Skip to main content
Log in

Mannose-6-phosphate receptors (MPR 300 and 46) from the highly evolved invertebrate Asterias rubens (Echinodermate): biochemical and functional characterization of MPR 46 protein

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Mammalian mannose 6-phosphate receptors (MPR 300 and 46) mediate transport of lysosomal enzymes to lysosomes. Recent studies established that the receptors are conserved throughout vertebrates. Although we purified the mollusc receptors and identified only a lysosomal enzyme receptor protein (LERP) in the Drosophila melanogaster, little is known about their structure and functional roles in the invertebrates. In the present study, we purified the putative receptors from the highly evolved invertebrate, starfish, cloned the cDNA for the MPR 46, and expressed it in mpr(−/−) mouse embryonic fibroblast cells. Structural comparison of starfish receptor sequences with other vertebrate receptors gave valuable information on its extensive structural homology with the vertebrate MPR 46 proteins. The expressed protein efficiently sorts lysosomal enzymes within the cells establishing a functional role for this protein. This first report on the invertebrate MPR 46 further confirms the structural and functional conservation of the receptor not only in the vertebrates but also in the invertebrates.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Suresh, K., Raju, V.S.N., Siva Kumar, N.: Molecular cloning of goat mannose 6-phophate receptors (MPR 300 and 46). Glycoconjugate J. 20, 257–265 (2004)

    Article  CAS  Google Scholar 

  2. Kang, J.X., Li, Y., Leaf, A.: Mannose 6-phosphate /insulin-like growth factor II is a receptor for retinoic acid. Proc. Natl. Acad. Sci. U. S. A. 94, 13671–13676 (1997)

    Article  PubMed  CAS  Google Scholar 

  3. Nykjaer, A., Christensen, E.I., Vorum, H., Hager, H., Petersen, C.M., Roigaard, H., Min, H.Y., Vilhardt, F., Moller, L.B., Cornfields, S., Gliemann, J.: Mannose 6-phosphate/insulin-like growth factor-II receptor targets the urokinase receptor to lysosomes via a novel binding interaction. Cell. Biol. 141, 815–828 (1998)

    Article  CAS  Google Scholar 

  4. Siva Kumar, N., Hille-Rehfeld, A., von Figura, K.: Mannose 6-phosphate receptor proteins from reptiles and amphibians, evidence for the presence of MPR 300 and MPR 46. Comp. Biochem. Physiol. 118B, 805–809 (1997)

    Google Scholar 

  5. Siva Kumar, N., Udaya Lakshmi, Y., Hille-Rehfeld, A., von Figura, K.: Mannose 6-phosphate receptors (MPR 300 and MPR 46) from a teleostean fish (trout). Comp. Biochem. Physiol. 123B, 261–265 (1999)

    Google Scholar 

  6. Siva Kumar, N., von Figura, K.: Identification of the putative Mannose 6-phosphate receptor (MPR 46) protein in the invertebrate mollusc. Bioscience Reports. 22. 5 and 6, 513–521 (2002)

    Google Scholar 

  7. Matzner, U., Annette, H.R., von Figura, K., Pohlmann, R.: Expression of mannose 6-phosphate receptors in chicken. Dev. Dyn. 207, 11–24 (1996)

    Article  PubMed  CAS  Google Scholar 

  8. Siva Kumar, N., Raju, V.S.N., Suresh, K., Venkatesh, B., von Figura, K., Pohlmann, R.: Molecular cloning and sequencing of Mannose 6-phosphate receptor (MPR) 300 protein from fugu fish 45th Annual Meeting of the ASCB. San Francisco. USA, 10–14th December. (2005)

  9. Suresh, K., Vegiraju, S.R., Siva Kumar, N., von Figura, K., Pohlmann, R., Dennes, A.: The early vertebrate Danio rerio Mr 46000 mannose 6-phosphate receptor: biochemical and functional characterization. Dev. Genes Evol. 216(3), 133–143(2005)

    Google Scholar 

  10. Siva Kumar, N., Nirmala, P., Suresh, K.: Biochemical and immunological characterization of a glycosylated a-fucosidase from the invertebrate Unio. Interaction of the enzyme with its in vivo binding partners. Prot. Exp. and Pur. 37, 279–287 (2004)

    Article  Google Scholar 

  11. Dennes, A., Cromme, C., Suresh, K., Siva Kumar, N., Johannes, A.E., Hahnenkamp, A., Pohlmann, R.: The novel drosophila lysosomal enzyme receptor protein mediates lysosomal sorting in mammalian cells and binds mammalian and drosophila GGA adaptors. J. Biol. Chem. 280, 12849–12857 (2005)

    Article  PubMed  CAS  Google Scholar 

  12. Raju, V.S.N., von Figura, K., Siva Kumar, N.: Mannose 6-phosphate receptor (MPR 300) like polypeptides in the Arthropods and Annelidae. Glycoconjugate J18, 292–210 (2001)

    Google Scholar 

  13. Praveen Kumar, A., Suresh, K., Siva Kumar, N.: Biochemical and functional characterization of cation dependent (Mr 46,000) goat mannose 6-phosphate receptor. Glycoconjugate J. 24, 221–229 (2007)

    Article  Google Scholar 

  14. Suresh, K., Siva Kumar, N.: An immuno-affinity method for the purification of mannose 6-phosphate receptor protein. J. Biochem. Biophys. Meth. 57, 237–235 (2003)

    Article  PubMed  CAS  Google Scholar 

  15. Waheed, A., Hasilik, A., von Figura, K.: Synthesis and processing of arylsulfatase A in human skin fibroblasts. Hoppe-Seyler’s Z. Physiol. Chem. 363, 425–430 (1982)

    CAS  Google Scholar 

  16. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of T bacteriophage. Nature 227, 680–685 (1970)

    Article  PubMed  CAS  Google Scholar 

  17. Blum, H., Beier, H., Gross, H.J.: Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8, 93–99 (1987)

    Article  CAS  Google Scholar 

  18. Towbin, H., Staehelin, T., Gordon, J.: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76, 4350–4354 (1979)

    Article  PubMed  CAS  Google Scholar 

  19. Braulke, T., Tippmer, S., Chao, H.J., von Figura, K.: Regulation of mannose 6-phosphate/insulin-like growth factor II receptor distribution by activators and inhibitors of protein kinase C. Eur. J. Biochem. 189(3), 609–16 (1990)

    Article  PubMed  CAS  Google Scholar 

  20. Dahms, N.M., Hancock, M.K.: P-Type lectins. Biochem. Biophys. Acta. 1572, 317–340 (2002)

    PubMed  CAS  Google Scholar 

  21. Suresh, K., Sivaramakrishna, Y., Siva Kumar, N.: Mannose 6-phosphate receptor (MPR 300) from goat and chicken bind human IGF-II. Biosci. Rep. 26, 101–112 (2006)

    Article  Google Scholar 

  22. Nolan, C.M., McCarthy, K., Eivers, E., Randy, L.J., Lucy, B.: Mannose 6-phosphate receptors in an ancient vertebrate, zebra fish. Dev Genes Evol. 216, 144–151 (2006)

    Article  PubMed  CAS  Google Scholar 

  23. Mendez, E., Planas, J.V., Castillo, J., Navarro, I., Gutierrez, J.: Identification of a type II insulin-like growth factor receptor in fish embryos. Endocrinology. 142, 1090–1097 (2001)

    Article  PubMed  CAS  Google Scholar 

  24. Gabel, C.A., Costello, C.E., Reinhold, V.N., Kurz, L., Kornfeld, S.: Identification of methylphosphomannosyl residues as components of the high mannose oligosaccharides of Dictyostelium discoideum glycoproteins. J. Biol. Chem. 259, 13762–13769 (1984)

    PubMed  CAS  Google Scholar 

  25. Couso, R., Lang, L., Roberts, R.M., Kornfeld, S.: Phosphorylation of the oligosaccharide of uteroferrin by UDP-GlcNAc: glycoprotein N-acetylglucosamine-1-phosphotransferases from rat liver, Acanthamoeba castellani, and Dictyostelium discoideum requires α1,2-linked mannose residues. J. Biol. Chem. 261, 6326–6331 (1986)

    PubMed  CAS  Google Scholar 

  26. Sun, G., Zhao, H., Kalyanaraman, B., Dahms, N.M.: Identification of residues essential for carbohydrate recognition and cation dependence of the 46 kDa mannose 6-phosphate receptor. Glycobiology 15, 1136–1149 (2005)

    Article  PubMed  CAS  Google Scholar 

  27. Ghosh, P., Dahms, N.M., Kornfeld, S.: Mannose 6-phosphate receptors: new twists in the tale. Nat. Rev. Mol. Cell. Biol. 4, 202–212 (2003)

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

NSK thanks the Volkswagen stiftung, Germany for a research support (I/78913) together with Prof. Dr. K. von Figura, University of Goettingen, and Prof. Dr. R. Pohlmann, University of Muenster, Germany. Research work on the MPR proteins in the laboratory of NSK is supported by a research grant from Department of Science and Technology SR/SO/BB/60-2003. YSRK thanks Council of Scientific and Industrial Research, New Delhi, India for a research fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Siva Kumar Nadimpalli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yadavalli, S., Nadimpalli, S.K. Mannose-6-phosphate receptors (MPR 300 and 46) from the highly evolved invertebrate Asterias rubens (Echinodermate): biochemical and functional characterization of MPR 46 protein. Glycoconj J 25, 889–901 (2008). https://doi.org/10.1007/s10719-008-9153-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-008-9153-5

Keywords

Navigation