Hemingway is required for sperm flagella assembly and ciliary motility in Drosophila

Molecular Biology of the Cell

Volumn 25, Issue 8, 2014, Pages 1276-1286

  Soulavie, Fabien ^a   Piepenbrock, David ^b   Thomas, Joëlle ^a   Vieillard, Jennifer ^a   Duteyrat, Jean Luc ^a   Cortier, Elisabeth ^a   Laurençon, Anne ^a,c   Göpfert, Martin C ^b   Duranda, Bénédicte ^a  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; HEMINGWAY PROTEIN; TUBULIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; HEMINGWAY PROTEIN, DROSOPHILA; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; AXONEME; CILIARY MOTILITY; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE TARGETING; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SPERMATID; SPERMATOGENESIS; SPERMATOZOON TAIL; TESTIS; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; BIOSYNTHESIS; CILIARY DYSKINESIA; EUKARYOTIC FLAGELLUM; GENE INACTIVATION; GENETICS; HEARING IMPAIRMENT; MALE; MALE INFERTILITY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROMOTER REGION; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; TRANSGENIC ANIMAL;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BINDING SITES; CILIA; CILIARY MOTILITY DISORDERS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE KNOCKOUT TECHNIQUES; HEARING LOSS; INFERTILITY, MALE; MALE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SPERM TAIL; SPERMATOGENESIS; TRANSCRIPTION FACTORS;

EID: 84922998895     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-10-0616     Document Type: Article

References (44)

1. Amos LA (2008). The tektin family of microtubule-stabilizing proteins. Genome Biol 9, 229.
2. Avidor-Reiss T, Maer A, Koundakjian E, Polyanovsky A, Keil T, Subramaniam S, Zuker C (2004). Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117, 527-539.
3. Baron D, Ralston K, Kabututu Z, Hill K (2007). Functional genomics in Trypanosoma brucei identifies evolutionarily conserved components of motile flagella. J Cell Sci 120, 478-491.
4. Bonnafe E et al. (2004). The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol Cell Biol 24, 4417-4427.
5. Bré MH et al. (1996). Axonemal tubulin polyglycylation probed with two monoclonal antibodies: widespread evolutionary distribution, appearance during spermatozoan maturation and possible function in motility. J Cell Sci 109, 727-738.
6. Combet C, Blanchet C, Geourjon C, Deléage G (2000). NPS@: network protein sequence analysis. Trends Biochem Sci 25, 147-150.
7. Drummond IA (2012). Cilia functions in development. Curr Opin Cell Biol 24, 24-30.
8. Dubruille R, Laurençon A, Vandaele C, Shishido E, Coulon-Bublex M, Swoboda P, Couble P, Kernan M, Durand B (2002). Drosophila regulatory factor X is necessary for ciliated sensory neuron differentiation. Development 129, 5487-5498.
9. Effertz T, Wiek R, Göpfert MC (2011). NompC TRP channel is essential for Drosophila sound receptor function. Curr Biol 21, 592-597.
10. Enjolras C, Thomas J, Chhin B, Cortier E, Duteyrat JL, Soulavie F, Kernan MJ, Laurencon A, Durand B (2012). Drosophila chibby is required for basal body formation and ciliogenesis but not for Wg signaling. J Cell Biol 197, 313-325.
11. Frazer K, Pachter L, Poliakov A, Rubin E, Dubchak I (2004). VISTA: computational tools for comparative genomics. Nucleic Acids Res 32, W273-W279.
12. Gagnon C, White D, Cosson J, Huitorel P, Edde B, Desbruyeres E, Paturle-Lafanechère L, Multigner L, Job D, Cibert C (1996). The polyglutamylated lateral chain of alpha-tubulin plays a key role in flagellar motility. J Cell Sci 109, 1545-1553.
13. Göpfert MC, Albert JT, Nadrowski B, Kamikouchi A (2006). Specification of auditory sensitivity by Drosophila TRP channels. Nat Neurosci 9, 999-1000.
14. Göpfert MC, Humphris ADL, Albert JT, Robert D, Hendrich O (2005). Power gain exhibited by motile mechanosensory neurons in Drosophila ears. Proc Natl Acad Sci USA 102, 325-330.
15. Göpfert MC, Robert D (2003). Motion generation by Drosophila mechanosensory neurons. Proc Natl Acad Sci USA 100, 5514-5519.
16. Hildebrandt F, Benzing T, Katsanis N (2011). Ciliopathies. N Engl J Med 364, 1533-1543.
17. Hoyle HD, Turner FR, Raff EC (2008). Axoneme-dependent tubulin modifications in singlet microtubules of the Drosophila sperm tail. Cell Motil Cytoskeleton 65, 295-313.
18. Ikegami K, Sato S, Nakamura K, Ostrowski LE, Setou M (2010). Tubulin polyglutamylation is essential for airway ciliary function through the regulation of beating asymmetry. Proc Natl Acad Sci USA 107, 10490-10495.
19. Jarman A, Grau Y, Jan L, Jan Y (1993). atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73, 1307-1321.
20. Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A, Göpfert MC, Ito K (2009). The neural basis of Drosophila gravity-sensing and hearing. Nature 458, 165-171.
21. Kamikouchi A, Shimada T, Ito K (2006). Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J Comp Neurol 499, 317-356.
22. Kavlie RG, Kernan MJ, Eberl DF (2010). Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility. Genetics 185, 177-188.
23. King RD, Saqi M, Sayle R, Sternberg MJ (1997). DSC: public domain protein secondary structure predication. Comput Appl Biosci 13, 473-474.
24. Kubo T, Yanagisawa H-A, Yagi T, Hirono M, Kamiya R (2010). Tubulin polyglutamylation regulates axonemal motility by modulating activities of inner-arm dyneins. Curr Biol 20, 441-445.
25. Laurençon A, Dubruille R, Efimenko E, Grenier G, Bissett R, Cortier E, Rolland V, Swoboda P, Durand B (2007). Identification of novel regulatory factor X (RFX) target genes by comparative genomics in Drosophila species. Genome Biol 8, R195.
26. Lindemann CB, Lesich KA (2010). Flagellar and ciliary beating: the proven and the possible. J Cell Sci 123, 519-528.
27. Maggert KA, Gong WJ, Golic KG (2008). Methods for homologous recombination in Drosophila. Methods Mol Biol 420, 155-174.
28. McGrath J, Brueckner M (2003). Cilia are at the heart of vertebrate left-right asymmetry. Curr Opin Genet Dev 13, 385-392.
29. Merchant SS et al. (2007). The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250.
30. O'Hagan R, Piasecki BP, Silva M, Phirke P, Nguyen KCQ, Hall DH, Swoboda P, Barr MM (2011). The tubulin deglutamylase CCPP-1 regulates the function and stability of sensory cilia in C. elegans. Curr Biol 21, 1685-1694.
31. Ostrowski L, Blackburn K, Radde K, Moyer M, Schlatzer D, Moseley A, Boucher R (2002). A proteomic analysis of human cilia: identification of novel components. Mol Cell Proteomics 1, 451-465.
32. Rogowski K et al. (2009). Evolutionary divergence of enzymatic mechanisms for posttranslational polyglycylation. Cell 137, 1076-1087.
33. Rogowski K et al. (2010). A family of protein-deglutamylating enzymes associated with neurodegeneration. Cell 143, 564-578.
34. Roy A, Lin YN, Agno JE, DeMayo FJ, Matzuk MM (2007). Absence of tektin 4 causes asthenozoospermia and subfertility in male mice. FASEB J 21, 1013-1025.
35. Satir P (1989). The role of axonemal components in ciliary motility. Comp Biochem Physiol A Comp Physiol 94, 351-357.
36. Senthilan PR, Piepenbrock D, Ovezmyradov G, Nadrowski B, Bechstedt S, Pauls S, Winkler M, Möbius W, Howard J, Göpfert MC (2012). Drosophila auditory organ genes and genetic hearing defects. Cell 150, 1042-1054.
37. Suryavanshi S, Eddé B, Fox LA, Guerrero S, Hard R, Hennessey T, Kabi A, Malison D, Pennock D, Sale WS (2010). Tubulin glutamylation regulates ciliary motility by altering inner dynein arm activity. Curr Biol 20, 435-440.
38. Swoboda P, Adler HT, Thomas JH (2000). The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol Cell 5, 411-421.
39. Tanaka H, Iguchi N, Toyama Y, Kitamura K, Takahashi T, Kaseda K, Maekawa M, Nishimune Y (2004). Mice deficient in the axonemal protein tektin-t exhibit male infertility and immotile-cilium syndrome due to impaired inner arm dynein function. Mol Cell Biol 24, 7958-7964.
40. Thomas J, Morle L, Soulavie F, Laurencon A, Sagnol S, Durand B (2010). Transcriptional control of genes involved in ciliogenesis: a first step in making cilia. Biol Cell 102, 499-513.
41. Wickstead B, Gull K (2007). Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8, 1708-1721.
42. Wloga D, Gaertig J (2010). Post-translational modifications of microtubules. J Cell Sci 124, 154-154.
43. Wloga D, Webster DM, Rogowski K, Bré M-H, Levilliers N, Jerka-Dziadosz M, Janke C, Dougan ST, Gaertig J (2009). TTLL3 is a tubulin glycine ligase that regulates the assembly of cilia. Dev Cell 16, 867-876.
44. Wolff A, de Néchaud B, Chillet D, Mazarguil H, Desbruyeres E, Audebert S, Edde B, Gros F, Denoulet P (1992). Distribution of glutamylated alpha and beta-tubulin in mouse tissues using a specific monoclonal antibody, GT335. Eur J Cell Biol 59, 425-432.