Exercise-induced heart mitochondrial cholesterol depletion influences the inhibition of mitochondrial swelling

Experimental Physiology

Volumn 98, Issue 10, 2013, Pages 1457-1468

  Ziolkowski, Wieslaw ^a,b   Vadhana Ms, Dhivya ^c   Kaczor, Jan Jacek ^a,b   Olek, Robert Antoni ^a,b   Flis, Damian Jozef ^a   Halon, Malgorzata ^b   Wozniak, Michal ^b   Fedeli, Donatella ^c   Carloni, Manuel ^c   Antosiewicz, Jedrzej ^d   Gabbianelli, Rosita ^c  

^a GDANSK UNIVERSITY OF PHYSICAL EDUCATION AND SPORT   (Poland)

^b MEDICAL UNIVERSITY OF GDANSK   (Poland)

^c UNIVERSITY OF CAMERINO   (Italy)

^d SWPS UNIVERSITY OF SOCIAL SCIENCES AND HUMANITIES   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ALKADIENE; CALCIUM CHLORIDE; CARBONYL DERIVATIVE; CHOLESTEROL; CYTOCHROME C OXIDASE; LACTIC ACID; METHYL BETA CYCLODEXTRIN; MITOCHONDRIAL ENZYME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOENERGY; BLOOD SAMPLING; BODY WEIGHT; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; EXERCISE TEST; HEART MITOCHONDRION; HEART MUSCLE CELL; LACTATE BLOOD LEVEL; MALE; MEMBRANE FLUIDITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION SWELLING; MITOPHAGY; NONHUMAN; OXIDATIVE STRESS; RAT; SWIMMING;

ANIMALS; CALCIUM CHLORIDE; CHOLESTEROL; LACTIC ACID; MALE; MEMBRANE FLUIDITY; MITOCHONDRIA, HEART; MITOCHONDRIAL SWELLING; OXIDATIVE STRESS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR; SWIMMING;

EID: 84884706456     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2013.073007     Document Type: Article

References (51)

1. Ardail D, Privat JP, Egret-Charlier M, Levrat C, Lerme F & Louisot P (1990). Mitochondrial contact sites. Lipid composition and dynamics. J Biol Chem 265, 18797-18802.
2. Area-Gomez E, Del Carmen Lara Castillo M, Tambini MD, Guardia-Laguarta C, de Groof AJ, Madra M, Ikenouchi J, Umeda M, Bird TD, Sturley SL & Schon EA (2012). Upregulated function of mitochondria-associated ER membranes in Alzheimer disease. EMBO J 31, 4106-4123.
3. Ascensao A, Lumini-Oliveira J, Machado NG, Ferreira RM, Goncalves IO, Moreira AC, Marques F, Sardao VA, Oliveira PJ & Magalhaes J (2011). Acute exercise protects against calcium-induced cardiac mitochondrial permeability transition pore opening in doxorubicin-treated rats. Clin Sci (Lond) 120, 37-49.
4. Avital A, Richter-Levin G, Leschiner S, Spanier I, Veenman L, Weizman A & Gavish M (2001). Acute and repeated swim stress effects on peripheral benzodiazepine receptors in the rat hippocampus, adrenal, and kidney. Neuropsycho-pharmacology 25, 669-678.
5. Bernardi P & Rasola A (2007). Calcium and cell death: the mitochondrial connection. Subcell Biochem 45, 481-506.
6. Bernardi P, Scorrano L, Colonna R, Petronilli V & Di Lisa F (1999). Mitochondria and cell death. Mechanistic aspects and methodological issues. Eur J Biochem 264, 687-701.
7. Ciminelli M, Ascah A, Bourduas K & Burelle Y (2006). Short term training attenuates opening of the mitochondrial permeability transition pore without affecting myocardial function following ischemia-reperfusion. Mol Cell Biochem 291, 39-47.
8. Csukly K, Ascah A, Matas J, Gardiner PF, Fontaine E & Burelle Y (2006). Muscle denervation promotes opening of the permeability transition pore and increases the expression of cyclophilin D. J Physiol 574, 319-327.
9. Davies KJ, Quintanilha AT, Brooks GA & Packer L (1982). Free radicals and tissue damage produced by exercise. Biochem Biophys Res Commun 107, 1198-1205.
10. Estabrook RW (1967). Mitochondrial respiratory control and the polarographic measurements of ADP:O ratio. In Methods in Enzymology, volume 10, ed. Estabrook RW & Pullman ME, pp. 41-47. Academic Press, New York
11. Fernstrom M, Tonkonogi M & Sahlin K (2004). Effects of acute and chronic endurance exercise on mitochondrial uncoupling in human skeletal muscle. J Physiol 554, 755-763.
12. Fujimoto M, Hayashi T & Su TP (2012). The role of cholesterol in the association of endoplasmic reticulum membranes with mitochondria. Biochem Biophys Res Commun 417, 635-639.
13. Garofalo T, Giammarioli AM, Misasi R, Tinari A, Manganelli V, Gambardella L, Pavan A, Malorni W & Sorice M (2005). Lipid microdomains contribute to apoptosis-associated modifications of mitochondria in T cells. Cell Death Differ 12, 1378-1389.
14. Garofalo T, Tinari A, Matarrese P, Giammarioli AM, Manganelli V, Ciarlo L, Misasi R, Sorice M & Malorni W (2007). Do mitochondria act as "cargo boats" in the journey of GD3 to the nucleus during apoptosis FEBS Lett 581, 3899-3903.
15. Harder T, Rentero C, Zech T & Gaus K (2007). Plasma membrane segregation during T cell activation: probing the order of domains. Curr Opin Immunol 19, 470-475.
16. Keatisuwan W, Kinjo M & Koyama T (1991). Changes in phospholipid constituents in mitochondrial membranes after long lasting exercise in rat heart. Life Sci 48, 2173-2181.
17. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S & Stadtman ER (1990). Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186, 464-478.
18. Liu J, Yeo HC, Overvik-Douki E, Hagen T, Doniger SJ, Chyu DW, Brooks GA & Ames BN (2000). Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 89, 21-28.
19. Lowry OH, Rosebrough NJ, Farr AL & Randall RJ (1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265-275.
20. Lumini-Oliveira J, Magalhaes J, Pereira CV, Moreira AC, Oliveira PJ & Ascensao A (2011). Endurance training reverts heart mitochondrial dysfunction, permeability transition and apoptotic signaling in long-term severe hyperglycemia. Mitochondrion 11, 54-63.
21. McCommis KS, McGee AM, Laughlin MH, Bowles DK & Baines CP (2011). Hypercholesterolemia increases mitochondrial oxidative stress and enhances the MPT response in the porcine myocardium: beneficial effects of chronic exercise. Am J Physiol Regul Integr Comp Physiol 301, R1250-R1258.
22. 2+-induced permeability transition pore opening in heart mitochondria. Am J Physiol Heart Circ Physiol 290, H1549-H1557.
23. Marguet D, Lenne PF, Rigneault H & He HT (2006). Dynamics in the plasma membrane: how to combine fluidity and order. EMBO J 25, 3446-3457.
24. Martinez-Abundis E, Correa F, Pavon N & Zazueta C (2009). Bax distribution into mitochondrial detergent-resistant microdomains is related to ceramide and cholesterol content in postischemic hearts. FEBS J 276, 5579-5588.
25. Martinez-Abundis E, Garcia N, Correa F, Franco M & Zazueta C (2007). Changes in specific lipids regulate BAX-induced mitochondrial permeability transition. FEBS J 274, 6500-6510.
26. Matas J, Young NT, Bourcier-Lucas C, Ascah A, Marcil M, Deschepper CF & Burelle Y (2009). Increased expression and intramitochondrial translocation of cyclophilin-D associates with increased vulnerability of the permeability transition pore to stress-induced opening during compensated ventricular hypertrophy. J Mol Cell Cardiol 46, 420-430.
27. 31P NMR study. Gen Physiol Biophys 11, 317-325.
28. Ohtani Y, Irie T, Uekama K, Fukunaga K & Pitha J (1989). Differential effects of α-, β- and γ-cyclodextrins on human erythrocytes. Eur J Biochem 186, 17-22.
29. Paradis S, Leoni V, Caccia C, Berdeaux A & Morin D (2013). Cardioprotection by the TSPO ligand 4′-chlorodiazepam is associated with inhibition of mitochondrial accumulation of cholesterol at reperfusion. Cardiovasc Res DOI: 10.1093/cvr/cvt079.
30. Parasassi T, De Stasio G, d'Ubaldo A & Gratton E (1990). Phase fluctuation in phospholipid membranes revealed by Laurdan fluorescence. Biophys J 57, 1179-1186.
31. Parasassi T, De Stasio G, Ravagnan G, Rusch RM & Gratton E (1991). Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of Laurdan fluorescence. Biophys J 60, 179-189.
32. Perez AC, Cabral de Oliveira AC, Estevez E, Molina AJ, Prieto JG & Alvarez AI (2003). Mitochondrial, sarcoplasmic membrane integrity and protein degradation in heart and skeletal muscle in exercised rats. Comp Biochem Physiol C Toxicol Pharmacol 134, 199-206.
33. Powers SK, Nelson WB & Hudson MB (2011a). Exercise-induced oxidative stress in humans: cause and consequences. Free Radic Biol Med 51, 942-950.
34. Powers SK, Talbert EE & Adhihetty PJ (2011b). Reactive oxygen and nitrogen species as intracellular signals in skeletal muscle. J Physiol 589, 2129-2138.
35. Raimondo F, Morosi L, Chinello C, Perego R, Bianchi C, Albo G, Ferrero S, Rocco F, Magni F & Pitto M (2012). Protein profiling of microdomains purified from renal cell carcinoma and normal kidney tissue samples. Mol Biosyst 8, 1007-1016.
36. Rizzuto R, Pinton P, Brini M, Chiesa A, Filippin L & Pozzan T (1999). Mitochondria as biosensors of calcium microdomains. Cell Calcium 26, 193-199.
37. Rone MB, Liu J, Blonder J, Ye X, Veenstra TD, Young JC & Papadopoulos V (2009). Targeting and insertion of the cholesterol-binding translocator protein into the outer mitochondrial membrane. Biochemistry 48, 6909-6920.
38. Rouslin W, MacGee J, Gupte S, Wesselman A & Epps DE (1982). Mitochondrial cholesterol content and membrane properties in porcine myocardial ischemia. Am J Physiol 242, H254-H259.
39. Rouslin W, MacGee J, Wesselman AR, Adams RJ & Gupte S (1980). Canine myocardial ischemia: increased mitochondrial cholesterol, a marker of mitochondrial membrane injury. J Mol Cell Cardiol 12, 1475-1482.
40. Shinitzky M & Barenholz Y (1978). Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim Biophys Acta 515, 367-394.
41. Skulachev VP (2000). Mitochondria in the programmed death phenomena; a principle of biology: "it is better to die than to be wrong". IUBMB Life 49, 365-373.
42. Sorice M, Mattei V, Matarrese P, Garofalo T, Tinari A, Gambardella L, Ciarlo L, Manganelli V, Tasciotti V, Misasi R & Malorni W (2012). Dynamics of mitochondrial raft-like microdomains in cell life and death. Commun Integr Biol 5, 217-219.
43. Vadhana D, Carloni M, Fedeli D, Nasuti C & Gabbianelli R (2011a). Perturbation of rat heart plasma membrane fluidity due to metabolites of permethrin insecticide. Cardiovasc Toxicol 11, 226-234.
44. Vadhana MS, Carloni M, Nasuti C, Fedeli D & Gabbianelli R (2011b). Early life permethrin insecticide treatment leads to heart damage in adult rats. Exp Gerontol 46, 731-738.
45. Vadhana MS, Nasuti C & Gabbianelli R (2010). Purine bases oxidation and repair following permethrin insecticide treatment in rat heart cells. Cardiovasc Toxicol 10, 199-207.
46. Voelker DR (2005). Bridging gaps in phospholipid transport. Trends Biochem Sci 30, 396-404.
47. Wharton DC & Tzagoloff A (1967). Cytochrome oxidase from beef heart mitochondria. In Methods in Enzymology, volume 10, ed. Estabrook RW & Pullman ME, pp. 245-250. Academic Press, New York
48. Wheeler G & Tyler KM (2011). Widefield microscopy for live imaging of lipid domains and membrane dynamics. Biochim Biophys Acta 1808, 634-641.
49. Wieckowski MR, Giorgi C, Lebiedzinska M, Duszynski J & Pinton P (2009). Isolation of mitochondria-associated membranes and mitochondria from animal tissues and cells. Nat Protoc 4, 1582-1590.
50. Zheng YZ, Berg KB & Foster LJ (2009). Mitochondria do not contain lipid rafts, and lipid rafts do not contain mitochondrial proteins. J Lipid Res 50, 988-998.
51. Ziolkowski W, Szkatula M, Nurczyk A, Wakabayashi T, Kaczor JJ, Olek RA, Knap N, Antosiewicz J, Wieckowski MR & Wozniak M (2010). Methyl-beta-cyclodextrin induces mitochondrial cholesterol depletion and alters the mitochondrial structure and bioenergetics. FEBS Lett 584, 4606-4610.