Journal of Embryo Transfer (한국수정란이식학회지)

The Korean Society of Embryo Transfer (한국수정란이식학회)
권호 표지

Sperm Cytosolic Factor Activation for Bovine Somatic Cell Nuclear Transfer

  • Received : 2011.08.05
  • Accepted : 2011.08.23
  • Published : 2011.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

In this study I report that in vitro development rates of bovine nuclear transfer embryos activated either with boar sperm cytosolic factor (SCF) or with ionomycin followed by cycloheximide (CHX) and subsequent in vivo developmental rates after embryo transfer are related to blastocyst quality as evaluated by apoptosis analysis. SCF was extracted from porcine semen then purified for post-activation injection after nuclear transfer. The optimal timing for SCF injection was determined to be at least 22 h post-IVM for parthenogenetic activation of bovine oocyies. A total of 364 oocytes were successfully enucleated and 268 (73.6%) fused and were injected with SCF. The survival rate of fused and injected embryos was 109/113 (96.5%) after 2 h. The cleavage rates of nuclear transfer embryos after 3 d of culture in the ionomycin/CHX treated group were significantly higher than those of the SCF-activated group (93.3% vs 81.7%, p<0.01, respectively). However, at 7 d and 9 d there was no significant difference between the total developmental rates to blastocyst for either treatment group. Total blastocyst cell numbers were also not significantly different between the two activation treatments (ionomycin/CHX: 149.5${\pm}$7.7 vs. SCF: 139.3${\pm}$4.4 cells). In contrast, the apoptotic levels in the SCF blastocysts were higher than those produced after the chemical treatment (28.2${\pm}$5.1% vs. 8.8${\pm}$0.6%, respectively). A total of 18 expanded or hatching blastocysts was transferred to nine synchronized recipients in each activation group; 5/9 (55.5%) and 2/9 (22.2%) were pregnant at 40 d in the ionomycin/CHX treatment and SCF activated group, respectively. However, only one went to term in the ionomycin/CHX treatment while none of the pregnancies from the SCF group were maintained by 90 d. In conclusion, these results suggest that SCF derived from different species is a limited activator to be used for activation after bovine nuclear transfer in lieu of a chemical activation protocol.

Keywords

References

  1. Baguisi A, Behboodi E, Melican DT, Pollock JS, Destrempes MM, Cammuso C, Williams JL, Nims SD, Porter CA, Midura P, Palacios MJ, Ayres SL, Denniston RS, Hayes ML, Ziomek CA, Meade HM, Godke RA, Gavin WG, Overstrom EW and Echelard Y. 1999. Production of goats by somatic cell nuclear transfer. Nat. Biotech. 17:456-461. https://doi.org/10.1038/8632
  2. Brison DR and Schultz RM. 1997. Apoptosis during mouse blastocyst formation; evidence for a role for survival factors including transforming growth factor $\alpha$. Biol. Reprod. 56:1088-1096. https://doi.org/10.1095/biolreprod56.5.1088
  3. Brison DR and Schultz RM. 1998. Increased incidence of apoptosis in transforming growth factor $\alpha$-deficient mouse blastocysts. Biol. Reprod. 59:136-144. https://doi.org/10.1095/biolreprod59.1.136
  4. Chesne P, Adenot PG, Viglietta C, Baratte M, Boulanger L and Renard JP. 2002. Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat. Biotech. 20:366-369. https://doi.org/10.1038/nbt0402-366
  5. Cibelli J, Stice SL, Golueke PJ, Kane JJ, Jerry J, Blackwell C, Ponce de Leon FA and Robl JM. 1998. Transgenic bovine chimeric offspring produced from somatic cell-derived stemlike cells. Nat. Biotech. 16:642-646. https://doi.org/10.1038/nbt0798-642
  6. Cuthbertson KS and Cobbold PH. 1985. Phorbol ester and sperm activate mouse oocytes by inducing sustained oscillations in cell $Ca^{2+}$. Nature 316:541-542. https://doi.org/10.1038/316541a0
  7. de Nadai C, Fenichel P, Donzeau M, Epel D and Ciapa B. 1996. Characterisation and role of integrins during gametic interaction and egg activation. Zygote 4:31-40. https://doi.org/10.1017/S0967199400002860
  8. Dozortsev D, Rybouchkin A, DeSutter P, Qian C and Dhont M. 1995. Human oocyte activation following intracytoplasmic sperm injection : The role of the sperm cell. Hum. Reprod. 10:403-407. https://doi.org/10.1093/oxfordjournals.humrep.a135952
  9. Dupont G, McGuiness OM, Johnson MH, Berridge Mj and Borghese F. 1996. Phospholipase C in mouse oocytes : Characterization of $\beta$ and $\gamma$ isoforms and their possible involvement in sperm-induced $Ca^{2+}$ spiking. Biochemistry Journal 316:583-591. https://doi.org/10.1042/bj3160583
  10. Fissore RA, Dobrinsky JR, Balise JJ, Duby RT and Robl, JM. 1992. Patterns of intracellular $Ca^{2+}$concentration in fertilized bovine eggs. Biol. Reprod. 47:960-969. https://doi.org/10.1095/biolreprod47.6.960
  11. Fissore RA, Gordo AC and Wu H. 1998. Activation of development in mammals: Is there a role for a sperm cytosolic factor ? Theiogenology 49:43-52. https://doi.org/10.1016/S0093-691X(97)00401-9
  12. Fissore RA, Long CR, Duncan RP and Robl JM. 1999a. Initiation and organization of events during the first cell cycle in mammals: Applications in cloning. Cloning 1:89-100. https://doi.org/10.1089/15204559950019979
  13. Fissore RA, Reis MM and Palermo GD. 1999b. Sperm-induced calcium oscillations; Isolation of the $Ca^{2+}$ releasing component( s) of mammalian sperm extracts: The search continues. Mol. Human. Reprod. 5:189-192. https://doi.org/10.1093/molehr/5.3.189
  14. Galli C, Lagutina I, Crotti G, Colleoni S, Turini P, Ponderato N, Duchi R and Lazzari G. 2003. Pregnancy: A cloned horse born to its dam twin. Nature 424:635.
  15. Gardner DK, Lane M, Spitzer A and Batt PA. 1994. Enhanced rates of cleavage and development for sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: Amino acids, vitamins, and culturing embryos in groups stimulate development. Biol. Reprod. 50:390-400. https://doi.org/10.1095/biolreprod50.2.390
  16. Gordo AC, Wu H, He CL and Fissore RA. 2000. Injection of sperm cytosolic factor into mouse metaphase II oocytes induces different developmental fates according to the frequency of [$Ca^{2+}$]i oscillations and oocyte age. Biol. Reprod. 62:1370-1379. https://doi.org/10.1095/biolreprod62.5.1370
  17. Hardy K. 1997. Cell death in the mammalian blastocyst. Mol. Hum. Reprod. 3:919-925. https://doi.org/10.1093/molehr/3.10.919
  18. Hill JR, Winger QA, Long CR, Looney CR, Thompson JA and Westhusin ME. 2000. Development rates of male bovine nuclear transfer embryos derived from adult and fetal cells. Biol. Reprod. 62:1135-1140. https://doi.org/10.1095/biolreprod62.5.1135
  19. Jaffe LF. 1980. Calcium explosions as triggers of development. Ann. N.Y. Acad. Sci. 339:86-101. https://doi.org/10.1111/j.1749-6632.1980.tb15971.x
  20. Jurisicova A, Varmuza S and Casper RF. 1996. Programmed cell death and human embryo fragmentation. Mol. Hum. Reprod. 2:93-98. https://doi.org/10.1093/molehr/2.2.93
  21. Kato Y, Tani T, Sotomaru Y, Kurokawa K, Kato J, Doguchi H, Yasue H and Tsunoda Y. 1998. Eight calves cloned from somatic cells of a single adult. Science 282:2095-2098. https://doi.org/10.1126/science.282.5396.2095
  22. Kim MK, Jang G, Oh HJ, Yuda F, Kim HJ, Hwang WS, Hossein MS, Kim JJ, Shin NS, Kang SK and Lee BC. 2007. Endangered wolves cloned from adult somatic cells. Cloning and Stem Cells 9:130-137. https://doi.org/10.1089/clo.2006.0034
  23. Kline D and Kline JT. 1992. Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149:80-89. https://doi.org/10.1016/0012-1606(92)90265-I
  24. Knott JG, Kasinathan P, Wu H, Spell A, Fissore RA and Robl JM. 2001. Effect of porcine sperm factor on intracellular calcium and activation of bovine oocytes and development of nuclear transfer embryos. Theriogenology 55:455.
  25. Krisher RL, Lane M and Bavister BD. 1999. Developmental competence and metabolism of bovine embryos cultured in semi-defined and defined culture media. Biol. Reprod. 60: 1345-1352. https://doi.org/10.1095/biolreprod60.6.1345
  26. Kubota C, Yamakuchi H, Todoroki J, Mizoshita K, Tabara N,Barber M and Yang X. 2000. Six cloned calves produced from adult fibroblast cells after long-term culture. PNAS. 97:990-995. https://doi.org/10.1073/pnas.97.3.990
  27. Lee BC, Kim MK, Jang G, Oh HJ, Yuda F, Kim HJ, Hossein MS, Kim JJ, Kang SK, Schatten G and Hwang WS. 2005. Dog cloned from adult somatic cells. Nature 436:641. https://doi.org/10.1038/436641a
  28. Liu L, Ju J and Yang X. 1998. Differential inactivation of maturation- promoting factor and mitogen-activated protein kinase following parthenogenetic activation of bovine oocytes. Biol. Reprod. 59:537-545. https://doi.org/10.1095/biolreprod59.3.537
  29. Long CR, Dobrinsky, JR, Garret, WM and Johnson LA. 1998. Dual labeling of the cytoskeleton and DNA strand breaks in porcine embryos produced in vivo and in vitro. Mol. Reprod. Dev. 51:59-65. https://doi.org/10.1002/(SICI)1098-2795(199809)51:1<59::AID-MRD7>3.0.CO;2-V
  30. Matwee C, Betts DH and King WA. 2000. Apoptosis in the early bovine embryo. Zygote 8:57-68. https://doi.org/10.1017/S0967199400000836
  31. McCreath KJ, Howcroft J, Campbell KHS, Colman A, Schnieke AE, Kind AJ. 2000. Production of gene-targeted sheep by nuclear transfer from cultured somatic cells. Nature 405:1066-1069. https://doi.org/10.1038/35016604
  32. Miyazaki S, Hashimoto N, Yoshimoto Y, Kishimoto T and Igusa Y. 1986. Temporal and spatial dynamics of the periodic increase in intracellular free calcium at fertilization of golden hamster eggs. Dev. Biol. 118:259-267. https://doi.org/10.1016/0012-1606(86)90093-X
  33. Miyazaki S, Shirakawa H, Nakada K and Honda Y. 1993. Essential role of the inositol 1,4,5-triphosphate receptor/$Ca^{2+}$ release channel in $Ca^{2+}$ waves and $Ca^{2+}$ oscillations after fertilization in mammalian eggs. Dev. Biol. 158:62-78. https://doi.org/10.1006/dbio.1993.1168
  34. Miyazaki S. 1988. Inositol-1,4,5-triphosphate-induced calcium release and guanine nucleotide binding protein-mediated periodic calcium rises in golden hamster eggs. Journal of Cell Biology 106:345-353. https://doi.org/10.1083/jcb.106.2.345
  35. Nagai T. 1987. Parthenogenetic activation of cattle follicular oocytes in vitro with ethanol. Gamete Res. 16:243-249. https://doi.org/10.1002/mrd.1120160306
  36. Polejaeva IA, Chen S, Vaught TD, Page RL, Mullins J, Ball S, Boone J, Walker S, Ayares D, Colman A and Campbell KHS. 2000. Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407:86-90. https://doi.org/10.1038/35024082
  37. Presicce G and Yang X. 1994. Parthenogenetic development of bovine oocytes matured in vitro for 24 hr and activated by ethanol and cycloheximide. Mol. Reprod. Dev. 38:380-385. https://doi.org/10.1002/mrd.1080380405
  38. Schnieke AE, Kind AJ, Ritchie WA, Mycock K, Scott AR, Ritchie M, Wilmut I, Colman A and Campbell KH. 1997. Human Factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science 278:2130- 2133. https://doi.org/10.1126/science.278.5346.2130
  39. Schultz RM and Kopf GS. 1995. Molecular basis of mammalian egg activation. Curr. Top Dev. Biol. 30:21-62.
  40. Shin T, Kraemer D, Pryor J, Liu L, Rugila J, Howe L, Buck S, Murphy K, Lyons L and Westhusin M. 2002. A cat cloned by nuclear transplantation. Nature 415:859. https://doi.org/10.1038/nature723
  41. Spanos S, Becker DL, Winston RML and Hardy K. 2000. Antiapoptotic action of insulin-like growth factor-I during human preimplantation embryo development. Biol. Reprod. 63: 1413- 1420. https://doi.org/10.1095/biolreprod63.5.1413
  42. Stice SL and Robl RM. 1990. Activation of mammalian oocytes by a factor obtained from rabbit sperm. Mol. Reprod. Dev. 25:271-280.
  43. Susko-Parrish JL, Liebfried-Rutledge ML, Northey DL, Schutzkus V and First NL. 1994. Inhibition of protein kinases after an induced calcium transient causes transition of bovine oocytes to embryonic cycles without meiotic completion. Dev. Biol. 166:729-739. https://doi.org/10.1006/dbio.1994.1351
  44. Swann K and Lai FA. 1997. A novel signaling mechanisms for generation $Ca^{2+}$ oscillations at fertilization in mammals. BioEssays 19:371-378. https://doi.org/10.1002/bies.950190504
  45. Swann K. 1990. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development 110:1295-1302.
  46. Swann K. 1992. $Ca^{2+}$ oscillations and sensitization of $Ca^{2+}$ release in unfertilized mouse eggs injected with a sperm factor. Cell Calcium 15:331-339.
  47. Tesarik J, Souza M and Testart J. 1994. Human oocyte activation after intracytoplasmic sperm injection. Hum. Reprod. 9:511-518. https://doi.org/10.1093/oxfordjournals.humrep.a138537
  48. Wakayama T, Perry AC, Zuccoti M, Johnson KR and Yanagimachi R. 1998. Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394:369-374. https://doi.org/10.1038/28615
  49. Ware CB, Barnes FL, Maiki-Laurila M and First NL. 1989. Age dependence of bovine oocyte activation. Gamete Res. 22:265-275. https://doi.org/10.1002/mrd.1120220304
  50. Watson AJ, De Sousa P, Caveney A, Barcroft LC, Natale D, Urquhart J and Westhusin ME. 2000. Impact of bovine oocyte maturation media on oocyte transcript levels, blastocyst development, cell number, and apoptosis. Biol. Reprod. 62:355-364. https://doi.org/10.1095/biolreprod62.2.355
  51. Wells DN, Misica PM and Tervit HR. 1999. Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol. Reprod. 60:996-1005. https://doi.org/10.1095/biolreprod60.4.996
  52. Whitaker MJ and Patel R. 1990. Calcium and cell cycle control. Development 108:525-542.
  53. Williams CJ, Schultz RM and Kopf GS. 1992. Role of G proteins in mouse egg activation: Stimulatory effects of acetylcholine on the ZP2 to ZP2f conversion and pronuclear formation in eggs expressing a functional m1 muscarinic receptor. Dev. Biol. 151:288-296. https://doi.org/10.1016/0012-1606(92)90233-7
  54. Wilmut I, Schnieke AE, McWhir J, Kind AJ and Campbell KHS. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature 385:810-812. https://doi.org/10.1038/385810a0
  55. Wood GL, White KL, Vanderwall DK, Li GP, Aston KI, Bunch TD, Meerdo LN and Pate BJ. 2003. A mule cloned from fetal cells by nuclear transfer. Science 301:1063. https://doi.org/10.1126/science.301.5636.1036
  56. Wu H, He CL and Fissore RA. 1997. Injection of a porcine sperm factor triggers calcium oscillations in mouse oocytes and bovine eggs. Mol. Reprod. Dev. 46:176-189. https://doi.org/10.1002/(SICI)1098-2795(199702)46:2<176::AID-MRD8>3.0.CO;2-N
  57. Wu H, He CL, Jehn B, Black S and Fissore RA. 1998. Partial characterization of the calcium-releasing activity of porcine sperm cytosolic extracts. Dev. Biol. 203:369-381. https://doi.org/10.1006/dbio.1998.9070
  58. Yin XJ, Lee HS, Yu XF, Choi E, Koo BC, Kwon MS, Lee YS, Cho SJ, Jin GZ, Kim LH, Shin HD, Kim T, Kim NH and Kong IK. 2008. Generation of cloned transgenic cats expressing red fluorescence protein. Biol. Reprod. 78:425- 431. https://doi.org/10.1095/biolreprod.107.065185
  59. Zakhartchenko V, Durcova-Hills G, Stojkovic M, Schernthaner W, Prelle K, Steinborn R, Muller M, Brem G and Wolf E. 1999. Effects of serum starvation and re-cloning on the efficiency of nuclear transfer using bovine fetal fibroblasts. J. Reprod. Fert. 115:325-331. https://doi.org/10.1530/jrf.0.1150325
  60. Zhou Q, Renard JP, Le Friec G, Brochard V, Beaujean N, Cherifi Y, Fraichard A and Cozzi J. 2003. Generation of fertile cloned rats by regulating oocyte activation. Science 302: 1179. https://doi.org/10.1126/science.1088313