Mutations in PIH proteins MOT48, TWI1 and PF13 define common and unique steps for preassembly of each, different ciliary dynein
Autoři:
Ryosuke Yamamoto aff001; Shiho Yanagi aff001; Masahito Nagao aff001; Yuya Yamasaki aff001; Yui Tanaka aff001; Winfield S. Sale aff002; Toshiki Yagi aff003; Takahide Kon aff001
Působiště autorů:
Department of Biological Sciences, Graduate School of Science, Osaka University, Osaka, Japan
aff001; Department of Cell Biology, School of Medicine, Emory University, Atlanta, Georgia, United States of America
aff002; Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Shobara, Hiroshima, Japan
aff003
Vyšlo v časopise:
Mutations in PIH proteins MOT48, TWI1 and PF13 define common and unique steps for preassembly of each, different ciliary dynein. PLoS Genet 16(11): e1009126. doi:10.1371/journal.pgen.1009126
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009126
Souhrn
Ciliary dyneins are preassembled in the cytoplasm before being transported into cilia, and a family of proteins containing the PIH1 domain, PIH proteins, are involved in the assembly process. However, the functional differences and relationships between members of this family of proteins remain largely unknown. Using Chlamydomonas reinhardtii as a model, we isolated and characterized two novel Chlamydomonas PIH preassembly mutants, mot48-2 and twi1-1. A new allele of mot48 (ida10), mot48-2, shows large defects in ciliary dynein assembly in the axoneme and altered motility. A second mutant, twi1-1, shows comparatively smaller defects in motility and dynein assembly. A double mutant mot48-2; twi1-1 displays greater reduction in motility and in dynein assembly compared to each single mutant. Similarly, a double mutant twi1-1; pf13 also shows a significantly greater defect in motility and dynein assembly than either parent mutant. Thus, MOT48 (IDA10), TWI1 and PF13 may define different steps, and have partially overlapping functions, in a pathway required for ciliary dynein preassembly. Together, our data suggest the three PIH proteins function in preassembly steps that are both common and unique for different ciliary dyneins.
Klíčová slova:
Cilia – Cytoplasm – Dyneins – Chlamydomonas reinhardtii – Immunoblotting – Motor proteins – Phenotypes – Swimming
Zdroje
1. Ishikawa T. Axoneme Structure from Motile Cilia. Cold Spring Harb Perspect Biol. 2017;9(1):a028076. doi: 10.1101/cshperspect.a028076 27601632
2. Satir P. CILIA: before and after. Cilia. 2017;6:1. doi: 10.1186/s13630-017-0046-8 28293419
3. Zariwala MA, Omran H, Ferkol TW. The emerging genetics of primary ciliary dyskinesia. Proc Am Thorac Soc. 2011;8(5):430–3. doi: 10.1513/pats.201103-023SD 21926394
4. Chodhari R, Mitchison HM, Meeks M. Cilia, primary ciliary dyskinesia and molecular genetics. Paediatr Respir Rev. 2004;5(1):69–76. doi: 10.1016/j.prrv.2003.09.005 15222957
5. Rubbo B, Lucas JS. Clinical care for primary ciliary dyskinesia: current challenges and future directions. Eur Respir Rev. 2017;26(145):170023. doi: 10.1183/16000617.0023-2017 28877972
6. Horani A, Ferkol TW. Advances in the Genetics of Primary Ciliary Dyskinesia: Clinical Implications. Chest. 2018;154(3):645–52. doi: 10.1016/j.chest.2018.05.007 29800551
7. Viswanadha R, Sale WS, Porter ME. Ciliary Motility: Regulation of Axonemal Dynein Motors. Cold Spring Harb Perspect Biol. 2017;9(8):a018325. doi: 10.1101/cshperspect.a018325 28765157
8. Kamiya R, Yagi T. Functional diversity of axonemal dyneins as assessed by in vitro and in vivo motility assays of Chlamydomonas mutants. Zoolog Sci. 2014;31(10):633–44. doi: 10.2108/zs140066 25284382
9. King SM. Axonemal Dynein Arms. Cold Spring Harb Perspect Biol. 2016;8(11):a028100. doi: 10.1101/cshperspect.a028100 27527589
10. Brokaw CJ, Kamiya R. Bending patterns of Chlamydomonas flagella: IV. Mutants with defects in inner and outer dynein arms indicate differences in dynein arm function. Cell Motil Cytoskeleton. 1987;8(1):68–75. doi: 10.1002/cm.970080110 2958145
11. Fowkes ME, Mitchell DR. The role of preassembled cytoplasmic complexes in assembly of flagellar dynein subunits. Mol Biol Cell. 1998;9(9):2337–47. doi: 10.1091/mbc.9.9.2337 9725897
12. Viswanadha R, Hunter EL, Yamamoto R, Wirschell M, Alford LM, Dutcher SK, et al. The ciliary inner dynein arm, I1 dynein, is assembled in the cytoplasm and transported by IFT before axonemal docking. Cytoskeleton (Hoboken). 2014;71(10):573–86. doi: 10.1002/cm.21192 25252184
13. Yamamoto R, Hirono M, Kamiya R. Discrete PIH proteins function in the cytoplasmic preassembly of different subsets of axonemal dyneins. J Cell Biol. 2010;190(1):65–71. doi: 10.1083/jcb.201002081 20603327
14. Kobayashi D, Takeda H. Ciliary motility: the components and cytoplasmic preassembly mechanisms of the axonemal dyneins. Differentiation. 2012;83(2):S23–9. doi: 10.1016/j.diff.2011.11.009 22154137
15. Desai PB, Dean AB, Mitchell DR. Cytoplasmic preassembly and trafficking of axonemal dyneins: Dyneins (The Biology of Dynein Motors). 2nd Edition ed: Academic Press; 2017. 684 p.
16. Mitchison HM, Schmidts M, Loges NT, Freshour J, Dritsoula A, Hirst RA, et al. Mutations in axonemal dynein assembly factor DNAAF3 cause primary ciliary dyskinesia. Nat Genet. 2012;44(4):381–9, s1-2. doi: 10.1038/ng.1106 22387996
17. Omran H, Kobayashi D, Olbrich H, Tsukahara T, Loges NT, Hagiwara H, et al. Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins. Nature. 2008;456(7222):611–16. doi: 10.1038/nature07471 19052621
18. Olcese C, Patel MP, Shoemark A, Kiviluoto S, Legendre M, Williams HJ, et al. X-linked primary ciliary dyskinesia due to mutations in the cytoplasmic axonemal dynein assembly factor PIH1D3. Nat Commun. 2017;8:14279. doi: 10.1038/ncomms14279 28176794
19. Paff T, Loges NT, Aprea I, Wu K, Bakey Z, Haarman EG, et al. Mutations in PIH1D3 cause X-linked primary ciliary dyskinesia with outer and inner dynein arm defects. Am J Hum Genet. 2017;100(1):160–8. doi: 10.1016/j.ajhg.2016.11.019 28041644
20. Tarkar A, Loges NT, Slagle CE, Francis R, Dougherty GW, Tamayo JV, et al. DYX1C1 is required for axonemal dynein assembly and ciliary motility. Nat Genet. 2013;45(9):995–1003. doi: 10.1038/ng.2707 23872636
21. Dong F, Shinohara K, Botilde Y, Nabeshima R, Asai Y, Fukumoto A, et al. Pih1d3 is required for cytoplasmic preassembly of axonemal dynein in mouse sperm. J Cell Biol. 2014;204(2):203–13. doi: 10.1083/jcb.201304076 24421334
22. Yamaguchi H, Oda T, Kikkawa M, Takeda H. Systematic studies of all PIH proteins in zebrafish reveal their distinct roles in axonemal dynein assembly. Elife. 2018;7:e36979. doi: 10.7554/eLife.36979 29741156
23. Huizar RL, Lee C, Boulgakov AA, Horani A, Tu F, Marcotte EM, et al. A liquid-like organelle at the root of motile ciliopathy. Elife. 2018;7:e38497. doi: 10.7554/eLife.38497 30561330
24. Li X, Zhang R, Patena W, Gang SS, Blum SR, Ivanova N, et al. An indexed, mapped mutant library enables reverse genetics studies of biological processes in Chlamydomonas reinhardtii. Plant Cell. 2016;28(2):367–87. doi: 10.1105/tpc.15.00465 26764374
25. Liu G, Wang L, Pan J. Chlamydomonas WDR92 in association with R2TP-like complex and multiple DNAAFs to regulate ciliary dynein preassembly. J Mol Cell Biol. 2019;11(9):770–80. doi: 10.1093/jmcb/mjy067 30428028
26. Hom EF, Witman GB, Harris EH, Dutcher SK, Kamiya R, Mitchell DR, et al. A unified taxonomy for ciliary dyneins. Cytoskeleton (Hoboken). 2011;68(10):555–65. doi: 10.1002/cm.20533 21953912
27. Fabczak H, Osinka A. Role of the novel Hsp90 co-chaperones in dynein arms' preassembly. Int J Mol Sci. 2019;20(24):6174. doi: 10.3390/ijms20246174 31817850
28. Yamamoto R, Obbineni JM, Alford LM, Ide T, Owa M, Hwang J, et al. Chlamydomonas DYX1C1/PF23 is essential for axonemal assembly and proper morphology of inner dynein arms. PLoS Genet. 2017;13(9):e1006996. doi: 10.1371/journal.pgen.1006996 28892495
29. Zhao R, Kakihara Y, Gribun A, Huen J, Yang G, Khanna M, et al. Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J Cell Biol. 2008;180(3):563–78. doi: 10.1083/jcb.200709061 18268103
30. Pal M, Morgan M, Phelps SEL, Roe SM, Parry-Morris S, Downs JA, et al. Structural basis for phosphorylation-dependent recruitment of Tel2 to Hsp90 by Pih1. Structure (London, England: 1993). 2014;22(6):805–18. doi: 10.1016/j.str.2014.04.001 24794838
31. King SM. 7—Composition and Assembly of Axonemal Dyneins. In: King SM, editor. Dyneins. Boston: Academic Press; 2012. p. 208–43.
32. Huang B, Piperno G, Luck DJ. Paralyzed flagella mutants of Chlamydomonas reinhardtii. Defective for axonemal doublet microtubule arms. J Biol Chem. 1979;254(8):3091–9. 429335
33. Stolc V, Samanta MP, Tongprasit W, Marshall WF. Genome-wide transcriptional analysis of flagellar regeneration in Chlamydomonas reinhardtii identifies orthologs of ciliary disease genes. Proc Natl Acad Sci U S A. 2005;102(10):3703–7. doi: 10.1073/pnas.0408358102 15738400
34. King SM, Patel-King RS. The oligomeric outer dynein arm assembly factor CCDC103 is tightly integrated within the ciliary axoneme and exhibits periodic binding to microtubules. J Biol Chem. 2015;290(12):7388–401. doi: 10.1074/jbc.M114.616425 25572396
35. Kim KS, Kustu S, Inwood W. Natural history of transposition in the green alga Chlamydomonas reinhardtii: use of the AMT4 locus as an experimental system. Genetics. 2006;173(4):2005–19. doi: 10.1534/genetics.106.058263 16702425
36. Bui KH, Yagi T, Yamamoto R, Kamiya R, Ishikawa T. Polarity and asymmetry in the arrangement of dynein and related structures in the Chlamydomonas axoneme. J Cell Biol. 2012;198(5):913–25. doi: 10.1083/jcb.201201120 22945936
37. Yagi T, Uematsu K, Liu Z, Kamiya R. Identification of dyneins that localize exclusively to the proximal portion of Chlamydomonas flagella. J Cell Sci. 2009;122(9):1306–14. doi: 10.1242/jcs.045096 19351714
38. Horani A, Ustione A, Huang T, Firth AL, Pan J, Gunsten SP, et al. Establishment of the early cilia preassembly protein complex during motile ciliogenesis. Proc Natl Acad Sci U S A. 2018;115(6):E1221–28. doi: 10.1073/pnas.1715915115 29358401
39. Mali GR, Yeyati PL, Mizuno S, Dodd DO, Tennant PA, Keighren MA, et al. ZMYND10 functions in a chaperone relay during axonemal dynein assembly. Elife. 2018;7:e34389. doi: 10.7554/eLife.34389 29916806
40. Zur Lage P, Stefanopoulou P, Styczynska-Soczka K, Quinn N, Mali G, von Kriegsheim A, et al. Ciliary dynein motor preassembly is regulated by Wdr92 in association with HSP90 co-chaperone, R2TP. J Cell Biol. 2018;217(7):2583–98. doi: 10.1083/jcb.201709026 29743191
41. Kakihara Y, Houry WA. The R2TP complex: discovery and functions. Biochim Biophys Acta. 2012;1823(1):101–7. doi: 10.1016/j.bbamcr.2011.08.016 21925213
42. Maurizy C, Quinternet M, Abel Y, Verheggen C, Santo PE, Bourguet M, et al. The RPAP3-Cterminal domain identifies R2TP-like quaternary chaperones. Nat Commun. 2018;9(1):2093. doi: 10.1038/s41467-018-04431-1 29844425
43. Patel-King RS, Sakato-Antoku M, Yankova M, King SM. WDR92 is required for axonemal dynein heavy chain stability in cytoplasm. Mol Biol Cell. 2019;30(15):1834–45. doi: 10.1091/mbc.E19-03-0139 31116681
44. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science. 2007;318(5848):245–50. doi: 10.1126/science.1143609 17932292
45. Harris EH. The Chlamydomonas sourcebook: a comprehensive guide to biology and laboratory use: Academic Press, San Diego, 780pp; 1989.
46. Craige B, Brown JM, Witman GB. Isolation of Chlamydomonas flagella. Curr Protoc Cell Biol. 2013;Chapter 3:Unit 3.41.1–9. doi: 10.1002/0471143030.cb0341s59 23728744
47. Bölling C, Fiehn O. Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiol. 2005;139(4):1995–2005. doi: 10.1104/pp.105.071589 16306140
48. Shimogawara K, Fujiwara S, Grossman A, Usuda H. High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics. 1998;148(4):1821–8. 9560396
49. Fischer N, Rochaix JD. The flanking regions of PsaD drive efficient gene expression in the nucleus of the green alga Chlamydomonas reinhardtii. Mol Genet Genomics. 2001;265(5):888–94. doi: 10.1007/s004380100485 11523806
50. Wirschell M, Olbrich H, Werner C, Tritschler D, Bower R, Sale WS, et al. The nexin-dynein regulatory complex subunit DRC1 is essential for motile cilia function in algae and humans. Nat Genet. 2013;45(3):262–8. doi: 10.1038/ng.2533 23354437
51. Lin J, Le TV, Augspurger K, Tritschler D, Bower R, Fu G, et al. FAP57/WDR65 targets assembly of a subset of inner arm dyneins and connects to regulatory hubs in cilia. Mol Biol Cell. 2019;30(21):2659–80. doi: 10.1091/mbc.E19-07-0367 31483737
52. Lechtreck KF, Witman GB. Chlamydomonas reinhardtii hydin is a central pair protein required for flagellar motility. J Cell Biol. 2007;176(4):473–82. doi: 10.1083/jcb.200611115 17296796
53. Tang W-JY. Chapter 5 Blot-Affinity Purification of Antibodies. In: Asai DJ, editor. Methods Cell Biol. 37: Academic Press; 1993. p. 95–104. doi: 10.1016/s0091-679x(08)60245-9 8255253
54. Grodzki AC, Berenstein E. Antibody purification: affinity chromatography—protein A and protein G Sepharose. Methods Mol Biol. 2010;588:33–41. doi: 10.1007/978-1-59745-324-0_5 20012816
55. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–5. doi: 10.1038/227680a0 5432063
56. Kurien BT, Scofield RH. Western blotting. Methods. 2006;38(4):283–93. doi: 10.1016/j.ymeth.2005.11.007 16483794
57. Kato-Minoura T, Hirono M, Kamiya R. Chlamydomonas inner-arm dynein mutant, ida5, has a mutation in an actin-encoding gene. J Cell Biol. 1997;137(3):649–56. doi: 10.1083/jcb.137.3.649 9151671
58. LeDizet M, Piperno G. The light chain p28 associates with a subset of inner dynein arm heavy chains in Chlamydomonas axonemes. Mol Biol Cell. 1995;6(6):697–711. doi: 10.1091/mbc.6.6.697 7579689
59. Yamamoto R, Yanagisawa HA, Yagi T, Kamiya R. A novel subunit of axonemal dynein conserved among lower and higher eukaryotes. FEBS Lett. 2006;580(27):6357–60. doi: 10.1016/j.febslet.2006.10.047 17094970
60. Hendrickson TW, Perrone CA, Griffin P, Wuichet K, Mueller J, Yang P, et al. IC138 is a WD-repeat dynein intermediate chain required for light chain assembly and regulation of flagellar bending. Mol Biol Cell. 2004;15(12):5431–42. doi: 10.1091/mbc.e04-08-0694 15469982
61. King SM, Otter T, Witman GB. Characterization of monoclonal antibodies against Chlamydomonas flagellar dyneins by high-resolution protein blotting. Proc Natl Acad Sci U S A. 1985;82(14):4717–21. doi: 10.1073/pnas.82.14.4717 3161075
62. Sanders MA, Salisbury JL. Immunofluorescence microscopy of cilia and flagella. Methods Cell Biol. 1995;47:163–9. doi: 10.1016/s0091-679x(08)60805-5 7476482
63. Jarvik JW, Rosenbaum JL. Oversized flagellar membrane protein in paralyzed mutants of Chlamydomonas reinhardrii. J Cell Biol. 1980;85(2):258–72. doi: 10.1083/jcb.85.2.258 7372708
64. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5. doi: 10.1038/nmeth.2089 22930834
65. Yamamoto R, Yagi T, Kamiya R. Functional binding of inner-arm dyneins with demembranated flagella of Chlamydomonas mutants. Cell Motil Cytoskeleton. 2006;63(5):258–65. doi: 10.1002/cm.20121 16518818
66. Piperno G. Regulation of dynein activity within Chlamydomonas flagella. Cell Motil Cytoskeleton. 1995;32(2):103–5. doi: 10.1002/cm.970320206 8681388
67. Kagami O, Kamiya R. Translocation and rotation of microtubules caused by multiple species of Chlamydomonas inner-arm dynein. J Cell Sci. 1992;103(3):653–64.
68. Sakakibara H, Takada S, King SM, Witman GB, Kamiya R. A Chlamydomonas outer arm dynein mutant with a truncated beta heavy chain. J Cell Biol. 1993;122(3):653–61. doi: 10.1083/jcb.122.3.653 8335691
69. Liu Z, Takazaki H, Nakazawa Y, Sakato M, Yagi T, Yasunaga T, et al. Partially functional outer-arm dynein in a novel Chlamydomonas mutant expressing a truncated gamma heavy chain. Eukaryot Cell. 2008;7(7):1136–45. doi: 10.1128/EC.00102-08 18487347
70. Myster SH, Knott JA, O'Toole E, Porter ME. The Chlamydomonas Dhc1 gene encodes a dynein heavy chain subunit required for assembly of the I1 inner arm complex. Mol Biol Cell. 1997;8(4):607–20. doi: 10.1091/mbc.8.4.607 9247642
71. Perrone CA, Myster SH, Bower R, O'Toole ET, Porter ME. Insights into the structural organization of the I1 inner arm dynein from a domain analysis of the 1beta dynein heavy chain. Mol Biol Cell. 2000;11(7):2297–313. doi: 10.1091/mbc.11.7.2297 10888669
72. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–25. doi: 10.1093/oxfordjournals.molbev.a040454 3447015
73. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39(4):783–91. doi: 10.1111/j.1558-5646.1985.tb00420.x 28561359
74. Nei M, Kumar S. Molecular Evolution and Phylogenetics: Oxford University Press, New York; 2000.
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 11
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- „Jednohubky“ z klinického výzkumu – 2024/44
Nejčtenější v tomto čísle
- Stability of SARS-CoV-2 phylogenies
- Formal commentary
- No association between SCN9A and monogenic human epilepsy disorders
- Oxidative stress antagonizes fluoroquinolone drug sensitivity via the SoxR-SUF Fe-S cluster homeostatic axis