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Published in: Seminars in Immunopathology 2/2007

01-06-2007 | Review

The role of macrophage migration inhibitory factor in maintaining the immune privilege at the fetal–maternal interface

Authors: Paola Viganò, Marcella Cintorino, Frederick Schatz, Charles J. Lockwood, Felice Arcuri

Published in: Seminars in Immunopathology | Issue 2/2007

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Abstract

Macrophage migration inhibitory factor (MIF) is a pivotal regulator of the innate and adaptive immunity affecting the response and behavior of macrophages and lymphocytes. MIF is also implicated in other fundamental cellular processes including angiogenesis and cell proliferation. Several studies examined the expression of MIF in reproductive organs and tissues and its involvement in different aspects of human and animal reproduction. The goal of this review was to summarize these findings and discuss, in particular, the role of MIF in the maintenance of the immune privilege at the human fetal–maternal interface.
Literature
1.
go back to reference George M, Vaughan JH (1962) In vitro cell migration as a model for delayed hypersensitivity. Proc Soc Exp Biol Med 111:514–521PubMed George M, Vaughan JH (1962) In vitro cell migration as a model for delayed hypersensitivity. Proc Soc Exp Biol Med 111:514–521PubMed
2.
go back to reference Bloom BR, Bennett B (1966) Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 153:80–82PubMed Bloom BR, Bennett B (1966) Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 153:80–82PubMed
3.
go back to reference David JR (1966) Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell–ntigen interaction. Proc Natl Acad Sci USA 56:72–77PubMed David JR (1966) Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell–ntigen interaction. Proc Natl Acad Sci USA 56:72–77PubMed
4.
go back to reference Churchill WH Jr, Piessens WF, Sulis CA, David JR (1975) Macrophages activated as suspension cultures with lymphocyte mediators devoid of antigen become cytotoxic for tumor cells. J Immunol 115:781–786PubMed Churchill WH Jr, Piessens WF, Sulis CA, David JR (1975) Macrophages activated as suspension cultures with lymphocyte mediators devoid of antigen become cytotoxic for tumor cells. J Immunol 115:781–786PubMed
5.
go back to reference Nathan CF, Remold HG, David JR (1973) Characterization of a lymphocyte factor which alters macrophage functions. J Exp Med 137:275–290PubMed Nathan CF, Remold HG, David JR (1973) Characterization of a lymphocyte factor which alters macrophage functions. J Exp Med 137:275–290PubMed
6.
go back to reference Paralkar V, Wistow G (1994) Cloning the human gene for macrophage migration inhibitory factor (MIF). Genomics 19:48–51PubMed Paralkar V, Wistow G (1994) Cloning the human gene for macrophage migration inhibitory factor (MIF). Genomics 19:48–51PubMed
7.
go back to reference Budarf M, McDonald T, Sellinger B, Kozak C, Graham C, Wistow G (1997) Localization of the human gene for macrophage migration inhibitory factor (MIF) to chromosome 22q11.2. Genomics 39:235–236PubMed Budarf M, McDonald T, Sellinger B, Kozak C, Graham C, Wistow G (1997) Localization of the human gene for macrophage migration inhibitory factor (MIF) to chromosome 22q11.2. Genomics 39:235–236PubMed
8.
go back to reference Bozza M, Kolakowski LF Jr, Jenkins NA, Gilbert DJ, Copeland NG, David JR, Gerard C (1995) Structural characterization and chromosomal location of the mouse macrophage migration inhibitory factor gene and pseudogenes. Genomics 27:412–419PubMed Bozza M, Kolakowski LF Jr, Jenkins NA, Gilbert DJ, Copeland NG, David JR, Gerard C (1995) Structural characterization and chromosomal location of the mouse macrophage migration inhibitory factor gene and pseudogenes. Genomics 27:412–419PubMed
9.
go back to reference Mitchell R, Bacher M, Bernhagen J, Pushkarskaya T, Seldin MF, Bucala R (1995) Cloning and characterization of the gene for mouse macrophage migration inhibitory factor (MIF). J Immunol 154:3863–3870PubMed Mitchell R, Bacher M, Bernhagen J, Pushkarskaya T, Seldin MF, Bucala R (1995) Cloning and characterization of the gene for mouse macrophage migration inhibitory factor (MIF). J Immunol 154:3863–3870PubMed
10.
go back to reference Calandra T, Roger T (2003) Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 3:791–800PubMed Calandra T, Roger T (2003) Macrophage migration inhibitory factor: a regulator of innate immunity. Nat Rev Immunol 3:791–800PubMed
11.
go back to reference Magi B, Bini L, Liberatori S, Marzocchi B, Raggiaschi R, Arcuri F, Tripodi SA, Cintorino M, Tosi P, Pallini V (1998) Charge heterogeneity of macrophage migration inhibitory factor (MIF) in human liver and breast tissue. Electrophoresis 19:2010–2013PubMed Magi B, Bini L, Liberatori S, Marzocchi B, Raggiaschi R, Arcuri F, Tripodi SA, Cintorino M, Tosi P, Pallini V (1998) Charge heterogeneity of macrophage migration inhibitory factor (MIF) in human liver and breast tissue. Electrophoresis 19:2010–2013PubMed
12.
go back to reference Suzuki M, Sugimoto H, Nakagawa A, Tanaka I, Nishihira J, Sakai M (1996) Crystal structure of the macrophage migration inhibitory factor from rat liver. Nat Struct Biol 3:259–266PubMed Suzuki M, Sugimoto H, Nakagawa A, Tanaka I, Nishihira J, Sakai M (1996) Crystal structure of the macrophage migration inhibitory factor from rat liver. Nat Struct Biol 3:259–266PubMed
13.
go back to reference Sun HW, Bernhagen J, Bucala R, Lolis E (1996) Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor. Proc Natl Acad Sci USA 93:5191–5196PubMed Sun HW, Bernhagen J, Bucala R, Lolis E (1996) Crystal structure at 2.6-A resolution of human macrophage migration inhibitory factor. Proc Natl Acad Sci USA 93:5191–5196PubMed
14.
go back to reference Blocki FA, Schlievert PM, Wackett LP (1992) Rat liver protein linking chemical and immunological detoxification systems. Nature 360:269–270PubMed Blocki FA, Schlievert PM, Wackett LP (1992) Rat liver protein linking chemical and immunological detoxification systems. Nature 360:269–270PubMed
15.
go back to reference Nishihira J, Kuriyama T, Nishino H, Ishibashi T, Sakai M, Nishi S (1993) Purification and characterization of human macrophage migration inhibitory factor: evidence for specific binding to glutathione and formation of subunit structure. Biochem Mol Biol Int 31:841–850PubMed Nishihira J, Kuriyama T, Nishino H, Ishibashi T, Sakai M, Nishi S (1993) Purification and characterization of human macrophage migration inhibitory factor: evidence for specific binding to glutathione and formation of subunit structure. Biochem Mol Biol Int 31:841–850PubMed
16.
go back to reference Sun HW, Swope M, Cinquina C, Bedarkar S, Bernhagen J, Bucala R, Lolis E (1996) The subunit structure of human macrophage migration inhibitory factor: evidence for a trimer. Protein Eng 9:631–635PubMed Sun HW, Swope M, Cinquina C, Bedarkar S, Bernhagen J, Bucala R, Lolis E (1996) The subunit structure of human macrophage migration inhibitory factor: evidence for a trimer. Protein Eng 9:631–635PubMed
17.
go back to reference Mischke R, Kleemann R, Brunner H, Bernhagen J (1998) Cross-linking and mutational analysis of the oligomerization state of the cytokine macrophage migration inhibitory factor (MIF). FEBS Lett 427:85–90PubMed Mischke R, Kleemann R, Brunner H, Bernhagen J (1998) Cross-linking and mutational analysis of the oligomerization state of the cytokine macrophage migration inhibitory factor (MIF). FEBS Lett 427:85–90PubMed
18.
go back to reference Philo JS, Yang TH, LaBarre M (2004) Re-examining the oligomerization state of macrophage migration inhibitory factor (MIF) in solution. Biophys Chem 108:77–87PubMed Philo JS, Yang TH, LaBarre M (2004) Re-examining the oligomerization state of macrophage migration inhibitory factor (MIF) in solution. Biophys Chem 108:77–87PubMed
19.
go back to reference Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA, Bucala R (2003) MIF signal transduction initiated by binding to CD74. J Exp Med 197:1467–1476PubMed Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA, Bucala R (2003) MIF signal transduction initiated by binding to CD74. J Exp Med 197:1467–1476PubMed
20.
go back to reference Beswick EJ, Pinchuk IV, Suarez G, Sierra JC, Reyes VE (2006) Helicobacter pylori CagA-dependent macrophage migration inhibitory factor produced by gastric epithelial cells binds to CD74 and stimulates procarcinogenic events. J Immunol 176:6794–6801PubMed Beswick EJ, Pinchuk IV, Suarez G, Sierra JC, Reyes VE (2006) Helicobacter pylori CagA-dependent macrophage migration inhibitory factor produced by gastric epithelial cells binds to CD74 and stimulates procarcinogenic events. J Immunol 176:6794–6801PubMed
21.
go back to reference Meyer-Siegler KL, Iczkowski KA, Leng L, Bucala R, Vera PL (2006) Inhibition of macrophage migration inhibitory factor or its receptor (CD74) attenuates growth and invasion of DU-145 prostate cancer cells. J Immunol 177:8730–8739PubMed Meyer-Siegler KL, Iczkowski KA, Leng L, Bucala R, Vera PL (2006) Inhibition of macrophage migration inhibitory factor or its receptor (CD74) attenuates growth and invasion of DU-145 prostate cancer cells. J Immunol 177:8730–8739PubMed
22.
go back to reference Shi X, Leng L, Wang T, Wang W, Du X, Li J, McDonald C, Chen Z, Murphy JW, Lolis E, Noble P, Knudson W, Bucala R (2006) CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 25:595–606PubMed Shi X, Leng L, Wang T, Wang W, Du X, Li J, McDonald C, Chen Z, Murphy JW, Lolis E, Noble P, Knudson W, Bucala R (2006) CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 25:595–606PubMed
23.
go back to reference Bozza M, Satoskar AR, Lin G, Lu B, Humbles AA, Gerard C, David JR (1999) Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J Exp Med 189:341–346PubMed Bozza M, Satoskar AR, Lin G, Lu B, Humbles AA, Gerard C, David JR (1999) Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis. J Exp Med 189:341–346PubMed
24.
go back to reference Bernhagen J, Bacher M, Calandra T, Metz CN, Doty SB, Donnelly T, Bucala R (1996) An essential role for macrophage migration inhibitory factor in the tuberculin delayed-type hypersensitivity reaction. J Exp Med 183:277–282PubMed Bernhagen J, Bacher M, Calandra T, Metz CN, Doty SB, Donnelly T, Bucala R (1996) An essential role for macrophage migration inhibitory factor in the tuberculin delayed-type hypersensitivity reaction. J Exp Med 183:277–282PubMed
25.
go back to reference Leech M, Metz C, Hall P, Hutchinson P, Gianis K, Smith M, Weedon H, Holdsworth SR, Bucala R, Morand EF (1999) Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids. Arthritis Rheum 42:1601–1608PubMed Leech M, Metz C, Hall P, Hutchinson P, Gianis K, Smith M, Weedon H, Holdsworth SR, Bucala R, Morand EF (1999) Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids. Arthritis Rheum 42:1601–1608PubMed
26.
go back to reference Kleemann R, Kapurniotu A, Frank RW, Gessner A, Mischke R, Flieger O, Juttner S, Brunner H, Bernhagen J (1998) Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J Mol Biol 280:85–102PubMed Kleemann R, Kapurniotu A, Frank RW, Gessner A, Mischke R, Flieger O, Juttner S, Brunner H, Bernhagen J (1998) Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase. J Mol Biol 280:85–102PubMed
27.
go back to reference Bini L, Magi B, Marzocchi B, Arcuri F, Tripodi S, Cintorino M, Sanchez JC, Frutiger S, Hughes G, Pallini V, Hochstrasser DF, Tosi P (1997) Protein expression profiles in human breast ductal carcinoma and histologically normal tissue. Electrophoresis 18:2832–2841PubMed Bini L, Magi B, Marzocchi B, Arcuri F, Tripodi S, Cintorino M, Sanchez JC, Frutiger S, Hughes G, Pallini V, Hochstrasser DF, Tosi P (1997) Protein expression profiles in human breast ductal carcinoma and histologically normal tissue. Electrophoresis 18:2832–2841PubMed
28.
go back to reference Meyer-Siegler K, Hudson PB (1996) Enhanced expression of macrophage migration inhibitory factor in prostatic adenocarcinoma metastases. Urology 48:448–452PubMed Meyer-Siegler K, Hudson PB (1996) Enhanced expression of macrophage migration inhibitory factor in prostatic adenocarcinoma metastases. Urology 48:448–452PubMed
29.
go back to reference del Vecchio MT, Tripodi SA, Arcuri F, Pergola L, Hako L, Vatti R, Cintorino M (2000) Macrophage migration inhibitory factor in prostatic adenocarcinoma: correlation with tumor grading and combination endocrine treatment-related changes. Prostate 45:51–57PubMed del Vecchio MT, Tripodi SA, Arcuri F, Pergola L, Hako L, Vatti R, Cintorino M (2000) Macrophage migration inhibitory factor in prostatic adenocarcinoma: correlation with tumor grading and combination endocrine treatment-related changes. Prostate 45:51–57PubMed
30.
go back to reference Chesney J, Metz C, Bacher M, Peng T, Meinhardt A, Bucala R (1999) An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol Med 5:181–191PubMed Chesney J, Metz C, Bacher M, Peng T, Meinhardt A, Bucala R (1999) An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Mol Med 5:181–191PubMed
31.
go back to reference White ES, Flaherty KR, Carskadon S, Brant A, Iannettoni MD, Yee J, Orringer MB, Arenberg DA (2003) Macrophage migration inhibitory factor and CXC chemokine expression in non-small cell lung cancer: role in angiogenesis and prognosis. Clin Cancer Res 9:853–860PubMed White ES, Flaherty KR, Carskadon S, Brant A, Iannettoni MD, Yee J, Orringer MB, Arenberg DA (2003) Macrophage migration inhibitory factor and CXC chemokine expression in non-small cell lung cancer: role in angiogenesis and prognosis. Clin Cancer Res 9:853–860PubMed
32.
go back to reference Shimizu T, Abe R, Nakamura H, Ohkawara A, Suzuki M, Nishihira J (1999) High expression of macrophage migration inhibitory factor in human melanoma cells and its role in tumor cell growth and angiogenesis. Biochem Biophys Res Commun 264:751–758PubMed Shimizu T, Abe R, Nakamura H, Ohkawara A, Suzuki M, Nishihira J (1999) High expression of macrophage migration inhibitory factor in human melanoma cells and its role in tumor cell growth and angiogenesis. Biochem Biophys Res Commun 264:751–758PubMed
33.
go back to reference Nishihira J (1998) Novel pathophysiological aspects of macrophage migration inhibitory factor (review). Int J Mol Med 2:17–28PubMed Nishihira J (1998) Novel pathophysiological aspects of macrophage migration inhibitory factor (review). Int J Mol Med 2:17–28PubMed
34.
go back to reference Baugh JA, Bucala R (2002) Macrophage migration inhibitory factor. Crit Care Med 30:S27–S35 Baugh JA, Bucala R (2002) Macrophage migration inhibitory factor. Crit Care Med 30:S27–S35
35.
go back to reference Lue H, Kleemann R, Calandra T, Roger T, Bernhagen J (2002) Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect 4:449–460PubMed Lue H, Kleemann R, Calandra T, Roger T, Bernhagen J (2002) Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect 4:449–460PubMed
36.
go back to reference Mitchell RA (2004) Mechanisms and effectors of MIF-dependent promotion of tumourigenesis. Cell Signal 16:13–19PubMed Mitchell RA (2004) Mechanisms and effectors of MIF-dependent promotion of tumourigenesis. Cell Signal 16:13–19PubMed
37.
go back to reference Bacher M, Metz CN, Calandra T, Mayer K, Chesney J, Lohoff M, Gemsa D, Donnelly T, Bucala R (1996) An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc Natl Acad Sci USA 93:7849–7854PubMed Bacher M, Metz CN, Calandra T, Mayer K, Chesney J, Lohoff M, Gemsa D, Donnelly T, Bucala R (1996) An essential regulatory role for macrophage migration inhibitory factor in T-cell activation. Proc Natl Acad Sci USA 93:7849–7854PubMed
38.
go back to reference Calandra T, Spiegel LA, Metz CN, Bucala R (1998) Macrophage migration inhibitory factor is a critical mediator of the activation of immune cells by exotoxins of Gram-positive bacteria. Proc Natl Acad Sci USA 95:11383–11388PubMed Calandra T, Spiegel LA, Metz CN, Bucala R (1998) Macrophage migration inhibitory factor is a critical mediator of the activation of immune cells by exotoxins of Gram-positive bacteria. Proc Natl Acad Sci USA 95:11383–11388PubMed
39.
go back to reference Abe R, Peng T, Sailors J, Bucala R, Metz CN (2001) Regulation of the CTL response by macrophage migration inhibitory factor. J Immunol 166:747–753PubMed Abe R, Peng T, Sailors J, Bucala R, Metz CN (2001) Regulation of the CTL response by macrophage migration inhibitory factor. J Immunol 166:747–753PubMed
40.
go back to reference Yan X, Orentas RJ, Johnson BD (2006) Tumor-derived macrophage migration inhibitory factor (MIF) inhibits T lymphocyte activation. Cytokine 33:188–198PubMed Yan X, Orentas RJ, Johnson BD (2006) Tumor-derived macrophage migration inhibitory factor (MIF) inhibits T lymphocyte activation. Cytokine 33:188–198PubMed
41.
go back to reference Bernhagen J, Calandra T, Mitchell RA, Martin SB, Tracey KJ, Voelter W, Manogue KR, Cerami A, Bucala R (1993) MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 365:756–759PubMed Bernhagen J, Calandra T, Mitchell RA, Martin SB, Tracey KJ, Voelter W, Manogue KR, Cerami A, Bucala R (1993) MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia. Nature 365:756–759PubMed
42.
go back to reference Bacher M, Meinhardt A, Lan HY, Mu W, Metz CN, Chesney JA, Calandra T, Gemsa D, Donnelly T, Atkins RC, Bucala R (1997) Migration inhibitory factor expression in experimentally induced endotoxemia. Am J Pathol 150:235–246PubMed Bacher M, Meinhardt A, Lan HY, Mu W, Metz CN, Chesney JA, Calandra T, Gemsa D, Donnelly T, Atkins RC, Bucala R (1997) Migration inhibitory factor expression in experimentally induced endotoxemia. Am J Pathol 150:235–246PubMed
43.
go back to reference Calandra T, Echtenacher B, Roy DL, Pugin J, Metz CN, Hultner L, Heumann D, Mannel D, Bucala R, Glauser MP (2000) Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat Med 6:164–170PubMed Calandra T, Echtenacher B, Roy DL, Pugin J, Metz CN, Hultner L, Heumann D, Mannel D, Bucala R, Glauser MP (2000) Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat Med 6:164–170PubMed
44.
go back to reference Lind M, Trindade MC, Nakashima Y, Schurman DJ, Goodman SB, Smith L (1999) Chemotaxis and activation of particle-challenged human monocytes in response to monocyte migration inhibitory factor and C-C chemokines. J Biomed Mater Res 48:246–250PubMed Lind M, Trindade MC, Nakashima Y, Schurman DJ, Goodman SB, Smith L (1999) Chemotaxis and activation of particle-challenged human monocytes in response to monocyte migration inhibitory factor and C-C chemokines. J Biomed Mater Res 48:246–250PubMed
45.
go back to reference Hermanowski-Vosatka A, Mundt SS, Ayala JM, Goyal S, Hanlon WA, Czerwinski RM, Wright SD, Whitman CP (1999) Enzymatically inactive macrophage migration inhibitory factor inhibits monocyte chemotaxis and random migration. Biochemistry 38:12841–12849PubMed Hermanowski-Vosatka A, Mundt SS, Ayala JM, Goyal S, Hanlon WA, Czerwinski RM, Wright SD, Whitman CP (1999) Enzymatically inactive macrophage migration inhibitory factor inhibits monocyte chemotaxis and random migration. Biochemistry 38:12841–12849PubMed
46.
go back to reference Gregory JL, Morand EF, McKeown SJ, Ralph JA, Hall P, Yang YH, McColl SR, Hickey MJ (2006) Macrophage migration inhibitory factor induces macrophage recruitment via CC chemokine ligand 2. J Immunol 177:8072–8079PubMed Gregory JL, Morand EF, McKeown SJ, Ralph JA, Hall P, Yang YH, McColl SR, Hickey MJ (2006) Macrophage migration inhibitory factor induces macrophage recruitment via CC chemokine ligand 2. J Immunol 177:8072–8079PubMed
47.
go back to reference Calandra T, Bernhagen J, Mitchell RA, Bucala R (1994) The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 179:1895–1902PubMed Calandra T, Bernhagen J, Mitchell RA, Bucala R (1994) The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 179:1895–1902PubMed
48.
go back to reference Roger T, David J, Glauser MP, Calandra T (2001) MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature 414:920–924PubMed Roger T, David J, Glauser MP, Calandra T (2001) MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature 414:920–924PubMed
49.
go back to reference Onodera S, Suzuki K, Matsuno T, Kaneda K, Takagi M, Nishihira J (1997) Macrophage migration inhibitory factor induces phagocytosis of foreign particles by macrophages in autocrine and paracrine fashion. Immunology 92:131–137PubMed Onodera S, Suzuki K, Matsuno T, Kaneda K, Takagi M, Nishihira J (1997) Macrophage migration inhibitory factor induces phagocytosis of foreign particles by macrophages in autocrine and paracrine fashion. Immunology 92:131–137PubMed
50.
go back to reference Juttner S, Bernhagen J, Metz CN, Rollinghoff M, Bucala R, Gessner A (1998) Migration inhibitory factor induces killing of Leishmania major by macrophages: dependence on reactive nitrogen intermediates and endogenous TNF-alpha. J Immunol 161:2383–2390PubMed Juttner S, Bernhagen J, Metz CN, Rollinghoff M, Bucala R, Gessner A (1998) Migration inhibitory factor induces killing of Leishmania major by macrophages: dependence on reactive nitrogen intermediates and endogenous TNF-alpha. J Immunol 161:2383–2390PubMed
51.
go back to reference Pozzi LA, Weiser WY (1992) Human recombinant migration inhibitory factor activates human macrophages to kill tumor cells. Cell Immunol 145:372–379PubMed Pozzi LA, Weiser WY (1992) Human recombinant migration inhibitory factor activates human macrophages to kill tumor cells. Cell Immunol 145:372–379PubMed
52.
go back to reference Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, Cerami A, Bucala R (1995) MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377:68–71PubMed Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, Cerami A, Bucala R (1995) MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377:68–71PubMed
53.
go back to reference Daun JM, Cannon JG (2000) Macrophage migration inhibitory factor antagonizes hydrocortisone-induced increases in cytosolic IkappaBalpha. Am J Physiol Regul Integr Comp Physiol 279:R1043–R1049PubMed Daun JM, Cannon JG (2000) Macrophage migration inhibitory factor antagonizes hydrocortisone-induced increases in cytosolic IkappaBalpha. Am J Physiol Regul Integr Comp Physiol 279:R1043–R1049PubMed
54.
go back to reference Apte RS, Sinha D, Mayhew E, Wistow GJ, Niederkorn JY (1998) Cutting edge: role of macrophage migration inhibitory factor in inhibiting NK cell activity and preserving immune privilege. J Immunol 160:5693–5696PubMed Apte RS, Sinha D, Mayhew E, Wistow GJ, Niederkorn JY (1998) Cutting edge: role of macrophage migration inhibitory factor in inhibiting NK cell activity and preserving immune privilege. J Immunol 160:5693–5696PubMed
55.
go back to reference Repp AC, Mayhew ES, Apte S, Niederkorn JY (2000) Human uveal melanoma cells produce macrophage migration-inhibitory factor to prevent lysis by NK cells. J Immunol 165:710–715PubMed Repp AC, Mayhew ES, Apte S, Niederkorn JY (2000) Human uveal melanoma cells produce macrophage migration-inhibitory factor to prevent lysis by NK cells. J Immunol 165:710–715PubMed
56.
go back to reference Arcuri F, Cintorino M, Carducci A, Papa S, Riparbelli MG, Mangioni S, Di Blasio AM, Tosi P, Vigano P (2006) Human decidual natural killer cells as a source and target of macrophage migration inhibitory factor. Reproduction 131:175–182PubMed Arcuri F, Cintorino M, Carducci A, Papa S, Riparbelli MG, Mangioni S, Di Blasio AM, Tosi P, Vigano P (2006) Human decidual natural killer cells as a source and target of macrophage migration inhibitory factor. Reproduction 131:175–182PubMed
57.
go back to reference Esumi N, Budarf M, Ciccarelli L, Sellinger B, Kozak CA, Wistow G (1998) Conserved gene structure and genomic linkage for d-dopachrome tautomerase (DDT) and MIF. Mamm Genome 9:753–757PubMed Esumi N, Budarf M, Ciccarelli L, Sellinger B, Kozak CA, Wistow G (1998) Conserved gene structure and genomic linkage for d-dopachrome tautomerase (DDT) and MIF. Mamm Genome 9:753–757PubMed
58.
go back to reference Rosengren E, Bucala R, Aman P, Jacobsson L, Odh G, Metz CN, Rorsman H (1996) The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction. Mol Med 2:143–149PubMed Rosengren E, Bucala R, Aman P, Jacobsson L, Odh G, Metz CN, Rorsman H (1996) The immunoregulatory mediator macrophage migration inhibitory factor (MIF) catalyzes a tautomerization reaction. Mol Med 2:143–149PubMed
59.
go back to reference Rosengren E, Aman P, Thelin S, Hansson C, Ahlfors S, Bjork P, Jacobsson L, Rorsman H (1997) The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase. FEBS Lett 417:85–88PubMed Rosengren E, Aman P, Thelin S, Hansson C, Ahlfors S, Bjork P, Jacobsson L, Rorsman H (1997) The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase. FEBS Lett 417:85–88PubMed
60.
go back to reference Matsunaga J, Sinha D, Pannell L, Santis C, Solano F, Wistow GJ, Hearing VJ (1999) Enzyme activity of macrophage migration inhibitory factor toward oxidized catecholamines. J Biol Chem 274:3268–3271PubMed Matsunaga J, Sinha D, Pannell L, Santis C, Solano F, Wistow GJ, Hearing VJ (1999) Enzyme activity of macrophage migration inhibitory factor toward oxidized catecholamines. J Biol Chem 274:3268–3271PubMed
61.
go back to reference Bendrat K, Al-Abed Y, Callaway DJ, Peng T, Calandra T, Metz CN, Bucala R (1997) Biochemical and mutational investigations of the enzymatic activity of macrophage migration inhibitory factor. Biochemistry 36:15356–15362PubMed Bendrat K, Al-Abed Y, Callaway DJ, Peng T, Calandra T, Metz CN, Bucala R (1997) Biochemical and mutational investigations of the enzymatic activity of macrophage migration inhibitory factor. Biochemistry 36:15356–15362PubMed
62.
go back to reference Mischke R, Gessner A, Kapurniotu A, Juttner S, Kleemann R, Brunner H, Bernhagen J (1997) Structure activity studies of the cytokine macrophage migration inhibitory factor (MIF) reveal a critical role for its carboxy terminus. FEBS Lett 414:226–232PubMed Mischke R, Gessner A, Kapurniotu A, Juttner S, Kleemann R, Brunner H, Bernhagen J (1997) Structure activity studies of the cytokine macrophage migration inhibitory factor (MIF) reveal a critical role for its carboxy terminus. FEBS Lett 414:226–232PubMed
63.
go back to reference Wen Y, Li GW, Bekhor I (1996) Lens epithelial cell mRNA. III. Elevated expression of macrophage migration inhibitory factor mRNA in galactose cataracts. Curr Eye Res 15:125–130PubMed Wen Y, Li GW, Bekhor I (1996) Lens epithelial cell mRNA. III. Elevated expression of macrophage migration inhibitory factor mRNA in galactose cataracts. Curr Eye Res 15:125–130PubMed
64.
go back to reference Mitchell RA, Metz CN, Peng T, Bucala R (1999) Sustained mitogen-activated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF). Regulatory role in cell proliferation and glucocorticoid action. J Biol Chem 274:18100–18106PubMed Mitchell RA, Metz CN, Peng T, Bucala R (1999) Sustained mitogen-activated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF). Regulatory role in cell proliferation and glucocorticoid action. J Biol Chem 274:18100–18106PubMed
65.
go back to reference Kleemann R, Hausser A, Geiger G, Mischke R, Burger-Kentischer A, Flieger O, Johannes FJ, Roger T, Calandra T, Kapurniotu A, Grell M, Finkelmeier D, Brunner H, Bernhagen J (2000) Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature 408:211–216PubMed Kleemann R, Hausser A, Geiger G, Mischke R, Burger-Kentischer A, Flieger O, Johannes FJ, Roger T, Calandra T, Kapurniotu A, Grell M, Finkelmeier D, Brunner H, Bernhagen J (2000) Intracellular action of the cytokine MIF to modulate AP-1 activity and the cell cycle through Jab1. Nature 408:211–216PubMed
66.
go back to reference Takahashi N, Nishihira J, Sato Y, Kondo M, Ogawa H, Ohshima T, Une Y, Todo S (1998) Involvement of macrophage migration inhibitory factor (MIF) in the mechanism of tumor cell growth. Mol Med 4:707–714PubMed Takahashi N, Nishihira J, Sato Y, Kondo M, Ogawa H, Ohshima T, Une Y, Todo S (1998) Involvement of macrophage migration inhibitory factor (MIF) in the mechanism of tumor cell growth. Mol Med 4:707–714PubMed
67.
go back to reference Ren Y, Chan HM, Fan J, Xie Y, Chen YX, Li W, Jiang GP, Liu Q, Meinhardt A, Tam PK (2006) Inhibition of tumor growth and metastasis in vitro and in vivo by targeting macrophage migration inhibitory factor in human neuroblastoma. Oncogene 25:3501–3508PubMed Ren Y, Chan HM, Fan J, Xie Y, Chen YX, Li W, Jiang GP, Liu Q, Meinhardt A, Tam PK (2006) Inhibition of tumor growth and metastasis in vitro and in vivo by targeting macrophage migration inhibitory factor in human neuroblastoma. Oncogene 25:3501–3508PubMed
68.
go back to reference Ogawa H, Nishihira J, Sato Y, Kondo M, Takahashi N, Oshima T, Todo S (2000) An antibody for macrophage migration inhibitory factor suppresses tumour growth and inhibits tumour-associated angiogenesis. Cytokine 12:309–314PubMed Ogawa H, Nishihira J, Sato Y, Kondo M, Takahashi N, Oshima T, Todo S (2000) An antibody for macrophage migration inhibitory factor suppresses tumour growth and inhibits tumour-associated angiogenesis. Cytokine 12:309–314PubMed
69.
go back to reference Ren Y, Tsui HT, Poon RT, Ng IO, Li Z, Chen Y, Jiang G, Lau C, Yu WC, Bacher M, Fan ST (2003) Macrophage migration inhibitory factor: roles in regulating tumor cell migration and expression of angiogenic factors in hepatocellular carcinoma. Int J Cancer 107:22–29PubMed Ren Y, Tsui HT, Poon RT, Ng IO, Li Z, Chen Y, Jiang G, Lau C, Yu WC, Bacher M, Fan ST (2003) Macrophage migration inhibitory factor: roles in regulating tumor cell migration and expression of angiogenic factors in hepatocellular carcinoma. Int J Cancer 107:22–29PubMed
70.
go back to reference Hira E, Ono T, Dhar DK, El-Assal ON, Hishikawa Y, Yamanoi A, Nagasue N (2005) Overexpression of macrophage migration inhibitory factor induces angiogenesis and deteriorates prognosis after radical resection for hepatocellular carcinoma. Cancer 103:588–598PubMed Hira E, Ono T, Dhar DK, El-Assal ON, Hishikawa Y, Yamanoi A, Nagasue N (2005) Overexpression of macrophage migration inhibitory factor induces angiogenesis and deteriorates prognosis after radical resection for hepatocellular carcinoma. Cancer 103:588–598PubMed
71.
go back to reference Shun CT, Lin JT, Huang SP, Lin MT, Wu MS (2005) Expression of macrophage migration inhibitory factor is associated with enhanced angiogenesis and advanced stage in gastric carcinomas. World J Gastroenterol 11:3767–3771PubMed Shun CT, Lin JT, Huang SP, Lin MT, Wu MS (2005) Expression of macrophage migration inhibitory factor is associated with enhanced angiogenesis and advanced stage in gastric carcinomas. World J Gastroenterol 11:3767–3771PubMed
72.
go back to reference Ren Y, Law S, Huang X, Lee PY, Bacher M, Srivastava G, Wong J (2005) Macrophage migration inhibitory factor stimulates angiogenic factor expression and correlates with differentiation and lymph node status in patients with esophageal squamous cell carcinoma. Ann Surg 242:55–63PubMed Ren Y, Law S, Huang X, Lee PY, Bacher M, Srivastava G, Wong J (2005) Macrophage migration inhibitory factor stimulates angiogenic factor expression and correlates with differentiation and lymph node status in patients with esophageal squamous cell carcinoma. Ann Surg 242:55–63PubMed
73.
go back to reference Yang Y, Degranpre P, Kharfi A, Akoum A (2000) Identification of macrophage migration inhibitory factor as a potent endothelial cell growth-promoting agent released by ectopic human endometrial cells. J Clin Endocrinol Metab 85:4721–4727PubMed Yang Y, Degranpre P, Kharfi A, Akoum A (2000) Identification of macrophage migration inhibitory factor as a potent endothelial cell growth-promoting agent released by ectopic human endometrial cells. J Clin Endocrinol Metab 85:4721–4727PubMed
74.
go back to reference Lue H, Kapurniotu A, Fingerle-Rowson G, Roger T, Leng L, Thiele M, Calandra T, Bucala R, Bernhagen J (2006) Rapid and transient activation of the ERK MAPK signalling pathway by macrophage migration inhibitory factor (MIF) and dependence on JAB1/CSN5 and Src kinase activity. Cell Signal 18:688–703PubMed Lue H, Kapurniotu A, Fingerle-Rowson G, Roger T, Leng L, Thiele M, Calandra T, Bucala R, Bernhagen J (2006) Rapid and transient activation of the ERK MAPK signalling pathway by macrophage migration inhibitory factor (MIF) and dependence on JAB1/CSN5 and Src kinase activity. Cell Signal 18:688–703PubMed
75.
go back to reference Aeberli D, Yang Y, Mansell A, Santos L, Leech M, Morand EF (2006) Endogenous macrophage migration inhibitory factor modulates glucocorticoid sensitivity in macrophages via effects on MAP kinase phosphatase-1 and p38 MAP kinase. FEBS Lett 580:974–981PubMed Aeberli D, Yang Y, Mansell A, Santos L, Leech M, Morand EF (2006) Endogenous macrophage migration inhibitory factor modulates glucocorticoid sensitivity in macrophages via effects on MAP kinase phosphatase-1 and p38 MAP kinase. FEBS Lett 580:974–981PubMed
76.
go back to reference Amin MA, Haas CS, Zhu K, Mansfield PJ, Kim MJ, Lackowski NP, Koch AE (2006) Migration inhibitory factor up-regulates vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 via Src, PI3 kinase, and NFkappaB. Blood 107:2252–2261PubMed Amin MA, Haas CS, Zhu K, Mansfield PJ, Kim MJ, Lackowski NP, Koch AE (2006) Migration inhibitory factor up-regulates vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 via Src, PI3 kinase, and NFkappaB. Blood 107:2252–2261PubMed
77.
go back to reference Lacey D, Sampey A, Mitchell R, Bucala R, Santos L, Leech M, Morand E (2003) Control of fibroblast-like synoviocyte proliferation by macrophage migration inhibitory factor. Arthritis Rheum 48:103–109PubMed Lacey D, Sampey A, Mitchell R, Bucala R, Santos L, Leech M, Morand E (2003) Control of fibroblast-like synoviocyte proliferation by macrophage migration inhibitory factor. Arthritis Rheum 48:103–109PubMed
78.
go back to reference Hudson JD, Shoaibi MA, Maestro R, Carnero A, Hannon GJ, Beach DH (1999) A proinflammatory cytokine inhibits p53 tumor suppressor activity. J Exp Med 190:1375–1382PubMed Hudson JD, Shoaibi MA, Maestro R, Carnero A, Hannon GJ, Beach DH (1999) A proinflammatory cytokine inhibits p53 tumor suppressor activity. J Exp Med 190:1375–1382PubMed
79.
go back to reference Mitchell RA, Liao H, Chesney J, Fingerle-Rowson G, Baugh J, David J, Bucala R (2002) Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci USA 99:345–350PubMed Mitchell RA, Liao H, Chesney J, Fingerle-Rowson G, Baugh J, David J, Bucala R (2002) Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci USA 99:345–350PubMed
80.
go back to reference Petrenko O, Fingerle-Rowson G, Peng T, Mitchell RA, Metz CN (2003) Macrophage migration inhibitory factor deficiency is associated with altered cell growth and reduced susceptibility to Ras-mediated transformation. J Biol Chem 278:11078–11085PubMed Petrenko O, Fingerle-Rowson G, Peng T, Mitchell RA, Metz CN (2003) Macrophage migration inhibitory factor deficiency is associated with altered cell growth and reduced susceptibility to Ras-mediated transformation. J Biol Chem 278:11078–11085PubMed
81.
go back to reference Petrenko O, Moll UM (2005) Macrophage migration inhibitory factor MIF interferes with the Rb-E2F pathway. Mol Cell 17:225–236PubMed Petrenko O, Moll UM (2005) Macrophage migration inhibitory factor MIF interferes with the Rb-E2F pathway. Mol Cell 17:225–236PubMed
82.
go back to reference Claret FX, Hibi M, Dhut S, Toda T, Karin M (1996) A new group of conserved coactivators that increase the specificity of AP-1 transcription factors. Nature 383:453–457PubMed Claret FX, Hibi M, Dhut S, Toda T, Karin M (1996) A new group of conserved coactivators that increase the specificity of AP-1 transcription factors. Nature 383:453–457PubMed
83.
go back to reference Deng XW, Dubiel W, Wei N, Hofmann K, Mundt K, Colicelli J, Kato J, Naumann M, Segal D, Seeger M, Carr A, Glickman M, Chamovitz DA (2000) Unified nomenclature for the COP9 signalosome and its subunits: an essential regulator of development. Trends Genet 16:202–203PubMed Deng XW, Dubiel W, Wei N, Hofmann K, Mundt K, Colicelli J, Kato J, Naumann M, Segal D, Seeger M, Carr A, Glickman M, Chamovitz DA (2000) Unified nomenclature for the COP9 signalosome and its subunits: an essential regulator of development. Trends Genet 16:202–203PubMed
84.
go back to reference Shaulian E, Karin M (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4:E131–E136PubMed Shaulian E, Karin M (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4:E131–E136PubMed
85.
go back to reference Tomoda K, Kubota Y, Kato J (1999) Degradation of the cyclin-dependent-kinase inhibitor p27Kip1 is instigated by Jab1. Nature 398:160–165PubMed Tomoda K, Kubota Y, Kato J (1999) Degradation of the cyclin-dependent-kinase inhibitor p27Kip1 is instigated by Jab1. Nature 398:160–165PubMed
86.
go back to reference Suzuki H, Kanagawa H, Nishihira J (1996) Evidence for the presence of macrophage migration inhibitory factor in murine reproductive organs and early embryos. Immunol Lett 51:141–147PubMed Suzuki H, Kanagawa H, Nishihira J (1996) Evidence for the presence of macrophage migration inhibitory factor in murine reproductive organs and early embryos. Immunol Lett 51:141–147PubMed
87.
go back to reference Wada S, Fujimoto S, Mizue Y, Nishihira J (1997) Macrophage migration inhibitory factor in the human ovary: presence in the follicular fluids and production by granulosa cells. Biochem Mol Biol Int 41:805–814PubMed Wada S, Fujimoto S, Mizue Y, Nishihira J (1997) Macrophage migration inhibitory factor in the human ovary: presence in the follicular fluids and production by granulosa cells. Biochem Mol Biol Int 41:805–814PubMed
88.
go back to reference Matsuura T, Sugimura M, Iwaki T, Ohashi R, Kanayama N, Nishihira J (2002) Anti-macrophage inhibitory factor antibody inhibits PMSG-hCG-induced follicular growth and ovulation in mice. J Assist Reprod Genet 19:591–595PubMed Matsuura T, Sugimura M, Iwaki T, Ohashi R, Kanayama N, Nishihira J (2002) Anti-macrophage inhibitory factor antibody inhibits PMSG-hCG-induced follicular growth and ovulation in mice. J Assist Reprod Genet 19:591–595PubMed
89.
go back to reference Bove SE, Petroff MG, Nishibori M, Pate JL (2000) Macrophage migration inhibitory factor in the bovine corpus luteum: characterization of steady-state messenger ribonucleic acid and immunohistochemical localization. Biol Reprod 62:879–885PubMed Bove SE, Petroff MG, Nishibori M, Pate JL (2000) Macrophage migration inhibitory factor in the bovine corpus luteum: characterization of steady-state messenger ribonucleic acid and immunohistochemical localization. Biol Reprod 62:879–885PubMed
90.
go back to reference Arcuri F, Ricci C, Ietta F, Cintorino M, Tripodi SA, Cetin I, Garzia E, Schatz F, Klemi P, Santopietro R, Paulesu L (2001) Macrophage migration inhibitory factor in the human endometrium: expression and localization during the menstrual cycle and early pregnancy. Biol Reprod 64:1200–1205PubMed Arcuri F, Ricci C, Ietta F, Cintorino M, Tripodi SA, Cetin I, Garzia E, Schatz F, Klemi P, Santopietro R, Paulesu L (2001) Macrophage migration inhibitory factor in the human endometrium: expression and localization during the menstrual cycle and early pregnancy. Biol Reprod 64:1200–1205PubMed
91.
go back to reference Kats R, Al-Akoum M, Guay S, Metz C, Akoum A (2005) Cycle-dependent expression of macrophage migration inhibitory factor in the human endometrium. Hum Reprod 20:3518–3525PubMed Kats R, Al-Akoum M, Guay S, Metz C, Akoum A (2005) Cycle-dependent expression of macrophage migration inhibitory factor in the human endometrium. Hum Reprod 20:3518–3525PubMed
92.
go back to reference Paulesu L, Cateni C, Romagnoli R, Ietta F, Dantzer V (2005) Variation in macrophage-migration-inhibitory-factor immunoreactivity during porcine gestation. Biol Reprod 72:949–953PubMed Paulesu L, Cateni C, Romagnoli R, Ietta F, Dantzer V (2005) Variation in macrophage-migration-inhibitory-factor immunoreactivity during porcine gestation. Biol Reprod 72:949–953PubMed
93.
go back to reference Wang B, Goff AK (2003) Interferon-tau stimulates secretion of macrophage migration inhibitory factor from bovine endometrial epithelial cells. Biol Reprod 69:1690–1696PubMed Wang B, Goff AK (2003) Interferon-tau stimulates secretion of macrophage migration inhibitory factor from bovine endometrial epithelial cells. Biol Reprod 69:1690–1696PubMed
94.
go back to reference Akoum A, Metz CN, Morin M (2005) Marked increase in macrophage migration inhibitory factor synthesis and secretion in human endometrial cells in response to human chorionic gonadotropin hormone. J Clin Endocrinol Metab 90:2904–2910PubMed Akoum A, Metz CN, Morin M (2005) Marked increase in macrophage migration inhibitory factor synthesis and secretion in human endometrial cells in response to human chorionic gonadotropin hormone. J Clin Endocrinol Metab 90:2904–2910PubMed
95.
go back to reference Cao WG, Morin M, Metz C, Maheux R, Akoum A (2005) Stimulation of macrophage migration inhibitory factor expression in endometrial stromal cells by interleukin 1, beta involving the nuclear transcription factor NFkappaB. Biol Reprod 73:565–570PubMed Cao WG, Morin M, Metz C, Maheux R, Akoum A (2005) Stimulation of macrophage migration inhibitory factor expression in endometrial stromal cells by interleukin 1, beta involving the nuclear transcription factor NFkappaB. Biol Reprod 73:565–570PubMed
96.
go back to reference Cao WG, Morin M, Sengers V, Metz C, Roger T, Maheux R, Akoum A (2006) Tumour necrosis factor-alpha up-regulates macrophage migration inhibitory factor expression in endometrial stromal cells via the nuclear transcription factor NF-kappaB. Hum Reprod 21:421–428PubMed Cao WG, Morin M, Sengers V, Metz C, Roger T, Maheux R, Akoum A (2006) Tumour necrosis factor-alpha up-regulates macrophage migration inhibitory factor expression in endometrial stromal cells via the nuclear transcription factor NF-kappaB. Hum Reprod 21:421–428PubMed
97.
go back to reference Schaefer TM, Fahey JV, Wright JA, Wira CR (2005) Migration inhibitory factor secretion by polarized uterine epithelial cells is enhanced in response to the TLR3 agonist poly (I:C). Am J Reprod Immunol 54:193–202PubMed Schaefer TM, Fahey JV, Wright JA, Wira CR (2005) Migration inhibitory factor secretion by polarized uterine epithelial cells is enhanced in response to the TLR3 agonist poly (I:C). Am J Reprod Immunol 54:193–202PubMed
98.
go back to reference Arcuri F, Buchwalder L, Toti P, Cintorino M, Tosi P, Lockwood CJ, Rybalov B, Schatz F (2007) Differential regulation of colony stimulating factor 1 and macrophage migration inhibitory factor expression by inflammatory cytokines in term human decidua: implications for macrophage trafficking at the fetal-maternal interface. Biol Reprod 76:433–439PubMed Arcuri F, Buchwalder L, Toti P, Cintorino M, Tosi P, Lockwood CJ, Rybalov B, Schatz F (2007) Differential regulation of colony stimulating factor 1 and macrophage migration inhibitory factor expression by inflammatory cytokines in term human decidua: implications for macrophage trafficking at the fetal-maternal interface. Biol Reprod 76:433–439PubMed
99.
go back to reference Lockwood CJ, Matta P, Krikun G, Koopman LA, Masch R, Toti P, Arcuri F, Huang ST, Funai EF, Schatz F (2006) Regulation of monocyte chemoattractant protein-1 expression by tumor necrosis factor-alpha and interleukin-1beta in first trimester human decidual cells: implications for preeclampsia. Am J Pathol 168:445–452PubMed Lockwood CJ, Matta P, Krikun G, Koopman LA, Masch R, Toti P, Arcuri F, Huang ST, Funai EF, Schatz F (2006) Regulation of monocyte chemoattractant protein-1 expression by tumor necrosis factor-alpha and interleukin-1beta in first trimester human decidual cells: implications for preeclampsia. Am J Pathol 168:445–452PubMed
100.
go back to reference Lockwood CJ, Arcuri F, Toti P, Felice CD, Krikun G, Guller S, Buchwalder LF, Schatz F (2006) Tumor necrosis factor-alpha and interleukin-1beta regulate interleukin-8 expression in third trimester decidual cells: implications for the genesis of chorioamnionitis. Am J Pathol 169:1294–1302PubMed Lockwood CJ, Arcuri F, Toti P, Felice CD, Krikun G, Guller S, Buchwalder LF, Schatz F (2006) Tumor necrosis factor-alpha and interleukin-1beta regulate interleukin-8 expression in third trimester decidual cells: implications for the genesis of chorioamnionitis. Am J Pathol 169:1294–1302PubMed
101.
go back to reference Zeng FY, Weiser WY, Kratzin H, Stahl B, Karas M, Gabius HJ (1993) The major binding protein of the interferon antagonist sarcolectin in human placenta is a macrophage migration inhibitory factor. Arch Biochem Biophys 303:74–80PubMed Zeng FY, Weiser WY, Kratzin H, Stahl B, Karas M, Gabius HJ (1993) The major binding protein of the interferon antagonist sarcolectin in human placenta is a macrophage migration inhibitory factor. Arch Biochem Biophys 303:74–80PubMed
102.
go back to reference Arcuri F, Cintorino M, Vatti R, Carducci A, Liberatori S, Paulesu L (1999) Expression of macrophage migration inhibitory factor transcript and protein by first-trimester human trophoblasts. Biol Reprod 60:1299–1303PubMed Arcuri F, Cintorino M, Vatti R, Carducci A, Liberatori S, Paulesu L (1999) Expression of macrophage migration inhibitory factor transcript and protein by first-trimester human trophoblasts. Biol Reprod 60:1299–1303PubMed
103.
go back to reference Ietta F, Todros T, Ticconi C, Piccoli E, Zicari A, Piccione E, Paulesu L (2002) Macrophage migration inhibitory factor in human pregnancy and labor. Am J Reprod Immunol 48:404–409PubMed Ietta F, Todros T, Ticconi C, Piccoli E, Zicari A, Piccione E, Paulesu L (2002) Macrophage migration inhibitory factor in human pregnancy and labor. Am J Reprod Immunol 48:404–409PubMed
104.
go back to reference Chaiworapongsa T, Romero R, Espinoza J, Kim YM, Edwin S, Bujold E, Gomez R, Kuivaniemi H (2005) Macrophage migration inhibitory factor in patients with preterm parturition and microbial invasion of the amniotic cavity. J Matern Fetal Neonatal Med 18:405–416PubMed Chaiworapongsa T, Romero R, Espinoza J, Kim YM, Edwin S, Bujold E, Gomez R, Kuivaniemi H (2005) Macrophage migration inhibitory factor in patients with preterm parturition and microbial invasion of the amniotic cavity. J Matern Fetal Neonatal Med 18:405–416PubMed
105.
go back to reference Ietta F, Wu Y, Romagnoli R, Soleymanlou N, Orsini B, Zamudio S, Paulesu L, Caniggia I (2007) Oxygen regulation of macrophage migration inhibitory factor in human placenta. Am J Physiol Endocrinol Metab 292:E272–E280PubMed Ietta F, Wu Y, Romagnoli R, Soleymanlou N, Orsini B, Zamudio S, Paulesu L, Caniggia I (2007) Oxygen regulation of macrophage migration inhibitory factor in human placenta. Am J Physiol Endocrinol Metab 292:E272–E280PubMed
106.
go back to reference Zicari A, Ticconi C, Ietta F, Belmonte A, Bechi N, Realacci M, Di Vito M, Arcuri F, Russo M, Piccione E, Paulesu L (2006) Macrophage migration inhibitory factor-nitric oxide interaction in human fetal membranes at term pregnancy. J Soc Gynecol Investig 13:263–270PubMed Zicari A, Ticconi C, Ietta F, Belmonte A, Bechi N, Realacci M, Di Vito M, Arcuri F, Russo M, Piccione E, Paulesu L (2006) Macrophage migration inhibitory factor-nitric oxide interaction in human fetal membranes at term pregnancy. J Soc Gynecol Investig 13:263–270PubMed
107.
go back to reference Todros T, Bontempo S, Piccoli E, Ietta F, Romagnoli R, Biolcati M, Castellucci M, Paulesu L (2005) Increased levels of macrophage migration inhibitory factor (MIF) in preeclampsia. Eur J Obstet Gynecol Reprod Biol 123:162–166PubMed Todros T, Bontempo S, Piccoli E, Ietta F, Romagnoli R, Biolcati M, Castellucci M, Paulesu L (2005) Increased levels of macrophage migration inhibitory factor (MIF) in preeclampsia. Eur J Obstet Gynecol Reprod Biol 123:162–166PubMed
108.
go back to reference Yamada H, Kato EH, Morikawa M, Shimada S, Saito H, Watari M, Minakami H, Nishihira J (2003) Decreased serum levels of macrophage migration inhibition factor in miscarriages with normal chromosome karyotype. Hum Reprod 18:616–620PubMed Yamada H, Kato EH, Morikawa M, Shimada S, Saito H, Watari M, Minakami H, Nishihira J (2003) Decreased serum levels of macrophage migration inhibition factor in miscarriages with normal chromosome karyotype. Hum Reprod 18:616–620PubMed
109.
go back to reference Hristoskova S, Holzgreve W, Zhong XY, Hahn S (2006) Macrophage migration inhibition factor is elevated in pregnancy, but not to a greater extent in preeclampsia. Arch Gynecol Obstet 274:25–28PubMed Hristoskova S, Holzgreve W, Zhong XY, Hahn S (2006) Macrophage migration inhibition factor is elevated in pregnancy, but not to a greater extent in preeclampsia. Arch Gynecol Obstet 274:25–28PubMed
110.
go back to reference Kats R, Metz CN, Akoum A (2002) Macrophage migration inhibitory factor is markedly expressed in active and early-stage endometriotic lesions. J Clin Endocrinol Metab 87:883–889PubMed Kats R, Metz CN, Akoum A (2002) Macrophage migration inhibitory factor is markedly expressed in active and early-stage endometriotic lesions. J Clin Endocrinol Metab 87:883–889PubMed
111.
go back to reference Kats R, Collette T, Metz CN, Akoum A (2002) Marked elevation of macrophage migration inhibitory factor in the peritoneal fluid of women with endometriosis. Fertil Steril 78:69–76PubMed Kats R, Collette T, Metz CN, Akoum A (2002) Marked elevation of macrophage migration inhibitory factor in the peritoneal fluid of women with endometriosis. Fertil Steril 78:69–76PubMed
112.
go back to reference Morin M, Bellehumeur C, Therriault MJ, Metz C, Maheux R, Akoum A (2005) Elevated levels of macrophage migration inhibitory factor in the peripheral blood of women with endometriosis. Fertil Steril 83:865–872PubMed Morin M, Bellehumeur C, Therriault MJ, Metz C, Maheux R, Akoum A (2005) Elevated levels of macrophage migration inhibitory factor in the peripheral blood of women with endometriosis. Fertil Steril 83:865–872PubMed
113.
go back to reference Mahutte NG, Matalliotakis IM, Goumenou AG, Koumantakis GE, Vassiliadis S, Arici A (2004) Elevations in peritoneal fluid macrophage migration inhibitory factor are independent of the depth of invasion or stage of endometriosis. Fertil Steril 82:97–101PubMed Mahutte NG, Matalliotakis IM, Goumenou AG, Koumantakis GE, Vassiliadis S, Arici A (2004) Elevations in peritoneal fluid macrophage migration inhibitory factor are independent of the depth of invasion or stage of endometriosis. Fertil Steril 82:97–101PubMed
114.
go back to reference Akoum A, Metz CN, Al-Akoum M, Kats R (2006) Macrophage migration inhibitory factor expression in the intrauterine endometrium of women with endometriosis varies with disease stage, infertility status, and pelvic pain. Fertil Steril 85:1379–1385PubMed Akoum A, Metz CN, Al-Akoum M, Kats R (2006) Macrophage migration inhibitory factor expression in the intrauterine endometrium of women with endometriosis varies with disease stage, infertility status, and pelvic pain. Fertil Steril 85:1379–1385PubMed
115.
go back to reference Redman CW, Sacks GP, Sargent IL (1999) Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 180:499–506PubMed Redman CW, Sacks GP, Sargent IL (1999) Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 180:499–506PubMed
116.
go back to reference Moffett-King A (2002) Natural killer cells and pregnancy. Nat Rev Immunol 2:656–663PubMed Moffett-King A (2002) Natural killer cells and pregnancy. Nat Rev Immunol 2:656–663PubMed
117.
go back to reference Kudo Y, Boyd CA, Spyropoulou I, Redman CW, Takikawa O, Katsuki T, Hara T, Ohama K, Sargent IL (2004) Indoleamine 2,3-dioxygenase: distribution and function in the developing human placenta. J Reprod Immunol 61:87–98PubMed Kudo Y, Boyd CA, Spyropoulou I, Redman CW, Takikawa O, Katsuki T, Hara T, Ohama K, Sargent IL (2004) Indoleamine 2,3-dioxygenase: distribution and function in the developing human placenta. J Reprod Immunol 61:87–98PubMed
118.
go back to reference Girardi G, Bulla R, Salmon JE, Tedesco F (2006) The complement system in the pathophysiology of pregnancy. Mol Immunol 43:68–77PubMed Girardi G, Bulla R, Salmon JE, Tedesco F (2006) The complement system in the pathophysiology of pregnancy. Mol Immunol 43:68–77PubMed
119.
go back to reference Trundley A, Moffett A (2004) Human uterine leukocytes and pregnancy. Tissue Antigens 63:1–12PubMed Trundley A, Moffett A (2004) Human uterine leukocytes and pregnancy. Tissue Antigens 63:1–12PubMed
120.
go back to reference Dosiou C, Giudice LC (2005) Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr Rev 26:44–62PubMed Dosiou C, Giudice LC (2005) Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr Rev 26:44–62PubMed
121.
go back to reference Saito S, Morii T, Enomoto M, Sakakura S, Nishikawa K, Narita N, Ichijo M (1993) The effect of interleukin 2 and transforming growth factor-beta 2 (TGF-beta 2) on the proliferation and natural killer activity of decidual CD16- CD56bright natural killer cells. Cell Immunol 152:605–613PubMed Saito S, Morii T, Enomoto M, Sakakura S, Nishikawa K, Narita N, Ichijo M (1993) The effect of interleukin 2 and transforming growth factor-beta 2 (TGF-beta 2) on the proliferation and natural killer activity of decidual CD16- CD56bright natural killer cells. Cell Immunol 152:605–613PubMed
122.
go back to reference Verma S, Hiby SE, Loke YW, King A (2000) Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol Reprod 62:959–968PubMed Verma S, Hiby SE, Loke YW, King A (2000) Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol Reprod 62:959–968PubMed
123.
go back to reference Guimond MJ, Luross JA, Wang B, Terhorst C, Danial S, Croy BA (1997) Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 mice. Biol Reprod 56:169–179PubMed Guimond MJ, Luross JA, Wang B, Terhorst C, Danial S, Croy BA (1997) Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 mice. Biol Reprod 56:169–179PubMed
124.
go back to reference Guimond MJ, Wang B, Croy BA (1998) Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice. J Exp Med 187:217–223PubMed Guimond MJ, Wang B, Croy BA (1998) Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice. J Exp Med 187:217–223PubMed
125.
go back to reference Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D (1991) Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 6:791–798PubMed Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D (1991) Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 6:791–798PubMed
126.
go back to reference Avril T, Jarousseau AC, Watier H, Boucraut J, Le Bouteiller P, Bardos P, Thibault G (1999) Trophoblast cell line resistance to NK lysis mainly involves an HLA class I-independent mechanism. J Immunol 162:5902–5909PubMed Avril T, Jarousseau AC, Watier H, Boucraut J, Le Bouteiller P, Bardos P, Thibault G (1999) Trophoblast cell line resistance to NK lysis mainly involves an HLA class I-independent mechanism. J Immunol 162:5902–5909PubMed
127.
go back to reference Saito S, Umekage H, Nishikawa K, Morii T, Narita N, Enomoto M, Sakakura S, Harada N, Ichijo M, Morikawa H (1996) Interleukin 4 (IL-4) blocks the IL-2-induced increased in natural killer activity and DNA synthesis of decidual CD16-CD56bright NK cells by inhibiting expression of the IL-2 receptor alpha, beta, and gamma. Cell Immunol 170:71–77PubMed Saito S, Umekage H, Nishikawa K, Morii T, Narita N, Enomoto M, Sakakura S, Harada N, Ichijo M, Morikawa H (1996) Interleukin 4 (IL-4) blocks the IL-2-induced increased in natural killer activity and DNA synthesis of decidual CD16-CD56bright NK cells by inhibiting expression of the IL-2 receptor alpha, beta, and gamma. Cell Immunol 170:71–77PubMed
128.
go back to reference McIntire RH, Hunt JS (2005) Antigen presenting cells and HLA-G-a review. Placenta 26 Suppl A:S104–S109PubMed McIntire RH, Hunt JS (2005) Antigen presenting cells and HLA-G-a review. Placenta 26 Suppl A:S104–S109PubMed
129.
go back to reference Mosser DM (2003) The many faces of macrophage activation. J Leukoc Biol 73:209–212PubMed Mosser DM (2003) The many faces of macrophage activation. J Leukoc Biol 73:209–212PubMed
130.
go back to reference Duffield JS (2003) The inflammatory macrophage: a story of Jekyll and Hyde. Clin Sci (Lond) 104:27–38CrossRef Duffield JS (2003) The inflammatory macrophage: a story of Jekyll and Hyde. Clin Sci (Lond) 104:27–38CrossRef
131.
go back to reference Starkey PM, Sargent IL, Redman CW (1988) Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry. Immunology 65:129–134PubMed Starkey PM, Sargent IL, Redman CW (1988) Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry. Immunology 65:129–134PubMed
132.
go back to reference Mor G, Abrahams VM (2003) Potential role of macrophages as immunoregulators of pregnancy. Reprod Biol Endocrinol 1:119PubMed Mor G, Abrahams VM (2003) Potential role of macrophages as immunoregulators of pregnancy. Reprod Biol Endocrinol 1:119PubMed
133.
go back to reference Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23–35PubMed Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23–35PubMed
134.
go back to reference Heikkinen J, Mottonen M, Komi J, Alanen A, Lassila O (2003) Phenotypic characterization of human decidual macrophages. Clin Exp Immunol 131:498–505PubMed Heikkinen J, Mottonen M, Komi J, Alanen A, Lassila O (2003) Phenotypic characterization of human decidual macrophages. Clin Exp Immunol 131:498–505PubMed
135.
go back to reference Jones RL, Stoikos C, Findlay JK, Salamonsen LA (2006) TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132:217–232PubMed Jones RL, Stoikos C, Findlay JK, Salamonsen LA (2006) TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132:217–232PubMed
136.
go back to reference Reister F, Frank HG, Kingdom JC, Heyl W, Kaufmann P, Rath W, Huppertz B (2001) Macrophage-induced apoptosis limits endovascular trophoblast invasion in the uterine wall of preeclamptic women. Lab Invest 81:1143–1152PubMed Reister F, Frank HG, Kingdom JC, Heyl W, Kaufmann P, Rath W, Huppertz B (2001) Macrophage-induced apoptosis limits endovascular trophoblast invasion in the uterine wall of preeclamptic women. Lab Invest 81:1143–1152PubMed
137.
go back to reference Bowen JM, Chamley L, Mitchell MD, Keelan JA (2002) Cytokines of the placenta and extra-placental membranes: biosynthesis, secretion and roles in establishment of pregnancy in women. Placenta 23:239–256PubMed Bowen JM, Chamley L, Mitchell MD, Keelan JA (2002) Cytokines of the placenta and extra-placental membranes: biosynthesis, secretion and roles in establishment of pregnancy in women. Placenta 23:239–256PubMed
138.
go back to reference Medawar PB (1953) Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp Soc Exp Biol 7:320–338 Medawar PB (1953) Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp Soc Exp Biol 7:320–338
Metadata
Title
The role of macrophage migration inhibitory factor in maintaining the immune privilege at the fetal–maternal interface
Authors
Paola Viganò
Marcella Cintorino
Frederick Schatz
Charles J. Lockwood
Felice Arcuri
Publication date
01-06-2007
Publisher
Springer-Verlag
Published in
Seminars in Immunopathology / Issue 2/2007
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-007-0074-3

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