Activation of microglia and induction of proinflammatory cytokines in the hippocampus of type 2 diabetic rats

Neurological Research

Volumn 36, Issue 9, 2014, Pages 824-832

  Hwang, In Koo ^a   Choi, Jung Hoon ^b   Nam, Sung Min ^a   Park, Ok Kyu ^c   Yoo, Dae Young ^a   Kim, Woosuk ^a   Yi, Sun Shin ^a,d   Won, Moo Ho ^b   Seong, Je Kyung ^a   Yoon, Yeo Sung ^a  

^a Seoul National University   (South Korea)

^b Kangwon National University   (South Korea)

^c Korea Basic Science Institute (KBSI)   (South Korea)

^d Soonchunhyang University   (South Korea)

Author keywords

Diabetes; Hippocampus; Interferon gamma; Interleukin 1beta; Ionized calcium binding adapter molecule; Microglia

Indexed keywords

ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; CALCIUM BINDING PROTEIN; GAMMA INTERFERON; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE BLOOD LEVEL; IL1B PROTEIN, RAT; INTERLEUKIN 1BETA;

ACUTE DISEASE; AGING; ANIMAL; ASTROCYTE; CHRONIC DISEASE; EXPERIMENTAL DIABETES MELLITUS; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; MICROGLIA; PATHOLOGY; PHYSIOLOGY; WESTERN BLOTTING; ZUCKER RAT;

ACUTE DISEASE; AGING; ANIMALS; ASTROCYTES; BLOOD GLUCOSE; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CHRONIC DISEASE; DIABETES MELLITUS, EXPERIMENTAL; FLUORESCENT ANTIBODY TECHNIQUE; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERFERON-GAMMA; INTERLEUKIN-1BETA; MICROFILAMENT PROTEINS; MICROGLIA; RATS, ZUCKER;

EID: 84905161064     PISSN: 01616412     EISSN: 17431328     Source Type: Journal    
DOI: 10.1179/1743132814Y.0000000330     Document Type: Article

References (70)

1. Davis EJ, Foster TD, Thomas WE. Cellular forms and functions of brain microglia. Brain Res Bull. 1994; 34: 73-8.
2. Block ML, Hong JS. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol. 2005; 76: 77-98.
3. Gehrmann J, Banati RB, Wiessner C, Hossmann KA, Kreutzberg GW. Reactive microglia in cerebral ischaemia: an early mediator of tissue damage? Neuropathol Appl Neurobiol. 1995; 21: 277-89.
4. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996; 19: 312-8.
5. Boche D, Perry VH, Nicoll JA. Review: activation patterns of microglia and their identification in the human brain. Neuropathol Appl Neurobiol. 2013; 39: 3-18.
6. Schöbitz B, De Kloet ER, Holsboer F. Gene expression and function of interleukin 1, interleukin 6 and tumor necrosis factor in the brain. Prog Neurobiol. 1994; 44: 397-432.
7. Hopkins SJ, Rothwell NJ. Cytokine and the nervous system I: expression and recognition. Trends Neurosci. 1995; 18: 83-8.
8. Benveniste EN, Benos DJ. TNF-α-and IFN-γ-mediated signal transduction pathways: effects on glial cell gene expression and function. FASEB J. 1995; 9: 1577-84.
9. Neumann H. Control of glial immune function by neurons. Glia. 2001; 36: 191-9.
10. Mrak RE, Griffin WS. Glia and their cytokines in progression of neurodegeneration. Neurobiol Aging. 2005; 26: 349-54.
11. Porterfield VM, Gabella KM, Simmons MA, Johnson JD. Repeated stressor exposure regionally enhances beta-adrenergic receptor-mediated brain IL-1b production. Brain Behav Immun. 2012; 26: 1249-55.
12. Del Rey A, Apkarian AV, Martina M, Besedovsky HO. Chronic neuropathic pain-like behavior and brain-borne IL-1b. Ann N Y Acad Sci. 2012; 1262: 101-7.
13. Chao PK, Lu KT, Jhu JY, Wo YY, Huang TC, Ro LS, et al. Indomethacin protects rats from neuronal damage induced by traumatic brain injury and suppresses hippocampal IL-1b release through the inhibition of Nogo-A expression. J Neuroinflammation. 2012; 9: 121.
14. Szczytkowski JL, Lebonville C, Hutson L, Fuchs RA, Lysle DT. Heroin-induced conditioned immunomodulation requires expression of IL-1bin the dorsal hippocampus. Brain Behav Immun. 2013; 30: 95-102.
15. Cribbs DH, Berchtold NC, Perreau V, Coleman PD, Rogers J, Tenner AJ, et al. Extensive innate immune gene activation accompanies brain aging, increasing vulnerability to cognitive decline and neurodegeneration: a microarray study. J Neuroinflammation. 2012; 9: 179.
16. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer's disease. Neurobiol Aging. 2000; 21: 383-421.
17. Griffin WS, Sheng JG, Royston MC, Gentleman SM, McKenzie JE, Graham DI, et al. Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol. 1998; 8: 65-72.
18. Griffin WS, Mrak RE. Interleukin-1 in the genesis and progression of and risk for development of neuronal degeneration in Alzheimer's disease. J Leukoc Biol. 2002; 72: 233-8.
19. Rogers J, Mastroeni D, Leonard B, Joyce J, Grover A. Neuroinflammation in Alzheimer's disease and Parkinson's disease: are microglia pathogenic in either disorder? Int Rev Neurobiol. 2007; 82: 235-46.
20. Colangelo V, Schurr J, Ball MJ, Pelaez RP, Bazan NG, Lukiw WJ. Gene expression profiling of 12633 genes in Alzheimer hippocampal CA1: transcription and neurotrophic factor down-regulation and up-regulation of apoptotic and proinflammatory signaling. J Neurosci Res. 2002; 70: 462-73.
21. Ricciarelli R, d'Abramo C, Massone S, Marinari U, Pronzato M, Tabaton M. Microarray analysis in Alzheimer's disease and normal aging. IUBMB Life. 2004; 56: 349-54.
22. Yamamoto M, Kiyota T, Horiba M, Buescher JL, Walsh SM, Gendelman HE, et al. Interferon-cand tumor necrosis factor-a regulate amyloid-bplaque deposition andb-secretase expression in Swedish mutant APP transgenic mice. Am J Pathol. 2007; 170: 680-92.
23. Griffin WS, Nicoll JA, Grimaldi LM, Sheng JG, Mrak RE. The pervasiveness of interleukin-1 in Alzheimer pathogenesis: a role for specific polymorphisms in disease risk. Exp Gerontol. 2000; 35: 481-7.
24. Kilander L, Nyman H, Boberg M, Lithell H. Cognitive function, vascular risk factors and education. A cross-sectional study based on a cohort of 70-year-old men. J Intern Med. 1997; 242: 313-21.
25. Messier C, Awad N, Gagnon M. The relationships between atherosclerosis, heart disease, type 2 diabetes and dementia. Neurol Res. 2004; 26: 567-72.
26. Rönnemaa E, Zethelius B, Sundelöf J, Sundström J, Degerman-Gunnarsson M, Berne C, et al. Impaired insulin secretion increases the risk of Alzheimer disease. Neurology. 2008; 71: 1065-71.
27. Van den Berg E, Kessels RP, Kappelle LJ, de Haan EH, Biessels GJ, Utrecht Diabetic Encephalopathy Study Group. Type 2 diabetes, cognitive function and dementia: vascular and metabolic determinants. Drugs Today (Barc). 2006; 42: 741-54.
28. Li XL, Aou S, Oomura Y, Hori N, Fukunaga K, Hori T. Impairment of long-term potentiation and spatial memory in leptin receptor-deficient rodents. Neuroscience. 2002; 113: 607-15.
29. Clodfelder-Miller BJ, Zmijewska AA, Johnson GV, Jope RS. Tau is hyperphosphorylated at multiple sites in mouse brainin vivo after streptozotocin-induced insulin deficiency. Diabetes. 2006; 55: 3320-5.
30. Li ZG, Zhang W, Sima AA. Alzheimer-like changes in rat models of spontaneous diabetes. Diabetes. 2007; 56: 1817-24.
31. Planel E, Tatebayashi Y, Miyasaka T, Liu L, Wang L, Herman M, et al. Insulin dysfunction induces in vivo tau hyperphosphorylation through distinct mechanisms. J Neurosci. 2007; 27: 13635-48.
32. Stranahan AM, Arumugam TV, Cutler RG, Lee K, Egan JM, Mattson MP. Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci. 2008; 11: 309-17.
33. Stewart R, Liolitsa D. Type 2 diabetes mellitus, cognitive impairment and dementia. Diabet Med. 1999; 16: 93-112.
34. Li L, Hölscher C. Common pathological processes in Alzheimer disease and type 2 diabetes: a review. Brain Res Rev. 2007; 56: 384-402.
35. Moreira RO, Campos SC, Soldera AL. Type 2 diabetes mellitus and Alzheimer's disease: from physiopathology to treatment implications. Diabetes Metab Res Rev. 2013; doi:10.1002/ dmrr. 2442 [Epub ahead of print].
36. Mastrocola R, Restivo F, Vercellinatto I, Danni O, Brignardello E, Aragno M, et al. Oxidative and nitrosative stress in brain mitochondria of diabetic rats. J Endocrinol. 2005; 187: 37-44.
37. Somfai GM, Knippel B, Ruzicska E, Stadler K, Tóth M, Salacz G, et al. Soluble semicarbazide-sensitive amine oxidase (SSAO) activity is related to oxidative stress and subchronic inflammation in streptozotocin-induced diabetic rats. Neurochem Int. 2006; 48: 746-52.
38. Temelkova-Kurktschiev T, Henkel E, Koehler C, Karrei K, Hanefeld M. Subclinical inflammation in newly detected Type II diabetes and impaired glucose tolerance. Diabetologia. 2002; 45: 151.
39. Hwang IK, Yi SS, Kim YN, Kim IY, Lee IS, Yoon YS, et al. Reduced hippocampal cell differentiation in the subgranular zone of the dentate gyrus in a rat model of type II diabetes. Neurochem Res. 2008; 33: 394-400.
40. Yi SS, Hwang IK, Chun MS, Kim YN, Kim IY, Lee IS, et al. Glucocorticoid receptor changes associate with age in the paraventricular nucleus of type II diabetic rat model. Neurochem Res. 2009; 34: 851-8.
41. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. Amsterdam: Elsevier Academic Press; 2007.
42. Bruehl H, Rueger M, Dziobek I, Sweat V, Tirsi A, Javier E, et al. Hypothalamic-pituitary-adrenal axis dysregulation and memory impairments in type 2 diabetes. J Clin Endocrinol Metab. 2007; 92: 2439-45.
43. Debling D, Amelang M, Hasselbach P, Stürmer T. Diabetes and cognitive function in a population-based study of elderly women and men. J Diabetes Complications. 2006; 20: 238-45.
44. Bruehl H, Wolf OT, Sweat V, Tirsi A, Richardson S, Convit A. Modifiers of cognitive function and brain structure in middleaged and elderly individuals with type 2 diabetes mellitus. Brain Res. 2009; 1280: 186-94.
45. Kodl CT, Seaquist ER. Cognitive dysfunction and diabetes mellitus. Endocr Rev. 2008; 29: 494-511.
46. Kawano K, Hirashima T, Mori S, Saitoh Y, Kurosumi M, Natori T. New inbred strain of Long-Evans Tokushima lean rats with IDDM without lymphopenia. Diabetes. 1991; 40: 1375-81.
47. Abrahám H, Losonczy A, Czéh G, Lázár G. Rapid activation of microglial cells by hypoxia, kainic acid, and potassium ions in slice preparations of the rat hippocampus. Brain Res. 2001; 906: 115-26.
48. Cho BP, Sugama S, Shin DH, DeGiorgio LA, Kim SS, Kim YS, et al. Microglial phagocytosis of dopamine neurons at early phases of apoptosis. Cell Mol Neurobiol. 2003; 23: 551-60.
49. Cho BP, Song DY, Sugama S, Shin DH, Shimizu Y, Kim SS, et al. Pathological dynamics of activated microglia following medial forebrain bundle transection. Glia. 2006; 53: 92-102.
50. Graeber MB, Streit WJ, Kreutzberg GW. Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J Neurosci Res. 1988; 21: 18-24.
51. Shaw JA, Perry VH, Mellanby J. Tetanus toxin-induced seizures cause microglial activation in rat hippocampus. Neurosci Lett. 1990; 120: 66-9.
52. Sugama S, Cho BP, Degiorgio LA, Shimizu Y, Kim SS, Kim YS, et al. Temporal and sequential analysis of microglia in the substantia nigra following medial forebrain bundle axotomy in rat. Neuroscience. 2003; 116: 925-33.
53. Zucconi GG, Laurenzi MA, Semprevivo M, Torni F, Lindgren JA, Marinucci E. Microglia activation and cell death in response to diethyl-dithiocarbamate acute administration. J Comp Neurol. 2002; 446: 135-50.
54. Choi JH, Lee CH, Hwang IK, Won MH, Seong JK, Yoon YS, et al. Age-related changes in ionized calcium-binding adapter molecule 1 immunoreactivity and protein level in the gerbil hippocampal CA1 region. J Vet Med Sci. 2007; 69: 1131-6.
55. Hwang IK, Lee CH, Li H, Yoo KY, Choi JH, Kim DW, et al. Comparison of ionized calcium-binding adapter molecule 1 immunoreactivity of the hippocampal dentate gyrus and CA1 region in adult and aged dogs. Neurochem Res. 2008; 33: 1309-15.
56. Yoon SY, Park JS, Choi JE, Choi JM, Lee WJ, Kim SW, et al. Rosiglitazone reduces tau phosphorylation via JNK inhibition in the hippocampus of rats with type 2 diabetes and tau transfected SH-SY5Y cells. Neurobiol Dis. 2010; 40: 449-55.
57. Dinkel K, MacPherson A, Sapolsky RM. Novel glucocorticoid effects on acute inflammation in the CNS. J Neurochem. 2003; 84: 705-16.
58. Nair A, Bonneau, RH. Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J Neuroimmunol. 2006; 171: 72-85.
59. Hwang IK, Yi SS, Yoo KY, Park OK, Yan B, Song W, et al. Effect of treadmill exercise on blood glucose, serum corticosterone levels and glucocorticoid receptor immunoreactivity in the hippocampus in chronic diabetic rats. Neurochem Res. 2011; 36: 281-7.
60. Wei YP, Kita M, Shinmura K, Yan XQ, Fukuyama R, Fushiki S, et al. Expression of IFN-cin cerebrovascular endothelial cells from aged mice. J Interferon Cytokine Res. 2000; 20: 403-9.
61. Hashioka S, Han YH, Fujii S, Kato T, Monji A, Utsumi H, et al. Phosphatidylserine and phosphatidylcholine-containing liposomes inhibit amyloid band interferon-c-induced microglial activation. Free Radic Biol Med. 2007; 42: 945-54.
62. Meda L, Cassatella MA, Szendrei GI, Otvos L Jr, Baron P, Villalba M, et al. Activation of microglial cells by b-amyloid protein and interferon-c. Nature. 1995; 374: 647-50.
63. Mrak RE, Sheng JG, Griffin WS. Glial cytokines in Alzheimer's disease: review and pathogenic implications. Hum Pathol. 1995; 26: 816-23.
64. Akiyama H, Arai T, Kondo H, Tanno E, Haga C, Ikeda K. Cell mediators of inflammation in the Alzheimer disease brain. Alzheimer Dis Assoc Disord. 2000; 14(Suppl 1): S47-53.
65. Murray C, Lynch MA. Evidence that increased hippocampal expression of the cytokine interleukin-1bis a common trigger for age-and stress-induced impairments in long-term potentiation. J Neurosci. 1998; 18: 2974-81.
66. Depino AM, Alonso M, Ferrari C, del Rey A, Anthony D, Besedovsky H, et al. Learning modulation by endogenous hippocampal IL-1: blockade of endogenous IL-1 facilitates memory formation. Hippocampus. 2004; 14: 526-35.
67. Lynch AM, Lynch MA. The age-related increase in IL-1 type I receptor in rat hippocampus is coupled with an increase in caspase-3 activation. Eur J Neurosci. 2001; 15: 1779-88.
68. Koo JW, Duman RS. IL-1bis an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci U S A. 2008; 105: 751-6.
69. Hwang IK, Yi SS, Song W, Won MH, Yoon YS, Seong JK. Effects of age and treadmill exercise in chronic diabetic stages on neuroblast differentiation in a rat model of type 2 diabetes. Brain Res. 2010; 1341: 63-71.
70. Razani-Boroujerdi S, Langley RJ, Singh SP, Pena-Philippides JC, Rir-sima-ah J, Gundavarapu S, et al. The role of IL-1bin nicotine-induced immunosuppression and neuroimmune communication. J Neuroimmune Pharmacol. 2011; 6: 585-96.