Toward a quantitative understanding of the Wnt/β-catenin pathway through simulation and experiment

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 5, Issue 4, 2013, Pages 391-407

  Lloyd Lewis, Bethan ^a,b   Fletcher, Alexander G ^c   Dale, Trevor C ^b   Byrne, Helen M ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYCLIN DEPENDENT KINASE; EXPORTIN 1; KARYOPHERIN; UVOMORULIN; WNT PROTEIN; ZINC FINGER PROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; CARCINOGENESIS; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CHEMICAL INTERACTION; CYTOPLASM; DROSOPHILA; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; LIGAND BINDING; MATHEMATICAL MODEL; NONHUMAN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; WNT SIGNALING PATHWAY;

BETA CATENIN; CELL COMMUNICATION; CELL CYCLE; HUMANS; MODELS, THEORETICAL; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84879319984     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.1221     Document Type: Article

References (124)

1. Nusse R. Wnt signaling in disease and in development. Cell Res 2005, 15:28-32.
2. Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell 2012, 149:1192-1205.
3. van Amerongen R. Alternative Wnt pathways and receptors. Cold Spring Harb Perspect Biol 2012, a007914.
4. MacDonald BT, He X. A finger on the pulse of Wnt receptor signaling. Cell Res 2012, 22:1410-1412.
5. Pinson KI, Brennan J, Monkley S, Avery BJ, Skarnes WC. An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 2000, 407:535-538.
6. Lu W, Yamamoto V, Ortega B, Baltimore D. Mammalian Ryk is a Wnt coreceptor required for stimulation of neurite outgrowth. Cell 2004, 119:97-108.
7. Hikasa H, Shibata M, Hiratani I, Taira M. The Xenopus receptor tyrosine kinase Xror2 modulates morphogenetic movements of the axial mesoderm and neuroectoderm via Wnt signaling. Development 2002, 129:5227-5239.
8. Kestler HA, Kuhl M. From individual Wnt pathways towards a Wnt signalling network. Phil Trans R Soc B 2008, 363:1333-1347.
9. Mikels AJ, Nusse R. Purified Wnt5a protein activates or inhibits β-catenin-TCF signaling depending on receptor context. PLoS Biol 2006, 4:e115.
10. Rui Y, Xu Z, Lin S, Li Q, Rui H, Luo W, Zhou HM, Cheung PY, Wu Z, Ye Z, et al. Axin stimulates p53 functions by activation of HIPK2 kinase through multimeric complex formation. EMBO J 2004, 23:4583-4594.
11. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science 1998, 281:1509-1512.
12. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, Ben-Ze'ev A. The cyclin D1 gene is a target of the β-catenin/LEF-1 pathway. Proc Natl Acad Sci U S A 1999, 96:5522-5527.
13. Ha NC, Tonozuka T, Stamos JL, Choi HJ, Weis WI. Mechanism of phosphorylation-dependent binding of APC to β-catenin and its role in β-catenin degradation. Mol Cell 2004, 15:511-521.
14. Rubinfeld B, Tice DA, Polakis P. Axin-dependent phosphorylation of the adenomatous polyposis coli protein mediated by casein kinase 1ε. J Biol Chem 2001, 276:39037-39045.
15. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X. Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002, 108:837-847.
16. Orford K, Crockett C, Jensen JP, Weissman AM, Byers SW. Serine phosphorylation-regulated ubiquitination and degradation of β-catenin. J Biol Chem 1997, 272:24735-24738.
17. Daniels DL, Weis WI. β-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat Struct Mol Biol 2005, 12:364-371.
18. Janda CY, Waghray D, Levin AM, Thomas C, Garcia KC. Structural basis of Wnt recognition by Frizzled. Science 2012, 337:59-64.
19. Cliffe A, Hamada F, Bienz M. A role of dishevelled in relocating axin to the plasma membrane during wingless signaling. Curr Biol 2003, 13:960-966.
20. Cong F, Schweizer L, Chamorro M, Varmus H. Requirement for a nuclear function of β-catenin in Wnt signaling. Mol Cell Biol 2003, 23:8462-8470.
21. Tyson JJ, Chen K, Novak B. Network dynamics and cell physiology. Nat Rev Mol Cell Biol 2001, 2:908-916.
22. De Jong H. Modeling and simulation of genetic regulatory systems: a literature review. J Comp Biol 2002, 9:67-103.
23. Gaffney EA, Monk N. Gene expression time delays and Turing pattern formation systems. Bull Math Biol 2006, 68:99-130.
24. Basan M, Idema T, Lenz M, Joanny JF, Risler T. A reaction-diffusion model of the cadherin-catenin system: a possible mechanism for contact inhibition and implications for tumorigenesis. Biophys J 2010, 98:2770-2779.
25. Arkin A, Ross J, McAdams HH. Stochastic kinetic analysis of developmental pathway bifurcation in phage λ-infected Escherichia coli cells. Genetics 1998, 149:1633-1648.
26. Mirams GR, Byrne HM, King JR. A multiple timescale analysis of a mathematical model of the Wnt/β-catenin signalling pathway. J Math Biol 2010, 60:131-160.
27. Goentoro L, Kirschner MW. Evidence that fold-change, and not absolute level, of β-catenin dictates Wnt signaling. Mol Cell 2009, 36:872-884.
28. Wawra C, Kuhl M, Kestler HA. Extended analyses of the Wnt/β-catenin pathway: robustness and oscillatory behaviour. FEBS Lett 2007, 581:4043-4048.
29. Kruger R, Heinrich R. Model reduction and analysis of robustness for the Wnt/β-catenin signal transduction pathway. Genome Inform 2004, 15:138-148.
30. Hernandez AR, Klein AM, Kirschner MW. Kinetic responses of β-catenin specify the sites of Wnt control. Science 2012, 338:1337-1340.
31. Kogan Y, Halevi-Tobias KE, Hochman G, Baczmanska AK, Leyns L, Agur Z. A new validated mathematical model of the Wnt signalling pathway predicts effective combinational therapy by sFRP and Dkk. Biochem J 2012, 444:115-125.
32. Tan CW, Gardiner BS, Hirokawa Y, Layton MJ, Smith DW, Burgess AW. Wnt signalling pathway parameters for mammalian cells. PloS One 2012, 7:e31882.
33. Lee E, Salic A, Kruger R, Heinrich R, Kirschner MW. The roles of APC and axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol 2003, 1:E10.
34. Kim D, Rath O, Kolch W, Cho KH. A hidden oncogenic positive feedback loop caused by crosstalk between Wnt and ERK pathways. Oncogene 2007, 26:4571-4579.
35. Cho KH, Baek S, Sung MH. Wnt pathway mutations selected by optimal β-catenin signaling for tumorigenesis. FEBS Lett 2006, 580:3665-3670.
36. Schmitz Y, Wolkenhauer O, Rateitschak K. Nucleo-cytoplasmic shuttling of APC can maximize β-catenin/TCF concentration. J Theor Biol 2011, 279:132-142.
37. van Leeuwen IM, Byrne HM, Jensen OE, King JR. Elucidating the interactions between the adhesive and transcriptional functions of β-catenin in normal and cancerous cells. J Theor Biol 2007, 247:77-102.
38. Shin SY, Rath O, Zebisch A, Choo SM, Kolch W, Cho KH. Functional roles of multiple feedback loops in extracellular signal-regulated kinase and Wnt signaling pathways that regulate epithelial-mesenchymal transition. Cancer Res 2010, 70:6715-6724.
39. Ramis-Conde I, Drasdo D, Anderson AR, Chaplain MA. Modeling the influence of the E-cadherin-β-catenin pathway in cancer cell invasion: a multiscale approach. Biophys J 2008, 95:155-165.
40. Mirams GR, Fletcher AG, Maini PK, Byrne HM. A theoretical investigation of the effect of proliferation and adhesion on monoclonal conversion in the colonic crypt. J Theor Biol 2012, 312:143-156.
41. Fletcher AG, Breward CJ, Chapman SJ. Mathematical modeling of monoclonal conversion in the colonic crypt. J Theor Biol 2012, 300:118-133.
42. Murray PJ, Kang JW, Mirams GR, Shin SY, Byrne HM, Maini PK, Cho KH. Modelling spatially regulated β-catenin dynamics and invasion in intestinal crypts. Biophys J 2010, 99:716-725.
43. Murray PJ, Walter A, Fletcher AG, Edwards CM, Tindall MJ, Maini PK. Comparing a discrete and continuum model of the intestinal crypt. Phys Biol 2011, 8:026011.
44. van Leeuwen IM, Mirams GR, Walter A, Fletcher A, Murray P, Osborne J, Varma S, Young SJ, Cooper J, Doyle B, et al. An integrative computational model for intestinal tissue renewal. Cell Prolif 2009, 42:617-636.
45. Buske P, Galle J, Barker N, Aust G, Clevers H, Loeffler M. A comprehensive model of the spatio-temporal stem cell and tissue organisation in the intestinal crypt. PLoS Comput Biol 2011, 7:e1001045.
46. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/β-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 2002, 22:1172-1183.
47. Niida A, Hiroko T, Kasai M, Furukawa Y, Nakamura Y, Suzuki Y, Sugano S, Akiyama T. DKK1, a negative regulator of Wnt signaling, is a target of the β-catenin//TCF pathway. Oncogene 2004, 23:8520-8526.
48. Hao H-X, Xie Y, Zhang Y, Charlat O, Oster E, Avello M, Lei H, Mickanin C, Liu D, Ruffner H, et al. ZNRF3 promotes Wnt receptor turnover in an R-spondin-sensitive manner. Nature 2012, 485:195-200.
49. Wehrli M, Dougan ST, Caldwell K, O'Keefe L, Schwartz S, Vaizel-Ohayon D, Schejter E, Tomlinson A, DiNardo S. arrow encodes an LDL-receptor-related protein essential for Wingless signalling Nature 2000, 407:527-530.
50. Bikkavilli RK, Malbon CC. Dishevelled-KSRP complex regulates Wnt signaling through post-transcriptional stabilization of β-catenin mRNA. J Cell Sci 2010, 123:1352-1362.
51. Bikkavilli RK, Malbon CC. Arginine methylation of G3BP1 in response to Wnt3a regulates β-catenin mRNA. J Cell Sci 2011, 124:2310-2320.
52. Furusawa C, Kaneko K. A dynamical-systems view of stem cell biology. Science 2012, 338:215-217.
53. Tymchyshyn O, Kwiatkowska M. Combining intra- and inter-cellular dynamics to investigate intestinal homeostasis. In: Fisher J, ed. Formal Methods in Systems Biology, vol 5054. Berlin, Heidelberg: Springer; 2008, 63-76.
54. Metcalfe c, Bienz M. Inhibition of GSK3 by Wnt signalling-two contrasting models. J Cell Sci 2011, 124:3537-3544.
55. van Amerongen R, Nawijn M, Franca-Koh J, Zevenhoven J, van der Gulden H, Jonkers J, Berns A. Frat is dispensable for canonical Wnt signaling in mammals. Genes Dev 2005, 19:425-430.
56. Cselenyi CS, Jernigan KK, Tahinci E, Thorne CA, Lee LA, Lee E. LRP6 transduces a canonical Wnt signal independently of Axin degradation by inhibiting GSK3's phosphorylation of β-catenin. Proc Natl Acad Sci U S A 2008, 105:8032-8037.
57. Wu G, Huang H, Garcia Abreu J, He X. Inhibition of GSK3 phosphorylation of β-catenin via phosphorylated PPPSPXS motifs of Wnt coreceptor LRP6. PLoS One 2009, 4:e4926.
58. Taelman VF, Dobrowolski R, Plouhinec J-L, Fuentealba LC, Vorwald PP, Gumper I, Sabatini DD, De Robertis EM. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 2010, 143:1136-1148.
59. Li VSW, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP, Mohammed S, Heck AJR, Maurice MM, Mahmoudi T, et al. Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell 2012, 149:1245-1256.
60. Major MB, Roberts BS, Berndt JD, Marine S, Anastas J, Chung N, Ferrer M, Yi X, Stoick-Cooper CL, von Haller PD, et al. New regulators of Wnt/β-catenin signaling revealed by integrative molecular screening. Sci Signal 2008, 1:1-12.
61. Tang W, Dodge M, Gundapaneni D, Michnoff C, Roth M, Lum L. A genome-wide RNAi screen for Wnt/β-catenin pathway components identifies unexpected roles for TCF transcription factors in cancer. Proc Natl Acad Sci U S A 2008, 105:9697-9702.
62. Dasgupta R, Kaykas A, Moon RT, Perrimon N. Functional genomic analysis of the Wnt-wingless signaling pathway. Science 2005, 308:826-832.
63. Röttinger E, Besnardeau L, Lepage T. A Raf/MEK/ ERK signaling pathway is required for development of the sea urchin embryo micromere lineage through phosphorylation of the transcription factor Ets. Development 2004, 131:1075-1087.
64. Yun MS, Kim SE, Jeon SH, Lee JS, Choi KY. Both ERK and Wnt/β-catenin pathways are involved in Wnt3a-induced proliferation. J Cell Sci 2005, 118:313-322.
65. McManus EJ, Sakamoto K, Armit LJ, Ronaldson L, Shpiro N, Marquez R, Alessi DR. Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knockin analysis. EMBO J 2005, 24:1571-1583.
66. Cajanek L, Adlerz L, Bryja V, Arenas E. WNT unrelated activities in commercially available preparations of recombinant WNT3a. J Cell Biochem 2010, 111:1077-1079.
67. Niehrs C, Shen J. Regulation of Lrp6 phosphorylation. Cell Mol Life Sci 2010, 67:2551-2562.
68. Cadigan KM, Liu YI. Wnt signaling: complexity at the surface. J Cell Sci 2006, 119:395-402.
69. Cadigan KM. TCFs and Wnt/β-catenin signaling: more than one way to throw the switch. In: Serge P, François P, eds. Current Topics in Developmental Biology, vol 98. Salt Lake City, UT: Academic Press; 2012, 1-34.
70. Fiedler M, Mendoza-Topaz C, Rutherford TJ, Mieszczanek J, Bienz M. Dishevelled interacts with the DIX domain polymerization interface of Axin to interfere with its function in down-regulating β-catenin. Proc Natl Acad Sci U S A 2011, 108:1937-1942.
71. Bilic J, Huang YL, Davidson G, Zimmermann T, Cruciat CM, Bienz M, Niehrs C. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 2007, 316:1619-1622.
72. Yamamoto H, Sakane H, Michiue T, Kikuchi A. Wnt3a and Dkk1 regulate distinct internalization pathways of LRP6 to tune the activation of β-catenin signaling. Dev Cell 2008, 15:37-48.
73. Kikuchi A, Yamamoto H. Regulation of Wnt signalling by receptor-mediated endocytosis. J Biochem 2007, 141:443-451.
74. Peifer M, Orsulic S, Sweeton D, Wieschaus E. A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development 1993, 118:1191-1207.
75. Willert K, Jones KA. Wnt signaling: is the party in the nucleus? Genes Dev 2006, 20:1394-1404.
76. Sharma M, Jamieson C, Johnson M, Molloy MP, Henderson BR. Specific armadillo repeat sequences facilitate β-catenin nuclear transport in live cells via direct binding to nucleoporins Nup62, Nup153 and RANBP2/Nup358. J Biol Chem 2011.
77. Henderson BR. Nuclear-cytoplasmic shuttling of APC regulates β-catenin subcellular localization and turnover. Nat Cell Biol 2000, 2:653-660.
78. Jamieson C, Sharma M, Henderson BR. Regulation of β-catenin nuclear dynamics by GSK-3β involves a LEF-1 positive feedback loop. Traffic 2011, 12:983-999.
79. Wiechens N, Heinle K, Englmeier L, Schohl A, Fagotto F. Nucleo-cytoplasmic shuttling of Axin, a negative regulator of the Wnt-β-catenin pathway. J Biol Chem 2004, 279:5263-5267.
80. Blythe SA, Cha SW, Tadjuidje E, Heasman J, Klein PS. β-catenin primes organizer gene expression by recruiting a histone H3 arginine 8 methyltransferase, Prmt2. Dev Cell 2010, 19:220-231.
81. Yap AS, Brieher WM, Gumbiner BM. Molecular and functional analysis of cadherin-based adherens junctions. Annu Rev Cell Dev Biol 1997, 13:119-146.
82. Gottardi CJ, Gumbiner BM. Distinct molecular forms of β-catenin are targeted to adhesive or transcriptional complexes. J Cell Biol 2004, 167:339-349.
83. Gottardi CJ, Wong E, Gumbiner BM. E-cadherin suppresses cellular transformation by inhibiting β-catenin signaling in an adhesion-independent manner. J Cell Biol 2001, 153:1049-1060.
84. Sadot E, Simcha I, Shtutman M, Ben-Ze'ev A, Geiger B. Inhibition of β-catenin-mediated transactivation by cadherin derivatives. Proc Natl Acad Sci U S A 1998, 95:15339-15344.
85. van de Wetering M, Barker N, Harkes IC, van der Heyden M, Dijk NJ, Hollestelle A, Klijn JG, Clevers H, Schutte M. Mutant E-cadherin breast cancer cells do not display constitutive Wnt signaling. Cancer Res 2001, 61:278-284.
86. Kuphal F, Behrens Jr. E-cadherin modulates Wnt-dependent transcription in colorectal cancer cells but does not alter Wnt-independent gene expression in fibroblasts. Exp Cell Res 2006, 312:457-467.
87. Herzig M, Savarese F, Novatchkova M, Semb H, Christofori G. Tumor progression induced by the loss of E-cadherin independent of β-catenin/Tcf-mediated Wnt signaling. Oncogene 2006, 26:2290-2298.
88. Heuberger J, Birchmeier W. Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2010, a002915.
89. Daugherty RL, Gottardi CJ. Phospho-regulation of β-catenin adhesion and signalling functions. Physiology 2007, 22:303-309.
90. Staal FJ, Noort Mv M, Strous GJ, Clevers HC. Wnt signals are transmitted through N-terminally dephosphorylated β-catenin. EMBO Rep 2002, 3:63-68.
91. Guger KA, Gumbiner BM. A mode of regulation of β-catenin signaling activity in Xenopus embryos independent of its levels. Dev Biol 2000, 223:441-448.
92. Maher MT, Mo R, Flozak AS, Peled ON, Gottardi CJ. β-Catenin phosphorylated at serine 45 is spatially uncoupled from β-catenin phosphorylated in the GSK3 domain: implications for signaling. PLoS One 2010, 5:e10184.
93. Roura S, Miravet S, Piedra J, de Herreros AG, Dunach M. Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J Biol Chem 1999, 274:36734-36740.
94. Piedra J. p120 Catenin-associated Fer and Fyn tyrosine kinases regulate β-catenin Tyr-142 phosphorylation and β-catenin-α-catenin interaction. Mol Cell Biol 2003, 23:2287-2297.
95. Brembeck FH, Schwarz-Romond T, Bakkers J, Wilhelm S, Hammerschmidt M, Birchmeier W. Essential role of BCL9-2 in the switch between β-catenin's adhesive and transcriptional functions. Genes Dev 2004, 18:2225-2230.
96. Buchert M, Athineos D, Abud HE, Burke ZD, Faux MC, Samuel MS, Jarnicki AG, Winbanks CE, Newton IP, Meniel VS, et al. Genetic dissection of differential signaling threshold requirements for the Wnt/β-catenin pathway in vivo. PLoS Genet 2010, 6:e1000816.
97. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715.
98. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, Itzkovitz S, Noske A, Zurrer-Hardi U, Bell G, et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 2012, 148:1015-1028.
99. Kemler R, Hierholzer A, Kanzler B, Kuppig S, Hansen K, Taketo MM, de Vries WN, Knowles BB, Solter D. Stabilization of β-catenin in the mouse zygote leads to premature epithelial-mesenchymal transition in the epiblast. Development 2004, 131:5817-5824.
100. Chen YT, Stewart DB, Nelson WJ. Coupling assembly of the E-cadherin/β-catenin complex to efficient endoplasmic reticulum exit and basal-lateral membrane targeting of E-cadherin in polarized MDCK cells. J Cell Biol 1999, 144:687-699.
101. Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, Knuechel R, Kirchner T. Variable β-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci U S A 2001, 98:10356-10361.
102. Miyoshi H, Ajima R, Luo CT, Yamaguchi TP, Stappenbeck TS. Wnt5a potentiates TGF-β signaling to promote colonic crypt regeneration after tissue injury. Science 2012, 338:108-113.
103. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
104. Gaspar C, Fodde R. APC dosage effects in tumorigenesis and stem cell differentiation. Int J Dev Biol 2004, 48:377-386.
105. Meineke FA, Potten CS, Loeffler M. Cell migration and organization in the intestinal crypt using a lattice-free model. Cell Prolif 2001, 34:253-266.
106. Whitehead J, Vignjevic D, Futterer C, Beaurepaire E, Robine S, Farge E. Mechanical factors activate ß-catenin-dependent oncogene expression in APC1638N/+ mouse colon. HFSP J 2008, 2:286-294.
107. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, Clevers H. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009, 457:608-611.
108. Hirata A, Utikal J, Yamashita S, Aoki H, Watanabe A, Yamamoto T, Okano H, Bardeesy N, Kunisada T, Ushijima T, et al. Dose-dependent roles for canonical Wnt signalling in de novo crypt formation and cell cycle properties of the colonic epithelium. Development 2013, 140:66-75.
109. Paulus U, Loeffler M, Zeidler J, Owen G, Potten CS. The differentiation and lineage development of goblet cells in the murine small intestinal crypt: experimental and modelling studies. J Cell Sci 1993, 106:473-483.
110. Winton DJ, Ponder BAJ. Stem-cell organization in mouse small intestine. Proc R Soc B 1990, 241:13-18.
111. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP, Batlle E, Simon-Assmann P, Clevers H, Nathke IS, et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 2004, 18:1385-1390.
112. van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, et al. Notch/γ-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 2005, 435:959-963.
113. Crampton SP, Wu B, Park EJ, Kim J-H, Solomon C, Waterman ML, Hughes CCW. Integration of the β-catenin-dependent Wnt pathway with integrin signaling through the adaptor molecule Grb2. PLoS One 2009, 4:e7841.
114. Tyson JJ, Csikasz-Nagy A, Novak B. The dynamics of cell cycle regulation. Bioessays 2002, 24:1095-1109.
115. Davidson G, Niehrs C. Emerging links between CDK cell cycle regulators and Wnt signaling. Trends Cell Biol 2010, 20:453-460.
116. Davidson G, Shen J, Huang YL, Su Y, Karaulanov E, Bartscherer K, Hassler C, Stannek P, Boutros M, Niehrs C. Cell cycle control of Wnt receptor activation. Dev Cell 2009, 17:788-799.
117. Niehrs C, Acebron SP. Mitotic and mitogenic Wnt signalling. EMBO J 2012, 31:2705-2713.
118. Hadjihannas MV, Bernkopf DB, Bruckner M, Behrens J. Cell cycle control of Wnt/β-catenin signalling by conductin/axin2 through CDC20. EMBO Rep 2012, 13:347-354.
119. Olmeda D, Castel S, Vilaro S, Cano A. β-Catenin regulation during the cell cycle: implications in G2/M and apoptosis. Mol Biol Cell 2003, 14:2844-2860.
120. Hayward P, Kalmar T, Martinez Arias A. Wnt/Notch signalling and information processing during development. Development 2008, 135:411-424.
121. Edwards CM, Chapman SJ. Biomechanical modelling of colorectal crypt budding and fission. Bull Math Biol 2007, 69:1927-1942.
122. Nelson MR, Howard D, Jensen OE, King JR, Rose FR, Waters SL. Growth-induced buckling of an epithelial layer. Biomech Model Mechanobiol 2011, 10:883-900.
123. Kitano H. Systems biology: a brief overview. Science 2002, 295:1662-1664.
124. Crudu A, Debussche A, Radulescu O. Hybrid stochastic simplifications for multiscale gene networks. BMC Syst Biol 2009, 3:89.