Endocytic proteins in the regulation of nuclear signaling, transcription and tumorigenesis

Molecular Oncology

Volumn 3, Issue 4, 2009, Pages 321-338

  Pyrzynska, Beata ^a   Pilecka, Iwona ^a   Miaczynska, Marta ^a  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

Author keywords

Endocytosis; Transcription; Tumorigenesis

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; MEMBRANE PROTEIN;

CARCINOGENESIS; CELL NUCLEUS; CELL PROLIFERATION; ENDOCYTOSIS; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; INTERNALIZATION; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; ENDOCYTOSIS; GENE EXPRESSION REGULATION; HUMANS; NEOPLASMS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 67949106368     PISSN: 15747891     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molonc.2009.06.001     Document Type: Review

References (142)

1. Adams A., Thorn J.M., Yamabhai M., Kay B.K., and O'Bryan J.P. Intersectin, an adaptor protein involved in clathrin-mediated endocytosis, activates mitogenic signaling pathways. J. Biol. Chem. 275 (2000) 27414-27420
2. Alber F., Dokudovskaya S., Veenhoff L.M., Zhang W., Kipper J., Devos D., Suprapto A., Karni-Schmidt O., Williams R., Chait B.T., Sali A., and Rout M.P. The molecular architecture of the nuclear pore complex. Nature 450 (2007) 695-701
3. Anupam K., Tusharkant C., Gupta S.D., and Ranju R. Loss of disabled-2 expression is an early event in esophageal squamous tumorigenesis. World J. Gastroenterol. 12 (2006) 6041-6045
4. Aramaki Y., Ogawa K., Toh Y., Ito T., Akimitsu N., Hamamoto H., Sekimizu K., Matsusue K., Kono A., Iguchi H., and Takiguchi S. Direct interaction between metastasis-associated protein 1 and endophilin 3. FEBS Lett. 579 (2005) 3731-3736
5. Archangelo L.F., Glasner J., Krause A., and Bohlander S.K. The novel CALM interactor CATS influences the subcellular localization of the leukemogenic fusion protein CALM/AF10. Oncogene 25 (2006) 4099-4109
6. Argani P., Lui M.Y., Couturier J., Bouvier R., Fournet J.C., and Ladanyi M. A novel CLTC-TFE3 gene fusion in pediatric renal adenocarcinoma with t(X;17)(p11.2;q23). Oncogene 22 (2003) 5374-5378
7. Asao H., Sasaki Y., Arita T., Tanaka N., Endo K., Kasai H., Takeshita T., Endo Y., Fujita T., and Sugamura K. Hrs is associated with STAM, a signal-transducing adaptor molecule. Its suppressive effect on cytokine-induced cell growth. J. Biol. Chem. 272 (1997) 32785-32791
8. Bagadi S.A., Prasad C.P., Srivastava A., Prashad R., Gupta S.D., and Ralhan R. Frequent loss of Dab2 protein and infrequent promoter hypermethylation in breast cancer. Breast Cancer Res. Treat. 104 (2007) 277-286
9. Bhattacharyya N.P., Banerjee M., and Majumder P. Huntington's disease: roles of huntingtin-interacting protein 1 (HIP-1) and its molecular partner HIPPI in the regulation of apoptosis and transcription. FEBS J. 275 (2008) 4271-4279
10. Bohlander S.K., Muschinsky V., Schrader K., Siebert R., Schlegelberger B., Harder L., Schemmel V., Fonatsch C., Ludwig W.D., Hiddemann W., and Dreyling M.H. Molecular analysis of the CALM/AF10 fusion: identical rearrangements in acute myeloid leukemia, acute lymphoblastic leukemia and malignant lymphoma patients. Leukemia 14 (2000) 93-99
11. Boissan M., Wendum D., Arnaud-Dabernat S., Munier A., Debray M., Lascu I., Daniel J.Y., and Lacombe M.L. Increased lung metastasis in transgenic NM23-Null/SV40 mice with hepatocellular carcinoma. J. Natl. Cancer Inst. 97 (2005) 836-845
12. Bradley S.V., Holland E.C., Liu G.Y., Thomas D., Hyun T.S., and Ross T.S. Huntingtin interacting protein 1 is a novel brain tumor marker that associates with epidermal growth factor receptor. Cancer Res. 67 (2007) 3609-3615
13. Bradley S.V., Smith M.R., Hyun T.S., Lucas P.C., Li L., Antonuk D., Joshi I., Jin F., and Ross T.S. Aberrant Huntingtin interacting protein 1 in lymphoid malignancies. Cancer Res. 67 (2007) 8923-8931
14. Bridge J.A., Kanamori M., Ma Z., Pickering D., Hill D.A., Lydiatt W., Lui M.Y., Colleoni G.W., Antonescu C.R., Ladanyi M., and Morris S.W. Fusion of the ALK gene to the clathrin heavy chain gene, CLTC, in inflammatory myofibroblastic tumor. Am. J. Pathol. 159 (2001) 411-415
15. Buchanan F.G., and DuBois R.N. Emerging roles of β-arrestins. Cell Cycle 5 (2006) 2060-2063
16. Buchanan F.G., Gorden D.L., Matta P., Shi Q., Matrisian L.M., and DuBois R.N. Role of β-arrestin 1 in the metastatic progression of colorectal cancer. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 1492-1497
17. Burgdorf S., Leister P., and Scheidtmann K.H. TSG101 interacts with apoptosis-antagonizing transcription factor and enhances androgen receptor-mediated transcription by promoting its monoubiquitination. J. Biol. Chem. 279 (2004) 17524-17534
18. Calvisi D.F., Ladu S., Gorden A., Farina M., Lee J.S., Conner E.A., Schroeder I., Factor V.M., and Thorgeirsson S.S. Mechanistic and prognostic significance of aberrant methylation in the molecular pathogenesis of human hepatocellular carcinoma. J. Clin. Invest. 117 (2007) 2713-2722
19. Carlson K.M., Vignon C., Bohlander S., Martinez-Climent J.A., Le Beau M.M., and Rowley J.D. Identification and molecular characterization of CALM/AF10fusion products in T cell acute lymphoblastic leukemia and acute myeloid leukemia. Leukemia 14 (2000) 100-104
20. Carstens M.J., Krempler A., Triplett A.A., Van Lohuizen M., and Wagner K.U. Cell cycle arrest and cell death are controlled by p53-dependent and p53-independent mechanisms in Tsg101-deficient cells. J. Biol. Chem. 279 (2004) 35984-35994
21. Chang M.Y., Boulden J., Sutanto-Ward E., Duhadaway J.B., Soler A.P., Muller A.J., and Prendergast G.C. Bin1 ablation in mammary gland delays tissue remodeling and drives cancer progression. Cancer Res. 67 (2007) 100-107
22. Chen W., ten Berge D., Brown J., Ahn S., Hu L.A., Miller W.E., Caron M.G., Barak L.S., Nusse R., and Lefkowitz R.J. Dishevelled 2 recruits β-arrestin 2 to mediate Wnt5A-stimulated endocytosis of Frizzled 4. Science 301 (2003) 1391-1394
23. Cho S.Y., Jeon J.W., Lee S.H., and Park S.S. p67 isoform of mouse disabled 2 protein acts as a transcriptional activator during the differentiation of F9 cells. Biochem. J. 352 Pt 3 (2000) 645-650
24. Chua H.H., Lee H.H., Chang S.S., Lu C.C., Yeh T.H., Hsu T.Y., Cheng T.H., Cheng J.T., Chen M.R., and Tsai C.H. Role of the TSG101 gene in Epstein-Barr virus late gene transcription. J. Virol. 81 (2007) 2459-2471
25. Colaluca I.N., Tosoni D., Nuciforo P., Senic-Matuglia F., Galimberti V., Viale G., Pece S., and Di Fiore P.P. NUMB controls p53 tumour suppressor activity. Nature 451 (2008) 76-80
26. Curtis C.D., Likhite V.S., McLeod I.X., Yates J.R., and Nardulli A.M. Interaction of the tumor metastasis suppressor nonmetastatic protein 23 homologue H1 and estrogen receptor α alters estrogen-responsive gene expression. Cancer Res. 67 (2007) 10600-10607
27. Das M., Scappini E., Martin N.P., Wong K.A., Dunn S., Chen Y.J., Miller S.L., Domin J., and O'Bryan J.P. Regulation of neuron survival through an intersectin-phosphoinositide 3′-kinase C2beta-AKT pathway. Mol. Cell Biol. 27 (2007) 7906-7917
28. Disanza A., Frittoli E., Palamidessi A., and Scita G. Endocytosis and spatial restriction of cell signaling. Mol. Oncol. 3 (2009) 280-296
29. Diwakar R., Pearson A.L., Colville-Nash P., Baines D.L., and Dockrell M.E. Role played by disabled-2 in albumin induced MAP kinase signalling. Biochem. Biophys. Res. Commun. 366 (2008) 675-680
30. DuHadaway J.B., Lynch F.J., Brisbay S., Bueso-Ramos C., Troncoso P., McDonnell T., and Prendergast G.C. Immunohistochemical analysis of Bin1/Amphiphysin II in human tissues: diverse sites of nuclear expression and losses in prostate cancer. J. Cell Biochem. 88 (2003) 635-642
31. DuHadaway J.B., Sakamuro D., Ewert D.L., and Prendergast G.C. Bin1 mediates apoptosis by c-Myc in transformed primary cells. Cancer Res. 61 (2001) 3151-3156
32. Elliott K., Sakamuro D., Basu A., Du W., Wunner W., Staller P., Gaubatz S., Zhang H., Prochownik E., Eilers M., and Prendergast G.C. Bin1 functionally interacts with Myc and inhibits cell proliferation via multiple mechanisms. Oncogene 18 (1999) 3564-3573
33. Enari M., Ohmori K., Kitabayashi I., and Taya Y. Requirement of clathrin heavy chain for p53-mediated transcription. Genes Dev. 20 (2006) 1087-1099
34. Fan H., Luttrell L.M., Tempel G.E., Senn J.J., Halushka P.V., and Cook J.A. Beta-arrestins 1 and 2 differentially regulate LPS-induced signaling and pro-inflammatory gene expression. Mol. Immunol. 44 (2007) 3092-3099
35. Fan Z., Beresford P.J., Oh D.Y., Zhang D., and Lieberman J. Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor. Cell 112 (2003) 659-672
36. Feng Q., and Zhang Y. The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev. 15 (2001) 827-832
37. Fish K.N., Schmid S.L., and Damke H. Evidence that dynamin-2 functions as a signal-transducing GTPase. J. Cell. Biol. 150 (2000) 145-154
38. Fong A.M., Premont R.T., Richardson R.M., Yu Y.R., Lefkowitz R.J., and Patel D.D. Defective lymphocyte chemotaxis in beta-arrestin2- and GRK6-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 7478-7483
39. Fuerthauer M., and Gonzalez-Gaitan M. Endocytosis, asymmetric cell division, stem cells and cancer: Unus pro omnibus, omnes pro uno. Mol. Oncol. 3 (2009) 339-353
40. Gallahan D., Jhappan C., Robinson G., Hennighausen L., Sharp R., Kordon E., Callahan R., Merlino G., and Smith G.H. Expression of a truncated Int3 gene in developing secretory mammary epithelium specifically retards lobular differentiation resulting in tumorigenesis. Cancer Res. 56 (1996) 1775-1785
41. Ge K., DuHadaway J., Du W., Herlyn M., Rodeck U., and Prendergast G.C. Mechanism for elimination of a tumor suppressor: aberrant splicing of a brain-specific exon causes loss of function of Bin1 in melanoma. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 9689-9694
42. Gutmann D.H., Haipek C.A., Burke S.P., Sun C.X., Scoles D.R., and Pulst S.M. The NF2 interactor, hepatocyte growth factor-regulated tyrosine kinase substrate (HRS), associates with merlin in the "open" conformation and suppresses cell growth and motility. Hum. Mol. Genet. 10 (2001) 825-834
43. Hartsough M.T., and Steeg P.S. Nm23/nucleoside diphosphate kinase in human cancers. J. Bioenerg. Biomembr. 32 (2000) 301-308
44. Hittelman A.B., Burakov D., Iniguez-Lluhi J.A., Freedman L.P., and Garabedian M.J. Differential regulation of glucocorticoid receptor transcriptional activation via AF-1-associated proteins. EMBO J. 18 (1999) 5380-5388
45. Hocevar B.A., Mou F., Rennolds J.L., Morris S.M., Cooper J.A., and Howe P.H. Regulation of the Wnt signaling pathway by disabled-2 (Dab2). EMBO J. 22 (2003) 3084-3094
46. Hocevar B.A., Prunier C., and Howe P.H. Disabled-2 (Dab2) mediates transforming growth factor beta (TGFbeta)-stimulated fibronectin synthesis through TGFbeta-activated kinase 1 and activation of the JNK pathway. J. Biol. Chem. 280 (2005) 25920-25927
47. Hocevar B.A., Smine A., Xu X.X., and Howe P.H. The adaptor molecule Disabled-2 links the transforming growth factor beta receptors to the Smad pathway. EMBO J. 20 (2001) 2789-2801
48. Huang Y., Friess H., Kleeff J., Esposito I., Zhu Z., Liu S., Mok S.C., Zimmermann A., and Buchler M.W. Doc-2/hDab2 expression is up-regulated in primary pancreatic cancer but reduced in metastasis. Lab. Invest. 81 (2001) 863-873
49. Hyman J., Chen H., Di Fiore P.P., De Camilli P., and Brunger A.T. Epsin 1 undergoes nucleocytosolic shuttling and its eps15 interactor NH(2)-terminal homology (ENTH) domain, structurally similar to Armadillo and HEAT repeats, interacts with the transcription factor promyelocytic leukemia Zn(2)+ finger protein (PLZF). J. Cell Biol. 149 (2000) 537-546
50. Ishibashi Y., Maita H., Yano M., Koike N., Tamai K., Ariga H., and Iguchi-Ariga S.M. Pim-1 translocates sorting nexin 6/TRAF4-associated factor 2 from cytoplasm to nucleus. FEBS Lett. 506 (2001) 33-38
51. Jiang Y., Prunier C., and Howe P.H. The inhibitory effects of Disabled-2 (Dab2) on Wnt signaling are mediated through Axin. Oncogene 27 (2008) 1865-1875
52. Juven-Gershon T., Shifman O., Unger T., Elkeles A., Haupt Y., and Oren M. The Mdm2 oncoprotein interacts with the cell fate regulator Numb. Mol. Cell Biol. 18 (1998) 3974-3982
53. Kamura T., Burian D., Khalili H., Schmidt S.L., Sato S., Liu W.J., Conrad M.N., Conaway R.C., Conaway J.W., and Shilatifard A. Cloning and characterization of ELL-associated proteins EAP45 and EAP20. A role for yeast EAP-like proteins in regulation of gene expression by glucose. J. Biol. Chem. 276 (2001) 16528-16533
54. Kang J., Shi Y., Xiang B., Qu B., Su W., Zhu M., Zhang M., Bao G., Wang F., Zhang X., Yang R., Fan F., Chen X., Pei G., and Ma L. A nuclear function of beta-arrestin1 in GPCR signaling: regulation of histone acetylation and gene transcription. Cell 123 (2005) 833-847
55. Kantor J.D., McCormick B., Steeg P.S., and Zetter B.R. Inhibition of cell motility after nm23 transfection of human and murine tumor cells. Cancer Res. 53 (1993) 1971-1973
56. Karam J.A., Shariat S.F., Huang H.Y., Pong R.C., Ashfaq R., Shapiro E., Lotan Y., Sagalowsky A.I., Wu X.R., and Hsieh J.T. Decreased DOC-2/DAB2 expression in urothelial carcinoma of the bladder. Clin. Cancer Res. 13 (2007) 4400-4406
57. Kleeff J., Huang Y., Mok S.C., Zimmermann A., Friess H., and Buchler M.W. Down-regulation of DOC-2 in colorectal cancer points to its role as a tumor suppressor in this malignancy. Dis. Colon Rectum 45 (2002) 1242-1248
58. Krishnan K.S., Rikhy R., Rao S., Shivalkar M., Mosko M., Narayanan R., Etter P., Estes P.S., and Ramaswami M. Nucleoside diphosphate kinase, a source of GTP, is required for dynamin-dependent synaptic vesicle recycling. Neuron 30 (2001) 197-210
59. Kurten R.C., Cadena D.L., and Gill G.N. Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science 272 (1996) 1008-1010
60. Lanctot C., Cheutin T., Cremer M., Cavalli G., and Cremer T. Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat. Rev. Genet. 8 (2007) 104-115
61. Lanzetti L., and Di Fiore P.P. Endocytosis and cancer: an 'insider' network with dangerous liaisons. Traffic 9 (2008) 2011-2021
62. Li J., Belogortseva N., Porter D., and Park M. Chmp1A functions as a novel tumor suppressor gene in human embryonic kidney and ductal pancreatic tumor cells. Cell Cycle 7 (2008) 2886-2893
63. Li L., and Cohen S.N. Tsg101: a novel tumor susceptibility gene isolated by controlled homozygous functional knockout of allelic loci in mammalian cells. Cell 85 (1996) 319-329
64. Li L., Liao J., Ruland J., Mak T.W., and Cohen S.N. A TSG101/MDM2 regulatory loop modulates MDM2 degradation and MDM2/p53 feedback control. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 1619-1624
65. Liu H., Chen B., Xiong H., Huang Q.H., Zhang Q.H., Wang Z.G., Li B.L., Chen Z., and Chen S.J. Functional contribution of EEN to leukemogenic transformation by MLL-EEN fusion protein. Oncogene 23 (2004) 3385-3394
66. Ma L., and Pei G. β-Arrestin signaling and regulation of transcription. J. Cell Sci. 120 (2007) 213-218
67. Majumder P., Choudhury A., Banerjee M., Lahiri A., and Bhattacharyya N.P. Interactions of HIPPI, a molecular partner of Huntingtin interacting protein HIP1, with the specific motif present at the putative promoter sequence of the caspase-1, caspase-8 and caspase-10 genes. FEBS J. 274 (2007) 3886-3899
68. Miaczynska M., Christoforidis S., Giner A., Shevchenko A., Uttenweiler-Joseph S., Habermann B., Wilm M., Parton R.G., and Zerial M. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116 (2004) 445-456
69. Mills I.G., Gaughan L., Robson C., Ross T., McCracken S., Kelly J., and Neal D.E. Huntingtin interacting protein 1 modulates the transcriptional activity of nuclear hormone receptors. J. Cell Biol. 170 (2005) 191-200
70. Mishra S.K., Keyel P.A., Hawryluk M.J., Agostinelli N.R., Watkins S.C., and Traub L.M. Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J. 21 (2002) 4915-4926
71. Miura S., Takeshita T., Asao H., Kimura Y., Murata K., Sasaki Y., Hanai J.I., Beppu H., Tsukazaki T., Wrana J.L., Miyazono K., and Sugamura K. Hgs (Hrs), a FYVE domain protein, is involved in Smad signaling through cooperation with SARA. Mol. Cell Biol. 20 (2000) 9346-9355
72. Mo W., Zhang L., Yang G., Zhai J., Hu Z., Chen Y., Chen X., Hui L., Huang R., and Hu G. Nuclear beta-arrestin1 functions as a scaffold for the dephosphorylation of STAT1 and moderates the antiviral activity of IFN-γ. Mol. Cell 31 (2008) 695-707
73. Mohney R.P., Das M., Bivona T.G., Hanes R., Adams A.G., Philips M.R., and O'Bryan J.P. Intersectin activates Ras but stimulates transcription through an independent pathway involving JNK. J. Biol. Chem. 278 (2003) 47038-47045
74. Morita E., Sandrin V., Chung H.Y., Morham S.G., Gygi S.P., Rodesch C.K., and Sundquist W.I. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26 (2007) 4215-4227
75. Mosesson Y., Mills G.B., and Yarden Y. Derailed endocytosis: an emerging feature of cancer. Nat. Rev. Cancer 8 (2008) 835-850
76. Mukherjee A., Veraksa A., Bauer A., Rosse C., Camonis J., and Artavanis-Tsakonas S. Regulation of Notch signalling by non-visual β-arrestin. Nat. Cell Biol. 7 (2005) 1191-1201
77. Munn D.H., and Mellor A.L. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J. Clin. Invest. 117 (2007) 1147-1154
78. Muromoto R., Sugiyama K., Yamamoto T., Oritani K., Shimoda K., and Matsuda T. Physical and functional interactions between Daxx and TSG101. Biochem. Biophys. Res. Commun. 316 (2004) 827-833
79. Neuhaus E.M., Mashukova A., Barbour J., Wolters D., and Hatt H. Novel function of β-arrestin2 in the nucleus of mature spermatozoa. J. Cell Sci. 119 (2006) 3047-3056
80. Nguyen L.N., Holdren M.S., Nguyen A.P., Furuya M.H., Bianchini M., Levy E., Mordoh J., Liu A., Guncay G.D., Campbell J.S., and Parks W.T. Sorting nexin 1 down-regulation promotes colon tumorigenesis. Clin. Cancer Res. 12 (2006) 6952-6959
81. Nicolas M., Wolfer A., Raj K., Kummer J.A., Mill P., van Noort M., Hui C.C., Clevers H., Dotto G.P., and Radtke F. Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 33 (2003) 416-421
82. Niehof M., and Borlak J. EPS15R, TASP1, and PRPF3 are novel disease candidate genes targeted by HNF4α splice variants in hepatocellular carcinomas. Gastroenterology 134 (2008) 1191-1202
83. Oh K.B., Stanton M.J., West W.W., Todd G.L., and Wagner K.U. Tsg101 is upregulated in a subset of invasive human breast cancers and its targeted overexpression in transgenic mice reveals weak oncogenic properties for mammary cancer initiation. Oncogene 26 (2007) 5950-5959
84. Ohmori K., Endo Y., Yoshida Y., Ohata H., Taya Y., and Enari M. Monomeric but not trimeric clathrin heavy chain regulates p53-mediated transcription. Oncogene 27 (2008) 2215-2227
85. Palacios F., Schweitzer J.K., Boshans R.L., and D'Souza-Schorey C. ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat. Cell Biol. 4 (2002) 929-936
86. Passananti C., Floridi A., and Fanciulli M. Che-1/AATF, a multivalent adaptor connecting transcriptional regulation, checkpoint control, and apoptosis. Biochem. Cell Biol. 85 (2007) 477-483
87. Pece S., Serresi M., Santolini E., Capra M., Hulleman E., Galimberti V., Zurrida S., Maisonneuve P., Viale G., and Di Fiore P.P. Loss of negative regulation by Numb over Notch is relevant to human breast carcinogenesis. J. Cell Biol. 167 (2004) 215-221
88. Pilecka I., Banach-Orlowska M., and Miaczynska M. Nuclear functions of endocytic proteins. Eur. J. Cell Biol. 86 (2007) 533-547
89. Pineda-Lucena A., Ho C.S., Mao D.Y., Sheng Y., Laister R.C., Muhandiram R., Lu Y., Seet B.T., Katz S., Szyperski T., Penn L.Z., and Arrowsmith C.H. A structure-based model of the c-Myc/Bin1 protein interaction shows alternative splicing of Bin1 and c-Myc phosphorylation are key binding determinants. J. Mol. Biol. 351 (2005) 182-194
90. Postel E.H., Berberich S.J., Rooney J.W., and Kaetzel D.M. Human NM23/nucleoside diphosphate kinase regulates gene expression through DNA binding to nuclease-hypersensitive transcriptional elements. J. Bioenerg. Biomembr. 32 (2000) 277-284
91. Prendergast G.C., Muller A.J., Ramalingam A., and Chang M.Y. BAR the door: cancer suppression by amphiphysin-like genes. Biochim. Biophys. Acta 1795 (2009) 25-36
92. Radtke F., and Raj K. The role of Notch in tumorigenesis: oncogene or tumour suppressor?. Nat. Rev. Cancer 3 (2003) 756-767
93. Ramalingam A., Duhadaway J.B., Sutanto-Ward E., Wang Y., Dinchuk J., Huang M., Donover P.S., Boulden J., McNally L.M., Soler A.P., Muller A.J., Duncan M.K., and Prendergast G.C. Bin3 deletion causes cataracts and increased susceptibility to lymphoma during aging. Cancer Res. 68 (2008) 1683-1690
94. Ramalingam A., Farmer G.E., Stamato T.D., and Prendergast G.C. Bin1 interacts with and restrains the DNA end-binding protein complex Ku. Cell Cycle 6 (2007) 1914-1918
95. Rao D.S., Bradley S.V., Kumar P.D., Hyun T.S., Saint-Dic D., Oravecz-Wilson K., Kleer C.G., and Ross T.S. Altered receptor trafficking in Huntingtin Interacting Protein 1-transformed cells. Cancer Cell 3 (2003) 471-482
96. Rao D.S., Hyun T.S., Kumar P.D., Mizukami I.F., Rubin M.A., Lucas P.C., Sanda M.G., and Ross T.S. Huntingtin-interacting protein 1 is overexpressed in prostate and colon cancer and is critical for cellular survival. J. Clin. Invest. 110 (2002) 351-360
97. Rashid S., Pilecka I., Torun A., Olchowik M., Bielinska B., and Miaczynska M. Endosomal adaptor proteins APPL1 and APPL2 are novel activators of beta-catenin/TCF-mediated transcription. J. Biol. Chem. (2009) (Epub ahead of print)
98. Rayner K., Chen Y.X., Hibbert B., White D., Miller H., Postel E.H., and O'Brien E.R. Discovery of NM23-H2 as an estrogen receptor beta-associated protein: role in estrogen-induced gene transcription and cell migration. J. Steroid Biochem. Mol. Biol. 108 (2008) 72-81
99. Ren G., Vajjhala P., Lee J.S., Winsor B., and Munn A.L. The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol Mol. Biol. Rev. 70 (2006) 37-120
100. Rochdi M.D., Laroche G., Dupre E., Giguere P., Lebel A., Watier V., Hamelin E., Lepine M.C., Dupuis G., and Parent J.L. Nm23-H2 interacts with a G protein-coupled receptor to regulate its endocytosis through an Rac1-dependent mechanism. J. Biol. Chem. 279 (2004) 18981-18989
101. Roscic A., Moller A., Calzado M.A., Renner F., Wimmer V.C., Gresko E., Ludi K.S., and Schmitz M.L. Phosphorylation-dependent control of Pc2 SUMO E3 ligase activity by its substrate protein HIPK2. Mol. Cell 24 (2006) 77-89
102. Ross T.S., Bernard O.A., Berger R., and Gilliland D.G. Fusion of Huntingtin interacting protein 1 to platelet-derived growth factor β receptor (PDGFbetaR) in chronic myelomonocytic leukemia with t(5;7)(q33;q11.2). Blood 91 (1998) 4419-4426
103. Ruland J., Sirard C., Elia A., MacPherson D., Wakeham A., Li L., de la Pompa J.L., Cohen S.N., and Mak T.W. p53 Accumulation, defective cell proliferation, and early embryonic lethality in mice lacking tsg101. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 1859-1864
104. Saito T., Jones C.C., Huang S., Czech M.P., and Pilch P.F. The interaction of Akt with APPL1 is required for insulin-stimulated Glut4 translocation. J. Biol. Chem. 282 (2007) 32280-32287
105. Sakamuro D., Elliott K.J., Wechsler-Reya R., and Prendergast G.C. BIN1 is a novel MYC-interacting protein with features of a tumour suppressor. Nat. Genet. 14 (1996) 69-77
106. Schmid E.M., and McMahon H.T. Integrating molecular and network biology to decode endocytosis. Nature 448 (2007) 883-888
107. Scoles D.R., Huynh D.P., Chen M.S., Burke S.P., Gutmann D.H., and Pulst S.M. The neurofibromatosis 2 tumor suppressor protein interacts with hepatocyte growth factor-regulated tyrosine kinase substrate. Hum. Mol. Genet. 9 (2000) 1567-1574
108. Scoles D.R., Nguyen V.D., Qin Y., Sun C.X., Morrison H., Gutmann D.H., and Pulst S.M. Neurofibromatosis 2 (NF2) tumor suppressor schwannomin and its interacting protein HRS regulate STAT signaling. Hum. Mol. Genet. 11 (2002) 3179-3189
109. Sheng Z., Sun W., Smith E., Cohen C., and Xu X.X. Restoration of positioning control following Disabled-2 expression in ovarian and breast tumor cells. Oncogene 19 (2000) 4847-4854
110. Shilatifard A. Identification and purification of the Holo-ELL complex. Evidence for the presence of ELL-associated proteins that suppress the transcriptional inhibitory activity of ELL. J. Biol. Chem. 273 (1998) 11212-11217
111. So C.W., Lin M., Ayton P.M., Chen E.H., and Cleary M.L. Dimerization contributes to oncogenic activation of MLL chimeras in acute leukemias. Cancer Cell 4 (2003) 99-110
112. Stauffer D.R., Howard T.L., Nyun T., and Hollenberg S.M. CHMP1 is a novel nuclear matrix protein affecting chromatin structure and cell-cycle progression. J. Cell Sci. 114 (2001) 2383-2393
113. Stuffers S., Brech A., and Stenmark H. ESCRT proteins in physiology and disease. Exp. Cell Res. 315 (2009) 1619-1626
114. Sun J., and Lin X. β-Arrestin 2 is required for lysophosphatidic acid-induced NF-κB activation. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 17085-17090
115. Sun Z., Pan J., Hope W.X., Cohen S.N., and Balk S.P. Tumor susceptibility gene 101 protein represses androgen receptor transactivation and interacts with p300. Cancer 86 (1999) 689-696
116. Tanaka N., Kyuuma M., and Sugamura K. Endosomal sorting complex required for transport proteins in cancer pathogenesis, vesicular transport, and non-endosomal functions. Cancer. Sci. 99 (2008) 1293-1303
117. Tong X.K., Hussain N.K., Adams A.G., O'Bryan J.P., and McPherson P.S. Intersectin can regulate the Ras/MAP kinase pathway independent of its role in endocytosis. J. Biol. Chem. 275 (2000) 29894-29899
118. Toyoshima M., Tanaka N., Aoki J., Tanaka Y., Murata K., Kyuuma M., Kobayashi H., Ishii N., Yaegashi N., and Sugamura K. Inhibition of tumor growth and metastasis by depletion of vesicular sorting protein Hrs: its regulatory role on E-cadherin and β-catenin. Cancer Res. 67 (2007) 5162-5171
119. Tsang H.T., Connell J.W., Brown S.E., Thompson A., Reid E., and Sanderson C.M. A systematic analysis of human CHMP protein interactions: additional MIT domain-containing proteins bind to multiple components of the human ESCRT III complex. Genomics 88 (2006) 333-346
120. Tseng C.P., Ely B.D., Li Y., Pong R.C., and Hsieh J.T. 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 (1998) 3542-3553
121. Tseng C.P., Ely B.D., Pong R.C., Wang Z., Zhou J., and Hsieh J.T. 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 (1999) 31981-31986
122. Vaccari T., and Bilder D. At the crossroads of polarity, proliferation and apoptosis: the use of Drosophila to unravel the multifaceted role of endocytosis in tumor suppression. Mol. Oncol. 3 (2009) 354-365
123. Vecchi M., and Di Fiore P.P. It's HIP to be a hub: new trends for old-fashioned proteins. J. Cell Biol. 170 (2005) 169-171
124. Vecchi M., Polo S., Poupon V., van de Loo J.W., Benmerah A., and Di Fiore P.P. Nucleocytoplasmic shuttling of endocytic proteins. J. Cell Biol. 153 (2001) 1511-1517
125. Walker J.K., Fong A.M., Lawson B.L., Savov J.D., Patel D.D., Schwartz D.A., and Lefkowitz R.J. Beta-arrestin-2 regulates the development of allergic asthma. J. Clin. Invest. 112 (2003) 566-574
126. Wang P., Wu Y., Ge X., Ma L., and Pei G. Subcellular localization of beta-arrestins is determined by their intact N domain and the nuclear export signal at the C terminus. J. Biol. Chem. 278 (2003) 11648-11653
127. Wang S.C., Makino K., Xia W., Kim J.S., Im S.A., Peng H., Mok S.C., Singletary S.E., and Hung M.C. DOC-2/hDab-2 inhibits ILK activity and induces anoikis in breast cancer cells through an Akt-independent pathway. Oncogene 20 (2001) 6960-6964
128. Wang Z., Tseng C.P., Pong R.C., Chen H., McConnell J.D., Navone N., and Hsieh J.T. The mechanism of growth-inhibitory effect of DOC-2/DAB2 in prostate cancer. Characterization of a novel GTPase-activating protein associated with N-terminal domain of DOC-2/DAB2. J. Biol. Chem. 277 (2002) 12622-12631
129. Watanabe M., Yanagi Y., Masuhiro Y., Yano T., Yoshikawa H., Yanagisawa J., and Kato S. A putative tumor suppressor, TSG101, acts as a transcriptional suppressor through its coiled-coil domain. Biochem. Biophys. Res. Commun. 245 (1998) 900-905
130. Wechsler-Reya R., Elliott K., Herlyn M., and Prendergast G.C. The putative tumor suppressor BIN1 is a short-lived nuclear phosphoprotein, the localization of which is altered in malignant cells. Cancer Res. 57 (1997) 3258-3263
131. Wechsler-Reya R.J., Elliott K.J., and Prendergast G.C. A role for the putative tumor suppressor Bin1 in muscle cell differentiation. Mol. Cell Biol. 18 (1998) 566-575
132. Xiao K., McClatchy D.B., Shukla A.K., Zhao Y., Chen M., Shenoy S.K., Yates III J.R., and Lefkowitz R.J. Functional specialization of β-arrestin interactions revealed by proteomic analysis. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 12011-12016
133. Xie W., Li L., and Cohen S.N. Cell cycle-dependent subcellular localization of the TSG101 protein and mitotic and nuclear abnormalities associated with TSG101 deficiency. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 1595-1600
134. Xu Z., Liang L., Wang H., Li T., and Zhao M. HCRP1, a novel gene that is downregulated in hepatocellular carcinoma, encodes a growth-inhibitory protein. Biochem. Biophys. Res. Commun. 311 (2003) 1057-1066
135. Yang D.H., Smith E.R., Cohen C., Wu H., Patriotis C., Godwin A.K., Hamilton T.C., and Xu X.X. Molecular events associated with dysplastic morphologic transformation and initiation of ovarian tumorigenicity. Cancer 94 (2002) 2380-2392
136. Yang L., Lin H.K., Altuwaijri S., Xie S., Wang L., and Chang C. APPL suppresses androgen receptor transactivation via potentiating Akt activity. J. Biol. Chem. 278 (2003) 16820-16827
137. Young T.W., Mei F.C., Rosen D.G., Yang G., Li N., Liu J., and Cheng X. Up-regulation of tumor susceptibility gene 101 protein in ovarian carcinomas revealed by proteomics analyses. Mol. Cell Proteomics 6 (2007) 294-304
138. Young T.W., Rosen D.G., Mei F.C., Li N., Liu J., Wang X.F., and Cheng X. Up-regulation of tumor susceptibility gene 101 conveys poor prognosis through suppression of p21 expression in ovarian cancer. Clin. Cancer Res. 13 (2007) 3848-3854
139. Zhong Q., Chen Y., Jones D., and Lee W.H. Perturbation of TSG101 protein affects cell cycle progression. Cancer Res. 58 (1998) 2699-2702
140. Zhou J., and Hsieh J.T. The inhibitory role of DOC-2/DAB2 in growth factor receptor-mediated signal cascade. DOC-2/DAB2-mediated inhibition of ERK phosphorylation via binding to Grb2. J. Biol. Chem. 276 (2001) 27793-27798
141. Zhou J., Scholes J., and Hsieh J.T. Characterization of a novel negative regulator (DOC-2/DAB2) of c-Src in normal prostatic epithelium and cancer. J. Biol. Chem. 278 (2003) 6936-6941
142. Zhoul J., Hernandez G., Tu S.W., Huang C.L., Tseng C.P., and Hsieh J.T. The role of DOC-2/DAB2 in modulating androgen receptor-mediated cell growth via the nongenomic c-Src-mediated pathway in normal prostatic epithelium and cancer. Cancer Res. 65 (2005) 9906-9913