Universal patterns of stem cell fate in cycling adult tissues

Development

Volumn 138, Issue 15, 2011, Pages 3103-3111

  Klein, Allon M ^a,b   Simons, Benjamin D ^b,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Stem cells; Stochastic cell fate; Tissue homeostasis

Indexed keywords

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL RENEWAL; CYCLING; GERM CELL; HOMEOSTASIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEMINIFEROUS TUBULE; SPERMATOGENESIS; STEM CELL; TISSUE REPAIR;

ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; GERM CELLS; HOMEOSTASIS; MODELS, BIOLOGICAL; STEM CELLS; STOCHASTIC PROCESSES;

EID: 79958268849     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.060103     Document Type: Article

References (69)

1. Ben-Naim, E., Frachebourg, L. and Krapivsky, P. L. (1996). Coarsening and persistence in the voter model. Phys. Rev. E 53, 3078-3087.
2. Bienayme, I. J. (1845). De la loi de multiplication et de la duree des familles. Soc. Philomath. Paris Extraits Ser. 5, 37-39.
3. Bramson, M. and Griffeath, D. (1980). Asymptotics for interacting particle systems on z^d. Probability Theory and Related Fields 53, 183-196.
4. Braun, K. M. and Watt, F. M. (2004). Epidermal label-retaining cells: background and recent applications. J. Invest. Dermatol. Symp. Proc. 9, 196-201.
5. Brawley, C. and Matunis, E. (2004). Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304, 1331.
6. Bullough, W. S. (1962). Growth control in mammalian skin. Nature 193, 520-523.
7. Cairns, J. (1975). Mutation selection and the natural history of cancer. Nature 255, 197-200.
8. Campos-Ortega, J. A. (1997). Asymmetic division: dynastic intricacies of neuroblast division. Curr. Biol. 7, R726-R728.
9. Canham, M. A., Sharov, A. A., Ko, M. S. and Brickman, J. M. (2010). Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biol. 8, e1000379.
10. Chang, H. H., Hemberg, M., Barahona, M., Ingber, D. E. and Huang, S. (2008). Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453, 544-547.
11. Cheng, H. and Leblond, C. P. (1974). Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian theory of the origin of the four epithelial cell types. Am. J. Anat. 141, 537-561.
12. Clayton, E., Doupe, D. P., Klein, A. M., Winton, D. J., Simons, B. D. and Jones, P. H. (2007). A single type of progenitor cell maintains normal epidermis. Nature 446, 185-189.
13. Cotsarelis, G., Sun, T. T. and Lavker, R. M. (1990). Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61, 1329-1337.
14. de Rooij, D. G. and Russell, L. D. (2000). All you wanted to know about spermatogonia but were afraid to ask. J. Androl. 21, 776.
15. Doupe, D. P., Klein, A. M., Simons, B. D. and Jones, P. H. (2010). The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate. Dev. Cell 18, 317-323.
16. Elgjo, K. (1969). Cell renewal of the normal mouse cornea. Acta Pathol. Microbiol. Scand. 76, 25-30.
17. Enver, T., Pera, M., Peterson, C. and Andrews, P. W. (2009). Stem cell states, fates, and the rules of attraction. Cell Stem Cell 4, 387-397.
18. Epstein, W. L. and Maibach, H. I. (1965). Cell renewal in human epidermis. Arch. Dermatol. 92, 462-468.
19. Frachebourg, L. and Krapivsky, P. L. (1996). Exact results for kinetics of catalytic reactions. Phys. Rev. E Stat. Phys. 53, R3009-R3012.
20. Gonczy, P. (2008). Mechanisms of asymmetric cell division: flies and worms pave the way. Nat. Rev. Mol. Cell Biol. 9, 355-366.
21. Harris, T. E. (1948). Branching processes. Ann. Math. Stat. 19, 474.
22. Holley, R. A. and Liggett, T. M. (1975). Ergodic theorems for weakly interacting systems and the voter model. Ann. Probab. 8, 643-663.
23. Kai, T. and Spradling, A. (2004). Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428, 564-569.
24. Kalmar, T., Lim, C., Hayward, P., Munoz-Descalzo, S., Nichols, J., Garcia- Ojalvo, J. and Martinez Arias, A. (2009). Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells. PLoS Biol. 7, e1000149.
25. Kiel, M. J., He, S., Ashkenazi, R., Gentry, S. N., Teta, M., Kushner, J. A., Jackson, T. L. and Morrison, S. J. (2007). Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature 449, 238-242.
26. Kimura, M. (1983). The Neutral Theory of Molecular Evolution. Cambridge and New York: Cambridge University Press.
27. Kimura, M. and Weiss, G. H. (1964). The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49, 561.
28. Klein, A. M., Brash, D. E., Jones, P. H. and Simons, B. D. (2010a). Stochastic fate of p53-mutant epidermal progenitor cells is tilted toward proliferation by UV B during preneoplasia. Proc. Natl. Acad. Sci. USA 107, 270-275.
29. Klein, A. M., Nakagawa, T., Ichikawa, R., Yoshida, S. and Simons, B. D. (2010b). Mouse germ line stem cells undergo rapid and stochastic turnover. Cell Stem Cell 7, 214-224.
30. Knoblich, J. A. (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
31. Kobayashi, T., Mizuno, H., Imayoshi, I., Furusawa, C., Shirahige, K. and Kageyama, R. (2009). The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Genes Dev. 23, 1870-1875.
32. Korolev, K. S., Avlund, M., Hallatschek, O. and Nelson, D. R. (2010). Genetic demixing and evolution in linear stepping stone models. Rev. Mod. Phys. 82, 1691.
33. Krapivsky, P. L. (1992). Kinetics of monomer-monomer surface catalytic reactions. Phys. Rev. A 45, 1067-1072.
34. Kuang, S., Kuroda, K., Le Grand, F. and Rudnicki, M. A. (2007). Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129, 999-1010.
35. Lajtha, L. G. (1979). Stem cell concepts. Differentiation 14, 23-34.
36. Leblond, C. P. (1981). The life history of cells in renewing systems. Am. J. Anat. 160, 114-158.
37. Leblond, C. P., Greulich, R. C. and Marques-Pereira, J. P. (1964). Relationship of cell formation and cell migration in the renewal of stratified squameous epithelia. Adv. Biol. Skin 5, 39-67.
38. Li, L. and Xie, T. (2005). Stem cell niche: structure and function. Annu. Rev. Cell Dev. Biol. 21, 605.
39. Liggett, T. M. (1985). Interacting Particle Systems. New York: Springer-Verlag.
40. Lopez-Garcia, C., Klein, A. M., Simons, B. D. and Winton, D. J. (2010). Intestinal stem cell replacement follows a pattern of neutral drift. Science 330, 822-825.
41. Losick, R. and Desplan, C. (2008). Stochasticity and cell fate. Science 320, 65-68.
42. Marques-Pereira, J. P. and Leblond, C. P. (1965). Mitosis and differentiation in the stratified squamous epithelium of the rat esophagus. Am. J. Anat. 117, 73-87.
43. Mombaerts, P. (2004). Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr. Opin. Neurobiol. 14, 31-36.
44. Montgomery, R. K., Carlone, D. L., Richmond, C. A., Farilla, L., Kranendonk, M. E., Henderson, D. E., Baffour-Awuah, N. Y., Ambruzs, D. M., Fogli, L. K., Algra, S. et al. (2011). Mouse telomerase reverse transcriptase (mTert) expression marks slowly cycling intestinal stem cells. Proc. Natl. Acad. Sci. USA 108, 179-184.
45. Moran, P. A. P. (1962). The Statistical Processes of Evolutionary Theory. Oxford: Clarendon Press.
46. Morrison, S. J. and Kimble, J. (2006). Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441, 1068-1074.
47. Mort, R. L., Ramaesh, T., Kleinjan, D. A., Morley, S. D. and West, J. D. (2009). Mosaic analysis of stem cell function and wound healing in the mouse corneal epithelium. BMC Dev. Biol. 9, 4.
48. Nakagawa, T., Nabeshima, Y. and Yoshida, S. (2007). Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev. Cell 12, 195.
49. Nakagawa, T., Sharma, M., Nabeshima, Y., Braun, R. E. and Yoshida, S. (2010). Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 328, 62-67.
50. Potten, C. S. and Loeffler, M. (1990). Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110, 1001-1020.
51. Quyn, A. J., Appleton, P. L., Carey, F. A., Steele, R. J., Barker, N., Clevers, H., Ridgway, R. A., Sansom, O. J. and Nathke, I. S. (2010). Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 6, 175-181.
52. Rubin, H. (2002). The disparity between human cell senescence in vitro and lifelong replication in vivo. Nat. Biotechnol. 20, 675-681.
53. Russell, L., Ettlin, R., Sinha Hikim, A. and Clegg, E. (1990). Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River Press.
54. Sada, A., Suzuki, A., Suzuki, H. and Saga, Y. (2009). The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 325, 1394-1398.
55. Sawyer, S. (1979). A limit theorem for patch sizes in a selectively-neutral migration model. J. Appl. Probab. 16, 482-495.
56. Schroeder, T. (2007). Asymmetric cell division in normal and malignant hematopoietic precursor cells. Cell Stem Cell 1, 479-481.
57. Sheng, X. R., Brawley, C. M. and Matunis, E. L. (2009). Dedifferentiating spermatogonia outcompete somatic stem cells for niche occupancy in the Drosophila testis. Cell Stem Cell 5, 191-203.
58. Smallwood, P. M., Wang, Y. and Nathans, J. (2002). Role of a locus control region in the mutually exclusive expression of human red and green cone pigment genes. Proc. Natl. Acad. Sci. USA 99, 1008-1011.
59. Snippert, H. J., van der Flier, L. G., Sato, T., van Es, J. H., van den Born, M., Kroon-Veenboer, C., Barker, N., Klein, A. M., van Rheenen, J., Simons, B. D. et al. (2010). Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143, 134-144.
60. Sood, V. and Redner, S. (2005). Voter model on heterogeneous graphs. Phys. Rev. Lett. 94, 178701.
61. Sudbury, A. (1976). The size of the region occupied by one type in an invasion process. J. Appl. Probab. 13, 355-356.
62. Till, J. E., McCulloch, E. A. and Siminovitch, L. (1964). A stochastic model of stem cell proliferation, based on the growth of spleen colony-forming cells. Proc. Natl. Acad. Sci. USA 51, 29-36.
63. van Kampen, N. G. (2007). Stochastic Processes in Physics and Chemistry. Amsterdam and London: Elsevier.
64. Voog, J. and Jones, D. L. (2010). Stem cells and the niche: a dynamic duo. Cell Stem Cell 6, 103-115.
65. Watt, F. M. and Hogan, B. L. (2000). Out of Eden: stem cells and their niches. Science 287, 1427-1430.
66. Wernet, M. F., Mazzoni, E. O., Celik, A., Duncan, D. M., Duncan, I. and Desplan, C. (2006). Stochastic spineless expression creates the retinal mosaic for colour vision. Nature 440, 174-180.
67. Wiktor-Brown, D. M., Kwon, H. S., Nam, Y. S., So, P. T. and Engelward, B. P. (2008). Integrated one- and two-photon imaging platform reveals clonal expansion as a major driver of mutation load. Proc. Natl. Acad. Sci. USA 105, 10314-10319.
68. Wu, M., Kwon, H. Y., Rattis, F., Blum, J., Zhao, C., Ashkenazi, R., Jackson, T. L., Gaiano, N., Oliver, T. and Reya, T. (2007). Imaging hematopoietic precursor division in real time. Cell Stem Cell 1, 541-554.
69. Yoshida, S., Sukeno, M. and Nabeshima, Y. (2007). A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317, 1722.