Engineering strategies to recapitulate epithelial morphogenesis within synthetic three-dimensional extracellular matrix with tunable mechanical properties

Physical Biology

Volumn 8, Issue 2, 2011, Pages

  Miroshnikova, Y A ^a,b   Jorgens, D M ^c   Spirio, L ^d   Auer, M ^c   Sarang Sieminski, A L ^a   Weaver, V M ^b  

^a FRANKLIN W OLIN COLLEGE OF ENGINEERING   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d PuraMatrix/3DM Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDE;

ARTICLE; BIOMECHANICS; CHEMISTRY; EPITHELIUM; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HYDROGEL; MORPHOGENESIS; POROSITY; TISSUE ENGINEERING;

BIOMECHANICS; EPITHELIUM; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMANS; HYDROGELS; MORPHOGENESIS; PEPTIDES; POROSITY; TISSUE ENGINEERING;

EID: 79954540720     PISSN: 14783967     EISSN: 14783975     Source Type: Journal    
DOI: 10.1088/1478-3975/8/2/026013     Document Type: Article

References (94)

1. Ingber D E 2006 Mechanical control of tissue morphogenesis during embryological development Int. J. Dev. Biol. 50 255-66
2. Yu H, Mouw J K and Weaver V M 2010 Forcing form and function: biomechanical regulation of tumor evolution Trends Cell Biol. 21 47-56
3. Engler A J et al 2006 Matrix elasticity directs stem cell lineage specification Cell 126 677-89 (Pubitemid 44233625)
4. Engler A J et al 2008 Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating J. Cell Sci. 121 3794-802
5. Klocke R et al 2003 Arterial stiffness and central blood pressure, as determined by pulse wave analysis, in rheumatoid arthritis Ann. Rheum. Dis. 62 414-8 (Pubitemid 36469730)
6. Flanagan L A et al 2002 Neurite branching on deformable substrates Neuroreport 13 2411-5 (Pubitemid 36143534)
7. Flanagan L A, Ju Y E and Janmey P A 2000 Growth and branching of neuronal processes on deformable substrates Mol. Biol. Cell 11 458
8. Levental K R et al 2009 Matrix crosslinking forces tumor progression by enhancing integrin signaling Cell 139 891-906
9. Paszek M J and Weaver V M 2004 The tension mounts: mechanics meets morphogenesis and malignancy J. Mammary Gland Biol. Neoplasia 9 325-42 (Pubitemid 41149140)
10. Paszek M J et al 2005 Tensional homeostasis and the malignant phenotype Cancer Cell 8 241-54 (Pubitemid 41317594)
11. Pelham R J Jr and Wang Y 1997 Cell locomotion and focal adhesions are regulated by substrate flexibility Proc. Natl Acad. Sci. USA 94 13661-5 (Pubitemid 28009639)
12. Yeung T et al 2005 Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion Cell Motil. Cytoskeleton 60 24-34 (Pubitemid 40066224)
13. Wong J Y et al 2003 Directed movement of vascular smooth muscle cells on gradient-compliant hydrogels Langmuir 19 1908-13
14. Gaudet C et al 2003 Influence of type I collagen surface density on fibroblast spreading, motility, and contractility Biophys. J. 85 3329-35 (Pubitemid 37345821)
15. Heidemann S R and Wirtz D 2004 Towards a regional approach to cell mechanics Trends Cell Biol. 14 160-6 (Pubitemid 38447115)
16. Discher D E, Janmey P and Wang Y L 2005 Tissue cells feel and respond to the stiffness of their substrate Science 310 1139-43 (Pubitemid 41681732)
17. Engler A J et al 2004 Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments J. Cell Biol. 166 877-87 (Pubitemid 39249838)
18. Khatiwala C B et al 2009 ECM compliance regulates osteogenesis by influencing MAPK signaling downstream of RhoA and ROCK J. Bone Miner. Res. 24 886-98
19. Gardel M L et al 2008 Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed J. Cell Biol. 183 999-1005
20. Pasapera A M et al 2010 Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation J. Cell Biol. 188 877-90
21. Gardel M L et al 2010 Mechanical integration of actin and adhesion dynamics in cell migration Annu. Rev. Cell Dev. Biol. 26 315-33
22. Lee J S et al 2006 Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow J. Cell Sci. 119 1760-8 (Pubitemid 43811002)
23. Khatau S B et al 2009 A perinuclear actin cap regulates nuclear shape Proc. Natl Acad. Sci. USA 106 19017-22
24. Lee J S et al 2007 Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration Biophys. J. 93 2542-52 (Pubitemid 47511153)
25. Spencer V A, Xu R and Bissell M J 2010 Gene expression in the third dimension: the ECM-nucleus connection J. Mammary Gland Biol. Neoplasia 15 65-71
26. Boudreau N, Werb Z and Bissell M J 1996 Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle Proc. Natl Acad. Sci. USA 93 3509-13 (Pubitemid 26125651)
27. Wang F et al 2002 Phenotypic reversion or death of cancer cells by altering signaling pathways in three-dimensional contexts J. Natl Cancer Inst. 94 1494-503 (Pubitemid 35243746)
28. Weaver V M et al 1997 Reversion of the malignant phenotype of human breast cells in three- dimensional culture and in vivo by integrin blocking antibodies J. Cell Biol. 137 231-45 (Pubitemid 27167310)
29. Weaver V M et al 1996 The importance of the microenvironment in breast cancer progression: recapitulation of mammary tumorigenesis using a unique human mammary epithelial cell model and a three-dimensional culture assay Biochem. Cell Biol. 74 833-51 (Pubitemid 126733744)
30. Pedersen J A and Swartz M A 2005 Mechanobiology in the third dimension Ann. Biomed. Eng. 33 1469-90 (Pubitemid 41801636)
31. Pampaloni F, Reynaud E G and Stelzer E H 2007 The third dimension bridges the gap between cell culture and live tissue Nat. Rev. Mol. Cell Biol. 8 839-45 (Pubitemid 47462131)
32. Weaver V M et al 2002 Beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium Cancer Cell 2 205-16 (Pubitemid 41043976)
33. Zahir N and Weaver V M 2004 Death in the third dimension: apoptosis regulation and tissue architecture Curr. Opin. Genet. Dev. 14 71-80 (Pubitemid 38167480)
34. Jacks T and Weinberg R A 2002 Taking the study of cancer cell survival to a new dimension Cell 111 923-5 (Pubitemid 36044684)
35. Tse J R and Engler A J 2011 Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate PLoS One 6 e15978
36. Provenzano P P et al 2008 Collagen density promotes mammary tumor initiation and progression BMC Med. 6 11
37. Barcellos-Hoff M H et al 1989 Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane Development 105 223-35 (Pubitemid 19053272)
38. Foster C S et al 1983 Human mammary gland morphogenesis in vitro: the growth and differentiation of normal breast epithelium in collagen gel cultures defined by electron microscopy, monoclonal antibodies, and autoradiography Dev. Biol. 96 197-216
39. Richards J et al 1983 Response of end bud cells from immature rat mammary gland to hormones when cultured in collagen gel Exp. Cell Res. 147 95-109 (Pubitemid 13009630)
40. Emerman J T, Burwen S J and Pitelka D R 1979 Substrate properties influencing ultrastructural differentiation of mammary epithelial cells in culture Tissue Cell 11 109-19 (Pubitemid 9136074)
41. Chalupowicz D G et al 1995 Fibrin II induces endothelial cell capillary tube formation J. Cell Biol. 130 207-15
42. Ghajar C M et al 2008 The effect of matrix density on the regulation of 3D capillary morphogenesis Biophys. J. 94 1930-41
43. Roeder B A et al 2002 Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure J. Biomech. Eng. 124 214-22 (Pubitemid 34407065)
44. Ulrich T A et al 2010 Probing cellular mechanobiology in three-dimensional culture with collagen-agarose matrices Biomaterials 31 1875-84
45. Lutolf M P et al 2003 Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics Proc. Natl Acad. Sci. USA 100 5413-8 (Pubitemid 36542719)
46. Seliktar D et al 2004 MMP-2 sensitive, VEGF-bearing bioactive hydrogels for promotion of vascular healing J. Biomed. Mater. Res. A 68 704-16 (Pubitemid 38263935)
47. Schmedlen R H, Masters K S and West J L 2002 Photocrosslinkable polyvinyl alcohol hydrogels that can be modified with cell adhesion peptides for use in tissue engineering Biomaterials 23 4325-32
48. Mann B K and West J L 2002 Cell adhesion peptides alter smooth muscle cell adhesion, proliferation, migration, and matrix protein synthesis on modified surfaces and in polymer scaffolds J. Biomed. Mater. Res. 60 86-93 (Pubitemid 34126989)
49. Kloxin A M et al 2009 Photodegradable hydrogels for dynamic tuning of physical and chemical properties Science 324 59-63
50. DeForest C A, Polizzotti B D and Anseth K S 2009 Sequential click reactions for synthesizing and patterning three-dimensional cell microenvironments Nat. Mater. 8 659-64
51. Caplan M R et al 2002 Control of self-assembling oligopeptide matrix formation through systematic variation of amino acid sequence Biomaterials 23 219-27 (Pubitemid 33041357)
52. Zhang S et al 1995 Self-complementary oligopeptide matrices support mammalian cell attachment Biomaterials 16 1385-93
53. Sieminski A L et al 2007 The stiffness of three-dimensional ionic self-assembling peptide gels affects the extent of capillary-like network formation Cell Biochem. Biophys. 49 73-83 (Pubitemid 47574999)
54. Gelain F et al 2006 Designer self-assembling peptide nanofiber scaffolds for adult mouse neural stem cell 3-dimensional cultures PLoS One 1 e119
55. Horii A et al 2007 Biological designer self-assembling peptide nanofiber scaffolds significantly enhance osteoblast proliferation, differentiation and 3D migration PLoS One 2 e190
56. Wang S et al 2008 Three-dimensional primary hepatocyte culture in synthetic self-assembling peptide hydrogel Tissue Eng. A 14 227-36
57. Genove E et al 2009 Functionalized self-assembling peptide hydrogel enhance maintenance of hepatocyte activity in vitro J. Cell Mol. Med. 13 3387-97
58. Johnson K R, Leight J L and Weaver V M 2007 Demystifying the effects of a three-dimensional microenvironment in tissue morphogenesis Methods Cell Biol. 83 547-83
59. Zahir N et al 2003 Autocrine laminin-5 ligates alpha6beta4 integrin and activates RAC and NFkappaB to mediate anchorage-independent survival of mammary tumors J. Cell Biol. 163 1397-407 (Pubitemid 38032099)
60. Gudjonsson T et al 2002 Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition J. Cell Sci. 115 39-50 (Pubitemid 34105527)
61. Lopez et al 2011 In situ force mapping of breast tissue transformation Integ. Biol. submitted
62. Fischer R S et al 2009 Local cortical tension by myosin II guides 3D endothelial cell branching Curr. Biol. 19 260-5
63. Zaman M H, Matsudaira P and Lauffenburger D A 2007 Understanding effects of matrix protease and matrix organization on directional persistence and translational speed in three-dimensional cell migration Ann. Biomed. Eng. 35 91-100 (Pubitemid 44916318)
64. Kim H D et al 2008 Epidermal growth factor-induced enhancement of glioblastoma cell migration in 3D arises from an intrinsic increase in speed but an extrinsic matrix- and proteolysis-dependent increase in persistence Mol. Biol. Cell 19 4249-59
65. Provenzano P P et al 2008 Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization Biophys. J. 95 5374-84
66. Cima L G et al 1991 Hepatocyte culture on biodegradable polymeric substrates Biotechnol. Bioeng. 38 145-58
67. Cima L G et al 1991 Tissue engineering by cell transplantation using degradable polymer substrates J. Biomech. Eng. 113 143-51
68. Domansky K et al 2010 Perfused multiwell plate for 3D liver tissue engineering Lab Chip 10 51-8
69. Burdick J A and Anseth K S 2002 Photoencapsulation of osteoblasts in injectable RGD-modified PEG hydrogels for bone tissue engineering Biomaterials 23 4315-23
70. Hoque M E et al 2005 Fabrication using a rapid prototyping system and in vitro characterization of PEG-PCL-PLA scaffolds for tissue engineering J. Biomater. Sci. Polym. Ed. 16 1595-610 (Pubitemid 44717548)
71. Brigham M D et al 2009 Mechanically robust and bioadhesive collagen and photocrosslinkable hyaluronic acid semi-interpenetrating networks Tissue Eng. A 15 1645-53
72. Chung C et al 2009 The influence of degradation characteristics of hyaluronic acid hydrogels on in vitro neocartilage formation by mesenchymal stem cells Biomaterials 30 4287-96
73. Genove E et al 2005 The effect of functionalized self-assembling peptide scaffolds on human aortic endothelial cell function Biomaterials 26 3341-51 (Pubitemid 39647267)
74. Sieminski A L et al 2008 Primary sequence of ionic self-assembling peptide gels affects endothelial cell adhesion and capillary morphogenesis J. Biomed. Mater. Res. A 87 494-504
75. Paszek M J et al 2005 Tensional homeostasis and the malignant phenotype Cancer Cell 8 241-54 (Pubitemid 41317594)
76. Beil M et al 2003 Sphingosylphosphorylcholine regulates keratin network architecture and visco-elastic properties of human cancer cells Nat. Cell Biol. 5 803-11 (Pubitemid 37087168)
77. Colpaert C et al 2001 The presence of a fibrotic focus is an independent predictor of early metastasis in lymph node-negative breast cancer patients Am. J. Surg. Pathol. 25 1557-8 (Pubitemid 33096974)
78. Peyton S R et al 2006 The use of poly(ethylene glycol) hydrogels to investigate the impact of ECM chemistry and mechanics on smooth muscle cells Biomaterials 27 4881-93 (Pubitemid 43866921)
79. Peyton S R et al 2008 The effects of matrix stiffness and RhoA on the phenotypic plasticity of smooth muscle cells in a 3D biosynthetic hydrogel system Biomaterials 29 2597-607
80. Patterson J and Hubbell J A 2010 Enhanced proteolytic degradation of molecularly engineered PEG hydrogels in response to MMP-1 and MMP-2 Biomaterials 31 7836-45
81. Ayala P, Lopez J I and Desai T A 2010 Microtopographical cues in 3D attenuate fibrotic phenotype and extracellular matrix deposition: implications for tissue regeneration Tissue Eng. A 16 2519-27
82. Collins J M et al 2010 Three-dimensional culture with stiff microstructures increases proliferation and slows osteogenic differentiation of human mesenchymal stem cells Small 6 355-60
83. Bernards D A and Desai T A 2010 Nanotemplating of biodegradable polymer membranes for constant-rate drug delivery Adv. Mater. 22 2358-62
84. Choquet D, Felsenfeld D P and Sheetz M P 1997 Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages Cell 88 39-48 (Pubitemid 27180329)
85. Chen C S et al 1997 Geometric control of cell life and death Science 276 1425-8 (Pubitemid 27235413)
86. Provenzano P P et al 2006 Collagen reorganization at the tumor-stromal interface facilitates local invasion BMC Med. 4 38
87. Rhee S and Grinnell F 2007 Fibroblast mechanics in 3D collagen matrices Adv. Drug Deliv. Rev. 59 1299-305 (Pubitemid 350088254)
88. Harley B A et al 2008 Microarchitecture of three-dimensional scaffolds influences cell migration behavior via junction interactions Biophys. J. 95 4013-24
89. Zaman M H et al 2005 Computational model for cell migration in three-dimensional matrices Biophys. J. 89 1389-97 (Pubitemid 41099020)
90. Zaman M H et al 2006 Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis Proc. Natl Acad. Sci. USA 103 10889-94 (Pubitemid 44148391)
91. Butcher D T, Alliston T and Weaver V M 2009 A tense situation: forcing tumour progression Nat. Rev. Cancer 9 108-22
92. Albiges-Rizo C et al 2009 Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions J. Cell Sci. 122 3037-49
93. Stricker J, Falzone T and Gardel M L 2010 Mechanics of the F-actin cytoskeleton J. Biomech. 43 9-14
94. Borghi N et al 2010 Regulation of cell motile behavior by crosstalk between cadherin- and integrin-mediated adhesions Proc. Natl Acad. Sci. USA 107 13324-9