Leukemia inhibitory factor is an anti-inflammatory and analgesic cytokine

Journal of Neuroscience

Volumn 18, Issue 14, 1998, Pages 5456-5462

  Banner, Lisa R ^a   Patterson, Paul H ^a   Allchorne, Andrew ^b   Poole, Steve ^c   Woolf, Clifford J ^b,d  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Analgesia; Edema; Hyperalgesia; Inflammation; Pain; Primary sensory neuron

Indexed keywords

ANALGESIC AGENT; ANTIINFLAMMATORY AGENT; CYTOKINE; FREUND ADJUVANT; LEUKEMIA INHIBITORY FACTOR; RECOMBINANT LEUKEMIA INHIBITORY FACTOR; UNCLASSIFIED DRUG;

ANALGESIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; EDEMA; HYPERALGESIA; IMMUNE RESPONSE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SKIN INFLAMMATION;

EID: 0032527595     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-14-05456.1998     Document Type: Article

References (51)

1. Alexander HR, Billingsley KG, Block MI, Fraker DL (1994) D-factor/leukemia inhibitory factor: evidence for its role as a mediator in acute and chronic inflammatory disease. Cytokines 6:589-596.
2. Baba H, Kohno T, Okamoto M, Goldstein PA, Shimoji K, Yoshimura M (1998) Muscarinic facilitation of GABA release in substantia gelatinosa of the rat spinal dorsal horn. J Physiol (Lond) 508:83-93.
3. Banner LR, Patterson PH (1994) Major changes in the expression of the mRNAs for CDF/LIF and its receptor following injury to adult peripheral nerves and ganglia. Proc Natl Acad Sci USA 91:7109-7113.
4. Banner LR, Moayeri NN, Patterson PH (1997) Leukemia inhibitory factor is expressed in astrocytes following cortical injury. Exp Neurol 147:1-9.
5. Barnes PJ (1996) Neuroeffector mechanisms: the interface between inflamniution and neuronal responses. J Allergy Clin Immunol 98:S73-S81.
6. Benigni F, Fantuzzi G, Sacco S, Sironi M, Possi P, Dinarello CA, Sipe JD, Poli V, Cappelletti M, Paonessa G, Pennica D, Panryotatos N, Ghezzi P (1996) Six different cytokines that share GP130 as a receptor subunit induce serum amyloid A and potentiate the induction of interleukin-6 and the activation of the hypothalamus-pituitary-adrenal axis by interleukin-1. Blood 87:1851-1854.
7. Block MI, Berg M, McNamara MJ, Norton JA, Fraker DL, Alexander HR (1993) Passive immunization of mice against D factor blocks lethality and cytokine release during endotoxemia. J Exp Med 178:1085-1090.
8. Brown MA, Metcalf D, Gough NM (1994) Leukemia inhibitory factor and interleukin 6 are expressed at very low levels in the normal adult mouse and are induced by inflammation. Cytokines 6:300-309.
9. Campbell IK, Waring P, Novak U, Hamilton JA (1993) Production of leukemia inhibitory factor by human articular chondrocytes and cartilage in response to interleukin-1 and tumor necrosis factor α. Arthritis Rheum 36:790-794.
10. Carroll GJ, Bell MC, Chapman HM, Mills JN, Robinson WF (1995) Leukemia inhibitory factor induces leukocyte infiltration and cartilage proteoglycan degradation in goat joints. J Interferon Cytokine Res 15:567-573.
11. Corness J, Shi T-J, Xu Z-Q, Brulet P, Hokfelt T (1996) Influence of leukemia inhibitory factor on galanin/GMAP and neuropeptide Y expression in mouse primary sensory neurons after axotomy. Exp Brain Res 112:79-88.
12. Dinarello CA (1996) Biological basis for interleukin-1 in disease. Blood 87:2095-2147
13. Donnerer J, Schuligoi R, Stein C (1992) Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: evidence for a regulatory function of nerve growth factor in vivo. Neuroscience 49:693-698.
14. + current in nociceptors. Proc Natl Acad Sci USA 93:1108-1112.
15. Heyman D, L'Her E, Nguyen J-M, Raher S, Canfrere I, Coupey L, Fixe P, Chailleux S, De Grotte D, Praloran V, Godard A (1996) Leukemia inhibitory factor (LIF) production in pleural effusions: comparison with production of IL-4, IL-8, IL-10, and macrophage-colony stimulating factor (M-CSF). Cytokines 8:410-416.
16. Kurek JB, Austin L, Cheema SS, Bartlett PF, Murphy M (1996) Upregulation of leukemia inhibitory factor and interleukin-6 in transected sciatic nerve and muscle following denervation. Neuromuscul Disord 6:105-114.
17. Leslie TA, Emson PC, Dowd PM, Woolf CJ (1995) Nerve growth factor contributes to the upregulation of GAP-43 and preprotachykinin A mRNA in primary sensory neurons following peripheral inflammation. Neuroscience 67:753-761.
18. Levine JD, Taiwo YO (1994) Inflammatory pain. In: Textbook of Pain (Wall PD, Melzack R, eds), pp 45-56. Edinburgh: Churchill Livingstone.
19. Lewin GR, Ritter AM, Mendell LM (1993) Nerve growth factor-induced hyperalgesia in the neonatal and adult rat. J Neurosci 13:2136-2148.
20. Lewin GR, Rueff A, Mendell LM (1994) Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur J Neurosci 6:1903-1912.
21. Liles WC, van Voorhis WC (1995) Review: nomenclature and biological significance of cytoki nes involved in inflammation and the host immune response. J Infect Dis 172:1573-1580.
22. Lotz M, Moats T, Villiger PM (1992) Leukemia inhibitory factor is expressed in cartilage and synovium and can contribute to the pathogenesis of arthritis. J Clin Invest 90:888-896.
23. Lynn B, Schutterle S, Pierau FK (1996) The vasodilator component of neurogenic inflammation is caused by a special subclass of heat-sensitive nociceptors in the skin of the pig. J Physiol (Lond) 494:587-593.
24. McKenzie RC, Paglia D, Kondo S, Sauder DN (1996) A novel endogenous mediator of cutaneous inflammation: leukemia inhibitory factor. Acta Derm Venereol (Stockh) 76:111-114.
25. McMahon SB, Bennett DLH, Priestley JV, Shelton DL (1995) The biological effects of endogenous NGF in adult sensory neurones revealed by a trkA IgG fusion molecule. Nat Med 1:774-780.
26. Mehlen P, Hickey E, Weber LA, Arrigo A-P (1997) Large unphosphorylated aggregates as the active form of hsp27 which controls intracellular reactive oxygen species and glutathione levels and generates a protection against TNFα in NIH-3T3-ras cells. Biochem Biophys Res Commun 241:187-192.
27. Neumann S, Doubell TP, Leslie TA, Woolf CJ (1996) Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurones. Nature 384:360-364.
28. Paglia D, Kondo S, Ng K-M, Sauder DN, McKenzie RC (1996) Leukemia inhibitory factor is expressed by normal human keratinocytes in vitro and in vivo. Br J Dermatol 134:817-823.
29. Patterson PH (1994) Leukemia inhibitory factor, a cytokine at the interface between neurobiology and immunology. Proc Natl Acad Sci USA 91:7833-7835.
30. Patterson PH, Kou S-Y, Sugiura S, Lahav R, Banner LR (1997) LIF coordinates neuronal and inflammatory responses to nerve injury. Soc Neurosci Abstr 23:997.
31. Perry GW, Burmeister DW, Grafstein B (1987) Fast axonally transported proteins in regenerating goldfish optic axons. J Neurosci 7:792-806.
32. Rao MS, Sun Y, Escrary JL, Perreau J, Tresser S, Patterson PH, Zigmond RE, Brulet P, Landes SL (1993) Leukemia inhibitory factor mediates an injury response but not a target-directed developmental transmitter switch in sympathetic neurons. Neuron 11:1175-1185.
33. Reeh PW (1994) Chemical excitation and sensitization of nociceptors. In: Cellular mechanisms of sensory processing, NATO ASI series, Cell biology, vol 79 (Urban L, ed), pp 119-131. Berlin: Springer.
34. Ryffel B (1993) Pathology induced by leukemia inhibitory factor. Int Rev Exp Pathol 34:69-72
35. Safieh-Garabedian B, Poole S, Allchorne A, Winter J, Woolf CJ (1995) Contribution of imerleukin-1/3 to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br J Pharmacol 115:1265-1275.
36. Sendtner M, Gotz R, Holtman B, Escary J-L, Masu Y, Carroll P, Wolf E, Brem G, Brulet P, Thoenen H (1996) Cryptic physiological trophic support of motoneurons by LIF revealed by double gene targeting of CNTF and LIF. Curr Biol 6:686-694.
37. Shimon I, Van X, Ray DW, Melmed S (1997) Cytokine-dependent gp130 receptor subunit regulates human fetal pituitary adrenocorticotropin hormone and growth hormone secretion. J Clin Invest 100:357-363.
38. Stahl N, Yancopoulos GD (1994) The tripartite CNRF receptor complex: activation and signaling involves components shared with other cytokines. J Neurobiol 25:1454-1466.
39. Stein C, Millan MJ, Herz A (1988) Unilateral inflammation of the hindpaw in rats as a model of prolonged noxious stimulation: alterations in behavior and noeiceptive thresholds. Pharmacol Biochem Behav 31:445-451.
40. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ (1992) Blastocyst implantation depends on maternal expression of leukemia inhibitory factor. Nature 359:76-79.
41. Sun Y, Zigmond RE (1996) Leukemia inhibitory factor induced in the sciatic nerve after axotomy is involved in the induction of galanin in sensory neurons. Eur J Neurosci 8:2213-2220.
42. Szepietowski JC, McKenzie RC, Keohane SG, Walker C, Aldridge RD, Hunter JA (1997) Leukemia inhibitory factor: induction in the early phase of allergic contact dermatitis. Contact Dermatitis 36:21-57.
43. Thompson SWN, Dray A, Urban L (1996) Leukemia inhibitory factor induces mechanical allodynia but not thermal hyperalgesia in the juvenile rat. Neuroscience 71:1091-1094.
44. Ulich TR, Fann M-J, Patterson PH, Williams JH, Samal B, Del Castillo J, Yin S, Guo K, Remick DG (1994) Intratracheal injection of LPS and cytokines. V. LPS induces expression of LIF and LIF inhibits acute inflammation. Am J Physiol 267:442-446.
45. Waring P, Wycherley K, Gary D, Nicola N, Metcalf D (1992) Leukemia inhibitory factor levels arc elevated in septic shock and various inflammatory body fluids. J Clin Invest 90:2031-2037.
46. Watkins LR, Maier SF, Goehler LE (1995) Immune activation: the role of proinflammatory cytokines in inflammation, illness responses and pathological pain states. Pain 63:289-302.
47. Weinhold B, Ruther U (1997) Interleukin-6-dependent and-independent regulation of the human C-reactive protein gene. Biochem J 327:425-429.
48. Woolf CJ (1983) Evidence for a central component of postinjury pain hypersensitivity. Nature 306:686-688.
49. Woolf CJ, Safieh-Garabedian B, Ma Q-P, Crilly P, Winter J (1994) Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity. Neuroscience 62:327-331.
50. Woolf CJ, Ma Q-P, Allchorne A, Poole S (1996) Peripheral cell types contributing to the hyperalgesic action of nerve growth factor in inflammation. J Neurosci 16:2716-2723.
51. Woolf CJ, Allchorne A, Safieh-Garabedian B, Poole S (1997) Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumor necrosis factor a. Br J Pharmacol 121:417-424.