Effect of triiodothyronine on mitochondrial energy coupling in human skeletal muscle
Open accessAbstract
The mechanism underlying the regulation of basal metabolic rate by thyroid hormone remains unclear. Although it has been suggested that thyroid hormone might uncouple substrate oxidation from ATP synthesis, there are no data from studies on humans to support this hypothesis. To examine this possibility, we used a novel combined 13C/31P nuclear magnetic resonance (NMR) approach to assess mitochondrial energy coupling in skeletal muscle of seven healthy adults before and after three days of triiodothyronine (T3) treatment. Rates of ATP synthesis and tricarboxylic acid (TCA) cycle fluxes were measured by 31P and 13C NMR spectroscopy, respectively, and mitochondrial energy coupling was assessed as the ratio. Muscle TCA cycle flux increased by approximately 70% following T3 treatment. In contrast, the rate of ATP synthesis remained unchanged. Given the disproportionate increase in TCA cycle flux compared with ATP synthesis, these data suggest that T3 promotes increased thermogenesis in part by promoting mitochondrial energy uncoupling in skeletal muscle.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Short-term studies of supraphysiologic thyroid hormone doses uniformly showed increased resting and 24-hour energy expenditure, but were too brief to document changes in body composition.
“These studies uniformly showed increased resting and 24-hour energy expenditure, but were too brief to document changes in body composition.”
From Effects of levothyroxine replacement or suppressive therapy on energy expenditure and body composition (2016) · cites this paper as [7]
Most prior studies of supraphysiologic thyroid hormone doses utilized high doses of levotriiodothyronine (LT3), not minimally suppressive doses of LT4.
“In addition, most utilized high doses of levotriiodothyronine (LT3), not minimally suppressive doses of LT4.”
From Effects of levothyroxine replacement or suppressive therapy on energy expenditure and body composition (2016) · cites this paper as [7]
Past studies have reported increased resting or 24-hour energy expenditure and whole body oxygen consumption with exogenous administration of pharmacologic doses of LT4 or LT3 to healthy humans due to increased expression of uncoupling proteins and decreased mitochondrial efficiency.
“Past studies have reported increased resting or 24-hour energy expenditure and whole body oxygen consumption with exogenous administration of pharmacologic doses of LT4 or LT3 to healthy humans (3-7) due to increased expression of uncoupling proteins and decreased mitochondrial efficiency (3,4,7).”
From Effects of levothyroxine replacement or suppressive therapy on energy expenditure and body composition (2016) · cites this paper as [7]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Overweight and obesity in the United States: prevalence and trends, 1960–1994
Flegal, K., Carroll, M., Kuczmarski, R., & Johnson, C. (1998) · International Journal of Obesity · doi:10.1038/sj.ijo.0800541 · Cited by 3,045 · see citing works
Cellular mechanisms of insulin resistance
Shulman, G. I. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10583 · Cited by 2,714 · see citing works
Self-citationBoss, O., Samec, S., Paoloni‐Giacobino, A., Rossier, C., Dulloo, A. G., Seydoux, J., Muzzin, P., & Giacobino, J. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00384-0 · Cited by 1,041 · see citing works
Harris, R. C., Hultman, E., & Nordesjö, L. ‐. (1974) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.3109/00365517409082477 · Cited by 857 · see citing works
Brodie, S. E. (1996) · Survey of Ophthalmology · doi:10.1016/s0039-6257(96)80075-0 · Cited by 770 · see citing works
Gong, D., He, Y., Karas, M., & Reitman, M. L. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.39.24129 · Cited by 740 · see citing works
Quantification of the contribution of various steps to the control of mitochondrial respiration.
Groen, A. K., Wanders, R. J. A., Westerhoff, H. V., van der Meer, R., & Tager, J. M. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)81026-8 · Cited by 629 · see citing works
Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean
Clapham, J. C., Arch, J. R. S., Chapman, H., Haynes, A., Lister, C., Moore, G. B. T., Piercy, V., Carter, S. A., Lehner, I., Smith, S. A., et al. (2000) · Nature · doi:10.1038/35019082 · Cited by 604 · see citing works
Gong, D., Monemdjou, S., Gavrilova, O., Leon, L. R., Marcus‐Samuels, B., Chou, C. J., Everett, C. A., Kozak, L. P., Li, C., Deng, C., et al. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m910177199 · Cited by 385 · see citing works
Harris, R. C., Hultman, E., & Nordesjö, L. O. (1974) · PubMed · Cited by 315 · see citing works
NMR Determination of the TCA Cycle Rate and α-Ketoglutarate/Glutamate Exchange Rate in Rat Brain
Mason, G. F., Rothman, D. L., Behar, K. L., & Shulman, R. G. (1992) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1992.61 · Cited by 249 · see citing works
Self-citationMechanism of Thyroid Calorigenesis: Role of Active Sodium Transport
Ismail‐Beigi, F., & Edelman, I. S. (1970) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.67.2.1071 · Cited by 243 · see citing works
Metabolism of Tissues Excised From Thyroxine-Injected Rats
Barker, S. B., & Klitgaard, H. M. (1952) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1952.170.1.81 · Cited by 239 · see citing works
Substrate cycles in metabolic regulation and in heat generation.
Newsholme, E. A., & Crabtree, B. (1976) · PubMed · Cited by 235 · see citing works
Gustafsson, R. G., Tata, J. R., Lindberg, O. R., & Ernster, L. (1965) · The Journal of Cell Biology · doi:10.1083/jcb.26.2.555 · Cited by 216 · see citing works
The mode of action of thyroxin
Martius, C. A., & Hess, B. (1951) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(51)90137-3 · Cited by 181 · see citing works
Regulation of the Third Member of the Uncoupling Protein Family, UCP3, by Cold and Thyroid Hormone
Larkin, S., Mull, E., Miao, W., Pittner, R. A., Albrandt, K., Moore, C., Young, A., Denaro, M., & Beaumont, K. C. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.7636 · Cited by 178 · see citing works
Thermogenesis and Thyroid Function
Freake, H. C., & Oppenheimer, J. H. (1995) · Annual Review of Nutrition · doi:10.1146/annurev.nu.15.070195.001403 · Cited by 177 · see citing works
Hafner, R. P., Nobes, C. D., McGown, A. D., & Brand, M. D. (1988) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1988.tb14477.x · Cited by 151 · see citing works
Improvements on an in Vivo automatic shimming method (FASTERMAP)
Shen, J., Rycyna, R. E., & Rothman, D. L. (1997) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910380521 · Cited by 123 · see citing works
Self-citationBarbe, P., Larrouy, D., Boulanger, C., Chevillotte, E., Viguerie, N., Thalamas, C., Oliva Trastoy, M., Roques, M., Vidal, H., & Langin, D. (2001) · The FASEB Journal · doi:10.1096/fj.00-0502fje · Cited by 118 · see citing works
Lanni, A., Beneduce, L., Lombardi, A., Moreno, M., Boss, O., Muzzin, P., Giacobino, J., & Goglia, F. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)00061-7 · Cited by 112 · see citing works
Field, J., Belding, H. S., & Martin, A. W. (1939) · Journal of Cellular and Comparative Physiology · doi:10.1002/jcp.1030140202 · Cited by 110 · see citing works
Shulman, G. I., Ladenson, P. W., WOLFE, M. H., Ridgway, E. C., & Wolfe, R. R. (1985) · Journal of Clinical Investigation · doi:10.1172/jci112032 · Cited by 102 · see citing works
Self-citationThe mechanism of the increase in mitochondrial proton permeability induced by thyroid hormones
Brand, M. D., Steverding, D., Kadenbach, B., Stevenson, P. M., & Hafner, R. P. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb16984.x · Cited by 101 · see citing works
METABOLIC EFFECTS OF THYROXINE IN VITRO
Lardy, H. A., & Feldott, G. (1951) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1951.tb54465.x · Cited by 101 · see citing works
Assessment of mitochondrial energy coupling in vivo by 13 C/ 31 P NMR
Jucker, B. M., Dufour, S., Ren, J., Cao, X., Previs, S. F., Underhill, B., Cadman, K. S., & Shulman, G. I. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.120131997 · Cited by 99 · see citing works
Self-citationMETABOLIC EFFECTS OF THYROXINE IN VITRO
Lardy, H. A., & Feldott, G. (1951) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1951.tb46619.x · Cited by 94 · see citing works
Chatham, J. C., Forder, J. R., Glickson, J. D., & Chance, E. M. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.14.7999 · Cited by 93 · see citing works
Jekabsons, M. B., Gregoire, F. M., SCHONFELD-WARDEN, N. A., Warden, C. H., & Horwitz, B. A. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.277.2.e380 · Cited by 58 · see citing works
Cusin, I., Rouru, J., Visser, T. J., Burger, A., & Rohner‐Jeanrenaud, F. (2000) · Diabetes · doi:10.2337/diabetes.49.7.1101 · Cited by 49 · see citing works
Indirect measurement of mitochondrial proton leak and its application
Porter, R. K., Joyce, O., Farmer, M., Heneghan, R., Tipton, K. F., Andrews, J., McBennett, S., Lund, M., Jensen, C., & Melia, H. P. (1999) · International Journal of Obesity · doi:10.1038/sj.ijo.0800937 · Cited by 36 · see citing works
Pedersen, S. B., Kristensen, K., Fisker, S., Jørgensen, J. O. L., Christiansen, J. S., & Richelsen, B. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.11.6109 · Cited by 27 · see citing works
Expression of rat uncoupling protein family mRNA levels by chronic treatment with thyroid hormone
Masaki, T., Yoshimatsu, H., & Sakata, T. (2000) · International Journal of Obesity · doi:10.1038/sj.ijo.0801315 · Cited by 25 · see citing works
Pedersen, S. B. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.11.4073 · Cited by 15 · see citing works
(2000) · International Journal of Obesity · doi:10.1038/sj/ijo/0801315 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Mason, G.F. 2000. CWave: software for the design and analysis of 13 C labeling studies performed in vivo. Proc. Intl. Soc. Mag. Reson. Med. 3:1870 (Abstr.)
- Field, J., Beldings, H.S., and Martin, A.W. 1939. An analysis of the rela- tion between basal metabolism and summated tissue respiration in the rat. Journal of Cellular and Comparative Physiology. 14:143-157.
Cited by
Sorted by citations
Impaired Mitochondrial Activity in the Insulin-Resistant Offspring of Patients with Type 2 Diabetes
Petersen, K. F., Dufour, S., Befroy, D., Garcia, R., & Shulman, G. I. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa031314 · Cited by 2,193 · see citing works
Self-citationMitochondrial dysfunction in the elderly: possible role in insulin resistance
Petersen, K. F., Befroy, D., Dufour, S., Dziura, J., Ariyan, C., Rothman, D. L., DiPietro, L., Cline, G. W., & Shulman, G. I. (2003) · Science · doi:10.1126/science.1082889 · Cited by 2,107 · see citing works
Self-citationLipid-induced insulin resistance: unravelling the mechanism
Samuel, V. T., Petersen, K. F., & Shulman, G. I. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60408-4 · Cited by 1,189 · see citing works
Self-citationDisordered lipid metabolism and the pathogenesis of insulin resistance.
Savage, D. B., Petersen, K. F., & Shulman, G. I. (2007) · Physiological Reviews · doi:10.1152/physrev.00024.2006 · Cited by 1,107 · see citing works
Self-citationCellular and Molecular Basis of Deiodinase-Regulated Thyroid Hormone Signaling1
Gereben, B., Zavacki, A. M., Ribich, S., Kim, B. W., Huang, S. A., Simonides, W. S., Zeöld, A., & Bianco, A. C. (2008) · Endocrine Reviews · doi:10.1210/er.2008-0019 · Cited by 891 · see citing works
Deiodinases: implications of the local control of thyroid hormone action
Bianco, A. C., & Kim, B. W. (2006) · Journal of Clinical Investigation · doi:10.1172/jci29812 · Cited by 845 · see citing works
Leptin reverses insulin resistance and hepatic steatosis in patients with severe lipodystrophy
Petersen (2002) · Journal of Clinical Investigation · doi:10.1172/jci0215001 · Cited by 622 · see citing works
Self-citationReinehr, T. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.06.005 · Cited by 500 · see citing works
Befroy, D. E., Petersen, K. F., Dufour, S., Mason, G. F., de Graaf, R. A., Rothman, D. L., & Shulman, G. I. (2007) · Diabetes · doi:10.2337/db06-0783 · Cited by 453 · see citing works
Self-citationKurdiova, T., Balaz, M., Vician, M., Maderova, D., Vlcek, M., Valkovic, L., Srbecky, M., Imrich, R., Kyselovicova, O., Belan, V., et al. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2013.264655 · Cited by 401 · see citing works
Thyroid hormones and skeletal muscle—new insights and potential implications
Salvatore, D., Simonides, W. S., Dentice, M., Zavacki, A. M., & Larsen, P. R. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.238 · Cited by 389 · see citing works
Thyroid Hormone as a Determinant of Energy Expenditure and the Basal Metabolic Rate
Kim, B. W. (2008) · Thyroid · doi:10.1089/thy.2007.0266 · Cited by 383 · see citing works
Energy metabolism, fuel selection and body weight regulation
Galgani, J. E., & Ravussin, É. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.246 · Cited by 372 · see citing works
The TRH neuron: a hypothalamic integrator of energy metabolism
Lechan, R. M., & Fekete, C. (2006) · Progress in brain research · doi:10.1016/s0079-6123(06)53012-2 · Cited by 338 · see citing works
Implications of nonshivering thermogenesis for energy balance regulation in humans
Lichtenbelt, W. D. V. M., & Schrauwen, P. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00652.2010 · Cited by 306 · see citing works
Petersen, K. F., Dufour, S., & Shulman, G. I. (2005) · PLoS Medicine · doi:10.1371/journal.pmed.0020233 · Cited by 308 · see citing works
Self-citationChoi, C. S., Befroy, D. E., Codella, R., Kim, S., Reznick, R. M., Hwang, Y.-J., Liu, Z.-X., Lee, H.-Y., Distefano, A., Samuel, V. T., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810339105 · Cited by 279 · see citing works
Self-citationThyroid hormone mimetics: potential applications in atherosclerosis, obesity and type 2 diabetes
Baxter, J. D., & Webb, P. (2009) · Nature Reviews Drug Discovery · doi:10.1038/nrd2830 · Cited by 253 · see citing works
Chapter 20: Functional Assessment of Isolated Mitochondria In Vitro
Lanza, I. R., & Nair, K. S. (2009) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(09)05020-4 · Cited by 248 · see citing works
Muscle Mitochondrial ATP Synthesis and Glucose Transport/Phosphorylation in Type 2 Diabetes
Szendroedi, J., Schmid, A. I., Chmelik, M., Toth, C., Brehm, A., Krssak, M., Nowotny, P., Wolzt, M., Waldhausl, W., & Roden, M. (2007) · PLoS Medicine · doi:10.1371/journal.pmed.0040154 · Cited by 243 · see citing works
Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle
Brehm, A., Krssak, M., Schmid, A. I., Nowotny, P., Waldhäusl, W., & Roden, M. (2006) · Diabetes · doi:10.2337/diabetes.55.01.06.db05-1286 · Cited by 239 · see citing works
Mild mitochondrial uncoupling impacts cellular aging in human muscles in vivo
Amara, C. E., Shankland, E. G., Jubrias, S. A., Marcinek, D. J., Kushmerick, M. J., & Conley, K. E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610131104 · Cited by 223 · see citing works
Anti-obesity therapy: from rainbow pills to polyagonists
Müller, T. D., Clemmensen, C., Finan, B., DiMarchi, R. D., & Tschöp, M. H. (2018) · Pharmacological Reviews · doi:10.1124/pr.117.014803 · Cited by 199 · see citing works
In Vivo Regulation of Human Skeletal Muscle Gene Expression by Thyroid Hormone
Clément, K., Viguerie, N., Diehn, M., Alizadeh, A., Barbe, P., Thalamas, C., Storey, J. D., Brown, P. O., Barsh, G. S., & Langin, D. (2002) · Genome Research · doi:10.1101/gr.207702 · Cited by 169 · see citing works
The Impact of Overt and Subclinical Hyperthyroidism on Skeletal Muscle
Brennan, M. D., Powell, C., Kaufman, K. R., Sun, P. C., Bahn, R. S., & Nair, K. S. (2006) · Thyroid · doi:10.1089/thy.2006.16.375 · Cited by 155 · see citing works
Thyroid hormone and uncoupling proteins
Lanni, A., Moreno, M., Lombardi, A., & Goglia, F. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)00320-x · Cited by 150 · see citing works
Links between Thyroid Hormone Action, Oxidative Metabolism, and Diabetes Risk?
Crunkhorn, S., & Patti, M. (2008) · Thyroid · doi:10.1089/thy.2007.0249 · Cited by 139 · see citing works
Adaptive Activation of Thyroid Hormone and Energy Expenditure
Bianco, A. C., Maia, A. L., da‐Silva, W. S., & Christoffolete, M. A. (2005) · Bioscience Reports · doi:10.1007/s10540-005-2885-6 · Cited by 138 · see citing works
Wijers, S. L. J., Schrauwen, P., Saris, W. H. M., & van Marken Lichtenbelt, W. D. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001777 · Cited by 135 · see citing works
Dynamic MRS and MRI of skeletal muscle function and biomechanics
Prompers, J. J., Jeneson, J. A. L., Drost, M. R., Oomens, C., Strijkers, G. J., & Nicolay, K. (2006) · NMR in Biomedicine · doi:10.1002/nbm.1095 · Cited by 133 · see citing works
Recent advances in adaptive thermogenesis: potential implications for the treatment of obesity
Wijers, S. L. J., Saris, W. H. M., & Lichtenbelt, W. D. V. M. (2009) · Obesity Reviews · doi:10.1111/j.1467-789x.2008.00538.x · Cited by 116 · see citing works
Mitchell, C. S., Savage, D. B., Dufour, S., Schoenmakers, N. A., Murgatroyd, P. R., Befroy, D. E., Halsall, D. J., Northcott, S., Raymond‐Barker, P., Curran, S., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci38793 · Cited by 115 · see citing works
Self-citationHypophosphatemia promotes lower rates of muscle ATP synthesis
Pesta, D. H., Tsirigotis, D. N., Befroy, D. E., Caballero, D., Jurczak, M. J., Rahimi, Y., Cline, G. W., Dufour, S., Birkenfeld, A. L., Rothman, D. L., et al. (2016) · The FASEB Journal · doi:10.1096/fj.201600473r · Cited by 106 · see citing works
Self-citationThe history of energetic efficiency research: Where have we been and where are we going?
Johnson, D. E., Ferrell, C. L., & Jenkins, T. G. (2003) · Journal of Animal Science · doi:10.2527/2003.8113_suppl_1e27x · Cited by 101 · see citing works
Schrauwen, P., Joris Hoeks, J., & Hesselink, M. K. C. (2005) · Progress in Lipid Research · doi:10.1016/j.plipres.2005.11.001 · Cited by 97 · see citing works
Mitochondrial dysfunction in patients with primary congenital insulin resistance
Sleigh, A., Raymond‐Barker, P., Thackray, K., Porter, D. A., Hatunic, M., Vottero, A., Burren, C. P., Mitchell, C., McIntyre, M., Brage, S., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci46405 · Cited by 95 · see citing works
Befroy, D. E., Perry, R. J., Jain, N., Dufour, S., Cline, G. W., Trimmer, J. K., Brosnan, J. M., Rothman, D. L., Petersen, K. F., & Shulman, G. I. (2013) · Nature Medicine · doi:10.1038/nm.3415 · Cited by 95 · see citing works
Self-citationMitochondrial function, fibre types and ageing: new insights from human muscle in vivo
Conley, K. E., Amara, C. E., Jubrias, S. A., & Marcinek, D. J. (2006) · Experimental Physiology · doi:10.1113/expphysiol.2006.034330 · Cited by 96 · see citing works
Thyroid hormones as molecular determinants of thermogenesis
Silvestri, E., Schiavo, L., Lombardi, A., & Goglia, F. (2005) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2005.01463.x · Cited by 94 · see citing works
Packer, M. (2016) · Circulation Heart Failure · doi:10.1161/circheartfailure.116.003604 · Cited by 88 · see citing works
Samuels, M. H., Kolobova, I., Smeraglio, A., Peters, D., Purnell, J. Q., & Schuff, K. G. (2016) · Thyroid · doi:10.1089/thy.2015.0345 · Cited by 87 · see citing works
Human Uncoupling Protein‐3 and Obesity: An Update
Hesselink, M. K. C., Mensink, M., & Schrauwen, P. (2003) · Obesity Research · doi:10.1038/oby.2003.192 · Cited by 85 · see citing works
Energy dissipation in brown adipose tissue: From mice to men
Vosselman, M. J., Lichtenbelt, W. D. V. M., & Schrauwen, P. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.04.017 · Cited by 85 · see citing works
Jamurtas, A. Z., Koutedakis, Y., Paschalis, V., Tofas, T., Yfanti, C., Tsiokanos, A., Koukoulis, G., Kouretas, D., & Loupos, D. (2004) · European Journal of Applied Physiology · doi:10.1007/s00421-004-1156-8 · Cited by 81 · see citing works
Exercise efficiency is reduced by mitochondrial uncoupling in the elderly
Conley, K. E., Jubrias, S. A., Cress, M. E., & Esselman, P. C. (2012) · Experimental Physiology · doi:10.1113/expphysiol.2012.067314 · Cited by 78 · see citing works
Goedeke, L., Perry, R. J., & Shulman, G. I. (2019) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010716-104727 · Cited by 76 · see citing works
Self-citationCollin, A., Cassy, S., Buyse, J. G., Decuypere, E. M. P., & Damon, M. (2005) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2005.02.007 · Cited by 74 · see citing works
Grozovsky, R., Ribich, S. A., Rosene, M. L., Mulcahey, M. A., Huang, S. A., Patti, M., Bianco, A. C., & Kim, B. W. (2008) · Endocrinology · doi:10.1210/en.2008-0938 · Cited by 72 · see citing works
Trenell, M. I., Hollingsworth, K. G., Lim, E. L., & Taylor, R. (2008) · Diabetes Care · doi:10.2337/dc08-0303 · Cited by 71 · see citing works
Differential effects of thyroid hormones on energy metabolism of rat slow‐ and fast‐twitch muscles
Bahi, L., Garnier, A., Fortin, D., Serrurier, B., Veksler, V., Bigard, A. X., & Ventura‐Clapier, R. (2004) · Journal of Cellular Physiology · doi:10.1002/jcp.20273 · Cited by 70 · see citing works
Mitochondrial function and endocrine diseases
Stark, R., & Roden, M. (2007) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2007.01773.x · Cited by 69 · see citing works
Chng, C. L., Lim, A. Y., Tan, H. C., Kovalik, J., Tham, K. W., Bee, Y. M., Lim, W., Acharyya, S., Lai, O. F., Chong, S. C., et al. (2016) · Thyroid · doi:10.1089/thy.2015.0602 · Cited by 69 · see citing works
Kemp, G. J., & Brindle, K. M. (2012) · Diabetes · doi:10.2337/db11-1725 · Cited by 67 · see citing works
Schär, M., El‐Sharkawy, A. M., Weiss, R. G., & Bottomley, P. A. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22347 · Cited by 68 · see citing works
Schmid, A. I., Chmelík, M., Szendroedi, J., Krššák, M., Brehm, A., Moser, E., & Roden, M. (2008) · NMR in Biomedicine · doi:10.1002/nbm.1207 · Cited by 67 · see citing works
Mitochondrial function in vivo: Spectroscopy provides window on cellular energetics
Amara, C. E., Marcinek, D. J., Shankland, E. G., Schenkman, K. A., Arakaki, L. S. L., & Conley, K. E. (2008) · Methods · doi:10.1016/j.ymeth.2008.10.001 · Cited by 65 · see citing works
Schrauwen, P., & Hesselink, M. K. C. (2003) · Proceedings of The Nutrition Society · doi:10.1079/pns2003277 · Cited by 66 · see citing works
Mitochondrial uncoupling protein 3 and its role in cardiac- and skeletal muscle metabolism
Nabben, M., & Joris Hoeks, J. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.11.039 · Cited by 65 · see citing works
From, A. H. L., & Uǧurbil, K. (2011) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00345.2010 · Cited by 63 · see citing works
31P-Magnetization Transfer Magnetic Resonance Spectroscopy Measurements of In Vivo Metabolism
Befroy, D. E., Rothman, D. L., Petersen, K. F., & Shulman, G. I. (2012) · Diabetes · doi:10.2337/db12-0558 · Cited by 61 · see citing works
Self-citationEvolution of ligands, receptors and metabolizing enzymes of thyroid signaling
Holzer, G., Roux, N., & Laudet, V. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.03.021 · Cited by 62 · see citing works
Thyroid hormone action in metabolic regulation
Song, Y., Yao, X., & Ying, H. (2011) · Protein & Cell · doi:10.1007/s13238-011-1046-x · Cited by 59 · see citing works
Johannsen, D. L., Galgani, J. E., Johannsen, N. M., Zhang, Z., Covington, J. D., & Ravussin, E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040837 · Cited by 57 · see citing works
Combatting type 2 diabetes by turning up the heat
Schrauwen, P., & Lichtenbelt, W. D. V. M. (2016) · Diabetologia · doi:10.1007/s00125-016-4068-3 · Cited by 59 · see citing works
Eichler, R. A. D. S., Alfadda, A. A., Eto, K., Kadowaki, T., & Silva, J. E. (2003) · Endocrinology · doi:10.1210/en.2003-0687 · Cited by 58 · see citing works
Impaired insulin stimulation of muscular ATP production in patients with type 1 diabetes
Kacerovsky, M., Brehm, A., Chmelík, M., Schmid, A. I., Szendroedi, J., Kacerovsky-Bielesz, G., Nowotny, P., Lettner, A., Wolzt, M., Jones, J. G., et al. (2010) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2010.02298.x · Cited by 57 · see citing works
Weight gain following treatment of hyperthyroidism—A forgotten tale
Kyriacou, A., Kyriacou, A., Makris, K. C., Syed, A. A., & Perros, P. (2019) · Clinical Obesity · doi:10.1111/cob.12328 · Cited by 53 · see citing works
Lombardi, A., Moreno, M., de Lange, P., Iossa, S., Busiello, R. A., & Goglia, F. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00237 · Cited by 52 · see citing works
Chow, L. S., From, A. H. L., & Seaquist, E. R. (2009) · Metabolism · doi:10.1016/j.metabol.2009.07.009 · Cited by 53 · see citing works
Thyroid Hormone, Thyromimetics, and Metabolic Efficiency
Yehuda‐Shnaidman, E., Kalderon, B., & Bar‐Tana, J. (2013) · Endocrine Reviews · doi:10.1210/er.2013-1006 · Cited by 52 · see citing works
Are Alterations in Skeletal Muscle Mitochondria a Cause or Consequence of Insulin Resistance?
Genders, A. J., Holloway, G. P., & Bishop, D. J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186948 · Cited by 51 · see citing works
Chaumeil, M. M., Valette, J., Guillermier, M., Brouillet, E., Boumezbeur, F., Hérard, A., Bloch, G., Hantraye, P., & Lebon, V. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806516106 · Cited by 51 · see citing works
Self-citationArruda, A. P., da‐Silva, W. S., de Carvalho, D. P., & MEIS, L. D. (2003) · Biochemical Journal · doi:10.1042/bj20031015 · Cited by 48 · see citing works
Savage, D. B., Murgatroyd, P. R., Chatterjee, V. K., & O’Rahilly, S. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1494 · Cited by 47 · see citing works
Thyroid disease and the nervous system
Wood-Allum, C. A., & Shaw, P. J. (2013) · Handbook of clinical neurology · doi:10.1016/b978-0-7020-4087-0.00048-6 · Cited by 45 · see citing works
Genetic relationships of body composition, serum leptin, and age at puberty in gilts12
Kuehn, L. A., Nonneman, D., Klindt, J., & Wise, T. (2008) · Journal of Animal Science · doi:10.2527/jas.2008-0936 · Cited by 44 · see citing works
Kemp, G. J. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00797.2007 · Cited by 43 · see citing works
Moreno, M., Lombardi, A., De Lange, P., Silvestri, E., Ragni, M., Lanni, A., & Goglia, F. (2003) · The FASEB Journal · doi:10.1096/fj.02-0839fje · Cited by 42 · see citing works
Bays, H., & Dujovne, C. (2002) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.11.9.1189 · Cited by 40 · see citing works
Plasma proteome and metabolome characterization of an experimental human thyrotoxicosis model
Pietzner, M., Engelmann, B., Kacprowski, T., Golchert, J., Dirk, A.-L., Hammer, E., Iwen, K. A., Nauck, M., Wallaschofski, H., Führer, D., et al. (2017) · BMC Medicine · doi:10.1186/s12916-016-0770-8 · Cited by 40 · see citing works
Harper, J. M., Gałecki, A. T., Burke, D., Pinkosky, S. L., & Miller, R. A. (2003) · Physiological Genomics · doi:10.1152/physiolgenomics.00063.2003 · Cited by 39 · see citing works
Chapter 21 Assessment of In Vivo Mitochondrial Metabolism by Magnetic Resonance Spectroscopy
Befroy, D. E., Petersen, K. F., Rothman, D. L., & Shulman, G. I. (2009) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(09)05021-6 · Cited by 39 · see citing works
Self-citationHampl, R., Stárka, L., & Janský, L. (2006) · Physiological Research · doi:10.33549/physiolres.930758 · Cited by 38 · see citing works
Valkovič, L., Chmelík, M., Kukurová, I. J., Krššák, M., Gruber, S., Frollo, I., Trattnig, S., & Bogner, W. (2011) · European Journal of Radiology · doi:10.1016/j.ejrad.2011.09.024 · Cited by 37 · see citing works
Increased plasma leptin attenuates adaptive metabolism in early lactating dairy cows
Ehrhardt, R., Foskolos, A., Giesy, S. L., Wesolowski, S. R., Krumm, C. S., Butler, W. R., Quirk, S. M., Waldron, M. R., & Boisclair, Y. R. (2016) · Journal of Endocrinology · doi:10.1530/joe-16-0031 · Cited by 36 · see citing works
Reduced expression of mitochondrial frataxin in mice exacerbates diet-induced obesity
Pomplun, D., Voigt, A., Schulz, T. J., Thierbach, R., Pfeiffer, A. F. H., & Ristow, M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611631104 · Cited by 35 · see citing works
Reis, M. M., Farage, M., & MEIS, L. D. (2002) · Molecular Membrane Biology · doi:10.1080/09687680210166217 · Cited by 35 · see citing works
BRENNAN, M. D., Coenen-Schimke, J. M., Bigelow, M. L., & Nair, K. S. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-1074 · Cited by 34 · see citing works
Ren, J., Yang, B., Sherry, A. D., & Malloy, C. R. (2014) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25256 · Cited by 33 · see citing works
Self-citationAcute elevation of plasma lipids does not affect ATP synthesis in human skeletal muscle
Brehm, A., Krššák, M., Schmid, A. I., Nowotny, P., Waldhäusl, W. K., & Roden, M. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00756.2009 · Cited by 33 · see citing works
Conley, K. E., Jubrias, S. A., Cress, M. E., & Esselman, P. C. (2012) · Experimental Physiology · doi:10.1113/expphysiol.2012.069633 · Cited by 32 · see citing works
Previs, S. F., & Kelley, D. E. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00216.2015 · Cited by 31 · see citing works
Thyroid wars: the rise of central actions
Capelli, V., Diéguez, C., Mittag, J., & López, M. (2021) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2021.05.006 · Cited by 31 · see citing works
Harper, J. M., Wolf, N. S., Gałecki, A. T., Pinkosky, S. L., & Miller, R. A. (2003) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(03)00133-7 · Cited by 31 · see citing works
Svyatova, A. I., Kozinenko, V. P., Chukanov, N. V., Буруева, Д. Б., Chekmenev, E. Y., Chen, Y., Hwang, D. W., Kovtunov, K. V., & Koptyug, I. V. (2021) · Scientific Reports · doi:10.1038/s41598-021-85136-2 · Cited by 30 · see citing works
Valkovič, L., Ukropcová, B., Chmelík, M., Baláž, M., Bogner, W., Schmid, A. I., Frollo, I., Zemková, E., Klimeś, I., Ukropec, J., et al. (2013) · NMR in Biomedicine · doi:10.1002/nbm.3008 · Cited by 30 · see citing works
Schrauwen, P. (2002) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/00075197-200205000-00005 · Cited by 30 · see citing works
Bio-energetic impairment in human calf muscle in thyroid disorders: a 31P MRS study
Khushu, S., Rana, P., Sekhri, T., Gopalakrishnan, S., & Tripathi, R. P. (2010) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2010.01.006 · Cited by 30 · see citing works
Gu, Y., Meng, G., Wu, H., Zhang, Q., Liu, L., Bao, X., Wang, Y., Zhang, S., Sun, S., Wang, X., et al. (2019) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2019.06.014 · Cited by 29 · see citing works
Bays, H. E., & Dujovne, C. A. (2002) · American Journal of Cardiovascular Drugs · doi:10.2165/00129784-200202040-00004 · Cited by 27 · see citing works
- Authors
- Lebon, V., Dufour, S., Petersen, K. F., Ren, J., Jucker, B. M., Slezak, L. A., Cline, G. W., Rothman, D. L., & Shulman, G. I.
- Affiliations
- Howard Hughes Medical Institute (US)
- Yale University (US)
- Bristol-Myers Squibb (United States) (US)
- Corresponding author
- Shulman, Gerald I.
- Venue
- Journal of Clinical Investigation
- Published
- 2001-09-01
- Volume
- 108
- Issue
- 5
- Pages
- 733-737
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC209375
- OpenAlex
- W2141034558
- Cited by
- 174
- References
- 36
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 3 · 2023: 4 · 2022: 1 · 2021: 7 · 2020: 3 · 2019: 7 · 2018: 3 · 2017: 6 · 2016: 11 · 2015: 8 · 2014: 4 · 2013: 8 · 2012: 9
- FWCI
- 3.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- Yale University
- U.S. Public Health Service (P30 DK45735, R01 DK-49230)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK45735, R01DK049230, R01 DK-49230, P30DK045735)
- National Center for Research Resources (M01RR000125, M01 RR-00125)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
- Keywords
- triiodothyronine, thyroid hormones, uncoupling, skeletal muscle, basal metabolic rate, thermogenesis, ATP production, TCA cycle flux, substrate oxidation
- MeSH terms
- Adenosine Triphosphate, Adult, Citric Acid Cycle, Female, Humans, Male, Mitochondria, Magnetic Resonance Spectroscopy, Oxidative Phosphorylation, Triiodothyronine, Muscle, Skeletal, Glutamic Acid
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