Skip to main content
SpringerLink
Log in

Tight Junctions during Development

  • Chapter
Tight Junctions

Abstract

During early development, tight junction biogenesis and the differentiation of the first epithelium in the blastocyst is critical for embryonic patterning and organization. Here, we discuss the programme of exactly timed transcription, translation, and post-translational modification of specific junctional proteins that regulates the stepwise membrane assembly of tight junctions during cleavage in the mouse model. Underlying mechanisms that coordinate these processes are discussed along with newly emerging data from other mammalian species. In the mouse embryo, junction assembly follows the establishment of cell polarity at the 8-cell stage and is characterized by sequential membrane delivery of JAM-1, ZO-1α− and Rab13, cingulin and ZO-2 followed by ZO-1α+ and occludin. Tight junction assembly occurs over three developmental stages; compaction, first differentiative division and cavitation. Post-translational modification of occludin, the late expression of ZO-1α+ isoform and their intracellular colocalisation may all contribute to the rapid coordinated delivery of these two proteins to the membrane, resulting in the final sealing of the tight junction followed by blastocoel cavitation. This coordinated delivery of these two tight junction-associated proteins may therefore provide a rate limiting step for the sealing of tight junctions and regulated timing of blastocoel cavitation. Taken together, our studies in mouse, human and bovine embryos suggest that defects in the tightly controlled programming of early development may contribute to reduced embryo viability.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 1991; 251:1451–1455.

    PubMed  CAS  Google Scholar 

  2. McCrea PD, Brieher WM, Gumbiner B. Induction of a secondary body axis in xenopus by antibodies to beta catenin. J Cell Biol 1993; 123:477–484.

    PubMed  CAS  Google Scholar 

  3. Aberle H, Schwartz H, Kemler R. Cadherin-catenin complex: Protein interactions and their implications for cadherin function. J Cell Biochem 1996; 61(4):514–523.

    PubMed  CAS  Google Scholar 

  4. Fleming TP, Papenbrock T, Fesenko I et al. Assembly of tight junctions during early vertebrate development. Semin Cell Dev Biol 2000; 11(4):291–299.

    PubMed  CAS  Google Scholar 

  5. Johnson MH, Ziomek CA. The foundation of two distinct cell lineages within the mouse morula. Cell 1981; 24:71–80.

    PubMed  CAS  Google Scholar 

  6. Fleming TP. A quantitative analysis of cell allocation to trophectoderm and inner cell mass in the mouse blastocyst. Dev Biol 1987; 119:520–531.

    PubMed  CAS  Google Scholar 

  7. DiZio SM, Tasca RJ. Sodium-dependent aminoacid transport in preimplantation embryos. III. Na+,K+,-ATPase linked mechanism in blastocysts. Dev Biol 1977; 59:198–205.

    PubMed  CAS  Google Scholar 

  8. Vorbrodt A, Konwinski M, Solter D et al. Ultrastructural cytochemistryof membrane-bound phosphatases in preimplantation mouse embryos. Dev Biol 1977; 55:117–134.

    PubMed  CAS  Google Scholar 

  9. Watson AJ, Kidder GM. Immunofluorescence assessment of the timing of appearance and cellular distribution of Na/K-ATPase during mouse embryogenesis. Dev Biol 1988; 126:80–90.

    PubMed  CAS  Google Scholar 

  10. MacPhee DJ, Barr KJ, DeSousa PA et al. Regulation of Na+,K+-ATPase alpha subunit gene expression during mouse preimplantation development. Dev Biol 1994; 162:259–266.

    PubMed  CAS  Google Scholar 

  11. MacPhee DJ, Jones DH, Barr KJ et al. Differential involvement of Na(+), K(+)-ATPase isozymes in preimplantation development. Dev Biol 2000; 222:486–498.

    PubMed  CAS  Google Scholar 

  12. Jones DH, Davies TC, Kidder GM. Embryonic expression of the putative gamma subunit of the sodium pump is required for aquisition of fluid transport capacity during mouse blastocyst development. J Cell Biol 1997; 139:1545–1552.

    PubMed  CAS  Google Scholar 

  13. Fleming TP, Pickering SJ. Maturation and polarisation of the endocytotic system in outside blastomeres during mouse preimplantation embryos. J Embryol Exp Morphol 1985; 89:175–208.

    PubMed  CAS  Google Scholar 

  14. Heyner S, Rao LV, Jarett L et al. Preimplantation mouse embryos internalize maternal insulin via receptor-mediated endocytosis: Pattern uptake and functional correlations. Dev Biol 1989; 134:48–58.

    PubMed  CAS  Google Scholar 

  15. Manejwala FM, Cragoe EJ, Schultz RM. Blastocoel expansion in the preimplantation mouse embryo: A role for extracellular sodium and chloride and possible apical routes of their entry. Dev Biol 1986; 133:210–220.

    Google Scholar 

  16. Dardik A, Schultz RM. Protein secretion by the mouse blastocyst: Differences in the polypeptide composition secreted into the bastocoel and medium. Biol Reprod 1991; 45:328–333.

    PubMed  CAS  Google Scholar 

  17. Wiley LM, Lever JE, Pape C et al. Antibodies to a renal Na+/glucose cotransport systemlocalize to the apical membrane domain of polar mouse embryo blastomeres. Dev Biol 1991; 143:149–161.

    PubMed  CAS  Google Scholar 

  18. Aghayan M, Rao LV, Smith RM et al. Developmental expression and cellular localization of glucose transporter molecules during mouse preimplantation development. Development 1992; 115:305–312.

    PubMed  CAS  Google Scholar 

  19. Hewitson LC, Leese HJ. Energy metabolism of the trophectoderm and inner cell mass of the mouse blastocyst. J Exp Zool 1993; 267:337–343.

    PubMed  CAS  Google Scholar 

  20. Brison DR, Hewitson LC, Leese HJ. Glucose, pyruvate and lactate concentrations in the blastocoel cavity of rat and mouse embryos. Mol Reprod Dev 1993; 35:272–232.

    Google Scholar 

  21. Smith RM, Garside WT, Aghayan M et al. Mouse preimplantation embryos exhibit receptor-mediated binding and transcytosis of maternal insulin-like growth factor I. Biol Reprod 1993; 49:1–12.

    PubMed  CAS  Google Scholar 

  22. Barr KJ, Garrill A, Jones DH et al. Contributions of Na+/H+ exchanger isoforms to preimplantation development of the mouse. Reprod Dev 1998; 50:146–153.

    CAS  Google Scholar 

  23. Offenberg H, Barcroft LC, Caveney A et al. mRNAs encoding aquaporins are present during murine preimplantation development. Mol Reprod Dev 2000; 57(4):323–330.

    PubMed  CAS  Google Scholar 

  24. Watson AJ, Barcroft LC. Regulation of blastocyst formation. Front Biosci 2001; 6:D708–D730.

    PubMed  CAS  Google Scholar 

  25. Rossant J, Chazaud C, Yamanaka Y. Lineage allocation and asymmetries in the early mouse embryo. Philos Trans R Soc Lond B Biol Sci 2003; 358:1341–1349.

    PubMed  CAS  Google Scholar 

  26. Ducibella T, Albertini DF, Anderson E et al. The preimplantation mammalian embryo: Characterization of intercellular junctions and their appearance during development. Dev Biol 1975; 45:231–250.

    PubMed  CAS  Google Scholar 

  27. Magnuson T, Demsey A, Stackpole CW. Characterization of intercellular junctions in the preimplantation embryo by freeze-fracture and thin-section electron microscopy. Dev Biol 1977; 61:252–261.

    PubMed  CAS  Google Scholar 

  28. Vestweber D, Gossler A, Boller K et al. Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev Biol 1987; 124:451–456.

    PubMed  CAS  Google Scholar 

  29. Ohsugi M, Hwang S, Butz S et al. Expression and cell membrane localisationof catenins during mouse preimplantation development. Dev Dyn 1996; 206:391–402.

    PubMed  CAS  Google Scholar 

  30. Handyside AH. 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.

    PubMed  CAS  Google Scholar 

  31. Ziomek CA, Johnson MH. Cell surface interactions induce polarisation of mouse 8-cell blastomeres at compaction. Cell 1980; 21:935–942.

    PubMed  CAS  Google Scholar 

  32. Reeve WJ, Ziomek CA. Distribution of microvilli on dissociated blastomeres from mouse embryos: Evidence for surface polarisation at compaction. J Embryol Exp Morphol 1981; 62:339–350.

    PubMed  CAS  Google Scholar 

  33. Johnson MH, Maro B. The distribution of cytoplasmic actin in mouse 8-cell blastomeres. J Embryol Exp Morphol 1984; 82:97–117.

    PubMed  CAS  Google Scholar 

  34. Houliston E, Pickering SJ, Maro B. Redistribution of microtubules and pericentriole material during the development of polarity in mouse blastomeres. J Cell Biol 1987; 104:1299–1308.

    PubMed  CAS  Google Scholar 

  35. Johnson MH, Maro B, Takeichi M. The role of cell adhesion in the synchronisation and orientation of polarisation in 8-cell mouse blastomeres. J Embryol Exp Morphol 1986; 93:239–255.

    PubMed  CAS  Google Scholar 

  36. Matter K, Balda MS. Signalling to and from tight junctions. Nature Reviews 2003; 4:225–236.

    PubMed  CAS  Google Scholar 

  37. D’Atri F, Citi S. Molecular complexity of vertebrate tight junctions. Mol Membr Biol 2002; 19:103–112.

    PubMed  CAS  Google Scholar 

  38. Gonzalez-Mariscal L, Betanzos A, Nava P et al. Tight junction proteins. Prog Biophys Mol Biol 2003; 81:1–44.

    PubMed  CAS  Google Scholar 

  39. Stevenson BR, Siliciano JD, Mooseker MS et al. 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(3):755–766.

    PubMed  CAS  Google Scholar 

  40. Anderson JM, Stevenson BR, Jesaitis LA et al. Characterization of ZO-1, a protein component of the tight junction from mouse liver and Madin-Darby canine kidney cells. J Cell Biol 1988; 106(4):1141–1149.

    PubMed  CAS  Google Scholar 

  41. Itoh M, Nagafuchi A, Yonemura S et al. The 220-kD protein colocalizing with cadherins in nonepithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J Cell Biol 1993; 121(3):491–502.

    PubMed  CAS  Google Scholar 

  42. Willott E, Balda MS, Fanning AS et al. The tight junction protein ZO-1 is homologous to the Drosophila discs-large tumor suppressor protein of septate junctions. Proc Natl Acad Sci USA 1993; 90(16):7834–7838.

    PubMed  CAS  Google Scholar 

  43. Fleming TP, McConnell J, Johnson MH et al. 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(4):1407–1418.

    PubMed  CAS  Google Scholar 

  44. Gonzalez-Mariscal L, Betanzos A, Avila-Flores A. MAGUK proteins: Structure and role in the tight junction. Semin Cell Dev Biol 2000; 11(4):315–324.

    PubMed  CAS  Google Scholar 

  45. Willott E, Balda MS, Heintzelman M et al. Localization and differential expression of two isoforms of the tight junction protein ZO-1. Am J Physiol 1992; 262(5 Pt 1):C1119–C1124.

    PubMed  CAS  Google Scholar 

  46. Balda MS, Anderson JM. Two classes of tight junctions are revealed by ZO-1 isoforms. Am J Physiol 1993; 264(4 Pt 1):C918–C924.

    PubMed  CAS  Google Scholar 

  47. Sheth B, Fesenko I, Collins JE et al. Tight junction assembly during mouse blastocyst formation is regulated by late expression of ZO-1 alpha+ isoform. Development 1997; 124(10):2027–2037.

    PubMed  CAS  Google Scholar 

  48. Novick P, Zettl KS. The diversity of rab proteins in vesicle transport. Curr Opin Cell Biol 1997; 9:496–504.

    PubMed  CAS  Google Scholar 

  49. Chavrier P, Gour BJ. The role of ARF and rab GTPases in membrane transport. Curr Opin Cell Biol 1999; 11:466–475.

    PubMed  CAS  Google Scholar 

  50. Zahraoui A, Louvard D, Galli T. Tight junction, a platform for trafficking and signaling protein complexes. J Cell Biol 2000; 151(5):F31–F36.

    PubMed  CAS  Google Scholar 

  51. Zahraoui A, Joberty G, Arpin M et al. A small rab GTPase is distributed in cytoplasmic vesicles in non polarized cells but colocalizes with the tight junction marker ZO-1 in polarized epithelial cells. J Cell Biol 1994; 124(1–2):101–115.

    PubMed  CAS  Google Scholar 

  52. Marzesco AM, Dunia I, Pandjaitan R et al. The small GTPase Rab13 regulates assembly of functional tight junctions in epithelial cells. Mol Cell Biol 2002;13:1819–1831.

    CAS  Google Scholar 

  53. Sheth B, Fontaine JJ, Ponza E et al. 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.

    PubMed  CAS  Google Scholar 

  54. Joberty G, Tavitian A, Zahraoui A. Isoprenylation of rab proteins possessing a C-terminal CaaX motif. FEBS Lett 1993;330:323–328.

    PubMed  CAS  Google Scholar 

  55. Marzesco AM, Galli T, Louvard D et al. The rod cGMP phosphodiesterase δ subunit dissociates the small GTPase rab13 from membranes. J Biol Chem 1998;273:22340–22345.

    PubMed  CAS  Google Scholar 

  56. Bazzoni G. The JAM family of junctional adhesion molecules. Curr Opin Cell Biol 2003;15:525–530.

    PubMed  CAS  Google Scholar 

  57. Martin-Padura I, Lostaglio S, Schneemann M et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 1998; 142(1):117–127.

    PubMed  CAS  Google Scholar 

  58. Thomas FC, Sheth B, Eckert JJ et al. Contribution of JAM-1 to epithelial differentiation and tight junction biogenesis in mouse pre-implantation embryo. J Cell Sci 2004;117:5599–5608.

    PubMed  CAS  Google Scholar 

  59. Martinez-Estrada OM, Villa A, Breviario F et al. Association of junctional adhesion molecule with calcium/calmodulin-dependent serine protein kinase (CASK/Lin-2) in human epithelial Caco2 cells. J Biol Chem 2001;276:9291–9296.

    PubMed  CAS  Google Scholar 

  60. Bazzoni G, Martinez-Estrada OM, Orsenigo F et al. Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and occludin. J Biol Chem 2000;275(27):20520–20526.

    PubMed  CAS  Google Scholar 

  61. Citi S, Sabanay H, Jakes R et al. Cingulin, a new peripheral component of tight junctions. Nature 1988;333(6170):272–276.

    PubMed  CAS  Google Scholar 

  62. Citi S, Sabanay H, Kendrick-Jones J et al. Cingulin: Characterization and localization. J Cell Sci 1989;93 (Pt l):107–122.

    PubMed  CAS  Google Scholar 

  63. Cordenonsi M, D’Atri F, Hammar E et al. Cingulin contains globular and coiled-coil domains and interacts with ZO-1, ZO-2 and myosin. J Cell Biol 1999;147:1569–1582.

    PubMed  CAS  Google Scholar 

  64. Fleming TP, Hay M, Javed Q et al. Localisation of tight junction protein cingulin is temporally and spatially regulated during early mouse development. Development 1993;117(3):1135–1144.

    PubMed  CAS  Google Scholar 

  65. Javed Q, Fleming TP, Hay M et al. Tight junction protein cingulin is expressed by maternal and embryonic genomes during early mouse development. Development 1993;117(3):1145–1151.

    PubMed  CAS  Google Scholar 

  66. Nowak RL, Sheth B, Fleming TP. Expression of the tight junction protein, ZO-2 in mouse preimplantation embryos. Mol Biol Cell 2000;11S:512a.

    Google Scholar 

  67. Gumbiner B, Lowenkopf T, Apatira D. Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc Natl Acad Sci USA 1991;88(8):3460–3464.

    PubMed  CAS  Google Scholar 

  68. Balda MS, Gonzalez-Mariscal L, Matter K et al. Assembly of the tight junction: The role of diacylglycerol. J Cell Biol 1993;123(2):293–302.

    PubMed  CAS  Google Scholar 

  69. Wittchen ES, Haskins J, Stevenson BR. 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(49):35179–35185.

    PubMed  CAS  Google Scholar 

  70. Islas S, Vega J, Ponce L et al. Nuclear localization of the tight junction protein ZO-2 in epithelial cells. Exp Cell Res 2002;274(1):138–148.

    PubMed  CAS  Google Scholar 

  71. Traweger A, Fuchs R, Krizbai IA et al. The tight junction protein ZO-2 localizes to the nucleus and interacts with the heterogeneous nuclear ribonucleoprotein scaffold attachment factor-B. J Biol Chem 2003;278(4):2692–2700.

    PubMed  CAS  Google Scholar 

  72. Fleming TP, Sheth B, Fesenko I. Cell adhesion in the preimplantation mammalian embryo and its role in trophectoderm differentiation and blastocyst morphogenesis. Front Biosci 2001;6:D1000–D1007.

    PubMed  CAS  Google Scholar 

  73. Furuse M, Hirase T, Itoh M et al. Occludin: A novel integral membrane protein localising at tight junctions. Journal of Cell Biology 1993;123(6(2)):1777–1788.

    PubMed  CAS  Google Scholar 

  74. Morita K, Furuse M, Fujimoto K et al. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA 1999;96(2):511–516.

    PubMed  CAS  Google Scholar 

  75. Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Biol 2001;2:285–293.

    CAS  Google Scholar 

  76. Sheth B, Moran B, Anderson JM et al. 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(4):831–840.

    PubMed  CAS  Google Scholar 

  77. Cordenonsi M, Mazzon E, De Rigo L et al. Occludin dephosphorylation in early development of xenopus laevis. J Cell Sci 1997;110 ( Pt 24):3131–3139.

    PubMed  CAS  Google Scholar 

  78. Sakakibara A, Furuse M, Saitou M et al. Possible involvement of phosphorylation of occludin in tight junction formation. J Cell Biol 1997;137(6):1393–1401.

    PubMed  CAS  Google Scholar 

  79. Wong V. Phosphorylation of occludin correlates with occludin localization and function at the tight junction. Am J Physiol 1997;273(6 Pt 1):C1859–C1867.

    PubMed  CAS  Google Scholar 

  80. Furuse M, Fujita K, Hiragi T et al. Claudin-1 and-2: Novel integral membrane proteins localising at tight junctions with no sequence similarity to occludin. Journal of Cell Biology 1998;141:1539–1550.

    PubMed  CAS  Google Scholar 

  81. Magnuson T, Jacobson JB, Stackpole CW. Relationship between intercellular permeability and junction organisation in the preimplantation mouse embryo. Developmental Biology 1978;67:214–224.

    PubMed  CAS  Google Scholar 

  82. Furuse M, Itoh M, Hirase T et al. Direct association of occludin with ZO-1 and its possible involvement in the localisation of occludin at tight junction. J Cell Biol 1994;127:1617–1626.

    PubMed  CAS  Google Scholar 

  83. Cordenonsi M, Turco F, D’Atri F et al. Xenopus laevis occludin. Identification of in vitro phosphorylation sites by protein kinase CK2 and its association with cingulin. Eur J Biochem 1999;264:374–384.

    PubMed  CAS  Google Scholar 

  84. Rajasekaran AK, Hojo M, Huima T et al. Catenins and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J Cell Biol 1996;132(3):451–463.

    PubMed  CAS  Google Scholar 

  85. Larue L, Ohsugi M, Hierchenhain J et al. E-cadherin null mutants fail to form a trophectoderm epithelium. Proc Natl Acad Sci USA 1994;91:8263–8267.

    PubMed  CAS  Google Scholar 

  86. Reithmacher DBV, Birchmeier C. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc Nad Acad Sci USA 1995;92:855–859.

    Google Scholar 

  87. Torres M, Stoykova A, Huber O et al. An a-E-catenin gene trap mutation defines its function in preimplantation development. Proc Nad Acad Sci USA 1997;94:901–906.

    CAS  Google Scholar 

  88. Ohsugi M, Larue L, Schwartz H et al. Cell-junctional and cytoskeletal organisation in mouse blastocysts lacking E-cadhern. Dev Biol 1997;185:261–271.

    PubMed  CAS  Google Scholar 

  89. Sefton M, Johnson MH, Clayton L. Synthesis and phosphorylation of uvomorulin during mouse early development. Development 1992;115:313–318.

    PubMed  CAS  Google Scholar 

  90. Winkel GK, Ferguson JE, Takeichi M et al. Activation of protein kinase C triggers premature compaction in the 4-cell stage mouse embryo. Dev Biol 1990;138:1–15.

    PubMed  CAS  Google Scholar 

  91. Pauken CM, Capco DG. Regulation of cell adhesion during embryonic compaction of mammalian embryos: Roles for PKC and β-catenin. Mol Reprod Dev 1999;54:135–144.

    PubMed  CAS  Google Scholar 

  92. Dodane V, Kachar B. Identification of isoforms of G proteins and PKC that colocalize with tight junctions. J Membr Biol 1996;149(3):199–209.

    PubMed  CAS  Google Scholar 

  93. Izumi Y, Hirose T, Tamai Y et al. An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J Cell Biol 1998;143(1):95–106.

    PubMed  CAS  Google Scholar 

  94. Balda MS, Anderson JM, Matter K. The SH3 domain of the tight junction protein ZO-1 binds to a serine protein kinase that phosphorylates a region C-terminal to this domain. FEBS Lett 1996;399(3):326–332.

    PubMed  CAS  Google Scholar 

  95. Pauken CM, Capco DG. The expression and stage-specific localisation of protein kinase C isotypes during mouse preimplantation development. Dev Biol 2000;223:411–421.

    PubMed  CAS  Google Scholar 

  96. Eckert JJ, McCallum A, Mears A et al. Specific PKC isoforms regulate blastocoel formation during mouse pre-implantation development. Dev Biol 2004;274:384–401.

    PubMed  CAS  Google Scholar 

  97. Etienne-Manneville S, Hall A. Rho-GTPases in cell biology. Nature 2002;420:629–635.

    PubMed  CAS  Google Scholar 

  98. Benais-Pont G, Punn A, Flores-Maldonado C et al. Identification of a tight junction-associated guanine nudeotide exchange factor that activates Rho and regulates paracellular permeability. J Cell Biol 2003;160(5):729–740.

    PubMed  CAS  Google Scholar 

  99. Reima I, Lehtonen E, Virtanen I et al. The cytoskeleton and associated proteins during cleavage, compaction and blastocyst differentiation in the pig. Differentiation 1993;54:35–45.

    PubMed  CAS  Google Scholar 

  100. Barcroft LC, Hay-Schmidt A, Caveney A et al. Trophectoderm differentiation in the bovine embryo: Characterization of a polarized epithelium. J Reprod Fertil 1998;114(2):327–339.

    PubMed  CAS  Google Scholar 

  101. Bloor DJ, Metcalfe AD, Rutherford A et al. Expression of cell adhesion molecules during human preimplantation embryo development. Mol Hum Reprod 2002;8(3):237–245.

    PubMed  CAS  Google Scholar 

  102. Nikas G, Ao A, Winston RM et al. Compaction and surface polarity in the human embryo. Biol Reprod 1996;55:32–37.

    PubMed  CAS  Google Scholar 

  103. Miller DJ, Eckert JJ, Lazzari G et al. Tight junction messenger RNA expression levels in bovine embryos are dependent upon the ability to compact and in vitro culture methods. Biol Reprod 2003;68(4):1394–1402.

    PubMed  CAS  Google Scholar 

  104. Ghassemirar MR, Eckert JJ, Houghton FD et al. Gene expression regulating epithelial intercellular junction biogenesis during human blastocyst development in vitro. Mol Hum Reprod 2003;9(5):245–252.

    Google Scholar 

  105. Ghassemirar MR, Sheth B, Papenbrock T et al. Occludin TM4(-): An isoform of the tight junction protein present in primates lacking the fourth transmembrane domain. J Cell Sci 2002;115 (Pt 15):3171–3180.

    Google Scholar 

  106. Eckert JJ, Houghton FD, Fleming TP. Impaired assembly of junctional proteins in human embryos may be regulated by specific PKC isoforms. Theriogenology 2002;57:635.

    Google Scholar 

  107. Eckert JJ, McCallum A, Rumsby MG et al. Protein kinase C isotypes are differentially involved in the biogenesis of the mouse blastocyst. Theriogenology 2001;55:319.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biological Sciences, University of Southampton, Southampton, UK

    Bhavwanti Sheth, Fay Thomas & Tom P. Fleming

  2. Developmental Origins of Health and Disease School of Medicine, University of Southampton, Southampton, UK

    Judith Eckert

Authors
  1. Bhavwanti Sheth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Judith Eckert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fay Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tom P. Fleming
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Sheth, B., Eckert, J., Thomas, F., Fleming, T.P. (2006). Tight Junctions during Development. In: Tight Junctions. Springer, Boston, MA. https://doi.org/10.1007/0-387-36673-3_12

Download citation

Publish with us

Policies and ethics

Search

Navigation