Hyperosmotic Stress Induces Unconventional Autophagy Independent of the Ulk1 Complex

REFERENCES

• Burg MB, Ferraris JD, Dmitrieva NI. 2007. Cellular response to hyperosmotic stresses. Physiol Rev 87:1441–1474. https://doi.org/10.1152/physrev.00056.2006.
   PubMed Web of Science ®Google Scholar
• Hoffmann EK, Lambert IH, Pedersen SF. 2009. Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193–277. https://doi.org/10.1152/physrev.00037.2007.
   PubMed Web of Science ®Google Scholar
• Houpt TR. 1991. Patterns of duodenal osmolality in young pigs fed solid food. Am J Physiol 261:R569–R575. https://doi.org/10.1152/ajpregu.1991.261.3.R569.
   PubMedGoogle Scholar
• Stookey JD. 2005. High prevalence of plasma hypertonicity among community-dwelling older adults: results from NHANES III. J Am Diet Assoc 105:1231–1239. https://doi.org/10.1016/j.jada.2005.05.003.
   PubMedGoogle Scholar
• Jantzen JP. 2007. Prevention and treatment of intracranial hypertension. Best Pract Res Clin Anaesthesiol 21:517–538. https://doi.org/10.1016/j.bpa.2007.09.001.
   PubMed Web of Science ®Google Scholar
• Whitmarsh AJ. 2010. A central role for p38 MAPK in the early transcriptional response to stress. BMC Biol 8:47. https://doi.org/10.1186/1741-7007-8-47.
   PubMed Web of Science ®Google Scholar
• Coulombe P, Meloche S. 2007. Atypical mitogen-activated protein kinases: structure, regulation and functions. Biochim Biophys Acta 1773:1376–1387. https://doi.org/10.1016/j.bbamcr.2006.11.001.
   PubMed Web of Science ®Google Scholar
• Dmitrieva NI, Burg MB, Ferraris JD. 2005. DNA damage and osmotic regulation in the kidney. Am J Physiol Renal Physiol 289:F2–F7. https://doi.org/10.1152/ajprenal.00041.2005.
   PubMed Web of Science ®Google Scholar
• Nunes P, Roth I, Meda P, Feraille E, Brown D, Hasler U. 2015. Ionic imbalance, in addition to molecular crowding, abates cytoskeletal dynamics and vesicle motility during hypertonic stress. Proc Natl Acad Sci U S A 112:E3104–E3113. https://doi.org/10.1073/pnas.1421290112.
   PubMed Web of Science ®Google Scholar
• Nunes P, Ernandez T, Roth I, Qiao X, Strebel D, Bouley R, Charollais A, Ramadori P, Foti M, Meda P, Feraille E, Brown D, Hasler U. 2013. Hypertonic stress promotes autophagy and microtubule-dependent autophagosomal clusters. Autophagy 9:550–567. https://doi.org/10.4161/auto.23662.
   PubMed Web of Science ®Google Scholar
• Di Ciano C, Nie Z, Szaszi K, Lewis A, Uruno T, Zhan X, Rotstein OD, Mak A, Kapus A. 2002. Osmotic stress-induced remodeling of the cortical cytoskeleton. Am J Physiol Cell Physiol 283:C850–C865. https://doi.org/10.1152/ajpcell.00018.2002.
   PubMed Web of Science ®Google Scholar
• Bustamante M, Roger F, Bochaton-Piallat ML, Gabbiani G, Martin PY, Feraille E. 2003. Regulatory volume increase is associated with p38 kinase-dependent actin cytoskeleton remodeling in rat kidney MTAL. Am J Physiol Renal Physiol 285:F336–F347. https://doi.org/10.1152/ajprenal.00003.2003.
   PubMed Web of Science ®Google Scholar
• Hansen SH, Sandvig K, van Deurs B. 1993. Clathrin and HA2 adaptors: effects of potassium depletion, hypertonic medium, and cytosol acidification. J Cell Biol 121:61–72. https://doi.org/10.1083/jcb.121.1.61.
   PubMed Web of Science ®Google Scholar
• Hasler U, Nunes P, Bouley R, Lu HA, Matsuzaki T, Brown D. 2008. Acute hypertonicity alters aquaporin-2 trafficking and induces a MAPK-dependent accumulation at the plasma membrane of renal epithelial cells. J Biol Chem 283:26643–26661. https://doi.org/10.1074/jbc.M801071200.
   PubMedGoogle Scholar
• Heuser JE, Anderson RG. 1989. Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108:389–400. https://doi.org/10.1083/jcb.108.2.389.
   PubMed Web of Science ®Google Scholar
• Burkewitz K, Choe K, Strange K. 2011. Hypertonic stress induces rapid and widespread protein damage in C. elegans. Am J Physiol Cell Physiol 301:C566–C576. https://doi.org/10.1152/ajpcell.00030.2011.
   PubMed Web of Science ®Google Scholar
• Lamitina T, Huang CG, Strange K. 2006. Genome-wide RNAi screening identifies protein damage as a regulator of osmoprotective gene expression. Proc Natl Acad Sci U S A 103:12173–12178. https://doi.org/10.1073/pnas.0602987103.
   PubMed Web of Science ®Google Scholar
• Moronetti Mazzeo LE, Dersh D, Boccitto M, Kalb RG, Lamitina T. 2012. Stress and aging induce distinct polyQ protein aggregation states. Proc Natl Acad Sci U S A 109:10587–10592. https://doi.org/10.1073/pnas.1108766109.
   PubMed Web of Science ®Google Scholar
• Lee SH, Park Y, Yoon SK, Yoon JB. 2010. Osmotic stress inhibits proteasome by p38 MAPK-dependent phosphorylation. J Biol Chem 285:41280–41289. https://doi.org/10.1074/jbc.M110.182188.
   PubMed Web of Science ®Google Scholar
• Pena-Oyarzun D, Troncoso R, Kretschmar C, Hernando C, Budini M, Morselli E, Lavandero S, Criollo A. 2017. Hyperosmotic stress stimulates autophagy via polycystin-2. Oncotarget 8:55984–55997. https://doi.org/10.18632/oncotarget.18995.
   PubMedGoogle Scholar
• Galluzzi L, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM, Cecconi F, Choi AM, Chu CT, Codogno P, Colombo MI, Cuervo AM, Debnath J, Deretic V, Dikic I, Eskelinen E-L, Fimia GM, Fulda S, Gewirtz DA, Green DR, Hansen M, Harper JW, Jäättelä M, Johansen T, Juhasz G, Kimmelman AC, Kraft C, Ktistakis NT, Kumar S, Levine B, Lopez-Otin C, Madeo F, Martens S, Martinez J, Melendez A, Mizushima N, Münz C, Murphy LO, Penninger JM, Piacentini M, Reggiori F, Rubinsztein DC, Ryan KM, Santambrogio L, Scorrano L, Simon AK, Simon H-U, Simonsen A, Tavernarakis N, Tooze SA, Yoshimori T, Yuan J, Yue Z, Zhong Q, Kroemer G. 2017. Molecular definitions of autophagy and related processes. EMBO J 36:1811–1836. https://doi.org/10.15252/embj.201796697.
   PubMed Web of Science ®Google Scholar
• Hawley SA, Ross FA, Chevtzoff C, Green KA, Evans A, Fogarty S, Towler MC, Brown LJ, Ogunbayo OA, Evans AM, Hardie DG. 2010. Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab 11:554–565. https://doi.org/10.1016/j.cmet.2010.04.001.
   PubMed Web of Science ®Google Scholar
• Yuan HX, Wang Z, Yu FX, Li F, Russell RC, Jewell JL, Guan KL. 2015. NLK phosphorylates Raptor to mediate stress-induced mTORC1 inhibition. Genes Dev 29:2362–2376. https://doi.org/10.1101/gad.265116.115.
   PubMed Web of Science ®Google Scholar
• Kwak D, Choi S, Jeong H, Jang JH, Lee Y, Jeon H, Lee MN, Noh J, Cho K, Yoo JS, Hwang D, Suh PG, Ryu SH. 2012. Osmotic stress regulates mammalian target of rapamycin (mTOR) complex 1 via c-Jun N-terminal kinase (JNK)-mediated Raptor protein phosphorylation. J Biol Chem 287:18398–18407. https://doi.org/10.1074/jbc.M111.326538.
   PubMedGoogle Scholar
• Polson HE, de Lartigue J, Rigden DJ, Reedijk M, Urbe S, Clague MJ, Tooze SA. 2010. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6:506–522. https://doi.org/10.4161/auto.6.4.11863.
   PubMed Web of Science ®Google Scholar
• Kaizuka T, Mizushima N. 2016. Atg13 is essential for autophagy and cardiac development in mice. Mol Cell Biol 36:585–595. https://doi.org/10.1128/MCB.01005-15.
   PubMed Web of Science ®Google Scholar
• Hara T, Takamura A, Kishi C, Iemura S, Natsume T, Guan JL, Mizushima N. 2008. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 181:497–510. https://doi.org/10.1083/jcb.200712064.
   PubMed Web of Science ®Google Scholar
• Han YK, Kim YG, Kim JY, Lee GM. 2010. Hyperosmotic stress induces autophagy and apoptosis in recombinant Chinese hamster ovary cell culture. Biotechnol Bioeng 105:1187–1192. https://doi.org/10.1002/bit.22643.
   PubMed Web of Science ®Google Scholar
• Jiang LB, Cao L, Yin XF, Yasen M, Yishake M, Dong J, Li XL. 2015. Activation of autophagy via Ca(2+)-dependent AMPK/mTOR pathway in rat notochordal cells is a cellular adaptation under hyperosmotic stress. Cell Cycle 14:867–879. https://doi.org/10.1080/15384101.2015.1004946.
   PubMed Web of Science ®Google Scholar
• Papinski D, Kraft C. 2016. Regulation of autophagy by signaling through the Atg1/ULK1 complex. J Mol Biol 428:1725–1741. https://doi.org/10.1016/j.jmb.2016.03.030.
   PubMed Web of Science ®Google Scholar
• Wong PM, Puente C, Ganley IG, Jiang X. 2013. The ULK1 complex: sensing nutrient signals for autophagy activation. Autophagy 9:124–137. https://doi.org/10.4161/auto.23323.
   PubMed Web of Science ®Google Scholar
• Martinez J, Almendinger J, Oberst A, Ness R, Dillon CP, Fitzgerald P, Hengartner MO, Green DR. 2011. Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci U S A 108:17396–17401. https://doi.org/10.1073/pnas.1113421108.
   PubMed Web of Science ®Google Scholar
• Sanjuan MA, Dillon CP, Tait SW, Moshiach S, Dorsey F, Connell S, Komatsu M, Tanaka K, Cleveland JL, Withoff S, Green DR. 2007. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450:1253–1257. https://doi.org/10.1038/nature06421.
   PubMed Web of Science ®Google Scholar
• Cheong H, Lindsten T, Wu J, Lu C, Thompson CB. 2011. Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc Natl Acad Sci U S A 108:11121–11126. https://doi.org/10.1073/pnas.1107969108.
   PubMed Web of Science ®Google Scholar
• Mejlvang J, Olsvik H, Svenning S, Bruun JA, Abudu YP, Larsen KB, Brech A, Hansen TE, Brenne H, Hansen T, Stenmark H, Johansen T. 2018. Starvation induces rapid degradation of selective autophagy receptors by endosomal microautophagy. J Cell Biol 217:3640–3655. https://doi.org/10.1083/jcb.201711002.
   PubMed Web of Science ®Google Scholar
• Danieli A, Martens S. 2018. p62-mediated phase separation at the intersection of the ubiquitin-proteasome system and autophagy. J Cell Sci 131:jcs214304. https://doi.org/10.1242/jcs.214304.
   PubMed Web of Science ®Google Scholar
• Sun D, Wu R, Zheng J, Li P, Yu L. 2018. Polyubiquitin chain-induced p62 phase separation drives autophagic cargo segregation. Cell Res 28:405–415. https://doi.org/10.1038/s41422-018-0017-7.
   PubMed Web of Science ®Google Scholar
• Zaffagnini G, Savova A, Danieli A, Romanov J, Tremel S, Ebner M, Peterbauer T, Sztacho M, Trapannone R, Tarafder AK, Sachse C, Martens S. 2018. p62 filaments capture and present ubiquitinated cargos for autophagy. EMBO J 37:e98308. https://doi.org/10.15252/embj.201798308.
   Google Scholar
• Plescher M, Teleman AA, Demetriades C. 2015. TSC2 mediates hyperosmotic stress-induced inactivation of mTORC1. Sci Rep 5:13828. https://doi.org/10.1038/srep13828.
   PubMed Web of Science ®Google Scholar
• Reiling JH, Sabatini DM. 2006. Stress and mTORture signaling. Oncogene 25:6373–6383. https://doi.org/10.1038/sj.onc.1209889.
   PubMed Web of Science ®Google Scholar
• Ortells MC, Morancho B, Drews-Elger K, Viollet B, Laderoute KR, López-Rodríguez C, Aramburu J. 2012. Transcriptional regulation of gene expression during osmotic stress responses by the mammalian target of rapamycin. Nucleic Acids Res 40:4368–4384. https://doi.org/10.1093/nar/gks038.
   PubMed Web of Science ®Google Scholar
• Terada Y, Tomita K, Homma MK, Nonoguchi H, Yang T, Yamada T, Yuasa Y, Krebs EG, Sasaki S, Marumo F. 1994. Sequential activation of Raf-1 kinase, mitogen-activated protein (MAP) kinase kinase, MAP kinase, and S6 kinase by hyperosmolality in renal cells. J Biol Chem 269:31296–31301.
   PubMed Web of Science ®Google Scholar
• Gan B, Peng X, Nagy T, Alcaraz A, Gu H, Guan JL. 2006. Role of FIP200 in cardiac and liver development and its regulation of TNFalpha and TSC-mTOR signaling pathways. J Cell Biol 175:121–133. https://doi.org/10.1083/jcb.200604129.
   PubMed Web of Science ®Google Scholar