Pharmacological blockade of cannabinoid CB1 receptors in diet-induced obesity regulates mitochondrial dihydrolipoamide dehydrogenase in muscle

PLoS ONE

Volumn 10, Issue 12, 2015, Pages

  Arrabal, Sergio ^a,b   Lucena, Miguel Angel ^a   Canduela, Miren Josune ^c   Ramos Uriarte, Almudena ^c   Rivera, Patricia ^a,b   Serrano, Antonia ^a,b   Pavón, Francisco Javier ^a,b   Decara, Juan ^a,b   Vargas, Antonio ^a,b   Baixeras, Elena ^a,b   Martín Rufián, Mercedes ^a   Márquez, Javier ^a   Fernández Llébrez, Pedro ^a   De Roos, Baukje ^d   Grandes, Pedro ^c   De Fonseca, Fernando Rodríguez ^a,b   Suárez, Juan ^a,b  

^a Instituto de Investigación Biomédica de Málaga y Plataforma en Nanomedicina IBIMA Plataforma Bionand   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^d ROWETT RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABINOID 1 RECEPTOR; DIHYDROLIPOAMIDE DEHYDROGENASE; ENOLASE; GLUCOSE 6 PHOSPHATE ISOMERASE; GLUTATHIONE REDUCTASE; LACTATE DEHYDROGENASE; LACTOYLGLUTATHIONE LYASE; METHYLGLYOXAL; PYRUVATE DEHYDROGENASE; TRIOSEPHOSPHATE ISOMERASE; CARBOHYDRATE DIET; GLUCOSE; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE; PYRUVIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE DIET; CELLULAR DISTRIBUTION; CITRIC ACID CYCLE; CONTROLLED STUDY; DIET INDUCED OBESITY; DOWN REGULATION; GENE EXPRESSION; GLYCOLYSIS; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; MUSCLE MITOCHONDRION; NONHUMAN; PROTEIN EXPRESSION; PROTEOMICS; RAT; RECTUS ABDOMINIS MUSCLE; TWO DIMENSIONAL ELECTROPHORESIS; UPREGULATION; WEIGHT REDUCTION; ANIMAL; BODY WEIGHT; C57BL MOUSE; CELL LINE; DIET; DRUG EFFECTS; ELECTROSPRAY MASS SPECTROMETRY; ENZYMOLOGY; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; MITOCHONDRION; MUSCLE; OBESITY; OXIDATION REDUCTION REACTION; SKELETAL MUSCLE CELL; TWO DIMENSIONAL GEL ELECTROPHORESIS; WISTAR RAT;

ANIMALS; BODY WEIGHT; CELL LINE; DIET; DIETARY CARBOHYDRATES; DIHYDROLIPOAMIDE DEHYDROGENASE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GLUCOSE; GLUTATHIONE REDUCTASE; MALE; MICE, INBRED C57BL; MITOCHONDRIA; MUSCLE FIBERS, SKELETAL; MUSCLES; OBESITY; OXIDATION-REDUCTION; PIPERIDINES; PYRAZOLES; PYRUVIC ACID; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84970923498     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0145244     Document Type: Article

References (44)

1. Di Marzo V. The endocannabinoid system in obesity and type 2 diabetes. Diabetologia 2008; 51: 1356-1367. doi: 10.1007/s00125-008-1048-2 PMID: 18563385.
2. Engeli S. Dysregulation of the endocannabinoid system in obesity. J Neuroendocrinol. 2008; 20: 110-115.
3. Matias I, Petrosino S, Racioppi A, Capasso R, Izzo AA, Di Marzo V. Dysregulation of peripheral endocannabinoid levels in hyperglycemia and obesity: Effect of high fat diets. Mol Cell Endocrinol. 2008; 286: S66-S78. doi: 10.1016/j.mce.2008.01.026 PMID: 18343566.
4. Pagotto U, Marsicano G, Cota D, Lutz B, Pasquali R. The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocr Rev. 2006; 27: 73-100. PMID: 16306385.
5. Crespillo A, Suárez J, Bermúdez-Silva FJ, Rivera P, Vida M, Alonso M, et al. Expression of the cannabinoid system in muscle: effects of a high-fat diet and CB1 receptor blockade. Biochem J. 2011; 433: 175-185. doi: 10.1042/BJ20100751 PMID: 20955176.
6. Rivera P, Luque-Rojas MJ, Pastor A, Blanco E, Pavón FJ, Serrano A, et al. Diet-dependent modulation of hippocampal expression of endocannabinoid signaling-related proteins in cannabinoid antagonisttreated obese rats. Eur J Neurosci. 2013; 37: 105-17. doi: 10.1111/ejn.12012 PMID: 23033907.
7. Cavuoto P, McAinch AJ, Hatzinikolas G, Cameron-Smith D, Wittert GA. Effects of cannabinoid receptors on skeletal muscle oxidative pathways. Mol Cell Endocrinol. 2007; 267: 63-69. PMID: 17270342.
8. Liu YL, Connoley IP, Wilson CA, Stock MJ. Effects of the cannabinoid CB1 receptor antagonist SR141716 on oxygen consumption and soleus muscle glucose uptake in Lep(ob)/Lep(ob) mice. Int J Obes. 2005; 29: 183-187.
9. Pagano C, Rossato M, Vettor R. Endocannabinoids, adipose tissue and lipid metabolism. J Neuroendocrinol. 2008; 20: 124-129. doi: 10.1111/j.1365-2826.2008.01690.x PMID: 18426511.
10. Vida M, Rivera P, Gavito AL, Suárez J, Pavón FJ, Arrabal S, et al. CB1 blockade potentiates down-regulation of lipogenic gene expression in perirenal adipose tissue in high carbohydrate diet-induced obesity. PLoS One 2014; 9: e90016. doi: 10.1371/journal.pone.0090016 PMID: 24587189.
11. Di Marzo V, Piscitelli F, Mechoulam R. Cannabinoids and endocannabinoids in metabolic disorders with focus on diabetes. Handb Exp Pharmacol. 2011; 203: 75-104. doi: 10.1007/978-3-642-17214-4-4 PMID: 21484568.
12. Højlund K, Mogensen M, Sahlin K, Beck-Nielsen H. Mitochondrial dysfunction in type 2 diabetes and obesity. Endocrinol Metab Clin North Am. 2008; 37: 713-731. doi: 10.1016/j.ecl.2008.06.006 PMID: 18775360.
13. Sivitz WI, Yorek MA. Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Anti oxid Redox Signal 2010; 12, 537-577. doi: 10.1089/ars. 2009.2531 PMID: 19650713.
14. Tuomilehto J, Lindström J, Eriksson JG, Valle TT, Hämäläinen H, Ilanne-Parikka P, et al. Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med. 2001; 344: 1343-1350. PMID: 11333990.
15. Wilson PW, D'Agostino RB, Sullivan L, Parise H, Kannel WB. Overweight and obesity as determinants of cardiovascular risk: The Framingham experience. Arch. Intern. Med. 2002; 162: 1867-72. PMID: 12196085.
16. Alonso M, Serrano A, Vida M, Crespillo A, Hernandez-Folgado L, Jagerovic N, et al. Anti-obesity efficacy of LH-21, a cannabinoid CB(1) receptor antagonist with poor brain penetration, in diet-induced obese rats. Br J Pharmacol. 2012; 165: 2274-2291 doi: 10.1111/j.1476-5381.2011.01698.x PMID: 21951309.
17. Riedel G, Fadda P, McKillop-Smith S, Pertwee RG, Platt B, Robinson L. Synthetic and plant-derived cannabinoid receptor antagonists show hypophagic properties in fasted and non-fasted mice. Br J Pharmacol. 2009; 156: 1154-1166. PMID: 19378378.
18. Tam J, Vemuri VK, Liu J, Bátkai S, Mukhopadhyay B, Godlewski G, et al. Peripheral CB1 cannabinoid receptor blockade improves cardiometabolic risk in mouse models of obesity. J. Clin. Invest. 2010; 120, 2953-66. doi: 10.1172/JCI42551 PMID: 20664173.
19. Van Gaal LF, Rissanen AM, Scheen AJ, Ziegler O, Rössner S, RIO-Europe Study Group. Effects of the cannabinoid-1 receptor blocker rimonabant on weight reduction and cardiovascular risk factors inoverweight patients: 1-year experience from the RIO-Europe study. Lancet 2005; 365: 1389-1397. PMID: 15836887.
20. Pi-Sunyer FX, Aronne LJ, Heshmati HM, Devin J, Rosenstock J, RIO-North America Study Group. Effect of rimonabant, a cannabinoid-1 receptor blocker, on weight and cardiometabolic risk factors in overweight or obese patients: RIO-North America: A randomized controlled trial. JAMA 2006; 295: 761-775. PMID: 16478899.
21. Christensen R, Kristensen PK, Bartels EM, Bliddal H, Astrup A. Efficacy and safety of the weight-loss drug rimonabant: A meta-analysis of randomised trials. Lancet 2007; 370: 1706-13. PMID: 18022033.
22. Christopoulou FD, Kiortsis DN. An overview of the metabolic effects of rimonabant in randomized controlled trials: potential for other cannabinoid 1 receptor blockers in obesity. J Clin Pharm Ther. 2011; 36: 10-18. doi: 10.1111/j.1365-2710.2010.01164.x PMID: 21198716.
23. Pavón FJ, Serrano A, Pérez-Valero V, Jagerovic N, Hernández-Folgado L, Bermúdez-Silva FJ, et al. Central versus peripheral antagonism of cannabinoid CB1 receptor in obesity: effects of LH-21, a peripherally acting neutral cannabinoid receptor antagonist, in Zucker rats. J Neuroendocrinol. 2008; 20: 116-23. doi: 10.1111/j.1365-2826.2008.01693.x PMID: 18426510.
24. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, et al. The endogenous cannabinoid system controls extinction of aversive memories. Nature 2002; 418: 530-534. PMID: 12152079.
25. de Roos B, Duivenvoorden I, Rucklidge G, Reid M, Ross K, Lamers RJ, et al. Response of apolipoprotein E∗3-Leiden transgenic mice to dietary fatty acids: combining liver proteomics with physiological data. FASEB J. 2005; 19: 813-5. PMID: 15755870.
26. Bae N, Yang JW, Sitte H, Pollak A, Marquez J, Lubec G. An electrophoretic approach to screen for glutamine deamidation. Anal. Biochem. 2012; 428: 1-3. doi: 10.1016/j.ab.2012.05.016 PMID: 22640603.
27. Benard G, Faustin B, Passerieux E, Galinier A, Rocher C, Bellance N, et al. Physiological diversity of mitochondrial oxidative phosphorylation. Am J Physiol Cell Physiol. 2006; 291: C1172-82. PMID: 16807301.
28. Iannotti FA, Silvestri C, Mazzarella E, Martella A, Calvigioni D, Piscitelli F, et al. The endocannabinoid 2-AG controls skeletal muscle cell differentiation via CB1 receptor-dependent inhibition of Kv7 channels. Proc Natl Acad Sci USA. 2014; 111: E2472-81. doi: 10.1073/pnas.1406728111 PMID: 24927567.
29. Benard G, Bellance N, James D, Parrone P, Fernandez H, Letellier T, et al. Mitochondrial bioenergetics and structural network organization. J Cell Sci. 2007; 120: 838-48. PMID: 17298981.
30. Hebert-Chatelain E, Reguero L, Puente N, Lutz B, Chaouloff F, Rossignol R, et al. Studying mitochondrial CB1 receptors: Yes we can. Mol Metab. 2014; 3: 339. doi: 10.1016/j.molmet.2014.03.008 PMID: 24944889.
31. Bénard G, Massa F, Puente N, Lourenço J, Bellocchio L, Soria-Gómez E, et al. Mitochondrial CB1 receptors regulate neuronal energy metabolism. Nat Neurosci. 2012; 15: 558-564. doi: 10.1038/nn. 3053 PMID: 22388959.
32. Bermudez-Silva FJ, Sanchez-Vera I, Suárez J, Serrano A, Fuentes E, Juan-Pico P, et al. Role of cannabinoid CB2 receptors in glucose homeostasis in rats. Eur J Pharmacol. 2007; 565: 207-211. PMID: 17499236.
33. Patti ME, Corvera S. The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr Rev. 2010; 31: 364-95. doi: 10.1210/er.2009-0027 PMID: 20156986.
34. Yu J, Yu B, He J, Zheng P, Mao X, Han G, et al. Chronic glucocorticoid exposure-induced epididymal adiposity is associated with mitochondrial dysfunction in white adipose tissue of male C57BL/6J mice. PLoS One 2014; 9: e112628. doi: 10.1371/journal.pone.0112628 PMID: 25389775.
35. Tedesco L, Valerio A, Cervino C, Cardile A, Pagano C, Vettor R, et al. Cannabinoid type 1 receptor blockade promotes mitochondrial biogenesis through endothelial nitric oxide synthase expression in white adipocytes. Diabetes 2008; 57: 2028-2036. doi: 10.2337/db07-1623 PMID: 18477809.
36. p38 MAPK and AMPK pathways. Diabetes 2010; 59: 2826-2836. doi: 10.2337/db09-1881 PMID: 20739683.
37. pH-dependent substrate preference of pig heart lipoamide dehydrogenase varies with oligomeric state: response to mitochondrial matrix acidification. J Biol Chem. 2005; 280: 16106-16114. PMID: 15710613.
38. Constantin-Teodosiu D. Regulation of muscle pyruvate dehydrogenase complex in insulin resistance: effects of exercise and dichloroacetate. Diabetes Metab J. 2013; 37: 301-14. doi: 10.4093/dmj.2013. 37.5.301 PMID: 24199158.
39. Tiyerili V, Zimmer S, Jung S, Wassmann K, Naehle CP, Lütjohann D, et al. CB1 receptor inhibition leads to decreased vascular AT1 receptor expression, inhibition of oxidative stress and improvedendothelial function. Basic Res Cardiol. 2010; 105: 465-77. doi: 10.1007/s00395-010-0090-7 PMID: 20361197.
40. Mailloux RJ. Teaching the fundamentals of electron transfer reactions in mitochondria and the production and detection of reactive oxygen species. Redox Biol. 2015; 4: 381-98. doi: 10.1016/j.redox.2015. 02.001 PMID: 25744690.
41. Athanasiou A, Clarke AB, Turner AE, Kumaran NM, Vakilpour S, Smith PA, et al. Cannabinoid receptor agonists are mitochondrial inhibitors: A unified hypothesis of how cannabinoids modulate mitochondrial function and induce cell death. Biochem Biophys Res Commun. 2007; 364: 131-137 PMID: 17931597.
42. Hebert-Chatelain E, Reguero L, Puente N, Lutz B, Chaouloff F, Rossignol R, et al. Cannabinoid control of brain bioenergetics: Exploring the subcellular localization of the CB1 receptor. Mol Metab. 2014; 3: 495-504. doi: 10.1016/j.molmet.2014.03.007 PMID: 24944910.
43. Bartova A, Birmingham MK. Effect of delta9-tetrahydrocannabinol on mitochondrial NADH-oxidase activity. J Biol Chem. 1976; 251: 5002-5006. PMID: 956173.
44. Lipina C, Irving AJ, Hundal HS. Mitochondria: A possible nexus for the regulation of energy homeostasis by the endocannabinoid system? Am J Physiol Endocrinol Metab. 2014; 307: E1-13. doi: 10.1152/ajpendo.00100.2014 PMID: 24801388.