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Psychological stress: neuroimmune roles in periodontal disease

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Abstract

Periodontitis is a chronic inflammatory disease that starts with pathogenic bacteria and is mediated by a combination of multiple factors. Psychosomatic factors are considered to be one of the most critical risk factors for periodontal disease. Psychological stress may threaten periodontal immune homeostasis in multiple ways by affecting the hypothalamic–pituitary–adrenal cortex system, the locus ceruleus–sympathetic–adrenal medulla system, and the peptidergic nervous system. In this review, we outline the complex role of psychological stress in promoting the development of periodontal disease, focusing on the effects of stress on flora metabolism, tissue inflammation, and alveolar bone homeostasis. At the same time, we broadly and deeply summarize the potential mechanisms of psychological stress-induced periodontal disease, emphasize the importance of neuroimmune modulation for periodontal health, and expect to provide a new perspective for periodontal science based on psychoneuroimmunology.

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The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Chen MX, Zhong YJ, Dong QQ, Wong HM, Wen YF. Global, regional, and national burden of severe periodontitis, 1990–2019: an analysis of the global burden of disease study 2019. J Clin Periodontol. 2021;48:1165–88.

    Article  PubMed  Google Scholar 

  2. Jiao J, Jing W, Si Y, Feng X, Tai B, Hu D, Lin H, Wang B, Wang C, Zheng S, Liu X, Rong W, Wang W, Li W, Meng H, Wang X. The prevalence and severity of periodontal disease in Mainland china: data from the fourth national oral health survey (2015–2016). J Clin Periodontol. 2021;48:168–79.

    Article  PubMed  Google Scholar 

  3. Iao S, Pei X, Ouyang X, Liu J, Liu W, Cao C. Natural progression of periodontal diseases in Chinese villagers based on the 2018 classification. J Periodontol. 2021;92:1232–42.

    Article  PubMed  Google Scholar 

  4. Akcali A, Huck O, Tenenbaum H, Davideau JL, Buduneli N. Periodontal diseases and stress: a brief review. J Oral Rehabil. 2013;40:60–8.

    Article  PubMed  Google Scholar 

  5. Spector AM, Postolache TT, Akram F, Scott AJ, Wadhawan A, Reynolds MA. Psychological stress: a predisposing and exacerbating factor in periodontitis. Current Oral Health Reports. 2020;7:208–15.

    Article  Google Scholar 

  6. D’Ambrosio F, Caggiano M, Schiavo L, Savarese G, Carpinelli L, Amato A, Iandolo A. Chronic stress and depression in periodontitis and peri-implantitis: a narrative review on neurobiological, neurobehavioral and immune-microbiome interplays and clinical management implications. Dent J. 2022. https://doi.org/10.3390/dj10030049.

    Article  Google Scholar 

  7. Genco RJ, Ho AW, Kopman J, Grossi SG, Dunford RG, Tedesco LA. Models to evaluate the role of stress in periodontal disease. Ann Periodontol. 1998;3:288–302.

    Article  PubMed  Google Scholar 

  8. Genco RJ, Ho AW, Grossi SG, Dunford RG, Tedesco LA. Relationship of stress, distress and inadequate coping behaviors to periodontal disease. J Periodontol. 1999;70:711–23.

    Article  PubMed  Google Scholar 

  9. Castro MML, Ferreira RO, Fagundes NCF, Almeida A, Maia LC, Lima RR. Association between Psychological Stress and Periodontitis: a systematic review. Eur J Dent. 2020;14:171–9.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Coelho JMF, Miranda SS, da Cruz SS, Dos Santos DN, Trindade SC, Cerqueira EMM, Passos-Soares JS, Costa M, Figueiredo A, Hintz AM, de Almeida ARB, Pereira MN, de Souza NM, Barreto ML, Gomes-Filho IS. Common mental disorder is associated with periodontitis. J Periodontal Res. 2020;55:221–8.

    Article  PubMed  Google Scholar 

  11. Coelho JMF, Miranda SS, da Cruz SS, Trindade SC, Passos-Soares JS, Cerqueira EMM, Costa M, Figueiredo A, Hintz AM, Barreto ML, Seymour GJ, Scannapieco F, Gomes-Filho IS. Is there association between stress and periodontitis? Clin Oral Investig. 2020;24:2285–94.

    Article  PubMed  Google Scholar 

  12. Tanveer A, S, Afaq A, Alqutub N, Aldahiyan N, AlMubarak M, Shaikh C, Naseem M, Vohra F, Abduljabbar T. Association of Self-Perceived Psychological Stress with the Periodontal Health of Socially Deprived Women in Shelter Homes. Int J Environ Res Public Health. 2021;18:5160.

    Article  Google Scholar 

  13. Wimmer G, Janda M, Wieselmann-Penkner K, Jakse N, Polansky R, Pertl C. Coping with stress: its influence on periodontal disease. J Periodontol. 2002;73:1343–51.

    Article  PubMed  Google Scholar 

  14. Li Q, Zhao Y, Deng D, Yang J, Chen Y, Liu J, Zhang M. Aggravating effects of psychological stress on ligature-induced periodontitis via the involvement of local oxidative damage and nf-kappab activation. Mediators Inflamm. 2022;2022:6447056.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Breivik T, Gundersen Y, Myhrer T, Fonnum F, Osmundsen H, Murison R, Gjermo P, von Horsten S, Opstad PK. Enhanced susceptibility to periodontitis in an animal model of depression: reversed by chronic treatment with the anti-depressant tianeptine. J Clin Periodontol. 2006;33:469–77.

    Article  PubMed  Google Scholar 

  16. Prolo P, Chiappelli F, Fiorucci A, Dovio A, Sartori ML, Angeli A. Psychoneuroimmunology: new avenues of research for the twenty-first century. Ann N Y Acad Sci. 2002;966:400–8.

    Article  PubMed  Google Scholar 

  17. Breivik T, Thrane PS, Murison R, Gjermo P. Emotional stress effects on immunity, gingivitis and periodontitis. Eur J Oral Sci. 1996;104:327–34.

    Article  PubMed  Google Scholar 

  18. Proctor GB. The physiology of salivary secretion. Periodontol. 2000;2016(70):11–25.

    Google Scholar 

  19. Keremi B, Beck A, Fabian TK, Fabian G, Szabo G, Nagy A, Varga G. Stress and Salivary Glands. Curr Pharm Des. 2017;23:4057–65.

    Article  PubMed  Google Scholar 

  20. Kuhn M, Turp JC. Risk factors for bruxism. Swiss Dent J. 2018;128:118–24.

    PubMed  Google Scholar 

  21. Ulrich-Lai YM, Fulton S, Wilson M, Petrovich G, Rinaman L. Stress exposure, food intake and emotional state. Stress. 2015;18:381–99.

    PubMed  PubMed Central  Google Scholar 

  22. Rosania AE, Low KG, McCormick CM, Rosania DA. Stress, depression, cortisol, and periodontal disease. J Periodontol. 2009;80:260–6.

    Article  PubMed  Google Scholar 

  23. Papathanassoglou ED, Giannakopoulou M, Mpouzika M, Bozas E, Karabinis A. Potential effects of stress in critical illness through the role of stress neuropeptides. Nurs Crit Care. 2010;15:204–16.

    Article  PubMed  Google Scholar 

  24. Besedovsky HO, Rey AD. Physiology of psychoneuroimmunology: a personal view. Brain Behav Immun. 2007;21:34–44.

    Article  PubMed  Google Scholar 

  25. Ader R, Felten D, Cohen N. Interactions between the brain and the immune system. Annu Rev Pharmacol Toxicol. 1990;30:561–602.

    Article  PubMed  Google Scholar 

  26. Miller DB, O’Callaghan JP. Neuroendocrine aspects of the response to stress. Metabolism. 2002;51:5–10.

    Article  PubMed  Google Scholar 

  27. de Medeiros GF, Minni AM, Helbling JC, Moisan MP. Chronic stress does not further exacerbate the abnormal psychoneuroendocrine phenotype of Cbg-deficient male mice. Psychoneuroendocrinology. 2016;70:33–7.

    Article  PubMed  Google Scholar 

  28. Richard EM, Helbling JC, Tridon C, Desmedt A, Minni AM, Cador M, Pourtau L, Konsman JP, Mormede P, Moisan MP. Plasma transcortin influences endocrine and behavioral stress responses in mice. Endocrinology. 2010;151:649–59.

    Article  PubMed  Google Scholar 

  29. Taupenot L, Harper KL, O’Connor DT. The chromogranin-secretogranin family. N Engl J Med. 2003;348:1134–49.

    Article  PubMed  Google Scholar 

  30. Saruta J, Tsukinoki K, Sasaguri K, Ishii H, Yasuda M, Osamura YR, Watanabe Y, Sato S. Expression and localization of chromogranin A gene and protein in human submandibular gland. Cells Tissues Organs. 2005;180:237–44.

    Article  PubMed  Google Scholar 

  31. Gallina S, Di Mauro M, D’Amico MA, D’Angelo E, Sablone A, Di Fonso A, Bascelli A, Izzicupo P, Di Baldassarre A. Salivary chromogranin A, but not alpha-amylase, correlates with cardiovascular parameters during high-intensity exercise. Clin Endocrinol (Oxf). 2011;75:747–52.

    Article  PubMed  Google Scholar 

  32. Chojnowska S, Ptaszynska-Sarosiek I, Kepka A, Knas M, Waszkiewicz N. Salivary biomarkers of stress, anxiety and depression. J. Clin Med. 2021;10:517.

    Google Scholar 

  33. Wei P, Keller C, Li L. Neuropeptides in gut-brain axis and their influence on host immunity and stress. Comput Struct Biotechnol J. 2020;18:843–51.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Barik A, Sathyamurthy A, Thompson J, Seltzer M, Levine A, Chesler A. A spinoparabrachial circuit defined by Tacr1 expression drives pain. Elife. 2021. https://doi.org/10.7554/eLife.61135.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Choi S, Hachisuka J, Brett MA, Magee AR, Omori Y, Iqbal N-U-A, Zhang D, DeLisle MM, Wolfson RL, Bai L, Santiago C, Gong S, Goulding M, Heintz N, Koerber HR, Ross SE, Ginty DD. Parallel ascending spinal pathways for affective touch and pain. Nature. 2020;587:258–63.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Fioranelli M, Bottaccioli AG, Bottaccioli F, Bianchi M, Rovesti M, Roccia MG. Stress and Inflammation in coronary artery disease: a review psychoneuroendocrineimmunology-based. Front Immunol. 2018;9:2031.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Yang Y, Bi M, Xiao L, Chen Q, Chen W, Li W, Wu Y, Hu Y, Huang Y. Perceived stress status and sympathetic nervous system activation in young male patients with coronary artery disease in China. Eur J Intern Med. 2015;26:726–30.

    Article  PubMed  Google Scholar 

  38. Zhang B, Zhong W, Yang B, Li Y, Duan S, Huang J, Mao Y. Gene expression profiling reveals candidate biomarkers and probable molecular mechanisms in chronic stress. Bioengineered. 2022;13:6048–60.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Marek-Jozefowicz L, Czajkowski R, Borkowska A, Nedoszytko B, Zmijewski MA, Cubala WJ, Slominski AT. The Brain-Skin axis in psoriasis-psychological, psychiatric, hormonal, and dermatological aspects. Int J Mol Sci. 2022;23(2):669.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Feng X, Zhao Y, Yang T, Song M, Wang C, Yao Y, Fan H. Glucocorticoid-Driven NLRP3 inflammasome activation in hippocampal microglia mediates chronic stress-induced depressive-like behaviors. Front Mol Neurosci. 2019;12:210.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Iwata M, Ota KT, Li XY, Sakaue F, Li N, Dutheil S, Banasr M, Duric V, Yamanashi T, Kaneko K, Rasmussen K, Glasebrook A, Koester A, Song D, Jones KA, Zorn S, Smagin G, Duman RS. Psychological stress activates the inflammasome via release of adenosine triphosphate and stimulation of the purinergic type 2x7 receptor. Biol Psychiatry. 2016;80:12–22.

    Article  PubMed  Google Scholar 

  42. Theoharides TC. The impact of psychological stress on mast cells. Ann Allergy Asthma Immunol. 2020;125:388–92.

    Article  PubMed  Google Scholar 

  43. Ren J, Han X, Lohner H, Liang R, Liang S, Wang H. Serum- and Glucocorticoid-Inducible Kinase 1 promotes alternative macrophage polarization and restrains inflammation through FoxO1 and STAT3 Signaling. J Immunol. 2021;207:268–80.

    Article  PubMed  Google Scholar 

  44. Shin KJ, Lee YJ, Yang YR, Park S, Suh PG, Follo MY, Cocco L, Ryu SH. Molecular mechanisms underlying psychological stress and cancer. Curr Pharm Des. 2016;22:2389–402.

    Article  PubMed  Google Scholar 

  45. Cakmak O, Tasdemir Z, Aral CA, Dundar S, Koca HB. Gingival crevicular fluid and saliva stress hormone levels in patients with chronic and aggressive periodontitis. J Clin Periodontol. 2016;43:1024–31.

    Article  PubMed  Google Scholar 

  46. Rai B, Kaur J, Anand SC, Jacobs R. Salivary stress markers, stress, and periodontitis: a pilot study. J Periodontol. 2011;82:287–92.

    Article  PubMed  Google Scholar 

  47. Lu H, Xu M, Wang F, Liu S, Gu J, Lin S, Zhao L. Chronic stress accelerates ligature-induced periodontitis by suppressing glucocorticoid receptor-alpha signaling. Exp Mol Med. 2016;48: e223.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Duran-Pinedo AE, Solbiati J, Frias-Lopez J. The effect of the stress hormone cortisol on the metatranscriptome of the oral microbiome. NPJ Biofilms Microbiomes. 2018;4:25.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Qin ZY, Gu X, Chen YL, Liu JB, Hou CX, Lin SY, Hao NN, Liang Y, Chen W, Meng HY. Tolllike receptor 4 activates the NLRP3 inflammasome pathway and periodontal inflammaging by inhibiting Bmi1 expression. Int J Mol Med. 2021;47:137–50.

    Article  PubMed  Google Scholar 

  50. Zhu Y, Li Q, Zhou Y, Li W. TLR activation inhibits the osteogenic potential of human periodontal ligament stem cells through Akt signaling in a Myd88- or TRIF-dependent manner. J Periodontol. 2019;90:400–15.

    Article  PubMed  Google Scholar 

  51. Guo R, Huang Y, Liu H, Zheng Y, Jia L, Li W. Long Non-Coding RNA H19 Participates in periodontal inflammation via activation of autophagy. J Inflamm Res. 2020;13:635–46.

    Article  PubMed  PubMed Central  Google Scholar 

  52. AlQranei MS, Senbanjo LT, Aljohani H, Hamza T, Chellaiah MA. Lipopolysaccharide- TLR-4 Axis regulates Osteoclastogenesis independent of RANKL/RANK signaling. BMC Immunol. 2021;22:23.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Swanson KV, Deng M, Ting JP. The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat Rev Immunol. 2019;19:477–89.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Jurberg AD, Cotta-de-Almeida V, Temerozo JR, Savino W, Bou-Habib DC, Riederer I. Neuroendocrine control of macrophage development and function. Front Immunol. 2018;9:1440.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Dattilo V, Amato R, Perrotti N, Gennarelli M. The Emerging role of SGK1 (Serum- and Glucocorticoid-Regulated Kinase 1) in major depressive disorder: hypothesis and mechanisms. Front Genet. 2020;11:826.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Menke A, Nitschke F, Hellmuth A, Helmel J, Wurst C, Stonawski S, Blickle M, Weiss C, Weber H, Hommers L, Domschke K, Deckert J. Stress impairs response to antidepressants via HPA axis and immune system activation. Brain Behav Immun. 2021;93:132–40.

    Article  PubMed  Google Scholar 

  57. Furlan PM, Ten Have T, Cary M, Zemel B, Wehrli F, Katz IR, Gettes DR, Evans DL. The role of stress-induced cortisol in the relationship between depression and decreased bone mineral density. Biol Psychiatry. 2005;57:911–7.

    Article  PubMed  Google Scholar 

  58. Ng JS, Chin KY. Potential mechanisms linking psychological stress to bone health. Int J Med Sci. 2021;18:604–14.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Han L, Wang B, Wang R, Gong S, Chen G, Xu W. The shift in the balance between osteoblastogenesis and adipogenesis of mesenchymal stem cells mediated by glucocorticoid receptor. Stem Cell Res Ther. 2019;10:377.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Sousa LH, Moura EV, Queiroz AL, Val D, Chaves H, Lisboa M, Furlaneto F, Brito GA, Goes P. Effects of glucocorticoid-induced osteoporosis on bone tissue of rats with experimental periodontitis. Arch Oral Biol. 2017;77:55–61.

    Article  PubMed  Google Scholar 

  61. Canalis E, Mazziotti G, Giustina A, Bilezikian JP. Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int. 2007;18:1319–28.

    Article  PubMed  Google Scholar 

  62. Mesa F, Magan-Fernandez A, Munoz R, Papay-Ramirez L, Poyatos R, Sanchez-Fernandez E, Galindo-Moreno P, Rodriguez-Barranco M. Catecholamine metabolites in urine, as chronic stress biomarkers, are associated with higher risk of chronic periodontitis in adults. J Periodontol. 2014;85:1755–62.

    Article  PubMed  Google Scholar 

  63. Takada T, Yoshinari N, Sugiishi S, Kawase H, Yamane T, Noguchi T. Effect of restraint stress on the progression of experimental periodontitis in rats. J Periodontol. 2004;75:306–15.

    Article  PubMed  Google Scholar 

  64. Lu H, Xu M, Wang F, Liu S, Gu J, Lin S. Chronic stress enhances progression of periodontitis via alpha1-adrenergic signaling: a potential target for periodontal disease therapy. Exp Mol Med. 2014;46: e118.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Breivik T, Gundersen Y, Opstad PK, Fonnum F. Chemical sympathectomy inhibits periodontal disease in Fischer 344 rats. J Periodontal Res. 2005;40:325–30.

    Article  PubMed  Google Scholar 

  66. Muramatsu R, Sato T, Hamamura K, Miyazawa K, Takeguchi A, Tabuchi M, Togari A, Goto S. Guanabenz inhibits alveolar bone resorption in a rat model of periodontitis. J Pharmacol Sci. 2021;147:294–304.

    Article  PubMed  Google Scholar 

  67. Hironaka M, Ansai T, Soh I, Ishisaka A, Awano S, Yoshida A, Hamasaki T, Sonoki K, Takata Y, Takehara T. Association between salivary levels of chromogranin A and periodontitis in older Japanese. Biomed Res. 2008;29:125–30.

    Article  PubMed  Google Scholar 

  68. Matsumoto T, Asakura H, Hayashi T. Increased salivary chromogranin A in women with severe negative mood states in the premenstrual phase. J Psychosom Obstet Gynaecol. 2012;33:120–8.

    Article  PubMed  Google Scholar 

  69. Reshma AP, Arunachalam R, Pillai JK, Kurra SB, Varkey VK, Prince MJ. Chromogranin a: novel biomarker between periodontal disease and psychosocial stress. J Indian Soc Periodontol. 2013;17:214–8.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Boyanova L. Stress hormone epinephrine (adrenaline) and norepinephrine (noradrenaline) effects on the anaerobic bacteria. Anaerobe. 2017;44:13–9.

    Article  PubMed  Google Scholar 

  71. Pillai DK, Cha E, Mosier D. Role of the stress-associated chemicals norepinephrine, epinephrine and substance P in dispersal of Mannheimia haemolytica from biofilms. Vet Microbiol. 2018;215:11–7.

    Article  PubMed  Google Scholar 

  72. Ozuna H, Uriarte SM, Demuth DR. The hunger games: Aggregatibacter actinomycetemcomitans Exploits human neutrophils as an epinephrine source for survival. Front Immunol. 2021;12: 707096.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Jentsch HF, Marz D, Kruger M. The effects of stress hormones on growth of selected periodontitis related bacteria. Anaerobe. 2013;24:49–54.

    Article  PubMed  Google Scholar 

  74. Sharma D, Farrar JD. Adrenergic regulation of immune cell function and inflammation. Semin Immunopathol. 2020;42:709–17.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Moraes RM, Elefteriou F, Anbinder AL. Response of the periodontal tissues to beta-adrenergic stimulation. Life Sci. 2021;281: 119776.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Chen L, Wang W, Peng X, Liu L, Zhang A, Li X, Ma K, Wang L. alpha1 -Adrenoceptors activate the NLRP3 inflammasome through downregulation of Kir21 in cardiac inflammation. Exp Physiol. 2022;107:589–600.

    Article  PubMed  Google Scholar 

  77. Xin JZ, Wu JM, Hu GM, Gu HJ, Feng YN, Wang SX, Cong WW, Li MZ, Xu WL, Song Y, Xiao H, Zhang YY, Wang L. alpha1-AR overactivation induces cardiac inflammation through NLRP3 inflammasome activation. Acta Pharmacol Sin. 2020;41:311–8.

    Article  PubMed  Google Scholar 

  78. Suryono KJ, Hayashi N, Kataoka M, Shinohara Y, Nagata T. Norepinephrine stimulates calprotectin expression in human monocytic cells. J Periodontal Res. 2006;41:159–64.

    Article  PubMed  Google Scholar 

  79. Gao H, Hou J, Meng H, Zhang X, Zheng Y, Peng L. Proinflammatory effects and mechanisms of calprotectin on human gingival fibroblasts. J Periodontal Res. 2017;52:975–83.

    Article  PubMed  Google Scholar 

  80. Nakamura T, Kido J, Kido R, Ohishi K, Yamauchi N, Kataoka M, Nagata T. The association of calprotectin level in gingival crevicular fluid with gingival index and the activities of collagenase and aspartate aminotransferase in adult periodontitis patients. J Periodontol. 2000;71:361–7.

    Article  PubMed  Google Scholar 

  81. Xiao H, Li H, Wang JJ, Zhang JS, Shen J, An XB, Zhang CC, Wu JM, Song Y, Wang XY, Yu HY, Deng XN, Li ZJ, Xu M, Lu ZZ, Du J, Gao W, Zhang AH, Feng Y, Zhang YY. IL-18 cleavage triggers cardiac inflammation and fibrosis upon beta-adrenergic insult. Eur Heart J. 2018;39:60–9.

    Article  PubMed  Google Scholar 

  82. Zhang D, Shooshtarizadeh P, Laventie BJ, Colin DA, Chich JF, Vidic J, de Barry J, Chasserot-Golaz S, Delalande F, Van Dorsselaer A, Schneider F, Helle K, Aunis D, Prevost G, Metz-Boutigue MH. Two chromogranin a-derived peptides induce calcium entry in human neutrophils by calmodulin-regulated calcium independent phospholipase A2. PLoS ONE. 2009;4: e4501.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Hann J, Bueb JL, Tolle F, Brechard S. Calcium signaling and regulation of neutrophil functions: Still a long way to go. J Leukoc Biol. 2020;107:285–97.

    Article  PubMed  Google Scholar 

  84. Marenzana M, De Souza RL, Chenu C. Blockade of beta-adrenergic signaling does not influence the bone mechano-adaptive response in mice. Bone. 2007;41:206–15.

    Article  PubMed  Google Scholar 

  85. Yirmiya R, Goshen I, Bajayo A, Kreisel T, Feldman S, Tam J, Trembovler V, Csernus V, Shohami E, Bab I. Depression induces bone loss through stimulation of the sympathetic nervous system. Proc Natl Acad Sci U S A. 2006;103:16876–81.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Takeguchi A, Miyazawa K, Sato T, Tabuchi M, Muramatsu R, Maeda H, Togari A, Goto S. Effects of a beta2-adrenergic receptor blocker on experimental periodontitis in spontaneously hypertensive rats. Life Sci. 2021;277: 119593.

    Article  PubMed  Google Scholar 

  87. Breivik T, Gundersen Y, Gjermo P, Fristad I, Opstad PK. Systemic chemical desensitization of peptidergic sensory neurons with resiniferatoxin inhibits experimental periodontitis. Open Dent J. 2011;5:1–6.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Goto T, Kido MA, Yamaza T, Tanaka T. Substance P and substance P receptors in bone and gingival tissues. Med Electron Microsc. 2001;34:77–85.

    Article  PubMed  Google Scholar 

  89. Azuma H, Kido J, Ikedo D, Kataoka M, Nagata T. Substance P enhances the inhibition of osteoblastic cell differentiation induced by lipopolysaccharide from Porphyromonas gingivalis. J Periodontol. 2004;75:974–81.

    Article  PubMed  Google Scholar 

  90. Pradeep AR, Raj S, Aruna G, Chowdhry S. Gingival crevicular fluid and plasma levels of neuropeptide substance-P in periodontal health, disease and after nonsurgical therapy. J Periodontal Res. 2009;44:232–7.

    Article  PubMed  Google Scholar 

  91. Yan K, Lin Q, Tang K, Liu S, Du Y, Yu X, Li S. Substance P participates in periodontitis by upregulating HIF-1alpha and RANKL/OPG ratio. BMC Oral Health. 2020;20:27.

    Article  PubMed  PubMed Central  Google Scholar 

  92. Vasconcelos RC, Costa AdLL, Freitas RdA, Bezerra BAdA, Santos BRMd, Pinto LP, Gurgel BCdV. Immunoexpression of HIF-1α and VEGF in Periodontal disease and healthy gingival tissues. Braz Dent J. 2016;27:117–22.

    Article  PubMed  Google Scholar 

  93. Xiao C, Bai G, Du Y, Jiang H, Yu X. Association of high HIF-1α levels in serous periodontitis with external root resorption by the NFATc1 pathway. J Mol Histol. 2020;51:649–58.

    Article  PubMed  Google Scholar 

  94. Lee HJ, Jeong GS, Pi SH, Lee SI, Bae WJ, Kim SJ, Lee SK, Kim EC. Heme oxygenase-1 protects human periodontal ligament cells against substance P-induced RANKL expression. J Periodontal Res. 2010;45:367–74.

    Article  PubMed  Google Scholar 

  95. An S, Zhang Y, Chen Q, Xiong B, Hao J, Zheng Y, Zhou X, Wang J. Effect of systemic delivery of substance P on experimental tooth movement in rats. Am J Orthod Dentofacial Orthop. 2019;155:642–9.

    Article  PubMed  Google Scholar 

  96. Haririan H, Andrukhov O, Bottcher M, Pablik E, Wimmer G, Moritz A, Rausch-Fan X. Salivary neuropeptides, stress, and periodontitis. J Periodontol. 2018;89:9–18.

    PubMed  Google Scholar 

  97. Wu J-Q, Jiang N, Yu B. Mechanisms of action of neuropeptide Y on stem cells and its potential applications in orthopaedic disorders. World J Stem Cells. 2020. https://doi.org/10.4252/wjsc.v12.i9.986.

    Article  PubMed  PubMed Central  Google Scholar 

  98. Yu Q, Hu F. Zhu T [Correlation between salivary stress markers and clinical parameters of periodontitis]. Shanghai Kou Qiang Yi Xue. 2020;29:93–6.

    PubMed  Google Scholar 

  99. Sato S, Hanada R, Kimura A, Abe T, Matsumoto T, Iwasaki M, Inose H, Ida T, Mieda M, Takeuchi Y, Fukumoto S, Fujita T, Kato S, Kangawa K, Kojima M, Shinomiya K, Takeda S. Central control of bone remodeling by neuromedin U. Nat Med. 2007;13:1234–40.

    Article  PubMed  Google Scholar 

  100. Reineke LC, Neilson JR. Differences between acute and chronic stress granules, and how these differences may impact function in human disease. Biochem Pharmacol. 2019;162:123–31.

    Article  PubMed  Google Scholar 

  101. Caton JG, Armitage G, Berglundh T, Chapple ILC, Jepsen S, Kornman KS, Mealey BL, Papapanou PN, Sanz M, Tonetti MS. A new classification scheme for periodontal and peri-implant diseases and conditions–Introduction and key changes from the 1999 classification. J Clin Periodontol. 2018;45(Suppl 20):S1–8.

    PubMed  Google Scholar 

  102. Herrera D, Retamal-Valdes B, Alonso B, Feres M. Acute periodontal lesions (periodontal abscesses and necrotizing periodontal diseases) and endo-periodontal lesions. J Periodontol. 2018;89(Suppl):1.

    Google Scholar 

  103. Herrera D, Alonso B, de Arriba L, Santa Cruz I, Serrano C, Sanz M. Acute periodontal lesions. Periodontol. 2000;2014(65):149–77.

    Google Scholar 

  104. Rowland RW. Necrotizing ulcerative gingivitis. Ann Periodontol. 1999;4:65–73.

    Article  PubMed  Google Scholar 

  105. Song L-T, Lai W, Li J-S, Mu Y-Z, Li C-Y, Jiang S-Y. The interaction between serum amyloid A and Toll-like receptor 2 pathway regulates inflammatory cytokine secretion in human gingival fibroblasts. J Periodontol. 2020;91:129–37.

    Article  PubMed  Google Scholar 

  106. Kataoka N, Hioki H, Kaneko T, Nakamura K. Psychological stress activates a dorsomedial hypothalamus-medullary raphe circuit driving brown adipose tissue thermogenesis and hyperthermia. Cell Metab. 2014;20:346–58.

    Article  PubMed  Google Scholar 

  107. Goldfarb EV, Rosenberg MD, Seo D, Constable RT, Sinha R. Hippocampal seed connectome-based modeling predicts the feeling of stress. Nat Commun. 2020;11:2650.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Yuan J, Ho T, Coury S, Chahal R, Colich N, Gotlib I. Early life stress, systemic inflammation, and neural correlates of implicit emotion regulation in adolescents. Brain Behav Immun. 2022;105:169–79.

    Article  PubMed  Google Scholar 

  109. Fossati P. Neural correlates of emotion processing: from emotional to social brain. Eur Neuropsychopharmacol. 2012;22(Suppl 3):S487–91.

    Article  PubMed  Google Scholar 

  110. Choi KS, Riva-Posse P, Gross RE, Mayberg HS. Mapping the “Depression Switch” during intraoperative testing of subcallosal cingulate deep brain stimulation. JAMA Neurol. 2015;72:1252–60.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (81873709), Shanghai Health Committee (20204Y0278), and Natural Science Foundation of Shanghai (20ZR1463000)

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  1. Jiayao Zhang and Shuxian Lin have equally contributed to the paper.

Authors and Affiliations

  1. Department of Prosthodontics, Stomatological Hospital and Dental School of Tongji University, Shanghai Engineering Research Center of Tooth Restoration and Regeneration, Shanghai, China

    Jiayao Zhang, Shuxian Lin, Yi Jiao & Weicai Liu

  2. Department of Periodontology, Stomatological Hospital and Dental School of Tongji University, Shanghai Engineering Research Center of Tooth Restoration and Regeneration, Shanghai, China

    Lijun Luo

  3. Shanghai Key Laboratory of Brain Functional Genomics (Ministry of Education), Affiliated Mental Health Center (ECNU), School of Psychology and Cognitive Science, East China Normal University, Shanghai, 200062, China

    Qi Zhang

  4. Shanghai Changning Mental Health Center, Shanghai, 200335, China

    Qi Zhang

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  1. Jiayao Zhang
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  3. Lijun Luo
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  4. Qi Zhang
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Correspondence to Weicai Liu.

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Zhang, J., Lin, S., Luo, L. et al. Psychological stress: neuroimmune roles in periodontal disease. Odontology 111, 554–564 (2023). https://doi.org/10.1007/s10266-022-00768-8

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