Cadherin defects in inherited human diseases

Progress in Molecular Biology and Translational Science

Volumn 116, Issue , 2013, Pages 361-384

  El Amraoui, Aziz ^a,b   Petit, Christine ^a,b,c  

^a Institut Pasteur   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c Centre de Recherche Interdisciplinaire en Biologie   (France)

Author keywords

Adhesion; Blindness; Cadherin; Cardiomyopathies; Deafness; Hair bundle; Hair cell; Hypotrichosis; Photoreceptor cell; Usher syndrome

Indexed keywords

EID: 84875234957     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394311-8.00016-9     Document Type: Chapter

References (105)

1. T.J. Harris, and U. Tepass Adherens junctions: from molecules to morphogenesis Nat Rev Mol Cell Biol 11 2010 502 514
2. G.A. Gomez, R.W. McLachlan, and A.S. Yap Productive tension: force-sensing and homeostasis of cell-cell junctions Trends Cell Biol 21 2011 499 505
3. S. Hirano, and M. Takeichi Cadherins in brain morphogenesis and wiring Physiol Rev 92 2012 597 634
4. H. Oda, and M. Takeichi Evolution: structural and functional diversity of cadherin at the adherens junction J Cell Biol 193 2011 1137 1146
5. G.F. Weber, M.A. Bjerke, and D.W. DeSimone Integrins and cadherins join forces to form adhesive networks J Cell Sci 124 2011 1183 1193
6. J. Brasch, O.J. Harrison, B. Honig, and L. Shapiro Thinking outside the cell: how cadherins drive adhesion Trends Cell Biol 22 2012 299 310
7. P. Hulpiau, and F. van Roy Molecular evolution of the cadherin superfamily Int J Biochem Cell Biol 41 2009 349 369
8. P. Hulpiau, and F. van Roy New insights into the evolution of metazoan cadherins Mol Biol Evol 28 2011 647 657
9. A. El-Amraoui, and C. Petit Cadherins as targets for genetic diseases Cold Spring Harb Perspect Biol 2 2010 a003095
10. C. Jamora, R. DasGupta, P. Kocieniewski, and E. Fuchs Links between signal transduction, transcription and adhesion in epithelial bud development Nature 422 2003 317 322
11. E. Sprecher, R. Bergman, G. Richard, R. Lurie, S. Shalev, and D. Petronius Hypotrichosis with juvenile macular dystrophy is caused by a mutation in CDH3, encoding P-cadherin Nat Genet 29 2001 134 136
12. M. Indelman, J. Eason, M. Hummel, O. Loza, M. Suri, and M.J. Leys Novel CDH3 mutations in hypotrichosis with juvenile macular dystrophy Clin Exp Dermatol 32 2007 191 196
13. K.W. Kjaer, L. Hansen, G.C. Schwabe, A.P. Marques-de-Faria, H. Eiberg, and S. Mundlos Distinct CDH3 mutations cause ectodermal dysplasia, ectrodactyly, macular dystrophy (EEM syndrome) J Med Genet 42 2005 292 298
14. Y. Shimomura, M. Wajid, L. Shapiro, and A.M. Christiano P-cadherin is a p63 target gene with a crucial role in the developing human limb bud and hair follicle Development 135 2008 743 753
15. Y. Shimomura Congenital hair loss disorders: rare, but not too rare J Dermatol 39 2012 3 10
16. E. Delva, D.K. Tucker, and A.P. Kowalczyk The desmosome Cold Spring Harb Perspect Biol 1 2009 a002543
17. J.A. McGrath Inherited disorders of desmosomes Australas J Dermatol 46 2005 221 229
18. M.A. Brooke, D. Nitoiu, and D.P. Kelsell Cell-cell connectivity: desmosomes and disease J Pathol 226 2012 158 171
19. L. Rickman, D. Simrak, H.P. Stevens, D.M. Hunt, I.A. King, and S.P. Bryant N-terminal deletion in a desmosomal cadherin causes the autosomal dominant skin disease striate palmoplantar keratoderma Hum Mol Genet 8 1999 971 976
20. A. Kljuic, H. Bazzi, J.P. Sundberg, A. Martinez-Mir, R. O'Shaughnessy, and M.G. Mahoney Desmoglein 4 in hair follicle differentiation and epidermal adhesion: evidence from inherited hypotrichosis and acquired pemphigus vulgaris Cell 113 2003 249 260
21. M. Ayub, S. Basit, M. Jelani, F. Ur Rehman, M. Iqbal, and M. Yasinzai A homozygous nonsense mutation in the human desmocollin-3 (DSC3) gene underlies hereditary hypotrichosis and recurrent skin vesicles Am J Hum Genet 85 2009 515 520
22. M.B. Dua-Awereh, Y. Shimomura, L. Kraemer, M. Wajid, and A.M. Christiano Mutations in the desmoglein 1 gene in five Pakistani families with striate palmoplantar keratoderma J Dermatol Sci 53 2009 192 197
23. D. Hershkovitz, J. Lugassy, M. Indelman, R. Bergman, and E. Sprecher Novel mutations in DSG1 causing striate palmoplantar keratoderma Clin Exp Dermatol 34 2009 224 228
24. H. Wan, P.J. Dopping-Hepenstal, M.J. Gratian, M.G. Stone, G. Zhu, and P.E. Purkis Striate palmoplantar keratoderma arising from desmoplakin and desmoglein 1 mutations is associated with contrasting perturbations of desmosomes and the keratin filament network Br J Dermatol 150 2004 878 891
25. M. Wajid, H. Bazzi, J. Rockey, J. Lubetkin, A. Zlotogorski, and A.M. Christiano Localized autosomal recessive hypotrichosis due to a frameshift mutation in the desmoglein 4 gene exhibits extensive phenotypic variability within a Pakistani family J Invest Dermatol 127 2007 1779 1782
26. J. Schweizer More than one gene involved in monilethrix: intracellular but also extracellular players J Invest Dermatol 126 2006 1216 1219
27. Y. Shimomura, F. Sakamoto, N. Kariya, K. Matsunaga, and M. Ito Mutations in the desmoglein 4 gene are associated with monilethrix-like congenital hypotrichosis J Invest Dermatol 126 2006 1281 1285
28. H. Bazzi, A. Getz, M.G. Mahoney, A. Ishida-Yamamoto, L. Langbein, and J.K. Wahl 3rd Desmoglein 4 is expressed in highly differentiated keratinocytes and trichocytes in human epidermis and hair follicle Differentiation 74 2006 129 140
29. A.S. Payne No evidence of skin blisters with human desmocollin-3 gene mutation Am J Hum Genet 86 2010 292 (author reply 292)
30. M. Amagai, and J.R. Stanley Desmoglein as a target in skin disease and beyond J Invest Dermatol 132 2012 776 784
31. P. Syrris, D. Ward, A. Evans, A. Asimaki, E. Gandjbakhch, and S. Sen-Chowdhry Arrhythmogenic right ventricular dysplasia/cardiomyopathy associated with mutations in the desmosomal gene desmocollin-2 Am J Hum Genet 79 2006 978 984
32. M.M. Awad, H. Calkins, and D.P. Judge Mechanisms of disease: molecular genetics of arrhythmogenic right ventricular dysplasia/cardiomyopathy Nat Clin Pract Cardiovasc Med 5 2008 258 267
33. J.E. Saffitz Arrhythmogenic cardiomyopathy: advances in diagnosis and disease pathogenesis Circulation 124 2011 e390 e392
34. J.E. Saffitz The pathobiology of arrhythmogenic cardiomyopathy Annu Rev Pathol 6 2011 299 321
35. H. Watkins, H. Ashrafian, and C. Redwood Inherited cardiomyopathies N Engl J Med 364 2011 1643 1656
36. C. Basso, B. Bauce, D. Corrado, and G. Thiene Pathophysiology of arrhythmogenic cardiomyopathy Nat Rev Cardiol 9 2012 223 233
37. D. Jacoby, and W.J. McKenna Genetics of inherited cardiomyopathy Eur Heart J 33 2012 296 304
38. K. Pilichou, C.R. Bezzina, G. Thiene, and C. Basso Arrhythmogenic cardiomyopathy: transgenic animal models provide novel insights into disease pathobiology Circ Cardiovasc Genet 4 2011 318 326
39. C. Basso, E. Czarnowska, M. Della Barbera, B. Bauce, G. Beffagna, and E.K. Wlodarska Ultrastructural evidence of intercalated disc remodelling in arrhythmogenic right ventricular cardiomyopathy: an electron microscopy investigation on endomyocardial biopsies Eur Heart J 27 2006 1847 1854
40. K. Pilichou, C.A. Remme, C. Basso, M.E. Campian, S. Rizzo, and P. Barnett Myocyte necrosis underlies progressive myocardial dystrophy in mouse dsg2-related arrhythmogenic right ventricular cardiomyopathy J Exp Med 206 2009 1787 1802
41. C.A. Krusche, B. Holthofer, V. Hofe, A.M. van de Sandt, L. Eshkind, and E. Bockamp Desmoglein 2 mutant mice develop cardiac fibrosis and dilation Basic Res Cardiol 106 2011 617 633
42. S. Goossens, B. Janssens, S. Bonne, R. De Rycke, F. Braet, and J. van Hengel A unique and specific interaction between alphaT-catenin and plakophilin-2 in the area composita, the mixed-type junctional structure of cardiac intercalated discs J Cell Sci 120 2007 2126 2136
43. J. Li, S. Goossens, J. van Hengel, E. Gao, L. Cheng, and K. Tyberghein Loss of alphaT-catenin alters the hybrid adhering junctions in the heart and leads to dilated cardiomyopathy and ventricular arrhythmia following acute ischemia J Cell Sci 125 2012 1058 1067
44. D. Swope, L. Cheng, E. Gao, J. Li, and G.L. Radice Loss of cadherin-binding proteins beta-catenin and plakoglobin in the heart leads to gap junction remodeling and arrhythmogenesis Mol Cell Biol 32 2012 1056 1067
45. R. Lombardi, M. da Graca Cabreira-Hansen, A. Bell, R.R. Fromm, J.T. Willerson, and A.J. Marian Nuclear plakoglobin is essential for differentiation of cardiac progenitor cells to adipocytes in arrhythmogenic right ventricular cardiomyopathy Circ Res 109 2011 1342 1353
46. F.I. Marcus, W.J. McKenna, D. Sherrill, C. Basso, B. Bauce, and D.A. Bluemke Diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia: proposed modification of the Task Force Criteria Eur Heart J 31 2010 806 814
47. A. Asimaki, H. Tandri, H. Huang, M.K. Halushka, S. Gautam, and C. Basso A new diagnostic test for arrhythmogenic right ventricular cardiomyopathy N Engl J Med 360 2009 1075 1084
48. B. Murray Arrhythmogenic right ventricular dysplasia/cardiomyopathy (ARVD/C): a review of molecular and clinical literature J Genet Couns 21 2012 494 504
49. K. Bhalla, Y. Luo, T. Buchan, M.A. Beachem, G.F. Guzauskas, and S. Ladd Alterations in CDH15 and KIRREL3 in patients with mild to severe intellectual disability Am J Hum Genet 83 2008 703 713
50. K. Wang, H. Zhang, D. Ma, M. Bucan, J.T. Glessner, and B.S. Abrahams Common genetic variants on 5p14.1 associate with autism spectrum disorders Nature 459 2009 528 533
51. S.M. Singh, C. Castellani, and R. O'Reilly Autism meets schizophrenia via cadherin pathway Schizophr Res 116 2010 293 294
52. P. Soronen, H.M. Ollila, M. Antila, K. Silander, O.M. Palo, and T. Kieseppa Replication of GWAS of bipolar disorder: association of SNPs near CDH7 with bipolar disorder and visual processing Mol Psychiatry 15 2010 4 6
53. M.H. Willemsen, B.A. Fernandez, C.A. Bacino, E. Gerkes, A.P. de Brouwer, and R. Pfundt Identification of ANKRD11 and ZNF778 as candidate genes for autism and variable cognitive impairment in the novel 16q24.3 microdeletion syndrome Eur J Hum Genet 18 2010 429 435
54. A.T. Pagnamenta, H. Khan, S. Walker, D. Gerrelli, K. Wing, and M.C. Bonaglia Rare familial 16q21 microdeletions under a linkage peak implicate cadherin 8 (CDH8) in susceptibility to autism and learning disability J Med Genet 48 2011 48 54
55. S.Y. Kim, S. Yasuda, H. Tanaka, K. Yamagata, and H. Kim Non-clustered protocadherin Cell Adh Migr 5 2011 97 105
56. M.D. Speevak, and S.A. Farrell Non-syndromic language delay in a child with disruption in the Protocadherin11X/Y gene pair Am J Med Genet B Neuropsychiatr Genet 156B 2011 484 489
57. L.M. Dibbens, P.S. Tarpey, K. Hynes, M.A. Bayly, I.E. Scheffer, and R. Smith X-linked protocadherin 19 mutations cause female-limited epilepsy and cognitive impairment Nat Genet 40 2008 776 781
58. C. Depienne, D. Bouteiller, B. Keren, E. Cheuret, K. Poirier, and O. Trouillard Sporadic infantile epileptic encephalopathy caused by mutations in PCDH19 resembles Dravet syndrome but mainly affects females PLoS Genet 5 2009 e1000381
59. C. Depienne, O. Trouillard, D. Bouteiller, I. Gourfinkel-An, K. Poirier, and F. Rivier Mutations and deletions in PCDH19 account for various familial or isolated epilepsies in females Hum Mutat 32 2011 E1959 E1975
60. L.M. Dibbens, R. Kneen, M.A. Bayly, S.E. Heron, T. Arsov, and J.A. Damiano Recurrence risk of epilepsy and mental retardation in females due to parental mosaicism of PCDH19 mutations Neurology 76 2011 1514 1519
61. C. Depienne, and E. LeGuern PCDH19-related infantile epileptic encephalopathy: an unusual X-linked inheritance disorder Hum Mutat 33 2012 627 634
62. E. Caberlotto, V. Michel, J.B. de Monvel, and C. Petit Coupling of the mechanotransduction machinery and F-actin polymerization in the cochlear hair bundles Bioarchitecture 1 2011 169 174
63. A. El-Amraoui, and C. Petit Usher I syndrome: unravelling the mechanisms that underlie the cohesion of the growing hair bundle in inner ear sensory cells J Cell Sci 118 2005 4593 4603
64. C. Petit, and G. Richardson Linking deafness genes to hair-bundle development and function Nat Neurosci 12 2009 703 710
65. C. Bonnet, and A. El-Amraoui Usher syndrome (sensorineural deafness and retinitis pigmentosa): pathogenesis, molecular diagnosis and therapeutic approaches Curr Opin Neurol 25 2012 42 49
66. G.P. Richardson, J.B. de Monvel, and C. Petit How the genetics of deafness illuminates auditory physiology Annu Rev Physiol 73 2011 311 334
67. G. Lefèvre, V. Michel, D. Weil, L. Lepelletier, E. Bizard, and U. Wolfrum A core cochlear phenotype in USH1 mouse mutants implicates fibrous links of the hair bundle in its cohesion, orientation and differential growth Development 135 2008 1427 1437
68. B. Boëda, A. El-Amraoui, A. Bahloul, R. Goodyear, L. Daviet, and S. Blanchard Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle EMBO J 21 2002 6689 6699
69. J. Siemens, P. Kazmierczak, A. Reynolds, M. Sticker, A. Littlewood-Evans, and U. Muller The Usher syndrome proteins cadherin 23 and harmonin form a complex by means of PDZ-domain interactions Proc Natl Acad Sci U S A 99 2002 14946 14951
70. V. Michel, R.J. Goodyear, D. Weil, W. Marcotti, I. Perfettini, and U. Wolfrum Cadherin 23 is a component of the transient lateral links in the developing hair bundles of cochlear sensory cells Dev Biol 280 2005 281 294
71. A. Lagziel, Z.M. Ahmed, J.M. Schultz, R.J. Morell, I.A. Belyantseva, and T.B. Friedman Spatiotemporal pattern and isoforms of cadherin 23 in wild type and waltzer mice during inner ear hair cell development Dev Dyn 205 2005 295 306
72. N. Michalski, V. Michel, A. Bahloul, G. Lefèvre, S. Chardenoux, and H. Yagi Molecular characterization of the ankle link complex in cochlear hair cells and its role in the hair bundle functioning J Neurosci 27 2007 6478 6488
73. S.W. Webb, N. Grillet, L.R. Andrade, W. Xiong, L. Swarthout, and C.C. Della Santina Regulation of PCDH15 function in mechanosensory hair cells by alternative splicing of the cytoplasmic domain Development 138 2011 1607 1617
74. E. Caberlotto, V. Michel, I. Foucher, A. Bahloul, R.J. Goodyear, and E. Pepermans Usher type 1 G protein sans is a critical component of the tip-link complex, a structure controlling actin polymerization in stereocilia Proc Natl Acad Sci U S A 108 2011 5825 5830
75. A. Adato, G. Lefevre, B. Delprat, V. Michel, N. Michalski, and S. Chardenoux Usherin, the defective protein in Usher syndrome type IIA, is likely to be a component of interstereocilia ankle links in the inner ear sensory cells Hum Mol Genet 14 2005 3921 3932
76. L. Pan, and M. Zhang Structures of usher syndrome 1 proteins and their complexes Physiology (Bethesda) 27 2012 25 42
77. P. Kazmierczak, H. Sakaguchi, J. Tokita, E.M. Wilson-Kubalek, R.A. Milligan, and U. Muller Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells Nature 449 2007 87 91
78. N. Michalski, V. Michel, E. Caberlotto, G.M. Lefèvre, A.F.J. van Aken, and J.-Y. Tinevez Harmonin-b, an actin-binding scaffold protein, is involved in the adaptation of mechanoelectrical transduction by sensory hair cells Pflugers Arch 459 2009 115 130
79. N. Grillet, W. Xiong, A. Reynolds, P. Kazmierczak, T. Sato, and C. Lillo Harmonin mutations cause mechanotransduction defects in cochlear hair cells Neuron 62 2009 375 387
80. A. Bahloul, V. Michel, J.P. Hardelin, S. Nouaille, S. Hoos, and A. Houdusse Cadherin-23, myosin VIIa and harmonin, encoded by Usher syndrome type I genes, form a ternary complex and interact with membrane phospholipids Hum Mol Genet 19 2010 3557 3565
81. R. Fettiplace, and C.M. Hackney The sensory and motor roles of auditory hair cells Nat Rev Neurosci 7 2006 19 29
82. J. Vendome, S. Posy, X. Jin, F. Bahna, G. Ahlsen, and L. Shapiro Molecular design principles underlying beta-strand swapping in the adhesive dimerization of cadherins Nat Struct Mol Biol 18 2011 693 700
83. H.M. Elledge, P. Kazmierczak, P. Clark, J.S. Joseph, A. Kolatkar, and P. Kuhn Structure of the N terminus of cadherin 23 reveals a new adhesion mechanism for a subset of cadherin superfamily members Proc Natl Acad Sci U S A 107 2010 10708 10712
84. M. Sotomayor, W.A. Weihofen, R. Gaudet, and D.P. Corey Structural determinants of cadherin-23 function in hearing and deafness Neuron 66 2010 85 100
85. M. Sotomayor, W.A. Weihofen, R. Gaudet, and D.P. Corey Structure of a force-conveying cadherin bond essential for inner-ear mechanotransduction Nature 492 2012 128 132
86. J. Reiners, K. Nagel-Wolfrum, K. Jurgens, T. Marker, and U. Wolfrum Molecular basis of human Usher syndrome: deciphering the meshes of the Usher protein network provides insights into the pathomechanisms of the Usher disease Exp Eye Res 83 2006 97 119
87. D.S. Williams Usher syndrome: animal models, retinal function of Usher proteins, and prospects for gene therapy Vision Res 48 2008 433 441
88. C. Petit Usher syndrome: from genetics to pathogenesis Annu Rev Genomics Hum Genet 2 2001 271 297
89. S.G. Jacobson, A.V. Cideciyan, T.S. Aleman, A. Sumaroka, A.J. Roman, and L.M. Gardner Usher syndromes due to MYO7A, PCDH15, USH2A or GPR98 mutations share retinal disease mechanism Hum Mol Genet 17 2008 2405 2415
90. S.G. Jacobson, A.V. Cideciyan, D. Gibbs, A. Sumaroka, A.J. Roman, and T.S. Aleman Retinal disease course in Usher syndrome 1B due to MYO7A mutations Invest Ophthalmol Vis Sci 52 2011 7924 7936
91. E. Malm, V. Ponjavic, C. Moller, W.J. Kimberling, and S. Andreasson Phenotypes in defined genotypes including siblings with Usher syndrome Ophthalmic Genet 32 2011 65 74
92. E. Malm, V. Ponjavic, C. Moller, W.J. Kimberling, E.S. Stone, and S. Andreasson Alteration of rod and cone function in children with Usher syndrome Eur J Ophthalmol 21 2011 30 38
93. R.T. Libby, J. Kitamoto, R.H. Holme, D.S. Williams, and K.P. Steel Cdh23 mutations in the mouse are associated with retinal dysfunction but not retinal degeneration Exp Eye Res 77 2003 731 739
94. S.L. Ball, D. Bardenstein, and K.N. Alagramam Assessment of retinal structure and function in Ames waltzer mice Invest Ophthalmol Vis Sci 44 2003 3986 3992
95. R.J. Haywood-Watson 2nd, Z.M. Ahmed, S. Kjellstrom, R.A. Bush, Y. Takada, and L.L. Hampton Ames Waltzer deaf mice have reduced electroretinogram amplitudes and complex alternative splicing of Pcdh15 transcripts Invest Ophthalmol Vis Sci 47 2006 3074 3084
96. A. El-Amraoui, J.-S. Schonn, P. Küssel-Andermann, S. Blanchard, C. Desnos, and J.-P. Henry MyRIP, a novel Rab effector, enables myosin VIIa recruitment to retinal melanosomes EMBO Rep 3 2002 463 470
97. D. Gibbs, S.M. Azarian, C. Lillo, J. Kitamoto, A.E. Klomp, and K.P. Steel Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes J Cell Sci 117 2004 6473 6483
98. X. Liu, I.P. Udovichenko, S.D. Brown, K.P. Steel, and D.S. Williams Myosin VIIa participates in opsin transport through the photoreceptor cilium J Neurosci 19 1999 6267 6274
99. I. Sahly, E. Dufour, C. Schietroma, V. Michel, A. Bahloul, and I. Perfettini Localization of Usher 1 proteins to the photoreceptor calyceal processes, which are absent from mice J Cell Biol 199 2012 381 399
100. R.H. Henderson, Z. Li, M.M. Abd El Aziz, D.S. Mackay, M.A. Eljinini, and M. Zeidan Biallelic mutation of protocadherin-21 (PCDH21) causes retinal degeneration in humans Mol Vis 16 2010 46 52
101. E. Ostergaard, M. Batbayli, M. Duno, K. Vilhelmsen, and T. Rosenberg Mutations in PCDH21 cause autosomal recessive cone-rod dystrophy J Med Genet 47 2010 665 669
102. A. Rattner, P.M. Smallwood, J. Williams, C. Cooke, A. Savchenko, and A. Lyubarsky A photoreceptor-specific cadherin is essential for the structural integrity of the outer segment and for photoreceptor survival Neuron 32 2001 775 786
103. Z. Yang, Y. Chen, C. Lillo, J. Chien, Z. Yu, and M. Michaelides Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice J Clin Invest 118 2008 2908 2916
104. M. Michaelides, M.C. Gaillard, P. Escher, L. Tiab, M. Bedell, and F.X. Borruat The PROM1 mutation p.R373C causes an autosomal dominant bull's eye maculopathy associated with rod, rod-cone, and macular dystrophy Invest Ophthalmol Vis Sci 51 2010 4771 4780
105. J. Permanyer, R. Navarro, J. Friedman, E. Pomares, J. Castro-Navarro, and G. Marfany Autosomal recessive retinitis pigmentosa with early macular affectation caused by premature truncation in PROM1 Invest Ophthalmol Vis Sci 51 2010 2656 2663