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Journal of Histochemistry and Cytochemistry, Vol. 49, 333-340, March 2001, Copyright © 2001, The Histochemical Society, Inc.

ARTICLE

Occludin and Claudin-1 Concentrate in the Midbody of Immortalized Mouse Hepatocytes During Cell Division

Takashi Kojimaa, Yasuo Kokaib, Hideki Chibab, Makoto Osanaib, Kazuhide Kuwaharab, Michio Morib, Yohichi Mochizukia, and Norimasa Sawadab
a Department of Pathology, Cancer Research Institute, Sapporo Medical University School of Medicine, Sapporo, Japan
b Department of Pathology, Sapporo Medical University School of Medicine, Sapporo, Japan

Correspondence to: Takashi Kojima, Dept. of Pathology, Cancer Research Inst., Sapporo Medical Univ. School of Medicine, S1, W17, Sapporo 060-8556, Japan. E-mail: ktakashi@sapmed.ac.jp


*   Summary
*Top
 *Summary
*Introduction
 *Materials and Methods
 *Results
 *Discussion
 *Literature Cited

It has been believed that epithelial cells maintain tight junctions at all times, including during cell division, to provide a continuous epithelial seal. However, changes in localization of integral tight junction proteins during cell division have not been examined. In this study, using SV40-immortalized mouse hepatocytes transfected with human Cx32 cDNA, in which tight junction strands and the endogenous tight junction proteins occludin, claudin-1, ZO-1, and ZO-2 were induced, we examined changes in localization of the tight junction proteins at all stages of cell division. All tight junction proteins were present between mitotic cells and neighboring cells throughout cell division. In late telophase, the integral tight junction proteins occludin and claudin-1, but not the cytoplasmic proteins ZO-1 and ZO-2, were concentrated in the midbody between the daughter cells and were observed at cell borders between the daugher and neighboring cells. These results indicate that the integral tight junction proteins are regulated in a different manner from the cytoplasmic proteins ZO-1 and ZO-2 during cytokinesis. (J Histochem Cytochem 49:333–339, 2001)

Key Words: connexin 32, occludin, claudin-1, ZO-1, ZO-2, midbody, mitosis


*   Introduction
*Top
 *Summary
 *Introduction
*Materials and Methods
 *Results
 *Discussion
 *Literature Cited

Tight junctions, the most apical component of intercellular junctional complexes, separate the apical from the basolateral cell surface domains to establish cell polarity (performing the function of a fence). They also provide a barrier function, inhibiting solute and water flow through the paracellular space (Schneeberger and Lynch 1992 Down; Gumbiner 1993 Down). Tight junctions show a particular net-like meshwork of fibrils (Staehelin 1973 Down) formed by the integral membrane proteins occludin (Furuse et al. 1993 Down), the claudin family (Furuse et al. 1998 Down; Morita et al. 1999 Down), and JAM (Martin-Padura et al. 1998 Down). Several peripheral membrane proteins, ZO-1 (Stevenson et al. 1986 Down), ZO-2 (Jesaitis and Goodenough 1994 Down), ZO-3 (Haskins et al. 1998 Down), 7H6 antigen (Zhong et al. 1993 Down), cingulin (Citi et al. 1988 Down), symplekin (Keon et al. 1996 Down), Rab3B (Weber et al. 1994 Down), Ras target AF-6 (Yamamoto et al. 1997 Down), and ASIP, an atypical protein kinase C interacting protein (Izumi et al. 1998 Down), have been reported. The cytoplasmic domains of occludin and claudins bind to ZO-1, ZO-2, and ZO-3 (Furuse et al. 1994 Down; Haskins et al. 1998 Down; Itoh et al. 1999a Down, Itoh et al. 1999b Down). It is also believed that the integral tight junction proteins, occludin and claudins, bind to cortical actin filaments through the scaffold proteins ZO-1 and ZO-2 (Itoh et al. 1999a Down; Wittchen et al. 1999 Down).Previously, we established cell lines that stably expressed Cx32 (Kojima et al. 1999 Down) by introduction of human Cx32 cDNA into an immortalized mouse hepatocyte cell line (CHST8 cells) that lacked expression of Cx26 and Cx32. When we examined changes in expression and function of tight junctions in the transfectants compared to parental cells, the integral tight junction proteins occludin and claudin-1 and -2 were induced and the number of tight junction strands increased (Kojima et al. 1999 Down). Therefore, these transfectants appear to be useful for studies on regulation of the endogenous tight junctions.

In this study, to elucidate the mechanisms involved in maintenance of the epithelial barrier during cell division, we immunocytochemically examined changes in localization of occludin, claudin-1, ZO-1, and ZO-2 during cell division of immortalized mouse hepatocytes transfected with human Cx32 cDNA. To frequently observe cells at the M-phase of the cell cycle, the cells were treated with Taxol (Taxus brevifolia), which reduces the rate of cytokinesis at low concentrations by kinetically stabilizing spindle microtubules (Jordan et al. 1993 Down; Rowinsky and Donehower 1995 Down; Snyder and McLelland 1996 Down). By immunocytochemistry on the transfectants treated with Taxol, all tight junction proteins were present between mitotic cells and neighboring cells throughout all phases of mitosis. In the late telophase, however, the integral tight junction proteins occludin and claudin-1, but not the cytoplasmic proteins ZO-1 and ZO-2, were concentrated in the midbody between the daughter cells.


*   Materials and Methods
*Top
 *Summary
 *Introduction
 *Materials and Methods
*Results
 *Discussion
 *Literature Cited

Cell Culture, cDNA Construction, and Transfection
CHST8 is a clonal cell line derived from female C3H/HeJ mouse hepatocytes conditionally immortalized with the temperature-sensitive SV40 large T-antigen gene as described previously (Lee et al. 1995 Down). The cells were incubated with DMEM medium (GIBCO BRL; Gaithersburg, MD) with 4% fetal bovine serum (Sigma; St Louis, MO), 20 mM HEPES (Sigma), 0.5 mg/liter insulin (Sigma), 10-7 M dexamethasone (Sigma), 1 g/liter galactose (Sigma), 30 mg/liter proline (Sigma), 1 mM sodium pyruvate (Sigma), and antibiotics at 33C.

A fragment containing nucleotides 1–1558 of human connexin32 (Cx32) cDNA (Kumar and Gilula 1986 Down) was subcloned into the expression vector pREP9 (Invitrogen; Carlsbad, CA) at the KpnI-BamHI restriction site. CHST8 cells were transfected with 2 µg of Cx32 cDNA using the LIPOfectamine regent (GIBCO). After 48 hr, the cells were transferred to selection medium containing 2 µg/ml puromycin (Sigma). When surviving colonies were large enough to detect visually, they were individually picked and separately propagated. After initial screening of five clones for Cx32 expression by immunocytochemistry, we chose highly expressing clones and expression of human Cx32 and its mRNA in the stable cell lines was confirmed by immunocytochemistry and by Western and Northern blotting analyses, as previously reported (Kojima et al. 1999 Down).

It is known that Taxol at a low concentration (10 nM) reduces the rate of cytokinesis (Snyder and McLelland 1996 Down) and induces many mitotic cells (Jordan et al. 1993 Down). To examine changes in localization of tight junctional proteins in many mitotic cells, the transfectants were treated with 10 nM Taxol (Sigma) for 24 hr.

Immunofluorescence Microscopy
Cells grown on glass coverslips were fixed with cold absolute acetone for 10 min. Double immunocytochemistry with monoclonal anti-{alpha}-tubulin (Amersham; Poole, UK) and with polyclonal anti-occludin (Zymed Laboratories; San Francisco, CA), polyclonal anti-claudin-1, polyclonal anti-ZO-1 (Zymed), polyclonal anti-ZO-2 (Zymed) antibodies, and rhodamine–phalloidin (Molecular Probes; Eugene, OR) was performed. Rabbit polyclonal anti-claudin-1 antibody was raised against the synthetic polypeptide SYPTPRPYPKPTPSSGKD, which corresponds to the COOH-terminal cytoplasmic domains of mouse claudin-1 (amino acids 192–209) (Immuno-Biological Laboratories; Fuzioka, Japan). {alpha}-Tubulin was visualized using Alexia 594 (red)-conjugated anti-mouse IgG (Molecular Probes) and occludin, ZO-1, ZO-2 by Alexia 488 (green)-conjugated anti-rabbit IgG (Molecular Probes). {alpha}-Tubulin was visualized using Alexia 488 (green)-conjugated anti-mouse IgG (Molecular Probes) and actin by rhodamine–phalloidin (red). The specimens were examined with an epifluorescence microscope (Nikon; Tokyo, Japan) and a laser scanning confocal microscope (MRC 1024; Bio-Rad, Hercules, CA).


*   Results
*Top
 *Summary
 *Introduction
 *Materials and Methods
 *Results
*Discussion
 *Literature Cited

In immortalized mouse hepatocytes transfected with human Cx32 cDNA, occludin, claudin-1, ZO-1, and ZO-2 were clearly localized at cell borders (Fig 1). When the transfectants were treated with 10 nM Taxol for 24 hr, many mitotic cells (~20%) at various stages of cell division were observed. However, no conspicuous changes of polymerized microtubules in cytoplasm were observed. To examine changes in localization of tight junction proteins during cell division, double immunocytochemistry with {alpha}-tubulin and either occludin, claudin-1, ZO-1, or ZO-2 was performed. Localization of {alpha}-tubulin indicated the phases of mitotic cells: the metaphase, anaphase, telophase, and cytokinesis (Fig 1a, Fig 1c, Fig 1e, and Fig 1g). All tight junction proteins, occludin, claudin-1, ZO-1, and ZO-2, were present between mitotic cells and neighboring cells throughout all phases of mitosis (Fig 1b, Fig 1d, Fig 1f, and Fig 1g).



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  		Figure 1. Double immunocytochemistry with {alpha}-tubulin (a,c,e,g,i) and either occludin (b), claudin-1 (d), ZO-1 (f), ZO-2 (h), or rhodamine–phalloidin (j) in mitosis of transfectants treated with Taxol. All tight junction proteins, occludin, claudin-1, ZO-1, and ZO-2, are present between mitotic cells and neighboring cells throughout all phases of mitosis (arrows). Bar = 10 µm.

Next, attempting to elucidate changes in tight junctions during cell division, we further focused on changes in localization of tight junction proteins between the two daughter cells of mitosis. As shown in Fig 2a–2f, staining of {alpha}-tubulin and actin clearly demonstrated a tiny area not stained by either one, between two thick bundles of tubulin and actin in the middle of the midbody. Double immunostaining with {alpha}-tubulin and occludin demonstrated that occludin was concentrated in the midbody (Fig 2g–2r). In Z-sections, occludin was clearly observed in the midbody on the most apical site between the two daughter cells (Fig 2j–2l). Furthermore, occludin was observed not only in the midbody but also at cell borders between daughter cells and neighboring cells (Fig 2m–2o). Occludin was also observed at cell borders beneath the midbody between the daughter cells (Fig 2p–2r). Double immunostaining with {alpha}-tubulin and claudin-1 demonstrated that claudin-1 was also present in the midbody and between daughter cells and neighboring cells, like occludin (Fig 3a–3f). Double immunostaining with {alpha}-tubulin and tight junction-associated cytoplasmic proteins ZO-1 or ZO-2 demonstrated that both ZO-1 and ZO-2 were localized just beneath the midbody, not in it (Fig 3g–3r). Fig 3s and Fig 3t show schematic figures of localization of tight junction proteins during epithelial cell division. All tight junction proteins, occludin, claudin-1, ZO-1, and ZO-2, were present between mitotic cells and neighboring cells, regardless of the phase of mitosis, but only occludin and claudin-1 were localized in the midbody between the daughter cells. Line 1 of Fig 3t corresponds to Fig 2j–2l and Fig 3d–3f (occludin, claudin-1), and Line 2 corresponds to Fig 3j–3l, and Fig 3p–3r (ZO-1, ZO-2). Between the daughter cells at late telophase, the most apical part formed the midbody, in which only occludin and claudin-1 were localized, while all tight junction proteins were detected at the cell borders beneath the midbody.



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  		Figure 2. Confocal laser microscopy after double staining with {alpha}-tubulin (a,d,g,j,m,p) and either rhodamine–phalloidin (b,e) or occludin (h,k,n,q) in the midbody region of transfectants treated with Taxol. XY-sections: a–c, g–i, m–r; Z-sections: d–f, j–l. {alpha}-Tubulin and actin demonstrated a tiny area not stained for {alpha}-tubulin and actin in the middle of the midbody. Occludin is concentrated in the midbody and is observed at cell borders between daughter cells and neighboring cells or beneath the midbody between the daughter cells. Bar = 10 µm.



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  		Figure 3. Confocal laser microscopy after double staining for {alpha}-tubulin (a,d,g,j,m,p) and either claudin-1 (b,e), ZO-1 (h,k), or ZO-2 (n,q) in the midbody region of transfectants treated with Taxol. XY-sections: a–c, g–i, m–o; Z-sections: d–f, j–l, p–r. Claudin-1 is concentrated in the midbody, like occludin. Both ZO-1 and ZO-2 are localized just beneath the midbody, not in the midbody. Bar = 10 µm. (s,t) Schematic figures of localization of tight junction proteins during epithelial cell division.


*   Discussion
*Top
 *Summary
 *Introduction
 *Materials and Methods
 *Results
 *Discussion
*Literature Cited

In immortalized mouse hepatocytes transfected with human Cx32 cDNA, increases in the number of tight junction strands and in the amount of integral tight junction proteins occludin and claudin-1 and -2 were observed, as we previously reported (Kojima et al. 1999 Down). Therefore, this transfectant appears to be useful for studies on regulation of tight junction proteins, because the expression of the tight junction proteins is endogenously upregulated. In this study we focused on changes of localization of tight junction proteins of the epithelial cells during cell division to minimize the focal deficit of the continuous epithelial seal caused by mitosis.

It is well known that tight junction structures in epithelial cells are maintained during mitosis (Jinguji and Ishikawa 1992 Down; Baker and Garrod 1993 Down; Fishkind and Wang 1995 Down). Furthermore, it has also been reported that the tight junction-associated protein ZO-1 is observed at all stages of mitosis (Reinsch and Karsenti 1994 Down). In this study the tight junction proteins, occludin, claudin-1, ZO-1, and ZO-2 were present between mitotic cells and neighboring cells throughout all phases of mitosis. These findings strongly suggest that the paracellular barrier between mitotic cells and neighboring cells is maintained even during cell division.

In ultrastructural studies, intestinal epithelial cells at late telophase still show tight junction structures between the midbody and neighboring cells (Jinguji and Ishikawa 1992 Down). Consistently, the present study demonstrated that the tight junction proteins occludin, claudin-1, ZO-1, and ZO-2 were localized at cell borders between mitotic cells and neighboring cells throughout all stages of mitosis, whereas occludin and claudin-1, but not ZO-1 and ZO-2, were located in the midbody as well as at cell borders. These results indicated that the integral tight junction proteins were regulated in a different manner from the cytoplasmic proteins ZO-1 and ZO-2 during cytokinesis. Because ZO-1 and ZO-2 may be required for tight junctions to perform the barrier function (Schneeberger and Lynch 1992 Down; Gumbiner 1993 Down), the paracellular pathway around the midbody might be permeable. Just beneath the midbody, however, the integral and cytoplasmic tight junction proteins were localized throughout the cell borders, including between the daughter cells. Thus, the continuous epithelial seal was maintained even during cytokinesis.

It is known that many cytoskeletal proteins, including ERM, are located in the midbody (Sandig and Kalnins 1990 Down; Sato et al. 1991 Down). Furthermore, small GTPase RhoA, which controls the formation of actin structures (Hall 1998 Down) and the assembly of tight junctions (Jou et al. 1998 Down), is also concentrated in the midbody (Madaule et al. 1998 Down). In the present experiments, however, the scaffold protein ZO-1 that links actin and tight junction proteins was not detected in the midbody, althought occludin and claudin-1 were localized in it. Taken together, these results suggest that there may be other scaffold proteins that bind to occludin and claudins or another mechanism of interaction between the integral tight junction proteins and actin filaments. Alternatively, it may be very difficult to detect ZO-1 and ZO-2 by immunocytochemistry, probably because these cytoplasmic proteins are too condensed in the midbody, since the midbody was negative for both tubulin and actin by immunocytochemistry in our study despite the observation of microtubules in it by electron microscopy.


*   Acknowledgments

Supported in part by Grants-in-Aid from the Ministry of Education, Culture, Sports and Science, and the Ministry of Welfare of Japan.

Received for publication June 13, 2000; accepted October 17, 2000.


*   Literature Cited
*Top
 *Summary
 *Introduction
 *Materials and Methods
 *Results
 *Discussion
 *Literature Cited

Baker J, Garrod D (1993) Epithelial cells retain junctions during mitosis. J Cell Sci 104:415-425[Abstract]

Citi S, Sabanay H, Jakes R, Geiger B, Kendrick-Jones J (1988) Cingulin, a new peripheral component of tight junctions. Nature 333:272-275[Medline]

Fishkind DJ, Wang YL (1995) New horizons for cytokinesis. Curr Opin Cell Biol 7:23-31[Medline]

Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S (1998) Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141:1539-1550[Abstract/Free Full Text]

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

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

Gumbiner B (1993) Breaking through the tight junction barrier. J Cell Biol 123:1631-1633[Free Full Text]

Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509-514[Abstract/Free Full Text]

Haskins J, Gu L, Wittchen ES, Hibbard J, Stevenson BR (1998) ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J Cell Biol 141:199-208[Abstract/Free Full Text]

Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S (1999a) Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 147:1351-1363[Abstract/Free Full Text]

Itoh M, Morita K, Tsukita S (1999b) Characterization of ZO-2 as a MAGUK family member associated with tight as well as adherens junctions with a binding affinity to occludin and alpha catenin. J Biol Chem 274:5981-5986[Abstract/Free Full Text]

Izumi Y, Hirose T, Tamai Y, Hirai S, Nagashima Y, Fujimoto T, Tabuse Y, Kemphues KJ, Ohno S (1998) 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 143:95-106[Abstract/Free Full Text]

Jesaitis LA, Goodenough DA (1994) Molecular characterization and tissue distribution of ZO-2, a tight junction protein homologous to ZO-1 and the Drosophila discs-large tumor suppressor protein. J Cell Biol 124:949-961[Abstract/Free Full Text]

Jinguji Y, Ishikawa H (1992) Electron microscopic observations on the maintenance of the tight junction during cell division in the epithelium of the mouse small intestine. Cell Struct Funct 17:27-37[Medline]

Jordan MA, Toso RJ, Thrower D, Wilson L (1993) Mechanism of mitotic block and inhibition of cell proliferation by Taxol at low concentrations. Proc Natl Acad Sci USA 90:9552-9556[Abstract/Free Full Text]

Jou TS, Schneeberger EE, Nelson WJ (1998) Structural and functional regulation of tight junctions by RhoA and Rac1 small GTPases. J Cell Biol 142:101-115[Abstract/Free Full Text]

Keon BH, Schafer S, Kuhn C, Grund C, Franke WW (1996) Symplekin, a novel type of tight junction plaque protein. J Cell Biol 134:1003-1018[Abstract/Free Full Text]

Kojima T, Sawada N, Chiba H, Kokai Y, Yamamoto M, Urban M, Lee GH, Hertzberg EL, Mochizuki Y, Spray DC (1999) Induction of tight junctions in human connexin 32 (hCx32)-transfected mouse hepatocytes: connexin 32 interacts with occludin. Biochem Biophys Res Commun 266:222-229[Medline]

Kumar NM, Gilula NB (1986) Cloning and characterization of human and rat liver cDNAs coding for a gap junction protein. J Cell Biol 103:767-776[Abstract/Free Full Text]

Lee GH, Ogawa K, Drinkwater NR (1995) Conditional transformation of mouse liver epithelial cells: an in vitro model for analysis of genetic events in hepatocarcinogenesis. Am J Pathol 147:1811-1822[Abstract]

Madaule P, Eda M, Watanabe N, Fujisawa K, Matsuoka T, Bito H, Ishizaki T, Narumiya S (1998) Role of citron kinase as a target of the small GTPase Rho in cytokinesis. Nature 394:491-494[Medline]

Martin–Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E (1998) Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142:117-127[Abstract/Free Full Text]

Morita K, Furuse M, Fujimoto K, Tsukita S (1999) Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA 96:511-516[Abstract/Free Full Text]

Reinsch S, Karsenti E (1994) Orientation of spindle axis and distribution of plasma membrane proteins during cell division in polarized MDCKII cells. J Cell Biol 126:1509-1526[Abstract/Free Full Text]

Rowinsky E, Donehower R (1995) Paclitaxel (Taxol). N Engl J Med 332:1004-1014[Free Full Text]

Sandig M, Kalnins VI (1990) Reorganization of circumferential microfilament bundles in retinal epithelial cells during mitosis. Cell Motil Cytoskel 17:133-141[Medline]

Sato N, Yonemura S, Obinata T, Tsukita S (1991) Radixin, a barbed end-capping actin-modulating protein, is concentrated at the cleavage furrow during cytokinesis. J Cell Biol 113:321-330[Abstract/Free Full Text]

Schneeberger EE, Lynch RD (1992) Structure, function, and regulation of cellular tight junctions. Am J Physiol 262:L647-661[Abstract/Free Full Text]

Snyder JA, McLelland SL (1996) Taxol reduces the rate of cytokinesis in PtK1 cells. Cell Biol Int 20:573-578[Medline]

Staehelin LA (1973) Further observations on the fine structure of freeze-cleaved tight junctions. J Cell Sci 13:763-786[Abstract/Free Full Text]

Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA (1986) Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludin) in a variety of epithelia. J Cell Biol 103:755-766[Abstract/Free Full Text]

Weber E, Berta G, Tousson A, St John P, Green MW, Gopalokrishnan U, Jilling T, Sorscher EJ, Elton TS, Abrahamson DR, Kirk KL (1994) Expression and polarized targeting of a rab3 isoform in epithelial cells. J Cell Biol 125:583-594[Abstract/Free Full Text]

Wittchen ES, Haskins J, Stevenson BR (1999) 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 274):35179-35185

Yamamoto T, Harada N, Kano K, Taya S, Canaani E, Matsuura Y, Mizoguchi A, Ide C, Kaibuchi K (1997) The Ras target AF-6 interacts with ZO-1 and serves as a peripheral component of tight junctions in epithelial cells. J Cell Biol 139:785-795[Abstract/Free Full Text]

Zhong Y, Saitoh T, Minase T, Sawada N, Enomoto K, 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[Abstract/Free Full Text]


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