IκB kinase complex (IKK) triggers detachment-induced autophagy in mammary epithelial cells independently of the PI3K-AKT-MTORC1 pathway

Autophagy

Volumn 9, Issue 8, 2013, Pages 1214-1227

  Chen, Nan ^a   Debnath, Jayanta ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anoikis; Autophagy; Extracellular matrix; Integrin; Mammary epithelial cells

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; I KAPPA B KINASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOGEN ACTIVATED PROTEIN KINASE 7; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RETROVIRUS VECTOR; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; VERY LATE ACTIVATION ANTIGEN 3; VERY LATE ACTIVATION ANTIGEN 4;

ANIMAL CELL; ANOIKIS; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST EPITHELIUM; CELL ADHESION; CELL CULTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MORPHOGENESIS; MOUSE; NONHUMAN; THREE DIMENSIONAL IMAGING; WILD TYPE;

ANOIKIS; AUTOPHAGY; EXTRACELLULAR MATRIX; INTEGRIN; MAMMARY EPITHELIAL CELLS;

ANIMALS; ANTIBODIES; ANTIGENS, CD29; APOPTOSIS; AUTOPHAGY; CELL ADHESION; EMBRYO, MAMMALIAN; ENZYME ACTIVATION; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FIBROBLASTS; HUMANS; I-KAPPA B KINASE; INTEGRIN ALPHA3; MAMMARY GLANDS, HUMAN; MAP KINASE KINASE KINASES; MICE; MULTIPROTEIN COMPLEXES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; TOR SERINE-THREONINE KINASES;

EID: 84883004080     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.24870     Document Type: Article

References (47)

1. Gilmore AP. Anoikis. Cell Death Differ 2005; 12(Suppl 2):1473-7; PMID:16247493; http://dx.doi. org/10.1038/sj.cdd.4401723
2. Frisch SM, Francis H. Disruption of epithelial cellmatrix interactions induces apoptosis. J Cell Biol 1994; 124:619-26; PMID:8106557; http://dx.doi. org/10.1083/jcb.124.4.619
3. Debnath J, Brugge JS. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 2005; 5:675-88; PMID:16148884; http://dx.doi. org/10.1038/nrc1695
4. 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; PMID:18094039; http://dx.doi.org/10.1091/mbc.E07-10-1092
5. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93; PMID:19653858; http://dx.doi. org/10.1146/annurev-genet-102808-114910
6. 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 2012; PMID:23160380; http://dx.doi.org/10.1038/onc.2012.512
7. Yan SR, Joseph RR, Rosen K, Reginato MJ, Jackson A, Allaire N, et al. Activation of NF-kappaB following detachment delays apoptosis in intestinal epithelial cells. Oncogene 2005; 24:6482-91; PMID:16007176
8. Criollo A, Senovilla L, Authier H, Maiuri MC, Morselli E, Vitale I, et al. The IKK complex contributes to the induction of autophagy. EMBO J 2010; 29:619-31; PMID:19959994; http://dx.doi.org/10.1038/emboj.2009.364
9. Siebenlist U, Franzoso G, Brown K. Structure, regulation and function of NF-kappa B. Annu Rev Cell Biol 1994; 10:405-55; PMID:7888182; http://dx.doi. org/10.1146/annurev.cb.10.110194.002201
10. Chariot A. The NF-kappaB-independent functions of IKK subunits in immunity and cancer. Trends Cell Biol 2009; 19:404-13; PMID:19648011; http://dx.doi.org/10.1016/j.tcb.2009.05.006
11. Comb WC, Cogswell P, Sitcheran R, Baldwin AS. IKK-dependent, NF-κB-independent control of autophagic gene expression. Oncogene 2011; 30:1727-32; PMID:21151171; http://dx.doi.org/10.1038/onc.2010.553
12. Kim JE, You DJ, Lee C, Ahn C, Seong JY, Hwang JI. Suppression of NF-kappaB signaling by KEAP1 regulation of IKKbeta activity through autophagic degradation and inhibition of phosphorylation. Cell Signal 2010; 22:1645-54; PMID:20600852; http://dx.doi.org/10.1016/j.cellsig.2010.06.004
13. Niida M, Tanaka M, Kamitani T. Downregulation of active IKK beta by Ro52-mediated autophagy. Mol Immunol 2010; 47:2378-87; PMID:20627395; http://dx.doi.org/10.1016/j.molimm.2010.05.004
14. Magnuson B, Ekim B, Fingar DC. Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J 2012; 441:1-21; PMID:22168436; http://dx.doi.org/10.1042/BJ20110892
15. Kwiatkowski DJ. Tuberous sclerosis: from tubers to mTOR. Ann Hum Genet 2003; 67:87-96; PMID:12556239; http://dx.doi.org/10.1046/j.1469-1809.2003.00012. x
16. Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley LC. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol Cell 2002; 10:151-62; PMID:12150915; http://dx.doi. org/10.1016/S1097-2765(02)00568-3
17. Inoki K, Li Y, Zhu T, Wu J, Guan KL. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 2002; 4:648-57; PMID:12172553; http://dx.doi.org/10.1038/ncb839
18. Urano J, Sato T, Matsuo T, Otsubo Y, Yamamoto M, Tamanoi F. Point mutations in TOR confer Rhebindependent growth in fission yeast and nutrientindependent mammalian TOR signaling in mammalian cells. Proc Natl Acad Sci U S A 2007; 104:3514-9; PMID:17360675; http://dx.doi.org/10.1073/pnas. 0608510104
19. Sancak Y, Thoreen CC, Peterson TR, Lindquist RA, Kang SA, Spooner E, et al. PRAS40 is an insulinregulated inhibitor of the mTORC1 protein kinase. Mol Cell 2007; 25:903-15; PMID:17386266; http://dx.doi.org/10.1016/j.molcel.2007.03. 003
20. Kovacina KS, Park GY, Bae SS, Guzzetta AW, Schaefer E, Birnbaum MJ, et al. Identification of a proline-rich Akt substrate as a 14-3-3 binding partner. J Biol Chem 2003; 278:10189-94; PMID:12524439; http://dx.doi. org/10.1074/jbc.M210837200
21. Pierce JW, Schoenleber R, Jesmok G, Best J, Moore SA, Collins T, et al. Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem 1997; 272:21096-103; PMID:9261113; http://dx.doi.org/10.1074/ jbc.272.34.21096
22. Geleziunas R, Ferrell S, Lin X, Mu Y, Cunningham ET Jr., Grant M, et al. Human T-cell leukemia virus type 1 Tax induction of NF-kappaB involves activation of the IkappaB kinase α (IKKalpha) and IKKbeta cellular kinases. Mol Cell Biol 1998; 18:5157-65; PMID:9710600
23. Nakano H, Shindo M, Sakon S, Nishinaka S, Mihara M, Yagita H, et al. Differential regulation of IkappaB kinase α and β by two upstream kinases, NF-kappaBinducing kinase and mitogen-activated protein kinase/ERK kinase kinase-1. Proc Natl Acad Sci U S A 1998; 95:3537-42; PMID:9520401; http://dx.doi. org/10.1073/pnas.95.7.3537
24. Skaug B, Jiang X, Chen ZJ. The role of ubiquitin in NF-kappaB regulatory pathways. Annu Rev Biochem 2009; 78:769-96; PMID:19489733; http://dx.doi. org/10.1146/annurev.biochem.78.070907.102750
25. Brown K, Gerstberger S, Carlson L, Franzoso G, Siebenlist U. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 1995; 267:1485-8; PMID:7878466; http://dx.doi. org/10.1126/science. 7878466
26. Kim C, Ye F, Ginsberg MH. Regulation of integrin activation. Annu Rev Cell Dev Biol 2011; 27:321-45; PMID:21663444; http://dx.doi.org/10.1146/ annurevcellbio- 100109-104104
27. Ruoslahti E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 1996; 12:697-715; PMID:8970741; http://dx.doi.org/10.1146/annurev. cellbio.12.1.697
28. Nishiuchi R, Takagi J, Hayashi M, Ido H, Yagi Y, Sanzen N, et al. Ligand-binding specificities of laminin-binding integrins: a comprehensive survey of laminin-integrin interactions using recombinant α3β1, α6β1, α7β1 and α6β4 integrins. Matrix Biol 2006; 25:189-97; PMID:16413178; http://dx.doi. org/10.1016/j.matbio.2005.12.001
29. Carter WG, Wayner EA, Bouchard TS, Kaur P. The role of integrins α 2 β 1 and α 3 β 1 in cell-cell and cell-substrate adhesion of human epidermal cells. J Cell Biol 1990; 110:1387-404; PMID:1691191; http://dx.doi.org/10.1083/jcb.110.4.1387
30. Werb Z, Tremble PM, Behrendtsen O, Crowley E, Damsky CH. Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J Cell Biol 1989; 109:877-89; PMID:2547805; http://dx.doi.org/10.1083/jcb.109.2.877
31. Dedhar S, Jewell K, Rojiani M, Gray V. The receptor for the basement membrane glycoprotein entactin is the integrin α 3/β 1. J Biol Chem 1992; 267:18908-14; PMID:1527019
32. Egles C, Huet HA, Dogan F, Cho S, Dong S, Smith A, et al. Integrin-blocking antibodies delay keratinocyte re-epithelialization in a human three-dimensional wound healing model. PLoS One 2010; 5:e10528; PMID:20502640; http://dx.doi.org/10.1371/journal. pone.0010528
33. Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, Brugge JS. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 2002; 111:29-40; PMID:12372298; http://dx.doi. org/10.1016/S0092-8674(02)01001-2
34. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003; 30:256-68; PMID:12798140; http://dx.doi.org/10.1016/ S1046-2023(03)00032-X
35. Jung CH, Ro SH, Cao J, Otto NM, Kim DH. mTOR regulation of autophagy. FEBS Lett 2010; 584:1287-95; PMID:20083114; http://dx.doi.org/10.1016/j. febslet.2010.01.017
36. Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Codogno P. Distinct classes of phosphatidylinositol 3'-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 2000; 275:992-8; PMID:10625637; http://dx.doi. org/10.1074/jbc.275.2.992
37. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006; 10:51-64; PMID:16843265; http://dx.doi.org/10. 1016/j. ccr.2006.06.001
38. Lock R, Roy S, Kenific CM, Su JS, Salas E, Ronen SM, et al. Autophagy facilitates glycolysis during Rasmediated oncogenic transformation. Mol Biol Cell 2011; 22:165-78; PMID:21119005; http://dx.doi. org/10.1091/mbc.E10-06-0500
39. Dan HC, Baldwin AS. Differential involvement of IkappaB kinases α and β in cytokine- and insulininduced mammalian target of rapamycin activation determined by Akt. J Immunol 2008; 180:7582-9; PMID:18490760
40. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[κ]B activity. Annu Rev Immunol 2000; 18:621-63; PMID:10837071; http://dx.doi.org/10.1146/annurev.immunol.18.1.621
41. Friedland JC, Lakins JN, Kazanietz MG, Chernoff J, Boettiger D, Weaver VM. α6β4 integrin activates Racdependent p21-activated kinase 1 to drive NF-kappaBdependent resistance to apoptosis in 3D mammary acini. J Cell Sci 2007; 120:3700-12; PMID:17911169; http://dx.doi.org/10.1242/jcs.03484
42. Weaver VM, Lelièvre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, et al. β4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2002; 2:205-16; PMID:12242153; http://dx.doi.org/10. 1016/S1535-6108(02)00125-3
43. Scaife CL, Kuang J, Wills JC, Trowbridge DB, Gray P, Manning BM, et al. Nuclear factor kappaB inhibitors induce adhesion-dependent colon cancer apoptosis: implications for metastasis. Cancer Res 2002; 62:6870-8; PMID:12460901
44. Chen N, Eritja N, Lock R, Debnath J. Autophagy restricts proliferation driven by oncogenic phosphatidylinositol 3-kinase in three-dimensional culture. Oncogene 2012; PMID:22777351; http://dx.doi. org/10.1038/onc.2012.277
45. Gong C, Bauvy C, Tonelli G, Yue W, Deloménie C, Nicolas V, et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene 2013; 32:2261-72; PMID:22733132; http://dx.doi.org/10.1038/onc.2012.252
46. Debnath J, Walker SJ, Brugge JS. Akt activation disrupts mammary acinar architecture and enhances proliferation in an mTOR-dependent manner. J Cell Biol 2003; 163:315-26; PMID:14568991; http://dx.doi. org/10.1083/jcb.200304159
47. Debnath J. Detachment-induced autophagy in threedimensional epithelial cell cultures. Methods Enzymol 2009; 452:423-39; PMID:19200896; http://dx.doi. org/10.1016/S0076-6879(08)03625-2