Fiber stretch and reorientation modulates mesenchymal stem cell morphology and fibrous gene expression on oriented nanofibrous microenvironments

Annals of Biomedical Engineering

Volumn 39, Issue 11, 2011, Pages 2780-2790

  Heo, Su Jin ^a   Nerurkar, Nandan L ^a   Baker, Brendon M ^a,c   Shin, Jung Woog ^b   Elliott, Dawn M ^a,c   Mauck, Robert L ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Inje University   (South Korea)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Biomaterials; Electrospinning; Mechanobiology; Microenvironment

Indexed keywords

AFFINE APPROXIMATION; CELL ORIENTATION; MACROSCOPIC STRAINS; MECHANICAL STIMULATION; MECHANO-BIOLOGY; MECHANOSENSITIVITY; MESENCHYMAL STEM CELL; MICROENVIRONMENTS; MICROPATTERNED; MICROSCOPIC SCALE; NUCLEAR DEFORMATIONS; SOFT TISSUE; SUBCELLULAR SCALE; SUBSTRATE ALIGNMENT; SUBSTRATE MICROSTRUCTURE;

CELL CULTURE; DEFORMATION; FLOWCHARTING; NANOFIBERS; SCAFFOLDS (BIOLOGY); STEM CELLS; STRAIN; TISSUE;

GENE EXPRESSION;

CAPROLACTONE; COLLAGEN TYPE 1; FIBRONECTIN; HEXANOIC ACID DERIVATIVE; LACTONE; NANOFIBER; PROTEIN LYSINE 6 OXIDASE; TENASCIN; TISSUE SCAFFOLD;

ANIMAL; ARTICLE; BIOMECHANICS; CATTLE; CELL DIFFERENTIATION; CELL POLARITY; CELL SHAPE; CHEMISTRY; CULTURE TECHNIQUE; CYTOLOGY; CYTOSKELETON; GENE EXPRESSION; GENETICS; MESENCHYMAL STEM CELL; METABOLISM; METHODOLOGY; NUCLEAR SHAPE; PHYSIOLOGY; TENSILE STRENGTH; TISSUE ENGINEERING;

ANIMALS; BIOMECHANICS; CATTLE; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL NUCLEUS SHAPE; CELL POLARITY; CELL SHAPE; COLLAGEN TYPE I; CYTOSKELETON; FIBRONECTINS; GENE EXPRESSION; HEXANOIC ACIDS; LACTONES; MESENCHYMAL STEM CELLS; NANOFIBERS; PROTEIN-LYSINE 6-OXIDASE; TENASCIN; TENSILE STRENGTH; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 80755139367     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-011-0365-7     Document Type: Article

References (44)

1. BM Baker RL Mauck 2007 The effect of nanofiber alignment on the maturation of engineered meniscus constructs Biomaterials 28 11 1967 1977 17250888 10.1016/j.biomaterials.2007.01.004 1:CAS:528:DC%2BD2sXht1GgsLk%3D (Pubitemid 46176172)
2. BM Baker AS Nathan AO Gee RL Mauck 2010 The influence of an aligned nanofibrous topography on human mesenchymal stem cell fibrochondrogenesis Biomaterials 31 24 6190 6200 20494438 10.1016/j.biomaterials.2010.04.036 1:CAS:528:DC%2BC3cXnt12rtLo%3D
3. BM Baker AS Nathan GR Huffman RL Mauck 2009 Tissue engineering with meniscus cells derived from surgical debris Osteoarthr Cartil 17 3 336 345 18848784 10.1016/j.joca.2008.08.001 1:STN:280:DC%2BD1M7kt1Shuw%3D%3D
4. BM Baker NL Nerurkar JA Burdick DM Elliott RL Mauck 2009 Fabrication and modeling of dynamic multi-polymer nanofibrous scaffold J. Biomech. Eng. 131 10 101012 19831482 10.1115/1.3192140
5. BM Baker SP Shah AH Huang RL Mauck 2011 Dynamic tensile loading improves the functional properties of mesenchymal stem cell-laden nanofiber-based fibrocartilage Tissue Eng. Part A 17 9 1 11 10.1089/ten.tea.2010.0535
6. SB Bruehlmann PA Hulme NA Duncan 2004 In situ intercellular mechanics of the bovine outer annulus fibrosus subjected to biaxial strains J. Biomech. 37 2 223 231 14706325 10.1016/S0021-9290(03)00244-6 (Pubitemid 38050053)
7. SB Bruehlmann JR Matyas NA Duncan 2004 Collagen fibril sliding governs cell mechanics in the anulus fibrosus: an in situ confocal microscopy study of bovine discs Spine 29 23 2612 2620 15564909 10.1097/01.brs.0000146465.05972.56 (Pubitemid 40353246)
8. JT Connelly AJ Garcia ME Levenston 2007 Inhibition of in vitro chondrogenesis in RGD-modified three-dimensional alginate gels Biomaterials 28 1071 1083 17123602 10.1016/j.biomaterials.2006.10.006 1:CAS:528: DC%2BD28Xht1Kiu7bN (Pubitemid 44809418)
9. KN Dahl EA Booth-Gauthier B Ladoux, et al. 2009 In the middle of it all: mutual mechanical regulation between the nucleus and the cytoskeleton J. Biomech. 43 1 2 8 19804886 10.1016/j.jbiomech.2009.09.002
10. KN Dahl SM Kahn KL Wilson DE Discher 2004 The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber J. Cell Sci. 117 4779 4786 15331638 10.1242/jcs.01357 1:CAS:528:DC%2BD2cXptVygurs%3D (Pubitemid 39433444)
11. KN Dahl AJ Ribeiro J Lammerding 2008 Nuclear shape, mechanics, and mechanotransduction Circ. Res. 102 11 1307 1318 18535268 10.1161/CIRCRESAHA.108. 173989 1:CAS:528:DC%2BD1cXmt1yhsbs%3D
12. DE Discher DJ Mooney PW Zandstra 2009 Growth factors, matrices, and forces combine and control stem cells Science 324 1673 1677 19556500 10.1126/science.1171643 1:CAS:528:DC%2BD1MXnsFOmtbo%3D
13. Driscoll, T. D.; N. L. Nerurkar, N. T. Jacobs, D. M. Elliott, and R. L. Mauck. Shear mechanics of electrospun scaffold for annulus fibrosus tissue engineering. J. Mech. Behav. Biomed. Mater. (in press).
14. AJ Engler S Sen HL Sweeney DE Discher 2006 Matrix elasticity directs stem cell lineage specification Cell 126 4 677 689 16923388 10.1016/j.cell.2006.06. 044 1:CAS:528:DC%2BD28Xpt1aktbg%3D (Pubitemid 44233625)
15. AH Huang MJ Farrell M Kim RL Mauck 2010 Long-term dynamic loading improves the mechanical properties of chondrogenic mesenchymal stem cell-laden hydrogels Eur. Cell. Mater. 19 72 85 20186667 1:CAS:528:DC%2BC3cXivFSnsbo%3D
16. AH Huang A Stein RL Mauck 2010 The complex transcriptional topography of mesenchymal stem cell chondrogenesis for cartilage tissue engineering Tissue Eng. Part A 16 9 2699 2708 20367254 10.1089/ten.tea.2010.0042 1:CAS:528:DC%2BC3cXhtVOiu7fF
17. K Kurpinski J Chu C Hashi S Li 2006 Anisotropic mechanosensing by mesenchymal stem cells Proc. Natl Acad. Sci. USA 103 44 16095 16100 17060641 10.1073/pnas.0604182103 1:CAS:528:DC%2BD28Xht1WmsL%2FN (Pubitemid 44715157)
18. SP Lake KS Miller DM Elliott LJ Soslowsky 2009 Effect of fiber distribution and realignment on the nonlinear and inhomogeneous mechanical properties of human supraspinatus tendon under longitudinal tensile loading J. Orthop. Res. 27 12 1596 1602 19544524 10.1002/jor.20938
19. Y Li JS Chu K Kurpinski X Li DM Bautista L Yang KL Paul Sung S Li 2011 Biophysical regulation of histone acetylation in mesenchymal stem cells Biophys. J. 100 8 1902 1909 21504726 10.1016/j.bpj.2011.03.008 1:CAS:528: DC%2BC3MXkvVKhsrs%3D
20. WJ Li RL Mauck JA Cooper X Yuan RS Tuan 2007 Engineering controllable anisotropy in electrospun biodegradable nanofibrous scaffolds for musculoskeletal tissue engineering J. Biomech. 40 8 1686 1693 17056048 10.1016/j.jbiomech.2006.09.004 (Pubitemid 46702147)
21. HA Lynch W Johannessen JP Wu A Jawa DM Elliott 2003 Effect of fiber orientation and strain-rate on the uniaxial tensile material properties of tendon J. Biomech. Eng. 125 726 731 14618932 10.1115/1.1614819 (Pubitemid 37315342)
22. F Marchand AM Ahmed 1990 Investigation of the laminate structure of lumbar disc anulus fibrosus Spine 15 402 410 2363068 10.1097/00007632-199005000- 00011 1:STN:280:DyaK3czgt1SnsQ%3D%3D (Pubitemid 20188042)
23. RL Mauck BM Baker NL Nerurkar JA Burdick WJ Li RS Tuan DM Elliott 2009 Engineering on the straight and narrow: the mechanics of nanofibrous assemblies for fiber-reinforced Tissue Eng. Part B Rev. 15 171 193 19207040 10.1089/ten.teb.2008.0652 1:CAS:528:DC%2BD1MXntlCqtr8%3D
24. RL Mauck X Yuan RS Tuan 2006 Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture Osteoarthr Cartil 14 2 179 189 16257243 10.1016/j.joca.2005.09.002 1:STN:280:DC%2BD28%2FislOmtA%3D%3D (Pubitemid 43079315)
25. R McBeath DM Pirone CM Nelson K Bhadriraju CS Chen 2004 Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev. Cell. 6 4 483 495 15068789 10.1016/S1534-5807(04)00075-9 1:CAS:528: DC%2BD2cXjsFeqsbk%3D (Pubitemid 38456178)
26. KL Moffat AS Kwei JP Spalazzi SB Doty WN Levine HH Lu 2009 Novel nanofiber-based scaffold for rotator cuff repair and augmentation Tissue Eng. Part A 15 1 115 126 18788982 10.1089/ten.tea.2008.0014 1:CAS:528: DC%2BD1MXht1elsA%3D%3D
27. Mow, V. C.; and R. Huiskes. Basic Orthopaedic Biomechanics and Mechanobiology. Philadelphia, PA: Lippincott Williams & Wilkins, 1991.
28. AS Nathan BM Baker NL Nerurkar RL Mauck 2011 Mechano-topographic modulation of stem cell nuclear shape on nanofibrous scaffolds Acta Biomater. 7 1 57 66 20709198 10.1016/j.actbio.2010.08.007 1:CAS:528:DC%2BC3cXhtlKlsrrL
29. NL Nerurkar BM Baker S Sen EE Wible DM Elliott RL Mauck 2009 Nanofibrous biologic laminates replicate the form and function of the annulus fibrosus Nat. Mater. 8 12 986 992 19855383 10.1038/nmat2558 1:CAS:528:DC%2BD1MXhsVGlt7vN
30. NL Nerurkar DM Elliott RL Mauck 2007 Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering J. Orthop. Res. 25 8 1018 1028 17457824 10.1002/jor.20384 1:CAS:528:DC%2BD2sXovFKitL8%3D (Pubitemid 47233078)
31. NL Nerurkar RL Mauck DM Elliott 2008 ISSLS prize winner: integrating theoretical and experimental methods for functional tissue engineering of the annulus fibrosus Spine 33 25 2691 2701 19018251 10.1097/BRS.0b013e31818e61f7
32. Nerurkar, N. L.; R. L. Mauck, and D. M. Elliott. Modeling interlamellar interactions in angle-ply biologic laminates for annulus fibrosus tissue engineering. Biomech. Model Mechanobiol. doi: 10.1007/s10237-011-0288-0, 2011.
33. NL Nerurkar S Sen AH Huang DM Elliott RL Mauck 2010 Engineered disc-like angle-ply structures for intervertebral disc replacement Spine 35 8 867 873 20354467 10.1097/BRS.0b013e3181d74414
34. LJ Nesti WJ Li RM Shanti YJ Jiang W Jackson BA Freedman TR Kuklo JR Giuliani RS Tuan 2008 Intervertebral disc tissue engineering using a novel hyaluronic acid-nanofibrous scaffold (HANFS) amalgam Tissue Eng. Part A 14 9 1527 1537 18707229 10.1089/ten.tea.2008.0215 1:CAS:528:DC%2BD1cXhtFWlt7vJ
35. CD Peltz SM Perry CL Getz LJ Soslowsky 2009 Mechanical properties of the long-head of the biceps tendon are altered in the presence of rotator cuff tears in a rat model J. Orthop. Res. 27 3 416 420 18924143 10.1002/jor.20770
36. TA Petrie JE Raynor DW Dumbauld TT Lee S Jagtap KL Templeman DM Collard AJ Garcia 2010 Multivalent integrin-specific ligands enhance tissue healing and biomaterial integration Sci. Transl. Med. 2 45 45ra60 20720217 10.1126/scitranslmed.3001002
37. MF Pittenger AM Mackay SC Beck RK Jaiswal R Douglas JD Mosca MA Moorman DW Simonetti S Craig DR Marshak 1999 Multilineage potential of adult human mesenchymal stem cells Science 284 5411 143 147 10102814 10.1126/science.284. 5411.143 1:CAS:528:DyaK1MXitlCnu7o%3D (Pubitemid 29282067)
38. JA Stella J Liao Y Hong W David Merryman WR Wagner MS Sacks 2008 Tissue-to-cellular level deformation coupling in cell-microintegrated elastomeric scaffolds Biomaterials 29 22 3228 3236 18472154 10.1016/j. biomaterials.2008.04.029 1:CAS:528:DC%2BD1cXmt1ejtbk%3D
39. JA Stella WR Wagner MS Sacks 2010 Scale-dependent fiber kinematics of elastomeric electrospun scaffolds for soft tissue engineering J. Biomed. Mater. Res. A 93 3 1032 1042 19753623
40. CH Thomas JH Collier CS Sfeir KE Healy 2002 Engineering gene expression and protein synthesis by modulation of nuclear shape Proc. Natl Acad. Sci. USA 99 4 1972 1977 11842191 10.1073/pnas.032668799 1:CAS:528:DC%2BD38XitVSrsLw%3D (Pubitemid 34168999)
41. ML Upton CL Gilchrist F Guilak LA Setton 2008 Transfer of macroscale tissue strain to microscale cell regions in the deformed meniscus Biophys. J. 95 4 2116 2124 18487290 10.1529/biophysj.107.126938 1:CAS:528:DC%2BD1cXpslKksLY%3D
42. M Webster KL Witkin O Cohen-Fix 2009 Sizing up the nucleus: nuclear shape, size and nuclear envelope assembly J. Cell Sci. 122 1970 1978 10.1242/jcs.037333
43. J Xie X Li J Lipner CN Manning AG Schwartz S Thomopoulos Y Xia 2010 "Aligned-to-random" nanofiber scaffolds for mimicking the structure of the tendon-to-bone insertion site Nanoscale 2 6 923 926 20648290 10.1039/c0nr00192a 1:CAS:528:DC%2BC3cXhtlKru7nE
44. L Yang RA Kandel G Chang JP Santerre 2009 Polar surface chemistry of nanofibrous polyurethane scaffold affects annulus fibrosus cell attachment and early matrix accumulation J. Biomed. Mater. Res. A 91 4 1089 1099 19107787