Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype

Human Molecular Genetics

Volumn 20, Issue 4, 2011, Pages 790-805

  Villalta, S Armando ^a   Rinaldi, Chiara ^a   Deng, Bo ^a   Liu, Grace ^a   Fedor, Brian ^a   Tidball, James G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; MYOGENIN; TRANSCRIPTION FACTOR PAX7;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DISEASE SEVERITY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOUSE; MUSCLE CELL; MUSCLE STRENGTH; MUSCULAR DYSTROPHY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATION; SKELETAL MUSCLE SATELLITE CELL; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; INTERLEUKIN-10; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; PHAGOCYTOSIS; PHENOTYPE; RECEPTORS, INTERLEUKIN-10; REGENERATION;

MUS;

EID: 78751682676     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq523     Document Type: Article

References (67)

1. Hoffman, E.P., Brown, R.H. Jr. and Kunkel, L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell, 51, 919-928.
2. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A.M. and Sweeney, H.L. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl Acad. Sci. USA, 90, 3710-3714.
3. Tidball, J.G. and Wehling-Henricks, M. (2004) Evolving therapeutic strategies for Duchenne muscular dystrophy: targeting downstream events. Pediatr. Res., 56, 831-841.
4. Gorospe, J.R., Tharp, M., Demitsu, T. and Hoffman, E.P. (1994) Dystrophin-deficient myofibers are vulnerable to mast cell granule-induced necrosis. Neuromuscul. Disord., 4, 325-333.
5. Hodgetts, S., Radley, H., Davies, M. and Grounds, M.D. (2006) Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking TNFalpha function with Etanercept in mdx mice. Neuromuscul. Disord., 16, 591-602.
6. Wehling, M., Spencer, M.J. and Tidball, J.G. (2001) A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J. Cell Biol., 155, 123-131.
7. Wehling-Henricks, M., Sokolow, S., Lee, J.J., Myung, K.H., Villalta, S.A. and Tidball, J.G. (2008) Major basic protein-1 promotes fibrosis of dystrophic muscle and attenuates the cellular immune response in muscular dystrophy. Hum. Mol. Genet., 17, 2280-2292.
8. Spencer, M.J., Montecino-Rodriguez, E., Dorshkind, K. and Tidball, J.G. (2001) Helper (CD4(+)) and cytotoxic (CD8(+)) T cells promote the pathology of dystrophin-deficient muscle. Clin. Immunol., 98, 235-243.
9. Cai, B., Spencer, M.J., Nakamura, G., Tseng-Ong, L. and Tidball, J.G. (2000) Eosinophilia of dystrophin-deficient muscle is promoted by perforin-mediated cytotoxicity by T cell effectors. Am. J. Pathol., 156, 1789-1796.
10. Manzur, A.Y., Kuntzer, T., Pike, M. and Swan, A. (2008) Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane DB Syst. Rev., 1, CD003725.
11. Moxley, R.T. III, Ashwal, S., Pandya, S., Connolly, A., Florence, J., Mathews, K., Baumbach, L., McDonald, C., Sussman, M. and Wade, C. (2005) Practice parameter: corticosteroid treatment of Duchenne dystrophy: report of the Quality Standards Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society. Neurology, 64, 13-20.
12. Moore, K.W., de Waal Malefyt, R., Coffman, R.L. and O'Garra, A. (2001) Interleukin-10 and the interleukin-10 receptor. Ann. Rev. Immunol., 19, 683-765.
13. Fiorentino, D.F., Bond, M.W. and Mosmann, T.R. (1989) Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J. Exp. Med., 170, 2081-2095.
14. Fiorentino, D.F., Zlotnik, A., Mosmann, T.R., Howard, M. and O'Garra, A. (1991) IL-10 inhibits cytokine production by activated macrophages. J. Immunol., 147, 3815-3822.
15. Mosser, D.M. (2003) The many faces of macrophage activation. J. Leukoc. Biol., 73, 209-212.
16. Murray, P.J. (2006) Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol., 6, 379-386.
17. Mosser, D.M. and Zhang, X. (2008) Interleukin-10: new perspectives on an old cytokine. Immunol. Rev., 226, 205-218.
18. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A. and Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol., 25, 677-686.
19. Lang, R., Rutschman, R.L., Greaves, D.R. and Murray, P.J. (2002) Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing IL-10 under control of the human CD68 promoter. J. Immunol., 168, 3402-3411.
20. Schaer, D.J., Boretti, F.S., Hongegger, A., Poehler, D., Linnscheid, P., Staege, H., Muller, C., Schoedon, G. and Schaffner, A. (2001) 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.
21. Sulahian, T.H., Hogger, P., Wahner, A.E., Wardwell, K., Goulding, N.J., Sorg, C., Droste, A., Stehling, M., Wallace, P.K., Morganelli, P.M. et al. (2000) Human monocytes express CD163, which is upregulated by IL-10 and identical to p155. Cytokine, 12, 1312-1321.
22. Lang, R., Patel, D., Morris, J.J., Rutschman, R.L. and Murray, P.J. (2002) Shaping gene expression in activated and resting primary macrophages by IL-10. J. Immunol., 169, 2253-2263.
23. Martinez-Pomares, L., Reid, D.M., Brown, G.D., Taylor, P.R., Stillion, R.J., Linehan, S.A., Zamze, S., Gordon, S. and Wong, S.Y. (2003) Analysis of mannose receptor regulation by IL-4, IL-10, and proteolytic processing using novel monoclonal antibodies. J. Leukoc. Biol., 73, 604-613.
24. Villalta, S.A., Nguyen, H.X., Deng, B., Gotoh, T. and Tidball, J.G. (2009) Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum. Mol. Genet., 18, 482-496.
25. Massimino, M.L., Rapizzi, E., Cantini, M., Libera, L.D., Mazzoleni, F., Arslan, P. and Carraro, U. (1997) ED2+ macrophages increase selectively myoblast proliferation in muscle cultures. Biochem. Biophys. Res. Commun., 235, 754-759.
26. Strle, K., McCusker, R.H., Tran, L., King, A., Johnson, R.W., Freund, G.G., Dantzer, R. and Kelley, K.W. (2007) Novel activity of an anti-inflammatory cytokine: IL-10 prevents TNFalpha-induced resistance to IGF-I in myoblasts. J. Neuroimmunol., 188, 48-55.
27. Strle, K., McCusker, R.H., Johnson, R.W., Zunich, S.M., Dantzer, R. and Kelley, K.W. (2008) Prototypical anti-inflammatory cytokine IL-10 prevents loss of IGF-I-induced myogenin protein expression caused by IL-1beta. Am. J. Physiol. Endocrinol. Metab., 294, E709-718.
28. Stein, M., Keshav, S., Harris, N. and Gordon, S. (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med., 176, 287-292.
29. Horsley, V., Jansen, K.M., Mills, S.T. and Pavlath, G.K. (2003) IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell, 113, 483-494.
30. Chesrown, S.E., Monnier, J., Visner, G. and Nick, H.S. (1994) Regulation of inducible nitric oxide synthase mRNA levels by LPS, INF-gamma, TGF-beta, and IL-10 in murine macrophage cell lines and rat peritoneal macrophages. Biochem. Biophys. Res. Commun., 200, 126-134.
31. Arnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., Gherardi, R.K. and Chazaud, B. (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med., 204, 1057-1069.
32. Varin, A., Mukhopadhyay, S., Herbein, G. and Gordon, S. (2010) Alternative activation of macrophages by IL-4 impairs phagocytosis of pathogens but potentiates microbial-induced signalling and cytokine secretion. Blood, 115, 353-362.
33. Acharyya, S., Villalta, S.A., Bakkar, N., Bupha-Intr, T., Janssen, P.M., Carathers, M., Li, Z.W., Beg, A.A., Ghosh, S., Sahenk, Z. et al. (2007) Interplay of IKK/NF-kappaB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J. Clin. Invest., 117, 889-901.
34. Wehling-Henricks, M., Lee, J.J. and Tidball, J.G. (2004) Prednisolone decreases cellular adhesion molecules required for inflammatory cell infiltration in dystrophin-deficient skeletal muscle. Neuromuscul. Disord., 14, 483-490.
35. Li, H., Mittal, A., Makonchuk, D.Y., Bhatnagar, S. and Kumar, A. (2009) Matrix metalloproteinase-9 inhibition ameliorates pathogenesis and improves skeletal muscle regeneration in muscular dystrophy. Hum. Mol. Genet., 18, 2584-2598.
36. Kumar, A., Bhatnagar, S. and Kumar, A. (2010) Matrix metalloproteinase inhibitor batimastat alleviates pathology and improves skeletal muscle function in dystrophin-deficient mdx mice. Am. J. Pathol., 177, 248-260.
37. Whitehead, N.P., Pham, C., Gervasio, O.L. and Allen, D.G. (2008) N-acetylcysteine ameliorates skeletal muscle pathophysiology in mdx mice. J. Physiol., 586, 2003-2014.
38. Krippendorf, B.B. and Riley, D.A. (1993) Distinguishing unloading-versus reloading-induced changes in rat soleus muscle. Muscle Nerve, 16, 99-108.
39. St Pierre, B.A. and Tidball, J.G. (1994) Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension. J. Appl. Physiol., 77, 290-297.
40. Tidball, J.G. and Wehling-Henricks, M. (2007) Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J. Physiol, 578, 327-336.
41. Wehling-Henricks, M., Jordan, M.C., Gotoh, T., Grody, W.W., Roos, K.P. and Tidball, J.G. (2010) Arginine metabolism by macrophages promotes cardiac and muscle fibrosis in mdx muscular dystrophy. PLoS ONE, 5, e10763.
42. Kristiansen, M., Graversen, J.H., Jacobsen, C., Sonne, O., Hoffman, H.J., Law, S.K. and Moestrup, S.K. (2001) Identification of the haemoglobin scavenger receptor. Nature, 409, 198-201.
43. Moestrup, S.K. and Moller, H.J. (2004) CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann. Med., 36, 347-354.
44. Kim, H.D., Luthra, M.G., Watts, R.P. and Stern, L.Z. (1980) Factors influencing osmotic fragility of red blood cells in Duchenne muscular dystrophy. Neurology, 30, 726-731.
45. Lim, S.K., Kim, H., Lim, S.K., bin Ali, A., Lim, Y.K., Wang, Y., Chong, S.M., Costantini, F. and Baumman, H. (1998) Increased susceptibility in Hp knockout mice during acute hemolysis. Blood, 92, 1870-1877.
46. Sadrzadeh, S.M., Graf, E., Panter, S.S., Hallaway, P.E. and Eaton, J.W. (1984) Hemoglobin. A biologic Fenton reagent. J. Biol. Chem., 259, 14354-14356.
47. Philippidis, P., Mason, J.C., Evans, B.J., Nadra, I., Taylor, K.M., Haskard, D.O. and Landis, R.C. (2004) Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ. Res., 94, 119-126.
48. Schaer, D.J., Boretti, F.S., Schoedon, G. and Schaffner, A. (2002) Induction of the CD163-dependent haemoglobin uptake by macrophages as a novel anti-inflammatory action of glucocorticoids. Br. J. Haematol., 119, 239-243.
49. Cornelison, D.D. and Wold, B.J. (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol., 191, 270-283.
50. Fuchtbauer, E.M. and Westphal, H. (1992) MyoD and myogenin are coexpressed in regenerating skeletal muscle of the mouse. Dev. Dynam., 193, 34-39.
51. Yablonka-Reuveni, Z. and Rivera, A.J. (1994) Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev. Biol., 164, 588-603.
52. Lluis, F., Perdiguero, E., Nebreda, A.R. and Munoz-Canoves, P. (2006) Regulation of skeletal muscle gene expression by p38 MAP kinases. Trends Cell Biol., 16, 36-44.
53. Raingeaud, J., Gupta, S., Rogers, J.S., Dickens, M., Han, J., Ulevitch, R.J. and Davis, R.J. (1995) 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.
54. Zerria, K., Jerbi, E., Hammami, S., Maaroufi, A., Boubaker, S., Xiong, J.P., Arnaout, M.A. and Fathallah, D.M. (2006) Recombinant integrin CD11b A-domain blocks polymorphonuclear cells recruitment and protects against skeletal muscle inflammatory injury in the rat. Immunology, 119, 431-440.
55. Spencer, M.J., Walsh, C.M., Dorshkind, K.A., Rodriguez, E.M. and Tidball, J.G. (1997) Myonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity. J. Clin. Invest., 99, 2745-2751.
56. Amalfitano, A. and Chamberlain, J.S. (1996) The mdx-amplification-resistant mutation system assay, a simple and rapid polymerase chain reaction-based detection of the mdx allele. Muscle Nerve, 19, 1549-1553.
57. Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J. and Wittwer, C.T. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem., 55, 611-622.
58. Nolan, T., Hands, R.E. and Bustin, S.A. (2006) Quantification of mRNA using real-time RT-PCR. Nat. Protoc., 1, 1559-1582.
59. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol., 3, research/0034.1-0034.11.
60. Pilbrow, A.P., Ellmers, L.J., Black, M.A., Moravec, C.S., Sweet, W.E., Troughton, R.W., Richards, A.M., Frampton, C.M. and Cameron, V.A. (2008) Genomic selection of reference genes for real-time PCR in human myocardium. BMC Med. Genomics, 1, 64.
61. Chazaud, B., Sonnet, C., Lafuste, P., Bassez, G., Rimaniol, A.C., Poron, F., Authier, F.J., Dreyfus, P.A. and Gherardi, R.K. (2003) Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J. Cell Biol., 163, 1133-1143.
62. Nguyen, H.X. and Tidball, J.G. (2003) Null mutation of gp91phox reduces muscle membrane lysis during muscle inflammation in mice. J. Physiol., 553, 833-841.
63. Van Rooijen, N. and Sanders, A. (1994) Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods, 174, 83-93.
64. Gomez, C.M., Maselli, R., Gundeck, J.E., Chao, M., Day, J.W., Tamamizu, S., Lasalde, J.A., McNamee, M. and Wollmann, R.L. (1997) Slow-channel transgenic mice: a model of postsynaptic organellar degeneration at the neuromuscular junction. J. Neurosci., 17, 4170-4179.
65. Lumeng, C.N., DelProposto, J.B., Westcott, D.J. and Saltiel, A.R. (2008) Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes, 57, 3239-3246.
66. Martinez, F.O., Sica, A., Mantovani, A. and Locati, M. (2008) Macrophage activation and polarization. Front. Biosci., 13, 453-461.
67. Odegaard, J.I., Ricardo-Gonzalez, R.R., Red Eagle, A., Vats, D., Morel, C.R., Goforth, M.H., Subramanian, V., Mukundan, L., Ferrante, A.W. and Chawla, A. (2008) Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab., 7, 496-507.