Mechanosensory responses of osteocytes to physiological forces occur along processes and not cell body and require αvβ3 integrin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 52, 2013, Pages 21012-21017

  Thi, Mia M ^a   Suadicani, Sylvia O ^a   Schaffler, Mitchell B ^b   Weinbaum, Sheldon ^b   Spray, David C ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b City College of New York   (United States)

Author keywords

Cell process attachment; Fluid flow activation; Intracellular calcium; Purinergic signaling

Indexed keywords

ADENOSINE TRIPHOSPHATE; APYRASE; CALCIUM; VITRONECTIN RECEPTOR;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; CALCIUM CELL LEVEL; CELL ACTIVATION; CELL POLARITY; HYDRODYNAMICS; LONG BONE; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; OSTEOCYTE; PRIORITY JOURNAL;

EID: 84891364059     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321210110     Document Type: Article

References (35)

1. Pead MJ, Suswillo R, Skerry TM, Vedi S, Lanyon LE (1988) Increased 3H-uridine levels in osteocytes following a single short period of dynamic bone loading in vivo. Calcif Tissue Int 43(2): 92-96.
2. Skerry TM, Bitensky L, Chayen J, Lanyon LE (1989) Early strain-related changes in enzyme activity in osteocytes following bone loading in vivo. J Bone Miner Res 4(5): 783-788.
3. Klein-Nulend J, et al. (1995) Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J 9(5): 441-445.
4. Reilly GC, Haut TR, Yellowley CE, Donahue HJ, Jacobs CR (2003) Fluid flow induced PGE2 release by bone cells is reduced by glycocalyx degradation whereas calcium signals are not. Biorheology 40(6): 591-603.
5. Tatsumi S, et al. (2007) Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab 5(6): 464-475.
6. Klein-Nulend J, Bakker AD, Bacabac RG, Vatsa A, Weinbaum S (2013) Mechanosensation and transduction in osteocytes. Bone 54(2): 182-190.
7. Doty SB (1981) Morphological evidence of gap junctions between bone cells. Calcif Tissue Int 33(5): 509-512.
8. Fritton SP, Weinbaum S (2009) Fluid and solute transport in bone: Flow-induced mechanotransduction. Annu Rev Fluid Mech 41: 347-374.
9. Han Y, Cowin SC, Schaffler MB, Weinbaum S (2004) Mechanotransduction and strain amplification in osteocyte cell processes. Proc Natl Acad Sci USA 101(47): 16689-16694.
10. You L, Cowin SC, Schaffler MB, Weinbaum S (2001) A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech 34(11): 1375-1386.
11. You LD, Weinbaum S, Cowin SC, Schaffler MB (2004) Ultrastructure of the osteocyte process and its pericellular matrix. Anat Rec A Discov Mol Cell Evol Biol 278(2): 505-513.
12. McNamara LM, Majeska RJ, Weinbaum S, Friedrich V, Schaffler MB (2009) Attachment of osteocyte cell processes to the bone matrix. Anat Rec (Hoboken) 292(3): 355-363.
13. Wang Y, McNamara LM, Schaffler MB, Weinbaum S (2007) A model for the role of integrins in flow induced mechanotransduction in osteocytes. Proc Natl Acad Sci USA 104(40): 15941-15946.
14. Hynes RO (2002) Integrins: Bidirectional, allosteric signaling machines. Cell 110(6): 673-687.
15. Yamada KM (1997) Integrin signaling. Matrix Biol 16(4): 137-141.
16. Aarden EM, et al. (1996) Adhesive properties of isolated chick osteocytes in vitro. Bone 18(4): 305-313.
17. Miyauchi A, et al. (2006) AlphaVbeta3 integrin ligands enhance volume-sensitive calcium influx in mechanically stretched osteocytes. J Bone Miner Metab 24(6): 498-504.
18. Horton MA, Davies J (1989) Perspectives: Adhesion receptors in bone. J Bone Miner Res 4(6): 803-808.
19. Hughes DE, Salter DM, Dedhar S, Simpson R (1993) Integrin expression in human bone. J Bone Miner Res 8(5): 527-533.
20. Adachi T, et al. (2009) Calciumresponse in single osteocytes to locally appliedmechanical stimulus: Differences in cell process and cell body. J Biomech 42(12): 1989-1995.
21. Wu D, Ganatos P, Spray DC, Weinbaum S (2011) On the electrophysiological response of bone cells using a Stokesian fluid stimulus probe for delivery of quantifiable localized picoNewton level forces. J Biomech 44(9): 1702-1708.
22. Wu D, Schaffler MB, Weinbaum S, Spray DC (2013) Matrix-dependent adhesion mediates network responses to physiological stimulation of the osteocyte cell process. Proc Natl Acad Sci USA 110(29): 12096-12101.
23. Lu XL, Huo B, Park M, Guo XE (2012) Calcium response in osteocytic networks under steady and oscillatory fluid flow. Bone 51(3): 466-473.
24. Genetos DC, Kephart CJ, Zhang Y, Yellowley CE, Donahue HJ (2007) Oscillating fluid flow activation of gap junction hemichannels induces ATP release from MLO-Y4 osteocytes. J Cell Physiol 212(1): 207-214.
25. Ishihara Y, et al. (2012) In situ imaging of the autonomous intracellular Ca(2+) oscillations of osteoblasts and osteocytes in bone. Bone 50(4): 842-852.
26. Lu XL, Huo B, Chiang V, Guo XE (2012) Osteocytic network is more responsive in calcium signaling than osteoblastic network under fluid flow. J Bone Miner Res 27(3): 563-574.
27. Burnstock G, Arnett TR, Orriss IR (2013) Purinergic signalling in the musculoskeletal system. Purinergic Signal, 10.1007/s11302-013-9381-4.
28. Stains JP, Watkins MP, Grimston SK, Hebert C, Civitelli R (2013) Molecular mechanisms of osteoblast/osteocyte regulation by connexin43. Calcif Tissue Int, 10.1007/s00223- 013-9742-6.
29. Arcangeli A, Becchetti A (2006) Complex functional interaction between integrin receptors and ion channels. Trends Cell Biol 16(12): 631-639.
30. Ingber DE (2006) Cellular mechanotransduction: Putting all the pieces together again. FASEB J 20(7): 811-827.
31. Wu X, Davis GE, Meininger GA, Wilson E, Davis MJ (2001) Regulation of the L-type calcium channel by alpha 5beta 1 integrin requires signaling between focal adhesion proteins. J Biol Chem 276(32): 30285-30292.
32. Burra S, et al. (2010) Dendritic processes of osteocytes are mechanotransducers that induce the opening of hemichannels. Proc Natl Acad Sci USA 107(31): 13648-13653.
33. Litzenberger JB, Kim JB, Tummala P, Jacobs CR (2010) Beta1 integrins mediate mechanosensitive signaling pathways in osteocytes. Calcif Tissue Int 86(4): 325-332.
34. Batra N, et al. (2012) Mechanical stress-activated integrin α5β1 induces opening of connexin 43 hemichannels. Proc Natl Acad Sci USA 109(9): 3359-3364.
35. Kato Y, Windle JJ, Koop BA, Mundy GR, Bonewald LF (1997) Establishment of an osteocyte-like cell line, MLO-Y4. J Bone Miner Res 12(12): 2014-2023.