Engineering the hematopoietic stem cell niche: Frontiers in biomaterial science

Biotechnology Journal

Volumn 10, Issue 10, 2015, Pages 1529-1545

  Choi, Ji Sun ^a   Mahadik, Bhushan P ^a   Harley, Brendan A C ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Biomimetics; Hematopoietic stem cells; Hydrogel and scaffold fabrication; Stem cell fate; Stem cell niche engineering

Indexed keywords

BIOMATERIALS; BIOMIMETICS; BLOOD; BONE; CELLS; CYTOLOGY; SCAFFOLDS (BIOLOGY); STEM CELLS;

BIOMIMETIC APPROACHES; CLINICAL APPLICATION; DIRECTED DIFFERENTIATIONS; HEMATOPOIETIC STEM CELLS; LINEAGE SPECIFICATION; SCAFFOLD FABRICATION; SIGNALING MECHANISMS; STEM-CELL NICHES;

CELL ENGINEERING;

BIOMATERIAL;

BONE MARROW; CELL DIFFERENTIATION; CELL ENGINEERING; CELL INTERACTION; CELL ISOLATION; CELL POPULATION; COCULTURE; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HYDROGEL; IN VITRO STUDY; MICROENVIRONMENT; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; REVIEW; SINGLE CELL ANALYSIS; STEM CELL EXPANSION; STEM CELL NICHE; VASCULAR ENDOTHELIUM; CELL LINEAGE; CYTOLOGY; GENETICS; PROCEDURES; SIGNAL TRANSDUCTION;

CELL DIFFERENTIATION; CELL LINEAGE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS; STEM CELL NICHE;

EID: 84943365159     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201400758     Document Type: Review

References (189)

1. Wang, L. D., Wagers, A. J., Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat. Rev. Mol. Cell Biol. 2011, 12, 643-655.
2. Schofield, R., The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978, 4, 7-25.
3. Haylock, D. N., Nilsson, S. K., Stem cell regulation by the hematopoietic stem cell niche. Cell Cycle 2005, 4, 1353-1355.
4. Tokoyoda, K., Egawa, T., Sugiyama, T., Choi, B. I., Nagasawa, T., Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 2004, 20, 707-718.
5. Purton, L. E., Scadden, D. T., The hematopoietic stem cell niche, StemBook, Cambridge, MA 2008.
6. Adams, G. B., Chabner, K. T., Alley, I. R., Olson, D. P. et al., Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 2006, 439, 599-603.
7. Adams, G. B., Scadden, D. T., The hematopoietic stem cell in its place. Nature immunology 2006, 7, 333-337.
8. Yin, T., Li, L., The stem cell niche in bone. J. Clin. Invest. 2006, 116, 1195-1201.
9. Hines, M., Nielsen, L., Cooper-White, J., The hematopoietic stem cell niche: What are we trying to replicate? J. Chem. Technol. Biotechnol. 2008, 83, 421-443.
10. Ehninger, A., Trumpp, A., The bone marrow stem cell niche grows up: Mesenchymal stem cells and macrophages move in. J. Exp. Med. 2011, 208, 421-428.
11. Bonig, H., Papayannopoulou, T., Hematopoietic stem cell mobilization: Updated conceptual renditions. Leukemia 2013, 27, 24-31.
12. Kopp, H. G., Avecilla, S. T., Hooper, A. T., Rafii, S., The bone marrow vascular niche: Home of HSC differentiation and mobilization. Physiology (Bethesda) 2005, 20, 349-356.
13. Wilson, A., Trumpp, A., Bone-marrow haematopoietic-stem-cell niches. Nat. Rev. Immunol. 2006, 6, 93-106.
14. Morrison, S. J., Scadden, D. T., The bone marrow niche for haematopoietic stem cells. Nature 2014, 505, 327-334.
15. Krause, D. S., Scadden, D. T., Preffer, F. I., The hematopoietic stem cell niche - home for friend and foe? Cytometry Part B 2013, 84, 7-20.
16. Mendez-Ferrer, S., Michurina, T. V., Ferraro, F., Mazloom, A. R. et al., Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010, 466, 829-834.
17. Challen, G. A., Boles, N., Lin, K. K., Goodell, M. A., Mouse hematopoietic stem cell identification and analysis. Cytometry Part A 2009, 75, 14-24.
18. Thomas, E. D., Lochte, H. L. Jr., Lu, W. C., Ferrebee, J. W., Intravenous infusion of bone marrow in patients receiving radiation and chemotherapy. N. Engl. J. Med. 1957, 257, 491-496.
19. Rao, M., Ahrlund-Richter, L., Kaufman, D. S., Concise review: Cord blood banking, transplantation and induced pluripotent stem cell: Success and opportunities. Stem Cells 2012, 30, 55-60.
20. Hong, R., Cooper, M. D., Allan, M. J., Kay, H. E. et al., Immunological restitution in lymphopenic immunological deficiency syndrome. Lancet 1968, 1, 503-506.
21. Cheuk, D. K., Optimal stem cell source for allogeneic stem cell transplantation for hematological malignancies. World J. Transplant. 2013, 3, 99-112.
22. Brunstein, C. G., Gutman, J. A., Weisdorf, D. J., Woolfrey, A. E. et al., Allogeneic hematopoietic cell transplantation for hematologic malignancy: Relative risks and benefits of double umbilical cord blood. Blood 2010, 116, 4693-4699.
23. Copelan, E. A., Hematopoietic stem-cell transplantation. N. Engl. J. Med. 2006, 354, 1813-1826.
24. Spitzer, T. R., Dey, B. R., Chen, Y. B., Attar, E., Ballen, K. K., The expanding frontier of hematopoietic cell transplantation. Cytometry Part B 2012, 82, 271-279.
25. van der Loo, J. C., Ploemacher, R. E., Marrow- and spleen-seeding efficiencies of all murine hematopoietic stem cell subsets are decreased by preincubation with hematopoietic growth factors. Blood 1995, 85, 2598-2606.
26. Liang, Y., Van Zant, G., Szilvassy, S. J., Effects of aging on the homing and engraftment of murine hematopoietic stem and progenitor cells. Blood 2005, 106, 1479-1487.
27. Szilvassy, S. J., Meyerrose, T. E., Grimes, B., Effects of cell cycle activation on the short-term engraftment properties of ex vivo expanded murine hematopoietic cells. Blood 2000, 95, 2829-2837.
28. Wagner, J. E., Barker, J. N., DeFor, T. E., Baker, K. S. et al., Transplantation of unrelated donor umbilical cord blood in 102 patients with malignant and nonmalignant diseases: Influence of CD34 cell dose and HLA disparity on treatment-related mortality and survival. Blood 2002, 100, 1611-1618.
29. Barker, J. N., Umbilical cord blood (UCB) transplantation: An alternative to the use of unrelated volunteer donors? In: ASH Education Program Book, Vol. 2007, 2007, 55-61.
30. Passegue, E., Weisman, I. L., Leukemic stem cells: Where do they come from? Stem Cell Rev. 2005, 1, 181-188.
31. Passegue, E., Jamieson, C. H., Ailles, L. E., Weissman, I. L., Normal and leukemic hematopoiesis: Are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 1 11842-11849.
32. Passegue, E., Hematopoietic stem cells, leukemic stem cells and chronic myelogenous leukemia. Cell Cycle 2005, 4, 266-268.
33. Jude, C. D., Gaudet, J. J., Speck, N. A., Ernst, P., Leukemia and hematopoietic stem cells: Balancing proliferation and quiescence. Cell Cycle 2008, 7, 586-591.
34. Ng, Y., Baert, M. M., de Haas, E. E., Pike-Overzet, K., Staal, F. T., Isolation of human and mouse hematopoietic stem cells, in: Genetic Modification of Hematopoietic Stem Cells, Humana Press 2009, pp. 13-21.
35. Kiel, M. J., Yilmaz, O. H., Iwashita, T., Terhorst, C., Morrison, S. J., SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005, 121, 1109-1121.
36. Purton, L. E., Scadden, D. T., Limiting factors in murine hematopoietic stem cell assays. Cell Stem Cell 2007, 1, 263-270.
37. Perry, J. M., Li, L., Functional assays for hematopoietic stem cell self-renewal, in: Ding, S. (Ed.), Cellular Programming and Reprogramming: Methods and Protocols 2010, pp. 45-54.
38. Kokkaliaris, K. D., Loeffler, D., Schroeder, T., Advances in tracking hematopoiesis at the single-cell level. Curr. Opin. Hematol. 2012, 19, 243-249.
39. Gurkan, U. A., Akkus, O., The mechanical environment of bone marrow: A review. Ann. Biomed. Eng. 2008, 36, 1978-1991.
40. Nombela-Arrieta, C., Pivarnik, G., Winkel, B., Canty, K. J. et al., Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat. Cell. Biol. 2013, 15, 533-543.
41. Xie, Y., Yin, T., Wiegraebe, W., He, X. C. et al., Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 2009, 457, 97-101.
42. Levesque, J. P., Helwani, F. M., Winkler, I. G., The endosteal 'osteoblastic' niche and its role in hematopoietic stem cell homing and mobilization. Leukemia 2010, 24, 1979-1992.
43. Smith, J. N., Calvi, L. M., Concise review: Current concepts in bone marrow microenvironmental regulation of hematopoietic stem and progenitor cells. Stem Cells 2013, 31, 1044-1050.
44. Kunisaki, Y., Bruns, I., Scheiermann, C., Ahmed, J. et al., Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 2013, 502, 637-643.
45. Taichman, R., Reilly, M., Emerson, S., Human osteoblasts support human hematopoietic progenitor cells in vitro bone marrow cultures. Blood 1996, 87, 518-524.
46. Calvi, L. M., Adams, G. B., Weibrecht, K. W., Weber, J. M. et al., Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425, 841-846.
47. Zhang, J., Niu, C., Ye, L., Huang, H. et al., Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003, 425, 836-841.
48. Calvi, L. M., Bromberg, O., Rhee, Y., Weber, J. M. et al., Osteoblastic expansion induced by parathyroid hormone receptor signaling in murine osteocytes is not sufficient to increase hematopoietic stem cells. Blood 2012, 119, 2489-2499.
49. Chitteti, B. R., Cheng, Y.-H., Streicher, D. A., Rodriguez-Rodriguez, S. et al., Osteoblast lineage cells expressing high levels of Runx2 enhance hematopoietic progenitor cell proliferation and function. J. Cell. Biochem. 2010, 111, 284-294.
50. Yoshihara, H., Arai, F., Hosokawa, K., Hagiwara, T. et al., Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 2007, 1, 685-697.
51. Arai, F., Hirao, A., Ohmura, M., Sato, H. et al., Tie2/Angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004, 118, 149-161.
52. Nilsson, S. K., Johnston, H. M., Coverdale, J. A., Spatial localization of transplanted hemopoietic stem cells: Inferences for the localization of stem cell niches. Blood 2001, 97, 2293-2299.
53. Rafii, S., Shapiro, F., Pettengell, R., Ferris, B. et al., Human bone marrow microvascular endothelial cells support long-term proliferation and differentiation of myeloid and megakaryocytic progenitors. Blood 1995, 86, 3353-3363.
54. Butler, J. M., Nolan, D. J., Vertes, E. L., Varnum-Finney, B. et al., Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell 2010, 6, 251-264.
55. Ding, L., Saunders, T. L., Enikolopov, G., Morrison, S. J., Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012, 481, 457-462.
56. Sipkins, D. A., Wei, X. B., Wu, J. W., Runnels, J. M. et al., In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 2005, 435, 969-973.
57. Travlos, G. S., Normal structure, function, and histology of the bone marrow. Toxicologic Pathol. 2006, 34, 548-565.
58. Chute, J. P., Saini, A. A., Chute, D. J., Wells, M. R. et al., Ex vivo culture with human brain endothelial cells increases the SCID-repopulating capacity of adult human bone marrow. Blood 2002, 100, 4433-4439.
59. Avecilla, S. T., Hattori, K., Heissig, B., Tejada, R. et al., Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nature Medicine 2004, 10, 64-71.
60. Heissig, B., Hattori, K., Dias, S., Friedrich, M. et al., Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of Kit-ligand. Cell 2002, 109, 625-637.
61. Anthony, B. A., Link, D. C., Regulation of hematopoietic stem cells by bone marrow stromal cells. Trends Immunol. 2014, 35, 32-37.
62. Mazo, I. B., Massberg, S., von Andrian, U. H., Hematopoietic stem and progenitor cell trafficking. Trends Immunol 2011, 32, 493-503.
63. Massberg, S., Schaerli, P., Knezevic-Maramica, I., Kollnberger, M. et al., Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 2007, 131, 994-1008.
64. Miller, C. L., Eaves, C. J., Expansion in vitro of adult murine hematopoietic stem cells with transplantable lympho-myeloid reconstituting ability. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 13648-13653.
65. Bhatia, M., Bonnet, D., Kapp, U., Wang, J. C. Y. et al., Quantitative analysis reveals expansion of human hematopoietic repopulating cells after short-term ex vivo culture. The J. Exp. Med. 1997, 186, 619-624.
66. Conneally, E., Cashman, J., Petzer, A., Eaves, C., Expansion in vitro of transplantable human cord blood stem cells demonstrated using a quantitative assay of their lympho-myeloid repopulating activity in nonobese diabetic-scid/scid mice. Proc. Natl. Acad. Sci. USA. 1997, 94, 9836-9841.
67. Ueda, T., Tsuji, K., Yoshino, H., Ebihara, Y. et al., Expansion of human NOD/SCID-repopulating cells by stem cell factor, Flk2/Flt3 ligand, thrombopoietin, IL-6, and soluble IL-6 receptor. J. Clin. Invest. 2000, 105, 1013-1021.
68. Magnon, C., Frenette, P. S., Hematopoietic stem cell trafficking, StemBook, Cambridge, MA 2008.
69. Sauvageau, G., Iscove, N. N., Humphries, R. K., In vitro and in vivo expansion of hematopoietic stem cells. Oncogene 2004, 23, 7223-7232.
70. Walasek, M. A., van Os, R., de Haan, G., Hematopoietic stem cell expansion: Challenges and opportunities. Ann. N. Y. Acad. Sci. 2012, 1266, 138-150.
71. Friel, J., Heberlein, C., Geldmacher, M., Ostertag, W., Diverse isoforms of colony-stimulating factor-1 have different effects on the development of stroma-dependent hematopoietic cells. J. Cell. Physiol. 2005, 204, 247-259.
72. Zandstra, P. W., Lauffenburger, D. A., Eaves, C. J., A ligand-receptor signaling threshold model of stem cell differentiation control: A biologically conserved mechanism applicable to hematopoiesis. Blood 2000, 96, 1215-1222.
73. Doran, M. R., Markway, B. D., Aird, I. A., Rowlands, A. S. et al., Surface-bound stem cell factor and the promotion of hematopoietic cell expansion. Biomaterials 2009, 30, 4047-4052.
74. Thoren, L. A., Liuba, K., Bryder, D., Nygren, J. M. et al., Kit regulates maintenance of quiescent hematopoietic stem cells. J. Immunol. 2008, 180, 2045-2053.
75. Casella, I., Feccia, T., Chelucci, C., Samoggia, P. et al., Autocrine-paracrine VEGF loops potentiate the maturation of megakaryocytic precursors through Flt1 receptor. Blood 2003, 101, 1316-1323.
76. Gerber, H. P., Malik, A. K., Solar, G. P., Sherman, D. et al., VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 2002, 417, 954-958.
77. Majka, M., Janowska-Wieczorek, A., Ratajczak, J., Ehrenman, K. et al., Numerous growth factors, cytokines, and chemokines are secreted by human CD34(+) cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/paracrine manner. Blood 2001, 97, 3075-3085.
78. Mayani, H., Little, M. T., Dragowska, W., Thornbury, G., Lansdorp, P. M., Differential effects of the hematopoietic inhibitors MIP-1 alpha, TGF-beta, and TNF-alpha on cytokine-induced proliferation of subpopulations of CD34+ cells purified from cord blood and fetal liver. Exp. Hematol. 1995, 23, 422-427.
79. Doan, P. L., Himburg, H. A., Helms, K., Russell, J. L. et al., Epidermal growth factor regulates hematopoietic regeneration after radiation injury. Nat. Med. 2013, 19, 295-304.
80. Su, R. J., Zhang, X. B., Li, K., Yang, M. et al., Platelet-derived growth factor promotes ex vivo expansion of CD34+ cells from human cord blood and enhances long-term culture-initiating cells, non-obese diabetic/severe combined immunodeficient repopulating cells and formation of adherent cells. Br.J. Haematol. 2002, 117, 735-746.
81. Zhang, C. C., Sadek, H. A., Hypoxia and metabolic properties of hematopoietic stem cells. Antioxid. Redox Signal. 2013, 20, 1891-1901.
82. Suda, T., Takubo, K., Semenza, G. L., Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 2011, 9, 298-310.
83. Hanoun, M., Frenette, Paul S., This niche is a maze; an amazing niche. Cell Stem Cell 2013, 12, 391-392.
84. Ding, L., Morrison, S. J., Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 2013, 495, 231-235.
85. Chen, J., Jacobs-Helber, S. M., Barber, D. L., Sawyer, S. T., Erythropoietin-dependent autocrine secretion of tumor necrosis factor-alpha in hematopoietic cells modulates proliferation via MAP kinase--ERK-1/2 and does not require tyrosine docking sites in the EPO receptor. Exp. Cell Res. 2004, 298, 155-166.
86. Sitnicka, E., Bryder, D., Theilgaard-Monch, K., Buza-Vidas, N. et al., Key role of flt3 ligand in regulation of the common lymphoid progenitor but not in maintenance of the hematopoietic stem cell pool. Immunity 2002, 17, 463-472.
87. Adolfsson, J., Borge, O. J., Bryder, D., Theilgaard-Monch, K. et al., Upregulation of Flt3 expression within the bone marrow Lin(-)Sca1(+)c-kit(+) stem cell compartment is accompanied by loss of self-renewal capacity. Immunity 2001, 15, 659-669.
88. Csaszar, E., Kirouac, Daniel C., Yu, M., Wang, W. et al., Rapid expansion of human hematopoietic stem cells by automated control of inhibitory feedback signaling. Cell Stem Cell 2012, 10, 218-229.
89. Engler, A. J., Sen, S., Sweeney, H. L., Discher, D. E., Matrix elasticity directs stem cell lineage specification. Cell 2006, 126, 677-689.
90. Chowdhury, F., Na, S., Li, D., Poh, Y.-C. et al., Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat. Mater. 2010, 9, 82-88.
91. Dao, M. A., Hashino, K., Kato, I., Nolta, J. A., Adhesion to fibronectin maintains regenerative capacity during ex vivo culture and transduction of human hematopoietic stem and progenitor cells. Blood 1998, 92, 4612-4621.
92. Sagar, B. M. M., Rentala, S., Gopal, P. N. V., Sharma, S., Mukhopadhyay, A., Fibronectin and laminin enhance engraftibility of cultured hematopoietic stem cells. Biochem. Biophys. Res. Commun 2006, 350, 1000-1005.
93. Yokota, T., Oritani, K., Mitsui, H., Aoyama, K. et al., Growth-supporting activities of fibronectin on hematopoietic stem progenitor cells in vitro and in vivo: Structural requirement for fibronectin activities of CS1 and cell-binding domains. Blood 1998, 91, 3263-3272.
94. Nilsson, S. K., Debatis, M. E., Dooner, M. S., Madri, J. A. et al., Immunofluorescence characterization of key extracellular matrix proteins in murine bone marrow in situ. J. Histochem. Cytochem. 1998, 46, 371-377.
95. Çelebi, B., Pineault, N., Mantovani, D., The role of collagen type I on hematopoietic and mesenchymal stem cells expansion and differentiation. Adv. Mater. Res. 2012, 409, 111-116.
96. Siler, U., Seiffert, M., Puch, S., Richards, A. et al., Characterization and functional analysis of laminin isoforms in human bone marrow. Blood 2000, 96, 4194-4203.
97. Klamer, S., Voermans, C., The role of novel and known extracellular matrix and adhesion molecules in the homeostatic and regenerative bone marrow microenvironment. Cell Adh. Migr. 2014, 8, 563-577.
98. Gu, Y. C., Kortesmaa, J., Tryggvason, K., Persson, J. et al., Laminin isoform-specific promotion of adhesion and migration of human bone marrow progenitor cells. Blood 2003, 101, 877-885.
99. Qian, H., Tryggvason, K., Jacobsen, S. E., Ekblom, M., Contribution of alpha6 integrins to hematopoietic stem and progenitor cell homing to bone marrow and collaboration with alpha4 integrins. Blood 2006, 107, 3503-3510.
100. Stier, S., Ko, Y., Forkert, R., Lutz, C. et al., Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J. Exp. Med. 2005, 201, 1781-1791.
101. Nilsson, S. K., Johnston, H. M., Whitty, G. A., Williams, B. et al., Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 2005, 106, 1232-1239.
102. Nishida, C., Kusubata, K., Tashiro, Y., Gritli, I. et al., MT1-MMP plays a critical role in hematopoiesis by regulating HIF-mediated chemokine/cytokine gene transcription within niche cells. Blood 2012, 119, 5405-5416.
103. Greenbaum, A., Hsu, Y.-M. S., Day, R. B., Schuettpelz, L. G. et al., CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 2013, 495, 227-230.
104. Lee, H. J., Li, N., Evans, S. M., Diaz, M. F., Wenzel, P. L., Biomechanical force in blood development: Extrinsic physical cues drive pro-hematopoietic signaling. Differentiation 2013, 86, 92-103.
105. Discher, D. E., Mooney, D. J., Zandstra, P. W., Growth factors, matrices, and forces combine and control stem cells. Science 2009, 324, 1673-1677.
106. Baker, B. M., Chen, C. S., Deconstructing the third dimension: How 3D culture microenvironments alter cellular cues. J. Cell Sci. 2012, 125, 3015-3024.
107. Saha, K., Keung, A. J., Irwin, E. F., Li, Y. et al., Substrate modulus directs neural stem cell behavior. Biophys. J. 2008, 95, 4426-4438.
108. Lee-Thedieck, C., Spatz, J. P., Artificial niches: Biomimetic materials for hematopoietic stem cell culture. Macromol. Rapid Commun. 2012, 33, 1432-1438.
109. Holst, J., Watson, S., Lord, M. S., Eamegdool, S. S. et al., Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells. Nat. Biotechnol. 2010, 28, 1123-1128.
110. Choi, J. S., Harley, B. A. C., The combined influence of substrate elasticity and ligand density on the viability and biophysical properties of hematopoietic stem and progenitor cells. Biomaterials 2012, 33, 4460-4468.
111. Lee-Thedieck, C., Rauch, N., Fiammengo, R., Klein, G., Spatz, J. P., Impact of substrate elasticity on human hematopoietic stem and progenitor cell adhesion and motility. J. Cell Sci. 2012, 125, 3765-3775.
112. Kurth, I., Franke, K., Pompe, T., Bornhauser, M., Werner, C., Hematopoietic stem and progenitor cells in adhesive microcavities. Integr. Biol. 2009, 1, 427-434.
113. Kurth, I., Franke, K., Pompe, T., Bornhauser, M., Werner, C., Extracellular matrix functionalized microcavities to control hematopoietic stem and progenitor cell fate. Macromol. Biosci. 2011, 11, 739-747.
114. Chua, K.-N., Chai, C., Lee, P.-C., Tang, Y.-N. et al., Surface-aminated electrospun nanofibers enhance adhesion and expansion of human umbilical cord blood hematopoietic stem/progenitor cells. Biomaterials 2006, 27, 6043-6051.
115. Altrock, E., Muth, C. A., Klein, G., Spatz, J. P., Lee-Thedieck, C., The significance of integrin ligand nanopatterning on lipid raft clustering in hematopoietic stem cells. Biomaterials 2012, 33, 3107-3118.
116. Muth, C. A., Steinl, C., Klein, G., Lee-Thedieck, C., Regulation of hematopoietic stem cell behavior by the nanostructured presentation of extracellular matrix components. PLoS One 2013, 8, e54778.
117. Lutolf, M. P., Doyonnas, R., Havenstrite, K., Koleckar, K., Blau, H. M., Perturbation of single hematopoietic stem cell fates in artificial niches. Integr. Biol. 2009, 1, 59-69.
118. Lecault, V., Vaninsberghe, M., Sekulovic, S., Knapp, D. J. et al., High-throughput analysis of single hematopoietic stem cell proliferation in microfluidic cell culture arrays. Nat. Methods 2011, 8, 581-586.
119. Kobel, S., Lutolf, M., Fabrication of PEG hydrogel microwell arrays for high-throughput single stem cell culture and analysis, in: Navarro, M., Planell, J. A. (Eds.), Nanotechnology in Regenerative Medicine, Humana Press 2012, pp. 101-112.
120. Verfaillie, C. M., Hematopoietic stem cells for transplantation. Nat. Immunol. 2002, 3, 314-317.
121. Fraser, C. C., Szilvassy, S. J., Eaves, C. J., Humphries, R. K., Proliferation of totipotent hematopoietic stem cells in vitro with retention of long-term competitive in vivo reconstituting ability. Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 1968-1972.
122. Jing, D., Fonseca, A.-V., Alakel, N., Fierro, F. A. et al., Hematopoietic stem cells in co-culture with mesenchymal stromal cells - modeling the niche compartments in vitro. Haematologica 2010, 95, 542-550.
123. Giarratana, M. C., Kobari, L., Lapillonne, H., Chalmers, D. et al., Ex vivo generation of fully mature human red blood cells from hematopoietic stem cells. Nat. Biotechnol. 2005, 23, 69-74.
124. Hatami, J., Andrade, P., Cabral, J., Da Silva, C., Ferreira, F., Effective megakaryocytic differentiation of umbilical cord blood hematopoietic stem/progenitor cells using a two-phase protocol. Cell Journal (Yakhteh) 2013, 15, 44.
125. Dezell, S. A., Ahn, Y.-O., Spanholtz, J., Wang, H. et al., Natural killer cell differentiation from hematopoietic stem cells: A comparative analysis of heparin- and stromal cell-supported methods. Biol. Blood Marrow Transplant. 2012, 18, 536-545.
126. Vieira, P., Cumano, A., Differentiation of B lymphocytes from hematopoietic stem cells, in: Gu, H., Rajewsky, K. (Eds.), B Cell Protocols, Humana Press 2004, pp. 67-76.
127. Taqvi, S., Dixit, L., Roy, K., Biomaterial-based notch signaling for the differentiation of hematopoietic stem cells into T cells. J. Biomed. Mater. Res. Part A 2006, 79, 689-697.
128. Miharada, K., Hiroyama, T., Sudo, K., Nagasawa, T., Nakamura, Y., Efficient enucleation of erythroblasts differentiated in vitro from hematopoietic stem and progenitor cells. Nat. Biotechnol. 2006, 24, 1255-1256.
129. Kirouac, D. C., Madlambayan, G. J., Yu, M., Sykes, E. A. et al., Cell-cell interaction networks regulate blood stem and progenitor cell fate. Mol. Syst. Biol. 2009, 5, 293.
130. Grayson, W. L., Fröhlich, M., Yeager, K., Bhumiratana, S. et al., Engineering anatomically shaped human bone grafts. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 3299-3304.
131. Hollister, S. J., Lin, C. Y., Saito, E., Lin, C. Y. et al., Engineering craniofacial scaffolds. Orthod. Craniofac. Res. 2005, 8, 162-173.
132. Al-Munajjed, A. A., Gleeson, J. P., O'Brien, F. J., Development of a collagen calcium-phosphate scaffold as a novel bone graft substitute. Stud. Health Technol. Inform. 2008, 133, 11-20.
133. Caliari, S. R., Harley, B. A. C., The effect of anisotropic collagen-GAG scaffolds and growth factor supplementation on tendon cell recruitment, alignment, and metabolic activity. Biomaterials 2011, 32, 5330-5340.
134. Williams, J. M., Adewunmi, A., Schek, R. M., Flanagan, C. L. et al., Bone tissue engineering using polycaprolactone scaffolds fabricated via selective laser sintering. Biomaterials 2005, 26, 4817-4827.
135. Nichols, J. E., Cortiella, J., Lee, J., Niles, J. A. et al., In vitro analog of human bone marrow from 3D scaffolds with biomimetic inverted colloidal crystal geometry. Biomaterials 2009, 30, 1071-1079.
136. Taqvi, S., Roy, K., Influence of scaffold physical properties and stromal cell coculture on hematopoietic differentiation of mouse embryonic stem cells. Biomaterials 2006, 27, 6024-6031.
137. Peyton, S. R., Kim, P. D., Ghajar, C. M., Seliktar, D., Putnam, A. J., The effects of matrix stiffness and RhoA on the phenotypic plasticity of smooth muscle cells in a 3-D biosynthetic hydrogel system. Biomaterials 2008, 29, 2597-2607.
138. Murphy, C. M., Haugh, M. G., O'Brien, F. J., The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials 2010, 31, 461-466.
139. Harley, B. A., Kim, H. D., Zaman, M. H., Yannas, I. V. et al., Microarchitecture of three-dimensional scaffolds influences cell migration behavior via junction interactions. Biophys. J. 2008, 95, 4013-4024.
140. Caliari, S. R., Harley, B. A. C., Structural and biochemical modification of a collagen scaffold to selectively enhance MSC tenogenic, chondrogenic, and osteogenic differentiation. Adv. Healthcare Mater. 2014, 3, 1086-1096.
141. Raic, A., Rodling, L., Kalbacher, H., Lee-Thedieck, C., Biomimetic macroporous PEG hydrogels as 3D scaffolds for the multiplication of human hematopoietic stem and progenitor cells. Biomaterials 2014, 35, 929-940.
142. Leisten, I., Kramann, R., Ventura Ferreira, M. S., Bovi, M. et al., 3D co-culture of hematopoietic stem and progenitor cells and mesenchymal stem cells in collagen scaffolds as a model of the hematopoietic niche. Biomaterials 2012, 33, 1736-1747.
143. Thevenot, P. T., Nair, A. M., Shen, J., Lotfi, P. et al., The effect of incorporation of SDF-1alpha into PLGA scaffolds on stem cell recruitment and the inflammatory response. Biomaterials 2010, 31, 3997-4008.
144. Ferreira, M. S., Jahnen-Dechent, W., Labude, N., Bovi, M. et al., Cord blood-hematopoietic stem cell expansion in 3D fibrin scaffolds with stromal support. Biomaterials 2012, 33, 6987-6997.
145. Cook, M. M., Futrega, K., Osiecki, M., Kabiri, M. et al., Micromarrows - three-dimensional coculture of hematopoietic stem cells and mesenchymal stromal cells. Tissue Eng. Part C 2012, 18, 319-328.
146. Walenda, T., Bork, S., Horn, P., Wein, F. et al., Co-culture with mesenchymal stromal cells increases proliferation and maintenance of haematopoietic progenitor cells. J. Cell. Mol. Med. 2010, 14, 337-350.
147. Tan, J., Liu, T., Hou, L., Meng, W. et al., Maintenance and expansion of hematopoietic stem/progenitor cells in biomimetic osteoblast niche. Cytotechnology 2010, 62, 439-448.
148. Spencer, J. A., Ferraro, F., Roussakis, E., Klein, A. et al., Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 2014, 508, 269-273.
149. Roy, S., Tripathy, M., Mathur, N., Jain, A., Mukhopadhyay, A., Hypoxia improves expansion potential of human cord blood-derived hematopoietic stem cells and marrow repopulation efficiency. Eur. J. Haematol. 2012, 88, 396-405.
150. Danet, G. H., Pan, Y., Luongo, J. L., Bonnet, D. A., Simon, M. C., Expansion of human SCID-repopulating cells under hypoxic conditions. J. Clin. Invest. 2003, 112, 126-135.
151. Ivanovic, Z., Dello Sbarba, P., Trimoreau, F., Faucher, J. L., Praloran, V., Primitive human HPCs are better maintained and expanded in vitro at 1 percent oxygen than at 20 percent. Transfusion 2000, 40, 1482-1488.
152. Sharma, M. B., Limaye, L. S., Kale, V. P., Mimicking the functional hematopoietic stem cell niche in vitro: Recapitulation of marrow physiology by hydrogel-based three-dimensional cultures of mesenchymal stromal cells. Haematologica 2012, 97, 651-660.
153. Miyoshi, H., Murao, M., Ohshima, N., Tun, T., Three-dimensional culture of mouse bone marrow cells within a porous polymer scaffold: Effects of oxygen concentration and stromal layer on expansion of haematopoietic progenitor cells. J. Tissue Eng. Regener. Med. 2011, 5, 112-118.
154. Jungreuthmayer, C., Jaasma, M. J., Al-Munajjed, A. A., Zanghellini, J. et al., Deformation simulation of cells seeded on a collagen-GAG scaffold in a flow perfusion bioreactor using a sequential 3D CFD-elastostatics model. Med. Eng. Phys. 2009, 31, 420-427.
155. Jaasma, M. J., O'Brien, F. J., Mechanical stimulation of osteoblasts using steady and dynamic fluid flow. Tissue Eng. Part A 2008, 14, 1213-1223.
156. Braccini, A., Wendt, D., Jaquiery, C., Jakob, M. et al., Three-dimensional perfusion culture of human bone marrow cells and generation of osteoinductive grafts. Stem Cells 2005, 23, 1066-1072.
157. Wendt, D., Marsano, A., Jakob, M., Heberer, M., Martin, I., Oscillating perfusion of cell suspensions through three-dimensional scaffolds enhances cell seeding efficiency and uniformity. Biotechnol. Bioeng. 2003, 84, 205-214.
158. Scherberich, A., Galli, R., Jaquiery, C., Farhadi, J., Martin, I., Three-dimensional perfusion culture of human adipose tissue-derived endothelial and osteoblastic progenitors generates osteogenic constructs with intrinsic vascularization capacity. Stem Cells 2007, 25, 1823-1829.
159. Di Maggio, N., Piccinini, E., Jaworski, M., Trumpp, A. et al., Toward modeling the bone marrow niche using scaffold-based 3D culture systems. Biomaterials 2011, 32, 321-329.
160. Schmelzer, E., Finoli, A., Nettleship, I., Gerlach, J. C., Long-term three-dimensional perfusion culture of human adult bone marrow mononuclear cells in bioreactors. Biotechnol. Bioeng. 2014.
161. Mahadik, B. P., Wheeler, T. D., Skertich, L. J., Kenis, P. J. A., Harley, B. A. C., Microfluidic generation of gradient hydrogels to modulate hematopoietic stem cell culture environment. Adv. Healthcare Mater. 2014, 3, 449-458.
162. Cuchiara, M. L., Horter, K. L., Banda, O. A., West, J. L., Covalent immobilization of stem cell factor and stromal derived factor 1alpha for in vitro culture of hematopoietic progenitor cells. Acta Biomater. 2013, 9, 9258-9269.
163. Fedorovich, N. E., Oudshoorn, M. H., van Geemen, D., Hennink, W. E. et al., The effect of photopolymerization on stem cells embedded in hydrogels. Biomaterials 2009, 30, 344-353.
164. Copley, M. R., Beer, P. A., Eaves, C. J., Hematopoietic stem cell heterogeneity takes center stage. Cell Stem Cell 2012, 10, 690-697.
165. Schroeder, T., Tracking hematopoiesis at the single cell level. Ann. N. Y. Acad. Sci. 2005, 1044, 201-209.
166. Schroeder, T., Hematopoietic stem cell heterogeneity: Subtypes, not unpredictable behavior. Cell Stem Cell 2010, 6, 203-207.
167. Endele, M., Etzrodt, M., Schroeder, T., Instruction of hematopoietic lineage choice by cytokine signaling. Exp. Cell Res. 2014, 329, 207-213.
168. Rieger, M. A., Schroeder, T., Exploring hematopoiesis at single cell resolution. Cells Tissues Organs 2008, 188, 139-149.
169. Rieger, M. A., Hoppe, P. S., Smejkal, B. M., Eitelhuber, A. C., Schroeder, T., Hematopoietic cytokines can instruct lineage choice. Science 2009, 325, 217-218.
170. Eilken, H. M., Nishikawa, S.-I., Schroeder, T., Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 2009, 457, 896-900.
171. Schroeder, T., Long-term single-cell imaging of mammalian stem cells. Nat. Meth. 2011, 8, S30-S35.
172. Kobel, S. A., Burri, O., Griffa, A., Girotra, M. et al., Automated analysis of single stem cells in microfluidic traps. Lab Chip 2012, 12, 2843-2849.
173. Bladergroen, B. A., Siebum, B., Siebers-Vermeulen, K. G., Van Kuppevelt, T. H. et al., In vivo recruitment of hematopoietic cells using stromal cell-derived factor 1 alpha-loaded heparinized three-dimensional collagen scaffolds. Tissue Eng. Part A 2009, 15, 1591-1599.
174. Torisawa, Y. S., Spina, C. S., Mammoto, T., Mammoto, A. et al., Bone marrow-on-a-chip replicates hematopoietic niche physiology in vitro. Nat. Methods 2014, 11, 663-669.
175. Gabrielson, N. P., Desai, A. V., Mahadik, B., Hofmann, M. C. et al., Cell-laden hydrogels in integrated microfluidic devices for long-term cell culture and tubulogenesis assays. Small 2013, 9, 3076-3081.
176. Park, S. Y., Wolfram, P., Canty, K., Harley, B. et al., Focal adhesion kinase regulates the localization and retention of pro-B cells in bone marrow microenvironments. J. Immunol. 2013, 190, 1094-1102.
177. Le, Y., Zhu, B. M., Harley, B., Park, S. Y. et al., SOCS3 protein developmentally regulates the chemokine receptor CXCR4-FAK signaling pathway during B lymphopoiesis. Immunity 2007, 27, 811-823.
178. Pedron, S., Becka, E., Harley, B. A. C., Spatially-gradated hydrogel platform as a three-dimensional engineered tumor microenvironment. Adv. Mater. 2015, 27, 1567-1572.
179. Jamil, M. M. A., Denyer, M. C. T., Youseffi, M., Britland, S. T. et al., Imaging of the cell surface interface using objective coupled widefield surface plasmon microscopy. J. Struct. Biol. 2008, 164, 75-80.
180. Peterson, A. W., Halter, M., Tona, A., Bhadriraju, K., Plant, A. L., Surface plasmon resonance imaging of cells and surface-associated fibronectin. BMC Cell Biol. 2009, 10, 16.
181. Lin, B., Li, P. Y., Cunningham, B. T., A label-free biosensor-based cell attachment assay for characterization of cell surface molecules. Sens. Actuators, B 2006, 114, 559-561.
182. McGuinness, R., Impedance-based cellular assay technologies: Recent advances, future promise. Curr Opin Pharmacol 2007, 7, 535-540.
183. Chen, W., Long, K. D., Yu, H., Tan, Y. et al., Enhanced live cell imaging via photonic crystal enhanced fluorescence microscopy. Analyst 2014, 139, 5954-5963.
184. Chen, W., Long, K. D., Lu, M., Chaudhery, V. et al., Photonic crystal enhanced microscopy for imaging of live cell adhesion. Analyst 2013, 138, 5886-5894.
185. Frisz, J. F., Choi, J. S., Wilson, R. L., Harley, B. A. C., Kraft, M. L., Identifying differentiation stage of individual primary hematopoietic cells from mouse bone marrow by multivariate analysis of TOF-secondary ion mass spectrometry data. Anal. Chem. 2012, 84, 4307-4313.
186. van Galen, P., Kreso, A., Mbong, N., Kent, D. G. et al., The unfolded protein response governs integrity of the haematopoietic stem-cell pool during stress. Nature 2014, 510, 268-272.
187. Weissman, I. L., Shizuru, J. A., The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoimmune diseases. Blood 2008, 112, 3543-3553.
188. Chotinantakul, K., Leeanansaksiri, W., Hematopoietic stem cell development, niches, and signaling pathways. Bone Marrow Res. 2012, 2012, 270425.
189. DeForest, C. A., Polizzotti, B. D., Anseth, K. S., Sequential click reactions for synthesizing and patterning three-dimensional cell microenvironments. Nat. Mater. 2009, 8, 659-664.