Macromolecular crowding directs extracellular matrix organization and mesenchymal stem cell behavior

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Zeiger, Adam S ^a,b   Loe, Felicia C ^b,c   Li, Ran ^a   Raghunath, Michael ^b,c,d   van Vliet, Krystyn J ^a,b  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

SCLEROPROTEIN; FICOLL;

ACTIN FILAMENT; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CELL CULTURE; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOSKELETON; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MACROMOLECULE; MESENCHYMAL STEM CELL; BIOLOGICAL MODEL; CELL CYCLE; CELL DIFFERENTIATION; CELL MOTION; CULTURE TECHNIQUE; IN VITRO STUDY; METABOLISM; METHODOLOGY; ORGANISMAL INTERACTION; PHYSIOLOGY; TISSUE ENGINEERING; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL CYCLE; CELL DIFFERENTIATION; CELL MOVEMENT; EXTRACELLULAR MATRIX; FICOLL; HUMANS; IMMUNOHISTOCHEMISTRY; MACROMOLECULAR SUBSTANCES; MESENCHYMAL STEM CELLS; MICROBIAL INTERACTIONS; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; TISSUE ENGINEERING;

EID: 84861366837     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037904     Document Type: Article

References (55)

1. Oreffo RO, Cooper C, Mason C, Clements M, (2005) Mesenchymal stem cells: lineage, plasticity, and skeletal therapeutic potential. Stem Cell Rev 1: 169-178.
2. Maloney JM, Nikova D, Lautenschlager F, Clarke E, Langer R, et al. (2010) Mesenchymal stem cell mechanics from the attached to the suspended state. Biophys J 99: 2479-2487.
3. Prockop DJ, (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276: 71.
4. Schratt G, Philippar U, Berger J, Schwarz H, Heidenreich O, et al. (2002) Serum response factor is crucial for actin cytoskeletal organization and focal adhesion assembly in embryonic stem cells. The Journal of cell biology 156: 737-750.
5. Discher DE, Janmey P, Wang Y, (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310: 1139.
6. Thompson MT, Berg MC, Tobias IS, Lichter JA, Rubner MF, et al. (2006) Biochemical functionalization of polymeric cell substrata can alter mechanical compliance. Biomacromolecules 7: 1990-1995.
7. Fan VH, Tamama K, Au A, Littrell R, Richardson LB, et al. (2007) Tethered epidermal growth factor provides a survival advantage to mesenchymal stem cells. Stem Cells 25: 1241-1251.
8. Engler AJ, Sen S, Sweeney HL, Discher DE, (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
9. McNamara LE, McMurray RJ, Biggs MJ, Kantawong F, Oreffo RO, et al. (2010) Nanotopographical control of stem cell differentiation. J Tissue Eng 2010: 120623.
10. Yow SZ, Quek CH, Yim EK, Lim CT, Leong KW, (2009) Collagen-based fibrous scaffold for spatial organization of encapsulated and seeded human mesenchymal stem cells. Biomaterials 30: 1133-1142.
11. Ng CP, Hinz B, Swartz MA, (2005) Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. Journal of cell science 118: 4731-4739.
12. Ellis R, (2001) Macromolecular crowding: an important but neglected aspect of the intracellular environment. Current opinion in structural biology 11: 114-119.
13. Price PJ, Gregory EA, (1982) Relationship between in vitro growth promotion and biophysical and biochemical properties of the serum supplement. In Vitro 18: 576-584.
14. Aukland K, Kramer GC, Renkin EM, (1984) Protein concentration of lymph and interstitial fluid in the rat tail. Am J Physiol 247: H74-79.
15. Bates DO, Levick JR, Mortimer PS, (1993) Change in macromolecular composition of interstitial fluid from swollen arms after breast cancer treatment, and its implications. Clin Sci (Lond) 85: 737-746.
16. Wadsworth GR, Oliveiro CJ, (1953) Plasma protein concentration of normal adults living in Singapore. British medical journal 2: 1138-1139.
17. Madden TL, Herzfeld J, (1993) Crowding-induced organization of cytoskeletal elements: I. Spontaneous demixing of cytosolic proteins and model filaments to form filament bundles. Biophys J 65: 1147-1154.
18. Drenckhahn D, Pollard TD, (1986) Elongation of actin filaments is a diffusion-limited reaction at the barbed end and is accelerated by inert macromolecules. J Biol Chem 261: 12754-12758.
19. Minton AP, (1997) Influence of excluded volume upon macromolecular structure and associations in 'crowded' media. Curr Opin Biotechnol 8: 65-69.
20. Chen C, Loe F, Blocki A, Peng Y, Raghunath M, (2011) Applying macromolecular crowding to enhance extracellular matrix deposition and its remodeling in vitro for tissue engineering and cell-based therapies. Adv Drug Deliv Rev 63: 277-290.
21. Folkow B, Gurevich M, Hallback M, Lundgren Y, Weiss L, (1971) The hemodynamic consequences of regional hypotension in spontaneously hypertensive and normotensive rats. Acta Physiol Scand 83: 532-541.
22. Minton AP, (2006) How can biochemical reactions within cells differ from those in test tubes? Journal of cell science 119: 2863-2869.
23. Lareu RR, Harve KS, Raghunath M, (2007) Emulating a crowded intracellular environment in vitro dramatically improves RT-PCR performance. Biochem Biophys Res Commun 363: 171-177.
24. Lareu R, Subramhanya K, Peng Y, Benny P, Chen C, et al. (2007) Collagen matrix deposition is dramatically enhanced in vitro when crowded with charged macromolecules: the biological relevance of the excluded volume effect. FEBS letters 581: 2709-2714.
25. Chebotareva NA, Kurganov BI, Livanova NB, (2004) Biochemical effects of molecular crowding. Biochemistry (Mosc) 69: 1239-1251.
26. Chen CZ, Peng YX, Wang ZB, Fish PV, Kaar JL, et al. (2009) The Scar-in-a-Jar: studying potential antifibrotic compounds from the epigenetic to extracellular level in a single well. Br J Pharmacol 158: 1196-1209.
27. Beil M, Braxmeier H, Fleischer F, Schmidt V, Walther P, (2005) Quantitative analysis of keratin filament networks in scanning electron microscopy images of cancer cells. J Microsc 220: 84-95.
28. Zimmerman SB, Minton AP, (1993) Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 22: 27-65.
29. Lareu RR, Arsianti I, Subramhanya HK, Yanxian P, Raghunath M, (2007) In vitro enhancement of collagen matrix formation and crosslinking for applications in tissue engineering: a preliminary study. Tissue Eng 13: 385-391.
30. Bateman JF, Cole WG, Pillow JJ, Ramshaw JA, (1986) Induction of procollagen processing in fibroblast cultures by neutral polymers. J Biol Chem 261: 4198-4203.
31. Ellis RJ, (2001) Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci 26: 597-604.
32. Onsager L, (1949) The Effects of Shape on the Interaction of Colloidal Particles. Annals of the New York Academy of Sciences 51: 627-659.
33. Kulkarni AM, Chatterjee AP, Schweizer KS, Zukoski CF, (2000) Effects of polyethylene glycol on protein interactions. Journal of Chemical Physics 113: 9863-9873.
34. Lode A, Bernhardt A, Gelinsky M, (2008) Cultivation of human bone marrow stromal cells on three-dimensional scaffolds of mineralized collagen: influence of seeding density on colonization, proliferation and osteogenic differentiation. J Tissue Eng Regen Med 2: 400-407.
35. Rodriguez LG, Wu X, Guan JL, (2005) Wound-healing assay. Methods Mol Biol 294: 23-29.
36. Hocking D, Chang C, (2003) Fibronectin matrix polymerization regulates small airway epithelial cell migration. Am J Physiol Lung Cell Mol Physiol 285: 169-179.
37. Loe F, Zeiger AS, Chen C, Van Vliet KJ, Raghunath M, (2011, in preparation).
38. Laurent TC, (1995) An Early Look at Macromolecular Crowding. Biophysical Chemistry 57: 7-14.
39. Cheung MS, Klimov D, Thirumalai D, (2005) Molecular crowding enhances native state stability and refolding rates of globular proteins. Proc Natl Acad Sci U S A 102: 4753-4758.
40. Homouz D, Stagg L, Wittung-Stafshede P, Cheung MS, (2009) Macromolecular crowding modulates folding mechanism of alpha/beta protein apoflavodoxin. Biophys J 96: 671-680.
41. Rodríguez-Almazán C, Torner FJ, Costas M, Pérez-Montfort R, Gómez-Puyou MTD, et al. (2007) The Stability and Formation of Native Proteins from Unfolded Monomers Is Increased through Interactions with Unrelated Proteins. PLoS ONE 2: e497.
42. Sasahara K, McPhie P, Minton AP, (2003) Effect of dextran on protein stability and conformation attributed to macromolecular crowding. J Mol Biol 326: 1227-1237.
43. Hancock R, (2004) Internal organisation of the nucleus: assembly of compartments by macromolecular crowding and the nuclear matrix model. Biology of the Cell 96: 595-602.
44. Iborra FJ, (2007) Can visco-elastic phase separation, macromolecular crowding and colloidal physics explain nuclear organisation? Theor Biol Med Model 4: 15.
45. Richter K, Nessling M, Lichter P, (2008) Macromolecular crowding and its potential impact on nuclear function. Biochim Biophys Acta 1783: 2100-2107.
46. Ellis RJ, Minton AP, (2003) Cell biology: join the crowd. Nature 425: 27-28.
47. Yeoman D, (1994) Animal Cell Technology- Basic & Applied.
48. Batra J, Xu K, Zhou HX, (2009) Nonadditive effects of mixed crowding on protein stability. Proteins 77: 133-138.
49. Vogel V, Sheetz M, (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7: 265-275.
50. Janes KA, Kelly JR, Gaudet S, Albeck JG, Sorger PK, et al. (2004) Cue-signal-response analysis of TNF-induced apoptosis by partial least squares regression of dynamic multivariate data. J Comput Biol 11: 544-561.
51. Ingber DE, (2008) Can cancer be reversed by engineering the tumor microenvironment? Seminars in cancer biology 18: 356-364.
52. Hutmacher DW, (2010) Biomaterials offer cancer research the third dimension. Nat Mater 9: 90-93.
53. Hu Y, Litwin T, Nagaraja AR, Kwong B, Katz J, et al. (2007) Cytosolic delivery of membrane-impermeable molecules in dendritic cells using pH-responsive core-shell nanoparticles. Nano Lett 7: 3056-3064.
54. Jähne B, Books24x7 Inc. (2005) Digital image processing, 6th revised and extended edition. 6th rev. and ext. ed Berlin; New York Springer.
55. Wilf J, Gladner JA, Minton AP, (1985) Acceleration of fibrin gel formation by unrelated proteins. Thromb Res 37: 681-688.