Strategies for homeostatic stem cell self-renewal in adult tissues

Cell

Volumn 145, Issue 6, 2011, Pages 851-862

  Simons, Benjamin D ^a,b   Clevers, Hans ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DAMAGE; CELL DIFFERENTIATION; CELL FATE; CELL MATURATION; CELL PROLIFERATION; CELL RENEWAL; DROSOPHILA; EPIDERMIS; GERM LINE; HOMEOSTASIS; HUMAN; INTESTINE EPITHELIUM; MAMMAL; MIDGUT; NERVOUS TISSUE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPERMATOGENESIS; STEM CELL; TISSUE TYPES;

EID: 79958263078     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.05.033     Document Type: Review

References (80)

1. L. Alonso, and E. Fuchs The hair cycle J. Cell Sci. 119 2006 391 393
2. N.T. Bailey Elements of Stochastic Processes with Applications to the Natural Sciences First Edition 1964 Wiley New York
3. N. Barker, J.H. van Es, J. Kuipers, P. Kujala, M. van den Born, M. Cozijnsen, A. Haegebarth, J. Korving, H. Begthel, and P.J. Peters Identification of stem cells in small intestine and colon by marker gene Lgr5 Nature 449 2007 1003 1007 (Pubitemid 350014593)
4. Y. Barrandon, and H. Green Three clonal types of keratinocyte with different capacities for multiplication Proc. Natl. Acad. Sci. USA 84 1987 2302 2306 (Pubitemid 17075859)
5. M. Bjerknes, and H. Cheng Multipotential stem cells in adult mouse gastric epithelium Am. J. Physiol. Gastrointest. Liver Physiol. 283 2002 G767 G777
6. C. Blanpain, and E. Fuchs Epidermal homeostasis: a balancing act of stem cells in the skin Nat. Rev. Mol. Cell Biol. 10 2009 207 217
7. C. Blanpain, W.E. Lowry, A. Geoghegan, L. Polak, and E. Fuchs Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche Cell 118 2004 635 648 (Pubitemid 39179715)
8. A.H. Brand, and N. Perrimon Targeted gene expression as a means of altering cell fates and generating dominant phenotypes Development 118 1993 401 415 (Pubitemid 23214028)
9. H. Cheng, and C.P. Leblond Origin, differentiation and renewal of 4 main epithelial cell types in mouse small intestine. 5 Unitarian theory of origin of 4 epithelial cell types Am. J. Anat. 141 1974 537
10. E. Clayton, D.P. Doupe, A.M. Klein, D.J. Winton, B.D. Simons, and P.H. Jones A single type of progenitor cell maintains normal epidermis Nature 446 2007 185 189 (Pubitemid 46398664)
11. G. Cotsarelis, T.-T. Sun, and R.M. Lavker Label-retaining cells reside in the bulge area of pilosebaceous unit: Implications for follicular stem cells, hair cycle, and skin carcinogenesis Cell 61 1990 1329 1337
12. D.G. de Rooij, and L.D. Russell All you wanted to know about spermatogonia but were afraid to ask J. Androl. 21 2000 776 798
13. W. Deng, and H. Lin Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila Dev. Biol. 189 1997 79 94 (Pubitemid 27402465)
14. C.Q. Doe, and B. Bowerman Asymmetric cell division: fly neuroblast meets worm zygote Curr. Opin. Cell Biol. 13 2001 68 75 (Pubitemid 32119295)
15. D.P. Doupe, A.M. Klein, B.D. Simons, and P.H. Jones The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate Dev. Cell 18 2010 317 323
16. B. Egger, J.M. Chell, and A.H. Brand Insights into neural stem cell biology from flies Philos. Trans. R. Soc. B. Biol. Sci. 363 2008 39 56 (Pubitemid 350174576)
17. T. Enver, C.M. Heyworth, and T.M. Dexter Do stem cells play dice? Blood 92 1998 348 351
18. P.J. Fialkow, R.J. Jacobson, and T. Papayannopoulou Chronic myelocytic leukemia: Clonal origin in a stem cell common to the granulocyte, erythrocyte, platelet and monocyte/macrophage Am. J. Med. 63 1977 125 130 (Pubitemid 8146659)
19. D.T. Fox, L.X. Morris, N. Nystul, and A.C. Spralding Lineage analysis of stem cells StemBook 2009 Harvard Stem Cell Institute Cambridge, MA
20. E. Fuchs, and V. Horsley Ferreting out stem cells from their niches Nat. Cell Biol. 13 2011 513 518
21. M.T. Fuller, and A.C. Spradling Male and female Drosophila germline stem cells: Two versions of immortality Science 316 2007 402 404 (Pubitemid 46651479)
22. D.A. Harrison, and N. Perrimon Simple and efficient generation of marked clones in Drosophila Curr. Biol. 3 1993 424 433
23. S.X. Hou Intestinal stem cell asymmetric division in the Drosophila posterior midgut J. Cell. Physiol. 224 2010 581 584
24. Y.-C. Hsu, H.A. Pasolli, and E. Fuchs Dynamics between stem cells, niche, and progeny in the hair follicle Cell 144 2011 92 105
25. M. Ito, Y. Liu, Z. Yang, J. Nguyen, F. Liang, R.J. Morris, and G. Cotsarelis Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis Nat. Med. 11 2005 1351 1354 (Pubitemid 41752917)
26. K.B. Jensen, C.A. Collins, E. Nascimento, D.W. Tan, M. Frye, S. Itami, and F.M. Watt Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis Cell Stem Cell 4 2009 427 439
27. P.H. Jones, S. Harper, and F.M. Watt Stem cell patterning and fate in human epidermis Cell 80 1995 83 93
28. C.T. Jordan, and I.R. Lemischka Clonal and systemic analysis of long-term hematopoiesis in the mouse Genes Dev. 4 1990 220 232
29. A.A. Kiger, D.L. Jones, C. Schulz, M.B. Rogers, and M.T. Fuller Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue Science 294 2001 2542 2545 (Pubitemid 34027293)
30. A.M. Klein, D.E. Brash, P.H. Jones, and B.D. Simons Stochastic fate of p53-mutant epidermal progenitor cells is tilted toward proliferation by UVB during preneoplasia Proc. Natl. Acad. Sci. USA 107 2010 270 275
31. A.M. Klein, T. Nakagawa, R. Ichikawa, S. Yoshida, and B.D. Simons Mouse germ line stem cells undergo rapid and stochastic turnover Cell Stem Cell 7 2010 214 224
32. A.M. Klein, and B.D. Simons Universal patterns of stem cell fate in cycling adult tissues Development 2011 in press. 101242/dev060103
33. J.L. Leatherman, and S. DiNardo Germline self-renewal requires cyst stem cells and stat regulates niche adhesion in Drosophila testes Nat. Cell Biol. 12 2010 806 811
34. V. Levy, C. Lindon, B.D. Harfe, and B.A. Morgan Distinct stem cell populations regenerate the follicle and interfollicular epidermis Dev. Cell 9 2005 855 861 (Pubitemid 41724112)
35. C. Lopez-Garcia, A.M. Klein, B.D. Simons, and D.J. Winton Intestinal stem cell replacement follows a pattern of neutral drift Science 330 2010 822 825
36. I.C. Mackenzie Relationship between mitosis and the ordered structure of the stratum corneum in mouse epidermis Nature 226 1970 653 655
37. C.A. Micchelli, and N. Perrimon Evidence that stem cells reside in the adult Drosophila midgut epithelium Nature 439 2006 475 479 (Pubitemid 43152838)
38. R.J. Morris, Y. Liu, L. Marles, Z. Yang, C. Trempus, S. Li, J.S. Lin, J.A. Sawicki, and G. Cotsarelis Capturing and profiling adult hair follicle stem cells Nat. Biotechnol. 22 2004 411 417 (Pubitemid 38451371)
39. S.J. Morrison, and J. Kimble Asymmetric and symmetric stem-cell divisions in development and cancer Nature 441 2006 1068 1074 (Pubitemid 43990718)
40. S.J. Morrison, and A.C. Spradling Stem cells and niches: Mechanisms that promote stem cell maintenance throughout life Cell 132 2008 598 611 (Pubitemid 351253690)
41. T. Nakagawa, Y.-i. Nabeshima, and S. Yoshida Functional identification of the actual and "potential" stem cell compartments in mouse spermatogenesis Dev. Cell 12 2007 195 206 (Pubitemid 46172906)
42. T. Nakagawa, M. Sharma, Y.-i. Nabeshima, R.E. Braun, and S. Yoshida Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment Science 328 2010 62 67
43. B. Ohlstein, and A. Spradling The adult Drosophila posterior midgut is maintained by pluripotent stem cells Nature 439 2006 470 474 (Pubitemid 43152837)
44. K.W. Orford, and D.T. Scadden Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation Nat. Rev. Genet. 9 2008 115 128
45. C.S. Potten, and C. Booth Keratinocyte stem cells: A commentary J. Invest. Dermatol. 119 2002 888 899 (Pubitemid 35340915)
46. C.S. Potten, and M. Loeffler Stem-cells-attributes, cycles, spirals, pitfalls and uncertainties-lessons for and from the crypt Development 110 1990 1001 1020 (Pubitemid 120009472)
47. C.S. Potten, L. Kovacs, and E. Hamilton Continuous labelling studies on mouse skin and intestine Cell Prolif. 7 1974 271 283
48. J.R. Rock, M.W. Onaitis, E.L. Rawlins, Y. Lu, C.P. Clark, Y. Xue, S.H. Randell, and B.L.M. Hogan Basal cells as stem cells of the mouse trachea and human airway epithelium Proc. Natl. Acad. Sci. USA 106 2009 12771 12775
49. A. Sada, A. Suzuki, H. Suzuki, and Y. Saga The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells Science 325 2009 1394 1398
50. E. Sangiorgi, and M.R. Capecchi Bmi1 is expressed in vivo in intestinal stem cells Nat. Genet. 40 2008 915 920 (Pubitemid 351913652)
51. T. Sato, J.H. van Es, H.J. Snippert, D.E. Stange, R.G. Vries, M. van den Born, N. Barker, N.F. Shroyer, M. van de Wetering, and H. Clevers Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts Nature 469 2010 415 418
52. T. Sato, R.G. Vries, H.J. Snippert, M. van de Wetering, N. Barker, D.E. Stange, J.H. van Es, A. Abo, P. Kujala, and P.J. Peters Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche Nature 459 2009 262 265
53. B. Sauer Inducible gene targeting in mice using the Cre/lox system Methods 14 1998 381 392
54. D.T. Scadden The stem-cell niche as an entity of action Nature 441 2006 1075 1079 (Pubitemid 43990719)
55. T. Schroeder Imaging stem-cell-driven regeneration in mammals Nature 453 2008 345 351 (Pubitemid 351693141)
56. X.R. Sheng, C.M. Brawley, and E.L. Matunis Dedifferentiating spermatogonia outcompete somatic stem cells for niche occupancy in the Drosophila testis Cell Stem Cell 5 2009 191 203
57. L. Siminovitch, E.A. McCulloch, and J.E. Till The distribution of colony-forming cells among spleen colonies J. Cell. Comp. Physiol. 62 1963 327 336
58. D.P. Slaughter, H.W. Southwick, and W. Smejkal "Field cancerization" in oral stratified squamous epithelium. Clinical implications of multicentric origin Cancer 6 1953 963 968
59. H.J. Snippert, and H. Clevers Tracking adult stem cells EMBO Rep. 12 2011 113 122
60. H.J. Snippert, J.H. van Es, M. van den Born, H. Begthel, D.E. Stange, N. Barker, and H. Clevers Prominin-1/CD133 marks stem cells and early progenitors in mouse small intestine Gastroenterology 136 2009 2187 2194 e1
61. H.J. Snippert, A. Haegebarth, M. Kasper, V. Jaks, J.H. van Es, N. Barker, M. van de Wetering, M. van den Born, H. Begthel, and R.G. Vries Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin Science 327 2010 1385 1389
62. H.J. Snippert, L.G. van der Flier, T. Sato, J.H. van Es, M. van den Born, C. Kroon-Veenboer, N. Barker, A.M. Klein, J. van Rheenen, and B.D. Simons Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells Cell 143 2010 134 144
63. P. Soriano Generalized lacZ expression with the ROSA26 Cre reporter strain Nat. Genet. 21 1999 70 71 (Pubitemid 29036285)
64. J. Takeda, T. Miyata, K. Kawagoe, Y. Iida, Y. Endo, T. Fujita, M. Takahashi, T. Kitani, and T. Kinoshita Deficiency of the GPI anchor caused by a somatic mutation of the PIG-A gene in paroxysmal nocturnal hemoglobinuria Cell 73 1993 703 711 (Pubitemid 23159009)
65. N. Tulina, and E. Matunis Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling Science 294 2001 2546 2549 (Pubitemid 34027294)
66. T. Tumbar, G. Guasch, V. Greco, C. Blanpain, W.E. Lowry, M. Rendl, and E. Fuchs Defining the epithelial stem cell niche in skin Science 303 2004 359 363 (Pubitemid 38095773)
67. L.G. van der Flier, M.E. van Gijn, P. Hatzis, P. Kujala, A. Haegebarth, D.E. Stange, H. Begthel, M. van den Born, V. Guryev, and I. Oving Transcription factor achaete scute-like 2 controls intestinal stem cell fate Cell 136 2009 903 912
68. J. Voog, and D.L. Jones Stem cells and the niche: A dynamic duo Cell Stem Cell 6 2010 103 115
69. F.M. Watt, and B.L.M. Hogan Out of Eden: Stem cells and their niches Science 287 2000 1427 1430 (Pubitemid 30127126)
70. A. Wilson, E. Laurenti, G. Oser, R.C. van der Wath, W. Blanco-Bose, M. Jaworski, S. Offner, C.F. Dunant, L. Eshkind, and E. Bockamp Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair Cell 135 2008 1118 1129
71. D.J. Winton, and B.A.J. Ponder Stem-cell organization in mouse small intestine Proc. R. Soc. Lond. B Biol. Sci. 241 1990 13 18 (Pubitemid 20256943)
72. D.J. Winton, M.A. Blount, and B.A.J. Ponder A clonal marker induced by mutation in mouse intestinal epithelium Nature 333 1988 463 466
73. N.A. Wright Epithelial stem cell repertoire in the gut: clues to the origin of cell lineages, proliferative units and cancer Int. J. Exp. Pathol. 81 2000 117 143 (Pubitemid 30253351)
74. T. Xie, and A.C. Spradling A niche maintaining germ line stem cells in the Drosophila ovary Science 290 2000 328 330
75. Y.M. Yamashita, D.L. Jones, and M.T. Fuller Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome Science 301 2003 1547 1550 (Pubitemid 37128549)
76. Y.M. Yamashita, A.P. Mahowald, J.R. Perlin, and M.T. Fuller Asymmetric inheritance of mother versus daughter centrosome in stem cell division Science 315 2007 518 521 (Pubitemid 46175756)
77. Y.M. Yamashita, H. Yuan, J. Cheng, and A.J. Hunt Polarity in stem cell division: Asymmetric stem cell division in tissue homeostasis Cold Spring Harb. Perspect. Biol. 2 2010 a001313
78. S. Yoshida, M. Sukeno, and Y.-i. Nabeshima A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis Science 317 2007 1722 1726 (Pubitemid 47461832)
79. Y.V. Zhang, J. Cheong, N. Ciapurin, D.J. McDermitt, and T. Tumbar Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells Cell Stem Cell 5 2009 267 278
80. L. Zhu, P. Gibson, D.S. Currle, Y. Tong, R.J. Richardson, I.T. Bayazitov, H. Poppleton, S. Zakharenko, D.W. Ellison, and R.J. Gilbertson Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation Nature 457 2009 603 607