Neutrophils' Contribution to Periodontitis and Periodontitis-Associated Cardiovascular Diseases.


Journal

International journal of molecular sciences
ISSN: 1422-0067
Titre abrégé: Int J Mol Sci
Pays: Switzerland
ID NLM: 101092791

Informations de publication

Date de publication:
19 Oct 2023
Historique:
received: 04 09 2023
revised: 11 10 2023
accepted: 12 10 2023
medline: 30 10 2023
pubmed: 28 10 2023
entrez: 28 10 2023
Statut: epublish

Résumé

Neutrophils represent the primary defense against microbial threats playing a pivotal role in maintaining tissue homeostasis. This review examines the multifaceted involvement of neutrophils in periodontitis, a chronic inflammatory condition affecting the supporting structures of teeth summarizing the contribution of neutrophil dysfunction in periodontitis and periodontal-related comorbidities. Periodontitis, a pathological condition promoted by dysbiosis of the oral microbiota, is characterized by the chronic inflammation of the gingiva and subsequent tissue destruction. Neutrophils are among the first immune cells recruited to the site of infection, releasing antimicrobial peptides, enzymes, and reactive oxygen species to eliminate pathogens. The persistent inflammatory state in periodontitis can lead to aberrant neutrophil activation and a sustained release of proinflammatory mediators, finally resulting in tissue damage, bone resorption, and disease progression. Growing evidence now points to the correlation between periodontitis and systemic comorbidities. Indeed, the release of inflammatory mediators, immune complexes, and oxidative stress by neutrophils, bridge the gap between local and systemic immunity, thus highlighting neutrophils as key players in linking periodontal inflammation to chronic conditions, including cardiovascular diseases, diabetes mellitus, and rheumatoid arthritis. This review underscores the crucial role of neutrophils in the pathogenesis of periodontitis and the complex link between neutrophil dysfunction, local inflammation, and systemic comorbidities. A comprehensive understanding of neutrophil contribution to periodontitis development and their impact on periodontal comorbidities holds significant implications for the management of oral health. Furthermore, it highlights the need for the development of novel approaches aimed at limiting the persistent recruitment and activation of neutrophils, also reducing the impact of periodontal inflammation on broader health contexts, offering promising avenues for improved disease management and patient care.

Identifiants

pubmed: 37895050
pii: ijms242015370
doi: 10.3390/ijms242015370
pmc: PMC10607037
pii:
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Références

J Exp Med. 2023 Sep 4;220(9):
pubmed: 37261457
Blood. 2003 Nov 15;102(10):3562-8
pubmed: 12893769
Science. 2018 Sep 28;361(6409):
pubmed: 30262472
J Exp Med. 2010 Aug 30;207(9):1853-62
pubmed: 20733033
J Clin Periodontol. 2019 Jan;46(1):20-30
pubmed: 30362631
Annu Rev Physiol. 2022 Feb 10;84:183-207
pubmed: 34614373
Front Cardiovasc Med. 2023 Feb 27;10:1114927
pubmed: 36923959
Front Immunol. 2022 Mar 16;13:866747
pubmed: 35371088
Front Immunol. 2022 May 24;13:895216
pubmed: 35686129
J Clin Periodontol. 2020 Mar;47(3):268-288
pubmed: 32011025
Semin Immunol. 2021 Oct;57:101595
pubmed: 35125298
Respir Physiol Neurobiol. 2013 Jun 1;187(1):74-7
pubmed: 23499796
Front Physiol. 2021 Oct 27;12:709438
pubmed: 34776994
Arterioscler Thromb Vasc Biol. 2018 Jun;38(6):1415-1423
pubmed: 29699973
Front Immunol. 2021 Jul 28;12:706432
pubmed: 34394107
Nat Rev Immunol. 2011 Sep 09;11(10):685-92
pubmed: 21904387
Nat Rev Dis Primers. 2017 Jun 22;3:17038
pubmed: 28805207
Periodontol 2000. 2020 Oct;84(1):14-34
pubmed: 32844416
Nat Rev Cardiol. 2018 Sep;15(9):505-522
pubmed: 30065258
Sci Immunol. 2018 Aug 24;3(26):
pubmed: 30143555
Nat Rev Rheumatol. 2017 Oct;13(10):606-620
pubmed: 28835673
Proc Natl Acad Sci U S A. 2015 Mar 3;112(9):2817-22
pubmed: 25730848
Sci Rep. 2018 Feb 19;8(1):3290
pubmed: 29459661
Hypertension. 2021 May 5;77(5):1765-1774
pubmed: 33775115
Cell. 2020 Jul 23;182(2):447-462.e14
pubmed: 32758418
Clin Chem. 2005 Sep;51(9):1577-86
pubmed: 16020501
J Clin Invest. 2022 May 16;132(10):
pubmed: 35358095
J Immunol. 2010 Dec 15;185(12):7413-25
pubmed: 21098229
Cell Rep. 2020 Nov 17;33(7):108387
pubmed: 33207187
Community Dent Oral Epidemiol. 2002 Jun;30(3):182-92
pubmed: 12000341
Blood. 2013 Oct 17;122(16):2784-94
pubmed: 24009232
Cell. 2018 Jan 11;172(1-2):135-146.e9
pubmed: 29328908
Dev Cell. 2017 Nov 20;43(4):449-462.e5
pubmed: 29103955
Gut. 2017 May;66(5):872-885
pubmed: 26838600
Cell Rep. 2016 Dec 6;17(10):2584-2595
pubmed: 27926863
Blood. 2019 May 16;133(20):2178-2185
pubmed: 30898862
J Clin Periodontol. 2004 Dec;31(12):1122-7
pubmed: 15560816
Periodontol 2000. 2016 Feb;70(1):53-64
pubmed: 26662482
Int J Stroke. 2020 Feb;15(2):175-187
pubmed: 30794103
Cardiovasc Res. 2020 Jan 1;116(1):28-39
pubmed: 31549149
Infect Immun. 2017 Nov 17;85(12):
pubmed: 28947649
Arch Oral Biol. 2013 Sep;58(9):1187-98
pubmed: 23583017
Clin Exp Immunol. 2007 Feb;147(2):255-64
pubmed: 17223966
Cell Death Differ. 2009 Nov;16(11):1438-44
pubmed: 19609275
Science. 2021 Dec 24;374(6575):eabl5450
pubmed: 34941394
J Dent Res. 2020 Jul;99(7):839-846
pubmed: 32176550
J Wound Care. 2022 Oct 2;31(10):882-885
pubmed: 36240794
Cell. 2022 May 12;185(10):1709-1727.e18
pubmed: 35483374
Mucosal Immunol. 2016 Sep;9(5):1163-1172
pubmed: 26732676
Nat Med. 2019 Dec;25(12):1822-1832
pubmed: 31806905
PLoS Pathog. 2015 Mar 12;11(3):e1004651
pubmed: 25764063
Nat Rev Immunol. 2019 Apr;19(4):255-265
pubmed: 30816340
Front Immunol. 2013 Jan 24;4:1
pubmed: 23355837
Nat Commun. 2018 Jul 27;9(1):2958
pubmed: 30054480
Science. 2004 Mar 5;303(5663):1532-5
pubmed: 15001782
Int J Med Microbiol. 2015 Jun-Aug;305(4-5):453-63
pubmed: 25959370
Periodontol 2000. 2020 Jun;83(1):7-13
pubmed: 32385880
Int J Mol Sci. 2022 Oct 11;23(20):
pubmed: 36292925
Cell Host Microbe. 2011 Oct 20;10(4):302-6
pubmed: 22018230
Cell. 2018 Jan 11;172(1-2):162-175.e14
pubmed: 29328911
J Dent Res. 2021 Mar;100(3):318-325
pubmed: 33078669
J Exp Med. 2011 Feb 14;208(2):251-60
pubmed: 21282380
Annu Rev Immunol. 2005;23:197-223
pubmed: 15771570
Front Immunol. 2017 Feb 06;8:81
pubmed: 28220120
Glob Heart. 2020 Feb 03;15(1):1
pubmed: 32489774
Cell. 2020 Oct 29;183(3):771-785.e12
pubmed: 33125892
Cell Stem Cell. 2014 Apr 3;14(4):460-72
pubmed: 24561082
Immunol Rev. 2023 Mar;314(1):142-157
pubmed: 36190144
Exp Hematol Oncol. 2022 Nov 16;11(1):99
pubmed: 36384979
Nat Rev Immunol. 2015 Jan;15(1):30-44
pubmed: 25534621
Lancet. 2005 Nov 19;366(9499):1809-20
pubmed: 16298220
Mol Oral Microbiol. 2015 Oct;30(5):361-75
pubmed: 25869817
Periodontol 2000. 2020 Jun;83(1):90-106
pubmed: 32385879
Nat Rev Immunol. 2020 Jun;20(6):375-388
pubmed: 32132681
Nat Immunol. 2014 Jul;15(7):602-11
pubmed: 24940954
Front Immunol. 2021 Jan 29;11:578129
pubmed: 33584645
Curr Atheroscler Rep. 2020 Jun 8;22(7):28
pubmed: 32514778
Periodontol 2000. 2022 Jun;89(1):215-230
pubmed: 35244943
Cell Host Microbe. 2011 May 19;9(5):355-61
pubmed: 21575907
Immunity. 2018 Feb 20;48(2):364-379.e8
pubmed: 29466759
Curr Biol. 2006 Feb 21;16(4):401-7
pubmed: 16488875
Cell. 2018 Jan 11;172(1-2):176-190.e19
pubmed: 29328912
J Leukoc Biol. 2006 Dec;80(6):1281-8
pubmed: 16963624
J Cell Biol. 2009 Jan 26;184(2):205-13
pubmed: 19153223
J Exp Med. 2003 Nov 17;198(10):1507-15
pubmed: 14623906
JACC Cardiovasc Imaging. 2019 Nov;12(11 Pt 1):2271-2273
pubmed: 31326471
PLoS Pathog. 2019 May 20;15(5):e1007773
pubmed: 31107907
J Periodontol. 2002 Jan;73(1):73-8
pubmed: 11846202
Nat Rev Immunol. 2011 Jul 25;11(8):519-31
pubmed: 21785456
Mol Immunol. 2013 Aug;55(1):59-69
pubmed: 23141302
Medicina (Kaunas). 2020 May 30;56(6):
pubmed: 32486269
J Immunol Res. 2018 Jan 14;2018:8917804
pubmed: 29507865
Nature. 2017 Feb 8;542(7640):177-185
pubmed: 28179656
Nat Immunol. 2023 Apr;24(4):575-584
pubmed: 36959290
Quintessence Int. 2008 Jun;39(6):485-9
pubmed: 19057744
Periodontol 2000. 2022 Jun;89(1):9-18
pubmed: 35244969
J Clin Periodontol. 2006 Jun;33(6):401-7
pubmed: 16677328
Int J Cancer. 2017 Jun 1;140(11):2557-2567
pubmed: 28247912
Annu Rev Immunol. 2012;30:459-89
pubmed: 22224774
Periodontol 2000. 2013 Oct;63(1):165-97
pubmed: 23931060
Cell. 2018 Jan 11;172(1-2):147-161.e12
pubmed: 29328910
J Periodontal Res. 2012 Aug;47(4):439-45
pubmed: 22150619
Exp Hematol. 2021 Jan;93:1-13
pubmed: 33068648
J Inflamm (Lond). 2022 Nov 24;19(1):22
pubmed: 36424665
Nat Chem Biol. 2011 Feb;7(2):75-7
pubmed: 21170021
J Oral Biosci. 2021 Dec;63(4):360-369
pubmed: 34728373
Cell Stem Cell. 2019 Sep 5;25(3):357-372.e7
pubmed: 31230859
Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17537-42
pubmed: 22988082
Periodontol 2000. 2007;44:127-53
pubmed: 17474930
Nat Rev Immunol. 2021 Jul;21(7):426-440
pubmed: 33510490
Nature. 2017 Apr 6;544(7648):53-58
pubmed: 28355185
J Cell Biol. 2007 Jan 15;176(2):231-41
pubmed: 17210947
J Clin Periodontol. 2011 Mar;38 Suppl 11:126-41
pubmed: 21323710
J Immunol Res. 2017;2017:4218254
pubmed: 28428965
J Exp Med. 2023 Sep 4;220(9):
pubmed: 37552469
Adv Immunol. 2016;129:25-53
pubmed: 26791857
Nat Rev Immunol. 2022 Mar;22(3):173-187
pubmed: 34230649
Cell Stem Cell. 2018 May 3;22(5):627-638
pubmed: 29727678
JCI Insight. 2017 Oct 5;2(19):
pubmed: 28978799
J Clin Invest. 2000 Apr;105(8):1117-24
pubmed: 10772656
Mol Oral Microbiol. 2017 Aug;32(4):288-300
pubmed: 27476978
Br Dent J. 2019 Oct;227(7):577-584
pubmed: 31605062
Oncol Rev. 2020 Mar 18;14(1):465
pubmed: 32231765
Lancet Oncol. 2008 Jun;9(6):510-2
pubmed: 18510985
Diabetes. 2023 Jul 1;72(7):986-998
pubmed: 37058471
Science. 2019 Feb 8;363(6427):582-583
pubmed: 30733403
J Periodontal Res. 1995 May;30(3):159-66
pubmed: 7472997
J Innate Immun. 2010;2(6):576-86
pubmed: 20829609

Auteurs

Barbara Bassani (B)

Laboratory of Innate Immunity, Unit of Molecular Pathology, Biochemistry and Immunology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) MultiMedica, 20138 Milan, Italy.

Martina Cucchiara (M)

Laboratory of Innate Immunity, Unit of Molecular Pathology, Biochemistry and Immunology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) MultiMedica, 20138 Milan, Italy.
Immunology and General Pathology Laboratory, Department of Biotechnology and Life Sciences, University of Insubria, 21100 Varese, Italy.

Andrea Butera (A)

Unit of Dental Hygiene, Section of Dentistry, Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, 27100 Pavia, Italy.

Omar Kayali (O)

Laboratory of Innate Immunity, Unit of Molecular Pathology, Biochemistry and Immunology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) MultiMedica, 20138 Milan, Italy.

Alessandro Chiesa (A)

Unit of Dental Hygiene, Section of Dentistry, Department of Clinical, Surgical, Diagnostic and Pediatric Sciences, University of Pavia, 27100 Pavia, Italy.

Maria Teresa Palano (MT)

Laboratory of Innate Immunity, Unit of Molecular Pathology, Biochemistry and Immunology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) MultiMedica, 20138 Milan, Italy.

Francesca Olmeo (F)

Laboratory of Innate Immunity, Unit of Molecular Pathology, Biochemistry and Immunology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) MultiMedica, 20138 Milan, Italy.

Matteo Gallazzi (M)

Laboratory of Innate Immunity, Unit of Molecular Pathology, Biochemistry and Immunology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) MultiMedica, 20138 Milan, Italy.

Claudia Paola Bruna Dellavia (CPB)

Department of Biomedical, Surgical and Dental Sciences, University of Milan, 20122 Milan, Italy.

Lorenzo Mortara (L)

Immunology and General Pathology Laboratory, Department of Biotechnology and Life Sciences, University of Insubria, 21100 Varese, Italy.

Luca Parisi (L)

Department of Biomedical, Surgical and Dental Sciences, University of Milan, 20122 Milan, Italy.

Antonino Bruno (A)

Laboratory of Innate Immunity, Unit of Molecular Pathology, Biochemistry and Immunology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) MultiMedica, 20138 Milan, Italy.
Immunology and General Pathology Laboratory, Department of Biotechnology and Life Sciences, University of Insubria, 21100 Varese, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH