Identification of a novel AMPK-PEA15 axis in the anoikis-resistant growth of mammary cells

Breast Cancer Research

Volumn 16, Issue 4, 2014, Pages

  Hindupur, Sravanth K ^a   Balaji, Sai A ^a   Saxena, Meera ^a   Pandey, Shubham ^a   Sravan, Gopalkrishnashetty S ^a   Heda, Namrata ^a   Kumar, M V ^b   Mukherjee, Geetashree ^b   Dey, Devaveena ^a   Rangarajan, Annapoorni ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b KIDWAI MEMORIAL INSTITUTE OF ONCOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PEA15 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; PEA15 PROTEIN, HUMAN; PHOSPHOPROTEIN; SIGNAL PEPTIDE;

ANCHORAGE INDEPENDENT GROWTH; ANOIKIS; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; BREAST EPITHELIUM; CARCINOGENICITY; CELL GROWTH; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; CELL CULTURE TECHNIQUE; CELL PROLIFERATION; CELL TRANSFORMATION; CYTOLOGY; EPITHELIUM CELL; FEMALE; MAMMARY GLAND; METABOLISM; MULTICELLULAR SPHEROID; PHOSPHORYLATION; TUMOR CELL LINE;

AMP-ACTIVATED PROTEIN KINASES; ANOIKIS; APOPTOSIS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; ENZYME ACTIVATION; EPITHELIAL CELLS; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAMMARY GLANDS, HUMAN; PHOSPHOPROTEINS; PHOSPHORYLATION; SPHEROIDS, CELLULAR;

EID: 84906828142     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-014-0420-z     Document Type: Article

References (52)

1. Giancotti FG, Ruoslahti E. Integrin signaling. Science 1999, 285:1028-1032. 10.1126/science.285.5430.1028, 10446041.
2. Schafer ZT, Grassian AR, Song L, Jiang Z, Gerhart-Hines Z, Irie HY, Gao S, Puigserver P, Brugge JS. Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 2009, 461:109-113. 10.1038/nature08268, 19693011.
3. Frisch SM, Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994, 124:619-626. 10.1083/jcb.124.4.619, 8106557.
4. Frisch SM, Ruoslahti E. Integrins and anoikis. Curr Opin Cell Biol 1997, 9:701-706. 10.1016/S0955-0674(97)80124-X, 9330874.
5. Schwartz MA. Integrins, oncogenes, and anchorage independence. J Cell Biol 1997, 139:575-578. 10.1083/jcb.139.3.575, 9348275.
6. Merto GR, Cella N, Hynes NE. Apoptosis is accompanied by changes in Bcl-2 and Bax expression, induced by loss of attachment, and inhibited by specific extracellular matrix proteins in mammary epithelial cells. Cell Growth Differ 1997, 8:251-260. 9040947.
7. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003, 17:1253-1270. 10.1101/gad.1061803, 12756227.
8. Dey D, Saxena M, Paranjape AN, Krishnan V, Giraddi R, Kumar MV, Mukherjee G, Rangarajan A. Phenotypic and functional characterization of human mammary stem/progenitor cells in long term culture. PLoS One 2009, 4:e5329. 10.1371/journal.pone.0005329, 19390630.
9. Kim YN, Koo KH, Sung JY, Yun UJ, Kim H. Anoikis resistance: an essential prerequisite for tumor metastasis. Int J Cell Biol 2012, 2012:306879. 10.1155/2012/306879, 22505926.
10. Jay R, Harris MEL, Monica M, Kent Osborne C. Diseases of the Breast 1999, Lippincott Williams & Wilkins Annals of Surgery, Philadelphia, PA.
11. Steinberg GR, Kemp BE. AMPK in health and disease. Physiol Rev 2009, 89:1025-1078. 10.1152/physrev.00011.2008, 19584320.
12. Ting L, Bo W, Li R, Chen X, Wang Y, Jun Z, Yu L. AMP-activated protein kinase supports the NGF-induced viability of human HeLa cells to glucose starvation. Mol Biol Rep 2010, 37:2593-2598. 10.1007/s11033-009-9780-3, 19728147.
13. Poels J, Spasic MR, Callaerts P, Norga KK. Expanding roles for AMP-activated protein kinase in neuronal survival and autophagy. Bioessays 2009, 31:944-952. 10.1002/bies.200900003, 19644919.
14. Kumar SH, Rangarajan A. Simian virus 40 small T antigen activates AMPK and triggers autophagy to protect cancer cells from nutrient deprivation. J Virol 2009, 83:8565-8574. 10.1128/JVI.00603-09, 19515765.
15. Ng TL, Leprivier G, Robertson MD, Chow C, Martin MJ, Laderoute KR, Davicioni E, Triche TJ, Sorensen PH. The AMPK stress response pathway mediates anoikis resistance through inhibition of mTOR and suppression of protein synthesis. Cell Death Differ 2012, 19:501-510. 10.1038/cdd.2011.119, 21941369.
16. Avivar-Valderas A, Bobrovnikova-Marjon E, Alan Diehl J, Bardeesy N, Debnath J, Aguirre-Ghiso JA. Regulation of autophagy during ECM detachment is linked to a selective inhibition of mTORC1 by PERK. Oncogene 2013, 32:4932-4940. 10.1038/onc.2012.512, 23160380.
17. Jeon SM, Chandel NS, Hay N. AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress. Nature 2012, 485:661-665. 10.1038/nature11066, 22660331.
18. Fung C, Lock R, Gao S, Salas E, Debnath J. Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell 2008, 19:797-806. 10.1091/mbc.E07-10-1092, 18094039.
19. Araujo H, Danziger N, Cordier J, Glowinski J, Chneiweiss H. Characterization of PEA-15, a major substrate for protein kinase C in astrocytes. J Biol Chem 1993, 268:5911-5920. 8449955.
20. Callaway K, Abramczyk O, Martin L, Dalby KN. The anti-apoptotic protein PEA-15 is a tight binding inhibitor of ERK1 and ERK2, which blocks docking interactions at the D-recruitment site. Biochemistry 2007, 46:9187-9198. 10.1021/bi700206u, 17658892.
21. Sulzmaier F, Opoku-Ansah J, Ramos JW. Phosphorylation is the switch that turns PEA-15 from tumor suppressor to tumor promoter. Small GTPases 2012, 3:173-177. 10.4161/sgtp.20021, 22694972.
22. Renganathan H, Vaidyanathan H, Knapinska A, Ramos JW. Phosphorylation of PEA-15 switches its binding specificity from ERK/MAPK to FADD. Biochem J 2005, 390:729-735. 10.1042/BJ20050378, 15916534.
23. Eckert A, Bock BC, Tagscherer KE, Haas TL, Grund K, Sykora J, Herold-Mende C, Ehemann V, Hollstein M, Chneiweiss H, Wiestler OD, Walczak H, Roth W. The PEA-15/PED protein protects glioblastoma cells from glucose deprivation-induced apoptosis via the ERK/MAP kinase pathway. Oncogene 2007, 27:1155-1166. 10.1038/sj.onc.1210732, 17700518.
24. Goransson O, McBride A, Hawley SA, Ross FA, Shpiro N, Foretz M, Viollet B, Hardie DG, Sakamoto K. Mechanism of action of A-769662, a valuable tool for activation of AMP-activated protein kinase. J Biol Chem 2007, 282:32549-32560. 10.1074/jbc.M706536200, 17855357.
25. Kim JE, Kim YW, Lee IK, Kim JY, Kang YJ, Park SY. AMP-activated protein kinase activation by 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside (AICAR) inhibits palmitate-induced endothelial cell apoptosis through reactive oxygen species suppression. J Pharmacol Sci 2008, 106:394-403. 10.1254/jphs.FP0071857, 18360094.
26. Dunn EF, Fearns R, Connor JH. Akt inhibitor Akt-IV blocks virus replication through an Akt-independent mechanism. J Virol 2009, 83:11665-11672. 10.1128/JVI.01092-09, 19740993.
27. Paranjape AN, Mandal T, Mukherjee G, Kumar MV, Sengupta K, Rangarajan A. Introduction of SV40ER and hTERT into mammospheres generates breast cancer cells with stem cell properties. Oncogene 2012, 31:1896-1909. 10.1038/onc.2011.378, 21874052.
28. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001, 108:1167-1174. 10.1172/JCI13505, 11602624.
29. Frisch SM. Evidence for a function of death-receptor-related, death-domain-containing proteins in anoikis. Curr Biol 1999, 9:1047-1049. 10.1016/S0960-9822(99)80455-2, 10508612.
30. Moreno D, Knecht E, Viollet B, Sanz P. A769662, a novel activator of AMP-activated protein kinase, inhibits non-proteolytic components of the 26S proteasome by an AMPK-independent mechanism. FEBS Lett 2008, 582:2650-2654. 10.1016/j.febslet.2008.06.044, 18593584.
31. Sanders MJ, Ali ZS, Hegarty BD, Heath R, Snowden MA, Carling D. Defining the mechanism of activation of AMP-activated protein kinase by the small molecule A-769662, a member of the thienopyridone family. J Biol Chem 2007, 282:32539-32548. 10.1074/jbc.M706543200, 17728241.
32. Lavrik I, Golks A, Krammer PH. Death receptor signaling. J Cell Sci 2005, 118:265-267. 10.1242/jcs.01610, 15654015.
33. Fiory F, Formisano P, Perruolo G, Beguinot F. Frontiers: PED/PEA-15, a multifunctional protein controlling cell survival and glucose metabolism. Am J Physiol Endocrinol Metab 2009, 297:E592-E601. 10.1152/ajpendo.00228.2009, 19531639.
34. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 2008, 30:214-226. 10.1016/j.molcel.2008.03.003, 18439900.
35. Weekes J, Ball KL, Caudwell FB, Hardie DG. Specificity determinants for the AMP-activated protein kinase and its plant homologue analysed using synthetic peptides. FEBS Lett 1993, 334:335-339. 10.1016/0014-5793(93)80706-Z, 7902296.
36. Xiao C, Yang BF, Asadi N, Beguinot F, Hao C. Tumor necrosis factor-related apoptosis-inducing ligand-induced death-inducing signaling complex and its modulation by c-FLIP and PED/PEA-15 in glioma cells. J Biol Chem 2002, 277:25020-25025. 10.1074/jbc.M202946200, 11976344.
37. Shi X, Gipp J, Bushman W. Anchorage-independent culture maintains prostate stem cells. Dev Biol 2007, 312:396-406. 10.1016/j.ydbio.2007.09.042, 17976567.
38. Lombaert IM, Brunsting JF, Wierenga PK, Faber H, Stokman MA, Kok T, Visser WH, Kampinga HH, de Haan G, Coppes RP. Rescue of salivary gland function after stem cell transplantation in irradiated glands. PLoS One 2008, 3:e2063. 10.1371/journal.pone.0002063, 18446241.
39. Boudreau N, Sympson CJ, Werb Z, Bissell MJ. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 1995, 267:891-893. 10.1126/science.7531366, 7531366.
40. Van Keymeulen A, Rocha AS, Ousset M, Beck B, Bouvencourt G, Rock J, Sharma N, Dekoninck S, Blanpain C. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011, 479:189-193. 10.1038/nature10573, 21983963.
41. Liang J, Mills GB. AMPK: a contextual oncogene or tumor suppressor?. Cancer Res 2013, 73:2929-2935. 10.1158/0008-5472.CAN-12-3876, 23644529.
42. Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, Birnbaum MJ, Thompson CB. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 2005, 18:283-293. 10.1016/j.molcel.2005.03.027, 15866171.
43. Dasgupta B, Milbrandt J. AMP-activated protein kinase phosphorylates retinoblastoma protein to control mammalian brain development. Dev Cell 2009, 16:256-270. 10.1016/j.devcel.2009.01.005, 19217427.
44. Laderoute KR, Amin K, Calaoagan JM, Knapp M, Le T, Orduna J, Foretz M, Viollet B. 5'-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol Cell Biol 2006, 26:5336-5347. 10.1128/MCB.00166-06, 16809770.
45. Harhaji-Trajkovic L, Vilimanovich U, Kravic-Stevovic T, Bumbasirevic V, Trajkovic V. AMPK-mediated autophagy inhibits apoptosis in cisplatin-treated tumour cells. J Cell Mol Med 2009, 13:3644-3654. 10.1111/j.1582-4934.2009.00663.x, 20196784.
46. Avivar-Valderas A, Salas E, Bobrovnikova-Marjon E, Diehl JA, Nagi C, Debnath J, Aguirre-Ghiso JA. PERK integrates autophagy and oxidative stress responses to promote survival during extracellular matrix detachment. Mol Cell Biol 2011, 31:3616-3629. 10.1128/MCB.05164-11, 21709020.
47. Hardie DG, Salt IP, Hawley SA, Davies SP. AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem J 1999, 338:717-722. 10.1042/0264-6021:3380717, 10051444.
48. Osler ME, Zierath JR. Adenosine 5'-monophosphate-activated protein kinase regulation of fatty acid oxidation in skeletal muscle. Endocrinology 2008, 149:935-941. 10.1210/en.2007-1441, 18202133.
49. Shen X, Kramer RH. Adhesion-mediated squamous cell carcinoma survival through ligand-independent activation of epidermal growth factor receptor. Am J Pathol 2004, 165:1315-1329. 10.1016/S0002-9440(10)63390-1, 15466396.
50. Nagaprashantha LD, Vatsyayan R, Lelsani PC, Awasthi S, Singhal SS. The sensors and regulators of cell-matrix surveillance in anoikis resistance of tumors. Int J Cancer 2011, 128:743-752. 10.1002/ijc.25725, 20949625.
51. Singh AB, Sharma A, Dhawan P. Claudin-1 expression confers resistance to anoikis in colon cancer cells in a Src-dependent manner. Carcinogenesis 2012, 33:2538-2547. 10.1093/carcin/bgs275, 22941059.
52. Kato K, Ogura T, Kishimoto A, Minegishi Y, Nakajima N, Miyazaki M, Esumi H. Critical roles of AMP-activated protein kinase in constitutive tolerance of cancer cells to nutrient deprivation and tumor formation. Oncogene 2002, 21:6082-6090. 10.1038/sj.onc.1205737, 12203120.