Macrophage migration inhibitory factor: A central regulator of wound healing

American Journal of Pathology

Volumn 167, Issue 6, 2005, Pages 1561-1574

  Hardman, Matthew J ^a   Waite, Alexander ^a   Zeef, Leo ^a   Burow, Matthew ^b   Nakayama, Toshinori ^c   Ashcroft, Gillian S ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ESTROGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MACROPHAGE MIGRATION INHIBITION FACTOR;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION PROFILING; GENE TARGETING; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; IN VIVO STUDY; INFLAMMATION; MALE; MOUSE; NONHUMAN; NORMAL HUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; TISSUE MICROARRAY; TRANSCRIPTION REGULATION; WILD TYPE; WOUND HEALING;

EID: 28244456280     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)61241-2     Document Type: Article

References (56)

1. Ashcroft GS, Horan MA, Ferguson MW: Aging is associated with reduced deposition of specific extracellular matrix components, an upregulation of angiogenesis, and an altered inflammatory response in a murine incisional wound healing model. J Invest Dermatol 1997, 108:430-437
2. Ashcroft GS, Horan MA, Herrick SE, Tarnuzzer RW, Schultz GS, Ferguson MW: Age-related differences in the temporal and spatial regulation of matrix metalloproteinases (MMPs) in normal skin and acute cutaneous wounds of healthy humans. Cell Tissue Res 1997, 290:581-591
3. Ashcroft, GS, Kielty CM, Horan MA, Ferguson MW: Age-related changes in the temporal and spatial distributions of fibrillin and elastin mRNAs and proteins in acute cutaneous wounds of healthy humans. J Pathol 1997, 183:80-89
4. Ashcroft GS, Mills SJ, Ashworth JJ: Ageing and wound healing. Biogerontology 2002, 3:337-345
5. Ashcroft GS, Dodsworth J, van Boxtel E, Tarnuzzer RW, Horan MA, Schultz GS, Ferguson MW: Estrogen accelerates cutaneous wound healing associated with an increase in TGF-beta1 levels. Nat Med 1997, 3:1209-1215
6. Ashcroft GS, Mills SJ, Lei K, Gibbons L, Jeong MJ, Taniguchi M, Burow M, Horan MA, Wahl SM, Nakayama T: Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J Clin Invest 2003, 111:1309-1318
7. Calandra T, Roger T: Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 2003, 3:791-800
8. Hudson JD, Shoaibi MA, Maestro R, Carnero A, Hannon GJ, Beach DH: A proinflammatory cytokine inhibits p53 tumor suppressor activity, J Exp Med 1999, 190:1375-1382
9. Morand EF, Leech M: Macrophage migration inhibitory factor in rheumatoid arthritis. Front Biosci 2005, 10:12-22
10. Schober A, Bernhagen J, Thiele M, Zeiffer U, Knarren S, Roller M, Bucala R, Weber C: Stabilization of atherosclerotic plaques by blockade of macrophage migration inhibitory factor after vascular injury in apolipoprotein E-deficient mice. Circulation 2004, 109:380-385
11. Bernhagen J, Calandra T, Mitchell RA, Martin SB, Tracey KJ, Voelter W, Manogue KR, Cerami A, Bucala R: MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 1993, 365:756-759
12. Yu CM, Lai KW, Chen YX, Huang XR, Lan HY: Expression of macrophage migration inhibitory factor in acute ischemic myocardial injury. J Histochem Cytochem 2003, 51:625-631
13. Bolstad BM, Irizarry RA, Astrand M, Speed TP: A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003, 19:185-193
14. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA: Identifying biological themes within lists of genes with EASE. Genome Biol 2003, 4:R70
15. Piatetsky-Shapiro G, Tamayo P: Microarray data mining: facing the Challenges, SIGKDD Explorations 2003, 5:1-5
16. Werner S, Grose R: Regulation of wound healing by growth factors and cytokines, Physiol Rev 2003, 83:835-870
17. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA: Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002, 3:349-363
18. Takubo T, Tatsumi N: Microscopic co-distributions of myosin, actin, alpha-actinin and vinculin in human neutrophils during movement. Haematologia 1999, 29:285-294
19. Donate F, Juarez JC, Guan X, Shipulina NV, Plunkett ML, Tel-Tsur Z, Shaw DE, Morgan WT, Mazar AP: Peptides derived from the histidine-proline domain of the histidine-proline-rich glycoprotein bind to tropomyosin and have antiangiogenic and antitumor activities. Cancer Res 2004, 64:5812-5817
20. Richard P, Charron P, Carrier L, Ledeuil C, Cheav T, Pichereau C, Benaiche A, Isrard R, Dubourg O, Burban M, Gueffet JP, Millaire A, Desnos M, Schwartz K, Hainque B, Komajda M, EUROGENE Heart Failure Project: Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation 2003, 107:2227-2232
21. Agah A, Kyriakides TR, Letrondo N, Bjorkblom B, Bornstein P: Thrombospondin 2 levels are increased in aged mice: consequences for cutaneous wound heating and angiogenesis. Matrix Biol 2004 22:539-547
22. Kyriakides TR, Tam JW, Bornstein P: Accelerated wound heating in mice with a disruption of the thrombospondin 2 gene. J Invest Dermatol 1999, 113:782-787
23. Meyer-Siegler K: Macrophage migration inhibitory factor increases MMP-2 activity in DU-145 prostate cells. Cytokine 2000, 12:914-921
24. Chen YH, Layne MD, Chung SW, Ejima K, Baron RM, Yet SF, Perrella MA: Elk-3 is a transcriptional represser of nitric-oxide synthases 2. J Biol Chem 2003, 278:39572-39577
25. McLoughtin RM, Hurst SM, Nowell MA, Harris DA, Horiuohi S, Morgan LW, Wilkinson TS, Yamamoto N, Topley N, Jones SA: Differential regulation of neutrophil-activating chemokines by IL-6 and its soluble receptor isoforms. J Immunol 2004, 172:5676-5683
26. Garnis C, Campbell J, Davies JJ, Macaulay C, Lam S, Lam WL: Involvement of multiple developmental genes on chromosome 1p in lung tumorigenesis. Hum Mol Genet 2005, 14:475-482
27. Mitchell RA: Mechanisms and effectors of MIF-dependent promotion of tumourigenesis. Cell Signal 2004, 16:13-19
28. Thelu J, Rossio P, Favier B: Notch signalling is linked to epidermal cell differentiation level in basal cell carcinoma, psoriasis and wound healing. BMC Dermatol 2002, 2:7
29. Jacinto A, Martinez-Arias A, Martin P: Mechanisms of epithelial fusion and repair. Nat Cell Biol 2001, 3:E117-E123
30. Pedersen TX, Leethanakul C, Patel V, Mitola D, Lund LR, Dano K, Johnsen M, Gutkind JS, Bugge TH: Laser capture microdissection-based in vivo genomic profiling of wound keratinocytes identifies similarities and differences to squamous cell carcinoma. Oncogene 2003, 22:3964-3976
31. Esworthy RS, Aranda R, Martin MG, Doroshow JH, Binder SW, Chu FF: Mice with combined disruption of Gpx1 and Gpx2 genes have colitis. Am J Physiol Gastrointest Liver Physiol 2001, 281:G848-G855
32. Satoskar AR, Bozza M, Rodriguez Sosa M, Lin G, David JR: Migration-inhibitory factor gene-deficient mice are susceptible to cutaneous Leishmania major infection. Infect Immunol 2001, 69:906-911
33. Brown FG, Nikolic-Paterson DJ, Hill PA, Isbel NM, Dowling J, Metz CM, Atkins RC: Urine macrophage migration inhibitory factor reflects the severity of renal injury in human glomerulonephritis. J Am Soc Nephrol 2002, 13(Suppl 1):S7-S13
34. Girard MT, Matsubara M, Kublin C, Tessier MJ, Cintron C, Fini ME: Stromal fibroblasts synthesize collagenase and stromelysin during long-term tissue remodeling. J Cell Sci 1993, 104:1001-1011
35. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC: Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004, 10:858-864
36. Neurath MF, Finotto S, Glimcher LH: The role of Th1/Th2 polarization in mucosal immunity, Nat Med 2002, 8:567-573
37. Pentecost BT: Expression and estrogen regulation of the HEM45 MRNA in human tumor lines and in the rat uterus. J Steroid Biochem Mol Biol 1998, 64:25-33
38. Agrawal S, Agarwal ML, Chatterjee-Kishore M, Stark GR, Chisolm GM: Stall-dependent, p53-independent expression of p21(waf1) modulates oxysterol-induced apoptosis. Mol Cell Biol 2002, 22:1981-1992
39. Thiboutot D, Jabara S, McAllister JM, Sivarajah A, Gilliland K, Cong Z, Clawson G: Human skin is a steroidogenic tissue: steroidogenic enzymes and cofactors are expressed in epidermis, normal sebocytes, and an immortalized sebocyte cell line (SEB-1). J Invest Dermatol 2003, 120:905-914
40. Slominski A, Zjawiony J, Wortsman J, Semak I, Stewart J Pisarchik A, Sweatman T, Marcos J, Dunbar C, Tuckey RC: A novel pathway for sequential transformation of 7-dehydrocholesterol and expression of the P450scc system in mammalian skin. Eur J Biochem 2004, 271:4178-4188
41. Araneo BA, Ryu SY, Barton S, Daynes RA: Dehydroepiandrosterone reduces progressive dermal ischemia caused by thermal injury J Surg Res 1995, 59:250-262
42. Parks WT, Frank DB, Huff C, Renfrew Haft C, Martin J, Meng X, de Caestecker MP, McNally JG, Reddi A, Taylor SI, Roberts AB, Wang T Lechleider RJ: Sorting nexin 6, a novel SNX, interacts with the transforming growth factor-beta family of receptor serine-threonine kinases. J Biol Chem 2001, 276:19332-19339
43. Guzeloglu-Kayisli O, Kayisli UA, AI-Rejjal R, Zheng W, Luleci G, Arici A: Regulation of PTEN (phosphatase and tensin homolog deleted on chromosome 10) expression by estradiol and progesterone in human endometrium. J Clin Endocrinol Metab 2003, 88:5017-5026
44. Kato Y, Fujita N, Kunita A, Sato S, Kaneko M, Osawa M, Tsuruo T: Molecular identification of Aggrus/T1alpha as a platelet aggregation-inducing factor expressed in colorectal tumors. J Biol Chem 2003 278:51599-51605
45. Ashcroft GS, Greenwell-Wild T, Horan MA, Wahl SM, Ferguson MW: Topical estrogen accelerates cutaneous wound healing in aged humans associated with an altered inflammatory response. Am J Pathol 1999, 155:1137-1146
46. Margoils DJ, Knauss J, Bilker W: Hormone replacement therapy and prevention of pressure ulcers and venous leg ulcers. Lancet 2002, 359:675-677
47. Coulombe PA, Tong X, Mazzalupo S, Wang Z, Wong P: Great promises yet to be fulfilled: defining keratin intermediate filament function in vivo. Eur J Cell Biol 2004, 83:735-746
48. Huang X, Griffiths M, Wu J, Farese RV Jr, Sheppard D: Normal development, wound healing, and adenovirus susceptibility in beta5-deficient mice. Mol Cell Biol 2000, 20:755-759
49. Evans MJ, Eckert A, Lai K, Adelman SJ, Harnish DC: Reciprocal antagonism between estrogen receptor and NF-kappaB activity in vivo. Circ Res 2001, 89:823-830
50. Rollerova E, Urbancikova M: Intracellular estrogen receptors, their characterization and function. Endocr Regul 2000, 34:203-218
51. Speir E, Yu ZX, Takeda K, Ferrans, VJ, Cannon RO III: Competition for p300 regulates transcription by estrogen receptors and nuclear factor-kappaB in human coronary smooth muscle cells. Circ Res 2000, 87:1006-1011
52. Fan C, Li Q, Zhang Y, Liu X, Luo M, Abbott D, Zhou W, Engelhardt JF: IkappaBalpha and IkappaBbeta possess injury context-specific functions that uniquely influence hepatic NF-kappaB induction and inflammation. J Clin Invest 2004, 113:746-755
53. Chantome A, Pance A, Gauthier N, Vandroux D, Chenu J, Solary E, Jeannin JF, Reveneau S: Casein kinase II-mediated phosphorylation of NF-kappaB p65 subunit enhances inducible nitric-oxide synthase gene transcription in vivo. J Biol Chem 2004, 279:23953-23960
54. Denkinger CM, Denkinger M, Kort JJ, Metz C, Forsthuber TG: In vivo blockade of macrophage migration inhibitory factor ameliorates acute experimental autoimmune encephalomyelitis by impairing the homing of encephalitogenic T cells to the central nervous system. J Immunol 2003, 170:1274-1282
55. Pence H, Petty WM, Rocklin RE: Suppression of maternal responsiveness to paternal antigen by maternal plasma. J Immunol 1975, 114:525-528
56. Tofoski JG Gill TJ III: The production of migration inhibitory factor and reproductive capacity in allogeneic pregnancies. Am J Pathol 1977, 88:333-344