Cancer immunotherapy using a polysaccharide from Codium fragile in a murine model

References

• Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J clin oncol. 2015;33:1974–1982. doi: 10.1200/JCO.2014.59.4358.
   Web of Science ®Google Scholar
• Kyi C, Postow MA. Immune checkpoint inhibitor combinations in solid tumors: opportunities and challenges. Immunotherapy. 2016;8:821–11. doi:10.2217/imt-2016-0002.
   PubMed Web of Science ®Google Scholar
• Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348:56–61. doi:10.1126/science.aaa8172.
   PubMed Web of Science ®Google Scholar
• Neelapu SS, Tummala S, Kebriaei P, Wierda W, Gutierrez C, Locke FL, Komanduri KV, Lin Y, Jain N, Daver N, et al. Chimeric antigen receptor T-cell therapy - assessment and management of toxicities. Nat Rev Clin Oncol. 2018;15:47–62. doi: 10.1038/nrclinonc.2017.148.
   Web of Science ®Google Scholar
• Xu L, Kwak M, Zhang W, Zeng L, Lee PC, Jin JO. Rehmannia glutinosa polysaccharide induces toll-like receptor 4 dependent spleen dendritic cell maturation and anti-cancer immunity. Oncoimmunology. 2017;6:e1325981. doi:10.1080/2162402X.2017.1325981.
   PubMed Web of Science ®Google Scholar
• Miconnet I, Coste I, Beermann F, Haeuw JF, Cerottini JC, Bonnefoy JY, Romero P, Renno T. Cancer vaccine design: a novel bacterial adjuvant for peptide-specific CTL induction. J Immunol. 2001;166:4612–4619. doi:10.4049/jimmunol.166.7.4612.
   PubMed Web of Science ®Google Scholar
• Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392:245–252. doi:10.1038/32588.
   PubMed Web of Science ®Google Scholar
• Naik SH, Proietto AI, Wilson NS, Dakic A, Schnorrer P, Fuchsberger M, Lahoud MH, O’Keeffe M, Shao QX, Chen WF, et al. Cutting edge: generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J Immunol. 2005;174:6592–6597. doi:10.4049/jimmunol.174.11.6592.
   PubMed Web of Science ®Google Scholar
• Schnorrer P, Behrens GM, Wilson NS, Pooley JL, Smith CM, El-Sukkari D, Davey G, Kupresanin F, Li M, Maraskovsky E, et al. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc Natl Acad Sci U S A. 2006;103:10729–10734. doi:10.1073/pnas.0601956103.
   PubMed Web of Science ®Google Scholar
• Pooley JL, Heath WR, Shortman K. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J Immunol. 2001;166:5327–5330. doi:10.4049/jimmunol.166.9.5327.
   PubMed Web of Science ®Google Scholar
• Jongbloed SL, Kassianos AJ, McDonald KJ, Clark GJ, Ju X, Angel CE, Chen CJ, Dunbar PR, Wadley RB, Jeet V, et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med. 2010;207:1247–1260. doi:10.1084/jem.20092140.
   PubMed Web of Science ®Google Scholar
• Tabarsa M, Karnjanapratum S, Cho M, Kim J-K, You S. Molecular characteristics and biological activities of anionic macromolecules from Codium fragile. Int J Biol Macromol. 2013;59:1–12.
   Google Scholar
• Tabarsa M, You S, Dabaghian EH, Surayot U. Water-soluble polysaccharides from Ulva intestinalis: molecular properties, structural elucidation and immunomodulatory activities. J Food Drug Anal. 2018;26:599–608. doi:10.1016/j.jfda.2017.07.016.
   PubMed Web of Science ®Google Scholar
• Cui W, Joshi NS, Liu Y, Meng H, Kleinstein SH, Kaech SM. TLR4 ligands lipopolysaccharide and monophosphoryl lipid a differentially regulate effector and memory CD8+ T cell differentiation. J Immunol. 2014;192:4221–4232. doi:10.4049/jimmunol.1302569.
   PubMed Web of Science ®Google Scholar
• Zhang W, Xu L, Park H-B, Hwang J, Kwak M, Lee PC, Liang G, Zhang X, Xu J, Jin J-O. Escherichia coli adhesion portion FimH functions as an adjuvant for cancer immunotherapy. Nat Commun. 2020;11:1–14. doi:10.1038/s41467-019-13993-7.
   PubMed Web of Science ®Google Scholar
• Kool M, Soullié T, van Nimwegen M, Willart MA, Muskens F, Jung S, Hoogsteden HC, Hammad H, Lambrecht BN. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med. 2008;205:869–882. doi:10.1084/jem.20071087.
   PubMed Web of Science ®Google Scholar
• Kajiwara Y, Schiff T, Voloudakis G, Sosa MAG, Elder G, Bozdagi O, Buxbaum JD. A critical role for human caspase-4 in endotoxin sensitivity. J Immunol. 2014;193:335–343. doi:10.4049/jimmunol.1303424.
   PubMed Web of Science ®Google Scholar
• Meredith TC, Aggarwal P, Mamat U, Lindner B, Woodard RW. Redefining the requisite lipopolysaccharide structure in Escherichia coli. ACS Chem Biol. 2006;1:33–42. doi:10.1021/cb0500015.
   PubMed Web of Science ®Google Scholar
• Rhee SH. Lipopolysaccharide: basic biochemistry, intracellular signaling, and physiological impacts in the gut. Intestinal Res. 2014;12:90–95. doi:10.5217/ir.2014.12.2.90.
   PubMedGoogle Scholar
• Coffman RL, Sher A, Seder RA. Vaccine adjuvants: putting innate immunity to work. Immunity. 2010;33:492–503. doi:10.1016/j.immuni.2010.10.002.
   PubMed Web of Science ®Google Scholar
• Zhang W, Okimura T, Xu L, Zhang L, Oda T, Kwak M, Yu Q, Jin JO. Ascophyllan functions as an adjuvant to promote anti-cancer effect by dendritic cell activation. Oncotarget. 2016;7:19284–19298. doi:10.18632/oncotarget.8200.
   PubMedGoogle Scholar
• Ale MT, Meyer AS. Fucoidans from brown seaweeds: an update on structures, extraction techniques and use of enzymes as tools for structural elucidation. RSC Adv. 2013;3:8131–8141. doi:10.1039/C3RA23373A.
   Web of Science ®Google Scholar
• Zaharoff DA, Rogers CJ, Hance KW, Schlom J, Greiner JWJV. Chitosan solution enhances both humoral and cell-mediated immune responses to subcutaneous vaccination. Vaccine. 2007;25:2085–2094.
   Google Scholar
• Zhang W, Du JY, Jiang Z, Okimura T, Oda T, Yu Q, Jin JO. Ascophyllan purified from Ascophyllum nodosum induces Th1 and Tc1 immune responses by promoting dendritic cell maturation. Mar Drugs. 2014;12:4148–4164. doi:10.3390/md12074148.
   PubMed Web of Science ®Google Scholar
• Xu L, Kwak M, Zhang W, Lee PC, Jin JO. Time-dependent effect of E. coli LPS in spleen DC activation in vivo: alteration of numbers, expression of co-stimulatory molecules, production of pro-inflammatory cytokines, and presentation of antigens. Mol Immunol. 2017;85:205–213. doi:10.1016/j.molimm.2017.02.017.
   PubMed Web of Science ®Google Scholar
• Shang N, Figini M, Shangguan J, Wang B, Sun C, Pan L, Ma Q, Zhang Z. Dendritic cells based immunotherapy. Am J Cancer Res. 2017;7:2091–2102.
   PubMed Web of Science ®Google Scholar
• Cohn L, Delamarre L. Dendritic cell-targeted vaccines. Front Immunol. 2014;5:255. doi:10.3389/fimmu.2014.00255.
   PubMed Web of Science ®Google Scholar
• Wilkinson RW, Leishman AJ. Further advances in cancer immunotherapy: going beyond checkpoint blockade. Front Immunol. 2018;9:1082. doi:10.3389/fimmu.2018.01082.
   PubMed Web of Science ®Google Scholar
• Wei SC, Duffy CR, Allison JP. Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov. 2018;8:1069–1086. doi:10.1158/2159-8290.CD-18-0367.
   PubMed Web of Science ®Google Scholar
• Sato-Kaneko F, Yao S, Ahmadi A, Zhang SS, Hosoya T, Kaneda MM, Varner JA, Pu M, Messer KS, Guiducci C, et al. Combination immunotherapy with TLR agonists and checkpoint inhibitors suppresses head and neck cancer. JCI Insight. 2017;2. doi:10.1172/jci.insight.93397.
   PubMed Web of Science ®Google Scholar
• Zhang W, Oda T, Yu Q, Jin J-O. Fucoidan from Macrocystis pyrifera has powerful immune-modulatory effects compared to three other fucoidans. Mar Drugs. 2015;13:1084–1104. doi:10.3390/md13031084.
   PubMed Web of Science ®Google Scholar
• Senthilkumar K, Kim S-K. Anticancer effects of fucoidan. Adv Food Nutr Res. 2014;72:195–213. doi: 10.1016/B978-0-12-800269-8.00011-7.
   Google Scholar
• Jin J-O, Zhang W, Du J-Y, Wong K-W, Oda T, Yu Q. Fucoidan can function as an adjuvant in vivo to enhance dendritic cell maturation and function and promote antigen-specific T cell immune responses. PLoS One. 2014;9:e99396. doi:10.1371/journal.pone.0099396.
   PubMed Web of Science ®Google Scholar
• Li B, Lu F, Wei X, Zhao R. Fucoidan: structure and bioactivity. Molecules. 2008;13:1671–1695.
   PubMed Web of Science ®Google Scholar
• Ahmed TA, Aljaeid BM. Preparation, characterization, and potential application of chitosan, chitosan derivatives, and chitosan metal nanoparticles in pharmaceutical drug delivery. Drug Des Devel Ther. 2016;10:483–507. doi:10.2147/DDDT.S99651.
   PubMed Web of Science ®Google Scholar
• Mohammed MA, Syeda JTM, Wasan KM, Wasan EK. An overview of chitosan nanoparticles and its application in non-parenteral drug delivery. Pharmaceutics. 2017;9:53. doi:10.3390/pharmaceutics9040053.
   PubMed Web of Science ®Google Scholar
• Surayot U, You S. Structural effects of sulfated polysaccharides from Codium fragile on NK cell activation and cytotoxicity. Int J Biol Macromol. 2017;98:117–124. doi:10.1016/j.ijbiomac.2017.01.108.
   PubMed Web of Science ®Google Scholar
• You S, Yang C, Lee H, Lee B-Y. Molecular characteristics of partially hydrolyzed fucoidans from sporophyll of Undaria Pinnatifida and their in vitro anticancer activity. Food Chem. 2010;119:554–559. doi:10.1016/j.foodchem.2009.06.054.
   Web of Science ®Google Scholar
• Tabarsa M, Park G-M, Shin I-S, Lee E, Kim J-K, You SJMB. Structure-activity relationships of sulfated glycoproteins from Codium fragile on nitric oxide releasing capacity from RAW264. 7 cells. Mar Biotechnol. 2015;17:266–276.
   Google Scholar
• Xu L, Zhang W, Park HB, Kwak M, Oh J, Lee PCW, Jin JO. Indocyanine green and poly I:C containing thermo-responsive liposomes used in immune-photothermal therapy prevent cancer growth and metastasis. J Immunother Cancer. 2019;7:220. doi:10.1186/s40425-019-0702-1.
   PubMed Web of Science ®Google Scholar
• Dubensky TW Jr, Reed SG. Adjuvants for cancer vaccines, seminars in immunology. Semin Immunol. 2010 Jun;22(3):155–161. doi: 10.1016/j.smim.2010.04.007.
   Google Scholar
• Ebensen T, Delandre S, Prochnow B, Guzman CA, Schulze K. The combination vaccine adjuvant system alum/c-di-AMP results in quantitative and qualitative enhanced immune responses post immunization. Front Cell Infect Microbiol. 2019;9:31. doi:10.3389/fcimb.2019.00031.
   PubMed Web of Science ®Google Scholar
• Kool M, Fierens K, Lambrecht BN. Alum adjuvant: some of the tricks of the oldest adjuvant. J Med Microbiol. 2012;61:927–934. doi:10.1099/jmm.0.038943-0.
   PubMed Web of Science ®Google Scholar
• Mata-Haro V, Cekic C, Martin M, Chilton PM, Casella CR, Mitchell TC. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science. 2007;316:1628–1632. doi:10.1126/science.1138963.
   PubMed Web of Science ®Google Scholar
• Casella CR, Mitchell TC. Putting endotoxin to work for us: monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cell Mol Life Sci. 2008;65:3231. doi:10.1007/s00018-008-8228-6.
   PubMed Web of Science ®Google Scholar
• Rothenfusser S, Tuma E, Endres S, Hartmann G. Plasmacytoid dendritic cells: the key to CpG. Hum Immunol. 2002;63:1111–1119. doi:10.1016/S0198-8859(02)00749-8.
   PubMed Web of Science ®Google Scholar
• Mo JH, Chung YJ, Hayashi T, Lee J, Raz E. The role of plasmacytoid and myeloid dendritic cells in induction of asthma in a mouse model and the effect of a TLR9 agonist on dendritic cells. Allergy Asthma Immunol Res. 2011;3:199–204. doi:10.4168/aair.2011.3.3.199.
   PubMed Web of Science ®Google Scholar
• Behrens EM, Sriram U, Shivers DK, Gallucci M, Ma Z, Finkel TH, Gallucci S. Complement receptor 3 ligation of dendritic cells suppresses their stimulatory capacity. J Immunol. 2007;178:6268–6279. doi:10.4049/jimmunol.178.10.6268.
   PubMed Web of Science ®Google Scholar
• Capasso A, Lang J, Pitts TM, Jordan KR, Lieu CH, Davis SL, Diamond JR, Kopetz S, Barbee J, Peterson J, et al. Characterization of immune responses to anti-PD-1 mono and combination immunotherapy in hematopoietic humanized mice implanted with tumor xenografts. J Immunother Cancer. 2019;7:37. doi:10.1186/s40425-019-0518-z.
   PubMed Web of Science ®Google Scholar