Loss of Neutrophil Homing to the Periodontal Tissues Modulates the Composition and Disease Potential of the Oral Microbiota

Periodontal disease is considered to arise from an imbalance in the interplay between the host and its commensal microbiota, characterized by inflammation, destructive periodontal bone loss, and a dysbiotic oral microbial community. The neutrophil is a key component of defense of the periodontium: d...

Full description

Saved in:
Bibliographic Details
Published in:Infection and immunity Vol. 89; no. 12; p. e0030921
Main Authors: Hashim, A, Alsam, A, Payne, M A, Aduse-Opoku, J, Curtis, M A, Joseph, S
Format: Journal Article
Language:English
Published: United States 16.11.2021
Subjects:
Animals
Biomarkers
Disease Models, Animal
Disease Susceptibility
Dysbiosis
Mice
Mice, Knockout
Microbiota
Neutrophil Infiltration
Neutrophils - physiology
Periodontal Diseases - etiology
Periodontal Diseases - metabolism
Periodontal Diseases - pathology
Periodontitis - etiology
Periodontitis - metabolism
Periodontitis - pathology
Receptors, Interleukin-8B - genetics
Receptors, Interleukin-8B - metabolism
CXCR2
periodontitis
oral microbiology
oral microbiome
neutrophils
bone loss
dysbiosis
ISSN:1098-5522, 1098-5522
Online Access:Get more information
Tags: Add Tag
No Tags, Be the first to tag this record!
Abstract Periodontal disease is considered to arise from an imbalance in the interplay between the host and its commensal microbiota, characterized by inflammation, destructive periodontal bone loss, and a dysbiotic oral microbial community. The neutrophil is a key component of defense of the periodontium: defects in their number or efficacy of function predisposes individuals to development of periodontal disease. Paradoxically, neutrophil activity, as part of a deregulated inflammatory response, is considered an important element in the destructive disease process. In this investigation, we examined the role the neutrophil plays in the regulation of the oral microbiota by analysis of the microbiome composition in mice lacking the CXCR2 neutrophil receptor required for recruitment to the periodontal tissues. A breeding protocol was employed that ensured that only the oral microbiota of wild-type (CXCR2 ) mice was transferred to subsequent generations of wild-type, heterozygote, and homozygote littermates. In the absence of neutrophils, the microbiome undergoes a significant shift in total load and composition compared to when normal levels of neutrophil recruitment into the gingival tissues occur, and this is accompanied by a significant increase in periodontal bone pathology. However, transfer of the oral microbiome of CXCR2 mice into germfree CXCR2 mice led to restoration of the microbiome to the wild-type CXCR2 composition and the absence of pathology. These data demonstrate that the composition of the oral microbiome is inherently flexible and is governed to a significant extent by the genetics and resultant phenotype of the host organism.
AbstractList Periodontal disease is considered to arise from an imbalance in the interplay between the host and its commensal microbiota, characterized by inflammation, destructive periodontal bone loss, and a dysbiotic oral microbial community. The neutrophil is a key component of defense of the periodontium: defects in their number or efficacy of function predisposes individuals to development of periodontal disease. Paradoxically, neutrophil activity, as part of a deregulated inflammatory response, is considered an important element in the destructive disease process. In this investigation, we examined the role the neutrophil plays in the regulation of the oral microbiota by analysis of the microbiome composition in mice lacking the CXCR2 neutrophil receptor required for recruitment to the periodontal tissues. A breeding protocol was employed that ensured that only the oral microbiota of wild-type (CXCR2 ) mice was transferred to subsequent generations of wild-type, heterozygote, and homozygote littermates. In the absence of neutrophils, the microbiome undergoes a significant shift in total load and composition compared to when normal levels of neutrophil recruitment into the gingival tissues occur, and this is accompanied by a significant increase in periodontal bone pathology. However, transfer of the oral microbiome of CXCR2 mice into germfree CXCR2 mice led to restoration of the microbiome to the wild-type CXCR2 composition and the absence of pathology. These data demonstrate that the composition of the oral microbiome is inherently flexible and is governed to a significant extent by the genetics and resultant phenotype of the host organism.
Periodontal disease is considered to arise from an imbalance in the interplay between the host and its commensal microbiota, characterized by inflammation, destructive periodontal bone loss, and a dysbiotic oral microbial community. The neutrophil is a key component of defense of the periodontium: defects in their number or efficacy of function predisposes individuals to development of periodontal disease. Paradoxically, neutrophil activity, as part of a deregulated inflammatory response, is considered an important element in the destructive disease process. In this investigation, we examined the role the neutrophil plays in the regulation of the oral microbiota by analysis of the microbiome composition in mice lacking the CXCR2 neutrophil receptor required for recruitment to the periodontal tissues. A breeding protocol was employed that ensured that only the oral microbiota of wild-type (CXCR2+/+) mice was transferred to subsequent generations of wild-type, heterozygote, and homozygote littermates. In the absence of neutrophils, the microbiome undergoes a significant shift in total load and composition compared to when normal levels of neutrophil recruitment into the gingival tissues occur, and this is accompanied by a significant increase in periodontal bone pathology. However, transfer of the oral microbiome of CXCR2-/- mice into germfree CXCR2+/+ mice led to restoration of the microbiome to the wild-type CXCR2+/+ composition and the absence of pathology. These data demonstrate that the composition of the oral microbiome is inherently flexible and is governed to a significant extent by the genetics and resultant phenotype of the host organism.Periodontal disease is considered to arise from an imbalance in the interplay between the host and its commensal microbiota, characterized by inflammation, destructive periodontal bone loss, and a dysbiotic oral microbial community. The neutrophil is a key component of defense of the periodontium: defects in their number or efficacy of function predisposes individuals to development of periodontal disease. Paradoxically, neutrophil activity, as part of a deregulated inflammatory response, is considered an important element in the destructive disease process. In this investigation, we examined the role the neutrophil plays in the regulation of the oral microbiota by analysis of the microbiome composition in mice lacking the CXCR2 neutrophil receptor required for recruitment to the periodontal tissues. A breeding protocol was employed that ensured that only the oral microbiota of wild-type (CXCR2+/+) mice was transferred to subsequent generations of wild-type, heterozygote, and homozygote littermates. In the absence of neutrophils, the microbiome undergoes a significant shift in total load and composition compared to when normal levels of neutrophil recruitment into the gingival tissues occur, and this is accompanied by a significant increase in periodontal bone pathology. However, transfer of the oral microbiome of CXCR2-/- mice into germfree CXCR2+/+ mice led to restoration of the microbiome to the wild-type CXCR2+/+ composition and the absence of pathology. These data demonstrate that the composition of the oral microbiome is inherently flexible and is governed to a significant extent by the genetics and resultant phenotype of the host organism.
Author Aduse-Opoku, J
Curtis, M A
Payne, M A
Alsam, A
Joseph, S
Hashim, A
Author_xml – sequence: 1
  givenname: A
  surname: Hashim
  fullname: Hashim, A
  organization: Department of Biomedical Sciences, College of Dentistry, King Faisal Universitygrid.412140.2, Al-Ahsa, Saudi Arabia
– sequence: 2
  givenname: A
  surname: Alsam
  fullname: Alsam, A
  organization: Institute of Dentistry, Barts and The London School of Medicine and Dentistry, Queen Mary University of Londongrid.4868.2, London, United Kingdom
– sequence: 3
  givenname: M A
  surname: Payne
  fullname: Payne, M A
  organization: Institute of Dentistry, Barts and The London School of Medicine and Dentistry, Queen Mary University of Londongrid.4868.2, London, United Kingdom
– sequence: 4
  givenname: J
  surname: Aduse-Opoku
  fullname: Aduse-Opoku, J
  organization: Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, United Kingdom
– sequence: 5
  givenname: M A
  surname: Curtis
  fullname: Curtis, M A
  organization: Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, United Kingdom
– sequence: 6
  givenname: S
  orcidid: 0000-0002-0297-5405
  surname: Joseph
  fullname: Joseph, S
  organization: Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, United Kingdom
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34491788$$D View this record in MEDLINE/PubMed
BookMark eNpNkM1LAzEQxYNU7IfePEuOXrYm2Ww3OZb6VWith3pekiZrI7uZuskexH_eFCsIA_Ngfu8xM2M08OAtQteUTCll4m45X04JyYnMGD1DI0qkyIqCscE_PUTjED4IoZxzcYGGOeeSlkKM0PcKQsBQ4xfbxw4Oe9fgZ2idf8cRcNxb_Go7BwZ8VA3euhB6G_AaTN-omNSRWEB7gOCiA4-VN_jeBatCckK0PrrkS_lHcNMlvXa7DrSDqC7Rea2aYK9OfYLeHh-2i-dstXlaLuarTHHBYyaZqUmtdjMxU1zpdIOUllstKRWGaUWJkjWflUVptSaKmVxLYrhKI1vonLMJuv3NPXTwmdaPVevCzjaN8hb6ULGiJHnJUyX05oT2urWmOnSuVd1X9fcw9gNr8nAd
CitedBy_id crossref_primary_10_1111_odi_14803
crossref_primary_10_3390_dj12100299
crossref_primary_10_1016_j_chom_2023_02_009
crossref_primary_10_1038_s41423_025_01261_2
crossref_primary_10_1080_1744666X_2023_2182291
crossref_primary_10_3389_froh_2022_866695
crossref_primary_10_1177_00220345221149675
crossref_primary_10_1002_1873_3468_70113
crossref_primary_10_1186_s12967_022_03636_9
crossref_primary_10_7554_eLife_88183_3
crossref_primary_10_1002_JLB_3MR0822_645RR
crossref_primary_10_7554_eLife_88183
crossref_primary_10_1016_j_celrep_2025_116245
crossref_primary_10_3389_fped_2022_914243
crossref_primary_10_3389_fnut_2025_1551349
crossref_primary_10_3390_nu17050762
ContentType Journal Article
DBID CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1128/IAI.00309-21
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE
MEDLINE - Academic
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Medicine
Biology
EISSN 1098-5522
ExternalDocumentID 34491788
Genre Research Support, Non-U.S. Gov't
Journal Article
GrantInformation_xml – fundername: UKRI | Medical Research Council (MRC)
  grantid: MR/P012175/1
– fundername: Medical Research Council
  grantid: MR/P012175/2
– fundername: Medical Research Council
  grantid: MR/J011118/1
– fundername: Medical Research Council
  grantid: MR/P012175/1
GroupedDBID ---
-DZ
-~X
.55
0R~
18M
29I
2WC
39C
4.4
53G
5GY
5RE
5VS
85S
AAGFI
ABOCM
ACGFO
ADBBV
AENEX
AGVNZ
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BAWUL
BTFSW
CGR
CS3
CUY
CVF
DIK
DU5
E3Z
EBS
ECM
EIF
F5P
FRP
GX1
H13
HYE
HZ~
IH2
KQ8
L7B
NPM
O9-
OK1
P2P
RHI
RNS
RPM
RSF
SJN
TR2
TWZ
UPT
W2D
W8F
WH7
WOQ
X7M
~KM
7X8
ID FETCH-LOGICAL-a484t-92df0fac686a4ab14499e4eb9118d2ba10a9f46757ebb0a2d3b90d4a2bae5b342
IEDL.DBID 7X8
ISICitedReferencesCount 16
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000754004400007&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1098-5522
IngestDate Fri Sep 05 07:46:06 EDT 2025
Sat May 31 02:10:19 EDT 2025
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 12
Keywords CXCR2
periodontitis
oral microbiology
oral microbiome
neutrophils
bone loss
dysbiosis
Language English
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-a484t-92df0fac686a4ab14499e4eb9118d2ba10a9f46757ebb0a2d3b90d4a2bae5b342
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0002-0297-5405
OpenAccessLink https://kclpure.kcl.ac.uk/portal/en/publications/5fecb834-e1e1-4a93-8b44-b6b38e3d4d11
PMID 34491788
PQID 2570374374
PQPubID 23479
ParticipantIDs proquest_miscellaneous_2570374374
pubmed_primary_34491788
PublicationCentury 2000
PublicationDate 20211116
PublicationDateYYYYMMDD 2021-11-16
PublicationDate_xml – month: 11
  year: 2021
  text: 20211116
  day: 16
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Infection and immunity
PublicationTitleAlternate Infect Immun
PublicationYear 2021
SSID ssj0014448
Score 2.4554296
Snippet Periodontal disease is considered to arise from an imbalance in the interplay between the host and its commensal microbiota, characterized by inflammation,...
SourceID proquest
pubmed
SourceType Aggregation Database
Index Database
StartPage e0030921
SubjectTerms Animals
Biomarkers
Disease Models, Animal
Disease Susceptibility
Dysbiosis
Mice
Mice, Knockout
Microbiota
Neutrophil Infiltration
Neutrophils - physiology
Periodontal Diseases - etiology
Periodontal Diseases - metabolism
Periodontal Diseases - pathology
Periodontitis - etiology
Periodontitis - metabolism
Periodontitis - pathology
Receptors, Interleukin-8B - genetics
Receptors, Interleukin-8B - metabolism
Title Loss of Neutrophil Homing to the Periodontal Tissues Modulates the Composition and Disease Potential of the Oral Microbiota
URI https://www.ncbi.nlm.nih.gov/pubmed/34491788
https://www.proquest.com/docview/2570374374
Volume 89
WOSCitedRecordID wos000754004400007&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV3dS8MwEA_qVHzxY37NLyL4Wtc1adM8yVDHBtvcw5S9jaRJcKDN3DpB_Oe9tB17EgRfSqBJCZfrfeR-d4fQjR_6KiZaeYY3Eo9GJnZyMPSIBj_Mj3SY5LlVL13W78ejER-UF27zEla5lIm5oFY2cXfkdddtjYC6Y_Ru-uG5rlEuulq20FhHFQKmjIN0sdEqikApLVLheOyFYGgsge9BXO80O7d-EV5o_G5c5kqmtfff7e2j3dK8xM2CHw7Qmk6raKtoOPlVRdu9MpR-iL67oB6xNbivF9nMTl8nb7ht30GT4cxiMAvxAJgTnFaXLomH-fnMcc8q1-8LRm6GEyYl6AuLVOGHItqDBzZzICRYB993E59mMO5NiqJPmThCz63H4X3bKzsxeILGNPN4oIxvRBLFkaBCAmE511RLkJSxCqRo-IIbELkh01L6IlBEcl9RAa90KAkNjtFGalN9irA2TKuIJcyVyAbrQOiIaWGo5JJIwlgNXS8JPAZOd-ELkWq7mI9XJK6hk-KUxtOiJMeYwI4a4M2f_WH1OdoJHDDFYfmiC1Qx8J_rS7SZfGaT-ewqZyF49ge9H60l0dU
linkProvider ProQuest
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Loss+of+Neutrophil+Homing+to+the+Periodontal+Tissues+Modulates+the+Composition+and+Disease+Potential+of+the+Oral+Microbiota&rft.jtitle=Infection+and+immunity&rft.au=Hashim%2C+A&rft.au=Alsam%2C+A&rft.au=Payne%2C+M+A&rft.au=Aduse-Opoku%2C+J&rft.date=2021-11-16&rft.issn=1098-5522&rft.eissn=1098-5522&rft.volume=89&rft.issue=12&rft.spage=e0030921&rft_id=info:doi/10.1128%2FIAI.00309-21&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1098-5522&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1098-5522&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1098-5522&client=summon