Occludin confers adhesiveness when expressed in fibroblasts

C.M. Van Itallie; J.M. Anderson

Summary

Occludin is an integral membrane protein specifically associated with tight junctions. Previous studies suggest it is likely to function in forming the intercellular seal. In the present study, we expressed occludin under an inducible promotor in occludin-null fibroblasts to determine whether this protein confers intercellular adhesion. When human occludin is stably expressed in NRK and Rat-1 fibroblasts, which lack endogenous occludin and tight junctions but do have well developed ZO-1-containing adherens-like junctions, occludin colocalizes with ZO-1 to points of cell-cell contact. In contrast, L-cell fibroblasts which lack cadherin-based adherens junctions, target neither ZO-1 nor occludin to sites of cell contact. Occludin-induced adhesion was next quantified using a suspended cell assay. In NRK and Rat-1 cells, occludin expression induces adhesion in the absence of calcium, thus independent of cadherin-cadherin contacts. In contrast, L-cells are nonadhesive in this assay and show no increase in adhesion after induction of occludin expression. Binding of an antibody to the first of the putative extracellular loops of occludin confirmed that this sequence was exposed on the cell surface, and synthetic peptides containing the amino acid sequence of this loop inhibit adhesion induced by occludin expression. These results suggest that the extracellular surface of occludin is directly involved in cell-cell adhesion and the ability to confer adhesiveness correlates with the ability to colocalize with its cytoplasmic binding protein, ZO-1.

REFERENCES

1. Anderson J. M. and
2. Van Itallie C. M.
(1995). Tight junctions and the molecular basis for regulation of paracellular permeability. Am. J Physiol 269, 467–.
OpenUrl
1. Ando-Akatsuka Y.,
2. Saitou M.,
3. Hirase T.,
4. Kishi M.,
5. Sakakibara A.,
6. Itoh M.,
7. Yonemura S.,
8. Furuse M. and
9. Tsukita S.
(1996). Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. J. Cell Biol 133, 43–47
OpenUrl Abstract/FREE Full Text
1. Angres B.,
2. Barth A. and
3. Nelson W. J.
(1996). Mechanism for transition from initial to stable cell-cell adhesion: kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay. J. Cell Biol 134, 1–10
OpenUrl Abstract/FREE Full Text
1. Balda M. S.,
2. Whitney J. A.,
3. Flores C.,
4. Gonzalez S.,
5. Cereijido M. and
6. Matter K.
(1996). Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J. Cell Biol 134, 1031–1049
OpenUrl Abstract/FREE Full Text
1. Blaschuk O. W.,
2. Sullivan R.,
3. David S. and
4. Pouliot Y.
(1990). Identification of a cadherin cell adhesion recognition sequence. Dev. Biol 139, 227–229
OpenUrl CrossRef PubMed Web of Science
1. Chen C. A. and
2. Okayama A.
(1988). Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques 6, 632–638
OpenUrl PubMed Web of Science
1. Citi S.,
2. Sabannay H.,
3. Jakes R.,
4. Geiger B. and
5. Kendrich-Jones J.
(1988). Cingulin, a new peripheral component of tight junctions. Nature 333, 272–275
OpenUrl CrossRef PubMed Web of Science
1. Dehar S. and
2. Hannigan G. E.
(1996). Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr. Opin. Cell Biol 8, 657–669
OpenUrl CrossRef PubMed Web of Science
1. Dragsten P. R.,
2. Blumenthal R. and
3. Handler J. S.
(1981). Membrane asymmetry in epithelia: is the tight junction a barrier to diffusion in the plasma membrane?. Nature 294, 718–722
OpenUrl CrossRef PubMed
1. Fallon M. B.,
2. Brecher A.,
3. Balda M. S.,
4. Matter K. and
5. Anderson J. M.
(1995). Altered expression and localization of the tight junction proteins occludin and ZO-1 after common bile duct ligation. Am. J. Physiol 260, 1057–.
OpenUrl
1. Fujimoto K.
(1995). Freeze fracture replica electronmicroscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J. Cell Sci 108, 3443–3449
OpenUrl Abstract/FREE Full Text
1. Furuse M.,
2. Hirase T.,
3. Itoh M.,
4. Nagafuchi A.,
5. Yonemura S. and
6. Tsukita S.
(1993). Occludin: A novel integral membrane protein localizing at tight junctions. J. Cell Biol 123, 1777–1788
OpenUrl Abstract/FREE Full Text
1. Furuse M.,
2. Itoh M.,
3. Hirase T.,
4. Nagafuchi A.,
5. Yonemura S.,
6. Tsukita S. and
7. Tsukita S.
(1994). Direct association between occludin and ZO-1 andits possible involvement in the localization of occludin at tight junctions. J. Cell Biol 127, 1617–1626
OpenUrl Abstract/FREE Full Text
1. Furuse M.,
2. Fujimoto K.,
3. Sato N.,
4. Hirase T. and
5. Tsukita S.
(1996). Overexpression of occludin, a tight junction-associated integral membrane protein, induces the formation of intracellular multilamellar bodies bearing tight junction-like structures. J. Cell Sci 109, 429–435
OpenUrl Abstract/FREE Full Text
1. Gumbiner B.,
2. Lowenkopf T. and
3. Apatira D.
(1991). Identification of 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc. Nat. Acad. Sci. USA 88, 3460–3464
OpenUrl Abstract/FREE Full Text
1. Keon B. H.,
2. Schafer S.,
3. Kuhn C.,
4. Grund C. and
5. Franke W. W.
(1996). Symplekin, a novel type of tight junction plaque protein. J. Cell Biol 134, 1003–1017
OpenUrl Abstract/FREE Full Text
1. Laemmli U. K.
(1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685
OpenUrl CrossRef PubMed Web of Science
1. McCarthy K. M.,
2. Skare I. B.,
3. Stankewich M. D.,
4. Furuse M.,
5. Tsukita S.,
6. Rogers R. A.,
7. Lynch R. D. and
8. Schneeberger E. E.
(1996). Occludin is a functional component of the tight junction. J. Cell Sci 109, 2287–2298
OpenUrl Abstract/FREE Full Text
1. Peluso J. J.,
2. Pappalardo A. and
3. Trolice M. P.
(1996). N-Cadherin-mediated cell contact inhibits granulosa cell apoptosis in a progesterone-independent manner. Endocrinology 137, 1196–1203
OpenUrl CrossRef PubMed Web of Science
1. Rajasekaran A. K.,
2. Hojo M.,
3. Huima T. and
4. Rodriguez-Boulan E.
(1996). Catenin and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J. Cell Biol 132, 451–463
OpenUrl Abstract/FREE Full Text
1. Roy N.,
2. Mahadevan M. S.,
3. McLean M.,
4. Shutler G.,
5. Yaraghi Z.,
6. Farahani R.,
7. Baird S.,
8. Besner-Johnston A.,
9. Lefebvre C.,
10. Kang X. and
11. et al.
(1995). The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80, 167–178
OpenUrl CrossRef PubMed Web of Science
1. Staehelin L. A.
(1973). Further observations of the fine structure of freeze-cleaved tight junctions. J. Cell Sci 13, 763–786
OpenUrl Abstract/FREE Full Text
1. Stevenson B. R.,
2. Silicano J. D.,
3. Mooseker M. and
4. Goodenough D. A.
(1986). Identification of ZO-1: A high molecular weight polypeptideassociated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol 103, 755–766
OpenUrl Abstract/FREE Full Text
1. Towbin H.,
2. Staelin T. and
3. Gordon J.
(1979). Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Nat. Acad. Sci. USA 76, 44350–4354
OpenUrl
1. van Meer G. and
2. Simons K.
(1986). The function of tight junctions in maintaining differences in lipid composition between the apical and the basolateral cell surface domains of MDCK cells. EMBO J 5, 1455–1464
OpenUrl PubMed Web of Science
1. Warner A.,
2. Clements D. K.,
3. Parikh S.,
4. Evans W. H. and
5. DeHaan R. L.
(1995). Specific motifs in the external loops of connexin proteins can determine gap junction formation between chick heart myocytes. J. Physiol 488, 721–728
OpenUrl PubMed Web of Science
1. Weber E.,
2. Berta G.,
3. Tousson A.,
4. St John P.,
5. Green M. W.,
6. Gopalokrishnan U.,
7. Jilling T.,
8. Sorscher E. J.,
9. Elton T. S.,
10. Abrahamson D. R. and
11. Kirk K. L.
(1994). Expression and polarized targeting of a Rab3 isoform in epithelial cells. J. Cell Biol 125, 583–594
OpenUrl Abstract/FREE Full Text
1. Wesseling J.,
2. van der Valk S. W. and
3. Hilkens J.
(1996). A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membrane-associated mucin episialin/MUC1. Mol. Biol. Cell 7, 565–577
OpenUrl Abstract/FREE Full Text
1. Wong V. and
2. Gumbiner B.
(1997). A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J. Cell Biol 136, 399–410
OpenUrl Abstract/FREE Full Text
1. Yonemura S.,
2. Itoh M.,
3. Nagafuchi A. and
4. Tsukita S.
(1995). Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells. J. Cell Sci 108, 127–142
OpenUrl Abstract/FREE Full Text
1. Zhong Y.,
2. Saitoh T.,
3. Minase T.,
4. Sawada N.,
5. Enomoto K. and
6. Mori M.
(1993). Monoclonal antibody 7H6 reacts with a novel tight junction-associated protein distinct from ZO-1, cingulin and ZO-2. J. Cell Biol 120, 477–483
OpenUrl Abstract/FREE Full Text

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[1] Anderson J. M. and
Van Itallie C. M.
(1995). Tight junctions and the molecular basis for regulation of paracellular permeability. Am. J Physiol 269, 467–.
OpenUrl

[2] Anderson J. M. and

[3] Van Itallie C. M.

[4] Ando-Akatsuka Y.,
Saitou M.,
Hirase T.,
Kishi M.,
Sakakibara A.,
Itoh M.,
Yonemura S.,
Furuse M. and
Tsukita S.
(1996). Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. J. Cell Biol 133, 43–47
OpenUrl Abstract/FREE Full Text

[5] Ando-Akatsuka Y.,

[6] Saitou M.,

[7] Hirase T.,

[8] Kishi M.,

[9] Sakakibara A.,

[10] Itoh M.,

[11] Yonemura S.,

[12] Furuse M. and

[13] Tsukita S.

[14] Angres B.,
Barth A. and
Nelson W. J.
(1996). Mechanism for transition from initial to stable cell-cell adhesion: kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay. J. Cell Biol 134, 1–10
OpenUrl Abstract/FREE Full Text

[15] Angres B.,

[16] Barth A. and

[17] Nelson W. J.

[18] Balda M. S.,
Whitney J. A.,
Flores C.,
Gonzalez S.,
Cereijido M. and
Matter K.
(1996). Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J. Cell Biol 134, 1031–1049
OpenUrl Abstract/FREE Full Text

[19] Balda M. S.,

[20] Whitney J. A.,

[21] Flores C.,

[22] Gonzalez S.,

[23] Cereijido M. and

[24] Matter K.

[25] Blaschuk O. W.,
Sullivan R.,
David S. and
Pouliot Y.
(1990). Identification of a cadherin cell adhesion recognition sequence. Dev. Biol 139, 227–229
OpenUrl CrossRef PubMed Web of Science

[26] Blaschuk O. W.,

[27] Sullivan R.,

[28] David S. and

[29] Pouliot Y.

[30] Chen C. A. and
Okayama A.
(1988). Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques 6, 632–638
OpenUrl PubMed Web of Science

[31] Chen C. A. and

[32] Okayama A.

[33] Citi S.,
Sabannay H.,
Jakes R.,
Geiger B. and
Kendrich-Jones J.
(1988). Cingulin, a new peripheral component of tight junctions. Nature 333, 272–275
OpenUrl CrossRef PubMed Web of Science

[34] Citi S.,

[35] Sabannay H.,

[36] Jakes R.,

[37] Geiger B. and

[38] Kendrich-Jones J.

[39] Dehar S. and
Hannigan G. E.
(1996). Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr. Opin. Cell Biol 8, 657–669
OpenUrl CrossRef PubMed Web of Science

[40] Dehar S. and

[41] Hannigan G. E.

[42] Dragsten P. R.,
Blumenthal R. and
Handler J. S.
(1981). Membrane asymmetry in epithelia: is the tight junction a barrier to diffusion in the plasma membrane?. Nature 294, 718–722
OpenUrl CrossRef PubMed

[43] Dragsten P. R.,

[44] Blumenthal R. and

[45] Handler J. S.

[46] Fallon M. B.,
Brecher A.,
Balda M. S.,
Matter K. and
Anderson J. M.
(1995). Altered expression and localization of the tight junction proteins occludin and ZO-1 after common bile duct ligation. Am. J. Physiol 260, 1057–.
OpenUrl

[47] Fallon M. B.,

[48] Brecher A.,

[49] Balda M. S.,

[50] Matter K. and

[51] Anderson J. M.

[52] Fujimoto K.
(1995). Freeze fracture replica electronmicroscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J. Cell Sci 108, 3443–3449
OpenUrl Abstract/FREE Full Text

[53] Fujimoto K.

[54] Furuse M.,
Hirase T.,
Itoh M.,
Nagafuchi A.,
Yonemura S. and
Tsukita S.
(1993). Occludin: A novel integral membrane protein localizing at tight junctions. J. Cell Biol 123, 1777–1788
OpenUrl Abstract/FREE Full Text

[55] Furuse M.,

[56] Hirase T.,

[57] Itoh M.,

[58] Nagafuchi A.,

[59] Yonemura S. and

[60] Tsukita S.

[61] Furuse M.,
Itoh M.,
Hirase T.,
Nagafuchi A.,
Yonemura S.,
Tsukita S. and
Tsukita S.
(1994). Direct association between occludin and ZO-1 andits possible involvement in the localization of occludin at tight junctions. J. Cell Biol 127, 1617–1626
OpenUrl Abstract/FREE Full Text

[62] Furuse M.,

[63] Itoh M.,

[64] Hirase T.,

[65] Nagafuchi A.,

[66] Yonemura S.,

[67] Tsukita S. and

[68] Tsukita S.

[69] Furuse M.,
Fujimoto K.,
Sato N.,
Hirase T. and
Tsukita S.
(1996). Overexpression of occludin, a tight junction-associated integral membrane protein, induces the formation of intracellular multilamellar bodies bearing tight junction-like structures. J. Cell Sci 109, 429–435
OpenUrl Abstract/FREE Full Text

[70] Furuse M.,

[71] Fujimoto K.,

[72] Sato N.,

[73] Hirase T. and

[74] Tsukita S.

[75] Gumbiner B.,
Lowenkopf T. and
Apatira D.
(1991). Identification of 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc. Nat. Acad. Sci. USA 88, 3460–3464
OpenUrl Abstract/FREE Full Text

[76] Gumbiner B.,

[77] Lowenkopf T. and

[78] Apatira D.

[79] Keon B. H.,
Schafer S.,
Kuhn C.,
Grund C. and
Franke W. W.
(1996). Symplekin, a novel type of tight junction plaque protein. J. Cell Biol 134, 1003–1017
OpenUrl Abstract/FREE Full Text

[80] Keon B. H.,

[81] Schafer S.,

[82] Kuhn C.,

[83] Grund C. and

[84] Franke W. W.

[85] Laemmli U. K.
(1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685
OpenUrl CrossRef PubMed Web of Science

[86] Laemmli U. K.

[87] McCarthy K. M.,
Skare I. B.,
Stankewich M. D.,
Furuse M.,
Tsukita S.,
Rogers R. A.,
Lynch R. D. and
Schneeberger E. E.
(1996). Occludin is a functional component of the tight junction. J. Cell Sci 109, 2287–2298
OpenUrl Abstract/FREE Full Text

[88] McCarthy K. M.,

[89] Skare I. B.,

[90] Stankewich M. D.,

[91] Furuse M.,

[92] Tsukita S.,

[93] Rogers R. A.,

[94] Lynch R. D. and

[95] Schneeberger E. E.

[96] Peluso J. J.,
Pappalardo A. and
Trolice M. P.
(1996). N-Cadherin-mediated cell contact inhibits granulosa cell apoptosis in a progesterone-independent manner. Endocrinology 137, 1196–1203
OpenUrl CrossRef PubMed Web of Science

[97] Peluso J. J.,

[98] Pappalardo A. and

[99] Trolice M. P.

[100] Rajasekaran A. K.,
Hojo M.,
Huima T. and
Rodriguez-Boulan E.
(1996). Catenin and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J. Cell Biol 132, 451–463
OpenUrl Abstract/FREE Full Text

[101] Rajasekaran A. K.,

[102] Hojo M.,

[103] Huima T. and

[104] Rodriguez-Boulan E.

[105] Roy N.,
Mahadevan M. S.,
McLean M.,
Shutler G.,
Yaraghi Z.,
Farahani R.,
Baird S.,
Besner-Johnston A.,
Lefebvre C.,
Kang X. and
et al.
(1995). The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80, 167–178
OpenUrl CrossRef PubMed Web of Science

[106] Roy N.,

[107] Mahadevan M. S.,

[108] McLean M.,

[109] Shutler G.,

[110] Yaraghi Z.,

[111] Farahani R.,

[112] Baird S.,

[113] Besner-Johnston A.,

[114] Lefebvre C.,

[115] Kang X. and

[116] et al.

[117] Staehelin L. A.
(1973). Further observations of the fine structure of freeze-cleaved tight junctions. J. Cell Sci 13, 763–786
OpenUrl Abstract/FREE Full Text

[118] Staehelin L. A.

[119] Stevenson B. R.,
Silicano J. D.,
Mooseker M. and
Goodenough D. A.
(1986). Identification of ZO-1: A high molecular weight polypeptideassociated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol 103, 755–766
OpenUrl Abstract/FREE Full Text

[120] Stevenson B. R.,

[121] Silicano J. D.,

[122] Mooseker M. and

[123] Goodenough D. A.

[124] Towbin H.,
Staelin T. and
Gordon J.
(1979). Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Nat. Acad. Sci. USA 76, 44350–4354
OpenUrl

[125] Towbin H.,

[126] Staelin T. and

[127] Gordon J.

[128] van Meer G. and
Simons K.
(1986). The function of tight junctions in maintaining differences in lipid composition between the apical and the basolateral cell surface domains of MDCK cells. EMBO J 5, 1455–1464
OpenUrl PubMed Web of Science

[129] van Meer G. and

[130] Simons K.

[131] Warner A.,
Clements D. K.,
Parikh S.,
Evans W. H. and
DeHaan R. L.
(1995). Specific motifs in the external loops of connexin proteins can determine gap junction formation between chick heart myocytes. J. Physiol 488, 721–728
OpenUrl PubMed Web of Science

[132] Warner A.,

[133] Clements D. K.,

[134] Parikh S.,

[135] Evans W. H. and

[136] DeHaan R. L.

[137] Weber E.,
Berta G.,
Tousson A.,
St John P.,
Green M. W.,
Gopalokrishnan U.,
Jilling T.,
Sorscher E. J.,
Elton T. S.,
Abrahamson D. R. and
Kirk K. L.
(1994). Expression and polarized targeting of a Rab3 isoform in epithelial cells. J. Cell Biol 125, 583–594
OpenUrl Abstract/FREE Full Text

[138] Weber E.,

[139] Berta G.,

[140] Tousson A.,

[141] St John P.,

[142] Green M. W.,

[143] Gopalokrishnan U.,

[144] Jilling T.,

[145] Sorscher E. J.,

[146] Elton T. S.,

[147] Abrahamson D. R. and

[148] Kirk K. L.

[149] Wesseling J.,
van der Valk S. W. and
Hilkens J.
(1996). A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membrane-associated mucin episialin/MUC1. Mol. Biol. Cell 7, 565–577
OpenUrl Abstract/FREE Full Text

[150] Wesseling J.,

[151] van der Valk S. W. and

[152] Hilkens J.

[153] Wong V. and
Gumbiner B.
(1997). A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J. Cell Biol 136, 399–410
OpenUrl Abstract/FREE Full Text

[154] Wong V. and

[155] Gumbiner B.

[156] Yonemura S.,
Itoh M.,
Nagafuchi A. and
Tsukita S.
(1995). Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells. J. Cell Sci 108, 127–142
OpenUrl Abstract/FREE Full Text

[157] Yonemura S.,

[158] Itoh M.,

[159] Nagafuchi A. and

[160] Tsukita S.

[161] Zhong Y.,
Saitoh T.,
Minase T.,
Sawada N.,
Enomoto K. and
Mori M.
(1993). Monoclonal antibody 7H6 reacts with a novel tight junction-associated protein distinct from ZO-1, cingulin and ZO-2. J. Cell Biol 120, 477–483
OpenUrl Abstract/FREE Full Text

[162] Zhong Y.,

[163] Saitoh T.,

[164] Minase T.,

[165] Sawada N.,

[166] Enomoto K. and

[167] Mori M.

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Introducing FocalPlane’s new Community Manager, Esperanza Agullo-Pascual

New funding scheme supports sustainable events

Read & Publish participation continues to grow

Cell scientist to watch: Romain Levayer

Live lactating mammary tissue

JCS and COVID-19

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Search

Summary

REFERENCES

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Related articles

Cited by...

More in this TOC section

Similar articles

Other journals from The Company of Biologists

Introducing FocalPlane’s new Community Manager, Esperanza Agullo-Pascual

New funding scheme supports sustainable events

Read & Publish participation continues to grow

Cell scientist to watch: Romain Levayer

Live lactating mammary tissue

JCS and COVID-19