Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy
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Duchenne muscular dystrophy (DMD) is the most common, lethal, muscle-wasting disease of childhood. Previous investigations have shown that muscle macrophages may play an important role in promoting the pathology in the mdx mouse model of DMD. In the present study, we investigate the mechanism through which macrophages promote mdx dystrophy and assess whether the phenotype of the macrophages changes between the stage of peak muscle necrosis (4 weeks of age) and muscle regeneration (12 weeks). We find that 4-week-old mdx muscles contain a population of pro-inflammatory, classically activated M1 macrophages that lyse muscle in vitro by NO-mediated mechanisms. Genetic ablation of the iNOS gene in mdx mice also significantly reduces muscle membrane lysis in 4-week-old mdx mice in vivo. However, 4-week mdx muscles also contain a population of alternatively activated, M2a macrophages that express arginase. In vitro assays show that M2a macrophages reduce lysis of muscle cells by M1 macrophages through the competition of arginase in M2a cells with iNOS in M1 cells for their common, enzymatic substrate, arginine. During the transition from the acute peak of mdx pathology to the regenerative stage, expression of IL-4 and IL-10 increases, either of which can deactivate the M1 phenotype and promote activation of a CD163+, M2c phenotype that can increase tissue repair. Our findings further show that IL-10 stimulation of macrophages activates their ability to promote satellite cell proliferation. Deactivation of the M1 phenotype is also associated with a reduced expression of iNOS, IL-6, MCP-1 and IP-10. Thus, these results show that distinct subpopulations of macrophages can promote muscle injury or repair in muscular dystrophy, and that therapeutic interventions that affect the balance between M1 and M2 macrophage populations may influence the course of muscular dystrophy.
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In models of muscular dystrophy, macrophage polarization may play an important role in muscle wasting; progenitor cells are recruited to sites of mixed M1/M2 inflammation, and the lack of an M1 to M2 switch leads to ineffective remodeling and depletion of progenitor reserves.
“Studies have also suggested that macrophage polarization may play an important role in the process of muscle wasting which occurs in models of muscular dystrophy [124,126,127].”
From Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine (2012) · cites this paper as [126]
Transition from specific M2a to M2c sub-populations may play an important role in late stage differentiation and functional recovery.
“Additional studies have suggested that transition from specific M2a to M2c sub-populations may also play an important role in directing late stage differentiation and functional recovery [126].”
From Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine (2012) · cites this paper as [126]
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The chemokine system in diverse forms of macrophage activation and polarization
MANTOVANI, A., SICA, A., SOZZANI, S., ALLAVENA, P., VECCHI, A., & LOCATI, M. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.09.015 · Cited by 6,534 · see citing works
Alternative activation of macrophages
Gordon, S. (2003) · Nature Reviews Immunology · doi:10.1038/nri978 · Cited by 6,189 · see citing works
Dystrophin: the protein product of the Duchenne muscular dystrophy locus
Hoffman, E. P., Brown, R. H., & Kunkel, L. M. (1987) · Cell · doi:10.1016/0092-8674(87)90579-4 · Cited by 4,693 · see citing works
Arginine metabolism: nitric oxide and beyond
WU, G., & MORRIS, S. M. (1998) · Biochemical Journal · doi:10.1042/bj3360001 · Cited by 2,811 · see citing works
Arnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., Gherardi, R. K., & Chazaud, B. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20070075 · Cited by 2,002 · see citing works
The many faces of macrophage activation
Mosser, D. M. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0602325 · Cited by 1,902 · see citing works
Dystrophin protects the sarcolemma from stresses developed during muscle contraction
Petrof, B. J., Shrager, J. B., Stedman, H. H., Kelly, A. M., & Sweeney, H. L. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.8.3710 · Cited by 1,526 · see citing works
Nitric Oxide Synthases: Properties and Catalytic Mechanism
Griffith, O. W., & Stuehr, D. J. (1995) · Annual Review of Physiology · doi:10.1146/annurev.ph.57.030195.003423 · Cited by 1,311 · see citing works
Stuehr, D. J., Cho, H. J., Kwon, N. S., Weise, M. F., & Nathan, C. F. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.17.7773 · Cited by 816 · see citing works
Buechler, C., Ritter, M., Orsó, E., Langmann, T., Klucken, J., & Schmitz, G. (2000) · Journal of Leukocyte Biology · doi:10.1002/jlb.67.1.97 · Cited by 704 · see citing works
Munder, M., Eichmann, K., & Modolell, M. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.11.5347 · Cited by 647 · see citing works
Stem and Progenitor Cells in Skeletal Muscle Development, Maintenance, and Therapy
Péault, B., Rudnicki, M. A., Torrente, Y., Cossu, G., Tremblay, J. P., Partridge, T. A., Gussoni, E., Kunkel, L. M., & Huard, J. (2007) · Molecular Therapy · doi:10.1038/mt.sj.6300145 · Cited by 572 · see citing works
Th1/Th2-Regulated Expression of Arginase Isoforms in Murine Macrophages and Dendritic Cells
Munder, M., Eichmann, K., Morán, J. M., Centeno, F., Soler, G., & Modolell, M. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.7.3771 · Cited by 561 · see citing works
Glucocorticoid corticosteroids for Duchenne muscular dystrophy
Manzur, A. Y., Küntzer, T., Pike, M. G., & Swan, A. V. (2004) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003725.pub2 · Cited by 539 · see citing works
A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice
Wehling, M., Spencer, M. J., & Tidball, J. G. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200105110 · Cited by 530 · see citing works
Self-citationIL-4 Acts as a Myoblast Recruitment Factor during Mammalian Muscle Growth
Horsley, V., Jansen, K. M., Mills, S. T., & Pavlath, G. K. (2003) · Cell · doi:10.1016/s0092-8674(03)00319-2 · Cited by 508 · see citing works
Chazaud, B., Sonnet, C., Lafuste, P., Bassez, G., Rimaniol, A., Poron, F., Authier, F., Dreyfus, P. A., & Gherardi, R. K. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200212046 · Cited by 452 · see citing works
Acharyya, S., Villalta, S. A., Bakkar, N., Bupha‐Intr, T., Janssen, P. M. L., Carathers, M., Li, Z.-W., Beg, A. A., Ghosh, S., Sahenk, Z., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30556 · Cited by 439 · see citing works
Self-citationTidball, J. G., & Wehling‐Henricks, M. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2006.118265 · Cited by 375 · see citing works
Self-citationBlotta, M. H. S. L., DeKruyff, R. H., & Umetsu, D. T. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.158.12.5589 · Cited by 352 · see citing works
Temporal expression of different pathways of 1-arginine metabolism in healing wounds.
Albina, J. E., Mills, C. D., Henry, W. L., & Caldwell, M. D. (1990) · The Journal of Immunology · doi:10.4049/jimmunol.144.10.3877 · Cited by 351 · see citing works
Cutting Edge: Stat6-Dependent Substrate Depletion Regulates Nitric Oxide Production
Rutschman, R. L., Lang, R., Hesse, M., Ihle, J. N., Wynn, T. A., & Murray, P. J. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.4.2173 · Cited by 324 · see citing works
Practice Parameter: Corticosteroid treatment of Duchenne dystrophy [RETIRED]
Moxley, R. T., Ashwal, S., Pandya, S., Connolly, A. M., Florence, J. M., Mathews, K. D., Baumbach, L. L., McDonald, C. M., Sussman, M. D., & Wade, C. (2005) · Neurology · doi:10.1212/01.wnl.0000148485.00049.b7 · Cited by 301 · see citing works
HUMAN MONOCYTES EXPRESS CD163, WHICH IS UPREGULATED BY IL-10 AND IDENTICAL TO p155
Sulahian, T. H., Högger, P., Wahner, A. E., Wardwell, K., Goulding, N. J., Sorg, C., Droste, A., Stehling, M., Wallace, P. K., Morganelli, P. M., et al. (2000) · Cytokine · doi:10.1006/cyto.2000.0720 · Cited by 281 · see citing works
St Pierre, B. A., & Tidball, J. G. (1994) · Journal of Applied Physiology · doi:10.1152/jappl.1994.77.1.290 · Cited by 251 · cited 3× · see citing works
“Previous, in vivo studies showed that macrophage phenotype switching occurs in skeletal muscle following acute damage, as macrophage populations change from a phagocytic, M1 population to an M2 population that promotes muscle growth, differentiation and regeneration (18,20,39).”
BackgroundSelf-citationDeKruyff, R. H., Fang, Y., & Umetsu, D. T. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.5.2231 · Cited by 241 · see citing works
Hodgetts, S. I., Radley‐Crabb, H. G., Davies, M. J., & Grounds, M. D. (2006) · Neuromuscular Disorders · doi:10.1016/j.nmd.2006.06.011 · Cited by 228 · see citing works
Regulation of Nitric Oxide Synthesis and Apoptosis by Arginase and Arginine Recycling
Mori, M. (2007) · Journal of Nutrition · doi:10.1093/jn/137.6.1616s · Cited by 221 · see citing works
Gotoh, T., & Mori, M. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.144.3.427 · Cited by 196 · see citing works
Self-citationGriggs, R. C., Moxley, R. T., Mendell, J. R., Fenichel, G. M., Brooke, M. H., Pestronk, A., Miller, J. P., Cwik, V. A., Pandya, S. K., Robison, J., et al. (1993) · Neurology · doi:10.1212/wnl.43.3_part_1.520 · Cited by 196 · see citing works
Lundberg, I. E., Brengman, J. M., & Engel, A. G. (1995) · Journal of Neuroimmunology · doi:10.1016/0165-5728(95)00122-0 · Cited by 193 · see citing works
Nguyen, H. X., & Tidball, J. (2003) · Journal of Physiology · doi:10.1111/j..2002.00125.x · Cited by 181 · see citing works
Self-citationMyonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity.
Spencer, M. J., Walsh, C. M., Dorshkind, K. A., Rodriguez, E. M., & Tidball, J. G. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119464 · Cited by 176 · see citing works
Self-citationED2+ macrophages increase selectively myoblast proliferation in muscle cultures.
Massimino, M., Rapizzi, E., Cantini, M., Libera, L., Mazzoleni, F., Arslan, P., & Carraro, U. (1997) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1006/bbrc.1997.6823 · Cited by 162 · see citing works
Signalling events involved in interferon‐γ‐inducible macrophage nitric oxide generation
Blanchette, J., Jaramillo, M., & Olivier, M. (2003) · Immunology · doi:10.1046/j.1365-2567.2003.01620.x · Cited by 145 · see citing works
Tenu, J., Lepoivre, M., Moali, C., Brollo, M., Mansuy, D., & Boucher, J. (1999) · Nitric Oxide · doi:10.1006/niox.1999.0255 · Cited by 141 · see citing works
Martínez‐Pomares, L., Reid, D. M., Brown, G. D., Taylor, P. R., Stillion, R. J., Linehan, S. A., ZAMZE, S. E., Gordon, S., & Wong, S. Y. C. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0902450 · Cited by 139 · see citing works
Schaer, D. J., Boretti, F. S., Schoedon, G., & Schaffner, A. (2002) · British Journal of Haematology · doi:10.1046/j.1365-2141.2002.03790.x · Cited by 135 · see citing works
Early prednisone treatment in Duchenne muscular dystrophy
Merlini, L., Cicognani, A., Malaspina, E., Gennari, M., Gnudi, S., Talim, B., & Franzonı, E. (2002) · Muscle & Nerve · doi:10.1002/mus.10319 · Cited by 131 · see citing works
Amano, F., & Noda, T. (1995) · FEBS Letters · doi:10.1016/0014-5793(95)00700-j · Cited by 124 · see citing works
Nguyen, H. X., & Tidball, J. G. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.031450 · Cited by 122 · see citing works
Self-citationEffect of Supplemental Ornithine on Wound Healing
Shi, H., Fishel, R. S., Efron, D. T., Williams, J. Z., Fischel, M. H., & Barbul, A. (2002) · Journal of Surgical Research · doi:10.1006/jsre.2002.6471 · Cited by 116 · see citing works
Systemic administration of L ‐arginine benefits mdx skeletal muscle function
Barton, E. R., Morris, L. D., Kawana, M., Bish, L. T., & Toursel, T. (2005) · Muscle & Nerve · doi:10.1002/mus.20425 · Cited by 108 · see citing works
Evolving Therapeutic Strategies for Duchenne Muscular Dystrophy: Targeting Downstream Events
Tidball, J. G., & Wehling‐Henricks, M. (2004) · Pediatric Research · doi:10.1203/01.pdr.0000145578.01985.d0 · Cited by 108 · see citing works
Self-citationA role for mast cells in the progression of Duchenne muscular dystrophy?
Gorospe, J. R. M., Tharp, M. D., Hinckley, J., Kornegay, J. N., & Hoffman, E. P. (1994) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(94)90050-7 · Cited by 107 · see citing works
Wehling‐Henricks, M., Lee, J. J., & Tidball, J. G. (2004) · Neuromuscular Disorders · doi:10.1016/j.nmd.2004.04.008 · Cited by 107 · see citing works
Self-citationDistinguishing unloading. Versus reloading‐induced changes in rat soleus muscle
Krippendorf, B. B., & Riley, D. A. (1993) · Muscle & Nerve · doi:10.1002/mus.880160116 · Cited by 104 · see citing works
McLennan, I. S. (1993) · Cell and Tissue Research · doi:10.1007/bf00323586 · Cited by 104 · see citing works
-arginine improves dystrophic phenotype in mice
Voisin, V., Sebrié, C., Matecki, S., Yu, H., Gillet, B., Ramonatxo, M., Israël, M., & de la Porte, S. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.02.010 · Cited by 101 · see citing works
Wehling‐Henricks, M., Sokolow, S., Lee, J. J., Myung, K. H., Villalta, S. A., & Tidball, J. G. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn129 · Cited by 96 · see citing works
Self-citationViral-mediated gene therapy for the muscular dystrophies: Successes, limitations and recent advances
Odom, G. L., Gregorevic, P., & Chamberlain, J. S. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2006.09.007 · Cited by 95 · see citing works
Amalfitano, A., & Chamberlain, J. S. (1996) · Muscle & Nerve · doi:10.1002/(sici)1097-4598(199612)19:12 · Cited by 88 · see citing works
Gratchev, A. N., Schledzewski, K., Guillot, P., & Goerdt, S. (2001) · Skin Pharmacology and Physiology · doi:10.1159/000056357 · Cited by 79 · see citing works
Dystrophin-deficient myofibers are vulnerable to mast cell granule-induced necrosis
Gorospe, J. R. M., Tharp, M. D., Demitsu, T., & Hoffman, E. P. (1994) · Neuromuscular Disorders · doi:10.1016/0960-8966(94)90068-x · Cited by 76 · see citing works
Mesenchymal stem cells are recruited to striated muscle by NFAT/IL-4-mediated cell fusionPreprint
Schulze, M., Bedada, F. B., Technau, A., & Braun, T. W. (2005) · Genes & Development · doi:10.1101/gad.339305 · Cited by 73 · see citing works
Kinali, M., Mercuri, E. M., Main, M. L., Francesco Muntoni, A., & Dubowitz, V. (2002) · Neuromuscular Disorders · doi:10.1016/s0960-8966(02)00097-4 · Cited by 66 · see citing works
Dubowitz, V., Kinali, M., Main, M. L., Mercuri, E. M., & Francesco Muntoni, A. (2002) · European Journal of Paediatric Neurology · doi:10.1053/ejpn.2002.0583 · Cited by 56 · see citing works
Lagrota-Cândido, J., Vasconcellos, R., Cavalcanti, M. G., Bozza, M. T., Savino, W., & Quírico‐Santos, T. (2002) · International Journal of Experimental Pathology · doi:10.1046/j.1365-2613.2002.00221.x · Cited by 41 · see citing works
Spolarics, Z., & Bond, J. S. (1989) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(89)90455-4 · Cited by 25 · see citing works
Oligonucleotide-mediated gene therapy for muscular dystrophies
Rando, T. A. (2002) · Neuromuscular Disorders · doi:10.1016/s0960-8966(02)00083-4 · Cited by 20 · see citing works
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Microglial <scp>M1/M2</scp> polarization and metabolic states
Orihuela, R., McPherson, C. A., & Harry, G. J. (2016) · British Journal of Pharmacology · doi:10.1111/bph.13139 · Cited by 2,070 · see citing works
Repertoire of microglial and macrophage responses after spinal cord injury
David, S., & Kroner, A. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3053 · Cited by 1,437 · see citing works
Regulatory interactions between muscle and the immune system during muscle regeneration
Tidball, J. G., & Villalta, S. A. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00735.2009 · Cited by 1,105 · see citing works
Self-citationBrown, B. N., Ratner, B. D., Goodman, S. B., Amar, S., & Badylak, S. F. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.02.034 · Cited by 926 · see citing works
“Studies have also suggested that macrophage polarization may play an important role in the process of muscle wasting which occurs in models of muscular dystrophy [124,126,127].”
BackgroundAberrant repair and fibrosis development in skeletal muscle
Mann, C. J., Perdiguero, E., Kharraz, Y., Aguilar, S., Pessina, P., Serrano, A. L., & Muñoz-Cánoves, P. (2011) · Skeletal Muscle · doi:10.1186/2044-5040-1-21 · Cited by 853 · see citing works
Lemos, D. R., Babaeijandaghi, F., Low, M., Chang, C.-K., Lee, S. T., Fiore, D., Zhang, R.-H., Natarajan, A., Nedospasov, S. A., & Rossi, F. M. V. (2015) · Nature Medicine · doi:10.1038/nm.3869 · Cited by 740 · see citing works
Satellite Cells and Skeletal Muscle Regeneration
Dumont, N. A., Bentzinger, C. F., Sincennes, M., & Rudnicki, M. A. (2015) · Comprehensive Physiology · doi:10.1002/cphy.c140068 · Cited by 719 · see citing works
Macrophage phenotypes during tissue repair
Novak, M. L., & Koh, T. J. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.1012512 · Cited by 658 · see citing works
Beck, K. D., Nguyen, H. X., Galvan, M. D., Salazar, D. L., Woodruff, T. M., & Anderson, A. J. (2010) · Brain · doi:10.1093/brain/awp322 · Cited by 649 · see citing works
Self-citationPreparing the ground for tissue regeneration: from mechanism to therapy
Forbes, S. J., & Rosenthal, N. A. (2014) · Nature Medicine · doi:10.1038/nm.3653 · Cited by 585 · see citing works
Panduro, M., Benoist, C., & Mathis, D. (2016) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-095948 · Cited by 536 · see citing works
IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration
Deng, B., Wehling-Henricks, M., Villalta, S. A., Wang, Y., & Tidball, J. G. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1103180 · Cited by 472 · see citing works
Self-citationSussman, E. M., Halpin, M. C., Muster, J., Moon, R. T., & Ratner, B. D. (2014) · Annals of Biomedical Engineering · doi:10.1007/s10439-013-0933-0 · Cited by 416 · see citing works
Cellular dynamics in the muscle satellite cell niche
Bentzinger, C. F., Wang, Y. X., Dumont, N. A., & Rudnicki, M. A. (2013) · The EMBO Reports · doi:10.1038/embor.2013.182 · Cited by 398 · see citing works
Mechanisms of Muscle Injury, Repair, and Regeneration
Tidball, J. G. (2011) · Comprehensive physiology · doi:10.1002/cphy.c100092 · Cited by 439 · see citing works
Self-citationShaul, M. E., Bennett, G., Strissel, K. J., Greenberg, A. S., & Obin, M. S. (2010) · Diabetes · doi:10.2337/db09-1402 · Cited by 370 · see citing works
A Muscle Stem Cell Support Group: Coordinated Cellular Responses in Muscle Regeneration
Wosczyna, M. N., & Rando, T. A. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.06.018 · Cited by 353 · see citing works
Skeletal muscle regeneration is modulated by inflammation
Yang, W.-J., & Hu, P. (2018) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2018.01.002 · Cited by 303 · see citing works
OsteoMacs: Key players around bone biomaterials.
Miron, R., & Bosshardt, D. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2015.12.017 · Cited by 295 · see citing works
Tonkin, J. N., Temmerman, L., Sampson, R. D., Gallego-Colón, E., Barberi, L., Bilbao, D., Schneider, M. D., Musarò, A., & Rosenthal, N. A. (2015) · Molecular Therapy · doi:10.1038/mt.2015.66 · Cited by 320 · see citing works
Regulatory factors and cell populations involved in skeletal muscle regeneration
Broek, R. W. T., Grefte, S., & den Hoff, J. W. V. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22127 · Cited by 315 · see citing works
Immune-mediated pathology in Duchenne muscular dystrophy
Rosenberg, A. S., Puig, M., Nagaraju, K., Hoffman, E. P., Villalta, S. A., Rao, V. A., Wakefield, L. M., & Woodcock, J. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa7322 · Cited by 306 · see citing works
Self-citationMacrophage Plasticity and the Role of Inflammation in Skeletal Muscle Repair
Kharraz, Y., Guerra, J., Mann, C. J., Serrano, A. L., & Muñoz‐Cánoves, P. (2013) · Mediators of Inflammation · doi:10.1155/2013/491497 · Cited by 302 · see citing works
Villalta, S. A., Rinaldi, C., Deng, B., Liu, G., Fedor, B., & Tidball, J. G. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddq523 · Cited by 299 · see citing works
Self-citationWhen Immune Cells Turn Bad—Tumor-Associated Microglia/Macrophages in Glioma
Roesch, S., Rapp, C., Dettling, S., & Herold‐Mende, C. C. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020436 · Cited by 293 · see citing works
Regulation and dysregulation of fibrosis in skeletal muscle
Serrano, A. L., & Muñoz‐Cánoves, P. (2010) · Experimental Cell Research · doi:10.1016/j.yexcr.2010.05.035 · Cited by 291 · see citing works
Pillon, N. J., Bilan, P. J., Fink, L. N., & Klip, A. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00553.2012 · Cited by 285 · see citing works
Brown, B. N., & Badylak, S. F. (2012) · Acta Biomaterialia · doi:10.1016/j.actbio.2012.10.025 · Cited by 262 · see citing works
Regulatory T cells suppress muscle inflammation and injury in muscular dystrophy
Villalta, S. A., Rosenthal, W. L., Martinez, L., Kaur, A., Sparwasser, T. D., Tidball, J. G., Margeta, M., Spencer, M. J., & Bluestone, J. A. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009925 · Cited by 253 · see citing works
Self-citationForcina, L., Cosentino, M., & Musarò, A. (2020) · Cells · doi:10.3390/cells9051297 · Cited by 252 · see citing works
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Perdiguero, E., Sousa-Victor, P., Ruiz-Bonilla, V., Jardí, M., Caelles, C., Serrano, A. L., & Muñoz-Cánoves, P. (2011) · Journal of Cell Biology · doi:10.1083/jcb.201104053 · Cited by 236 · see citing works
Choi, K. M., Kashyap, P. C., Dutta, N., Stoltz, G. J., Ordog, T., Shea Donohue, T., Bauer, A. J., Linden, D. R., Szurszewski, J. H., Gibbons, S. J., et al. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.02.014 · Cited by 233 · see citing works
Anti-Inflammatory Targets for the Treatment of Reperfusion Injury in Stroke
Mizuma, A., & Yenari, M. A. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00467 · Cited by 226 · see citing works
Desguerre, I., Mayer, M., Leturcq, F., Barbet, J., Gherardi, R., & Christov, C. (2009) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/nen.0b013e3181aa31c2 · Cited by 205 · see citing works
Juban, G., Saclier, M., Yacoub‐Youssef, H., Kernou, A., Arnold, L., Boisson, C., Larbi, S. B., Magnan, M., Cuvellier, S., Théret, M., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.077 · Cited by 223 · see citing works
Macrophage activation and skeletal muscle healing following traumatic injury
Novak, M. L., Weinheimer-Haus, E. M., & Koh, T. J. (2013) · The Journal of Pathology · doi:10.1002/path.4301 · Cited by 209 · see citing works
Eduardo Fuentes, Q., Fuentes, F., Vilahur, G., Badimón, L., & Palomo, I. F. (2013) · Mediators of Inflammation · doi:10.1155/2013/136584 · Cited by 208 · see citing works
Wang, Y., Wehling‐Henricks, M., Samengo, G., & Tidball, J. G. (2015) · Aging Cell · doi:10.1111/acel.12350 · Cited by 205 · see citing works
Self-citationMacrophage Plasticity in Skeletal Muscle Repair
Rigamonti, E., Zordan, P., Sciorati, C., Rovere-Querini, P., & Brunelli, S. (2014) · BioMed Research International · doi:10.1155/2014/560629 · Cited by 196 · see citing works
Cellular and Molecular Mechanisms Regulating Fibrosis in Skeletal Muscle Repair and Disease
Serrano, A. L., Mann, C. J., Vidal, B., Ardite, E., Perdiguero, E., & Muñoz-Cánoves, P. (2011) · Current Topics in Developmental Biology · doi:10.1016/b978-0-12-385940-2.00007-3 · Cited by 200 · see citing works
Macrophages Are Key Regulators of Stem Cells during Skeletal Muscle Regeneration and Diseases
Dort, J., Fabre, P., Molina, T., & Dumont, N. A. (2019) · Stem Cells International · doi:10.1155/2019/4761427 · Cited by 196 · see citing works
Macrophage and dendritic cell phenotypic diversity in the context of biomaterials
Kou, P. M., & Babensee, J. E. (2011) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.32971 · Cited by 190 · see citing works
Rethinking Regenerative Medicine: A Macrophage-Centered Approach
Brown, B., Sicari, B. M., & Badylak, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00510 · Cited by 185 · see citing works
Regulation and phylogeny of skeletal muscle regeneration
Baghdadi, M. B., & Tajbakhsh, S. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.07.026 · Cited by 186 · see citing works
Ding, H., Chen, S., Pan, X., Dai, X., Pan, G., Li, Z., Mai, X., Tian, Y., Zhang, S., Liu, B., et al. (2021) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12700 · Cited by 181 · see citing works
Inflammasome Up-Regulation and Activation in Dysferlin-Deficient Skeletal Muscle
Rawat, R., Cohen, T. V., Ampong, B., Francia, D., Henriques‐Pons, A., Hoffman, E. P., & Nagaraju, K. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090058 · Cited by 176 · see citing works
Asynchronous remodeling is a driver of failed regeneration in Duchenne muscular dystrophy
Dadgar, S., Wang, Z., Johnston, H., Kesari, A., Nagaraju, K., Chen, Y., Hill, D. A., Partridge, T. A., Giri, M., Freishtat, R. J., et al. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201402079 · Cited by 174 · see citing works
Divergent Roles of Inflammation in Skeletal Muscle Recovery From Injury
Howard, E. E., Pasiakos, S. M., Blesso, C. N., Fussell, M. A., & Rodriguez, N. R. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00087 · Cited by 176 · see citing works
Villalta, S. A., Deng, B., Rinaldi, C., Wehling-Henricks, M., & Tidball, J. G. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1101267 · Cited by 158 · see citing works
Self-citationIchim, T. E., Alexandrescu, D. T., Solano, F., Lara, F., Campion, R. D. N., Paris, E., Woods, E. J., Murphy, M. P., Dasanu, C. A., Patel, A. N., et al. (2009) · Cellular Immunology · doi:10.1016/j.cellimm.2009.10.006 · Cited by 160 · see citing works
Perandini, L. A., Chimin, P., Lutkemeyer, D. D. S., & Câmara, N. O. S. (2018) · FEBS Journal · doi:10.1111/febs.14417 · Cited by 160 · see citing works
Skeletal muscle regeneration and impact of aging and nutrition
Domingues-Faria, C., Vasson, M.-P., Goncalves-Mendes, N., Boirie, Y., & Walrand, S. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2015.12.004 · Cited by 157 · see citing works
Mojumdar, K., Liang, F., Giordano, C., Lemaire, C. F., Danialou, G., Okazaki, T., Bourdon, J., Rafei, M., Galipeau, J., Divangahi, M., et al. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201403967 · Cited by 155 · see citing works
Impact of ageing on muscle cell regeneration.
Carosio, S., Berardinelli, M., Aucello, M., & Musarò, A. (2011) · Ageing Research Reviews · doi:10.1016/j.arr.2009.08.001 · Cited by 156 · see citing works
Santa, F. D., Vitiello, L., Torcinaro, A., & Ferraro, E. (2018) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7420 · Cited by 154 · see citing works
Immunobiology of Inherited Muscular Dystrophies
Tidball, J. G., Welc, S. S., & Wehling‐Henricks, M. (2018) · Comprehensive physiology · doi:10.1002/cphy.c170052 · Cited by 166 · see citing works
Self-citationChahbouni, M., Escames, G., Venegas, C., Sevilla, B., García, J. A. G., López, L. C., Muñoz‐Hoyos, A., Molina‐Carballo, A., & Acuña-Castroviejo, D. (2010) · Journal of Pineal Research · doi:10.1111/j.1600-079x.2010.00752.x · Cited by 151 · see citing works
Coulis, G., Jaime, D., Guerrero-Juarez, C., Kastenschmidt, J. M., Farahat, P. K., Nguyen, Q., Pervolarakis, N., McLinden, K., Thurlow, L., Movahedi, S., et al. (2023) · Science Advances · doi:10.1126/sciadv.add9984 · Cited by 150 · see citing works
Self-citationTargeting Fibrosis in Duchenne Muscular Dystrophy
Zhou, L., & Lu, H. (2010) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181e9a34b · Cited by 149 · see citing works
Sun, C., Li, S., Yang, C.-L., Xue, R., Xi, Y., Wang, L., Zhao, Q.-L., & Li, D. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.655019 · Cited by 147 · see citing works
RetractedWasting mechanisms in muscular dystrophy
Shin, J. S., Tajrishi, M. M., Ogura, Y., & Kumar, A. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.05.001 · Cited by 145 · see citing works
Wermuth, P. J., & Jiménez, S. (2015) · Clinical and Translational Medicine · doi:10.1186/s40169-015-0047-4 · Cited by 151 · see citing works
Satellite Cells and Skeletal Muscle Regeneration
Dumont, N. A., Bentzinger, C. F., Sincennes, M., & Rudnicki, M. A. (2015) · Comprehensive physiology · doi:10.1002/j.2040-4603.2015.tb00646.x · Cited by 143 · see citing works
Bier, A., Berenstein, P., Kronfeld, N., Morgoulis, D., Ziv-Av, A., Goldstein, H., Kazimirsky, G., Cazacu, S., Meir, R., Popovtzer, R., et al. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.04.055 · Cited by 138 · see citing works
The Basis of Muscle Regeneration
Musarò, A. (2014) · Advances in Biology · doi:10.1155/2014/612471 · Cited by 138 · see citing works
Duddy, W. J., Duguez, S., Johnston, H., Cohen, T. V., Phadke, A., Gordish‐Dressman, H., Nagaraju, K., Gnocchi, V. F., Low, S., & Partridge, T. A. (2015) · Skeletal Muscle · doi:10.1186/s13395-015-0041-y · Cited by 130 · see citing works
Immune Cells and Inflammation in Diabetic Nephropathy
Zheng, Z., & Zheng, F. (2015) · Journal of Diabetes Research · doi:10.1155/2016/1841690 · Cited by 136 · see citing works
Temporal Changes in Myeloid Cells in the Cervix during Pregnancy and Parturition
Timmons, B. C., Fairhurst, A., & Mahendroo, M. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803138 · Cited by 135 · see citing works
Shared signaling systems in myeloid cell-mediated muscle regeneration
Tidball, J., Dorshkind, K., & Wehling-Henricks, M. (2014) · Development · doi:10.1242/dev.098285 · Cited by 130 · see citing works
Self-citationMultiscale analysis of a regenerative therapy for treatment of volumetric muscle loss injury
Aguilar, C. A., Greising, S. M., Watts, A., Goldman, S. M., Peragallo, C., Zook, C., Larouche, J. A., & Corona, B. T. (2018) · Cell Death Discovery · doi:10.1038/s41420-018-0027-8 · Cited by 133 · see citing works
The Muscle Stem Cell Niche in Health and Disease
Mashinchian, O., Pisconti, A., Moal, E. L., & Bentzinger, C. F. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.08.003 · Cited by 127 · see citing works
Paepe, B. D., & Bleecker, J. D. (2013) · Mediators of Inflammation · doi:10.1155/2013/540370 · Cited by 131 · see citing works
Regenerative function of immune system: Modulation of muscle stem cells
Saini, J., McPhee, J. S., Al-Dabbagh, S., Stewart, C. E., & Al‐Shanti, N. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.03.006 · Cited by 129 · see citing works
Jiang, G.-L., Yang, X., Zhou, H., Long, J., Liu, B., Zhang, L.-M., & Lü, D. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.03.010 · Cited by 128 · see citing works
Arginine Metabolism by Macrophages Promotes Cardiac and Muscle Fibrosis in mdx Muscular Dystrophy
Wehling‐Henricks, M., Jordan, M. C., Gotoh, T., Grody, W. W., Roos, K. P., & Tidball, J. G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010763 · Cited by 126 · see citing works
Self-citationJudge, S. M., Howard, T. M., Ahn, B., Ferreira, L. F., & Judge, A. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062687 · Cited by 125 · see citing works
Cellular Players in Skeletal Muscle Regeneration
Ceafalan, L. C., Popescu, B. O., & Hinescu, M. E. (2014) · BioMed Research International · doi:10.1155/2014/957014 · Cited by 122 · see citing works
Capote, J. C., Kramerova, I. A., Martinez, L., Vetrone, S. A., Barton, E. R., Sweeney, H. L., Miceli, M. C., & Spencer, M. J. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201510086 · Cited by 122 · see citing works
Evans, N. P., Misyak, S. A., Robertson, J. L., Bassaganya-Riera, J., & Grange, R. W. (2009) · PM&R · doi:10.1016/j.pmrj.2009.04.010 · Cited by 119 · see citing works
A Perspective on Immunomodulation and Tissue Repair
Mokarram, N., & Bellamkonda, R. (2014) · Annals of Biomedical Engineering · doi:10.1007/s10439-013-0941-0 · Cited by 106 · see citing works
Adeno-associated viral vectors do not efficiently target muscle satellite cells
Arnett, A. L. H., Konieczny, P., Ramos, J. N., Hall, J. K., Odom, G., Yablonka‐Reuveni, Z., Chamberlain, J. R., & Chamberlain, J. S. (2014) · Molecular Therapy — Methods & Clinical Development · doi:10.1038/mtm.2014.38 · Cited by 110 · see citing works
Physical activity and the endocannabinoid system: an overview
Tantimonaco, M., Ceci, R., Sabatini, S., Catani, M. V., Rossi, A., Gasperi, V., & Maccarrone, M. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1575-6 · Cited by 112 · see citing works
Automated drug screening with contractile muscle tissue engineered from dystrophic myoblasts
Vandenburgh, H. H., Shansky, J., Benesch, F., Skelly, K., Spinazzola, J. M., Saponjian, Y., & Tseng, B. S. (2009) · The FASEB Journal · doi:10.1096/fj.09-134411 · Cited by 110 · see citing works
Calcium silicate bioactive ceramics induce osteogenesis through oncostatin M
Zhou, P., Xia, D., Ni, Z., Ou, T., Wang, Y., Zhang, H., Mao, L., Lin, K., Xu, S., & Liu, J. (2020) · Bioactive Materials · doi:10.1016/j.bioactmat.2020.09.018 · Cited by 109 · see citing works
In vitro response of macrophage polarization to a keratin biomaterial
Fearing, B. V., & Dyke, M. E. V. (2014) · Acta Biomaterialia · doi:10.1016/j.actbio.2014.04.003 · Cited by 109 · see citing works
Inflammation in tissue engineering: The Janus between engraftment and rejection
Crupi, A., Costa, A., Tarnok, A., Melzer, S., & Teodori, L. (2015) · European Journal of Immunology · doi:10.1002/eji.201545818 · Cited by 108 · see citing works
Extrinsic and intrinsic control of macrophage inflammatory responses
Cohen, H. B., & Mosser, D. M. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.0413236 · Cited by 102 · see citing works
Crosstalk Between Skeletal Muscle and Immune System: Which Roles Do IL-6 and Glutamine Play?
Rogeri, P. S., Gasparini, S. O., Martins, G. L., Costa, L. K. F., Araujo, C. C., Lugaresi, R., Kopfler, M., & Lancha, A. H. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.582258 · Cited by 102 · see citing works
Moratal, C., Raffort, J., Arrighi, N., Rekima, S., Schaub, S., Dechesne, C. A., Chinetti, G., & Dani, C. (2018) · Scientific Reports · doi:10.1038/s41598-018-35429-w · Cited by 101 · see citing works
Novel and optimized strategies for inducing fibrosis in vivo: focus on Duchenne Muscular Dystrophy
Pessina, P., Cabrera, D., Morales, M. G., Riquelme, C. A., Gutiérrez, J., Serrano, A. L., Brandan, E., & Muñoz‐Cánoves, P. (2014) · Skeletal Muscle · doi:10.1186/2044-5040-4-7 · Cited by 100 · see citing works
Regeneration versus fibrosis in skeletal muscle
Moyer, A. L., & Wagner, K. R. (2011) · Current Opinion in Rheumatology · doi:10.1097/bor.0b013e32834bac92 · Cited by 99 · see citing works
Giordano, C., Mojumdar, K., Liang, F., Lemaire, C. F., Li, T., Richardson, J., Divangahi, M., Qureshi, S. T., & Petrof, B. J. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu735 · Cited by 97 · see citing works
Extracellular microRNAs are dynamic non-vesicular biomarkers of muscle turnover
Roberts, T. C., Godfrey, C., McClorey, G., Vader, P., Briggs, D. A., Gardiner, C., Aoki, Y., SARGENT, I. L., Morgan, J. E., & Wood, M. J. A. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt724 · Cited by 95 · see citing works
Bernard, C. E., Gibbons, S., Mann, I., Froschauer, L., Parkman, H., Harbison, S., Abell, T., Snape, W., Hasler, W., McCallum, R. W., et al. (2014) · Neurogastroenterology and Motility · doi:10.1111/nmo.12389 · Cited by 91 · see citing works
Selective inhibition and augmentation of alternative macrophage activation by progesterone
Menzies, F. M., Henriquez, F., Alexander, J., & Roberts, C. W. (2011) · Immunology · doi:10.1111/j.1365-2567.2011.03488.x · Cited by 85 · see citing works
Gordon, B. S., Delgado-Diaz, D. C., & Kostek, M. C. (2012) · Clinical Nutrition · doi:10.1016/j.clnu.2012.06.003 · Cited by 94 · see citing works
Regulatory T cells in skeletal muscle repair and regeneration: recent insights
Wu, J., Ren, B., Wang, D., & Lin, H. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05142-8 · Cited by 94 · see citing works
Fibrosis development in early-onset muscular dystrophies: Mechanisms and translational implications
Serrano, A. L., & Muñoz‐Cánoves, P. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.09.013 · Cited by 94 · see citing works
- Authors
- Villalta, S. A., Nguyen, H. X., Deng, B., Gotoh, T., & Tidball, J. G.
- Affiliations
- University of California, Los Angeles (US)
- Kumamoto University (JP)
- Corresponding author
- Tidball, J. G.
- Venue
- Human Molecular Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-11-07
- Volume
- 18
- Issue
- 3
- Pages
- 482-496
- ISSN
- 0964-6906 (ISSN-L)
- 1460-2083
- PMC
- PMC2638796
- OpenAlex
- W2144067550
- Cited by
- 512
- References
- 60
- Citations by year
- 2026: 11 · 2025: 25 · 2024: 18 · 2023: 28 · 2022: 41 · 2021: 32 · 2020: 32 · 2019: 33 · 2018: 39 · 2017: 37 · 2016: 25 · 2015: 39 · 2014: 40 · 2013: 32 · 2012: 27
- FWCI
- 7.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Human Molecular Genetics (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Muscular Dystrophy Association
- National Institutes of Health (5r01ar040343-12, AR40343)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR047855, R01 AR47721, R01 AR 40343, R01AR047721, F31AR054724)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Health Sciences › Medicine › Genetics › Neurogenetic and Muscular Disorders Research
- Keywords
- Duchenne muscular dystrophy, mdx mice, macrophage polarization, M1 macrophages, M2 macrophages, arginine metabolism, arginase, inducible nitric oxide synthase, nitric oxide, muscle necrosis, muscle regeneration, IL-10, IL-4, CD163, satellite cell proliferation, tissue repair
- MeSH terms
- Animals, Arginine, Cells, Cultured, Humans, Macrophage Activation, Macrophages, Mice, Inbred C57BL, Mice, Transgenic, Muscular Dystrophy, Animal, Nitric Oxide, Phenotype, Severity of Illness Index, Cytokines, Muscle, Skeletal, Muscular Dystrophy, Duchenne, Cell Proliferation, Mice, Nitric Oxide Synthase Type II
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