Response to pregabalin and progesterone differs in male and female rat models of neuropathic and cancer pain

References

• Baron R. Mechanisms of disease: neuropathic pain—a clinical perspective. Nat Clin Pract Neurol. 2006;2(2):95–106. doi:10.1038/ncpneuro0113.
   PubMedGoogle Scholar
• Zhu Y, Henry JL. Excitability of Aβ sensory neurons is altered in an animal model of peripheral neuropathy. BMC Neurosci. 2012;13(1):15. doi:10.1186/1471-2202-13-15.
   Google Scholar
• Jimenez-Andrade JM, Mantyh WG, Bloom AP, Ferng AS, Geffre CP, Mantyh PW. Bone cancer pain. Ann N Y Acad Sci. 2010;1198:173–81. doi:10.1111/j.1749-6632.2009.05429.x.
   PubMed Web of Science ®Google Scholar
• Colvin L, Fallon M. Challenges in cancer pain management–bone pain. Eur J Cancer. 2008;44(8):1083–90. doi:10.1016/j.ejca.2008.03.001.
   Web of Science ®Google Scholar
• Roglio I, Bianchi R, Gotti S, Scurati S, Giatti S, Pesaresi M, Caruso D, Panzica GC, Melcangi RC. Neuroprotective effects of dihydroprogesterone and progesterone in an experimental model of nerve crush injury. Neuroscience. 2008;155(3):673–85. doi:10.1016/j.neuroscience.2008.06.034.
   Web of Science ®Google Scholar
• Coronel MF, Labombarda F, Villar MJ, De Nicola AF, González SL. Progesterone prevents allodynia after experimental spinal cord injury. J Pain. 2011;12(1):71–83. doi:10.1016/j.jpain.2010.04.013.
   PubMed Web of Science ®Google Scholar
• Meyer L, Patte-Mensah C, Taleb O, Mensah-Nyagan AG. Cellular and functional evidence for a protective action of neurosteroids against vincristine chemotherapy-induced painful neuropathy. Cell Mol Life Sci. 2010;67(17):3017–34. doi:10.1007/s00018-010-0372-0.
   Web of Science ®Google Scholar
• Dableh LJ, Henry JL. Progesterone prevents development of neuropathic pain in a rat model: timing and duration of treatment are critical. J Pain Res. 2011;4:91–101. doi:10.2147/JPR.S17009.
   Google Scholar
• Landau RL, Ehrlich EN, Huggins C. Estradiol benzoate and progesterone in advanced human-breast cancer. JAMA. 1962;182(6):632–36. doi:10.1001/jama.1962.03050450032008.
   Web of Science ®Google Scholar
• Sribnick EA, Del Re AM, Ray SK, Woodward JJ, Banik NL. Estrogen attenuates glutamate-induced cell death by inhibiting Ca2+ influx through L-type voltage-gated Ca2+ channels. Brain Res. 2009;1276:159–70. doi:10.1016/j.brainres.2009.04.022.
   PubMed Web of Science ®Google Scholar
• Luoma JI, Kelley BG, Mermelstein PG. Progesterone inhibition of voltage-gated calcium channels is a potential neuroprotective mechanism against excitotoxicity. Steroids. 2011 March. doi:10.1016/j.steroids.2011.02.013.
   Web of Science ®Google Scholar
• Verma V, Singh N, Singh Jaggi A. Pregabalin in neuropathic pain: evidences and possible mechanisms. Curr Neuropharmacol. 2014;12(1):44–56. doi:10.2174/1570159X1201140117162802.
   PubMed Web of Science ®Google Scholar
• Raptis E, Vadalouca A, Stavropoulou E, Argyra E, Melemeni A, Siafaka I. Pregabalin vs. Opioids for the treatment of neuropathic cancer pain: A prospective, head-to-head, randomized, open-label study. Pain Pract. 2014;14(1):32–42. doi:10.1111/papr.12045.
   Web of Science ®Google Scholar
• Mishra S, Bhatnagar S, Goyal GN, Rana SPS, Upadhya SP. A comparative efficacy of amitriptyline, gabapentin, and pregabalin in neuropathic cancer pain: a prospective randomized double-blind placebo-controlled study. Am J Hosp Palliat Med. 2012;29(3):177–82. doi:10.1177/1049909111412539.
   PubMed Web of Science ®Google Scholar
• Fallon M, Hoskin PJ, Colvin LA, Fleetwood-Walker SM, Adamson D, Byrne A, Murray GD, Laird BJA. Randomized double-blind trial of pregabalin versus placebo in conjunction with palliative radiotherapy for cancer-induced bone pain. J Clin Oncol. 2016;34(6):550–56. doi:10.1200/JCO.2015.63.8221.
   Web of Science ®Google Scholar
• Gong HC, Hang J, Kohler W, Li L, Su TZ. Tissue-specific expression and gabapentin-binding properties of calcium channel α2δ subunit subtypes. J Membr Biol. 2001;184(1):35–43. doi:10.1007/s00232-001-0072-7.
   PubMed Web of Science ®Google Scholar
• Ha K-Y, Kim Y-H, Rhyu K-W, Kwon S-E. Pregabalin as a neuroprotector after spinal cord injury in rats. Eur Spine J. 2008;17(6):864–72. doi:10.1007/s00586-008-0653-6.
   PubMed Web of Science ®Google Scholar
• Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983;16(2):109–10. doi:10.1016/0304-3959(83)90201-4.
   PubMed Web of Science ®Google Scholar
• Doré-Savard L, Otis V, Belleville K, Lemire M, Archambault M, Tremblay L, Beaudoin J-F, Beaudet N, Lecomte R, Lepage M, et al. Behavioral, medical imaging and histopathological features of a new rat model of bone cancer pain. Lowenstein PR, ed. PLoS One. 2010;5(10):e13774. doi:10.1371/journal.pone.0013774.
   Web of Science ®Google Scholar
• Tétreault P, Dansereau M-A, Doré-Savard L, Beaudet N, Sarret P. Weight bearing evaluation in inflammatory, neuropathic and cancer chronic pain in freely moving rats. Physiol Behav. 2011;104(3):495–502. doi:10.1016/j.physbeh.2011.05.015.
   PubMed Web of Science ®Google Scholar
• Mosconi T, Kruger L. Fixed-diameter polyethylene cuffs applied to the rat sciatic nerve induce a painful neuropathy: ultrastructural morphometric analysis of axonal alterations. Pain. 1996;64(1):37–57. doi:10.1016/0304-3959(95)00077-1.
   PubMed Web of Science ®Google Scholar
• Zhu YF, Wu Q, Henry JL. Changes in functional properties of A-type but not C-type sensory neurons in vivo in a rat model of peripheral neuropathy. J Pain Res. 2012;5:175–92. doi:10.2147/JPR.S26367.
   PubMedGoogle Scholar
• Ungard RG, Seidlitz EP, Singh G. Inhibition of breast cancer-cell glutamate release with sulfasalazine limits cancer-induced bone pain. Pain. 2014;155(1):28–36. doi:10.1016/j.pain.2013.08.030.
   Web of Science ®Google Scholar
• Miladinovic T, Ungard RG, Linher-Melville K, Popovic S, Singh G. Functional effects of TrkA inhibition on system x C − -mediated glutamate release and cancer-induced bone pain. Mol Pain. 2018;14:174480691877646. doi:10.1177/1744806918776467.
   Web of Science ®Google Scholar
• Ungard RG, Linher-Melville K, Nashed M, Sharma M, Wen J, Singh G. xCT knockdown in human breast cancer cells delays onset of cancer-induced bone pain. Mol Pain. 2019;15:174480691882218. doi:10.1177/1744806918822185.
   Web of Science ®Google Scholar
• Pitcher GM, Ritchie J, Henry JL. Paw withdrawal threshold in the von Frey hair test is influenced by the surface on which the rat stands. J Neurosci Methods. 1999;87(2):185–93. doi:10.1016/S0165-0270(99)00004-7.
   Web of Science ®Google Scholar
• Dixon WJ. The up-and-down method for small samples. J Am Stat Assoc. 1965;60(312):967. doi:10.2307/2283398.
   Web of Science ®Google Scholar
• Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 1994;53(1):55–63. doi:10.1016/0165-0270(94)90144-9.
   PubMed Web of Science ®Google Scholar
• Wu Q, Henry JL. Delayed onset of changes in soma action potential genesis in nociceptive A-beta DRG neurons in vivo in a rat model of osteoarthritis. Mol Pain. 2009;5(1):57. doi:10.1186/1744-8069-5-57.
   Google Scholar
• Zhu YF, Ungard R, Seidlitz E, Zacal N, Huizinga J, Henry JL, Singh G. Differences in electrophysiological properties of functionally identified nociceptive sensory neurons in an animal model of cancer-induced bone pain. Mol Pain. 2016;12:174480691662877. doi:10.1177/1744806916628778.
   Web of Science ®Google Scholar
• Zhu YF, Ungard R, Zacal N, Huizinga JD, Henry JL, Singh G. Rat model of cancer-induced bone pain: changes in nonnociceptive sensory neurons in vivo. Pain Rep. 2017;2(4):e603. doi:10.1097/PR9.0000000000000603.
   PubMedGoogle Scholar
• Djouhri L, Bleazard L, Lawson SN. Association of somatic action potential shape with sensory receptive properties in guinea-pig dorsal root ganglion neurones. J Physiol. 1998;513(3):857–72. doi:10.1111/j.1469-7793.1998.857ba.x.
   Web of Science ®Google Scholar
• Lawson SN, Crepps BA, Perl ER. Relationship of substance P to afferent characteristics of dorsal root ganglion neurones in guinea-pig. J Physiol. 1997 November;177–91. doi:10.1111/j.1469-7793.1997.00177.x.
   Web of Science ®Google Scholar
• Zhu YF, Kwiecien JM, Dabrowski W, Ungard R, Zhu KL, Huizinga JD, Henry JL, Singh G. Cancer pain and neuropathic pain are associated with A β sensory neuronal plasticity in dorsal root ganglia and abnormal sprouting in lumbar spinal cord. Mol Pain. 2018;14:174480691881009. doi:10.1177/1744806918810099.
   Web of Science ®Google Scholar
• Singh M, Su C. Progesterone and neuroprotection. Horm Behav. 2013;63(2):284–90. doi:10.1016/j.yhbeh.2012.06.003.
   Web of Science ®Google Scholar
• Finnerup NB, Jensen TS. Clinical use of pregabalin in the management of central neuropathic pain. Neuropsychiatr Dis Treat. 2007;3(6):885–91. doi:10.2147/NDT.S1715.
   Google Scholar
• Zamponi GW, Lewis RJ, Todorovic SM, Arneric SP, Snutch TP. Role of voltage-gated calcium channels in ascending pain pathways. Brain Res Rev. 2009;60(1):84–89. doi:10.1016/j.brainresrev.2008.12.021.
   PubMedGoogle Scholar
• Fuchs A, Rigaud M, Sarantopoulos CD, Filip P, Hogan QH. Contribution of calcium channel subtypes to the intracellular calcium signal in sensory neurons: the effect of injury. Anesthesiology. 2007;107:117–27. doi:10.1097/01.anes.0000267511.21864.93.
   Web of Science ®Google Scholar
• Bauer CS, Nieto-Rostro M, Rahman W, Tran-Van-Minh A, Ferron L, Douglas L, Kadurin I, Sri Ranjan Y, Fernandez-Alacid L, Millar NS, et al. The increased trafficking of the calcium channel subunit α2δ-l to presynaptic terminals in neuropathic pain is inhibited by the α2δ ligand pregabalin. J Neurosci. 2009;29(13):4076–88. doi:10.1523/JNEUROSCI.0356-09.2009.
   PubMed Web of Science ®Google Scholar
• Wang H, Sun H, Della Penna K, Benz RJ, Xu J, Gerhold DL, Holder DJ, Koblan KS. Chronic neuropathic pain is accompanied by global changes in gene expression and shares pathobiology with neurodegenerative diseases. Neuroscience. 2002;114(3):529–46. doi:10.1016/S0306-4522(02)00341-X.
   PubMed Web of Science ®Google Scholar
• Newton RA, Bingham S, Case PC, Sanger GJ, Lawson SN. Dorsal root ganglion neurons show increased expression of the calcium channel α2δ-1 subunit following partial sciatic nerve injury. Brain Res Mol Brain Res. 2001;95(1–2):1–8. doi:10.1016/s0169-328x(01)00188-7.
   Google Scholar
• Han DW, Kweon TD, Lee JS, Lee Y-W. Antiallodynic effect of pregabalin in rat models of sympathetically maintained and sympathetic independent neuropathic pain. Yonsei Med J. 2007;48(1):41–47. doi:10.3349/ymj.2007.48.1.41.
   Web of Science ®Google Scholar
• Fink K, Dooley DJ, Meder WP, Suman-Chauhan N, Duffy S, Clusmann H, Göthert M. Inhibition of neuronal Ca2+ influx by gabapentin and pregabalin in the human neocortex. Neuropharmacology. 2002;42(2):229–36. doi:10.1016/S0028-3908(01)00172-1.
   PubMed Web of Science ®Google Scholar
• Carmignoto G, Pasti L, Pozzan T. On the role of voltage-dependent calcium channels in calcium signaling of astrocytes in situ. J Neurosci. 1998;18(12):4637–45. doi:10.1523/JNEUROSCI.18-12-04637.1998.
   Web of Science ®Google Scholar
• Lozano-Ondoua AN, Symons-Liguori AM, Vanderah TW. Cancer-induced bone pain: mechanisms and models. Neurosci Lett. 2013;557:52–59. doi:10.1016/j.neulet.2013.08.003.
   PubMed Web of Science ®Google Scholar
• Mantyh PW, Clohisy DR, Koltzenburg M, Hunt SP. Molecular mechanisms of cancer pain. Nat Rev Cancer. 2002;2(3):201–09. doi:10.1038/nrc747.
   PubMed Web of Science ®Google Scholar
• Sorge RE, Mapplebeck JCS, Rosen S, Beggs S, Taves S, Alexander JK, Martin LJ, Austin J-S, Sotocinal SG, Chen D, et al. Different immune cells mediate mechanical pain hypersensitivity in male and female mice. Nat Neurosci. 2015;18(8):1081–83. doi:10.1038/nn.4053.
   PubMed Web of Science ®Google Scholar
• Gattlen C, Clarke CB, Piller N, Kirschmann G, Pertin M, Decosterd I, Gosselin RD, Suter MR. Spinal cord t-cell infiltration in the rat spared nerve injury model: a time course study. Int J Mol Sci. 2016;17(3):352. doi:10.3390/ijms17030352.
   PubMed Web of Science ®Google Scholar
• Mapplebeck JCS, Dalgarno R, Tu YS, Moriarty O, Beggs S, Kwok CHT, Halievski K, Assi S, Mogil JS, Trang T, et al. Microglial P2X4R-evoked pain hypersensitivity is sexually dimorphic in rats. Pain. 2018;159(9):1752–63. doi:10.1097/j.pain.0000000000001265.
   PubMed Web of Science ®Google Scholar
• Yang Y, Li H, Li -T-T, Luo H, Gu X-Y, Lu N, Ji -R-R, Zhang Y-Q. Delayed activation of spinal microglia contributes to the maintenance of bone cancer pain in female Wistar rats via P2X7 receptor and IL-18. J Neurosci. 2015;35(20):7950–63. doi:10.1523/JNEUROSCI.5250-14.2015.
   PubMed Web of Science ®Google Scholar
• Moalem G, Xu K, Yu L. T lymphocytes play a role in neuropathic pain following peripheral nerve injury in rats. Neuroscience. 2004;129(3):767–77. doi:10.1016/j.neuroscience.2004.08.035.
   PubMed Web of Science ®Google Scholar
• Nadeau S, Filali M, Zhang J, Kerr BJ, Rivest S, Soulet D, Iwakura Y, de Rivero Vaccari JP, Keane RW, Lacroix S. Functional recovery after peripheral nerve injury is dependent on the pro-inflammatory cytokines IL-1β and TNF: implications for neuropathic pain. J Neurosci. 2011;31(35):12533–42. doi:10.1523/JNEUROSCI.2840-11.2011.
   PubMed Web of Science ®Google Scholar
• Barrette B, Hébert MA, Filali M, Lafortune K, Vallieres N, Gowing G, Julien J-P, Lacroix S. Requirement of myeloid cells for axon regeneration. J Neurosci. 2008;28(38):9363–76. doi:10.1523/JNEUROSCI.1447-08.2008.
   Web of Science ®Google Scholar