Mouse Chromosome 17A3.3 Contains 13 Genes That Encode Functional Tryptic-like Serine Proteases with Distinct Tissue and Cell Expression Patterns

Abstract

Probing of the mouse EST data base at GenBank™ with known tryptase cDNAs resulted in the identification of undiscovered serine protease transcripts whose genes reside at a 1.5-Mb complex on mouse chromosome 17A3.3. Mouse tryptase-5 (mT5), tryptase-6 (mT6), and mast cell protease-11 (mMCP-11) are new members of this serine protease superfamily whose amino acid sequences are 36–54% identical to each other and to their other 10 family members. The 13 functional mouse proteases can be subdivided into two subgroups based on conserved features in their propeptides. Of the three new serine proteases, mT6 is most widely expressed in tissues. mT5 is preferentially expressed in smooth muscle, whereas mMCP-11 is preferentially expressed in the spleen and bone marrow. In contrast to mT5 and mT6, mMCP-11 is also expressed in mast cells. Although mT6 and mMCP-11 are constitutively secreted when expressed in mammalian and insect cells, mT5 remains membrane-associated. The fact that recombinant mT5, mT6, and mMCP-11 possess non-identical expression patterns and substrate specificities suggests that each protease has a unique function in vivo. Of the 13 functional mouse tryptase genes identified at the complex, 12 have orthologs that reside in the syntenic region of human chromosome 16p13.3. The establishment of these ortholog pairs helps clarify the evolutionary relationship of the serine protease locus in the two species. This information provides a useful framework for the functional analysis of each protease using gene targeting and other molecular approaches. Probing of the mouse EST data base at GenBank™ with known tryptase cDNAs resulted in the identification of undiscovered serine protease transcripts whose genes reside at a 1.5-Mb complex on mouse chromosome 17A3.3. Mouse tryptase-5 (mT5), tryptase-6 (mT6), and mast cell protease-11 (mMCP-11) are new members of this serine protease superfamily whose amino acid sequences are 36–54% identical to each other and to their other 10 family members. The 13 functional mouse proteases can be subdivided into two subgroups based on conserved features in their propeptides. Of the three new serine proteases, mT6 is most widely expressed in tissues. mT5 is preferentially expressed in smooth muscle, whereas mMCP-11 is preferentially expressed in the spleen and bone marrow. In contrast to mT5 and mT6, mMCP-11 is also expressed in mast cells. Although mT6 and mMCP-11 are constitutively secreted when expressed in mammalian and insect cells, mT5 remains membrane-associated. The fact that recombinant mT5, mT6, and mMCP-11 possess non-identical expression patterns and substrate specificities suggests that each protease has a unique function in vivo. Of the 13 functional mouse tryptase genes identified at the complex, 12 have orthologs that reside in the syntenic region of human chromosome 16p13.3. The establishment of these ortholog pairs helps clarify the evolutionary relationship of the serine protease locus in the two species. This information provides a useful framework for the functional analysis of each protease using gene targeting and other molecular approaches. The serine protease gene cluster at chromosome 16p13.3 contains the genes that encode human tryptase α (1.Miller J.S. Westin E.H. Schwartz L.B. J. Clin. Investig. 1989; 84: 1188-1195Crossref PubMed Scopus (177) Google Scholar), tryptase βI (2.Vanderslice P. Ballinger S.M. Tam E.K. Goldstein S.M. Craik C.S. Caughey G.H. Proc. Natl. Acad. Sci. U. S. A. 1990; 87: 3811-3815Crossref PubMed Scopus (202) Google Scholar), tryptase βII (2.Vanderslice P. Ballinger S.M. Tam E.K. Goldstein S.M. Craik C.S. Caughey G.H. Proc. Natl. Acad. Sci. U. S. A. 1990; 87: 3811-3815Crossref PubMed Scopus (202) Google Scholar, 3.Miller J.S. Moxley G. Schwartz L.B. J. Clin. Investig. 1990; 86: 864-870Crossref PubMed Scopus (153) Google Scholar), tryptase βIII (2.Vanderslice P. Ballinger S.M. Tam E.K. Goldstein S.M. Craik C.S. Caughey G.H. Proc. Natl. Acad. Sci. U. S. A. 1990; 87: 3811-3815Crossref PubMed Scopus (202) Google Scholar), transmembrane tryptase (TMT) 1The abbreviations used are: TMT, transmembrane tryptase; Bssp-4, brain-specific serine protease-4; Disp, distal intestinal serine protease; Esp-1, eosinophil serine protease-1; G3PDH, glyceraldehyde-3-phosphate dehydrogenase; GPI, glycosylphosphatidylinositol; IL, interleukin; MC, mast cell; Isp, implantation serine protease; mMCP, mouse MC protease; mT4, mouse tryptase-4; mT5, mouse tryptase-5; mT6, mouse tryptase-6; PPACK, d-phenylalanyl-l-prolyl-l-arginine chloromethyl ketone; PRSS, protease serine member S; Tessp1, testis serine protease-1; PNGaseF, peptide:N-glycosidase; pNA, p-nitroanilide; mBMMCs, mouse bone marrow-derived MCs.1The abbreviations used are: TMT, transmembrane tryptase; Bssp-4, brain-specific serine protease-4; Disp, distal intestinal serine protease; Esp-1, eosinophil serine protease-1; G3PDH, glyceraldehyde-3-phosphate dehydrogenase; GPI, glycosylphosphatidylinositol; IL, interleukin; MC, mast cell; Isp, implantation serine protease; mMCP, mouse MC protease; mT4, mouse tryptase-4; mT5, mouse tryptase-5; mT6, mouse tryptase-6; PPACK, d-phenylalanyl-l-prolyl-l-arginine chloromethyl ketone; PRSS, protease serine member S; Tessp1, testis serine protease-1; PNGaseF, peptide:N-glycosidase; pNA, p-nitroanilide; mBMMCs, mouse bone marrow-derived MCs./tryptase γ (4.Wong G.W. Tang Y. Feyfant E. Šali A. Li L. Li Y. Huang C. Friend D.S. Krilis S.A. Stevens R.L. J. Biol. Chem. 1999; 274: 30784-30793Abstract Full Text Full Text PDF PubMed Scopus (84) Google Scholar, 5.Caughey G.H. Raymond W.W. Blount J.L. Hau L.W. Pallaoro M. Wolters P.J. Verghese G.M. J. Immunol. 2000; 164: 6566-6575Crossref PubMed Scopus (103) Google Scholar), tryptase δ (6.Pallaoro M. Fejzo M.S. Shayesteh L. Blount J.L. Caughey G.H. J. Biol. Chem. 1999; 274: 3355-3362Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar), tryptase ϵ/protease serine member S22 (PRSS22) (7.Wong G.W. Yasuda S. Madhusudhan M.S. Li L. Yang Y. Krilis S.A. Šali A. Stevens R.L. J. Biol. Chem. 2001; 276: 49169-49182Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar), pancreasin/marapsin/PRSS27 (8.Bhagwandin V.J. Hau L.W. Mallen-St. Clair J. Wolters P.J. Caughey G.H. J. Biol. Chem. 2003; 278: 3363-3371Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar), eosinophil serine protease-1 M. M. PubMed Scopus Google Scholar, J.L. 1999; Google Scholar), and C. J.S. P. J. 2003; PubMed Scopus Google are genes and the locus that encode to the of (7.Wong G.W. Yasuda S. Madhusudhan M.S. Li L. Yang Y. Krilis S.A. Šali A. Stevens R.L. J. Biol. Chem. 2001; 276: 49169-49182Abstract Full Text Full Text PDF PubMed Scopus (47) Google The region of human chromosome these genes reside is at a the of the in J. 2000; PubMed Scopus Google for this is that is evolutionary to of the genes and of the and The serine protease locus in the mouse at chromosome 17A3.3. this 10 genes identified at the that encode mouse mast cell protease D.S. D.S. J. Biol. Chem. Full Text PDF PubMed Google Scholar), D.S. D.S. Stevens R.L. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar), (4.Wong G.W. Tang Y. Feyfant E. Šali A. Li L. Li Y. Huang C. Friend D.S. Krilis S.A. 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Chem. 2003; 278: 3363-3371Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar), implantation serine protease 2001; PubMed Scopus Google Scholar), and 2001; PubMed Scopus Google Of these proteases, and have expressed and the recombinant proteases each member of this family of serine proteases to a unique that also is that of of and that recombinant and possess substrate specificities C. G.W. Šali A. Stevens R.L. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, C. Friend D.S. G.W. G. J. Stevens R.L. J. Immunol. Google and also have to be (7.Wong G.W. Yasuda S. Madhusudhan M.S. Li L. Yang Y. Krilis S.A. Šali A. Stevens R.L. J. Biol. Chem. 2001; 276: 49169-49182Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar, C. Li L. Krilis S.A. Tang Y. Li Stevens R.L. J. Biol. Chem. 1999; 274: Full Text Full Text PDF PubMed Scopus Google Scholar, C. P.J. Friend D.S. Stevens R.L. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google Scholar, J.L. A. M. M. Craik C.S. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google Scholar, G.W. Yasuda S. S. G. Li L. Krilis S.A. Stevens R.L. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, A. M. J. Immunol. PubMed Scopus Google In to their in of recombinant βI into the the of to a C. P.J. Friend D.S. Stevens R.L. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google This is in the of βI and to of C. Friend D.S. G.W. G. J. Stevens R.L. J. Immunol. Google Scholar, C. P.J. Friend D.S. Stevens R.L. J. Biol. Chem. 2001; 276: Full Text Full Text PDF PubMed Scopus Google Scholar, J. U. M. L. G. 2000; PubMed Scopus Google In of these in C. G. M. J. Immunol. PubMed Scopus Google that can be in the tryptase Although the amino acid sequences of D.S. D.S. J. Biol. Chem. Full Text PDF PubMed Google and D.S. D.S. Stevens R.L. Proc. Natl. Acad. Sci. U. S. A. 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