Skip to main content
Erschienen in: Odontology 3/2019

14.12.2018 | Original Article

ADAM28 dramatically regulates the biological features of human gingival fibroblasts

verfasst von: Zheng Zhao, Jie Li, Xiu-Na Ding, Lei Zhou, De-Gang Sun

Erschienen in: Odontology | Ausgabe 3/2019

Einloggen, um Zugang zu erhalten

Abstract

This study was to explore the effects of a disintegrin and metalloproteinase 28 (ADAM28) on the proliferation, differentiation, and apoptosis of human gingival fibroblasts (HGFs) and probable mechanism. After ADAM28 antisense oligodeoxynucleotide (AS-ODN) and sense oligodeoxynucleotide (S-ODN) were transfected into HGFs by Lipofectamine 2000, respectively, the expression discrepancies of ADAM28 among various groups were evaluated by reverse transcription-polymerase chain reaction (RT-PCR) and Western-blotting. Methabenzthiazuron (MTT) and cell-cycle assays were used to test the HGFs proliferation activity. Annexin V fluorescein isothiocyanate (FITC)/propidium iodide (PI) and alkaline phosphatase (ALP) analysis were performed separately to measure apoptosis and the cytodifferentiation standard. Immunocytochemistry and Western-blotting were carried out to determine the influence of ADAM28 AS-ODN on HGFs expressing core binding factor α1 (Cbfα1), cementum protein 1 (CEMP1), osteopontin (OPN) and dentin matrix protein 1 (DMP1). The AS-ODN group displayed the lowest expression level in HGFs, meanwhile the ADAM28 S-ODN group showed the highest. Furthermore, blocking of ADAM28 could inhibit the proliferation of HGFs, enhance HGFs differentiation and induce apoptosis of HGFs. Whereas, overexpression of ADAM28 generated the opposite effects and inhibited apoptosis. ADAM28 AS-ODN was able to notably suppress the expressions of Cbfα1 and CEMP1, and ADAM28 had positive correlations with cbfα1 and CEMP1. These provided conspicuous evidence that ADAM28 may play a crucial role in root development as a potential regulator of growth, differentiation, and apoptosis of HGFs.
Literatur
1.
Zurück zum Zitat Sawada S, Chosa N, Ishisaki A, Naruishi K. Enhancement of gingival inflammation induced by synergism of IL-1β and IL-6. Biomed Res. 2013;34:31–40.CrossRefPubMed Sawada S, Chosa N, Ishisaki A, Naruishi K. Enhancement of gingival inflammation induced by synergism of IL-1β and IL-6. Biomed Res. 2013;34:31–40.CrossRefPubMed
2.
Zurück zum Zitat Lu X, Lu D, Scully MF, Kakkar VV. Snake venom metalloproteinase containing a disintegrin-like domain, its structure-activity relationships at interacting with integrins. Curr Med Chem Cardiovasc Hematol Agents. 2005;3:249–60.CrossRefPubMed Lu X, Lu D, Scully MF, Kakkar VV. Snake venom metalloproteinase containing a disintegrin-like domain, its structure-activity relationships at interacting with integrins. Curr Med Chem Cardiovasc Hematol Agents. 2005;3:249–60.CrossRefPubMed
3.
Zurück zum Zitat Zhao Z, Wen LY, Jin M, Deng ZH, Jin Y. ADAM28 participates in the regulation of tooth development. Arch Oral Biol. 2006;51:996–1005.CrossRefPubMed Zhao Z, Wen LY, Jin M, Deng ZH, Jin Y. ADAM28 participates in the regulation of tooth development. Arch Oral Biol. 2006;51:996–1005.CrossRefPubMed
4.
Zurück zum Zitat Apajalahti S, Hölttä P, Turtola L, Pirinen S. Prevalence of short-root anomaly in healthy young adults. Acta Odontol Scand. 2002;60:56–9.CrossRefPubMed Apajalahti S, Hölttä P, Turtola L, Pirinen S. Prevalence of short-root anomaly in healthy young adults. Acta Odontol Scand. 2002;60:56–9.CrossRefPubMed
5.
Zurück zum Zitat Bermúdez M, Imaz-Rosshandler I, Rangel-Escareño C, Zeichner-David M, Arzate H, Mercado-Celis GE. CEMP1 induces transformation in human gingival fibroblasts. PLoS One. 2015;10:0127286. Bermúdez M, Imaz-Rosshandler I, Rangel-Escareño C, Zeichner-David M, Arzate H, Mercado-Celis GE. CEMP1 induces transformation in human gingival fibroblasts. PLoS One. 2015;10:0127286.
6.
Zurück zum Zitat Zhao Z, Tang L, Deng Z, Wen L, Jin Y. Essential role of ADAM28 in regulating the proliferation and differentiation of human dental papilla mesenchymal cells hDPMCs. Histochem Cell Biol. 2008;130:1015–25.CrossRefPubMed Zhao Z, Tang L, Deng Z, Wen L, Jin Y. Essential role of ADAM28 in regulating the proliferation and differentiation of human dental papilla mesenchymal cells hDPMCs. Histochem Cell Biol. 2008;130:1015–25.CrossRefPubMed
7.
Zurück zum Zitat Wu G, Lin N, Xu L, Liu B, Feitelson MA. UCN-01 induces S and G2/M cell cycle arrest through the p53/p21(waf1) or CHK2/CDC25C pathways and can suppress invasion in human hepatoma cell lines. BMC Cancer. 2013;13:167–77.CrossRefPubMedPubMedCentral Wu G, Lin N, Xu L, Liu B, Feitelson MA. UCN-01 induces S and G2/M cell cycle arrest through the p53/p21(waf1) or CHK2/CDC25C pathways and can suppress invasion in human hepatoma cell lines. BMC Cancer. 2013;13:167–77.CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Zhao Z, Liu H, Wang D. ADAM28 manipulates proliferation, differentiation, and apoptosis of human dental pulp stem cells [J]. J Endod. 2011;37:332–9.CrossRefPubMed Zhao Z, Liu H, Wang D. ADAM28 manipulates proliferation, differentiation, and apoptosis of human dental pulp stem cells [J]. J Endod. 2011;37:332–9.CrossRefPubMed
9.
Zurück zum Zitat Fourie AM, Coles F, Moreno V, Karlsson L. Catalytic activity of ADAM8, ADAM15, and MDC-l (ADAM28) on synthetic peptide substrates and in ectodomain cleavage of CD23. J Biol Chem. 2003;278:30469–77.CrossRefPubMed Fourie AM, Coles F, Moreno V, Karlsson L. Catalytic activity of ADAM8, ADAM15, and MDC-l (ADAM28) on synthetic peptide substrates and in ectodomain cleavage of CD23. J Biol Chem. 2003;278:30469–77.CrossRefPubMed
10.
Zurück zum Zitat Jowett JB, Okada Y, Leedman PJ, Curran JE, Johnson MP, Moses EK. Goring HH, Mochizuki S, Blangero J, Stone L, et al. ADAM28 is elevated in humans with the metabolic syndrome and is a novel sheddase of human tumour necrosis factor-α. Immunol Cell Biol. 2012;90:966–73.CrossRefPubMed Jowett JB, Okada Y, Leedman PJ, Curran JE, Johnson MP, Moses EK. Goring HH, Mochizuki S, Blangero J, Stone L, et al. ADAM28 is elevated in humans with the metabolic syndrome and is a novel sheddase of human tumour necrosis factor-α. Immunol Cell Biol. 2012;90:966–73.CrossRefPubMed
11.
Zurück zum Zitat Baurakiades E, Costa VH Jr., Raboni SM, de Almeida VR, Larsen KS, Kohler JN, Gozzo Pdo C, Klassen G, Manica GC, de Noronha L. The roles of ADAM33, ADAM28, IL-13 and IL-4 in the development of lung injuries in children with lethal non-pandemic acute infectious pneumonia. J Clin Virol. 2014;61:585–9.CrossRefPubMed Baurakiades E, Costa VH Jr., Raboni SM, de Almeida VR, Larsen KS, Kohler JN, Gozzo Pdo C, Klassen G, Manica GC, de Noronha L. The roles of ADAM33, ADAM28, IL-13 and IL-4 in the development of lung injuries in children with lethal non-pandemic acute infectious pneumonia. J Clin Virol. 2014;61:585–9.CrossRefPubMed
12.
Zurück zum Zitat Zhang XH, Wang CC, Jiang Q, Yang SM, Jiang H, Lu J, Wang QM, Feng FE, Zhu XL, Zhao T, et al. ADAM28 overexpression regulated via the PI3K/AKT pathway is associated with relapse in de novo adult B-cell acute lymphoblastic leukemia. Leuk Res. 2015;15:30359–63. Zhang XH, Wang CC, Jiang Q, Yang SM, Jiang H, Lu J, Wang QM, Feng FE, Zhu XL, Zhao T, et al. ADAM28 overexpression regulated via the PI3K/AKT pathway is associated with relapse in de novo adult B-cell acute lymphoblastic leukemia. Leuk Res. 2015;15:30359–63.
13.
Zurück zum Zitat Mitsui Y, Mochizuki S, Kodama T, Shimoda M, Ohtsuka T, Shiomi T, Chijiiwa M, Ikeda T, Kitajima M, Okada Y. ADAM28 is overexpressed in human breast carcinomas: Implications for carcinoma cell proliferation through cleavage of insulin-like growth factor binding protein-3. Cancer Res. 2006;66:9913–20.CrossRefPubMed Mitsui Y, Mochizuki S, Kodama T, Shimoda M, Ohtsuka T, Shiomi T, Chijiiwa M, Ikeda T, Kitajima M, Okada Y. ADAM28 is overexpressed in human breast carcinomas: Implications for carcinoma cell proliferation through cleavage of insulin-like growth factor binding protein-3. Cancer Res. 2006;66:9913–20.CrossRefPubMed
14.
Zurück zum Zitat Wood O, Woo J, Seumois G, Savelyeva N, McCann KJ, Singh D, Jones T, Peel L, Breen M, Ward M, et al. Gene expression analysis of TIL rich HPV-driven head and neck tumors reveals a distinct B-cell signature when compared to HPV independent tumors. Oncotarget. 2016;7:56781–97.CrossRefPubMedPubMedCentral Wood O, Woo J, Seumois G, Savelyeva N, McCann KJ, Singh D, Jones T, Peel L, Breen M, Ward M, et al. Gene expression analysis of TIL rich HPV-driven head and neck tumors reveals a distinct B-cell signature when compared to HPV independent tumors. Oncotarget. 2016;7:56781–97.CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Buckley CD, Pilling D, Lord JM, Akbar AN, Scheel-Toellner D, Salmon M. Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation. Trends Immunol. 2001;22:199–204.CrossRefPubMed Buckley CD, Pilling D, Lord JM, Akbar AN, Scheel-Toellner D, Salmon M. Fibroblasts regulate the switch from acute resolving to chronic persistent inflammation. Trends Immunol. 2001;22:199–204.CrossRefPubMed
16.
Zurück zum Zitat Takada H, Mihara J, Morisaki I, Hamada S. Induction of interleukin-1 and -6 in human gingival fibroblast cultures stimulated with bacteroides lipopolysaccharides. Infect Immun. 1991;59:295–301.PubMedPubMedCentral Takada H, Mihara J, Morisaki I, Hamada S. Induction of interleukin-1 and -6 in human gingival fibroblast cultures stimulated with bacteroides lipopolysaccharides. Infect Immun. 1991;59:295–301.PubMedPubMedCentral
17.
Zurück zum Zitat Slavkin HC. Antisense oligonucleotides: an experimental strategy to advance a causal analysis of development. Int J Dev Biol. 1995;39:123–6.PubMed Slavkin HC. Antisense oligonucleotides: an experimental strategy to advance a causal analysis of development. Int J Dev Biol. 1995;39:123–6.PubMed
18.
Zurück zum Zitat Santamaria D, Ortega S. Cyclins and CDKs in development and cancer: lessons from genetically modified mice. Front Biosci. 2006;11:1164–88.CrossRefPubMed Santamaria D, Ortega S. Cyclins and CDKs in development and cancer: lessons from genetically modified mice. Front Biosci. 2006;11:1164–88.CrossRefPubMed
19.
Zurück zum Zitat Partanen AM, Thesleff I. Growth factors and tooth development. Int J Dev Biol. 1989;33:165–72.PubMed Partanen AM, Thesleff I. Growth factors and tooth development. Int J Dev Biol. 1989;33:165–72.PubMed
20.
Zurück zum Zitat Cheng R, Choudhury D, Liu C, Billet S, Hu T, Bhowmick NA. Gingival fibroblasts resist apoptosis in response to oxidative stress in a model of periodontal diseases. Cell Death Discov. 2015;9:15046–56.CrossRef Cheng R, Choudhury D, Liu C, Billet S, Hu T, Bhowmick NA. Gingival fibroblasts resist apoptosis in response to oxidative stress in a model of periodontal diseases. Cell Death Discov. 2015;9:15046–56.CrossRef
21.
Zurück zum Zitat Peterkova R, Peterka M, Lesot H. The developing murine dentition: a new tool for apoptosis study. Ann N Y Acad Sci. 2003;1010:453–66.CrossRefPubMed Peterkova R, Peterka M, Lesot H. The developing murine dentition: a new tool for apoptosis study. Ann N Y Acad Sci. 2003;1010:453–66.CrossRefPubMed
22.
Zurück zum Zitat Vaahtokari A, Aberg T, Thesleff I. Apoptosis in the developing tooth: association with an embryonic signaling center and suppression by EGF and FGF-4. Development. 1996;122:121–9.PubMed Vaahtokari A, Aberg T, Thesleff I. Apoptosis in the developing tooth: association with an embryonic signaling center and suppression by EGF and FGF-4. Development. 1996;122:121–9.PubMed
23.
Zurück zum Zitat Bolean M, Simão AMS, Barioni MB, Favarin BZ, Sebinelli HG, Veschi EA, Janku TAB, Bottini M, Hoylaerts MF, Itri R, Millán JL, Ciancaglini P. Biophysical aspects of biomineralization. Biophys Rev. 2017;9:747–60.CrossRefPubMedPubMedCentral Bolean M, Simão AMS, Barioni MB, Favarin BZ, Sebinelli HG, Veschi EA, Janku TAB, Bottini M, Hoylaerts MF, Itri R, Millán JL, Ciancaglini P. Biophysical aspects of biomineralization. Biophys Rev. 2017;9:747–60.CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Unda FJ, Martin A, Hernandez C, Perez-Nanclares G, Hilario E, Arechaga J. FGFs-1 and -2, and TGFb1 as inductive signals modulating in vitro odontoblast differentiation. Adv Dent Res. 2001;15:34–7.CrossRefPubMed Unda FJ, Martin A, Hernandez C, Perez-Nanclares G, Hilario E, Arechaga J. FGFs-1 and -2, and TGFb1 as inductive signals modulating in vitro odontoblast differentiation. Adv Dent Res. 2001;15:34–7.CrossRefPubMed
25.
Zurück zum Zitat Shiba H, Mouri Y, Komatsuzawa H, Mizuno N, Xu W, Noguchi T, et al. Enhancement of alkaline phosphatase synthesis in pulp cells co-cultured with epithelial cells derived from lower rabbit incisors. Cell Biol Int. 2003;27:815–23.CrossRefPubMed Shiba H, Mouri Y, Komatsuzawa H, Mizuno N, Xu W, Noguchi T, et al. Enhancement of alkaline phosphatase synthesis in pulp cells co-cultured with epithelial cells derived from lower rabbit incisors. Cell Biol Int. 2003;27:815–23.CrossRefPubMed
26.
Zurück zum Zitat Zhu L, Skoultchi AI. Coordinating cell proliferation and differentiation. Curr Opin Genet Dev. 2001;11:91–7.CrossRefPubMed Zhu L, Skoultchi AI. Coordinating cell proliferation and differentiation. Curr Opin Genet Dev. 2001;11:91–7.CrossRefPubMed
27.
Zurück zum Zitat Kobayashi I, Kiyoshima T, Wada H, Matsuo K, Nonaka K, Honda JY, et al. Type II/III Runx2/Cbfα1 is required for tooth germ development. Bone. 2006;38:836–44.CrossRefPubMed Kobayashi I, Kiyoshima T, Wada H, Matsuo K, Nonaka K, Honda JY, et al. Type II/III Runx2/Cbfα1 is required for tooth germ development. Bone. 2006;38:836–44.CrossRefPubMed
28.
Zurück zum Zitat Kitagawa M, Tahara H, Kitagawa S, Oka H, Kudo Y, Sato S, et al. Characterization of established cementoblasts-like cells from human cementum-lining cells in vitro and in vivo. Bone. 2006;39:1035–42.CrossRefPubMed Kitagawa M, Tahara H, Kitagawa S, Oka H, Kudo Y, Sato S, et al. Characterization of established cementoblasts-like cells from human cementum-lining cells in vitro and in vivo. Bone. 2006;39:1035–42.CrossRefPubMed
29.
Zurück zum Zitat Arzate HJ, Chimal-Monroy L, Hernández-Lagunas L. Díaz de León. Human cementum protein extract promotes chondrogenesis and mineralization in mesenchymal cells. J Periodont Res. 1996;31:144–8.CrossRef Arzate HJ, Chimal-Monroy L, Hernández-Lagunas L. Díaz de León. Human cementum protein extract promotes chondrogenesis and mineralization in mesenchymal cells. J Periodont Res. 1996;31:144–8.CrossRef
30.
Zurück zum Zitat Alvarez Pérez MA, Pitaru S, Alvarez Fregoso O, Reyes Gasga J, Arzate H. Anti-cementoblastoma-derived protein antibody partially inhibits mineralization on a cementoblastic cell line. J Struct Biol. 2003;143:1–13.CrossRefPubMed Alvarez Pérez MA, Pitaru S, Alvarez Fregoso O, Reyes Gasga J, Arzate H. Anti-cementoblastoma-derived protein antibody partially inhibits mineralization on a cementoblastic cell line. J Struct Biol. 2003;143:1–13.CrossRefPubMed
31.
Zurück zum Zitat Carmona-Rodríguez B, Alvarez-Pérez MA, Narayanan AS, Zeichner-David M, Reyes-Gasga J, Molina-Guarneros J, et al. Human cementum protein 1 induces expression of bone and cementum proteins by human gingival fibroblasts. Biochem Biophys Res Commun. 2007;358:763–9.CrossRefPubMed Carmona-Rodríguez B, Alvarez-Pérez MA, Narayanan AS, Zeichner-David M, Reyes-Gasga J, Molina-Guarneros J, et al. Human cementum protein 1 induces expression of bone and cementum proteins by human gingival fibroblasts. Biochem Biophys Res Commun. 2007;358:763–9.CrossRefPubMed
32.
Zurück zum Zitat Zhao Z, Liu H, Wang D. ADAM28 manipulates proliferation, differentiation, and apoptosis of human dental pulp stem cells. J Endod. 2011;37:332–9.CrossRefPubMed Zhao Z, Liu H, Wang D. ADAM28 manipulates proliferation, differentiation, and apoptosis of human dental pulp stem cells. J Endod. 2011;37:332–9.CrossRefPubMed
33.
Zurück zum Zitat Herat L, Rudnicka C, Okada Y, Mochizuki S, Schlaich M, Matthews V. The metalloproteinase ADAM28 promotes metabolic dysfunction in mice. Int J Mol Sci. 2017;18:263–73.CrossRef Herat L, Rudnicka C, Okada Y, Mochizuki S, Schlaich M, Matthews V. The metalloproteinase ADAM28 promotes metabolic dysfunction in mice. Int J Mol Sci. 2017;18:263–73.CrossRef
34.
Zurück zum Zitat Mochizuki S, Shimoda M, Shiomi T, Fujii Y, Okada Y. ADAM28 is activated by MMP-7 (matrilysin-1) and cleaves insulin-like growth factor binding protein-3. Biochem Biophys Res Commun. 2004;315:79–84.CrossRefPubMed Mochizuki S, Shimoda M, Shiomi T, Fujii Y, Okada Y. ADAM28 is activated by MMP-7 (matrilysin-1) and cleaves insulin-like growth factor binding protein-3. Biochem Biophys Res Commun. 2004;315:79–84.CrossRefPubMed
35.
Zurück zum Zitat Shalhoub V, Aslam F, Breen E, Van Wijnen A, Bortell R, Stein GS, et al. Multiple levels of steroid hormone-dependent control of osteocalcin during osteoblast differentiation: glucocorticoid regulation of basal and vitamin D stimulated gene expression. J Cell Biochem. 1998;69:154–68.CrossRefPubMed Shalhoub V, Aslam F, Breen E, Van Wijnen A, Bortell R, Stein GS, et al. Multiple levels of steroid hormone-dependent control of osteocalcin during osteoblast differentiation: glucocorticoid regulation of basal and vitamin D stimulated gene expression. J Cell Biochem. 1998;69:154–68.CrossRefPubMed
36.
Zurück zum Zitat Qin C, D’Souza R, Feng JQ. Dentin matrix protein 1 (DMP1): new and important roles for biomineralization and phosphate homeostasis. J Dent Res. 2007;86:1134–41.CrossRefPubMed Qin C, D’Souza R, Feng JQ. Dentin matrix protein 1 (DMP1): new and important roles for biomineralization and phosphate homeostasis. J Dent Res. 2007;86:1134–41.CrossRefPubMed
Metadaten
Titel
ADAM28 dramatically regulates the biological features of human gingival fibroblasts
verfasst von
Zheng Zhao
Jie Li
Xiu-Na Ding
Lei Zhou
De-Gang Sun
Publikationsdatum
14.12.2018
Verlag
Springer Japan
Erschienen in
Odontology / Ausgabe 3/2019
Print ISSN: 1618-1247
Elektronische ISSN: 1618-1255
DOI
https://doi.org/10.1007/s10266-018-0403-0

Weitere Artikel der Ausgabe 3/2019

Odontology 3/2019 Zur Ausgabe

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Zahnmedizin und bleiben Sie gut informiert – ganz bequem per eMail.