Activation of RANKL-induced osteoclasts and memory T lymphocytes by Porphyromonas gingivalis is serotype dependant

Aim Destructive periodontitis is associated with a Th1–Th17 immune response and activation of RANKL‐induced osteoclasts. In addition, Porphyromonas gingivalis K1 and K2 serotypes induce a strong Th1–Th17 response. This study aimed to investigate whether these P. gingivalis serotypes induce higher os...

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Published inJournal of clinical periodontology Vol. 41; no. 5; pp. 451 - 459
Main Authors Vernal, Rolando, Díaz-Zúñiga, Jaime, Melgar-Rodríguez, Samanta, Pujol, Myriam, Diaz-Guerra, Eva, Silva, Augusto, Sanz, Mariano, Garcia-Sanz, Jose A.
Format Journal Article
LanguageEnglish
Published United States Blackwell Publishing Ltd 01.05.2014
Subjects
Acid Phosphatase - analysis
Acid Phosphatase - immunology
Animals
Antigens
Antigens, Bacterial - immunology
bone resorption
CD4-Positive T-Lymphocytes - immunology
CD4-Positive T-Lymphocytes - microbiology
Cell Differentiation - immunology
Cell Line
Chronic Periodontitis - immunology
Clonal Selection, Antigen-Mediated
Dendritic Cells - immunology
Dentistry
Forkhead Transcription Factors - analysis
GATA3 Transcription Factor - analysis
Gum disease
Humans
Immunologic Memory - immunology
Isoenzymes - analysis
Isoenzymes - immunology
Lymphocytes
Macrophages - immunology
Mice
Nuclear Receptor Subfamily 1, Group F, Member 3 - analysis
Osteoclasts - drug effects
Osteoclasts - immunology
Pathogenesis
periodontitis
Porphyromonas gingivalis
Porphyromonas gingivalis - classification
Porphyromonas gingivalis - immunology
RANK Ligand - analysis
RANK Ligand - immunology
RANKL
Serogroup
serotypes
T lymphocytes
T-Box Domain Proteins - analysis
T-Lymphocytes - immunology
T-Lymphocytes - microbiology
Tartrate-Resistant Acid Phosphatase
Th1 Cells - immunology
Th17 Cells - immunology
Porphyromonas gingivalis
T lymphocytes
RANKL
serotypes
bone resorption
periodontitis
Online AccessGet full text
ISSN0303-6979
1600-051X
1600-051X
DOI10.1111/jcpe.12236

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Abstract Aim Destructive periodontitis is associated with a Th1–Th17 immune response and activation of RANKL‐induced osteoclasts. In addition, Porphyromonas gingivalis K1 and K2 serotypes induce a strong Th1–Th17 response. This study aimed to investigate whether these P. gingivalis serotypes induce higher osteoclasts activation, by increased Th17‐associated RANKL production, and an antigen‐specific memory T‐lymphocyte response. Material and Methods The RANKL production and TRAP+ osteoclast induction were quantified on naïve T lymphocytes stimulated with dendritic cells primed with the P. gingivalis serotypes. The T‐bet, GATA‐3, RORC2 and Foxp3 expression was correlated with RANKL production. The frequency of proliferating memory T lymphocytes in response to P. gingivalis serotypes was determined in both periodontitis and healthy subjects. Results T lymphocytes stimulated by K1 or K2‐primed dendritic cells elicited higher levels of RANKL and TRAP+ osteoclasts than cells stimulated with the other serotypes. RANKL positively correlated with RORC2. Whereas periodontitis patients had a higher frequency of memory T lymphocytes responding to K1 or K2, healthy subjects had a higher frequency of memory T lymphocytes responding to K4 or K−. Conclusions P. gingivalis serotypes K1 and K2, but not others, are associated with an increased production of the osteoclastogenesis‐related factor RANKL. This important information suggests that these serotypes could elicit a greater bone resorption in vivo and have a role in the periodontitis pathogenesis.
AbstractList Destructive periodontitis is associated with a Th1-Th17 immune response and activation of RANKL-induced osteoclasts. In addition, Porphyromonas gingivalis K1 and K2 serotypes induce a strong Th1-Th17 response. This study aimed to investigate whether these P. gingivalis serotypes induce higher osteoclasts activation, by increased Th17-associated RANKL production, and an antigen-specific memory T-lymphocyte response. The RANKL production and TRAP(+) osteoclast induction were quantified on naïve T lymphocytes stimulated with dendritic cells primed with the P. gingivalis serotypes. The T-bet, GATA-3, RORC2 and Foxp3 expression was correlated with RANKL production. The frequency of proliferating memory T lymphocytes in response to P. gingivalis serotypes was determined in both periodontitis and healthy subjects. T lymphocytes stimulated by K1 or K2-primed dendritic cells elicited higher levels of RANKL and TRAP(+) osteoclasts than cells stimulated with the other serotypes. RANKL positively correlated with RORC2. Whereas periodontitis patients had a higher frequency of memory T lymphocytes responding to K1 or K2, healthy subjects had a higher frequency of memory T lymphocytes responding to K4 or K(-) . P. gingivalis serotypes K1 and K2, but not others, are associated with an increased production of the osteoclastogenesis-related factor RANKL. This important information suggests that these serotypes could elicit a greater bone resorption in vivo and have a role in the periodontitis pathogenesis.
Aim Destructive periodontitis is associated with a Th1–Th17 immune response and activation of RANKL‐induced osteoclasts. In addition, Porphyromonas gingivalis K1 and K2 serotypes induce a strong Th1–Th17 response. This study aimed to investigate whether these P. gingivalis serotypes induce higher osteoclasts activation, by increased Th17‐associated RANKL production, and an antigen‐specific memory T‐lymphocyte response. Material and Methods The RANKL production and TRAP+ osteoclast induction were quantified on naïve T lymphocytes stimulated with dendritic cells primed with the P. gingivalis serotypes. The T‐bet, GATA‐3, RORC2 and Foxp3 expression was correlated with RANKL production. The frequency of proliferating memory T lymphocytes in response to P. gingivalis serotypes was determined in both periodontitis and healthy subjects. Results T lymphocytes stimulated by K1 or K2‐primed dendritic cells elicited higher levels of RANKL and TRAP+ osteoclasts than cells stimulated with the other serotypes. RANKL positively correlated with RORC2. Whereas periodontitis patients had a higher frequency of memory T lymphocytes responding to K1 or K2, healthy subjects had a higher frequency of memory T lymphocytes responding to K4 or K−. Conclusions P. gingivalis serotypes K1 and K2, but not others, are associated with an increased production of the osteoclastogenesis‐related factor RANKL. This important information suggests that these serotypes could elicit a greater bone resorption in vivo and have a role in the periodontitis pathogenesis.
Aim Destructive periodontitis is associated with a Th1-Th17 immune response and activation of RANKL-induced osteoclasts. In addition, Porphyromonas gingivalis K1 and K2 serotypes induce a strong Th1-Th17 response. This study aimed to investigate whether these P. gingivalis serotypes induce higher osteoclasts activation, by increased Th17-associated RANKL production, and an antigen-specific memory T-lymphocyte response. Material and Methods The RANKL production and TRAP+ osteoclast induction were quantified on naïve T lymphocytes stimulated with dendritic cells primed with the P. gingivalis serotypes. The T-bet, GATA-3, RORC2 and Foxp3 expression was correlated with RANKL production. The frequency of proliferating memory T lymphocytes in response to P. gingivalis serotypes was determined in both periodontitis and healthy subjects. Results T lymphocytes stimulated by K1 or K2-primed dendritic cells elicited higher levels of RANKL and TRAP+ osteoclasts than cells stimulated with the other serotypes. RANKL positively correlated with RORC2. Whereas periodontitis patients had a higher frequency of memory T lymphocytes responding to K1 or K2, healthy subjects had a higher frequency of memory T lymphocytes responding to K4 or K-. Conclusions P. gingivalis serotypes K1 and K2, but not others, are associated with an increased production of the osteoclastogenesis-related factor RANKL. This important information suggests that these serotypes could elicit a greater bone resorption in vivo and have a role in the periodontitis pathogenesis. [PUBLICATION ABSTRACT]
Destructive periodontitis is associated with a Th1-Th17 immune response and activation of RANKL-induced osteoclasts. In addition, Porphyromonas gingivalis K1 and K2 serotypes induce a strong Th1-Th17 response. This study aimed to investigate whether these P. gingivalis serotypes induce higher osteoclasts activation, by increased Th17-associated RANKL production, and an antigen-specific memory T-lymphocyte response.AIMDestructive periodontitis is associated with a Th1-Th17 immune response and activation of RANKL-induced osteoclasts. In addition, Porphyromonas gingivalis K1 and K2 serotypes induce a strong Th1-Th17 response. This study aimed to investigate whether these P. gingivalis serotypes induce higher osteoclasts activation, by increased Th17-associated RANKL production, and an antigen-specific memory T-lymphocyte response.The RANKL production and TRAP(+) osteoclast induction were quantified on naïve T lymphocytes stimulated with dendritic cells primed with the P. gingivalis serotypes. The T-bet, GATA-3, RORC2 and Foxp3 expression was correlated with RANKL production. The frequency of proliferating memory T lymphocytes in response to P. gingivalis serotypes was determined in both periodontitis and healthy subjects.MATERIAL AND METHODSThe RANKL production and TRAP(+) osteoclast induction were quantified on naïve T lymphocytes stimulated with dendritic cells primed with the P. gingivalis serotypes. The T-bet, GATA-3, RORC2 and Foxp3 expression was correlated with RANKL production. The frequency of proliferating memory T lymphocytes in response to P. gingivalis serotypes was determined in both periodontitis and healthy subjects.T lymphocytes stimulated by K1 or K2-primed dendritic cells elicited higher levels of RANKL and TRAP(+) osteoclasts than cells stimulated with the other serotypes. RANKL positively correlated with RORC2. Whereas periodontitis patients had a higher frequency of memory T lymphocytes responding to K1 or K2, healthy subjects had a higher frequency of memory T lymphocytes responding to K4 or K(-) .RESULTST lymphocytes stimulated by K1 or K2-primed dendritic cells elicited higher levels of RANKL and TRAP(+) osteoclasts than cells stimulated with the other serotypes. RANKL positively correlated with RORC2. Whereas periodontitis patients had a higher frequency of memory T lymphocytes responding to K1 or K2, healthy subjects had a higher frequency of memory T lymphocytes responding to K4 or K(-) .P. gingivalis serotypes K1 and K2, but not others, are associated with an increased production of the osteoclastogenesis-related factor RANKL. This important information suggests that these serotypes could elicit a greater bone resorption in vivo and have a role in the periodontitis pathogenesis.CONCLUSIONSP. gingivalis serotypes K1 and K2, but not others, are associated with an increased production of the osteoclastogenesis-related factor RANKL. This important information suggests that these serotypes could elicit a greater bone resorption in vivo and have a role in the periodontitis pathogenesis.
Destructive periodontitis is associated with a Th1-Th17 immune response and activation of RANKL-induced osteoclasts. In addition, Porphyromonas gingivalis K1 and K2 serotypes induce a strong Th1-Th17 response. This study aimed to investigate whether these P. gingivalis serotypes induce higher osteoclasts activation, by increased Th17-associated RANKL production, and an antigen-specific memory T-lymphocyte response. The RANKL production and TRAP+ osteoclast induction were quantified on naive T lymphocytes stimulated with dendritic cells primed with the P. gingivalis serotypes. The T-bet, GATA-3, RORC2 and Foxp3 expression was correlated with RANKL production. The frequency of proliferating memory T lymphocytes in response to P. gingivalis serotypes was determined in both periodontitis and healthy subjects. T lymphocytes stimulated by K1 or K2-primed dendritic cells elicited higher levels of RANKL and TRAP+ osteoclasts than cells stimulated with the other serotypes. RANKL positively correlated with RORC2. Whereas periodontitis patients had a higher frequency of memory T lymphocytes responding to K1 or K2, healthy subjects had a higher frequency of memory T lymphocytes responding to K4 or K-. P. gingivalis serotypes K1 and K2, but not others, are associated with an increased production of the osteoclastogenesis-related factor RANKL. This important information suggests that these serotypes could elicit a greater bone resorption in vivo and have a role in the periodontitis pathogenesis.
Author Garcia-Sanz, Jose A.
Vernal, Rolando
Silva, Augusto
Melgar-Rodríguez, Samanta
Sanz, Mariano
Díaz-Zúñiga, Jaime
Diaz-Guerra, Eva
Pujol, Myriam
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  surname: Díaz-Zúñiga
  fullname: Díaz-Zúñiga, Jaime
  organization: Periodontal Biology Laboratory, Department of Conservative Dentistry, Dental School, Universidad de Chile, Santiago de Chile, Chile
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  surname: Melgar-Rodríguez
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  organization: Department of Cellular and Molecular Medicine, Centro de Investigaciones Biológicas (CIB-CSIC), Madrid, Spain
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  email: Address:Jose A. Garcia-SanzCentro de Investigaciones Biológicas (CIB-CSIC)Ramiro de Maeztu 9E-28040 MadridSpain., jasanz@cib.csic.es
  organization: Department of Cellular and Molecular Medicine, Centro de Investigaciones Biológicas (CIB-CSIC), Madrid, Spain
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Issue 5
Keywords Porphyromonas gingivalis
T lymphocytes
RANKL
serotypes
bone resorption
periodontitis
Language English
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2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
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Spanish Ministry of Science and Technology - No. SAF2009-07974
Chilean Government - No. FONDECYT 11100298
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Spanish National Research Council - No. PIE200420E240; No. PIE200420E586
Instituto de Salud Carlos III - No. RD06/0010/1010
Conflict of interest and source of funding statement
The authors declare that they have no conflict of interests. The research in our laboratories has been supported by grants from the Spanish Ministry of Science and Technology (SAF2009‐07974), Instituto de Salud Carlos III (RD06/0010/1010), Spanish National Research Council (PIE200420E240 and PIE200420E586) and Chilean Government (FONDECYT 11100298).
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OpenAccessLink https://repositorio.uchile.cl/handle/2250/158943
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PublicationDate May 2014
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  year: 2014
  text: May 2014
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PublicationPlace United States
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PublicationTitle Journal of clinical periodontology
PublicationTitleAlternate J Clin Periodontol
PublicationYear 2014
Publisher Blackwell Publishing Ltd
Publisher_xml – name: Blackwell Publishing Ltd
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Lacey, D. L., Timms, E., Tan, H. L., Kelley, M. J., Dunstan, C. R., Burgess, T., Elliott, R., Colombero, A., Elliott, G., Scully, S., Hsu, H., Sullivan, J., Hawkins, N., Davy, E., Capparelli, C., Eli, A., Qian, Y. X., Kaufman, S., Sarosi, I., Shalhoub, V., Senaldi, G., Guo, J., Delaney, J. & Boyle, W. J. (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93, 165-176.
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Hernandez, M., Dutzan, N., Garcia-Sesnich, J., Abusleme, L., Dezerega, A., Silva, N., Gonzalez, F. E., Vernal, R., Sorsa, T. & Gamonal, J. (2011) Host-pathogen interactions in progressive chronic periodontitis. Journal of Dental Research 90, 1164-1170.
Laine, M. L. & van Winkelhoff, A. J. (1998) Virulence of six capsular serotypes of Porphyromonas gingivalis in a mouse model. Oral Microbiology and Immunology 13, 322-325.
Toraldo, G., Roggia, C., Qian, W. P., Pacifici, R. & Weitzmann, M. N. (2003) IL-7 induces bone loss in vivo by induction of receptor activator of nuclear factor kappa B ligand and tumor necrosis factor alpha from T cells. Proceedings of the National Academy of Sciences of the United States of America 100, 125-130.
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References_xml – reference: Crotti, T., Smith, M. D., Hirsch, R., Soukoulis, S., Weedon, H., Capone, M., Ahern, M. J. & Haynes, D. (2003) Receptor activator NF kappaB ligand (RANKL) and osteoprotegerin (OPG) protein expression in periodontitis. Journal of Periodontal Research 38, 380-387.
– reference: Farquharson, S. I., Germaine, G. R. & Gray, G. R. (2000) Isolation and characterization of the cell-surface polysaccharides of Porphyromonas gingivalis ATCC 53978. Oral Microbiology and Immunology 15, 151-157.
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– reference: Herath, T. D., Darveau, R. P., Seneviratne, C. J., Wang, C. Y., Wang, Y. & Jin, L. (2013) Tetra- and penta-acylated lipid A structures of Porphyromonas gingivalis LPS differentially activate TLR4-mediated NF-kappaB signal transduction cascade and immuno-inflammatory response in human gingival fibroblasts. PLoS ONE 8, e58496.
– reference: Laine, M. L. & van Winkelhoff, A. J. (1998) Virulence of six capsular serotypes of Porphyromonas gingivalis in a mouse model. Oral Microbiology and Immunology 13, 322-325.
– reference: Dutzan, N., Gamonal, J., Silva, A., Sanz, M. & Vernal, R. (2009a) Over-expression of forkhead box P3 and its association with receptor activator of nuclear factor-kappa B ligand, interleukin (IL)-17, IL-10 and transforming growth factor-beta during the progression of chronic periodontitis. Journal of Clinical Periodontology 36, 396-403.
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Snippet Aim Destructive periodontitis is associated with a Th1–Th17 immune response and activation of RANKL‐induced osteoclasts. In addition, Porphyromonas gingivalis...
Destructive periodontitis is associated with a Th1-Th17 immune response and activation of RANKL-induced osteoclasts. In addition, Porphyromonas gingivalis K1...
Aim Destructive periodontitis is associated with a Th1-Th17 immune response and activation of RANKL-induced osteoclasts. In addition, Porphyromonas gingivalis...
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SubjectTerms Acid Phosphatase - analysis
Acid Phosphatase - immunology
Animals
Antigens
Antigens, Bacterial - immunology
bone resorption
CD4-Positive T-Lymphocytes - immunology
CD4-Positive T-Lymphocytes - microbiology
Cell Differentiation - immunology
Cell Line
Chronic Periodontitis - immunology
Clonal Selection, Antigen-Mediated
Dendritic Cells - immunology
Dentistry
Forkhead Transcription Factors - analysis
GATA3 Transcription Factor - analysis
Gum disease
Humans
Immunologic Memory - immunology
Isoenzymes - analysis
Isoenzymes - immunology
Lymphocytes
Macrophages - immunology
Mice
Nuclear Receptor Subfamily 1, Group F, Member 3 - analysis
Osteoclasts - drug effects
Osteoclasts - immunology
Pathogenesis
periodontitis
Porphyromonas gingivalis
Porphyromonas gingivalis - classification
Porphyromonas gingivalis - immunology
RANK Ligand - analysis
RANK Ligand - immunology
RANKL
Serogroup
serotypes
T lymphocytes
T-Box Domain Proteins - analysis
T-Lymphocytes - immunology
T-Lymphocytes - microbiology
Tartrate-Resistant Acid Phosphatase
Th1 Cells - immunology
Th17 Cells - immunology
Title Activation of RANKL-induced osteoclasts and memory T lymphocytes by Porphyromonas gingivalis is serotype dependant
URI https://api.istex.fr/ark:/67375/WNG-2L17JSZZ-D/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fjcpe.12236
https://www.ncbi.nlm.nih.gov/pubmed/24476556
https://www.proquest.com/docview/1513260648
https://www.proquest.com/docview/1514429197
https://www.proquest.com/docview/1520383508
Volume 41
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