A comprehensive siRNA screen for kinases that suppress macroautophagy in optimal growth conditions

Autophagy

Volumn 7, Issue 8, 2011, Pages 892-903

  Szyniarowski, Piotr ^a,b   Corcelle Termeau, Elisabeth ^a   Farkas, Thomas ^a   Hyøer Hansen, Maria ^a   Nylandsted, Jesper ^a   Kallunki, Tuula ^a   Jäättelä, Marja ^a  

^a Institute of Cancer Biology   (Denmark)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Autophagy; Breast; Cancer; Lysosome; mTORC1; Signaling; siRNA

Indexed keywords

BETA N ACETYLGLUCOSAMINYLGLYCOPEPTIDE BETA 1,4 GALACTOSYLTRANSFERASE; CASEIN KINASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MAMMALIAN TARGET OF RAPAMYCIN; N ACETYL BETA GLUCOSAMINIDASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE; PORPHOBILINOGEN DEAMINASE; PROTEIN KINASE C; PYRUVATE KINASE; RHEB PROTEIN; S6 KINASE; SMALL INTERFERING RNA;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL STRAIN MCF 7; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SUBSTRATE; HUMAN; HUMAN CELL CULTURE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 79961118337     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.7.8.15770     Document Type: Article

References (48)

1. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75. (Pubitemid 351317450)
2. Wang CW, Klionsky DJ. The molecular mechanism of autophagy. Mol Med 2003; 9:65-76. (Pubitemid 36819962)
3. Yoshimori T. Autophagy: a regulated bulk degradation process inside cells. Biochem Biophys Res Commun 2004; 313:453-8. (Pubitemid 37543608)
4. Sarkar S, Ravikumar B, Floto RA, Rubinsztein DC. Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine- expanded huntingtin and related proteinopathies. Cell Death Differ 2009; 16:46-56.
5. Yorimitsu T, Klionsky DJ. Endoplasmic reticulum stress: a new pathway to induce autophagy. Autophagy 2007; 3:160-2. (Pubitemid 46449112)
6. Hoyer-Hansen M, Bastholm L, Mathiasen IS, Elling F, Jaattela M. Vitamin D analog EB1089 triggers dramatic lysosomal changes and Beclin 1-mediated autophagic cell death. Cell Death Differ 2005; 12:1297-309. (Pubitemid 41486100)
7. Farkas T, Hoyer-Hansen M, Jaattela M. Identification of novel autophagy regulators by a luciferase-based assay for the kinetics of autophagic flux. Autophagy 2009; 5:1018-25.
8. Kroemer G, Jäättelä M. Lysosomes and autophagy in cell death control. Nat Rev Cancer 2005; 5:886-97. (Pubitemid 41746033)
9. Mathew R, Karantza-Wadsworth V, White E. Role of autophagy in cancer. Nat Rev Cancer 2007; 7:961-7. (Pubitemid 350165856)
10. Hoyer-Hansen M, Jaattela M. Autophagy: an emerging target for cancer therapy. Autophagy 2008; 4:574-80.
11. Degtyarev M, De Maziere A, Orr C, Lin J, Lee BB, Tien JY, et al. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Biol 2008; 183:101-16.
12. Ostenfeld MS, Hoyer-Hansen M, Bastholm L, Fehrenbacher N, Olsen OD, Groth-Pedersen L, et al. Anti-cancer agent siramesine is a lysosomotropic detergent that induces cytoprotective autophagosome accumulation. Autophagy 2008; 4:487-99. (Pubitemid 351705145)
13. Vazquez-Martin A, Oliveras-Ferraros C, Menendez JA. Autophagy facilitates the development of breast cancer resistance to the anti-HER2 monoclonal antibody trastuzumab. PLoS One 2009; 4:6251.
14. Dowling RJ, Topisirovic I, Fonseca BD, Sonenberg N. Dissecting the role of mTOR: Lessons from mTOR inhibitors. Biochim Biophys Acta 2009.
15. Corcelle EA, Puustinen P, Jaattela M. Apoptosis and autophagy: Targeting autophagy signalling in cancer cells - 'trick or treats'? FEBS J 2009; 276:6084-96.
16. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 2000; 150:1507-13.
17. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20:1992-2003.
18. Ganley IG, Lam du H, Wang J, Ding X, Chen S, Jiang X. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 2009; 284:12297-305.
19. Chan EY, Kir S, Tooze SA. siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J Biol Chem 2007; 282:25464-74. (Pubitemid 47372826)
20. Seglen PO, Gordon PB. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci USA 1982; 79:1889-92. (Pubitemid 12088533)
21. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-75. (Pubitemid 351231180)
22. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005; 171:603-14. (Pubitemid 41668720)
23. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140:313-26.
24. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282:24131-45. (Pubitemid 47328003)
25. Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007; 3:452-60. (Pubitemid 47293726)
26. Nylandsted J, Gyrd-Hansen M, Danielewicz A, Fehrenbacher N, Lademann U, Hoyer-Hansen M, et al. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J Exp Med 2004; 200:425-35. (Pubitemid 39121900)
27. Saftig P, Klumperman J. Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat Rev Mol Cell Biol 2009; 10:623-35.
28. Jung CH, Ro SH, Cao J, Otto NM, Kim DH. mTOR regulation of autophagy. FEBS Lett 2010; 584:1287-95.
29. Bhaskar PT, Hay N. The two TORCs and Akt. Dev Cell 2007; 12:487-502. (Pubitemid 46523652)
30. Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, et al. Localization of phosphatidylinositol- 3-phosphate in yeast and mammalian cells. EMBO J 2000; 19:4577-88.
31. Lipinski MM, Hoffman G, Ng A, Zhou W, Py BF, Hsu E, et al. A genome-wide siRNA screen reveals multiple mTORC1 independent signaling pathways regulating autophagy under normal nutritional conditions. Dev Cell 2010; 18:1041-52.
32. Comes F, Matrone A, Lastella P, Nico B, Susca FC, Bagnulo R, et al. A novel cell type-specific role of p38alpha in the control of autophagy and cell death in colorectal cancer cells. Cell Death Differ 2007; 14:693-702. (Pubitemid 46444507)
33. Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta and Bcl-2. Mol Cell 2007; 25:193-205. (Pubitemid 46109606)
34. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J, et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 2010; 465:942-6.
35. Inbal B, Bialik S, Sabanay I, Shani G, Kimchi A. DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J Cell Biol 2002; 157:455-68. (Pubitemid 34839809)
36. Wang X, Hoekstra MF, DeMaggio AJ, Dhillon N, Vancura A, Kuret J, et al. Prenylated isoforms of yeast casein kinase I, including the novel Yck3p, suppress the gcs1 blockage of cell proliferation from stationary phase. Mol Cell Biol 1996; 16:5375-85. (Pubitemid 26315056)
37. Gross SD, Hoffman DP, Fisette PL, Baas P, Anderson RA. A phosphatidylinositol-4,5-bisphosphate-sensitive casein kinase Ialpha associates with synaptic vesicles and phosphorylates a subset of vesicle proteins. J Cell Biol 1995; 130:711-24.
38. Gross SD, Anderson RA. Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family. Cell Signal 1998; 10:699-711. (Pubitemid 28520022)
39. Hoyer-Hansen M, Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007; 14:1576-82. (Pubitemid 47278843)
40. Swanton C, Marani M, Pardo O, Warne PH, Kelly G, Sahai E, et al. Regulators of mitotic arrest and ceramide metabolism are determinants of sensitivity to paclitaxel and other chemotherapeutic drugs. Cancer Cell 2007; 11:498-512. (Pubitemid 46856907)
41. Birmingham A, Anderson EM, Reynolds A, Ilsley- Tyree D, Leake D, Fedorov Y, et al. 3′ UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat Methods 2006; 3:199-204.
42. Walker KS, Deak M, Paterson A, Hudson K, Cohen P, Alessi DR. Activation of protein kinase Bbeta and gamma isoforms by insulin in vivo and by 3-phosphoinositide- dependent protein kinase-1 in vitro: comparison with protein kinase B alpha. Biochem J 1998; 331:299-308.
43. Martin KA, Merenick BL, Ding M, Fetalvero KM, Rzucidlo EM, Kozul CD, et al. Rapamycin promotes vascular smooth muscle cell differentiation through insulin receptor substrate-1/phosphatidylinositol-3-kinase/Akt2 feedback signaling. J Biol Chem 2007; 282:36112-20. (Pubitemid 350277159)
44. Neumann B, Walter T, Heriche JK, Bulkescher J, Erfle H, Conrad C, et al. Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 2010; 464:721-7.
45. Flicek P, Aken BL, Ballester B, Beal K, Bragin E, Brent S, et al. Ensembl's 10th year. Nucleic Acids Res 2010; 38:557-62.
46. Herrero-Martin G, Hoyer-Hansen M, Garcia-Garcia C, Fumarola C, Farkas T, Lopez-Rivas A, et al. TAK1 activates AMPK-dependent cytoprotective autophagy in TRAIL-treated epithelial cells. EMBO J 2009; 28:677-85.
47. Rohde M, Daugaard M, Jensen MH, Helin K, Nylandsted J, Jaattela M. Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev 2005; 19:570-82. (Pubitemid 40314989)
48. Foghsgaard L, Wissing D, Mauch D, Lademann U, Bastholm L, Boes M, et al. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor. J Cell Biol 2001; 153:999-1010.