Disruption of the murine Ap2β1 gene causes nonsyndromic cleft palate

Cleft Palate-Craniofacial Journal

Volumn 47, Issue 6, 2010, Pages 566-573

  Li, Wei ^a,b   Puertollano, Rosa ^c,d   Bonifacino, Juan S ^c   Overbeek, Paul A ^e   Everett, Eric T ^a,f  

^a INDIANA UNIVERSITY SCHOOL OF DENTISTRY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

2 adaptin; Clathrin coated pits; Cleft palate; Mouse; Transgene insertional mutagenesis

Indexed keywords

ADAPTOR PROTEIN; BETA ACTIN; BETA1 ADAPTIN; BETA2 ADAPTIN; CLATHRIN; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AP2BETA1 GENE; ARTICLE; BIRTH DEFECT; CHROMOSOME 11; CLEFT PALATE; EMBRYO; ENDOCYTOSIS; FIBROBLAST; GENE; GENE DISRUPTION; GENE EXPRESSION; GENE INSERTION; GENE LOCATION; GENE MUTATION; GENETIC ORGANIZATION; HETEROZYGOSITY; HOMOZYGOSITY; MAMMAL; MOUSE; MUTAGENESIS; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN ASSEMBLY; TRANSGENE;

ANIMALS; CLEFT PALATE; DISEASE MODELS, ANIMAL; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MUTAGENESIS, INSERTIONAL; SYNDROME; TRANSCRIPTION FACTOR AP-2;

EID: 77956802326     PISSN: 10556656     EISSN: 15451569     Source Type: Journal    
DOI: 10.1597/09-145     Document Type: Article

References (56)

1. Ahle S, Mann A, Eichelsbacher U, Ungewickell E. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J. 1988;7:919-929.
2. Anders RA, Arline SL, Dore JJ, Leof EB. Distinct endocytic responses of heteromeric and homomeric transforming growth factor beta receptors. Mol Biol Cell. 1997;8:2133-2143.
3. Anders RA, Dore JJ Jr, Arline SL, Garamszegi N, Leof EB. Differential requirement for type I and type II transforming growth factor-beta receptor kinase activity in ligand-mediated receptor endocytosis. J Biol Chem. 1998;273:23118-23125. (Pubitemid 28417494)
4. Bishop CE, Whitworth DJ, Qin Y, Agoulnik AI, Agoulnik IU, Harrison WR, Behringer RR, Overbeek PA. A transgenic insertion upstream of sox9 is associated with dominant XX sex reversal in the mouse. Nat Genet. 2000;26:490-494.
5. Boehm M, Bonifacino JS. Adaptins: the final recount. Mol Biol Cell. 2001;12:2907-2920.
6. Boehm M, Bonifacino JS. Genetic analyses of adaptin function from yeast to mammals. Gene. 2002;286:175-186. (Pubitemid 34273874)
7. Boll W, Ohno H, Songyang Z, Rapoport I, Cantley LC, Bonifacino JS, Kirchhausen T. Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO J. 1996;15:5789-5795. (Pubitemid 26375500)
8. Camidge DR, Pearse BM. Cloning of Drosophila beta-adaptin and its localization on expression in mammalian cells. J Cell Sci. 1994;107(pt 3):709-718.
9. Chaudhuri R, Lindwasser OW, Smith WJ, Hurley JH, Bonifacino JS. Downregulation of CD4 by human immunodeficiency virus type 1 Nef is dependent on clathrin and involves direct interaction of Nef with the AP2 clathrin adaptor. J Virol. 2007;81:3877-3890. (Pubitemid 46586884)
10. Chong SS, Cheah FSH, Jabs EW. Genes implicated in lip and palate development. In: Wyszynski DF, ed. Cleft Lip and Palate From Origin to Treatment. New York: Oxford University Press; 2002:25-39.
11. Cui XM, Chai Y, Chen J, Yamamoto T, Ito Y, Bringas P, Shuler CF. TGF-beta3-dependent SMAD2 phosphorylation and inhibition of MEE proliferation during palatal fusion. Dev Dyn. 2003;227:387-394. (Pubitemid 36828759)
12. Cui XM, Shiomi N, Chen J, Saito T, Yamamoto T, Ito Y, Bringas P, Chai Y, Shuler CF. Overexpression of Smad2 in Tgf-beta3-null mutant mice rescues cleft palate. Dev Biol. 2005;278:193-202.
13. Cui XM, Shuler CF. The TGF-beta type III receptor is localized to the medial edge epithelium during palatal fusion. Int J Dev Biol. 2000;44:397-402.
14. Cunningham D, Xiao Q, Chatterjee A, Sulik K, Juriloff D, Elder F, Harrison W, Schuster G, Overbeek PA, Herman GE. exma: an X-linked insertional mutation that disrupts forebrain and eye development. Mamm Genome. 2002;13:179-185.
15. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol. 2003;5:410-421. (Pubitemid 36592263)
16. Doray B, Lee I, Knisely J, Bu G, Kornfeld S. The gamma/sigma1 and alpha/sigma2 hemicomplexes of clathrin adaptors AP-1 and AP-2 harbor the dileucine recognition site. Mol Biol Cell. 2007;18:1887-1896.
17. Ehrlich M, Shmuely A, Henis YI. A single internalization signal from the di-leucine family is critical for constitutive endocytosis of the type II TGF-beta receptor. J Cell Sci. 2001;114:1777-1786. (Pubitemid 32454675)
18. Feng XH, Derynck R. Specificity and versatility in TGF-beta signaling through Smads. Annu Rev Cell Dev Biol. 2005;21:659-693. (Pubitemid 41740650)
19. Ferguson MW. Palate development. Development. 1988;103(suppl):41-60.
20. Guilbaud C, Peyrard M, Fransson I, Clifton SW, Roe BA, Carter NP, Dumanski JP. Characterization of the mouse beta-prime adaptin gene; cDNA sequence, genomic structure, and chromosomal localization. Mamm Genome. 1997;8:651-656.
21. Hagiwara N, Katarova Z, Siracusa LD, Brilliant MH. Nonneuronal expression of the GABA(A) beta3 subunit gene is required for normal palate development in mice. Dev Biol. 2003;254:93-101. (Pubitemid 36259874)
22. Hayes S, Chawla A, Corvera S. TGF-beta receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2. J Cell Biol. 2002;158:1239-1249.
23. Herring D, Huang R, Singh M, Robinson LC, Dillon GH, Leidenheimer NJ. Constitutive GABAA receptor endocytosis is dynamin-mediated and dependent on a dileucine AP2 adaptin-binding motif within the beta 2 subunit of the receptor. J Biol Chem. 2003;278:24046-24052. (Pubitemid 36830237)
24. Homanics GE, DeLorey TM, Firestone LL, Quinlan JJ, Handforth A, Harrison NL, Krasowski MD, Rick CE, Korpi ER, Makela R, et al. Mice devoid of gamma-aminobutyrate type A receptor beta3 subunit have epilepsy, cleft palate, and hypersensitive behavior. Proc Natl Acad Sci U S A. 1997;94:4143-4148.
25. Itoh F, Divecha N, Brocks L, Oomen L, Janssen H, Calafat J, Itoh S, Dijke Pt P. The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-beta/Smad signalling. Genes Cells. 2002;7:321-331. (Pubitemid 34257665)
26. Keyel PA, Thieman JR, Roth R, Erkan E, Everett ET, Watkins SC, Heuser JE, Traub LM. The AP-2 adaptor beta2 appendage scaffolds alternate cargo endocytosis. Mol Biol Cell. 2008;19:5309-5326.
27. Kirchhausen T. Clathrin adaptors really adapt. Cell. 2002;109:413-416.
28. Kirchhausen T, Nathanson KL, Matsui W, Vaisberg A, Chow EP, Burne C, Keen JH, Davis AE. Structural and functional division into two domains of the large (100- to 115-kDa) chains of the clathrin-associated protein complex AP-2. Proc Natl Acad Sci U S A. 1989;86:2612-2616. (Pubitemid 19112597)
29. Kittler JT, Chen G, Honing S, Bogdanov Y, McAinsh K, Arancibia- Carcamo IL, Jovanovic JN, Pangalos MN, Haucke V, Yan Z, et al. Phospho-dependent binding of the clathrin AP2 adaptor complex to GABAA receptors regulates the efficacy of inhibitory synaptic transmission. Proc Natl Acad Sci U S A. 2005;102:14871-14876.
30. Kittler JT, Delmas P, Jovanovic JN, Brown DA, Smart TG, Moss SJ. Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J Neurosci. 2000;20:7972-7977.
31. Lidral AC, Moreno LM, Bullard SA. Genetic factors and orofacial clefting. Semin Orthod. 2008;14:103-114.
32. Marazita ML, Lidral AC, Murray JC, Field LL, Maher BS, Goldstein McHenry T, Cooper ME, Govil M, Daack-Hirsch S, Riley B, et al. Genome scan, fine-mapping, and candidate gene analysis of nonsyndromic cleft lip with or without cleft palate reveals phenotypespecific differences in linkage and association results. Hum Hered. 2009;68:151-170.
33. Meisler MH. Insertional mutation of "classical" and novel genes in transgenic mice. Trends Genet. 1992;8:341-344.
34. Meyer C, Zizioli D, Lausmann S, Eskelinen EL, Hamann J, Saftig P, von Figura K, Schu P. mu1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 2000;19:2193-2203. (Pubitemid 30259000)
35. Mitchell RS, Chaudhuri R, Lindwasser OW, Tanaka KA, Lau D, Murillo R, Bonifacino JS, Guatelli JC. Competition model for upregulation of the major histocompatibility complex class II-associated invariant chain by human immunodeficiency virus type 1 Nef. J Virol. 2008;82:7758-7767.
36. Mitsunari T, Nakatsu F, Shioda N, Love PE, Grinberg A, Bonifacino JS, Ohno H. Clathrin adaptor AP-2 is essential for early embryonal development. Mol Cell Biol. 2005;25:9318-9323. (Pubitemid 41507833)
37. Nakajima A, Ito Y, Asano M, Maeno M, Iwata K, Mitsui N, Shimizu N, Cui XM, Shuler CF. Functional role of transforming growth factor-beta type III receptor during palatal fusion. Dev Dyn. 2007;236: 791-801. (Pubitemid 46449190)
38. Ohno H, Fournier MC, Poy G, Bonifacino JS. Structural determinants of interaction of tyrosine-based sorting signals with the adaptor medium chains. J Biol Chem. 1996;271:29009-29015. (Pubitemid 26382605)
39. Ohno H, Stewart J, Fournier MC, Bosshart H, Rhee I, Miyatake S, Saito T, Gallusser A, Kirchhausen T, Bonifacino JS. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science. 1995;269:1872-1875.
40. Overbeek PA, Aguilar-Cordova E, Hanten G, Schaffner DL, Patel P, Lebovitz RM, Lieberman MW. Coinjection strategy for visual identification of transgenic mice. Transgenic Res. 1991;1:31-37.
41. Overbeek PA, Gorlov IP, Sutherland RW, Houston JB, Harrison WR, Boettger-Tong HL, Bishop CE, Agoulnik AI. A transgenic insertion causing cryptorchidism in mice. Genesis. 2001;30:26-35.
42. Page LJ, Robinson MS. Targeting signals and subunit interactions in coated vesicle adaptor complexes. J Cell Biol. 1995;131:619-630.
43. Ponnambalam S, Robinson MS, Jackson AP, Peiperl L, Parham P. Conservation and diversity in families of coated vesicle adaptins. J Biol Chem. 1990;265:4814-4820.
44. Proetzel G, Pawlowski SA, Wiles MV, Yin M, Boivin GP, Howles PN, Ding J, Ferguson MW, Doetschman T. Transforming growth factorbeta 3 is required for secondary palate fusion. Nat Genet. 1995;11: 409-414. (Pubitemid 3007193)
45. Robinson MS. Cloning of cDNAs encoding two related 100-kD coated vesicle proteins (alpha-adaptins). J Cell Biol. 1989;108:833-842.
46. Robinson MS. Adaptable adaptors for coated vesicles. Trends Cell Biol. 2004;14:167-174.
47. Runyan CE, Schnaper HW, Poncelet AC. The role of internalization in transforming growth factor beta1-induced Smad2 association with Smad anchor for receptor activation (SARA) and Smad2- dependent signaling in human mesangial cells. J Biol Chem. 2005; 280:8300-8308.
48. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T. TGF beta2 knockout mice have multiple developmental defects that are non-overlapping with other TGF beta knockout phenotypes. Development. 1997;124:2659-2670. (Pubitemid 27341765)
49. Schutte BC, Murray JC. The many faces and factors of orofacial clefts. Hum Mol Genet. 1999;8:1853-1859.
50. Shawlot W, Siciliano MJ, Stallings RL, Overbeek PA. Insertional inactivation of the downless gene in a family of transgenic mice. Mol Biol Med. 1989;6:299-307. (Pubitemid 20108306)
51. Shi M, Mostowska A, Jugessur A, Johnson MK, Mansilla MA, Christensen K, Lie RT, Wilcox AJ, Murray JC. Identification of microdeletions in candidate genes for cleft lip and/or palate. Birth Defects Res A Clin Mol Teratol. 2009;85:42-51.
52. Traub LM. Clathrin-associated adaptor proteins - putting it all together. Trends Cell Biol. 1997;7:43-46.
53. Traub LM. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J Cell Biol. 2003;163:203-208.
54. Tudela C, Formoso MA, Martinez T, Perez R, Aparicio M, Maestro C, Del Rio A, Martinez E, Ferguson M, Martinez-Alvarez C. TGF-beta3 is required for the adhesion and intercalation of medial edge epithelial cells during palate fusion. Int J Dev Biol. 2002;46:333-336. (Pubitemid 34619722)
55. Yao D, Ehrlich M, Henis YI, Leof EB. Transforming growth factor-beta receptors interact with AP2 by direct binding to beta2 subunit. Mol Biol Cell. 2002;13:4001-4012. (Pubitemid 35398566)
56. Yokoyama T, Silversides DW, Waymire KG, Kwon BS, Takeuchi T, Overbeek PA. Conserved cysteine to serine mutation in tyrosinase is responsible for the classical albino mutation in laboratory mice. Nucleic Acids Res. 1990;18:7293-7298. (Pubitemid 120006030)