Inclusion of cocoa as a dietary supplement represses expression of inflammatory proteins in spinal trigeminal nucleus in response to chronic trigeminal nerve stimulation

Molecular Nutrition and Food Research

Volumn 57, Issue 6, 2013, Pages 996-1006

  Cady, Ryan J ^a   Denson, Jennifer E ^a   Durham, Paul L ^a  

^a MISSOURI STATE UNIVERSITY   (United States)

Author keywords

Cocoa; Cytokines; Inflammation; Sensitization; Trigeminal

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CD53 ANTIGEN; CD53 PROTEIN, RAT; CYTOKINE; DUSP1 PROTEIN, RAT; EXCITATORY AMINO ACID TRANSPORTER 1; FREUND ADJUVANT; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; PROTEIN; SLC1A3 PROTEIN, RAT;

ANIMAL; ARTICLE; CACAO; CENTRAL NERVOUS SYSTEM SENSITIZATION; DIET SUPPLEMENTATION; DIET THERAPY; DISEASE MODEL; DRUG EFFECT; FACE PAIN; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; TEMPOROMANDIBULAR JOINT DISORDER; TRIGEMINAL NERVE; TRIGEMINAL NUCLEUS;

ANIMALS; ANTIGENS, CD53; CACAO; CALCITONIN GENE-RELATED PEPTIDE; CENTRAL NERVOUS SYSTEM SENSITIZATION; CYTOKINES; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; DUAL SPECIFICITY PHOSPHATASE 1; EXCITATORY AMINO ACID TRANSPORTER 1; FACIAL PAIN; FREUND'S ADJUVANT; MALE; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; TEMPOROMANDIBULAR JOINT DISORDERS; TRIGEMINAL NERVE; TRIGEMINAL NUCLEUS, SPINAL;

ANIMALIA; RATTUS; THEOBROMA CACAO;

EID: 84878943147     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200630     Document Type: Article

References (82)

1. Dworkin, S. F., LeResche, L., DeRouen, T., Von Korff, M., Assessing clinical signs of temporomandibular disorders: reliability of clinical examiners. J. Prosthet. Dent. 1990, 63, 574-579.
2. Al-Jundi, M. A., John, M. T., Setz, J. M., Szentpetery, A. et al., Meta-analysis of treatment need for temporomandibular disorders in adult nonpatients. J. Orofac. Pain. 2008, 22, 97-107.
3. Isong, U., Gansky, S. A., Plesh, O., Temporomandibular joint and muscle disorder-type pain in U.S. adults: the National Health Interview Survey. J. Orofac. Pain. 2008, 22, 317-322.
4. Herb, K., Cho, S., Stiles, M. A., Temporomandibular joint pain and dysfunction. Curr. Pain. Headache Rep. 2006, 10, 408-414.
5. Bereiter, D. A., Okamoto, K., Bereiter, D. F., Effect of persistent monoarthritis of the temporomandibular joint region on acute mustard oil-induced excitation of trigeminal subnucleus caudalis neurons in male and female rats. Pain 2005, 117, 58-67.
6. Shimizu, K., Guo, W., Wang, H., Zou, S. et al., Differential involvement of trigeminal transition zone and laminated subnucleus caudalis in orofacial deep and cutaneous hyperalgesia: the effects of interleukin-10 and glial inhibitors. Mol. Pain 2009, 5, 75.
7. Xie, Y. F., Zhang, S., Chiang, C. Y., Hu, J. W. et al., Involvement of glia in central sensitization in trigeminal subnucleus caudalis (medullary dorsal horn). Brain Behav. Immun. 2007, 21, 634-641.
8. Damodaram, S., Thalakoti, S., Freeman, S. E., Garrett, F. G. et al., Tonabersat inhibits trigeminal ganglion neuronal-satellite glial cell signaling. Headache 2009, 49, 5-20.
9. Ren, K., Emerging role of astroglia in pain hypersensitivity. Jpn. Dent. Sci. Rev. 2010, 46, 86.
10. Guo, W., Wang, H., Watanabe, M., Shimizu, K. et al., Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J. Neurosci. 2007, 27, 6006-6018.
11. Chen, Y., Li, G. W., Wang, C., Gu, Y. et al., Mechanisms underlying enhanced P2X receptor-mediated responses in the neuropathic pain state. Pain 2005, 119, 38-48.
12. Xie, Y. F., Glial involvement in trigeminal central sensitization. Acta Pharmacol. Sin. 2008, 29, 641-645.
13. Seybold, V. S., The role of peptides in central sensitization. Handb. Exp. Pharmacol. 2009, 451-491.
14. Burnstock, G., Purinergic signalling-an overview. Novartis. Found. Symp. 2006, 276, 26-48; discussion 48-57, 275-281.
15. Wang, Z., Ma, W., Chabot, J. G., Quirion, R., Cell-type specific activation of p38 and ERK mediates calcitonin gene-related peptide involvement in tolerance to morphine-induced analgesia. FASEB J. 2009, 23, 2576-2586.
16. Burnstock, G., Wood, J. N., Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr. Opin. Neurobiol. 1996, 6, 526-532.
17. Latremoliere, A., Woolf, C. J., Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J. Pain 2009, 10, 895-926.
18. Aley, K. O., Levine, J. D., Role of protein kinase A in the maintenance of inflammatory pain. J. Neurosci. 1999, 19, 2181-2186.
19. Hucho, T., Levine, J. D., Signaling pathways in sensitization: toward a nociceptor cell biology. Neuron 2007, 55, 365-376.
20. Uceyler, N., Schafers, M., Sommer, C., Mode of action of cytokines on nociceptive neurons. Exp. Brain Res. 2009, 196, 67-78.
21. Ji, R. R., Gereau, R. W. T., Malcangio, M., Strichartz, G. R., MAP kinase and pain. Brain Res. Rev. 2009, 60, 135-148.
22. Shanley, T. P., Phosphatases: counterregulatory role in inflammatory cell signaling. Crit. Care Med. 2002, 30, S80-S88.
23. Dickinson, R. J., Keyse, S. M., Diverse physiological functions for dual-specificity MAP kinase phosphatases. J. Cell Sci. 2006, 119, 4607-4615.
24. Lasa, M., Abraham, S. M., Boucheron, C., Saklatvala, J. et al., Dexamethasone causes sustained expression of mitogen-activated protein kinase (MAPK) phosphatase 1 and phosphatase-mediated inhibition of MAPK p38. Mol. Cell Biol. 2002, 22, 7802-7811.
25. Clark, A. R., MAP kinase phosphatase 1: a novel mediator of biological effects of glucocorticoids? J. Endocrinol. 2003, 178, 5-12.
26. Cady, R. J., Durham, P. L., Cocoa-enriched diets enhance expression of phosphatases and decrease expression of inflammatory molecules in trigeminal ganglion neurons. Brain Res. 2010, 1323, 18-32.
27. Grassi, D., Lippi, C., Necozione, S., Desideri, G. et al., Short-term administration of dark chocolate is followed by a significant increase in insulin sensitivity and a decrease in blood pressure in healthy persons. Am. J. Clin. Nutr. 2005, 81, 611-614.
28. Selmi, C., Mao, T., Keen, C., Schmitz, H. et al., The anti-inflammatory properties of cocoa flavanols. J. Cardiovasc. Pharmacol. 2006, 47, S163-S176.
29. Dillinger, T. L., Barriga, P., Escarcega, S., Jimenez, M. et al., Food of the gods: cure for humanity? A cultural history of the medicinal and ritual use of chocolate. J. Nutr. 2000, 130, 2057S-2072S.
30. Newman, D. J., Cragg, G. M., Natural products as sources of new drugs over the last 25 years. J. Nat. Prod. 2007, 70, 461-477.
31. Vuorelaa, P., Leinonenb, M., Saikkuc, P., Tammelaa, P. et al., Natural products in the process of finding new drug candidates. Curr. Med. Chem. 2004, 11, 1375-1389.
32. Katz, D. L., Doughty, K., Ali, A., Cocoa and chocolate in human health and disease. Antioxid. Redox Signal. 2011, 15, 2779-2811.
33. Jourdain, C., Tenca, G., Deguercy, A., Troplin, P. et al., In-vitro effects of polyphenols from cocoa and beta-sitosterol on the growth of human prostate cancer and normal cells. Eur. J. Cancer Prev. 2006, 15, 353-361.
34. Singleton, V., Rossi, J., Colorimetry of total phenolics with phosphomolybdicphosphotungstic acid reagents. Am. J. Enol. Vitic. 1965, 16, 144-158.
35. Garrett, F. G., Durham, P. L., Differential expression of connexins in trigeminal ganglion neurons and satellite glial cells in response to chronic or acute joint inflammation. Neuron. Glia. Biol. 2008, 4, 295-306.
36. Cady, R. J., Hirst, J. J., Durham, P. L., Dietary grape seed polyphenols repress neuron and glia activation in trigeminal ganglion and trigeminal nucleus caudalis. Mol. Pain 2010, 6, 91.
37. Cady, R. J., Glenn, J. R., Smith, K. M., Durham, P. L., Calcitonin gene-related peptide promotes cellular changes in trigeminal neurons and glia implicated in peripheral and central sensitization. Mol. Pain 2011, 7, 94.
38. Harper, R. P., Kerins, C. A., McIntosh, J. E., Spears, R. et al., Modulation of the inflammatory response in the rat TMJ with increasing doses of complete Freund's adjuvant. Osteoarthritis Cartilage 2001, 9, 619-624.
39. Hutchins, B., Spears, R., Hinton, R. J., Harper, R. P., Calcitonin gene-related peptide and substance P immunoreactivity in rat trigeminal ganglia and brainstem following adjuvant-induced inflammation of the temporomandibular joint. Arch. Oral. Biol. 2000, 45, 335-345.
40. Thut, P. D., Hermanstyne, T. O., Flake, N. M., Gold, M. S., An operant conditioning model to assess changes in feeding behavior associated with temporomandibular joint inflammation in the rat. J. Orofac. Pain 2007, 21, 7-18.
41. Raghavendra, V., Tanga, F. Y., DeLeo, J. A., Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur. J. Neurosci. 2004, 20, 467-473.
42. Suzuki, I., Harada, T., Asano, M., Tsuboi, Y. et al., Phosphorylation of ERK in trigeminal spinal nucleus neurons following passive jaw movement in rats with chronic temporomandibular joint inflammation. J. Orofac. Pain 2007, 21, 225-231.
43. Ren, K., Neuron, glia and reciprocal relationships in pain processing. Open. Pain J. 2009, 2, 7-31.
44. Sessle, B. J., Peripheral and central mechanisms of orofacial inflammatory pain. Int. Rev. Neurobiol. 2011, 97, 179-206.
45. Anderson, L. E., Seybold, V. S., Calcitonin gene-related peptide regulates gene transcription in primary afferent neurons. J. Neurochem. 2004, 91, 1417-1429.
46. Sun, R. Q., Tu, Y. J., Lawand, N. B., Yan, J. Y. et al., Calcitonin gene-related peptide receptor activation produces PKA- and PKC-dependent mechanical hyperalgesia and central sensitization. J. Neurophysiol. 2004, 92, 2859-2866.
47. Xin, W. J., Weng, H. R., Dougherty, P. M., Plasticity in expression of the glutamate transporters GLT-1 and GLAST in spinal dorsal horn glial cells following partial sciatic nerve ligation. Mol. Pain 2009, 5, 15.
48. Fitzgerald, E. M., Okuse, K., Wood, J. N., Dolphin, A. C. et al., cAMP-dependent phosphorylation of the tetrodotoxin-resistant voltage-dependent sodium channel SNS. J. Physiol. 1999, 516, 433-446.
49. Kawasaki, Y., Kohno, T., Zhuang, Z. Y., Brenner, G. J. et al., Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J. Neurosci. 2004, 24, 8310-8321.
50. 3 receptor by calcitonin gene-related peptide in trigeminal sensory neurons. J. Biol. Chem. 2008, 283, 18743-18752.
51. Nakatsuka, T., Tsuzuki, K., Ling, J. X., Sonobe, H. et al., Distinct roles of P2X receptors in modulating glutamate release at different primary sensory synapses in rat spinal cord. J. Neurophysiol. 2003, 89, 3243-3252.
52. Burnstock, G., Pathophysiology and therapeutic potential of purinergic signaling. Pharmacol. Rev. 2006, 58, 58-86.
53. Ramos, K. M., Lewis, M. T., Morgan, K. N., Crysdale, N. Y. et al., Spinal upregulation of glutamate transporter GLT-1 by ceftriaxone: therapeutic efficacy in a range of experimental nervous system disorders. Neuroscience 2010, 169, 1888-1900.
54. Rathee, P. K., Distler, C., Obreja, O., Neuhuber, W. et al., PKA/AKAP/VR-1 module: a common link of Gs-mediated signaling to thermal hyperalgesia. J. Neurosci. 2002, 22, 4740-4745.
55. 3 receptors by the migraine mediators CGRP and NGF. Mol. Neurobiol. 2008, 37, 83-90.
56. Ji, R. R., Peripheral and central mechanisms of inflammatory pain, with emphasis on MAP kinases. Curr. Drug. Targets Inflamm. Allergy 2004, 3, 299-303.
57. Ji, R. R., Suter, M. R., p38 MAPK, microglial signaling, and neuropathic pain. Mol. Pain 2007, 3, 33.
58. Crown, E. D., Ye, Z., Johnson, K. M., Xu, G. Y. et al., Increases in the activated forms of ERK 1/2, p38 MAPK, and CREB are correlated with the expression of at-level mechanical allodynia following spinal cord injury. Exp. Neurol. 2006, 199, 397-407.
59. Kawasaki, Y., Zhang, L., Cheng, J. K., Ji, R. R., Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J. Neurosci. 2008, 28, 5189-5194.
60. Hammer, M., Echtenachter, B., Weighardt, H., Jozefowski, K. et al., Increased inflammation and lethality of Dusp1-/- mice in polymicrobial peritonitis models. Immunology 2010, 131, 395-404.
61. Vandevyver, S., Dejager, L., Van Bogaert, T., Kleyman, A. et al., Glucocorticoid receptor dimerization induces MKP1 to protect against TNF-induced inflammation. J. Clin. Invest. 2012, 122, 2130-2140.
62. Durham, P. L., Russo, A. F., Differential regulation of mitogen-activated protein kinase-responsive genes by the duration of a calcium signal. Mol. Endocrinol. 2000, 14, 1570-1582.
63. Durham, P. L., Russo, A. F., Stimulation of the calcitonin gene-related peptide enhancer by mitogen-activated protein kinases and repression by an antimigraine drug in trigeminal ganglia neurons. J. Neurosci. 2003, 23, 807-815.
64. Svensson, C. I., Marsala, M., Westerlund, A., Calcutt, N. A. et al., Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J. Neurochem. 2003, 86, 1534-1544.
65. Ren, K., Torres, R., Role of interleukin-1beta during pain and inflammation. Brain Res. Rev. 2009, 60, 57-64.
66. Andujar, I., Recio, M. C., Giner, R. M., Rios, J. L., Cocoa polyphenols and their potential benefits for human health. Oxid. Med. Cell. Longev. 2012, 2012, 906252.
67. Faridi, Z., Njike, V. Y., Dutta, S., Ali, A. et al., Acute dark chocolate and cocoa ingestion and endothelial function: a randomized controlled crossover trial. Am. J. Clin. Nutr. 2008, 88, 58-63.
68. Ramos-Romero, S., Perez-Cano, F. J., Ramiro-Puig, E., Franch, A. et al., Cocoa intake attenuates oxidative stress associated with rat adjuvant arthritis. Pharmacol. Res. 2012, 66, 207-212.
69. Jansen, P. J., Lutjohann, D., Abildayeva, K., Vanmierlo, T. et al., Dietary plant sterols accumulate in the brain. Biochim. Biophys. Acta 2006, 1761, 445-453.
70. Vanmierlo, T., Weingartner, O., van der Pol, S., Husche, C. et al., Dietary intake of plant sterols stably increases plant sterol levels in the murine brain. J. Lipid. Res. 2012, 53, 726-735.
71. Spencer, J. P., Vafeiadou, K., Williams, R. J., Vauzour, D., Neuroinflammation: modulation by flavonoids and mechanisms of action. Mol. Aspects Med. 2012, 33, 83-97.
72. Williams, R. J., Spencer, J. P., Rice-Evans, C., Flavonoids: antioxidants or signalling molecules? Free Radic. Biol. Med. 2004, 36, 838-849.
73. Nehlig, A., The neuroprotective effects of cocoa flavanol and its influence on cognitive performance. Br. J. Clin. Pharmacol. 2012, 75, 716-727.
74. Spencer, J. P., Flavonoids and brain health: multiple effects underpinned by common mechanisms. Genes Nutr. 2009, 4, 243-250.
75. Mahajan, S. G., Mehta, A. A., Suppression of ovalbumin-induced Th2-driven airway inflammation by beta-sitosterol in a guinea pig model of asthma. Eur. J. Pharmacol. 2011, 650, 458-464.
76. Valerio, M., Awad, A. B., Beta-sitosterol down-regulates some pro-inflammatory signal transduction pathways by increasing the activity of tyrosine phosphatase SHP-1 in J774A.1 murine macrophages. Int. Immunopharmacol. 2011, 11, 1012-1017.
77. Bonjardim, L. R., Lopes-Filho, R. J., Amado, G., Albuquerque, R. L., Jr. et al., Association between symptoms of temporomandibular disorders and gender, morphological occlusion, and psychological factors in a group of university students. Indian J. Dent. Res. 2009, 20, 190-194.
78. Sessle, B., The neurobiology of facial and dental pain: present knowledge, future directions. J. Dent. Res. 1987, 66, 962-981.
79. Lipton, J., Ship, J. A., Larach-Robinson, D., Estimated prevalence and distribution of reported orofacial pain in the United States. J. Am. Dent. Assoc. 1993, 124, 115-121.
80. Carlsson, G., LeResche, L., in: Barry, J., Sessle, P. S. B., and Raymond A. Dionne (Ed.), Temporomandibular disorders and related pain conditions. Progress in pain research and management, IASP Press, Seattle 1995, pp. 211-226.
81. Funk, C. D., FitzGerald, G. A., COX-2 inhibitors and cardiovascular risk. J. Cardiovasc. Pharmacol. 2007, 50, 470-479.
82. Triantafyllou, K., Vlachogiannakos, J., Ladas, S. D., Gastrointestinal and liver side effects of drugs in elderly patients. Best Pract. Res. Clin. Gastroenterol. 2010, 24, 203-215.