Insulin therapy modulates mitochondrial dynamics and biogenesis, autophagy and tau protein phosphorylation in the brain of type 1 diabetic rats

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 7, 2014, Pages 1154-1166

  Santos, R X ^a,b   Correia, S C ^b,c   Alves, M G ^d   Oliveira, P F ^d   Cardoso, S ^a,b   Carvalho, C ^a,b   Duarte, A I ^b,c   Santos, M S ^a,b   Moreira, P I ^b,e  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF BEIRA INTERIOR   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Autophagy; Cerebral cortex; Insulin treatment; Mitochondrial fission, fusion and biogenesis; Tau protein phosphorylation; Type 1 diabetes

Indexed keywords

BRAIN PROTEIN; CASPASE 3; CASPASE 9; DYNAMIN I; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3BETA; HEMOGLOBIN A1C; HUMULIN NPH; ISOPHANE INSULIN; MITOCHONDRIAL DNA; POSTSYNAPTIC DENSITY PROTEIN 95; PYRUVIC ACID; STREPTOZOCIN; SYNAPTOPHYSIN; TAU PROTEIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BIOGENESIS; BRAIN CORTEX; CONTROLLED STUDY; DNA DETERMINATION; DRUG EFFECT; DRUG MECHANISM; DRUG SCREENING; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE DOSAGE; GLUCOSE BLOOD LEVEL; HEMOGLOBIN BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN TREATMENT; MALE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RESPIRATORY CHAIN; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS;

AUTOPHAGY; CEREBRAL CORTEX; INSULIN TREATMENT; MITOCHONDRIAL FISSION, FUSION AND BIOGENESIS; TAU PROTEIN PHOSPHORYLATION; TYPE 1 DIABETES;

ANIMALS; AUTOPHAGY; CASPASE 3; CASPASE 9; CEREBRAL CORTEX; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DYNAMINS; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3; INSULIN; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; NF-E2-RELATED FACTOR 2; PHOSPHORYLATION; PYRUVIC ACID; RATS; RATS, WISTAR; TAU PROTEINS;

EID: 84899789863     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.04.011     Document Type: Article

References (66)

1. Gan M.J., Albanese-O'Neill A., Haller M.J. Type 1 diabetes: current concepts in epidemiology, pathophysiology, clinical care, and research. Curr. Probl. Pediatr. Adolesc. Health Care 2012, 42:269-291.
2. Biessels G.J., Deary I.J., Ryan C.M. Cognition and diabetes: a lifespan perspective. Lancet Neurol. 2008, 7:184-190.
3. Ryan C., Vega A., Drash A. Cognitive deficits in adolescents who developed diabetes early in life. Pediatrics 1985, 75:921-927.
4. Jolivalt C.G., Hurford R., Lee C.A., Dumaop W., Rockenstein E., Masliah E. Type 1 diabetes exaggerates features of Alzheimer's disease in APP transgenic mice. Exp. Neurol. 2010, 223:422-431.
5. Cardoso S., Correia S., Santos R.X., Carvalho C., Santos M.S., Oliveira C.R., Perry G., Smith M.A., Zhu X., Moreira P.I. Insulin is a two-edged knife on the brain. J. Alzheimers Dis. 2009, 18:483-507.
6. Zhao W.Q., Chen H., Quon M.J., Alkon D.L. Insulin and the insulin receptor in experimental models of learning and memory. Eur. J. Pharmacol. 2004, 490:71-81.
7. Dore S., Kar S., Quirion R. Insulin-like growth factor I protects and rescues hippocampal neurons against beta-amyloid- and human amylin-induced toxicity. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4772-4777.
8. Takadera T., Sakura N., Mohri T., Hashimoto T. Toxic effect of a beta-amyloid peptide (beta 22-35) on the hippocampal neuron and its prevention. Neurosci. Lett. 1993, 161:41-44.
9. Hong M., Lee V.M. Insulin and insulin-like growth factor-1 regulate tau phosphorylation in cultured human neurons. J. Biol. Chem. 1997, 272:19547-19553.
10. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 1979, 59:527-605.
11. Moreira P.I., Zhu X., Wang X., Lee H.G., Nunomura A., Petersen R.B., Perry G., Smith M.A. Mitochondria: a therapeutic target in neurodegeneration. Biochim. Biophys. Acta 2010, 1802:212-220.
12. Santos R.X., Correia S.C., Wang X., Perry G., Smith M.A., Moreira P.I., Zhu X. Alzheimer's disease: diverse aspects of mitochondrial malfunctioning. Int. J. Clin. Exp. Pathol. 2010, 3:570-581.
13. Correia S.C., Santos R.X., Cardoso S., Carvalho C., Candeias E., Duarte A.I., Placido A.I., Santos M.S., Moreira P.I. Alzheimer disease as a vascular disorder: where do mitochondria fit?. Exp. Gerontol. 2012, 47:878-886.
14. Virbasius J.V., Scarpulla R.C. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:1309-1313.
15. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
16. Santos R.X., Cardoso S., Correia S., Carvalho C., Santos M.S., Moreira P.I. Targeting autophagy in the brain: a promising approach?. Cent. Nerv. Syst. Agents Med. Chem. 2010, 10:158-168.
17. Moreira P.I., Santos R.X., Zhu X., Lee H.G., Smith M.A., Casadesus G., Perry G. Autophagy in Alzheimer's disease. Expert. Rev. Neurother. 2010, 10:1209-1218.
18. Moreira P.I., Santos M.S., Sena C., Seica R., Oliveira C.R. Insulin protects against amyloid beta-peptide toxicity in brain mitochondria of diabetic rats. Neurobiol. Dis. 2005, 18:628-637.
19. Moreira P.I., Santos M.S., Moreno A., Oliveira C. Amyloid beta-peptide promotes permeability transition pore in brain mitochondria. Biosci. Rep. 2001, 21:789-800.
20. Gornall A.G., Bardawill C.J., David M.M. Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 1949, 177:751-766.
21. Estabrook R.E. Mitochondrial respiratory control and the polarographic measurement of ADP/O ratios. Methods Enzymol. 1967, 10:41-47.
22. Chance B., Williams G.R. The respiratory chain and oxidative phosphorylation. Adv. Enzymol. Relat. Subj. Biochem. 1956, 17:65-134.
23. Silva A.M., Oliveira P.J. Evaluation of respiration with clark type electrode in isolated mitochondria and permeabilized animal cells. Methods Mol. Biol. 2012, 810:7-24.
24. Kamo N., Muratsugu M., Hongoh R., Kobatake Y. Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J. Membr. Biol. 1979, 49:105-121.
25. +) to measure membrane potentials in mitochondria: membrane binding and respiratory effects. Biophys. J. 1984, 45:92.
26. Muratsugu M., Kamo N., Kurihara K., Kobatake Y. Selective electrode for dibenzyl dimethyl ammonium cation as indicator of the membrane potential in biological systems. Biochim. Biophys. Acta 1977, 464:613-619.
27. Fuke S., Kubota-Sakashita M., Kasahara T., Shigeyoshi Y., Kato T. Regional variation in mitochondrial DNA copy number in mouse brain. Biochim. Biophys. Acta 2011, 1807:270-274.
28. Brussee V., Cunningham F.A., Zochodne D.W. Direct insulin signaling of neurons reverses diabetic neuropathy. Diabetes 2004, 53:1824-1830.
29. Francis G., Martinez J., Liu W., Nguyen T., Ayer A., Fine J., Zochodne D., Hanson L.R., Frey W.H., Toth C. Intranasal insulin ameliorates experimental diabetic neuropathy. Diabetes 2009, 58:934-945.
30. Reichard P., Nilsson B.Y., Rosenqvist U. The effect of long-term intensified insulin treatment on the development of microvascular complications of diabetes mellitus. N. Engl. J. Med. 1993, 329:304-309.
31. Cardoso S., Santos M.S., Seica R., Moreira P.I. Cortical and hippocampal mitochondria bioenergetics and oxidative status during hyperglycemia and/or insulin-induced hypoglycemia. Biochim. Biophys. Acta 2010, 1802:942-951.
32. Cardoso S., Santos R.X., Correia S.C., Carvalho C., Santos M.S., Baldeiras I., Oliveira C.R., Moreira P.I. Insulin-induced recurrent hypoglycemia exacerbates diabetic brain mitochondrial dysfunction and oxidative imbalance. Neurobiol. Dis. 2012, 49C:1-12.
33. Cooke D.W., Plotnick L. Type 1 diabetes mellitus in pediatrics. Pediatr. Rev. 2008, 29:374-384. (quiz 385).
34. Shah K., Desilva S., Abbruscato T. The role of glucose transporters in brain disease: diabetes and Alzheimer's disease. Int. J. Mol. Sci. 2012, 13:12629-12655.
35. Mans A.M., DeJoseph M.R., Davis D.W., Hawkins R.A. Brain energy metabolism in streptozotocin-diabetes. Biochem. J. 1988, 249:57-62.
36. Planel E., Tatebayashi Y., Miyasaka T., Liu L., Wang L., Herman M., Yu W.H., Luchsinger J.A., Wadzinski B., Duff K.E., Takashima A. Insulin dysfunction induces in vivo tau hyperphosphorylation through distinct mechanisms. J. Neurosci. 2007, 27:13635-13648.
37. Qu Z., Jiao Z., Sun X., Zhao Y., Ren J., Xu G. Effects of streptozotocin-induced diabetes on tau phosphorylation in the rat brain. Brain Res. 2011, 1383:300-306.
38. Abraha A., Ghoshal N., Gamblin T.C., Cryns V., Berry R.W., Kuret J., Binder L.I. C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J. Cell Sci. 2000, 113:3737-3745.
39. Evans D.B., Rank K.B., Bhattacharya K., Thomsen D.R., Gurney M.E., Sharma S.K. Tau phosphorylation at serine 396 and serine 404 by human recombinant tau protein kinase II inhibits tau's ability to promote microtubule assembly. J. Biol. Chem. 2000, 275:24977-24983.
40. Simón D., García-García E., Royo F., Falcón-Pérez J.M., Avila J. Proteostasis of tau. Tau overexpression results in its secretion via membrane vesicles. FEBS Lett. 2012, 586:47-54.
41. Johnson G.V., Jope R.S., Binder L.I. Proteolysis of tau by calpain. Biochem. Biophys. Res. Commun. 1989, 163:1505-1511.
42. Papon M.A., El Khoury N.B., Marcouiller F., Julien C., Morin F., Bretteville A., Petry F.R., Gaudreau S., Amrani A., Mathews P.M., Hebert S.S., Planel E. Deregulation of protein phosphatase 2A and hyperphosphorylation of tau protein following onset of diabetes in NOD mice. Diabetes 2013, 62:609-617.
43. Sharma R., Buras E., Terashima T., Serrano F., Massaad C.A., Hu L., Bitner B., Inoue T., Chan L., Pautler R.G. Hyperglycemia induces oxidative stress and impairs axonal transport rates in mice. PLoS One 2010, 5:e13463.
44. Clodfelder-Miller B.J., Zmijewska A.A., Johnson G.V., Jope R.S. Tau is hyperphosphorylated at multiple sites in mouse brain in vivo after streptozotocin-induced insulin deficiency. Diabetes 2006, 55:3320-3325.
45. Duarte A.I., Santos P., Oliveira C.R., Santos M.S., Rego A.C. Insulin neuroprotection against oxidative stress is mediated by Akt and GSK-3beta signaling pathways and changes in protein expression. Biochim. Biophys. Acta 2008, 1783:994-1002.
46. Ho L., Qin W., Pompl P.N., Xiang Z., Wang J., Zhao Z., Peng Y., Cambareri G., Rocher A., Mobbs C.V., Hof P.R., Pasinetti G.M. Diet-induced insulin resistance promotes amyloidosis in a transgenic mouse model of Alzheimer's disease. FASEB J. 2004, 18:902-904.
47. Yang Y., Zhang J., Ma D., Zhang M., Hu S., Shao S., Gong C.X. Subcutaneous administration of liraglutide ameliorates Alzheimer-associated tau hyperphosphorylation in rats with type 2 diabetes. J. Alzheimers Dis. 2013, 37:637-648.
48. Zhang J.Y., Peng C., Shi H., Wang S., Wang Q., Wang J.Z. Inhibition of autophagy causes tau proteolysis by activating calpain in rat brain. J. Alzheimers Dis. 2009, 16:39-47.
49. Scott P.H., Brunn G.J., Kohn A.D., Roth R.A., Jr Lawrence JC J.C. Evidence of insulin-stimulated phosphorylation and activation of the mammalian target of rapamycin mediated by a protein kinase B signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:7772-7777.
50. Caccamo A., Majumder S., Richardson A., Strong R., Oddo S. Molecular interplay between mammalian target of rapamycin (mTOR), amyloid-beta, and Tau: effects on cognitive impairments. J. Biol. Chem. 2010, 285:13107-13120.
51. Copp J., Manning G., Hunter T. TORC-specific phosphorylation of mammalian target of rapamycin (mTOR): phospho-Ser2481 is a marker for intact mTOR signaling complex 2. Cancer Res. 2009, 69:1821-1827.
52. Klionsky D.J., et al, Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012, 8:445-544.
53. Seibenhener M.L., Babu J.R., Geetha T., Wong H.C., Krishna N.R., Wooten M.W. Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol. Cell. Biol. 2004, 24:8055-8068.
54. Kopeikina K.J., Carlson G.A., Pitstick R., Ludvigson A.E., Peters A., Luebke J.I., Koffie R.M., Frosch M.P., Hyman B.T., Spires-Jones T.L. Tau accumulation causes mitochondrial distribution deficits in neurons in a mouse model of tauopathy and in human Alzheimer's disease brain. Am. J. Pathol. 2011, 179:2071-2082.
55. DuBoff B., Gotz J., Feany M.B. Tau promotes neurodegeneration via DRP1 mislocalization in vivo. Neuron 2012, 75:618-632.
56. Manczak M., Reddy P.H. Abnormal interaction between the mitochondrial fission protein Drp1 and hyperphosphorylated tau in Alzheimer's disease neurons: implications for mitochondrial dysfunction and neuronal damage. Hum. Mol. Genet. 2012, 21:2538-2547.
57. Shenouda S.M., Widlansky M.E., Chen K., Xu G., Holbrook M., Tabit C.E., Hamburg N.M., Frame A.A., Caiano T.L., Kluge M.A., Duess M.A., Levit A., Kim B., Hartman M.L., Joseph L., Shirihai O.S., Vita J.A. Altered mitochondrial dynamics contributes to endothelial dysfunction in diabetes mellitus. Circulation 2011, 124:444-453.
58. Bernardi P., Azzone G.F. Cytochrome c as an electron shuttle between the outer and inner mitochondrial membranes. J. Biol. Chem. 1981, 256:7187-7192.
59. Scorrano L., Ashiya M., Buttle K., Weiler S., Oakes S.A., Mannella C.A., Korsmeyer S.J. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell 2002, 2:55-67.
60. Yamaguchi R., Perkins G. Dynamics of mitochondrial structure during apoptosis and the enigma of Opa1. Biochim. Biophys. Acta 2009, 1787:963-972.
61. Scarpulla R.C. Nuclear control of respiratory gene expression in mammalian cells. J. Cell. Biochem. 2006, 97:673-683.
62. Scarpulla R.C. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 2008, 88:611-638.
63. Edwards J.L., Quattrini A., Lentz S.I., Figueroa-Romero C., Cerri F., Backus C., Hong Y., Feldman E.L. Diabetes regulates mitochondrial biogenesis and fission in mouse neurons. Diabetologia 2010, 53:160-169.
64. Vincent A.M., Edwards J.L., McLean L.L., Hong Y., Cerri F., Lopez I., Quattrini A., Feldman E.L. Mitochondrial biogenesis and fission in axons in cell culture and animal models of diabetic neuropathy. Acta Neuropathol. 2010, 120:477-489.
65. Liu H.Y., Yehuda-Shnaidman E., Hong T., Han J., Pi J., Liu Z., Cao W. Prolonged exposure to insulin suppresses mitochondrial production in primary hepatocytes. J. Biol. Chem. 2009, 284:14087-14095.
66. Valtorta F., Pennuto M., Bonanomi D., Benfenati F. Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis?. Bioessays 2004, 26:445-453.