Online citations, reference lists, and bibliographies.
Please confirm you are human
(Sign Up for free to never see this)
← Back to Search

Expansion Of The Mast Cell Chymase Locus Over The Past 200 Million Years Of Mammalian Evolution

Maike Gallwitz, J. Reimer, L. Hellman
Published 2006 · Biology, Medicine

Save to my Library
Download PDF
Analyze on Scholarcy
Share
The acidic granules of natural killer (NK) cells, T cells, mast cells, and neutrophils store large amounts of serine proteases. Functionally, these proteases are involved, e.g., in the induction of apoptosis, the recruitment of inflammatory cells, and the remodeling of extra-cellular matrix. Among the granule proteases are the phylogenetically related mast cell chymases, neutrophil cathepsin G, and T-cell granzymes (Gzm B to H and Gzm N), which share the characteristic absence of a Cys191–Cys220 bridge. The genes of these proteases are clustered in one locus, the mast cell chymase locus, in all previously investigated mammals. In this paper, we present a detailed analysis of the chymase locus in cattle (Bos taurus) and opossum (Monodelphis domestica). The gained information delineates the evolution of the chymase locus over more than 200 million years. Surprisingly, the cattle chymase locus contains two α-chymase and two cathepsin G genes where all other studied chymase loci have single genes. Moreover, the cattle locus holds at least four genes for duodenases, which are not found in other chymase loci. Interestingly, duodenases seem to have digestive rather than immune functions. In opossum, on the other hand, only two chymase locus-related genes have been identified. These two genes are not arranged in one locus, but appear to have been separated by a marsupial-specific chromosomal rearrangement. Phylogenetic analyses place one of the opossum genes firmly with mast cell α-chymases, which indicates that the α-chymase had already evolved as a separate, clearly identifiable gene before the separation of marsupials and placental mammals. In contrast, the second gene in opossum is positioned phylogenetically between granzymes, cathepsin G, and the duodenases. These genes, therefore, probably evolved as separate subfamilies after the separation of placental mammals from marsupials. In platypus, only one chymase locus-like sequence could be identified. This previously published “granzyme” does not cluster clearly with any of the chymase locus gene families, but shares the absence of the Cys191–Cys220 bridge with the other chymase locus proteases. These findings indicate that all chymase locus genes are derived from a single ancestor that was present more than 200 million years ago.
This paper references
Angiotensin II generation by mast cell alpha- and beta-chymases.
G. Caughey (2000)
10.1023/A:1023006317321
Graspases—a Special Group of Serine Proteases of the Chymotrypsin Family That Has Lost a Conserved Active Site Disulfide Bond
T. S. Zamolodchikova (2004)
Quantitation of histamine, tryptase, and chymase in dispersed human T and TC mast cells.
L. Schwartz (1987)
10.1042/BJ3210665
Sheep mast cell proteinase-1: characterization as a member of a new class of dual-specific ruminant chymases.
A. Pemberton (1997)
10.1093/NAR/25.24.4876
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
J. Thompson (1997)
10.2210/pdb3rp2/pdb
The structure of rat mast cell protease II at 1.9-A resolution.
S. Remington (1988)
10.1016/S0168-9525(02)02772-5
Marsupial genetics and genomics.
J. Graves (2002)
10.1101/GR.2034704
Characterization of evolutionary rates and constraints in three Mammalian genomes.
G. Cooper (2004)
10.1016/J.DCI.2005.10.014
Granzyme-like sequences in bony fish shed light on the emergence of hematopoietic serine proteases during vertebrate evolution.
S. Wernersson (2006)
10.1073/PNAS.0408539102
Comparative sequencing provides insights about the structure and conservation of marsupial and monotreme genomes.
E. H. Margulies (2005)
10.1016/S1097-2765(03)00308-3
A despecialization step underlying evolution of a family of serine proteases.
M. A. Wouters (2003)
10.1101/GR.1064503
Quantitative estimates of sequence divergence for comparative analyses of mammalian genomes.
G. Cooper (2003)
10.1111/J.1432-1033.1995.0866P.X
Duodenase, a new serine protease of unusual specificity from bovine duodenal mucosa. Primary structure of the enzyme.
T. S. Zamolodchikova (1995)
10.1016/S0167-4838(98)00085-5
Specificity of human cathepsin G.
J. Polanowska (1998)
10.1016/S0161-5890(02)00087-1
New developments in the genetics and activation of mast cell proteases.
G. Caughey (2002)
10.1016/S0167-4838(00)00076-5
Angiotensin II generation by mast cell α- and β-chymases
G. Caughey (2000)
10.1081/RRS-200054355
Species Differences in Angiotensin II Generation and Degradation by Mast Cell Chymases
Y. Kunori (2005)
10.1007/s00251-003-0560-2
Evolution of major histocompatibility complex class I genes in Cetartiodactyls
E. Holmes (2003)
Cutting Edge – Cleavage Specificity and Biochemical Characterization of Mast Cell Serine Proteases
U. Karlson (2003)
10.1074/jbc.274.43.30468
The Human Cytotoxic T Cell Granule Serine Protease Granzyme H Has Chymotrypsin-like (Chymase) Activity and Is Taken Up into Cytoplasmic Vesicles Reminiscent of Granzyme B-containing Endosomes*
K. Edwards (1999)
10.1074/JBC.M410396200
A Key Role for Mast Cell Chymase in the Activation of Pro-matrix Metalloprotease-9 and Pro-matrix Metalloprotease-2*
E. Tchougounova (2005)
10.1016/J.CCCN.2004.04.019
Human chymase degrades human fibronectin.
K. Okumura (2004)
10.1101/GR.1946304
A genomic analysis of rat proteases and protease inhibitors.
X. S. Puente (2004)
10.1084/jem.20030671
The Chymase, Mouse Mast Cell Protease 4, Constitutes the Major Chymotrypsin-like Activity in Peritoneum and Ear Tissue. A Role for Mouse Mast Cell Protease 4 in Thrombin Regulation and Fibronectin Turnover
E. Tchougounova (2003)
10.1038/nature02426
Genome sequence of the Brown Norway rat yields insights into mammalian evolution
R. Gibbs (2004)
10.1038/NSB0694-364
Conversion of the substrate specificity of mouse proteinase granzyme B
A. Caputo (1994)
10.1073/PNAS.94.17.9017
Chymase cleavage of stem cell factor yields a bioactive, soluble product.
B. Longley (1997)
10.1074/jbc.M301512200
Extended Substrate Specificity of Rat Mast Cell Protease 5, a Rodent α-Chymase with Elastase-like Primary Specificity*
U. Karlson (2003)
10.1002/PRO.5560040301
Structural basis of substrate specificity in the serine proteases
J. Perona (1995)
10.1042/BJ3330801
Sheep mast-cell proteinases-1 and -3: cDNA cloning, primary structure and molecular modelling of the enzymes and further studies on substrate specificity.
S. McAleese (1998)
10.1007/s002390010060
The Mitochondrial Genome of the Sperm Whale and a New Molecular Reference for Estimating Eutherian Divergence Dates
U. Arnason (2000)
10.1016/S1055-7903(03)00113-1
The evolution of tribospheny and the antiquity of mammalian clades.
M. O. Woodburne (2003)
10.1002/j.1460-2075.1996.tb00933.x
The 1.8 A crystal structure of human cathepsin G in complex with Suc‐Val‐Pro‐PheP‐(OPh)2: a Janus‐faced proteinase with two opposite specificities.
P. Hof (1996)
10.1093/MOLBEV/MSJ064
The platypus is in its place: nuclear genes and indels confirm the sister group relation of monotremes and Therians.
Teun van Rheede (2006)
10.1073/pnas.0334222100
Placental mammal diversification and the Cretaceous–Tertiary boundary
M. Springer (2003)
PHYLIP-Phylogeny Interference Package (Version 3.2)
J Felsenstein (1989)
10.1038/31927
A molecular timescale for vertebrate evolution
S. Kumar (1998)
10.1111/J.1432-1033.1997.T01-1-00612.X
Subcellular localization, substrate specificity and crystallization of duodenase, a potential activator of enteropeptidase.
T. S. Zamolodchikova (1997)
10.1093/OXFORDJOURNALS.MOLBEV.A003860
Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes.
R. Adkins (2001)
10.1046/J.1432-1033.2002.03316.X
Rodent α‐chymases are elastase‐like proteases
Y. Kunori (2002)
10.1007/s00239-002-2396-z
Molecular Evolution of Vertebrate Goose-Type Lysozyme Genes
D. Irwin (2003)
10.1007/BF02337544
Evolutionary histories of highly repeated DNA families among the artiodactyla (mammalia)
W. Modi (2006)
10.1002/(SICI)1521-4141(199803)28:03<1022::AID-IMMU1022>3.0.CO;2-1
Characterization of mouse mast cell protease‐8, the first member of a novel subfamily of mouse mast cell serine proteases, distinct from both the classical chymases and tryptases
C. Lützelschwab (1998)
Codon-substitution models for heterogeneous selection pressure at amino acid sites.
Z. Yang (2000)
10.1016/S0021-9150(00)00544-X
Chymase bound to heparin is resistant to its natural inhibitors and capable of proteolyzing high density lipoproteins in aortic intimal fluid.
L. Lindstedt (2001)
10.1038/78992
The structure of the pro-apoptotic protease granzyme B reveals the molecular determinants of its specificity
S. M. Waugh (2000)
10.1101/GR.1967904
Identification of evolutionary hotspots in the rodent genomes.
V. B. Yap (2004)
10.1016/s0021-9258(18)52407-8
Human cytotoxic lymphocyte granzyme B. Its purification from granules and the characterization of substrate and inhibitor specificity.
M. Poe (1991)
10.1002/1097-0134(20001001)41:1<8::AID-PROT30>3.0.CO;2-2
Crystal structure of bovine duodenase, a serine protease, with dual trypsin and chymotrypsin‐like specificities
V. Pletnev (2000)
10.1074/jbc.272.41.25628
Dog Mast Cell α-Chymase Activates Progelatinase B by Cleaving the Phe88-Gln89 and Phe91-Glu92 Bonds of the Catalytic Domain*
K. Fang (1997)
10.1074/jbc.M304087200
Albumin Is a Substrate of Human Chymase
W. Raymond (2003)
Selective conversion of big endothelins to tracheal smooth muscle-constricting 31-amino acid-length endothelins by chymase from human mast cells.
A. Nakano (1997)
10.1007/s002510000246
Identification and structural analysis of four serine proteases in a monotreme, the platypus, Ornithorhynchus anatinus
M. Poorafshar (2000)
10.1007/s00251-006-0123-4
Rapid lineage-specific diversification of the mast cell chymase locus during mammalian evolution
Maike Gallwitz (2006)



This paper is referenced by
10.1371/journal.pone.0143091
Granule Associated Serine Proteases of Hematopoietic Cells – An Analysis of Their Appearance and Diversification during Vertebrate Evolution
Srinivas Akula (2015)
10.1371/journal.pone.0048308
Human Cord Blood Derived Immature Basophils Show Dual Characteristics, Expressing Both Basophil and Eosinophil Associated Proteins
J. Grundström (2012)
caspase-independent cell-death program derived human granzyme H induces an alternative, - Natural killer cell
E. Fellows (2013)
10.1007/978-1-60327-951-2_6
Protease Mediators of Anaphylaxis
G. Caughey (2011)
Mast cell recruitment and activation as measures of cyathostomin burden
Ruth Clements (2015)
10.4155/fmc-2016-0030
In silico approach to find chymase inhibitors among biogenic compounds.
Amit Dubey (2016)
10.1182/BLOOD-2006-10-051649
Natural killer cell-derived human granzyme H induces an alternative, caspase-independent cell-death program.
E. Fellows (2007)
10.1016/S0065-2776(07)95006-3
Mast cell proteases.
G. Pejler (2007)
10.1111/j.1742-4658.2010.07642.x
Arg143 and Lys192 of the human mast cell chymase mediate the preference for acidic amino acids in position P2′ of substrates
M. Andersson (2010)
10.1074/jbc.M707157200
Structural Basis for Elastolytic Substrate Specificity in Rodent α-Chymases*
J. Kervinen (2008)
10.1093/intimm/dxs081
Extended cleavage specificity of the mast cell chymase from the crab-eating macaque (Macaca fascicularis): an interesting animal model for the analysis of the function of the human mast cell chymase.
M. Thorpe (2012)
10.1007/s00251-007-0202-1
Expression profile of novel members of the rat mast cell protease (rMCP)-2 and (rMCP)-8 families, and functional analyses of mouse mast cell protease (mMCP)-8
Maike Gallwitz (2007)
10.4049/jimmunol.1002292
How Immune Peptidases Change Specificity: Cathepsin G Gained Tryptic Function but Lost Efficiency during Primate Evolution
W. Raymond (2010)
10.1007/s00251-010-0443-2
High degree of conservation of the multigene tryptase locus over the past 150–200 million years of mammalian evolution
J. Reimer (2010)
during Primate Evolution Tryptic Function but Lost Efficiency Specificity: Cathepsin G Gained How Immune Peptidases Change
C. Craik (2010)
10.1074/jbc.M710502200
Guinea Pig Chymase Is Leucine-specific
G. Caughey (2008)
10.1016/j.ejphar.2015.04.045
Mast cell proteases as pharmacological targets.
G. Caughey (2016)
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 429 Cleavage Specificity of Mast Cell
M. Andersson (2008)
This information is current as Lost Efficiency during Primate Evolution Cathepsin G Gained Tryptic Function but How Immune Peptidases Change Specificity :
Wilfred W. Raymond (2010)
10.3390/ijms21010319
Extended Cleavage Specificities of Two Mast Cell Chymase-Related Proteases and One Granzyme B-Like Protease from the Platypus, a Monotreme
Zhirong Fu (2020)
10.1016/j.coi.2018.06.006
Mast cells and basophils in allergic inflammation.
M. Kubo (2018)
Peptidases in Ancestral Vertebrates-Like Transmembrane γ Evolved from Rapidly during Primate Speciation and Tryptases Changed
George H. Caughey (2007)
10.1371/journal.pone.0131720
rMCP-2, the Major Rat Mucosal Mast Cell Protease, an Analysis of Its Extended Cleavage Specificity and Its Potential Role in Regulating Intestinal Permeability by the Cleavage of Cell Adhesion and Junction Proteins
Zhirong Fu (2015)
10.1016/j.bcp.2010.06.014
Potency variation of small-molecule chymase inhibitors across species.
J. Kervinen (2010)
10.1111/imr.12548
Recent advances in understanding basophil‐mediated Th2 immune responses
Y. Yamanishi (2017)
10.1007/s00251-018-1062-6
Identification and annotation of bovine granzyme genes reveals a novel granzyme encoded within the trypsin-like locus
J. Yang (2018)
10.1111/j.1600-065X.2007.00509.x
Mast cell tryptases and chymases in inflammation and host defense
G. Caughey (2007)
10.1515/hsz-2014-0174
Analysis of the evolution of granule associated serine proteases of immune defence (GASPIDs) suggests a revised nomenclature
Jamshaid Ahmad (2014)
10.1111/J.1750-3841.2006.00131.X
Soy-derived immunoglobulin production stimulating factor enhances IgM production of mouse spleen lymphocytes
N. Maeda (2006)
10.3390/ijms20246340
Extended Cleavage Specificities of Rabbit and Guinea Pig Mast Cell Chymases: Two Highly Specific Leu-Ases
Yuan Zhongwei (2019)
Cleavage Specificity of Mast Cell Chymases
M. Andersson (2008)
Supplemental Section S1 – Genome Sequencing and Assembly........................................... 2 Supplemental Section S2 – Indel Assessment with the Neutral Indel Model ................11 Supplemental Section S3 – Great Ape Divergence Estimate via Wgs Read Mapping..11 Supplemental Section S7 –
()
See more
Semantic Scholar Logo Some data provided by SemanticScholar