Vitamin D receptor and enzyme expression in dorsal root ganglia of adult female rats: Modulation by ovarian hormones

Journal of Chemical Neuroanatomy

Volumn 41, Issue 1, 2011, Pages 1-12

  Tague, Sarah E ^a   Smith, Peter G ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

1,25 Dihydroxyvitamin D3; CYP24; CYP27B1; Pain; Reproductive hormones; Sensory

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CALCITRIOL; CYTOCHROME P450; CYTOCHROME P450 24; CYTOCHROME P450 27B1; OVARY HORMONE; PERIPHERIN; SEX HORMONE; UNCLASSIFIED DRUG; VITAMIN D RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CELL POPULATION; CLIMACTERIUM; CONTROLLED STUDY; DISEASE ASSOCIATION; ESTRUS; FEMALE; HORMONAL REGULATION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; NEUROMODULATION; NONHUMAN; OVARIECTOMY; OVARY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SENSORY NERVE CELL; SPINAL GANGLION; WESTERN BLOTTING;

25-HYDROXYVITAMIN D3 1-ALPHA-HYDROXYLASE; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CALCITRIOL; CELL NUCLEUS; ESTROGENS; FEMALE; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; NERVE FIBERS, UNMYELINATED; NOCICEPTORS; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CALCITRIOL; STEROID HYDROXYLASES;

EID: 78650200728     PISSN: 08910618     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2010.10.001     Document Type: Article

References (80)

1. Ambalavanar R., Morris R. An ultrastructural study of the binding of an alpha-d-galactose specific lectin from Griffonia simplicifolia to trigeminal ganglion neurons and the trigeminal nucleus caudalis in the rat. Neuroscience 1993, 52:699-709.
2. Andersson H.I., Ejlertsson G., Leden I., Rosenberg C. Chronic pain in a geographically defined general population: studies of differences in age, gender, social class, and pain localization. Clin. J. Pain 1993, 9:174-182.
3. Baas D., Prufer K., Ittel M.E., Kuchler-Bopp S., Labourdette G., Sarlieve L.L., Brachet P. Rat oligodendrocytes express the vitamin D(3) receptor and respond to 1,25-dihydroxyvitamin D(3). Glia 2000, 31:59-68.
4. Becker J.B., Arnold A.P., Berkley K.J., Blaustein J.D., Eckel L.A., Hampson E., Herman J.P., Marts S., Sadee W., Steiner M., Taylor J., Young E. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 2005, 146:1650-1673.
5. Bennett D.L., Michael G.J., Ramachandran N., Munson J.B., Averill S., Yan Q., McMahon S.B., Priestley J.V. A distinct subgroup of small DRG cells express GDNF receptor components and GDNF is protective for these neurons after nerve injury. J. Neurosci. 1998, 18:3059-3072.
6. Benson J., Wilson A., Stocks N., Moulding N. Muscle pain as an indicator of vitamin D deficiency in an urban Australian Aboriginal population. Med. J. Aust. 2006, 185:76-77.
7. Bergman S., Herrstrom P., Hogstrom K., Petersson I.F., Svensson B., Jacobsson L.T. Chronic musculoskeletal pain, prevalence rates, and sociodemographic associations in a Swedish population study. J. Rheumatol. 2001, 28:1369-1377.
8. Berkley K.J., Robbins A., Sato Y. Functional differences between afferent fibers in the hypogastric and pelvic nerves innervating female reproductive organs in the rat. J. Neurophysiol. 1993, 69:533-544.
9. Birklein F., Schmelz M. Neuropeptides, neurogenic inflammation and complex regional pain syndrome (CRPS). Neurosci. Lett. 2008, 437:199-202.
10. Bischoff-Ferrari H.A., Dawson-Hughes B., Willett W.C., Staehelin H.B., Bazemore M.G., Zee R.Y., Wong J.B. Effect of vitamin D on falls: a meta-analysis. JAMA 2004, 291:1999-2006.
11. Casellini C.M., Vinik A.I. Clinical manifestations and current treatment options for diabetic neuropathies. Endocr. Pract. 2007, 13:550-566.
12. Cekic M., Sayeed I., Stein D.G. Combination treatment with progesterone and vitamin D hormone may be more effective than monotherapy for nervous system injury and disease. Front. Neuroendocrinol. 2009, 30:158-172.
13. Chan J.R., Rodriguez-Waitkus P.M., Ng B.K., Liang P., Glaser M. Progesterone synthesized by Schwann cells during myelin formation regulates neuronal gene expression. Mol. Biol. Cell 2000, 11:2283-2295.
14. Cornet A., Baudet C., Neveu I., Baron-Van Evercooren A., Brachet P., Naveilhan P. 1,25-Dihydroxyvitamin D3 regulates the expression of VDR and NGF gene in Schwann cells in vitro. J. Neurosci. Res. 1998, 53:742-746.
15. Croft P., Rigby A.S., Boswell R., Schollum J., Silman A. The prevalence of chronic widespread pain in the general population. J. Rheumatol. 1993, 20:710-713.
16. de Torrente de la Jara G., Pecoud A., Favrat B. Female asylum seekers with musculoskeletal pain: the importance of diagnosis and treatment of hypovitaminosis D. BMC Fam. Pract. 2006, 7:4.
17. Diesel B., Radermacher J., Bureik M., Bernhardt R., Seifert M., Reichrath J., Fischer U., Meese E. Vitamin D(3) metabolism in human glioblastoma multiforme: functionality of CYP27B1 splice variants, metabolism of calcidiol, and effect of calcitriol. Clin. Cancer Res. 2005, 11:5370-5380.
18. Dugan S.A., Powell L.H., Kravitz H.M., Everson Rose S.A., Karavolos K., Luborsky J. Musculoskeletal pain and menopausal status. Clin. J. Pain 2006, 22:325-331.
19. Eyles D.W., Smith S., Kinobe R., Hewison M., McGrath J.J. Distribution of the vitamin D receptor and 1 alpha-hydroxylase in human brain. J. Chem. Neuroanat. 2005, 29:21-30.
20. Faulkner K.A., Cauley J.A., Zmuda J.M., Landsittel D.P., Newman A.B., Studenski S.A., Redfern M.S., Ensrud K.E., Fink H.A., Lane N.E., Nevitt M.C. Higher 1,25-dihydroxyvitamin D3 concentrations associated with lower fall rates in older community-dwelling women. Osteoporos. Int. 2006, 17:1318-1328.
21. Felson D.T., Cummings S.R. Aromatase inhibitors and the syndrome of arthralgias with estrogen deprivation. Arthritis Rheum. 2005, 52:2594-2598.
22. Freeman M.E. The neuroendocrine control of the ovarian cycle of the rat. The Physiology of Reproduction 1994, 613-658. Raven Press, New York. 2nd ed. E.J.D.N. Knobil (Ed.).
23. Friedman A.J., Juneau-Norcross M., Rein M.S. Adverse effects of leuprolide acetate depot treatment. Fertil. Steril. 1993, 59:448-450.
24. Gangula P.R., Lanlua P., Wimalawansa S., Supowit S., DiPette D., Yallampalli C. Regulation of calcitonin gene-related peptide expression in dorsal root ganglia of rats by female sex steroid hormones. Biol. Reprod. 2000, 62:1033-1039.
25. Garreau J.R., Delamelena T., Walts D., Karamlou K., Johnson N. Side effects of aromatase inhibitors versus tamoxifen: the patients' perspective. Am. J. Surg. 2006, 192:496-498.
26. Gilad L.A., Bresler T., Gnainsky J., Smirnoff P., Schwartz B. Regulation of vitamin D receptor expression via estrogen-induced activation of the ERK 1/2 signaling pathway in colon and breast cancer cells. J. Endocrinol. 2005, 185:577-592.
27. Glaser S.D., Veenstra T.D., Jirikowski G.F., Prufer K. Distribution of 1,25-dihydroxyvitamin D3 receptor immunoreactivity in the rat olfactory system. Cell. Mol. Neurobiol. 1999, 19:613-624.
28. Glerup H., Eriksen E.F. Acroparaesthesia - a typical finding in vitamin D deficiency. Rheumatology (Oxford) 1999, 38:482.
29. Glerup H., Mikkelsen K., Poulsen L., Hass E., Overbeck S., Andersen H., Charles P., Eriksen E.F. Hypovitaminosis D myopathy without biochemical signs of osteomalacic bone involvement. Calcif. Tissue Int. 2000, 66:419-424.
30. Gloth F.M., Lindsay J.M., Zelesnick L.B., Greenough W.B. Can vitamin D deficiency produce an unusual pain syndrome?. Arch. Intern. Med. 1991, 151:1662-1664.
31. Goldstein M.E., House S.B., Gainer H. NF-L and peripherin immunoreactivities define distinct classes of rat sensory ganglion cells. J. Neurosci. Res. 1991, 30:92-104.
32. Gonzalez Pardo V., Boland R., de Boland A.R. Vitamin D receptor levels and binding are reduced in aged rat intestinal subcellular fractions. Biogerontology 2008, 9:109-118.
33. Greendale G.A., Reboussin B.A., Hogan P., Barnabei V.M., Shumaker S., Johnson S., Barrett-Connor E. Symptom relief and side effects of postmenopausal hormones: results from the Postmenopausal Estrogen/Progestin Interventions Trial. Obstet. Gynecol. 1998, 92:982-988.
34. Holick M.F., Chen T.C. Vitamin D deficiency: a worldwide problem with health consequences. Am. J. Clin. Nutr. 2008, 87:1080S-1086S.
35. Huhtakangas J.A., Olivera C.J., Bishop J.E., Zanello L.P., Norman A.W. The vitamin D receptor is present in caveolae-enriched plasma membranes and binds 1 alpha,25(OH)2-vitamin D3 in vivo and in vitro. Mol. Endocrinol. 2004, 18:2660-2671.
36. Johnson J.A., Grande J.P., Windebank A.J., Kumar R. 1,25-Dihydroxyvitamin D(3) receptors in developing dorsal root ganglia of fetal rats. Brain Res. Dev. Brain Res. 1996, 92:120-124.
37. Jones G. Expanding role for vitamin D in chronic kidney disease: importance of blood 25-OH-D levels and extra-renal 1alpha-hydroxylase in the classical and nonclassical actions of 1alpha,25-dihydroxyvitamin D(3). Semin. Dial. 2007, 20:316-324.
38. Khan Q.J., Reddy P.S., Kimler B.F., Sharma P., Baxa S.E., O'Dea A.P., Klemp J.R., Fabian C.J. Effect of vitamin D supplementation on serum 25-hydroxy vitamin D levels, joint pain, and fatigue in women starting adjuvant letrozole treatment for breast cancer. Breast Cancer Res. Treat. 2009.
39. Lawson S.N. Morphological and biochemical cell types of sensory neurons. Sensory Neurons: Diversity, Development, and Plasticity 1992, 27-59. Oxford Press, New York. S.A. Scott (Ed.).
40. Lechner D., Bajna E., Adlercreutz H., Cross H.S. Genistein and 17beta-estradiol, but not equol, regulate vitamin D synthesis in human colon and breast cancer cells. Anticancer Res. 2006, 26:2597-2603.
41. Levenson C.W., Figueiroa S.M. Gestational vitamin D deficiency: long-term effects on the brain. Nutr. Rev. 2008, 66:726-729.
42. Losel R.M., Falkenstein E., Feuring M., Schultz A., Tillmann H.C., Rossol-Haseroth K., Wehling M. Nongenomic steroid action: controversies, questions, and answers. Physiol. Rev. 2003, 83:965-1016.
43. Macfarlane G.J., Palmer B., Roy D., Afzal C., Silman A.J., O'Neill T. An excess of widespread pain among South Asians: are low levels of vitamin D implicated?. Ann. Rheum. Dis. 2005, 64:1217-1219.
44. Masood H., Narang A.P., Bhat I.A., Shah G.N. Persistent limb pain and raised serum alkaline phosphatase the earliest markers of subclinical hypovitaminosis D in Kashmir. Indian J. Physiol. Pharmacol. 1989, 33:259-261.
45. Mastaglia F.L., Hilton-Jones D. Myopathies 2007, Elsevier, Edinburgh, New York.
46. Mizwicki M.T., Norman A.W. The vitamin D sterol-vitamin D receptor ensemble model offers unique insights into both genomic and rapid-response signaling. Sci. Signal 2009, 2:re4.
47. Morales L., Pans S., Paridaens R., Westhovens R., Timmerman D., Verhaeghe J., Wildiers H., Leunen K., Amant F., Berteloot P., Smeets A., Van Limbergen E., Weltens C., Van den Bogaert W., De Smet L., Vergote I., Christiaens M.R., Neven P. Debilitating musculoskeletal pain and stiffness with letrozole and exemestane: associated tenosynovial changes on magnetic resonance imaging. Breast Cancer Res. Treat. 2006.
48. Mouridsen H.T. Incidence and management of side effects associated with aromatase inhibitors in the adjuvant treatment of breast cancer in postmenopausal women. Curr. Med. Res. Opin. 2006, 22:1609-1621.
49. Mowa C.N., Usip S., Collins J., Storey-Workley M., Hargreaves K.M., Papka R.E. The effects of pregnancy and estrogen on the expression of calcitonin gene-related peptide (CGRP) in the uterine cervix, dorsal root ganglia and spinal cord. Peptides 2003, 24:1163-1174.
50. Muller K.A., Ryals J.M., Feldman E.L., Wright D.E. Abnormal muscle spindle innervation and large-fiber neuropathy in diabetic mice. Diabetes 2008, 57:1693-1701.
51. Myhr K.M. Vitamin D treatment in multiple sclerosis. J. Neurol. Sci. 2009, 286:104-108.
52. Nangia A.K., Butcher J.L., Konety B.R., Vietmeier B.N., Getzenberg R.H. Association of vitamin D receptors with the nuclear matrix of human and rat genitourinary tissues. J. Steroid Biochem. Mol. Biol. 1998, 66:241-246.
53. Nardone A., Galante M., Pareyson D., Schieppati M. Balance control in sensory neuron disease. Clin. Neurophysiol. 2007, 118:538-550.
54. Naveilhan P., Neveu I., Baudet C., Ohyama K.Y., Brachet P., Wion D. Expression of 25(OH) vitamin D3 24-hydroxylase gene in glial cells. Neuroreport 1993, 5:255-257.
55. Neveu I., Naveilhan P., Jehan F., Baudet C., Wion D., De Luca H.F., Brachet P. 1,25-Dihydroxyvitamin D3 regulates the synthesis of nerve growth factor in primary cultures of glial cells. Brain Res. Mol. Brain Res. 1994, 24:70-76.
56. Newmark H.L., Newmark J. Vitamin D and Parkinson's disease - a hypothesis. Mov. Disord. 2007, 22:461-468.
57. Omdahl J.L., Bobrovnikova E.V., Annalora A., Chen P., Serda R. Expression, structure-function, and molecular modeling of vitamin D P450s. J. Cell. Biochem. 2003, 88:356-362.
58. Perez-Fernandez R., Alonso M., Segura C., Munoz I., Garcia-Caballero T., Diguez C. Vitamin D receptor gene expression in human pituitary gland. Life Sci. 1997, 60:35-42.
59. Plotnikoff G.A., Quigley J.M. Prevalence of severe hypovitaminosis D in patients with persistent, nonspecific musculoskeletal pain. Mayo Clin. Proc. 2003, 78:1463-1470.
60. Prufer K., Racz A., Lin G.C., Barsony J. Dimerization with retinoid X receptors promotes nuclear localization and subnuclear targeting of vitamin D receptors. J. Biol. Chem. 2000, 275:41114-41123.
61. Prufer K., Veenstra T.D., Jirikowski G.F., Kumar R. Distribution of 1,25-dihydroxyvitamin D3 receptor immunoreactivity in the rat brain and spinal cord. J. Chem. Neuroanat. 1999, 16:135-145.
62. Racz A., Barsony J. Hormone-dependent translocation of vitamin D receptors is linked to transactivation. J. Biol. Chem. 1999, 274:19352-19360.
63. Ruscheweyh R., Forsthuber L., Schoffnegger D., Sandkuhler J. Modification of classical neurochemical markers in identified primary afferent neurons with Abeta-Adelta-, and C-fibers after chronic constriction injury in mice. J. Comp. Neurol. 2007, 502:325-336.
64. Sakaki T., Kagawa N., Yamamoto K., Inouye K. Metabolism of vitamin D3 by cytochromes P450. Front. Biosci. 2005, 10:119-134.
65. Shaffer P.L., Gewirth D.T. Vitamin D receptor-DNA interactions. Vitam. Horm. 2004, 68:257-273.
66. Sohrabji F., Miranda R.C., Toran-Allerand C.D. Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J. Neurosci. 1994, 14:459-471.
67. Steinman J.L., Carlton S.M., Willis W.D. The segmental distribution of afferent fibers from the vaginal cervix and hypogastric nerve in rats. Brain Res. 1992, 575:25-31.
68. Takahashi Y., Chiba T., Kurokawa M., Aoki Y. Dermatomes and the central organization of dermatomes and body surface regions in the spinal cord dorsal horn in rats. J. Comp. Neurol. 2003, 462:29-41.
69. Tanaka K., Matsugami T., Chiba T. The origin of sensory innervation of the peritoneum in the rat. Anat. Embryol. 2002, 205:307-313.
70. Tanaka Y., Castillo L., Wineland M.J., DeLuca H.F. Synergistic effect of progesterone, testosterone, and estradiol in the stimulation of chick renal 25-hydroxyvitamin D3-1alpha-hydroxylase. Endocrinology 1978, 103:2035-2039.
71. Tishkoff D.X., Nibbelink K.A., Holmberg K.H., Dandu L., Simpson R.U. Functional vitamin D receptor (VDR) in the t-tubules of cardiac myocytes: VDR knockout cardiomyocyte contractility. Endocrinology 2008, 149:558-564.
72. Tseng K.W., Chau Y.P., Yang M.F., Lu K.S., Chien C.L. Abnormal cellular translocation of alpha-internexin in spinal motor neurons of Dystonia musculorum mice. J. Comp. Neurol. 2008, 507:1053-1064.
73. Veenstra T.D., Prufer K., Koenigsberger C., Brimijoin S.W., Grande J.P., Kumar R. 1,25-Dihydroxyvitamin D3 receptors in the central nervous system of the rat embryo. Brain Res. 1998, 804:193-205.
74. Walbert T., Jirikowski G.F., Prufer K. Distribution of 1,25-dihydroxyvitamin D3 receptor immunoreactivity in the limbic system of the rat. Horm. Metab. Res. 2001, 33:525-531.
75. Waltman N.L., Ott C.D., Twiss J.J., Gross G.J., Lindsey A.M. Vitamin D insufficiency and musculoskeletal symptoms in breast cancer survivors on aromatase inhibitor therapy. Cancer Nurs. 2009, 32:143-150.
76. White K.P., Speechley M., Harth M., Ostbye T. The London Fibromyalgia Epidemiology Study: the prevalence of fibromyalgia syndrome in London, Ontario. J. Rheumatol. 1999, 26:1570-1576.
77. Wietzke J.A., Ward E.C., Welsh J. Regulation of the human vitamin D3 receptor promoter in breast cancer cells is mediated through Sp1 sites. Mol. Cell. Endocrinol. 2005, 230:59-68.
78. Wolfe F., Ross K., Anderson J., Russell I.J., Hebert L. The prevalence and characteristics of fibromyalgia in the general population. Arthritis Rheum. 1995, 38:19-28.
79. Yasuhara O., Aimi Y., Matsuo A., Kimura H. Distribution of a splice variant of choline acetyltransferase in the trigeminal ganglion and brainstem of the rat: comparison with calcitonin gene-related peptide and substance P. J. Comp. Neurol. 2008, 509:436-448.
80. Zehnder D., Bland R., Williams M.C., McNinch R.W., Howie A.J., Stewart P.M., Hewison M. Extrarenal expression of 25-hydroxyvitamin d(3)-1 alpha-hydroxylase. J. Clin. Endocrinol. Metab. 2001, 86:888-894.