Modulating the stem cell niche for tissue regeneration

Nature Biotechnology

Volumn 32, Issue 8, 2014, Pages 795-803

  Lane, Steven W ^a   Williams, David A ^b,c   Watt, Fiona M ^d  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d GUY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MATERIALS; CYTOLOGY; REPAIR; STEM CELLS;

CELL TRANSPLANTATION; DIFFERENTIATED CELLS; ENDOGENOUS STEM CELLS; MICROENVIRONMENTS; REGENERATIVE MEDICINE; SMALL MOLECULES; STEM-CELL NICHES; TISSUE REPAIR;

MOLECULAR BIOLOGY;

ANIMAL; CYTOLOGY; EXTRACELLULAR MATRIX; HUMAN; REGENERATION; STEM CELL;

ANIMALS; EXTRACELLULAR MATRIX; HUMANS; REGENERATION; STEM CELLS;

EID: 84905741637     PISSN: 10870156     EISSN: 15461696     Source Type: Journal    
DOI: 10.1038/nbt.2978     Document Type: Article

References (131)

1. Watt, F.M. & Driskell, R.R. The therapeutic potential of stem cells. Phil. Trans. R. Soc. Lond. B 365, 155-163 (2010).
2. Daley, G.Q. The promise and perils of stem cell therapeutics. Cell Stem Cell 10, 740-749 (2012).
3. Pellegrini, G., Rama, P., Di Rocco, A., Panaras, A. & De Luca, M. Concise review: hurdles in a successful example of limbal stem cell-based regenerative medicine. Stem Cells 32, 26-34 (2014).
4. Oldershaw, R.A. Cell sources for the regeneration of articular cartilage: the past, the horizon and the future. Int. J. Exp. Pathol. 93, 389-400 (2012).
5. Bretzner, F., Gilbert, F., Baylis, F. & Brownstone, R.M. Target populations for first-inhuman embryonic stem cell research in spinal cord injury. Cell Stem Cell 8, 468-475 (2011).
6. Wirth, E. III, Lebkowski, J.S. & Lebacqz, K. Response to Frederic Bretzner et al. "Target populations for first-in-human embryonic stem cell research in spinal cord injury." Cell Stem Cell 8, 476-478 (2011).
7. Ramsden, C.M. et al. Stem cells in retinal regeneration: past, present and future. Development 140, 2576-2585 (2013).
8. Abad, M. et al. Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature 502, 340-345 (2013).
9. Farrar, C.A., Kupiec-Weglinski, J.W. & Sacks, S.H. The innate immune system and transplantation. Cold Spring Harb. Perspect. Med. 3, a015479 (2013).
10. Schofield, R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4, 7-25 (1978). (Pubitemid 8376317)
11. Hall, P.A. & Watt, F.M. Stem cells: the generation and maintenance of cellular diversity. Development 106, 619-633 (1989). (Pubitemid 19221519)
12. Watt, F.M. & Hogan, B.L. Out of Eden: stem cells and their niches. Science 287, 1427-1430 (2000). (Pubitemid 30127126)
13. Morrison, S.J. & Scadden, D.T. The bone marrow niche for haematopoietic stem cells. Nature 505, 327-334 (2014).
14. Fuchs, E. Finding one's niche in the skin. Cell Stem Cell 4, 499-502 (2009).
15. Tan, D.W. & Barker, N. Intestinal stem cells and their defining niche. Curr. Top. Dev. Biol. 107, 77-107 (2014).
16. Barker, N. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nat. Rev. Mol. Cell Biol. 15, 19-33 (2014).
17. van Es, J.H. et al. Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol. 14, 1099-1104 (2012).
18. Sato, T. et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418 (2011).
19. Conover, J.C. & Notti, R.Q. The neural stem cell niche. Cell Tissue Res. 331, 211-224 (2008). (Pubitemid 350265498)
20. Gilbertson, R.J. & Rich, J.N. Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat. Rev. Cancer 7, 733-736 (2007). (Pubitemid 47463683)
21. Simman, R., Priebe, C.J. Jr. & Simon, M. Reconstruction of aplasia cutis congenita of the trunk in a newborn infant using acellular allogenic dermal graft and cultured epithelial autografts. Ann. Plast. Surg. 44, 451-454 (2000). (Pubitemid 30202502)
22. Green, H. The birth of therapy with cultured cells. BioEssays 30, 897-903 (2008).
23. Watt, F.M. & Jensen, K.B. Epidermal stem cell diversity and quiescence. EMBO Mol. Med. 1, 260-267 (2009).
24. Arwert, E.N. et al. Tumor formation initiated by nondividing epidermal cells via an inflammatory infiltrate. Proc. Natl. Acad. Sci. USA 107, 19903-19908 (2010).
25. Driskell, R.R., Clavel, C., Rendl, M. & Watt, F.M. Hair follicle dermal papilla cells at a glance. J. Cell Sci. 124, 1179-1182 (2011).
26. Plikus, M.V. et al. Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451, 340-344 (2008).
27. Festa, E. et al. Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146, 761-771 (2011).
28. Fujiwara, H. et al. The basement membrane of hair follicle stem cells is a muscle cell niche. Cell 144, 577-589 (2011).
29. Driskell, R.R. et al. Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature 504, 277-281 (2013).
30. Lo Celso, C. et al. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 457, 92-96 (2009).
31. 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 121, 1109-1121 (2005). (Pubitemid 40884400)
32. Kunisaki, Y. et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502, 637-643 (2013).
33. Katayama, Y. et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124, 407-421 (2006). (Pubitemid 43121987)
34. Olson, T.S. et al. Megakaryocytes promote murine osteoblastic HSC niche expansion and stem cell engraftment after radioablative conditioning. Blood 121, 5238-5249 (2013).
35. Winkler, I.G. et al. Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 116, 4815-4828 (2010).
36. Fujisaki, J. et al. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 474, 216-219 (2011).
37. Barker, N. et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007 (2007). (Pubitemid 350014593)
38. Rothenberg, M.E. et al. Identification of a cKit(+) colonic crypt base secretory cell that supports Lgr5(+) stem cells in mice. Gastroenterology 142, 1195-1205 (2012).
39. Kai, T. & Spradling, A. An empty Drosophila stem cell niche reactivates the proliferation of ectopic cells. Proc. Natl. Acad. Sci. USA 100, 4633-4638 (2003). (Pubitemid 36457782)
40. Rompolas, P., Mesa, K.R. & Greco, V. Spatial organization within a niche as a determinant of stem-cell fate. Nature 502, 513-518 (2013).
41. Yanger, K. et al. Robust cellular reprogramming occurs spontaneously during liver regeneration. Genes Dev. 27, 719-724 (2013).
42. Tian, H. et al. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478, 255-259 (2011).
43. Watt, F.M., Estrach, S. & Ambler, C.A. Epidermal Notch signalling: differentiation, cancer and adhesion. Curr. Opin. Cell Biol. 20, 171-179 (2008).
44. Ambler, C.A. & Watt, F.M. Adult epidermal Notch activity induces dermal accumulation of T cells and neural crest derivatives through upregulation of jagged 1. Development 137, 3569-3579 (2010).
45. Butler, J.M. et al. Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell 6, 251-264 (2010).
46. Srinivasan, S., Mahowald, A.P. & Fuller, M.T. The receptor tyrosine phosphatase Lar regulates adhesion between Drosophila male germline stem cells and the niche. Development 139, 1381-1390 (2012).
47. Winkler, I.G. et al. Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat. Med. 18, 1651-1657 (2012).
48. Driessen, R.L., Johnston, H.M. & Nilsson, S.K. Membrane-bound stem cell factor is a key regulator in the initial lodgment of stem cells within the endosteal marrow region. Exp. Hematol. 31, 1284-1291 (2003). (Pubitemid 37510034)
49. Toksoz, D. et al. Support of human hematopoiesis in long-term bone marrow cultures by murine stromal cells selectively expressing the membrane-bound and secreted forms of the human homolog of the steel gene product, stem cell factor. Proc. Natl. Acad. Sci. USA 89, 7350-7354 (1992).
50. Schittenhelm, M.M. et al. Dasatinib (BMS-354825), a dual SRC/ABL kinase inhibitor, inhibits the kinase activity of wild-type, juxtamembrane, and activation loop mutant KIT isoforms associated with human malignancies. Cancer Res. 66, 473-481 (2006). (Pubitemid 43166056)
51. Czechowicz, A., Kraft, D., Weissman, I.L. & Bhattacharya, D. Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science 318, 1296-1299 (2007). (Pubitemid 350172893)
52. To, L.B., Levesque, J.P. & Herbert, K.E. How I treat patients who mobilize hematopoietic stem cells poorly. Blood 118, 4530-4540 (2011).
53. Calvi, L.M. et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841-846 (2003). (Pubitemid 37351468)
54. Adams, G.B. et al. Therapeutic targeting of a stem cell niche. Nat. Biotechnol. 25, 238-243 (2007). (Pubitemid 46227124)
55. Lymperi, S. et al. Strontium can increase some osteoblasts without increasing hematopoietic stem cells. Blood 111, 1173-1181 (2008). (Pubitemid 351213398)
56. Greenbaum, A. et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495, 227-230 (2013).
57. Ding, L. & Morrison, S.J. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495, 231-235 (2013).
58. Reya, T. & Clevers, H. Wnt signalling in stem cells and cancer. Nature 434, 843-850 (2005). (Pubitemid 40558990)
59. Silva-Vargas, V. et al. Beta-catenin and Hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells. Dev. Cell 9, 121-131 (2005). (Pubitemid 40903665)
60. Tanimura, S. et al. Hair follicle stem cells provide a functional niche for melanocyte stem cells. Cell Stem Cell 8, 177-187 (2011).
61. Collins, C.A., Kretzschmar, K. & Watt, F.M. Reprogramming adult dermis to a neonatal state through epidermal activation of beta-catenin. Development 138, 5189-5199 (2011).
62. Ito, M. et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447, 316-320 (2007). (Pubitemid 46788832)
63. Garber, K. Drugging the Wnt pathway: problems and progress. J. Natl. Cancer Inst. 101, 548-550 (2009).
64. Willert, K. & Nusse, R. Wnt proteins. Cold Spring Harb. Perspect. Biol. 4, a007864 (2012).
65. Habib, S.J. et al. A localized Wnt signal orients asymmetric stem cell division in vitro. Science 339, 1445-1448 (2013).
66. Alexandre, C., Baena-Lopez, A. & Vincent, J.P. Patterning and growth control by membrane-tethered Wingless. Nature 505, 180-185 (2014).
67. Siggins, S.L. et al. The Hedgehog receptor Patched1 regulates myeloid and lymphoid progenitors by distinct cell-extrinsic mechanisms. Blood 114, 995-1004 (2009).
68. Morris, J.P.T., Wang, S.C. & Hebrok, M. KRAS, Hedgehog, Wnt and the twisted developmental biology of pancreatic ductal adenocarcinoma. Nat. Rev. Cancer 10, 683-695 (2010).
69. Rudin, C.M. et al. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N. Engl. J. Med. 361, 1173-1178 (2009).
70. Tang, J.Y. et al. Inhibiting the hedgehog pathway in patients with the basal-cell nevus syndrome. N. Engl. J. Med. 366, 2180-2188 (2012).
71. Lane, S.W., Scadden, D.T. & Gilliland, D.G. The leukemic stem cell niche: current concepts and therapeutic opportunities. Blood 114, 1150-1157 (2009).
72. Psaila, B. & Lyden, D. The metastatic niche: adapting the foreign soil. Nat. Rev. Cancer 9, 285-293 (2009).
73. Frisch, B.J. et al. Functional inhibition of osteoblastic cells in an in vivo mouse model of myeloid leukemia. Blood 119, 540-550 (2012).
74. Li, W., Li, K., Wei, W. & Ding, S. Chemical approaches to stem cell biology and therapeutics. Cell Stem Cell 13, 270-283 (2013).
75. Hartwell, K.A. et al. Niche-based screening identifies small-molecule inhibitors of leukemia stem cells. Nat. Chem. Biol. 9, 840-848 (2013).
76. Coleman, M.A. et al. Tolerance induction with gene-modified stem cells and immunepreserving conditioning in primed mice: restricting antigen to differentiated antigenpresenting cells permits efficacy. Blood 121, 1049-1058 (2013).
77. Rosenfeld, S.J., Kimball, J., Vining, D. & Young, N.S. Intensive immunosuppression with antithymocyte globulin and cyclosporine as treatment for severe acquired aplastic anemia. Blood 85, 3058-3065 (1995).
78. Jaiswal, S. et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138, 271-285 (2009).
79. Roth, T.L. et al. Transcranial amelioration of inflammation and cell death after brain injury. Nature 505, 223-228 (2014).
80. Gay, D. et al. Fgf9 from dermal gammadelta T cells induces hair follicle neogenesis after wounding. Nat. Med. 19, 916-923 (2013).
81. Sabelström, H. et al. Resident neural stem cells restrict tissue damage and neuronal loss after spinal cord injury in mice. Science 342, 637-640 (2013).
82. Watt, F.M. & Huck, W.T. Role of the extracellular matrix in regulating stem cell fate. Nat. Rev. Mol. Cell Biol. 14, 467-473 (2013).
83. Brizzi, M.F., Tarone, G. & Defilippi, P. Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche. Curr. Opin. Cell Biol. 24, 645-651 (2012).
84. Williams, C.K. et al. Regulation of CXCR4 by the Notch ligand delta-like 4 in endothelial cells. Cancer Res. 68, 1889-1895 (2008). (Pubitemid 351416575)
85. Goodman, S.L. & Picard, M. Integrins as therapeutic targets. Trends Pharmacol. Sci. 33, 405-412 (2012).
86. Byron, A. et al. Anti-integrin monoclonal antibodies. J. Cell Sci. 122, 4009-4011 (2009).
87. E vans, R.D. et al. A tumor-associated beta 1 integrin mutation that abrogates epithelial differentiation control. J. Cell Biol. 160, 589-596 (2003). (Pubitemid 36254396)
88. Swift, J. et al. Nuclear lamin-A scales with tissue stiffness and enhances matrixdirected differentiation. Science 341, 1240104 (2013).
89. Lu, B. & Atala, A. Small molecules and small molecule drugs in regenerative medicine. Drug Discov. Today 19, 801-808. (2013).
90. Ren, J. et al. Melt-electrospun polycaprolactone strontium-substituted bioactive glass scaffolds for bone regeneration. J. Biomed. Mater. Res. A doi:10.1002/jbma.34985 (7 October 2013).
91. Gobaa, S. et al. Artificial niche microarrays for probing single stem cell fate in high throughput. Nat. Methods 8, 949-955 (2011).
92. Ko, I.K., Lee, S.J., Atala, A. & Yoo, J.J. In situ tissue regeneration through host stem cell recruitment. Exp. Mol. Med. 45, e57 (2013).
93. Lampe, K.J. & Heilshorn, S.C. Building stem cell niches from the molecule up through engineered peptide materials. Neurosci. Lett. 519, 138-146 (2012).
94. Uitto, J., Christiano, A.M., McLean, W.H. & McGrath, J.A. Novel molecular therapies for heritable skin disorders. J. Invest. Dermatol. 132, 820-828 (2012).
95. Mavilio, F. et al. Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells. Nat. Med. 12, 1397-1402 (2006). (Pubitemid 44924498)
96. Wong, T. et al. Potential of fibroblast cell therapy for recessive dystrophic epidermolysis bullosa. J. Invest. Dermatol. 128, 2179-2189 (2008).
97. Wagner, J.E. et al. Bone marrow transplantation for recessive dystrophic epidermolysis bullosa. N. Engl. J. Med. 363, 629-639 (2010).
98. Abdul-Wahab, A., Petrof, G. & McGrath, J.A. Bone marrow transplantation in epidermolysis bullosa. Immunotherapy 4, 1859-1867 (2012).
99. Tamai, K. et al. PDGFRalpha-positive cells in bone marrow are mobilized by high mobility group box 1 (HMGB1) to regenerate injured epithelia. Proc. Natl. Acad. Sci. USA 108, 6609-6614 (2011).
100. Pasmooij, A.M., Jonkman, M.F. & Uitto, J. Revertant mosaicism in heritable skin diseases: mechanisms of natural gene therapy. Discov. Med. 14, 167-179 (2012).
101. Lai-Cheong, J.E., McGrath, J.A. & Uitto, J. Revertant mosaicism in skin: natural gene therapy. Trends Mol. Med. 17, 140-148 (2011).
102. Tolar, J. et al. Patient-specific naturally gene-reverted induced pluripotent stem cells in recessive dystrophic epidermolysis bullosa. J. Invest. Dermatol. 134, 1246-1254 (2013).
103. Holst, J. et al. Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells. Nat. Biotechnol. 28, 1123-1128 (2010).
104. Gilbert, P.M. et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078-1081 (2010).
105. Slove, S. et al. Potassium channel openers increase aortic elastic fiber formation and reverse the genetically determined elastin deficit in the BN rat. Hypertension 62, 794-801 (2013).
106. North, T.E. et al. Hematopoietic stem cell development is dependent on blood flow. Cell 137, 736-748 (2009).
107. Shin, J.W. et al. Contractile forces sustain and polarize hematopoiesis from stem and progenitor cells. Cell Stem Cell 14, 81-93 (2014).
108. McBeath, R., Pirone, D.M., Nelson, C.M., Bhadriraju, K. & Chen, C.S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495 (2004). (Pubitemid 38456178)
109. Kilian, K.A., Bugarija, B., Lahn, B.T. & Mrksich, M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Natl. Acad. Sci. USA 107, 4872-4877 (2010).
110. Connelly, J.T., Mishra, A., Gautrot, J.E. & Watt, F.M. Shape-induced terminal differentiation of human epidermal stem cells requires p38 and is regulated by histone acetylation. PLoS ONE 6, e27259 (2011).
111. Kimura, W. & Sadek, H.A. The cardiac hypoxic niche: emerging role of hypoxic microenvironment in cardiac progenitors. Cardiovasc. Diagn. Ther. 2, 278-289 (2012).
112. Muscari, C. et al. Priming adult stem cells by hypoxic pretreatments for applications in regenerative medicine. J. Biomed. Sci. 20, 63 (2013).
113. Speth, J.M., Hoggatt, J., Singh, P. & Pelus, L.M. Pharmacologic increase in HIF1alpha enhances hematopoietic stem and progenitor homing and engraftment. Blood 123, 203-207 (2014).
114. Forristal, C.E. et al. Pharmacologic stabilization of HIF-1alpha increases hematopoietic stem cell quiescence in vivo and accelerates blood recovery after severe irradiation. Blood 121, 759-769 (2013).
115. Shyh-Chang, N., Daley, G.Q. & Cantley, L.C. Stem cell metabolism in tissue development and aging. Development 140, 2535-2547 (2013).
116. Spéder, P., Liu, J. & Brand, A.H. Nutrient control of neural stem cells. Curr. Opin. Cell Biol. 23, 724-729 (2011).
117. Signer, R.A. & Morrison, S.J. Mechanisms that regulate stem cell aging and life span. Cell Stem Cell 12, 152-165 (2013).
118. Janich, P. et al. Human epidermal stem cell function is regulated by circadian oscillations. Cell Stem Cell 13, 745-753 (2013).
119. Belloni, E. et al. Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nat. Genet. 14, 353-356 (1996).
120. Kode, A. et al. Leukaemogenesis induced by an activating beta-catenin mutation in osteoblasts. Nature 506, 240-244 (2014).
121. Ballen, K. et al. Phase II trial of parathyroid hormone after double umbilical cord blood transplantation. Biol. Blood Marrow Transplant. 18, 1851-1858 (2012).
122. Olnes, M.J. et al. Eltrombopag and improved hematopoiesis in refractory aplastic anemia. N. Engl. J. Med. 367, 11-19 (2012).
123. Hayes, H.B. et al. Daily intermittent hypoxia enhances walking after chronic spinal cord injury: a randomized trial. Neurology 82, 104-113 (2014).
124. McKay, W.F., Peckham, S.M. & Badura, J.M. A comprehensive clinical review of recombinant human bone morphogenetic protein-2 (INFUSE Bone Graft). Int. Orthop. 31, 729-734 (2007). (Pubitemid 350160311)
125. Solchaga, L.A., Hee, C.K., Roach, S. & Snel, L.B. Safety of recombinant human platelet-derived growth factor-BB in Augment((R)) Bone Graft. J. Tissue Eng. 3, 2041731412442668 (2012).
126. Wieman, T.J., Smiell, J.M. & Su, Y. Efficacy and safety of a topical gel formulation of recombinant human platelet-derived growth factor-BB (becaplermin) in patients with chronic neuropathic diabetic ulcers. A phase III randomized placebo-controlled double-blind study. Diabetes Care 21, 822-827 (1998). (Pubitemid 28487079)
127. Cianfarani, F. et al. Granulocyte/macrophage colony-stimulating factor treatment of human chronic ulcers promotes angiogenesis associated with de novo vascular endothelial growth factor transcription in the ulcer bed. Br. J. Dermatol. 154, 34-41 (2006). (Pubitemid 43381317)
128. Fleming, H.E. et al. Wnt signaling in the niche enforces hematopoietic stem cell quiescence and is necessary to preserve self-renewal in vivo. Cell Stem Cell 2, 274-283 (2008). (Pubitemid 351298592)
129. Tavazoie, M. et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3, 279-288 (2008).
130. Méndez-Ferrer, S., Lucas, D., Battista, M. & Frenette, P.S. Haematopoietic stem cell release is regulated by circadian oscillations. Nature 452, 442-447 (2008). (Pubitemid 351450836)
131. 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). (Pubitemid 21896743)