Original article. Patterns of microglial innate immune responses elicited by amyloid β_1–42 and lipopolysaccharide: the similarities of the differences

1. Duyckaerts C, Delatour B, Potier MC. Classification and basic pathology of Alzheimer disease. Acta Neuropathol. 2009; 118:5-36.10.1007/s00401-009-0532-1Open DOISearch in Google Scholar

2. Roychaudhuri R, Yang M, Hoshi MM, Teplow DB. Amyloid β-protein assembly and Alzheimer disease. J Biol Chem. 2009; 284:4749-53.10.1074/jbc.R800036200Search in Google Scholar

3. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, et al. Diffusible, nonfibrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA. 1998; 95:6448-53.10.1073/pnas.95.11.6448Search in Google Scholar

4. Butterfield S, Hejjaoui M, Fauvet B, Awad L, Lashuel HA. Chemical strategies for controlling protein folding and elucidating the molecular mechanisms of amyloid formation and toxicity. J Mol Biol. 2012; 421:204-36.10.1016/j.jmb.2012.01.051Search in Google Scholar

5. Yankner BA, Lu T. Amyloid β-protein toxicity and the pathogenesis of Alzheimer disease. J Biol Chem. 2009; 284:4755-9.10.1074/jbc.R800018200Search in Google Scholar

6. Wang HY, Lee DH, Davis CB, Shank RP. Amyloid peptide Aβ1-42 binds selectively and with picomolar affinity to α7 nicotinic acetylcholine receptors. J Neurochem. 2000; 75:1155-61.10.1016/S0197-0186(00)00007-3Open DOISearch in Google Scholar

7. Yaar M, Zhai S, Pilch PF, Doyle SM, Eisenhauer PB, Fine RE, et al. Binding of β-amyloid to the p75 neurotrophin receptor induces apoptosis. A possible mechanism for Alzheimer’s disease. J Clin Invest. 1997; 100:2333-40.10.1172/JCI119772Open DOISearch in Google Scholar

8. El Khoury J, Hickman SE, Thomas CA, Cao L, Silverstein SC, Loike JD. Scavenger receptor-mediated adhesion of microglia to β-amyloid fibrils. Nature. 1996; 382:716-9.10.1038/382716a0Search in Google Scholar

9. Husemann J, Loike JD, Anankov R, Febbraio M, Silverstein SC. Scavenger receptors in neurobiology and neuropathology: their role on microglia and other cells of the nervous system. Glia. 2002; 40:195-205.10.1002/glia.10148Open DOISearch in Google Scholar

10. Coraci IS, Husemann J, Berman JW, Hulette C, Dufour JH, Campanella GK, et al. CD36, a class B scavenger receptor, is expressed on microglia in Alzheimer’s disease brains and can mediate production of reactive oxygen species in response to β-amyloid fibrils. Am J Pathol. 2002; 160:101-12.10.1016/S0002-9440(10)64354-4Search in Google Scholar

11. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE. A cell surface receptor complex for fibrillar β-amyloid mediates microglial activation. J Neurosci. 2003; 23:2665-74.10.1523/JNEUROSCI.23-07-02665.2003Search in Google Scholar

12. Lynch MA. The multifaceted profile of activated microglia. Mol Neurobiol. 2009; 40:139-56.10.1007/s12035-009-8077-919629762Open DOISearch in Google Scholar

13. Venkatesan C, Chrzaszcz M, Choi N, Wainwright MS. Chronic upregulation of activated microglia immunoreactive for galectin-3/Mac-2 and nerve growth factor following diffuse axonal injury. J Neuroinflammation. 2010; 7:32.10.1186/1742-2094-7-32289172020507613Search in Google Scholar

14. Nakajima K, Honda S, Tohyama Y, Imai Y, Kohsaka S, Kurihara T. Neurotrophin secretion from cultured microglia. J Neurosci Res. 2001; 65:322-31.10.1002/jnr.115711494368Open DOISearch in Google Scholar

15. Kaur C, Sivakumar V, Dheen ST, Ling EA. Insulin-like growth factor I and II expression and modulation in amoeboid microglial cells by lipopolysaccharide and retinoic acid. Neuroscience. 2006; 138:1233-44.10.1016/j.neuroscience.2005.12.02516448778Search in Google Scholar

16. Tanaka T, Ueno M, Yamashita T. Engulfment of axon debris by microglia requires p38 MAPK activity. J Biol Chem. 2009; 284:21626-36.10.1074/jbc.M109.005603275588619531468Search in Google Scholar

17. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, et al. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell. 2010; 7:483-95.10.1016/j.stem.2010.08.014400849620887954Open DOISearch in Google Scholar

18. Lee SC, Liu W, Dickson DW, Brosnan CF, Berman JW. Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1β. J Immunol. 1993;150: 2659-67.Search in Google Scholar

19. Barger SW, Goodwin ME, Porter MM, Beggs ML. Glutamate release from activated microglia requires the oxidative burst and lipid peroxidation. J Neurochem. 2007; 101:1205-13.10.1111/j.1471-4159.2007.04487.x194934717403030Open DOISearch in Google Scholar

20. Gottschall PE, Yu X, Bing B. Increased production of gelatinase B (matrix metalloproteinase-9) and interleukin-6 by activated rat microglia in culture. J Neurosci Res. 1995; 42:335-42.10.1002/jnr.4904203078583501Open DOISearch in Google Scholar

21. Qin L, Liu Y, Cooper C, Liu B, Wilson B, Hong JS. Microglia enhance β-amyloid peptide-induced toxicity in cortical and mesencephalic neurons by producing reactive oxygen species. J Neurochem. 2002; 83: 973-83.10.1046/j.1471-4159.2002.01210.x12421370Open DOISearch in Google Scholar

22. Giulian D, Haverkamp LJ, Li J, Karshin WL, Yu J, Tom D, et al. Senile plaques stimulate microglia to release a neurotoxin found in Alzheimer brain. Neurochem Int. 1995; 27:119-37.10.1016/0197-0186(95)00067-IOpen DOISearch in Google Scholar

23. Boje KM, Arora PK. Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res. 1992; 587:250-6.10.1016/0006-8993(92)91004-XSearch in Google Scholar

24. Le W, Rowe D, Xie W, Ortiz I, He Y, Appel SH. Microglial activation and dopaminergic cell injury: an in vitro model relevant to Parkinson’s disease. J Neurosci. 2001; 21:8447-55.10.1523/JNEUROSCI.21-21-08447.2001Search in Google Scholar

25. Henry CJ, Huang Y, Wynne AM, Godbout JP. Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both proinflammatory IL-1β and anti-inflammatory IL-10 cytokines. Brain Behav Immun. 2009; 23:309-17.10.1016/j.bbi.2008.09.002Search in Google Scholar

26. Kondo S, Kohsaka S, Okabe S. Long-term changes of spine dynamics and microglia after transient peripheral immune response triggered by LPS in vivo. Mol Brain. 2011; 4:27.10.1186/1756-6606-4-27Open DOISearch in Google Scholar

27. Lee MS, Kim YJ. Signaling pathways downstream of pattern-recognition receptors and their cross talk. Ann Rev Biochem. 2007; 76:447-80.10.1146/annurev.biochem.76.060605.122847Open DOISearch in Google Scholar

28. Paresce DM, Ghosh RN, Maxfield FR. Microglial cells internalize aggregates of the Alzheimer’s disease amyloid β-protein via a scavenger receptor. Neuron. 1996; 17:553-65.10.1016/S0896-6273(00)80187-7Open DOISearch in Google Scholar

29. Koenigsknecht J, Landreth G. Microglial phagocytosis of fibrillar β-amyloid through a β1 integrin-dependent mechanism. J Neurosci. 2004; 24:9838-46.10.1523/JNEUROSCI.2557-04.2004Open DOISearch in Google Scholar

30. Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci. 2007; 8:57-69.10.1038/nrn2038Open DOISearch in Google Scholar

31. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F. Immortalization of murine microglial cells by a v-raf/ v-myc carrying retrovirus. J Neuroimmunol. 1990; 27: 229-37.10.1016/0165-5728(90)90073-VOpen DOISearch in Google Scholar

32. He FQ, Qiu BY, Li TK, Xie Q, Cui de J, Huang XL, et al. Tetrandrine suppresses amyloid-β-induced inflammatory cytokines by inhibiting NF-κB pathway in murine BV2 microglial cells. Int Immunopharmacol. 2011; 11:1220-5.10.1016/j.intimp.2011.03.023Open DOISearch in Google Scholar

33. Kim YG, Ohta T, Takahashi T, Kushiro A, Nomoto K, Yokokura T, et al. Probiotic Lactobacillus casei activates innate immunity via NF-κB and p38 MAP kinase signaling pathways. Microbes Infect. 2006; 8: 994-1005.10.1016/j.micinf.2005.10.019Open DOISearch in Google Scholar

34. Hickman SE, Allison EK, El Khoury J. Microglial dysfunction and defective β-amyloid clearance pathways in aging Alzheimer’s disease mice. J Neurosci. 2008; 28:8354-60.10.1523/JNEUROSCI.0616-08.2008Open DOISearch in Google Scholar

35. Mishin V, Gray JP, Heck DE, Laskin DL, Laskin JD. Application of the Amplex red/horseradish peroxidase assay to measure hydrogen peroxide generation by recombinant microsomal enzymes. Free Radic Biol Med. 2010; 48:1485-91.10.1016/j.freeradbiomed.2010.02.030Search in Google Scholar

36. Cagnin A, Brooks DJ, Kennedy AM, Gunn RN, Myers R, Turkheimer FE, et al. In-vivo measurement of activated microglia in dementia. Lancet. 2001; 358: 461-7.10.1016/S0140-6736(01)05625-2Search in Google Scholar

37. Yasuno F, Kosaka J, Ota M, Higuchi M, Ito H, Fujimura Y, et al. Increased binding of peripheral benzodiazepine receptor in mild cognitive impairmentdementia converters measured by positron emission tomography with [11C]DAA1106. Psychiatry Res. 2012; 203:67-74.10.1016/j.pscychresns.2011.08.01322892349Search in Google Scholar

38. Jou I, Lee JH, Park SY, Yoon HJ, Joe EH, Park EJ. Gangliosides trigger inflammatory responses via TLR4 in brain glia. Am J Pathol. 2006; 168:1619-30.10.2353/ajpath.2006.050924160659516651628Search in Google Scholar

39. Reed-Geaghan EG, Savage JC, Hise AG, Landreth GE. CD14 and Toll-like receptors 2 and 4 are required for fibrillar Aβ-stimulated microglial activation. J Neurosci. 2009; 29:11982-92.10.1523/JNEUROSCI.3158-09.2009277884519776284Search in Google Scholar

40. Sankala M, Brannstrom A, Schulthess T, Bergmann U, Morgunova E, Engel J, et al. Characterization of recombinant soluble macrophage scavenger receptor MARCO. J Biol Chem. 2002; 277:33378-85.10.1074/jbc.M20449420012097327Search in Google Scholar

41. Alarcon R, Fuenzalida C, Santibanez M, von Bernhardi R. Expression of scavenger receptors in glial cells. Comparing the adhesion of astrocytes and microglia from neonatal rats to surface-bound β-amyloid. J Biol Chem. 2005; 280:30406-15.Search in Google Scholar

42. Hoebe K, Georgel P, Rutschmann S, Du X, Mudd S, Crozat K, et al. CD36 is a sensor of diacylglycerides. Nature. 2005; 433:523-7.10.1038/nature0325315690042Search in Google Scholar

43. Baranova IN, Kurlander R, Bocharov AV, Vishnyakova TG, Chen Z, Remaley AT, et al. Role of human CD36 in bacterial recognition, phagocytosis, and pathogeninduced JNK-mediated signaling. J Immunol. 2008; 181:7147-56.10.4049/jimmunol.181.10.7147Search in Google Scholar

44. Ajit D, Udan ML, Paranjape G, Nichols MR. Amyloid- β(1-42) fibrillar precursors are optimal for inducing tumor necrosis factor-α production in the THP-1 human monocytic cell line. Biochemistry. 2009; 48:9011-21.10.1021/bi9003777Open DOISearch in Google Scholar

45. Jourquin J, Tremblay E, Decanis N, Charton G, Hanessian S, Chollet AM, et al. Neuronal activitydependent increase of net matrix metalloproteinase activity is associated with MMP-9 neurotoxicity after kainate. Eur J Neurosci. 2003; 18:1507-17.10.1046/j.1460-9568.2003.02876.xOpen DOISearch in Google Scholar

46. Schonbeck U, Mach F, Libby P. Generation of biologically active IL-1β by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1β processing. J Immunol. 1998; 161:3340-6.Search in Google Scholar

47. Edison P, Archer HA, Gerhard A, Hinz R, Pavese N, Turkheimer FE, et al. Microglia, amyloid, and cognition in Alzheimer’s disease: an [11C](R)PK11195-PET and [11C]PIB-PET study. Neurobiol Dis. 2008; 32:412-9.10.1016/j.nbd.2008.08.001Search in Google Scholar

48. Okello A, Edison P, Archer HA, Turkheimer FE, Kennedy J, Bullock R, et al. Microglial activation and amyloid deposition in mild cognitive impairment: a PET study. Neurology. 2009; 72:56-62.10.1212/01.wnl.0000338622.27876.0dOpen DOISearch in Google Scholar

49. Thanopoulou K, Fragkouli A, Stylianopoulou F, Georgopoulos S. Scavenger receptor class B type I (SR-BI) regulates perivascular macrophages and modifies amyloid pathology in an Alzheimer mouse model. Proc Natl Acad Sci USA. 2010; 107:20816-21.10.1073/pnas.1005888107Search in Google Scholar

50. Husemann J, Loike JD, Kodama T, Silverstein SC. Scavenger receptor class B type I (SR-BI) mediates adhesion of neonatal murine microglia to fibrillar β-amyloid. J Neuroimmunol. 2001; 114:142-50.10.1016/S0165-5728(01)00239-9Search in Google Scholar

51. Tahara K, Kim HD, Jin JJ, Maxwell JA, Li L, Fukuchi K. Role of toll-like receptor signalling in A uptake and clearance. Brain. 2006; 129:3006-19.10.1093/brain/awl249244561316984903Search in Google Scholar

52. Qin L, Li G, Qian X, Liu Y, Wu X, Liu B, et al. Interactive role of the toll-like receptor 4 and reactive oxygen species in LPS-induced microglia activation. Glia. 2005; 52:78-84.10.1002/glia.2022515920727Search in Google Scholar