Mutation of NEKL-4/NEK10 and TTLL genes suppress neuronal ciliary degeneration caused by loss of CCPP-1 deglutamylase function


Autoři: Kade M. Power aff001;  Jyothi S. Akella aff001;  Amanda Gu aff001;  Jonathon D. Walsh aff001;  Sebastian Bellotti aff001;  Margaret Morash aff001;  Winnie Zhang aff001;  Yasmin H. Ramadan aff001;  Nicole Ross aff002;  Andy Golden aff003;  Harold E. Smith aff003;  Maureen M. Barr aff001;  Robert O’Hagan aff002
Působiště autorů: Department of Genetics and Human Genetics Institute of New Jersey, Rutgers University, Piscataway, NJ, United States of America aff001;  Biology Department, Montclair State University, Montclair, NJ, United States of America aff002;  National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, United States of America aff003
Vyšlo v časopise: Mutation of NEKL-4/NEK10 and TTLL genes suppress neuronal ciliary degeneration caused by loss of CCPP-1 deglutamylase function. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009052
Kategorie: Research Article
doi: 10.1371/journal.pgen.1009052

Souhrn

Ciliary microtubules are subject to post-translational modifications that act as a “Tubulin Code” to regulate motor traffic, binding proteins and stability. In humans, loss of CCP1, a cytosolic carboxypeptidase and tubulin deglutamylating enzyme, causes infantile-onset neurodegeneration. In C. elegans, mutations in ccpp-1, the homolog of CCP1, result in progressive degeneration of neuronal cilia and loss of neuronal function. To identify genes that regulate microtubule glutamylation and ciliary integrity, we performed a forward genetic screen for suppressors of ciliary degeneration in ccpp-1 mutants. We isolated the ttll-5(my38) suppressor, a mutation in a tubulin tyrosine ligase-like glutamylase gene. We show that mutation in the ttll-4, ttll-5, or ttll-11 gene suppressed the hyperglutamylation-induced loss of ciliary dye filling and kinesin-2 mislocalization in ccpp-1 cilia. We also identified the nekl-4(my31) suppressor, an allele affecting the NIMA (Never in Mitosis A)-related kinase NEKL-4/NEK10. In humans, NEK10 mutation causes bronchiectasis, an airway and mucociliary transport disorder caused by defective motile cilia. C. elegans NEKL-4 localizes to the ciliary base but does not localize to cilia, suggesting an indirect role in ciliary processes. This work defines a pathway in which glutamylation, a component of the Tubulin Code, is written by TTLL-4, TTLL-5, and TTLL-11; is erased by CCPP-1; is read by ciliary kinesins; and its downstream effects are modulated by NEKL-4 activity. Identification of regulators of microtubule glutamylation in diverse cellular contexts is important to the development of effective therapies for disorders characterized by changes in microtubule glutamylation. By identifying C. elegans genes important for neuronal and ciliary stability, our work may inform research into the roles of the tubulin code in human ciliopathies and neurodegenerative diseases.

Klíčová slova:

Caenorhabditis elegans – Cilia – Glutamate – Microtubules – Neuronal dendrites – Neurons – Suppressor genes – Tubulins


Zdroje

1. Reiter JF, Leroux MR. Genes and molecular pathways underpinning ciliopathies. Nat Rev Mol Cell Biol. 2017;18: 533–547. doi: 10.1038/nrm.2017.60 28698599

2. Verhey KJ, Gaertig J. The tubulin code. Cell Cycle. 2007;6: 2152–2160. doi: 10.4161/cc.6.17.4633 17786050

3. Magiera MM, Bodakuntla S, Žiak J, Lacomme S, Marques Sousa P, Leboucher S, et al. Excessive tubulin polyglutamylation causes neurodegeneration and perturbs neuronal transport. EMBO J. 2018;37. doi: 10.15252/embj.2018100440 30420556

4. Bodakuntla S, Schnitzler A, Villablanca C, Gonzalez-Billault C, Bieche I, Janke C, et al. Tubulin polyglutamylation is a general traffic control mechanism in hippocampal neurons. J Cell Sci. 2020. doi: 10.1242/jcs.241802 31932508

5. Rogowski K, van Dijk J, Magiera MM, Bosc C, Deloulme J-C, Bosson A, et al. A family of protein-deglutamylating enzymes associated with neurodegeneration. Cell. 2010;143: 564–578. doi: 10.1016/j.cell.2010.10.014 21074048

6. Kimura Y, Kurabe N, Ikegami K, Tsutsumi K, Konishi Y, Kaplan OI, et al. Identification of tubulin deglutamylase among Caenorhabditis elegans and mammalian cytosolic carboxypeptidases (CCPs). J Biol Chem. 2010;285: 22936–22941. doi: 10.1074/jbc.C110.128280 20519502

7. Janke C, Rogowski K, Wloga D, Regnard C, Kajava AV, Strub J-M, et al. Tubulin polyglutamylase enzymes are members of the TTL domain protein family. Science. 2005;308: 1758–1762. doi: 10.1126/science.1113010 15890843

8. Ikegami K, Mukai M, Tsuchida J-I, Heier RL, Macgregor GR, Setou M. TTLL7 is a mammalian beta-tubulin polyglutamylase required for growth of MAP2-positive neurites. J Biol Chem. 2006;281: 30707–30716. doi: 10.1074/jbc.M603984200 16901895

9. van Dijk J, Rogowski K, Miro J, Lacroix B, Eddé B, Janke C. A targeted multienzyme mechanism for selective microtubule polyglutamylation. Mol Cell. 2007;26: 437–448. doi: 10.1016/j.molcel.2007.04.012 17499049

10. Garnham CP, Roll-Mecak A. The chemical complexity of cellular microtubules: tubulin post-translational modification enzymes and their roles in tuning microtubule functions. Cytoskeleton. 2012;69: 442–463. Available: doi: 10.1002/cm.21027 22422711

11. Mullen RJ. Site of pcd gene action and Purkinje cell mosaicism in cerebella of chimaeric mice. Nature. 1977;270: 245–247. doi: 10.1038/270245a0 593342

12. Landis SC, Mullen RJ. The development and degeneration of Purkinje cells in pcd mutant mice. J Comp Neurol. 1978;177: 125–143. doi: 10.1002/cne.901770109 200636

13. Fernandez-Gonzalez A. Purkinje cell degeneration (pcd) Phenotypes Caused by Mutations in the Axotomy-Induced Gene, Nna1. Science. 2002. pp. 1904–1906. doi: 10.1126/science.1068912 11884758

14. Lee JE, Silhavy JL, Zaki MS, Schroth J, Bielas SL, Marsh SE, et al. CEP41 is mutated in Joubert syndrome and is required for tubulin glutamylation at the cilium. Nat Genet. 2012;44: 193–199. doi: 10.1038/ng.1078 22246503

15. Brady ST, Morfini GA. Regulation of motor proteins, axonal transport deficits and adult-onset neurodegenerative diseases. Neurobiol Dis. 2017;105: 273–282. doi: 10.1016/j.nbd.2017.04.010 28411118

16. Alexander AG, Marfil V, Li C. Use of Caenorhabditis elegans as a model to study Alzheimer’s disease and other neurodegenerative diseases. Front Genet. 2014;5: 279. doi: 10.3389/fgene.2014.00279 25250042

17. Ward S, Thomson N, White JG, Brenner S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematodecaenorhabditis elegans. The Journal of Comparative Neurology. 1975. pp. 313–337. doi: 10.1002/cne.901600305 1112927

18. Perkins LA, Hedgecock EM, Nichol Thomson J, Culotti JG. Mutant sensory cilia in the nematode Caenorhabditis elegans. Developmental Biology. 1986. pp. 456–487. doi: 10.1016/0012-1606(86)90314-3 2428682

19. Ware RW, Clark D, Crossland K, Russell RL. The nerve ring of the nematodeCaenorhabditis elegans: Sensory input and motor output. The Journal of Comparative Neurology. 1975. pp. 71–110. doi: 10.1002/cne.901610107 1133228

20. Evans JE, Snow JJ, Gunnarson AL, Ou G, Stahlberg H, McDonald KL, et al. Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans. The Journal of Cell Biology. 2006. pp. 663–669. doi: 10.1083/jcb.200509115 16492809

21. O’Hagan R, Piasecki BP, Silva M, Phirke P, Nguyen KCQ, Hall DH, et al. The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans. Curr Biol. 2011;21: 1685–1694. doi: 10.1016/j.cub.2011.08.049 21982591

22. O’Hagan R, Silva M, Nguyen KCQ, Zhang W, Bellotti S, Ramadan YH, et al. Glutamylation Regulates Transport, Specializes Function, and Sculpts the Structure of Cilia. Curr Biol. 2017;27: 3430–3441.e6. doi: 10.1016/j.cub.2017.09.066 29129530

23. Sergouniotis PI, Chakarova C, Murphy C, Becker M, Lenassi E, Arno G, et al. Biallelic variants in TTLL5, encoding a tubulin glutamylase, cause retinal dystrophy. Am J Hum Genet. 2014;94: 760–769. doi: 10.1016/j.ajhg.2014.04.003 24791901

24. Sun X, Park JH, Gumerson J, Wu Z, Swaroop A, Qian H, et al. Loss of RPGR glutamylation underlies the pathogenic mechanism of retinal dystrophy caused by TTLL5 mutations. Proc Natl Acad Sci U S A. 2016;113: E2925–34. doi: 10.1073/pnas.1523201113 27162334

25. Porpora M, Sauchella S, Rinaldi L, Delle Donne R, Sepe M, Torres-Quesada O, et al. Counterregulation of cAMP-directed kinase activities controls ciliogenesis. Nat Commun. 2018;9: 1224. doi: 10.1038/s41467-018-03643-9 29581457

26. Chivukula RR, Montoro DT, Leung HM, Yang J, Shamseldin HE, Taylor MS, et al. A human ciliopathy reveals essential functions for NEK10 in airway mucociliary clearance. Nature Medicine. 2020. doi: 10.1038/s41591-019-0730-x 31959991

27. Bompard G, van Dijk J, Cau J, Lannay Y, Marcellin G, Lawera A, et al. CSAP Acts as a Regulator of TTLL-Mediated Microtubule Glutamylation. Cell Rep. 2018;25: 2866–2877.e5. doi: 10.1016/j.celrep.2018.10.095 30517872

28. Chawla DG, Shah RV, Barth ZK, Lee JD, Badecker KE, Naik A, et al. Caenorhabditis elegans glutamylating enzymes function redundantly in male mating. Biol Open. 2016;5: 1290–1298. doi: 10.1242/bio.017442 27635036

29. WormBase: Nematode Information Resource. [cited 27 Jan 2020]. Available: https://wormbase.org//

30. T-Coffee Server. [cited 27 Jan 2020]. Available: http://tcoffee.crg.cat/apps/tcoffee/do:expresso

31. Wang J, Barr MM. Ciliary Extracellular Vesicles: Txt Msg Organelles. Cell Mol Neurobiol. 2016;36: 449–457. doi: 10.1007/s10571-016-0345-4 26983828

32. Valenstein ML, Roll-Mecak A. Graded Control of Microtubule Severing by Tubulin Glutamylation. Cell. 2016;164: 911–921. doi: 10.1016/j.cell.2016.01.019 26875866

33. Sharma N, Bryant J, Wloga D, Donaldson R, Davis RC, Jerka-Dziadosz M, et al. Katanin regulates dynamics of microtubules and biogenesis of motile cilia. J Cell Biol. 2007;178: 1065–1079. doi: 10.1083/jcb.200704021 17846175

34. Ghosh-Roy A, Goncharov A, Jin Y, Chisholm AD. Kinesin-13 and tubulin posttranslational modifications regulate microtubule growth in axon regeneration. Dev Cell. 2012;23: 716–728. doi: 10.1016/j.devcel.2012.08.010 23000142

35. Hatzfeld M. The armadillo family of structural proteins. Int Rev Cytol. 1999;186: 179–224. doi: 10.1016/s0074-7696(08)61054-2 9770300

36. EMBOSS: epestfind. [cited 27 Jan 2020]. Available: http://emboss.bioinformatics.nl/cgi-bin/emboss/epestfind

37. Rogers S, Wells R, Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science. 1986. pp. 364–368. doi: 10.1126/science.2876518 2876518

38. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215: 403–410. doi: 10.1016/S0022-2836(05)80360-2 2231712

39. Paix A, Folkmann A, Seydoux G. Precision genome editing using CRISPR-Cas9 and linear repair templates in C. elegans. Methods. 2017. pp. 86–93. doi: 10.1016/j.ymeth.2017.03.023 28392263

40. Dickinson DJ, Goldstein B. CRISPR-Based Methods for Caenorhabditis elegans Genome Engineering. Genetics. 2016. pp. 885–901. doi: 10.1534/genetics.115.182162 26953268

41. Yi P, Xie C, Ou G. The kinases male germ cell-associated kinase and cell cycle-related kinase regulate kinesin-2 motility in Caenorhabditis elegans neuronal cilia. Traffic. 2018;19: 522–535. doi: 10.1111/tra.12572 29655266

42. Haycraft CJ, Schafer JC, Zhang Q, Taulman PD, Yoder BK. Identification of CHE-13, a novel intraflagellar transport protein required for cilia formation. Exp Cell Res. 2003;284: 251–263. doi: 10.1016/s0014-4827(02)00089-7 12651157

43. Wolff A, de Néchaud B, Chillet D, Mazarguil H, Desbruyères E, Audebert S, et al. Distribution of glutamylated alpha and beta-tubulin in mouse tissues using a specific monoclonal antibody, GT335. Eur J Cell Biol. 1992;59: 425–432. Available: https://www.ncbi.nlm.nih.gov/pubmed/1493808 1493808

44. Pathak N, Obara T, Mangos S, Liu Y, Drummond IA. The Zebrafish fleer Gene Encodes an Essential Regulator of Cilia Tubulin Polyglutamylation. Molecular Biology of the Cell. 2007. pp. 4353–4364. doi: 10.1091/mbc.e07-06-0537 17761526

45. Silva M, Morsci N, Nguyen KCQ, Rizvi A, Rongo C, Hall DH, et al. Cell-Specific α-Tubulin Isotype Regulates Ciliary Microtubule Ultrastructure, Intraflagellar Transport, and Extracellular Vesicle Biology. Curr Biol. 2017;27: 968–980. doi: 10.1016/j.cub.2017.02.039 28318980

46. Scholey JM, Ou G, Snow J, Gunnarson A. Intraflagellar transport motors in Caenorhabditis elegans neurons. Biochemical Society Transactions. 2004. pp. 682–684. doi: 10.1042/BST0320682 15493987

47. Ou G, Blacque OE, Snow JJ, Leroux MR, Scholey JM. Functional coordination of intraflagellar transport motors. Nature. 2005. pp. 583–587. doi: 10.1038/nature03818 16049494

48. Prevo B, Mangeol P, Oswald F, Scholey JM, Peterman EJG. Functional differentiation of cooperating kinesin-2 motors orchestrates cargo import and transport in C. elegans cilia. Nat Cell Biol. 2015;17: 1536–1545. doi: 10.1038/ncb3263 26523365

49. Hao L, Efimenko E, Swoboda P, Scholey JM. The retrograde IFT machinery of C. elegans cilia: two IFT dynein complexes? PLoS One. 2011;6: e20995. doi: 10.1371/journal.pone.0020995 21695221

50. Imanishi M, Endres NF, Gennerich A, Vale RD. Autoinhibition regulates the motility of the C. elegans intraflagellar transport motor OSM-3. The Journal of Cell Biology. 2006. pp. 931–937. doi: 10.1083/jcb.200605179 17000874

51. Kubo T, Yanagisawa H-A, Yagi T, Hirono M, Kamiya R. Tubulin polyglutamylation regulates axonemal motility by modulating activities of inner-arm dyneins. Curr Biol. 2010;20: 441–445. doi: 10.1016/j.cub.2009.12.058 20188560

52. Lin H, Zhang Z, Guo S, Chen F, Kessler JM, Wang YM, et al. A NIMA-Related Kinase Suppresses the Flagellar Instability Associated with the Loss of Multiple Axonemal Structures. PLoS Genet. 2015;11: e1005508. doi: 10.1371/journal.pgen.1005508 26348919

53. Cohen S, Aizer A, Shav-Tal Y, Yanai A, Motro B. Nek7 kinase accelerates microtubule dynamic instability. Biochim Biophys Acta. 2013;1833: 1104–1113. doi: 10.1016/j.bbamcr.2012.12.021 23313050

54. Wloga D, Camba A, Rogowski K, Manning G, Jerka-Dziadosz M, Gaertig J. Members of the NIMA-related Kinase Family Promote Disassembly of Cilia by Multiple Mechanisms. Molecular Biology of the Cell. 2006. pp. 2799–2810. doi: 10.1091/mbc.e05-05-0450 16611747

55. Chaya T, Omori Y, Kuwahara R, Furukawa T. ICK is essential for cell type-specific ciliogenesis and the regulation of ciliary transport. EMBO J. 2014;33: 1227–1242. doi: 10.1002/embj.201488175 24797473

56. Luo M, Cao M, Kan Y, Li G, Snell W, Pan J. The phosphorylation state of an aurora-like kinase marks the length of growing flagella in Chlamydomonas. Curr Biol. 2011;21: 586–591. doi: 10.1016/j.cub.2011.02.046 21458267

57. Pan J, Wang Q, Snell WJ. An aurora kinase is essential for flagellar disassembly in Chlamydomonas. Dev Cell. 2004;6: 445–451. doi: 10.1016/s1534-5807(04)00064-4 15030766

58. Liang Y, Pang Y, Wu Q, Hu Z, Han X, Xu Y, et al. FLA8/KIF3B phosphorylation regulates kinesin-II interaction with IFT-B to control IFT entry and turnaround. Dev Cell. 2014;30: 585–597. doi: 10.1016/j.devcel.2014.07.019 25175706

59. van de Kooij B, Creixell P, van Vlimmeren A, Joughin BA, Miller CJ, Haider N, et al. Comprehensive substrate specificity profiling of the human Nek kinome reveals unexpected signaling outputs. Elife. 2019;8. doi: 10.7554/eLife.44635 31124786

60. Monteiro MI, Ahlawat S, Kowalski JR, Malkin E, Koushika SP, Juo P. The kinesin-3 family motor KLP-4 regulates anterograde trafficking of GLR-1 glutamate receptors in the ventral nerve cord of Caenorhabditis elegans. Mol Biol Cell. 2012;23: 3647–3662. doi: 10.1091/mbc.E12-04-0334 22855524

61. Lacroix B, Bourdages KG, Dorn JF, Ihara S, Sherwood DR, Maddox PS, et al. In situ imaging in C. elegans reveals developmental regulation of microtubule dynamics. Dev Cell. 2014;29: 203–216. doi: 10.1016/j.devcel.2014.03.007 24780738

62. Ou G, Koga M, Blacque OE, Murayama T, Ohshima Y, Schafer JC, et al. Sensory ciliogenesis in Caenorhabditis elegans: assignment of IFT components into distinct modules based on transport and phenotypic profiles. Mol Biol Cell. 2007;18: 1554–1569. doi: 10.1091/mbc.e06-09-0805 17314406

63. Bell LR, Stone S, Yochem J, Shaw JE, Herman RK. The molecular identities of the Caenorhabditis elegans intraflagellar transport genes dyf-6, daf-10 and osm-1. Genetics. 2006;173: 1275–1286. doi: 10.1534/genetics.106.056721 16648645

64. Qin H, Rosenbaum JL, Barr MM. An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons. Curr Biol. 2001;11: 457–461. doi: 10.1016/s0960-9822(01)00122-1 11301258

65. Bae Y-K, Qin H, Knobel KM, Hu J, Rosenbaum JL, Barr MM. General and cell-type specific mechanisms target TRPP2/PKD-2 to cilia. Development. 2006;133: 3859–3870. doi: 10.1242/dev.02555 16943275

66. Chen N, Mah A, Blacque OE, Chu J, Phgora K, Bakhoum MW, et al. Identification of ciliary and ciliopathy genes in Caenorhabditis elegans through comparative genomics. Genome Biol. 2006;7: R126. doi: 10.1186/gb-2006-7-12-r126 17187676

67. Burghoorn J, Dekkers MPJ, Rademakers S, de Jong T, Willemsen R, Jansen G. Mutation of the MAP kinase DYF-5 affects docking and undocking of kinesin-2 motors and reduces their speed in the cilia of Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2007;104: 7157–7162. doi: 10.1073/pnas.0606974104 17420466

68. Maurya AK, Rogers T, Sengupta P. A CCRK and a MAK Kinase Modulate Cilia Branching and Length via Regulation of Axonemal Microtubule Dynamics in Caenorhabditis elegans. Current Biology. 2019. pp. 1286–1300.e4. doi: 10.1016/j.cub.2019.02.062 30955935

69. Joseph BB, Wang Y, Edeen P, Lažetić V, Grant BD, Fay DS. Control of clathrin-mediated endocytosis by NIMA family kinases. PLoS Genet. 2020;16: e1008633. doi: 10.1371/journal.pgen.1008633 32069276

70. Lažetić 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 Genetics. 2018. p. e1007313. doi: 10.1371/journal.pgen.1007313 29608564

71. Lažetić 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: 273–293. doi: 10.1534/genetics.116.194464 27799278

72. Kaplan OI, Doroquez DB, Cevik S, Bowie RV, Clarke L, Sanders AAWM, et al. Endocytosis Genes Facilitate Protein and Membrane Transport in C. elegans Sensory Cilia. Curr Biol. 2012;22: 451–460. doi: 10.1016/j.cub.2012.01.060 22342749

73. Vaart A van der, van der Vaart A, Rademakers S, Jansen G. DLK-1/p38 MAP Kinase Signaling Controls Cilium Length by Regulating RAB-5 Mediated Endocytosis in Caenorhabditis elegans. PLOS Genetics. 2015. p. e1005733. doi: 10.1371/journal.pgen.1005733 26657059

74. Kubo T, Hirono M, Aikawa T, Kamiya R, Witman GB. Reduced tubulin polyglutamylation suppresses flagellar shortness in Chlamydomonas. Mol Biol Cell. 2015;26: 2810–2822. doi: 10.1091/mbc.E15-03-0182 26085508

75. Hao L, Thein M, Brust-Mascher I, Civelekoglu-Scholey G, Lu Y, Acar S, et al. Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments. Nat Cell Biol. 2011;13: 790–798. doi: 10.1038/ncb2268 21642982

76. Das A, Dickinson D, Wood C, Goldstein B, Slep KC. The CHE-12 protein family uses a TOG domain array to regulate microtubules in the primary cilium. MOLECULAR BIOLOGY OF THE CELL. AMER SOC CELL BIOLOGY 8120 WOODMONT AVE, STE 750, BETHESDA, MD 20814–2755 USA; 2014.

77. Sanders A, Cevik S, Kida K, Bowie R, Blacque O. Investigation of a novel cilia-related gene K04F10.2/KIAA0556 in C. elegans. Cilia. 2012. doi: 10.1186/2046-2530-1-s1-p43

78. Chang J, Baloh RH, Milbrandt J. The NIMA-family kinase Nek3 regulates microtubule acetylation in neurons. J Cell Sci. 2009;122: 2274–2282. doi: 10.1242/jcs.048975 19509051

79. O’regan L, Blot J, Fry AM. Mitotic regulation by NIMA-related kinases. Cell Div. 2007;2: 25. doi: 10.1186/1747-1028-2-25 17727698

80. Jackson PK. Nek8 couples renal ciliopathies to DNA damage and checkpoint control. Molecular cell. 2013. pp. 407–408. doi: 10.1016/j.molcel.2013.08.013 23973371

81. Bryan MS, Argos M, Andrulis IL, Hopper JL, Chang-Claude J, Malone KE, et al. Germline Variation and Breast Cancer Incidence: A Gene-Based Association Study and Whole-Genome Prediction of Early-Onset Breast Cancer. Cancer Epidemiol Biomarkers Prev. 2018;27: 1057–1064. doi: 10.1158/1055-9965.EPI-17-1185 29898891

82. Keller BM, McCarthy AM, Chen J, Armstrong K, Conant EF, Domchek SM, et al. Associations between breast density and a panel of single nucleotide polymorphisms linked to breast cancer risk: a cohort study with digital mammography. BMC Cancer. 2015;15: 143. doi: 10.1186/s12885-015-1159-3 25881232

83. García-Díez I, Hernández-Muñoz I, Hernández-Ruiz E, Nonell L, Puigdecanet E, Bódalo-Torruella M, et al. Transcriptome and cytogenetic profiling analysis of matched in situ/invasive cutaneous squamous cell carcinomas from immunocompetent patients. Genes Chromosomes Cancer. 2019;58: 164–174. Available: https://onlinelibrary.wiley.com/doi/abs/10.1002/gcc.22712 doi: 10.1002/gcc.22712 30474248

84. 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: 1824–1835. doi: 10.1093/hmg/ddw054 26908619

85. Mahjoub MR, Montpetit B, Zhao L, Finst RJ, Goh B, Kim AC, et al. The FA2 gene of Chlamydomonas encodes a NIMA family kinase with roles in cell cycle progression and microtubule severing during deflagellation. J Cell Sci. 2002;115: 1759–1768. Available: https://www.ncbi.nlm.nih.gov/pubmed/11950892 11950892

86. Bradley BA. A NIMA-related kinase, Cnk2p, regulates both flagellar length and cell size in Chlamydomonas. Journal of Cell Science. 2005. pp. 3317–3326. doi: 10.1242/jcs.02455 16030138

87. Westermann S, Weber K. Identification of CfNek, a novel member of the NIMA family of cell cycle regulators, as a polypeptide copurifying with tubulin polyglutamylation activity in Crithidia. J Cell Sci. 2002;115: 5003–5012. doi: 10.1242/jcs.00170 12432086

88. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77: 71–94. Available: https://www.ncbi.nlm.nih.gov/pubmed/4366476 4366476

89. WormBook. [cited 27 Jan 2020]. Available: http://wormbook.org/

90. Doitsidou M, Jarriault S, Poole RJ. Next-Generation Sequencing-Based Approaches for Mutation Mapping and Identification in Caenorhabditis elegans. Genetics. 2016;204: 451–474. doi: 10.1534/genetics.115.186197 27729495

91. Wang Y, Wang JT, Rasoloson D, Stitzel ML, O’ Connell KF, Smith HE, et al. Identification of suppressors of mbk-2/DYRK by whole-genome sequencing. G3. 2014;4: 231–241. doi: 10.1534/g3.113.009126 24347622

92. Homer N. Bfast: Blat-like fast accurate search tool. 2009. Available: https://vcru.wisc.edu/simonlab/bioinformatics/programs/bfast/bfast-book.pdf

93. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009. pp. 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943

94. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38: e164. doi: 10.1093/nar/gkq603 20601685

95. Huang S, Holt J, -Y. Kao C, McMillan L, Wang W. A novel multi-alignment pipeline for high-throughput sequencing data. Database. 2014. pp. bau057–bau057. doi: 10.1093/database/bau057 24948510

96. UniProt. [cited 27 Jan 2020]. Available: https://www.uniprot.org/

97. interpro7-client. [cited 27 Jan 2020]. Available: https://www.ebi.ac.uk/interpro/

98. ScanProsite. [cited 27 Jan 2020]. Available: https://prosite.expasy.org/scanprosite/

99. Protein BLAST: search protein databases using a protein query. [cited 27 Jan 2020]. Available: https://blast.ncbi.nlm.nih.gov/Blast.cgi?PAGE=Proteins

100. WormWeb.org—Exon-Intron Graphic Maker—by nikhil bhatla. [cited 27 Jan 2020]. Available: http://wormweb.org/exonintron

101. DOG 2.0—Protein Domain Structure Visualization. [cited 27 Jan 2020]. Available: http://dog.biocuckoo.org/

102. Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X. DOG 1.0: illustrator of protein domain structures. Cell Res. 2009;19: 271–273. doi: 10.1038/cr.2009.6 19153597

103. BoxShade Server. [cited 27 Jan 2020]. Available: https://embnet.vital-it.ch/software/BOX_form.html

104. Kimura Y, Tsutsumi K, Konno A, Ikegami K, Hameed S, Kaneko T, et al. Environmental responsiveness of tubulin glutamylation in sensory cilia is regulated by the p38 MAPK pathway. Sci Rep. 2018;8: 8392. doi: 10.1038/s41598-018-26694-w 29849065

105. ImageJ. [cited 27 Jan 2020]. Available: https://imagej.net/Welcome

106. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA 3rd, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6: 343–345. doi: 10.1038/nmeth.1318 19363495

107. Dokshin GA, Ghanta KS, Piscopo KM, Mello CC. Robust Genome Editing with Short Single-Stranded and Long, Partially Single-Stranded DNA Donors in Caenorhabditis elegans. Genetics. 2018;210: 781–787. doi: 10.1534/genetics.118.301532 30213854

108. Paix A, Folkmann A, Goldman DH, Kulaga H, Grzelak MJ, Rasoloson D, et al. Precision genome editing using synthesis-dependent repair of Cas9-induced DNA breaks. Proc Natl Acad Sci U S A. 2017;114: E10745–E10754. doi: 10.1073/pnas.1711979114 29183983

109. Haeussler M, Schönig K, Eckert H, Eschstruth A, Mianné J, Renaud J-B, et al. Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR. Genome Biol. 2016;17: 148. doi: 10.1186/s13059-016-1012-2 27380939

110. CRISPOR. [cited 27 Jan 2020]. Available: http://crispor.tefor.net/

111. WatCut: An on-line tool for restriction analysis, silent mutation scanning, SNP-RFLP analysis. [cited 27 Jan 2020]. Available: http://watcut.uwaterloo.ca/template.php?act=silent_new

112. Connolly AA, Osterberg V, Christensen S, Price M, Lu C, Chicas-Cruz K, et al. Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1. Mol Biol Cell. 2014;25: 1298–1311. doi: 10.1091/mbc.E13-11-0687 24554763


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PLOS Genetics


2020 Číslo 10

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