Microtubule sliding movement in tilapia sperm flagella axoneme is regulated by Ca2+/calmodulin-dependent protein phosphorylation

Cell Motility and the Cytoskeleton

Volumn 63, Issue 8, 2006, Pages 459-470

  Morita, Masaya ^a   Takemura, Akihiro ^a   Nakajima, Ayako ^b   Okuno, Makoto ^b  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Ca 2+ binding protein; Ca2+; Ca2+ CaM dependent protein kinase; Eukaryotic flagella; Flagellar motility; Protein phosphorylation

Indexed keywords

CALCIUM 45; CALCIUM BINDING PROTEIN; CALMODULIN; DYNEIN ADENOSINE TRIPHOSPHATASE; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; PHOSPHORUS 32; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE (CALCIUM,CALMODULIN) IV; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AXONEME; CALCIUM CELL LEVEL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; FLAGELLATE; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SPERM; SPERMATOZOON MOTILITY; TILAPIA;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CALMODULIN; MALE; MICROTUBULES; PHOSPHORUS RADIOISOTOPES; PHOSPHORYLATION; SPERM TAIL; TILAPIA;

OREOCHROMIS MOSSAMBICUS; TILAPIA;

EID: 33746690358     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20137     Document Type: Article

References (46)

1. Bannai H, Yoshimura M, Takahashi K, Shingyoji C. 2000. Calcium regulation of microtubule sliding in reactivated sea urchin sperm flagella. J Cell Sci 113:831-839.
2. Bessen M, Fay RB, Witman GB. 1980. Calcium control of waveform in isolated flagellar axonemes of Chlamydomonas. J Cell Biol 86:446-455.
3. Brokaw CJ. 1967. Adenosine triphosphate usage by flagella. Science 156:76-78.
4. Brokaw CJ. 1971. Bend-propagation by a sliding filament model for flagella. J Exp Biol 55:289-304.
5. Brokaw CJ. 1979. Calcium-induced asymmetrical beating of triton-demembranated sea urchin sperm flagella. J Cell Biol 82:401-411.
6. Brokaw CJ. 1991. Microtubule sliding in swimming sperm flagella: Direct and indirect measurements on sea urchin and tunicate spermatozoa. J Cell Biol 114:1201-1215.
7. Brokaw CJ, Nagayama SM. 1985. Modulation of the asymmetry of sea urchin sperm flagellar bending by calmodulin. J Cell Biol 100:1875-1883.
8. Gray J, Hancock GJ. 1995. The propulsion of sea-urchin spermatozoa. J Exp Biol 32:802-814.
9. Gibbons BH, Gibbons IR. 1973. The effect of partial extraction of dynein arms on the movement of reactivated sea-urchin sperm. J Cell Sci 13:337-357.
10. Gibbons BH, Gibbons IR. 1980. Calcium-induced quiescence in reactivated sea urchin sperm. J Cell Biol 84:13-27.
11. Gibbons IR, Fronk E. 1972. Some properties of bound and soluble dynein from sea urchin sperm flagella. J Cell Biol 54:365-381.
12. Hayashi H, Yamamoto K, Yonekawa H, Morisawa M. 1987. Involvement of tyrosine protein kinase in the initiation of flagellar movement in rainbow trout spermatozoa. J Biol Chem 262:16692-16698.
13. Hirabayashi T. 1981. Two-dimensional gel electrophoresis of chicken skeletal muscle proteins with agarose gels in first dimension. Anal Biochem 117:443-451.
14. Hulen D, Baron A, Salisbury A, Clarke M. 1991. Production and specificity of monoclonal antibodies against calmodulin from dictyostelium discoideum. Cell Motil Cytoskel 18:113-122.
15. Hyams JS, Borisy GG. 1978. Isolated flagellar apparatus of Chlamydomonas: Characterization of forward swimming and alteration of waveform and reversal of motion by calcium ions in vitro. J Cell Sci 33:235-253.
16. Inaba K. 2003. Molecular architecture of the sperm flagella: Molecules for motility and signaling. Zool Sci 20:1043-1056.
17. 2+-binding protein localized on the outer arm dynein in sperm flagella of Ciona intestinalis. Zool Sci 20:1538.
18. Inaba K, Akazome Y, Morisawa M. 1993. Purification of proteasomes from salmonid fish sperm and their localization along sperm flagella. J Cell Sci 104:907-915.
19. Itoh A, Inaba K, Ohtake H, Fujinoki M, Morisawa M. 2003. Characterization of a cAMP-dependent protein kinase catalytic subunit from rainbow trout spermatozoa. Biochem Biophys Res Commun 305:855-861.
20. 2+ influx and subsequent initiation of sperm motility in the common carp. Proc Natl Acad Sci USA 97:2052-2057.
21. Leammli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
22. 45Ca autoradiography on nitrocellulose membrane after sodium dodecyl sulfate gel electrophoresis. J Biochem 95:511-519.
23. Morisawa M. 1994. Cell signaling mechanisms for sperm motility. Zoo Sci 11:647-662.
24. Morisawa M, Hayashi H. 1985. Phosphorylation of a 15 k axonemal protein is the trigger initiating trout sperm motility. Biomed Res 6:181-184.
25. 2+ on activation of sperm motility in euryhaline tilapia Oreochromis mossambicus. J Exp Biol 206:913-921.
26. Morita M, Takemura A, Okuno M. 2004. Acclimation of sperm motility apparatus in seawater-acclimated euryhaline tilapia, Oreochromis mossambicus. J Exp Biol 207:337-345.
27. Nakano I, Kobayashi T, Yoshimura M, Shingyoji C. 2003. Central-pair-linked regulation of microtubule sliding by calcium in flagellar axonemes. J Cell Sci 116:1627-1636.
28. 2+ and pH mediate the initiation of sperm motility by the hyperosmolality in marine teleosts. Cell Motil Cytoskeleton 25:171-178.
29. Omoto CK, Brokaw CJ. 1985. Bending patterns of Chlamydomonas flagella: II. Calcium effects on reactivated Chlamydomonas flagella. Cell Motil 5:53-60.
30. Piperno G, Huang B, Ramanis Z, Luck DJL. 1981. Radial spokes of Chlamydomonas flagella: Polypeptide composition and phosphorylation of stalk components. J Cell Biol 88:73-79.
31. Porter ME, Sale WS. 2000. The 9+2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J Cell Biol 151:F37-F42.
32. Shingyoji C, Gibbons IR, Murakami A, Takahashi K. 1991. Effect of imposed head vibration on the stability and waveform of flagellar beating in sea urchin spermatozoa. J Exp Biol 156:63-80.
33. Shingyoji C, Yoshimura K, Eshel D, Takahashi K, Gibbons IR. 1995. Effect of beat frequency on the velocity of microtubule sliding in reactivated sea urchin sperm flagella under imposed head vibration. J Exp Biol 198:645-653.
34. Smith EF. 2002. Regulation of flagellar dynein by calcium and a role for an axonemal calmodulin and calmodulin-dependent kinase. Mol Biol Cell 13:3303-3313.
35. Smith EF, Lafebvre PA. 1997. The role of central apparatus components in flagellar motility and microtubule assembly. Cell Motil Cytoskeleton 18:258-268.
36. Smith EF, Sale WS. 1992. Regulation of dynein-driven microtubule sliding by the radial spokes in flagella. Science 257:1557-1559.
37. Smith EF, Sale WS. 1994. Mechanisms of flagellar movement: functional interactions between dynein arms and the radial spoke-central apparatus complex. In: Hyams CW, Lloyd JS, editors. Microtubules. New York: Wiley. p 381-392.
38. Tash JS, Bracho GE. 1994. Regulation of sperm motility: Emerging evidence for a major role for protein phosphatase. J Androl 15:505-509.
39. Tash JS, Means AR. 1983. Cyclic adenosine 3′, 5′ monophosphate, calcium and protein phosphorylation in flagellar motility. Biol Reprod 28:75-104.
40. Tash JS, Krinks M, Patel J, Means RL, Klee CB, Means AR. 1988. Identification, characterization, and functional correlation of calmodulin-dependent protein phosphatase in sperm. J Cell Biol 106:1625-1633.
41. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354.
42. Vines CA, Yoshida K, Griffin FJ, Pillai MC, Morisawa M, Yanagimachi R, Cherr GN. 2002. Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange. Proc Natl Acad Sci USA 99:2026-2031.
43. Walczack CE, Nelson DL. 1994. Regulation of dynein-driven motility in cilia and flagella. Cell Motil Cytoskeleton 27:101-107.
44. Wargo MJ, McPeek MA, Smith EF. 2004. Analysis of microtubule sliding patterns in Chlamydomonas flagellar axonemes reveals dynein activity on specific doublet microtubules. J Cell Sci 117:2533-2544.
45. Witman GB, Plummer J, Sander G. 1978. Chlamydomonas flagellar mutants lacking radial spokes and central tubules. J Cell Biol 76:729-747.
46. Yang P, Fox L, Colbran R, Sale WS. 2000. Protein phosphatase PP1 and PP2A are located in distinct positions in the Chlamydomonas flagellar axoneme. J Cell Sci 113:91-102.