Small peptides: Could they have a big role in metabolism and the response to exercise?
Open accessAbstract
Exercise is a powerful non-pharmacological intervention for the treatment and prevention of numerous chronic diseases. Contracting skeletal muscles provoke widespread perturbations in numerous cells, tissues and organs, which stimulate multiple integrated adaptations that ultimately contribute to the many health benefits associated with regular exercise. Despite much research, the molecular mechanisms driving such changes are not completely resolved. Technological advancements beginning in the early 1960s have opened new avenues to explore the mechanisms responsible for the many beneficial adaptations to exercise. This has led to increased research into the role of small peptides (<100 amino acids) and mitochondrially derived peptides in metabolism and disease, including those coded within small open reading frames (sORFs; coding sequences that encode small peptides). Recently, it has been hypothesized that sORF-encoded mitochondrially derived peptides and other small peptides play significant roles as exercise-sensitive peptides in exercise-induced physiological adaptation. In this review, we highlight the discovery of mitochondrially derived peptides and newly discovered small peptides involved in metabolism, with a specific emphasis on their functions in exercise-induced adaptations and the prevention of metabolic diseases. In light of the few studies available, we also present data on how both single exercise sessions and exercise training affect expression of sORF-encoded mitochondrially derived peptides. Finally, we outline numerous research questions that await investigation regarding the roles of mitochondrially derived peptides in metabolism and prevention of various diseases, in addition to their roles in exercise-induced physiological adaptations, for future studies.
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Mitochondria-derived peptides play a key role in regulating muscle homeostasis and preventing sarcopenia.
“Recent studies have shown that mitochondria-derived peptides (MDPs) play a key role in regulating muscle homeostasis and preventing sarcopenia [24].”
From Exerkines and Sarcopenia: Unveiling the Mechanism Behind Exercise-Induced Mitochondrial Homeostasis (2025) · cites this paper as [24]
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Cites
AMPK: guardian of metabolism and mitochondrial homeostasis
Herzig, S., & Shaw, R. J. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.95 · Cited by 4,094 · see citing works
Exercise as medicine - evidence for prescribing exercise as therapy in 26 different chronic diseases
Pedersen, B. K., & Saltin, B. (2015) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/sms.12581 · Cited by 3,514 · see citing works
Muscles, exercise and obesity: skeletal muscle as a secretory organ
Pedersen, B. K., & Febbraio, M. A. (2012) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2012.49 · Cited by 2,909 · see citing works
Lack of Exercise Is a Major Cause of Chronic Diseases
Booth, F. W., Roberts, C. K., & Laye, M. J. (2012) · Comprehensive Physiology · doi:10.1002/cphy.c110025 · Cited by 2,575 · see citing works
Yakes, F. M., & Van Houten, B. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.2.514 · Cited by 1,854 · see citing works
Mitochondrial form and function
Friedman, J. R., & Nunnari, J. (2014) · Nature · doi:10.1038/nature12985 · Cited by 1,803 · see citing works
Diet, muscle glycogen and physical performance.
Bergström, J., Hermansen, L., Hultman, E., & Saltin, B. (1967) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1967.tb03720.x · Cited by 1,740 · cited 1× · see citing works
“Seminal works published in the 1960s were the first to provide mechanistic insights into how training-induced changes to skeletal muscle might contribute to improved health (Bergström et al., 1967; Hermansen et al., 1967).”
BackgroundThe PI3K/AKT Pathway in Obesity and Type 2 Diabetes
Huang, X., Liu, G., Guo, J., & Su, Z. (2018) · International Journal of Biological Sciences · doi:10.7150/ijbs.27173 · Cited by 1,673 · see citing works
Biochemical Adaptations in Muscle
Holloszy, J. O. (1967) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)96046-1 · Cited by 1,517 · see citing works
Cellular functions of long noncoding RNAs
Yao, R.-W., Wang, Y., & Chen, L. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0311-8 · Cited by 1,381 · see citing works
A micropeptide encoded by a putative long noncoding RNA regulates muscle performance
Anderson, D. M., Anderson, K. M., Chang, C.-L., Makarewich, C. A., Nelson, B. R., McAnally, J. R., Kasaragod, P., Shelton, J. M., Liou, J., Bassel-Duby, R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.01.009 · Cited by 1,216 · see citing works
Integrative Biology of Exercise
Hawley, J. A., Hargreaves, M., Joyner, M. J., & Zierath, J. R. (2014) · Cell · doi:10.1016/j.cell.2014.10.029 · Cited by 1,152 · see citing works
Regulation and function of AMPK in physiology and diseases
Jeon, S. (2016) · Experimental & Molecular Medicine · doi:10.1038/emm.2016.81 · Cited by 1,122 · see citing works
Role of Mitochondrial Dysfunction in Insulin Resistance
Kim, J.-A., Wei, Y., & Sowers, J. R. (2008) · Circulation Research · doi:10.1161/circresaha.107.165472 · Cited by 1,103 · see citing works
The role of exercise and PGC1α in inflammation and chronic disease
Handschin, C., & Spiegelman, B. M. (2008) · Nature · doi:10.1038/nature07206 · Cited by 1,083 · see citing works
Exerkines in health, resilience and disease
Chow, L. S., Gerszten, R. E., Taylor, J. M., Pedersen, B. K., van Praag, H., Trappe, S., Febbraio, M. A., Galis, Z. S., Gao, Y., Haus, J. M., et al. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00641-2 · Cited by 927 · see citing works
Mitonuclear communication in homeostasis and stress
Quirós, P. M., Mottis, A., & Auwerx, J. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.23 · Cited by 787 · see citing works
Metabolic Control of Longevity
López-Otín, C., Galluzzi, L., Freije, J. M. P., Madeo, F., & Kroemer, G. (2016) · Cell · doi:10.1016/j.cell.2016.07.031 · Cited by 753 · see citing works
Muscle Glycogen during Prolonged Severe Exercise
Hermansen, L., Hultman, E., & Saltin, B. (1967) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1967.tb03719.x · Cited by 752 · see citing works
A peptide encoded by a transcript annotated as long noncoding RNA enhances SERCA activity in muscle
Nelson, B. R., Makarewich, C. A., Anderson, D. M., Winders, B. R., Troupes, C. D., Wu, F.-F., Reese, A. L., McAnally, J. R., Chen, X.-W., Kavalali, E., et al. (2016) · Science · doi:10.1126/science.aad4076 · Cited by 730 · see citing works
Lee, C., Zeng, J., Drew, B. G., Sallam, T., Martin-Montalvo, A., Wan, J., Kim, S.-J., Mehta, H., Hevener, A. L., de Cabo, R., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.02.009 · Cited by 715 · see citing works
Exercise-induced oxidative stress: Friend or foe?
Powers, S. K., Deminice, R., Ozdemir, M., Yoshihara, T., Bomkamp, M. P., & Hyatt, H. (2020) · Journal of Sport and Health Science · doi:10.1016/j.jshs.2020.04.001 · Cited by 655 · see citing works
Gureev, A. P., Shaforostova, E. A., & Popov, V. N. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00435 · Cited by 651 · see citing works
Role of cardiolipin alterations in mitochondrial dysfunction and disease
Chicco, A. J., & Sparagna, G. C. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00243.2006 · Cited by 641 · see citing works
Hashimoto, Y., Niikura, T., Tajima, H., Yasukawa, T., Sudo, H., Ito, Y., Kita, Y. A., Kawasumi, M., Kouyama, K., Doyu, M., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.101133498 · Cited by 624 · see citing works
The Translational Landscape of the Human Heart
van Heesch, S., Witte, F., Schneider-Lunitz, V., Schulz, J. F., Adami, E., Faber, A. B., Kirchner, M., Maatz, H., Blachut, S., Sandmann, C.-L., et al. (2019) · Cell · doi:10.1016/j.cell.2019.05.010 · Cited by 619 · see citing works
Mitochondrial calcium overload is a key determinant in heart failure
Santulli, G., Xie, W., Reiken, S. R., & Marks, A. R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1513047112 · Cited by 561 · see citing works
The HUGO Gene Nomenclature Committee (HGNC)
Povey, S., Lovering, R. C., Bruford, E. A., Wright, M. W., Lush, M. J., & Wain, H. (2001) · Human Genetics · doi:10.1007/s00439-001-0615-0 · Cited by 509 · see citing works
Tarnopolsky, M. A., Rennie, C. D., Robertshaw, H. A., Fedak-Tarnopolsky, S. N., Devries, M. C., & Hamadeh, M. J. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00472.2006 · Cited by 457 · see citing works
Transcriptomic profiling of skeletal muscle adaptations to exercise and inactivity
Pillon, N. J., Gabriel, B. M., Dollet, L., Smith, J. A. B., Sardón Puig, L., Botella, J., Bishop, D. J., Krook, A., & Zierath, J. R. (2020) · Nature Communications · doi:10.1038/s41467-019-13869-w · Cited by 457 · see citing works
Self-citationEffects of exercise on mitochondrial content and function in aging human skeletal muscle
Menshikova, E. V., Ritov, V. B., Fairfull, L., Ferrell, R. E., Kelley, D. E., & Goodpaster, B. H. (2006) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/61.6.534 · Cited by 398 · see citing works
The Effect of Physical Exercise on Endothelial Function
Francescomarino, S. D., Sciartilli, A., Valerio, V. D., Baldassarre, A. D., & Gallina, S. (2009) · Sports Medicine · doi:10.2165/11317750-000000000-00000 · Cited by 379 · see citing works
Daussin, F. N., Zoll, J., Dufour, S. P., Ponsot, E., Lonsdorfer-Wolf, E., Doutreleau, S., Mettauer, B., Piquard, F., Geny, B., & Richard, R. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00875.2007 · Cited by 375 · see citing works
Exercise and metabolic health: beyond skeletal muscle
Thyfault, J., & Bergouignan, A. (2020) · Diabetologia · doi:10.1007/s00125-020-05177-6 · Cited by 373 · see citing works
Conserved Regulation of Cardiac Calcium Uptake by Peptides Encoded in Small Open Reading Frames
Magny, E. G., Pueyo, J. I., Pearl, F. M. G., Céspedes, M. A., Niven, J. E., Bishop, S. A., & Couso, J. P. (2013) · Science · doi:10.1126/science.1238802 · Cited by 368 · see citing works
Control of muscle formation by the fusogenic micropeptide myomixer
Bi, P., Ramirez-Martinez, A., Li, H., Cannavino, J., McAnally, J. R., Shelton, J., Sánchez-Ortiz, E., Bassel-Duby, R., & Olson, E. (2017) · Science · doi:10.1126/science.aam9361 · Cited by 363 · see citing works
Classification and function of small open reading frames
Couso, J. P., & Patraquim, P. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.58 · Cited by 335 · see citing works
Montero, D., & Lundby, C. (2017) · The Journal of Physiology · doi:10.1113/jp273480 · Cited by 327 · cited 1× · see citing works
“…adaptations in humans, including elevated abundance of mitochondrial proteins, increased mitochondrial content and greater mitochondrial respiratory function (Daussin et al., 2008; Granata et al., 2016a, b; Montero & Lundby, 2017; for a comprehensive review, please see Granata et al., 2018).”
BackgroundKim, K. H., Son, J. M., Benayoun, B. A., & Lee, C. D. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.06.008 · Cited by 311 · see citing works
Insulin-Stimulated Akt Kinase Activity Is Reduced in Skeletal Muscle From NIDDM Subjects
Krook, A., Roth, R. A., Jiang, X. J., Zierath, J. R., & Wallberg‐Henriksson, H. (1998) · Diabetes · doi:10.2337/diab.47.8.1281 · Cited by 309 · see citing works
AMPK and Exercise: Glucose Uptake and Insulin Sensitivity
O'Neill, H. M. (2013) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2013.37.1.1 · Cited by 295 · see citing works
Cobb, L. J., Lee, C. D., Xiao, J., Yen, K., Wong, R. G., Nakamura, H. K., Mehta, H. H., Gao, Q., Ashur, C., Huffman, D. M., et al. (2016) · Aging · doi:10.18632/aging.100943 · Cited by 288 · see citing works
Humanin: a harbinger of mitochondrial-derived peptides
Lee, C., Yen, K., & Cohen, P. (2013) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2013.01.005 · Cited by 284 · see citing works
Egan, B., & Sharples, A. P. (2023) · Physiological Reviews · doi:10.1152/physrev.00054.2021 · Cited by 278 · see citing works
Stein, C. S., Jadiya, P., Zhang, X., McLendon, J. M., Abouassaly, G. M., Witmer, N. H., Anderson, E. J., Elrod, J. W., & Boudreau, R. L. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.002 · Cited by 271 · see citing works
Humanin: A Novel Central Regulator of Peripheral Insulin Action
Muzumdar, R. H., Huffman, D. M., Atzmon, G., Buettner, C., Cobb, L. J., Fishman, S., Budagov, T., Cui, L., Einstein, F. H., Poduval, A., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006334 · Cited by 248 · see citing works
Training-Induced Changes in Mitochondrial Content and Respiratory Function in Human Skeletal Muscle
Granata, C., Jamnick, N. A., & Bishop, D. J. (2018) · Sports Medicine · doi:10.1007/s40279-018-0936-y · Cited by 247 · cited 4× · see citing works
“…adaptations in humans, including elevated abundance of mitochondrial proteins, increased mitochondrial content and greater mitochondrial respiratory function (Daussin et al., 2008; Granata et al., 2016a, b; Montero & Lundby, 2017; for a comprehensive review, please see Granata et al., 2018).”
BackgroundInfluentialSelf-citationMitocellular communication: Shaping health and disease
Mottis, A., Herzig, S., & Auwerx, J. H. (2019) · Science · doi:10.1126/science.aax3768 · Cited by 238 · see citing works
The role of mitochondria in health and disease
Johannsen, D. L., & Ravussin, É. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2009.09.002 · Cited by 235 · see citing works
Hashimoto, Y., Ito, Y., Niikura, T., Shao, Z., Hata, M., Oyama, F., & Nishimoto, I. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.4765 · Cited by 223 · see citing works
Hashimoto, Y., Niikura, T., Ito, Y., Sudo, H., Hata, M., Arakawa, E., Abe, Y., Kita, Y. A., & Nishimoto, I. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09235.2001 · Cited by 219 · see citing works
Granata, C., Oliveira, R. S. F., Little, J. P., Renner, K., & Bishop, D. J. (2016) · The FASEB Journal · doi:10.1096/fj.15-276907 · Cited by 215 · see citing works
Self-citationHuman pluripotent stem cells: an emerging model in developmental biology
Zhu, Z., & Huangfu, D. (2013) · Development · doi:10.1242/dev.086165 · Cited by 205 · see citing works
Exosomes as Mediators of the Systemic Adaptations to Endurance Exercise
Safdar, A., & Tarnopolsky, M. A. (2018) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029827 · Cited by 203 · see citing works
Reynolds, J. C., Lai, R. W., Woodhead, J. S. T., Joly, J. H., Mitchell, C. J., Cameron-Smith, D., Lu, R., Cohen, P., Graham, N. A., Benayoun, B. A., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20790-0 · Cited by 199 · see citing works
Hashimoto, Y., Kurita, M., Aiso, S., Nishimoto, I., & Matsuoka, M. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-02-0168 · Cited by 198 · see citing works
Kang, S., Dahl, R. S., Hsieh, W., Shin, A. C., Zsebo, K. M., Buettner, C., Hajjar, R. J., & Lebeche, D. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.705012 · Cited by 189 · see citing works
The Limits of Exercise Physiology: From Performance to Health
Gabriel, B. M., & Zierath, J. R. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.04.018 · Cited by 188 · see citing works
Mitochondrially derived peptides as novel regulators of metabolism
Kim, S., Xiao, J., Wan, J., Cohen, P., & Yen, K. (2017) · The Journal of Physiology · doi:10.1113/jp274472 · Cited by 184 · see citing works
Place, N., Ivarsson, N., Venckūnas, T., Neyroud, D., Brazaitis, M., Cheng, A. J., Ochala, J., Kamandulis, S., Girard, S., Volungevičius, G., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1507176112 · Cited by 183 · see citing works
Bishop, D. J., Botella, J., Genders, A. J., Lee, M. J.-C., Saner, N. J., Kuang, J., Yan, X., & Granata, C. (2019) · Physiology · doi:10.1152/physiol.00038.2018 · Cited by 180 · see citing works
Self-citationMOXI Is a Mitochondrial Micropeptide That Enhances Fatty Acid β-Oxidation
Makarewich, C. A., Baskin, K. K., Munir, A. Z., Bezprozvannaya, S., Sharma, G., Khemtong, C., Shah, A. M., McAnally, J., Malloy, C. R., Szweda, L. I., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.058 · Cited by 170 · see citing works
Defective Signaling Through Akt-2 and -3 But Not Akt-1 in Insulin-Resistant Human Skeletal Muscle
Brozinick, J. T., Roberts, B. R., & Dohm, G. L. (2003) · Diabetes · doi:10.2337/diabetes.52.4.935 · Cited by 164 · see citing works
Xu, H., & Remmen, H. V. (2021) · Skeletal Muscle · doi:10.1186/s13395-021-00280-7 · Cited by 150 · see citing works
Xu, X., Chua, C. C., Gao, J., Chua, K., Wang, H., Hamdy, R. C., & Chua, B. H. L. (2008) · Brain Research · doi:10.1016/j.brainres.2008.06.018 · Cited by 149 · see citing works
Maurya, S. K., Bal, N. C., Sopariwala, D. H., Pant, M., Rowland, L. A., Shaikh, S. A., & Periasamy, M. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.636878 · Cited by 146 · see citing works
Mitochondrial peptide BRAWNIN is essential for vertebrate respiratory complex III assembly
Zhang, S., Reljić, B., Liang, C., Kerouanton, B., Francisco, J. C., Peh, J. H., Mary, C., Jagannathan, N. S., Olexiouk, V., Tang, C., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14999-2 · Cited by 143 · see citing works
The role of extracellular vesicles in skeletal muscle and systematic adaptation to exercise
Vechetti, I. J., Valentino, T., Mobley, C. B., & McCarthy, J. J. (2021) · The Journal of Physiology · doi:10.1113/jp278929 · Cited by 141 · see citing works
Mitochondrial-derived peptides in energy metabolism
Merry, T. L., Chan, A., Woodhead, J. S. T., Reynolds, J. C., Kumagai, H., Kim, S.-J., & Lee, C. (2020) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00249.2020 · Cited by 141 · see citing works
Hoang, P. T., Park, P., Cobb, L. J., Paharkova-Vatchkova, V., Hakimi, M., Cohen, P., & Lee, K. (2009) · Metabolism · doi:10.1016/j.metabol.2009.08.001 · Cited by 140 · see citing works
Granata, C., Oliveira, R. S. F., Little, J. P., Renner, K., & Bishop, D. J. (2016) · The FASEB Journal · doi:10.1096/fj.201500100r · Cited by 135 · see citing works
Self-citationRegulation of Gene Expression in Skeletal Muscle by Contractile Activity
Williams, R. S., & Neufer, P. D. (1996) · Comprehensive physiology · doi:10.1002/cphy.cp120125 · Cited by 132 · see citing works
Smith, I. C. P., Bombardier, É., Vigna, C., & Tupling, A. R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068924 · Cited by 128 · see citing works
Circulating humanin levels are associated with preserved coronary endothelial function
Widmer, R. J., Flammer, A. J., Herrmann, S. M., Rodriguez-Porcel, M. G., Wan, J., Cohen, P., Lerman, L. O., & Lerman, A. (2012) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00765.2012 · Cited by 117 · see citing works
Mitochondrial stress and mitokines in aging
Burtscher, J., Soltany, A., Visavadiya, N. P., Burtscher, M., Millet, G. P., Khoramipour, K., & Khamoui, A. V. (2023) · Aging Cell · doi:10.1111/acel.13770 · Cited by 116 · see citing works
LINC00116 codes for a mitochondrial peptide linking respiration and lipid metabolism
Chugunova, A. A., Loseva, E., Mazin, P., Mitina, A., Navalayeu, T., Bilan, D. S., Vishnyakova, P., Marey, M. V., Golovina, A. Y., Serebryakova, M. V., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1809105116 · Cited by 115 · see citing works
Mitochondria-derived peptides in aging and healthspan
Miller, B., Kim, S.-J., Kumagai, H., Yen, K., & Cohen, P. (2022) · Journal of Clinical Investigation · doi:10.1172/jci158449 · Cited by 115 · see citing works
Kim, S., Guerrero, N., Wassef, G., Xiao, J., Mehta, H. H., Cohen, P., & Yen, K. (2016) · Oncotarget · doi:10.18632/oncotarget.10380 · Cited by 114 · see citing works
Revisiting sORFs: overcoming challenges to identify and characterize functional microproteins
Schlesinger, D., & Elsässer, S. J. (2021) · FEBS Journal · doi:10.1111/febs.15769 · Cited by 111 · see citing works
Mitochondrial-Derived Peptides Are Down Regulated in Diabetes Subjects
Ramanjaneya, M., Bettahi, I., Jerobin, J., Chandra, P., Khalil, C. A., Skarulis, M. C., Atkin, S. L., & Abou‐Samra, A. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00331 · Cited by 110 · see citing works
Effects of fatigue and training on sarcoplasmic reticulum Ca2+regulation in human skeletal muscle
Li, J. L., Wang, X. N., Fraser, S. F., Carey, M., Wrigley, T. V., & McKenna, M. J. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00643.2000 · Cited by 106 · see citing works
Humanin and Age-Related Diseases: A New Link?
Gong, Z., Tas, E., & Muzumdar, R. H. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00210 · Cited by 102 · see citing works
The mitochondrial‐derived peptide <scp>MOTS</scp> ‐c: a player in exceptional longevity?
Fuku, N., Pareja‐Galeano, H., Zempo, H., Alis, R., Arai, Y., Lucia, A., & Hirose, N. (2015) · Aging Cell · doi:10.1111/acel.12389 · Cited by 98 · see citing works
Humanin: A mitochondrial-derived peptide in the treatment of apoptosis-related diseases
Hazafa, A., Batool, A., Ahmad, S., Amjad, M., Chaudhry, S. N., Asad, J., Ghuman, H. F., Khan, H. M., Naeem, M., & Ghani, U. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118679 · Cited by 96 · see citing works
Granata, C., Caruana, N. J., Botella, J., Jamnick, N. A., Huynh, K., Kuang, J., Janssen, H. A., Reljic, B., Mellett, N. A., Laskowski, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27153-3 · Cited by 93 · see citing works
Self-citationHuang, T., Zheng, D., Houmard, J. A., Brault, J. J., Hickner, R. C., & Cortright, R. N. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00331.2016 · Cited by 90 · see citing works
Du, C., Zhang, C., Wu, W., Liang, Y., Wang, A., Wu, S., Zhao, Y., Hou, L., Ning, Q., & Luo, X. (2018) · Pediatric Diabetes · doi:10.1111/pedi.12685 · Cited by 90 · see citing works
Yang, B., Yu, Q., Chang, B., Guo, Q., Xu, S.-T., Yi, X., & Cao, S. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2021.166126 · Cited by 90 · see citing works
MOTS-c peptide regulates adipose homeostasis to prevent ovariectomy-induced metabolic dysfunction
Lu, H., Wei, M., Zhai, Y., Li, Q., Ye, Z., Wang, L., Luo, W., Chen, J., & Lu, Z. (2019) · Journal of Molecular Medicine · doi:10.1007/s00109-018-01738-w · Cited by 84 · see citing works
Miller, B., Kim, S., Kumagai, H., Mehta, H. H., Wang, X., Liu, J., Yen, K., & Cohen, P. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112056 · Cited by 84 · see citing works
Cytochrome b5 reductase and the control of lipid metabolism and healthspan
Martín‐Montalvo, A., Sun, Y., Díaz‐Ruiz, A., Ali, A., Gutierrez, V., Palacios, H. H., Curtis, J., Siendones, E., Ariza, J., Abulwerdi, G. A., et al. (2016) · npj Aging and Mechanisms of Disease · doi:10.1038/npjamd.2016.6 · Cited by 81 · see citing works
Liu, C., Gidlund, E., Witasp, A., Qureshi, A. R., Söderberg, M. P., Thorell, A., Nader, G. A., Barany, P. F., Stenvinkel, P., & von Walden, F. (2019) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00202.2019 · Cited by 81 · see citing works
Kuliawat, R., Klein, L., Gong, Z., Nicoletta-Gentile, M., Nemkal, A., Cui, L., Bastie, C. C., Su, K., Huffman, D. M., Surana, M., et al. (2013) · The FASEB Journal · doi:10.1096/fj.13-231092 · Cited by 76 · see citing works
Nashine, S., Cohen, P., Nesburn, A. B., Kuppermann, B. D., & Kenney, M. C. (2018) · Scientific Reports · doi:10.1038/s41598-018-33290-5 · Cited by 74 · see citing works
The role of mitochondria-derived peptides in cardiovascular disease: Recent updates
Yang, Y., Gao, H., Zhou, H., Liu, Q., Qi, Z., Zhang, Y., & Zhang, J. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.109075 · Cited by 74 · see citing works
Wang, Y., Li, N., Zeng, Z., Tang, L., Zhao, S., Zhou, F., Zhou, L., Xia, W., Zhu, C., & Rao, M. (2020) · Molecular Human Reproduction · doi:10.1093/molehr/gaaa081 · Cited by 74 · see citing works
Lin, Y.-F., Xiao, M.-H., Chen, H.-X., Meng, Y., Zhao, N., Yang, L., Tang, H., Wang, J.-L., Liu, X., Zhu, Y., et al. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1767-y · Cited by 73 · see citing works
Mitochondrial-derived peptides in aging and age-related diseases
Kim, S., Miller, B., Kumagai, H., Silverstein, A. R., Flores, M., & Yen, K. (2020) · GeroScience · doi:10.1007/s11357-020-00262-5 · Cited by 73 · see citing works
Mitochondria-Derived Peptide MOTS-c: Effects and Mechanisms Related to Stress, Metabolism and Aging
Wan, W., Zhang, L., Lin, Y., Rao, X., Wang, X., Hua, F., & Ying, J. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-03885-2 · Cited by 70 · see citing works
Kim, S., Miller, B., Mehta, H. H., Xiao, J., Wan, J., Arpawong, T. E., Yen, K., & Cohen, P. (2019) · Physiological Reports · doi:10.14814/phy2.14171 · Cited by 66 · see citing works
Potential Roles of Humanin on Apoptosis in the Heart
Charununtakorn, S. T., Shinlapawittayatorn, K., Chattipakorn, S. C., & Chattipakorn, N. (2015) · Cardiovascular Therapeutics · doi:10.1111/1755-5922.12168 · Cited by 65 · see citing works
Gidlund, E., von Walden, F., Venojärvi, M., Risérus, U., Heinonen, O. J., Norrbom, J., & Sundberg, C. J. (2016) · Physiological Reports · doi:10.14814/phy2.13063 · Cited by 64 · see citing works
Plasma Mots-C Levels are Associated with Insulin Sensitivity in Lean but Not in Obese Individuals
Cataldo, L. R., Fernández‐Verdejo, R., Santos, J. L., & Galgani, J. E. (2018) · Journal of Investigative Medicine · doi:10.1136/jim-2017-000681 · Cited by 62 · see citing works
Mitochondrial-encoded MOTS-c prevents pancreatic islet destruction in autoimmune diabetes
Kong, B. S., Min, S. H., Lee, C. D., & Cho, Y. M. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109447 · Cited by 62 · see citing works
Mitochondrial microproteins link metabolic cues to respiratory chain biogenesis
Liang, C., Zhang, S., Robinson, D. R. L., Ploeg, M. R. V., Wilson, R. J., Nah, J. M., Taylor, D. F., Beh, S., Lim, R., Sun, L., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111204 · Cited by 60 · see citing works
Self-citationThe micropeptide LEMP plays an evolutionarily conserved role in myogenesis
Wang, L., Fan, J., Han, L., Qi, H., Wang, Y., Wang, H., Chen, S., Du, L., Li, S., Zhang, Y., et al. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-2570-5 · Cited by 59 · see citing works
Woodhead, J. S. T., D’Souza, R. F., Hedges, C. P., Wan, J., Berridge, M. V., Cameron-Smith, D., Cohen, P., Hickey, A. J. R., Mitchell, C. J., & Merry, T. L. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00032.2020 · Cited by 57 · see citing works
Guo, Q., Chang, B., Yu, Q., Xu, S.-T., Yi, X., & Cao, S. (2020) · Diabetologia · doi:10.1007/s00125-020-05269-3 · Cited by 57 · see citing works
Mitochondrial trifunctional protein defects: Clinical implications and therapeutic approaches
Rector, R. S., Payne, R. M., & Ibdah, J. A. (2008) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2008.04.014 · Cited by 56 · see citing works
A Mitochondrially Encoded Hormone Ameliorates Obesity and Insulin Resistance
Zarse, K., & Ristow, M. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.02.013 · Cited by 56 · see citing works
Exercise Pills: At the Starting Line
Li, S., & Laher, I. (2015) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2015.08.014 · Cited by 54 · see citing works
A pro-diabetogenic mtDNA polymorphism in the mitochondrial-derived peptide, MOTS-c
Zempo, H., Kim, S., Fuku, N., Nishida, Y., Higaki, Y., Wan, J., Yen, K., Miller, B., Vicinanza, R., Miyamoto‐Mikami, E., et al. (2021) · Aging · doi:10.18632/aging.202529 · Cited by 54 · see citing works
Fisher, M. E., Bovo, E., Cho, E. E., et al. (2021) · eLife · doi:10.7554/elife.65545 · Cited by 54 · see citing works
Voigt, A., & Jelinek, H. F. (2016) · Physiological Reports · doi:10.14814/phy2.12796 · Cited by 48 · see citing works
Transcriptomic Profiling of Skeletal Muscle Adaptations to Exercise and InactivityPreprint
Pillon, N. J., Gabriel, B. M., Dollet, L., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/813048 · Cited by 48 · see citing works
Humanin promotes mitochondrial biogenesis in pancreatic MIN6 β-cells
Qin, Q., Jin, J., He, F., Zheng, Y., Li, T., Zhang, Y., & He, J.-D. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.02.071 · Cited by 46 · see citing works
Role of humanin, a mitochondrial-derived peptide, in cardiovascular disorders
Rochette, L., Méloux, A., Zeller, M., Cottin, Y., & Vergely, C. (2020) · Archives of cardiovascular diseases · doi:10.1016/j.acvd.2020.03.020 · Cited by 46 · see citing works
Mitoregulin Controls β-Oxidation in Human and Mouse Adipocytes
Friesen, M., Warren, C. R., Yu, H., Toyohara, T., Ding, Q., Florido, M. H. C., Sayre, C., Pope, B. D., Goff, L. A., Rinn, J. L., et al. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.03.002 · Cited by 45 · see citing works
Humanin detected in skeletal muscles of MELAS patients: a possible new therapeutic agent
Kariya, S., Hirano, M., Furiya, Y., Sugie, K., & Ueno, S. (2005) · Acta Neuropathologica · doi:10.1007/s00401-004-0965-5 · Cited by 42 · see citing works
Williams, C. J., Li, Z., Harvey, N. R., Lea, R. A., Gurd, B. J., Bonafiglia, J. T., Papadimitriou, I. D., Jacques, M., Croci, I., Stensvold, D., et al. (2021) · Journal of Biomedical Science · doi:10.1186/s12929-021-00733-7 · Cited by 42 · see citing works
Self-citationAcute endurance exercise stimulates circulating levels of mitochondrial-derived peptides in humans
von Walden, F., Fernandez‐Gonzalo, R., Norrbom, J., Emanuelsson, E. B., Figueiredo, V. C., Gidlund, E., Norrbrand, L., Liu, C., Sandström, P., Hansson, B., et al. (2021) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00706.2019 · Cited by 42 · see citing works
The sarcoplasmic reticulum and SERCA: a nexus for muscular adaptive thermogenesis
Gamu, D., Juracic, E. S., Hall, K. J., & Tupling, A. R. (2019) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2019-0067 · Cited by 40 · see citing works
Kwon, C., Sun, J. L., Jeong, J. H., & Jung, T. W. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.03.128 · Cited by 40 · see citing works
Kariya, S., Hirano, M., Furiya, Y., & Ueno, S. (2005) · Neuropeptides · doi:10.1016/j.npep.2004.11.004 · Cited by 38 · see citing works
Lipids and insulin regulate mitochondrial‐derived peptide (MOTS‐c) in PCOS and healthy subjects
Ramanjaneya, M., Jerobin, J., Bettahi, I., Bensila, M., Aye, M., Siveen, K. S., Sathyapalan, T., Skarulis, M. C., Abou‐Samra, A., & Atkin, S. L. (2019) · Clinical Endocrinology · doi:10.1111/cen.14007 · Cited by 38 · see citing works
Duhamel, T. A., Stewart, R. D., Tupling, A. R., et al. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00437.2007 · Cited by 36 · see citing works
Dieli-Conwright, C. M., Sami, N., Norris, M. K., Wan, J., Kumagai, H., Kim, S., & Cohen, P. (2021) · Scientific Reports · doi:10.1038/s41598-021-96419-z · Cited by 36 · see citing works
Bupha‐Intr, T., Laosiripisan, J., & Wattanapermpool, J. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00407.2009 · Cited by 34 · see citing works
The transmembrane peptide DWORF activates SERCA2a via dual mechanisms
Li, A., Yuen, S. L., Stroik, D. R., et al. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100412 · Cited by 34 · see citing works
Tarp, J., Fagerland, M. W., Dalene, K. E., Johannessen, J. S., Hansen, B. H., Jefferis, B. J. M. H., Whincup, P. H., Diaz, K. M., Hooker, S. P., Howard, V. J., et al. (2021) · British Journal of Sports Medicine · doi:10.1136/bjsports-2021-104827 · Cited by 34 · see citing works
Zhong, P., Peng, J., Hu, Y., Zhang, J., & Shen, C. (2022) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.17551 · Cited by 34 · see citing works
Central effects of humanin on hepatic triglyceride secretion
Gong, Z., Su, K., Cui, L., Tas, E., Zhang, T., Dong, H. H., Yakar, S., & Muzumdar, R. H. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00043.2015 · Cited by 33 · see citing works
Eshima, H. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.758316 · Cited by 32 · see citing works
Discordant skeletal muscle gene and protein responses to exercise
Bishop, D. J., Hoffman, N. J., Taylor, D. F., Saner, N. J., Lee, M. J.-C., & Hawley, J. A. (2023) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2023.08.005 · Cited by 32 · see citing works
Self-citationHyatt, H. W., & Powers, S. K. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.615351 · Cited by 31 · see citing works
Reassessing the relationship between mRNA levels and protein abundance in exercised skeletal muscles
Bishop, D. J., & Hawley, J. A. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00541-3 · Cited by 31 · see citing works
Self-citationMorales, E. D., Yue, Y., Watkins, T. B., et al. (2023) · Journal of the American Heart Association · doi:10.1161/jaha.122.027480 · Cited by 30 · see citing works
A CRISPR view of the 2020 Nobel Prize in Chemistry
Uyhazi, K. E., & Bennett, J. (2020) · Journal of Clinical Investigation · doi:10.1172/jci145214 · Cited by 29 · see citing works
Current Progress of Mitochondrial Genome Editing by CRISPR
Yin, T., Luo, J., Huang, D.-Q., & Li, H. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.883459 · Cited by 29 · see citing works
Sequeira, I. R., Woodhead, J. S. T., Chan, A., D’Souza, R. F., Wan, J., Hollingsworth, K. G., Plank, L. D., Cohen, P., Poppitt, S. D., & Merry, T. L. (2021) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2021.129991 · Cited by 27 · see citing works
Mitochondrial-derived peptides and exercise
Woodhead, J. S. T., & Merry, T. L. (2021) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2021.130011 · Cited by 27 · see citing works
Morissette, M., Susser, S. E., Stammers, A. N., O’Hara, K. A., Gardiner, P. F., Sheppard, P. C., Moffatt, T. L., & Duhamel, T. A. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00092.2014 · Cited by 26 · see citing works
Small Open Reading Frames: How Important Are They for Molecular Evolution?
Guerra-Almeida, D., & da Fonseca, R. N. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.574737 · Cited by 24 · see citing works
Kinnunen, S., & Mänttäri, S. (2012) · Journal of Muscle Research and Cell Motility · doi:10.1007/s10974-012-9290-0 · Cited by 23 · see citing works
Yu, W. D., Kim, Y. J., Cho, M. J., Seok, J., Kim, G. J., Lee, C. D., Ko, J. J., Kim, Y. S., & Lee, J. H. (2021) · Mitochondrion · doi:10.1016/j.mito.2021.02.010 · Cited by 23 · see citing works
Wang, Y., Zeng, Z., Zhao, S., Tang, L., Yan, J., Li, N., Zou, L., Fan, X., Xu, C., Huang, J., et al. (2021) · Endocrinology · doi:10.1210/endocr/bqab056 · Cited by 22 · see citing works
Mitochondrial peptide Mtln contributes to oxidative metabolism in mice
Averina, O. A., Permyakov, O. A., Emelianova, M. A., Grigoryeva, O. O., Gulyaev, M. V., Pavlova, O. S., Mariasina, S. S., Frolova, O., Kurkina, M. V., Baydakova, G., et al. (2022) · Biochimie · doi:10.1016/j.biochi.2022.09.009 · Cited by 22 · see citing works
Gejl, K. D., Andersson, E. P., Nielsen, J., Holmberg, H., & Ørtenblad, N. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00810 · Cited by 21 · see citing works
Hyatt, J. K. (2022) · Physiological Reports · doi:10.14814/phy2.15377 · Cited by 21 · see citing works
MOTS-c: an equal opportunity insulin sensitizer
Kim, S., Miller, B., Kumagai, H., Yen, K., & Cohen, P. (2019) · Journal of Molecular Medicine · doi:10.1007/s00109-019-01758-0 · Cited by 20 · see citing works
Zhang, P., Cui, Z., & Li, S. (2021) · Bioengineered · doi:10.1080/21655979.2021.1979914 · Cited by 19 · see citing works
Microproteins in skeletal muscle: hidden keys in muscle physiology
Bonilauri, B., & Dallagiovanna, B. (2021) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12866 · Cited by 19 · see citing works
Differential Effects of Exercise Training on Skeletal Muscle SERCA Gene Expression
Kubo, H., Libonati, J. R., Kendrick, Z. V., PAOLONE, A. M., Gaughan, J., & Houser, S. R. (2003) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200301000-00005 · Cited by 16 · see citing works
Ma, Y., Li, S., Wei, X., Huang, J., Lai, M., Wang, N., Huang, Q., Zhao, L., Peng, Y., & Wang, Y. (2018) · Gynecological Endocrinology · doi:10.1080/09513590.2018.1482869 · Cited by 12 · see citing works
Sarcolipin expression in human skeletal muscle: Influence of energy balance and exercise
Morales‐Álamo, D., Martinez‐Canton, M., Gelabert‐Rebato, M., Martín-Rincón, M., de Pablos-Velasco, P. L., Holmberg, H., & Calbet, J. A. L. (2019) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.13594 · Cited by 12 · see citing works
[The level of circulating humanin in patients with ischemic heart disease.]
Жлоба, А. А., Subbotina, T. F., Сергеевич, М. Н., & Polushin, Y. S. (2018) · PubMed · doi:10.18821/0869-2084-2018-63-8-466-470 · Cited by 10 · see citing works
The protective effects of S14G-humanin on gestational diabetes mellitus symptoms
Jiang, H., Xu, Y., & Cao, L. (2022) · Gynecological Endocrinology · doi:10.1080/09513590.2022.2073348 · Cited by 4 · see citing works
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Exerkines and Sarcopenia: Unveiling the Mechanism Behind Exercise-Induced Mitochondrial Homeostasis
Wang, J., Jia, D., Zhang, Z., & Wang, D. (2025) · Metabolites · doi:10.3390/metabo15010059 · Cited by 23 · see citing works
- Authors
- Atakan, M. M., Türkel, İ., Özerkliğ, B., Koşar, Ş. N., Taylor, D. F., Yan, X., & Bishop, D. J.
- Affiliations
- Hacettepe University (TR)
- Victoria University (AU)
- Australian Institute for Musculoskeletal Science (AU)
- Corresponding author
- Bishop, David J.
- ORCID
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2024-01-09
- Volume
- 602
- Issue
- 4
- Pages
- 545-568
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- OpenAlex
- W4390700673
- Cited by
- 13
- References
- 157
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 3
- FWCI
- 0.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Journal of Physiology (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Victoria University
- Topics
- Health Sciences › Medicine › Rehabilitation › Exercise and Physiological Responses
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Keywords
- small peptides, small open reading frames, exercise-induced adaptations, metabolism, exercise training, metabolic disorders, skeletal muscle, disease prevention
- MeSH terms
- Peptides, Open Reading Frames
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