Skip to main content
Log in

Cloning and mRNA expression of macrophage migration inhibitory factor (MIF) gene of large yellow croaker (Pseudosciaena crocea)

  • Published:
Acta Oceanologica Sinica Aims and scope Submit manuscript

Abstract

Mammalian macrophage migration inhibitory factor (MIF) plays an important role as an indispensable mediator in the pathogenesis of inflammatory disease like septicemia, but little is known about the role of MIF homologue in fish septicemia. The authors have cloned the MIF homologue in large yellow croaker Pseudosciaena crocea (LycMIF) using RACE approach. The full-length cDNA of LycMIF was 634 bases and contained an ORF of 345 bases encoding a protein of 115 amino acid residues. As demonstrated by RT-PCR and QRT-PCR assay, MIF mRNAs were constitutively expressed in 11 selected tissues and were abundant in brain and liver. Moreover, the LycMIF transcripts in the liver and head kidney were responsive to bacteria infection and could be significantly up-regulated. Our results provide the first direct evidence that fish MIF was implicated in pathogenesis of fish vibrosis and play an important role in response to bacteria infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bacher M, Meinhardt A, Lan H Y, et al. 1998. MIF expression in the rat brain: implications for neuronal function. Mol Med, 4(4): 217–230

    Google Scholar 

  • Bernhagen J, Calandra T, Mitchell R A, et al. 1993. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature, 365(6448): 756–759

    Article  Google Scholar 

  • Bernhagen J, Mitchell R A, Calandra T. 1994. Purification, Bioactivity, and Secondary Structure Analysis of Mouse and Human Macrophage Migration Inhibitory Factor (MIF). Biochemistry, 33(47): 14144–14155

    Article  Google Scholar 

  • Calandra T, Bernhagen J, Mitchell R A, et al. 1994. The macrophage is an important and previously unrecongnized source of macrophage migration inhibitory factor. J Exp Med, 179(6): 1895–1902

    Article  Google Scholar 

  • Calandra T, Roger T. 2003. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol, 3(10): 791–800

    Article  Google Scholar 

  • Chang Mingxian, Nie Pin, Wei Lili. 2007. Short and long peptidoglycan recognition proteins (PGRPs) in zebrafish, with findings of multiple PGRP homologs in teleost fish. Mol Immunol, 44(11): 3005–3023

    Article  Google Scholar 

  • Chen Yafang, Wang Jun, Su Yongquan, et al. 2006. Study on the extra cellular products (ECP) of the pathogenic Vibrio harveyi isolated from the farmed groupers. Marine Sciences (in Chinese), 30(10): 30–34

    Google Scholar 

  • Chen Qiang, Yan Qingpi, Wang Kejuan, et al. 2008. Portal of entry for pathogenic Vibrio alginolyticus into large yellow croaker Pseudosciaena crocea, and characteristics of bacterial adhesion to mucus. Dis Aquat Organ, 80(3): 181–188

    Article  Google Scholar 

  • Flaster H, Bernhagen J, Calandra T, et al. 2007. The macrophage migration inhibitory factor glucocorticoid dyad: regulation of inflammation and immunity. Mol Endocrinol, 21(6): 1267–1280

    Article  Google Scholar 

  • Fingerle R G, Koch P, Bikoff R, et al. 2003. Regulation of macrophage migration inhibitory factor expression by glucocorticoids in vivo. Am J Pathol, 162(1): 47–56

    Google Scholar 

  • Froidevaux C, Roger T, Martin C. 2001. Macrophage migration inhibitory factor and innate immune responses to bacterial infections. Crit Care Med, 29(7 supp): S13–15

    Article  Google Scholar 

  • Gando S, Sawamura A, Hayakawa M, et al. 2007. High macrophage migration inhibitory factor levels in disseminated intravascular coagulation patients with systemic inflammation. Inflammation, 30(3–4): 118–124

    Article  Google Scholar 

  • Gao L, Flores C, Fan-Ma S, et al. 2007. Macrophage migration inhibitory factor in acute lung injury: expression, biomarker, and associations. Transl Res, 150(1): 18–29

    Article  Google Scholar 

  • Huang Xiaoru, Chun Hui C W, Chen Yongxiong, et al. 2001. Macrophage migration inhibitory factor is an important mediator in the pathogenesis of gastric inflammation in rats. Gastroenterology, 121(3): 619–630

    Article  Google Scholar 

  • Ito K, Yoshiura Y, Ototake M, et al. 2008. Macrophage migration inhibitory factor (MIF) is essential for development of zebrafish, Danio rerio. Dev Comp Immunol, 32(6): 664–672

    Article  Google Scholar 

  • Jin Hongjian, Xiang Lixin, Shao Jianzhong. 2007. Molecular cloning and identification of macrophage migration inhibitory factor (MIF) in teleost fish. Dev-Comp Immunol, 31(11): 1131–1144

    Article  Google Scholar 

  • Kleemann R, Hausser A, Geiger G, et al. 2000. Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature, 408(6809): 211–216

    Article  Google Scholar 

  • Kleemann R, Kapurniotu A, Frank R W, et al. 1998. Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J Mol Biol, 280(1): 85–102

    Article  Google Scholar 

  • Kleemann R, Rorsman H, Rosengren E. 2000. Dissection of the enzymatic and immunologic functions of macrophage migration inhibitory factor. Full immunologic activity of N-terminally truncated mutants. Eur J Biochem, 267(24): 7183–7193

    Article  Google Scholar 

  • Larson D F, Horak K. 2006. Macrophage migration inhibitory factor: controller of systemic inflammation. Crit Care, 10(2): 138

    Article  Google Scholar 

  • Lubetsky J B, Swope M, Dealwis C, et al. 1999. Pro-1 of macrophage migration inhibitory factor functions as a catalytic base in the phenylpyruvate tautomerase activity. Biochemistry, 38(22): 7346–7354

    Article  Google Scholar 

  • Maaser C, Eckmann L, Paesold G, et al. 2002. Ubiquitous production of macrophage migration inhibitory factor by human gastric and intestinal epithelium. Gastroenterology Mar, 122(3): 667–680

    Article  Google Scholar 

  • Miska K B, Fetterer R H, Lillehoj H S, et al. 2007. Characterisation of macrophage migration inhibitory factor from Eimeria species infectious to chickens. Mol Biochem Parasitol, 151(2): 173–183

    Article  Google Scholar 

  • O’Toole R, Von Hofsten J, Rosqvist R, et al. 2004. Visualisation of zebrafish infection by GFP-labelled Vibrio anguillarum. Microb Pathog, 37(1): 41–46

    Article  Google Scholar 

  • Rahman S H, Menon K V, Holmfield J H, et al. 2007. Serum macrophage migration inhibitory factor is an early marker of pancreatic necrosis in acute pancreatitis. Ann Surg, 245(2): 282–289

    Article  Google Scholar 

  • Ringϕ E, Salinas I, Olsen R E, et al. 2007. Histological changes in intestine of Atlantic salmon (Salmo salar L.) following in vitro exposure to pathogenic and probiotic bacterial strains. Cell Tissue Res, 328(1): 109–116

    Article  Google Scholar 

  • Roger T, Ding X, Chanson A L, et al. 2007. Regulation of constitutive and microbial pathogen-induced human macrophage migration inhibitory factor (MIF) gene expression. Eur J Immunol, 37(12): 3509–3521

    Article  Google Scholar 

  • Rosengren E, Bucala R, Aman P, et al. 1996. The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction. Mol Med, 2(1): 143–149

    Google Scholar 

  • Sakai Y, Masamune A, Satoh A, et al. 2003. Macrophage migration inhibitory factor is a critical mediator of severe acute pancreatitis. Gastroenterology, 124(3): 725–736

    Article  Google Scholar 

  • Sato A, Uinukool T S, Kuroda N, et al. 2003. Macrophage migration inhibitory factor (MIF) of jawed and jawless fishes: implications for its evolutionary origin. Dev Comp Immunol, 27(5): 401–412

    Article  Google Scholar 

  • Stosic G S, Stojanovic I, Nicoletti F. 2008. MIF in autoimmunity and novel therapeutic approaches. Autoimmun Rev, 19: 1–6

    Google Scholar 

  • Sugita H, Ito Y. 2006. Identification of intestinal bacteria from Japanese flounder (Paralichthys olivaceus) and their ability to digest chitin. Lett Appl Microbiol, 43(3): 336–342

    Article  Google Scholar 

  • Swope M D, Lolis E. 1999. Macrophage migration inhibitory factor: cytokine, hormone, or enzyme? Rev Physiol Biochem Pharmacol, 139: 1–32

    Article  Google Scholar 

  • Swope M, Sun H W, Blake P R, et al. 1998. Direct link between cytokine activity and a catalytic site for macrophage migration inhibitory factor. EMBO J, 17(13): 3534–3541

    Article  Google Scholar 

  • Taylor A B, Johnson Jr W H, Czerwinski R M, et al. 1999. Crystal structure of macrophage migration inhibitory factor complexed with (E)-2-fluorophydroxycinnamate at 1.8A resolution: implications for enzymatic catalysis and inhibition. Biochemistry, 38(23): 7444–7452

    Article  Google Scholar 

  • Thiele M, Bernhagen J. 2005. Link between macrophage migration inhibitory factor and cellular redox regulation. Antioxid redox signal, 7: 1234–1248

    Article  Google Scholar 

  • Wang Chuanjuan, Zhang Xiaohua, Jia Airong, et al. 2008. Identification of immune-related genes from kidney and spleen of turbot, Psetta maxima (L.), by suppression subtractive hybridization following challenge with Vibrio harveyi. J Fish Dis, 31(7): 505–514

    Article  Google Scholar 

  • Xia H H, Yang Y, Chu K M, et al. 2009. Serum macrophage migration-inhibitory factor as a diagnostic and prognostic biomarker for gastric cancer. Cancer, 115(23): 5441–5449

    Article  Google Scholar 

  • Zang Xingxing, Taylor P, Wang Jiming, et al. 2002. Homologues of human macrophage migration inhibitory factor from a parasitic nematode. Gene cloning, protein activity, and crystal structure. J Biol Chem, 277(46): 44261–44267

    Article  Google Scholar 

  • Zhang Chongwen, Yu Lian, Qian Ronghua. 2008. Cloning and expression of Vibrio harveyi OmpK* and GAPDH* genes and their potential application as vaccines in large yellow croakers Pseudosciaena crocea. J Aquat Anim Health, 20(1): 1–11

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jun Wang.

Additional information

Foundation item: The National Natural Science Foundation of China under contract No. 40976096; the National Department Public Benefit Research Foundation of China under contract No. 200903029; the National High Technology Research and Development Program of China (863 Program) under contract No. 2006AA10A405.

Contributed equally.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mao, Y., Xu, B., Su, Y. et al. Cloning and mRNA expression of macrophage migration inhibitory factor (MIF) gene of large yellow croaker (Pseudosciaena crocea). Acta Oceanol. Sin. 29, 63–73 (2010). https://doi.org/10.1007/s13131-010-0037-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13131-010-0037-8

Key words

Navigation