Localization and expression profiles of gingival monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1)

Lili Yu; Yigit Firatli; Samira Elmanfi; Mervi Gürsoy; Meltem Özdemir Kabalak; Gökhan Kasnak; Pirkko Pussinen; Floris J. Bikker; Feriha Caglayan; Erhan Firatli; Ulvi Kahraman Gürsoy

doi:10.1007/s00784-023-05010-5

Localization and expression profiles of gingival monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1)

Lili Yu, Yigit Firatli, Samira Elmanfi, Mervi Gürsoy, Meltem Özdemir Kabalak, Gökhan Kasnak, Pirkko Pussinen, Floris J. Bikker, Feriha Caglayan, Erhan Firatli, Ulvi Kahraman Gürsoy^*

^*Corresponding author for this work

Oral Biochemistry

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Objectives: The purposes of this study were to localize monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and its suppressor mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1) in gingival tissues and to profile their protein expression levels in relation to the clinical inflammation, Porphyromonas gingivalis colonization, and interleukin (IL)-8 levels. Materials and methods: Study samples were collected from two independent study populations: (1) Gingival tissues were collected from eight periodontally healthy individuals and eight periodontitis patients to localize MCPIP-1 and MALT-1 immunohistochemically, and (2) forty-one gingival tissue samples with marginal, mild, or moderate to severe inflammation were collected from 20 periodontitis patients to determine MCPIP-1 and MALT-1 levels using immunoblots, P. gingivalis levels with qPCR, P. gingivalis gingipain activities with fluorogenic substrates, and IL-8 levels with multiplex technique. Results: MCPIP-1 was detectable in the epithelium and in connective tissue, being especially prominent around the blood vessel walls in healthy periodontal tissues. MALT-1 was observed at all layers of gingival epithelium and especially around the accumulated inflammatory cells in connective tissue. No difference in gingival tissue MCPIP-1 and MALT-1 levels was observed in relation to the severity of gingival inflammation. MALT-1 levels were elevated (p = 0.023) with the increase in tissue P. gingivalis levels, and there was an association between MALT-1 and IL-8 levels (β = 0.054, p = 0.001). Conclusions: Interactions of MALT-1 levels with gingival tissue P. gingivalis counts and IL-8 levels suggest that activation of MALT-1 can take part in P. gingivalis-regulated host immune responses. Clinical relevance: Pharmacological targeting the crosstalk between immune response and MCPIP-1/MALT-1 may have benefits in periodontal treatment.

Original language	English
Pages (from-to)	2065-2074
Number of pages	10
Journal	Clinical Oral Investigations
Volume	27
Issue number	5
Early online date	3 Apr 2023
DOIs	https://doi.org/10.1007/s00784-023-05010-5
Publication status	Published - May 2023

Bibliographical note

Funding Information:
This study was partly supported by SHS the Finnish Dental Society Apollonia, Helsinki, Finland (U.K.G.), and Minerva Foundation, Helsinki, Finland (U.K.G.). The authors are grateful for the technical assistance of Katja Sampalahti, Oona Hällfors, and Tatjana Peskova from the University of Turku.

Funding Information:
Open Access funding provided by University of Turku (UTU) including Turku University Central Hospital. This study was partly supported by SHS the Finnish Dental Society Apollonia, Helsinki, Finland (U.K.G.), and Minerva Foundation, Helsinki, Finland (U.K.G.).

Publisher Copyright:
© 2023, The Author(s).

Funding

This study was partly supported by SHS the Finnish Dental Society Apollonia, Helsinki, Finland (U.K.G.), and Minerva Foundation, Helsinki, Finland (U.K.G.). The authors are grateful for the technical assistance of Katja Sampalahti, Oona Hällfors, and Tatjana Peskova from the University of Turku. Open Access funding provided by University of Turku (UTU) including Turku University Central Hospital. This study was partly supported by SHS the Finnish Dental Society Apollonia, Helsinki, Finland (U.K.G.), and Minerva Foundation, Helsinki, Finland (U.K.G.).

Keywords

Interleukin-8
MALT-1 protein
MCPIP1 protein, Human/Regnase-1 protein, human
Porphyromonas gingivalis

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10.1007/s00784-023-05010-5

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Yu, L., Firatli, Y., Elmanfi, S., Gürsoy, M., Özdemir Kabalak, M., Kasnak, G., Pussinen, P., Bikker, F. J., Caglayan, F., Firatli, E., & Gürsoy, U. K. (2023). Localization and expression profiles of gingival monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1). Clinical Oral Investigations, 27(5), 2065-2074. https://doi.org/10.1007/s00784-023-05010-5

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abstract = "Objectives: The purposes of this study were to localize monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and its suppressor mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1) in gingival tissues and to profile their protein expression levels in relation to the clinical inflammation, Porphyromonas gingivalis colonization, and interleukin (IL)-8 levels. Materials and methods: Study samples were collected from two independent study populations: (1) Gingival tissues were collected from eight periodontally healthy individuals and eight periodontitis patients to localize MCPIP-1 and MALT-1 immunohistochemically, and (2) forty-one gingival tissue samples with marginal, mild, or moderate to severe inflammation were collected from 20 periodontitis patients to determine MCPIP-1 and MALT-1 levels using immunoblots, P. gingivalis levels with qPCR, P. gingivalis gingipain activities with fluorogenic substrates, and IL-8 levels with multiplex technique. Results: MCPIP-1 was detectable in the epithelium and in connective tissue, being especially prominent around the blood vessel walls in healthy periodontal tissues. MALT-1 was observed at all layers of gingival epithelium and especially around the accumulated inflammatory cells in connective tissue. No difference in gingival tissue MCPIP-1 and MALT-1 levels was observed in relation to the severity of gingival inflammation. MALT-1 levels were elevated (p = 0.023) with the increase in tissue P. gingivalis levels, and there was an association between MALT-1 and IL-8 levels (β = 0.054, p = 0.001). Conclusions: Interactions of MALT-1 levels with gingival tissue P. gingivalis counts and IL-8 levels suggest that activation of MALT-1 can take part in P. gingivalis-regulated host immune responses. Clinical relevance: Pharmacological targeting the crosstalk between immune response and MCPIP-1/MALT-1 may have benefits in periodontal treatment.",

keywords = "Interleukin-8, MALT-1 protein, MCPIP1 protein, Human/Regnase-1 protein, human, Porphyromonas gingivalis",

author = "Lili Yu and Yigit Firatli and Samira Elmanfi and Mervi G{\"u}rsoy and \{{\"O}zdemir Kabalak\}, Meltem and G{\"o}khan Kasnak and Pirkko Pussinen and Bikker, \{Floris J.\} and Feriha Caglayan and Erhan Firatli and G{\"u}rsoy, \{Ulvi Kahraman\}",

note = "Funding Information: This study was partly supported by SHS the Finnish Dental Society Apollonia, Helsinki, Finland (U.K.G.), and Minerva Foundation, Helsinki, Finland (U.K.G.). The authors are grateful for the technical assistance of Katja Sampalahti, Oona H{\"a}llfors, and Tatjana Peskova from the University of Turku. Funding Information: Open Access funding provided by University of Turku (UTU) including Turku University Central Hospital. This study was partly supported by SHS the Finnish Dental Society Apollonia, Helsinki, Finland (U.K.G.), and Minerva Foundation, Helsinki, Finland (U.K.G.). Publisher Copyright: {\textcopyright} 2023, The Author(s).",

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month = may,

doi = "10.1007/s00784-023-05010-5",

language = "English",

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Yu, L, Firatli, Y, Elmanfi, S, Gürsoy, M, Özdemir Kabalak, M, Kasnak, G, Pussinen, P, Bikker, FJ, Caglayan, F, Firatli, E & Gürsoy, UK 2023, 'Localization and expression profiles of gingival monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1)', Clinical Oral Investigations, vol. 27, no. 5, pp. 2065-2074. https://doi.org/10.1007/s00784-023-05010-5

Localization and expression profiles of gingival monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1). / Yu, Lili; Firatli, Yigit; Elmanfi, Samira et al.
In: Clinical Oral Investigations, Vol. 27, No. 5, 05.2023, p. 2065-2074.

Research output: Contribution to Journal › Article › Academic › peer-review

TY - JOUR

T1 - Localization and expression profiles of gingival monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1)

AU - Yu, Lili

AU - Firatli, Yigit

AU - Elmanfi, Samira

AU - Gürsoy, Mervi

AU - Özdemir Kabalak, Meltem

AU - Kasnak, Gökhan

AU - Pussinen, Pirkko

AU - Bikker, Floris J.

AU - Caglayan, Feriha

AU - Firatli, Erhan

AU - Gürsoy, Ulvi Kahraman

N1 - Funding Information: This study was partly supported by SHS the Finnish Dental Society Apollonia, Helsinki, Finland (U.K.G.), and Minerva Foundation, Helsinki, Finland (U.K.G.). The authors are grateful for the technical assistance of Katja Sampalahti, Oona Hällfors, and Tatjana Peskova from the University of Turku. Funding Information: Open Access funding provided by University of Turku (UTU) including Turku University Central Hospital. This study was partly supported by SHS the Finnish Dental Society Apollonia, Helsinki, Finland (U.K.G.), and Minerva Foundation, Helsinki, Finland (U.K.G.). Publisher Copyright: © 2023, The Author(s).

PY - 2023/5

Y1 - 2023/5

N2 - Objectives: The purposes of this study were to localize monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and its suppressor mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1) in gingival tissues and to profile their protein expression levels in relation to the clinical inflammation, Porphyromonas gingivalis colonization, and interleukin (IL)-8 levels. Materials and methods: Study samples were collected from two independent study populations: (1) Gingival tissues were collected from eight periodontally healthy individuals and eight periodontitis patients to localize MCPIP-1 and MALT-1 immunohistochemically, and (2) forty-one gingival tissue samples with marginal, mild, or moderate to severe inflammation were collected from 20 periodontitis patients to determine MCPIP-1 and MALT-1 levels using immunoblots, P. gingivalis levels with qPCR, P. gingivalis gingipain activities with fluorogenic substrates, and IL-8 levels with multiplex technique. Results: MCPIP-1 was detectable in the epithelium and in connective tissue, being especially prominent around the blood vessel walls in healthy periodontal tissues. MALT-1 was observed at all layers of gingival epithelium and especially around the accumulated inflammatory cells in connective tissue. No difference in gingival tissue MCPIP-1 and MALT-1 levels was observed in relation to the severity of gingival inflammation. MALT-1 levels were elevated (p = 0.023) with the increase in tissue P. gingivalis levels, and there was an association between MALT-1 and IL-8 levels (β = 0.054, p = 0.001). Conclusions: Interactions of MALT-1 levels with gingival tissue P. gingivalis counts and IL-8 levels suggest that activation of MALT-1 can take part in P. gingivalis-regulated host immune responses. Clinical relevance: Pharmacological targeting the crosstalk between immune response and MCPIP-1/MALT-1 may have benefits in periodontal treatment.

AB - Objectives: The purposes of this study were to localize monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and its suppressor mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1) in gingival tissues and to profile their protein expression levels in relation to the clinical inflammation, Porphyromonas gingivalis colonization, and interleukin (IL)-8 levels. Materials and methods: Study samples were collected from two independent study populations: (1) Gingival tissues were collected from eight periodontally healthy individuals and eight periodontitis patients to localize MCPIP-1 and MALT-1 immunohistochemically, and (2) forty-one gingival tissue samples with marginal, mild, or moderate to severe inflammation were collected from 20 periodontitis patients to determine MCPIP-1 and MALT-1 levels using immunoblots, P. gingivalis levels with qPCR, P. gingivalis gingipain activities with fluorogenic substrates, and IL-8 levels with multiplex technique. Results: MCPIP-1 was detectable in the epithelium and in connective tissue, being especially prominent around the blood vessel walls in healthy periodontal tissues. MALT-1 was observed at all layers of gingival epithelium and especially around the accumulated inflammatory cells in connective tissue. No difference in gingival tissue MCPIP-1 and MALT-1 levels was observed in relation to the severity of gingival inflammation. MALT-1 levels were elevated (p = 0.023) with the increase in tissue P. gingivalis levels, and there was an association between MALT-1 and IL-8 levels (β = 0.054, p = 0.001). Conclusions: Interactions of MALT-1 levels with gingival tissue P. gingivalis counts and IL-8 levels suggest that activation of MALT-1 can take part in P. gingivalis-regulated host immune responses. Clinical relevance: Pharmacological targeting the crosstalk between immune response and MCPIP-1/MALT-1 may have benefits in periodontal treatment.

KW - Interleukin-8

KW - MALT-1 protein

KW - MCPIP1 protein, Human/Regnase-1 protein, human

KW - Porphyromonas gingivalis

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JO - Clinical Oral Investigations

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Yu L, Firatli Y, Elmanfi S, Gürsoy M, Özdemir Kabalak M, Kasnak G et al. Localization and expression profiles of gingival monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1). Clinical Oral Investigations. 2023 May;27(5):2065-2074. Epub 2023 Apr 3. doi: 10.1007/s00784-023-05010-5

Localization and expression profiles of gingival monocyte chemoattractant protein-1-induced protein-1 (MCPIP-1) and mucosa-associated lymphoid tissue lymphoma translocation protein 1 (MALT-1)

Abstract

Bibliographical note

Funding

Keywords

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