Chitin digestibility is dependent on feeding behaviors, which determine acidic chitinase mRNA levels in mammalian and poultry stomachs
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29362395
PubMed Central
PMC5780506
DOI
10.1038/s41598-018-19940-8
PII: 10.1038/s41598-018-19940-8
Knihovny.cz E-zdroje
- MeSH
- chitin chemie MeSH
- chitinasy genetika metabolismus MeSH
- druhová specificita MeSH
- kur domácí MeSH
- messenger RNA genetika MeSH
- morčata MeSH
- psi MeSH
- regulace genové exprese MeSH
- skot MeSH
- stravovací zvyklosti MeSH
- žaludek chemie enzymologie MeSH
- zvířata MeSH
- Check Tag
- morčata MeSH
- psi MeSH
- skot MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- chitin MeSH
- chitinasy MeSH
- messenger RNA MeSH
Chitin, a polymer of N-acetyl-D-glucosamine (GlcNAc), functions as a major structural component in chitin-containing organism including crustaceans, insects and fungi. Recently, we reported that acidic chitinase (Chia) is highly expressed in mouse, chicken and pig stomach tissues and that it can digest chitin in the respective gastrointestinal tracts (GIT). In this study, we focus on major livestock and domestic animals and show that the levels of Chia mRNA in their stomach tissues are governed by the feeding behavior. Chia mRNA levels were significantly lower in the bovine (herbivores) and dog (carnivores) stomach than those in mouse, pig and chicken (omnivores). Consistent with the mRNA levels, Chia protein was very low in bovine stomach. In addition, the chitinolytic activity of E. coli-expressed bovine and dog Chia enzymes were moderately but significantly lower compared with those of the omnivorous Chia enzymes. Recombinant bovine and dog Chia enzymes can degrade chitin substrates under the artificial GIT conditions. Furthermore, genomes of some herbivorous animals such as rabbit and guinea pig do not contain functional Chia genes. These results indicate that feeding behavior affects Chia expression levels as well as chitinolytic activity of the enzyme, and determines chitin digestibility in the particular animals.
Bioinova Ltd Videnska 1083 Prague 142 20 Czech Republic
Department of Chemistry and Life Science Kogakuin University Hachioji Tokyo 192 0015 Japan
Zobrazit více v PubMed
Wysokowski M, et al. Poriferan chitin as a versatile template for extreme biomimetics. Polymers. 2015;7:235–265. doi: 10.3390/polym7020235. DOI
Neville AC, Parry DA, Woodhead-Galloway J. The chitin crystallite in arthropod cuticle. J. Cell Sci. 1976;21:73–82. PubMed
Liu S, et al. Extraction and characterization of chitin from the beetle Holotrichia parallela Motschulsky. Molecules. 2012;17:4604–4611. doi: 10.3390/molecules17044604. PubMed DOI PMC
Merzendorfer H. Insect chitin synthases: a review. J. Comp. Physiol. B. 2006;176:1–15. doi: 10.1007/s00360-005-0005-3. PubMed DOI
Kaya M, Seyyar O, Baran T, Erdogan S, Kar M. A physicochemical characterization of fully acetylated chitin structure isolated from two spider species: with new surface morphology. Int. J. Biol. Macromol. 2014;65:553–558. doi: 10.1016/j.ijbiomac.2014.02.010. PubMed DOI
Garcia Mendoza C, Novaes Ledieu M. Chitin in the new wall of regenerating protoplasts of Candida utilis. Nature. 1968;220:1035. doi: 10.1038/2201035a0. PubMed DOI
Blumenthal HJ, Roseman S. Quantitative estimation of chitin in fungi. J. Bacteriol. 1957;74:222–224. PubMed PMC
Elorza MV, Rico H, Sentandreu R. Calcofluor white alters the assembly of chitin fibrils in Saccharomyces cerevisiae and Candida albicans cells. J. Gen. Microbiol. 1983;129:1577–1582. PubMed
Muzzarelli RAA, et al. Current views on fungal chitin/chitosan, human chitinases, food preservation, glucans, pectins and inulin: A tribute to Henri Braconnot, precursor of the carbohydrate polymers science, on the chitin bicentennial. Carbohydr. Polym. 2012;87:995–1012. doi: 10.1016/j.carbpol.2011.09.063. DOI
Das S, Gillin FD. Chitin synthase in encysting Entamoeba invadens. Biochem. J. 1991;280(Pt 3):641–647. doi: 10.1042/bj2800641. PubMed DOI PMC
Campos-Gongora E, Ebert F, Willhoeft U, Said-Fernandez S, Tannich E. Characterization of chitin synthases from Entamoeba. Protist. 2004;155:323–330. doi: 10.1078/1434461041844204. PubMed DOI
Richards AG. Studies on Arthropod Cuticle. III. The Chitin of Limulus. Science. 1949;109:591–592. doi: 10.1126/science.109.2841.591. PubMed DOI
Giraud-Guille MM. Fine structure of the chitin-protein system in the crab cuticle. Tissue Cell. 1984;16:75–92. doi: 10.1016/0040-8166(84)90020-X. PubMed DOI
Ando Y, Fukada E, Glimicher MJ. Piezoelectricity of chitin in lobster shell and apodeme. Biorheology. 1977;14:175–179. doi: 10.3233/BIR-1977-14404. PubMed DOI
Horst MN. The biosynthesis of crustacean chitin by a microsomal enzyme from larval brine shrimp. J. Biol. Chem. 1981;256:1412–1419. PubMed
Rodde R, Einbu A, Vårum KM. A seasonal study of the chemical composition and chitin quality of shrimp shells obtained from northern shrimp (Pandalus borealis) Carbohydr. Polym. 2008;71:388–393. doi: 10.1016/j.carbpol.2007.06.006. DOI
Bo M, et al. Isolation and identification of chitin in the black coral Parantipathes larix (Anthozoa: Cnidaria) Int. J. Biol. Macromol. 2012;51:129–137. doi: 10.1016/j.ijbiomac.2012.04.016. PubMed DOI
Weiss IM, Schonitzer V. The distribution of chitin in larval shells of the bivalve mollusk Mytilus galloprovincialis. J. Struct. Biol. 2006;153:264–277. doi: 10.1016/j.jsb.2005.11.006. PubMed DOI
Weiss IM, Schonitzer V, Eichner N, Sumper M. The chitin synthase involved in marine bivalve mollusk shell formation contains a myosin domain. FEBS Lett. 2006;580:1846–1852. doi: 10.1016/j.febslet.2006.02.044. PubMed DOI
Gaill F, Shillito B, Lechaire JP, Chanzy H, Goffinet G. The chitin secreting system from deep sea hydrothermal vent worms. Biol. Cell. 1992;76:201–204. doi: 10.1016/0248-4900(92)90213-K. DOI
Durkin CA, Mock T, Armbrust EV. Chitin in diatoms and its association with the cell wall. Eukaryot Cell. 2009;8:1038–1050. doi: 10.1128/EC.00079-09. PubMed DOI PMC
Brunner E, et al. Chitin-based organic networks: An integral part of cell wall biosilica in the diatom Thalassiosira Pseudonana. Angew. Chem. Int. Ed. 2009;48:9724–9727. doi: 10.1002/anie.200905028. PubMed DOI
Ehrlich H, et al. First evidence of the presence of chitin in skeletons of marine sponges. Part II. Glass sponges (Hexactinellida: Porifera) J. Exp. Zool. B Mol. Dev. Evol. 2007;308:473–483. doi: 10.1002/jez.b.21174. PubMed DOI
Ehrlich H, et al. Identification and first insights into the structure and biosynthesis of chitin from the freshwater sponge Spongilla lacustris. J. Struct. Biol. 2013;183:474–483. doi: 10.1016/j.jsb.2013.06.015. PubMed DOI
Wysokowski M, et al. Isolation and identification of chitin in three-dimensional skeleton of Aplysina fistularis marine sponge. Int. J. Biol. Macromol. 2013;62:94–100. doi: 10.1016/j.ijbiomac.2013.08.039. PubMed DOI
Calström D. The crystal structure of α-chitin (poly-N-acetyl-D-glucosamine) J. Biophys. Biochem. Cytol. 1957;3:669–683. doi: 10.1083/jcb.3.5.669. PubMed DOI PMC
Sikorski P, Hori R, Wada M. Revisit of alpha-chitin crystal structure using high resolution X-ray diffraction data. Biomacromolecules. 2009;10:1100–1105. doi: 10.1021/bm801251e. PubMed DOI
Minke R, Blackwell J. The structure of alpha-chitin. J. Mol. Biol. 1978;120:167–181. doi: 10.1016/0022-2836(78)90063-3. PubMed DOI
Rudall K, Kenchington W. The chitin system. Biol. Rev. 1973;49:597–636. doi: 10.1111/j.1469-185X.1973.tb01570.x. DOI
Kaya M, et al. On chemistry of gamma-chitin. Carbohydr Polym. 2017;176:177–186. doi: 10.1016/j.carbpol.2017.08.076. PubMed DOI
Herrero M, Thornton PK. Livestock and global change: emerging issues for sustainable food systems. Proc. Natl. Acad. Sci. USA. 2013;110:20878–20881. doi: 10.1073/pnas.1321844111. PubMed DOI PMC
Kupferschmidt K. Buzz food. Science. 2015;350:267–269. doi: 10.1126/science.350.6258.267. PubMed DOI
van Huis A. Edible insects are the future? Proc. Nutr. Soc. 2016;75:294–305. doi: 10.1017/S0029665116000069. PubMed DOI
Lee CG, et al. Role of chitin and chitinase/chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu. Rev. Physiol. 2011;73:479–501. doi: 10.1146/annurev-physiol-012110-142250. PubMed DOI PMC
Koch BE, Stougaard J, Spaink HP. Keeping track of the growing number of biological functions of chitin and its interaction partners in biomedical research. Glycobiology. 2015;25:469–482. doi: 10.1093/glycob/cwv005. PubMed DOI PMC
Bueter CL, Specht CA, Levitz SM. Innate sensing of chitin and chitosan. PLoS Pathog. 2013;9:e1003080. doi: 10.1371/journal.ppat.1003080. PubMed DOI PMC
Bussink AP, Speijer D, Aerts JM, Boot RG. Evolution of mammalian chitinase(-like) members of family 18 glycosyl hydrolases. Genetics. 2007;177:959–970. doi: 10.1534/genetics.107.075846. PubMed DOI PMC
Hollak CE, van Weely S, van Oers MH, Aerts JM. Marked elevation of plasma chitotriosidase activity. A novel hallmark of Gaucher disease. J. Clin. Invest. 1994;93:1288–1292. doi: 10.1172/JCI117084. PubMed DOI PMC
Letuve S, et al. Lung chitinolytic activity and chitotriosidase are elevated in chronic obstructive pulmonary disease and contribute to lung inflammation. Am. J. Pathol. 2010;176:638–649. doi: 10.2353/ajpath.2010.090455. PubMed DOI PMC
Watabe-Rudolph M, et al. Chitinase enzyme activity in CSF is a powerful biomarker of Alzheimer disease. Neurology. 2012;78:569–577. doi: 10.1212/WNL.0b013e318247caa1. PubMed DOI
Artieda M, et al. Serum chitotriosidase activity is increased in subjects with atherosclerosis disease. Arterioscler. Thromb. Vasc. Biol. 2003;23:1645–1652. doi: 10.1161/01.ATV.0000089329.09061.07. PubMed DOI
Sonmez A, et al. Chitotriosidase activity predicts endothelial dysfunction in type-2 diabetes mellitus. Endocrine. 2010;37:455–459. doi: 10.1007/s12020-010-9334-4. PubMed DOI
Livnat G, et al. Duplication in CHIT1 gene and the risk for Aspergillus lung disease in CF patients. Pediatr. Pulmonol. 2014;49:21–27. doi: 10.1002/ppul.22749. PubMed DOI
Seibold MA, et al. Chitotriosidase is the primary active chitinase in the human lung and is modulated by genotype and smoking habit. J. Allergy Clin. Immunol. 2008;122:944–950 e943. doi: 10.1016/j.jaci.2008.08.023. PubMed DOI PMC
Zhu Z, et al. Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science. 2004;304:1678–1682. doi: 10.1126/science.1095336. PubMed DOI
Reese TA, et al. Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature. 2007;447:92–96. doi: 10.1038/nature05746. PubMed DOI PMC
Bierbaum S, et al. Polymorphisms and haplotypes of acid mammalian chitinase are associated with bronchial asthma. Am. J. Respir. Crit. Care Med. 2005;172:1505–1509. doi: 10.1164/rccm.200506-890OC. PubMed DOI PMC
Seibold MA, et al. Differential enzymatic activity of common haplotypic versions of the human acidic mammalian chitinase protein. J. Biol. Chem. 2009;284:19650–19658. doi: 10.1074/jbc.M109.012443. PubMed DOI PMC
Okawa K, et al. Loss and gain of human acidic mammalian chitinase activity by nonsynonymous SNPs. Mol. Biol. Evol. 2016;33:3183–3193. doi: 10.1093/molbev/msw198. PubMed DOI PMC
Ohno M, et al. Acidic mammalian chitinase is a proteases-resistant glycosidase in mouse digestive system. Sci. Rep. 2016;6:37756. doi: 10.1038/srep37756. PubMed DOI PMC
Tabata E, et al. 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. doi: 10.1038/s41598-017-07146-3. PubMed DOI PMC
Tabata E, 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;7:12963. doi: 10.1038/s41598-017-13526-6. PubMed DOI PMC
Ohno M, Tsuda K, Sakaguchi M, Sugahara Y, Oyama F. Chitinase mRNA levels by quantitative PCR using the single standard DNA: acidic mammalian chitinase is a major transcript in the mouse stomach. PLoS One. 2012;7:e50381. doi: 10.1371/journal.pone.0050381. PubMed DOI PMC
Ohno M, et al. Quantification of chitinase mRNA levels in human and mouse tissues by real-time PCR: species-specific expression of acidic mammalian chitinase in stomach tissues. PLoS One. 2013;8:e67399. doi: 10.1371/journal.pone.0067399. PubMed DOI PMC
Kageyama T. Pepsinogens, progastricsins, and prochymosins: structure, function, evolution, and development. Cell. Mol. Life Sci. 2002;59:288–306. doi: 10.1007/s00018-002-8423-9. PubMed DOI PMC
Zainuddin A, Chua KH, Abdul Rahim N, Makpol S. Effect of experimental treatment on GAPDH mRNA expression as a housekeeping gene in human diploid fibroblasts. BMC Mol. Biol. 2010;11:59. doi: 10.1186/1471-2199-11-59. PubMed DOI PMC
Suzuki M, Morimatsu M, Yamashita T, Iwanaga T, Syuto B. A novel serum chitinase that is expressed in bovine liver. FEBS Lett. 2001;506:127–130. doi: 10.1016/S0014-5793(01)02893-9. PubMed DOI
Kouadjo KE, Nishida Y, Cadrin-Girard JF, Yoshioka M, St-Amand J. Housekeeping and tissue-specific genes in mouse tissues. BMC Genomics. 2007;8:127. doi: 10.1186/1471-2164-8-127. PubMed DOI PMC
Dabek J, Wilczok J, Kulach A, Gasior Z. Altered transcriptional activity of gene encoding GAPDH in peripheral blood mononuclear cells from patients with cardiac syndrome X - an important part in pathology of microvascular angina? Arch. Med. Sci. 2010;6:709–712. doi: 10.5114/aoms.2010.17085. PubMed DOI PMC
Kashimura A, et al. Protein A-mouse acidic mammalian chitinase-V5-His expressed in periplasmic space of Escherichia coli possesses chitinase functions comparable to CHO-expressed protein. PLoS One. 2013;8:e78669. doi: 10.1371/journal.pone.0078669. PubMed DOI PMC
Boot RG, et al. Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J. Biol. Chem. 2001;276:6770–6778. doi: 10.1074/jbc.M009886200. PubMed DOI
Hibino S, et al. Reduced expression of DENND2D through promoter hypermethylation is an adverse prognostic factor in squamous cell carcinoma of the esophagus. Oncol. Rep. 2014;31:693–700. doi: 10.3892/or.2013.2901. PubMed DOI
Sakha S, Muramatsu T, Ueda K, Inazawa J. Exosomal microRNA miR-1246 induces cell motility and invasion through the regulation of DENND2D in oral squamous cell carcinoma. Sci. Rep. 2016;6:38750. doi: 10.1038/srep38750. PubMed DOI PMC
Kinzel D, et al. Pitchfork regulates primary cilia disassembly and left-right asymmetry. Dev. Cell. 2010;19:66–77. doi: 10.1016/j.devcel.2010.06.005. PubMed DOI PMC
Richter C, Tanaka T, Yada RY. Mechanism of activation of the gastric aspartic proteinases: pepsinogen, progastricsin and prochymosin. Biochem. J. 1998;335(Pt 3):481–490. doi: 10.1042/bj3350481. PubMed DOI PMC
Gerstein M, Zheng D. The real life of pseudogenes. Sci. Am. 2006;295:48–55. doi: 10.1038/scientificamerican0806-48. PubMed DOI
Dobson DE, Prager EM, Wilson AC. Stomach lysozymes of ruminants. I. Distribution and catalytic properties. J. Biol. Chem. 1984;259:11607–11616. PubMed
Zhao H, Yang JR, Xu H, Zhang J. Pseudogenization of the umami taste receptor gene Tas1r1 in the giant panda coincided with its dietary switch to bamboo. Mol. Biol. Evol. 2010;27:2669–2673. doi: 10.1093/molbev/msq153. PubMed DOI PMC
Birben E, et al. The effects of an insertion in the 5′UTR of the AMCase on gene expression and pulmonary functions. Respir. Med. 2011;105:1160–1169. doi: 10.1016/j.rmed.2011.03.017. PubMed DOI
Latunde-Dada GO, Yang W, Vera Aviles M. In vitro iron availability from insects and sirloin beef. J. Agric. Food Chem. 2016;64:8420–8424. doi: 10.1021/acs.jafc.6b03286. PubMed DOI
Oonincx DG, de Boer IJ. Environmental impact of the production of mealworms as a protein source for humans - a life cycle assessment. PLoS One. 2012;7:e51145. doi: 10.1371/journal.pone.0051145. PubMed DOI PMC
Van Huis A, et al. Edible insects: future prospects for food and feed security. FAO Forestry Paper. 2013;171:1–201.
Bays HE, et al. Chitin-glucan fiber effects on oxidized low-density lipoprotein: a randomized controlled trial. Eur. J. Clin. Nutr. 2013;67:2–7. doi: 10.1038/ejcn.2012.121. PubMed DOI PMC
Gernat AG. The effect of using different levels of shrimp meal in laying hen diets. Poult. Sci. 2001;80:633–636. doi: 10.1093/ps/80.5.633. PubMed DOI
Jin XH, Heo PS, Hong JS, Kim NJ, Kim YY. Supplementation of dried mealworm (Tenebrio molitor larva) on growth performance, nutrient digestibility and blood profiles in weaning pigs. Asian-Australas J Anim Sci. 2016;29:979–986. doi: 10.5713/ajas.15.0535. PubMed DOI PMC
Strobel S, Roswag A, Becker NI, Trenczek TE, Encarnacao JA. Insectivorous bats digest chitin in the stomach using acidic mammalian chitinase. PLoS One. 2013;8:e72770. doi: 10.1371/journal.pone.0072770. PubMed DOI 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., in press (2017). PubMed
Van Huis A. Potential of insects as food and feed in assuring food security. Annu. Rev. Entomol. 2013;58:563–583. doi: 10.1146/annurev-ento-120811-153704. PubMed DOI
Veldkamp T, Bosch G. Insects: a protein-rich feed ingredient in pig and poultry diets. Animal Frontiers. 2015;5:45–50.
Brulc JM, et al. Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc. Natl. Acad. Sci. USA. 2009;106:1948–1953. doi: 10.1073/pnas.0806191105. PubMed DOI PMC
Hess M, et al. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science. 2011;331:463–467. doi: 10.1126/science.1200387. PubMed DOI
Deusch S, et al. A structural and functional elucidation of the rumen microbiome influenced by various diets and microenvironments. Front. Microbiol. 2017;8:1605. doi: 10.3389/fmicb.2017.01605. PubMed DOI PMC
Manninen TJ, Rinkinen ML, Beasley SS, Saris PE. Alteration of the canine small-intestinal lactic acid bacterium microbiota by feeding of potential probiotics. Appl. Environ. Microbiol. 2006;72:6539–6543. doi: 10.1128/AEM.02977-05. PubMed DOI PMC
Uyeno Y, Shigemori S, Shimosato T. Effect of probiotics/prebiotics on cattle health and productivity. Microbes Environ. 2015;30:126–132. doi: 10.1264/jsme2.ME14176. PubMed DOI PMC
Hyperactivation of human acidic chitinase (Chia) for potential medical use
Noninsect-Based Diet Leads to Structural and Functional Changes of Acidic Chitinase in Carnivora