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Histochemistry and Cell Biology

, Volume 130, Issue 5, pp 943–956 | Cite as

Differential expression pattern of protein ARVCF in nephron segments of human and mouse kidney

  • Britta Walter
  • Tanja Schlechter
  • Michaela Hergt
  • Irina Berger
  • Ilse HofmannEmail author
Original Paper

Abstract

The protein ARVCF is a member of the p120 subfamily of armadillo proteins whose members have been described to occur in junction-bound and non-junction-bound forms. Studies on ARVCF were constrained because the endogenous protein was difficult to detect with the available reagents. We have generated novel monoclonal and polyclonal antibodies usable for biochemical and localization studies. By systematic immunohistochemical analysis of various tissues protein ARVCF is prominently detected in mouse, bovine and human kidney. Using antibodies against specific markers of nephron segments protein ARVCF is localized in proximal tubules according to double label immunofluorescence. Besides its occurrence in proximal tubules of adult kidney and in renal cell carcinoma derived from proximal tubules ARVCF is also detected in maturing nephrons in early mouse developmental stages such as, for example, 15 days of gestation (E15). Immunoblotting of total extracts of cultured cells of renal origin showed that ARVCF is detected in all human and murine cultured cells analyzed. Upon immunolocalization ARVCF is mostly detected in the cytoplasm occurring in a fine granular form. This prominent cytoplasmic localization of ARVCF in cultured cells and its occurrence in proximal tubules implies an involvement of ARVCF in specific functional processes of proximal tubules of kidney.

Keywords

Arm-repeat protein p120-catenin subfamily Nephron Proximal tubule Renal cell carcinoma 

Notes

Acknowledgments

We thank C. Kuhn (Division of Cell Biology, German Cancer Research Center) for experimental help in the initial course of this study and A. Wiss (Department of Pathology, University of Heidelberg) for competent help in sectioning paraffin-embedded human tissues. For continuous and generous support Prof. Dr. W. W. Franke is thanked (Division of Cell Biology, German Cancer Research Center). We gratefully acknowledge the critical comments of Dr. M. Elger (Institute of Anatomy, University Heidelberg) and Dr. B. Falkowska-Hansen (Genetics of Skin Carcinogenesis, German Cancer Research Center). This study was supported by a project grant from the German Ministry for Education and Research (BMBF) in a cooperative research program entitled “Standardization of mesenchymal stem cells for regenerative medicine (START-MSC)”.

Supplementary material

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References

  1. Abuazza G, Becker A, Williams SS, Chakravarty S, Truong H-T, Lin F, Baum M (2006) Claudins 6, 9 and 13 are developmentally express renal tight junction proteins. Am J Physiol Renal Physiol 291:1132–F1141CrossRefGoogle Scholar
  2. Agre P (2000) Aquaporin water channels in kidney. J Am Soc Nephrol 11:764–777PubMedGoogle Scholar
  3. Anastasiadis PZ, Reynolds AB (2000) The p120 catenin family: complex roles in adhesion, signaling and cancer. J Cell Sci 113:1319–1334PubMedGoogle Scholar
  4. Barberini F, Famliari G, Vittoru I, Carpino F, Melis M (1984) Morphological and statistical investigation of the occurrence of “tubule-like cells” in the renal corpuscle of the mouse kidney induced by sex hormones. Renal Physiol 7:227–236PubMedGoogle Scholar
  5. Behrens J (2000) Control of beta-catenin in signaling in tumor development. Ann N Y Acad Sci 910:21–33PubMedCrossRefGoogle Scholar
  6. Bonné S, van Hengel J, Nollet F, Kools P, van Roy F (1999) Plakophilin-3, a novel armadillo-like protein present in nuclei and desmosomes of epithelial cells. J Cell Sci 112:2265–2276PubMedGoogle Scholar
  7. Borrmann CM, Grund C, Kuhn C, Hofmann I, Pieperhoff S, Franke WW (2006) The area composita of adhering junctions connecting heart muscle cells of vertebrates. II. Occurrence of both desmosomal and fascia adhaerens molecules in the intercalated disks. Eur J Cell Biol 85:469–485PubMedCrossRefGoogle Scholar
  8. Dietert SE (1967) The columnar cells occurring in the parietal layer of Bowman’s capsule. Cellular fine structure and protein transport. J Cell Biol 35:435–444PubMedCrossRefGoogle Scholar
  9. Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17:375–412PubMedCrossRefGoogle Scholar
  10. Franke WW, Goldschmidt MD, Zimbelmann R, Mueller HM, Schiller DL, Cowin P (1989) Molecular cloning and amino acid sequence of human plakoglobin, the common junctional plaque protein. Proc Natl Acad Sci USA 86:4027–4031PubMedCrossRefGoogle Scholar
  11. Golenhofen N, Drenckhahn D (2000) The catenin, p120ctn, is a common membrane-associated protein in various epithelial cells and tissues. Histochem Cell Biol 114:147–155PubMedGoogle Scholar
  12. Halbleib JM, Nelson WJ (2007) Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev 20:3199–3214CrossRefGoogle Scholar
  13. Hatzfeld M, Kristjansson GI, Plessmann U, Weber K (1994) Band 6 protein, a major constituent of desmosomes from stratified epithelia, is a novel member of the armadillo multigene family. J Cell Sci 107:2259–2270PubMedGoogle Scholar
  14. Hatzfeld M, Nachtsheim C (1996) Cloning and characterization of a new armadillo family member, p0071, associated with the junctional plaque: evidence for a subfamily of closely related proteins. J Cell Sci 109:2767–2778PubMedGoogle Scholar
  15. Hatzfeld M (2005) The p120 family of cell adhesion molecules. Eur J Cell Biol 84:205–214PubMedCrossRefGoogle Scholar
  16. Heid HW, Schmidt A, Zimbelmann R, Schäfer S, Winter-Simanowski S, Stumpp S, Keith M, Figge U, Schnölzer M, Franke WW (1994) Cell type-specific desmosomal plaque proteins of the plakoglobin family: plakophilin 1 (band 6 protein). Differentiation 58:113–131PubMedCrossRefGoogle Scholar
  17. Hession C, Decker JM, Sherblom AP, Kumar S, Yue CC, Mataliano RJ, Tizard R, Kawashima E, Schmeissner U, Heletky S, Chow EP, Burne CA, Shaw A, Muchmore AW (1987) Uromodulin (Tamm-Horsfall glycoprotein): a renal ligand for lymphokines. Science (Washington DC) 237:1479–1484CrossRefGoogle Scholar
  18. Hofmann I, Schnölzer M, Kaufmann I, Franke WW (2002) Symplekin, a constitutive protein of karyo- and cytoplasmic particles involved in mRNA biogenesis in Xenopus laevis oocytes. Mol Biol Cell 13:1665–1676PubMedCrossRefGoogle Scholar
  19. Hofmann I, Casella M, Schnölzer M, Schlechter T, Spring H, Franke WW (2006) Identification of the junctional plaque protein plakophilin 3 in cytoplasmic particles containing RNA-binding proteins and the recruitment of plakophilins 1 and 3 to stress granules. Mol Biol Cell 17:1388–1398PubMedCrossRefGoogle Scholar
  20. Jung K-Y, Dean D, Jiang J, Gaylor S, Griffith WH, Burghardt RC, Parrish AR (2004) Loss of N-cadherin and α-catenin in the proximal tubules of aging male Fischer 344 rats. Mechan Aging Dev 125:445–453CrossRefGoogle Scholar
  21. Katz AI, Doucet A, Morel F (1979) Na-K-ATPase activity along the rabbit, rat, and mouse nephron. Am J Physiol 237:F114–120PubMedGoogle Scholar
  22. Kaufman MH (1995) The atlas of mouse development. Revised 2nd edn. Academic Press Limited, LondonGoogle Scholar
  23. Kaufmann U, Zuppinger C, Waibler Z, Rudiger M, Urbich C, Martin B, Jockusch BM, Eppenberger H, Starzinski-Powitz A (2000) The armadillo repeat region targets ARVCF to cadherin-based cellular junctions. J Cell Sci 113:4121–4135PubMedGoogle Scholar
  24. Keirsebilck A, Bonné S, Staes K, van Hengel J, Nollet F, Reynolds A, van Roy F (1998) Molecular cloning of the human p120ctn catenin gene (CTNND1): expression of multiple alternatively spliced isoforms. Genomics 50:129–146PubMedCrossRefGoogle Scholar
  25. Kim G, Rajasekaran SA, Thomas G, Rosen EA, Landaw EM, Shintaku P, Lassman C, Said J, Rajasekaran AK (2005) Renal clear-cell carcinoma: an ultrastructural study on the junctional complexes. Histol Histopathol 20:35–44PubMedGoogle Scholar
  26. 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
  27. Koeser J, Troyanovsky SM, Grund C, Franke WW (2003) De novo formation of desmosomes in cultured cells upon transfection of genes encoding specific desmosomal components. Exp Cell Res 285:114–130PubMedCrossRefGoogle Scholar
  28. Kwon O, Myers BD, Sibley R, Dafoe D, Alfrey E, Nelson WJ (1998) Distribution of cell membrane-associated proteins along the human nephron. J Histochem Cytochem 46:1423–1434PubMedGoogle Scholar
  29. Mariner DJ, Wang J, Reynolds AB (2000) ARVCF localizes to the nucleus and adherens junction and is mutually exclusive with p120(ctn) in E-cadherin complexes. J Cell Sci 113:1481–1490PubMedGoogle Scholar
  30. Mertens C, Kuhn C, Franke WW (1996) Plakophilins 2a and 2b constitutive proteins of dual location in the karyoplasm and the desmosomal plaque. J Cell Biol 13:1009–1025CrossRefGoogle Scholar
  31. Mertens C, Hofmann I, Wang Z, Teichmann M, Sepehri Chong S, Schnölzer M, Franke WW (2001) Nuclear particles containing RNA polymerase III complexes associated with junctional plaque protein plakophilin 2. Proc Natl Acad Sci 98:7795–7800PubMedCrossRefGoogle Scholar
  32. Moll R, Hage C, Thoenes W (1991) Expression of intermediate filament proteins in fetal and adult human kidney: modulations of intermediate filament patterns during development and in damaged tissue. Lab Invest 65:74–86PubMedGoogle Scholar
  33. Nouwen EJ, Dauwe S, van der Biest I, De Broe ME (1993) Stage- and segment-specific expression of cell-adhesion molecules N-Cam, A-Cam, and L-Cam in the kidney. Kidney Int 44:147–158PubMedCrossRefGoogle Scholar
  34. Ohta H, Adachi H, Takiguchi M, Inaba M (2006) Restricted localization of claudin-16 at the tight junction in the thick ascending limb of Henle’s loop together with claudins 3, 4 and 10 in bovine nephrons. J Vet Med Sci 68:453–463PubMedCrossRefGoogle Scholar
  35. Oosterwijk E, van Mujen GNP, Oosterwijk-Wakka JC, Warnaar SO (1990) Expression of intermediate-sized filaments in developing and adult kidney and in renal cell carcinoma. J Histochem Cytochem 38:385–392PubMedGoogle Scholar
  36. Paffenholz R, Franke WW (1997) Identification and localization of a neurally expressed member of the plakoglobin/armadillo multigene family. Differentiation 61:293–304PubMedCrossRefGoogle Scholar
  37. Paffenholz R, Kuhn C, Grund C, Stehr S, Franke WW (1999) The arm-repeat protein NPRAP (neurojungin) is a constituent of the plaques of the outer limiting zone in the retina, defining a novel type of adhering junction. Exp Cell Res 250:452–464PubMedCrossRefGoogle Scholar
  38. Paul R, Ewing CM, Robinson JC, Marshall FF, Johnson KR, Wheelock MJ, Isaacs WB (1997) Cadherin-6, a cell adhesion molecule specifically expressed in proximal renal tubule and renal cell carcinoma. Cancer Res 57:2741–2748PubMedGoogle Scholar
  39. Paulson AF, Mooney E, Fang X, Ji H, McCrea PD (2000) Xarvcf, Xenopus member of the p120 catenin subfamily associating with cadherin juxtamembrane region. J Biol Chem 275:30124–30131PubMedCrossRefGoogle Scholar
  40. Peifer M, Berg S, Reynolds AB (1994) A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 76:789–791PubMedCrossRefGoogle Scholar
  41. Peitsch WK, Hofmann I, Endlich N, Prätzel S, Kuhn C, Spring H, Gröne H-J, Kriz W, Franke WW (2003) Cell Biological and biochemical characterization of drebrin complexes in mesangial cells and podocytes of renal glomeruli. J Am Soc Nephrol 14:1452–1463PubMedCrossRefGoogle Scholar
  42. Perez-Moreno M, Fuchs E (2006) Catenins: keeping cells from getting their signals crossed. Dev Cell 11:601–612PubMedCrossRefGoogle Scholar
  43. Piepenhagen PA, Nelson WJ (1998) Biogenesis of polarized epithelial cells during kidney development in situ: roles of E-cadherin-mediated cell–cell adhesion and membrane cytoskeleton organization. Mol Biol Cell 11:3161–3177Google Scholar
  44. Piepenhagen PA, Peters LL, Lux SE, Nelson WJ (1995) Differential expression of Na(+)–(K +)-ATPase, ankyrin, fodrin, and E-cadherin along the kidney nephron. Am J Physiol 269:C1417–1432PubMedGoogle Scholar
  45. Prozialeck WC, Lamar PC, Lynch SM (2003) Cadmium alters the localization of N-cadherin, and beta-catenin in the proximal tubule epithelium. Toxicol Appl Pharmacol 189:180–195PubMedCrossRefGoogle Scholar
  46. Prozialeck WC, Lamar PC, Appelt DM (2004) Differential expression of E-cadherin, N-cadherin and beta-catenin in proximal and distal segments of the rat nephron. BMC Physiol 4:10PubMedCrossRefGoogle Scholar
  47. Reynolds AB, Daniel J, McCrea PD, Wheelock MJ, Wu J, Zang Z (1994) Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol Cell Biol 14:8333–8342PubMedGoogle Scholar
  48. Reynolds AB, Roczniak-Ferguson A (2004) Emerging roles for p120-catenin in cell adhesion and cancer. Oncogene 23:7947–7956PubMedCrossRefGoogle Scholar
  49. Sáenz-Morales D, Escribese MM, Stamatakis K, Garcia-Martos M, Alegre L, Conde E, Perez-Sala D, Mampaso F, Garcia-Bermejo ML (2006) Requirements for proximal tubule epithelial cell detachment in response to ischemia: role of oxidative stress. Exp Cell Res 312:3711–3727PubMedCrossRefGoogle Scholar
  50. Schmidt A, Langbein L, Rode M, Prätzel S, Zimbelmann R, Franke WW (1997) Plakophilins 1a and 1b: widespread nuclear proteins recruited in specific epithelial cells as desmosmal plaque components. Cell Tissue Res 290:481–499PubMedCrossRefGoogle Scholar
  51. Schmidt A, Langbein L, Prätzel S, Rode M, Rackwitz H-R, Franke WW (1999) Plakophilin 3—a novel cell-type-specific desmosomal plaque protein. Differentiation 64:291–306PubMedGoogle Scholar
  52. Sirotkin H, O’Donnell H, DasGupta R, Halford S, St Jore B, Puech A, Parimoo S, Morrow S, Skoultchi A, Weissman SM, Scambler P, Kucherlapati R (1997) Identification of a new human catenin gene family member (ARVCF) from the region deleted in velo-cardio-facial syndrome. Genomics 41:75–83PubMedCrossRefGoogle Scholar
  53. Tanoue T, Takeichi M (2005) New insights into fat cadherins. J Cell Sci 118:2347–2353PubMedCrossRefGoogle Scholar
  54. Takeichi M (1991) Cadherin adhesion receptors as a morphogenetic regulator. Science 251:1451–1455PubMedCrossRefGoogle Scholar
  55. Uchida S, Sasaki S, Nitta K, Uchida K, Horita S, Nihei H, Marumo F (1995) Localization and functional characterization of rat kidney-specific chloride channel, ClC-K1. J Clin Invest 95:104–113PubMedCrossRefGoogle Scholar
  56. Ulfig N, Chan WY (2004) Expression of ARVCF in the human ganglionic eminence during fetal development. Dev Neurosci 26:38–44PubMedCrossRefGoogle Scholar
  57. van Hengel J, Vanhoenacker P, Staes K, van Roy F (1999) Nuclear localization of the p120(ctn) armadillo-like catenin is counteracted by a nuclear export signal and by E-cadherin. Proc Natl Acad Sci USA 96:7980–7985PubMedCrossRefGoogle Scholar
  58. Waibler Z, Schafer A, Starzinski-Powitz A (2001) mARVCF cellular localisation and binding to cadherins is influenced by the cellular context but not by alternative splicing. J Cell Sci 114:3873–3884PubMedGoogle Scholar
  59. Yu J, McMahon AP, Valerius MT (2004) Recent genetic studies of mouse kidney development. Curr Opin Genet Dev 14:550–557PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Britta Walter
    • 1
    • 3
  • Tanja Schlechter
    • 1
    • 2
  • Michaela Hergt
    • 1
  • Irina Berger
    • 3
  • Ilse Hofmann
    • 1
    • 4
    Email author
  1. 1.Division of Cell BiologyGerman Cancer Research CenterHeidelbergGermany
  2. 2.Progen BiotechnikHeidelbergGermany
  3. 3.Institute of PathologyUniversity of HeidelbergHeidelbergGermany
  4. 4.Joint Research Division Vascular Biology of the Medical Faculty MannheimUniversity of Heidelberg and the German Cancer Research Center, CBTMMannheimGermany

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