MAP kinase phosphatase-1, a critical negative regulator of the innate immune response

International Journal of Clinical and Experimental Medicine

Volumn 2, Issue 1, 2009, Pages 48-67

  Li, Liwu ^a   Chen, Shuang Feng ^b   Liu, Yusen ^c  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b LIAOCHENG PEOPLE'S HOSPITAL   (China)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Cytokines; Inflammation; Innate immune response; MAP kinase; MKP 1; Negative regulator

Indexed keywords

ANTIINFLAMMATORY AGENT; CORTICOSTEROID; CYTOKINE; DEXAMETHASONE; GLUCOCORTICOID; IMMUNOMODULATING AGENT; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR;

ACETYLATION; ADAPTIVE IMMUNITY; ANTIINFLAMMATORY ACTIVITY; BACTERIAL INFECTION; CARBOXY TERMINAL SEQUENCE; CYTOKINE PRODUCTION; DISEASE SEVERITY; DNA SEQUENCE; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME SUBSTRATE; FEEDBACK SYSTEM; GENE EXPRESSION; GENE MUTATION; HOST PATHOGEN INTERACTION; HUMAN; HYPOTENSION; IMMUNOREGULATION; IMMUNOSTIMULATION; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MORTALITY; MULTIPLE ORGAN FAILURE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; REVIEW; SEPTIC SHOCK; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION;

BACTERIA (MICROORGANISMS); MUS;

EID: 65549143733     PISSN: None     EISSN: 19405901     Source Type: Journal    
DOI: None     Document Type: Review

References (107)

1. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J and Pinsky MR. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001; 29: 1303-1310.
2. Martin GS, Mannino DM, Eaton S and Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 2003; 348: 1546-1554.
3. Wang JE, Dahle MK, Yndestad A, Bauer I, McDonald MC, Aukrust P, Foster SJ, Bauer M, Aasen AO and Thiemermann C. Peptidoglycan of Staphylococcus aureus causes inflammation and organ injury in the rat. Crit Care Med 2004; 32: 546-552.
4. Centers for Disease Control (CDC). Increase in National Hospital Discharge Survey rates for septicemia--United States, 1979-1987. MMWR Morb Mortal Wkly Rep 1990; 39: 31-34.
5. Watson RS, Carcillo JA. Scope and epidemiology of pediatric sepsis. Pediatr Crit Care Med 2005; 6: S3-S5.
6. Watson RS, Carcillo JA, Linde-Zwirble WT, Clermont G, Lidicker J and Angus DC. The epidemiology of severe sepsis in children in the United States. Am J Respir Crit Care Med 2003; 167: 695-701.
7. Siddiqui S. Not "surviving sepsis" in the developing countries. J Indian Med Assoc 2007; 105: 221.
8. Tanriover MD, Guven GS, Sen D, Unal S and Uzun O. Epidemiology and outcome of sepsis in a tertiary-care hospital in a developing country. Epidemiol Infect 2006; 134: 315-322.
9. Cheng AC, Limmathurotsakul D, Chierakul W, Getchalarat N, Wuthiekanun V, Stephens DP, Day NP, White NJ, Chaowagul W, Currie BJ and Peacock SJ. A randomized controlled trial of granulocyte colony-stimulating factor for the treatment of severe sepsis due to melioidosis in Thailand. Clin Infect Dis 2007; 45: 308-314.
10. Cheng B, Xie G, Yao S, Wu X, Guo Q, Gu M, Fang Q, Xu Q, Wang D, Jin Y, Yuan S, Wang J, Du Z, Sun Y and Fang X. Epidemiology of severe sepsis in critically ill surgical patients in ten university hospitals in China. Crit Care Med 2007; 35: 2538-2546.
11. Song, S. Sepsis in neonates. Chin. J. Neonatol 2001; 16: 233-234.
12. Wang H, Ma S. The cytokine storm and factors determining the sequence and severity of organ dysfunction in multiple organ dysfunction syndrome. Am J Emerg Med 2008; 26: 711-715.
13. Faulkner L, Cooper A, Fantino C, Altmann DM and Sriskandan S. The mechanism of superantigen-mediated toxic shock: not a simple Th1 cytokine storm. J Immunol 2005; 175: 6870-6877.
14. Cohen J. The immunopathogenesis of sepsis. Nature 2002; 420: 885-891.
15. Parrillo JE. Pathogenetic mechanisms of septic shock. N Engl J Med 1993; 328: 1471-1477.
16. Ceneviva G, Paschall JA, Maffei F and Carcillo JA. Hemodynamic support in fluid-refractory pediatric septic shock. Pediatrics 1998; 102: e19.
17. Kumar A, Brar R, Wang P, Dee L, Skorupa G, Khadour F, Schulz R and Parrillo JE. Role of nitric oxide and cGMP in human septic serum-induced depression of cardiac myocyte contractility. Am J Physiol 1999; 276: R265-R276.
18. Levi M. Disseminated intravascular coagulation: What's new? Crit Care Clin 2005; 21: 449-467.
19. Beutler B, Kruys V. Lipopolysaccharide signal transduction, regulation of tumor necrosis factor biosynthesis, and signaling by tumor necrosis factor itself. J Cardiovasc Pharmacol 1995; 25 Suppl 2: S1-S8.
20. Akira S. Mammalian Toll-like receptors. Curr Opin Immunol 2003; 15: 5-11.
21. Janeway CAJ, Travers P, Walport M, Shlomchik MJ: Immunobiology: the immune system in health and disease. New York, Garland Publishing, 2001.
22. Ringwood L, Li L. The involvement of the interleukin-1 receptor-associated kinases (IRAKs) in cellular signaling networks controlling inflammation. Cytokine 2008; 42: 1-7.
23. Li L, Cousart S, Hu J and McCall CE. Characterization of interleukin-1 receptor-associated kinase in normal and endotoxin-tolerant cells. J Biol Chem 2000; 275: 23340-23345.
24. Kawagoe T, Sato S, Matsushita K, Kato H, Matsui K, Kumagai Y, Saitoh T, Kawai T, Takeuchi O and Akira S. Sequential control of Toll-like receptor-dependent responses by IRAK1 and IRAK2. Nat Immunol 2008; 9: 684-691.
25. Lye E, Dhanji S, Calzascia T, Elford AR and Ohashi PS. IRAK-4 kinase activity is required for IRAK-4-dependent innate and adaptive immune responses. Eur J Immunol 2008; 38: 870-876.
26. Su J, Xie Q, Wilson I and Li L. Differential regulation and role of interleukin-1 receptor associated kinase-M in innate immunity signaling. Cell Signal 2007; 19: 1596-1601.
27. Hu J, Jacinto R, McCall C and Li L. Regulation of IL-1 receptor-associated kinases by lipopolysaccharide. J Immunol 2002; 168: 3910-3914.
28. Learn CA, Boger MS, Li L and McCall CE. The phosphatidylinositol 3-kinase pathway selectively controls sIL-1RA not interleukin-1beta production in the septic leukocytes. J Biol Chem 2001; 276: 20234-20239.
29. Ono K, Han J. The p38 signal transduction pathway: activation and function. Cell Signal 2000; 12: 1-13.
30. Dong C, Davis RJ and Flavell RA. MAP kinases in the immune response. Annu Rev Immunol 2002; 20: 55-72.
31. Keyse SM. Protein phosphatases and the regulation of mitogen-activated protein kinase signalling. Curr Opin Cell Biol 2000; 12: 186-192.
32. Zhao Q, Wang X, Nelin LD, Yao Y, Matta R, Manson ME, Baliga RS, Meng X, Smith CV, Bauer JA, Chang CH and Liu Y. MAP kinase phosphatase 1 controls innate immune responses and suppresses endotoxic shock. J Exp Med 2006; 203: 131-140.
33. Hammer M, Mages J, Dietrich H, Servatius A, Howells N, Cato AC and Lang R. Dual specificity phosphatase 1 (DUSP1) regulates a subset of LPS-induced genes and protects mice from lethal endotoxin shock. J Exp Med 2006; 203: 15-20.
34. Salojin KV, Owusu IB, Millerchip KA, Potter M, Platt KA and Oravecz T. Essential role of MAPK phosphatase-1 in the negative control of innate immune responses. J Immunol 2006; 176: 1899-1907.
35. Chi H, Barry SP, Roth RJ, Wu JJ, Jones EA, Bennett AM and Flavell RA. Dynamic regulation of pro- and anti-inflammatory cytokines by MAPK phosphatase 1 (MKP-1) in innate immune responses. Proc Natl Acad Sci U S A 2006; 103: 2274-2279.
36. Whitmarsh AJ, Davis RJ. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 1996; 74: 589-607.
37. Davis RJ. The mitogen-activated protein kinase signal transduction pathway. J Biol Chem 1993; 268: 14553-14556.
38. Carballo E, Lai WS and Blackshear PJ. Feedback Inhibition of Macrophage Tumor Necrosis Factor-{alpha} Production by Tristetraprolin. Science 1998; 281: 1001-1005.
39. Mahtani KR, Brook M, Dean JL, Sully G, Saklatvala J and Clark AR. Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor alpha mRNA stability. Mol Cell Biol 2001; 21: 6461-6469.
40. Stoecklin G, Stubbs T, Kedersha N, Wax S, Rigby WF, Blackwell TK and Anderson P. MK2-induced tristetraprolin:14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J 2004; 23: 1313-1324.
41. Lai WS, Parker JS, Grissom SF, Stumpo DJ and Blackshear PJ. Novel mRNA targets for tristetraprolin (TTP) identified by global analysis of stabilized transcripts in TTP-deficient fibroblasts. Mol Cell Biol 2006; 26: 9196-9208.
42. Lau LF, Nathans D. Identification of a set of genes expressed during the G0/G1 transition of cultured mouse cells. EMBO J 1985; 4: 3145-3151.
43. Charles CH, Abler AS and Lau LF. cDNA sequence of a growth factor-inducible immediate early gene and characterization of its encoded protein. Oncogene 1992; 7: 187-190.
44. Keyse SM, Emslie EA. Oxidative stress and heat shock induce a human gene encoding a protein-tyrosine phosphatase. Nature 1992; 359: 644-647.
45. Charles CH, Sun H, Lau LF and Tonks NK. The growth factor-inducible immediate-early gene 3CH134 encodes a protein-tyrosine-phosphatase. Proc Natl Acad Sci U S A 1993; 90: 5292-5296.
46. Alessi DR, Smythe C and Keyse SM. The human CL100 gene encodes a Tyr/ Thr-protein phosphatase which potently and specifically inactivates MAP kinase and suppresses its activation by oncogenic ras in Xenopus oocyte extracts. Oncogene 1993; 8: 2015-2020.
47. Zheng CF, Guan KL. Dephosphorylation and inactivation of the mitogen-activated protein kinase by a mitogen-induced Thr/Tyr protein phosphatase. J Biol Chem 1993; 268: 16116-16119.
48. Sun H, Charles CH, Lau LF and Tonks NK. MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 1993; 75: 487-493.
49. Liu Y, Gorospe M, Yang C and Holbrook NJ. Role of mitogen-activated protein kinase phosphatase during the cellular response to genotoxic stress. Inhibition of c-Jun N-terminal kinase activity and AP-1-dependent gene activation. J Biol Chem 1995; 270: 8377-8380.
50. Raingeaud J, Gupta S, Rogers JS, Dickens M, Han J, Ulevitch RJ and Davis RJ. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem 1995; 270: 7420-7426.
51. Franklin CC, Kraft AS. Conditional expression of the mitogen-activated protein kinase (MAPK) phosphatase MKP-1 preferentially inhibits p38 MAPK and stress-activated protein kinase in U937 cells. J Biol Chem 1997; 272: 16917-16923.
52. Laderoute KR, Mendonca HL, Calaoagan JM, Knapp AM, Giaccia AJ and Stork PJ. Mitogen-activated protein kinase phosphatase-1 (MKP-1) expression is induced by low oxygen conditions found in solid tumor microenvironments. A candidate MKP for the inactivation of hypoxia- inducible stress-activated protein kinase/c-Jun N-terminal protein kinase activity. J Biol Chem 1999; 274: 12890-12897.
53. Brondello JM, Pouyssegur J and McKenzie FR. Reduced MAP kinase phosphatase-1 degradation after p42/p44MAPK-dependent phosphorylation. Science 1999; 286: 2514-2517.
54. Sohaskey ML, Ferrell JE, Jr. Activation of p42 mitogen-activated protein kinase (MAPK), but not c-Jun NH(2)-terminal kinase, induces phosphorylation and stabilization of MAPK phosphatase XCL100 in Xenopus oocytes. Mol Biol Cell 2002; 13: 454-468.
55. Hutter D, Chen P, Barnes J and Liu Y. Catalytic activation of mitogen-activated protein (MAP) kinase phosphatase-1 by binding to p38 MAP kinase: critical role of the p38 C-terminal domain in its negative regulation. Biochem J 2000; 352 Pt 1: 155-163.
56. Slack DN, Seternes OM, Gabrielsen M and Keyse SM. Distinct binding determinants for erk2/p38alpha and jnk map kinases mediate catalytic activation and substrate selectivity of map kinase phosphatase-1. J Biol Chem 2001; 276: 16491-16500.
57. Stewart AE, Dowd S, Keyse SM and McDonald NQ. Crystal structure of the MAPK phosphatase Pyst1 catalytic domain and implications for regulated activation. Nat Struct Biol 1999; 6: 174-181.
58. Schwan WR, Kugler S, Schuller S, Kopecko DJ and Goebel W. Detection and characterization by differential PCR of host eukaryotic cell genes differentially transcribed following uptake of intracellular bacteria. Infect Immun 1996; 64: 91-99.
59. Kugler S, Schuller S and Goebel W. Involvement of MAP-kinases and -phosphatases in uptake and intracellular replication of Listeria monocytogenes in J774 macrophage cells. FEMS Microbiol Lett 1997; 157: 131-136.
60. Valledor AF, Xaus J, Comalada M, Soler C and Celada A. Protein kinase C epsilon is required for the induction of mitogen-activated protein kinase phosphatase-1 in lipopolysaccharide-stimulated macrophages. J Immunol 2000; 164: 29-37.
61. Chen P, Li J, Barnes J, Kokkonen GC, Lee JC and Liu Y. Restraint of proinflammatory cytokine biosynthesis by mitogen-activated protein kinase phosphatase-1 in lipopolysaccharide-stimulated macrophages. J Immunol 2002; 169: 6408-6416.
62. Shepherd EG, Zhao Q, Welty SE, Hansen TN, Smith CV and Liu Y. The function of mitogen-activated protein kinase phosphatase-1 in peptidoglycan-stimulated macrophages. J Biol Chem 2004; 279: 54023-54031.
63. Zhao Q, Shepherd EG, Manson ME, Nelin LD, Sorokin A and Liu Y. The role of mitogen-activated protein kinase phosphatase-1 in the response of alveolar macrophages to lipopolysaccharide: Attenuation of proinflammatory cytokine biosynthesis via feedback control of p38. J Biol Chem 2005; 280: 8101-8108.
64. Dorfman K, Carrasco D, Gruda M, Ryan C, Lira SA and Bravo R. Disruption of the erp/mkp-1 gene does not affect mouse development: normal MAP kinase activity in ERP/MKP-1-deficient fibroblasts. Oncogene 1996; 13: 925-931.
65. Wang X, Meng X, Kuhlman JR, Nelin LD, Nicol KK, English BK and Liu Y. Knockout of Mkp-1 enhances the host inflammatory responses to Gram-positive bacteria. J Immunol 2007; 178: 5312-5320.
66. Zingarelli B, Cook JA. Peroxisome proliferator-activated receptor-gamma is a new therapeutic target in sepsis and inflammation. Shock 2005; 23: 393-399.
67. Medeiros AI, Serezani CH, Lee SP and Peters-Golden M. Efferocytosis impairs pulmonary macrophage and lung antibacterial function via PGE2/ EP2 signaling. J Exp Med 2009"; 206: 61-68.
68. Ha UH, Lim JH, Kim HJ, Wu W, Jin S, Xu H and Li JD. MKP1 regulates the induction of MUC5AC mucin by Streptococcus pneumoniae pneumolysin by inhibiting the PAK4-JNK signaling pathway. J Biol Chem 2008; 283: 30624-30631.
69. Sommers CL, Samelson LE and Love PE. LAT: a T lymphocyte adapter protein that couples the antigen receptor to downstream signaling pathways. Bioessays 2004; 26: 61-67.
70. Sanchez-Tillo E, Comalada M, Xaus J, Farrera C, Valledor AF, Caelles C, Lloberas J and Celada A. JNK1 Is required for the induction of Mkp1 expression in macrophages during proliferation and lipopolysaccharide-dependent activation. J Biol Chem 2007; 282: 12566-12573.
71. Noguchi T, Metz R, Chen L, Mattei MG, Carrasco D and Bravo R. Structure, mapping, and expression of erp, a growth factor-inducible gene encoding a nontransmembrane protein tyrosine phosphatase, and effect of ERP on cell growth. Mol Cell Biol 1993; 13: 5195-5205.
72. Kwak SP, Hakes DJ, Martell KJ and Dixon JE. Isolation and characterization of a human dual specificity protein-tyrosine phosphatase gene. J Biol Chem 1994; 269: 3596-3604.
73. Li J, Gorospe M, Hutter D, Barnes J, Keyse SM and Liu Y. Transcriptional induction of MKP-1 in response to stress is associated with histone H3 phosphorylation-acetylation. Mol Cell Biol 2001; 21: 8213-8224.
74. Liu Y, Shepherd EG and Nelin LD. MAPK phosphatases - regulating the immune response. Nat Rev Immunol 2007; 7: 202-212.
75. Ananieva O, Darragh J, Johansen C, Carr JM, McIlrath J, Park JM, Wingate A, Monk CE, Toth R, Santos SG, Iversen L and Arthur JS. The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat Immunol 2008; 9: 1028-1036.
76. Jacobs D, Glossip D, Xing H, Muslin AJ and Kornfeld K. Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev 1999; 13: 163-175.
77. Kim HG, Kim NR, Gim MG, Lee JM, Lee SY, Ko MY, Kim JY, Han SH and Chung DK. Lipoteichoic acid isolated from Lactobacillus plantarum inhibits lipopolysaccharide-induced TNF-alpha production in THP-1 cells and endotoxin shock in mice. J Immunol 2008; 180: 2553-2561.
78. West MA, Heagy W. Endotoxin tolerance: A review. Crit Care Med 2002; 30: S64-S73.
79. Liu Y, Shanley TP. Mitogen-activated protein kinase phosphatase-1 and septic shock. J Organ Dysfunct (in press).
80. Cross AS. Endotoxin tolerance-current concepts in historical perspective. J Endotoxin Res 2002; 8: 83-98.
81. Kobayashi K, Hernandez LD, Galan JE, Janeway CA, Jr., Medzhitov R and Flavell RA. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 2002; 110: 191-202.
82. Deng JC, Cheng G, Newstead MW, Zeng X, Kobayashi K, Flavell RA and Standiford TJ. Sepsis-induced suppression of lung innate immunity is mediated by IRAK-M. J Clin Invest 2006; 116: 2532-2542.
83. Wiersinga WJ, Van't Veer C, van den Pangaart PS, Dondorp AM, Day NP, Peacock SJ and van der PT. Immunosuppression associated with interleukin-1R-associated-kinase-M upregulation predicts mortality in Gram-negative sepsis (melioidosis). Crit Care Med 2009.
84. Cao W, Bao C, Padalko E and Lowenstein CJ. Acetylation of mitogen-activated protein kinase phosphatase-1 inhibits Toll-like receptor signaling. J Exp Med 2008; 205: 1491-1503.
85. Tanoue T, Adachi M, Moriguchi T and Nishida E. A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat Cell Biology 2000; 2: 110-116.
86. Swantek JL, Cobb MH and Geppert TD. Jun N-terminal kinase/ stress-activated protein kinase (JNK/SAPK) is required for lipopolysaccharide stimulation of tumor necrosis factor alpha (TNF-alpha) translation: glucocorticoids inhibit TNF-alpha translation by blocking JNK/SAPK. Mol Cell Biol 1997; 17: 6274-6282.
87. Lasa M, Mahtani KR, Finch A, Brewer G, Saklatvala J and Clark AR. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol Cell Biol 2000; 20: 4265-4274.
88. Lasa M, Brook M, Saklatvala J and Clark AR. Dexamethasone destabilizes cyclooxygenase 2 mRNA by inhibiting mitogen-activated protein kinase p38. Mol Cell Biol 2001; 21: 771-780.
89. Lasa M, Abraham SM, Boucheron C, Saklatvala J and Clark AR. Dexamethasone causes sustained expression of mitogen-activated protein kinase (MAPK) phosphatase 1 and phosphatase-mediated inhibition of MAPK p38. Mol Cell Biol 2002; 22: 7802-7811.
90. Kassel O, Sancono A, Kratzschmar J, Kreft B, Stassen M and Cato AC. Glucocorticoids inhibit MAP kinase via increased expression and decreased degradation of MKP-1. EMBO J 2001; 20: 7108-7116.
91. Abraham SM, Lawrence T, Kleiman A, Warden P, Medghalchi M, Tuckermann J, Saklatvala J and Clark AR. Antiinflammatory effects of dexamethasone are partly dependent on induction of dual specificity phosphatase 1. J Exp Med 2006; 203: 1883-1889.
92. Wang X, Nelin LD, Kuhlman JR, Meng X, Welty SE and Liu Y. The role of MAP kinase phosphatase-1 in the protective mechanism of dexamethasone against endotoxemia. Life Sci 2008; 83: 671-680.
93. Bhattacharyya S, Brown DE, Brewer JA, Vogt SK and Muglia LJ. Macrophage glucocorticoid receptors regulate Toll-like receptor 4-mediated inflammatory responses by selective inhibition of p38 MAP kinase. Blood 2007; 109: 4313-4319.
94. Goulding NJ. The molecular complexity of glucocorticoid actions in inflammation - a fourring circus. Curr Opin Pharmacol 2004; 4: 629-636.
95. Maier JV, Brema S, Tuckermann J, Herzer U, Klein M, Stassen M, Moorthy A and Cato AC. Dual specificity phosphatase 1 knockout mice show enhanced susceptibility to anaphylaxis but are sensitive to glucocorticoids. Mol Endocrinol 2007; 21: 2663-2671.
96. Hammer M, Mages J, Dietrich H, Schmitz F, Striebel F, Murray PJ, Wagner H and Lang R. Control of dual-specificity phosphatase-1 expression in activated macrophages by IL-10. Eur J Immunol 2005; 35: 2991-3001.
97. Collart MA, Belin D, Vassalli JD, de Kossodo S and Vassalli P. Gamma interferon enhances macrophage transcription of the tumor necrosis factor/cachectin, interleukin 1, and urokinase genes, which are controlled by short-lived repressors. J Exp Med 1986; 164: 2113-2118.
98. Gordon S. The macrophage. Bioessays 1995; 17: 977-986.
99. Valledor AF, Arpa L, Sanchez-Tillo E, Comalada M, Casals C, Xaus J, Caelles C, Lloberas J and Celada A. IFN-{gamma}-mediated inhibition of MAPK phosphatase expression results in prolonged MAPK activity in response to M-CSF and inhibition of proliferation. Blood 2008; 112: 3274-3282.
100. Valledor AF, Sanchez-Tillo E, Arpa L, Park JM, Caelles C, Lloberas J and Celada A. Selective roles of MAPKs during the macrophage response to IFN-gamma. J Immunol 2008; 180: 4523-4529.
101. Calandra T, Echtenacher B, Roy DL, Pugin J, Metz CN, Hultner L, Heumann D, Mannel D, Bucala R and Glauser MP. Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat Med 2000; 6: 164-170.
102. Roger T, David J, Glauser MP and Calandra T. MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature 2001; 414: 920-924.
103. Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, Cerami A and Bucala R. MIF as a glucocorticoid-induced modulator of cytokine production. Nature 1995; 377: 68-71.
104. Roger T, Chanson AL, Knaup-Reymond M and Calandra T. Macrophage migration inhibitory factor promotes innate immune responses by suppressing glucocorticoid-induced expression of mitogen-activated protein kinase phosphatase-1. Eur J Immunol 2005; 35: 3405-3413.
105. Aeberli D, Yang Y, Mansell A, Santos L, Leech M and Morand EF. Endogenous macrophage migration inhibitory factor modulates glucocorticoid sensitivity in macrophages via effects on MAP kinase phosphatase-1 and p38 MAP kinase. FEBS Lett 2006; 580: 974-981.
106. Fan H, Cook JA. Molecular mechanisms of endotoxin tolerance. J Endotoxin Res 2004; 10: 71-84.
107. Nomura F, Akashi S, Sakao Y, Sato S, Kawai T, Matsumoto M, Nakanishi K, Kimoto M, Miyake K, Takeda K and Akira S. Cutting edge: endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J Immunol 2000; 164: 3476-3479.