Evolutionary activation of acidic chitinase in herbivores through the H128R mutation in ruminant livestock
Status PubMed-not-MEDLINE Language English Country United States Media electronic-ecollection
Document type Journal Article
PubMed
37502259
PubMed Central
PMC10368815
DOI
10.1016/j.isci.2023.107254
PII: S2589-0042(23)01331-7
Knihovny.cz E-resources
- Keywords
- Evolutionary biology, Molecular biology, Zoology,
- Publication type
- Journal Article MeSH
Placental mammals' ancestors were insectivores, suggesting that modern mammals may have inherited the ability to digest insects. Acidic chitinase (Chia) is a crucial enzyme hydrolyzing significant component of insects' exoskeleton in many species. On the other hand, herbivorous animal groups, such as cattle, have extremely low chitinase activity compared to omnivorous species, e.g., mice. The low activity of cattle Chia has been attributed to R128H mutation. The presence of either of these amino acids correlates with the feeding behavior of different bovid species with R and H determining the high and low enzymatic activity, respectively. Evolutionary analysis indicated that selective constraints were relaxed in 67 herbivorous Chia in Cetartiodactyla. Despite searching for another Chia paralog that could compensate for the reduced chitinase activity, no active paralogs were found in this order. Herbivorous animals' Chia underwent genetic alterations and evolved into a molecule with low activity due to the chitin-free diet.
Bioinova a s Videnska 1083 142 00 Prague Czech Republic
Department of Chemistry and Life Science Kogakuin University Hachioji Tokyo 192 0015 Japan
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O'Leary M.A., Bloch J.I., Flynn J.J., Gaudin T.J., Giallombardo A., Giannini N.P., Goldberg S.L., Kraatz B.P., Luo Z.X., Meng J., et al. The placental mammal ancestor and the post-K-Pg radiation of placentals. Science. 2013;339:662–667. PubMed
Wysokowski M., Petrenko I., Stelling A., Stawski D., Jesionowski T., Ehrlich H. Poriferan chitin as a versatile template for extreme biomimetics. Polymers. 2015;7:235–265.
Van Dyken S.J., Locksley R.M. Chitins and chitinase activity in airway diseases. J. Allergy Clin. Immunol. 2018;142:364–369. PubMed PMC
Bueter C.L., Specht C.A., Levitz S.M. Innate sensing of chitin and chitosan. PLoS Pathog. 2013;9 PubMed PMC
Koch B.E.V., Stougaard J., Spaink H.P. Keeping track of the growing number of biological functions of chitin and its interaction partners in biomedical research. Glycobiology. 2015;25:469–482. PubMed PMC
Hollak C.E., van Weely S., van Oers M.H., Aerts J.M. Marked elevation of plasma chitotriosidase activity. A novel hallmark of Gaucher disease. J. Clin. Invest. 1994;93:1288–1292. PubMed PMC
Renkema G.H., Boot R.G., Muijsers A.O., Donker-Koopman W.E., Aerts J.M. Purification and characterization of human chitotriosidase, a novel member of the chitinase family of proteins. J. Biol. Chem. 1995;270:2198–2202. PubMed
Boot R.G., Renkema G.H., Strijland A., van Zonneveld A.J., Aerts J.M. Cloning of a cDNA encoding chitotriosidase, a human chitinase produced by macrophages. J. Biol. Chem. 1995;270:26252–26256. PubMed
Boot R.G., Blommaart E.F., Swart E., Ghauharali-van der Vlugt K., Bijl N., Moe C., Place A., Aerts J.M. Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J. Biol. Chem. 2001;276:6770–6778. PubMed
Zhu Z., Zheng T., Homer R.J., Kim Y.K., Chen N.Y., Cohn L., Hamid Q., Elias J.A. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science. 2004;304:1678–1682. PubMed
Reese T.A., Liang H.E., Tager A.M., Luster A.D., Van Rooijen N., Voehringer D., Locksley R.M. Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature. 2007;447:92–96. PubMed PMC
Bucolo C., Musumeci M., Maltese A., Drago F., Musumeci S. Effect of chitinase inhibitors on endotoxin-induced uveitis (EIU) in rabbits. Pharmacol. Res. 2008;57:247–252. PubMed
Musumeci M., Aragona P., Bellin M., Maugeri F., Rania L., Bucolo C., Musumeci S. Acidic mammalian chitinase in dry eye conditions. Cornea. 2009;28:667–672. PubMed
Bucolo C., Musumeci M., Musumeci S., Drago F. Acidic mammalian chitinase and the eye: implications for ocular inflammatory diseases. Front. Pharmacol. 2011;2:43. PubMed PMC
Cozzarini E., Bellin M., Norberto L., Polese L., Musumeci S., Lanfranchi G., Paoletti M.G. CHIT1 and AMCase expression in human gastric mucosa: correlation with inflammation and Helicobacter pylori infection. Eur. J. Gastroenterol. Hepatol. 2009;21:1119–1126. PubMed
Nookaew I., Thorell K., Worah K., Wang S., Hibberd M.L., Sjövall H., Pettersson S., Nielsen J., Lundin S.B. Transcriptome signatures in Helicobacter pylori-infected mucosa identifies acidic mammalian chitinase loss as a corpus atrophy marker. BMC Med. Genom. 2013;6:41. PubMed PMC
Bierbaum S., Nickel R., Koch A., Lau S., Deichmann K.A., Wahn U., Superti-Furga A., Heinzmann A. Polymorphisms and haplotypes of acid mammalian chitinase are associated with bronchial asthma. Am. J. Respir. Crit. Care Med. 2005;172:1505–1509. PubMed PMC
Seibold M.A., Reese T.A., Choudhry S., Salam M.T., Beckman K., Eng C., Atakilit A., Meade K., Lenoir M., Watson H.G., et al. Differential enzymatic activity of common haplotypic versions of the human acidic mammalian chitinase protein. J. Biol. Chem. 2009;284:19650–19658. PubMed PMC
Okawa K., Ohno M., Kashimura A., Kimura M., Kobayashi Y., Sakaguchi M., Sugahara Y., Kamaya M., Kino Y., Bauer P.O., Oyama F. Loss and gain of human acidic mammalian chitinase activity by nonsynonymous SNPs. Mol. Biol. Evol. 2016;33:3183–3193. PubMed PMC
Fitz L.J., DeClercq C., Brooks J., Kuang W., Bates B., Demers D., Winkler A., Nocka K., Jiao A., Greco R.M., et al. Acidic mammalian chitinase is not a critical target for allergic airway disease. Am. J. Respir. Cell Mol. Biol. 2012;46:71–79. PubMed
Van Dyken S.J., Liang H.E., Naikawadi R.P., Woodruff P.G., Wolters P.J., Erle D.J., Locksley R.M. Spontaneous chitin accumulation in airways and age-related fibrotic lung disease. Cell. 2017;169:497–509.e13. PubMed PMC
Strobel S., Roswag A., Becker N.I., Trenczek T.E., Encarnação J.A. Insectivorous bats digest chitin in the stomach using acidic mammalian chitinase. PLoS One. 2013;8 PubMed PMC
Ohno M., Kimura M., Miyazaki H., Okawa K., Onuki R., Nemoto C., Tabata E., Wakita S., Kashimura A., Sakaguchi M., et al. Acidic mammalian chitinase is a proteases-resistant glycosidase in mouse digestive system. Sci. Rep. 2016;6 PubMed PMC
Tabata E., Kashimura A., Wakita S., Ohno M., Sakaguchi M., Sugahara Y., Kino Y., Matoska V., Bauer P.O., Oyama F. Gastric and intestinal proteases resistance of chicken acidic chitinase nominates chitin-containing organisms for alternative whole edible diets for poultry. Sci. Rep. 2017;7:6662. PubMed PMC
Tabata E., Kashimura A., Wakita S., Ohno M., Sakaguchi M., Sugahara Y., Imamura Y., Seki S., Ueda H., Matoska V., et al. Protease resistance of porcine acidic mammalian chitinase under gastrointestinal conditions implies that chitin-containing organisms can be sustainable dietary resources. Sci. Rep. 2017;7 PubMed PMC
Ma J.E., Li L.M., Jiang H.Y., Zhang X.J., Li J., Li G.Y., Yuan L.H., Wu J., Chen J.P. Transcriptomic analysis identifies genes and pathways related to myrmecophagy in the Malayan pangolin (Manis javanica) PeerJ. 2017;5 PubMed PMC
Ma J.E., Li L.M., Jiang H.Y., Zhang X.J., Li J., Li G.Y., Chen J.P. Acidic mammalian chitinase gene is highly expressed in the special oxyntic glands of Manis javanica. FEBS Open Bio. 2018;8:1247–1255. PubMed PMC
Shao-Chen Cheng C.-B.L., Yao X.-Q., Hu J.-Y., Yin T.-T., Lim B.K., Chen W., Wang G.-D., Zhang C.-L., Irwin D.M., Zhang Z.-G., et al. Hologenomic insights into mammalian adaptations to myrmecophagy. Natl. Sci. Rev. 2022;nwac174 doi: 10.1093/nsr/nwac174. PubMed DOI PMC
Zhang F., Xu N., Yu Y., Wu S., Li S., Wang W. Expression profile of the digestive enzymes of Manis javanica reveals its adaptation to diet specialization. ACS Omega. 2019;4:19925–19933. PubMed PMC
Uehara M., Tabata E., Okuda M., Maruyama Y., Matoska V., Bauer P.O., Oyama F. Robust chitinolytic activity of crab-eating monkey (Macaca fascicularis) acidic chitinase under a broad pH and temperature range. Sci. Rep. 2021;11 PubMed PMC
Tabata E., Kashimura A., Uehara M., Wakita S., Sakaguchi M., Sugahara Y., Yurimoto T., Sasaki E., Matoska V., Bauer P.O., Oyama F. High expression of acidic chitinase and chitin digestibility in the stomach of common marmoset (Callithrix jacchus), an insectivorous nonhuman primate. Sci. Rep. 2019;9:159. PubMed PMC
Tabata E., Kashimura A., Kikuchi A., Masuda H., Miyahara R., Hiruma Y., Wakita S., Ohno M., Sakaguchi M., Sugahara Y., et al. Chitin digestibility is dependent on feeding behaviors, which determine acidic chitinase mRNA levels in mammalian and poultry stomachs. Sci. Rep. 2018;8:1461. PubMed PMC
Emerling C.A., Delsuc F., Nachman M.W. Chitinase genes (CHIAs) provide genomic footprints of a post-Cretaceous dietary radiation in placental mammals. Sci. Adv. 2018;4 PubMed PMC
Janiak M.C., Chaney M.E., Tosi A.J. Evolution of acidic mammalian chitinase genes (CHIA) is related to body mass and insectivory in primates. Mol. Biol. Evol. 2018;35:607–622. PubMed
Tabata E., Itoigawa A., Koinuma T., Tayama H., Kashimura A., Sakaguchi M., Matoska V., Bauer P.O., Oyama F. Noninsect-based diet leads to structural and functional changes of acidic chitinase in Carnivora. Mol. Biol. Evol. 2022;39 PubMed PMC
Bovine Genome Sequencing and Analysis Consortium, Elsik C.G., Tellam R.L., Worley K.C., Gibbs R.A., Muzny D.M., Weinstock G.M., Adelson D.L., Eichler E.E., Guigó R., et al. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science. 2009;324:522–528. PubMed PMC
Jiang Y., Xie M., Chen W., Talbot R., Maddox J.F., Faraut T., Wu C., Muzny D.M., Li Y., Zhang W., et al. The sheep genome illuminates biology of the rumen and lipid metabolism. Science. 2014;344:1168–1173. PubMed PMC
Dong Y., Xie M., Jiang Y., Xiao N., Du X., Zhang W., Tosser-Klopp G., Wang J., Yang S., Liang J., et al. Sequencing and automated whole-genome optical mapping of the genome of a domestic goat (Capra hircus) Nat. Biotechnol. 2013;31:135–141. PubMed
Jumper J., Evans R., Pritzel A., Green T., Figurnov M., Ronneberger O., Tunyasuvunakool K., Bates R., Žídek A., Potapenko A., et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596:583–589. PubMed PMC
Tunyasuvunakool K., Adler J., Wu Z., Green T., Zielinski M., Žídek A., Bridgland A., Cowie A., Meyer C., Laydon A., et al. Highly accurate protein structure prediction for the human proteome. Nature. 2021;596:590–596. PubMed PMC
Li H., Robertson A.D., Jensen J.H. Very fast empirical prediction and rationalization of protein pKa values. Proteins. 2005;61:704–721. PubMed
Heller R., Frandsen P., Lorenzen E.D., Siegismund H.R. Are there really twice as many bovid species as we thought? Syst. Biol. 2013;62:490–493. PubMed
Hofmann R.R., Stewart D.R.M. Grazer or browser:a classification based on the stomach structure andfeeding habits of East African ruminants. Mammalia. 1972;36:226–240.
Cantalapiedra J.L., Fitzjohn R.G., Kuhn T.S., Fernández M.H., Demiguel D., Azanza B., Morales J., Mooers A.Ø. Dietary innovations spurred the diversification of ruminants during the Caenozoic. Proc. Biol. Sci. 2014;281 PubMed PMC
Yang Z. Paml 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 2007;24:1586–1591. PubMed
Wertheim J.O., Murrell B., Smith M.D., Kosakovsky Pond S.L., Scheffler K. RELAX: Detecting relaxed selection in a phylogenetic framework. Mol. Biol. Evol. 2015;32:820–832. PubMed PMC
Chen L., Qiu Q., Jiang Y., Wang K., Lin Z., Li Z., Bibi F., Yang Y., Wang J., Nie W., et al. Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits. Science. 2019;364 PubMed
Barad B.A., Liu L., Diaz R.E., Basilio R., Van Dyken S.J., Locksley R.M., Fraser J.S. Differences in the chitinolytic activity of mammalian chitinases on soluble and insoluble substrates. Protein Sci. 2020;29:966–977. PubMed PMC
Kumar S., Stecher G., Li M., Knyaz C., Tamura K. Mega X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018;35:1547–1549. PubMed PMC
Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. PubMed PMC
Kumar S., Stecher G., Suleski M., Hedges S.B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 2017;34:1812–1819. PubMed
Hyperactivation of human acidic chitinase (Chia) for potential medical use