Host neuro- immuno-endocrine responses in periodontal disease

Current Pharmaceutical Design

Volumn 20, Issue 29, 2014, Pages 4749-4759

  Rettori, Elisa ^a,c   De Laurentiis, Andrea ^a   Les Dees, W ^b   Endruhn, Axel ^c   Rettori, Valeria ^a  

^a Centre de Estudios Farmacologicos y Botanicos   (Argentina)

^b TEXAS A AND M UNIVERSITY   (United States)

^c DEPARTAMENTO DE CIENCIAS NATURALES Y ANTROPOLOGÍA   (Argentina)

Author keywords

Cytokines; Endocannabinoids; Gingiva; Inflammation; Neuropeptides; Stress

Indexed keywords

ENDOCANNABINOID; OXYTOCIN;

ANATOMY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; CARDIOVASCULAR DISEASE; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; COPING BEHAVIOR; DIABETES MELLITUS; GINGIVA; IMMUNE RESPONSE; IMMUNE SYSTEM; INFLAMMATION; METABOLIC SYNDROME X; MOLECULAR BIOLOGY; NEUROENDOCRINE SYSTEM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PERIODONTAL DISEASE; PERIODONTITIS; PERIODONTIUM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRESS; COMPLICATION; HUMAN; IMMUNOLOGY; NEUROSECRETION; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

CARDIOVASCULAR DISEASES; DIABETES COMPLICATIONS; ENDOCANNABINOIDS; HUMANS; IMMUNE SYSTEM; NEUROSECRETORY SYSTEMS; PERIODONTITIS; STRESS, PHYSIOLOGICAL; STROKE;

EID: 84906232620     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612820666140130204043     Document Type: Article

References (96)

1. Carranza F, Shklar G. The history of periodontology. Chicago: Quintessence 2003.
2. Brut B, Greenwell H, Fiorellini J, et al. Epidemiology of Periodontal Disease. J Periodontol 2005; 76: 1406-19.
3. Dye BA. Global periodontal disease epidemiology. Periodontology 2000 2012; 58: 10-25.
4. Romanelli H, Gonzalez Y, Rivas M, Chiappe V, Gomez M, Macchi R. Periodontal treatment needs in Argentine adult subjects. Acta Odontol Latinoam 2007; 20: 39-47.
5. Loos BG, van der Velden U, Laine ML. Susceptibility. In: Lindhe J, Lang NP, Karring T, Eds. Clinical Periodontology and Implant Dentistry. Iowa: Blackwell Minksgaard 2008; pp: 328-346.
6. Scantamburlo G, Scheen AJ. Role du stress psycho-social dans les maladies complexes. Rev Med Liege 2012; 67: 234-242.
7. Davanian H, Stranneheim H, Bage T, et al. Gene expression profiles in paired gingival biopsies from periodontitis-affected and healthy tissue revealed by massively parallel sequencing. Plos One 2012; 7: 1-12.
8. Peters EWJ, Liezmann C, Klapp BF, Kruse J. The neuroimmune connection interferes with tissue regeneration and chronic inflammatory disease in the skin. Ann NY Acad Sci 2012; 1262: 118-126.
9. Bartold PM, Walsh LJ, Narayanan AS. Molecular and cell biology of the gingiva. Periodontology 2000; 24: 28-55.
10. Damek-Poprawa M, Korostoff J, Gill R, DiRienzo JM. Cell junction remodeling in gingival tissue exposed to a microbial toxin. J Dent Res 2013; 92 (6): 518-523.
11. Caffesse RG, Nasjleti CE, Castelli WA. The role of sulcular environment in controlling epithelial keratinization. J Periodontol 1979; 50: 1-6.
12. Hujoel PP, White BA, García RI, Listgarten MA. The dentogingi-val epithelial surface area revisited. J Periodont Res 2001; 36: 48-55.
13. Tsukamoto Y, Usui M, Yamamoto G, et al. Role of the junctional epithelium in periodontal innate defense and homeostasis. J Perio-dontol Res 2012; 47: 750-757.
14. Fiorellini JP, Kim DM, Ishikawa SO. The Gingiva. Normal Perio-dontium. In: Carranza FA Ed. Carranza's Clinical Periodontology. St. Louis, Missouri. Saunders Elsevier 2006; pp: 46-67.
15. Lindhe J, Karring T, Araujo M. The anatomy of periodontal tissues. Anatomy. In: Lindhe J, Lang NP, Karring T, Eds. Clinical Perio-dontology and Implant Dentistry. Oxford UK: Blackwell Munks-gaard 2008; pp: 3-49.
16. Gyorfi A, Fazekas A, Rosivall L. Neurogenic inflammation and the oral mucosa. J Clin Periodontol 1992; 19: 731-736.
17. Newman MG. The Normal Periodontium.Blood Supply, Lymphatics and Nerves. In Carranza's FA, Ed. Clinical Periodontology. Saunders Elsevier. Missouri 2006; pp: 59-61.
18. Iwasaki K, Komaki M, Yokoyama N, et al. Periodontal ligament stem cells possess the characteristics of pericytes. J Periodontol 2012; Dec 14 Epub.
19. Liu D, Xu J, Liu O, et al. Mesenchymal stem cells derived from inflamed periodontal ligament exhibit impaired immunomodula-tion. J Clin Periodontol 2012; 39: 1174-1182.
20. Park JC, Kim JM, Jung IH, et al. Isolation and characterization of human periodontal ligament (PDL) stem cells (PDLSCs) from the inflamed PDL tissue: in vitro and in vivo evaluations. J ClinPerio-dontol 2011; 38: 721-731.
21. Liang S, Hosur KB, Domon H, Hajishengallis G. Periodontal inflammation and bone loss in aged mice. J Periodontal Res 2010; 45: 574-578.
22. De la Fuente M. Role of neuroimmunomodulation in aging. Neuro-immunomodulation 2008; 15: 213-223.
23. th European Workshop of Pe-riodontology. J Clin Periodontol 2005; 32: 87-107.
24. Offenbacher S. Maternal periodontal infections, prematurity, and growth restriction. Clin Obstet Gynec 2004; 47: 808-821.
25. Mahanonda R, Pichyangkul S. Toll-like receptors and their role in periodontal health and disease. Periodontol 2000 2007; 43: 41-55.
26. Beklen A, Hukkanen M, Richardson R, Konttinen YT. Immunohis-tochemical localization of toll-like receptors 1-10 in periodontitis. Oral Microbiol Immunol 2008; 23: 425-431.
27. Mayank Hans, VeenuMadaan Hans. Toll-like receptors and their dual role in periodontitis: a review. J Oral Sci 2011; 53: 263-271.
28. Kirkwood KL, Taba M Jr, Rossa C, et al. Molecular biology of the host-microbe interaction in periodontal diseases: Selected topics: Molecular signaling aspects of pathogen-mediated bone destruction in periodontal disease. In: Carranza FA, Eds. Carranza's Clinical Periodontology. Saunders-Elsevier 10th edit 2006; pp: 259-282.
29. Breivik T, Sluyter F, Hof M, Cools A. Differential susceptibility to periodontitis in genetically selected Wistar rat lines that differ in their behavioral and endocrinological response to stressors. Behavioral Genetics 2000; 30: 123-130.
30. Belibasakis GN, Bostanci N. The RANKL-OPG system in clinical periodontology. J Clin Periodontol 2012; 39: 239-248.
31. Selye H. A syndrome produced by diverse nocuous agents. Nature 1936; 138: 32
32. Selye H. The general adaptation syndrome and the diseases of adaptation. J Clin Endocrinol 1946; 6: 117-130.
33. Selye H. Stress and disease. Science 1955; 122: 625-631.
34. Bear MF, Connors BW, Paradiso MA. Neuroscience: Exploring the Brain. 3rd ed. Philadelphia: Lippincott 2006.
35. Fristad I, Vandemska-Radunovick K, Fjild K, Wimalawansa SI and Kvinnsland IH. NBK1, NK2, NK3 and CGRP1 receptors identified in rat oral soft tissues and in bone and dental hard tissue cells. Cell Tissue Res 2003; 311: 383-91.
36. Dees WL, Kozlowski GP. Effect of castration and ethanol on amygdaloid substance P immunoreactivity. Neuroendocrinology 1984; 39: 231-35.
37. ÓConnor TM, ÓHalloran DJ and Shanahan F. The stress response and the hypothalamic-pituitary-adrenal axis: from molecule to melancholia. Q J Med 2000; 93: 323-333.
38. Chrousos GP. Stressors, stress and neuroendocrine integration of the adaptive response. In: Stress of life from molecules to man. Czermely P. Edit. Ann New York Acad Scie. New York 1998; 851: 311-335.
39. McEwen BC. Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 2008; 583: 174-185.
40. Dantzer R, O'Connor J, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosc 2008; 9: 46-57.
41. Tymen SD, Rojas IG, Zhou X, Fang ZJ, Zhao Y, Marucha PT. Restrain stress alters neurophil and macrophage phenotypes during wound healing. Brain Behav Immun 2012. pii: S0889-1591(12)00196-1. doi: 10.1016/j.bbi.2012.07.013.
42. Samuel BS, Gordon JI. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci USA 2006; 103: 10011-10016.
43. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immuno-modulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005; 122: 107-118.
44. Clarke MB, Hughes DT, Zhu C, Boedeker EC, Sperandio V. The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci USA 2006; 103: 10420-10426.
45. Zaborina O, Lepine F, Xiao G, et al. Dynorphin activates quórum sensing quinolone signaling in Pseudomonas aeruginosa. PloS Pathog 2007; 3: e35.
46. Akcali A, Huck O, Tenenbaum H, Davideau JL, Buduneli N. Periodontal diseases and stress: a brief review. J Oral Rehabil 2012; 40:60-68.
47. Silverman MN, Sternberg EM. Glucocorticoid regulation of inflammation and its functional correlates: from HPA axis to gluco-corticoid receptor dysfunction. Ann N.Y. AcadSci 2012; 1261: 55-63.
48. Webster JC, Oakley RH, Jewell CM, Cidlowski JA. Proinflamma-tory cytokines regulate human glucocorticoid receptor gene expression and lead to the accumulation of the dominant negative beta isoform: a mechanism for the generation of glucocorticoid resistance. Proc Natl Acad Sci USA 2001; 98: 6865-6870.
49. McGowan PO, Sasaki A, D'Alessio AC, et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 2009; 12: 338-342.
50. Armario A, Davin N, Muñoz-Abellan C, et al. What can we know from pituitary-adrenal hormones about the nature and consequences of exposure to emotional stressors? Cell Mol Neurobiol 2012; 32: 749-758.
51. Erin N, Ersoy Y, Ercan F, Akici A, Oktay S. NK-1 antagonist CP99994 inhibits stress-induced mast cell degranulation in rats. Clin Exper Dermatol 2004; 29: 644-648.
52. Dantzer R, and Kelley KW. Twenty years of research on cytokine-induced sickness behavior. Brain, Behavior Immunity 2007; 21: 153-160.
53. 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: 711-723.
54. 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: 1343-1351.
55. Nagasawa M, Kikusui T, Onaka T, Ohta M. Doǵs gaze at his owner increases owners urinary oxytocin during social interaction. Horm Behav 2009; 55: 434-441.
56. Zak P. The neurobiology of trust. Sci Am 2008; 298: 88-95.
57. Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Ferh E. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 2008; 58: 639-650.
58. Dabrowska J, Hazra R, Ahern TH, et al. Neuroanatomical evidence for reciprocal regulation of the corticotrophin-releasing factor and oxytocin system in the hypothalamus and the bed nucleus of the stria terminalis of the rat: implications for balancing stress and affect. Psychoneuroendocrinology 2011; 36: 1312-1326.
59. Lee HJ, Macbeth AH, Pagana JH, Scott Young 3rd W. Oxytocin: The great facilitator of life. Prog Neurobiol 2009; 88: 127-151.
60. Smith AS, Wang Z. Salubrious effects of oxytocin on social stress-induced deficits. Hormones Behavior 2012; 61: 320-330.
61. Furman D, Chen M, Gotlib I, et al. Variant in oxytocin receptor gene is associated with amygdale volume. Psyconeuroendocrinol-ogy 2011; 36: 891-897.
62. Shinozaki G. The integrated model of serotonin transporter gene variation (5HTTLPR) and the glial cell transporter in stress vulnerability and depression. Med Hypotheses 2012; 78: 410-414.
63. Rodrigues SM, Saslow IR, Garcia N, John OP, Keltner D. Oxyto-cin receptor genetic variation relates to empathy and stress reactivity in humans. Proc Natl Acad Sci USA 2009; 106: 21437-21441.
64. Gaoni Y, Mechoulam R. Isolation, structure and partial synthesis of an active constituent of hashish. J Am ChemSoc 1964; 86: 1646-1647.
65. Mechoulam R, Braun R, Gaoni Y. A stereospecific synthesis of (-) delta 1 and (-) delta 6 -tetrahydrocannabinols. J Am Chem Soc 1967; 89: 4552-4554.
66. Devane WA, Dysarz FA 3rd, Johnson MR, Melvin IS, Howlett AC. Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol 1988; 34: 605-613.
67. Matsuda LA, Lolair SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990; 346: 561-564.
68. Devane WA, Hanus I, Breuer A, et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992; 258: 1946-1949.
69. Riebe CI, Wotjak CT. Endocannabinoids and stress. Stress 2011; 14: 384-397.
70. Mechoulam R, Parker LA. The endocannabinoid system and the brain. Annu Rev Psychol 2013; 64: 6.1-6.27.
71. Burstein SH, Zurier R. Cannabinoids, Endocannabinoids and related analogs in inflammation. The AAPS Journal 2009; 11: 109-111.
72. Nakajima Y, Furuichi Y, Biswas KK, et al. Endocannabinoid, anandamide in gingival tissue regulates the periodontal inflammation through NF-kB pathway inhibition. FEBS Letters 2006; 580: 613-619.
73. Rettori E, De Laurentiis A, Zubilete-Zorrilla M, Rettori V, Elverdin JC. Anti-inflammatory effect of the endocannabinoid anandamide in experimental periodontitis and stress in the rat. Neuroimmuno-modulation 2012; 19: 293-303.
74. Napimoga MN, Benatti BB, Lima FO, et al. Cannabidiol decreases bone resorption by inhibiting RANK/RANKL expression and pro-inflammatory cytokines during experimental periodontitis in rats. Int Immunopharmacol 2009; 9: 216-222.
75. Qian H, Zhao Y, Peng Y, et al. Activation of cannabinoid receptor CB2 regulates osteogenic and osteoclastogenic gene expression in human periodontal ligament cells. J Periodont Res 2010; 45: 504-511.
76. Chavarry NGM, Vettore MV, Sansone C, Sheiham A. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent 2009; 7: 107-127.
77. Preshaw PM, Alba AL, Herrera D, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia 2012; 55: 21-31.
78. Lalla E, and Papapanou PN. Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol 2011; 7: 738-748.
79. Teeuw WJ, Gerdes VF, Loos BG. Effect of periodontal treatment on glycemic control of diabetic patients: a systematic review and meta-analysis. Diabetes Care 2010; 33: 421-427.
80. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005; 54: 1615-1625.
81. Mealey BL, and Oates TW. Diabetes Mellitus and Periodontal Disease. J Priodontol 2006; 77: 1289-1303.
82. Engebretson SP, Hey-Hadavi J, Ehrhardt FJ et al. Gingival crevicu-lar fluid levels of IL-1beta and glycemic control in patients with chronic periodontitis and type 2 diabetes. J Periodontol 2004; 75: 1201-1208.
83. Mattila KJ, Nieminen VV, Valtonen VP, et al. Association between dental health and acute myocardial infarction. BMJ 1989; 298: 779-781.
84. Syrjanen J, Peltola J, Valtonen V, Iivanainen M, Kaste M, Huttu-nen JK. Dental infections in association with cerebral infarction in Young and middle-aged men. J intern Med 1989; 225: 179-184.
85. Belstrom D, Damgaard C, Nielsen CH, Holmstrup P. Does a causal relation between cardiovascular disease and periodontitis exist? Microbes Infection 2012; 14: 411-418.
86. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation 2002; 105: 1135-1143.
87. Inaha P, Amano A. Roles of oral bacteria in cardiovascular diseases - from molecular mechanisms to clinical cases implication of periodontal diseases in development of systemic diseases. J Pharmacol Sci 2010; 113: 103-109.
88. Koren O, Spor A, Felin J, et al. Human oral, gut and plaque micro-biota in patients with atherosclerosis. ProcNatl Acad Sci USA 201;108:4592-4598.
89. Kebschull M, Demmer RT, Papapanou PN. Gum bug, leave my heart alone!" -epidemiologic and mechanistic evidence linking periodontal infections and atherosclerosis. J Dent Res 2010; 89: 879-902.
90. Belstrom D, Holmstrop P, Damgard C, et al. Atherogenic bacterium Porphyromonasgingivalis evades circulating phagocytes by adhering to erythrocytes. Infect Immun 2011; 79: 1559-1565.
91. Ridker PM, and Silvertown JD. Inflammation, C-Reactive Protein, and atherothrombosis. J Periodontol 2008; 79: 1544-51.
92. Sfyroeras GS, Roussas N, Saleptsis GV, Argyriou C, Giannoukas D. Association between periodontal disease and stroke. J Vasc Surg 2012; 55: 1178-1184.
93. Ghizoni JS, Taveira LA, Garlet GP, et al. Increased levels of Por-phyromonas gingivalis are associated with ischemic and hemor-rhagic cerebrovascular disease in humans: an in vivo study. J Appl Oral Sci 2012; 20:104-112.
94. Eckel RH, Grundy SM, Zimmet PZ. The Metabolic Syndrome. Lancet 2005; 365: 1415-1428.
95. Cameron AJ, Show JE, Zimmet PZ. The metabolic syndrome prevalence in world wide population. Endocrinol Metab Clin North Am 2004; 33: 351-375.
96. Bullon P, Morillo JM, Ramirez-Tortosa MC, et al. Metabolic Syndrome and periodontitis: Is oxidative stress a common link? J Dent Res 2009; 88: 503-518.