Age-Dependent Transition from Cell-Level to Population-Level Control in Murine Intestinal Homeostasis Revealed by Coalescence Analysis

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In multi-cellular organisms, tissue homeostasis is maintained by an exquisite balance between stem cell proliferation and differentiation. This equilibrium can be achieved either at the single cell level (a.k.a. cell asymmetry), where stem cells follow strict asymmetric divisions, or the population level (a.k.a. population asymmetry), where gains and losses in individual stem cell lineages are randomly distributed, but the net effect is homeostasis. In the mature mouse intestinal crypt, previous evidence has revealed a pattern of population asymmetry through predominantly symmetric divisions of stem cells. In this work, using population genetic theory together with previously published crypt single-cell data obtained at different mouse life stages, we reveal a strikingly dynamic pattern of stem cell homeostatic control. We find that single-cell asymmetric divisions are gradually replaced by stochastic population-level asymmetry as the mouse matures to adulthood. This lifelong process has important developmental and evolutionary implications in understanding how adult tissues maintain their homeostasis integrating the trade-off between intrinsic and extrinsic regulations.

Vyšlo v časopise: Age-Dependent Transition from Cell-Level to Population-Level Control in Murine Intestinal Homeostasis Revealed by Coalescence Analysis. PLoS Genet 9(2): e32767. doi:10.1371/journal.pgen.1003326
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003326

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Zdroje

1. Wolpert L, Tickle C (2010) Principles of Development. Oxford University Press, USA.

2. Cannon WB (1963) Wisdom Of The Body. W. W. Norton and Company, Inc.

3. BeckerAJ, McCE, TillJE (1963) Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 197 : 452–454.

4. MooreKA, LemischkaIR (2006) Stem cells and their niches. Science 311 : 1880–1885.

5. MorrisonSJ, KimbleJ (2006) Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441 : 1068–1074.

6. DoetschF, CailleI, LimDA, Garcia-VerdugoJM, Alvarez-BuyllaA (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97 : 703–716.

7. KimbleJE, WhiteJG (1981) On the control of germ cell development in Caenorhabditis elegans. Dev Biol 81 : 208–219.

8. LiL, XieT (2005) Stem cell niche: structure and function. Annu Rev Cell Dev Biol 21 : 605–631.

9. SchofieldR (1978) The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4 : 7–25.

10. WattFM, HoganBL (2000) Out of Eden: stem cells and their niches. Science 287 : 1427–1430.

11. KnoblichJA (2008) Mechanisms of asymmetric stem cell division. Cell 132 : 583–597.

12. MorrisonSJ, SpradlingAC (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132 : 598–611.

13. ClaytonE, DoupeDP, KleinAM, WintonDJ, SimonsBD, et al. (2007) A single type of progenitor cell maintains normal epidermis. Nature 446 : 185–189.

14. SimonsBD, CleversH (2011) Strategies for homeostatic stem cell self-renewal in adult tissues. Cell 145 : 851–862.

15. BjerknesM, ChengH (1999) Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 116 : 7–14.

16. CrosnierC, StamatakiD, LewisJ (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 7 : 349–359.

17. MarshmanE, BoothC, PottenCS (2002) The intestinal epithelial stem cell. Bioessays 24 : 91–98.

18. van der FlierLG, CleversH (2009) Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71 : 241–260.

19. el MarjouF, JanssenKP, ChangBH, LiM, HindieV, et al. (2004) Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39 : 186–193.

20. IrelandH, KempR, HoughtonC, HowardL, ClarkeAR, et al. (2004) Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: effect of loss of beta-catenin. Gastroenterology 126 : 1236–1246.

21. SauerB (1998) Inducible gene targeting in mice using the Cre/lox system. Methods 14 : 381–392.

22. BarkerN, van EsJH, KuipersJ, KujalaP, van den BornM, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 : 1003–1007.

23. Lopez-GarciaC, KleinAM, SimonsBD, WintonDJ (2010) Intestinal stem cell replacement follows a pattern of neutral drift. Science 330 : 822–825.

24. SnippertHJ, van der FlierLG, SatoT, van EsJH, van den BornM, et al. (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143 : 134–144.

25. ItzkovitzS, BlatIC, JacksT, CleversH, van OudenaardenA (2012) Optimality in the development of intestinal crypts. Cell 148 : 608–619.

26. QuynAJ, AppletonPL, CareyFA, SteeleRJ, BarkerN, et al. (2010) Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 6 : 175–181.

27. SternCD, FraserSE (2001) Tracing the lineage of tracing cell lineages. Nat Cell Biol 3: E216–218.

28. ReizelY, Chapal-IlaniN, AdarR, ItzkovitzS, ElbazJ, et al. (2011) Colon stem cell and crypt dynamics exposed by cell lineage reconstruction. PLoS Genet 7: e1002192.

29. BakerSM, PlugAW, ProllaTA, BronnerCE, HarrisAC, et al. (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13 : 336–342.

30. Ewens WJ (2004) Mathematical Population Genetics. New York: Springer.

31. KingmanJFC (1982) The coalescent. Stochast Proc Appl 13 : 235–248.

32. KingmanJFC (1982) On the genealogy of large populations. J Appl Prob 19A: 27–43.

33. Wakeley J (2008) Coalescent Theory: An Introduction. Roberts & Company Publishers. 432 p.

34. FuYX (2006) Exact coalescent for the Wright-Fisher model. Theor Popul Biol 69 : 385–394.

35. FelsensteinJ (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17 : 368–376.

36. MetropolisN, UlamS (1949) The Monte Carlo method. J Am Stat Assoc 44 : 335–341.

37. Efron B, Tibshirani RJ (1994) An Introduction to the Bootstrap. Chapman and Hall. 456 p.

38. de NavascuesJ, PerdigotoCN, BianY, SchneiderMH, BardinAJ, et al. (2012) Drosophila midgut homeostasis involves neutral competition between symmetrically dividing intestinal stem cells. EMBO J 31 : 2473–2485.

39. CaussinusE, GonzalezC (2005) Induction of tumor growth by altered stem-cell asymmetric division in Drosophila melanogaster. Nat Genet 37 : 1125–1129.

40. FloresI, CayuelaML, BlascoMA (2005) Effects of telomerase and telomere length on epidermal stem cell behavior. Science 309 : 1253–1256.

41. RandoTA (2006) Stem cells, ageing and the quest for immortality. Nature 441 : 1080–1086.

42. SatoT, van EsJH, SnippertHJ, StangeDE, VriesRG, et al. (2011) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469 : 415–418.

43. ChakkalakalJV, JonesKM, BassonMA, BrackAS (2012) The aged niche disrupts muscle stem cell quiescence. Nature 490 : 355–360.

44. ConboyIM, ConboyMJ, WagersAJ, GirmaER, WeissmanIL, et al. (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433 : 760–764.

45. MedzhitovR (2008) Origin and physiological roles of inflammation. Nature 454 : 428–435.

46. BuchonN, BroderickNA, ChakrabartiS, LemaitreB (2009) Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev 23 : 2333–2344.

47. CroninSJ, NehmeNT, LimmerS, LiegeoisS, PospisilikJA, et al. (2009) Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 325 : 340–343.

48. DingliD, TraulsenA, MichorF (2007) (A)symmetric stem cell replication and cancer. PLoS Comput Biol 3: e53.

49. WilliamsGC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11 : 398–411.

50. CongdonKL, ReyaT (2008) Divide and conquer: how asymmetric division shapes cell fate in the hematopoietic system. Curr Opin Immunol 20 : 302–307.

51. WuM, KwonHY, RattisF, BlumJ, ZhaoC, et al. (2007) Imaging hematopoietic precursor division in real time. Cell Stem Cell 1 : 541–554.

52. SharplessNE, DePinhoRA (2007) How stem cells age and why this makes us grow old. Nat Rev Mol Cell Biol 8 : 703–713.

53. GotzM, HuttnerWB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6 : 777–788.

54. LechlerT, FuchsE (2005) Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437 : 275–280.

55. PoulsonND, LechlerT (2010) Robust control of mitotic spindle orientation in the developing epidermis. J Cell Biol 191 : 915–922.

56. EmaH, TakanoH, SudoK, NakauchiH (2000) In vitro self-renewal division of hematopoietic stem cells. J Exp Med 192 : 1281–1288.

57. TakanoH, EmaH, SudoK, NakauchiH (2004) Asymmetric division and lineage commitment at the level of hematopoietic stem cells: inference from differentiation in daughter cell and granddaughter cell pairs. J Exp Med 199 : 295–302.

58. PennisiE (2012) The biology of genomes. Single-cell sequencing tackles basic and biomedical questions. Science 336 : 976–977.

59. ZongC, LuS, ChapmanAR, XieXS (2012) Genome-wide detection of single-nucleotide and copy-number variations of a single human cell. Science 338 : 1622–1626.

60. PottenCS, LoefflerM (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110 : 1001–1020.

61. SchepersAG, SnippertHJ, StangeDE, van den BornM, van EsJH, et al. (2012) Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 337 : 730–735.

62. ChengH, BjerknesM (1985) Whole population cell kinetics and postnatal development of the mouse intestinal epithelium. Anat Rec 211 : 420–426.

63. DehmerJJ, GarrisonAP, SpeckKE, DekaneyCM, Van LandeghemL, et al. (2011) Expansion of intestinal epithelial stem cells during murine development. PLoS One 6: e27070.

64. Ross MS (2006) Simulation. Academic Press. 312 p.

65. YangZ (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39 : 306–314.

66. SokalR, MichenerC (1958) A statistical method for evaluating systematic relationships. University of Kansas Science Bulletin 38 : 1409–1438.

67. PopescuAA, HuberKT, ParadisE (2012) ape 3.0: New tools for distance-based phylogenetics and evolutionary analysis in R. Bioinformatics 28 : 1536–1537.