Subscribe to RSS
Please copy the URL and add it into your RSS Feed Reader.
https://www.thieme-connect.de/rss/thieme/en/10.1055-s-00000072.xml
Download PDF
Semin Reprod Med 2000; 18(2): 185-194
DOI: 10.1055/s-2000-12557
DOI: 10.1055/s-2000-12557
Junctional Complexes in the Early Mammalian Embryo
Further Information
Publication History
Publication Date:
31 December 2000 (online)
ABSTRACT
Preimplantation embryos generate intercellular junctions during differentiation of the trophectoderm epithelium and the formation of the blastocyst. These membrane complexes comprise gap junctions, adherens junctions, tight junctions, and desmosomes, each performing fundamental roles in cellular communication, adhesion, and differentiation. The mouse embryo has been used as a model for the biogenesis of cell junctions. Their construction is achieved by temporally regulated gene expression programs. Mechanisms of junction membrane assembly include the timing of transcription, translation, and posttranslational modifications of specific junctional proteins. Human embryos exhibit similar expression programs, and defects in these programs may contribute to reduced embryo viability.
KEYWORD
junctions - blastocyst
REFERENCES
- 1 Simon A M, Goodenough D A. Diverse functions of vertebrate gap junctions. Trends Cell Biol . 1998; 8 477-483
- 2 Barron D J, Valdimarrson G, Paul D L, Kidder G M. Connexin32, a gap junction protein, is a persistent oogenetic product through preimplantation development in the mouse. Dev Genet . 1989; 10 318-323
- 3 Valdimarrson G, De Sousa A P, Beyer E C, Paul D L, Kidder G M. Zygotic expression of the connexin43 gene supplies subunits for gap junction assembly during mouse preimplantation development. Mol Reprod Dev . 1991; 30 18-26
- 4 De Sousa A P, Valdimarsson G, Nicholson B J, Kidder G M. Connexin trafficking and the control of gap junction assembly in mouse preimplantation embryos. Development . 1993; 117 1355-1367
- 5 Davies T C, Barr K J, Jones D H, Zhu D, Kidder G M. Multiple members of the connexin gene family participate in preimplantation development of the mouse. Dev Genet . 1996; 18 234-243
- 6 Lo C W, Gilula N B. Gap junctional communication in the preimplantation mouse embryo. Cell . 1979; 18 399-409
- 7 Goodall H, Johnson M H. The nature of intercellular coupling within the preimplantation mouse embryo. J Embryol Exp Morphol . 1984; 79 53-76
- 8 McLachlin J R, Kidder G M. Intercellular junctional coupling in preimplantation mouse embryos: effect of blocking transcription or translation. Dev Biol . 1986; 117 146-155
- 9 Valdimarsson G, Kidder G M. Temporal control of gap junction assembly in preimplantation mouse embryos. J Cell Sci . 1995; 108 1715-1722
- 10 Ogawa H, Oyamada M, Mori T, Mori M, Shimizu H. Relationship of gap junction formation to phosphorylation of connexin43 in mouse preimplantation embryos. Mol Reprod Dev . 2000; 55 393-398
- 11 Lee S, Gilula N B, Warner A E. Gap junctional communication and compaction during preimplantation stages of mouse development. Cell . 1987; 51 851-860
- 12 Becker D K, Evans W H, Green C R, Warner A. Functional analysis of amino acid sequences in connexin43 involved in intercellular communication through gap junctions. J Cell Sci . 1995; 108 1455-1467
- 13 Buehr M, Lee S, McLaren A, Warner A. Reduced gap junctional communication is associated with the lethal condition characteristic of DDK mouse eggs fertilized by foreign sperm. Development . 1987; 101 449-459
- 14 Leclerc C, Becker D, Buehr M, Warner A. Low intracellular pH is involved in the early embryonic death of DDK mouse eggs fertilized by alien sperm. Dev Dyn . 1994; 200 257-267
- 15 De Sousa A P, Juneja S C, Caveney S. Normal development of preimplantation mouse embryos deficient in gap junctional coupling. J Cell Sci . 1997; 110 1751-1758
- 16 Houghton F D, Thonnissen E, Kidder G M, Naus C CG, Willecke K, Winterhager E. Doubly mutant mice, deficient in connexin32 and -43, show normal prenatal development of organs where the two gap junction proteins are expressed in the same cells. Dev Genet . 1999; 24 5-12
- 17 Vance M M, Wiley L M. Gap junction intercellular communication mediates the competitive cell proliferation disadvantage of irradiated mouse preimplantation embryos in aggregation chimeras. Radiat Res . 1999; 152 544-551
- 18 Boni R, Tosti E, Roviello S, Dale B. Intercellular communication in in vivo- and in vitro-produced bovine embryos. Biol Reprod . 1999; 61 1050-1055
- 19 Wrenzycki C, Herrmann D, Carnwath J W, Niemann H. Expression of the gap junction gene connexin43 (Cx43) in preimplantation bovine embryos derived in vitro or in vivo. J Reprod Fertil . 1996; 108 17-24
- 20 Niemann H, Wrenzycki C. Alterations of expression of developmentally important genes in preimplantation bovine embryos by in vitro culture conditions: implications for subsequent development. Theriogenology . 2000; 53 21-34
- 21 Dale B, Gualtieri R, Talevi R, Tosti E, Santella L, Elder K. Intercellular communication in the early human embryo. Mol Reprod Dev . 1991; 29 22-28
- 22 Hardy K, Warner A, Winston R M, Becker D L. Expression of intercellular junctions during preimplantation development of the human embryo. Mol Hum Reprod . 1996; 2 621-632
- 23 Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science . 1991; 251 1451-1455
- 24 McCrea P D, Brieher W M, Gumbiner B. Induction of a secondary body axis in Xenopus by antibodies to β-catenin. J Cell Biol . 1993; 123 477-484
- 25 Yeaman C, Grindstaff K K, Nelson W J. New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol Rev . 1999; 79 73-98
- 26 Ozawa M, Baribault H, Kemler R. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J . 1989; 8 1711-1717
- 27 McCrea P D, Turck C W, Gumbiner B. A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science . 1991; 254 1359-1361
- 28 Staddon J M, Smales C, Schulze C, Esch F S, Rubin L L. p120, a p120-related protein (p100), and the cadherin/catenin complex. J Cell Biol . 1995; 130 369-381
- 29 Hirano S, Nose A, Hatta K, Kawakami A, Takeichi M. Calcium-dependent cell-cell adhesion molecules (cadherins): subclass specificities and possible involvement of actin bundles. J Cell Biol . 1987; 105 2501-2510
- 30 Rimm D L, Koslov E R, Kebriaei P, Cianci C D, Morrow J S. Alpha 1(E)-catenin in an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc Natl Acad Sci U S A . 1995; 92 8813-8817
- 31 Aberle H, Schwartz H, Kemler R. Cadherin-catenin complex: protein interactions and their implications for cadherin function. J Cell Biochem . 1996; 61 514-523
- 32 Vestweber D, Gossler A, Boller K, Kemler R. Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev Biol . 1987; 124 451-456
- 33 Johnson M H, Maro B, Takeichi M. The role of cell adhesion in the synchronisation and orientation of polarization in 8-cell mouse blastomeres. J Embryol Exp Morphol . 1986; 93 239-255
- 34 Sefton M, Johnson M H, Clayton L. Synthesis and phosphorylation of uvomorulin during mouse early development. Development . 1992; 115 313-318
- 35 Ohsugi M, Hwang S Y, Butz S, Knowles B B, Solter D, Kemler R. Expression and cell membrane localization of catenins during mouse preimplantation development. Dev Dyn . 1996; 206 391-402
- 36 Winkel G K, Ferguson J E, Takeichi M, Nuccitelli R. Activation of protein kinase C triggers premature compaction in the four-cell stage mouse embryo. Dev Biol . 1990; 138 1-15
- 37 Pauken C M, Capco D G. Regulation of cell adhesion during embryonic compaction of mammalian embryos: roles for PKC and β-catenin. Mol Reprod Dev . 1999; 54 135-144
- 38 Sefton M, Johnson M H, Clayton L, McConnell J M. Experimental manipulations of compaction and their effects on the phosphorylation of uvomorulin. Mol Reprod Dev . 1996; 44 77-87
- 39 Ohsugi M, Butz S, Kemler R. β-catenin is a major tyrosine-phosphorylated protein during mouse oocyte maturation and preimplantation development. Dev Dyn . 1999; 216 168-176
- 40 Goval J J, Alexandre H. Effect of genistein on the temporal coordination of cleavage and compaction in mouse preimplantation embryos. Eur J Morphol . 2000; 38 88-96
- 41 Kabir N, Yamamura H, Takagishi Y, Inouye M, Oda S, Hidaka H. Regulation of preimplantation development of mouse embryos: effects of inhibition of myosin light-chain kinase, a Ca2+/calmodulin-dependent enzyme. J Exp Zool . 1996; 274 101-110
- 42 Larue L, Ohsugi M, Hirchenhain J, Kemler R. E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci U S A . 1994; 91 8263-8267
- 43 Riethmacher D, Brinkmann V, Birchmeier C. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc Natl Acad Sci U S A . 1995; 92 855-859
- 44 Wianny F, Zernicka-Goetz M. Specific interference with gene function by double-stranded RNA in early mouse development. Nat Cell Biol . 2000; 2 70-75
- 45 Torres M, Stoykova A, Huber O. An α-E-catenin gene trap mutation defines its function in preimplantation development. Proc Natl Acad Sci U S A . 1997; 94 901-906
- 46 Ziomek C A, Johnson M H. Cell surface interactions induce polarisation of mouse 8-cell blastomeres at compaction. Cell . 1980; 21 935-942
- 47 Handyside A H. Distribution of antibody- and lectin-binding sites on dissociated blastomeres of mouse morulae: evidence for polarization at compaction. J Embryol Exp Morphol . 1980; 60 99-116
- 48 Johnson M H, Maro B. The distribution of cytoplasmic actin in mouse 8-cell blastomeres. J Embryol Exp Morphol . 1984; 82 97-117
- 49 Fleming T P, Pickering S J. Maturation and polarisation of the endocytotic system in outside blastomeres during mouse preimplantation development. J Embryol Exp Morphol . 1985; 89 175-208
- 50 Houliston E, Pickering S J, Maro B. Redistribution of microtubules and pericentriolar material during the development of polarity in mouse blastomeres. J Cell Biol . 1987; 104 1299-1308
- 51 Clayton L, Hall A, Johnson M H. A role for rho-like GTPases in the polarisation of mouse eight-cell blastomeres. Dev Biol . 1999; 205 322-331
- 52 Johnson M H, Ziomek C A. The foundation of two distinct cell lineages within mouse morula. Cell . 1981; 24 71-80
- 53 Fleming T P. A quantitative analysis of cell allocation to trophectoderm and inner cell mass in the mouse blastocyst. Dev Biol . 1987; 119 520-531
- 54 Barcroft L C, Hay-Schmidt A, Caveney A. Trophectoderm differentiation in the bovine embryo: characterization of a polarized epithelium. J Reprod Fertil . 1998; 114 327-339
- 55 Reima I, Lehtonen E, Virtanen I, Flechon J E. The cytoskeleton and associated proteins during cleavage, compaction and blastocyst differentiation in the pig. Differentiation . 1993; 54 35-45
- 56 Plante L, King W A. Light and electron microscopic analysis of bovine embryos derived by in vitro and in vivo fertilization. J Assist Reprod Genet . 1994; 11 515-529
- 57 Walker S K, Hartwich K M, Seamark R F. The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenology . 1996; 45 111-120
- 58 Van Soom A, Boerjan M L, Bols P E. Timing of compaction and inner cell allocation in bovine embryos produced in vivo after superovulation. Biol Reprod . 1997; 57 1041-1049
- 59 Campbell S, Swann H R, Seif M W, Kimber S J, Aplin J D. Cell adhesion molecules on the oocyte and preimplantation human embryo. Hum Reprod . 1995; 10 1571-1578
- 60 Rufas O, Fisch B, Ziv S, Shalgi R. Expression of cadherin adhesion molecules on human gametes. Mol Hum Reprod . 2000; 6 163-169
- 61 Nikas G, Ao A, Winston R M, Handyside A H. Compaction and surface polarity in the human embryo in vitro. Biol Reprod . 1996; 55 32-37
- 62 Stevenson B R, Keon B H. The tight junction: morphology to molecules. Annu Rev Cell Dev Biol . 1998; 14 89-109
- 63 Furuse M, Hirase T, Itoh M. Occludin: a novel integral membrane protein localising at tight junctions. J Cell Biol . 1993; 123 1777-1788
- 64 Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol . 1998; 141 1539-1550
- 65 Morita K, Furuse M, Fujimoto K, Tsukita S. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci U S A . 1999; 96 511-516
- 66 McCarthy K M, Skare I B, Stankewich M C. Occludin is a functional component of the tight junction. J Cell Sci . 1996; 109 2287-2298
- 67 Van Itallie M C, Anderson J M. Occludin confers adhesiveness when expressed in fibroblasts. J Cell Sci . 1997; 110 1113-1121
- 68 Wong V, Gumbiner B M. A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J Cell Biol . 1997; 136 399-409
- 69 Stevenson B R, Siliciano J D, Mooseker M S, Goodenough D A. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol . 1986; 103 755-766
- 70 Citi S, Sabanay H, Jakes R, Geiger B, Kendrick-Jones J. Cingulin: a new peripheral component of tight junctions. Nature . 1988; 333 272-276
- 71 Willott E, Balda M S, Fanning A S, Jameson B, Van Itallie C, Anderson J M. The tight junction protein ZO-1 is homologous to the Drosophila discs-large tumor suppressor protein of septate junctions. Proc Natl Acad Sci U S A . 1993; 90 7834-7838
- 72 Furuse M, Itoh M, Hirase T. Direct association of occludin with ZO-1 and its possible involvement in the localisation of occludin at tight junctions. J Cell Biol . 1994; 127 1617-1626
- 73 Beatch M, Jesaitis L A, Gallin W J, Goodenough D A, Stevenson B R. The tight junction protein ZO-2 contains three PDZ (PSD-95/Discs-Large/ZO-1) domains and an alternatively spliced region. J Biol Chem . 1996; 271 25723-25726
- 74 Cordenonsi M, D'Atri F, Hammar E. Cingulin contains globular and coiled-coil domains and interacts with ZO-1, ZO-2, ZO-3, and myosin. J Cell Biol . 1999; 147 1569-1582
- 75 Cordenonsi M, Turco F, D'Atri F. Xenopus laevis occludin: identification of in vitro phosphorylation sites by protein kinase CK2 and association with cingulin. Eur J Biochem . 1999; 264 374-384
- 76 Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2 and ZO-3, with the COOH termini of claudins. J Cell Biol . 1999; 147 1351-1363
- 77 Fanning A S, Jameson B J, Jesaitis L A, Anderson J M. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem . 1998; 273 29745-29753
- 78 Wittchen E S, Haskins J, Stevenson B R. Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3. J Biol Chem . 1999; 274 35179-35185
- 79 Anderson J M. Cell signalling: MAGUK magic. Curr Biol . 1996; 6 382-384
- 80 Balda M S, Anderson J M. Two classes of tight junctions are revealed by ZO-1 isoforms. Am J Physiol . 1993; 264 C918-C924
- 81 Fleming T P, McConnell J, Johnson M H, Stevenson B R. Development of tight junctions de novo in the mouse early embryo: control of assembly of the tight junction-specific protein, ZO-1. J Cell Biol . 1989; 108 1407-1418
- 82 Ohsugi M, Larue L, Schwarz H, Kemler R. Cell-junctional and cytoskeletal organization in mouse blastocysts lacking E-cadherin. Dev Biol . 1997; 185 261-271
- 83 Javed Q, Fleming T P, Hay M, Citi S. Tight junction protein cingulin is expressed by maternal and embryonic genomes during early mouse development. Development . 1993; 117 1145-1151
- 84 Sheth B, Fesenko I, Collins J E. Tight junction assembly during mouse blastocyst formation is regulated by late expression of ZO-1α+ isoform. Development . 1997; 124 2027-2037
- 85 Sheth B, Fontaine J-J, Ponza E. Differentiation of the epithelial apical junctional complex during mouse preimplantation development: a role for rab13 in the early maturation of the tight junction. Mech Dev . 2000; 97 93-104
- 86 Novick P, Zerial M. The diversity of rab proteins in vesicle transport. Curr Opin Cell Biol . 1997; 9 496-504
- 87 Chavrier P, Goud B. The role of ARF and rab GTPases in membrane transport. Curr Opin Cell Biol . 1999; 11 466-475
- 88 Zahraoui A, Joberty G, Arpin M. A small rab GTPase is distributed in cytoplasmic vesicles in non-polarised cells but colocalised with the tight junction marker ZO-1 in polarised epithelial cells. J Cell Biol . 1994; 124 101-115
- 89 Fleming T P, Hay M, Javed Q, Citi S. Localisation of tight junction protein cingulin is temporally and spatially regulated during early mouse development. Development . 1993; 117 1135-1144
- 90 Sheth B, Moran B, Anderson B M, Fleming T P. Post-translational control of occludin membrane assembly in mouse trophectoderm: a mechanism to regulate timing of tight junction biogenesis and blastocyst formation. Development . 2000; 127 831-840
- 91 Rajasekaran A K, Hojo M, Huima T, Rodgiguez-Boulan E. Catenins and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J Cell Biol . 1996; 132 451-463
- 92 Ando-Akatsuka Y, Yonemura S, Itoh M, Furuse M, Tsukita S. Differential behavior of E-cadherin and occludin in their colocalization with ZO-1 during the establishment of epithelial cell polarity. J Cell Physiol . 1999; 179 115-125
- 93 Tesarik J. Involvement of oocyte-coded message in cell differentiation control of early human embryos. Development . 1989; 105 317-322
- 94 Gualtieri R, Santella L, Dale B. Tight junctions and cavitation in the human pre-embryo. Mol Reprod Dev . 1992; 32 81-87
- 95 Garrod D, Chidgey M, North A. Desmosomes: differentiation, development, dynamics and disease. Curr Opin Cell Biol . 1996; 8 670-678
- 96 Collins J E, Legan P K, Kenny T P, MacGarvie J, Holton J L, Garrod D R. Cloning and sequence analysis of desmosomal glycoproteins 2 and 3 (desmocollins): cadherin-like desmosomal adhesion molecules with heterogeneous cytoplasmic domains. J Cell Biol . 1991; 113 381-391
- 97 Fleming T P, Garrod D R, Elsmore A J. Desmosome biogenesis in the mouse preimplantation embryo. Development . 1991; 112 527-539
- 98 Collins J E, Lorimer J E, Garrod D R, Pidsley S C, Buxton R S, Fleming T P. Regulation of desmocollin transcription in mouse preimplantation embryos. Development . 1995; 121 743-753
- 99 Hardy K, Warner A, Winston R M, Becker D L. Expression of intercellular junctions during preimplantation development of the human embryo. Mol Hum Reprod . 1996; 2 621-632