Wnt signaling in stem and cancer stem cells

Current Opinion in Cell Biology

Volumn 25, Issue 2, 2013, Pages 254-264

  Holland, Jane D ^a   Klaus, Alexandra ^a   Garratt, Alistair N ^b   Birchmeier, Walter ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; FRIZZLED PROTEIN; WNT PROTEIN; WNT1 PROTEIN; WNT3A PROTEIN;

ADULT STEM CELL; ARTICLE; CANCER GROWTH; CANCER STEM CELL; CARCINOGENESIS; CELL ADHESION; CELL CYCLE PROGRESSION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; WNT SIGNALING PATHWAY; ANIMAL; ANIMAL EMBRYO; CELL TRANSFORMATION; CYTOLOGY; GENETIC TRANSCRIPTION; HEMATOPOIETIC SYSTEM; INTESTINE; MAMMARY GLAND; METABOLISM; NERVOUS SYSTEM; PATHOLOGY; PLURIPOTENT STEM CELL; PRENATAL DEVELOPMENT; REVIEW; SKIN; STEM CELL; SUMOYLATION; UBIQUITINATION;

ANIMALS; BETA CATENIN; CELL TRANSFORMATION, NEOPLASTIC; EMBRYO, MAMMALIAN; HEMATOPOIETIC SYSTEM; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INTESTINES; MAMMARY GLANDS, HUMAN; NEOPLASTIC STEM CELLS; NERVOUS SYSTEM; PLURIPOTENT STEM CELLS; SKIN; STEM CELLS; SUMOYLATION; TRANSCRIPTION, GENETIC; UBIQUITINATION; WNT PROTEINS; WNT SIGNALING PATHWAY;

MLCS; MLOWN;

EID: 84877929153     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2013.01.004     Document Type: Review

References (99)

1. Clevers H: Wnt/beta-catenin signaling in development and disease. Cell 2006, 127:469-480.
2. Klaus A, Birchmeier W: Wnt signalling and its impact on development and cancer. Nat Rev Cancer 2008, 8:387-398.
3. Wend P, Holland JD, Ziebold U, Birchmeier W: Wnt signaling in stem and cancer stem cells. Semin Cell Dev Biol 2010, 21:855-863.
4. Malanchi I, Peinado H, Kassen D, Hussenet T, Metzger D, Chambon P, Huber M, Hohl D, Cano A, Birchmeier W, Huelsken J: Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 2008, 452:650-653.
5. Carmon KS, Gong X, Lin Q, Thomas A, Liu Q: R-spondins function as ligands of the orphan receptors lgr4 and lgr5 to regulate wnt/beta-catenin signaling. Proc Natl Acad Sci USA 2011, 108:11452-11457.
6. de Lau W, Barker N, Low TY, Koo BK, Li VS, Teunissen H, Kujala P, Haegebarth A, Peters PJ, van de Wetering M et al.: Lgr5 homologues associate with wnt receptors and mediate rspondin signalling. Nature 2011, 476:293-297.
7. Janda CY, Waghray D, Levin AM, Thomas C, Garcia KC: Structural basis of wnt recognition by frizzled. Science 2012, 337:59-64.
8. Zhang X, Abreu JG, Yokota C, MacDonald BT, Singh S, Coburn KL, Cheong SM, Zhang MM, Ye QZ, Hang HC et al.: Tiki1 is required for head formation via wnt cleavage-oxidation and inactivation. Cell 2012, 149:1565-1577.
9. Cheng Z, Biechele T, Wei Z, Morrone S, Moon RT, Wang L, Xu W: Crystal structures of the extracellular domain of lrp6 and its complex with dkk1. Nat Struct Mol Biol 2011, 18:1204-1210.
10. Bazan JF, Janda CY, Garcia KC: Structural architecture and functional evolution of wnts. Dev Cell 2012, 23:227-232.
11. Cruciat CM, Ohkawara B, Acebron SP, Karaulanov E, Reinhard C, Ingelfinger D, Boutros M, Niehrs C: Requirement of prorenin receptor and vacuolar h+-atpase-mediated acidification for wnt signaling. Science 2010, 327:459-463.
12. Taelman VF, Dobrowolski R, Plouhinec JL, 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.
13. Li VS, Ng SS, Boersema PJ, Low TY, Karthaus WR, Gerlach JP, Mohammed S, Heck AJ, Maurice MM, Mahmoudi T, Clevers H: Wnt signaling through inhibition of beta-catenin degradation in an intact axin1 complex. Cell 2012, 149:1245-1256.
14. 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 beta-catenin. Proc Natl Acad Sci USA 2011, 108:1937-1942.
15. Waaler J, Machon O, Tumova L, Dinh H, Korinek V, Wilson SR, Paulsen JE, Pedersen NM, Eide TJ, Machonova O et al.: A novel tankyrase inhibitor decreases canonical wnt signaling in colon carcinoma cells and reduces tumor growth in conditional apc mutant mice. Cancer Res 2012, 72:2822-2832.
16. Morrone S, Cheng Z, Moon RT, Cong F, Xu W: Crystal structure of a tankyrase-axin complex and its implications for axin turnover and tankyrase substrate recruitment. Proc Natl Acad Sci USA 2012, 109:1500-1505.
17. Chilov D, Sinjushina N, Rita H, Taketo MM, Makela TP, Partanen J: Phosphorylated beta-catenin localizes to centrosomes of neuronal progenitors and is required for cell polarity and neurogenesis in developing midbrain. Dev Biol 2011, 357:259-268.
18. Mosimann C, Hausmann G, Basler K: Beta-catenin hits chromatin: regulation of wnt target gene activation. Nat Rev Mol Cell Biol 2009, 10:276-286.
19. Valenta T, Gay M, Steiner S, Draganova K, Zemke M, Hoffmans R, Cinelli P, Aguet M, Sommer L, Basler K: Probing transcriptionspecific outputs of beta-catenin in vivo. Genes Dev 2011, 25:2631-2643.
20. Hikasa H, Ezan J, Itoh K, Li X, Klymkowsky MW, Sokol SY: Regulation of tcf3 by wnt-dependent phosphorylation during vertebrate axis specification. Dev Cell 2010, 19:521-532.
21. Zhang N, Wei P, Gong A, Chiu WT, Lee HT, Colman H, Huang H, Xue J, Liu M, Wang Y et al.: Foxm1 promotes beta-catenin nuclear localization and controls wnt target-gene expression and glioma tumorigenesis. Cancer Cell 2011, 20:427-442.
22. Yu Y, Wu J, Wang Y, Zhao T, Ma B, Liu Y, Fang W, Zhu WG, Zhang H: Kindlin 2 forms a transcriptional complex with betacatenin and tcf4 to enhance wnt signalling. EMBO Rep 2012, 13:750-758.
23. Hadjihannas MV, Bernkopf DB, Bruckner M, Behrens J: Cell cycle control of wnt/beta-catenin signalling by conductin/axin2 through cdc20. EMBO Rep 2012, 13:347-354.
24. Brembeck FH, Wiese M, Zatula N, Grigoryan T, Dai Y, Fritzmann J, Birchmeier W: Bcl9-2 promotes early stages of intestinal tumor progression. Gastroenterology 2011, 141:1359-1370.
25. de la Roche M, Rutherford TJ, Gupta D, Veprintsev DB, Saxty B, Freund SM, Bienz M: An intrinsically labile alpha-helix abutting the bcl9-binding site of beta-catenin is required for its inhibition by carnosic acid. Nat Commun 2012, 3:680.
26. Takada K, Zhu D, Bird GH, Sukhdeo K, Zhao JJ, Mani M, Lemieux M, Carrasco DE, Ryan J, Horst D et al.: Targeted disruption of the bcl9/beta-catenin complex inhibits oncogenic wnt signaling. Sci Transl Med 2012, 4:148ra117.
27. Chen J, Luo Q, Yuan Y, Huang X, Cai W, Li C, Wei T, Zhang L, Yang M, Liu Q et al.: Pygo2 associates with mll2 histone methyltransferase and gcn5 histone acetyltransferase complexes to augment wnt target gene expression and breast cancer stem-like cell expansion. Mol Cell Biol 2010, 30:5621-5635.
28. Li Z, Nie F, Wang S, Li L: Histone h4 lys 20 monomethylation by histone methylase set8 mediates wnt target gene activation. Proc Natl Acad Sci USA 2011, 108:3116-3123.
29. Mohan M, Herz HM, Takahashi YH, Lin C, Lai KC, Zhang Y, Washburn MP, Florens L, Shilatifard A: Linking h3k79 trimethylation to wnt signaling through a novel dot1- containing complex (dotcom). Genes Dev 2010, 24:574-589.
30. Li X, Han Y, Xi R: Polycomb group genes psc and su(z)2 restrict follicle stem cell self-renewal and extrusion by controlling canonical and noncanonical wnt signaling. Genes Dev 2010, 24:933-946.
31. Hoffmeyer K, Raggioli A, Rudloff S, Anton R, Hierholzer A, Del Valle I, Hein K, Vogt R, Kemler R: Wnt/beta-catenin signaling regulates telomerase in stem cells and cancer cells. Science 2012, 336:1549-1554.
32. Hao HX, 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.
33. Koo BK, Spit M, Jordens I, Low TY, Stange DE, van de Wetering M, van Es JH, Mohammed S, Heck AJ, Maurice MM, Clevers H: Tumour suppressor rnf43 is a stem-cell e3 ligase that induces endocytosis of wnt receptors. Nature 2012, 488:665-669.
34. Callow MG, Tran H, Phu L, Lau T, Lee J, Sandoval WN, Liu PS, Bheddah S, Tao J, Lill JR et al.: Ubiquitin ligase rnf146 regulates tankyrase and axin to promote wnt signaling. PLoS ONE 2011, 6:e22595.
35. Zhang Y, Liu S, Mickanin C, Feng Y, Charlat O, Michaud GA, Schirle M, Shi X, Hild M, Bauer A et al.: Rnf146 is a poly(adpribose)- directed e3 ligase that regulates axin degradation and wnt signalling. Nat Cell Biol 2011, 13:623-629.
36. Lui TT, Lacroix C, Ahmed SM, Goldenberg SJ, Leach CA, Daulat AM, Angers S: The ubiquitin-specific protease usp34 regulates axin stability and wnt/beta-catenin signaling. Mol Cell Biol 2011, 31:2053-2065.
37. Hanson AJ, Wallace HA, Freeman TJ, Beauchamp RD, Lee LA, Lee E: Xiap monoubiquitylates groucho/tle to promote canonical wnt signaling. Mol Cell 2012, 45:619-628.
38. ten Berge D, Kurek D, Blauwkamp T, Koole W, Maas A, Eroglu E, Siu RK, Nusse R: Embryonic stem cells require wnt proteins to prevent differentiation to epiblast stem cells. Nat Cell Biol 2011, 13:1070-1075.
39. Biechele S, Cox BJ, Rossant J: Porcupine homolog is required for canonical wnt signaling and gastrulation in mouse embryos. Dev Biol 2011, 355:275-285.
40. Lyashenko N, Winter M, Migliorini D, Biechele T, Moon RT, Hartmann C: Differential requirement for the dual functions of beta-catenin in embryonic stem cell self-renewal and germ layer formation. Nat Cell Biol 2011, 13:753-761.
41. Wray J, Kalkan T, Gomez-Lopez S, Eckardt D, Cook A, Kemler R, Smith A: Inhibition of glycogen synthase kinase-3 alleviates tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nat Cell Biol 2011, 13:838-845.
42. Yi F, Pereira L, Hoffman JA, Shy BR, Yuen CM, Liu DR, Merrill BJ: Opposing effects of tcf3 and tcf1 control wnt stimulation of embryonic stem cell self-renewal. Nat Cell Biol 2011, 13:762-770.
43. Kelly KF, Ng DY, Jayakumaran G, Wood GA, Koide H, Doble BW: Beta-catenin enhances oct-4 activity and reinforces pluripotency through a tcf-independent mechanism. Cell Stem Cell 2011, 8:214-227.
44. Davidson KC, Adams AM, Goodson JM, McDonald CE, Potter JC, Berndt JD, Biechele TL, Taylor RJ, Moon RT: Wnt/beta-catenin signaling promotes differentiation, not self-renewal, of human embryonic stem cells and is repressed by oct4. Proc Natl Acad Sci USA 2012, 109:4485-4490.
45. Blauwkamp TA, Nigam S, Ardehali R, Weissman IL, Nusse R: Endogenous wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat Commun 2012, 3.
46. Singh AM, Reynolds D, Cliff T, Ohtsuka S, Mattheyses AL, Sun Y, Menendez L, Kulik M, Dalton S: Signaling network crosstalk in human pluripotent cells: a smad2/3-regulated switch that controls the balance between self-renewal and differentiation. Cell Stem Cell 2012, 10:312-326.
47. Inestrosa NC, Arenas E: Emerging roles of wnts in the adult nervous system. Nat Rev Neurosci 2010, 11:77-86.
48. Alvarez-Medina R, Le Dreau G, Ros M, Marti E: Hedgehog activation is required upstream of wnt signalling to control neural progenitor proliferation. Development 2009, 136:3301-3309.
49. Qu Q, Sun G, Li W, Yang S, Ye P, Zhao C, Yu RT, Gage FH, Evans RM, Shi Y: Orphan nuclear receptor tlx activates wnt/ beta-catenin signalling to stimulate neural stem cell proliferation and self-renewal. Nat Cell Biol 2010, 12:31-40.
50. Mazumdar J, O'Brien WT, Johnson RS, LaManna JC, Chavez JC, Klein PS, Simon MC: O2 regulates stem cells through wnt/betacatenin signalling. Nat Cell Biol 2010, 12:1007-1013.
51. Augustin I, Goidts V, Bongers A, Kerr G, Vollert G, Radlwimmer B, Hartmann C, Herold-Mende C, Reifenberger G, von Deimling A, Boutros M: The wnt secretion protein evi/gpr177 promotes glioma tumourigenesis. EMBO Mol Med 2012, 4:38-51.
52. Gibson P, Tong Y, Robinson G, Thompson MC, Currle DS, Eden C, Kranenburg TA, Hogg T, Poppleton H, Martin J et al.: Subtypes of medulloblastoma have distinct developmental origins. Nature 2010, 468:1095-1099.
53. Buchman JJ, Durak O, Tsai LH: Aspm regulates wnt signaling pathway activity in the developing brain. Genes Dev 2011, 25:1909-1914.
54. Endo Y, Ishiwata-Endo H, Yamada KM: Extracellular matrix protein anosmin promotes neural crest formation and regulates fgf, bmp, and wnt activities. Dev Cell 2012, 23:305-316.
55. Fancy SP, Harrington EP, Yuen TJ, Silbereis JC, Zhao C, Baranzini SE, Bruce CC, Otero JJ, Huang EJ, Nusse R et al.: Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat Neurosci 2011, 14:1009-1016.
56. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, Weissman IL: A role for wnt signalling in selfrenewal of haematopoietic stem cells. Nature 2003, 423:409-414.
57. Perry JM, He XC, Sugimura R, Grindley JC, Haug JS, Ding S, Li L: Cooperation between both wnt/{beta}-catenin and pten/pi3k/ akt signaling promotes primitive hematopoietic stem cell selfrenewal and expansion. Genes Dev 2011, 25:1928-1942.
58. Trompouki E, Bowman TV, Lawton LN, Fan ZP, Wu DC, DiBiase A, Martin CS, Cech JN, Sessa AK, Leblanc JL et al.: Lineage regulators direct bmp and wnt pathways to cell-specific programs during differentiation and regeneration. Cell 2011, 147:577-589.
59. Heidel FH, Bullinger L, Feng Z, Wang Z, Neff TA, Stein L, Kalaitzidis D, Lane SW, Armstrong SA: Genetic and pharmacologic inhibition of beta-catenin targets imatinibresistant leukemia stem cells in cml. Cell Stem Cell 2012, 10:412-424.
60. Yeung J, Esposito MT, Gandillet A, Zeisig BB, Griessinger E, Bonnet D, So CW: Beta-catenin mediates the establishment and drug resistance of mll leukemic stem cells. Cancer Cell 2010, 18:606-618.
61. Grigoryan T, Wend P, Klaus A, Birchmeier W: Deciphering the function of canonical wnt signals in development and disease: conditional loss- and gain-of-function mutations of betacatenin in mice. Genes Dev 2008, 22:2308-2341.
62. Nguyen H, Merrill BJ, Polak L, Nikolova M, Rendl M, Shaver TM, Pasolli HA, Fuchs E: Tcf3 and tcf4 are essential for long-term homeostasis of skin epithelia. Nat Genet 2009, 41:1068-1075.
63. Jaks V, Barker N, Kasper M, van Es JH, Snippert HJ, Clevers H, Toftgard R: Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 2008, 40:1291-1299.
64. Snippert HJ, Haegebarth A, Kasper M, Jaks V, van Es JH, Barker N, van de Wetering M, van den Born M, Begthel H, Vries RG et al.: Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 2010, 327:1385-1389.
65. Plikus MV, Baker RE, Chen CC, Fare C, de la Cruz D, Andl T, Maini PK, Millar SE, Widelitz R, Chuong CM: Self-organizing and stochastic behaviors during the regeneration of hair stem cells. Science 2011, 332:586-589.
66. Rabbani P, Takeo M, Chou W, Myung P, Bosenberg M, Chin L, Taketo MM, Ito M: Coordinated activation of wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration. Cell 2011, 145:941-955.
67. Fujiwara H, Ferreira M, Donati G, Marciano DK, Linton JM, Sato Y, Hartner A, Sekiguchi K, Reichardt LF, Watt FM: The basement membrane of hair follicle stem cells is a muscle cell niche. Cell 2011, 144:577-589.
68. Barker N, van Oudenaarden A, Clevers H: Identifying the stem cell of the intestinal crypt: Strategies and pitfalls. Cell Stem Cell 2012, 11:452-460.
69. Itzkovitz S, Lyubimova A, Blat IC, Maynard M, van Es J, Lees J, Jacks T, Clevers H, van Oudenaarden A: Single-molecule transcript counting of stem-cell markers in the mouse intestine. Nat Cell Biol 2011, 14:106-114.
70. Munoz J, Stange DE, Schepers AG, van de Wetering M, Koo BK, Itzkovitz S, Volckmann R, Kung KS, Koster J, Radulescu S et al.: The lgr5 intestinal stem cell signature: robust expression of proposed quiescent '+4' cell markers. EMBO J 2012, 31:3079-3091.
71. van Es JH, Sato T, van de Wetering M, Lyubimova A, Yee Nee AN, Gregorieff A, Sasaki N, Zeinstra L, van den Born M, Korving J et al.: Dll1(+) secretory progenitor cells revert to stem cells upon crypt damage. Nat Cell Biol 2012, 14:1099-1104.
72. Durand A, Donahue B, Peignon G, Letourneur F, Cagnard N, Slomianny C, Perret C, Shroyer NF, Romagnolo B: Functional intestinal stem cells after paneth cell ablation induced by the loss of transcription factor math1 (atoh1). Proc Natl Acad Sci USA 2012, 109:8965-8970.
73. Kim TH, Escudero S, Shivdasani RA: Intact function of lgr5 receptor-expressing intestinal stem cells in the absence of paneth cells. Proc Natl Acad Sci USA 2012, 109:3932-3937.
74. Yui S, Nakamura T, Sato T, Nemoto Y, Mizutani T, Zheng X, Ichinose S, Nagaishi T, Okamoto R, Tsuchiya K et al.: Functional engraftment of colon epithelium expanded in vitro from a single adult lgr5(+) stem cell. Nat Med 2012, 18:618-623.
75. Spence JR, Mayhew CN, Rankin SA, Kuhar MF, Vallance JE, Tolle K, Hoskins EE, Kalinichenko VV, Wells SI, Zorn AM et al.: Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 2011, 470:105-109.
76. Schepers AG, Snippert HJ, Stange DE, van den Born M, van Es JH, van de Wetering M, Clevers H: Lineage tracing reveals lgr5+ stem cell activity in mouse intestinal adenomas. Science 2012, 337:730-735.
77. Seshagiri S, Stawiski EW, Durinck S, Modrusan Z, Storm EE, Conboy CB, Chaudhuri S, Guan YH, Janakiraman V, Jaiswal BS et al.: Recurrent r-spondin fusions in colon cancer. Nature 2012, 488:660.
78. Vermeulen L, De Sousa EMF, van der Heijden M, Cameron K, de Jong JH, Borovski T, Tuynman JB, Todaro M, Merz C, Rodermond H et al.: Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 2010, 12:468-476.
79. Incassati A, Chandramouli A, Eelkema R, Cowin P: Key signaling nodes in mammary gland development and cancer: betacatenin. Breast Cancer Res 2010, 12:213.
80. Macias H, Moran A, Samara Y, Moreno M, Compton JE, Harburg G, Strickland P, Hinck L: Slit/robo1 signaling suppresses mammary branching morphogenesis by limiting basal cell number. Dev Cell 2011, 20:827-840.
81. Zeng YA, Nusse R: Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 2010, 6:568-577.
82. van Amerongen R, Bowman AN, Nusse R: Developmental stage and time dictate the fate of wnt/beta-catenin-responsive stem cells in the mammary gland. Cell Stem Cell 2012, 11:387-400.
83. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE: Generation of a functional mammary gland from a single stem cell. Nature 2006, 439:84-88.
84. Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF, Huelsken J: Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 2011, 481:85-89.
85. Wamstad JA, Alexander JM, Truty RM, Shrikumar A, Li F, Eilertson KE, Ding H, Wylie JN, Pico AR, Capra JA et al.: Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 2012, 151:206-220.
86. Song K, Nam YJ, Luo X, Qi X, Tan W, Huang GN, Acharya A, Smith CL, Tallquist MD, Neilson EG et al.: Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 2012, 485:599-604.
87. Klaus A, Muller M, Schulz H, Saga Y, Martin JF, Birchmeier W: Wnt/beta-catenin and bmp signals control distinct sets of transcription factors in cardiac progenitor cells. Proc Natl Acad Sci USA 2012, 109:10921-10926.
88. Kwon C, Cheng P, King IN, Andersen P, Shenje L, Nigam V, Srivastava D: Notch post-translationally regulates betacatenin protein in stem and progenitor cells. Nat Cell Biol 2011, 13:1244-1251.
89. Lian X, Hsiao C, Wilson G, Zhu K, Hazeltine LB, Azarin SM, Raval KK, Zhang J, Kamp TJ, Palecek SP: Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical wnt signaling. Proc Natl Acad Sci USA 2012, 109:E1848-E1857.
90. Mou H, Zhao R, Sherwood R, Ahfeldt T, Lapey A, Wain J, Sicilian L, Izvolsky K, Musunuru K, Cowan C, Rajagopal J: Generation of multipotent lung and airway progenitors from mouse escs and patient-specific cystic fibrosis ipscs. Cell Stem Cell 2012, 10:385-397.
91. Longmire TA, Ikonomou L, Hawkins F, Christodoulou C, Cao Y, Jean JC, Kwok LW, Mou H, Rajagopal J, Shen SS et al.: Efficient derivation of purified lung and thyroid progenitors from embryonic stem cells. Cell Stem Cell 2012, 10:398-411.
92. Pacheco-Pinedo EC, Durham AC, Stewart KM, Goss AM, Lu MM, Demayo FJ, Morrisey EE: Wnt/beta-catenin signaling accelerates mouse lung tumorigenesis by imposing an embryonic distal progenitor phenotype on lung epithelium. J Clin Invest 2011, 121:1935-1945.
93. Shin K, Lee J, Guo N, Kim J, Lim A, Qu L, Mysorekar IU, Beachy PA: Hedgehog/wnt feedback supports regenerative proliferation of epithelial stem cells in bladder. Nature 2011, 472:110-114.
94. Kypta RM, Waxman J: Wnt/beta-catenin signalling in prostate cancer. Nat Rev Urol 2012, 9:418-428.
95. Lukacs RU, Memarzadeh S, Wu H, Witte ON: Bmi-1 is a crucial regulator of prostate stem cell self-renewal and malignant transformation. Cell Stem Cell 2010, 7:682-693.
96. von Kries JP, Winbeck G, Asbrand C, Schwarz-Romond T, Sochnikova N, Dell'Oro A, Behrens J, Birchmeier W: Hot spots in beta-catenin for interactions with lef-1, conductin and apc. Nat Struct Biol 2000, 7:800-807.
97. Xing Y, Clements WK, Le Trong I, Hinds TR, Stenkamp R, Kimelman D, Xu W: Crystal structure of a beta-catenin/apc complex reveals a critical role for apc phosphorylation in apc function. Mol Cell 2004, 15:523-533.
98. Sampietro J, Dahlberg CL, Cho US, Hinds TR, Kimelman D, Xu W: Crystal structure of a beta-catenin/bcl9/tcf4 complex. Mol Cell 2006, 24:293-300.
99. Graham TA, Ferkey DM, Mao F, Kimelman D, Xu W: Tcf4 can specifically recognize beta-catenin using alternative conformations. Nat Struct Biol 2001, 8:1048-1052.