Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Oct 10;92(21):9762–9766. doi: 10.1073/pnas.92.21.9762

Cloning and expression of the cDNA of chicken cation-independent mannose-6-phosphate receptor.

M Zhou 1, Z Ma 1, W S Sly 1
PMCID: PMC40882  PMID: 7568213

Abstract

We cloned and sequenced the 8767-bp full-length cDNA for the chicken cation-independent mannose-6-phosphate receptor (CI-MPR), of interest because, unlike its mammalian homologs, it does not bind insulin-like growth factor II (IGF-II). The cDNA encodes a protein of 2470 aa that includes a putative signal sequence, an extracytoplasmic domain consisting of 15 homologous repeat sequences, a 23-residue transmembrane sequence, and a 161-residue cytoplasmic sequence. Overall, it shows 60% sequence identity with human and bovine CI-MPR homologs, and all but two of 122 cysteine residues are conserved. However, it shows much less homology in the N-terminal signal sequence, in repeat 11, which is proposed to contain the IGF-II-binding site in mammalian CI-MPR homologs, and in the 14-aa residue segment in the cytoplasmic sequence that has been proposed to mediate G-protein-coupled signal transduction in response to IGF-II binding by the human CI-MPR. Transient expression in COS-7 cells produced a functional CI-MPR which exhibited mannose-6-phosphate-inhibitable binding and mediated endocytosis of recombinant human beta-glucuronidase. Expression of the functional chicken CI-MPR in mice lacking the mammalian CI-MPR should clarify the controversy over the physiological role of the IGF-II-binding site in mammalian CI-MPR homologs.

Full text

PDF
9762

Images in this article

9765Fig. 4
on p.9765

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Canfield W. M., Kornfeld S. The chicken liver cation-independent mannose 6-phosphate receptor lacks the high affinity binding site for insulin-like growth factor II. J Biol Chem. 1989 May 5;264(13):7100–7103. [PubMed] [Google Scholar]
  2. Clairmont K. B., Czech M. P. Chicken and Xenopus mannose 6-phosphate receptors fail to bind insulin-like growth factor II. J Biol Chem. 1989 Oct 5;264(28):16390–16392. [PubMed] [Google Scholar]
  3. Dahms N. M., Rose P. A., Molkentin J. D., Zhang Y., Brzycki M. A. The bovine mannose 6-phosphate/insulin-like growth factor II receptor. The role of arginine residues in mannose 6-phosphate binding. J Biol Chem. 1993 Mar 15;268(8):5457–5463. [PubMed] [Google Scholar]
  4. Fischer H. D., Gonzalez-Noriega A., Sly W. S. Beta-glucuronidase binding to human fibroblast membrane receptors. J Biol Chem. 1980 Jun 10;255(11):5069–5074. [PubMed] [Google Scholar]
  5. Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Garmroudi F., MacDonald R. G. Localization of the insulin-like growth factor II (IGF-II) binding/cross-linking site of the IGF-II/mannose 6-phosphate receptor to extracellular repeats 10-11. J Biol Chem. 1994 Oct 28;269(43):26944–26952. [PubMed] [Google Scholar]
  7. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  8. Jadot M., Canfield W. M., Gregory W., Kornfeld S. Characterization of the signal for rapid internalization of the bovine mannose 6-phosphate/insulin-like growth factor-II receptor. J Biol Chem. 1992 Jun 5;267(16):11069–11077. [PubMed] [Google Scholar]
  9. Johnson K. F., Kornfeld S. The cytoplasmic tail of the mannose 6-phosphate/insulin-like growth factor-II receptor has two signals for lysosomal enzyme sorting in the Golgi. J Cell Biol. 1992 Oct;119(2):249–257. doi: 10.1083/jcb.119.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kornfeld S., Mellman I. The biogenesis of lysosomes. Annu Rev Cell Biol. 1989;5:483–525. doi: 10.1146/annurev.cb.05.110189.002411. [DOI] [PubMed] [Google Scholar]
  11. Kornfeld S. Structure and function of the mannose 6-phosphate/insulinlike growth factor II receptors. Annu Rev Biochem. 1992;61:307–330. doi: 10.1146/annurev.bi.61.070192.001515. [DOI] [PubMed] [Google Scholar]
  12. Kozak M. Structural features in eukaryotic mRNAs that modulate the initiation of translation. J Biol Chem. 1991 Oct 25;266(30):19867–19870. [PubMed] [Google Scholar]
  13. Körner C., Nürnberg B., Uhde M., Braulke T. Mannose 6-phosphate/insulin-like growth factor II receptor fails to interact with G-proteins. Analysis of mutant cytoplasmic receptor domains. J Biol Chem. 1995 Jan 6;270(1):287–295. doi: 10.1074/jbc.270.1.287. [DOI] [PubMed] [Google Scholar]
  14. Lau M. M., Stewart C. E., Liu Z., Bhatt H., Rotwein P., Stewart C. L. Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev. 1994 Dec 15;8(24):2953–2963. doi: 10.1101/gad.8.24.2953. [DOI] [PubMed] [Google Scholar]
  15. Lobel P., Dahms N. M., Breitmeyer J., Chirgwin J. M., Kornfeld S. Cloning of the bovine 215-kDa cation-independent mannose 6-phosphate receptor. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2233–2237. doi: 10.1073/pnas.84.8.2233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. MacDonald R. G., Pfeffer S. R., Coussens L., Tepper M. A., Brocklebank C. M., Mole J. E., Anderson J. K., Chen E., Czech M. P., Ullrich A. A single receptor binds both insulin-like growth factor II and mannose-6-phosphate. Science. 1988 Mar 4;239(4844):1134–1137. doi: 10.1126/science.2964083. [DOI] [PubMed] [Google Scholar]
  17. Morgan D. O., Edman J. C., Standring D. N., Fried V. A., Smith M. C., Roth R. A., Rutter W. J. Insulin-like growth factor II receptor as a multifunctional binding protein. Nature. 1987 Sep 24;329(6137):301–307. doi: 10.1038/329301a0. [DOI] [PubMed] [Google Scholar]
  18. Méresse S., Ludwig T., Frank R., Hoflack B. Phosphorylation of the cytoplasmic domain of the bovine cation-independent mannose 6-phosphate receptor. Serines 2421 and 2492 are the targets of a casein kinase II associated to the Golgi-derived HAI adaptor complex. J Biol Chem. 1990 Nov 5;265(31):18833–18842. [PubMed] [Google Scholar]
  19. Nolan C. M., Creek K. E., Grubb J. H., Sly W. S. Antibody to the phosphomannosyl receptor inhibits recycling of receptor in fibroblasts. J Cell Biochem. 1987 Oct;35(2):137–151. doi: 10.1002/jcb.240350207. [DOI] [PubMed] [Google Scholar]
  20. Nolan C. M., Kyle J. W., Watanabe H., Sly W. S. Binding of insulin-like growth factor II (IGF-II) by human cation-independent mannose 6-phosphate receptor/IGF-II receptor expressed in receptor-deficient mouse L cells. Cell Regul. 1990 Jan;1(2):197–213. doi: 10.1091/mbc.1.2.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Okamoto T., Katada T., Murayama Y., Ui M., Ogata E., Nishimoto I. A simple structure encodes G protein-activating function of the IGF-II/mannose 6-phosphate receptor. Cell. 1990 Aug 24;62(4):709–717. doi: 10.1016/0092-8674(90)90116-v. [DOI] [PubMed] [Google Scholar]
  22. Oshima A., Nolan C. M., Kyle J. W., Grubb J. H., Sly W. S. The human cation-independent mannose 6-phosphate receptor. Cloning and sequence of the full-length cDNA and expression of functional receptor in COS cells. J Biol Chem. 1988 Feb 15;263(5):2553–2562. [PubMed] [Google Scholar]
  23. Schmidt B., Kiecke-Siemsen C., Waheed A., Braulke T., von Figura K. Localization of the insulin-like growth factor II binding site to amino acids 1508-1566 in repeat 11 of the mannose 6-phosphate/insulin-like growth factor II receptor. J Biol Chem. 1995 Jun 23;270(25):14975–14982. doi: 10.1074/jbc.270.25.14975. [DOI] [PubMed] [Google Scholar]
  24. Stöger R., Kubicka P., Liu C. G., Kafri T., Razin A., Cedar H., Barlow D. P. Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell. 1993 Apr 9;73(1):61–71. doi: 10.1016/0092-8674(93)90160-r. [DOI] [PubMed] [Google Scholar]
  25. Szebenyi G., Rotwein P. The mouse insulin-like growth factor II/cation-independent mannose 6-phosphate (IGF-II/MPR) receptor gene: molecular cloning and genomic organization. Genomics. 1994 Jan 1;19(1):120–129. doi: 10.1006/geno.1994.1021. [DOI] [PubMed] [Google Scholar]
  26. Wang Z. Q., Fung M. R., Barlow D. P., Wagner E. F. Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature. 1994 Dec 1;372(6505):464–467. doi: 10.1038/372464a0. [DOI] [PubMed] [Google Scholar]
  27. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES