Abstract
Cytokines are a diverse family of intercellular signaling proteins that influence the movement, proliferation, differentiation, metabolism and membrane processes of target cells. Synthesis and release of cytokines from leukocytes in response to microbial stimuli are well known. This review, however, will present evidence that non-infectious stimuli can induce cytokine secretion from leukocytes and other cells (including muscle cells) following myocellular injury. The biological actions and potential adaptive values of these cytokines through the course of muscle necrosis and regeneration will be described.
Similar content being viewed by others
References
Thomson A. ed.: The Cytokine Handbook. Second edn. 1994, Academic Press, San Diego
Second International Lymphokine Workshop. Revised nomenclature for antigen-nonspecific T cell proliferation and helper factors. J Immunol 123: 2928–2929, 1979
Snell ES, Atkins E: The presence of endogenous pyrogen in normal rabbit tissues. J Exp Med 121: 1019–1038, 1965
Taniguchi T: Cytokine signalling through nonreceptor protein tyrosine kineses. Science 268: 251–255, 1995
Gearing DP, Comeau MR, Friend DJ, Gimpel SD, Thut CJ, McGourty J, Brasher KK, King JA, Gillis S, Mosley B, Ziegler SF, Cosman D: The IL-6 signal transducer, gp130: An oncostatin M receptor and affinity converter for the LIF receptor. Science 255: 1434–1437, 1992
Dinarello CA: Biologic basis for interleukin-1 in disease. Blood 87: 2095–2147, 1996
Novick D, Schulman LM, Chen L, Revel M: Enhancement of interleukin 6 cytostatic effect on human breast carcinoma cells by soluble IL-6 receptor from urine and reversion by monoclonal antibody. Cytokine 4: 6–11, 1992
Stahl N, Farruggella TJ, Boulton TG, Zhong Z, Darnell JJE, Yancopoulos GD: Choice of STATS and other substrates specified by modular tyrosinebased motifs in cytokine receptors. Science 267: 1349–1353, 1995
Florini JR, Ewton DZ, Magri KA: Hormones, growth factors, and myogenic differentiation. Ann Rev Physiol 53: 201–216, 1991
Sara VR, Hall K: Insulin-like growth factors and their binding proteins. Physiol Rev 70: 591–614, 1990
Friden J, Sfakianos PN, Hargens AR: Muscle soreness and intracellular fluid pressure: Comparison between eccentric and concentric load. J Appl Physiol 61: 2175–2179, 1986
Cannon JG, Orencole SF, Fielding RA, Meydani M, Meydani SN, Fiatarone MA, Blumberg JB, Evans WJ: The acute phase response in exercise: Interaction of age and vitamin E on neutrophils and muscle enzyme release. Am J Physiol 259: 1214–1219, 1990
Schwane JA, Armstrong RB: Effect of training on skeletal muscle injury from downhill running in rats. J Appl Physiol 55: 969–975, 1983
Newham DJ, Mills KR, Quigley BM, Edwards RHT: Pain and fatigue after concentric and eccentric muscle contractions. Clin Sci 64: 55–62, 1983
Zerba E, Komoroski TE, Faulkner JA: Free radical injury to skeletal muscles of young, adult and old mice. Am J Physiol 258: C429–C435, 1990
McCully KK, Faulkner JA: Characteristics of lengthening contractions associated with injury to skeletal muscle fibers. J Appl Physiol 61: 293–299, 1986
Warren GL, Hayes DA, Lowe DA, Williams JH, Armstrong RB: Eccentric contraction-induced injury in normal and hindlimb-suspended mouse soleus and EDL muscles. J Appl Physiol 77: 1421–1430, 1994
Ashton-Miller JA, He Y, Kadhiresan VA, McCubbrey DA, Faulkner JA: An apparatus to measure in vivo biomechanical behavior of dorsi-and plantar-flexors of mouse ankle. J Appl Physiol 72: 1205–1211, 1992
Walker BAM, Fantone JC: The inflammatory response. In: LH Sigal, Y Ron, (eds). Immunology and inflammation: Basic Mechanisms and Clinical Consequences, McGraw-Hill, New York, 1994, pp 359–388
Bevilacqua MP, Pober JS, Mendrick DL, Cotran RS, Gimbrone MA Jr: Identification of an inducible endothelial-leukocyte adhesion molecule. Proc Natl Acad Sci USA 84: 9238–9242, 1987
Gotsch U, Jager U, Dominis M, Vestweber D: Expression of P-selectin on endothelial cells is upregulated by LPS and TNF-alpha in vivo. Cell Adhes Commun 2: 7–14, 1994
Pober JS, Gimbrone MA Jr, Lapierre LA, Mendrick DL, Fiers W, Rothlein R, Springer TA: Overlapping patterns of activation of human endothelial cells by interleukin 1, tumor necrosis factor, and immune interferon. J Immunol 137: 1893–96, 1986
Pober JS, Bevilacqua MP, Mendrick DL, Lapierre LA, Fiers W, Gimbrone MA Jr: Two distinct monokines, interleukin 1 and tumor necrosis factor, each independently induce biosynthesis and transient expression of the same antigen on the surface of cultured human vascular endothelial cells. J Immunol 136: 1680–1687, 1986
Weller A, Isenmann S, Vestweber D: Cloning of the mouse endothelial selecting. Expression of both E-and P-selectin is inducible by tumor necrosis factor alpha. J Biol Chem 267: 15176–15183, 1992
Gath I, Closs EI, Gödtel-Armburst U, Schmitt S, Nakane M, Wessler I, Förestermann U: Inducible NO synthase II and neuronal NO synthase I are constitutively expressed in different structures of guinea pig skeletal muscle: Implications for contractile function. FASEB J 10: 1614–1620, 1996
Zsebo KM, Yuschenkoff VN, Schiffer S, Chang D, McCall E, Dinarello CA, Brown MA, Altrock B, Bagby GV Jr: Vascular endothelial cells and granulopoiesis: Interleukin-1 stimulates release of G-CSF and GM-CSF. Blood 71: 99–103, 1988
Kurt-Jones EA, Fiers W, Pober JS: Membrane interleukin 1 induction on human endothelial cells and dermal fibroblasts. J Immunol 139: 2317–2324, 1987
Warner SJ, Auger KR, Libby P: Interleukin 1 induces interleukin 1. II. Recombinant human interleukin 1 induces interleukin 1 production by adult human vascular endothelial cells. J Immunol 139: 1911–1917, 1987
Jirik FR, Podor TJ, Hirano T, Kishimoto T, Loskutoff DJ, Carson DA, Lotz M: Bacterial lipopolysaccharide and inflammatory mediators augment IL-6 secretion by human endothelial cells. J Immunol 142: 144–147, 1989
Gimbrone MA Jr, Obin MS, Brock AF, Luis EA, Hass PE, Hebert CA, Yip YK, Leung DW, Lowe DG, Kohr W, Darbonne WC, Bechtol LB, Baker JB: Endothelial interleukin-8: A novel inhibitor of leukocyteendothelial interactions. Science 246: 1601–1603, 1989
MacIntyre DL, Reid WD, Lyster DM, Szasz IJ, McKenzie DC: Presence of WBC, decreased strength, and delayed soreness in muscle after eccentric exercise. J Appl Physiol 80: 1006–1013, 1996
Kuipers H, Drukker J, Frederik PM, Geurten P, Kranenburg G: Muscle degeneration after exercise in rats. Int J Sports Med 4: 45–51, 1983
Lowe DA, Warren GL, Ingalls CP, Boorstein DB, Armstrong RB: Muscle function and protein metabolism after initiation of eccentric contractioninduced injury. J Appl Physiol 79: 1260–1270, 1995
Fielding RA, Manfredi TJ, Ding W, Fiatarone MA, Evans WJ, Cannon JG: Acute phase response in exercise III. Neutrophil and IL-1β accumulation in skeletal muscle. Am J Physiol 265: R166–R172, 1993
Hikida RS, Staron RS, Hagerman FC, Sherman WM, Costill DL: Muscle fiber necrosis associated with human marathon runners. J Neurol Sci 59: 185–203, 1983
Altstaedt J, Kirchner H, Rink L: Cytokine production of neutrophils is limited to interleukin-8. Immunology 89: 563–568, 1996
Bazzoni F, Cassatella MA, Rossi F, Ceska M, Dewald B, Baggiolini M: Phagocytosing neutrophils produce and release high amounts of the neutrophil-activating peptide 1/interleukin 8. J Exp Med 173: 771–774, 1991
Tiku K, Tiku ML, Skosey J: Interleukin 1 production by human polymorphonuclear neutrophils. J Immunol 136: 3677–3685, 1986
Fava RA, Olsen NJ, Postlethwaite AE, Broadley KN, Davidson JM, Nanney LB, Lucas C, Townes AS: Transforming growth factor β1 (TGF-β1) induced neutrophil recruitment to synovial tissues: Implications for TGF-β-driven synovial inflammation and hyperplasia. J Exp Med 173: 1121–1132, 1991
Dubravec DB, Spriggs DR, Mannick JA, Rodrick ML: Circulating human peripheral blood granulocytes synthesize and secrete tumor necrosis factor α. Proc Natl Acad Sci USA 87: 6758–6761, 1990
Springer T, Galfré G, Secher DS, Milstein C: Mac-1: A macrophage differentiation antigen identified by monoclonal antibody. Eur J Immunol 9: 301–306, 1979
Leenen PJM, Melis M, Kraal G, Hoogeveen AT, Van Ewijk W: The monoclonal antibody ER-BMDM1 recognizes a macrophage and dendritic cell differentiation antigen with aminopeptidase activity. Eur J Immunol 22: 1567–1572, 1992
Armstrong RB, Ogilvie RW, Schwane JA: Eccentric exercise-induced injury to rat skeletal muscle. J Appl Physiol 54: 80–93, 1983
McCully KK, Faulkner JA: Injury to skeletal muscle fibers of mice following lengthening contractions. J Appl Physiol 59: 119–126, 1985
St. Pierre BA, Tidball JG: Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension. J App Physiol 77: 290–297, 1994
Jones DA, Newham DJ, Round JM, Tolfree SEJ: Experimental human muscle damage: Morphological changes in relation to other indices of damage. J Physiol (London) 375: 435–448, 1986
Round JM, Jones DA, Cambridge G: Cellular infiltrates in human skeletal muscle: Exercise induced damage as a model for inflammatory muscle disease? J Neurol Sci 82: 1–11, 1987
March CJ, Mosley B, Larsen A, Cerretti DP, Braedt G, Price V, Gillis S, Henney CS, Kronheim SR, Grabstein K, Conlon PJ, Hopp TJ, Cosman D: Cloning, sequence and expression of two distinct human interleukin-1 complementary DNAs. Nature 315: 641–647, 1985
Nathan CF: Secretory products of macrophages. J Clin Invest. 79: 319–326, 1987
Baird A, Mormède P, Böhlen P: Immunoreactive fibroblast growth factor in cells of peritoneal exudate suggests its identity with macrophage-derived growth factor. Biochem Biophys Res Comm 126: 358–364, 1985
Arkins S, Rebeiz N, Biragyn A, Reese DL, Kelley KW: Murine macrophages express abundant insulin-like growth factor-I class I Ea and Eb transcripts. Endocrinology 133: 2334–2343, 1993
Arkins S, Rebeiz N, Brunke-Reese DL, Minshall C, Kelley KW: The colony-stimulating factors induce expression of insulin-like growth factor-I messenger ribonucleic acid during hematopoiesis. Endocrinology 136: 1153–1160, 1995
Horii Y, Muraguchi A, Suematsu S, Matsuda T, Yoshizaki K, Hirano T, Kishimoto T: Regulation of BSF-2/IL-6 production by human mononuclear cells: Macrophage-dependent synthesis of BSF2/IL-6 by T cells. J Immunol 141: 1529–1535, 1988
Grabstein KH, Eisenman J, Shanebeck K, Rauch C, Srinivasan S, Fung V, Beers C, Richardson J, Schoenborn MA, Ahdieh M, Johnson L, Alderson MR, Watson JD, Anderson DM, Giri JM: Cloning of a T cell growth factor that interacts with the β?chain of the interleukin-2 receptor. Science 264: 965–968, 1994
Doherty TM, Seder RA, Sher A: Induction and regulation of IL-15 expression in murine macrophages. J Immunol 156: 735–741, 1996
Shimokado K, Raines EW, Madtes DK, Barrett TB, Benditt EP, Ross R: A significant part of macrophage-derived growth factor consists of at least two forms of PDGF. Cell 43: 277–286, 1985
Assoian RK, Sporn MB: Type β ?transforming growth factor in human platelets: Release during platelet degranulation and action on vascular smooth muscle cells. J Cell Biol 102: 1217–1223, 1986
Kovacs EJ, DiPietro LA: Fibrogenic cytokines and connective tissue production. FASEB J 8: 854–861, 1994
Postlethwaite AE, Kang AH: Fibroblasts and matrix proteins. In: JI Gallin, IM Goldstein, R Snyderman (eds). Inflammation: Basic Principles and Clinical Correlates. Raven Press, New York, 1992, pp 747–773
Walther Z, May LT, Sehgal PB: Transcriptional regulation of the interferon-beta 2/B cell differentiation factor BSF-2/hepatocytestimulating factor gene in human fibroblasts by other cytokines. J Immunol 140: 974–977, 1988
Le J, Weinstein D, Gubler U, Vilcek J: Induction of membrane-associated interleukin 1 by tumor necrosis factor in human fibroblasts. J Immunol 138: 2137–2142, 1987
Kaplanski G, Farnarier C, Kaplanski S, Porat R, Shapiro L, Bongrand P, Dinarello CA: Interleukin-1 induces interleukin-8 from endothelial cells by a juxtacrine mechanism. Blood 84: 4242–4248, 1994
Fibbe WE, Van Damme J, Billiau A, Duinkerken N, Lurvink E, Ralph P, Altrock BW, Kaushansky K, Willemze R, Falkenburg JH: Human fibroblasts produce granulocyte-CSF, macrophage-CSF, and granulocytemacrophage CSF following stimulation by interleukin-1 and poly(rI).-poly(rC). Blood 72: 860–866, 1988
Stauber WT, Fritz VK, Vogelbach SW, Dahlmann B: Characterization of muscles injured by forced lengthening. I. Cellular infiltrates. Med Sci Sports Exer 20: 345–353, 1988
Noble PW, Lake FR, Henson PM, Riches DWH: Hyaluronate activation of CD44 induces insulin-like growth factor-1 expression by a tumor necrosis factor-α-dependent mechanism in murine macrophages. J Clin Invest 91: 2368–2377, 1993
Webb DSA, Shimizu Y, Van Seventer GA, Shaw S, Gerrard TL: LFA-3, CD44, and CD45: Physiologic triggers of human monocyte TNF and IL-1 release. Science 249: 1295–1297, 1990
Cannon JG, Evans WJ, Hughes VA, Meredith CN, Dinarello CA: Physiological mechanisms contributing to increased interleukin-1 secretion. J Appl Physiol 61: 1869–1874, 1986
Cannon JG, Fiatarone MA, Meydani M, Scott L, Blumberg JB, Evans WJ: Aging and dietary modulation of elastase and interleukin-1β secretion. Am J Physiol 268: R208–R213, 1995
Cannon JG, Meydani SN, Fielding RA, Fiatarone MA, Meydani M, Farhangmehr M, Orencole SF, Blumberg JB, Evans WJ: The acute phase response in exercise. II. Associations between vitamin E, cytokines and muscle proteolysis. Am J Physiol 260: R1235–R1240, 1991
Sterpetti AV, Cucina A, Morena AR, DiDonna S, D'Angelo LS, Cavalarro A, Stipa S: Shear stress increases the release of interleukin-1 and interleukin-6 by aortic endothelial cells. Surgery 114: 911–914, 1993
Gundersen K, Maehlen J: Nerve-evoked electrical activity regulates molecules and cells with immunological function in rat muscle tissue. Eur J Neurosci 6: 1113–1118, 1994
Morrow NG, Kraus WE, Moore JW, Williams RS, Swain JL. Increased expression of fibroblast growth factors in a rabbit skeletal muscle model of exercise conditioning. J Clin Invest 85: 1816–1820, 1990
Clarke MSF, Feeback DL: Mechanical load induces sarcoplasmic wounding and FGF release in differentiated human skeletal muscle cultures. FASEB J 10: 502–509, 1996
Yamada S, Buffinger N, DiMario J, Strohman RC: Fibroblast growth factor is stored in fiber extracellular matrix and plays a role in regulating muscle hypertrophy. Med Sci Sports Exer 21: S173–S180, 1989
McNeil PL, Khakee R: Disruptions of muscle fiber plasma membranes: Role in exercise-induced damage. Am J Path 140: 1097–1109, 1992
Fischer JE, Hasselgren P-O: Cytokines and glucocorticoids in the regulation of the hepato-skeletal muscle axis in sepsis. Am J Surg 161: 266–271, 1991
Clowes GHA, George BC, Villee CA, Saravis CA: Muscle proteolysis induced by a circulating peptide in patients with sepsis or trauma. N Engl J Med 308: 545–552, 1983
Cannon JG: Cytokines in muscle homeostasis and disease. In: JJ Oppenheim, JL Rossio, AJH Gearing (eds). Clinical Applications of Cytokines. Oxford University Press, New York, pp 329–336
Mealy K, Lanschot JJBv, Robinson BG, Pounds J, Wilmore DW: Are the catabolic effects of tumor necrosis factor mediated by glucocorticoids? Arch Surg 125: 42–48, 1990
Zamir O, Hasselgren P-O, Von Allmen D, Fischer JE: In vivo administration of interleukin-1α ?induces muscle proteolysis in normal and adrenalectomized rats. Metabolism 42: 204–208, 1993
Zamir O, Hasselgren P-O, O'Brien W, Thompson RC, Fischer JE: Muscle protein breakdown during endotoxemia in rats and after treatment with interleukin-1 receptor antagonist (IL-1ra). Ann Surg 216: 381–387, 1992
Unpublished observations
Hershko A: Ubiquitin-mediated protein degradation. J Biol Chem 263: 15237–15240, 1988
Baracos VE, DeVivo C, Hoyle DH, Goldberg AL: Activation of the ATPubiquitin-proteasome pathway in skeletal muscle of cachectic rats bearing a hepatoma. Am J Physiol 268: E996–E1006, 1995
Garcia-Martinez C, Llovera M, Agell N, Lopez-Soriano FJ, Argiles JM: Ubiquitin gene expression in skeletal muscle is increased during sepsis: Involvement of TNFα? but not IL-1. Biochem Biophys Res Comm 217: 839–844, 1995
Garcia-Martinez C, Agell N, Llovera M, Lopez-Soriano FJ, Argiles JM: Tumour necrosis factor-α ?increases the ubiquitinization of rat skeletal muscle proteins. FEBS Lett 323: 211–214, 1993
Unpublished observations
Barbin G, Manthorpe M, Varon S: Purification of the chick eye ciliary neurotrophic factor. J Neurochem 43: 1468–1478, 1984
Sendtner M, Schmalbruch H, Stochli KA, Carroll P, Kreutzberg GW, Thoenen H: Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy. Nature 358: 502–504, 1992
Davis S, Aldrich TH, Ip NY, Stahl N, Sherer S, Farruggella T, DiStefano PS, Curtis R, Panayotatos N, Gascan H, Chevalier S, Yancopoulos GD: Released form of CNTF receptor α? component as a soluble mediator of CNTF responses. Science 259: 1736–1739, 1993
Helgren ME, Squinto SP, Davis HL, Parry DJ, Boulton TG, Heck CS, Zhu Y, Yancopoulos GD, Lindsay RM, DiStefano PS: Trophic effect of ciliary neurotrophic factor on denervated skeletal muscle. Cell 76: 493–504, 1994
Henderson JT, Seniuk NA, Richardson PM, Gauldie J, Roder JC: Systemic administration of ciliary neurotrophic factor induces cachexia in rodents. J Clin Invest 93: 2632–2638, 1994
Kalovidouris AE, Plotkin Z, Graesser D: Interferon-gamma inhibits proliferation, differentiation, and creatine kinase activity of cultured human muscle cells. II. A possible role in myositis. J Rheumatol 20: 1718–1723, 1993
Kelic S, Olsson T, Kristensson K: Interferon-gamma promotes proliferation of rat skeletal muscle cells in vitro and alters their AChR distribution. J Neurol Sci 114: 62–67, 1993
Beauchamp JR, Abraham DJ, Bou-Gharios G, Partridge TA, Olsen I: Expression and function of heterotypic adhesion molecules during differentiation of human skeletal muscle in culture. Am J Path 140: 387–401, 1992
Katz FRS: The termination of the afferent nerve fiber in the muscle spindle of the frog. Phil Trans Royal Soc Lond 243: 221–225, 1961
Mauro A: Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493–498, 1961
Schultz E, Jaryszak DL, Valiere CR: Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 8: 217–222, 1985
Darr KC, Schultz E: Exercise-induced satellite cell activation in growing and mature skeletal muscle. J Appl Physiol 63: 1816–1821, 1987
Schultz E, McCormick KM: Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol 123: 213–257, 1994
Bischoff R: The satellite cell and muscle regeneration. In: AG Engel, C Franzini-Armstrong (eds). Myology. McGraw-Hill, New York, 1994, pp 97–118
Snow MH: The effects of aging on satellite cells in skeletal muscle of mice and rats. Cell Tissue Res 185: 399–410, 1977
Schmalbruch H, Hellhammer U: The number of satellite cells in normal human muscle. Anat Rec 185: 279–288, 1976
Goldberg AL: Work-induced growth of skeletal muscle in normal and hypophysectomized rats. Am J Physiol 213: 1193–1198, 1967
Jin P, Sejersen T, Ringertz NR: Recombinant platelet-derived growth factor-BB stimulates growth and inhibits differentiation of rat L6 myoblasts. J Biol Chem 266: 1245–1249, 1991
Olsson T, Kelic S, Edlund C, Bakhiet M, Hojeberg B, Van der Meide PH, Ljungdahl A, Kristensson K: Neuronal interferon-ϒ? immunoreactive molecule: Bioactivities and purification. Eur J Immunol 24: 308–314, 1994
Allen RE, Boxhorn LK: Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol 138: 311–315, 1989
Wei Y, Miller SC, Tsuji Y, Torti SV, Torti FM: Interleukin-1 induces ferritin heavy chain in human muscle cells. Biochem Biophys Res Comm 169: 289–296, 1990
Hauschka SD: The embryonic origin of muscle. In: AG Engel and C Franzini-Armstrong (eds). Myology. McGraw-Hill, New York, 1994, pp 3–73
Massague J, Cheifetz S, Endo T, Nadal-Ginard B: Type β? transforming growth factor is an inhibitor of myogenic differentiation. Proc Natl Acad Sci USA 83: 8206–8210, 1986
Roberts AB, Sporn MB, Assoian RK, Smith JM, Roche NS, Wakefield LM, Heine UI, Liotta LA, Falanga V, Kehrl JH, Fauci AS: Transforming growth factor type γ: Rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc Natl Acad Sci USA 83: 4167–4171, 1986
Keller H, Cannon JG: Association of IGF-1 with myofiber regeneration in vivo. Physiologist 39: A93, 1996
DeVol DL, Rotwein P, Sadow JL, Novakofski J, Bechtel PJ: Activation of insulin-like growth factor gene expression during work-induced skeletal muscle growth. Am J Physiol 259: E89–E95, 1990
Fan J, Wojnar MM, Theodorakis M, Lang CH: Regulation of insulin-like growth factor (IGF)-I mRNA and peptide and IGF-binding proteins by interleukin-1. Am J Physiol 270: R621–629, 1996
Lang CH, Fan J, Cooney R, Vary TC: IL-1 receptor antagonist attenuates sepsis-induced alterations in the IGF system and protein synthesis. Am J Physiol 270: E430–E437, 1996
Quinn LS, Haugk KL, Grabstein KH: Interleukin-15: A novel anabolic cytokine for skeletal muscle. Endocrinology 136: 3669–3672, 1995
Auron PE, Webb AC, Rosenwasser LJ, Mucci SF, Rich AF, Wolff SM, Dinarello CA: Nucleotide sequence of human monocyte interleukin 1 precursor cDNA. Proc Natl Acad Sci USA 81: 7907–7910, 1984
Mannel DN, Moore RN, Mergenhagen SE: Macrophages as a source of tumoricidal activity (tumor-necrotizing factor). Infect Immun 30: 523–530, 1980
Alterio J, Courtois Y, Robelin J, Bechet D, Martelly I: Acidic and basic fibroblast growth factor mRNAs are expressed by skeletal muscle satellite cells. Biochem Biophys Res Comm 166: 1205–1212, 1990
Moore JW, Dionne C, Jaye M, Swain JL: The mRNAs encoding acidic FGF, basic FGF and FGF receptor are coordinately downregulated during myogenic differentiation. Development 111: 741–748, 1991
Tollefesn SE, Lajara R, McCusker RH, Clemmons DR, Rotwein P: Insulin-like growth factors (IGF) in muscle development. Expression of IGF-I, the IGF-I receptor, and an IGF binding protein during myoblast differentiation. J Biol Chem 264: 13810–13817, 1989
Tollefsen, SE, Sadow JL, Rotwein P: Coordinate expression of the insulinlike growth factor II and its receptor during muscle differentiation. Proc Natl Acad Sci USA 86: 1543–1547, 1989
Rosen KM, Wentworth BM, Rosenthal N, Villa-Komaroff L: Specific, temporally regulated expression of the insulin-like growth factor II gene during muscle cell differentiation. Endocrinology 133: 474–481, 1993
Bartoccioni E, Michaelis D, Hohlfeld R: Constitutive and cytokineinduced production of interleukin-6 by human myoblasts. Immunol Lett 42: 135–138, 1994
Lafyatis R, Lechleider R, Roberts AB, Sporn AB: Secretion and transcriptional regulation of transforming growth factor-beta 3 during myogenesis. Mol Cell Biol 11: 3795–3803, 1991
Jin P, Rahm M, Claesson-Welsh L, Heldin C-H, Sejersen T: Expression of PDGF A-chain and β-receptor genes during rat myoblast differentiation. J Cell Biol 110: 1665–1672, 1990
Anderson JE, Mitchell CM, McGeachie JK, Grounds MD: The time course of basic fibroblast growth factor expression in crush-injured skeletal muscles of SJL/J and BALB/c mice. Exp Cell Res 216: 325–334, 1995
Jennische E, Skottner A, Hansson HA: Satellite cells express the trophic factor IGF-I in regenerating skeletal muscle. Acta Physiol Scand 129: 9–15, 1987
Edwall D, Schalling M, Jennische E, Norstedt G: Induction of insulinlike growth factor I messenger ribonucleic acid during regeneration of rat skeletal muscle. Endocrinology 124: 820–825, 1989
Levinovitz A, Jennische E, Oldfors A, Edwall D, Norstedt G: Activation of insulin-like growth factor II expression during skeletal muscle regeneration in the rat: Correlation with myotube formation. Mol Endocrinol 6: 1227–1234, 1992
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cannon, J.G., St. Pierre, B.A. Cytokines in exertion-induced skeletal muscle injury. Mol Cell Biochem 179, 159–168 (1998). https://doi.org/10.1023/A:1006828425418
Issue Date:
DOI: https://doi.org/10.1023/A:1006828425418