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Immunological Investigations
A Journal of Molecular and Cellular Immunology
Volume 52, 2023 - Issue 2
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Research Article

Interleukin-17 Promotes the Infiltration of CD8+ T Cells into the Brain in a Mouse Model for Alzheimer’s Disease

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References

  • Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, et al. 2000. Inflammation and Alzheimer’s disease. Neurobiol Aging. doi:10.1016/S0197-4580(00)00124-X.
  • Alves de Lima K, Rustenhoven J, Da Mesquita S, Wall M, Salvador AF, Smirnov I, Martelossi Cebinelli G, Mamuladze T, Baker W, Papadopoulos Z, et al. 2020. Meningeal γδ T cells regulate anxiety-like behavior via IL-17a signaling in neurons. Nat Immunol. 21(11):1421–29.
  • Barrett JP, Costello DA, O’Sullivan J, Cowley TR, Lynch MA. 2015. Bone marrow-derived macrophages from aged rats are more responsive to inflammatory stimuli. J Neuroinflammation. 12(1):1–11.
  • Blalock EM, Chen KC, Stromberg AJ, Norris CM, Kadish I, Kraner SD, Porter NM, Landfield PW. 2005. Harnessing the power of gene microarrays for the study of brain aging and Alzheimer’s disease: statistical reliability and functional correlation. Ageing Res Rev. 4(4):481–512.
  • Blau CW, Cowley TR, O'Sullivan J, Grehan B, Browne TC, Kelly L, Birch A, Murphy N, Kelly AM, Kerskens CM. 2012. The age-related deficit in LTP is associated with changes in perfusion and blood-brain barrier permeability. Neurobiol Aging. 33(5):1005. e1023–1005. e1035.
  • Brigas HC, Ribeiro M, Coelho JE, Gomes R, Gomez-Murcia V, Carvalho K, Faivre E, Costa-Pereira S, Darrigues J, de Almeida AA, et al. 2021. IL-17 triggers the onset of cognitive and synaptic deficits in early stages of Alzheimer’s disease. Cell Rep. 36(9):109574.
  • Bryson KJ, Lynch MA. 2016. Linking T cells to Alzheimer’s disease: from neurodegeneration to neurorepair. Curr Opin Pharmacol. 26:2667–73.
  • Cao Y, Xu H, Zhu Y, Shi MJ, Wei L, Zhang J, Cheng S, Shi Y, Tong H, Kang L, et al. 2019. ADAMTS13 maintains cerebrovascular integrity to ameliorate Alzheimer-like pathology. PLoS Biol. 17(6):e3000313.
  • Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N, Festari C, Ferrari C, Guerra UP, Paghera B, Muscio C, et al. 2017. Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging. 49:4960–68.
  • Chen JM, Jiang GX, Li QW, Zhou ZM, Cheng Q. 2014. Increased serum levels of interleukin-18, -23 and -17 in Chinese patients with Alzheimer’s disease. Dement Geriatr Cogn Disord. 38(5–6):321–29.
  • Chen JM, Li QW, Jiang GX, Liu JS, Cheng Q. 2019b. IL-18 induced IL-23/IL-17 expression impairs Aβ clearance in cultured THP-1 and BV2 cells. Cytokine. 119:119113–18.
  • Chen J, Ye X, Pitmon E, Lu M, Wan J, Jellison ER, Adler AJ, Vella AT, Wang K. 2019a. IL-17 inhibits CXCL9/10-mediated recruitment of CD8(+) cytotoxic T cells and regulatory T cells to colorectal tumors. J Immunother Cancer. 7(1):324.
  • Civitelli L, Marcocci ME, Celestino I, Piacentini R, Garaci E, Grassi C, De Chiara G, Palamara AT. 2015. Herpes simplex virus type 1 infection in neurons leads to production and nuclear localization of APP intracellular domain (AICD): implications for Alzheimer’s disease pathogenesis. J Neurovirol. 21(5):480–90.
  • Colangelo V, Schurr J, Ball MJ, Pelaez RP, Bazan NG, Lukiw WJ. 2002. Gene expression profiling of 12633 genes in Alzheimer hippocampal CA1: transcription and neurotrophic factor down-regulation and up-regulation of apoptotic and pro-inflammatory signaling. J Neurosci Res. 70(3):462–73.
  • Cristiano C, Volpicelli F, Lippiello P, Buono B, Raucci F, Piccolo M, Iqbal AJ, Irace C, Miniaci MC, Perrone Capano C, et al. 2019. Neutralization of IL-17 rescues amyloid-beta-induced neuroinflammation and memory impairment. Br J Pharmacol. 176(18):3544–57.
  • Datta S, Novotny M, Pavicic PG Jr., Zhao C, Herjan T, Hartupee J, Hamilton T. 2010. IL-17 regulates CXCL1 mRNA stability via an AUUUA/tristetraprolin-independent sequence. J Immunol. 184(3):1484–91.
  • De Chiara G, Marcocci ME, Civitelli L, Argnani R, Piacentini R, Ripoli C, Manservigi R, Grassi C, Garaci E, Palamara AT. 2010. APP processing induced by herpes simplex virus type 1 (HSV-1) yields several APP fragments in human and rat neuronal cells. PLoS One. 5(11):e13989.
  • Derkow K, Kruger C, Dembny P, Lehnardt S. 2015. Microglia induce neurotoxic IL-17+ gammadelta T cells dependent on TLR2, TLR4, and TLR9 activation. PLoS One. 10(8):e0135898.
  • Diaz A, Limon D, Chavez R, Zenteno E, Guevara J. 2012. Abeta 25-35 injection into the temporal cortex induces chronic inflammation that contributes to neurodegeneration and spatial memory impairment in rats. J Alzheimers Dis. 30(3):505–22.
  • Duan RS, Yang X, Chen ZG, Lu MO, Morris C, Winblad B, Zhu J. 2008. Decreased fractalkine and increased IP-10 expression in aged brain of APP(swe) transgenic mice. Neurochem Res. 33(6):1085–89.
  • Eikelenboom P, Bate C, Van Gool WA, Hoozemans JJ, Rozemuller JM, Veerhuis R, Williams A. 2002. Neuroinflammation in Alzheimer’s disease and prion disease. Glia. 40(2):232–39.
  • Eikelenboom P, Hoozemans JJ, Veerhuis R, van Exel E, Rozemuller AJ, van Gool WA. 2012. Whether, when and how chronic inflammation increases the risk of developing late-onset Alzheimer’s disease. Alzheimer’s Res Ther. 4:15.
  • Ertekin-Taner N. 2007. Genetics of Alzheimer’s disease: a centennial review. Neurol Clin. 25(3):611–67.
  • Farkas IG, Czigner A, Farkas E, Dobo E, Soos K, Penke B, Endresz V, Mihaly A. 2003. Beta-amyloid peptide-induced blood-brain barrier disruption facilitates T-cell entry into the rat brain. Acta Histochem. 105(2):115–25.
  • Gate D, Saligrama N, Leventhal O, Yang AC, Unger MS, Middeldorp J, Chen K, Lehallier B, Channappa D, De Los Santos MB, et al. 2020. Clonally expanded CD8 T cells patrol the cerebrospinal fluid in Alzheimer’s disease. Nature. 577(7790):399–404.
  • Heneka MT, Golenbock DT, Latz E. 2015. Innate immunity in Alzheimer’s disease. Nat Immunol. 16(3):229–36.
  • Heppner FL, Ransohoff RM, Becher B. 2015. Immune attack: the role of inflammation in Alzheimer disease. Nat Rev Neurosci. 16(6):358–72.
  • Hickey BLH WF, Kimura H. 1991. T-lymphocyte entry into the central nervous system. J Neurosci Res. 28:254–60.
  • Hu X, Das B, Hou H, He W, Yan R. 2018. BACE1 deletion in the adult mouse reverses preformed amyloid deposition and improves cognitive functions. J Exp Med. 215(3):927–40.
  • Hultman K, Strickland S, Norris EH. 2013. The APOE varepsilon4/varepsilon4 genotype potentiates vascular fibrin(ogen) deposition in amyloid-laden vessels in the brains of Alzheimer’s disease patients. J Cereb Blood Flow Metab. 33(8):1251–58.
  • Isailovic N, Daigo K, Mantovani A, Selmi C. 2015. Interleukin-17 and innate immunity in infections and chronic inflammation. J Autoimmun. 60:1–11.
  • Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, et al. 2004. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet. 13(2):159–70.
  • Jin W, Dong C. 2013. IL-17 cytokines in immunity and inflammation. Emerg Microbes Infect. 2(9):e60.
  • Katayama H. 2020. Anti-interleukin-17A and anti-interleukin-23 antibodies may be effective against Alzheimer’s disease: role of neutrophils in the pathogenesis. Brain Behav. 10(1):e01504.
  • Kaur C, Rathnasamy G, Ling EA. 2016. The choroid plexus in healthy and diseased brain. J Neuropathol Exp Neurol. 75(3):198–213.
  • Kebir H, Kreymborg K, Ifergan I, Dodelet-Devillers A, Cayrol R, Bernard M, Giuliani F, Arbour N, Becher B, Prat A. 2007. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med. 13(10):1173–75.
  • Kolls JK, Linden A. 2004. Interleukin-17 family members and inflammation. Immunity. 21(4):467–76.
  • Krauthausen M, Kummer MP, Zimmermann J, Reyes-Irisarri E, Terwel D, Bulic B, Heneka MT, Muller M. 2015. CXCR3 promotes plaque formation and behavioral deficits in an Alzheimer’s disease model. J Clin Invest. 125(1):365–78.
  • Kumar DK, Choi SH, Washicosky KJ, Eimer WA, Tucker S, Ghofrani J, Lefkowitz A, McColl G, Goldstein LE, Tanzi RE, et al. 2016. Amyloid-β peptide protects against microbial infection in mouse and worm models of Alzheimer’s disease. Sci Transl Med. 8.
  • Laurent C, Dorothée G, Hunot S, Martin E, Monnet Y, Duchamp M, Dong Y, Légeron F-P, Leboucher A, Burnouf S. 2017. Hippocampal T cell infiltration promotes neuroinflammation and cognitive decline in a mouse model of tauopathy. Brain. 140(1):184–200.
  • Li X, Feng Y, Wu W, Zhao J, Fu C, Li Y, Ding Y, Wu B, Gong Y, Yang G, et al. 2016. Sex differences between APPswePs1de9 mice in A-beta accumulation and pancreatic islet function during the development of Alzheimer’s disease. Lab Anim. 50(4):275–85.
  • Liu Q, Xin W, He P, Turner D, Yin J, Gan Y, Shi FD, Wu J. 2014a. Interleukin-17 inhibits adult hippocampal neurogenesis. Sci Rep. 4:7554.
  • Liu Y, Yu JT, Zhang W, Zong Y, Lu RC, Zhou J, Tan L. 2014b. Interleukin-23 receptor polymorphisms are associated with Alzheimer’s disease in Han Chinese. J Neuroimmunol. 271(1–2):43–48.
  • Maheshwari P, Eslick GD. 2015. Bacterial infection and Alzheimer’s disease: a meta-analysis. J Alzheimer’s Dis. 43:957–66.
  • Masters CL, Bateman R, Blennow K, Rowe CC, Sperling RA, Cummings JL. 2015. Alzheimer’s disease. Nat Rev Dis Primers. 1:115056.
  • McQuillan K, Lynch MA, Mills KH. 2010. Activation of mixed glia by Abeta-specific Th1 and Th17 cells and its regulation by Th2 cells. Brain Behav Immun. 24(4):598–607.
  • Meraz-Rios MA, Toral-Rios D, Franco-Bocanegra D, Villeda-Hernandez J, Campos-Pena V. 2013. Inflammatory process in Alzheimer’s Disease. Front Integr Neurosci. 7:59.
  • Meraz Rios MA, Toral-Rios D, Franco-Bocanegra D, Villeda-Hernández J, Campos-Peña V. 2013. Inflammatory process in Alzheimer’s disease. Front Integr Neurosci. 7(59). doi:10.3389/fnint.2013.00059
  • Merlini M, Kirabali T, Kulic L, Nitsch RM, Ferretti MT. 2018. Extravascular CD3+ T cells in brains of Alzheimer disease patients correlate with tau but not with amyloid pathology: an immunohistochemical study. Neurodegenerative Diseases. 18(1):49–56.
  • Mietelska-Porowska A, Wojda U. 2017. T lymphocytes and inflammatory mediators in the interplay between brain and blood in Alzheimer’s disease: potential pools of new biomarkers. J Immunol Res. 2017:20174626540.
  • Mifflin MA, Winslow W, Surendra L, Tallino S, Vural A, Velazquez R. 2021. Sex differences in the IntelliCage and the Morris water maze in the APP/PS1 mouse model of amyloidosis. Neurobiol Aging. 101:101130–40.
  • Montagne A, Zhao Z, Zlokovic BV. 2017. Alzheimer’s disease: a matter of blood-brain barrier dysfunction? J Exp Med. 214(11):3151–69.
  • Moseley TA, Haudenschild DR, Rose L, Reddi AH. 2003. Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev. 14(2):155–74.
  • Muller M, Carter S, Hofer MJ, Campbell IL. 2010. Review: the chemokine receptor CXCR3 and its ligands CXCL9, CXCL10 and CXCL11 in neuroimmunity–a tale of conflict and conundrum. Neuropathol Appl Neurobiol. 36(5):368–87.
  • Nelson AR, Sweeney MD, Sagare AP, Zlokovic BV. 2016. Neurovascular dysfunction and neurodegeneration in dementia and Alzheimer’s disease. Biochim Biophys Acta. 1862(5):887–900.
  • Ní Chasaide C, Lynch MA. 2020. The role of the immune system in driving neuroinflammation. Brain and neuroscience advances 4: 2398212819901082.
  • Olsen I, Singhrao SK. 2015. Can oral infection be a risk factor for Alzheimer’s disease? J Oral Microbiol. 7:29143.
  • Onishi RM, Gaffen SL. 2010. Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology. 129(3):311–21.
  • Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang Y-H, Wang Y, Hood L, Zhu Z, Tian Q, et al. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 6:1133–41. doi:10.1038/ni1261.
  • Piacentini R, Civitelli L, Ripoli C, Marcocci ME, De Chiara G, Garaci E, Azzena GB, Palamara AT, Grassi C. 2011. HSV-1 promotes Ca2+ -mediated APP phosphorylation and Abeta accumulation in rat cortical neurons. Neurobiol Aging. 32(12):2323 e13–26.
  • Pistollato F, Sumalla Cano S, Elio I, Masias Vergara M, Giampieri F, Battino M. 2016. Role of gut microbiota and nutrients in amyloid formation and pathogenesis of Alzheimer disease. Nutr Rev. 74(10):624–34.
  • Prokop S, Miller KR, Drost N, Handrick S, Mathur V, Luo J, Wegner A, Wyss-Coray T, Heppner FL. 2015. Impact of peripheral myeloid cells on amyloid-β pathology in Alzheimer’s disease–like mice. J Exp Med. 212(11):1811–18.
  • Roberts GW, Gentleman SM, Lynch A, Murray L, Landon M, Graham DI. 1994. Beta amyloid protein deposition in the brain after severe head injury: implications for the pathogenesis of Alzheimer’s disease. J Neurol Neurosurg Psychiatry. 57:419–25.
  • Sardi F, Fassina L, Venturini L, Inguscio M, Guerriero F, Rolfo E, Ricevuti G. 2011. Alzheimer’s disease, autoimmunity and inflammation. The good, the bad and the ugly. Autoimmun Rev. 11(2):149–53.
  • Serneels L, Van Biervliet J, Craessaerts K, Dejaegere T, Horre K, Van Houtvin T, Esselmann H, Paul S, Schafer MK, Berezovska O, et al. 2009. Gamma-Secretase heterogeneity in the Aph1 subunit: relevance for Alzheimer’s disease. Science. 324(5927):639–42.
  • Seshadri S, Fitzpatrick AL, Ikram MA, DeStefano AL, Gudnason V, Boada M, Bis JC, Smith AV, Carrasquillo MM, Lambert JC, et al. 2010. Genome-wide analysis of genetic loci associated with Alzheimer disease. JAMA. 303:1832.
  • Smith DH, Nakamura M, McIntosh TK, Wang J, Rodríguez A, Chen X-H, Raghupathi R, Saatman KE, Clemens J, Schmidt ML, et al. 1998. Brain trauma induces massive hippocampal neuron death linked to a surge in β-amyloid levels in mice overexpressing mutant amyloid precursor Protein. Am J Pathol. 153(3):1005–10.
  • Sun C, Zhang J, Chen L, Liu T, Xu G, Li C, Yuan W, Xu H, Su Z. 2017. IL-17 contributed to the neuropathic pain following peripheral nerve injury by promoting astrocyte proliferation and secretion of proinflammatory cytokines. Mol Med Rep. 15(1):89–96.
  • Swardfager W, Lanctot K, Rothenburg L, Wong A, Cappell J, Herrmann N. 2010. A meta-analysis of cytokines in Alzheimer’s disease. Biol Psychiatry. 68(10):930–41.
  • Sweeney MD, Sagare AP, Zlokovic BV. 2018. Blood-brain barrier breakdown in Alzheimer disease and other neurodegenerative disorders. Nat Rev Neurol. 14(3):133–50.
  • Tan MS, Yu JT, Jiang T, Zhu XC, Guan HS, Tan L. 2014. IL12/23 p40 inhibition ameliorates Alzheimer’s disease-associated neuropathology and spatial memory in SAMP8 mice. J Alzheimers Dis. 38(3):633–46.
  • Togo T, Akiyama H, Iseki E, Kondo H, Ikeda K, Kato M, Oda T, Tsuchiya K, Kosaka K. 2002. Occurrence of T cells in the brain of Alzheimer’s disease and other neurological diseases. J Neuroimmunol. 124:83–92.
  • Tokunaga R, Zhang W, Naseem M, Puccini A, Berger MD, Soni S, McSkane M, Baba H, Lenz HJ. 2018. CXCL9, CXCL10, CXCL11/CXCR3 axis for immune activation – a target for novel cancer therapy. Cancer Treat Rev. 63:6340–47.
  • Tuppo EE, Arias HR. 2005. The role of inflammation in Alzheimer’s disease. Int J Biochem Cell Biol. 37(2):289–305.
  • van de Haar HJ, Burgmans S, Jansen JF, van Osch MJ, van Buchem MA, Muller M, Hofman PA, Verhey FR, Backes WH. 2016. Blood-brain barrier leakage in patients with early Alzheimer disease. Radiology. 281(2):527–35.
  • Van Eldik LJ, Carrillo MC, Cole PE, Feuerbach D, Greenberg BD, Hendrix JA, Kennedy M, Kozauer N, Margolin RA, Molinuevo JL, et al. 2016. The roles of inflammation and immune mechanisms in Alzheimer’s disease. Alzheimer’s Dementia (NY). 2(2):99–109.
  • Varvel NH, Grathwohl SA, Degenhardt K, Resch C, Bosch A, Jucker M, Neher JJ. 2015. Replacement of brain-resident myeloid cells does not alter cerebral amyloid-β deposition in mouse models of Alzheimer’s disease. J Exp Med. 212(11):1803–09.
  • Verite J, Janet T, Chassaing D, Fauconneau B, Rabeony H, Page G. 2018. Longitudinal chemokine profile expression in a blood-brain barrier model from Alzheimer transgenic versus wild-type mice. J Neuroinflammation. 15(1):182.
  • Victoria E, Stewart W, Smith DH. 2010. Traumatic brain injury and amyloid‑β pathology: a link to Alzheimer’s disease? Nat Rev Neurosci. 11:361–70.
  • Vom Berg J, Prokop S, Miller KR, Obst J, Kalin RE, Lopategui-Cabezas I, Wegner A, Mair F, Schipke CG, Peters O, et al. 2012. Inhibition of IL-12/IL-23 signaling reduces Alzheimer’s disease-like pathology and cognitive decline. Nat Med. 18(12):1812–19.
  • Waisman A, Hauptmann J, Regen T. 2015. The role of IL-17 in CNS diseases. Acta Neuropathol. 129(5):625–37.
  • Westermann J, Pabst R. 1996. How organ-specific is the migration of ‘naive’ and ‘memory’ T cells? Immunol Today. 17:278–82.
  • Wyss-Coray T. 2006. Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med. 12(9):1005–15.
  • Xia MQ, Bacskai BJ, Knowles RB, Qin SX, Hyman BT. 2000. Expression of the chemokine receptor CXCR3 on neurons and the elevated expression of its ligand IP-10 in reactive astrocytes: in vitro ERK1/2 activation and role in Alzheimer’s disease. J Neuroimmunol. 108:227–35.
  • Yang J, Kou J, Lalonde R, Fukuchi KI. 2017. Intracranial IL-17A overexpression decreases cerebral amyloid angiopathy by upregulation of ABCA1 in an animal model of Alzheimer’s disease. Brain Behav Immun. 65:65262–73.
  • Ye P, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, Shellito JE, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med. 194:519–28.
  • Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med. 194(4):519–28.
  • Yin Y, Wen S, Li G, Wang D. 2009. Hypoxia enhances stimulating effect of amyloid beta peptide (25-35) for interleukin 17 and T helper lymphocyte subtype 17 upregulation in cultured peripheral blood mononuclear cells. Microbiol Immunol. 53(5):281–86.
  • Zhang J, Ke KF, Liu Z, Qiu YH, Peng YP. 2013. Th17 cell-mediated neuroinflammation is involved in neurodegeneration of abeta1-42-induced Alzheimer’s disease model rats. PLoS One. 8(10):e75786.
  • Zheng C, Zhou XW, Wang JZ. 2016. The dual roles of cytokines in Alzheimer’s disease: update on interleukins, TNF-alpha, TGF-beta and IFN-gamma. Transl Neurodegener. 5:7.
  • Zimmermann J, Emrich M, Krauthausen M, Saxe S, Nitsch L, Heneka MT, Campbell IL, Muller M. 2018. IL-17A promotes granulocyte infiltration, myelin loss, microglia activation, and behavioral deficits during cuprizone-induced demyelination. Mol Neurobiol. 55(2):946–57.

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