Effect of estrogen on morphine- and oxycodone-induced antinociception in a female femur bone cancer pain model

European Journal of Pharmacology

Volumn 773, Issue , 2016, Pages 1-12

  Ono, Hiroko ^a   Nakamura, Atsushi ^a   Kanemasa, Toshiyuki ^a   Sakaguchi, Gaku ^a   Shinohara, Shunji ^a  

^a SHIONOGI AND CO LTD   (Japan)

Author keywords

Dynorphin; Estrogen; Femur bone cancer pain; Morphine; Oxycodone

Indexed keywords

DELTA OPIATE RECEPTOR; DYNORPHIN A; DYNORPHIN A ANTIBODY; DYNORPHIN ANTIBODY; ESTRADIOL; ESTROGEN; KAPPA OPIATE RECEPTOR; MORPHINE; MU OPIATE RECEPTOR; OXYCODONE; PRODYNORPHIN; PROENKEPHALIN; PROOPIOMELANOCORTIN; UNCLASSIFIED DRUG; ANALGESIC AGENT; DYNORPHIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; BONE PAIN; CANCER PAIN; CONTROLLED STUDY; DELTA OPIATE RECEPTOR GENE; DISEASE MODEL; DRUG POTENCY; ESTROGEN ACTIVITY; FEMALE; FEMUR; FEMUR BONE CANCER PAIN; GENE EXPRESSION; GENE IDENTIFICATION; IN SITU HYBRIDIZATION; KAPPA OPIATE RECEPTOR GENE; MALE; MOUSE; MU OPIATE RECEPTOR GENE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PRODYNORPHIN GENE; PROENKEPHALIN GENE; PROOPIOMELANOCORTIN GENE; SHAM PROCEDURE; SPINAL CORD DORSAL HORN; ANIMAL; BONE TUMOR; COMPLICATION; DRUG EFFECTS; ESTRUS CYCLE; GENE EXPRESSION REGULATION; GENETICS; PAIN; PATHOPHYSIOLOGY; TUMOR CELL LINE;

ANALGESICS; ANIMALS; BONE NEOPLASMS; CELL LINE, TUMOR; DYNORPHINS; ESTROGENS; ESTROUS CYCLE; FEMALE; FEMUR; GENE EXPRESSION REGULATION; MALE; MICE; MORPHINE; OVARIECTOMY; OXYCODONE; PAIN;

EID: 84957426458     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2016.01.001     Document Type: Article

References (56)

1. A. Amandusson, O. Hermanson, and A. Blomqvist Estrogen receptor-like immunoreactivity in the medullary and spinal dorsal horn of the female rat Neurosci. Lett. 196 1995 25 28
2. R.J. Bodnar, and B. Kest Sex differences in opioid analgesia, hyperalgesia, tolerance and withdrawal: central mechanisms of action and roles of gonadal hormones Horm. Behav. 58 2010 72 81
3. H. Bradshaw, J. Miller, Q. Ling, K. Malsnee, and M.A. Ruda Sex differences and phases of the estrous cycle alter the response of spinal cord dynorphin neurons to peripheral inflammation and hyperalgesia Pain 85 2000 93 99
4. A. Buvanendran, A. Ali, T.R. Stoub, J.S. Kroin, and K.J. Tuman Brain activity associated with chronic cancer pain Pain Physician 13 2010 E337 E342
5. S. Chakrabarti, N.J. Liu, and A.R. Gintzler Formation of mu-/kappa-opioid receptor heterodimer is sex-dependent and mediates female-specific opioid analgesia Proc. Natl. Acad. Sci. USA 107 2010 20115 20119
6. A.K. Champlin, D.L. Dorr, and A.H. Gates Determining the stage of the estrous cycle in the mouse by the appearance of the vagina Biol. Reprod. 8 1973 491 494
7. C. Chavkin, I.F. James, and A. Goldstein Dynorphin is a specific endogenous ligand of the kappa opioid receptor Science 215 1982 413 415
8. Z.R. Chen, R.J. Irvine, A.A. Somogyi, and F. Bochner Mu receptor binding of some commonly used opioids and their metabolites Life Sci. 48 1991 2165 2171
9. R.I. Cone, E. Weber, J.D. Barchas, and A. Goldstein Regional distribution of dynorphin and neo-endorphin peptides in rat brain, spinal cord, and pituitary J. Neurosci. 3 1983 2146 2152
10. R.M. Craft, J.S. Mogil, and A.M. Aloisi Sex differences in pain and analgesia: the role of gonadal hormones Eur. J. Pain 8 2004 397 411
11. G. Draisci, K.C. Kajander, R. Dubner, G.J. Bennett, and M.J. Iadarola Up-regulation of opioid gene expression in spinal cord evoked by experimental nerve injuries and inflammation Brain Res. 560 1991 186 192
12. A.R. Gintzler, S.A. Schnell, D.S. Gupta, N.J. Liu, and M.W. Wessendorf Relationship of spinal dynorphin neurons to delta-opioid receptors and estrogen receptor alpha: anatomical basis for ovarian sex steroid opioid antinociception J. Pharmacol. Exp. Ther. 326 2008 725 731
13. S. González-Rodríguez, A. Hidalgo, A. Baamonde, and L. Menéndez Involvement of Gi/o proteins and GIRK channels in the potentiation of morphine-induced spinal analgesia in acutely inflamed mice Naunyn Schmiedebergs Arch. Pharmacol. 381 2010 59 71
14. F.T. Gordon, and M.R. Soliman The effects of estradiol and progesterone on pain sensitivity and brain opioid receptors in ovariectomized rats Horm. Behav. 30 1996 244 250
15. R.P. Hammer Jr., L. Bogic, and R.J. Handa Estrogenic regulation of proenkephalin mRNA expression in the ventromedial hypothalamus of the adult male rat Brain Res. Mol. Brain Res. 19 1993 129 134
16. Z. He, Y.J. He, A.L. Day, and J.W. Simpkins Proestrus levels of estradiol during transient global cerebral ischemia improves the histological outcome of the hippocampal CA1 region: perfusion-dependent and-independent mechanisms J. Neurol. Sci. 193 2002 79 87
17. P. Honore, N.M. Luger, M.A. Sabino, M.J. Schwei, S.D. Rogers, D.B. Mach, P.F. O'keefe, M.L. Ramnaraine, D.R. Clohisy, and P.W. Mantyh Osteroprotegerin blocks bone cancer-induced skeletal destruction, skeletal pain and pain-induced neurochemical reorganization of the spinal cord Nat. Med. 6 2000 521 528
18. R.R. Ji, X. Zhang, Z. Wiesenfeld-Hallin, and T. Hökfelt Expression of neuropeptide Y and neuropeptide Y (Y1) receptor mRNA in rat spinal cord and dorsal root ganglia following peripheral tissue inflammation J. Neurosci. 14 1994 6423 6434
19. Y. Ji, A.Z. Murphy, and R.J. Traub Estrogen modulation of morphine analgesia of visceral pain in female rats is supraspinally and peripherally mediated J. Pain 8 2007 494 502
20. B.A. Jordan, S. Cvejic, and L.A. Devi Kappa opioid receptor endocytosis by dynorphin peptides DNA Cell Biol. 19 2000 19 27
21. K.C. Kajander, Y. Sahara, M.J. Iadarola, and G.J. Bennett Dynorphin increases in the dorsal spinal cord in rats with a painful peripheral neuropathy Peptides 11 1990 719 728
22. K.L. Kepler, B. Kest, J.M. Kiefel, M.L. Cooper, and R.J. Bodnar Roles of gender, gonadectomy and estrous phase in the analgesic effects of intracerebroventricular morphine in rats Pharmacol. Biochem. Behav. 34 1989 119 127
23. S. Komiya, M. Zenmyo, and A. Inoue Bone tumors in the pelvis presenting growth during pregnancy Arch. Orthop. Trauma Surg. 119 1999 22 29
24. K.P. Lawson, S. Nag, A.D. Thompson, and S.S. Mokha Sex-specificity and estrogen-dependence of kappa opioid receptor-mediated antinociception and antihyperalgesia Pain 151 2010 806 815
25. K.K. Lemberg, V.K. Kontinen, A.O. Siiskonen, K.M. Viljakka, J.T. Yli-Kauhaluoma, E.R. Korpi, and E.A. Kalso Antinociception by spinal and systemic oxycodone: why does the route make a difference? In vitro and in vivo studies in rats Anesthesiology 105 2006 801 812
26. J.G. Li, F. Zhang, X.L. Jin, and L.Y. Liu-Chen Differential regulation of the human kappa opioid receptor by agonists: etorphine and levorphanol reduced dynorphin A- and U50,488H-induced internalization and phosphorylation J. Pharmacol. Exp. Ther. 305 2003 531 540
27. J. Maarrawi, R. Peyron, P. Mertens, N. Costes, M. Magnin, M. Sindou, B. Laurent, and L. Garcia-Larrea Motor cortex stimulation for pain control induces changes in the endogenous opioid system Neurology 69 2007 827 834
28. C.D. MacCalman, R. Farookhi, and O.W. Blaschuk Estradiol regulates E-cadherin mRNA levels in the surface epithelium of the mouse ovary Clin. Exp. Metastasis 12 1994 276 282
29. T.P. Malan, M.H. Ossipov, L.R. Gardell, M. Ibrahim, D. Bian, J. Lai, and F. Porreca Extraterritorial neuropathic pain correlates with multisegmental elevation of spinal dynorphin in nerve-injured rats Pain 86 2000 185 194
30. C.L. Marker, M. Stoffel, and K. Wickman Spinal G-protein-gated K+ channels formed by GIRK1 and GIRK2 subunits modulate thermal nociception and contribute to morphine analgesia J. Neurosci. 24 2004 2806 2812
31. A.C. McLean, N. Valenzuela, S. Fai, and S.A. Bennett Performing vaginal lavage, crystal violet staining, and vaginal cytological evaluation for mouse estrous cycle staging identification J. Vis. Exp. 15 2012 e4389
32. K. Minami, M. Hasegawa, H. Ito, A. Nakamura, T. Tomii, M. Matsumoto, S. Orita, S. Matsushima, T. Miyoshi, K. Masuno, M. Torii, K. Koike, S. Shimada, T. Kanemasa, T. Kihara, M. Narita, T. Suzuki, and A. Kato Morphine, oxycodone, and fentanyl exhibit different analgesic profiles in mouse pain models J. Pharmacol. Sci. 111 2009 60 72
33. H. Mizoguchi, H. Watanabe, T. Hayashi, W. Sakurada, T. Sawai, T. Fujimura, T. Sakurada, and S. Sakurada Possible involvement of dynorphin A-(1-17) release via mu1-opioid receptors in spinal antinociception by endomorphin-2 J. Pharmacol. Exp. Ther. 317 2006 362 368
34. S.R. Naik, M.R. Kelkar, and U.K. Sheth Attenuation of stereotyped behaviour by sex steroids Psychopharmacology 57 1978 211 214
35. A. Nakamura, M. Hasegawa, K. Minami, T. Kanbara, T. Tomii, A. Nishiyori, M. Narita, T. Suzuki, and A. Kato Differential activation of the μ-opioid receptor by oxycodone and morphine in pain-related brain regions in a bone cancer pain model Br. J. Pharmacol. 168 2013 375 388
36. A. Nakamura, M. Fujita, H. Ono, Y. Hongo, T. Kanbara, K. Ogawa, Y. Morioka, A. Nishiyori, M. Shibasaki, T. Mori, T. Suzuki, G. Sakaguchi, A. Kato, and M. Hasegawa G protein-gated inwardly rectifying potassium (KIR3) channels play a primary role in the antinociceptive effect of oxycodone, but not morphine, at supraspinal sites Br. J. Pharmacol. 171 2014 253 264
37. M. Narita, A. Nakamura, M. Ozaki, S. Imai, K. Miyoshi, M. Suzuki, and T. Suzuki Comparative pharmacological profiles of morphine and oxycodone under a neuropathic pain-like state in mice: evidence for less sensitivity to morphine Neuropsychopharmacology 33 2008 1097 1112
38. N. Pandit-Taskar, M. Batraki, and C.R. Divgi Radiopharmaceutical therapy for palliation of bone pain from osseous metastases J. Nucl. Med. 45 2004 1358 1365
39. M.C. Parra, T.N. Nguyen, R.W. Hurley, and D.L. Hammond Persistent inflammatory nociception increases levels of dynorphin 1-17 in the spinal cord, but not in supraspinal nuclei involved in pain modulation J. Pain 3 2002 330 336
40. K.L. Porter, S. Chanda, H.Q. Wang, K.W. Gaido, R.C. Smart, and C.L. Robinette 17 beta-estradiol is a hormonal regulator of mirex tumor promotion sensitivity in mice Toxicol. Sci. 69 2002 42 48
41. A. Rissanen, J. Puoliväli, T. van Groen, and P. Riekkinen Jr. In mice tonic estrogen replacement therapy improves non-spatial and spatial memory in a water maze task Neuroreport 10 1999 1369 1372
42. S.C. Roerig, and J.M. Fujimoto Multiplicative interaction between intrathecally and intracerebroventricularly administered mu opioid agonists but limited interactions between delta and kappa agonists for antinociception in mice J. Pharmacol. Exp. Ther. 249 1989 762 768
43. M. Sadeghi, S. Sianati, D.K. Anaraki, M. Ghasemi, M.J. Paydar, B. Sharif, S.E. Mehr, and A.R. Dehpour Study of morphine-induced dependence in gonadectomized male and female mice Pharmacol. Biochem. Behav. 91 2009 604 609
44. A. Sandner-Kiesling, and J.C. Eisenach Estrogen reduces efficacy of mu- but not kappa-opioid agonist inhibition in response to uterine cervical distension Anesthesiology 96 2002 375 379
45. W. Shen, L. Shen, G. Chen, F. Wang, C. Li, F. Lin, X. Yang, and S. Fu Ovariectomy modulation of morphine analgesia of neuropathic pain is associated with the change of K(+)-Cl(-) cotransporter 2 protein level in spinal dorsal horn. Int J. Clin. Exp. Med. 7 2014 3467 3472
46. T.H. Smith, J.R. Grider, W.L. Dewey, and H.I. Akbarali Morphine decreases enteric neuron excitability via inhibition of sodium channels PLoS One 7 2012 e45251
47. Y.R. Smith, C.S. Stohler, T.E. Nichols, J.A. Bueller, R.A. Koeppe, and J.K. Zubieta Pronociceptive and antinociceptive effects of estradiol through endogenous opioid neurotransmission in women J. Neurosci. 26 2006 5777 5785
48. Y.R. Smith, J.K. Zubieta, M. Del Carmen, R.F. Dannals, H. Ravert, H. Zacur, and J.J. Frost Brain mu opioid receptor measurements by positron emission tomography in normal cycling women: relationship to LH pulsatility and gonadal steroid hormones J. Clin. Endocrinol. Metab. 83 1998 4498 4505
49. C.W. Stevens, K.C. Kajander, G.J. Bennett, and V.S. Seybold Bilateral and differential changes in spinal mu, delta and kappa opioid binding in rats with a painful, unilateral neuropathy Pain 46 1991 315 326
50. E.C. Stoffel, C.M. Ulibarri, and R.M. Craft Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats Pain 103 2003 285 302
51. E.C. Stoffel, C.M. Ulibarri, J.E. Folk, K.C. Rice, and R.M. Craft Gonadal hormone modulation of mu, kappa, and delta opioid antinociception in male and female rats J. Pain 6 2005 261 274
52. K. Takasu, K. Ogawa, A. Nakamura, T. Kanbara, H. Ono, T. Tomii, Y. Morioka, M. Hasegawa, M. Shibasaki, T. Mori, T. Suzuki, and G. Sakaguchi Enhanced GABAergic synaptic transmission at VLPAG neurons and potent modulation by oxycodone in a bone cancer pain model Br. J. Pharmacol. 172 2015 2148 2164
53. E. Teodorov, R. Camarini, M.M. Bernardi, and L.F. Felicio Treatment with steroid hormones and morphine alters general activity, sexual behavior, and opioid gene expression in female rats Life Sci. 104 2014 47 54
54. F. Wilcoxon Individual Comparisons by Ranking Methods Biom. Bull. 1 1945 80 83
55. Y. Yanagisawa, H. Furue, T. Kawamata, D. Uta, J. Yamamoto, S. Furuse, T. Katafuchi, K. Imoto, Y. Iwamoto, and M. Yoshimura Bone cancer induces a unique central sensitization through synaptic changes in a wide area of the spinal cord Mol. Pain 6 2010 38
56. T. Yoshimura, Y. Suzuki, E. Makino, T. Suzuki, A. Kuroiwa, Y. Matsuda, T. Namikawa, and S. Ebihara Molecular analysis of avian circadian clock genes Brain Res. Mol. Brain Res. 78 2000 207 215