Current Understanding of the Pathways Involved in Adult Stem and Progenitor Cell Migration for Tissue Homeostasis and Repair

Stem Cell Reviews and Reports

Volumn 12, Issue 4, 2016, Pages 421-437

  Goichberg, Polina ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Adult stem cells; Cell migration; Cell motility; Live imaging; Progenitor cells

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; EPHRIN B1; EPHRIN B3; STROMAL CELL DERIVED FACTOR 1;

BONE MARROW TRANSPLANTATION; CELL COMMUNICATION AND CELL CONTACT; CELL MIGRATION; DEGENERATIVE DISEASE; DOWNSTREAM PROCESSING; EXTRACELLULAR MATRIX; HEALTH CARE PLANNING; HOMEOSTASIS; HUMAN; MUSCULAR DYSTROPHY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; SUBVENTRICULAR ZONE; ADULT; ADULT STEM CELL; CELL MOTION; CYTOLOGY; METABOLISM; PATHOPHYSIOLOGY; PROCEDURES; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION; TRENDS; WOUNDS AND INJURIES;

ADULT; ADULT STEM CELLS; CELL MOVEMENT; HOMEOSTASIS; HUMANS; REGENERATIVE MEDICINE; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; STEM CELLS; WOUNDS AND INJURIES;

EID: 84969791632     PISSN: 15508943     EISSN: 15586804     Source Type: Journal    
DOI: 10.1007/s12015-016-9663-7     Document Type: Review

References (275)

1. Devreotes, P., & Horwitz, A. R. (2015). Signaling networks that regulate cell migration. Cold Spring Harbor Perspectives in Biology, 7(8), a005959.
2. Haeger, A., Wolf, K., Zegers, M. M., & Friedl, P. (2015). Collective cell migration: guidance principles and hierarchies. Trends in Cell Biology, 25(9), 556–566.
3. Lara Rodriguez, L., & Schneider, I. C. (2013). Directed cell migration in multi-cue environments. Integrative Biology: Quantitative Biosciences from Nano to Macro, 5(11), 1306–1323.
4. Shaw, T. J., & Martin, P. (2016). Wound repair: a showcase for cell plasticity and migration. Current Opinion in Cell Biology, 42, 29–37.
5. Visvader, J. E., & Clevers, H. (2016). Tissue-specific designs of stem cell hierarchies. Nature Cell Biology, 18(4), 349–355.
6. Lalli, G. (2014). Extracellular signals controlling neuroblast migration in the postnatal brain. Advances in Experimental Medicine and Biology, 800, 149–180.
7. Magnon, C., Lucas, D., & Frenette, P. S. (2011). Trafficking of stem cells. Methods in Molecular Biology (Clifton, NJ), 750, 3–24.
8. Urao, N., & Ushio-Fukai, M. (2013). Redox regulation of stem/progenitor cells and bone marrow niche. Free Radical Biology & Medicine, 54, 26–39.
9. Xin, T., Greco, V., & Myung, P. (2016). Hardwiring stem cell communication through tissue structure. Cell, 164(6), 1212–1225.
10. Fox, I. J., Daley, G. Q., Goldman, S. A., Huard, J., Kamp, T. J., & Trucco, M. (2014). Stem cell therapy. Use of differentiated pluripotent stem cells as replacement therapy for treating disease. Science, 345(6199), 1247391.
11. Nguyen, P. K., Riegler, J., & Wu, J. C. (2014). Stem cell imaging: from bench to bedside. Cell Stem Cell, 14(4), 431–444.
12. Srijaya, T. C., Ramasamy, T. S., & Kasim, N. H. (2014). Advancing stem cell therapy from bench to bedside: lessons from drug therapies. Journal of Translational Medicine, 12, 243.
13. Bonig, H., & Papayannopoulou, T. (2013). Hematopoietic stem cell mobilization: updated conceptual renditions. Leukemia, 27(1), 24–31.
14. Boulais, P. E., & Frenette, P. S. (2015). Making sense of hematopoietic stem cell niches. Blood, 125(17), 2621–2629.
15. Golan, K., Vagima, Y., Goichberg, P., Gur-Cohen, S., & Lapidot, T. (2011). MT1-MMP and RECK: opposite and essential roles in hematopoietic stem and progenitor cell retention and migration. Journal of Molecular Medicine (Berlin, Germany), 89(12), 1167–1174.
16. Gur-Cohen, S., Kollet, O., Graf, C., Esmon, C.T., Ruf, W., Lapidot, T. (2016). Regulation of long-term repopulating hematopoietic stem cells by EPCR/PAR1 signaling. Annals of the New York Academy of Sciences. doi:10.1111/nyas.13013.
17. Hoggatt, J., Speth, J. M., & Pelus, L. M. (2013). Concise review: sowing the seeds of a fruitful harvest: hematopoietic stem cell mobilization. Stem Cells (Dayton, Ohio), 31(12), 2599–2606.
18. Kollet, O., Canaani, J., Kalinkovich, A., & Lapidot, T. (2012). Regulatory cross talks of bone cells, hematopoietic stem cells and the nervous system maintain hematopoiesis. Inflammation & Allergy: Drug Targets, 11(3), 170–180.
19. Lapid, K., Glait-Santar, C., Gur-Cohen, S., Canaani, J., Kollet, O., & Lapidot, T. (2008). Egress and mobilization of hematopoietic stem and progenitor cells: A dynamic multi-facet process. Cambridge, MA: StemBook.
20. Mazo, I. B., Massberg, S., & von Andrian, U. H. (2011). Hematopoietic stem and progenitor cell trafficking. Trends in Immunology, 32(10), 493–503.
21. Birbrair, A., Frenette, P.S. (2016). Niche heterogeneity in the bone marrow. Annals of the New York Academy of Sciences. doi:10.1111/nyas.13016.
22. Mendelson, A., & Frenette, P. S. (2014). Hematopoietic stem cell niche maintenance during homeostasis and regeneration. Nature Medicine, 20(8), 833–846.
23. Morrison, S. J., & Scadden, D. T. (2014). The bone marrow niche for haematopoietic stem cells. Nature, 505(7483), 327–334.
24. Scadden, D. T. (2014). Nice neighborhood: emerging concepts of the stem cell niche. Cell, 157(1), 41–50.
25. Abkowitz, J. L., Robinson, A. E., Kale, S., Long, M. W., & Chen, J. (2003). Mobilization of hematopoietic stem cells during homeostasis and after cytokine exposure. Blood, 102(4), 1249–1253.
26. Massberg, S., Schaerli, P., Knezevic-Maramica, I., Kollnberger, M., Tubo, N., Moseman, E. A., et al. (2007). Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell, 131(5), 994–1008.
27. Wright, D. E., Wagers, A. J., Gulati, A. P., Johnson, F. L., & Weissman, I. L. (2001). Physiological migration of hematopoietic stem and progenitor cells. Science, 294(5548), 1933–1936.
28. Casanova-Acebes, M., Pitaval, C., Weiss, L. A., Nombela-Arrieta, C., Chevre, R., A-González, N., et al. (2013). Rhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell, 153(5), 1025–1035.
29. Kollet, O., Vagima, Y., D’Uva, G., Golan, K., Canaani, J., Itkin, T., et al. (2013). Physiologic corticosterone oscillations regulate murine hematopoietic stem/progenitor cell proliferation and CXCL12 expression by bone marrow stromal progenitors. Leukemia, 27(10), 2006–2015.
30. Mendez-Ferrer, S., Lucas, D., Battista, M., & Frenette, P. S. (2008). Haematopoietic stem cell release is regulated by circadian oscillations. Nature, 452(7186), 442–447.
31. Kobayashi, H., Suda, T., & Takubo, K. (2016). How hematopoietic stem/progenitors and their niche sense and respond to infectious stress. Experimental Hematology, 44(2), 92–100.
32. Schuettpelz, L. G., & Link, D. C. (2013). Regulation of hematopoietic stem cell activity by inflammation. Frontiers in Immunology, 4, 204.
33. Badami, C. D., Livingston, D. H., Sifri, Z. C., Caputo, F. J., Bonilla, L., Mohr, A. M., & Deitch, E. A. (2007). Hematopoietic progenitor cells mobilize to the site of injury after trauma and hemorrhagic shock in rats. The Journal of Trauma, 63(3), 596–600. discussion 600–592.
34. Dalakas, E., Newsome, P. N., Harrison, D. J., & Plevris, J. N. (2005). Hematopoietic stem cell trafficking in liver injury. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 19(10), 1225–1231.
35. Kollet, O., Shivtiel, S., Chen, Y. Q., Suriawinata, J., Thung, S. N., Dabeva, M. D., et al. (2003). HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34+ stem cell recruitment to the liver. The Journal of Clinical Investigation, 112(2), 160–169.
36. Mocco, J., Afzal, A., Ansari, S., Wolfe, A., Caldwell, K., Connolly, E. S., & Scott, E. W. (2014). SDF1-a facilitates Lin-/Sca1+ cell homing following murine experimental cerebral ischemia. PloS One, 9(1), e85615.
37. Dutta, P., Sager, H. B., Stengel, K. R., Naxerova, K., Courties, G., Saez, B., et al. (2015). Myocardial Infarction Activates CCR2(+) Hematopoietic Stem and Progenitor Cells. Cell Stem Cell, 16(5), 477–487.
38. Klyachkin, Y. M., Karapetyan, A. V., Ratajczak, M. Z., & Abdel-Latif, A. (2014). The role of bioactive lipids in stem cell mobilization and homing: novel therapeutics for myocardial ischemia. BioMed Research International, 2014, 653543.
39. Cipriani, P., Ruscitti, P., & Giacomelli, R. (2015). Stem cell therapies for systemic sclerosis. British Journal of Haematology, 168(3), 328–337.
40. Maeshima, A., Nakasatomi, M., & Nojima, Y. (2014). Regenerative medicine for the kidney: renotropic factors, renal stem/progenitor cells, and stem cell therapy. BioMed Research International, 2014, 595493.
41. Margini, C., Vukotic, R., Brodosi, L., Bernardi, M., & Andreone, P. (2014). Bone marrow derived stem cells for the treatment of end-stage liver disease. World Journal of Gastroenterology, 20(27), 9098–9105.
42. Porada, C. D., Atala, A. J., & Almeida-Porada, G. (2015). The hematopoietic system in the context of regenerative medicine. Methods, 99, 44–61.
43. Barker, N. (2014). Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nature Reviews Molecular Cell Biology, 15(1), 19–33.
44. Clevers, H. (2013). The intestinal crypt, a prototype stem cell compartment. Cell, 154(2), 274–284.
45. Stange, D. E., & Clevers, H. (2013). Concise review: the yin and yang of intestinal (cancer) stem cells and their progenitors. Stem Cells (Dayton, Ohio), 31(11), 2287–2295.
46. Vanuytsel, T., Senger, S., Fasano, A., & Shea-Donohue, T. (2013). Major signaling pathways in intestinal stem cells. Biochimica et Biophysica Acta, 1830(2), 2410–2426.
47. Sancho, R., Cremona, C. A., & Behrens, A. (2015). Stem cell and progenitor fate in the mammalian intestine: Notch and lateral inhibition in homeostasis and disease. EMBO Reports, 16(5), 571–581.
48. Tan, S., & Barker, N. (2015). Epithelial stem cells and intestinal cancer. Seminars in Cancer Biology, 32, 40–53.
49. Vermeulen, L., & Snippert, H. J. (2014). Stem cell dynamics in homeostasis and cancer of the intestine. Nature Reviews Cancer, 14(7), 468–480.
50. Zeuner, A., Todaro, M., Stassi, G., & De Maria, R. (2014). Colorectal cancer stem cells: from the crypt to the clinic. Cell Stem Cell, 15(6), 692–705.
51. Sakthianandeswaren, A., Christie, M., D’Andreti, C., Tsui, C., Jorissen, R. N., Li, S., et al. (2011). PHLDA1 expression marks the putative epithelial stem cells and contributes to intestinal tumorigenesis. Cancer Research, 71(10), 3709–3719.
52. Arwert, E. N., Hoste, E., & Watt, F. M. (2012). Epithelial stem cells, wound healing and cancer. Nature Reviews Cancer, 12(3), 170–180.
53. Blanpain, C., & Fuchs, E. (2014). Stem cell plasticity. Plasticity of epithelial stem cells in tissue regeneration. Science, 344(6189), 1242281.
54. Hsu, Y. C., Li, L., & Fuchs, E. (2014). Emerging interactions between skin stem cells and their niches. Nature Medicine, 20(8), 847–856.
55. Kretzschmar, K., Watt, F.M. (2014). Markers of epidermal stem cell subpopulations in adult mammalian skin. Cold Spring Harbor Perspectives in Medicine. doi:10.1101/cshperspect.a013631.
56. Mesa, K. R., Rompolas, P., & Greco, V. (2015). The dynamic Duo: niche/stem cell interdependency. Stem Cell Reports, 4(6), 961–966.
57. Plikus, M. V., Gay, D. L., Treffeisen, E., Wang, A., Supapannachart, R. J., & Cotsarelis, G. (2012). Epithelial stem cells and implications for wound repair. Seminars in Cell & Developmental Biology, 23(9), 946–953.
58. Rompolas, P., & Greco, V. (2014). Stem cell dynamics in the hair follicle niche. Seminars in Cell & Developmental Biology, 25–26, 34–42.
59. Ito, M., Liu, Y., Yang, Z., Nguyen, J., Liang, F., Morris, R. J., & Cotsarelis, G. (2005). Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nature Medicine, 11(12), 1351–1354.
60. Mascre, G., Dekoninck, S., Drogat, B., Youssef, K. K., Brohee, S., Sotiropoulou, P. A., et al. (2012). Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature, 489(7415), 257–262.
61. Page, M. E., Lombard, P., Ng, F., Gottgens, B., & Jensen, K. B. (2013). The epidermis comprises autonomous compartments maintained by distinct stem cell populations. Cell Stem Cell, 13(4), 471–482.
62. Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W. E., Rendl, M., & Fuchs, E. (2004). Defining the epithelial stem cell niche in skin. Science, 303(5656), 359–363.
63. Wu, X., Shen, Q. T., Oristian, D. S., Lu, C. P., Zheng, Q., Wang, H. W., & Fuchs, E. (2011). Skin stem cells orchestrate directional migration by regulating microtubule-ACF7 connections through GSK3beta. Cell, 144(3), 341–352.
64. Flores, I., Cayuela, M. L., & Blasco, M. A. (2005). Effects of telomerase and telomere length on epidermal stem cell behavior. Science, 309(5738), 1253–1256.
65. Chou, W. C., Takeo, M., Rabbani, P., Hu, H., Lee, W., Chung, Y. R., et al. (2013). Direct migration of follicular melanocyte stem cells to the epidermis after wounding or UVB irradiation is dependent on Mc1r signaling. Nature Medicine, 19(7), 924–929.
66. Almada, A. E., & Wagers, A. J. (2016). Molecular circuitry of stem cell fate in skeletal muscle regeneration, ageing and disease. Nature Reviews Molecular Cell Biology, 17(5), 267–279.
67. Blau, H. M., Cosgrove, B. D., & Ho, A. T. (2015). The central role of muscle stem cells in regenerative failure with aging. Nature Medicine, 21(8), 854–862.
68. Brack, A. S., & Munoz-Canoves, P. (2015). The ins and outs of muscle stem cell aging. Skeletal Muscle, 6, 1.
69. Cerletti, M., Shadrach, J. L., Jurga, S., Sherwood, R., & Wagers, A. J. (2008). Regulation and function of skeletal muscle stem cells. Cold Spring Harbor Symposia on Quantitative Biology, 73, 317–322.
70. Conboy, I. M., & Rando, T. A. (2005). Aging, stem cells and tissue regeneration: lessons from muscle. Cell Cycle, 4(3), 407–410.
71. Dumont, N. A., Bentzinger, C. F., Sincennes, M. C., & Rudnicki, M. A. (2015). Satellite cells and skeletal muscle regeneration. Comprehensive Physiology, 5(3), 1027–1059.
72. Sincennes, M. C., Brun, C. E., & Rudnicki, M. A. (2016). Concise review: epigenetic regulation of myogenesis in health and disease. Stem Cells Translational Medicine, 5(3), 282–290.
73. Tierney, M.T., Sacco, A. (2016). Satellite cell heterogeneity in skeletal muscle homeostasis. Trends in Cell Biology. doi:10.1016/j.tcb.2016.02.004.
74. Webster, M. T., Manor, U., Lippincott-Schwartz, J., & Fan, C. M. (2016). Intravital imaging reveals ghost fibers as architectural units guiding myogenic progenitors during regeneration. Cell Stem Cell, 18(2), 243–252.
75. Neuhaus, P., Oustanina, S., Loch, T., Kruger, M., Bober, E., Dono, R., et al. (2003). Reduced mobility of fibroblast growth factor (FGF)-deficient myoblasts might contribute to dystrophic changes in the musculature of FGF2/FGF6/mdx triple-mutant mice. Molecular and Cellular Biology, 23(17), 6037–6048.
76. Collins-Hooper, H., Woolley, T. E., Dyson, L., Patel, A., Potter, P., Baker, R. E., et al. (2012). Age-related changes in speed and mechanism of adult skeletal muscle stem cell migration. Stem Cells (Dayton, Ohio), 30(6), 1182–1195.
77. Bond, A. M., Ming, G. L., & Song, H. (2015). Adult mammalian neural stem cells and neurogenesis: five decades later. Cell Stem Cell, 17(4), 385–395.
78. Capilla-Gonzalez, V., Lavell, E., Quinones-Hinojosa, A., & Guerrero-Cazares, H. (2015). Regulation of subventricular zone-derived cells migration in the adult brain. Advances in Experimental Medicine and Biology, 853, 1–21.
79. De Filippis, L., & Binda, E. (2012). Concise review: self-renewal in the central nervous system: neural stem cells from embryo to adult. Stem Cells Translational Medicine, 1(4), 298–308.
80. Lim, D. A., & Alvarez-Buylla, A. (2014). Adult neural stem cells stake their ground. Trends in Neurosciences, 37(10), 563–571.
81. Maki, T., Liang, A. C., Miyamoto, N., Lo, E. H., & Arai, K. (2013). Mechanisms of oligodendrocyte regeneration from ventricular-subventricular zone-derived progenitor cells in white matter diseases. Frontiers in Cellular Neuroscience, 7, 275.
82. Merino, J. J., Bellver-Landete, V., Oset-Gasque, M. J., & Cubelos, B. (2014). Review: CXCR4/CXCR7 molecular involvement in neuronal and neural progenitor migration: focus in CNS repair. Journal of Cellular Physiology, 230(1), 27–42.
83. Ibrahim, S., Hu, W., Wang, X., Gao, X., He, C., & Chen, J. (2016). Traumatic brain injury causes aberrant migration of adult-born neurons in the hippocampus. Scientific Reports, 6, 21793.
84. Capilla-Gonzalez, V., Herranz-Perez, V., & Garcia-Verdugo, J. M. (2015). The aged brain: genesis and fate of residual progenitor cells in the subventricular zone. Frontiers in Cellular Neuroscience, 9, 365.
85. Aboody, K. S., Brown, A., Rainov, N. G., Bower, K. A., Liu, S., Yang, W., et al. (2000). Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proceedings of the National Academy of Sciences of the United States of America, 97(23), 12846–12851.
86. Carney, B. J., & Shah, K. (2011). Migration and fate of therapeutic stem cells in different brain disease models. Neuroscience, 197, 37–47.
87. Vishwakarma, S. K., Bardia, A., Tiwari, S. K., Paspala, S. A., & Khan, A. A. (2014). Current concept in neural regeneration research: NSCs isolation, characterization and transplantation in various neurodegenerative diseases and stroke: A review. Journal of Advanced Research, 5(3), 277–294.
88. Chou, C. H., Fan, H. C., & Hueng, D. Y. (2015). Potential of neural stem cell-based therapy for Parkinson’s disease. Parkinson’s Disease, 2015, 571475.
89. Dunnett, S. B., & Rosser, A. E. (2014). Challenges for taking primary and stem cells into clinical neurotransplantation trials for neurodegenerative disease. Neurobiology of Disease, 61, 79–89.
90. Goldman, S. A. (2016). Stem and progenitor cell-based therapy of the central nervous system: hopes, hype, and wishful thinking. Cell Stem Cell, 18(2), 174–188.
91. Bentzinger, C. F., Wang, Y. X., Dumont, N. A., & Rudnicki, M. A. (2013). Cellular dynamics in the muscle satellite cell niche. EMBO Reports, 14(12), 1062–1072.
92. Bjornsson, C. S., Apostolopoulou, M., Tian, Y., & Temple, S. (2015). It takes a village: constructing the neurogenic niche. Developmental Cell, 32(4), 435–446.
93. Choi, H. R., Byun, S. Y., Kwon, S. H., & Park, K. C. (2015). Niche interactions in epidermal stem cells. World Journal of Stem Cells, 7(2), 495–501.
94. DeCarolis, N.A., Kirby, E.D., Wyss-Coray, T., Palmer, T.D. (2015). The role of the microenvironmental niche in declining stem-cell functions associated with biological aging. Cold Spring Harbor Perspectives in Medicine. doi:10.1101/cshperspect.a025874.
95. Lane, S. W., Williams, D. A., & Watt, F. M. (2014). Modulating the stem cell niche for tissue regeneration. Nature Biotechnology, 32(8), 795–803.
96. Tan, D. W., & Barker, N. (2014). Intestinal stem cells and their defining niche. Current Topics in Developmental Biology, 107, 77–107.
97. Thomas, K., Engler, A. J., & Meyer, G. A. (2015). Extracellular matrix regulation in the muscle satellite cell niche. Connective Tissue Research, 56(1), 1–8.
98. Bear, J. E., & Haugh, J. M. (2014). Directed migration of mesenchymal cells: where signaling and the cytoskeleton meet. Current Opinion in Cell Biology, 30, 74–82.
99. Sarris, M., & Sixt, M. (2015). Navigating in tissue mazes: chemoattractant interpretation in complex environments. Current Opinion in Cell Biology, 36, 93–102.
100. Wang, J., & Knaut, H. (2014). Chemokine signaling in development and disease. Development, 141(22), 4199–4205.
101. Karpova, D., & Bonig, H. (2015). Concise review: CXCR4/CXCL12 signaling in immature hematopoiesis--lessons from pharmacological and genetic models. Stem Cells (Dayton, Ohio), 33(8), 2391–2399.
102. Nagasawa, T. (2015). CXCL12/SDF-1 and CXCR4. Frontiers in Immunology, 6, 301.
103. Peled, A., Petit, I., Kollet, O., Magid, M., Ponomaryov, T., Byk, T., et al. (1999). Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science, 283(5403), 845–848.
104. Gallagher, K. A., Liu, Z. J., Xiao, M., Chen, H., Goldstein, L. J., Buerk, D. G., et al. (2007). Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed by hyperoxia and SDF-1 alpha. The Journal of Clinical Investigation, 117(5), 1249–1259.
105. Jaerve, A., Schira, J., & Muller, H. W. (2012). Concise review: the potential of stromal cell-derived factor 1 and its receptors to promote stem cell functions in spinal cord repair. Stem Cells Translational Medicine, 1(10), 732–739.
106. Pan, S., Dangaria, S., Gopinathan, G., Yan, X., Lu, X., Kolokythas, A., et al. (2013). SCF promotes dental pulp progenitor migration, neovascularization, and collagen remodeling - potential applications as a homing factor in dental pulp regeneration. Stem Cell Reviews, 9(5), 655–667.
107. Jalili, A., Shirvaikar, N., Marquez-Curtis, L. A., Turner, A. R., & Janowska-Wieczorek, A. (2010). The HGF/c-Met axis synergizes with G-CSF in the mobilization of hematopoietic stem/progenitor cells. Stem Cells and Development, 19(8), 1143–1151.
108. Tesio, M., Golan, K., Corso, S., Giordano, S., Schajnovitz, A., Vagima, Y., et al. (2011). Enhanced c-Met activity promotes G-CSF-induced mobilization of hematopoietic progenitor cells via ROS signaling. Blood, 117(2), 419–428.
109. Bischoff, R. (1997). Chemotaxis of skeletal muscle satellite cells. Developmental Dynamics: an Official Publication of the American Association of Anatomists, 208(4), 505–515.
110. Ishido, M., & Kasuga, N. (2012). In vivo real-time imaging of exogenous HGF-triggered cell migration in rat intact soleus muscles. Acta Histochemica et Cytochemica, 45(3), 193–199.
111. Li, J., & Johnson, S. E. (2013). Ephrin-A5 promotes bovine muscle progenitor cell migration before mitotic activation. Journal of Animal Science, 91(3), 1086–1093.
112. Siegel, A. L., Atchison, K., Fisher, K. E., Davis, G. E., & Cornelison, D. D. (2009). 3D timelapse analysis of muscle satellite cell motility. Stem Cells (Dayton, Ohio), 27(10), 2527–2538.
113. Webster, M. T., & Fan, C. M. (2013). c-MET regulates myoblast motility and myocyte fusion during adult skeletal muscle regeneration. PloS One, 8(11), e81757.
114. Binder, B. Y., Williams, P. A., Silva, E. A., & Leach, J. K. (2015). Lysophosphatidic acid and sphingosine-1-phosphate: a concise review of biological function and applications for tissue engineering. Tissue Engineering. Part B, Reviews, 21(6), 531–542.
115. Kunkel, G. T., Maceyka, M., Milstien, S., & Spiegel, S. (2013). Targeting the sphingosine-1-phosphate axis in cancer, inflammation and beyond. Nature Reviews Drug Discovery, 12(9), 688–702.
116. Maceyka, M., Harikumar, K. B., Milstien, S., & Spiegel, S. (2012). Sphingosine-1-phosphate signaling and its role in disease. Trends in Cell Biology, 22(1), 50–60.
117. Proia, R. L., & Hla, T. (2015). Emerging biology of sphingosine-1-phosphate: its role in pathogenesis and therapy. The Journal of Clinical Investigation, 125(4), 1379–1387.
118. Ratajczak, M. Z., Suszynska, M., Borkowska, S., Ratajczak, J., & Schneider, G. (2014). The role of sphingosine-1 phosphate and ceramide-1 phosphate in trafficking of normal stem cells and cancer cells. Expert Opinion on Therapeutic Targets, 18(1), 95–107.
119. Tsujiuchi, T., Hirane, M., Dong, Y., & Fukushima, N. (2014). Diverse effects of LPA receptors on cell motile activities of cancer cells. Journal of Receptor and Signal Transduction Research, 34(3), 149–153.
120. Walker, T. L., Overall, R. W., Vogler, S., Sykes, A. M., Ruhwald, S., Lasse, D., et al. (2016). Lysophosphatidic acid receptor is a functional marker of adult hippocampal precursor cells. Stem Cell Reports, 6(4), 552–565.
121. Golan, K., Kollet, O., & Lapidot, T. (2013). Dynamic cross talk between S1P and CXCL12 regulates hematopoietic stem cells migration, development and bone remodeling. Pharmaceuticals (Basel, Switzerland), 6(9), 1145–1169.
122. Pebay, A., Bonder, C. S., & Pitson, S. M. (2007). Stem cell regulation by lysophospholipids. Prostaglandins & Other Lipid Mediators, 84(3–4), 83–97.
123. Adamiak, M., Borkowska, S., Wysoczynski, M., Suszynska, M., Kucia, M., Rokosh, G., et al. (2015). Evidence for the involvement of sphingosine-1-phosphate in the homing and engraftment of hematopoietic stem cells to bone marrow. Oncotarget, 6(22), 18819–18828.
124. Bendall, L. J., & Basnett, J. (2013). Role of sphingosine 1-phosphate in trafficking and mobilization of hematopoietic stem cells. Current Opinion in Hematology, 20(4), 281–288.
125. Golan, K., Vagima, Y., Ludin, A., Itkin, T., Cohen-Gur, S., Kalinkovich, A., et al. (2012). S1P promotes murine progenitor cell egress and mobilization via S1P1-mediated ROS signaling and SDF-1 release. Blood, 119(11), 2478–2488.
126. Karapetyan, A. V., Klyachkin, Y. M., Selim, S., Sunkara, M., Ziada, K. M., Cohen, D. A., et al. (2013). Bioactive lipids and cationic antimicrobial peptides as new potential regulators for trafficking of bone marrow-derived stem cells in patients with acute myocardial infarction. Stem Cells and Development, 22(11), 1645–1656.
127. Calise, S., Blescia, S., Cencetti, F., Bernacchioni, C., Donati, C., & Bruni, P. (2012). Sphingosine 1-phosphate stimulates proliferation and migration of satellite cells: role of S1P receptors. Biochimica et Biophysica Acta, 1823(2), 439–450.
128. Cencetti, F., Bruno, G., Blescia, S., Bernacchioni, C., Bruni, P., & Donati, C. (2014). Lysophosphatidic acid stimulates cell migration of satellite cells. A role for the sphingosine kinase/sphingosine 1-phosphate axis. The FEBS Journal, 281(19), 4467–4478.
129. Ishii, M., Egen, J. G., Klauschen, F., Meier-Schellersheim, M., Saeki, Y., Vacher, J., Proia, R. L., & Germain, R. N. (2009). Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature, 458(7237), 524–528.
130. Ishii, M., Kikuta, J., Shimazu, Y., Meier-Schellersheim, M., & Germain, R. N. (2010). Chemorepulsion by blood S1P regulates osteoclast precursor mobilization and bone remodeling in vivo. The Journal of Experimental Medicine, 207(13), 2793–2798.
131. Novgorodov, A. S., El-Alwani, M., Bielawski, J., Obeid, L. M., & Gudz, T. I. (2007). Activation of sphingosine-1-phosphate receptor S1P5 inhibits oligodendrocyte progenitor migration. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 21(7), 1503–1514.
132. Kimura, A., Ohmori, T., Kashiwakura, Y., Ohkawa, R., Madoiwa, S., Mimuro, J., et al. (2008). Antagonism of sphingosine 1-phosphate receptor-2 enhances migration of neural progenitor cells toward an area of brain. Stroke; A Journal of Cerebral Circulation, 39(12), 3411–3417.
133. Blanc, C. A., Grist, J. J., Rosen, H., Sears-Kraxberger, I., Steward, O., & Lane, T. E. (2015). Sphingosine-1-phosphate receptor antagonism enhances proliferation and migration of engrafted neural progenitor cells in a model of viral-induced demyelination. The American Journal of Pathology, 185(10), 2819–2832.
134. Boyd, A. W., Bartlett, P. F., & Lackmann, M. (2014). Therapeutic targeting of EPH receptors and their ligands. Nature Reviews Drug Discovery, 13(1), 39–62.
135. Coulthard, M. G., Morgan, M., Woodruff, T. M., Arumugam, T. V., Taylor, S. M., Carpenter, T. C., et al. (2012). Eph/Ephrin signaling in injury and inflammation. The American Journal of Pathology, 181(5), 1493–1503.
136. Gucciardo, E., Sugiyama, N., & Lehti, K. (2014). Eph- and ephrin-dependent mechanisms in tumor and stem cell dynamics. Cellular and Molecular Life Sciences: CMLS, 71(19), 3685–3710.
137. Kania, A., & Klein, R. (2016). Mechanisms of ephrin-Eph signalling in development, physiology and disease. Nature Reviews Molecular Cell Biology, 17(4), 240–256.
138. Klein, R., & Kania, A. (2014). Ephrin signalling in the developing nervous system. Current Opinion in Neurobiology, 27C, 16–24.
139. Laussu, J., Khuong, A., Gautrais, J., & Davy, A. (2014). Beyond boundaries--Eph:ephrin signaling in neurogenesis. Cell Adhesion & Migration, 8(4), 349–359.
140. Lisabeth, E.M., Falivelli, G., Pasquale, E.B. (2013). Eph receptor signaling and ephrins. Cold Spring Harbor Perspectives in Biology. doi:10.1101/cshperspect.a009159.
141. Nikolov, D. B., Xu, K., & Himanen, J. P. (2014). Homotypic receptor-receptor interactions regulating Eph signaling. Cell Adhesion & Migration, 8(4), 360–365.
142. Park, I., & Lee, H. S. (2015). EphB/ephrinB signaling in cell adhesion and migration. Molecules and Cells, 38(1), 14–19.
143. Pasquale, E. B. (2010). Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nature Reviews Cancer, 10(3), 165–180.
144. Pitulescu, M. E., & Adams, R. H. (2010). Eph/ephrin molecules--a hub for signaling and endocytosis. Genes & Development, 24(22), 2480–2492.
145. Wilkinson, D. G. (2014). Regulation of cell differentiation by Eph receptor and ephrin signaling. Cell Adhesion & Migration, 8(4), 339–348.
146. Ting, M. J., Day, B. W., Spanevello, M. D., & Boyd, A. W. (2010). Activation of ephrin A proteins influences hematopoietic stem cell adhesion and trafficking patterns. Experimental Hematology, 38(11), 1087–1098.
147. Nguyen, T.M., Arthur, A., Gronthos, S. (2016). The role of Eph/ephrin molecules in stromal-hematopoietic interactions. International Journal of Hematology, 103(2), 145–154.
148. Nguyen, T. M., Arthur, A., Panagopoulos, R., Paton, S., Hayball, J. D., Zannettino, A. C., et al. (2015). EphB4 expressing stromal cells exhibit an enhanced capacity for hematopoietic stem cell maintenance. Stem Cells (Dayton, Ohio), 33(9), 2838–2849.
149. Okubo, T., Yanai, N., & Obinata, M. (2006). Stromal cells modulate ephrinB2 expression and transmigration of hematopoietic cells. Experimental Hematology, 34(3), 330–338.
150. Stokowski, A., Shi, S., Sun, T., Bartold, P. M., Koblar, S. A., & Gronthos, S. (2007). EphB/ephrin-B interaction mediates adult stem cell attachment, spreading, and migration: implications for dental tissue repair. Stem Cells (Dayton, Ohio), 25(1), 156–164.
151. Arthur, A., Koblar, S., Shi, S., & Gronthos, S. (2009). Eph/ephrinB mediate dental pulp stem cell mobilization and function. Journal of Dental Research, 88(9), 829–834.
152. Conover, J. C., Doetsch, F., Garcia-Verdugo, J. M., Gale, N. W., Yancopoulos, G. D., & Alvarez-Buylla, A. (2000). Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nature Neuroscience, 3(11), 1091–1097.
153. Catchpole, T., & Henkemeyer, M. (2011). EphB2 tyrosine kinase-dependent forward signaling in migration of neuronal progenitors that populate and form a distinct region of the dentate niche. Journal of Neuroscience, 31(32), 11472–11483.
154. Chumley, M. J., Catchpole, T., Silvany, R. E., Kernie, S. G., & Henkemeyer, M. (2007). EphB receptors regulate stem/progenitor cell proliferation, migration, and polarity during hippocampal neurogenesis. Journal of Neuroscience, 27(49), 13481–13490.
155. Holmberg, J., Armulik, A., Senti, K. A., Edoff, K., Spalding, K., Momma, S., et al. (2005). Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis. Genes & Development, 19(4), 462–471.
156. Parrinello, S., Napoli, I., Ribeiro, S., Wingfield Digby, P., Fedorova, M., Parkinson, D. B., et al. (2010). EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell, 143(1), 145–155.
157. Stark, D. A., Karvas, R. M., Siegel, A. L., & Cornelison, D. D. (2011). Eph/ephrin interactions modulate muscle satellite cell motility and patterning. Development, 138(24), 5279–5289.
158. Gu, J. M., Wang, D. J., Peterson, J. M., Shintaku, J., Liyanarachchi, S., Coppola, V., et al. (2016). An NF-kappaB - EphrinA5-Dependent Communication between NG2(+) Interstitial Cells and Myoblasts Promotes Muscle Growth in Neonates. Developmental Cell, 36(2), 215–224.
159. Goichberg, P., Bai, Y., D’Amario, D., Ferreira-Martins, J., Fiorini, C., Zheng, H., et al. (2011). The ephrin A1-EphA2 system promotes cardiac stem cell migration after infarction. Circulation Research, 108(9), 1071–1083.
160. Goichberg, P., Kannappan, R., Cimini, M., Bai, Y., Sanada, F., Sorrentino, A., et al. (2013). Age-associated defects in EphA2 signaling impair the migration of human cardiac progenitor cells. Circulation, 128(20), 2211–2223.
161. Dries, J. L., Kent, S. D., & Virag, J. A. (2011). Intramyocardial administration of chimeric ephrinA1-Fc promotes tissue salvage following myocardial infarction in mice. The Journal of Physiology, 589(Pt 7), 1725–1740.
162. DuSablon, A., Kent, S., Coburn, A., & Virag, J. (2014). EphA2-receptor deficiency exacerbates myocardial infarction and reduces survival in hyperglycemic mice. Cardiovascular Diabetology, 13, 114.
163. O’Neal, W. T., Griffin, W. F., Kent, S. D., Faiz, F., Hodges, J., Vuncannon, J., & Virag, J. A. (2014). Deletion of the EphA2 receptor exacerbates myocardial injury and the progression of ischemic cardiomyopathy. Frontiers in Physiology, 5, 132.
164. Popov, C., Kohler, J., & Docheva, D. (2015). Activation of EphA4 and EphB2 Reverse Signaling Restores the Age-Associated Reduction of Self-Renewal, Migration, and Actin Turnover in Human Tendon Stem/Progenitor Cells. Frontiers in Aging Neuroscience, 7, 246.
165. Batlle, E., Henderson, J. T., Beghtel, H., van den Born, M. M., Sancho, E., Huls, G., et al. (2002). Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell, 111(2), 251–263.
166. Genander, M., & Frisen, J. (2010). Eph receptors tangled up in two: Independent control of cell positioning and proliferation. Cell Cycle, 9(10), 1865–1866.
167. Genander, M. (2012). Eph and ephrins in epithelial stem cell niches and cancer. Cell Adhesion & Migration, 6(2), 126–130.
168. Holmberg, J., Genander, M., Halford, M. M., Anneren, C., Sondell, M., Chumley, M. J., et al. (2006). EphB receptors coordinate migration and proliferation in the intestinal stem cell niche. Cell, 125(6), 1151–1163.
169. Perez White, B. E., & Getsios, S. (2014). Eph receptor and ephrin function in breast, gut, and skin epithelia. Cell Adhesion & Migration, 8(4), 327–338.
170. Wijeratne, D. T., Rodger, J., Wood, F. M., & Fear, M. W. (2016). The role of Eph receptors and Ephrins in the skin. International Journal of Dermatology, 55(1), 3–10.
171. Genander, M., Halford, M. M., Xu, N. J., Eriksson, M., Yu, Z., Qiu, Z., et al. (2009). Dissociation of EphB2 signaling pathways mediating progenitor cell proliferation and tumor suppression. Cell, 139(4), 679–692.
172. Miao, H., Nickel, C. H., Cantley, L. G., Bruggeman, L. A., Bennardo, L. N., & Wang, B. (2003). EphA kinase activation regulates HGF-induced epithelial branching morphogenesis. The Journal of Cell Biology, 162(7), 1281–1292.
173. Lu, Q., Sun, E. E., Klein, R. S., & Flanagan, J. G. (2001). Ephrin-B reverse signaling is mediated by a novel PDZ-RGS protein and selectively inhibits G protein-coupled chemoattraction. Cell, 105(1), 69–79.
174. Vaught, D., Chen, J., & Brantley-Sieders, D. M. (2009). Regulation of mammary gland branching morphogenesis by EphA2 receptor tyrosine kinase. Molecular Biology of the Cell, 20(10), 2572–2581.
175. Dejana, E., & Giampietro, C. (2012). Vascular endothelial-cadherin and vascular stability. Current Opinion in Hematology, 19(3), 218–223.
176. Geiger, B., & Ayalon, O. (1992). Cadherins. Annual Review of Cell Biology, 8, 307–332.
177. Lecuit, T., & Yap, A. S. (2015). E-cadherin junctions as active mechanical integrators in tissue dynamics. Nature Cell Biology, 17(5), 533–539.
178. Miyamoto, Y., Sakane, F., & Hashimoto, K. (2015). N-cadherin-based adherens junction regulates the maintenance, proliferation, and differentiation of neural progenitor cells during development. Cell Adhesion & Migration, 9(3), 183–192.
179. van Roy, F. (2014). Beyond E-cadherin: roles of other cadherin superfamily members in cancer. Nature Reviews Cancer, 14(2), 121–134.
180. Chen, J. Y., Miyanishi, M., Wang, S. K., Yamazaki, S., Sinha, R., Kao, K. S., et al. (2016). Hoxb5 marks long-term haematopoietic stem cells and reveals a homogenous perivascular niche. Nature, 530(7589), 223–227.
181. Lay, K., Kume, T., Fuchs, E. (2016). FOXC1 maintains the hair follicle stem cell niche and governs stem cell quiescence to preserve long-term tissue-regenerating potential. Proceedings of the National Academy of Sciences of the United States of America, 13(11), E1506–E1515.
182. Porlan, E., Marti-Prado, B., Morante-Redolat, J. M., Consiglio, A., Delgado, A. C., Kypta, R., et al. (2014). MT5-MMP regulates adult neural stem cell functional quiescence through the cleavage of N-cadherin. Nature Cell Biology, 16(7), 629–638.
183. Zhang, J., Niu, C., Ye, L., Huang, H., He, X., Tong, W. G., et al. (2003). Identification of the haematopoietic stem cell niche and control of the niche size. Nature, 425(6960), 836–841.
184. Klingener, M., Chavali, M., Singh, J., McMillan, N., Coomes, A., Dempsey, P. J., et al. (2014). N-cadherin promotes recruitment and migration of neural progenitor cells from the SVZ neural stem cell niche into demyelinated lesions. Journal of Neuroscience, 34(29), 9590–9606.
185. Gonzalez-Nieto, D., Chang, K. H., Fasciani, I., Nayak, R., Fernandez-Garcia, L., Barrio, L. C., & Cancelas, J. A. (2015). Connexins: intercellular signal transmitters in lymphohematopoietic tissues. International Review of Cell and Molecular Biology, 318, 27–62.
186. Meier, C., & Rosenkranz, K. (2014). Cx43 expression and function in the nervous system-implications for stem cell mediated regeneration. Frontiers in Physiology, 5, 106.
187. Salmina, A. B., Morgun, A. V., Kuvacheva, N. V., Lopatina, O. L., Komleva, Y. K., Malinovskaya, N. A., & Pozhilenkova, E. A. (2014). Establishment of neurogenic microenvironment in the neurovascular unit: the connexin 43 story. Reviews in the Neurosciences, 25(1), 97–111.
188. Gonzalez-Nieto, D., Li, L., Kohler, A., Ghiaur, G., Ishikawa, E., Sengupta, A., et al. (2012). Connexin-43 in the osteogenic BM niche regulates its cellular composition and the bidirectional traffic of hematopoietic stem cells and progenitors. Blood, 119(22), 5144–5154.
189. Schajnovitz, A., Itkin, T., D’Uva, G., Kalinkovich, A., Golan, K., Ludin, A., et al. (2011). CXCL12 secretion by bone marrow stromal cells is dependent on cell contact and mediated by connexin-43 and connexin-45 gap junctions. Nature Immunology, 12(5), 391–398.
190. Papayannopoulou, T. (2003). Bone marrow homing: the players, the playfield, and their evolving roles. Current Opinion in Hematology, 10(3), 214–219.
191. Sahin, A. O., & Buitenhuis, M. (2012). Molecular mechanisms underlying adhesion and migration of hematopoietic stem cells. Cell Adhesion & Migration, 6(1), 39–48.
192. Leiva, M., Quintana, J. A., Ligos, J. M., & Hidalgo, A. (2016). Haematopoietic ESL-1 enables stem cell proliferation in the bone marrow by limiting TGFbeta availability. Nature Communications, 7, 10222.
193. Winkler, I. G., Barbier, V., Nowlan, B., Jacobsen, R. N., Forristal, C. E., Patton, J. T., et al. (2012). Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nature Medicine, 18(11), 1651–1657.
194. Chavakis, E., & Dimmeler, S. (2011). Homing of progenitor cells to ischemic tissues. Antioxidants & Redox Signaling, 15(4), 967–980.
195. Sackstein, R. (2011). The biology of CD44 and HCELL in hematopoiesis: the ‘step 2-bypass pathway’ and other emerging perspectives. Current Opinion in Hematology, 18(4), 239–248.
196. Sackstein, R. (2012). Engineering cellular trafficking via glycosyltransferase-programmed stereosubstitution. Annals of the New York Academy of Sciences, 1253, 193–200.
197. Abdi, R., Moore, R., Sakai, S., Donnelly, C. B., Mounayar, M., & Sackstein, R. (2015). HCELL expression on murine MSC licenses pancreatotropism and confers durable reversal of autoimmune diabetes in NOD mice. Stem Cells (Dayton, Ohio), 33(5), 1523–1531.
198. Merzaban, J. S., Imitola, J., Starossom, S. C., Zhu, B., Wang, Y., Lee, J., et al. (2015). Cell surface glycan engineering of neural stem cells augments neurotropism and improves recovery in a murine model of multiple sclerosis. Glycobiology, 25(12), 1392–1409.
199. Akhmanova, M., Osidak, E., Domogatsky, S., Rodin, S., & Domogatskaya, A. (2015). Physical, spatial, and molecular aspects of extracellular matrix of in vivo niches and artificial scaffolds relevant to stem cells research. Stem Cells International, 2015, 167025.
200. Frantz, C., Stewart, K. M., & Weaver, V. M. (2010). The extracellular matrix at a glance. Journal of Cell Science, 123(Pt 24), 4195–4200.
201. Freedman, B. R., Bade, N. D., Riggin, C. N., Zhang, S., Haines, P. G., Ong, K. L., & Janmey, P. A. (2015). The (dys)functional extracellular matrix. Biochimica et Biophysica Acta, 1853(11 Pt B), 3153–3164.
202. Handorf, A. M., Zhou, Y., Halanski, M. A., & Li, W. J. (2015). Tissue stiffness dictates development, homeostasis, and disease progression. Organogenesis, 11(1), 1–15.
203. Hynes, R. O., & Naba, A. (2012). Overview of the matrisome--an inventory of extracellular matrix constituents and functions. Cold Spring Harbor Perspectives in Biology, 4(1), a004903.
204. Theocharis, A. D., Skandalis, S. S., Gialeli, C., & Karamanos, N. K. (2016). Extracellular matrix structure. Advanced Drug Delivery Reviews, 97, 4–27.
205. Daley, W. P., & Yamada, K. M. (2013). ECM-modulated cellular dynamics as a driving force for tissue morphogenesis. Current Opinion in Genetics & Development, 23(4), 408–414.
206. Happe, C. L., & Engler, A. J. (2016). Mechanical forces reshape differentiation cues that guide cardiomyogenesis. Circulation Research, 118(2), 296–310.
207. Mammoto, T., Mammoto, A., & Ingber, D. E. (2013). Mechanobiology and developmental control. Annual Review of Cell and Developmental Biology, 29, 27–61.
208. Walters, N. J., & Gentleman, E. (2015). Evolving insights in cell-matrix interactions: elucidating how non-soluble properties of the extracellular niche direct stem cell fate. Acta Biomaterialia, 11, 3–16.
209. Chandra, P., & Lee, S. J. (2015). Synthetic extracellular microenvironment for modulating stem cell behaviors. Biomarker Insights, 10(Suppl 1), 105–116.
210. Chen, W., Shao, Y., Li, X., Zhao, G., & Fu, J. (2014). Nanotopographical surfaces for stem cell fate control: engineering mechanobiology from the bottom. Nano Today, 9(6), 759–784.
211. Dalby, M. J., Gadegaard, N., & Oreffo, R. O. (2014). Harnessing nanotopography and integrin-matrix interactions to influence stem cell fate. Nature Materials, 13(6), 558–569.
212. Dingal, P. C., & Discher, D. E. (2014). Combining insoluble and soluble factors to steer stem cell fate. Nature Materials, 13(6), 532–537.
213. Faissner, A., & Reinhard, J. (2015). The extracellular matrix compartment of neural stem and glial progenitor cells. Glia, 63(8), 1330–1349.
214. Humphrey, J. D., Dufresne, E. R., & Schwartz, M. A. (2014). Mechanotransduction and extracellular matrix homeostasis. Nature Reviews Molecular Cell Biology, 15(12), 802–812.
215. Huttenlocher, A., & Horwitz, A. R. (2011). Integrins in cell migration. Cold Spring Harbor Perspectives in Biology, 3(9), a005074.
216. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell, 110(6), 673–687.
217. Miranti, C. K., & Brugge, J. S. (2002). Sensing the environment: a historical perspective on integrin signal transduction. Nature Cell Biology, 4(4), E83–E90.
218. Schwartz, M. A. (2010). Integrins and extracellular matrix in mechanotransduction. Cold Spring Harbor Perspectives in Biology, 2(12), a005066.
219. Winograd-Katz, S. E., Fassler, R., Geiger, B., & Legate, K. R. (2014). The integrin adhesome: from genes and proteins to human disease. Nature Reviews Molecular Cell Biology, 15(4), 273–288.
220. Wolfenson, H., Lavelin, I., & Geiger, B. (2013). Dynamic regulation of the structure and functions of integrin adhesions. Developmental Cell, 24(5), 447–458.
221. Milner, R., Edwards, G., Streuli, C., & Ffrench-Constant, C. (1996). A role in migration for the alpha V beta 1 integrin expressed on oligodendrocyte precursors. Journal of Neuroscience, 16(22), 7240–7252.
222. Ernst, N., Yay, A., Biro, T., Tiede, S., Humphries, M., Paus, R., & Kloepper, J. E. (2013). beta1 integrin signaling maintains human epithelial progenitor cell survival in situ and controls proliferation, apoptosis and migration of their progeny. PloS One, 8(12), e84356.
223. Schofield, K. P., Rushton, G., Humphries, M. J., Dexter, T. M., & Gallagher, J. T. (1997). Influence of interleukin-3 and other growth factors on alpha4beta1 integrin-mediated adhesion and migration of human hematopoietic progenitor cells. Blood, 90(5), 1858–1866.
224. Strobel, E. S., Mobest, D., von Kleist, S., Dangel, M., Ries, S., Mertelsmann, R., & Henschler, R. (1997). Adhesion and migration are differentially regulated in hematopoietic progenitor cells by cytokines and extracellular matrix. Blood, 90(9), 3524–3532.
225. Gu, Y. C., Kortesmaa, J., Tryggvason, K., Persson, J., Ekblom, P., Jacobsen, S. E., & Ekblom, M. (2003). Laminin isoform-specific promotion of adhesion and migration of human bone marrow progenitor cells. Blood, 101(3), 877–885.
226. Muth, C. A., Steinl, C., Klein, G., & Lee-Thedieck, C. (2013). Regulation of hematopoietic stem cell behavior by the nanostructured presentation of extracellular matrix components. PloS One, 8(2), e54778.
227. Bershadsky, A., Kozlov, M., & Geiger, B. (2006). Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize. Current Opinion in Cell Biology, 18(5), 472–481.
228. Doyle, A.D., Yamada, K.M. (2016). Mechanosensing via cell-matrix adhesions in 3D microenvironments. Experimental Cell Research, 343(1), 60–66.
229. Geiger, B., Spatz, J. P., & Bershadsky, A. D. (2009). Environmental sensing through focal adhesions. Nature Reviews Molecular Cell Biology, 10(1), 21–33.
230. Bellas, E., & Chen, C. S. (2014). Forms, forces, and stem cell fate. Current Opinion in Cell Biology, 31, 92–97.
231. Holst, J., Watson, S., Lord, M. S., Eamegdool, S. S., Bax, D. V., Nivison-Smith, L. B., et al. (2010). Substrate elasticity provides mechanical signals for the expansion of hemopoietic stem and progenitor cells. Nature Biotechnology, 28(10), 1123–1128.
232. Lee-Thedieck, C., Rauch, N., Fiammengo, R., Klein, G., & Spatz, J. P. (2012). Impact of substrate elasticity on human hematopoietic stem and progenitor cell adhesion and motility. Journal of Cell Science, 125(Pt 16), 3765–3775.
233. Ehrbar, M., Sala, A., Lienemann, P., Ranga, A., Mosiewicz, K., Bittermann, A., et al. (2011). Elucidating the role of matrix stiffness in 3D cell migration and remodeling. Biophysical Journal, 100(2), 284–293.
234. Yang, K., Jung, K., Ko, E., Kim, J., Park, K. I., & Cho, S. W. (2013). Nanotopographical manipulation of focal adhesion formation for enhanced differentiation of human neural stem cells. ACS Applied Materials & Interfaces, 5(21), 10529–10540.
235. Magnusson, A. K., Linderholm, P., Vieider, C., Ulfendahl, M., & Erlandsson, A. (2008). Surface protein patterns govern morphology, proliferation, and expression of cellular markers but have no effect on physiological properties of cortical precursor cells. Journal of Neuroscience Research, 86(11), 2363–2375.
236. Ruiz, A., Buzanska, L., Gilliland, D., Rauscher, H., Sirghi, L., Sobanski, T., et al. (2008). Micro-stamped surfaces for the patterned growth of neural stem cells. Biomaterials, 29(36), 4766–4774.
237. Joo, S., Kim, J. Y., Lee, E., Hong, N., Sun, W., & Nam, Y. (2015). Effects of ECM protein micropatterns on the migration and differentiation of adult neural stem cells. Scientific Reports, 5, 13043.
238. DeMali, K. A., Sun, X., & Bui, G. A. (2014). Force transmission at cell-cell and cell-matrix adhesions. Biochemistry, 53(49), 7706–7717.
239. Gasparski, A. N., & Beningo, K. A. (2015). Mechanoreception at the cell membrane: More than the integrins. Archives of Biochemistry and Biophysics, 586, 20–26.
240. Priya, R., & Yap, A. S. (2015). Active tension: the role of cadherin adhesion and signaling in generating junctional contractility. Current Topics in Developmental Biology, 112, 65–102.
241. Zoller, M. (2015). CD44, hyaluronan, the hematopoietic stem cell, and leukemia-initiating cells. Frontiers in Immunology, 6, 235.
242. Avigdor, A., Goichberg, P., Shivtiel, S., Dar, A., Peled, A., Samira, S., et al. (2004). CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood, 103(8), 2981–2989.
243. Vagima, Y., Avigdor, A., Goichberg, P., Shivtiel, S., Tesio, M., Kalinkovich, A., et al. (2009). MT1-MMP and RECK are involved in human CD34+ progenitor cell retention, egress, and mobilization. The Journal of Clinical Investigation, 119(3), 492–503.
244. Healy, L., May, G., Gale, K., Grosveld, F., Greaves, M., & Enver, T. (1995). The stem cell antigen CD34 functions as a regulator of hemopoietic cell adhesion. Proceedings of the National Academy of Sciences of the United States of America, 92(26), 12240–12244.
245. Nielsen, J. S., & McNagny, K. M. (2009). CD34 is a key regulator of hematopoietic stem cell trafficking to bone marrow and mast cell progenitor trafficking in the periphery. Microcirculation, 16(6), 487–496.
246. Alfaro, L. A., Dick, S. A., Siegel, A. L., Anonuevo, A. S., McNagny, K. M., Megeney, L. A., et al. (2011). CD34 promotes satellite cell motility and entry into proliferation to facilitate efficient skeletal muscle regeneration. Stem Cells (Dayton, Ohio), 29(12), 2030–2041.
247. Ettinger, A., & Wittmann, T. (2014). Fluorescence live cell imaging. Methods in Cell Biology, 123, 77–94.
248. Fink, J., Andersson-Rolf, A., & Koo, B. K. (2015). Adult stem cell lineage tracing and deep tissue imaging. BMB Reports, 48(12), 655–667.
249. Kupfer, M. E., & Ogle, B. M. (2015). Advanced imaging approaches for regenerative medicine: Emerging technologies for monitoring stem cell fate in vitro and in vivo. Biotechnology Journal, 10(10), 1515–1528.
250. Vande Velde, G., Couillard-Despres, S., Aigner, L., Himmelreich, U., & van der Linden, A. (2012). In situ labeling and imaging of endogenous neural stem cell proliferation and migration. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, 4(6), 663–679.
251. Wang, J., & Jokerst, J. V. (2016). Stem cell imaging: tools to improve cell delivery and viability. Stem Cells International, 2016, 9240652.
252. Weissleder, R., & Nahrendorf, M. (2015). Advancing biomedical imaging. Proceedings of the National Academy of Sciences of the United States of America, 112(47), 14424–14428.
253. Vaz, R., Martins, G. G., Thorsteinsdottir, S., & Rodrigues, G. (2012). Fibronectin promotes migration, alignment and fusion in an in vitro myoblast cell model. Cell and Tissue Research, 348(3), 569–578.
254. Bentzinger, C. F., von Maltzahn, J., Dumont, N. A., Stark, D. A., Wang, Y. X., Nhan, K., et al. (2014). Wnt7a stimulates myogenic stem cell motility and engraftment resulting in improved muscle strength. The Journal of Cell Biology, 205(1), 97–111.
255. Brown, S., & Greco, V. (2014). Stem cells in the wild: understanding the World of stem cells through intravital imaging. Cell Stem Cell, 15(6), 683–686.
256. Pittet, M. J., & Weissleder, R. (2011). Intravital imaging. Cell, 147(5), 983–991.
257. Weigert, R. (2014). Advances in intravital microscopy: from basic to clinical research. Netherlands: Springer.
258. Mazo, I. B., Gutierrez-Ramos, J. C., Frenette, P. S., Hynes, R. O., Wagner, D. D., & von Andrian, U. H. (1998). Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. The Journal of Experimental Medicine, 188(3), 465–474.
259. Carlson, A. L., Fujisaki, J., Wu, J., Runnels, J. M., Turcotte, R., Spencer, J. A., et al. (2013). Tracking single cells in live animals using a photoconvertible near-infrared cell membrane label. PloS One, 8(8), e69257.
260. Khorshed, R. A., Hawkins, E. D., Duarte, D., Scott, M. K., Akinduro, O. A., Rashidi, N. M., et al. (2015). Automated Identification and Localization of Hematopoietic Stem Cells in 3D Intravital Microscopy Data. Stem Cell Reports, 5(1), 139–153.
261. Lo Celso, C., Fleming, H. E., Wu, J. W., Zhao, C. X., Miake-Lye, S., Fujisaki, J., et al. (2009). Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature, 457(7225), 92–96.
262. Lo Celso, C., Lin, C. P., & Scadden, D. T. (2011). In vivo imaging of transplanted hematopoietic stem and progenitor cells in mouse calvarium bone marrow. Nature Protocols, 6(1), 1–14.
263. Scott, M. K., Akinduro, O., & Lo Celso, C. (2014). In vivo 4-dimensional tracking of hematopoietic stem and progenitor cells in adult mouse calvarial bone marrow. Journal of Visualized Experiments: JoVE, 91, e51683.
264. Itkin, T., Gur-Cohen, S., Spencer, J. A., Schajnovitz, A., Ramasamy, S. K., Kusumbe, A. P., et al. (2016). Distinct bone marrow blood vessels differentially regulate haematopoiesis. Nature, 532(7599), 323–328.
265. Ishido, M., & Kasuga, N. (2011). In situ real-time imaging of the satellite cells in rat intact and injured soleus muscles using quantum dots. Histochemistry and Cell Biology, 135(1), 21–26.
266. Kovalchuk, Y., Homma, R., Liang, Y., Maslyukov, A., Hermes, M., Thestrup, T., et al. (2015). In vivo odourant response properties of migrating adult-born neurons in the mouse olfactory bulb. Nature Communications, 6, 6349.
267. Mesa, K. R., Rompolas, P., Zito, G., Myung, P., Sun, T. Y., Brown, S., et al. (2015). Niche-induced cell death and epithelial phagocytosis regulate hair follicle stem cell pool. Nature, 522(7554), 94–97.
268. Pineda, C. M., Park, S., Mesa, K. R., Wolfel, M., Gonzalez, D. G., Haberman, A. M., et al. (2015). Intravital imaging of hair follicle regeneration in the mouse. Nature Protocols, 10(7), 1116–1130.
269. Rompolas, P., Deschene, E. R., Zito, G., Gonzalez, D. G., Saotome, I., Haberman, A. M., & Greco, V. (2012). Live imaging of stem cell and progeny behaviour in physiological hair-follicle regeneration. Nature, 487(7408), 496–499.
270. Rompolas, P., Mesa, K. R., & Greco, V. (2013). Spatial organization within a niche as a determinant of stem-cell fate. Nature, 502(7472), 513–518.
271. Nam, S. C., Kim, Y., Dryanovski, D., Walker, A., Goings, G., Woolfrey, K., et al. (2007). Dynamic features of postnatal subventricular zone cell motility: a two-photon time-lapse study. The Journal of Comparative Neurology, 505(2), 190–208.
272. James, R., Kim, Y., Hockberger, P. E., & Szele, F. G. (2011). Subventricular zone cell migration: lessons from quantitative two-photon microscopy. Frontiers in Neuroscience, 5, 30.
273. Ortega, F., & Costa, M. R. (2016). Live imaging of adult neural stem cells in rodents. Frontiers in Neuroscience, 10, 78.
274. Sonego, M., Zhou, Y., Oudin, M.J., Doherty, P., Lalli, G. (2013). In vivo postnatal electroporation and time-lapse imaging of neuroblast migration in mouse acute brain slices. Journal of visualized experiments: JoVE. doi:10.3791/50905.
275. Cao, L., Pu, J., Scott, R. H., Ching, J., & McCaig, C. D. (2015). Physiological electrical signals promote chain migration of neuroblasts by up-regulating P2Y1 purinergic receptors and enhancing cell adhesion. Stem Cell Reviews, 11(1), 75–86.