The lipid kinase PI4KIIIβ and the eEF1A2 oncogene co-operate to disrupt three-dimensional in vitro acinar morphogenesis

Experimental Cell Research

Volumn 317, Issue 17, 2011, Pages 2503-2511

  Pinke, Dixie E ^a   Lee, Jonathan M ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Breast cancer; EEF1A2; Phosphatidylinositol; PI4KIII ; Three dimensional morphology

Indexed keywords

ELONGATION FACTOR 1ALPHA; EUKARYOTIC ELONGATION FACTOR 1ALPHA 2; PHOSPHATIDYLINOSITOL 4 KINASE IIIBETA; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHATIDYLINOSITOL KINASE; UNCLASSIFIED DRUG;

ARTICLE; BREAST DEVELOPMENT; BREAST EPITHELIUM; BREAST TUMOR; CARCINOGENESIS; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MORPHOGENESIS; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

EUKARYOTA;

EID: 80052632423     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.08.002     Document Type: Article

References (49)

1. Balla A., Balla T. Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 2006, 16:351-361.
2. Antonietta De Matteis M., Di Campli A., Godi A. The role of the phosphoinositides at the Golgi complex. Biochim. Biophys. Acta Mol. Cell Res. 2005, 1744:396-405.
3. Godi A., Campli A.D., Konstantakopoulos A., Tullio G.D., Alessi D.R., Kular G.S., Daniele T., Marra P., Lucocq J.M., Matteis M.A.D. FAPPs control Golgi-to-cell-surface membrane traffic by binding to ARF and PtdIns(4)P. Nat. Cell Biol. 2004, 6:393-404.
4. Balla A., Tuymetova G., Tsiomenko A., Varnai P., Balla T. A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type III alpha: studies with the PH domains of the oxysterol binding protein and FAPP1. Mol. Cell. Biol. 2005, 16:1282-1295.
5. Jeganathan S., Morrow A., Amiri A., Lee J.M. Eukaryotic elongation factor 1A2 cooperates with phosphatidylinositol-4 kinase III beta to stimulate production of filopodia through increased phosphatidylinositol-4,5 bisphosphate generation. Mol. Cell. Biol. 2008, 28:4549-4561.
6. Martin-Belmonte F., Gassama A., Datta A., Yu W., Rescher U., Gerke V., Mostov K. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 2007, 128:383-397.
7. Martin-Belmonte F., Mostov K. Phosphoinositides control membrane polarity in epithelial development. Cell Cycle 2007, 6:1957-1961.
8. Martin-Belmonte F., Mostov K. Regulation of cell polarity during epithelial morphogenesis. Curr. Opin. Cell Biol. 2008, 20:227-234.
9. Debnath J., Brugge J.S. Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 2005, 5:675-688.
10. Debnath J., Muthuswamy S.K., Brugge J.S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003, 30:256-268.
11. Plachot C., Chaboub L., Adissu H., Wang L., Urazaev A., Sturgis J., Asem E., Lelievre S. Factors necessary to produce basoapical polarity in human glandular epithelium formed in conventional and high-throughput three-dimensional culture: example of the breast epithelium. BMC Biol. 2009, 7:77.
12. Imbalzano K., Tatarkova I., Imbalzano A., Nickerson J. Increasingly transformed MCF-10A cells have a progressively tumor-like phenotype in three-dimensional basement membrane culture. Cancer Cell Int. 2009, 9:7.
13. Bissell M.J., Radisky D. Putting tumours in context. Nat. Rev. Cancer 2001, 1:46-54.
14. O'Brien L.E., Zegers M.M.P., Mostov K.E. Building epithelial architecture: insights from three-dimensional culture models. Nat. Rev. Mol. Cell Biol. 2002, 3:531-537.
15. Streuli C.H., Bissell M.J. Expression of extracellular matrix components is regulated by substratum. J. Cell Biol. 1990, 110:1405-1415.
16. Lee E.Y., Lee W.H., Kaetzel C.S., Parry G., Bissell M.J. Interaction of mouse mammary epithelial cells with collagen substrata: regulation of casein gene expression and secretion. Proc. Natl. Acad. Sci. 1985, 82:1419-1423.
17. Debnath J., Walker S.J., Brugge J.S. Akt activation disrupts mammary acinar architecture and enhances proliferation in an mTOR-dependent manner. J. Cell Biol. 2003, 163:315-326.
18. Shaw K.R.M., Wrobel C.N., Brugge J.S. Use of three-dimensional basement membrane cultures to model oncogene-induced changes in mammary epithelial morphogenesis. J. Mammary Gland Biol. Neoplasia 2004, 9:297-310.
19. Underwood J.M., Imbalzano K.M., Weaver V.M., Fischer A.H., Imbalzano A.N., Nickerson J.A. The ultrastructure of MCF-10A acini. J. Cell. Physiol. 2006, 208:141-148.
20. Amiri A., Noei F., Jeganathan S., Kulkarni G., Pinke D.E., Lee J.M. eEF1A2 activates Akt and stimulates Akt-dependent actin remodeling, invasion and migration. Oncogene 2006, 26:3027-3040.
21. Grignani F., Kinsella T., Mencarelli A., Valtieri M., Riganelli D., Grignani F., Lanfrancone L., Peschle C., Nolan G.P., Pelicci P.G. High-efficiency gene transfer and selection of human hematopoietic progenitor cells with a hybrid EBV/retroviral vector expressing the green fluorescence protein. Cancer Res. 1998, 58:14-19.
22. Weigelt B., Bissell M.J. Unraveling the microenvironmental influences on the normal mammary gland and breast cancer. Semin. Cancer Biol. 2008, 18:311-321.
23. de Graaf P., Klapisz E.E., Schulz T.K.F., Cremers A.F.M., Verkleij A.J., van Bergen en Henegouwen P.M.P. Nuclear localization of phosphatidylinositol 4-kinase {beta}. J. Cell Sci. 2002, 115:1769-1775.
24. Wong K., Meyers A.R., Cantley L.C. Subcellular locations of phosphatidylinositol 4-kinase isoforms. J. Biol. Chem. 1997, 272:13236-13241.
25. Barth A.I.M., Pollack A.L., Altschuler Y., Mostov K.E., Nelson W.J. NH2-terminal deletion of β-catenin results in stable colocalization of mutant β-catenin with adenomatous polyposis coli protein and altered MDCK cell adhesion. J. Cell Biol. 1997, 136:693-706.
26. Bruns J.R., Ellis M.A., Jeromin A., Weisz O.A. Multiple roles for phosphatidylinositol 4-kinase in biosynthetic transport in polarized Madin-Darby canine kidney cells. J. Biol. Chem. 2002, 277:2012-2018.
27. Jeganathan S., Lee J.M. Binding of elongation factor eEF1A2 to phosphatidylinositol 4-kinase IIIB stimulates lipid kinase activity and phosphatidylinositol 4-phosphate generation. J. Biol. Chem. 2007, 282:372-380.
28. Yang W., Boss W. Regulation of phosphatidylinositol 4-kinase by the protein activator PIK-A49. Activation requires phosphorylation of PIK-A49. J. Biol. Chem. 1994, 269:3852-3857.
29. Yang W., Burkhart W., Cavallius J., Merrick W., Boss W. Purification and characterization of a phosphatidylinositol 4-kinase activator in carrot cells. J. Biol. Chem. 1993, 268:392-398.
30. Anand N., Murthy S., Amann G., Wernick M., Porter L.A., Cukier I.H., Collins C., Gray J.W., Diebold J., Demetrick D.J., Lee J.M. Protein elongation factor EEF1A2 is a putative oncogene in ovarian cancer. Nat. Genet. 2002, 31:301-305.
31. Kulkarni G., Turbin D., Amiri A., Jeganathan S., Andrade-Navarro M., Wu T., Huntsman D., Lee J. Expression of protein elongation factor eEF1A2 predicts favorable outcome in breast cancer. Breast Cancer Res. Treat. 2007, 102:31-41.
32. Pinke D.E., Kalloger S.E., Francetic T., Huntsman D.G., Lee J.M. The prognostic significance of elongation factor eEF1A2 in ovarian cancer. Gynecol. Oncol. 2008, 108:561-568.
33. Sorensen S.D., Linseman D.A., McEwen E.L., Heacock A.M., Fisher S.K. A role for a Wortmannin-sensitive phosphatidylinositol-4-kinase in the endocytosis of muscarinic cholinergic receptors. Mol. Pharmacol. 1998, 53:827-836.
34. Szentpetery Z., Várnai P., Balla T. Acute manipulation of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc. Natl. Acad. Sci. 2010, 107:8225-8230.
35. Chu K.M.E., Minogue S., Hsuan J.J., Waugh M.G. Differential effects of the phosphatidylinositol 4-kinases, PI4KII[alpha] and PI4KIII[beta], on Akt activation and apoptosis. Cell Death Dis. 2010, 1:e106.
36. Balla A., Tuymetova G., Barshishat M., Geiszt M.s., Balla T. Characterization of type II phosphatidylinositol 4-kinase isoforms reveals association of the enzymes with endosomal vesicular compartments. J. Biol. Chem. 2002, 277:20041-20050.
37. Cain E.L., Braun S.E., Beeser A. Characterization of a human cell line stably over-expressing the candidate oncogene, dual specificity phosphatase 12. PLoS ONE 2011, 6:e18677.
38. Gao X., Li C., Zhang R., Yang R., Qu X., Qiu H., Xu J., Lu H., Li J., Chen L. Fluorescence in situ hybridization analysis of chromosome aberrations in 60 Chinese patients with multiple myeloma. Med. Oncol. 2011, 1-7.
39. Uchida K., Oga A., Mano T., Nagatsuka H., Ueyama Y., Sasaki K. Screening for DNA copy number aberrations in mucinous adenocarcinoma arising from the minor salivary gland: two case reports. Cancer Genet. Cytogenet. 2010, 203:324-327.
40. Vicinanza M., D'Angelo G., Di Campli A., De Matteis M. Membrane traffic in the secretory pathway. Cell. Mol. Life Sci. 2008, 65:2833-2841.
41. D'Angelo G., Vicinanza M., Di Campli A., De Matteis M.A. The multiple roles of PtdIns(4)P - not just the precursor of PtdIns(4,5)P2. J. Cell Sci. 2008, 121:1955-1963.
42. Vicinanza M., D'Angelo G., Di Campli A., De Matteis M. Function and dysfunction of the PI system in membrane trafficking. EMBO J. 2008, 27:2457-2470.
43. Balla T., Várnai P. Visualization of cellular phosphoinositide pools with GFP-fused protein-domains 2001, John Wiley & Sons, Inc.
44. Mailleux A., Overholtzer M., Brugge J. Lumen formation during mammary epithelial morphogenesis: insights from in vitro and in vivo models. Cell Cycle 2008, 7:57-62.
45. Hof W.v.t., Malik A., Vijayakumar S., Qiao J., Adelsberg J.v., Al-Awqati Q. The effect of apical and basolateral lipids on the function of the band 3 anion exchange protein. J. Cell Biol. 1997, 139:941-949.
46. Gassama-Diagne A., Yu W., ter Beest M., Martin-Belmonte F., Kierbel A., Engel J., Mostov K. Phosphatidylinositol-3,4,5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nat. Cell Biol. 2006, 8:963-970.
47. Liu H., Radisky D.C., Wang F., Bissell M.J. Polarity and proliferation are controlled by distinct signaling pathways downstream of PI3-kinase in breast epithelial tumor cells. J. Cell Biol. 2004, 164:603-612.
48. Várnai P., Balla T. Live cell imaging of phosphoinositides with expressed inositide binding protein domains. Methods 2008, 46:167-176.
49. Balla T., Bondeva T., Varnai P. How accurately can we image inositol lipids in living cells?. Trends Pharmacol. Sci. 2000, 21:238-241.