Local Mitochondrial-Endolysosomal Microfusion Cleaves Voltage-Dependent Anion Channel 1 To Promote Survival in Hypoxia

REFERENCES

• Brahimi-Horn MC, Bellot G, Pouyssegur J. 2011. Hypoxia and energetic tumour metabolism. Curr Opin Genet Dev 21:67–72. http://dx.doi.org/10.1016/j.gde.2010.10.006.
   PubMed Web of Science ®Google Scholar
• Marino G, Niso-Santano M, Baehrecke EH, Kroemer G. 2014. Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol 15:81–94. http://dx.doi.org/10.1038/nrm3735.
   PubMed Web of Science ®Google Scholar
• Boland ML, Chourasia AH, Macleod KF. 2013. Mitochondrial dysfunction in cancer. Front Oncol 3:292. http://dx.doi.org/10.3389/fonc.2013.00292.
   PubMedGoogle Scholar
• Friedman JR, Nunnari J. 2014. Mitochondrial form and function. Nature 505:335–343. http://dx.doi.org/10.1038/nature12985.
   PubMed Web of Science ®Google Scholar
• Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, Gonzalez FJ, Semenza GL. 2008. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 283:10892–10903. http://dx.doi.org/10.1074/jbc.M800102200.
   PubMed Web of Science ®Google Scholar
• Chiche J, Rouleau M, Gounon P, Brahimi-Horn MC, Pouyssegur J, Mazure NM. 2010. Hypoxic enlarged mitochondria protect cancer cells from apoptotic stimuli. J Cell Physiol 222:648–657. http://dx.doi.org/10.1002/jcp.21984.
   PubMed Web of Science ®Google Scholar
• Ding WX, Guo F, Ni HM, Bockus A, Manley S, Stolz DB, Eskelinen EL, Jaeschke H, Yin XM. 2012. Parkin and mitofusins reciprocally regulate mitophagy and mitochondrial spheroid formation. J Biol Chem 287:42379–42388. http://dx.doi.org/10.1074/jbc.M112.413682.
   PubMed Web of Science ®Google Scholar
• Gomes LC, Di Benedetto G, Scorrano L. 2011. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 13:589–598. http://dx.doi.org/10.1038/ncb2220.
   PubMed Web of Science ®Google Scholar
• Rambold AS, Kostelecky B, Elia N, Lippincott-Schwartz J. 2011. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci U S A 108:10190–10195. http://dx.doi.org/10.1073/pnas.1107402108.
   PubMed Web of Science ®Google Scholar
• Tondera D, Grandemange S, Jourdain A, Karbowski M, Mattenberger Y, Herzig S, Da Cruz S, Clerc P, Raschke I, Merkwirth C, Ehses S, Krause F, Chan DC, Alexander C, Bauer C, Youle R, Langer T, Martinou JC. 2009. SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J 28:1589–1600. http://dx.doi.org/10.1038/emboj.2009.89.
   PubMed Web of Science ®Google Scholar
• Wappler EA, Institoris A, Dutta S, Katakam PV, Busija DW. 2013. Mitochondrial dynamics associated with oxygen-glucose deprivation in rat primary neuronal cultures. PLoS One 8:e63206. http://dx.doi.org/10.1371/journal.pone.0063206.
   PubMedGoogle Scholar
• Brahimi-Horn MC, Ben-Hail D, Ilie M, Gounon P, Rouleau M, Hofman V, Doyen J, Mari B, Shoshan-Barmatz V, Hofman P, Pouyssegur J, Mazure NM. 2012. Expression of a truncated active form of VDAC1 in lung cancer associates with hypoxic cell survival and correlates with progression to chemotherapy resistance. Cancer Res 72:2140–2150. http://dx.doi.org/10.1158/0008-5472.CAN-11-3940.
   PubMed Web of Science ®Google Scholar
• Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, Arbel N. 2010. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31:227–285. http://dx.doi.org/10.1016/j.mam.2010.03.002.
   PubMed Web of Science ®Google Scholar
• De Stefani D, Bononi A, Romagnoli A, Messina A, De Pinto V, Pinton P, Rizzuto R. 2012. VDAC1 selectively transfers apoptotic Ca2+ signals to mitochondria. Cell Death Differ 19:267–273. http://dx.doi.org/10.1038/cdd.2011.92.
   PubMed Web of Science ®Google Scholar
• Weisthal S, Keinan N, Ben-Hail D, Arif T, Shoshan-Barmatz V. 2014. Ca-mediated regulation of VDAC1 expression levels is associated with cell death induction. Biochim Biophys Acta 1843:2270–2281. http://dx.doi.org/10.1016/j.bbamcr.2014.03.021.
   PubMed Web of Science ®Google Scholar
• Berkers CR, Maddocks OD, Cheung EC, Mor I, Vousden KH. 2013. Metabolic regulation by p53 family members. Cell Metab 18:617–633. http://dx.doi.org/10.1016/j.cmet.2013.06.019.
   PubMed Web of Science ®Google Scholar
• Gottlieb E. 2011. p53 guards the metabolic pathway less travelled. Nat Cell Biol 13:195–197. http://dx.doi.org/10.1038/ncb2177.
   PubMedGoogle Scholar
• Bornstein C, Brosh R, Molchadsky A, Madar S, Kogan-Sakin I, Goldstein I, Chakravarti D, Flores ER, Goldfinger N, Sarig R, Rotter V. 2011. SPATA18, a spermatogenesis-associated gene, is a novel transcriptional target of p53 and p63. Mol Cell Biol 31:1679–1689. http://dx.doi.org/10.1128/MCB.01072-10.
   PubMed Web of Science ®Google Scholar
• Nakamura Y, Kitamura N, Shinogi D, Yoshida M, Goda O, Murai R, Kamino H, Arakawa H. 2012. BNIP3 and NIX mediate Mieap-induced accumulation of lysosomal proteins within mitochondria. PLoS One 7:e30767. http://dx.doi.org/10.1371/journal.pone.0030767.
   PubMed Web of Science ®Google Scholar
• Miyamoto Y, Kitamura N, Nakamura Y, Futamura M, Miyamoto T, Yoshida M, Ono M, Ichinose S, Arakawa H. 2011. Possible existence of lysosome-like organella within mitochondria and its role in mitochondrial quality control. PLoS One 6:e16054. http://dx.doi.org/10.1371/journal.pone.0016054.
   PubMed Web of Science ®Google Scholar
• Elbaz-Alon Y, Rosenfeld-Gur E, Shinder V, Futerman AH, Geiger T, Schuldiner M. 2014. A dynamic interface between vacuoles and mitochondria in yeast. Dev Cell 30:95–102. http://dx.doi.org/10.1016/j.devcel.2014.06.007.
   PubMed Web of Science ®Google Scholar
• Honscher C, Mari M, Auffarth K, Bohnert M, Griffith J, Geerts W, van der Laan M, Cabrera M, Reggiori F, Ungermann C. 2014. Cellular metabolism regulates contact sites between vacuoles and mitochondria. Dev Cell 30:86–94. http://dx.doi.org/10.1016/j.devcel.2014.06.006.
   PubMed Web of Science ®Google Scholar
• Sheftel AD, Zhang AS, Brown C, Shirihai OS, Ponka P. 2007. Direct interorganellar transfer of iron from endosome to mitochondrion. Blood 110:125–132. http://dx.doi.org/10.1182/blood-2007-01-068148.
   PubMed Web of Science ®Google Scholar
• Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ. 2010. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 8:e1000298. http://dx.doi.org/10.1371/journal.pbio.1000298.
   PubMed Web of Science ®Google Scholar
• Bellot G, Garcia-Medina R, Gounon P, Chiche J, Roux D, Pouyssegur J, Mazure NM. 2009. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 29:2570–2581. http://dx.doi.org/10.1128/MCB.00166-09.
   PubMed Web of Science ®Google Scholar
• Richard DE, Berra E, Gothie E, Roux D, Pouyssegur J. 1999. p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1alpha (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J Biol Chem 274:32631–32637. http://dx.doi.org/10.1074/jbc.274.46.32631.
   PubMed Web of Science ®Google Scholar
• Keller A, Nesvizhskii AI, Kolker E, Aebersold R. 2002. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74:5383–5392. http://dx.doi.org/10.1021/ac025747h.
   PubMed Web of Science ®Google Scholar
• Nesvizhskii AI, Keller A, Kolker E, Aebersold R. 2003. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75:4646–4658. http://dx.doi.org/10.1021/ac0341261.
   PubMed Web of Science ®Google Scholar
• Djouder N, Metzler SC, Schmidt A, Wirbelauer C, Gstaiger M, Aebersold R, Hess D, Krek W. 2007. S6K1-mediated disassembly of mitochondrial URI/PP1gamma complexes activates a negative feedback program that counters S6K1 survival signaling. Mol Cell 28:28–40. http://dx.doi.org/10.1016/j.molcel.2007.08.010.
   PubMed Web of Science ®Google Scholar
• Hiller S, Garces RG, Malia TJ, Orekhov VY, Colombini M, Wagner G. 2008. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321:1206–1210. http://dx.doi.org/10.1126/science.1161302.
   PubMed Web of Science ®Google Scholar
• Varnier A, Kermarrec F, Blesneac I, Moreau C, Liguori L, Lenormand JL, Picollet-D'hahan N. 2010. A simple method for the reconstitution of membrane proteins into giant unilamellar vesicles. J Membr Biol 233:85–92. http://dx.doi.org/10.1007/s00232-010-9227-8.
   PubMed Web of Science ®Google Scholar
• Li DN, Matthews SP, Antoniou AN, Mazzeo D, Watts C. 2003. Multistep autoactivation of asparaginyl endopeptidase in vitro and in vivo. J Biol Chem 278:38980–38990. http://dx.doi.org/10.1074/jbc.M305930200.
   PubMed Web of Science ®Google Scholar
• Travis WD, Brambilla E, Müller-Hermelink HK, Harris CC(ed). 2004. Pathology and genetics of tumours of the lung, pleura, thymus and heart. WHO histological classification of tumors of the lung. World Health Organization, Geneva, Switzerland.
   Google Scholar
• Mountain CF. 1997. Revisions in the international system for staging lung cancer. Chest 111:1710–1717. http://dx.doi.org/10.1378/chest.111.6.1710.
   PubMed Web of Science ®Google Scholar
• Hietanen S, Lain S, Krausz E, Blattner C, Lane DP. 2000. Activation of p53 in cervical carcinoma cells by small molecules. Proc Natl Acad Sci U S A 97:8501–8506. http://dx.doi.org/10.1073/pnas.97.15.8501.
   PubMed Web of Science ®Google Scholar
• Candi E, Agostini M, Melino G, Bernassola F. 2014. How the TP53 family proteins TP63 and TP73 contribute to tumorigenesis: regulators and effectors. Hum Mutat 35:702–714. http://dx.doi.org/10.1002/humu.22523.
   PubMed Web of Science ®Google Scholar
• Yoshikawa H, Nagashima M, Khan MA, McMenamin MG, Hagiwara K, Harris CC. 1999. Mutational analysis of p73 and p53 in human cancer cell lines. Oncogene 18:3415–3421. http://dx.doi.org/10.1038/sj.onc.1202677.
   PubMedGoogle Scholar
• Barth S, Glick D, Macleod KF. 2010. Autophagy: assays and artifacts. J Pathol 221:117–124. http://dx.doi.org/10.1002/path.2694.
   PubMed Web of Science ®Google Scholar
• Malka F, Guillery O, Cifuentes-Diaz C, Guillou E, Belenguer P, Lombes A, Rojo M. 2005. Separate fusion of outer and inner mitochondrial membranes. EMBO Rep 6:853–859. http://dx.doi.org/10.1038/sj.embor.7400488.
   PubMed Web of Science ®Google Scholar
• Rong Y, Liu M, Ma L, Du W, Zhang H, Tian Y, Cao Z, Li Y, Ren H, Zhang C, Li L, Chen S, Xi J, Yu L. 2012. Clathrin and phosphatidylinositol-4,5-bisphosphate regulate autophagic lysosome reformation. Nat Cell Biol 14:924–934. http://dx.doi.org/10.1038/ncb2557.
   PubMed Web of Science ®Google Scholar
• Bensaad K, Vousden KH. 2007. p53: new roles in metabolism. Trends Cell Biol 17:286–291. http://dx.doi.org/10.1016/j.tcb.2007.04.004.
   PubMed Web of Science ®Google Scholar
• Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM. 2012. p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 149:1536–1548. http://dx.doi.org/10.1016/j.cell.2012.05.014.
   PubMed Web of Science ®Google Scholar
• McLelland GL, Soubannier V, Chen CX, McBride HM, Fon EA. 2014. Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J 33:282–295. http://dx.doi.org/10.1002/embj.201385902.
   PubMed Web of Science ®Google Scholar
• Soubannier V, McLelland GL, Zunino R, Braschi E, Rippstein P, Fon EA, McBride HM. 2012. A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr Biol 22:135–141. http://dx.doi.org/10.1016/j.cub.2011.11.057.
   PubMed Web of Science ®Google Scholar
• Maschalidi S, Hassler S, Blanc F, Sepulveda FE, Tohme M, Chignard M, van Endert P, Si-Tahar M, Descamps D, Manoury B. 2012. Asparagine endopeptidase controls anti-influenza virus immune responses through TLR7 activation. PLoS Pathog 8:e1002841. http://dx.doi.org/10.1371/journal.ppat.1002841.
   PubMedGoogle Scholar
• Guo P, Zhu Z, Sun Z, Wang Z, Zheng X, Xu H. 2013. Expression of legumain correlates with prognosis and metastasis in gastric carcinoma. PLoS One 8:e73090. http://dx.doi.org/10.1371/journal.pone.0073090.
   PubMedGoogle Scholar
• Wang L, Chen S, Zhang M, Li N, Chen Y, Su W, Liu Y, Lu D, Li S, Yang Y, Li Z, Stupack D, Qu P, Hu H, Xiang R. 2012. Legumain: a biomarker for diagnosis and prognosis of human ovarian cancer. J Cell Biochem 113:2679–2686. http://dx.doi.org/10.1002/jcb.24143.
   PubMedGoogle Scholar
• Basurto-Islas G, Grundke-Iqbal I, Tung YC, Liu F, Iqbal K. 2013. Activation of asparaginyl endopeptidase leads to Tau hyperphosphorylation in Alzheimer disease. J Biol Chem 288:17495–17507. http://dx.doi.org/10.1074/jbc.M112.446070.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Song M, Liu X, Kang SS, Kwon IS, Duong DM, Seyfried NT, Hu WT, Liu Z, Wang JZ, Cheng L, Sun YE, Yu SP, Levey AI, Ye K. 2014. Cleavage of tau by asparagine endopeptidase mediates the neurofibrillary pathology in Alzheimer's disease. Nat Med 20:1254–1262. http://dx.doi.org/10.1038/nm.3700.
   PubMed Web of Science ®Google Scholar
• Yamane T, Murao S, Kato-Ose I, Kashima L, Yuguchi M, Kozuka M, Takeuchi K, Ogita H, Ohkubo I, Ariga H. 2013. Transcriptional regulation of the legumain gene by p53 in HCT116 cells. Biochem Biophys Res Commun 438:613–618. http://dx.doi.org/10.1016/j.bbrc.2013.08.007.
   PubMed Web of Science ®Google Scholar
• Halfon S, Patel S, Vega F, Zurawski S, Zurawski G. 1998. Autocatalytic activation of human legumain at aspartic acid residues. FEBS Lett 438:114–118. http://dx.doi.org/10.1016/S0014-5793(98)01281-2.
   PubMedGoogle Scholar