Accumulation of advanced glycation end-products and activation of the SCAP/SREBP lipogenetic pathway occur in diet-induced obese mouse skeletal muscle

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Mastrocola, Raffaella ^a   Collino, Massimo ^a   Nigro, Debora ^a   Chiazza, Fausto ^a   D'Antona, Giuseppe ^b   Aragno, Manuela ^a   Minetto, Marco A ^c  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; REGULATOR PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN CLEAVAGE ACTIVATING PROTEIN; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; MYOSIN HEAVY CHAIN; SIGNAL PEPTIDE; SREBP CLEAVAGE-ACTIVATING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC OBESITY; DISEASE ASSOCIATION; GASTROCNEMIUS MUSCLE; LIPID STORAGE; MALE; MOUSE; MUSCLE CELL; MUSCLE MASS; MYOSTEATOSIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STEATOSIS; ADVERSE EFFECTS; ANIMAL; BLOOD; C57BL MOUSE; LIPID DIET; LIPOGENESIS; METABOLISM; OBESITY; SKELETAL MUSCLE;

ANIMALIA; MUS;

ANIMALS; DIET, HIGH-FAT; GLYCOSYLATION END PRODUCTS, ADVANCED; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOGENESIS; MEMBRANE PROTEINS; MICE, INBRED C57BL; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; OBESITY; STEROL REGULATORY ELEMENT BINDING PROTEINS;

EID: 84928884545     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119587     Document Type: Article

References (50)

1. Bifulco M, Caruso MG. From the gastronomic revolution to the new globesity epidemic. J Am Diet Assoc. 2007;107:2058-2060. PMID: 18060890
2. Yamagishi S, Matsui T. Advanced glycation end products, oxidative stress and diabetic nephropathy. Oxid Med Cell Longev. 2010;3:101-108. doi: 10.4161/oxim.3.2.11148 PMID: 20716934
3. Yuan Y, Zhao L, Chen Y, Moorhead JF, Varghese Z, Powis SH, et al. Advanced glycation end products (AGEs) increase human mesangial foam cell formation by increasing Golgi SCAP glycosylation in vitro. Am J Physiol Renal Physiol. 2011;301:F236-243. doi: 10.1152/ajprenal.00646.2010 PMID: 21511699
4. Yamagishi S. Role of advanced glycation end products (AGEs) and receptor for AGEs (RAGE) in vascular damage in diabetes. Exp Gerontol. 2011;46:217-224. doi: 10.1016/j.exger.2010.11.007 PMID: 21111800
5. Chilelli NC, Burlina S, Lapolla A. AGEs, rather than hyperglycemia, are responsible for microvascular complications in diabetes: a "glycoxidation-centric" point of view. Nutr Metab Cardiovasc Dis. 2013;23:913-919. doi: 10.1016/j.numecd.2013.04.004 PMID: 23786818
6. El-Bassossy HM, Dsokey N, Fahmy A. Characterization of vascular complications in experimental model of fructose-induced metabolic syndrome. Toxicol Mech Methods. 2014;24:536-543. doi: 10. 3109/15376516.2014.945109 PMID: 25046175
7. Lee TW, Kao YH, Lee TI, Chang CJ, Lien GS, Chen YJ. Calcitriol modulates receptor for advanced glycation end products (RAGE) in diabetic hearts. Int J Cardiol. 2014;173:236-241. doi: 10.1016/j.ijcard. 2014.02.041 PMID: 24630381
8. Yamagishi S. Role of advanced glycation end products (AGEs) in osteoporosis in diabetes. Curr Drug Targets. 2011;12:2096-2102. PMID: 22023404
9. Yang DH, Chiang TI, Chang IC, Lin FH, Wei CC, Cheng YW. Increased levels of circulating advanced glycation end-products in menopausal women with osteoporosis. Int J Med Sci. 2014;11:453-460. doi: 10.7150/ijms.8172 PMID: 24688308
10. Chen H, Wu L, Li Y, Meng J, Lin N, Yang D, et al. Advanced glycation end products increase carbohydrate responsive element binding protein expression and promote cancer cell proliferation. Mol Cell Endocrinol. 2014;395:69-78. doi: 10.1016/j.mce.2014.07.021 PMID: 25111846
11. Shimomura I, Bashmakov Y, Horton JD. Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus. J Biol Chem. 1999;274:30028-30032. PMID: 10514488
12. Cohen JC, Horton JD, Hobbs HH. Human fatty liver disease: old questions and new insights. Science. 2011;332:1519-1523. doi: 10.1126/science.1204265 PMID: 21700865
13. Moon YA, Liang G, Xie X, Frank-Kamenetsky M, Fitzgerald K, Koteliansky V. The Scap/SREBP pathway is essential for developing diabetic fatty liver and carbohydrate-induced hypertriglyceridemia in animals. Cell Metab. 2012;15:240-246. doi: 10.1016/j.cmet.2011.12.017 PMID: 22326225
14. Mastrocola R, Collino M, Rogazzo M, Medana C, Nigro D, Boccuzzi G, et al. Advanced glycation end products promote hepatosteatosis by interfering with SCAP-SREBP pathway in fructose-drinking mice. Am J Physiol Gastrointest Liver Physiol. 2013;305:G398-407. doi: 10.1152/ajpgi.00450.2012 PMID: 23868406
15. Cassese A, Esposito I, Fiory F, Barbagallo AP, Paturzo F, Mirra P, et al. In skeletal muscle advanced glycation end products (AGEs) inhibit insulin action and induce the formation of multimolecular complexes including the receptor for AGEs. J Biol Chem. 2008;283:36088-36099. doi: 10.1074/jbc. M801698200 PMID: 18955497
16. Uribarri J, Cai W, Ramdas M, Goodman S, Pyzik R, Chen X, et al. Restriction of advanced glycation end products improves insulin resistance in human type 2 diabetes: potential role of AGER1 and SIRT1. Diabetes Care. 2011;34:1610-1616. doi: 10.2337/dc11-0091 PMID: 21709297
17. Puddu A, Viviani GL. Advanced glycation endproducts and diabetes. Beyond vascular complications. Endocr Metab Immune Disord Drug Targets. 2011;11:132-140. PMID: 21476962
18. Tan KC, Shiu SW, Wong Y, Tam X. Serum advanced glycation end products (AGEs) are associated with insulin resistance. Diabetes Metab Res Rev. 2011;27:488-492. doi: 10.1002/dmrr.1188 PMID: 21337488
19. Song F, Schmidt AM. Glycation and insulin resistance: novel mechanisms and unique targets? Arterioscler Thromb Vasc Biol. 2012;32:1760-1765. doi: 10.1161/ATVBAHA.111.241877 PMID: 22815341
20. Miljkovic I, Zmuda JM. Epidemiology of myosteatosis. Curr Opin Clin Nutr Metab Care. 2010;13:260-264. doi: 10.1097/MCO.0b013e328337d826 PMID: 20179586
21. Ramamurthy B, Larsson L. Detection of an aging-related increase in advanced glycation end products in fast- and slow-twitch skeletal muscles in the rat. Biogerontology. 2013;14:293-301. doi: 10.1007/s10522-013-9430-y PMID: 23681254
22. Gumucio JP, Korn MA, Saripalli AL, Flood MD, Phan AC, Roche SM, et al. Aging-associated exacerbation in fatty degeneration and infiltration after rotator cuff tear. J Shoulder Elbow Surg. 2014;23:99-108. doi: 10.1016/j.jse.2013.04.011 PMID: 23790676
23. De Wilde J, Mohren R, Van Den Berg S, Boekschoten M, Dijk KW, De Groot P, et al. Short-term high fatfeeding results in morphological and metabolic adaptations in the skeletal muscle of C57BL/6J mice. Physiol Genomics. 2008;32:360-369. PMID: 18042831
24. Kemp JG, Blazev R, Stephenson DG, Stephenson GM. Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes (Lond). 2009;33:831-841. doi: 10.1038/ijo.2009.100 PMID: 19528970
25. Shortreed KE, Krause MP, Huang JH, Dhanani D, Moradi J, Ceddia RB, et al. Muscle-specific adaptations, impaired oxidative capacity and maintenance of contractile function characterize diet-induced obese mouse skeletal muscle. PLoS One. 2009;4:e7293. doi: 10.1371/journal.pone.0007293 PMID: 19806198
26. Benetti E, Mastrocola R, Rogazzo M, Chiazza F, Aragno M, Fantozzi R, et al. High sugar intake and development of skeletal muscle insulin resistance and inflammation in mice: a protective role for PPAR-ä agonism. Mediators Inflamm. 2013;2013:509502. doi: 10.1155/2013/509502 PMID: 23861559
27. Collino M, Mastrocola R, Nigro D, Chiazza F, Aragno M, D'Antona G, et al. Variability in myosteatosis and insulin resistance induced by high-fat diet in mouse skeletal muscles. Biomed Res Int. 2014;2014:569623. doi: 10.1155/2014/569623 PMID: 25197650
28. Spangenburg EE, Pratt SJ, Wohlers LM, Lovering RM. Use of BODIPY (493/503) to visualize intramuscular lipid droplets in skeletal muscle. J Biomed Biotechnol 2011;2011:598358. doi: 10.1155/2011/598358 PMID: 21960738
29. Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest. 2002;109:1125-1131. PMID: 11994399
30. Horton JD. Sterol regulatory element-binding proteins: transcriptional activators of lipid synthesis. Biochem Soc Trans. 2002;30:1091-1095. PMID: 12440980
31. Shimomura I, Bashmakov Y, Ikemoto S, Horton JD, Brown MS, Goldstein JL. Insulin selectively increases SREBP-1c mRNA in the livers of rats with streptozotocin-induced diabetes. Proc Natl Acad Sci U S A. 1999;96:13656-13661. PMID: 10570128
32. Matsuda M, Korn BS, Hammer RE, Moon YA, Komuro R, Horton JD, et al. SREBP cleavage-activating protein (SCAP) is required for increased lipid synthesis in liver induced by cholesterol deprivation and insulin elevation. Genes Dev. 2001;15:1206-1216. PMID: 11358865
33. Dif N, Euthine V, Gonnet E, Laville M, Vidal H, Lefai E. Insulin activates human sterol-regulatoryelementbinding protein-1c (SREBP-1c) promoter through SRE motifs. Biochem J. 2006;400:179-188. PMID: 16831124
34. Streicher R, Kotzka J, Müller-Wieland D, Siemeister G, Munck M, Avci H, et al. SREBP-1 mediates activation of the low density lipoprotein receptor promoter by insulin and insulin-like growth factor-I. J Biol Chem. 1996;271:7128-7133. PMID: 8636148
35. Endo M, Masaki T, Seike M, Yoshimatsu H. TNF-alpha induces hepatic steatosis in mice by enhancing gene expression of sterol regulatory element binding protein-1c (SREBP-1c). Exp Biol Med (Maywood). 2007;232:614-621. PMID: 17463157
36. Chen H, Wu L, Li Y, Meng J, Lin N, Yang D, et al. Advanced glycation end products increase carbohydrate responsive element binding protein expression and promote cancer cell proliferation. Mol Cell Endocrinol. 2014;395:69-78. doi: 10.1016/j.mce.2014.07.021 PMID: 25111846
37. Filhoulaud G, Guilmeau S, Dentin R, Girard J, Postic C. Novel insights into ChREBP regulation and function. Trends Endocrinol Metab. 2013;24:257-268. doi: 10.1016/j.tem.2013.01.003 PMID: 23597489
38. Tsintzas K, Norton L, Chokkalingam K, Nizamani N, Cooper S, Stephens F, et al. Independent and combined effects of acute physiological hyperglycaemia and hyperinsulinaemia on metabolic gene expression in human skeletal muscle. Clin Sci (Lond). 2013;124:675-684. doi: 10.1042/CS20120481 PMID: 23316693
39. Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T, Arnold B, et al. Understanding RAGE, the receptor for advanced glycation end products. J Mol Med (Berl). 2005;83:876-886. PMID: 16133426
40. Alexiou P, Chatzopoulou M, Pegklidou K, Demopoulos VJ. RAGE: a multi-ligand receptor unveiling novel insights in health and disease. Curr Med Chem. 2010;17:2232-2252. PMID: 20459381
41. Mahajan N, Dhawan V. Receptor for advanced glycation end products (RAGE) in vascular and inflammatory diseases. Int J Cardiol. 2013;168:1788-1794. doi: 10.1016/j.ijcard.2013.05.013 PMID: 23722052
42. Bottinelli R, Reggiani C. Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol. 2000;73:195-262. PMID: 10958931
43. Schiaffino S, Reggiani C. Fiber types inmammalian skeletalmuscles. Physiol Rev. 2011;91:1447-1531. doi: 10.1152/physrev. 00031.2010 PMID: 22013216
44. Schiaffino S, Reggiani C. Myosin isoforms in mammalian skeletal muscle. J Appl Physiol (1985). 1994;77:493-501. PMID: 8002492
45. Canepari M, Pellegrino MA, D'Antona G, Bottinelli R. Skeletal muscle fibre diversity and the underlying mechanisms. Acta Physiol (Oxf). 2010;199:465-476. doi: 10.1111/j.1748-1716.2010.02118.x PMID: 20345415
46. Rome S, Lecomte V, Meugnier E, Rieusset J, Debard C, Euthine V, et al. Microarray analyses of SREBP-1a and SREBP-1c target genes identify new regulatory pathways in muscle. Physiol Genomics. 2008;34:327-337. doi: 10.1152/physiolgenomics.90211.2008 PMID: 18559965
47. Lecomte V, Meugnier E, Euthine V, Durand C, Freyssenet D, Nemoz G, et al. A new role for sterol regulatory element binding protein 1 transcription factors in the regulation of muscle mass and muscle cell differentiation. Mol Cell Biol. 2010;30:1182-1198. doi: 10.1128/MCB.00690-09 PMID: 20028734
48. Dessalle K, Euthine V, Chanon S, Delarichaudy J, Fujii I, Rome S, et al. SREBP-1 transcription factors regulate skeletal muscle cell size by controlling protein synthesis through myogenic regulatory factors. PLoS One. 2012;7:e50878. doi: 10.1371/journal.pone.0050878 PMID: 23226416
49. Allen DL, Cleary AS, Speaker KJ, Lindsay SF, Uyenishi J, Reed JM, et al. Myostatin, activin receptor IIb, and follistatin-like-3 gene expression are altered in adipose tissue and skeletal muscle of obese mice. Am J Physiol Endocrinol Metab. 2008;294:E918-927. doi: 10.1152/ajpendo.00798.2007 PMID: 18334608
50. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature. 1997;387:83-90. PMID: 9139826