Antidiabetic drug glyburide modulates depressive-like behavior comorbid with insulin resistance

Journal of Neuroinflammation

Volumn 14, Issue 1, 2017, Pages

  Su, Wen Jun ^a   Peng, Wei ^a   Gong, Hong ^a   Liu, Yun Zi ^a   Zhang, Yi ^a   Lian, Yong Jie ^a   Cao, Zhi Yong ^a,b   Wu, Ran ^a   Liu, Lin Lin ^a   Wang, Bo ^a   Wang, Yun Xia ^a   Jiang, Chun Lei ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b The 102nd Hospital of PLA   (China)

Author keywords

Depression; Glyburide; Inflammation; Insulin resistance; NLRP3 inflammasome; Stress

Indexed keywords

CORTICOSTERONE; CRYOPYRIN; FLUOXETINE; GLIBENCLAMIDE; INFLAMMASOME; INTERLEUKIN 1BETA; THIOREDOXIN INTERACTING PROTEIN; ANTIDIABETIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC STRESS; COMORBIDITY; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; DRUG DETERMINATION; DRUG EFFECT; HIPPOCAMPUS; INSULIN RESISTANCE; INSULIN SIGNALING; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PANCREAS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; METABOLISM; PHYSIOLOGY; PSYCHOLOGY;

ANIMALS; COMORBIDITY; DEPRESSIVE DISORDER; GLYBURIDE; HYPOGLYCEMIC AGENTS; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL;

EID: 85032575586     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-017-0985-4     Document Type: Article

References (75)

1. Kelly SJ, Ismail M. Stress and type 2 diabetes: a review of how stress contributes to the development of type 2 diabetes. Annu Rev Public Health. 2015;36:441-62.
2. DALYs GBD, Collaborators H. Global, regional, and national disability-adjusted life-years (DALYs) for 315 diseases and injuries and healthy life expectancy (HALE), 1990-2015: a systematic analysis for the global burden of disease study 2015. Lancet. 2016;388:1603-58.
3. Tabak AG, Herder C, Rathmann W, Brunner EJ, Kivimaki M. Prediabetes: a high-risk state for diabetes development. Lancet. 2012;379:2279-90.
4. Demakakos P, Pierce MB, Hardy R. Depressive symptoms and risk of type 2 diabetes in a national sample of middle-aged and older adults: the English longitudinal study of aging. Diabetes Care. 2010;33:792-7.
5. Rustad JK, Musselman DL, Nemeroff CB. The relationship of depression and diabetes: pathophysiological and treatment implications. Psychoneuroendocrinology. 2011;36:1276-86.
6. Mezuk B, Eaton WW, Albrecht S, Golden SH. Depression and type 2 diabetes over the lifespan: a meta-analysis. Diabetes Care. 2008;31:2383-90.
7. Campayo A, de Jonge P, Roy JF, Saz P, de la Camara C, Quintanilla MA, Marcos G, Santabarbara J, Lobo A, Project Z. Depressive disorder and incident diabetes mellitus: the effect of characteristics of depression. Am J Psychiatry. 2010;167:580-8.
8. Pan A, Lucas M, Sun Q, van Dam RM, Franco OH, Manson JE, Willett WC, Ascherio A, FB H. Bidirectional association between depression and type 2 diabetes mellitus in women. Arch Intern Med. 2010;170:1884-91.
9. Marazziti D, Rutigliano G, Baroni S, Landi P, Dell'Osso L. Metabolic syndrome and major depression. CNS Spectr. 2014;19:293-304.
10. Moulton CD, Pickup JC, Ismail K. Depression and diabetes 2 the link between depression and diabetes: the search for shared mechanisms. Lancet Diabetes & Endocrinology. 2015;3:461-71.
11. Joseph JJ, Golden SH. Cortisol dysregulation: the bidirectional link between stress, depression, and type 2 diabetes mellitus. Ann N Y Acad Sci. 2017;1391:20-34.
12. Stienstra R, Joosten LA, Koenen T, van Tits B, van Diepen JA, van den Berg SA, Rensen PC, Voshol PJ, Fantuzzi G, Hijmans A, et al. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab. 2010;12:593-605.
13. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT, Brickey WJ, Ting JP. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol. 2011;12:408-15.
14. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM, Dixit VD. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med. 2011;17:179-88.
15. Hotamisligil GS. Inflammation, metaflammation and immunometabolic disorders. Nature. 2017;542:177-85.
16. Lee HM, Kim JJ, Kim HJ, Shong M, BJ K, Jo EK. Upregulated NLRP3 inflammasome activation in patients with type 2 diabetes. Diabetes. 2013;62:194-204.
17. Larsen CM, Faulenbach M, Vaag A, Volund A, Ehses JA, Seifert B, Mandrup-Poulsen T, Donath MY. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med. 2007;356:1517-26.
18. Li M, Li C, Yu H, Cai X, Shen X, Sun X, Wang J, Zhang Y, Wang C. Lentivirus-mediated interleukin-1beta (IL-1beta) knock-down in the hippocampus alleviates lipopolysaccharide (LPS)-induced memory deficits and anxiety- and depression-like behaviors in mice. J Neuroinflammation. 2017;14:190.
19. Goshen I, Kreisel T, Ben-Menachem-Zidon O, Licht T, Weidenfeld J, Ben-Hur T, Yirmiya R. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol Psychiatry. 2008;13:717-28.
20. Alcocer-Gomez E, Ulecia-Moron C, Marin-Aguilar F, Rybkina T, Casas-Barquero N, Ruiz-Cabello J, Ryffel B, Apetoh L, Ghiringhelli F, Bullon P, et al. Stress-induced depressive behaviors require a functional NLRP3 Inflammasome. Mol Neurobiol. 2016;53:4874-82.
21. WJ S, Zhang Y, Chen Y, Gong H, Lian YJ, Peng W, Liu YZ, Wang YX, You ZL, Feng SJ, et al. NLRP3 gene knockout blocks NF-kappaB and MAPK signaling pathway in CUMS-induced depression mouse model. Behav Brain Res. 2017;322:1-8.
22. Zhang Y, Liu L, Liu YZ, Shen XL, Wu TY, Zhang T, Wang W, Wang YX, Jiang CL. NLRP3 Inflammasome mediates chronic mild stress-induced depression in mice via neuroinflammation. Int J Neuropsychopharmacol. 2015;18:pyv006-pyv006.
23. Alcocer-Gomez E, de Miguel M, Casas-Barquero N, Nunez-Vasco J, Sanchez-Alcazar JA, Fernandez-Rodriguez A, Cordero MD. NLRP3 inflammasome is activated in mononuclear blood cells from patients with major depressive disorder. Brain Behav Immun. 2014;36:111-7.
24. Maes M, Song C, Yirmiya R. Targeting IL-1 in depression. Expert Opin Ther Targets. 2012;16:1097-112.
25. Iwata M, Ota KT, Duman RS. The inflammasome: pathways linking psychological stress, depression, and systemic illnesses. Brain Behav Immun. 2013;31:105-14.
26. Kaufmann FN, Costa AP, Ghisleni G, Diaz AP, Rodrigues ALS, Peluffo H, Kaster MP. NLRP3 inflammasome-driven pathways in depression: clinical and preclinical findings. Brain Behav Immun. 2017;64:367-83.
27. Liu YZ, Wang YX, Jiang CL. Inflammation: the common pathway of stress-related diseases. Front Hum Neurosci. 2017;11:316.
28. Frank MG, Watkins LR, Maier SF. The permissive role of glucocorticoids in neuroinflammatory priming: mechanisms and insights. Curr Opin Endocrinol Diabetes Obes. 2015;22:300-5.
29. Busillo JM, Azzam KM, Cidlowski JA: Glucocorticoids sensitize the innate immune system through regulation of the NLRP3 inflammasome (vol 286, pg 38703, 2011). J Biol Chem 2012, 287:13559-13559.
30. Reich E, Tamary A, Sionov RV, Melloul D. Involvement of thioredoxin-interacting protein (TXNIP) in glucocorticoid-mediated beta cell death. Diabetologia. 2012;55:1048-57.
31. Fransson L, Franzen S, Rosengren V, Wolbert P, Sjoholm A, Ortsater H. Beta-cell adaptation in a mouse model of glucocorticoid-induced metabolic syndrome. J Endocrinol. 2013;219:231-41.
32. Lamkanfi M, Mueller JL, Vitari AC, Misaghi S, Fedorova A, Deshayes K, Lee WP, Hoffman HM, Dixit VM. Glyburide inhibits the cryopyrin/Nalp3 inflammasome. J Cell Biol. 2009;187:61-70.
33. Lopez-Castejon G, Pelegrin P. Current status of inflammasome blockers as anti-inflammatory drugs. Expert Opin Investig Drugs. 2012;21:995-1007.
34. Lustman PJ, Freedland KE, Griffith LS, Clouse RE. Fluoxetine for depression in diabetes: a randomized double-blind placebo-controlled trial. Diabetes Care. 2000;23:618-23.
35. Lahmann C, Kramer HB, Ashcroft FM. Systemic administration of glibenclamide Fails to achieve therapeutic levels in the brain and cerebrospinal fluid of rodents. PLoS One. 2015;10:e0134476.
36. Gainey SJ, Kwakwa KA, Bray JK, Pillote MM, Tir VL, Towers AE, Freund GG. Short-term high-fat diet (HFD) induced anxiety-like behaviors and cognitive impairment are improved with treatment by glyburide. Front Behav Neurosci. 2016;10:156.
37. RH D, Tan J, Sun XY, Lu M, Ding JH, Hu G. Fluoxetine inhibits NLRP3 Inflammasome activation: implication in depression. Int J Neuropsychopharmacol. 2016;19
38. Brereton MF, Iberl M, Shimomura K, Zhang Q, Adriaenssens AE, Proks P, Spiliotis II, Dace W, Mattis KK, Ramracheya R, et al. Reversible changes in pancreatic islet structure and function produced by elevated blood glucose. Nat Commun. 2014;5:4639.
39. Pan Y, Chen XY, Zhang QY, Kong LD. Microglial NLRP3 inflammasome activation mediates IL-1beta-related inflammation in prefrontal cortex of depressive rats. Brain Behav Immun. 2014;41:90-100.
40. Tahara A, Matsuyama-Yokono A, Shibasaki M. Effects of antidiabetic drugs in high-fat diet and streptozotocin-nicotinamide-induced type 2 diabetic mice. Eur J Pharmacol. 2011;655:108-16.
41. Meier DT, Morcos M, Samarasekera T, Zraika S, Hull RL, Kahn SE. Islet amyloid formation is an important determinant for inducing islet inflammation in high-fat-fed human IAPP transgenic mice. Diabetologia. 2014;57:1884-8.
42. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol. 2010;11:136-40.
43. Wohleb ES, Franklin T, Iwata M, Duman RS. Integrating neuroimmune systems in the neurobiology of depression. Nat Rev Neurosci. 2016;17:497-511.
44. Lamkanfi M, Dixit VM. Mechanisms and functions of inflammasomes. Cell. 2014;157:1013-22.
45. Boni-Schnetzler M, Donath MY. Increased IL-1beta activation, the culprit not only for defective insulin secretion but also for insulin resistance? Cell Res. 2011;21:995-7.
46. Zhang X, Zhang JH, Chen XY, QH H, Wang MX, Jin R, Zhang QY, Wang W, Wang R, Kang LL, et al. Reactive oxygen species-induced TXNIP drives fructose-mediated hepatic inflammation and lipid accumulation through NLRP3 inflammasome activation. Antioxid Redox Signal. 2015;22:848-70.
47. Chen W, Zhao M, Zhao S, Lu Q, Ni L, Zou C, Lu L, Xu X, Guan H, Zheng Z, Qiu Q. Activation of the TXNIP/NLRP3 inflammasome pathway contributes to inflammation in diabetic retinopathy: a novel inhibitory effect of minocycline. Inflamm Res. 2017;66:157-66.
48. Feng H, Gu J, Gou F, Huang W, Gao C, Chen G, Long Y, Zhou X, Yang M, Liu S, et al. High glucose and lipopolysaccharide prime NLRP3 Inflammasome via ROS/TXNIP pathway in mesangial cells. J Diabetes Res. 2016;2016:6973175.
49. Du RH, Wu FF, Lu M, Shu XD, Ding JH, Wu G, Hu G. Uncoupling protein 2 modulation of the NLRP3 inflammasome in astrocytes and its implications in depression. Redox Biol. 2016;9:178-87.
50. Pan Y, Hong Y, Zhang QY, Kong LD. Impaired hypothalamic insulin signaling in CUMS rats: restored by icariin and fluoxetine through inhibiting CRF system. Psychoneuroendocrinology. 2013;38:122-34.
51. Patel SS, Mehta V, Changotra H, Udayabanu M. Depression mediates impaired glucose tolerance and cognitive dysfunction: a neuromodulatory role of rosiglitazone. Horm Behav. 2016;78:200-10.
52. Su Q, Tao W, Wang H, Chen Y, Huang H, Chen G. Umbelliferone attenuates unpredictable chronic mild stress induced-insulin resistance in rats. IUBMB Life. 2016;68:403-9.
53. Shen JD, Wei Y, Li YJ, Qiao JY, Li YC. Curcumin reverses the depressive-like behavior and insulin resistance induced by chronic mild stress. Metab Brain Dis. 2017;
54. Lim SM, Park SH, Sharma N, Kim SS, Lee JR, Jung JS, Suh HW. Blood glucose regulation mechanism in depressive disorder animal model during hyperglycemic states. Brain Res Bull. 2016;124:116-22.
55. Quan W, Jo EK, Lee MS. Role of pancreatic beta-cell death and inflammation in diabetes. Diabetes Obes Metab. 2013;15(Suppl 3):141-51.
56. Cucak H, Grunnet LG, Rosendahl A. Accumulation of M1-like macrophages in type 2 diabetic islets is followed by a systemic shift in macrophage polarization. J Leukoc Biol. 2014;95:149-60.
57. Donath MY, Dalmas E, Sauter NS, Boni-Schnetzler M. Inflammation in obesity and diabetes: islet dysfunction and therapeutic opportunity. Cell Metab. 2013;17:860-72.
58. Kugelberg E. Diabetes: macrophages mediate beta-cell loss in T2DM. Nat Rev Endocrinol. 2013;9:626.
59. Ernst A, Sharma AN, Elased KM, Guest PC, Rahmoune H, Bahn S. Diabetic db/db mice exhibit central nervous system and peripheral molecular alterations as seen in neurological disorders. Transl Psychiatry. 2013;3:e263.
60. Sharma AN, Elased KM, Garrett TL, Lucot JB. Neurobehavioral deficits in db/db diabetic mice. Physiol Behav. 2010;101:381-8.
61. Kleinridders A, Cai W, Cappellucci L, Ghazarian A, Collins WR, Vienberg SG, Pothos EN, Kahn CR. Insulin resistance in brain alters dopamine turnover and causes behavioral disorders. Proc Natl Acad Sci U S A. 2015;112:3463-8.
62. Dutheil S, Ota KT, Wohleb ES, Rasmussen K, Duman RS. High-fat diet induced anxiety and anhedonia: impact on brain homeostasis and inflammation. Neuropsychopharmacology. 2016;41:1874-87.
63. Yue N, Huang H, Zhu X, Han Q, Wang Y, Li B, Liu Q, Wu G, Zhang Y, Yu J. Activation of P2X7 receptor and NLRP3 inflammasome assembly in hippocampal glial cells mediates chronic stress-induced depressive-like behaviors. J Neuroinflammation. 2017;14:102.
64. Greenwood EA, Pasch LA, Shinkai K, Cedars MI, Huddleston HG. Putative role for insulin resistance in depression risk in polycystic ovary syndrome. Fertil Steril. 2015;104:707-14. e701
65. Yu Q, Hao S, Wang H, Song X, Shen Q, Kang J. Depression-like behavior in a dehydroepiandrosterone-induced mouse model of polycystic ovary syndrome. Biol Reprod. 2016;95:79.
66. Masters SL, Dunne A, Subramanian SL, Hull RL, Tannahill GM, Sharp FA, Becker C, Franchi L, Yoshihara E, Chen Z, et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat Immunol. 2010;11:897-904.
67. ZM X, Yuan F, Liu YL, Ding J, Tian HL. Glibenclamide attenuates blood-brain barrier disruption in adult mice after traumatic brain injury. J Neurotrauma. 2017;34:925-33.
68. Sheth KN, Kimberly WT, Elm JJ, Kent TA, Yoo AJ, Thomalla G, Campbell B, Donnan GA, Davis SM, Albers GW, et al. Exploratory analysis of glyburide as a novel therapy for preventing brain swelling. Neurocrit Care. 2014;21:43-51.
69. Fukuen S, Iwaki M, Yasui A, Makishima M, Matsuda M, Shimomura I. Sulfonylurea agents exhibit peroxisome proliferator-activated receptor gamma agonistic activity. J Biol Chem. 2005;280:23653-9.
70. Chesnokova V, Pechnick RN, Wawrowsky K. Chronic peripheral inflammation, hippocampal neurogenesis, and behavior. Brain Behav Immun. 2016;58:1-8.
71. Aston-Mourney K, Proietto J, Morahan G, Andrikopoulos S. Too much of a good thing: why it is bad to stimulate the beta cell to secrete insulin. Diabetologia. 2008;51:540-5.
72. Remedi MS, Nichols CG. Chronic antidiabetic sulfonylureas in vivo: reversible effects on mouse pancreatic beta-cells. PLoS Med. 2008;5:e206.
73. Gold PW, Licinio J, Pavlatou MG. Pathological parainflammation and endoplasmic reticulum stress in depression: potential translational targets through the CNS insulin, klotho and PPAR-gamma systems. Mol Psychiatry. 2013;18:154-65.
74. Colle R, de Larminat D, Rotenberg S, Hozer F, Hardy P, Verstuyft C, Feve B, Corruble E. PPAR-gamma agonists for the treatment of major depression: a review. Pharmacopsychiatry. 2017;50:49-55.
75. Li R, Wang X, Qin T, Qu R, Ma S. Apigenin ameliorates chronic mild stress-induced depressive behavior by inhibiting interleukin-1beta production and NLRP3 inflammasome activation in the rat brain. Behav Brain Res. 2016;296:318-25.