Proteomic profiling reveals compartment-specific, novel functions of ascidian sperm proteins

Molecular Reproduction and Development

Volumn 78, Issue 7, 2011, Pages 529-549

  Nakachi, Mia ^a   Nakajima, Ayako ^a   Nomura, Mamoru ^a   Yonezawa, Kouki ^b   Ueno, Keisuke ^b   Endo, Toshinori ^b   Inaba, Kazuo ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYISOBUTYRYL COENZYME A HYDROLASE; ACONITATE HYDRATASE; ACTIN; ALPHA ENOLASE; ALPHA TUBULIN; BETA TUBULIN; CALCIUM BINDING PROTEIN; CELL PROTEIN; CITRATE SYNTHASE; CREATINE KINASE; DEAMINASE; FRUCTOSE BISPHOSPHATE ALDOLASE; FUMARATE HYDRATASE; GLUTATHIONE REDUCTASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; ISOCITRATE DEHYDROGENASE (NAD); MALATE DEHYDROGENASE; PF16 PROTEIN; POLYACRYLAMIDE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE DEHYDROGENASE; PYRUVATE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SPERM PROTEIN; THREONINE DEHYDRATASE; TRITON X 100; UNCLASSIFIED DRUG; UNINDEXED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASCIDIACEA; AXONEME; CIONA INTESTINALIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO DEVELOPMENT; FLAGELLUM; FUNCTIONAL PROTEOMICS; GENE EXPRESSION; ISOELECTRIC FOCUSING; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPERM; SPERMATOGENESIS; TESTIS;

ACTINS; ANIMALS; AXONEME; CIONA INTESTINALIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GTP-BINDING PROTEINS; MALE; OCTOXYNOL; ORGAN SPECIFICITY; PROTEIN-SERINE-THREONINE KINASES; PROTEOME; PROTEOMICS; SPERM HEAD; SPERM TAIL; UBIQUITIN;

ASCIDIA; CIONA INTESTINALIS;

EID: 79960563562     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.21341     Document Type: Article

References (91)

1. Azumi K, Sabau SV, Fujie M, Usami T, Koyanagi R, Kawashima T, Fujiwara S, Ogasawara M, Satake M, Nonaka M, Wang HG, Satou Y, Satoh N. 2007. Gene expression profile during the life cycle of the urochordate Ciona intestinalis Dev Biol 308: 572-582.
2. Baker MA, Hetherington L, Reeves GM, Aitken RJ. 2008. The mouse sperm proteome characterized via IPG strip prefractionation and LC-MS/MS identification. Proteomics 8: 1720-1730.
3. Bera TK, Hahn Y, Lee B, Pastan IH. 2003. TEPP, a new gene specifically expressed in testis, prostate, and placenta and well conserved in chordates. Biochem Biophys Res Commun 312: 1209-1215.
4. Bernstein M, Beech PL, Katz SG, Rosenbaum JL. 1994. A new kinesin-like protein (Klp1) localized to a single microtubule of the Chlamydomonas flagellum. J Cell Biol 125: 1313-1326.
5. Bielke W, Blaschke RJ, Miescher GC, Zurcher G, Andres AC, Ziemiecki A. 1994. Characterization of a novel murine testis-specific serine/threonine kinase. Gene 139: 235-239.
6. Bradford MM. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72: 248-254.
7. Cao W, Gerton GL, Moss SB. 2006. Proteomic profiling of accessory structures from the mouse sperm flagellum. Mol Cell Proteomics 5: 801-810.
8. Chiba S, Awazu S, Itoh M, Chin-Bow ST, Satoh N, Satou Y, Hastings KE. 2003. A genomewide survey of developmentally relevant genes in Ciona intestinalis. IX. Genes for muscle structural proteins. Dev Genes Evol 213: 291-302.
9. Chu DS, Liu H, Nix P, Wu TF, Ralston EJ, Yates JR III, Meyer BJ. 2006. Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature 443: 101-105.
10. Clapham DE. 2003. TRP channels as cellular sensors. Nature 426: 517-524.
11. Corbo JC, Di Gregorio A, Levine M. 2001. The ascidian as a model organism in developmental and evolutionary biology. Cell 106: 535-538.
12. Darszon A, Wood CD, Beltran C, Sanchez D, Rodriguez E, Gorelik J, Korchev YE, Nishigaki T. 2004. Measuring ion fluxes in sperm. Methods Cell Biol 74: 545-576.
13. Dawe HR, Farr H, Portman N, Shaw MK, Gull K. 2005. The Parkin co-regulated gene product, PACRG, is an evolutionarily conserved axonemal protein that functions in outer-doublet microtubule morphogenesis. J Cell Sci 118: 5421-5430.
14. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KE, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang HG, Awazu S, Azumi K, Boore J, Branno M, Chin-Bow S, DeSantis R, Doyle S, Francino P, Keys DN, Haga S, Hayashi H, Hino K, Imai KS, Inaba K, Kano S, Kobayashi K, Kobayashi M, Lee BI, Makabe KW, Manohar C, Matassi G, Medina M, Mochizuki Y, Mount S, Morishita T, Miura S, Nakayama A, Nishizaka S, Nomoto H, Ohta F, Oishi K, Rigoutsos I, Sano M, Sasaki A, Sasakura Y, Shoguchi E, Shin-i T, Spagnuolo A, Stainier D, Suzuki MM, Tassy O, Takatori N, Tokuoka M, Yagi K, Yoshizaki F, Wada S, Zhang C, Hyatt PD, Larimer F, Detter C, Doggett N, Glavina T, Hawkins T, Richardson P, Lucas S, Kohara Y, Levine M, Satoh N, Rokhsar DS. 2002. The draft genome of Ciona intestinalis: Insights into chordate and vertebrate origins. Science 298: 2157-2167.
15. Dutcher SK, Huang B, Luck DJ. 1984. Genetic dissection of the central pair microtubules of the flagella of Chlamydomonas reinhardtii J Cell Biol 98: 229-236.
16. Endo T, Ueno K, Yonezawa K, Mineta K, Hotta K, Satou Y, Yamada L, Ogasawara M, Takahashi H, Nakajima A, Nakachi M, Nomura M, Yaguchi J, Sasakura Y, Yamasaki C, Sera M, Yoshizawa AC, Imanishi T, Taniguchi H, Inaba K. 2011. CIPRO 2.5: Ciona intestinalis protein database, a unique integrated repository of large-scale omics data, bioinformatic analyses and curated annotation, with user rating and reviewing functionality. Nucleic Acids Res 39: D807-D814.
17. Evans JP, Florman HM. 2002. The state of the union: The cell biology of fertilization. Nat Cell Biol 4: s57-s63.
18. Fewell SW, Travers KJ, Weissman JS, Brodsky JL. 2001. The action of molecular chaperones in the early secretory pathway. Annu Rev Genet 35: 149-191.
19. Ficarro S, Chertihin O, Westbrook VA, White F, Jayes F, Kalab P, Marto JA, Shabanowitz J, Herr JC, Hunt DF, Visconti PE. 2003. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J Biol Chem 278: 11579-11589.
20. Fujita A, Nakamura K, Kato T, Watanabe N, Ishizaki T, Kimura K, Mizoguchi A, Narumiya S. 2000. Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella. J Cell Sci 113: 103-112.
21. Fujiwara S, Maeda Y, Shin IT, Kohara Y, Takatori N, Satou Y, Satoh N. 2002. Gene expression profiles in Ciona intestinalis cleavage-stage embryos. Mech Dev 112: 115-127.
22. Fuke TM. 1983. Self and non-self recognition between gametes of the ascidian, Halocynthia roretzi Roux's Arch Dev Biol 192: 347-352.
23. Gibbons IR. 1981. Cilia and flagella of eukaryotes. J Cell Biol 91: 107s-124s.
24. Gingras D, White D, Garin J, Multigner L, Job D, Cosson J, Huitorel P, Zingg H, Dumas F, Gagnon C. 1996. Purification, cloning, and sequence analysis of a Mr=30, 000 protein from sea urchin axonemes that is important for sperm motility. Relationship of the protein to a dynein light chain. J Biol Chem 271: 12807-12813.
25. Hao Z, Jha KN, Kim YH, Vemuganti S, Westbrook VA, Chertihin O, Markgraf K, Flickinger CJ, Coppola M, Herr JC, Visconti PE. 2004. Expression analysis of the human testis-specific serine/threonine kinase (TSSK) homologues. A TSSK member is present in the equatorial segment of human sperm. Mol Hum Reprod 10: 433-444.
26. Harada Y, Takagaki Y, Sunagawa M, Saito T, Yamada L, Taniguchi H, Shoguchi E, Sawada H. 2008. Mechanism of self-sterility in a hermaphroditic chordate. Science 320: 548-550.
27. Hinsch KD, Habermann B, Just I, Hinsch E, Pfisterer S, Schill WB, Aktories K. 1993. ADP-ribosylation of Rho proteins inhibits sperm motility. FEBS Lett 334: 32-36.
28. Hozumi A, Satouh Y, Makino Y, Toda T, Ide H, Ogawa K, King SM, Inaba K. 2006. Molecular characterization of Ciona sperm outer arm dynein reveals multiple components related to outer arm docking complex protein 2. Cell Motil Cytoskeleton 63: 591-603.
29. Hozumi A, Padma P, Toda T, Ide H, Inaba K. 2008. Molecular characterization of axonemal proteins and signaling molecules responsible for chemoattractant-induced sperm activation in Ciona intestinalis Cell Motil Cytoskeleton 65: 249-267.
30. Ikeda K, Brown JA, Yagi T, Norrander JM, Hirono M, Eccleston E, Kamiya R, Linck RW. 2003. Rib72, a conserved protein associated with the ribbon compartment of flagellar A-microtubules and potentially involved in the linkage between outer doublet microtubules. J Biol Chem 278: 7725-7734.
31. Inaba K. 2003. Molecular architecture of the sperm flagella: Molecules for motility and signaling. Zoolog Sci 20: 1043-1056.
32. Inaba K. 2007. Molecular basis of sperm flagellar axonemes: Structural and evolutionary aspects. Ann NY Acad Sci 1101: 506-526.
33. Inaba K. 2011. Sperm flagella: Comparative and phylogenetic perspectives of protein components. Mol Hum Reprod (in press; doi: 10.1093/molehr/gar034).
34. Inaba K, Mizuno K. 2009. Purification of dyneins from sperm flagella. Methods Cell Biol 92: 49-63.
35. Inaba K, Morisawa S, Morisawa M. 1998. Proteasomes regulate the motility of salmonid fish sperm through modulation of cAMP-dependent phosphorylation of an outer arm dynein light chain. J Cell Sci 111: 1105-1115.
36. Inaba K, Padma P, Satouh Y, Shin IT, Kohara Y, Satoh N, Satou Y. 2002. EST analysis of gene expression in testis of the ascidian Ciona intestinalis Mol Reprod Dev 62: 431-445.
37. Inaba K, Nomura M, Nakajima A, Hozumi A. 2007. Functional proteomics in Ciona intestinalis: A breakthrough in the exploration of the molecular and cellular mechanism of ascidian development. Dev Dyn 236: 1782-1789.
38. Kamiya R. 2002. Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants. Int Rev Cytol 219: 115-155.
39. Karr TL. 2007. Fruit flies and the sperm proteome. Hum Mol Genet 16: R124-R133.
40. Konno A, Padma P, Ushimaru Y, Inaba K. 2010. Multidimensional analysis of uncharacterized sperm proteins in Ciona intestinalis: EST-based analysis and functional immunoscreening of testis-expressed genes. Zoolog Sci 27: 204-215.
41. Krisfalusi M, Miki K, Magyar PL, O'Brien DA. 2006. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol Reprod 75: 270-278.
42. Kueng P, Nikolova Z, Djonov V, Hemphill A, Rohrbach V, Boehlen D, Zuercher G, Andres AC, Ziemiecki A. 1997. A novel family of serine/threonine kinases participating in spermiogenesis. J Cell Biol 139: 1851-1859.
43. Lambert CC, Koch RA. 1988. Sperm binding and penetration during ascidian fertilization. Dev Growth Differ 30: 325-336.
44. Li Y, Sosnik J, Brassard L, Reese M, Spiridonov NA, Bates TC, Johnson GR, Anguita J, Visconti PE, Salicioni AM. 2011. Expression and localization of five members of the testis-specific serine kinase (Tssk) family in mouse and human sperm and testis. Mol Hum Reprod 17: 42-56.
45. Liang P, MacRae TH. 1997. Molecular chaperones and the cytoskeleton. J Cell Sci 110: 1431-1440.
46. Marino R, Pinto MR, Cotelli F, Lamia CL, De Santis R. 1998. The hsp70 protein is involved in the acquisition of gamete self-sterility in the ascidian Ciona intestinalis Development 125: 899-907.
47. Martinez-Heredia J, Estanyol JM, Ballesca JL, Oliva R. 2006. Proteomic identification of human sperm proteins. Proteomics 6: 4356-4369.
48. Miller RL. 1975. Chemotaxis of the spermatozoa of Ciona intestinalis Nature 254: 244-245.
49. Mizuno K, Padma P, Konno A, Satouh Y, Ogawa K, Inaba K. 2009. A novel neuronal calcium sensor family protein, calaxin, is a potential Ca(2+)-dependent regulator for the outer arm dynein of metazoan cilia and flagella. Biol Cell 101: 91-103.
50. Mohri H. 1968. Amino-acid composition of "Tubulin" constituting microtubules of sperm flagella. Nature 217: 1053-1054.
51. Morgan TH. 1923. Removal of the block to self-fertilization in the ascidian Ciona Proc Natl Acad Sci USA 9: 170-171.
52. Neilson LI, Schneider PA, Van Deerlin PG, Kiriakidou M, Driscoll DA, Pellegrini MC, Millinder S, Yamamoto KK, French CK, Strauss JF III. 1999. cDNA cloning and characterization of a human sperm antigen (SPAG6) with homology to the product of the Chlamydomonas PF16 locus. Genomics 60: 272-280.
53. Nishikata T, Yamada L, Mochizuki Y, Satou Y, Shin-i T, Kohara Y, Satoh N. 2001. Profiles of maternally expressed genes in fertilized eggs of Ciona intestinalis Dev Biol 238: 315-331.
54. Nomura M, Inaba K, Morisawa M. 2000. Phosphorylation of axonemal 21kDa and 26kDa proteins modulates activation of sperm motility in the ascidian, Ciona intestinalis Zygote 8: S59-S60.
55. Nomura M, Nakajima A, Inaba K. 2009. Proteomic profiles of embryonic development in the ascidian Ciona intestinalis Dev Biol 325: 468-481.
56. Ogasawara M, Sasaki A, Metoki H, Shin-i T, Kohara Y, Satoh N, Satou Y. 2002. Gene expression profiles in young adult Ciona intestinalis Dev Genes Evol 212: 173-185.
57. Ogawa K, Inaba K. 2006. Ap58: A novel in situ outer dynein arm-binding protein. Biochem Biophys Res Commun 343: 385-390.
58. Padma P, Hozumi A, Ogawa K, Inaba K. 2001. Molecular cloning and characterization of a thioredoxin/nucleoside diphosphate kinase related dynein intermediate chain from the ascidian, Ciona intestinalis Gene 275: 177-183.
59. Padma P, Satouh Y, Wakabayashi K, Hozumi A, Ushimaru Y, Kamiya R, Inaba K. 2003. Identification of a novel leucine-rich repeat protein as a component of flagellar radial spoke in the Ascidian Ciona intestinalis Mol Biol Cell 14: 774-785.
60. Pazour GL, Agrin N, Leszyk J, Witman GB. 2005. Proteomic analysis of a eukaryotic cilium. J Cell Biol 170: 103-113.
61. Piperno G, Luck DJ. 1981. Inner arm dyneins from flagella of Chlamydomonas reinhardtii Cell 27: 331-340.
62. 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.
63. Satoh N. 2001. Ascidian embryos as a model system to analyze expression and function of developmental genes. Differentiation 68: 1-12.
64. Satoh N. 2003. The ascidian tadpole larva: Comparative molecular development and genomics. Nat Rev Genet 4: 285-295.
65. Satou Y, Takatori N, Fujiwara S, Nishikata T, Saiga H, Kusakabe T, Shin-i T, Kohara Y, Satoh N. 2002a. Ciona intestinalis cDNA projects: Expressed sequence tag analyses and gene expression profiles during embryogenesis. Gene 287: 83-96.
66. Satou Y, Yamada L, Mochizuki Y, Takatori N, Kawashima T, Sasaki A, Hamaguchi M, Awazu S, Yagi K, Sasakura Y, Nakayama A, Ishikawa H, Inaba K, Satoh N. 2002b. A cDNA resource from the basal chordate Ciona intestinalis Genesis 33: 153-154.
67. Satou Y, Kawashima T, Shoguchi E, Nakayama A, Satoh N. 2005. An integrated database of the ascidian, Ciona intestinalis: Towards functional genomics. Zoolog Sci 22: 837-843.
68. Satou Y, Mineta K, Ogasawara M, Sasakura Y, Shoguchi E, Ueno K, Yamada L, Matsumoto J, Wasserscheid J, Dewar K, Wiley GB, Macmil SL, Roe BA, Zeller RW, Hastings KE, Lemaire P, Lindquist E, Endo T, Hotta K, Inaba K. 2008. Improved genome assembly and evidence-based global gene model set for the chordate Ciona intestinalis: New insight into intron and operon populations. Genome Biol 9: R152.
69. Satouh Y, Inaba K. 2009. Proteomic characterization of sperm radial spokes identifies a novel spoke protein with an ubiquitin domain. FEBS Lett 583: 2201-2207.
70. Satouh Y, Padma P, Toda T, Satoh N, Ide H, Inaba K. 2005. Molecular characterization of radial spoke subcomplex containing radial spoke protein 3 and heat shock protein 40 in sperm flagella of the ascidian Ciona intestinalis Mol Biol Cell 16: 626-636.
71. Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, Kodama E, Takizawa S, Yokosawa H. 2002. Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc Natl Acad Sci USA 99: 1223-1228.
72. Sleight SB, Miranda PV, Plaskett NW, Maier B, Lysiak J, Scrable H, Herr JC, Visconti PE. 2005. Isolation and proteomic analysis of mouse sperm detergent-resistant membrane fractions: Evidence for dissociation of lipid rafts during capacitation. Biol Reprod 73: 721-729.
73. Smith EF, Lefebvre PA. 1997. PF20 gene product contains WD repeats and localizes to the intermicrotubule bridges in Chlamydomonas flagella. Mol Biol Cell 8: 455-467.
74. Sutton KA, Jungnickel MK, Wang Y, Cullen K, Lambert S, Florman HM. 2004. Enkurin is a novel calmodulin and TRPC channel binding protein in sperm. Dev Biol 274: 426-435.
75. Takamura K, Oka N, Akagi A, Okamoto K, Okada T, Fukuoka T, Hogaki A, Naito D, Oobayashi Y, Satoh N. 2001. EST analysis of genes that are expressed in the neural complex of Ciona intestinalis adults. Zoolog Sci 18: 1231-1236.
76. Tanaka K. 2009. The proteasome: Overview of structure and functions. Proc Jpn Acad Ser B 85: 12-36.
77. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. 2003. The COG database: An updated version includes eukaryotes. BMC Bioinformatics 4: 41.
78. Ushimaru Y, Konno A, Kaizu M, Ogawa K, Satoh N, Inaba K. 2006. Association of a 66kDa homolog of Chlamydomonas DC2, a subunit of the outer arm docking complex, with outer arm dynein of sperm flagella in the ascidian Ciona intestinalis Zoolog Sci 23: 679-687.
79. Vacquier VD, Hirohashi N. 2004. Sea urchin spermatozoa. Methods Cell Biol 74: 523-544.
80. Vacquier VD, Moy GW. 1977. Isolation of bindin: The protein responsible for adhesion of sperm to sea urchin eggs. Proc Natl Acad Sci USA 74: 2456-2460.
81. Wheeler AP, Ridley AJ. 2004. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp Cell Res 301: 43-49.
82. Wu H, Chen Y, Miao S, Zhang C, Zong S, Koide SS, Wang L. 2010. Sperm associated antigen 8 (SPAG8), a novel regulator of activator of CREM in testis during spermatogenesis. FEBS Lett 584: 2807-2815.
83. Xu B, Hao Z, Jha KN, Zhang Z, Urekar C, Digilio L, Pulido S, Strauss JF III, Flickinger CJ, Herr JC. 2008. TSKS concentrates in spermatid centrioles during flagellogenesis. Dev Biol 319: 201-210.
84. Yamada L, Kobayashi K, Satou Y, Satoh N. 2005. Microarray analysis of localization of maternal transcripts in eggs and early embryos of the ascidian, Ciona intestinalis Dev Biol 284: 536-550.
85. Yamada L, Saito T, Taniguchi H, Sawada H, Harada Y. 2009. Comprehensive egg coat proteome of the ascidian Ciona intestinalis reveals gamete recognition molecules involved in self-sterility. J Biol Chem 284: 9402-9410.
86. Yoshida M, Inaba K, Morisawa M. 1993. Sperm chemotaxis during the process of fertilization in the ascidians Ciona savignyi and Ciona intestinalis Dev Biol 157: 497-506.
87. Yoshida M, Murata M, Inaba K, Morisawa M. 2002. A chemoattractant for ascidian spermatozoa is a sulfated steroid. Proc Natl Acad Sci USA 99: 14831-14836.
88. Yoshida M, Ishikawa M, Izumi H, De Santis R, Morisawa M. 2003. Store-operated calcium channel regulates the chemotactic behavior of ascidian sperm. Proc Natl Acad Sci USA 100: 149-154.
89. Zhang Z, Sapiro R, Kapfhamer D, Bucan M, Bray J, Chennathukuzhi V, McNamara P, Curtis A, Zhang M, Blanchette-Mackie EJ, Strauss JF III. 2002. A sperm-associated WD repeat protein orthologous to Chlamydomonas PF20 associates with Spag6, the mammalian orthologue of Chlamydomonas PF16. Mol Cell Biol 22: 7993-8004.
90. Zhang Z, Tang W, Zhou R, Shen X, Wei Z, Patel AM, Povlishock JT, Bennett J, Strauss JF III. 2007. Accelerated mortality from hydrocephalus and pneumonia in mice with a combined deficiency of SPAG6 and SPAG16L reveals a functional interrelationship between the two central apparatus proteins. Cell Motil Cytoskeleton 64: 360-376.
91. Zhang Z, Shen X, Jones BH, Xu B, Herr JC, Strauss JF III. 2008. Phosphorylation of mouse sperm axoneme central apparatus protein SPAG16L by a testis-specific kinase, TSSK2. Biol Reprod 79: 75-83.