Expression of muscle anabolic and metabolic factors in mechanically loaded MLO-Y4 osteocytes

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 4, 2012, Pages

  Juffer, Petra ^a   Jaspers, Richard T ^b   Lips, Paul ^c   Bakker, Astrid D ^a   Klein Nulend, Jenneke ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Bone remodeling; Mechanical loading; Osteocytes; Signaling pathways

Indexed keywords

GROWTH FACTOR; MESSENGER RNA; MYOSTATIN; NITRIC OXIDE; SCATTER FACTOR; SOMATOMEDIN C; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; BIOSYNTHESIS; BONE REMODELING; CONTROLLED STUDY; FLUID FLOW; MECHANICS; OSSIFICATION; OSTEOCYTE; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; SHEAR STRESS; UPREGULATION;

ANIMALS; CELL LINE; HEPATOCYTE GROWTH FACTOR; INSULIN-LIKE GROWTH FACTOR I; MICE; MUSCLE, SKELETAL; NITRIC OXIDE; OSTEOCYTES; PULSATILE FLOW; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WEIGHT-BEARING;

EID: 84856602560     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00320.2011     Document Type: Article

References (67)

1. Adamopoulos IE, Xia Z, Lau YS, Athanasou NA. Hepatocyte growth factor can substitute for M-CSF to support osteoclastogenesis. Biochem Biophys Res Commun 350: 478-483, 2006.
2. Alzghoul MB, Gerrard D, Watkins BA, Hannon K. Ectopic expression of IGF-I and Shh by skeletal muscle inhibits disuse-mediated skeletal muscle atrophy and bone osteopenia in vivo. FASEB J 18: 221-223, 2004.
3. Andersen TL, Sondergaard TE, Skorzynska KE, Dagnaes-Hansen F, Plesner TL, Hauge EM, Plesner T, Delaisse JM. A physical mechanism for coupling bone resorption and formation in adult human bone. Am J Pathol 174: 239-247, 2009.
4. Anderson J, Pilipowicz O. Activation of muscle satellite cells in singlefiber cultures. Nitric Oxide 7: 36-41, 2002.
5. Bacabac RG, Smit TH, Cowin SC, Van Loon JJ, Nieuwstadt FT, Heethaar R, Klein-Nulend J. Dynamic shear stress in parallel-plate flow chambers. J Biomech 38: 159-167, 2005.
6. Bamman MM, Petrella JK, Kim JS, Mayhew DL, Cross JM. Cluster analysis tests the importance of myogenic gene expression during myofiber hypertrophy in humans. J Appl Physiol 102: 2232-2239, 2007.
7. Blitz E, Viukov S, Sharir A, Shwartz Y, Galloway JL, Pryce BA, Johnson RL, Tabin CJ, Schweitzer R, Zelzer E. Bone ridge patterning during musculoskeletal assembly is mediated through SCX regulation of Bmp4 at the tendon-skeleton junction. Dev Cell 17: 861-873, 2009.
8. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019, 2001.
9. Boudignon BM, Bikle DD, Kurimoto P, Elalieh H, Nishida S, Wang Y, Burghardt A, Majumdar S, Orwoll BE, Rosen C, Halloran BP. Insulin-like growth factor I stimulates recovery of bone lost after a period of skeletal unloading. J Appl Physiol 103: 125-131, 2007.
10. Burger EH, Klein-Nulend J, Smit TH. Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon-a proposal. J Biomech 36: 1453-1459, 2003.
11. Burger EH, Klein-Nulend J, van der Plas A, Nijweide PJ. Function of osteocytes in bone-their role in mechanotransduction. J Nutr 125: 2020S-2023S, 1995.
12. Cheung WY, Liu C, Tonelli-Zasarsky RM, Simmons CA, You L. Osteocyte apoptosis is mechanically regulated and induces angiogenesis in vitro. J Orthop Res 29: 523-530, 2011.
13. Cowin SC, Moss-Salentijn L, Moss ML. Candidates for the mechanosensory system in bone. J Biomech Eng 113: 191-197, 1991.
14. Deckers MM, Karperien M, van der Bent C, Yamashita T, Papapoulos SE, Lowik CW. Expression of vascular endothelial growth factors and their receptors during osteoblast differentiation. Endocrinology 141: 1667-1674, 2000.
15. Deng M, Zhang B, Wang K, Liu F, Xiao H, Zhao J, Liu P, Li Y, Lin F, Wang Y. Mechano growth factor E peptide promotes osteoblasts proliferation and bone-defect healing in rabbits. Int Orthop 35: 1099-1106, 2011.
16. Egginton S, Badr I, Williams J, Hauton D, Baan GC, Jaspers RT. Physiological angiogenesis is a graded, not threshold, response. J Physiol 589: 195-206, 2011.
17. Egginton S, Hudlicka O, Brown MD, Walter H, Weiss JB, Bate A. Capillary growth in relation to blood flow and performance in overloaded rat skeletal muscle. J Appl Physiol 85: 2025-2032, 1998.
18. Elkasrawy MN, Hamrick MW. Myostatin (GDF-8) as a key factor linking muscle mass and bone structure. J Musculoskelet Neuronal Interact 10: 56-63, 2010.
19. Fowlkes JL, Thrailkill KM, Liu L, Wahl EC, Bunn RC, Cockrell GE, Perrien DS, Aronson J, Lumpkin CK Jr. Effects of systemic and local administration of recombinant human IGF-I (rhIGF-I) on de novo bone formation in an aged mouse model. J Bone Miner Res 21: 1359-1366, 2006.
20. Furumatsu T, Shen ZN, Kawai A, Nishida K, Manabe H, Oohashi T, Inoue H, Ninomiya Y. Vascular endothelial growth factor principally acts as the main angiogenic factor in the early stage of human osteoblastogenesis. J Biochem 133: 633-639, 2003.
21. Gavin TP, Spector DA, Wagner H, Breen EC, Wagner PD. Nitric oxide synthase inhibition attenuates the skeletal muscle VEGF mRNA response to exercise. J Appl Physiol 88: 1192-1198, 2000.
22. Goldspink G. Mechanical signals, IGF-I gene splicing, and muscle adaptation. Physiology (Bethesda) 20: 232-238, 2005.
23. Grano M, Gelimi F, Zambonin G, Colucci S, Cottone E, Zambonin Zallone A, Comoglio P. Hepatocyte growth factor is a coupling factor for osteoclasts and osteoblasts in vitro. Proc Natl Acad Sci USA 93: 7644-7648, 1996.
24. Guicheux J, Heymann D, Rousselle AV, Gouin F, Pilet P, Yamada S, Daculsi G. Growth hormone stimulatory effects on osteoclastic resorption are partly mediated by insulin-like growth factor I: an in vitro study. Bone 22: 25-31, 1998.
25. Hamrick MW, McNeil PL, Patterson SL. Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact 10: 64-70, 2010.
26. Hamrick MW, Shi X, Zhang W, Pennington C, Thakore H, Haque M, Kang B, Isales CM, Fulzele S, Wenger KH. Loss of myostatin (GDF8) function increases osteogenic differentiation of bone marrow-derived mesenchymal stem cells but the osteogenic effect is ablated with unloading. Bone 40: 1544-1553, 2007.
27. Heinemeier KM, Olesen JL, Schjerling P, Haddad F, Langberg H, Baldwin KM, Kjaer M. Short-term strength training and the expression of myostatin and IGF-I isoforms in rat muscle and tendon: differential effects of specific contraction types. J Appl Physiol 102: 573-581, 2007.
28. Honda H, Abe S, Ishida R, Watanabe Y, Iwanuma O, Sakivama K, Ide Y. Expression of HGF and IGF-1 during regeneration of masseter muscle in mdx mice. J Muscle Res Cell Motil 31: 71-77, 2010.
29. Hossain M, Irwin R, Baumann MJ, McCabe LR. Hepatocyte growth factor (HGF) adsorption kinetics and enhancement of osteoblast differentiation on hydroxyapatite surfaces. Biomaterials 26: 2595-2602, 2005.
30. Huijing PA, Jaspers RT. Adaptation of muscle size and myofascial force transmission: a review and some new experimental results. Scand J Med Sci Sports 15: 349-380, 2005.
31. Iida K, Itoh E, Kim DS, Rincon JP, Coschigano KT, Kopchick JJ, Thorner MO. Muscle mechano growth factor is preferentially induced by growth hormone-deficient lit/lit mice. J Physiol 560: 341-349, 2004.
32. Jacquemin V, Butler-Browne GS, Furling D, Mouly V. IL-13 mediates the recruitment of reserve cells for fusion during IGF-1-induced hypertrophy of human myotubes. J Cell Sci 120: 670-681, 2007.
33. Karasik D, Kiel DP. Evidence for pleiotropic factors in genetics of the musculoskeletal system. Bone 46: 1226-1237, 2010.
34. Kato Y, Windle JJ, Koop BA, Mundy GR, Bonewald LF. Establishment of an osteocyte-like cell line, MLO-Y4. J Bone Miner Res 12: 2014-2023, 1997.
35. Klein-Nulend J, Burger EH, Semeins CM, Raisz LG, Pilbeam CC. Pulsating fluid flow stimulates prostaglandin release and inducible prostaglandin G/H synthase mRNA expression in primary mouse bone cells. J Bone Miner Res 12: 45-51, 1997.
36. 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 Biophys Res Commun 217: 640-648, 1995.
37. Kondo H, Nifuji A, Takeda S, Ezura Y, Rittling SR, Denhardt DT, Nakashima K, Karsenty G, Noda M. Unloading induces osteoblastic cell suppression and osteoclastic cell activation to lead to bone loss via sympathetic nervous system. J Biol Chem 280: 30192-30200, 2005.
38. Lalani R, Bhasin S, Byhower F, Tarnuzzer R, Grant M, Shen R, Asa S, Ezzat S, Ganzalez-Cadavid NF. Myostatin and insulin-like growth factor-I and-II expression in the muscle of rats exposed to the microgravity environment of the NeuroLab space shuttle flight. J Endocrinol 167: 417-428, 2000.
39. Leick L, Hellsten Y, Fentz J, Lyngby SS, Wojtaszewski JFP, Hidalgo J, Pilegaard H. PGC-1 mediates exercise-induced skeletal muscle VEGF expression in mice. J Appl Physiol 102: 573-581, 2007.
40. Li SH, Guo DZ, Li B, Yin HB, Li JK, Xiang JM, Deng GZ. The stimulatory effect of insulin-like growth factor-1 on the proliferation, differentiation, and mineralisation of osteoblastic cells from Holstein cattle. Vet J 179: 430-436, 2010.
41. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R. Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162: 1135-1147, 2003.
42. McGarry JG, Klein-Nulend J, Mullender MG, Prendergast PJ. A comparison of strain and fluid shear stress in stimulating bone cell responses-a computational and experimental study. FASEB J 19: 482-484, 2005.
43. Middleton J, Arnott N, Walsh S, Beresford J. Osteoblasts and osteoclasts in adult human osteophyte tissue express the mRNAs for insulinlike growth factors I and II and the type 1 IGF receptor. Bone 16: 287-293, 1995.
44. Mills P, Lafrenière JF, Benabdallah BF, El Fahimeel M, Tremblay JP. A new pro-migratory activity on human myogenic precursor cells for a synthetic peptide within the E domain of the mechano growth factor. Exp Cell Res 313: 527-537, 2007.
45. Mullender MG, Tan SD, Vico L, Alexandre C, Klein-Nulend J. Differences in osteocyte density and bone histomorphometry between men and women and between healthy and osteoporotic subjects. Calcif Tissue Int 77: 291-296, 2005.
46. Petrella JK, Kim JS, Cross JM, Kosek DJ, Bamman MM. Efficacy of myonuclear addition may explain differential myofiber growth among resistance-trained young and older men and women. Am J Physiol Endocrinol Metab 291: E937-E946, 2006.
47. 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.
48. Rittweger J, Felsenberg D. Recovery of muscle atrophy and bone loss from 90 days bed rest: results from a one-year follow-up. Bone 44: 214-224, 2009.
49. Russell ST, Marcelle JR, Rama SV, Karen E, Stephen GE. Hepatocyte growth factor is secreted by osteoblasts and cooperatively permits the survival of haematopoietic progenitors. Br J Haematol 112: 438-448, 2001.
50. Schonau E. The development of the skeletal system in children and the influence of muscular strength. Horm Res 49: 27-31, 1998.
51. Sheehan SM, Tatsumi R, Temm-Grove CJ, Allen RE. HGF is an autocrine growth factor for skeletal muscle satellite cells in vitro. Muscle Nerve 23: 239-245, 2000.
52. Shuto T, Sarkar G, Bronk JT, Matsui N, Bolander ME. Osteoblasts express types I and II activin receptors during early intramembranous and endochondral bone formation. J Bone Miner Res 12: 403-411, 1997.
53. Spangenburg EE, Bowles DK, Booth FW. Insulin-like growth factorinduced transcriptional activity of the skeletal alpha-actin gene is regulated by signaling mechanisms linked to voltage-gated calcium channels during myoblast differentiation. Endocrinology 145: 2054-2063, 2004.
54. Standal T, Abildgaard N, Fagerli UM, Stordal B, Hjertner O, Borset M, Sundan A. HGF inhibits BMP-induced osteoblastogenesis: possible implications for the bone disease of multiple myeloma. Blood 109: 3024-3030, 2007.
55. Tan SD, de Vries TJ, Kuijpers-Jagtman AM, Semeins CM, Everts V, Klein-Nulend J. Osteocytes subjected to fluid flow inhibit osteoclast formation and bone resorption. Bone 41: 745-751, 2007.
56. Tang L, Xian C, Wang Y. The MGF expression of osteoblasts in response to mechanical overload. Arch Oral Biol 51: 1080-1085, 2006.
57. Tatsumi S, Ishii K, Amizuka N, Li M, Kobayashi T, Kohno K, Ito M, Takeshita S, Ikeda K. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab 5: 464-475, 2007.
58. van Wessel T, de Haan A, van der Laarse WJ, Jaspers RT. The muscle fiber type-fiber size paradox: hypertrophy or oxidative metabolism? Eur J Appl Physiol 110: 665-694, 2010.
59. Vezeridis PS, Semeins CM, Chen Q, Klein-Nulend J. Osteocytes subjected to pulsating fluid flow regulate osteoblast proliferation and differentiation. Biochem Biophys Res Commun 348: 1082-1088, 2006.
60. Wang Y, Nishida S, Elalieh HZ, Long RK, Halloran BP, Bikle DD. Role of IGF-I signaling in regulating osteoclastogenesis. J Bone Miner Res 21: 1350-1358, 2006.
61. Wang Y, Wan C, Gilbert SR, Clemens TL. Oxygen sensing and osteogenesis. Ann NY Acad Sci 1117: 1-11, 2007.
62. Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 27: 339-360, 1994.
63. Wozniak AC, Anderson JE. Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Dev Dyn 236: 240-250, 2007.
64. Yang Q, McHugh KP, Patntirapong S, Gu X, Wunderlich L, Hauschka PV. VEGF enhancement of osteoclast survival and bone resorption involves VEGF receptor-2 signaling and beta3-integrin. Matrix Biol 27: 589-599, 2008.
65. Yang SY, Goldspink G. Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett 522: 156-160, 2002.
66. You L, Cowin S, Schaffler M, Weinbaum S. A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech 34: 1375-1386, 2001.
67. Zaman G, Saxon LK, Sunters A, Hilton H, Underhill P, Williams D, Price JS, Lanyon LE. Loading-related regulation of gene expression in bone in the contexts of estrogen deficiency, lack of estrogen receptor alpha and disuse. Bone 46: 628-642, 2010.