Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells

Nature Biotechnology

Volumn 28, Issue 10, 2010, Pages 1123-1128

  Holst, Jeff ^a,b   Watson, Sarah ^a   Lord, Megan S ^c   Eamegdool, Steven S ^d   Bax, Daniel V ^d   Nivison Smith, Lisa B ^d   Kondyurin, Alexey ^d   Ma, Liang ^e   Oberhauser, Andres F ^e   Weiss, Anthony S ^d   Rasko, John E J ^a,b,f  

^a CENTENARY INSTITUTE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e University of Texas Medical Branch School of Medicine   (United States)

^f ROYAL PRINCE ALFRED HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADDITIVE EFFECTS; BIOLOGICAL EFFECTS; CYTOKINES; HEMOPOIETIC CELLS; MATRIX; MECHANICAL SIGNALS; MECHANOTRANSDUCTION; MICROENVIRONMENTS; PHYSICAL EFFECTS; PROGENITOR CELL; TENSEGRITIES; TROPOELASTIN; UNDIFFERENTIATED CELLS;

ANIMAL CELL CULTURE; BIOLOGICAL MATERIALS; CELL CULTURE; ELASTICITY; EXPANSION; SUBSTRATES;

STEM CELLS;

CD150 ANTIGEN; CD48 ANTIGEN; CYTOKINE; INTERLEUKIN 3; INTERLEUKIN 6; MYOSIN ADENOSINE TRIPHOSPHATASE; STEM CELL FACTOR; TROPOELASTIN;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL CULTURE; EX VIVO STUDY; HEMATOPOIETIC STEM CELL; INTRACELLULAR SIGNALING; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHEAR STRESS; STEM CELL EXPANSION;

ANIMALS; CELL PROLIFERATION; COLLAGEN; CROSS-LINKING REAGENTS; ELASTICITY; FETAL BLOOD; FIBRONECTINS; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, INBRED C57BL; MUTANT PROTEINS; QUARTZ CRYSTAL MICROBALANCE TECHNIQUES; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TROPOELASTIN;

EID: 77957940500     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.1687     Document Type: Article

References (54)

1. Sauvageau, G., Iscove, N.N. & Humphries, R.K. In vitro and in vivo expansion of hematopoietic stem cells. Oncogene 23, 7223-7232 (2004).
2. Carter, W.G. & Wayner, E.A. Characterization of the class III collagen receptor, a phosphorylated, transmembrane glycoprotein expressed in nucleated human cells. J. Biol. Chem. 263, 4193-4201 (1988).
3. Ghaffari, S., Dougherty, G.J., Lansdorp, P.M., Eaves, A.C. & Eaves, C.J. Differentiation-associated changes in CD44 isoform expression during normal hematopoiesis and their alteration in chronic myeloid leukemia. Blood 86, 2976-2985 (1995).
4. Williams, D.A., Rios, M., Stephens, C. & Patel, V.P. Fibronectin and VLA-4 in haematopoietic stem cell-microenvironment interactions. Nature 352, 438-441 (1991).
5. Wilson, A. & Trumpp, A. Bone-marrow haematopoietic-stem-cell niches. Nat. Rev. Immunol. 6, 93-106 (2006).
6. Janmey, P.A. & McCulloch, C.A. Cell mechanics: integrating cell responses to mechanical stimuli. Annu. Rev. Biomed. Eng. 9, 1-34 (2007).
7. Ainsworth, C. Cell biology: stretching the imagination. Nature 456, 696-699 (2008).
8. Adamo, L. et al. Biomechanical forces promote embryonic haematopoiesis. Nature 459, 1131-1135 (2009).
9. Engler, A.J., Sen, S., Sweeney, H.L. & Discher, D.E. Matrix elasticity directs stem cell lineage specifcation. Cell 126, 677-689 (2006).
10. Knowles, T.P. et al. Role of intermolecular forces in defning material properties of protein nanofbrils. Science 318, 1900-1903 (2007).
11. Holst, J. et al. Generation of T-cell receptor retrogenic mice. Nat. Protoc. 1, 406-417 (2006).
12. Holst, J., Vignali, K.M., Burton, A.R. & Vignali, D.A. Rapid analysis of T-cell selection in vivo using T cell-receptor retrogenic mice. Nat. Methods 3, 191-197 (2006).
13. Holst, J. et al. Scalable signaling mediated by T cell antigen receptor-CD3 ITAMs ensures effective negative selection and prevents autoimmunity. Nat. Immunol. 9, 658-666 (2008).
14. Kiel, M.J. et al. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109-1121 (2005).
15. Foudi, A. et al. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat. Biotechnol. 27, 84-90 (2009).
16. Gan, B.K., Kondyurin, A. & Bilek, M.M. Comparison of protein surface attachment on untreated and plasma immersion ion implantation treated polystyrene: protein islands and carpet. Langmuir 23, 2741-2746 (2007).
17. Clark, K., Langeslag, M., Figdor, C.G. & van Leeuwen, F.N. Myosin II and mechanotransduction: a balancing act. Trends Cell Biol. 17, 178-186 (2007).
18. Passegué, E., Wagers, A.J., Giuriato, S., Anderson, W.C. & Weissman, I.L. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J. Exp. Med. 202, 1599-1611 (2005).
19. Kiel, M.J. & Morrison, S.J. Uncertainty in the niches that maintain haematopoietic stem cells. Nat. Rev. Immunol. 8, 290-301 (2008).
20. Wang, N., Tytell, J.D. & Ingber, D.E. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75-82 (2009).
21. Discher, D.E., Mooney, D.J. & Zandstra, P.W. Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673-1677 (2009).
22. Even-Ram, S., Artym, V. & Yamada, K.M. Matrix control of stem cell fate. Cell 126, 645-647 (2006).
23. Bax, D.V., Rodgers, U.R., Bilek, M.M. & Weiss, A.S. Cell adhesion to tropoelastin is mediated via the C-terminal GRKRK motif and integrin alphaVbeta3. J. Biol. Chem. 284, 28616-28623 (2009).
24. Broekelmann, T.J. et al. Tropoelastin interacts with cell-surface glycosaminoglycans via its COOH-terminal domain. J. Biol. Chem. 280, 40939-40947 (2005).
25. Mecham, R.P. et al. Elastin binds to a multifunctional 67-kilodalton peripheral membrane protein. Biochemistry 28, 3716-3722 (1989).
26. Rodgers, U.R. & Weiss, A.S. Cellular interactions with elastin. Pathol. Biol. (Paris) 53, 390-398 (2005).
27. Spofford, C.M. & Chilian, W.M. The elastin-laminin receptor functions as a mechanotransducer in vascular smooth muscle. Am. J. Physiol. Heart Circ. Physiol. 280, H1354-H1360 (2001).
28. Spofford, C.M. & Chilian, W.M. Mechanotransduction via the elastin-laminin receptor (ELR) in resistance arteries. J. Biomech. 36, 645-652 (2003).
29. Galbraith, C.G., Yamada, K.M. & Galbraith, J.A. Polymerizing actin fbers position integrins primed to probe for adhesion sites. Science 315, 992-995 (2007).
30. Schwaiger, I., Sattler, C., Hostetter, D.R. & Rief, M. The myosin coiled-coil is a truly elastic protein structure. Nat. Mater. 1, 232-235 (2002).
31. Puttini, S. et al. Gene-mediated restoration of normal myofber elasticity in dystrophic muscles. Mol. Ther. 17, 19-25 (2009).
32. Ji, L., Lim, J. & Danuser, G. Fluctuations of intracellular forces during cell protrusion. Nat. Cell Biol. 10, 1393-1400 (2008).
33. Lutolf, M.P., Gilbert, P.M. & Blau, H.M. Designing materials to direct stem-cell fate. Nature 462, 433-441 (2009).
34. Zovein, A.C. et al. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3, 625-636 (2008).
35. Chen, M.J., Yokomizo, T., Zeigler, B.M., Dzierzak, E. & Speck, N.A. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457, 887-891 (2009).
36. Bertrand, J.Y. et al. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464, 108-111 (2010).
37. Boisset, J.C. et al. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464, 116-120 (2010).
38. Kissa, K. & Herbomel, P. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464, 112-115 (2010).
39. Mithieux, S.M., Rasko, J.E. & Weiss, A.S. Synthetic elastin hydrogels derived from massive elastic assemblies of self-organized human protein monomers. Biomaterials 25, 4921-4927 (2004).
40. Mitragotri, S. & Lahann, J. Physical approaches to biomaterial design. Nat. Mater. 8, 15-23 (2009).
41. Martin, S.L., Vrhovski, B. & Weiss, A.S. Total synthesis and expression in Escherichia coli of a gene encoding human tropoelastin. Gene 154, 159-166 (1995).
42. Wu, W.J., Vrhovski, B. & Weiss, A.S. Glycosaminoglycans mediate the coacervation of human tropoelastin through dominant charge interactions involving lysine side chains. J. Biol. Chem. 274, 21719-21724 (1999).
43. Debelle, L. & Tamburro, A.M. Elastin: molecular description and function. Int. J. Biochem. Cell Biol. 31, 261-272 (1999).
44. Ostuni, A., Lograno, M.D., Gasbarro, A.R., Bisaccia, F. & Tamburro, A.M. Novel properties of peptides derived from the sequence coded by exon 26A of human elastin. Int. J. Biochem. Cell Biol. 34, 130-135 (2002).
45. Wu, W.J. & Weiss, A.S. Defcient coacervation of two forms of human tropoelastin associated with supravalvular aortic stenosis. Eur. J. Biochem. 266, 308-314 (1999).
46. Rodgers, U.R. & Weiss, A.S. Integrin alpha v beta 3 binds a unique non-RGD site near the C-terminus of human tropoelastin. Biochimie 86, 173-178 (2004).
47. Toonkool, P., Jensen, S.A., Maxwell, A.L. & Weiss, A.S. Hydrophobic domains of human tropoelastin interact in a context-dependent manner. J. Biol. Chem. 276, 44575-44580 (2001).
48. Hu, Y. & Smyth, G.K. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J. Immunol. Methods 347, 70-78 (2009).
49. Miller, E., Garcia, T., Hultgren, S. & Oberhauser, A.F. The mechanical properties of E. coli type 1 pili measured by atomic force microscopy techniques. Biophys. J. 91, 3848-3856 (2006).
50. Greene, D.N. et al. Single-molecule force spectroscopy reveals a stepwise unfolding of Caenorhabditis elegans giant protein kinase domains. Biophys. J. 95, 1360-1370 (2008).
51. Florin, E.L. et al. Sensing specific molecular interactions with the atomic force microscope. Biosens. Bioelectron. 10, 895-901 (1995).
52. Lord, M.S. et al. Monitoring cell adhesion on tantalum and oxidised polystyrene using a quartz crystal microbalance with dissipation. Biomaterials 27, 4529-4537 (2006).
53. Mecham, R.P. & Heuser, J.E. The elastic fber. in Cell Biology of Extracellular Matrix (ed. Hay, E.D.) 79-110 (Plenum Press, New York, 1991).
54. Yin, Y. et al. Covalent immobilisation of tropoelastin on a plasma deposited interface for enhancement of endothelialisation on metal surfaces. Biomaterials 30, 1675-1681 (2009).