2,156
Views
73
CrossRef citations to date
0
Altmetric
Reviews

Marine oligosaccharides originated from seaweeds: Source, preparation, structure, physiological activity and applications

ORCID Icon, , &

References

  • Anastyuk, S. D., N. M. Shevchenko, S. P. Ermakova, O. S. Vishchuk, E. L. Nazarenko, P. S. Dmitrenok, and T. N. Zvyagintseva. 2012. Anticancer activity in vitro of a fucoidan from the brown alga Fucus evanescens and its low-molecular fragments, structurally characterized by tandem mass-spectrometry. Carbohydrate Polymers 87 (1):186–94. doi: 10.1016/j.carbpol.2011.07.036.
  • Antonio, M., S. Andrea, S. Nunziacarla, A. Valbona, S. Marilena, and C. Gioele. 2017. Gracilaria gracilis, Source of Agar: A short review. Current Organic Chemistry 21 (5):380–6. doi: 10.2174/1385272820666161017164605.
  • Assreuy, A. M. S., D. M. Gomes, M. S. J. da Silva, V. M. Torres, R. C. L. Siqueira, A. d. F. Pires, D. N. Criddle, N. M. N. de Alencar, B. S. Cavada, A. H. Sampaio, et al. 2008. Biological effects of a sulfated-polysaccharide isolated from the marine red algae Champia feldmannii. Biological & Pharmaceutical Bulletin 31 (4):691–5. doi: 10.1248/bpb.31.691.
  • Azofeifa, K., Y. Angulo, and B. Lomonte. 2008. Ability of fucoidan to prevent muscle necrosis induced by snake venom myotoxins: Comparison of high- and low-molecular weight fractions. Toxicon 51 (3):373–80. doi: 10.1016/j.toxicon.2007.10.008.
  • Bakunina, I. Y., O. I. Nedashkovskaya, S. A. Alekseeva, E. P. Ivanova, L. A. Romanenko, N. M. Gorshkova, V. V. Isakov, T. N. Zvyagintseva, and V. V. Mikhailov. 2002. Degradation of fucoidan by the marine proteobacterium pseudoalteromonas citrea. Microbiology 71 (1):41–7. doi: 10.1023/A:1017994131769.
  • Bilan, M. I., A. A. Grachev, A. S. Shashkov, M. Kelly, C. J. Sanderson, N. E. Nifantiev, and A. I. Usov. 2010. Further studies on the composition and structure of a fucoidan preparation from the brown alga Saccharina latissima. Carbohydrate Research 345 (14):2038–47. doi: 10.1016/j.carres.2010.07.009.
  • Borgogna, M., B. Bellich, and A. Cesaro. 2011. Marine polysaccharides in microencapsulation and application to aquaculture: “From sea to sea. Marine Drugs 9 (12):2572–604. doi: 10.3390/md9122572.
  • Bo-Yang, H. U., Y. Nie, L. Sun, N. Satoru, L. J. Yin, H. Zhou, and Y. Q. Cheng. 2016. Antioxidant evaluation of alginate oligosaccharides prepared by acid hydrolysis with different conditions. Science Technology of Food Industry 37 (10):136–40.
  • Campo, V. L., D. F. Kawano, D. B. d. Silva, and I. Carvalho. 2009. Carrageenans: Biological properties, chemical modifications and structural analysis – A review. Carbohydrate Polymers 77 (2):167–80. doi: 10.1016/j.carbpol.2009.01.020.
  • Chabut, D., A.-M. Fischer, S. Colliec-Jouault, I. Laurendeau, S. Matou, B. Le Bonniec, and D. Helley. 2003. Low molecular weight fucoidan and heparin enhance the basic fibroblast growth factor-induced tube formation of endothelial cells through heparan sulfate-dependent α6 overexpression. Molecular Pharmacology 64 (3):696–702. doi: 10.1124/mol.64.3.696.
  • Chandia, N. P., B. Matsuhiro, and A. E. Vasquez. 2001. Alginic acids in Lessonia trabeculata: Characterization by formic acid hydrolysis and FT-IR spectroscopy. Carbohydrate Polymers 46 (1):81–7.
  • Chen, J., Y. Hu, L. Zhang, Y. Wang, S. Wang, Y. Zhang, H. Guo, D. Ji, and Y. Wang. 2017. Alginate Oligosaccharide DP5 exhibits antitumor effects in osteosarcoma patients following surgery. Frontiers in Pharmacology 8:1–13. doi: 10.3389/fphar.2017.00623.
  • Chen, Y. J., W. M. Wang, S. H. Chen, and E. Y. Xie. 2012. Study on the degradation conditions of fucoidan from Sargassum henslowianum. Science Technology of Food Industry 20:284–287.
  • Chen, S. H., W. M. Wang, H. Liu, C. L. Li, and C. Y. Liu. 2010. Study on the purification and lowing hyperlipidemia activity of fucoidan from Sargassum henslowianum. Food Fermentation Industries 36 (5):28–31.
  • Chen, H. M., and X. J. Yan. 2006. Effects of agar-oligosaccharides on blood glucose level and oxidation-antioxidation status of diabetic mice. Acta Nutrimenta Sinica 28 (2):152–155.
  • Chen, H. M., X. J. Yan, W. Feng, L. Jing, and W. F. Xu. 2007. In vitro anti-angiogenic action of lambda-carrageenan oligosaccharides. Yao Xue Xue Bao = Acta Pharmaceutica Sinica 42 (6):595–600.
  • Chen, H. M., X. J. Yan, T. Y. Mai, F. Wang, and W. F. Xu. 2009. Lambda-carrageenan oligosaccharides elicit reactive oxygen species production resulting in mitochondrial-dependent apoptosis in human umbilical vein endothelial cells. International Journal of Molecular Medicine 24 (6):801–806. doi: 10.3892/ijmm_00000295.
  • Chen, H. M., X. J. Yan, F. Wang, J. Lin, and X. U. Wei-Feng. 2007. Study on the Anti-angiogenic role of Agaro-oligosaccharide. Acta Nutrimenta Sinica 29 (4):405–407.
  • Chen, H., X. Yan, P. Zhu, and J. Lin. 2006. Antioxidant activity and hepatoprotective potential of agaro-oligosaccharides in vitro and in vivo. Nutrition Journal 5 (1):31. doi: 10.1186/1475-2891-5-31.
  • Choi, J. I., and H. J. Kim. 2013. Preparation of low molecular weight fucoidan by gamma-irradiation and its anticancer activity. Carbohydrate Polymers 97 (2):358–362. doi: 10.1016/j.carbpol.2013.05.002.
  • Choi, E. M., A. J. Kim, Y. O. Kim, and J. K. Hwang. 2005. Immunomodulating activity of arabinogalactan and fucoidan in vitro. Journal of Medicinal Food 8 (4):446–453. doi: 10.1089/jmf.2005.8.446.
  • Chu, H. R., and J. C. Tang. 2008. Effects of alginate oligosaccharides on rhizosphere microbial communities in petroleum contaminated soils using PCR-DGGE analysis. Journal of Biotechnology 136:S696. doi: 10.1016/j.jbiotec.2008.07.1615.
  • Colliec Jouault, S., S. Mauray, J. Theveniaux, C. Sternberg, B. Vidal, A. M. Fischer, and J. Millet. 1999. Antithrombotic and anticoagulant activities of a low molecular weight fucoidan by the subcutaneous route. Thrombosis and Haemostasis 81 (3):391–395. doi: 10.1055/s-0037-1614484.
  • Daniel, R., O. Berteau, J. Jozefonvicz, and N. Goasdoue. 1999. Degradation of algal (Ascophyllum nodosum) fucoidan by an enzymatic activity contained in digestive glands of the marine mollusc Pecten maximus. Carbohydrate Research 322 (3–4):291–297. doi: 10.1016/S0008-6215(99)00223-2.
  • Doubet, R. S., and R. S. Quatrano. 1982. Isolation of marine bacteria capable of producing specific lyases for alginate degradation. Applied and Environmental Microbiology 44 (3):754–756. doi: 10.1128/AEM.44.3.754-756.1982.
  • Duan, F., Y. Yu, Z. Liu, L. Tian, and H. Mou. 2016. An effective method for the preparation of carrageenan oligosaccharides directly from Eucheuma cottonii using cellulase and recombinant κ-carrageenase. Algal Research 15:93–99. doi: 10.1016/j.algal.2016.02.006.
  • Duarte, M. E. R., M. A. Cardoso, M. D. Noseda, and A. S. Cerezo. 2001. Structural studies on fucoidans from the brown seaweed Sargassum stenophyllum. Carbohydrate Research 333 (4):281–293. doi: 10.1016/S0008-6215(01)00149-5.
  • Duckworth, M., and W. Yaphe. 1971. The structure of agar. Part I. Fractionation of a complex mixture of polysaccharides. Carbohydrate Research 16 (1):189–197. doi: 10.1016/S0008-6215(00)86113-3.
  • Durand, E., D. Helley, A. Al Haj Zen, C. Dujols, P. Bruneval, S. Colliec-Jouault, A.-M. Fischer, and A. Lafont. 2008. Effect of low molecular weight fucoidan and low molecular weight heparin in a rabbit model of arterial thrombosis. Journal of Vascular Research 45 (6):529–537. doi: 10.1159/000129687.
  • Enoki, T., S. Okuda, Y. Kudo, F. Tskashima, H. Sagawa, and I. Kato. 2010. Oligosaccharides from agar inhibit pro-inflammatory mediator release by inducing heme oxygenase 1. Journal of the Agricultural Chemical Society of Japan 74 (4):766–770. doi: 10.1271/bbb.90803.
  • Falkeborg, M., L.-Z. Cheong, C. Gianfico, K. M. Sztukiel, K. Kristensen, M. Glasius, X. Xu, and Z. Guo. 2014. Alginate oligosaccharides: Enzymatic preparation and antioxidant property evaluation. Food Chemistry 164:185–194. doi: 10.1016/j.foodchem.2014.05.053.
  • Gao, K., and K. R. McKinley. 1994. Use of macroalgae for marine biomass production and CO2remediation: A review. Journal of Applied Phycology 6 (1):45–60. doi: 10.1007/BF02185904.
  • Ghanbarzadeh, M., A. Golmoradizadeh, and A. Homaei. 2018. Carrageenans and carrageenases: Versatile polysaccharides and promising marine enzymes. Phytochemistry Reviews 17 (3):535–37. doi: 10.1007/s11101-018-9548-2.
  • Goh, C. H., P. W. S. Heng, and L. W. Chan. 2012. Alginates as a useful natural polymer for microencapsulation and therapeutic applications. Carbohydrate Polymers 88 (1):1–12. doi: 10.1016/j.carbpol.2011.11.012.
  • González Ocampo, J. I., N. Bassous, C. P. Ossa Orozco, and T. J. Webster. 2018. Evaluation of cytotoxicity and antimicrobial activity of an injectable bone substitute of carrageenan and nano hydroxyapatite. Journal of Biomedical Materials Research Part A (9999):1–10. doi: 10.1002/jbm.a.36488.
  • Grasdalen, H. 1983. High-field, 1H-n.m.r. spectroscopy of alginate: Sequential structure and linkage conformations. Carbohydrate Research 118 (1):255–260. doi: 10.1016/0008-6215(83)88053-7.
  • Guicun Li, Z. Z., and G. Meiyu. 2002. Oxidative degradation of κ-Carrageenan. Journal of Qingdao Institute of Chemical Technology 23 (4):48–51.
  • Guo, J.-J., L.-L. Ma, H.-T. Shi, J.-B. Zhu, J. Wu, Z.-W. Ding, Y. An, Y.-Z. Zou, and J.-B. Ge. 2016. Alginate oligosaccharide prevents acute doxorubicin cardiotoxicity by suppressing oxidative stress and endoplasmic reticulum-mediated apoptosis. Marine Drugs 14 (12):231. doi: 10.3390/md14120231.
  • Guo, J., Z. Zheng, L. Xu, S. Zeng, C. Chi, L. Zhang, and B. Zheng. 2018. Purification and characterisation of κ-carrageenan oligosaccharides prepared by κ-Carrageenase from Thalassospira sp. Fjfst-332. Carbohydrate Polymers 180:314–327. doi: 10.1016/j.carbpol.2017.10.043.
  • Haige Wu, Z. Y. 2019. Effects of enzymatic hydrolysate of Laminaria japonica on growth and immune-related factors of sea cucumber. China Brewing 38 (4):160–164.
  • Hamer, G. K., S. S. Bhattacharjee, and W. Yaphe. 1977. Analysis of the enzymic hydrolysis products of agarose by13C-n.m.r. spectroscopy. Carbohydrate Research 54 (1):C7–C10. doi: 10.1016/S0008-6215(00)80567-4.
  • Higashimura, Y., Y. Naito, T. Takagi, K. Mizushima, Y. Hirai, A. Harusato, H. Ohnogi, R. Yamaji, H. Inui, Y. Nakano, et al. 2013. Oligosaccharides from agar inhibit murine intestinal inflammation through the induction of heme oxygenase-1 expression. Journal of Gastroenterology 48 (8):897–909. doi: 10.1007/s00535-012-0719-4.
  • Higashimura, Y., Y. Naito, T. Takagi, Y. Tanimura, K. Mizushima, A. Harusato, and H. Ohnogi. 2014. Preventive effect of agaro-oligosaccharides on non-steroidal anti-inflammatory drug-induced small intestinal injury in mice. Journal of Gastroenterology and Hepatology 29 (2):310–317. doi: 10.1111/jgh.12373.
  • Hlawaty, H., N. Suffee, A. Sutton, O. Oudar, O. Haddad, V. Ollivier, C. Laguillier-Morizot, L. Gattegno, D. Letourneur, and N. Charnaux. 2011. Low molecular weight fucoidan prevents intimal hyperplasia in rat injured thoracic aorta through the modulation of matrix metalloproteinase-2 expression. Biochemical Pharmacology 81 (2):233–243. doi: 10.1016/j.bcp.2010.09.021.
  • Holtkamp, A. D., S. Kelly, R. Ulber, and S. Lang. 2009. Fucoidans and fucoidanases—focus on techniques for molecular structure elucidation and modification of marine polysaccharides. Applied Microbiology and Biotechnology 82 (1):1–11. doi: 10.1007/s00253-008-1790-x.
  • Huafang Bao, L. L.., Y. Bao, and J. C. Brewing. 2010. Oligoalginate product by alginate lyase and its antioxidant capacity. China Brewing 29 (4):82–84.
  • Hu, B., Q. Gong, Y. Wang, Y. Ma, J. Li, and W. Yu. 2006. Prebiotic effects of neoagaro-oligosaccharides prepared by enzymatic hydrolysis of agarose. Anaerobe 12 (5–6):260–266. doi: 10.1016/j.anaerobe.2006.07.005.
  • Hu, X. K., X. L. Jiang, H. M. Hwang, S. L. Liu, and H. S. Guan. 2004. Antitumour activities of alginate-derived oligosaccharides and their sulphated substitution derivatives. European Journal of Phycology 39 (1):67–71. doi: 10.1080/09670260310001636695.
  • Iwamoto, M., M. Kurachi, T. Nakashima, D. Kim, K. Yamaguchi, T. Oda, Y. Iwamoto, and T. Muramatsu. 2005. Structure-activity relationship of alginate oligosaccharides in the induction of cytokine production from RAW264.7 cells. FEBS Letters 579 (20):4423–4429. doi: 10.1016/j.febslet.2005.07.007.
  • Jeong, B. E., E.-J. Ko, and H.-G. Joo. 2012. Cytoprotective effects of fucoidan, an algae-derived polysaccharide on 5-fluorouracil-treated dendritic cells. Food and Chemical Toxicology 50 (5):1480–1484. doi: 10.1016/j.fct.2012.01.034.
  • Jin, H. G. L., W. H. Wang, and J. Zhang. 2017. Fucoidan degradation and preparation of fuco-oligosaccharides from Saccharina japonica. Chemical Journal of Chinese Universities 38 (12):2193–2197.
  • Jung, L., L. Sung, K. Taeseong, J. Seon-A, K. Se, K. Hyun, and K. Hyoung. 2015. Fucoidan from Fucus vesiculosus protects against alcohol-induced liver damage by modulating inflammatory mediators in mice and HepG2 Cells. Marine Drugs 13 (2):1051–1067.
  • Kamińska-Dwórznicka, A., A. Antczak, K. Samborska, and A. Lenart. 2015. Acid hydrolysis of kappa-carrageenan as a way of gaining new substances for freezing process modification and protection from excessive recrystallisation of ice. International Journal of Food Science & Technology 50 (8):1799–1806. doi: 10.1111/ijfs.12820.
  • Kang, D. H., S. K. You, Y. C. Joo, K. S. Sang, J. E. Hyeon, and S. O. Han. 2018. Synergistic effect of the enzyme complexes comprising agarase, carrageenase and neoagarobiose hydrolase on degradation of the red algae. Bioresource Technology 250 (6):666–672. doi: 10.1016/j.biortech.2017.11.098.
  • Kanjanamosit, N., C. Muangnapoh, and M. Phisalaphong. 2010. Biosynthesis and characterization of bacteria cellulose-alginate film. Journal of Applied Polymer Science 115 (3):1581–1588. doi: 10.1002/app.31138.
  • Kawada, A., N. Hiura, M. Shiraiwa, S. Tajima, M. Hiruma, K. Hara, and H. Takahara. 1997. Stimulation of human keratinocyte growth by alginate oligosaccharides, a possible co-factor for epidermal growth factor in cell culture. FEBS Letter 408 (1):43–46.
  • Kawada, A., N. Hiura, S. Tajima, and H. Takahara. 1999. Alginate oligosaccharides stimulate VEGF-mediated growth and migration of human endothelial cells. Archives of Dermatological Research 291 (10):542–547. doi: 10.1007/s004030050451.
  • Khan, S., A. Tøndervik, H. Sletta, G. Klinkenberg, C. Emanuel, E. Onsøyen, R. Myrvold, R. A. Howe, T. R. Walsh, K. E. Hill, et al. 2012. Overcoming drug resistance with alginate oligosaccharides able to potentiate the action of selected antibiotics. Antimicrobial Agents and Chemotherapy 56 (10):5134–5141. doi: 10.1128/AAC.00525-12.
  • Kusaykin, M., I. Bakunina, V. Sova, S. Ermakova, T. Kuznetsova, N. Besednova, T. Zaporozhets, and T. Zvyagintseva. 2008. Structure, biological activity, and enzymatic transformation of fucoidans from the brown seaweeds. Biotechnology Journal 3 (7):904–915. doi: 10.1002/biot.200700054.
  • Lang, Y. Z., X. Zhao, L. L. Liu, and G. L. Yu. 2014. Applications of mass spectrometry to structural analysis of marine oligosaccharides. Marine Drugs 12 (7) :4005–4030. doi: 10.3390/md12074005.
  • Larsen, B., and A. Haug. 1958. Chemical composition of the brown alga Ascophyllum nodosum (L.) Le Jol.: Presence of reducing compounds in Ascophyllum nodosum. Nature 181 (4617):1224–1224. doi: 10.1038/1811224a0.
  • Laurienzo, P. 2010. Marine polysaccharides in pharmaceutical applications: An overview. Marine Drugs 8 (9):2435–2465. doi: 10.3390/md8092435.
  • Li, J., F. Han, X. Lu, X. Fu, C. Ma, Y. Chu, and W. Yu. 2007. A simple method of preparing diverse neoagaro-oligosaccharides with β-agarase. Carbohydrate Research 342 (8):1030–1033. doi: 10.1016/j.carres.2007.02.008.
  • Lii, C. Y., C. H. Chen, A. I. Yeh, and M. F. Lai. 1999. Preliminary study on the degradation kinetics of agarose and carrageenans by ultrasound. Food Hydrocolloids 13 (6):477–481. doi: 10.1016/S0268-005X(99)00031-4.
  • Li, L., X. Jiang, H. Guan, and P. Wang. 2011. Preparation, purification and characterization of alginate oligosaccharides degraded by alginate lyase from Pseudomonas sp. HZJ 216. Carbohydrate Research 346 (6):794–800. doi: 10.1016/j.carres.2011.01.023.
  • Li, B., F. Lu, X. Wei, and R. Zhao. 2008. Fucoidan: Structure and bioactivity. Molecules 13 (8):1671–1695. doi: 10.3390/molecules13081671.
  • Liping Sun, C. X. J. J. o. O. U. o. Q. 2005. A study of the antioxidant abilities of alginate oligosaccharides. Journal of Ocean University of Qingdao 35 (5):811–814.
  • Liu, R., X. Jiang, H. Guan, X. Li, Y. Du, P. Wang, and H. Mou. 2009. Promotive effects of alginate-derived oligosaccharides on the inducing drought resistance of tomato. Journal of Ocean University of China 8 (3):303–311. doi: 10.1007/s11802-009-0303-6.
  • Li, X. X., A. H. Xu, H. G. Xie, W. T. Yu, W. Y. Xie, and X. J. Ma. 2010. Preparation of low molecular weight alginate by hydrogen peroxide depolymerization for tissue engineering. Carbohydrate Polymers 79 (3):660–664. doi: 10.1016/j.carbpol.2009.09.020.
  • Lu, W., L. Li, W. Y. Mei, Y. Quan, L. I. Zhi En, and X. Z. Hong. 2001. Comparative research on the structures and physical-chemical properties of agars from several agarophyta. Oceanologia Et Limnologia Sinica 32 (6):658–664.
  • Luo, M., B. Shao, W. Nie, X.-W. Wei, Y.-L. Li, B.-L. Wang, Z.-Y. He, X. Liang, T.-H. Ye, Y.-Q. Wei. 2015. Antitumor and adjuvant activity of λ-carrageenan by stimulating immune response in cancer immunotherapy. Scientific Report 5:11062.
  • Luyt, C.-E., A. Meddahi-Pellé, B. Ho-Tin-Noe, S. Colliec-Jouault, J. Guezennec, L. Louedec, H. Prats, M.-P. Jacob, M. Osborne-Pellegrin, D. Letourneur, et al. 2003. Low-molecular-weight fucoidan promotes therapeutic revascularization in a rat model of critical Hindlimb Ischemia. Journal of Pharmacology and Experimental Therapeutics 305 (1):24–30. doi: 10.1124/jpet.102.046144.
  • Ma, L. 2007. Effects of alginate-derived oligosaccharide on seed germination and some physiological characters of seedlings in garden pea (Pisum sativum L.). Plant Physiology Communications 43 (6):1097–1100.
  • Malfait, T., and F. V. Cauwelaert. 1990. Preparative and analytical separation of oligosaccharides from κ-carrageenan. Journal of Chromatography A 504 (2):369–380. doi: 10.1016/S0021-9673(01)89540-6.
  • Ma, L. J., X. M. Li, N. Bu, and N. Li. 2010. An alginate-derived oligosaccharide enhanced wheat tolerance to cadmium stress. Plant Growth Regulation 62 (1):71–76. doi: 10.1007/s10725-010-9489-2.
  • Mao, S., T. Zhang, W. Sun, and X. Ren. 2012. The depolymerization of sodium alginate by oxidative degradation. Pharmaceutical Development and Technology 17 (6):763–769. doi: 10.3109/10837450.2011.583927.
  • Maruyama, H., H. Tamauchi, M. Hashimoto, and T. Nakano. 2003. Antitumor activity and immune response of Mekabu fucoidan extracted from Sporophyll of Undaria pinnatifida. In Vivo (Athens, Greece) 17 (3):245–249.
  • Matsubara, K., C. Xue, X. Zhao, M. Mori, T. Sugawara, and T. Hirata. 2005. Effects of middle molecular weight fucoidans on in vitro and ex vivo angiogenesis of endothelial cells. International Journal of Molecular Medicine 15 (4):695–699. doi: 10.3892/ijmm.15.4.695.
  • Mazumder, S., P. K. Ghosal, C. A. Pujol, M. a. J. Carlucci, E. B. Damonte, and B. Ray. 2002. Isolation, chemical investigation and antiviral activity of polysaccharides from Gracilaria corticata (Gracilariaceae, Rhodophyta). International Journal of Biological Macromolecules 31 (1–3):87–95. doi: 10.1016/S0141-8130(02)00070-3.
  • Mensi, F., J. Ksouri, E. Seale, M. S. Romdhane, and J. Fleurence. 2012. A statistical approach for optimization of R-phycoerythrin extraction from the red algae Gracilaria verrucosa by enzymatic hydrolysis using central composite design and desirability function. Journal of Applied Phycology 24 (4):915–926. doi: 10.1007/s10811-011-9712-1.
  • Miao, L. I., X. N. Zhang, M. A. Lian-Ju, and B. U. Ning. 2008. Effects of alginate derived oligosaccharide on the growth of bifidobacterium in vitro. Food Research Development 29 (11):16–19.
  • Montesano, R., C. Drevon, T. Kuroki, L. S. Vincent, S. Handleman, K. K. Sanford, D. DeFeo, and I. B. Weinstein. 1977. Test for malignant transformation of rat liver cells in culture: Cytology, growth in soft agar, and production of plasminogen activator. JNCI: Journal of the National Cancer Institute59 (6):1651–1658. doi: 10.1093/jnci/59.6.1651.
  • Mou, H., X. Jiang, and H. Guan. 2003. A κ-carrageenan derived oligosaccharide prepared by enzymatic degradation containing anti-tumor activity. Journal of Applied Phycology 15 (4):297–303.
  • Mou, H., X. Jiang, Z. Liu, and H. Guan. 2004. Structural analysis of kappa-carrageenan oligosaccharides released by carrageenase from marine Cytophaga sp. MCA-2. Journal of Food Biochemistry 28 (3):245–260. doi: 10.1111/j.1745-4514.2004.tb00068.x.
  • Mulloy, B., A. C. Ribeiro, A. P. Alves, R. P. Vieira, and P. a. S. Mourão. 1994. Sulfated fucans from echinoderms have a regular tetrasaccharide repeating unit defined by specific patterns of sulfation at the 0-2 and 0-4 positions. The Journal of Biological Chemistry 269 (35):22113–22123.
  • Murano, E., R. Toffanin, F. Zanetti, S. H. Knutsen, S. Paoletti, and R. Rizzo. 1992. Chemical and macromolecular characterisation of agar polymers from Gracilaria dura (C. Agardh) J. Agardh (Gracilariaceae, Rhodophyta). Carbohydrate Polymers 18 (3):171–178. doi: 10.1016/0144-8617(92)90061-T.
  • Natsume, M., Y. Kamo, M. Hirayama, and T. Adachi. 1994. Isolation and characterization of alginate-derived oligosaccharides with root growth-promoting activities. Carbohydrate Research 258 (6):187–197. doi: 10.1016/0008-6215(94)84085-7.
  • Niemelä, K., and E. Sjöström. 1985. Alkaline degradation of alginates to carboxylic acids. Carbohydrate Research 144 (2):241–249. doi: 10.1016/S0008-6215(00)90672-4.
  • Otterlei, M., K. Østgaard, G. Skjåk-Braek, O. Smidsrød, P. Soon-Shiong, and T. Espevik. 1991. Induction of cytokine production from human monocytes stimulated with alginate. Journal of Immunotherapy 10 (4):286–291. doi: 10.1097/00002371-199108000-00007.
  • Patankar, M. S., S. Oehninger, T. Barnett, R. L. Williams, and G. F. Clark. 1993. A revised structure for fucoidan may explain some of its biological activities. The Journal of Biological Chemistry 268 (29):21770–21776.
  • Penman, A., and D. A. Rees. 1973. Carrageenans. Part X. Synthesis of 3,6-di-O-methyl-D-galactose, a new sugar from the methylation analysis of polysaccharides related to ξ-carrageenan. Journal of the Chemical Society, Perkin Transactions 2:1288–1291.
  • Powell, L. C., A. Sowedan, S. Khan, C. J. Wright, K. Hawkins, E. Onsøyen, R. Myrvold, K. E. Hill, and D. W. Thomas. 2013. The effect of alginate oligosaccharides on the mechanical properties of Gram-negative biofilms. Biofouling 29 (4):413–421. doi: 10.1080/08927014.2013.777954.
  • Qiang Xu, C. X. J. C. J. o. M. D. 2002. Preparation of agar oligosaccharides by acid hydrolysis and determination of their antioxidative effect. Chinese Journal of Marine Drugs 21 (1):19–22.
  • Qiang, S., G. Qiang, X. W. Ping, L. Zandong, Z. T. Tong, and Y. Zhiping. 2015. Specific inhibitory effect of κ-carrageenan polysaccharide on swine pandemic 2009 H1N1 influenza virus. Plos One 10 (5):e0126577.
  • Qu, G., X. Liu, D. Wang, Y. Yuan, and L. Han. 2014. Isolation and characterization of fucoidans from five brown algae and evaluation of their antioxidant activity. Journal of Ocean University of China 13 (5):851–856. doi: 10.1007/s11802-014-2260-y.
  • Quemener, B., M. Lahaye, and F. Metro. 1995. Assessment of methanolysis for the determination of composite sugars of gelling carrageenans and agarose by HPLC. Carbohydrate Research 266 (1):53–64. doi: 10.1016/0008-6215(94)00249-F.
  • Ramos, P. E., P. Silva, M. M. Alario, L. M. Pastrana, J. A. Teixeira, M. A. Cerqueira, and A. A. Vicente. 2018. Effect of alginate molecular weight and M/G ratio in beads properties foreseeing the protection of probiotics. Food Hydrocolloids 77:8–16. doi: 10.1016/j.foodhyd.2017.08.031.
  • Religa, P., M. Kazi, J. Thyberg, Z. Gaciong, J. Swedenborg, and U. Hedin. 2000. Fucoidan inhibits smooth muscle cell proliferation and reduces mitogen-activated protein kinase activity. European Journal of Vascular and Endovascular Surgery 20 (5):419–426. doi: 10.1053/ejvs.2000.1220.
  • Ruiter, G. A. D., and B. Rudolph. 1997. Carrageenan biotechnology. Trends in Food Science & Technology 8 (12):389–395. doi: 10.1016/S0924-2244(97)01091-1.
  • Salomonsen, T., H. M. Jensen, F. H. Larsen, S. Steuernagel, and S. r. B. Engelsen. 2009. Direct quantification of M/G ratio from 13C CP-MAS NMR spectra of alginate powders by multivariate curve resolution. Carbohydrate Research 344 (15):2014–2022. doi: 10.1016/j.carres.2009.06.025.
  • Sen, M. 2011. Effects of molecular weight and ratio of guluronic acid to mannuronic acid on the antioxidant properties of sodium alginate fractions prepared by radiation-induced degradation. Applied Radiation and Isotopes: Including Data, Instrumentation and Methods for Use in Agriculture, Industry and Medicine 69 (1):126–129. doi: 10.1016/j.apradiso.2010.08.017.
  • Seungbeom, P., C. Kwangrok, K. Jaekwan, S. Kyungho, J. Youngmi, and L. Wonha. 2010. The differential effect of high and low molecular weight fucoidans on the severity of collagen-induced arthritis in mice. Phytotherapy Research 24 (9):1384–1391.
  • Shimokawa, T., S. Yoshida, T. Takeuchi, K. Murata, T. Ishii, and I. Kusakabe. 1996. Preparation of two series of oligo-guluronic acids from sodium alginate by acid hydrolysis and enzymatic degradation. Journal of the Agricultural Chemical Society of Japan 60 (9):1532–1534. doi: 10.1271/bbb.60.1532.
  • Shu, Z., X. Shi, D. Nie, and B. Guan. 2015. Low-molecular-weight fucoidan inhibits the viability and invasiveness and triggers apoptosis in IL-1β-treated human rheumatoid arthritis fibroblast synoviocytes. Inflammation 38 (5):1777–1786. doi: 10.1007/s10753-015-0155-8.
  • Son, E. H., E. Y. Moon, D. K. Rhee, and S. Pyo. 2001. Stimulation of various functions in murine peritoneal macrophages by high mannuronic acid-containing alginate (HMA) exposure in vivo. International Immunopharmacology 1 (1):147–154. doi: 10.1016/S1567-5769(00)00012-6.
  • Sun, J. H., J. H. Lee, E. J. Kim, H. J. Yang, Y. K. Chang, J. S. Park, and S. K. Hong. 2017. In vitro and in vivo investigation for biological activities of neoagarooligosaccharides prepared by hydrolyzing agar with β-agarase. Biotechnology and Bioprocess Engineering 22 (4):489–496. doi: 10.1007/s12257-017-0049-8.
  • Sun, T., H. N. Tao, D. X. Zhou, and M. Fang. 2011. Antioxidant activity of phthaloyl derivative of κ-carrageenan oligosaccharides. Natural Product Research Development 23:530–533.
  • Sun, Y., B. Yang, Y. Wu, Y. Liu, X. Gu, H. Zhang, C. Wang, H. Cao, L. Huang, and Z. Wang. 2015. Structural characterization and antioxidant activities of κ-carrageenan oligosaccharides degraded by different methods. Food Chemistry 178:311–318. doi: 10.1016/j.foodchem.2015.01.105.
  • Synytsya, A., D. J. Choi, R. Pohl, Y. S. Na, P. Capek, E. Lattová, T. Taubner, J. W. Choi, C. W. Lee, J. K. Park, et al. 2015. Structural features and anti-coagulant activity of the sulphated polysaccharide SPS-CF from a green alga capsosiphon fulvescens. Marine Biotechnology 17 (6):718–735. doi: 10.1007/s10126-015-9643-y.
  • Tadhani, M. B., V. H. Patel, and R. Subhash. 2007. In vitro antioxidant activities of Stevia rebaudiana leaves and callus. Journal of Food Composition and Analysis 20 (3–4):323–329. doi: 10.1016/j.jfca.2006.08.004.
  • Tajima, S., H. Inoue, A. Kawada, A. Ishibashi, H. Takahara, and N. Hiura. 1999. Alginate oligosaccharides modulate cell morphology, cell proliferation and collagen expression in human skin fibroblasts in vitro. Archives of Dermatological Research 291 (7–8):432–436. doi: 10.1007/s004030050434.
  • Tang, M. 2004. Anti-oxidation of agar oligosaccharides produced by agarase from a marine bacterium. Journal of Applied Phycology 16:333–340.
  • Tatsuji, E., S. Hiroaki, S. Takeshi, O. Haruo, S. Hitoshi, O. Kazuyori, and K. Ikunoshin. 2017. In vitro and in vivo investigation for biological activities of neoagarooligosaccharides prepared by hydrolyzing agar with β-agarase. Biotechnology and Bioprocess Engineering 22:1–3.
  • Tatyana, K., B. Natalya, S. Larisa, and P. Natalya. 2014. Fucoidan extracted from Fucus evanescens prevents endotoxin-induced damage in a mouse model of endotoxemia. Marine Drugs 12 (2):886–898.
  • Tondervik, A., G. Klinkenberg, O. A. Aarstad, F. Drablos, H. Ertesvag, T. E. Ellingsen, … H. Sletta. 2010. Isolation of mutant alginate lyases with cleavage specificity for di-guluronic acid linkages. Journal of Biological Chemistry 285 (46):35284–35292. doi: 10.1074/jbc.M110.162800.
  • Tondervik, A., H. Sletta, G. Klinkenberg, C. Emanuel, L. C. Powell, M. F. Pritchard, … K. E. Hill. 2014. Alginate oligosaccharides inhibit fungal cell growth and potentiate the activity of antifungals against candida and Aspergillus spp. PLoS One 9 (11):e112518. doi: 10.1371/journal.pone.0112518.
  • Trincone, A. 2014. Molecular fishing: Marine oligosaccharides. Frontiers in Marine Science 1 (26):1–5. doi: 10.3389/fmars.2014.00026.
  • Trincone, A. 2015. Short bioactive marine oligosaccharides: Diving into recent literature. Current Biotechnology 4 (3):212–222. doi: 10.2174/1574893610999150703112934.
  • Tusi, S. K., L. Khalaj, G. Ashabi, M. Kiaei, and F. Khodagholi. 2011. Alginate oligosaccharide protects against endoplasmic reticulum- and mitochondrial-mediated apoptotic cell death and oxidative stress. Biomaterials 32 (23):5438–5458. doi: 10.1016/j.biomaterials.2011.04.024.
  • Vera, J., J. Castro, A. Gonzalez, and A. Moenne. 2011. Seaweed polysaccharides and derived oligosaccharides stimulate defense responses and protection against pathogens in plants. Marine Drugs 9 (12):2514–2525. doi: 10.3390/md9122514.
  • Wan, J., J. Zhang, D. Chen, B. Yu, Z. Huang, X. Mao, P. Zheng, J. Yu, and J. He. 2018. Alginate oligosaccharide enhances intestinal integrity of weaned pigs through altering intestinal inflammatory responses and antioxidant status. Rsc Advances 8 (24):13482–13492. doi: 10.1039/C8RA01943F.
  • Wang, X., H. Chen, and X. Yan. 2011. Research on the mechanism of Agaro-oligosaccharides induced reactive oxygen related defense response against kidney bean (Phaseolus vulgaris L.). Chinese Journal of Biological Control 27 (2):254–259.
  • Wang, P., X. Jiang, Y. Jiang, H. Mou, and M. Li. 2011. Structure-function relationship of anti-ultraviolet radiation in series of marine derived characteristic oligosaccharides. Natural Product Research and Research 23 (5):874–877. doi: 10.1080/14786410701371215.
  • Wang, J., X. Jiang, H. Mou, and H. Guan. 2004. Anti-oxidation of agar oligosaccharides produced by agarase from a marine bacterium. Journal of Applied Phycology 16 (5):333–340. doi: 10.1023/B:JAPH.0000047944.40463.e6.
  • Wang, Y., B. Li, X. Zhao, and M. Piao. 2014. Isolation and characterization of a fucoidan-degrading bacterium from Laminaria japonica. Journal of Ocean University of China 13 (1):153–156. doi: 10.1007/s11802-014-2011-0.
  • Wang, J., H. Mou, X. Jiang, and H. Guan. 2005. Biological activities of a neutral water-soluble agar polysaccharide prepared by agarase degradation. High Technology Letters 11 (4):415–420.
  • Wang, W., P. Zhang, C. Hao, X.-E. Zhang, Z.-Q. Cui, and H.-S. Guan. 2011. In vitro inhibitory effect of carrageenan oligosaccharide on influenza A H1N1 virus. Antiviral Research 92 (2):237–246. doi: 10.1016/j.antiviral.2011.08.010.
  • Whiteley, M., M. G. Bangera, R. E. Bumgarner, M. R. Parsek, G. M. Teitzel, S. Lory, and E. P. Greenberg. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413 (6858):860–864. doi: 10.1038/35101627.
  • Wilson, A. J., and A. T. Critchiey. 1998. Studies on Gracilaria gracilis (Stackhouse) steentoft, Irvine and Farnham and Gracilaria aculeata (Hering) Papenfuss from Southern Africa. II. Agar production. South African Journal of Botany 64 (2):110–115. doi: 10.1016/S0254-6299(15)30843-7.
  • Wong, T. Y., L. A. Preston, and N. L. Schiller. 2000. Alginate lyase: Review of major sources and enzyme characteristics, structure-function analysis, biological roles, and applications. Annual Review of Microbiology 54 (1):289–340. doi: 10.1146/annurev.micro.54.1.289.
  • Xing, L., Zhu, C. Sun, W. Zhai, Y. Zhaoxin, L. I. Miao, and J. Standards. 2011. Determination of monosaccharides and uronic acids of Fucoidon by high performance liquid chromatography with pre-column derivatization. Chinese Fishery Quality 1 (1):64–69.
  • Xu, X.-Q., B.-M. Su, J.-S. Xie, R.-K. Li, J. Yang, J. Lin, and X.-Y. Ye. 2018. Preparation of bioactive neoagaroligosaccharides through hydrolysis of Gracilaria lemaneiformis agar: A comparative study. Food Chemistry 240 (1):330–337. doi: 10.1016/j.foodchem.2016.09.032.
  • Xu, X., X. Wu, Q. Wang, N. Cai, H. Zhang, Z. Jiang, M. Wan, and T. Oda. 2014. Immunomodulatory effects of alginate oligosaccharides on murine macrophage RAW264.7 cells and their structure-activity relationships. Journal of Agricultural and Food Chemistry 62 (14):3168–3176. doi: 10.1021/jf405633n.
  • Xu, L., Z. Yao, H. Wu, F. Wang, and S. Zhang. 2012. The immune regulation of κ-carrageenan oligosaccharide and its desulfated derivatives on LPS-activated microglial cells. Neurochemistry International 61 (5):689–696. doi: 10.1016/j.neuint.2012.06.019.
  • Yamamoto, Y., M. Kurachi, K. Yamaguchi, and T. Oda. 2007a. Induction of multiple cytokine secretion from RAW264.7 cells by alginate oligosaccharides. Bioscience, Biotechnology, and Biochemistry 71 (1):238–241. doi: 10.1271/bbb.60416.
  • Yamamoto, Y., M. Kurachi, K. Yamaguchi, and T. Oda. 2007b. Stimulation of multiple cytokine production in mice by alginate oligosaccharides following intraperitoneal administration. Carbohydrate Research 342 (8):1133–1137. doi: 10.1016/j.carres.2007.02.015.
  • Yang, Z., and Y. Fan. 2007. The structural characterization of the alginate derived oligo-mannuronates by different preparation methods. Chinese Journal of Biochemical Pharmaceutics (1):69–71.
  • Yang, L., P. Wang, H. Wang, Q. Li, H. Teng, Z. Liu, W. Yang, L. Hou, and X. Zou. 2013. Fucoidan derived from Undaria pinnatifida induces apoptosis in human hepatocellular carcinoma SMMC-7721 cells via the ROS-mediated mitochondrial pathway. Marine Drugs 11 (6):1961–1976. doi: 10.3390/md11061961.
  • Yao, Z., F. Wang, Z. Gao, L. Jin, and H. Wu. 2013. Characterization of a κ-Carrageenase from Marine Cellulophaga lytica strain N5-2 and analysis of its degradation products. International Journal of Molecular Sciences 14 (12):24592–24602. doi: 10.3390/ijms141224592.
  • Yao, Z. A., L. Xu, and H. G. Wu. 2014. Immunomodulatory function of κ-carrageenan oligosaccharides acting on LPS-activated microglial cells. Neurochemical Research 39 (2):333–343. doi: 10.1007/s11064-013-1228-4.
  • Yaqin, H. U., and M. Zhu. 2005. Study progress of carrageenans and their structure. Transaction of Oceanology (1):94–102.
  • Yoon, H. S., J. Y. Lee, S. M. Boo, and D. Bhattacharya. 2001. Phylogeny of Alariaceae, Laminariaceae, and Lessoniaceae (Phaeophyceae) based on plastid-encoded RuBisCo spacer and nuclear-encoded ITS sequence comparisons. Molecular Phylogenetics and Evolution 21 (2):231–243. doi: 10.1006/mpev.2001.1009.
  • Yoshida, T., A. Hirano, H. Wada, K. Takahashi, and M. Hattori. 2004. Alginic acid oligosaccharide suppresses Th2 development and IgE production by inducing IL-12 production. International Archives of Allergy and Immunology 133 (3):239–247. doi: 10.1159/000076830.
  • You, S. G., C. Yang, H. Lee, and B.-Y. Lee. 2010. Molecular characteristics of partially hydrolyzed fucoidans from sporophyll of Undaria Pinnatifida and their in vitro anticancer activity. Food Chemistry 119 (2):554–559. doi: 10.1016/j.foodchem.2009.06.054.
  • Yu, L., C. Xue, Y. Chang, X. Xu, L. Ge, G. Liu, and Y. Wang. 2014. Structure elucidation of fucoidan composed of a novel tetrafucose repeating unit from sea cucumber Thelenota ananas. Food Chemistry 146 (3):113–119. doi: 10.1016/j.foodchem.2013.09.033.
  • Yuan, H., J. Song, X. Li, N. Li, and J. Dai. 2006. Immunomodulation and antitumor activity of κ-carrageenan oligosaccharides. Cancer Letters 243 (2):228–234. doi: 10.1016/j.canlet.2005.11.032.
  • Yuan, H. M., J. M. Song, W. W. Zhang, X. G. Li, N. Li, and X. Gao. 2006. Antioxidant activity and cytoprotective effect of kappa-carrageenan oligosaccharides and their different derivatives. Bioorganic & Medicinal Chemistry Letters 16 (5):1329–1334. doi: 10.1016/j.bmcl.2005.11.057.
  • Yuan, H., W. Zhang, X. Li, X. Lü, N. Li, X. Gao, and J. Song. 2005. Preparation and in vitro antioxidant activity of κ-carrageenan oligosaccharides and their oversulfated, acetylated, and phosphorylated derivatives. Carbohydrate Research 340 (4):685–692. doi: 10.1016/j.carres.2004.12.026.
  • Zhang, Y. H., H. Liu, H. Yin, W. X. Wang, X. M. Zhao, and Y. G. Du. 2013. Nitric oxide mediates alginate oligosaccharides-induced root development in wheat (Triticum aestivum L.). Plant Physiology and Biochemistry 71:49–56.
  • Zhang, H. R., C. Y. Wang, B. Liu, Y. X. Wei, B. G. Wang, M. Y. Geng, and H. S. Guan. 2006. A method for preparation of saturated oligosaccharides from alginate. Chinese Journal of Marine Drugs 25 (3):1–6.
  • Zhang, Z., G. Yu, H. Guan, X. Zhao, Y. Du, and X. Jiang. 2004. Preparation and structure elucidation of alginate oligosaccharides degraded by alginate lyase from Vibro sp. 510. Carbohydrate Research 339 (8):1475–1481. doi: 10.1016/j.carres.2004.03.010.
  • Zhao, X., J. F. Wang, and C. H. Xue. 2011. The inhibitory effects of fucoidans from laminaria japonica on oxidation of human low-density lipoproteins. Advanced Materials Research 236–238:2067–2071. doi: 10.4028/www.scientific.net/AMR.236-238.2067.
  • Zhao, X., H. Xu, X. C. Q. Xu, J. C. L., Z. J. Lin. and H. 2002. Antioxidant abilities of agar oligosaccharides. Journal of Fishery Sciences of China 9 (3):280–282. doi: 10.3724/SP.J.1118.2017.16150.
  • Zhou, G., Y. Sun, H. Xin, Y. Zhang, Z. Li, and Z. Xu. 2004. In vivo antitumor and immunomodulation activities of different molecular weight lambda-carrageenans from Chondrus ocellatus. Pharmacological Research 50 (1):47–53. doi: 10.1016/j.phrs.2003.12.002.
  • Zhou, X.-X., J. Xu, and Y. T. Ding. 2014. Alginate-derived oligosaccharides product by alginate lyase and detection of the antioxidant activity. Food and Fermentation Industries 40 (2):116–120.
  • Zhu, B. W., L.-S.-X. Huang, H.-D. Tan, Y.-Q. Qin, Y.-G. Du, and H. Yin. 2015. Characterization of a new endo-type poly M-specific alginate lyase from Pseudomona ssp. Biotechnology Letters 37 (2):409–415. doi: 10.1007/s10529-014-1685-0.
  • Zhu, B. W., F. Hu, H. Yuan, Y. Sun, and Z. Yao. 2018. Biochemical characterization and degradation pattern of a unique pH-stable PolyM-specific alginate lyase from newly isolated serratia marcescens NJ-07. Marine Drugs 16 (4):129. doi: 10.3390/md16040129.
  • Zhu, B., C. Meijuan, Y. Heng, D. Yuguang, and N. Limin. 2016. Enzymatic hydrolysis of alginate to produce oligosaccharides by a new purified endo-type alginate lyase. Marine Drugs 14 (6):108. doi: 10.3390/md14060108.
  • Zhu, B., F. Ni, L. Ning, Y. Sun, and Z. Yao. 2018. Cloning and characterization of a new pH-stable alginate lyase with high salt tolerance from marine Vibrio sp. NJ-04. International Journal of Biological Macromolecules 115:1063–1070.
  • Zhu, B., F. Ni, L. Ning, Z. Yao, and Y. Du. 2018. Cloning and biochemical characterization of a novel κ-carrageenase from newly isolated marine bacterium Pedobacter hainanensis NJ-02. International Journal of Biological Macromolecules 108:1331–1338.
  • Zhu, B., F. Ni, Y. Sun, X. Zhu, H. Yin, Z. Yao, and Y. Du. 2018. Insight into carrageenases: Major review of sources, category, property, purification method, structure, and applications. Critical Reviews in Biotechnology 38 (8):1261–1276. doi: 10.1080/07388551.2018.1472550.
  • Zhu, B. W., Q. Xiong, F. Ni, Y. Sun, and Z. Yao. 2018. High-level expression and characterization of a new κ -carrageenase from marine bacterium Pedobacter hainanensis NJ-02. Letters in Applied Microbiology 66 (5):409–415. doi: 10.1111/lam.12865.
  • Zhu, N., and Z. Yao. 2009. Research progress on carrageenan oligosaccharides. Chemistry & Bioengineering 26 (10):9–12.
  • Zhu, B., and H. Yin. 2015. Alginate lyase: Review of major sources and classification, properties, structure-function analysis and applications. Bioengineered Bugs 6 (3):125–131. doi: 10.1080/21655979.2015.1030543.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.