Literature DB >> 18325577

Chimerism, point mutation, and truncation dramatically transformed mast cell delta-tryptases during primate evolution.

Neil N Trivedi1, Wilfred W Raymond, George H Caughey.   

Abstract

BACKGROUND: Tryptases are serine peptidases stored in mast cell granules. Rodents express 2 soluble tryptases, mast cell proteases (MCPs) 6 and 7. Human alpha- and beta-tryptases are orthologs of MCP-6. However, much of the ancestral MCP-7 ortholog was replaced by parts of other tryptases, creating chimeric delta-tryptase. Human delta-tryptase's limited activity is hypothesized to be due to truncation and processing mutations.
OBJECTIVE: We sought to probe the origins and consequences of mutations in primate delta-tryptases.
METHODS: Prosimian (lemur), monkey (macaque), great ape (orangutan, gorilla, and chimpanzee), and human delta-tryptase genes were identified by means of data mining and genomic sequencing. Resulting genes were analyzed phylogenetically and structurally.
RESULTS: The seminal conversion event generating the delta-tryptase chimera occurred early because all primates studied contain delta-tryptase genes. Truncation, resulting from a nonsense mutation of Trp206, occurred much later, after orangutans and other great apes last shared an ancestor. The Arg-3Gln propeptide mutation occurred most recently, being present in humans and chimpanzees but not in other primates. Surprisingly, the major active tryptase in monkeys is full-length delta-tryptase, not beta-tryptase, which is the main active tryptase in human subjects. Models of macaque delta-tryptase reveal that the segment truncated in human subjects contains antiparallel beta-strands coursing through the substrate-binding cleft, accounting for truncation's drastic effect on activity.
CONCLUSIONS: Transformations in the ancestral MCP-7-like gene during primate evolution caused dramatic variations in function. Although delta-tryptases are nearly inactive in humans, they are active and dominant in monkeys.

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Year:  2008        PMID: 18325577     DOI: 10.1016/j.jaci.2008.01.019

Source DB:  PubMed          Journal:  J Allergy Clin Immunol        ISSN: 0091-6749            Impact factor:   10.793


  11 in total

Review 1.  Mast cell peptidases: chameleons of innate immunity and host defense.

Authors:  Neil N Trivedi; George H Caughey
Journal:  Am J Respir Cell Mol Biol       Date:  2009-11-20       Impact factor: 6.914

Review 2.  Mast cell proteases as pharmacological targets.

Authors:  George H Caughey
Journal:  Eur J Pharmacol       Date:  2015-05-07       Impact factor: 4.432

Review 3.  Protective and pathological roles of mast cells and basophils.

Authors:  David Voehringer
Journal:  Nat Rev Immunol       Date:  2013-04-05       Impact factor: 53.106

4.  Promiscuous processing of human alphabeta-protryptases by cathepsins L, B, and C.

Authors:  Quang T Le; Hae-Ki Min; Han-Zhang Xia; Yoshihiro Fukuoka; Nobuhiko Katunuma; Lawrence B Schwartz
Journal:  J Immunol       Date:  2011-05-11       Impact factor: 5.422

5.  High degree of conservation of the multigene tryptase locus over the past 150-200 million years of mammalian evolution.

Authors:  Jenny M Reimer; Paul B Samollow; Lars Hellman
Journal:  Immunogenetics       Date:  2010-04-10       Impact factor: 2.846

Review 6.  Mast cell proteases as protective and inflammatory mediators.

Authors:  George H Caughey
Journal:  Adv Exp Med Biol       Date:  2011       Impact factor: 2.622

Review 7.  Advances in mechanisms of asthma, allergy, and immunology in 2008.

Authors:  Joshua A Boyce; David Broide; Kenji Matsumoto; Bruce S Bochner
Journal:  J Allergy Clin Immunol       Date:  2009-03       Impact factor: 10.793

8.  Mutational tail loss is an evolutionary mechanism for liberating marapsins and other type I serine proteases from transmembrane anchors.

Authors:  Kavita Raman; Neil N Trivedi; Wilfred W Raymond; Rajkumar Ganesan; Daniel Kirchhofer; George M Verghese; Charles S Craik; Eric L Schneider; Shilpa Nimishakavi; George H Caughey
Journal:  J Biol Chem       Date:  2013-02-27       Impact factor: 5.157

9.  Human subjects are protected from mast cell tryptase deficiency despite frequent inheritance of loss-of-function mutations.

Authors:  Neil N Trivedi; Bani Tamraz; Catherine Chu; Pui-Yan Kwok; George H Caughey
Journal:  J Allergy Clin Immunol       Date:  2009-09-12       Impact factor: 10.793

10.  A simple, sensitive and safe method to determine the human α/β-tryptase genotype.

Authors:  Quang Trong Le; Sahar Lotfi-Emran; Hae-Ki Min; Lawrence B Schwartz
Journal:  PLoS One       Date:  2014-12-29       Impact factor: 3.240

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