Glucose Stimulation Induces Dynamic Change of Mitochondrial Morphology to Promote Insulin Secretion in the Insulinoma Cell Line INS-1E

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Jhun, Bong Sook ^b   Lee, Hakjoo ^a   Jin, Zheng Gen ^c   Yoon, Yisang ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; GLUCOSE; PROTON;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CANCER CELL CULTURE; CELL MEMBRANE DEPOLARIZATION; CELL SHAPE; CELL STIMULATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; HORMONAL REGULATION; IN VITRO STUDY; INSULIN METABOLISM; INSULIN RELEASE; INSULIN RESPONSE; INSULINOMA; METABOLIC PARAMETERS; MITOCHONDRIAL MEMBRANE; MUTANT; NONHUMAN; RAT; STRUCTURE ANALYSIS;

ADENOSINE TRIPHOSPHATE; CALCIUM; CELL LINE, TUMOR; GLUCOSE; HUMANS; INSULIN; INSULINOMA;

EID: 84875652238     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060810     Document Type: Article

References (47)

1. Santel A, Fuller MT, (2001) Control of mitochondrial morphology by a human mitofusin. J Cell Sci 114: 867-874.
2. Smirnova E, Griparic L, Shurland DL, van der Bliek AM, (2001) Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell 12: 2245-2256.
3. Pitts KR, Yoon Y, Krueger EW, McNiven MA, (1999) The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol Biol Cell 10: 4403-4417.
4. Cipolat S, Martins de Brito O, Dal Zilio B, Scorrano L, (2004) OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc Natl Acad Sci U S A 101: 15927-15932.
5. Yoon Y, Galloway CA, Jhun BS, Yu T, (2011) Mitochondrial dynamics in diabetes. Antioxid Redox Signal 14: 439-457.
6. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, et al. (2000) OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 26: 211-215.
7. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, et al. (2000) Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 26: 207-210.
8. Zuchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, et al. (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 36: 449-451.
9. Waterham HR, Koster J, van Roermund CW, Mooyer PA, Wanders RJ, et al. (2007) A lethal defect of mitochondrial and peroxisomal fission. N Engl J Med 356: 1736-1741.
10. Benard G, Bellance N, James D, Parrone P, Fernandez H, et al. (2007) Mitochondrial bioenergetics and structural network organization. J Cell Sci 120: 838-848.
11. De Vos KJ, Allan VJ, Grierson AJ, Sheetz MP, (2005) Mitochondrial function and actin regulate dynamin-related protein 1-dependent mitochondrial fission. Curr Biol 15: 678-683.
12. Koopman WJ, Visch HJ, Verkaart S, van den Heuvel LW, Smeitink JA, et al. (2005) Mitochondrial network complexity and pathological decrease in complex I activity are tightly correlated in isolated human complex I deficiency. Am J Physiol Cell Physiol 289: C881-890.
13. Legros F, Lombes A, Frachon P, Rojo M, (2002) Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol Biol Cell 13: 4343-4354.
14. Kennedy ED, Maechler P, Wollheim CB, (1998) Effects of depletion of mitochondrial DNA in metabolism secretion coupling in INS-1 cells. Diabetes 47: 374-380.
15. Maechler P, Wollheim CB, (1998) Role of mitochondria in metabolism-secretion coupling of insulin release in the pancreatic beta-cell. Biofactors 8: 255-262.
16. Plecita-Hlavata L, Lessard M, Santorova J, Bewersdorf J, Jezek P, (2008) Mitochondrial oxidative phosphorylation and energetic status are reflected by morphology of mitochondrial network in INS-1E and HEP-G2 cells viewed by 4Pi microscopy. Biochim Biophys Acta 1777: 834-846.
17. Bindokas VP, Kuznetsov A, Sreenan S, Polonsky KS, Roe MW, et al. (2003) Visualizing superoxide production in normal and diabetic rat islets of Langerhans. J Biol Chem 278: 9796-9801.
18. Dlaskova A, Spacek T, Santorova J, Plecita-Hlavata L, Berkova Z, et al. (2010) 4Pi microscopy reveals an impaired three-dimensional mitochondrial network of pancreatic islet beta-cells, an experimental model of type-2 diabetes. Biochim Biophys Acta.
19. Park KS, Wiederkehr A, Kirkpatrick C, Mattenberger Y, Martinou JC, et al. (2008) Selective actions of mitochondrial fission/fusion genes on metabolism-secretion coupling in insulin-releasing cells. J Biol Chem 283: 33347-33356.
20. Molina AJ, Wikstrom JD, Stiles L, Las G, Mohamed H, et al. (2009) Mitochondrial networking protects beta-cells from nutrient-induced apoptosis. Diabetes 58: 2303-2315.
21. Anello M, Lupi R, Spampinato D, Piro S, Masini M, et al. (2005) Functional and morphological alterations of mitochondria in pancreatic beta cells from type 2 diabetic patients. Diabetologia 48: 282-289.
22. Deng S, Vatamaniuk M, Huang X, Doliba N, Lian MM, et al. (2004) Structural and functional abnormalities in the islets isolated from type 2 diabetic subjects. Diabetes 53: 624-632.
23. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, et al. (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. Embo J 27: 433-446.
24. Zhang Z, Wakabayashi N, Wakabayashi J, Tamura Y, Song WJ, et al. (2011) The dynamin-related GTPase Opa1 is required for glucose-stimulated ATP production in pancreatic beta cells. Mol Biol Cell 22: 2235-2245.
25. Men X, Wang H, Li M, Cai H, Xu S, et al. (2009) Dynamin-related protein 1 mediates high glucose induced pancreatic beta cell apoptosis. Int J Biochem Cell Biol 41: 879-890.
26. Merglen A, Theander S, Rubi B, Chaffard G, Wollheim CB, et al. (2004) Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells. Endocrinology 145: 667-678.
27. Asfari M, Janjic D, Meda P, Li G, Halban PA, et al. (1992) Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130: 167-178.
28. Morgan NG, Short CD, Rumford GM, Montague W, (1985) Effects of the calcium-channel agonist CGP 28392 on insulin secretion from isolated rat islets of Langerhans. Biochem J 231: 629-634.
29. Somers G, Devis G, Malaisse WJ, (1979) Calcium antagonists and islet function. IX. Is extracellular calcium required for insulin release? Acta Diabetol Lat 16: 9-18.
30. MacDonald MJ, Fahien LA, (1990) Insulin release in pancreatic islets by a glycolytic and a Krebs cycle intermediate: contrasting patterns of glyceraldehyde phosphate and succinate. Arch Biochem Biophys 279: 104-108.
31. McCormack JG, Longo EA, Corkey BE, (1990) Glucose-induced activation of pyruvate dehydrogenase in isolated rat pancreatic islets. Biochem J 267: 527-530.
32. Kennedy ED, Maechler P, Wollheim CB, (1998) Effects of depletion of mitochondrial DNA in metabolism secretion coupling in INS-1 cells. Diabetes 47: 374-380.
33. Chen H, Chan DC, (2005) Emerging functions of mammalian mitochondrial fusion and fission. Hum Mol Genet 14: R283-R289.
34. Koopman WJ, Verkaart S, Visch HJ, van der Westhuizen FH, Murphy MP, et al. (2005) Inhibition of complex I of the electron transport chain causes O2-.-mediated mitochondrial outgrowth. Am J Physiol Cell Physiol 288: C1440-C1450.
35. Yu T, Sheu SS, Robotham JL, Yoon Y, (2008) Mitochondrial fission mediates high glucose-induced cell death through elevated production of reactive oxygen species. Cardiovasc Res 79: 341-351.
36. Yoon Y, Pitts KR, McNiven MA, (2001) Mammalian dynamin-like protein DLP1 tubulates membranes. Mol Biol Cell 12: 2894-2905.
37. Perry SW, Norman JP, Barbieri J, Brown EB, Gelbard HA, (2011) Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotechniques 50: 98-115.
38. Nesher R, Cerasi E, (2002) Modeling phasic insulin release: immediate and time-dependent effects of glucose. Diabetes 51Suppl 1: S53-59.
39. Rorsman P, Eliasson L, Renstrom E, Gromada J, Barg S, et al. (2000) The Cell Physiology of Biphasic Insulin Secretion. News Physiol Sci 15: 72-77.
40. Hackenbrock CR, (1966) Ultrastructural bases for metabolically linked mechanical activity in mitochondria: I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J Cell Biol 30: 269-297.
41. Mannella CA, (2006) Structure and dynamics of the mitochondrial inner membrane cristae. Biochim Biophys Acta 1763: 542-548.
42. Gomes LC, Di Benedetto G, Scorrano L, (2011) During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 13: 589-598.
43. Tondera D, Grandemange S, Jourdain A, Karbowski M, Mattenberger Y, et al. (2009) SLP-2 is required for stress-induced mitochondrial hyperfusion. Embo J 28: 1589-1600.
44. Mitra K, Wunder C, Roysam B, Lin G, Lippincott-Schwartz J, (2009) A hyperfused mitochondrial state achieved at G1-S regulates cyclin E buildup and entry into S phase. Proc Natl Acad Sci U S A 106: 11960-11965.
45. Ishihara N, Nomura M, Jofuku A, Kato H, Suzuki SO, et al. (2009) Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat Cell Biol 11: 958-966.
46. Parone PA, Da Cruz S, Tondera D, Mattenberger Y, James DI, et al. (2008) Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS ONE 3: e3257.
47. Benard G, Rossignol R, (2008) Ultrastructure of the mitochondrion and its bearing on function and bioenergetics. Antioxid Redox Signal 10: 1313-1342.