Osteocyte-derived insulin-like growth factor I is essential for determining bone mechanosensitivity

American Journal of Physiology - Endocrinology and Metabolism

Volumn 305, Issue 2, 2013, Pages

  William Lau, K H ^a,b   Baylink, David J ^a   Zhou, Xiao Dong ^a   Rodriguez, Denise ^a   Bonewald, Lynda F ^c   Li, Zihui ^d   Ruffoni, Davide ^d   Müller, Ralph ^d   Kesavan, Chandrasekhar ^b   Sheng, Matilda H C ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Jerry L Pettis Memorial VA Medical Center   (United States)

^c UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^d ETH ZURICH   (Switzerland)

Author keywords

Insulin like growth factor I; Mechanical loading; Mechanotransduction; Osteocytes; Wnt

Indexed keywords

BETA CATENIN; DICKKOPF 1 PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5; OSTEOCALCIN; SOMATOMEDIN C; WNT PROTEIN; WNT10B PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE; BONE DEVELOPMENT; CELL DENSITY; CONTROLLED STUDY; GENE INACTIVATION; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TIBIA;

INSULIN-LIKE GROWTH FACTOR I; MECHANICAL LOADING; MECHANOTRANSDUCTION; OSTEOCYTES; WNT;

ANIMALS; BETA CATENIN; BIOMECHANICS; BLOTTING, WESTERN; BONE AND BONES; BONE DEVELOPMENT; DNA; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENOTYPE; INSULIN-LIKE GROWTH FACTOR I; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; OSTEOCYTES; PHOSPHATIDYLINOSITOLS; REAL-TIME POLYMERASE CHAIN REACTION; TIBIA; TOMOGRAPHY, X-RAY COMPUTED; WNT SIGNALING PATHWAY;

EID: 84880154299     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00092.2013     Document Type: Article

References (67)

1. Akhter MP, Cullen DM, Pedersen EA, Kimmel DB, Recker RR. Bone response to in vivo mechanical loading in two breeds of mice. Calcif Tissue Int 63: 442-449, 1998.
2. Bafico A, Gazit A, Pramila TM, Finch PW, Yaniv A, Aaronson SA. Interaction of frizzled related protein (FRP) with wnt ligands and the frizzled receptor suggests alternative mechanisms for FRP inhibition of wnt signaling. J Biol Chem 274: 16180-16187, 1999.
3. Bass SL, Saxon L, Daly RM, Turner CH, Robling AG, Seeman E, Stuckey S. The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res 17: 2274-2280, 2002.
4. Brun J, Fromigue O, Dieudonne FX, Marty C, Chen J, Dahan J, Wei Y, Marie PJ. The LIM-only protein FHL2 controls mesenchymal cell osteogenic differentiation and bone formation through Wnt5a and Wnt10b. Bone 53: 6-12, 2013.
5. Cawthorn WP, Bree AJ, Yao Y, Du B, Hemati N, Martinez-Santibanez G, MacDougald OA. Wnt6, wnt10a and wnt10b inhibit adipogenesis and stimulate osteoblastogenesis through a β-catenin-dependent mechanism. Bone 50: 477-489, 2012.
6. Chambers TJ, Fox S, Jagger CJ, Lean JM, Chow JW. The role of prostaglandins and nitric oxide in the response of bone to mechanical forces. Osteoarthritis Cartilage 7: 422-423, 1999.
7. Chen RH, Ding WV, McCormick F. Wnt signaling to beta-catenin involves two interactive components. Glycogen synthase kinase-3beta inhibition and activation of protein kinase C. J Biol Chem 275: 17894-17899, 2000.
8. Christiansen BA, Kotiya AA, Silva MJ. Constrained tibial vibration does not produce an anabolic bone response in adult mice. Bone 45: 750-759, 2009.
9. Courtwright A, Siamakpour-Reihani S, Arbiser JL, Banet N, Hilliard E, Fried L, Livasy C, Ketelsen D, Nepal DB, Perou CM, Patterson C, Klauber-Demore N. Secreted frizzle-related protein 2 stimulates angiogenesis via a calcineurin/NFAT signaling pathway. Cancer Res 69: 4621-4628, 2009.
10. nd Ed.). Washington, DC: CRC Press, 2001.
11. Esteve P, Sandonis A, Ibanez C, Shimono A, Guerrero I, Bovolenta P. Secreted frizzled-related proteins are required for wnt/β-catenin signaling activation in the vertebrate optic cup. Development 138: 4179-4184, 2011.
12. Fedi P, Bafico A, Nieto Soria A, Burgess WH, Miki T, Bottaro DP, Kraus MH, Aaronson SA. Isolation and biochemical characterization of the human Dkk-1 homologue, a novel inhibitor of mammalian wnt signaling. J Biol Chem 274: 19465-19472, 1999.
13. Gaston J, Quinchia Rios B, Bartlett R, Berchtold C, Thibeault SL. The response of vocal fold fibroblasts and mesenchymal stromal cells to vibration. PLoS One 7: e30965, 2012.
14. Grimston SK, Goldberg DB, Watkins M, Brodt MD, Silva MJ, Civitelli R. Connexin43 deficiency reduces the sensitivity of cortical bone to the effects of muscle paralysis. J Bone Miner Res 26: 2151-2160, 2011.
15. Hara M, Tabata K, Suzuki T, Do MK, Mizunoya W, Nakamura M, Nishimura S, Tabata S, Ikeuchi Y, Sunagawa K, Anderson JE, Allen RE, Tatsumi R. Calcium influx through a possible coupling of cation channels impacts skeletal muscle satellite cell activation in response to mechanical stretch. Am J Physiol Cell Physiol 302: C1741-C1750, 2012.
16. Hsieh HJ, Li NQ, Frangos JA. Pulsatile and steady flow induces c-fos expression in human endothelial cells. J Cell Physiol 154: 143-151, 1993.
17. 2+ signaling in living bone in response to shear stress applied on the bone surface. Bone 53: 204-215, 2013.
18. Kamioka H, Honjo T, Takano-Yamamoto T. A three-dimentional distribution of osteocyte processes revealed by the combination of confocal laser scanning microscopy and differential interference contrast microscopy. Bone 28: 145-149, 2001.
19. Kamioka H, Ishiharra Y, Ris H, Murshid SA, Sugawara Y, Takano-Yamamoto T, Lim SS. Primary cultures of chick osteocytes retain functional gap junctions between osteocytes and between osteocytes and osteoblasts. Microsc Microanal 13: 108-117, 2007.
20. Kapur S, Amoui M, Kesavan C, Wang X, Mohan S, Baylink DJ, Lau KHW. Leptin receptor (Lepr) is a negative modulator of bone mechanosensitivity and genetic variations in Lepr may contribute to the differential osteogenic response to mechanical stimulation in the C57BL/6J and C3H/HeJ pair of mouse strains. J Biol Chem 285: 37607-37618, 2010.
21. Kapur S, Baylink DJ, Lau KHW. Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 32: 241-251, 2003.
22. Kapur S, Mohan S, Baylink DJ, Lau KHW. Fluid shear stress synergizes with insulin-like growth factor-I (IGF-I) on osteoblast proliferation through integrin-dependent activation of IGF-I mitogenic signaling pathway. J Biol Chem 280: 20163-20170, 2005.
23. Kawata A, Mikuni-Takagaki Y. Mechanotransduction in stretched osteocytes-temporal expression of immediate early and other genes. Biochem Biophys Res Commun 246: 404-408, 1998.
24. Kele J, Andersson ER, Villaescusa JC, Cajanek L, Parish CL, Bonilla S, Toledo EM, Bryja V, Rubin JS, Shimono A, Arenas E. SFRP1 and SFRP2 does-dependently regulate midbrain dopamine neuron development in vivo and in embryonic stem cells. Stem Cells 30: 865-875, 2012.
25. Kesavan C, Wergedal JE, Lau KHW, Mohan S. Conditional disruption of IGF-I gene in type 1α collagen-expressing cells shows an essential role of IGF-I in skeletal anabolic response to loading. Am J Physiol Endocrinol Metab 301: E1191-E1197, 2011.
26. Kim SW, Pajevic PD, Selig M, Barry KJ, Yang JY, Shin CS, Baek WY, Kim JE, Kronenberg HM. Intermittent parathyroid hormone administration converts quiescent lining cells to active osteoblasts. J Bone Miner Res 27: 2075-2084, 2012.
27. Klein-Nulend J, Semeins CM, Ajubi NE, Nijweide PJ, Burger EH. Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts-correlation with prostaglandin upregulation. Biochem Biophy Res Commun 217: 640-648, 1995.
28. Klein-Nulend J, Van der Plas A, Semeins CM, Ajubi NE, Frangos JA, Nijweide PJ, Burger EH. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J 9: 441-445, 1995.
29. Kodama Y, Umemura Y, Nagasawa S, Beamer WG, Donahue LR, Rosen CR, Baylink DJ, Farley JR. Exercise and mechanical loading increase periosteal bone formation and whole bone strength in C57BL/6J mice but not in C3H/HeJ mice. Calcif Tissue Int 66: 298-306, 2000.
30. Kohler T, Beyeler M, Webster D, Müller R. Compartmental bone morphometry in the mouse femur: reproducibility and resolution dependence of microtomographic measurements. Calcif Tissue Int 77: 281-290, 2005.
31. Kohler T, Stauber M, Donahue LR, Müller R. Automated compartmental analysis for high-throughput skeletal phenotyping in femora of genetic mouse models. Bone 41: 659-667, 2007.
32. Lean JM, Jagger CJ, Chambers TJ, Chow JWM. Increased insulin-like growth factor I mRNA expression in rat osteocytes in response to mechanical stimulation. Am J Physiol Endocrinol Metab 268: E318-E327, 1995.
33. Lean JM, Mackay AG, Chow JWM, Chambers TJ. Osteocytic expression of mRNA for c-fos and IGF-I: an immediate early response to an osteogenic stimulus. Am J Physiol Endocrinol Metab 270: E937-E945, 1996.
34. Li X, Zhang Y, Kang H, Liu W, Liu P, Zhang J, Harris SE, Wu D. Sclerostin binds to LRP5/6 and antagonizes canonical wnt signaling. J Biol Chem 280: 19883-19887, 2005.
35. Liu C, Li Y, Semenov M, Han C, Baeq GH, Tan Y, Zhang Z, Lin X, He X. Control of beta-catenin phosphorylation/degradation by a dualkinase mechanism. Cell 108: 837-847, 2002.
36. Lu XL, Huo B, Chiang V, Guo XE. Osteocytic network is more responsive in calcium signaling than osteoblastic network under fluid flow. J Bone Miner Res 27: 563-574, 2012.
37. Main RP, Lynch ME, van der Meulen MCH. In vivo tibial stiffness is maintained by whole bone morphology and cross-sectional geometry in growing female mice. J Biomech 43: 2689-2694, 2010.
38. Mao B, Wu W, Davidson G, Marhold J, Li M, Mechler BM, Delius H, Hoppe D, Stannek P, Walter C, Glinka A, Niehrs C. Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signaling. Nature 417: 664-667, 2002.
39. Mason DJ, Hillam RA, Skerry TM. Constitutive in vivo mRNA expression by osteocytes of beta-actin, osteocalcin, connexin-43, IGF-I, c-fos and c-jun, but not TNF-alpha nor tartrate-resistant acid phosphatase. J Bone Miner Res 11: 350-357, 1996.
40. Mii Y, Taira M. Secreted wnt "inhibitors" are not just inhibitors: regulation of extracellular wnt by secreted frizzled-related proteins. Dev Growth Differ 53: 911-923, 2011.
41. Mikuni-Takagaki Y. Mechanical responses and signal transduction pathways in stretched osteocytes. J Bone Miner Metab 17: 57-60, 1999.
42. Mohan S, Baylink DJ. Bone growth factors. Clin Orthop Relat Res 263: 30-38, 1991.
43. Papachristou DJ, Papachroni KK, Papavassiliou GA, Pirttiniemi P, Gorgoulis VG, Piperi C, Basdra EK. Functional alterations in mechanical loading of condylar cartilage induces changes in the bony subcondylar region. Arch Oral Biol 54: 1035-1045, 2009.
44. Pavalko FM, Chen NX, Turner CH, Burr DB, Atkinson S, Hsieh YF, Qiu J, Duncan RL. Fluid shear-induced mechanical signaling in MC3T3-E1 osteoblasts requires cytoskeleton-integrin interactions. Am J Physiol Cell Physiol 275: C1591-C1601, 1998.
45. Powell WF Jr, Barry KJ, Tulum I, Kobayashi T, Harris SE, Bringhurst FR, Pajevic PD. Targeted ablation of the PTH/PTHrP receptor in osteocytes impairs bone structure and homeostatic calcemic responses. J Endocrinol 209: 21-32, 2011.
46. Qiao M, Shapiro P, Kumar R, Passaniti A. Insulin-like growth factor-1 regulates endogenous RUNX2 activity in endothelial cells through a phosphatidylinositol 3-kinase/ERK-dependent and Akt-independent signaling pathway. J Biol Chem 279: 42709-42718, 2004.
47. Radcliff K, Tang TB, Lim J, Zhang Z, Abedin M, Demer LL, Tintut Y. Insulin-like growth factor regulates proliferation and osteoblastic differentiation of calcifying vascular cells via extracellular signal-regulated protein kinase and phosphatidylinositol 3-kinase pathways. Circ Res 96: 398-400, 2005.
48. Reijnders CMA, Bravenboer N, Tromp AM, Blankenstein MA, Lips P. Effect of mechanical loading on insulin-like growth factor-I gene expression in rat tibia. J Endocrinol 192: 131-140, 2007.
49. Robinson JA, Chatterjee-Kishore M, Yaworsky PJ, Cullen DM, Zhao W, Li C, Kharode Y, Sauter L, Babij P, Brown EL, Hill AA, Akhter MP, Johnson ML, Recker RR, Komm BS, Bex FJ. Wnt/β-catenin signaling is a normal physiological response to mechanical loading in bone. J Biol Chem 281: 31720-31728, 2006.
50. Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I, Mantila SM, Gluhak-Heinrich J, Bellido TM, Harris SE, Turner CH. Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/Sclerostin. J Biol Chem 283: 5866-5875, 2008.
51. Rubin CT, Gross TS, McLeod KJ, Bain SD. Morphologic stages in lamellar bone formation stimulated by a potent mechanical stimulus. J Bone Miner Res 10: 488-495, 1995.
52. Sakata T, Halloran BP, Elalieh HZ, Munson SJ, Rudner L, Venton L, Ginzinger D, Rosen CJ, Bikle DD. Skeletal unloading induces resistance to insulin-like growth factor I on bone formation. Bone 32: 669-680, 2003.
53. Sakata T, Wang Y, Halloran BP, Elalieh HZ, Cao J, Bikle DD. Skeletal unloading induces resistance to insulin-like growth factor-I (IGF-I) by inhibiting activation of the IGF-I signaling pathways. J Bone Miner Res 19: 235-244, 2004.
54. Sheng MHC, Lau KHW, Beamer WG, Baylink DJ, Wergedal JE. In vivo and in vitro evidence that the high osteoblastic activity in C3H/HeJ mice compared to C57BL/6J mice is intrinsic to bone cells. Bone 35:711-719, 2004.
55. Sheng MHC, Zhou XD, Bonewald LF, Baylink DJ, Lau KHW. Disruption of the insulin-like growth factor-1 gene in osteocytes impairs developmental bone growth in mice. Bone 52: 133-144, 2013.
56. Sobiesiak M, Sivasubramaniyan K, Hermann C, Tan C, Orgel M, Treml S, Cerabona F, de Zawart P, Ochs U, Müller CA, Gargett CE, Kalbacher H, Bühring HJ. The mesenchymal stem cell antigen MSCA-1 is identical to tissue non-specific alkaline phosphatase. Stem Cells Dev 19: 669-677, 2010.
57. 2+-sensitive channel currents recorded from mouse and human embryonic stem cells. J Membr Biol 246: 215-230, 2013.
58. Tatsumi S, Ishii K, Amizuka N, Li M, Kobayashi T, Kokno K, Ito M, Takeshita S, Ikeda Kyoji. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab 5: 464-485, 2007.
59. Temiyasathit S, Tang WJ, Leucht P, Anderson CT, Monica SD, Castillo AB, Helms JA, Stearns T, Jacobs CR. Mechanosensing by the primary cilium: deletion of kif3A reduces bone formation due to loading. PLoS ONE 7: e33368, 2012.
60. Tu X, Rhee Y, Condon KW, Bivi N, Allen MR, Dwyer D, Stolina M, Turner CH, Robling AG, Plotkin LI, Bellido T. Sost downregulation and local wnt signaling are required for the osteogenic response to mechanical loading. Bone 50: 209-217, 2012.
61. Turner Bone strength: current concepts CH. Ann NY Acad Sci 1068: 429-446, 2006.
62. Turner CH, Forwood MR, Rho JY, Yoshikawa T. Mechanical loading thresholds for lamellar and woven bone formation. J Bone Miner Res 9: 87-97, 1994.
63. von Marschall Z, Fisher LW. Secreted frizzled-regulated protein-2 (sFRP2) augments canonical wnt3a-induced signaling. Biochem Biophy Res Commun 400: 299-304, 2010.
64. Wergedal JE, Mohan S, Lundy M, Baylink DJ. Skeletal growth factor and other growth factors known to be present in bone matrix stimulate proliferation and protein synthesis in human bone cells. J Bone Miner Res 5: 179-186, 1990.
65. Winkler DG, Sutherland MS, Ojala E, Turcott E, Geoghegan JC, Shpektor D, Skonier JE, Yu C, Latham JA. Sclerostin inhibition of wnt-3a-induced C3H10T1/2 cell differentiation is indirect and mediated by bone morphogenetic proteins. J Biol Chem 280: 2498-2502, 2005.
66. Xiao Z, Dallas M, Qin N, Nicolella D, Cao L, Johnson M, Boneward L, Quarles LD. Conditional deletion of Pkd1 in osteocytes disrupts skeletal mechanosensing in mice. FASEB J 25: 1-15, 2011.
67. Zhou H, Newnum AB, Martin JR, Li P, Nelson MT, Moh A, Fu XY, Yokota H, Li J. Osteoblast/osteocyte-specific inactivation of Stat3 decreases load-driven bone formation and accumulates reactive oxygen species. Bone 49: 404-411, 2011.