Progesterone prevents allodynia after experimental spinal cord injury

Journal of Pain

Volumn 12, Issue 1, 2011, Pages 71-83

  Coronel, María F ^a,c   Labombarda, Florencia ^a,b   Villar, Marcelo J ^c   De Nicola, Alejandro F ^a,b   González, Susana L ^a,b  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c UNIVERSIDAD AUSTRAL   (Argentina)

Author keywords

Chronic pain; kappa opioid receptors; N methyl D aspartate receptor; preprodynorphin; protein kinase C

Indexed keywords

KAPPA OPIATE RECEPTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; PREPRODYNORPHIN; PROGESTERONE; PROTEIN KINASE C GAMMA; RECEPTOR SUBTYPE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; GENE EXPRESSION; MALE; NEUROMODULATION; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PAIN THRESHOLD; RAT; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; STIMULUS RESPONSE; UPREGULATION;

ANIMALS; DISEASE MODELS, ANIMAL; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; HYPERALGESIA; MALE; NEURALGIA; PAIN MEASUREMENT; PAIN THRESHOLD; PROGESTERONE; PROGESTINS; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, OPIOID, KAPPA; SPINAL CORD INJURIES; TUBERCULIN;

EID: 78650706125     PISSN: 15265900     EISSN: 15288447     Source Type: Journal    
DOI: 10.1016/j.jpain.2010.04.013     Document Type: Article

References (97)

1. A.M. Aloisi, and M. Bonifazi Sex hormones, central nervous system and pain Horm Behav 50 2006 1 7
2. G. Alonso, V. Phan, I. Guillemain, M. Saunier, A. Legrand, M. Anoal, and T. Maurice Immunocytochemical localization of the sigma(1) receptor in the adult rat central nervous system Neuroscience 97 2000 155 170
3. C. Baastrup, and N.B. Finnerup Pharmacological management of neuropathic pain following spinal cord injury CNS Drugs 22 2008 455 475
4. M. Bajo, E.F. Crawford, M. Roberto, S.G. Madamba, and G.R. Siggins Chronic morphine treatment alters expression of N-methyl-D-aspartate receptor subunits in the extended amygdala J Neurosci Res 83 2006 532 537
5. B. Balasubramanian, W. Portillo, A. Reyna, J.Z. Chen, A.N. Moore, P.K. Dash, and S.K. Mani Nonclassical mechanisms of progesterone action in the brain: I. Protein kinase C activation in the hypothalamus of female rats Endocrinology 149 2008 5509 5517
6. A.I. Basbaum, D.M. Bautista, G. Scherrer, and D. Julius Cellular and molecular mechanisms of pain Cell 139 2009 267 284
7. E.E. Baulieu Neurosteroids, their role in brain physiology: Neurotrophycity, memory, aging J Bull Acad Natl Med 185 2001 349 372
8. L.A. Bee, and A.H. Dickenson Rostral ventromedial medulla control of spinal sensory processing in normal and pathophysiological states Neuroscience 147 2007 786 793
9. K.J. Burchiel, and F.P. Hsu Pain and spasticity after spinal cord injury: Mechanisms and treatment Spine 26 2001 146 160
10. R.M. Caudle, F.M. Perez, C. King, C.G. Yu, and R.P. Yezierski N-methyl-D-aspartate receptor subunit expression and phosphorylation following excitotoxic spinal cord injury in rats Neurosci Lett 349 2003 37 40
11. S. Chaplan, F. Bach, J. Pogrel, J. Chung, and T. Yaksh Quantitative assessment of tactile allodynia in the rat paw J Neurosci 16 1994 7711 7724
12. A. Charlet, F. Lasbennes, P. Darbon, and P. Poisbeau Fast non-genomic effects of progesterone-derived neurosteroids on nociceptive thresholds and pain symptoms Pain 139 2008 603 609
13. Y. Choi, Y.W. Yoon, H.S. Na, S.H. Kim, and J.M. Chung Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain Pain 59 1994 369 376
14. M.D. Christensen, A.W. Everhart, J.T. Pickelman, and C.E. Hulsebosch Mechanical and thermal allodynia in chronic central pain following spinal cord injury Pain 68 1996 97 107
15. M.D. Christensen, and C.E. Hulsebosch Chronic central pain after spinal cord injury J Neurotrauma 14 1997 517 537
16. M.F. Coronel, A. Hernando-Insúa, J.M. Rodriguez, F. Elías, N.A. Chasseing, A.D. Montaner, and M.J. Villar Oligonucleotide IMT504 reduces neuropathic pain after peripheral nerve injury Neurosci Lett 444 2008 69 73
17. M. Costigan, J. Scholz, and C.J. Woolf Neuropathic pain: A maladaptive response of the nervous system to damage Annu Rev Neurosci 32 2009 1 32
18. S.M. Cutler, M. Cekic, D.M. Miller, B. Wali, J.W. VanLandingham, and D.G. Stein Progesterone improves acute recovery after traumatic brain injury in the aged rat J Neurotrauma 24 2007 1475 1486
19. D. Dai, E.S. Litman, E. Schonteich, and K.K. Leslie Progesterone regulation of activating protein-1 transcriptional activity: A possible mechanism of progesterone inhibition of endometrial cancer cell growth J Steroid Biochem Mol Biol 87 2003 123 131
20. M.E. Dawson-Basoa, and A.R. Gintzler Gestational and ovarian sex steroid antinociception: Synergy between spinal kappa and delta opioid systems Brain Res 794 1998 61 67
21. B. De la Puente, X. Nadal, E. Portillo-Salido, R. Sánchez-Arroyos, S. Ovalle, G. Palacios, A. Muro, L. Romero, J.M. Entrena, J.M. Baeyens, J.A. López-García, R. Maldonado, D. Zamanillo, and J.M. Vela Sigma-1 receptors regulate activity-induced spinal sensitization and neuropathic pain after peripheral nerve injury Pain 145 2009 294 303
22. A.F. De Nicola, F. Labombarda, M.C. Gonzalez Deniselle, S.L. Gonzalez, L. Garay, M. Meyer, G. Gargiulo, R. Guennoun, and M. Schumacher Progesterone neuroprotection in traumatic CNS injury and motoneuron degeneration Front Neuroendocrinol 30 2009 173 187
23. A. Dogrul, M.H. Ossipov, and F. Porreca Differential mediation of descending pain facilitation and inhibition by spinal 5HT-3 and 5HT-7 receptors Brain Res 1280 2009 52 59
24. N.B. Finnerup, I.L. Johannesen, S.H. Sindrup, F.W. Bach, and T.S. Jensen Pain and dysesthesia in patients with spinal cord injury: A postal survey Spinal Cord 39 2001 256 262
25. C.A. Frye, and J.E. Duncan Progesterone metabolites, effective at the GABAA receptor complex, attenuate pain sensitivity in rats Brain Res 643 1994 194 203
26. X. Gao, H.K. Kim, J.M. Chung, and K. Chung Enhancement of NMDA receptor phosphorylation of the spinal dorsal horn and nucleus gracilis neurons in neuropathic rats Pain 116 2005 62 72
27. L.R. Gardell, T.W. Vanderah, S.E. Gardell, R. Wang, M.H. Ossipov, J. Lai, and F. Porreca Enhanced evoked excitatory transmitter release in experimental neuropathy requires descending facilitation J Neurosci 23 2003 8370 8379
28. L.R. Gardell, M. Ibrahim, R. Wang, Z. Wang, M.H. Ossipov, T.P. Malan, F. Porreca, and J. Lai Mouse strains that lack spinal dynorphin upregulation after peripheral nerve injury do not develop neuropathic pain Neuroscience 123 2004 43 52
29. A.R. Gintzler, and N.J. Liu The maternal spinal cord: Biochemical and physiological correlates of steroid-activated antinociceptive processes Prog Brain Res 133 2001 83 97
30. S.D. Grossman, B.B. Wolfe, R.P. Yasuda, and J.R. Wrathall Changes in NMDA receptor subunit expression in response to contusive spinal cord injury J Neurochem 75 2000 174 184
31. R. Guennoun, D. Meffre, F. Labombarda, S.L. Gonzalez, M.C. Gonzalez Deniselle, D.G. Stein, A.F. De Nicola, and M. Schumacher The membrane-associated progesterone-binding protein 25-Dx: Expression, cellular localization and up-regulation after brain and spinal cord injuries Brain Res Rev 57 2008 493 505
32. W. Guo, H. Wang, M. Watanabe, K. Shimizu, S. Zou, S.C. LaGraize, F. Wei, R. Dubner, and K. Ren Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain J Neurosci 27 2007 6006 6018
33. Y.S. Gwak, and C.E. Hulsebosch Remote astrocytic and microglial activation modulates neuronal hyperexcitability and below-level neuropathic pain after spinal injury in rat Neuroscience 161 2009 895 903
34. S.L. Haberny, and K.D. Carr Comparison of basal and D-1 dopamine receptor agonist-stimulated neuropeptide gene expression in caudate-putamen and nucleus accumbens of ad libitum fed and food-restricted rats Brain Res Mol Brain Res 141 2005 121 127
35. B.C. Hains, and S.G. Waxman Activated microglia contribute to the maintenance of chronic pain after spinal cord injury J Neurosci 26 2006 4308 4317
36. M.M. Heinricher, I. Tavares, J.L. Leith, and B.M. Lumb Descending control of nociception: Specificity, recruitment and plasticity Brain Res Rev 60 2009 214 225
37. C.E. Hulsebosch, B.C. Hains, E.D. Crown, and S.M. Carlton Mechanisms of chronic central neuropathic pain after spinal cord injury Brain Res Rev 60 2009 202 213
38. H. Jing, Y. Iwasaki, M. Nishiyama, T. Taguchi, M. Tsugita, Y. Taniguchi, M. Kambayashi, and K. Hashimoto Multisignal regulation of the rat NMDA1 receptor subunit gene-a pivotal role of glucocorticoid-dependent transcription Life Sci 82 2008 1137 1141
39. C. Kibaly, L. Meyer, C. Patte-Mensah, and A.G. Mensah-Nyagan Biochemical and functional evidence for the control of pain mechanisms by dehydroepiandrosterone endogenously synthesized in the spinal cord FASEB J 22 2008 93 104
40. H.W. Kim, D.H. Roh, S.Y. Yoon, H.S. Seo, Y.B. Kwon, H.J. Han, K.W. Kim, A.J. Beitz, and J.H. Lee Activation of the spinal sigma-1 receptor enhances NMDA-induced pain via PKC- and PKA-dependent phosphorylation of the NR1 subunit in mice Br J Pharmacol 154 2008 1125 1134
41. D. Kondo, R. Yabe, T. Kurihara, H. Saegusa, S. Zong, and T. Tanabe Progesterone receptor antagonist is effective in relieving neuropathic pain Eur J Pharmacol 541 2006 44 48
42. F. Labombarda, A. Pianos, P. Liere, B. Eychenne, S. González, A. Cambourg, A.F. De Nicola, M. Schumacher, and R. Guennoun Injury elicited increase in spinal cord neurosteroid content analyzed by gas chromatography mass spectrometry Endocrinology 147 2006 1847 1859
43. F. Labombarda, M.F. Coronel, M.J. Villar, A.F. De Nicola, and S.L. Gonzalez Neuropathic pain and temporal expression of preprodynorphin, protein kinase C and N-methyl-D-aspartate receptor subunits after spinal cord injury Neurosci Lett 447 2008 115 119
44. F. Labombarda, S.L. Gonzalez, A. Lima, P. Roig, R. Guennoun, M. Schumacher, and A.F. De Nicola Effects of progesterone on oligodendrocyte progenitors, oligodendrocyte transcription factors and myelin proteins following spinal cord injury Glia 57 2009 884 897
45. M.L. Lacroix-Fralish, V.L. Tawfik, N. Nutile-McMenemy, and J.A. DeLeo Progesterone mediates gonadal hormone differences in tactile and thermal hypersensitivity following L5 nerve root ligation in female rats Neuroscience 138 2006 601 608
46. M.L. Lacroix-Fralish, V.L. Tawfik, N. Nutile-McMenemy, and J.A. Deleo Neuregulin 1 is a pronociceptive cytokine that is regulated by progesterone in the spinal cord: Implications for sex specific pain modulation Eur J Pain 12 2008 94 103
47. J. Lai, M.H. Ossipov, T.W. Vanderah, T.P. Malan, and F. Porreca Neuropathic pain: The paradox of dynorphin Mol Interv 1 2001 160 167
48. J.Y. Lan, V.A. Skeberdis, T. Jover, S.Y. Grooms, Y. Lin, R.C. Araneda, X. Zheng, M.V.L. Bennet, and R.S. Zukin Protein kinase C modulates NMDA receptor traffiking and gating Nat Neurosci 4 2001 382 390
49. A. Latremoliere, and C.J. Woolf Central sensitization: A generator of pain hypersensitivity by central neural plasticity J Pain 10 2009 895 926
50. T.M. Laughlin, T.W. Vanderah, J. Lashbrook, M.L. Nichols, M. Ossipov, F. Porreca, and G.L. Wilcox Spinally administered dynorphin A produces long-lasting allodynia: Involvement of NMDA but not opioid receptors Pain 72 1997 253 260
51. E. Leonelli, R. Bianchi, G. Cavaletti, D. Caruso, D. Crippa, L.M. García-Segura, G. Lauria, I. Roglio, and R.C. Melcangi Progesterone and its derivatives are neuroprotective agents in experimental diabetic neuropathy: A multimodal analysis Neurscience 144 2007 1293 1304
52. G. Lim, S. Wang, Q. Zeng, B. Sung, L. Yang, and J. Mao Expression of spinal NMDA receptor and PKCgamma after chronic morphine is regulated by spinal glucocorticoid receptor J Neurosci 25 2005 11145 11154 (Pubitemid 43089559)
53. A. Liu, P.W. Hoffman, W. Lu, and G. Bai NF-kappaB site interacts with Sp factors and up-regulates the NR1 promoter during neuronal differentiation J Biol Chem 279 2004 17449 17458
54. N.J. Liu, and A.R. Gintzler Prolonged ovarian sex steroid treatment of male rats produces antinociception: Identification of sex-based divergent analgesic mechanisms Pain 85 2000 273 281
55. N.J. Liu, H. von Gizycki, and A.R. Gintzler Sexually dimorphic recruitment of spinal opioid analgesic pathways by the spinal application of morphine J Pharmacol Exp Ther 322 2007 654 660
56. T) method Methods 25 2001 402 408
57. T.A. Lovick, and A.J. Devall Progesterone withdrawal-evoked plasticity of neural function in the female periaqueductal grey matter Neural Plast 2008 Dec 2 [Epub ahead of print]
58. W.J. Martin, A.B. Malmberg, and A.I. Basbaum PKCgamma contributes to a subset of the NMDA-dependent spinal circuits that underlie injury-induced persistent pain J Neurosci 21 2001 5321 5327
59. T. Maurice, C. Grégoire, and J. Espallergues Neuro(active)steroids actions at the neuromodulatory sigma1 (sigma1) receptor: Biochemical and physiological evidences, consequences in neuroprotection Pharmacol Biochem Behav 84 2006 581 597
60. C.J. McBain, and M.L. Mayer N-methyl-D-aspartic acid receptor structure and function Physiol Rev 74 1994 723 760
61. A.G. Mensah-Nyagan, C. Kibaly, V. Schaeffer, C. Venard, L. Meyer, and C. Patte-Mensah Endogenous steroid production in the spinal cord and potential involvement in neuropathic pain modulation J Steroid Biochem Mol Biol 109 2008 286 293
62. A.G. Mensah-Nyagan, L. Meyer, V. Schaeffer, C. Kibaly, and C. Patte-Mensah Evidence for a key role of steroids in the modulation of pain Psychoneuroendocrinology 34 Suppl 1 2009 S169 S177
63. L.S. Miraucourt, R. Dallel, and D.L. Voisin Glycine inhibitory dysfunction turns touch into pain through PKCgamma interneurons PLoS One 2 2007 1116
64. C. Molander, and G. Grant Spinal Cord Cytoarchitecture The Rat Nervous System 2nd ed. 1995 Academic Press San Diego, CA 39 45
65. F.P. Monnet, and T. Maurice The sigma1 protein as a target for the non-genomic effects of neuro(active)steroids: Molecular, physiological, and behavioral aspects J Pharmacol Sci 100 2006 93 118
66. G.G. Nagy, M. Watanabe, M. Fukaya, and A.J. Todd Synaptic distribution of the NR1, NR2A and NR2B subunits of the N-methyl-d-aspartate receptor in the rat lumbar spinal cord revealed with an antigen-unmasking technique Eur J Neurosci 20 2004 3301 3312
67. S. Neumann, J.M. Braz, K. Skinner, I.J. Llewellyn-Smith, and A.I. Basbaum Innocuous, not noxious, input activates PKCgamma interneurons of the spinal dorsal horn via myelinated afferent fibers J Neurosci 28 2008 7936 7944
68. S. Pathirathna, B.C. Brimelow, M.M. Jagodic, K. Krishnan, X. Jiang, C.F. Zorumski, S. Mennerick, D.F. Covey, S.M. Todorovic, and V. Jevtovic-Todorovic New evidence that both T-type calcium channels and GABAA channels are responsible for the potent peripheral analgesic effects of 5alpha-reduced neuroactive steroids Pain 114 2005 429 443
69. C. Patte-Mensah, S. Li, and A.G. Mensah-Nyagan Impact of neuropathic pain on the gene expression and activity of cytochrome P450side-chain-cleavage in sensory neural networks Cell Mol Life Sci 61 2004 2274 2284
70. C. Patte-Mensah, C. Kibaly, and A.G. Mensah-Nyagan Substance P inhibits progesterone conversion to neuroactive metabolites in spinal sensory circuit: A potential component of nociception PNAS 102 2005 9044 9049
71. A. Peinnequin, C. Mouret, O. Birot, A. Alonso, J. Mathieu, D. Clarenon, D. Agay, Y. Chancerelle, and E. Multon Rat pro-inflammatory cytokine and cytokine related mRNA quantification by real-time polymerase chain reaction using SYBR green BMC Immunol 5 2004 3
72. H.Y. Peng, G.D. Chen, S.D. Lee, C.Y. Lai, C.H. Chiu, C.L. Cheng, Y.S. Chang, M.C. Hsieh, K.C. Tung, and T.B. Lin Neuroactive steroids inhibit spinal reflex potentiation by selectively enhancing specific spinal GABA(A) receptor subtypes Pain 143 2009 12 20
73. E.H. Pettus, D.W. Wright, D.G. Stein, and S.W. Hoffman Progesterone treatment inhibits the inflammatory agents that accompany traumatic brain injury Brain Res 1049 2005 112 119
74. N. Pluchino, M. Luisi, E. Lenzi, M. Centofanti, S. Begliuomini, L. Freschi, F. Ninni, and A.R. Genazzani Progesterone and progestins: Effects on brain, allopregnanolone and beta-endorphin J Steroid Biochem Mol Biol 102 2006 205 213
75. P. Poisbeau, C. Patte-Mensah, A.F. Keller, M. Barrot, J.D. Breton, O.E. Luis-Delgado, M.J. Freund-Mercier, A.G. Mensah-Nyagan, and R. Schlichter Inflammatory pain upregulates spinal inhibition via endogenous neurosterois production J Neurosci 25 2005 11768 11776
76. F. Porreca, M.H. Ossipov, and G.F. Gebhart Chronic pain and medullary descending facilitation Trends Neurosci 25 2002 319 325
77. M. Qiang, and M.K. Ticku Role of AP-1 in ethanol-induced N-methyl-D-aspartate receptor 2B subunit gene up-regulation in mouse cortical neurons J Neurochem 95 2005 1332 1341
78. K. Ren, R. Dubne, A. Murphy, and G.E. Hoffman Progesterone attenuates persistent inflammatory hyperalgesia in females rats: Involvement of spinal NMDA receptor mechanism Brain Res 865 2000 272 277
79. K. Ren, and R. Dubner Descending modulation in persistent pain: An update Pain 100 2002 1 6
80. J. Roberts, M.H. Ossipov, and F. Porreca Glial activation in the rostroventromedial medulla promotes descending facilitation to mediate inflammatory hypersensitivity Eur J Neurosci 30 2009 229 241
81. J.M. Rodriguez Parkitna, W. Bilecki, P. Mierzejewski, R. Stefanski, A. Ligeza, A. Bargiela, B. Ziolkowska, W. Kostowski, and R. Przewlocki Effects of morphine on gene expression in the rat amygdala J Neurochem 91 2004 38 48
82. I. Roglio, R. Bianchi, S. Gotti, S. Scurati, S. Giatti, M. Pesaresi, D. Caruso, G.C. Panzica, and R.C. Melcangi Neuroprotective effects of dihydroprogesterone and progesterone in an experimental model of nerve crush injury Neuroscience 155 2008 673 685
83. D.H. Roh, H.W. Kim, S.Y. Yoon, H.S. Seo, Y.B. Kwon, H.J. Han, A.J. Beitz, and J.H. Lee Depletion of capsaicin-sensitive afferents prevents lamina-dependent increases in spinal N-methyl-D-aspartate receptor subunit 1 expression and phosphorylation associated with thermal hyperalgesia in neuropathic rats Eur J Pain 12 2008 552 563
84. A.M. Rometo, and N.E. Rance Changes in prodynorphin gene expression and neuronal morphology in the hypothalamus of postmenopausal women J Neuroendocrinol 20 2008 1376 1381
85. M. Schumacher, R. Guennoun, A. Ghoumari, C. Massaad, F. Robert, M. El-Etr, Y. Akwa, K. Rajkowski, and E.E. Baulieu Novel perspectives for progesterone in hormone replacement therapy, with special reference to the nervous system Endocr Rev 28 2007 387 439
86. M. Schumacher, R. Sitruk-Ware, and A.F. De Nicola Progesterone and progestins: Neuroprotection and myelin repair Curr Opin Pharmacol 8 2008 740 746
87. A.J. Thomas, R.P. Nockels, H.Q. Pan, C.I. Shaffrey, and M. Chopp Progesterone is neuroprotective after experimental acute spinal cord trauma in rats Spine 24 1999 2134 2138
88. M. Tomiyama, K. Furusawa, M. Kamijo, T. Kimura, M. Matsunaga, and M. Baba Upregulation of mRNAs coding for AMPA and NMDA receptor subunits and metabotropic glutamate receptors in the dorsal horn of the spinal cord in a rat model of diabetes mellitus Brain Res Mol Brain Res 136 2005 275 281
89. C. Ultenius, B. Linderoth, B.A. Meyerson, and J. Wallin Spinal NMDA receptor phosphorylation correlates with the presence of neuropathic signs following peripheral nerve injury in the rat Neurosci Lett 399 2006 85 90
90. I.D. Vats, K.S. Dolt, K. Kumar, J. Karar, M. Nath, A. Mohan, M.A. Pasha, and S. Pasha YFa, a chimeric opioid peptide, induces kappa-specific antinociception with no tolerance development during 6 days of chronic treatment J Neurosci Res 86 2008 1599 1607
91. Z. Wang, L.R. Gardell, M.H. Ossipov, T.W. Vanderah, M.B. Brennan, U. Hochgeschwender, V.J. Hruby, T.P. Malan, J. Lai, and F. Porreca Pronociceptive actions of dynorphin maintain chronic neuropathic pain J Neurosci 21 2001 1779 1786
92. F. Wei, W. Guo, S. Zou, K. Ren, and R. Dubner Supraspinal glial-neuronal interactions contribute to descending pain facilitation J Neurosci 28 2008 10482 10495
93. A.R. Weyerbacher, Q. Xu, C. Tamasdan, S.J. Shin, and C.E. Inturrisi N-Methyl-d-aspartate receptor (NMDAR) independent maintenance of inflammatory pain Pain 148 2 2010 237 246
94. A.S. Woods, R. Kaminski, M. Oz, Y. Wang, K. Hauser, R. Goody, H.Y. Wang, S.N. Jackson, P. Zeitz, K.P. Zeitz, D. Zolkowska, R. Schepers, M. Nold, J. Danielson, A. Gräslund, V. Vukojevic, G. Bakalkin, A. Basbaum, and T. Shippenberg Decoy peptides that bind dynorphin noncovalently prevent NMDA receptor-mediated neurotoxicity J Proteome Res 5 2006 1017 1023
95. D.W. Wright, A.L. Kellermann, V.S. Hertzberg, P.L. Clark, M. Frankel, F.C. Goldstein, J.P. Salomone, L.L. Dent, O.A. Harris, D.S. Ander, D.W. Lowery, M.M. Patel, D.D. Denson, A.B. Gordon, M.M. Wald, S. Gupta, S.W. Hoffman, and D.G. Stein ProTECT: A randomized clinical trial of progesterone for acute traumatic brain injury Ann Emerg Med 49 2007 391 402
96. G. Xiao, J. Wei, W. Yan, W. Wang, and Z. Lu Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: A randomized controlled trial Crit Care 12 2 2008 R61
97. R.P. Yezierski Spinal cord injury pain: Spinal and supraspinal mechanisms J Rehabil Res Dev 46 2009 95 107