Fluoxetine-induced pancreatic beta cell dysfunction: New insight into the benefits of folic acid in the treatment of depression

Journal of Affective Disorders

Volumn 166, Issue , 2014, Pages 6-13

  De Long, Nicole E ^a   Hyslop, Jillian R ^a   Raha, Sandeep ^a   Hardy, Daniel B ^b   Holloway, Alison C ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Antidepressant; Beta cell; Folic acid; Mitochondrial dysfunction; Reactive oxygen species; Selective serotonin reuptake inhibitor

Indexed keywords

FLUOXETINE; FOLIC ACID; GLUCOSE; INSULIN; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE; SEROTONIN UPTAKE INHIBITOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DEPRESSION; ENZYME ACTIVITY; INSULIN RELEASE; MITOCHONDRIAL DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RESPIRATORY CHAIN; ANIMAL; CELL LINE; DEPRESSIVE DISORDER, MAJOR; DRUG EFFECTS; FEMALE; HUMAN; MALE; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; CELL LINE; DEPRESSIVE DISORDER, MAJOR; FEMALE; FLUOXETINE; FOLIC ACID; HUMANS; INSULIN-SECRETING CELLS; MALE; RATS; REACTIVE OXYGEN SPECIES; SEROTONIN UPTAKE INHIBITORS;

EID: 84901370946     PISSN: 01650327     EISSN: 15732517     Source Type: Journal    
DOI: 10.1016/j.jad.2014.04.063     Document Type: Article

References (75)

1. W. Abdel-Razaq, D.A. Kendall, and T.E. Bates The effects of antidepressants on mitochondrial function in a model cell system and isolated mitochondria Neurochem. Res. 36 2010 327 338
2. F.R. Agostinho, G.Z. Réus, R.B. Stringari, K.F. Ribeiro, A.K. Ferraro, J. Benedet, N. Rochi, G. Scaini, E.L. Streck, and J. Quevedo Treatment with olanzapine, fluoxetine and olanzapine/fluoxetine alters citrate synthase activity in rat brain Neurosci. Lett. 487 2011 278 281
3. B. Ahren Type 2 diabetes, insulin secretion and beta-cell mass Curr. Mol. Med 5 2005 275 286 (Pubitemid 40663134)
4. F. Andersohn, R. Schade, S. Suissa, and E. Garbe Long-term use of antidepressants for depressive disorders and the risk of diabetes mellitus Am. J. Psychiatry 166 2009 591 598
5. C.A. Beck, S.B. Patten, J.V.A. Williams, J.L. Wang, S.R. Currie, C.J. Maxwell, and N. El-Guebaly Antidepressant utilization in Canada Soc. Psychiatry Psychiatr. Epidemiol. 40 2005 799 807 (Pubitemid 41600191)
6. M. Beyazyüz, Y. Albayrak, O.B. Eǧilmez, N. Albayrak, and E. Beyazyüz Relationship between SSRIs and metabolic syndrome abnormalities in patients with generalized anxiety disorder: a prospective study Psychiatry Investig. 10 2013 148 154
7. S. Bhattacharjee, R. Bhattacharya, G.A. Kelley, and U. Sambamoorthi Antidepressant use and new-onset diabetes: a systematic review and meta-analysis Diabetes Metab. Res. Rev. 29 2013 273 284
8. B. Birmaher, D.A. Brent, and R.S. Benson Summary of the practice parameters for the assessment and treatment of children and adolescents with depressive disorders. J. Am. Acad. Child Adolesc. Psychiatry 11 1998 1234 1238
9. S. Bolisetty, and E.A. Jaimes Mitochondria and reactive oxygen species: physiology and pathophysiology IJMS 14 2013 6306 6344
10. G. Boonstra, D.E. Grobbee, E. Hak, R.S. Kahn, and H. Burger Initiation of antipsychotic treatment by general practitioners. A case-control study J. Eval. Clin. Pract. 17 2011 12 17
11. J.E. Bruin, M.A. Petre, M.A. Lehman, S. Raha, H.C. Gerstein, K.M. Morrison, and A.C. Holloway Maternal nicotine exposure increases oxidative stress in the offspring Free Radic. Biol. Med. 44 2008 1919 1925
12. S. Caccia, M. Cappi, C. Fracasso, and S. Garattini Influence of dose and route of administration on the kinetics of fluoxetine and its metabolite norfluoxetine in the rat Psychopharmacology 100 1990 509 514 (Pubitemid 20102360)
13. J.L. Chiasson, and R. Rabasa-Lhoret Prevention of type 2 diabetes insulin resistance and beta-cell function Diabetes 53 2004 534 538
14. A. Coppen Treatment of depression: time to consider folic acid and vitamin B12 J. Psychopharmacol. 19 2005 59 65
15. A.S. Czaja, and R. Valuck Off-label antidepressant use in children and adolescents compared with young adults: extent and level of evidence Pharmacoepidemiol. Drug Saf. 21 2012 997 1004
16. S. Del Prato, and P. Marchetti Beta-and alpha-cell dysfunction in type 2 diabetes Horm. Metab. Res 11-12 2004 775 781 (Pubitemid 40115899)
17. K. Demyttenaere, R. Bruffaerts, J. Posada-Villa, I. Gasquet, V. Kovess, J.-P. Lépine, M.C. Angermeyer, S. Bernert, G. de Girolamo, P. Morosini, G. Polidori, T. Kikkawa, N. Kawakami, Y. Ono, T. Takeshima, H. Uda, E.G. Karam, J.A. Fayyad, A.N. Karam, Z.N. Mneimneh, M.E. Medina-Mora, G. Borges, C. Lara, R. de Graaf, J. Ormel, O. Gureje, Y. Shen, Y. Huang, M. Zhang, J. Alonso, J.M. Haro, G. Vilagut, E.J. Bromet, S. Gluzman, C. Webb, R.C. Kessler, K.R. Merikangas, J.C. Anthony, Korff, M.R. Von, P.S. Wang, T.S. Brugha, S. Aguilar-Gaxiola, S. Lee, S. Heeringa, B.-E. Pennell, A.M. Zaslavsky, T.B. Ustun, S. Chatterji WHO World Mental Health Survey Consortium Prevalence, severity, and unmet need for treatment of mental disorders in the World Health Organization World Mental Health Surveys JAMA 291 2004 2581 2590 (Pubitemid 38702776)
18. H. Ding, N. Jiang, H. Liu, X. Liu, D. Liu, F. Zhao, L. Wen, S. Liu, L.L. Ji, and Y. Zhang Response of mitochondrial fusion and fission protein gene expression to exercise in rat skeletal muscle Biochim. Biophys. Acta 1800 2010 250 256
19. G. Drews, P. Krippeit-Drews, and M. Düfer Oxidative stress and beta-cell dysfunction Pflug. Arch. 460 2010 703 718
20. M. Fava, and D. Mischoulon Folate in depression: efficacy, safety, differences in formulations, and clinical issues J. Clin. Psychiatry 70 2008 12 17
21. P.A. Figueiredo, R.M. Ferreira, H.J. Appell, and J.A. Duarte Age-induced morphological, biochemical, and functional alterations in isolated mitochondria from murine skeletal muscle J. Gerontology A Biol. Sci. Med. Sci. 63 2008 350 359 (Pubitemid 351738416)
22. M.P.M. Freeman, M.M. Fava, J.J. Lake, M.H.M. Trivedi, K.L.K. Wisner, and D.D. Mischoulon Complementary and alternative medicine in major depressive disorder: the American Psychiatric Association Task Force report J. Clin. Psychiatry 71 2010 669 681
23. A.J. Gelenberg A review of the current guidelines for depression treatment J. Clin. Psychiatry 7 2010 e15
24. S. Gilbody, T. Lightfoot, and T. Sheldon Is low folate a risk factor for depression? a meta-analysis and exploration of heterogeneity J. Epidemiol. Community Health 61 2007 631 637 (Pubitemid 46998897)
25. J.M. Graham Isolation of mitochondria from tissues and cells by differential centrifugation Curr. Protoc. Cell Biol. 4 2001 3.4.1 3.4.2 (Chapter 3, Unit 3.3)
26. Y.S. Han, and C.S. Lee Antidepressants reveal differential effect against 1-methyl-4-phenylpyridinium toxicity in differentiated PC12 cells Eur. J. Pharmacol. 604 2009 36 44
27. H.-C. Hsu, J.-F. Chiou, Y.-H. Wang, C.-H. Chen, S.-Y. Mau, C.-T. Ho, P.-J. Chang, T.-Z. Liu, and C.-H. Chen Folate deficiency triggers an oxidative-nitrosative stress-mediated apoptotic cell death and impedes insulin biosynthesis in RINm5F pancreatic islet β-cells: relevant to the pathogenesis of diabetes PLoS ONE 8 2013 e77931
28. I. Inkielewicz-Stêpniak Impact of fluoxetine on liver damage in rats Pharmacol. Rep. 63 2011 441 447
29. R. Isaac, S. Boura-Halfon, D. Gurevitch, A. Shainskaya, Y. Levkovitz, and Y. Zick Selective Serotonin Reuptake Inhibitors (SSRIs) inhibit insulin secretion and action in pancreatic β cells J. Biol. Chem. 288 2013 5682 5693
30. J.M. Jerrell, A. Tripathi, A.A. Rizvi, and R.S. McIntyre The risk of developing type 2 diabetes mellitus associated with psychotropic drug use in children and adolescents: a retrospective cohort analysis Prim Care Companion CNS Disord. 14 2012
31. P. Ježek, A. Dlasková, and L. Plecitá-Hlavatá Redox homeostasis in pancreatic β cells Oxidative Med. Cell. Longev. 2012 2012 932838
32. S.E. Kahn, D.B. Carr, M.V. Faulenbach, and K.M. Utzschneider An examination of beta-cell function measures and their potential use for estimating beta-cell mass Diabetes, Obes. Metab. 10 Suppl 4 2008 63 76
33. T. Keller, N. Cambon, M. Genevray, F. Crivelli, M. Crivelli, L. Bo, P. Mazzucchelli, S. Ismaili, and A. Marzo Bioequivalence study of fluoxetine hydrochloride in healthy volunteers Arzneimittelforschung 55 2005 491 497 (Pubitemid 41367747)
34. R.W. Lam, S.H. Kennedy, S. Grigoriadis, R.S. McIntyre, R. Milev, R. Ramasubbu, S.V. Parikh, S.B. Patten, A.V. Ravindran Canadian Network for Mood and Anxiety Treatments (CANMAT) Canadian Network for Mood and Anxiety Treatments (CANMAT) clinical guidelines for the management of major depressive disorder in adults. III. pharmacotherapy J. Affect. Disord 117 2009 526 543
35. B.P. Lazalde-Ramos, A.L. Zamora-Perez, M. Sosa-Macías, C. Guerrero-Velázquez, and G.M. Zúñiga-González DNA and oxidative damages decrease after ingestion of folic acid in patients with type 2 diabetes Arch. Med. Res. 43 2012 476 481
36. J.L. Leahy Pathogenesis of type 2 diabetes mellitus Arch. Med. Res 36 2005 197 209 (Pubitemid 40755133)
37. C.S. Lee, Y.J. Kim, E.R. Jang, W. Kim, and S.C. Myung Fluoxetine induces apoptosis in ovarian carcinoma cell line OVCAR-3 through reactive oxygen species-dependent activation of nuclear factor-kappaB Basic Clin. Pharmacol. Toxicol. 106 2010 446 453
38. E. Lee, and A.R. Teschemaker Off-label prescribing patterns of antidepressants in children and adolescents Pharmacoepidemiol. Drug Saf 21 2012 137 144
39. S. Lenzen, J. Drinkgern, and M. Tiedge Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues Free Radic. Biol. Med. 20 1996 463 466 (Pubitemid 26077870)
40. J. Li, S. Donath, Y. Li, D. Qin, B.S. Prabhakar, and P. Li miR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway PLoS Genet. 6 2010 e1000795
41. N. Li, T. Brun, M. Cnop, D.A. Cunha, D.L. Eizirik, and P. Maechler Transient oxidative stress damages mitochondrial machinery inducing persistent beta-cell dysfunction J. Biol. Chem. 284 2009 23602 23612
42. Y. Li, L. Couch, M. Higuchi, J.-L. Fang, and L. Guo Mitochondrial dysfunction induced by sertraline, an antidepressant agent Toxicol. Sci. 127 2012 582 591
43. M Victor, V. Rocha, M. Herance, and R. Hernandez-Mijares, A. Oxidative stress and mitochondrial dysfunction in type 2 diabetes Curr. Pharm. Des. 17 2011 3947 3958
44. M.J. MacDonald, and L.A. Fahien Insulin release in pancreatic islets by a glycolytic and a Krebs cycle intermediate: contrasting patterns of glyceraldehyde phosphate and succinate Arch. Biochem. Biophys. 279 1990 104 108 (Pubitemid 20149779)
45. P. Maechler Mitochondrial function and insulin secretion Mol. Cell. Endocrinol 379 2013 12 18
46. P. Maechler, L. Jornot, and C.B. Wollheim Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells J. Biol. Chem. 274 1999 27905 27913
47. P. Maechler, N. Li, M. Casimir, L. Vetterli, F. Frigerio, and T. Brun Role of mitochondria in beta-cell function and dysfunction Adv. Exp. Med. Biol. 654 2010 193 216
48. S. Majumdar, S. Mukherjee, A. Maiti, S. Karmakar, A.S. Das, M. Mukherjee, A. Nanda, and C. Mitra Folic acid or combination of folic acid and vitamin B 12prevents short-term arsenic trioxide-induced systemic and mitochondrial dysfunction and DNA damage Environ. Toxicol. 24 2009 377 387
49. R.S. McIntyre, K.Y. Park, C.W.Y. Law, F. Sultan, A. Adams, M.T. Lourenco, A.K.S. Lo, J.K. Soczynska, H. Woldeyohannes, M. Alsuwaidan, J. Yoon, and S.H. Kennedy The association between conventional antidepressants and the metabolic syndrome: a review of the evidence and clinical implications CNS Drugs 24 2010 741 753
50. A.-R. Mun, S.-J. Lee, G.-B. Kim, H.-S. Kang, J.-S. Kim, and S.-J. Kim Fluoxetine-induced apoptosis in hepatocellular carcinoma cells Anticancer Res. 33 2013 3691 3697
51. P. Newsholme, E.P. Haber, S.M. Hirabara, E.L.O. Rebelato, J. Procopio, D. Morgan, H.C. Oliveira-Emilio, A.R. Carpinelli, and R. Curi Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity J. Physiol. (Lond.) 583 2007 9 24 (Pubitemid 47244241)
52. M. Olfson, and S.C. Marcus National patterns in antidepressant medication treatment Arch. Gen. Psychiatry 66 2009 848 856
53. A. Pan, N. Keum, O.I. Okereke, Q. Sun, M. Kivimäki, R.R. Rubin, and F.B. Hu Bidirectional association between depression and metabolic syndrome: a systematic review and meta-analysis of epidemiological studies Diabetes Care 35 2012 1171 1180
54. G. Parise, S.M. Phillips, J.J. Kaczor, and M.A. Tarnopolsky Antioxidant enzyme activity is up-regulated after unilateral resistance exercise training in older adults Free Radic. Biol. Med. 39 2005 289 295 (Pubitemid 40814554)
55. N.S. Philip, L.L. Carpenter, A.R. Tyrka, and L.H. Price Augmentation of antidepressants with atypical antipsychotics: a review of the current literature J. Psychiatr. Pract. 14 2008 34 44 (Pubitemid 351158846)
56. J. Pi, Q. Zhang, J. Fu, C.G. Woods, Y. Hou, B.E. Corkey, S. Collins, and M.E. Andersen ROS signaling, oxidative stress and Nrf2 in pancreatic beta-cell function Toxicol. Appl. Pharmacol. 244 2010 77 83
57. 2 signaling pathway: a possible bridge between insulin receptor and mitochondria Curr. Neuropharmacol. 10 2012 311 320
58. L.A. Pratt, D.J. Brody, and Q. Gu Antidepressant use in persons aged 12 and over: United States, NCHS Data Brief Oct (76) 2011 1 8
59. M. Reis, T. Aamo, O. Spigset, and J. Ahlner Serum concentrations of antidepressant drugs in a naturalistic setting: compilation based on a large therapeutic drug monitoring database Ther. Drug Monit. 31 2009 42 56
60. B.N. Renn, L. Feliciano, and D.L. Segal The bidirectional relationship of depression and diabetes: a systematic review Clin. Psychol. Rev. 31 2011 1239 1246
61. S.H. Roberts, E. Bedson, D. Hughes, K. Lloyd, D.B. Menkes, S. Moat, M. Pirmohamed, G. Slegg, J. Thome, R. Tranter, R. Whitaker, C. Wilkinson, and I. Russell Folate augmentation of treatment evaluation for depression (FolATED): protocol of a randomised controlled trial BMC Psychiatry 7 2007 65
62. F. Rotella, and E. Mannucci Depression as a risk factor for diabetes: a meta-analysis of longitudinal studies J. Clin. Psychiatry 74 2013 31 37
63. A. Serretti, and L. Mandelli Antidepressants and body weight: a comprehensive review and meta-analysis J. Clin. Psychiatry 71 2010 1259 1272
64. M.E. Souza, A.C. Polizello, S.A. Uyemura, O. Castro-Silva, and C. Curti Effect of fluoxetine on rat liver mitochondria Biochem. Pharmacol. 48 1994 535 541 (Pubitemid 24257016)
65. L. Stiles, and O.S. Shirihai Mitochondrial dynamics and morphology in beta-cells Best Pract. Res. Clin. Endocrinol. Metab. 26 2012 725 738
66. S. Supale, N. Li, T. Brun, and P. Maechler Mitochondrial dysfunction in pancreatic β cells Trends Endocrinol. Metab. 23 2012 477 487
67. M.J. Taylor, S. Carney, J. Geddes, and G. Goodwin Folate for depressive disorders Cochrane Database Syst. Rev. 2 2, 2003 (CD003390-CD003390)
68. M.J. Taylor, S.M. Carney, G.M. Goodwin, and J.R. Geddes Folate for depressive disorders: systematic review and meta-analysis of randomized controlled trials J. Psychopharmacol. 18 2004 251 256 (Pubitemid 38954914)
69. M. Tiedge, S. Lortz, J. Drinkgern, and S. Lenzen Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells Diabetes 46 1997 1733 1742 (Pubitemid 27456404)
70. S. Unterecker, P. Riederer, F. Proft, J. Maloney, J. Deckert, and B. Pfuhlmann Effects of gender and age on serum concentrations of antidepressants under naturalistic conditions J. Neural Transm. 120 2012 1237 1246
71. D.S. Wald, L. Bishop, N.J. Wald, M. Law, E. Hennessy, D. Weir, J. McPartlin, and J. Scott Randomized trial of folic acid supplementation and serum homocysteine levels Arch. Intern. Med. 161 2001 695 700 (Pubitemid 32200221)
72. D.C. Wallace A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine Annu. Rev. Genet. 39 2005 359 407 (Pubitemid 43011120)
73. J. Wang, J. Williams, D. Lavorato, N. Schmitz, C. Dewa, and S.B. Patten The incidence of major depression in Canada: the nationalpPopulation health survey J. Affect Disord. 123 2010 158 163
74. J.D.L.M.A.A.P.R.N.W. Won-Kyu Ju Glutamate receptor activation triggers OPA1 release and induces apoptotic cell death in ischemic rat retina Mol. Vis. 14 2008 2629
75. C.-S. Wu, S.S.-F. Gau, and M.-S. Lai Long-term antidepressant use and the risk of type 2 diabetes mellitus: a population-based, nested case-control study in Taiwan J. Clin Psychiatry 75 2014 31 38