Rat diaphragm mitochondria have lower intrinsic respiratory rates than mitochondria in limb muscles

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 300, Issue 6, 2011, Pages 1311-1315

  Garcia Cazarin, Mary L ^a   Gamboa, Jorge L ^a   Andrade, Francisco H ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

Mitochondria respiration; Respiratory muscles; Triceps surae; Uncoupling proteins

Indexed keywords

CYTOCHROME C OXIDASE; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3; VOLTAGE DEPENDENT ANION CHANNEL 1;

AEROBIC CAPACITY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREATHING RATE; CELL FUNCTION; CELL ISOLATION; DIAPHRAGM; MALE; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; RAT; TRICEPS SURAE MUSCLE;

ANIMALS; CELL RESPIRATION; DIAPHRAGM; EXTREMITIES; ION CHANNELS; MALE; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MODELS, ANIMAL; MUSCLE, SKELETAL; OXYGEN CONSUMPTION; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MUSCLES; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 79958852511     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00203.2010     Document Type: Article

References (48)

1. Azzu V, Brand MD. The on-off switches of the mitochondrial uncoupling proteins. Trends Biochem Sci 35: 298-307, 2010.
2. Barrett T, Suzek TO, Troup DB, Wilhite SE, Ngau WC, Ledoux P, Rudnev D, Lash AE, Fujibuchi W, Edgar R. NCBI GEO: mining millions of expression profiles- database and tools. Nucleic Acids Res 33: D562-D566, 2005.
3. Benard G, Faustin B, Passerieux E, Galinier A, Rocher C, Bellance N, Delage JP, Casteilla L, Letellier T, Rossignol R. Physiological diversity of mitochondrial oxidative phosphorylation. Am J Physiol Cell Physiol 291: C1172-C1182, 2006.
4. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
5. Cioffi F, Senese R, de Lange P, Goglia F, Lanni A, Lombardi A. Uncoupling proteins: a complex journey to function discovery. Biofactors 35: 417-428, 2009.
6. Cogswell AM, Stevens RJ, Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol 264: C383-C389, 1993.
7. Couplan E, Gelly C, Goubern M, Fleury C, Quesson B, Silberberg M, Thiaudiere E, Mateo P, Lonchampt M, Levens N, De Montrion C, Ortmann S, Klaus S, Gonzalez-Barroso MD, Cassard-Doulcier AM, Ricquier D, Bigard AX, Diolez P, Bouillaud F. High level of uncoupling protein 1 expression in muscle of transgenic mice selectively affects muscles at rest and decreases their IIb fiber content. J Biol Chem 277: 43079-43088, 2002.
8. De Pinto V, Messina A, Lane DJ, Lawen A. Voltage-dependent anion-selective channel (VDAC) in the plasma membrane. FEBS Lett 584: 1793-1799.
9. Echtay KS. Mitochondrial uncoupling proteins-what is their physiological role? Free Radic Biol Med 43: 1351-1371, 2007.
10. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210, 2002.
11. Finocchietto PV, Franco MC, Holod S, Gonzalez AS, Converso DP, Arciuch VG, Serra MP, Poderoso JJ, Carreras MC. Mitochondrial nitric oxide synthase: a masterpiece of metabolic adaptation, cell growth, transformation, and death. Exp Biol Med (Maywood) 234: 1020-1028, 2009.
12. Frezza C, Cipolat S, Scorrano L. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat Protoc 2: 287-295, 2007.
13. Galganska H, Karachitos A, Wojtkowska M, Stobienia O, Budzinska M, Kmita H. Communication between mitochondria and nucleus: Putative role for VDAC in reduction/oxidation mechanism. Biochim Biophys Acta 1797: 1276-1280.
14. Gamboa JL, Andrade FH. Mitochondrial content and distribution changes specific to mouse diaphragm after chronic normobaric hypoxia. Am J Physiol Regul Integr Comp Physiol 298: R575-R583, 2010.
15. Garcia-Cazarin ML, Fisher TM, Andrade FH. Glucose uptake in rat extraocular muscles: effect of insulin and contractile activity. Invest Ophthalmol Vis Sci 51: 6364-6368.
16. Gilmour MV, Lemberg MR, Chance B. Cytochrome oxidase and its derivatives. IX. Spectrophotometric studies on the rapid reaction of ferrous cytochrome c oxidase with molecular oxygen under conditions of complete and partial oxygenation. Biochim Biophys Acta 172: 37-51, 1969.
17. Hoppeler H, Mathieu O, Krauer R, Claassen H, Armstrong RB, Weibel ER. Design of the mammalian respiratory system. VI. Distribution of mitochondria and capillaries in various muscles. Respir Physiol 44: 87-111, 1981.
18. Keipert S, Klaus S, Heldmaier G, Jastroch M. UCP1 ectopically expressed in murine muscle displays native function and mitigates mitochondrial superox-ide production. Biochim Biophys Acta 1797: 324-330, 2010.
19. Kim EH, Koh EH, Park JY, Lee KU. Adenine nucleotide translocator as a regulator of mitochondrial function: implication in the pathogenesis of metabolic syndrome. Korean Diabetes J 34: 146-153, 2010.
20. Klaus S, Rudolph B, Dohrmann C, Wehr R. Expression of uncoupling protein 1 in skeletal muscle decreases muscle energy efficiency and affects thermoregu-lation and substrate oxidation. Physiol Genomics 21: 193-200, 2005.
21. Kunz WS. Different metabolic properties of mitochondrial oxidative phosphorylation in different cell types-important implications for mito-chondrial cytopathies. Exp Physiol 88: 149-154, 2003.
22. Larrarte E, Margareto J, Novo FJ, Marti A, Alfredo Martinez J. UCP1 muscle gene transfer and mitochondrial proton leak mediated thermogenesis. Arch Biochem Biophys 404: 166-171, 2002.
23. Lawler JM, Kim JH, Kwak HB, Barnes WS. Redox modulation of diaphragm contractility: interaction between DHPR and RyR channels. Free Radic Biol Med. 49: 1969-1977, 2010.
24. Lemasters JJ, Holmuhamedov E. Voltage-dependent anion channel (VDAC) as mitochondrial governator-thinking outside the box. Biochim Biophys Acta 1762: 181-190, 2006.
25. Li B, Nolte LA, Ju JS, Han DH, Coleman T, Holloszy JO, Semenk-ovich CF. Skeletal muscle respiratory uncoupling prevents diet-induced obesity and insulin resistance in mice. Nat Med 6: 1115-1120, 2000.
26. Lindstedt SL, Wells DJ. Skeletal muscle mitochondria: the aerobic gate? Adv Exp Med Biol 227: 207-213, 1988.
27. Manneschi L, Federico A. Polarographic analyses of subsarcolemmal and intermyofibrillar mitochondria from rat skeletal and cardiac muscle. J Neurol Sci 128: 151-156, 1995.
28. Mathieu O, Krauer R, Hoppeler H, Gehr P, Lindstedt SL, Alexander RM, Taylor CR, Weibel ER. Design of the mammalian respiratory system. VII. Scaling mitochondrial volume in skeletal muscle to body mass. Respir Physiol 44: 113-128, 1981.
29. Mathieu-Costello O, Suarez RK, Hochachka PW. Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle. Respir Physiol 89: 113-132, 1992.
30. Mayr R. Structure and distribution of fibre types in the external eye muscles of the rat. Tissue Cell 3: 433-462, 1971.
31. Mollica MP, Lionetti L, Crescenzo R, D'Andrea E, Ferraro M, Liverini G, Iossa S. Heterogeneous bioenergetic behaviour of subsar-colemmal and intermyofibrillar mitochondria in fed and fasted rats. Cell Mol Life Sci 63: 358-366, 2006.
32. Oelkrug R, Kutschke M, Meyer CW, Heldmaier G, Jastroch M. Uncoupling protein 1 decreases superoxide production in brown adipose tissue mitochondria. J Biol Chem 285: 21961-21968, 2009.
33. Paradies G, Petrosillo G, Paradies V, Reiter RJ, Ruggiero FM. Melatonin, cardiolipin and mitochondrial bioenergetics in health and disease. J Pineal Res 48: 297-310, 2008.
34. Parker N, Crichton PG, Vidal-Puig AJ, Brand MD. Uncoupling pro-tein-1 (UCP1) contributes to the basal proton conductance of brown adipose tissue mitochondria. J Bioenerg Biomembr 41: 335-342, 2009.
35. Patel SP, Gamboa JL, McMullen CA, Rabchevsky A, Andrade FH. Lower respiratory capacity in extraocular muscle mitochondria: evidence for intrinsic differences in mitochondrial composition and function. Invest Ophthalmol Vis Sci 50: 180-186, 2009.
36. Patel SP, Sullivan PG, Lyttle TS, Rabchevsky AG. Acetyl-L-carnitine ameliorates mitochondrial dysfunction following contusion spinal cord injury. J Neurochem 114: 291-301, 2006.
37. Patel SP, Sullivan PG, Pandya JD, Rabchevsky AG. Differential effects of the mitochondrial uncoupling agent, 2,4-dinitrophenol, or the nitroxide antioxidant, Tempol, on synaptic or nonsynaptic mitochondria after spinal cord injury. J Neurosci Res 87: 130-140, 2009.
38. Raha S, Robinson BH. Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem Sci 25: 502-508, 2000.
39. Rostovtseva T, Colombini M. VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function. Biophys J 72: 1954-1962, 1997.
40. Rostovtseva TK, Bezrukov SM. VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J Bioenerg Biomembr 40: 163-170, 2008.
41. Rousset S, Alves-Guerra MC, Mozo J, Miroux B, Cassard-Doulcier AM, Bouillaud F, Ricquier D. The biology of mitochondrial uncoupling proteins. Diabetes 53, Suppl 1: S130-S135, 2004.
42. Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, Arbel N. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31: 227-285, 2005.
43. Shoshan-Barmatz V, Israelson A, Brdiczka D, Sheu SS. The voltage-dependent anion channel (VDAC): function in intracellular signalling, cell life and cell death. Curr Pharm Des 12: 2249-2270, 2006.
44. Shoshan-Barmatz V, Keinan N, Zaid H. Uncovering the role of VDAC in the regulation of cell life and death. J Bioenerg Biomembr 40: 183-191, 2008.
45. Sluse FE, Jarmuszkiewicz W, Navet R, Douette P, Mathy G, Sluse-Goffart CM. Mitochondrial UCPs: new insights into regulation and impact. Biochim Biophys Acta 1757: 480-485, 2006.
46. Suarez RK. Hummingbird flight: sustaining the highest mass-specific metabolic rates among vertebrates. Experientia 48: 565-570, 1992.
47. Suarez RK, Lighton JR, Brown GS, Mathieu-Costello O. Mitochon-drial respiration in hummingbird flight muscles. Proc Natl Acad Sci USA 88: 4870-4873, 1991.
48. Supinski G, Nethery D, Stofan D, DiMarco A. Extracellular calcium modulates generation of reactive oxygen species by the contracting diaphragm. J Appl Physiol 87: 2177-2185, 1999.