Regional Fibronectin and Collagen Fibril Co-Assembly Directs Cell Proliferation and Microtissue Morphology

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Sevilla, Carlos A ^a   Dalecki, Diane ^a   Hocking, Denise C ^a,b  

^a University of Rochester   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COLLAGEN FIBRIL; FIBRONECTIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; EXTRACELLULAR MATRIX; FIBROBLAST; HISTOGENESIS; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; MOUSE; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; TISSUE STRUCTURE;

ACTINS; ANIMALS; CELL LINE; CELL PROLIFERATION; COLLAGEN TYPE I; FIBROBLASTS; FIBRONECTINS; HUMANS; MICE; PROTEIN BINDING; RATS;

EID: 84885123952     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077316     Document Type: Article

References (46)

1. Ingber DE, Mow VC, Butler D, Niklason L, Huard J, et al. (2006) Tissue engineering and developmental biology: going biomimetic. Tissue Eng 12: 3265-3283. doi:10.1089/ten.2006.12.3265. PubMed: 17518669.
2. Mironov V, Visconti RP, Kasyanov V, Forgacs G, Drake CJ, et al. (2009) Organ printing: tissue spheroids as building blocks. Biomaterials 30: 2164-2174. doi:10.1016/j.biomaterials.2008.12.084. PubMed: 19176247.
3. Lubarsky B, Krasnow MA, (2003) Tube morphogenesis: making and shaping biological tubes. Cell 112: 19-28. doi:10.1016/S0092-8674(02)01283-7. PubMed: 12526790.
4. Nogawa H, Morita K, Cardoso WV, (1998) Bud formation precedes the appearance of differential cell proliferation during branching morphogenesis of mouse lung epithelium in vitro. Dev Dyn 213: 228-235. doi:10.1002/(SICI)1097-0177(199810)213:2. PubMed: 9786423.
5. Patel VN, Rebustini IT, Hoffman MP, (2006) Salivary gland branching morphogenesis. Differentiation 74: 349-364. doi:10.1111/j.1432-0436.2006.00088.x. PubMed: 16916374.
6. Rossomando E, Alexander S, (1992) Morphogenesis: An Analysis of the Development of Biological Form. Marcel Dekker, INC.
7. Wells JM, Melton DA, (1999) Vertebrate endoderm development. Annu Rev Cell Dev Biol 15: 393-410. doi:10.1146/annurev.cellbio.15.1.393. PubMed: 10611967.
8. Whitesides GM, Grzybowski B, (2002) Self-assembly at all scales. Science 295: 2418-2421. doi:10.1126/science.1070821. PubMed: 11923529.
9. Adams JC, Watt FM, (1993) Regulation of development and differentiation by the extracellular matrix. Development 117: 1183-1198. PubMed: 8404525.
10. Rozario T, DeSimone DW, (2010) The extracellular matrix in development and morphogenesis: a dynamic view. Dev Biol 341: 126-140. doi:10.1016/j.ydbio.2009.10.026. PubMed: 19854168.
11. Rozario T, Dzamba B, Weber GF, Davidson LA, DeSimone DW, (2009) The physical state of fibronectin matrix differentially regulates morphogenetic movements in vivo. Dev Biol 327: 386-398. doi:10.1016/j.ydbio.2008.12.025. PubMed: 19138684.
12. Sakai T, Larsen M, Yamada KM, (2003) Fibronectin requirement in branching morphogenesis. Nature 423: 876-881. doi:10.1038/nature01712. PubMed: 12815434.
13. Shiraishi I, Takamatsu T, Fujita S, (1995) Three-dimensional observation with a confocal scanning laser microscope of fibronectin immunolabeling during cardiac looping in the chick embryo. Anat Embryol (Berl) 191: 183-189. PubMed: 7771682.
14. Rebres RA, McKeown-Longo PJ, Vincent PA, Cho E, Saba TM, (1995) Extracellular matrix incorporation of normal and NEM-alkylated fibronectin: liver and spleen deposition. Am J Physiol 269: G902-G912. PubMed: 8572222.
15. Hocking DC, Titus PA, Sumagin R, Sarelius IH, (2008) Extracellular matrix fibronectin mechanically couples skeletal muscle contraction with local vasodilation. Circ Res 102: 372-379. doi:10.1161/CIRCRESAHA.107.158501. PubMed: 18032733.
16. Sottile J, Hocking DC, Swiatek PJ, (1998) Fibronectin matrix assembly enhances adhesion-dependent cell growth. J Cell Sci 111: 2933-2943. PubMed: 9730985.
17. Hocking DC, Chang CH, (2003) Fibronectin matrix polymerization regulates small airway epithelial cell migration. Am J Physiol Lung Cell Mol Physiol 285: L169-L179. PubMed: 12639845.
18. Hocking DC, Sottile J, Langenbach KJ, (2000) Stimulation of integrin-mediated cell contractility by fibronectin polymerization. J Biol Chem 275: 10673-10682. doi:10.1074/jbc.275.14.10673. PubMed: 10744764.
19. Robinson EE, Foty RA, Corbett SA, (2004) Fibronectin matrix assembly regulates alpha5beta1-mediated cell cohesion. Mol Cell Biol 15: 973-981. PubMed: 14718567.
20. Salmenperä P, Kankuri E, Bizik J, Sirén V, Virtanen I, et al. (2008) Formation and activation of fibroblast spheroids depend on fibronectin-integrin interaction. Exp Cell Res 314: 3444-3452. doi:10.1016/j.yexcr.2008.09.004. PubMed: 18824166.
21. Sevilla CA, Dalecki D, Hocking DC, (2010) Extracellular matrix fibronectin stimulates the self-assembly of microtissues on native collagen gels. Tissue Eng A 16: 3805-3819. doi:10.1089/ten.tea.2010.0316. PubMed: 20673131.
22. Engvall E, Ruoslahti E, Miller EJ, (1978) Affinity of fibronectin to collagens of different genetic types and to fibrinogen. J Exp Med 147: 1584-1595. doi:10.1084/jem.147.6.1584. PubMed: 567240.
23. Sottile J, Hocking DC, (2002) Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol Cell Biol 13: 3546-3559. doi:10.1091/mbc.E02-01-0048. PubMed: 12388756.
24. Velling T, Risteli J, Wennerberg K, Mosher DF, Johansson S, (2002) Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta 1. J Biol Chem 277: 37377-37381. doi:10.1074/jbc.M206286200. PubMed: 12145303.
25. Gildner CD, Lerner AL, Hocking DC, (2004) Fibronectin matrix polymerization increases tensile strength of model tissue. Am J Physiol Heart Circ Physiol 287: H46-H53. doi:10.1152/ajpheart.00859.2003. PubMed: 15001442.
26. Sottile J, Shi F, Rublyevska I, Chiang HY, Lust J, et al. (2007) Fibronectin-dependent collagen I deposition modulates the cell response to fibronectin. Am J Physiol Cell Physiol 293: C1934-C1946. doi:10.1152/ajpcell.00130.2007. PubMed: 17928541.
27. Akiyama S, (2001). urif Fibronectin Current Protoc Cell Biol 10.15.11-10.15: 13.
28. Roy DC, Hocking DC, (2013) Recombinant fibronectin matrix mimetics specify integrin adhesion and extracellular matrix assembly. Tissue Eng A 19: 558-570. doi:10.1089/ten.tea.2012.0257. PubMed: 23020251.
29. Lindmark H, Guss B, (1999) SFS, a novel fibronectin-binding protein from Streptococcus equi, inhibits the binding between fibronectin and collagen. Infect Immun 67: 2383-2388. PubMed: 10225899.
30. North AJ, (2006) Seeing is believing? A beginners' guide to practical pitfalls in image acquisition. J Cell Biol 172: 9-18. doi:10.1083/jcb.200507103. PubMed: 16390995.
31. Plafker K, Macara IG, (2002) Fluorescence resonance energy transfer biosensors that detect Ran conformational changes and a Ran x GDP-importin-beta-RanBP1 complex in vitro and in intact cells. J Biol Chem 277: 30121-30127. doi:10.1074/jbc.M203006200. PubMed: 12034733.
32. Van de Lest CH, Versteeg EM, Veerkamp JH, Van Kuppevelt TH, (1995) Elimination of autofluorescence in immunofluorescence microscopy with digital image processing. J Histochem Cytochem 43: 727-730. doi:10.1177/43.7.7608528. PubMed: 7608528.
33. Freund I, Deutsch M, Sprecher A, (1986) Connective tissue polarity. Optical second-harmonic microscopy, crossed-beam summation, and small-angle scattering in rat-tail tendon. Biophys J 50: 693-712. doi:10.1016/S0006-3495(86)83510-X. PubMed: 3779007.
34. Hansen AE, Kristensen AT, Jørgensen JT, McEvoy FJ, Busk M, et al. (2012) (64)Cu-ATSM and (18)FDG PET uptake and (64)Cu-ATSM autoradiography in spontaneous canine tumors: comparison with pimonidazole hypoxia immunohistochemistry. Radiol Oncol 7: 89. doi:10.1186/1748-717X-7-89. PubMed: 22704363.
35. da Rocha-Azevedo B, Ho CH, Grinnell F, (2012) Fibroblast cluster formation on 3D collagen matrices requires cell contraction dependent fibronectin matrix organization. Exp Cell Res, 319: 546-55. PubMed: 23117111.
36. Guo WH, Frey MT, Burnham NA, Wang YL, (2006) Substrate rigidity regulates the formation and maintenance of tissues. Biophys J 90: 2213-2220. doi:10.1529/biophysj.105.070144. PubMed: 16387786.
37. Gui L, Wojciechowski K, Gildner CD, Nedelkovska H, Hocking DC, (2006) Identification of the heparin-binding determinants within fibronectin repeat III1: role in cell spreading and growth. J Biol Chem 281: 34816-34825. doi:10.1074/jbc.M608611200. PubMed: 16982604.
38. Hocking DC, Kowalski K, (2002) A cryptic fragment from fibronectin's III1 module localizes to lipid rafts and stimulates cell growth and contractility. J Cell Biol 158: 175-184. doi:10.1083/jcb.200112031. PubMed: 12105189.
39. Baneyx G, Baugh L, Vogel V, (2002) Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension. Proc Natl Acad Sci U S A 99: 5139-5143. doi:10.1073/pnas.072650799. PubMed: 11959962.
40. Gao M, Craig D, Lequin O, Campbell ID, Vogel V, et al. (2003) Structure and functional significance of mechanically unfolded fibronectin type III1 intermediates. Proc Natl Acad Sci U S A 100: 14784-14789. doi:10.1073/pnas.2334390100. PubMed: 14657397.
41. Oberhauser AF, Badilla-Fernandez C, Carrion-Vazquez M, Fernandez JM, (2002) The mechanical hierarchies of fibronectin observed with single-molecule AFM. J Mol Biol 319: 433-447. doi:10.1016/S0022-2836(02)00306-6. PubMed: 12051919.
42. Li L, Huang HH, Badilla CL, Fernandez JM, (2005) Mechanical unfolding intermediates observed by single-molecule force spectroscopy in a fibronectin type III module. J Mol Biol 345: 817-826. doi:10.1016/j.jmb.2004.11.021. PubMed: 15588828.
43. Pereira M, Rybarczyk BJ, Odrljin TM, Hocking DC, Sottile J, et al. (2002) The incorporation of fibrinogen into extracellular matrix is dependent on active assembly of a fibronectin matrix. J Cell Sci 115: 609-617. PubMed: 11861767.
44. Shi F, Sottile J, (2008) Caveolin-1-dependent beta1 integrin endocytosis is a critical regulator of fibronectin turnover. J Cell Sci 121: 2360-2371. doi:10.1242/jcs.014977. PubMed: 18577581.
45. Lefort CT, Wojciechowski K, Hocking DC, (2011) N-cadherin cell-cell adhesion complexes are regulated by fibronectin matrix assembly. J Biol Chem 286: 3149-3160. doi:10.1074/jbc.M110.115733. PubMed: 21084302.
46. Chiang HY, Korshunov VA, Serour A, Shi F, Sottile J, (2009) Fibronectin is an important regulator of flow-induced vascular remodeling. Arterioscler Thromb Vasc Biol 29: 1074-1079. doi:10.1161/ATVBAHA.108.181081. PubMed: 19407246.