An anti-inflammatory role for leukemia inhibitory factor receptor signaling in regenerating skeletal muscle

Histochemistry and Cell Biology

Volumn 139, Issue 1, 2013, Pages 13-34

  Hunt, Liam C ^a,b   Upadhyay, Aradhana ^c   Jazayeri, Jalal A ^c   Tudor, Elizabeth M ^a   White, Jason D ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ROYAL CHILDREN'S HOSPITAL   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Cytokines; Inflammation; Leukemia inhibitory factor; Myogenic differentiation; Regeneration; Skeletal muscle

Indexed keywords

CYTOKINE RECEPTOR ANTAGONIST; INTERLEUKIN 1BETA; INTERLEUKIN 6; LEUKEMIA INHIBITORY FACTOR RECEPTOR; MH 35 BD; MYOGENIN; NOTEXIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATORY CELL; MACROPHAGE; MALE; MAST CELL; MOUSE; MUSCLE REGENERATION; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; TISSUE HOMOGENATE;

ANIMALS; CELLS, CULTURED; CYTOKINES; ELAPID VENOMS; GENE EXPRESSION REGULATION; INFLAMMATION; INFLAMMATION MEDIATORS; INJECTIONS, INTRAPERITONEAL; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR ALPHA SUBUNIT; MACROPHAGES; MALE; MAST CELLS; MICE; MICE, INBRED C57BL; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MUTATION; MYOGENIN; NEUTROPHILS; RECOMBINANT PROTEINS; REGENERATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS;

MUS;

EID: 84872319737     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-012-1018-0     Document Type: Article

References (67)

1. Akita S, Malkin J, Melmed S (1996) Disrupted murine leukemia inhibitory factor (LIF) gene attenuates adrenocorticotropic hormone (ACTH) secretion. Endocrinology 137:3140 (Pubitemid 26192213)
2. Alter J, Rozentzweig D, Bengal E (2008) Inhibition of myoblast differentiation by tumor necrosis factor is mediated by c-Jun N-terminal Kinase 1 and leukemia inhibitory factor. J Biol Chem 283:23224
3. Alvarez B, Quinn LBS, Busquets S, Quiles MT, López-Soriano FJ, Argilés JM (2002) Tumor necrosis factor-[alpha] exerts interleukin-6-dependent and-independent effects on cultured skeletal muscle cells. Biochimica et Biophysica Acta (BBA)-Mol Cell Res 1542:66-72
4. Austin L, Burgess A (1991) Stimulation of myoblast proliferation in culture by leukaemia inhibitory factor and other cytokines. J Neurol Sci 101:193-197
5. Austin L, Bower J, Kurek J, Vakakis N (1992) Effects of leukaemia inhibitory factor and other cytokines on murine and human myoblast proliferation. J Neurol Sci 112:185-191
6. Austin L, Bower J, Bennett T, Lynch G, Kapsa R, White J, Barnard W, Gregorevic P, Byrne E (2000) Leukemia inhibitory factor ameliorates muscle fiber degeneration in the mdx mouse. Muscle Nerve 23:1700-1705
7. Bamberger AM, Schulte HM, Wullbrand A, Jung R, Beil FU, Bamberger CM (2000) Expression of leukemia inhibitory factor (LIF) and LIF receptor (LIF-R) in the human adrenal cortex: implications for steroidogenesis. Mol Cell Endocrinol 162:145-149 (Pubitemid 30347457)
8. Banner LR, Patterson PH, Allchorne A, Poole S, Woolf CJ (1998) Leukemia inhibitory factor is an anti-inflammatory and analgesic cytokine. J Neurosci 18:5456
9. Barnard W, Bower J, Brown MA, Murphy M, Austin L (1994) Leukemia inhibitory factor (LIF) infusion stimulates skeletal muscle regeneration after injury: injured muscle expresses lif mRNA. J Neurol Sci 123:108-113 (Pubitemid 24167435)
10. Bower J, Vakakis N, Nicola N, Austin L (1995) Specific binding of leukemia inhibitory factor to murine myoblasts in culture. J Cell Physiol 164:93-98
11. Briguet A, Courdier-Fruh I, Foster M, Meier T, Magyar JP (2004) Histological parameters for the quantitative assessment of muscular dystrophy in the mdx-mouse. Neuromuscul Disord 14:675-682 (Pubitemid 39194668)
12. Broussard SR, McCusker RH, Novakofski JE, Strle K, Shen WH, Johnson RW, Dantzer R, Kelley KW (2004) IL-1 impairs insulin-like growth factor I-induced differentiation and downstream activation signals of the insulin-like growth factor I receptor in myoblasts. J Immunol 172:7713
13. Contreras-Shannon V, Ochoa O, Reyes-Reyna SM, Sun D, Michalek JE, Kuziel WA, McManus LM, Shireman PK (2007) Fat accumulation with altered inflammation and regeneration in skeletal muscle of CCR2-/-mice following ischemic injury. Am J Physiol-Cell Physiol 292:C953
14. Duluc D, Delneste Y, Tan F, Moles MP, Grimaud L, Lenoir J, Preisser L, Anegon I, Catala L, Ifrah N (2007) Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood 110:4319-4330 (Pubitemid 351377797)
15. Fairlie WD, Uboldi AD, McCoubrie JE, Wang CC, Lee EF, Yao S, De Souza DP, Mifsud S, Metcalf D, Nicola NA (2004) Affinity maturation of leukemia inhibitory factor and conversion to potent antagonists of signaling. J Biol Chem 279:2125 (Pubitemid 38084486)
16. Fielding R, Manfredi T, Ding W, Fiatarone M, Evans W, Cannon J (1993) Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in skeletal muscle. Am J Physiol-Regul, Integr Comp Physiol 265:R166
17. Gadient RA, Patterson PH (1999) Leukemia inhibitory factor, interleukin 6, and other cytokines using the GP130 transducing receptor: roles in inflammation and injury. Stem Cells 17:127-137 (Pubitemid 29226663)
18. Galli SJ, Zsebo KM, Geissler EN (1993) The kit ligand, stem cell factor. Adv Immunol 55:1-96
19. Gearing DP, Gough N, King J, Hilton D, Nicola N, Simpson R, Nice E, Kelso A, Metcalf D (1987) Molecular cloning and expression of cDNA encoding a murine myeloid leukaemia inhibitory factor (LIF). EMBO J 6:3995
20. Gearing DP, Comeau MR, Friend DJ, Gimpel SD, Thut CJ, McGourty J, Brasher KK, King JA, Gillis S, Mosley B (1992) The IL-6 signal transducer, gp130: an oncostatin M receptor and affinity converter for the LIF receptor. Science 255:1434
21. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23-35 (Pubitemid 37328697)
22. Gorospe JRM, Tharp M, Demitsu T, Hoffman EP (1994) Dystrophin-deficient myofibers are vulnerable to mast cell granule-induced necrosis. Neuromuscul Disord 4:325-333 (Pubitemid 24280929)
23. Gregorevic P, Hayes A, Lynch GS, Williams DA (2000) Functional properties of regenerating skeletal muscle following LIF administration. Muscle Nerve 23:1586-1588
24. Helliwell T, Gunhan O, Edwards R (1990) Mast cells in neuromuscular diseases. J Neurol Sci 98:267-276 (Pubitemid 20288822)
25. Hendriks JJA, Slaets H, Carmans S, de Vries HE, Dijkstra CD, Stinissen P, Hellings N (2008) Leukemia inhibitory factor modulates production of inflammatory mediators and myelin phagocytosis by macrophages. J Neuroimmunol 204:52-57
26. Hilton D, Nicola N, Metcalf D (1988) Specific binding of murine leukemia inhibitory factor to normal and leukemic monocytic cells. Proc Nat Acad Sci 85:5971
27. Hilton DJ, Nicola NA, Waring PM, Metcalf D (1991) Clearance and fate of leukemia inhibitory factor (LIF) after injection into mice. J Cell Physiol 148:430-439 (Pubitemid 21926079)
28. Hodgetts S, Radley H, Davies M, Grounds MD (2006) Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking TNFα function with Etanercept in mdx mice. Neuromuscul Disord: NMD 16:591-602 (Pubitemid 44374323)
29. Holtmann B, Wiese S, Samsam M, Grohmann K, Pennica D, Martini R, Sendtner M (2005) Triple knock-out of CNTF, LIF, and CT-1 defines cooperative and distinct roles of these neurotrophic factors for motoneuron maintenance and function. J Neurosci 25:1778 (Pubitemid 40279283)
30. Hunt L, Tudor E, White J (2010) Leukemia inhibitory factor-dependent increase in myoblast cell number is associated with phosphotidylinositol 3-kinase-mediated inhibition of apoptosis and not mitosis. Exp Cell Res 316:1002-1009
31. Hunt LC, Upadhyay A, Jazayeri JA, Tudor EM, White JD (2011) Caspase-3, myogenic transcription factors and cell cycle inhibitors are regulated by leukemia inhibitory factor to mediate inhibition of myogenic differentiation. Skeletal Muscle 1:17
32. Iida N, Grotendorst GR (1990) Cloning and sequencing of a new gro transcript from activated human monocytes: expression in leukocytes and wound tissue. Mol Cell Biol 10:5596
33. Jazayeri JA, De Weerd N, Raye W, Kivivuori S, Zabihi E, Carroll GJ (2007) In vitro evaluation of leukemia inhibitory factor receptor antagonists as candidate therapeutics for inflammatory arthritis. J Interferon Cytokine Res 27:281-290 (Pubitemid 46786930)
34. Jo C, Kim H, Jo I, Choi I, Jung SC, Kim J, Kim SS, Jo SA (2005) Leukemia inhibitory factor blocks early differentiation of skeletal muscle cells by activating ERK. Biochimica et Biophysica Acta (BBA)-Molecul Cell Res 1743:187-197 (Pubitemid 40544414)
35. Kovanen PT, Kaartinen M, Paavonen T (1995) Infiltrates of activated mast cells at the site of coronary atheromatous erosion or rupture in myocardial infarction. Circulation 92:1084-1088
36. Kurek JB, Nouri S, Kannourakis G, Murphy M, Austin L (1996) Leukemia inhibitory factor and interleukin-6 are produced by diseased and regenerating skeletal muscle. Muscle Nerve 19:1291-1301 (Pubitemid 26313826)
37. Kurek JB, Bower JJ, Romanella M, Koentgen F, Murphy M, Austin L (1997) The role of leukemia inhibitory factor in skeletal muscle regeneration. Muscle Nerve 20:815-822 (Pubitemid 27250667)
38. Kwon YW, Abbondanzo SJ, Stewart CL, Gurney ME (1995) Leukemia inhibitory factor influences the timing of programmed synapse withdrawal from neonatal muscles. J Neurobiol 28:35-50
39. Layton MJ, Owczarek CM, Metcalf D, Clark RL, Smith DK, Treutlein HR, Nicola NA (1994) Conversion of the biological specificity of murine to human leukemia inhibitory factor by replacing 6 amino acid residues. J Biol Chem 269:29891-29896 (Pubitemid 24365155)
40. Lefaucheur JP, Sebille A (1995) Muscle regeneration following injury can be modified in vivo by immune neutralization of basic fibroblast growth factor, transforming growth factor [beta] 1 or insulin-like growth factor I. J Neuroimmunol 57:85-91
41. Li YP (2003) TNF- is a mitogen in skeletal muscle. Am J Physiol-Cell Physiol 285:C370
42. Metcalf D, Hilton D, Nicola N (1988) Clonal analysis of the actions of the murine leukemia inhibitory factor on leukemic and normal murine hemopoietic cells. Leuk Off J Leuk Soc Am, Leuk Res Fund, UK 2:216
43. Miyake T, Alli NS, Aziz A, Knudson J, Fernando P, Megeney LA, McDermott JC (2009) Cardiotrophin-1 maintains the undifferentiated state in skeletal myoblasts. J Biol Chem 284:19679
44. Moritz DR, Rodewald H-R, Gheyselinck J, Klemenz R (1998) The IL-1 receptor-related T1 antigen is expressed on immature and mature mast cells and on fetal blood mast cell progenitors. J Immunol 161:4866-4874 (Pubitemid 28492065)
45. Nishikawa J, Sakuma K, Sorimachi Y, Yoshimoto K, Yasuhara M (2005) Increase of cardiotrophin 1 immunoreactivity in regenerating and overloaded but not denervated muscles of rats. Neuropathology 25:54-65 (Pubitemid 40477713)
46. Ochoa O, Sun D, Reyes-Reyna SM, Waite LL, Michalek JE, McManus LM, Shireman PK (2007) Delayed angiogenesis and VEGF production in CCR2-/-mice during impaired skeletal muscle regeneration. Am J Physiol Regul Integrat Comp Physiol 293:R651 (Pubitemid 47205047)
47. Pelus LM, Fukuda S (2006) Peripheral blood stem cell mobilization: the CXCR2 ligand GRO [beta] rapidly mobilizes hematopoietic stem cells with enhanced engraftment properties. Exp Hematol 34:1010-1020 (Pubitemid 44080384)
48. Peterson JM, Feeback KD, Baas JH, Pizza FX (2006) Tumor necrosis factor-α promotes the accumulation of neutrophils and macrophages in skeletal muscle. J Appl Physiol 101:1394
49. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
50. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509-515 (Pubitemid 38448421)
51. Radley HG, Grounds MD (2006) Cromolyn administration (to block mast cell degranulation) reduces necrosis of dystrophic muscle in mdx mice. Neurobiol Dis 23:387-397 (Pubitemid 44097034)
52. Ray DW, Ren SG, Melmed S (1996) Leukemia inhibitory factor (LIF) stimulates proopiomelanocortin (POMC) expression in a corticotroph cell line. Role of STAT pathway. J Clin Investig 97:1852
53. Schofield G, Kimber SJ (2005) Leukocyte subpopulations in the uteri of leukemia inhibitory factor knockout mice during early pregnancy. Biol Reprod 72:872-878 (Pubitemid 40404261)
54. Shireman PK, Contreras-Shannon V, Ochoa O, Karia BP, Michalek JE, McManus LM (2007) MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration. J Leukoc Biol 81:775 (Pubitemid 46393555)
55. Spencer MJ, Montecino-Rodriguez E, Dorshkind K, Tidball JG (2001) Helper (CD4+) and cytotoxic (CD8+) T cells promote the pathology of dystrophin-deficient muscle. Clin Immunol 98:235-243 (Pubitemid 32150612)
56. Srikuea R, Esser KA, Pholpramool C (2011) Leukaemia inhibitory factor is expressed in rat gastrocnemius muscle after contusion and increases proliferation of rat L6 myoblasts via c-Myc signalling. Clin Exp Pharmacol Physiol 38:501-509
57. Tham S, Dowsing B, Finkelstein D, Donato R, Cheema SS, Bartlett PF, Morrison WA (1997) Leukemia inhibitory factor enhances the regeneration of transected rat sciatic nerve and the function of reinnervated muscle. J Neurosci Res 47:208-215 (Pubitemid 27053379)
58. Tidball JG, Villalta SA (2010) Regulatory interactions between muscle and the immune system during muscle regeneration. Am J Physiol Regul Integrat Comp Physiol 298:R1173
59. Upadhyay A, Sharma G, Kivivuori S, Raye WS, Zabihi E, Carroll GJ, Jazayeri JA (2009) Role of a LIF antagonist in LIF and OSM induced MMP-1, MMP-3, and TIMP-1 expression by primary articular chondrocytes. Cytokine 46:332-338
60. Villalta SA, Rinaldi C, Deng B, Liu G, Fedor B, Tidball JG (2011) Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype. Hum Mol Genet 20:790-805
61. Wang X, Wu H, Zhang Z, Liu S, Yang J, Chen X, Fan M (2008) Effects of interleukin-6, leukemia inhibitory factor, and ciliary neurotrophic factor on the proliferation and differentiation of adult human myoblasts. Cell Mol Neurobiol 28:113-124
62. Wehling M, Spencer MJ, Tidball JG (2001) A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 155:123-132 (Pubitemid 34286213)
63. White JD, Davies M, Grounds MD (2001) Leukaemia inhibitory factor increases myoblast replication and survival and affects extracellular matrix production: combined in vivo and in vitro studies in post-natal skeletal muscle. Cell Tissue Res 306:129-141 (Pubitemid 32905605)
64. White JD, Davies M, McGeachie J, Grounds MD (2002) An evaluation of leukaemia inhibitory factor as a potential therapeutic agent in the treatment of muscle disease. Neuromuscul Disord 12:909-916 (Pubitemid 35408672)
65. Wolpe SD, Sherry B, Juers D, Davatelis G, Yurt RW, Cerami A (1989) Identification and characterization of macrophage inflammatory protein 2. Proc Nat Acad Sci 86:612 (Pubitemid 19037791)
66. Woods AM, McIlmoil CJ, Rankin EN, Packer AA, Stevens JC, Macievic JA, Brown AB, Porter JP, Judd AM (2008) Leukemia inhibitory factor protein and receptors are expressed in the bovine adrenal cortex and increase cortisol and decrease adrenal androgen release. Domest Anim Endocrinol 35:217-230
67. Zentella A, Massague J (1992) Transforming growth factor beta induces myoblast differentiation in the presence of mitogens. Proc Nat Acad Sci 89:5176