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. 1990 Apr;87(8):3230–3234. doi: 10.1073/pnas.87.8.3230

Different mouse mast cell populations express various combinations of at least six distinct mast cell serine proteases.

D S Reynolds 1, R L Stevens 1, W S Lane 1, M H Carr 1, K F Austen 1, W E Serafin 1
PMCID: PMC53869  PMID: 2326280

Abstract

Mouse serosal mast cells (SMCs) and Kirsten sarcoma virus-immortalized mast cells store large amounts of mast cell carboxypeptidase A and serine proteases in their secretory granules. Secretory granule proteins from 2.6 x 10(6) purified SMCs were separated by NaDodSO4/PAGE, trans-blotted to poly(vinylidine difluoride) membranes, and subjected to amino-terminal amino acid sequencing. Four distinct mast cell serine proteases were identified. With mast cell carboxypeptidase A, these serine proteases comprise the major proteins of mouse SMC secretory granules. Each of the four SMC serine proteases was distinct from the two serine proteases present in mucosal mast cells in the intestines of helminth-infected mice. The secretory granules of a Kirsten sarcoma virus-immortalized mast cell line contained three of the SMC-derived serine proteases and one of the mucosal mast cell-derived serine proteases. Thus, the family of mouse mast cell secretory granule serine proteases has at least six distinct members that can be expressed in different combinations in different mast cell populations.

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Selected References

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

  1. Benfey P. N., Yin F. H., Leder P. Cloning of the mast cell protease, RMCP II. Evidence for cell-specific expression and a multi-gene family. J Biol Chem. 1987 Apr 15;262(11):5377–5384. [PubMed] [Google Scholar]
  2. Caughey G. H., Viro N. F., Ramachandran J., Lazarus S. C., Borson D. B., Nadel J. A. Dog mastocytoma tryptase: affinity purification, characterization, and amino-terminal sequence. Arch Biochem Biophys. 1987 Nov 1;258(2):555–563. doi: 10.1016/0003-9861(87)90377-8. [DOI] [PubMed] [Google Scholar]
  3. DuBuske L., Austen K. F., Czop J., Stevens R. L. Granule-associated serine neutral proteases of the mouse bone marrow-derived mast cell that degrade fibronectin: their increase after sodium butyrate treatment of the cells. J Immunol. 1984 Sep;133(3):1535–1541. [PubMed] [Google Scholar]
  4. Enerbäck L. Mast cells in rat gastrointestinal mucosa. 2. Dye-binding and metachromatic properties. Acta Pathol Microbiol Scand. 1966;66(3):303–312. doi: 10.1111/apm.1966.66.3.303. [DOI] [PubMed] [Google Scholar]
  5. Gershenfeld H. K., Weissman I. L. Cloning of a cDNA for a T cell-specific serine protease from a cytotoxic T lymphocyte. Science. 1986 May 16;232(4752):854–858. doi: 10.1126/science.2422755. [DOI] [PubMed] [Google Scholar]
  6. Gibson S., Miller H. R. Mast cell subsets in the rat distinguished immunohistochemically by their content of serine proteinases. Immunology. 1986 May;58(1):101–104. [PMC free article] [PubMed] [Google Scholar]
  7. HUMMEL B. C. A modified spectrophotometric determination of chymotrypsin, trypsin, and thrombin. Can J Biochem Physiol. 1959 Dec;37:1393–1399. [PubMed] [Google Scholar]
  8. Hunkapiller M. W., Lujan E., Ostrander F., Hood L. E. Isolation of microgram quantities of proteins from polyacrylamide gels for amino acid sequence analysis. Methods Enzymol. 1983;91:227–236. doi: 10.1016/s0076-6879(83)91019-4. [DOI] [PubMed] [Google Scholar]
  9. Kido H., Fukusen N., Katunuma N. Chymotrypsin- and trypsin-type serine proteases in rat mast cells: properties and functions. Arch Biochem Biophys. 1985 Jun;239(2):436–443. doi: 10.1016/0003-9861(85)90709-x. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Lagunoff D., Pritzl P. Characterization of rat mast cell granule proteins. Arch Biochem Biophys. 1976 Apr;173(2):554–563. doi: 10.1016/0003-9861(76)90292-7. [DOI] [PubMed] [Google Scholar]
  12. Le Trong H., Neurath H., Woodbury R. G. Substrate specificity of the chymotrypsin-like protease in secretory granules isolated from rat mast cells. Proc Natl Acad Sci U S A. 1987 Jan;84(2):364–367. doi: 10.1073/pnas.84.2.364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Le Trong H., Parmelee D. C., Walsh K. A., Neurath H., Woodbury R. G. Amino acid sequence of rat mast cell protease I (chymase). Biochemistry. 1987 Nov 3;26(22):6988–6994. doi: 10.1021/bi00396a020. [DOI] [PubMed] [Google Scholar]
  14. Lobe C. G., Finlay B. B., Paranchych W., Paetkau V. H., Bleackley R. C. Novel serine proteases encoded by two cytotoxic T lymphocyte-specific genes. Science. 1986 May 16;232(4752):858–861. doi: 10.1126/science.3518058. [DOI] [PubMed] [Google Scholar]
  15. Masson D., Tschopp J. A family of serine esterases in lytic granules of cytolytic T lymphocytes. Cell. 1987 Jun 5;49(5):679–685. doi: 10.1016/0092-8674(87)90544-7. [DOI] [PubMed] [Google Scholar]
  16. Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem. 1987 Jul 25;262(21):10035–10038. [PubMed] [Google Scholar]
  17. Miller H. R., Jarrett W. F. Immune reactions in mucous membranes. I. Intestinal mast cell response during helminth expulsion in the rat. Immunology. 1971 Mar;20(3):277–288. [PMC free article] [PubMed] [Google Scholar]
  18. Miller J. S., Westin E. H., Schwartz L. B. Cloning and characterization of complementary DNA for human tryptase. J Clin Invest. 1989 Oct;84(4):1188–1195. doi: 10.1172/JCI114284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nakano T., Sonoda T., Hayashi C., Yamatodani A., Kanayama Y., Yamamura T., Asai H., Yonezawa T., Kitamura Y., Galli S. J. Fate of bone marrow-derived cultured mast cells after intracutaneous, intraperitoneal, and intravenous transfer into genetically mast cell-deficient W/Wv mice. Evidence that cultured mast cells can give rise to both connective tissue type and mucosal mast cells. J Exp Med. 1985 Sep 1;162(3):1025–1043. doi: 10.1084/jem.162.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Newlands G. F., Gibson S., Knox D. P., Grencis R., Wakelin D., Miller H. R. Characterization and mast cell origin of a chymotrypsin-like proteinase isolated from intestines of mice infected with Trichinella spiralis. Immunology. 1987 Dec;62(4):629–634. [PMC free article] [PubMed] [Google Scholar]
  21. Pasternack M. S., Eisen H. N. A novel serine esterase expressed by cytotoxic T lymphocytes. 1985 Apr 25-May 1Nature. 314(6013):743–745. doi: 10.1038/314743a0. [DOI] [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. Reynolds D. S., Serafin W. E., Faller D. V., Wall D. A., Abbas A. K., Dvorak A. M., Austen K. F., Stevens R. L. Immortalization of murine connective tissue-type mast cells at multiple stages of their differentiation by coculture of splenocytes with fibroblasts that produce Kirsten sarcoma virus. J Biol Chem. 1988 Sep 5;263(25):12783–12791. [PubMed] [Google Scholar]
  25. Reynolds D. S., Stevens R. L., Gurley D. S., Lane W. S., Austen K. F., Serafin W. E. Isolation and molecular cloning of mast cell carboxypeptidase A. A novel member of the carboxypeptidase gene family. J Biol Chem. 1989 Nov 25;264(33):20094–20099. [PubMed] [Google Scholar]
  26. 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]
  27. Schwartz L. B., Lewis R. A., Austen K. F. Tryptase from human pulmonary mast cells. Purification and characterization. J Biol Chem. 1981 Nov 25;256(22):11939–11943. [PubMed] [Google Scholar]
  28. Schägger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 1987 Nov 1;166(2):368–379. doi: 10.1016/0003-2697(87)90587-2. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Serafin W. E., Reynolds D. S., Rogelj S., Lane W. S., Conder G. A., Johnson S. S., Austen K. F., Stevens R. L. Identification and molecular cloning of a novel mouse mucosal mast cell serine protease. J Biol Chem. 1990 Jan 5;265(1):423–429. [PubMed] [Google Scholar]
  31. 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]
  32. Trong H. L., Newlands G. F., Miller H. R., Charbonneau H., Neurath H., Woodbury R. G. Amino acid sequence of a mouse mucosal mast cell protease. Biochemistry. 1989 Jan 10;28(1):391–395. doi: 10.1021/bi00427a054. [DOI] [PubMed] [Google Scholar]
  33. Vanderslice P., Craik C. S., Nadel J. A., Caughey G. H. Molecular cloning of dog mast cell tryptase and a related protease: structural evidence of a unique mode of serine protease activation. Biochemistry. 1989 May 16;28(10):4148–4155. doi: 10.1021/bi00436a004. [DOI] [PubMed] [Google Scholar]
  34. Woodbury R. G., Everitt M. T., Neurath H. Mast cell proteases. Methods Enzymol. 1981;80(Pt 100):588–609. doi: 10.1016/s0076-6879(81)80047-x. [DOI] [PubMed] [Google Scholar]
  35. Woodbury R. G., Gruzenski G. M., Lagunoff D. Immunofluorescent localization of a serine protease in rat small intestine. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2785–2789. doi: 10.1073/pnas.75.6.2785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Woodbury R. G., Katunuma N., Kobayashi K., Titani K., Neurath H., Anderson W. F., Matthews B. W. Covalent structure of a group-specific protease from rat small intestine. Appendix: crystallographic data for a group specific protease from rat intestine. Biochemistry. 1978 Mar 7;17(5):811–819. doi: 10.1021/bi00598a010. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. Yurt R., Austen K. F. Preparative purification of the rat mast cell chymase: characterization and interaction with granule components. J Exp Med. 1977 Nov 1;146(5):1405–1419. doi: 10.1084/jem.146.5.1405. [DOI] [PMC free article] [PubMed] [Google Scholar]

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