Functional Adaptation in Female Rats: The Role of Estrogen Signaling

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Sample, Susannah J ^a   Racette, Molly A ^a   Hao, Zhengling ^a   Thomas, Cathy F ^a   Behan, Mary ^a   Muir, Peter ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CALCITONIN GENE RELATED PEPTIDE ALPHA; ESTROGEN; ESTROGEN RECEPTOR ALPHA; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 30; MESSENGER RNA; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE STRENGTH; BRACHIAL PLEXUS; CONTROLLED STUDY; ESTROGEN BLOOD LEVEL; ESTROGEN DEFICIENCY; ESTROGEN RECEPTOR ALPHA GENE; ESTROGEN RECEPTOR BETA GENE; ESTROGEN THERAPY; FEMALE; G COUPLED ESTROGEN RECEPTOR GENE; GENE; GENE EXPRESSION; HORMONE ACTION; LOADING TEST; NERVE FUNCTION; NONHUMAN; OSSIFICATION; PERIOSTEUM; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SPINAL GANGLION; TRANSIENT RECEPTOR POTENTIAL ANKYRIN 1 GENE; TRANSIENT RECEPTOR POTENTIAL VANILLOID 1 GENE; TRANSIENT RECEPTOR POTENTIAL VANILLOID 4 GENE; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; ANESTHESIA; ANIMALS; BRACHIAL PLEXUS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; FEMALE; GANGLIA, SPINAL; MALE; MODELS, BIOLOGICAL; OSTEOGENESIS; OVARIECTOMY; PERIOSTEUM; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; TRPV CATION CHANNELS; ULNA; WEIGHT-BEARING;

RATTUS;

EID: 84866292874     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043215     Document Type: Article

References (48)

1. Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, et al. (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. J Bone Miner Res 22: 465-467.
2. Lanyon L, Skerry T, (2001) Postmenopausal osteoporosis as a failure of bone's adaptive to functional loading: a hypothesis. J Bone Miner Res 16: 1937-1947.
3. Lanyon LE, Rubin CT, (1984) Static vs. dynamic loads as an influence on bone remodeling. J Biomech 17: 897-905.
4. Sample SJ, Behan M, Smith L, Oldenhoff WE, Markel MD, et al. (2008) Functional adaptation to loading of a single bone is neuronally regulated and involves multiple bones. J Bone Miner Res 23: 1372-1381.
5. Sample SJ, Behan M, Collins RJ, Wilson AP, Markel MD, et al. (2010) Systemic effects of ulna loading in young male rats during functional adaptation. J Bone Miner Res 25: 2016-2028.
6. Wu Q, Sample SJ, Baker TA, Thomas CF, Behan M, et al. (2009) Mechanical loading of a long bone induces plasticity in sensory input to the central nervous system. Neurosci Lett 463: 254-257.
7. Imai S, Rauvala H, Konttinen YT, Tokunaga T, Maeda T, et al. (1997) Efferent targets of osseus CGRP-immunoreactive nerve fiber before and after bone destruction in adjuvant arthritic rat: An ultramorphological study on their terminal-target relations. J Bone Miner Res 12: 1018-1027.
8. Martin CD, Jiminez-Andrade JM, Ghilardi JR, Mantyh PW, (2007) Organization of a unique net-like meshwork of CGRP+ sensory fibers in the mouse periosteum: Implications for the generation and maintenance of bone fracture pain. Neurosci Lett 427: 148-152.
9. Hill EL, Elde R, (1991) Distribution of CGRP, VIP, DβH, SP, and NPY-immunoreactive nerves in the periosteum of the rat. Cell Tissue Res 264: 469-480.
10. Serre CM, Farlay D, Delmas PD, Chenu C, (1999) Evidence for a dense and intimate innervation of the bone tissue, including glutamate-containing fibers. Bone 25: 623-629.
11. Jiminez-Andrade JM, Mantyh WG, Bloom AP, Xu H, Ferng AS, et al. (2010) A phenotypically restricted set of primary afferent fibers innervate the bone versus skin: Therapeutic opportunity for treating skeletal pain. Bone 46: 306-313.
12. Li J, Kreicbergs A, Bergstrom J, Stark A, Ahmed M, (2007) Site-specific CGRP innervation coincides with bone formation during fracture healing and modeling: A study in rat angulated tibia. J Orthop Res 25: 1204-1212.
13. Kwan KY, Glazer JM, Corey DP, Rice FL, Stucky CL, (2009) TRPA1 modulates mechanotransduction in cutaneous sensory neurons. J Neurosci 29: 4808-4819.
14. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, et al. (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288: 306-313.
15. Suzuki M, Mizuno A, Kodaira K, Imai M, (2003) Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278: 22664-22668.
16. Burt-Pichat B, Lafage-Proust MH, Duboeuf F, Laroche N, Izstein C, et al. (2005) Dramatic decrease of innervation density in bone after ovariectomy. Endocrinology 146: 503-510.
17. Riggs BL, Shosla S, Melton LJ 3rd, (2002) Sex steroids and the construction and conservation of the adult skeleton. Endocr Rev 23: 279-302.
18. Lee KC, Jessop H, Suswillo R, Zaman G, Lanyon LE, (2004) The adaptive response of bone to mechanical loading in female transgenic mice is deficient in the absence of oestrogen receptor-alpha and-beta. J Endocrinol 182: 193-201.
19. Saxon LK, Robling AG, Castillo AB, Mohan S, Turner CH, (2007) The skeletal responsiveness to mechanical loading is enhanced in mice with a null mutation in estrogen receptor-beta. Am J Physiol Endocrinol Metab 293: E484-491.
20. Roepke TA, Bosch MA, Rick EA, Lee B, Wagner EJ, et al. (2010) Contribution of a membrane estrogen receptor to the estrogenic regulation of body temperature and energy homeostasis. Endocrinology 151: 4926-4937.
21. Ford J, Hajibeigi A, Long M, Hahner L, Gore C, et al. (2011) GPR30 deficiency causes increased bone mass, mineralization, and growth plate proliferative activity in male mice. J Bone Miner Res 26: 298-307.
22. Fitts JM, Klein RM, Powers CA, (2011) Tamoxifen regulation of bone growth and endocrine function in the ovariectomized rat: Discrimination of responses involving estrogen receptor α/estrogen receptor β, G protein-coupled estrogen receptor, or estrogen-related receptor γ using fulvestrant (ICI 182780). J Pharmacol Exp Ther 338: 246-254.
23. Brailoiu E, Dun SL, Brailoiu GC, Mizuo K, Sklar LA, et al. (2007) Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J Endocrinol 193: 311-321.
24. Raz L, Khan MM, Mahesh VB, Vadlamudi RK, (2008) Rapid estrogen signaling in the brain. Neurosignals 16: 140-153.
25. Kuhn J, Dina OA, Goswami C, Suckow V, Levine JD, Hucho T, (2008) GPR30 estrogen receptor agonists induce mechanical hyperalgesia in the rat. Eur J Neurosci 27: 1700-1709.
26. Prossnitz ER, Barton M, (2011) The G-protein-coupled estrogen receptor GPER in health and disease. Nat Rev Endocrinol 7: 715-726.
27. Wang C, Dehghani B, Li Y, Kaler LJ, Proctor T, et al. (2009) Membrane estrogen receptor regulates experimental autoimmune encephalomyelitis through up-regulation of programmed death. J Immunol 182: 3294-3303.
28. Reed WR, Chadha HK, Hubscher CH, (2009) Effects of 17beta-estradiol on responses of viscerosomatic convergent thalamic neurons in the ovariectomized female rat. J Neurophysiol 102: 1062-1074.
29. Zhao H, Sprunger LK, Simasko SM, (2010) Expression of transient receptor potentials and two-pore potassium channels in subtypes of vagal afferent neurons in rats. Am J Phyiol Gastrointest Liver Physiol 298: G212-221.
30. Kotha SP, Hsieh YF, Strigel RM, Muller R, Silva MJ, (2004) Experimental and finite element analysis of the rat ulnar loading model - correlations between strain and bone formation following fatigue loading. J Biomech 37: 541-548.
31. Hseih Y-F, Wang T, Turner CH, (1999) Viscoelastic response of the rat loading model: Implications for studies of strain-adaptive bone formation. Bone 25: 379-382.
32. Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H, (2006) Quantitative real-time RT-PCR data analysis: current concepts and the novel "gene expression's CT difference" formula. J Mol Med 84: 901-910.
33. Cohen J (1988) Some issues in power analysis. Statistical power analysis for the behavioral sciences. Second Edition. Hillsdale, New Jersey: Lawrence Erlbaum Associates. pp 531-537.
34. Mosley JR, Lanyon LE, (2002) Growth rate rather than gender determines the size of the adaptive response of the growing skeleton to mechanical strain. Bone 30: 314-319.
35. Lee KC, Jessop H, Suswillo R, Zaman G, Lanyon L, (2003) Bone adaptation requires oestrogen receptor-α. Nature 424: 389.
36. Heino TJ, Chagin AS, Sävendahl L, (2008) The novel estrogen receptor G-protein-coupled receptor 30 is expressed in human bone. J Endocrinol 197: R1-6.
37. Jagger CJ, Chow JWM, Chambers TJ, (1996) Estrogen suppresses activation but enhances formation phase of osteogenic response to mechanical stimulation in rat bone. J Clin Invest 98: 2351-2357.
38. Järvinen TLN, Kannus P, Pajamäki I, Vuohelainen T, Tuukkanen J, et al. (2003) Estrogen deposits extra mineral into bones of female rats in puberty, but simultaneously seems to suppress the responsiveness of female skeleton to mechanical loading. Bone 32: 642-651.
39. Saxon LK, Turner CH, (2006) Low-dose estrogen treatment suppresses periosteal bone formation in response to mechanical loading. Bone 39: 1261-1267.
40. Ohlsson C, Engdahl C, Börjesson AE, Winahl SH, Studer E, et al. (2012) Estrogen receptor-∝ expression in neuronal cells affects bone mass. Proc Natl Acad Sci 109: 983-988.
41. Mårtensson UE, Salehi SA, Windahl S, Gomez MF, Swärd K, et al. (2009) Deletion of the G protein-coupled receptor 30 impairs glucose tolerance, reduces bone growth, increases blood pressure, and eliminates estradiol-stimulated insulin release in female mice. Endocrinology 150: 687-698.
42. Chagin AS, Sävendahl L, (2007) GPR30 estrogen receptor expression in the growth plate declines as puberty progresses. J Clin Endocrinol Metab 92: 4873-4877.
43. Windahl SH, Andersson N, Chagin AS, Mårtensson UE, Carlsten H, et al. (2009) The role of the G protein-coupled receptor GPR30 in the effects of estrogen in ovariectomized mice. Am J Physiol Endocrinol Metab 296: E490-E496.
44. Sohrabji F, Miranda RC, Toran-Allerand CD, (1994) Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J Neurosci 74: 459-471.
45. Dun SL, Brailoiu GC, Gao X, Brailoiu E, Arterburn JB, et al. (2009) Expression of estrogen receptor GPR30 in the rat spinal cord and in autonomic and sensory ganglia. J Neurosci Res 87: 1610-1619.
46. Papka RE, Storey-Workley M, (2002) Estrogen receptor-α and-β coexist in a subpopulation of sensory neurons of female rat dorsal root ganglia. Neurosci Lett 319: 71-74.
47. Hou YX, Jia SS, Liu YH, (2010) 17beta-Estradiol accentuates contractility of rat genioglossal muscle via regulation of estrogen receptor alpha. Arch Oral Biol 55: 309-317.
48. Yang XR, Lin MJ, McIntosh LS, Sham JS, (2006) Functional expression of transient receptor potential melastatin- and vanilloid-related channels in pulmonary arterial and aortic smooth muscle. Am J Physiol Lung Cell Mol Physiol 290: L1267-1276.