Minor role of mitochondrial respiration for fatty-acid induced insulin secretion

International Journal of Molecular Sciences

Volumn 14, Issue 9, 2013, Pages 18989-18998

  Schulz, Nadja ^a   Kluth, Oliver ^a   Jastroch, Martin ^b   Schürmann, Annette ^a  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Coupling efficiency; Insulin secretion; Pancreatic islets; Respiratory activity

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA; FATTY ACID; GLUCOSE; INSULIN; OXYGEN; PALMITIC ACID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ANALYZER; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA CONTENT; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR FLUX ANALYZER; FATTY ACID METABOLISM; INSULIN RELEASE; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PANCREAS ISLET; SYNTHESIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; GLUCOSE; INSULIN; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED DBA; MITOCHONDRIA; OXYGEN CONSUMPTION; PALMITIC ACID;

EID: 84884180095     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140918989     Document Type: Article

References (29)

1. Bartlett, K.; Eaton, S. Mitochondrial beta-oxidation. Eur. J. Biochem. 2004, 271, 462-469.
2. Houten, S.M.; Wanders, R.J. A general introduction to the biochemistry of mitochondrial fatty acid β-oxidation. J. Inherit. Metab. Dis. 2010, 33, 469-477.
3. Hue, L.; Taegtmeyer, H. The Randle cycle revisited: A new head for an old hat. Am. J. Physiol. Endocrinol. Metab. 2009, 297, E578-E591.
4. Kluth, O.; Mirhashemi, F.; Scherneck, S.; Kaiser, D.; Kluge, R.; Neschen, S.; Joost, H.G.; Schürmann, A. Dissociation of lipotoxicity and glucotoxicity in a mouse model of obesity associated diabetes: Role of forkhead box O1 (FOXO1) in glucose-induced beta cell failure. Diabetologia 2011, 54, 605-616.
5. Vernier, S.; Chiu, A.; Schober, J.; Weber, T.; Nguyen, P.; Luer, M.; McPherson, T.; Wanda, P.E.; Marshall, C.; Rohatgi, N. Beta-cell metabolic alterations under chronic nutrient overload in rat and human islets. Islets 2012, 4, 379-392.
6. Henquin, J.C. The dual control of insulin secretion by glucose involves triggering and amplifying pathways in beta-cells. Diabetes Res. Clin. Pract. 2011, 93, S27-S31.
7. MacDonald, P.E. Signal integration at the level of ion channel and exocytotic function in pancreatic β-cells. Am. J. Physiol. Endocrinol. Metab. 2011, 301, E1065-E1069.
8. Roduit, R.; Nolan, C.; Alarcon, C.; Moore, P.; Barbeau, A.; Delghingaro-Augusto, V.; Przybykowski, E.; Morin, J.; Masse, F.; Massie, B.; et al. A role for the malonyl-CoA/long-chain acyl-CoA pathway of lipid signaling in the regulation of insulin secretion in response to both fuel and nonfuel stimuli. Diabetes 2004, 53, 1007-1019.
9. Crespin, S.R.; Greenough, W.B., III; Steinberg, D. Stimulation of insulin secretion by infusion of free fatty acids. J. Clin. Invest. 1969, 48, 1934-1943.
10. Alquier, T.; Peyot, M.L.; Latour, M.G.; Kebede, M.; Sorensen, C.M.; Gesta, S.; Kahn, R.C.; Smith, R.D.; Jetton, T.L.; Metz, T.O. Deletion of GPR40 impairs glucose-induced insulin secretion in vivo in mice without affecting intracellular fuel metabolism in islets. Diabetes 2009, 58, 2607-2615.
11. Latour, M.G.; Alquier, T.; Oseid, E.; Tremblay, C.; Jetton, T.L.; Luo, J.; Lin, D.C.; Poitout, V. GPR40 is necessary but not sufficient for fatty acid stimulation of insulin secretion in vivo. Diabetes 2007, 56, 1087-1094.
12. Poitout, V.; Hagman, D.; Stein, R.; Artner, I.; Robertson, R.P.; Harmon, J.S. Regulation of the insulin gene by glucose and fatty acids. J. Nutr. 2006, 136, 873-876.
13. Prentki, M.; Joly, E.; El-Assaad, W.; Roduit, R. Malonyl-CoA signaling, lipid partitioning, and glucolipotoxicity: Role in beta-cell adaptation and failure in the etiology of diabetes. Diabetes 2002, 51, S405-S413.
14. Lee, Y.; Hirose, H.; Ohneda, M.; Johnson, J.H.; McGarry, J.D.; Unger, R.H. Beta-cell lipotoxicity in the pathogenesis of non-insulin-dependent diabetes mellitus of obese rats: Impairment in adipocyte-beta-cell relationships. Proc. Natl. Acad. Sci. USA 1994, 91, 10878-10882.
15. El-Assaad, W.; Buteau, J.; Peyot, M.L.; Nolan, C.; Roduit, R.; Hardy, S.; Joly, E.; Dbaibo, G.; Rosenberg, L.; Prentki, M. Saturated fatty acids synergize with elevated glucose to cause pancreatic beta-cell death. Endocrinology 2003, 144, 4154-4163.
16. Wikstrom, J.D.; Sereda, S.B.; Stiles, L.; Elorza, A.; Allister, E.M.; Neilson, A.; Ferrick, D.A.; Wheeler, M.B.; Shirihai, O.S. A novel high-throughput assay for islet respiration reveals uncoupling of rodent and human islets. PLoS One 2012, 7, e33023.
17. Schulz, N.; Himmelbauer, H.; Rath, M.; van Weeghel, M.; Houten, S.; Kulik, W.; Suhre, K.; Scherneck, S.; Vogel, H.; Kluge, R.; et al. Role of medium- and short-chain L-3-hydroxyacyl-CoA dehydrogenase in the regulation of body weight and thermogenesis. Endocrinology 2011, 152, 4641-4651.
18. Warnotte, C.; Gilon, P.; Nenquin, M.; Henquin, J.C. Mechanisms of the stimulation of insulin release by saturated fatty acids. Diabetes 1994, 43, 703-711.
19. Henquin, J.; Ishiyama, N.; Nenquin, M.; Ravier, M.A.; Jonas, J.C. Signals and pools underlying biphasic insulin secretion. Diabetes 2002, 51, S60-S67.
20. Cantley, J.; Biden, T.J. Targeting triglyceride/fatty acid cycling in beta-cells as a therapy for augmenting glucose-stimulated insulin secretion. Islets 2010, 2, 127-129.
21. Nolan, C.J.; Prentki, M. The islet beta-cell: Fuel responsive and vulnerable. Trends Endocrinol. Metab. 2008, 19, 285-291.
22. St-Pierre, J.; Buckingham, J.A.; Roebuck, S.J.; Brand, M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 2002, 277, 44784-44790.
23. Echtay, K.S.; Murphy, M.P.; Smith, R.A.; Talbot, D.A.; Brand, M.D. Superoxide activates mitochondrial uncoupling protein 2 from the matrix side. Studies using targeted antioxidants. J. Biol. Chem. 2002, 277, 47129-47135.
24. Brand, M.D.; Affourtit, C.; Esteves, T.C.; Green, K.; Lambert, A.J.; Miwa, S.; Pakay, J.L.; Parker, N. Mitochondrial superoxide: Production, biological effects, and activation of uncoupling proteins. Free Radic. Biol. Med. 2004, 37, 755-767.
25. Affourtit, C.; Brand, M.D. Stronger control of ATP/ADP by proton leak in pancreatic beta-cells than skeletal muscle mitochondria. Biochem. J. 2006, 393, 151-159.
26. Affourtit, C.; Jastroch, M.; Brand, M.D. Uncoupling protein-2 attenuates glucose-stimulated insulin secretion in INS-1E insulinoma cells by lowering mitochondrial reactive oxygen species. Free Radic. Biol. Med. 2010, 50, 609-616.
27. Prentki, M.; Corkey, B.E. Are the beta-cell signaling molecules malonyl-CoA and cystolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 1996, 45, 273-283.
28. Preparation of bovine serum albumin-conjugated palmitate. Technical protocol access from Seahorse Bioscience resources. Available online: http://www.seahorsebio.com/resources/tech-writing/protocol-bsa-palmitate.pdf (accessed on 30 December 2011).
29. Ferrick, D.A.; Neilson, A.; Beeson, C. Advances in measuring cellular bioenergetics using extracellular flux. Drug Discov. Today 2008, 13, 268-274.