Protein Tyrosine Kinase Gene Expression Profiles in the Embryonic Bursa of Fabricius of Chicken Lines Selected for High and Low Antibody Responses
DOI:
https://doi.org/10.3923/ijps.2021.173.178Keywords:
Bursa of fabricius, fyn-related kinase, high antibody line, low antibody line, receptor tyrosine kinase genesAbstract
Background and Objective: The chicken lines selected for high (HAS line) and low (LAS) antibody responses to antigenic challenge represent a valuable model for identifying genes controlling the development of humoral immunity. In this study, we evaluated the expression of receptor tyrosine kinase (RTK) and non-receptor tyrosine kinase (nRTK) genes in the developing bursa from both chicken lines. These genes have a critical role in cell survival, migration and differentiation. In addition, we examined bursas from embryos exposed to testosterone, to detect changes in the expression of these genes when normal bursa development was inhibited. Materials and Methods: cDNA was synthesized from whole bursa RNA and PCR amplified with degenerate primers. The nucleotide sequence of the PCR products was analyzed with the NCBI database. Results: A total of 172 cDNAs from the HAS and 183 cDNAs from the LAS lines were sequenced. The most abundant nRTK and RTK cDNAs were from the Fyn-related kinase (FRK) and Ephrin A1 receptor (EphA1) genes and the expression levels differed significantly between the HAS and LAS bursas. Embryonic exposure to testosterone increased the number of cDNAs from the FRK gene. Conclusion: The significant differences in transcription of the FRK and EphA1 genes due to genetic selection may result in differences in bursal development between the HAS and LAS lines. Testosterone treatment significantly modulated FRK expression, which suggests a role for this gene in the differentiation and organization of the epithelium in the developing bursa.
References
Zhao, X.L., C.F. Honaker and P.B. Siegel, 2012. Phenotypic responses of chickens to long-term selection for high or low antibody titers to sheep red blood cells. Poult. Sci., 91: 1047-1056.
Dorshorst, B.J., P.B. Siegel and C.M. Ashwell, 2011. Genomic regions associated with antibody response to sheep red blood cells in the chicken. Anim. Genet., 42: 300-308.
Ubosi, C.O., W.B. Gross and P.B. Siegel, 1985. Divergent selection of chickens for antibody production to sheep erythrocytes: age effect in parental lines and their crosses. Avian Dis., 1: 150-158.
Masteller, E.L., K.P. Lee, L.M. Carlson and C.B. Thompson, 1995. Expression of sialyl Lewis(x) and Lewis(x) defines distinct stages of chicken B cell maturation. J. Immunol., 155: 5550-5556.
Felfoldi, B., G.T. Pharr, L.M. Pinchuk, A.M. Cooksey and J.P. Thaxton, 2008. Preliminary protein profile analysis of the late embryonic b-cell stages in the chicken bursa of fabricius. Int. J. Poult. Sci., 7: 117-124.
Pharr, G.T., A.M. Cooksey, B.M. McGruder, B. Felfoldi, E.D. Peebles, M.T. Kidd and J.P. Thaxton, 2009. Ephrin receptor expression in the embryonic bursa of fabricius. Int. J. Poult. Sci., 8: 426-431.
Andrae, J., R. Gallini and C. Betsholtz, 2008. Role of platelet-derived growth factors in physiology and medicine. Genes Dev., 22: 1276-1312.
Casaletto, J.B. and A.I. McClatchey, 2012. Spatial regulation of receptor tyrosine kinases in development and cancer. Nat. Rev. Cancer, 12: 387-400.
Iwama, A., K. Okano, T. Sudo, Y. Matsuda and T. Suda, 1994. Molecular cloning of a novel receptor tyrosine kinase gene, STK, derived from enriched hematopoietic stem cells. Blood, 83: 3160-3169.
Nagy, N. and I. Olah, 2009. Locally applied testosterone is a novel method to influence the development of the avian bursa of Fabricius. J. Immunol. Methods., 343: 79-102.
Audic, S. and J.M. Claverie, 1997. The significance of digital gene expression profiles. Genome Res., 7: 986-995.
Claverie, J.M. and T.N. Ta, 2019. ACDtool: a web-server for the generic analysis of large data sets of counts. Bioinformatics, 35: 170-171.
Cance, W.G., R.J. Craven, M. Bergman, L. Xu, K. Alitalo and E.T. Liu, 1994. Rak, a novel nuclear tyrosine kinase expressed in epithelial cells. Cell Growth Differ., 12: 1347-1355.
Nuthalapati, N.K., J.D. Evans, R.L. Taylor, S.L. Branton, B. Nanduri and G.T. Pharr, 2019. Transcriptomic analysis of early B-cell development in the chicken embryo. Poult. Sci., 98: 5342-5354.
Goel, R.K. and K.E. Lukong, 2016. Understanding the cellular roles of Fyn-related kinase (FRK): implications in cancer biology. Cancer Metastasis Rev., 35: 179-199.
Zhou, X., L. Hua, W. Zhang, M. Zhu and Q. Shi. et al., 2012. FRK controls migration and invasion of human glioma cells by regulating JNK/c-Jun signaling. J. Neuro-Oncology, 110: 9-19.
Ogunbolude, Y., C. Dai, E.T. Bagu, R.K. Goel and S. Miah et al., 2017. FRK inhibits breast cancer cell migration and invasion by suppressing epithelial-mesenchymal transition. Oncotarget, 8: 113034-113065.
Jin, L. and R.J. Craven, 2014. The Rak/Frk tyrosine kinase associates with and internalizes the epidermal growth factor receptor. Oncogene, 33: 326-335.
Chen, J., F. Zeng, S.J. Forrester, S. Eguchi, M.Z. Zhang and R.C. Harris, 2016. Expression and function of the epidermal growth factor receptor in physiology and disease. Physiol. Rev., 96: 1025-1069.
Omi, M., M. Fisher, N.J. Maihle and C.N. Dealy, 2005. Studies on epidermal growth factor receptor signaling in vertebrate limb patterning. Dev. Dyn., 233: 288-300.
White, P.M., J.S. Stone, A.K. Groves and N. Segil., 2012. EGFR signaling is required for regenerative proliferation in the cochlea: Conservation in birds and mammals. Dev. Biol., 363: 191-200.
Nagy, N. and I. Olah, 2010. Experimental evidence for the ectodermal origin of the epithelial anlage of the bursa of Fabricius. Development., 137: 3019-3023.
Dai, D., Q. Huang, R. Nussinov and B. Ma, 2014. Promiscuous and specific recognition among ephrins and Eph receptors. Biochim. Biophys. Acta (BBA) - Proteins Proteomics, 1844: 1729-1740.
Allen-Sharpley, M.R. and K.S. Cramer, 2012. Coordinated Eph-ephrin signaling guides migration and axon targeting in the avian auditory system. Neural Dev., Vol. 7, No. 29.
North, H.A., X. Zhao, S.M. Kolk, M.A. Clifford, D.M. Ziskind and M.J. Donoghue, 2009. Promotion of proliferation in the developing cerebral cortex by EphA4 forward signaling. Development, 136: 2467-2476.
Qiu, R., X. Wang, A. Davy, C. Wu and K. Murai et al., 2008. Regulation of neural progenitor cell state by ephrin-B. J. Cell Biol., 181: 973-983.
Coulthard, M.G., J.D. Lickliter, N. Subanesan, K. Chen and G.C. Webb et al., 2001. Characterization of the EphA1 receptor tyrosine kinase: Expression in epithelial tissues. Growth Factors, 18: 303-317.
Duffy, S.L., M.G. Coulthard, M.D. Spanevello, N.I. Herath and T.M. Yeadon et al., 2008. Generation and characterization of EphA1 receptor tyrosine kinase reporter knockout mice. Genesis, 46: 553-561.
Sasaki, E. and R.J. Etches, 2001. Expression of protein tyrosine kinases and stem cell factor in chicken blastodermal cells. Poult. Sci., 80: 161-171.
Sasaki, E., H. Hikono, Y. Kaku, T. Kuwana, M. Naito and M. Sakurai, 2003. EphA9, a novel avian receptor tyrosine kinase gene. Gene, 316: 103-110.
Downloads
Published
Issue
Section
License
Copyright (c) 2021 The Author(s)
This work is licensed under a Creative Commons Attribution 4.0 International License.
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.
