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Involvement of interleukin-1β in the autophagic process of microglia: relevance to Alzheimer’s disease

François, Arnaud, Terro, Faraj, Janet, Thierry, Bilan, Agnès Rioux, Paccalin, Marc, Page, Guylène·2013·Journal of Neuroinflammation

Abstract

Background: Autophagy is a major pathway of protein and organelle degradation in the lysosome. Autophagy exists at basal constitutive level and can be induced as a defense mechanism under stress conditions. Molecular relationships between autophagy and inflammation at the periphery were recently evidenced, highlighting a role of autophagy in the regulation of inflammation. Impairment of autophagy (with accumulation of autophagic vacuoles) and substantial inflammation are found in neurodegenerative diseases such as Alzheimer’s Disease (AD). However, the links between autophagy and inflammation in AD remain to be determined. Methods: Here, we examined the inflammatory reaction and autophagy in murine tri-cultures of neurons, astrocytes, and microglia. Tri-cultures were exposed to various inflammatory stresses (lipopolysaccharide (LPS), amyloid peptide (Aβ42) with or without cytokines) for 48 hours. Furthermore, the relationships between inflammation and autophagy were also analyzed in astrocyte- and microglia-enriched cultures. Data for multiple variable comparisons were analyzed by a one-way ANOVA followed by a Newman-keuls’ test. Results: Aβ42 induced a low inflammation without accumulation of acidic vesicles contrary to moderate or severe inflammation induced by LPS or the cytokine cocktail (IL-1β, TNF-α, and IL-6) or IL-1β alone which led to co-localization of p62 and LC3, two markers of autophagy, with acidic vesicles stained with Lyso-ID Red dye. Moreover, the study reveals a major role of IL-1β in the induction of autophagy in tri-cultures in the presence or absence of Aβ42. However, the vulnerability of the autophagic process in purified microglia to IL-1β was prevented by Aβ42. Conclusion: These findings show a close relationship between inflammation and autophagy, in particular a major role of IL-1β in the induction of the microglial autophagy which could be the case in AD. New therapeutic strategies could target inflammasome and autophagy in microglia to maintain its role in the amyloid immunosurveillance.

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Research works printed but not linked: 62

  1. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, Massey DC, Menzies FM, Moreau K, Narayanan U, Renna M, Siddiqi FH, Underwood BR, Winslow AR, Rubinsztein DC: Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 2010, 90:1383–1435. · DOI
  2. Choi AM, Ryter SW, Levine B: Autophagy in human health and disease. N Engl J Med 2013, 368:651–662. · DOI · Paper page
  3. Shrivastava S, Raychoudhuri A, Steele R, Ray R, Ray RB: Knockdown of autophagy enhances the innate immune response in hepatitis C virus-infected hepatocytes. Hepatology 2011, 53:406–414. · DOI
  4. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, Choi AM: Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011, 12:222–230. · DOI · Paper page
  5. Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, Tanaka K, Kawai T, Tsujimura T, Takeuchi O, Yoshimori T, Akira S: Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008, 456:264–268. · DOI
  6. Nixon RA, Yang DS: Autophagy failure in Alzheimer’s disease–locating the primary defect. Neurobiol Dis 2011, 43:38–45. · DOI · Paper page
  7. Yang Y, Coleman M, Zhang L, Zheng X, Yue Z: Autophagy in axonal and dendritic degeneration. Trends Neurosci 2013, 36:418–428. · DOI
  8. Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T: The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Investig 2008, 118:2190–2199.
  9. Salminen A, Kaarniranta K, Haapasalo A, Hiltunen M, Soininen H, Alafuzoff I: Emerging role of p62/sequestosome-1 in the pathogenesis of Alzheimer’s disease. Progress Neurobiol 2012, 96:87–95. · DOI · Paper page
  10. Moscat J, Diaz-Meco MT: p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 2009, 137:1001–1004. · DOI · Paper page
  11. Cataldo AM, Petanceska S, Terio NB, Peterhoff CM, Durham R, Mercken M, Mehta PD, Buxbaum J, Haroutunian V, Nixon RA: Abeta localization in abnormal endosomes: association with earliest Abeta elevations in AD and Down syndrome. Neurobiol Aging 2004, 25:1263–1272. · DOI · Paper page
  12. Couturier J, Paccalin M, Morel M, Terro F, Milin S, Pontcharraud R, Fauconneau B, Page G: Prevention of the beta-amyloid peptide-induced inflammatory process by inhibition of double-stranded RNA-dependent protein kinase in primary murine mixed co-cultures. J Neuroinflam 2011, 8:72. · DOI
  13. Muller JM, Ziegler-Heitbrock HW, Baeuerle PA: Nuclear factor kappa B, a mediator of lipopolysaccharide effects. Immunobiology 1993, 187:233–256. · DOI
  14. Rossol M, Heine H, Meusch U, Quandt D, Klein C, Sweet MJ, Hauschildt S: LPS-induced cytokine production in human monocytes and macrophages. Critic Rev Immunol 2011, 31:379–446. · DOI
  15. Couturier J, Page G, Morel M, Gontier C, Claude J, Pontcharraud R, Fauconneau B, Paccalin M: Inhibition of double-stranded RNA-dependent protein kinase strongly decreases cytokine production and release in peripheral blood mononuclear cells from patients with Alzheimer’s disease. J Alzheimers Dis 2010, 21:1217–1231. · DOI
  16. Lu B, Nakamura T, Inouye K, Li J, Tang Y, Lundback P, Valdes-Ferrer SI, Olofsson PS, Kalb T, Roth J, Zou Y, Erlandsson-Harris H, Yang H, Ting JP, Wang H, Andersson U, Antoine DJ, Chavan SS, Hotamisligil GS, Tracey KJ: Novel role of PKR in inflammasome activation and HMGB1 release. Nature 2012, 488:670–674. · DOI
  17. Jammi NV, Whitby LR, Beal PA: Small molecule inhibitors of the RNA-dependent protein kinase. Biochem Biophys Res Commun 2003, 308:50–57. · DOI
  18. Kang R, Zeh HJ, Lotze MT, Tang D: The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 2011, 18:571–580. · DOI · Paper page
  19. Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y: Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 1991, 266:17707–17712. · DOI
  20. Fenton TR, Gout IT: Functions and regulation of the 70kDa ribosomal S6 kinases. Int J Biochem Cell Biol 2011, 43:47–59. · DOI
  21. Chong ZZ, Shang YC, Zhang L, Wang S, Maiese K: Mammalian target of rapamycin: hitting the bull’s-eye for neurological disorders. Oxid Med Cell Longev 2010, 3:374–391. · DOI
  22. 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:S47-S53. · DOI
  23. Scharl M, Rogler G: Inflammatory bowel disease: dysfunction of autophagy? Dig Dis 2012, 30:12–19. · DOI
  24. Lin H, Hua F, Hu ZW: Autophagic flux, supported by toll-like receptor 2 activity, defends against the carcinogenesis of hepatocellular carcinoma. Autophagy 2012, 8:1859–1861. · DOI
  25. Lee HM, Shin DM, Yuk JM, Shi G, Choi DK, Lee SH, Huang SM, Kim JM, Kim CD, Lee JH, Jo EK: Autophagy negatively regulates keratinocyte inflammatory responses via scaffolding protein p62/SQSTM1. J Immunol 2011, 186:1248–1258. · DOI
  26. Wang Y, Li YB, Yin JJ, Zhu LB, Xie GY, Pan SH: Autophagy regulates inflammation following oxidative injury in diabetes. Autophagy 2013, 9:272–277. · DOI
  27. Trepanier CH, Milgram NW: Neuroinflammation in Alzheimer’s disease: are NSAIDs and selective COX-2 inhibitors the next line of therapy? J Alzheimers Dis 2010, 21:1089–1099. · DOI
  28. Xu Y, Jagannath C, Liu XD, Sharafkhaneh A, Kolodziejska KE, Eissa NT: Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 2007, 27:135–144. · DOI · Paper page
  29. Gu X, Lu Y, Chen J, He H, Li P, Yang T, Li L, Liu G, Chen Y, Zhang L: Mechanisms mediating propofol protection of pulmonary epithelial cells against lipopolysaccharide-induced cell death. Clin Exp Pharmacol Physiol 2012, 39:447–453. · DOI
  30. Into T, Inomata M, Takayama E, Takigawa T: Autophagy in regulation of Toll-like receptor signaling. Cell Signal 2012, 24:1150–1162. · DOI
  31. Bales KR, Du Y, Dodel RC, Yan GM, Hamilton-Byrd E, Paul SM: The NF-kappaB/Rel family of proteins mediates Abeta-induced neurotoxicity and glial activation. Brain Res Mol Brain Res 1998, 57:63–72. · DOI
  32. Liu MH, Lin YS, Sheu SY, Sun JS: Anti-inflammatory effects of daidzein on primary astroglial cell culture. Nutr Neurosci 2009, 12:123–134. · DOI
  33. Floden AM, Combs CK: Beta-amyloid stimulates murine postnatal and adult microglia cultures in a unique manner. J Neurosci 2006, 26:4644–4648. · DOI · Paper page
  34. Franciosi S, Choi HB, Kim SU, McLarnon JG: IL-8 enhancement of amyloid-beta (Abeta 1–42)-induced expression and production of pro-inflammatory cytokines and COX-2 in cultured human microglia. J Neuroimmunol 2005, 159:66–74. · DOI
  35. Morel M, Couturier J, Pontcharraud R, Gil R, Fauconneau B, Paccalin M, Page G: Evidence of molecular links between PKR and mTOR signalling pathways in Abeta neurotoxicity: role of p53, Redd1 and TSC2. Neurobiol Dis 2009, 36:151–161. · DOI · Paper page
  36. Zhang L, Cardinal JS, Bahar R, Evankovich J, Huang H, Nace G, Billiar TR, Rosengart MR, Pan P, Tsung A: Interferon regulatory factor-1 regulates the autophagic response in LPS-stimulated macrophages through nitric oxide. Mol Med 2012, 18:201–208. · DOI
  37. Waltz P, Carchman EH, Young AC, Rao J, Rosengart MR, Kaczorowski D, Zuckerbraun BS: Lipopolysaccaride induces autophagic signaling in macrophages via a TLR4, heme oxygenase-1 dependent pathway. Autophagy 2011, 7:315–320. · DOI
  38. Goldfinger M, Shmuel M, Benhamron S, Tirosh B: Protein synthesis in plasma cells is regulated by crosstalk between endoplasmic reticulum stress and mTOR signaling. Eur J Immunol 2011, 41:491–502. · DOI
  39. Czapski GA, Gajkowska B, Strosznajder JB: Systemic administration of lipopolysaccharide induces molecular and morphological alterations in the hippocampus. Brain Res 2010, 1356:85–94. · DOI
  40. Hagiwara S, Iwasaka H, Koga H, Hasegawa A, Kudo K, Kusaka J, Oyama Y, Noguchi T: Stimulation of autophagy in the liver by lipopolysaccharide-induced systemic inflammation in a rat model of diabetes mellitus. Biomed Res 2010, 31:263–271. · DOI
  41. Son SM, Jung ES, Shin HJ, Byun J, Mook-Jung I: Aβ-induced formation of autophagosomes is mediated by RAGE-CaMKKbeta-AMPK signaling. Neurobiol Aging 2012, 33:1006. · DOI
  42. Avrahami L, Farfara D, Shaham-Kol M, Vassar R, Frenkel D, Eldar-Finkelman H: Inhibition of glycogen synthase kinase-3 ameliorates beta-amyloid pathology and restores lysosomal acidification and mammalian target of rapamycin activity in the Alzheimer disease mouse model: in vivo and in vitro studies. J Biol Chem 2013, 288:1295–1306. · DOI
  43. Couturier J, Paccalin M, Lafay-Chebassier C, Chalon S, Ingrand I, Pinguet J, Pontcharraud R, Guillard O, Fauconneau B, Page G: Pharmacological inhibition of PKR in APPswePS1dE9 mice transiently prevents inflammation at 12 months of age but increases Abeta42 levels in the late stages of the Alzheimer’s disease. Current Alzheimer Res 2012, 9:344–360. · DOI
  44. Araki K, Ellebedy AH, Ahmed R: TOR in the immune system. Curr Opin Cell Biol 2011, 23:707–715. · DOI
  45. Dello Russo C, Lisi L, Tringali G, Navarra P: Involvement of mTOR kinase in cytokine-dependent microglial activation and cell proliferation. Biochem Pharmacol 2009, 78:1242–1251. · DOI
  46. Schaeffer V, Arbabi S, Garcia IA, Knoll ML, Cuschieri J, Bulger EM, Maier RV: Role of the mTOR pathway in LPS-activated monocytes: influence of hypertonic saline. J Surg Res 2011, 171:769–776. · DOI
  47. Li XZ, Sui CY, Chen Q, Chen XP, Zhang H, Zhou XP: Promotion of autophagy at the maturation step by IL-6 is associated with the sustained mitogen-activated protein kinase/extracellular signal-regulated kinase activity. Mol Cell Biochem 2013, 380:219–227. · DOI
  48. Shen S, Niso-Santano M, Adjemian S, Takehara T, Malik SA, Minoux H, Souquere S, Marino G, Lachkar S, Senovilla L, Galluzzi L, Kepp O, Pierron G, Maiuri MC, Hikita H, Kroemer R, Kroemer G: Cytoplasmic STAT3 represses autophagy by inhibiting PKR activity. Mol Cell 2012, 48:667–680. · DOI · Paper page
  49. Harris J: Autophagy and IL-1 Family Cytokines. Frontiers Immunol 2013, 4:83. · DOI
  50. Lussignol M, Queval C, Bernet-Camard MF, Cotte-Laffitte J, Beau I, Codogno P, Esclatine A: The herpes simplex virus 1 Us11 protein inhibits autophagy through its interaction with the protein kinase PKR. J Virol 2013, 87:859–871. · DOI
  51. Talloczy Z, Jiang W, Virgin HW, Leib DA, Scheuner D, Kaufman RJ, Eskelinen EL, Levine B: Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci USA 2002, 99:190–195. · DOI
  52. Yang C, Shogren KL, Goyal R, Bravo D, Yaszemski MJ, Maran A: RNA-dependent protein kinase is essential for 2-methoxyestradiol-induced autophagy in osteosarcoma cells. PloS One 2013, 8:e59406. · DOI
  53. Ghosh S, Wu MD, Shaftel SS, Kyrkanides S, LaFerla FM, Olschowka JA, O’Banion MK: Sustained interleukin-1beta overexpression exacerbates tau pathology despite reduced amyloid burden in an Alzheimer’s mouse model. J Neurosci 2013, 33:5053–5064. · DOI · Paper page
  54. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S: Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer’s disease. Neuron 2006, 49:489–502. · DOI · Paper page
  55. Shi CS, Shenderov K, Huang NN, Kabat J, Abu-Asab M, Fitzgerald KA, Sher A, Kehrl JH: Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol 2012, 13:255–263. · DOI · Paper page
  56. Harris J, Hartman M, Roche C, Zeng SG, O’Shea A, Sharp FA, Lambe EM, Creagh EM, Golenbock DT, Tschopp J, Kornfeld H, Fitzgerald KA, Lavelle EC: Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J Biol Chem 2011, 286:9587–9597. · DOI · Paper page
  57. Medeiros R, LaFerla FM: Astrocytes: conductors of the Alzheimer disease neuroinflammatory symphony. Exp Neurol 2013, 239:133–138. · DOI
  58. Di Malta C, Fryer JD, Settembre C, Ballabio A: Autophagy in astrocytes: a novel culprit in lysosomal storage disorders. Autophagy 2012, 8:1871–1872. · DOI
  59. Ogolla PS, Portillo JA, White CL, Patel K, Lamb B, Sen GC, Subauste CS: The protein kinase double-stranded RNA-dependent (PKR) enhances protection against disease cause by a non-viral pathogen. PLoS Pathog 2013, 9:e1003557. · DOI
  60. Wake H, Moorhouse AJ, Nabekura J: Functions of microglia in the central nervous system–beyond the immune response. Neuron Glia Biol 2011, 7:47–53. · DOI · Paper page
  61. Gao Z, Zhu Q, Zhang Y, Zhao Y, Cai L, Shields CB, Cai J: Reciprocal modulation between microglia and astrocyte in reactive gliosis following the CNS injury. Cell Mol Neurobiol 2013, 48:690–701. · DOI
  62. Barbierato M, Facci L, Argentini C, Marinelli C, Skaper SD, Giusti P: Astrocyte-microglia cooperation in the expression of a pro-inflammatory phenotype. CNS Neurol Disord Drug Targets 2013, 12:608–618. · DOI

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Metadata

Authors
François, A., Terro, F., Janet, T., Bilan, A. R., Paccalin, M., & Page, G.
Venue
Journal of Neuroinflammation
Published
2013-12
Volume
10
Issue
1
ISSN
1742-2094
Cited by
92
References
14
Language
en

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