Atypical centrioles during sexual reproduction

Frontiers in Cell and Developmental Biology

Volumn 3, Issue APR, 2015, Pages

  Avidor Reiss, Tomer ^a   Khire, Atul ^a   Fishman, Emily L ^a   Jo, Kyoung H ^a  

^a UNIVERSITY OF TOLEDO   (United States)

Author keywords

Centriole; Centrosome; Cilium; Fertilization; Microtubules; Reproduction; Sperm; Zygote

Indexed keywords

EID: 85052193588     PISSN: None     EISSN: 2296634X     Source Type: Journal    
DOI: 10.3389/fcell.2015.00021     Document Type: Review

References (150)

1. Avasthi, P., and Marshall, W. F. (2012). Stages of ciliogenesis and regulation of ciliary length. Differentiation 83, S30-S42. doi: 10.1016/j.diff.2011.11.015
2. Avidor-Reiss, T., and Gopalakrishnan, J. (2013). Building a centriole. Curr. Opin. Cell Biol. 25, 72-77. doi: 10.1016/j.ceb.2012.10.016
3. Avidor-Reiss, T., Gopalakrishnan, J., Blachon, S., and Polyanovsky, A. (2012). 'Centriole duplication and inheritance in Drosophila melanogaster'. in The Centrosome: Cell and Molecular Mechanisms of Functions and Dysfunctions in Disease, ed H. Schatten (New York, NY: Humana Press), 3-31
4. Baccetti, B., and Afzelius, B. A. (1976). The biology of the sperm cell. Monogr. Dev. Biol. 1-254
5. Baccetti, B., Burrini, A. G., Dallai, R., Pallini, V.P., Periti, P., Piantelli, F., et al. (1973). Structure and function in the spermatozoon of Bacillus rossius. The spermatozoon of arthropoda. XIX. J. Ultrastruct. Res. 12, 1-73
6. Bahe, S., Stierhof, Y. D., Wilkinson, C. J., Leiss, F., and Nigg, E. A. (2005). Rootletin forms centriole-associated filaments and functions in centrosome cohesion. J. Cell Biol. 171, 27-33. doi: 10.1083/jcb.200504107
7. Bangs, F. K., Schrode, N., Hadjantonakis, A. K., and Anderson, K. V. (2015). Lineage specificity of primary cilia in the mouse embryo. Nat. Cell Biol. 17, 113-122. doi: 10.1038/ncb3091
8. Basiri, M. L., Ha, A., Chadha, A., Clark, N. M., Polyanovsky, A., Cook, B., et al. (2014). A migrating ciliary gate compartmentalizes the site of axoneme assembly in Drosophila Spermatids. Curr. Biol. 24, 2622-2631. doi: 10.1016/j.cub.2014.09.047
9. Basto, R., Lau, J., Vinogradova, T., Gardiol, A., Woods, C. G., Khodjakov, A., et al. (2006). Flies without Centrioles. Cell 125, 1375-1386. doi: 10.1016/j.cell.2006.05.025
10. Bernardini, G., Stipani, R., and Melone, G. (1986). The ultrastructure of Xenopus spermatozoon. J. Ultrastruct. Mol. Struct. Res. 94, 188-194. doi: 10.1016/0889-1605(86)90065-0
11. Blachon, S., Cai, X., Roberts, K. A., Yang, K., Polyanovsky, A., Church, A., et al. (2009). A proximal centriole-like structure is present in Drosophila spermatids and can serve as a model to study centriole duplication. Genetics 182, 133-144. doi: 10.1534/genetics.109.101709
12. Blachon, S., Khire, A., and Avidor-Reiss, T. (2014). The origin of the second centriole in the zygote of Drosophila melanogaster. Genetics 197, 199-205. doi: 10.1534/genetics.113.160523
13. Brevini, T. A., Pennarossa, G., Vanelli, A., Maffei, S., and Gandolfi, F. (2012). Parthenogenesis in non-rodent species: developmental competence and differentiation plasticity. Theriogenology 77, 766-772. doi: 10.1016/j.theriogenology.2011.11.010
14. Calarco, P. G. (2000). Centrosome precursors in the acentriolar mouse oocyte. Microsc. Res. Tech. 49, 428-434. doi: 10.1002/(SICI)1097-0029(20000601)49:5<428::AID-JEMT4>3.0.CO;2-K
15. Callaini, G., and Riparbelli, M. G. (1996). Fertilization in Drosophila melanogaster: centrosome inheritance and organization of the first mitotic spindle. Dev. Biol. 176, 199-208. doi: 10.1006/dbio.1996.0127
16. Callaini, G., Whitfield, W. G., and Riparbelli, M. G. (1997). Centriole and centrosome dynamics during the embryonic cell cycles that follow the formation of the cellular blastoderm in Drosophila. Exp. Cell Res. 234, 183-190. doi: 10.1006/excr.1997.3618
17. Carvalho-Santos, Z., Machado, P., Alvarez-Martins, I., Gouveia, S. M., Jana, S. C., Duarte, P., et al. (2012). BLD10/CEP135 is a microtubule-associated protein that controls the formation of the flagellum central microtubule pair. Dev. Cell 23, 412-424. doi: 10.1016/j.devcel.2012.06.001
18. Chemes, H. E., and Rawe, V. Y. (2010). The making of abnormal spermatozoa: cellular and molecular mechanisms underlying pathological spermiogenesis. Cell Tissue Res. 341, 349-357. doi: 10.1007/s00441-010-1007-3
19. Coelho, P. A., Bury, L., Sharif, B., Riparbelli, M. G., Fu, J., Callaini, G., et al. (2013). Spindle formation in the mouse embryo requires Plk4 in the absence of centrioles. Dev. Cell 27, 586-597. doi: 10.1016/j.devcel.2013.09.029
20. Connolly, J. A., and Kalnins, V. I. (1978). Visualization of centrioles and basal bodies by fluorescent staining with nonimmune rabbit sera. J. Cell Biol. 79, 526-532. doi: 10.1083/jcb.79.2.526
21. Courtois, A., Schuh, M., Ellenberg, J., and Hiiragi, T. (2012). The transition from meiotic to mitotic spindle assembly is gradual during early mammalian development. J. Cell Biol. 198, 357-370. doi: 10.1083/jcb.201202135
22. Crozet, N., Dahirel, M., and Chesne, P. (2000). Centrosome inheritance in sheep zygotes: centrioles are contributed by the sperm. Microsc. Res. Tech. 49, 445-450. doi: 10.1002/(SICI)1097-0029(20000601)49:5<445::AID-JEMT6>3.0.CO;2-B
23. Dammermann, A., Muller-Reichert, T., Pelletier, L., Habermann, B., Desai, A., and Oegema, K. (2004). Centriole assembly requires both centriolar and pericentriolar material proteins. Dev. Cell 7, 815-829. doi: 10.1016/j.devcel.2004.10.015
24. Daniels, E. W., Longwell, A. C., McNiff, J. M., and Wolfgang, R. W. (1971). Ultrastructure of spermatozoa from the American oyster Crassostrea virginica. Trans. Am. Microsc. Soc. 90, 275-282. doi: 10.2307/3225187
25. Debec, A., and Abbadie, C. (1989). The acentriolar state of the Drosophila cell lines 1182. Biol. Cell 67, 307-311
26. de Fried, E. P., Ross, P., Zang, G., Divita, A., Cunniff, K., Denaday, F., et al. (2008). Human parthenogenetic blastocysts derived from noninseminated cryopreserved human oocytes. Fertil. Steril. 89, 943-947. doi: 10.1016/j.fertnstert.2007.04.045
27. Delattre, M., and Gonczy, P. (2004). The arithmetic of centrosome biogenesis. J. Cell Sci. 117, 1619-1630. doi: 10.1242/jcs.01128
28. Dias, G., Lino-Neto, J., and Dallai, R. (2015). The sperm ultrastructure of Stictoleptura cordigera (Fussli, 1775) (Insecta, Coleoptera, Cerambycidae). Tissue Cell 47, 73-77. doi: 10.1016/j.tice.2014.11.007
29. Dix, C. I., and Raff, J. W. (2007). Drosophila Spd-2 recruits PCM to the sperm centriole, but is dispensable for centriole duplication. Curr. Biol. 17, 1759-1764. doi: 10.1016/j.cub.2007.08.065
30. Fawcett, D. W. (1965). The anatomy of the mammalian spermatozoon with particular reference to the guinea pig. Z. Zellforsch. Mikrosk. Anat. 67, 279-296. doi: 10.1007/BF00339376
31. Fawcett, D. W., and Phillips, D. M. (1969). The fine structure and development of the neck region of the mammalian spermatozoon. Anat. Rec. 165, 153-164. doi: 10.1002/ar.1091650204
32. Fechter, J., Schoneberg, A., and Schatten, G. (1996). Excision and disassembly of sperm tail microtubules during sea urchin fertilization: requirements for microtubule dynamics. Cell Motil. Cytoskeleton 35, 281-288. doi: 10.1002/(SICI)1097-0169(1996)35:4<281::AID-CM1>3.0.CO;2-A
33. Felix, M. A., Antony, C., Wright, M., and Maro, B. (1994). Centrosome assembly in vitro: role of gamma-tubulin recruitment in Xenopus sperm aster formation. J. Cell Biol. 124, 19-31
34. Fong, C. S., Kim, M., Yang, T. T., Liao, J. C., and Tsou, M. F. (2014). SAS-6 assembly templated by the lumen of cartwheel-less centrioles precedes centriole duplication. Dev. Cell 30, 238-245. doi: 10.1016/j.devcel.2014.05.008
35. Friedlander, M. (1980). The sperm centriole persists during early egg cleavage in the insect Chrysopa carnea (Neuroptera, Chrysopidae). J. Cell Sci. 42, 221-226
36. Fu, J., and Glover, D. M. (2012). Structured illumination of the interface between centriole and peri-centriolar material. Open Biol. 2:120104. doi: 10.1098/rsob.120104
37. Fuller, M. T. (1993). 'Spermatogenesis'. in The Development of Drosophila melanogaster, eds M. Bate and A. Martinez-Arias (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), 71-174
38. Ganem, N. J., Godinho, S. A., and Pellman, D. (2009). A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282. doi: 10.1038/nature08136
39. Godinho, S. A., Picone, R., Burute, M., Dagher, R., Su, Y., Leung, C. T., et al. (2014). Oncogene-like induction of cellular invasion from centrosome amplification. Nature 510, 167-171. doi: 10.1038/nature13277
40. Goetz, S. C., and Anderson, K. V. (2010). The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 11, 331-344. doi: 10.1038/nrg2774
41. Gonczy, P. (2012). Towards a molecular architecture of centriole assembly. Nat. Rev. Mol. Cell Biol. 13, 425-435. doi: 10.1038/nrm3373
42. Gopalakrishnan, J., Mennella, V., Blachon, S., Zhai, B., Smith, A. H., Megraw, T. L., et al. (2011). Sas-4 provides a scaffold for cytoplasmic complexes and tethers them in a centrosome. Nat. Commun. 2, 359. doi: 10.1038/ncomms1367
43. Goshima, G., Wollman, R., Goodwin, S. S., Zhang, N., Scholey, J. M., Vale, R. D., et al. (2007). Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316, 417-421. doi: 10.1126/science.1141314
44. Goto, M., O'Brien, D. A., and Eddy, E. M. (2010). Speriolin is a novel human and mouse sperm centrosome protein. Hum. Reprod. 25, 1884-1894. doi: 10.1093/humrep/deq138
45. Gottardo, M., Callaini, G., and Riparbelli, M. G. (2013). The cilium-like region of the Drosophila spermatocyte: an emerging flagellum? J. Cell Sci. 126, 5441-5452. doi: 10.1242/jcs.136523
46. Gueth-Hallonet, C., Antony, C., Aghion, J., Santa-Maria, A., Lajoie-Mazenc, I., Wright, M., et al. (1993). gamma-Tubulin is present in acentriolar MTOCs during early mouse development. J. Cell Sci. 105(Pt 1), 157-166
47. Guichard, P., Chretien, D., Marco, S., and Tassin, A. M. (2010). Procentriole assembly revealed by cryo-electron tomography. EMBO J. 29, 1565-1572. doi: 10.1038/emboj.2010.45
48. Heidemann, S. R., and Kirschner, M. W. (1975). Aster formation in eggs of Xenopus laevis. Induction by isolated basal bodies. J. Cell Biol. 67, 105-117. doi: 10.1083/jcb.67.1.105
49. Hinchcliffe, E. H., Miller, F. J., Cham, M., Khodjakov, A., and Sluder, G. (2001). Requirement of a centrosomal activity for cell cycle progression through G1 into S phase. Science 291, 1547-1550. doi: 10.1126/science.291.5508.1547
50. Hiraki, M., Nakazawa, Y., Kamiya, R., and Hirono, M. (2007). Bld10p constitutes the cartwheel-spoke tip and stabilizes the 9-fold symmetry of the centriole. Curr. Biol. 17, 1778-1783. doi: 10.1016/j.cub.2007.09.021
51. Holland, A. J., Lan, W., and Cleveland, D. W. (2010). Centriole duplication: a lesson in self-control. Cell Cycle 9, 2731-2736. doi: 10.4161/cc.9.14.12184
52. Jana, S. C., Marteil, G., and Bettencourt-Dias, M. (2014). Mapping molecules to structure: unveiling secrets of centriole and cilia assembly with near-atomic resolution. Curr. Opin. Cell Biol. 26, 96-106. doi: 10.1016/j.ceb.2013.12.001
53. Jin, Y. X., Cui, X. S., Yu, X. F., Lee, S. H., Wang, Q. L., Gao, W. W., et al. (2012). Cat fertilization by mouse sperm injection. Zygote 20, 371-378. doi: 10.1017/S0967199411000451
54. Khodjakov, A., and Rieder, C. L. (2001). Centrosomes enhance the fidelity of cytokinesis in vertebrates and are required for cell cycle progression. J. Cell Biol. 153, 237-242. doi: 10.1083/jcb.153.1.237
55. Kim, D. Y., and Roy, R. (2006). Cell cycle regulators control centrosome elimination during oogenesis in Caenorhabditis elegans. J. Cell Biol. 174, 751-757. doi: 10.1083/jcb.200512160
56. Kim, H. K., Kang, J. G., Yumura, S., Walsh, C. J., Cho, J. W., and Lee, J. (2005). De novo formation of basal bodies in Naegleria gruberi: regulation by phosphorylation. J. Cell Biol. 169, 719-724. doi: 10.1083/jcb.200410052
57. Kimura, A., and Onami, S. (2005). Computer simulations and image processing reveal length-dependent pulling force as the primary mechanism for C. elegans male pronuclear migration. Dev. Cell 8, 765-775. doi: 10.1016/j.devcel.2005.03.007
58. Kirkham, M., Muller-Reichert, T., Oegema, K., Grill, S., and Hyman, A. A. (2003). SAS-4 is a C. elegans centriolar protein that controls centrosome size. Cell 112, 575-587. doi: 10.1016/S0092-8674(03)00117-X
59. Krioutchkova, M. M., and Onishchenko, G. E. (1999). Structural and functional characteristics of the centrosome in gametogenesis and early embryogenesis of animals. Int. Rev. Cytol. 185, 107-156
60. La Terra, S., English, C. N., Hergert, P., McEwen, B. F., Sluder, G., and Khodjakov, A. (2005). The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation. J. Cell Biol. 168, 713-722. doi: 10.1083/jcb.200411126
61. Langreth, S. G. (1969). Spermiogenesis in Cancer crabs. J. Cell Biol. 43, 575-603
62. Lau, L., Lee, Y. L., Sahl, S. J., Stearns, T., and Moerner, W. E. (2012). STED microscopy with optimized labeling density reveals 9-fold arrangement of a centriole protein. Biophys. J. 102, 2926-2935. doi: 10.1016/j.bpj.2012.05.015
63. Lee, J., Kang, S., Choi, Y. S., Kim, H., Yeo, C., Lee, Y., et al. (2014). Identification of a cell cycle-dependent duplicating complex that assembles basal bodies de novo in naegleria. Protist 166, 1-13. doi: 10.1016/j.protis.2014.11.001
64. Li, K., Xu, E. Y., Cecil, J. K., Turner, F. R., Megraw, T. L., and Kaufman, T. C. (1998). Drosophila centrosomin protein is required for male meiosis and assembly of the flagellar axoneme. J. Cell Biol. 141, 455-467. doi: 10.1083/jcb.141.2.455
65. Longo, F. J., and Anderson, E. (1968). The fine structure of pronuclear development and fusion in the sea urchin, Arbacia punctulata. J. Cell Biol. 39, 339-368
66. Longo, F. J., and Anderson, E. (1969). Sperm differentiation in the sea urchins Arbacia punctulata and Strongylocentrotus purpuratus. J. Ultrastruct. Res. 27, 486-509
67. Luksza, M., Queguigner, I., Verlhac, M. H., and Brunet, S. (2013). Rebuilding MTOCs upon centriole loss during mouse oogenesis. Dev. Biol. 382, 48-56. doi: 10.1016/j.ydbio.2013.07.029
68. Mahjoub, M. R., and Stearns, T. (2012). Supernumerary centrosomes nucleate extra cilia and compromise primary cilium signaling. Curr. Biol. 22, 1628-1634. doi: 10.1016/j.cub.2012.06.057
69. Malicki, J., and Avidor-Reiss, T. (2014). From the cytoplasm into the cilium: bon voyage. Organogenesis 10, 138-157. doi: 10.4161/org.29055
70. Manandhar, G., and Schatten, G. (2000). Centrosome reduction during Rhesus spermiogenesis: gamma-tubulin, centrin, and centriole degeneration. Mol. Reprod. Dev. 56, 502-511. doi: 10.1002/1098-2795(200008)56:4<502::AID-MRD8>3.0.CO;2-Q
71. Manandhar, G., Schatten, H., and Sutovsky, P. (2005). Centrosome reduction during gametogenesis and its significance. Biol. Reprod. 72, 2-13. doi: 10.1095/biolreprod.104.031245
72. Manandhar, G., Simerly, C., and Schatten, G. (2000). Centrosome reduction during mammalian spermiogenesis. Curr. Top. Dev. Biol. 49, 343-363. doi: 10.1016/S0070-2153(99)49017-9
73. Manandhar, G., Sutovsky, P., Joshi, H. C., Stearns, T., and Schatten, G. (1998). Centrosome reduction during mouse spermiogenesis. Dev. Biol. 203, 424-434
74. Marescalchi, O., Zauli, C., and Scali, V. (2002). Centrosome dynamics and inheritance in related sexual and parthenogenetic Bacillus (Insecta Phasmatodea). Mol. Reprod. Dev. 63, 89-95. doi: 10.1002/mrd.10177
75. Maro, B., Johnson, M. H., Pickering, S. J., and Flach, G. (1984). Changes in actin distribution during fertilization of the mouse egg. J. Embryol. Exp. Morphol. 81, 211-237
76. Matsuura, K., Lefebvre, P. A., Kamiya, R., and Hirono, M. (2004). Bld10p, a novel protein essential for basal body assembly in Chlamydomonas: localization to the cartwheel, the first ninefold symmetrical structure appearing during assembly. J. Cell Biol. 165, 663-671. doi: 10.1083/jcb.200402022
77. McGill, M., and Brinkley, B. R. (1975). Human chromosomes and centrioles as nucleating sites for the in vitro assembly of microtubules from bovine brain tubulin. J. Cell Biol. 67, 189-199. doi: 10.1083/jcb.67.1.189
78. McNally, K. L., Fabritius, A. S., Ellefson, M. L., Flynn, J. R., Milan, J. A., and McNally, F. J. (2012). Kinesin-1 prevents capture of the oocyte meiotic spindle by the sperm aster. Dev. Cell 22, 788-798. doi: 10.1016/j.devcel.2012.01.010
79. Mennella, V., Keszthelyi, B., McDonald, K. L., Chhun, B., Kan, F., Rogers, G. C., et al. (2012). Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat. Cell Biol. 14, 1159-1168. doi: 10.1038/ncb2597
80. Mikeladze-Dvali, T., von Tobel, L., Strnad, P., Knott, G., Leonhardt, H., Schermelleh, L., et al. (2012). Analysis of centriole elimination during C. elegans oogenesis. Development 139, 1670-1679. doi: 10.1242/dev.075440
81. Morito, Y., Terada, Y., Nakamura, S., Morita, J., Yoshimoto, T., Murakami, T., et al. (2005). Dynamics of microtubules and positioning of female pronucleus during bovine parthenogenesis. Biol. Reprod. 73, 935-941. doi: 10.1095/biolreprod.105.042366
82. Mottier-Pavie, V., and Megraw, T. L. (2009). Drosophila bld10 is a centriolar protein that regulates centriole, basal body, and motile cilium assembly. Mol. Biol. Cell 20, 2605-2614. doi: 10.1091/mbc.E08-11-1115
83. Nakashima, S., and Kato, K. H. (2001). Centriole behavior during meiosis in oocytes of the sea urchin Hemicentrotus pulcherrimus. Dev. Growth Differ. 43, 437-445. doi: 10.1046/j.1440-169x.2001.00580.x
84. Nakazawa, Y., Hiraki, M., Kamiya, R., and Hirono, M. (2007). SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Curr. Biol. 17, 2169-2174. doi: 10.1016/j.cub.2007.11.046
85. Navara, C. S., First, N. L., and Schatten, G. (1994). Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: the role of the sperm aster. Dev. Biol. 162, 29-40. doi: 10.1006/dbio.1994.1064
86. Nigg, E. A., and Stearns, T. (2011). The centrosome cycle: centriole biogenesis, duplication and inherent asymmetries. Nat. Cell Biol. 13, 1154-1160. doi: 10.1038/ncb2345
87. Noguchi, T., and Miller, K. G. (2003). A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development 130, 1805-1816. doi: 10.1242/dev.00406
88. O'Connell, K. F., Caron, C., Kopish, K. R., Hurd, D. D., Kemphues, K. J., Li, Y., et al. (2001). The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105, 547-558. doi: 10.1016/S0092-8674(01)00338-5
89. O'Donnell, L., Nicholls, P. K., O'Bryan, M. K., McLachlan, R. I., and Stanton, P. G. (2011). Spermiation: the process of sperm release. Spermatogenesis 1, 14-35. doi: 10.4161/spmg.1.1.14525
90. O'Toole, E. T., and Dutcher, S. K. (2014). Site-specific basal body duplication in Chlamydomonas. Cytoskeleton (Hoboken) 71, 108-118. doi: 10.1002/cm.21155
91. Paffoni, A., Brevini, T. A., Somigliana, E., Restelli, L., Gandolfi, F., and Ragni, G. (2007). In vitro development of human oocytes after parthenogenetic activation or intracytoplasmic sperm injection. Fertil. Steril. 87, 77-82. doi: 10.1016/j.fertnstert.2006.05.063
92. Palazzo, R. E., Vogel, J. M., Schnackenberg, B. J., Hull, D. R., and Wu, X. (2000). Centrosome maturation. Curr. Top. Dev. Biol. 49, 449-470. doi: 10.1016/S0070-2153(99)49021-0
93. Pampliega, O., Orhon, I., Patel, B., Sridhar, S., Diaz-Carretero, A., Beau, I., et al. (2013). Functional interaction between autophagy and ciliogenesis. Nature 502, 194-200. doi: 10.1038/nature12639
94. Paweletz, N., Mazia, D., and Finze, E. M. (1987). Fine structural studies of the bipolarization of the mitotic apparatus in the fertilized sea urchin egg. I. The structure and behavior of centrosomes before fusion of the pronuclei. Eur. J. Cell Biol. 44, 195-204
95. Pelletier, L., O'Toole, E., Schwager, A., Hyman, A. A., and Muller-Reichert, T. (2006). Centriole assembly in Caenorhabditis elegans. Nature 444, 619-623. doi: 10.1038/nature05318
96. Pelletier, L., Ozlü, N., Hannak, E., Cowan, C., Habermann, B., Ruer, M., et al. (2004). The Caenorhabditis elegans centrosomal protein SPD-2 is required for both pericentriolar material recruitment and centriole duplication. Curr. Biol. 14, 863-873. doi: 10.1016/j.cub.2004.04.012
97. Peters, N., Perez, D. E., Song, M. H., Liu, Y., Muller-Reichert, T., Caron, C., et al. (2010). Control of mitotic and meiotic centriole duplication by the Plk4-related kinase ZYG-1. J. Cell Sci. 123, 795-805. doi: 10.1242/jcs.050682
98. Phillips, D. M. (1970). Insect sperm: their structure and morphogenesis. J. Cell Biol. 44, 243-277
99. Rattner, J. B. (1972). Observations of centriole formation in male meiosis. J. Cell Biol. 54, 20-29
100. Rawe, V. Y., Diaz, E. S., Abdelmassih, R., Wojcik, C., Morales, P., Sutovsky, P., et al. (2008). The role of sperm proteasomes during sperm aster formation and early zygote development: implications for fertilization failure in humans. Hum. Reprod. 23, 573-580. doi: 10.1093/humrep/dem385
101. Riparbelli, M. G., and Callaini, G. (2010). Detachment of the basal body from the sperm tail is not required to organize functional centrosomes during Drosophila embryogenesis. Cytoskeleton (Hoboken) 67, 251-258. doi: 10.1002/cm.20440
102. Riparbelli, M. G., Callaini, G., and Glover, D. M. (2000). Failure of pronuclear migration and repeated divisions of polar body nuclei associated with MTOC defects in polo eggs of Drosophila. J. Cell Sci. 113(Pt 18), 3341-3350
103. Riparbelli, M. G., Callaini, G., and Megraw, T. L. (2012). Assembly and persistence of primary cilia in dividing Drosophila spermatocytes. Dev. Cell 23, 425-432. doi: 10.1016/j.devcel.2012.05.024
104. Riparbelli, M. G., Dallai, R., and Callaini, G. (2010). The insect centriole: a land of discovery. Tissue Cell 42, 69-80. doi: 10.1016/j.tice.2010.01.002
105. Riparbelli, M. G., Whitfield, W. G., Dallai, R., and Callaini, G. (1997). Assembly of the zygotic centrosome in the fertilized Drosophila egg. Mech. Dev. 65, 135-144
106. Marshall, R. D., and Luykx, P. (1973). Observations on the centrioles of the sea urchin spermatozoon. Dev. Growth Differ. 14, 311-324. doi: 10.1111/j.1440-169X.1973.00311.x
107. Rodrigues-Martins, A., Bettencourt-Dias, M., Riparbelli, M., Ferreira, C., Ferreira, I., Callaini, G., et al. (2007a). DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr. Biol. 17, 1465-1472. doi: 10.1016/j.cub.2007.07.034
108. Rodrigues-Martins, A., Riparbelli, M., Callaini, G., Glover, D. M., and Bettencourt-Dias, M. (2007b). Revisiting the role of the mother centriole in centriole biogenesis. Science 316, 1046-1050. doi: 10.1126/science.1142950
109. Sathananthan, A. H., Ratnam, S. S., Ng, S. C., Tarin, J. J., Gianaroli, L., and Trounson, A. (1996). The sperm centriole: its inheritance, replication and perpetuation in early human embryos. Hum. Reprod. 11, 345-356. doi: 10.1093/HUMREP/11.2.345
110. Sathananthan, A. H., Selvaraj, K., Girijashankar, M. L., Ganesh, V., Selvaraj, P., and Trounson, A. O. (2006). From oogonia to mature oocytes: inactivation of the maternal centrosome in humans. Microsc. Res. Tech. 69, 396-407. doi: 10.1002/jemt.20299
111. Schatten, G. (1994). The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev. Biol. 165, 299-335. doi: 10.1006/dbio.1994.1256
112. Schatten, G., Simerly, C., and Schatten, H. (1985). Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc. Natl. Acad. Sci. U.S.A. 82, 4152-4156. doi: 10.1073/pnas.82.12.4152
113. Schatten, H., Schatten, G., Mazia, D., Balczon, R., and Simerly, C. (1986). Behavior of centrosomes during fertilization and cell division in mouse oocytes and in sea urchin eggs. Proc. Natl. Acad. Sci. U.S.A. 83, 105-109. doi: 10.1073/pnas.83.1.105
114. Schatten, H., and Sun, Q. Y. (2009). The role of centrosomes in mammalian fertilization and its significance for ICSI. Mol. Hum. Reprod. 15, 531-538. doi: 10.1093/molehr/gap049
115. Schatten, H., and Sun, Q. Y. (2011). New insights into the role of centrosomes in mammalian fertilization and implications for ART. Reproduction 142, 793-801. doi: 10.1530/REP-11-0261
116. Scheer, U. (2014). Historical roots of centrosome research: discovery of Boveri's microscope slides in Wurzburg. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369. doi: 10.1098/rstb.2013.0469
117. Shirato, Y., Tamura, M., Yoneda, M., and Nemoto, S. (2006). Centrosome destined to decay in starfish oocytes. Development 133, 343-350. doi: 10.1242/dev.02193
118. Simerly, C., Wu, G. J., Zoran, S., Ord, T., Rawlins, R., Jones, J., et al. (1995). The paternal inheritance of the centrosome, the cell's microtubule-organizing center, in humans, and the implications for infertility. Nat. Med. 1, 47-52. doi: 10.1038/nm0195-47
119. Sluder, G. (2014). One to only two: a short history of the centrosome and its duplication. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369. doi: 10.1098/rstb.2013.0455
120. Sluder, G., and Khodjakov, A. (2010). Centriole duplication: analogue control in a digital age. Cell Biol. Int. 34, 1239-1245. doi: 10.1042/CBI20100612
121. Sluder, G., and Rieder, C. L. (1985a). Centriole number and the reproductive capacity of spindle poles. J. Cell Biol. 100, 887-896. doi: 10.1083/jcb.100.3.887y
122. Sluder, G., and Rieder, C. L. (1985b). Experimental separation of pronuclei in fertilized sea urchin eggs: chromosomes do not organize a spindle in the absence of centrosomes. J. Cell Biol. 100, 897-903. doi: 10.1083/jcb.100.3.897
123. Sluder, G., Miller, F. J., and Rieder, C. L. (1989). Reproductive capacity of sea urchin centrosomes without centrioles. Cell Motil. Cytoskeleton 13, 264-273. doi: 10.1002/cm.970130405
124. Stearns, T., and Kirschner, M. (1994). In vitro reconstitution of centrosome assembly and function: the central role of gamma-tubulin. Cell 76, 623-637. doi: 10.1016/0092-8674(94)90503-7
125. Stevens, N. R., Dobbelaere, J., Brunk, K., Franz, A., and Raff, J. W. (2010). Drosophila Ana2 is a conserved centriole duplication factor. J. Cell Biol. 188, 313-323. doi: 10.1083/jcb.200910016
126. Stevens, N. R., Raposo, A. A., Basto, R., St Johnston, D., and Raff, J. W. (2007). From stem cell to embryo without centrioles. Curr. Biol. 17, 1498-1503. doi: 10.1016/j.cub.2007.07.060
127. Stevermann, L., and Liakopoulos, D. (2012). Molecular mechanisms in spindle positioning: structures and new concepts. Curr. Opin. Cell Biol. 24, 816-824. doi: 10.1016/j.ceb.2012.10.005
128. Sun, Q. Y., and Schatten, H. (2007). Centrosome inheritance after fertilization and nuclear transfer in mammals. Adv. Exp. Med. Biol. 591, 58-71. doi: 10.1007/978-0-387-37754-4_4
129. Sutovsky, P., and Schatten, G. (2000). Paternal contributions to the mammalian zygote: fertilization after sperm-egg fusion. Int. Rev. Cytol. 195, 1-65. doi: 10.1016/S0074-7696(08)62703-5
130. Szollosi, A. (1975). Electron microscope study of spermiogenesis in Locusta migratoria (Insect Orthoptera). J. Ultrastruct. Res. 50, 322-346. doi: 10.1016/S0022-5320(75)80064-5
131. Szollosi, D., Calarco, P., and Donahue, R. P. (1972). Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J. Cell Sci. 11, 521-541
132. Tang, Z., Lin, M. G., Stowe, T. R., Chen, S., Zhu, M., Stearns, T., et al. (2013). Autophagy promotes primary ciliogenesis by removing OFD1 from centriolar satellites. Nature 502, 254-257. doi: 10.1038/nature12606
133. Tates, A. D. (1971). Cytodifferentiation during Spermatogenesis in Drosophila melanogaster: An Electron Microscope Study. Leiden: Rijksuniversiteit de Leiden
134. Terada, Y., Hasegawa, H., Ugajin, T., Murakami, T., Yaegashi, N., and Okamura, K. (2009). Microtubule organization during human parthenogenesis. Fertil. Steril. 91, 1271-1272. doi: 10.1016/j.fertnstert.2008.05.051
135. Terada, Y., Schatten, G., Hasegawa, H., and Yaegashi, N. (2010). Essential roles of the sperm centrosome in human fertilization: developing the therapy for fertilization failure due to sperm centrosomal dysfunction. Tohoku J. Exp. Med. 220, 247-258. doi: 10.1620/tjem.220.247
136. Tokuyasu, K. T. (1975). Dynamics of spermiogenesis in Drosophila melanogaster. V. Head-tail alignment. J. Ultrastruct. Res. 50, 117-129. doi: 10.1016/S0022-5320(75)90013-1
137. Uetake, Y., Kato, K. H., Washitani-Nemoto, S., and Nemoto Si, S. (2002). Nonequivalence of maternal centrosomes/centrioles in starfish oocytes: selective casting-off of reproductive centrioles into polar bodies. Dev. Biol. 247, 149-164. doi: 10.1006/dbio.2002.0682
138. van Breugel, M., Hirono, M., Andreeva, A., Yanagisawa, H. A., Yamaguchi, S., Nakazawa, Y., et al. (2011). Structures of SAS-6 suggest its organization in centrioles. Science 331, 1196-1199. doi: 10.1126/science.1199325
139. Varmark, H., Llamazares, S., Rebollo, E., Lange, B., Reina, J., Schwarz, H., et al. (2007). Asterless is a centriolar protein required for centrosome function and embryo development in Drosophila. Curr. Biol. 17, 1735-1745. doi: 10.1016/j.cub.2007.09.031
140. Wasbrough, E. R., Dorus, S., Hester, S., Howard-Murkin, J., Lilley, K., Wilkin, E., et al. (2010). The Drosophila melanogaster sperm proteome-II (DmSP-II). J. Proteomics 73, 2171-2185. doi: 10.1016/j.jprot.2010.09.002
141. Washitani-Nemoto, S., Saitoh, C., and Nemoto, S. (1994). Artificial parthenogenesis in starfish eggs: behavior of nuclei and chromosomes resulting in tetraploidy of parthenogenotes produced by the suppression of polar body extrusion. Dev. Biol. 163, 293-301. doi: 10.1006/dbio.1994.1148
142. Wheatley, D. N. (1982). The Centriole, a Central Enigma of Cell Biology. Amsterdam: Elsevier Biomedical Press
143. Wilson, P. G., Zheng, Y., Oakley, C. E., Oakley, B. R., Borisy, G. G., and Fuller, M. T. (1997). Differential expression of two gamma-tubulin isoforms during gametogenesis and development in Drosophila. Dev. Biol. 184, 207-221. doi: 10.1006/dbio.1997.8545
144. Winey, M., and O'Toole, E. (2014). Centriole structure. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369. doi: 10.1098/rstb.2013.0457
145. Woolley, D. M., and Fawcett, D. W. (1973). The degeneration and disappearance of the centrioles during the development of the rat spermatozoon. Anat. Rec. 177, 289-301. doi: 10.1002/ar.1091770209
146. Xiao, X., and Yang, W. X. (2007). Actin-based dynamics during spermatogenesis and its significance. J. Zhejiang Univ. Sci. B 8, 498-506. doi: 10.1631/jzus.2007.B0498
147. Yang, J., Adamian, M., and Li, T. (2006). Rootletin interacts with C-Nap1 and may function as a physical linker between the pair of centrioles/basal bodies in cells. Mol. Biol. Cell 17, 1033-1040. doi: 10.1091/mbc.E05-10-0943
148. Yasuno, Y., and Yamamoto, M. T. (2014). Electron microscopic observation of the sagittal structure of Drosophila mature sperm. Microsc. Res. Tech. 77, 661-666. doi: 10.1002/jemt.22386
149. Zamboni, L., Chakraborty, J., and Smith, D. M. (1972). First cleavage division of the mouse zygot. An ultrastructural study. Biol. Reprod. 7, 170-193
150. Zamboni, L., and Stefanini, M. (1971). The fine structure of the neck of mammalian spermatozoa. Anat. Rec. 169, 155-172. doi: 10.1002/ar.1091690203