Abstract
The putative mannose receptor (MR), previously implicated in mannosyl-rich glycoprotein-induced mitogenesis in bovine airway smooth muscle (ASM) cells, was studied to determine its properties. Specific binding of the mitogenic neoglycoprotein, mannosylated bovine serum albumin (Man-BSA) to ASM cells was saturable, with an apparent Kd = 5.0 x 10(-8) M. Cell-bound ManBSA-colloidal gold conjugate was localized by electron microscopy to clathrin-coated pits on the cell surface, and was found to undergo internalization to endosomes; this was inhibitable by weak bases and swainsonine, that also inhibited ligand-induced mitogenesis. The ASM-MR, isolated by mannose-affinity chromatography, had the same apparent molecular mass as the macrophage (Mø) MR (M(r) = 175 kD), and was immunoprecipitated by an anti-MøMR immune serum. This antiserum blocked 125I-labeled-ManBSA binding to intact ASM cells, stimulated mitogenesis, and immunolocalized the ASM-MR in cytoplasmic vesicles compatible with endosomes. A monoclonal antibody directed against the MøMR also reacted with the ASM-MR; like the polyclonal antibodies, it stimulated mitogenesis as effectively as beta-hexosaminidases. These data indicate that the ASM-MR shares a number of functional and structural properties with the MøMR and suggest that similar receptors may have different main functions in different cells.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bradley J. R., Johnson D. R., Pober J. S. Four different classes of inhibitors of receptor-mediated endocytosis decrease tumor necrosis factor-induced gene expression in human endothelial cells. J Immunol. 1993 Jun 15;150(12):5544–5555. [PubMed] [Google Scholar]
- Carter L. L., Redelmeier T. E., Woollenweber L. A., Schmid S. L. Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis. J Cell Biol. 1993 Jan;120(1):37–45. doi: 10.1083/jcb.120.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chung K. N., Shepherd V. L., Stahl P. D. Swainsonine and castanospermine blockade of mannose glycoprotein uptake by macrophages. Apparent inhibition of receptor-mediated endocytosis by endogenous ligands. J Biol Chem. 1984 Dec 10;259(23):14637–14641. [PubMed] [Google Scholar]
- Dohlman J. G., Payan D. G., Goetzl E. J. Generation of a unique fibroblast-activating factor by human monocytes. Immunology. 1984 Jul;52(3):577–584. [PMC free article] [PubMed] [Google Scholar]
- Dunnill M. S., Massarella G. R., Anderson J. A. A comparison of the quantitative anatomy of the bronchi in normal subjects, in status asthmaticus, in chronic bronchitis, and in emphysema. Thorax. 1969 Mar;24(2):176–179. doi: 10.1136/thx.24.2.176. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fuh G., Cunningham B. C., Fukunaga R., Nagata S., Goeddel D. V., Wells J. A. Rational design of potent antagonists to the human growth hormone receptor. Science. 1992 Jun 19;256(5064):1677–1680. doi: 10.1126/science.256.5064.1677. [DOI] [PubMed] [Google Scholar]
- GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haltiwanger R. S., Hill R. L. The isolation of a rat alveolar macrophage lectin. J Biol Chem. 1986 Jun 5;261(16):7440–7444. [PubMed] [Google Scholar]
- Haltiwanger R. S., Hill R. L. The ligand binding specificity and tissue localization of a rat alveolar macrophage lectin. J Biol Chem. 1986 Nov 25;261(33):15696–15702. [PubMed] [Google Scholar]
- Ishizaki J., Hanasaki K., Higashino K., Kishino J., Kikuchi N., Ohara O., Arita H. Molecular cloning of pancreatic group I phospholipase A2 receptor. J Biol Chem. 1994 Feb 25;269(8):5897–5904. [PubMed] [Google Scholar]
- 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]
- Kosugi S., Ban T., Kohn L. D. Identification of thyroid-stimulating antibody-specific interaction sites in the N-terminal region of the thyrotropin receptor. Mol Endocrinol. 1993 Jan;7(1):114–130. doi: 10.1210/mend.7.1.8095322. [DOI] [PubMed] [Google Scholar]
- Kotlikoff M. I., Murray R. K., Reynolds E. E. Histamine-induced calcium release and phorbol antagonism in cultured airway smooth muscle cells. Am J Physiol. 1987 Oct;253(4 Pt 1):C561–C566. doi: 10.1152/ajpcell.1987.253.4.C561. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lambeau G., Ancian P., Barhanin J., Lazdunski M. Cloning and expression of a membrane receptor for secretory phospholipases A2. J Biol Chem. 1994 Jan 21;269(3):1575–1578. [PubMed] [Google Scholar]
- Lennartz M. R., Cole F. S., Shepherd V. L., Wileman T. E., Stahl P. D. Isolation and characterization of a mannose-specific endocytosis receptor from human placenta. J Biol Chem. 1987 Jul 25;262(21):9942–9944. [PubMed] [Google Scholar]
- Lennartz M. R., Cole F. S., Stahl P. D. Biosynthesis and processing of the mannose receptor in human macrophages. J Biol Chem. 1989 Feb 5;264(4):2385–2390. [PubMed] [Google Scholar]
- Lennartz M. R., Wileman T. E., Stahl P. D. Isolation and characterization of a mannose-specific endocytosis receptor from rabbit alveolar macrophages. Biochem J. 1987 Aug 1;245(3):705–711. doi: 10.1042/bj2450705. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lew D. B., Chodimella V., Murlas C. G. Guinea pig ozone-induced airway hyperreactivity is associated with increased N-acetyl-beta-D-glucosaminidase activity in bronchoalveolar lavage fluid. Lung. 1990;168(5):273–283. doi: 10.1007/BF02719704. [DOI] [PubMed] [Google Scholar]
- Lew D. B., Nebigil C., Malik K. U. Dual regulation by cAMP of beta-hexosaminidase-induced mitogenesis in bovine tracheal myocytes. Am J Respir Cell Mol Biol. 1992 Dec;7(6):614–619. doi: 10.1165/ajrcmb/7.6.614. [DOI] [PubMed] [Google Scholar]
- Lew D. B., Rattazzi M. C. Mitogenic effect of lysosomal hydrolases on bovine tracheal myocytes in culture. J Clin Invest. 1991 Dec;88(6):1969–1975. doi: 10.1172/JCI115522. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lutz W., Kumar R. Hypertonic sucrose treatment enhances second messenger accumulation in vasopressin-sensitive cells. Am J Physiol. 1993 Feb;264(2 Pt 2):F228–F233. doi: 10.1152/ajprenal.1993.264.2.F228. [DOI] [PubMed] [Google Scholar]
- Mahuran D., Lowden J. A. The subunit and polypeptide structure of hexosaminidases from human placenta. Can J Biochem. 1980 Apr;58(4):287–294. doi: 10.1139/o80-038. [DOI] [PubMed] [Google Scholar]
- Mayorga L. S., Diaz R., Stahl P. D. Regulatory role for GTP-binding proteins in endocytosis. Science. 1989 Jun 23;244(4911):1475–1477. doi: 10.1126/science.2499930. [DOI] [PubMed] [Google Scholar]
- Milligan G. Mechanisms of multifunctional signalling by G protein-linked receptors. Trends Pharmacol Sci. 1993 Jun;14(6):239–244. doi: 10.1016/0165-6147(93)90019-g. [DOI] [PubMed] [Google Scholar]
- Murray J. J., Tonnel A. B., Brash A. R., Roberts L. J., 2nd, Gosset P., Workman R., Capron A., Oates J. A. Release of prostaglandin D2 into human airways during acute antigen challenge. N Engl J Med. 1986 Sep 25;315(13):800–804. doi: 10.1056/NEJM198609253151304. [DOI] [PubMed] [Google Scholar]
- Nagayama Y., Rapoport B. The thyrotropin receptor 25 years after its discovery: new insight after its molecular cloning. Mol Endocrinol. 1992 Feb;6(2):145–156. doi: 10.1210/mend.6.2.1569961. [DOI] [PubMed] [Google Scholar]
- Otter M., Kuiper J., Bos R., Rijken D. C., van Berkel T. J. Characterization of the interaction both in vitro and in vivo of tissue-type plasminogen activator (t-PA) with rat liver cells. Effects of monoclonal antibodies to t-PA. Biochem J. 1992 Jun 1;284(Pt 2):545–550. doi: 10.1042/bj2840545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pearse B. M., Robinson M. S. Clathrin, adaptors, and sorting. Annu Rev Cell Biol. 1990;6:151–171. doi: 10.1146/annurev.cb.06.110190.001055. [DOI] [PubMed] [Google Scholar]
- Pontow S. E., Kery V., Stahl P. D. Mannose receptor. Int Rev Cytol. 1992;137B:221–244. doi: 10.1016/s0074-7696(08)62606-6. [DOI] [PubMed] [Google Scholar]
- Reis e Sousa C., Stahl P. D., Austyn J. M. Phagocytosis of antigens by Langerhans cells in vitro. J Exp Med. 1993 Aug 1;178(2):509–519. doi: 10.1084/jem.178.2.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Russo D., Chazenbalk G. D., Nagayama Y., Wadsworth H. L., Seto P., Rapoport B. A new structural model for the thyrotropin (TSH) receptor, as determined by covalent cross-linking of TSH to the recombinant receptor in intact cells: evidence for a single polypeptide chain. Mol Endocrinol. 1991 Nov;5(11):1607–1612. doi: 10.1210/mend-5-11-1607. [DOI] [PubMed] [Google Scholar]
- Shepherd V. L., Hoidal J. R. Clearance of neutrophil-derived myeloperoxidase by the macrophage mannose receptor. Am J Respir Cell Mol Biol. 1990 Apr;2(4):335–340. doi: 10.1165/ajrcmb/2.4.335. [DOI] [PubMed] [Google Scholar]
- Shepherd V. L., Tarnowski B. I., McLaughlin B. J. Isolation and characterization of a mannose receptor from human pigment epithelium. Invest Ophthalmol Vis Sci. 1991 May;32(6):1779–1784. [PubMed] [Google Scholar]
- Stahl P. D., Rodman J. S., Miller M. J., Schlesinger P. H. Evidence for receptor-mediated binding of glycoproteins, glycoconjugates, and lysosomal glycosidases by alveolar macrophages. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1399–1403. doi: 10.1073/pnas.75.3.1399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stahl P. D. The macrophage mannose receptor: current status. Am J Respir Cell Mol Biol. 1990 Apr;2(4):317–318. doi: 10.1165/ajrcmb/2.4.317. [DOI] [PubMed] [Google Scholar]
- Stahl P., Schlesinger P. H., Sigardson E., Rodman J. S., Lee Y. C. Receptor-mediated pinocytosis of mannose glycoconjugates by macrophages: characterization and evidence for receptor recycling. Cell. 1980 Jan;19(1):207–215. doi: 10.1016/0092-8674(80)90402-x. [DOI] [PubMed] [Google Scholar]
- Stephenson J. D., Shepherd V. L. Purification of the human alveolar macrophage mannose receptor. Biochem Biophys Res Commun. 1987 Oct 29;148(2):883–889. doi: 10.1016/0006-291x(87)90958-2. [DOI] [PubMed] [Google Scholar]
- Summerfield J. A., Vergalla J., Jones E. A. Modulation of a glycoprotein recognition system on rat hepatic endothelial cells by glucose and diabetes mellitus. J Clin Invest. 1982 Jun;69(6):1337–1347. doi: 10.1172/JCI110573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takizawa T., Thurlbeck W. M. Muscle and mucous gland size in the major bronchi of patients with chronic bronchitis, asthma, and asthmatic bronchitis. Am Rev Respir Dis. 1971 Sep;104(3):331–336. doi: 10.1164/arrd.1971.104.3.331. [DOI] [PubMed] [Google Scholar]
- Taylor M. E., Bezouska K., Drickamer K. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor. J Biol Chem. 1992 Jan 25;267(3):1719–1726. [PubMed] [Google Scholar]
- Taylor M. E., Drickamer K. Structural requirements for high affinity binding of complex ligands by the macrophage mannose receptor. J Biol Chem. 1993 Jan 5;268(1):399–404. [PubMed] [Google Scholar]
- Tietze C., Schlesinger P., Stahl P. Chloroquine and ammonium ion inhibit receptor-mediated endocytosis of mannose-glycoconjugates by macrophages: apparent inhibition of receptor recycling. Biochem Biophys Res Commun. 1980 Mar 13;93(1):1–8. doi: 10.1016/s0006-291x(80)80237-3. [DOI] [PubMed] [Google Scholar]
- Tonnel A. B., Joseph M., Gosset P., Fournier E., Capron A. Stimulation of alveolar macrophages in asthmatic patients after local provocation test. Lancet. 1983 Jun 25;1(8339):1406–1408. doi: 10.1016/s0140-6736(83)92356-5. [DOI] [PubMed] [Google Scholar]
- Valente W. A., Vitti P., Yavin Z., Yavin E., Rotella C. M., Grollman E. F., Toccafondi R. S., Kohn L. D. Monoclonal antibodies to the thyrotropin receptor: stimulating and blocking antibodies derived from the lymphocytes of patients with Graves disease. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6680–6684. doi: 10.1073/pnas.79.21.6680. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wahl M. I., Nishibe S., Suh P. G., Rhee S. G., Carpenter G. Epidermal growth factor stimulates tyrosine phosphorylation of phospholipase C-II independently of receptor internalization and extracellular calcium. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1568–1572. doi: 10.1073/pnas.86.5.1568. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zanolari B., Raths S., Singer-Krüger B., Riezman H. Yeast pheromone receptor endocytosis and hyperphosphorylation are independent of G protein-mediated signal transduction. Cell. 1992 Nov 27;71(5):755–763. doi: 10.1016/0092-8674(92)90552-n. [DOI] [PubMed] [Google Scholar]