Generic placeholder image

Protein & Peptide Letters


ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

The Roles of Bursal Nonapeptide (BP9) on AIV Vaccine Immune Response in Chick Immunization and on Avian Immature B Cell

Author(s): Yang Zheng, Man M. Zong, Bo Y. Chen, Xiao H. Zhou, Zi N. Liu, Guang F. Zhou, Pu Y. Chen and Xiu L. Feng*

Volume 26 , Issue 12 , 2019

Page: [940 - 948] Pages: 9

DOI: 10.2174/0929866526666190730101455

Price: $65


Background: Bursa of Fabricius plays the vital functions on B cell development and antibody production in poultry. The bursal-derived peptide plays the essential roles on avian immature B cell development.

Objectives: Here we explored the functions of the recently reported bursal nonapeptide (BP9) on the antibody production and the molecular basis of BP9 on avian immature B cell.

Methods: Chicken were twice immunized with Avian Influenza Virus (AIV) inactivated vaccine plus with BP9 at three dosages, respectively. On two weeks after the second immunization, sera samples were collected from all experimental groups to measure AIV-specific Agglutination Inhibition (HI) antibody titers. Also, on 7th day after the second immunization, spleen lymphocytes were isolated from the immunized chicken to detect the lymphocyte viabilities. DT40 cells were treated with BP9 from 0.02 to 2 μg/mL for 4 and 20h to detect sIgM mRNA levels, and total RNAs from BP9-treated DT40 cells were collected to investigate the gene expression profiles of DT40 cells, and to analyze the enriched pathways and functional biological processes. Finally, nine gene expressions were validated with quantitative PCR (qPCR).

Results: Our investigation proved the strong regulatory roles of BP9 on AIV-specific HI antibody titers and lymphocyte viabilities. BP9 promoted sIgM mRNA levels in DT40 cells, and upregulated 598 gene expressions and downregulated 395 gene expressions in DT40 cells with 0.2μg/mL BP9 treatment. Moreover, our findings verified the significantly enriched six pathways and various the biological functional processes of BP9 on avian immature B cell. Also, we found eight signaling pathways in the enriched biological processes of BP9-treated DT40 cells, and the expressions of nine selected genes with qPCR were identical to that of microarray data.

Conclusion: BP9 promoted the antibody production in the 21-old-day chicken immunization, and stimulated the sIgM expression in DT40 cells. Furthermore, we analyzed the gene expression profile and immune-related biological processes of DT40 cells treated with BP9, which provided some new insights into the mechanism on immature B cell development, and provided important references for adjuvant development on vaccine improvement and clinical application.

Keywords: Bursal nonapeptide (BP9), AIV inactivated vaccine, antibody response, DT40 cells, enriched pathways, functional biological processes.

Graphical Abstract
Cooper, M.D.; Peterson, R.D.; Good, R.A.; Peterson, R.D.A.; Good, R.A. Delineation of the thymic and bursal lymphoid systems in the chicken. Nature, 1965, 205(4967), 143-146.
[] [PMID: 14276257]
Ribatti, D.; Max, D.; Max, D. Cooper and the delineation of two lymphoid lineages in the adaptive immune system. Immunol. Lett., 2014, 162(1 Pt A), 233-236.
[] [PMID: 25236938]
Gitlin, A.D.; Nussenzweig, M.C. Immunology: fifty years of B lymphocytes. Nature, 2015, 517(7533), 139-141.
[] [PMID: 25567266]
Audhya, T.; Kroon, D.; Heavner, G.; Viamontes, G.; Goldstein, G. Tripeptide structure of bursin, a selective B-cell-differentiating hormone of the bursa of Fabricius. Science, 1986, 231(4741), 997-999.
[] [PMID: 3484838]
Brand, A.; Gilmour, D.G.; Goldstein, G. Lymphocyte-differentiating hormone of bursa of Fabricius. Science, 1976, 193(4250), 319-321.
[] [PMID: 180600]
Feng, X.L.; Liu, Q.T.; Cao, R.B.; Zhou, B.; Ma, Z.Y.; Deng, W.L.; Wei, J.C.; Qiu, Y.F.; Wang, F.Q.; Gu, J.Y.; Wang, F.J.; Zheng, Q.S.; Ishag, H.; Chen, P.Y. Identification and characterization of novel immunomodulatory bursal-derived pentapeptide-II (BPP-II). J. Biol. Chem., 2012, 287(6), 3798-3807.
[] [PMID: 22184121]
Feng, X.; Cao, R.; Zhou, B.; Liu, Q.; Liu, K.; Liu, X.; Zhang, Y.; Gu, J.; Miao, D.; Chen, P. The potential mechanism of Bursal-derived BPP-II on the antibody production and avian pre-B cell. Vaccine, 2013, 31(11), 1535-1539.
[] [PMID: 23000123]
Arakawa, H.; Buerstedde, J.M. Immunoglobulin gene conversion: insights from bursal B cells and the DT40 cell line. Dev. Dyn., 2004, 229(3), 458-464.
[] [PMID: 14991701]
Kikuchi, K.; Abdel-Aziz, H.I.; Taniguchi, Y.; Yamazoe, M.; Takeda, S.; Hirota, K. Bloom DNA helicase facilitates homologous recombination between diverged homologous sequences. J. Biol. Chem., 2009, 284(39), 26360-26367.
[] [PMID: 19661064]
Liu, X.D.; Zhou, B.; Feng, X.L.; Cao, R.B.; Chen, P.Y. BP8, a novel peptide from avian immune system, modulates B cell developments. Amino Acids, 2014, 46(12), 2705-2713.
[] [PMID: 25168247]
Liu, X.D.; Zhou, B.; Cao, R.B.; Feng, X.L.; Ma, Z.Y.; Chen, P.Y. BP5 regulated B cell development promoting anti-oxidant defence. Amino Acids, 2014, 46(1), 209-222.
[] [PMID: 24292101]
Ratcliffe, M.J. Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development. Dev. Comp. Immunol., 2006, 30(1-2), 101-118.
[] [PMID: 16139886]
Feng, X.L.; Zong, M.M.; Zhou, G.F.; Zheng, Y.; Yu, Y.N.; Cao, R.B.; Chen, P.Y.; Yang, M. The functions and mechanism of a new oligopeptide BP9 from Avian Bursa on antibody responses, immature B cell, and autophagy. J. Immunol. Res., 2019, 20191574383
[] [PMID: 30723747]
Lu, H.; Castro, A.E. Evaluation of the infectivity, length of infection, and immune response of a low-pathogenicity H7N2 avian influenza virus in specific-pathogen-free chickens. Avian Dis., 2004, 48(2), 263-270.
[] [PMID: 15283413]
Liu, Q.; Chen, H.; Huang, J.; Chen, Y.; Gu, M.; Wang, X.; Hu, S.; Liu, X.; Liu, X. A nonpathogenic duck-origin H9N2 influenza A virus adapts to high pathogenicity in mice. Arch. Virol., 2014, 159(9), 2243-2252.
[] [PMID: 24696271]
Liu, Q.; Huang, J.; Chen, Y.; Chen, H.; Li, Q.; He, L.; Hao, X.; Liu, J.; Gu, M.; Hu, J.; Wang, X.; Hu, S.; Liu, X.; Liu, X. Virulence determinants in the PB2 gene of a mouse-adapted H9N2 virus. J. Virol., 2015, 89(1), 877-882.
[] [PMID: 25339773]
Liu, Q.; Liu, Y.; Yang, J.; Huang, X.; Han, K.; Zhao, D.; Bi, K.; Li, Y. Two genetically similar H9N2 Influenza A viruses show different pathogenicity in mice. Front. Microbiol., 2016, 7, 1737.
[] [PMID: 27867373]
Egawa, T.; Bhattacharya, D. Regulation of metabolic supply and demand during B cell activation and subsequent differentiation. Curr. Opin. Immunol., 2019, 57, 8-14.
[] [PMID: 30339937]
Romero-Ramírez, S.; Navarro-Hernandez, I.C.; Cervantes-Díaz, R.; Sosa-Hernández, V.A.; Acevedo-Ochoa, E.; Kleinberg-Bild, A.; Valle-Rios, R.; Meza-Sánchez, D.E.; Hernández-Hernández, J.M.; Maravillas-Montero, J.L. Innate-like B cell subsets during immune responses: Beyond antibody production. J. Leukoc. Biol., 2018. Epub ahead of print
[] [PMID: 30457676]
Nguyen, T.T.T.; Graf, B.A.; Randall, T.D.; Baumgarth, N. sIgM-FcμR interactions regulate early B cell activation and plasma cell development after influenza virus infection. J. Immunol., 2017, 199(5), 1635-1646.
[] [PMID: 28747342]
Tsiantoulas, D.; Kiss, M.; Bartolini-Gritti, B.; Bergthaler, A.; Mallat, Z.; Jumaa, H.; Binder, C.J. Secreted IgM deficiency leads to increased BCR signaling that results in abnormal splenic B cell development. Sci. Rep., 2017, 7(1), 3540.
[] [PMID: 28615655]
Nguyen, T.T.; Elsner, R.A.; Baumgarth, N. Natural IgM prevents autoimmunity by enforcing B cell central tolerance induction. J. Immunol., 2015, 194(4), 1489-1502.
[] [PMID: 25595791]
Lam, J.H.; Baumgarth, N. The multifaceted B cell response to influenza virus. J. Immunol., 2019, 202(2), 351-359.
[] [PMID: 30617116]
Tokunaga, R.; Naseem, M.; Lo, J.H.; Battaglin, F.; Soni, S.; Puccini, A.; Berger, M.D.; Zhang, W.; Baba, H.; Lenz, H.J. B cell and B cell-related pathways for novel cancer treatments. Cancer Treat. Rev., 2019, 73, 10-19.
[] [PMID: 30551036]
Silveira, E.L.V.; Dominguez, M.R.; Soares, I.S. To B or Not to B: Understanding B cell responses in the development of malaria infection. Front. Immunol., 2018, 9, 2961.
[] [PMID: 30619319]
Nisini, R.; Poerio, N.; Mariotti, S.; De Santis, F.; Fraziano, M. The multirole of liposomes in therapy and prevention of infectious diseases. Front. Immunol., 2018, 9, 155.
[] [PMID: 29459867]
Choi, S.Y.; Park, S.K.; Yoo, H.W.; Pi, J.H.; Kang, C.J. Charged amino acid-rich leucine zipper-1 (Crlz-1) as a target of Wnt signaling pathway controls Pre-B cell proliferation by affecting Runx/CBFβ-targeted VpreB and λ5 genes. J. Biol. Chem., 2016, 291(29), 15008-15019.
[] [PMID: 27226553]
Wang, L.; Huang, J.; Jiang, M.; Lin, H. Tissue-specific transplantation antigen P35B (TSTA3) immune response-mediated metabolism coupling cell cycle to postreplication repair network in no-tumor hepatitis/cirrhotic tissues (HBV or HCV infection) by biocomputation. Immunol. Res., 2012, 52(3), 258-268.
[] [PMID: 22528125]
Jayachandran, N.; Mejia, E.M.; Sheikholeslami, K.; Sher, A.A.; Hou, S.; Hatch, G.M.; Marshall, A.J. TAPP adaptors control B cell metabolism by modulating the phosphatidylinositol 3-kinase signaling pathway: a novel regulatory circuit preventing autoimmunity. J. Immunol., 2018, 201(2), 406-416.
[] [PMID: 29884706]
Nakayama, S.; Matsuda, M.; Adachi, T.; Sueda, S.; Ueda, K.; Kawahara, K.; Ohashi, Y.; Awaji, S.; Hashimoto, S.; Matsumura, I. Tumor necrosis factor- and interleukin-6-producing high-grade B-cell lymphoma, not otherwise specified in the pleura. Leuk. Res. Rep., 2018, 10, 1-3.
[] [PMID: 29998057]
Dlouhy, I.; Filella, X.; Rovira, J.; Magnano, L.; Rivas-Delgado, A.; Baumann, T.; Martínez-Trillos, A.; Balagué, O.; Martínez, A.; González-Farre, B.; Karube, K.; Gine, E.; Delgado, J.; Campo, E.; López-Guillermo, A. High serum levels of soluble Interleukin-2 Receptor (sIL2-R), Interleukin-6 (IL-6) and Tumor Necrosis Factor alpha (TNF) are associated with adverse clinical features and predict poor outcome in diffuse large B-cell lymphoma. Leuk. Res., 2017, 59, 20-25.
[] [PMID: 28544905]
Tanaka, T.; Narazaki, M.; Kishimoto, T. IL-6 in inflammation, immunity, and disease. Cold Spring Harb. Perspect. Biol., 2014, 6(10)a016295
[] [PMID: 25190079]
Eddahri, F.; Denanglaire, S.; Bureau, F.; Spolski, R.; Leonard, W.J.; Leo, O.; Andris, F. Interleukin-6/STAT3 signaling regulates the ability of naive T cells to acquire B-cell help capacities. Blood, 2009, 113(11), 2426-2433.
[] [PMID: 19020307]
Sin, S.H.; Kang, S.A.; Kim, Y.; Eason, A.; Tan, K.; An, H.; Dittmer, D.P. Kaposi’s Sarcoma-Associated herpesvirus latency locus compensates for interleukin-6 in initial B cell activation. J. Virol., 2015, 90(4), 2150-2154.
[] [PMID: 26656696]

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy