Mapping the mechanome of live stem cells using a novel method to measure local strain fields in situ at the fluid-cell interface

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Song, Min Jae ^a   Brady Kalnay, Susann M ^b   McBride, Sara H ^a   Phillips Mason, Polly ^b   Dean, David ^c   Tate, Melissa L Knothe ^a,d  

^a Case Western Reserve University   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d Case Western Reserve University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONCANAVALIN A; MICROSPHERE;

ANIMAL CELL; ARTICLE; CALCULATION; CELL FATE; CELL LINEAGE; CELL STRAIN; CELL STRESS; CELL SURFACE; CELL TRACKING; CELLULAR STRESS SIGNAL; COMPUTATIONAL FLUID DYNAMICS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORRELATIONAL STUDY; EMBRYO; FLOW KINETICS; GENETIC TRANSCRIPTION; IMAGE RECONSTRUCTION; LIVE STEM CELL MECHANOME; MECHANICAL STRESS; MECHANICS; MESENCHYMAL STEM CELL; MICROPARTICLE IMAGE VELOCIMETRY; MOLECULAR MECHANICS; NONHUMAN; PARTICLE IMAGE VELOCIMETRY; PREDICTIVE VALUE; STRUCTURE ACTIVITY RELATION; YOUNG MODULUS; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; CYTOLOGY; METABOLISM; METHODOLOGY; MOUSE; MULTIPOTENT STEM CELL; PHYSIOLOGY; STEM CELL; TIME;

ANIMALS; BIOMECHANICS; CELL DIFFERENTIATION; CELL LINE; CELL SURVIVAL; MICE; MICROSPHERES; MODELS, BIOLOGICAL; MULTIPOTENT STEM CELLS; RHEOLOGY; STEM CELLS; STRESS, MECHANICAL; TIME FACTORS;

EID: 84871516550     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043601     Document Type: Article

References (62)

1. Knothe Tate ML, Falls TD, McBride SH, Atit R, Knothe UR (2008) Mechanical modulation of osteochondroprogenitor cell fate. Int J Biochem Cell Biol 40: 2720-2738.
2. Knothe Tate ML, Dolejs S, Miller RM, Knothe UR (2010) Role of mechanical loading in healing of massive bone autografts. J Orthop Res 28: 1657-1664.
3. Zimmerman J, Knothe Tate ML (2011) Structure - function relationships in the stem cell's mechanical world A: Seeding protocols as a means to control shape and fate in live cells. Mol Cell Biomech 8: 275-296.
4. Chang H, Knothe Tate ML (2011) Structure - function relationships in the stem cell's mechanical world B: Emergent anisotropy of the cytoskeleton correlates to volume and shape changing stress exposure. Mol Cell Biomech 8: 297-318.
5. Anderson EJ, Knothe Tate ML (2007) Design of tissue engineering scaffolds as delivery devices for mechanical and mechanically modulated signals. Tissue Eng 13: 2525-2538.
6. Ensley AE, Nerem RM, Anderson DE, Hanson SR, Hinds MT (2011) Fluid Shear Stress Alters the Hemostatic Properties of Endothelial Outgrowth Cells. Tissue Eng Part A 18:127-136.
7. Kasirer-Friede A, Ruggeri ZM, Shattil SJ (2010) Role for ADAP in shear flowinduced platelet mechanotransduction. Blood 115: 2274-2282.
8. Kraemer BF, Schmidt C, Urban B, Bigalke B, Schwanitz L, et al. (2011) High shear flow induces migration of adherent human platelets. Platelets 22: 415-421.
9. Smith RL, Trindade MC, Ikenoue T, Mohtai M, Das P, et al. (2000) Effects of shear stress on articular chondrocyte metabolism. Biorheology 37: 95-107.
10. Potter CM, Lundberg MH, Harrington LS, Warboys CM, Warner TD, et al. (2011) Role of shear stress in endothelial cell morphology and expression of cyclooxygenase isoforms. Arterioscler Thromb Vasc Biol 31: 384-391.
11. Rouleau L, Farcas M, Tardif JC, Mongrain R, Leask RL (2010) Endothelial cell morphologic response to asymmetric stenosis hemodynamics: effects of spatial wall shear stress gradients. J Biomech Eng 132: 081013.
12. Shi ZD, Tarbell JM (2011) Fluid flow mechanotransduction in vascular smooth muscle cells and fibroblasts. Ann Biomed Eng 39: 1608-1619.
13. Wang H, Yan S, Chai H, Riha GM, Li M, et al. (2006) Shear stress induces endothelial transdifferentiation from mouse smooth muscle cells. Biochem Biophys Res Commun 346: 860-865.
14. Zeng Y, Liu XH, Shen Y, Lai Y, Liu XJ (2011) Laminar shear stress promotes endothelial cell migration and inhibits cell apoptosis in the presence of hydroxyurea. Cell Mol Biol (Noisy-le-grand) 57 Suppl: OL1550-OL1557.
15. Ahsan T, Nerem RM (2010) Fluid shear stress promotes an endothelial-like phenotype during the early differentiation of embryonic stem cells. Tissue Eng Part A 16: 3547-3553.
16. Akimoto T, Ushida T, Miyaki S, Akaogi H, Tsuchiya K, et al. (2005) Mechanical stretch inhibits myoblast-to-adipocyte differentiation through Wnt signaling. Biochem Biophys Res Commun 329: 381-385.
17. Angele P, Yoo JU, Smith C, Mansour J, Jepsen KJ, et al. (2003) Cyclic hydrostatic pressure enhances the chondrogenic phenotype of human mesenchymal progenitor cells differentiated in vitro. J Orthop Res 21: 451-457.
18. Arnsdorf EJ, Tummala P, Castillo AB, Zhang F, Jacobs CR (2010) The epigenetic mechanism of mechanically induced osteogenic differentiation. J Biomech 43: 2881-2886.
19. Bai K, Huang Y, Jia X, Fan Y, Wang W (2010) Endothelium oriented differentiation of bone marrow mesenchymal stem cells under chemical and mechanical stimulations. J Biomech 43: 1176-1181.
20. Bakker AD, Soejima K, Klein-Nulend J, Burger EH (2001) The production of nitric oxide and prostaglandin E(2) by primary bone cells is shear stress dependent. J Biomech 34: 671-677.
21. Baksh D, Tuan RS (2007) Canonical and non-canonical Wnts differentially affect the development potential of primary isolate of human bone marrow mesenchymal stem cells. J Cell Physiol 212: 817-826.
22. Billotte WG, Dumas K, Hofmann MC (2001) Transcriptional pathways induced by fluid shear stress in mouse preosteoblast cells. Biomed Sci Instrum 37: 1-6.
23. Campbell JJ, Lee DA, Bader DL (2006) Dynamic compressive strain influences chondrogenic gene expression in human mesenchymal stem cells. Biorheology 43: 455-470.
24. Datta N, Pham QP, Sharma U, Sikavitsas VI, Jansen JA, et al. (2006) In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc Natl Acad Sci U S A 103: 2488-2493.
25. David V, Martin A, Lafage-Proust MH, Malaval L, Peyroche S, et al. (2007) Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology 148: 2553-2562.
26. Elder SH, Fulzele KS, McCulley WR (2005) Cyclic hydrostatic compression stimulates chondroinduction of C3H/10T1/2 cells. Biomech Model Mechanobiol 3: 141-146.
27. Huang Y, Jia X, Bai K, Gong X, Fan Y (2010) Effect of fluid shear stress on cardiomyogenic differentiation of rat bone marrow mesenchymal stem cells. Arch Med Res 41: 497-505.
28. Illi B, Scopece A, Nanni S, Farsetti A, Morgante L, et al. (2005) Epigenetic histone modification and cardiovascular lineage programming in mouse embryonic stem cells exposed to laminar shear stress. Circ Res 96: 501-508.
29. Knippenberg M, Helder MN, Doulabi BZ, Semeins CM, Wuisman PI, et al. (2005) Adipose tissue-derived mesenchymal stem cells acquire bone cell-like responsiveness to fluid shear stress on osteogenic stimulation. Tissue Eng 11: 1780-1788.
30. Kreke MR, Sharp LA, Lee YW, Goldstein AS (2008) Effect of intermittent shear stress on mechanotransductive signaling and osteoblastic differentiation of bone marrow stromal cells. Tissue Eng Part A 14: 529-537.
31. McBride SH, Falls T, Knothe Tate ML (2008) Modulation of stem cell shape and fate B: mechanical modulation of cell shape and gene expression. Tissue Eng Part A 14: 1573-1580.
32. Meinel L, Karageorgiou V, Fajardo R, Snyder B, Shinde-Patil V, et al. (2004) Bone tissue engineering using human mesenchymal stem cells: effects of scaffold material and medium flow. Ann Biomed Eng 32: 112-122.
33. Miyanishi K, Trindade MC, Lindsey DP, Beaupre GS, Carter DR, et al. (2006) Effects of hydrostatic pressure and transforming growth factor-beta 3 on adult human mesenchymal stem cell chondrogenesis in vitro. Tissue Eng 12: 1419- 1428.
34. Nikmanesh M, Shi ZD, Tarbell JM (2012) Heparan sulfate proteoglycan mediates shear stress-induced endothelial gene expression in mouse embryonic stem cell-derived endothelial cells. Biotechnol Bioeng 109: 583-594.
35. Roelofsen J, Klein-Nulend J, Burger EH (1995) Mechanical stimulation by intermittent hydrostatic compression promotes bone-specific gene expression in vitro. J Biomech 28: 1493-1503.
36. Stolberg S, McCloskey KE (2009) Can shear stress direct stem cell fate? Biotechnol Prog 25: 10-19.
37. Takahashi I, Nuckolls GH, Takahashi K, Tanaka O, Semba I, et al. (1998) Compressive force promotes sox9, type II collagen and aggrecan and inhibits IL- 1beta expression resulting in chondrogenesis in mouse embryonic limb bud mesenchymal cells. J Cell Sci 111 (Pt 14): 2067-2076.
38. Vinardell T, Rolfe RA, Buckley CT, Meyer EG, Ahearne M, et al. (2012) Hydrostatic pressure acts to stabilise a chondrogenic phenotype in porcine joint tissue derived stem cells. Eur Cell Mater 23: 121-132.
39. Wagner DR, Lindsey DP, Li KW, Tummala P, Chandran SE, et al. (2008) Hydrostatic pressure enhances chondrogenic differentiation of human bone marrow stromal cells in osteochondrogenic medium. Ann Biomed Eng 36: 813- 820.
40. Wu CC, Chao YC, Chen CN, Chien S, Chen YC, et al. (2008) Synergism of biochemical and mechanical stimuli in the differentiation of human placentaderived multipotent cells into endothelial cells. J Biomech 41: 813-821.
41. Ye C, Bai L, Yan ZQ, Wang YH, Jiang ZL (2008) Shear stress and vascular smooth muscle cells promote endothelial differentiation of endothelial progenitor cells via activation of Akt. Clin Biomech (Bristol, Avon) 23 Suppl 1: S118-S124.
42. Yourek G, McCormick SM, Mao JJ, Reilly GC (2010) Shear stress induces osteogenic differentiation of human mesenchymal stem cells. Regen Med 5: 713-724.
43. Zhang P, Moudgill N, Hager E, Tarola N, Dimatteo C, et al. (2011) Endothelial differentiation of adipose-derived stem cells from elderly patients with cardiovascular disease. Stem Cells Dev 20: 977-988.
44. McBride SH, Knothe Tate ML (2008) Modulation of stem cell shape and fate A: The role of density and seeding protocol on nucleus shape and gene expression. Tissue Eng Part A 14: 1561-1572.
45. McBride SH, Dolejs S, Brianza S, Knothe U, Tate ML (2011) Net change in periosteal strain during stance shift loading after surgery correlates to rapid de novo bone generation in critically sized defects. Ann Biomed Eng 39: 1570- 1581.
46. Song MJ, Dean D, Knothe Tate ML (2010) In situ spatiotemporal mapping of flow fields around seeded stem cells at the subcellular length scale. PLoS One 5. pii: e12796.
47. Anderson EJ, Falls TD, Sorkin AM, Knothe Tate ML (2006) The imperative for controlled mechanical stresses in unraveling cellular mechanisms of mechanotransduction. Biomed Eng Online 5: 27.
48. Anderson EJ, Knothe Tate ML (2007) Open access to novel dual flow chamber technology for in vitro cell mechanotransduction, toxicity and pharamacokinetic studies. Biomed Eng Online 6: 46.
49. Malek AM, Izumo S (1996) Mechanism of endothelial cell shape change and cytoskeletal remodeling in response to fluid shear stress. J Cell Sci 109 (Pt 4): 713-726.
50. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6: 483-495.
51. Anderson EJ, Kaliyamoorthy S, Iwan J, Alexander D, Knothe Tate ML (2005) Nano-microscale models of periosteocytic flow show differences in stresses imparted to cell body and processes. Ann Biomed Eng 33: 52-62.
52. Takai E, Costa KD, Shaheen A, Hung CT, Guo XE (2005) Osteoblast elastic modulus measured by atomic force microscopy is substrate dependent. Ann Biomed Eng 33: 963-971.
53. Trickey WR, Baaijens FP, Laursen TA, Alexopoulos LG, Guilak F (2006) Determination of the Poisson's ratio of the cell: recovery properties of chondrocytes after release from complete micropipette aspiration. J Biomech 39: 78-87.
54. Chowdhury F, Na S, Collin O, Tay B, Li F, et al. (2008) Is cell rheology governed by nonequilibrium-to-equilibrium transition of noncovalent bonds? Biophys J 95: 5719-5727.
55. Kuhn LT, Liu Y, Advincula M, Wang YH, Maye P, et al. (2010) A nondestructive method for evaluating in vitro osteoblast differentiation on biomaterials using osteoblast-specific fluorescence. Tissue Eng Part C Methods 16: 1357-1366.
56. Maniotis AJ, Chen CS, Ingber DE (1997) Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci USA 94: 849-854.
57. Gao L, McBeath R, Chen CS (2010) Stem Cell Shape Regulates a Chondrogenic Versus Myogenic Fate through Rac1 and N-Cadherin. Stem Cells. 28: 564-572.
58. Eggenschwiler JT, Anderson KV (2007) Cilia and developmental signaling. Annu Rev Cell Dev Biol 23:345-373.
59. Breunig JJ, Sarkisian MR, Arellano JI, Morozov YM, Ayoub AE, et al. (2008) Primary cilia regulate hippocampal neurogenesis by mediating sonic hedgehog signaling. Proc Natl Acad Sci 105(35):13127-32.
60. Zhu D, Shi S, Wang H, Liao K (2009) Growth arrest induces primary-cilium formations by mediating IGF-1-receptor signaling during differentiation induction of 3T3-L1 preadipocytes. J Cell Sci 122(Pt 15):2760-8.
61. Tummala P, Arnsdorf EJ, Jacobs CR (2010) The role of primary cilia in mesenchymal stem cell differentiation: A pivotal switch in guiding lineage commitment. Cell Mol Bioeng 3(3):207-212.
62. Gardiner MB (2005) The importance of being cilia. Howard Hughes Medical Institute Bulletin, 18 (2), 32-36 64.