Rodent models of neuroinflammation for Alzheimer's disease

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Nazem, Amir ^a   Sankowski, Roman ^a   Bacher, Michael ^b   Al Abed, Yousef ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Alzheimer's disease; Amyloid ; Animal models; Innate immunity; Neurodegeneration; Neuroinflammation; Tau protein

Indexed keywords

AMYLOID BETA PROTEIN; COLCHICINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MAJOR HISTOCOMPATIBILITY ANTIGEN; NERVE GROWTH FACTOR; OKADAIC ACID; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN P25; REACTIVE OXYGEN METABOLITE; STREPTOZOCIN; TAU PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ASTROCYTOSIS; C3 GENE; CELL ACTIVATION; COGNITIVE DEFECT; DISEASE MODEL; EXPERIMENTAL ANIMAL; GENE INACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC MANIPULATION; HUMAN; LEARNING DISORDER; MEMORY DISORDER; MHC GENE; MICROGLIA; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROFIBRILLARY TANGLE; NONHUMAN; OXIDATIVE STRESS; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN HYPERPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REVIEW; TRANSGENIC ANIMAL; ANIMAL; COMPLICATION; ENCEPHALITIS;

ALZHEIMER DISEASE; ANIMALS; DISEASE MODELS, ANIMAL; ENCEPHALITIS; HUMANS;

EID: 84949117638     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0291-y     Document Type: Review

References (167)

1. Castellani RJ, Perry G. Pathogenesis and disease-modifying therapy in Alzheimer's disease: the flat line of progress. Arch Med Res. 2012;43(8):694-8. 10.1016/j.arcmed.2012.09.009..
2. Nazem A, Mansoori GA. Nanotechnology solutions for Alzheimer's disease: advances in research tools, diagnostic methods and therapeutic agents. J Alzheimers Dis. 2008;13(2):199-223.
3. Mangialasche F, Solomon A, Winblad B, Mecocci P, Kivipelto M. Alzheimer's disease: clinical trials and drug development. Lancet Neurol. 2010;9(7):702-16. 10.1016/s1474-4422(10)70119-8..
4. Sabbagh JJ, Kinney JW, Cummings JL. Animal systems in the development of treatments for Alzheimer's disease: challenges, methods, and implications. Neurobiol Aging. 2013;34(1):169-83. 10.1016/j.neurobiolaging.2012.02.027..
5. Krstic D, Madhusudan A, Doehner J, Vogel P, Notter T, Imhof C, et al. Systemic immune challenges trigger and drive Alzheimer-like neuropathology in mice. J Neuroinflammation. 2012;9:151. 10.1186/1742-2094-9-151..
6. Epis R, Gardoni F, Marcello E, Genazzani A, Canonico PL, Di Luca M. Searching for new animal models of Alzheimer's disease. Eur J Pharmacol. 2010;626(1):57-63. 10.1016/j.ejphar.2009.10.020..
7. Duyckaerts C, Potier MC, Delatour B. Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol. 2008;115(1):5-38. 10.1007/s00401-007-0312-8..
8. Chetelat G. Alzheimer disease: Abeta-independent processes-rethinking preclinical AD. Nat Rev Neurol. 2013;9(3):123-4. 10.1038/nrneurol.2013.21..
9. Zlokovic BV. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat Rev Neurosci. 2011;12(12):723-38. 10.1038/nrn3114..
10. Ankarcrona M, Mangialasche F, Winblad B. Rethinking Alzheimer's disease therapy: are mitochondria the key? J Alzheimers Dis. 2010;20 Suppl 2:S579-90. 10.3233/jad-2010-100327..
11. Oresic M, Hyotylainen T, Herukka SK, Sysi-Aho M, Mattila I, Seppanan-Laakso T, et al. Metabolome in progression to Alzheimer's disease. Translational Psychiatry. 2011;1, e57. 10.1038/tp.2011.55..
12. Kuusisto J, Koivisto K, Mykkänen L, Helkala EL, Vanhanen M, Hänninen T, et al. Association between features of the insulin resistance syndrome and Alzheimer's disease independently of apolipoprotein E4 phenotype: cross sectional population based study. BMJ. 1997;315(7115):1045-9.
13. Krstic D, Knuesel I. Deciphering the mechanism underlying late-onset Alzheimer disease. Nat Rev Neurol. 2013;9(1):25-34. 10.1038/nrneurol.2012.236..
14. Pizza V, Agresta A, D'Acunto CW, Festa M, Capasso A. Neuroinflamm-aging and neurodegenerative diseases: an overview. CNS Neurol Disord Drug Targets. 2011;10(5):621-34.
15. Franceschi C, Capri M, Monti D, Giunta S, Olivieri F, Sevini F, et al. Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev. 2007;128(1):92-105. 10.1016/j.mad.2006.11.016..
16. Frank-Cannon TC, Alto LT, McAlpine FE, Tansey MG. Does neuroinflammation fan the flame in neurodegenerative diseases? Mol Neurodegener. 2009;4:47. 10.1186/1750-1326-4-47..
17. Wyss-Coray T. Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med. 2006;12(9):1005-15. 10.1038/nm1484..
18. Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, et al. TREM2 variants in Alzheimer's disease. N Engl J Med. 2013;368(2):117-27. 10.1056/NEJMoa1211851..
19. Jonsson T, Stefansson H, Steinberg S, Jonsdottir I, Jonsson PV, Snaedal J, et al. Variant of TREM2 associated with the risk of Alzheimer's disease. N Engl J Med. 2013;368(2):107-16. 10.1056/NEJMoa1211103..
20. Naj AC, Jun G, Beecham GW, Wang LS, Vardarajan BN, Buros J, et al. Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer's disease. Nat Genet. 2011;43(5):436-41. 10.1038/ng.801..
21. Puglielli L, Tanzi RE, Kovacs DM. Alzheimer's disease: the cholesterol connection. Nat Neurosci. 2003;6(4):345-51. 10.1038/nn0403-345..
22. Eikelenboom P, van Exel E, Hoozemans JJ, Veerhuis R, Rozemuller AJ, van Gool WA. Neuroinflammation - an early event in both the history and pathogenesis of Alzheimer's disease. Neurodegener Dis. 2010;7(1-3):38-41. 10.1159/000283480..
23. Ferretti MT, Cuello AC. Does a pro-inflammatory process precede Alzheimer's disease and mild cognitive impairment? Curr Alzheimer Res. 2011;8(2):164-74.
24. Buckwalter MS, Wyss-Coray T. Modelling neuroinflammatory phenotypes in vivo. J Neuroinflammation. 2004;1(1):10. 10.1186/1742-2094-1-10..
25. Frohman EM, Racke MK, Raine CS. Multiple sclerosis - the plaque and its pathogenesis. N Engl J Med. 2006;354(9):942-55. 10.1056/NEJMra052130..
26. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, et al. Activation of innate immunity in the CNS triggers neurodegeneration through a toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A. 2003;100(14):8514-9. 10.1073/pnas.1432609100..
27. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer's disease. Neurobiol Aging. 2000;21(3):383-421.
28. Walker DG, Dalsing-Hernandez JE, Campbell NA, Lue LF. Decreased expression of CD200 and CD200 receptor in Alzheimer's disease: a potential mechanism leading to chronic inflammation. Exp Neurol. 2009;215(1):5-19. 10.1016/j.expneurol.2008.09.003..
29. Johnson VE, Stewart JE, Begbie FD, Trojanowski JQ, Smith DH, Stewart W. Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain. 2013;136(Pt 1):28-42. 10.1093/brain/aws322..
30. Xu WL, Atti AR, Gatz M, Pedersen NL, Johansson B, Fratiglioni L. Midlife overweight and obesity increase late-life dementia risk: a population-based twin study. Neurology. 2011;76(18):1568-74. 10.1212/WNL.0b013e3182190d09..
31. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007;8(1):57-69. 10.1038/nrn2038..
32. Streit WJ, Xue QS. Human CNS immune senescence and neurodegeneration. Curr Opin Immunol. 2014;29:93-6. 10.1016/j.coi.2014.05.005..
33. Streit WJ, Braak H, Xue QS, Bechmann I. Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer's disease. Acta Neuropathol. 2009;118(4):475-85. 10.1007/s00401-009-0556-6..
34. Wojtera M, Sobow T, Kloszewska I, Liberski PP, Brown DR, Sikorska B. Expression of immunohistochemical markers on microglia in Creutzfeldt-Jakob disease and Alzheimer's disease: morphometric study and review of the literature. Folia neuropathologica / Association of Polish Neuropathologists and Medical Research Centre, Polish Academy of Sciences. 2012;50(1):74-84.
35. Li W. Phagocyte dysfunction, tissue aging and degeneration. Ageing Res Rev. 2013;12(4):1005-12. 10.1016/j.arr.2013.05.006..
36. Caldeira C, Oliveira AF, Cunha C, Vaz AR, Falcao AS, Fernandes A, et al. Microglia change from a reactive to an age-like phenotype with the time in culture. Front Cell Neurosci. 2014;8:152. 10.3389/fncel.2014.00152..
37. Schwab C, Klegeris A, McGeer PL. Inflammation in transgenic mouse models of neurodegenerative disorders. Biochim Biophys Acta. 2010;1802(10):889-902. 10.1016/j.bbadis.2009.10.013..
38. Janelsins MC, Mastrangelo MA, Oddo S, LaFerla FM, Federoff HJ, Bowers WJ. Early correlation of microglial activation with enhanced tumor necrosis factor-alpha and monocyte chemoattractant protein-1 expression specifically within the entorhinal cortex of triple transgenic Alzheimer's disease mice. J Neuroinflammation. 2005;2:23. 10.1186/1742-2094-2-23..
39. Moore AH, Wu M, Shaftel SS, Graham KA, O'Banion MK. Sustained expression of interleukin-1beta in mouse hippocampus impairs spatial memory. Neuroscience. 2009;164(4):1484-95. 10.1016/j.neuroscience.2009.08.073..
40. Burton M, Johnson R. Interleukin-6 trans-signaling in the senescent mouse brain is involved in infection-related deficits in contextual fear conditioning. Brain Behav Immun. 2012;26(5):732-8. doi: 10.1016/j.bbi.2011.10.008.
41. McLarnon JG. Correlated inflammatory responses and neurodegeneration in peptide-injected animal models of Alzheimer's disease. Biomed Res Int. 2014;2014:923670. 10.1155/2014/923670..
42. Kitazawa M, Oddo S, Yamasaki TR, Green KN, LaFerla FM. Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J Neurosci. 2005;25(39):8843-53. 10.1523/JNEUROSCI.2868-05.2005..
43. Hauss-Wegrzyniak B, Dobrzanski P, Stoehr JD, Wenk GL. Chronic neuroinflammation in rats reproduces components of the neurobiology of Alzheimer's disease. Brain Res. 1998;780(2):294-303.
44. Sheng JG, Bora SH, Xu G, Borchelt DR, Price DL, Koliatsos VE. Lipopolysaccharide-induced-neuroinflammation increases intracellular accumulation of amyloid precursor protein and amyloid beta peptide in APPswe transgenic mice. Neurobiol Dis. 2003;14(1):133-45.
45. Hailman E, Lichenstein HS, Wurfel MM, Miller DS, Johnson DA, Kelley M, et al. Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14. J Exp Med. 1994;179(1):269-77.
46. Rivest S. Regulation of innate immune responses in the brain. Nat Rev Immunol. 2009;9(6):429-39. 10.1038/nri2565..
47. Mizuno T, Sawada M, Marunouchi T, Suzumura A. Production of interleukin-10 by mouse glial cells in culture. Biochem Biophys Res Commun. 1994;205(3):1907-15. 10.1006/bbrc.1994.2893..
48. Welser-Alves JV, Milner R. Microglia are the major source of TNF-α and TGF-β1 in postnatal glial cultures; regulation by cytokines, lipopolysaccharide, and vitronectin. Neurochem Int. 2013;63(1):47-53. 10.1016/j.neuint.2013.04.007..
49. Bardou I, Kaercher RM, Brothers HM, Hopp SC, Royer S, Wenk GL. Age and duration of inflammatory environment differentially affect the neuroimmune response and catecholaminergic neurons in the midbrain and brainstem. Neurobiol Aging. 2014;35(5):1065-73. 10.1016/j.neurobiolaging.2013.11.006..
50. Lee JW, Lee YK, Yuk DY, Choi DY, Ban SB, Oh KW, et al. Neuro-inflammation induced by lipopolysaccharide causes cognitive impairment through enhancement of beta-amyloid generation. J Neuroinflammation. 2008;5:37. 10.1186/1742-2094-5-37..
51. Czerniawski J, Miyashita T, Lewandowski G, Guzowski JF. Systemic lipopolysaccharide administration impairs retrieval of context-object discrimination, but not spatial, memory: evidence for selective disruption of specific hippocampus-dependent memory functions during acute neuroinflammation. Brain Behav Immun. 2015;44:159-66. 10.1016/j.bbi.2014.09.014..
52. Grudzien A, Shaw P, Weintraub S, Bigio E, Mash DC, Mesulam MM. Locus coeruleus neurofibrillary degeneration in aging, mild cognitive impairment and early Alzheimer's disease. Neurobiol Aging. 2007;28(3):327-35. 10.1016/j.neurobiolaging.2006.02.007..
53. Cerbai F, Lana D, Nosi D, Petkova-Kirova P, Zecchi S, Brothers H, et al. The neuron-astrocyte-microglia triad in normal brain ageing and in a model of neuroinflammation in the rat hippocampus. PLoS One. 2012;7(9), e45250.
54. Hauss-Wegrzyniak B, Vannucchi MG, Wenk GL. Behavioral and ultrastructural changes induced by chronic neuroinflammation in young rats. Brain Res. 2000;859(1):157-66.
55. Wenk GL, McGann K, Mencarelli A, Hauss-Wegrzyniak B, Del Soldato P, Fiorucci S. Mechanisms to prevent the toxicity of chronic neuroinflammation on forebrain cholinergic neurons. Eur J Pharmacol. 2000;402(1-2):77-85.
56. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. Microstructure of a spatial map in the entorhinal cortex. Nature. 2005;436(7052):801-6. 10.1038/nature03721..
57. Hauss-Wegrzyniak B, Lynch MA, Vraniak PD, Wenk GL. Chronic brain inflammation results in cell loss in the entorhinal cortex and impaired LTP in perforant path-granule cell synapses. Exp Neurol. 2002;176(2):336-41.
58. DiCarlo G, Wilcock D, Henderson D, Gordon M, Morgan D. Intrahippocampal LPS injections reduce Abeta load in APP + PS1 transgenic mice. Neurobiol Aging. 2001;22(6):1007-12.
59. Deng XH, Ai WM, Lei DL, Luo XG, Yan XX, Li Z. Lipopolysaccharide induces paired immunoglobulin-like receptor B (PirB) expression, synaptic alteration, and learning-memory deficit in rats. Neuroscience. 2012;209:161-70. 10.1016/j.neuroscience.2012.02.022..
60. Liu Y, Qin L, Wilson B, Wu X, Qian L, Granholm AC, et al. Endotoxin induces a delayed loss of TH-IR neurons in substantia nigra and motor behavioral deficits. Neurotoxicology. 2008;29(5):864-70. 10.1016/j.neuro.2008.02.014..
61. Perry VH, Nicoll JA, Holmes C. Microglia in neurodegenerative disease. Nat Rev Neurol. 2010;6(4):193-201. 10.1038/nrneurol.2010.17..
62. Perry VH. Contribution of systemic inflammation to chronic neurodegeneration. Acta Neuropathol. 2010;120(3):277-86. 10.1007/s00401-010-0722-x..
63. Town T, Jeng D, Alexopoulou L, Tan J, Flavell RA, Alexopoulou L, et al. Microglia recognize double-stranded RNA via TLR3 recognition of double-stranded RNA and activation of NF-kappaB by toll-like receptor 3. J Immunol. 2006;176(6):3804-12. 10.1038/35099560..
64. De Miranda J, Yaddanapudi K, Hornig M, Villar G, Serge R, Lipkin WI. Induction of toll-like receptor 3-mediated immunity during gestation inhibits cortical neurogenesis and causes behavioral disturbances. MBio. 2010;1(4). 10.1128/mBio.00176-10..
65. Kimura M, Toth LA, Agostini H, Cady AB, Majde JA, Krueger JM. Comparison of acute phase responses induced in rabbits by lipopolysaccharide and double-stranded RNA. Am J Physiol. 1994;267(6 Pt 2):R1596-605.
66. Meyer U, Nyffeler M, Engler A, Urwyler A, Schedlowski M, Knuesel I, et al. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci. 2006;26(18):4752-62. 10.1523/JNEUROSCI.0099-06.2006..
67. Bilbo SD, Smith SH, Schwarz JM. A lifespan approach to neuroinflammatory and cognitive disorders: a critical role for glia. J Neuroimmune Pharmacol. 2012;7(1):24-41. 10.1007/s11481-011-9299-y..
68. Bitanihirwe BK, Peleg-Raibstein D, Mouttet F, Feldon J, Meyer U. Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Neuropsychopharmacology. 2010;35(12):2462-78. 10.1038/npp.2010.129..
69. Hoyer S, Nitsch R. Cerebral excess release of neurotransmitter amino acids subsequent to reduced cerebral glucose metabolism in early-onset dementia of Alzheimer type. J Neural Transm (Vienna, Austria: 1996). 1989;75(3):227-32.
70. Hoyer S, Nitsch R, Oesterreich K. Predominant abnormality in cerebral glucose utilization in late-onset dementia of the Alzheimer type: a cross-sectional comparison against advanced late-onset and incipient early-onset cases. J Neural Transm Park Dis Dement Sect. 1991;3(1):1-14.
71. Craft S, Zallen G, Baker LD. Glucose and memory in mild senile dementia of the Alzheimer type. J Clin Exp Neuropsychol. 1992;14(2):253-67. 10.1080/01688639208402827..
72. Sims-Robinson C, Kim B, Rosko A, Feldman EL. How does diabetes accelerate Alzheimer disease pathology? Nat Rev Neurol. 2010;6(10):551-9. 10.1038/nrneurol.2010.130..
73. Yamamoto H, Uchigata Y, Okamoto H. Streptozotocin and alloxan induce DNA strand breaks and poly(ADP-ribose) synthetase in pancreatic islets. Nature. 1981;294(5838):284-6.
74. Mansford KR, Opie L. Comparison of metabolic abnormalities in diabetes mellitus induced by streptozotocin or by alloxan. Lancet. 1968;1(7544):670-1.
75. Like AA, Rossini AA. Streptozotocin-induced pancreatic insulitis: new model of diabetes mellitus. Science. 1976;193(4251):415-7.
76. 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(3):309-17. 10.1038/nn2055..
77. Wang JQ, Yin J, Song YF, Zhang L, Ren YX, Wang DG, et al. Brain aging and AD-like pathology in streptozotocin-induced diabetic rats. J Diabetes Res. 2014;2014:796840. 10.1155/2014/796840..
78. Lenzen S. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia. 2008;51(2):216-26. 10.1007/s00125-007-0886-7..
79. Szkudelski T. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res. 2001;50(6):537-46.
80. Takasu N, Komiya I, Asawa T, Nagasawa Y, Yamada T. Streptozocin- and alloxan-induced H2O2 generation and DNA fragmentation in pancreatic islets. H2O2 as mediator for DNA fragmentation. Diabetes. 1991;40(9):1141-5.
81. Turk J, Corbett JA, Ramanadham S, Bohrer A, McDaniel ML. Biochemical evidence for nitric oxide formation from streptozotocin in isolated pancreatic islets. Biochem Biophys Res Commun. 1993;197(3):1458-64. 10.1006/bbrc.1993.2641..
82. Murata M, Takahashi A, Saito I, Kawanishi S. Site-specific DNA methylation and apoptosis: induction by diabetogenic streptozotocin. Biochem Pharmacol. 1999;57(8):881-7.
83. Pieper AA, Brat DJ, Krug DK, Watkins CC, Gupta A, Blackshaw S, et al. Poly(ADP-ribose) polymerase-deficient mice are protected from streptozotocin-induced diabetes. Proc Natl Acad Sci U S A. 1999;96(6):3059-64.
84. Mensah-Brown EP, Obineche EN, Galadari S, Chandranath E, Shahin A, Ahmed I, et al. Streptozotocin-induced diabetic nephropathy in rats: the role of inflammatory cytokines. Cytokine. 2005;31(3):180-90. 10.1016/j.cyto.2005.04.006..
85. Chen YLZ, Blanchard J, Dai CL, Sun S, Lee MH, Grundke-Iqbal I, et al. A non-transgenic mouse model (icv-STZ Mouse) of Alzheimer's disease: similarities to and differences from the transgenic model (3xTg-AD Mouse). Mol Neurobiol. 2013;47(2):711-25.
86. Nitsch R, Hoyer S. Local action of the diabetogenic drug, streptozotocin, on glucose and energy metabolism in rat brain cortex. Neurosci Lett. 1991;128(2):199-202.
87. Plaschke K, Hoyer S. Action of the diabetogenic drug streptozotocin on glycolytic and glycogenolytic metabolism in adult rat brain cortex and hippocampus. Int J Dev Neurosci. 1993;11(4):477-83.
88. Lester-Coll N, Rivera EJ, Soscia SJ, Doiron K, Wands JR, de la Monte SM. Intracerebral streptozotocin model of type 3 diabetes: relevance to sporadic Alzheimer's disease. J Alzheimer's Disease: JAD. 2006;9(1):13-33.
89. Kraska ASM, Dorieux O, Joseph-Mathurin N, Bourrin E, Petit F, Jan C, et al. In vivo cross-sectional characterization of cerebral alterations induced by intracerebroventricular administration of streptozotocin. PLoS One. 2012;7(9), e46196. 10.1371/journal.pone.0046196..
90. Chen Y, Liang Z, Tian Z, Blanchard J, Dai CL, Chalbot S, et al. Intracerebroventricular streptozotocin exacerbates Alzheimer-like changes of 3xTg-AD mice. Mol Neurobiol. 2014;49(1):547-62. 10.1007/s12035-013-8539-y..
91. Plaschke K, Kopitz J, Siegelin M, Schliebs R, Salkovic-Petrisic M, Riederer P, et al. Insulin-resistant brain state after intracerebroventricular streptozotocin injection exacerbates Alzheimer-like changes in Tg2576 AbetaPP-overexpressing mice. J Alzheimers Dis. 2010;19(2):691-704. 10.3233/jad-2010-1270..
92. Ke YD, Delerue F, Gladbach A, Götz J, Ittner LM. Experimental diabetes mellitus exacerbates tau pathology in a transgenic mouse model of Alzheimer's disease. PLoS One. 2009;4(11), e7917. 10.1371/journal.pone.0007917..
93. Devi L, Alldred MJ, Ginsberg SD, Ohno M. Mechanisms underlying insulin deficiency-induced acceleration of β-amyloidosis in a mouse model of Alzheimer's disease. PLoS One. 2012;7(3):e32792. 10.1371/journal.pone.0032792..
94. Jolivalt CG, Hurford R, Lee CA, Dumaop W, Rockenstein E, Masliah E. Type 1 diabetes exaggerates features of Alzheimer's disease in APP transgenic mice. Exp Neurol. 2010;223(2):422-31. 10.1016/j.expneurol.2009.11.005..
95. Liu P, Zou LB, Wang LH, Jiao Q, Chi TY, Ji XF, et al. Xanthoceraside attenuates tau hyperphosphorylation and cognitive deficits in intracerebroventricular-streptozotocin injected rats. Psychopharmacology (Berl). 2013. 10.1007/s00213-013-3240-4..
96. Salkovic-Petrisic M, Osmanovic-Barilar J, Brückner M, Hoyer S, Arendt T, Riederer P. Cerebral amyloid angiopathy in streptozotocin rat model of sporadic Alzheimer's disease: a long-term follow up study. J Neural Transm. 2011;118(5):765-72.
97. Grünblatt ES-PM, Osmanovic J, Riederer P, Hoyer S. Brain insulin system dysfunction in streptozotocin intracerebroventricularly treated rats generates hyperphosphorylated tau protein. J Neurochem. 2007;101(3):757-70.
98. Tapia R, Pena F, Arias C. Neurotoxic and synaptic effects of okadaic acid, an inhibitor of protein phosphatases. Neurochem Res. 1999;24(11):1423-30.
99. Sontag JM, Sontag E. Protein phosphatase 2A dysfunction in Alzheimer's disease. Front Mol Neurosci. 2014;7:16. 10.3389/fnmol.2014.00016..
100. Cohen PT, Brewis ND, Hughes V, Mann DJ. Protein serine/threonine phosphatases; an expanding family. FEBS Lett. 1990;268(2):355-9.
101. Kamat PK, Tota S, Rai S, Shukla R, Ali S, Najmi AK, et al. Okadaic acid induced neurotoxicity leads to central cholinergic dysfunction in rats. Eur J Pharmacol. 2012;690(1-3):90-8. 10.1016/j.ejphar.2012.06.006..
102. Costa AP, Tramontina AC, Biasibetti R, Batassini C, Lopes MW, Wartchow KM, et al. Neuroglial alterations in rats submitted to the okadaic acid-induced model of dementia. Behav Brain Res. 2012;226(2):420-7. 10.1016/j.bbr.2011.09.035..
103. Kamat PK, Tota S, Saxena G, Shukla R, Nath C. Okadaic acid (ICV) induced memory impairment in rats: a suitable experimental model to test anti-dementia activity. Brain Res. 2010;1309:66-74. 10.1016/j.brainres.2009.10.064..
104. Kamat PK, Rai S, Swarnkar S, Shukla R, Nath C. Molecular and cellular mechanism of okadaic acid (OKA)-induced neurotoxicity: a novel tool for Alzheimer's disease therapeutic application. Mol Neurobiol. 2014;50(3):852-65. 10.1007/s12035-014-8699-4..
105. Arendt T, Holzer M, Fruth R, Bruckner MK, Gartner U. Phosphorylation of tau, Abeta-formation, and apoptosis after in vivo inhibition of PP-1 and PP-2A. Neurobiol Aging. 1998;19(1):3-13.
106. Lee J, Hong H, Im J, Byun H, Kim D. The formation of PHF-1 and SMI-31 positive dystrophic neurites in rat hippocampus following acute injection of okadaic acid. Neurosci Lett. 2000;282(1-2):49-52.
107. Kamat PK, Tota S, Rai S, Swarnkar S, Shukla R, Nath C. A study on neuroinflammatory marker in brain areas of okadaic acid (ICV) induced memory impaired rats. Life Sci. 2012;90(19-20):713-20. 10.1016/j.lfs.2012.03.012..
108. Rajasekar N, Dwivedi S, Tota SK, Kamat PK, Hanif K, Nath C, et al. Neuroprotective effect of curcumin on okadaic acid induced memory impairment in mice. Eur J Pharmacol. 2013;715(1-3):381-94. 10.1016/j.ejphar.2013.04.033..
109. Kamat PK, Rai S, Swarnkar S, Shukla R, Ali S, Najmi AK, et al. Okadaic acid-induced tau phosphorylation in rat brain: role of NMDA receptor. Neuroscience. 2013;238:97-113. 10.1016/j.neuroscience.2013.01.075..
110. Zimmer ER, Kalinine E, Haas CB, Torrez VR, Souza DO, Muller AP, et al. Pretreatment with memantine prevents Alzheimer-like alterations induced by intrahippocampal okadaic acid administration in rats. Curr Alzheimer Res. 2012;9(10):1182-90.
111. Kamat PK, Rai S, Swarnkar S, Shukla R, Nath C. Mechanism of synapse redox stress in okadaic acid (ICV) induced memory impairment: role of NMDA receptor. Neurochem Int. 2014;76:32-41. 10.1016/j.neuint.2014.06.012..
112. Valdiglesias V, Laffon B, Pasaro E, Cemeli E, Anderson D, Mendez J. Induction of oxidative DNA damage by the marine toxin okadaic acid depends on human cell type. Toxicon. 2011;57(6):882-8. 10.1016/j.toxicon.2011.03.005..
113. Kumar A, Seghal N, Naidu PS, Padi SS, Goyal R. Colchicines-induced neurotoxicity as an animal model of sporadic dementia of Alzheimer's type. Pharmacol Rep. 2007;59(3):274-83.
114. Nakayama T, Sawada T. Involvement of microtubule integrity in memory impairment caused by colchicine. Pharmacol Biochem Behav. 2002;71(1-2):119-38.
115. Tilson HA, Rogers BC, Grimes L, Harry GJ, Peterson NJ, Hong JS, et al. Time-dependent neurobiological effects of colchicine administered directly into the hippocampus of rats. Brain Res. 1987;408(1-2):163-72.
116. Ho L, Osaka H, Aisen PS, Pasinetti GM. Induction of cyclooxygenase (COX)-2 but not COX-1 gene expression in apoptotic cell death. J Neuroimmunol. 1998;89(1-2):142-9.
117. Sil S, Goswami AR, Dutta G, Ghosh T. Effects of naproxen on immune responses in a colchicine-induced rat model of Alzheimer's disease. Neuroimmunomodulation. 2014;21(6):304-21. 10.1159/000357735..
118. Geddes JW, Bondada V, Keller JN. Effects of intrahippocampal colchicine administration on the levels and localization of microtubule-associated proteins, tau and MAP2. Brain Res. 1994;633(1-2):1-8.
119. McMartin DN, Schedlbauer LM. Effect of experimental colchicine encephalopathy on brain protein synthesis and tubulin metabolism. J Neurobiol. 1978;9(6):453-63. 10.1002/neu.480090605..
120. Merrick SE, Demoise DC, Lee VM. Site-specific dephosphorylation of tau protein at Ser202/Thr205 in response to microtubule depolymerization in cultured human neurons involves protein phosphatase 2A. J Biol Chem. 1996;271(10):5589-94.
121. Shaftel SS, Griffin WS, O'Banion MK. The role of interleukin-1 in neuroinflammation and Alzheimer disease: an evolving perspective. J Neuroinflammation. 2008;5:7. 10.1186/1742-2094-5-7..
122. Alboni S, Cervia D, Sugama S, Conti B. Interleukin 18 in the CNS. J Neuroinflammation. 2010;7:9. 10.1186/1742-2094-7-9..
123. Griffin WS, Stanley LC, Ling C, White L, MacLeod V, Perrot LJ, et al. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc Natl Acad Sci U S A. 1989;86(19):7611-5.
124. Ojala J, Alafuzoff I, Herukka SK, van Groen T, Tanila H, Pirttilä T. Expression of interleukin-18 is increased in the brains of Alzheimer's disease patients. Neurobiol Aging. 2009;30(2):198-209. 10.1016/j.neurobiolaging.2007.06.006..
125. Malaguarnera L, Motta M, Di Rosa M, Anzaldi M, Malaguarnera M. Interleukin-18 and transforming growth factor-beta 1 plasma levels in Alzheimer's disease and vascular dementia. Neuropathology. 2006;26(4):307-12.
126. Shaftel SS, Kyrkanides S, Olschowka JA, Miller JN, Johnson RE, O'Banion MK. Sustained hippocampal IL-1 beta overexpression mediates chronic neuroinflammation and ameliorates Alzheimer plaque pathology. J Clin Invest. 2007;117(6):1595-604. 10.1172/jci31450..
127. Matousek SB, Ghosh S, Shaftel SS, Kyrkanides S, Olschowka JA, O'Banion MK. Chronic IL-1beta-mediated neuroinflammation mitigates amyloid pathology in a mouse model of Alzheimer's disease without inducing overt neurodegeneration. J Neuroimmune Pharmacol. 2012;7(1):156-64. 10.1007/s11481-011-9331-2..
128. Ghosh S, Wu MD, Shaftel SS, Kyrkanides S, Laferla FM, Olschowka JA, et al. Sustained interleukin-1beta overexpression exacerbates tau pathology despite reduced amyloid burden in an Alzheimer's mouse model. J Neurosci. 2013;11:5053-64.
129. Neumann H, Kotter MR, Franklin RJ. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain. 2009;132(Pt 2):288-95. 10.1093/brain/awn109..
130. Norden DM, Muccigrosso MM, Godbout JP., Microglial Priming and Enhanced Reactivity to Secondary Insult in Aging, and Traumatic CNS injury, and Neurodegenerative Disease., Neuropharmacology. 2014. pii: S0028-3908(14)00403-1. doi: 10.1016/j.neuropharm.2014.10.028.
131. Smith MZ, Nagy Z, Esiri MM. Cell cycle-related protein expression in vascular dementia and Alzheimer's disease. Neurosci Lett. 1999;271(1):45-8.
132. Yang Y, Geldmacher DS, Herrup K. DNA replication precedes neuronal cell death in Alzheimer's disease. J Neurosci. 2001;21(8):2661-8.
133. Smith TW, Lippa CF. Ki-67 immunoreactivity in Alzheimer's disease and other neurodegenerative disorders. J Neuropathol Exp Neurol. 1995;54(3):297-303.
134. Busser J, Geldmacher DS, Herrup K. Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J Neurosci. 1998;18(8):2801-7.
135. Morgan DO. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu Rev Cell Dev Biol. 1997;13:261-91. doi: 10.1146/annurev.cellbio.13.1.261.
136. Nikolic M, Dudek H, Kwon YT, Ramos YF, Tsai LH. The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 1996;10(7):816-25.
137. Hellmich MR, Pant HC, Wada E, Battey JF. Neuronal cdc2-like kinase: a cdc2-related protein kinase with predominantly neuronal expression. Proc Natl Acad Sci U S A. 1992;89(22):10867-71.
138. Tsai LH, Delalle I, Caviness VS, Chae T, Harlow E. p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature. 1994;371(6496):419-23. 10.1038/371419a0..
139. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature. 1999;402(6762):615-22. 10.1038/45159..
140. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature. 2000;405(6784):360-4. 10.1038/35012636..
141. Ahlijanian MK, Barrezueta NX, Williams RD, Jakowski A, Kowsz KP, McCarthy S, et al. Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc Natl Acad Sci U S A. 2000;97(6):2910-5.
142. Monaco EA. Recent evidence regarding a role for Cdk5 dysregulation in Alzheimer's disease. Curr Alzheimer Res. 2004;1(1):33-8.
143. Sundaram JR, Chan ES, Poore CP, Pareek TK, Cheong WF, Shui G, et al. Cdk5/p25-induced cytosolic PLA2-mediated lysophosphatidylcholine production regulates neuroinflammation and triggers neurodegeneration. J Neurosci. 2012;32(3):1020-34. doi: 10.523/JNEUROSCI.5177-11.2012.
144. Fischer A, Sananbenesi F, Pang PT, Lu B, Tsai LH. Opposing roles of transient and prolonged expression of p25 in synaptic plasticity and hippocampus-dependent memory. Neuron. 2005;48(5):825-38.
145. Muyllaert D, Terwel D, Kremer A, Sennvik K, Borghgraef P, Devijver H, et al. Neurodegeneration and neuroinflammation in cdk5/p25-inducible mice: a model for hippocampal sclerosis and neocortical degeneration. Am J Pathol. 2008;172(2):470-85. 10.2353/ajpath.008.070693. Epub 2008 Jan 17..
146. Houeland G, Romani A, Marchetti C, Amato G, Capsoni S, Cattaneo A, et al. Transgenic mice with chronic NGF deprivation and Alzheimer's disease-like pathology display hippocampal region-specific impairments in short- and long-term plasticities. J Neurosci. 2010;30(39):13089-94. 10.1523/jneurosci.0457-10.2010..
147. Capsoni S, Tiveron C, Vignone D, Amato G, Cattaneo A. Dissecting the involvement of tropomyosin-related kinase A and p75 neurotrophin receptor signaling in NGF deficit-induced neurodegeneration. Proc Natl Acad Sci U S A. 2010;107(27):12299-304. 10.1073/pnas.1007181107..
148. De Rosa R, Garcia AA, Braschi C, Capsoni S, Maffei L, Berardi N, et al. Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proc Natl Acad Sci U S A. 2005;102(10):3811-6. 10.1073/pnas.0500195102..
149. Capsoni S, Giannotta S, Cattaneo A. Beta-amyloid plaques in a model for sporadic Alzheimer's disease based on transgenic anti-nerve growth factor antibodies. Mol Cell Neurosci. 2002;21(1):15-28.
150. Capsoni S, Cattaneo A. On the molecular basis linking nerve growth factor (NGF) to Alzheimer's disease. Cell Mol Neurobiol. 2006;26(4-6):619-33. 10.1007/s10571-006-9112-2..
151. D'Onofrio M, Arisi I, Brandi R, Di Mambro A, Felsani A, Capsoni S, et al. Early inflammation and immune response mRNAs in the brain of AD11 anti-NGF mice. Neurobiol Aging. 2011;32(6):1007-22. 10.1016/j.neurobiolaging.2009.05.023..
152. Capsoni S, Brandi R, Arisi I, D'Onofrio M, Cattaneo A. A dual mechanism linking NGF/proNGF imbalance and early inflammation to Alzheimer's disease neurodegeneration in the AD11 anti-NGF mouse model. CNS Neurol Disord Drug Targets. 2011;10(5):635-47.
153. Capsoni S, Tiveron C, Amato G, Vignone D, Cattaneo A. Peripheral neutralization of nerve growth factor induces immunosympathectomy and central neurodegeneration in transgenic mice. J Alzheimers Dis. 2010;20(2):527-46. 10.3233/jad-2010-091357..
154. Tzanoulinou S, Brandi R, Arisi I, D'Onofrio M, Urfer SM, Sandi C, et al. Pathogen-free husbandry conditions alleviate behavioral deficits and neurodegeneration in AD10 anti-NGF mice. J Alzheimers Dis. 2014;38(4):951-64. 10.3233/jad-131037..
155. Flanders KC, Ren RF, Lippa CF. Transforming growth factor-betas in neurodegenerative disease. Prog Neurobiol. 1998;54(1):71-85.
156. Ueberham U, Ueberham E, Bruckner MK, Seeger G, Gartner U, Gruschka H, et al. Inducible neuronal expression of transgenic TGF-beta1 in vivo: dissection of short-term and long-term effects. Eur J Neurosci. 2005;22(1):50-64. 10.1111/j.1460-9568.2005.04189.x..
157. Unsicker K, Krieglstein K. TGF-betas and their roles in the regulation of neuron survival. Adv Exp Med Biol. 2002;513:353-74.
158. Grammas P, Ovase R. Cerebrovascular transforming growth factor-beta contributes to inflammation in the Alzheimer's disease brain. Am J Pathol. 2002;160(5):1583-7.
159. Wyss-Coray T, Lin C, Yan F, Yu GQ, Rohde M, McConlogue L, et al. TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat Med. 2001;7(5):612-8. 10.1038/87945..
160. Brionne TC, Tesseur I, Masliah E, Wyss-Coray T. Loss of TGF-beta 1 leads to increased neuronal cell death and microgliosis in mouse brain. Neuron. 2003;40(6):1133-45.
161. Wyss-Coray T, Mucke L. Inflammation in neurodegenerative disease - a double-edged sword. Neuron. 2002;35(3):419-32.
162. Dhull DK, Jindal A, Dhull RK, Aggarwal S, Bhateja D, Padi SS. Neuroprotective effect of cyclooxygenase inhibitors in ICV-STZ induced sporadic Alzheimer's disease in rats. J Mol Neurosci. 2012;46(1):223-35. 10.1007/s12031-011-9583-6..
163. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci U S A. 1986;83(13):4913-7.
164. Jaworski T, Dewachter I, Seymour CM, Borghgraef P, Devijver H, Kugler S, et al. Alzheimer's disease: old problem, new views from transgenic and viral models. Biochim Biophys Acta. 2010;1802(10):808-18. 10.1016/j.bbadis.2010.03.005..
165. Pintado C, Gavilan MP, Gavilan E, Garcia-Cuervo L, Gutierrez A, Vitorica J, et al. Lipopolysaccharide-induced neuroinflammation leads to the accumulation of ubiquitinated proteins and increases susceptibility to neurodegeneration induced by proteasome inhibition in rat hippocampus. J Neuroinflammation. 2012;9(1):87. 10.1186/1742-2094-9-87..
166. Heneka MT, Nadrigny F, Regen T, Martinez-Hernandez A, Dumitrescu-Ozimek L, Terwel D, et al. Locus ceruleus controls Alzheimer's disease pathology by modulating microglial functions through norepinephrine. Proc Natl Acad Sci U S A. 2010;107(13):6058-63. 10.1073/pnas.0909586107..
167. Maia LF, Kaeser SA, Reichwald J, Hruscha M, Martus P, Staufenbiel M, et al. Changes in amyloid-β and tau in the cerebrospinal fluid of transgenic mice overexpressing amyloid precursor protein. Sci Transl Med. 2013;5(194):194re2. doi: 10.1126/scitranslmed.3006446.