Ubiquitin expression is up-regulated in human and rat skeletal muscles during aging

Cai, Dongqing; Lee, K.K.H; Li, M; Tang, M.K; Chan, K.M

doi:10.1016/j.abb.2004.02.027

Cited by 65Muscle Physiology and DisordersUbiquitin and proteasome pathwaysMuscle metabolism and nutrition

Ubiquitin expression is up-regulated in human and rat skeletal muscles during aging

Cai, Dongqing, Lee, K.K.H, Li, M, Tang, M.K, Chan, K.M·2004·Archives of Biochemistry and Biophysics

DOI 10.1016/j.abb.2004.02.027

Open this paper in CoChat — free account

Abstract

In this study, we have used two-dimensional electrophoresis, protein sequencing, immunoblotting, and immunohistochemistry to identify proteins that were differentially expressed during aging in human and rat skeletal muscles. Ubiquitin was identified. It was expressed at high levels in old fast-twitch muscles but at low levels in young fast-twitch muscles. It was also discovered that exogenous ubiquitin could suppress the growth of C2C12 cells, in vitro. The reduction in C2C12 cell growth was not attributed to an increase in apoptosis but to an inhibition in cell cycle entry. Furthermore, it was possible to induce muscles to degenerate in vivo by injecting a high dose of exogenous ubiquitin into young healthy skeletal muscles. These results suggest that hyperactivity of the ubiquitin-proteasome pathway is involved in the aging process of fast-twitch muscles. In addition, ubiquitin-dependent growth suppression in satellite cells may be associated with the poor healing potential of old skeletal muscles.

Integrity signals

Registry

Crossref · 10.1016/j.abb.2004.02.027

Cites

62 of 62 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Ubiquitin is greater in quadriceps muscles of older humans (70-79 years) than young adults (20-29 years).
“ubiquitin was found to be greater in quadriceps muscles of older (70-79 yrs old) human subjects as compared to young adults (20-29 yrs old) (17).”
From Mitochondria initiate and regulate sarcopenia (2017) · cites this paper as [17]

A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays
Mosmann, T. (1983) · Journal of Immunological Methods · doi:10.1016/0022-1759(83)90303-4 · Cited by 56,104 · see citing works
SATELLITE CELL OF SKELETAL MUSCLE FIBERS
Mauro, A. (1961) · The Journal of Cell Biology · doi:10.1083/jcb.9.2.493 · Cited by 3,683 · see citing works
A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels
Oakley, B. R., Kirsch, D. R., & Morris, N. R. (1980) · Analytical Biochemistry · doi:10.1016/0003-2697(80)90470-4 · Cited by 3,248 · see citing works
STRUCTURE AND FUNCTIONS OF THE 20S AND 26S PROTEASOMES
Coux, O., Tanaka, K., & Goldberg, A. L. (1996) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.65.070196.004101 · Cited by 2,438 · see citing works
Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle
Yaffe, D., & Saxel, O. (1977) · Nature · doi:10.1038/270725a0 · Cited by 2,153 · see citing works
A Multifactorial Intervention to Reduce the Risk of Falling among Elderly People Living in the Community
Tinetti, M. E., Baker, D. I., McAvay, G., Claus, E. B., Garrett, P., Gottschalk, M., Koch, M. L., Trainor, K. M., & Horwitz, R. I. (1994) · New England Journal of Medicine · doi:10.1056/nejm199409293311301 · Cited by 2,135 · see citing works
What is the cause of the ageing atrophy?
Lexell, J. E., Taylor, C. C., & Sjöstróm, M. (1988) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(88)90132-3 · Cited by 2,080 · see citing works
Dynamic properties of mammalian skeletal muscles.
Close, R. I. (1972) · Physiological Reviews · doi:10.1152/physrev.1972.52.1.129 · Cited by 1,890 · see citing works
THE UBIQUITIN SYSTEM FOR PROTEIN DEGRADATION
Hershko, A., & Ciechanover, A. J. (1992) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.61.070192.003553 · Cited by 1,419 · see citing works
Ubiquitin, proteasomes, and the regulation of intracellular protein degradation
Hochstrasser, M. (1995) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(95)80031-x · Cited by 895 · see citing works
Plasticity of the Differentiated State
Blau, H. M., Pavlath, G. K., Hardeman, E. C., Chiu, C., Silberstein, L., Webster, S. G., Miller, S. C., & Webster, C. (1985) · Science · doi:10.1126/science.2414846 · Cited by 840 · see citing works
Isolation of a polypeptide that has lymphocyte-differentiating properties and is probably represented universally in living cells.
Goldstein, G., Scheid, M. P., Hämmerling, U., Schlesinger, D. H., Niall, H. D., & Boyse, E. A. (1975) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.72.1.11 · Cited by 752 · see citing works
Type of Fall and Risk of Hip and Wrist Fractures: The Study of Osteoporotic Fractures
Nevitt, M. C., & Cummings, S. R. (1993) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1993.tb07307.x · Cited by 571 · see citing works
THE UBIQUITIN-CONJUGATION SYSTEM
Jentsch, S. (1992) · Annual Review of Genetics · doi:10.1146/annurev.ge.26.120192.001143 · Cited by 552 · see citing works
The ubiquitin system
Varshavsky, A. J. (1997) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(97)01122-5 · Cited by 546 · see citing works
TYPE OF FALL AND RISK OF HIP AND WRIST FRACTURES: THE STUDY OF OSTEOPOROTIC FRACTURES
Drinka, P. J. (1994) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1994.tb06547.x · Cited by 475 · see citing works
Skeletal muscle weakness in old age: underlying mechanisms.
Brooks, S. V., & Faulkner, J. A. (1994) · PubMed · Cited by 463 · see citing works
The mechanism and functions of ATP‐dependent proteases in bacterial and animal cells
Goldberg, A. L. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb19822.x · Cited by 454 · see citing works
Ubiquitination
Finley, D., & Chau, V. (1991) · Annual Review of Cell Biology · doi:10.1146/annurev.cb.07.110191.000325 · Cited by 442 · see citing works
Importance of the ATP-Ubiquitin-Proteasome Pathway in the Degradation of Soluble and Myofibrillar Proteins in Rabbit Muscle Extracts
Solomon, V., & Goldberg, A. L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.43.26690 · Cited by 432 · see citing works
Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates ‘reserve cells
Yoshida, N., Yoshida, S., Koishi, K., Masuda, K., & Nabeshima, Y.-I. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.6.769 · Cited by 425 · see citing works
Changes in skeletal muscle with aging: effects of exercise training.
Rogers, M. A., & Evans, W. J. (1993) · PubMed · Cited by 396 · see citing works
Adaptive transformation of rat soleus motor units during growth
Kugelberg, E. (1976) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(76)90001-0 · Cited by 382 · see citing works
Sample application by in‐gel rehydration improves the resolution of two‐dimensional electrophoresis with immobilized pH gradients in the first dimension
Rabilloud, T., Valette, C., & Lawrence, J. (1994) · Electrophoresis · doi:10.1002/elps.11501501223 · Cited by 367 · see citing works
Distribution of different fibre types in human skeletal muscles
Lexell, J. E., Downham, D. Y., & Sjöstróm, M. (1986) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(86)90009-2 · Cited by 342 · see citing works
Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: Implications for cell and gene therapy
Webster, C., & Blau, H. M. (1990) · Somatic Cell and Molecular Genetics · doi:10.1007/bf01233096 · Cited by 298 · see citing works
Increase in levels of polyubiquitin and proteasome mRNA in skeletal muscle during starvation and denervation atrophy
Medina, R., Wing, S. S., & Goldberg, A. L. (1995) · Biochemical Journal · doi:10.1042/bj3070631 · Cited by 294 · see citing works
IGF-I restores satellite cell proliferative potential in immobilized old skeletal muscle
Chakravarthy, M. V., Davis, B. S., & Booth, F. W. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.89.4.1365 · Cited by 262 · see citing works
Sepsis stimulates nonlysosomal, energy-dependent proteolysis and increases ubiquitin mRNA levels in rat skeletal muscle.
Tiao, G. M., Fagan, J. M., Samuels, N., James, J. H., Hudson, K., Lieberman, M. A., Fischer, J. E., & Hasselgren, P.-O. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117588 · Cited by 255 · see citing works
Contraction-induced injury: recovery of skeletal muscles in young and old mice
Brooks, S. V., & Faulkner, J. A. (1990) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1990.258.3.c436 · Cited by 238 · see citing works
Histochemical and Ultrastructural Changes in Senile Human Skeletal Muscle
Tomonaga, M. (1977) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1977.tb00274.x · Cited by 224 · see citing works
Increased ATP-ubiquitin-dependent proteolysis in skeletal muscles of tumor-bearing rats.
Temparis, S., Asensi, M., Taillandier, D., AUROUSSEAU, E., Larbaud, D., Obled, A., Béchet, D., Ferrara, M., Estrela, J. M., & Attaix, D. (1994) · PubMed · Cited by 214 · see citing works
Correlative histochemical study of skeletal muscle after suprasegmental denervation, peripheral nerve section, and skeletal fixation
Karpati, G., & Engel, W. K. (1968) · Neurology · doi:10.1212/wnl.18.7.681 · Cited by 202 · see citing works
Enhancement of skeletal muscle regeneration
Bischoff, R., & Heintz, C. (1994) · Developmental Dynamics · doi:10.1002/aja.1002010105 · Cited by 193 · see citing works
Plasma creatine kinase activity and exercise-induced muscle damage in older men
Manfredi, T. G., Fielding, R. A., REILLY, K. P. O., MEREDITH, C. N., LEE, H. Y., & Evans, W. J. (1991) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199109000-00006 · Cited by 182 · see citing works
Morphology and physiology of skeletal muscle in aging rodents
Caccia, M. R., Harris, J. B., & Johnson, M. A. (1979) · Muscle & Nerve · doi:10.1002/mus.880020308 · Cited by 168 · see citing works
Healing of experimental muscle strains and the effects of nonsteroidal antiinflammatory medication
Almekinders, L. C., & Gilbert, J. A. (1986) · The American Journal of Sports Medicine · doi:10.1177/036354658601400411 · Cited by 165 · see citing works
New insights into proteasome function: from archaebacteria to drug development
Goldberg, A. L., Stein, R. L., & Adams, J. (1995) · Chemistry & Biology · doi:10.1016/1074-5521(95)90182-5 · Cited by 134 · see citing works
Satellite cells and myonuclei in long‐term denervated rat muscles
Rodrigues, A. D. C., & Schmalbruch, H. (1995) · The Anatomical Record · doi:10.1002/ar.1092430405 · Cited by 133 · see citing works
Running and the Development of Disability with Age
Fries, J. F., Singh, G., Morfeld, D., Hubert, H. B., Lane, N. E., & Brown, B. W. (1994) · Annals of Internal Medicine · doi:10.7326/0003-4819-121-7-199410010-00005 · Cited by 132 · see citing works
Genome‐wide examination of myoblast cell cycle withdrawal during differentiation
Shen, X., Collier, J. M., Hlaing, M., Zhang, L., Delshad, E. H., Bristow, J. D., & Bernstein, H. S. (2002) · Developmental Dynamics · doi:10.1002/dvdy.10200 · Cited by 122 · see citing works
Fibre-type composition, structure and cytoskeletal protein location of fibres in anterior tibial muscle
Jakobsson, F., Borg, K., & Edstr�m, L. (1990) · Acta Neuropathologica · doi:10.1007/bf00294604 · Cited by 118 · see citing works
Induction of apoptosis by extracellular ubiquitin in human hematopoietic cells: possible involvement of STAT3 degradation by proteasome pathway in interleukin 6-dependent hematopoietic cells
Daino, H., Matsumura, I., Takada, K., Odajima, J., Tanaka, H., Ueda, S., Shibayama, H., Ikeda, H., Hibi, M., Machii, T., et al. (2000) · Blood · doi:10.1182/blood.v95.8.2577 · Cited by 115 · see citing works
The ATP dependence of the degradation of short- and long-lived proteins in growing fibroblasts.
Gronostajski, R. M., Pardee, A. B., & Goldberg, A. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83626-8 · Cited by 114 · see citing works
Histochemical and ultrastructural aspects of M. vastus lateralis in sedentary old people (age 65?89 years)
Scelsi, R., Marchetti, C., & Poggi, P. (1980) · Acta Neuropathologica · doi:10.1007/bf00690450 · Cited by 105 · see citing works
Effects of aging on skeletal muscle regeneration
Sadeh, M. (1988) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(88)90055-x · Cited by 102 · see citing works
In Vivo Activation of STAT3 Signaling in Satellite Cells and Myofibers in Regenerating Rat Skeletal Muscles
Kami, K., & Senba, E. (2002) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215540205001202 · Cited by 96 · see citing works
Reinnervation of long-term denervated rat muscle freely grafted into an innervated limb
Carlson, B. M., & Faulkner, J. A. (1988) · Experimental Neurology · doi:10.1016/0014-4886(88)90077-5 · Cited by 83 · see citing works
Cross-sectional study of muscle strength and bone mineral density in a population of 106 women between the ages of 44 and 87 years: relationship with age and menopause
Calmels, P., Vico, L., Alexandre, C., & MINAIRE, P. M. (1995) · European Journal of Applied Physiology · doi:10.1007/bf00361547 · Cited by 66 · see citing works
The role of DNA hypermethylation in human neoplasia
Toyota, M., & Issa, J. J. (2000) · Electrophoresis · doi:10.1002/(sici)1522-2683(20000101)21:2 · Cited by 55 · see citing works
Self-citation
Bisphosphonate modulates proliferation and differentiation of rat periodontal ligament cells during wound healing
Lekic, P., Rubbino, I., Krasnoshtein, F., Cheifetz, S., McCulloch, C. A., & Tenenbaum, H. C. (1997) · The Anatomical Record · doi:10.1002/(sici)1097-0185(199703)247:3 · Cited by 42 · see citing works
Ubiquitin-like moiety of the monoclonal nonspecific suppressor factor β is responsible for its activity
Nakamura, M., Xavier, R. M., & Tanigawa, Y. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.2.532 · Cited by 42 · see citing works
Effect of ubiquitin on platelet functions: possible identity with platelet activity suppressive lymphokine (PASL)
Pancré, V., Pierce, R. J., Fournier, F., Mehtali, M., Delanoye, A., Capron, A., & Auriault, C. (1991) · European Journal of Immunology · doi:10.1002/eji.1830211113 · Cited by 37 · see citing works
Mutational and DNA Binding Specificity of the Carcinogen 2-Amino-3,8-dimethylimidazo[4,5-f]quinoxaline
Solomon, M. S., Leong-Morgenthaler, P.-M., Turesky, R. J., & Essigmann, J. M. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.31.18368 · Cited by 31 · see citing works
Inhibition against CFU-C and CFU-E colony formation by soluble factor(s) derived from hairy cells
Taniguchi, N., Kuratsune, H., Kanamaru, A., Tokumine, Y., Tagawa, S., Machii, T., & Kitani, T. (1989) · Blood · doi:10.1182/blood.v73.4.907.907 · Cited by 26 · see citing works
Extracellular Ubiquitin Regulates the Growth of Human Hematopoietic Cells
Daino, H., Shibayama, H., Machii, T., & Kitani, T. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.0875 · Cited by 24 · see citing works
Age-related changes in fibre number, fibre size, fibre type composition and adenosine triphosphatase activity in rat soleus muscle
Fujimoto, S., Watanabe, J., Ogawa, R., & Kanamura, S. (1994) · Annals of Anatomy - Anatomischer Anzeiger · doi:10.1016/s0940-9602(11)80471-1 · Cited by 15 · see citing works
Inhibition against CFU-C and CFU-E colony formation by soluble factor(s) derived from hairy cells
Taniguchi, N., Kuratsune, H., Kanamaru, A., et al. (1989) · Blood · doi:10.1182/blood.v73.4.907.bloodjournal734907 · Cited by 13 · see citing works
Restriction of the injury response following an acute muscle strain
Reddy, A. S., Reedy, M. K., Seaber, A. V., & Garrett, W. E. J. (1993) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199303000-00005 · Cited by 12 · see citing works
Establishment of a new cell line from a patient with hairy cell leukemia-japanese variant
Shibayama, H., Machii, T., Tokumine, Y., Nishimori, Y., Nojima, J., Inoue, R., Kanamaru, A., Tagawa, S., & Kitani, T. (1997) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428199709114176 · Cited by 6 · see citing works
Untitled work
(1999) · doi:10.1002/(sici)1097-4598(199910)22:10

Flagged first, then by citations

Sorted by citations

The Role of Inflammation in Age-Related Sarcopenia
Dalle, S., Rossmeislova, L., & Koppo, K. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.01045 · Cited by 668 · see citing works
Effect of Physical Activity/Exercise on Oxidative Stress and Inflammation in Muscle and Vascular Aging
El Assar, M., Álvarez-Bustos, A., Sosa, P., Angulo, J., & Rodríguez-Mañas, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158713 · Cited by 371 · see citing works
Atrogin-1, MuRF-1, and sarcopenia
Gumucio, J. P., & Mendias, C. L. (2012) · Endocrine · doi:10.1007/s12020-012-9751-7 · Cited by 368 · see citing works
Skeletal Muscle Mitochondria and Aging: A Review
Peterson, C. M., Johannsen, D. L., & Ravussin, É. (2012) · Journal of Aging Research · doi:10.1155/2012/194821 · Cited by 318 · see citing works
The role of E3 ubiquitin-ligases MuRF-1 and MAFbx in loss of skeletal muscle mass
Rom, O., & Reznick, A. Z. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.12.031 · Cited by 258 · see citing works
Protein degradation and aging
Martínez‐Vicente, M., Sovak, G., & Cuervo, A. M. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.07.005 · Cited by 245 · see citing works
Muscle Wasting in Aged, Sarcopenic Rats Is Associated with Enhanced Activity of the Ubiquitin Proteasome Pathway
Altun, M., Besche, H. C., Overkleeft, H. S., Piccirillo, R., Edelmann, M. J., Kessler, B. M., Goldberg, A. L., & Ulfhake, B. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.129718 · Cited by 226 · see citing works
Atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 are up-regulated in aged rat Tibialis Anterior muscle
Clavel, S., Coldefy, A.-S., Kurkdjian, E., Salles, J., Margaritis, I., & Dérijard, B. (2006) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2006.07.005 · Cited by 218 · see citing works
Beneficial effects of exercise on age‐related mitochondrial dysfunction and oxidative stress in skeletal muscle
Joseph, A., Adhihetty, P. J., & Leeuwenburgh, C. (2016) · The Journal of Physiology · doi:10.1113/jp270659 · Cited by 186 · see citing works
Vitamin D Promotes Skeletal Muscle Regeneration and Mitochondrial Health
Latham, C. M., Brightwell, C. R., Keeble, A. R., Munson, B. D., Thomas, N. T., Zagzoog, A. M., Fry, C. S., & Fry, J. L. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.660498 · Cited by 163 · see citing works
Mitochondria initiate and regulate sarcopenia
Alway, S. E., Mohamed, J. S., & Myers, M. J. (2017) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000101 · Cited by 153 · see citing works
“For example, ubiquitin (17), 26S proteasome, polyubiquitinated proteins (3), MuRF-1, and MAFbx expression were all reported to be elevated in hindlimb muscles of sarcopenic rats as compared with young adult animals (3,30).”
Background
Skeletal muscle proteolysis in aging
Combaret, L., Dardevet, D. P., Béchet, D., Taillandier, D., Mosoni, L., & Attaix, D. (2008) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32831b9c31 · Cited by 152 · see citing works
Sarcopenia and cachexia: the adaptations of negative regulators of skeletal muscle mass
Sakuma, K., & Yamaguchi, A. (2012) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1007/s13539-011-0052-4 · Cited by 137 · see citing works
Altered responses in skeletal muscle protein turnover during aging in anabolic and catabolic periods
Attaix, D., Mosoni, L., Dardevet, D., Combaret, L., Mirand, P. P., & Grizard, J. (2005) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2005.04.009 · Cited by 123 · see citing works
Extracellular ubiquitin: immune modulator and endogenous opponent of damage-associated molecular pattern molecules
Majetschak, M. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.0510316 · Cited by 114 · see citing works
Aging and regulated protein degradation: who has the UPPer hand?
Vernace, V. A., Schmidt‐Glenewinkel, T., & Figueiredo‐Pereira, M. E. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00329.x · Cited by 110 · see citing works
Chronic hypobaric hypoxia mediated skeletal muscle atrophy: role of ubiquitin–proteasome pathway and calpains
Chaudhary, P., Suryakumar, G., Prasad, R., Singh, S. N., Ali, S., & Ilavazhagan, G. (2012) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-011-1210-x · Cited by 108 · see citing works
Ubiquitin-proteasome pathway in skeletal muscle atrophy
Pang, X., Zhang, P., Chen, X., & Liu, W. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1289537 · Cited by 106 · see citing works
The CXC Chemokine Receptor 4 Ligands Ubiquitin and Stromal Cell-derived Factor-1α Function through Distinct Receptor Interactions
Saini, V., Staren, D. M., Ziarek, J. J., Nashaat, Z. N., Campbell, E. M., Volkman, B. F., Marchese, A., & Majetschak, M. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.233742 · Cited by 93 · see citing works
Caloric restriction optimizes the proteasome pathway with aging in rat plantaris muscle: implications for sarcopenia
Hepple, R. T., Qin, M., Nakamoto, H., & Goto, S. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90478.2008 · Cited by 83 · see citing works
Vitamin E in Sarcopenia: Current Evidences on Its Role in Prevention and Treatment
Khor, S. C., Karim, N. A., Ngah, W. Z. W., Yusof, Y. A. M., & Makpol, S. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/914853 · Cited by 77 · see citing works
Skeletal muscle atrogenes: From rodent models to human pathologies
Taillandier, D., & Polge, C. (2019) · Biochimie · doi:10.1016/j.biochi.2019.07.014 · Cited by 66 · see citing works
The Effect of Aging on Anaerobic and Aerobic Enzyme Activities in Human Skeletal Muscle
Kaczor, J. J., Ziółkowski, W., Antosiewicz, J., Hać, S., Tarnopolsky, M. A., & Popinigis, J. (2006) · The Journals of Gerontology Series A · doi:10.1093/gerona/61.4.339 · Cited by 62 · see citing works
Psychological stress and aging: role of glucocorticoids (GCs)
Hasan, K., Rahman, M. S., Arif, K. M. T., & Sobhani, M. E. (2011) · AGE · doi:10.1007/s11357-011-9319-0 · Cited by 59 · see citing works
Selective downregulation of ubiquitin conjugation cascade mRNA occurs in the senescent rat soleus muscle
DeRuisseau, K. C., Kavazis, A. N., & Powers, S. K. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.04.005 · Cited by 58 · see citing works
Sarcopenia-related apoptosis is regulated differently in fast- and slow-twitch muscles of the aging F344/N×BN rat model
Rice, K. M., & Blough, E. R. (2006) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2006.03.005 · Cited by 52 · see citing works
Therapeutic Consequences of Targeting the IGF-1/PI3K/AKT/FOXO3 Axis in Sarcopenia: A Narrative Review
Gellhaus, B., Böker, K. O., Schilling, A. F., & Saul, D. (2023) · Cells · doi:10.3390/cells12242787 · Cited by 52 · see citing works
Characterisation and expression analysis of cathepsins and ubiquitin-proteasome genes in gilthead sea bream (Sparus aurata) skeletal muscle
Salmerón, C., Navarro, I., Johnston, I. A., Gutiérrez, J., & Capilla, E. (2015) · BMC Research Notes · doi:10.1186/s13104-015-1121-0 · Cited by 49 · see citing works
Involvement of the calcium-dependent proteolytic system in skeletal muscle aging
Dargelos, É., Brulé, C., Combaret, L., Hadj-Sassi, A., Dulong, S., Poussard, S., & Cottin, P. (2007) · Experimental Gerontology · doi:10.1016/j.exger.2007.08.009 · Cited by 47 · see citing works
Ubiquitin Ligases in Longevity and Aging Skeletal Muscle
Hughes, D. C., Baehr, L. M., Waddell, D. S., Sharples, A. P., & Bodine, S. C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23147602 · Cited by 45 · see citing works
Curcumin treatment prevents increased proteasome and apoptosome activities in rat skeletal muscle during reloading and improves subsequent recovery
Vazeille, E., Slimani, L., Claustre, A., Magne, H., Labas, R., Béchet, D., Taillandier, D., Dardevet, D. P., Astruc, T., Attaix, D., et al. (2011) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2010.11.021 · Cited by 45 · see citing works
Targeting mitochondrial quality control for treating sarcopenia: lessons from physical exercise
Picca, A., Calvani, R., Leeuwenburgh, C., Coelho‐Júnior, H. J., Bernabei, R., Landi, F., & Marzetti, E. (2018) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2019.1559827 · Cited by 42 · see citing works
Aging and the ubiquitinome: Traditional and non-traditional functions of ubiquitin in aging cells and tissues
Grillari, J., Katinger, H. W. D., & Voglauer, R. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2006.07.003 · Cited by 40 · see citing works
The Current Landscape of Pharmacotherapies for Sarcopenia
Bahat, G., & Özkök, S. (2024) · Drugs & Aging · doi:10.1007/s40266-023-01093-7 · Cited by 41 · see citing works
Essential role of proteasomes in maintaining self-renewal in neural progenitor cells
Zhao, Y., Liu, X., He, Z., Niu, X., Shi, W., Ding, J., Zhang, L., Yuan, T., Li, A., Yang, W., et al. (2016) · Scientific Reports · doi:10.1038/srep19752 · Cited by 33 · see citing works
Proteolysis activation and proteome alterations in murine skeletal muscle submitted to 1 week of hindlimb suspension
Ferreira, R. M., Vitorino, R. M. P., Neuparth, M. J., Appell, H.-J., Duarte, J. A., & Amado, F. M. L. (2009) · European Journal of Applied Physiology · doi:10.1007/s00421-009-1151-1 · Cited by 30 · see citing works
Proteasome activities in the rectus abdominis muscle of young and older individuals
Bossola, M., Pacelli, F., Costelli, P., Tortorelli, A. P., Rosa, F., & Doglietto, G. B. (2008) · Biogerontology · doi:10.1007/s10522-008-9135-9 · Cited by 29 · see citing works
Proteolytic systems’ expression during myogenesis and transcriptional regulation by amino acids in gilthead sea bream cultured muscle cells
Vélez, E. J., Azizi, S., Verheyden, D., Salmerón, C., Lutfi, E., Sánchez-Moya, A., Navarro, I., Gutiérrez, J., & Capilla, E. (2017) · PLoS ONE · doi:10.1371/journal.pone.0187339 · Cited by 29 · see citing works
Effects of ageing on expression of the muscle-specific E3 ubiquitin ligases and Akt-dependent regulation of Foxo transcription factors in skeletal muscle
Wagatsuma, A., Shiozuka, M., Takayama, Y., Hoshino, T., Mabuchi, K., & Matsuda, R. (2015) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-015-2608-7 · Cited by 27 · see citing works
Extracellular Ubiquitin: Role in Myocyte Apoptosis and Myocardial Remodeling
Scofield, S. L. C., Amin, P., Singh, M., & Singh, K. (2015) · Comprehensive physiology · doi:10.1002/cphy.c150025 · Cited by 19 · see citing works
Sarcopenic metabolomic profile reflected a sarcopenic phenotype associated with amino acid and essential fatty acid changes
Opazo, R., Bárbara Angel, B., Márquez, C., Lera, L., dos Santos, G. R. C., Monnerat, G., & Cecilia Albala, B. (2021) · Metabolomics · doi:10.1007/s11306-021-01832-0 · Cited by 18 · see citing works
Skeletal muscle myostatin mRNA expression is upregulated in aged human adults with excess adiposity but is not associated with insulin resistance and ageing
Wilhelmsen, A., Stephens, F. B., Bennett, A. J., Karagounis, L. G., Jones, S. W., & Tsintzas, K. (2023) · GeroScience · doi:10.1007/s11357-023-00956-6 · Cited by 17 · see citing works
Functional and structural consequences of chemokine (C-X-C motif) receptor 4 activation with cognate and non-cognate agonists
Eby, J. M., Abdelkarim, H., Albee, L. J., Tripathi, A., Gao, X., Volkman, B. F., Gaponenko, V., & Majetschak, M. (2017) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-017-3044-7 · Cited by 17 · see citing works
Sarcopenia; functional concerns, molecular mechanisms involved, and seafood as a nutritional intervention – review article
Jayawardena, T. U., Kim, S., & Jeon, Y. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1969889 · Cited by 15 · see citing works
Does Antigen Masking by Ubiquitin Chains Protect from the Development of Autoimmune Diseases?
Weil, R. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00262 · Cited by 14 · see citing works
Cellular Degradation Machineries in Age-Related Loss of Muscle Mass (Sarcopenia)
Altun, M., Grönholdt-Klein, M., Wang, L.-Z., & Ulfhake, B. (2012) · InTech eBooks · doi:10.5772/34274 · Cited by 15 · see citing works
Activation of NFκB and Ub-proteasome pathway during apoptosis induced by a serum factor is mediated through the upregulation of the 26S proteasome subunits
Singh, S., & Khar, A. (2006) · APOPTOSIS · doi:10.1007/s10495-006-5878-4 · Cited by 12 · see citing works
Variation in ACE activity affects myogenic differentiation in C2C12 cells
Mori, S., & Tokuyama, K. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.12.056 · Cited by 8 · see citing works
A review of omics studies in sarcopenia: from molecular mechanisms to hepatic-gut-muscle interactions in chronic liver disease comorbidity
Xue, X., Xu, J., Wang, H., Wang, K., Chen, Y., Xu, Y., Que, S., & Liu, Z. (2026) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1710582 · Cited by 6 · see citing works
Potential benefits of nutritional supplementation in diabetic sarcopenia
Lee, H., Yang, S. J., & Lim, Y. (2022) · Redox Experimental Medicine · doi:10.1530/rem-22-0001 · Cited by 6 · see citing works
Antioxidants and Polyphenols Mediate Mitochondrial Mediated Muscle Death Signaling in Sarcopenia
Alway, S. E. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-810422-4.00026-9 · Cited by 6 · see citing works
Muscle diseases and aging
Oflazer, P. (2007) · Handbook of clinical neurology · doi:10.1016/s0072-9752(07)86018-0 · Cited by 4 · see citing works
Advances in understanding the mitogenic, metabolic, and cell death signaling in teleost development: the case of greater amberjack (Seriola dumerili, Risso 1810)
Panteli, N., Demertzioglou, M., Feidantsis, K. G., Karapanagiotis, S., Tsele, N., Tsakoniti, K., Gkagkavouzis, K., Mylonas, C. C., Kormas, K. A., Mente, E., et al. (2022) · Fish Physiology and Biochemistry · doi:10.1007/s10695-022-01146-5 · Cited by 4 · see citing works
Skeletal muscle transcriptome is affected by age in severely burned mice
Song, J., Widen, S. G., Wolf, S. E., & Ayadi, A. E. (2022) · Scientific Reports · doi:10.1038/s41598-022-26040-1 · Cited by 4 · see citing works
MLM3 and MLM5 head and neck cancer models promote age-dependent musculoskeletal deterioration in mice
Jones, A. J., Esteca, M. V., Huot, J. R., Simabuco, F. M., Moore, M. G., & Pin, F. (2025) · Scientific Reports · doi:10.1038/s41598-025-25601-4 · Cited by 2 · see citing works
Isolation and optimization of mice skeletal muscle satellite cells using preplating method and culture media substitution
Bakhtiari, N. (2016) · Cited by 1 · see citing works
Linking mitochondrial dysfunction to sarcopenia
Alway, S. E. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-822146-4.00004-1 · Cited by 1 · see citing works
The role of osteoprotegerin (OPG) in exercise-induced skeletal muscle adaptation
Owens, A., Santos, L., Brook, M. S., Hunt, J. A., Piasecki, M., & Piasecki, J. (2024) · Translational Exercise Biomedicine · doi:10.1515/teb-2024-0033 · Cited by 1 · see citing works
Extracellular Ubiquitin: Role in Myocyte Apoptosis and Myocardial Remodeling
Scofield, S. L. C., Amin, P., Singh, M., & Singh, K. (2016) · Comprehensive physiology · doi:10.1002/j.2040-4603.2016.tb00684.x · Cited by 1 · see citing works
Old-age muscle atrophy : Cellular mechanisms and behavioral consequenses
Altun, M. (2007) · Figshare
The Effects of Aging on Muscle Loss and Nuclear Factor Kappa-B Levels in Rats Fed a Diet Containing Suboptimal Leucine Levels
Kohlen, C. R. (2009) · doi:10.15368/theses.2009.3
An investigation of NADPH oxidase in normal and diseased skeletal muscle.
Sullivan, M. (2010) · doi:10.13140/rg.2.2.12785.33124
Mini-Review Protein degradation and aging
Martínez‐Vicente, M., Sovak, G., & Cuervo, A. M. (2005)
Characterization of the Coca Chemokine Receptor Four Agonist Activity of Ubiquitin
Staren, D. M. (2012) · Loyola eCommons (Loyola University of Chicago)
Peucedanum japonicum Thunb. ameliorates age-related muscle loss by improving mitochondrial function in aged mice
Kim, Y. I., Young-Soo, K., Jung, C. H., & Ahn, J. (2026) · GeroScience · doi:10.1007/s11357-026-02123-z

Selective downregulation of ubiquitin conjugation cascade mRNA occurs in the senescent rat soleus muscle
DeRuisseau, K. C., Kavazis, A. N., & Powers, S. K. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.04.005 · Cited by 58 · see citing works
Muscle Wasting in Aged, Sarcopenic Rats Is Associated with Enhanced Activity of the Ubiquitin Proteasome Pathway
Altun, M., Besche, H. C., Overkleeft, H. S., Piccirillo, R., Edelmann, M. J., Kessler, B. M., Goldberg, A. L., & Ulfhake, B. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.129718 · Cited by 226 · see citing works
Atrophy-related ubiquitin ligases, atrogin-1 and MuRF1 are up-regulated in aged rat Tibialis Anterior muscle
Clavel, S., Coldefy, A.-S., Kurkdjian, E., Salles, J., Margaritis, I., & Dérijard, B. (2006) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2006.07.005 · Cited by 218 · see citing works
Dysregulation of the ubiquitin–proteasome system in aging skeletal muscle
Song, G., Lee, B.-Y., & Baek, K. (2026) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2026.119504 · Cited by 1 · see citing works
Aging is Associated with a Downregulation of Genes Linked to Protein Ubiquitination and Glucose Metabolism in Human Skeletal Muscle
Hart, C. B. (2022) · ScholarWorks (Central Washington University)

Authors: Cai, D., Lee, K. K. H., Li, M., Tang, M. K., & Chan, K. M.
Affiliations: Jinan University (CN)
Chinese University of Hong Kong (HK)
Corresponding author: Cai, Dongqing
ORCID: Lee, K.K.H
Li, M
Venue: Archives of Biochemistry and Biophysics
Publisher: Elsevier BV
Published: 2004-05
Volume: 425
Issue: 1
Pages: 42-50
ISSN: 0003-9861 (ISSN-L)
DOI: 10.1016/j.abb.2004.02.027
OpenAlex: W1991015655
Cited by: 65
References: 61
Citations by year: 2026: 2 · 2025: 1 · 2024: 2 · 2023: 3 · 2022: 5 · 2021: 4 · 2019: 1 · 2018: 2 · 2017: 4 · 2016: 3 · 2015: 5 · 2014: 2 · 2012: 6
FWCI: 1.66
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Archives of Biochemistry and Biophysics (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 › Ubiquitin and proteasome pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
Keywords: ubiquitin, skeletal muscle aging, fast-twitch muscle, ubiquitin-proteasome system, satellite cells, muscle degeneration, cell cycle entry, muscle healing, differentially expressed proteins
MeSH terms: Adult, Aged, Aging, Animals, Cell Cycle, Humans, Middle Aged, Electrophoresis, Gel, Two-Dimensional, Up-Regulation, Rats, Sprague-Dawley, Muscle, Skeletal, Muscle Fibers, Fast-Twitch, In Situ Nick-End Labeling, Ubiquitin, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Ubiquitin expression is up-regulated in human and rat skeletal muscles during aging

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks