Hypertonic stress promotes autophagy and microtubule-dependent autophagosomal clusters

Autophagy

Volumn 9, Issue 4, 2013, Pages 550-567

  Nunes, Paula ^a,b   Ernandez, Thomas ^a   Roth, Isabelle ^a   Qiao, Xiaomu ^a   Strebel, Deborah ^a   Bouley, Richard ^b   Charollais, Anne ^a   Ramadori, Pierluigi ^a   Foti, Michelangelo ^a   Meda, Paolo ^a   Feraille, Eric ^a   Brown, Dennis ^b   Hasler, Udo ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Apoptosis; ATG12; Autophagy; Dynein; Golgi apparatus; Lysosome; MAP1LC3 LC3; MAPRE1 EB1; Microtubule; MTOC; Osmotic stress; Proteasome; Rapamycin; SQSTM1 p62; Tubulin; Ubiquitin

Indexed keywords

BAFILOMYCIN A1; CHLOROQUINE; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; RAPAMYCIN; SMALL INTERFERING RNA; TUBULIN; UBIQUITIN;

ANIMAL CELL; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CELL DEATH; CELL SURVIVAL; CENTROSOME; DEPOLYMERIZATION; GENE SILENCING; GOLGI COMPLEX; HYPEROSMOTIC STRESS; MAMMAL CELL; MICROTUBULE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

EID: 84877327062     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.23662     Document Type: Article

References (94)

1. Houpt TR. Patterns of duodenal osmolality in young pigs fed solid food. Am J Physiol 1991; 261:R569-75; PMID:1887946
2. Anjaria DJ, Mohr AM, Deitch EA. Haemorrhagic shock therapy. Expert Opin Pharmacother 2008; 9:901-11; PMID:18377334; http://dx.doi.org/10.1517/14656566. 9.6.901
3. Daviskas E, Anderson SD. Hyperosmolar agents and clearance of mucus in the diseased airway. J Aerosol Med 2006; 19:100-9; PMID:16551221; http://dx.doi.org/10.1089/jam.2006.19.100
4. Soupart A, Decaux G. Therapeutic recommendations for management of severe hyponatremia: Current concepts on pathogenesis and prevention of neurologic complications. Clin Nephrol 1996; 46:149-69; PMID:8879850
5. Alfieri RR, Petronini PG. Hyperosmotic stress response: Comparison with other cellular stresses. Pflugers Arch 2007; 454:173-85; PMID:17206446; http://dx.doi.org/10.1007/s00424-006-0195-x
6. Burg MB, Ferraris JD, Dmitrieva NI. Cellular response to hyperosmotic stresses. Physiol Rev 2007; 87:1441-74; PMID:17928589; http://dx.doi.org/10. 1152/physrev.00056.2006
7. Zhou HX, Rivas G, Minton AP. Macromolecular crowding and confinement: Biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 2008; 37:375-97; PMID:18573087; http://dx.doi.org/10.1146/annurev.bio- phys.37.032807.125817
8. Hoffmann EK, Lambert IH, Pedersen SF. Physiology of cell volume regulation in vertebrates. Physiol Rev 2009; 89:193-277; PMID:19126758; http://dx.doi.org/10.1152/physrev.00037.2007
9. Burkewitz K, Choe K, Strange K. Hypertonic stress induces rapid and widespread protein damage in C. elegans. Am J Physiol Cell Physiol 2011; 301:C566-76; PMID:21613604; http://dx.doi.org/10.1152/ajpcell. 00030.2011
10. Ellis RJ, Minton AP. Protein aggregation in crowded environments. Biol Chem 2006; 387:485-97; PMID:16740119; http://dx.doi.org/10.1515/BC.2006.064
11. Munishkina LA, Ahmad A, Fink AL, Uversky VN. Guiding protein aggregation with macromolecular crowding. Biochemistry 2008; 47:8993-9006; PMID:18665616; http://dx.doi.org/10.1021/bi8008399
12. Choe KP, Strange K. Genome-wide RNAi screen and in vivo protein aggregation reporters identify degradation of damaged proteins as an essential hypertonic stress response. Am J Physiol Cell Physiol 2008; 295:C1488-98; PMID:18829898; http://dx.doi.org/10.1152/ajpcell. 00450.2008
13. Goldberg AL. Protein degradation and protection against misfolded or damaged proteins. Nature 2003; 426:895-9; PMID:14685250; http://dx.doi.org/10. 1038/nature02263
14. Burman C, Ktistakis NT. Autophagosome formation in mammalian cells. Semin Immunopathol 2010; 32:397-413; PMID:20740284; http://dx.doi.org/10.1007/s00281- 010-0222-z
15. Levine B, Klionsky DJ. Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6:463-77; PMID:15068787; http://dx.doi.org/10.1016/S1534-5807(04)00099-1
16. Longatti A, Tooze SA. Vesicular trafficking and autophagosome formation. Cell Death Differ 2009; 16:956-65; PMID:19373247; http://dx.doi.org/10.1038/cdd. 2009.39
17. Yoshimori T. Autophagy: A regulated bulk degradation process inside cells. Biochem Biophys Res Commun 2004; 313:453-8; PMID:14684184; http://dx.doi.org/10.1016/j.bbrc.2003.07.023
18. Mariño G, Madeo F, Kroemer G. Autophagy for tissue homeostasis and neuroprotection. Curr Opin Cell Biol 2011; 23:198-206; PMID:21030235; http://dx.doi.org/10.1016/j.ceb.2010.10.001
19. Wong E, Cuervo AM. Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 2010; 13:805-11; PMID:20581817; http://dx.doi.org/10.1038/nn.2575
20. Kraft C, Peter M, Hofmann K. Selective autophagy: Ubiquitin-mediated recognition and beyond. Nat Cell Biol 2010; 12:836-41; PMID:20811356; http://dx.doi.org/10.1038/ncb0910-836
21. Shaid S, Brandts CH, Serve H, Dikic I. Ubiquitination and selective autophagy. Cell Death Differ 2013; 20:21-30; PMID:22722335; http://dx.doi.org/ 10.1038/cdd.2012.72
22. Kirkin V, Lamark T, Sou YS, Bjørkøy G, Nunn JL, Bruun JA, et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 2009; 33:505-16; PMID:19250911; http://dx.doi.org/10.1016/ j.molcel.2009.01.020
23. Carpentier JL, Sawano F, Geiger D, Gorden P, Perrelet A, Orci L. Potassium depletion and hypertonic medium reduce "non-coated" and clathrin-coated pit formation, as well as endocytosis through these two gates. J Cell Physiol 1989; 138:519-26; PMID:2466853; http://dx.doi.org/10.1002/jcp. 1041380311
24. Hansen SH, Sandvig K, van Deurs B. Clathrin and HA2 adaptors: Effects of potassium depletion, hypertonic medium, and cytosol acidification. J Cell Biol 1993; 121:61-72; PMID:8458873; http://dx.doi.org/10.1083/jcb.121.1.61
25. Hasler U, Nunes P, Bouley R, Lu HA, Matsuzaki T, Brown D. Acute hypertonicity alters aquaporin-2 trafficking and induces a MAPK-dependent accumulation at the plasma membrane of renal epithelial cells. J Biol Chem 2008; 283:26643-61; PMID:18664568; http://dx.doi.org/10.1074/jbc.M801071200
26. Heuser JE, Anderson RG. Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrincoated pit formation. J Cell Biol 1989; 108:389-400; PMID:2563728; http://dx.doi.org/10.1083/jcb.108.2.389
27. Zhou EH, Trepat X, Park CY, Lenormand G, Oliver MN, Mijailovich SM, et al. Universal behavior of the osmotically compressed cell and its analogy to the colloidal glass transition. Proc Natl Acad Sci U S A 2009; 106:10632-7; PMID:19520830
28. Jahreiss L, Menzies FM, Rubinsztein DC. The itinerary of autophagosomes: From peripheral formation to kissand-run fusion with lysosomes. Traffic 2008; 9:574-87; PMID:18182013; http://dx.doi.org/10.1111/j.1600-0854.2008.00701.x
29. Fass E, Shvets E, Degani I, Hirschberg K, Elazar Z. Microtubules support production of starvationinduced autophagosomes but not their targeting and fusion with lysosomes. J Biol Chem 2006; 281:36303-16; PMID:16963441; http://dx.doi.org/10.1074/jbc. M607031200
30. Ravikumar B, Acevedo-Arozena A, Imarisio S, Berger Z, Vacher C, O'Kane CJ, et al. Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat Genet 2005; 37:771-6; PMID:15980862; http://dx.doi.org/10.1038/ ng1591
31. Iwai K, Hori M, Kitabatake A, Kurihara H, Uchida K, Inoue M, et al. Disruption of microtubules as an early sign of irreversible ischemic injury. Immunohistochemical study of in situ canine hearts. Circ Res 1990; 67:694-706; PMID:1697795; http://dx.doi.org/10.1161/01.RES.67.3.694
32. Abbate M, Bonventre JV, Brown D. The microtubule network of renal epithelial cells is disrupted by ischemia and reperfusion. Am J Physiol 1994; 267:F971-8; PMID:7810705
33. Banan A, Choudhary S, Zhang Y, Fields JZ, Keshavarzian A. Oxidant-induced intestinal barrier disruption and its prevention by growth factors in a human colonic cell line: Role of the microtubule cytoskeleton. Free Radic Biol Med 2000; 28:727-38; PMID:10754268; http://dx.doi.org/10.1016/S0891-5849(00)00160-X
34. Inoue S. Effect of temperature on the birefringence of the mitotic spindle. Biol Bull 1952; 103:316
35. Inoue S. Organization and function of the mitotic spindle. In: Allen R, Kamiya N, eds. Primitive Motile Systems in Cell Biology. New-York: Academic Press, Inc, 1964
36. Rieder C, Bajer AS. Heat-induced reversible hexagonal packing of spindle microtubules. J Cell Biol 1977; 74:717-25; PMID:561787; http://dx.doi.org/10. 1083/jcb.74.3.717
37. Breton S, Brown D. Cold-induced microtubule disruption and relocalization of membrane proteins in kidney epithelial cells. J Am Soc Nephrol 1998; 9:155-66; PMID:9527391
38. Zaremba TG, Irwin RD. Effect of 60Co gamma irradiation on the polymerization of microtubules in vitro. Radiat Res 1977; 71:300-10; PMID:897069; http://dx.doi.org/10.2307/3574674
39. Hughes K, Forer A, Wilson P, Leggiadro C. Ultraviolet microbeam irradiation of microtubules in vitro. The action spectrum for local depolymerization of marginal band microtubules in vitro matches that for reducing birefringence of chromosomal spindle fibres in vivo. J Cell Sci 1988; 91:469-78; PMID:3076589
40. Han YK, Kim YG, Kim JY, Lee GM. Hyperosmotic stress induces autophagy and apoptosis in recombinant Chinese hamster ovary cell culture. Biotechnol Bioeng 2010; 105:1187-92; PMID:20014438
41. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-75; PMID:18188003
42. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140:313-26; PMID:20144757; http://dx.doi.org/10.1016/j. cell.2010.01.028
43. Chen D, Fan W, Lu Y, Ding X, Chen S, Zhong Q. A mammalian autophagosome maturation mechanism mediated by TECPR1 and the Atg12-Atg5 conjugate. Mol Cell 2012; 45:629-41; PMID:22342342; http://dx.doi.org/10.1016/j.molcel.2011.12.036
44. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 1998; 23:33-42; PMID:9639028; http://dx.doi.org/10.1247/csf. 23.33
45. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D, et al. Linking of autophagy to ubiquitinproteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 2007; 171:513-24; PMID:17620365; http://dx.doi.org/10.2353/ajpath.2007.070188
46. Ishida Y, Yamamoto A, Kitamura A, Lamandé SR, Yoshimori T, Bateman JF, et al. Autophagic elimination of misfolded procollagen aggregates in the endoplasmic reticulum as a means of cell protection. Mol Biol Cell 2009; 20:2744-54; PMID:19357194; http://dx.doi.org/10.1091/mbc.E08-11-1092
47. Fortun J, Dunn WA Jr., Joy S, Li J, Notterpek L. Emerging role for autophagy in the removal of aggresomes in Schwann cells. J Neurosci 2003; 23:10672-80; PMID:14627652
48. Tong J, Yan X, Yu L. The late stage of autophagy: Cellular events and molecular regulation. Protein Cell 2010; 1:907-15; PMID:21204017; http://dx.doi.org/10.1007/s13238-010-0121-z
49. De Brabander MJ, Van de Veire RM, Aerts FE, Borgers M, Janssen PA. The effects of methyl (5-(2-thienylcarbonyl)-1H-benzimidazol-2-yl) carbamate, (R 17934; NSC 238159), a new synthetic antitumoral drug interfering with microtubules, on mammalian cells cultured in vitro. Cancer Res 1976; 36:905-16; PMID:766963
50. Di Bartolomeo S, Corazzari M, Nazio F, Oliverio S, Lisi G, Antonioli M, et al. The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy. J Cell Biol 2010; 191:155-68; PMID:20921139; http://dx.doi.org/10.1083/jcb.201002100
51. Geeraert C, Ratier A, Pfisterer SG, Perdiz D, Cantaloube I, Rouault A, et al. Starvation-induced hyperacetylation of tubulin is required for the stimulation of autophagy by nutrient deprivation. J Biol Chem 2010; 285:24184-94; PMID:20484055; http://dx.doi.org/10.1074/jbc.M109.091553
52. Köchl R, Hu XW, Chan EY, Tooze SA. Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 2006; 7:129-45; PMID:16420522; http://dx.doi.org/10.1111/j.1600-0854.2005.00368. x
53. Yu QC, Marzella L. Modification of lysosomal proteolysis in mouse liver with taxol. Am J Pathol 1986; 122:553-61; PMID:2869690
54. Orsi A, Polson HE, Tooze SA. Membrane trafficking events that partake in autophagy. Curr Opin Cell Biol 2010; 22:150-6; PMID:20036114; http://dx.doi.org/10.1016/j.ceb.2009.11.013
55. Klionsky DJ. Autophagy: From phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007; 8:931-7; PMID:17712358; http://dx.doi.org/10.1038/nrm2245
56. Mimori-Kiyosue Y, Shiina N, Tsukita S. The dynamic behavior of the APC-binding protein EB1 on the distal ends of microtubules. Curr Biol 2000; 10:865-8; PMID:10899006; http://dx.doi.org/10.1016/S0960-9822(00)00600-X
57. Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM, Andreyeva N, et al. Asymmetric CLASPdependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev Cell 2007; 12:917-30; PMID:17543864; http://dx.doi.org/10.1016/j.devcel. 2007.04.002
58. Rivero S, Cardenas J, Bornens M, Rios RM. Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J 2009; 28:1016-28; PMID:19242490; http://dx.doi.org/10.1038/emboj.2009.47
59. Chabin-Brion K, Marceiller J, Perez F, Settegrana C, Drechou A, Durand G, et al. The Golgi complex is a microtubule-organizing organelle. Mol Biol Cell 2001; 12:2047-60; PMID:11452002
60. de Forges H, Bouissou A, Perez F. Interplay between microtubule dynamics and intracellular organization. Int J Biochem Cell Biol 2012; 44:266-74; PMID:22108200; http://dx.doi.org/10.1016/j.biocel. 2011.11.009
61. Aplin A, Jasionowski T, Tuttle DL, Lenk SE, Dunn WA Jr. Cytoskeletal elements are required for the formation and maturation of autophagic vacuoles. J Cell Physiol 1992; 152:458-66; PMID:1506410; http://dx.doi.org/10.1002/jcp. 1041520304
62. Thomes PG, Ehlers RA, Trambly CS, Clemens DL, Fox HS, Tuma DJ, et al. Multilevel regulation of autophagosome content by ethanol oxidation in HepG2 cells. Autophagy 2013; 9:63-73; PMID:23090141; http://dx.doi.org/10.4161/auto. 22490
63. Xie R, Nguyen S, McKeehan WL, Liu L. Acetylated microtubules are required for fusion of autophagosomes with lysosomes. BMC Cell Biol 2010; 11:89; PMID:21092184; http://dx.doi.org/10.1186/1471-2121-11-89
64. Webb JL, Ravikumar B, Rubinsztein DC. Microtubule disruption inhibits autophagosome-lysosome fusion: Implications for studying the roles of aggresomes in polyglutamine diseases. Int J Biochem Cell Biol 2004; 36:2541-50; PMID:15325591; http://dx.doi.org/10.1016/j.biocel.2004.02.003
65. Kimura S, Noda T, Yoshimori T. Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct Funct 2008; 33:109-22; PMID:18388399; http://dx.doi.org/10.1247/csf.08005
66. Burkhardt JK, Echeverri CJ, Nilsson T, Vallee RB. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol 1997; 139:469-84; PMID:9334349; http://dx.doi.org/10.1083/jcb.139.2.469
67. Burakov A, Kovalenko O, Semenova I, Zhapparova O, Nadezhdina E, Rodionov V. Cytoplasmic dynein is involved in the retention of microtubules at the centrosome in interphase cells. Traffic 2008; 9:472-80; PMID:18182007; http://dx.doi.org/10.1111/j.1600-0854.2007.00698.x
68. Watanabe Y, Tanaka M. p62/SQSTM1 in autophagic clearance of a non-ubiquitylated substrate. J Cell Sci 2011; 124:2692-701; PMID:21771882; http://dx.doi.org/10.1242/jcs.081232
69. Thurston TL, Wandel MP, von Muhlinen N, Foeglein A, Randow F. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 2012; 482:414-8; PMID:22246324; http://dx.doi.org/10.1038/ nature10744
70. Kwon HM. Protein misfolding in hypertonic stress: New insights into an old idea. Focus on "genome-wide RNAi screen and in vivo protein aggregation reporters identify degradation of damaged protein as an essential hypertonic stress response". Am J Physiol Cell Physiol 2008; 295:C1474-5; PMID:18971387; http://dx.doi.org/10.1152/ajpcell.00548.2008
71. Franchi-Gazzola R, Visigalli R, Bussolati O, Dall'Asta V, Gazzola GC. Adaptive increase of amino acid transport system A requires ERK1/2 activation. J Biol Chem 1999; 274:28922-8; PMID:10506137; http://dx.doi.org/10.1074/jbc.274. 41.28922
72. Bustamante M, Roger F, Bochaton-Piallat ML, Gabbiani G, Martin PY, Feraille E. Regulatory volume increase is associated with p38 kinase-dependent actin cytoskeleton remodeling in rat kidney MTAL. Am J Physiol Renal Physiol 2003; 285:F336-47; PMID:12724128
73. Di Ciano C, Nie Z, Szászi K, Lewis A, Uruno T, Zhan X, et al. Osmotic stress-induced remodeling of the cortical cytoskeleton. Am J Physiol Cell Physiol 2002; 283:C850-65; PMID:12176742
74. Hallows KR, Packman CH, Knauf PA. Acute cell volume changes in anisotonic media affect F-actin content of HL-60 cells. Am J Physiol 1991; 261:C1154-61; PMID:1767817
75. Pedersen SF, Mills JW, Hoffmann EK. Role of the F-actin cytoskeleton in the RVD and RVI processes in Ehrlich ascites tumor cells. Exp Cell Res 1999; 252:63-74; PMID:10502400; http://dx.doi.org/10.1006/excr.1999.4615
76. Rizoli SB, Rotstein OD, Parodo J, Phillips MJ, Kapus A. Hypertonic inhibition of exocytosis in neutrophils: Central role for osmotic actin skeleton remodeling. Am J Physiol Cell Physiol 2000; 279:C619-33; PMID:10942712
77. Galjart N. Plus-end-tracking proteins and their interactions at microtubule ends. Curr Biol 2010; 20:R528-37; PMID:20620909; http://dx.doi.org/10.1016/j.cub.2010.05.022
78. Lüders J, Stearns T. Microtubule-organizing centres: A re-evaluation. Nat Rev Mol Cell Biol 2007; 8:161-7; PMID:17245416; http://dx.doi.org/10.1038/nrm2100
79. Wehland J, Henkart M, Klausner R, Sandoval IV. Role of microtubules in the distribution of the Golgi apparatus: Effect of taxol and microinjected antialpha-tubulin antibodies. Proc Natl Acad Sci U S A 1983; 80:4286-90; PMID:6136036; http://dx.doi.org/10.1073/pnas.80.14.4286
80. Geng J, Klionsky DJ. The Golgi as a potential membrane source for autophagy. Autophagy 2010; 6:950-1; PMID:20729630; http://dx.doi.org/10.4161/ auto.6.7.13009
81. Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 2000; 10:524-30; PMID:11121744; http://dx.doi.org/10.1016/S0962- 8924(00)01852-3
82. Matteoni R, Kreis TE. Translocation and clustering of endosomes and lysosomes depends on microtubules. J Cell Biol 1987; 105:1253-65; PMID:3308906; http://dx.doi.org/10.1083/jcb.105.3.1253
83. Korolchuk VI, Saiki S, Lichtenberg M, Siddiqi FH, Roberts EA, Imarisio S, et al. Lysosomal positioning coordinates cellular nutrient responses. Nat Cell Biol 2011; 13:453-60; PMID:21394080; http://dx.doi.org/10.1038/ncb2204
84. Hurt K, Bilton D. Inhaled mannitol for the treatment of cystic fibrosis. Expert Rev Respir Med 2012; 6:19-26; PMID:22283575; http://dx.doi.org/10.1586/ ers.11.87
85. Pettit RS, Johnson CE. Airway-rehydrating agents for the treatment of cystic fibrosis: Past, present, and future. Ann Pharmacother 2011; 45:49-59; PMID:21156814; http://dx.doi.org/10.1345/aph.1P428
86. Luciani A, Villella VR, Esposito S, Brunetti-Pierri N, Medina DL, Settembre C, et al. Cystic fibrosis: A disorder with defective autophagy. Autophagy 2011; 7:104-6; PMID:21048426; http://dx.doi.org/10.4161/auto.7.1.13987
87. Yousefi S, Simon HU. Autophagy in cells of the blood. Biochim Biophys Acta 2009; 1793:1461-4; PMID:19168096; http://dx.doi.org/10.1016/j.bbamcr. 2008.12.023
88. Xu M, Zhang HL. Death and survival of neuronal and astrocytic cells in ischemic brain injury: A role of autophagy. Acta Pharmacol Sin 2011; 32:1089-99; PMID:21804578; http://dx.doi.org/10.1038/aps.2011.50
89. Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 2007; 3:452-60; PMID:17534139
90. Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science 2011; 334:678-83; PMID:22053050; http://dx.doi.org/10.1126/science. 1207056
91. Kiyomitsu T, Cheeseman IM. Chromosome-and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nat Cell Biol 2012; 14:311-7; PMID:22327364; http://dx.doi.org/10.1038/ncb2440
92. Rusan NM, Fagerstrom CJ, Yvon AM, Wadsworth P. Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein-alpha tubulin. Mol Biol Cell 2001; 12:971-80; PMID:11294900
93. Hasler U, Vinciguerra M, Vandewalle A, Martin PY, Féraille E. Dual effects of hypertonicity on aquaporin-2 expression in cultured renal collecting duct principal cells. J Am Soc Nephrol 2005; 16:1571-82; PMID:15843469; http://dx.doi.org/10.1681/ASN.2004110930
94. Hasler U, Nielsen S, Féraille E, Martin PY. Posttranscriptional control of aquaporin-2 abundance by vasopressin in renal collecting duct principal cells. Am J Physiol Renal Physiol 2006; 290:F177-87; PMID:15985652; http://dx.doi.org/10.1152/ajprenal. 00056.2005