Aromatase inhibition exacerbates pain and reactive gliosis in the dorsal horn of the spinal cord of female rats caused by spinothalamic tract injury

Endocrinology (United States)

Volumn 155, Issue 11, 2014, Pages 4341-4355

  Ghorbanpoor, Samar ^a   Garcia Segura, Luis Miguel ^b   Haeri Rohani, Ali ^a   Khodagholi, Fariba ^c   Jorjani, Masoumeh ^c  

^a UNIVERSITY OF TEHRAN   (Iran)

^b INSTITUTO CAJAL   (Spain)

^c SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLIAL FIBRILLARY ACIDIC PROTEIN; LETROZOLE; MESSENGER RNA; AROMATASE INHIBITOR;

ADULT; ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL ACTIVATION; CONTROLLED STUDY; DISEASE EXACERBATION; ELECTROLYSIS; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GLIOSIS; HORMONE SYNTHESIS; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; MICROGLIA; NONHUMAN; PAIN; PAIN THRESHOLD; PHENOTYPE; PROTEIN EXPRESSION; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; SPINOTHALAMIC TRACT; SPINOTHALAMIC TRACT INJURY; ANIMAL; CHEMICALLY INDUCED; COMPLICATION; DISEASE COURSE; DRUG EFFECTS; GENETICS; HYPERALGESIA; METABOLISM; PATHOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; AROMATASE; AROMATASE INHIBITORS; DISEASE PROGRESSION; FEMALE; GLIOSIS; HYPERALGESIA; PAIN; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD DORSAL HORN; SPINAL CORD INJURIES; SPINOTHALAMIC TRACTS;

EID: 84908042396     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2014-1158     Document Type: Article

References (72)

1. Treede RD, Jensen TS, Campbell JN, Neuropathic pain: Redefinition and a grading system for clinical and research purposes. Neurology. 2008;70(18):1630-1635.
2. Sandkühler R. Models and mechanisms of hyperalgesia and allodynia. Physiol Rev. 2009;89(2):707-758.
3. Baron R, Binder A, Wasner G. Neuropathic pain: Diagnosis, pathophysiological mechanisms, and treatment. Lancet Neurol. 2010;9(8):807-819.
4. Von Hehn CA, Baron R, Woolf CJ. Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron. 2012;73(4):638-652.
5. Moore R, Derry S, Aldington D, Cole P, Wiffen P. Amitriptyline for neuropathic pain and fibromyalgia in adults. Cochrane Database Syst Rev. 2012;12(12):CD008242
6. Moore R, Wiffen P, Derry S, Toelle T, Rice A. Gabapentin for chronic neuropathic pain and fibromyalgia in adults. Cochrane Database Syst Rev. 2014;27(4):CD007938.
7. Wang G, Thompson SM. Maladaptive homeostatic plasticity in a rodent model of central pain syndrome: Thalamic hyperexcitability after spinothalamic tract lesions. J Neurosci. 2008;28(46):11959-11969.
8. Masri R, Quiton RL, Lucas JM, Murray PD, Thompson SM, Keller A. Zona incerta: A role in central pain. J Neurophysiol. 2009;102(1):181-191.
9. McMahon SB, Malcangio M. Current challenges in glia-pain biology. Neuron. 2009;64(1):46-54.
10. Cao H, Zhang YQ. Spinal glial activation contributes to pathological pain states. Neurosci Biobehav Rev. 2008;32(5):972-983.
11. Gao YJ, Ji RR. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol Ther. 2010;126(1):56-68.
12. Naseri K, Saghaei E, Abbaszadeh F, et al. Role of Microglia and Astrocyte in Central Pain Syndrome Following Electrolytic Lesion at the Spinothalamic Tract in Rats. J Mol Neurosci. 2013;49(3):470-479.
13. Arevalo MA, Santos-Galindo M, Bellini MJ, Azcoitia I, Garcia-Segura LM. Actions of estrogens on glial cells: Implications for neuroprotection. Biochim Biophys Acta. 2010;1800(10):1106-1012.
14. Amandusson A˚, Blomqvist A. Estrogenic influences in pain processing. Front Neuroendocrinol. 2013;34(4):329-349.
15. Gintzler AR, Liu NJ. Importance of sex to pain and its amelioration; relevance of spinal estrogens and its membrane receptors. Front Neuroendocrinol. 2012;33(4):412-424.
16. Saghaei E, Abbaszadeh F, Naseri K, et al. Estradiol attenuates spinal cord injury-induced pain by suppressing microglial activation in thalamic VPL nuclei of rats. Neurosci Res. 2013;75(4):316-323.
17. Balthazart J, Ball GF. Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci. 2006;29(5):241-149.
18. Fester L, Prange-Kiel J, Jarry H, Rune GM. Estrogen synthesis in the hippocampus. Cell Tissue Res. 2011;345(3):285-294.
19. Saldanha CJ, Remage-Healey L, Schlinger BA. Synaptocrine signaling: Steroid synthesis and action at the synapse. Endocr Rev. 2011;32(4):532-549.
20. Cornil CA, Seredynski AL, de Bournonville C, et al. Rapid control of reproductive behaviour by locally synthesised oestrogens: Focus on aromatase. J Neuroendocrinol. 2013;25(11):1070-1078.
21. Garcia-Segura LM, Wozniak A, Azcoitia I, Rodriguez JR, Hutchison RE, Hutchison JB. Aromatase expression by astrocytes after brain injury: Implications for local estrogen formation in brain repair. Neuroscience. 1999;89(2):567-578.
22. Peterson RS, Saldanha CJ, Schlinger BA. Rapid Upregulation of Aromatase mRNA and Protein Following Neural Injury in the Zebra Finch (Taeniopygia guttata). J Neuroendocrinol. 2001;13(4):317-323.
23. Duncan KA, Saldanha CJ. Neuroinflammation induces glial aromatase expression in the uninjured songbird brain. J Neuroinflammation. 2011;8(1):81-92.
24. Azcoitia I, Sierra A, Veiga S, Honda S, Harada N, Garcia-Segura LM. Brain aromatase is neuroprotective. J Neurobiol. 2001;47(4):318-329.
25. McCullough LD, Blizzard K, Simpson ER, Oz OK, Hurn PD. Aromatase cytochrome P450 and extragonadal estrogen play a role in ischemic neuroprotection. J Neurosci. 2003;23(25):8701-8705.
26. Garcia-Segura LM, Veiga S, Sierra A, Melcangi RC, Azcoitia I. Aromatase: A neuroprotective enzyme. Prog Neurobiol. 2003;71(1):31-41.
27. Wynne RD, Walters BJ, Bailey DJ, Saldanha CJ. Inhibition of injury-induced glial aromatase reveals a wave of secondary degeneration in the songbird brain. Glia. 2008;56(1):97-105.
28. Saldanha CJ, Duncan KA, Walters BJ. Neuroprotective actions of brain aromatase. Front Neuroendocrinol. 2009;30(2):106-118.
29. Duncan KA, Walters BJ, Saldanha CJ. Traumatized and inflamed-but resilient: Glial aromatization and the avian brain. Horm Behav. 2013;63(2):208-215.
30. Evrard HC. Estrogen synthesis in the spinal dorsal horn: A new central mechanism for the hormonal regulation of pain. Am J Physiol Regul Integr Comp Physiol. 2006;291(2):291-299.
31. Evrard HC, Balthazart J. Rapid regulation of pain by estrogens synthesized in spinal dorsal horn neurons. J Neurosci. 2004;24(33):7225-7229.
32. Liu NJ, Chakrabarti S, Schnell S, Wessendorf M, Gintzler AR. Spinal synthesis of estrogen and concomitant signaling by membrane estrogen receptors regulate spinal κ- and μ-opioid receptor heterodimerization and female-specific spinal morphine antinociception. J Neurosci. 2011;31(33):11836-11845.
33. Amandusson A, Hermanson O, Blomqvist A. Colocalization of oestrogen receptor immunoreactivity and preproenkephalin mRNA expression to neurons in the superficial laminae of the spinal and medullary dorsal horn of rats. Eur J Neurosci. 1996;8(11):2440-2445.
34. Shughrue PJ, Lane MV, Merchenthaler I. Comparative Distribution of Estrogen Receptor-alpha and -beta mRNA in the Rat Central Nervous System. J Comp Neurol. 1997;388:507-525.
35. Papka RE, Storey-Workley M, Shughrue PJ, et al. Estrogen receptor-alpha and beta- immunoreactivity and mRNA in neurons of sensory and autonomic ganglia and spinal cord. Cell Tissue Res. 2001;304(2):193-214.
36. Platania P, Laureanti F, Bellomo M, et al. Differential expression of estrogen receptors alpha and beta in the spinal cord during postnatal development: Localization in glial cells. Neuroendocrinology. 2003;77(5):334-340.
37. Obata H, Li X, Eisenach JC. Spinal adenosine receptor activation reduces hypersensitivity after surgery by a different mechanism than after nerve injury. Anesthesiology. 2004;100(5):1258-1262.
38. Beyer C, Green SJ, Barker PJ, Huskisson NS, Hutchison JB. Aromatase-immunoreactivity is localised specifically in neurones in the developing mouse hypothalamus and cortex. Brain Res. 1994;638(1-2):203-210.
39. Praporski S, Ng SM, Nguyen AD, et al. Organization of cytochrome P450 enzymes involved in sex steroid synthesis: Protein-protein interactions in lipid membranes. J Biol Chem. 2009;284(48):33224-33232.
40. Jiang W, Ghosh D. Motion and flexibility in human cytochrome p450 aromatase. PLoS One. 2012;7(2):e32565.
41. Ren K. An Improved method for assessing mechanical allodynia in the rat. Physiol Behav. 1999;67(5):711-716.
42. Howard CV, Reed MG. Unbiased stereology. Three-dimensional measurement in microscopy. Oxford: Bios; 1998.
43. Hatton WJ, von Bartheld CS. Analysis of cell death in the trochlear nucleus of the chick embryo: Calibration of the optical disector counting method reveals systematic bias. J Comp Neurol. 1999;409(2):169-186.
44. Diz-Chaves Y, Pernía O, Carrero P, Garcia-Segura LM. Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice. J Neuroinflammation. 2012;9(1):71-87.
45. Diz-Chaves Y, Astiz M, Bellini MJ, Garcia-Segura LM. Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice. Brain Behav Immun. 2013;28:196-206.
46. Tapia-Gonzalez S, Carrero P, Pernia O, Garcia-Segura LM, Diz-Chaves Y. Selective oestrogen receptor (ER) modulators reduce microglia reactivity in vivo after peripheral inflammation: Potential role of microglial ERs. J Endocrinol. 2008;198(1):219-230.
47. Blurton-Jones M, Tuszynski MH. Reactive astrocytes express estrogen receptors in the injured primate brain. J Comp Neurol. 2001;433(1):115-123.
48. García-Ovejero D, Veiga S, García-Segura LM, Doncarlos LL. Glial expression of estrogen and androgen receptors after rat brain injury. J Comp Neurol. 2002;450(3):256-271.
49. Dubal DB, Rau SW, Shughrue PJ, et al. Differential modulation of estrogen receptors (ERs) in ischemic brain injury: A role for ER alpha in estradiol-mediated protection against delayed cell death. Endocrinology. 2006;147(6):3076-3084.
50. Aldskogius H, Kozlova EN. Central neuron-glial and glial-glial interactions following axon injury. Prog Neurobiol. 1998;55(1):1-26.
51. Arvanitis DN, Wang H, Bagshaw RD, Callahan JW, Boggs JM. Membrane-associated estrogen receptor and caveolin-1 are present in central nervous system myelin and oligodendrocyte plasma membranes. J Neurosci Res. 2004;75(5):603-613.
52. Giraud SN, Caron CM, Pham-Dinh D, Kitabgi P, Nicot AB. Estradiol inhibits ongoing autoimmune neuroinflammation and NF-κB-dependent CCL2 expression in reactive astrocytes. Proc Natl Acad Sci U S A. 2010;107(18):8416-8421.
53. Lee JY, Choi SY, Oh TH, Yune TY. 17β-Estradiol inhibits apoptotic cell death of oligodendrocytes by inhibiting RhoA-JNK3 activation after spinal cord injury. Endocrinology. 2012;153(8):3815-3827.
54. Wu WF, Tan XJ, Dai Y, Krishnan V, Warner M, Gustafsson JA˚. Targeting estrogen receptor β in microglia and T cells to treat experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2013;110(9):3543-3548.
55. Amandusson A, Hallbeck M, Hallbeck AL, Hermanson O, Blomqvist A. Estrogen-induced alterations of spinal cord enkephalin gene expression. Pain. 1999;83(2):243-248.
56. Zhong YQ, Li KC, Zhang X. Potentiation of excitatory transmission in substantia gelatinosa neurons of rat spinal cord by inhibition of estrogen receptor alpha. Mol Pain. 2010;6(1):92-100.
57. Schaeffer V, Meyer L, Patte-Mensah C, Eckert A, Mensah-Nyagan AG. Sciatic nerve injury induces apoptosis of dorsal root ganglion satellite glial cells and selectively modifies neurosteroidogenesis in sensory neurons. Glia. 2010;58(2):169-180.
58. Geisler J, Haynes B, Anker G, Dowsett M, Lønning PE. Influence of letrozole and anastrozole on total body aromatization and plasma estrogen levels in postmenopausal breast cancer patients evaluated in a randomized, cross-over study. J Clin Oncol. 2002;20(3):751-757.
59. Moradi-Azani M, Ahmadiani A, Amini H. Increase in formalin-induced tonic pain by 5alpha-reductase and aromatase inhibition in female rats. Pharmacol Biochem Behav. 2011;98(1):62-66.
60. Mika J, Zychowska M, Popiolek-Barczyk K, Rojewska E, Przewlocka B. Importance of glial activation in neuropathic pain. Eur J Pharmacol. 2013;716(1-3):106-119.
61. Guptarak J, Wanchoo S, Durham-Lee J, et al. Inhibition of IL-6 signaling: A novel therapeutic approach to treating spinal cord injury pain. Pain. 2013;154(7):1115-1128.
62. Won KA, Kim MJ, Yang KY, et al. The Glial-neuronal GRK2 pathway participates in the development of trigeminal neuropathic pain in rats. J Pain. 2013. doi:10.1016/j.jpain.2013.10.013.
63. Clark AK, Old EA, Malcangio M. Neuropathic pain and cytokines: Current perspectives. J Pain Res. 2013;6:803-814.
64. Stokes JA, Cheung J, Eddinger K, Corr M, Yaksh TL. Toll-like receptor signaling adapter proteins govern spread of neuropathic pain and recovery following nerve injury in male mice. J Neuroinflammation. 2013;10:148.
65. Ji RR, Berta T, Nedergaard M. Glia and pain: Is chronic pain a gliopathy? Pain. 2013;154(Suppl 1):S10-S28.
66. Zhu X, Cao S, Zhu MD, Liu JQ, Chen JJ, Gao YJ. Contribution of chemokine CCL2/CCR2 signaling in the dorsal root ganglion and spinal cord to the maintenance of neuropathic pain in a rat model of lumbar disc herniation. J Pain. 2014;15(5):516-526.
67. Wang D, Couture R, Hong Y. Activated microglia in the spinal cord underlies diabetic neuropathic pain. Eur J Pharmacol. 2014;728:59-66.
68. Tiwari V, Guan Y, Raja SN. Modulating the delicate glial-neuronal interactions in neuropathic pain: promises and potential caveats. Neurosci Biobehav Rev. 2014;45:19-27.
69. Milligan ED, Watkins LR. Pathological and protective roles of glia in chronic pain. Nat Rev Neurosci. 2009;10(1):23-26.
70. Arevalo MA, Santos-Galindo M, Acaz-Fonseca E, Azcoitia I, Garcia-Segura LM. Gonadal hormones and the control of reactive gliosis. Horm Behav. 2013;63(2):216-221.
71. Acaz-Fonseca E, Gonzalez RS, Azcoitia I, Arevalo MA, Garcia-Segura LM. Role of astrocytes in the neuroprotective actions of 17β-estradiol and selective estrogen receptor modulators. Mol Cell Endocrinol. 2014;389(1-2):48-57.
72. Hatashita S, Sekiguchi M, Kobayashi H, Konno S, Kikuchi S. Contralateral neuropathic pain and neuropathology in dorsal root ganglion and spinal cord following hemilateral nerve injury in rats. Spine (Phila Pa 1976). 2008;33(12):1344-1351.