Disruption of calcium transfer from ER to mitochondria links alterations of mitochondria-associated ER membrane integrity to hepatic insulin resistance

Diabetologia

Volumn 59, Issue 3, 2016, Pages 614-623

  Rieusset, Jennifer ^a   Fauconnier, Jeremy ^b   Paillard, Melanie ^a   Belaidi, Elise ^a   Tubbs, Emily ^a   Chauvin, Marie Agnès ^a   Durand, Annie ^a   Bravard, Amélie ^a   Teixeira, Geoffrey ^a   Bartosch, Birke ^c   Michelet, Maud ^c   Theurey, Pierre ^a   Vial, Guillaume ^a   Demion, Marie ^b   Blond, Emilie ^a,d   Zoulim, Fabien ^c,d   Gomez, Ludovic ^a   Vidal, Hubert ^a   Lacampagne, Alain ^b   Ovize, Michel ^a,d  

^a UNIVERSITÉ LYON 1   (France)

^b UNIV MONTPELLIER   (France)

^c CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^d HOSPICES CIVILS DE LYON   (France)

Author keywords

Calcium signalling; Cyclophilin D; Endoplasmic reticulum; Inositol 1,4,5 triphosphate receptor; Insulin resistance; Liver; Mitochondria; Mitochondria associated endoplasmic reticulum membranes; PKC

Indexed keywords

CALCIUM ION; CYCLOPHILIN D; DIACYLGLYCEROL; INSULIN; PROTEIN KINASE C EPSILON; STRESS ACTIVATED PROTEIN KINASE; TRIACYLGLYCEROL; CALCIUM; CYCLOPHILIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM MEMBRANE; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GENE EXPRESSION; HORMONE ACTION; IN VITRO STUDY; INSULIN RESISTANCE; INSULIN RESPONSE; INTRACELLULAR TRANSPORT; KNOCKOUT MOUSE; LIPID STORAGE; LIVER METABOLISM; LIVER MITOCHONDRION; MEMBRANE DAMAGE; MITOCHONDRIA ASSOCIATED ENDOPLASMIC RETICULUM MEMBRANE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; CELL LINE; GENETICS; HUMAN; LIVER; LIVER CELL; MALE; METABOLISM; PHYSIOLOGY;

ANIMALS; CALCIUM; CELL LINE; CYCLOPHILINS; ENDOPLASMIC RETICULUM; HEPATOCYTES; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INSULIN RESISTANCE; LIVER; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA;

EID: 84957436899     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-015-3829-8     Document Type: Article

References (31)

1. Giorgi C, De Stefani D, Bononi A, Rizzuto R, Pinton P (2009) Structural and functional link between the mitochondrial network and the endoplasmic reticulum. Int J Biochem Cell Biol 41:1817–1827
2. 2+ channels. J Cell Biol 175:901–911
3. 2+ responses. Science 280:1763–1766
4. de Brito OM, Scorrano L (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456:605–610
5. Simmen T, Aslan JE, Blagoveshchenskaya AD et al (2005) PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO J 24:717–729
6. Csordas G, Renken C, Varnai P et al (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174:915–921
7. van Vliet AR, Verfaillie T, Agostinis P (2014) New functions of mitochondria associated membranes in cellular signaling. Biochim Biophys Acta 1843:2253–2262
8. Woodfield K, Ruck A, Brdiczka D, Halestrap AP (1998) Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochem J 336:287–290
9. Paillard M, Tubbs E, Thiebaut PA et al (2013) Depressing mitochondria-reticulum interactions protects cardiomyocytes from lethal hypoxia-reoxygenation injury. Circulation 128:1555–1565
10. Tubbs E, Theurey P, Vial G et al (2014) Mitochondria-associated endoplasmic reticulum membrane (MAM) integrity is required for insulin signaling and is implicated in hepatic insulin resistance. Diabetes 63:3279–3294
11. Betz C, Stracka D, Prescianotto-Baschong C, Frieden M, Demaurex N, Hall MN (2013) Feature article: mTOR complex 2-Akt signaling at mitochondria-associated endoplasmic reticulum membranes (MAM) regulates mitochondrial physiology. Proc Natl Acad Sci U S A 110:12526–12534
12. Sebastian D, Hernandez-Alvarez MI, Segales J et al (2012) Mitofusin 2 (Mfn2) links mitochondrial and endoplasmic reticulum function with insulin signaling and is essential for normal glucose homeostasis. Proc Natl Acad Sci U S A 109:5523–5528
13. Hagiwara A, Cornu M, Cybulski N et al (2012) Hepatic mTORC2 activates glycolysis and lipogenesis through Akt, glucokinase, and SREBP1c. Cell Metab 15:725–738
14. Ye R, Ni M, Wang M et al (2011) Inositol 1,4,5-trisphosphate receptor 1 mutation perturbs glucose homeostasis and enhances susceptibility to diet-induced diabetes. J Endocrinol 210:209–217
15. Schinzel AC, Takeuchi O, Huang Z et al (2005) Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci U S A 102:12005–12010
16. Takahashi A, Camacho P, Lechleiter JD, Herman B (1999) Measurement of intracellular calcium. Physiol Rev 79:1089–1125
17. Berry MN, Friend DS (1969) High-yield preparation of isolated rat liver parenchymal cells: a biochemical and fine structural study. J Cell Biol 43:506–520
18. Nicolli A, Basso E, Petronilli V, Wenger RM, Bernardi P (1996) Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, and cyclosporin A-sensitive channel. J Biol Chem 271:2185–2192
19. Zhao Q, Wang J, Levichkin IV, Stasinopoulos S, Ryan MT, Hoogenraad NJ (2002) A mitochondrial specific stress response in mammalian cells. EMBO J 21:4411–4419
20. Ozcan U, Cao Q, Yilmaz E et al (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457–461
21. Bravo R, Vicencio JM, Parra V et al (2011) Increased ER-mitochondrial coupling promotes mitochondrial respiration and bioenergetics during early phases of ER stress. J Cell Sci 124:2143–2152
22. Cardenas C, Miller RA, Smith I et al (2010) Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 142:270–283
23. Kumashiro N, Erion DM, Zhang D et al (2011) Cellular mechanism of insulin resistance in nonalcoholic fatty liver disease. Proc Natl Acad Sci U S A 108:16381–16385
24. Quarato G, D'Aprile A, Gavillet B et al (2012) The cyclophilin inhibitor alisporivir prevents hepatitis C virus-mediated mitochondrial dysfunction. Hepatology 55:1333–1343
25. Li H, Min Q, Ouyang C et al (2014) AMPK activation prevents excess nutrient-induced hepatic lipid accumulation by inhibiting mTORC1 signaling and endoplasmic reticulum stress response. Biochim Biophys Acta 1842:1844–1854
26. Ning J, Hong T, Ward A et al (2011) Constitutive role for IRE1a-XBP1 signaling pathway in the insulin-mediated hepatic lipogenic program. Endocrinology 152:2247–2255
27. Zhang C, Chen X, Zhu RM et al (2012) Endoplasmic reticulum stress is involved in hepatic SREBP-1c activation and lipid accumulation in fructose-fed mice. Toxicol Lett 212:229–240
28. Jurczak MJ, Lee AH, Jornayvaz FR et al (2012) Dissociation of inositol-requiring enzyme (IRE1alpha)-mediated c-Jun N-terminal kinase activation from hepatic insulin resistance in conditional X-box-binding protein-1 (XBP1) knock-out mice. J Biol Chem 287:2558–2567
29. Ozcan L, Wong CC, Li G et al (2012) Calcium signaling through CaMKII regulates hepatic glucose production in fasting and obesity. Cell Metab 15:739–751
30. Wang Y, Li G, Goode J et al (2012) Inositol-1,4,5-trisphosphate receptor regulates hepatic gluconeogenesis in fasting and diabetes. Nature 485:128–132
31. Arruda AP, Pers BM, Parlakgül G et al (2014) Chronic enrichment of hepatic endoplasmic reticulum-mitochondria contact leads to mitochondrial dysfunction in obesity. Nat Med 20:1427–1435