[go: up one dir, main page]
Skip to main content
PMC 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
. 1988 Apr;85(7):2284–2287. doi: 10.1073/pnas.85.7.2284

Identification of chondroitin sulfate E proteoglycans and heparin proteoglycans in the secretory granules of human lung mast cells.

R L Stevens 1, C C Fox 1, L M Lichtenstein 1, K F Austen 1
PMCID: PMC279975  PMID: 3353378

Abstract

The predominant subclasses of mast cells in both the rat and the mouse can be distinguished from one another by their preferential synthesis of 35S-labeled proteoglycans that contain either heparin or oversulfated chondroitin sulfate glycosaminoglycans. Although [35S]heparin proteoglycans have been isolated from human lung mast cells of 40-70% purity and from a skin biopsy specimen of a patient with urticaria pigmentosa, no highly sulfated chondroitin sulfate proteoglycan has been isolated from any enriched or highly purified population of human mast cells. We here demonstrate that human lung mast cells of 96% purity incorporate [35S] sulfate into separate heparin and chondroitin sulfate proteoglycans in an approximately equal to 2:1 ratio. As assessed by HPLC of the chondroitinase ABC digests, the chondroitin [35S]sulfate proteoglycans isolated from these human lung mast cells contain the same unusual chondroitin sulfate E disaccharide that is present in proteoglycans produced by interleukin 3-dependent mucosal-like mouse mast cells. Both the chondroitin [35S]sulfate E proteoglycans and the [35S]heparin proteoglycans were exocytosed from the [35S]sulfate-labeled cells via perturbation of the IgE receptor, indicating that both types of 35S-labeled proteoglycans reside in the secretory granules of these human lung mast cells.

Full text

PDF
2284

Selected References

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

  1. Benyon R. C., Lowman M. A., Church M. K. Human skin mast cells: their dispersion, purification, and secretory characterization. J Immunol. 1987 Feb 1;138(3):861–867. [PubMed] [Google Scholar]
  2. Bourdon M. A., Oldberg A., Pierschbacher M., Ruoslahti E. Molecular cloning and sequence analysis of a chondroitin sulfate proteoglycan cDNA. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1321–1325. doi: 10.1073/pnas.82.5.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dayton E. T., Pharr P., Ogawa M., Serafin W. E., Austen K. F., Levi-Schaffer F., Stevens R. L. 3T3 fibroblasts induce cloned interleukin 3-dependent mouse mast cells to resemble connective tissue mast cells in granular constituency. Proc Natl Acad Sci U S A. 1988 Jan;85(2):569–572. doi: 10.1073/pnas.85.2.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Eliakim R., Gilead L., Ligumsky M., Okon E., Rachmilewitz D., Razin E. Histamine and chondroitin sulfate E proteoglycan released by cultured human colonic mucosa: indication for possible presence of E mast cells. Proc Natl Acad Sci U S A. 1986 Jan;83(2):461–464. doi: 10.1073/pnas.83.2.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fox C. C., Dvorak A. M., Peters S. P., Kagey-Sobotka A., Lichtenstein L. M. Isolation and characterization of human intestinal mucosal mast cells. J Immunol. 1985 Jul;135(1):483–491. [PubMed] [Google Scholar]
  6. Gillespie E., Lichtenstein L. M. Histamine release from human leukocytes: studies with deuterium oxide, colchicine, and cytochalasin B. J Clin Invest. 1972 Nov;51(11):2941–2947. doi: 10.1172/JCI107118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Goldstein S. M., Kaempfer C. E., Proud D., Schwartz L. B., Irani A. M., Wintroub B. U. Detection and partial characterization of a human mast cell carboxypeptidase. J Immunol. 1987 Oct 15;139(8):2724–2729. [PubMed] [Google Scholar]
  8. Irani A. A., Schechter N. M., Craig S. S., DeBlois G., Schwartz L. B. Two types of human mast cells that have distinct neutral protease compositions. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4464–4468. doi: 10.1073/pnas.83.12.4464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Irani A. M., Craig S. S., DeBlois G., Elson C. O., Schechter N. M., Schwartz L. B. Deficiency of the tryptase-positive, chymase-negative mast cell type in gastrointestinal mucosa of patients with defective T lymphocyte function. J Immunol. 1987 Jun 15;138(12):4381–4386. [PubMed] [Google Scholar]
  10. Ishizaka T., Conrad D. H., Schulman E. S., Sterk A. R., Ishizaka K. Biochemical analysis of initial triggering events of IgE-mediated histamine release from human lung mast cells. J Immunol. 1983 May;130(5):2357–2362. [PubMed] [Google Scholar]
  11. Katz H. R., Austen K. F., Caterson B., Stevens R. L. Secretory granules of heparin-containing rat serosal mast cells also possess highly sulfated chondroitin sulfate proteoglycans. J Biol Chem. 1986 Oct 15;261(29):13393–13396. [PubMed] [Google Scholar]
  12. Kolset S. O. Oversulfated chondroitin sulfate proteoglycan in cultured human peritoneal macrophages. Biochem Biophys Res Commun. 1986 Sep 14;139(2):377–382. doi: 10.1016/s0006-291x(86)80001-8. [DOI] [PubMed] [Google Scholar]
  13. Lawrence I. D., Warner J. A., Cohan V. L., Hubbard W. C., Kagey-Sobotka A., Lichtenstein L. M. Purification and characterization of human skin mast cells. Evidence for human mast cell heterogeneity. J Immunol. 1987 Nov 1;139(9):3062–3069. [PubMed] [Google Scholar]
  14. Levi-Schaffer F., Austen K. F., Caulfield J. P., Hein A., Gravallese P. M., Stevens R. L. Co-culture of human lung-derived mast cells with mouse 3T3 fibroblasts: morphology and IgE-mediated release of histamine, prostaglandin D2, and leukotrienes. J Immunol. 1987 Jul 15;139(2):494–500. [PubMed] [Google Scholar]
  15. Levi-Schaffer F., Austen K. F., Gravallese P. M., Stevens R. L. Coculture of interleukin 3-dependent mouse mast cells with fibroblasts results in a phenotypic change of the mast cells. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6485–6488. doi: 10.1073/pnas.83.17.6485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Levi-Schaffer F., Dayton E. T., Austen K. F., Hein A., Caulfield J. P., Gravallese P. M., Liu F. T., Stevens R. L. Mouse bone marrow-derived mast cells cocultured with fibroblasts. Morphology and stimulation-induced release of histamine, leukotriene B4, leukotriene C4, and prostaglandin D2. J Immunol. 1987 Nov 15;139(10):3431–3441. [PubMed] [Google Scholar]
  17. Metcalfe D. D., Lewis R. A., Silbert J. E., Rosenberg R. D., Wasserman S. I., Austen K. F. Isolation and characterization of heparin from human lung. J Clin Invest. 1979 Dec;64(6):1537–1543. doi: 10.1172/JCI109613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Metcalfe D. D., Soter N. A., Wasserman S. I., Austen K. F. Identification of sulfated mucopolysaccharides including heparin in the lesional skin of a patient with mastocytosis. J Invest Dermatol. 1980 Apr;74(4):210–215. doi: 10.1111/1523-1747.ep12541737. [DOI] [PubMed] [Google Scholar]
  19. Otsu K., Nakano T., Kanakura Y., Asai H., Katz H. R., Austen K. F., Stevens R. L., Galli S. J., Kitamura Y. Phenotypic changes of bone marrow-derived mast cells after intraperitoneal transfer into W/Wv mice that are genetically deficient in mast cells. J Exp Med. 1987 Mar 1;165(3):615–627. doi: 10.1084/jem.165.3.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Paterson N. A., Wasserman S. I., Said J. W., Austen K. F. Release of chemical mediators from partially purified human lung mast cells. J Immunol. 1976 Oct;117(4):1356–1362. [PubMed] [Google Scholar]
  21. Razin E., Cordon-Cardo C., Good R. A. Growth of a pure population of mouse mast cells in vitro with conditioned medium derived from concanavalin A-stimulated splenocytes. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2559–2561. doi: 10.1073/pnas.78.4.2559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Razin E., Ihle J. N., Seldin D., Mencia-Huerta J. M., Katz H. R., LeBlanc P. A., Hein A., Caulfield J. P., Austen K. F., Stevens R. L. Interleukin 3: A differentiation and growth factor for the mouse mast cell that contains chondroitin sulfate E proteoglycan. J Immunol. 1984 Mar;132(3):1479–1486. [PubMed] [Google Scholar]
  23. Razin E., Stevens R. L., Akiyama F., Schmid K., Austen K. F. Culture from mouse bone marrow of a subclass of mast cells possessing a distinct chondroitin sulfate proteoglycan with glycosaminoglycans rich in N-acetylgalactosamine-4,6-disulfate. J Biol Chem. 1982 Jun 25;257(12):7229–7236. [PubMed] [Google Scholar]
  24. Rothenberg M. E., Caulfield J. P., Austen K. F., Hein A., Edmiston K., Newburger P. E., Stevens R. L. Biochemical and morphological characterization of basophilic leukocytes from two patients with myelogenous leukemia. J Immunol. 1987 Apr 15;138(8):2616–2625. [PubMed] [Google Scholar]
  25. Ruitenberg E. J., Gustowska L., Elgersma A., Ruitenberg H. M. Effect of fixation on the light microscopical visualization of mast cells in the mucosa and connective tissue of the human duodenum. Int Arch Allergy Appl Immunol. 1982;67(3):233–238. doi: 10.1159/000233024. [DOI] [PubMed] [Google Scholar]
  26. Saito H., Yamagata T., Suzuki S. Enzymatic methods for the determination of small quantities of isomeric chondroitin sulfates. J Biol Chem. 1968 Apr 10;243(7):1536–1542. [PubMed] [Google Scholar]
  27. Schechter N. M., Choi J. K., Slavin D. A., Deresienski D. T., Sayama S., Dong G., Lavker R. M., Proud D., Lazarus G. S. Identification of a chymotrypsin-like proteinase in human mast cells. J Immunol. 1986 Aug 1;137(3):962–970. [PubMed] [Google Scholar]
  28. Schulman E. S., MacGlashan D. W., Jr, Peters S. P., Schleimer R. P., Newball H. H., Lichtenstein L. M. Human lung mast cells: purification and characterization. J Immunol. 1982 Dec;129(6):2662–2667. [PubMed] [Google Scholar]
  29. Seldin D. C., Austen K. F., Stevens R. L. Purification and characterization of protease-resistant secretory granule proteoglycans containing chondroitin sulfate di-B and heparin-like glycosaminoglycans from rat basophilic leukemia cells. J Biol Chem. 1985 Sep 15;260(20):11131–11139. [PubMed] [Google Scholar]
  30. Seldin D. C., Seno N., Austen K. F., Stevens R. L. Analysis of polysulfated chondroitin disaccharides by high-performance liquid chromatography. Anal Biochem. 1984 Aug 15;141(1):291–300. doi: 10.1016/0003-2697(84)90459-7. [DOI] [PubMed] [Google Scholar]
  31. Serafin W. E., Dayton E. T., Gravallese P. M., Austen K. F., Stevens R. L. Carboxypeptidase A in mouse mast cells. Identification, characterization, and use as a differentiation marker. J Immunol. 1987 Dec 1;139(11):3771–3776. [PubMed] [Google Scholar]
  32. Serafin W. E., Katz H. R., Austen K. F., Stevens R. L. Complexes of heparin proteoglycans, chondroitin sulfate E proteoglycans, and [3H]diisopropyl fluorophosphate-binding proteins are exocytosed from activated mouse bone marrow-derived mast cells. J Biol Chem. 1986 Nov 15;261(32):15017–15021. [PubMed] [Google Scholar]
  33. Siraganian R. P. An automated continuous-flow system for the extraction and fluorometric analysis of histamine. Anal Biochem. 1974 Feb;57(2):383–394. doi: 10.1016/0003-2697(74)90093-1. [DOI] [PubMed] [Google Scholar]
  34. Stevens R. L., Austen K. F. Effect of p-nitrophenyl-beta-D-xyloside on proteoglycan and glycosaminoglycan biosynthesis in rat serosal mast cell cultures. J Biol Chem. 1982 Jan 10;257(1):253–259. [PubMed] [Google Scholar]
  35. Stevens R. L., Lee T. D., Seldin D. C., Austen K. F., Befus A. D., Bienenstock J. Intestinal mucosal mast cells from rats infected with Nippostrongylus brasiliensis contain protease-resistant chondroitin sulfate di-B proteoglycans. J Immunol. 1986 Jul 1;137(1):291–295. [PubMed] [Google Scholar]
  36. Stevens R. L., Otsu K., Austen K. F. Purification and analysis of the core protein of the protease-resistant intracellular chondroitin sulfate E proteoglycan from the interleukin 3-dependent mouse mast cell. J Biol Chem. 1985 Nov 15;260(26):14194–14200. [PubMed] [Google Scholar]
  37. Strobel S., Miller H. R., Ferguson A. Human intestinal mucosal mast cells: evaluation of fixation and staining techniques. J Clin Pathol. 1981 Aug;34(8):851–858. doi: 10.1136/jcp.34.8.851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tantravahi R. V., Stevens R. L., Austen K. F., Weis J. H. A single gene in mast cells encodes the core peptides of heparin and chondroitin sulfate proteoglycans. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9207–9210. doi: 10.1073/pnas.83.23.9207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Tharp M. D., Kagey-Sobotka A., Fox C. C., Marone G., Lichtenstein L. M., Sullivan T. J. Functional heterogeneity of human mast cells from different anatomic sites: in vitro responses to morphine sulfate. J Allergy Clin Immunol. 1987 Apr;79(4):646–653. doi: 10.1016/s0091-6749(87)80162-8. [DOI] [PubMed] [Google Scholar]
  40. Yurt R. W., Leid R. W., Jr, Austen K. F. Native heparin from rat peritoneal mast cells. J Biol Chem. 1977 Jan 25;252(2):518–521. [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