Mitochondrial biogenesis during skeletal muscle regeneration
Abstract
Myogenesis requires energy production for the execution of a number of regulatory and biosynthesis events. We hypothesized that mitochondrial biogenesis would be stimulated during skeletal muscle regeneration. Tibialis anterior muscles of male Sprague-Dawley rats were injected with 0.75% bupivacaine and removed at 3, 5, 7, 10, 14, 21, or 35 days after injection ( n = 5–7/group). Two main periods emerged from the histochemical analyses of muscle sections and the expression of proliferating cell nuclear antigen, desmin, and creatine phosphokinase: 1) activation/proliferation of satellite cells ( days 3–14) and 2) differentiation into muscle fibers ( days 5–35). The onset of muscle differentiation was accompanied by a marked stimulation of mitochondrial biogenesis, as indicated by a nearly fivefold increase in citrate synthase activity and state 3 rate of respiration between days 5 and 10. Peroxisome proliferator-activated receptor-γ coactivator-1 (PGC-1) mRNA level and mitochondrial transcription factor A (mtTFA) protein level peaked on day 10 concurrently with the state 3 rate of respiration. Therefore, transcriptional activation by PGC-1 and mtTFA may be one of the mechanisms regulating mitochondrial biogenesis in regenerating skeletal muscle. Taken together, our results suggest that mitochondrial biogenesis may be an important regulatory event during muscle regeneration.
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Increased mitochondrial volume density has been detected after endurance exercise and in regenerating skeletal muscle.
“Increased mitochondrial volume density has been detected after endurance exercise (28,29) and in regenerating skeletal muscle (30).”
From Increased mitochondrial mass in mitochondrial myopathy mice (2002) · cites this paper as [30]
Cites
Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)80611-x · Cited by 4,139 · see citing works
A Flexible System of Enzymatic Analysis
Lowry, O. H., & Passonneau, J. V. (1972) · Elsevier eBooks · doi:10.1016/b978-0-12-457950-7.x5001-3 · Cited by 4,050 · see citing works
Virbasius, J. V., & Scarpulla, R. C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.4.1309 · Cited by 819 · see citing works
Invited Review: Contractile activity-induced mitochondrial biogenesis in skeletal muscle
Hood, D. A. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.3.1137 · Cited by 692 · see citing works
Biswas, G., Adebanjo, O. A., Freedman, B. D., Anandatheerthavarada, H. K., Vijayasarathy, C., Zaidi, M., Kotlikoff, M., & Avadhani, N. G. (1999) · The EMBO Journal · doi:10.1093/emboj/18.3.522 · Cited by 369 · see citing works
What regulates mitochondrial DNA copy number in animal cells?
Moraes, C. T. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02238-7 · Cited by 299 · see citing works
Growth factors in skeletal muscle regeneration
Husmann, I., Soulet, L., Gautron, J., Martelly, I., & Barritault, D. (1996) · Cytokine & Growth Factor Reviews · doi:10.1016/s1359-6101(96)00029-9 · Cited by 274 · see citing works
What does chronic electrical stimulation teach us about muscle plasticity?
Pette, D., & Vrbov�, G. (1999) · Muscle & Nerve · doi:10.1002/(sici)1097-4598(199906)22:6 · Cited by 246 · see citing works
Reichmann, H., Hoppeler, H. H., Mathieu-Costello, O. A., Bergen, F., & Pette, D. (1985) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00581484 · Cited by 226 · see citing works
Rantanen, J., Hurme, T., Lukka, R., Heino, J., & Kalimo, H. (1995) · PubMed · Cited by 223 · see citing works
Mitochondrial biogenesis during cellular differentiation
Moyes, C. D., Mathieu-Costello, O. A., Tsuchiya, N., Filburn, C. R., & Hansford, R. G. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.272.4.c1345 · Cited by 222 · see citing works
Rochard, P., Rodier, A., Casas, F., Cassar‐Malek, I., Marchal-Victorion, S., Daury, L., Wrutniak‐Cabello, C., & Cabello, G. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.4.2733 · Cited by 210 · see citing works
Herzig, R. P., Scacco, S., & Scarpulla, R. C. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.17.13134 · Cited by 197 · see citing works
Hall-Craggs, E. C. B. (1974) · Experimental Neurology · doi:10.1016/0014-4886(74)90176-9 · Cited by 169 · see citing works
Gordon, J. W., Rungi, A. A., Inagaki, H., & Hood, D. A. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.1.389 · Cited by 160 · see citing works
Analysis of inflammatory cells and complement C3 in bupivacaine‐induced myonecrosis
Orimo, S., Hiyamuta, E., Arahata, K., et al. (1991) · Muscle & Nerve · doi:10.1002/mus.880140605 · Cited by 155 · see citing works
Calcineurin Co-regulates Contractile and Metabolic Components of Slow Muscle Phenotype
Bigard, X. A., Sanchez, H., Zoll, J., Matéo, P., Rousseau, V., Veksler, V., & Ventura‐Clapier, R. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000430200 · Cited by 144 · see citing works
Regulation of creatine kinase induction in differentiating mouse myoblasts.
Chamberlain, J. S., Jaynes, J. B., & Hauschka, S. D. (1985) · Molecular and Cellular Biology · doi:10.1128/mcb.5.3.484 · Cited by 136 · see citing works
Desmin and vimentin in regenerating muscles
Bornemann, A., & Schmalbruch, H. (1992) · Muscle & Nerve · doi:10.1002/mus.880150104 · Cited by 135 · see citing works
Interactions between bioenergetics and mitochondrial biogenesis
Leary, S. C., Battersby, B. J., Hansford, R. G., & Moyes, C. D. (1998) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00105-4 · Cited by 118 · see citing works
Calcium-dependent Regulation of Cytochromec Gene Expression in Skeletal Muscle Cells
Freyssenet, D. G., Carlo, M. D., & Hood, D. A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.14.9305 · Cited by 107 · see citing works
Self-citationGeorge‐Weinstein, M., Foster, R. F., Gerhart, J. V., & Kaufman, S. J. (1993) · Developmental Biology · doi:10.1006/dbio.1993.1071 · Cited by 104 · see citing works
Molecular Basis of Skeletal Muscle Regeneration
Chambers, R. L., & McDermott, J. C. (1996) · Canadian Journal of Applied Physiology · doi:10.1139/h96-014 · Cited by 93 · see citing works
Korzeniewski, B., & Mazat, J. (1996) · Biochemical Journal · doi:10.1042/bj3190143 · Cited by 92 · see citing works
Neuropathy and mortality in diabetes: Influence of pancreas transplantation
Navarro, X., Kennedy, W. R., Aeppli, D. M., & Sutherland, D. E. R. (1996) · Muscle & Nerve · doi:10.1002/(sici)1097-4598(199608)19:8 · Cited by 85 · see citing works
Concentration dependence of the dielectric constant in mixed oxides MxOyMp′Oq
Devine, R. A. B., & Revesz, A. G. (2001) · Journal of Applied Physics · doi:10.1063/1.1375806 · Cited by 76 · see citing works
Differentiation and proliferation of respiration-deficient human myoblasts
Herzberg, N. H., Zwart, R., Wolterman, R. A., Ruiter, J. P. N., Wanders, R. J. A., Bolhuis, P. A., & den Bogert, C. V. (1993) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/0925-4439(93)90091-e · Cited by 75 · see citing works
On the nature of the mitochondrial proton leak
Brown, G. C., & Brand, M. D. (1991) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(05)80187-2 · Cited by 74 · see citing works
Mitochondrial Biogenesis in Skeletal Muscle in Response to Endurance Exercises
Freyssenet, D. G., Berthon, P. M., & Denis, C. (1996) · Archives of Physiology and Biochemistry · doi:10.1076/apab.104.2.129.12878 · Cited by 72 · see citing works
Self-citationHall-Craggs, E. C. (1980) · PubMed · Cited by 71 · see citing works
Nuclear respiratory factors and the pathways of nuclear-mitochondrial interaction.
Scarpulla, R. (1996) · Trends in cardiovascular medicine · doi:10.1016/1050-1738(95)00129-8 · Cited by 70 · see citing works
Brown, J. M. C., Henriksson, J., & Salmons, S. (1989) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1989.0003 · Cited by 70 · see citing works
Inhibition of Mitochondrial Protein Synthesis Impaired C2C12 Myoblast Differentiation.
Hamai, N., Nakamura, M., & Asano, A. (1997) · Cell Structure and Function · doi:10.1247/csf.22.421 · Cited by 67 · see citing works
Assembly of the cellular powerhouse: current issues in muscle mitochondrial biogenesis.
Hood, D. A., Takahashi, M., Connor, M. K., & Freyssenet, D. G. (2000) · PubMed · Cited by 58 · see citing works
Self-citationMitochondrial creatine kinase activity alterations in skeletal muscle during long-distance running
Apple, F. S., & Rogers, M. A. (1986) · Journal of Applied Physiology · doi:10.1152/jappl.1986.61.2.482 · Cited by 57 · see citing works
Tissue-Specific Stability of Nuclear- and Mitochondrially Encoded mRNAs
Connor, M. K., Takahashi, M. T., & Hood, D. A. (1996) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1996.0369 · Cited by 52 · see citing works
Initiation of satellite cell replication in bupivacaine-induced myonecrosis
Saito, Y., & Nonaka, I. (1994) · Acta Neuropathologica · doi:10.1007/bf00293401 · Cited by 50 · see citing works
Molecular orbital wave functions for methane and silane
Carter, C. (1956) · Proceedings of the Royal Society of London A Mathematical and Physical Sciences · doi:10.1098/rspa.1956.0085 · Cited by 49 · see citing works
Korohoda, W., Pietrzkowski, Z. J., & Reiss, K. (1993) · PubMed · Cited by 44 · see citing works
Marsh, D. R., Criswell, D. S., Hamilton, M. T., et al. (1997) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1997.273.1.r353 · Cited by 43 · see citing works
Mitochondrial ATP production rate in 55 to 73‐year‐old men: effect of endurance training
Berthon, P. M., Freyssenet, D. G., Chatard, J., CASTELLS, J., Mujika, I., GEYSSANT, A., Guezennec, C. Y., & Denis, C. (1995) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1995.tb09908.x · Cited by 38 · see citing works
Self-citationSurvival of satellite cells following exposure to the local anesthetic bupivacaine (Marcaine)
Hall-Craggs, E. C. B. (1980) · Cell and Tissue Research · doi:10.1007/bf00219929 · Cited by 36 · see citing works
Expression of creative kinase M and B mRNAs in treadmill trained rat skeletal muscle
Apple, F. S., & Billadello, J. J. (1994) · Life Sciences · doi:10.1016/0024-3205(94)00484-6 · Cited by 33 · see citing works
Changes in serum enzyme activities after injection of bupivacaine into rat tibialis anterior
Nosaka, K. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.81.2.876 · Cited by 22 · see citing works
The impairment of muscle blood vessels after intramuscular injection of local anaesthetics
Grim, M., Stingl, J., & Mr�zkov�, O. (1983) · The Histochemical Journal · doi:10.1007/bf01002960 · Cited by 17 · see citing works
Freyssenet, D. G., Berthon, P. M., GEYSSANT, A., & Denis, C. (1994) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(94)90182-1 · Cited by 17 · see citing works
Self-citationPéréon, Y., Navarro, J., Sorrentino, V., et al. (1996) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050271 · Cited by 15 · see citing works
Zidovudine (AZT) induced alterations in mitochondrial biogenesis in rat striated muscles
Freyssenet, D. G., DiCarlo, M., Escobar, P., et al. (1999) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-77-1-29 · Cited by 15 · see citing works
Self-citationProtein degradation in bupivacaine-treated muscles
Steer, J. H., & Mastaglia, F. L. (1986) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(86)90081-x · Cited by 12 · see citing works
Zidovudine (AZT) induced alterations in mitochondrial biogenesis in rat striated muscles
Freyssenet, D. G., DiCarlo, M., Escobar, P., et al. (1999) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y98-151 · Cited by 11 · see citing works
Self-citationOno, K., Abe, J., Kagawa, N., et al. (1993) · PubMed · Cited by 6 · see citing works
Calcium in bupivacaine-induced muscle necrosis.
Sadeh, M., Czyźewski, K., & Lz, S. (1985) · PubMed · Cited by 4 · see citing works
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Mitophagy is required for mitochondrial biogenesis and myogenic differentiation of C2C12 myoblasts
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- Authors
- Duguez, S., Féasson, L., Denis, C., & Freyssenet, D.
- Affiliations
- Laboratoire de Physiologie, Groupe Physiologie et Physiopathologie de l'Exercice et du Handicap Groupement d'Intérêt Public-E2S, Faculté de Médecine, 42023 Saint-Etienne, France
- Venue
- American Journal of Physiology-Endocrinology and Metabolism
- Publisher
- American Physiological Society
- Published
- 2002-04-01
- Volume
- 282
- Issue
- 4
- Pages
- E802-E809
- ISSN
- 0193-1849 (ISSN-L)
- 1522-1555
- OpenAlex
- W2157388197
- Cited by
- 183
- References
- 52
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 3 · 2023: 7 · 2022: 5 · 2021: 8 · 2020: 11 · 2019: 8 · 2018: 12 · 2017: 5 · 2016: 5 · 2015: 11 · 2014: 8 · 2013: 11 · 2012: 11
- FWCI
- 2.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Endocrinology and Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- mitochondrial biogenesis, skeletal muscle regeneration, satellite cells, PGC-1, TFAM, myogenesis, citrate synthase, state 3 respiration, proliferating cell nuclear antigen, desmin, creatine kinase
- MeSH terms
- Animals, Body Weight, Bupivacaine, Cell Differentiation, Cell Division, Citrate (si)-Synthase, Creatine Kinase, Desmin, DNA-Binding Proteins, Histocytochemistry, L-Lactate Dehydrogenase, Male, Mitochondria, Muscle Proteins, Necrosis, Nuclear Proteins, Organ Size, Oxygen Consumption, Regeneration, RNA, Messenger, Transcription Factors, Rats, Sprague-Dawley, Muscle, Skeletal, Proliferating Cell Nuclear Antigen, Mitochondrial Proteins, Phosphofructokinases, Rats
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