Long-lasting reflexive and nonreflexive pain responses in two mouse models of fibromyalgia-like condition.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
12 06 2022
12 06 2022
Historique:
received:
04
04
2022
accepted:
31
05
2022
entrez:
12
6
2022
pubmed:
13
6
2022
medline:
15
6
2022
Statut:
epublish
Résumé
Nociplastic pain arises from altered nociception despite no clear evidence of tissue or somatosensory system damage, and fibromyalgia syndrome can be highlighted as a prototype of this chronic pain subtype. Currently, there is a lack of effective treatments to alleviate both reflexive and nonreflexive pain responses associated with fibromyalgia condition, and suitable preclinical models are needed to assess new pharmacological strategies. In this context, although in recent years some remarkable animal models have been developed to mimic the main characteristics of human fibromyalgia, most of them show pain responses in the short term. Considering the chronicity of this condition, the present work aimed to develop two mouse models showing long-lasting reflexive and nonreflexive pain responses after several reserpine (RIM) or intramuscular acid saline solution (ASI) injections. To our knowledge, this is the first study showing that RIM6 and ASI mouse models show reflexive and nonreflexive responses up to 5-6 weeks, accompanied by either astro- or microgliosis in the spinal cord as pivotal physiopathology processes related to such condition development. In addition, acute treatment with pregabalin resulted in reflexive pain response alleviation in both the RIM6 and ASI models. Consequently, both may be considered suitable experimental models of fibromyalgia-like condition, especially RIM6.
Identifiants
pubmed: 35691979
doi: 10.1038/s41598-022-13968-7
pii: 10.1038/s41598-022-13968-7
pmc: PMC9189106
doi:
Substances chimiques
Pregabalin
55JG375S6M
Reserpine
8B1QWR724A
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9719Informations de copyright
© 2022. The Author(s).
Références
Treede, R. D. et al. A classification of chronic pain for ICD-11. Pain 156, 1003–1007 (2015).
pubmed: 25844555
pmcid: 4450869
doi: 10.1097/j.pain.0000000000000160
Basbaum, A. I., Bautista, D. M., Scherrer, G. & Julius, D. Cellular and molecular mechanisms of pain. Cell 139, 267–284 (2009).
pubmed: 19837031
pmcid: 2852643
doi: 10.1016/j.cell.2009.09.028
Shraim, M. A., Massé-Alarie, H., Hall, L. M. & Hodges, P. W. Systematic review and synthesis of mechanism-based classification systems for pain experienced in the musculoskeletal system. Clin. J. Pain 36, 793–812 (2020).
pubmed: 32852923
doi: 10.1097/AJP.0000000000000860
Treede, R. D. et al. Chronic pain as a symptom or a disease: The IASP Classification of Chronic Pain for the International Classification of Diseases (ICD-11). Pain 160, 19–27 (2019).
pubmed: 30586067
doi: 10.1097/j.pain.0000000000001384
Fitzcharles, M. A. et al. Nociplastic pain: Towards an understanding of prevalent pain conditions. Lancet 397, 2098–2110 (2021).
pubmed: 34062144
doi: 10.1016/S0140-6736(21)00392-5
Nicholas, M. et al. The IASP classification of chronic pain for ICD-11: Chronic primary pain. Pain 160, 28–37 (2019).
pubmed: 30586068
doi: 10.1097/j.pain.0000000000001390
Fitzcharles, M. A., Petzke, F., Tölle, T. R. & Häuser, W. Cannabis-based medicines and medical cannabis in the treatment of nociplastic pain. Drugs 81, 2103–2116 (2021).
pubmed: 34800285
doi: 10.1007/s40265-021-01602-1
Arnold, L. M. et al. AAPT diagnostic criteria for fibromyalgia. J. Pain. 20, 611–628 (2019).
pubmed: 30453109
doi: 10.1016/j.jpain.2018.10.008
Hurtig, I. M., Raak, R. I., Kendall, S. A., Gerdle, B. & Wahren, L. K. Quantitative sensory testing in fibromyalgia patients and in healthy subjects: Identification of subgroups. Clin J Pain. 17, 316–322 (2001).
pubmed: 11783811
doi: 10.1097/00002508-200112000-00005
Staud, R., Godfrey, M. M. & Robinson, M. E. Fibromyalgia patients are not only hypersensitive to painful stimuli but also to acoustic stimuli. J Pain. 22, 914–925 (2021).
pubmed: 33636370
doi: 10.1016/j.jpain.2021.02.009
Queiroz, L. P. Worldwide epidemiology of fibromyalgia. Curr. Pain Headache Rep. 17, 356 (2013).
pubmed: 23801009
doi: 10.1007/s11916-013-0356-5
Ablin, J. N. & Häuser, W. Fibromyalgia syndrome: Novel therapeutic targets. Pain Manag. 6, 371–381 (2016).
pubmed: 27296699
doi: 10.2217/pmt-2016-0007
Calandre, E. P., Rico-Villademoros, F. & Slim, M. An update on pharmacotherapy for the treatment of fibromyalgia. Expert Opin. Pharmacother. 16, 1347–1368 (2015).
pubmed: 26001183
doi: 10.1517/14656566.2015.1047343
Borchers, A. T. & Gershwin, M. E. Fibromyalgia: A critical and comprehensive review. Clin. Rev. Allergy Immunol. 49, 100–151 (2015).
pubmed: 26445775
doi: 10.1007/s12016-015-8509-4
Nagakura, Y., Oe, T., Aoki, T. & Matsuoka, N. Biogenic amine depletion causes chronic muscular pain and tactile allodynia accompanied by depression: A putative animal model of fibromyalgia. Pain 146, 26–33 (2009).
pubmed: 19646816
doi: 10.1016/j.pain.2009.05.024
Nagakura, Y. et al. Different pathophysiology underlying animal models of fibromyalgia and neuropathic pain: Comparison of reserpine-induced myalgia and chronic constriction injury rats. Behav. Brain Res. 226, 242–249 (2012).
pubmed: 21945299
doi: 10.1016/j.bbr.2011.09.023
Taguchi, T. et al. Peripheral and spinal mechanisms of nociception in a rat reserpine-induced pain model. Pain 156, 415–427 (2015).
pubmed: 25599239
doi: 10.1097/01.j.pain.0000460334.49525.5e
Arora, V. & Chopra, K. Possible involvement of oxido-nitrosative stress induced neuro-inflammatory cascade and monoaminergic pathway: Underpinning the correlation between nociceptive and depressive behaviour in a rodent model. J. Affect Disord. 151, 1041–1052 (2013).
pubmed: 24126118
doi: 10.1016/j.jad.2013.08.032
Liu, S. B. et al. Attenuation of reserpine-induced pain/depression dyad by Gentiopicroside through downregulation of GluN2B receptors in the amygdala of mice. NeuroMol. Med. 16, 350–359 (2014).
doi: 10.1007/s12017-013-8280-8
Klein, C. P. et al. Coadministration of resveratrol and rice oil mitigates nociception and oxidative state in a mouse fibromyalgia-like model. Pain Res. Treat. 2016, 3191638 (2016).
Ejiri, Y., Uta, D., Ota, H., Mizumura, K. & Taguchi, T. Nociceptive chemical hypersensitivity in the spinal cord of a rat reserpine-induced fibromyalgia model. Neurosci. Res. S0168–0102(22), 00080–00083 (2022).
Sharma, N. K., Ryals, J. M., Liu, H., Liu, W. & Wright, D. E. Acidic saline-induced primary and secondary mechanical hyperalgesia in mice. J. Pain. 10, 1231–1241 (2009).
pubmed: 19592308
pmcid: 2787877
doi: 10.1016/j.jpain.2009.04.014
Yen, L. T., Hsieh, C. L., Hsu, H. C. & Lin, Y. W. Targeting ASIC3 for relieving mice fibromyalgia pain: Roles of electroacupuncture, opioid, and adenosine. Sci Rep. 7, 46663 (2017).
pubmed: 28440280
pmcid: 5404229
doi: 10.1038/srep46663
Jasper, L. L. & MacNeil, B. J. Diverse sensory inputs permit priming in the acidic saline model of hyperalgesia. Eur. J. Pain. 16, 966–973 (2012).
pubmed: 22337570
pmcid: 3357443
doi: 10.1002/j.1532-2149.2011.00103.x
Lin, J. G., Hsieh, C. L. & Lin, Y. W. Analgesic effect of electroacupuncture in a mouse fibromyalgia model: Roles of TRPV1, TRPV4, and pERK. PLoS ONE 10, 1–16 (2015).
Yokoyama, T., Maeda, Y., Audette, K. M. & Sluka, K. A. Pregabalin reduces muscle and cutaneous hyperalgesia in two models of chronic muscle pain in rats. J. Pain. 8, 422–429 (2007).
pubmed: 17293165
doi: 10.1016/j.jpain.2006.11.007
Liu, Y.-T., Shao, Y.-W., Yen, C.-T. & Shaw, F.-Z. Acid-induced hyperalgesia and anxio-depressive comorbidity in rats. Physiol. Behav. 131, 105–110 (2014).
pubmed: 24726391
doi: 10.1016/j.physbeh.2014.03.030
Morton, D. B. & Griffiths, P. H. Guidelines on the recognition of pain, distress and discomfort in experimental animals and an hypothesis for assessment. Vet. Rec. 116, 431–436 (1985).
pubmed: 3923690
doi: 10.1136/vr.116.16.431
Brum, E. S., Becker, G., Fialho, M. F. P. & Oliveira, S. M. Animal models of fibromyalgia: What is the best choice?. Pharmacol. Ther. 230, 107959 (2022).
pubmed: 34265360
doi: 10.1016/j.pharmthera.2021.107959
Naudon, L. et al. Reserpine affects differentially the density of the vesicular monoamine transporter and dihydrotetrabenazine binding sites. Eur. J. Neurosci. 8, 842–846 (1996).
pubmed: 9081637
doi: 10.1111/j.1460-9568.1996.tb01271.x
Antkiewicz-Michaluk, L., Wąsik, A., Możdżeń, E., Romańska, I. & Michaluk, J. Withdrawal from repeated administration of a low dose of reserpine induced opposing adaptive changes in the noradrenaline and serotonin system function: A behavioral and neurochemical ex vivo and in vivo studies in the rat. Prog. Neuropsychopharmacol. Biol. Psychiatry. 57, 146–154 (2015).
pubmed: 25445479
doi: 10.1016/j.pnpbp.2014.10.009
Kiso, T., Moriyama, A., Furutani, M., Matsuda, R. & Funatsu, Y. Effects of pregabalin and duloxetine on neurotransmitters in the dorsal horn of the spinal cord in a rat model of fibromyalgia. Eur. J. Pharmacol. 827, 117–124 (2018).
pubmed: 29530591
doi: 10.1016/j.ejphar.2018.03.011
Ogino, S. et al. Systemic administration of 5-HT 2C receptor agonists attenuates muscular hyperalgesia in reserpine-induced myalgia model. Pharmacol. Biochem. Behav. 108, 8–15 (2013).
pubmed: 23603031
doi: 10.1016/j.pbb.2013.04.007
Lariviere, W. R. & Melzack, R. The role of corticotropin-releasing factor in pain and analgesia. Pain 84, 1–12 (2000).
pubmed: 10601667
doi: 10.1016/S0304-3959(99)00193-1
Martínez-Lorenzana, G., Palma-Tirado, L., Cifuentes-Diaz, C., González-Hernández, A. & Condés-Lara, M. Ultrastructural evidence for oxytocin and oxytocin receptor at the spinal dorsal horn: Mechanism of nociception modulation. Neuroscience 475, 117–126 (2021).
pubmed: 34530103
doi: 10.1016/j.neuroscience.2021.09.004
Koga, K. et al. Ascending noradrenergic excitation from the locus coeruleus to the anterior cingulate cortex. Mol. Brain. 13, 49 (2020).
pubmed: 32216807
pmcid: 7098117
doi: 10.1186/s13041-020-00586-5
Barasi, S. & Clatworthy, A. The effects of intrathecally applied noradrenaline and 5-hydroxytryptamine on spinal nocifensive reflexes and the rostral transmission of noxious information to the thalamus in the rat. Neurosci. Lett. 78, 328–332 (1987).
pubmed: 2819789
doi: 10.1016/0304-3940(87)90382-X
Hoheisel, U., Reinöhl, J., Unger, T. & Mense, S. Acidic pH and capsaicin activate mechanosensitive group IV muscle receptors in the rat. Pain 110, 149–157 (2004).
pubmed: 15275762
doi: 10.1016/j.pain.2004.03.043
Fujii, Y. et al. TRP channels and ASICs mediate mechanical hyperalgesia in models of inflammatory muscle pain and delayed onset muscle soreness. Pain 140, 292–304 (2008).
pubmed: 18834667
doi: 10.1016/j.pain.2008.08.013
Yen, L. T., Hsieh, C. L., Hsu, H. C. & Lin, Y. W. Targeting ASIC3 for relieving mice fibromyalgia pain: Roles of electroacupuncture, opioid, and adenosine. Sci. Rep. 7, 46663 (2017).
pubmed: 28440280
pmcid: 5404229
doi: 10.1038/srep46663
Gautam, M., Benson, C. J., Ranier, J. D., Light, A. R. & Sluka, K. A. ASICs do not play a role in maintaining hyperalgesia induced by repeated intramuscular acid injections. Pain Res. Treat. 2012, 817347 (2012).
pubmed: 22191025
Uta, D., Tsuboshima, K., Nishijo, H., Mizumura, K. & Taguchi, T. Neuronal sensitization and synaptic facilitation in the superficial dorsal horn of a rat reserpine-induced pain model. Neuroscience 479, 125–139 (2021).
pubmed: 34673142
doi: 10.1016/j.neuroscience.2021.10.010
Abd-ellatief, R. B., Mohamed, H. K. & Kotb, H. I. Reactive astrogliosis in an experimental model of fibromyalgia: Effect of dexmedetomidine. Cells Tissues Organs 205, 105–119 (2018).
pubmed: 29843137
doi: 10.1159/000488757
Ji, R. R., Nackley, A., Huh, Y., Terrando, N. & Maixner, W. Neuroinflammation and central sensitization in chronic and widespread pain. Anesthesiology 129, 343–366 (2018).
pubmed: 29462012
doi: 10.1097/ALN.0000000000002130
Handa, J., Sekiguchi, M., Krupkova, O. & Konno, S. The effect of serotonin-noradrenaline reuptake inhibitor duloxetine on the intervertebral disk-related radiculopathy in rats. Eur. Spine J. 25, 877–887 (2016).
pubmed: 26394856
doi: 10.1007/s00586-015-4239-9
Bar El, Y., Kanner, S., Barzilai, A. & Hanein, Y. Activity changes in neuron-astrocyte networks in culture under the effect of norepinephrine. PLoS ONE 13, e0203761 (2018).
pubmed: 30332429
pmcid: 6192555
doi: 10.1371/journal.pone.0203761
Tawfik, M. K., Helmy, S. A., Badran, D. I. & Zaitone, S. A. Neuroprotective effect of duloxetine in a mouse model of diabetic neuropathy: Role of glia suppressing mechanisms. Life Sci. 205, 113–124 (2018).
pubmed: 29763613
doi: 10.1016/j.lfs.2018.05.025
Tsuda, M., Koga, K., Chen, T. & Zhuo, M. Neuronal and microglial mechanisms for neuropathic pain in the spinal dorsal horn and anterior cingulate cortex. J. Neurochem. 141, 486–498 (2017).
pubmed: 28251660
doi: 10.1111/jnc.14001
Zhao, H. et al. The role of microglia in the pathobiology of neuropathic pain development: What do we know?. Br. J. Anaesth. 118, 504–516 (2017).
pubmed: 28403399
doi: 10.1093/bja/aex006
Inoue, K. & Tsuda, M. Microglia in neuropathic pain: Cellular and molecular mechanisms and therapeutic potential. Nat. Rev. Neurosci. 19, 138–152 (2018).
pubmed: 29416128
doi: 10.1038/nrn.2018.2
Carson, M. J., Thomas, E. A., Danielson, P. E. & Sutcliffe, J. G. The 5HT5A serotonin receptor is expressed predominantly by astrocytes in which it inhibits cAMP accumulation: A mechanism for neuronal suppression of reactive astrocytes. Glia 17, 317–326 (1996).
pubmed: 8856328
doi: 10.1002/(SICI)1098-1136(199608)17:4<317::AID-GLIA6>3.0.CO;2-W
Gavrilyuk, V. et al. Norepinephrine increases I kappa B alpha expression in astrocytes. J. Biol. Chem. 277, 29662–29668 (2002).
pubmed: 12050158
doi: 10.1074/jbc.M203256200
Morioka, N., Tanabe, H., Inoue, A., Dohi, T. & Nakata, Y. Noradrenaline reduces the ATP-stimulated phosphorylation of p38 MAP kinase via beta-adrenergic receptors-cAMP-protein kinase A-dependent mechanism in cultured rat spinal microglia. Neurochem. Int. 55, 226–234 (2009).
pubmed: 19524113
doi: 10.1016/j.neuint.2009.03.004
Fujita, H., Tanaka, J., Maeda, N. & Sakanaka, M. Adrenergic agonists suppress the proliferation of microglia through beta 2-adrenergic receptor. Neurosci. Lett. 242, 37–40 (1998).
pubmed: 9509999
doi: 10.1016/S0304-3940(98)00003-2
Sweitzer, S. M., Colburn, R. W., Rutkowski, M. & DeLeo, J. A. Acute peripheral inflammation induces moderate glial activation and spinal IL-1beta expression that correlates with pain behavior in the rat. Brain Res. 829, 209–221 (1999).
pubmed: 10350552
doi: 10.1016/S0006-8993(99)01326-8
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. 20, 467–473 (2004).
pubmed: 15233755
doi: 10.1111/j.1460-9568.2004.03514.x
Clark, A. K., Gentry, C., Bradbury, E. J., McMahon, S. B. & Malcangio, M. Role of spinal microglia in rat models of peripheral nerve injury and inflammation. Eur. J. Pain. 11, 223–230 (2007).
pubmed: 16545974
doi: 10.1016/j.ejpain.2006.02.003
Vega-Avelaira, D., Ballesteros, J. J. & López-García, J. A. Inflammation-induced hyperalgesia and spinal microglia reactivity in neonatal rats. Eur. J. Pain. 17, 1180–1188 (2013).
pubmed: 23553993
doi: 10.1002/j.1532-2149.2013.00308.x
Kettenmann, H., Hanisch, U. K., Noda, M. & Verkhratsky, A. Physiology of microglia. Physiol. Rev. 91, 461–553 (2011).
pubmed: 21527731
doi: 10.1152/physrev.00011.2010
Verkhratsky, A. & Chvátal, A. NMDA receptors in astrocytes. Neurochem. Res. 45, 122–133 (2019).
pubmed: 30767094
doi: 10.1007/s11064-019-02750-3
Boadas-Vaello, P., Homs, J., Reina, F., Carrera, A. & Verdú, E. Neuroplasticity of supraspinal structures associated with pathological pain. Anat. Rec. (Hoboken). 300, 1481–1501 (2017).
pubmed: 28263454
doi: 10.1002/ar.23587
D’Amico, R. et al. Inhibition of P2X7 purinergic receptor ameliorates fibromyalgia syndrome by suppressing NLRP3 pathway. Int. J. Mol. Sci. 22, 6471 (2021).
pubmed: 34208781
pmcid: 8234677
doi: 10.3390/ijms22126471
Fusco, R. et al. Melatonin plus folic acid treatment ameliorates reserpine-induced fibromyalgia: An evaluation of pain, oxidative stress, and inflammation. Antioxidants 8, 628 (2019).
pmcid: 6943570
doi: 10.3390/antiox8120628
Boada, M. D., Martin, T. J. & Ririe, D. G. Nerve injury induced activation of fast-conducting high threshold mechanoreceptors predicts non-reflexive pain related behavior. Neurosci. Lett. 632, 44–49 (2016).
pubmed: 27544012
pmcid: 5310223
doi: 10.1016/j.neulet.2016.08.029
Cho, H. et al. Voluntary movements as a possible non-reflexive pain assay. Mol. Pain. 9, 25 (2013).
pubmed: 23688027
pmcid: 3716716
doi: 10.1186/1744-8069-9-25
de la Puente, B. et al. Pharmacological sensitivity of reflexive and nonreflexive outcomes as a correlate of the sensory and affective responses to visceral pain in mice. Sci. Rep. 7, 13428 (2017).
pubmed: 29044171
pmcid: 5647413
doi: 10.1038/s41598-017-13987-9
Chodroff, L., Bendele, M., Valenzuela, V., Henry, M. & Ruparel, S. EXPRESS: BDNF signaling contributes to oral cancer pain in a preclinical orthotopic rodent model. Mol. Pain. 12, 1744806916666841 (2016).
pubmed: 27590070
pmcid: 5015823
doi: 10.1177/1744806916666841
Nagakura, Y. et al. Spontaneous pain-associated facial expression and efficacy of clinically used drugs in the reserpine-induced rat model of fibromyalgia. Eur. J. Pharmacol. 864, 172716 (2019).
pubmed: 31589868
doi: 10.1016/j.ejphar.2019.172716
Tanei, S., Miwa, M., Yoshida, M., Miura, R. & Nagakura, Y. The method simulating spontaneous pain in patients with nociplastic pain using rats with fibromyalgia-like condition. MethodsX. 7, 100826 (2020).
pubmed: 32195142
pmcid: 7078388
doi: 10.1016/j.mex.2020.100826
de la Puente, B. et al. Comprehensive preclinical assessment of sensory, functional, motivational-affective, and neurochemical outcomes in neuropathic pain: The case of the sigma-1 receptor. ACS Pharmacol. Transl. Sci. 5, 240–254 (2022).
pubmed: 35434530
doi: 10.1021/acsptsci.2c00005
Nagakura, Y. et al. Monoamine system disruption induces functional somatic syndromes associated symptomatology in mice. Physiol. Behav. 194, 505–514 (2018).
pubmed: 29981307
doi: 10.1016/j.physbeh.2018.07.007
Schossler Garcia, C. et al. Effect of m-trifluoromethyl-diphenyl diselenide on the pain-depression dyad induced by reserpine: Insights on oxidative stress, apoptotic, and glucocorticoid receptor modulation. Mol. Neurobiol. 58, 5078–5089 (2021).
pubmed: 34245440
doi: 10.1007/s12035-021-02483-x
Park, J. H. et al. Effect of pregabalin on nociceptive thresholds and immune responses in a mouse model of incisional pain. Korean J. Pain. 34, 185–192 (2021).
pubmed: 33785670
pmcid: 8019952
doi: 10.3344/kjp.2021.34.2.185
Kim, J. Y., Abdi, S., Huh, B. & Kim, K. H. Mirogabalin: Could it be the next generation gabapentin or pregabalin?. Korean J. Pain. 34, 4–18 (2021).
pubmed: 33380563
pmcid: 7783847
doi: 10.3344/kjp.2021.34.1.4
Gonzalez-Soler, E. M. et al. Chronic pregabalin treatment ameliorates pain, but not depressive-like behaviors, in a reserpine-induced myalgia model in rats. Pain Phys. 23, E581–E590 (2020).
Field, M. J. Identification of the alpha2-delta-1 subunit of voltage-dependent calcium channels as a molecular target for pain mediating the analgesic actions of pregabalin. Proc. Natl. Acad. Sci. USA 103, 17537–17542 (2006).
pubmed: 17088553
pmcid: 1859964
doi: 10.1073/pnas.0409066103
Matsuzawa, R. et al. Presynaptic inhibitory actions of pregabalin on excitatory transmission in superficial dorsal horn of mouse spinal cord: Further characterization of presynaptic mechanisms. Neurosci. Lett. 558, 186–191 (2014).
pubmed: 24269977
doi: 10.1016/j.neulet.2013.11.017
Tuchman, M., Barrett, J. A., Donevan, S., Hedberg, T. G. & Taylor, C. P. Central sensitization and Ca(V)α
pubmed: 20472509
doi: 10.1016/j.jpain.2010.02.024
Cao, Y., Wang, H., Chiang, C. Y., Dostrovsky, J. O. & Sessle, B. J. Pregabalin suppresses nociceptive behavior and central sensitization in a rat trigeminal neuropathic pain model. J. Pain. 14, 193–204 (2013).
pubmed: 23374941
pmcid: 3575215
doi: 10.1016/j.jpain.2012.11.005
Skowrońska, K., Obara-Michlewska, M., Zielińska, M. & Albrecht, J. NMDA receptors in astrocytes: In search for roles in neurotransmission and astrocytic homeostasis. Int. J. Mol. Sci. 20, 309 (2019).
pmcid: 6358855
doi: 10.3390/ijms20020309
Hansen, R. R. & Malcangio, M. Astrocytes—multitaskers in chronic pain. Eur. J. Pharmacol. 716, 120–128 (2013).
pubmed: 23528354
doi: 10.1016/j.ejphar.2013.03.023
Zimmermann, M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16, 109–110 (1983).
pubmed: 6877845
doi: 10.1016/0304-3959(83)90201-4
Kim, S. H., Song, J., Mun, H. & Keon, U. P. Effect of the combined use of tramadol and milnacipran on pain threshold in an animal model of fibromyalgia. Korean J. Intern Med. 24, 139–142 (2009).
pubmed: 19543493
pmcid: 2698623
doi: 10.3904/kjim.2009.24.2.139
Hargreaves, K., Dubner, R., Brown, F., Flores, C. & Joris, J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32, 77–88 (1988).
pubmed: 3340425
doi: 10.1016/0304-3959(88)90026-7
Castany, S. et al. Critical role of sigma-1 receptors in central neuropathic pain-related behaviours after mild spinal cord injury in mice. Sci. Rep. 8, 3873 (2018).
pubmed: 29497125
pmcid: 5832850
doi: 10.1038/s41598-018-22217-9
Castany, S. et al. Repeated sigma-1 receptor antagonist MR309 administration modulates central neuropathic pain development after spinal cord injury in mice. Front Pharmacol. 10, 222 (2019).
pubmed: 30967775
pmcid: 6439356
doi: 10.3389/fphar.2019.00222
Chaplan, S. R., Bach, F. W., Pogrel, J. W., Chung, J. M. & Yaksh, T. L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods. 53, 55–63 (1994).
pubmed: 7990513
doi: 10.1016/0165-0270(94)90144-9
Bisaz, R., Boadas-Vaello, P., Genoux, D. & Sandi, C. Age-related cognitive impairments in mice with a conditional ablation of the neural cell adhesion molecule. Learn. Mem. 20, 183–193 (2013).
pubmed: 23504516
doi: 10.1101/lm.030064.112
Porsolt, R. D., Bertin, A. & Jalfre, M. Behavioral despair in mice: A primary screening test for antidepressants. Arch. Int. Pharmacodyn. Thérapie. 229, 327–336 (1977).
Caldarone, B. J., Zachariou, V. & King, S. L. Rodent models of treatment-resistant depression. Eur. J. Pharmacol. 753, 51–65 (2015).
pubmed: 25460020
doi: 10.1016/j.ejphar.2014.10.063
Zamboni, L. & De Martino, C. Buffered picric acid-formaldehyde: A new, rapid, fixative for electron microscopy. J. Cell Biol. 35, 148A (1967).
Álvarez-Pérez, B. et al. Epigallocatechin-3-gallate treatment reduces thermal hyperalgesia after spinal cord injury by down-regulating RhoA expression in mice. Eur. J. Pain. 20, 341–352 (2016).
pubmed: 25913854
doi: 10.1002/ejp.722
Hanisch, U. K. & Kettenmann, H. Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10, 1387–1394 (2007).
pubmed: 17965659
doi: 10.1038/nn1997