Grass carp MAP3K4 participates in the intestinal immune response to bacterial challenge

被引:2
作者
Qu, Fufa [1 ]
Li, Jialing [1 ]
Zeng, Xuan [1 ]
She, Qing [1 ]
Li, Yurong [1 ]
Xie, Wenjie [1 ]
Cao, Shenping [1 ]
Zhou, Yonghua [1 ]
He, Zhimin [1 ]
Tang, Jianzhou [1 ]
Mao, Zhuangwen [1 ]
Wang, Yuping [1 ]
Fang, Jiamei [1 ]
Xu, Wenqian [1 ]
Liu, Zhen [1 ]
机构
[1] Changsha Univ, Dept Biol & Environm Engn, Hunan Prov Key Lab Nutr & Qual Control Aquat Anim, Changsha 410022, Peoples R China
基金
中国国家自然科学基金;
关键词
Grass carp; MAP3K4; Molecular characteristics; Bacterial challenge; Intestinal immunity; KINASE KINASE KINASE; P38; MAPK; CTENOPHARYNGODON-IDELLA; MOLECULAR CHARACTERIZATION; EPITHELIAL-CELLS; EXPRESSION; MEKK4; PATHWAYS; CLONING; STRESS;
D O I
10.1016/j.fsi.2021.11.016
中图分类号
S9 [水产、渔业];
学科分类号
0908 ;
摘要
Mitogen-activated protein kinase kinase kinase 4 (MAP3K4) is a multifunctional mediator of the conserved MAPK signaling pathway that plays essential roles in the regulation of immune responses in mammals. However, the function of teleost MAP3K4s in innate immunity, especially in the intestinal immune system, is still poorly understood. In the current study, we identified a fish MAP3K4 homolog (CiMAP3K4) in Ctenopharyngodon idella as well as its immune function in intestine following bacterial infection in vivo and in vitro. The open reading frame (ORF) of CiMAP3K4 encodes putative peptide of 1544 amino acids containing a predicted serine/threonine protein kinase (S_TKc) domain with high identity with other fish MAP3K4s. Phylogenetic analysis revealed the CiMAP3K4 belonged to the fish cluster and showed the closest relationship to Pimephales promelas. Quantitative real-time PCR (qRT-PCR) analysis revealed that CiMAP3K4 transcripts were widely distributed in all tested tissues, especially with high expression in the muscle and intestine of healthy grass carp. In vitro, CiMAP3K4 gene expression was upregulated by bacterial PAMPs (lipolysaccharide (LPS), peptidoglycan (PGN), L-Ala-gamma-D-Glu-meso-diaminopimelic acid (Tri-DAP) and muramyl dipeptide (MDP)) and pathogens (Aeromonas hydrophila and Aeromonas veronii) in primary intestinal cells. In vivo, the mRNA expression levels of CiMAP3K4 in the intestine were significantly induced by bacterial MDP challenge in a time-dependent manner; however, this effect could be inhibited by the bioactive dipeptides beta-alanyl-L-histidine (carnosine) and alanyl-glutamine (Ala-Gln). Moreover, CiMAP3K4 was located primarily in the cytoplasm, and its overexpression increased the transcriptional activity of AP-1 in HEK293T cells. Collectively, these results suggested that CiMAP3K4 might play an important role in the intestinal immune response to bacterial infections, which paves the way for a better understanding of the intestinal immune system of grass carp.
引用
收藏
页码:82 / 91
页数:10
相关论文
共 54 条
[1]   MEKK4 stimulation of p38 and JNK activity is negatively regulated by GSK3β [J].
Abell, Amy N. ;
Granger, Deborah A. ;
Johnson, Gary L. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2007, 282 (42) :30476-30484
[2]   Gadd45a Protein Promotes Skeletal Muscle Atrophy by Forming a Complex with the Protein Kinase MEKK4 [J].
Bullard, Steven A. ;
Seo, Seongjin ;
Schilling, Birgit ;
Dyle, Michael C. ;
Dierdorff, Jason M. ;
Ebert, Scott M. ;
DeLau, Austin D. ;
Gibson, Bradford W. ;
Adams, Christopher M. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2016, 291 (34) :17496-17509
[3]   A major secreted elastase is essential for pathogenicity of Aeromonas hydrophila [J].
Cascón, A ;
Yugueros, J ;
Temprano, A ;
Sánchez, M ;
Hernanz, C ;
Luengo, JM ;
Naharro, G .
INFECTION AND IMMUNITY, 2000, 68 (06) :3233-3241
[4]   Mammalian MAP kinase signalling cascades [J].
Chang, LF ;
Karin, M .
NATURE, 2001, 410 (6824) :37-40
[5]   Peptidoglycan-mediated IL-8 expression in human alveolar type II epithelial cells requires lipid raft formation and MAPK activation [J].
Cheon, In Su ;
Woo, Sang Su ;
Kang, Seok-Seong ;
Im, Jintaek ;
Yun, Cheol-Heui ;
Chung, Dae Kyun ;
Park, Dong Ki ;
Han, Seung Hyun .
MOLECULAR IMMUNOLOGY, 2008, 45 (06) :1665-1673
[6]   Loss of mitogen-activated protein kinase kinase kinase 4 (MEKK4) results in enhanced apoptosis and defective neural tube development [J].
Chi, HB ;
Sarkisian, MR ;
Rakic, P ;
Flavell, RA .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (10) :3846-3851
[7]   MEKK4 sequesters RIP2 to dictate NOD2 signal specificity [J].
Clark, Nivedita M. ;
Marinis, Jill M. ;
Cobb, Brian A. ;
Abbott, Derek W. .
CURRENT BIOLOGY, 2008, 18 (18) :1402-1408
[8]   Mitogen-activated protein kinases: new signaling pathways functioning in cellular responses to environmental stress [J].
Cowan, KJ ;
Storey, KB .
JOURNAL OF EXPERIMENTAL BIOLOGY, 2003, 206 (07) :1107-1115
[9]   PepT1 mediates transport of the proinflammatory bacterial tripeptide L-Ala-γ-D-Glu-meso-DAP in intestinal epithelial cells [J].
Dalmasso, Guillaume ;
Nguyen, Hang Thi Thu ;
Charrier-Hisamuddin, Laetitia ;
Yan, Yutao ;
Laroui, Hamed ;
Demoulin, Benjamin ;
Sitaraman, Shanthi V. ;
Merlin, Didier .
AMERICAN JOURNAL OF PHYSIOLOGY-GASTROINTESTINAL AND LIVER PHYSIOLOGY, 2010, 299 (03) :G687-G696
[10]   First molluscan transcription factor activator protein-1 (Ap-1) member from disk abalone and its expression profiling against immune challenge and tissue injury [J].
De Zoysa, Mahanama ;
Nikapitiya, Chamilani ;
Lee, Youngdeuk ;
Lee, Sukkyoung ;
Oh, Chulhong ;
Whang, Ilson ;
Yeo, Sang-Yeop ;
Choi, Cheol Young ;
Lee, Jehee .
FISH & SHELLFISH IMMUNOLOGY, 2010, 29 (06) :1028-1036