Antidepressant-like and anxiolytic-like effects of hydrogen sulfide in streptozotocin-induced diabetic rats through inhibition of hippocampal oxidative stress

Behavioural Pharmacology

Volumn 26, Issue 5, 2015, Pages 427-435

  Tang, Zhuo Jun ^a,b   Zou, Wei ^a   Yuan, Juan ^a,b   Zhang, Ping ^a   Tian, Ying ^c   Xiao, Zhi Fang ^a   Li, Mang Hong ^a,b   Wei, Hai Jun ^a,b   Tang, Xiao Qing ^a,b  

^a UNIVERSITY OF SOUTH CHINA   (China)

^b Institute of Neuroscience   (China)

^c Sichuan Medical College   (China)

Author keywords

anxiety; depression; diabetes; hydrogen sulfide; oxidative stress; rat; streptozotocin

Indexed keywords

4 HYDROXYNONENAL; GLUCOSE; GLUTATHIONE; HYDROGEN SULFIDE; MALONALDEHYDE; SUPEROXIDE DISMUTASE; 4-HYDROXY-2-NONENAL; ALDEHYDE; ANTIDEPRESSANT AGENT; ANXIOLYTIC AGENT; GLUCOSE BLOOD LEVEL;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ANXIETY; ARTICLE; CONTROLLED STUDY; DEPRESSION; ELEVATED PLUS MAZE TEST; ENZYME INHIBITION; FORCED SWIM TEST; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; MALE; NONHUMAN; OXIDATIVE STRESS; RAT; SIGNAL TRANSDUCTION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; TAIL SUSPENSION TEST; TRANQUILIZING ACTIVITY; ANIMAL; ANXIETY DISORDERS; DEPRESSIVE DISORDER; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ALDEHYDES; ANIMALS; ANTI-ANXIETY AGENTS; ANTIDEPRESSIVE AGENTS; ANXIETY DISORDERS; BLOOD GLUCOSE; DEPRESSIVE DISORDER; DIABETES MELLITUS, EXPERIMENTAL; GLUTATHIONE; HIPPOCAMPUS; HYDROGEN SULFIDE; MALE; MALONDIALDEHYDE; OXIDATIVE STRESS; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE;

EID: 84938782928     PISSN: 09558810     EISSN: 14735849     Source Type: Journal    
DOI: 10.1097/FBP.0000000000000143     Document Type: Article

References (65)

1. Abe K, Kimura H (1996). The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066-1071
2. Anderson RJ, Freedland KE, Clouse RE, Lustman PJ (2001). The prevalence of comorbid depression in adults with diabetes: a meta-Analysis. Diabetes Care 24:1069-1078
3. Baynes JW, Thorpe SR (1999). Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 48:1-9
4. Behr GA, Moreira JC, Frey BN (2012). Preclinical and clinical evidence of antioxidant effects of antidepressant agents: implications for the pathophysiology of major depressive disorder. Oxid Med Cell Longev 2012:609421
5. Bilici M, Efe H, Koroglu MA, Uydu HA, Bekaroglu M, Deger O (2001). Antioxidative enzyme activities and lipid peroxidation in major depression: alterations by antidepressant treatments. J Affect Disord 64:43-51
6. Calvert JW, Coetzee WA, Lefer DJ (2010). Novel insights into hydrogen sulfide - mediated cytoprotection. Antioxid Redox Signal 12:1203-1217
7. Castagné V, Moser P, Roux S, Porsolt RD (2011). Rodent models of depression: forced swim and tail suspension behavioral despair tests in rats and mice. Curr Protoc Neurosci Chapter 8, Unit 8:10A
8. Ceriello A, Bortolotti N, Motz E, Pieri C, Marra M, Tonutti L, et al. (1999). Mealinduced oxidative stress and low-density lipoprotein oxidation in diabetes: the possible role of hyperglycemia. Metabolism 48:1503-1508
9. Chen C, Wang Y, Zhang J, Ma L, Gu J, Ho G (2014). Contribution of neural cell death to depressive phenotypes of streptozotocin-induced diabetic mice. Dis Model Mech 7:723-730
10. Chen WL, Xie B, Zhang C, Xu KL, Niu YY, Tang XQ, et al. (2013). Antidepressantlike and anxiolytic-like effects of hydrogen sulfide in behavioral models of depression and anxiety. Behav Pharmacol 24:590-597
11. Collins MM, Corcoran P, Perry IJ (2009). Anxiety and depression symptoms in patients with diabetes. Diabet Med 26:153-161
12. De Morais H, de Souza CP, da Silva LM, Ferreira DM, Werner MF, Andreatini R, et al. (2014). Increased oxidative stress in prefrontal cortex and hippocampus is related to depressive-like behavior in streptozotocin-diabetic rats. Behav Brain Res 258:52-64
13. Denollet J, Maas K, Knottnerus A, Keyzer JJ, Pop VJ (2009). Anxiety predicted premature all-cause and cardiovascular death in a 10-year follow-up of middle- aged women. J Clin Epidemiol 62:452-456
14. Detke MJ, Rickels M, Lucki I (1995). Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berl) 121:66-72
15. El-Seweidy MM, Sadik NA, Shaker OG (2011). Role of sulfurous mineral water and sodium hydrosulfide as potent inhibitors of fibrosis in the heart of diabetic rats. Arch Biochem Biophys 506:48-57
16. Fava M (2003). Diagnosis and definition of treatment-resistant depression. Biol Psychiatry 53:649-659
17. Feillet-Coudray C, Rock E, Coudray C, Grzelkowska K, Azais-Braesco V, Dardevet D, Mazur A (1999). Lipid peroxidation and antioxidant status in experimental diabetes. Clin Chim Acta 284:31-43
18. Fuchs E, Flïugge G (2006). Experimental animal models for the simulation of depression and anxiety. Dialogues Clin Neurosci 8:323-333
19. Giuliani D, Ottani A, Zaffe D, Galantucci M, Strinati F, Lodi R, Guarini S (2013). Hydrogen sulfide slows down progression of experimental Alzheimer's disease by targeting multiple pathophysiological mechanisms. Neurobiol Learn Mem 104:82-91
20. Gong QH, Wang Q, Pan LL, Liu XH, Huang H, Zhu YZ (2010). Hydrogen sulfide attenuates lipopolysaccharide-induced cognitive impairment: a proinflammatory pathway in rats. Pharmacol Biochem Behav 96:52-58
21. Hirano S, Miyata S, Kamei J (2007). Antidepressant-like effect of leptin in streptozotocin-induced diabetic mice. Pharmacol Biochem Behav 86:27-31
22. Ho N, Balu DT, Hilario MR, Blendy JA, Lucki I (2012). Depressive phenotypes evoked by experimental diabetes are reversed by insulin. Physiol Behav 105:702-708
23. Hovatta I, Juhila J, Donner J (2010). Oxidative stress in anxiety and comorbid disorders. Neurosci Res 68:261-275
24. Hu LF, Lu M, Wu ZY, Wong PT, Bian JS (2009). Hydrogen sulfide inhibits rotenone-induced apoptosis via preservation of mitochondrial function. Mol Pharmacol 75:27-34
25. Hu LF, Lu M, Hon Wong PT, Bian JS (2011). Hydrogen sulfide: neurophysiology and neuropathology. Antioxid Redox Signal 15:405-419
26. Iosifescu DV (2007). Treating depression in the medically ill. Psychiatr Clin North Am 30:77-90
27. Jain SK, Bull R, Rains JL, Bass PF, Levine SN, Reddy S, et al. (2010). Low levels of hydrogen sulfide in the blood of diabetes patients and streptozotocintreated rats causes vascular inflammation? Antioxid Redox Signal 12:1333-1337
28. Kang HJ, Voleti B, Hajszan T, Rajkowska G, Stockmeier CA, Licznerski P, et al. (2012). Decreased expression of synapse-related genes and loss of synapses in major depressive disorder. Nat Med 18:1413-1417
29. Kimura Y, Kimura H (2004). Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18:1165-1167
30. Lee B, Sur B, Kwon S, Yeom M, Shim I, Lee H, Hahm DH (2013). Chronic administration of catechin decreases depression and anxiety-like behaviors in a rat model using chronic corticosterone injections. Biomol Ther (Seoul) 21:313-322
31. Lee SW, Hu YS, Hu LF, Lu Q, Dawe GS, Moore PK, et al. (2006). Hydrogen sulphide regulates calcium homeostasis in microglial cells. Glia 54:116-124
32. Liu J, Guo M, Zhang D, Cheng SY, Liu M, Ding J, et al. (2012). Adiponectin is critical in determining susceptibility to depressive behaviors and has antidepressant-like activity. Proc Natl Acad Sci U S A 109:12248-12253
33. Lu M, Choo CH, Hu LF, Tan BH, Hu G, Bian JS (2010). Hydrogen sulfide regulates intracellular pH in rat primary cultured glia cells. Neurosci Res 66:92-98
34. Lucki I (1997). The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behav Pharmacol 8:523-532
35. Maes M, Galecki P, Chang YS, Berk M (2011). A review on the oxidative and nitrosative stress (O& NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuropsychopharmacol Biol Psychiatry 35:676-692
36. Maritim AC, Sanders RA, Watkins JB III (2003). Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol 17:24-38
37. Mikaliukstiene A, Zagminas K, Juozulynas A, Narkauskaite L, Salyga J, Jankauskiene K, et al. (2014). Prevalence and determinants of anxiety and depression symptoms in patients with type 2 diabetes in Lithuania. Med Sci Monit 20:182-190
38. Miyata S, Hirano S, Kamei J (2005). Abnormal benzodiazepine receptor function in the depressive-like behavior of diabetic mice. Pharmacol Biochem Behav 82:615-620
39. Nagai Y, Tsugane M, Oka J, Kimura H (2004). Hydrogen sulfide induces calcium waves in astrocytes. FASEB J 18:557-559
40. Pan A, Lucas M, Sun Q, van Dam RM, Franco OH, Manson JE, et al. (2010). Bidirectional association between depression and type 2 diabetes mellitus in women. Arch Intern Med 170:1884-1891
41. Patel M, Shah G (2010). Possible role of hydrogen sulfide in insulin secretion and in development of insulin resistance. J Young Pharm 2:148-151
42. Pellow S, Chopin P, File SE, Briley M (1985). Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149-167
43. Pollack MH, Marzol PC (2000). Pharmacotherapeutic options in the treatment of comorbid depression and anxiety. CNS Spectr 5:23-30
44. Porsolt RD, Bertin A, Jalfre M (1977). Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229:327-336
45. Rösen P, Nawroth PP, King G, Möller W, Tritschler HJ, Packer L (2001). The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab Res Rev 17:189-212
46. Schreier SM, Muellner MK, Steinkellner H, Hermann M, Esterbauer H, Exner M, et al. (2010). Hydrogen sulfide scavenges the cytotoxic lipid oxidation product 4-HNE. Neurotox Res 17:249-256
47. Shrivastava SR, Shrivastava PS, Ramasamy J (2013). Role of self-care in management of diabetes mellitus. J Diabetes Metab Disord 12:14
48. Steru L, Chermat R, Thierry B, Simon P (1985). The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl) 85:367-370
49. Szabo C (2012). Roles of hydrogen sulfide in the pathogenesis of diabetes mellitus and its complications. Antioxid Redox Signal 17:68-80
50. Tan BH, Wong PT, Bian JS (2010). Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56:3-10
51. Tang XQ, Yang CT, Chen J, Yin WL, Tian SW, Hu B, et al. (2008). Effect of hydrogen sulphide on beta-Amyloid-induced damage in PC12 cells. Clin Exp Pharmacol Physiol 35:180-186
52. Trief PM, Xing D, Foster NC, Maahs DM, Kittelsrud JM, Olson BA, et al. (2014). Depression in adults in the T1D Exchange Clinic Registry. Diabetes Care 37:1563-1572
53. Verhoof E, Maurice-Stam H, Heymans H, Grootenhuis M (2013). Health-related quality of life, anxiety and depression in young adults with disability benefits due to childhood-onset somatic conditions. Child Adolesc Psychiatry Ment Health 7:12
54. Walf AA, Frye CA (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2:322-328
55. Wang R (2002). Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792-1798
56. Wang R (2010). Hydrogen sulfide: the third gasotransmitter in biology and medicine. Antioxid Redox Signal 12:1061-1064
57. Wetzler S, Katz MM (1989). Problems with the differentiation of anxiety and depression. J Psychiatr Res 23:1-12
58. Whiteman M, Armstrong JS, Chu SH, Jia-Ling S, Wong BS, Cheung NS, et al. (2004). The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J Neurochem 90:765-768
59. Whiteman M, Cheung NS, Zhu YZ, Chu SH, Siau JL, Wong BS, et al. (2005). Hydrogen sulphide: a novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem Biophys Res Commun 326:794-798
60. Xuan A, Long D, Li J, Ji W, Zhang M, Hong L, et al. (2012). Hydrogen sulfide attenuates spatial memory impairment and hippocampal neuroinflammation in beta-Amyloid rat model of Alzheimer's disease. J Neuroinflammation 9:202
61. Yamamoto J, Sato W, Kosugi T, Yamamoto T, Kimura T, Taniguchi S, et al. (2013). Distribution of hydrogen sulfide (H(2)S)-producing enzymes and the roles of the H(2)S donor sodium hydrosulfide in diabetic nephropathy. Clin Exp Nephrol 17:32-40
62. Yin J, Tu C, Zhao J, Ou D, Chen G, Liu Y, Xiao X (2013). Exogenous hydrogen sulfide protects against global cerebral ischemia/reperfusion injury via its antioxidative, anti-inflammatory and anti-Apoptotic effects in rats. Brain Res 1491:188-196
63. Yong QC, Choo CH, Tan BH, Low CM, Bian JS (2010). Effect of hydrogen sulfide on intracellular calcium homeostasis in neuronal cells. Neurochem Int 56:508-515
64. Zhang G, Zhao MS, Xia RH, Wang YH, Zhang GH (2012). Relationship between oxidative stress and depression in patients with rheumatoid arthritis. Beijing Da Xue Xue Bao 44:199-203
65. Zhang Y, Tang ZH, Ren Z, Qu SL, Liu MH, Liu LS, Jiang ZS (2013). Hydrogen sulfide, the next potent preventive and therapeutic agent in aging and ageassociated diseases. Mol Cell Biol 33:1104-1113