Geometry and force control of cell function

Journal of Cellular Biochemistry

Volumn 108, Issue 5, 2009, Pages 1047-1058

  Freytes, Donald O ^a   Wan, Leo Q ^a   Vunjak Novakovic, Gordana ^a  

^a Columbia University ^*  (United States)

Author keywords

Biophysical regulation; Bioreactors; Scaffolds; Stem cells; Tissue engineering

Indexed keywords

BIOMIMETIC MATERIAL; TISSUE SCAFFOLD;

CELL CULTURE; CELL FUNCTION; CULTURE TECHNIQUE; GEOMETRY; HEART DEVELOPMENT; HUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TISSUE ENGINEERING; TISSUE REGENERATION;

ANIMALS; BIOMEDICAL RESEARCH; BIOMIMETICS; CELL CULTURE TECHNIQUES; HUMANS; MODELS, BIOLOGICAL; RATS; REGENERATION; STEM CELLS; STRESS, PHYSIOLOGICAL; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TRANSPLANTS;

EID: 72449126726     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22355     Document Type: Review

References (77)

1. Abu-Issa R, Kirby ML. 2007. Heart field: From mesoderm to heart tube. Annu Rev Cell Dev Biol 23:45-68.
2. Altman GH, Horan RL, Martin I, Farhadi J, Stark PR, Volloch V, Richmond JC, Vunjak-Novakovic G, Kaplan DL. 2002. Cell differentiation by mechanical stress. FASEB J 16:270-272.
3. Belousov LV, Ermakov AS. 2001. Artificially applied tensions normalize development of relaxed Xenopus Laevis embryos. Ontogenez 32:288-294.
4. Benoit DS, Schwartz MP, Durney AR, Anseth KS. 2008. Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat Mater 7:816-823.
5. Benya PD, Shaffer JD. 1982. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30:215-224.
6. Bettinger CJ, Langer R, Borenstein JT. 2009. Engineering substrate topography at the micro- and nanoscale to control cell function. Angew Chem Int Ed Engl 48:5406-5415.
7. Bissell MJ, Aggeler J. 1987. Dynamic reciprocity: How do extracellular matrix and hormones direct gene expression? Prog Clin Biol Res 249:251-262.
8. Bornstein P, Duksin D, Balian G, Davidson JM, Crouch E. 1978. Organization of extracellular proteins on the connective tissue cell surface: Relevance to cell-matrix interactions in vitro and in vivo. Ann NY Acad Sci 312:93-105. (Pubitemid 8385430)
9. Butler DL, Goldstein SA, Guilak F. 2000. Functional tissue engineering: The role of biomechanics. J Biomech Eng 122:570-575. (Pubitemid 32047018)
10. Caplan AI, Bruder SP. 2001. Mesenchymal stem cells: Building blocks for molecular medicine in the 21st century. Trends Mol Med 7:259-264. (Pubitemid 32545522)
11. Chen H, Feyereisen M, Long XP, Fitzgerald G. 1993. Stability, bonding, and geometric structure of Ti8C12, Ti8N12, V8C12, and Zr8C12. Phys Rev Lett 71:1732-1735.
12. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. 1997. Geometric control of cell life and death. Science 276:1425-1428. (Pubitemid 27235413)
13. Chen CS, Tan J, Tien J. 2004. Mechanotransduction at cell-matrix and cellcell contacts. Annu Rev Biomed Eng 6:275-302.
14. Choi NW, Cabodi M, Held B, Gleghorn JP, Bonassar LJ, Stroock AD. 2007. Microfluidic scaffolds for tissue engineering. Nat Mater 6:908-915.
15. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, Wilkinson CD, Oreffo RO. 2007. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6:997-1003. (Pubitemid 350210577)
16. Dembo M, Wang YL. 1999. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys J 76:2307-2316. (Pubitemid 29266384)
17. Dike LE, Chen CS, Mrksich M, Tien J, Whitesides GM, Ingber DE. 1999. Geometric control of switching between growth, apoptosis, and differentiation during angiogenesis using micropatterned substrates. In Vitro Cell Dev Biol Anim 35:441-448. (Pubitemid 29463765)
18. Discher DE, Janmey P, Wang YL. 2005. Tissue cells feel and respond to the stiffness of their substrate. Science 310:1139-1143. (Pubitemid 41681732)
19. Discher DE, Mooney DJ, Zandstra PW. 2009. Growth factors, matrices, and forces combine and control stem cells. Science 324:1673-1677.
20. Elisseeff J, Ferran A, Hwang S, Varghese S, Zhang Z. 2006. The role of biomaterials in stem cell differentiation: Applications in the musculoskeletal system. Stem Cells Dev 15:295-303. (Pubitemid 44100008)
21. Engelmayr GC, Cheng M, Bettinger CJ, Borenstein JT, Langer R, Freed LE. 2008. Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat Mater 7:1003-1010.
22. Engler AJ, Sen S, Sweeney HL, Discher DE. 2006. Matrix elasticity directs stem cell lineage specification. Cell 126:677-689. (Pubitemid 44233625)
23. Engler AJ, Carag-Krieger C, Johnson CP, Raab M, Tang HY, Speicher DW, Sanger JW, Sanger JM, Discher DE. 2008. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: Scar-like rigidity inhibits beating. J Cell Sci 121:3794-3802.
24. Ferguson M, O'Kane S. 2004. Scar-free healing: From embryonic mechanisms to adult therapeutic intervention. Philos Trans R Soc Lond B Biol Sci 359:839-850. (Pubitemid 38673751)
25. Gerecht S, Burdick JA, Ferreira LS, Townsend SA, Langer R, Vunjak-Novakovic G. 2007. Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc Natl Acad Sci USA 104:11298-11303. (Pubitemid 47175135)
26. Grayson WL, Bhumiratana S, Cannizzaro C, Chao PH, Lennon DP, Caplan AI, Vunjak-Novakovic G. 2008. Effects of initial seeding density and fluid perfusion rate on formation of tissue-engineered bone. Tissue Eng Part A 14:1809-1820.
27. Harrison RG. 1907. Observations on the living developing nerve fiber. Anat Rec 1:116-118.
28. Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M. 2003. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421:172-177. (Pubitemid 36090985)
29. Hui EE, Bhatia SN. 2007. Micromechanical control of cell-cell interactions. Proc Natl Acad Sci USA 104:5722-5726.
30. Hwang NS, Varghese S, Elisseeff J. 2008. Controlled differentiation of stem cells. Adv Drug Deliv Rev 60:199-214.
31. Kloxin AM, Kasko AM, Salinas CN, Anseth KS. 2009. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 324:59-63.
32. Lang T, LeBlanc A, Evans H, Lu Y, Genant H, Yu A. 2004. Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J Bone Miner Res 19:1006-1012. (Pubitemid 41103458)
33. Langer R, Tirrell DA. 2004. Designing materials for biology and medicine. Nature 428:487-492.
34. Li Jeon N, Baskaran H, Dertinger SK, Whitesides GM, Van de Water L, Toner M. 2002. Neutrophil chemotaxis in linear and complex gradients of interleukin-8 formed in a microfabricated device. Nat Biotechnol 20:826-830. (Pubitemid 34836761)
35. Lin CQ, Bissell MJ. 1993. Multi-faceted regulation of cell differentiation by extracellular matrix. FASEB J 7:737-743. (Pubitemid 23199531)
36. Little CD, Rongish BJ. 1995. The extracellular matrix during heart development. Experientia 51:873-882.
37. Lucchetta EM, Lee JH, Fu LA, Patel NH, Ismagilov RF. 2005. Dynamics of Drosophila embryonic patterning network perturbed in space and time using microfluidics. Nature 434:1134-1138.
38. Lutolf MP, Hubbell JA. 2005. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23:47-55.
39. Mauck RL, Soltz MA, Wang CC, Wong DD, Chao PH, Valhmu WB, Hung CT, Ateshian GA. 2000. Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng 122:252-260.
40. 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. (Pubitemid 38456178)
41. Meinel L, Karageorgiou V, Fajardo R, Snyder B, Shinde-Patil V, Zichner L, Kaplan D, Langer R, Vunjak-Novakovic G. 2004. Bone tissue engineering using human mesenchymal stem cells: Effects of scaffold material and medium flow. Ann Biomed Eng 32:112-122.
42. Mohr JC, de Pablo JJ, Palecek SP. 2006. 3-D microwell culture of human embryonic stem cells. Biomaterials 27:6032-6042. (Pubitemid 44414976)
43. Moutos FT, Freed LE, Guilak F. 2007. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat Mater 6:162-167. (Pubitemid 46197652)
44. Nelson CM, Bissell MJ. 2005. Modeling dynamic reciprocity: Engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Semin Cancer Biol 15:342-352.
45. Nelson CM, Jean RP, Tan JL, Liu WF, Sniadecki NJ, Spector AA, Chen CS. 2005. Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci USA 102:11594-11599.
46. Nelson CM, Vanduijn MM, Inman JL, Fletcher DA, Bissell MJ. 2006. Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science 314:298-300.
47. Niklason LE, Gao J, Abbott WM, Hirschi KK, Houser S, Marini R, Langer R. 1999. Functional arteries grown in vitro. Science 284:489-493.
48. Oh S, Brammer KS, Li YS, Teng D, Engler AJ, Chien S, Jin S. 2009. Stem cell fate dictated solely by altered nanotube dimension. Proc Natl Acad Sci USA 106:2130-2135.
49. Patwari P, Lee RT. 2008. Mechanical control of tissue morphogenesis. Circ Res 103:234-243.
50. Peerani R, Rao BM, Bauwens C, Yin T, Wood GA, Nagy A, Kumacheva E, Zandstra PW. 2007. Niche-mediated control of human embryonic stem cell self-renewal and differentiation. EMBO J 26:4744-4755. (Pubitemid 350126801)
51. Petersen OW, Rønnov-Jessen L, Howlett AR, Bissell MJ. 1992. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci USA 89:9064-9068.
52. Radisic M, Park H, Shing H, Consi T, Schoen FJ, Langer R, Freed LE, Vunjak-Novakovic G. 2004a. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci USA 101:18129-18134. (Pubitemid 40054085)
53. Radisic M, Yang L, Boublik J, Cohen RJ, Langer R, Freed LE, Vunjak-Novakovic G. 2004b. Medium perfusion enables engineering of compact and contractile cardiac tissue. Am J Physiol Heart Circ Physiol 286:H507-H516. (Pubitemid 38140330)
54. Radisic M, Park H, Chen F, Salazar-Lazzaro JE, Wang Y, Dennis R, Langer R, Freed LE, Vunjak-Novakovic G. 2006. Biomimetic approach to cardiac tissue engineering: Oxygen carriers and channeled scaffolds. Tissue Eng 12:2077-2091. (Pubitemid 44734968)
55. Richardson TP, Peters MC, Ennett AB, Mooney DJ. 2001. Polymeric system for dual growth factor delivery. Nat Biotechnol 19:1029-1034. (Pubitemid 33041886)
56. Roskelley CD, Bissell MJ. 1995. Dynamic reciprocity revisited: A continuous, bidirectional flow of information between cells and the extracellular matrix regulates mammary epithelial cell function. Biochem Cell Biol 73:391-397.
57. Roskelley CD, Desprez PY, Bissell MJ. 1994. Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc Natl Acad Sci USA 91:12378-12382.
58. Roskelley CD, Srebrow A, Bissell MJ. 1995. A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression. Curr Opin Cell Biol 7:736-747.
59. Sarraf C. 2007. Cell and tissue organisation. westminsterresearch.wmin. ac.uk.
60. Sawano A, Takayama S, Matsuda M, Miyawaki A. 2002. Lateral propagation of EGF signaling after local stimulation is dependent on receptor density. Dev Cell 3:245-257.
61. Sikavitsas VI, Bancroft GN, Holtorf HL, Jansen JA, Mikos AG. 2003. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc Natl Acad Sci USA 100:14683-14688.
62. Stocum DL. 2001. Stem cells in regenerative biology and medicine. Wound Repair Regen 9:429-442. (Pubitemid 34266724)
63. Stokes IA, Aronsson DD, Dimock AN, Cortright V, Beck S. 2006. Endochondral growth in growth plates of three species at two anatomical locations modulated by mechanical compression and tension. J Orthop Res 24:1327-1334. (Pubitemid 43870896)
64. Tan JL, Tien J, Pirone DM, Gray DS, Bhadriraju K, Chen CS. 2003. Cells lying on a bed of microneedles: An approach to isolate mechanical force. Proc Natl Acad Sci USA 100:1484-1489. (Pubitemid 36254472)
65. Tandon N, Cannizzaro C, Chao PH, Maidhof R, Marsano A, Au HT, Radisic M, Vunjak-Novakovic G. 2009. Electrical stimulation systems for cardiac tissue engineering. Nat Protoc 4:155-173.
66. Tibbitt MW, Anseth KS. 2009. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng 103:655-663.
67. Uebersax L, Hagenmüller H, Hofmann S, Gruenblatt E, Müller R, Vunjak-Novakovic G, Kaplan DL, Merkle HP, Meinel L. 2006. Effect of scaffold design on bone morphology in vitro. Tissue Eng 12:3417-3429. (Pubitemid 46037165)
68. Vandenburgh H, Del Tatto M, Shansky J, Lemaire J, Chang A, Payumo F, Lee P, Goodyear A, Raven L. 1996. Tissue-engineered skeletal muscle organoids for reversible gene therapy. Hum Gene Ther 7:2195-2200. (Pubitemid 26400744)
69. Vandenburgh H, Shansky J, Benesch-Lee F, Skelly K, Spinazzola JM, Saponjian Y, Tseng BS. 2009. Automated drug screening with contractile muscle tissue engineered from dystrophic myoblasts. FASEB J [Epub ahead of print].
70. Wang SJ, Saadi W, Lin F, Minh-Canh Nguyen C, Li Jeon N. 2004. Differential effects of EGF gradient profiles on MDA-MB-231 breast cancer cell chemotaxis. Exp Cell Res 300:180-189. (Pubitemid 39286227)
71. Wang Y, Kim HJ, Vunjak-Novakovic G, Kaplan DL. 2006. Stem cell-based tissue engineering with silk biomaterials. Biomaterials 27:6064-6082. (Pubitemid 44437574)
72. Wang DA, Varghese S, Sharma B, Strehin I, Fermanian S, Gorham J, Fairbrother DH, Cascio B, Elisseeff JH. 2007. Multifunctional chondroitin sulphate for cartilage tissue-biomaterial integration. Nat Mater 6:385-392. (Pubitemid 46693196)
73. Whitesides GM. 2006. The origins and the future of microfluidics. Nature 442:368-373.
74. Yang L, Soonpaa MH, Adler ED, Roepke TK, Kattman SJ, Kennedy M, Henckaerts E, Bonham K, Abbott GW, Linden RM, Field LJ, Keller GM. 2008. Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 453:524-528. (Pubitemid 351733312)
75. Zagris N. 2001. Extracellular matrix in development of the early embryo. Micron 32:427-438. (Pubitemid 32062531)
76. Zimmermann WH, Schneiderbanger K, Schubert P, Didie M, Munzel F, Heubach JF, Kostin S, Neuhuber WL, Eschenhagen T. 2002. Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90:223-230. (Pubitemid 34627092)
77. Zimmermann WH, Melnychenko I, Wasmeier G, Didié M, Naito H, Nixdorff U, Hess A, Budinsky L, Brune K, Michaelis B, Dhein S, Schwoerer A, Ehmke H, Eschenhagen T. 2006. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 12:452-458.