Skeletal muscle PGC-1α controls whole-body lactate homeostasis through estrogen-related receptor α- Dependent activation of LDH B and repression of LDH A

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 21, 2013, Pages 8738-8743

  Summermatter, Serge ^a   Santos, Gesa ^a   Pérez Schindler, Joaquín ^a   Handschin, Christoph ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Metabolic reprogramming; Mitochondria; Muscle plasticity; Oxidative metabolism; Transcriptional regulation

Indexed keywords

ESTROGEN RELATED RECEPTOR ALPHA; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE ISOENZYME 1; LACTATE DEHYDROGENASE ISOENZYME 5; LACTIC ACID; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EXERCISE; HOMEOSTASIS; LACTATE BLOOD LEVEL; MALE; METABOLISM; MOUSE; MYELOCYTOMATOSIS ONCOGENE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; TRANSCRIPTION REGULATION;

METABOLIC REPROGRAMMING; MITOCHONDRIA; MUSCLE PLASTICITY; OXIDATIVE METABOLISM; TRANSCRIPTIONAL REGULATION;

ANIMALS; CELL LINE; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HOMEOSTASIS; ISOENZYMES; L-LACTATE DEHYDROGENASE; LACTIC ACID; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHYSICAL CONDITIONING, ANIMAL; TRANS-ACTIVATORS;

EID: 84878162702     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1212976110     Document Type: Article

References (48)

1. Summermatter S, Handschin C (2012) PGC-1alpha and exercise in the control of body weight. Int J Obes 36(11): 1428-1435.
2. Handschin C (2010) Regulation of skeletal muscle cell plasticity by the peroxisome proliferator- activated receptor γ coactivator 1α. J Recept Signal Transduct Res 30(6): 376-384.
3. Calvo JA, et al. (2008) Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake. J Appl Physiol 104(5): 1304-1312.
4. Lin J, et al. (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418(6899): 797-801.
5. Summermatter S, et al. (2012) Remodeling of calcium handling in skeletal muscle through PGC-1α: Impact on force, fatigability, and fiber type. Am J Physiol Cell Physiol 302(1):C88-C99.
6. Arany Z, et al. (2008) HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 451(7181): 1008-1012.
7. Handschin C, et al. (2007) PGC-1alpha regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev 21(7): 770-783.
8. Lin J, Handschin C, Spiegelman BM (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 1(6): 361-370.
9. Summermatter S, Troxler H, Santos G, Handschin C (2011) Coordinated balancing of muscle oxidative metabolism through PGC-1α increases metabolic flexibility and preserves insulin sensitivity. Biochem Biophys Res Commun 408(1): 180-185.
10. Summermatter S, Baum O, Santos G, Hoppeler H, Handschin C (2010) Peroxisome proliferator-activated receptor gamma coactivator 1alpha (PGC-1alpha) promotes skeletal muscle lipid refueling in vivo by activating de novo lipogenesis and the pentose phosphate pathway. J Biol Chem 285(43): 32793-32800.
11. Wende AR, et al. (2007) A role for the transcriptional coactivator PGC-1alpha in muscle refueling. J Biol Chem 282(50): 36642-36651.
12. Cairns SP (2006) Lactic acid and exercise performance: Culprit or friend? Sports Med 36(4): 279-291.
13. Hagberg JM, et al. (1988) Metabolic responses to exercise in young and older athletes and sedentary men. J Appl Physiol 65(2): 900-908.
14. Dawson DM, Goodfriend TL, Kaplan NO (1964) Lactic dehydrogenases: Functions of the two types rates of synthesis of the two major forms can be correlated with metabolic differentiation. Science 143(3609): 929-933.
15. Draoui N, Feron O (2011) Lactate shuttles at a glance: from physiological paradigms to anti-cancer treatments. Dis Model Mech 4(6): 727-732.
16. Van Hall G (2000) Lactate as a fuel for mitochondrial respiration. Acta Physiol Scand 168(4): 643-656.
17. Juel C, Halestrap AP (1999) Lactate transport in skeletal muscle - role and regulation of the monocarboxylate transporter. J Physiol 517(pt 3): 633-642.
18. Hashimoto T, Hussien R, Brooks GA (2006) Colocalization of MCT1, CD147, and LDH in mitochondrial inner membrane of L6 muscle cells: evidence of a mitochondrial lactate oxidation complex. Am J Physiol Endocrinol Metab 290(6):E1237-E1244.
19. Kirk P, et al. (2000) CD147 is tightly associated with lactate transporters MCT1 and MCT4 and facilitates their cell surface expression. EMBO J 19(15): 3896-3904.
20. Benton CR, et al. (2008) PGC-1alpha increases skeletal muscle lactate uptake by increasing the expression of MCT1 but not MCT2 or MCT4. Physiol Genomics 35(1): 45-54.
21. Calvo S, et al. (2006) Systematic identification of human mitochondrial disease genes through integrative genomics. Nat Genet 38(5): 576-582.
22. Charest-Marcotte A, et al. (2010) The homeobox protein Prox1 is a negative modulator of ERRalpha/PGC-1alpha bioenergetic functions. Genes Dev 24(6): 537-542.
23. Pachkov M, Erb I, Molina N, van Nimwegen E (2007) SwissRegulon: A database of genome-wide annotations of regulatory sites. Nucleic Acids Res 35(database issue): D127-D131.
24. Gan Z, et al. (2011) The nuclear receptor PPARβ/δ programs muscle glucose metabolism in cooperation with AMPK and MEF2. Genes Dev 25(24): 2619-2630.
25. Fan J, et al. (2011) Tyrosine phosphorylation of lactate dehydrogenase A is important for NADH/NAD(+) redox homeostasis in cancer cells. Mol Cell Biol 31(24): 4938-4950.
26. Park EJ, Kiselev E, Conda-Sheridan M, Cushman M, Pezzuto JM (2012) Induction of apoptosis by 3-amino-6-(3-aminopropyl)-5,6-dihydro-5,11-dioxo-11H- indeno[1,2-c] isoquinoline via modulation of MAPKs (p38 and c-Jun N-terminal kinase) and c-Myc in HL-60 human leukemia cells. J Nat Prod 75(3): 378-384.
27. Park EJ, et al. (2011) Induction of retinoid X receptor activity and consequent upregulation of p21WAF1/CIP1 by indenoisoquinolines in MCF7 cells. Cancer Prev Res (Phila) 4(4): 592-607.
28. Mortensen OH, et al. (2007) PGC-1beta is downregulated by training in human skeletal muscle: No effect of training twice every second day vs. once daily on expression of the PGC-1 family. J Appl Physiol 103(5): 1536-1542.
29. Gertz EW, Wisneski JA, Stanley WC, Neese RA (1988) Myocardial substrate utilization during exercise in humans. Dual carbon-labeled carbohydrate isotope experiments. J Clin Invest 82(6): 2017-2025.
30. Ahlborg G, Juhlin-Dannfelt A (1994) Effect of beta-receptor blockade on splanchnic and muscle metabolism during prolonged exercise in men. J Appl Physiol 76(3): 1037-1042.
31. Oberbach A, et al. (2006) Altered fiber distribution and fiber-specific glycolytic and oxidative enzyme activity in skeletal muscle of patients with type 2 diabetes. Diabetes Care 29(4): 895-900.
32. Py G, et al. (2001) Impaired sarcolemmal vesicle lactate uptake and skeletal muscle MCT1 and MCT4 expression in obese Zucker rats. Am J Physiol Endocrinol Metab 281(6):E1308-E1315.
33. DeBerardinis RJ, Thompson CB (2012) Cellular metabolism and disease: what do metabolic outliers teach us? Cell 148(6): 1132-1144.
34. Apple FS, Rogers MA (1986) Skeletal muscle lactate dehydrogenase isozyme alterations in men and women marathon runners. J Appl Physiol 61(2): 477-481.
35. Simoneau JA, Pette D (1989) Species-specific responses of muscle lactate dehydrogenase isozymes to increased contractile activity. Pflugers Arch 413(6): 679-681.
36. Seyer P, et al. (2006) Mitochondrial activity regulates myoblast differentiation by control of c-Myc expression. J Cell Physiol 207(1): 75-86.
37. Veal EA, Jackson MJ (1998) C-myc is expressed in mouse skeletal muscle nuclei during post-natal maturation. Int J Biochem Cell Biol 30(7): 811-821.
38. Kemp JG, Blazev R, Stephenson DG, Stephenson GM (2009) Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes (Lond) 33(8): 831-841.
39. Apple FS, Tesch PA (1989) CK and LD isozymes in human single muscle fibers in trained athletes. J Appl Physiol 66(6): 2717-2720.
40. Bayley JP, Devilee P (2012) The Warburg effect in 2012. Curr Opin Oncol 24(1): 62-67.
41. Yeung SJ, Pan J, Lee MH (2008) Roles of p53, MYC and HIF-1 in regulating glycolysis - the seventh hallmark of cancer. Cell Mol Life Sci 65(24): 3981-3999.
42. Richter EA, Kiens B, Saltin B, Christensen NJ, Savard G (1988) Skeletal muscle glucose uptake during dynamic exercise in humans: Role of muscle mass. Am J Physiol 254(5 pt 1):E555-E561.
43. Jorfeldt L, Wahren J (1970) Human forearm muscle metabolism during exercise. V. Quantitative aspects of glucose uptake and lactate production during prolonged exercise. Scand J Clin Lab Invest 26(1): 73-81.
44. Omachi A, Lifson N (1956) Metabolism of isotopic lactate by the isolated perfused dog gastrocnemius. Am J Physiol 185(1): 35-40.
45. van Hall G (2010) Lactate kinetics in human tissues at rest and during exercise. Acta Physiol (Oxf) 199(4): 499-508.
46. Handschin C, et al. (2007) Abnormal glucose homeostasis in skeletal muscle-specific PGC-1alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk. J Clin Invest 117(11): 3463-3474.
47. Howell BF, McCune S, Schaffer R (1979) Lactate-to-pyruvate or pyruvate-to-lactate assay for lactate dehydrogenase: a re-examination. Clin Chem 25(2): 269-272.
48. Summermatter S, et al. (2009) Adipose tissue plasticity during catch-up fat driven by thrifty metabolism: relevance for muscle-adipose glucose redistribution during catchup growth. Diabetes 58(10): 2228-2237.