Experimental peri-implantitis induces neuroinflammation: An exploratory study in rats.
Animals
Rats
Male
Tumor Necrosis Factor-alpha
/ metabolism
Peri-Implantitis
/ pathology
Interleukin-6
/ analysis
Neuroinflammatory Diseases
/ pathology
Microglia
/ pathology
Lipopolysaccharides
Glial Fibrillary Acidic Protein
/ metabolism
Calcium-Binding Proteins
/ analysis
Disease Models, Animal
Brain
/ pathology
Astrocytes
/ pathology
Amyloid beta-Peptides
/ metabolism
Rats, Sprague-Dawley
Microfilament Proteins
Alzheimer’s disease
Animal model
Neurodegeneration
Neurodegenerative disease
Neuroinflammation
Peri-implantitis
Rat
Journal
BMC oral health
ISSN: 1472-6831
Titre abrégé: BMC Oral Health
Pays: England
ID NLM: 101088684
Informations de publication
Date de publication:
18 Oct 2024
18 Oct 2024
Historique:
received:
05
06
2024
accepted:
01
10
2024
medline:
19
10
2024
pubmed:
19
10
2024
entrez:
18
10
2024
Statut:
epublish
Résumé
Cumulating evidence supports the close association between periodontal diseases, neuroinflammation and neurodegenerative pathologies, except for peri-implantitis (PI). Thus, this study explored the association between experimental PI and neuropathological changes in the rat brain. After bilateral first molars extraction, experimental PI was induced at titanium implants placed in the maxillae by lipopolysaccharide injections and ligature placement. Following 28-weeks of disease progression, the maxillae and brains were retrieved from 6 rats. Healthy brains from 3 rats were used as control. Brains were analyzed by immunohistochemistry to detect signs of neuroinflammation (interleukin (IL)-6 and tumor necrosis factor (TNF)-α)), microglial activation (IBA-1) and astrogliosis (GFAP). To explore signs of neurodegeneration, hematoxylin/eosin and Nissl stainings were used. Also, four different antibodies against amyloid beta (Aβ 1-42) were tested. Chronic PI lesions showed peri-implant bone resorption accompanied by large inflammatory infiltrates. IL-6 Chronic experimental PI lesions led to an increased detection of IL-6 and TNF-α, GFAP
Identifiants
pubmed: 39425138
doi: 10.1186/s12903-024-04995-z
pii: 10.1186/s12903-024-04995-z
doi:
Substances chimiques
Tumor Necrosis Factor-alpha
0
Interleukin-6
0
Lipopolysaccharides
0
Glial Fibrillary Acidic Protein
0
Calcium-Binding Proteins
0
Aif1 protein, rat
0
Amyloid beta-Peptides
0
Microfilament Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1238Informations de copyright
© 2024. The Author(s).
Références
Derks J, Tomasi C. Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol. 2015;42(Suppl 16):S158–171. https://doi.org/10.1111/jcpe.12334 .
doi: 10.1111/jcpe.12334
pubmed: 25495683
Nie J, Zhang Q, Zheng H, Xu LX, Wang XY, Chen F. Pyrosequencing of the subgingival microbiome in peri-implantitis after non-surgical mechanical debridement therapy. J Periodont Res. 2020;55:238–46. https://doi.org/10.1111/jre.12708 .
doi: 10.1111/jre.12708
Alves CH, Russi KL, Rocha NC, Bastos F, Darrieux M, Parisotto TM, et al. Host-microbiome interactions regarding peri-implantitis and dental implant loss. J Transl Med. 2022;20:425. https://doi.org/10.1186/s12967-022-03636-9 .
doi: 10.1186/s12967-022-03636-9
pubmed: 36138430
pmcid: 9502891
Schwarz F, Derks J, Monje A, Wang HL. Peri-implantitis. J Clin Periodontol. 2018;45(Suppl 20):S246–66. https://doi.org/10.1111/jcpe.12954 .
doi: 10.1111/jcpe.12954
pubmed: 29926484
Eke PI, Dye BA, Wei L, Thornton-Evans GO, Genco RJ, CDC Periodontal Disease Surveillance workgroup. Prevalence of periodontitis in adults in the United States: 2009 and 2010. J Dent Res. 2012;91:914–20. https://doi.org/10.1177/0022034512457373 .
doi: 10.1177/0022034512457373
pubmed: 22935673
Carcuac O, Berglundh T. Composition of human peri-implantitis and periodontitis lesions. J Dent Res. 2014;93:1083–8. https://doi.org/10.1177/0022034514551754 .
doi: 10.1177/0022034514551754
pubmed: 25261052
pmcid: 4293768
Berglundh T, Gislason O, Lekholm U, Sennerby L, Lindhe J. Histopathological observations of human periimplantitis lesions. J Clin Periodontol. 2004;31:341–7. https://doi.org/10.1111/j.1600-051X.2004.00486.x .
doi: 10.1111/j.1600-051X.2004.00486.x
pubmed: 15086615
Huang H, Chen D, Lippuner K, Hunziker EB. Induced experimental peri-implantitis and periodontitis: what are the differences in the inflammatory response? J Oral Implantol. 2021;4:359–69. https://doi.org/10.1563/aaid-joi-D-19-00362 .
doi: 10.1563/aaid-joi-D-19-00362
Zhang H, Yuan Y, Xue H, Yu R, Huang H. MicroRNA sequence and function analysis in peri-implantitis and periodontitis: an animal study. J Periodontal Res. 2022;57:1043–55. https://doi.org/10.1111/jre.13045 .
doi: 10.1111/jre.13045
pubmed: 35944133
Hiyari S, Wong RL, Yaghsezian A, Naghibi A, Tetradis S, Camargo PM, et al. Ligature-induced peri-implantitis and periodontitis in mice. J Periodontol. 2018;45:89–99. https://doi.org/10.1111/jcpe.12817 .
doi: 10.1111/jcpe.12817
Sahrmann P, Gilli F, Wiedemeier DB, Attin T, Schmidlin PR, Karygianni L. The microbiome of peri-implantitis: a systematic review and meta-analysis. Microorganisms. 2020;8:661. https://doi.org/10.3390/microorganisms8050661 .
doi: 10.3390/microorganisms8050661
pubmed: 32369987
pmcid: 7284896
Rakic M, Grusovin MG, Canullo L. The microbiologic profile associated with peri-implantitis in humans: a systematic review. Int J Oral Maxillofac Implants. 2016;31:359–68. https://doi.org/10.11607/jomi.4150 .
doi: 10.11607/jomi.4150
pubmed: 26478978
Lafaurie GI, Sabogal MA, Castillo DM, Rincón MV, Gómez LA, Lesmes YA, et al. Microbiome and microbial biofilm profiles of peri-implantitis: a systematic review. J Periodontol. 2017;88:1066–89. https://doi.org/10.1902/jop.2017.170123 .
doi: 10.1902/jop.2017.170123
pubmed: 28625077
Vohra F, Alkhudhairy F, Al-Kheraif AA, Akram Z, Javed F. Peri-implant parameters and C-reactive protein levels among patients with different obesity levels. Clin Implant Dent Relat Res. 2018;20:130–6. https://doi.org/10.1111/cid.12556 .
doi: 10.1111/cid.12556
pubmed: 29148260
Taylor BA, Tofler GH, Carey HM, Morel-Kopp MC, Philcox S, Carter TR, et al. Full-mouth tooth extraction lowers systemic inflammatory and thrombotic markers of cardiovascular risk. J Dent Res. 2006;85:74–8. https://doi.org/10.1177/154405910608500113 .
doi: 10.1177/154405910608500113
pubmed: 16373685
Wang IC, Sugai JV, Majzoub J, Johnston J, Giannobile WV, Wang HL. Pro-inflammatory profiles in cardiovascular disease patients with peri-implantitis. J Periodontol. 2022;93:824–36. https://doi.org/10.1002/JPER.21-0419 .
doi: 10.1002/JPER.21-0419
pubmed: 34807456
Radaelli K, Alberti A, Corbella S, Francetti L. The impact of peri-implantitis on systemic diseases and conditions: a review of the literature. Int J Dent. 2021;2021:5536566. https://doi.org/10.1155/2021/5536566 .
doi: 10.1155/2021/5536566
pubmed: 34054959
pmcid: 8143885
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(Suppl 1):S47–53. https://doi.org/10.1097/00002093-200000001-0000 .
doi: 10.1097/00002093-200000001-0000
pubmed: 10850730
Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole G, et al. Inflammation and Alzheimer’s disease. Neurobiol Aging. 2000;21:383–421. https://doi.org/10.1016/s0197-4580(00)00124-x .
doi: 10.1016/s0197-4580(00)00124-x
pubmed: 10858586
pmcid: 3887148
Tessarin GWL, Santos RM, dos Pereira RF, Mattera MS, de de LC, Tsosura TVS. Periapical Disease and the Prefrontal Cortex. Is there a relationship between calcium-binding protein and neurodegenerative diseases? Arch Health Invest. 2021;11:141–52. https://doi.org/10.21270/archi.v11i1.5350 .
doi: 10.21270/archi.v11i1.5350
Alvarenga MOP, Frazão DR, de Matos IG, Bittencourt LO, Fagundes NCF, Rösing CK, et al. Is there any association between neurodegenerative diseases and periodontitis? A systematic review. Front Aging Neurosci. 2021;13:651437. https://doi.org/10.3389/fnagi.2021.651437 .
doi: 10.3389/fnagi.2021.651437
pubmed: 34108875
pmcid: 8180549
Gil-Montoya JA, Sanchez-Lara I, Carnero-Pardo C, Fornieles F, Montes J, Vilchez R, et al. Is periodontitis a risk factor for cognitive impairment and dementia? A case-control study. J Periodontol. 2015;86:244–53. https://doi.org/10.1902/jop.2014.140340 .
doi: 10.1902/jop.2014.140340
pubmed: 25345338
Poole S, Singhrao SK, Kesavalu L, Curtis MA, Crean S. Determining the presence of periodontopathic virulence factors in short-term postmortem Alzheimer’s disease brain tissue. J Alzheimers Dis. 2013;36:665–77. https://doi.org/10.3233/JAD-121918 .
doi: 10.3233/JAD-121918
pubmed: 23666172
Adams B, Nunes JM, Page MJ, Roberts T, Carr J, Nell TA, et al. Parkinson’s Disease: a systemic inflammatory disease accompanied by bacterial inflammagens. Front Aging Neurosci. 2019;11:210. https://doi.org/10.3389/fnagi.2019.00210 .
doi: 10.3389/fnagi.2019.00210
pubmed: 31507404
pmcid: 6718721
Ilievski V, Zuchowska PK, Green SJ, Toth PT, Ragozzino ME, Le K, Aljewari HW, et al. Chronic oral application of a periodontal pathogen results in brain inflammation, neurodegeneration and amyloid beta production in wild type mice. PLoS ONE. 2018;13:e0204941. https://doi.org/10.1371/journal.pone.0204941 .
doi: 10.1371/journal.pone.0204941
pubmed: 30281647
pmcid: 6169940
Sansores-España LD, Melgar-Rodríguez S, Olivares-Sagredo K, Cafferata EA, Martínez-Aguilar VM, Vernal R, et al. Oral-gut-brain Axis in experimental models of periodontitis: associating gut dysbiosis with neurodegenerative diseases. Front Aging. 2021;2:781582. https://doi.org/10.3389/fragi.2021.781582 .
doi: 10.3389/fragi.2021.781582
pubmed: 35822001
pmcid: 9261337
Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev. 2005;57:173–85. https://doi.org/10.1124/pr.57.2.4 .
doi: 10.1124/pr.57.2.4
pubmed: 15914466
Perry VH. The influence of systemic inflammation on inflammation in the brain: implications for chronic neurodegenerative disease. Brain Behav Immun. 2004;18:407–13. https://doi.org/10.1016/j.bbi.2004.01.004 .
doi: 10.1016/j.bbi.2004.01.004
pubmed: 15265532
Frost GR, Li YM. The role of astrocytes in amyloid production and Alzheimer’s Disease. Open Biol. 2017;7:170228. https://doi.org/10.1098/rsob.170228 .
doi: 10.1098/rsob.170228
pubmed: 29237809
pmcid: 5746550
Block ML, Hong JS. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol. 2005;76:77–98. https://doi.org/10.1016/j.pneurobio.2005.06.004 .
doi: 10.1016/j.pneurobio.2005.06.004
pubmed: 16081203
Riviere GR, Riviere KH, Smith KS. Molecular and immunological evidence of oral treponema in the human brain and their association with Alzheimer’s Disease. Oral Microbiol Immunol. 2002;17:113–8. https://doi.org/10.1046/j.0902-0055.2001.00100.x .
doi: 10.1046/j.0902-0055.2001.00100.x
pubmed: 11929559
Parra-Torres V, Melgar-Rodríguez S, Muñoz-Manríquez C, Sanhueza B, Cafferata EA, Paula-Lima AC, et al. Periodontal bacteria in the brain-implication for Alzheimer’s disease: a systematic review. Oral Dis. 2023;29:21–8. https://doi.org/10.1111/odi.14054 .
doi: 10.1111/odi.14054
pubmed: 34698406
Nakajima M, Arimatsu K, Kato T, Matsuda Y, Minagawa T, Takahashi N, et al. Oral administration of P. Gingivalis induces dysbiosis of gut microbiota and impaired barrier function leading to dissemination of Enterobacteria to the liver. PLoS ONE. 2015;10:e0134234. https://doi.org/10.1371/journal.pone.0134234 .
doi: 10.1371/journal.pone.0134234
pubmed: 26218067
pmcid: 4517782
Arimatsu K, Yamada H, Miyazawa H, Minagawa T, Nakajima M, Ryder MI, et al. Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota. Sci Rep. 2014;4:4828. https://doi.org/10.1038/srep04828 .
doi: 10.1038/srep04828
pubmed: 24797416
pmcid: 4010932
Ramanauskaite A, Krüger N, Obreja K, Borchert F, Dahmer I, Schwarz F. Influence of antiresorptive/antiangiogenic therapy on the surgical treatment outcomes of experimentally induced peri-implantitis lesions. Clin Oral Investig. 2023;27(11):6657–6666. https://doi.org/10.1007/s00784-023-05275-w .
Ozawa R, Saita M, Sakaue S, Okada R, Sato T, Kawamata R, et al. Redox injectable gel protects osteoblastic function against oxidative stress and suppresses alveolar bone loss in a rat peri-implantitis model. Acta Biomater. 2020;110:82–94. https://doi.org/10.1016/j.actbio.2020.04.003 .
doi: 10.1016/j.actbio.2020.04.003
pubmed: 32348918
Takamori Y, Atsuta I, Nakamura H, Sawase T, Koyano K, Hara Y. Histopathological comparison of the onset of peri-implantitis and periodontitis in rats. Clin Oral Implants Res. 2017;28:163–70. https://doi.org/10.1111/clr.12777 .
doi: 10.1111/clr.12777
pubmed: 26804139
Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, NC3Rs Reporting Guidelines Working Group. Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol. 2010;160:1577–9. https://doi.org/10.1111/j.1476-5381.2010.00872.x .
doi: 10.1111/j.1476-5381.2010.00872.x
pubmed: 20649561
pmcid: 2936830
Green TRF, Murphy SM, Rowe RK. Comparisons of quantitative approaches for assessing microglial morphology reveal inconsistencies, ecological fallacy, and a need for standardization. Sci Rep. 2022;12:18196. https://doi.org/10.1038/s41598-022-23091-2 .
doi: 10.1038/s41598-022-23091-2
pubmed: 36307475
pmcid: 9616881
Loos BG, Van Dyke TE. The role of inflammation and genetics in periodontal disease. Periodontol 2000. 2020;83:26–39. https://doi.org/10.1111/prd.12297 .
doi: 10.1111/prd.12297
pubmed: 32385877
pmcid: 7319430
Zhang W, Xiao D, Mao Q, Xia H. Role of neuroinflammation in neurodegeneration development. Signal Transduc Target Ther. 2023;8:67. https://doi.org/10.1038/s41392-023-01486-5 .
doi: 10.1038/s41392-023-01486-5
Zhang S, Yang F, Wang Z, Qian X, Ji Y, Gong L, et al. Poor oral health conditions and cognitive decline: studies in humans and rats. PLoS ONE. 2020;15:e0234659. https://doi.org/10.1371/journal.pone.0234659 .
doi: 10.1371/journal.pone.0234659
pubmed: 32614834
pmcid: 7332063
Qian X, Zhang S, Duan L, Yang F, Zhang K, Yan F, et al. Periodontitis deteriorates cognitive function and impairs neurons and glia in a mouse model of Alzheimer’s Disease. J Alzheimers Dis. 2021;79:1785–800. https://doi.org/10.3233/JAD-201007 .
doi: 10.3233/JAD-201007
pubmed: 33459718
Duan L, Qian X, Wang Q, Huang L, Ge S. Experimental periodontitis deteriorates cognitive function and impairs insulin signaling in a streptozotocin-induced Alzheimer’s Disease rat model. J Alzheimers Dis. 2022;88:57–74. https://doi.org/10.3233/JAD-215720 .
doi: 10.3233/JAD-215720
pubmed: 35527550
Feng YK, Wu QL, Peng YW, Liang FY, You HJ, Feng YW, et al. Oral P. gingivalis impairs gut permeability and mediates immune responses associated with neurodegeneration in LRRK2 R1441G mice. J Neuroinflammation. 2020;17:347. https://doi.org/10.1186/s12974-020-02027-5 .
doi: 10.1186/s12974-020-02027-5
pubmed: 33213462
pmcid: 7677837
Houser MC, Tansey MG. The gut-brain axis: is intestinal inflammation a silent driver of Parkinson’s disease pathogenesis? NPJ Parkinson’s disease. 2017;3:3. https://doi.org/10.1038/s41531-016-0002-0 .
Farhad SZ, Rezazadeh F, Mohammadi M. Interleukin – 17 and interleukin-10 as inflammatory and prevention biomarkers in periimplant diseases. Int J Prev Med. 2019;10:137. https://doi.org/10.4103/ijpvm.IJPVM_27_19 .
doi: 10.4103/ijpvm.IJPVM_27_19
pubmed: 31516678
pmcid: 6710915
Schenkein HA, Koertge TE, Brooks CN, Sabatini R, Purkall DE, Tew JG. IL-17 in sera from patients with aggressive periodontitis. J Dent Res. 2010;89:943–7. https://doi.org/10.1177/0022034510369297 .
doi: 10.1177/0022034510369297
pubmed: 20400718
pmcid: 3144093
Swardfager W, Lanctôt K, Rothenburg L, Wong A, Cappell J, Herrmann N. A meta-analysis of cytokines in Alzheimer’s disease. Biol Psychiatr. 2010;68(10):930–41. https://doi.org/10.1016/j.biopsych.2010.06.012 .
doi: 10.1016/j.biopsych.2010.06.012
Lyra E, Silva NM, Gonçalves RA, Pascoal TA, Lima-Filho RAS, Resende EPF, Vieira ELM, et al. Pro-inflammatory interleukin-6 signaling links cognitive impairments and peripheral metabolic alterations in Alzheimer’s disease. Transl Psychiatry. 2021;11(1):251. https://doi.org/10.1038/s41398-021-01349-z .
doi: 10.1038/s41398-021-01349-z
Green HF, Khosousi S, Svenningsson P, Plasma. IL-6 and IL-17A correlate with severity of motor and non-motor symptoms in Parkinson’s Disease. J Parkinsons Dis. 2019;9:705–9. https://doi.org/10.3233/JPD-191699 .
doi: 10.3233/JPD-191699
pubmed: 31524180
pmcid: 6839458
Balschun D, Wetzel W, del Rey A, Pitossi F, Schneider H, Zuschratter W, et al. Interleukin-6: a cytokine to forget. FASEB J. 2004;18:1788–90. https://doi.org/10.1096/fj.04-1625fje .
doi: 10.1096/fj.04-1625fje
pubmed: 15345694
Burton MD, Rytych JL, Freund GG, Johnson RW. Central inhibition of interleukin-6 trans-signaling during peripheral infection reduced neuroinflammation and sickness in aged mice. Brain Behav Immun. 2013;30:66–72. https://doi.org/10.1016/j.bbi.2013.01.002 .
doi: 10.1016/j.bbi.2013.01.002
pubmed: 23354002
pmcid: 3641158
Erta M, Quintana A, Hidalgo J. Interleukin-6, a major cytokine in the central nervous system. Int J Biol Sci. 2012;8:1254–66. https://doi.org/10.7150/ijbs.4679 .
doi: 10.7150/ijbs.4679
pubmed: 23136554
pmcid: 3491449
Rothaug M, Becker-Pauly C, Rose-John S. The role of interleukin-6 signaling in nervous tissue. Biochim Biophys Acta. 2016;1863(6 Pt A):1218–27. https://doi.org/10.1016/j.bbamcr.2016.03.018 .
doi: 10.1016/j.bbamcr.2016.03.018
pubmed: 27016501
Chakrabarty P, Jansen-West K, Beccard A, Ceballos‐Diaz C, Levites Y, Verbeeck C, et al. Massive gliosis induced by interleukin‐6 suppresses Aβ deposition in vivo: evidence against inflammation as a driving force for amyloid deposition. FASEB J. 2010;24:548–59. https://doi.org/10.1096/fj.09-141754 .
doi: 10.1096/fj.09-141754
pubmed: 19825975
pmcid: 3083918
Ng A, Tam WW, Zhang MW, Ho CS, Husain SF, McIntyre RS, et al. IL-1β, IL-6, TNF- α and CRP in elderly patients with depression or Alzheimer’s disease: systematic review and meta-analysis. Sci Rep. 2018;8:12050. https://doi.org/10.1038/s41598-018-30487-6 .
doi: 10.1038/s41598-018-30487-6
pubmed: 30104698
pmcid: 6089986
Tarkowski E, Andreasen N, Tarkowski A, Blennow K. Intrathecal inflammation precedes development of Alzheimer’s disease. J Neurol Neurosurg Psychiatry. 2003;74:1200–5. https://doi.org/10.1136/jnnp.74.9.1200 .
doi: 10.1136/jnnp.74.9.1200
pubmed: 12933918
pmcid: 1738668
Hu WT, Howell JC, Ozturk T, Gangishetti U, Kollhoff AL, Hatcher-Martin JM, et al. CSF cytokines in aging, multiple sclerosis, and dementia. Front Immunol. 2019;10:480. https://doi.org/10.3389/fimmu.2019.00480 .
doi: 10.3389/fimmu.2019.00480
pubmed: 30930904
pmcid: 6428695
Xiromerisiou G, Marogianni C, Lampropoulos IC, Dardiotis E, Speletas M, Ntavaroukas P, et al. Peripheral inflammatory markers TNF-α and CCL2 revisited: Association with Parkinson’s Disease severity. Int J Mol Sci. 2022;24:264. https://doi.org/10.3390/ijms24010264 .
doi: 10.3390/ijms24010264
pubmed: 36613708
pmcid: 9820450
Amin R, Quispe C, Docea AO, Ydyrys A, Kulbayeva M, Durna Daştan S, et al. The role of tumour necrosis factor in neuroinflammation associated with Parkinson’s Disease and targeted therapies. Neurochem Int. 2022;158:105376. https://doi.org/10.1016/j.neuint.2022.105376 .
doi: 10.1016/j.neuint.2022.105376
pubmed: 35667491
Torres-Acosta N, O’Keefe JH, O’Keefe EL, Isaacson R, Small G. Therapeutic potential of TNF-α inhibition for Alzheimer’s Disease prevention. J Alzheimers Dis. 2020;78:619–26. https://doi.org/10.3233/JAD-200711 .
doi: 10.3233/JAD-200711
pubmed: 33016914
pmcid: 7739965
Dhapola R, Hota SS, Sarma P, Bhattacharyya A, Medhi B, Reddy DH. Recent advances in molecular pathways and therapeutic implications targeting neuroinflammation for Alzheimer’s disease. Inflammopharmacology. 2021;29:1669–81. https://doi.org/10.1007/s10787-021-00889-6 .
doi: 10.1007/s10787-021-00889-6
pubmed: 34813026
pmcid: 8608577
Wu Y, Eisel ULM. Microglia-astrocyte communication in Alzheimer’s Disease. J Alzheimers Dis. 2023;95:785–803. https://doi.org/10.3233/JAD-230199 .
doi: 10.3233/JAD-230199
pubmed: 37638434
pmcid: 10578295
Chen K, Wang H, Ilyas I, Mahmood A, Hou L. Microglia and astrocytes dysfunction and key neuroinflammation-based biomarkers in Parkinson’s Disease. Brain Sci. 2023;13:634. https://doi.org/10.3390/brainsci13040634 .
doi: 10.3390/brainsci13040634
pubmed: 37190599
pmcid: 10136556
Fakhoury M. Microglia and astrocytes in Alzheimer’s Disease: implications for therapy. Curr Neuropharmacol. 2018;16:508–18. https://doi.org/10.2174/1570159X15666170720095240 .
doi: 10.2174/1570159X15666170720095240
pubmed: 28730967
pmcid: 5997862
Minagar A, Shapshak P, Fujimura R, Ownby R, Heyes M, Eisdorfer C. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J Neurol Sci. 2002;202:13–23. https://doi.org/10.1016/s0022-510x(02)00207-1 .
doi: 10.1016/s0022-510x(02)00207-1
pubmed: 12220687
Kantarci A, Tognoni CM, Yaghmoor W, Marghalani A, Stephens D, Ahn JY, Carreras I, et al. Microglial response to experimental periodontitis in a murine model of Alzheimer’s disease. Sci Rep. 2020;10:18561. https://doi.org/10.1038/s41598-020-75517-4 .
doi: 10.1038/s41598-020-75517-4
pubmed: 33122702
pmcid: 7596239
Zhang X, Zhang X, Qiu C, Shen H, Zhang H, He Z, et al. The imbalance of Th17/Treg via STAT3 activation modulates cognitive impairment in P. Gingivalis LPS-induced periodontitis mice. J Leukoc Biol. 2021;110:511–24. https://doi.org/10.1002/JLB.3MA0521-742RRR .
doi: 10.1002/JLB.3MA0521-742RRR
pubmed: 34342041
Kam TI, Hinkle JT, Dawson TM, Dawson VL. Microglia and astrocyte dysfunction in Parkinson’s disease. Neurobiol Dis. 2020;144:105028. https://doi.org/10.1016/j.nbd.2020.105028 .
doi: 10.1016/j.nbd.2020.105028
pubmed: 32736085
pmcid: 7484088
Hajishengallis G, Diaz PI. Porphyromonas gingivalis: Immune subversion activities and role in periodontal dysbiosis. Curr Oral Health Rep. 2020;7(1):12–21. https://doi.org/10.1007/s40496-020-00249-3 .
doi: 10.1007/s40496-020-00249-3
pubmed: 33344104
pmcid: 7747940
Tzach-Nahman R, Mizraji G, Shapira L, Nussbaum G, Wilensky A. Oral infection with Porphyromonas gingivalis induces peri-implantitis in a murine model: evaluation of bone loss and the local inflammatory response. J Clin Periodontol. 2017;44:739–48. https://doi.org/10.1111/jcpe.12735 .
doi: 10.1111/jcpe.12735
pubmed: 28453225
de Waal YC, Eijsbouts HV, Winkel EG, van Winkelhoff AJ. Microbial characteristics of peri-implantitis: a case-control study. J Periodontol. 2017;88:209–17. https://doi.org/10.1902/jop.2016.160231 .
doi: 10.1902/jop.2016.160231
pubmed: 27666672
Díaz-Zúñiga J, More J, Melgar-Rodríguez S, Jiménez-Unión M, Villalobos-Orchard F, Muñoz-Manríquez C, et al. Alzheimer’s Disease-like pathology triggered by Porphyromonas gingivalis in wild type rats is serotype dependent. Front Immunol. 2020;11:588036. https://doi.org/10.3389/fimmu.2020.588036 .
doi: 10.3389/fimmu.2020.588036
pubmed: 33240277
pmcid: 7680957
Olsen I. Porphyromonas gingivalis-induced neuroinflammation in Alzheimer’s Disease. Front Neurosci. 2021;15:691016. https://doi.org/10.3389/fnins.2021.691016 .
doi: 10.3389/fnins.2021.691016
pubmed: 34720846
pmcid: 8551391
Díaz-Zúñiga J, Muñoz Y, Melgar-Rodríguez S, More J, Bruna B, Lobos P, et al. Serotype b of Aggregatibacter actinomycetemcomitans triggers pro-inflammatory responses and amyloid beta secretion in hippocampal cells: a novel link between periodontitis and Alzheimer´s disease? J Oral Microbiol. 2019;11:1586423. https://doi.org/10.1080/20002297.2019.1586423 .
doi: 10.1080/20002297.2019.1586423
pubmed: 31044031
pmcid: 6484476
Dominy SS, Lynch C, Ermini F, Benedyk M, Marczyk A, Konradi A, et al. Porphyromonas gingivalis in Alzheimer’s disease brevidenceidence for disease causation and treatment with small-molecule inhibitors. Sci Adv. 2019;5:eaau3333. https://doi.org/10.1126/sciadv.aau3333 .
doi: 10.1126/sciadv.aau3333
pubmed: 30746447
pmcid: 6357742
Ding Y, Ren J, Yu H, Yu W, Zhou Y. Porphyromonas gingivalis, a periodontitis causing bacterium, induces memory impairment and age-dependent neuroinflammation in mice. Immun Ageing. 2018;15:6. https://doi.org/10.1186/s12979-017-0110-7 .
doi: 10.1186/s12979-017-0110-7
pubmed: 29422938
pmcid: 5791180
Ishida N, Ishihara Y, Ishida K, Tada H, Funaki-Kato Y, Hagiwara M, et al. Periodontitis induced by bacterial infection exacerbates features of Alzheimer’s disease in transgenic mice. NPJ Aging Mech Dis. 2017;3:15. https://doi.org/10.1038/s41514-017-0015-x .
doi: 10.1038/s41514-017-0015-x
pubmed: 29134111
pmcid: 5673943
Vargas-Caraveo A, Sayd A, Maus SR, Caso JR, Madrigal JLM, García-Bueno B, et al. Lipopolysaccharide enters the rat brain by a lipoprotein-mediated transport mechanism in physiological conditions. Sci Rep. 2017;7:13113. https://doi.org/10.1038/s41598-017-13302-6 .
doi: 10.1038/s41598-017-13302-6
pubmed: 29030613
pmcid: 5640642
Vila J, Sáez-López E, Johnson JR, Römling U, Dobrindt U, Cantón R, et al. Escherichia coli: an old friend with new tidings. FEMS Microbiol Rev. 2016;40:437–63. https://doi.org/10.1093/femsre/fuw005 .
doi: 10.1093/femsre/fuw005
pubmed: 28201713
Nam HY, Nam JH, Yoon G, Lee JY, Nam Y, Kang HJ, et al. Ibrutinib suppresses LPS-induced neuroinflammatory responses in BV2 microglial cells and wild-type mice. J Neuroinflammation. 2018;15:271. https://doi.org/10.1186/s12974-018-1308-0 .
doi: 10.1186/s12974-018-1308-0
pubmed: 30231870
pmcid: 6145206
Subedi L, Kwon OW, Pak C, Lee G, Lee K, Kim H, et al. N,N-disubstituted azines attenuate LPS-mediated neuroinflammation in microglia and neuronal apoptosis via inhibiting MAPK signaling pathways. BMC Neurosci. 2017;18:82. https://doi.org/10.1186/s12868-017-0399-3 .
doi: 10.1186/s12868-017-0399-3
pubmed: 29281977
pmcid: 5745756
Xu J, Yuan C, Wang G, Luo J, Ma H, Xu L, et al. Urolithins attenuate LPS-induced neuroinflammation in BV2 microglia via MAPK, akt, and NF-κB signaling pathways. J Agric Food Chem. 2018;66:571–80. https://doi.org/10.1021/acs.jafc.7b03285 .
doi: 10.1021/acs.jafc.7b03285
pubmed: 29336147
La Vitola P, Balducci C, Baroni M, Artioli L, Santamaria G, Castiglioni M, et al. Peripheral inflammation exacerbates α-synuclein toxicity and neuropathology in Parkinson’s models. Neuropath Appl Neuro. 2021;47:43–60. https://doi.org/10.1111/nan.12644 .
doi: 10.1111/nan.12644
Rutherford NJ, Sacino AN, Brooks M, Ceballos-Diaz C, Ladd TB, Howard JK, et al. Studies of lipopolysaccharide effects on the induction of α-synuclein pathology by exogenous fibrils in transgenic mice. Mol Neurodegener. 2015;10:32. https://doi.org/10.1186/s13024-015-0029-4 .
doi: 10.1186/s13024-015-0029-4
pubmed: 26223783
pmcid: 4520273
Zhan X, Stamova B, Jin LW, DeCarli C, Phinney B, Sharp FR. Gram-negative bacterial molecules associate with Alzheimer disease pathology. Neurology. 2016;87:2324–32. https://doi.org/10.1212/WNL.0000000000003391 .
doi: 10.1212/WNL.0000000000003391
pubmed: 27784770
pmcid: 5135029
Savica R, Carlin JM, Grossardt BR, Bower JH, Ahlskog JE, Maraganore DM, et al. Medical records documentation of constipation preceding Parkinson disease: a case-control study. Neurology. 2009;73:1752–8. https://doi.org/10.1212/WNL.0b013e3181c34af5 .
doi: 10.1212/WNL.0b013e3181c34af5
pubmed: 19933976
pmcid: 2788809
Sampson TR, Challis C, Jain N, Moiseyenko A, Ladinsky MS, Shastri GG, et al. A gut bacterial amyloid promotes α-synuclein aggregation and motor impairment in mice. eLife. 2020;9:e53111. https://doi.org/10.7554/eLife.53111 .
doi: 10.7554/eLife.53111
pubmed: 32043464
pmcid: 7012599
Qiu C, Yuan Z, He Z, Chen H, Liao Y, Li S, et al. Lipopolysaccharide preparation derived from Porphyromonas gingivalis induces a weaker immuno-inflammatory response in BV-2 microglial cells than Escherichia coli by differentially activating TLR2/4-mediated NF-κB/STAT3 signaling pathways. Front Cell Infect Microbiol. 2021;11:606986. https://doi.org/10.3389/fcimb.2021.606986 .
doi: 10.3389/fcimb.2021.606986
pubmed: 33816329
pmcid: 8012810
Gao HM, Zhang F, Zhou H, Kam W, Wilson B, Hong JS. Neuroinflammation and α-synuclein dysfunction potentiate each other, driving chronic progression of neurodegeneration in a mouse model of Parkinson’s disease. Environ Health Perspect. 2011;119:807–14. https://doi.org/10.1289/ehp.1003013 .
doi: 10.1289/ehp.1003013
pubmed: 21245015
pmcid: 3114815
Lee DY, Shin YJ, Kim JK, Jang HM, Joo MK, Kim DH. Alleviation of cognitive impairment by gut microbiota lipopolysaccharide production-suppressing Lactobacillus plantarum and Bifidobacterium longum in mice. Food Funct. 2021;12:10750–63. https://doi.org/10.1039/d1fo02167b .
doi: 10.1039/d1fo02167b
pubmed: 34608923
Batista CRA, Gomes GF, Candelario-Jalil E, Fiebich BL, de Oliveira ACP. Lipopolysaccharide-induced neuroinflammation as a bridge to understand neurodegeneration. Int J Mol Sci. 2019;20:2293. https://doi.org/10.3390/ijms20092293 .
doi: 10.3390/ijms20092293
pubmed: 31075861
pmcid: 6539529
Skrzypczak-Wiercioch A, Sałat K. Lipopolysaccharide-induced model of neuroinflammation: mechanisms of action, research application and future directions for its use. Molecules. 2022;27:5481. https://doi.org/10.3390/molecules27175481 .
doi: 10.3390/molecules27175481
pubmed: 36080253
pmcid: 9457753
Hu Y, Zhang X, Zhang J, Xia X, Li H, Qiu C, et al. Activated STAT3 signaling pathway by ligature-induced periodontitis could contribute to neuroinflammation and cognitive impairment in rats. J Neuroinflammation. 2021;18:80. https://doi.org/10.1186/s12974-021-02071-9 .
doi: 10.1186/s12974-021-02071-9
pubmed: 33757547
pmcid: 7986277
Nakamura T, Zou K, Shibuya Y, Michikawa M. Oral dysfunctions and cognitive impairment/dementia. J Neurosci Res. 2021;99:518–28. https://doi.org/10.1002/jnr.24745 .
doi: 10.1002/jnr.24745
pubmed: 33164225
Galindo-Moreno P, Lopez-Chaichio L, Padial-Molina M, Avila-Ortiz G, O’Valle F, Ravida A, et al. The impact of tooth loss on cognitive function. Clin Oral Investig. 2022;26:3493–500. https://doi.org/10.1007/s00784-021-04318-4 .
doi: 10.1007/s00784-021-04318-4
pubmed: 34881401
Oue H, Miyamoto Y, Koretake K, Okada S, Doi K, Jung CG, Michikawa M, Akagawa Y. Tooth loss might not alter molecular pathogenesis in an aged transgenic Alzheimer’s disease model mouse. Gerodontology. 2016;33:308–14. https://doi.org/10.1111/ger.12153 .
doi: 10.1111/ger.12153
pubmed: 25243637
Hu Y, Li H, Zhang J, Zhang X, Xia X, Qiu C, et al. Periodontitis induced by P. gingivalis-LPS is associated with neuroinflammation and learning and memory impairment in Sprague-Dawley rats. Front Neurosci. 2020;14:658. https://doi.org/10.3389/fnins.2020.00658 .
doi: 10.3389/fnins.2020.00658
pubmed: 32714134
pmcid: 7344110