Synthetic matrices reveal contributions of ECM biophysical and biochemical properties to epithelial morphogenesis

Journal of Cell Biology

Volumn 212, Issue 1, 2016, Pages 113-124

  Enemchukwu, Nduka O ^a,b   Cruz Acuña, Ricardo ^b   Bongiorno, Tom ^a,b   Johnson, Christopher T ^b   García, José R ^a,b   Sulchek, Todd ^a,b   García, Andrés J ^a,b  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETIC MATERIAL; MACROGOL; MALEIMIDE; HYDROGEL;

ADHESIVE LIGAND DENSITY; ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BASEMENT MEMBRANE; BIOCHEMISTRY; BIOMECHANICS; BIOMIMETICS; BIOPHYSICS; CELL ADHESION; CELL MATURATION; CELL POLARITY; CELL PROLIFERATION; CONTROLLED STUDY; DENSITY; ELASTICITY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HYDROGEL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SYNTHETIC BIOLOGY; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; DOG; METABOLISM; SYNTHESIS;

ANIMALS; BIOMIMETIC MATERIALS; BIOPHYSICAL PHENOMENA; CELLS, CULTURED; DOGS; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; HYDROGELS; MORPHOGENESIS;

EID: 84978834491     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201506055     Document Type: Article

References (41)

1. Barcellos-Hoff, M.H., J. Aggeler, T.G. Ram, and M.J. Bissell. 1989. Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development. 105:223-235.
2. Beck, J.N., A. Singh, A.R. Rothenberg, J.H. Elisseeff, and A.J. Ewald. 2013. The independent roles of mechanical, structural and adhesion characteristics of 3D hydrogels on the regulation of cancer invasion and dissemination. Biomaterials. 34:9486-9495. http://dx.doi.org/10.1016/j.biomaterials.2013.08.077
3. Bryant, D.M., and K.E. Mostov. 2008. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 9:887-901. http://dx.doi.org/10.1038/nrm2523
4. Canal, T., and N.A. Peppas. 1989. Correlation between mesh size and equilibrium degree of swelling of polymeric networks. J. Biomed. Mater. Res. 23:1183-1193. http://dx.doi.org/10.1002/jbm.820231007
5. Flory, P.J., and J. Rehner. 1943. Statistical mechanics of cross-linked polymer networks II. Swelling. J. Chem. Phys. 11:1183-1193.
6. Ghajar, C.M., X. Chen, J.W. Harris, V. Suresh, C.C. Hughes, N.L. Jeon, A.J. Putnam, and S.C. George. 2008. The effect of matrix density on the regulation of 3-D capillary morphogenesis. Biophys. J. 94:1930-1941. http://dx.doi.org/10.1529/biophysj.107.120774
7. Gill, B.J., D.L. Gibbons, L.C. Roudsari, J.E. Saik, Z.H. Rizvi, J.D. Roybal, J.M. Kurie, and J.L. West. 2012. A synthetic matrix with independently tunable biochemistry and mechanical properties to study epithelial morphogenesis and EMT in a lung adenocarcinoma model. Cancer Res. 72:6013-6023. http://dx.doi.org/10.1158/0008-5472.CAN-12-0895
8. Hoffman, M.P., M. Nomizu, E. Roque, S. Lee, D.W. Jung, Y. Yamada, and H.K. Kleinman. 1998. Laminin-1 and laminin-2 G-domain synthetic peptides bind syndecan-1 and are involved in acinar formation of a human submandibular gland cell line. J. Biol. Chem. 273:28633-28641. http://dx.doi.org/10.1074/jbc.273.44.28633
9. Huebsch, N., P.R. Arany, A.S. Mao, D. Shvartsman, O.A. Ali, S.A. Bencherif, J. Rivera-Feliciano, and D.J. Mooney. 2010. Harnessing tractionmediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 9:518-526. http://dx.doi.org/10.1038/nmat2732
10. Hughes, C.S., L.M. Postovit, and G.A. Lajoie. 2010. Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics. 10:1886-1890. http://dx.doi.org/10.1002/pmic.200900758
11. Khetan, S., M. Guvendiren, W.R. Legant, D.M. Cohen, C.S. Chen, and J.A. Burdick. 2013. Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat. Mater. 12:458-465. http://dx.doi.org/10.1038/nmat3586
12. Klinowska, T.C., J.V. Soriano, G.M. Edwards, J.M. Oliver, A.J. Valentijn, R. Montesano, and C.H. Streuli. 1999. Laminin and beta1 integrins are crucial for normal mammary gland development in the mouse. Dev. Biol. 215:13-32. http://dx.doi.org/10.1006/dbio.1999.9435
13. Kloxin, A.M., A.M. Kasko, C.N. Salinas, and K.S. Anseth. 2009. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science. 324:59-63. http://dx.doi.org/10.1126/science.1169494
14. Koutsopoulos, S., L.D. Unsworth, Y. Nagai, and S. Zhang. 2009. Controlled release of functional proteins through designer self-assembling peptide nanofiber hydrogel scaffold. Proc. Natl. Acad. Sci. USA. 106:4623-4628. http://dx.doi.org/10.1073/pnas.0807506106
15. Levental, K.R., H. Yu, L. Kass, J.N. Lakins, M. Egeblad, J.T. Erler, S.F. Fong, K. Csiszar, A. Giaccia, W. Weninger, et al. 2009. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell. 139:891-906. http://dx.doi.org/10.1016/j.cell.2009.10.027
16. Lubarsky, B., and M.A. Krasnow. 2003. Tube morphogenesis: making and shaping biological tubes. Cell. 112:19-28. http://dx.doi.org/10.1016/S0092-8674(02)01283-7
17. Lutolf, M.P., G.P. Raeber, A.H. Zisch, N. Tirelli, and J.A. Hubbell. 2003. Cellresponsive synthetic hydrogels. Adv. Mater. 15:888-892. http://dx.doi.org/10.1002/adma.200304621
18. Martín-Belmonte, F., W. Yu, A.E. Rodríguez-Fraticelli, A.J. Ewald, Z. Werb, M.A. Alonso, and K. Mostov. 2008. Cell-polarity dynamics controls the mechanism of lumen formation in epithelial morphogenesis. Curr. Biol. 18:507-513. http://dx.doi.org/10.1016/j.cub.2008.02.076
19. McAteer, J.A., A.P. Evan, E.E. Vance, and K.D. Gardner. 1986. MDCK cysts: An in vitro model of epithelial cyst formation and growth. Methods Cell Sci. 10:245-248.
20. Miles, A.J., A.P. Skubitz, L.T. Furcht, and G.B. Fields. 1994. Promotion of cell adhesion by single-stranded and triple-helical peptide models of basement membrane collagen alpha 1(IV)531-543. Evidence for conformationally dependent and conformationally independent type IV collagen cell adhesion sites. J. Biol. Chem. 269:30939-30945.
21. Mroue, R., and M.J. Bissell. 2013. Three-dimensional cultures of mouse mammary epithelial cells. Methods Mol. Biol. 945:221-250. http://dx.doi.org/10.1007/978-1-62703-125-714
22. Nelson, C.M., M.M. Vanduijn, J.L. Inman, D.A. Fletcher, and M.J. Bissell. 2006. Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science. 314:298-300. http://dx.doi.org/10.1126/science.1131000
23. O'Brien, L.E., T.S. Jou, A.L. Pollack, Q. Zhang, S.H. Hansen, P. Yurchenco, and K.E. Mostov. 2001. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3:831-838. http://dx.doi.org/10.1038/ncb0901-831
24. O'Brien, L.E., M.M. Zegers, and K.E. Mostov. 2002. Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat. Rev. Mol. Cell Biol. 3:531-537. http://dx.doi.org/10.1038/nrm859
25. O'Brien, L.E., W. Yu, K. Tang, T.S. Jou, M.M. Zegers, and K.E. Mostov. 2006. Morphological and biochemical analysis of Rac1 in three-dimensional epithelial cell cultures. Methods Enzymol. 406:676-691. http://dx.doi.org/10.1016/S0076-6879(06)06053-8
26. Paszek, M.J., N. Zahir, K.R. Johnson, J.N. Lakins, G.I. Rozenberg, A. Gefen, C.A. Reinhart-King, S.S. Margulies, M. Dembo, D. Boettiger, et al. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell. 8:241-254. http://dx.doi.org/10.1016/j.ccr.2005.08.010
27. Patterson, J., and J.A. Hubbell. 2010. Enhanced proteolytic degradation of molecularly engineered PEG hydrogels in response to MMP-1 and MMP-2. Biomaterials. 31:7836-7845. http://dx.doi.org/10.1016/j.biomaterials.2010.06.061
28. Phelps, E.A., N.O. Enemchukwu, V.F. Fiore, J.C. Sy, N. Murthy, T.A. Sulchek, T.H. Barker, and A.J. García. 2012. Maleimide cross-linked bioactive PEG hydrogel exhibits improved reaction kinetics and cross-linking for cell encapsulation and in situ delivery. Adv. Mater. 24:64-70: 2. http://dx.doi.org/10.1002/adma.201103574
29. Phelps, E.A., D.M. Headen, W.R. Taylor, P.M. Thulé, and A.J. García. 2013. Vasculogenic bio-synthetic hydrogel for enhancement of pancreatic islet engraftment and function in type 1 diabetes. Biomaterials. 34:4602-4611. http://dx.doi.org/10.1016/j.biomaterials.2013.03.012
30. Provenzano, P.P., D.R. Inman, K.W. Eliceiri, and P.J. Keely. 2009. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene. 28:4326-4343. http://dx.doi.org/10.1038/onc.2009.299
31. Raza, A., C.S. Ki, and C.C. Lin. 2013. The influence of matrix properties on growth and morphogenesis of human pancreatic ductal epithelial cells in 3D. Biomaterials. 34:5117-5127. http://dx.doi.org/10.1016/j.biomaterials.2013.03.086
32. Roignot, J., X. Peng, and K. Mostov. 2013. Polarity in mammalian epithelial morphogenesis. Cold Spring Harb. Perspect. Biol. 5:a013789. http://dx.doi.org/10.1101/cshperspect.a013789
33. Salimath, A.S., E.A. Phelps, A.V. Boopathy, P.L. Che, M. Brown, A.J. García, and M.E. Davis. 2012. Dual delivery of hepatocyte and vascular endothelial growth factors via a protease-degradable hydrogel improves cardiac function in rats. PLoS One. 7:e50980. http://dx.doi.org/10.1371/journal.pone.0050980
34. Suzuki, N., H. Nakatsuka, M. Mochizuki, N. Nishi, Y. Kadoya, A. Utani, S. Oishi, N. Fujii, H.K. Kleinman, and M. Nomizu. 2003. Biological activities of homologous loop regions in the laminin alpha chain G domains. J. Biol. Chem. 278:45697-45705. http://dx.doi.org/10.1074/jbc. M304667200
35. Teräväinen, T.P., S.M. Myllymäki, J. Friedrichs, N. Strohmeyer, J.V. Moyano, C. Wu, K.S. Matlin, D.J. Muller, and A. Manninen. 2013. aV-integrins are required for mechanotransduction in MDCK epithelial cells. PLoS One. 8:e71485. http://dx.doi.org/10.1371/journal.pone.0071485
36. Weaver, S.A., B. Wolters, N. Ito, A.M. Woskowicz, K. Kaneko, Y. Shitomi, M. Seiki, and Y. Itoh. 2014. Basal localization of MT1-MMP is essential for epithelial cell morphogenesis in 3D collagen matrix. J. Cell Sci. 127:1203-1213. http://dx.doi.org/10.1242/jcs.135236
37. Weiss, M.S., B.P. Bernabé, A. Shikanov, D.A. Bluver, M.D. Mui, S. Shin, L.J. Broadbelt, and L.D. Shea. 2012. The impact of adhesion peptides within hydrogels on the phenotype and signaling of normal and cancerous mammary epithelial cells. Biomaterials. 33:3548-3559. http://dx.doi.org/10.1016/j.biomaterials.2012.01.055
38. Wozniak, M.A., R. Desai, P.A. Solski, C.J. Der, and P.J. Keely. 2003. ROCKgenerated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J. Cell Biol. 163:583-595. http://dx.doi.org/10.1083/jcb.200305010
39. Yu, W., A. Datta, P. Leroy, L.E. O'Brien, G. Mak, T.S. Jou, K.S. Matlin, K.E. Mostov, and M.M. Zegers. 2005. Beta1-integrin orients epithelial polarity via Rac1 and laminin. Mol. Biol. Cell. 16:433-445. http://dx.doi.org/10.1091/mbc. E04-05-0435
40. Zhang, H., F. Landmann, H. Zahreddine, D. Rodriguez, M. Koch, and M. Labouesse. 2011. A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature. 471:99-103. http://dx.doi.org/10.1038/nature09765
41. Zhang, X., G. Mernaugh, D.H. Yang, L. Gewin, M.B. Srichai, R.C. Harris, J.M. Iturregui, R.D. Nelson, D.E. Kohan, D. Abrahamson, et al. 2009. beta1 integrin is necessary for ureteric bud branching morphogenesis and maintenance of collecting duct structural integrity. Development. 136:3357-3366. http://dx.doi.org/10.1242/dev.036269