Oscillatory fluid flow affects human marrow stromal cell proliferation and differentiation

wbldb

Li, Ying Jun^1,2; Batra, Nikhil N.^1,2; You, Lidan^1,2; Meier, Stephen C.^1,2; Coe, Ian A.^1,2; Yellowley, Clare E.³; Jacobs, Christopher R.^1,2

Oscillatory fluid flow affects human marrow stromal cell proliferation and differentiation

J Orthop Res. November 2004;22(6):1283-1289

©2004 Orthopaedic Research Society. Published by Elsevier Ltd. All rights reserved.

Affiliations

¹Palo Alto Veterans Administration Medical Center, Palo Alto, CA 94304, USA

²Department of Mechanical Engineering, Stanford University, Stanford, CA 94305, USA

³Department of Veterinary Medicine, University of California Davis, Davis, CA 95616, USA
Abstract and keywords

Mechanical loading is an important regulator of bone formation and bone loss. Decreased osteoblast number and function are important cellular mechanisms by which mechanical disuse leads to decreased bone formation. Decreased ostesed osteoblast number may be a result of decreased osteoprogenitor proliferation, differentiation, or both. However, the effects of cellular level physical signals on osteoprogenitors are not well understood. In this study, we examined the effects of loading induced oscillatory fluid flow (OFF), a potent regulator of osteoblastic cell function, on marrow stromal cells (MSCs). MSCs subjected to OFF exhibited increased intracellular Ca2+ mobilization. In addition, MSCs exhibited increased proliferation and increased mRNA levels for osteopontin and osteocalcin genes. Collagen I and core binding factor 1 mRNA levels did not change. MSCs subjected to OFF also exhibited decreased alkaline phosphatase activity. These results suggest that MSCs are mechanosensitive and that Ca2+ may play a role in the signaling pathway.

Keywords: Mechanical loading; Stromal cells; Osteoprogenitors; Osteoblasts; Differentiation; Calcium imaging
Links

DOI: 10.1016/j.orthres.2004.04.002

PubMed: 15475210

WoS: 000224762000019

Cited Works (11)

Year	Entry
1997	Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP. Osteogenic differentiation of purified, culture‐expanded human mesenchymal stem cells in vitro. J Cell Biochem. February 1997;64(2):295-312.
2001	Donahue SW, Jacobs CR, Donahue HJ. Flow-induced calcium oscillations in rat osteoblasts are age, loading frequency, and shear stress dependent. Am J Physiol Cell Physiol. November 2001;281(5):C1635-C1641.
1998	Jacobs CR, Yellowley CE, Davis BR, Zhou Z, Cimbala JM, Donahue HJ. Differential effect of steady versus oscillating flow on bone cells. J Biomech. November 1998;31(11):969-976.
1999	Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. April 2, 1999;284(5411):143-147.
2001	You J, Reilly GC, Zhen X, Yellowley CE, Chen Q, Donahue HJ, Jacobs CR. Osteopontin gene regulation by oscillatory fluid flow via intracellular calcium mobilization and activation of mitogen-activated protein kinase in MC3T3–E1 osteoblasts. J Biol Chem. April 20, 2001;276(16):13365-13371.
1998	Turner CH, Owan I, Alvey T, Hulman J, Hock JM. Recruitment and proliferative responses of osteoblasts after mechanical loading in vivo determined using sustained-release bromodeoxyuridine. Bone. May 1998;22(5):463-469.
2002	Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. January 11, 2002;108(1):17-29.
1997	Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao Y-H, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. May 30, 1997;89(5):755-764.
2000	You J, Yellowley CE, Donahue HJ, Zhang Y, Chen Q, Jacobs CR. Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fluid flow. J Biomech Eng. August 2000;122(4):387-393.
1998	Chow JWM, Wilson AJ, Chambers TJ, Fox SW. Mechanical loading stimulates bone formation by reactivation of bone lining cells in 13‐week‐old rats. J Bone Miner Res. November 1998;13(11):1760-1767.
1994	Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech. March 1994;27(3):339-360.

Cited By (32)

Year	Entry
2011	Klika V, Maršík F. Feasible simulation of diseases related to bone remodelling and of their treatment. In: Klika V, ed. Theoretical Biomechanics. InTech; 2011:187-210.
2007	Taylor AF, Saunders MM, Shingle DL, Cimbala JM, Zhou Z, Donahue HJ. Mechanically stimulated osteocytes regulate osteoblastic activity via gap junctions. Am J Physiol Cell Physiol. January 2007;292(1):C545-C552.
2008	Gurkan UA, Akkus O. The mechanical environment of bone marrow: a review. Ann Biomed Eng. December 2008;36(12):1978-1991.
2010	Jacobs CR, Temiyasathit S, Castillo AB. Osteocyte mechanobiology and pericellular mechanics. Annu Rev Biomed Eng. 2010;12:369-400.
2008	You L, Temiyasathit S, Lee P, Kim CH, Tummala P, Yao W, Kingery W, Malone AM, Kwon RY, Jacobs CR. Osteocytes as mechanosensors in the inhibition of bone resorption due to mechanical loading. Bone. January 2008;42(1):172-179.
2020	Pei S, Parthasarathy S, Parajuli A, Martinez J, Lv M, Jiang S, Wu D, Wei S, Lu XL, Farach-Carson MC, Kirn-Safran CB, Wang L. Perlecan/Hspg2 deficiency impairs bone’s calcium signaling and associated transcriptome in response to mechanical loading. Bone. February 2020;131:115078.
2020	Willie BM, Zimmermann EA, Vitienes I, Main RP, Komarova SV. Bone adaptation: safety factors and load predictability in shaping skeletal form. Bone. February 2020;131:115114.
2006	Rubin J, Rubin C, Jacobs CR. Molecular pathways mediating mechanical signaling in bone. Gene. February 15, 2006;367:1-16.
2006	Sawakami K, Robling AG, Ai M, Pitner ND, Liu D, Warden SJ, Li J, Maye P, Rowe DW, Duncan RL, Warman ML, Turner CH. The Wnt co-receptor LRP5 is essential for skeletal mechanotransduction but not for the anabolic bone response to parathyroid hormone treatment. J Biol Chem. August 18, 2006;281(33):23698-23711.
2010	Chen J-H, Liu C, You L, Simmons CA. Boning up on Wolff's Law: mechanical regulation of the cells that make and maintain bone. J Biomech. January 5, 2010;43(1):108-118.
2011	Sen B, Xie Z, Case N, Styner M, Rubin CT, Rubin J. Mechanical signal influence on mesenchymal stem cell fate is enhanced by incorporation of refractory periods into the loading regimen. J Biomech. February 24, 2011;44(4):593-599.
2009	Riddle RC, Donahue HJ. From streaming-potentials to shear stress: 25 years of bone cell mechanotransduction. J Orthop Res. February 2009;27(2):143-149.
2013	Miller GJ. Mechanoregulation and Mechanotransduction in Skeletal Tissue Differentiation [Master's thesis]. Boston University; 2013.
2017	Cresswell EN. Spatial Regulation of Bone Formation in Functional Adaptation of Cancellous Bone [PhD thesis]. Ithaca, NY: Cornell University; May 2017.
2005	Case ND. Oscillatory Compressive Loading Effects on Mesenchymal Progenitor Cells Undergoing Chondrogenic Differentiation in Hydrogel Suspension [PhD thesis]. Atlanta, GA: Georgia Institute of Technology; May 2005.
2007	Geris L. Mathematical Modelling of Bone Regeneration During Fracture Healing and Implant Osseointegration [PhD thesis]. Leuven, Belgium: Katholieke Universiteit Leuven; May 2007.
2013	Charoenpanich A. Analyses of Human Adipose Derived Stem Cells and Human Mesenchymal Stem Cells for Functional Tissue Engineering Using Biomimetic Physical Stimuli [PhD thesis]. North Carolina State University; 2013.
2014	Steward AJ. The Mechanotransduction of Hydrostatic Pressure by Mesenchymal Stem Cells [PhD thesis]. University of Notre Dame; April 2014.
2015	Coughlin TR. Mechanobiological Signals in Trabecular Bone and Marrow [PhD thesis]. University of Notre Dame; July 2015.
2016	Metzger TA. Experimental and Computational Investigation of Bone Marrow Mechanobiology [PhD thesis]. University of Notre Dame; April 2016.
2017	Kreipke TC. Structural, Mechanical, and Biological Relationships of Trabecular Bone in Osteoporosis [PhD thesis]. Notre Dame, IN: University of Notre Dame; April 2017.
2010	Gurkan UA. Engineering of Bone Marrow in Vitro for Investigating the Role of Growth Factors and Their Mechanoresponsiveness in Osteogenesis [PhD thesis]. Purdue University; May 2010.
2018	Yang F. The Synergistic Effect of Bone Graft Substitute Architecture and Mechanical Environment on HMSCs Responses in Vitro [PhD thesis]. Queen Mary University of London; December 2018.
2014	Puwanun S. Developing a Tissue Engineering Strategy for Cleft Palate Repair [PhD thesis]. University of Sheffield; October 2014.
2008	Arnsdorf EJ. Guiding Osteogenic Lineage Commitment: The Role of Mesenchymal Stem Cell Biology and the Mechanical Microenvironment [PhD thesis]. Stanford University; September 2008.
2015	Messina SL. Effects of Oscillatory Shear Stress on Early Differentiation and Mechanotransduction [PhD thesis]. Tulane University; 2015.
2020	Pei S. Osteocyte Mechanosensing: Interstitial Fluid Flow, Cellular Response, and Turnover of Pericellular Matrix [PhD thesis]. University of Delaware; 2020.
2017	Sharma P. The Influence of Vimentin Intermediate Filaments on Human Mesenchymal Stem Cell Response to Physical Stimuli [PhD thesis]. University of Maryland; 2017.
2007	Rossello RA. Cell-to-Cell Communication as a Strategy to Regenerate Three-Dimensional Tissue [PhD thesis]. University of Michigan; 2007.
2010	Joiner DM. The Effect of Age on Bone and Its Response to Mechanical Stimulation [PhD thesis]. University of Michigan; 2010.
2010	Soves CP. The Potential Role of Megakaryocytes in Mechanically Mediated Bone Adaptation [PhD thesis]. University of Michigan; 2010.
2013	Liu CC. Effects of a New Conjugate Drug in a Rat Model of Postmenopausal Osteoporosis [Master's thesis]. University of Toronto; 2013.