Estrogen effects on pain sensitivity and neuropeptide expression in rat sensory neurons

Experimental Neurology

Volumn 224, Issue 1, 2010, Pages 163-169

  Sarajari, Susan ^a   Oblinger, Monica M ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

DRG cells; Estrogen; Gonadal steroids; Neuropeptides; Peripheral neurons; Sensory neurons; Steroid receptors

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; NEUROPEPTIDE; SUBSTANCE P;

ALLODYNIA; ANIMAL CELL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; HORMONE SUBSTITUTION; HYPERALGESIA; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; NERVE INJURY; NOCICEPTION; NONHUMAN; OVARIECTOMY; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCIATIC NERVE; SENSORY NERVE CELL; SPINAL GANGLION;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CELL COUNT; DOWN-REGULATION; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; FEMALE; GANGLIA, SPINAL; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; OVARIECTOMY; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ESTROGEN; RNA, MESSENGER; SCIATIC NEUROPATHY; SENSORY RECEPTOR CELLS; SUBSTANCE P;

EID: 77953486186     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.03.006     Document Type: Article

References (48)

1. Ahmed Y., Lin D.L., et al. Effect of estrogen on urethral function and nerve regeneration following pudendal nerve crush in the female rat. J. Urol. 2006, 175:1948-1952.
2. Amara S.G., Arriza J.L., et al. Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide. Science 1985, 209:1094-1097.
3. Berkley K. Sex differences in pain. Behav. Brain Sci. 1997, 20:371-380.
4. Brown E.R., Harlan R.E., et al. Gonadal steroid regulation of substance P (SP)-encoding messenger ribonucleic acids in the rat anterior pituitary and hypothalamus. Endocrin. 1990, 126:330-340.
5. Carter M.S., Krause J.E. Structure, expression and some regulatory mechanisms of the rat preprotachykinin gene encoding substance P, neurokinin A, neuropeptide K and neuropeptide gamma. J. Neurosci. 1990, 10:2203-2214.
6. Coyle D.E., Sehlhorst C.S., et al. Intact female rats are more susceptible to the development of tactile allodynia than ovariectomized female rats following partial sciatic nerve ligation (PSNL). Neurosci. Lett. 1996, 203:37-40.
7. Coyle D.E., Sehlhorst C.S., et al. Female rats are more susceptible to the development of neuropathic pain using the partial sciatic nerve ligation (PSNL) model. Neurosci. Lett. 1995, 186:135-138.
8. Craft R. Modulation of pain by estrogens. Pain 2007, 132(Supplement 1):S3-S12.
9. Craft R., Ulibarri C., et al. Dose- and time-dependent estradiol modulation of morphine antinociception in adult female rats. Eur. J. Pain 2008, 12(4):472-479.
10. Fillingem R., Ness T. Sex-related hormonal influences on pain and analgesic responses. Neurosci. Biobehav. Rev. 2000, 24:485-501.
11. Fitzgerald M., Wall P.D., et al. Nerve growth factor counteracts the neurophysiological and neurochemical effects of chronic sciatic nerve section. Brain Res. 1985, 332:131-141.
12. Flake N., Bonebreak D., et al. Estrogen and inflammation increase the excitability of rat temporomandibular joint afferent neurons. J. Neurophysiol. 2005, 93:1585-1597.
13. Gangula P., Chauhan M., et al. Age-related changes in dorsal root ganglia, circulating and vascular calcitonin gene-related peptide (CGRP) concentrations in female rats: effect of female sex steroid hormones. Neurosci. Lett. 2009, 454:118-123.
14. Gangula P., Lanlua P., et al. Regulation of calcitonin gene-related peptide expression in dorsal root ganglia of rats by female sex steroid hormones. Biol. Reprod. 2000, 62:1033-1039.
15. Gaumond I., Arsenault P., et al. The role of sex hormones on formalin-induced nociceptive responses. Brain Res. 2002, 958:139-145.
16. Ginzler A. Endorphin-mediated increases in pain threshold during pregnancy. Science 1980, 210:193-195.
17. Gon G., Giaid A., et al. Localization of immunoreactivity for calcitonin gene-related peptide in the rat anterior pituitary during ontogeny and gonadal steroid manipulations and detection of its messenger ribonucleic acid. Endocrinol. 1990, 127:2618-2629.
18. Gupta S., Mehrotra S., et al. Potential role of female sex hormones in the pathophysiology of migraine. Pharmacol. Ther. 2007, 113(2):321-340.
19. Herbison A.E., Theodosis D.T. Immunocytochemical identification of oestrogen receptors in preoptic neurons containing calcitonin gene-related peptide in the male and female rat. Neuroendocrin. 1992, 56:761-764.
20. Lauber A.H., Mobbs C.V., et al. Estrogen receptor mRNA expression in rat hypothalamus as a function of genetic sex and estrogen dose. Endocrinol. 1991, 129:3180-3186.
21. Lee Y., Takami K., et al. Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistence with substance P. Neuroscience 1985, 15:1227-1237.
22. Liuzzi F.J., Scoville S.A., et al. Long-term estrogen replacement coordinately decreases trkA and B-PPT mRNA levels in dorsal root ganglion neurons. Exp. Neurol. 1999, 155:260-267.
23. Liuzzi F.J., Bufton S.M., et al. Effects of short-term estrogen replacement on trkA mRNA levels in axotomized dorsal root ganglion neurons. Exp. Neurol. 1999, 159:433-440.
24. Ma D., Zhao C., et al. Response of substance P-immunoreactive nerve fibres in the anterior pituitary to plasma oestrogen levels in the rat. J. Neuroendocrinol. 1997, 9:735-740.
25. Mannino C., South S., et al. Estradiol replacement in ovariectomized rats is antihyperalgesic in the formalin test. J. Pain 2007, 8:334-342.
26. Marcus D. Interrelationships of neurochemicals, estrogen and recurring headache. Pain 1995, 62:129-139.
27. Martinez-Gomez M., Cruz Y., et al. Assessing pain threshold in the rat: changes with estrus and time of day. Physiol. Behav. 1994, 55(4):651-657.
28. Micevych P.E., Matt D.W., et al. Concentrations of cholecystokinin, substance P, and bombesin in discrete regions of male and female rat brain: sex differences and estrogen effects. Exp. Neurol. 1988, 100:416-425.
29. Multon S., Pardutz A., et al. Lack of estrogen increases pain in the trigeminal formalin model: a behavioral and immunocytochemical study of transgenic ARKO mice. Pain 2005, 114(1):257-265.
30. Noguchi K., Senba E., et al. alpha-CGRP and beta-CGRP mRNAs are differentially regulated in the rat spinal cord and dorsal root ganglion. Mol. Brain Res. 1990, 7:299-304.
31. O'Halloran D.J., Jones P.M., et al. The regulation of neuropeptide expression in rat anterior pituitary following chronic manipulation of estrogen status: a comparison between substance P, neuropeptide Y, neurotensin, and vasoactive intestinal peptide. Endocrinol. 1990, 127:1463-1469.
32. Rance N.E., Young W.S.I. Hypertrophy and increased gene expression of neurons containing neurokinin-B and substance P messenger ribonucleic acids in the hypothalami of postmenopausal women. Endocrin. 1991, 128:2239-2247.
33. Rasmussen B., Breslau N. Migraine: epidemiology. The Headaches 1993, 169-173. Raven Press, New York, NY. J. Olsen, P. Tfelt-Hansen, K. Welch (Eds.).
34. Sanoja R., Cervero F. Estrogen modulation of ovariectomy-induced hyperalgesia in adult mice. Eur. J. Pain 2008, 12(5):573-581.
35. Selzer Z., Dubner R., et al. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 1990, 43:205-218.
36. Shi S.-R., Key M.E., et al. Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 1991, 39.
37. Shir Y., Selzer Z. A-fibers mediate mechanical hyperesthesia and allodynia and C-fibers mediate thermal hyperalgesia in a new model of causaliform pain disorders in rats. Neurosci. Lett. 1990, 115:62-67.
38. Spinetti A., Margutti A., et al. Hormonal replacement therapy affects calcitonin gene-related peptide and atrial natriuretic peptide secretion in postmenopausal women. Eur. J. Endocrinol. 1997, 137:664-669.
39. Taleghany N., Sarajari S., et al. Differential expression of estrogen receptor alpha and beta in rat dorsal root ganglion neurons. J. Neurosci. Res. 1999, 57(5):603-615.
40. Taniuchi M., Clark H.B., et al. Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural location, suppression by axonal contact, and binding properties. J. Neurosci. 1988, 8:664-681.
41. Toran-Allerand C.D., Miranda R.C., et al. Estrogen receptors colocalize with low-affinity nerve growth factor receptors in cholinergic neurons of the basal forebrain. PNAS 1992, 89:4668-4672.
42. Verge V.M.K., Richardson P.M., et al. Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. J. Neurosci. 1995, 15:2081-2096.
43. Wong J., Oblinger M.M. NGF rescues substance P expression but not neurofilament or tubulin gene expression in axotomized sensory neurons. J. Neurosci. 1991, 11:543-552.
44. Yan T., Liu B., et al. Estrogen amplifies pain responses to uterine cervical distension in rats by altering transient receptor potential-1 function. Anesth. Analg. 2007, 104:1246-1250.
45. Yang Y., Ozawa H., et al. Immunocytochemical analysis of sex differences in calcitonin gene-related peptide in the rat dorsal root ganglion, with special reference to estrogen and its receptor. Brain Res. 1998, 791:35-42.
46. Yuri K., Kawata M. Time-course analysis of changes in calcitonin gene-related peptide and methionine-enkephalin-immunoreactivity in the female rat preoptic area after estrogen treatment. Neuroscience 1993, 55:1067-1074.
47. Yuri K., Kawata M. Estrogen affects calcitonin gene-related peptide- and methionine-enkephalin-immunoreactive neuron in the female rat preoptic area. Neurosci. Lett. 1994, 169:5-8.
48. Yuri K., Kawata M. Estrogen receptor-immunoreactive neurons contain calcitonin gene-related peptide, methionine-enkephalin or tyrosine hydroxylase in the female rat preoptic area. Neurosci. Res. 1994, 21:135-141.