Cloning and Expression of the CDNA of Chicken Cation-independent Mannose-6-phosphate Receptor

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1995 Oct 10

PMID 7568213

Citations 13

Authors

M Zhou

Z Ma

W S Sly

Affiliations

Soon will be listed here.

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.

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References

Jadot M, Canfield W, 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; 267(16):11069-77. View

Schmidt B, 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; 270(25):14975-82. DOI: 10.1074/jbc.270.25.14975. View

Fischer H, Gonzalez-Noriega A, Sly W . Beta-glucuronidase binding to human fibroblast membrane receptors. J Biol Chem. 1980; 255(11):5069-74. View

Henikoff S . Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984; 28(3):351-9. DOI: 10.1016/0378-1119(84)90153-7. View

von Heijne G . A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986; 14(11):4683-90. PMC: 311474. DOI: 10.1093/nar/14.11.4683. View

Lobel P, Dahms N, Breitmeyer J, Chirgwin J, Kornfeld S . Cloning of the bovine 215-kDa cation-independent mannose 6-phosphate receptor. Proc Natl Acad Sci U S A. 1987; 84(8):2233-7. PMC: 304623. DOI: 10.1073/pnas.84.8.2233. View

MORGAN D, Edman J, Standring D, Fried V, Smith M, Roth R . Insulin-like growth factor II receptor as a multifunctional binding protein. Nature. 1987; 329(6137):301-7. DOI: 10.1038/329301a0. View

Oshima A, Nolan C, KYLE J, Grubb J, Sly W . 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; 263(5):2553-62. View

Nolan C, Creek K, Grubb J, Sly W . Antibody to the phosphomannosyl receptor inhibits recycling of receptor in fibroblasts. J Cell Biochem. 1987; 35(2):137-51. DOI: 10.1002/jcb.240350207. View

10.

MacDonald R, Pfeffer S, Coussens L, Tepper M, Brocklebank C, Mole J . A single receptor binds both insulin-like growth factor II and mannose-6-phosphate. Science. 1988; 239(4844):1134-7. DOI: 10.1126/science.2964083. View

11.

Frohman M, Dush M, Martin G . 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; 85(23):8998-9002. PMC: 282649. DOI: 10.1073/pnas.85.23.8998. View

12.

Canfield W, 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; 264(13):7100-3. View

13.

Clairmont K, Czech M . Chicken and Xenopus mannose 6-phosphate receptors fail to bind insulin-like growth factor II. J Biol Chem. 1989; 264(28):16390-2. View

14.

Kornfeld S, Mellman I . The biogenesis of lysosomes. Annu Rev Cell Biol. 1989; 5:483-525. DOI: 10.1146/annurev.cb.05.110189.002411. View

15.

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; 62(4):709-17. DOI: 10.1016/0092-8674(90)90116-v. View

16.

Meresse 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; 265(31):18833-42. View

17.

Nolan C, KYLE J, Watanabe H, Sly W . 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; 1(2):197-213. PMC: 361444. DOI: 10.1091/mbc.1.2.197. View

18.

Kozak M . Structural features in eukaryotic mRNAs that modulate the initiation of translation. J Biol Chem. 1991; 266(30):19867-70. View

19.

Johnson K, 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; 119(2):249-57. PMC: 2289647. DOI: 10.1083/jcb.119.2.249. View

20.

Dahms N, ROSE P, Molkentin J, Zhang Y, Brzycki M . 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; 268(8):5457-63. View