Role of Fibroblast Populations in Periodontal Wound Healing and Tissue Remodeling

After injury to periodontal tissues, a sequentially phased healing response is initiated that enables wound closure and partial restoration of tissue structure and function. Wound closure in periodontal tissues involves the tightly regulated coordination of resident cells in epithelial and connectiv...

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Published inFrontiers in physiology Vol. 10; p. 270
Main Authors Smith, Patricio C., Martínez, Constanza, Martínez, Jorge, McCulloch, Christopher A.
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 24.04.2019
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Abstract After injury to periodontal tissues, a sequentially phased healing response is initiated that enables wound closure and partial restoration of tissue structure and function. Wound closure in periodontal tissues involves the tightly regulated coordination of resident cells in epithelial and connective tissue compartments. Multiple cell populations in these compartments synergize their metabolic activities to reestablish a mucosal seal that involves the underlying periodontal connective tissues and the attachment of these tissues to the tooth surface. The formation of an impermeable seal around the circumference of the tooth is of particular significance in oral health since colonization of tooth surfaces by pathogenic biofilms promotes inflammation, which can contribute to periodontal tissue degradation and tooth loss. The reformation of periodontal tissue structures in the healing response centrally involves fibroblasts, which synthesize and organize the collagen fibers that link alveolar bone and gingiva to the cementum covering the tooth root. The synthesis and remodeling of nascent collagen matrices are of fundamental importance for the reestablishment of a functional periodontium and are mediated by diverse, multi-functional fibroblast populations that reside within the connective tissues of gingiva and periodontal ligament. Notably, after gingival wounding, a fibroblast sub-type (myofibroblast) arises, which is centrally involved in collagen synthesis and fibrillar remodeling. While myofibroblasts are not usually seen in healthy, mature connective tissues, their formation is enhanced by wound-healing cytokines. The formation of myofibroblasts is also modulated by the stiffness of the extracellular matrix, which is mechanosensed by resident precursor cells in the gingival connective tissue microenvironment. Here, we consider the cellular origins and the factors that control the differentiation and matrix remodeling functions of periodontal fibroblasts. An improved understanding of the regulation and function of periodontal fibroblasts will be critical for the development of new therapies to optimize the restoration of periodontal structure and function after wounding.
AbstractList After injury to periodontal tissues, a sequentially phased healing response is initiated that enables wound closure and partial restoration of tissue structure and function. Wound closure in periodontal tissues involves the tightly regulated coordination of resident cells in epithelial and connective tissue compartments. Multiple cell populations in these compartments synergize their metabolic activities to reestablish a mucosal seal that involves the underlying periodontal connective tissues and the attachment of these tissues to the tooth surface. The formation of an impermeable seal around the circumference of the tooth is of particular significance in oral health since colonization of tooth surfaces by pathogenic biofilms promotes inflammation, which can contribute to periodontal tissue degradation and tooth loss. The reformation of periodontal tissue structures in the healing response centrally involves fibroblasts, which synthesize and organize the collagen fibers that link alveolar bone and gingiva to the cementum covering the tooth root. The synthesis and remodeling of nascent collagen matrices are of fundamental importance for the reestablishment of a functional periodontium and are mediated by diverse, multi-functional fibroblast populations that reside within the connective tissues of gingiva and periodontal ligament. Notably, after gingival wounding, a fibroblast sub-type (myofibroblast) arises, which is centrally involved in collagen synthesis and fibrillar remodeling. While myofibroblasts are not usually seen in healthy, mature connective tissues, their formation is enhanced by wound-healing cytokines. The formation of myofibroblasts is also modulated by the stiffness of the extracellular matrix, which is mechanosensed by resident precursor cells in the gingival connective tissue microenvironment. Here, we consider the cellular origins and the factors that control the differentiation and matrix remodeling functions of periodontal fibroblasts. An improved understanding of the regulation and function of periodontal fibroblasts will be critical for the development of new therapies to optimize the restoration of periodontal structure and function after wounding.
After injury to periodontal tissues, a sequentially phased healing response is initiated that enables wound closure and partial restoration of tissue structure and function. Wound closure in periodontal tissues involves the tightly regulated coordination of resident cells in epithelial and connective tissue compartments. Multiple cell populations in these compartments synergize their metabolic activities to reestablish a mucosal seal that involves the underlying periodontal connective tissues and the attachment of these tissues to the tooth surface. The formation of an impermeable seal around the circumference of the tooth is of particular significance in oral health since colonization of tooth surfaces by pathogenic biofilms promotes inflammation, which can contribute to periodontal tissue degradation and tooth loss. The reformation of periodontal tissue structures in the healing response centrally involves fibroblasts, which synthesize and organize the collagen fibers that link alveolar bone and gingiva to the cementum covering the tooth root. The synthesis and remodeling of nascent collagen matrices are of fundamental importance for the reestablishment of a functional periodontium and are mediated by diverse, multi-functional fibroblast populations that reside within the connective tissues of gingiva and periodontal ligament. Notably, after gingival wounding, a fibroblast sub-type (myofibroblast) arises, which is centrally involved in collagen synthesis and fibrillar remodeling. While myofibroblasts are not usually seen in healthy, mature connective tissues, their formation is enhanced by wound-healing cytokines. The formation of myofibroblasts is also modulated by the stiffness of the extracellular matrix, which is mechanosensed by resident precursor cells in the gingival connective tissue microenvironment. Here, we consider the cellular origins and the factors that control the differentiation and matrix remodeling functions of periodontal fibroblasts. An improved understanding of the regulation and function of periodontal fibroblasts will be critical for the development of new therapies to optimize the restoration of periodontal structure and function after wounding.After injury to periodontal tissues, a sequentially phased healing response is initiated that enables wound closure and partial restoration of tissue structure and function. Wound closure in periodontal tissues involves the tightly regulated coordination of resident cells in epithelial and connective tissue compartments. Multiple cell populations in these compartments synergize their metabolic activities to reestablish a mucosal seal that involves the underlying periodontal connective tissues and the attachment of these tissues to the tooth surface. The formation of an impermeable seal around the circumference of the tooth is of particular significance in oral health since colonization of tooth surfaces by pathogenic biofilms promotes inflammation, which can contribute to periodontal tissue degradation and tooth loss. The reformation of periodontal tissue structures in the healing response centrally involves fibroblasts, which synthesize and organize the collagen fibers that link alveolar bone and gingiva to the cementum covering the tooth root. The synthesis and remodeling of nascent collagen matrices are of fundamental importance for the reestablishment of a functional periodontium and are mediated by diverse, multi-functional fibroblast populations that reside within the connective tissues of gingiva and periodontal ligament. Notably, after gingival wounding, a fibroblast sub-type (myofibroblast) arises, which is centrally involved in collagen synthesis and fibrillar remodeling. While myofibroblasts are not usually seen in healthy, mature connective tissues, their formation is enhanced by wound-healing cytokines. The formation of myofibroblasts is also modulated by the stiffness of the extracellular matrix, which is mechanosensed by resident precursor cells in the gingival connective tissue microenvironment. Here, we consider the cellular origins and the factors that control the differentiation and matrix remodeling functions of periodontal fibroblasts. An improved understanding of the regulation and function of periodontal fibroblasts will be critical for the development of new therapies to optimize the restoration of periodontal structure and function after wounding.
Author Martínez, Jorge
Martínez, Constanza
McCulloch, Christopher A.
Smith, Patricio C.
AuthorAffiliation 1 Faculty of Medicine, School of Dentistry, Pontificia Universidad Católica de Chile , Santiago , Chile
2 Laboratory of Cell Biology, Institute of Nutrition and Food Technology, INTA, Universidad de Chile , Santiago , Chile
3 Faculty of Dentistry, University of Toronto , Toronto, ON , Canada
AuthorAffiliation_xml – name: 3 Faculty of Dentistry, University of Toronto , Toronto, ON , Canada
– name: 1 Faculty of Medicine, School of Dentistry, Pontificia Universidad Católica de Chile , Santiago , Chile
– name: 2 Laboratory of Cell Biology, Institute of Nutrition and Food Technology, INTA, Universidad de Chile , Santiago , Chile
Author_xml – sequence: 1
  givenname: Patricio C.
  surname: Smith
  fullname: Smith, Patricio C.
– sequence: 2
  givenname: Constanza
  surname: Martínez
  fullname: Martínez, Constanza
– sequence: 3
  givenname: Jorge
  surname: Martínez
  fullname: Martínez, Jorge
– sequence: 4
  givenname: Christopher A.
  surname: McCulloch
  fullname: McCulloch, Christopher A.
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Cites_doi 10.1189/jlb.1012512
10.1902/jop.2017.160730
10.1016/j.retram.2016.09.003
10.1074/jbc.272.35.22103
10.1083/jcb.122.1.103
10.1126/science.283.5398.83
10.1089/ten.tea.2009.0796
10.1111/jre.12228
10.1177/0022034513497961
10.22203/eCM.v031a04
10.1083/jcb.120.6.1381
10.1016/j.celrep.2017.01.061
10.1242/bio.20135090
10.1016/j.biomaterials.2013.10.059
10.1083/jcb.39.1.135
10.1111/j.1749-6632.2003.tb03224.x
10.1177/154405910608500207
10.1016/S0002-9440(10)65334-5
10.1083/jcb.76.3.561
10.1016/j.yexcr.2004.06.007
10.1242/jcs.114.1.119
10.1038/nri3399
10.1159/000451078
10.1111/j.1524-475X.2011.00707.x
10.1007/s00441-016-2440-8
10.1097/00006534-200201000-00026
10.1177/00220345960750030601
10.1242/jcs.114.18.3285
10.1002/jcp.22405
10.1038/ni.2705
10.1111/j.1600-0765.1980.tb00258.x
10.1371/journal.pone.0036173
10.1189/jlb.0802406
10.1001/jama.2018.12426
10.3109/03008208409013684
10.1002/path.4359
10.1038/nature07039
10.1016/j.jdermsci.2009.09.005
10.1074/jbc.M104179200
10.1371/journal.pone.0042596
10.1002/ar.1091700312
10.1096/fj.11-196279
10.1083/jcb.44.3.645
10.1097/SLA.0b013e3182251559
10.1902/jop.2015.150360
10.4049/jimmunol.173.5.3514
10.15252/msb.20178174
10.1002/aja.1001670105
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Keywords wound healing
gingival
fibroblast
periodontal
connective tissue
Language English
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Reviewed by: Natalina Quarto, University of Naples Federico II, Italy; Monica Mattioli-Belmonte, Polytechnical University of Marche, Italy
This article was submitted to Craniofacial Biology and Dental Research, a section of the journal Frontiers in Physiology
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References Mak (ref28) 2009; 56
Kao (ref26) 2011; 254
Desmoulière (ref11) 1995; 146
Fournier (ref16) 2010; 16
Martinez (ref29) 2016; 87
Dumin (ref15) 2001; 276
Jones (ref25) 2018; 320
Sudbeck (ref43) 1997; 272
Chiron (ref3) 2012; 7
Williams (ref47) 1984; 12
Gould (ref20) 1980; 15
Gurtner (ref21) 2008; 453
Kolaczkowska (ref580) 2013; 3
Mirastschijski (ref31) 2004; 299
Klinkert (ref27) 2017; 58
Arora (ref1) 1999; 154
Mohammadi (ref32) 2014; 35
Chrysanthopoulou (ref4) 2014; 233
Davies (ref8) 2013; 14
Smith (ref41) 2006; 85
Dugina (ref14) 2001; 114
Tang (ref44) 2011; 226
Segal (ref40) 2001; 114
Coelho (ref5) 2016; 365
Giannopoulou (ref19) 1996; 75
Fournier (ref17) 2016; 31
Coelho (ref6) 2017; 18
Desmoulière (ref10) 1993; 122
Rognoni (ref38) 2018; 14
Iyer (ref23) 1999; 283
Dor (ref12) 2003; 995
Novak (ref33) 2013; 93
Ogawa (ref35) 2011; 19
Retamal (ref37) 2017; 88
Beanes (ref2) 2002; 109
Jin (ref24) 2015; 50
Odland (ref34) 1968; 39
Staudinger (ref42) 2013; 2
Desmoulière (ref9) 1992; 67
Hinz (ref22) 2016; 64
McCulloch (ref30) 1983; 167
Zhang (ref49) 2004; 173
Pacios (ref36) 2012; 26
Ten Cate (ref45) 1971; 170
Xu (ref48) 2013; 92
Toriseva (ref46) 2012; 7
Ross (ref39) 1970; 44
Conrad (ref7) 1993; 120
Dovi (ref13) 2003; 73
Gabbiani (ref18) 1978; 76
References_xml – volume: 93
  start-page: 875
  year: 2013
  ident: ref33
  article-title: Macrophage phenotypes during tissue repair
  publication-title: J. Leukocyte Biol.
  doi: 10.1189/jlb.1012512
– volume: 88
  start-page: 926
  year: 2017
  ident: ref37
  article-title: Glycated collagen stimulates differentiation of gingival myofibroblasts
  publication-title: J. Periodontol.
  doi: 10.1902/jop.2017.160730
– volume: 64
  start-page: 171
  year: 2016
  ident: ref22
  article-title: The role of myofibroblasts in wound healing
  publication-title: Curr. Res. Transl. Med.
  doi: 10.1016/j.retram.2016.09.003
– volume: 272
  start-page: 22103
  year: 1997
  ident: ref43
  article-title: Induction and repression of collagenase-1 by keratinocytes is controlled by distinct components of different extracellular matrix compartments
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.272.35.22103
– volume: 122
  start-page: 103
  year: 1993
  ident: ref10
  article-title: Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts
  publication-title: J. Cell. Biol.
  doi: 10.1083/jcb.122.1.103
– volume: 283
  start-page: 83
  year: 1999
  ident: ref23
  article-title: The transcriptional program in the response of human fibroblasts to serum
  publication-title: Science
  doi: 10.1126/science.283.5398.83
– volume: 16
  start-page: 2891
  year: 2010
  ident: ref16
  article-title: Multipotent progenitor cells in gingival connective tissue
  publication-title: Tissue Eng. Part A.
  doi: 10.1089/ten.tea.2009.0796
– volume: 50
  start-page: 461
  year: 2015
  ident: ref24
  article-title: Isolation and characterization of human mesenchymal stem cells from gingival connective tissue
  publication-title: J. Periodontal. Res.
  doi: 10.1111/jre.12228
– volume: 92
  start-page: 825
  year: 2013
  ident: ref48
  article-title: Gingivae contain neural-crest- and mesoderm-derived mesenchymal stem cells
  publication-title: J. Dent. Res.
  doi: 10.1177/0022034513497961
– volume: 31
  start-page: 40
  year: 2016
  ident: ref17
  article-title: Characterization of human gingival neural crest-derived stem cells in monolayer and neurosphere cultures
  publication-title: Eur. Cell. Mater.
  doi: 10.22203/eCM.v031a04
– volume: 120
  start-page: 1381
  year: 1993
  ident: ref7
  article-title: Relative distribution of actin, myosin I, and myosin II during the wound healing response of fibroblasts
  publication-title: J. Cell. Biol.
  doi: 10.1083/jcb.120.6.1381
– volume: 67
  start-page: 716
  year: 1992
  ident: ref9
  article-title: Heparin induces alpha-smooth muscle actin expression in cultured fibroblasts and in granulation tissue myofibroblasts
  publication-title: Lab. Invest.
– volume: 18
  start-page: 1774
  year: 2017
  ident: ref6
  article-title: Discoidin domain receptor 1 mediates myosin-dependent collagen contraction
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2017.01.061
– volume: 2
  start-page: 1148
  year: 2013
  ident: ref42
  article-title: Interactions between the discoidin domain receptor 1 and β1 integrin regulate attachment to collagen
  publication-title: Biol. Open
  doi: 10.1242/bio.20135090
– volume: 35
  start-page: 1138
  year: 2014
  ident: ref32
  article-title: Lateral boundary mechanosensing by adherent cells in a collagen gel system
  publication-title: Biomaterials
  doi: 10.1016/j.biomaterials.2013.10.059
– volume: 39
  start-page: 135
  year: 1968
  ident: ref34
  article-title: Human wound repair I. Epidermal regeneration
  publication-title: J. Cell. Biol.
  doi: 10.1083/jcb.39.1.135
– volume: 995
  start-page: 208
  year: 2003
  ident: ref12
  article-title: Induction of vascular networks in adult organs: implications to proangiogenic therapy
  publication-title: Ann. N.Y. Acad. Sci.
  doi: 10.1111/j.1749-6632.2003.tb03224.x
– volume: 85
  start-page: 150
  year: 2006
  ident: ref41
  article-title: Differential uPA expression by TGF-beta1 in gingival fibroblasts
  publication-title: J. Dent. Res.
  doi: 10.1177/154405910608500207
– volume: 154
  start-page: 871
  year: 1999
  ident: ref1
  article-title: The compliance of collagen gels regulates transforming growth factor-beta induction of alpha-smooth muscle actin in fibroblasts
  publication-title: Am. J. Pathol.
  doi: 10.1016/S0002-9440(10)65334-5
– volume: 76
  start-page: 561
  year: 1978
  ident: ref18
  article-title: Cytoplasmic filaments and gap junctions in epithelial cells and myofibroblasts during wound healing
  publication-title: J. Cell. Biol.
  doi: 10.1083/jcb.76.3.561
– volume: 299
  start-page: 465
  year: 2004
  ident: ref31
  article-title: Matrix metalloproteinase inhibitor GM 6001 attenuates keratinocyte migration, contraction and myofibroblast formation in skin wounds
  publication-title: Exp. Cell. Res.
  doi: 10.1016/j.yexcr.2004.06.007
– volume: 114
  start-page: 119
  year: 2001
  ident: ref40
  article-title: Involvement of actin filaments and integrins in the binding step in collagen phagocytosis by human fibroblasts
  publication-title: J. Cell Sci.
  doi: 10.1242/jcs.114.1.119
– volume: 3
  start-page: 159
  year: 2013
  ident: ref580
  article-title: Neutrophil recruitment and function in health and inflammation
  publication-title: Nat. Rev. Immunol.
  doi: 10.1038/nri3399
– volume: 58
  start-page: 109
  year: 2017
  ident: ref27
  article-title: Selective M2 macrophage depletion leads to prolonged inflammation in surgical wounds
  publication-title: Eur. Surg. Res.
  doi: 10.1159/000451078
– volume: 19
  start-page: s2
  year: 2011
  ident: ref35
  article-title: Mechanobiology of scarring
  publication-title: Wound Repair Regen.
  doi: 10.1111/j.1524-475X.2011.00707.x
– volume: 365
  start-page: 521
  year: 2016
  ident: ref5
  article-title: Contribution of collagen adhesion receptors to tissue fibrosis
  publication-title: Cell Tissue Res.
  doi: 10.1007/s00441-016-2440-8
– volume: 109
  start-page: 160
  year: 2002
  ident: ref2
  article-title: Confocal microscopic analysis of scarless repair in the fetal rat: defining the transition
  publication-title: Plast. Reconstr. Surg.
  doi: 10.1097/00006534-200201000-00026
– volume: 75
  start-page: 895
  year: 1996
  ident: ref19
  article-title: Functional characteristics of gingival and periodontal ligament fibroblasts
  publication-title: J. Dent. Res.
  doi: 10.1177/00220345960750030601
– volume: 114
  start-page: 3285
  year: 2001
  ident: ref14
  article-title: Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors
  publication-title: J. Cell Sci.
  doi: 10.1242/jcs.114.18.3285
– volume: 226
  start-page: 832
  year: 2011
  ident: ref44
  article-title: Characterization of mesenchymal stem cells from human normal and hyperplastic gingiva
  publication-title: J. Cell. Physiol.
  doi: 10.1002/jcp.22405
– volume: 14
  start-page: 986
  year: 2013
  ident: ref8
  article-title: Tissue-resident macrophages
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.2705
– volume: 15
  start-page: 20
  year: 1980
  ident: ref20
  article-title: Migration and division of progenitor cell populations in periodontal ligament after wounding
  publication-title: J. Periodontal. Res.
  doi: 10.1111/j.1600-0765.1980.tb00258.x
– volume: 7
  start-page: e36173
  year: 2012
  ident: ref3
  article-title: Complex interactions between human myoblasts and the surrounding 3D fibrin-based matrix
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0036173
– volume: 73
  start-page: 448
  year: 2003
  ident: ref13
  article-title: Accelerated wound closure in neutrophil-depleted mice
  publication-title: J. Leukocyte Biol.
  doi: 10.1189/jlb.0802406
– volume: 320
  start-page: 1481
  year: 2018
  ident: ref25
  article-title: Management of chronic wounds
  publication-title: JAMA
  doi: 10.1001/jama.2018.12426
– volume: 12
  start-page: 211
  year: 1984
  ident: ref47
  article-title: The distribution of types I and III collagen and fibronectin in the healing equine tendon
  publication-title: Connect. Tissue Res.
  doi: 10.3109/03008208409013684
– volume: 233
  start-page: 294
  year: 2014
  ident: ref4
  article-title: Neutrophil extracellular traps promote differentiation and function of fibroblasts
  publication-title: J. Pathol.
  doi: 10.1002/path.4359
– volume: 453
  start-page: 314
  year: 2008
  ident: ref21
  article-title: Wound repair and regeneration
  publication-title: Nature
  doi: 10.1038/nature07039
– volume: 56
  start-page: 168
  year: 2009
  ident: ref28
  article-title: Scarless healing of oral mucosa is characterized by faster resolution of inflammation and control of myofibroblast action compared to skin wounds in the red Duroc pig model
  publication-title: J. Dermatol. Sci.
  doi: 10.1016/j.jdermsci.2009.09.005
– volume: 276
  start-page: 29368
  year: 2001
  ident: ref15
  article-title: Pro-collagenase-1 (matrix metalloproteinase-1) binds the alpha(2)beta(1) integrin upon release from keratinocytes migrating on type I collagen
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M104179200
– volume: 146
  start-page: 56
  year: 1995
  ident: ref11
  article-title: Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar
  publication-title: Am. J. Pathol.
– volume: 7
  start-page: e42596
  year: 2012
  ident: ref46
  article-title: MMP-13 regulates growth of wound granulation tissue and modulates gene expression signatures involved in inflammation, proteolysis, and cell viability
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0042596
– volume: 170
  start-page: 365
  year: 1971
  ident: ref45
  article-title: The development of the periodontium. A transplantation and autoradiographic study
  publication-title: Anat. Rec.
  doi: 10.1002/ar.1091700312
– volume: 26
  start-page: 1423
  year: 2012
  ident: ref36
  article-title: Diabetes aggravates periodontitis by limiting repair through enhanced inflammation
  publication-title: FASEB J.
  doi: 10.1096/fj.11-196279
– volume: 44
  start-page: 645
  year: 1970
  ident: ref39
  article-title: Wound healing and collagen formation. VI. The origin of the wound fibroblast studied in parabiosis
  publication-title: J. Cell. Biol.
  doi: 10.1083/jcb.44.3.645
– volume: 254
  start-page: 1066
  year: 2011
  ident: ref26
  article-title: Peripheral blood fibrocytes: enhancement of wound healing by cell proliferation, re-epithelialization, contraction, and angiogenesis
  publication-title: Ann. Surg.
  doi: 10.1097/SLA.0b013e3182251559
– volume: 87
  start-page: e18
  year: 2016
  ident: ref29
  article-title: Platelet poor plasma and platelet rich plasma stimulate bone lineage differentiation in periodontal ligament stem cells
  publication-title: J. Periodontol.
  doi: 10.1902/jop.2015.150360
– volume: 173
  start-page: 3514
  year: 2004
  ident: ref49
  article-title: Short- and long-term effects of IL-1 and TNF antagonists on periodontal wound healing
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.173.5.3514
– volume: 14
  start-page: e8174
  year: 2018
  ident: ref38
  article-title: Fibroblast state switching orchestrates dermal maturation and wound healing
  publication-title: Mol. Syst. Biol.
  doi: 10.15252/msb.20178174
– volume: 167
  start-page: 43
  year: 1983
  ident: ref30
  article-title: Cell density and cell generation in the periodontal ligament of mice
  publication-title: Am. J. Anat.
  doi: 10.1002/aja.1001670105
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Snippet After injury to periodontal tissues, a sequentially phased healing response is initiated that enables wound closure and partial restoration of tissue structure...
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StartPage 270
SubjectTerms connective tissue
fibroblast
gingival
periodontal
Physiology
wound healing
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Title Role of Fibroblast Populations in Periodontal Wound Healing and Tissue Remodeling
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