Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy

Human Molecular Genetics

Volumn 18, Issue 3, 2009, Pages 482-496

  Villalta, S Armando ^a   Nguyen, Hal X ^a   Deng, Bo ^a   Gotoh, Tomomi ^c   Tidbal, James G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c KUMAMOTO UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CD163 ANTIGEN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE SYNTHASE;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL FUNCTION; CELL PROLIFERATION; CELL STIMULATION; CELL SUBPOPULATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DUCHENNE MUSCULAR DYSTROPHY; IN VITRO STUDY; MACROPHAGE; MOUSE; MUSCLE CELL; MUSCLE FIBER MEMBRANE; MUSCLE NECROSIS; MUSCLE REGENERATION; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ARGININE; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHENOTYPE; SEVERITY OF ILLNESS INDEX;

MUS;

EID: 58749098598     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn376     Document Type: Article

References (59)

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. 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.
4. Tidball, J.G. and Wehling-Henricks, M. (2004) Evolving therapeutic strategies for Duchenne muscular dystrophy: Targeting downstream events. Pediatr. Res., 56, 831-841.
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. 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.
7. Gorospe, J.R., Tharp, M.D., Hinckley, J., Kornegay, J.N. and Hoffman, E.P. (1994) A role for mast cells in the progression of Duchenne muscular dystrophy? Correlations in dystrophin-deficient humans, dogs, and mice. J. Neurol. Sci., 122, 44-56.
8. 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.
9. 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.
10. Manzur, A.Y., Kuntzer, T., Pike, M. and Swan, A. (2008) Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst. Rev., 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. Griggs, R.C., Moxley, R.T. III, Mendell, J.R., Fenichel, G.M., Brooke, M.H., Pestronk, A., Miller, J.P., Cwik, V.A., Pandya, S., Robison, J. et al. (1993) Duchenne dystrophy: Randomized, controlled trial of prednisone (18 months) and azathioprine (12 months). Neurology, 43, 520-527.
13. 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.
14. Gordon, S. (2003) Alternative activation of macrophages. Nat. Rev. Immunol., 3, 23-35.
15. 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.
16. Gratchev, A., Schledzewski, K., Guillot, P. and Goerdt, S. (2001) Alternatively activated antigen-presenting cells: Molecular repertoire, immune regulation, and healing. Skin Pharmacol. Appl. Skin Physiol. 14, 272-279.
17. Nguyen, H.X. and Tidball, J.G. (2003) Interactions between neutrophils and macrophages promote macrophage killing of rat muscle cells in vitro. J. Physiol., 547, 125-132.
18. 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.
19. Krippendorf, B.B. and Riley, D.A. (1993) Distinguishing unloading-versus reloading-induced changes in rat soleus muscle. Muscle Nerve, 16, 99-108.
20. 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.
21. Munder, M., Eichmann, K., Moran, J.M., Centeno, F., Soler, G. and Modolell, M. (1999) Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol., 163, 3771-3777.
22. Munder, M., Eichmann, K. and Modolell, M. (1998) Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/ arginase balance: Competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype. J. Immunol., 160, 5347-5354.
23. Albina, J.E., Mills, C.D., Henry, W.L. Jr and Caldwell, M.D. (1990) Temporal expression of different pathways of 1-arginine metabolism in healing wounds. J. Immunol., 144, 3877-3880.
24. Shi, H.P., Fishel, R.S., Efron, D.T., Williams, J.Z., Fishel, M.H. and Barbul, A. (2002) Effect of supplemental ornithine on wound healing. J. Surg. Res., 106, 299-302.
25. Lundberg, I., Brengman, J.M. and Engel, A.G. (1995) Analysis of cytokine expression in muscle in inflammatory myopathies, Duchenne dystrophy, and non-weak controls. J. Neuroimmunol., 63, 9-16.
26. Lagrota-Candido, J., Vasconcellos, R., Cavalcanti, M., Bozza, M., Savino, W. and Quirico-Santos, T. (2002) Resolution of skeletal muscle inflammation in mdx dystrophic mouse is accompanied by increased immunoglobulin and interferon-gamma production. Int. J. Exp. Pathol. 83, 121-132.
27. Mosser, D.M. (2003) The many faces of macrophage activation. J. Leukoc. Biol., 73, 209-212.
28. Blanchette, J., Jaramillo, M. and Olivier, M. (2003) Signalling events involved in interferon-gamma-inducible macrophage nitric oxide generation. Immunology, 108, 513-522.
29. Mori, M. (2007) Regulation of nitric oxide synthesis and apoptosis by arginase and arginine recycling. J. Nutr., 137, 1616S-1620S.
30. Griffith, O.W. and Stuehr, D.J. (1995) Nitric oxide synthases: properties and catalytic mechanism. Annu. Rev. Physiol., 57, 707-736.
31. Stuehr, D.J., Cho, H.J., Kwon, N.S., Weise, M.F. and Nathan, C.F. (1991) Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: An FAD- and FMN-containing flavoprotein. Proc. Natl Acad. Sci. USA, 88, 7773-7777.
32. Wu, G. and Morris, S.M. Jr (1998) Arginine metabolism: Nitric oxide and beyond. Biochem. J., 336, 1-17.
33. Spolarics, Z. and Bond, J.S. (1989) Comparison of biochemical properties of liver arginase from streptozocin-induced diabetic and control mice. Arch. Biochem. Biophys., 274, 426-433.
34. Tenu, J.P., Lepoivre, M., Moali, C., Brollo, M., Mansuy, D. and Boucher, J.L. (1999) Effects of the new arginase inhibitor N(omega)-hydroxy-nor-L-arginine on NO synthase activity in murine macrophages. Nitric Oxide, 3, 427-438.
35. Gotoh, T. and Mori, M. (1999) Arginase II downregulates nitric oxide (NO) production and prevents NO-mediated apoptosis in murine macrophage-derived RAW 264.7 cells. J. Cell. Biol., 144, 427-434.
36. Rutschman, R., Lang, R., Hesse, M., Ihle, J.N., Wynn, T.A. and Murray, P.J. (2001) Cutting edge: Stat6-dependent substrate depletion regulates nitric oxide production. J. Immunol., 166, 2173-2177.
37. Barton, E.R., Morris, L., Kawana, M., Bish, L.T. and Toursel, T. (2005) Systemic administration of L-arginine benefits mdx skeletal muscle function. Muscle Nerve, 32, 751-760.
38. Voisin, V., Sebrie, C., Matecki, S., Yu, H., Gillet, B., Ramonatxo, M., Israel, M. and De la Porte, S. (2005) L-arginine improves dystrophic phenotype in mdx mice. Neurobiol. Dis., 20, 123-130.
39. 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 skeletalmuscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med., 204, 1057-1069.
40. 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.
41. McLennan, I.S. (1993) Resident macrophages (ED2- and ED3-positive) do not phagocytose degenerating rat skeletal muscle fibres. Cell Tissue Res., 272, 193-196.
42. Buechler, C., Ritter, M., Orso, E., Langmann, T., Klucken, J. and Schmitz, G. (2000) Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and antiinflammatory stimuli. J. Leukoc. Biol., 67, 97-103.
43. 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.
44. 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.
45. 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.
46. Dubowitz, V., Kinali, M., Main, M., Mercuri, E. and Muntoni, F. (2002) Remission of clinical signs in early duchenne muscular dystrophy on intermittent low-dosage prednisolone therapy. Eur. J. Paediatr. Neurol., 6, 153-159.
47. Kinali, M., Mercuri, E., Main, M., Muntoni, F. and Dubowitz, V. (2002) An effective, low-dosage, intermittent schedule of prednisolone in the long-term treatment of early cases of Duchenne dystrophy. Neuromuscul. Disord., 12 (Suppl. 1), S169-S174.
48. Merlini, L., Cicognani, A., Malaspina, E., Gennari, M., Gnudi, S., Talim, B. and Franzoni, E. (2003) Early prednisone treatment in Duchenne muscular dystrophy. Muscle Nerve, 27, 222-227.
49. Blotta, M.H., DeKruyff, R.H. and Umetsu, D.T. (1997) Corticosteroids inhibit IL-12 production in human monocytes and enhance their capacity to induce IL-4 synthesis in CD4+ lymphocytes. J. Immunol., 158 5589-5595.
50. DeKruyff, R.H., Fang, Y. and Umetsu, D.T. (1998) Corticosteroids enhance the capacity of macrophages to induce Th2 cytokine synthesis in CD4+ lymphocytes by inhibiting IL-12 production. J. Immunol., 160 2231-2237.
51. 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.
52. Schulze, M., Belema-Bedada, F., Technau, A. and Braun, T. (2005) Mesenchymal stem cells are recruited to striated muscle by NFAT/ IL-4-mediated cell fusion. Genes Dev., 19, 1787-1798.
53. Rando, T.A. (2002) Oligonucleotide-mediated gene therapy for muscular dystrophies. Neuromuscul. Disord., 12 (Suppl. 1), S55-S60.
54. Odom, G.L., Gregorevic, P. and Chamberlain, J.S. (2007) Viral-mediated gene therapy for the muscular dystrophies: Successes, limitations and recent advances. Biochim. Biophys. Acta., 1772, 243-262.
55. Peault, B., Rudnicki, M., Torrente, Y., Cossu, G., Tremblay, J.P., Partridge, T., Gussoni, E., Kunkel, L.M. and Huard, J. (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol. Ther., 15, 867-877.
56. 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.
57. 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.
58. Amano, F. and Noda, T. (1995) Improved detection of nitric oxide radical (NO.) production in an activated macrophage culture with a radical scavenger, carboxy PTIO and Griess reagent. FEBS Lett., 368, 425-428.
59. 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.