Abstract
Mice have proven to be a particularly powerful model to study molecular mechanisms of development and disease. The reason for this is the close evolutionary relationship between rodents and humans, similarities in physiological mechanisms in mice and human, and the large number of techniques available to study gene functions in mice. A large number of mice mutations, either germ line, conditional or inducible, have been generated in the past years for adherens junctions components, and the number is still increasing. In this review we will discuss mice models that have contributed to understanding the developmental and physiological role of adherens junctions and their components in mammals and have revealed novel mechanistic aspects of how adherens junctions regulate morphogenesis and tissue homeostasis.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Abe A, Fukui H, Fujii S, Kono T, Mukawa K, Yoshitake N, Sekikawa A, Ichikawa K, Tomita S, Yamagishi H, Imai Y, Shinoda M, Ishizaki H, Tanaka-Okamoto M, Kubota K, Miyoshi J, Takai Y, Fujimori T (2009) Role of Necl-5 in the pathophysiology of colorectal lesions induced by dimethylhydrazine and/or dextran sodium sulphate. J Pathol 217:42–53
Ai D, Fu X, Wang J, Lu M, Chen L, Baldini A, Klein W, Martin J (2007) Canonical Wnt signaling functions in second heart field to promote right ventricular growth. Proc Natl Acad Sci U S A 104:9319–9324
Akar F, Tomaselli G (2005) Conduction abnormalities in nonischemic dilated cardiomyopathy: basic mechanisms and arrhythmic consequences. Trends Cardiovasc Med 15:259–264
Akiyama H, Lyons J, Mori-Akiyama Y, Yang X, Zhang R, Zhang Z, Deng J, Taketo M, Nakamura T, Behringer R, McCrea P, de Crombrugghe B (2004) Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev 18:1072–1087
Anastasiadis PZ, Moon SY, Thoreson MA, Mariner DJ, Crawford HC, Zheng Y, Reynolds AB (2000) Inhibition of RhoA by p120 catenin. Nat Cell Biol 2:637–644
Arango N, Szotek P, Manganaro T, Oliva E, Donahoe P, Teixeira J (2005) Conditional deletion of beta-catenin in the mesenchyme of the developing mouse uterus results in a switch to adipogenesis in the myometrium. Dev Biol 288:276–283
Atit R, Sgaier S, Mohamed O, Taketo M, Dufort D, Joyner A, Niswander L, Conlon R (2006) β-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Dev Biol 296:164–176
Aulehla A, Wiegraebe W, Baubet V, Wahl M, Deng C, Taketo M, Lewandoski M, Pourquié O (2008) A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nat Cell Biol 10:186–193
Backman M, Machon O, Mygland L, van den Bout C, Zhong W, Taketo M, Krauss S (2005) Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev Biol 279:155–168
Barron M, Brookes S, Draper C, Garrod D, Kirkham J, Shore R, Dixon M (2008) The cell adhesion molecule nectin-1 is critical for normal enamel formation in mice. Hum Mol Genet 17:3509–3520
Barrow J, Thomas K, Boussadia-Zahui O, Moore R, Kemler R, Capecchi M, McMahon A (2003) Ectodermal Wnt3/beta-catenin signaling is required for the establishment and maintenance of the apical ectodermal ridge. Genes Dev 17:394–409
Bartlett J, Dobeck J, Tye C, Perez-Moreno M, Stokes N, Reynolds A, Fuchs E, Skobe Z (2010) Targeted p120-catenin ablation disrupts dental enamel development. PLoS One 5:e12703
Battle M, Konopka G, Parviz F, Gaggl A, Yang C, Sladek F, Duncan S (2006) Hepatocyte nuclear factor 4alpha orchestrates expression of cell adhesion proteins during the epithelial transformation of the developing liver. Proc Natl Acad Sci U S A 103:8419–8424
Berx G, van Roy F (2009) Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb Perspect Biol 1:a003129
Bierkamp C, Mclaughlin K, Schwarz H, Huber O, Kemler R (1996) Embryonic heart and skin defects in mice lacking plakoglobin. Dev Biol 180:780–785
Bouchard M, Dong Y, McDermott BJ, Lam D, Brown K, Shelanski M, Bellvé A, Racaniello V (2000) Defects in nuclear and cytoskeletal morphology and mitochondrial localization in spermatozoa of mice lacking nectin-2, a component of cell-cell adherens junctions. Mol Cell Biol 20:2865–2873
Boussadia O, Kutsch S, Hierholzer A, Delmas V, Kemler R (2002) E-cadherin is a survival factor for the lactating mouse mammary gland. Mech Dev 115:53–62
Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch D, McMahon A, Sommer L, Boussadia O, Kemler R (2001) Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128:1253–1264
Bridgewater D, Cox B, Cain J, Lau A, Athaide V, Gill P, Kuure S, Sainio K, Rosenblum N (2008) Canonical WNT/beta-catenin signaling is required for ureteric branching. Dev Biol 317:83–94
Cali G, Zannini M, Rubini P, Tacchetti C, D’Andrea B, Affuso A, Wintermantel T, Boussadia O, Terracciano D, Silberschmidt D, Amendola E, De Felice M, Schutz G, Kemler R, Di Lauro R, Nitsch L (2007) Conditional inactivation of the E-cadherin gene in thyroid follicular cells affects gland development but does not impair junction formation. Endocrinology 148:2737–2746
Campos V, Du M, Li Y (2004) Increased seizure susceptibility and cortical malformation in beta-catenin mutant mice. Biochem Biophys Res Commun 320:606–614
Carmeliet P, Lampugnani M, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oosthuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter M, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert J, Collen D, Dejana E (1999) Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98:147–157
Carnahan R, Rokas A, Gaucher E, Reynolds A (2011) The molecular evolution of the p120-catenin subfamily and its functional associations. PLoS One 5:e15747
Cattelino A, Liebner S, Gallini R, Zanetti A, Balconi G, Corsi A, Bianco P, Wolburg H, Moore R, Oreda B, Kemler R, Dejana E (2003) The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J Cell Biol 162:1111–1122
Cerruti Mainardi P (1996) Cri du Chat syndrome. Orphanet J Rare Dis 1:33
Chang H, Gao F, Guillou F, Taketo M, Huff V, Behringer R (2008) Wt1 negatively regulates beta-catenin signaling during testis development. Development 135:1875–1885
Chen X, Shevtsov S, Hsich E, Cui L, Haq S, Aronovitz M, Kerkelä R, Molkentin J, Liao R, Salomon R, Patten R, Force T (2006) The beta-catenin/T-cell factor/lymphocyte enhancer factor signaling pathway is required for normal and stress-induced cardiac hypertrophy. Mol Cell Biol 26:4462–4473
Cohen E, Wang Z, Lepore J, Lu M, Taketo M, Epstein D, Morrisey E (2007) Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J Clin Invest 117:1794–1804
Corada M, Mariotti M, Thurston G, Smith K, Kunkel R, Brockhaus M, Lampugnani M, Martin-Padura I, Stoppacciaro A, Ruco L, Macdonald D, Ward P, Dejana E (1999) Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc Natl Acad Sci U S A 96:9815–9820
Davis M, Reynolds A (2006) Blocked acinar development, E-cadherin reduction, and intraepithelial neoplasia upon ablation of p120-catenin in the mouse salivary gland. Dev Cell 10:21–31
Day T, Guo X, Garrett-Beal L, Yang Y (2005) Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell 8:739–750
De Langhe S, Carraro G, Tefft D, Li C, Xu X, Chai Y, Minoo P, Hajihosseini M, Drouin J, Kaartinen V, Bellusci S (2008) Formation and differentiation of multiple mesenchymal lineages during lung development is regulated by beta-catenin signaling. PLoS One 3:e1516
De Vries W, Evsikov A, Haac B, Fancher K, Holbrook A, Kemler R, Solter D, Knowles B (2004) Maternal beta-catenin and E-cadherin in mouse development. Development 131:4435–4445
Dejana E, Tournier-Lasserve E, Weinstein BM (2009) The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev Cell 16:209–221
Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B, van Beijnum JR, Griffioen AW, Vink J, Krimpenfort P, Peterse JL, Cardiff RD, Berns A, Jonkers J (2006) Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10:437–449
Derksen PW, Braumuller TM, van der Burg E, Hornsveld M, Mesman E, Wesseling J, Krimpenfort P, Jonkers J (2011) Mammary-specific inactivation of E-cadherin and p53 impairs functional gland development and leads to pleomorphic invasive lobular carcinoma in mice. Dis Model Mech 4:347–358
Dessimoz J, Bonnard C, Huelsken J, Grapin-Botton A (2005) Pancreas-specific deletion of beta-catenin reveals Wnt-dependent and Wnt-independent functions during development. Curr Biol 15:1677–1683
Deutscher E, Hung-Chang Yao H (2007) Essential roles of mesenchyme-derived beta-catenin in mouse Müllerian duct morphogenesis. Dev Biol 307:227–236
Dunty WJ, Biris K, Chalamalasetty R, Taketo M, Lewandoski M, Yamaguchi T (2008) Wnt3a/beta-catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development 135:85–94
Elia L, Yamamoto M, Zang K, Reichardt L (2006) p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 51:43–56
Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17:375–412
Fleming T, Johnson M (1988) From egg to epithelium. Annu Rev Cell Biol 4:459–485
Fleming T, Javed Q, Collins J, Hay M (1993) Biogenesis of structural intercellular junctions during cleavage in the mouse embryo. J Cell Sci Suppl 17:119–125
Fleming TP, Papenbrock T, Fesenko I, Hausen P, Sheth B (2000) Assembly of tight junctions during early vertebrate development. Semin Cell Dev Biol 11:291–299
Fu X, Sun H, Klein W, Mu X (2006) Beta-catenin is essential for lamination but not neurogenesis in mouse retinal development. Dev Biol 299:424–437
Fujita E, Kouroku Y, Ozeki S, Tanabe Y, Toyama Y, Maekawa M, Kojima N, Senoo H, Toshimori K, Momoi T (2006) Oligo-astheno-teratozoospermia in mice lacking RA175/TSLC1/SynCAM/IGSF4A, a cell adhesion molecule in the immunoglobulin superfamily. Mol Cell Biol 26:718–726
Gao X, Arlotta P, Macklis J, Chen J (2007) Conditional knock-out of beta-catenin in postnatal-born dentate gyrus granule neurons results in dendritic malformation. J Neurosci 27:14317–14325
Gavard J, Gutkind J (2006) VEGF controls endothelial-cell permeability by promoting the β-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 8:1223–1234
Giangreco A, Jensen K, Takai Y, Miyoshi J, Watt F (2009) Necl2 regulates epidermal adhesion and wound repair. Development 136:3505–3514
Gladden A, Hebert A, Schneeberger E, McClatchey A (2010) The NF2 tumor suppressor, Merlin, regulates epidermal development through the establishment of a junctional polarity complex. Dev Cell 19:727–739
Glass D, Bialek P, Ahn J, Starbuch M, Patel M, Clevers H, Taketo M, Long F, McMahon A, Lang R et al (2005) Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 8:751–764
Gory-Fauré S, Prandini M, Pointu H, Roullot V, Pignot-Paintrand I, Vernet M, Huber P (1999) Role of vascular endothelial-cadherin in vascular morphogenesis. Development 126:2093–2102
Gottardi CJ, Wong E, Gumbiner BM (2001) E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J Cell Biol 153:1049–1060
Grigoryan T, Wend P, Klaus A, Birchmeier W (2008) Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of b-catenin in mice. Genes Dev 22:2308–2341
Grivennikov S, Greten F, Karin M (2010) Immunity, inflammation, and cancer. Cell 140:883–899
Gumbiner B, Stevenson B, Grimaldi A (1988) The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J Cell Biol 107:1575–1587
Guo X, Day T, Jiang X, Garrett-Beal L, Topol L, Yang Y (2004) Wnt/beta-catenin signaling is sufficient and necessary for synovial joint formation. Genes Dev 18:2404–2417
Gustafson-Wagner E, Sinn H, Chen Y, Wang D, Reiter R, Lin J, Yang B, Williamson R, Chen J, Lin C, Lin J (2007) Loss of mXinalpha, an intercalated disk protein, results in cardiac hypertrophy and cardiomyopathy with conduction defects. Am J Physiol Heart Circ Physiol 293:H2680–2692
Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, Kemler R (1995) Lack of beta-catenin affects mouse development at gastrulation. Development 121:3529–3537
Hari L, Brault V, Kléber M, Lee H, Ille F, Leimeroth R, Paratore C, Suter U, Kemler R, Sommer L (2002) Lineage-specific requirements of beta-catenin in neural crest development. J Cell Biol 159:867–880
Harris TJ, Peifer M (2005) The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila. J Cell Biol 170:813–823
Harris TJ, Tepass U (2010) Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 11:502–514
Hatta K, Takagi S, Fujisawa H, Takeichi M (1987) Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev Biol 120:215–227
Hermiston ML, Gordon JI (1995a) In vivo analysis of cadherin function in the mouse intestinal epithelium: essential roles in adhesion, maintenance of differentiation, and regulation of programmed cell death. J Cell Biol 129:489–506
Hermiston ML, Gordon JI (1995b) Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 270:1203–1207
Hermiston ML, Wong MH, Gordon JI (1996) Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system. Genes Dev 10:985–996
Hill T, Später D, Taketo M, Birchmeier W, Hartmann C (2005) Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 8:727–738
Hill T, Taketo M, Birchmeier W, Hartmann C (2006) Multiple roles of mesenchymal beta-catenin during murine limb patterning. Development 133:1219–1229
Hirai Y, Nose A, Kobayashi S, Takeichi M (1989) Expression and role of E- and P-cadherin adhesion molecules in embryonic histogenesis II. Skin morphogenesis. Development 105:271–277
Honda T, Sakisaka T, Yamada T, Kumazawa N, Hoshino T, Kajita M, Kayahara T, Ishizaki H, Tanaka-Okamoto M, Mizoguchi A, Manabe T, Miyoshi J, Takai Y (2006) Involvement of nectins in the formation of puncta adherentia junctions and the mossy fiber trajectory in the mouse hippocampus. Mol Cell Neurosci 31:315–325
Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W (2000) Requirement for beta-catenin in anterior-posterior axis formation in mice. J Cell Biol 148:567–578
Huelsken J, Vogel R, Erdmann B, Cotsarelis G, Birchmeier W (2001) beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105:533–545
Ikeda W, Nakanishi H, Miyoshi J, Mandai K, Ishizaki H, Tanaka M, Togawa A, Takahashi K, Nishioka H, Yoshida H, Mizoguchi A, Nishikawa S, Takai Y (1999) Afadin: a key molecule essential for structural organization of cell-cell junctions of polarized epithelia during embryogenesis. J Cell Biol 146:1117–1132
Inagaki M, Irie K, Ishizaki H, Tanaka-Okamoto M, Morimoto K, Inoue E, Ohtsuka T, Miyoshi J, Takai Y (2005) Roles of cell-adhesion molecules nectin 1 and nectin 3 in ciliary body development. Development 132:1525–1537
Inoue T, Tanaka T, Suzuki S, Takeichi M (1998) Cadherin-6 in the developing mouse brain: expression along restricted connection systems and synaptic localization suggest a potential role in neuronal circuitry. Dev Dyn 211:338–351
Israely I, Costa R, Xie C, Silva A, Kosik K, Liu X (2004) Deletion of the neuron-specific protein delta-catenin leads to severe cognitive and synaptic dysfunction. Curr Biol 14:1657–1663
Itoh M, Nagafuchi A, Moroi S, Tsukita S (1997) Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J Cell Biol 138:181–192
Jelani M, Chishti MS, Ahmad W (2011) Mutation in PVRL4 gene encoding nectin-4 underlies ectodermal-dysplasia-syndactyly syndrome (EDSS1). J Hum Genet 56:352–357
Junghans D, Hack I, Frotscher M, Taylor V, Kemler R (2005) Beta-catenin-mediated cell-adhesion is vital for embryonic forebrain development. Dev Dyn 233:528–539
Kadowaki M, Nakamura S, Machon O, Krauss S, Radice G, Takeichi M (2007) N-cadherin mediates cortical organization in the mouse brain. Dev Biol 304:22–33
Kan N, Stemmler M, Junghans D, Kanzler B, de Vries W, Dominis M, Kemler R (2007) Gene replacement reveals a specific role for E-cadherin in the formation of a functional trophectoderm. Development 134:31–41
Kanno S, Saffitz J (2001) The role of myocardial gap junctions in electrical conduction and arrhythmogenesis. Cardiovasc Pathol 10:169–177
Kioussi C, Briata P, Baek S, Rose D, Hamblet N, Herman T, Ohgi K, Lin C, Gleiberman A, Wang J, Brault V, Ruiz-Lozano P, Nguyen H, Kemler R, Glass C, Wynshaw-Boris A, Rosenfeld M (2002) Identification of a Wnt/Dvl/beta-Catenin → Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 111:673–685
Kirchhof P, Fabritz L, Zwiener M, Witt H, Schafers M, Zellerhoff S, Paul M, Athai T, Hiller K, Baba H, Breithardt G, Ruiz P, Wichter T, Levkau B (2006) Age- and training-dependent development of arrhythmogenic right ventricular cardiomyopathy in heterozygous plakoglobin-deficient mice. Circulation 114:1799–1806
Kjaer K, Hansen L, Schwabe G, Marques-de-Faria A, Eiberg H, Mundlos S, Tommerup N, Rosenberg T (2005) Distinct CDH3 mutations cause ectodermal dysplasia, ectrodactyly, macular dystrophy (EEM syndrome). J Med Genet 42:292–298
Klaus A, Saga Y, Taketo M, Tzahor E, Birchmeier W (2007) Distinct roles of Wnt/beta-catenin and Bmp signaling during early cardiogenesis. Proc Natl Acad Sci U S A 104:18531–18536
Kobielak A, Fuchs E (2006) Links between alpha-catenin, NF-kB, and squamous cell carcinoma in skin. Proc Natl Acad Sci U S A 103:2322–2327
Koster M (2010) p63 in skin development and ectodermal dysplasias. J Invest Derm 130:2352–2358
Kostetskii I, Moore R, Kemler R, Radice G (2001) Differential adhesion leads to segregation and exclusion of N-cadherin-deficient cells in chimeric embryos. Dev Biol 234:72–79
Kostetskii I, Li J, Xiong Y, Zhou R, Ferrari VA, Patel VV, Molkentin JD, Radice GL (2005) Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure. Circ Res 96:346–354
Kovtun IV, Harris KJ, Jatoi A, Jevremovic D (2011) Increased incidence of endometrioid tumors caused by aberrations in E-cadherin promoter of mismatch repair-deficient mice. Carcinogenesis 32:1085–1092
Kwon C, Arnold J, Hsiao E, Taketo M, Conklin B, Srivastava D (2007) Canonical Wnt signaling is a positive regulator of mammalian cardiac progenitors. Proc Natl Acad Sci U S A 104:10894–10899
Lallemand D, Curto M, Saotome I, Giovannini M, McClatchey AI (2003) NF2 deficiency promotes tumorigenesis and metastasis by destabilizing adherens junctions. Genes Dev 17:1090–1100
Larue L, Ohsugi M, Hirchenhain J, Kemler R (1994) E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci U S A 91:8263–8267
Lewis JE, Jensen PJ, Wheelock MJ (1994) Cadherin function is required for human keratinocytes to assemble desmosomes and stratify in response to calcium. J Invest Dermatol 102:870–877
Li J, Radice GL (2010) A new perspective on intercalated disc organization: implications for heart disease. Dermatol Res Pract 2010:207835
Li J, Patel VV, Kostetskii I, Xiong Y, Chu AF, Jacobson JT, Yu C, Morley GE, Molkentin JD, Radice GL (2005) Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ Res 97:474–481
Li J, Levin MD, Xiong Y, Petrenko N, Patel VV, Radice GL (2008) N-cadherin haploinsufficiency affects cardiac gap junctions and arrhythmic susceptibility. J Mol Cell Cardiol 44:597–606
Li X, Dong X, Luo S, Zhang B, Lee D, Ting A, Neiswender H, Kim C, Carpenter-Hyland E, Gao T, Xiong W, Mei L (2008) Retrograde regulation of motoneuron differentiation by muscle beta-catenin. Nat Neurosci 11:262–268
Li D, Liu Y, Maruyama M, Zhu W, Chen H, Zhang W, Reuter S, Lin S, Haneline L, Field L, Chen P, Shou W (2011) Restrictive loss of plakoglobin in cardiomyocytes leads to arrhythmogenic cardiomyopathy. Hum Mol Genet 20:4582–4596
Libusova L, Stemmler M, Hierholzer A, Schwarz E, Kemler R (2010) N-cadherin can structurally substitute for E-cadherin during intestinal development but leads to polyp formation. Development 137:2297–2305
Lickert H, Kutsch S, Kanzler B, Tamai Y, Taketo M, Kemler R (2002) Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm. Dev Cell 3:171–181
Liebner S, Cattelino A, Gallini R, Rudini N, Iurlaro M, Piccolo S, Dejana E (2004) Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. Cell Biol 166:359–367
Lien W, Klezovitch O, Fernandez T, Delrow J, Vasioukhin V (2006) alphaE-catenin controls cerebral cortical size by regulating the hedgehog signaling pathway. Science 311:1609–1612
Lien WH, Klezovitch O, Null M, Vasioukhin V (2008) alphaE-catenin is not a significant regulator of beta-catenin signaling in the developing mammalian brain. J Cell Sci 121:1357–1362
Lin L, Cui L, Zhou W, Dufort D, Zhang X, Cai C, Bu L, Yang L, Martin J, Kemler R, Rosenfeld M, Chen J, Evans S (2007) Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. Proc Natl Acad Sci U S A 104:9313–9318
Luo Y, Radice G (2005) N-cadherin acts upstream of VE-cadherin in controlling vascular morphogenesis. J Cell Biol 169:29–34
Luo Y, Ferreira-Cornwell M, Baldwin H, Kostetskii I, Lenox J, Lieberman M, Radice G (2001) Rescuing the N-cadherin knockout by cardiac-specific expression of N- or E-cadherin. Development 128:459–469
Luo Y, High F, Epstein J, Radice G (2006) N-cadherin is required for neural crest remodeling of the cardiac outflow tract. Dev Biol 299:517–528
Machon O, van den Bout C, Backman M, Kemler R, Krauss S (2003) Role of beta-catenin in the developing cortical and hippocampal neuroepithelium. Neuroscience 122:129–143
Maiden SL, Hardin J (2011) The secret life of alpha-catenin: moonlighting in morphogenesis. J Cell Biol 195:543–552
Majima T, Ogita H, Yamada T, Amano H, Togashi H, Sakisaka T, Tanaka-Okamoto M, Ishizaki H, Miyoshi J, Takai Y (2009) Involvement of afadin in the formation and remodeling of synapses in the hippocampus. Biochem Biophys Res Commun 385:539–544
Marose T, Merkel C, McMahon A, Carroll T (2008) Beta-catenin is necessary to keep cells of ureteric bud/Wolffian duct epithelium in a precursor state. Dev Biol 314:112–126
Matter C, Pribadi M, Liu X, Trachtenberg J (2009) Delta-catenin is required for the maintenance of neural structure and function in mature cortex in vivo. Neuron 64:320–327
McAllister A (2007) Dynamic aspects of CNS synapse formation. Annu Rev Neurosci 30:425–450
McCrea PD, Park JI (2007) Developmental functions of the P120-catenin sub-family. Biochim Biophys Acta 1773:17–33
Michels C, Buchta T, Bloch W, Krieg T, Niessen C (2009) Classical cadherins regulate desmosome formation. J Invest Derm 129:2072–2075
Miller L, Smith A, Taketo M, Lang R (2006) Optic cup and facial petterning defects in ocular ectoderm β-catenin gain-of-function mice. BMC Dev Biol 6:14
Mucenski M, Wert S, Nation J, Loudy D, Huelsken J, Birchmeier W, Morrisey E, Whitsett J (2003) beta-Catenin is required for specification of proximal/distal cell fate during lung morphogenesis. J Biol Chem 278:40231–40238
Mueller S, Rosenquist T, Takai Y, Bronson R, Wimmer E (2003) Loss of nectin-2 at Sertoli-spermatid junctions leads to male infertility and correlates with severe spermatozoan head and midpiece malformation, impaired binding to the zona pellucida, and oocyte penetration. Biol Reprod 69:1330–1340
Murtaugh L, Law A, Dor Y, Melton D (2005) Beta-catenin is essential for pancreatic acinar but not islet development. Development 132:4663–4674
Navarro P, Ruco L, Dejana E (1998) Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization. J Cell Biol 140:1475–1484
Nemade R, Bierie B, Nozawa M, Bry C, Smith G, Vasioukhin V, Fuchs E, Hennighausen L (2004) Biogenesis and function of mouse mammary epithelium depends on the presence of functional alpha-catenin. Mech Dev 121:91–99
Niessen CM, Gottardi CJ (2008) Molecular components of the adherens junction. Biochim Biophys Acta 1778:562–571
Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, Furuse M, Tsukita S (2003) Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 161:653–660
Noren NK, Liu BP, Burridge K, Kreft B (2000) p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J Cell Biol 150:567–580
Nose A, Takeichi M (1986) A novel cadherin cell adhesion molecule: its expression patterns associated with implantation and organogenesis of mouse embryos. J Cell Biol 103:2649–2658
Oas R, Xiao K, Summers S, Wittich K, Chiasson C, Martin W, Grossniklaus H, Vincent P, Reynolds A, Kowalczyk A (2010) p120-Catenin is required for mouse vascular development. Circ Res 106:941–951
Oda H, Takeichi M (2011) Evolution: structural and functional diversity of cadherin at the adherens junction. J Cell Biol 193:1137–1146
Ohtola J, Myers J, Akhtar-Zaidi B, Zuzindlak D, Sandesara P, Yeh K, Mackem S, Atit R (2008) beta-Catenin has sequential roles in the survival and specification of ventral dermis. Development 135:2321–2329
Ohyama T, Mohamed O, Taketo M, Dufort D, Groves A (2006) Wnt signals mediate a fate decision between otic placode and epidermis. Development 133:865–875
Olson L, Tollkuhn J, Scafoglio C, Krones A, Zhang J, Ohgi K, Wu W, Taketo M, Kemler R, Grosschedl R, Rose D, Li X, Rosenfeld M (2006) Homeodomain-mediated beta-catenin-dependent switching events dictate cell-lineage determination. Cell 125:593–605
Ozaki-Kuroda K, Nakanishi H, Ohta H, Tanaka H, Kurihara H, Mueller S, Irie K, Ikeda W, Sakai T, Wimmer E, Nishimune Y, Takai Y (2002) Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 12:1145–1150
Park C, Finger J, Cooper J, Ackerman S (2002) The cerebellar deficient folia (cdf) gene acts intrinsically in Purkinje cell migrations. Genesis 32:32–41
Park J, Valerius M, McMahon A (2007) Wnt/beta-catenin signaling regulates nephron induction during mouse kidney development. Development 134:2533–2539
Park J, Liu B, Chen T, Li H, Hu X, Gao J, Zhu Y, Zhu Q, Qiang B, Yuan J, Peng X, Qiu M (2008) Disruption of Nectin-like 1 cell adhesion molecule leads to delayed axonal myelination in the CNS. J Neurosci 28:12815–12819
Perez-Moreno M, Davis M, Wong E, Pasolli H, Reynolds A, Fuchs E (2006) p120-catenin mediates inflammatory responses in the skin. Cell 124:631–644
Perez-Moreno M, Song W, Pasolli H, Williams S, Fuchs E (2008) Loss of p120 catenin and links to mitotic alterations, inflammation, and skin cancer. Proc Natl Acad Sci U S A 105:15399–15404
Pieters T, van Hengel J, van Roy F (2012) Functions of p120ctn in development and disease. Front Biosci 17:760–783
Piven O, Kostetskii I, Macewicz L, Kolomiets Y, Radice G, Lukash L (2011) Requirement for N-cadherin-catenin complex in heart development. Exp Biol Med (Maywood) 236:816–822
Pontoriero G, Smith A, Miller L, Radice G, West-Mays J, Lang R (2009) Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival. Dev Biol 326:403–417
Radice G, Ferreira-Cornwell M, Robinson S, Rayburn H, Chodosh L, Takeichi M, Hynes R (1997a) Precocious mammary gland development in P-cadherin-deficient mice. J Cell Biol 139:1025–1032
Radice G, Rayburn H, Matsunami H, Knudsen K, Takeichi M, Hynes R (1997b) Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181:64–78
Reynolds A, Roczniak-Ferguson A (2004) Emerging roles for p120-catenin in cell adhesion and cancer. Oncogene 23:7947–7956
Riethmacher D, Brinkmann V, Birchmeier C (1995) A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc Natl Acad Sci U S A 92:855–859
Rodda S, McMahon A (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133:3231–3244
Ruiz P, Brinkmann V, Ledermann B, Behrend M, Grund C, Thalhammer C, Vogel F, Birchmeier C, Gtinthert U, Franke W, Birchmeier W (1996) Targeted mutation of plakoglobin in mice reveals essential functions of desmosomes in the embryonic heart. J Cell Biol 135:215–225
Satomi-Kobayashi S, Ueyama T, Mueller S, Toh R, Masano T, Sakoda T, Rikitake Y, Miyoshi J, Matsubara H, Oh H, Kawashima S, Hirata K, Takai Y (2009) Deficiency of nectin-2 leads to cardiac fibrosis and dysfunction under chronic pressure overload. Hypertension 54:825–831
Schackmann RC, van Amersfoort M, Haarhuis JH, Vlug EJ, Halim VA, Roodhart JM, Vermaat JS, Voest EE, van der Groep P, van Diest PJ, Jonkers J, Derksen PW (2011) Cytosolic p120-catenin regulates growth of metastatic lobular carcinoma through Rock1-mediated anoikis resistance. J Clin Invest 121:3176–3188
Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, Camargo FD (2011) Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144:782–795
Schneider MR, Dahlhoff M, Horst D, Hirschi B, Trulzsch K, Muller-Hocker J, Vogelmann R, Allgauer M, Gerhard M, Steininger S, Wolf E, Kolligs FT (2010) A key role for E-cadherin in intestinal homeostasis and Paneth cell maturation. PLoS One 5:e14325
Schüller U, Rowitch D (2007) Beta-catenin function is required for cerebellar morphogenesis. Brain Res 1140:161–169
Sekine S, Lan B, Bedolli M, Feng S, Hebrok M (2006) Liver-specific loss of beta-catenin blocks glutamine synthesis pathway activity and cytochrome p450 expression in mice. Hepatology 43:817–825
Sekine S, Gutiérrez P, Lan B, Feng S, Hebrok M (2007) Liver-specific loss of beta-catenin results in delayed hepatocyte proliferation after partial hepatectomy. Hepatology 45:361–368
Sheikh F, Chen Y, Liang X, Hirschy A, Stenbit A, Gu Y, Dalton N, Yajima T, Lu Y, Knowlton K, Peterson K, Perriard J, Chen J (2006) alpha-E-catenin inactivation disrupts the cardiomyocyte adherens junction, resulting in cardiomyopathy and susceptibility to wall rupture. Circulation 114:1046–1055
Shimada S, Mimata A, Sekine M, Mogushi K, Akiyama Y, Fukamachi H, Jonkers J, Tanaka H, Eishi Y, Yuasa Y (2011) Synergistic tumour suppressor activity of E-cadherin and p53 in a conditional mouse model for metastatic diffuse-type gastric cancer. Gut 61:344–353
Shimomura Y, Wajid M, Shapiro Lea (2008) P-cadherin is a p63 target gene with a crucial role in the developing human limb bud and hair follicle. Development 135:743–753
Silvis M, Kreger B, Lien W, Klezovitch O, Rudakova G, Camargo F, Lantz D, Seykora J, Vasioukhin V (2011) α-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci Signal 4:ra33
Smalley-Freed W, Efimov A, Burnett P, Short S, Davis M, Gumucio D, Washington M, Coffey R, Reynolds A (2010) p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J Clin Invest 120:1824–1835
Smith A, Miller L, Song N, Taketo M, Lang R (2005) The duality of beta-catenin function: a requirement in lens morphogenesis and signaling suppression of lens fate in periocular ectoderm. Dev Biol 285:477–489
Smith JD, Meehan MH, Crean J, McCann A (2011) Alpha T-catenin (CTNNA3): a gene in the hand is worth two in the nest. Cell Mol Life Sci 68:2493–2498
Soshnikova N, Zechner D, Huelsken J, Mishina Y, Behringer R, Taketo M, Crenshaw Er, Birchmeier W (2003) Genetic interaction between Wnt/beta-catenin and BMP receptor signaling during formation of the AER and the dorsal-ventral axis in the limb. Genes Dev 17:1963–1968
Sozen M, Suzuki K, Tolarova M, Bustos T, Fernandez Iglesias J, Spritz R (2001) Mutation of PVRL1 is associated with sporadic, non-syndromic cleft lip/palate in northern Venezuela. Nat Genet 29:141–142
Sprecher E, Bergman R, Richard G, Lurie R, Shalev S, Petronius D, Shalata A, Anbinder Y, Leibu R, Perlman I, Cohen N, Szargel R (2001) Hypotrichosis with juvenile macular dystrophy is caused by a mutation in CDH3, encoding P-cadherin. Nat Genet 29:134–136
Stairs D, Bayne L, Rhoades B, Vega M, Waldron T, Kalabis J, Klein-Szanto A, Lee J, Katz J, Diehl J, Reynolds A, Vonderheide R, Rustgi A (2011) Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a tumor suppressor gene. Cancer Cell 19:470–483
Stepniak E, Radice GL, Vasioukhin V (2009) Adhesive and signaling functions of cadherins and catenins in vertebrate development. Cold Spring Harb Perspect Biol 1:a002949
Stocker AM, Chenn A (2006) Differential expression of alpha-E-catenin and alpha-N-catenin in the developing cerebral cortex. Brain Res 1073–1074:151–158
Suzuki K, Hu D, Bustos T, Zlotogora J, Richieri-Costa A, Helms J, Spritz R (2000) Mutations of PVRL1, encoding a cell-cell adhesion molecule/herpesvirus receptor, in cleft lip/palate-ectodermal dysplasia. Nat Genet 25:427–430
Taddei A, Giampietro C, Conti A, Orsenigo F, Breviario F, Pirazzoli V, Potente M, Daly C, Dimmeler S, Dejana E (2008) Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat Cell Biol 10:923–934
Tan X, Behari J, Cieply B, Michalopoulos G, Monga S (2006) Conditional deletion of beta-catenin reveals its role in liver growth and regeneration. Gastroenterology 131:1561–1572
Tan X, Yuan Y, Zeng G, Apte U, Thompson M, Cieply B, Stolz D, Michalopoulos G, Kaestner K, Monga S (2008) Beta-catenin deletion in hepatoblasts disrupts hepatic morphogenesis and survival during mouse development. Hepatology 47:1667–1679
Tanaka-Okamoto M, Hori K, Ishizaki H, Itoh Y, Onishi S, Yonemura S, Takai Y, Miyoshi J (2011) Involvement of afadin in barrier function and homeostasis of mouse intestinal epithelia. J Cell Sci 124:2231–2240
Thoreson M, Reynolds A (2002) Altered expression of the catenin p120 in human cancer: implications for tumor progression. Differentiation 70:583–589
Tinkle C, Lechler T, Pasolli H, Fuchs E (2004) Conditional targeting of E-cadherin in skin: insights into hyperproliferative and degenerative responses. Proc Natl Acad Sci U S A 101:552–557
Tinkle C, Pasolli H, Stokes N, Fuchs E (2008) New insights into cadherin function in epidermal sheet formation and maintenance of tissue integrity. Proc Natl Acad Sci U S A 105:15405–15410
Togashi H, Abe K, Mizoguchi A, Takaoka K, Chisaka O, Takeichi M (2002) Cadherin regulates dendritic spine morphogenesis. Neuron 35:77–89
Togashi H, Kominami K, Waseda M, Komura H, Miyoshi J, Takeichi M, Takai Y (2011) Nectins establish a checkerboard-like cellular pattern in the auditory epithelium. Science 333:1144–1147
Torres M, Stoykova A, Huber O, Chowdhury K, Bonaldo P, Mansouri A, Butz S, Kemler R, Gruss P (1997) An alpha-E-catenin gene trap mutation defines its function in preimplantation development. Proc Natl Acad Sci U S A 94:901–906
Tunggal J, Helfrich I, Schmitz A, Schwarz H, Gunzel D, Fromm M, Kemler R, Krieg T, Niessen C (2005) E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J 24:1146–1156
Uchida N, Shimamura K, Miyatani S, Copeland N, Gilbert D, Jenkins N, Takeichi M (1994) Mouse alpha N-catenin: two isoforms, specific expression in the nervous system, and chromosomal localization of the gene. Dev Biol 163:75–85
Uemura M, Takeichi M (2006) Alpha N-catenin deficiency causes defects in axon migration and nuclear organization in restricted regions of the mouse brain. Dev Dyn 235:2559–2566
van Hengel J, van Roy F (2007) Diverse functions of p120ctn in tumors. Biochim Biophys Acta 1773:78–88
Vasioukhin V, Bauer C, Yin M, Fuchs E (2000) Directed actin polymerization is the driving force for epithelial cell--cell adhesion. Cell 100:209–219
Vasioukhin V, Bauer C, Degenstein L, Wise B, Fuchs E (2001) Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin. Cell 104:605–617
Wakamatsu K, Ogita H, Okabe N, Irie K, Tanaka-Okamoto M, Ishizaki H, Ishida-Yamamoto A, Takai Y (2007) Up-regulation of loricrin expression by cell adhesion molecule nectin-1 through Rap1-ERK signaling in keratinocytes. J Biol Chem 282:18173–18181
Wells J, Esni F, Boivin G, Aronow B, Stuart W, Combs C, Sklenka A, Leach S, Lowy A (2007) Wnt/beta-catenin signaling is required for development of the exocrine pancreas. BMC Dev Biol 7:4
Wong AS, Gumbiner BM (2003) Adhesion-independent mechanism for suppression of tumor cell invasion by E-cadherin. J Cell Biol 161:1191–1203
Xiao K, Garner J, Buckley K, Vincent P, Chiasson C, Dejana E, Faundez V, Kowalczyk A (2005) p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin. Mol Biol Cell 16:5141–5151
Xu W, Baribault H, Adamson E (1998) Vinculin knockout results in heart and brain defects during embryonic development. Development 125:327–337
Yang A, Zhu Z, Kapranov P, McKeon F, Church G, Gingeras T, Struhl K (2006) Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol Cell 24:593–602
Yin Y, White A, Huh S, Hilton M, Kanazawa H, Long F, Ornitz D (2008) An FGF-WNT gene regulatory network controls lung mesenchyme development. Dev Biol 319:426–436
Yonemura S (2011) Cadherin-actin interactions at adherens junctions. Curr Opin Cell Biol 23:515–522
Yoshida T, Miyoshi J, Takai Y, Thesleff I (2010) Cooperation of nectin-1 and nectin-3 is required for normal ameloblast function and crown shape development in mouse teeth. Dev Dyn 239:2558–2569
Young P, Boussadia O, Berger P, Leone D, Charnay P, Kemler R, Suter U (2002) E-cadherin is required for the correct formation of autotypic adherens junctions of the outer mesaxon but not for the integrity of myelinated fibers of peripheral nerves. Mol Cell Neurosci 21:341–351
Young P, Boussadia O, Halfter H, Grose R, Berger P, Leone D, Robenek H, Charnay P, Kemler R, Suter U (2003) E-cadherin controls adherens junctions in the epidermis and the renewal of hair follicles. EMBO J 22:5723–5733
Zamora M, Männer J, Ruiz-Lozano P (2007) Epicardium-derived progenitor cells require beta-catenin for coronary artery formation. Proc Natl Acad Sci U S A 104:18109–18114
Zechner D, Fujita Y, Hülsken J, Müller T, Walther I, Taketo M, Crenshaw Er, Birchmeier W, Birchmeier C (2003) beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol 258:406–418
Zemljic-Harpf A, Ponrartana S, Avalos R, Jordan M, Roos K, Dalton N, Phan V, Adamson E, Ross R (2004) Heterozygous inactivation of the vinculin gene predisposes to stress-induced cardiomyopathy. Am J Pathol 165:1033–1044
Zemljic-Harpf A, Miller J, Henderson S, Wright A, Manso A, Elsherif L, Dalton N, Thor A, Perkins G, McCulloch A, Ross R (2007) Cardiac-myocyte-specific excision of the vinculin gene disrupts cellular junctions, causing sudden death or dilated cardiomyopathy. Mol Cell Biol 27:7522–7537
Zhadanov A, Provance DJ, Speer C, Coffin J, Goss D, Blixt J, Reichert C, Mercer J (1999) Absence of the tight junctional protein AF-6 disrupts epithelial cell-cell junctions and cell polarity during mouse development. Curr Biol 9:880–888
Zhang J, Woodhead GJ, Swaminathan SK, Noles SR, McQuinn ER, Pisarek AJ, Stocker AM, Mutch CA, Funatsu N, Chenn A (2010) Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of beta-catenin signaling. Dev Cell 18:472–479
Zhao C, Blum J, Chen A, Kwon H, Jung S, Cook J, Lagoo A, Reya T (2007) Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 12:528–541
Zhou J, Liyanage U, Medina M, Ho C, Simmons A, Lovett M, Kosik K (1997) Presenilin 1 interaction in the brain with a novel member of the Armadillo family. Neuroreport 8:2085–2090
Zhou J, Qu J, Yi X, Graber K, Huber L, Wang X, Gerdes A, Li F (2007) Upregulation of gamma-catenin compensates for the loss of beta-catenin in adult cardiomyocytes. Am J Physiol Heart Circ Physiol 292:270–276
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Boggetti, B., Niessen, C.M. (2012). Adherens Junctions in Mammalian Development, Homeostasis and Disease: Lessons from Mice. In: Harris, T. (eds) Adherens Junctions: from Molecular Mechanisms to Tissue Development and Disease. Subcellular Biochemistry, vol 60. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4186-7_14
Download citation
DOI: https://doi.org/10.1007/978-94-007-4186-7_14
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-4185-0
Online ISBN: 978-94-007-4186-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)