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Published in: Odontology 4/2022

28-02-2022 | Caries | Original Article

Upregulation of TRPA1 and reduction of NF-κB translocation could be part of the immunomodulatory process during primary tooth inflammation

Authors: Kullanun Nukaeow, Namthip Patinotham, Supita Tanasawet, Aunwaya Kaewpitak

Published in: Odontology | Issue 4/2022

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Abstract

Transient receptor potential ankyrin 1 (TRPA1) is expressed on neurons and immune and endothelial cells, and acts as a chemosensor that is activated by bacterial components and endotoxins. This study aimed to better understand how TRPA1 responds to inflammation induced by bacterial-related stimuli during dental caries. The pulp of 40 primary teeth and 46 permanent teeth were categorized into three stages of carious progression: intact dentin, exposed dentin and exposed pulp. We measured the percentages of cells with NF-κB nuclear translocation to verify the severity of inflammation, and then assessed TRPA1 expression by immunofluorescence technique in the pulpal horn, subodontoblastic and mid-coronal regions of the dental pulp samples at various stages of caries. We found NF-κB nuclear translocation gradually reduced during the progression of caries in all three areas of the dental pulp in both primary and permanent teeth. TRPA1 was gradually upregulated in the pulp of primary teeth as caries progressed, but did not significantly vary during caries in the pulp of permanent teeth. This study of TRPA1 expression demonstrates primary and permanent teeth exhibit distinct responses when undergoing carious infection.
Literature
1.
go back to reference Kawai T, Akira S. Signaling to NF-kappa B by Toll-like receptors. Trends Mol Med. 2007;13(11):460–9.CrossRef Kawai T, Akira S. Signaling to NF-kappa B by Toll-like receptors. Trends Mol Med. 2007;13(11):460–9.CrossRef
2.
go back to reference Fischer MJM, Mak SWY, McNaughton PA. Sensitisation of nociceptors—what are ion channels doing? Open Pain J. 2010;3:82–96.CrossRef Fischer MJM, Mak SWY, McNaughton PA. Sensitisation of nociceptors—what are ion channels doing? Open Pain J. 2010;3:82–96.CrossRef
3.
go back to reference Haas ET, Rowland K, Gautam M. Tooth injury increases expression of the cold sensitive TRP channel TRPA1 in trigeminal neurons. Arch Oral Biol. 2011;56(12):1604–9.CrossRef Haas ET, Rowland K, Gautam M. Tooth injury increases expression of the cold sensitive TRP channel TRPA1 in trigeminal neurons. Arch Oral Biol. 2011;56(12):1604–9.CrossRef
4.
go back to reference Meseguer V, Alpizar YA, Luis E, Tajada S, Denlinger B, Fajardo O, Manenschijn JA, Fernández-Peña C, Talavera A, Kichko T, Navia B, Sánchez A, Señarís R, Reeh P, Pérez-García MT, López-López JR, Voets T, Belmonte C, Talavera K, Viana F. TRPA1 channels mediate acute neurogenic inflammation and pain produced by bacterial endotoxins. Nat Commun. 2014;5:3125.CrossRef Meseguer V, Alpizar YA, Luis E, Tajada S, Denlinger B, Fajardo O, Manenschijn JA, Fernández-Peña C, Talavera A, Kichko T, Navia B, Sánchez A, Señarís R, Reeh P, Pérez-García MT, López-López JR, Voets T, Belmonte C, Talavera K, Viana F. TRPA1 channels mediate acute neurogenic inflammation and pain produced by bacterial endotoxins. Nat Commun. 2014;5:3125.CrossRef
5.
go back to reference Nilius B, Appendino G, Owsianik G. The transient receptor potential channel TRPA1: from gene to pathophysiology. Pflugers Arch Eur J Physiol. 2012;464(5):425–58.CrossRef Nilius B, Appendino G, Owsianik G. The transient receptor potential channel TRPA1: from gene to pathophysiology. Pflugers Arch Eur J Physiol. 2012;464(5):425–58.CrossRef
6.
go back to reference Blaecke A, Delneste Y, Herbault N, Jeannin P, Bonnefoy JY, Beck A, Aubry JP. Measurement of nuclear factor-Kappa B translocation on lipopolysaccharide-activated human dendritic cells by confocal microscopy and flow cytometry. Cytometry. 2002;48(2):71–9.CrossRef Blaecke A, Delneste Y, Herbault N, Jeannin P, Bonnefoy JY, Beck A, Aubry JP. Measurement of nuclear factor-Kappa B translocation on lipopolysaccharide-activated human dendritic cells by confocal microscopy and flow cytometry. Cytometry. 2002;48(2):71–9.CrossRef
7.
go back to reference Chen G, Sun W, Liang Y, Chen T, Guo W, Tian W. Maternal diabetes modulates offspring cell proliferation and apoptosis during odontogenesis via the TLR4/NF-κB signalling pathway. Cell Prolif. 2017;50(3):e12324.CrossRef Chen G, Sun W, Liang Y, Chen T, Guo W, Tian W. Maternal diabetes modulates offspring cell proliferation and apoptosis during odontogenesis via the TLR4/NF-κB signalling pathway. Cell Prolif. 2017;50(3):e12324.CrossRef
8.
go back to reference Pr C, Holder MJ, Smith AJ. Inflammation and regeneration in the dentin pulp complex: a double-edged sword. J Endod. 2014;40(4 suppl.):46–51. Pr C, Holder MJ, Smith AJ. Inflammation and regeneration in the dentin pulp complex: a double-edged sword. J Endod. 2014;40(4 suppl.):46–51.
11.
go back to reference Magloire H, Romeas A, Melin M, Couble ML, Bleicher F, Farges JC. Molecular regulation of odontoblast activity under dentin injury. Adv Dent Res. 2001;15:46–50.CrossRef Magloire H, Romeas A, Melin M, Couble ML, Bleicher F, Farges JC. Molecular regulation of odontoblast activity under dentin injury. Adv Dent Res. 2001;15:46–50.CrossRef
12.
go back to reference Hozhabri NS, Benson MD, Vu MD, et al. Decreasing NF-κB expression enhances odontoblastic differentiation and collagen expression in dental pulp stem cells exposed to inflammatory cytokines. PLoS ONE. 2015;10(1):e0113334.CrossRef Hozhabri NS, Benson MD, Vu MD, et al. Decreasing NF-κB expression enhances odontoblastic differentiation and collagen expression in dental pulp stem cells exposed to inflammatory cytokines. PLoS ONE. 2015;10(1):e0113334.CrossRef
13.
go back to reference Tazawa K, Kawashima N, Kuramoto M, Noda S, Mayuko F, Nara K, Hashimoto K, Okiji T. Transient receptor potential ankyrin 1 is up-regulated in response to lipopolysaccharide via P38/Mitogen-Activated protein kinase in dental pulp cells and promotes mineralization. Am J Pathol. 2020;190(12):2417–26.CrossRef Tazawa K, Kawashima N, Kuramoto M, Noda S, Mayuko F, Nara K, Hashimoto K, Okiji T. Transient receptor potential ankyrin 1 is up-regulated in response to lipopolysaccharide via P38/Mitogen-Activated protein kinase in dental pulp cells and promotes mineralization. Am J Pathol. 2020;190(12):2417–26.CrossRef
14.
go back to reference Ko HK, Lin AH, Perng DW, Lee TS, Kou YU. Lung epithelial TRPA1 mediates lipopolysaccharide-induced lung inflammation in bronchial epithelial cells and mice. Front Physiol. 2020;11:596314.CrossRef Ko HK, Lin AH, Perng DW, Lee TS, Kou YU. Lung epithelial TRPA1 mediates lipopolysaccharide-induced lung inflammation in bronchial epithelial cells and mice. Front Physiol. 2020;11:596314.CrossRef
15.
go back to reference Kaewpitak A, Bauer CS, Seward EP, Boissonade FM, Douglas CWI. Porphyromonas gingivalis lipopolysaccharide rapidly activates trigeminal sensory neurons and may contribute to pulpal pain. Int Endod J. 2020;53(6):846–58.CrossRef Kaewpitak A, Bauer CS, Seward EP, Boissonade FM, Douglas CWI. Porphyromonas gingivalis lipopolysaccharide rapidly activates trigeminal sensory neurons and may contribute to pulpal pain. Int Endod J. 2020;53(6):846–58.CrossRef
16.
go back to reference Kim YS, Jung HK, Kwon TK, et al. Expression of transient receptor potential ankyrin 1 in human dental pulp. J Endod. 2012;38(8):1087–92.CrossRef Kim YS, Jung HK, Kwon TK, et al. Expression of transient receptor potential ankyrin 1 in human dental pulp. J Endod. 2012;38(8):1087–92.CrossRef
17.
go back to reference Luostarinen S, Hämäläinen M, Hatano N, Muraki K, Moilanen E. The inflammatory regulation of TRPA1 expression in human A549 lung epithelial cells. Pulm Pharmacol Ther. 2021;70:102059.CrossRef Luostarinen S, Hämäläinen M, Hatano N, Muraki K, Moilanen E. The inflammatory regulation of TRPA1 expression in human A549 lung epithelial cells. Pulm Pharmacol Ther. 2021;70:102059.CrossRef
18.
go back to reference Luostarinen S, Hämäläinen M, Moilanen E. Transient receptor potential ankyrin 1 (TRPA1)—an inflammation-induced factor in human HaCaT keratinocytes. Int J Mol Sci. 2021;22(7):3322.CrossRef Luostarinen S, Hämäläinen M, Moilanen E. Transient receptor potential ankyrin 1 (TRPA1)—an inflammation-induced factor in human HaCaT keratinocytes. Int J Mol Sci. 2021;22(7):3322.CrossRef
19.
go back to reference Lee HS, Lee SY, Son DJ, Lee H, Yoo HS, Song S, Oh KW, Han DC, Kwon BM, Hong JT. Inhibitory effect of 20 -hydroxycinnamaldehyde on nitric oxide production through inhibition of NF-κB activation in RAW 264.7 cells. Biochem Pharmacol. 2005;69(5):791–9.CrossRef Lee HS, Lee SY, Son DJ, Lee H, Yoo HS, Song S, Oh KW, Han DC, Kwon BM, Hong JT. Inhibitory effect of 20 -hydroxycinnamaldehyde on nitric oxide production through inhibition of NF-κB activation in RAW 264.7 cells. Biochem Pharmacol. 2005;69(5):791–9.CrossRef
20.
go back to reference Nirwana I, Agustantina TH, Soekartono RH. NF-κB expressions on rat dental pulp mechanically exposured after pomegranate fruit extract administration. J Int dent. 2017;10(1):123–7. Nirwana I, Agustantina TH, Soekartono RH. NF-κB expressions on rat dental pulp mechanically exposured after pomegranate fruit extract administration. J Int dent. 2017;10(1):123–7.
21.
go back to reference Farges JC, Bellanger A, Ducret M, Aubert-Foucher E, Richard B, Alliot-Licht B, Bleicher F, Carrouel F. Human odontoblast-like cells produce nitric oxide with antibacterial activity upon TLR2 activation. Front Physiol. 2015;6:185.CrossRef Farges JC, Bellanger A, Ducret M, Aubert-Foucher E, Richard B, Alliot-Licht B, Bleicher F, Carrouel F. Human odontoblast-like cells produce nitric oxide with antibacterial activity upon TLR2 activation. Front Physiol. 2015;6:185.CrossRef
22.
go back to reference Farges JC, Alliot-Licht B, Renard E, et al. Dental pulp defence and repair mechanisms in dental caries. Mediat Inflamm. 2015;2015:230251.CrossRef Farges JC, Alliot-Licht B, Renard E, et al. Dental pulp defence and repair mechanisms in dental caries. Mediat Inflamm. 2015;2015:230251.CrossRef
23.
go back to reference Krivanek J, Soldatov RA, Kastriti ME, et al. Dental cell type atlas reveals stem and differentiated cell types in mouse and human teeth. Nat Commun. 2020;11(1):4816.CrossRef Krivanek J, Soldatov RA, Kastriti ME, et al. Dental cell type atlas reveals stem and differentiated cell types in mouse and human teeth. Nat Commun. 2020;11(1):4816.CrossRef
24.
go back to reference Fristad I, Berggreen E. Structure and functions of the dentin-pulp complex. In: Hargreaves KM, Berman LH, editors. Cohen’s pathways of the pulp. 11th ed. St. Louis, Missouri: Elsevier; 2016. p. 532–66. Fristad I, Berggreen E. Structure and functions of the dentin-pulp complex. In: Hargreaves KM, Berman LH, editors. Cohen’s pathways of the pulp. 11th ed. St. Louis, Missouri: Elsevier; 2016. p. 532–66.
25.
go back to reference Pei F, Wang HS, Chen Z, Zhang L. Autophagy regulates odontoblast differentiation by suppressing NF-κB activation in an inflammatory environment. Cell Death Dis. 2016;7(3):e2122.CrossRef Pei F, Wang HS, Chen Z, Zhang L. Autophagy regulates odontoblast differentiation by suppressing NF-κB activation in an inflammatory environment. Cell Death Dis. 2016;7(3):e2122.CrossRef
26.
go back to reference Diogenes A, Ferraz CC, Akopian AN, Henry MA, Hargreaves KM. LPS sensitizes TRPV1 via activation of TLR4 in trigeminal sensory neurons. J Dent Res. 2011;90(6):759–64.CrossRef Diogenes A, Ferraz CC, Akopian AN, Henry MA, Hargreaves KM. LPS sensitizes TRPV1 via activation of TLR4 in trigeminal sensory neurons. J Dent Res. 2011;90(6):759–64.CrossRef
27.
go back to reference Li WW, Guo TZ, Shi X, Birklein F, Schlereth T, Kingery WS, Clark JD. Neuropeptide regulation of adaptive immunity in the tibia fracture model of complex regional pain syndrome. J Neuroinflammation. 2018;15(1):105.CrossRef Li WW, Guo TZ, Shi X, Birklein F, Schlereth T, Kingery WS, Clark JD. Neuropeptide regulation of adaptive immunity in the tibia fracture model of complex regional pain syndrome. J Neuroinflammation. 2018;15(1):105.CrossRef
28.
go back to reference Boonen B, Alpizar YA, Meseguer VM, Talavera K. TRP channels as sensors of bacterial endotoxins. Toxins (Basel). 2018;10(8):326.CrossRef Boonen B, Alpizar YA, Meseguer VM, Talavera K. TRP channels as sensors of bacterial endotoxins. Toxins (Basel). 2018;10(8):326.CrossRef
29.
go back to reference Yin S, Wang P, Xing R, Zhao L, Li X, Zhang L, Xiao Y. Transient receptor potential ankyrin 1 (TRPA1) mediates lipopolysaccharide (LPS)-induced inflammatory responses in primary human osteoarthritic fibroblast-like synoviocytes. Inflammation. 2018;41(2):700–9.CrossRef Yin S, Wang P, Xing R, Zhao L, Li X, Zhang L, Xiao Y. Transient receptor potential ankyrin 1 (TRPA1) mediates lipopolysaccharide (LPS)-induced inflammatory responses in primary human osteoarthritic fibroblast-like synoviocytes. Inflammation. 2018;41(2):700–9.CrossRef
30.
go back to reference Mazgaeen L, Gurung P. Recent advances in lipopolysaccharide recognition systems. Int J Mol Sci. 2020;21(2):379.CrossRef Mazgaeen L, Gurung P. Recent advances in lipopolysaccharide recognition systems. Int J Mol Sci. 2020;21(2):379.CrossRef
31.
go back to reference El Karim I, McCrudden MT, Linden GJ, Abdullah H, Curtis TM, McGahon M, About I, Irwin C, Lundy FT. TNF-α-induced p38MAPK activation regulates TRPA1 and TRPV4 activity in odontoblast-like cells. Am J Pathol. 2015;185(11):2994–3002.CrossRef El Karim I, McCrudden MT, Linden GJ, Abdullah H, Curtis TM, McGahon M, About I, Irwin C, Lundy FT. TNF-α-induced p38MAPK activation regulates TRPA1 and TRPV4 activity in odontoblast-like cells. Am J Pathol. 2015;185(11):2994–3002.CrossRef
32.
go back to reference Hatano N, Itoh Y, Suzuki H, Muraki Y, Hayashi H, Onozaki K, Wood IC, Beech DJ, Muraki K. Hypoxia-inducible factor-1α (HIF1α) switches on transient receptor potential ankyrin repeat 1 (TRPA1) gene expression via a hypoxia response element-like motif to modulate cytokine release. J Biol Chem. 2012;287(38):31962–72.CrossRef Hatano N, Itoh Y, Suzuki H, Muraki Y, Hayashi H, Onozaki K, Wood IC, Beech DJ, Muraki K. Hypoxia-inducible factor-1α (HIF1α) switches on transient receptor potential ankyrin repeat 1 (TRPA1) gene expression via a hypoxia response element-like motif to modulate cytokine release. J Biol Chem. 2012;287(38):31962–72.CrossRef
33.
go back to reference Kang J, Ding Y, Li B, et al. TRPA1 mediated aggravation of allergic contact dermatitis induced by DINP and regulated by NF-κB activation. Sci Rep. 2017;7:43586.CrossRef Kang J, Ding Y, Li B, et al. TRPA1 mediated aggravation of allergic contact dermatitis induced by DINP and regulated by NF-κB activation. Sci Rep. 2017;7:43586.CrossRef
34.
go back to reference Wu CK, Lin JF, Lee TS, Kou YR, Tarng DC. Role of TRPA1 in tissue damage and kidney disease. Int J Mol Sci. 2021;22(7):3415.CrossRef Wu CK, Lin JF, Lee TS, Kou YR, Tarng DC. Role of TRPA1 in tissue damage and kidney disease. Int J Mol Sci. 2021;22(7):3415.CrossRef
35.
go back to reference Magnusson BO. Pulpotomy in primary molars: long-term clinical and histological evaluation. Int Endod J. 1980;13:143–55.CrossRef Magnusson BO. Pulpotomy in primary molars: long-term clinical and histological evaluation. Int Endod J. 1980;13:143–55.CrossRef
36.
go back to reference Kennedy DB, Kapala JT. The dental pulp: biological considerations of protection and treatment. In: Braham L, Morris E, editors. Textbook of pediatric dentistry. Baltimore: Williams&Wilkins; 1985. p. 237–49. Kennedy DB, Kapala JT. The dental pulp: biological considerations of protection and treatment. In: Braham L, Morris E, editors. Textbook of pediatric dentistry. Baltimore: Williams&Wilkins; 1985. p. 237–49.
37.
go back to reference Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA. 2003;100(10):5807–12.CrossRef Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA. 2003;100(10):5807–12.CrossRef
38.
go back to reference Casagrande L, Cordeiro MM, Nör SA, Nör JE. Dental pulp stem cells in regenerative dentistry. Odontology. 2011;99(1):1–7.CrossRef Casagrande L, Cordeiro MM, Nör SA, Nör JE. Dental pulp stem cells in regenerative dentistry. Odontology. 2011;99(1):1–7.CrossRef
Metadata
Title
Upregulation of TRPA1 and reduction of NF-κB translocation could be part of the immunomodulatory process during primary tooth inflammation
Authors
Kullanun Nukaeow
Namthip Patinotham
Supita Tanasawet
Aunwaya Kaewpitak
Publication date
28-02-2022
Publisher
Springer Nature Singapore
Keyword
Caries
Published in
Odontology / Issue 4/2022
Print ISSN: 1618-1247
Electronic ISSN: 1618-1255
DOI
https://doi.org/10.1007/s10266-022-00696-7

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