ALX4 dysfunction disrupts craniofacial and epidermal development

Human Molecular Genetics

Volumn 18, Issue 22, 2009, Pages 4357-4366

  Kayserili, Hulya ^a   Uz, Elif ^b   Niessen, Carien ^c   Vargel, Ibrahim ^b,e   Alanay, Yasemin ^b   Tuncbilek, Gokhan ^b   Yigit, Gokhan ^c   Uyguner, Oya ^a   Candan, Sukru ^a   Okur, Hamza ^b   Kaygin, Serkan ^d   Balci, Sevim ^b   Mavili, Emin ^b   Alikasifoglu, Mehmet ^b   Haase, Ingo ^c   Wollnik, Bernd ^c   Akarsu, Nurten Ayse ^b  

^a ISTANBUL UNIVERSITY   (Turkey)

^b HACETTEPE UNIVERSITY   (Turkey)

^c UNIVERSITY OF COLOGNE   (Germany)

^d Hemosoft Inc   (Turkey)

^e KIRIKKALE UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

ARISTALESS LIKE HOMEOBOX 4; CYTOSINE; GENE PRODUCT; RNA; THYMIDINE; UNCLASSIFIED DRUG;

ALOPECIA; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CARBOXY TERMINAL SEQUENCE; CHROMOSOME 11P; CONTROLLED STUDY; CORPUS CALLOSUM AGENESIS; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MALFORMATION; CRANIOFACIAL SYNOSTOSIS; EPIDERMAL DEVELOPMENT; FEMALE; FRONTOFACIAL DYSOSTOSIS SYNDROME; GENE MAPPING; HOMOZYGOSITY; HUMAN; HUMAN TISSUE; HYPERTELORISM; HYPOGONADISM; MENTAL DEFICIENCY; MORPHOGENESIS; NONSENSE MUTATION; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN FUNCTION; SKIN BIOPSY; SKULL DEFECT; STOP CODON; TURKEY (REPUBLIC);

CHILD; CHILD, PRESCHOOL; CHROMOSOME MAPPING; CRANIOFACIAL DYSOSTOSIS; DNA-BINDING PROTEINS; EPIDERMIS; FACIAL BONES; HUMANS; INFANT; MALE; MUTATION; TRANSCRIPTION FACTORS;

EID: 70350671697     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp391     Document Type: Article

References (44)

1. Carlson, B.M. (1994) Human Embryology and Developmental Biology. Mosby-Year Book Inc., Von Hoffmann Press, St Louis, Missouri.
2. Richman, J.M. and Tickle, C. (1992) Epithelial-mesenchymal interactions in the outgrowth of the limb buds and facial primordial in chick embryos. Dev. Biol., 54, 299-308.
3. Helms, J.A. and Schneider, R.A. (2003) Cranial skeletal biology. Nature, 423, 326-330.
4. Sedano, H.O., Cohen, M.M. Jr, Jirasek, J. and Gorlin, R.J. (1970) Frontonasal dysplasia. J. Pediatr., 76, 906-913.
5. Sedano, H.O. and Gorlin, R.J. (1988) Frontonasal malformation as a field defect and in syndromic associations. Oral. Surg. Oral. Med. Oral. Path., 65, 704-710.
6. Guion-Almeida, M.L., Richieri-Costa, A., Saavedra, D. and Cohen, M.M. Jr (1996) Frontonasal dysplasia, analysis of 21 cases and literature review. In. J. Oral. Maxillofac. Surg., 25, 91-97.
7. Slaney, S.F., Goodman, F.R., Eilers-Walsman, B.L.C., Hall, B.D., Williams, D.K., Young, I.D., Hayward, R.D., Jones, B.M., Christianson, A.L. and Winter, R.M. (1999) Acromelic frontonasal dysostosis. Am. J. Med. Genet., 83, 109-116.
8. Guion-Almeida, M.L. and Richieri-Costa, A. (2001) Frontonasal dysplasia, macroblepharon, eyelid colobomas, ear anomalies, macrostomia, mental retardation and CNS structural anomalies, defining the phenotype. Clin. Dysmorphol., 10, 81-86.
9. Twigg, S.R.F., Kan, R., Babbs, C., Bochukova, E.G., Robertson, S.P., Wall, S.A., Morriss-Kay, G.M. and Wilkie, A.O.M. (2004) Mutations of ephrin-B1 (EFNB1), a marker of tissue boundary formation, cause craniofrontonasal syndrome. Proc. Natl Acad. Sci. USA, 101, 8652-8657.
10. Wieland, I., Jakubiczka, S., Muschke, P., Cohen, M., Thiele, H., Gerlach, K.L., Adams, R.H. and Wieacker, P. (2004) Mutations of the ephrin-B1 gene cause craniofrontonasal syndrome. Am. J. Hum. Genet. 74, 1209-1215.
11. Tessier, P. (1976) Anatomical classification facial, cranio-facial and latero-facial clefts. J. Maxillofac. Surg., 4, 69-92.
12. Kawamoto, H.K. Jr (1976) The kaleidoscopic world of rare craniofacial clefts, order out of chaos (Tessier classification). Clin. Plast. Surg., 3, 529-572.
13. Lander, E.S. and Botstein, D. (1987) Homozygosity mapping, a way to map human recessive traits with the DNA of inbred children. Science, 236, 1567-1570.
14. Qu, S., Niswender, K.D., Ji, Q., van der Meer, R., Keeney, D., Magnuson, M.A. and Wisdom, R. (1997) Polydactyly and ectopic ZPA formation in Alx-4 mutant mice. Development, 124, 3999-4008.
15. Qu, S., Tucker, S.C., Ehrlich, J.S., Levorse, J.M., Flaherty, L.A., Wisdom, R. and Vogt, T.F. (1998) Mutations in mouse aristaless-like4 cause Strong's luxoid polydactyly. Development, 125, 2711-2721.
16. Wuyts, W., Cleiren, E., Homfray, T., Rasore-Quartino, A., Vanhoenacker, F. and Van Hul, W. (2000) The ALX4 homeobox gene is mutated in patients with ossification defects of the skull (foramina parietalia permagna, OMIM 168500). J. Med. Genet., 37, 916-920.
17. Mavrogiannis, L.A., Antonopoulou, I., Baxova, A., Kutilek, S., Kim, C.A., Sugayama, S.M., Salamanca, A., Wall, S.A., Morriss-Kay, G.M. and Wilkie, A.O.M. (2001) Haploinsufficiency of the human homeobox gene ALX4 causes skull ossification defects. Nat. Genet., 27, 17-18.
18. Mavrogiannis, L.A., Taylor, I.B., Davies, S.J., Ramos, F.J., Olivares, J.L. and Wilkie, A.O.M. (2006) Enlarged parietal foramina caused by mutations in the homeobox genes ALX4 and MSX2, from genotype to phenotype. Eur. J. Hum. Genet., 14, 151-158.
19. Qu, S., Li, L. and Wisdom, R. (1997) Alx-4, cDNA cloning and characterization of a novel paired-type homeodomain protein. Gene, 203, 217-223.
20. Hudson, R., Taniguchi-Sidle, A., Boras, K., Wiggan, O. and Hamel, P.A. (1998) Alx-4, a transcriptional activator whose expression is restricted to sites of epithelial-mesenchymal interactions. Dev. Dyn., 213 159-169.
21. Boras, K. and Hamel, P.A. (2002) Alx4 binding to LEF-1 regulates N-CAM promoter activity. J. Biol. Chem., 277, 1120-1127.
22. Toriello, H.V., Radecki, L.L., Sharda, J., Looyenga, D. and Mann, R. (1986) Frontonasal 'dysplasia,' cerebral anomalies, and polydactyly, report of a new syndrome and discussion from a developmental field perspective. Am. J. Med. Genet. Suppl., 2, 89-96.
23. Pai, G.S., Levkoff, A.H. and Leithiser, R.E. Jr (1987) Median cleft of the upper lip associated with lipomas of the central nervous system and cutaneous polyps. Am. J. Med. Genet., 26, 921-924.
24. Lees, M.M., Hodgkins, P., Reardon, W., Taylor, D., Stanhope, R., Jones, B., Hayward, R., Hockley, A.D., Baraitser, M. and Winter, R.M. (1998) Frontonasal dysplasia with optic disc anomalies and other midline craniofacial defects, a report of six cases. Clin. Dysmorphol., 7, 157-162.
25. Masuno, M., Imaizumi, K., Aida, N., Nishimura, G., Kimura, J. and Kuroki, Y. (2000) Frontonasal dysplasia, macroblepharon, eyelid colobomas, ear anomalies, macrostomia, mental retardation, and CNS structural anomalies, another observation. Clin. Dysmorph., 9 59-60.
26. Tange, I. (1997) A peculiar malformation of the upper lip, Report of six cases. Cleft Palate Craniofac. J., 34, 73-78.
27. Mindikoglu, A.N., Partington, M.W. and Cohen, M.M. Jr (1991) Noses nobody knows for real-rhiny and craniorhiny. Am. J. Med. Genet., 40, 250-251.
28. Lees, M.M., Kangesu, L., Hall, P. and Hennekam, R.C. (2007) Two siblings with an unusual nasal malformation, Further instances of craniorhiny? Am. J. Med. Genet. A., 143A, 3290-3294.
29. Hing, A.V., Syed, N. and Cunningham, M.L. (2004) Familial acromelic frontonasal dysostosis, autosomal dominant inheritance with reduced penetrance. Am. J. Med. Genet. A., 128A, 374-382.
30. Valente, M., Valente, K.D., Sugayama, S.S. and Kim, C.A. (2004) Malformation of cortical and vascular development in one family with parietal foramina determined by an ALX4 homeobox gene mutation. Am. J. Neuroradiol., 25, 1836-1839.
31. Meijlink, F., Beverdam, A., Brouwer, A., Oosterveen, T.C. and Berge, D.T. (1999) Vertebrate aristaless-related genes. Int. J. Dev. Biol. 43, 651-663.
32. Gehring, W.J., Qian, Y.Q., Billeter, M., Furukubo-Tokunaga, K., Schier, A.F., Resendez-Perez, D., Affolter, M., Otting, G. and Wüthrich, K. (1994) Homeodomain-DNA recognition. Cell, 78, 211-223.
33. Tucker, S.C. and Wisdom, R. (1999) Site-specific heterodimerization by paired class homeodomain proteins mediates selective transcriptional responses. J. Biol. Chem., 274, 32325-32332.
34. Wilson, D., Sheng, G., Lecuit, T., Dostatni, N. and Desplan, C. (1993) Cooperative dimerization of paired class homeodomains on DNA. Genes Dev., 7, 2120-2134.
35. Chi, Y.I. (2005) Homeodomain revisited. A lesson from disease-causing mutations. Hum. Genet., 116, 433-444.
36. Dreyer, S.D., Morello, R., German, M.S., Zabel, B., Winterpacht, A., Lunstrum, G.P., Horton, W.A., Oberg, K.C. and Lee, B. (2000) LMX1B transactivation and expression in nail-patella syndrome. LMX1B transactivation and expression in nail-patella syndrome. Hum. Mol. Genet., 9, 1067-1074.
37. Forsthoefel, P.F., Fritts, M.L. and Hatzenbeler, L.J. (1966) The origin and development of alopecia in mice homozygous for Strong's luxoid gene. J. Morph., 118, 565-580.
38. Takahashi, M., Tamura, K., Büscher, D., Masuya, H., Yonei-Tamura, S., Matsumoto, K., Naitoh-Matsuo, M., Takeuchi, J., Ogura, K., Shiroishi, T. et al. (1998) The role of Alx-4 in the establishment of anteroposterior polarity during vertebrate limb development. Development, 125, 4417-4425.
39. Beverdam, A., Brouwer, A., Reijnen, M., Korving, J. and Meijlink, F. (2001) Severe nasal clefting and abnormal embryonic apoptosis in Alx3/ Alx4 double mutant mice. Development, 128, 3975-3986.
40. Ettensohn, C.A., Illies, M.R., Oliveri, P. and De Jong, D.L. (2003) Alx1, a member of the Cart1/Alx3/Alx4 subfamily of Paired-class homeodomain proteins, is an essential component of the gene network controlling skeletogenic fate specification in the sea urchin embryo. Development, 130, 2917-2928.
41. Twigg, S.R.F., Versnel, S.L., Nürnberg, G., Lees, M.M., Bhat, M., Hammond, P., Hennekam, R.C.M., Hoogeboom, A.J.M., Hurst, J.A., Johnson, D. et al. (2009) Frontorhiny, a distinctive presentation of frontonasal dysplasia caused by recessive mutations in the ALX3 homeobox gene. Am. J. Hum. Genet., 84, 698-705.
42. Niessen, C.M. (2007) Tight junctions/adherens junctions, basic structure and function. J. Invest. Dermatol., 127, 2525-2532.
43. Young, P., Boussadia, O., Halfter, H., Grose, R., Berger, P., Leone, D.P., Robenek, H., Charnay, P., Kemler, R. and Suter, U. (2003) E-cadherin controls adherens junctions in the epidermis and the renewal of hair follicles. EMBO J., 22, 5723-5733.
44. Tinkle, C.L., Lechler, T., Pasolli, H.A. and Fuchs, E. (2004) Conditional targeting of E-cadherin in skin, insights into hyperproliferative and degenerative responses. Proc. Natl Acad. Sci. USA, 101, 552-557.