A comprehensive model of the spatio-temporal stem cell and tissue organisation in the intestinal crypt

PLoS Computational Biology

Volumn 7, Issue 1, 2011, Pages

  Buske, Peter ^a   Galle, Jörg ^a   Barker, Nick ^b   Aust, Gabriela ^a   Clevers, Hans ^b   Loeffler, Markus ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; CELL SIGNALING; TISSUE;

CELLULAR LEVELS; CELLULARS; COMPREHENSIVE MODELING; DYNAMICS MODELS; MODEL LINKS; MOLECULAR LEVELS; SPATIO-TEMPORAL; STEM TISSUES; STEM-CELL; TISSUE LEVELS;

STEM CELLS;

BETA CATENIN; NOTCH RECEPTOR; WNT PROTEIN;

ANALYTIC METHOD; APOPTOSIS; ARTICLE; CALCULATION; CELL DAMAGE; CELL INTERACTION; CELL LINEAGE; CELL MIGRATION; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; INTESTINE CRYPT; MOUSE; NONHUMAN; PREDICTION; SIMULATION; STEM CELL; BIOLOGICAL MODEL; CYTOLOGY; INTESTINE; METABOLISM; SIGNAL TRANSDUCTION;

MURINAE;

APOPTOSIS; CELL PROLIFERATION; INTESTINES; MODELS, BIOLOGICAL; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STEM CELLS; WNT PROTEINS;

EID: 79551565619     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1001045     Document Type: Article

References (65)

1. Ireland H, Houghton C, Howard L, Winton DJ (2005) Cellular inheritance of a Cre-activated reporter gene to determine Paneth cell longevity in the murine small intestine. Dev Dyn 233: 1332-1336.
2. Potten CS (1975) Kinetics and possible regulation of crypt cell populations under normal and stress conditions. Bull Cancer 62: 419-430.
3. Barker N, van de Wetering M, Clevers H (2008) The intestinal stem cell. Genes Dev 22: 1856-1864.
4. Brittan M, Wright NA (2002) Gastrointestinal stem cells. J Pathol 197: 492-509.
5. Scoville DH, Sato T, He XC, Li L (2008) Current view: intestinal stem cells and signaling. Gastroenterology 134: 849-864.
6. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007.
7. Sangiorgi E, Capecchi MR (2009) Bmi1 lineage tracing identifies a self-renewing pancreatic acinar cell subpopulation capable of maintaining pancreatic organ homeostasis. Proc Natl Acad Sci U S A 106: 7101-7106.
8. Potten CS, Loeffler M (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110: 1001-1020.
9. Potten CS, Gandara R, Mahida YR, Loeffler M, Wright NA (2009) The stem cells of small intestinal crypts: where are they? Cell Prolif 42: 731-750.
10. Montgomery RK, Breault DT (2008) Small intestinal stem cell markers. J Anat 213: 52-58.
11. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, et al. (1998) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19: 379-383.
12. van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, et al. (2005) Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435: 959-963.
13. Hoffmann M, Chang HH, Huang S, Ingber DE, Loeffler M, et al. (2008) Noisedriven stem cell and progenitor population dynamics. PLoS One 3: e2922.
14. Loeffler M, Roeder I (2002) Tissue stem cells: definition, plasticity, heterogeneity, self-organization and models-a conceptual approach. Cells Tissues Organs 171: 8-26.
15. Loeffler M, Roeder I (2004) Conceptual models to understand tissue stem cell organization. Curr Opin Hematol 11: 81-87.
16. van der Flier LG, Clevers H (2009) Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 71: 241-260.
17. Gregorieff A, Clevers H (2005) Wnt signaling in the intestinal epithelium: from endoderm to cancer. Genes Dev 19: 877-890.
18. van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, et al. (2002) The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111: 241-250.
19. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, et al. (2002) Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111: 251-263.
20. Bastide P, Darido C, Pannequin J, Kist R, Robine S, et al. (2007) Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J Cell Biol 178: 635-648.
21. Andreu P, Colnot S, Godard C, Gad S, Chafey P, et al. (2005) Crypt-restricted proliferation and commitment to the Paneth cell lineage following Apc loss in the mouse intestine. Development 132: 1443-1451.
22. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, et al. (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265.
23. Ingber DE (2005) Mechanical control of tissue growth: function follows form. Proc Natl Acad Sci U S A 102: 11571-11572.
24. Nelson CM, Jean RP, Tan JL, Liu WF, Sniadecki NJ, et al. (2005) Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci U S A 102: 11594-11599.
25. Radtke F, Clevers H (2005) Self-renewal and cancer of the gut: two sides of a coin. Science 307: 1904-1909.
26. Nakamura T, Tsuchiya K, Watanabe M (2007) Crosstalk between Wnt and Notch signaling in intestinal epithelial cell fate decision. J Gastroenterol 42: 705-710.
27. Ehebauer M, Hayward P, Arias AM (2006) Notch, a universal arbiter of cell fate decisions. Science 314: 1414-1415.
28. Buchert M, Athineos D, Abud HE, Burke ZD, Faux MC, et al. (2010) Genetic dissection of differential signaling threshold requirements for the Wnt/betacatenin pathway in vivo. PLoS Genet 6: e1000816.
29. Sprinzak D, Lakhanpal A, Lebon L, Santat LA, Fontes ME, et al. (2010) Cisinteractions between Notch and Delta generate mutually exclusive signaling states. Nature 465: 86-90.
30. Collier JR, Monk NA, Maini PK, Lewis JH (1996) Pattern formation by lateral inhibition with feedback: a mathematical model of delta-notch intercellular signalling. J Theor Biol 183: 429-446.
31. Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, et al. (2005) Notch signals control the fate of immature progenitor cells in the intestine. Nature 435: 964-968.
32. van Es JH, Jay P, Gregorieff A, van Gijn ME, Jonkheer S, et al. (2005) Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 7: 381-386.
33. Fevr T, Robine S, Louvard D, Huelsken J (2007) Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol Cell Biol 27: 7551-7559.
34. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, et al. (2004) Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 18: 1385-1390.
35. Mori-Akiyama Y, van den Born M, van Es JH, Hamilton SR, Adams HP, et al. (2007) SOX9 is required for the differentiation of paneth cells in the intestinal epithelium. Gastroenterology 133: 539-546.
36. Galle J, Loeffler M, Drasdo D (2005) Modeling the effect of deregulated proliferation and apoptosis on the growth dynamics of epithelial cell populations in vitro. Biophys J 88: 62-75.
37. Galle J, Hoffmann M, Aust G (2009) From single cells to tissue architecture-a bottom-up approach to modelling the spatio-temporal organisation of complex multi-cellular systems. J Math Biol 58: 261-283.
38. Bullen TF, Forrest S, Campbell F, Dodson AR, Hershman MJ, et al. (2006) Characterization of epithelial cell shedding from human small intestine. Lab Invest 86: 1052-1063.
39. Marshman E, Ottewell PD, Potten CS, Watson AJ (2001) Caspase activation during spontaneous and radiation-induced apoptosis in the murine intestine. J Pathol 195: 285-292.
40. Chwalinski S, Potten CS (1989) Crypt base columnar cells in ileum of BDF1 male mice-their numbers and some features of their proliferation. Am J Anat 186: 397-406.
41. Bjerknes M, Cheng H (1981) The stem-cell zone of the small intestinal epithelium. II. Evidence from paneth cells in the newborn mouse. Am J Anat 160: 65-75.
42. Paulus U, Loeffler M, Zeidler J, Owen G, Potten CS (1993) The differentiation and lineage development of goblet cells in the murine small intestinal crypt: experimental and modelling studies. J Cell Sci 106(Pt 2): 473-483.
43. Li YQ, Roberts SA, Paulus U, Loeffler M, Potten CS (1994) The crypt cycle in mouse small intestinal epithelium. J Cell Sci 107(Pt 12): 3271-3279.
44. Winton DJ, Ponder BA (1990) Stem-cell organization in mouse small intestine. Proc Biol Sci 241: 13-18.
45. van der Flier LG, van Gijn ME, Hatzis P, Kujala P, Haegebarth A, et al. (2009) Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136: 903-912.
46. Potten CS, Loeffler M (1987) A comprehensive model of the crypts of the small intestine of the mouse provides insight into the mechanisms of cell migration and the proliferation hierarchy. J Theor Biol 127: 381-391.
47. Gerike TG, Paulus U, Potten CS, Loeffler M (1998) A dynamic model of proliferation and differentiation in the intestinal crypt based on a hypothetical intraepithelial growth factor. Cell Prolif 31: 93-110.
48. van Leeuwen IM, Mirams GR, Walter A, Fletcher A, Murray P, et al. (2009) An integrative computational model for intestinal tissue renewal. Cell Prolif 42: 617-636.
49. Meineke FA, Potten CS, Loeffler M (2001) Cell migration and organization in the intestinal crypt using a lattice-free model. Cell Prolif 34: 253-266.
50. Sangiorgi E, Capecchi MR (2008) Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40: 915-920.
51. Roeder I, Horn M, Glauche I, Hochhaus A, Mueller MC, et al. (2006) Dynamic modeling of imatinib-treated chronic myeloid leukemia: functional insights and clinical implications. Nat Med 12: 1181-1184.
52. Krinner A, Zscharnack M, Bader A, Drasdo D, Galle J (2009) Impact of oxygen environment on mesenchymal stem cell expansion and chondrogenic differentiation. Cell Prolif 42: 471-484.
53. Roeder I, Horn K, Sieburg HB, Cho R, Muller-Sieburg C, et al. (2008) Characterization and quantification of clonal heterogeneity among hematopoietic stem cells: a model-based approach. Blood 112: 4874-4883.
54. Eilken HM, Nishikawa S, Schroeder T (2009) Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 457: 896-900.
55. Oloumi A, McPhee T, Dedhar S (2004) Regulation of E-cadherin expression and beta-catenin/Tcf transcriptional activity by the integrin-linked kinase. Biochim Biophys Acta 1691: 1-15.
56. Oloumi A, Syam S, Dedhar S (2006) Modulation of Wnt3a-mediated nuclear beta-catenin accumulation and activation by integrin-linked kinase in mammalian cells. Oncogene 25: 7747-7757.
57. Lee JY, Marston DJ, Walston T, Hardin J, Halberstadt A, et al. (2006) Wnt/Frizzled signaling controls C. elegans gastrulation by activating actomyosin contractility. Curr Biol 16: 1986-1997.
58. Chisholm AD (2006) Gastrulation: Wnts signal constriction. Curr Biol 16: R874-876.
59. Cummings FW (2001) The interaction of surface geometry with morphogens. J Theor Biol 212: 303-313.
60. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, et al. (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457: 608-611.
61. Radford IR, Lobachevsky PN (2006) An enteroendocrine cell-based model for a quiescent intestinal stem cell niche. Cell Prolif 39: 403-414.
62. Yen TH, Wright NA (2006) The gastrointestinal tract stem cell niche. Stem Cell Rev 2: 203-212.
63. Li L, Clevers H (2010) Coexistence of quiescent and active adult stem cells in mammals. Science 327: 542-545.
64. Jin YH, Kim H, Ki H, Yang I, Yang N, et al. (2009) Beta-catenin modulates the level and transcriptional activity of Notch1/NICD through its direct interaction. Biochim Biophys Acta 1793: 290-299.
65. Haramis AP, Begthel H, van den Born M, van Es J, Jonkheer S, et al. (2004) De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 303: 1684-1686.