The Role of Hypoxia in Periodontal Diseases

Bejna Bozyel; Ahmet Çağlar Kalkan; Burcu Özdemir

EN

The Role of Hypoxia in Periodontal Diseases

Abstract

Environmental and genetic factors are effective in influencing the progression of periodontal diseases that are chronic in nature and are triggered by dysbiotic oral microbiota. Periodontal infection and inflammation are accompanied by hypoxia which is the pathological depletion of oxygen in generalized or localized tissues. Hypoxia, increases the rate of periodontal disease progression and creates related hypoxic changes in periodontal inflammation. Hypoxic changes in tissues are primarily the result of the transcriptional regulatory proteins and hypoxia induced factors. Recently, clinical studies about the relationship between hypoxia and periodontal diseases have been gaining importance throughout the literature. In the present review, we aimed to summarize the association of hypoxia and periodontal disease, depending on the evidence presented in the recent literature.

Keywords

Periodontal diseases, hypoxia, inflammation

References

Aarup, A., Pedersen, T. X., Junker, N., Christoffersen, C., Bartels, E. D., Madsen, M., Nielsen, C. H., & Nielsen, L. B. (2016). Hypoxia-inducible factor-1α expression in macrophages promotes development of atherosclerosis. Arteriosclerosis, thrombosis, and vascular biology, 36(9), 1782-1790.
Afacan, B., Öztürk, V. Ö., Paşalı, Ç., Bozkurt, E., Köse, T., & Emingil, G. (2019). Gingival crevicular fluid and salivary HIF‐1α, VEGF, and TNF‐α levels in periodontal health and disease. Journal of periodontology, 90(7), 788-797.
Afacan, B., Yücel, Z. P. K., Paşali, Ç., İlhan, H. A., Köse, T., & Emingil, G. (2020). Effect of non‐surgical periodontal treatment on gingival crevicular fluid hypoxia inducible factor‐1 alpha, vascular endothelial growth factor and tumour necrosis factor‐alpha levels in generalized aggressive periodontitis patients. Journal of periodontology.
Agis, H., Watzek, G., & Gruber, R. (2012). Prolyl hydroxylase inhibitors increase the production of vascular endothelial growth factor by periodontal fibroblasts. Journal of Periodontal Research, 47(2), 165-173.
Bergström, J., Eliasson, S., & Dock, J. (2000). A 10‐year prospective study of tobacco smoking and periodontal health. Journal of periodontology, 71(8), 1338-1347.
Bergström, J., & Ellasson, S. (1987). Noxious effect of cigarette smoking on periodontal health. Journal of Periodontal Research, 22(6), 513-517.
Biddlestone, J., Bandarra, D., & Rocha, S. (2015). The role of hypoxia in inflammatory disease. International journal of molecular medicine, 35(4), 859-869.
Blouin, C. C., Pagé, E. L., Soucy, G. M., & Richard, D. E. (2004). Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1α. Blood, 103(3), 1124-1130.
Bodden, B.-H. H. M. W. MK Windsor LJ Birkedal-Hansen B DeCarlo A Engler JA 1993 Matrix metalloproteinases: a review. Critical Reviews in Oral Biology and Medicine, 4, 197-250.
Carmeliet, P., Dor, Y., Herbert, J.-M., Fukumura, D., Brusselmans, K., Dewerchin, M., Neeman, M., Bono, F., Abramovitch, R., & Maxwell, P. (1998). Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature, 394(6692), 485-490.

Cetinkaya, B. O., Keles, G. C., Ayas, B., Sakallioglu, E. E., & Acikgoz, G. (2007). The expression of vascular endothelial growth factor in a rat model at destruction and healing stages of periodontal disease. Journal of periodontology, 78(6), 1129-1135.
Cheng, R., Liu, W., Zhang, R., Feng, Y., Bhowmick, N. A., & Hu, T. (2017). Porphyromonas gingivalis-derived lipopolysaccharide combines hypoxia to induce caspase-1 activation in periodontitis. Frontiers in cellular and infection microbiology, 7, 474.
de Araújo, M. F., Etchebehere, R. M., de Melo, M. L. R., Beghini, M., Severino, V. O., de Castro Côbo, E., Rodrigues, D. B. R., & de Lima Pereira, S. A. (2017). Analysis of CD15, CD57 and HIF-1α in biopsies of patients with peri-implantitis. Pathology-Research and Practice, 213(9), 1097-1101.
Déry, M.-A. C., Michaud, M. D., & Richard, D. E. (2005). Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. The international journal of biochemistry & cell biology, 37(3), 535-540.
Eltzschig, H. K., & Carmeliet, P. (2011). Hypoxia and inflammation. New England Journal of Medicine, 364(7), 656-665.
Engebretson, S. P., Emingil, G., & Lamster, I. B. (2003). Inflammatory Response in Periodontal Diseases. Fundamentals of Periodontics, 2nd ed. Chicago: Quintessence, 144-157.
Feldser, D., Agani, F., Iyer, N. V., Pak, B., Ferreira, G., & Semenza, G. L. (1999). Reciprocal positive regulation of hypoxia-inducible factor 1α and insulin-like growth factor 2. Cancer research, 59(16), 3915-3918.
Genco, R. J., & LÖE, H. (1993). The role of systemic conditions and disorders in periodontal disease. Periodontology 2000, 2(1), 98-116.
Gold, S. I. (1985). Periodontics. The past: Part (I). Early sources. Journal of clinical periodontology, 12(2), 79-97.
Gonzalez, F. J., Xie, C., & Jiang, C. (2019). The role of hypoxia-inducible factors in metabolic diseases. Nature Reviews Endocrinology, 15(1), 21-32.
Gölz, L., Memmert, S., Rath-Deschner, B., Jäger, A., Appel, T., Baumgarten, G., Götz, W., & Frede, S. (2014). LPS from P. gingivalis and hypoxia increases oxidative stress in periodontal ligament fibroblasts and contributes to periodontitis. Mediators of Inflammation, 2014.
Gölz, L., Memmert, S., Rath-Deschner, B., Jäger, A., Appel, T., Baumgarten, G., Götz, W., & Frede, S. (2015). Hypoxia and P. gingivalis synergistically induce HIF-1 and NF-κB activation in PDL cells and periodontal diseases. Mediators of Inflammation, 2015.
Haber, J., Wattles, J., Crowley, M., Mandell, R., Joshipura, K., & Kent, R. L. (1993). Evidence for cigarette smoking as a major risk factor for periodontitis. Journal of periodontology, 64(1), 16-23.
Haddad, J. J., & Harb, H. L. (2005). Cytokines and the regulation of hypoxia-inducible factor (HIF)-1α. International immunopharmacology, 5(3), 461-483.
Hewitson, K. S., & Schofield, C. J. (2004). The HIF pathway as a therapeutic target. Drug discovery today, 9(16), 704-711.
Hirai, K., Furusho, H., Hirota, K., & Sasaki, H. (2018). Activation of hypoxia-inducible factor 1 attenuates periapical inflammation and bone loss. International journal of oral science, 10(2), 1-10.
Ikeda, E. (2005). Cellular response to tissue hypoxia and its involvement in disease progression. Pathology international, 55(10), 603-610.
Ingman, T., Tervahartiala, T., Ding, Y., Tschesche, H., Haerian, A., Kinane, D. F., Konttinen, Y. T., & Sorsa, T. (1996). Matrix metalloproteinases and their inhibitors in gingival crevicular fluid and saliva of periodontitis patients. Journal of clinical periodontology, 23(12), 1127-1132.
Karatas, O., Balci Yuce, H., Taskan, M. M., Gevrek, F., Lafci, E., & Kasap, H. (2019). Histological evaluation of peri-implant mucosal and gingival tissues in peri-implantitis, peri-implant mucositis and periodontitis patients: a cross-sectional clinical study. Acta Odontologica Scandinavica, 1-9.
Karatas, O., Balci Yuce, H., Tulu, F., Taskan, M. M., Gevrek, F., & Toker, H. (2019). Evaluation of apoptosis and hypoxia‐related factors in gingival tissues of smoker and non‐smoker periodontitis patients. Journal of Periodontal Research.
Karhausen, J., Haase, V. H., & Colgan, S. P. (2005). Inflammatory hypoxia: role of hypoxia-inducible factor. Cell Cycle, 4(2), 255-257.
Kempf, V. A., Lebiedziejewski, M., Alitalo, K., Wälzlein, J.-H., Ehehalt, U., Fiebig, J., Huber, S., Schütt, B., Sander, C. A., & Müller, S. (2005). Activation of hypoxia-inducible factor-1 in bacillary angiomatosis: evidence for a role of hypoxia-inducible factor-1 in bacterial infections. Circulation, 111(8), 1054-1062.
Kim, S. (1985). Regulation of pulpal blood flow. Journal of Dental Research, 64(4), 590-596.
Kim, Y. S., Shin, S. I., Kang, K. L., Chung, J. H., Herr, Y., Bae, W. J., & Kim, E. C. (2012). Nicotine and lipopolysaccharide stimulate the production of MMPs and prostaglandin E2 by hypoxia‐inducible factor‐1α up‐regulation in human periodontal ligament cells. Journal of Periodontal Research, 47(6), 719-728.
Koh, M. Y., & Powis, G. (2012). Passing the baton: the HIF switch. Trends in biochemical sciences, 37(9), 364-372.
Lee, J.-W., Bae, S.-H., Jeong, J.-W., Kim, S.-H., & Kim, K.-W. (2004). Hypoxia-inducible factor (HIF-1) α: its protein stability and biological functions. Experimental & molecular medicine, 36(1), 1-12.
Mendes, R. T., Nguyen, D., Stephens, D., Pamuk, F., Fernandes, D., Hasturk, H., Van Dyke, T. E., & Kantarci, A. (2018). Hypoxia‐induced endothelial cell responses–possible roles during periodontal disease. Clinical and Experimental Dental Research, 4(6), 241-248.
Mettraux, G., Gusberti, F., & Graf, H. (1984). Oxygen tension (pO2) in untreated human periodontal pockets. Journal of periodontology, 55(9), 516-521.
Motohira, H., Hayashi, J., Tatsumi, J., Tajima, M., Sakagami, H., & Shin, K. (2007). Hypoxia and reoxygenation augment bone‐resorbing factor production from human periodontal ligament cells. Journal of periodontology, 78(9), 1803-1809.
Nagase, H., & Woessner, J. F. (1999). Matrix metalloproteinases. Journal of Biological chemistry, 274(31), 21491-21494.
Ng, K. T., Li, J. P., Ng, K. M., Tipoe, G. L., Leung, W. K., & Fung, M. L. (2011). Expression of hypoxia‐inducible factor‐1α in human periodontal tissue. Journal of periodontology, 82(1), 136-141.
Ohuchi, M., & Fujimura, A. (2004). Changes of blood flow in pressure side of periodontal ligament tooth movement. Dent. J. Iwate Med. University, 29, 15-23.
Özer, D. Ö., & Demiralp, B. (2005). Periodontitis Kardiyovasküler Hastaliğa Neden Olur Mu? Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi, 2005(2), 62-70.
Papapanou, P. N., Sanz, M., Buduneli, N., Dietrich, T., Feres, M., Fine, D. H., Flemmig, T. F., Garcia, R., Giannobile, W. V., & Graziani, F. (2018). Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri‐Implant Diseases and Conditions. Journal of periodontology, 89, S173-S182.
Pradeep, A., Prapulla, D., Sharma, A., & Sujatha, P. (2011). Gingival crevicular fluid and serum vascular endothelial growth factor: their relationship in periodontal health, disease and after treatment. Cytokine, 54(2), 200-204.
Ratcliffe, P. J. (2007). HIF-1 and HIF-2: working alone or together in hypoxia? The Journal of clinical investigation, 117(4), 862-865.
Semenza, G. (2011). Regulation of metabolism by hypoxia-inducible factor 1. Cold Spring Harbor symposia on quantitative biology,
Semenza, G. L. (2000). HIF-1 and human disease: one highly involved factor. Genes & development, 14(16), 1983-1991.
Semenza, G. L. (2001). Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends in molecular medicine, 7(8), 345-350.
Semenza, G. L. (2007). Hypoxia-inducible factor 1 (HIF-1) pathway. Science's STKE, 2007(407), cm8-cm8.
Shay, J. E., & Simon, M. C. (2012). Hypoxia-inducible factors: crosstalk between inflammation and metabolism. Seminars in cell & developmental biology,
Shi, Q.-Y., Huang, S.-G., Zeng, J.-H., & Fang, X.-G. (2015). Expression of hypoxia inducible factor-1α and vascular endothelial growth factor-C in human chronic periodontitis. Journal of Dental Sciences, 10(3), 323-333.
Silverstein, P. (1992). Smoking and wound healing. The American journal of medicine, 93(1), S22-S24.
Sorsa, T., Tjäderhane, L., Konttinen, Y. T., Lauhio, A., Salo, T., Lee, H. M., Golub, L. M., Brown, D. L., & Mäntylä, P. (2006). Matrix metalloproteinases: contribution to pathogenesis, diagnosis and treatment of periodontal inflammation. Annals of medicine, 38(5), 306-321.
Sun, Y., Shu, R., Zhang, M.-Z., & Wu, A.-P. (2008). Toll-like receptor 4 signaling plays a role in triggering periodontal infection. FEMS Immunology & Medical Microbiology, 52(3), 362-369.
Takedachi, M., Iyama, M., Sawada, K., Mori, K., Yamamoto, S., Morimoto, C., Yanagita, M., & Murakami, S. (2017). Hypoxia‐inducible factor‐1α inhibits interleukin‐6 and‐8 production in gingival epithelial cells during hypoxia. Journal of Periodontal Research, 52(1), 127-134.
Tayman, M. A., Kurgan, Ş., Önder, C., Güney, Z., Serdar, M. A., Kantarcı, A., & Günhan, M. (2019). A disintegrin‐like and metalloproteinase with thrombospondin‐1 (ADAMTS‐1) levels in gingival crevicular fluid correlate with vascular endothelial growth factor‐A, hypoxia‐inducible factor‐1α, and clinical parameters in patients with advanced periodontitis. Journal of periodontology, 90(10), 1182-1189.
Toker, H., Balci Yuce, H., Lektemur Alpan, A., Gevrek, F., & Elmastas, M. (2018). Morphometric and histopathological evaluation of the effect of grape seed proanthocyanidin on alveolar bone loss in experimental diabetes and periodontitis. Journal of Periodontal Research, 53(3), 478-486.
Tomar, S. L., & Asma, S. (2000). Smoking‐attributable periodontitis in the United States: findings from NHANES III. Journal of periodontology, 71(5), 743-751.
Tonetti, M. S., Van Dyke, T. E., & workshop*, w. g. o. t. j. E. A. (2013). Periodontitis and atherosclerotic cardiovascular disease: consensus report of the Joint EFP/AAPWorkshop on Periodontitis and Systemic Diseases. Journal of periodontology, 84, S24-S29.
Turnbull, B. (1995). Smoking and periodontal disease. A review. Journal of the New Zealand Society of Periodontology(79), 10-15.
Vasconcelos, R. C., Costa Ade, L., Freitas Rde, A., Bezerra, B. A., Santos, B. R., Pinto, L. P., & Gurgel, B. C. (2016). Immunoexpression of HIF-1alpha and VEGF in Periodontal Disease and Healthy Gingival Tissues. Braz Dent J, 27(2), 117-122. https://doi.org/10.1590/0103-6440201600533
Vasconcelos, R. C., Costa, A. d. L. L., Freitas, R. d. A., Bezerra, B. A. d. A., Santos, B. R. M. d., Pinto, L. P., & Gurgel, B. C. d. V. (2016). Immunoexpression of HIF-1α and VEGF in periodontal disease and healthy gingival tissues. Brazilian dental journal, 27(2), 117-122.
Wang, G. L., Jiang, B. H., Rue, E. A., & Semenza, G. L. (1995). Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A, 92(12), 5510-5514. https://doi.org/10.1073/pnas.92.12.5510
Wu, Y., Cao, H., Yang, Y., Zhou, Y., Gu, Y., Zhao, X., Zhang, Y., Zhao, Z., Zhang, L., & Yin, J. (2013). Effects of vascular endothelial cells on osteogenic differentiation of noncontact co‐cultured periodontal ligament stem cells under hypoxia. Journal of Periodontal Research, 48(1), 52-65.
Xu, Q., Liu, Z., Guo, L., Liu, R., Li, R., Chu, X., Yang, J., Luo, J., Chen, F., & Deng, M. (2019). Hypoxia Mediates Runt-Related Transcription Factor 2 Expression via Induction of Vascular Endothelial Growth Factor in Periodontal Ligament Stem Cells. Molecules and cells, 42(11), 763.
Yu, X.-J., Xiao, C.-J., Du, Y.-M., Liu, S., Du, Y., & Li, S. (2015). Effect of hypoxia on the expression of RANKL/OPG in human periodontal ligament cells in vitro. International journal of clinical and experimental pathology, 8(10), 12929.
Zhu, H., & Bunn, H. F. (2001). How do cells sense oxygen? Science, 292(5516), 449-451.

Details

Primary Language

English

Subjects

Dentistry

Journal Section

Review

Authors

Bejna Bozyel ^*
0000-0002-9558-8139
Türkiye

Ahmet Çağlar Kalkan
0000-0001-7649-6290
Türkiye

Burcu Özdemir
0000-0003-0356-7769
Türkiye

Publication Date

April 30, 2021

Submission Date

February 24, 2021

Acceptance Date

April 26, 2021

Published in Issue

Year 2021 Volume: 3 Number: 1

IZ

https://izlik.org/JA77AZ83HW

APA

Bozyel, B., Kalkan, A. Ç., & Özdemir, B. (2021). The Role of Hypoxia in Periodontal Diseases. Journal of Gazi University Health Sciences Institute, 3(1), 36-44. https://izlik.org/JA77AZ83HW

AMA

1.Bozyel B, Kalkan AÇ, Özdemir B. The Role of Hypoxia in Periodontal Diseases. GUHES. 2021;3(1):36-44. https://izlik.org/JA77AZ83HW

Chicago

Bozyel, Bejna, Ahmet Çağlar Kalkan, and Burcu Özdemir. 2021. “The Role of Hypoxia in Periodontal Diseases”. Journal of Gazi University Health Sciences Institute 3 (1): 36-44. https://izlik.org/JA77AZ83HW.

EndNote

Bozyel B, Kalkan AÇ, Özdemir B (April 1, 2021) The Role of Hypoxia in Periodontal Diseases. Journal of Gazi University Health Sciences Institute 3 1 36–44.

IEEE

[1]B. Bozyel, A. Ç. Kalkan, and B. Özdemir, “The Role of Hypoxia in Periodontal Diseases”, GUHES, vol. 3, no. 1, pp. 36–44, Apr. 2021, [Online]. Available: https://izlik.org/JA77AZ83HW

ISNAD

Bozyel, Bejna - Kalkan, Ahmet Çağlar - Özdemir, Burcu. “The Role of Hypoxia in Periodontal Diseases”. Journal of Gazi University Health Sciences Institute 3/1 (April 1, 2021): 36-44. https://izlik.org/JA77AZ83HW.

JAMA

1.Bozyel B, Kalkan AÇ, Özdemir B. The Role of Hypoxia in Periodontal Diseases. GUHES. 2021;3:36–44.

MLA

Bozyel, Bejna, et al. “The Role of Hypoxia in Periodontal Diseases”. Journal of Gazi University Health Sciences Institute, vol. 3, no. 1, Apr. 2021, pp. 36-44, https://izlik.org/JA77AZ83HW.

Vancouver

1.Bejna Bozyel, Ahmet Çağlar Kalkan, Burcu Özdemir. The Role of Hypoxia in Periodontal Diseases. GUHES [Internet]. 2021 Apr. 1;3(1):36-44. Available from: https://izlik.org/JA77AZ83HW

Abstract

The Role of Hypoxia in Periodontal Diseases

Abstract

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References

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