β-Cell mitochondria exhibit membrane potential heterogeneity that can be altered by stimulatory or toxic fuel levels

Diabetes

Volumn 56, Issue 10, 2007, Pages 2569-2578

  Wikstrom, Jakob D ^a   Katzman, Shana M ^a   Mohamed, Hibo ^a   Twig, Gilad ^a   Graf, Solomon A ^a   Heart, Emma ^b   Molina, Anthony J A ^a   Corkey, Barbara E ^b   De Vargas, Lina Moitoso ^b   Danial, Nika N ^c   Collins, Sheila ^d   Shirihai, Orian S ^a,e  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

^e TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOKINASE; GLUCOSE; PROTEIN BAD; PROTEIN BCL 2; SUCCINIC ACID METHYL ESTER; UNCOUPLING PROTEIN 2;

ANIMAL CELL; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIABETES MELLITUS; DISEASE MODEL; ELECTRIC POTENTIAL; IN VITRO STUDY; MALE; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN FAMILY; STIMULATION;

ANIMALS; BCL-ASSOCIATED DEATH PROTEIN; CALCIUM; CELL CULTURE TECHNIQUES; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; ION CHANNELS; ISLETS OF LANGERHANS; MAGNESIUM; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS;

EID: 34948890528     PISSN: 00121797     EISSN: 00121797     Source Type: Journal    
DOI: 10.2337/db06-0757     Document Type: Article

References (45)

1. Duchen MR: Roles of mitochondria in health and disease. Diabetes 53 (Suppl. 1):S96-S102, 2004
2. Lowell BB, Shulman GI: Mitochondrial dysfunction and type 2 diabetes. Science 307:384-387, 2005
3. Antinozzi PA, Ishihara H, Newgard CB, Wollheim CB: Mitochondrial metabolism sets the maximal limit of fuel-stimulated insulin secretion in a model pancreatic beta cell: a survey of four fuel secretagogues. J Biol Chem 277:11746-11755, 2002
4. Chan CB, De Leo D, Joseph JW, McQuaid TS, Ha XF, Xu F, Tsushima RG, Pennefather PS, Salapatek AM, Wheeler MB: Increased uncoupling protein-2 levels in β-cells are associated with impaired glucose-stimulated insulin secretion: mechanism of action. Diabetes 50:1302-1310, 1999
5. Heart E, Corkey RF, Wikstrom JD, Shirihai OS, Corkey BE: Glucose-dependent increase in mitochondrial membrane potential, but not cytoplasmic calcium, correlates with insulin secretion in single islet cells. Am J Physiol Endocrinol Metab 290:143-148, 2006
6. Nicholls DG: Mitochondrial membrane potential and aging. Aging Cell 3:35-40, 2004
7. Collins TJ, Berridge MJ, Lipp P, Bootman MD: Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J 21:1616-1627, 2002
8. Kuznetsov AV, Schneeberger S, Renz O, Meusburger H, Saks V, Usson Y, Margreiter R: Functional heterogeneity of mitochondria after cardiac cold ischemia and reperfusion revealed by confocal imaging. Transplantation 77:754-756, 2004
9. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele GD Jr, Chen LB: Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci U S A 88:3671-3675, 1991
10. Diaz G, Setzu MD, Zucca A, Isola R, Diana A, Murru R, Sogos V, Gremo F: Subcellular heterogeneity of mitochondrial membrane potential: relationship with organelle distribution and intercellular contacts in normal, hypoxic and apoptotic cells. J Cell Sci 112:1077-1084, 1999
11. Salvioli S, Dobrucki J, Moretti L, Troiano L, Fernandez MG, Pinti M, Pedrazzi J, Franceschi C, Cossarizza A: Mitochondrial heterogeneity during staurosporine-induced apoptosis in HL60 cells: analysis at the single cell and single organelle level. Cytometry 40:189-197, 2000
12. Kirischuk S, Neuhaus J, Verkhratsky A, Kettenmann H: Preferential localization of active mitochondria in process tips of immature retinal oligodendrocytes. Neuroreport 6:737-741, 1995
13. Danial NN, Gramm CF, Scorrano L, Zhang CY, Krauss S, Ranger AM, Datta SR, Greenberg ME, Licklider LJ, Lowell BB, Gygi SP, Korsmeyer SJ: BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 424:952-956, 2003
14. Krauss S, Zhang CY, Lowell BB: The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol 6:248-261, 2005
15. Boss O, Hagen T, Lowell BB: Uncoupling proteins 2 and 3: potential regulators of mitochondrial energy metabolism. Diabetes 49:143-156, 2000
16. Chan CB, Saleh MC, Koshkin V, Wheeler MB: Uncoupling protein 2 and islet function. Diabetes 53 (Suppl. 1):S136-S142, 2004
17. Zhang CY, Baffy G, Perret P, Krauss S, Peroni O, Grujic D, Hagen T, Vidal-Puig AJ, Boss O, Kim YB, Zheng XX, Wheeler MB, Shulman GI, Chan CB, Lowell BB: Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes. Cell 105:745-755, 2001
18. Joseph JW, Koshkin V, Zhang CY, Wang J, Lowell BB, Chan CB, Wheeler MB: Uncoupling protein 2 knockout mice have enhanced insulin secretory capacity after a high-fat diet. Diabetes 51:3211-3219, 2002
19. Chan CB, MacDonald PE, Saleh MC, Johns DC, Marban E, Wheeler MB: Overexpression of uncoupling protein 2 inhibits glucose-stimulated insulin secretion from rat islets. Diabetes 48:1482-1486, 2001
20. Ranger AM, Zha J, Harada H, Datta SR, Danial NN, Gilmore AP, Kutok JL, Le Beau MM, Greenberg ME, Korsmeyer SJ: Bad-deficient mice develop diffuse large B cell lymphoma. Proc Natl Acad Sci U S A 100:9324-9329, 2003
21. Arsenijevic D, Onuma H, Pecqueur C, Raimbault S, Manning BS, Miroux B, Couplan E, ves-Guerra MC, Goubern M, Surwit R, Bouillaud F, Richard D, Collins S, Ricquier D: Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat Genet 26:435-439, 2000
22. Roduit R, Morin J, Masse F, Segall L, Roche E, Newgard CB, Assimacopoulos-Jeannet F, Prentki M: Glucose down-regulates the expression of the peroxisome proliferator-activated receptor-alpha gene in the pancreatic beta-cell. J Biol Chem 275:35799-35806, 2000
23. Quesada I, Todorova MG, Soria B: Different metabolic responses in alpha, beta and delta-cells of the islet of Langerhans monitored by redox confocal microscopy. Biophys J 90:2641-2650, 2006
24. th, Kuhtreiber WM, Habener JF: Pancreatic beta-cells are rendered glucose-competent by the insulinotropic hormone glucagon-like peptide-1. Nature 361:362-365, 1993
25. Wang X, Zeng W, Murakawa M, Freeman MW, Seed B: Episomal segregation of the adenovirus enhancer sequence by conditional genome rearrangement abrogates late viral gene expression. J Virol 74:11296-11303, 2000
26. de Vargas LM, Sobolewski J, Siegel R, Moss LG: Individual beta cells within the intact islet differentially respond to glucose. J Biol Chem 272:26573-26577, 1997
27. Twig G, Graf SA, Wikstrom JD, Mohamed H, Haigh SE, Elorza AG, Deutsch M, Zurgil N, Reynolds N, Shirihai OS: Tagging and tracking individual networks within a complex mitochondrial web using photoactivatable GFP. Am J Physiol Cell Physiol 291:176-184, 2006
28. Duchen MR, Surin A, Jacobson J: Imaging mitochondrial function in intact cells. Methods Enzymol 361:353-389, 2003
29. Ehrenberg B, Montana V, Wei MD, Wuskell JP, Loew LM: Membrane potential can be determined in individual cells from the nernstian distribution of cationic dyes. Biophys J 53:785-794, 1988
30. O'Reilly CM, Fogarty KE, Drummond RM, Tuft RA, Walsh JV Jr: Quantitative analysis of spontaneous mitochondrial depolarizations. Biophys J 85:3350-3357, 2003
31. Pendergrass W, Wolf N, Poot M: Efficacy of MitoTracker Green and CMXrosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytometry 61:A162-A169, 2004
32. Brand MD, Esteves TC: Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab 2:85-93, 2005
33. Mitchell P: Vectorial chemistry and the molecular mechanics of chemiosmotic coupling: power transmission by proticity. Biochem Soc Trans 4:399-430, 1976
34. Ishihara N, Jofuku A, Eura Y, Mihara K: Regulation of mitochondrial morphology by membrane potential, and DRP1-dependent division and FZO1-dependent fusion reaction in mammalian cells. Biochem Biophys Res Commun 301:891-898, 2003
35. Henquin JC: Pathways in beta-cell stimulus-secretion coupling as targets for therapeutic insulin secretagogues. Diabetes 53 (Suppl. 3):48-58, 2004
36. Kim WH, Lee JW, Suh YH, Hong SH, Choi JS, Lim JH, Song JH, Gao B, Jung MH: Exposure to chronic high glucose induces β-cell apoptosis through decreased interaction of glucokinase with mitochondria: downregulation of glucokinase in pancreatic β-cells. Diabetes 54:2602-2611, 2005
37. Polster BM, Kinnally KW, Fiskum G: BH3 death domain peptide induces cell type-selective mitochondrial outer membrane permeability. J Biol Chem 276:37887-37894, 2001
38. Margineantu DH, Brown RM, Brown GK, Marcus AH, Capaldi RA: Heterogeneous distribution of pyruvate dehydrogenase in the matrix of mitochondria. Mitochondrion 1:327-338, 2002
39. Vanhoutte C, Sener A, Malaisse WJ: Subcellular distribution of hexokinase isoenzymes in pancreatic single beta cells exposed to digitonin after incubation at a low or high concentration of D-glucose. Mol Cell Biochem 175:131-136, 1997
40. Arden C, Harbottle A, Baltrusch S, Tiedge M, Agius L: Glucokinase is an integral component of the insulin granules in glucose-responsive insulin secretory cells and does not translocate during glucose stimulation. Diabetes 53:2346-2352, 2004
41. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J: Role of arabidopsis glucose sensor HXK1 in nutrient, light and hormonal signaling. Science 300:332-336, 2003
42. Mozo J, Ferry G, Studeny A, Pecqueur C, Rodriguez M, Boutin JA, Bouillaud F: Expression of UCP3 in CHO cells does not cause uncoupling but controls mitochondrial activity in the presence of glucose. Biochem J 393:431-439, 2006
43. Takeda Y, Perez-Pinzon MA, Ginsberg MD, Sick TJ: Mitochondria consume energy and compromise cellular membrane potential by reversing ATP synthetase activity during focal ischemia in rats. J Cereb Blood Flow Metab 24:986-992, 2004
44. McCormack JG, Halestrap AP, Denton RM: Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70:391-425, 1990
45. Chen H, Chan DC: Emerging functions of mammalian mitochondrial fusion and fission. Hum Mol Genet 14:283-389, 2005