Protocadherins, not prototypical: A complex tale of their interactions, expression, and functions

Frontiers in Molecular Neuroscience

Volumn , Issue MARCH 2013, 2013, Pages

  Weiner, Joshua A ^a   Jontes, James ^b  

^a UNIVERSITY OF IOWA   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Adhesion; Cadherin superfamily; Neural circuits; Pcdh; Protocadherins

Indexed keywords

CADHERIN; PROTEIN BAX; PROTEIN RET; PROTOCADHERIN; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG;

APOPTOSIS; CANCER GROWTH; CELL ADHESION; CELL AGGREGATION; CELL SURFACE; DENDRITE; ENVIRONMENTAL STRESS; GENE EXPRESSION REGULATION; HISTONE METHYLATION; HUMAN; INTERNEURON; NERVE CELL NETWORK; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SYNAPTOGENESIS;

EID: 84874907679     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2013.00004     Document Type: Review

References (91)

1. Abe, M., Ohira, M., Kaneda, A., Yagi, Y., Yamamoto, S., Kitano, Y., Takato, T., Nakagawara, A., and Ushijima, T. (2005). CpG island methylator phenotype is a strong determinant of poor prognosis in neuroblastomas. Cancer Res. 65, 828-834.
2. Arregui, C., Pathre, P., Lilien, J., and Balsamo, J. (2000). The nonreceptor tyrosine kinase fer mediates cross-talk between N-cadherin and beta1-integrins. J. Cell Biol. 149, 1263-1274.
3. Biswas, S., Emond, M.R., and Jontes, J.D. (2010). Protocadherin-19 and N-cadherin interact to control cell movements during anterior neurulation. J Cell Biol 191, 1029-1041.
4. Biswas, S., Emond, M.R., and Jontes, J.D. (2012). The clustered protocadherins Pcdhalpha and Pcdhgamma form a heteromeric complex in zebrafish. Neuroscience 219, 280-289.
5. Blank M, Triana-Baltzer GB, Richards CS and Berg, D.K. (2004). Alpha-protocadherins are presynaptic and axonal in nicotinic pathways. Mol. Cell. Neurosci. 26:530-43.
6. Cavallaro, U. and Christofori, G. (2004). Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat. Rev. Cancer, 4, 118-132.
7. Chen, J., Lu, Y., Meng, S., Han, M.H., Lin, C., and Wang, X. (2009a). alpha-and gamma-Protocadherins negatively regulate PYK2. J. Biol. Chem. 284, 2880-2890.
8. Chen, X., and Gumbiner, B.M. (2006). Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity. J. Cell Biol. 174, 301-313.
9. Chen, X., Koh, E., Yoder, M., and Gumbiner, B.M. (2009b). A protocadherin-cadherin-FLRT3 complex controls cell adhesion and morphogenesis. PloS One 4, e8411.
10. Chen, W., Alvarez, F.J., Lefebvre, J.L., Friedman, B., Nwakeze, C., Geiman, E., Smith, C., Thu, C.A., Tapia, J.C., Tasic, B., Sanes, J.R., and Maniatis, T. (2012). Functional significance of isoform diversification in the protocadherin gamma gene cluster. Neuron, 75, 402-409.
11. Chong, J.A., Tapia-Ramirez, J., Kim, S., Toledo-Aral, J.J., Zheng, Y., Boutros, M.C., Altshuller, Y.M., Frohman, M.A., Kraner, S.D., and Mandel, G. (1995). REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80, 949-957.
12. Dallosso, A.R., Hancock, A.L., Szemes, M., Moorwood, K., Chilukamarri, L., Tsai, H.H., Sarkar, A., Barasch, J., Vuononvirta, R., Jones, C., Pritchard-Jones, K., Royer-Pokora, B., Lee, S.B., Owen, C., Malik, S., Feng, Y., Frank, M., Ward, A., Brown, K.W., and Malik, K. (2009). Frequent long-range epigenetic silencing of protocadherin gene clusters on chromosome 5q31 in Wilms' tumor. PLoS Gen. 5, e1000745.
13. Dallosso, A.R., Oster, B., Greenhough, A., Thorsen, K., Curry, T.J., Owen, C., Hancock, A.L., Szemes, M., Paraskeva, C., Frank, M., Andersen, C.L., and Malik, K. (2012). Longrange epigenetic silencing of chromosome 5q31 protocadherins is involved in early and late stages of colorectal tumorigenesis through modulation of oncogenic pathways. Oncogene 31, 4409-4419.
14. Emond, M.R., Biswas, S., Blevins, C.J., and Jontes, J.D. (2011). A complex of Protocadherin-19 and N-cadherin mediates a novel mechanism of cell adhesion. J Cell Biol 195, 1115-1121.
15. Emond, M.R., and Jontes, J.D. (2008). Inhibition of protocadherin-alpha function results in neuronal death in the developing zebrafish. Dev. Biol. 321, 175-187.
16. Esumi, S., Kakazu, N., Taguchi, Y., Hirayama, T., Sasaki, A., Hirabayashi, T., Koide, T., Kitsukawa, T., Hamada, S., and Yagi, T. (2005). Monoallelic yet combinatorial expression of variable exons of the protocadherin-alpha gene cluster in single neurons. Nature genetics 37, 171-176.
17. Fernandez-Monreal, M., Kang, S., and Phillips, G.R. (2009). Gamma-protocadherin homophilic interaction and intracellular trafficking is controlled by the cytoplasmic domain in neurons. Mol. Cell. Neurosci. 40, 344-353.
18. Fuerst, P. G., Koizumi, A., Masland, R. H., and Burgess, R. W. (2008). Neurite Arborization and Mosaic Spacing in the Mouse Retina Require DSCAM. Nature 451, 470.
19. Fuerst, P. G., Bruce, F., Tian, M., Wei, W., Elstrott, J., Feller, M. B., Erskine, L., Singer, J. H. and Burgess, R. W. (2009). DSCAM and DSCAML1 Function in Self-Avoidance in Multiple Cell Types in the Developing Mouse Retina. Neuron 64, 484-497.
20. Frank, M., Ebert, M., Shan, W., Phillips, G.R., Arndt, K., Colman, D.R., and Kemler, R. (2005). Differential expression of individual gamma-protocadherins during mouse brain development. Mol. Cell. Neurosci. 29, 603-616.
21. Garrett, A. M. and Weiner, J. A. (2009). Control of CNS Synapse Development by G-Protocadherin-Mediated Astrocyte-Neuron Contact. J. Neurosci. 29, 11723-11731.
22. Garrett, A.M., Schreiner, D., Lobas, M.A., and Weiner, J.A. (2012). gamma-protocadherins control cortical dendrite arborization by regulating the activity of a FAK/PKC/MARCKS signaling pathway. Neuron 74, 269-276.
23. Gillen, A.E., and Harris, A. (2011). The role of CTCF in coordinating the expression of single gene loci. Biochem. Cell Biol. 89, 489-494.
24. Golan-Mashiach, M., Grunspan, M., Emmanuel, R., Gibbs-Bar, L., Dikstein, R., and Shapiro, E. (2012). Identification of CTCF as a master regulator of the clustered protocadherin genes. Nuc. Acids Res. 40, 3378-3391.
25. Gumbiner, B.M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
26. Han, M.H., Lin, C., Meng, S., and Wang, X. (2010). Proteomics analysis reveals overlapping functions of clustered protocadherins. Mol. Cell. Proteom. 9, 71-83.
27. Hanson, H.H., Kang, S., Fernandez-Monreal, M., Oung, T., Yildirim, M., Lee, R., Suyama, K., Hazan, R.B., and Phillips, G.R. (2010). LC3-dependent intracellular membrane tubules induced by gamma-protocadherins A3 and B2: a role for intraluminal interactions. J. Biol. Chem. 285, 20982-20992.
28. Hasegawa, S., Hamada, S., Kumode, Y., Esumi, S., Katori, S., Fukuda, E., Uchiyama, Y., Hirabayashi, T., Mombaerts, P., and Yagi, T. (2008). The protocadherin-alpha family is involved in axonal coalescence of olfactory sensory neurons into glomeruli of the olfactory bulb in mouse. Mol. Cell. Neurosci. 38, 66-79.
29. Hasegawa, S., Hirabayashi, T., Kondo, T., Inoue, K., Esumi, S., Okayama, A., Hamada, S., and Yagi, T. (2012). Constitutively expressed Protocadherin-alpha regulates the coalescence and elimination of homotypic olfactory axons through its cytoplasmic region. Front. Mol. Neurosci. 5, 97.
30. Hirano, K., Kaneko, R., Izawa, T., Kawaguchi, M., Kitsukawa, T., and Yagi, T. (2012). Singleneuron diversity generated by Protocadherin-beta cluster in mouse central and peripheral nervous systems. Front. Mol. Neurosci. 5, 90.
31. Hong, E., and Brewster, R. (2006). N-cadherin is required for the polarized cell behaviors that drive neurulation in the zebrafish. Development 133, 3895-3905.
32. Hulpiau, P., and Van Roy, F. (2009). Molecular evolution of the cadherin superfamily. Int. J. Biochem. Cell Biol. 41, 349-369.
33. Hulpiau, P., and Van Roy, F. (2011). New insights into the evolution of metazoan cadherins. Mol. Biol. Evol. 28, 647-657.
34. Kaneko, R., Kato, H., Kawamura, Y., Esumi, S., Hirayama, T., Hirabayashi, T., and Yagi, T. (2006). Allelic gene regulation of Pcdh-alpha and Pcdh-gamma clusters involving both monoallelic and biallelic expression in single Purkinje cells. J. Biol. Chem. 281, 30551-30560.
35. Kang, J.S., Feinleib, J.L., Knox, S., Ketteringham, M.A., and Krauss, R.S. (2003). Promyogenic members of the Ig and cadherin families associate to positively regulate differentiation. Proc Natl Acad Sci USA 100, 3989-3994.
36. Katori, S., Hamada, S., Noguchi, Y., Fukuda, E., Yamamoto, T., Yamamoto, H., Hasegawa, S., and Yagi, T. (2009). Protocadherin-alpha family is required for serotonergic projections to appropriately innervate target brain areas. J. Neurosci. 29, 9137-9147.
37. Kawaguchi, M., Toyama, T., Kaneko, R., Hirayama, T., Kawamura, Y., and Yagi, T. (2008). Relationship between DNA methylation states and transcription of individual isoforms encoded by the protocadherin-alpha gene cluster. J Biol Chem 283, 12064-12075.
38. Kehayova, P., Monahan, K., Chen, W., and Maniatis, T. (2011). Regulatory elements required for the activation and repression of the protocadherin-alpha gene cluster. Proc Natl Acad Sci USA 108, 17195-17200.
39. Kim, S.H., Yamamoto, A., Bouwmeester, T., Agius, E., and Robertis, E.M. (1998). The role of paraxial protocadherin in selective adhesion and cell movements of the mesoderm during Xenopus gastrulation. Development 125, 4681-4690.
40. Kim, S.Y., Yasuda, S., Tanaka, H., Yamagata, K., and Kim, H. (2011). Non-clustered protocadherin. Cell adhesion & migration 5, 97-105.
41. Kohmura N, Senzaki K, Hamada S, Kai, N., Yasuda, R., Watanabe, M., Ishii, H., Yasuda, M., Mishina, M., and Yagi, T. (1998). Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron 20,1137-51.
42. Lefebvre, J.L., Zhang, Y., Meister, M., Wang, X., and Sanes, J.R. (2008). gamma-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina. Development 135, 4141-4151.
43. Lefebvre, J.L., Kostadinov, D., Chen, W.V., Maniatis, T., and Sanes, J.R. (2012). Protocadherins mediate dendritic self-avoidance in the mammalian nervous system. Nature, 488: 517-521.
44. Lele, Z., Folchert, A., Concha, M., Rauch, G.-J., Geisler, R., Rosa, F., Wilson, S.W., Hammerschmidt, M., and Bally-Cuif, L. (2002). parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 129, 3281-3294.
45. Li, H., Leung, T.C., Hoffman, S., Balsamo, J., and Lilien, J. (2000). Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan. J. Cell Biol. 149, 1275-1288.
46. Li, Y., Xiao, H., Chiou, T.T., Jin, H., Bonhomme, B., Miralles, C.P., Pinal, N., Ali, R., Chen, W.V., Maniatis, T., and De Blas, A.L. (2012). Molecular and functional interaction between protocadherin-gammaC5 and GABAA receptors. J. Neurosci. 32, 11780-11797.
47. Mcgowan, P.O., Suderman, M., Sasaki, A., Huang, T.C., Hallett, M., Meaney, M.J., and Szyf, M. (2011). Broad epigenetic signature of maternal care in the brain of adult rats. PloS One 6, e14739.
48. Monahan, K., Rudnick, N.D., Kehayova, P.D., Pauli, F., Newberry, K.M., Myers, R.M., and Maniatis, T. (2012). Role of CCCTC binding factor (CTCF) and cohesin in the generation of single-cell diversity of protocadherin-alpha gene expression. Proc Natl Acad Sci USA 109, 9125-9130.
49. Morishita H, Kawaguchi M, Murata Y, Seiwa, C., Hamada, S., Asou, H., and Yagi, T. (2004). Myelination triggers local loss of axonal CNR/protocadherin alpha family protein expression. Eur J Neurosci 20, 2843-7.
50. Morishita, H., Umitsu, M., Murata, Y., Shibata, N., Udaka, K., Higuchi, Y., Akutsu, H., Yamaguchi, T., Yagi, T., and Ikegami, T. (2006). Structure of the cadherin-related neuronal receptor/protocadherin-alpha first extracellular cadherin domain reveals diversity across cadherin families. J. Biol. Chem. 281, 33650-33663.
51. Morishita, H., and Yagi, T. (2007). Protocadherin family: diversity, structure, and function. Curr. Opin. Cell Biol. 19, 584-592.
52. Morita, H., Nandadasa, S., Yamamoto, T.S., Terasaka-Iioka, C., Wylie, C., and Ueno, N. (2010). Nectin-2 and N-cadherin interact through extracellular domains and induce apical accumulation of F-actin in apical constriction of Xenopus neural tube morphogenesis. Development 137, 1315-1325.
53. Murata, Y., Hamada, S., Morishita, H., Mutoh, T., and Yagi, T. (2004). Interaction with protocadherin-gamma regulates the cell surface expression of protocadherin-alpha. J Biol Chem 279, 49508-49516.
54. Mutoh, T., Hamada, S., Senzaki, K., Murata, Y., and Yagi, T. (2004). Cadherin-related neuronal receptor 1 (CNR1) has cell adhesion activity with beta1 integrin mediated through the RGD site of CNR1. Exp. Cell Res. 294, 494-508.
55. Nelson, W.J. (2008). Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem. Soc. Trans. 36, 149-155.
56. Niessen, C.M., Leckband, D., and Yap, A.S. (2011). Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation. Physiol. Rev. 91, 691-731.
57. Noguchi, Y., Hirabayashi, T., Katori, S., Kawamura, Y., Sanbo, M., Hirabayashi, M., Kiyonari, H., Nakao, K., Uchimura, A., and Yagi, T. (2009). Total expression and dual gene-regulatory mechanisms maintained in deletions and duplications of the Pcdha cluster. J Biol Chem 284, 32002-32014.
58. Nollet, F., Kools, P., and Van Roy, F. (2000). Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J. Mol. Biol. 299, 551-572.
59. O'Leary, R., Reilly, J.E., Hanson, H.H., Kang, S., Lou, N., and Phillips, G.R. (2011). A variable cytoplasmic domain segment is necessary for gamma-protocadherin trafficking and tubulation in the endosome/lysosome pathway. Mol. Biol. Cell 22, 4362-4372.
60. Phillips, G.R., Tanaka, H., Frank, M., Elste, A., Fidler, L., Benson, D.L., and Colman, D.R. (2003). Gamma-protocadherins are targeted to subsets of synapses and intracellular organelles in neurons. Journal of Neuroscience 23, 5096-5104.
61. Prasad, T., Wang, X., Gray, P.A., and Weiner, J.A. (2008). A differential developmental pattern of spinal interneuron apoptosis during synaptogenesis: insights from genetic analyses of the protocadherin-gamma gene cluster. Development 135, 4153-4164.
62. Prasad, T. and Weiner, J.A. (2011). Direct and indirect regulation of spinal cord Ia afferent terminal formation by the t-Protocadherins. Front. Mol. Neurosci, 4:54.
63. Redies, C., Hertel, N., and Hubner, C.A. (2012). Cadherins and neuropsychiatric disorders. Brain Res. 1470, 130-144.
64. Redies, C., Vanhalst, K., and Roy, F. (2005). delta-Protocadherins: unique structures and functions. Cell. Mol. Life Sci. 62, 2840-2852.
65. Rhee, J., Buchan, T., Zukerberg, L., Lilien, J., and Balsamo, J. (2007). Cables links Robo-bound Abl kinase to N-cadherin-bound beta-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat. Cell Biol. 9, 883-892.
66. Rhee, J., Mahfooz, N.S., Arregui, C., Lilien, J., Balsamo, J., and Vanberkum, M.F. (2002). Activation of the repulsive receptor Roundabout inhibits N-cadherin-mediated cell adhesion. Nat. Cell Biol. 4, 798-805.
67. Ribich, S., Tasic, B., and Maniatis, T. (2006). Identification of long-range regulatory elements in the protocadherin-alpha gene cluster. Proc Natl Acad Sci USA 103, 19719-19724.
68. Sano, K., Tanihara, H., Heimark, R.L., Obata, S., Davidson, M., St John, T., Taketani, S., and Suzuki, S. (1993). Protocadherins: a large family of cadherin-related molecules in central nervous system. EMBO J. 12, 2249-2256.
69. Schalm, S.S., Ballif, B.A., Buchanan, S.M., Phillips, G.R., and Maniatis, T. (2010). Phosphorylation of protocadherin proteins by the receptor tyrosine kinase Ret. Proc Natl Acad Sci USA 107, 13894-13899.
70. Schoenherr, C.J., and Anderson, D.J. (1995). Silencing is golden: negative regulation in the control of neuronal gene transcription. Curr. Opin. Neurobiol. 5, 566-571.
71. Schreiner, D., and Weiner, J.A. (2010). Combinatorial homophilic interaction between gammaprotocadherin multimers greatly expands the molecular diversity of cell adhesion. Proc Natl Acad Sci USA 107, 14893-14898.
72. Shapiro, L., and Colman, D.R. (1999). The diversity of cadherins and implications for a synaptic adhesive code in the CNS. Neuron 23, 427-430.
73. Suderman, M., Mcgowan, P.O., Sasaki, A., Huang, T.C., Hallett, M.T., Meaney, M.J., Turecki, G., and Szyf, M. (2012). Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. Proc Natl Acad Sci USA 109 Suppl 2, 17266-17272.
74. Sugino, H., Hamada, S., Yasuda, R., Tuji, A., Matsuda, Y., Fujita, M., and Yagi, T. (2000). Genomic organization of the family of CNR cadherin genes in mice and humans. Genomics 63, 75-87.
75. Suo, L., Lu, H., Ying, G., Capecchi, M.R., and Wu, Q. (2012). Protocadherin clusters and cell adhesion kinase regulate dendrite complexity through Rho GTPase. J. Mol. Cell Biol.
76. Takeichi, M. (2007). The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci. 8, 11-20.
77. Tan, Y.P., Li, S., Jiang, X.J., Loh, W., Foo, Y.K., Loh, C.B., Xu, Q., Yuen, W.H., Jones, M., Fu, J., Venkatesh, B., and Yu, W.P. (2010). Regulation of protocadherin gene expression by multiple neuron-restrictive silencer elements scattered in the gene cluster. Nuc. Acids Res. 38, 4985-4997.
78. Tasic, B., Nabholz, C.E., Baldwin, K.K., Kim, Y., Rueckert, E.H., Ribich, S.A., Cramer, P., Wu, Q., Axel, R., and Maniatis, T. (2002). Promoter choice determines splice site selection in protocadherin alpha and gamma pre-mRNA splicing. Mol. Cell 10, 21-33.
79. Vanhalst, K., Kools, P., Staes, K., Van Roy, F., and Redies, C. (2005). delta-Protocadherins: a gene family expressed differentially in the mouse brain. Cell. Mol. Life Sci. 62, 1247-1259.
80. Wang, X., Su, H., and Bradley, A. (2002a). Molecular mechanisms governing Pcdh-gamma gene expression: evidence for a multiple promoter and cis-alternative splicing model. Genes Dev. 16, 1890-1905.
81. Wang, X., Weiner, J.A., Levi, S., Craig, A.M., Bradley, A., and Sanes, J.R. (2002b). Gamma protocadherins are required for survival of spinal interneurons. Neuron 36, 843-854.
82. Weiner, J.A., Wang, X., Tapia, J.C., and Sanes, J.R. (2005). Gamma protocadherins are required for synaptic development in the spinal cord. Proc Natl Acad Sci USA 102, 8-14.
83. Williams, E.J., Williams, G., Howell, F.V., Skaper, S.D., Walsh, F.S., and Doherty, P. (2001). Identification of an N-cadherin motif that can interact with the fibroblast growth factor receptor and is required for axonal growth. J. Biol. Chem. 276, 43879-43886.
84. Wolverton, T., and Lalande, M. (2001). Identification and characterization of three members of a novel subclass of protocadherins. Genomics 76, 66-72.
85. Wu, Q., and Maniatis, T. (1999). A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell 97, 779-790.
86. Wu, Q., Zhang, T., Cheng, J.F., Kim, Y., Grimwood, J., Schmutz, J., Dickson, M., Noonan, J.P., Zhang, M.Q., Myers, R.M., and Maniatis, T. (2001). Comparative DNA sequence analysis of mouse and human protocadherin gene clusters. Genome research 11, 389-404.
87. Yagi, T. (2012). Molecular codes for neuronal individuality and cell assembly in the brain. Front. Mol. Neurosci. 5, 45.
88. Yagi, T., and Takeichi, M. (2000). Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes & development 14, 1169-1180.
89. Yasuda, S., Tanaka, H., Sugiura, H., Okamura, K., Sakaguchi, T., Tran, U., Takemiya, T., Mizoguchi, A., Yagita, Y., Sakurai, T., De Robertis, E.M., and Yamagata, K. (2007). Activity-induced protocadherin arcadlin regulates dendritic spine number by triggering Ncadherin endocytosis via TAO2beta and p38 MAP kinases. Neuron 56, 456-471.
90. Yokota, S., Hirayama, T., Hirano, K., Kaneko, R., Toyoda, S., Kawamura, Y., Hirabayashi, M., Hirabayashi, T., and Yagi, T. (2011). Identification of the cluster control region for the protocadherin-beta genes located beyond the protocadherin-gamma cluster. J. Biol. Chem. 286, 31885-31895.
91. Zipursky, S.L., and Sanes, J.R. (2010). Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 143, 343-353.