Diabetes reduces β-cell mitochondria and induces distinct morphological abnormalities, which are reproducible by high glucose in vitro with attendant dysfunction

Islets

Volumn 4, Issue 3, 2012, Pages 233-242

  Ma, Zuheng ^a   Wirström, Tina ^a   Borg, L A Håkan ^b   Larsson Nyrén, Gerd ^c   Hals, Ingrid ^d   Hansen, John Bondo ^e   Grill, Valdemar ^a,d,f   Björklund, Anneli ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UMEÅ UNIVERSITY   (Sweden)

^d NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^e NOVO NORDISK A S   (Denmark)

^f TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

Author keywords

Diabetes; Electron microscopy; Glucotoxicity; Insulin secretion; Islet transplantation; K+ ATP channel opener; Mitochondria

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE (POTASSIUM); GLUCOSE; TIFENAZOXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DIABETES MELLITUS; FEMALE; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; MALE; MITOCHONDRION; MORPHOMETRICS; NONHUMAN; PANCREAS ISLET BETA CELL; RAT; STREPTOZOCIN DIABETES;

ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; CYCLIC S-OXIDES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; FEMALE; HYPERGLYCEMIA; HYPOGLYCEMIC AGENTS; ISLETS OF LANGERHANS; MALE; MICROSCOPY, ELECTRON; MITOCHONDRIA; RATS; RATS, INBRED WF; RATS, SPRAGUE-DAWLEY;

EID: 84864397721     PISSN: 19382014     EISSN: 19382022     Source Type: Journal    
DOI: 10.4161/isl.20516     Document Type: Article

References (26)

1. Wiederkehr A, Wollheim CB. Minireview: implication of mitochondria in insulin secretion and action. Endocrinology 2006; 147:2643-9; PMID:16556766; http://dx.doi.org/10.1210/en.2006-0057.
2. Fujimoto S, Nabe K, Takehiro M, Shimodahira M, Kajikawa M, Takeda T, et al. Impaired metabolism-secretion coupling in pancreatic β-cells: role of determinants of mitochondrial ATP production. Diabetes Res Clin Pract 2007; 77:2-10; PMID:17449130; http://dx.doi.org/10.1016/j.diabres.2007.01.026.
3. Kennedy ED, Maechler P, Wollheim CB. Effects of depletion of mitochondrial DNA in metabolism secretion coupling in INS-1 cells. Diabetes 1998; 47:374-80; PMID:9519742; http://dx.doi.org/10.2337/diabetes.47.3.374.
4. Soejima A, Inoue K, Takai D, Kaneko M, Ishihara H, Oka Y, et al. Mitochondrial DNA is required for regulation of glucose-stimulated insulin secretion in a mouse pancreatic beta cell line, MIN6. J Biol Chem 1996; 271:26194-9; PMID:8824267; http://dx.doi.org/10.1074/jbc.271.42.26194.
5. Maassen JA, Janssen GM, Hart LM. Molecular mechanisms of mitochondrial diabetes (MIDD). Ann Med 2005; 37:213-21; PMID:16019720; http://dx.doi.org/10. 1080/07853890510007188.
6. Koeck T, Olsson AH, Nitert MD, Sharoyko VV, Ladenvall C, Kotova O, et al. A common variant in TFB1M is associated with reduced insulin secretion and increased future risk of type 2 diabetes. Cell Metab 2011; 13:80-91; PMID:21195351; http://dx.doi.org/10.1016/j.cmet.2010.12.007.
7. Anello M, Lupi R, Spampinato D, Piro S, Masini M, Boggi U, et al. Functional and morphological alterations of mitochondria in pancreatic beta cells from type 2 diabetic patients. Diabetologia 2005; 48:282-9; PMID:15654602; http://dx.doi.org/10.1007/s00125-004-1627-9.
8. Lu H, Koshkin V, Allister EM, Gyulkhandanyan AV, Wheeler MB. Molecular and metabolic evidence for mitochondrial defects associated with beta-cell dysfunction in a mouse model of type 2 diabetes. Diabetes 2010; 59:448-59; PMID:19903739; http://dx.doi.org/10.2337/db09-0129.
9. Hackenbrock CR. 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 1966; 30:269-97; PMID:5968972; http://dx.doi.org/10.1083/jcb.30.2.269.
10. Dimmer KS, Scorrano L. (De)constructing mitochondria: what for? Physiology (Bethesda) 2006; 21:233-41; PMID:16868312; http://dx.doi.org/10.1152/ physiol.00010.2006.
11. Björklund A, Bondo Hansen J, Falkmer S, Grill V. Openers of ATP-dependent K+-channels protect against a signal-transduction-linked and not freely reversible defect of insulin secretion in a rat islet transplantation model of Type 2 diabetes. Diabetologia 2004; 47:885-91; PMID:15088085; http://dx.doi.org/10.1007/s00125-004-1386-7.
12. Choi SY, Huang P, Jenkins GM, Chan DC, Schiller J, Frohman MA. A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat Cell Biol 2006; 8:1255-62; PMID:17028579; http://dx.doi.org/10.1038/ncb1487.
13. Bossy-Wetzel E, Barsoum MJ, Godzik A, Schwarzenbacher R, Lipton SA. Mitochondrial fission in apoptosis, neurodegeneration and aging. Curr Opin Cell Biol 2003; 15:706-16; PMID:14644195; http://dx.doi.org/10.1016/j.ceb.2003.10. 015.
14. Bensellam M, Van Lommel L, Overbergh L, Schuit FC, Jonas JC. Cluster analysis of rat pancreatic islet gene mRNA levels after culture in low-, intermediate- and high-glucose concentrations. Diabetologia 2009; 52:463-76; PMID:19165461; http://dx.doi.org/10.1007/s00125-008-1245-z.
15. Serradas P, Giroix MH, Saulnier C, Gangnerau MN, Borg LA, Welsh M, et al. Mitochondrial deoxyribonucleic acid content is specifically decreased in adult, but not fetal, pancreatic islets of the Goto-Kakizaki rat, a genetic model of noninsulin-dependent diabetes. Endocrinology 1995; 136:5623-31; PMID:7588317; http://dx.doi.org/10.1210/en.136.12.5623.
16. Mizukami H, Wada R, Koyama M, Takeo T, Suga S, Wakui M, et al. Augmented beta cell loss and mitochondrial abnormalities in sucrose-fed GK rats. Virchows Arch 2008; 452:383-92; PMID:18236074; http://dx.doi.org/10.1007/s00428-007-0508- 2.
17. Wikstrom JD, Katzman SM, Mohamed H, Twig G, Graf SA, Heart E, et al. Beta-cell mitochondria exhibit membrane potential heterogeneity that can be altered by stimulatory or toxic fuel levels. Diabetes 2007; 56:2569-78; PMID:17686943; http://dx.doi.org/10.2337/db06-0757.
18. Chen H, Chan DC. Physiological functions of mitochondrial fusion. Ann NY Acad Sci 2010; 1201:21-5; PMID:20649534; http://dx.doi.org/10.1111/j.1749-6632. 2010.05615.x.
19. Zhang Z, Wakabayashi N, Wakabayashi J, Tamura Y, Song WJ, Sereda S, et al. The dynamin-related GTPase Opa1 is required for glucose-stimulated ATP production in pancreatic beta cells. Mol Biol Cell 2011; 22:2235-45; PMID:21551073; http://dx.doi.org/10.1091/mbc.E10-12-0933.
20. Korsgren O, Jansson L, Andersson A. Effects of hyperglycemia on function of isolated mouse pancreatic islets transplanted under kidney capsule. Diabetes 1989; 38:510-5; PMID:2494093; http://dx.doi.org/10.2337/diabetes.38.4.510.
21. Weibel ER, Gomez DM. A principle for counting tissue structures on random sections. J Appl Physiol 1962; 17:343-8; PMID:14005589.
22. Borg LA, Andersson A, Berne C, Westman J. Glucose dependent alterations of mitochondrial ultrastructure and enzyme content in mouse pancreatic islets maintained in tissue culture: a morphometrical and biochemical study. Cell Tissue Res 1975; 162:313-21; PMID:1102103; http://dx.doi.org/10.1007/BF00220177.
23. Herbert V, Lau KS, Gottlieb CW, Bleicher SJ. Coated charcoal immunoassay of insulin. J Clin Endocrinol Metab 1965; 25:1375-84; PMID:5320561; http://dx.doi.org/10.1210/jcem-25-10-1375.
24. Grill V, Rundfeldt M, Efendi S. Previous exposure to glucose enhances somatostatin secretion from the isolated perfused rat pancreas. Diabetologia 1981; 20:495-500; PMID:6113182; http://dx.doi.org/10.1007/BF00253414.
25. Schultz V, Sussman I, Bokvist K, Tornheim K. Bioluminometric assay of ADP and ATP at high ATP/ADP ratios: assay of ADP after enzymatic removal of ATP. Anal Biochem 1993; 215:302-4; PMID:8122794; http://dx.doi.org/10.1006/abio.1993. 1591.
26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262.