Cancer stem cell drugs target K-ras signaling in a stemness context

Oncogene

Volumn 35, Issue 40, 2016, Pages 5248-5262

  Najumudeen, A K ^a   Jaiswal, A ^b   Lectez, B ^a   Oetken Lindholm, C ^a   Guzman C ^a   Siljamaki E ^a   Posada, I M D ^a   Lacey, E ^c   Aittokallio, T ^b   Abankwa, D ^a  

^a ÅBO AKADEMI UNIVERSITY   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c MICROBIAL SCREENING TECHNOLOGIES PTY LTD   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; AVERMECTIN; CALMODULIN; CONGLOBATIN A; DIMETHYL SULFOXIDE; DOXORUBICIN; IVERMECTIN; K RAS PROTEIN; KAZUSAMYCIN B; LASALOCID; LEPTOMYCIN B; NIGERICIN; OPHIOBOLIN A; RUFOCROMOMYCIN; SALINOMYCIN; UNCLASSIFIED DRUG; CONGLOBATIN; K-RAS4B PROTEIN, HUMAN; OXAZOLE DERIVATIVE; PROTEIN P21; PYRAN DERIVATIVE; RAS PROTEIN; SESTERTERPENE;

ANIMAL CELL; ARTICLE; BHK CELL LINE; CANCER RESISTANCE; CANCER STEM CELL; CAVEOLA; CONTROLLED STUDY; DRUG POTENCY; DRUG RESPONSE; DRUG SENSITIVITY; DRUG SPECIFICITY; DRUG TARGETING; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MDCK CELL LINE; MEMBRANE STRUCTURE; NONHUMAN; ONCOGENE H RAS; PREDICTIVE VALUE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MCF-7 CELL LINE; NEOPLASMS; PATHOLOGY;

CALMODULIN; CAVEOLAE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MCF-7 CELLS; NEOPLASMS; NEOPLASTIC STEM CELLS; OXAZOLES; PROTO-ONCOGENE PROTEINS P21(RAS); PYRANS; RAS PROTEINS; SESTERTERPENES;

EID: 84961223582     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2016.59     Document Type: Article

References (68)

1. Kreso A, Dick JE. Evolution of the cancer stem cell model. Cell Stem Cell 2014; 14: 275-291.
2. Ansieau S. EMT in breast cancer stem cell generation. Cancer Lett 2013; 338: 63-68.
3. Medema JP. Cancer stem cells: The challenges ahead. Nat Cell Biol 2013; 15: 338-344.
4. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-284.
5. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010; 29: 4741-4751.
6. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA et al. Identification of selective inhibitors of cancer stem cells by high-Throughput screening. Cell 2009; 138: 645-659.
7. Zhou S, Wang F, Wong ET, Fonkem E, Hsieh T-C, Wu JM et al. Salinomycin: a novel anti-cancer agent with known anti-coccidial activities. Curr Med Chem 2013; 20: 4095-4101.
8. Naujokat C, Steinhart R. Salinomycin as a drug for targeting human cancer stem cells. J Biomed Biotechnol 2012; 2012: 950658.
9. Riccioni R, Dupuis ML, Bernabei M, Petrucci E, Pasquini L, Mariani G et al. The cancer stem cell selective inhibitor salinomycin is a p-glycoprotein inhibitor. Blood Cells Mol Dis 2010; 45: 86-92.
10. Lu D, Choi MY, Yu J, Castro JE, Kipps TJ, Carson DA. Salinomycin inhibits Wnt signaling and selectively induces apoptosis in chronic lymphocytic leukemia cells. Proc Natl Acad Sci USA 2011; 108: 13253-13257.
11. Fuchs D, Heinold A, Opelz G, Daniel V, Naujokat C. Salinomycin induces apoptosis and overcomes apoptosis resistance in human cancer cells. Biochem Biophys Res Commun 2009; 390: 743-749.
12. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
13. Hancock JF. Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 2003; 4: 373-385.
14. Spiegel J, Cromm PM, Zimmermann G, Grossmann TN, Waldmann H. Small-molecule modulation of Ras signaling. Nat Chem Biol 2014; 10: 613-622.
15. Abankwa D, Gorfe AA, Hancock JF. Ras nanoclusters: molecular structure and assembly. Semin Cell Dev Biol 2007; 18: 599-607.
16. Rotblat B, Belanis L, Liang H, Haklai R, Elad-Zefadia G, Hancock JF et al. H-Ras nanocluster stability regulates the magnitude of MAPK signal output. PLoS One 2010; 5: e11991.
17. Guzmán C, Solman M, Ligabue A, Blazevitš O, Andrade DM, Reymond L et al. The efficacy of Raf kinase recruitment to the GTPase H-ras depends on H-ras membrane conformer-specific nanoclustering. J Biol Chem 2014; 289: 9519-9533.
18. Zhou Y, Liang H, Rodkey T, Ariotti N, Parton RG, Hancock JF. Signal integration by lipid-mediated spatial cross talk between Ras nanoclusters. Mol Cell Biol 2014; 34: 862-876.
19. Ariotti N, Fernández-Rojo MA, Zhou Y, Hill MM, Rodkey TL, Inder KL et al. Caveolae regulate the nanoscale organization of the plasma membrane to remotely control Ras signaling. J Cell Biol 2014; 204: 777-792.
20. Köhnke M, Schmitt S, Ariotti N, Piggott AM, Parton RG, Lacey E et al. Design and application of in vivo FRET biosensors to identify protein prenylation and nanoclustering inhibitors. Chem Biol 2012; 19: 866-874.
21. Najumudeen AK, Köhnke M, Solman M, Alexandrov K, Abankwa D. Cellular FRET-biosensors to detect membrane targeting inhibitors of N-myristoylated proteins. PLoS One 2013; 8: e66425.
22. Najumudeen AK, Posada IMD, Lectez B, Zhou Y, Landor SK-J, Fallarero A et al. Phenotypic screening identifies protein synthesis inhibitors as H-Ras-nanoclusterincreasing tumor growth inducers. Biochemistry 2015; 54: 7212-7221.
23. Coxon F, Joachimiak Ł, Najumudeen AK, Breen G, Gmach J, Oetken-Lindholm C et al. Synthesis and characterization of novel phosphonocarboxylate inhibitors of RGGT. Eur J Med Chem 2014; 84: 77-89.
24. Crouthamel M, Abankwa D, Zhang L, DiLizio C, Manning DR, Hancock JF et al. An N-Terminal polybasic motif of Gaq is required for signaling and influences membrane nanodomain distribution. Mol Pharmacol 2010; 78: 767-777.
25. Sykes AM, Palstra N, Abankwa D, Hill JM, Skeldal S, Matusica D et al. The effects of transmembrane sequence and dimerization on cleavage of the p75 neurotrophin receptor by gamma-secretase. J Biol Chem 2012; 287: 43810-43824.
26. Tian T, Harding A, Inder K, Plowman S, Parton RG, Hancock JF. Plasma membrane nanoswitches generate high-fidelity Ras signal transduction. Nat Cell Biol 2007; 9: 905-914.
27. Solman M, Ligabue A, Blazevitš O, Jaiswal A, Zhou Y, Liang H et al. Specific cancerassociated mutations in the switch III region of Ras increase tumorigenicity by nanocluster augmentation. eLife 2015; 4: e08905.
28. Zhou Y, Hancock JF. Ras nanoclusters: Versatile lipid-based signaling platforms. Biochim Biophys Acta 2015; 1853: 841-849.
29. Abankwa D, Hanzal-Bayer M, Ariotti N, Plowman SJ, Gorfe AA, Parton RG et al. A novel switch region regulates H-ras membrane orientation and signal output. EMBO J 2008; 27: 727-735.
30. Abankwa D, Vogel H. A FRET map of membrane anchors suggests distinct microdomains of heterotrimeric G proteins. J Cell Sci 2007; 120: 2953-2962.
31. Huczyński A. Polyether ionophores-promising bioactive molecules for cancer therapy. Bioorg Med Chem Lett 2012; 22: 7002-7010.
32. Cho K-J, Park J-H, Piggott AM, Salim AA, Gorfe AA, Parton RG et al. Staurosporines disrupt phosphatidylserine trafficking and mislocalize Ras proteins. J Biol Chem 2012; 287: 43573-43584.
33. Fairn GD, Schieber NL, Ariotti N, Murphy S, Kuerschner L, Webb RI et al. High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine. J Cell Biol 2011; 194: 257-275.
34. Abankwa D, Gorfe AA, Inder K, Hancock JF. Ras membrane orientation and nanodomain localization generate isoform diversity. Proc Natl Acad Sci USA 2010; 107: 1130-1135.
35. Hill MM, Bastiani M, Luetterforst R, Kirkham M, Kirkham A, Nixon SJ et al. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 2008; 132: 113-124.
36. Bastiani M, Liu L, Hill MM, Jedrychowski MP, Nixon SJ, Lo HP et al. MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol 2009; 185: 1259-1273.
37. Hell SW. Far-field optical nanoscopy. Science (New York, NY) 2007; 316: 1153-1158.
38. Seguin L, Kato S, Franovic A, Camargo MF, Lesperance J, Elliott KC et al. An integrin β3-KRAS-RalB complex drives tumour stemness and resistance to EGFR inhibition. Nat Cell Biol 2014; 16: 457-468.
39. Kong L, Aho K-L, Granberg K, Lund R, Järvenpää L, Seppälä J et al. ESTOOLS Data@Hand: human stem cell gene expression resource. Nat Methods 2013; 10: 814-815.
40. Blair K, Wray J, Smith A. The liberation of embryonic stem cells. PLoS Genet 2011; 7: e1002019.
41. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012; 483: 603-607.
42. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH et al. CD44+/CD24-breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 2006; 8: R59.
43. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ et al. In vitro propagation and transcriptional profiling of human mammary stem/.progenitor cells. Genes Dev 2003; 17: 1253-1270.
44. Kong Au T, Chow Leung P. Identification of the binding and inhibition sites in the calmodulin molecule for ophiobolin A by site-directed mutagenesis. Plant Physiol 1998; 118: 965-973.
45. Wang M-T, Holderfield M, Galeas J, Delrosario R, To MD, Balmain A et al. K-Ras promotes tumorigenicity through suppression of non-canonical Wnt signaling. Cell 2015; 163: 1237-1251.
46. Nussinov R, Muratcioglu S, Tsai CJ, Jang H, Gursoy A, Keskin O. The key role of calmodulin in KRAS-driven adenocarcinomas. Mol Cancer Res 2015; 13: 1265-1273.
47. Quinlan MP, Quatela SE, Philips MR, Settleman J. Activated Kras, but not Hras or Nras, may initiate tumors of endodermal origin via stem cell expansion. Mol Cell Biol 2008; 28: 2659-2674.
48. Li Q, Bohin N, Wen T, Ng V, Magee J, Chen S-C et al. Oncogenic Nras has bimodal effects on stem cells that sustainably increase competitiveness. Nature 2013; 504: 143-147.
49. Nussinov R, Tsai CJ, Chakrabarti M, Jang H. A new view of Ras isoforms in cancers. Cancer Res 2016; 76: 18-23.
50. Tsai FD, Lopes MS, Zhou M, Court H, Ponce O, Fiordalisi JJ et al. K-Ras4A splice variant is widely expressed in cancer and uses a hybrid membranetargeting motif. Proc Natl Acad Sci USA 2015; 112: 779-784.
51. Mani SA, Guo W, Liao M-J, Eaton EN, Ayyanan A, Zhou AY et al. The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
52. Lemieux E, Cagnol S, Beaudry K, Carrier J, Rivard N. Oncogenic KRAS signalling promotes the Wnt/[beta]-catenin pathway through LRP6 in colorectal cancer. Oncogene 2014; 34: 4914-4927.
53. Lu Z, Ghosh S, Wang Z, Hunter T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of β-catenin, and enhanced tumor cell invasion. Cancer Cell 2003; 4: 499-515.
54. Baker N, Tuan RS. The less-often-Traveled surface of stem cells: caveolin-1 and caveolae in stem cells, tissue repair and regeneration. Stem Cell Res Ther 2013; 4: 1-1.
55. Sotgia F, Williams TM, Cohen AW, Minetti C, Pestell RG, Lisanti MP. Caveolin-1-deficient mice have an increased mammary stem cell population with upregulation of Wnt/beta-catenin signaling. Cell Cycle 2005; 4: 1808-1816.
56. Witkiewicz AK, Dasgupta A, Sotgia F, Mercier I, Pestell RG, Sabel M et al. An absence of stromal caveolin-1 expression predicts early tumor recurrence and poor clinical outcome in human breast cancers. Am J Pathol 2009; 174: 2023-2034.
57. Nassar ZD, Hill MM, Parton RG, Parat M-O. Caveola-forming proteins caveolin-1 and PTRF in prostate cancer. Nat Rev Urol 2013; 10: 529-536.
58. Collins BM, Davis MJ, Hancock JF, Parton RG. Structure-based reassessment of the caveolin signaling model: do caveolae regulate signaling through caveolinprotein interactions? Dev Cell 2012; 23: 11-20.
59. Kirkham M, Nixon SJ, Howes MT, Abi-Rached L, Wakeham DE, Hanzal-Bayer M et al. Evolutionary analysis and molecular dissection of caveola biogenesis. J Cell Sci 2008; 121: 2075-2086.
60. Sachlos E, Risueño RM, Laronde S, Shapovalova Z, Lee J-H, Russell J et al. Identification of drugs including a dopamine receptor antagonist that selectively target cancer stem cells. Cell 2012; 149: 1284-1297.
61. Boehmerle W, Muenzfeld H, Springer A, Huehnchen P, Endres M. Specific targeting of neurotoxic side effects and pharmacological profile of the novel cancer stem cell drug salinomycin in mice. J Mol Med 2014; 92: 889-900.
62. Eppert K, Takenaka K, Lechman ER, Waldron L, Nilsson B, van Galen P et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 2011; 17: 1086-1093.
63. Buganim Y, Faddah DA, Jaenisch R. Mechanisms and models of somatic cell reprogramming. Nat Rev Genet 2013; 14: 427-439.
64. Sinha B, Köster D, Ruez R, Gonnord P, Bastiani M, Abankwa D et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 2011; 144: 402-413.
65. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126: 677-689.
66. Meissner P, Pick H, Kulangara A, Chatellard P, Friedrich K, Wurm FM. Transient gene expression: recombinant protein production with suspension-Adapted HEK293-EBNA cells. Biotechnol Bioeng 2001; 75: 197-203.
67. Guzmán C, Oetken-Lindholm C, Abankwa D. Automated High-Throughput Fluorescence Lifetime Imaging Microscopy to Detect Protein-Protein Interactions. J Lab Autom; e-pub ahead of print 17 September 2015; doi:10.1177-/2211068215606048.
68. Zhu Y, Qiu P, Ji Y. TCGA-Assembler: open-source software for retrieving and processing TCGA data. Nat Methods 2014; 11: 599-600.