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Liver-specific ZP domain-containing protein (LZP) as a new partner of Tamm-Horsfall protein harbors on renal tubules

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Abstract

Liver-specific ZP domain-containing protein (LZP) was recently identified as a secreted protein that is specifically expressed in liver. However, the physiological effects of LZP are largely unknown. In this study, we found that LZP was detectable in mouse kidneys, testes, ovaries and heart, in addition to liver. LZP was localized in the spermatid cells of testes, corpus luteum cells of ovaries, and cardiac muscle cells of heart. But the protein mainly anchored on the apical membrane of the thick ascending limb of the loop of Henle (TAL) cell in mouse kidney. In rat kidney LZP and Tamm-Horsfall protein (THP) were co-localized in TAL. The in vivo interaction between LZP and THP was confirmed in kidney and urine by co-immunoprecipitation assay, and the in vitro interaction was detected by GST pull-down assay, implying that the interaction could be independent on N-linked glycosylated modification of LZP. Surprisingly, LZPs with intramolecular disulfide bridges could self-interact, and then self-aggregate into spheres of varying sizes, but not polymerize into filaments. The finding that LZP might act as a new partner of THP would provide novel insights into renal functions related to THP and LZP, such as the urothelial permeability barrier and the host defense against the adhesion of pathogens.

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References

  1. Xu ZG, Du JJ, Zhang X et al (2003) A novel liver-specific zona pellucida domain containing protein that is expressed rarely in hepatocellular carcinoma. Hepatology 38:735–744. doi:10.1053/jhep.2003.50340

    Article  PubMed  CAS  Google Scholar 

  2. Xu ZG, Du JJ, Sj Cui et al (2004) Identification of LZP gene from mus musculus and rattus norvegicus coding for a novel liver-specific ZP domain-containing secretory protein. DNA Seq 15:81–87. doi:10.1080/10425170310001652200

    PubMed  CAS  Google Scholar 

  3. Jovine L, Darie CC, Litscher ES et al (2005) Zona pellucida domain proteins. Annu Rev Biochem 74:83–114. doi:10.1146/annurev.biochem.74.082803.133039

    Article  PubMed  CAS  Google Scholar 

  4. Tamm I, Horsfall FL Jr (1950) Characterization and separation of an inhibitor of viral hemagglutination present in Urine. Proc Soc Exp Biol Med 74:106–108

    PubMed  CAS  Google Scholar 

  5. Kumar S, Muchmore AV (1990) Tamm-Horsfall protein–uromodulin (1950–1990). Kidney Int 37:1395–1401. doi:10.1038/ki.1990.128

    Article  PubMed  CAS  Google Scholar 

  6. Bachmann S, Dawnay AB, Bouby N et al (1991) Tamm-horsfall protein excretion during chronic alterations in urinary concentration and protein intake in the rat. Ren Physiol Biochem 14:236–245

    Article  PubMed  CAS  Google Scholar 

  7. Hession C, Decker JM, Sherblom AP et al (1987) Uromodulin (Tamm-Horsfall glycoprotein): a renal ligand for lymphokines. Science 237:1479–1484. doi:10.1126/science.3498215

    Article  PubMed  CAS  Google Scholar 

  8. Rhodes DC (2000) Binding of Tamm-Horsfall protein to complement 1q measured by ELISA and resonant mirror biosensor techniques under various ionic-strength conditions. Immunol Cell Biol 78:474–482. doi:10.1046/j.1440-1711.2000.00930.x

    Article  PubMed  CAS  Google Scholar 

  9. Rhodes DC, Hinsman EJ, Rhodes JA (1993) Tamm-Horsfall glycoprotein binds IgG with high affinity. Kidney Int 44:1014–1021. doi:10.1038/ki.1993.343

    Article  PubMed  CAS  Google Scholar 

  10. Sherblom AP, Decker JM, Muchmore AV (1988) The lectin-like interaction between recombinant tumor necrosis factor and uromodulin. J Biol Chem 263:5418–5424

    PubMed  CAS  Google Scholar 

  11. Winkelstein A, Muchmore AV, Decker JM et al (1990) Uromodulin: a specific inhibitor of IL-1-initiated human T-cell colony formation. Immunopharmacology 20:201–205. doi:10.1016/0162-3109(90)90035-D

    Article  PubMed  CAS  Google Scholar 

  12. Ying WZ, Sanders PW (2001) Mapping the binding domain of immunoglobulin light chains for Tamm-Horsfall protein. Am J Pathol 158:1859–1866

    PubMed  CAS  Google Scholar 

  13. Eto K, Eda K, Kanemoto S, Abe S (2006) The immunoglobulin-like domain is involved in interaction of Neuregulin 1 with ErbB. Biochem Biophys Res Commun 350:263–271. doi:10.1016/j.bbrc.2006.09.028

    Article  PubMed  CAS  Google Scholar 

  14. Kuroda S, Tanizawa K (1999) Involvement of epidermal growth factor-like domain of NELL proteins in the novel protein-protein interaction with protein kinase C. Biochem Biophys Res Commun 265(3):752–757. doi:10.1006/bbrc.1999.1753

    Article  PubMed  CAS  Google Scholar 

  15. Lin HH, Stacey M, Saxby C et al (2001) Molecular analysis of the epidermal growth factor-like short consensus repeat domain-mediated protein-protein interactions: dissection of the CD97-CD55 complex. J Biol Chem 276:24160–24169. doi:10.1074/jbc.M101770200

    Article  PubMed  CAS  Google Scholar 

  16. Ortiz JA, Castillo M, del Toro ED et al (2003) The Tat protein of the human immunodeficiency virus type 1 (HIV-1) interacts with the EGF-like repeats of the Notch proteins and the EGF precursor. Virus Res 98:57–61. doi:10.1016/j.virusres.2003.08.016

    Article  Google Scholar 

  17. Sasanami T, Ohtsuki M, Ishiguro T et al (2006) Zona pellucida domain of ZPB1 controls specific binding of ZPB1 and ZPC in Japanese quail (Coturnix japonica). Cells Tissues Organs 183:41–52. doi:10.1159/000094905

    Article  PubMed  Google Scholar 

  18. Jovine L, Qi H, Williams Z, Litscher ES et al (2002) The ZP domain is a conserved module for polymerization of extracellular proteins. Nat Cell Biol 4:457–461. doi:10.1038/ncb802

    Article  PubMed  CAS  Google Scholar 

  19. Jovine L, Qi H, Williams Z et al (2004) A duplicated motif controls assembly of zona pellucida domain proteins. Proc Natl Acad Sci USA 101:5922–5927. doi:10.1073/pnas.0401600101

    Article  PubMed  CAS  Google Scholar 

  20. Devuyst O, Dahan K, Pirson Y (2005) Tamm-Horsfall protein or uromodulin: new ideas about an old molecule. Nephrol Dial Transplant 20:1290–1294. doi:10.1093/ndt/gfh851

    Article  PubMed  CAS  Google Scholar 

  21. Stein P, Rajasekaran M, Parsons CL (2005) Tamm-Horsfall protein protects urothelial permeability barrier. Urology 66:903–907. doi:10.1016/j.urology.2005.05.021

    Article  PubMed  Google Scholar 

  22. Dean JD, Goodwin PH, Hsiang T (2002) Comparison of relative RT-PCR and Northern Blot analyses to measure expression of β-1, 3-Glucanase in Nicotiana benthamiana infected with Colltotrichum destructivum. Plant Mol Biol Rep 20:347–356. doi:10.1007/BF02772122

    Article  CAS  Google Scholar 

  23. Silva AM, Pires EG, Abrantes EF et al (1999) Application of the differential display RT-PCR strategy for the identification of inflammation-related mouse genes. Braz J Med Biol Res 32:845–852

    PubMed  CAS  Google Scholar 

  24. Fukuoka SI, Freedman SD, Yu H et al (1992) GP-2/THP gene family encodes self-binding glycosylphosphatidylinositol-anchored proteins in apical secretory compartments of pancreas and kidney. Proc Natl Acad Sci USA 89:1189–1193. doi:10.1073/pnas.89.4.1189

    Article  PubMed  CAS  Google Scholar 

  25. Rankin T, Talbot P, Lee E et al (1999) Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development 126:3847–3855

    PubMed  CAS  Google Scholar 

  26. Bats JM, Raffi HM, Prasadan K et al (2004) Tamm-horsfall protein knockout mice are more prone to urinary tract infection: rapid communication. Kidney Int 65:791–797. doi:10.1111/j.1523-1755.2004.00452.x

    Article  Google Scholar 

  27. Mo L, Zhu XH, Huang HY et al (2004) Ablation of the Tamm-Horsfall protein gene increases susceptibility of mice to bladder colonization by type1-fimbriated Escherichia coli. Am J Physiol Renal Physiol 286:F795–F802. doi:10.1152/ajprenal.00357.2003

    Article  PubMed  CAS  Google Scholar 

  28. Pak J, Pu Y, Zhang ZT et al (2001) Tamm-horsfall protein binds to type 1 fimbriated Escherichia coli and prevents E. coli from binding to uroplakin Ia and Ib receptor. J Biol Chem 276:9924–9930. doi:10.1074/jbc.M008610200

    Article  PubMed  CAS  Google Scholar 

  29. Arolas JL, Aviles FX, Chang JY et al (2006) Folding of small disulfide-rich proteins: clarifying the puzzle. Trends Biochem Sci 31:292–301. doi:10.1016/j.tibs.2006.03.005

    Article  PubMed  CAS  Google Scholar 

  30. Helenius A, Aebi M (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73:1019–1049. doi:10.1146/annurev.biochem.73.011303.073752

    Article  PubMed  CAS  Google Scholar 

  31. Kobata A (1992) Structures and functions of sugar chains of glycoproteins. Eur J Biochem 209:483–501. doi:10.1111/j.1432-1033.1992.tb17313.x

    Article  PubMed  CAS  Google Scholar 

  32. Mitra N, Sinha S, Ramya TN (2006) N-linked oligosaccharides as outfitters for glycoprotein folding form and function. Trends Biochem Sci 31:156–163. doi:10.1016/j.tibs.2006.01.003

    Article  PubMed  CAS  Google Scholar 

  33. Su SJ, Chang KL, Lin TM (1997) Uromodulin and Tamm-Horsfall protein induce human monocytes to secrete TNF and express tissue factor. J Immunol 158:3449–3456

    PubMed  CAS  Google Scholar 

  34. Roller RJ, Wassarman PM (1983) Role of asparagine-linked oligosaccharides in secretion of glycoproteins of the mouse egg’s extracellular coat. J Biol Chem 258:13243–13249

    PubMed  CAS  Google Scholar 

  35. Wassarman PM, Litscher ES (2008) Mammalian fertilization: the egg’s multifunctional zona pellucid. Int J Dev Biol 52:665–676. doi:10.1387/ijdb.072524pw

    Article  PubMed  CAS  Google Scholar 

  36. Fujita T, Shimizum M, Hiramatsu N et al (2002) Purification of serum precursor proteins to vitelline envelope (choriogenins) in masu salmo, oncorhynchus masou. Comp Biochem Physiol Part B 132:599–610. doi:10.1016/S1096-4959(02)00075-1

    Article  Google Scholar 

  37. Murata K, Sugiyama H, Yasumasu S et al (1997) Cloning of cDNA and estrogen-induced hepatic gene expression for choriogenin H, a precursor protein of the fish egg envelope (chorion). Proc Natl Acad Sci USA 94:2050–2055. doi:10.1073/pnas.94.5.2050

    Article  PubMed  CAS  Google Scholar 

  38. Fujita T, Fukada H, Shimizu M et al (2008) Molecular cloning and characterization of three distinct choriogenins in masu salmon, oncorhynchus masou. Mol Reprod Dev 75(7):1217–1228. doi:10.1002/mrd.20857

    Article  PubMed  CAS  Google Scholar 

  39. Sugiyama H, Murata K, Iuchi I et al (1999) Formation of mature egg envelope subunit proteins from their precursors (choriogenins) in the fish, Oryzias latipes: loss of partial C-terminal sequences of the choriogenins. J Biochem 125:469–475

    PubMed  CAS  Google Scholar 

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Acknowledgment

This work was supported by the Chinese high-Tech research and development program (863-2006AA02Z193, 863-2006AA02A305), Chinese national key program on basic research (2004CB518605), National Natural Science Foundation for Outstanding Youth (30425019), National Science Foundation for Postdoctoral Scientists of China (2005038415), Shanghai science and technology developing program (03DZ14024), and the Shanghai Postdoctoral sustentation Fund (0525).

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Authors and Affiliations

  1. Shanghai-Ministry Key Laboratory of Disease and Health Genomics, Chinese National Human Genome Center, 351 Guo Shou-Jing Road, Shanghai, 201203, China

    Hai-Lian Shen, Zhi-Gang Xu, Li-Yu Huang, Dong Liu, Jia-Bin Cao, Xin Zhang, Zhi-Qin Wang & Ze-Guang Han

  2. Institutes of Biomedical Sciences, Fudan University, 220 Handan Road, Shanghai, 200433, China

    Hai-Lian Shen, Peng-Yuan Yang & Ze-Guang Han

  3. Department of Pharmacology, New York Medical College, Valhalla, New York, NY, 10595, USA

    Dao-Hong Lin & Wen-Hui Wang

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  1. Hai-Lian Shen
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  2. Zhi-Gang Xu
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  4. Dong Liu
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Correspondence to Ze-Guang Han.

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Hai-Lian Shen and Zhi-Gang Xu both are contributed equally to this work.

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Shen, HL., Xu, ZG., Huang, LY. et al. Liver-specific ZP domain-containing protein (LZP) as a new partner of Tamm-Horsfall protein harbors on renal tubules. Mol Cell Biochem 321, 73–83 (2009). https://doi.org/10.1007/s11010-008-9921-3

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