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Protein p0071, an armadillo plaque protein of adherens junctions, is predominantly expressed in distal renal tubules

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Abstract

Protein p0071 is a member of the p120-subfamily of armadillo proteins and is well known as a junctional plaque component involved in cell–cell adhesion, especially in adherens junctions. By systematic immunohistochemical analysis of mouse and human kidney tissues, p0071 was prominently detected in distinct kidney tubules. Upon double-labeling immunolocalization experiments with segment-specific markers, p0071 was predominantly localized in distal straight and convoluted tubules and to a lesser extent in proximal tubules, in the ascending thin limb of loop of Henle and in the collecting ducts. In capillaries of the kidney, p0071 co-localized with VE-cadherin an endothelium-specific cadherin. Protein p0071 was also detected in both, renal cell carcinomas derived from distal tubules and in maturing nephrons of early mouse developmental stages. Immunoblotting of total extracts of cultured cells of renal origin showed that p0071 was detected in all human and murine cells analyzed. Upon immunolocalization, p0071 was observed in adherens junctions but also in distinct cytoplasmic structures at the cell periphery of cultured cells. Possible structural and functional roles of p0071 are suggested by its preferential occurrence in distinct tubule segments, and its potential use as a cytodiagnostic cell type marker in renal pathology is discussed.

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References

  • 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:F1132–F1141

    Article  CAS  PubMed  Google Scholar 

  • Anastasiadis PZ, Reynolds AB (2000) The p120 catenin family: complex roles in adhesion, signaling and cancer. J Cell Sci 113:1319–1334

    CAS  PubMed  Google Scholar 

  • Batlle D, Ghanekar H, Jain S, Mitra A (2001) Hereditary distal renal tubular acidosis: new understandings. Annu Rev Med 52:471–484

    Article  CAS  PubMed  Google Scholar 

  • Breviario F, Caveda L, Corada M, Martin-Padura I, Navarro P, Golay J, Introna M, Gulino D, Lampugnani MG, an Dejana E (1995) Functional properties of human vascular endothelial cadherin (7B4/cadherin-5), an endothelium-specific cadherin. Arterioscler Thromb Vasc Biol 15:1229–1239

    CAS  PubMed  Google Scholar 

  • Calkins CC, Hoepner BL, Law CM, Novak MR, Setzer SV, Hatzfeld M, Kowalczyk AP (2003) The armadillo family protein p0071 is a VE-cadherin and desmoplakin-binding protein. J Biol Chem 278:1774–1783

    Article  CAS  PubMed  Google Scholar 

  • Deguchi M, Iizuka T, Hata Y, Nishimury W, Hirao K, Yao I, Kawabe H, Takai Y (2000) Papin. A novel multiple PSD95/Dlg-A/ZO-1 protein interacting with neural plakophilin-related armadillo repeat protein/δ-catenin and p0071. J Biol Chem 275:29875–29880

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara TM, Bichet DG (2005) Molecular biology of hereditary diabetes insipidus. J Am Soc Nephrol 16:2836–2846

    Article  CAS  PubMed  Google Scholar 

  • Getsios S, Huen AC, Green KJ (2004) Working out the strength and flexibility of desmosomes. Nat Rev Mol Cell Biol 5:271–281

    Article  CAS  PubMed  Google Scholar 

  • Golenhofen N, Drenckhahn D (2000) The catenin, p120ctn, is a common membrane-associated protein in various epithelial cells and tissues. Histochem Cell Biol 114:147–155

    CAS  PubMed  Google Scholar 

  • Hartsock A, Nelson WJ (2008) Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778:660–669

    Article  CAS  PubMed  Google Scholar 

  • Hatzfeld M (2005) The p120 family of cell adhesion molecules. Eur J Cell Biol 84:205–214

    Article  CAS  PubMed  Google Scholar 

  • 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 109:2767–2778

    CAS  PubMed  Google Scholar 

  • Hatzfeld M, Green KJ, Sauter H (2003) Targeting of p0071 to desmosomes and adherens junctions is mediated by different protein domains. J Cell Sci 116:1219–1233

    Article  CAS  PubMed  Google Scholar 

  • 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 58:113–131

    Article  CAS  PubMed  Google Scholar 

  • 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 13:1665–1676

    Article  CAS  PubMed  Google Scholar 

  • 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 17:1388–1398

    Article  CAS  PubMed  Google Scholar 

  • Hofmann I, Kuhn C, Franke WW (2008) Protein p0071, a major plaque protein of non-desmosomal adhering junctions, is a selective cell type marker. Cell Tissue Res 334:381–399

    Article  CAS  PubMed  Google Scholar 

  • Hofmann I, Schlechter T, Kuhn C, Hergt M, Franke WW (2009) Protein p0071, an armadillo plaque protein that characterizes a specific subtype of adherens junctions. J Cell Sci 122:21–24

    Article  CAS  PubMed  Google Scholar 

  • Izawa I, Nishizawa M, Tomono Y, Ohtakara K, Takahasi T, Inagaki M (2002) Erbin assosciates with p0071, an armadillo protein, at cell–cell junctions of epithelial cells. Genes Cells 7:475–485

    Article  CAS  PubMed  Google Scholar 

  • Jaulin-Bastard F, Arsanto J-P, Le Bivic A, Navarro C, Vély F, Saito H, Marchetto S, Hatzfeld M, Santoni M-J, Birnbaum D, Borg J-P (2002) Interaction between erbin and a catenin-related protein in epithelial cells. J Biol Chem 277:2869–2875

    Article  CAS  PubMed  Google Scholar 

  • Keil R, Wolf A, Hüttelmaier S, Hatzfeld M (2007) Beyond regulation of cell adhesion. Cell Cycle 6:122–125

    CAS  PubMed  Google Scholar 

  • 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 50:129–146

    Article  CAS  PubMed  Google Scholar 

  • 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 46:1423–1434

    CAS  PubMed  Google Scholar 

  • McCrea PD, Park JI (2007) Developmental functions of the p120-catenin sub-family. Biochim Biophys Acta 1773:17–33

    Article  CAS  PubMed  Google Scholar 

  • 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 13:1009–1025

    Article  Google Scholar 

  • 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 98:7795–7800

    Article  CAS  PubMed  Google Scholar 

  • 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 44:147–158

    Article  CAS  PubMed  Google Scholar 

  • Ohno H, Hirabayashi S, Iizuka T, Ohnishi H, Fujita T, Hata Y (2002) Localization of p0071-interacting proteins, plakophilin-related armadillo-repeat protein-interacting protein (papin) and erbin, in epithelial cells. Oncogene 21:7042–7049

    Article  CAS  PubMed  Google Scholar 

  • Paul R, Ewing CM, Robinson JC, Marshall FF, Johnson KR, Wheelock MJ, Isaacs WB (1997) Cadherin-6, a cell adhesion molecule specifically expressed in the proximal renal tubule and renal cell carcinoma. Cancer Res 57:2741–2748

    CAS  PubMed  Google Scholar 

  • 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 14:1452–1463

    Article  PubMed  Google Scholar 

  • Perez-Moreno M, Fuchs E (2006) Catenins: keeping cells from getting their signals crossed. Dev Cell 11:601–612

    Article  CAS  PubMed  Google Scholar 

  • 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 11:3161–3177

    Google Scholar 

  • Prasad SR, Narra VR, Shah R, Humphrey PA, Jagirdar J, Catena JR, Dalrymple NC, Siegel CL (2007) Segmental disorders of the nephron: histopathological and imaging perspective. Brit J Radiol 80:593–602

    Article  CAS  PubMed  Google Scholar 

  • Prozialeck WC, Edwards JR (2007) Cell adhesion molecules in chemically-induced renal injury. Pharmacol Ther 114:74–93

    Article  CAS  PubMed  Google Scholar 

  • Redies C, Heyder J, Kohoutek T, Staes K, Van Roy F (2008) Expression of protocadherin-1 (Pcdh1) during mouse development. Dev Dyn 237:2496–2505

    Article  CAS  PubMed  Google Scholar 

  • 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 14:8333–8342

    CAS  PubMed  Google Scholar 

  • Schmidt A, Jäger S (2005) Plakophilins—hard work in the desmosome, recreation in the nucleus? Eur J Cell Biol 84:189–204

    Article  CAS  PubMed  Google Scholar 

  • 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 64:291–306

    CAS  PubMed  Google Scholar 

  • Setzer SV, Calkins CC, Garner J, Summers S, Green KJ, Kowalczyk AP (2004) Comparative analysis of armadillo family proteins in the regulation of A431 epithelial cell junction assembly, adhesion and migration. J Invest Dermatol 123:426–433

    Article  CAS  PubMed  Google Scholar 

  • Shen SS, Bhuvaneswari K, Chirala R, Amato RJ, Truong LD (2005) Kidney-specific cadherin, a specific marker for the distal portion of the nephron and related renal neoplasms. Modern Pathol 18:933–940

    Article  CAS  Google Scholar 

  • Stahl B, Diehlmann A, Südhof TC (1999) Direct interaction of alzheimer’s disease-related presenilin 1 with armadillo protein p0071. J Biol Chem 274:9141–9148

    Article  CAS  PubMed  Google Scholar 

  • Störkel S, Steart PV, Drenckhahn D, Thoenes W (1989) The human chromophobe cell renal carcinoma: its probable relation to intercalated cells of the collecting duct. Virchows Arch B Cell Pathol Incl Mol Pathol 56:237–245

    Article  PubMed  Google Scholar 

  • Tani T, Laitinen L, Kangas L, Lehto VP, Virtanen I (1995) Expression of E- and N-cadherin in renal cell carcinomas, in renal cell lines in vitro and in their xenografts. Int J Cancer 64:407–414

    Article  CAS  PubMed  Google Scholar 

  • Walter B, Schlechter T, Hergt M, Berger I, Hofmann I (2008) Differential expression pattern of protein ARVCF in nephron segments of human and mouse kidney. Histochem Cell Biol 130:943–956

    Article  CAS  PubMed  Google Scholar 

  • Wolf A, Keil R, Götzl O, Mun A, Schwarze K, Lederer M, Hüttelmaier S, Hatzfeld M (2006) The armadillo protein p0071 regulates Rho signaling during cytokinesis. Nat Cell Biol 8:1432–1440

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank A. Wiss (Department of Pathology, University of Heidelberg) for competent help in sectioning paraffin-embedded human tissues. For continuous and generous support we thank Prof. Dr. W. W. Franke (Helmholtz Group for Cell Biology, German Cancer Research Center). We gratefully acknowledge the critical comments of Dr. L. Murrells (Helmholtz International Graduate School for Cancer Research, German Cancer Research Center).

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Authors and Affiliations

  1. Joint Research Division Vascular Biology of the Medical Faculty Mannheim, University of Heidelberg, and the German Cancer Research Center, CBTM, Ludolf-Krehl-Strasse 13-17, 68167, Mannheim, Germany

    Britta Walter, Ulrike Krebs & Ilse Hofmann

  2. Institute of Pathology, University of Heidelberg, Im Neuenheimer Feld 220/221, 69120, Heidelberg, Germany

    Britta Walter & Irina Berger

  3. Institute of Pathology, Klinikum Kassel, Mönchebergstrasse 41-43, 34125, Kassel, Germany

    Irina Berger

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  1. Britta Walter
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  4. Ilse Hofmann
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Correspondence to Ilse Hofmann.

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Walter, B., Krebs, U., Berger, I. et al. Protein p0071, an armadillo plaque protein of adherens junctions, is predominantly expressed in distal renal tubules. Histochem Cell Biol 133, 69–83 (2010). https://doi.org/10.1007/s00418-009-0645-6

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