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PMID: 11086030 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The proinflammatory mediator macrophage migration inhibitory factor induces glucose catabolism in muscle.

The Journal of clinical investigation ·Vol. 106 ·No. 10 ·2000-11-00 ·Pages 1291-300

Benigni F, Atsumi T, Calandra T, Metz C, Echtenacher B, Peng T, Bucala R

Abstract

Severe infection or tissue invasion can provoke a catabolic response, leading to severe metabolic derangement, cachexia, and even death. Macrophage migration inhibitory factor (MIF) is an important regulator of the host response to infection. Released by various immune cells and by the anterior pituitary gland, MIF plays a critical role in the systemic inflammatory response by counterregulating the inhibitory effect of glucocorticoids on immune-cell activation and proinflammatory cytokine production. We describe herein an unexpected role for MIF in the regulation of glycolysis. The addition of MIF to differentiated L6 rat myotubes increased synthesis of fructose 2,6-bisphosphate (F2,6BP), a positive allosteric regulator of glycolysis. Increased expression of the enzyme 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase (PFK-2) enhanced F2,6BP production and, consequently, cellular lactate production. The catabolic effect of TNF-alpha on myotubes was mediated by MIF, which served as an autocrine stimulus for F2, 6BP production. TNF-alpha administered to mice decreased serum glucose levels and increased muscle F2,6BP levels; pretreatment with a neutralizing anti-MIF mAb completely inhibited these effects. Anti-MIF also prevented hypoglycemia and increased muscle F2,6BP levels in TNF-alpha-knockout mice that were administered LPS, supporting the intrinsic contribution of MIF to these inflammation-induced metabolic changes. Taken together with the recent finding that MIF is a positive, autocrine stimulator of insulin release, these data suggest an important role for MIF in the control of host glucose disposal and carbohydrate metabolism.

MeSH Terms
Animals Cell Line Cell Movement/physiology Fructosediphosphates/biosynthesis Glucose/metabolism Glycolysis/drug effects Humans Lactic Acid/biosynthesis Liver/metabolism Macrophage Migration-Inhibitory Factors/metabolism,pharmacology Macrophages/metabolism Mice Muscles/metabolism Phosphofructokinase-2 Phosphoric Monoester Hydrolases/metabolism Phosphotransferases (Alcohol Group Acceptor)/metabolism Rats Tumor Cells, Cultured Tumor Necrosis Factor-alpha/pharmacology
Chemicals
Fructosediphosphates Macrophage Migration-Inhibitory Factors Tumor Necrosis Factor-alpha Lactic Acid fructose 2,6-diphosphate Phosphotransferases (Alcohol Group Acceptor) Phosphofructokinase-2 Phosphoric Monoester Hydrolases Glucose
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Benigni F
The Picower Institute for Medical Research, Manhasset, New York 10030, USA.
Atsumi T
Calandra T
Metz C
Echtenacher B
Peng T
Bucala R
References (56)
56 references, click to expand
  1. Human recombinant IL-1 alters glucocorticoid receptor function in Reuber hepatoma cells.
    J Immunol. 1988 Sep 1;141(5):1522-8 PMID: 2842396
  2. Molecular cloning of a cDNA encoding a human macrophage migration inhibitory factor.
    Proc Natl Acad Sci U S A. 1989 Oct;86(19):7522-6 PMID: 2552447
  3. Tumor necrosis factor enhances glucose uptake by peripheral tissues.
    Am J Physiol. 1989 Nov;257(5 Pt 2):R1182-9 PMID: 2589544
  4. Lethal hypoglycemia and hypothermia induced by administration of low doses of tumor necrosis factor to adrenalectomized rats.
    Metabolism. 1990 Mar;39(3):242-50 PMID: 2155369
  5. Tumor necrosis factor acutely increases plasma levels of very low density lipoproteins of normal size and composition.
    Endocrinology. 1990 Sep;127(3):1016-21 PMID: 2387245
  6. Tumor necrosis factor mimics the metabolic response to acute infection in healthy humans.
    Am J Physiol. 1991 Oct;261(4 Pt 1):E457-65 PMID: 1928337
  7. Chronic intraperitoneal infusion of low doses of tumor necrosis factor alpha in rats induces a reduction in plasma triglyceride levels.
    Cytokine. 1992 Nov;4(6):561-7 PMID: 1292639
  8. Mammalian 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: a bifunctional enzyme that controls glycolysis.
    Prog Nucleic Acid Res Mol Biol. 1993;45:99-127 PMID: 8393580
  9. Fructose 2,6-bisphosphate and the control of glycolysis by growth factors, tumor promoters and oncogenes.
    Adv Enzyme Regul. 1993;33:97-110 PMID: 8395137
  10. Tumor necrosis factor: an updated review of its biology.
    Crit Care Med. 1993 Oct;21(10 Suppl):S415-22 PMID: 8403979
  11. MIF is a pituitary-derived cytokine that potentiates lethal endotoxaemia.
    Nature. 1993 Oct 21;365(6448):756-9 PMID: 8413654
  12. Cachectin/TNF-mediated lactate production in cultured myocytes is linked to activation of a futile substrate cycle.
    Cytokine. 1993 Sep;5(5):436-47 PMID: 8142598
  13. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor.
    J Exp Med. 1994 Jun 1;179(6):1895-902 PMID: 8195715
  14. Correlation between fructose 2,6-bisphosphate and lactate production in skeletal muscle.
    J Appl Physiol (1985). 1994 May;76(5):2169-76 PMID: 8063683
  15. Tumor necrosis factor alpha: a key component of the obesity-diabetes link.
    Diabetes. 1994 Nov;43(11):1271-8 PMID: 7926300
  16. Purification, bioactivity, and secondary structure analysis of mouse and human macrophage migration inhibitory factor (MIF).
    Biochemistry. 1994 Nov 29;33(47):14144-55 PMID: 7947826
  17. The structure and physicochemical properties of rat liver macrophage migration inhibitory factor.
    Biochim Biophys Acta. 1995 Feb 22;1247(1):159-62 PMID: 7873586
  18. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance.
    J Clin Invest. 1995 May;95(5):2409-15 PMID: 7738205
  19. MIF as a glucocorticoid-induced modulator of cytokine production.
    Nature. 1995 Sep 7;377(6544):68-71 PMID: 7659164
  20. Effects of tumour necrosis factor alpha (TNF alpha) on glucose transport and lipid metabolism of newly-differentiated human fat cells in cell culture.
    Diabetologia. 1995 Jul;38(7):764-71 PMID: 7556976
  21. Localization of macrophage migration inhibitory factor (MIF) to secretory granules within the corticotrophic and thyrotrophic cells of the pituitary gland.
    Mol Med. 1995 Nov;1(7):781-8 PMID: 8612200
  22. Effect of tumor necrosis factor-alpha on insulin action in cultured rat skeletal muscle cells.
    Endocrinology. 1996 Jun;137(6):2441-6 PMID: 8641197
  23. Metabolism of sepsis and multiple organ failure.
    World J Surg. 1996 May;20(4):460-4 PMID: 8662135
  24. An essential regulatory role for macrophage migration inhibitory factor in T-cell activation.
    Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7849-54 PMID: 8755565
  25. Effect of tumor necrosis factor-alpha on basal and insulin-stimulated glucose transport in cultured muscle and fat cells.
    Metabolism. 1996 Sep;45(9):1089-94 PMID: 8781295
  26. TNF-alpha stimulates glucose uptake in L6 myoblasts.
    Diabetes Res Clin Pract. 1996 Apr;32(1-2):11-8 PMID: 8803477
  27. MIF rediscovered: cytokine, pituitary hormone, and glucocorticoid-induced regulator of the immune response.
    FASEB J. 1996 Dec;10(14):1607-13 PMID: 9002552
  28. Migration inhibitory factor expression in experimentally induced endotoxemia.
    Am J Pathol. 1997 Jan;150(1):235-46 PMID: 9006339
  29. Regulatory role for macrophage migration inhibitory factor in acute respiratory distress syndrome.
    Nat Med. 1997 Mar;3(3):320-3 PMID: 9055860
  30. The pathogenic role of macrophage migration inhibitory factor in immunologically induced kidney disease in the rat.
    J Exp Med. 1997 Apr 21;185(8):1455-65 PMID: 9126926
  31. Insulin secretion is regulated by the glucose-dependent production of islet beta cell macrophage migration inhibitory factor.
    Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4782-7 PMID: 9114069
  32. TNF-alpha has no direct in vivo metabolic effect on human muscle.
    Int J Cancer. 1997 Apr 10;71(2):148-54 PMID: 9139834
  33. Tumor necrosis factor inhibits the transcriptional rate of glucose-6-phosphatase in vivo and in vitro.
    Metabolism. 1997 May;46(5):579-83 PMID: 9160827
  34. Macrophage migration inhibitory factor is involved in the pathogenesis of collagen type II-induced arthritis in mice.
    J Immunol. 1997 Jun 1;158(11):5514-7 PMID: 9164975
  35. Acute and chronic exposure to tumor necrosis factor-alpha fails to affect insulin-stimulated glucose metabolism of isolated rat soleus muscle.
    Endocrinology. 1997 Jul;138(7):2674-9 PMID: 9202203
  36. Cytokines modulate glucose transport in skeletal muscle by inducing the expression of inducible nitric oxide synthase.
    Biochem J. 1997 Jul 15;325 ( Pt 2):487-93 PMID: 9230132
  37. Insulin-like growth factor-I improves glucose utilization in tumor necrosis factor-treated rats under hyperinsulinemic-euglycemic conditions.
    Metabolism. 1997 Sep;46(9):1052-8 PMID: 9284895
  38. Human circulating eosinophils secrete macrophage migration inhibitory factor (MIF). Potential role in asthma.
    J Clin Invest. 1998 Jun 15;101(12):2869-74 PMID: 9637721
  39. Macrophage migration inhibitory factor is a critical mediator of the activation of immune cells by exotoxins of Gram-positive bacteria.
    Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11383-8 PMID: 9736745
  40. Effects of tumor necrosis factor-alpha on glucose metabolism in cultured human muscle cells from nondiabetic and type 2 diabetic subjects.
    Endocrinology. 1998 Dec;139(12):4793-800 PMID: 9832415
  41. Targeted disruption of migration inhibitory factor gene reveals its critical role in sepsis.
    J Exp Med. 1999 Jan 18;189(2):341-6 PMID: 9892616
  42. An inducible gene product for 6-phosphofructo-2-kinase with an AU-rich instability element: role in tumor cell glycolysis and the Warburg effect.
    Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):3047-52 PMID: 10077634
  43. TNF-alpha impairs insulin signaling and insulin stimulation of glucose uptake in C2C12 muscle cells.
    Am J Physiol. 1999 May;276(5 Pt 1):E849-55 PMID: 10329978
  44. 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. 1999 Jun 18;274(25):18100-6 PMID: 10364264
  45. Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids.
    Arthritis Rheum. 1999 Aug;42(8):1601-8 PMID: 10446857
  46. MIF mediation of sepsis.
    Nat Med. 2000 Feb;6(2):140-1 PMID: 10655098
  47. Protection from septic shock by neutralization of macrophage migration inhibitory factor.
    Nat Med. 2000 Feb;6(2):164-70 PMID: 10655104
  48. Tumor necrosis factor-alpha inhibits leptin production in subcutaneous and omental adipocytes from morbidly obese humans.
    J Clin Endocrinol Metab. 2000 Feb;85(2):530-5 PMID: 10690850
  49. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity.
    Science. 1966 Jul 1;153(3731):80-2 PMID: 5938421
  50. Studies on the mechanisms underlying adaptive changes in rat liver phosphoenolpyruvate carboxykinase.
    Biochemistry. 1966 Feb;5(2):555-62 PMID: 5940940
  51. The enzymatic carboxylation of phosphoenolpyruvate. II. Purification and properties of liver mitochondrial phosphoenolpyruvate carboxykinase.
    J Biol Chem. 1966 May 25;241(10):2413-20 PMID: 5911620
  52. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction.
    Proc Natl Acad Sci U S A. 1966 Jul;56(1):72-7 PMID: 5229858
  53. Influence of endotoxin treatment on dexamethasone induction of hepatic phosphoenolpyruvate carboxykinase.
    Infect Immun. 1983 Jan;39(1):213-9 PMID: 6822414
  54. A kinetic study of pyrophosphate: fructose-6-phosphate phosphotransferase from potato tubers. Application to a microassay of fructose 2,6-bisphosphate.
    Eur J Biochem. 1982 Dec;129(1):191-5 PMID: 6297885
  55. The contribution of gluconeogenesis to glycogen repletion during glucose infusion in endotoxemia.
    Metabolism. 1987 Feb;36(2):180-7 PMID: 3543615
  56. Effect of endotoxin-induced monokines on glucose metabolism in the muscle cell line L6.
    Proc Natl Acad Sci U S A. 1987 May;84(9):2590-4 PMID: 3472226
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2000-11-00
Pages
1291-300
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC381433
Subset
IM
Grants
NIAID NIH HHS · R01 AI042310 · United States
NIAID NIH HHS · 1 R01 AI 42310-01 · United States
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