The cytokine macrophage migration inhibitory factor (MIF) acts as a neurotrophin in the developing inner ear of the zebrafish, Danio rerio

Developmental Biology

Volumn 363, Issue 1, 2012, Pages 84-94

  Shen, Yu Chi ^a   Thompson, Deborah L ^a,d   Kuah, Meng Kiat ^b,c   Wong, Kah Loon ^b   Wu, Karen L ^a   Linn, Stephanie A ^a   Jewett, Ethan M ^d,e   Shu Chien, Alexander Chong ^b,c   Barald, Kate F ^a,d  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b SCHOOL OF PHYSICS   (Malaysia)

^c Kemeneterian Sains Teknologi dan Inovasi   (Malaysia)

^d UNIVERSITY OF MICHIGAN   (United States)

^e STANFORD UNIVERSITY   (United States)

Author keywords

Immune cytokines; Inner ear; Macrophage migration inhibitory factor; Neurotrophin; Sensory HC; Statoacoustic ganglion; Zebrafish

Indexed keywords

MACROPHAGE MIGRATION INHIBITION FACTOR; NEUROTROPHIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; HAIR CELL; INNER EAR DEVELOPMENT; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSORY NERVE CELL; ZEBRA FISH;

ANURA; AVES; DANIO RERIO; MAMMALIA; MUS; VERTEBRATA;

EID: 84857030458     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.12.023     Document Type: Article

References (46)

1. Adamska M., Leger S., Brand M., Hadrys T., Braun T., Bober E. Inner ear and lateral line expression of a zebrafish Nkx5-1 gene and its downregulation in the ears of FGF8 mutant, ace. Mech. Dev. 2000, 97:161-165.
2. Ard M.D., Morest D.K., Hauger S.H. Trophic interactions between the cochleovestibular ganglion of the chick embryo and its synaptic targets in culture. Neuroscience 1985, 16:151-170.
3. Bacher M., Meinhardt A., Lan H.Y., Mu W., Metz C.N., Chesney J.A., Calandra T., Gemsa D., Donnelly T., Atkins R.C., Bucala R. Migration inhibitory factor expression in experimentally induced endotoxemia. Am. J. Pathol. 1997, 150:235-246.
4. Bacher M., Meinhardt A., Lan H.Y., Dhabhar F.S., Mu W., Metz C.N., Chesney J.A., Gemsa D., Donnelly T., Atkins R.C., Bucala R. MIF expression in the rat brain: implications for neuronal function. Mol. Med. 1998, 4:217-230.
5. Barald K.F., Kelley M.W. From placode to polarization: new tunes in inner ear development. Development 2004, 131:4119-4130.
6. Bernhagen J., Krohn R., Lue H., Gregory J.L., Zernecke A., Koenen R.R., Dewor M., Georgiev I., Schober A., Leng L., Kooistra T., Fingerle-Rowson G., Ghezzi P., Kleemann R., McColl S.R., Bucala R., Hickey M.J., Weber C. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat. Med. 2007, 13:587-596.
7. Bianchi L.M., Cohan C.S. Developmental regulation of a neurite-promoting factor influencing statoacoustic neurons. Brain Res. Dev. Brain Res. 1991, 64:167-174.
8. Bianchi L.M., Daruwalla Z., Roth T.M., Attia N.P., Lukacs N.W., Richards A.L., White I.O., Allen S.J., Barald K.F. Immortalized mouse inner ear cell lines demonstrate a role for chemokines in promoting the growth of developing statoacoustic ganglion neurons. J. Assoc. Res. Otolaryngol. 2005, 6:355-367.
9. Chong S.W., Emelyanov A., Gong Z., Korzh V. Expression pattern of two zebrafish genes, cxcr4a and cxcr4b. Mech. Dev. 2001, 109:347-354.
10. Dagia N.M., Kamath D.V., Bhatt P., Gupte R.D., Dadarkar S.S., Fonseca L., Agarwal G., Chetrapal-Kunwar A., Balachandran S., Srinivasan S., Bose J., Pari K., B-Rao C., Parkale S.S., Gadekar P.K., Rodge A.H., Mandrekar N., Vishwakarma R.A., Sharma S. A fluorinated analog of ISO-1 blocks the recognition and biological function of MIF and is orally efficacious in a murine model of colitis. Eur. J. Pharmacol. 2009, 607:201-212.
11. Dambly-Chaudière C., Cubedo N., Ghysen A. Control of cell migration in the development of the posterior lateral line: antagonistic interactions between the chemokine receptors CXCR4 and CXCR7/RDC1. BMC Dev. Biol. 2007, 7:23.
12. Deverman B.E., Patterson P.H. Cytokines and CNS development. Neuron 2009, 64:61-78.
13. Esumi N., Budarf M., Ciccarelli L., Sellinger B., Kozak C.A., Wistow G. Conserved gene structure and genomic linkage for D-dopachrome tautomerase (DDT) and MIF. Mamm. Genome 1998, 9:753-757.
14. Feng Y., Xu Q. Pivotal role of hmx2 and hmx3 in zebrafish inner ear and lateral line development. Dev. Biol. 2010, 339:507-518.
15. Hertzano R., Puligilla C., Chan S.L., Timothy C., Depireux D.A., Ahmed Z., Wolf J., Eisenman D.J., Friedman T.B., Riazuddin S., Kelley M.W., Strome S.E. CD44 is a marker for the outer pillar cells in the early postnatal mouse inner ear. J. Assoc. Res. Otolaryngol. 2010, 11:407-418.
16. Holmes K.E., Wyatt M.J., Shen Y.C., Thompson D.A., Barald K.F. Direct Delivery of MIF Morpholinos Into the Zebrafish Otocyst by Injection and Electroporation Affects Inner Ear Development. J. Vis. Exp. 2011, http://www.jove.com/index/Details.stp?ID=2466, 10.3791/2466.
17. Ito K., Yoshiura Y., Ototake M., Nakanishi T. Macrophage migration inhibitory factor (MIF) is essential for development of zebrafish, Danio rerio. Dev. Comp. Immunol. 2008, 32:664-672.
18. Kobayashi S., Satomura K., Levsky J.M., Sreenath T., Wistow G.J., Semba I., Shum L., Slavkin H.C., Kulkarni A.B. Expression pattern of macrophage migration inhibitory factor during embryogenesis. Mech. Dev. 1999, 84:153-156.
19. Koda M., Nishio Y., Hashimoto M., Kamada T., Koshizuka S., Yoshinaga K., Onodera S., Nishihira J., Moriya H., Yamazaki M. Up-regulation of macrophage migration-inhibitory factor expression after compression-induced spinal cord injury in rats. Acta Neuropathol. 2004, 108:31-36.
20. Larson D.F., Horak K. Macrophage migration inhibitory factor: controller of systemic inflammation. Crit. Care 2006, 10:138.
21. Lefebvre P.P., Leprince P., Weber T., Rigo J.M., Delree P., Moonen G. Neuronotrophic effect of developing otic vesicle on cochleo-vestibular neurons: evidence for nerve growth factor involvement. Brain Res. 1990, 507:254-260.
22. Leng L., Metz C.N., Fang Y., Xu J., Donnelly S., Baugh J., Delohery T., Chen Y., Mitchell R.A., Bucala R. MIF signal transduction initiated by binding to CD74. J. Exp. Med. 2003, 197:1467-1476.
23. Lubetsky J.B., Dios A., Han J., Aljabari B., Ruzsicska B., Mitchell R., Lolis E., Al-Abed Y. The tautomerase active site of macrophage migration inhibitory factor is a potential target for discovery of novel anti-inflammatory agents. J. Biol. Chem. 2002, 277:24976-24982.
24. Lugrin J., Ding X.C., Le Roy D., Chanson A.L., Sweep F.C., Calandra T., Roger T. Histone deacetylase inhibitors repress macrophage migration inhibitory factor (MIF) expression by targeting MIF gene transcription through a local chromatin deacetylation. Biochim. Biophys. Acta 2009, 1793:1749-1758.
25. McGrath K.E., Koniski A.D., Maltby K.M., McGann J.K., Palis J. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev. Biol. 1999, 213:442-456.
26. Mitchell R.A., Liao H., Chesney J., Fingerle-Rowson G., Baugh J., David J., Bucala R. Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:345-350.
27. Nishino T., Bernhagen J., Shiiki H., Calandra T., Dohi K., Bucala R. Localization of macrophage migration inhibitory factor (MIF) to secretory granules within the corticotrophic and thyrotrophic cells of the pituitary gland. Mol. Med. 1995, 1:781-788.
28. Nishio Y., Minami A., Kato H., Kaneda K., Nishihira J. Identification of macrophage migration inhibitory factor (MIF) in rat peripheral nerves: its possible involvement in nerve regeneration. Biochim. Biophys. Acta 1999, 1453:74-82.
29. Nishio Y., Nishihira J., Ishibashi T., Kato H., Minami A. Role of macrophage migration inhibitory factor (MIF) in peripheral nerve regeneration: anti-MIF antibody induces delay of nerve regeneration and the apoptosis of Schwann cells. Mol. Med. 2002, 8:509-520.
30. Noh E.J., Lim D.S., Jeong G., Lee J.S. An HDAC inhibitor, trichostatin A, induces a delay at G2/M transition, slippage of spindle checkpoint, and cell death in a transcription-dependent manner. Biochem. Biophys. Res. Commun. 2009, 378:326-331.
31. Purves D., Augustine G.J., Fitzpatrick D., Katz L.C., LaMantia A.-S., McNamara James O., Williams S.Mark Neuroscience 2001, Sinauer Associates, Sunderland (MA). 2nd edition.
32. Shen Y.C., Raymond P.A. Zebrafish cone-rod (crx) homeobox gene promotes retinogenesis. Dev. Biol. 2004, 269:237-251.
33. Shen Y.C., Jeyabalan A.K., Wu K.L., Hunker K.L., Kohrman D.C., Thompson D.L., Liu D., Barald K.F. The transmembrane inner ear (tmie) gene contributes to vestibular and lateral line development and function in the zebrafish (Danio rerio). Dev. Dyn. 2008, 237:941-952.
34. Suzuki M., Takamura Y., Maeno M., Tochinai S., Iyaguchi D., Tanaka I., Nishihira J., Ishibashi T. Xenopus laevis macrophage migration inhibitory factor is essential for axis formation and neural development. J. Biol. Chem. 2004, 279:21406-21414.
35. Takahashi A., Iwabuchi K., Suzuki M., Ogasawara K., Nishihira J., Onoe K. Antisense macrophage migration inhibitory factor (MIF) prevents anti-IgM mediated growth arrest and apoptosis of a murine B cell line by regulating cell cycle progression. Microbiol. Immunol. 1999, 43:61-67.
36. Tissir F., Wang C.E., Goffinet A.M. Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development. Brain Res. Dev. Brain Res. 2004, 149:63-71.
37. Tiveron M.C., Cremer H. CXCL12/CXCR4 signalling in neuronal cell migration. Curr. Opin. Neurobiol. 2008, 18:237-244.
38. Valentin G., Haas P., Gilmour D. The chemokine SDF1a coordinates tissue migration through the spatially restricted activation of Cxcr7 and Cxcr4b. Curr. Biol. 2007, 17:1026-1031.
39. Waterman R.E., Bell D.H. Epithelial fusion during early semicircular canal formation in the embryonic zebrafish, Brachydanio rerio. Anat. Rec. 1984, 210:101-114.
40. Weiser W.Y., Temple P.A., Witek-Giannotti J.S., Remold H.G., Clark S.C., David J.R. Molecular cloning of a cDNA encoding a human macrophage migration inhibitory factor. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:7522-7526.
41. Westerfield M. The Zebrafish Book. A guide for the laboratory use fo zebrafish (Danio rerio) 2000, University of Oregen Press, Eugene, OR.
42. Wilson A.L., Shen Y.C., Babb-Clendenon S.G., Rostedt J., Liu B., Barald K.F., Marrs J.A., Liu Q. Cadherin-4 plays a role in the development of zebrafish cranial ganglia and lateral line system. Dev. Dyn. 2007, 236:893-902.
43. Winner M., Meier J., Zierow S., Rendon B.E., Crichlow G.V., Riggs R., Bucala R., Leng L., Smith N., Lolis E., Trent J.O., Mitchell R.A. A novel, macrophage migration inhibitory factor suicide substrate inhibits motility and growth of lung cancer cells. Cancer Res. 2008, 68:7253-7257.
44. Yoder J.A., Haire R.N., Litman G.W. Cloning of two zebrafish cDNAs that share domains with the MHC class II-associated invariant chain. Immunogenetics 1999, 50:84-88.
45. Yoshimoto T., Nishihira J., Tada M., Houkin K., Abe H. Induction of macrophage migration inhibitory factor messenger ribonucleic acid in rat forebrain by reperfusion. Neurosurgery 1997, 41:648-653.
46. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., Littman D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998, 393:595-599.