Medial prefrontal cortex nitric oxide modulates neuropathic pain behavior through mu opioid receptors in rats
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Background: The neocortex, including the medial prefrontal cortex (mPFC), contains many neurons expressing nitric oxide synthase (NOS). In addition, increasing evidence shows that the nitric oxide (NO) and opioid systems interact in the brain. However, there have been no studies on the interaction of the opioid and NO systems in the mPFC. The objective of this study was to investigate the effects of administrating L-arginine (L-Arg, a precursor of NO) and N(gamma)-nitro-L-arginine methyl ester (L-NAME, an inhibitor of NOS) into the mPFC for neuropathic pain in rats. Also, we used selective opioid receptor antagonists to clarify the possible participation of the opioid mechanism. Methods: Complete transection of the peroneal and tibial branches of the sciatic nerve was applied to induce neuropathic pain, and seven days later, the mPFC was cannulated bilaterally. The paw withdrawal threshold fifty percent (50% PWT) was recorded on the 14th day. Results: Microinjection of L-Arg (2.87, 11.5 and 45.92 nmol per 0.25 µL) increased 50% PWT. L-NAME (17.15 nmol per 0.25 µL) and naloxonazine (an antagonist of mu opioid receptors, 1.54 nmol per 0.25 µL) inhibited anti-allodynia induced by LArg (45.92 nmol per 0.25 µL). Naltrindole (a delta opioid receptor antagonist, 2.45 nmol per 0.25 µL) and nor-binaltorphimine (a kappa opioid receptor antagonist, 1.36 nmol per 0.25 µL) were unable to prevent L-Arg (45.92 nmol per 0.25 µL)-induced antiallodynia. Conclusions: Our results indicate that the NO system in the mPFC regulates neuropathic pain. Mu opioid receptors of this area might participate in pain relief caused by L-Arg.
Abstract
Background: The neocortex, including the medial prefrontal cortex (mPFC), contains many neurons expressing nitric oxide synthase (NOS). In addition, increasing evidence shows that the nitric oxide (NO) and opioid systems interact in the brain. However, there have been no studies on the interaction of the opioid and NO systems in the mPFC. The objective of this study was to investigate the effects of administrating L-arginine (L-Arg, a precursor of NO) and N(gamma)-nitro-L-arginine methyl ester (L-NAME, an inhibitor of NOS) into the mPFC for neuropathic pain in rats. Also, we used selective opioid receptor antagonists to clarify the possible participation of the opioid mechanism. Methods: Complete transection of the peroneal and tibial branches of the sciatic nerve was applied to induce neuropathic pain, and seven days later, the mPFC was cannulated bilaterally. The paw withdrawal threshold fifty percent (50% PWT) was recorded on the 14th day. Results: Microinjection of L-Arg (2.87, 11.5 and 45.92 nmol per 0.25 µL) increased 50% PWT. L-NAME (17.15 nmol per 0.25 µL) and naloxonazine (an antagonist of mu opioid receptors, 1.54 nmol per 0.25 µL) inhibited anti-allodynia induced by LArg (45.92 nmol per 0.25 µL). Naltrindole (a delta opioid receptor antagonist, 2.45 nmol per 0.25 µL) and nor-binaltorphimine (a kappa opioid receptor antagonist, 1.36 nmol per 0.25 µL) were unable to prevent L-Arg (45.92 nmol per 0.25 µL)-induced antiallodynia. Conclusions: Our results indicate that the NO system in the mPFC regulates neuropathic pain. Mu opioid receptors of this area might participate in pain relief caused by L-Arg.
참고문헌 (49)
- Cury Y, "Pain and analgesia : the dual effect of nitric oxide in the nociceptive system", Nitric Oxide, 25, pp.243~254 (2011)
- Spiller F, "Targeting nitric oxide as a key modulator of sepsis, arthritis and pain", Nitric Oxide, 89, pp.32~40 (2019)
- Toda N, "Modulation of opioid actions by nitric oxide signaling", Anesthesiology, 110, pp.166~181 (2009)
- Lotfipour S, "Morphine hyposensitivity in streptozotocin-diabetic rats : reversal by dietary l-arginine treatment", Clin Exp Pharmacol Physiol, 45, pp.42~49 (2018)
- Salighedar R, "Medial prefrontal cortex oxytocin-opioid receptors interaction in spatial memory processing in rats", Physiol Behav, 209, pp.112599~ (2019)
- Xu P, "Medial prefrontal cortex in neurological diseases", Physiol Genomics, 51, pp.432~442 (2019)
- Qian Y, "MKP1 in the medial prefrontal cortex modulates chronic neuropathic pain via regulation of p38 and JNK1", 2, 2020, pp.130, 643~652
- Ong WY, "Role of the prefrontal cortex in pain processing", Mol Neurobiol, 56, pp.1137~1166 (2019)
- Kummer KK, "The medial prefrontal cortex as a central hub for mental comorbidities associated with chronic pain", Int J Mol Sci, 21, pp.3440~ (2020)
- Tamaddonfard E, "Medial prefrontal cortex diclofenac-induced antinociception is mediated through GPR55, cannabinoid CB1, and mu-opioid receptors of this area and periaqueductal gray", Naunyn Schmiedebergs Arch Pharmacol, 393, pp.371~379 (2020)
- Tu Y, "Abnormal medial prefrontal cortex functional connectivity and its association with clinical symptoms in chronic low back pain", Pain, 160, pp.1308~1318 (2019)
- Scholz J, "The IASP classification of chronic pain for ICD-11 : chronic neuropathic pain", Pain, 160, pp.53~59 (2019)
- Jensen TS, "Allodynia and hyperalgesia in neuropathic pain : clinical manifestations and mechanisms", Lancet Neurol, 13, pp.924~935 (2014)
- Challa SR, "Surgical animal models of neuropathic pain : pros and cons", Int J Neurosci, 125, pp.170~174 (2015)
- Vila-Verde C, "Nitric oxide in the prelimbic medial prefrontal cortex is involved in the anxiogenic-like effect induced by acute restraint stress in rats", Neuroscience, 320, pp.30~42 (2016)
- Liu W, "Repeated nitrous oxide exposure exerts antidepressant-like effects through neuronal nitric oxide synthase activation in the medial prefrontal cortex", Front Psychiatry, 11, pp.837~ (2020)
- Liang HY, "nNOS-expressing neurons in the vmPFC transform pPVTderived chronic pain signals into anxiety behaviors", Nat Commun, 11, pp.2501~ (2020)
- Salimi S, "Microinjection of histamine and its H3 receptor agonist and antagonist into the agranular insular cortex influence sensory and affective components of neuropathic pain in rats", Eur J Pharmacol, 857, pp.172450~ (2019)
- Taati M, "Ventrolateral orbital cortex oxytocin attenuates neuropathic pain through periaqueductal gray opioid receptor", Pharmacol Rep, 70, pp.577~583 (2018)
- Paxinos G, "The rat brain in stereotaxic coordinates" (2007), Elsevier
- Erfanparast A, "Involvement of central opiate receptors in modulation of centrally administered oxytocin-induced antinociception", Iran J Basic Med Sci, 21, pp.1275~1280 (2018)
- Karimi S, "Reversal effect of intra-central amygdala microinjection of L-arginine on place aversion induced by naloxone in morphine conditioned rats", Iran Biomed J, 15, pp.92~99 (2011)
- Dixon WJ, "Efficient analysis of experimental observations", Annu Rev Pharmacol Toxicol, 20, pp.441~462 (1980)
- Chaplan SR, "Quantitative assessment of tactile allodynia in the rat paw", J Neurosci Methods, 53, pp.55~63 (1994)
- Bastuji H, "Pain networks from the inside : spatiotemporal analysis of brain responses leading from nociception to conscious perception", Hum Brain Mapp, 37, pp.4301~4315 (2016)
- Xu N, "Spared nerve injury increases the expression of microglia M1 markers in the prefrontal cortex of rats and provokes depressionlike behaviors", Front Neurosci, 11, pp.209~ (2017)
- Parvardeh S, "Role of L-arginine", NO, KATP channel signaling pathway in the central and peripheral antinociceptive effect of thymoquinone in rats, pp.Iran J Basic Med Sci, 2018[DOI]
- Fan W, "The role of nitric oxide in orofacial pain", Nitric Oxide, 26, pp.32~37 (2012)
- Miranda HF, "Nitric oxide mediated dexketoprofen antinociception", J Exp Res, 8, pp.16~22 (2020)
- Fakhri S, "The antinociceptive mechanisms of melatonin : role of L-arginine", nitric oxide, KATP channel signaling pathway, pp.Behav Pharmacol, 2020[DOI]
- Mohammadi S, "Astaxanthin engages the l-arginine", NO, KATP channel signaling pathway toward antinociceptive effects, pp.Behav Pharmacol, 2021[DOI]
- Zhuo M, "Endogenous nitric oxide is required for tonic cholinergic inhibition of spinal mechanical transmission", Pain, 54, pp.71~78 (1993)
- Iwamoto ET, "Pharmacological evidence that nitric oxide mediates the antinociception produced by muscarinic agonists in the rostral ventral medulla of rats", J Pharmacol Exp Ther, 269, pp.699~708 (1994)
- Pan HL, "Role of spinal NO in antiallodynic effect of intrathecal clonidine in neuropathic rats", Anesthesiology, 89, pp.1518~1523 (1998)
- Kawabata A, "Antinociceptive effect of L-arginine on the carrageenin-induced hyperalgesia of the rat : possible involvement of central opioidergic systems", Eur J Pharmacol, 218, pp.153~158 (1992)
- Roche AK, "A nitric oxide synthesis inhibitor(L-NAME)reduces licking behavior and Fos-labeling in the spinal cord of rats during formalininduced inflammation", Pain, 66, pp.331~341 (1996)
- 오민혜, "흰쥐의 포르말린시험에서 복강 내로 투여한 비선택적 산화질소합성효소 억제제의 항통각효과", The Korean Journal of Pain, 19(2), pp.3~3 (2006), 대한통증학회
- Kampa M, "Opioids are non-competitive inhibitors of nitric oxide synthase in T47D human breast cancer cells", Cell Death Differ, 8, pp.943~952 (2001)
- Dietis N, "Opioid receptor subtypes : fact or artifact", Br J Anaesth, 107, pp.8~18 (2011)
- Chung E, "Dynorphin-mediated antinociceptive effects of L-arginine and SIN-1(an NO donor)in mice", Brain Res Bull, 70, pp.245~250 (2006)
- Javanmardi K, "Involvement of N-methyl-D-aspartate receptors and nitric oxide in the rostral ventromedial medulla in modulating morphine pain-inhibitory signals from the periaqueductal grey matter in rats", Clin Exp Pharmacol Physiol, 32, pp.585~589 (2005)
- Hafeshjani ZK, "Nitric oxide in the hippocampal cortical area interacts with naloxone in inducing pain", Indian J Pharmacol, 44, pp.443~447 (2012)
- Pol O, "The involvement of the nitric oxide in the effects and expression of opioid receptors during peripheral inflammation", Curr Med Chem, 14, pp.1945~1955 (2007)
- Hervera A, "Peripheral effects of morphine and expression of μ-opioid receptors in the dorsal root ganglia during neuropathic pain : nitric oxide signaling", Mol Pain, 7, pp.25~ (2011)
- Cadet P, "Real-time RTPCR measurement of the modulation of Mu opiate receptor expression by nitric oxide in human mononuclear cells", Med Sci Monit, 7, pp.1123~1128 (2001)
- Babey AM, "Nitric oxide and opioid tolerance", Neuropharmacology, 33, pp.1463~1470 (1994)
- Heinzen EL, "Neuronal nitric oxide modulates morphine antinociceptive tolerance by enhancing constitutive activity of the mu-opioid receptor", Biochem Pharmacol, 69, pp.679~688 (2005)
- Huang L, "Nitric oxide modulates μ-opioid receptor function in vitro", Clin Exp Pharmacol Physiol, 46, pp.676~685 (2019)
- Cheriyan J, "Altered excitability and local connectivity of mPFC-PAG neurons in a mouse model of neuropathic pain", J Neurosci, 38, pp.4829~4839 (2018)