Reciprocal regulation of cilia and autophagy via the MTOR and proteasome pathways

Autophagy

Volumn 11, Issue 4, 2015, Pages 607-616

  Wang, Shixuan ^a   Livingston, Man J ^a   Su, Yunchao ^b   Dong, Zheng ^a,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Autophagy; Cilia; MTOR; Polycystic kidney disease; Proteasome

Indexed keywords

3 METHYLADENINE; BAFILOMYCIN A1; CHLOROQUINE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEASOME; RAPAMYCIN; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE; UBIQUITIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL DIFFERENTIATION; CELL ELONGATION; CELL GROWTH; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; HUMAN; HUMAN CELL; NONHUMAN; ANIMAL; CELL LINE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; CELL LINE; CILIA; HUMANS; MICE, KNOCKOUT; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UBIQUITIN;

EID: 84953853724     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1023983     Document Type: Article

References (50)

1. Graser S, Stierhof YD, Lavoie SB, Gassner OS, Lamla S, Le Clech M, Nigg EA. Cep164, a novel centriole appendage protein required for primary cilium formation. J Cell Biol 2007; 179:321-30; PMID:17954613; http://dx.doi.org/10.1083/jcb.200707181
2. Cole DG, Diener DR, Himelblau AL, Beech PL, Fuster JC, Rosenbaum JL. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J Cell Biol 1998; 141:993-1008; PMID:9585417; http://dx.doi.org/10.1083/jcb.141.4.993
3. Pan J, Wang Q, Snell WJ. Cilium-generated signaling and cilia-related disorders. Lab Invest 2005; 85:452-63; PMID:15723088; http://dx.doi.org/10.1038/labinvest.3700253
4. Follit JA, Xu F, Keady BT, Pazour GJ. Characterization of mouse IFT complex B. Cell Motil Cytoskeleton 2009; 66:457-68; PMID:19253336; http://dx.doi.org/10.1002/cm.20346
5. Ishikawa H, Marshall WF. Ciliogenesis: building the cell’s antenna. Nat Rev Mol Cell Biol 2011; 12:222-34; PMID:21427764; http://dx.doi.org/10.1038/nrm3085
6. Barr MM, Sternberg PW. A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 1999; 401:386-9; PMID:10517638
7. Yoder BK, Tousson A, Millican L, Wu JH, Bugg CE Jr., Schafer JA, Balkovetz DF. Polaris, a protein disrupted in orpk mutant mice, is required for assembly of renal cilium. Am J Physiol Renal Physiol 2002; 282: F541-52; PMID:11832437; http://dx.doi.org/10.1152/ajprenal.00273.2001
8. Abou Alaiwi WA, Lo ST, Nauli SM. Primary cilia: highly sophisticated biological sensors. Sensors 2009; 9:7003-20; PMID:22423203; http://dx.doi.org/10.3390/s90907003
9. Jones C, Roper VC, Foucher I, Qian D, Banizs B, Petit C, Yoder BK, Chen P. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nat Genet 2008; 40:69-77; PMID:18066062; http://dx.doi.org/10.1038/ng.2007.54
10. Yoder BK. Role of primary cilia in the pathogenesis of polycystic kidney disease. J Am Soc Nephrol 2007; 18:1381-8; PMID:17429051; http://dx.doi.org/10.1681/ASN.2006111215
11. Baldari CT, Rosenbaum J. Intraflagellar transport: it’s not just for cilia anymore. Curr Opin Cell Biol 2010; 22:75-80; PMID:19962875; http://dx.doi.org/10.1016/j.ceb.2009.10.010
12. Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ., et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 2003; 33:129-37; PMID:12514735; http://dx.doi.org/10.1038/ng1076
13. Wang S, Dong Z. Primary cilia and kidney injury: current research status and future perspectives. Am J Physiol Renal Physiol 2013; 305:F1085-98; PMID:23904226; http://dx.doi.org/10.1152/ajprenal.00399.2013
14. van Reeuwijk J, Arts HH, Roepman R. Scrutinizing ciliopathies by unraveling ciliary interaction networks. Hum Mol Genet 2011; 20:R149-57; PMID:21862450; http://dx.doi.org/10.1093/hmg/ddr354
15. Badano JL, Mitsuma N, Beales PL, Katsanis N. The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 2006; 7:125-48; PMID:16722803; http://dx.doi.org/10.1146/annurev.genom.7.080505.115610
16. Mizushima N. Physiological functions of autophagy. Curr Top Microbiol Immunol 2009; 335:71-84; PMID:19802560
17. Rubinsztein DC, Shpilka T, Elazar Z. Mechanisms of autophagosome biogenesis. Curr Biol 2012; 22:R29-34; PMID:22240478; http://dx.doi.org/10.1016/j.cub.2011.11.034
18. Yang Y, Feng LQ, Zheng XX. Microtubule and kinesin/dynein-dependent, bi-directional transport of autolysosomes in neurites of PC12 cells. Int J Biochem Cell Biol 2011; 43:1147-56; PMID:21530677; http://dx.doi.org/10.1016/j.biocel.2011.04.007
19. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, 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
20. Belibi F, Zafar I, Ravichandran K, Segvic AB, Jani A, Ljubanovic DG, Edelstein CL. Hypoxia-inducible factor-1alpha (HIF-1alpha) and autophagy in polycystic kidney disease (PKD). Am J Physiol Renal Physiol 2011; 300:F1235-43; PMID:21270095; http://dx.doi.org/10.1152/ajprenal.00348.2010
21. Tang Z, Lin MG, Stowe TR, Chen S, Zhu M, Stearns T, Franco B, Zhong Q. Autophagy promotes primary ciliogenesis by removing OFD1 from centriolar satellites. Nature 2013; 502:254-7; PMID:24089205; http://dx.doi.org/10.1038/nature12606
22. Pampliega O, Orhon I, Patel B, Sridhar S, Diaz-Carretero A, Beau I, Codogno P, Satir BH, Satir P, Cuervo AM. Functional interaction between autophagy and ciliogenesis. Nature 2013; 502:194-200; PMID:24089209; http://dx.doi.org/10.1038/nature12639
23. Wang S, Wei Q, Dong G, Dong Z. ERK-mediated suppression of cilia in cisplatin-induced tubular cell apoptosis and acute kidney injury. Biochim Biophys Acta 2013; 1832:1582-90; PMID:23727409; http://dx.doi.org/10.1016/j.bbadis.2013.05.023
24. Periyasamy-Thandavan S, Jiang M, Schoenlein P, Dong Z. Autophagy: molecular machinery, regulation, and implications for renal pathophysiology. Am J Physiol Renal Physiol 2009; 297:F244-56; PMID:19279132; http://dx.doi.org/10.1152/ajprenal.00033.2009
25. Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC. Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and a-synuclein. J Biol Chem 2007; 282:5641-52; PMID:17182613; http://dx.doi.org/10.1074/jbc.M609532200
26. Shoji-Kawata S, Sumpter R, Leveno M, Campbell GR, Zou Z, Kinch L, Wilkins AD, Sun Q, Pallauf K, MacDuff D., et al. Identification of a candidate therapeutic autophagy-inducing peptide. Nature 2013; 494:201-6; PMID:23364696; http://dx.doi.org/10.1038/nature11866
27. Ding WX, Yin XM. Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 2008; 4:141-50; PMID:17986870; http://dx.doi.org/10.4161/auto.5190
28. Huber TB, Edelstein CL, Hartleben B, Inoki K, Dong Z, Koya D, Kume S, Lieberthal W, Pallet N, Quiroga A., et al. Emerging role of autophagy in kidney function, diseases and aging. Autophagy 2012; 8:1009-31; PMID:22692002; http://dx.doi.org/10.4161/auto.19821
29. Jimenez-Sanchez M, Menzies FM, Chang YY, Simecek N, Neufeld TP, Rubinsztein DC. The Hedgehog signalling pathway regulates autophagy. Nat Commun 2012; 3:1200; PMID:23149744; http://dx.doi.org/10.1038/ncomms2212
30. Jonassen JA, San Agustin J, Follit JA, Pazour GJ. Deletion of IFT20 in the mouse kidney causes misorientation of the mitotic spindle and cystic kidney disease. J Cell Biol 2008; 183:377-84; PMID:18981227; http://dx.doi.org/10.1083/jcb.200808137
31. Bell PD, Fitzgibbon W, Sas K, Stenbit AE, Amria M, Houston A, Reichert R, Gilley S, Siegal GP, Bissler J., et al. Loss of primary cilia upregulates renal hypertrophic signaling and promotes cystogenesis. J Am Soc Nephrol 2011; 22:839-48; PMID:21493775; http://dx.doi.org/10.1681/ASN.2010050526
32. Wang Y, Ding Q, Yen CJ, Xia W, Izzo JG, Lang JY, Li CW, Hsu JL, Miller SA, Wang X., et al. The crosstalk of mTOR/S6K1 and Hedgehog pathways. Cancer Cell 2012; 21:374-87; PMID:22439934; http://dx.doi.org/10.1016/j.ccr.2011.12.028
33. Wong SY, Reiter JF. The primary cilium at the crossroads of mammalian hedgehog signaling. Curr Top Dev Biol 2008; 85:225-60; PMID:19147008; http://dx.doi.org/10.1016/S0070-2153(08)00809-0
34. Rohatgi R, Milenkovic L, Scott MP. Patched1 regulates hedgehog signaling at the primary cilium. Science 2007; 317:372-6; PMID:17641202; http://dx.doi.org/10.1126/science.1139740
35. Park TJ, Haigo SL, Wallingford JB. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat Genet 2006; 38:303-11; PMID:16493421; http://dx.doi.org/10.1038/ng1753
36. Shillingford JM, Murcia NS, Larson CH, Low SH, Hedgepeth R, Brown N, Flask CA, Novick AC, Goldfarb DA, Kramer-Zucker A., et al. The mTOR pathway is regulated by polycystin-1, and its inhibition reverses renal cystogenesis in polycystic kidney disease. Proc Natl Acad Sci U S A 2006; 103:5466-71; PMID:16567633; http://dx.doi.org/10.1073/pnas.0509694103
37. Fischer DC, Jacoby U, Pape L, Ward CJ, KuwertzBroeking E, Renken C, Nizze H, Querfeld U, Rudolph B, Mueller-Wiefel DE., et al. Activation of the AKT/ mTOR pathway in autosomal recessive polycystic kidney disease (ARPKD). Nephrol Dial Transplant 2009; 24:1819-27; PMID:19176689; http://dx.doi.org/10.1093/ndt/gfn744
38. Wang S, Wu M, Yao G, Zhang J, Zhou J. The cytoplasmic tail of FPC antagonizes the full-length protein in the regulation of mTOR pathway. PLoS One 2014; 9:e95630; PMID:24851866; http://dx.doi.org/10.1371/journal.pone.0095630
39. Tao Y, Kim J, Schrier RW, Edelstein CL. Rapamycin markedly slows disease progression in a rat model of polycystic kidney disease. J Am Soc Nephrol 2005; 16:46-51; PMID:15563559; http://dx.doi.org/10.1681/ASN.2004080660
40. Harris PC, Torres VE. Genetic mechanisms and signaling pathways in autosomal dominant polycystic kidney disease. J Clin Invest 2014; 124:2315-24; PMID:24892705; http://dx.doi.org/10.1172/JCI72272
41. Ravichandran K, Edelstein CL. Polycystic kidney disease: a case of suppressed autophagy? Semin Nephrol 2014; 34:27-33; PMID:24485027; http://dx.doi.org/10.1016/j.semnephrol.2013.11.005
42. Huang K, Diener DR, Rosenbaum JL. The ubiquitin conjugation system is involved in the disassembly of cilia and flagella. J Cell Biol 2009; 186:601-13; PMID:19704024; http://dx.doi.org/10.1083/jcb.200903066
43. Praetorius HA, Spring KR. A physiological view of the primary cilium. Annu Rev Physiol 2005; 67:515-29; PMID:15709968; http://dx.doi.org/10.1146/annurev.physiol.67.040403.101353
44. Praetorius HA, Frokiaer J, Nielsen S, Spring KR. Bending the primary cilium opens Ca2C-sensitive intermediate-conductance KC channels in MDCK cells. J Membr Biol 2003; 191:193-200; PMID:12571753; http://dx.doi.org/10.1007/s00232-002-1055-z
45. Nauli SM, Jin X, AbouAlaiwi WA, El-Jouni W, Su X, Zhou J. Non-motile primary cilia as fluid shear stress mechanosensors. Methods Enzymol 2013; 525:1-20; PMID:23522462; http://dx.doi.org/10.1016/B978-0-12-397944-5.00001-8
46. Follit JA, Tuft RA, Fogarty KE, Pazour GJ. The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol Biol Cell 2006; 17:3781-92; PMID:16775004; http://dx.doi.org/10.1091/mbc.E06-02-0133
47. Pisitkun T, Shen RF, Knepper MA. Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A 2004; 101:13368-73; PMID:15326289; http://dx.doi.org/10.1073/pnas.0403453101
48. Lin YC, Niewiadomski P, Lin B, Nakamura H, Phua SC, Jiao J, Levchenko A, Inoue T, Rohatgi R, Inoue T. Chemically inducible diffusion trap at cilia reveals molecular sieve-like barrier. Nat Chem Biol 2013; 9:437-43; PMID:23666116; http://dx.doi.org/10.1038/nchembio.1252
49. Pabla N, Dong G, Jiang M, Huang S, Kumar MV, Messing RO, Dong Z. Inhibition of PKCdelta reduces cisplatin-induced nephrotoxicity without blocking chemotherapeutic efficacy in mouse models of cancer. J Clin Invest 2011; 121:2709-22; PMID:21633170; http://dx.doi.org/10.1172/JCI45586
50. Jiang M, Wei Q, Dong G, Komatsu M, Su Y, Dong Z. Autophagy in proximal tubules protects against acute kidney injury. Kidney Int 2012; 82:1271-83; PMID:22854643; http://dx.doi.org/10.1038/ki.2012.261