Detailed structural and biochemical characterization of the nexin-dynein regulatory complex

Molecular Biology of the Cell

Volumn 26, Issue 2, 2015, Pages 294-304

  Oda, Toshiyuki ^a   Yanagisawa, Haruaki ^a   Kikkawa, Masahide ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NEXIN DYNEIN REGULATORY COMPLEX PROTEIN; PROTEIN; PROTEIN DRC1; PROTEIN DRC2; PROTEIN DRC4; UNCLASSIFIED DRUG; ACETYL COENZYME A CARBOXYLASE; ALGAL PROTEIN; AXONEMAL DYNEIN; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE NEXIN; MULTIPROTEIN COMPLEX; PROTEIN SUBUNIT;

ARTICLE; AXONEME; BINDING AFFINITY; CHEMICAL LABELING; CHLAMYDOMONAS REINHARDTII; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; EUKARYOTIC FLAGELLUM; FLAGELLUM; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SUBUNIT; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON MICROSCOPY; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOBLOTTING; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE;

ACETYL-COA CARBOXYLASE; ALGAL PROTEINS; AMINO ACID SEQUENCE; AXONEMAL DYNEINS; AXONEME; CHLAMYDOMONAS REINHARDTII; FLAGELLA; IMMUNOBLOTTING; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MUTATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

EID: 84920971273     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-09-1367     Document Type: Article

References (42)

1. Austin-Tse C, Halbritter J, Zariwala MA, Gilberti RM, Gee HY, Hellman N, Pathak N, Liu Y, Panizzi JR, Patel-King RS, et al. (2013). Zebrafish ciliopathy screen plus human mutational analysis identifies C21orf59 and CCDC65 defects as causing primary ciliary dyskinesia. Am J Hum Genet 93, 672-686.
2. Badano JL, Mitsuma N, Beales PL, Katsanis N (2006). The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 7, 125-148.
3. Bower R, Tritschler D, Vanderwaal K, Perrone CA, Mueller J, Fox L, Sale WS, Porter ME (2013). The N-DRC forms a conserved biochemical complex that maintains outer doublet alignment and limits microtubule sliding in motile axonemes. Mol Biol Cell 24, 1134-1152.
4. Burgess WH (1982). Characterization of calmodulin and calmodulin isotypes from sea urchin gametes. J Biol Chem 257, 1800-1804.
5. Drummond IA (2012). Cilia functions in development. Curr Opin Cell Biol 24, 24-30.
6. Fliegauf M, Benzing T, Omran H (2007). When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8, 880-893.
7. Furuta A, Yagi T, Yanagisawa HA, Higuchi H, Kamiya R (2009). Systematic comparison of in vitro motile properties between Chlamydomonas wild-type and mutant outer arm dyneins each lacking one of the three heavy chains. J Biol Chem 284, 5927-5935.
8. Gardner LC, O'Toole E, Perrone CA, Giddings T, Porter ME (1994). Components of a "dynein regulatory complex" are located at the junction between the radial spokes and the dynein arms in Chlamydomonas flagella. J Cell Biol 127, 1311-1325.
9. Goodenough UW, Heuser JE (1985). Outer and inner dynein arms of cilia and flagella. Cell 41, 341-342.
10. Haimo LT, Rosenbaum JL (1981). Cilia, flagella, and microtubules. J Cell Biol 91, 125s-130s.
11. Heuser T, Raytchev M, Krell J, Porter ME, Nicastro D (2009). The dynein regulatory complex is the nexin link and a major regulatory node in cilia and flagella. J Cell Biol 187, 921-933.
12. Huang B, Ramanis Z, Luck DJ (1982). Suppressor mutations in Chlamydomonas reveal a regulatory mechanism for Flagellar function. Cell 28, 115-124.
13. Kamiya R (1988). Mutations at twelve independent loci result in absence of outer dynein arms in Chylamydomonas reinhardtii. J Cell Biol 107, 2253-2258.
14. Kato T, Kagami O, Yagi T, Kamiya R (1993). Isolation of two species of Chlamydomonas reinhardtii flagellar mutants, ida5 and ida6, that lack a newly identified heavy chain of the inner dynein arm. Cell Struct Funct 18, 371-377.
15. Kikkawa M (2013). Big steps toward understanding dynein. J Cell Biol 202, 15-23.
16. King SM (2011). Composition and assembly of axonemal dyneins. In: Dyneins: Structure, Biology and Disease, ed. SM King, Boston: Academic Press, 208-243.
17. King SM, Kamiya R (2009). Axonemal dyneins: assembly, structure, and force generation. In: The Chlamydomonas Sourcebook, Vol. 3, 2nd ed., ed. GB Witman, Oxford, UK: Academic Press, 144-145.
18. King SM, Witman GB (1989). Molecular structure of Chlamydomonas outer arm dynein. In: Cell Movements, Vol. 1: The Dynein ATPases, ed. FD Warner, P Satir, and IR Gibbons, New York: Alan R. Liss, 61-75.
19. Kremer JR, Mastronarde DN, McIntosh JR (1996). Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116, 71-76.
20. Lin J, Tritschler D, Song K, Barber CF, Cobb JS, Porter ME, Nicastro D (2011). Building blocks of the nexin-dynein regulatory complex in Chlamydomonas flagella. J Biol Chem 286, 29175-29191.
21. Lindemann CB, Macauley LJ, Lesich KA (2005). The counterbend phenomenon in dynein-disabled rat sperm flagella and what it reveals about the interdoublet elasticity. Biophys J 89, 1165-1174.
22. Lupas A, Van, Dyke M, Stock J (1991). Predicting coiled coils from protein sequences. Science 252, 1162-1164.
23. Metlagel Z, Kikkawa YS, Kikkawa M (2007). Ruby-Helix: an implementation of helical image processing based on object-oriented scripting language. J Struct Biol 157, 95-105.
24. Minoura I, Yagi T, Kamiya R (1999). Direct measurement of inter-doublet elasticity in flagellar axonemes. Cell Struct Funct 24, 27-33.
25. Nicastro D, Schwartz C, Pierson J, Gaudette R, Porter ME, McIntosh JR (2006). The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313, 944-948.
26. Oda T, Kikkawa M (2013). Novel structural labeling method using cryo-electron tomography and biotin-streptavidin system. J Struct Biol 183, 305-311.
27. Oda T, Yagi T, Yanagisawa H, Kikkawa M (2013). Identification of the outer-inner dynein linker as a hub controller for axonemal dynein activities. Curr Biol 23, 656-664.
28. Oda T, Yanagisawa H, Kamiya R, Kikkawa M (2014a). Cilia and flagella molecular ruler determines the repeat length in eukaryotic cilia and flagella. Science 346, 857-886.
29. Oda T, Yanagisawa H, Yagi T, Kikkawa M (2014b). Mechanosignaling between central apparatus and radial spokes controls axonemal dynein activity. J Cell Biol 204, 807-819.
30. Pazour GJ, Rosenbaum JL (2002). Intraflagellar transport and cilia-dependent diseases. Trends Cell Biol 12, 551-555.
31. Perrone CA, Yang P, O'Toole E, Sale WS, Porter ME (1998). The Chlamydomonas IDA7 locus encodes a 140-kDa dynein intermediate chain required to assemble the I1 inner arm complex. Mol Biol Cell 9, 3351-3365.
32. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004). UCSF Chimera-A visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612.
33. Piperno G, Huang B, Luck DJ (1977). Two-dimensional analysis of flagellar proteins from wild-type and paralyzed mutants of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 74, 1600-1604.
34. Piperno G, Ramanis Z, Smith EF, Sale WS (1990). Three distinct inner dynein arms in Chlamydomonas flagella: molecular composition and location in the axoneme. J Cell Biol 110, 379-389.
35. Rupp G, Porter ME (2003). A subunit of the dynein regulatory complex in Chlamydomonas is a homologue of a growth arrest-specific gene product. J Cell Biol 162, 47-57.
36. Schleicher M, Watterson DM (1983). Analysis of differences between coomassie blue stain and silver stain procedures in polyacrylamide gels: conditions for the detection of calmodulin and troponin C. Anal Biochem 131, 312-317.
37. Summers KE, Gibbons IR (1971). Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea-urchin sperm. Proc Natl Acad Sci USA 68, 3092-3096.
38. Warner FD (1976). Ciliary inter-microtubule bridges. J Cell Sci 20, 101-114.
39. Weber C, Lee VD, Chazin WJ, Huang B (1994). High level expression in Escherichia coli and characterization of the EF-hand calcium-binding protein caltractin. J Biol Chem 269, 15795-15802.
40. Wirschell M, Olbrich H, Werner C, Tritschler D, Bower R, Sale WS, Loges NT, Pennekamp P, Lindberg S, Stenram U, et al. (2013). The nexin-dynein regulatory complex subunit DRC1 is essential for motile cilia function in algae and humans. Nat Genet 45, 262-268.
41. Yanagisawa HA, Mathis G, Oda T, Hirono M, Richey EA, Ishikawa H, Marshall WF, Kikkawa M, Qin H (2014). FAP20 is an inner junction protein of doublet microtubules essential for both the planar asymmetrical waveform and stability of flagella in Chlamydomonas. Mol Biol Cell 25, 1472-1483.
42. Yang P, Diener DR, Rosenbaum JL, Sale WS (2001). Localization of calmodulin and dynein light chain LC8 in flagellar radial spokes. J Cell Biol 153, 1315-1326.