Intermediate and Transitory Inflammation Mediate Proper Alveolar Bone Healing Outcome in Contrast to Extreme Low/High Responses: Evidence from Mice Strains Selected for Distinct Inflammatory Phenotypes

Alveolar bone healing is influenced by various local and systemic factors, including the local inflammatory response. This study aimed to evaluate the role of inflammatory responsiveness in alveolar bone healing using 8-week-old male and female mice (N = 5/time/group) strains selected for maximum (A...

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Main Authors: Priscila Maria Colavite, Michelle de Campos Soriani Azevedo, Carolina Fávaro Francisconi, Angélica Cristina Fonseca, André Petenucci Tabanez, Jéssica Lima Melchiades, Daniela Carignatto Passadori, Andrea Borrego, Marcelo De Franco, Ana Paula Favaro Trombone, Gustavo Pompermaier Garlet
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Biology
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Online Access:https://www.mdpi.com/2079-7737/13/12/972
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author Priscila Maria Colavite
Michelle de Campos Soriani Azevedo
Carolina Fávaro Francisconi
Angélica Cristina Fonseca
André Petenucci Tabanez
Jéssica Lima Melchiades
Daniela Carignatto Passadori
Andrea Borrego
Marcelo De Franco
Ana Paula Favaro Trombone
Gustavo Pompermaier Garlet
author_facet Priscila Maria Colavite
Michelle de Campos Soriani Azevedo
Carolina Fávaro Francisconi
Angélica Cristina Fonseca
André Petenucci Tabanez
Jéssica Lima Melchiades
Daniela Carignatto Passadori
Andrea Borrego
Marcelo De Franco
Ana Paula Favaro Trombone
Gustavo Pompermaier Garlet
author_sort Priscila Maria Colavite
collection DOAJ
description Alveolar bone healing is influenced by various local and systemic factors, including the local inflammatory response. This study aimed to evaluate the role of inflammatory responsiveness in alveolar bone healing using 8-week-old male and female mice (N = 5/time/group) strains selected for maximum (AIRmax) or minimum (AIRmin) acute inflammatory response carrying distinct homozygous RR/SS <i>Slc11a1</i> genotypes, namely AIRminRR, AIRminSS, AIRmaxRR, and AIRmaxSS mice. After upper right incisor extraction, bone healing was analyzed at 0, 3, 7, and 14 days using micro-computed tomography, histomorphometry, birefringence, immunohistochemistry, and PCRArray analysis. AIRmaxSS and AIRminRR presented the highest and lowest inflammatory readouts, respectively, associated with lowest repair levels in both strains, while intermediate inflammatory phenotypes observed in AIRminSS and AIRmaxRR were associated with higher repair levels in such strains. The better healing outcomes are associated with intermediate inflammatory cell counts, a balanced expression of pro- and anti-inflammatory cytokines and chemokines, increased expression of growth and osteogenic factors and MSCs markers. Our results demonstrate that extreme high and low inflammatory responses are not ideal for a proper bone repair outcome, while an intermediate and transitory inflammation is associated with a proper alveolar bone healing outcome.
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spelling doaj-art-2ed53b185ab341cfa3c5babc5e3450142024-12-27T14:11:53ZengMDPI AGBiology2079-77372024-11-01131297210.3390/biology13120972Intermediate and Transitory Inflammation Mediate Proper Alveolar Bone Healing Outcome in Contrast to Extreme Low/High Responses: Evidence from Mice Strains Selected for Distinct Inflammatory PhenotypesPriscila Maria Colavite0Michelle de Campos Soriani Azevedo1Carolina Fávaro Francisconi2Angélica Cristina Fonseca3André Petenucci Tabanez4Jéssica Lima Melchiades5Daniela Carignatto Passadori6Andrea Borrego7Marcelo De Franco8Ana Paula Favaro Trombone9Gustavo Pompermaier Garlet10Department of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Al. Octávio Pinheiro Brisola, 9-75, Bauru CEP 17012-901, SP, BrazilDepartment of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Al. Octávio Pinheiro Brisola, 9-75, Bauru CEP 17012-901, SP, BrazilDepartment of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Al. Octávio Pinheiro Brisola, 9-75, Bauru CEP 17012-901, SP, BrazilDepartment of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Al. Octávio Pinheiro Brisola, 9-75, Bauru CEP 17012-901, SP, BrazilDepartment of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Al. Octávio Pinheiro Brisola, 9-75, Bauru CEP 17012-901, SP, BrazilDepartment of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Al. Octávio Pinheiro Brisola, 9-75, Bauru CEP 17012-901, SP, BrazilDepartment of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Al. Octávio Pinheiro Brisola, 9-75, Bauru CEP 17012-901, SP, BrazilLaboratory of Immunogenetics, Butantan Institute, Secretary of Health, Government of the State of São Paulo, Sao Paulo CEP 05503-900, SP, BrazilLaboratory of Immunogenetics, Butantan Institute, Secretary of Health, Government of the State of São Paulo, Sao Paulo CEP 05503-900, SP, BrazilDepartment of Health Science, Universidade do Sagrado Coração, Bauru CEP 17011-160, SP, BrazilDepartment of Biological Sciences, Bauru School of Dentistry, University of São Paulo, Al. Octávio Pinheiro Brisola, 9-75, Bauru CEP 17012-901, SP, BrazilAlveolar bone healing is influenced by various local and systemic factors, including the local inflammatory response. This study aimed to evaluate the role of inflammatory responsiveness in alveolar bone healing using 8-week-old male and female mice (N = 5/time/group) strains selected for maximum (AIRmax) or minimum (AIRmin) acute inflammatory response carrying distinct homozygous RR/SS <i>Slc11a1</i> genotypes, namely AIRminRR, AIRminSS, AIRmaxRR, and AIRmaxSS mice. After upper right incisor extraction, bone healing was analyzed at 0, 3, 7, and 14 days using micro-computed tomography, histomorphometry, birefringence, immunohistochemistry, and PCRArray analysis. AIRmaxSS and AIRminRR presented the highest and lowest inflammatory readouts, respectively, associated with lowest repair levels in both strains, while intermediate inflammatory phenotypes observed in AIRminSS and AIRmaxRR were associated with higher repair levels in such strains. The better healing outcomes are associated with intermediate inflammatory cell counts, a balanced expression of pro- and anti-inflammatory cytokines and chemokines, increased expression of growth and osteogenic factors and MSCs markers. Our results demonstrate that extreme high and low inflammatory responses are not ideal for a proper bone repair outcome, while an intermediate and transitory inflammation is associated with a proper alveolar bone healing outcome.https://www.mdpi.com/2079-7737/13/12/972bone repairinflammation<i>Slc11a1</i>
spellingShingle Priscila Maria Colavite
Michelle de Campos Soriani Azevedo
Carolina Fávaro Francisconi
Angélica Cristina Fonseca
André Petenucci Tabanez
Jéssica Lima Melchiades
Daniela Carignatto Passadori
Andrea Borrego
Marcelo De Franco
Ana Paula Favaro Trombone
Gustavo Pompermaier Garlet
Intermediate and Transitory Inflammation Mediate Proper Alveolar Bone Healing Outcome in Contrast to Extreme Low/High Responses: Evidence from Mice Strains Selected for Distinct Inflammatory Phenotypes
Biology
bone repair
inflammation
<i>Slc11a1</i>
title Intermediate and Transitory Inflammation Mediate Proper Alveolar Bone Healing Outcome in Contrast to Extreme Low/High Responses: Evidence from Mice Strains Selected for Distinct Inflammatory Phenotypes
title_full Intermediate and Transitory Inflammation Mediate Proper Alveolar Bone Healing Outcome in Contrast to Extreme Low/High Responses: Evidence from Mice Strains Selected for Distinct Inflammatory Phenotypes
title_fullStr Intermediate and Transitory Inflammation Mediate Proper Alveolar Bone Healing Outcome in Contrast to Extreme Low/High Responses: Evidence from Mice Strains Selected for Distinct Inflammatory Phenotypes
title_full_unstemmed Intermediate and Transitory Inflammation Mediate Proper Alveolar Bone Healing Outcome in Contrast to Extreme Low/High Responses: Evidence from Mice Strains Selected for Distinct Inflammatory Phenotypes
title_short Intermediate and Transitory Inflammation Mediate Proper Alveolar Bone Healing Outcome in Contrast to Extreme Low/High Responses: Evidence from Mice Strains Selected for Distinct Inflammatory Phenotypes
title_sort intermediate and transitory inflammation mediate proper alveolar bone healing outcome in contrast to extreme low high responses evidence from mice strains selected for distinct inflammatory phenotypes
topic bone repair
inflammation
<i>Slc11a1</i>
url https://www.mdpi.com/2079-7737/13/12/972
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