Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension
Abstract
The hypothesis that distinct populations of macrophages are associated with muscle necrosis and regeneration was examined in Wistar rat soleus muscle after 10 days of hindlimb suspension and 2, 4, and 7 days after the resumption of weight bearing. Necrosis was identified using histological features, such as muscle fiber infiltration, and regeneration was identified using immunohistochemical techniques for developmental myosin heavy chain (dMHC). Light-microscopic observations show that necrotic fibers in 2-day reloaded soleus muscle were invaded by ED1+ and Ia+ macrophages. The number of invaded fibers in muscles reloaded for 2 days increased to 2.8/mm2 compared with 0.2/mm2 in age-matched normal muscle but returned to control values by the 4th day of resumed weight bearing. In the interstitial spaces of 2-day recovery muscle, ED1+ and Ia+ macrophages numbered 369 and 332/mm2, respectively, compared with 12 and 72/mm2, respectively, in control soleus. After 7 days of reloading, the number of ED1+ cells was similar to that of control. Ia+ macrophages decreased to 240/mm2 at 4 days but after 7 days rose above control values to 429/mm2. ED2+ macrophages in 4- and 7-day reloaded soleus increased 70-80% in the interstitial spaces compared with control but were not observed to infiltrate necrotic muscle fibers at any time points. Immunohistochemistry and immunoblots using a monoclonal anti-dMHC antibody demonstrate a greater proportion of myofibers expressing dMHC isoforms after 4…
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After the initial pro-inflammatory phase, a switch to an M2 phenotype and resolution of inflammation occurs with the initial differentiation of muscle satellite cells.
“Following the initial pro-inflammatory phase, a switch to an M2 macrophage phenotype and resolution of the inflammatory response has been shown to occur with the initial stages of differentiation of muscle satellite cells into differentiated skeletal muscle cells [123].”
From Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine (2012) · cites this paper as [123]
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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
“Studies in rat have shown that ED1+ MPs are associated with muscle necrosis, whereas ED2+ (CD163) MPs, regarded as “resident MPs”, invade muscle once necrosis has been removed and are associated with regenerative myofibers (17,28).”
BackgroundInflammatory processes in muscle injury and repair.
Tidball, J. (2005) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00454.2004 · Cited by 1,392 · see citing works
“1) and then decline in number at the end of the phagocytic stage (82).”
BackgroundSelf-citationRegulatory 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
Regulation of Muscle Growth and Regeneration by the Immune System
Tidball, J. G. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2016.150 · Cited by 740 · see citing works
Self-citationMuscle injuries and repair: current trends in research.
Huard, J., Li, Y., & Fu, F. H. (2002) · Journal of Bone and Joint Surgery. American volume · doi:10.2106/00004623-200205000-00022 · Cited by 688 · see citing works
Macrophages in inflammation, repair and regeneration
Oishi, Y., & Manabe, I. (2018) · International Immunology · doi:10.1093/intimm/dxy054 · Cited by 645 · see citing works
Villalta, S. A., Nguyen, H. X., Deng, B., Gotoh, T., & Tidball, J. G. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn376 · Cited by 512 · 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-citationIL-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
“The number of CD163 macrophages begins to increase in regenerative muscle at ∼2 d postinjury and reaches maximum levels at ∼4 d (7, 10).”
BackgroundSelf-citationMalm, C., Nyberg, P., Engström, M., Sjödin, B., Lenkei, R., Ekblom, B., & Lundberg, I. (2000) · Journal of Physiology · doi:10.1111/j.1469-7793.2000.00243.x · Cited by 409 · see citing works
“The appearance of CD56+ muscle cells before macrophage infiltration in both groups (Table 5) indicates a process of regeneration rather than necrosis (St Pierre & Tidball, 1994).”
BackgroundMechanisms of Muscle Injury, Repair, and Regeneration
Tidball, J. (2011) · Comprehensive Physiology · doi:10.1002/j.2040-4603.2011.tb00387.x · Cited by 401 · see citing works
Self-citationRole of Inflammation in Muscle Homeostasis and Myogenesis
Costamagna, D., Costelli, P., Sampaolesi, M., & Penna, F. (2015) · Mediators of Inflammation · doi:10.1155/2015/805172 · Cited by 390 · see citing works
Tidball, J. G., & Wehling‐Henricks, M. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2006.118265 · Cited by 375 · see citing works
“Muscle reloading when returned to normal ambulation causes muscle inflammation, fibre injury and membrane lesions in soleus muscle fibres (Krippendorf & Riley, 1993; St Pierre & Tidball, 1994; Kasper, 1995; Tidball et al. 1999).”
BackgroundResultInfluentialSelf-citationThe Cytokine Response to Physical Activity and Training
Moldoveanu, A., Shephard, R., & Shek, P. (2001) · Sports Medicine · doi:10.2165/00007256-200131020-00004 · Cited by 339 · see citing works
“At the molecular level, thiol proteases such as calpain mediate protein degradation of muscle myofibrillar complexes, with depletion of sarcomeric Disruption of striation pattern [158] Mild neutrophil activation but not cause of tissue damage [159] Reduced heavy-light filament overlap resulting in decreased contractil…”
BackgroundRegeneration of skeletal muscle
Turner, N., & Badylak, S. (2011) · Cell and Tissue Research · doi:10.1007/s00441-011-1185-7 · Cited by 308 · see citing works
“…by an increase in nonphagocytic (M2) macrophages that peak in numbers at ~4 days following injury and persist until well into the remodeling phase of skeletal muscle repair (Brunelli and Rovere-Querini 2008; Frenette et al. 2000; St Pierre and Tidball 1994a; Tidball 1995; Chazaud et al. 2009).”
BackgroundSkeletal 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
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-citationMacintyre, D. L., Reid, W., & Mckenzie, D. (1995) · Sports Medicine · doi:10.2165/00007256-199520010-00003 · Cited by 275 · see citing works
Dual and Beneficial Roles of Macrophages During Skeletal Muscle Regeneration
Chazaud, B., Brigitte, M., Yacoub-Youssef, H., Arnold, L., Gherardi, R., Sonnet, C., Lafuste, P., & Chrétien, F. (2009) · Exercise and sport sciences reviews · doi:10.1097/jes.0b013e318190ebdb · Cited by 238 · see citing works
“Macrophages have been known for a long time to be associated with skeletal muscle regeneration (16,25) and several in vivo studies have shown that they actually participate in the muscle repair process.”
BackgroundModulation of myostatin expression during modified muscle use
Wehling, M., Cai, B.-Y., & Tidball, J. (2000) · The FASEB Journal · doi:10.1096/fasebj.14.1.103 · Cited by 238 · see citing works
Self-citationTeixeira, C. F., Zamuner, S., Zuliani, J., Fernandes, C. M., Cruz-Hofling, M. A., Fernandes, I., Chaves, F., & Gutiérrez, J. (2003) · Muscle and Nerve · doi:10.1002/mus.10453 · Cited by 223 · see citing works
Macrophages accumulate in the early phase of tendon–bone healing
Kawamura, S., Ying, L., Kim, H.-J., Dynybil, C., & Rodeo, S. A. (2005) · Journal of Orthopaedic Research · doi:10.1016/j.orthres.2005.01.014.1100230627 · Cited by 207 · 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
“The distribution of the different macrophage subsets in DMD was in accordance with the classic ED1/ED2 paradigm in rats, in which different macrophage phenotypes are associated with different stages of muscle repair (40, 41).”
BackgroundMethodFishman, J. M., Lowdell, M. W., Urbani, L., Ansari, T., Burns, A. J., Turmaine, M., North, J., Sibbons, P., Seifalian, A. M., Wood, K. J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1213228110 · Cited by 199 · see citing works
Cytokines in exertion-induced skeletal muscle injury
Cannon, J., & Pierre, B. S. S. (1998) · Molecular and Cellular Biochemistry · doi:10.1023/a:1006828425418 · Cited by 191 · see citing works
“Connective tissue concentrations of the ED2 + macrophage subpopulation reach peak levels later than the ED1 + macrophages, around post-injury day 4 in reloaded muscle [45].”
BackgroundAltered Macrophage Phenotype Transition Impairs Skeletal Muscle Regeneration
Wang, H., Melton, D. W., Porter, L., Sarwar, Z. U., McManus, L. M., & Shireman, P. K. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2013.12.020 · Cited by 198 · see citing works
“In rats, M1 and M2 subsets were defined as ED1þ and ED2þ macrophages, respectively.(33,34) Although these studies suggest that different monocyte/macrophage subsets are associated with different stages of skeletal muscle regeneration, the kinetics and influence of different monocyte/macrophage subsets in skeletal musc…”
BackgroundRethinking 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
Nguyen, H. X., & Tidball, J. (2003) · Journal of Physiology · doi:10.1111/j..2002.00125.x · Cited by 181 · see citing works
“ED1 antigen is expressed by phagocytic macrophages that are early invaders of injured muscle (Dijkstra et al. 1985; St Pierre & Tidball, 1994).”
BackgroundSelf-citationBarbe, M., Barr, A., Gorzelany, I., Amin, M., Gaughan, J., & Safadi, F. (2003) · Journal of Orthopaedic Research · doi:10.1016/s0736-0266(02)00086-4 · Cited by 162 · see citing works
ED2+ 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
Neutrophils and macrophages accumulate sequentially following Achilles tendon injury
Marsolais, D., Côt́e, C., & Frenette, J. (2001) · Journal of Orthopaedic Research · doi:10.1016/s0736-0266(01)00031-6 · Cited by 161 · see citing works
Przybyla, B., Gurley, C., Harvey, J. F., Bearden, E., Kortebein, P., Evans, W., Sullivan, D., Peterson, C. A., & Dennis, R. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2005.12.007 · Cited by 158 · see citing works
Muscle injuries and repair: the role of prostaglandins and inflammation.
Prisk, V., & Huard, J. (2003) · Histology and Histopathology · doi:10.14670/hh-18.1243 · Cited by 158 · 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
“…predominant inflammatory cell type within the injured area and several findings suggest that macrophages play a direct role not only in removing tissue debris, but also in the activation of stem cell-mediated muscle repair and regeneration (St. Pierre and Tidball, 1994; Arnold et al., 2007) (Fig.”
InfluentialThe Basis of Muscle Regeneration
Musarò, A. (2014) · Advances in Biology · doi:10.1155/2014/612471 · Cited by 138 · see citing works
Brown, S., Child, R., Day, S. H., & Donnelly, A. (1997) · European Journal of Applied Physiology and Occupational Physiology · doi:10.1007/s004210050174 · Cited by 142 · see citing works
“The macrophage response observed in injured muscle has been characterised by an infiltration of ED1+ and Ia+ macrophage sub-populations, and later by an accumulation of ED2+ cells (Stauber et al. 1988; St. Pierre and Tidball 1994).”
BackgroundRegulatory T cells and skeletal muscle regeneration
Schiaffino, S., Pereira, M. G., Ciciliot, S., & Rovere-Querini, P. (2017) · The FEBS Journal · doi:10.1111/febs.13827 · Cited by 136 · see citing works
Muire, P. J., Mangum, L. H., & Wenke, J. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01056 · Cited by 134 · see citing works
“anti-inflammatory macrophages are present from 2 to 7 dpi, peaking at 4 dpi (35) (Figure 2).”
BackgroundFibroadipogenic progenitors are responsible for muscle loss in limb girdle muscular dystrophy 2B
Hogarth, M., Defour, A., Lazarski, C., Gallardo, E., Díaz-Manera, J., Partridge, T., Nagaraju, K., & Jaiswal, J. (2019) · Nature Communications · doi:10.1038/s41467-019-10438-z · Cited by 133 · see citing works
The immune system and the repair of skeletal muscle.
Brunelli, S., & Rovere-Querini, P. (2008) · Pharmacological Research · doi:10.1016/j.phrs.2008.06.008 · Cited by 132 · see citing works
Macrophage invasion does not contribute to muscle membrane injury during inflammation
Tidball, J., Berchenko, E., & Frenette, J. (1999) · Journal of Leukocyte Biology · doi:10.1002/jlb.65.4.492 · Cited by 132 · see citing works
“We have focused on invading ED11 macrophages because they reach peak concentration in muscle at the stage when histologically discernible muscle damage is most pronounced [15].”
BackgroundMethodInfluentialSelf-citationShared 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
“Conversely, the CD68low/CD163+ M2 macrophages reached peak numbers by 4 days post-injury, coinciding with early stages of muscle differentiation and were closely associated with the surfaces of regenerative myotubes and nascent muscle fibers (St Pierre and Tidball, 1994).”
BackgroundSelf-citationAge-dependent alteration in muscle regeneration: the critical role of tissue niche
Barberi, L., Scicchitano, B. M., Rossi, M. D., Bigot, A., Duguez, S., Wielgosik, A., Stewart, C., McPhee, J., Conte, M., Narici, M., et al. (2013) · Biogerontology (Dordrecht) · doi:10.1007/s10522-013-9429-4 · Cited by 128 · see citing works
“In contrast to M1, M2 cells tune the inflammatory response, scavenge debris and promote angiogenesis, tissue remodeling and repair (St. Pierre and Tidball 1994; Krippendorf and Riley 1993; Tidball and Wehling-Henricks 2007): their absence causes a delay in muscle growth and inhibits muscle…”
BackgroundResultInfluentialIbuprofen inhibits skeletal muscle hypertrophy in rats.
Soltow, Q. A., Betters, J., Sellman, J., Lira, V., Long, J. H. D., & Criswell, D. (2006) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000218142.98704.66 · Cited by 117 · see citing works
Biologic scaffold remodeling in a dog model of complex musculoskeletal injury.
Turner, N., Badylak, J. S., Weber, D., & Badylak, S. (2012) · Journal of Surgical Research · doi:10.1016/j.jss.2011.11.1029 · Cited by 114 · see citing works
Araya, R., Eckardt, D., Maxeiner, S., Krüger, O., Theis, M., Willecke, K., & Sáez, J. (2005) · Journal of Cell Science · doi:10.1242/jcs.01553 · Cited by 111 · see citing works
Complement activation promotes muscle inflammation during modified muscle use.
Frenette, J., Cai, B.-Y., & Tidball, J. (2000) · American Journal of Pathology · doi:10.1016/s0002-9440(10)65081-x · Cited by 108 · see citing works
“Inflammation, fiber necrosis, edema, and complement activation were measured after muscle unloading and in animals experiencing muscle reloading for 2, 6, or 24 hours because that time course encompasses that in which extensive inflammation and fiber damage have been shown to occur.(2) The results of this study suppor…”
ResultSelf-citationA Perspective on Immunomodulation and Tissue Repair
Mokarram, N., & Bellamkonda, R. V. (2013) · Annals of Biomedical Engineering · doi:10.1007/s10439-013-0941-0 · Cited by 114 · see citing works
Frenette, J., & Tidball, J. (1998) · American Journal of Physiology - Cell Physiology · doi:10.1152/ajpcell.1998.275.3.c818 · Cited by 104 · see citing works
Self-citationMetabolic regulation of macrophages during tissue repair: insights from skeletal muscle regeneration
Juban, G., & Chazaud, B. (2017) · FEBS Letters · doi:10.1002/1873-3468.12703 · Cited by 103 · see citing works
Barr, A., & Barbe, M. (2004) · Journal of Electromyography & Kinesiology · doi:10.1016/j.jelekin.2003.09.008 · Cited by 95 · see citing works
Frenette, J., St-Pierre, M., Côt́e, C., Mylona, E., & Pizza, F. (2002) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00189.2001 · Cited by 94 · see citing works
“The possibility that invading inflammatory cells contribute to muscle injury in the model of HS is indirectly supported by the observation that significant elevations in muscle neutrophil and macrophage concentrations occur at time points when ultrastructural signs of injury are exacerbated and fiber necrosis occurs (…”
BackgroundUnloading of juvenile muscle results in a reduced muscle size 9 wk after reloading.
Mozdziak, P., Pulvermacher, P. M., & Schultz, E. (2000) · Journal of applied physiology · doi:10.1152/jappl.2000.88.1.158 · Cited by 93 · see citing works
“Macrophages secrete substances, such as plateletderived growth factor, basic fibroblast growth factor, and insulin-like growth factor, that can stimulate satellite cell mitotic activity (5, 31).”
BackgroundNull Mutation of gp91phox Reduces Muscle Membrane Lysis During Muscle Inflammation in Mice
Nguyen, H. X., & Tidball, J. (2003) · Journal of Physiology · doi:10.1113/jphysiol.2003.051912 · Cited by 87 · see citing works
“Macrophages are also frequently found in the highest concentrations in muscle that is in the process of growth or regeneration that results from modified muscle loading in vivo (St Pierre & Tidball, 1994; Merly et al. 1999) or muscle grafting (Lescaudron et al. 1999).”
BackgroundSelf-citationNguyen, H. X., & Tidball, J. (2003) · Journal of Physiology · doi:10.1113/jphysiol.2003.040907 · Cited by 86 · see citing works
“Reloading for 24 h by return to normal ambulation has been shown previously to produce muscle inflammation, fibre injury and membrane lesions in soleus muscle fibres (Krippendorf & Riley, 1993, 1994; St Pierre & Tidball, 1994; Kasper, 1995; Tidball et al. 1999a).”
BackgroundMethodSelf-citationMuscle regeneration during hindlimb unloading results in a reduction in muscle size after reloading.
Mozdziak, P., Pulvermacher, P. M., & Schultz, E. (2001) · Journal of applied physiology · doi:10.1152/jappl.2001.91.1.183 · Cited by 86 · see citing works
Regulation of mandibular postures: mechanisms and clinical implications.
Woda, A., Pionchon, P., & Palla, S. (2001) · Critical Reviews in Oral Biology and Medicine · doi:10.1177/10454411010120020601 · Cited by 85
Bosurgi, L., Manfredi, A., & Rovere-Querini, P. (2011) · Front. Immun. · doi:10.3389/fimmu.2011.00062 · Cited by 80 · see citing works
“This is due to a unique feature of macrophages, i.e., their ability to perceive signals heralding ongoing tissue injury and to broadcast the news to cells suited at regenerating the tissue such as stem and progenitor cells.”
BackgroundSex differences in leukocyte invasion in injured murine skeletal muscle.
Schneider, B. S. P., Correia, L. A., & Cannon, J. G. (1999) · Research in Nursing and Health · doi:10.1002/(sici)1098-240x(199906)22:3 · Cited by 80 · see citing works
Hirata, K., Mitoma, H., Ueno, N., He, J.-W., & Kawabuchi, M. (1999) · Journal of Neurocytology · doi:10.1023/a:1007012916530 · Cited by 77 · see citing works
Association of IGF‐I and IGF‐II with myofiber regeneration in vivo
Keller, H. L., Schneider, B. S. P., Eppihimer, L. A., & Cannon, J. G. (1999) · Muscle and Nerve · doi:10.1002/(sici)1097-4598(199903)22:3 · Cited by 77 · see citing works
Regrowth of skeletal muscle atrophied from inactivity.
Machida, S., & Booth, F. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000106175.24978.84 · Cited by 77 · see citing works
“(43,65), inducing an inflammatory response within skeletal”
BackgroundNguyen, H. X., Lusis, A., & Tidball, J. (2005) · Journal of Physiology · doi:10.1113/jphysiol.2005.085506 · Cited by 75 · see citing works
“Reloading for 24 h by returning to normal ambulation produces muscle inflammation, fibre injury and membrane lesions in soleus muscle fibres (Krippendorf & Riley, 1993; St Pierre & Tidball, 1994; Kasper, 1995; Tidball et al. 1999).”
BackgroundSelf-citationBrophy, R., Kovacevic, D., Imhauser, C., Stasiak, M., Bedi, A., Fox, A. J. S., Deng, X.-H., & Rodeo, S. (2011) · Journal of Bone and Joint Surgery. American volume · doi:10.2106/jbjs.i.00933 · Cited by 73 · see citing works
Conti, G., Scarpini, E., Baron, P., Livraghi, S., Tiriticco, M., Bianchi, R., Vedeler, C., & Scarlato, G. (2002) · Journal of Neurological Sciences · doi:10.1016/s0022-510x(01)00684-0 · Cited by 73 · see citing works
Phua, W. W. T., Wong, M. X. Y., Liao, Z., & Tan, N. S. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19051425 · Cited by 72 · see citing works
“The damaged tissues are then cleared by infiltrated immune cells, such as macrophages and neutrophils, through phagocytosis [146].”
BackgroundJames, G., Sluka, K., Blomster, L. V., Hall, L. M., Schmid, A., Shu, C. C., Little, C., Melrose, J., & Hodges, P. (2018) · European spine journal · doi:10.1007/s00586-018-5652-7 · Cited by 72 · see citing works
“M1 and M2 have specialized roles in muscle regeneration [39, 40].”
BackgroundReloading of atrophied rat soleus muscle induces tenascin-C expression around damaged muscle fibers.
Flück, M., Chiquet, M., Schmutz, S., Mayet-Sornay, M., & Desplanches, D. (2003) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.00060.2002 · Cited by 70 · see citing works
“4, arrowheads), which may reflect internalized myonuclei of regenerating fibers or may indicate infiltrating immune cells (7, 50, 61).”
Backgroundvan der Velden, J. L., Langen, R., Kelders, M., Willems, J., Wouters, E., Janssen-Heininger, Y., & Schols, A. (2007) · American Journal of Physiology - Cell Physiology · doi:10.1152/ajpcell.00504.2006 · Cited by 68 · see citing works
“Previous studies have shown that muscle reloading induces fiber injury and inflammation (32, 52).”
Reidy, P., McKenzie, A. I., Mahmassani, Z., Petrocelli, J. J., Nelson, D. B., Lindsay, C. C., Gardner, J. E., Morrow, V. R., Keefe, A., Huffaker, T., et al. (2019) · American Journal of Physiology. Endocrinology and Metabolism · doi:10.1152/ajpendo.00422.2018 · Cited by 67 · see citing works
Quantitative assessment of the tissue response to films of hyaluronan derivatives.
Campoccia, D., Hunt, J. A., Doherty, P., Zhong, S. P., O'Regan, M., Benedetti, L., & Williams, D. F. (1996) · Biomaterials · doi:10.1016/0142-9612(96)84670-9 · Cited by 67
Roche, J. A., Lovering, R., Roche, R., Ru, L. W., Reed, P., & Bloch, R. (2010) · American Journal of Physiology - Cell Physiology · doi:10.1152/ajpcell.00122.2009 · Cited by 66 · see citing works
Apoptosis of macrophages during the resolution of muscle inflammation
Tidball, J., & Pierre, B. S. S. (1996) · Journal of Leukocyte Biology · doi:10.1002/jlb.59.3.380 · Cited by 66 · see citing works
“4) is similar to that reported previously [7] in that peak invasion occurred at 2 days of reloading following hindlimb suspension.”
BackgroundMethodResultInfluentialSelf-citationMirzoev, T. M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21217940 · Cited by 65 · see citing works
Impaired recovery of dysferlin-null skeletal muscle after contraction-induced injury in vivo
Roche, J. A., Lovering, R., & Bloch, R. (2008) · NeuroReport · doi:10.1097/wnr.0b013e328311ca35 · Cited by 64 · see citing works
“Myogenesis We assessed myogenesis by counting the number of centrally nucleated fibers (CNFs) [16,17] and the number of myofibers expressing the developmental isoforms of the heavy chain of myosin (dMHC) [18].”
Interactions between muscle and the immune system during modified musculoskeletal loading.
Tidball, J. (2002) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-200210001-00012 · Cited by 64 · see citing works
Self-citationThe Repair of Skeletal Muscle Requires Iron Recycling through Macrophage Ferroportin
Corna, G., Caserta, I., Monno, A., Apostoli, P., Manfredi, A. A., Camaschella, C., & Rovere-Querini, P. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1501417 · Cited by 63 · see citing works
Ovarian hormone status and skeletal muscle inflammation during recovery from disuse in rats
McClung, J. M., Davis, J. M., & Carson, J. A. (2007) · Experimental Physiology · doi:10.1113/expphysiol.2006.035071 · Cited by 63 · see citing works
“ED1+ macrophage concentrations decline in conjunction with the completion of tissue necrosis occurring during reloading recovery (St Pierre & Tidball, 1994a).”
BackgroundThe Skeletal Muscle as an Active Player Against Cancer Cachexia
Penna, F., Ballarò, R., Beltrà, M., Lucia, S. D., Garcia‐Castillo, L., & Costelli, P. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00041 · Cited by 69 · see citing works
“…the PI3K-Akt-mTOR signaling is poised toward activation in mice implanted with the C26 tumor (Penna et al., 2010a), while protein synthesis rates are unchanged with respect to controls in rats hosting the Yoshida AH-130 hepatoma or the MCA sarcoma (Tessitore et al., 1987; Stallion et al., 1995).”
BackgroundMorphological changes in rat hindlimb muscle fibres during recovery from disuse atrophy.
Itai, Y., Kariya, Y., & Hoshino, Y. (2004) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2004.01271.x · Cited by 59 · see citing works
Part III • Chapter 8 – Acute phase immune responses in exercise
Cannon, J., & Blumberg, J. (2000) · Elsevier eBooks · doi:10.1016/b978-044482650-3/50008-0 · Cited by 59 · see citing works
Inflammation during post-injury skeletal muscle regeneration.
Panci, G., & Chazaud, B. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.05.031 · Cited by 58 · see citing works
Diaphragm injury in individuals with airflow obstruction.
Macgowan, N. A., Evans, K. G., Road, J. D., & Reid, W. (2001) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.163.7.2001042 · Cited by 58 · see citing works
The role of inflammation modulation in dental pulp regeneration.
Zaky, S., Shehabeldin, M., Ray, H., & Sfeir, C. (2021) · European Cells & Materials · doi:10.22203/ecm.v041a13 · Cited by 56 · see citing works
Ultrasound Modulates the Inflammatory Response and Promotes Muscle Regeneration in Injured Muscles
Nagata, K., Nakamura, T., Fujihara, S., & Tanaka, E. (2013) · Annals of Biomedical Engineering · doi:10.1007/s10439-013-0757-y · Cited by 56 · see citing works
Bajotto, G., & Shimomura, Y. (2006) · Journal of Nutritional Science and Vitaminology · doi:10.3177/jnsv.52.233 · Cited by 54 · see citing works
Postpartum Symptoms After Antepartum Bed Rest
Maloni, J. A., & Park, S. (2005) · Journal of Obstetric, Gynecologic & Neonatal Nursing · doi:10.1177/0884217504274416 · Cited by 53 · see citing works
“Fatigue among women after bed rest could be due to musculoskeletal and cardiovascular deconditioning, postpartum sleep interruptions, depression, or a combination of these factors (Affonso, Lovett, Paul, & Sheptak, 1990; Gard- March/April 2005 JOGNN 167 TABLE 2 Mean Number of Postpartum Symptoms Reported by 106 Women…”
InfluentialThe Impact of Immune Cells on the Skeletal Muscle Microenvironment During Cancer Cachexia
VanderVeen, B. N., Murphy, E. A., & Carson, J. A. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.01037 · Cited by 52 · see citing works
Transplanted Mesoangioblasts Require Macrophage IL-10 for Survival in a Mouse Model of Muscle Injury
Bosurgi, L., Corna, G., Vezzoli, M., Touvier, T., Cossu, G., Manfredi, A., Brunelli, S., & Rovere-Querini, P. (2012) · Journal of Immunology · doi:10.4049/jimmunol.1102680 · Cited by 52 · see citing works
Nonmyogenic Cells in Skeletal Muscle Regeneration
Paylor, B., Natarajan, A., Zhang, R.-H., & Rossi, F. (2011) · Current Topics in Developmental Biology · doi:10.1016/b978-0-12-385940-2.00006-1 · Cited by 49 · see citing works
Myeloid Hypoxia-Inducible Factor-1α Is Essential for Skeletal Muscle Regeneration in Mice
Scheerer, N., Dehne, N., Stockmann, C., Swoboda, S., Baba, H., Neugebauer, A., Johnson, R., & Fandrey, J. (2013) · Journal of Immunology · doi:10.4049/jimmunol.1103779 · Cited by 49 · see citing works
“to M2 populations that normally induces the change from the proliferative stage to the differentiation phase of muscle regeneration during the period of days 2 and 4 after injury (6, 33).”
BackgroundResultWhite, J., Confides, A. L., Moore-Reed, S. D., Hoch, J., & Dupont-Versteegden, E. (2015) · Experimental Gerontology · doi:10.1016/j.exger.2015.02.007 · Cited by 48 · see citing works
“Muscle reloading after atrophy has been shown to be associated with early damage and a transient inflammatory response (Oishi et al., 2008; St Pierre and Tidball, 1994; Tidball and Wehling-Henricks, 2007) and this inflammatory response seems critical for full recovery as a decrease in macrophages…”
BackgroundFlück, M., Däpp, C., Schmutz, S., Wit, E. C., & Hoppeler, H. H. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00050.2005 · Cited by 43 · see citing works
Stem Cell Transplantation for Muscular Dystrophy: The Challenge of Immune Response
Maffioletti, S., Noviello, M., English, K., & Tedesco, F. S. (2014) · BioMed Research International · doi:10.1155/2014/964010 · Cited by 46 · see citing works
The Myotendinous Junction—A Vulnerable Companion in Sports. A Narrative Review
Jakobsen, J., & Krogsgaard, M. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.635561 · Cited by 45 · see citing works
Nitric oxide synthase inhibition reduces muscle inflammation and necrosis in modified muscle use
Pizza, F., Hernandez, I. J., & Tidball, J. (1998) · Journal of Leukocyte Biology · doi:10.1002/jlb.64.4.427 · Cited by 45 · see citing works
“Previous investigations have shown that this technique of modifying muscle loading results in significant muscle inflammation and necrosis [1, 2, 6, 37].”
BackgroundMethodResultInfluentialSelf-citationMcLennan, I. S., & Koishi, K. (1997) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199702)208:2 · Cited by 45 · see citing works
Transcriptional reprogramming during reloading of atrophied rat soleus muscle
Flück, M., Schmutz, S., Wittwer, M., Hoppeler, H., & Desplanches, D. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00833.2004 · Cited by 44 · see citing works
Inactivity: Symptoms Associated With Gastrocnemius Muscle Disuse During Pregnancy
Maloni, J. A., & Schneider, B. S. P. (2002) · AACN Clinical Issues: Advanced Practice in Acute and Critical Care · doi:10.1097/00044067-200205000-00010 · Cited by 43 · see citing works
Activity‐induced fiber regeneration in rat soleus muscle
Wanek, L., & Snow, M. H. (2000) · The Anatomical Record · doi:10.1002/(sici)1097-0185(20000201)258:2 · Cited by 43 · see citing works
- Authors
- St Pierre, B. A., & Tidball, J. G.
- Affiliations
- School of Nursing, Department of Physiological Science, University of California, Los Angeles 90024–1527.
- University of California, Los Angeles (US)
- ORCID
- Tidball, J. G.
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 1994-07-01
- Volume
- 77
- Issue
- 1
- Pages
- 290-297
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- OpenAlex
- W1806632103
- Cited by
- 251
- References
- 0
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 5 · 2022: 11 · 2021: 10 · 2020: 10 · 2019: 9 · 2018: 12 · 2017: 8 · 2016: 9 · 2015: 8 · 2014: 11 · 2013: 7 · 2012: 13
- FWCI
- 1.63
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ar040343-12, 1f31nr006503-01)
- National Institute of Nursing Research (NR 06503)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR-40343)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology › Spaceflight effects on biology
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
- Keywords
- macrophage subpopulations, soleus muscle, hindlimb unloading, muscle unloading, muscle reloading, muscle necrosis, muscle regeneration, ED1 macrophages, weight-bearing recovery
- MeSH terms
- Acid Phosphatase, Animals, Animals, Newborn, Body Weight, Female, Hindlimb, Immunohistochemistry, Macrophages, Organ Size, Immunoblotting, Myosin Subfragments, Rats, Wistar, Gravity, Altered, Muscle, Skeletal, Muscle Fibers, Skeletal, Rats
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