Control of clathrin-mediated endocytosis by NIMA family kinases
Autoři:
Braveen B. Joseph aff001; Yu Wang aff002; Phil Edeen aff001; Vladimir Lažetić aff001; Barth D. Grant aff002; David S. Fay aff001
Působiště autorů:
Department of Molecular Biology, College of Agriculture and Natural Resources, University of Wyoming, Laramie, Wyoming, United States of America
aff001; Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, New Jersey, United States of America
aff002; Department of Biochemistry and Molecular Biology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China
aff003
Vyšlo v časopise:
Control of clathrin-mediated endocytosis by NIMA family kinases. PLoS Genet 16(2): e32767. doi:10.1371/journal.pgen.1008633
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008633
Souhrn
Endocytosis, the process by which cells internalize plasma membrane and associated cargo, is regulated extensively by posttranslational modifications. Previous studies suggested the potential involvement of scores of protein kinases in endocytic control, of which only a few have been validated in vivo. Here we show that the conserved NIMA-related kinases NEKL-2/NEK8/9 and NEKL-3/NEK6/7 (the NEKLs) control clathrin-mediated endocytosis in C. elegans. Loss of NEKL-2 or NEKL-3 activities leads to penetrant larval molting defects and to the abnormal localization of trafficking markers in arrested larvae. Using an auxin-based degron system, we also find that depletion of NEKLs in adult-stage C. elegans leads to gross clathrin mislocalization and to a dramatic reduction in clathrin mobility at the apical membrane. Using a non-biased genetic screen to identify suppressors of nekl molting defects, we identified several components and regulators of AP2, the major clathrin adapter complex acting at the plasma membrane. Strikingly, reduced AP2 activity rescues both nekl mutant molting defects as well as associated trafficking phenotypes, whereas increased levels of active AP2 exacerbate nekl defects. Moreover, in a unique example of mutual suppression, NEKL inhibition alleviates defects associated with reduced AP2 activity, attesting to the tight link between NEKL and AP2 functions. We also show that NEKLs are required for the clustering and internalization of membrane cargo required for molting. Notably, we find that human NEKs can rescue molting and trafficking defects in nekl mutant worms, suggesting that the control of intracellular trafficking is an evolutionarily conserved function of NEK family kinases.
Klíčová slova:
Auxins – Caenorhabditis elegans – Cell membranes – Endocytosis – Fluorescence recovery after photobleaching – Larvae – Molting – RNA interference
Zdroje
1. Johnstone IL. The cuticle of the nematode Caenorhabditis elegans: a complex collagen structure. Bioessays. 1994;16(3):171–8. Epub 1994/03/01. doi: 10.1002/bies.950160307 8166670.
2. Johnstone IL. Cuticle collagen genes. Expression in Caenorhabditis elegans. Trends Genet. 2000;16(1):21–7. Epub 2000/01/19. doi: 10.1016/s0168-9525(99)01857-0 10637627.
3. Page AP, Johnstone IL. The cuticle. WormBook. 2007:1–15. Epub 2007/12/01. doi: 10.1895/wormbook.1.138.1 18050497.
4. Lazetic V, Fay DS. Molting in C. elegans. Worm. 2017;6(1):e1330246. Epub 2017/07/14. doi: 10.1080/21624054.2017.1330246 28702275.
5. Singh RN, Sulston JE. Some observations on the moulting of Caenorhabditis elegans. Nematologica. 1978;24(1):63–71.
6. Frand AR, Russel S, Ruvkun G. Functional genomic analysis of C. elegans molting. PLoS Biol. 2005;3(10):e312. Epub 2005/08/27. doi: 10.1371/journal.pbio.0030312 16122351.
7. Cox GN, Kusch M, DeNevi K, Edgar RS. Temporal regulation of cuticle synthesis during development of Caenorhabditis elegans. Dev Biol. 1981;84(2):277–85. Epub 1981/06/01. doi: 10.1016/0012-1606(81)90395-x 20737865.
8. Roberts B, Clucas C, Johnstone IL. Loss of SEC-23 in Caenorhabditis elegans causes defects in oogenesis, morphogenesis, and extracellular matrix secretion. Mol Biol Cell. 2003;14(11):4414–26. Epub 2003/10/11. doi: 10.1091/mbc.E03-03-0162 14551256.
9. Hayes GD, Frand AR, Ruvkun G. The mir-84 and let-7 paralogous microRNA genes of Caenorhabditis elegans direct the cessation of molting via the conserved nuclear hormone receptors NHR-23 and NHR-25. Development. 2006;133(23):4631–41. Epub 2006/10/27. doi: 10.1242/dev.02655 17065234.
10. Kouns NA, Nakielna J, Behensky F, Krause MW, Kostrouch Z, Kostrouchova M. NHR-23 dependent collagen and hedgehog-related genes required for molting. Biochem Biophys Res Commun. 2011;413(4):515–20. Epub 2011/09/14. doi: 10.1016/j.bbrc.2011.08.124 21910973.
11. Monsalve GC, Frand AR. Toward a unified model of developmental timing: A "molting" approach. Worm. 2012;1(4):221–30. Epub 2013/09/24. doi: 10.4161/worm.20874 24058853.
12. Martin R, Entchev EV, Kurzchalia TV, Knolker HJ. Steroid hormones controlling the life cycle of the nematode Caenorhabditis elegans: stereoselective synthesis and biology. Org Biomol Chem. 2010;8(4):739–50. Epub 2010/02/06. doi: 10.1039/b918488k 20135027.
13. Entchev EV, Kurzchalia TV. Requirement of sterols in the life cycle of the nematode Caenorhabditis elegans. Semin Cell Dev Biol. 2005;16(2):175–82. Epub 2005/03/31. doi: 10.1016/j.semcdb.2005.01.004 15797828.
14. Merris M, Wadsworth WG, Khamrai U, Bittman R, Chitwood DJ, Lenard J. Sterol effects and sites of sterol accumulation in Caenorhabditis elegans: developmental requirement for 4alpha-methyl sterols. J Lipid Res. 2003;44(1):172–81. Epub 2003/01/09. doi: 10.1194/jlr.m200323-jlr200 12518036.
15. Yochem J, Tuck S, Greenwald I, Han M. A gp330/megalin-related protein is required in the major epidermis of Caenorhabditis elegans for completion of molting. Development. 1999;126(3):597–606. Epub 1999/01/07. 9876188.
16. Roudier N, Lefebvre C, Legouis R. CeVPS-27 is an endosomal protein required for the molting and the endocytic trafficking of the low-density lipoprotein receptor-related protein 1 in Caenorhabditis elegans. Traffic. 2005;6(8):695–705. Epub 2005/07/07. doi: 10.1111/j.1600-0854.2005.00309.x 15998324.
17. Holmes A, Flett A, Coudreuse D, Korswagen HC, Pettitt J. C. elegans Disabled is required for cell-type specific endocytosis and is essential in animals lacking the AP-3 adaptor complex. J Cell Sci. 2007;120(Pt 15):2741–51. Epub 2007/07/20. doi: 10.1242/jcs.03474 17636000.
18. Kamikura DM, Cooper JA. Lipoprotein receptors and a disabled family cytoplasmic adaptor protein regulate EGL-17/FGF export in C. elegans. Genes Dev. 2003;17(22):2798–811. Epub 2003/11/25. doi: 10.1101/gad.1136103 14630941.
19. Conner SD, Schmid SL. Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J Cell Biol. 2002;156(5):921–9. Epub 2002/03/06. doi: 10.1083/jcb.200108123 11877461.
20. Yochem J, Lazetic V, Bell L, Chen L, Fay D. C. elegans NIMA-related kinases NEKL-2 and NEKL-3 are required for the completion of molting. Dev Biol. 2015;398(2):255–66. Epub 2014/12/20. doi: 10.1016/j.ydbio.2014.12.008 25523392.
21. Lazetic V, Fay DS. Conserved ankyrin repeat proteins and their NIMA kinase partners regulate extracellular matrix remodeling and intracellular trafficking in Caenorhabditis elegans. Genetics. 2017;205:273–93. doi: 10.1534/genetics.116.194464 27799278
22. Czarnecki PG, Gabriel GC, Manning DK, Sergeev M, Lemke K, Klena NT, et al. ANKS6 is the critical activator of NEK8 kinase in embryonic situs determination and organ patterning. Nat Commun. 2015;6:6023. Epub 2015/01/21. doi: 10.1038/ncomms7023 25599650.
23. Hoff S, Halbritter J, Epting D, Frank V, Nguyen TM, van Reeuwijk J, et al. ANKS6 is a central component of a nephronophthisis module linking NEK8 to INVS and NPHP3. Nat Genet. 2013;45(8):951–6. Epub 2013/06/26. doi: 10.1038/ng.2681 23793029.
24. Ramachandran H, Engel C, Muller B, Dengjel J, Walz G, Yakulov TA. Anks3 alters the sub-cellular localization of the Nek7 kinase. Biochem Biophys Res Commun. 2015;464(3):901–7. Epub 2015/07/19. doi: 10.1016/j.bbrc.2015.07.063 26188091.
25. Shiba D, Manning DK, Koga H, Beier DR, Yokoyama T. Inv acts as a molecular anchor for Nphp3 and Nek8 in the proximal segment of primary cilia. Cytoskeleton (Hoboken). 2010;67(2):112–9. Epub 2010/02/20. doi: 10.1002/cm.20428 20169535.
26. Hemalatha A, Mayor S. Recent advances in clathrin-independent endocytosis. F1000Res. 2019;8. Epub 2019/02/19. doi: 10.12688/f1000research.16549.1 30774931.
27. Kadlecova Z, Spielman SJ, Loerke D, Mohanakrishnan A, Reed DK, Schmid SL. Regulation of clathrin-mediated endocytosis by hierarchical allosteric activation of AP2. J Cell Biol. 2017;216(1):167–79. Epub 2016/12/23. doi: 10.1083/jcb.201608071 28003333.
28. Lacy MM, Ma R, Ravindra NG, Berro J. Molecular mechanisms of force production in clathrin-mediated endocytosis. FEBS Lett. 2018;592(21):3586–605. Epub 2018/07/15. doi: 10.1002/1873-3468.13192 30006986.
29. Mettlen M, Chen PH, Srinivasan S, Danuser G, Schmid SL. Regulation of Clathrin-Mediated Endocytosis. Annu Rev Biochem. 2018;87:871–96. Epub 2018/04/18. doi: 10.1146/annurev-biochem-062917-012644 29661000.
30. Smith SM, Baker M, Halebian M, Smith CJ. Weak Molecular Interactions in Clathrin-Mediated Endocytosis. Front Mol Biosci. 2017;4:72. Epub 2017/12/01. doi: 10.3389/fmolb.2017.00072 29184887.
31. Sochacki KA, Taraska JW. From Flat to Curved Clathrin: Controlling a Plastic Ratchet. Trends Cell Biol. 2019;29(3):241–56. Epub 2019/01/02. doi: 10.1016/j.tcb.2018.12.002 30598298.
32. Taylor MJ, Perrais D, Merrifield CJ. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 2011;9(3):e1000604. Epub 2011/03/30. doi: 10.1371/journal.pbio.1000604 21445324.
33. Keen JH. Clathrin assembly proteins: affinity purification and a model for coat assembly. J Cell Biol. 1987;105(5):1989–98. Epub 1987/11/01. doi: 10.1083/jcb.105.5.1989 2890644.
34. Pearse BM, Robinson MS. Purification and properties of 100-kd proteins from coated vesicles and their reconstitution with clathrin. EMBO J. 1984;3(9):1951–7. Epub 1984/09/01. 6149117.
35. Park SY, Guo X. Adaptor protein complexes and intracellular transport. Biosci Rep. 2014;34(4). Epub 2014/07/01. doi: 10.1042/BSR20140069 24975939.
36. Matsui W, Kirchhausen T. Stabilization of clathrin coats by the core of the clathrin-associated protein complex AP-2. Biochemistry. 1990;29(48):10791–8. Epub 1990/12/04. doi: 10.1021/bi00500a011 2125494.
37. Rapoport I, Miyazaki M, Boll W, Duckworth B, Cantley LC, Shoelson S, et al. Regulatory interactions in the recognition of endocytic sorting signals by AP-2 complexes. EMBO J. 1997;16(9):2240–50. Epub 1997/05/01. doi: 10.1093/emboj/16.9.2240 9171339.
38. Jackson LP, Kelly BT, McCoy AJ, Gaffry T, James LC, Collins BM, et al. A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell. 2010;141(7):1220–9. Epub 2010/07/07. doi: 10.1016/j.cell.2010.05.006 20603002.
39. Beacham GM, Partlow EA, Hollopeter G. Conformational regulation of AP1 and AP2 clathrin adaptor complexes. Traffic. 2019. Epub 2019/07/18. doi: 10.1111/tra.12677 31313456.
40. Hollopeter G, Lange JJ, Zhang Y, Vu TN, Gu M, Ailion M, et al. The membrane-associated proteins FCHo and SGIP are allosteric activators of the AP2 clathrin adaptor complex. Elife. 2014;3. Epub 2014/10/11. doi: 10.7554/eLife.03648 25303366.
41. Umasankar PK, Ma L, Thieman JR, Jha A, Doray B, Watkins SC, et al. A clathrin coat assembly role for the muniscin protein central linker revealed by TALEN-mediated gene editing. Elife. 2014;3. Epub 2014/10/11. doi: 10.7554/eLife.04137 25303365.
42. Beacham GM, Partlow EA, Lange JJ, Hollopeter G. NECAPs are negative regulators of the AP2 clathrin adaptor complex. Elife. 2018;7. Epub 2018/01/19. doi: 10.7554/eLife.32242 29345618.
43. Smythe E. Regulating the clathrin-coated vesicle cycle by AP2 subunit phosphorylation. Trends Cell Biol. 2002;12(8):352–4. Epub 2002/08/23. doi: 10.1016/s0962-8924(02)02333-4 12191904.
44. Joseph BB, Blouin NA, Fay DS. Use of a Sibling Subtraction Method for Identifying Causal Mutations in Caenorhabditis elegans by Whole-Genome Sequencing. G3 (Bethesda). 2018;8(2):669–78. Epub 2017/12/15. doi: 10.1534/g3.117.300135 29237702.
45. Lazetic V, Fay DS. Conserved Ankyrin Repeat Proteins and Their NIMA Kinase Partners Regulate Extracellular Matrix Remodeling and Intracellular Trafficking in Caenorhabditis elegans. Genetics. 2017;205(1):273–93. Epub 2016/11/02. doi: 10.1534/genetics.116.194464 27799278.
46. Pan CL, Baum PD, Gu M, Jorgensen EM, Clark SG, Garriga G. C. elegans AP-2 and retromer control Wnt signaling by regulating mig-14/Wntless. Dev Cell. 2008;14(1):132–9. Epub 2007/12/28. doi: 10.1016/j.devcel.2007.12.001 18160346.
47. Gu M, Schuske K, Watanabe S, Liu Q, Baum P, Garriga G, et al. Mu2 adaptin facilitates but is not essential for synaptic vesicle recycling in Caenorhabditis elegans. J Cell Biol. 2008;183(5):881–92. Epub 2008/12/03. doi: 10.1083/jcb.200806088 19047463.
48. McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol. 2011;12(8):517–33. Epub 2011/07/23. doi: 10.1038/nrm3151 21779028.
49. Gu M, Liu Q, Watanabe S, Sun L, Hollopeter G, Grant BD, et al. AP2 hemicomplexes contribute independently to synaptic vesicle endocytosis. Elife. 2013;2:e00190. Epub 2013/03/14. doi: 10.7554/eLife.00190 23482940.
50. Boehm M, Bonifacino JS. Adaptins: the final recount. Mol Biol Cell. 2001;12(10):2907–20. Epub 2001/10/13. doi: 10.1091/mbc.12.10.2907 11598180.
51. Shim J, Sternberg PW, Lee J. Distinct and redundant functions of mu1 medium chains of the AP-1 clathrin-associated protein complex in the nematode Caenorhabditis elegans. Mol Biol Cell. 2000;11(8):2743–56. Epub 2000/08/10. doi: 10.1091/mbc.11.8.2743 10930467.
52. Henne WM, Boucrot E, Meinecke M, Evergren E, Vallis Y, Mittal R, et al. FCHo proteins are nucleators of clathrin-mediated endocytosis. Science. 2010;328(5983):1281–4. Epub 2010/05/08. doi: 10.1126/science.1188462 20448150.
53. Ma L, Umasankar PK, Wrobel AG, Lymar A, McCoy AJ, Holkar SS, et al. Transient Fcho1/2Eps15/RAP-2 Nanoclusters Prime the AP-2 Clathrin Adaptor for Cargo Binding. Dev Cell. 2016;37(5):428–43. Epub 2016/05/31. doi: 10.1016/j.devcel.2016.05.003 27237791.
54. Ritter B, Murphy S, Dokainish H, Girard M, Gudheti MV, Kozlov G, et al. NECAP 1 regulates AP-2 interactions to control vesicle size, number, and cargo during clathrin-mediated endocytosis. PLoS Biol. 2013;11(10):e1001670. Epub 2013/10/17. doi: 10.1371/journal.pbio.1001670 24130457 software to collect images and analyze the data.
55. Murshid A, Srivastava A, Kumar R, Presley JF. Characterization of the localization and function of NECAP 1 in neurons. J Neurochem. 2006;98(6):1746–62. Epub 2006/08/02. doi: 10.1111/j.1471-4159.2006.04066.x 16879712.
56. Ritter B, Denisov AY, Philie J, Allaire PD, Legendre-Guillemin V, Zylbergold P, et al. The NECAP PHear domain increases clathrin accessory protein binding potential. EMBO J. 2007;26(18):4066–77. Epub 2007/09/01. doi: 10.1038/sj.emboj.7601836 17762867.
57. Chamberland JP, Antonow LT, Dias Santos M, Ritter B. NECAP2 controls clathrin coat recruitment to early endosomes for fast endocytic recycling. J Cell Sci. 2016;129(13):2625–37. Epub 2016/05/22. doi: 10.1242/jcs.173708 27206861.
58. Ritter B, Philie J, Girard M, Tung EC, Blondeau F, McPherson PS. Identification of a family of endocytic proteins that define a new alpha-adaptin ear-binding motif. EMBO Rep. 2003;4(11):1089–95. Epub 2003/10/14. doi: 10.1038/sj.embor.7400004 14555962.
59. Lazetic V, Joseph BB, Bernazzani SM, Fay DS. Actin organization and endocytic trafficking are controlled by a network linking NIMA-related kinases to the CDC-42-SID-3/ACK1 pathway. PLoS Genet. 2018;14(4):e1007313. Epub 2018/04/03. doi: 10.1371/journal.pgen.1007313 29608564.
60. Holland AJ, Fachinetti D, Han JS, Cleveland DW. Inducible, reversible system for the rapid and complete degradation of proteins in mammalian cells. Proc Natl Acad Sci U S A. 2012;109(49):E3350–7. Epub 2012/11/15. doi: 10.1073/pnas.1216880109 23150568.
61. Zhang L, Ward JD, Cheng Z, Dernburg AF. The auxin-inducible degradation (AID) system enables versatile conditional protein depletion in C. elegans. Development. 2015;142(24):4374–84. Epub 2015/11/11. doi: 10.1242/dev.129635 26552885.
62. Greener T, Grant B, Zhang Y, Wu X, Greene LE, Hirsh D, et al. Caenorhabditis elegans auxilin: a J-domain protein essential for clathrin-mediated endocytosis in vivo. Nat Cell Biol. 2001;3(2):215–9. Epub 2001/02/15. doi: 10.1038/35055137 11175756.
63. Wu X, Zhao X, Baylor L, Kaushal S, Eisenberg E, Greene LE. Clathrin exchange during clathrin-mediated endocytosis. J Cell Biol. 2001;155(2):291–300. Epub 2001/10/18. doi: 10.1083/jcb.200104085 11604424.
64. Kang YL, Yochem J, Bell L, Sorensen EB, Chen L, Conner SD. Caenorhabditis elegans reveals a FxNPxY-independent low-density lipoprotein receptor internalization mechanism mediated by epsin1. Mol Biol Cell. 2013;24(3):308–18. Epub 2012/12/18. doi: 10.1091/mbc.E12-02-0163 23242996.
65. Okkema PG, Harrison SW, Plunger V, Aryana A, Fire A. Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics. 1993;135(2):385–404. Epub 1993/10/01. 8244003.
66. Gallegos JE, Rose AB. The enduring mystery of intron-mediated enhancement. Plant Sci. 2015;237:8–15. Epub 2015/06/20. doi: 10.1016/j.plantsci.2015.04.017 26089147.
67. Hussain MM. Structural, biochemical and signaling properties of the low-density lipoprotein receptor gene family. Front Biosci. 2001;6:D417–28. Epub 2001/03/07. doi: 10.2741/hussain1 11229872.
68. Wang L, Johnson A, Hanna M, Audhya A. Eps15 membrane-binding and -bending activity acts redundantly with Fcho1 during clathrin-mediated endocytosis. Mol Biol Cell. 2016;27(17):2675–87. Epub 2016/07/08. doi: 10.1091/mbc.E16-03-0151 27385343.
69. Huttlin EL, Bruckner RJ, Paulo JA, Cannon JR, Ting L, Baltier K, et al. Architecture of the human interactome defines protein communities and disease networks. Nature. 2017;545(7655):505–9. Epub 2017/05/18. doi: 10.1038/nature22366 28514442.
70. Hein MY, Hubner NC, Poser I, Cox J, Nagaraj N, Toyoda Y, et al. A human interactome in three quantitative dimensions organized by stoichiometries and abundances. Cell. 2015;163(3):712–23. Epub 2015/10/27. doi: 10.1016/j.cell.2015.09.053 26496610.
71. Sousa R, Lafer EM. The role of molecular chaperones in clathrin mediated vesicular trafficking. Front Mol Biosci. 2015;2:26. Epub 2015/06/05. doi: 10.3389/fmolb.2015.00026 26042225.
72. Scheele U, Kalthoff C, Ungewickell E. Multiple interactions of auxilin 1 with clathrin and the AP-2 adaptor complex. J Biol Chem. 2001;276(39):36131–8. Epub 2001/07/27. doi: 10.1074/jbc.M106511200 11470803.
73. Shih W, Gallusser A, Kirchhausen T. A clathrin-binding site in the hinge of the beta 2 chain of mammalian AP-2 complexes. J Biol Chem. 1995;270(52):31083–90. Epub 1995/12/29. doi: 10.1074/jbc.270.52.31083 8537368.
74. Wu X, Zhao X, Puertollano R, Bonifacino JS, Eisenberg E, Greene LE. Adaptor and clathrin exchange at the plasma membrane and trans-Golgi network. Mol Biol Cell. 2003;14(2):516–28. Epub 2003/02/18. doi: 10.1091/mbc.E02-06-0353 12589051.
75. Cremona O, Di Paolo G, Wenk MR, Luthi A, Kim WT, Takei K, et al. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell. 1999;99(2):179–88. Epub 1999/10/27. doi: 10.1016/s0092-8674(00)81649-9 10535736.
76. Gad H, Ringstad N, Low P, Kjaerulff O, Gustafsson J, Wenk M, et al. Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron. 2000;27(2):301–12. Epub 2000/09/14. doi: 10.1016/s0896-6273(00)00038-6 10985350.
77. Stenmark H. Cycling lipids. Curr Biol. 2000;10(2):R57–9. Epub 2000/02/09. doi: 10.1016/s0960-9822(00)00279-7 10662657.
78. Schlossman DM, Schmid SL, Braell WA, Rothman JE. An enzyme that removes clathrin coats: purification of an uncoating ATPase. J Cell Biol. 1984;99(2):723–33. Epub 1984/08/01. doi: 10.1083/jcb.99.2.723 6146630.
79. Heuser JE, Keen J. Deep-etch visualization of proteins involved in clathrin assembly. J Cell Biol. 1988;107(3):877–86. Epub 1988/09/01. doi: 10.1083/jcb.107.3.877 3417785.
80. Greene LE, Eisenberg E. Dissociation of clathrin from coated vesicles by the uncoating ATPase. J Biol Chem. 1990;265(12):6682–7. Epub 1990/04/25. 1969864.
81. Buxbaum E, Woodman PG. Selective action of uncoating ATPase towards clathrin-coated vesicles from brain. J Cell Sci. 1995;108 (Pt 3):1295–306. Epub 1995/03/01. 7622612.
82. Hannan LA, Newmyer SL, Schmid SL. ATP- and cytosol-dependent release of adaptor proteins from clathrin-coated vesicles: A dual role for Hsc70. Mol Biol Cell. 1998;9(8):2217–29. Epub 1998/08/07. doi: 10.1091/mbc.9.8.2217 9693377.
83. Semerdjieva S, Shortt B, Maxwell E, Singh S, Fonarev P, Hansen J, et al. Coordinated regulation of AP2 uncoating from clathrin-coated vesicles by rab5 and hRME-6. J Cell Biol. 2008;183(3):499–511. Epub 2008/11/05. doi: 10.1083/jcb.200806016 18981233.
84. Heuser JE, Anderson RG. Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol. 1989;108(2):389–400. Epub 1989/02/01. doi: 10.1083/jcb.108.2.389 2563728.
85. Newmyer SL, Schmid SL. Dominant-interfering Hsc70 mutants disrupt multiple stages of the clathrin-coated vesicle cycle in vivo. J Cell Biol. 2001;152(3):607–20. Epub 2001/02/07. doi: 10.1083/jcb.152.3.607 11157986.
86. Pelkmans L, Fava E, Grabner H, Hannus M, Habermann B, Krausz E, et al. Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature. 2005;436(7047):78–86. Epub 2005/05/13. doi: 10.1038/nature03571 15889048.
87. Collinet C, Stoter M, Bradshaw CR, Samusik N, Rink JC, Kenski D, et al. Systems survey of endocytosis by multiparametric image analysis. Nature. 2010;464(7286):243–9. Epub 2010/03/02. doi: 10.1038/nature08779 20190736.
88. Govindaraghavan M, McGuire Anglin SL, Shen KF, Shukla N, De Souza CP, Osmani SA. Identification of interphase functions for the NIMA kinase involving microtubules and the ESCRT pathway. PLoS Genet. 2014;10(3):e1004248. Epub 2014/03/29. doi: 10.1371/journal.pgen.1004248 24675878.
89. de Souza EE, Meirelles GV, Godoy BB, Perez AM, Smetana JH, Doxsey SJ, et al. Characterization of the human NEK7 interactome suggests catalytic and regulatory properties distinct from those of NEK6. J Proteome Res. 2014;13(9):4074–90. Epub 2014/08/06. doi: 10.1021/pr500437x 25093993.
90. Meirelles GV, Perez AM, de Souza EE, Basei FL, Papa PF, Melo Hanchuk TD, et al. "Stop Ne(c)king around": How interactomics contributes to functionally characterize Nek family kinases. World J Biol Chem. 2014;5(2):141–60. Epub 2014/06/13. 24921005.
91. Vaz Meirelles G, Ferreira Lanza DC, da Silva JC, Santana Bernachi J, Paes Leme AF, Kobarg J. Characterization of hNek6 interactome reveals an important role for its short N-terminal domain and colocalization with proteins at the centrosome. J Proteome Res. 2010;9(12):6298–316. Epub 2010/09/30. doi: 10.1021/pr100562w 20873783.
92. Nassirpour R, Shao L, Flanagan P, Abrams T, Jallal B, Smeal T, et al. Nek6 mediates human cancer cell transformation and is a potential cancer therapeutic target. Mol Cancer Res. 2010;8(5):717–28. Epub 2010/04/22. doi: 10.1158/1541-7786.MCR-09-0291 20407017.
93. Wang R, Song Y, Xu X, Wu Q, Liu C. The expression of Nek7, FoxM1, and Plk1 in gallbladder cancer and their relationships to clinicopathologic features and survival. Clin Transl Oncol. 2013;15(8):626–32. Epub 2013/01/30. doi: 10.1007/s12094-012-0978-9 23359173.
94. Zhou L, Wang Z, Xu X, Wan Y, Qu K, Fan H, et al. Nek7 is overexpressed in hepatocellular carcinoma and promotes hepatocellular carcinoma cell proliferation in vitro and in vivo. Oncotarget. 2016;7(14):18620–30. Epub 2016/02/28. doi: 10.18632/oncotarget.7620 26921196.
95. Choudhury AD, Schinzel AC, Cotter MB, Lis RT, Labella K, Lock YJ, et al. Castration Resistance in Prostate Cancer Is Mediated by the Kinase NEK6. Cancer Res. 2017;77(3):753–65. Epub 2016/12/03. doi: 10.1158/0008-5472.CAN-16-0455 27899381.
96. He Z, Ni X, Xia L, Shao Z. Overexpression of NIMA-related kinase 6 (NEK6) contributes to malignant growth and dismal prognosis in Human Breast Cancer. Pathol Res Pract. 2018;214(10):1648–54. Epub 2018/08/30. doi: 10.1016/j.prp.2018.07.030 30153958.
97. Jeon YJ, Lee KY, Cho YY, Pugliese A, Kim HG, Jeong CH, et al. Role of NEK6 in tumor promoter-induced transformation in JB6 C141 mouse skin epidermal cells. J Biol Chem. 2010;285(36):28126–33. Epub 2010/07/03. doi: 10.1074/jbc.M110.137190 20595392.
98. Kasap E, Gerceker E, Boyacioglu SO, Yuceyar H, Yildirm H, Ayhan S, et al. The potential role of the NEK6, AURKA, AURKB, and PAK1 genes in adenomatous colorectal polyps and colorectal adenocarcinoma. Tumour Biol. 2016;37(3):3071–80. Epub 2015/10/02. doi: 10.1007/s13277-015-4131-6 26423403.
99. Quarmby LM, Mahjoub MR. Caught Nek-ing: cilia and centrioles. J Cell Sci. 2005;118(Pt 22):5161–9. Epub 2005/11/11. doi: 10.1242/jcs.02681 16280549.
100. Grampa V, Delous M, Zaidan M, Odye G, Thomas S, Elkhartoufi N, et al. Novel NEK8 Mutations Cause Severe Syndromic Renal Cystic Dysplasia through YAP Dysregulation. PLoS Genet. 2016;12(3):e1005894. Epub 2016/03/12. doi: 10.1371/journal.pgen.1005894 26967905.
101. Rajagopalan R, Grochowski CM, Gilbert MA, Falsey AM, Coleman K, Romero R, et al. Compound heterozygous mutations in NEK8 in siblings with end-stage renal disease with hepatic and cardiac anomalies. Am J Med Genet A. 2016;170(3):750–3. Epub 2015/12/25. doi: 10.1002/ajmg.a.37512 26697755.
102. Manning DK, Sergeev M, van Heesbeen RG, Wong MD, Oh JH, Liu Y, et al. Loss of the ciliary kinase Nek8 causes left-right asymmetry defects. J Am Soc Nephrol. 2013;24(1):100–12. Epub 2013/01/01. doi: 10.1681/ASN.2012050490 23274954.
103. Zalli D, Bayliss R, Fry AM. The Nek8 protein kinase, mutated in the human cystic kidney disease nephronophthisis, is both activated and degraded during ciliogenesis. Hum Mol Genet. 2012;21(5):1155–71. Epub 2011/11/23. doi: 10.1093/hmg/ddr544 22106379.
104. Otto EA, Trapp ML, Schultheiss UT, Helou J, Quarmby LM, Hildebrandt F. NEK8 mutations affect ciliary and centrosomal localization and may cause nephronophthisis. J Am Soc Nephrol. 2008;19(3):587–92. Epub 2008/01/18. doi: 10.1681/ASN.2007040490 18199800.
105. Mahjoub MR, Trapp ML, Quarmby LM. NIMA-related kinases defective in murine models of polycystic kidney diseases localize to primary cilia and centrosomes. J Am Soc Nephrol. 2005;16(12):3485–9. Epub 2005/11/04. doi: 10.1681/ASN.2005080824 16267153.
106. Casey JP, Brennan K, Scheidel N, McGettigan P, Lavin PT, Carter S, et al. Recessive NEK9 mutation causes a lethal skeletal dysplasia with evidence of cell cycle and ciliary defects. Hum Mol Genet. 2016;25(9):1824–35. Epub 2016/02/26. doi: 10.1093/hmg/ddw054 26908619.
107. Stiernagle T. Maintenance of C. elegans. WormBook. 2006:1–11. Epub 2007/12/01. doi: 10.1895/wormbook.1.101.1 18050451.
108. Arribere JA, Bell RT, Fu BX, Artiles KL, Hartman PS, Fire AZ. Efficient marker-free recovery of custom genetic modifications with CRISPR/Cas9 in Caenorhabditis elegans. Genetics. 2014;198(3):837–46. Epub 2014/08/28. doi: 10.1534/genetics.114.169730 25161212.
109. Paix A, Wang Y, Smith HE, Lee CY, Calidas D, Lu T, et al. Scalable and versatile genome editing using linear DNAs with microhomology to Cas9 Sites in Caenorhabditis elegans. Genetics. 2014;198(4):1347–56. Epub 2014/09/25. doi: 10.1534/genetics.114.170423 25249454.
110. Paix A, Folkmann A, Rasoloson D, Seydoux G. High Efficiency, Homology-Directed Genome Editing in Caenorhabditis elegans Using CRISPR-Cas9 Ribonucleoprotein Complexes. Genetics. 2015;201(1):47–54. Epub 2015/07/19. doi: 10.1534/genetics.115.179382 26187122.
111. Dickinson DJ, Pani AM, Heppert JK, Higgins CD, Goldstein B. Streamlined Genome Engineering with a Self-Excising Drug Selection Cassette. Genetics. 2015;200(4):1035–49. Epub 2015/06/06. doi: 10.1534/genetics.115.178335 26044593.
112. Mello CC, Kramer JM, Stinchcomb D, Ambros V. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991;10(12):3959–70. Epub 1991/12/01. 1935914.
113. Frokjaer-Jensen C, Davis MW, Sarov M, Taylor J, Flibotte S, LaBella M, et al. Random and targeted transgene insertion in Caenorhabditis elegans using a modified Mos1 transposon. Nat Methods. 2014;11(5):529–34. Epub 2014/05/14. doi: 10.1038/nmeth.2889 24820376.
114. El Mouridi S, Lecroisey C, Tardy P, Mercier M, Leclercq-Blondel A, Zariohi N, et al. Reliable CRISPR/Cas9 Genome Engineering in Caenorhabditis elegans Using a Single Efficient sgRNA and an Easily Recognizable Phenotype. G3 (Bethesda). 2017;7(5):1429–37. Epub 2017/03/11. doi: 10.1534/g3.117.040824 28280211.
115. Kohnlein K, Urban N, Guerrero-Gomez D, Steinbrenner H, Urbanek P, Priebs J, et al. A Caenorhabditis elegans ortholog of human selenium-binding protein 1 is a pro-aging factor protecting against selenite toxicity. Redox Biol. 2019;28:101323. Epub 2019/09/27. doi: 10.1016/j.redox.2019.101323 31557719.
116. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391(6669):806–11. Epub 1998/03/05. doi: 10.1038/35888 9486653.
117. Ahringer J. Reverse Genetics, WormBook. 2005.
118. Wang D, Kennedy S, Conte D Jr., Kim JK, Gabel HW, Kamath RS, et al. Somatic misexpression of germline P granules and enhanced RNA interference in retinoblastoma pathway mutants. Nature. 2005;436(7050):593–7. Epub 2005/07/29. 16049496.
119. Fay DS, Gerow K. A biologist’s guide to statistical thinking and analysis. WormBook. 2013:1–54. Epub 2013/08/03. doi: 10.1895/wormbook.1.159.1 23908055.
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