Biocatalytic Production of Hetero-Chitosan Oligosaccharides as Anti-oxidants Chapter First Online: 05 June 2019
Part of the
Sustainable Agriculture Reviews
book series (SARV, volume 35) Abstract
Abundantly available chitin/chitosan and their derivatives are full of useful bioactivities. They have numerous applications in industries like food, wastewater treatment, pharmaceuticals, agriculture, cosmetics etc. However, their insolubility in water plays spoilsport in way of their use as cost-effective biomolecules for various sectors. Breakage of chitosan to smaller oligosaccharides solves this problem to larger extent preferably using highly specific enzymes. It is well known that that bioactivities of oligosaccharides improve upon hydrolysis to lower molecular weight chitosan i.e. chitooligosaccharides. Availability and production of anti-oxidant chitooligosaccharides by non-chemical approach is desirable for consumer satisfaction. Bioprocessing of chitin/chitosan generated from marine waste to be used as bioactive chitooligosaccharides, can reduce both environmental and human health hazards to a great extent.
Here we review (1) biocatalytic approaches for chitooligosaccharides production, (2) bioprocess strategies for large scale production, (3) functionalization and (4) anti-oxidant activity of chitooligosaccharides. Specific and non-specific biocatalysts are used for chitooligomer preparation either by hydrolysis and transglycosylation approaches. Cellulase enzymes have been found to be most frequently used non-specific enzymes for chitosan hydrolysis but microbial chitosanases show excellent performance for chitooligosaccharides production both in terms of yield and specificity. Transglycosylation also have been found to be promising for chitooligosaccharides production especially at small scale. Combination reactors have been found to be most suitable for upscaling of chitooligomer production. Immobilized packed column with ultrafiltration membrane reactors are used for simultaneous hydrolysis and separation of chitooligomers. Chemically synthesized derivatives of chitooligomers have been reported in many studies by introducing carboxyl, quaternized amino, amino ethyl, sulfate, gallyl and many more groups. Amino ethyl, Gallyl, sulphated, phenolic acid conjugated and carboxylated derivatized chitooligomers have shown anti-oxidant activity. Anti-oxidant activity of chitooligomers and relation with their structure and polymerisation has been well established. Chitooligomers longer than trimer show good activity while best activity has been reported in degree of polymerisation from 10 to 12. Acetylation of chitooligomers leads to improvement in anti-oxidant activity than their deacetylated version.
Keywords Anti-oxidant Oligosaccharides Chito-oligosaccharides Chitosanase Chitin Chitosan Radical-scavenging DPPH Bioactivity Abbreviations ABTS
degree of deacetylation
electron spin resonance
ferric reducing power
polyacrylonitrile nanofibrous membrane
quaternised carboxymethyl chitooligosaccharide
reactive oxygen species
thiobarbituric acid reactive substances
tertiary butyl hydroquinone
Corresponding author acknowledges Department of Science & Technology, Government of India for financial support vide reference no (SR/WOS-A/LS-1004/2015) and (SR/WOS-A/LS-129/2009) under Women Scientist Scheme.
Aam BB, Heggset EB, Norberg AL, Sørlie M, Vårum KM, Eijsink VGH (2010) Production of chitooligosaccharides and their potential applications in medicine. Mar Drugs 8:1482–1517.
https://doi.org/10.3390/md8051482 CrossRef PubMed PubMedCentral Google Scholar
Abdel-Aziz SM, Kahil T, Keera AA (2014) Kinetic behavior of free and in situ immobilized chitosanases produced by the fungus
. World Appl Sci J 30:1–09.
https://doi.org/10.5829/idosi.wasj.2014.30.01.13980 CrossRef Google Scholar
Aiba S (1994) Preparation of N-acetylchitooligosaccharides by hydrolysis of chitosan with chitinase followed by N-acetylation. Carbohydr Res 265:323–328.
https://doi.org/10.1016/0008-6215(94)00243-6 CrossRef PubMed Google Scholar
Akiyama K, Kawazu K, Kobayashi A (1995) A novel method for chemo-enzymatic synthesis of elicitor-active chitosan oligomers and partially N-deacetylated chitin oligomers using N-acylated chitotrioses as substrates in a lysozyme-catalyzed transglycosylation reaction system. Carbohydr Res 279:151–160.
https://doi.org/10.1016/0008-6215(95)00288-X CrossRef PubMed Google Scholar
Ando T, Kataoka S (1980) Acylations of chitin with acid anhydrides in trichloroacetic acid systems. Kobunshi Ronbunshu 37:1–7.
https://doi.org/10.1295/koron.37.1 CrossRef Google Scholar
Anraku M, Gebicki JM, Iohara D, Hisao T, Kaneto U, Toru M, Hirayamaa F, Otagiri M (2018) Antioxidant activities of chitosans and its derivatives in
studies. Carbohydr Polym 199:141–149.
https://doi.org/10.1016/j.carbpol.2018.07.016 CrossRef Google Scholar
Cabrera JC, Messiaen J, Cambier P, Van Cutsem P (2006) Size, acetylation and concentration of chitooligosaccharide elicitors determine the switch from defence involving PAL activation to cell death and water peroxide production in Arabidopsis cell suspensions. Physiol Plant 127:44–56.
https://doi.org/10.1111/j.1399-3054.2006.00677.x CrossRef Google Scholar
Chang SH, Wu CH, Tsai GJ (2018) Effects of chitosan molecular weight on its antioxidant and antimutagenic properties. Carbohydr Polym 181:1026–1032.
https://doi.org/10.1016/J.CARBPOL.2017.11.047 CrossRef Google Scholar
Chatelain PG, Pintado ME, Vasconcelos MW (eds) (2014) Evaluation of chitooligosaccharide application on mineral accumulation and plant growth in Phaseolus vulgaris. Plant Sci 215:134–140.
https://doi.org/10.1016/j.plantsci.2013.11.009 CrossRef Google Scholar
Chen AS, Taguchi T, Sakai K, Kikuchi K, Wang MW, Miwa I (2003) Antioxidant activities of chitobiose and chitotriose. Biol Pharm Bull 26:1326–1330.
https://doi.org/10.1248/bpb.26.1326 CrossRef PubMed Google Scholar
Cho SY, Lee JH, Song MJ, Park PJ, Shin ES, Sohn JH (2010) Effects of chitooligosaccharide lactate salt on sleep deprivation-induced fatigue in mice. Biol Pharm Bull 33:1128–1132.
https://doi.org/10.1248/bpb.33.1128 CrossRef PubMed Google Scholar
Choi WS, Ahn KJ, Lee DW, Byun MW, Park HJ (2002) Preparation of chitosan oligomers by irradiation. Polym Degrad Stab 78:533–538.
https://doi.org/10.1248/bpb.33.1128 CrossRef Google Scholar
de Assis CF, Araújo NK, Pagnoncelli MGB, da Silva Pedrini MR, de Macedo GR, dos Santos ES (2010) Chitooligosaccharides enzymatic production by
. Bioprocess Biosyst Eng 33:893–899.
https://doi.org/10.1007/s00449-010-0412-z CrossRef PubMed Google Scholar
de Assis CF, Costa LS, Melo-Silveira RF, Oliveira RM, Pagnoncelli MGB, Rocha HAO, Macedo GR, Santos ES (2012) Chitooligosaccharides antagonize the cytotoxic effect of glucosamine. World J Microbiol Biotechnol 28:1097–1105.
https://doi.org/10.1007/s11274-011-0910-4 CrossRef PubMed Google Scholar
Dou J, Tan C, Du Y, Bai X, Wang K, Ma X (2007) Effects of chitooligosaccharides on rabbit neutrophils
. Carbohydr Polym 69:209–213.
https://doi.org/10.1016/j.carbpol.2006.09.029 CrossRef Google Scholar
El-Sayed ST, Omar NI, El Sayed ESM, Shousha WG (2017) Evaluation antioxidant and cytotoxic activities of novel chitooligosaccharides prepared from chitosan via enzymatic hydrolysis and ultrafiltration. J Appl Pharm Sci 7:50–55.
https://doi.org/10.7324/JAPS.2017.71107 CrossRef Google Scholar
Eom TK, Senevirathne M, Kim SK (2012) Synthesis of phenolic acid conjugated chitooligosaccharides and evaluation of their antioxidant activity. Environ Toxicol Pharmacol 34:519–527.
https://doi.org/10.1016/j.etap.2012.05.004 CrossRef PubMed Google Scholar
Feng T, Du Y, Li J, Wei Y, Yao P (2007) Antioxidant activity of half N-acetylated water-soluble chitosan
. Eur Food Res Technol 225:133–138.
https://doi.org/10.1007/s00217-006-0391-0 CrossRef Google Scholar
Fernandes JC, Eaton P, Nascimento H, Gião MS, Ramos ÓS, Belo L (2010) Antioxidant activity of chitooligosaccharides upon two biological systems: erythrocytes and bacteriophages. Carbohydr Polym 79:1101–1106.
https://doi.org/10.1016/j.carbpol.2009.10.050 CrossRef Google Scholar
Hamed I, Özogul F, Regenstein JM (2016) Review: regenstein industrial applications of crustacean by-products (chitin, chitosan, and chitooligosaccharides). Trends Food Sci Technol 48:40–50.
https://doi.org/10.1016/j.tifs.2015.11.007 CrossRef Google Scholar
Huang R, Rajapakse N, Kim SK (2006) Structural factors affecting radical scavenging activity of chitooligosaccharides (COS) and its derivatives. Carbohydr Polym 63:122–129.
https://doi.org/10.1016/j.carbpol.2005.08.022 CrossRef Google Scholar
Huang HC, Hong L, Chang P, Zhang J, Lu SY, Zheng BW, Jiang ZF (2015) Chitooligosaccharides attenuate Cu2+-induced cellular oxidative damage and cell apoptosis involving Nrf2 activation. Neurotox Res 27:411–420.
https://doi.org/10.1007/s12640-014-9512-x CrossRef PubMed Google Scholar
Il’ina AV, Varlamov VP (2004) Hydrolysis of chitosan in lactic acid. Appl Biochem Microbiol 40:300–303.
https://doi.org/10.1023/B:ABIM.0000025956.98250.30 CrossRef Google Scholar
Il’ina AV, Varlamov VP (2015)
antitumor activity of heterochitooligosaccharides (a review). Prikl Biokhim Mikrobiol 51:5–14.
https://doi.org/10.7868/S0555109915010067 CrossRef PubMed Google Scholar
Je JY, Park PJ, Kim SK (2004) Free radical scavenging properties of hetero chitooligosaccharides using an ESR spectroscopy. Food Chem Toxicol 42:381–387.
https://doi.org/10.1016/j.fct.2003.10.001 CrossRef PubMed Google Scholar
Jeon YJ, Kim SK (2000) Continuous production of chitooligosaccharides using a dual reactor system. Process Biochem 35:623–632.
https://doi.org/10.1016/S0032-9592(99)00118-1 CrossRef Google Scholar
Jing H, Li H (2015) Chitooligosaccharide prolongs vase life of cut roses by decreasing reactive oxygen species. Kor J Hort Sci Technol 33:383–389.
https://doi.org/10.7235/hort.2015.14188 CrossRef Google Scholar
Karadeniz F, Artan M, Kong CS, Kim SK (2010) Chitooligosaccharides protect pancreatic β-cells from hydrogen peroxide-induced deterioration. Carbohydr Polym 82:143–147.
https://doi.org/10.1016/j.carbpol.2010.04.046 CrossRef Google Scholar
Kaur S, Dhillon GS (2015) Review: recent trends in biological extraction of chitin from marine shell wastes. Crit Rev Biotechnol:44–61.
https://doi.org/10.3109/07388551.2013.798256 CrossRef Google Scholar
Khairullin RM, Yarullina LG, Troshina NB, Akhmetova IE (2001) Chitooligosaccharide-induced activation of o-phenylenediamine oxidation by wheat seedlings in the presence of oxalic acid. Biochemist 66:286–289.
https://doi.org/10.1023/A:1010247712723 CrossRef Google Scholar
Kim S K (ed) (2011) Chitin, chitosan, oligosaccharides and their derivatives: biological activities and applications. CRC Press, Boca Raton, 225p.
Kim SK, Rajapakse N (2005) Review: enzymatic production and biological activities of chitosan oligosaccharides (COS). Carbohydr Polym 62:357–368.
https://doi.org/10.1016/j.foodchem.2006.01.038 CrossRef Google Scholar
Kim KW, Thomas RL (2006) Antioxidative activity of chitosans with varying molecular weights. Food Chem 101:308–313.
https://doi.org/10.1016/j.foodchem.2006.01.038 CrossRef Google Scholar
Koryagin AS, Erofeeva EA, Yakimovich NO, Aleksandrova EA, Smirnova LA, Mal’kov AV (2006) Analysis of antioxidant properties of chitosan and its oligomers. Bull Exp Biol Med 142:461–463.
https://doi.org/10.1007/s10517-006-0392-9 CrossRef PubMed Google Scholar
Laokuldilok T, Potivas T, Kanha N, Surawang S, Seesuriyachan P, Wangtueai S (2017) Physicochemical, antioxidant, and antimicrobial properties of chitooligosaccharides produced using three different enzyme treatment. Food Biosci 18:28–33.
https://doi.org/10.1016/j.fbio.2017.03.004 CrossRef Google Scholar
Li X, Liu BO, Wang X, Han Y, Su H, Zeng X (2012) Synthesis, characterization and antioxidant activity of quaternized carboxymethyl chitosan oligosaccharides. J Macromol Sci A 49:861–868.
https://doi.org/10.1080/10601325.2012.714679 CrossRef Google Scholar
Li K, Xing R, Liu S, Li P (2016) Advances in preparation, analysis and biological activities of single chitooligosaccharides. Carbohydr Polym 139:178–190.
https://doi.org/10.1016/j.carbpol.2015.12.016 CrossRef PubMed Google Scholar
Liaqat F, Rengin E (2018) Review: chitooligosaccharides and their biological activities. Carbohydr Polym 184:243–259.
https://doi.org/10.1016/j.carbpol.2017.12.067 CrossRef PubMed Google Scholar
Liu HT, Li WM, Xu G, Li XY, Bai XF, Wei P (2009) Chitosan oligosaccharides attenuate hydrogen peroxide-induced stress injury in human umbilical vein endothelial cells. Pharmacol Res 59:167–175.
https://doi.org/10.1016/j.phrs.2008.12.001 CrossRef PubMed Google Scholar
Lodhi G, Yon SK, Hwang JW, Kim SK, Jeon YJ, Je JY (2014) Chitooligosaccharide and its derivatives: preparation and biological applications. Biomed Res Int:1–13.
https://doi.org/10.1155/2014/654913 Google Scholar
Lu X, Guo H, Zhang Y (2012) Protective effects of sulfated chitooligosaccharides against hydrogen peroxide-induced damage in MIN6 cells. Int J Biol Macromol 50:50–58.
https://doi.org/10.1016/j.ijbiomac.2011.09.020 CrossRef PubMed Google Scholar
Lu C, Park MK, Lu C, Lee YH, Chai KY (2015) A mussel-inspired chitooligosaccharide based multidentate ligand for highly stabilized nanoparticles. J Mater Chem B 3:3730–3737.
https://doi.org/10.1039/c5tb00114e CrossRef Google Scholar
Luo Z, Dong X, Ke Q, Duan Q, Shen L (2014) Chitooligosaccharides inhibit ethanol-induced oxidative stress via activation of Nrf2 and reduction of MAPK phosphorylation. Oncol Rep 32:2215–2222.
https://doi.org/10.3892/or.2014.3463 CrossRef PubMed Google Scholar
Mendis E, Kim MM, Rajapakse N, Kim SK (2007) An in vitro cellular analysis of the radical scavenging efficacy of chitooligosaccharides. Life Sci 80:2118–2127.
https://doi.org/10.1016/j.lfs.2007.03.016 CrossRef PubMed Google Scholar
Montilla A, Ruiz-Matute AI, Corzo N, Giacomini C, Irazoqui G (2013) Enzymatic generation of chitooligosaccharides from chitosan using soluble and immobilized glycosyltransferase (Branchzyme). J Agric Food Chem 60:10360–10367.
https://doi.org/10.1021/jf403321r CrossRef Google Scholar
Mourya VK, Inamdar NN (2009) Trimethyl chitosan and its applications in drug delivery. J Mater Sci Mater Med 20:1057–1079.
https://doi.org/10.1007/s10856-008-3659-z CrossRef PubMed Google Scholar
Mourya VK, Inamdar NN, Choudhari YM (2011) Chitooligosaccharides: synthesis, characterization and applications. Polym Sci Ser A 53:583–612.
https://doi.org/10.1134/S0965545X11070066 CrossRef Google Scholar
Ngo DN, Lee SH, Kim MM, Kim SK (2009) Production of chitin oligosaccharides with different molecular weights and their antioxidant effect in RAW 264.7 cells. J Funct Foods 1:60–198.
https://doi.org/10.1016/j.jff.2009.01.008 CrossRef Google Scholar
Ngo DH, Qian ZJ, Ngo DN, Vo TS, Wijesekara I, Kim SK (2011) Gallyl chitooligosaccharides inhibit intracellular free radical-mediated oxidation. Food Chem 128:974–981.
https://doi.org/10.1016/j.foodchem.2011.03.128 CrossRef Google Scholar
Ngo D, Ngo D, Vo T, Ryu B, Van TQ, Kim S (2012) Protective effects of aminoethyl-chitooligosaccharides against oxidative stress and inflammation in murine microglial BV-2 cells. Carbohydr Polym 88:743–747.
https://doi.org/10.1016/j.carbpol.2012.01.037 CrossRef Google Scholar
Nidheesh T, Pal GK, Suresh PV (2015) Chitooligomers preparation by chitosanase produced under solid state fermentation using shrimp by-products as substrate. Carbohydr Polym 121:1–9.
https://doi.org/10.1016/j.carbpol.2014.12.017 CrossRef PubMed Google Scholar
Oh SH, Ryu BM, Ngo DH, Kim WS, Kim DG, Kim SK (2017) 4-hydroxybenzaldehyde-chitooligomers suppresses H2O2-induced oxidative damage in microglia BV-2 cells. Carbohydr Res 440–441:32–37.
https://doi.org/10.1016/j.carres.2017.01.007 CrossRef PubMed Google Scholar
Park PJ, Je JY, Kim SK (2003) Free radical scavenging activity of chitooligosaccharides by electron spin resonance spectrometry. J Agric Food Chem 51:4624–4627.
https://doi.org/10.1021/jf034039 CrossRef PubMed Google Scholar
Park PJ, Lee HK, Kim SK (2004) Preparation of hetero-chitooligosaccharides and their antimicrobial activity on
. J Microbiol Biotechnol 14:41–47. Retrieved from:
http://www.jmb.or.kr/journal/main.html?mod=vol&tops=&year=2004 Google Scholar
Pham-Huy LA, He H, Pham-Huy C (2008) Free radicals, antioxidants in disease and health. Int J Biomed Sci 4:89–96.
https://doi.org/10.1073/pnas.0804252105 CrossRef PubMed PubMedCentral Google Scholar
Popa-Nita S, Lucas JM, Ladavière C, David L, Domard A (2009) Mechanisms involved during the ultrasonically induced depolymerization of chitosan: characterization and control. Biomacromolecules 10:1203–1211.
https://doi.org/10.1021/bm8014472 CrossRef PubMed Google Scholar
Qu D, Han J (2016) Investigation of the antioxidant activity of chitooligosaccharides on mice with high-fat diet. Rev Bras Zootec 45:661–666.
https://doi.org/10.1590/S1806-92902016001100004 CrossRef Google Scholar
Rao MS, Chander R, Sharma A (2006) Radiation processed chitosan a potent antioxidant. Food Technol 27:188–194. 10.1.1.563.3945.
Salgaonkar N, Prakash D, Nawani NN, Kapadnis BP (2015) Comparative studies on ability of N-acetylated chitooligosaccharides to scavenge reactive oxygen species and protect DNA from oxidative damage. Indian J Biotechnol 14:186–192.
http://nopr.niscair.res.in/handle/123456789/31805 Google Scholar
Santos-Moriano P, Woodley JM, Plou FJ (2016) Continuous production of chitooligosaccharides by an immobilized enzyme in a dual-reactor system. J Mol Catal B Enzym 133:211–217.
https://doi.org/10.1016/j.molcatb.2016.09.001 CrossRef Google Scholar
Sindhi V, Gupta V, Sharma K, Bhatnagar S, Kumari R, Dhaka N (2013) Review: potential applications of antioxidants. J Pharm Res 7:828–835.
https://doi.org/10.1016/j.jopr.2013.10.001 CrossRef Google Scholar
Singh P (2016) Review: effect of chitosans and chitooligosaccharides on the processing and storage quality of foods of animal and aquatic origin. Nutr Food Sci 46:51–81.
https://doi.org/10.1108/NFS-08-2015-0092 CrossRef Google Scholar
Sinha S, Tripathi P, Chand S (2012a) A new bifunctional chitosanase enzyme from
sp. and its application in production of antioxidant chitooligosaccharides. Appl Biochem Biotechnol 167:1029–1039.
https://doi.org/10.1007/s12010-012-9546-6 CrossRef PubMed Google Scholar
Sinha S, Dhakate SR, Kumar P, Mathur RB, Tripathi P, Chand S (2012b) Electrospun polyacrylonitrile nanofibrous membranes for chitosanase immobilization and its application in selective production of chitooligosaccharides. Bioresour Technol 115:152–157.
https://doi.org/10.1016/j.biortech.2011.11.101 CrossRef PubMed Google Scholar
Sinha S, Chand S, Tripathi P (2014) Microbial degradation of chitin waste for production of chitosanase and food related bioactive compounds. Appl Biochem Microbiol 50(2):125–133.
https://doi.org/10.1134/S0003683814020173 CrossRef Google Scholar
Sinha S, Chand S, Tripathi P (2016a) Enzymatic production of glucosamine and chitooligosaccharides using newly isolated exo-β-d-glucosaminidase having transglycosylation activity. 3 Biotech 6(1):1–9.
https://doi.org/10.1007/s13205-015-0330-5 CrossRef Google Scholar
Sinha S, Chand S, Tripathi P (2016b) Recent progress in chitosanase production of monomer-free chitooligosaccharides: bioprocess strategies and future applications. Appl Biochem Biotechnol 180:883–899.
https://doi.org/10.1007/s12010-016-2140-6 CrossRef PubMed Google Scholar
Sun T, Yun Z, Jing X, Xuhong Y (2011) Antioxidant activity of N-acyl chitosan oligosaccharide with same substituting degree. Bioorg Med Chem Lett 21:798–800.
https://doi.org/10.1016/j.bmcl.2010.11.097 CrossRef PubMed Google Scholar
Usui T, Hidenori M, Kiyoshi I (1990) Enzymic synthesis of useful Chito-oligosaccharides utilizing transglycosylation by chitinolytic enzymes in a buffer containing ammonium sulfate. Carbohydr Res 203:65–77.
https://doi.org/10.1016/0008-6215(90)80046-6 CrossRef PubMed Google Scholar
Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84.
https://doi.org/10.1016/j.biocel.2006.07.001 CrossRef PubMed Google Scholar
Vårum KM, Holme HK, Izume M, Stokke BT, Smidsrød O (1996) Determination of enzymatic hydrolysis specificity of partially N-acetylated chitosans. Biochim Biophys Acta, Gen Subj 1291(1):5–15.
https://doi.org/10.1016/0304-4165(96)00038-4 CrossRef Google Scholar
Vasconcelos MW (2012) Chitosan and chitooligosaccharide utilization in phytoremediation and biofortification programs: current knowledge and future perspectives. Front Plant Sci 5:1–4.
https://doi.org/10.3389/fpls.2014.00616 CrossRef Google Scholar
Vidanarachchi J, Kurukulasuriya M, Kim SK (2010) Chitin, chitosan, and their oligosaccharides in food industry. In: Chitin, chitosan, oligosaccharides and their derivatives. CRC Press, Boca Raton, pp 543–560.
https://doi.org/10.1201/EBK1439816035-c38 CrossRef Google Scholar
Vo TS, Ngo DH, Bach LG, Ngo DN, Kim SK (2017) The free radical scavenging and anti inflammatory activities of gallate-chitooligosaccharides in human lung epithelial A549 cells. Process Biochem 54:188–194.
https://doi.org/10.1016/j.procbio.2017.01.001 CrossRef Google Scholar
Wu GJ, Tsai GJ (2004) Cellulase degradation of shrimp chitosan for the preparation of a water-soluble hydrolysate with immunoactivity. Fish Sci 70:1113–1120.
https://doi.org/10.1111/j.1444-2906.2004.00912.x CrossRef Google Scholar
Xia W, Liu P, Liu J (2008) Advance in chitosan hydrolysis by non-specific cellulases. Bioresour Technol:6751–6762.
https://doi.org/10.1016/j.biortech.2008.01.011 CrossRef Google Scholar
Xie C, Xin W, Cimin L, Qinhua W, Zhiyong F, Li S (2016) Chitosan oligosaccharide affects antioxidant defense capacity and placental amino acids transport of sows. BMC Vet Res 12(1):1–8.
https://doi.org/10.1186/s12917-016-0872-8 CrossRef Google Scholar
Xu Y, Wang L, Li YK, Wang CQ (2016) Reduction and pH dual-responsive nanoparticles based chitooligosaccharide-based graft copolymer for doxorubicin delivery. Colloids Surf A Physicochem Eng Asp 497:8–15.
https://doi.org/10.1016/j.colsurfa.2016.01.049 CrossRef Google Scholar
Yamaguchi R, Arai Y, Itoh T (1982) A microfibril formation from depolymerized chitosan by n-acetylation. Agric Biol Chem 46:2379–2381.
https://doi.org/10.1080/00021369.1982.10865442 CrossRef Google Scholar
Yang Y, Biao Y (2014) Recent advances in the synthesis of chitooligosaccharides and congeners. Tetrahedron 70:1023–1046.
https://doi.org/10.1016/j.tet.2013.11.064 CrossRef Google Scholar
Yang Y, Shu R, Shao J, Xu G, Gu X (2006) Radical scavenging activity of chitooligosaccharide with different molecular weights. Eur Food Res Technol 222:36–40.
https://doi.org/10.1007/s00217-005-0028-8 CrossRef Google Scholar
Yu BP (ed) (1994) Cellular defenses against damage from reactive oxygen species. Physiol Rev 74(1):139–162.
https://doi.org/10.1152/physrev.1918.104.22.168 CrossRef Google Scholar
Yuan W (2009) Antioxidant activity of chito-oligosaccharides on pancreatic islet cells in streptozotocin-induced diabetes in rats. World J Gastroenterol 15(11):1339.
https://doi.org/10.3748/wjg.15.1339 CrossRef PubMed PubMedCentral Google Scholar
Zhang H, Zhao X, Yang J, Yin H, Wang W, Lu H, Du Y (2011) Nitric oxide production and its functional link with OIPK in tobacco defense response elicited by chitooligosaccharide. Plant Cell Rep 30:1153–1162.
https://doi.org/10.1007/s00299-011-1024-z CrossRef PubMed Google Scholar
Zhang Y, Zhou X, Lusha J, Du X, Sang Q, Chen F (2017) Enzymatic single-step preparation and antioxidant activity of hetero-chitooligosaccharides using non-pretreated housefly larvae powder. Carbohydr Polym 172:113–119.
https://doi.org/10.1016/j.carbpol.2017.05.037 CrossRef PubMed Google Scholar
Zhou TX, Chen YJ, Yoo JS, Huang Y, Lee JH, Jang HD (2009) Effects of chitooligosaccharide supplementation on performance, blood characteristics, relative organ weight, and meat quality in broiler chickens. Poult Sci 88:593–600.
https://doi.org/10.3382/ps.2008-00285 CrossRef PubMed Google Scholar Copyright information
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