RAS and RHO family GTPase mutations in cancer: twin sons of different mothers?

References

• Abraham MT, Kuriakose MA, Sacks PG, Yee H, Chiriboga L, Bearer EL, Delacure MD. 2001. Motility-related proteins as markers for head and neck squamous cell cancer. Laryngoscope. 111(7):1285–1289.
   PubMed Web of Science ®Google Scholar
• Adamson P, Marshall CJ, Hall A, Tilbrook PA. 1992. Post-translational modifications of p21rho proteins. J Biol Chem. 267(28):20033–20038.
   PubMed Web of Science ®Google Scholar
• Amano M, Mukai H, Ono Y, Chihara K, Matsui T, Hamajima Y, Okawa K, Iwamatsu A, Kaibuchi K. 1996. Identification of a putative target for Rho as the serine-threonine kinase protein kinase N. Science. 271(5249):648–650.
   PubMed Web of Science ®Google Scholar
• Avraham H, Weinberg R. 1989. Characterization and expression of the human rhoH12 gene product. Mol Cell Biol. 9(5):2058–2066.
   PubMed Web of Science ®Google Scholar
• Bazarbachi A, Suarez F, Fields P, Hermine O. 2011. How I treat adult T-cell leukemia/lymphoma. Blood. 118(7):1736–1745.
   PubMed Web of Science ®Google Scholar
• Berzat AC, Buss JE, Chenette EJ, Weinbaum CA, Shutes A, Der CJ, Minden A, Cox AD. 2005. Transforming activity of the Rho family GTPase, Wrch-1, a Wnt-regulated Cdc42 homolog, is dependent on a novel carboxyl-terminal palmitoylation motif. J Biol Chem. 280(38):33055–33065.
   PubMed Web of Science ®Google Scholar
• Bos JL, Rehmann H, Wittinghofer A. 2007. GEFs and GAPs: critical elements in the control of small G proteins. Cell. 129(5):865–877.
   PubMed Web of Science ®Google Scholar
• Botton T, Talevich E, Mishra VK, Zhang T, Shain AH, Berquet C, Gagnon A, Judson RL, Ballotti R, Ribas A, et al. 2019. Genetic heterogeneity of BRAF fusion kinases in melanoma affects drug responses. Cell Rep. 29(3):573–588.e577.
   PubMed Web of Science ®Google Scholar
• Bourne HR, Sanders DA, McCormick F. 1990. The GTPase superfamily: a conserved switch for diverse cell functions. Nature. 348(6297):125–132.
   PubMed Web of Science ®Google Scholar
• Bourne HR, Sanders DA, McCormick F. 1991. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 349(6305):117–127.
   PubMed Web of Science ®Google Scholar
• Cairns R, Iqbal J, Lemonnier F, Kucuk C, de Leval L, Jais J-P, Parrens M, Martin A, Xerri L, Brousset P, et al. 2012. IDH2 mutations are frequent in angioimmunoblastic T-cell lymphoma. Blood. 119(8):1901–1903.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research N. 2014. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 513:202–209.
   PubMed Web of Science ®Google Scholar
• Casey PJ, Solski PA, Der CJ, Buss JE. 1989. p21ras is modified by a farnesyl isoprenoid. Proc Natl Acad Sci USA. 86(21):8323–8327.
   PubMed Web of Science ®Google Scholar
• Chandra A, Grecco HE, Pisupati V, Perera D, Cassidy L, Skoulidis F, Ismail SA, Hedberg C, Hanzal-Bayer M, Venkitaraman AR, et al. 2011. The GDI-like solubilizing factor PDEdelta sustains the spatial organization and signalling of Ras family proteins. Nat Cell Biol. 14(2):148–158.
   PubMed Web of Science ®Google Scholar
• Chen SY, Huff SY, Lai CC, Der CJ, Powers S. 1994. Ras-15A protein shares highly similar dominant-negative biological properties with Ras-17N and forms a stable, guanine-nucleotide resistant complex with CDC25 exchange factor. Oncogene. 9(9):2691–2698.
   PubMed Web of Science ®Google Scholar
• Chen B, Xu M, Xu M. 2019. Upregulation of DLC-1 inhibits pancreatic cancer progression: Studies with clinical samples and a pancreatic cancer model. Oncol Lett. 18:5600–5606.
   PubMed Web of Science ®Google Scholar
• Chenette EJ, Abo A, Der CJ. 2005. Critical and distinct roles of amino- and carboxyl-terminal sequences in regulation of the biological activity of the Chp atypical Rho GTPase. J Biol Chem. 280(14):13784–13792.
   PubMed Web of Science ®Google Scholar
• Cherfils J, Zeghouf M. 2013. Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol Rev. 93(1):269–309.
   PubMed Web of Science ®Google Scholar
• Chmielecki J, Hutchinson KE, Frampton GM, Chalmers ZR, Johnson A, Shi C, Elvin J, Ali SM, Ross JS, Basturk O, et al. 2014. Comprehensive genomic profiling of pancreatic acinar cell carcinomas identifies recurrent RAF fusions and frequent inactivation of DNA repair genes. Cancer Discov. 4(12):1398–1405.
   PubMed Web of Science ®Google Scholar
• Cho HJ, Baek KE, Park SM, Kim IK, Choi YL, Cho HJ, Nam IK, Hwang EM, Park JY, Han JY, et al. 2009. RhoGDI2 expression is associated with tumor growth and malignant progression of gastric cancer. Clin Cancer Res. 15(8):2612–2619.
   PubMed Web of Science ®Google Scholar
• Cook DR, Rossman KL, Der CJ. 2014. Rho guanine nucleotide exchange factors: regulators of Rho GTPase activity in development and disease. Oncogene. 33(31):4021–4035.
   PubMed Web of Science ®Google Scholar
• Cortes J, Ambesi-Impiombato A, Couronne L, Quinn S, Kim C, da Silva Almeida A, West Z, Belver L, Martin M, Scourzic L, et al. 2018. RHOA G17V induces T follicular helper cell specification and promotes lymphomagenesis. Cancer Cell. 33(2):259–273.
   PubMed Web of Science ®Google Scholar
• Cox AD, Fesik SW, Kimmelman AC, Luo J, Der CJ. 2014. Drugging the undruggable RAS: mission possible? Nat Rev Drug Discov. 13(11):828–851.
   PubMed Web of Science ®Google Scholar
• Dave SS, Fu K, Wright GW, Lam LT, Kluin P, Boerma E-J, Greiner TC, Weisenburger DD, Rosenwald A, Ott G, et al. 2006. Molecular diagnosis of Burkitt’s lymphoma. N Engl J Med. 354(23):2431–2442.
   PubMed Web of Science ®Google Scholar
• Davis MJ, Ha BH, Holman EC, Halaban R, Schlessinger J, Boggon TJ. 2013. RAC1P29S is a spontaneously activating cancer-associated GTPase. Proc Natl Acad Sci USA. 110(3):912–917.
   PubMed Web of Science ®Google Scholar
• Der CJ, Finkel T, Cooper GM. 1986. Biological and biochemical properties of human rasH genes mutated at codon 61. Cell. 44(1):167–176.
   PubMed Web of Science ®Google Scholar
• Der CJ, Krontiris TG, Cooper GM. 1982. Transforming genes of human bladder and lung carcinoma cell lines are homologous to the ras genes of Harvey and Kirsten sarcoma viruses. Proc Natl Acad Sci USA. 79(11):3637–3640.
   PubMed Web of Science ®Google Scholar
• Derewenda U, Oleksy A, Stevenson AS, Korczynska J, Dauter Z, Somlyo AP, Otlewski J, Somlyo AV, Derewenda ZS. 2004. The crystal structure of RhoA in complex with the DH/PH fragment of PDZRhoGEF, an activator of the Ca2+ sensitization pathway in smooth muscle. Structure. 12(11):1955–1965.
   PubMed Web of Science ®Google Scholar
• Dharmaiah S, Bindu L, Tran TH, Gillette WK, Frank PH, Ghirlando R, Nissley DV, Esposito D, McCormick F, Stephen AG, et al. 2016. Structural basis of recognition of farnesylated and methylated KRAS4b by PDEdelta. Proc Natl Acad Sci USA. 113(44):E6766–E6775.
   PubMed Web of Science ®Google Scholar
• Doody GM, Bell SE, Vigorito E, Clayton E, McAdam S, Tooze R, Fernandez C, Lee IJ, Turner M. 2001. Signal transduction through Vav-2 participates in humoral immune responses and B cell maturation. Nat Immunol. 2(6):542–547.
   PubMed Web of Science ®Google Scholar
• Feig LA, Cooper GM. 1988. Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol Cell Biol. 8(8):3235–3243.
   PubMed Web of Science ®Google Scholar
• Franchini G. 1995. Molecular mechanisms of human T-cell leukemia/lymphotropic virus type I infection. Blood. 86(10):3619–3639.
   PubMed Web of Science ®Google Scholar
• Fritz G, Brachetti C, Bahlmann F, Schmidt M, Kaina B. 2002. Rho GTPases in human breast tumours: expression and mutation analyses and correlation with clinical parameters. Br J Cancer. 87(6):635–644.
   PubMed Web of Science ®Google Scholar
• Fritz G, Just I, Kaina B. 1999. Rho GTPases are over-expressed in human tumors. Int J Cancer. 81(5):682–687.
   PubMed Web of Science ®Google Scholar
• Fujisawa M, Sakata-Yanagimoto M, Nishizawa S, Komori D, Gershon P, Kiryu M, Tanzima S, Fukumoto K, Enami T, Muratani M, et al. 2018. Activation of RHOA-VAV1 signaling in angioimmunoblastic T-cell lymphoma. Leukemia. 32(3):694–702.
   PubMed Web of Science ®Google Scholar
• Gadea G, Blangy A. 2014. Dock-family exchange factors in cell migration and disease. Eur J Cell Biol. 93(10–12):466–477.
   PubMed Web of Science ®Google Scholar
• Garcia-Mata R, Boulter E, Burridge K. 2011. The ‘invisible hand’: regulation of RHO GTPases by RHOGDIs. Nat Rev Mol Cell Biol. 12(8):493–504.
   PubMed Web of Science ®Google Scholar
• Gildea JJ, Seraj MJ, Oxford G, Harding MA, Hampton GM, Moskaluk CA, Frierson HF, Conaway MR, Theodorescu D. 2002. RhoGDI2 is an invasion and metastasis suppressor gene in human cancer. Cancer Res. 62(22):6418–6423.
   PubMed Web of Science ®Google Scholar
• Hall A, Marshall CJ, Spurr NK, Weiss RA. 1983. Identification of transforming gene in two human sarcoma cell lines as a new member of the ras gene family located on chromosome 1. Nature. 303(5916):396–400.
   PubMed Web of Science ®Google Scholar
• Hancock JF, Magee AI, Childs JE, Marshall CJ. 1989. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell. 57(7):1167–1177.
   PubMed Web of Science ®Google Scholar
• Hart M, Maru Y, Leonard D, Witte O, Evans T, Cerione R. 1992. A GDP dissociation inhibitor that serves as a GTPase inhibitor for the Ras-like protein CDC42Hs. Science. 258(5083):812–815.
   PubMed Web of Science ®Google Scholar
• Harvey JJ. 1964. An unidentified virus which causes the rapid production of tumours in mice. Nature. 204:1104–1105.
   PubMed Web of Science ®Google Scholar
• Hirshberg M, Stockley RW, Dodson G, Webb MR. 1997. The crystal structure of human rac1, a member of the rho-family complexed with a GTP analogue. Nat Struct Biol. 4(2):147–152.
   PubMedGoogle Scholar
• Hodge RG, Ridley AJ. 2016. Regulating Rho GTPases and their regulators. Nat Rev Mol Cell Biol. 17(8):496–510.
   PubMed Web of Science ®Google Scholar
• Hodis E, Watson IR, Kryukov GV, Arold ST, Imielinski M, Theurillat JP, Nickerson E, Auclair D, Li L, Place C, et al. 2012. A landscape of driver mutations in melanoma. Cell. 150(2):251–263.
   PubMed Web of Science ®Google Scholar
• Hoffman GR, Nassar N, Cerione RA. 2000. Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell. 100(3):345–356.
   PubMed Web of Science ®Google Scholar
• Huff LP, Decristo MJ, Trembath D, Kuan PF, Yim M, Liu J, Cook DR, Miller CR, Der CJ, Cox AD. 2013. The role of Ect2 nuclear RhoGEF activity in ovarian cancer cell transformation. Genes Cancer. 4(11–12):460–475.
   PubMedGoogle Scholar
• Hummel M, Bentink S, Berger H, Klapper W, Wessendorf S, Barth TFE, Bernd H-W, Cogliatti SB, Dierlamm J, Feller AC, et al. 2006. A biologic definition of Burkitt’s lymphoma from transcriptional and genomic profiling. N Engl J Med. 354(23):2419–2430.
   PubMed Web of Science ®Google Scholar
• Ihara K, Muraguchi S, Kato M, Shimizu T, Shirakawa M, Kuroda S, Kaibuchi K, Hakoshima T. 1998. Crystal structure of human RhoA in a dominantly active form complexed with a GTP analogue. J Biol Chem. 273(16):9656–9666.
   PubMed Web of Science ®Google Scholar
• Ishizaki T, Maekawa M, Fujisawa K, Okawa K, Iwamatsu A, Fujita A, Watanabe N, Saito Y, Kakizuka A, Morii N, et al. 1996. The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. Embo J. 15(8):1885–1893.
   PubMed Web of Science ®Google Scholar
• Joneson T, McDonough M, Bar-Sagi D, Van Aelst L. 1996. RAC regulation of actin polymerization and proliferation by a pathway distinct from Jun Kinase. Science. 274(5291):1374–1376.
   PubMed Web of Science ®Google Scholar
• Justilien V, Ali SA, Jamieson L, Yin N, Cox AD, Der CJ, Murray NR, Fields AP. 2017. Ect2-dependent rRNA synthesis is required for KRAS-TRP53-driven lung adenocarcinoma. Cancer Cell. 31(2):256–269.
   PubMed Web of Science ®Google Scholar
• Kakiuchi M, Nishizawa T, Ueda H, Gotoh K, Tanaka A, Hayashi A, Yamamoto S, Tatsuno K, Katoh H, Watanabe Y, et al. 2014. Recurrent gain-of-function mutations of RHOA in diffuse-type gastric carcinoma. Nat Genet. 46(6):583–587.
   PubMed Web of Science ®Google Scholar
• Kamai T, Yamanishi T, Shirataki H, Takagi K, Asami H, Ito Y, Yoshida K. 2004. Overexpression of RhoA, Rac1, and Cdc42 GTPases is associated with progression in testicular cancer. Clin Cancer Res. 10(14):4799–4805.
   PubMed Web of Science ®Google Scholar
• Katayama M, Kawata M, Yoshida Y, Horiuchi H, Yamamoto T, Matsuura Y, Takai Y. 1991. The posttranslationally modified C-terminal structure of bovine aortic smooth muscle rhoA p21. J Biol Chem. 266(19):12639–12645.
   PubMed Web of Science ®Google Scholar
• Khosravi-Far R, White MA, Westwick JK, Solski PA, Chrzanowska-Wodnicka M, Van Aelst L, Wigler MH, Der CJ. 1996. Oncogenic Ras activation of Raf/mitogen-activated protein kinase-independent pathways is sufficient to cause tumorigenic transformation. Mol Cell Biol. 16(7):3923–3933.
   PubMed Web of Science ®Google Scholar
• Kirsten WH, Mayer LA. 1967. Morphologic responses to a murine erythroblastosis virus. J Natl Cancer Inst. 39(2):311–335.
   PubMedGoogle Scholar
• Krauthammer M, Kong Y, Ha BH, Evans P, Bacchiocchi A, McCusker JP, Cheng E, Davis MJ, Goh G, Choi M, et al. 2012. Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat Genet. 44(9):1006–1014.
   PubMed Web of Science ®Google Scholar
• Kristelly R, Gao G, Tesmer JJ. 2004. Structural determinants of RhoA binding and nucleotide exchange in leukemia-associated Rho guanine-nucleotide exchange factor. J Biol Chem. 279(45):47352–47362.
   PubMed Web of Science ®Google Scholar
• Kuhne MR, Ku G, Weiss A. 2000. A guanine nucleotide exchange factor-independent function of Vav1 in transcriptional activation. J Biol Chem. 275(3):2185–2190.
   PubMed Web of Science ®Google Scholar
• Lamarche N, Tapon N, Stowers L, Burbelo PD, Aspenstrom P, Bridges T, Chant J, Hall A. 1996. Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell. 87(3):519–529.
   PubMed Web of Science ®Google Scholar
• Lammers M, Meyer S, Kuhlmann D, Wittinghofer A. 2008. Specificity of interactions between mDia isoforms and Rho proteins. J Biol Chem. 283(50):35236–35246.
   PubMed Web of Science ®Google Scholar
• Lawson CD, Ridley AJ. 2018. Rho GTPase signaling complexes in cell migration and invasion. J Cell Biol. 217(2):447–457.
   PubMed Web of Science ®Google Scholar
• Leconte J, Bagherzadeh Yazdchi S, Panneton V, Suh W-K. 2016. Inducible costimulator (ICOS) potentiates TCR-induced calcium flux by augmenting PLCγ1 activation and actin remodeling. Mol Immunol. 79:38–46.
   PubMed Web of Science ®Google Scholar
• Lemonnier F, Couronné L, Parrens M, Jaïs J-P, Travert M, Lamant L, Tournillac O, Rousset T, Fabiani B, Cairns RA, et al. 2012. Recurrent TET2 mutations in peripheral T-cell lymphomas correlate with TFH-like features and adverse clinical parameters. Blood. 120(7):1466–1469.
   PubMed Web of Science ®Google Scholar
• Leonard D, Hart MJ, Platko JV, Eva A, Henzel W, Evans T, Cerione RA. 1992. The identification and characterization of a GDP-dissociation inhibitor (GDI) for the CDC42Hs protein. J Biol Chem. 267(32):22860–22868.
   PubMed Web of Science ®Google Scholar
• Leung T, Manser E, Tan L, Lim L. 1995. A novel serine/threonine kinase binding the Ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J Biol Chem. 270(49):29051–29054.
   PubMed Web of Science ®Google Scholar
• Lim Y, Lim ST, Tomar A, Gardel M, Bernard-Trifilo JA, Chen XL, Uryu SA, Canete-Soler R, Zhai J, Lin H, et al. 2008. PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J Cell Biol. 180(1):187–203.
   PubMed Web of Science ®Google Scholar
• Lunning MA, Vose JM. 2017. Angioimmunoblastic T-cell lymphoma: the many-faced lymphoma. Blood. 129(9):1095–1102.
   PubMed Web of Science ®Google Scholar
• Madaule P, Axel R. 1985. A novel ras-related gene family. Cell. 41(1):31–40.
   PubMed Web of Science ®Google Scholar
• Matsui T, Amano M, Yamamoto T, Chihara K, Nakafuku M, Ito M, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K. 1996. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. Embo J. 15(9):2208–2216.
   PubMed Web of Science ®Google Scholar
• Miki T, Smith CL, Long JE, Eva A, Fleming TP. 1993. Oncogene ect2 is related to regulators of small GTP-binding proteins. Nature. 362(6419):462–465.
   PubMed Web of Science ®Google Scholar
• Molyneux EM, Rochford R, Griffin B, Newton R, Jackson G, Menon G, Harrison CJ, Israels T, Bailey S. 2012. Burkitt’s lymphoma. The Lancet. 379(9822):1234–1244.
   PubMed Web of Science ®Google Scholar
• Moskowitz AJ, Lunning MA, Horwitz SM. 2014. How I treat the peripheral T-cell lymphomas. Blood. 123(17):2636–2644.
   PubMed Web of Science ®Google Scholar
• Mott HR, Owen D. 2015. Structures of Ras superfamily effector complexes: what have we learnt in two decades? Crit Rev Biochem Mol Biol. 50(2):85–133.
   PubMed Web of Science ®Google Scholar
• Nagata Y, Kontani K, Enami T, Kataoka K, Ishii R, Totoki Y, Kataoka TR, Hirata M, Aoki K, Nakano K, et al. 2016. Variegated RHOA mutations in adult T-cell leukemia/lymphoma. Blood. 127(5):596–604.
   PubMed Web of Science ®Google Scholar
• Narumiya S, Thumkeo D. 2018. Rho signaling research: history, current status and future directions. FEBS Lett. 592(11):1763–1776.
   PubMed Web of Science ®Google Scholar
• Nimnual AS, Yatsula BA, Bar-Sagi D. 1998. Coupling of Ras and Rac guanosine triphosphatases through the Ras exchanger Sos. Science. 279(5350):560–563.
   PubMed Web of Science ®Google Scholar
• Pai EF, Krengel U, Petsko GA, Goody RS, Kabsch W, Wittinghofer A. 1990. Refined crystal structure of the triphosphate conformation of H-ras p21 at 1.35 A resolution: implications for the mechanism of GTP hydrolysis. Embo J. 9(8):2351–2359.
   PubMed Web of Science ®Google Scholar
• Palomero T, Couronne L, Khiabanian H, Kim MY, Ambesi-Impiombato A, Perez-Garcia A, Carpenter Z, Abate F, Allegretta M, Haydu JE, et al. 2014. Recurrent mutations in epigenetic regulators, RHOA and FYN kinase in peripheral T cell lymphomas. Nat Genet. 46(2):166–170.
   PubMed Web of Science ®Google Scholar
• Parada LF, Tabin CJ, Shih C, Weinberg RA. 1982. Human EJ bladder carcinoma oncogene is homologue of Harvey sarcoma virus ras gene. Nature. 297(5866):474–478.
   PubMed Web of Science ®Google Scholar
• Paterson HF, Self AJ, Garrett MD, Just I, Aktories K, Hall A. 1990. Microinjection of recombinant p21rho induces rapid changes in cell morphology. J Cell Biol. 111(3):1001–1007.
   PubMed Web of Science ®Google Scholar
• Poulin EJ, Bera AK, Lu J, Lin YJ, Strasser SD, Paulo JA, Huang TQ, Morales C, Yan W, Cook J, et al. 2019. Tissue-specific oncogenic activity of KRAS(A146T). Cancer Discov. 9(6):738–755.
   PubMed Web of Science ®Google Scholar
• Powers S, O'Neill K, Wigler M. 1989. Dominant yeast and mammalian RAS mutants that interfere with the CDC25-dependent activation of wild-type RAS in Saccharomyces cerevisiae. Mol Cell Biol. 9(2):390–395.
   PubMed Web of Science ®Google Scholar
• Prior IA, Hood FE, Hartley JL. 2020. The frequency of ras mutations in cancer. Cancer Res. 80(14):2969–2974.
   PubMed Web of Science ®Google Scholar
• Qian X, Durkin ME, Wang D, Tripathi BK, Olson L, Yang XY, Vass WC, Popescu NC, Lowy DR. 2012. Inactivation of the Dlc1 gene cooperates with downregulation of p15INK4b and p16Ink4a, leading to neoplastic transformation and poor prognosis in human cancer. Cancer Res. 72(22):5900–5911.
   PubMed Web of Science ®Google Scholar
• Qiu RG, Chen J, Kirn D, McCormick F, Symons M. 1995. An essential role for Rac in Ras transformation. Nature. 374(6521):457–459.
   PubMed Web of Science ®Google Scholar
• Qiu RG, Chen J, McCormick F, Symons M. 1995. A role for Rho in Ras transformation. Proc Natl Acad Sci USA. 92(25):11781–11785.
   PubMed Web of Science ®Google Scholar
• Reid T, Furuyashiki T, Ishizaki T, Watanabe G, Watanabe N, Fujisawa K, Morii N, Madaule P, Narumiya S. 1996. Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rho-binding domain. J Biol Chem. 271(23):13556–13560.
   PubMed Web of Science ®Google Scholar
• Reid TS, Terry KL, Casey PJ, Beese LS. 2004. Crystallographic analysis of CaaX prenyltransferases complexed with substrates defines rules of protein substrate selectivity. J Mol Biol. 343(2):417–433.
   PubMed Web of Science ®Google Scholar
• Ridley AJ, Hall A. 1992. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70(3):389–399.
   PubMed Web of Science ®Google Scholar
• Rittinger K, Walker PA, Eccleston JF, Smerdon SJ, Gamblin SJ. 1997. Structure at 1.65 Å of RhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature. 389(6652):758–762.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Viciana P, Warne PH, Khwaja A, Marte BM, Pappin D, Das P, Waterfield MD, Ridley AJ, Downward J. 1997. Role of phosphoinositide 3-OH Kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell. 89(3):457–467.
   PubMed Web of Science ®Google Scholar
• Rohde M, Richter J, Schlesner M, Betts MJ, Claviez A, Bonn BR, Zimmermann M, Damm-Welk C, Russell RB, Borkhardt A, et al. 2014. Recurrent RHOA mutations in pediatric Burkitt lymphoma treated according to the NHL-BFM protocols. Genes Chromosomes Cancer. 53(11):911–916.
   PubMed Web of Science ®Google Scholar
• Rose R, Weyand M, Lammers M, Ishizaki T, Ahmadian MR, Wittinghofer A. 2005. Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature. 435(7041):513–518.
   PubMed Web of Science ®Google Scholar
• Sahai E, Alberts AS, Treisman R. 1998. RhoA effector mutants reveal distinct effector pathways for cytoskeletal reorganization, SRF activation and transformation. Embo J. 17(5):1350–1361.
   PubMed Web of Science ®Google Scholar
• Sakata-Yanagimoto M, Enami T, Yoshida K, Shiraishi Y, Ishii R, Miyake Y, Muto H, Tsuyama N, Sato-Otsubo A, Okuno Y, et al. 2014. Somatic RHOA mutation in angioimmunoblastic T cell lymphoma. Nat Genet. 46(2):171–175.
   PubMed Web of Science ®Google Scholar
• Santos E, Tronick SR, Aaronson SA, Pulciani S, Barbacid M. 1982. T24 human bladder carcinoma oncogene is an activated form of the normal human homologue of BALB- and Harvey-MSV transforming genes. Nature. 298(5872):343–347.
   PubMed Web of Science ®Google Scholar
• Saraste M, Sibbald PR, Wittinghofer A. 1990. The P-loop–a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci. 15(11):430–434.
   PubMed Web of Science ®Google Scholar
• Schafer WR, Kim R, Sterne R, Thorner J, Kim SH, Rine J. 1989. Genetic and pharmacological suppression of oncogenic mutations in ras genes of yeast and humans. Science. 245(4916):379–385.
   PubMed Web of Science ®Google Scholar
• Schunke D, Span P, Ronneburg H, Dittmer A, Vetter M, Holzhausen HJ, Kantelhardt E, Krenkel S, Muller V, Sweep FC, et al. 2007. Cyclooxygenase-2 is a target gene of rho GDP dissociation inhibitor beta in breast cancer cells. Cancer Res. 67(22):10694–10702.
   PubMed Web of Science ®Google Scholar
• Scolnick EM, Parks WP. 1974. Harvey sarcoma virus: a second murine type C sarcoma virus with rat genetic information. J Virol. 13(6):1211–1219.
   PubMed Web of Science ®Google Scholar
• Scolnick EM, Rands E, Williams D, Parks WP. 1973. Studies on the nucleic acid sequences of Kirsten sarcoma virus: a model for formation of a mammalian RNA-containing sarcoma virus. J Virol. 12(3):458–463.
   PubMed Web of Science ®Google Scholar
• Seeburg PH, Colby WW, Capon DJ, Goeddel DV, Levinson AD. 1984. Biological properties of human c-Ha-ras1 genes mutated at codon 12. Nature. 312(5989):71–75.
   PubMed Web of Science ®Google Scholar
• Shimizu K, Goldfarb M, Perucho M, Wigler M. 1983. Isolation and preliminary characterization of the transforming gene of a human neuroblastoma cell line. Proc Natl Acad Sci USA. 80(2):383–387.
   PubMed Web of Science ®Google Scholar
• Sigal IS, Gibbs JB, D’Alonzo JS, Scolnick EM. 1986. Identification of effector residues and a neutralizing epitope of Ha-ras-encoded p21. Proc Natl Acad Sci USA. 83(13):4725–4729.
   PubMed Web of Science ®Google Scholar
• Sigal IS, Gibbs JB, D’Alonzo JS, Temeles GL, Wolanski BS, Socher SH, Scolnick EM. 1986. Mutant ras-encoded proteins with altered nucleotide binding exert dominant biological effects. Proc Natl Acad Sci USA. 83(4):952–956.
   PubMed Web of Science ®Google Scholar
• Snyder JT, Worthylake DK, Rossman KL, Betts L, Pruitt WM, Siderovski DP, Der CJ, Sondek J. 2002. Structural basis for the selective activation of Rho GTPases by Dbl exchange factors. Nat Struct Biol. 9(6):468–475.
   PubMedGoogle Scholar
• Srivastava SK, Wheelock RH, Aaronson SA, Eva A. 1986. Identification of the protein encoded by the human diffuse B-cell lymphoma (dbl) oncogene. Proc Natl Acad Sci USA. 83(23):8868–8872.
   PubMed Web of Science ®Google Scholar
• Stevens EV, Banet N, Onesto C, Plachco A, Alan JK, Nikolaishvili-Feinberg N, Midkiff BR, Kuan PF, Liu J, Miller CR, et al. 2011. RhoGDI2 antagonizes ovarian carcinoma growth, invasion and metastasis. Small GTPases. 2(4):202–210.
   PubMedGoogle Scholar
• Stone JC. 2011. Regulation and function of the RasGRP family of Ras activators in blood cells. Genes Cancer. 2(3):320–334.
   PubMedGoogle Scholar
• Stransky N, Egloff AM, Tward AD, Kostic AD, Cibulskis K, Sivachenko A, Kryukov GV, Lawrence MS, Sougnez C, McKenna A, et al. 2011. The mutational landscape of head and neck squamous cell carcinoma. Science. 333(6046):1157–1160.
   PubMed Web of Science ®Google Scholar
• Tanaka A, Ishikawa S, Ushiku T, Yamazawa S, Katoh H, Hayashi A, Kunita A, Fukayama M. 2018. Frequent CLDN18-ARHGAP fusion in highly metastatic diffuse-type gastric cancer with relatively early onset. Oncotarget. 9(50):29336–29350.
   PubMedGoogle Scholar
• Tcherkezian J, Lamarche-Vane N. 2007. Current knowledge of the large RhoGAP family of proteins. Biol Cell. 99(2):67–86.
   PubMed Web of Science ®Google Scholar
• Tedford K, Nitschke L, Girkontaite I, Charlesworth A, Chan G, Sakk V, Barbacid M, Fischer KD. 2001. Compensation between Vav-1 and Vav-2 in B cell development and antigen receptor signaling. Nat Immunol. 2(6):548–555.
   PubMed Web of Science ®Google Scholar
• Theodorescu D, Sapinoso LM, Conaway MR, Oxford G, Hampton GM, Frierson HF. Jr. 2004. Reduced expression of metastasis suppressor RhoGDI2 is associated with decreased survival for patients with bladder cancer. Clin Cancer Res. 10(11):3800–3806.
   PubMed Web of Science ®Google Scholar
• Tomino T, Tajiri H, Tatsuguchi T, Shirai T, Oisaki K, Matsunaga S, Sanematsu F, Sakata D, Yoshizumi T, Maehara Y, et al. 2018. DOCK1 inhibition suppresses cancer cell invasion and macropinocytosis induced by self-activating Rac1(P29S) mutation. Biochem Biophys Res Commun. 497(1):298–304.
   PubMed Web of Science ®Google Scholar
• Ueda T, Kikuchi A, Ohga N, Yamamoto J, Takai Y. 1990. Purification and characterization from bovine brain cytosol of a novel regulatory protein inhibiting the dissociation of GDP from and the subsequent binding of GTP to rhoB p20, a ras p21-like GTP-binding protein. J Biol Chem. 265(16):9373–9380.
   PubMed Web of Science ®Google Scholar
• Vallois D, Dobay MPD, Morin RD, Lemonnier F, Missiaglia E, Juilland M, Iwaszkiewicz J, Fataccioli V, Bisig B, Roberti A, et al. 2016. Activating mutations in genes related to TCR signaling in angioimmunoblastic and other follicular helper T-cell–derived lymphomas. Blood. 128(11):1490–1502.
   PubMed Web of Science ®Google Scholar
• Vigil D, Cherfils J, Rossman KL, Der CJ. 2010. Ras superfamily GEFs and GAPs: validated and tractable targets for cancer therapy? Nat Rev Cancer. 10(12):842–857.
   PubMed Web of Science ®Google Scholar
• Wang K, Yuen ST, Xu J, Lee SP, Yan HH, Shi ST, Siu HC, Deng S, Chu KM, Law S, et al. 2014. Whole-genome sequencing and comprehensive molecular profiling identify new driver mutations in gastric cancer. Nat Genet. 46(6):573–582.
   PubMed Web of Science ®Google Scholar
• Warner H, Wilson BJ, Caswell PT. 2019. Control of adhesion and protrusion in cell migration by Rho GTPases. Curr Opin Cell Biol. 56:64–70.
   PubMed Web of Science ®Google Scholar
• Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S. 1997. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. Embo J. 16(11):3044–3056.
   PubMed Web of Science ®Google Scholar
• Watanabe G, Saito Y, Madaule P, Ishizaki T, Fujisawa K, Morii N, Mukai H, Ono Y, Kakizuka A, Narumiya S. 1996. Protein kinase N (PKN) and PKN-related protein rhophilin as targets of small GTPase Rho. Science. 271(5249):645–648.
   PubMed Web of Science ®Google Scholar
• Wennerberg K, Rossman KL, Der CJ. 2005. The Ras superfamily at a glance. J Cell Sci. 118(5):843–846.
   PubMed Web of Science ®Google Scholar
• Westwick JK, Lambert QT, Clark GJ, Symons M, Van Aelst L, Pestell RG, Der CJ. 1997. Rac regulation of transformation, gene expression, and actin organization by multiple, PAK-independent pathways. Mol Cell Biol. 17(3):1324–1335.
   PubMed Web of Science ®Google Scholar
• White MA, Nicolette C, Minden A, Polverino A, Van Aelst L, Karin M, Wigler MH. 1995. Multiple Ras functions can contribute to mammalian cell transformation. Cell. 80(4):533–541.
   PubMed Web of Science ®Google Scholar
• Wittinghofer A, Vetter IR. 2011. Structure-function relationships of the G domain, a canonical switch motif. Annu Rev Biochem. 80(1):943–971.
   PubMedGoogle Scholar
• Worthylake DK, Rossman KL, Sondek J. 2000. Crystal structure of Rac1 in complex with the guanine nucleotide exchange region of Tiam1. Nature. 408(6813):682–688.
   PubMed Web of Science ®Google Scholar
• Yao F, Kausalya JP, Sia YY, Teo AS, Lee WH, Ong AG, Zhang Z, Tan JH, Li G, Bertrand D, et al. 2015. Recurrent fusion genes in gastric cancer: CLDN18-ARHGAP26 induces loss of epithelial integrity. Cell Rep. 12(2):272–285.
   PubMed Web of Science ®Google Scholar
• Yeramian P, Chardin P, Madaule P, Tavitian A. 1987. Nucleotide sequence of human rho cDNA clone 12. Nucleic Acids Res. 15(4):1869.
   PubMed Web of Science ®Google Scholar
• Yoo HY, Sung MK, Lee SH, Kim S, Lee H, Park S, Kim SC, Lee B, Rho K, Lee JE, et al. 2014. A recurrent inactivating mutation in RHOA GTPase in angioimmunoblastic T cell lymphoma. Nat Genet. 46(4):371–375.
   PubMed Web of Science ®Google Scholar
• Zang S, Li J, Yang H, Zeng H, Han W, Zhang J, Lee M, Moczygemba M, Isgandarova S, Yang Y, et al. 2017. Mutations in 5-methylcytosine oxidase TET2 and RhoA cooperatively disrupt T cell homeostasis. J Clin Invest. 127(8):2998–3012.
   PubMed Web of Science ®Google Scholar
• Zehir A, Benayed R, Shah RH, Syed A, Middha S, Kim HR, Srinivasan P, Gao J, Chakravarty D, Devlin SM, et al. 2017. Mutational landscape of metastatic cancer revealed from prospective clinical sequencing of 10,000 patients. Nat Med. 23(6):703–713.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Li G. 2020. A tumor suppressor DLC1: the functions and signal pathways. J Cell Physiol. 235(6):4999–5007.
   PubMed Web of Science ®Google Scholar
• Zhang H, Schaefer A, Wang Y, Hodge RG, Blake DR, Diehl JN, Papageorge AG, Stachler MD, Liao J, Zhou J, et al. 2020. Gain-of-function RHOA mutations promote focal adhesion kinase activation and dependency in diffuse gastric cancer. Cancer Discov. 10(2):288–305.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang B. 2006. D4-GDI, a Rho GTPase regulator, promotes breast cancer cell invasiveness. Cancer Res. 66(11):5592–5598.
   PubMed Web of Science ®Google Scholar
• Zohar M, Teramoto H, Katz B-Z, Yamada KM, Gutkind JS. 1998. Effector domain mutants of Rho dissociate cytoskeletal changes from nuclear signaling and cellular transformation. Oncogene. 17(8):991–998.
   PubMed Web of Science ®Google Scholar
• Zong H, Kaibuchi K, Quilliam LA. 2001. The insert region of RhoA is essential for Rho kinase activation and cellular transformation. Mol Cell Biol. 21(16):5287–5298.
   PubMed Web of Science ®Google Scholar