Hyper-dependence of breast cancer cell types on the nuclear transporter Importin β1

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 8, 2015, Pages 1870-1878

  Kuusisto, Henna V ^a,b   Jans, David A ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b Australian Government Australian Research Council   (Australia)

Author keywords

Importin; Isogenic cell pairs; Silencing RNA; Transformed cells

Indexed keywords

KARYOPHERIN BETA1; NUCLEAR PROTEIN; UNCLASSIFIED DRUG; KARYOPHERIN BETA; KPNB1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ARTICLE; BREAST CANCER CELL LINE; CANCER CELL; CELL DEATH; DNA TRANSFECTION; GENE OVEREXPRESSION; MAMMAL CELL; MCF10 CELL LINE; NUCLEAR IMPORT; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSFORMED CELL; TUMOR GROWTH; WESTERN BLOTTING; XTT ASSAY; ACTIVE TRANSPORT; ANTAGONISTS AND INHIBITORS; BREAST TUMOR; CELL CULTURE; CELL NUCLEUS; CELL PROLIFERATION; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; BETA KARYOPHERINS; BREAST NEOPLASMS; CELL DEATH; CELL NUCLEUS; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; PROTEIN TRANSPORT; RNA, SMALL INTERFERING;

EID: 84929448313     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2015.05.002     Document Type: Article

References (45)

1. Christiansen A., Dyrskjot L. The functional role of the novel biomarker karyopherin 2 (KPNA2) in cancer. Cancer Lett. 2013, 331:18-23.
2. Kuusisto H.V., Wagstaff K.M., Alvisi G., Roth D.M., Jans D.A. Global enhancement of nuclear localization-dependent nuclear transport in transformed cells. FASEB J. 2012, 26:1181-1193.
3. Dyrskjot L., Kruhoffer M., Thykjaer T., Marcussen N., Jensen J.L., Moller K., Orntoft T.F. Gene expression in the urinary bladder: a common carcinoma in situ gene expression signature exists disregarding histopathological classification. Cancer Res. 2004, 64:4040-4048.
4. van der Watt P.J., Maske C.P., Hendricks D.T., Parker M.I., Denny L., Govender D., Birrer M.J., Leaner V.D. The Karyopherin proteins, Crm1 and Karyopherin beta1, are overexpressed in cervical cancer and are critical for cancer cell survival and proliferation. Int. J. Cancer 2009, 124:1829-1840.
5. Wu M.-S., Lin Y.-S., Chang Y.-T., Shun C.-T., Lin M.-T., Lin J.-T. Gene expression profiling of gastric cancer by microarray combined with laser capture microdissection. World J. Gastroenterol. 2005, 11:7405-7412.
6. Miura K., Yoshinobu K., Imaizumi T., Haruna K., Miyamoto Y., Yoneda Y., Nakagata N., Araki M., Miyakawa T., Yamamura K.-i., Araki K. Impaired expression of importin/karyopherin beta1 leads to post-implantation lethality. Biochem. Biophys. Res. Commun. 2006, 341:132-138.
7. Tirian L., Puro J., Erdelyi M., Boros I., Papp B., Lippai M., Szabad J. The Ketel(D) dominant-negative mutations identify maternal function of the Drosophila importin-beta gene required for cleavage nuclei formation. Genetics 2000, 156:1901-1912.
8. Quan Y., Ji Z.-L., Wang X., Tartakoff A.M., Tao T. Evolutionary and transcriptional analysis of karyopherin beta superfamily proteins. Mol. Cell. Proteomics 2008, 7:1254-1269.
9. Lam M.H., Briggs L.J., Hu W., Martin T.J., Gillespie M.T., Jans D.A. Importin beta recognizes parathyroid hormone-related protein with high affinity and mediates its nuclear import in the absence of importin alpha. J. Biol. Chem. 1999, 274:7391-7398.
10. Chook Y.M., Suel K.E. Nuclear import by karyopherin-s: recognition and inhibition. Biochim. Biophys. Acta 2011, 1813:1593-1606.
11. Malki S., Nef S., Notarnicola C., Thevenet L., Gasca S., Mejean C., Berta P., Poulat F., Boizet-Bonhoure B. Prostaglandin D2 induces nuclear import of the sex-determining factor SOX9 via its cAMP-PKA phosphorylation. EMBO J. 2005, 24:1798-1809.
12. Harley V.R., Layfield S., Mitchell C.L., Forwood J.K., John A.P., Briggs L.J., McDowall S.G., Jans D.A. Defective importin beta recognition and nuclear import of the sex-determining factor SRY are associated with XY sex-reversing mutations. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:7045-7050.
13. Forwood J.K., Lam M.H., Jans D.A. Nuclear import of Creb and AP-1 transcription factors requires importin-beta 1 and Ran but is independent of importin-alpha. Biochemistry 2001, 40:5208-5217.
14. Hu W., Kemp B.E., Jans D.A. Kinetic properties of nuclear transport conferred by the retinoblastoma (Rb) NLS. J. Cell. Biochem. 2005, 95:782-793.
15. Zacksenhaus E., Jiang Z., Hei Y.J., Phillips R.A., Gallie B.L. Nuclear localization conferred by the pocket domain of the retinoblastoma gene product. Biochim. Biophys. Acta 1999, 1451:288-296.
16. Liang S.H., Clarke M.F. A bipartite nuclear localization signal is required for p53 nuclear import regulated by a carboxyl-terminal domain. J. Biol. Chem. 1999, 274:32699-32703.
17. Reich N.C., Liu L. Tracking STAT nuclear traffic. Nat. Rev. Immunol. 2006, 6:602-612.
18. Fagerlund R., Kinnunen L., Kohler M., Julkunen I., Melen K. NF-{kappa}B is transported into the nucleus by importin {alpha}3 and importin {alpha}4. J. Biol. Chem. 2005, 280:15942-15951.
19. Harel A., Forbes D.J. Importin beta: conducting a much larger cellular symphony. Mol. Cell 2004, 16:319-330.
20. Roscioli E., Di Francesco L., Bolognesi A., Giubettini M., Orlando S., Harel A., Schinina M.E., Lavia P. Importin-beta negatively regulates multiple aspects of mitosis including RANGAP1 recruitment to kinetochores. J. Cell Biol. 2012, 196:435-450.
21. Clarke P.R., Zhang C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat. Rev. Mol. Cell Biol. 2008, 9:464-477.
22. Santner S.J., Dawson P.J., Tait L., Soule H.D., Eliason J., Mohamed A.N., Wolman S.R., Heppner G.H., Miller F.R. Malignant MCF10CA1 cell lines derived from premalignant human breast epithelial MCF10AT cells. Breast Cancer Res. Treat. 2001, 65:101-110.
23. Arlett C.F., Green M.H., Priestley A., Harcourt S.A., Mayne L.V. Comparative human cellular radiosensitivity: I. The effect of SV40 transformation and immortalisation on the gamma-irradiation survival of skin derived fibroblasts from normal individuals and from ataxia-telangiectasia patients and heterozygotes. Int. J. Radiat. Biol. 1988, 54:911-928.
24. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. (RESEARCH0034).
25. Alvisi G., Ripalti A., Ngankeu A., Giannandrea M., Caraffi S.G., Dias M.M., Jans D.A. Human cytomegalovirus DNA polymerase catalytic subunit pUL54 possesses independently acting nuclear localization and pp UL44 binding motifs. Traffic 2006, 7:1322-1332.
26. Soderholm J.F., Bird S.L., Kalab P., Sampathkumar Y., Hasegawa K., Uehara-Bingen M., Weis K., Heald R. Importazole, a small molecule inhibitor of the transport receptor importin-beta. ACS Chem. Biol. 2011, 6:700-708.
27. Ciciarello M., Roscioli E., Di Fiore B., Di Francesco L., Sobrero F., Bernard D., Mangiacasale R., Harel A., Schinina M.E., Lavia P. Nuclear reformation after mitosis requires downregulation of the Ran GTPase effector RanBP1 in mammalian cells. Chromosoma 2010, 119:651-668.
28. Huber J., Cronshagen U., Kadokura M., Marshallsay C., Wada T., Sekine M., Luhrmann R. Snurportin1, an m3G-cap-specific nuclear import receptor with a novel domain structure. EMBO J. 1998, 17:4114-4126.
29. Choi Y.J., Li X., Hydbring P., Sanda T., Stefano J., Christie A.L., Signoretti S., Look A.T., Kung A.L., von Boehmer H., Sicinski P. The requirement for cyclin D function in tumor maintenance. Cancer Cell 2012, 22:438-451.
30. Soucek L., Whitfield J., Martins C.P., Finch A.J., Murphy D.J., Sodir N.M., Karnezis A.N., Swigart L.B., Nasi S., Evan G.I. Modelling Myc inhibition as a cancer therapy. Nature 2008, 455:679-683.
31. Kennedy R.D., Chen C.C., Stuckert P., Archila E.M., De la Vega M.A., Moreau L.A., Shimamura A., D'Andrea A.D. Fanconi anemia pathway-deficient tumor cells are hypersensitive to inhibition of ataxia telangiectasia mutated. J. Clin. Invest. 2007, 117:1440-1449.
32. Chen Z., Xiao Z., Gu W.Z., Xue J., Bui M.H., Kovar P., Li G., Wang G., Tao Z.F., Tong Y., Lin N.H., Sham H.L., Wang J.Y., Sowin T.J., Rosenberg S.H., Zhang H. Selective Chk1 inhibitors differentially sensitize p53-deficient cancer cells to cancer therapeutics. Int. J. Cancer 2006, 119:2784-2794.
33. Bonnet S., Archer S.L., Allalunis-Turner J., Haromy A., Beaulieu C., Thompson R., Lee C.T., Lopaschuk G.D., Puttagunta L., Harry G., Hashimoto K., Porter C.J., Andrade M.A., Thebaud B., Michelakis E.D. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 2007, 11:37-51.
34. Huang L., Wang H.Y., Li J.D., Wang J.H., Zhou Y., Luo R.Z., Yun J.P., Zhang Y., Jia W.H., Zheng M. KPNA2 promotes cell proliferation and tumorigenicity in epithelial ovarian carcinoma through upregulation of c-Myc and downregulation of FOXO3a. Cell Death Dis. 2013, 4:e745.
35. Wang C.I., Chien K.Y., Wang C.L., Liu H.P., Cheng C.C., Chang Y.S., Yu J.S., Yu C.J. Quantitative proteomics reveals regulation of karyopherin subunit alpha-2 (KPNA2) and its potential novel cargo proteins in nonsmall cell lung cancer. Mol. Cell. Proteomics 2012, 11:1105-1122.
36. Arvey A., Larsson E., Sander C., Leslie C.S., Marks D.S. Target mRNA abundance dilutes microRNA and siRNA activity. Mol. Syst. Biol. 2010, 6:363.
37. Sandy P., Ventura A., Jacks T. Mammalian RNAi: a practical guide. Biotechniques 2005, 39:215-224.
38. Turner J.G., Dawson J., Sullivan D.M. Nuclear export of proteins and drug resistance in cancer. Biochem. Pharmacol. 2012, 83:1021-1032.
39. Kudo N., Matsumori N., Taoka H., Fujiwara D., Schreiner E.P., Wolff B., Yoshida M., Horinouchi S. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9112-9117.
40. London C.A., Bernabe L.F., Barnard S., Kisseberth W.C., Borgatti A., Henson M., Wilson H., Jensen K., Ito D., Modiano J.F., Bear M.D., Pennell M.L., Saint-Martin J.-R., McCauley D., Kauffman M., Shacham S. Preclinical evaluation of the novel, orally bioavailable selective inhibitor of nuclear export (SINE) KPT-335 in spontaneous canine cancer: results of a phase I study. PLoS ONE 2014, 9:e87585.
41. Sekimoto T., Fukumoto M., Yoneda Y. 14-3-3 Suppresses the nuclear localization of threonine 157-phosphorylated p27(Kip1). EMBO J. 2004, 23:1934-1942.
42. Thompson M.E. BRCA1 16years later: nuclear import and export processes. FEBS J. 2010, 277:3072-3078.
43. Osborne C., Wilson P., Tripathy D. Oncogenes and tumor suppressor genes in breast cancer: potential diagnostic and therapeutic applications. Oncologist 2004, 9:361-377.
44. Martens-de Kemp S.R., Nagel R., Stigter-van Walsum M., van der Meulen I.H., van Beusechem V.W., Braakhuis B.J.M., Brakenhoff R.H. Functional genetic screens identify genes essential for tumor cell survival in head and neck and lung cancer. Clin. Cancer Res. 2013, 19:1994-2003.
45. Quensel C., Friedrich B., Sommer T., Hartmann E., Kohler M. In vivo analysis of importin alpha proteins reveals cellular proliferation inhibition and substrate specificity. Mol. Cell. Biol. 2004, 24:10246-10255.