Loading-related regulation of gene expression in bone in the contexts of estrogen deficiency, lack of estrogen receptor α and disuse

Bone

Volumn 46, Issue 3, 2010, Pages 628-642

  Zaman, Gul ^a   Saxon, Leanne K ^a   Sunters, Andrew ^a   Hilton, Helen ^a   Underhill, Peter ^a   Williams, Debbie ^a   Price, Joanna S ^a   Lanyon, Lance E ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Bone; ER ; Estrogen; Gene expression; Mechanical loading

Indexed keywords

ESTROGEN RECEPTOR ALPHA; ESTROGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE; BONE DEVELOPMENT; BONE METABOLISM; CONTROLLED STUDY; DOWN REGULATION; ESTROGEN DEFICIENCY; FEMALE; GENE EXPRESSION REGULATION; GENE FUNCTION; MECHANICAL STRESS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; TIBIA; UPREGULATION; ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; DEFICIENCY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; PROCEDURES; PROTEIN MICROARRAY; WEIGHT BEARING;

ANIMALS; BONE AND BONES; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN ARRAY ANALYSIS; WEIGHT-BEARING;

EID: 77649181032     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2009.10.021     Document Type: Article

References (89)

1. Frost H.M. The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner. 1987, 2:73-85.
2. Wolf J. Das Gesetz der Transformation der Knochen. Berlin: A Hirschwald [trans. P Maquet & R Furlong as The Law of Bone Remodelling. Berlin: Springer, 1986] 1892.
3. Cooper C., Barker D.J., Wickham C. Physical activity, muscle strength, and calcium intake in fracture of the proximal femur in Britain. BMJ 1988, 297:1443-1446.
4. Welten D.C., Kemper H.C., Post G.B., Van Mechelen W., Twisk J., Lips P., et al. Weight-bearing activity during youth is a more important factor for peak bone mass than calcium intake. J. Bone Miner. Res. 1994, 9:1089-1096.
5. Pead M.J., Skerry T.M., Lanyon L.E. Direct transformation from quiescence to bone formation in the adult periosteum following a single brief period of bone loading. J. Bone Miner. Res. 1988, 3:647-656.
6. Lanyon L.E. Osteocytes, strain detection, bone modeling and remodeling. Calcif. Tissue Int. 1993, 53(Suppl 1):S102-S106. discussion S106-S107.
7. Greendale G.A., Edelstein S., Barrett-Connor E. Endogenous sex steroids and bone mineral density in older women and men: the Rancho Bernardo Study. J. Bone Miner. Res. 1997, 12:1833-1843.
8. Khosla S., Melton L.J., Atkinson E.J., O'Fallon W.M., Klee G.G., Riggs B.L. Relationship of serum sex steroid levels and bone turnover markers with bone mineral density in men and women: a key role for bioavailable estrogen. J. Clin. Endocrinol. Metab. 1998, 83:2266-2274.
9. Slemenda C.W., Longcope C., Zhou L., Hui S.L., Peacock M., Johnston C.C. Sex steroids and bone mass in older men. Positive associations with serum estrogens and negative associations with androgens. J. Clin. Invest. 1997, 100:1755-1759.
10. Riggs B.L., Khosla S., Melton L.J. Sex steroids and the construction and conservation of the adult skeleton. Endocr. Rev. 2002, 23:279-302.
11. Aguirre J.I., Plotkin L.I., Gortazar A.R., Millan M.M., O'Brien C.A., Manolagas S.C., et al. A novel ligand-independent function of the estrogen receptor is essential for osteocyte and osteoblast mechanotransduction. J. Biol. Chem. 2007, 282:25501-25508.
12. Jessop H.L., Sjoberg M., Cheng M.Z., Zaman G., Wheeler-Jones C.P., Lanyon L.E. Mechanical strain and estrogen activate estrogen receptor alpha in bone cells. J. Bone Miner. Res. 2001, 16:1045-1055.
13. Damien E., Price J.S., Lanyon L.E. The estrogen receptor's involvement in osteoblasts' adaptive response to mechanical strain. J. Bone Miner. Res. 1998, 13:1275-1282.
14. Lee K., Jessop H., Suswillo R., Zaman G., Lanyon L. Endocrinology: bone adaptation requires oestrogen receptor-alpha. Nature 2003, 424:389.
15. Remes T., Vaisanen S.B., Mahonen A., Huuskonen J., Kroger H., Jurvelin J.S., et al. Aerobic exercise and bone mineral density in middle-aged Finnish men: a controlled randomized trial with reference to androgen receptor, aromatase, and estrogen receptor alpha gene polymorphisms small star, filled. Bone 2003, 32:412-420.
16. Suuriniemi M., Mahonen A., Kovanen V., Alen M., Lyytikainen A., Wang Q., et al. Association between exercise and pubertal BMD is modulated by estrogen receptor alpha genotype. J. Bone Miner. Res. 2004, 19:1758-1765.
17. Wang C.L., Tang X.Y., Chen W.Q., Su Y.X., Zhang C.X., Chen Y.M. Association of estrogen receptor alpha gene polymorphisms with bone mineral density in Chinese women: a meta-analysis. Osteoporos. Int. 2007, 18:295-305.
18. Zaman G., Jessop H.L., Muzylak M., De Souza R.L., Pitsillides A.A., Price J.S., et al. Osteocytes use estrogen receptor alpha to respond to strain but their ERalpha content is regulated by estrogen. J. Bone Miner. Res. 2006, 21:1297-1306.
19. Lanyon L., Skerry T. Postmenopausal osteoporosis as a failure of bone's adaptation to functional loading: a hypothesis. J. Bone Miner. Res. 2001, 16:1937-1947.
20. Lanyon L., Armstrong V., Ong D., Zaman G., Price J. Is estrogen receptor alpha key to controlling bones' resistance to fracture?. J. Endocrinol. 2004, 182:183-191.
21. Lubahn D.B., Moyer J.S., Golding T.S., Couse J.F., Korach K.S., Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11162-11166.
22. De Souza R.L., Matsuura M., Eckstein F., Rawlinson S.C., Lanyon L.E., Pitsillides A.A. Non-invasive axial loading of mouse tibiae increases cortical bone formation and modifies trabecular organization: a new model to study cortical and cancellous compartments in a single loaded element. Bone 2005, 37:810-818.
23. Sugiyama T., Saxon L.K., Zaman G., Moustafa A., Sunters A., Price J.S., et al. Mechanical loading enhances the anabolic effects of intermittent parathyroid hormone (1-34) on trabecular and cortical bone in mice. Bone 2008, 43:238-248.
24. De Souza R.L., Pitsillides A.A., Lanyon L.E., Skerry T.M., Chenu C. Sympathetic nervous system does not mediate the load-induced cortical new bone formation. J. Bone Miner. Res. 2005, 20:2159-2168.
25. Sample S.J., Behan M., Smith L., Oldenhoff W.E., Markel M.D., Kalscheur V.L., et al. Functional adaptation to loading of a single bone is neuronally regulated and involves multiple bones. J. Bone Miner. Res. 2008, 23:1372-1381.
26. Sugiyama T., Price J.S., Lanyon L.E. Functional adaptation to mechanical loading in both cortical and cancellous bone is controlled locally and is confined to the loaded bones. Bone 2009, 10.1016/j.bone.2009.08.054.
27. Petalidis L., Bhattacharyya S., Morris G.A., Collins V.P., Freeman T.C., Lyons P.A. Global amplification of mRNA by template-switching PCR: linearity and application to microarray analysis. Nucleic Acids Res. 2003, e142:31.
28. Smyth G.K. limma: linear models for microarray data. Bioinformatics and Comutational biology Solutions Using R and bioconductor 2005, 397-420. Springer, New York. R. gentleman, V. Carey, S. Dudoit, R. irizarry, W. huber (Eds.).
29. Smyth G.K., Speed T.P. Normalization of cDNA microarray data. Methods 2003, 31:265-273.
30. Ritchie M.E., Diyagama D., Neilson J., van Laar R., Dobrovic A., Holloway A., et al. Empirical array quality weights in the analysis of microarray data. BMC Bioinformatics 2006, 7:261.
31. Smyth G.K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3. Article3.
32. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc.,. Ser. B. 1995, 57:289-300.
33. Hou N.N., Zhu Y.M., Huang H.F. The expression of estrogen receptor alpha and beta in the intervention of different estrogens in rat bone metabolism. Fen Zi Xi Bao Sheng Wu Xue Bao 2006, 39:289-296.
34. Radel C., Rizzo V. Integrin mechanotransduction stimulates caveolin-1 phosphorylation and recruitment of Csk to mediate actin reorganization. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H936-H945.
35. Sedding D.G., Hermsen J., Seay U., Eickelberg O., Kummer W., Schwencke C., et al. Caveolin-1 facilitates mechanosensitive protein kinase B (Akt) signaling in vitro and in vivo. Circ. Res. 2005, 96:635-642.
36. Rubin C.T., Lanyon L.E. Dynamic strain similarity in vertebrates; an alternative to allometric limb bone scaling. J. Theor. Biol. 1984, 107:321-327.
37. Inman C.L., Warren G.L., Hogan H.A., Bloomfield S.A. Mechanical loading attenuates bone loss due to immobilization and calcium deficiency. J. Appl. Physiol. 1999, 87:189-195.
38. Lee K.C., Maxwell A., Lanyon L.E. Validation of a technique for studying functional adaptation of the mouse ulna in response to mechanical loading. Bone 2002, 31:407-412.
39. Torrance A.G., Mosley J.R., Suswillo R.F., Lanyon L.E. Noninvasive loading of the rat ulna in vivo induces a strain-related modeling response uncomplicated by trauma or periostal pressure. Calcif. Tissue Int. 1994, 54:241-247.
40. Mosley J.R., Lanyon L.E. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone 1998, 23:313-318.
41. Srinivasan S., Ausk B.J., Poliachik S.L., Warner S.E., Richardson T.S., Gross T.S. Rest-inserted loading rapidly amplifies the response of bone to small increases in strain and load cycles. J. Appl. Physiol. 2007, 102:1945-1952.
42. Rawlinson S.C., Pitsillides A.A., Lanyon L.E. Involvement of different ion channels in osteoblasts' and osteocytes' early responses to mechanical strain. Bone 1996, 19:609-614.
43. Adachi T., Sato K., Tomita Y. Directional dependence of osteoblastic calcium response to mechanical stimuli. Biomech. Model Mechanobiol. 2003, 2:73-82.
44. Katsumi A., Orr A.W., Tzima E., Schwartz M.A. Integrins in mechanotransduction. J. Biol. Chem. 2004, 279:12001-12004.
45. Putnam A.J., Cunningham J.J., Pillemer B.B., Mooney D.J. External mechanical strain regulates membrane targeting of Rho GTPases by controlling microtubule assembly. Am. J. Physiol. Cell. Physiol. 2003, 284:C627-C639.
46. Rawlinson S.C., el-Haj A.J., Minter S.L., Tavares I.A., Bennett A., Lanyon L.E. Loading-related increases in prostaglandin production in cores of adult canine cancellous bone in vitro: a role for prostacyclin in adaptive bone remodeling?. J. Bone Miner. Res. 1991, 6:1345-1351.
47. Li J., Burr D.B., Turner C.H. Suppression of prostaglandin synthesis with NS-398 has different effects on endocortical and periosteal bone formation induced by mechanical loading. Calcif. Tissue Int. 2002, 70:320-329.
48. Pitsillides A.A., Rawlinson S.C., Suswillo R.F., Bourrin S., Zaman G., Lanyon L.E. Mechanical strain-induced NO production by bone cells: a possible role in adaptive bone (re)modeling?. FASEB J. 1995, 9:1614-1622.
49. Fox S.W., Chambers T.J., Chow J.W. Nitric oxide is an early mediator of the increase in bone formation by mechanical stimulation. Am. J. Physiol. 1996, 270:E955-E960.
50. Lindsay R., Hart D.M., Aitken J.M., MacDonald E.B., Anderson J.B., Clarke A.C. Long-term prevention of postmenopausal osteoporosis by oestrogen. Evidence for an increased bone mass after delayed onset of oestrogen treatment. Lancet 1976, 1:1038-1041.
51. Modder U.I., Riggs B.L., Spelsberg T.C., Fraser D.G., Atkinson E.J., Arnold R., et al. Dose-response of estrogen on bone versus the uterus in ovariectomized mice. Eur. J. Endocrinol. 2004, 151:503-510.
52. Kosa J.P., Balla B., Speer G., Kiss J., Borsy A., Podani J., et al. Effect of menopause on gene expression pattern in bone tissue of nonosteoporotic women. Menopause 2009, 16:367-377.
53. Karsenty G. Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell. Metab. 2006, 4:341-348.
54. Jessop H.L., Suswillo R.F., Rawlinson S.C., Zaman G., Lee K., Das-Gupta V., et al. Osteoblast-like cells from estrogen receptor alpha knockout mice have deficient responses to mechanical strain. J. Bone Miner. Res. 2004, 19:938-946.
55. Pendaries C., Darblade B., Rochaix P., Krust A., Chambon P., Korach K.S., et al. The AF-1 activation-function of ERalpha may be dispensable to mediate the effect of estradiol on endothelial NO production in mice. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:2205-2210.
56. Russell K.S., Haynes M.P., Sinha D., Clerisme E., Bender J.R. Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:5930-5935.
57. Lu Q., Pallas D.C., Surks H.K., Baur W.E., Mendelsohn M.E., Karas R.H. Striatin assembles a membrane signaling complex necessary for rapid, nongenomic activation of endothelial NO synthase by estrogen receptor alpha. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:17126-17131.
58. Callewaert F., Venken K., Ophoff J., De Gendt K., Torcasio A., van Lenthe G.H., et al. Differential regulation of bone and body composition in male mice with combined inactivation of androgen and estrogen receptor-alpha. FASEB J. 2009, 23:232-240.
59. Day T.F., Guo X., Garrett-Beal L., Yang Y. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell. 2005, 8:739-750.
60. Kato M., Patel M.S., Levasseur R., Lobov I., Chang B.H., Glass D.A., et al. Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J. Cell. Biol. 2002, 157:303-314.
61. Marenzana M., Chenu C. Sympathetic nervous system and bone adaptive response to its mechanical environment. J. Musculoskelet. Neuronal Interact. 2008, 8:111-120.
62. Burt-Pichat B., Lafage-Proust M.H., Duboeuf F., Laroche N., Itzstein C., Vico L., et al. Dramatic decrease of innervation density in bone after ovariectomy. Endocrinology 2005, 146:503-510.
63. Fujihara S., Yokozeki M., Oba Y., Higashibata Y., Nomura S., Moriyama K. Function and regulation of osteopontin in response to mechanical stress. J. Bone Miner. Res. 2006, 21:956-964.
64. Denhardt D.T., Noda M., O'Regan A.W., Pavlin D., Berman J.S. Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J. Clin. Invest. 2001, 107:1055-1061.
65. Sodek J., Ganss B., McKee M.D. Osteopontin. Crit. Rev. Oral. Biol. Med. 2000, 11:279-303.
66. Horiuchi K., Amizuka N., Takeshita S., Takamatsu H., Katsuura M., Ozawa H., et al. Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J. Bone Miner. Res. 1999, 14:1239-1249.
67. Zhu S., Barbe M.F., Liu C., Hadjiargyrou M., Popoff S.N., Rani S., et al. Periostin-like-factor in osteogenesis. J. Cell. Physiol. 2009, 218:584-592.
68. Rios H., Koushik S.V., Wang H., Wang J., Zhou H.M., Lindsley A., et al. Periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol. Cell. Biol. 2005, 25:11131-11144.
69. Thomas G., Moffatt P., Salois P., Gaumond M.H., Gingras R., Godin E., et al. Osteocrin, a novel bone-specific secreted protein that modulates the osteoblast phenotype. J. Biol. Chem. 2003, 278:50563-50571.
70. Bord S., Ireland D.C., Moffatt P., Thomas G.P., Compston J.E. Characterization of osteocrin expression in human bone. J. Histochem. Cytochem. 2005, 53:1181-1187.
71. Moustafa A., Sugiyama T., Saxon L.K., Zaman G., Sunters A., Armstrong V.J., et al. The mouse fibula as a suitable bone for the study of functional adaptation to mechanical loading. Bone 2009, 44:930-935.
72. Robling A.G., Niziolek P.J., Baldridge L.A., Condon K.W., Allen M.R., Alam I., et al. Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J. Biol. Chem. 2008, 283:5866-5875.
73. Lin C., Jiang X., Dai Z., Guo X., Weng T., Wang J., et al. Sclerostin mediates bone response to mechanical unloading via antagonizing Wnt/beta-catenin signaling. J. Bone Miner. Res. 2009, 24:1651-1661.
74. Gong Y., Slee R.B., Fukai N., Rawadi G., Roman-Roman S., Reginato A.M., et al. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 2001, 107:513-523.
75. Li X., Zhang Y., Kang H., Liu W., Liu P., Zhang J., et al. Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J. Biol. Chem. 2005, 280:19883-19887.
76. Puchner E.M., Alexandrovich A., Kho A.L., Hensen U., Schafer L.V., Brandmeier B., et al. Mechanoenzymatics of titin kinase. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13385-13390.
77. Qi J., Chi L., Labeit S., Banes A.J. Nuclear localization of the titin Z1Z2Zr domain and role in regulating cell proliferation. Am. J. Physiol. Cell. Physiol. 2008, 295:C975-C985.
78. Paic F, Igwe JC, Ravi N, Kronenberg MS, Franceschetti T, Harrington P, et al. Identification of differentially expressed genes between osteoblasts and osteocytes. Bone 2009;45:682-92.
79. Rashid S., Breckle R., Hupe M., Geisler S., Doerwald N., Neesen J. The murine Dnali1 gene encodes a flagellar protein that interacts with the cytoplasmic dynein heavy chain 1. Mol. Reprod. Dev. 2006, 73:784-794.
80. Gingras D., White D., Garin J., Multigner L., Job D., Cosson J., et al. Purification, cloning, and sequence analysis of a Mr = 30,000 protein from sea urchin axonemes that is important for sperm motility. Relationship of the protein to a dynein light chain. J. Biol. Chem. 1996, 271:12807-12813.
81. Chen C.T., Shih Y.R., Kuo T.K., Lee O.K., Wei Y.H. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem. Cells. 2008, 26:960-968.
82. Cheng M.Z., Rawlinson S.C., Pitsillides A.A., Zaman G., Mohan S., Baylink D.J., et al. Human osteoblasts' proliferative responses to strain and 17beta-estradiol are mediated by the estrogen receptor and the receptor for insulin-like growth factor I. J. Bone Miner. Res. 2002, 17:593-602.
83. Boutahar N., Guignandon A., Vico L., Lafage-Proust M.H. Mechanical strain on osteoblasts activates autophosphorylation of focal adhesion kinase and proline-rich tyrosine kinase 2 tyrosine sites involved in ERK activation. J. Biol. Chem. 2004, 279:30588-30599.
84. Sherr C.J. G1 phase progression: cycling on cue. Cell 1994, 79:551-555.
85. Zhao J. Coordination of DNA synthesis and histone gene expression during normal cell cycle progression and after DNA damage. Cell Cycle 2004, 3:695-697.
86. Sun L., Iqbal J., Dolgilevich S., Yuen T., Wu X.B., Moonga B.S., et al. Disordered osteoclast formation and function in a CD38 (ADP-ribosyl cyclase)-deficient mouse establishes an essential role for CD38 in bone resorption. FASEB J. 2003, 17:369-375.
87. Hagino H., Raab D.M., Kimmel D.B., Akhter M.P., Recker R.R. Effect of ovariectomy on bone response to in vivo external loading. J. Bone Miner. Res. 1993, 8:347-357.
88. Xing W., Baylink D., Kesavan C., Hu Y., Kapoor S., Chadwick R.B., et al. Global gene expression analysis in the bones reveals involvement of several novel genes and pathways in mediating an anabolic response of mechanical loading in mice. J. Cell. Biochem. 2005, 96:1049-1060.
89. Zhang P., Turner C.H., Yokota H. Joint loading-driven bone formation and signaling pathways predicted from genome-wide expression profiles. Bone 2009, 44:989-998.