Natural Diterpenes from Coffee, Cafestol, and Kahweol Induce Peripheral Antinoceception by Adrenergic System Interaction

Luciana Souza Guzzo; Marina Gomes Miranda e Castor; Andrea de Castro Perez; Igor Dimitri Gama Duarte; Thiago Roberto Lima Romero

doi:10.1055/s-0035-1558084

Planta Medica, Table of Contents

Planta Med 2016; 82(01/02): 106-112
DOI: 10.1055/s-0035-1558084

Biological and Pharmacological Activitiy

Original Papers

Georg Thieme Verlag KG Stuttgart · New York

Natural Diterpenes from Coffee, Cafestol, and Kahweol Induce Peripheral Antinoceception by Adrenergic System Interaction

Luciana Souza Guzzo

Department of Pharmacology, Institute of Biological Sciences, UFMG, Belo Horizonte, Brazil

,

Marina Gomes Miranda e Castor

Department of Pharmacology, Institute of Biological Sciences, UFMG, Belo Horizonte, Brazil

,

Andrea de Castro Perez

Department of Pharmacology, Institute of Biological Sciences, UFMG, Belo Horizonte, Brazil

,

Igor Dimitri Gama Duarte

Department of Pharmacology, Institute of Biological Sciences, UFMG, Belo Horizonte, Brazil

,

Thiago Roberto Lima Romero

Department of Pharmacology, Institute of Biological Sciences, UFMG, Belo Horizonte, Brazil

› Author Affiliations

Abstract

Cafestol and kahweol are diterpenes found only in the non-saponified lipid fraction of coffee. They are released during boiling and retained in the filtration process. Previous studies have shown peripheral antinociception induced by endogenous opioid peptides released by these diterpenes. Considering that the activation of the opioid system leads to a noradrenaline release, the aim of this study was to verify the participation of the noradrenergic system in the peripheral antinociception induced by cafestol and kahweol. Hyperalgesia was induced by an intraplantar injection of prostaglandin E₂ (2 µg). Cafestol or kahweol (80 µg/paw) were administered locally into the right hindpaw alone, and after the agents α ₂-adrenoceptor antagonist yohimbine (5, 10 and 20 µg/paw), α _2 A-adrenoceptor antagonist BRL 44 408 (40 µg/paw), α _2B-adrenoceptor antagonist imiloxan (40 µg/paw), α _2 C-adrenoceptor antagonist rauwolscine (10, 15 and 20 µg/paw), α _2D-adrenoceptor antagonist RX 821 002 (40 µg/paw), α ₁-adrenoceptor antagonist prazosin (0.5, 1 and 2 µg/paw), or β-adrenoceptor antagonist propranolol (150, 300 and 600 ng/paw), respectively. Noradrenaline reuptake inhibitor reboxetine (30 µg/paw) was administered prior to cafestol or kahweol low dose (40 µg/paw) and guanetidine 3 days prior to the experiment (30 mg/kg, once a day), depleting the noradrenaline storage. Intraplantar injection of cafestol or kahweol (80 µg/paw) induced a peripheral antinociception against hyperalgesia induced by PGE₂. This effect was reversed by intraplantar injections of yohimbine, rauwolscine, prazosin and propranolol. Reboxetine injection intensified the antinociceptive effect of cafestol or kahweol low-dose, and guanethidine reversed almost 70 % of the cafestol or kahweol-induced peripheral antinociception. This study gives evidence that the noradrenergic system participates in cafestol and kahweol-induced peripheral antinociception with the release of endogenous noradrenaline.

Key words

coffee - cafestol - kahweol - peripheral antinociception - adrenergic system - noradrenaline

Full Text

References

References
1 Higdon JV, Frei B. Coffee and health: a review of recent human research. Crit Rev Food Sci Nutr 2006; 46: 101-126
2 Urgert R, Essed N, van der Weg G, Kosmeijer-Schuil TG, Katan MB. Separate effects of the coffe diterpenes cafestol and kahweol on serum lipids and liver aminotransferases. Am J Clin Nutr 1997; 65: 519-524
3 Lee KJ, Choi JH, Jeong HG. Hepatoprotective and antioxidant effects of the coffee diterpenes kahweol and cafestol on carbon tetrachloride-induced liver damage in mice. Food Chem Toxicol 2007; 45: 2118-2125
4 Lee KJ, Jeong HG. Protective effects of kahweol and cafestol against hydrogen peroxide-induced oxidative stress and DNA damage. Toxicol Lett 2007; 173: 80-87
5 Hwang HP, Jeong HG. The coffee diterpene kahweol induces heme oxygenase-1 via the PI3K and p38/Nrf2 pathway to protect human dopaminergic neurons from 6-hydroxydopamine-derived oxidative stress. FEBS Lett 2008; 582: 2655-2662
6 Huber WW, Prustomersky S, Delbanco E, Uhl M, Scharf G, Turesky RJ, Thier R, Schulte-Hermann R. Enhancement of the chemoprotective enzymes glucuronosyl transferase and glutathione transferase in specific organs of the rat by the coffee components kahweol and cafestol. Arch Toxicol 2002; 76: 209-217
7 Huber WW, Scharf G, Nagel G, Prustomersky S, Schulte-Hermann R, Kaina B. Coffee and its chemopreventive components kahweol and cafestol increase the activity of O6-methylguanine-DNA methyltransferase in rat liver–comparison with phase II xenobiotic metabolism. Mutat Res 2003; 522: 57-68
8 Huber WW, Teitel CH, Coles BF, King RS, Wiese FW, Kaderlik KR, Casciano DA, Shaddock JG, Mulder GJ, Ilett KF, Kadlubar FF. Potential chemoprotective effects of the coffee components kahweol and cafestol palmitates via modification of hepatic N-acetyltransferase and glutathione S-transferase activities. Environ Mol Mutagen 2004; 44: 265-276
9 Huber WW, Rossmanith W, Grusch M, Haslinger E, Prustomersky S, Peter-Vörösmarty B, Parzefall W, Scharf G, Schulte-Hermann R. Effects of coffee and its chemopreventive components kahweol and cafestol on cytochrome P450 and sulfotransferase in rat liver. Food Chem Toxicol 2008; 46: 1230-1238
10 Cavin C, Holzhäuser D, Constable A, Huggett AC, Schilter B. The coffee-specific diterpenes cafestol and kahweol protect against aflatoxin B1-induced genotoxicity through a dual mechanism. Carcinogenesis 1998; 19: 1369-1375
11 Cavin C, Mace K, Offord EA, Schilter B. Protective effects of coffee diterpenes against aflatoxin B1-induced genotoxicity: mechanisms in rat and human cells. Food Chem Toxicol 2001; 39: 549-556
12 Cavin C, Holzhaeuser D, Scharf G, Constable A, Huber WW, Schilter B. Cafestol and kahweol, two coffee specific diterpenes with anticarcinogenic activity. Food Chem Toxicol 2002; 40: 1155-1163
13 Kim JY, Kim DH, Jeong HG. Inhibitory effect of the coffee diterpene kahweol on carrageenan-induced inflammation in rats. Biofactors 2006; 26: 17-28
14 Kim JY, Jung KS, Lee KJ, Na HK, Chun HK, Kho YH, Jeong HG. The coffee diterpene kahweol suppress the inducible nitric oxide synthase expression in macrophages. Cancer Lett 2004; 213: 147-154
15 Kim HG, Kim JY, Hwang YP, Lee KJ, Lee KY, Kim DH, Kim DH, Jeong HG. The coffee diterpene kahweol inhibits tumor necrosis factor-alpha-induced expression of cell adhesion molecules in human endothelial cells. Toxicol Appl Pharmacol 2006; 217: 332-341
16 Guzzo LS, Romero TRL, Perez AC, Duarte IDG. The coffee specific diterpene cafestol induces peripheral antinociception mediated by endogenous opioid peptides. Clin Exp Pharmacol Physiol 2012; 39: 412-416
17 Romero TR, Guzzo LS, Duarte ID. Mu, delta, and kappa opioid receptor agonists induce peripheral antinociception by activation of endogenous noradrenergic system. J Neurosci Res 2012; 90: 1654-1661
18 Wigdor S, Wilcox GL. Central and systemic morphine-induced antinociception in mice: contribution of descending serotonergic and noradrenergic pathways. J Pharmacol Exp Ther 1987; 242: 90-95
19 Lipp J. Possible mechanisms of morphine analgesia. Clin Neuropharmacol 1991; 14: 131-147
20 Hao JX, Xu IS, Xu XJ, Wiesenfeld-Hallin Z. Effects of intrathecal morphine, clonidine and baclofen on allodynia after partial sciatic nerve injury in the rat. Acta Anaesthesiol Scand 1999; 43: 1027-1034
21 Kapitzke D, Vetter I, Cabot PJ. Endogenous opioid analgesia in peripheral tissues and the clinical implications for pain control. Ther Clin Risk Manag 2005; 1: 279-297
22 Romero TR, Resende LC, Guzzo LS, Duarte ID. CB1 and CB2 cannabinoid receptor agonists induce peripheral antinociception by activation of the endogenous noradrenergic system. Anesth Analg 2013; 116: 463-472
23 Pertovaara A. Noradrenergic pain modulation. Prog Neurobiol 2006; 80: 53-83
24 Binder W, Mousa SA, Sitte N, Kaiser M, Stein C, Schafer M. Sympathetic activation triggers endogenous opioid release and analgesia within peripheral inflamed tissue. Eur J Neurosci 2004; 20: 92-100
25 Romero TR, Guzzo LS, Perez AC, Klein A, Duarte ID. Noradrenaline activates the NO/cGMP/ATP-sensitive K(+) channels pathway to induce peripheral antinociception in rats. Nitric Oxide 2012; 26: 157-161
26 Randall LO, Sellito JJ. A method for measurement of analgesic activity on inflamed tissues. Arch Int Pharmacodyn Ther 1957; 11: 409-419
27 Nakamura M, Ferreira SH. A peripheral sympathetic component in inflammatory hyperalgesia. Eur J Pharmacol 1987; 135: 145-153
28 Gold MS, Dastmalchi S, Levine JD. α2-Adrenergic receptor subtypes in rat dorsal root and superior cervical ganglion neurons. Pain 1997; 69: 179-190
29 Shi TS, Winzer-Serhan U, Leslie F, Hökfelt T. Distribution and regulation of alpha(2)-adrenoceptors in rat dorsal root ganglia. Pain 2000; 84: 319-330
30 Khasar SG, Green PG, Chou B, Levine DJ. Peripheral nociceptive effects of α2- adrenergic receptor agonist in the rat. Neuroscience 1995; 66: 427-432
31 Lorenz W, Lomasney JW, Collins S, Regan JW, Caron MG, Lefkowitz RJ. Expression of three α2-adrenergic receptor subtypes in rat tissues: implications for α2 receptor classification. Mol Pharmacol 1990; 38: 599-603
32 Takano Y, Takano M, Yaksh TL. The effect of intrathecally administered imiloxan and WB4101: possible role of alpha 2-adrenoceptors in the spinal cord. Eur J Pharmacol 1992; 219: 465-468
33 Oropeza VC, Page ME, Van Bockstaele EJ. Systemic administration of WIN 55, 212–2 increases norepinephrine release in the rat frontal cortex. Brain Res 2005; 1046: 45-54
34 Romero TRL, Perez AC, Francischi JN, Duarte IDG. Probable involvement of α2 C-adrenoceptor subtype and endogenous opioid peptides in the peripheral antinociceptive effect induced by Xylazine. Eur J Pharmacol 2009; 608: 23-27
35 Hunter JC, Fontana DJ, Hedley LR, Jasper JR, Lewis R, Link RE, Secchi R, Sutton J, Eglen RM. Assessment of the role of alpha2-adrenoceptor subtypes in the antinociceptive, sedative and hypothermic action of dexmedetomidine in transgenic mice. Br J Pharmacol 1997; 122: 1339-1344
36 Nicholson R, Dixon AK, Spanswick D, Lee K. Noradrenergic receptor mRNA expression in adult rat superficial dorsal horn and dorsal root ganglion neurons. Neurosci Lett 2005; 380: 316-321
37 Xie J, Ho Lee Y, Wang C, Mo Chung J, Chung K. Differential expression of alpha1-adrenoceptor subtype mRNAs in the dorsal root ganglion after spinal nerve ligation. Brain Res Mol Brain Res 2001; 93: 164-172
38 Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral cannabinoid receptor. Nature 1993; 365: 61-65
39 Choi B, Rowbotham MC. Effect of adrenergic receptor activation on post-herpetic neuralgia pain and sensory disturbances. Pain 1997; 69: 55-63
40 Khasar SG, McCarter G, Levine JD. Epinephrine produces a beta-adrenergic receptor-mediated mechanical hyperalgesia and in vitro sensitization of rat nociceptors. J Neurophysiol 1999; 81: 1104-1112
41 Ali Z, Raja SN, Wesselmann U, Fuchs PN, Meyer RA, Campbell JN. Intradermal injection of norepinephrine evokes pain in patients with sympathetically maintained pain. Pain 2000; 88: 161-168
42 Hong Y, Abbott FV. Contribution of peripheral alpha 1A-adrenoceptors to pain induced by formalin or by alpha-methyl-5-hydroxytryptamine plus noradrenaline. Eur J Pharmacol 1996; 301: 41-48
43 Kaplan R, Robinson CA, Scavulli JF, Vaughan JH. Propranolol and the treatment of rheumatoid arthritis. Arthritis Rheum 1980; 23: 253-255
44 Levine JD, Coderre TJ, Helms C, Basbaum AI. Beta 2-adrenergic mechanisms in experimental arthritis. Proc Natl Acad Sci U S A 1988; 85: 4553-4556
45 Coderre TJ, Basbaum AI, Dallman MF, Helms C, Levine JD. Epinephrine exacerbates arthritis by an action at presynaptic B2-adrenoceptors. Neuroscience 1990; 34: 521-523
46 Sehgal N, Smith HS, Manchikanti L. Peripherally acting opioids and clinical implications for pain control. Pain Physician 2011; 14: 249-258
47 Zöllner C, Stein C. Opioids. Handb Exp Pharmacol 2007; 177: 31-63
48 Bigliardi PL, Tobin DJ, Gaveriaux-Ruff C, Bigliardi-Qi M. Opioids and the skin–where do we stand?. Exp Dermatol 2009; 18: 424-430
49 Bigliardi-Qi M, Sumanovski LT, Büchner S, Rufli T, Bigliardi PL. Mu-opiate receptor and beta-endorphin expression in nerve endings and keratinocytes in human skin. Dermatology 2004; 209: 183-189
50 Cheng B, Liu HW, Fu XB, Sheng ZY, Li JF. Coexistence and upregulation of three types of opioid receptors, mu, delta and kappa, in human hypertrophic scars. Br J Dermatol 2008; 158: 713-720
51 Schallreuter KU. Epidermal adrenergic signal transduction as part of the neuronal network in the human epidermis. J Investig Dermatol Symp Proc 1997; 2: 37-40
52 Steenhuis P, Huntley RE, Gurenko Z, Yin L, Dale BA, Fazel N, Isseroff RR. Adrenergic signaling in human oral keratinocytes and wound repair. J Dent Res 2011; 90: 186-192
53 Aley KO, Levine JD. Multiple receptors involved in peripheral alpha 2, mu, and A1 antinociception, tolerance, and withdrawal. J Neurosci 1997; 17: 735-744
54 Jordan BA, Gomes I, Rios C, Filipovska J, Devi LA. Functional interactions between mu opioid and alpha 2A-adrenergic receptors. Mol Pharmacol 2003; 64: 1317-1324
55 Ständer S, Schmelz M, Metze D, Luger T, Rukwied R. Distribution of cannabinoid receptor 1 (CB1) and 2 (CB2) on sensory nerve fibers and adnexal structures in human skin. J Dermatol Sci 2005; 38: 177-188
56 Ibrahim MM, Porreca F, Lai J, Albrecht PJ, Rice FL, Khodorova A, Davar G, Makriyannis A, Vanderah TW, Mata HP, Malan TP. CB2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. Proc Natl Acad Sci U S A 2005; 102: 3093-3098
57 Magina S, Esteves-Pinto C, Moura E, Serrão MP, Moura D, Petrosino S, Di Marzo V, Vieira-Coelho MA. Inhibition of basal and ultraviolet B-induced melanogenesis by cannabinoid CB(1) receptors: a keratinocyte-dependent effect. Arch Dermatol Res 2011; 303: 201-210
58 Flierl MA, Rittirsch D, Sarma JV, Huber-Lang M, Ward PA. Adrenergic regulation of complement-induced acute lung injury. Adv Exp Med Biol 2008; 632: 93-103
59 Schallreuter KU. Epidermal adrenergic signal transduction as part of the neuronal network in the human epidermis. J Investig Dermatol Symp Proc 1997; 2: 37-40
60 Steenhuis P, Huntley RE, Gurenko Z, Yin L, Dale BA, Fazel N, Isseroff RR. Adrenergic signaling in human oral keratinocytes and wound repair. J Dent Res 2011; 90: 186-192
61 Hudson BD, Hébert TE, Kelly ME. Physical and functional interaction between CB1 cannabinoid receptors and beta2-adrenoceptors. Br J Pharmacol 2010; 160: 627-642
62 Page ME. The promises and pitfalls of reboxetine. CNS Drug Rev 2003; 9: 327-342