RASSF1A Suppresses the Invasion and Metastatic Potential of Human Non-Small Cell Lung Cancer Cells by Inhibiting YAP Activation through the GEF-H1/RhoB Pathway

Cancer Research

Volumn 76, Issue 6, 2016, Pages 1627-1640

  Dubois, Fatéméh ^a,b   Keller, Maureen ^a,b   Calvayrac, Olivier ^c   Soncin, Fabrice ^d   Hoa, Lily ^e   Hergovich, Alexander ^e   Parrini, Maria Carla ^f   Mazières, Julien ^c   Vaisse Lesteven, Mélissa ^a   Camonis, Jacques ^f   Levallet, Guénaëlle ^b   Zalcman, Gérard ^a,g  

^a NORMANDIE UNIVERSITÉ   (France)

^b UNIVERSITÉ DE CAEN   (France)

^c CANCER RESEARCH CENTER OF TOULOUSE   (France)

^d INSTITUT DE BIOLOGIE DE LILLE   (France)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f INSTITUT CURIE   (France)

^g BICHAT HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COFILIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN GEF H1; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN; ARHGEF2 PROTEIN, HUMAN; PHOSPHOPROTEIN; RASSF1 PROTEIN, HUMAN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL ADHESION; CELL TRANSFORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE INACTIVATION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; METASTASIS POTENTIAL; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSGENIC MOUSE; TUMOR GROWTH; TUMOR INVASION; TUMOR XENOGRAFT; DNA METHYLATION; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; METASTASIS; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; TUMOR SUPPRESSOR GENE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CARCINOMA, NON-SMALL-CELL LUNG; DNA METHYLATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, TUMOR SUPPRESSOR; HUMANS; LUNG NEOPLASMS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; RHOB GTP-BINDING PROTEIN; TUMOR SUPPRESSOR PROTEINS;

EID: 84962053998     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-1008     Document Type: Article

References (43)

1. Agathanggelou A, Honorio S, Macartney DP, Martinez A, Dallol A, Rader J, et al. Methylation associated inactivation of RASSF1A from region 3p21.3 in lung, breast and ovarian tumours. Oncogene 2001;20:1509-18.
2. Donninger H, Vos MD, Clark GJ. The RASSF1A tumor suppressor. J Cell Sci 2007;120:3163-72.
3. Dallol A, Agathanggelou A, Tommasi S, Pfeifer GP, Maher ER, Latif F. Involvement of the RASSF1A tumor suppressor gene in controlling cell migration. Cancer Res 2005;65:7653-9.
4. Hergovich A. Mammalian Hippo signalling: A kinase network regulated by protein-protein interactions. Bio chem Soc Trans 2012;40:124-8.
5. Piccolo S, Dupont S, Cordenonsi M. The biology of YAP/TAZ: hippo signaling and beyond. Physiol Rev 2014;94:1287-312.
6. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, et al. Role of YAP/TAZ in mechano transduction. Nature 2011;473:179-83.
7. Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 2008;9:690-701.
8. Vigil D, Cherfils J, Rossman KL, Der CJ. Ras superfamily GEFs and GAPs: validated and tractable targets for cancer therapy? Nat Rev Cancer 2010;10:842-57.
9. Bousquet E, Mazieres J, Privat M, Rizzati V, Casanova A, Ledoux A, et al. Loss of RhoB expression promotes migration and invasion of human bronchial cells via activation of AKT1. Cancer Res 2009;69:6092-9.
10. de Fraipont F, Levallet G, Creveuil C, Bergot E, Beau-Faller M, Mounawar M, et al. Anapoptosis methylation prognostic signature for early lung cancer in the IFCT-0002 trial. Clin Cancer Res 2012;18:2976-86.
11. SatoM, Larsen JE, Lee W, Sun H, Shames DS, Dalvi MP, et al. Human lung epithelial cells progressed to malignancy through specific oncogenic manipulations. Mol Cancer Res 2013;11:638-50.
12. LevalletG, Bergot E, Antoine M, Creveuil C, Santos AO, Beau-Faller M, et al. High TUBB3 expression, an independent prognostic marker in patients with early non-small cell lung cancer treated by preoperative chemotherapy, is regulated by K-Ras signaling pathway. Mol Cancer Ther 2012; 11:1203-13.
13. Bousquet E, Calvayrac O, Mazieres J, Lajoie-Mazenc I, Boubekeur N, Favre G, et al. RhoB loss induces Rac1-dependent mesenchymal cell invasion in lung cells through PP2A inhibition. Oncogene 2015 July 6. doi:10.1038/onc.2015.240. [Epub ahead of print].
14. Calvayrac O, Pradines A, Raymond-Letron I, Rouquette I, Bousquet E, Lauwers-Cances V, et al. RhoB determines tumor aggressiveness in a murine EGFRL858R-induced adenocarcinoma model and is a potential prognostic biomarker for lepidic lung cancer. Clin Cancer Res 2014;20:6541-50.
15. Friedl P, Locker J, Sahai E, Segall JE. Classifying collective cancer cell invasion. Nat Cell Biol 2012;14:777-83.
16. Reznik-Schuller H, Reznik G, Mohr U. Effects of cigarette smoke on the bronchial epithelium of Syrian hamsters: ultrastructural studies. J Natl Cancer Inst 1975;55:353-69.
17. Vos MD, Dallol A, Eckfeld K, Allen NP, Donninger H, Hesson LB, et al. The RASSF1A tumor suppressor activates Bax via MOAP-1. J Biol Chem 2006;281:4557-63.
18. Shao DD, Xue W, Krall EB, Bhutkar A, Piccioni F, Wang X, et al. KRAS and YAP1 converge to regulate EMT and tumor survival. Cell 2014;158:171-84.
19. Polesello C, Huelsmann S, Brown NH, Tapon N. The Drosophila RASSF homolog antagonizes the hippo pathway. Current Biol 2006;16:2459-65.
20. Zhi X, Zhao D, Zhou Z, Liu R, Chen C. YAP promotes breast cell proliferation and survival partially through stabilizing the KLF5 transcription factor. Am J Pathol 2012;180:2452-61.
21. Wang W, Mouneimne G, Sidani M, Wyckoff J, Chen X, Makris A, et al. The activity status of cofilin is directly related to invasion, intravasation, and metastasis of mammary tumors. J Cell Biol 2006;173:395-404.
22. Gohla A, Birkenfeld J, Bokoch GM. Chronophin, a novel HAD-type serine protein phosphatase, regulates cofilin-dependent actin dynamics. Nat Cell Biol 2005;7:21-9.
23. Maekawa M, Ishizaki T, Boku S, Watanabe N, Fujita A, Iwamatsu A, et al. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 1999;285:895-8.
24. Bernard O. Lim kinases, regulators of actin dynamics. Int J Biochem Cell Biol 2007;39:1071-6.
25. Lefranc F, Sauvage S, Van Goietsenoven G, Megalizzi V, Lamoral-Theys D, Debeir O, et al. Narciclasine, a plant growth modulator, activates Rho and stress fibers in glioblastoma cells. Mol Cancer Ther 2009;8:1739-50.
26. Gampel A, Mellor H. Small interfering RNAs as a tool to assign Rho GTPase exchange-factor function in vivo. Biochem J 2002;366:393-8.
27. Kamon H, Kawabe T, Kitamura H, Lee J, Kamimura D, Kaisho T, et al. TRIF-GEFH1-RhoB pathway is involved in MHCII expression on dendritic cells that is critical for CD4 T-cell activation. EMBO J 2006;25: 4108-19.
28. Srougi MC, Burridge K. The nuclear guanine nucleotide exchange factors Ect2 and Net1 regulate RhoB-mediated cell death after DNA damage. PLoS One 2011;6:e17108.
29. Nalbant P, Chang YC, Birkenfeld J, Chang ZF, Bokoch GM. Guanine nucleotide exchange factor-H1 regulates cell migration via localized activation of RhoA at the leading edge. Mol Biol Cell 2009;20: 4070-82.
30. Liu BP, Burridge K. Vav2 activates Rac1, Cdc42, and RhoA downstream from growth factor receptors but not beta1 integrins. Mol Cell Biol 2000;20:7160-9.
31. Fernandez-Borja M, Janssen L, Verwoerd D, Hordijk P, Neefjes J. RhoB regulates endosome transport by promoting actin assembly on endosomal membranes through Dia1. J Cell Sci 2005;118:2661-70.
32. Zalcman G, Closson V, Camonis J, Honore N, Rousseau-Merck MF, Tavitian A, et al. RhoGDI-3 is a new GDP dissociation inhibitor (GDI). Identification of a non-cytosolic GDI protein interacting with the small GTP-binding proteins RhoB and RhoG. J Biol Chem 1996;271:30366-74.
33. Glaven JA, Whitehead IP, Nomanbhoy T, Kay R, Cerione RA. LFC and LSC oncoproteins represent two new guanine nucleotide exchange factors for the Rho GTP-binding protein. J Biol Chem 1996;271:27374-81.
34. Cai H, Xu Y. The role of LPA and YAP signaling in long-term migration of human ovarian cancer cells. Cell Commun Signal 2013;11:31.
35. Lucas EP, Khanal I, Gaspar P, Fletcher GC, Polesello C, Tapon N, et al. The Hippo pathway polarizes the actin cytoskeleton during collective migration of Drosophila border cells. J Cell Biol 2013;201:875-85.
36. Feng X, Degese MS, Iglesias-Bartolome R, Vaque JP, Molinolo AA, Rodrigues M, et al. Hippo-independent activation of YAP by the GNAQ uveal melanoma oncogene through a trio-regulated rho GTPase signaling circuitry. Cancer Cell 2014;25:831-45.
37. Aragona M, Panciera T, Manfrin A, Giulitti S, Michielin F, Elvassore N, et al. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 2013;154:1047-59.
38. Sorrentino G, Ruggeri N, Specchia V, Cordenonsi M, Mano M, Dupont S, et al. Metabolic control of YAP and TAZ by the mevalonate pathway. Nat Cell Biol 2014;16:357-66.
39. Dallol A, Agathanggelou A, Fenton SL, Ahmed-Choudhury J, Hesson L, Vos MD, et al. RASSF1A interacts with microtubule-associated proteins and modulates microtubule dynamics. Cancer Res 2004;64:4112-6.
40. Tsapara A, Luthert P, Greenwood J, Hill CS, Matter K, Balda MS. The RhoA activator GEF-H1/Lfc is a transforming growth factor-beta target gene and effector that regulates alpha-smooth muscle actin expression and cell migration. Mol Biol Cell 2010;21:860-70.
41. Vega FM, Fruhwirth G, Ng T, Ridley AJ. RhoA and RhoC have distinct roles in migration and invasion by acting through different targets. J Cell Biol 2011;193:655-65.
42. Zenke FT, Krendel M, DerMardirossian C, King CC, Bohl BP, Bokoch GM. p21-activated kinase 1 phosphorylates and regulates 14-3-3 binding to GEF-H1, a microtubule-localized Rho exchange factor. J Biol Chem 2004; 279:18392-400.
43. Yu F-X, Zhao B, Panupinthu N, Jewell J, Lian I, Wang L, et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 2012;150:780-91.