RNAi-based functional selection identifies novel cell migration determinants dependent on PI3K and AKT pathways

Nature Communications

Volumn 5, Issue , 2014, Pages

  Seo, Minchul ^a,b   Lee, Shinrye ^a,c   Kim, Jong Heon ^a   Lee, Won Ha ^d   Hu, Guang ^e   Elledge, Stephen J ^f   Suk, Kyoungho ^a  

^a Kyungpook National University   (South Korea)

^b Dongguk University College of Medicine   (South Korea)

^c Korea Brain Research Institute (KBRI)   (South Korea)

^d Kyungpook National University   (South Korea)

^e NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ANAPLASTIC LYMPHOMA KINASE; CASEIN KINASE 2 ALPHA PRIME POLYPEPTIDE PROTEIN; COMPLEMENTARY DNA; CSNK2A2 PROTEIN; DOCK3 PROTEIN; GENOMIC DNA; INTERFERON REGULATORY FACTOR 4; MITOMYCIN; MYO5A PROTEIN; MYOTUBULARIN RELATED PROTEIN 1; P55GAMMA PROTEIN; P70S6K1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; PROTEIN P55; PROTEIN P85; PTPN14 PROTEIN; PUROMYCIN; RETINOBLASTOMA BINDING PROTEIN 1; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG; PROTEIN SUBUNIT; PROTEIN TYROSINE KINASE;

GENE EXPRESSION; GENETIC ANALYSIS; GENOME; IDENTIFICATION METHOD; MAMMAL; PHENOTYPE; RNA; SIGNALING;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL INVASION; CELL MIGRATION; CELL VIABILITY; COST EFFECTIVENESS ANALYSIS; EMBRYO; GENE OVEREXPRESSION; GENE SEQUENCE; GENE SILENCING; GENETIC SELECTION; HUMAN; HUMAN CELL; MOUSE; MTT ASSAY; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; WOUND HEALING; 3T3 CELL LINE; ANIMAL; CELL MOTION; CYTOLOGY; ENZYME ACTIVATION; FIBROBLAST; GENETIC TRANSFECTION; GENOME; HEK293 CELL LINE; IMMUNOPRECIPITATION; METABOLISM; PROTEIN SUBUNIT; REPRODUCIBILITY;

MAMMALIA;

ANIMALS; CELL MOVEMENT; ENZYME ACTIVATION; FIBROBLASTS; GENOME; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; MICE; NIH 3T3 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN SUBUNITS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RECEPTOR PROTEIN-TYROSINE KINASES; REPRODUCIBILITY OF RESULTS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84923369247     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6217     Document Type: Article

References (70)

1. Vicente-Manzanares, M., Webb, D. J. & Horwitz, A. R. Cell migration at a glance. J. Cell. Sci. 118, 4917-4919 (2005).
2. Franz, C. M., Jones, G. E. & Ridley, A. J. Cell migration in development and disease. Dev. Cell 2, 153-158 (2002).
3. Luster, A. D., Alon, R. & von Andrian, U. H. Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 6, 1182-1190 (2005).
4. Cram, E. J., Shang, H. & Schwarzbauer, J. E. A systematic RNA interference screen reveals a cell migration gene network in C. elegans. J. Cell Sci. 119, 4811-4818 (2006).
5. Wang, X. et al. Analysis of cell migration using whole-genome expression profiling of migratory cells in the Drosophila ovary. Dev. Cell 10, 483-495 (2006).
6. Dykxhoorn, D. M., Novina, C. D. & Sharp, P. A. Killing the messenger: short RNAs that silence gene expression. Nat. Rev. Mol. Cell Biol. 4, 457-467 (2003).
7. Paddison, P. J. et al. A resource for large-scale RNA-interference-based screens in mammals. Nature 428, 427-431 (2004).
8. Simpson, K. J. et al. Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat. Cell Biol. 10, 1027-1038 (2008).
9. Vitorino, P. & Meyer, T. Modular control of endothelial sheet migration. Gene Dev. 22, 3268-3281 (2008).
10. Winograd-Katz, S. E., Itzkovitz, S., Kam, Z. & Geiger, B. Multiparametric analysis of focal adhesion formation by RNAi-mediated gene knockdown. J. Cell Biol. 186, 423-436 (2009).
11. Collins, C. S. et al. A small interfering RNA screen for modulators of tumor cell motility identifies MAP4K4 as a promigratory kinase. Proc. Natl Acad. Sci. USA 103, 3775-3780 (2006).
12. Bai, S. W. et al. Identification and characterization of a set of conserved and new regulators of cytoskeletal organization, cell morphology and migration. BMC Biol. 9, 54-71 (2011).
13. Smolen, G. A. et al. A genome-wide RNAi screen identifies multiple RSK-dependent regulators of cell migration. Gene Dev. 24, 2654-2665 (2010).
14. Schlabach, M. R. et al. Cancer proliferation gene discovery through functional genomics. Science 319, 620-624 (2008).
15. Silva, J. M. et al. Second-generation shRNA libraries covering the mouse and human genomes. Nat. Genet. 37, 1281-1288 (2005).
16. Yang, J. et al. Genome-wide RNAi screening identifies genes inhibiting the migration of glioblastoma cells. PLoS ONE 8, e61915 (2013).
17. Qian, Y. et al. PI3K induced actin filament remodeling through Akt and p70S6K1: implication of essential role in cell migration. Am. J. Physiol. Cell Physiol. 286, C153-C163 (2004).
18. Song, M. S., Salmena, L. & Pandolfi, P. P. The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell Biol. 13, 283-296 (2012).
19. Martelli, A. M. et al. Targeting the translational apparatus to improve leukemia therapy: roles of the PI3K/PTEN/Akt/mTOR pathway. Leukemia 25, 1064-1079 (2011).
20. Schlessinger, J. & Ullrich, A. Growth factor signaling by receptor tyrosine kinases. Neuron 9, 383-391 (1992).
21. Raucher, D. et al. Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion. Cell 100, 221-228 (2000).
22. Zhu, Q. et al. Phosphoinositide 3-OH kinase p85alpha and p110beta are essential for androgen receptor transactivation and tumor progression in prostate cancers. Oncogene 27, 4569-4579 (2008).
23. Kim, D. H. & Rossi, J. J. Strategies for silencing human disease using RNA interference. Nat. Rev. Genet. 8, 173-184 (2007).
24. Cheng, J. C., Moore, T. B. & Sakamoto, K. M. RNA interference and human disease. Mol. Genet. Metab. 80, 121-128 (2003).
25. Alvarez-Calderon, F., Gregory, M. A. & Degregori, J. Using functional genomics to overcome therapeutic resistance in hematological malignancies. Immunol. Res. 33, 100-115 (2012).
26. Dahlman, K. B. et al. Modulators of prostate cancer cell proliferation and viability identified by short-hairpin RNA library screening. PLoS ONE 7, e34414 (2012).
27. Hu, K., Law, J. H., Fotovati, A. & Dunn, S. E. Small interfering RNA library screen identified polo-like kinase-1 (PLK1) as a potential therapeutic target for breast cancer that uniquely eliminates tumor-initiating cells. Breast Cancer Res. 14, R22 (2012).
28. Wan, X. et al. Identification of the FoxM1/Bub1b signaling pathway as a required component for growth and survival of rhabdomyosarcoma. Cancer Res. 72, 5889-5899 (2012).
29. Draviam, V. M. et al. A functional genomic screen identifies a role for TAO1 kinase in spindle-checkpoint signalling. Nat. Cell Biol. 9, 556-564 (2007).
30. Root, D. E., Hacohen, N., Hahn, W. C., Lander, E. S. & Sabatini, D. M. Genome-scale loss-of-function screening with a lentiviral RNAi library. Nat. Methods 3, 715-719 (2006).
31. Hu, G. et al. A genome-wide RNAi screen identifies a new transcriptional module required for self-renewal. Gene Dev. 23, 837-848 (2009).
32. Schmitz, M. H. et al. Live-cell imaging RNAi screen identifies PP2A-B55alpha and importin-beta1 as key mitotic exit regulators in human cells. Nat. Cell. Biol. 12, 886-893 (2010).
33. Yang, R. et al. A genome-wide siRNA screen to identify modulators of insulin sensitivity and gluconeogenesis. PLoS ONE 7, e36384 (2012).
34. Romieu-Mourez, R., Landesman-Bollag, E., Seldin, D. C. & Sonenshein, G. E. Protein kinase CK2 promotes aberrant activation of nuclear factor-kappaB, transformed phenotype, and survival of breast cancer cells. Cancer Res. 62, 6770-6778 (2002).
35. Channavajhala, P. & Seldin, D. C. Functional interaction of protein kinase CK2 and c-Myc in lymphomagenesis. Oncogene 21, 5280-5288 (2002).
36. Munstermann, U. et al. Casein kinase II is elevated in solid human tumours and rapidly proliferating non-neoplastic tissue. Eur. J. Biochem. 189, 251-257 (1990).
37. Zhang, P. et al. Identification and functional characterization of p130Cas as a substrate of protein tyrosine phosphatase nonreceptor 14. Oncogene 32, 2087-2095 (2012).
38. Buj-Bello, A. et al. Muscle-specific alternative splicing of myotubularin-related 1 gene is impaired in DM1 muscle cells. Hum. Mol. Genet. 11, 2297-2307 (2002).
39. Tronchere, H. et al. Production of phosphatidylinositol 5-phosphate by the phosphoinositide 3-phosphatase myotubularin in mammalian cells. J. Biol. Chem. 279, 7304-7312 (2004).
40. Ryeom, S. et al. Targeted deletion of the calcineurin inhibitor DSCR1 suppresses tumor growth. Cancer Cell 13, 420-431 (2008).
41. Aylon, Y. et al. A positive feedback loop between the p53 and Lats2 tumor suppressors prevents tetraploidization. Genes Dev. 20, 2687-2700 (2006).
42. McPherson, J. P. et al. Lats2/Kpm is required for embryonic development, proliferation control and genomic integrity. EMBO J. 23, 3677-3688 (2004).
43. Ke, H. et al. Putative tumor suppressor Lats2 induces apoptosis through downregulation of Bcl-2 and Bcl-x(L). Exp. Cell. Res. 298, 329-338 (2004).
44. Li, Y. et al. Lats2, a putative tumor suppressor, inhibits G1/S transition. Oncogene 22, 4398-4405 (2003).
45. Huang, H. & Tindall, D. J. Dynamic FoxO transcription factors. J. Cell Sci. 120, 2479-2487 (2007).
46. Zhang, H. et al. FOXO1 inhibits Runx2 transcriptional activity and prostate cancer cell migration and invasion. Cancer Res. 71, 3257-3267 (2011).
47. Huang, H. & Tindall, D. J. Regulation of FOXO protein stability via ubiquitination and proteasome degradation. Biochim. Biophys. Acta 1813, 1961-1964 (2011).
48. Brunet, A. et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868 (1999).
49. Meng, Q., Xia, C., Fang, J., Rojanasakul, Y. & Jiang, B. H. Role of PI3K and AKT specific isoforms in ovarian cancer cell migration, invasion and proliferation through the p70S6K1 pathway. Cell Signal. 18, 2262-2271 (2006).
50. Liu, L. et al. Rapamycin inhibits cell motility by suppression of mTORmediated S6K1 and 4E-BP1 pathways. Oncogene 25, 7029-7040 (2006).
51. Poon, M. et al. Rapamycin inhibits vascular smooth muscle cell migration. J. Clin. Invest. 98, 2277-2283 (1996).
52. Bunney, T. D. & Katan, M. Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat. Rev. Cancer 10, 342-352 (2010).
53. Inukai, K. et al. Five isoforms of the phosphatidylinositol 3-kinase regulatory subunit exhibit different associations with receptor tyrosine kinases and their tyrosine phosphorylations. FEBS Lett. 490, 32-38 (2001).
54. Vanhaesebroeck, B., Guillermet-Guibert, J., Graupera, M. & Bilanges, B. The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell Biol. 11, 329-341 (2010).
55. Courtney, K. D., Corcoran, R. B. & Engelman, J. A. The PI3K pathway as drug target in human cancer. J. Clin. Oncol. 28, 1075-1083 (2010).
56. Hu, J. et al. Overexpression of the N-terminal end of the p55gamma regulatory subunit of phosphatidylinositol 3-kinase blocks cell cycle progression in gastric carcinoma cells. Int. J. Oncol. 26, 1321-1327 (2005).
57. Wang, G. et al. PI3K stimulates DNA synthesis and cell-cycle progression via its p55PIK regulatory subunit interaction with PCNA. Mol. Cancer Ther. 12, 2100-2109 (2013).
58. Wang, G. et al. Blocking p55PIK signaling inhibits proliferation and induces differentiation of leukemia cells. Cell Death Differ. 19, 1870-1879 (2012).
59. Wang, G. et al. p55PIK-PI3K stimulates angiogenesis in colorectal cancer cell by activating NF-kappaB pathway. Angiogenesis 16, 561-573 (2013).
60. Zhang, L. et al. Integrative genomic analysis of phosphatidylinositol 30-kinase family identifies PIK3R3 as a potential therapeutic target in epithelial ovarian cancer. Clin. Cancer Res. 13, 5314-5321 (2007).
61. Waite, K. & Eickholt, B. J. The neurodevelopmental implications of PI3K signaling. Curr. Top. Microbiol. Immunol. 346, 245-265 (2010).
62. Roskoski, Jr. R. Anaplastic lymphoma kinase (ALK): structure, oncogenic activation, and pharmacological inhibition. Pharmacol. Res. 68, 68-94 (2013).
63. Polgar, D. et al. Truncated ALK derived from chromosomal translocation t(2;5)(p23;q35) binds to the SH3 domain of p85-PI3K. Mutat. Res. 570, 9-15 (2005).
64. Wasik, M. A. et al. Anaplastic lymphoma kinase (ALK)-induced malignancies: novel mechanisms of cell transformation and potential therapeutic approaches. Semin. Oncol. 36, S27-S35 (2009).
65. Palmer, R. H., Vernersson, E., Grabbe, C. & Hallberg, B. Anaplastic lymphoma kinase: signalling in development and disease. Biochem. J. 420, 345-361 (2009).
66. Iwahara, T. et al. Molecular characterization of ALK, a receptor tyrosine kinase expressed specifically in the nervous system. Oncogene 14, 439-449 (1997).
67. Yao, S. et al. Anaplastic lymphoma kinase is required for neurogenesis in the developing central nervous system of zebrafish. PLoS ONE 8, e63757 (2013).
68. Serrano, M., Lin, A. W., McCurrach, M. E., Beach, D. & Lowe, S. W. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88, 593-602 (1997).
69. Seo, M., Lee, W. H. & Suk, K. Identification of novel cell migration-promoting genes by a functional genetic screen. FASEB J. 24, 464-478 (2010).
70. Bassi, R. et al. HMGB1 as an autocrine stimulus in human T98G glioblastoma cells: role in cell growth and migration. J. Neurooncol. 87, 23-33 (2008).