Understanding cadherin EGF LAG seven-pass G-type receptors

Journal of Neurochemistry

Volumn 131, Issue 6, 2014, Pages 699-711

  Wang, Xiao Jing ^a,b   Zhang, Dao Lai ^a,b,c   Xu, Zhi Gang ^d   Ma, Ming Liang ^a,b   Wang, Wen Bo ^a,b   Li, Lin Lin ^a,b   Han, Xiao Lin ^a,b   Huo, Yuqing ^e   Yu, Xiao ^a,b   Sun, Jin Peng ^a,b  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b Shandong Provincial School Key Laboratory for Protein Science of Chronic Degenerative Diseases   (China)

^c BINZHOU MEDICAL UNIVERSITY   (China)

^d SHANDONG UNIVERSITY   (China)

^e MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

adhesion; CELSR; development; G protein coupled receptor; planar cell polarity

Indexed keywords

CADHERIN EPIDERMAL GROWTH FACTOR LAMININ G SEVEN PASS G TYPE RECEPTOR; CADHERIN EPIDERMAL GROWTH FACTOR LAMININ G SEVEN PASS G TYPE RECEPTOR 1; CADHERIN EPIDERMAL GROWTH FACTOR LAMININ G SEVEN PASS G TYPE RECEPTOR 2; CADHERIN EPIDERMAL GROWTH FACTOR LAMININ G SEVEN PASS G TYPE RECEPTOR 3; COMPLEMENTARY DNA; G PROTEIN COUPLED RECEPTOR; MESSENGER RNA; UNCLASSIFIED DRUG; CADHERIN; LAMININ;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; CALCIUM CELL LEVEL; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL MIGRATION; CELL POLARITY; CELL PROLIFERATION; CELSR1 GENE; CELSR2 GENE; CELSR3 GENE; CONFORMATIONAL TRANSITION; CYTOLOGY; ECTO DOMAIN; FACIAL BRANCHIOMOTOR NEURON; GAIN DOMAIN; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE LOCATION; GENE MUTATION; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC CONSERVATION; GLUCOSE HOMEOSTASIS; HUMAN; INTRALUMINAL VALVE FORMATION; KNOCKOUT MOUSE; LYMPH VESSEL; MOLECULAR CLONING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR PATHOLOGY; NERVE CELL; NEURAL STEM CELL; NEURAL TUBE DEFECT; NONHUMAN; ORGANOGENESIS; PANCREAS ISLET BETA CELL; PLANAR CELL POLARITY; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; TISSUE DISTRIBUTION; ANIMAL; METABOLISM; PHYSIOLOGY;

ANIMALS; CADHERINS; CELL DIFFERENTIATION; CELL POLARITY; HUMANS; LAMININ; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84915798937     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12955     Document Type: Review

References (110)

1. Adams J. N., Raffield L. M., Freedman B. I., Langefeld C. D., Ng M. C., Carr J. J., Cox A. J., and, Bowden D. W., (2014) Analysis of common and coding variants with cardiovascular disease in the Diabetes Heart Study. Cardiovasc. Diabetol. 13, 77.
2. Allache R., De Marco P., Merello E., Capra V., and, Kibar Z., (2012) Role of the planar cell polarity gene CELSR1 in neural tube defects and caudal agenesis. Birth Defects Res. Part A Clin. Mol. Teratol. 94, 176-181.
3. Ammerpohl O., Pratschke J., Schafmayer C., et al,. (2012) Distinct DNA methylation patterns in cirrhotic liver and hepatocellular carcinoma. Int. J. Cancer 130, 1319-1328.
4. Arac D., Boucard A. A., Bolliger M. F., Nguyen J., Soltis S. M., Sudhof T. C., and, Brunger A. T., (2012) A novel evolutionarily conserved domain of cell-adhesion GPCRs mediates autoproteolysis. EMBO J. 31, 1364-1378.
5. Arvind P., Nair J., Jambunathan S., Kakkar V. V., and, Shanker J,. (2014) CELSR2-PSRC1-SORT1 gene expression and association with coronary artery disease and plasma lipid levels in an Asian Indian cohort. J. Cardiol. doi: 10.1016/j.jjcc.2014.02.012.[Epub ahead of print]
6. Bae B. I., Tietjen I., Atabay K. D., et al,. (2014) Evolutionarily dynamic alternative splicing of GPR56 regulates regional cerebral cortical patterning. Science 343, 764-768.
7. Beall S. A., Boekelheide K., and, Johnson K. J., (2005) Hybrid GPCR/cadherin (Celsr) proteins in rat testis are expressed with cell type specificity and exhibit differential Sertoli cell-germ cell adhesion activity. J. Androl. 26, 529-538.
8. Bjarnadottir T. K., Fredriksson R., and, Schioth H. B., (2007) The adhesion GPCRs: a unique family of G protein-coupled receptors with important roles in both central and peripheral tissues. Cell. Mol. Life Sci. 64, 2104-2119.
9. Boutin C., Goffinet A. M., and, Tissir F., (2012) Celsr1-3 cadherins in PCP and brain development. Curr. Top. Dev. Biol. 101, 161-183.
10. Boutin C., Labedan P., Dimidschstein J., et al,. (2014) A dual role for planar cell polarity genes in ciliated cells. Proc. Natl Acad. Sci. USA 111, E3129-E3138.
11. Braun T. R., Been L. F., Singhal A., et al,. (2012) A replication study of GWAS-derived lipid genes in Asian Indians: the chromosomal region 11q23.3 harbors loci contributing to triglycerides. PLoS ONE 7, e37056.
12. Caddy J., Wilanowski T., Darido C., et al,. (2010) Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev. Cell 19, 138-147.
13. Chae J., Kim M. J., Goo J. H., Collier S., Gubb D., Charlton J., Adler P. N., and, Park W. J., (1999) The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 126, 5421-5429.
14. Chai G., Zhou L., Manto M., Helmbacher F., Clotman F., Goffinet A. M., and, Tissir F., (2014) Celsr3 is required in motor neurons to steer their axons in the hindlimb. Nat. Neurosci. 17, 1171-1179.
15. Cherezov V., Rosenbaum D. M., Hanson M. A., et al,. (2007) High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318, 1258-1265.
16. Chow K. B., Sun J., Chu K. M., Tai Cheung W., Cheng C. H., and, Wise H., (2012) The truncated ghrelin receptor polypeptide (GHS-R1b) is localized in the endoplasmic reticulum where it forms heterodimers with ghrelin receptors (GHS-R1a) to attenuate their cell surface expression. Mol. Cell. Endocrinol. 348, 247-254.
17. Cortijo C., Gouzi M., Tissir F., and, Grapin-Botton A., (2012) Planar cell polarity controls pancreatic beta cell differentiation and glucose homeostasis. Cell Rep. 2, 1593-1606.
18. Curtin J. A., Quint E., Tsipouri V., et al,. (2003) Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr. Biol. 13, 1129-1133.
19. Davies B., Baumann C., Kirchhoff C., Ivell R., Nubbemeyer R., Habenicht U. F., Theuring F., and, Gottwald U., (2004) Targeted deletion of the epididymal receptor HE6 results in fluid dysregulation and male infertility. Mol. Cell. Biol. 24, 8642-8648.
20. Del Giudice I., Messina M., Chiaretti S., et al,. (2012) Behind the scenes of non-nodal MCL: downmodulation of genes involved in actin cytoskeleton organization, cell projection, cell adhesion, tumour invasion, TP53 pathway and mutated status of immunoglobulin heavy chain genes. Br. J. Haematol. 156, 601-611.
21. Devenport D., and, Fuchs E., (2008) Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat. Cell Biol. 10, 1257-1268.
22. Doudney K., and, Stanier P., (2005) Epithelial cell polarity genes are required for neural tube closure. Am. J. Med. Genet. C Semin. Med. Genet. 135C, 42-47.
23. Feng J., Han Q., and, Zhou L., (2012a) Planar cell polarity genes, Celsr1-3, in neural development. Neurosci. Bull. 28, 309-315.
24. Feng J., Xu Y., Wang M., Ruan Y., So K. F., Tissir F., Goffinet A., and, Zhou L., (2012b) A role for atypical cadherin Celsr3 in hippocampal maturation and connectivity. J. Neurosci. 32, 13729-13743.
25. Fenstermaker A. G., Prasad A. A., Bechara A., Adolfs Y., Tissir F., Goffinet A., Zou Y., and, Pasterkamp R. J., (2010) Wnt/planar cell polarity signaling controls the anterior-posterior organization of monoaminergic axons in the brainstem. J. Neurosci. 30, 16053-16064.
26. Formstone C. J., (2010) 7TM-Cadherins: developmental roles and future challenges. Adv. Exp. Med. Biol. 706, 14-36.
27. Formstone C. J., and, Little P. F., (2001) The flamingo-related mouse Celsr family (Celsr1-3) genes exhibit distinct patterns of expression during embryonic development. Mech. Dev. 109, 91-94.
28. Formstone C. J., and, Mason I., (2005) Expression of the Celsr/flamingo homologue, c-fmi1, in the early avian embryo indicates a conserved role in neural tube closure and additional roles in asymmetry and somitogenesis. Dev. Dyn. 232, 408-413.
29. Formstone C. J., Barclay J., Rees M., and, Little P. F., (2000) Chromosomal localization of Celsr2 and Celsr3 in the mouse; Celsr3 is a candidate for the tippy (tip) lethal mutant on chromosome 9. Mamm. Genome 11, 392-394.
30. Fredriksson R., Lagerstrom M. C., Lundin L. G., and, Schioth H. B., (2003) The G protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol. 63, 1256-1272.
31. Gao F. B., Kohwi M., Brenman J. E., Jan L. Y., and, Jan Y. N., (2000) Control of dendritic field formation in Drosophila: the roles of flamingo and competition between homologous neurons. Neuron 28, 91-101.
32. Georgieva L., Nikolov I., Poriazova N., Jones G., Toncheva D., Kirov G., and, Owen M. J., (2003) Genetic variation in the seven-pass transmembrane cadherin CELSR1: lack of association with schizophrenia. Psychiatr. Genet. 13, 103-106.
33. Gross J., Grimm O., Ortega G., Teuber I., Lesch K. P., and, Meyer J., (2001) Mutational analysis of the neuronal cadherin gene CELSR1 and exclusion as a candidate for catatonic schizophrenia in a large family. Psychiatr. Genet. 11, 197-200.
34. Hadjantonakis A. K., Sheward W. J., Harmar A. J., de Galan L., Hoovers J. M., and, Little P. F., (1997) Celsr1, a neural-specific gene encoding an unusual seven-pass transmembrane receptor, maps to mouse chromosome 15 and human chromosome 22qter. Genomics 45, 97-104.
35. Hadjantonakis A. K., Formstone C. J., and, Little P. F., (1998) mCelsr1 is an evolutionarily conserved seven-pass transmembrane receptor and is expressed during mouse embryonic development. Mech. Dev. 78, 91-95.
36. Hanson M. A., and, Stevens R. C., (2009) Discovery of new GPCR biology: one receptor structure at a time. Structure 17, 8-14.
37. Hohenester E., Tisi D., Talts J. F., and, Timpl R., (1999) The crystal structure of a laminin G-like module reveals the molecular basis of alpha-dystroglycan binding to laminins, perlecan, and agrin. Mol. Cell 4, 783-792.
38. Hsiao C. C., Chen H. Y., Chang G. W., and, Lin H. H., (2011) GPS autoproteolysis is required for CD97 to up-regulate the expression of N-cadherin that promotes homotypic cell-cell aggregation. FEBS Lett. 585, 313-318.
39. Hu Q. X., Dong J. H., Du H. B., et al,. (2014) Constitutive Galphai Coupling Activity of VLGR1 and its Regulation by PDZD7. J. Biol. Chem. 289, 24215-24225.
40. Huber A. H., Stewart D. B., Laurents D. V., Nelson W. J., and, Weis W. I., (2001) The cadherin cytoplasmic domain is unstructured in the absence of beta-catenin. A possible mechanism for regulating cadherin turnover. J. Biol. Chem. 276, 12301-12309.
41. Jeemon P., Pettigrew K., Sainsbury C., Prabhakaran D., and, Padmanabhan S., (2011) Implications of discoveries from genome-wide association studies in current cardiovascular practice. World J. Cardiol. 3, 230-247.
42. Jin Z., Tietjen I., Bu L., Liu-Yesucevitz L., Gaur S. K., Walsh C. A., and, Piao X., (2007) Disease-associated mutations affect GPR56 protein trafficking and cell surface expression. Hum. Mol. Genet. 16, 1972-1985.
43. Johnson K. J., Patel S. R., and, Boekelheide K., (2000) Multiple cadherin superfamily members with unique expression profiles are produced in rat testis. Endocrinology 141, 675-683.
44. Juriloff D. M., and, Harris M. J., (2012) A consideration of the evidence that genetic defects in planar cell polarity contribute to the etiology of human neural tube defects. Birth Defects Res. Part A Clin. Mol. Teratol. 94, 824-840.
45. Kahsai A. W., Xiao K., Rajagopal S., Ahn S., Shukla A. K., Sun J., Oas T. G., and, Lefkowitz R. J., (2011) Multiple ligand-specific conformations of the beta2-adrenergic receptor. Nat. Chem. Biol. 7, 692-700.
46. Kathiresan S., Melander O., Guiducci C., et al,. (2008) Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nat. Genet. 40, 189-197.
47. Kaucka M., Plevova K., Pavlova S., et al,. (2013) The planar cell polarity pathway drives pathogenesis of chronic lymphocytic leukemia by the regulation of B-lymphocyte migration. Cancer Res. 73, 1491-1501.
48. Langenhan T., Aust G., and, Hamann J., (2013) Sticky signaling-adhesion class G protein-coupled receptors take the stage. Sci. Signal. 6, re3.
49. Lefkowitz R. J., Sun J. P., and, Shukla A. K., (2008) A crystal clear view of the beta2-adrenergic receptor. Nat. Biotechnol. 26, 189-191.
50. Lei Y., Zhu H., Yang W., Ross M. E., Shaw G. M., and, Finnell R. H., (2014) Identification of novel CELSR1 mutations in spina bifida. PLoS ONE 9, e92207.
51. Lewis A., Wilson N., Stearns G., Johnson N., Nelson R., and, Brockerhoff S. E., (2011) Celsr3 is required for normal development of GABA circuits in the inner retina. PLoS Genet. 7, e1002239.
52. Li S., Jin Z., Koirala S., Bu L., Xu L., Hynes R. O., Walsh C. A., Corfas G., and, Piao X., (2008) GPR56 regulates pial basement membrane integrity and cortical lamination. J. Neurosci. 28, 5817-5826.
53. Lin H. H., Chang G. W., Davies J. Q., Stacey M., Harris J., and, Gordon S., (2004) Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif. J. Biol. Chem. 279, 31823-31832.
54. McGee J., Goodyear R. J., McMillan D. R., et al,. (2006) The very large G protein-coupled receptor VLGR1: a component of the ankle link complex required for the normal development of auditory hair bundles. J. Neurosci. 26, 6543-6553.
55. McVey D., Samani N., and, Webb T., (2014) 214 Generation of Isogenic Cell Lines to Study a Single Disease Associated Variant at the 1P13 Cad Risk Locus. Heart 100 (Suppl 3), A117.
56. Meyer R. D., Srinivasan S., Singh A. J., Mahoney J. E., Gharahassanlou K. R., and, Rahimi N., (2011) PEST motif serine and tyrosine phosphorylation controls vascular endothelial growth factor receptor 2 stability and downregulation. Mol. Cell. Biol. 31, 2010-2025.
57. Montcouquiol M., Jones J. M., and, Sans N., (2008) Detection of planar polarity proteins in mammalian cochlea. Methods Mol. Biol. 468, 207-219.
58. Nakayama M., Nakajima D., Nagase T., Nomura N., Seki N., and, Ohara O., (1998) Identification of high-molecular-weight proteins with multiple EGF-like motifs by motif-trap screening. Genomics 51, 27-34.
59. Nakayama K., Bayasgalan T., Yamanaka K., et al,. (2009) Large scale replication analysis of loci associated with lipid concentrations in a Japanese population. J. Med. Genet. 46, 370-374.
60. Nishimura T., Honda H., and, Takeichi M., (2012) Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 149, 1084-1097.
61. Overduin M., Harvey T. S., Bagby S., Tong K. I., Yau P., Takeichi M., and, Ikura M., (1995) Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science 267, 386-389.
62. Overduin M., Tong K. I., Kay C. M., and, Ikura M., (1996) 1H, 15N and 13C resonance assignments and monomeric structure of the amino-terminal extracellular domain of epithelial cadherin. J. Biomol. NMR 7, 173-189.
63. Paavola K. J., and, Hall R. A., (2012) Adhesion G protein-coupled receptors: signaling, pharmacology, and mechanisms of activation. Mol. Pharmacol. 82, 777-783.
64. Paavola K. J., Stephenson J. R., Ritter S. L., Alter S. P., and, Hall R. A., (2011) The N-terminus of the adhesion G protein-coupled receptor GPR56 controls receptor signaling activity. J. Biol. Chem. 286, 28914-28921.
65. Piao X., Hill R. S., Bodell A., et al,. (2004) G protein-coupled receptor-dependent development of human frontal cortex. Science 303, 2033-2036.
66. Qi L., Ma J., Qi Q., Hartiala J., Allayee H., and, Campos H., (2011) Genetic risk score and risk of myocardial infarction in Hispanics. Circulation 123, 374-380.
67. Qu Y., Glasco D. M., Zhou L., et al,. (2010) Atypical cadherins Celsr1-3 differentially regulate migration of facial branchiomotor neurons in mice. J. Neurosci. 30, 9392-9401.
68. Qu Y., Huang Y., Feng J., Alvarez-Bolado G., Grove E. A., Yang Y., Tissir F., Zhou L., and, Goffinet A. M., (2014) Genetic evidence that Celsr3 and Celsr2, together with Fzd3, regulate forebrain wiring in a Vangl-independent manner. Proc. Natl Acad. Sci. USA 111, E2996-E3004.
69. Rasmussen S. G., Choi H. J., Rosenbaum D. M., et al,. (2007) Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 450, 383-387.
70. Ravni A., Qu Y., Goffinet A. M., and, Tissir F., (2009) Planar cell polarity cadherin Celsr1 regulates skin hair patterning in the mouse. J. Invest. Dermatol. 129, 2507-2509.
71. Robinson A., Escuin S., Doudney K., Vekemans M., Stevenson R. E., Greene N. D., Copp A. J., and, Stanier P., (2012) Mutations in the planar cell polarity genes CELSR1 and SCRIB are associated with the severe neural tube defect craniorachischisis. Hum. Mutat. 33, 440-447.
72. Rosenbaum D. M., Cherezov V., Hanson M. A., et al,. (2007) GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function. Science 318, 1266-1273.
73. Rosenbaum D. M., Rasmussen S. G., and, Kobilka B. K., (2009) The structure and function of G-protein-coupled receptors. Nature 459, 356-363.
74. Runge S., Thogersen H., Madsen K., Lau J., and, Rudolph R., (2008) Crystal structure of the ligand-bound glucagon-like peptide-1 receptor extracellular domain. J. Biol. Chem. 283, 11340-11347.
75. Saade S., Cazier J. B., Ghassibe-Sabbagh M., et al,. (2011) Large scale association analysis identifies three susceptibility loci for coronary artery disease. PLoS ONE 6, e29427.
76. Samani N. J., Erdmann J., Hall A. S., et al,. (2007) Genomewide association analysis of coronary artery disease. N. Engl. J. Med. 357, 443-453.
77. Samani N. J., Braund P. S., Erdmann J., et al,. (2008) The novel genetic variant predisposing to coronary artery disease in the region of the PSRC1 and CELSR2 genes on chromosome 1 associates with serum cholesterol. J. Mol. Med. (Berl) 86, 1233-1241.
78. Sandhu M. S., Waterworth D. M., Debenham S. L., et al,. (2008) LDL-cholesterol concentrations: a genome-wide association study. Lancet 371, 483-491.
79. Shapiro L., and, Weis W. I., (2009) Structure and biochemistry of cadherins and catenins. Cold Spring Harb. Perspect. Biol. 1, a003053.
80. Shima Y., Copeland N. G., Gilbert D. J., Jenkins N. A., Chisaka O., Takeichi M., and, Uemura T., (2002) Differential expression of the seven-pass transmembrane cadherin genes Celsr1-3 and distribution of the Celsr2 protein during mouse development. Dev. Dyn. 223, 321-332.
81. Shima Y., Kengaku M., Hirano T., Takeichi M., and, Uemura T., (2004) Regulation of dendritic maintenance and growth by a mammalian 7-pass transmembrane cadherin. Dev. Cell 7, 205-216.
82. Shima Y., Kawaguchi S. Y., Kosaka K., Nakayama M., Hoshino M., Nabeshima Y., Hirano T., and, Uemura T., (2007) Opposing roles in neurite growth control by two-seven-pass transmembrane cadherins. Nat. Neurosci. 10, 963-969.
83. Shukla A. K., Sun J. P., and, Lefkowitz R. J., (2008) Crystallizing thinking about the beta2-adrenergic receptor. Mol. Pharmacol. 73, 1333-1338.
84. Singer K., Luo R., Jeong S. J., and, Piao X., (2013) GPR56 and the developing cerebral cortex: cells, matrix, and neuronal migration. Mol. Neurobiol. 47, 186-196.
85. Singh G. P., Ganapathi M., Sandhu K. S., and, Dash D., (2006) Intrinsic unstructuredness and abundance of PEST motifs in eukaryotic proteomes. Proteins 62, 309-315.
86. Sun J. P., Li R., Ren H. Z., Xu A. T., Yu X., and, Xu Z. G., (2013) The very large G protein coupled receptor (Vlgr1) in hair cells. J. Mol. Neurosci. 50, 204-214.
87. Takeichi M., (1990) Cadherins: a molecular family important in selective cell-cell adhesion. Annu. Rev. Biochem. 59, 237-252.
88. 2+-dependent sites. Dev. Biol. 87, 340-350.
89. Talmud P. J., Drenos F., Shah S., et al,. (2009) Gene-centric association signals for lipids and apolipoproteins identified via the HumanCVD BeadChip. Am. J. Hum. Genet. 85, 628-642.
90. Tatin F., Taddei A., Weston A., Fuchs E., Devenport D., Tissir F., and, Makinen T., (2013) Planar cell polarity protein Celsr1 regulates endothelial adherens junctions and directed cell rearrangements during valve morphogenesis. Dev. Cell 26, 31-44.
91. Tissir F., and, Goffinet A. M., (2006) Expression of planar cell polarity genes during development of the mouse CNS. Eur. J. Neurosci. 23, 597-607.
92. Tissir F., Bar I., Goffinet A. M., and, Lambert De Rouvroit C., (2002a) Expression of the ankyrin repeat domain 6 gene (Ankrd6) during mouse brain development. Dev. Dyn. 224, 465-469.
93. Tissir F., De-Backer O., Goffinet A. M., and, Lambert de Rouvroit C., (2002b) Developmental expression profiles of Celsr (Flamingo) genes in the mouse. Mech. Dev. 112, 157-160.
94. Tissir F., Bar I., Jossin Y., De Backer O., and, Goffinet A. M., (2005) Protocadherin Celsr3 is crucial in axonal tract development. Nat. Neurosci. 8, 451-457.
95. Tissir F., Qu Y., Montcouquiol M., et al,. (2010) Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat. Neurosci. 13, 700-707.
96. Underwood C. R., Garibay P., Knudsen L. B., Hastrup S., Peters G. H., Rudolph R., and, Reedtz-Runge S., (2010) Crystal structure of glucagon-like peptide-1 in complex with the extracellular domain of the glucagon-like peptide-1 receptor. J. Biol. Chem. 285, 723-730.
97. Usui T., Shima Y., Shimada Y., Hirano S., Burgess R. W., Schwarz T. L., Takeichi M., and, Uemura T., (1999) Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585-595.
98. Venkatakrishnan A. J., Deupi X., Lebon G., Tate C. G., Schertler G. F., and, Babu M. M., (2013) Molecular signatures of G-protein-coupled receptors. Nature 494, 185-194.
99. Virtanen K. J., Remes V., Pajarinen J., Savolainen V., Bjorkenheim J. M., and, Paavola M., (2012) Sling compared with plate osteosynthesis for treatment of displaced midshaft clavicular fractures: a randomized clinical trial. J. Bone Joint Surg. Am. 94, 1546-1553.
100. Wada H., Tanaka H., Nakayama S., Iwasaki M., and, Okamoto H., (2006) Frizzled3a and Celsr2 function in the neuroepithelium to regulate migration of facial motor neurons in the developing zebrafish hindbrain. Development 133, 4749-4759.
101. Wang H. M., Dong J. H., Li Q., et al,. (2014) A stress response pathway in mice upregulates somatostatin level and transcription in pancreatic delta cells through Gs and beta-arrestin 1. Diabetologia 57, 1899-1910.
102. Waterworth D. M., Ricketts S. L., Song K., et al,. (2010) Genetic variants influencing circulating lipid levels and risk of coronary artery disease. Arterioscler. Thromb. Vasc. Biol. 30, 2264-2276.
103. Wu G., Huang X., Hua Y., and, Mu D., (2011) Roles of planar cell polarity pathways in the development of neural [correction of neutral] tube defects. J. Biomed. Sci. 18, 66.
104. Yates L. L., Papakrivopoulou J., Long D. A., Goggolidou P., Connolly J. O., Woolf A. S., and, Dean C. H., (2010a) The planar cell polarity gene Vangl2 is required for mammalian kidney-branching morphogenesis and glomerular maturation. Hum. Mol. Genet. 19, 4663-4676.
105. Yates L. L., Schnatwinkel C., Murdoch J. N., Bogani D., Formstone C. J., Townsend S., Greenfield A., Niswander L. A., and, Dean C. H., (2010b) The PCP genes Celsr1 and Vangl2 are required for normal lung branching morphogenesis. Hum. Mol. Genet. 19, 2251-2267.
106. Zhang R., and, Xie X., (2012) Tools for GPCR drug discovery. Acta Pharmacol. Sin. 33, 372-384.
107. Zhang Y., Sivasankar S., Nelson W. J., and, Chu S., (2009) Resolving cadherin interactions and binding cooperativity at the single-molecule level. Proc. Natl Acad. Sci. USA 106, 109-114.
108. Zhang B., Tran U., and, Wessely O., (2011) Expression of Wnt signaling components during Xenopus pronephros development. PLoS ONE 6, e26533.
109. Zhou L., Bar I., Achouri Y., et al,. (2008) Early forebrain wiring: genetic dissection using conditional Celsr3 mutant mice. Science 320, 946-949.
110. Zhou L., Qu Y., Tissir F., and, Goffinet A. M., (2009) Role of the atypical cadherin Celsr3 during development of the internal capsule. Cereb. Cortex 19 (Suppl 1), i114-i119.