Findlater, G.S., McDougall, R.D. and Kaufman, M.H. (1993) Eyelid development, fusion and subsequent reopening in the mouse. J. Anat., 183, 121-129.
34. Ng, S.K., Chan, W., Marcet, M.M., Kakizaki, H. and Selva, D. (2013) Levator palpebrae superioris: an anatomical update. Orbit, 32, 76-84.
35. Jeong, J., Li, X., McEvilly, R.J., Rosenfeld, M.G., Lufkin, T. and Rubenstein, J.L. (2008) Dlx genes pattern mammalian jaw primordium by regulating both lower jaw-specific and upper jaw-specific genetic programs. Development, 135, 2905-2916.
36. Walls, G.L. (1942) The Vertebrate Eye and its Adaptative Radiation. Hafner, New York.
37. Wotton, K.R., French, K.E. and Shimeld, S.M. (2007) The developmental expression of foxl2 in the dogfish Scyliorhinus canicula. Gene Expr. Patterns, 7, 793-797.
38. Cocquet, J., De Baere, E., Gareil, M., Pannetier, M., Xia, X., Fellous, M. and Veitia, R.A. (2003) Structure, evolution and expression of the FOXL2 transcription unit. Cytogenet. Genome Res., 101, 206-211.
39. Luetteke, N.C., Qiu, T.H., Peiffer, R.L., Oliver, P., Smithies, O. and Lee, D.C. (1993) TGF alpha deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell, 73, 263-278.
40. Mongan, M., Wang, J., Liu, H., Fan, Y., Jin, C., Kao, W.Y. and Xia, Y. (2011) Loss of MAP3K1 enhances proliferation and apoptosis during retinal development. Development, 138, 4001-4012.
41. Bildsoe, H., Loebel, D.A., Jones, V.J., Hor, A.C., Braithwaite, A. W., Chen, Y.T., Behringer, R.R. and Tam, P.P. (2013) The mesenchymal architecture of the cranial mesoderm of mouse embryos is disrupted by the loss of Twist1 function. Dev. Biol., 374, 295-307.
42. Swartz, M.E., Eberhart, J., Pasquale, E.B. and Krull, C.E. (2001) EphA4/ephrin-A5 interactions in muscle precursor cell migration in the avian forelimb. Development, 128, 4669-4680.
43. Rinon, A., Lazar, S., Marshall, H., Buchmann-Moller, S., Neufeld, A., Elhanany-Tamir, H., Taketo, M.M., Sommer, L., Krumlauf, R. and Tzahor, E. (2007) Cranial neural crest cells regulate head muscle patterning and differentiation during vertebrate embryogenesis. Development, 134, 3065-3075.
44. Heude, E., Bouhali, K., Kurihara, Y., Kurihara, H., Couly, G., Janvier, P. and Levi, G. (2010) Jaw muscularization requires Dlx expression by cranial neural crest cells. Proc. Natl Acad. Sci. USA, 107, 11441-11446.
45. De Baere, E. (2004) Blepharophimosis, ptosis, and epicanthus inversus. In: Pagon, R.A., Adam, M.P., Ardinger, H.H., Bird, T. D., Dolan, C.R., Fong, C.T., Smith, R.J.H. and Stephens, K. (eds) GeneReviews®, Seattle, WA: University of Washington, Seattle.
46. Tronina, S.A., Bobrova, N.F. and Khrinenko, V.P. (2006) Clinical and anatomical substantiation of levator resection in the complex surgical treatment of BPES. Orbit, 25, 5-10.
47. Albert, D.M., Frayer, W.C., Black, H.E., Massicotte, S.J., Sang, D. N. and Soque, J. (1986) The harderian gland: its tumors and its relevance to humans. Trans. Am. Ophthalmol. Soc., 84, 321-341.
48. Athappilly, G.K. and Braverman, R.S. (2009) Congenital alacrima in a patient with blepharophimosis syndrome. Ophthalmic Genet., 30, 37-39.
49. Byun, T.H., Kim, J.T., Park, H.W. and Kim, W.K. (2011) Timetable for upper eyelid development in staged human embryos and fetuses. Anat. Rec., 294, 789-796.
50. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 21, 70-71.
51. Matsuoka, T., Ahlberg, P.E., Kessaris, N., Iannarelli, P., Dennehy, U., Richardson, W.D., McMahon, A.P. and Koentges, G. (2005) Neural crest origins of the neck and shoulder. Nature, 436, 347-355.
52. Saga, Y., Miyagawa-Tomita, S., Takagi, A., Kitajima, S., Miyazaki, J. and Inoue, T. (1999) MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development, 126, 3437-3447.
53. Everett, M.M. and Miller, W.A. (1973) Adaptation of Mallory's trichrome stain to embryonic and fetal material. Stain Technol., 48, 5-8.