Exercise-induced changes in tumour LDH-B and MCT1 expression are modulated by oestrogen-related receptor alpha in breast cancer-bearing BALB/c mice

Journal of Physiology

Volumn 593, Issue 12, 2015, Pages 2635-2648

  Aveseh, Malihe ^a,b   Nikooie, Rohollah ^b   Aminaie, Mohsen ^b  

^a KERMAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b SHAHID BAHONAR UNIVERSITY OF KERMAN   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

CD147 ANTIGEN; ESTROGEN RELATED RECEPTOR ALPHA; ISOENZYME; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE A; LACTATE DEHYDROGENASE B; LACTIC ACID; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 4; UNCLASSIFIED DRUG; BSG PROTEIN, MOUSE; COTRANSPORTER; ERRALPHA ESTROGEN-RELATED RECEPTOR; ESTROGEN RECEPTOR; LACTATE DEHYDROGENASE 1; LACTATE DEHYDROGENASE 5; MONOCARBOXYLATE TRANSPORT PROTEIN 1; MONOCARBOXYLATE TRANSPORTER; MUSCLE PROTEIN; NITRILE; SLC16A4 PROTEIN, MOUSE; THIAZOLE DERIVATIVE; XCT790;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CONTROLLED STUDY; ENDURANCE; EXERCISE; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR VOLUME; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BREAST TUMOR; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD147; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; ISOENZYMES; L-LACTATE DEHYDROGENASE; LACTIC ACID; MICE, INBRED BALB C; MONOCARBOXYLIC ACID TRANSPORTERS; MUSCLE PROTEINS; NITRILES; PHYSICAL CONDITIONING, ANIMAL; RECEPTORS, ESTROGEN; SYMPORTERS; THIAZOLES; TUMOR BURDEN;

EID: 84931577546     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP270463     Document Type: Article

References (60)

1. Almeida PW, Gomes-Filho A, Ferreira AJ, Rodrigues CE, Dias-Peixoto MF, Russo RC, Teixeira MM, Cassali GD, Ferreira E, Santos IC, Garcia AM et al. (2009). Swim training suppresses tumor growth in mice. J Appl Physiol 107, 261-265.
2. Aveseh M, Nikooie R, Sheibani V, Esmaeili-Mahani S (2014). Endurance training increases brain lactate uptake during hypoglycemia by upregulation of brain lactate transporters. Mol Cell Endocrinol 394, 29-36.
3. Benton CR, Yoshida Y, Lally J, Han XX, Hatta H & Bonen A (2008). PGC-1alpha increases skeletal muscle lactate uptake by increasing the expression of MCT1 but not MCT2 or MCT4. Physiol Genomics 35, 45-54.
4. Busch BB, Stevens WC Jr, Martin R, Ordentlich P, Zhou S, Sapp DW, Horlick RA & Mohan R (2004). Identification of a selective inverse agonist for the orphan nuclear receptor estrogen-related receptor alpha. J Med Chem 47, 5593-5596.
5. Cai Q, Lin T, Kamarajugadda S & Lu J (2013). Regulation of glycolysis and the Warburg effect by estrogen-related receptors. Oncogene 32, 2079-2086.
6. Cairns RA, Harris IS & Mak TW (2011). Regulation of cancer cell metabolism. Nat Rev Cancer 11, 85-95.
7. + exchanger in metastasis. Nat Rev Cancer 5, 786-795.
8. Charest-Marcotte A, Dufour CR, Wilson BJ, Tremblay AM, Eichner LJ, Arlow DH, Mootha VK & Giguère V (2010). The homeobox protein Prox1 is a negative modulator of ERRα/PGC-1α bioenergetic functions. Genes Dev 24, 537-542.
9. Devries MC, Hamadeh MJ, Glover AW, Raha S, Samjoo IA & Tarnopolsky MA (2008). Endurance training without weight loss lowers systemic, but not muscle, oxidative stress with no effect on inflammation in lean and obese women. Free Radic Biol Med 45, 503-511.
10. Draoui N & Feron O (2011). Lactate shuttles at a glance: from physiological paradigms to anti-cancer treatments. Dis Model Mech 4, 727-732.
11. Dubouchaud H, Butterfield GE, Wolfel EE, Bergman BC & Brooks GA (2000). Endurance training, expression, and physiology of LDH, MCT1, and MCT4 in human skeletal muscle. Am J Physiol Endocrinol Metab 278, E571-E579.
12. Eichner LJ, Perry MC, Dufour CR, Bertos N, Park M, St-Pierre J & Giguère V (2010). miR-378 mediates metabolic shift in breast cancer cells via the PGC-1beta/ERRgamma transcriptional pathway. Cell Metab 12, 352-361.
13. Eickmeyer SM, Gamble GL, Shahpar S & Do KD (2012). The role and efficacy of exercise in persons with cancer. PM R 4, 874-81.
14. Elias AP & Dias S (2008). Microenvironment changes (in pH) affect VEGF alternative splicing. Cancer Microenviron 1, 131-139.
15. Feron O (2009). Pyruvate into lactate and back: from the Warburg effect to symbiotic energy fuel exchange in cancer cells. Radiother Oncol 92, 329-333.
16. Gallagher SM, Castorino JJ, Wang D & Philp NJ (2007). Monocarboxylate transporter 4 regulates maturation and trafficking of CD147 to the plasma membrane in the metastatic breast cancer cell line MDA-MB-231. Cancer Res 67, 4182-4189.
17. Gatenby RA, Gawlinski ET, Gmitro AF, Kaylor B & Gillies RJ (2006). Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res 66, 5216-5223.
18. Gatenby RA & Gillies RJ (2004). Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4, 891-899.
19. Giguere V (2008). Transcriptional control of energy homeostasis by the estrogen related receptors. Endocr Rev 29, 677-696.
20. Goh J, Tsai J, Bammler TK, Farin FM, Endicott E & Ladiges WC (2013). Exercise training in transgenic mice is associated with attenuation of early breast cancer growth in a dose-dependent manner. PLoS One 11, e80123.
21. Granchi C, Bertini S, Macchia M & Minutolo F (2010). Inhibitors of lactate dehydrogenase isoforms and their therapeutic potentials. Curr Med Chem 17, 672-697.
22. Gutmann L & Wahlefeld AW (1974). L-lactate determination with lactate dehydrogenase and NAD. Meth Enzym Anal 1464-1472.
23. Halestrap AP (2012). The monocarboxylate transporter family - structure and functional characterization. IUBMB Life 64, 1-9.
24. Hittel DS, Kraus WE, Tanner CJ, Houmard JA & Hoffman EP (2005). Exercise training increases electron and substrate shuttling proteins in muscle of overweight men and women with the metabolic syndrome. J Appl Physiol 98, 168-179.
25. Huss JM, Torra IP, Staels B, Giguère V & Kelly DP (2004). Estrogen-related receptor alpha directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol Cell Biol 24, 9079-9091.
26. Hussien R & Brooks GA (2010). Mitochondrial and plasma membrane lactate transporter and lactate dehydrogenase isoform expression in breast cancer cell lines. Physiol Genomics 43, 255-264.
27. Jones LW, Viglianti BL, Tashjian JA, Kothadia SM, Keir ST, Freedland SJ, Potter MQ, Moon EJ, Schroeder T, Herndon JE & Dewhirst MW (2010). Effect of aerobic exercise on tumor physiology in an animal model of human breast cancer. J Appl Physiol 108, 343-348.
28. Kennedy KM & Dewhirst MW (2010). Tumor metabolism of lactate: the influence and therapeutic potential for MCT and CD147 regulation. Future Oncol 6, 127-48.
29. Kim JH1, Kim EL, Lee YK, Park CB, Kim BW, Wang HJ, Yoon CH, Lee SJ & Yoon G (2011). Decreased lactate dehydrogenase B expression enhances claudin 1-mediated hepatoma cell invasiveness via mitochondrial defects. Exp Cell Res 317, 1108-1118.
30. Kossman DA, Williams NI, Domchek SM, Kurzer MS, Stopfer JE & Schmitz KH (2011). Exercise lowers estrogen and progesterone levels in premenopausal women at high risk of breast cancer. J Appl Physiol 111, 1687-1693.
31. Lanari C, Lüthy I, Lamb CA, Fabris V, Pagano E, Helguero LA, Sanjuan N, Merani S & Molinolo AA (2001). Five novel hormone-responsive cell lines derived from murine mammary ductal carcinomas: in vivo and in vitro effects of estrogens and progestins. Cancer Res 61, 293-302.
32. Le A, Cooper CR, Gouw AM, Dinavahi R, Maitra A, Deck LM, Royer RE, Vander Jagt DL, Semenza GL & Dang CV (2010). Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression. Proc Natl Acad Sci USA 107, 2037-2042.
33. + symporters MCT1 and hypoxia-inducible MCT4 is critical for energetics and growth of glycolytic tumors. Proc Natl Acad Sci USA 108, 16663-16668.
34. Leiblich A, Cross SS, Catto JW, Phillips JT, Leung HY, Hamdy FC & Rehman I (2006). Lactate dehydrogenase-B is silenced by promoter hypermethylation in human prostate cancer. Oncogene 25, 2953-2960.
35. Leiblich A, Cross SS, Catto JWF, Phillips JT, Leung HY, Hamdy FC & Rehman I (2013). Lactate dehydrogenase-B is silenced by promoter methylation in a high frequency of human breast cancers. PLoS One 2, e57697.
36. Lira VA, Benton CR, Yan Z & Bonen A (2010). PGC-1α regulation by exercise training and its influences on muscle function and insulin sensitivity. Am J Physiol Endocrinol Metab 299, E145-E161.
37. Markert CL, Shaklee JB & Whitt GS (1975). Evolution of a gene. Multiple genes for LDH isozymes provide a model of the evolution of gene structure, function and regulation. Science 189, 102-114.
38. Mirebeau-Prunier D, Le Pennec S, Jacques C, Fontaine JF, Gueguen N, Boutet-Bouzamondo N, Donnart A, Malthièry Y & Savagner F (2013). Estrogen-related receptor alpha modulates lactate dehydrogenase activity in thyroid tumors. PLoS One 8, e58683.
39. Moreno-Sanchez R, Rodriguez-Enriquez S, Marin-Hernandez A & Saavedra E (2007). Energy metabolism in tumor cells. FEBS J 274, 1393-1418.
40. Muñoz-Pinedo C, Mjiyad N El & Ricci J-E (2012). Cancer metabolism: current perspectives and future directions. Cell Death Dis 3, e248.
41. Murphy EA, Davis JM, Barrilleaux TL, McClellan JL, Steiner JL, Carmichael MD, Pena MM, Hebert Jr. & Green JE (2011). Benefits of exercise training on breast cancer progression and inflammation in C3(1)SV40Tag mice. Cytokine 55, 274-279.
42. Nikooie R, Rajabi H, Gharakhanlu R, Atabi F, Omidfar K, Aveseh M & Larijani B (2013). Exercise-induced changes of MCT1 in cardiac and skeletal muscles of diabetic rats induced by high-fat diet and STZ. J Physiol Biochem 69, 865-877.
43. Ntanasis-Stathopoulos J, Tzanninis JG, Philippou A & Koutsilieris M (2013). Epigenetic regulation on gene expression induced by physical exercise. J Musculoskelet Neuronal Interact 2, 133-146.
44. Pierce BL, Neuhouser ML, Wener MH, Bernstein L, Baumgartner RN, Ballard-Barbash R, Gilliland FD, Baumgartner KB, Sorensen B, McTiernan A & Ulrich CM (2009). Correlates of circulating C-reactive protein and serum amyloid A concentrations in breast cancer survivors. Breast Cancer Res Treat 114, 155-67.
45. Pinheiro C, Albergaria A, Paredes J, Sousa B, Dufloth R, Vieira D, Schmitt F & Baltazar F (2010). Monocarboxylate transporter 1 is up-regulated in basal-like breast carcinoma. Histopathology 56, 860-867.
46. Pinheiro C, Reis RM, Ricardo S, Longatto-Filho A, Schmitt F & Baltazar F (2010). Expression of monocarboxylate transporters 1, 2, and 4 in human tumors and their association with CD147 and CD44. J Biomed Biotechnol 2010, 427694; doi:10.1155/2010/427694.
47. Pinheiro C, Sousa B, Albergaria A, Paredes J, Dufloth R, Vieira D, Schmitt F & Baltazar F (2011). GLUT1 and CAIX expression profiles in breast cancer correlate with adverse prognostic factors and MCT1 overexpression. Histol Histopathol 26, 1279-1286.
48. Schmitz KH, Warren M, Rundle AG, Williams NI, Gross MD & Kurzer MS (2008). Exercise effect on oxidative stress is independent of change in estrogen metabolism. Cancer Epidemiol Biomarkers Prev 17, 220-223.
49. Schneiderhan W, Scheler M, Holzmann KH, Marx M, Gschwend JE, Bucholz M, Gress TM, Seufferlein T, Adler G & Oswald F (2009). CD147 silencing inhibits lactate transport and reduces malignant potential of pancreatic cancer cells in in vivo and in vitro models. Gut 58, 1391-1398.
50. Schwoch C & Pasoow H (1984). Preparation and properties of human erythrocyte ghosts. Mol Cell Biochem 2, 197-218.
51. Semenza GL (2008). Tumor metabolism: cancer cells give and take lactate. J Clin Invest 12, 3835-3847.
52. Sonveaux P, Végran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN, De Saedeleer CJ, Kennedy KM, Diepart C, Jordan BF et al. (2008). Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 118, 3930-3942.
53. Steiner JL, Davis M, McClellan JL, Enos RT & Murphy EA (2013). Effects of voluntary exercise on tumorigenesis in the C3(1)/SV40Tag transgenic mouse model of breast cancer. Int J Oncol 42, 1466-1472.
54. Summermatter S, Santos G, Pérez-Schindler J & Handschin C (2013). Skeletal muscle PGC-1α controls whole-body lactate homeostasis through estrogen-related receptor α-dependent activation of LDH B and repression of LDH A. Proc Natl Acad Sci USA 110, 8738-8743.
55. Ulrich CM, Wiskemann J & Steindorf K (2012). Physiologic and molecular mechanisms linking physical activity to cancer risk and progression. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 55, 3-9.
56. Végran F, Boidot R, Michiels C, Sonveaux P & Feron O.(2011). Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-κB/IL-8 pathway that drives tumor angiogenesis. Cancer Res 71, 2550-2560.
57. Wang ZY, Loo TY, Shen JG, Wang N, Wang DM, Yang DP, Mo SL, Guan XY & Chen JP (2012). LDH-A silencing suppresses breast cancer tumorigenicity through induction of oxidative stress-mediated mitochondrial pathway apoptosis. Breast Cancer Res Treat 131, 791-800.
58. Warburg O (1956). On the origin of cancer cells. Science 123, 309-314.
59. Yuasa Y, Nagasaki H, Akiyama Y, Hashimoto Y, Takizawa T, Kojima K, Kawano T, Sugihara K, Imai K & Nakachi K (2009). DNA methylation status is inversely correlated with green tea intake and physical activity in gastric cancer patients. Int J Cancer 11, 2677-2682.
60. Zeng H, Irwin ML, Lu L, Risch H, Mayne S, Mu L, Deng Q, Scarampi L, Mitidieri M, Katsaros D & Yu H (2012). Physical activity and breast cancer survival: an epigenetic link through reduced methylation of a tumor suppressor gene L3MBTL1. Breast Cancer Res Treat 133, 127-135.