Histochemistry and Cell Biology

, Volume 127, Issue 4, pp 457–462 | Cite as

Expression patterns of claudin family of tight-junction proteins in the mouse prostate

  • Naoyuki Sakai
  • Hideki Chiba
  • Hiroki Fujita
  • Yushi Akashi
  • Makoto Osanai
  • Takashi Kojima
  • Norimasa Sawada
Short Communication

Abstract

Claudins are the transmembrane proteins forming the backbone of tight junctions, and consist of over 20 members of a gene family. Claudins are expressed in a tissue- and cell-type specific fashion, and changes in their abundance and/or distribution are proposed to play important roles in the pathophysiology of numerous disorders. In the prostate, claudin-1, -3, -4 and -7 transcripts are known to be expressed, but it is unknown regarding mRNA expression of other claudins or concerning expression and localization of claudin proteins in this organ. We herein show, by RT-PCR and Western blotting analyses, that not only these four claudins but also claudin-5, -8 and -10 are expressed in the normal mouse prostate. Claudin-3, -4, -5, -8 and -10 were primarily localized at the apicalmost sites of lateral membranes of luminal epithelial cells in the prostate gland, whereas claudin-1 and -7 were distributed along the basolateral membranes of the epithelium. These findings provide basic information for elucidating the significance of claudins in prostate diseases, including prostate cancers.

Keywords

Claudins Tight junction Prostatic gland Epithelial cells 

References

  1. Acharya P, Beckel J, Ruiz WG, Wang E, Rojas R, Birder L, Apodaca G (2004) Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8 and -12 in bladder epithelium. Am J Physiol Renal Physiol 287:305–318CrossRefGoogle Scholar
  2. Anderson JM, Cereijido M (2001) Introduction: evolution of ideas on the tight junction. In: Cereijido M, Anderson JM (eds) Tight junctions, 2nd edn. CRC Press, Boca Raton, pp 1–18Google Scholar
  3. Agarwal R, D’Souza T, Morin PJ (2005) Claudin-3 and claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity. Cancer Res 65:7378–7385PubMedCrossRefGoogle Scholar
  4. Briehl MM, Miesfeld RL (1991) Isolation and characterization of transcripts induced by androgen withdrawal and apoptotic cell death in the rat ventral prostate. Mol Endocrinol 10:1381–1388CrossRefGoogle Scholar
  5. Chiba H, Clifford J, Metzger D, Chambon P (1997) Specific and redundant functions of retinoid X receptor/retinoic acid receptor heterodimers in differentiation, proliferation, and apoptosis of F9 embryonal carcinoma cells. J Cell Biol 139:735–747PubMedCrossRefGoogle Scholar
  6. Chiba H, Gotoh T, Kojima T, Satohisa S, Kikuchi K, Osanai M, Sawada N (2003) Hepatocyte nuclear factor (HNF)-4α triggers formation of functional tight junctions and establishment of polarized epithelial morphology in F9 embryonal carcinoma cells. Exp Cell Res 285:288–297CrossRefGoogle Scholar
  7. Chiba H, Itoh T, Satohisa S, Sakai N, Noguchi H, Osanai M, Kojima T, Sawada N (2005) Activation of p21CIP1/WAF1 gene expression and inhibition of cell proliferation by overexpression of hepatocyte nuclear factor-4α. Exp Cell Res 302:11–21PubMedCrossRefGoogle Scholar
  8. Chiba H, Kojima T, Osanai M, Sawada N (2006a) The significance of interferon-γ-triggered internalization of tight-junction proteins in inflammatory bowel disease. Sci STKE 316: pe1Google Scholar
  9. Chiba H, Sakai N, Murata M, Osanai M, Ninomiya T, Kojima T, Sawada N (2006b) The nuclear receptor hepatocyte nuclear factor 4α acts as a morphogen to induce the formation of microvilli. J Cell Biol 175:971–980CrossRefGoogle Scholar
  10. Coyne CB, Gambling TM, Boucher RC, Carson JL, Johnson LG (2003) Role of claudin interactions in airway tight junctional permeability. Am J Physiol Lung Cell Mol Physiol 285:1166–1178Google Scholar
  11. Fujita K, Katahira J, Horiguchi Y, Sonoda N, Furuse M, Tsukita S (2000) Clostridium perfringens enterotoxin binds to the second extracellular loop of claudin-3, a tight junction integral membrane protein. FEBS Lett 476:258–261PubMedCrossRefGoogle Scholar
  12. Fujita H, Chiba H, Yokozaki H, Sakai N, Sugimoto K, Wada T, Kojima T, Yamashita T, Sawada N (2006) Differential expression and subcellular localization of claudin-7, -8, -12, -13, and -15 along the mouse intestine. J Histochem Cytochem 54: 933–944PubMedCrossRefGoogle Scholar
  13. Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S (2002) Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 156:1099–1111PubMedCrossRefGoogle Scholar
  14. Gow A, Southwood CM, Li JS, Pariali M, Riordan GP, Brodie SE, Danias J, Bronstein JM, Kachar B, Lazzarini RA (1999) CNS myelin and Sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 99:649–659PubMedCrossRefGoogle Scholar
  15. Gregory M, Dufresne J, Hermo L, Cyr DG (2001) Claudin-1 is not restricted to tight junctions in the rat epididymis. Endocrinology 142:854–863PubMedCrossRefGoogle Scholar
  16. Holmes JL, Van Itallie CM, Rasmussen JE, Anderson JM (2006) Claudin profiling in the mouse during postnatal intestinal development and along the gastrointestinal tract reveals complex expression patterns. Gene Expr Patterns 6:581–588PubMedCrossRefGoogle Scholar
  17. Ishizaki T, Chiba H, Kojima T, Fujibe M, Soma T, Miyajima H, Nagasawa K, Wada I, Sawada N (2003) Cyclic AMP induces phosphorylation of claudin-5 immunoprecipitates and expression of claudin-5 gene in blood-brain barrier endothelial cells via protein kinase A-dependent and -independent pathways. Exp Cell Res 290:275–288PubMedCrossRefGoogle Scholar
  18. Katahira J, Inoue N, Horiguchi Y, Matsuda M, Sugimoto N (1997) Molecular cloning and functional characterization of the receptor for Clostridium perfringens enterotoxin. J Cell Biol 136:1239–1247PubMedCrossRefGoogle Scholar
  19. Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S (2002) Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13:875–886PubMedGoogle Scholar
  20. Kubota H, Chiba H, Takakuwa Y, Osanai M, Tobioka H, Kohama G, Mori M, Sawada N (2001) Retinoid X receptor α and retinoic acid receptor γ mediate expression of genes encoding tight junction proteins and barrier function in F9 cells during visceral endodermal differentiation. Exp Cell Res 263:163–172PubMedCrossRefGoogle Scholar
  21. Ladwein M, Pape UF, Schmidt DS, Schnolzer M, Fiedler S, Langbein L, Franke WW, Moldenhauer G, Zoller M (2005) The cell-cell adhesion molecule EpCAM interacts directly with the tight junction protein claudin-7. Exp Cell Res 309:345–357PubMedCrossRefGoogle Scholar
  22. Li WY, Huey CL, Yu ASL (2004) Expression of claudin-7 and -8 along the mouse nephron. Am J Physiol Renal Physiol 286:1063–1071CrossRefGoogle Scholar
  23. Long H, Crean CD, Lee W, Cummings OW, Gabig GB (2001) Expression of Clostridium perfringens enterotoxin receptors claudin-3 and claudin-4 in prostate cancer epithelium. Cancer Res 61:7878–7881PubMedGoogle Scholar
  24. Luk JM, Tong MK, Mok BW, Tam PC, Yeung WS, Lee KF (2004) Sp1 site is crucial for the mouse claudin-19 gene expression in the kidney cells. FEBS Lett 578:251–256PubMedCrossRefGoogle Scholar
  25. Morin PJ (2005) Claudin proteins in human cancer: promising new targets for diagnosis and therapy. Cancer Res 65: 9603–9606PubMedCrossRefGoogle Scholar
  26. Niimi T, Nagashima K, Ward JM, Minoo D, Zimonjic DB, Popescu NC, Kimura S (2001) Claudin-18, a novel downstream target gene for the T/EBP/NKX2.1 homeodomain transcription factor, encodes lung- and stomach-specific isoforms through alternative splicing. Mol Cell Biol 21:7830–7390CrossRefGoogle Scholar
  27. Oku N, Sasabe E, Ueta E, Yamamoto T, Osaki T (2006) Tight junction protein claudin-1 enhances the invasive activity of oral squamous cell carcinoma cells by promoting cleavage of laminin-5 γ2 chain via matrix metalloproteinase (MMP)-2 and membrane-type MMP-1. Cancer Res 66:5251–5257PubMedCrossRefGoogle Scholar
  28. Satohisa S, Chiba H, Osanai M, Ohno S, Kojima T, Saito T, Sawada N (2005) Behavior of tight-junction, adherens-junction and cell polarity proteins during HNF-4α-induced epithelial polarization. Exp Cell Res 310:66–78PubMedCrossRefGoogle Scholar
  29. Sawada N, Murata M, Kikuchi K, Osanai M, Tobioka H, Kojima T, Chiba H (2003) Tight junctions and human diseases. Med Electron Microsc 36:147–156PubMedCrossRefGoogle Scholar
  30. Sonoda N, Furuse M, Sasaki H, Yonemura S, Katahira J, Horiguchi Y, Tsukita S (1999) Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: evidence for direct involvement of claudins in tight junction barrier. J Cell Biol 147:195–204PubMedCrossRefGoogle Scholar
  31. Swisshelm K, Machl A, Planitzer S, Robertson R, Kubbies M, Hosier S (1999) SEMP1, a senescence-associated cDNA isolated from human mammary epithelial cells, is a member of an epithelial membrane protein superfamily. Gene 226:285–295PubMedCrossRefGoogle Scholar
  32. Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2:285–293PubMedCrossRefGoogle Scholar
  33. Turksen K, Troy TC (2004) Barriers built on claudins. J Cell Sci 117:2435–2447PubMedCrossRefGoogle Scholar
  34. Van Itallie CM, Anderson JM (2004) The molecular physiology of tight junction pores. Physiology 19:331–338PubMedCrossRefGoogle Scholar
  35. Van Itallie CM, Anderson JM (2006) Claudins and epithelial paracellular transport. Annu Rev Physiol 68:403–429PubMedCrossRefGoogle Scholar
  36. Zheng JY, Yu D, Foroohar M, Ko E, Chan J, Kim N, Chiu R, Pang S (2003) Regulation of the expression of the prostate-specific antigen by claudin-7. J Membr Biol 194:187–197PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Naoyuki Sakai
    • 1
  • Hideki Chiba
    • 1
  • Hiroki Fujita
    • 1
  • Yushi Akashi
    • 1
  • Makoto Osanai
    • 1
  • Takashi Kojima
    • 1
  • Norimasa Sawada
    • 1
  1. 1.Department of PathologySapporo Medical University School of MedicineSapporoJapan

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