Pressureless mechanical induction of stem cell differentiation is dose and frequency dependent

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Fuhrer, Roland ^a   Hofmann, Sandra ^a   Hild, Nora ^a   Vetsch, Jolanda R ^a   Herrmann, Inge K ^b   Grass, Robert N ^a   Stark, Wendelin J ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; TRANSFORMING GROWTH FACTOR BETA1; HYDROGEL;

ARTICLE; CELL DIFFERENTIATION; CHONDROGENESIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYDROGEL; MAGNETIC FIELD; MECHANICAL STIMULATION; MESENCHYMAL STEM CELL; CYTOLOGY; MECHANICS; MESENCHYMAL STROMA CELL; PHYSIOLOGY; TISSUE SCAFFOLD;

CELL DIFFERENTIATION; CHONDROGENESIS; HUMANS; HYDROGEL; MECHANICAL PHENOMENA; MESENCHYMAL STROMAL CELLS; TISSUE SCAFFOLDS;

EID: 84896737285     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081362     Document Type: Article

References (53)

1. Vunjak-Novakovic G, David Scadden T (2011) Biomimetic Platforms for Human Stem. Cell Research - Cell Stem Cell 8: 252-261. doi:10.1016/j.stem.2011.02. 014.
2. van Meer G (2005) Cellular lipidomics. EMBO J 24: 3159-3165. doi:10.1038/sj.emboj.7600798. PubMed: 16138081.
3. Gumbiner BM (1996) Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 84: 345-357. doi:10.1016/S0092-8674(00) 81279-9. PubMed: 8608588.
4. Burdick JA, Vunjak-Novakovic G (2009) Engineered Microenvironments for Controlled Stem. Cell Differentiation - Tissue Eng Part A 15: 205-219. doi:10.1089/ten.tea.2008.0131.
5. Grodzinsky AJ, Levenston ME, Jin M, Frank EH (2000) Cartilage tissue remodeling in response to mechanical forces. Annu Rev Biomed Eng 2: 691-713. doi:10.1146/annurev.bioeng.2.1.691. PubMed: 11701528.
6. Kim YJ, Sah RLY, Grodzinsky AJ, Plaas AHK, Sandy JD (1994) Mechanical regulation of cartilage biosynthetic behavior - physical stimuli. Arch Biochem Biophys 311: 1-12. doi:10.1006/abbi.1994.1201. PubMed: 8185305.
7. Mauck RL, Soltz MA, Wang CCB, Wong DD, Chao PHG et al. (2000) Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng 122: 252-260. doi:10.1115/1.429656. PubMed: 10923293.
8. Nagel-Heyer S, Goepfert C, Feyerabend F, Petersen JP, Adamietz P et al. (2005) Bioreactor cultivation of three-dimensional cartilage-carrierconstructs. Bioprocess Biosyst Eng 27: 273-280. doi:10.1007/s00449-005-0419-z. PubMed: 15928929.
9. Li Z, Yao SJ, Alini M, Stoddart MJ (2010) Chondrogenesis of Human Bone Marrow Mesenchymal Stem Cells in Fibrin-Polyurethane Composites Is Modulated by Frequency and Amplitude of Dynamic Compression and Shear. Stress - Tissue Eng Part A 16: 575-584. doi:10.1089/ten.tea.2009.0262.
10. Rogers BA, Murphy CL, Cannon SR, Briggs TWR (2006) Topographical variation in glycosaminoglycan content in human articular cartilage. J Bone Joint Surg Br 88B: 1670-1674. PubMed: 17159186.
11. Masuda T, Takahashi I, Anada T, Arai F, Fukuda T et al. (2008) Development of a cell culture system loading cyclic mechanical strain to chondrogenic cells. J Biotechnol 133: 231-238. doi:10.1016/j.jbiotec.2007.08. 007. PubMed: 17904677.
12. Grossi A, Yadav K, Lawson MA (2007) Mechanical stimulation increases proliferation, differentiation and protein expression in culture: Stimulation effects are substrate dependent. J Biomech 40: 3354-3362. doi:10.1016/j. jbiomech.2007.05.007. PubMed: 17582421.
13. Finger AR, Sargent CY, Dulaney KO, Bernacki SH, Loboa EG (2007) Differential effects on messenger ribonucleic acid expression by bone marrow-derived human mesenchymal stem cells seeded in agarose constructs due to ramped and steady applications of cyclic hydrostatic pressure. Tissue Eng 13: 1151-1158. doi:10.1089/ten.2006.0290. PubMed: 17518710.
14. Hoffman BD, Massiera G, Van Citters KM, Crocker JC (2006) The consensus mechanics of cultured mammalian cells. Proc Natl Acad Sci U S A 103: 10259-10264. doi:10.1073/pnas.0510348103. PubMed: 16793927.
15. Langelaan MLP, Boonen KJM, Rosaria-Chak KY, van der Schaft DWJ, Post MJ et al. (2011) Advanced maturation by electrical stimulation: Differences in response between C2C12 and primary muscle progenitor cells. J Tissue Eng Regen Med 5: 529-539. doi:10.1002/term.345. PubMed: 21695794.
16. Lee KBL, Hui JHP, Song IC, Ardany L, Lee EH (2007) Injectable mesenchymal stem cell therapy for large cartilage defects - A porcine model. Stem Cells 25: 2964-2971. doi:10.1634/stemcells.2006-0311. PubMed: 17656639.
17. Park H, Temenoff JS, Tabata Y, Caplan AI, Mikos AG (2007) Injectable biodegradable hydrogel composites for rabbit marrow mesenchymal stem cell and growth factor delivery for cartilage tissue engineering. Biomaterials 28: 3217-3227. doi:10.1016/j.biomaterials.2007.03.030. PubMed: 17445882.
18. Potier E, Noailly J, Ito K (2010) Directing bone marrow-derived stromal cell function with mechanics. J Biomech 43: 807-817. doi:10.1016/j.jbiomech. 2009.11.019. PubMed: 19962149.
19. Robling AG, Hinant FM, Burr DB, Turner CH (2002) Improved bone structure and strength after long-term mechanical loading is greatest if loading is separated into short bouts. J Bone Miner Res 17: 1545-1554. doi:10.1359/jbmr. 2002.17.8.1545. PubMed: 12162508.
20. Hunziker EB, Kapfinger E, Geiss J (2007) The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development. Osteoarthritis Cartilage 15: 403-413. doi:10.1016/j.joca.2006.09.010. PubMed: 17098451.
21. Roodenburg PJ, Wladimiroff JW, van Es A, Prechtl HFR (1991) Classification and quantitative aspects of fetal movements during the 2nd-half of normal-pregnancy. Early Hum Dev 25: 19-35. doi: 10.1016/0378-3782(91)90203-F. PubMed: 2055173.
22. Schilling F (1973) Reflex dystrophy and dystrophic pseudoarthritis of lower limbs. Z Rheumaforsch 32: 375-384. PubMed: 4129809.
23. Ohta A, Yamaguchi M, Kaneoka H, Nagayoshi T, Hiida M (1987) Adult stills disease - Review of 228 cases from the literature. J Rheumatol 14: 1139-1146. PubMed: 3325642.
24. Altman GH, Horan RL, Martin I, Farhadi J, Stark PRH et al. (2001) Cell differentiation by mechanical stress. FASEB J 15: 270-272. doi:10.1096/fj.00- 0170hyp. PubMed: 11149915.
25. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689. doi:10.1016/j.cell.2006.06. 044. PubMed: 16923388.
26. Trappmann B, Gautrot JE, Connelly JT, Strange DGT, Li Y et al. (2012) Extracellular-matrix tethering regulates stem-cell fate. Nat Mater 11: 642-649. doi:10.1038/nmat3339. PubMed: 22635042.
27. Caplan AI (1991) Mesenchymal stem-cells. J Orthop Res 9: 641-650. doi:10.1002/jor.1100090504. PubMed: 1870029.
28. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147. doi:10.1126/science.284.5411.143. PubMed: 10102814.
29. Prockop DJ (1997) Marrow stromal cells as steam cells for nonhematopoietic tissues. Science 276: 71-74. doi:10.1126/science.276.5309.71. PubMed: 9082988.
30. Puetzer JL, Petitte JN, Loboa EG (2010) Comparative Review of Growth Factors for Induction of Three-Dimensional In Vitro Chondrogenesis in Human Mesenchymal Stem Cells Isolated from Bone Marrow and Adipose Tissue. Tissue Eng Part B Rev 16: 435-444. doi:10.1089/ten.tec.2009.0247. PubMed: 20196646.
31. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480. doi:10.1016/j.cell.2006.10.018. PubMed: 17081971.
32. Fuhrer R, Athanassiou EK, Luechinger NA, Stark WJ (2009) Crosslinking Metal Nanoparticles into the Polymer Backbone of Hydrogels Enables Preparation of Soft, Magnetic Field-Driven Actuators with Muscle-Like Flexibility. Small 5: 383-388. doi:10.1002/smll.200801091. PubMed: 19180549.
33. Grass RN, Stark WJ (2006) Gas phase synthesis of fcc-cobalt nanoparticles. J Mater Chem 16: 1825-1830. doi:10.1039/b601013j.
34. Michalopoulos E, Knight RL, Korossis S, Kearney JN, Fisher J et al. (2012) Development of Methods for Studying the Differentiation of Human Mesenchymal Stem Cells Under Cyclic Compressive Strain. Tissue Eng Part C Methods 18: 252-262. doi:10.1089/ten.tea.2011.0142. PubMed: 22047076.
35. Reger RL, Tucker AH, Wolfe MR (2008) Differentiation and characterization of human MSCs. In: DJ ProckopDG PhinneyBA Bunnell. Methods in Molecular Biology. Humana Press Inc, Totowa, USA pp. 93-107.
36. 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. doi:10.1023/B:ABME.0000007796.48329.b4. PubMed: 14964727.
37. Herrmann IK, Urner M, Koehler FM, Hasler M, Roth-Z'Graggen B et al. (2010) Blood Purification Using Functionalized Core/Shell Nanomagnets. Small 6: 1388-1392. doi:10.1002/smll.201000438. PubMed: 20564487.
38. Weber W, Lienhart C, Baba MDE, Grass RN, Kohler T et al. (2009) Magnet-guided transduction of mammalian cells and mice using engineered magnetic lentiviral particles. J Biotechnol 141: 118-122. doi:10.1016/j.jbiotec.2009.02. 023. PubMed: 19433214.
39. Shintani N, Hunziker EB (2011) Differential effects of dexamethasone on the chondrogenesis of mesenchymal stromal cells: influence of microenvironment, tissue origin and growth factor. Eur Cell Mater 22: 302-320. PubMed: 22116649.
40. Johnson K, Zhu S, Tremblay MS, Payette JN, Wang J et al. (2012) A Stem Cell-Based Approach to Cartilage Repair. Science 336: 717-721. doi:10.1126/science.1215157. PubMed: 22491093.
41. Bi WM, Deng JM, Zhang ZP, Behringer RR, de Crombrugghe B (1999) Sox9 is required for cartilage formation. Nat Genet 22: 85-89. doi:10.1038/8792. PubMed: 10319868.
42. Magne D, Vinatier C, Julien M, Weiss P, Guicheux J (2005) Mesenchymal stem cell therapy to rebuild cartilage. Trends Mol Med 11: 519-526. doi:10.1016/j.molmed.2005.09.002. PubMed: 16213191.
43. Lutolf MP, Gilbert PM, Blau HM (2009) Designing materials to direct stem-cell fate. Nature 462: 433-441. doi:10.1038/nature08602. PubMed: 19940913.
44. Mitragotri S, Lahann J (2009) Physical approaches to biomaterial design. Nat Mater 8: 15-23. doi:10.1038/nmat2344. PubMed: 19096389.
45. Coburn JM, Gibson M, Monagle S, Patterson Z, Elisseeff JH (2012) Bioinspired nanofibers support chondrogenesis for articular cartilage repair. Proc Natl Acad Sci U S A 109: 10012-10017. doi:10.1073/pnas.1121605109. PubMed: 22665791.
46. Galle J, Bader A, Hepp P, Grill W, Fuchs B et al. (2010) Mesenchymal Stem Cells in Cartilage Repair: State of the Art and Methods to monitor Cell Growth, Differentiation and Cartilage Regeneration. Curr Med Chem 17: 2274-2291. doi:10.2174/092986710791331095. PubMed: 20459378.
47. Place ES, Evans ND, Stevens MM (2009) Complexity in biomaterials for tissue engineering. Nat Mater 8: 457-470. doi:10.1038/nmat2441. PubMed: 19458646.
48. Even-Ram S, Artym V, Yamada KM (2006) Matrix control of stem cell fate. Cell 126: 645-647. doi:10.1016/j.cell.2006.08.008. PubMed: 16923382.
49. Snow WB (1943) The relation of physical therapy to arthritis. N Engl J Med 229: 959-965. doi:10.1056/NEJM194312232292601.
50. Toyoda T, Matsumoto H, Fujikawa K, Saito S, Inoue K (1998) Tensile load and the metabolism of anterior cruciate ligament cells. Clin Orthop Relat Res: 247-255. PubMed: 9728181.
51. North TE, Goessling W, Peeters M, Li PL, Ceol C et al. (2009) Hematopoietic Stem Cell Development Is Dependent on Blood Flow. Cell 137: 736-748. doi:10.1016/j.cell.2009.04.023. PubMed: 19450519.
52. Gong Z, Calkins G, Cheng EC, Krause D, Niklason LE (2009) Influence of culture medium on smooth muscle cell differentiation from human bone marrow-derived mesenchymal stem cells. Tissue Eng Part A 15: 319-330. doi:10.1089/ten.tea.2008.0161. PubMed: 19115826.
53. Mayer-Wagner S, Passberger A, Sievers B, Aigner J, Summer B et al. (2011) Effects of Low Frequency Electromagnetic Fields on the Chondrogenic Differentiation of Human Mesenchymal Stem Cells. Bioelectromagnetics 32: 283-290. doi:10.1002/bem.20633. PubMed: 21452358.