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Science 1 July 1966:
Vol. 153. no. 3731, pp. 80 - 82
DOI: 10.1126/science.153.3731.80
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Articles

Mechanism of a Reaction in Vitro Associated with Delayed-Type Hypersensitivity

Barry R. Bloom 1 and Boyce Bennett 2

1 Department of Microbiology and Immunology and Department of Pathology, Albert Einstein College of Medicine, New York 10461
2 Departmnent of Microbiology and Immunology and Department of Pathology, Albert Einstein College of Medicine, New York 10461

The cell type responsible for inhibition by antigen of migration in vitro of peritoneal exudate cells obtained from tuberculin-hypersensitive guinea pigs was studied. Exudate populations were separated into component cell types, the lymphocyte and the macrophage. Peritoneal lymphocytes from sensitive donors were the immunologically active cells in this system, the macrophages, being merely indicator cells which migrate. Sensitized peritoneal lymphocyte populations, upon interaction with specific antigen in vitro, elaborated into the medium a soluble material capable of inhibiting migration of normal exudate cells.


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Innate Immunity 14, 63-87
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Interference of Macrophage Migration Inhibitory Factor Expression in a Mouse Melanoma Inhibits Tumor Establishment by Up-Regulating Thrombospondin-1.
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J. Biol. Chem. 282, 29910-29918
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Ovarian cancer cell-derived migration inhibitory factor enhances tumor growth, progression, and angiogenesis.
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Mol. Cancer Ther. 6, 1993-2002
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Functional Characterization of the Plasmodium falciparum and P. berghei Homologues of Macrophage Migration Inhibitory Factor.
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Exhaustion is Associated With Low Macrophage Migration Inhibitory Factor Expression in Patients With Coronary Artery Disease.
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Apoptotic Neutrophils Release Macrophage Migration Inhibitory Factor upon Stimulation with Tumor Necrosis Factor-{alpha}.
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Macrophage migration inhibitory factor and glucocorticoid sensitivity.
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Macrophage Migration Inhibitory Factor Contributes to Host Defense against Acute Trypanosoma cruzi Infection..
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Infect. Immun. 74, 3170-3179
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Macrophage Migration Inhibitory Factor-Nitric Oxide Interaction in Human Fetal Membranes at Term Pregnancy.
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Macrophage Migration Inhibitory Factor Increases Neuronal Delayed Rectifier K+ Current.
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Improved Resistance to Bacterial Superinfection in Mice by Treatment with Macrophage Migration Inhibitory Factor.
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Macrophage migration inhibitory factor in the human epididymis and semen.
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Glucocorticoids suppress macrophage migration inhibitory factor (MIF) expression in a cell-type-specific manner.
Z Alourfi, R P Donn, A Stevens, A Berry, A McMaster, and D W Ray (2005)
J. Mol. Endocrinol. 34, 583-595
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The Pathogenesis of Tuberculosis: The First One Hundred (and Twenty-Three) Years.
N. W. Schluger (2005)
Am. J. Respir. Cell Mol. Biol. 32, 251-256
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Variation in Macrophage-Migration-Inhibitory-Factor Immunoreactivity During Porcine Gestation.
L. Paulesu, C. Cateni, R. Romagnoli, F. Ietta, and V. Dantzer (2005)
Biol Reprod 72, 949-953
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Immunosuppressive Factors Secreted by Human Amniotic Epithelial Cells.
H. Li, J. Y. Niederkorn, S. Neelam, E. Mayhew, R. A. Word, J. P. McCulley, and H. Alizadeh (2005)
Invest. Ophthalmol. Vis. Sci. 46, 900-907
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Macrophage Migration Inhibitory Factor Promotes Tumor Invasion and Metastasis via the Rho-Dependent Pathway.
B. Sun, J. Nishihira, T. Yoshiki, M. Kondo, Y. Sato, F. Sasaki, and S. Todo (2005)
Clin. Cancer Res. 11, 1050-1058
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Macrophage Migration Inhibitory Factor Is Released from Pituitary Folliculo-Stellate-Like Cells by Endotoxin and Dexamethasone and Attenuates the Steroid-Induced Inhibition of Interleukin 6 Release.
T. Tierney, R. Patel, C. A. S. Stead, L. Leng, R. Bucala, and J. C. Buckingham (2005)
Endocrinology 146, 35-43
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Limited Capability of Regional Lymph Nodes to Eradicate Metastatic Cancer Cells.
H. Nagata, T. Arai, Y. Soejima, H. Suzuki, H. Ishii, and T. Hibi (2004)
Cancer Res. 64, 8239-8248
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Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues.
C. Murdoch, A. Giannoudis, and C. E. Lewis (2004)
Blood 104, 2224-2234
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Pathogenesis of Malaria and Clinically Similar Conditions.
I. A. Clark, L. M. Alleva, A. C. Mills, and W. B. Cowden (2004)
Clin. Microbiol. Rev. 17, 509-539
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Macrophage Migration Inhibitory Factor Deficiency Impairs Atherosclerosis in Low-Density Lipoprotein Receptor-Deficient Mice.
J.-H. Pan, G. K. Sukhova, J.-T. Yang, B. Wang, T. Xie, H. Fu, Y. Zhang, A. R. Satoskar, J. R. David, C. N. Metz, et al. (2004)
Circulation 109, 3149-3153
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Xenopus laevis Macrophage Migration Inhibitory Factor Is Essential for Axis Formation and Neural Development.
M. Suzuki, Y. Takamura, M. Maeno, S. Tochinai, D. Iyaguchi, I. Tanaka, J. Nishihira, and T. Ishibashi (2004)
J. Biol. Chem. 279, 21406-21414
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Macrophage Migration Inhibitory Factor Is Induced by Thrombin and Factor Xa in Endothelial Cells.
T. Shimizu, J. Nishihira, H. Watanabe, R. Abe, A. Honda, T. Ishibashi, and H. Shimizu (2004)
J. Biol. Chem. 279, 13729-13737
   Abstract »    Full Text »    PDF »
Role of Macrophage Migration Inhibitory Factor in Conjunctival Pathology in Ocular Cicatricial Pemphigoid.
M. S. Razzaque, C. S. Foster, and A. R. Ahmed (2004)
Invest. Ophthalmol. Vis. Sci. 45, 1174-1181
   Abstract »    Full Text »    PDF »
Ultraviolet A-induced Production of Matrix Metalloproteinase-1 Is Mediated by Macrophage Migration Inhibitory Factor (MIF) in Human Dermal Fibroblasts.
H. Watanabe, T. Shimizu, J. Nishihira, R. Abe, T. Nakayama, M. Taniguchi, H. Sabe, T. Ishibashi, and H. Shimizu (2004)
J. Biol. Chem. 279, 1676-1683
   Abstract »    Full Text »    PDF »
Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway.
R. BAUMANN, C. CASAULTA, D. SIMON, S. CONUS, S. YOUSEFI, and H.-U. SIMON (2003)
FASEB J 17, 2221-2230
   Abstract »    Full Text »    PDF »
Aldose Reductase and Macrophage Migration Inhibitory Factor Are Associated with Epididymosomes and Spermatozoa in the Bovine Epididymis.
G. Frenette, C. Lessard, E. Madore, M. A. Fortier, and R. Sullivan (2003)
Biol Reprod 69, 1586-1592
   Abstract »    Full Text »    PDF »
Interferon-{tau} Stimulates Secretion of Macrophage Migration Inhibitory Factor from Bovine Endometrial Epithelial Cells.
B. Wang and A. K. Goff (2003)
Biol Reprod 69, 1690-1696
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MIF Signal Transduction Initiated by Binding to CD74.
L. Leng, C. N. Metz, Y. Fang, J. Xu, S. Donnelly, J. Baugh, T. Delohery, Y. Chen, R. A. Mitchell, and R. Bucala (2003)
J. Exp. Med. 197, 1467-1476
   Abstract »    Full Text »    PDF »
Expression of Macrophage Migration Inhibitory Factor in Acute Ischemic Myocardial Injury.
C.-M. Yu, K. W.-H. Lai, Y.-X. Chen, X.-R. Huang, and H. Y. Lan (2003)
J. Histochem. Cytochem. 51, 625-631
   Abstract »    Full Text »    PDF »
Expression of macrophage migration inhibitory factor in diffuse systemic sclerosis.
E Selvi, S A Tripodi, M Catenaccio, S Lorenzini, D Chindamo, S Manganelli, R Romagnoli, F Ietta, L Paulesu, C Miracco, et al. (2003)
Ann Rheum Dis 62, 460-464
   Abstract »    Full Text »    PDF »
The Apa Protein of Mycobacterium tuberculosis Stimulates Gamma Interferon-Secreting CD4+ and CD8+ T Cells from Purified Protein Derivative-Positive Individuals and Affords Protection in a Guinea Pig Model.
P. Kumar, R. R. Amara, V. K. Challu, V. K. Chadda, and V. Satchidanandam (2003)
Infect. Immun. 71, 1929-1937
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Macrophage migration inhibitory factor (MIF) regulates host responses to endotoxin through modulation of Toll-like receptor 4 (TLR4).
T. Roger, C. Froidevaux, C. Martin, and T. Calandra (2003)
Innate Immunity 9, 119-123
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Macrophage Migration Inhibitory Factor Deficiency Is Associated with Altered Cell Growth and Reduced Susceptibility to Ras-mediated Transformation.
O. Petrenko, G. Fingerle-Rowson, T. Peng, R. A. Mitchell, and C. N. Metz (2003)
J. Biol. Chem. 278, 11078-11085
   Abstract »    Full Text »    PDF »
Macrophage Migration Inhibitory Factor and CXC Chemokine Expression in Non-Small Cell Lung Cancer: Role in Angiogenesis and Prognosis.
E. S. White, K. R. Flaherty, S. Carskadon, A. Brant, M. D. Iannettoni, J. Yee, M. B. Orringer, and D. A. Arenberg (2003)
Clin. Cancer Res. 9, 853-860
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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.
C. M. Denkinger, M. Denkinger, J. J. Kort, C. Metz, and T. G. Forsthuber (2003)
J. Immunol. 170, 1274-1282
   Abstract »    Full Text »    PDF »
Quantification of Macrophage Migration Inhibitory Factor mRNA Expression in Non-Small Cell Lung Cancer Tissues and Its Clinical Significance.
M. Tomiyasu, I. Yoshino, R. Suemitsu, T. Okamoto, and K. Sugimachi (2002)
Clin. Cancer Res. 8, 3755-3760
   Abstract »    Full Text »    PDF »
Homologues of Human Macrophage Migration Inhibitory Factor from a Parasitic Nematode. GENE CLONING, PROTEIN ACTIVITY, AND CRYSTAL STRUCTURE.
X. Zang, P. Taylor, J. M. Wang, D. J. Meyer, A. L. Scott, M. D. Walkinshaw, and R. M. Maizels (2002)
J. Biol. Chem. 277, 44261-44267
   Abstract »    Full Text »    PDF »
Macrophage migration inhibitory factor (MIF) plays a pivotal role in immunity against Salmonella typhimurium.
H. Koebernick, L. Grode, J. R. David, W. Rohde, M. S. Rolph, H.-W. Mittrucker, and S. H. E. Kaufmann (2002)
PNAS 99, 13681-13686
   Abstract »    Full Text »    PDF »
Release of Macrophage Migration Inhibitory Factor and CXCL8/Interleukin-8 from Lung Epithelial Cells Rendered Necrotic by Influenza A Virus Infection.
U. Arndt, G. Wennemuth, P. Barth, M. Nain, Y. Al-Abed, A. Meinhardt, D. Gemsa, and M. Bacher (2002)
J. Virol. 76, 9298-9306
   Abstract »    Full Text »    PDF »
The Presence of Macrophage Migration Inhibitory Factor in Human Trabecular Meshwork and its Upregulatory Effects on the T Helper 1 Cytokine.
H. Takase, S. Sugita, D. J. Rhee, Y. Imai, C. Taguchi, Y. Sugamoto, Y. Tagawa, J. Nishihira, P. Russell, and M. Mochizuki (2002)
Invest. Ophthalmol. Vis. Sci. 43, 2691-2696
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Accumulation of the mitochondrial form of the sulphydryl oxidase Erv1p/Alrp during the early stages of spermatogenesis.
M. Klissenbauer, S. Winters, U. A. O. Heinlein, and T. Lisowsky (2002)
J. Exp. Biol. 205, 1979-1986
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Contribution of Macrophage Migration Inhibitory Factor to Extracellular Signal-regulated Kinase Activation by Oxidative Stress in Cardiomyocytes.
J. Fukuzawa, J. Nishihira, N. Hasebe, T. Haneda, J. Osaki, T. Saito, T. Nomura, T. Fujino, N. Wakamiya, and K. Kikuchi (2002)
J. Biol. Chem. 277, 24889-24895
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The Tautomerase Active Site of Macrophage Migration Inhibitory Factor Is a Potential Target for Discovery of Novel Anti-inflammatory Agents.
J. B. Lubetsky, A. Dios, J. Han, B. Aljabari, B. Ruzsicska, R. Mitchell, E. Lolis, and Y. Al-Abed (2002)
J. Biol. Chem. 277, 24976-24982
   Abstract »    Full Text »    PDF »
Role of macrophage migration inhibitory factor in bleomycin-induced lung injury and fibrosis in mice.
Y. Tanino, H. Makita, K. Miyamoto, T. Betsuyaku, Y. Ohtsuka, J. Nishihira, and M. Nishimura (2002)
Am J Physiol Lung Cell Mol Physiol 283, L156-L162
   Abstract »    Full Text »    PDF »
Macrophage Migration Inhibitory Factor Up-regulates Matrix Metalloproteinase-9 and -13 in Rat Osteoblasts. RELEVANCE TO INTRACELLULAR SIGNALING PATHWAYS.
S. Onodera, J. Nishihira, K. Iwabuchi, Y. Koyama, K. Yoshida, S. Tanaka, and A. Minami (2002)
J. Biol. Chem. 277, 7865-7874
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Macrophage Migration Inhibitory Factor Is Markedly Expressed in Active and Early-Stage Endometriotic Lesions.
R. Kats, C. N. Metz, and A. Akoum (2002)
J. Clin. Endocrinol. Metab. 87, 883-889
   Abstract »    Full Text »    PDF »
Macrophage migration inhibitory factor (MIF) modulates innate immune responses induced by endotoxin and Gram-negative bacteria.
T. Roger, M. P. Glauser, and T. Calandra (2001)
Innate Immunity 7, 456-460
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Macrophage migration inhibitory factor as a redox-sensitive cytokine in cardiac myocytes.
M. Takahashi, J. Nishihira, M. Shimpo, Y. Mizue, S. Ueno, H. Mano, E. Kobayashi, U. Ikeda, and K. Shimada (2001)
Cardiovasc Res 52, 438-445
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Novel Role of Macrophage Migration Inhibitory Factor in Angiotensin II Regulation of Neuromodulation in Rat Brain.
S. Busche, S. Gallinat, M. A. Fleegal, M. K. Raizada, and C. Sumners (2001)
Endocrinology 142, 4623-4630
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Macrophage Migration Inhibitory Factor in the Human Endometrium: Expression and Localization During the Menstrual Cycle and Early Pregnancy.
F. Arcuri, C. Ricci, F. Ietta, M. Cintorino, S. A. Tripodi, I. Cetin, E. Garzia, F. Schatz, P. Klemi, R. Santopietro, et al. (2001)
Biol Reprod 64, 1200-1205
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De Novo Expression of Macrophage Migration Inhibitory Factor in Atherogenesis in Rabbits.
S.-G. Lin, X.-Y. Yu, Y.-X. Chen, X. R. Huang, C. Metz, R. Bucala, C.-P. Lau, and H. Y. Lan (2000)
Circ. Res. 87, 1202-1208
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Identification of Macrophage Migration Inhibitory Factor as a Potent Endothelial Cell Growth-Promoting Agent Released by Ectopic Human Endometrial Cells.
Y. Yang, P. Degranpré, A. Kharfi, and A. Akoum (2000)
J. Clin. Endocrinol. Metab. 85, 4721-4727
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Increase of macrophage migration inhibitory factor in sera of patients with iridocyclitis.
N. Kitaichi, S. Kotake, Y. Mizue, H. Matsuda, K. Onoé, and J. Nishihira (2000)
Br J Ophthalmol 84, 1423-1425
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Human Uveal Melanoma Cells Produce Macrophage Migration-Inhibitory Factor to Prevent Lysis by NK Cells.
A. C. Repp, E. S. Mayhew, S. Apte, and J. Y. Niederkorn (2000)
J. Immunol. 165, 710-715
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Macrophage Migration Inhibitory Factor-Induced Ca2+ Response in Rat Testicular Peritubular Cells.
G. Wennemuth, G. Aumüller, M. Bacher, and A. Meinhardt (2000)
Biol Reprod 62, 1632-1639
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Macrophage migration inhibitory factor levels in the vitreous of patients with proliferative diabetic retinopathy.
Y. Mitamura, S. Takeuchi, A. Matsuda, Y. Tagawa, Y. Mizue, and J. Nishihira (2000)
Br J Ophthalmol 84, 636-639
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Macrophage Migration Inhibitory Factor in the Bovine Corpus Luteum: Characterization of Steady-State Messenger Ribonucleic Acid and Immunohistochemical Localization.
S. E. Bove, M. G. Petroff, M. Nishibori, and J. L. Pate (2000)
Biol Reprod 62, 879-885
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Macrophage Migration Inhibitory Factor Up-regulates Expression of Matrix Metalloproteinases in Synovial Fibroblasts of Rheumatoid Arthritis.
S. Onodera, K. Kaneda, Y. Mizue, Y. Koyama, M. Fujinaga, and J. Nishihira (2000)
J. Biol. Chem. 275, 444-450
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Expression of Macrophage Migration Inhibitory Factor Transcript and Protein by First-Trimester Human Trophoblasts.
F. Arcuri, M. Cintorino, R. Vatti, A. Carducci, S. Liberatori, and L. Paulesu (1999)
Biol Reprod 60, 1299-1303
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Enzyme Activity of Macrophage Migration Inhibitory Factor toward Oxidized Catecholamines.
J. Matsunaga, D. Sinha, L. Pannell, C. Santis, F. Solano, G. J. Wistow, and V. J. Hearing (1999)
J. Biol. Chem. 274, 3268-3271
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Induction of macrophage migration inhibitory factor in human ovary by human chorionic gonadotrophin.
S.-i. Wada, T. Kudo, M. Kudo, N. Sakuragi, H. Hareyama, J. Nishihira, and S. Fujimoto (1999)
Hum. Reprod. 14, 395-399
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Macrophage migration inhibitory factor is a critical mediator of the activation of immune cells by exotoxins of Gram-positive bacteria.
T. Calandra, L. A. Spiegel, C. N. Metz, and R. Bucala (1998)
PNAS 95, 11383-11388
   Abstract »    Full Text »    PDF »
Migration Inhibitory Factor Induces Killing of Leishmania major by Macrophages: Dependence on Reactive Nitrogen Intermediates and Endogenous TNF-{alpha}.
S. Juttner, J. Bernhagen, C. N. Metz, M. Rollinghoff, R. Bucala, and A. Gessner (1998)
J. Immunol. 161, 2383-2390
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Effect of Anti-Macrophage Migration Inhibitory Factor Antibody on Lipopolysaccharide-induced Pulmonary Neutrophil Accumulation.
H. MAKITA, M. NISHIMURA, K. MIYAMOTO, T. NAKANO, Y. TANINO, J. HIROKAWA, J. NISHIHIRA, and Y. KAWAKAMI (1998)
Am. J. Respir. Crit. Care Med. 158, 573-579
   Abstract »    Full Text »    PDF »
Cutting Edge: Role of Macrophage Migration Inhibitory Factor in Inhibiting NK Cell Activity and Preserving Immune Privilege.
R. S. Apte, D. Sinha, E. Mayhew, G. J. Wistow, and J. Y. Niederkorn (1998)
J. Immunol. 160, 5693-5696
   Abstract »    Full Text »    PDF »
Macrophage Migration Inhibitory Factor Interactions with Glutathione and S-Hexylglutathione.
M. D. Swope, H.-W. Sun, B. Klockow, P. Blake, and E. Lolis (1998)
J. Biol. Chem. 273, 14877-14884
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Chemokines.
B. J. Rollins (1997)
Blood 90, 909-928
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Insulin secretion is regulated by the glucose-dependent production of islet beta  cell macrophage migration inhibitory factor.
G. Waeber, T. Calandra, R. Roduit, J.-A. Haefliger, C. Bonny, N. Thompson, B. Thorens, E. Temler, A. Meinhardt, M. Bacher, et al. (1997)
PNAS 94, 4782-4787
   Abstract »    Full Text »    PDF »
The Pathogenic Role of Macrophage Migration Inhibitory Factor in Immunologically Induced Kidney Disease in the Rat.
H. Y. Lan, M. Bacher, N. Yang, W. Mu, D. J. Nikolic-Paterson, C. Metz, A. Meinhardt, R. Bucala, and R. C. Atkins (1997)
J. Exp. Med. 185, 1455-1466
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Pituitary Cytokine and Growth Factor Expression and Action.
D. Ray and S. Melmed (1997)
Endocr. Rev. 18, 206-228
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Proton Magnetic Resonance Imaging and Spectroscopic Studies of the Pathogenesis and Treatment of Juvenile Dermatomyositis.
J.M. Slopis, E.F. Jackson, P.A. Narayana, S.C. Papasozomenos, and I.J. Butler (1993)
J Child Neurol 8, 242-249
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Colony-Stimulating Factors and Host Defense.
R. H. Weisbart, J. C. Gasson, and D. W. Golde (1989)
Ann Intern Med 110, 297-303
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Interferon-Gamma, the Activated Macrophage, and Host Defense Against Microbial Challenge.
H. W. MURRAY (1988)
Ann Intern Med 108, 595-608
   Abstract »    PDF »
Breast Milk Immunology: A Frontier in Infant Nutrition.
W. B. Pittard III (1979)
Arch Pediatr Adolesc Med 133, 83-87
   Abstract »    PDF »
Collagenase production by lymphokine-activated macrophages.
L. Wahl, S. Wahl, S. Mergenhagen, and G. Martin (1975)
Science 187, 261-263
   Abstract »    PDF »
Inhibition of Leukocyte Migration by Human Tumors: Effect on Patient Survival.
W. H. Wolberg (1974)
Arch Surg 109, 211-214
   Abstract »    PDF »
Modulation of Inflammation and Immunity by Cyclic AMP.
H. R. Bourne, Y. Weinstein, K. L. Melmon, L. M. Lichtenstein, C. S. Henney, and G. M. Shearer (1974)
Science 184, 19-28
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Cell-Mediated Hypersensitivity to Neural Antigens: Occurrence in Human Patients and Nonhuman Primates With Neurological Diseases.
P. O. Behan, W. M. H. Behan, R. G. Feldman, and M. W. Kies (1972)
Arch Neurol 27, 145-152
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Diseases of Cellular Immunity.
E. R. STIEHM, A. J. AMMANN, E. V. BARNETT, C. G. CRADDOCK, H. H. FUDENBERG, and G. J. LAWLOR JR. (1972)
Ann Intern Med 77, 101-116
   Abstract »    PDF »
Tumor hnmunity: Tumor Suppression in vivo Initiated by Soluble Products of Specifically Stimulated Lymphocytes.
I. D. Bernstein, D. E. Thor, B. Zbar, and H. J. Rapp (1971)
Science 172, 729-731
   Abstract »    PDF »
Production of Macrophage Inhibitory Factor by Patients With Leprosy.
S. I. Katz, B. H. DeBetz, and N. Zaias (1971)
Arch Dermatol 103, 358-361
   Abstract »    PDF »


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