Astaxanthin engages the l-arginine/NO/cGMP/KATP channel signaling pathway toward antinociceptive effects.
Analgesics
/ administration & dosage
Animals
Arginine
/ metabolism
Cyclic GMP
/ metabolism
Disease Models, Animal
Dose-Response Relationship, Drug
Glyburide
/ pharmacology
KATP Channels
/ metabolism
Male
Mice
NG-Nitroarginine Methyl Ester
/ pharmacology
Nitric Oxide
/ metabolism
Pain
/ drug therapy
Signal Transduction
/ drug effects
Sildenafil Citrate
/ pharmacology
Xanthophylls
/ administration & dosage
Journal
Behavioural pharmacology
ISSN: 1473-5849
Titre abrégé: Behav Pharmacol
Pays: England
ID NLM: 9013016
Informations de publication
Date de publication:
01 12 2021
01 12 2021
Historique:
pubmed:
26
9
2021
medline:
25
2
2022
entrez:
25
9
2021
Statut:
ppublish
Résumé
One of the main functions of the sensory system in our body is to maintain somatosensory homeostasis. Recent reports have led to a significant advance in our understanding of pain signaling mechanisms; however, the exact mechanisms of pain transmission have remained unclear. There is an urgent need to reveal the precise signaling mediators of pain to provide alternative therapeutic agents with more efficacy and fewer side effects. Accordingly, although the anti-inflammatory, antioxidative and anti-neuropathic effects of astaxanthin (AST) have been previously highlighted, its peripheral antinociceptive mechanisms are not fully understood. In this line, considering the engagement of l-arginine/nitric oxide (NO)/cyclic GMP (cGMP)/potassium channel (KATP) signaling pathway in the antinociceptive responses, the present study evaluated its associated role in the antinociceptive activity of AST. Male mice were intraperitoneally (i.p.) injected with l-arginine (100 mg/kg), SNAP (1 mg/kg), L-NAME (30 mg/kg), sildenafil (5 mg/kg), and glibenclamide (10 mg/kg) alone and prior to the most effective dose of AST. Following AST administration, intraplantarly (i.pl) injection of formalin was done, and pain responses were evaluated in mice during the primary (acute) and secondary (inflammatory) phases of formalin test. The results highlighted that 10 mg/kg i.p. dose of AST showed the greatest antinociceptive effect. Besides, while L-NAME and glibenclamide reduced the antinociceptive effect of AST, it was significantly increased by l-arginine, SNAP and sildenafil during both the primary and secondary phases of formalin test. These data suggest that the antinociceptive activity of AST is passing through the l-arginine/NO/cGMP/KATP pathway.
Identifiants
pubmed: 34561366
doi: 10.1097/FBP.0000000000000655
pii: 00008877-202112000-00001
doi:
Substances chimiques
Analgesics
0
KATP Channels
0
Xanthophylls
0
Nitric Oxide
31C4KY9ESH
astaxanthine
8XPW32PR7I
Arginine
94ZLA3W45F
Sildenafil Citrate
BW9B0ZE037
Cyclic GMP
H2D2X058MU
Glyburide
SX6K58TVWC
NG-Nitroarginine Methyl Ester
V55S2QJN2X
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
607-614Informations de copyright
Copyright © 2021 Wolters Kluwer Health, Inc. All rights reserved.
Références
Alves DP, Soares AC, Francischi JN, Castro MS, Perez AC, Duarte ID (Additive antinociceptive effect of the combination of diazoxide, an activator of ATP-sensitive K+ channels, and sodium nitroprusside and dibutyryl-cGMP. Eur J Pharmacol 2004). 489:59–65.
Borsook D, Youssef AM, Simons L, Elman I, Eccleston C (When pain gets stuck: the evolution of pain chronification and treatment resistance. Pain 2018). 159:2421–2436.
Brazill JM, Beeve AT, Craft CS, Ivanusic JJ, Scheller EL (Nerves in bone: evolving concepts in pain and anabolism. J Bone Miner Res 2019). 34:1393–1406.
Choi SK, Park YS, Choi DK, Chang HI (Effects of astaxanthin on the production of NO and the expression of COX-2 and iNOS in LPS-stimulated BV2 microglial cells. J Microbiol Biotechnol 2008). 18:1990–1996.
Conroy JL, Fang C, Gu J, Zeitlin SO, Yang W, Yang J, et al. (Opioids activate brain analgesic circuits through cytochrome P450/epoxygenase signaling. Nat Neurosci 2010). 13:284–286.
Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, et al. (BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 2005). 438:1017–1021.
Dahlhamer J, Lucas J, Zelaya C, Nahin R, Mackey S, DeBar L, et al. (Prevalence of chronic pain and high-impact chronic pain among adults—United States, 2016. Morb Mortal Wkly Rep 2018). 67:1001.
Dal D, Salman MA, Salman AE, Iskit AB, Aypar U (The involvement of nitric oxide on the analgesic effect of tramadol. Eur J Anaesthesiol 2006). 23:175–177.
Déciga-Campos M, López-Muñoz FJ (Participation of the L-arginine-nitric oxide-cyclic GMP-ATP-sensitive K+ channel cascade in the antinociceptive effect of rofecoxib. Eur J Pharmacol 2004). 484:193–199.
DeLeo JA, Yezierski RP (The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 2001). 90:1–6.
Donato F, Pavin NF, Goes AT, Souza LC, Soares LC, Rodrigues OE, et al. (Antinociceptive and anti-hyperalgesic effects of bis(4-methylbenzoyl) diselenide in mice: evidence for the mechanism of action. Pharm Biol 2015). 53:395–403.
Durate ID, Lorenzetti BB, Ferreira SH (Peripheral analgesia and activation of the nitric oxide-cyclic GMP pathway. Eur J Pharmacol 1990). 186:289–293.
Eccleston C (Role of psychology in pain management. Br J Anaesth 2001). 87:144–152.
Fakhri S, Abbaszadeh F, Dargahi L, Jorjani M (Astaxanthin: A mechanistic review on its biological activities and health benefits. Pharmacol Res 2018a). 136:1–20.
Fakhri S, Ahmadpour Y, Rezaei H, Kooshki L, Moradi SZ, Iranpanah A, et al. (The antinociceptive mechanisms of melatonin: role of L-arginine/nitric oxide/cyclic GMP/KATP channel signaling pathway. Behav Pharmacol 2020). 31:728–737.
Fakhri S, Dargahi L, Abbaszadeh F, Jorjani M (Astaxanthin attenuates neuroinflammation contributed to the neuropathic pain and motor dysfunction following compression spinal cord injury. Brain Res Bull 2018b). 143:217–224.
Fakhri S, Dargahi L, Abbaszadeh F, Jorjani M (Effects of astaxanthin on sensory-motor function in a compression model of spinal cord injury: involvement of ERK and AKT signalling pathway. Eur J Pain 2019a). 23:750–764.
Fakhri S, Aneva IY, Farzaei MH, Sobarzo-Sánchez E (The neuroprotective effects of astaxanthin: therapeutic targets and clinical perspective. Molecules 2019b). 24:E2640.
Florentino IF, Galdino PM, De Oliveira LP, Silva DP, Pazini F, Vanderlinde FA, et al. (Involvement of the NO/cGMP/KATP pathway in the antinociceptive effect of the new pyrazole 5-(1-(3-fluorophenyl)-1H-pyrazol-4-yl)-2H-tetrazole (LQFM-021). Nitric Oxide 2015). 47:17–24.
Follenfant R, Nakamura-Craig M, Henderson B, Higgs G (Inhibition by neuropeptides of interleukin-1β-induced, prostaglandin-independent hyperalgesia. Br J Pharmacol 1989). 98:41–43.
Fundytus ME (Glutamate receptors and nociception: implications for the drug treatment of pain. Cns Drugs 2001). 15:29–58.
Gatchel RJ (Clinical essentials of pain management. 2005). American Psychological Association.
Ghorbanzadeh B, Mansouri MT, Hemmati AA, Naghizadeh B, Mard SA, Rezaie A (Involvement of L-arginine/NO/cGMP/KATP channel pathway in the peripheral antinociceptive actions of ellagic acid in the rat formalin test. Pharmacol Biochem Behav 2014). 126:116–121.
Groh A, Mease R, Krieger P (Pain processing in the thalamocortical system. Neuroforum 2017). 23:117–122.
Hernández-Ortega M, Ortiz-Moreno A, Hernández-Navarro MD, Chamorro-Cevallos G, Dorantes-Alvarez L, Necoechea-Mondragón H (Antioxidant, antinociceptive, and anti-inflammatory effects of carotenoids extracted from dried pepper (Capsicum annuum L.). J Biomed Biotechnol 2012). 2012:524019.
Jiang X, Yan Q, Liu F, Jing C, Ding L, Zhang L, Pang C (Chronic trans-astaxanthin treatment exerts antihyperalgesic effect and corrects co-morbid depressive like behaviors in mice with chronic pain. Neurosci Lett 2018). 662:36–43.
Kasper D, Harrison TR (Harrison’s principles of internal medicine. Vol. 2005). 1. McGraw-Hill, Medical Publishing Division.
Kishimoto Y, Tani M, Uto-Kondo H, Iizuka M, Saita E, Sone H, et al. (Astaxanthin suppresses scavenger receptor expression and matrix metalloproteinase activity in macrophages. Eur J Nutr 2010). 49:119–126.
Kuedo Z, Sangsuriyawong A, Klaypradit W, Tipmanee V, Chonpathompikunlert P (Effects of astaxanthin from litopenaeus vannamei on carrageenan-induced edema and pain behavior in mice. Molecules 2016). 21:382.
Landa-Juárez AY, Ortiz MI, Castañeda-Hernández G, Chávez-Piña AE (Participation of potassium channels in the antinociceptive effect of docosahexaenoic acid in the rat formalin test. Eur J Pharmacol 2016). 793:95–100.
Lima MG, Maximino C, Matos Oliveira KR, Brasil A, Crespo-Lopez ME, Batista EdeJ, et al. (Nitric oxide as a regulatory molecule in the processing of the visual stimulus. Nitric Oxide 2014). 36:44–50.
Mudge AW, Leeman SE, Fischbach GD (Enkephalin inhibits release of substance P from sensory neurons in culture and decreases action potential duration. Proc Natl Acad Sci U S A 1979). 76:526–530.
Obara I, Cinar OG, Starowicz K, Benyhe S, Borsodi A, Przewlocka B (Agonist-dependent attenuation of μ-opioid receptor-mediated G-protein activation in the dorsal root ganglia of neuropathic rats. J Neural Transm 2010). 117:421–429.
Ocaña M, Cendán CM, Cobos EJ, Entrena JM, Baeyens JM (Potassium channels and pain: present realities and future opportunities. Eur J Pharmacol 2004). 500:203–219.
Ortiz MI, Medina-Tato DA, Sarmiento-Heredia D, Palma-Martínez J, Granados-Soto V (Possible activation of the NO–cyclic GMP–protein kinase G–K+ channels pathway by gabapentin on the formalin test. Pharmacol Biochem Behav 2006). 83:420–427.
Parvardeh S, Sabetkasaei M, Moghimi M, Masoudi A, Ghafghazi S, Mahboobifard F (Role of L-arginine/NO/cGMP/KATP channel signaling pathway in the central and peripheral antinociceptive effect of thymoquinone in rats. Iran J Basic Med Sci 2018). 21:625–633.
Ringkamp M, Dougherty PM, Raja SN (Benzon HT, Raja SN, Fishman SM, Liu SS, editors. Anatomy and physiology of the pain signaling process. In: Essentials of pain medicine. 2018). Elsevier. pp. 3–10.e11.
Safaripour S, Nemati Y, Parvardeh S, Ghafghazi S, Fouladzadeh A, Moghimi M (Role of l-arginine/SNAP/NO/cGMP/KATP channel signalling pathway in antinociceptive effect of α-terpineol in mice. J Pharm Pharmacol 2018). 70:507–515.
Sharma K, Sharma D, Sharma M, Sharma N, Bidve P, Prajapati N, et al. (Astaxanthin ameliorates behavioral and biochemical alterations in in-vitro and in-vivo model of neuropathic pain. Neurosci Lett 2018). 674:162–170.
Shimoji K, Kurokawa S (Shimoji K, Nader A, Hamann W, editors. Anatomical physiology of pain. In: Chronic Pain Management in General and Hospital Practice. 2020). Springer. pp. 21–42.
Srebro DP, Vučković SM, Savić Vujović KR, Prostran MŠ (TRPA1, NMDA receptors and nitric oxide mediate mechanical hyperalgesia induced by local injection of magnesium sulfate into the rat hind paw. Physiol Behav 2015). 139:267–273.
Taiwo YO, Levine JD (Effects of cyclooxygenase products of arachidonic acid metabolism on cutaneous nociceptive threshold in the rat. Brain Res 1990). 537:372–374.
Tsantoulas C (Emerging potassium channel targets for the treatment of pain. Curr Opin Support Palliat Care 2015). 9:147–154.
Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K (P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 2003). 424:778–783.
Yasui Y, Hosokawa M, Mikami N, Miyashita K, Tanaka T (Dietary astaxanthin inhibits colitis and colitis-associated colon carcinogenesis in mice via modulation of the inflammatory cytokines. Chem Biol Interact 2011). 193:79–87.
Zhao X, Zhang X, Liu H, Zhu H, Zhu Y (Enzyme-assisted extraction of astaxanthin from Haematococcus pluvialis and its stability and antioxidant activity. Food Sci Biotechnol 2019). 28:1637–1647.
Zhuang ZY, Xu H, Clapham DE, Ji RR (Phosphatidylinositol 3-kinase activates ERK in primary sensory neurons and mediates inflammatory heat hyperalgesia through TRPV1 sensitization. J Neurosci 2004). 24:8300–8309.