Skip to main content

Advertisement

SpringerLink
Log in

N-Glycans carried by Tamm-Horsfall glycoprotein have a crucial role in the defense against urinary tract diseases

  • Mini Review
  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Tamm-Horsfall glycoprotein (THGP), produced exclusively by renal cells from the thick ascending limb of Henle's loop, is attached by a glycosyl-phosphatidylinositol (GPI)-anchor to the luminal face of the cells. Urinary excretion of THGP (50–100 mg/day) occurs upon proteolytic cleavage of the large ectodomain of the GPI-anchored form. N-Glycans, consisting of a large repertoire of sialylated polyantennary chains and high-mannose structures, account for approximately 30% of the weight of human urinary THGP. We describe: (i) the involvement of urinary THGP high-mannose glycans in defense against infections of the urinary tract, caused by type-1 fimbriated Escherichia coli, which recognize high-mannose structures, (ii) the role of GalNAcβ1-4(NeuAcα2-3)Galβ1-4GlcNAcβ1-3Gal (Sda determinant) carried by human THGP in protecting the distal nephron from colonization of type-S fimbriated E. coli which recognise NeuAcα2-3Gal, (iii) the inhibitory effect of sialylated THGP on crystal aggregation of calcium oxalate and calcium phosphate, thus preventing nephrolithiasis. Finally, we outline the importance of N-glycans in promoting the polymerization of THGP, a process resulting in the formation of homopolymers with an M r of several million in urine. Since THGP defense against diseases of the urinary tract mainly consists in binding damaging agents, its ability to behave as a multivalent ligand significantly enhances this protective role.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Abbreviations

COD:

calcium oxalate dihydrate

COM:

calcium oxalate monohydrate

E. coli :

Escherichia coli

GPI:

glycosyl-phosphatidylinositol

MCKD2:

autosomal dominant medullary cystic kidney disease 2, PMN, polymorphonuclear leukocytes

TAL:

thick ascending limb of Henle's loop

THGP:

Tamm-Horsfall glycoprotein

UPI:

uroplakins

UTI:

urinary tract infections

References

  1. Tamm I, Horsfall FL, Characterization and separation of an inhibitor of viral Hemagglutination present in urine, Proc Soc Exp Biol Med 74, 108–14 (1950).

    CAS  Google Scholar 

  2. Gottschalk A, Carbohydrate residue of a urine mucoprotein inhibiting Influenza virus haemagglutination, Nature 170, 662–3 (1952).

    PubMed  CAS  Google Scholar 

  3. Odin L, Carbohydrate residue of a urine mucoprotein inhibiting Influenza virus haemagglutination, Nature 170, 663–4 (1952).

    PubMed  CAS  Google Scholar 

  4. Grant AM, Neuberger A, The development of a radioimmunoassay for the measurement of urinary Tamm-Horsfall glycoprotein in the presence of sodium dodecyl sulphate, Clinicalscience 44, 163–79 (1973).

    CAS  Google Scholar 

  5. Hoyer JR, Sisson SP, Vernier RL, Tamm-Horsfall glycoprotein: ultrastructural immunoperoxidase localization in rat kidney, Lab Invest 41, 168–73 (1979).

    PubMed  CAS  Google Scholar 

  6. Sikri KL, Foster CL, Bloomfield FJ, Marshall RD, Localization by immunofluorescence and by light- and electron-microscopic immunoperoxidase techniques of Tamm-Horsfall glycoprotein in adult hamster kidney, Biochem J 181, 525–32 (1979).

    PubMed  CAS  Google Scholar 

  7. Sikri KL, Foster CL, MacHugh N, Marshall RD, Localization of Tamm-Horsfall glycoprotein in the human kidney using immuno-fluorescence and immuno-electron microscopical techniques, J Anat 132, 597–605 (1981).

    PubMed  CAS  Google Scholar 

  8. Bachmann S, Metzger R, Bunnemann B, Tamm-Horsfall protein-mRNA synthesis is localized to the thick ascending limb of Henle's loop in rat kidney, Histochemistry 94, 517–23 (1990).

    Article  PubMed  CAS  Google Scholar 

  9. Gokhale JA, Glenton PA, Khan SR, Characterization of Tamm-Horsfall protein in a rat nephrolithiasis model, J Urol 166, 1492–7 (2001).

    PubMed  CAS  Google Scholar 

  10. Cavallone D, Malagolini N, Minni F, Serafini-Cessi F, Distribution in human kidney of Tamm-Horsfall glycoprotein and of glycosyltransferases involved in the biosynthesis of the Sda antigen, Giornale Italiano di Nefrologia 4, 418–24 (2001). (in Italian)

    Google Scholar 

  11. Pennica D, Kohr WJ, Kuang WJ, Glaister D, Aggarwal BB, Chen EY, Goeddel DV, Identification of human uromodulin as the Tamm-Horsfall urinary glycoprotein, Science 236, 83–8 (1987).

    PubMed  CAS  Google Scholar 

  12. Rindler MJ, Naik SS, Li N, Hoops TC, Peraldi MN, Uromodulin (Tamm-Horsfall glycoprotein/uromucoid) is a phosphatidylinositol-linked membrane protein, J Biol Chem 265, 20784–9 (1990).

    PubMed  CAS  Google Scholar 

  13. Malagolini N, Cavallone D, Serafini-Cessi F, Intracellular transport, cell-surface exposure and release of recombinant Tamm-Horsfall glycoprotein, Kidney Int 52, 1340–50 (1997).

    PubMed  CAS  Google Scholar 

  14. Kreft B, Jabs WJ, Laskay T, Klinger M, Solbach W, Kumar S, van Zandbergen G, Polarized expression of Tamm-Horsfall protein by renal tubular epithelial cells activates human granulocytes, Infect Immun 70, 2650–6 (2002).

    Article  PubMed  CAS  Google Scholar 

  15. Cavallone D, Malagolini N, Serafini-Cessi F, Mechanism of release of urinary Tamm-Horsfall glycoprotein from the kidney GPI-anchored counterpart, Biochem Biophys Res Commun 280, 110–14 (2001).

    Article  PubMed  CAS  Google Scholar 

  16. Fukuoka S, Kobayashi KI, Analysis of the C-terminal structure of urinary Tamm-Horsfall protein reveals that the release of glycosyl phosphatidylinositol-anchored counterpart from the kidney occurs by phenylalanine-specific proteolysis, Biochem Biophys Res Commun 289, 1044–8 (2001).

    Article  PubMed  CAS  Google Scholar 

  17. Fletcher AP, Neuberger A, Ratcliffe WA, Tamm-Horsfall urinary glycoprotein. The subunit structure, Biochem J 120, 425–32 (1970).

    PubMed  CAS  Google Scholar 

  18. Fletcher AP, Neuberger A, Ratcliffe WA, Tamm-Horsfall urinary glycoprotein. The chemical composition, Biochem J 120, 417–24 (1970).

    PubMed  CAS  Google Scholar 

  19. Dunstan DR, Grant AMS, Marshall RD, Neuberger A, A protein immunologically similar to Tamm-Horsfall glycoprotein, produced by cultured baby hamster kidney cells, Proc Soc Lond (B Biol Sci) 186, 297–316 (1974).

    CAS  Google Scholar 

  20. Williams J, Marshall RD, van Halbeek H, and Vliegenthart JFG, Structural analysis of the carbohydrate moieties of human Tamm-Horsfall glycoprotein, Carbohydr Res 134, 141–55 (1984).

    Article  PubMed  CAS  Google Scholar 

  21. Hard K, Van Zadelhoof G, Moonen P, Kamerling JP, Vliegenthart JFG, The Asn-linked carbohydrate chains of human Tamm-Horsfall glycoprotein of one male, Eur J Biochem 209, 895–915 (1992).

    Article  PubMed  CAS  Google Scholar 

  22. van Rooijen JJM, Kamerling JP, Vliegenthart JFG, Sulfated di-, tri- and tetraantennary N-glycans in human Tamm-Horsfall glycoprotein, Eur J Biochem 256, 471–87 (1998).

    Article  PubMed  CAS  Google Scholar 

  23. van Rooijen JJM, Kamerling JP, Vliegenthart JFG, The abundance of additional N-acetyllactosamine units in N-linked tetraantennary oligosaccharides of human Tamm-Horsfall glycoprotein is a donor-specific feature, Glycobiology 8, 1065–75 (1998).

    PubMed  CAS  Google Scholar 

  24. van Rooijen JJM, Voskamp AF, Kamerling JP, Vliegenthart JFG, Glycosylation sites and site-specific glycosylation in Tamm-Horsfall glycoprotein, Glycobiology 9, 21–30 (1999).

    Article  PubMed  CAS  Google Scholar 

  25. van Rooijen JJM, Hermentin P, Kamerling JP, Vliegenthart JFG, The patterns of the complex- and oligomannose-type glycans of uromodulin (Tamm-Horsfall glycoprotein) in the course of pregnancy, Glycoconjugate J 18, 539–46 (2001).

    Article  CAS  Google Scholar 

  26. Serafini-Cessi F, Malagolini N, Dall'Olio F, A tetraantennary glycopeptide from human Tamm-Horsfall glycoprotein inhibits agglutination of desialylated erythrocytes induced by leucoagglutinin, Biosci Rep 4, 973–8 (1984).

    PubMed  CAS  Google Scholar 

  27. Serafini-Cessi F, Franceschi C, Sperti S, Specific interaction of human Tamm-Horsfall glycoprotein with leucoagglutinin, a lectin from Phaseolus vulgaris (Red kidney bean), Biochem J 183, 381–8 (1979).

    PubMed  CAS  Google Scholar 

  28. Abbondanza A, Franceschi C, Licastro F, Serafini-Cessi F, Properties of glycopeptide isolated from human Tamm-Horsfall glycoprotein, Biochem J 187, 525–8 (1980).

    PubMed  CAS  Google Scholar 

  29. Serafini-Cessi F, Dall'Olio F, Malagolini N, High-mannose oligosaccharides from human Tamm-Horsfall glycoprotein, Biosci Rep 4, 269–74 (1984).

    PubMed  CAS  Google Scholar 

  30. Dall'Olio F, de Kanter FJJ, van den Eijnden DH, Serafini-Cessi F, Structural analysis of the preponderant high-mannose oligosaccharides of human Tamm-Horsfall glycoprotein, Carbohydr Res 178, 327–32 (1988).

    Article  PubMed  Google Scholar 

  31. Nielsen S, Smith BL, Christensen EI, Knepper MA, Agre P, CHIP28 water channels are localized in constitutively water-permeable segments of the nephron, J Cell Biol 120, 371–83 (1993).

    Article  PubMed  CAS  Google Scholar 

  32. Hannan LA, Edidin M, Traffic, polarity, and detergent solubility of a glycosylphosphatidylinositol-anchored protein after LDL-deprivation of MDCK cells, J Cell Biol 133, 1265–76 (1996).

    Article  PubMed  CAS  Google Scholar 

  33. Muchmore AV, Decker JM, Uromodulin: a unique 85-kilodalton immunosuppressive glycoprotein isolated from urine of pregnant women, Science 229, 479–81 (1985).

    PubMed  CAS  Google Scholar 

  34. Moonen P, Gaffner R, Wingfield P, Native cytokines do not bind to uromodulin (Tamm-Horsfall glycoprotein), FEBS Lett 226, 314–8 (1988).

    Article  PubMed  CAS  Google Scholar 

  35. Serafini-Cessi F, Malagolini N, Cavallone D, Tamm-Horsfall glycoprotein: Biology and clinical relevance, Am J Kidney Dis 42, 658–76 (2003).

    Article  PubMed  CAS  Google Scholar 

  36. Pak J, Pu Y, Zhang ZT, Hasty DL, Wu XR, Tamm-Horsfall protein binds to type 1 fimbriated Escherichia coli and prevents E. coli from binding to uroplakin Ia and Ib receptors, J Biol Chem 276, 9924–30 (2001).

    Article  PubMed  CAS  Google Scholar 

  37. Cavallone D, Malagolini N, Monti A, Wu XR, Serafini-Cessi F, Variation of high mannose chains of Tamm-Horsfall glycoprotein confers differential binding to type1-fimbriated Escherichia coli, J Biol Chem 279, 216–22 (2004).

    PubMed  CAS  Google Scholar 

  38. Bates JM, Raffi HM, Prasadan K, Mascarenhas R, Laszik Z, Maeda N, Hultgren SJ, Kumar S, Tamm-Horsfall protein knockout mice are more prone to urinary tract infection, Kidney Int 65, 791–7 (2004).

    Article  PubMed  CAS  Google Scholar 

  39. Mo L, Zhu XH, Huang HY, Hasty DL, Wu XR, Ablation of the Tamm-Horsfall protein gene increases susceptibility of mice to bladder colonization by type 1-fimbriated Escherichia coli, Am J Physiol Renal Physiol 286, F795–802 (2004).

    Google Scholar 

  40. Khan SR, Kok DJ, Modulators of urinary stone formation, Front Biosc 9, 1450–82 (2004).

    CAS  Google Scholar 

  41. Mo L, Huang HY, Zhu XH, Shapiro E, Hasty DL, Wu XR, Tamm-Horsfall protein is a critical renal defense factor protecting against calcium oxalate crystal formation, Kidney Int 66, 1159–66 (2004).

    Article  PubMed  CAS  Google Scholar 

  42. Wangsiripaisan A, Gengaro PE, Edelstein CL, Schrier RW, Role of polymeric Tamm-Horsfall protein in cast formation: oligosaccharide and tubular fluid ions, Kidney Int 59, 932–40 (2001).

    Article  PubMed  CAS  Google Scholar 

  43. Huang ZQ, Sanders PW, Biochemical interaction between Tamm-Horsfall glycoprotein and Ig light chains in the pathogenesis of cast nephropathy, Lab Invest 73, 810–17 (1995).

    PubMed  CAS  Google Scholar 

  44. Mulvey MA, Adhesion and entry of uropathogenic Escherichia coli, Cell Microbiol 4, 257–71 (2002).

    Article  PubMed  CAS  Google Scholar 

  45. Barnett BJ, Stephens DS, Urinary tract infection: an overview, Am J Med Sci 314, 245–9 (1997).

    PubMed  CAS  Google Scholar 

  46. Ofek I, Mirelman D, Sharon N, Aderence of Escherichia coli to microbal cells mediated by mannose receptors, Nature 265, 623–5 (1977).

    Article  PubMed  CAS  Google Scholar 

  47. Aronson M, Medalia O, Schory D, Mirelman D, Sharon N, Ofek I, Prevention of colonization of the urinary tract of mice with Escherichia coli by blocking of bacterial adherence with methyl α-D-mannopyranoside, J Infect Dis 139, 329–32 (1979).

    PubMed  CAS  Google Scholar 

  48. Hanson MS, Brinton CC, Identification and characterization of E.coli type-1 pilus tip adhesion protein Nature 332, 265–8 (1988).

    Google Scholar 

  49. Martinez JJ, Mulvey MA, Schilling JD, Pinker JS, Hultgren SJ, Type 1 pilus-mediated bacterial invasion of bladder epithelial cells, EMBO J 19, 2803–12 (2000).

    Article  PubMed  CAS  Google Scholar 

  50. Sokurenko EV, Courtney HS, Maslow J, Siitonen A, Hasty DL, Quantitative differences in adhesiveness of type 1 fimbriated Escherichia coli due to structural differences in fimH genes, J Bacteriol 177, 3680–6 (1995).

    PubMed  CAS  Google Scholar 

  51. Sokurenko EV, Chesnokova V, Doyle RJ, Hasty DL, Diversity of the Escherichia coli type 1 fimbrial lectin, Differential binding to mannosides and uroepithelial cells, J Biol Chem 272, 17880–6 (1997).

    Article  PubMed  CAS  Google Scholar 

  52. Sokurenko EV, Chesnokova V, Dykhuizen DE, Ofek I, Wu XR, Krogfelt KA, Struve C, Schembri MA, Hasty DL, Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin, Proc Natl Acad Sci USA 95, 8922–6 (1998).

    Article  PubMed  CAS  Google Scholar 

  53. Wu XR, Sun TT, Molecular cloning of a 47 kDa tissue-specific and differentiation-dependent urothelial cell-surface glycoprotein, J Cell Sci 106, 31–43 (1993).

    PubMed  CAS  Google Scholar 

  54. Malagolini N, Cavallone D, Wu XR, Serafini-Cessi F, Terminal glycosylation of bovine uroplakin III, One of the major integral-membrane glycoproteins of mammalian bladder, Biochem Biophys Acta, 1475, 231–7 (2000).

    Google Scholar 

  55. Wu XR, Lin JH, Walz T, Haner M, Yu J, Aebi U, Sun TT, Mammalian uroplakins. A group of highly conserved urothelial differentiation-related membrane proteins, J Biol Chem 269, 13716–24 (1994).

    PubMed  CAS  Google Scholar 

  56. Wu XR, Medina JJ, Sun TT, Selective interactions of UP Ia and UP Ib, two members of the transmembrane 4 superfamily, with distinct single transmembrane-domained proteins in differentiated urothelial cells, J Biol Chem 270, 29752–9 (1995).

    PubMed  CAS  Google Scholar 

  57. Wu XR, Sun TT, Medina JJ, In vitro binding of type 1-fimbriated Escherichia coli to uroplakins Ia and Ib: relation to urinary tract infections, Proc Natl Acad Sci USA 93, 9630–5 (1996).

    PubMed  CAS  Google Scholar 

  58. Ikaheimo R, Siitonen A, Heiskanen T, Karkkainen U, Kuosmanen P, Lipponen P, Makela PH, Recurrence of urinary tract infection in a primary care setting: analysis of a 1-year follow-up of 179 women, Clin Infect Dis 22, 91–9 (1996).

    PubMed  CAS  Google Scholar 

  59. Orskov I, Ferencz A, Orskov F, Tamm-Horsfall protein or uromucoid is the normal urinary slime that traps type 1 fimbriated Escherichia coli, Lancet 1, 887 (1980).

    Google Scholar 

  60. Parkkinen J, Virkola R, Korhonen TK, Identification of factors in human urine that inhibit the binding of Escherichia coli adhesins, Infect Immun 56, 2623–30 (1988).

    PubMed  CAS  Google Scholar 

  61. Reinhart HH, Obedeanu N, Sobel JD, Quantitation of Tamm-Horsfall protein binding to uropathogenic Escherichia coli and lectins, J Infect Dis 162, 1335–40 (1990).

    PubMed  CAS  Google Scholar 

  62. Benting JH, Rietveld AG, Simons K, N-glycans mediate the apical sorting of a GPI-anchored, raft associated protein in Madin-Darby canine kidney cells, J Cell Biol 146, 313–20 (1999).

    Article  PubMed  CAS  Google Scholar 

  63. Sherblom AP, Smagula RM, High-mannose chains of mammalian glycoproteins, Methods Mol Biol 14, 143–9 (1993).

    PubMed  CAS  Google Scholar 

  64. Serafini-Cessi F, Malagolini N, Hoops TC, Rindler MJ, Biosynthesis and oligosaccharide processing of human Tamm-Horsfall glycoprotein permanently expressed in HeLa cells, Biochem Biophys Res Commun 194, 784–90 (1993).

    PubMed  CAS  Google Scholar 

  65. Jovine L, Qi H, Williams Z, Litscher E, Wassarman PM, The ZP domain is a conserved module for polymerization of extracellular proteins, Nature Cell Biol 4, 457–61 (2000).

    Google Scholar 

  66. Firon N, Ofek I, Sharon N, Carbohydrate-binding sites of the mannose-specific fimbrial lectins of enterobacteria, Infect Immun 43, 1088–90 (1984).

    PubMed  CAS  Google Scholar 

  67. Neeser JR, Koellreutter B, Wuersch P, Oligomannoside-type glycopeptides inhibiting adhesion of Escherichia coli strains mediated by type 1 pili: preparation of potent inhibitors from plant glycoproteins, Infect Immun 52, 428-36 (1986).

    Google Scholar 

  68. Sharon N, Bacterial lectins, cell-cell recognition and infectious disease, FEBS Lett 217, 145–57 (1987).

    Article  PubMed  CAS  Google Scholar 

  69. Kuriyama SM, Silverblatt FJ, Effect of Tamm-Horsfall urinary glycoprotein on phagocytosis and killing of type I-fimbriated Escherichia coli, Infect Immun 51, 193–8 (1986).

    PubMed  CAS  Google Scholar 

  70. Hart TC, Gorry MC, Hart PS, Woodard AS, Shihabi Z, Sandhu J, Shirts B, Xu L, Zhu H, Barmada MM, Bleyer AJ, Mutations of the UMOD gene are responsible for medullary cystic kidney disease 2 and familial juvenile hyperuricaemic nephropathy, J Med Genet 39, 882–92 (2002).

    Article  PubMed  CAS  Google Scholar 

  71. Wolf MT, Mucha BE, Attanasio M, Zalewski I, Karle SM, Neumann HP, Rahman N, Bader B, Baldamus CA, Otto E, Witzgall R, Fuchshuber A, Hildebrandt F, Mutations of the Uromodulin gene in MCKD type 2 patients cluster in exon 4, which encodes three EGF-like domains, Kidney Int 64, 1580–7 (2003).

    Google Scholar 

  72. Kudo E, Kamatani N, Tezuka O, Taniguchi A, Yamanaka H, Yabe S, Osabe D, Shinohara S, Nomura K, Segawa M, Miyamoto T, Moritani M, Kunika K, Itakura M, Familial juvenile hyperuricemic nephropathy: Detection of mutations in the uromodulin gene in five Japanese families, Kidney Int 65, 1589–97 (2004).

    Article  PubMed  CAS  Google Scholar 

  73. Rampoldi L, Caridi G, Santon D, Boaretto F, Bernascone I, Lamorte G, Tardanico R, Dagnino M, Colussi G, Scolari F, Ghiggeri GM, Amoroso A, Casari G, Allelism of MCKD, FJHN and GCKD caused by impairment of uromodulin export dynamics, Hum Mol Genet 12, 3369–84 (2003).

    Article  PubMed  CAS  Google Scholar 

  74. Macvie SL, Morton JA, Picles MM, The reaction and inheritance of a new blood group antigen Sda, Vox Sang 13, 485–92 (1967).

    Article  Google Scholar 

  75. Renton PH, Howell P, Ikin E, Giles CM, Goldsmith KLG, Anti- Sda of a new blood group antibody, Vox Sang 13, 493–501 (1967).

    Google Scholar 

  76. Morton JA, Picles MM, Terry AM, The Sda blood group antigen in tissues and body fluid, Vox Sang 19, 151–61 (1970).

    PubMed  CAS  Google Scholar 

  77. Soh CP, Morgan WTJ, Watkins WM, Donald ASR, The relationship between the N-acetylgalactosamine content and the blood group Sda activity of Tamm and Horsfall urinary glycoprotein, Biochem Biophys Res Commun 93, 1132–9 (1980).

    Article  PubMed  CAS  Google Scholar 

  78. Donald ASR, Yates AD, Soh CPC, Morgan WTJ, Watkins WM, A blood group Sda-active pentasaccharide isolated from Tamm-Horsfall urinary glycoprotein, Biochem Biophys Res Commun 115, 625–31 (1983).

    Article  PubMed  CAS  Google Scholar 

  79. Donald ASR, Feeney J, Oligosaccharides obtained from a blood group Sd(a+) Tamm-Horsfall glycoprotein, an n.m.r. study, Biochem J 236, 821–8 (1986).

    PubMed  CAS  Google Scholar 

  80. Watkins WM, Sda and Cad antigen. Molecular basis of major human blood group antigen, edited by Cartron JP and Rouger F (Plenum Press, New York, 1995), vol 6, pp. 351–75.

  81. Wu JH, Watkins WM, Chen CP, Song SC, Chow LP, Lin JY, Interaction of a human blood group Sd (a-) Tamm-Horsfall glycoprotein with applied lectins, FEBS Lett 384, 231–4 (1996).

    Article  PubMed  CAS  Google Scholar 

  82. Wu AM, Watkins WM, Chen CP, Song SC, Chow LP, Lin JY, Native and/or asialo-Tamm-Horsfall glycoproteins Sd(a+) are important receptors for Triticum vulgaris (wheat germ) agglutinin and for three toxic lectins (abrin-a, ricin and mistletoe toxic lectin-I), FEBS Lett 371, 32–4 (1995).

    Article  PubMed  CAS  Google Scholar 

  83. Wu AM, Watkins WM, Chen CP, Song SC, Chow LP, Lin JY, Native and asialo-Tamm-Horsfall glycoproteins as important ligands for the detection of GalNAcβ1→ and Galβ1→4GlcNAc active lectins, Biochem Biophys Res Commun 209 103–10 (1995).

    Article  PubMed  CAS  Google Scholar 

  84. Serafini-Cessi F, Dall'Olio F, Guinea-pig kidney β-N-acetylgalactosaminyl-transferase towards Tamm-Horsfall glycoprotein. Requirement of sialic acid in the acceptor for transferase activity, Biochem J 215, 483–9 (1983).

    PubMed  CAS  Google Scholar 

  85. Serafini-Cessi F, Dall'Olio F, Malagolini N, Characterization of N-acetyl-D-galactosaminyltransferase from guinea-pig kidney involved in the biosynthesis of Sda antigen associated with Tamm-Horsfall glycoprotein, Carbohydr Res 151, 65–76 (1986).

    Article  PubMed  CAS  Google Scholar 

  86. Serafini-Cessi F, The Sda antigen and its biosynthetic enzyme: differentiation-dependent and onco-developmentally regulated expression, Trends Glycosci Glycotechnol 42, 279–95 (1996).

    Google Scholar 

  87. Smith PL, Lowe JB, Molecular cloning of a murine N-acetylgalactosamine transferase that determines expression of the T lymphocyte-specific CT oligosaccharide differentiation antigen, J Biol Chem 269, 15162–71 (1994).

    PubMed  CAS  Google Scholar 

  88. Piller F, Blanchard D, Huet M, Cartron JP, Identification of a α-NeuAc-(2-3)- β-D-galactopyranosyl N-acetyl- β-D-galactopyranosyltransferase in human kidney, Carbohydr Res 149, 171–84 (1986).

    Article  PubMed  CAS  Google Scholar 

  89. Malagolini N, Dall'Olio F, Di Stefano G, Minni F, Marrano D, Serafini-Cessi F, Expression of UDP-GalNAc:NeuAcα2,3Gal β-1,4(GalNAc to Gal) N-acetylgalactosaminyltransferase involved in the synthesis of Sda antigen in human large intestine and colorectal carcinomas, Cancer Res 49, 6466–70 (1989).

    Google Scholar 

  90. Serafini-Cessi F, Malagolini N, Dall'Olio F, Characterization and partial purification of β-N-acetyl-galactosaminyltransferase from urine of Sd(a+) individuals, Arch Biochem Biophys 266, 573–82 (1988).

    PubMed  CAS  Google Scholar 

  91. Capon C, Maes E, Michalski JC, Leffler H, Kim YS, Sd(a)-antigen-like structures carried on core 3 are prominent features of glycans from the mucin of normal human descending colon, Biochem J 358, 657–64 (2001).

    PubMed  CAS  Google Scholar 

  92. Robbe C, Capon C, Maes E, Rousset M, Zweibaum A, Zanetta JP, Michalski JC, Evidence of regio-specific glycosylation in human intestinal mucins: Presence of an acidic gradient along the intestinal tract, J Biol Chem 278, 46337–348 (2003).

    PubMed  CAS  Google Scholar 

  93. Dall'Olio F, Malagolini N, Serafini−Cessi F, Tissue distribution and age−dependent expression of β-4-N-acetylgalactosaminyltransferase in guinea−pig, Biosci Rep 7, 925–32 (1987).

    Article  PubMed  Google Scholar 

  94. Dall'Olio F, Malagolini N, DiStefano G, Ciambella M and Serafini-Cessi F, Postnatal development of rat colon epithelial cells is associated with changes in the expression of β1,4-N-acetylgalactosaminyltransferase involved in the synthesis of Sda antigen and of α2,6 sialyltransferase towards N-acetyllactosamine, Biochem J 270, 519–24 (1990).

    Google Scholar 

  95. Rohfritsch PF, Rinnbauer M, Vliegenthart JF, Kamerling JP, Donor specificity in the glycosylation of Tamm-Horsfall glycoprotein: Conservation of the Sd(a) determinant in pairs of twins, Glycobiology 14, 365–72 (2004).

    Article  PubMed  CAS  Google Scholar 

  96. Watkins WM, Greenwell P, Yates AD, Johnson PH, Regulation of expression of carbohydrate blood group antigens, Biochimie 70, 1597–611 (1988).

    Article  PubMed  CAS  Google Scholar 

  97. Runnel PL, Moon HV, Schneider RA, Development of resistance with host age to adhesion of K99+ and Escherichia coli to isolated intestinal epithelial cells, Infec Immunol 28, 298–300 (1980).

    Google Scholar 

  98. Hagberg L, Jodal U, Korhonen TK, Lidin-Janson G, Lindberg U, Svanborg Eden C, Adhesion, haemagglutination, and virulence of Escherichia coli causing urinary tract infection, Infect Immunol 31, 564–70 (1981).

    CAS  Google Scholar 

  99. Coe FL, Parks JH, Asplin JR, The pathogenesis and treatment of kidney stones, N Eng J Med 327, 1141–52 (1992).

    Article  CAS  Google Scholar 

  100. Marangella M, Vitale C, Petrarulo M, Bagnis C, Bruno M, Ramello A, Renal stones: from metabolic to physicochemical abnormalities. How useful are inhibitors? J Nephrology 13(Suppl 3), S51–60 (2000).

    Google Scholar 

  101. Hess B, Nakagawa Y, Coe FL, Inhibition of calcium oxalate monohydrate crystal aggregation by urine proteins, Am J Physiol Renal Physiol 257, 99–106 (1989).

    Google Scholar 

  102. Nakagawa Y, Abram V, Kezdy FJ, Kaiser ET, Coe FL, Purification and characterization of the principal inhibitor of calcium oxalate monohydrate crystal growth in human urine, J Biol Chem 258, 12594–600 (1983).

    PubMed  CAS  Google Scholar 

  103. Worcester EM, Blumenthal SS, Beshensky AM, Lewand DL, The calcium oxalate crystal growth inhibitor protein produced by mouse kidney cortical cells in culture is osteopontin, J Bone Miner Res 7, 1029–36 (1992).

    Article  PubMed  CAS  Google Scholar 

  104. Shiraga H, Min W, VanDusen WJ, Clayman MD, Miner D, Terrell CH, Sherbotie JR, Foreman JW, Przysiecki C, Neilson EG, et al, Inhibition of calcium oxalate crystal growth in vitro by uropontin: another member of the aspartic acid-rich protein superfamily, Proc Natl Acad Sci USA 89, 426–30 (1992).

    PubMed  CAS  Google Scholar 

  105. Ryall RL, Grover PK, Stapleton AM, Barrell DK, Tang Y, Simpson RJ, The urinary F1 activation peptide of human prothrombin is a potent inhibitor of calcium oxalate crystallization in undiluted human urine in vitro, Clin Sci 89, 533–41 (1995).

    PubMed  CAS  Google Scholar 

  106. Hess B, Kok DJ, Nucleation, growth and aggregation of stone forming crystals. In Kidney Stones, Medical and Surgical Management, edited by Coe FL, Favus MJ, Fak CYC, Parks JH, Preminger GM (Lippincott-Raven Publishers, Philadelphia, 1996), pp. 3–32

  107. Romero MC, Nocera S, Nesse AB, Decreased Tamm-Horsfall protein in lithiasic patients, Clin Biochem 30, 63–7 (1997).

    PubMed  CAS  Google Scholar 

  108. Ganter K, Bongartz D, Hesse A, Tamm-Horsfall protein excretion and its relation to citrate in urine of stone-forming patients, Urology 53, 492–5 (1999).

    Article  PubMed  CAS  Google Scholar 

  109. Bichler KH, Mittermuller B, Strohmaier WL, Feil G, Eipper E, Excretion of Tamm-Horsfall protein in patients with uric acid stones, Urol Int 62, 87–92 (1999).

    Article  PubMed  CAS  Google Scholar 

  110. Schnierle P, A simple diagnostic method for the differentiation of Tamm-Horsfall glycoproteins from healthy probands and those from recurrent calcium oxalate renal stone formers, Experientia 51, 1068–72 (1995).

    Article  PubMed  CAS  Google Scholar 

  111. Boeve ER, Cao LC, De Bruijn WC, Robertson WG, Romijn JC, Schroder FH, Zeta potential distribution on calcium oxalate crystal and Tamm-Horsfall protein surface analyzed with Doppler electrophoretic light scattering, J Urol 152, 531–6 (1994).

    PubMed  CAS  Google Scholar 

  112. Grover PK, and Resnick MI, Evidence for the presence of abnormal proteins in the urine of recurrent stone formers, J Urol 153, 1716–21 (1995).

    PubMed  CAS  Google Scholar 

  113. Trewick AL, and Rumsby G, Isoelectric focusing of native urinary uromodulin (Tamm-Horsfall protein) shows no physicochemical differences between stone formers and non-stone formers, Urol Res 27, 250–4 (1999).

    Article  PubMed  CAS  Google Scholar 

  114. Marengo SR, Chen DH, Kaung HL, Resnick MI, Yang L, Decreased renal expression of the putative calcium oxalate inhibitor Tamm-Horsfall protein in the ethylene glycol rat model of calcium oxalate urolithiasis, J Urol 167, 2192–7 (2002).

    PubMed  CAS  Google Scholar 

  115. Hallson PC, Choong SK, Kasidas GP, Samuell CT, Effects of Tamm-Horsfall protein with normal and reduced sialic acid content upon the crystallization of calcium phosphate and calcium oxalate in human urine, Br J Urol 80, 533-38 (1997).

    Google Scholar 

  116. Chen WC, Lin HS, Chen HY, Shih CH, Li CW, Effects of Tamm-Horsfall protein and albumin on calcium oxalate crystallization and importance of sialic acids, Mol Urol 5, 1–5 (2001).

    PubMed  Google Scholar 

  117. Wesson JA, Johnson RJ, Mazzali M, Beshensky AM, Stietz S, Giachelli C, Liaw L, Alpers CE, Couser WG, Kleinman JG, Hughes J, Osteopontin is a critical inhibitor of calcium oxalate crystal formation and retention in renal tubules, J Am Soc Nephrol 14, 139–47 (2003).

    Article  PubMed  CAS  Google Scholar 

  118. Lieske JC, Toback FG, Deganello S, Sialic acid-containing glycoproteins on renal cells determine nucleation of calcium oxalate dihydrate crystals, Kidney Int 60, 1784–91 (2001).

    Article  PubMed  CAS  Google Scholar 

  119. Verkoelen CF, van der Boom BG, Kok DJ, Romijn JC, Sialic acid and crystal binding, Kidney Int 57, 1072–82 (2000).

    Article  PubMed  CAS  Google Scholar 

  120. Bayer ME, An electron microscope examination of urinary mucoprotein and its interaction with influenza virus, J Cell Biol 21, 265–74 (1964).

    Article  PubMed  CAS  Google Scholar 

  121. Stevenson FK, Cleave AJ, Kent PW, The effect of ions on the viscometric and ultracentrifugal behaviour of Tamm-Horsfall glycoprotein, Biochim Biophys Acta 236, 59–66 (1971).

    PubMed  CAS  Google Scholar 

  122. Wiggins RC, Uromucoid (Tamm-Horsfall glycoprotein) forms different polymeric arrangements on a filter surface under different physicochemical conditions, Clin Chim Acta 162, 329–40 (1987).

    Article  PubMed  CAS  Google Scholar 

  123. Tamm I, Bugher JC, Horsfall FL, Ultracentrifugation studies of a urinary mucoprotein which reacts with various viruses, J Biol Chem 212, 125–33 (1955).

    PubMed  CAS  Google Scholar 

  124. McQueen EG, Composition of urinary casts, Lancet 1, 397–8 (1966).

  125. Serafini-Cessi F, Bellabarba G, Malagolini N, Dall'Olio F, Rapid isolation of Tamm-Horsfall glycoprotein (uromodulin) from human urine, J Immunol Methods 120, 185–9 (1989).

    Article  PubMed  CAS  Google Scholar 

  126. Cavallone D, Malagolini N, Frascà GM, Stefoni S, Serafini-Cessi F, Salt precipitation method does not isolate to homogeneity Tamm-Horsfall glycoprotein from urine of proteinuric patients and pregnant women, Clin Biochem 35, 405–10 (2002).

    Article  PubMed  CAS  Google Scholar 

  127. Lynn KL, Marshall RD, Excretion of Tamm-Horsfall glycoprotein in renal disease, Clin Nephrol 22, 253–7 (1984).

    PubMed  CAS  Google Scholar 

  128. Bleyer AJ, Hart TC, Shihabi Z, Robins V, Hoyer JR, Mutations in the uromodulin gene decrease urinary excretion of Tamm-Horsfall protein, Kidney Int 66, 974–7 (2004).

    Article  PubMed  CAS  Google Scholar 

  129. Korhonen TK, Parkkinen J, Hacker J, Finne J, Pere A, Rhen M, Holthofer H, Binding of Escherichia coli S fimbriae to human kidney epithelium, Infect Immun 54, 322–7 (1986).

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Experimental Pathology, University of Bologna, Bologna, Italy, 40126

    Franca Serafini-Cessi, Angela Monti & Daniela Cavallone

  2. Dept. Experimental Pathology, Via S.Giacomo 14, 40126, Bologna, Italy

    Franca Serafini-Cessi

Authors
  1. Franca Serafini-Cessi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angela Monti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniela Cavallone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Franca Serafini-Cessi.

Additional information

Dedicated to Winifred M. Watkins, who died on 3rd October 2003, and who contributed so much to identifying the Sda determinant structure expressed by Tamm-Horsfall glycoprotein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Serafini-Cessi, F., Monti, A. & Cavallone, D. N-Glycans carried by Tamm-Horsfall glycoprotein have a crucial role in the defense against urinary tract diseases. Glycoconj J 22, 383–394 (2005). https://doi.org/10.1007/s10719-005-2142-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-005-2142-z

Keywords

Search

Navigation