The role of centrosomes in mammalian fertilization and its significance for ICSI

Molecular Human Reproduction

Volumn 15, Issue 9, 2009, Pages 531-538

  Schatten, Heide ^a   Sun, Qing Yuan ^b  

^a UNIVERSITY OF MISSOURI   (United States)

^b INSTITUTE OF ZOOLOGY   (China)

Author keywords

Centrosome integrity; Centrosomes; Infertility; Sperm aster

Indexed keywords

CENTRIN; GAMMA TUBULIN; NUCLEAR PROTEIN; PERICENTRIN;

CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL FUNCTION; CELL STRUCTURE; CENTROSOME; FERTILIZATION; GAMETOGENESIS; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; MEIOSIS; MICROTUBULE ORGANIZING CENTER; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION; SPERMATOGENESIS;

ANIMALS; CENTROSOME; FEMALE; FERTILIZATION; HUMANS; INFERTILITY, MALE; MALE; SPERM INJECTIONS, INTRACYTOPLASMIC;

MAMMALIA;

EID: 69049115222     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gap049     Document Type: Review

References (65)

1. Aitken RJ. Just how safe is assisted reproductive technology for treating male factor infertility? Expert Rev Obstet Gynecol 2008;3:267-271.
2. Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M. Proteomic characterization of the human centrosome by protein correlation profiling. Nature 2003;426:570-574.
3. Baccetti B, Burrini AG, Collodel G, Magnano AR, Piomboni P, Renieri T, Sensini C. Morphogenesis of the decapitated and decaudated sperm defect in two brothers. Gamete Res 1989;23:181-188.
4. Bornens M. Centrosome composition and microtubule anchoring mechanisms. Curr Opin Cell Biol 2002;14:25-34.
5. Carrell DT. Paternal genetic and epigenetic influences on IVF outcome. Expert Rev Obstet Gynecol 2008;3:359-367.
6. Chemes HE, Puigdomenech ET, Carizza C, Brugo Olmedo S, Zanchetti F, Hermes A. Acephalic spermatozoa and abnormal development of the head-neck attachment. A human syndrome of genetic origin. Hum Reprod 1999;14:1811-1818.
7. Colombero LT, Moomjy M, Rosenwaks Z, Palermo GD. Indirect evidence of centrosome and spindle development in embryos generated by sperm segments. Hum Reprod 1996;11:21-22.
8. Comizzoli P, Wildt DE, Pukazhenthi BS. Poor centrosomal function of cat testicular spermatozoa impairs embryo development in vitro after intracytoplasmic sperm injection. Biol Reprod 2006;75 252-260.
9. Crozet N, Dahirel M, Chesne P. Centrosome inheritance in sheep zygotes; centrioles are contributed by the sperm. Microsc Res Tech 2000; 49:445-450.
10. Dam AHDM, Feenstra I, Westphal JR, Ramos L, van Golde RJT, Kremer JAM. Globozoospermia revisited. Hum Reprod Update 2007; 13:63-75.
11. Dictenberg J, Zimmerman W, Sparks C, Young A, Vidair C, Zheng Y, Carrington W, Fay F, Doxsey SJ. Pericentrin and gamma tubulin form a protein complex and are organized into a novel lattice at the centrosome. J Cell Biol 1998;141:163-174.
12. Doxsey SJ, Stein P, Evans L, Calarco P, Kirschner M. Pericentrin, a highly conserved protein of centrosomes involved in microtubule organization. Cell 1994;76:639-650.
13. Fawcett DW. The anatomy of the mammalian spermatozoon with particular reference to the guinea pig. Z Zellforsch 1965;67:279-296.
14. Fawcett DW, Ito S. The fine structure of bat spermatozoa. Am J Anat 1965; 116:567-609.
15. Fawcett DW, Phillips DM. The fine structure and development of the neck region of the mammalian spermatozoon. Anat Rec 1969;165 153-184.
16. Griffith E,Walker S, Martin C-A, Vagnarelli P, Stiff T, Vernay B, Al Sanna N, Saggar A, hamel B, Earnshaw WC et al. Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat Genet 2008;40:232-236.
17. Hayasaka S, Terada Y, Morita J, Tachibana M, Shima-Morito Y, Kakoi-Yoshimoto T, Nakamura S, Murakami T, Yaegashi N, Okamura K. Post-ICSI cytoskeletal dynamics during fertilization. J Mamm Ova Res 2006;23:21-26.
18. Hewitson L. Primate models for assisted reproductive technologies. Reproduction 2004;128:293-299.
19. Holstein AF, Roosen-Runge EC. Atlas of Human Spermatogenesis. Berlin:GRosse Verlag, 1981.
20. Kim NH, Moon SJ, Prather RS, Day BN. Cytoskeletal alteration in aged porcine oocytes and parthenogenesis. Mol Reprod Dev 1996;43 513-518.
21. Kochanski R, Borisy G. Mode of centriole duplication and distribution. J Cell Biol 1990;110:1599-1605.
22. Kono T, Obata Y, Wu Q, Niwa K, Ono Y, Yamamoto Y, Park ES, Seo JS, Ogawa H. Birth of parthenogenetic mice that can develop to adulthood. Nature 2004;428:860-864.
23. Jurczyk A, Gromley A, Redick S, Augustin JS, Witman G, Pazour GJ, Peters DJM, Doxsey S. Pericentrin forms a complex with intraflagellar transport proteins and polycystin-2 and is required for primary cilia assembly. J Cell Biol 2004;166:637-643.
24. Levy YY, Lai EY, Remillard SP, Heintzelman MB, Fulton C. Centrin is a conserved protein that forms diverse associations with centrioles and MTOCs in Naegleria and other organisms. Cell Motil Cytoskeleton 1996;33:298-323.
25. Lutz W, Lingle WL, McCormick D, Greenwood TM, Salisbury JL. Phosphorylation of centrin during the cell cycle and its role in centriole separation preceding centrosome duplication. J Biol Chem 2001;276:20774-20780.
26. Manandhar G, Simerly C, Schatten G. Highly degenerated distal centrioles in rhesus and human spermatozoa. Hum Reprod 2000;15:256-263.
27. Manandhar G, Schatten H, Sutovsky P. Centrosome reduction during gametogenesis and its significance. Biol Reprod 2005;72:2-13.
28. Manandhar G, Feng D, Yi YJ, Lai L, Letko J, Laurincik J, Sutovsky M, Salisbury JL, Prather RS, Schatten H et al. Centrosomal protein centrin is not detectable during early pre-implantation development but re-appears during late blastocyst stage in porcine embryos. Reproduction 2006;132:423-434.
29. McIntosh JR, Euteneuer U. Tubulin hooks as probes for microtubule polarity: An analysis of the method and an evaluation of data on microtubule polarity in the mitotic spindle. J Cell Biol 1984; 98:525-533.
30. Nakamura S, Terada Y, Horiuchi T, Emuta C, Murakami T, Yaegashi N, Okamura K. Human sperm aster formation and pronuclear decondensation in bovine eggs following intracytoplasmic sperm injection using a Piezo-driven pipette. Biol Reprod 2001;65:1359-1363.
31. Nakamura S, Terada Y, Horiuchi T, Emuta C, Murakami T, Yaegashi N, Okamura K. Analysis of the human sperm centrosomal function and the oocyte activation ability in a case of globozoospermia, by ICSI into bovine oocytes. Hum Reprod 2002;17:2930-2934.
32. Navara CS, First NL, Schatten G. Phenotypic variations among paternal centrosomes expressed within the zygote as disparate microtubule lengths and sperm aster organization: Correlations between centrosome activity and developmental success. Proc Natl Acad Sci USA 1996;93 5384-5388.
33. Ozil JP. The parthenogenetic development of rabbit oocytes after repetitive pulsatile electrical stimulation. Development 1990; 109:117-127.
34. Palermo G, Joris H, Devroey P, Van Steirteghem A. Pregnancies after intracytoplasmic sperm injection of single spermatozoon into an oocyte. Lancet 1992;340:17-18.
35. Palermo GD, Colombero LT, Rosenwaks Z. The human sperm centrosome is responsible for normal syngamy and early embryonic development. Rev Reprod 1997;2:19-27.
36. Paoletti A, Moudjou M, Paintrand M, Salisbury JL, Bornens M. Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J Cell Sci 1996; 109:3089-3102.
37. Paweletz N, Mazia D, Finze EM. 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 1987;44:195-204.
38. Porcu G, Mercier G, Boyer P, Achard V, Banet J, Vasserot M, Melone C, Saias-Magnan J, D'Ercole C, Chau C et al. Pregnancies after ICSI using sperm with abnormal head-tail junction from two brothers: Case report. Hum Reprod 2003;18:562-567.
39. Rawe V, Terada Y, Nakamura S, Chillik CF, Brugo Olmedo S, Chemes HE. A pathology of the sperm centriole responsible for defective sperm aster formation, sygamy and cleavage. Hum Reprod 2002; 17 2344-2349.
40. Rawe VY, Díaz ES, Abdelmassih R, Wójcik C, Morales P, Sutovsky P, Chemes HE. The role of sperm proteasomes during sperm aster formation and early zygote development: Implications for fertilization failure in humans. Human Reprod 2008;23:573-580.
41. Salisbury JL. Centrin, centrosomes, and mitotic spindle poles. Curr Opin Cell Biol 1995;7:39-45.
42. Salisbury JL, Suino KM, Busby R, Springett M. Centrin-2 is required for centriole duplication in mammalian cells. Curr Biol 2002;12 1287-1292.
43. Sathananthan AH, Osborne IKJ, Trounson A, Bongso SC, Ng A, Ratnam SS. Centrioles in the beginning of human development. Proc Natl Acad Sci USA 1991;88:4806-4810.
44. Sathananthan AH, Ratnam SS, Ng SC, Tarin JJ, Gianaroli L, Trounson A. The sperm centriole: Its inheritance, replication and perpetuation in early human embryos. Hum Reprod 1996;11:345-356.
45. Schatten H. The mammalian centrosome and its functional significance. Histochem Cell Biol 2008;129:667-686.
46. Schatten H, Sun QY. The functional significance of centrosomes in mammalian meiosis, fertilization, development, nuclear transfer, and stem cell differentiation. Environ Mol Mutagen 2009; Apr 28 [Epub ahead of print].
47. Schatten G, Simerly C, Schatten H. Maternal inheritance of centrosomes in mammals? Studies on parthenogenesis and polyspermy in mice. Proc Natl Acad Sci USA 1991;88:6785-6789.
48. Schatten H, Walter M, Biessmann H, Schatten G. Activation of maternal centrosomes in unfertilized sea urchin eggs. Cell Motil Cytoskeleton 1992;23:61-70.
49. Sofikitis N, Miyagawa I, Sharplip I, Hellstrom W, Mekras G, Mastelou E. Human pregnancies achieved by intra-ooplasmic injections of round spermatid (RS) nuclei isolated from testicular tissue of azoospermic men. J Urol 1995;153(Suppl 1):258A.
50. Sun QY, Schatten H. Multiple roles of NuMA in vertebrate cells: Review of an intriguing multi-functional protein. Front Biosci 2006;11 1137-1146.
51. Sun QY, Schatten H. Centrosome inheritance after fertilization and nuclear transfer in mammals. In: Sutovsky Peter (ed). Somatic Cell Nuclear Transfer, Vol. 591, Landes Bioscience, Adv Exp Med Biol, 2007, 58-71.
52. Szollosi D, Ozil JP. De novo formation of centrioles in parthenogenetically activated, diploidized rabbit embryos. Biol Cell 1991;72:61-66.
53. Tachibana M, Terada Y, Ogonuki N, Ugajin T, Ogura A, Murakami T, Yaegashi N, Okamura K. Functional assessment of centrosomes of spermatozoa and spermatids microinjected into rabbit oocytes. Mol Reprod Dev 2009;76:270-277.
54. Terada Y, Nakamura S, Simerly C, Hewitson L, Murakami T, Yaegashi N, Okamura K, Schatten G. Centrosomal function assessment in human sperm using heterologous ICSI with rabbit eggs; a new male factor infertility assay. Mol Reprod Dev 2004;67:360-365.
55. Terada Y. Functional analyses of the sperm centrosome in human reproduction: Implications for assisted reproductive technique. Soc Reprod Fertil Suppl 2007;63:507-513.
56. Terada Y, Simerly CR, Hewitson L, Schatten G. Sperm aster formation and pronuclear decondensation during rabbit fertilization and development of a functional assay for human sperm. Biol Reprod 2000;62 557-563.
57. Terada Y, Nakamura S, Hewitson L, Simerly CR, Horiuchi T, Murakami T, Okamura K, Schatten G. Human sperm aster formation after intracytoplasmic sperm injection with rabbit and bovine eggs. Fertil Steril 2002;77:1283-1284.
58. Terada Y, Hasegawa H, Ugajin T, Murakami T, Yaegashi N, Okamura K. Microtubule organization during human parthenogenesis. Fertil Steril 2009a;90:1271-1272.
59. Terada Y, Hasegawa H, Takahashi A, Ugajin T, Yaegashi N, Okamura K. Successful pregnancy after oocyte activation by a calcium ionophore for a patient with recurrent intracytoplasmic sperm injection failure, with an assessment of oocyte activation and sperm centrosomal function using bovine eggs. Fertil Steril 2009b;91:935.e11-935.e14.
60. Ugajin T, Terada Y, Hasegawa H, Murakami T, Yaegashi N, Okamura K. Novel strategy of ICSI - selection of sperm with morphologically normal midpiece by using IMSI. Fertil Steril 2008;90; abstract P-284.
61. Van Blerkom J, Davis P. Evolution of the sperm aster microinjection of isolated human sperm centrosomes into meiotically mature human oocytes. Hum Reprod 1995;10:2179-2182.
62. Winston N, Johnson M, Pickering S, Braude P. Parthenogenetic activation and development of fresh and aged human oocytes. Fertil Steril 1991; 56:904-912.
63. Yanagimachi R. Intracytoplasmic injection of spermatozoa and spermatogenic cells: Its biology and applications in humans and animals. Reproductive Biomedicine Online 2005;10:247-288.
64. Yoshimoto-Kakoi T, Terada Y, Tachibana M, Murakami T, Yaegashi N, Okamura K. Assessing centrosomal function of infertile males using heterologous ICSI. Syst Biol Reprod Med 2008;54:135-142.
65. Young A, Dictenberg JB, Purohit A, Tuft R, Doxsey SJ. Cytoplasmic dynein-mediated assembly of pericentrin and γ-tubulin onto centrosomes. Mol Biol Cell 2000;11:2047-2056.