Disabled-2 is required for mesoderm differentiation of murine embryonic stem cells

Journal of Cellular Physiology

Volumn 225, Issue 1, 2010, Pages 92-105

  Huang, Chien Ling ^a   Cheng, Ju Chien ^b   Kitajima, Kenji ^c   Nakano, Toru ^d   Yeh, Chun Fung ^a   Chong, Kowit Yu ^a   Tseng, Ching Ping ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTATE AMMONIA LIGASE; BETA CATENIN; DISABLED 2 PROTEIN; GLUTATHIONE PEROXIDASE 2; PHOSPHOTYROSINE; PLAKOGLOBIN; PROTEIN; PROTEIN P53; SMALL INTERFERING RNA; SOMATOMEDIN B; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL GROWTH; EMBRYONIC STEM CELL; ENZYME INDUCTION; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; MESODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BETA CATENIN; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; GAMMA CATENIN; MESODERM; MICE; MICROARRAY ANALYSIS; MICRORNAS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

MURINAE;

EID: 77956508436     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22200     Document Type: Article

References (66)

1. Anupam K, Tusharkant C, Gupta SD, Ranju R. 2006. Loss of disabled-2 expression is an early event in esophageal squamous tumorigenesis. World J Gastroenterol 12:6041-6045. (Pubitemid 44608486)
2. Calderwood DA, Fujioka Y, de Pereda JM, Garcia-Alvarez B, Nakamoto T, Margolis B, McGlade CJ, Liddington RC, Ginsberg MH. 2003. Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: A structural prototype for diversity in integrin signaling. Proc Natl Acad Sci USA 100:2272-2277.
3. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ. 2005. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:e179.
4. Cheong SM, Choi SC, Han JK. 2006. Xenopus Dab2 is required for embryonic angiogenesis. BMC Dev Biol 6:63-76.
5. Cuitino L, Matute R, Retamal C, Bu G, Inestrosa NC, Marzolo MP. 2005. ApoER2 is endocytosed by a clathrin-mediated process involving the adaptor protein Dab2 independent of its Rafts' association. Traffic 6:820-838. (Pubitemid 41179413)
6. Czyz J, Guan K, Zeng Q, Wobus AM. 2005. Loss of beta 1 integrin function results in upregulation of connexin expression in embryonic stem cell-derived cardiomyocytes. Int J Dev Biol 49:33-41.
7. Damalas A, Ben-Ze'ev A, Simcha I, Shtutman M, Leal JF, Zhurinsky J, Geiger B, Oren M. 1999. Excess beta-catenin promotes accumulation of transcriptionally active p53. EMBO J 18:3054-3063.
8. de Pooter RF, Schmitt TM, Zuñiga-Pflucker JC. 2006. In vitro generation of T lymphocytes from embryonic stem cells. Methods Mol Biol 330:113-121.
9. Fogal V, Gostissa M, Sandy P, Zacchi P, Sternsdorf T, Jensen K, Pandolfi PP, Will H, Schneider C, Del Sal G. 2000. Regulation of p53 activity in nuclear bodies by a specific PML isoform. EMBO J 19:6185-6195.
10. Fujimoto TT, Kohata S, Suzuki H, Miyazaki H, Fujimura K. 2003. Production of functional platelets by differentiated embryonic stem (ES) cells in vitro. Blood 102:4044-4051.
11. Furlong EE, Rein T, Martin F. 1996. YY1 and NF1 both activate the human p53 promoter by alternatively binding to a composite element, and YY1 and E1A cooperate to amplify p53 promoter activity. Mol Cell Biol 16:5933-5945.
12. Griffiths-Jones S. 2004. The microRNA registry. Nucleic Acids Res 32:D109-D111.
13. Griffiths-Jones S. 2006. miRBase: The microRNA sequence database. Methods Mol Biol 342:129-138.
14. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. 2008. miRBase: Tools for microRNA genomics. Nucleic Acids Res 36:D154-D158.
15. Hocevar BA, Smine A, Xu XX, Howe PH. 2001. The adaptor molecule Disabled-2 links the transforming growth factor receptors to the Smad pathway. EMBO J 20:2789-2801. (Pubitemid 32938562)
16. Hocevar BA, Mou F, Rennolds JL, Morris SM, Cooper JA, Howe PH. 2003. Regulation of the Wnt signaling pathway by disabled-2 (Dab2). EMBO J 22:3084-3094.
17. Houghton FD. 2005. Role of gap junctions during early embryo development. Reproduction 129:129-135.
18. Huang CL, Cheng JC, Liao CH, Stern A, Hsieh JT, Wang CH, Hsu HL, Tseng CP. 2004. Disabled-2 is a negative regulator of integrin αIIbβ3- mediated fibrinogen adhesion and cell signaling. J Biol Chem 279:42279-42289.
19. Huang CL, Cheng JC, Stern A, Hsieh JT, Liao CH, Tseng CP. 2006. Disabled-2 is a novel integrin αIIb-binding protein that negatively regulates platelet-fibrinogen interactions and platelet aggregation. J Cell Sci 119:4420-4430.
20. Huang CH, Cheng JC, Chen JC, Tseng CP. 2007. Evaluation of the role of Disabled-2 in nerve growth factor-mediated neurite outgrowth and cellular signaling. Cell Signal 19:1339-1347.
21. Karam JA, Shariat SF, Huang HY, Pong RC, Ashfaq R, Shapiro E, Lotan Y, Sagalowsky AI, Wu XR, Hsieh JT. 2007. Decreased DOC-2/DAB2 expression in urothelial carcinoma of the bladder. Clin Cancer Res 13:4400-4406.
22. Keller G. 2005. Embryonic stem cell differentiation: Emergence of a new era in biology and medicine. Genes Dev 19:1129-1155. (Pubitemid 40696181)
23. Kitajima K, Tanaka M, Zheng J, Sakai-Ogawa E, Nakano T. 2003. In vitro differentiation of mouse embryonic stem cells to hematopoietic cells on an OP9 stromal cell monolayer. Methods Enzymol 365:72-83.
24. Kitajima K, Tanaka M, Zheng J, Yen H, Sato A, Sugiyama D, Umehara H, Sakai E, Nakano T. 2006. Redirecting differentiation of hematopoietic progenitors by a transcription factor, GATA-2. Blood 107:1857-1863.
25. Kleeff J, Huang Y, Mok SC, Zimmermann A, Friess H, Buchler MW. 2002. Down-regulation of DOC-2 in colorectal cancer points to its role as a tumor suppressor in thismalignancy. Dis Colon Rectum 45:1242-1248.
26. Kurosawa H, Imamura T, Koike M, Sasaki K, Amano Y. 2003. A simple method for forming embryoid body from mouse embryonic stem cells. J Biosci Bioeng 96:409-411.
27. Lindsley RC, Gill JG, Kyba M, Murphy TL, Murphy KM. 2006. Canonical Wnt signaling is required for development of embryonic stem cell-derived mesoderm. Development 133:3787-3796.
28. Maurer ME, Cooper JA. 2005. Endocytosis of megalin by visceral endoderm cells requires the Dab2 adaptor protein. J Cell Sci 118:5345-5355.
29. Mok SC, Wong KK, Chan RK, Lau CC, Tsao SW, Knapp RC, Berkowitz RS. 1994. Molecular cloning of differentially expressed genes in human epithelial ovarian cancer. Gynecol Oncol 52:247-252.
30. Mongan NP, Martin KM, Gudas LJ. 2006. The putative human stem cellmarker, Rex-1 (Zfp42): Structural classification and expression in normal human epithelial and carcinoma cell cultures. Mol Carcinogenesis 45:887-900.
31. Morali OG, Jouneau A, McLaughlin KJ, Thiery JP, Larue L. 2000. IGF-II promotes mesoderm formation. Dev Biol 227:133-145.
32. Morris SM, Tallquist MD, Rock CO, Cooper JA. 2002. Dual roles for the Dab2 adaptor protein in embryonic development and kidney transport. EMBO J 21:1555-1564.
33. Nagano K, Taoka M, Yamauchi Y, Itagaki C, Shinkawa T, Nunomura K, Okamura N, Takahashi N, Izumi T, Isobe T. 2005. Large-scale identification of proteins expressed in mouse embryonic stem cells. Proteomics 5:1346-1361.
34. Nagaoka M, Koshimizu U, Yuasa S, Hattori F, Chen H, Tanaka T, Okabe M, Fukuda K, Akaike T. 2006. E-cadherin-coated plates maintain pluripotent ES cells without colony formation. PLoS ONE 1:e15.
35. Nakano T. 1996. In vitro development of hematopoietic system from mouse embryonic stem cells: A new approach for embryonic hematopoiesis. Int J Hematol 65:1-8.
36. Orlandinia M, Nucciottia S, Galvagnia F, Bardellia M, Rocchigiania M, Petragliab F, Oliviero S. 2008. Morphogenesis of human endothelial cells is inhibited by DAB2 via Src. FEBS Lett 582:2542-2548.
37. Prunier C, Howe PH. 2005. Disabled-2 (Dab2) is required for transforming growth factor beta-induced epithelial to mesenchymal transition (EMT). J Biol Chem 280:17540-17548. (Pubitemid 41389228)
38. Qin J, Guo X, Cui GH, Zhou YC, Zhou DR, Tang AF, Yu ZD, Gui YT, Cai ZM. 2009. Cluster characterization of mouse embryonic stem cell-derived pluripotent embryoid bodies in four distinct developmental stages. Biologicals 37:235-244.
39. Robertson SM, Kennedy M, Shannon JM, Keller G. 2000. A transitional stage in the commitment of mesoderm to hematopoiesis requiring the transcription factor SCL/tal-1. Development 127:2337-2459.
40. Rosenbauer F, Kallies A, Scheller M, Knobeloch KP, Rock CO, Schwieger M, Stocking C, Horak I. 2002. Disabled-2 is transcriptionally regulated by ICSBP and augments macrophage spreading and adhesion. EMBO J 21:211-220.
41. Rula ME, Cai KQ, Moore R, Yang DH, Staub CM, Capo-Chichi CD, Jablonski SA, Howe PH, Smith ER, Xu XX. 2007. Cell autonomous sorting and surface positioning in the formation of primitive endoderm in embryoid bodies. Genesis 45:327-338.
42. Schroeder T, Meier-Stiegen F, Schwanbeck R, Eilken H, Nishikawa S, Hasler R, Schreiber S, Bornkamm GW, Nishikawa S, Just U. 2006. Activated Notch1 alters differentiation of embryonic stem cells into mesodermal cell lineages at multiple stages of development. Mech Dev 123:570-579.
43. Shtutman M, Zhurinsky J, Oren M, Levina E, Ben-Ze'ev A. 2002. PML is a target gene of beta-catenin and plakoglobin, and coactivates beta-catenin-mediated transcription. Cancer Res 62:5947-5954.
44. Simcha I, Shtutman M, Salomon D, Zhurinsky J, Sadot E, Geiger B, Ben-Ze'ev A. 1998. Differential nuclear translocation and transactivation potential of beta-catenin and plakoglobin. J Cell Biol 141:1433-1448.
45. Song HD, Sun XJ, Deng M, Zhang GW, Zhou Y, Wu XY, Sheng Y, Chen Y, Ruan Z, Jiang CL, Fan HY, Zon LI, Kanki JP, Liu TX, Look AT, Chen Z. 2004. Hematopoietic gene expression profile in zebrafish kidney marrow. Proc Natl Acad Sci USA 101:16240-16245.
46. Stagliano KE, Carchman E, Deb S. 2003. Real-time polymerase chain reaction quantitation of relative expression of genes modulated by p53 using SYBR Green I. Methods Mol Biol 234:73-91.
47. Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, Meister G, Hermeking H. 2007. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6:1586-1593. (Pubitemid 47327945)
48. Tell S, Yi H, Jockovich ME, Murray TG, Hackam AS. 2006. The Wnt signaling pathway has tumor suppressor properties in retinoblastoma. Biochem Biophys Res Commun 349:261-269.
49. Tiede S, Kloepper JE, Bodo E, Tiwari S, KruseC, Paus R. 2007. Hair follicle stem cells: Walking the maze. Eur J Cell Biol 86:355-376.
50. Tomasini R, Samir AA, Carrier A, Isnardon D, Cecchinelli B, Soddu S, Malissen B, Dagorn JC, Iovanna JL, Dusetti NJ. 2003. TP53INP1s and homeodomain-interacting protein kinase-2 (HIPK2) are partners in regulating p53 activity. J Biol Chem 278:37722-37729.
51. Tseng CP, Ely BD, Li Y, Pong RC, Hsieh JT. 1998. Regulation of rat DOC-2 gene during castration-induced rat ventral prostate degeneration and its growth inhibitory function in human prostatic carcinoma cells. Endocrinology 139:3542-3553. (Pubitemid 28512312)
52. Tseng CP, Ely BD, Pong RC, Wang Z, Zhou J, Hsieh JT. 1999. The role of DOC-2/DAB2 protein phosphorylation in the inhibition of AP-1 activity. An underlying mechanism of its tumor-suppressive function in prostate cancer. J Biol Chem 274:31981-31986.
53. Tseng CP, Huang CH, Tseng CC, Lin MH, Hsieh JT, Tseng CH. 2001. Induction of disabled-2 gene during megakaryocyte differentiation of k562 cells. Biochem Biophys Res Commun 285:129-135.
54. Tseng CP, Huang CL, Huang CH, Stern A, Cheng JC, Tseng CH, Chiu DTY. 2003. Disabled-2 small interfering RNA modulates cellular adhesive function and MAPK activity during megakaryocytic differentiation of K562 cells. FEBS Lett 541:21-27. (Pubitemid 36428911)
55. Tseng CP, Chang P, Huang CL, Cheng JC, Chang SS. 2005. Autocrine signaling of platelet-derived growth factor regulates disabled-2 expression during megakaryocytic differentiation of K562 cells. FEBS Lett 579: 4395-4401.
56. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E. 2004. Defining the epithelial stem cell niche in skin. Science 303: 359-363. (Pubitemid 38095773)
57. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E. 2004. Defining the epithelial stem cell niche in skin. Science 303:359-363. (Pubitemid 38095773)
58. Xu XX, Yi T, Tang B, Lambeth JD. 1998. Disabled-2 (Dab2) is an SH3 domain-binding partner of Grb2. Oncogene 16:1561-1569. (Pubitemid 28159903)
59. Yan W, Chen X. 2006. GPX2, a direct target of p63, inhibits oxidative stress-induced apoptosis in a p53-dependent manner. J Biol Chem 281:7856-7862.
60. Yang DH, Smith ER, Roland IH, Sheng Z, He J, Martin WD, Hamilton TC, Lambeth JD, Xu XX. 2002. Disabled-2 is essential for endodermal cell positioning and structure formation during mouse embryogenesis. Dev Biol 251:27-44.
61. Yang DH, Cai KQ, Roland IH, Smith ER, Xu XX. 2007. Disabled-2 is an epithelial surface positioning gene. J Biol Chem 282:13114-13122.
62. Yin T, Getsios S, Caldelari R, Godsel LM, Kowalczyk AP, Muller EJ, Green KJ. 2005. Mechanisms of plakoglobin-dependent adhesion: Desmosome-specific functions in assembly and regulation by epidermal growth factor receptor. J Biol Chem 280:40355-40363. (Pubitemid 41779173)
63. Zhang L, Kashanchi F, Zhan Q, Zhan S, Brady JN, Fornace AJ, Seth P, Helman LJ. 1996. Regulation of insulin-like growth factor II P3 promotor by p53: A potential mechanism for tumorigenesis. Cancer Res 56:1367-1373.
64. Zhang L, ZhanQ, Zhan S, Kashanchi F, Fornace AJ, Jr., Seth P, Helman LJ. 1998. p53 regulates human insulin-like growth factor II gene expression through active P4 promoter in rhabdomyosarcoma cells. DNA Cell Biol 17:125-131.
65. Zhou J, Hsieh JT. 2001. The inhibitory role of DOC-2/DAB2 in growth factor receptor-mediated signal cascade. J Biol Chem 276:27793-27798.
66. Zhurinsky J, Shtutman M, Ben-Ze'ev A. 2000. Plakoglobin and beta-catenin: Protein interactions, regulation and biological roles. J Cell Sci 113:3127-3139.