Factors affecting fertilization and embryonic development during intracytoplasmic sperm injection in pigs

Journal of Reproduction and Development

Volumn 57, Issue 2, 2011, Pages 183-187

  Nakai, Michiko ^a   Kashiwazaki, Naomi ^b   Ito, Junya ^b   Maedomari, Naoki ^b   Ozawa, Manabu ^a   Shino, Masao ^b   Noguchi, Junko ^a   Kaneko, Hiroyuki ^a   Kikuchi, Kazuhiro ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b AZABU UNIVERSITY   (Japan)

Author keywords

Embryonic development; Fertilization; ICSI; Pig

Indexed keywords

ACROSOME; ANIMAL; ARTICLE; DNA FRAGMENTATION; EMBRYO DEVELOPMENT; ENZYMOLOGY; FERTILIZATION; INTRACYTOPLASMIC SPERM INJECTION; MALE; OOCYTE; PHYSIOLOGY;

ACROSOME; ANIMALS; DNA FRAGMENTATION; EMBRYONIC DEVELOPMENT; FERTILIZATION; MALE; OOCYTES; SPERM INJECTIONS, INTRACYTOPLASMIC;

SUIDAE;

EID: 79957573199     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.10-200E     Document Type: Article

References (67)

1. Yanagimachi R. Intracytoplasmic injection of spermatozoa and spermatogenic cells: its biology and applications in humans and animals. Reprod Biomed Online 2005; 10: 247-288.
2. Morozumi K, Yanagimachi R. Incorporation of the acrosome into the oocyte during intracytoplasmic sperm injection could be potentially hazardous to embryo development. PNAS 2005; 102: 14209-14214.
3. Lacham-Kaplan O, Trounson A. Intractoplasmic sperm injection in mice: increased fertilization and development to term after induction of the acrosome reaction. Hum Reprod 1995; 10: 2642-2649.
4. Dozortsev D, Rybouchkin A, De Sutter P, Dhont M. Sperm plasma membrane damage prior to intracytoplasmic sperm injection: a necessary condition for sperm nucleus decondensation. Hum Reprod 1995; 10: 2960-2964.
5. Gomez MC, Catt JW, Gillan L, Evans G, Maxwell WMC. Effect of culture, incubation and acrosome reaction of fresh and frozen-thawed ram spermatozoa for in vitro fertilization and intracytoplasmic sperm injection. Reprod Fretil Dev 1997; 9: 665-673.
6. Nakai M, Kashiwazaki N, Takizawa A, Hayashi Y, Nakatsukasa E, Fuchimoto D, Noguchi J, Kaneko H, Shino M, Kikuchi K. Viable piglets generated from porcine oocytes matured in vitro and fertilized by intracytoplasmic sperm head injection. Biol Reprod 2003; 68: 1003-1008.
7. Calvin HI, Bedford JM. Formation of disulfide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis. J Reprod Fertil Suppl 1971; 13: 65-75.
8. Calvin HI, Yu CC, Bedford JM. Effects of epididymal maturation, zinc and copper on the reactive sulfhydryl content of structural elements in rat spermatozoa. Exp Cell Res 1973; 81: 333-341.
9. Marushige Y, Marushige K. Transformation of sperm histone during formation and maturation of rat spermatozoa. J Biol Chem 1975; 250: 39-45.
10. Perreault SD, Barbee RR, Slott VL. Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev Biol 1988; 125: 181-186.
11. Zirkin BR, Perreault SD, Naish SL. Formation and function of the male pronucleus during mammalian fertilization. In: The Molecular Biology of Fertilization. San Diego, CA: Academic Press, 1989: 91-114.
12. Yoshida M, Ishigaki K, Nagai T, Chikyu M, Pursel GV. Glutathione concentration during maturation and after fertilization in pig oocytes: relevance to the ability of oocytes to form male pronucleus. Biol Reprod 1993; 49: 89-94.
13. Katagiri C, Ohsumi K. Remodeling of sperm chromatin induced in egg extracts of amphibians. Int J Dev Bil 1994; 38: 209-216.
14. Yanagimachi R. Mammalian fertilization. In: Knobil E, Neil JD (eds.), The Physiology of Reproduction, 2nd ed. New York: Raven Press, 1994: 189-317.
15. Shimada A, Kikuchi K, Noguchi J, Akama K, Nakano M, Kaneko H. Protamine dissociation before decondensation of sperm nuclei during in vitro fertilization of pig oocytes. J Reprod Fertil 2000; 120: 247-256.
16. Kren R, Kikuchi K, Nakai M, Miyano T, Ogushi S, Nagai T, Suzuki S, Fulka J, Fulka J Jr. Intracytoplasmic sperm injection in the pig: where is the problem? J Reprod Dev 2003; 49: 271-273.
17. Catt JW, Rhodes SL. Comparative intracytoplasmic sperm injection (ICSI) in human and domestic speices. Reprod Fertil Dev 1995; 7: 161-167.
18. Keefer CL, Younis AI, Brackett BG. Cleavage development of bovine oocytes fertilized by sperm injection. Mol Reprod Dev 1990; 25: 281-285.
19. Wei H, Fukui Y. Effects of bull, sperm type and sperm pretreatment on male pronulear formation after intracytoplasmic sperm injection in cattle. Reprod Fertil Dev 1999; 11: 59-65.
20. Reyes R, Rosado A, Hernandez O, Delgaldo NM. Heparin and dlutathione: physiological decondensing agents of human sperm nuclei. Gamete Res 1989; 23: 39-47.
21. Szcygiel MA, Ward WS. Combination of dithiothreitol and detergent treatment of spermatozoa causes paternal chromosomal damage. Biol Reprod 2007; 67: 1532-1537.
22. Galli C, Vassiliev I, Lagutina I, Galli A, Lazzari G. Bovine embryo development following ICSI: effect of activation, sperm capacitation and pre-treatment with dithiothreitol. Theriogenology 2003; 60: 8: 1467-1480.
23. Rho GJ, Kawarsky S, Johnson WH, Kochhar K, Betteridge KJ. Sperm and oocyte treatments to improve the formation of male and female pronuclei and subsequent development following intracytoplasmic sperm injection into bovine oocytes. Bio Reprod 1998; 59: 918-924.
24. Perreault SD, Barbee RR, Elstein KH, Zucker RM, Keefer CL. Interspecies difference in the stability of mammalian sperm nuclei assessed in vivo by sperm microinjection and in vitro by flow cytometry. Biol Reprod 1988; 39: 157-167.
25. Watanabe H, Fukui Y. Effects of dithiothreitol and boar on pronuclear formation and embryonic development following intracytoplasmic sperm injection in pigs. Theriogenology 2006; 65: 3: 528-539.
26. Yong HY, Hong JY, Kang SK, Lee BC, Lee ES, Hwang WS. Sperm movement in the ooplasm, dithiothreitol pretreatment and sperm freezing are not required for the development of porcine embryos derived from injection of head membrane-damaged sperm. Theriogenology 2005; 63: 3: 783-794.
27. Nakai M, Kashiwazaki N, Takizawa A, Maedomari N, Ozawa M, Noguchi J, Kaneko H, Shino M, Kikuchi K. Morphologic changes in boar sperm nuclei with reduced disulfide bonds in electrostimulated porcine oocytes. Reproduction 2006; 131: 603-611.
28. Kolbe T, Holtz W. Birth of a piglet derived from an oocyte fertilized by intracytoplasmic sperm injection (ICSI). Anim Reprod Sci 2000; 64: 97-101.
29. Martin MJ. Development of in vivo-matured porcine oocytes following intracytoplasmic sperm injection. Biol Reprod 2000; 63: 109-112.
30. Lai L, Sun Q, Wu G, Murphy CN, Kuhholzer B, Park KW, Bonk AJ, Day BN, Prather RS. Development of porcine embryos and offspring after intracytoplasmic sperm injection with liposome transfected or non-transfected sperm into in vitro matured oocytes. Zygote 2001; 9: 339-346.
31. Nagashima H, Fujimura T, Takahagi Y, Kurome M, Wako N, Ochiai T, Esaki R, Kano K, Saito S, Okabe M, Murakami H. Development of efficient strategies for the production of genetically modified pigs. Theriogenology 2003; 59: 95-106.
32. Lee JW, Tian XC, Yang X. Failure of male pronucleus formation is the major cause of lack of fertilization and embryo development in pig oocytes subjected to intracytoplasmic sperm injection. Biol Reprod 2003; 68: 1341-1347.
33. Probst S, Rath D. Production of piglets using intracytoplasmic sperm injection (ICSI) with flowcytometrically sorted boar semen and artificially activated oocytes. Theriogenology 2003; 961-973.
34. Miyoshi K, Fujimoto Y, Mori H, Yoshida M. Activation and parthenogenetic development of pig oocytes exposed to ultrasound in media containing different concentrations of Ca2+. J Reprod Dev 2008; 54: 42-45.
35. Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA. PLς: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 2002; 129: 3533-3544.
36. Sun JG, Jurisicova A, Casper RF. Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 1997; 56: 602-607.
37. Lopes S, Sun JG, Jurisicova A, Meriano J, Casper RF. Sperm deoxyribonucleic acid fragmentation correlates in poor quality semen samples amd correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril 1998; 69: 528-532.
38. Nakai M, Kashiwazaki N, Takizawa A, Maedomari N, Ozawa M, Noguchi J, Kaneko H, Shino M, Kikuchi K. Effects of chelating agents during freeze-drying of boar spermatozoa on DNA fragmentation and on developmental ability in vitro and in vivo after intracytoplasmic sperm head injection. Zygote 2007; 15: 15-24.
39. Perez-Crespo M, Moreira P, Pintado B, Gutierrez-Adan A. Factors from damaged sperm affect its DNA integrity and its ability to promote embryo implantation in mice. Biol Reprod 2008; 29: 47-54.
40. Fernandez-Gonzalez R, Moreria PN, Perez-Crespo M, Sanchez-Marrin M, Ramirez MA, Pericuesta E, Bilbao A, Bermejo-Alvarez P, Hourcade JD, Fonseca FR, Gutierrez-Adan A. Long-term effects of mouse intracytoplasmic sperm injection with DNAfragented sperm on health and behavior of adult offspring. Bio Reprod 2008; 78: 761-772.
41. Henkel R, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C, Menkveld R, Gips H, Schill W, Kruger T. Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril 2004; 81: 965-972.
42. Evenson DP, Thompson L, Test L. Flow cytometric evaluation of boar semen by the sperm chromatin structure assay as related to cryopreservation and fertility. Theriogenology 1994; 41: 637-651.
43. Mione B, Pittoggi C, Achene L, Lorenzini R, Spadafora C. Activation of endogenous nucleases in mature sperm cells upon interaction with exogenous DNA. DNA Cell Biol 1997; 16: 1087-1097.
44. Kusakabe H, Szczygiel MA, Whittingham DG, Yanagimachi R. Maintenance of genetic integrity in frozen and freeze-dried mouse spermatozoa. Proc Natl Acad Sci USA 2001; 98: 13501-13506.
45. Sotolongo B, Huang TTF, Isenberger E, Ward WS. An endogenous nuclease in hamster, mouse, and human spermatozoa cleaves DNA into loop-sized fragments. J Androl 2005; 26: 272-280.
46. Yamauchi Y, Ajduk A, Riel J, Ward MA. Ejaculated and epididymal mouse spermatozoa are different in their susceptibility to nuclease dependent DNA damage and in their nuclease activity. Biol Reprod 2007; 77: 636-647.
47. Russell LD, Brinster RL. Ultrastructural observation of spermatogenesis following transplantation of rat testis cells into mouse seminiferous tubules. J Androl 1996; 17: 615-627.
48. Franca LR, Ogawa T, Avarbock MR, Brinster RL, Russell LD. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 1998; 59: 1371-1377.
49. Ogawa T, Dobrinski I, Avarbock MR, Brinster RL. Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes. Bil Reprod 1999; 60: 515-521.
50. Dobrinski I, Avarbock MR, Brinster RL. Germ cell transplantation from large domestic animals into mouse testes. Mol Reprod Dev 2000; 57: 270-279.
51. Dobrinski I, Avarbock MR, Brinster RL. Transplantaion of germ cells from rabbits and dogs into mouse testes. Biol Reprod 1999; 61: 1331-1339.
52. Honaramooz A, Snedaker A, Boiani M, Scholer H, Dobrinski I, Schlatt S. Sperm from neonatal mammalian testes grafted in mice. Nature 2002; 418: 778-781.
53. Zeng W, Avelar GF, Rathi R, Franca LR, Dobrinski I. The length of the spermatogenesis cycle is conserved in porcine and ovine tetis xenografts. J Androl 2006; 27: 527-533.
54. Zeng W, Rathi R, Pan H, Dobrinski I. Comparison of grobal gene expression between porcine testis tissue xenografts and porcine testis in situ. Mol Reprod Dev 2007; 74: 674-679.
55. Snedaker AK, Honaramooz A, Dobrinski I. A game of cat and mouse: xenografting of testis tissue from domestic kittens results in complete cat spermatogenesis in a mouse host. J Androl 2004; 25: 926-930.
56. Honaramooz A, Li MW, Penedo MCT, Meyers S, Dobrinski I. Accelerated maturation of primate testis by xenografting into mice. Biol Reprod 2004; 70: 1500-1503.
57. Kaneko H, Kikuchi K, Nakai M, Noguchi J. Endocrine status and development of porcine testicular tissues in host mice. J Reprod Dev 2008; 54: 480-485.
58. Nakai M, Kaneko H, Somfai T, Maedomari N, Ozawa M, Noguchi J, Ito J, Kashiwazaki N, Kikuchi K. Generation of porcine diploid blastocysts ater injection of spermatozoa grown in nude mice. Theriogenology 2009; 72: 2-9.
59. Honaramooz A, Cui XS, Kim NH, Dobrinski I. Porcine embryos produced after intracytoplasmic sperm injection using xenogeneic pig sperm from neonatal testis tissue grafted in mice. Reprod Fertil Dev 2008; 20: 802-807.
60. Nakai M, Kaneko H, Somfai T, Maedomari N, Ozawa M, Noguchi J, Ito J, Kashiwazaki N, Kikuchi K. Production of viable piglets for the first time using sperm derived from ectopic testicular xenografts. Reproduction 2010; 139: 331-335.
61. Wakayama T, Yanagimachi R. Development of normal mice from oocytes injected with freeze-dried spermatozoa. Nat Biotech 1998; 16: 639-641.
62. Kaneko T, Whittingham DG, Yanagimachi R. Effects of pH value of freeze-drying solution on the chromosome integrity and development ability of mouse spermatozoa. Biol Reprod 2003;. 68: 136-139.
63. Kaneko T, Whittingham DG, Overstreet JW, Yanagimachi R. Tolerance of the mouse sperm nuclei to freeze-drying depends on their disulphide status. Biol Reprod 2003; 69: 1859-1862.
64. Liu JL, Kusakabe H, Chang CC, Suzuki H, Schmidt DW, Julian M, Pfeffer R, Bormann CL, Tian XC, Yanagimachi R, Yang X. Freeze-dried sperm fertilization leads to full-term development in rabbits. Biol Reprod 2004; 70: 1776-1781.
65. Hirabayashi M, Kato M, Ito J, Hochi S. Viable offspring derived from oocytes intracytoplasmically injected with freeze-dried sperm heads. Zygote 2005; 13: 79-85.
66. Kwon IK, Park KE, Niwa K. Activation, pronuclear formation, and development in vitro of pig oocytes following intracytoplasmic injection of freeze-dried spermatozoa. Biol Reprod 2004; 71: 1430-1436.
67. Keskintepe L, Pacholczyk G, Machinicka A, Norris K, Curuk, MA, Khan L, Brackett BG. Bovine blastocyst development from oocytes injected with freeze-dried spermatozoa. Biol Reprod 2002; 67: 409-415.