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Loss and Gain of Human Acidic Mammalian Chitinase Activity by Nonsynonymous SNPs

Acidic mammalian chitinase (AMCase) is implicated in asthma, allergic inflammation, and food processing. Little is known about genetic and evolutional regulation of chitinolytic activity of AMCase. Here, we relate human AMCase polymorphisms to the mouse AMCase, and show that the highly active varian...

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Autores principales: Okawa, Kazuaki, Ohno, Misa, Kashimura, Akinori, Kimura, Masahiro, Kobayashi, Yuki, Sakaguchi, Masayoshi, Sugahara, Yasusato, Kamaya, Minori, Kino, Yoshihiro, Bauer, Peter O., Oyama, Fumitaka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100053/
https://www.ncbi.nlm.nih.gov/pubmed/27702777
http://dx.doi.org/10.1093/molbev/msw198
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author Okawa, Kazuaki
Ohno, Misa
Kashimura, Akinori
Kimura, Masahiro
Kobayashi, Yuki
Sakaguchi, Masayoshi
Sugahara, Yasusato
Kamaya, Minori
Kino, Yoshihiro
Bauer, Peter O.
Oyama, Fumitaka
author_facet Okawa, Kazuaki
Ohno, Misa
Kashimura, Akinori
Kimura, Masahiro
Kobayashi, Yuki
Sakaguchi, Masayoshi
Sugahara, Yasusato
Kamaya, Minori
Kino, Yoshihiro
Bauer, Peter O.
Oyama, Fumitaka
author_sort Okawa, Kazuaki
collection PubMed
description Acidic mammalian chitinase (AMCase) is implicated in asthma, allergic inflammation, and food processing. Little is known about genetic and evolutional regulation of chitinolytic activity of AMCase. Here, we relate human AMCase polymorphisms to the mouse AMCase, and show that the highly active variants encoded by nonsynonymous single-nucleotide polymorphisms (nsSNPs) are consistent with the mouse AMCase sequence. The chitinolytic activity of the recombinant human AMCase was significantly lower than that of the mouse counterpart. By creating mouse-human chimeric AMCase protein we found that the presence of the N-terminal region of human AMCase containing conserved active site residues reduced the enzymatic activity of the molecule. We were able to significantly increase the activity of human AMCase by amino acid substitutions encoded by nsSNPs (N45, D47, and R61) with those conserved in the mouse homologue (D45, N47, and M61). For abolition of the mouse AMCase activity, introduction of M61R mutation was sufficient. M61 is conserved in most of primates other than human and orangutan as well as in other mammals. Orangutan has I61 substitution, which also markedly reduced the activity of the mouse AMCase, indicating that the M61 is a crucial residue for the chitinolytic activity. Altogether, our data suggest that human AMCase has lost its chitinolytic activity by integration of nsSNPs during evolution and that the enzyme can be reactivated by introducing amino acids conserved in the mouse counterpart.
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spelling pubmed-51000532016-11-10 Loss and Gain of Human Acidic Mammalian Chitinase Activity by Nonsynonymous SNPs Okawa, Kazuaki Ohno, Misa Kashimura, Akinori Kimura, Masahiro Kobayashi, Yuki Sakaguchi, Masayoshi Sugahara, Yasusato Kamaya, Minori Kino, Yoshihiro Bauer, Peter O. Oyama, Fumitaka Mol Biol Evol Discoveries Acidic mammalian chitinase (AMCase) is implicated in asthma, allergic inflammation, and food processing. Little is known about genetic and evolutional regulation of chitinolytic activity of AMCase. Here, we relate human AMCase polymorphisms to the mouse AMCase, and show that the highly active variants encoded by nonsynonymous single-nucleotide polymorphisms (nsSNPs) are consistent with the mouse AMCase sequence. The chitinolytic activity of the recombinant human AMCase was significantly lower than that of the mouse counterpart. By creating mouse-human chimeric AMCase protein we found that the presence of the N-terminal region of human AMCase containing conserved active site residues reduced the enzymatic activity of the molecule. We were able to significantly increase the activity of human AMCase by amino acid substitutions encoded by nsSNPs (N45, D47, and R61) with those conserved in the mouse homologue (D45, N47, and M61). For abolition of the mouse AMCase activity, introduction of M61R mutation was sufficient. M61 is conserved in most of primates other than human and orangutan as well as in other mammals. Orangutan has I61 substitution, which also markedly reduced the activity of the mouse AMCase, indicating that the M61 is a crucial residue for the chitinolytic activity. Altogether, our data suggest that human AMCase has lost its chitinolytic activity by integration of nsSNPs during evolution and that the enzyme can be reactivated by introducing amino acids conserved in the mouse counterpart. Oxford University Press 2016-12 2016-10-04 /pmc/articles/PMC5100053/ /pubmed/27702777 http://dx.doi.org/10.1093/molbev/msw198 Text en © The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Okawa, Kazuaki
Ohno, Misa
Kashimura, Akinori
Kimura, Masahiro
Kobayashi, Yuki
Sakaguchi, Masayoshi
Sugahara, Yasusato
Kamaya, Minori
Kino, Yoshihiro
Bauer, Peter O.
Oyama, Fumitaka
Loss and Gain of Human Acidic Mammalian Chitinase Activity by Nonsynonymous SNPs
title Loss and Gain of Human Acidic Mammalian Chitinase Activity by Nonsynonymous SNPs
title_full Loss and Gain of Human Acidic Mammalian Chitinase Activity by Nonsynonymous SNPs
title_fullStr Loss and Gain of Human Acidic Mammalian Chitinase Activity by Nonsynonymous SNPs
title_full_unstemmed Loss and Gain of Human Acidic Mammalian Chitinase Activity by Nonsynonymous SNPs
title_short Loss and Gain of Human Acidic Mammalian Chitinase Activity by Nonsynonymous SNPs
title_sort loss and gain of human acidic mammalian chitinase activity by nonsynonymous snps
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100053/
https://www.ncbi.nlm.nih.gov/pubmed/27702777
http://dx.doi.org/10.1093/molbev/msw198
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