Advertisement

Inflammasomes in CNS Diseases

  • Eduardo A. Albornoz
  • Trent M. Woodruff
  • Richard Gordon
Chapter
Part of the Experientia Supplementum book series (EXS, volume 108)

Abstract

Neuroinflammation is a common pathological feature in almost all neurological diseases and is a response triggered as a consequence of the chronic activation of the innate immune response in the CNS against a variety of stimuli, including infection, traumatic brain injury, toxic metabolites, aggregated proteins, or autoimmunity. Crucial mediators of this neurinflammatory process are the intracellular protein complexes known as inflammasomes which can be triggered by pathogens as well as pathogen-associated molecular patterns (PAMPs) and damage-associated molecular patterns (DAMPs). However, chronic inflammasome activation can eventually result in cellular death and tissue damage, leading to the release of DAMPs that can reactivate the inflammasome, thereby propagating a vicious cycle of inflammation. The primary cells involved in CNS inflammasome activation are the immunocompetent microglia and the infiltrating macrophages into the CNS. However, astrocytes and neurons also express inflammasomes, and the understanding of how they are engaged in the pathogenesis of a variety of neurological diseases is crucial to develop effective therapeutic approaches for CNS pathologies that are propagated by chronic inflammasome activation. This chapter covers the activation mechanisms of relevant inflammasomes in the brain and summarizes their roles in the pathogenesis and progression of different neurological conditions.

Keywords

Neuroinflammation Neurodegeneration NLRP3 Inflammasome Microglia IL-1β ASC 

References

  1. Abulafia DP, de Rivero Vaccari JP, Lozano JD, Lotocki G, Keane RW, Dietrich WD (2009) Inhibition of the inflammasome complex reduces the inflammatory response after thromboembolic stroke in mice. J Cereb Blood Flow Metab 29:534–544PubMedCrossRefPubMedCentralGoogle Scholar
  2. Adamczak S, Dale G, de Rivero Vaccari JP, Bullock MR, Dietrich WD, Keane RW (2012) Inflammasome proteins in cerebrospinal fluid of brain-injured patients as biomarkers of functional outcome: clinical article. J Neurosurg 117:1119–1125PubMedPubMedCentralCrossRefGoogle Scholar
  3. Alboni S, Cervia D, Sugama S, Conti B (2010) Interleukin 18 in the CNS. J Neuroinflammation 7:9PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alcocer-Gomez E, de Miguel M, Casas-Barquero N, Nunez-Vasco J, Sanchez-Alcazar JA, Fernandez-Rodriguez A, Cordero MD (2014) NLRP3 inflammasome is activated in mononuclear blood cells from patients with major depressive disorder. Brain Behav Immun 36:111–117PubMedCrossRefPubMedCentralGoogle Scholar
  5. Allan SM, Tyrrell PJ, Rothwell NJ (2005) Interleukin-1 and neuronal injury. Nat Rev Immunol 5:629–640PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bamberger ME, Harris ME, Mcdonald DR, Husemann J, Landreth GE (2003) A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J Neurosci 23:2665–2674PubMedCrossRefPubMedCentralGoogle Scholar
  7. Barclay W, Shinohara ML (2017) Inflammasome activation in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Brain Pathol 27:213–219PubMedCrossRefPubMedCentralGoogle Scholar
  8. Baroja-Mazo A, Martin-Sanchez F, Gomez AI, Martinez CM, Amores-Iniesta J, Compan V, Barbera-Cremades M, Yague J, Ruiz-Ortiz E, Anton J, Bujan S, Couillin I, Brough D, Arostegui JI, Pelegrin P (2014) The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response. Nat Immunol 15:738–748PubMedCrossRefPubMedCentralGoogle Scholar
  9. Barrington J, Lemarchand E, Allan SM (2017) A brain in flame; do inflammasomes and pyroptosis influence stroke pathology? Brain Pathol 27:205–212PubMedCrossRefPubMedCentralGoogle Scholar
  10. Boxer MB, Quinn AM, Shen M, Jadhav A, Leister W, Simeonov A, Auld DS, Thomas CJ (2010) A highly potent and selective caspase 1 inhibitor that utilizes a key 3-cyanopropanoic acid moiety. ChemMedChem 5:730–738PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bruck W (2005) Clinical implications of neuropathological findings in multiple sclerosis. J Neurol 252(Suppl 3):iii10–iii14PubMedCrossRefPubMedCentralGoogle Scholar
  12. Carson MJ, Doose JM, Melchior B, Schmid CD, Ploix CC (2006) CNS immune privilege: hiding in plain sight. Immunol Rev 213:48–65PubMedPubMedCentralCrossRefGoogle Scholar
  13. Codolo G, Plotegher N, Pozzobon T, Brucale M, Tessari I, Bubacco L, de Bernard M (2013) Triggering of inflammasome by aggregated alpha-synuclein, an inflammatory response in synucleinopathies. PLoS One 8:e55375PubMedPubMedCentralCrossRefGoogle Scholar
  14. Coll RC, Robertson AA, Chae JJ, Higgins SC, Munoz-Planillo R, Inserra MC, Vetter I, Dungan LS, Monks BG, Stutz A, Croker DE, Butler MS, Haneklaus M, Sutton CE, Nunez G, Latz E, Kastner DL, Mills KH, Masters SL, Schroder K, Cooper MA, O’Neill LA (2015) A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat Med 21:248–255PubMedPubMedCentralCrossRefGoogle Scholar
  15. Compston A, Coles A (2008) Multiple sclerosis. Lancet 372:1502–1517PubMedCrossRefPubMedCentralGoogle Scholar
  16. Coureuil M, Lecuyer H, Bourdoulous S, Nassif X (2017) A journey into the brain: insight into how bacterial pathogens cross blood-brain barriers. Nat Rev Microbiol 15:149–159PubMedCrossRefPubMedCentralGoogle Scholar
  17. Cutler RG, Kelly J, Storie K, Pedersen WA, Tammara A, Hatanpaa K, Troncoso JC, Mattson MP (2004) Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer’s disease. Proc Natl Acad Sci U S A 101:2070–2075PubMedPubMedCentralCrossRefGoogle Scholar
  18. Daniels MJ, Rivers-Auty J, Schilling T, Spencer NG, Watremez W, Fasolino V, Booth SJ, White CS, Baldwin AG, Freeman S, Wong R, Latta C, Yu S, Jackson J, Fischer N, Koziel V, Pillot T, Bagnall J, Allan SM, Paszek P, Galea J, Harte MK, Eder C, Lawrence CB, Brough D (2016) Fenamate NSAIDs inhibit the NLRP3 inflammasome and protect against Alzheimer’s disease in rodent models. Nat Commun 7:12504PubMedPubMedCentralCrossRefGoogle Scholar
  19. de Rivero Vaccari JP, Lotocki G, Alonso OF, Bramlett HM, Dietrich WD, Keane RW (2009) Therapeutic neutralization of the NLRP1 inflammasome reduces the innate immune response and improves histopathology after traumatic brain injury. J Cereb Blood Flow Metab 29:1251–1261PubMedPubMedCentralCrossRefGoogle Scholar
  20. Doens D, Fernandez PL (2014) Microglia receptors and their implications in the response to amyloid beta for Alzheimer’s disease pathogenesis. J Neuroinflammation 11:48PubMedPubMedCentralCrossRefGoogle Scholar
  21. Dong Y, Benveniste EN (2001) Immune function of astrocytes. Glia 36:180–190PubMedCrossRefPubMedCentralGoogle Scholar
  22. Donnan GA, Fisher M, Macleod M, Davis SM (2008) Stroke. Lancet 371:1612–1623PubMedCrossRefPubMedCentralGoogle Scholar
  23. Fan K, Ma J, Xiao W, Chen J, Wu J, Ren J, Hou J, Hu Y, Gu J, Yu B (2017) Mangiferin attenuates blast-induced traumatic brain injury via inhibiting NLRP3 inflammasome. Chem Biol Interact 271:15–23PubMedCrossRefPubMedCentralGoogle Scholar
  24. Fann DY, Lim YA, Cheng YL, Lok KZ, Chunduri P, Baik SH, Drummond GR, Dheen ST, Sobey CG, Jo DG, Chen CL, Arumugam TV (2018) Evidence that NF-kappaB and MAPK signaling promotes NLRP inflammasome activation in neurons following ischemic stroke. Mol Neurobiol 55(2):1082–1096PubMedCrossRefPubMedCentralGoogle Scholar
  25. Farina C, Aloisi F, Meinl E (2007) Astrocytes are active players in cerebral innate immunity. Trends Immunol 28:138–145PubMedCrossRefPubMedCentralGoogle Scholar
  26. Faustin B, Lartigue L, Bruey JM, Luciano F, Sergienko E, Bailly-Maitre B, Volkmann N, Hanein D, Rouiller I, Reed JC (2007) Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell 25:713–724PubMedCrossRefGoogle Scholar
  27. Feigin VL, Lawes CM, Bennett DA, Anderson CS (2003) Stroke epidemiology: a review of population-based studies of incidence, prevalence, and case-fatality in the late 20th century. Lancet Neurol 2:43–53PubMedCrossRefPubMedCentralGoogle Scholar
  28. Feigin VL, Forouzanfar MH, Krishnamurthi R, Mensah GA, Connor M, Bennett DA, Moran AE, Sacco RL, Anderson L, Truelsen T, O’Donnell M, Venketasubramanian N, Barker-Collo S, Lawes CM, Wang W, Shinohara Y, Witt E, Ezzati M, Naghavi M, Murray C, Global Burden of Diseases I, Risk Factors S, The, G. B. D. S. E. G (2014) Global and regional burden of stroke during 1990–2010: findings from the Global Burden of Disease Study 2010. Lancet 383:245–254PubMedPubMedCentralCrossRefGoogle Scholar
  29. Franklin BS, Bossaller L, De Nardo D, Ratter JM, Stutz A, Engels G, Brenker C, Nordhoff M, Mirandola SR, Al-Amoudi A, Mangan MS, Zimmer S, Monks BG, Fricke M, Schmidt RE, Espevik T, Jones B, Jarnicki AG, Hansbro PM, Busto P, Marshak-Rothstein A, Hornemann S, Aguzzi A, Kastenmuller W, Latz E (2014) The adaptor ASC has extracellular and ‘prionoid’ activities that propagate inflammation. Nat Immunol 15:727–737PubMedPubMedCentralCrossRefGoogle Scholar
  30. Friedlander RM, Gagliardini V, Hara H, Fink KB, Li W, Macdonald G, Fishman MC, Greenberg AH, Moskowitz MA, Yuan J (1997) Expression of a dominant negative mutant of interleukin-1 beta converting enzyme in transgenic mice prevents neuronal cell death induced by trophic factor withdrawal and ischemic brain injury. J Exp Med 185:933–940PubMedPubMedCentralCrossRefGoogle Scholar
  31. Friedrich RP, Tepper K, Ronicke R, Soom M, Westermann M, Reymann K, Kaether C, Fandrich M (2010) Mechanism of amyloid plaque formation suggests an intracellular basis of Abeta pathogenicity. Proc Natl Acad Sci U S A 107:1942–1947PubMedPubMedCentralCrossRefGoogle Scholar
  32. Furman D, Chang J, Lartigue L, Bolen CR, Haddad F, Gaudilliere B, Ganio EA, Fragiadakis GK, Spitzer MH, Douchet I, Daburon S, Moreau JF, Nolan GP, Blanco P, Dechanet-Merville J, Dekker CL, Jojic V, Kuo CJ, Davis MM, Faustin B (2017) Expression of specific inflammasome gene modules stratifies older individuals into two extreme clinical and immunological states. Nat Med 23:174–184PubMedPubMedCentralCrossRefGoogle Scholar
  33. Geldhoff M, Mook-Kanamori BB, Brouwer MC, Troost D, Leemans JC, Flavell RA, van der Ende A, van der Poll T, van de Beek D (2013) Inflammasome activation mediates inflammation and outcome in humans and mice with pneumococcal meningitis. BMC Infect Dis 13:358PubMedPubMedCentralCrossRefGoogle Scholar
  34. Ghajar J (2000) Traumatic brain injury. Lancet 356:923–929PubMedCrossRefPubMedCentralGoogle Scholar
  35. Gris D, Ye Z, Iocca HA, Wen H, Craven RR, Gris P, Huang M, Schneider M, Miller SD, Ting JP (2010) NLRP3 plays a critical role in the development of experimental autoimmune encephalomyelitis by mediating Th1 and Th17 responses. J Immunol 185:974–981PubMedPubMedCentralCrossRefGoogle Scholar
  36. Guo H, Callaway JB, Ting JP (2015) Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med 21:677–687PubMedPubMedCentralCrossRefGoogle Scholar
  37. Guo C, Fulp JW, Jiang Y, Li X, Chojnacki JE, Wu J, Wang XY, Zhang S (2017) Development and characterization of a hydroxyl-sulfonamide analogue, 5-chloro-N-[2-(4-hydroxysulfamoyl-phenyl)-ethyl]-2-methoxy-benzamide, as a novel NLRP3 inflammasome inhibitor for potential treatment of multiple sclerosis. ACS Chem Neurosci 8(10):2194–2201PubMedCrossRefGoogle Scholar
  38. Gustot A, Gallea JI, Sarroukh R, Celej MS, Ruysschaert JM, Raussens V (2015) Amyloid fibrils are the molecular trigger of inflammation in Parkinson’s disease. Biochem J 471:323–333PubMedCrossRefGoogle Scholar
  39. Hanamsagar R, Torres V, Kielian T (2011) Inflammasome activation and IL-1beta/IL-18 processing are influenced by distinct pathways in microglia. J Neurochem 119:736–748PubMedPubMedCentralCrossRefGoogle Scholar
  40. Hancock DB, Martin ER, Mayhew GM, Stajich JM, Jewett R, Stacy MA, Scott BL, Vance JM, Scott WK (2008) Pesticide exposure and risk of Parkinson’s disease: a family-based case-control study. BMC Neurol 8:6PubMedPubMedCentralCrossRefGoogle Scholar
  41. Heidary M, Rakhshi N, Pahlevan Kakhki M, Behmanesh M, Sanati MH, Sanadgol N, Kamaladini H, Nikravesh A (2014) The analysis of correlation between IL-1B gene expression and genotyping in multiple sclerosis patients. J Neurol Sci 343:41–45PubMedCrossRefPubMedCentralGoogle Scholar
  42. Heneka MT (2017) Inflammasome activation and innate immunity in Alzheimer’s disease. Brain Pathol 27:220–222PubMedCrossRefPubMedCentralGoogle Scholar
  43. Heneka MT, Kummer MP, Stutz A, Delekate A, Schwartz S, Vieira-Saecker A, Griep A, Axt D, Remus A, Tzeng TC, Gelpi E, Halle A, Korte M, Latz E, Golenbock DT (2013) NLRP3 is activated in Alzheimer’s disease and contributes to pathology in APP/PS1 mice. Nature 493:674–678PubMedCrossRefGoogle Scholar
  44. Heneka MT, Kummer MP, Latz E (2014) Innate immune activation in neurodegenerative disease. Nat Rev Immunol 14:463–477PubMedCrossRefPubMedCentralGoogle Scholar
  45. Hoegen T, Tremel N, Klein M, Angele B, Wagner H, Kirschning C, Pfister HW, Fontana A, Hammerschmidt S, Koedel U (2011) The NLRP3 inflammasome contributes to brain injury in pneumococcal meningitis and is activated through ATP-dependent lysosomal cathepsin B release. J Immunol 187:5440–5451PubMedCrossRefGoogle Scholar
  46. Huang WX, Huang P, Hillert J (2004) Increased expression of caspase-1 and interleukin-18 in peripheral blood mononuclear cells in patients with multiple sclerosis. Mult Scler 10:482–487PubMedCrossRefPubMedCentralGoogle Scholar
  47. Inoue M, Shinohara ML (2013) NLRP3 inflammasome and MS/EAE. Autoimmune Dis 2013:859145PubMedPubMedCentralGoogle Scholar
  48. Johann S, Heitzer M, Kanagaratnam M, Goswami A, Rizo T, Weis J, Troost D, Beyer C (2015) NLRP3 inflammasome is expressed by astrocytes in the SOD1 mouse model of ALS and in human sporadic ALS patients. Glia 63:2260–2273PubMedCrossRefPubMedCentralGoogle Scholar
  49. Kabba JA, Xu Y, Christian H, Ruan W, Chenai K, Xiang Y, Zhang L, Saavedra JM, Pang T (2018) Microglia: housekeeper of the central nervous system. Cell Mol Neurobiol 38(1):53–71PubMedCrossRefPubMedCentralGoogle Scholar
  50. Kaushal V, Dye R, Pakavathkumar P, Foveau B, Flores J, Hyman B, Ghetti B, Koller BH, Leblanc AC (2015) Neuronal NLRP1 inflammasome activation of Caspase-1 coordinately regulates inflammatory interleukin-1-beta production and axonal degeneration-associated Caspase-6 activation. Cell Death Differ 22:1676–1686PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kaushik DK, Gupta M, Kumawat KL, Basu A (2012) NLRP3 inflammasome: key mediator of neuroinflammation in murine Japanese encephalitis. PLoS One 7:e32270PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kigerl KA, de Rivero Vaccari JP, Dietrich WD, Popovich PG, Keane RW (2014) Pattern recognition receptors and central nervous system repair. Exp Neurol 258:5–16PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kim JY, Paton JC, Briles DE, Rhee DK, Pyo S (2015) Streptococcus pneumoniae induces pyroptosis through the regulation of autophagy in murine microglia. Oncotarget 6:44161–44178PubMedPubMedCentralGoogle Scholar
  54. Klein RS, Garber C, Howard N (2017) Infectious immunity in the central nervous system and brain function. Nat Immunol 18:132–141PubMedPubMedCentralCrossRefGoogle Scholar
  55. Koyuncu OO, Hogue IB, Enquist LW (2013) Virus infections in the nervous system. Cell Host Microbe 13:379–393PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kuklina EV, Tong X, George MG, Bansil P (2012) Epidemiology and prevention of stroke: a worldwide perspective. Expert Rev Neurother 12:199–208PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kumar M, Roe K, Orillo B, Muruve DA, Nerurkar VR, Gale M Jr, Verma S (2013) Inflammasome adaptor protein apoptosis-associated speck-like protein containing CARD (ASC) is critical for the immune response and survival in west Nile virus encephalitis. J Virol 87:3655–3667PubMedPubMedCentralCrossRefGoogle Scholar
  58. Lammerding L, Slowik A, Johann S, Beyer C, Zendedel A (2016) Poststroke inflammasome expression and regulation in the peri-infarct area by gonadal steroids after transient focal ischemia in the rat brain. Neuroendocrinology 103:460–475PubMedCrossRefPubMedCentralGoogle Scholar
  59. Latz E, Xiao TS, Stutz A (2013) Activation and regulation of the inflammasomes. Nat Rev Immunol 13:397–411PubMedCrossRefPubMedCentralGoogle Scholar
  60. Lawana V, Singh N, Sarkar S, Charli A, Jin H, Anantharam V, Kanthasamy AG, Kanthasamy A (2017) Involvement of c-Abl kinase in microglial activation of NLRP3 inflammasome and impairment in autolysosomal system. J Neuroimmune Pharmacol 12(4):624–660PubMedCrossRefPubMedCentralGoogle Scholar
  61. Levin HS, Diaz-Arrastia RR (2015) Diagnosis, prognosis, and clinical management of mild traumatic brain injury. Lancet Neurol 14:506–517PubMedCrossRefPubMedCentralGoogle Scholar
  62. Liang Y, Jing X, Zeng Z, Bi W, Chen Y, Wu X, Yang L, Liu J, Xiao S, Liu S, Lin D, Tao E (2015) Rifampicin attenuates rotenone-induced inflammation via suppressing NLRP3 inflammasome activation in microglia. Brain Res 1622:43–50PubMedCrossRefPubMedCentralGoogle Scholar
  63. Lin C, Chao H, Li Z, Xu X, Liu Y, Bao Z, Hou L, Liu Y, Wang X, You Y, Liu N, Ji J (2017) Omega-3 fatty acids regulate NLRP3 inflammasome activation and prevent behavior deficits after traumatic brain injury. Exp Neurol 290:115–122PubMedCrossRefPubMedCentralGoogle Scholar
  64. Lipinska K, Malone KE, Moerland M, Kluft C (2014) Applying caspase-1 inhibitors for inflammasome assays in human whole blood. J Immunol Methods 411:66–69PubMedCrossRefPubMedCentralGoogle Scholar
  65. Liu HD, Li W, Chen ZR, Hu YC, Zhang DD, Shen W, Zhou ML, Zhu L, Hang CH (2013) Expression of the NLRP3 inflammasome in cerebral cortex after traumatic brain injury in a rat model. Neurochem Res 38:2072–2083PubMedCrossRefPubMedCentralGoogle Scholar
  66. Losy J, Niezgoda A (2001) IL-18 in patients with multiple sclerosis. Acta Neurol Scand 104:171–173PubMedCrossRefPubMedCentralGoogle Scholar
  67. Lotharius J, Brundin P (2002) Pathogenesis of Parkinson’s disease: dopamine, vesicles and alpha-synuclein. Nat Rev Neurosci 3:932–942PubMedCrossRefPubMedCentralGoogle Scholar
  68. Louveau A, Harris TH, Kipnis J (2015a) Revisiting the mechanisms of CNS immune privilege. Trends Immunol 36:569–577PubMedPubMedCentralCrossRefGoogle Scholar
  69. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J (2015b) Structural and functional features of central nervous system lymphatic vessels. Nature 523:337–341PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lu M, Sun XL, Qiao C, Liu Y, Ding JH, Hu G (2014) Uncoupling protein 2 deficiency aggravates astrocytic endoplasmic reticulum stress and nod-like receptor protein 3 inflammasome activation. Neurobiol Aging 35:421–430PubMedCrossRefPubMedCentralGoogle Scholar
  71. Luo XG, Ding JQ, Chen SD (2010) Microglia in the aging brain: relevance to neurodegeneration. Mol Neurodegener 5:12PubMedPubMedCentralCrossRefGoogle Scholar
  72. Ma J, Xiao W, Wang J, Wu J, Ren J, Hou J, Gu J, Fan K, Yu B (2016) Propofol inhibits NLRP3 inflammasome and attenuates blast-induced traumatic brain injury in rats. Inflammation 39:2094–2103PubMedCrossRefGoogle Scholar
  73. Man SM, Hopkins LJ, Nugent E, Cox S, Gluck IM, Tourlomousis P, Wright JA, Cicuta P, Monie TP, Bryant CE (2014) Inflammasome activation causes dual recruitment of NLRC4 and NLRP3 to the same macromolecular complex. Proc Natl Acad Sci U S A 111:7403–7408PubMedPubMedCentralCrossRefGoogle Scholar
  74. Mao Z, Liu C, Ji S, Yang Q, Ye H, Han H, Xue Z (2017) The NLRP3 inflammasome is involved in the pathogenesis of Parkinson’s disease in rats. Neurochem Res 42:1104–1115PubMedCrossRefPubMedCentralGoogle Scholar
  75. Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10:417–426PubMedCrossRefPubMedCentralGoogle Scholar
  76. Mhyre TR, Boyd JT, Hamill RW, Maguire-Zeiss KA (2012) Parkinson’s disease. Subcell Biochem 65:389–455PubMedPubMedCentralCrossRefGoogle Scholar
  77. Ming X, Li W, Maeda Y, Blumberg B, Raval S, Cook SD, Dowling PC (2002) Caspase-1 expression in multiple sclerosis plaques and cultured glial cells. J Neurol Sci 197:9–18PubMedCrossRefPubMedCentralGoogle Scholar
  78. Minkiewicz J, De Rivero Vaccari JP, Keane RW (2013) Human astrocytes express a novel NLRP2 inflammasome. Glia 61:1113–1121PubMedCrossRefPubMedCentralGoogle Scholar
  79. Nyul-Toth A, Kozma M, Nagyoszi P, Nagy K, Fazakas C, Hasko J, Molnar K, Farkas AE, Vegh AG, Varo G, Galajda P, Wilhelm I, Krizbai IA (2017) Expression of pattern recognition receptors and activation of the non-canonical inflammasome pathway in brain pericytes. Brain Behav Immun 64:220–231PubMedCrossRefPubMedCentralGoogle Scholar
  80. Obeso JA, Rodriguez-Oroz MC, Goetz CG, Marin C, Kordower JH, Rodriguez M, Hirsch EC, Farrer M, Schapira AH, Halliday G (2010) Missing pieces in the Parkinson’s disease puzzle. Nat Med 16:653–661PubMedCrossRefPubMedCentralGoogle Scholar
  81. Panov A, Dikalov S, Shalbuyeva N, Taylor G, Sherer T, Greenamyre JT (2005) Rotenone model of Parkinson disease: multiple brain mitochondria dysfunctions after short term systemic rotenone intoxication. J Biol Chem 280:42026–42035PubMedCrossRefPubMedCentralGoogle Scholar
  82. Rabuffetti M, Sciorati C, Tarozzo G, Clementi E, Manfredi AA, Beltramo M (2000) Inhibition of caspase-1-like activity by Ac-Tyr-Val-Ala-Asp-chloromethyl ketone induces long-lasting neuroprotection in cerebral ischemia through apoptosis reduction and decrease of proinflammatory cytokines. J Neurosci 20:4398–4404PubMedCrossRefPubMedCentralGoogle Scholar
  83. Ramos HJ, Lanteri MC, Blahnik G, Negash A, Suthar MS, Brassil MM, Sodhi K, Treuting PM, Busch MP, Norris PJ, Gale M Jr (2012) IL-1beta signaling promotes CNS-intrinsic immune control of West Nile virus infection. PLoS Pathog 8:e1003039PubMedPubMedCentralCrossRefGoogle Scholar
  84. Ross J, Brough D, Gibson RM, Loddick SA, Rothwell NJ (2007) A selective, non-peptide caspase-1 inhibitor, VRT-018858, markedly reduces brain damage induced by transient ischemia in the rat. Neuropharmacology 53:638–642PubMedCrossRefPubMedCentralGoogle Scholar
  85. Rothwell NJ, Luheshi GN (2000) Interleukin 1 in the brain: biology, pathology and therapeutic target. Trends Neurosci 23:618–625PubMedCrossRefPubMedCentralGoogle Scholar
  86. Russo FB, Jungmann P, Beltrao-Braga PCB (2017) Zika infection and the development of neurological defects. Cell Microbiol 19:e12744CrossRefGoogle Scholar
  87. Salminen A, Ojala J, Kauppinen A, Kaarniranta K, Suuronen T (2009) Inflammation in Alzheimer’s disease: amyloid-beta oligomers trigger innate immunity defence via pattern recognition receptors. Prog Neurobiol 87:181–194PubMedCrossRefPubMedCentralGoogle Scholar
  88. Saresella M, La Rosa F, Piancone F, Zoppis M, Marventano I, Calabrese E, Rainone V, Nemni R, Mancuso R, Clerici M (2016) The NLRP3 and NLRP1 inflammasomes are activated in Alzheimer’s disease. Mol Neurodegener 11:23PubMedPubMedCentralCrossRefGoogle Scholar
  89. Schapira AH, Bezard E, Brotchie J, Calon F, Collingridge GL, Ferger B, Hengerer B, Hirsch E, Jenner P, Le Novere N, Obeso JA, Schwarzschild MA, Spampinato U, Davidai G (2006) Novel pharmacological targets for the treatment of Parkinson’s disease. Nat Rev Drug Discov 5:845–854PubMedCrossRefPubMedCentralGoogle Scholar
  90. Shi M, Mody CH (2016) Fungal infection in the brain: what we learned from intravital imaging. Front Immunol 7:292PubMedPubMedCentralGoogle Scholar
  91. Singhal G, Jaehne EJ, Corrigan F, Toben C, Baune BT (2014) Inflammasomes in neuroinflammation and changes in brain function: a focused review. Front Neurosci 8:315PubMedPubMedCentralCrossRefGoogle Scholar
  92. Song L, Pei L, Yao S, Wu Y, Shang Y (2017) NLRP3 inflammasome in neurological diseases, from functions to therapies. Front Cell Neurosci 11:63PubMedPubMedCentralGoogle Scholar
  93. Spittau B (2017) Aging microglia-phenotypes, functions and implications for age-related neurodegenerative diseases. Front Aging Neurosci 9:194PubMedPubMedCentralCrossRefGoogle Scholar
  94. Tan MS, Tan L, Jiang T, Zhu XC, Wang HF, Jia CD, Yu JT (2014) Amyloid-beta induces NLRP1-dependent neuronal pyroptosis in models of Alzheimer’s disease. Cell Death Dis e1382:5Google Scholar
  95. Tang Y, Le W (2016) Differential roles of M1 and M2 microglia in neurodegenerative diseases. Mol Neurobiol 53:1181–1194PubMedCrossRefPubMedCentralGoogle Scholar
  96. Tarawneh R, Holtzman DM (2012) The clinical problem of symptomatic Alzheimer disease and mild cognitive impairment. Cold Spring Harb Perspect Med 2:a006148PubMedPubMedCentralCrossRefGoogle Scholar
  97. Thonnings S, Knudsen JD, Schonheyder HC, Sogaard M, Arpi M, Gradel KO, Ostergaard C, Danish Collaborative Bacteraemia, N (2016) Antibiotic treatment and mortality in patients with Listeria monocytogenes meningitis or bacteraemia. Clin Microbiol Infect 22:725–730PubMedCrossRefPubMedCentralGoogle Scholar
  98. Tricarico PM, Caracciolo I, Crovella S, D’Agaro P (2017) Zika virus induces inflammasome activation in the glial cell line U87-MG. Biochem Biophys Res Commun 492(4):597–602PubMedCrossRefPubMedCentralGoogle Scholar
  99. Venegas C, Kumar S, Franklin BS, Dierkes T, Brinkschulte R, Tejera D, Vieira-Saecker A, Schwartz S, Santarelli F, Kummer MP, Griep A, Gelpi E, Beilharz M, Riedel D, Golenbock DT, Geyer M, Walter J, Latz E, Heneka MT (2017) Microglia-derived ASC specks cross-seed amyloid-β in Alzheimer’s disease. Nature 552(7685):355–361.  https://doi.org/10.1038/nature25158CrossRefPubMedPubMedCentralGoogle Scholar
  100. Waisman A, Ginhoux F, Greter M, Bruttger J (2015) Homeostasis of microglia in the adult brain: review of novel microglia depletion systems. Trends Immunol 36:625–636PubMedCrossRefPubMedCentralGoogle Scholar
  101. Wallisch JS, Simon DW, Bayir H, Bell MJ, Kochanek PM, Clark RS (2017) Cerebrospinal fluid NLRP3 is increased after severe traumatic brain injury in infants and children. Neurocrit Care 27(1):44–50PubMedPubMedCentralCrossRefGoogle Scholar
  102. Walsh JG, Muruve DA, Power C (2014) Inflammasomes in the CNS. Nat Rev Neurosci 15:84–97PubMedCrossRefGoogle Scholar
  103. Wang W, Nguyen LT, Burlak C, Chegini F, Guo F, Chataway T, Ju S, Fisher OS, Miller DW, Datta D, Wu F, Wu CX, Landeru A, Wells JA, Cookson MR, Boxer MB, Thomas CJ, Gai WP, Ringe D, Petsko GA, Hoang QQ (2016) Caspase-1 causes truncation and aggregation of the Parkinson’s disease-associated protein alpha-synuclein. Proc Natl Acad Sci U S A 113:9587–9592PubMedPubMedCentralCrossRefGoogle Scholar
  104. Wee Yong V (2010) Inflammation in neurological disorders: a help or a hindrance? Neuroscientist 16:408–420PubMedCrossRefPubMedCentralGoogle Scholar
  105. Werner C, Engelhard K (2007) Pathophysiology of traumatic brain injury. Br J Anaesth 99:4–9PubMedCrossRefPubMedCentralGoogle Scholar
  106. White CS, Lawrence CB, Brough D, Rivers-Auty J (2017) Inflammasomes as therapeutic targets for Alzheimer’s disease. Brain Pathol 27:223–234PubMedCrossRefPubMedCentralGoogle Scholar
  107. Wu J, Fernandes-Alnemri T, Alnemri ES (2010) Involvement of the AIM2, NLRC4, and NLRP3 inflammasomes in caspase-1 activation by Listeria monocytogenes. J Clin Immunol 30:693–702PubMedPubMedCentralCrossRefGoogle Scholar
  108. Wyss-Coray T (2016) Ageing, neurodegeneration and brain rejuvenation. Nature 539:180–186PubMedPubMedCentralCrossRefGoogle Scholar
  109. Yan Y, Jiang W, Liu L, Wang X, Ding C, Tian Z, Zhou R (2015) Dopamine controls systemic inflammation through inhibition of NLRP3 inflammasome. Cell 160:62–73PubMedCrossRefGoogle Scholar
  110. Yang F, Wang Z, Wei X, Han H, Meng X, Zhang Y, Shi W, Li F, Xin T, Pang Q, Yi F (2014) NLRP3 deficiency ameliorates neurovascular damage in experimental ischemic stroke. J Cereb Blood Flow Metab 34:660–667PubMedPubMedCentralCrossRefGoogle Scholar
  111. Ye X, Shen T, Hu J, Zhang L, Zhang Y, Bao L, Cui C, Jin G, Zan K, Zhang Z, Yang X, Shi H, Zu J, Yu M, Song C, Wang Y, Qi S, Cui G (2017) Purinergic 2X7 receptor/NLRP3 pathway triggers neuronal apoptosis after ischemic stroke in the mouse. Exp Neurol 292:46–55PubMedCrossRefPubMedCentralGoogle Scholar
  112. Yiannopoulou KG, Papageorgiou SG (2013) Current and future treatments for Alzheimer’s disease. Ther Adv Neurol Disord 6:19–33PubMedPubMedCentralCrossRefGoogle Scholar
  113. Youm YH, Nguyen KY, Grant RW, Goldberg EL, Bodogai M, Kim D, D’Agostino D, Planavsky N, Lupfer C, Kanneganti TD, Kang S, Horvath TL, Fahmy TM, Crawford PA, Biragyn A, Alnemri E, Dixit VD (2015) The ketone metabolite beta-hydroxybutyrate blocks NLRP3 inflammasome-mediated inflammatory disease. Nat Med 21:263–269PubMedPubMedCentralCrossRefGoogle Scholar
  114. Zhang P, Shao XY, Qi GJ, Chen Q, Bu LL, Chen LJ, Shi J, Ming J, Tian B (2016) Cdk5-dependent activation of neuronal inflammasomes in Parkinson’s disease. Mov Disord 31:366–376PubMedCrossRefPubMedCentralGoogle Scholar
  115. Zhou Y, Lu M, Du RH, Qiao C, Jiang CY, Zhang KZ, Ding JH, Hu G (2016) MicroRNA-7 targets Nod-like receptor protein 3 inflammasome to modulate neuroinflammation in the pathogenesis of Parkinson’s disease. Mol Neurodegener 11:28PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Eduardo A. Albornoz
    • 1
  • Trent M. Woodruff
    • 1
  • Richard Gordon
    • 1
    • 2
  1. 1.School of Biomedical Sciences, Faculty of MedicineUniversity of QueenslandBrisbaneAustralia
  2. 2.UQ Centre for Clinical Research, Faculty of MedicineUniversity of QueenslandBrisbaneAustralia

Personalised recommendations