Characterization of the adjuvant activity of lipid extracts of Sarcopeltis skottsbergii and Iridea cordata associated with recombinant protein rCP01850 as an immunogen against caseous lymphadenitis
Tallyson Nogueira Barbosa; Mara Thais de Oliveira Silva; Rodrigo Barros de Pinho; Nicole Ramos Scholl; Cláudio Martin Pereira de Pereira; Andrés Mansilla; Odir Antonio Dellagostind and Sibele Borsuk
Abstract
Fatty acids from macroalgae display various promising biological activities, including immunomodulatory activity. Here, we characterized the adjuvant potential of macroalgae lipid extracts in a recombinant vaccine against caseous lymphadenitis. Female BALB/c mice were divided into seven groups and immunized twice (Days 0 and 21) with 0.9% saline solution (G1); rCP01850 + saponin (G2); rCP01850 + Sarcopeltis skottsbergii gametophyte phase (SFG) (G3); rCP01850 + Sarcopeltis skottsbergii cystocarp phase (SFC) (G4); rCP01850 + Iridaea cordata cystocarp phase (IFC) (G5); rCP01850 + Iridaea cordata tetrasporophyte phase (IFT) (G6); or rCP01850 alone (G7). Blood samples were collected for total IgG, IgG1, and IgG2a quantification. Moreover, another assay measured the IFN-γ and IL-10 levels produced by each experimental group through in vitro stimulation of splenocytes with rCP01850. Groups G5 and G6 showed the highest antibody levels after day 42. Groups G3, G4, G5, and G6 significantly increased IgG1 levels when compared to G1 and G7, with no statistical difference between G3, G4, G5, and G6. Meanwhile, G5 and G6 showed a significantly higher increase in IgG2a levels than the other groups on day 42. Groups G3, G4, G5, and G6 significantly produced IL-10, while G3 and G5 showed the highest levels of IFN-γ (p < 0.05). We concluded that the lipid extracts of Sarcopeltis skottsbergii and Iridaea cordata, when associated with rCP01850, elicited both humoral and cellular immune responses and are, therefore, promising candidates as adjuvants in vaccines against caseous lymphadenitis.
Keywords
References
Barbosa, J. S., Sabry, D. A., Silva, C. H. F., Gomes, D. L., Santana-Filho, A. P., Sassaki, G. L., & Rocha, H. A. O. (2020). Immunostimulatory effect of sulfated galactans from the green seaweed Caulerpa cupressoides var. flabellata. Marine Drugs, 18(5), 234. http:// dx.doi.org/10.3390/md18050234. PMid:32365741.
Barbosa, T. N., Silva, M. T. O., Sena-Lopes, Â., Kremer, F. S., Sousa, F. S. S., Seixas, F. K., Collares, T. V., Pereira, C. M. P., & Borsuk, S. (2023). Bioprospection of the trichomonacidal activity of lipid extracts derived from marine macroalgae Gigartina skottsbergii. PLoS One, 18(5), e0285426. http://dx.doi.org/10.1371/journal. pone.0285426. PMid:37155662.
Bezerra, F. S. B., Rezende, A. F. S., Silva, M. T. O., Sena-Lopes, Â., Roesch-Ely, M., Henriques, J. A. P., Padilha, F. F., Azevedo, V. A. C., Portela, R. W. D., Seixas, F. K., Collares, T. V., Savegnago, L., & Borsuk, S. (2020). The combination of Brazilian red propolis and recombinant protein rCP01850 in the immunoprophylaxis of Corynebacterium pseudotuberculosis infection in mice. Microbial Pathogenesis, 149, 104354. http://dx.doi.org/10.1016/j. micpath.2020.104354. PMid:32569789.
Bezerra, F. S. B., Silva, M. T. O., Rezende, A. F. S., Lopes, A. S., Pinho, R. B., Seixas, F. K., Collares, T. V., Portela, R. W. D., Azevedo, V. A. C., & Borsuk, S. (2021). Saponin-adjuvanted recombinant vaccines containing rCP00660, rCP09720 or rCP01850 proteins against Corynebacterium pseudotuberculosis infection in mice. Vaccine, 39(18), 2568-2574. http://dx.doi.org/10.1016/j. vaccine.2021.03.062. PMid:33814234.
Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8), 911-917. http://dx.doi.org/10.1139/ o59-099. PMid:13671378. Charerntantanakul, W. (2020). Adjuvants for swine vaccines: Mechanisms of actions and adjuvant effects. Vaccine, 38(43), 6659-6681. http://dx.doi.org/10.1016/j.vaccine.2020.08.054. PMid:32888738.
Chiboub, O., Sifaoui, I., Lorenzo-Morales, J., Abderrabba, M., Mejri, M., Fernández, J. J., Piñero, J. E., & Díaz-Marrero, A. R. (2019). Spiralyde A, an antikinetoplastid dolabellane from the brown alga Dictyota spiralis. Marine Drugs, 17(3), 192. http://dx.doi. org/10.3390/md17030192. PMid:30934651.
Coolen, A.-L., Lacroix, C., Mercier-Gouy, P., Delaune, E., Monge, C., Exposito, J.-Y., & Verrier, B. (2019). Poly(lactic acid) nanoparticles and cell-penetrating peptide potentiate mRNAbased vaccine expression in dendritic cells triggering their activation. Biomaterials, 195, 23-37. http://dx.doi.org/10.1016/j. biomaterials.2018.12.019. PMid:30610991.
Gao, Y., Lu, J., Zeng, C., Yang, J., Huang, B., Zhang, N., Li, L., & Fu, X. (2020). IL-10 suppresses IFN-γ-mediated signaling in lung adenocarcinoma. Clinical and Experimental Medicine, 20(3), 449-459. http://dx.doi.org/10.1007/s10238-020-00626-3. PMid:32306136.
Gutiérrez, S., Svahn, S. L., & Johansson, M. E. (2019). Effects of omega-3 fatty acids on immune cells. International Journal of Molecular Sciences, 20(20), 5028. http://dx.doi.org/10.3390/ ijms20205028. PMid:31614433.
Jin, Y., Li, P., & Wang, F. (2018). β-glucans as potential immunoadjuvants: A review on the adjuvanticity, structure-activity relationship and receptor recognition properties. Vaccine, 36(35), 5235-5244. http://dx.doi.org/10.1016/j.vaccine.2018.07.038. PMid:30049632.
Jorgovanovic, D., Song, M., Wang, L., & Zhang, Y. (2020). Roles of IFN-γin tumor progression and regression: A review. Biomarker Research, 8(1), 49. http://dx.doi.org/10.1186/s40364-020- 00228-x. PMid:33005420.
Kak, G., Raza, M., & Tiwari, B. K. (2018). Interferon-gamma (IFN-γ): Exploring its implications in infectious diseases. Biomolecular Concepts, 9(1), 64-79. http://dx.doi.org/10.1515/bmc-2018- 0007. PMid:29856726.
Leal, K. S., Silva, M. T. O., Rezende, A. F. S., Bezerra, F. S. B., Begnini, K., Seixas, F., Collares, T., Dellagostin, O., Portela, R. W., Azevedo, V. A. C., & Borsuk, S. (2018). Recombinant M. bovis BCG expressing the PLD protein promotes survival in mice challenged with a C. pseudotuberculosis virulent strain. Vaccine, 36(25), 3578-3583. http://dx.doi.org/10.1016/j.vaccine.2018.05.049. PMid:29759378.
Martins, R. M., Nedel, F., Guimarães, V. B. S., Silva, A. F., Colepicolo, P., Pereira, C. M. P., & Lund, R. G. (2018). Macroalgae extracts from Antarctica have antimicrobial and anticancer potential. Frontiers in Microbiology, 9, 412. http://dx.doi.org/10.3389/ fmicb.2018.00412. PMid:29568291.
Miles, E. A., Childs, C. E., & Calder, P. C. (2021). Long-chain polyunsaturated fatty acids (LCPUFAs) and the developing immune system: A narrative review. Nutrients, 13(1), 247. http://dx.doi. org/10.3390/nu13010247. PMid:33467123.
Moss, C. W., Lambert, M. A., & Merwin, W. H. (1974). Comparison of rapid methods for analysis of bacterial fatty acids. Applied Microbiology, 28(1), 80-85. http://dx.doi.org/10.1128/ am.28.1.80-85.1974. PMid:4844271.
Nazarizadeh, A., Staudacher, A. H., Wittwer, N. L., Turnbull, T., Brown, M. P., & Kempson, I. (2022). Aluminium nanoparticles as efficient adjuvants compared to their microparticle counterparts: Current progress and perspectives. International Journal of Molecular Sciences, 23(9), 4707. http://dx.doi.org/10.3390/ ijms23094707. PMid:35563097.
Radzikowska, A. O. R. U., Rinaldi, A. O., Sözener, Z. Ç., Karaguzel, D., Wojcik, M., Cypryk, K., Akdis, M., Akdis, C. Z., & Sokolowska, M. (2019). The influence of dietary fatty acids on immune responses. Nutrients, 11(12), 2990. http://dx.doi.org/10.3390/ nu11122990. PMid:31817726.
Rezende, A. F. S., Brum, A. A., Bezerra, F. S. B., Braite, D. C., Sá, G. L., Thurow, H. S., Seixas, F. K., Azevedo, V. A. C., Portela, R. W., & Borsuk, S. (2020). Assessment of the acid phosphatase CP01850 from Corynebacterium pseudotuberculosis in DNA and subunit vaccine formulations against caseous lymphadenitis. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 72(1), 199-207. http://dx.doi.org/10.1590/1678-4162-10790.
Rezende, A. F. S., Brum, A. A., Reis, C. G., Angelo, H. R., Leal, K. S., Silva, M. T. O., Simionatto, S., Azevedo, V., Santos, A., Portela, R. W., Dellagostin, O., & Borsuk, S. (2016). In silico identification of Corynebacterium pseudotuberculosis antigenic targets and application in immunodiagnosis. Journal of Medical Microbiology, 65(6), 521-529. http://dx.doi.org/10.1099/jmm.0.000263. PMid:27071381.
Saadaoui, I., Rasheed, R., Abdulrahman, N., Bounnit, T., Cherif, M., Al Jabri, H., & Mraiche, F. (2020). Algae-derived bioactive compounds with anti-lung cancer potential. Marine Drugs, 18(4), 197. http://dx.doi.org/10.3390/md18040197. PMid:32276401.
Sena-Lopes, Â., Bezerra, F. S. B., Neves, R. N., Pinho, R. B., Silva, M. T. O., Savegnago, L., Collares, T., Seixas, F., Begnini, K., Henriques, J. A. P., Ely, M. R., Rufatto, L. C., Moura, S., Barcellos, T., Padilha, F., Dellagostin, O., & Borsuk, S. (2018). Chemical composition, immunostimulatory, cytotoxic and antiparasitic activities of the essential oil from Brazilian red propolis. PLoS One, 13(2), e0191797. http://dx.doi.org/10.1371/journal. pone.0191797. PMid:29390009.
Shakoor, H., Feehan, J., Al Dhaheri, A. S., Ali, H. I., Platat, C., Ismail, L. C., Apostolopoulos, V., & Stojanovska, L. (2021). Immune-boosting role of vitamins D, C, E, zinc, selenium and omega-3 fatty acids: Could they help against COVID-19? Maturitas, 143, 1-9. http://dx.doi.org/10.1016/j.maturitas.2020.08.003. PMid:33308613.
Silva, M. T. O., Pinho, R. B., Fonseca, B. R., Bezerra, F. S. B., Sousa, F. S. S., Seixas, F. K., Collares, T., Nascimento, R. J. M., Portela, R. W., Azevedo, V. A. C., & Borsuk, S. (2020). NanH and PknG putative virulence factors as a recombinant subunit immunogen against Corynebacterium pseudotuberculosis infection in mice. Vaccine, 38(51), 8099-8106. http://dx.doi.org/10.1016/j. vaccine.2020.11.010. PMid:33190945.
Sobrinho Santos, E. M., Almeida, A. C., Santos, H. O., Cangussu, A. S. R., Almeida, D. A., & Costa, K. S. (2018). Leader gene of Corynebacterium pseudotuberculosis may be useful in vaccines against caseous lymphadenitis of goats: A bioinformatics approach. The Journal of Veterinary Medical Science, 80(8), 1317-1324. http://dx.doi.org/10.1292/jvms.16-0581. PMid:29937460.
Sting, R., Geiger, C., Rietschel, W., Blazey, B., Schwabe, I., Rau, J., & Schneider‐Bühl, L. (2022). Corynebacterium pseudotuberculosis infections in alpacas (Vicugna pacos). Animals, 12(13), 1612. http://dx.doi.org/10.3390/ani12131612. PMid:35804511.
Tregoning, J. S., Russell, R. F., & Kinnear, E. (2018). Adjuvanted influenza vaccines. Human Vaccines & Immunotherapeutics, 14(3), 550-564. http://dx.doi.org/10.1080/21645515.2017.141 5684. PMid:29232151.
Wei, H.-X., Wang, B., & Li, B. (2020). IL-10 and IL-22 in mucosal immunity: Driving protection and pathology. Frontiers in Immunology, 11, 1315. http://dx.doi.org/10.3389/ fimmu.2020.01315. PMid:32670290.
Yue, T., Xiong, K., Deng, J., Hu, W., Tan, T., Li, S., Yang, T., & Xiao, T. (2022). Meta-analysis of omega-3 polyunsaturated fatty acids on immune functions and nutritional status of patients with colorectal cancer. Frontiers in Nutrition, 9, 945590. http:// dx.doi.org/10.3389/fnut.2022.945590. PMid:36479293. Zhou, X., Zhu, X., Li, C., Li, Y., Ye, Z., Shapiro, V. S., Copland III, J. A., Hitosugi, T., Bernlohr, D. A., & Sun, H. Z. J. (2021). Stearoyl- CoA Desaturase-Mediated Monounsaturated Fatty Acid Availability Supports Humoral Immunity. Physiology & Behavior, 176(1), 139-148. http://dx.doi.org/10.1016/j.celrep.2020.108601. Stearoyl-CoA.
Submitted date:
08/02/2023
Accepted date:
10/03/2023
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