RAS signalling through PI3-Kinase controls cell migration via modulation of Reelin expression

Nature Communications

Volumn 7, Issue , 2016, Pages

  Castellano, Esther ^a,b   Molina Arcas, Miriam ^a,c   Krygowska, Agata Adelajda ^b   East, Philip ^a   Warne, Patricia ^a   Nicol, Alastair ^a   Downward, Julian ^a,c  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN P110ALPHA; RAC PROTEIN; REELIN; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; PROTEIN BINDING; RAC1 PROTEIN; RAS PROTEIN; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

ANATOMY; CANCER; CELLS AND CELL COMPONENTS; GENE EXPRESSION; MATRIX; MOTILITY; MUTATION; PROTEIN; TUMOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CELL INTERACTION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CELL POLARITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GENE; GENE DISRUPTION; GENE EXPRESSION; GENE INTERACTION; LUNG CANCER; MOUSE; NONHUMAN; ONCOGENE RAS; PIK3CA GENE; POINT MUTATION; PROTEIN EXPRESSION; RNA BINDING; RNA STABILITY; UPREGULATION; ANIMAL; CELL MOTION; LUNG TUMOR; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

KRAS; SLOVENIA;

ANIMALS; CADHERINS; CELL ADHESION MOLECULES, NEURONAL; CELL MOVEMENT; CELL POLARITY; ENZYME ACTIVATION; EXTRACELLULAR MATRIX PROTEINS; LUNG NEOPLASMS; MICE; NERVE TISSUE PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN BINDING; RAC1 GTP-BINDING PROTEIN; RAS PROTEINS; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84963956141     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11245     Document Type: Article

References (67)

1. Cain, R. J. & Ridley, A. J. Phosphoinositide 3-kinases in cell migration. Biol. Cell 101, 13-29 (2009).
2. Raja, Sivamani, K., Garcia, M. S. & Isseroff, R. R. Wound re-epithelialization: modulating keratinocyte migration in wound healing. Front. Biosci. 12, 2849-2868 (2007).
3. Vicente-Manzanares, M. & Horwitz, A. R. Cell migration: an overview. Methods Mol. Biol. 769, 1-24 (2011).
4. Campbell, P. M. & Der, C. J. Oncogenic Ras and its role in tumor cell invasion and metastasis. Semin. Cancer Biol. 14, 105-114 (2004).
5. Giehl, K. Oncogenic Ras in tumour progression and metastasis. Biol. Chem. 386, 193-205 (2005).
6. Grunert, S., Jechlinger, M. & Beug, H. Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat. Rev. Mol. Cell Biol. 4, 657-665 (2003).
7. Smakman, N., Borel Rinkes, I. H., Voest, E. E. & Kranenburg, O. Control of colorectal metastasis formation by K-Ras. Biochim. Biophys. Acta 1756, 103-114 (2005).
8. Pollock, C. B., Shirasawa, S., Sasazuki, T., Kolch, W. & Dhillon, A. S. Oncogenic K-RAS is required to maintain changes in cytoskeletal organization, adhesion, and motility in colon cancer cells. Cancer Res. 65, 1244-1250 (2005).
9. Vial, E., Sahai, E. & Marshall, C. J. ERK-MAPK signaling coordinately regulates activity of Rac1 and RhoA for tumor cell motility. Cancer Cell 4, 67-79 (2003).
10. Jimenez, C. et al. Role of the PI3K regulatory subunit in the control of actin organization and cell migration. J. Cell Biol. 151, 249-262 (2000).
11. Tolias, K. F., Cantley, L. C. & Carpenter, C. L. Rho family GTPases bind to phosphoinositide kinases. J. Biol. Chem. 270, 17656-17659 (1995).
12. Yang, Y. et al. ZEB1 sensitizes lung adenocarcinoma to metastasis suppression by PI3K antagonism. J. Clin. Invest. 124, 2696-2708 (2014).
13. Johnson, L. et al. Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410, 1111-1116 (2001).
14. Makrodouli, E. et al. BRAF and RAS oncogenes regulate Rho GTPase pathways to mediate migration and invasion properties in human colon cancer cells: a comparative study. Mol. Cancer 10, 118 (2011).
15. Roberts, M. L. et al. Microarray analysis of the differential transformation mediated by Kirsten and Harvey Ras oncogenes in a human colorectal adenocarcinoma cell line. Int. J. Cancer 118, 616-627 (2006).
16. Gupta, S. et al. Binding of ras to phosphoinositide 3-kinase p110alpha is required for ras-driven tumorigenesis in mice. Cell 129, 957-968 (2007).
17. Parent, C. A. & Devreotes, P. N. A cell's sense of direction. Science 284, 765-770 (1999).
18. Ridley, A. J. et al. Cell migration: integrating signals from front to back. Science 302, 1704-1709 (2003).
19. Etienne-Manneville, S. Microtubules in cell migration. Annu. Rev. Cell Dev. Biol. 29, 471-499 (2013).
20. Siegrist, S. E. & Doe, C. Q. Microtubule-induced cortical cell polarity. Genes Dev. 21, 483-496 (2007).
21. Small, J. V. & Kaverina, I. Microtubules meet substrate adhesions to arrange cell polarity. Curr. Opin. Cell Biol. 15, 40-47 (2003).
22. Lara, R. et al. An siRNA screen identifies RSK1 as a key modulator of lung cancer metastasis. Oncogene 30, 3513-3521 (2011).
23. Heasman, S. J. & Ridley, A. J. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690-701 (2008).
24. Raftopoulou, M. & Hall, A. Cell migration: Rho GTPases lead the way. Dev. Biol. 265, 23-32 (2004).
25. Zhao, L. & Vogt, P. K. Hot-spot mutations in p110alpha of phosphatidylinositol 3-kinase (pI3K): differential interactions with the regulatory subunit p85 and with RAS. Cell Cycle 9, 596-600 (2010).
26. D'Arcangelo, G. Apoer2: a reelin receptor to remember. Neuron 47, 471-473 (2005).
27. Niu, S., Renfro, A., Quattrocchi, C. C., Sheldon, M. & D'Arcangelo, G. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2- Dab1 pathway. Neuron 41, 71-84 (2004).
28. Weeber, E. J. et al. Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J. Biol. Chem. 277, 39944-39952 (2002).
29. Sato, N., Fukushima, N., Chang, R., Matsubayashi, H. & Goggins, M. Differential and epigenetic gene expression profiling identifies frequent disruption of the RELN pathway in pancreatic cancers. Gastroenterology 130, 548-565 (2006).
30. Stein, T. et al. Loss of reelin expression in breast cancer is epigenetically controlled and associated with poor prognosis. Am. J. Pathol. 177, 2323-2333 (2010).
31. Dufourny, B., van Teeffelen, H. A., Hamelers, I. H., Sussenbach, J. S. & Steenbergh, P. H. Stabilization of cyclin D1 mRNA via the phosphatidylinositol 3-kinase pathway in MCF-7 human breast cancer cells. J. Endocrinol. 166, 329-338 (2000).
32. Graham, J. R., Hendershott, M. C., Terragni, J. & Cooper, G. M. mRNA degradation plays a significant role in the program of gene expression regulated by phosphatidylinositol 3-kinase signaling. Mol. Cell. Biol. 30, 5295-5305 (2010).
33. Monick, M. M. et al. Phosphatidylinositol 3-kinase activity negatively regulates stability of cyclooxygenase 2 mRNA. J. Biol. Chem. 277, 32992-33000 (2002).
34. D'Arcangelo, G. et al. Reelin is a ligand for lipoprotein receptors. Neuron 24, 471-479 (1999).
35. Rice, D. S. et al. Disabled-1 acts downstream of Reelin in a signaling pathway that controls laminar organization in the mammalian brain. Development 125, 3719-3729 (1998).
36. Trommsdorff, M. et al. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97, 689-701 (1999).
37. Ballif, B. A. et al. Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr. Biol. 14, 606-610 (2004).
38. Franco, S. J., Martinez-Garay, I., Gil-Sanz, C., Harkins-Perry, S. R. & Muller, U. Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex. Neuron 69, 482-497 (2011).
39. Kooistra, M. R., Dube, N. & Bos, J. L. Rap1: a key regulator in cell-cell junction formation. J. Cell Sci. 120, 17-22 (2007).
40. Castellano, E. et al. Requirement for interaction of PI3-kinase p110alpha with RAS in lung tumor maintenance. Cancer Cell 24, 617-630 (2013).
41. Jackson, E. L. et al. The differential effects of mutant p53 alleles on advanced murine lung cancer. Cancer Res. 65, 10280-10288 (2005).
42. Gyorffy, B., Surowiak, P., Budczies, J. & Lanczky, A. Online survival analysis software to assess the prognostic value of biomarkers using transcriptomic data in non-small-cell lung cancer. PloS ONE 8, e82241 (2013).
43. Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature 420, 629-635 (2002).
44. Sahai, E. & Marshall, C. J. RHO-GTPases and cancer. Nat. Rev. Cancer 2, 133-142 (2002).
45. Rodriguez-Viciana, P. et al. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell 89, 457-467 (1997).
46. Daub, H., Gevaert, K., Vandekerckhove, J., Sobel, A. & Hall, A. Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J. Biol. Chem. 276, 1677-1680 (2001).
47. Park, H. & Poo, M. M. Neurotrophin regulation of neural circuit development and function. Nat. Rev. Neurosci. 14, 7-23 (2013).
48. Tiberi, L., Vanderhaeghen, P. & van den Ameele, J. Cortical neurogenesis and morphogens: diversity of cues, sources and functions. Curr. Opin. Cell Biol. 24, 269-276 (2012).
49. Tissir, F. & Goffinet, A. M. Reelin and brain development. Nat. Rev. Neurosci. 4, 496-505 (2003).
50. Garcia-Miranda, P., Peral, M. J. & Ilundain, A. A. Rat small intestine expresses the reelin-Disabled-1 signalling pathway. Exp. Physiol. 95, 498-507 (2010).
51. Smalheiser, N. R. et al. Expression of reelin in adult mammalian blood, liver, pituitary pars intermedia, and adrenal chromaffin cells. Proc. Natl Acad. Sci. USA 97, 1281-1286 (2000).
52. Garcia-Miranda, P., Vazquez-Carretero, M. D., Gutierrez, G., Peral, M. J. & Ilundain, A. A. Lack of reelin modifies the gene expression in the small intestine of mice. J. Physiol. Biochem. 68, 205-218 (2012).
53. Garcia-Miranda, P., Vazquez-Carretero, M. D., Sesma, P., Peral, M. J. & Ilundain, A. A. Reelin is involved in the crypt-villus unit homeostasis. Tissue Eng. Part A 19, 188-198 (2013).
54. Grayson, D. R. et al. The human reelin gene: transcription factors (+), repressors (-) and the methylation switch (+/-) in schizophrenia. Pharmacol. Ther. 111, 272-286 (2006).
55. Noh, J. S. et al. DNA methyltransferase 1 regulates reelin mRNA expression in mouse primary cortical cultures. Proc. Natl Acad. Sci. USA 102, 1749-1754 (2005).
56. Dohi, O. et al. Epigenetic silencing of RELN in gastric cancer. Int. J. Oncol. 36, 85-92 (2010).
57. Evangelisti, C. et al. MiR-128 up-regulation inhibits Reelin and DCX expression and reduces neuroblastoma cell motility and invasiveness. FASEB J. 23, 4276-4287 (2009).
58. Kazlauskas, A. & Cooper, J. A. Autophosphorylation of the PDGF receptor in the kinase insert region regulates interactions with cell proteins. Cell 58, 1121-1133 (1989).
59. Yuan, Y., Chen, H., Ma, G., Cao, X. & Liu, Z. Reelin is involved in transforming growth factor-beta1-induced cell migration in esophageal carcinoma cells. PLoS ONE 7, e31802 (2012).
60. Canel, M., Serrels, A., Frame, M. C. & Brunton, V. G. E-cadherin-integrin crosstalk in cancer invasion and metastasis. J. Cell Sci. 126, 393-401 (2013).
61. Kardash, E. et al. A role for Rho GTPases and cell-cell adhesion in single-cell motility in vivo. Nat. Cell Biol. 12, 47-53 sup 1-11 (2010).
62. Frixen, U. H. et al. E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J. Cell Biol. 113, 173-185 (1991).
63. Castellano, E., De Las Rivas, J., Guerrero, C. & Santos, E. Transcriptional networks of knockout cell lines identify functional specificities of H-Ras and N-Ras: significant involvement of N-Ras in biotic and defense responses. Oncogene 26, 917-933 (2007).
64. Katso, R. M. et al. Phosphoinositide 3-Kinase C2beta regulates cytoskeletal organization and cell migration via Rac-dependent mechanisms. Mol. Biol. Cell 17, 3729-3744 (2006).
65. Gentleman, R. C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).
66. Ginos, M. A. et al. Identification of a gene expression signature associated with recurrent disease in squamous cell carcinoma of the head and neck. Cancer Res. 64, 55-63 (2004).
67. Sanchez-Carbayo, M., Socci, N. D., Lozano, J., Saint, F. & Cordon-Cardo, C. Defining molecular profiles of poor outcome in patients with invasive bladder cancer using oligonucleotide microarrays. J. Clin. Oncol. 24, 778-789 (2006).