Induction of nonapoptotic cell death by activated ras requires inverse regulation of Rac1 and Arf6

Molecular Cancer Research

Volumn 8, Issue 10, 2010, Pages 1358-1374

  Bhanot, Haymanti ^a   Young, Ashley M ^a   Overmeyer, Jean H ^a   Maltese, William A ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN GIT1; PROTEIN INHIBITOR; RAC1 PROTEIN; RAS PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; CELL STRUCTURE; CELL VACUOLE; CELL VIABILITY; ENDOSOME; ENZYME ACTIVATION; ENZYME INACTIVATION; GLIOMA CELL; HUMAN; HUMAN CELL; METHUOSIS; NUCLEOTIDE SEQUENCE; ONCOGENE H RAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADP-RIBOSYLATION FACTORS; APOPTOSIS; CELL CYCLE PROTEINS; CELL DEATH; CELL LINE, TUMOR; DOWN-REGULATION; ENDOCYTOSIS; ENDOSOMES; ENZYME ACTIVATION; GLIOBLASTOMA; HEK293 CELLS; HUMANS; OSTEOSARCOMA; RAC1 GTP-BINDING PROTEIN; RAS PROTEINS; VACUOLES;

EID: 78649670089     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-10-0090     Document Type: Article

References (77)

1. Bursch W, Ellinger A, Gerner C, Frohwein U, Schulte-Hermann R. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann N Y Acad Sci 2000;926:1-12.
2. Lockshin RA, Zakeri Z. Apoptosis, autophagy, and more. Int J Biochem Cell Biol 2004;36:2405-19.
3. Gozuacik D, Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004;23:2891-906.
4. Sperandio S, de Belle I, Bredesen DE. An alternative, nonapoptotic form of programmed cell death. Proc Natl Acad Sci U S A 2000;97:14376-81.
5. Wang Y, Li X, Wang L, et al. An alternative form of paraptosis-like cell death, triggered by TAJ/TROY and enhanced by PDCD5 overexpression. J Cell Sci 2004;117:1525-32.
6. Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 1995;146:3-15.
7. Trump BF, Berezesky IK, Chang SH, Phelps PC. The pathways of cell death: oncosis, apoptosis, and necrosis. Toxicol Pathol 1997;25:82-8.
8. Suarez Y, Gonzalez L, Cuadrado A, et al. Kahalalide F, a new marine-derived compound, induces oncosis in human prostate and breast cancer cells. Mol Cancer Ther 2003;2:863-72.
9. Degterev A, Huang Z, Boyce M, et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005;1:112-9.
10. Han W, Li L, Qiu S, et al. Shikonin circumvents cancer drug resistance by induction of a necroptotic death. Mol Cancer Ther 2007;6:1641-9.
11. Overholtzer M, Mailleux AA, Mouneimne G, et al. A nonapoptotic cell death process, entosis, that occurs by cell-in-cell invasion. Cell 2007;131:966-79.
12. Syntichaki P, Tavernarakis N. Death by necrosis. Uncontrollable catastrophe, or is there order behind the chaos? EMBO Rep 2002;3:604-9.
13. Edinger AL, Thompson CB. Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 2004;16:663-9.
14. Chi S, Kitanaka C, Noguchi K, et al. Oncogenic Ras triggers cell suicide through the activation of a caspase-independent cell death program in human cancer cells. Oncogene 1999;18:2281-90.
15. Overmeyer JH, Kaul A, Johnson EE, Maltese WA. Active ras triggers death in glioblastoma cells through hyperstimulation of macropinocytosis. Mol Cancer Res 2008;6:965-77.
16. Clarke PH. Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 1990;181:195-213.
17. Schweichel J-U, Merker HJ. The morphology of various types of cell death in prenatal tissues. Teratology 1973;7:253-66.
18. Hotchin NA, Cover TL, Akhtar N. Cell vacuolization induced by the VacA cytotoxin of Helicobacter pylori is regulated by the Rac1 GTPase. J Biol Chem 2000;275:14009-12.
19. Suzuki J, Ohnishi H, Wada A, et al. Involvement of syntaxin 7 in human gastric epithelial cell vacuolization induced by the Helicobacter pylori-produced cytotoxin VacA. J Biol Chem 2003;278:25585-90.
20. Walker RM, McElligott TF. Furosemide induced hepatotoxicity. J Pathol 1981;135:301-14.
21. Kaul A, Overmeyer JH, Maltese WA. Activated Ras induces cytoplasmic vacuolization and non-apoptotic death in glioblastoma cells via novel effector pathways. Cell Signal 2007;19:1034-43.
22. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992;70:401-10.
23. Castellano F, Montcourrier P, Chavrier P. Membrane recruitment of Rac1 triggers phagocytosis. J Cell Sci 2000;113:2955-61.
24. Lambert JM, Lambert QT, Reuther GW, et al. Tiam1 mediates Ras activation of Rac by a PI(3)K-independent mechanism. Nat Cell Biol 2002;4:621-5.
25. Miura K, Nam JM, Kojima C, Mochizuki N, Sabe H. EphA2 engages Git1 to suppress Arf6 activity modulating epithelial cell-cell contacts. Mol Biol Cell 2009;20:1949-59.
26. Kaul A, Maltese WA. Killing of cancer cells by the photoactivatable protein kinase C inhibitor, calphostin C, involves induction of endoplasmic reticulum stress. Neoplasia 2009;11:823-34.
27. Zeng X, Overmeyer JH, Maltese WA. Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J Cell Sci 2006;119:259-70.
28. Johnson EE, Overmeyer JH, Gunning WT, Maltese WA. Gene silencing reveals a specific function of hVps34 phosphatidylinositol 3-kinase in late versus early endosomes. J Cell Sci 2006;119:1219-32.
29. Ladd PD, Butler JS, Skalnik DG. Identification of a genomic fragment that directs hematopoietic-specific expression of Rac2 and analysis of the DNA methylation profile of the gene locus. Gene 2004;341:323-33.
30. Corbetta S, Gualdoni S, Albertinazzi C, et al. Generation and characterization of Rac3 knockout mice. Mol Cell Biol 2005;25:5763-76.
31. Hajdo-Milasinovic A, Ellenbroek SI, van Es S, van d V, Collard JG. Rac1 and Rac3 have opposing functions in cell adhesion and differentiation of neuronal cells. J Cell Sci 2007;120:555-66.
32. Bolis A, Corbetta S, Cioce A, de C, I. Differential distribution of Rac1 and Rac3 GTPases in the developing mouse brain: implications for a role of Rac3 in Purkinje cell differentiation. Eur J Neurosci 2003;18:2417-24.
33. Campbell SL, Khosravi-Far R, Rossman KL, Clark GJ, Der CJ. Increasing complexity of Ras signaling. Oncogene 1998;17:1395-413.
34. Giehl K. Oncogenic Ras in tumour progression and metastasis. Biol Chem 2005;386:193-205.
35. Shutes A, Onesto C, Picard V, Leblond B, Schweighoffer F, Der CJ. Specificity and mechanism of action of EHT 1864, a novel small molecule inhibitor of Rac family small GTPases. J Biol Chem 2007;282:35666-78.
36. Radhakrishna H, Al Awar O, Khachikian Z, Donaldson JG. ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J Cell Sci 1999;112:855-66.
37. Welch HC, Coadwell WJ, Stephens LR, Hawkins PT. Phosphoinositide 3-kinase-dependent activation of Rac. FEBS Lett 2003;546:93-7.
38. Li N, Batzer A, Daly R, et al. Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 1993;363:85-8.
39. Innocenti M, Zippel R, Brambilla R, Sturani E. CDC25(Mm)/Ras-GRF1 regulates both Ras and Rac signaling pathways. FEBS Lett 1999;460:357-62.
40. Innocenti M, Tenca P, Frittoli E, et al. Mechanisms through which Sos-1 coordinates the activation of Ras and Rac. J Cell Biol 2002;156:125-36.
41. Peters PJ, Hsu VW, Ooi CE, et al. Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments. J Cell Biol 1995;128:1003-17.
42. Radhakrishna H, Donaldson JG. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J Cell Biol 1997;139:49-61.
43. Porat-Shliom N, Kloog Y, Donaldson JG. A unique platform for HRas signaling involving clathrin-independent endocytosis. Mol Biol Cell 2008;19:765-75.
44. Burridge K, Wennerberg K. Rho and Rac take center stage. Cell 2004;116:167-79.
45. Van Aelst L, Joneson T, Bar-Sagi D. Identification of a novel Rac1-interacting protein involved in membrane ruffling. EMBO J 1996;15:3778-86.
46. D'Souza-Schorey C, Boshans RL, McDonough M, Stahl PD, Van Aelst L. A role for POR1, a Rac1-interacting protein, in ARF6-mediated cytoskeletal rearrangements. EMBO J 1997;16:5445-54.
47. Shin OH, Exton JH. Differential binding of arfaptin 2/POR1 to ADP-ribosylation factors and Rac1. Biochem Biophys Res Commun 2001;285:1267-73.
48. Inoue H, Randazzo PA. Arf GAPs and their interacting proteins. Traffic 2007;8:1465-75.
49. Di Cesare A, Paris S, Albertinazzi C, et al. p95-1 links membrane transport to Rac-mediated reorganization of actin. Nat Cell Biol 2000;2:521-30.
50. Turner CE, Brown MC, Perrotta JA, et al. Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: a role in cytoskeletal remodeling. J Cell Biol 1999;145:851-63.
51. Paris S, Longhi R, Santambrogio P, de C, I. Leucine-zipper-mediated homo- and hetero-dimerization of GIT family p95-ARF GTPase-activating protein, PIX-, paxillin-interacting proteins 1 and 2. Biochem J 2003;372:391-8.
52. Hajdo-Milasinovic A, van der Kammen RA, Moneva Z, Collard JG. Rac3 inhibits adhesion and differentiation of neuronal cells by modifying GIT1 downstream signaling. J Cell Sci 2009;122:2127-36.
53. Ishii N, Maier D, Merlo A, et al. Frequent co-alterations of TP53, p16/CDKN2A, p14arf, PTEN tumor suppressor genes in human glioma cell lines. Brain Pathol 1999;9:469-79.
54. Furnari FB, Fenton T, Bachoo RM, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 2007;21:2683-710.
55. Swanson JA, Watts C. Macropinocytosis. Trends Cell Biol 1995;5:424-8.
56. Donaldson JG, Porat-Shliom N, Cohen LA. Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell Signal 2009;21:1-6.
57. Racoosin EL, Swanson JA. Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol 1993;121:1011-20.
58. Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 2009;10:597-608.
59. Chan AY, Coniglio SJ, Chuang YY, et al. Roles of the Rac1 and Rac3 GTPases in human tumor cell invasion. Oncogene 2005;24:7821-9.
60. Ridley AJ. Rho proteins: linking signaling with membrane trafficking. Traffic 2001;2:303-10.
61. Symons M, Rusk N. Control of vesicular trafficking by Rho GTPases. Curr Biol 2003;13:R409-18.
62. Lamaze C, Chuang TH, Terlecky LJ, Bokoch GM, Schmid SL. Regulation of receptor-mediated endocytosis by Rho and Rac. Nature 1996;382:177-9.
63. Malecz N, McCabe PC, Spaargaren C, Qiu R, Chuang Y, Symons M. Synaptojanin 2, a novel Rac1 effector that regulates clathrin-mediated endocytosis. Curr Biol 2000;10:1383-6.
64. Sun Y, Buki KG, Ettala O, Vaaraniemi JP, Vaananen HK. Possible role of direct Rac1-Rab7 interaction in ruffled border formation of osteoclasts. J Biol Chem 2005;280:32356-61.
65. Frasa MA, Maximiano FC, Smolarczyk K, et al. Armus is a Rac1 effector that inactivates Rab7 and regulates E-cadherin degradation. Curr Biol 2010;20:198-208.
66. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005;122:735-49.
67. Bar-Sagi D, Feramisco JR. Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins. Science 1986;233:1061-8.
68. Walsh AB, Bar-Sagi D. Differential activation of the Rac pathway by Ha-Ras and K-Ras. J Biol Chem 2001;276:15609-15.
69. Keely PJ, Westwick JK, Whitehead IP, Der CJ, Parise LV. Cdc42 and Rac1 induce integrin-mediated cell motility and invasiveness through PI(3)K. Nature 1997;390:632-6.
70. Edwards DC, Sanders LC, Bokoch GM, Gill GN. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat Cell Biol 1999;1:253-9.
71. Santy LC, Ravichandran KS, Casanova JE. The DOCK180/Elmo complex couples ARNO-mediated Arf6 activation to the downstream activation of Rac1. Curr Biol 2005;15:1749-54.
72. Koo TH, Eipper BA, Donaldson JG. Arf6 recruits the Rac GEF Kalirin to the plasma membrane facilitating Rac activation. BMC Cell Biol 2007;8:29.
73. Premont RT, Perry SJ, Schmalzigaug R, Roseman JT, Xing Y, Claing A. The GIT/PIX complex: an oligomeric assembly of GIT family ARF GTPase-activating proteins and PIX family Rac1/Cdc42 guanine nucleotide exchange factors. Cell Signal 2004;16:1001-11.
74. Li M, Wang J, Ng SS, et al. Adenosine diphosphate-ribosylation factor 6 is required for epidermal growth factor-induced glioblastoma cell proliferation. Cancer 2009;115:4959-72.
75. Molinari M, Galli C, Norais N, et al. Vacuoles induced by Helicobacter pylori toxin contain both late endosomal and lysosomal markers. J Biol Chem 1997;272:25339-44.
76. Reaves BJ, Bright NA, Mullock BM, Luzio JP. The effect of wortmannin on the localisation of lysosomal type I integral membrane glycoproteins suggests a role for phosphoinositide 3-kinase activity in regulating membrane traffic late in the endocytic pathway. J Cell Sci 1996;109:749-62.
77. Chies R, Nobbio L, Edomi P, Schenone A, Schneider C, Brancolini C. Alterations in the Arf6-regulated plasma membrane endosomal recycling pathway in cells overexpressing the tetraspan protein Gas3/PMP22. J Cell Sci 2003;116:987-99. (Pubitemid 36395610)