Cited by 1,105Muscle Physiology and DisordersWound Healing and TreatmentsCardiac Fibrosis and Remodeling

Regulatory interactions between muscle and the immune system during muscle regeneration

Open access
Tidball, James G., Villalta, S. Armando·2010·American Journal of Physiology-Regulatory, Integrative and Comparative Physiology

Abstract

Recent discoveries reveal complex interactions between skeletal muscle and the immune system that regulate muscle regeneration. In this review, we evaluate evidence that indicates that the response of myeloid cells to muscle injury promotes muscle regeneration and growth. Acute perturbations of muscle activate a sequence of interactions between muscle and inflammatory cells. The initial inflammatory response is a characteristic Th1 inflammatory response, first dominated by neutrophils and subsequently by CD68 + M1 macrophages. M1 macrophages can propagate the Th1 response by releasing proinflammatory cytokines and cause further tissue damage through the release of nitric oxide. Myeloid cells in the early Th1 response stimulate the proliferative phase of myogenesis through mechanisms mediated by TNF-α and IL-6; experimental prolongation of their presence is associated with delayed transition to the early differentiation stage of myogenesis. Subsequent invasion by CD163 + /CD206 + M2 macrophages attenuates M1 populations through the release of anti-inflammatory cytokines, including IL-10. M2 macrophages play a major role in promoting growth and regeneration; their absence greatly slows muscle growth following injury or modified use and inhibits muscle differentiation and regeneration. Chronic muscle injury leads to profiles of macrophage invasion and function that differ from acute injuries. For example, mdx muscular dystrophy yields invasion of muscle by M1 macrophages, but their early invasion is accompanied by a subpopulation of M2a macrophages. M2a macrophages are IL-4 receptor + /CD206 + cells that reduce cytotoxicity of M1 macrophages. Subsequent invasion of dystrophic muscle by M2c macrophages is associated with progression of the regenerative phase in pathophysiology. Together, these findings show that transitions in macrophage phenotype are an essential component of muscle regeneration in vivo following acute or chronic muscle damage.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1152/ajpregu.00735.2009

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 147 · Cited by 1,105

Research works printed but not linked: 128

  1. [1]Abood EA, Jones MM. Macrophages in developing mammalian skeletal muscle: evidence for muscle fibre death as a normal developmental event. Acta Anat (Basel) 140: 201–212, 1991 [DOI] [PubMed] [Google Scholar]
  2. [3]Backman E, Henriksson KG. Low-dose prednisolone treatment in Duchenne and Becker muscular dystrophy. Neuromusc Disord 5: 233–241, 1995 [DOI] [PubMed] [Google Scholar]
  3. [4]Bakkar N, Wang J, Ladner KJ, Wang H, Dahlman JM, Carathers M, Acharyya S, Rudnicki MA, Hollenbach AD, Guttridge DC. IKK/NF-κB regulates skeletal myogenesis via a signaling switch to inhibit differentiation and promote mitochondrial biogenesis. J Cell Biol 180: 787–802, 2008 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. [5]Bartoli C, Civatte M, Pellissier JF, Figarella-Branger D. CCR2A and CCR2B, the two isoforms of the monocyte chemoattractant protein-1 receptor are up-regulated and expressed by different cell subsets in idiopathic inflammatory myopathies. Acta Neuropathol (Berl) 102: 385–392, 2001 [DOI] [PubMed] [Google Scholar]
  5. [6]Biancheri R, Falace A, Tessa A, Pedemonte M, Scapolan S, Cassandrini D, Aiello C, Rossi A, Broda P, Zara F, Santorelli FM, Minetti C, Bruno C. POMT2 gene mutation in limb-girdle muscular dystrophy with inflammatory changes. Biochem Biophys Res Commun 363: 1033–1037, 2007 [DOI] [PubMed] [Google Scholar]
  6. [7]Bondesen BA, Mills ST, Kegley KM, Pavlath GK. The COX-2 pathway is essential during early stages of skeletal muscle regeneration. Am J Physiol Cell Physiol 287: C475–C483, 2004 [DOI] [PubMed] [Google Scholar]
  7. [8]Bondesen BA, Mills ST, Pavlath GK. COX-2 pathway regulates growth of atrophied muscle via multiple mechanisms. Am J Physiol Cell Physiol 290: C1651–C1659, 2006 [DOI] [PubMed] [Google Scholar]
  8. [9]Bonecchi R, Facchetti F, Dusi S, Luini W, Lissandrini D, Simmelink M, Locati M, Bernasconi S, Allavena P, Brandt E, Rossi F, Mantovani A, Sozzani S. Induction of functional IL-8 receptors by IL-4 and IL-13 in human monocytes. J Immunol 164: 3862–3869, 2000 [DOI] [PubMed] [Google Scholar]
  9. [10]Brickson S, Ji LL, Olabisi R, Schneider BSP, Best TM. M1/70 attenuates blood-borne neutrophil oxidants, activation, and myofiber damage following stretch injury. J Appl Physiol 95: 969–976, 2003 [DOI] [PubMed] [Google Scholar]
  10. [11]Cai B, Spencer MJ, Nakamura G, Tseng-Ong L, Tidball JG. Eosinophilia of dystrophin-deficient muscle is promoted by perforin-mediated cytotoxicity by T cell effectors. Am J Pathol 156: 1789–1796, 2000 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. [12]Cantini M, Carraro U. Macrophage-released factor stimulates selectively myogenic cells in primary muscle culture. J Neuropathol Exp Neurol 54: 121–128, 1995 [DOI] [PubMed] [Google Scholar]
  12. [13]Cantini M, Giurisato E, Radu C, Tiozzo S, Pampinella F, Senigaglia D, Zaniolo G, Mazzoleni Vittiello L. Macrophage-secreted myogenic factors: a promising tool for greatly enhancing the proliferative capacity of myoblasts in vitro and in vivo. Neurol Sci 23: 189–194, 2002 [DOI] [PubMed] [Google Scholar]
  13. [15]Collins RA, Grounds MD. The role of tumor necrosis factor-alpha (TNF-α) in skeletal muscle regeneration. Studies in TNF-α(−/−) and TNF-α(−/−)/LT-α(−/−) mice. J Histochem Cytochem 49: 989–1001, 2001 [DOI] [PubMed] [Google Scholar]
  14. [16]Contreras-Shannon V, Ochoa O, Reyes-Reyna SM, Sun D, Michalek JE, Kuziel WA, McManus LM, Shireman PK. Fat accumulation with altered inflammation and regeneration in skeletal muscle of CCR2−/− mice following ischemic injury. Am J Physiol Cell Physiol 292: C953–C967, 2007 [DOI] [PubMed] [Google Scholar]
  15. [17]Cornelison DD, Wold BJ. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191: 270–283, 1997 [DOI] [PubMed] [Google Scholar]
  16. [18]Cornelison DD, Olwin BB, Rudnicki MA, Wold BJ. MyoD(−/−) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev Biol 224: 122–137, 2000 [DOI] [PubMed] [Google Scholar]
  17. [19]Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83: 64–70, 2008 [DOI] [PubMed] [Google Scholar]
  18. [20]Dijkstra CD, Döpp EA, Joling P, Kraal G. The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54: 589–599, 1985 [PMC free article] [PubMed] [Google Scholar]
  19. [21]DiPasquale DM, Cheng M, Billich W, Huang SA, van Rooijen N, Hornberger TA, Koh TJ. Urokinase-type plasminogen activator and macrophages are required for skeletal muscle hypertrophy in mice. Am J Physiol Cell Physiol 293: C1278–C1285, 2007 [DOI] [PubMed] [Google Scholar]
  20. [22]Doroshenko T, Chaly Y, Savitskiy V, Maslakova O, Portyanko A, Gorudko I, Voitenok NN. Phagocytosing neutrophils down-regulate the expression of chemokine receptors CXCR1 and CXCR2. Blood 100: 2668–2671, 2002 [DOI] [PubMed] [Google Scholar]
  21. [24]Fadok VA, Bratton DL, Guthrie L, Henson PM. Differential effects of apoptotic versus lysed cells on macrophage production of cytokines: role of proteases. J Immunol 166: 6847–6854, 2001 [DOI] [PubMed] [Google Scholar]
  22. [25]Fleming TJ, Fleming ML, Malek TR. Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6–8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family. J Immunol 151: 2399–2408, 1993 [PubMed] [Google Scholar]
  23. [26]Frenette J, Cai B, Tidball JG. Complement activation promotes muscle inflammation during modified muscle use. Am J Pathol 156: 2103–2110, 2000 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. [27]Füchtbauer EM, Westphal H. MyoD and myogenin are coexpressed in regenerating skeletal muscle of the mouse. Dev Dyn 193: 34–39, 1992 [DOI] [PubMed] [Google Scholar]
  25. [28]Ghosh S, May MJ, Kopp EB. NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16: 225–260, 1998 [DOI] [PubMed] [Google Scholar]
  26. [29]Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ, Willoughby DA. Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med 5: 698–701, 1999 [DOI] [PubMed] [Google Scholar]
  27. [31]Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953–64, 2005 [DOI] [PubMed] [Google Scholar]
  28. [32]Gorospe JR, Tharp M, Demitsu T, Hoffman EP. Dystrophin-deficient myofibers are vulnerable to mast cell granule-induced necrosis. Neuromuscul Disord 4: 325–333, 1994 [DOI] [PubMed] [Google Scholar]
  29. [34]Gussoni E, Pavlath GK, Miller RG, Panzara MA, Powell M, Blau HM, Steinman L. Specific T cell receptor gene rearrangements at the site of muscle degeneration in Duchenne muscular dystrophy. J Immunol 153: 4798–4805, 1994 [PubMed] [Google Scholar]
  30. [35]Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS., Jr NF-κB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 19: 5785–5799, 1999 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. [36]Guttridge DC, Mayo MW, Madrid LV, Wang CY, Baldwin AS. NF-κB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 289: 2363–2366, 2000 [DOI] [PubMed] [Google Scholar]
  32. [37]Han J, Jiang Y, Li Z, Kravchenko VV, Ulevitch RJ. Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature 386: 296–299, 1997 [DOI] [PubMed] [Google Scholar]
  33. [38]Hestdal K, Ruscetti FW, Ihle JN, Jacobsen SEW, Dubois CM, Kopp WC, Longo DL, Keller JR. Characterization and regulation of RB6–8C5 antigen expression on murine bone marrow cells. J Immunol 147: 22–28, 1991 [PubMed] [Google Scholar]
  34. [39]Hinz M, Krappmann D, Eichten A, Heder A, Scheidereit C, Strauss M. NF-κB function in growth control: regulation of cyclin D1 expression and G0/G1-to-S-phase transition. Mol Cell Biol 19: 2690–2698, 1999 [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. [40]Hodgetts S, Radley H, Davies M, Grounds MD. Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking TNFα function with Etanercept in mdx mice. Neuromuscul Disord 16: 591–602, 2006 [DOI] [PubMed] [Google Scholar]
  36. [41]Holmes WE, Lee J, Kuang WJ, Rice GC, Wood WI. Structure and functional expression of a human interleukin-8 receptor. Science 253: 1278–1280, 1991 [DOI] [PubMed] [Google Scholar]
  37. [42]Horsley V, Jansen KM, Mills ST, Pavlath GK. IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 113: 483–94, 2003 [DOI] [PubMed] [Google Scholar]
  38. [43]Jutila MA, Kroese FG, Jutila KL, Stall AM, Fiering S, Herzenberg LA, Berg EL, Butcher EC. Ly-6C is a monocyte/macrophage and endothelial cell differentiation antigen regulated by interferon-γ. Eur J Immunol 18: 1819–1826, 1988 [DOI] [PubMed] [Google Scholar]
  39. [44]Kinali M, Mercuri E, Main M, Muntoni F, Dubowitz V. An effective, low-dosage, intermittent schedule of prednisolone in the long-term treatment of early cases of Duchenne dystrophy. Neuromuscul Disord 12Suppl 1: S169–S174, 2002 [DOI] [PubMed] [Google Scholar]
  40. [45]Krippendorf BB, Riley DA. Distinguishing unloading- versus reloading-induced changes in rat soleus muscle. Muscle Nerve 16: 99–108, 1993 [DOI] [PubMed] [Google Scholar]
  41. [46]Kristiansen M, Graversen JH, Jacobsen C, Sonne O, Hoffman HJ, Law SK, Moestrup SK. Identification of the haemoglobin scavenger receptor. Nature 409: 198–201, 2001 [DOI] [PubMed] [Google Scholar]
  42. [47]Lamperti C, Cagliani R, Ciscato P, Moroni I, Viri M, Romeo A, Fagiolari G, Prelle A, Comi GP, Bresolin N, Moggio M. Congenital muscular dystrophy with muscle inflammation α dystroglycan glycosylation defect and no mutation in FKRP gene. J Neurol Sci 243: 47–51, 2006 [DOI] [PubMed] [Google Scholar]
  43. [48]Langen RC, Schols AM, Kelders MC, Wouters EF, Janssen-Heininger YM. Inflammatory cytokines inhibit myogenic differentiation through activation of nuclear factor-κB. FASEB J 15: 1169–1180, 2001, 2001 [DOI] [PubMed] [Google Scholar]
  44. [50]Langen RC, Schols AM, Kelders MC, van der Velden JL, Wouters EF, Janssen-Heininger YM. Muscle wasting and impaired muscle regeneration in a murine model of chronic pulmonary inflammation. Am J Respir Cell Mol Biol 35: 689–696, 2006 [DOI] [PubMed] [Google Scholar]
  45. [51]Launay T, Armand AS, Charbonnier F, Mira JC, Donsez E, Gallien CL, Chanoine C. Expression and neural control of myogenic regulatory factor genes during regeneration of mouse soleus. J Histochem Cytochem 49: 887–899, 2001 [DOI] [PubMed] [Google Scholar]
  46. [52]Le Grand F, Rudnicki MA. Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 19: 628–633, 2007 [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. [53]Li YP, Schwartz RJ, Waddell ID, Holloway BR, Reid MB. Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-κB activation in response to tumor necrosis factor α. FASEB J 12: 871–880, 1998 [DOI] [PubMed] [Google Scholar]
  48. [55]Lieber RL, Schmitz MC, Mishra DK, Friden J. Contractile and cellular remodeling in rabbit skeletal muscle after cyclic eccentric contractions. J Appl Physiol 77: 1926–1934, 1994 [DOI] [PubMed] [Google Scholar]
  49. [56]Lim SK, Kim H H, Lim SK, bin Ali A, Lim YK, Wang Y, Chong SM, Costantini F, Baumman H. Increased susceptibility in Hp knockout mice during acute hemolysis. Blood 92: 1870–1877, 1998 [PubMed] [Google Scholar]
  50. [57]Linder E, Lehto VP, Stenman S. Activation of complement by cytoskeletal intermediate filaments. Nature 278: 176–178, 1979 [DOI] [PubMed] [Google Scholar]
  51. [58]Linehan SA. The mannose receptor is expressed by subsets of APC in non-lymphoid organs. BMC Immunol 6: 4, 2005 [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. [59]Lluis F, Perdiguero E, Nebreda AR, Munoz-Canoves P. Regulation of skeletal muscle gene expression by p38 MAP Kinases. Trends Cell Biol 16: 36–44, 2005 [DOI] [PubMed] [Google Scholar]
  53. [60]Lolmede K, Campana L, Vezzoli M, Bosurgi L, Tonlorenzi R, Clementi E, Bianchi ME, Cossu G, Manfredi AA, Brunelli S, Rovere-Querini P. Inflammatory and alternatively activated human macrophages attract vessel-associated stem cells, relying on separate HMGB1- and MMP-9-dependent pathways. J Leukoc Biol 85: 779–87, 2009 [DOI] [PubMed] [Google Scholar]
  54. [62]Massimino M, Rapizzi E, Cantini M, Libera L, Mazzoeni F, Arsian P, Carraro U. ED2+ macrophages increase selectively myoblast proliferation in muscle cultures. Biochem Biophys Res Commun 235: 754–759, 1997 [DOI] [PubMed] [Google Scholar]
  55. [63]McLennan IS. Resident macrophages (ED2- and ED3-positive) do not phagocytose degenerating rat skeletal muscle fibres. Cell Tissue Res 272: 193–196, 1993 [DOI] [PubMed] [Google Scholar]
  56. [64]McLennan IS. Degenerating and regenerating skeletal muscles contain several subpopulations of macrophages with distinct spatial and temporal distributions. J Anat 188: 17–28, 1996 [PMC free article] [PubMed] [Google Scholar]
  57. [65]McLoon LK, Nguyen LT, Wirtschafter J. Time course of the regenerative response in bupivacaine injured orbicularis oculi muscle. Cell Tissue Res 294: 439–47, 1998 [DOI] [PubMed] [Google Scholar]
  58. [66]McNally EM, Ly CT, Rosenmann H, Mitrani Rosenbaum S, Jiang W, Anderson LV, Soffer D, Argov Z. Splicing mutation in dysferlin produces limb-girdle muscular dystrophy with inflammation. Am J Med Genet 91: 305–312, 2000 [DOI] [PubMed] [Google Scholar]
  59. [67]Mendias CL, Tatsumi R, Allen RE. Role of cyclooxygenase-1 and -2 in satellite cell proliferation, differentiation, and fusion. Muscle Nerve 30: 497–500, 2004 [DOI] [PubMed] [Google Scholar]
  60. [68]Merchant SH, Gurule DM, Larson RS. Amelioration of ischemia-reperfusion injury with cyclic peptide blockade of ICAM-1. Am J Physiol Heart Circ Physiol 284: H1260–H1268, 2003 [DOI] [PubMed] [Google Scholar]
  61. [69]Merly F, Lescaudron L, Rouaud T, Crossin F, Gardahaut MF. Macrophages enhance muscle satellite cell proliferation and delay their differentiation. Muscle Nerve 22: 724–732, 1999 [DOI] [PubMed] [Google Scholar]
  62. [70]Mishra DK, Friden J, Schmitz M, Lieber RL. Anti-inflammatory medication after muscle injury. J Bone Joint Surg 77: 1410–1519, 1995 [DOI] [PubMed] [Google Scholar]
  63. [71]Moestrup SK, Moller HJ. CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann Med 36: 347–354, 2004 [DOI] [PubMed] [Google Scholar]
  64. [72]Molkentin JD, Black BL, Martin JF, Olson EN. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83: 1125–1136, 1995 [DOI] [PubMed] [Google Scholar]
  65. [74]Mourkioti F, Rosenthal N. NF-κB signaling in skeletal muscle: prospects for intervention in muscle diseases. J Mol Med 86: 747–759, 2008 [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. [75]Nedachi T, Fujita H, Kanzaki M. Contractile C2C12 myotube model for studying exercise-inducible responses in skeletal muscle. Am J Physiol Endocrinol Metab 295: E1191–E1204, 2008 [DOI] [PubMed] [Google Scholar]
  67. [76]Nedachi T, Hatakeyama H, Kono T, Sato M, Kanzaki M. Characterization of contraction-inducible CXC chemokines and their roles in C2C12 myocytes. Am J Physiol Endocrinol Metab 297: E866–E878, 2009 [DOI] [PubMed] [Google Scholar]
  68. [77]Nguyen HX, Tidball JG. Interactions between neutrophils and macrophages promote macrophage killing of muscle cells in vitro. J Physiol 547: 125–132, 2003 [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. [78]Nguyen HX, Tidball JG. Null mutation of gp91phox reduces muscle membrane lysis during muscle inflammation in mice. J Physiol 553: 833–841, 2003 [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. [79]Nguyen HX, Lusis AJ, Tidball JG. Null mutation of myeloperoxidase in mice prevents mechanical activation of neutrophil lysis of muscle cell membranes in vitro and in vivo. J Physiol 565: 403–413, 2005 [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. [80]Ochoa O, Sun D, Reyes-Reyna SM, Waite LL, Michalek JE, McManus LM, Shireman PK. Delayed angiogenesis and VEGF production in CCR2−/− mice during impaired skeletal muscle regeneration. Am J Physiol Regul Integr Comp Physiol 293: R651–R661, 2007 [DOI] [PubMed] [Google Scholar]
  72. [81]Otis JS, Burkholder TJ, Pavlath GK. Stretch-induced myoblast proliferation is dependent on the COX2 pathway. Exp Cell Res 310: 417–425, 2005 [DOI] [PubMed] [Google Scholar]
  73. [82]Ottnad E, Parthasarathy S, Sambrano GR, Ramprasad MP, Quehenberger O, Kondratenko N, Green S, Steinberg D. A macrophage receptor for oxidized low density lipoprotein distinct from the receptor for acetyl low-density lipoprotein: partial purification and role in recognition of oxidatively damaged cells. Proc Natl Acad Sci USA 92: 1391–1395, 1995 [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. [83]Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6: 422–428, 2000 [DOI] [PubMed] [Google Scholar]
  75. [84]Otterbein LE, Choi AM. Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 279: L1029–L1037, 2000 [DOI] [PubMed] [Google Scholar]
  76. [85]Pavlath GK, Dominov JA, Kegley KM, Miller JB. Regeneration of transgenic skeletal muscles with altered timing of expression of the basic helix-loop-helix muscle regulatory factor MRF4. Am J Pathol 162: 1685–1691, 2003 [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. [87]Rabinowitz SS, Gordon S. Macrosialin, a macrophage-restricted membrane sialoprotein differentially glycosylated in response to inflammatory stimuli. J Exp Med 174: 827–836, 1991 [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. [88]Raingeaud J, Gupta S, Rogers JS, Dickens M, Han J, Ulevitch RJ, 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 270: 7420–7426, 1995 [DOI] [PubMed] [Google Scholar]
  79. [89]Ramprasad MP, Fischer W, Witztum JL, Sambrano GR, Quehenberger O, Steinberg D. The 94- to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc Natl Acad Sci USA 92: 9580–9584, 1995 [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. [90]Reyes-Reyna SM, Krolick KA. Chemokine production by rat myocytes exposed to interferon-γ. Clin Immunol 94: 105–113, 2000 [DOI] [PubMed] [Google Scholar]
  81. [91]Rose JJ, Foley JF, Murphy PM, Venkatesan S. On the mechanism and significance of ligand-induced internalization of human neutrophil chemokine receptors CXCR1 and CXCR2. J Biol Chem 279: 24372–24386, 2004 [DOI] [PubMed] [Google Scholar]
  82. [92]Ruiz-Bonilla V, Perdiguero E, Gresh L, Serrano AL, Zamora M, Sousa-Victor P, Jardí M, Wagner EF, Muñoz-Cánoves P. Efficient adult skeletal muscle regeneration in mice deficient in p38β, p38γ and p38ζ MAP kinases. Cell Cycle 7: 2208–2214, 2008 [DOI] [PubMed] [Google Scholar]
  83. [93]Sadrzadeh SM, Graf E, Panter SS, Hallaway PE, Eaton Hemoglobin JW. A biologic Fenton reagent. J Biol Chem 259: 14354–14356, 1984 [PubMed] [Google Scholar]
  84. [94]Sampaolesi M, Blot S, D'Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthélémy I, Perani L, Mantero S, Guttinger M, Pansarasa O, Rinaldi C, Cusella De Angelis MG, Torrente Y, Bordignon C, Bottinelli R, Cossu G. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444: 574–579, 2006 [DOI] [PubMed] [Google Scholar]
  85. [95]Schaer DJ, Boretti FS, Hongegger A, Poehler D, Linnscheid P, Staege H, Muller C, Schoedon G, Schaffner A. Molecular cloning and characterization of the mouse CD163 homologue, a highly glucocorticoid-inducible member of the scavenger receptor cysteine-rich family. Immunogenetics 53: 170–177, 2001 [DOI] [PubMed] [Google Scholar]
  86. [96]Schutzle UB, Wakelam MJ, Pette D. Prostaglandins and cyclic AMP stimulate creatine kinase synthesis but not fusion in cultured embryonic chick muscle cells. Biochim Biophys Acta 805: 204–210, 1984 [DOI] [PubMed] [Google Scholar]
  87. [97]Schwab N, Waschbisch A, Wrobel B, Lochmüller H, Sommer C, Wiendl H. Human myoblasts modulate the function of antigen-presenting cells. J Neuroimmunol 200: 62–70, 2008 [DOI] [PubMed] [Google Scholar]
  88. [98]Selva-O'Callaghan A, Labrador-Horrillo M, Gallardo E, Herruzo A, Grau-Junyent JM, Vilardell-Tarres M. Muscle inflammation, autoimmune Addison's disease and sarcoidosis in a patient with dysferlin deficiency. Neuromuscul Disord 16: 208–209, 2006 [DOI] [PubMed] [Google Scholar]
  89. [100]Shen W, Li Y, Tang Y, Cummins J, Huard J. NS-398, a cyclooxygenase-2-specific inhibitor, delays skeletal muscle healing by decreasing regeneration and promoting fibrosis. Am J Pathol 167: 1105–1117, 2005 [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. [101]Shepherd VL, Hoidal JR. Clearance of neutrophil-derived myeloperoxidase by the macrophage mannose receptor. Am J Respir Cell Mol Biol 2: 335–340, 1990 [DOI] [PubMed] [Google Scholar]
  91. [102]Shireman PK, Contreras-Shannon V, Ochoa O, Karia BP, Michalek JE, McManus LM. MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration. J Leukoc Biol 81: 775–785, 2007 [DOI] [PubMed] [Google Scholar]
  92. [103]Shortman K, Naik SH. Steady-state and inflammatory dendritic cell development. Nat Rev Immunol 7: 19–30, 2007 [DOI] [PubMed] [Google Scholar]
  93. [104]Smith RH, Palmer RM, Reeds PJ. Protein synthesis in isolated rabbit forelimb muscles. The possible role of metabolites of arachidonic acid in the response to intermittent stretching. Biochem J 214: 153–161, 1983 [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. [105]Smith J, Grisham M, Granger N, Korthuis R. Free radical defense mechanisms and neutrophil infiltration in postischemic skeletal muscle. Am J Physiol Heart Circ Physiol 256: H789–H793, 1989 [DOI] [PubMed] [Google Scholar]
  95. [106]Spencer MJ, Walsh CM, Dorshkind KA, Rodriguez EM, Tidball JG. Myonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity. J Clin Invest 99: 2745–2751, 1997 [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. [107]Spencer MJ, Montecino-Rodriguez E, Dorshkind K, Tidball JG. Helper (CD4+) and cytotoxic (CD8+) T cells promote the pathology of dystrophin-deficient muscle. Clin Immunol 98: 235–243, 2001 [DOI] [PubMed] [Google Scholar]
  97. [108]Srinivasan M, Frauwirth KA. Peripheral tolerance in CD8+ T cells. Cytokine 46: 147–159, 2009 [DOI] [PubMed] [Google Scholar]
  98. [110]Suelves M, Lluís F, Ruiz V, Nebreda AR, Muñoz-Cánoves P. Phosphorylation of MRF4 transactivation domain by p38 mediates repression of specific myogenic genes. EMBO J 23: 365–375, 2004 [DOI] [PMC free article] [PubMed] [Google Scholar]
  99. [111]Summan M, Warren GL, Mercer RR, Chapman R, Hulderman T, Van Rooijen N, Simeonova PP. Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study. Am J Physiol Regul Integr Comp Physiol 290: R1488–R1495, 2006 [DOI] [PubMed] [Google Scholar]
  100. [112]Sun D, Martinez CO, Ochoa O, Ruiz-Willhite L, Bonilla JR, Centonze VE, Waite LL, Michalek JE, McManus LM, Shireman PK. Bone marrow-derived cell regulation of skeletal muscle regeneration. FASEB J 23: 382–395, 2009 [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. [113]Suzuki K, Totsuka M, Nakaji S, Yamada M, Kudoh S, Liu Q, Sugawara K, Yamaya K, Sato K. Endurance exercise causes interaction among stress hormones, cytokines, neutrophil dynamics, and muscle damage. J Appl Physiol 87: 1360–1367, 1999 [DOI] [PubMed] [Google Scholar]
  102. [114]Teixeira CFP, Zamuner SR, Zuliani JP, Fernandes CM, Cruz-Hofling MA, Fernandes I, Chaves F, Gutierrez JM. Neutrophils do not contribute to local tissue damage, but play a key role in skeletal muscle regeneration, in mice injected with Bothrops asper snake venom. Muscle Nerve 28: 449–459, 2003 [DOI] [PubMed] [Google Scholar]
  103. [115]Theilgaard-Mönch K, Porse BT, Borregaard N. Systems biology of neutrophil differentiation and immune response. Curr Opin Immunol 18: 54–60, 2006 [DOI] [PubMed] [Google Scholar]
  104. [116]Tidball JG, St. Pierre BA. Apoptosis of macrophages during the resolution of muscle inflammation. J Leukoc Biol 59: 380–388, 1996 [DOI] [PubMed] [Google Scholar]
  105. [117]Tidball JG, Berchenko E, Frenette J. Macrophage invasion does not contribute to muscle membrane injury during inflammation. J Leukoc Biol 65: 492–498, 1999 [PubMed] [Google Scholar]
  106. [118]Tidball JG, Wehling-Henricks M. Evolving therapeutic strategies for Duchenne muscular dystrophy: targeting downstream events. Pediatr Res 56: 831–841, 2004 [DOI] [PubMed] [Google Scholar]
  107. [119]Tidball JG, Wehling-Henricks M. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J Physiol 578: 327–336, 2007 [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. [120]Torrente Y, El Fahime E, Caron NJ, Del Bo R, Belicchi M, Pisati F, Tremblay JP, Bresolin N. Tumor necrosis factor-alpha (TNF-α) stimulates chemotactic response in mouse myogenic cells. Cell Transplant 12: 91–100, 2003 [DOI] [PubMed] [Google Scholar]
  109. [121]Trappe TA, Fluckey JD, White F, Lambert CP, Evans WJ. Skeletal muscle PGF2α and PGE2 in response to eccentric resistance exercise: influence of ibuprofen acetaminophen. J Clin Endocrinol Metab 86: 5067–5070, 2001 [DOI] [PubMed] [Google Scholar]
  110. [122]Van Velzen AG, Da Silva RP, Gordon S, Van Berkel TJ. Characterization of a receptor for oxidized low-density lipoproteins on rat Kupffer cells: similarity to macrosialin. Biochem J 322: 411–415, 1997 [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. [124]Wang H, Hertlein E, Bakkar N, Sun H, Acharyya S, Wang J, Carathers M, Davuluri R, Guttridge DC. NF-κB regulation of YY1 inhibits skeletal myogenesis through transcriptional silencing of myofibrillar genes. Mol Cell Biol 27: 4374–4387, 2007 [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. [126]Warren GL, Hulderman T, Jensen N, McKinstry M, Mishra M, Luster MI, Simeonova PP. Physiological role of tumor necrosis factor α in traumatic muscle injury. FASEB J 16: 1630–1632, 2002 [DOI] [PubMed] [Google Scholar]
  113. [127]Warren GL, O'Farrell L, Summan M, Hulderman T, Mishra D, Luster MI, Kuziel WA, Simeonova PP. Role of CC chemokines in skeletal muscle functional restoration after injury. Am J Physiol Cell Physiol 286: C1031–C1036, 2004 [DOI] [PubMed] [Google Scholar]
  114. [128]Warren GL, Hulderman T, Mishra D, Gao X, Millecchia L, O'Farrell L, Kuziel WA, Simeonova PP. Chemokine receptor CCR2 involvement in skeletal muscle regeneration. FASEB J 19: 413–415, 2005 [DOI] [PubMed] [Google Scholar]
  115. [129]Wehling M, Spencer MJ, Tidball JG. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 155: 123–131, 2001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. [130]Wehling-Henricks M, Lee JJ, Tidball JG. Prednisolone decreases cellular adhesion molecules required for inflammatory cell infiltration in dystrophin-deficient skeletal muscle. Neuromuscul Disord 14: 483–490, 2004 [DOI] [PubMed] [Google Scholar]
  117. [131]Wehling-Henricks M, Sokolow S, Lee JJ, Myung KH, Villalta SA, Tidball JG. Major basic protein-1 promotes fibrosis of dystrophic muscle and attenuates the cellular immune response in muscular dystrophy. Hum Mol Genet 17: 2280–2292, 2008 [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. [132]Westerheide SD, Mayo MW, Anest V, Hanson JL, Baldwin AS., Jr The putative oncoprotein Bcl-3 induces cyclin D1 to stimulate G(1) transition. Mol Cell Biol 21: 8428–8436, 2001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. [133]Wu Z, Woodring PJ, Bhakta KS, Tamura K, Wen F, Feramisco JR, Karin M, Wang JY, Puri PL. p38 and extracellular signal-regulated kinases regulate the myogenic program at multiple steps. Mol Cell Biol 20: 3951–3964, 2000 [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. [134]Yablonka-Reuveni Z, Rivera AJ. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 164: 588–603, 1994 [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. [135]Yahiaoui L, Gvozdic D, Danialou G, Mack M, Petrof BJ. CC family chemokines directly regulate myoblast responses to skeletal muscle injury. J Physiol 586: 3991–4004, 2008 [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. [136]Yan Z, Choi S, Liu X, Zhang M, Schageman JJ, Lee SY, Hart R, Lin L, Thurmond FA, Williams RS. Highly coordinated gene regulation in mouse skeletal muscle regeneration. J Biol Chem 278: 8826–8836, 2003 [DOI] [PubMed] [Google Scholar]
  123. [137]Zádor E, Mendler L, Takács V, de Bleecker J, Wuytack F. Regenerating soleus and extensor digitorum longus muscles of the rat show elevated levels of TNF-α and its receptors, TNFR-60 and TNFR-80. Muscle Nerve 24: 1058–1067, 2001 [DOI] [PubMed] [Google Scholar]
  124. [138]Zerria K, Jerbi E, Hammami S, Maaroufi A, Boubaker S, Xiong JP, Arnaout MA, Fathallah DM. Recombinant integrin CD11b A-domain blocks polymorphonuclear cells recruitment and protects against skeletal muscle inflammatory injury in the rat. Immunology 1194: 431–440, 2006 [DOI] [PMC free article] [PubMed] [Google Scholar]
  125. [139]Zetser A, Gredinger E, Bengal E. p38 mitogen-activated protein kinase pathway promotes skeletal muscle differentiation. Participation of the Mef2c transcription factor. J Biol Chem 274: 5193–5200, 1999 [DOI] [PubMed] [Google Scholar]
  126. [140]Zouaoui Boudjeltia K, Moguilevsky N, Legssyer I, Babar S, Guillaume M, Delree P, Vanhaeverbeek M, Brohee D, Ducobu J, Remacle C. Oxidation of low density lipoproteins by myeloperoxidase at the surface of endothelial cells: an additional mechanism to subendothelium oxidation. Biochem Biophys Res Commun 3252: 434–438, 2004 [DOI] [PubMed] [Google Scholar]
  127. [141]Zalin RJ. Prostaglandins and myoblast fusion. Dev Biol 59: 241–248, 1977 [DOI] [PubMed] [Google Scholar]
  128. [142]Zalin RJ. The role of hormones and prostanoids in the in vitro proliferation and differentiation of human myoblasts. Exp Cell Res 172: 265–281, 1987 [DOI] [PubMed] [Google Scholar]

Authors
Tidball, J. G., & Villalta, S. A.
Affiliations
  • University of California, Los Angeles (US)
  • Molecular, Cellular and Integrative Physiology Program and
Corresponding author
Tidball, James G.
Venue
American Journal of Physiology-Regulatory, Integrative and Comparative Physiology
Published
2010-05
Volume
298
Issue
5
Pages
R1173-R1187
ISSN
  • 0363-6119 (ISSN-L)
  • 1522-1490
OpenAlex
W2112039060
Cited by
1,105
References
147
Citations by year
2026: 47 · 2025: 57 · 2024: 55 · 2023: 56 · 2022: 74 · 2021: 86 · 2020: 76 · 2019: 74 · 2018: 78 · 2017: 78 · 2016: 90 · 2015: 80 · 2014: 83 · 2013: 66 · 2012: 53
FWCI
4.69
Type
journal article
Language
en
Open access
Locations
  • American Journal of Physiology-Regulatory, Integrative and Comparative Physiology (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institute on Aging (R01 AR/AG054451)
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR047855, R01AR047721, F31AR054724)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
  • Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
Keywords
muscle regeneration, muscle damage, myeloid cells, macrophage polarization, M1 macrophages, M2 macrophages, neutrophils, myogenesis, TNF-α, interleukin-6, IL-10, nitric oxide, muscle growth
MeSH terms
Animals, Humans, Immune System, Macrophages, Muscular Dystrophies, Neutrophils, Regeneration, Muscle, Skeletal

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review