Brain transcriptome response to Streptococcus agalactiae infection and the heterogeneous regulation of neuropeptides on immune response in tilapia, Oreochromis niloticus

Abstract

Defense of the vertebrate brain against infection must be accomplished without the generation of potentially harmful inflammation since the brain has a limited capacity to repair damage. Neuropeptides are multifunctional neuronal signaling molecules that regulate physiological processes and behaviors. Recently, their potential roles in modulating immune responses and inflammation have been discovered in mammals. However, the role of neuropeptides in teleost brain immune response mediation is unknown. Herein, the brain transcriptional profiles of economically important fish, Nile tilapia (Oreochromis niloticus), against Streptococcus agalactiae, a common pathogen causing serious meningitis, was first revealed. Twelve cDNA libraries of O. niloticus brain from four treatment time points (0, 6, 24, and 48 h) were constructed. A total of 517 differentially expressed genes (DEGs) were obtained via pairwise comparison of the brain transcriptome data at different time points. KEGG pathway analysis showed that most DEGs were in “neuroactive ligand-receptor interaction” (ko04080). Besides, 37 neuropeptide families with 143 neuropeptide precursor genes (producing 204 different transcripts) were identified. Also, 15 neuropeptide precursor genes (ADCYAP1A, AVP, CCK2, GAL, GNRH3, NPY1, OXT, PDYN, PMCH1, PMCH2, POMC1A, SST1, TAC1, UCN3, and HAMP1) were differentially expressed (P < 0.05) during S. agalactiae infection. Among them, five mature neuropeptides (AVP, OXT, UCN3, SP, and NKA) were prepared and used to determine and characterize the heterogeneous regulation of immune response. Specifically, neuropeptides promoted inflammatory response, immune pathways, and the cAMP–PKA pathway to Lipopolysaccharide (LPS) stimulation. However, the responses to Lipoteichoic acid (LTA) were first promoted and soon reduced with neuropeptides treatment. This study represents the first comprehensive identification of neuropeptides in tilapia, and would contribute to a better understanding of the evolution and immunological roles of neuropeptides in teleosts.