2,587
Views
19
CrossRef citations to date
0
Altmetric
Basic Research Paper

GADD45A inhibits autophagy by regulating the interaction between BECN1 and PIK3C3

, , , , &
Pages 2247-2258 | Received 06 Apr 2015, Accepted 19 Oct 2015, Published online: 06 Jan 2016

References

  • Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 2008; 182:685-701; PMID:18725538; http://dx.doi.org/10.1083/jcb.200803137
  • Simonsen A, Tooze SA. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol 2009; 186:773-82; PMID:19797076; http://dx.doi.org/10.1083/jcb.200907014
  • Mizushima N. Autophagy: process and function. Genes Dev 2007; 21:2861-73; PMID:18006683; http://dx.doi.org/10.1101/gad.1599207
  • Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42; PMID:18191218; http://dx.doi.org/10.1016/j.cell.2007.12.018
  • Levine B. Cell biology: autophagy and cancer. Nature 2007; 446:745-7; PMID:17429391; http://dx.doi.org/10.1038/446745a
  • Eskelinen EL. The dual role of autophagy in cancer. Curr Opin Pharmacol 2011; 11:294-300; PMID:21498118; http://dx.doi.org/10.1016/j.coph.2011.03.009
  • Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402:672-6; PMID:10604474; http://dx.doi.org/10.1038/45257
  • Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A 2003; 100:15077-82; PMID:14657337; http://dx.doi.org/10.1073/pnas.2436255100
  • Morselli E, Galluzzi L, Kepp O, Marino G, Michaud M, Vitale I, Maiuri MC, Kroemer G. Oncosuppressive functions of autophagy. Antioxid Redox Signal 2011; 14:2251-69; PMID:20712403; http://dx.doi.org/10.1089/ars.2010.3478
  • Ma XH, Piao S, Wang D, McAfee QW, Nathanson KL, Lum JJ, Li LZ, Amaravadi RK. Measurements of tumor cell autophagy predict invasiveness, resistance to chemotherapy, and survival in melanoma. Clin Cancer Res 2011; 17:3478-89; PMID:21325076; http://dx.doi.org/10.1158/1078-0432.CCR-10-2372
  • Romano S, D'Angelillo A, Pacelli R, Staibano S, De Luna E, Bisogni R, Eskelinen EL, Mascolo M, Cali G, Arra C, et al. Role of FK506-binding protein 51 in the control of apoptosis of irradiated melanoma cells. Cell Death Differ 2010; 17:145-57; PMID:19696786; http://dx.doi.org/10.1038/cdd.2009.115
  • Marino ML, Fais S, Djavaheri-Mergny M, Villa A, Meschini S, Lozupone F, Venturi G, Della Mina P, Pattingre S, Rivoltini L, et al. Proton pump inhibition induces autophagy as a survival mechanism following oxidative stress in human melanoma cells. Cell Death Dis 2010; 1:e87; PMID:21368860; http://dx.doi.org/10.1038/cddis.2010.67
  • Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, Herman B, Levine B. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol 1998; 72:8586-96; PMID:9765397
  • Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122:927-39; PMID:16179260; http://dx.doi.org/10.1016/j.cell.2005.07.002
  • Pattingre S, Levine B. Bcl-2 inhibition of autophagy: a new route to cancer? Cancer Res 2006; 66:2885-8; PMID:16540632; http://dx.doi.org/10.1158/0008-5472.CAN-05-4412
  • Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007; 26:1749-60; PMID:17347651; http://dx.doi.org/10.1038/sj.emboj.7601623
  • Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8:741-52; PMID:17717517; http://dx.doi.org/10.1038/nrm2239
  • Levine B, Abrams J. p53: The Janus of autophagy? Nat Cell Biol 2008; 10:637-9; PMID:18521069; http://dx.doi.org/10.1038/ncb0608-637
  • Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri-Mergny M, D'Amelio M, Criollo A, Morselli E, Zhu C, Harper F, et al. Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 2008; 10:676-87; PMID:18454141; http://dx.doi.org/10.1038/ncb1730
  • Feng Z, Zhang H, Levine AJ, Jin S. The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci U S A 2005; 102:8204-9; PMID:15928081; http://dx.doi.org/10.1073/pnas.0502857102
  • Abida WM, Gu W. p53-Dependent and p53-independent activation of autophagy by ARF. Cancer Res 2008; 68:352-7; PMID:18199527; http://dx.doi.org/10.1158/0008-5472.CAN-07-2069
  • Maiuri MC, Galluzzi L, Morselli E, Kepp O, Malik SA, Kroemer G. Autophagy regulation by p53. Curr Opin Cell Biol 2010; 22:181-5; PMID:20044243; http://dx.doi.org/10.1016/j.ceb.2009.12.001
  • Fornace AJ, Jr., Alamo I, Jr., Hollander MC. DNA damage-inducible transcripts in mammalian cells. Proc Natl Acad Sci U S A 1988; 85:8800-4; PMID:3194391; http://dx.doi.org/10.1073/pnas.85.23.8800
  • Papathanasiou MA, Kerr NC, Robbins JH, McBride OW, Alamo I, Jr., Barrett SF, Hickson ID, Fornace AJ, Jr. Induction by ionizing radiation of the gadd45 gene in cultured human cells: lack of mediation by protein kinase C. Mol Cell Biol 1991; 11:1009-16; PMID:1990262; http://dx.doi.org/10.1128/MCB.11.2.1009
  • Kastan MB, Zhan Q, el-Deiry WS, Carrier F, Jacks T, Walsh WV, Plunkett BS, Vogelstein B, Fornace AJ, Jr. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 1992; 71:587-97; PMID:1423616; http://dx.doi.org/10.1016/0092-8674(92)90593-2
  • Zhan Q, Bae I, Kastan MB, Fornace AJ, Jr. The p53-dependent gamma-ray response of GADD45. Cancer Res 1994; 54:2755-60; PMID:8168107
  • Zhan Q, Chen IT, Antinore MJ, Fornace AJ, Jr. Tumor suppressor p53 can participate in transcriptional induction of the GADD45 promoter in the absence of direct DNA binding. Mol Cell Biol 1998; 18:2768-78; PMID:9566896; http://dx.doi.org/10.1128/MCB.18.5.2768
  • Zhan Q, Fan S, Smith ML, Bae I, Yu K, Alamo I, Jr., O'Connor PM, Fornace AJ, Jr. Abrogation of p53 function affects gadd gene responses to DNA base-damaging agents and starvation. DNA Cell Biol 1996; 15:805-15; PMID:8892753; http://dx.doi.org/10.1089/dna.1996.15.805
  • Jin S, Tong T, Fan W, Fan F, Antinore MJ, Zhu X, Mazzacurati L, Li X, Petrik KL, Rajasekaran B, et al. GADD45-induced cell cycle G2-M arrest associates with altered subcellular distribution of cyclin B1 and is independent of p38 kinase activity. Oncogene 2002; 21:8696-704; PMID:12483522; http://dx.doi.org/10.1038/sj.onc.1206034
  • Tong T, Ji J, Jin S, Li X, Fan W, Song Y, Wang M, Liu Z, Wu M, Zhan Q. Gadd45a expression induces Bim dissociation from the cytoskeleton and translocation to mitochondria. Mol Cell Biol 2005; 25:4488-500; PMID:15899854; http://dx.doi.org/10.1128/MCB.25.11.4488-4500.2005
  • Carrier F, Georgel PT, Pourquier P, Blake M, Kontny HU, Antinore MJ, Gariboldi M, Myers TG, Weinstein JN, Pommier Y, et al. Gadd45, a p53-responsive stress protein, modifies DNA accessibility on damaged chromatin. Mol Cell Biol 1999; 19:1673-85; PMID:10022855; http://dx.doi.org/10.1128/MCB.19.3.1673
  • Yang F, Zhang W, Li D, Zhan Q. Gadd45a suppresses tumor angiogenesis via inhibition of the mTOR/STAT3 protein pathway. J Biol Chem 2013; 288:6552-60; PMID:23329839; http://dx.doi.org/10.1074/jbc.M112.418335
  • Wang W, Huper G, Guo Y, Murphy SK, Olson JA, Jr., Marks JR. Analysis of methylation-sensitive transcriptome identifies GADD45a as a frequently methylated gene in breast cancer. Oncogene 2005; 24:2705-14; PMID:15735726; http://dx.doi.org/10.1038/sj.onc.1208464
  • Yamasawa K, Nio Y, Dong M, Yamaguchi K, Itakura M. Clinicopathological significance of abnormalities in Gadd45 expression and its relationship to p53 in human pancreatic cancer. Clin Cancer Res 2002; 8:2563-9; PMID:12171884
  • Ramachandran K, Gopisetty G, Gordian E, Navarro L, Hader C, Reis IM, Schulz WA, Singal R. Methylation-mediated repression of GADD45alpha in prostate cancer and its role as a potential therapeutic target. Cancer Res 2009; 69:1527-35; PMID:19190346; http://dx.doi.org/10.1158/0008-5472.CAN-08-3609
  • Hollander MC, Kovalsky O, Salvador JM, Kim KE, Patterson AD, Haines DC, Fornace AJ, Jr. Dimethylbenzanthracene carcinogenesis in Gadd45a-null mice is associated with decreased DNA repair and increased mutation frequency. Cancer Res 2001; 61:2487-91; PMID:11289119
  • Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
  • 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
  • Xu Y, Tian C, Wang SB, Xie WL, Guo Y, Zhang J, Shi Q, Chen C, Dong XP. Activation of the macroautophagic system in scrapie-infected experimental animals and human genetic prion diseases. Autophagy 2012; 8:1604-20; PMID:22874564; http://dx.doi.org/10.4161/auto.21482
  • Cao Y, Wang Y, Abi Saab WF, Yang F, Pessin JE, Backer JM. NRBF2 regulates macroautophagy as a component of Vps34 Complex I. Biochem J 2014; 461:315-22; PMID:24785657; http://dx.doi.org/10.1042/BJ20140515
  • Itakura E, Kishi C, Inoue K, Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 2008; 19:5360-72; PMID:18843052; http://dx.doi.org/10.1091/mbc.E08-01-0080
  • Funderburk SF, Wang QJ, Yue Z. The Beclin 1-VPS34 complex–at the crossroads of autophagy and beyond. Trends Cell Biol 2010; 20:355-62; PMID:20356743; http://dx.doi.org/10.1016/j.tcb.2010.03.002
  • Tamura RE, de Vasconcellos JF, Sarkar D, Libermann TA, Fisher PB, Zerbini LF. GADD45 proteins: central players in tumorigenesis. Curr Mol Med 2012; 12:634-51; PMID:22515981; http://dx.doi.org/10.2174/156652412800619978
  • Harkin DP, Bean JM, Miklos D, Song YH, Truong VB, Englert C, Christians FC, Ellisen LW, Maheswaran S, Oliner JD, et al. Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1. Cell 1999; 97:575-86; PMID:10367887; http://dx.doi.org/10.1016/S0092-8674(00)80769-2
  • Hocker R, Walker A, Schmitz I. Inhibition of autophagy through MAPK14-mediated phosphorylation of ATG5. Autophagy 2013; 9:426-8; PMID:23235332; http://dx.doi.org/10.4161/auto.22924
  • Keil E, Hocker R, Schuster M, Essmann F, Ueffing N, Hoffman B, Liebermann DA, Pfeffer K, Schulze-Osthoff K, Schmitz I. Phosphorylation of Atg5 by the Gadd45beta-MEKK4-p38 pathway inhibits autophagy. Cell Death Differ 2013; 20:321-32; PMID:23059785; http://dx.doi.org/10.1038/cdd.2012.129
  • Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature 2001; 411:342-8; PMID:11357141; http://dx.doi.org/10.1038/35077213
  • Kerr JF, Winterford CM, Harmon BV. Apoptosis. Its significance in cancer and cancer therapy. Cancer 1994; 73:2013-26; PMID:8156506; http://dx.doi.org/10.1002/1097-0142(19940415)73:8%3c2013::AID-CNCR2820730802%3e3.0.CO;2-J
  • Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005; 5:726-34; PMID:16148885; http://dx.doi.org/10.1038/nrc1692

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.