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(The FASEB Journal. 2004;18:39-51.)
© 2004 FASEB

Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression

STEWART H. LECKER1, R. THOMAS JAGOE*,1, ALEXANDER GILBERT, MARCELO GOMES{dagger}{dagger}, VICKIE BARACOS{dagger}, JAMES BAILEY{ddagger}, S. RUSS PRICE{ddagger}, WILLIAM E. MITCH§ and ALFRED L. GOLDBERG{dagger}{dagger},2

Renal Unit, Beth Israel Deaconess Medical Center, Boston, Massachusetts, USA;
* Pulmonary and Rehabilitation Research Group, Department of Medicine, University Hospital Aintree, Liverpool, L9 7AL, UK;
{dagger} Department of Agricultural, Food and Nutritional Sciences, University of Alberta, Edmonton, AB T6G 2M7, Canada;
{ddagger} Renal Division, Department of Medicine, Emory University School of Medicine, Atlanta, Georgia, USA;
§ Department of Medicine, University of Texas Medical Branch, Galveston Texas, USA; and
{dagger}{dagger} Department of Cell Biology, Harvard Medical School, Boston, Massachusetts, USA

2Correspondence: Department of Biology, Harvard Med. School, Boston, MA 02115, USA. E-mail: Alfred_goldberg{at}hms.harvard.edu

Skeletal muscle atrophy is a debilitating response to starvation and many systemic diseases including diabetes, cancer, and renal failure. We had proposed that a common set of transcriptional adaptations underlie the loss of muscle mass in these different states. To test this hypothesis, we used cDNA microarrays to compare the changes in content of specific mRNAs in muscles atrophying from different causes. We compared muscles from fasted mice, from rats with cancer cachexia, streptozotocin-induced diabetes mellitus, uremia induced by subtotal nephrectomy, and from pair-fed control rats. Although the content of >90% of mRNAs did not change, including those for the myofibrillar apparatus, we found a common set of genes (termed atrogins) that were induced or suppressed in muscles in these four catabolic states. Among the strongly induced genes were many involved in protein degradation, including polyubiquitins, Ub fusion proteins, the Ub ligases atrogin-1/MAFbx and MuRF-1, multiple but not all subunits of the 20S proteasome and its 19S regulator, and cathepsin L. Many genes required for ATP production and late steps in glycolysis were down-regulated, as were many transcripts for extracellular matrix proteins. Some genes not previously implicated in muscle atrophy were dramatically up-regulated (lipin, metallothionein, AMP deaminase, RNA helicase-related protein, TG interacting factor) and several growth-related mRNAs were down-regulated (P311, JUN, IGF-1-BP5). Thus, different types of muscle atrophy share a common transcriptional program that is activated in many systemic diseases.—Lecker, S. H., Jagoe, R. T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., Price, S. R., Mitch, W. E., Goldberg, A. L. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression.


Key Words: ubiquitin–proteasome pathway • transcription




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C. Dogra, H. Changotra, N. Wedhas, X. Qin, J. E. Wergedal, and A. Kumar
TNF-related weak inducer of apoptosis (TWEAK) is a potent skeletal muscle-wasting cytokine
FASEB J, June 1, 2007; 21(8): 1857 - 1869.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Endocrinol. Metab.Home page
C. H. Lang, R. A. Frost, and T. C. Vary
Skeletal muscle protein synthesis and degradation exhibit sexual dimorphism after chronic alcohol consumption but not acute intoxication
Am J Physiol Endocrinol Metab, June 1, 2007; 292(6): E1497 - E1506.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
B. J. Krawiec, G. J. Nystrom, R. A. Frost, L. S. Jefferson, and C. H. Lang
AMP-activated protein kinase agonists increase mRNA content of the muscle-specific ubiquitin ligases MAFbx and MuRF1 in C2C12 cells
Am J Physiol Endocrinol Metab, June 1, 2007; 292(6): E1555 - E1567.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
M. Granado, A. I Martin, M{a} A. Villanua, and A. Lopez-Calderon
Experimental arthritis inhibits the insulin-like growth factor-I axis and induces muscle wasting through cyclooxygenase-2 activation
Am J Physiol Endocrinol Metab, June 1, 2007; 292(6): E1656 - E1665.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T.-J. Zhao, Y.-B. Yan, Y. Liu, and H.-M. Zhou
The Generation of the Oxidized Form of Creatine Kinase Is a Negative Regulation on Muscle Creatine Kinase
J. Biol. Chem., April 20, 2007; 282(16): 12022 - 12029.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
E. G. Churchley, V. G. Coffey, D. J. Pedersen, A. Shield, K. A. Carey, D. Cameron-Smith, and J. A. Hawley
Influence of preexercise muscle glycogen content on transcriptional activity of metabolic and myogenic genes in well-trained humans
J Appl Physiol, April 1, 2007; 102(4): 1604 - 1611.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
M. L. Urso, Y.-W. Chen, A. G. Scrimgeour, P. C. Lee, K. F. Lee, and P. M. Clarkson
Alterations in mRNA expression and protein products following spinal cord injury in humans
J. Physiol., March 15, 2007; 579(3): 877 - 892.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
M. R. Deschenes
When size really does matter
J. Physiol., March 15, 2007; 579(3): 567 - 567.
[Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Crepaldi, F. Bersani, C. Scuoppo, P. Accornero, C. Prunotto, R. Taulli, P. E. Forni, C. Leo, R. Chiarle, J. Griffiths, et al.
Conditional Activation of MET in Differentiated Skeletal Muscle Induces Atrophy
J. Biol. Chem., March 2, 2007; 282(9): 6812 - 6822.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. Acharyya and D. C. Guttridge
Cancer Cachexia Signaling Pathways Continue to Emerge Yet Much Still Points to the Proteasome
Clin. Cancer Res., March 1, 2007; 13(5): 1356 - 1361.
[Abstract] [Full Text] [PDF]

Home page
 FASEB J.Home page
A. Koncarevic, R. W. Jackman, and S. C. Kandarian
The ubiquitin-protein ligase Nedd4 targets Notch1 in skeletal muscle and distinguishes the subset of atrophies caused by reduced muscle tension
FASEB J, February 1, 2007; 21(2): 427 - 437.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
P. Li, R. E. Waters, S. I. Redfern, M. Zhang, L. Mao, B. H. Annex, and Z. Yan
Oxidative Phenotype Protects Myofibers from Pathological Insults Induced by Chronic Heart Failure in Mice
Am. J. Pathol., February 1, 2007; 170(2): 599 - 608.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Endocrinol. Metab.Home page
T. M. Lehti, M. Silvennoinen, R. Kivela, H. Kainulainen, and J. Komulainen
Effects of streptozotocin-induced diabetes and physical training on gene expression of titin-based stretch-sensing complexes in mouse striated muscle
Am J Physiol Endocrinol Metab, February 1, 2007; 292(2): E533 - E542.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Endocrinol. Metab.Home page
R. A. Frost, G. J. Nystrom, L. S. Jefferson, and C. H. Lang
Hormone, cytokine, and nutritional regulation of sepsis-induced increases in atrogin-1 and MuRF1 in skeletal muscle
Am J Physiol Endocrinol Metab, February 1, 2007; 292(2): E501 - E512.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
Y. Bdolah, A. Segal, P. Tanksale, S. A. Karumanchi, and S. H. Lecker
Atrophy-related ubiquitin ligases atrogin-1 and MuRF-1 are associated with uterine smooth muscle involution in the postpartum period
Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2007; 292(2): R971 - R976.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
A. C. Marinovic, B. Zheng, W. E. Mitch, and S. R. Price
Tissue-specific regulation of ubiquitin (UbC) transcription by glucocorticoids: in vivo and in vitro analyses
Am J Physiol Renal Physiol, February 1, 2007; 292(2): F660 - F666.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
J. M. Sacheck, J.-P. K. Hyatt, A. Raffaello, R. T. Jagoe, R. R. Roy, V. R. Edgerton, S. H. Lecker, and A. L. Goldberg
Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases
FASEB J, January 1, 2007; 21(1): 140 - 155.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
C. H. Lang, D. Huber, and R. A. Frost
Burn-induced increase in atrogin-1 and MuRF-1 in skeletal muscle is glucocorticoid independent but downregulated by IGF-I
Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2007; 292(1): R328 - R336.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
H. Yang, W. Wei, M. Menconi, and P.-O. Hasselgren
Dexamethasone-induced protein degradation in cultured myotubes is p300/HAT dependent
Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2007; 292(1): R337 - R334.
[Abstract] [Full Text] [PDF]

Home page
 Physiol. GenomicsHome page
M. Salem, P. B. Kenney, C. E. Rexroad 3rd, and J. Yao
Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model
Physiol Genomics, December 13, 2006; 28(1): 33 - 45.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
C. A. C. Ottenheijm, L. M. A. Heunks, Y.-P. Li, B. Jin, R. Minnaard, H. W. H. van Hees, and P. N. R. Dekhuijzen
Activation of the Ubiquitin-Proteasome Pathway in the Diaphragm in Chronic Obstructive Pulmonary Disease
Am. J. Respir. Crit. Care Med., November 1, 2006; 174(9): 997 - 1002.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
M. Sandri, J. Lin, C. Handschin, W. Yang, Z. P. Arany, S. H. Lecker, A. L. Goldberg, and B. M. Spiegelman
PGC-1{alpha} protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription
PNAS, October 31, 2006; 103(44): 16260 - 16265.
[Abstract] [Full Text] [PDF]

Home page
 J EndocrinolHome page
M Granado, A I Martin, T Priego, A Lopez-Calderon, and M A Villanua
Tumour necrosis factor blockade did not prevent the increase of muscular muscle RING finger-1 and muscle atrophy F-box in arthritic rats.
J. Endocrinol., October 1, 2006; 191(1): 319 - 326.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
M. L. Urso, A. G. Scrimgeour, Y.-W. Chen, P. D. Thompson, and P. M. Clarkson
Analysis of human skeletal muscle after 48 h immobilization reveals alterations in mRNA and protein for extracellular matrix components
J Appl Physiol, October 1, 2006; 101(4): 1136 - 1148.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Cell Mol. Bio.Home page
A. Chambellan, P. J. Cruickshank, P. McKenzie, S. B. Cannady, K. Szabo, S. A. A. Comhair, and S. C. Erzurum
Gene Expression Profile of Human Airway Epithelium Induced by Hyperoxia In Vivo
Am. J. Respir. Cell Mol. Biol., October 1, 2006; 35(4): 424 - 435.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
X. Wang, Z. Hu, J. Hu, J. Du, and W. E. Mitch
Insulin Resistance Accelerates Muscle Protein Degradation: Activation of the Ubiquitin-Proteasome Pathway by Defects in Muscle Cell Signaling
Endocrinology, September 1, 2006; 147(9): 4160 - 4168.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
P. Costelli, M. Muscaritoli, M. Bossola, F. Penna, P. Reffo, A. Bonetto, S. Busquets, G. Bonelli, F. J. Lopez-Soriano, G. B. Doglietto, et al.
IGF-1 is downregulated in experimental cancer cachexia
Am J Physiol Regulatory Integrative Comp Physiol, September 1, 2006; 291(3): R674 - R683.
[Abstract] [Full Text] [PDF]

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 J Gerontol A Biol Sci Med SciHome page
E. Edstrom, M. Altun, M. Hagglund, and B. Ulfhake
Atrogin-1/MAFbx and MuRF1 Are Downregulated in Aging-Related Loss of Skeletal Muscle
J Gerontol A Biol Sci Med Sci, July 1, 2006; 61(7): 663 - 674.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
S. R. Powell
The ubiquitin-proteasome system in cardiac physiology and pathology
Am J Physiol Heart Circ Physiol, July 1, 2006; 291(1): H1 - H19.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
S. H. Lecker, A. L. Goldberg, and W. E. Mitch
Protein Degradation by the Ubiquitin-Proteasome Pathway in Normal and Disease States
J. Am. Soc. Nephrol., July 1, 2006; 17(7): 1807 - 1819.
[Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
M. U. Fareed, A. R. Evenson, W. Wei, M. Menconi, V. Poylin, V. Petkova, B. Pignol, and P.-O. Hasselgren
Treatment of rats with calpain inhibitors prevents sepsis-induced muscle proteolysis independent of atrogin-1/MAFbx and MuRF1 expression
Am J Physiol Regulatory Integrative Comp Physiol, June 1, 2006; 290(6): R1589 - R1597.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Endocrinol. Metab.Home page
T. M. Lehti, M. Silvennoinen, R. Kivela, H. Kainulainen, and J. Komulainen
Effects of streptozotocin-induced diabetes and physical training on gene expression of extracellular matrix proteins in mouse skeletal muscle
Am J Physiol Endocrinol Metab, May 1, 2006; 290(5): E900 - E907.
[Abstract] [Full Text] [PDF]

Home page
 J. Am. Soc. Nephrol.Home page
J. L. Bailey, B. Zheng, Z. Hu, S. R. Price, and W. E. Mitch
Chronic Kidney Disease Causes Defects in Signaling through the Insulin Receptor Substrate/Phosphatidylinositol 3-Kinase/Akt Pathway: Implications for Muscle Atrophy
J. Am. Soc. Nephrol., May 1, 2006; 17(5): 1388 - 1394.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Renal Physiol.Home page
G. R. Adams and N. D. Vaziri
Skeletal muscle dysfunction in chronic renal failure: effects of exercise
Am J Physiol Renal Physiol, April 1, 2006; 290(4): F753 - F761.
[Abstract] [Full Text] [PDF]

Home page
 Physiol. GenomicsHome page
A. Raffaello, P. Laveder, C. Romualdi, C. Bean, L. Toniolo, E. Germinario, A. Megighian, D. Danieli-Betto, C. Reggiani, and G. Lanfranchi
Denervation in murine fast-twitch muscle: short-term physiological changes and temporal expression profiling
Physiol Genomics, March 13, 2006; 25(1): 60 - 74.
[Abstract] [Full Text] [PDF]


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