Enhancing Immunity and Modulating Vaginal Microflora Against Candidal Vaginitis Through Nanoemulsion Supplemented with Porphyra Oligosaccharide as an Intravaginal Vaccine Adjuvant

References

• Pfaller MA, Diekema D. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007;20(1):133–163. doi:10.1128/CMR.00029-06
   PubMed Web of Science ®Google Scholar
• Aballéa S, Guelfucci F, Wagner J, et al. Subjective health status and health-related quality of life among women with recurrent vulvovaginal candidosis (RVVC) in Europe and the USA. Health Qual Life Outcomes. 2013;11(1):1–13. doi:10.1186/1477-7525-11-169
   PubMedGoogle Scholar
• Berkow EL, Lockhart SR. Fluconazole resistance in Candida species: a current perspective. Infect Drug Resist. 2017;10:237–245. doi:10.2147/IDR.S118892
   PubMed Web of Science ®Google Scholar
• Popp C, Hampe IA, Hertlein T, Ohlsen K, Rogers PD, Morschhäuser J. Competitive fitness of fluconazole-resistant clinical Candida albicans strains. Antimicrob Agents Chemother. 2017;61(7):e00584–00517. doi:10.1128/AAC.00584-17
   PubMed Web of Science ®Google Scholar
• Netea MG, Joosten LA, Van Der Meer JW, Kullberg B-J, Van De Veerdonk FL. Immune defence against Candida fungal infections. Nat Rev Immunol. 2015;15(10):630–642. doi:10.1038/nri3897
   PubMed Web of Science ®Google Scholar
• Medzhitov R, Janeway CA. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol. 1997;9(1):4–9. doi:10.1016/S0952-7915(97)80152-5
   PubMed Web of Science ®Google Scholar
• Pashine A, Valiante NM, Ulmer JB. Targeting the innate immune response with improved vaccine adjuvants. Nat Med. 2005;11(Suppl 4):S63–S68. doi:10.1038/nm1210
   PubMed Web of Science ®Google Scholar
• Lycke N. Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol. 2012;12(8):592–605. doi:10.1038/nri3251
   PubMed Web of Science ®Google Scholar
• Marasini N, Skwarczynski M, Toth I. Oral delivery of nanoparticle-based vaccines. Expert Rev Vaccines. 2014;13(11):1361–1376. doi:10.1586/14760584.2014.936852
   PubMed Web of Science ®Google Scholar
• Czerkinsky C, Holmgren J. Topical immunization strategies. Mucosal Immunol. 2010;3(6):545–555. doi:10.1038/mi.2010.55
   PubMed Web of Science ®Google Scholar
• Ramirez JEV, Sharpe LA, Peppas NA. Current state and challenges in developing oral vaccines. Adv Drug Deliv Rev. 2017;114:116–131. doi:10.1016/j.addr.2017.04.008
   PubMed Web of Science ®Google Scholar
• Black S. Safety and effectiveness of MF-59 adjuvanted influenza vaccines in children and adults. Vaccine. 2015;33:B3–B5. doi:10.1016/j.vaccine.2014.11.062
   PubMed Web of Science ®Google Scholar
• H-M H, Huang C-Y, Cheng Y-J, et al. Squalene nanoemulsion reinforces mucosal and immunological fingerprints following intravaginal delivery. Biomed Pharmacother. 2021;141:111799.
   PubMed Web of Science ®Google Scholar
• Cian RE, Fajardo MA, Alaiz M, Vioque J, González RJ, Drago SR. Chemical composition, nutritional and antioxidant properties of the red edible seaweed Porphyra columbina. Int J Food Sci Nutr. 2014;65(3):299–305. doi:10.3109/09637486.2013.854746
   PubMed Web of Science ®Google Scholar
• Yu P, Zhang Y. Separation and purification of Porphyra haitanensis polysaccharide and its preliminary structural characterization. Sep Sci Technol. 2017;52(11):1835–1842. doi:10.1080/01496395.2017.1296464
   Web of Science ®Google Scholar
• Wang Y, Hwang J-Y, H-b P, Yadav D, Oda T, Jin J-O. Porphyran isolated from Pyropia yezoensis inhibits lipopolysaccharide-induced activation of dendritic cells in mice. Carbohydr Polym. 2020;229:115457. doi:10.1016/j.carbpol.2019.115457
   PubMed Web of Science ®Google Scholar
• Wang Y, Hwang J, Yadav D, Oda T, Lee PC-W, Jin J-O. Inhibitory effect of porphyran on lipopolysaccharide-induced activation of human immune cells. Carbohydr Polym. 2020;232:115811. doi:10.1016/j.carbpol.2019.115811
   PubMed Web of Science ®Google Scholar
• Shi C, Pan T, Cao M, Liu Q, Zhang L, Liu G. Suppression of Th2 immune responses by the sulfated polysaccharide from Porphyra haitanensis in tropomyosin-sensitized mice. Int Immunopharmacol. 2015;24(2):211–218. doi:10.1016/j.intimp.2014.11.019
   PubMed Web of Science ®Google Scholar
• Osumi Y, Kawai M, Amano H, Noda H. Physiological activities of oligosaccharides derived from marine algae Porphyra yezoensis Porphyran. Fisher Sci. 2002;68(sup2):1441–1444. doi:10.2331/fishsci.68.sup2_1441
   Google Scholar
• Wu S-C, Kang S-K, Kazlowski B, C-j W, Pan C-L. Antivirus and prebiotic properties of seaweed-oligosaccharide-lysates derived from agarase AS-II. J Fish Soc Taiwan. 2012;39(1):11–21.
   Google Scholar
• Wei Y-J, Fang R-E, J-y O, Pan C-L, Huang C-H. Modulatory effects of Porphyra-derived polysaccharides, oligosaccharides and their mixture on antigen-specific immune responses in ovalbumin-sensitized mice. J Funct Foods. 2022;96:105209. doi:10.1016/j.jff.2022.105209
   Web of Science ®Google Scholar
• Esmaeili F, Rajabnejhad S, Partoazar AR, et al. Anti-inflammatory effects of eugenol nanoemulsion as a topical delivery system. Pharm Dev Technol. 2016;21(7):887–893. doi:10.3109/10837450.2015.1078353
   PubMed Web of Science ®Google Scholar
• Huang C-H, Huang C-Y, Huang M-H. Unsaturated squalene content in emulsion vaccine adjuvants plays a crucial role in ROS-mediated antigen uptake and cellular immunity. Mol Pharm. 2018;15(2):420–429. doi:10.1021/acs.molpharmaceut.7b00800
   PubMedGoogle Scholar
• Huang C-H, Lin Y-C, Jan T-R. Lactobacillus reuteri induces intestinal immune tolerance against food allergy in mice. J Funct Foods. 2017;31:44–51. doi:10.1016/j.jff.2017.01.034
   Web of Science ®Google Scholar
• Yano J, Fidel PL. Protocols for vaginal inoculation and sample collection in the experimental mouse model of Candida vaginitis. JoVE. 2011;58:e3382.
   Google Scholar
• Hebbar PB, Pai A, D S. Mycological and histological associations of Candida in oral mucosal lesions. J Oral Sci. 2013;55(2):157–160. doi:10.2334/josnusd.55.157
   PubMed Web of Science ®Google Scholar
• Sroka-Oleksiak A, Gosiewski T, Pabian W, et al. Next-Generation Sequencing as a tool to detect vaginal microbiota disturbances during pregnancy. Microorganisms. 2020;8(11):1813. doi:10.3390/microorganisms8111813
   PubMed Web of Science ®Google Scholar
• Wang L-J, Yang C-Y, Kuo H-C, Chou W-J, Tsai C-S, Lee S-Y. Effect of Bifidobacterium bifidum on clinical characteristics and gut microbiota in Attention-Deficit/Hyperactivity Disorder. J Personal Med. 2022;12(2):227. doi:10.3390/jpm12020227
   PubMed Web of Science ®Google Scholar
• Chee WJY, Chew SY, Than LTL. Vaginal microbiota and the potential of Lactobacillus derivatives in maintaining vaginal health. Microb Cell Fact. 2020;19(1):203. doi:10.1186/s12934-020-01464-4
   PubMed Web of Science ®Google Scholar
• Balakrishnan SN, Yamang H, Lorenz MC, Chew SY, Than LTL. Role of vaginal mucosa, host immunity and microbiota in vulvovaginal candidiasis. Pathogens. 2022;11(6):618. doi:10.3390/pathogens11060618
   PubMed Web of Science ®Google Scholar
• Faith DP, Minchin PR, Belbin L. Compositional dissimilarity as a robust measure of ecological distance. Vegetatio. 1987;69(1–3):57–68. doi:10.1007/BF00038687
   Google Scholar
• Gong G, Dang T, Fang J, et al. Preparation, structural characterization, and bioactivity of PHPD-IV-4 derived from Porphyra haitanensis. Food Chem. 2020;329:127042. doi:10.1016/j.foodchem.2020.127042
   PubMed Web of Science ®Google Scholar
• Isaka S, Cho K, Nakazono S, et al. Antioxidant and anti-inflammatory activities of porphyran isolated from discolored nori (Porphyra yezoensis). Int J Biol Macromol. 2015;74:68–75. doi:10.1016/j.ijbiomac.2014.11.043
   PubMed Web of Science ®Google Scholar
• Hou Y, Wang J, Simerly T, Jin W, Zhang H, Zhang Q. Hydrogen peroxide released from Pyropia yezoensis induced by oligo-porphyrans: mechanisms and effect. J Appl Phycol. 2015;27(4):1639–1649. doi:10.1007/s10811-014-0471-7
   Web of Science ®Google Scholar
• Wei YJ, Fang RE, Liu JS, et al. Influence of Porphyra-derived polysaccharides and oligosaccharides on attenuating food allergy and modulating enteric microflora in mice. Food Agric Immunol. 2023;34(1):2248419. doi:10.1080/09540105.2023.2248419
   Web of Science ®Google Scholar
• Hirano Y, Hattori M, Takahashi K. Interaction of porphyran with a hydrophobic surface and stabilization of liposomes. J Agric Food Chem. 2005;53(25):9800–9804. doi:10.1021/jf050793e
   PubMed Web of Science ®Google Scholar
• Xu X, Luo L, Liu C, McClements DJ. Utilization of anionic polysaccharides to improve the stability of rice glutelin emulsions: impact of polysaccharide type, pH, salt, and temperature. Food Hydrocoll. 2017;64:112–122. doi:10.1016/j.foodhyd.2016.11.005
   Web of Science ®Google Scholar
• Shao P, Feng J, Sun P, Xiang N, Lu B, Qiu D. Recent advances in improving stability of food emulsion by plant polysaccharides. Food Res Int. 2020;137:109376. doi:10.1016/j.foodres.2020.109376
   PubMed Web of Science ®Google Scholar
• Issara-Amphorn J, Dang CP, Saisorn W, Limbutara K, Leelahavanichkul A. Candida administration in bilateral nephrectomy mice elevates serum (1→ 3)-β-D-glucan that enhances systemic inflammation through energy augmentation in macrophages. Int J Mol Sci. 2021;22(9):5031. doi:10.3390/ijms22095031
   PubMed Web of Science ®Google Scholar
• Huang C-H, Huang C-Y, H-m H, et al. Nanoemulsion adjuvantation strategy of tumor-associated antigen therapy rephrases mucosal and immunotherapeutic signatures following intranasal vaccination. J Immunother Cancer. 2020;8(2):e001022. doi:10.1136/jitc-2020-001022
   PubMed Web of Science ®Google Scholar
• Lehtoranta L, Ala-Jaakkola R, Laitila A, Maukonen J. Healthy vaginal microbiota and influence of probiotics across the female life span. Front Microbiol. 2022;13:787.
   Web of Science ®Google Scholar
• Barfod KK, Roggenbuck M, Hansen LH, et al. The murine lung microbiome in relation to the intestinal and vaginal bacterial communities. BMC Microbiol. 2013;13(1):1–12. doi:10.1186/1471-2180-13-303
   PubMedGoogle Scholar
• Pavan Kumar J, Gomathi A, Vasconcelos V, Gothandam K. Bioactivity assessment of Indian origin—mangrove actinobacteria against Candida albicans. Mar Drugs. 2018;16(2):60. doi:10.3390/md16020060
   PubMed Web of Science ®Google Scholar
• Mendes TD, Borges WS, Rodrigues A, et al. Anti-Candida properties of urauchimycins from actinobacteria associated with Trachymyrmex ants. Biomed Res Int. 2013;2013:835081. doi:10.1155/2013/835081
   PubMed Web of Science ®Google Scholar
• Tortelli BA, Lewis WG, Allsworth JE, et al. Associations between the vaginal microbiome and Candida colonization in women of reproductive age. Am J Obstet Gynecol. 2020;222(5):471. doi:10.1016/j.ajog.2019.10.008
   Web of Science ®Google Scholar
• Sun Z, Ge X, Qiu B, et al. Vulvovaginal candidiasis and vaginal microflora interaction: microflora changes and probiotic therapy. Front Cell Infect Microbiol. 2023;13:1123026. doi:10.3389/fcimb.2023.1123026
   PubMed Web of Science ®Google Scholar
• McIntosh EDG. Development of vaccines against the sexually transmitted infections gonorrhoea, syphilis, Chlamydia, herpes simplex virus, human immunodeficiency virus and Zika virus. Therap Adv Vaccines Immunother. 2020;8:2515135520923887. doi:10.1177/2515135520923887
   Google Scholar
• Huang M, Zhang M, Zhu H, Du X, Wang J. Mucosal vaccine delivery: a focus on the breakthrough of specific barriers. Acta Pharm Sin B. 2022;12(9):3456–3474. doi:10.1016/j.apsb.2022.07.002
   PubMed Web of Science ®Google Scholar
• Vono M, Taccone M, Caccin P, et al. The adjuvant MF59 induces ATP release from muscle that potentiates response to vaccination. Proce Natl Acad Sci. 2013;110(52):21095–21100. doi:10.1073/pnas.1319784110
   PubMed Web of Science ®Google Scholar
• Vajdy M, Singh M, Kazzaz J, et al. Mucosal and systemic anti-HIV responses in rhesus macaques following combinations of intranasal and parenteral immunizations. AIDS Res Hum Retroviruses. 2004;20(11):1269–1281. doi:10.1089/aid.2004.20.1269
   PubMed Web of Science ®Google Scholar
• Johnson WT, Dorn NC, Ogbonna DA, Bottini N, Shah NJ. Lipid‐based regulators of immunity. Bioeng Transl Med. 2022;7(2):e10288. doi:10.1002/btm2.10288
   PubMed Web of Science ®Google Scholar
• Bakkari MA, Moni SS, Alshammari A, et al. Design, characterization, and immune augmentation of docosahexaenoic acid nanovesicles as a potential delivery system for recombinant HBsAg protein. Vaccines. 2022;10(6):954. doi:10.3390/vaccines10060954
   Web of Science ®Google Scholar
• Zhang L, Huang J, Chen X, et al. Self-assembly nanovaccine containing TLR7/8 agonist and STAT3 inhibitor enhances tumor immunotherapy by augmenting tumor-specific immune response. J Immunother Cancer. 2021;9(8):e003132. doi:10.1136/jitc-2021-003132
   PubMed Web of Science ®Google Scholar
• Sanina N. Vaccine adjuvants derived from marine organisms. Biomolecules. 2019;9(8):340. doi:10.3390/biom9080340
   PubMed Web of Science ®Google Scholar
• Kim S-Y, Joo H-G. Evaluation of adjuvant effects of fucoidan for improving vaccine efficacy. J Vet Sci. 2015;16(2):145–150. doi:10.4142/jvs.2015.16.2.145
   PubMed Web of Science ®Google Scholar