Gastric and intestinal proteases resistance of chicken acidic chitinase nominates chitin-containing organisms for alternative whole edible diets for poultry
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
28751762
PubMed Central
PMC5532213
DOI
10.1038/s41598-017-07146-3
PII: 10.1038/s41598-017-07146-3
Knihovny.cz E-zdroje
- MeSH
- chitin metabolismus MeSH
- chitinasy metabolismus MeSH
- koncentrace vodíkových iontů MeSH
- kur domácí metabolismus MeSH
- proteasy MeSH
- střeva enzymologie MeSH
- Tenebrio chemie MeSH
- trávení * MeSH
- žaludek enzymologie MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- chitin MeSH
- chitinasy MeSH
- proteasy MeSH
Chitin, a polymer of N-acetyl-D-glucosamine (GlcNAc), functions as a major structural component in crustaceans, insects and fungi and is the second most abundant polysaccharide in the nature. Although these chitin-containing organisms have been suggested as novel animal feed resources, chitin has long been considered as indigestible fibers in the animal body. Recently, we reported that acidic chitinase (Chia) is a protease-resistant major glycosidase in mouse gastrointestinal tract (GIT) and that it digests chitin in the mouse stomach. However, the physiological role of Chia in other animals including poultry remains unknown. Here, we report that Chia can function as a digestive enzyme that breaks down chitin-containing organisms in chicken GIT. Chia mRNA is predominantly expressed in the glandular stomach tissue in normal chicken. We also show that chicken Chia has a robust chitinolytic activity at pH 2.0 and is highly resistant to proteolysis by pepsin and trypsin/chymotrypsin under conditions mimicking GIT. Chia degraded shells of mealworm larvae in the presence of digestive proteases and produced (GlcNAc)2. Thus, functional similarity of chicken Chia with the mouse enzyme suggests that chitin-containing organisms can be used for alternative poultry diets not only as whole edible resources but also as enhancers of their nutritional value.
Bioinova Ltd Videnska 1083 Prague 142 20 Czech Republic
Department of Chemistry and Life Science Kogakuin University Hachioji Tokyo 192 0015 Japan
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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. 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
Khoushab F, Yamabhai M. Chitin research revisited. Mar. Drugs. 2010;8:1988–2012. doi: 10.3390/md8071988. 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
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
Veldkamp T, Bosch G. Insects: a protein-rich feed ingredient in pig and poultry diets. Animal Frontiers. 2015;5:45–50.
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
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
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
Renkema GH, Boot RG, Muijsers AO, Donker-Koopman WE, Aerts JM. Purification and characterization of human chitotriosidase, a novel member of the chitinase family of proteins. J. Biol. Chem. 1995;270:2198–2202. doi: 10.1074/jbc.270.5.2198. PubMed DOI
Boot RG, Renkema GH, Strijland A, van Zonneveld AJ, Aerts JM. Cloning of a cDNA encoding chitotriosidase, a human chitinase produced by macrophages. J. Biol. Chem. 1995;270:26252–26256. doi: 10.1074/jbc.270.44.26252. PubMed DOI
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
Boot RG, et al. Marked differences in tissue-specific expression of chitinases in mouse and man. J. Histochem. Cytochem. 2005;53:1283–1292. doi: 10.1369/jhc.4A6547.2005. PubMed DOI
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
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. doi: 10.1016/j.phrs.2008.02.002. PubMed DOI
Musumeci M, et al. Acidic mammalian chitinase in dry eye conditions. Cornea. 2009;28:667–672. doi: 10.1097/ICO.0b013e31819bc308. PubMed DOI
Bucolo C, Musumeci M, Musumeci S, Drago F. Acidic mammalian chitinase and the eye: implications for ocular inflammatory diseases. Front. Pharmacol. 2011;2:43. doi: 10.3389/fphar.2011.00043. PubMed DOI PMC
Cozzarini E, et al. CHIT1 and AMCase expression in human gastric mucosa: correlation with inflammation and Helicobacter pylori infection. Eur. J. Gastroenterol. Hepatol. 2009;21:1119–1126. doi: 10.1097/MEG.0b013e328329742a. PubMed DOI
Nookaew I, et al. Transcriptome signatures in Helicobacter pylori-infected mucosa identifies acidic mammalian chitinase loss as a corpus atrophy marker. BMC Med. Genomics. 2013;6:41. doi: 10.1186/1755-8794-6-41. 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
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
Chatterjee, R., Batra, J., Das, S., Sharma, S. K. & Ghosh, B. Genetic association of acidic mammalian chitinase with atopic asthma and serum total IgE levels. J. Allergy Clin. Immunol. 122, 202–208, 208 e201–207 (2008). PubMed
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
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
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
Kashimura A, et al. Functional properties of the catalytic domain of mouse acidic mammalian chitinase expressed in Escherichia coli. Int. J. Mol. Sci. 2015;16:4028–4042. doi: 10.3390/ijms16024028. 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
Crevieu-Gabriel I, Gomez J, Caffin JP, Carre B. Comparison of pig and chicken pepsins for protein hydrolysis. Reprod. Nutr. Dev. 1999;39:443–454. doi: 10.1051/rnd:19990404. PubMed DOI
Canfield VA, Levenson R. Structural organization and transcription of the mouse gastric H+, K+-ATPase beta subunit gene. Proc. Natl. Acad. Sci. USA. 1991;88:8247–8251. doi: 10.1073/pnas.88.18.8247. PubMed DOI PMC
Nygard AB, Jorgensen CB, Cirera S, Fredholm M. Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol. Biol. 2007;8:67. doi: 10.1186/1471-2199-8-67. PubMed DOI PMC
Suzuki M, et al. Cellular expression of gut chitinase mRNA in the gastrointestinal tract of mice and chickens. J. Histochem. Cytochem. 2002;50:1081–1089. doi: 10.1177/002215540205000810. PubMed DOI
Jackson P. The use of polyacrylamide-gel electrophoresis for the high-resolution separation of reducing saccharides labelled with the fluorophore 8-aminonaphthalene-1,3,6-trisulphonic acid. Detection of picomolar quantities by an imaging system based on a cooled charge-coupled device. Biochem. J. 1990;270:705–713. doi: 10.1042/bj2700705. PubMed DOI PMC
Wakita S, et al. Improved fluorescent labeling of chitin oligomers: chitinolytic properties of acidic mammalian chitinase under somatic tissue pH conditions. Carbohydr Polym. 2017;164:145–153. doi: 10.1016/j.carbpol.2017.01.095. PubMed DOI
Ramos-Elorduy J, González EA, Hernández AR, Pinoa JM. Use of Tenebrio molitor (Coleoptera: Tenebrionidae) to recycle organic wastes and as feed for broiler chickens. J. Econ. Entomol. 2002;95:214–220. doi: 10.1603/0022-0493-95.1.214. PubMed DOI
Finke MD. Complete nutrient content of four species of feeder insects. Zoo Biol. 2013;32:27–36. doi: 10.1002/zoo.21012. PubMed DOI
Yi L, et al. Extraction and characterisation of protein fractions from five insect species. Food Chem. 2013;141:3341–3348. doi: 10.1016/j.foodchem.2013.05.115. PubMed DOI
Bovera F, et al. Yellow mealworm larvae (Tenebrio molitor, L.) as a possible alternative to soybean meal in broiler diets. Br. Poult. Sci. 2015;56:569–575. PubMed
Islam MM, Yang CJ. Efficacy of mealworm and super mealworm larvae probiotics as an alternative to antibiotics challenged orally with Salmonella and E. coli infection in broiler chicks. Poult. Sci. 2017;96:27–34. doi: 10.3382/ps/pew220. PubMed DOI
Hussain M, Wilson JB. New paralogues and revised time line in the expansion of the vertebrate GH18 family. J. Mol. Evol. 2013;76:240–260. doi: 10.1007/s00239-013-9553-4. PubMed DOI
Han BK, Lee WJ, Jo DH. Chitinolytic enzymes from the gizzard and the chyme of the broiler (Gallus gallus L.) Biotechnol. Lett. 1997;19:981–984. doi: 10.1023/A:1018439131967. DOI
Turk R, et al. Gene expression variation between mouse inbred strains. BMC Genomics. 2004;5:57. doi: 10.1186/1471-2164-5-57. PubMed DOI PMC
Sacranie A, et al. The effect of insoluble fiber and intermittent feeding on gizzard development, gut motility, and performance of broiler chickens. Poult. Sci. 2012;91:693–700. doi: 10.3382/ps.2011-01790. PubMed DOI
Svihus B. The gizzard: function, influence of diet structure and effects on nutrient availability. Worlds Poult. Sci. J. 2011;67:207–223. doi: 10.1017/S0043933911000249. DOI
Sikorski P, Sorbotten A, Horn SJ, Eijsink VG, Varum KM. Serratia marcescens chitinases with tunnel-shaped substrate-binding grooves show endo activity and different degrees of processivity during enzymatic hydrolysis of chitosan. Biochemistry. 2006;45:9566–9574. doi: 10.1021/bi060370l. PubMed DOI
Aam BB, et al. Production of chitooligosaccharides and their potential applications in medicine. Mar. Drugs. 2010;8:1482–1517. doi: 10.3390/md8051482. PubMed DOI PMC
Eide KB, et al. Human chitotriosidase-catalyzed hydrolysis of chitosan. Biochemistry. 2012;51:487–495. doi: 10.1021/bi2015585. PubMed DOI
Fitz LJ, et al. Acidic mammalian chitinase is not a critical target for allergic airway disease. Am. J. Respir. Cell Mol. Biol. 2012;46:71–79. doi: 10.1165/rcmb.2011-0095OC. PubMed DOI
Van Dyken SJ, et al. Spontaneous chitin accumulation in airways and age-related fibrotic lung disease. Cell. 2017;169:497–509 e413. doi: 10.1016/j.cell.2017.03.044. PubMed DOI PMC
Vannella KM, et al. Acidic chitinase primes the protective immune response to gastrointestinal nematodes. Nat. Immunol. 2016;17:538–544. PubMed 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
Awoniyi TAM, Aletor VAA, Aina JM. Performance of broiler - chickens fed on maggot meal in place of fishmeal. International Journal of Poultry Science. 2003;2:271–274. doi: 10.3923/ijps.2003.271.274. DOI
Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0. PubMed DOI
Kimura M, et al. Functional properties of mouse chitotriosidase expressed in the periplasmic space of Escherichia coli. PLoS One. 2016;11:e0164367. doi: 10.1371/journal.pone.0164367. PubMed DOI PMC
Kania K, Byrnes EA, Beilby JP, Webb SA, Strong KJ. Urinary proteases degrade albumin: implications for measurement of albuminuria in stored samples. Ann. Clin. Biochem. 2010;47:151–157. doi: 10.1258/acb.2009.009247. PubMed DOI
Hyperactivation of human acidic chitinase (Chia) for potential medical use
Noninsect-Based Diet Leads to Structural and Functional Changes of Acidic Chitinase in Carnivora