Dysbiosis From a Microbial and Host Perspective Relative to Oral Health and Disease.

caries commensal metabolomics metaproteomics oral immunology oral microbiology pathobiont periodontitis

Journal

Frontiers in microbiology
ISSN: 1664-302X
Titre abrégé: Front Microbiol
Pays: Switzerland
ID NLM: 101548977

Informations de publication

Date de publication:
2021
Historique:
received: 14 10 2020
accepted: 09 02 2021
entrez: 25 3 2021
pubmed: 26 3 2021
medline: 26 3 2021
Statut: epublish

Résumé

The significance of microbiology and immunology with regard to caries and periodontal disease gained substantial clinical or research consideration in the mid 1960's. This enhanced emphasis related to several simple but elegant experiments illustrating the relevance of bacteria to oral infections. Since that point, the understanding of oral diseases has become increasingly sophisticated and many of the original hypotheses related to disease causality have either been abandoned or amplified. The COVID pandemic has reminded us of the importance of history relative to infectious diseases and in the words of Churchill "those who fail to learn from history are condemned to repeat it." This review is designed to present an overview of broad general directions of research over the last 60 years in oral microbiology and immunology, reviewing significant contributions, indicating emerging foci of interest, and proposing future directions based on technical advances and new understandings. Our goal is to review this rich history (standard microbiology and immunology) and point to potential directions in the future (omics) that can lead to a better understanding of disease. Over the years, research scientists have moved from a position of downplaying the role of bacteria in oral disease to one implicating bacteria as true pathogens that cause disease. More recently it has been proposed that bacteria form the ecological first line of defense against "foreign" invaders and also serve to train the immune system as an acquired host defensive stimulus. While early immunological research was focused on immunological exposure as a modulator of disease, the "hygiene hypothesis," and now the "old friends hypothesis" suggest that the immune response could be trained by bacteria for long-term health. Advanced "omics" technologies are currently being used to address changes that occur in the host and the microbiome in oral disease. The "omics" methodologies have shaped the detection of quantifiable biomarkers to define human physiology and pathologies. In summary, this review will emphasize the role that commensals and pathobionts play in their interaction with the immune status of the host, with a prediction that current "omic" technologies will allow researchers to better understand disease in the future.

Identifiants

pubmed: 33763040
doi: 10.3389/fmicb.2021.617485
pmc: PMC7982844
doi:

Types de publication

Journal Article Review

Langues

eng

Pagination

617485

Subventions

Organisme : NIDCR NIH HHS
ID : R01 DE017968
Pays : United States
Organisme : NIDCR NIH HHS
ID : R21 DE027125
Pays : United States

Informations de copyright

Copyright © 2021 Cugini, Ramasubbu, Tsiagbe and Fine.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

Age (Dordr). 2011 Sep;33(3):363-76
pubmed: 20953722
Infect Immun. 1983 Aug;41(2):501-6
pubmed: 6409807
BMC Genomics. 2014 Apr 27;15:311
pubmed: 24767457
Front Microbiol. 2017 Nov 01;8:2144
pubmed: 29163429
Annu Rev Immunol. 2018 Apr 26;36:359-381
pubmed: 29400985
J Periodontol. 2009 Jan;80(1):106-13
pubmed: 19228096
Dent Regist. 1911 Dec 15;65(12):579-596
pubmed: 33702091
Antonie Van Leeuwenhoek. 1987;53(6):537-43
pubmed: 3329827
Semin Immunol. 2018 Dec;40:17-35
pubmed: 30287177
Periodontol 2000. 2006;42:47-79
pubmed: 16930306
J Clin Periodontol. 2017 Mar;44 Suppl 18:S23-S38
pubmed: 28266108
mSphere. 2019 Oct 9;4(5):
pubmed: 31597722
Trends Immunol. 2009 Jul;30(7):374-81
pubmed: 19541538
Front Microbiol. 2020 Apr 09;11:482
pubmed: 32328037
Gut. 2019 Jun;68(6):1108-1114
pubmed: 30670574
Annu Rev Microbiol. 2001;55:709-42
pubmed: 11544372
Nature. 2003 May 15;423(6937):337-42
pubmed: 12748652
Proteomics Clin Appl. 2019 Jul;13(4):e1800143
pubmed: 30548171
Int J Mol Sci. 2019 Sep 26;20(19):
pubmed: 31561483
Nature. 2012 Jun 13;486(7402):207-14
pubmed: 22699609
Immunobiology. 2014 May;219(5):350-6
pubmed: 24565410
Virulence. 2013 Aug 15;4(6):453-66
pubmed: 23715053
Am J Pathol. 1963 Jun;42:759-72
pubmed: 13945368
Cold Spring Harb Perspect Med. 2019 Jan 2;9(1):
pubmed: 29610150
J Dent Res. 1981 Sep;60(9):1634-8
pubmed: 6943155
Nat Rev Immunol. 2004 Jun;4(6):478-85
pubmed: 15173836
Proteomics. 2016 Mar;16(6):1033-45
pubmed: 26711623
Adv Immunol. 2013;120:163-84
pubmed: 24070384
Int Rev Immunol. 2011 Feb;30(1):16-34
pubmed: 21235323
J Infect Dis. 1956 Jan-Feb;98(1):15-20
pubmed: 13295619
Hepatology. 2017 Jan;65(1):32-43
pubmed: 27770558
Arch Oral Biol. 1985;30(4):377-9
pubmed: 3857909
Mucosal Immunol. 2020 May;13(3):530-544
pubmed: 31953493
Lancet Infect Dis. 2001 Sep;1(2):101-14
pubmed: 11871461
Infect Immun. 2018 Jan 22;86(2):
pubmed: 29084893
Adv Exp Med Biol. 2008;635:135-46
pubmed: 18841709
Oral Microbiol Immunol. 2008 Apr;23(2):148-57
pubmed: 18279183
Antimicrob Agents Chemother. 2013 May;57(5):2326-32
pubmed: 23478961
FEMS Microbiol Ecol. 2008 Dec;66(3):637-44
pubmed: 18785881
Circ Res. 2013 Mar 1;112(5):751-4
pubmed: 23449544
J Dent Res. 1964 Jul-Aug;43:626
pubmed: 14183351
Clin Exp Immunol. 2010 Apr;160(1):70-9
pubmed: 20415854
Clin Oral Investig. 2019 Sep;23(9):3571-3580
pubmed: 30554327
Microb Pathog. 2019 Mar;128:405-413
pubmed: 30685363
J Pathol. 2013 Jan;229(2):176-85
pubmed: 23096265
Cell. 2018 May 3;173(4):920-933.e13
pubmed: 29576451
Calcif Tissue Int. 2018 May;102(5):503-511
pubmed: 29589061
Microbiology (Reading). 1996 Jan;142(1):33-39
pubmed: 33657745
J Innate Immun. 2016;8(3):223-7
pubmed: 26836137
J Clin Periodontol. 1998 Feb;25(2):134-44
pubmed: 9495612
J Clin Microbiol. 2013 Sep;51(9):2850-61
pubmed: 23784124
J Appl Oral Sci. 2015 May-Jun;23(3):329-55
pubmed: 26221929
J Biol Chem. 2003 Aug 8;278(32):29880-9
pubmed: 12775723
Hum Mol Genet. 2016 May 15;25(10):2113-2129
pubmed: 26962152
Lancet. 1999 Sep 18;354(9183):1040
pubmed: 10501404
Nat Rev Immunol. 2004 Sep;4(9):699-710
pubmed: 15343369
Proc Natl Acad Sci U S A. 1968 Jan;59(1):296-303
pubmed: 4873344
J Periodontol. 1971 Aug;42(8):485-96
pubmed: 4998039
mBio. 2014 Apr 01;5(2):e01012-14
pubmed: 24692635
Cold Spring Harb Perspect Biol. 2015 Jan 29;7(5):
pubmed: 25635046
Nat Rev Microbiol. 2007 Aug;5(8):647-51
pubmed: 17603517
J Appl Microbiol. 2004;97(6):1311-8
pubmed: 15546422
J Exp Med. 2010 Aug 30;207(9):1907-21
pubmed: 20696699
Curr Opin Immunol. 2012 Aug;24(4):385-91
pubmed: 22613090
Contemp Oncol (Pozn). 2018 Mar;22(1A):56-60
pubmed: 29628795
mBio. 2017 Feb 28;8(1):
pubmed: 28246359
J Oral Microbiol. 2013;5:
pubmed: 23565326
Science. 2012 Jun 8;336(6086):1255-62
pubmed: 22674335
Br Med J. 1930 Jun 14;1(3623):1100-1
pubmed: 20775513
Nat Rev Microbiol. 2013 Apr;11(4):227-38
pubmed: 23435359
Nutr Rev. 2012 Aug;70 Suppl 1:S2-9
pubmed: 22861804
J Clin Microbiol. 2000 Mar;38(3):1196-9
pubmed: 10699021
J Clin Periodontol. 1979 Dec;6(7):16-21
pubmed: 295292
Oral Sci Rev. 1976;9:65-107
pubmed: 1067529
Nat Rev Microbiol. 2011 Apr;9(4):233-43
pubmed: 21358670
Nat Rev Microbiol. 2018 Dec;16(12):745-759
pubmed: 30301974
Science. 2003 Jun 6;300(5625):1584-7
pubmed: 12791997
Periodontol 2000. 2017 Oct;75(1):52-115
pubmed: 28758303
Microb Pathog. 2016 May;94:21-6
pubmed: 26375893
Nat Rev Microbiol. 2010 Apr;8(4):296-307
pubmed: 20234378
Periodontol 2000. 1994 Jun;5:7-25
pubmed: 9673160
PLoS Biol. 2008 Nov 18;6(11):e280
pubmed: 19018661
J Exp Med. 1968 Oct 1;128(4):821-37
pubmed: 5691986
Expert Rev Mol Diagn. 2020 May;20(5):543-555
pubmed: 32223655
Immunol Rev. 2019 Jan;287(1):226-235
pubmed: 30565245
Gastroenterology. 2003 Aug;125(2):364-71
pubmed: 12891537
ISME J. 2014 Aug;8(8):1659-72
pubmed: 24599074
Ann N Y Acad Sci. 2012 Feb;1250:50-5
pubmed: 22276660
Front Microbiol. 2020 Feb 19;11:136
pubmed: 32140140
Clin Microbiol Rev. 2002 Apr;15(2):294-309
pubmed: 11932234
J Dent Res. 2004 Feb;83(2):156-60
pubmed: 14742655
J Immunol. 2000 Nov 15;165(10):5392-6
pubmed: 11067888
Nature. 2011 Aug 28;477(7366):592-5
pubmed: 21874021
Blood. 1995 Jun 1;85(11):3144-9
pubmed: 7756646
Clin Exp Immunol. 2014 Jul;177(1):1-12
pubmed: 24401109
mBio. 2017 Oct 10;8(5):
pubmed: 29018121
Mech Ageing Dev. 2009 Aug;130(8):538-46
pubmed: 19559723
Bioconjug Chem. 2003 May-Jun;14(3):507-12
pubmed: 12757372
J Periodontal Res. 2012 Jun;47(3):389-95
pubmed: 22126530
J Dent Res. 2011 Mar;90(3):294-303
pubmed: 20924061
J Bacteriol. 2005 Nov;187(21):7193-203
pubmed: 16237003
Philos Trans R Soc Lond B Biol Sci. 2015 Apr 19;370(1666):
pubmed: 25750239
Cell. 2006 Feb 24;124(4):695-7
pubmed: 16497580
J Periodontol. 2018 Jun;89 Suppl 1:S173-S182
pubmed: 29926951
Infect Immun. 2015 Jan;83(1):2-7
pubmed: 25385796
ISME J. 2013 May;7(5):1016-25
pubmed: 23303375
PLoS One. 2020 Mar 13;15(3):e0230334
pubmed: 32168352
Ther Clin Risk Manag. 2015 Feb 04;11:171-88
pubmed: 25691810
Nat Commun. 2018 Nov 12;9(1):4753
pubmed: 30420631
Curr Opin Infect Dis. 2019 Oct;32(5):490-496
pubmed: 31356239
J Periodontol. 2014 Aug;85(8):e295-303
pubmed: 24502627
BMC Genomics. 2017 Jan 25;18(Suppl 1):1041
pubmed: 28198672
Annu Rev Immunol. 1983;1:1-32
pubmed: 6399974
PLoS One. 2018 Apr 18;13(4):e0195534
pubmed: 29668720
PLoS One. 2014 Jun 05;9(6):e98541
pubmed: 24901458
Mucosal Immunol. 2016 Sep;9(5):1163-1172
pubmed: 26732676
Front Cell Infect Microbiol. 2019 Apr 24;9:99
pubmed: 31069173
Eur J Immunol. 2008 Dec;38(12):3257-64
pubmed: 19039772
Biotechniques. 1994 Oct;17(4):788-92
pubmed: 7833043
Trends Immunol. 2018 Apr;39(4):276-287
pubmed: 28923364
J Bone Miner Res. 2015 Mar;30(3):412-22
pubmed: 25264308
J Immunol Res. 2017;2017:9671604
pubmed: 28299345
Periodontol 2000. 2020 Feb;82(1):129-142
pubmed: 31850627
Immun Ageing. 2018 Sep 21;15:22
pubmed: 30258468
Evol Med Public Health. 2013 Jan;2013(1):46-64
pubmed: 24481186
Curr Med Res Opin. 2008 Jun;24(6):1635-43
pubmed: 18452645
PLoS Pathog. 2009 Jun;5(6):e1000474
pubmed: 19521507
Nat Rev Rheumatol. 2019 Aug;15(8):491-501
pubmed: 31227819
Arch Oral Biol. 1962 May-Jun;7:267-77
pubmed: 14455466
Nat Rev Genet. 2012 Mar 13;13(4):260-70
pubmed: 22411464
Microbes Infect. 1999 Jul;1(9):709-17
pubmed: 10611748
Dev Psychobiol. 2019 Jul;61(5):739-751
pubmed: 30460694
J Clin Periodontol. 1983 Nov;10(6):563-78
pubmed: 6581173
Expert Rev Clin Immunol. 2014 Aug;10(8):973-5
pubmed: 24931458
Infect Immun. 2014 Aug;82(8):3374-82
pubmed: 24866802
Cold Spring Harb Symp Quant Biol. 1989;54 Pt 1:1-13
pubmed: 2700931
J Immunol. 2005 Mar 15;174(6):3545-50
pubmed: 15749891
Adv Dent Res. 1994 Jul;8(2):263-71
pubmed: 7865085
Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):18525-30
pubmed: 24167272
Trends Microbiol. 2014 May;22(5):261-6
pubmed: 24618403
J Infect Dis. 2016 Dec 1;214(11):1629-1637
pubmed: 27630197
J Clin Periodontol. 2017 Mar;44 Suppl 18:S12-S22
pubmed: 28266111
J Dent Res. 1956 Apr;35(2):323-5
pubmed: 13319560
J Immunol. 2001 Feb 15;166(4):2610-6
pubmed: 11160323
N Engl J Med. 2011 Nov 3;365(18):1693-703
pubmed: 22047560
Front Physiol. 2018 Oct 31;9:1534
pubmed: 30429801
J Immunol. 2009 Jun 15;182(12):7690-7
pubmed: 19494293
J Clin Periodontol. 1987 Nov;14(10):588-93
pubmed: 3320100
Clin Rev Allergy Immunol. 2018 Oct;55(2):107-117
pubmed: 29488131
J Dent Res. 2006 Nov;85(11):990-5
pubmed: 17062737
Lab Invest. 1976 Mar;34(3):235-49
pubmed: 765622
J Bacteriol. 1929 Dec;18(6):395-412
pubmed: 16559404
J Infect Dis. 2002 Sep 15;186(6):798-806
pubmed: 12198614
Oral Microbiol Immunol. 2009 Feb;24(1):1-6
pubmed: 19121062
J Transl Med. 2018 Jan 19;16(1):11
pubmed: 29351798
J Immunol. 1972 Mar;108(3):738-47
pubmed: 4110988
Microbiol Mol Biol Rev. 2002 Sep;66(3):486-505, table of contents
pubmed: 12209001
Pediatr Allergy Immunol. 2002 Dec;13(6):402-11
pubmed: 12485315
Infect Immun. 1999 Aug;67(8):3703-13
pubmed: 10417127
Metabolomics. 2019 Oct 14;15(11):141
pubmed: 31612356
J Clin Periodontol. 2011 Jul;38(7):612-20
pubmed: 21488936
Genome Med. 2015 Apr 27;7(1):27
pubmed: 25918553
Curr Opin Immunol. 2014 Aug;29:16-22
pubmed: 24727150
J Periodontal Res. 1991 May;26(3 Pt 2):195-212
pubmed: 1831843
Infect Immun. 1984 Aug;45(2):356-9
pubmed: 6746094
Arch Pharm Res. 2016 Nov;39(11):1565-1576
pubmed: 27444041
Crit Rev Microbiol. 2013 Aug;39(3):229-46
pubmed: 22866947
J Proteomics. 2020 Feb 20;213:103602
pubmed: 31809901
Science. 2011 Jan 21;331(6015):337-41
pubmed: 21205640
Nature. 2001 Aug 16;412(6848):701-5
pubmed: 11507631
Cell Host Microbe. 2019 Aug 14;26(2):228-239.e8
pubmed: 31378677
Nature. 2008 May 29;453(7195):620-5
pubmed: 18509436
PLoS One. 2013 Aug 19;8(8):e72047
pubmed: 23977202
ISME J. 2012 Jun;6(6):1176-85
pubmed: 22170420
J Leukoc Biol. 2019 Jul;106(1):193-200
pubmed: 30776147
Br Med J. 1900 Jul 28;2(2065):215-6
pubmed: 20759127
Genome Med. 2016 Apr 27;8(1):51
pubmed: 27122046
Arthritis Res Ther. 2011;13(5):R168
pubmed: 22008667
Annu Rev Pathol. 2011;6:121-45
pubmed: 20936937
FASEB J. 1998 Apr;12(6):433-7
pubmed: 9535215
Annu Rev Microbiol. 2000;54:413-37
pubmed: 11018133
Front Immunol. 2019 Oct 25;10:2441
pubmed: 31749793
Sci Rep. 2018 Apr 3;8(1):5443
pubmed: 29615691
Periodontol 2000. 2020 Jun;83(1):14-25
pubmed: 32385883
Mayo Clin Proc. 2017 Apr;92(4):599-604
pubmed: 28209367
J Calif Dent Assoc. 2016 Jul;44(7):421-35
pubmed: 27514154
J Am Dent Assoc. 1960 Jul;61:9-19
pubmed: 13823312
Biochimie. 2011 Feb;93(2):296-305
pubmed: 20937352
J Infect Dis. 2011 May 15;203(10):1415-24
pubmed: 21398396
J Immunol. 2002 Jul 1;169(1):10-4
pubmed: 12077222
Nat Med. 2010 Feb;16(2):228-31
pubmed: 20081863
J Periodontol. 2016 Dec;87(12):1499-1507
pubmed: 27389962
ISME J. 2020 May;14(5):1154-1169
pubmed: 32020052
Microbiol Mol Biol Rev. 1998 Dec;62(4):1157-70
pubmed: 9841668
Mol Aspects Med. 2017 Dec;58:21-36
pubmed: 28483532
Z Rheumatol. 2016 Aug;75(6):531-3
pubmed: 27444621
Pathog Dis. 2016 Apr;74(3):
pubmed: 26884502
J Periodontol. 2009 Sep;80(9):1421-32
pubmed: 19722792
Arch Oral Biol. 1985;30(4):319-24
pubmed: 3857902
Periodontol 2000. 2003;31:55-76
pubmed: 12656996
Proc (Bayl Univ Med Cent). 2005 Jan;18(1):21-5
pubmed: 16200144
Cell. 2014 Aug 14;158(4):705-721
pubmed: 25126780
J Immunol. 2001 Oct 15;167(8):4693-700
pubmed: 11591800
J Can Dent Assoc. 2003 Dec;69(11):722-4
pubmed: 14653937
Trends Mol Med. 2015 Feb;21(2):109-17
pubmed: 25578246
J Periodontal Res. 1967;2(4):282-9
pubmed: 4249983
Periodontol 2000. 1995 Jun;8:87-107
pubmed: 9567948
J Clin Periodontol. 2016 Nov;43(11):889-900
pubmed: 27440507
Front Cell Infect Microbiol. 2017 Mar 28;7:97
pubmed: 28401067
Nutrition. 2008 Apr;24(4):348-59
pubmed: 18262391
J Cell Biochem. 2014 Aug;115(8):1412-9
pubmed: 24700654
Trends Mol Med. 2015 Mar;21(3):172-83
pubmed: 25498392
J Bacteriol. 2010 Oct;192(19):5002-17
pubmed: 20656903
Nutrients. 2019 Sep 06;11(9):
pubmed: 31489949
Yonago Acta Med. 2018 Mar 28;61(1):8-18
pubmed: 29599617
Pol Arch Med Wewn. 2013;123(6):309-13
pubmed: 23828150
Sci Rep. 2014 Aug 01;4:5922
pubmed: 25082483
Periodontol 2000. 1994 Jun;5:66-77
pubmed: 9673163
Adv Exp Med Biol. 1978;107:185-92
pubmed: 742482
Sci Transl Med. 2018 Oct 17;10(463):
pubmed: 30333238
Microbes Infect. 2009 Apr;11(5):625-30
pubmed: 19371791
World J Gastroenterol. 2017 Jun 14;23(22):3964-3977
pubmed: 28652651
J Exp Med. 1968 Oct 1;128(4):801-20
pubmed: 5691985
J Clin Immunol. 2010 May;30(3):373-83
pubmed: 20182777
Proc Jpn Acad Ser B Phys Biol Sci. 2015;91(8):423-39
pubmed: 26460320
Environ Microbiol. 2015 Mar;17(3):699-710
pubmed: 24800728
PLoS One. 2014 Mar 27;9(3):e92940
pubmed: 24675997
Microorganisms. 2020 Nov 13;8(11):
pubmed: 33202844
Curr Opin Gastroenterol. 2008 Nov;24(6):713-9
pubmed: 19122521
J Immunol. 2010 Mar 1;184(5):2355-68
pubmed: 20118281
J Am Dent Assoc. 1996 May;127(5):641-2, 645-6
pubmed: 8642144
Nat Rev Microbiol. 2003 Oct;1(1):17-24
pubmed: 15040176
Vaccine. 2012 Mar 9;30(12):2060-7
pubmed: 22289511
ISME J. 2018 May;12(5):1210-1224
pubmed: 29339824
J Bacteriol. 2008 May;190(10):3646-57
pubmed: 18359813
Oral Dis. 2019 Jan;25(1):265-273
pubmed: 30285304
Cell. 2013 Dec 19;155(7):1451-63
pubmed: 24315484
Infect Immun. 2012 Jan;80(1):62-73
pubmed: 22006564
J Proteomics. 2018 Oct 30;189:1-10
pubmed: 29476807
Nat Rev Immunol. 2017 Sep;17(9):532
pubmed: 28555672
J Oral Microbiol. 2014 Feb 25;6:
pubmed: 24578801
Nat Rev Immunol. 2009 May;9(5):313-23
pubmed: 19343057
BMC Biol. 2019 Sep 18;17(1):76
pubmed: 31533707
PLoS Pathog. 2015 Mar 05;11(3):e1004698
pubmed: 25741691
Adv Exp Med Biol. 1995;371A:97-101
pubmed: 8526027
Cell Microbiol. 2014 Jul;16(7):1024-33
pubmed: 24798552
Immunity. 2006 May;24(5):495-9
pubmed: 16713964
Annu Rev Phytopathol. 2017 Aug 4;55:109-137
pubmed: 28525309
Nat Rev Microbiol. 2009 Nov;7(11):787-97
pubmed: 19806153
J Immunol. 2002 Sep 15;169(6):3155-62
pubmed: 12218133
Caries Res. 2016;50(4):422-31
pubmed: 27458979
J Immunol. 2020 Feb 1;204(3):671-681
pubmed: 31871022
Trends Immunol. 2018 Nov;39(11):937-950
pubmed: 30293747
Clin Infect Dis. 1993 Jun;16 Suppl 4:S203-10
pubmed: 8324120
Mol Oral Microbiol. 2010 Aug;25(4):275-92
pubmed: 20618701
Nat Med. 2003 May;9(5):525-32
pubmed: 12692544
Periodontol 2000. 2016 Oct;72(1):54-75
pubmed: 27501491
PLoS Pathog. 2019 Nov 14;15(11):e1008058
pubmed: 31725797
J Innate Immun. 2018;10(5-6):432-441
pubmed: 29642066
Invest Ophthalmol Vis Sci. 2011 Jun 09;52(7):4106-12
pubmed: 21296813
Eur J Immunol. 2004 Apr;34(4):913-20
pubmed: 15048701
J Dent Res. 2015 Jul;94(7):921-7
pubmed: 25904141
J Dent Res. 2009 Nov;88(11):982-90
pubmed: 19828884
Nature. 2017 Aug 2;548(7665):43-51
pubmed: 28770836

Auteurs

Carla Cugini (C)

Department of Oral Biology, Rutgers School of Dental Medicine, Newark, NJ, United States.

Narayanan Ramasubbu (N)

Department of Oral Biology, Rutgers School of Dental Medicine, Newark, NJ, United States.

Vincent K Tsiagbe (VK)

Department of Oral Biology, Rutgers School of Dental Medicine, Newark, NJ, United States.

Daniel H Fine (DH)

Department of Oral Biology, Rutgers School of Dental Medicine, Newark, NJ, United States.

Classifications MeSH