Archives of Oral Biology
Volume 55, Issue 8 , Pages 583-590 , August 2010

Participation of the endocannabinoid system in lipopolysaccharide-induced inhibition of salivary secretion

  • Javier Fernandez-Solari

      Affiliations

    • Cátedra de Fisiología, Facultad de Odontología, Universidad de Buenos Aires, Argentina
    • Centro de Estudios Farmacológicos y Botánicos (CEFyBO-CONICET-UBA), Argentina
    • Corresponding Author InformationCorresponding author at: Centro de Estudios Farmacológicos y Botánicos (CEFyBO-CONICET-UBA), Paraguay 2155 (C1121ABG), Buenos Aires, Argentina. Tel.: +54 1145083680.
  • ,
  • Juan Pablo Prestifilippo

      Affiliations

    • Cátedra de Fisiología, Facultad de Odontología, Universidad de Buenos Aires, Argentina
  • ,
  • Cesar Angel Ossola

      Affiliations

    • Cátedra de Fisiología, Facultad de Odontología, Universidad de Buenos Aires, Argentina
  • ,
  • Valeria Rettori

      Affiliations

    • Centro de Estudios Farmacológicos y Botánicos (CEFyBO-CONICET-UBA), Argentina
  • ,
  • Juan Carlos Elverdin

      Affiliations

    • Cátedra de Fisiología, Facultad de Odontología, Universidad de Buenos Aires, Argentina

,Accepted 15 May 2010.

References 

  1. Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science. 1990;249:1431–1433
  2. Dentener MA, Bazil V, Von Asmuth EJ, Ceska M, Buurman WA. J Immunol. 1993;150:2885–2891
  3. Muller JM, Ziegler-Heitbrock HW, Bauerle PA. Nuclear factor kappa B, a mediator of lipopolysaccharide effects. Immunobiology. 1993;187:233–256
  4. Guha M, Mackman N. LPS induction of gene expression in human monocytes. Cell Signal. 2001;13:85–94
  5. Minghetti L, Levi G. Induction of prostanoid biosynthesis by bacterial lipopolysaccharide and isoproterenol in rat microglial cultures. J Neurochem. 1995;65:2690–2698
  6. Rankin JA, Sylvester I, Smith S, Yoshimura T, Leonard EJ. Macrophages cultured in vitro release leukotriene B4 and neutrophil attractant/activation protein (interleukin 8) sequentially in response to stimulation with lipopolysaccharide and zymosan. J Clin Invest. 1990;86:1556–1564
  7. Liu J, Bátkai S, Pacher P, Harvey-White J, Wagner JA, Cravatt BF, et al. Lipopolysaccharide induces anandamide synthesis in macrophages via CD14/MAPK/phosphoinositide 3-kinase/NF-kappaB independently of platelet-activating factor. J Biol Chem. 2003;278:45034–45039
  8. Mechoulam R, Fride E, Di Marzo V. Endocannabinoids. Eur J Pharmacol. 1998;359:1–18
  9. Devane WA, Dysarz FA, Johnson MR, Melvin LS, Howlett AC. Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol. 1988;34:605–613
  10. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, et al. Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA. 1990;87:1932–1936
  11. Pertwee RG. In:  Pertwee RG editors. Cannabinoid receptors. London: Academic Press; 1995;p. 1–34
  12. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature. 1993;365:61–65
  13. Howlett AC, Fleming RM. Cannabinoid inhibition of adenylate cyclase. Pharmacology of the response in neuroblastoma cell membranes. Mol Pharmacol. 1984;26:532–538
  14. Tandler B, Phillips CJ. Microstructure of mammalian salivary glands and its relationship to diet. In:  Garret JR,  Ekstrom J,  Anderson LC editor. Glandular mechanisms of salivary secretion. oral frontiers on biology. vol. 10:Basel, Switzerland: Karger; 1998;p. 21–35
  15. Prestifilippo JP, Fernández-Solari J, de la Cal C, Iribarne M, Suburo AM, Rettori V, et al. Inhibition of salivary secretion by activation of cannabinoid receptors. Exp Biol Med. 2006;231:1421–1429
  16. Lomniczi AC, Mohn A, Faletti A, Franchi A, McCann SM, Rettori V, et al. Inhibition of salivary secretion by lipopolysaccharide: possible role of prostaglandins. Am J Physiol Endocrinol Metab. 2001;281:E405–E411
  17. Fernandez-Solari J, Prestifilippo JP, Bornstein SR, McCann SM, Rettori V. Participation of the endocannabinoid system in the effect of TNFα on hypothalamic release of gonadotropin-releasing hormone. Ann NY Acad Sci. 2006;1088:238–250
  18. Berdyshev EV, Schmid PC, Krebsbach RJ, Schmid HH. Activation of PAF receptors results in enhanced synthesis of 2-arachidonoylglycerol (2-AG) in immune cells. FASEB J. 2001;15:2171–2178
  19. Facchinetti F, Del Giudice E, Furegato S, Passarotto M, Leon A. Cannabinoids ablate release of TNFα in rat microglial cells stimulated with lypopolysaccharide. Glia. 2003;41:161–168
  20. Bianciotti LG, Elverdin JC, Vatta MS, Colatrella C, Fernandez BE. Atrial natriuretic factor enhances induced salivary secretion in the rat. Regul Pept. 1994;49:195–202
  21. Gatley SJ, Gifford AN, Volkow ND, Lan R, Makriyannis A. 123Ilabeled AM251: a radioiodinated ligand which binds in vivo to mouse brain cannabinoid CB1 receptors. Eur J Pharmacol. 1996;307:331–338
  22. Pertwee R, Griffin G, Fernando S, Li X, Hill A, Makriyannis A. AM630, a competitive cannabinoid receptor antagonist. Life Sci. 1995;56:1949–1955
  23. Prestifilippo JP, Fernández-Solari J, Medina V, Rettori V, Elverdin JC. Role of the endocannabinoid system in ethanol-induced inhibition of salivary secretion. Alcohol Alcohol. 2009;44:443–448
  24. Paria B, Deutsch D, Dey S. The uterus is a potential site for anandamide synthesis and hydrolysis: differential profiles of anandamide synthase and hydrolase activities in the mouse uterus during the periimplantation period. Mol Reprod Dev. 1996;45:183–192
  25. Klein TW, Lane B, Newton CA, Friedman H. The cannabinoid system and cytokine network. Proc Soc Exp Biol Med. 2000;225:1–8
  26. Ramos JA, González S, Sagredo O, Gómez-Ruiz M, Fernández-Ruiz J. Therapeutic potential of the endocannabinoid system in the brain. Mini Rev Med Chem. 2005;5:609–617
  27. Maccarrone M, De Petrocellis L, Bari M, Fezza F, Salvati S, Di Marzo V, et al. Lipopolysaccharide downregulates fatty acid amide hydrolase expression and increases anandamide levels in human peripheral lymphocytes. Arch Biochem Biophys. 2001;393:321–328
  28. Bugrim AE. Regulation of Ca2+ release by cAMP-dependent protein kinase. A mechanism for agonist-specific calcium signaling?. Cell Calcium. 1999;25:219–226
  29. Zhang GH, Martinez JR. Effects of forksolin, dibutyryl cAMP and H89 on Ca2+ mobilization in submandibular salivary cells of newborn rats. Arch Oral Biol. 1999;44:735–744
  30. Bruce JI, Shuttleworth TJ, Giovannucci DR, Yule DI. Phosphorylation of inositol 1,4,5-trisphosphate receptors in parotid acinar cells. A mechanism for the synergistic effects of cAMP on Ca2+ signaling. J Biol Chem. 2002;277:1340–1348
  31. McConnell WR, Dewey WL, Harris LS, Borzelleca JF. A study of the effect of delta 9-tetrahydrocannabinol (delta9-THC) on mammalian salivary flow. J Pharmacol Exp Ther. 1978;206:567–573
  32. Yao C, Li X, Murdiastuti K, Kosugi-Tanaka C, Akamatsu T, Kanamori N, et al. Lipopolysaccharide-induced elevation and secretion of interleukin-1b in the submandibular gland of male mice. Immunology. 2005;116:213–222
  33. Baker OJ, Camden JM, Redman RS, Jones JE, Seye CI, Erb L, et al. Proinflammatory cytokines tumor necrosis factor-alpha and interferon-gamma alter tight junction structure and function in the rat parotid gland Par-C10 cell line. Am J Physiol Cell Physiol. 2008;295:C1191–C1201
  34. Jonsson MV, Delaleu N, Brokstad KA, Berggreen E, Skarstein K. Impaired salivary gland function in NOD mice association with changes in cytokine profile but not with histopathologic changes in the salivary gland. Arthritis Rheum. 2006;54:2300–2305
  35. Di Paola R, Mazzon E, Muià C, Crisafulli C, Terrana D, Greco S, et al. Effects of etanercept, a tumour necrosis factor-alpha antagonist, in an experimental model of periodontitis in rats. Br J of Pharmacol. 2007;150:286–297
  36. Iribarne M, Torbidoni V, Julián K, Prestifilippo JP, Sinha D, Rettori V, et al. Cannabinoid receptors in conjunctival epithelium: identification and functional properties. Invest Ophthalmol Vis Sci. 2008;49:4535–4544
  37. Sancho R, Calzado MA, Di Marzo V, Appendino G, Muñoz E. Anandamide inhibits nuclear factor-kappaB activation through a cannabinoid receptor-independent pathway. Mol Pharmacol. 2003;63:429–438
  38. Richardson JD, Kilo S, Hargreaves KM. Cannabinoids reduce hyperalgesia and inflammation via interaction with peripheral CB1 receptors. Pain. 1998;75:111–119
  39. Parolaro D. Presence and functional regulation of cannabinoid receptors in immune cells. Life Sci. 1999;65:637–644
  40. Sacerdote P, Massi P, Panerai AE, Parolaro D. In vivo and in vitro treatment with the synthetic cannabinoid CP55,940 decreases the in vitro migration of macrophages in the rat: involvement of both CB1 and CB2 receptors. J Neuroimmunol. 2000;109:155–163
  41. Renzi A, De Luca LA, Deróbio JG, Menani JV. Lesions of the lateral hypothalamus impair pilocarpine-induced salivation in rats. Brain Res Bull. 2002;58:455–459
  42. Fernandez-Solari J, Prestifilippo JP, Vissio P, Ehrhart-Bornstein M, Bornstein SR, Rettori V, et al. Anandamide injected into the lateral ventricle of the brain inhibits submandibular salivary secretion by attenuating parasympathetic neurotransmission. Braz J Med Biol Res. 2009;42:537–544
  43. Matsuo R, Kusano K. Lateral hypothalamic modulation of the gustatory-salivary reflex in rats. J Neurosci. 1984;4:1208–1216

PII: S0003-9969(10)00128-7

doi: 10.1016/j.archoralbio.2010.05.006

Archives of Oral Biology
Volume 55, Issue 8 , Pages 583-590 , August 2010