Download PDF
Semin Reprod Med 2000; 18(2): 151-160
DOI: 10.1055/s-2000-12554
Copyright © 2000 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

Cytoskeletal Aspects of Assisted Fertilization

L. Hewitson, D. Phil1,3 , C. Simerly1,3 , G. Schatten1,2,3
  • 1Department of Obstetrics & Gynecology, Oregon Health Sciences University, Portland, Oregon
  • 2Department of Cell and Development Biology, Oregon Health Sciences University, Portland, Oregon and
  • 3Division of Reproductive Sciences, Oregon Regional Primate Research Center, Beaverton, Oregon
Further Information

Publication History

Publication Date:
31 December 2000 (online)

    Permissions and Reprints

ABSTRACT

During mammalian fertilization, the zygotic centrosome organizes a large sperm aster, critical for uniting the male and female pronuclei prior to first mitosis. Fluorescent imaging of inseminated human oocytes has shown that centrosomal defects may result in abnormal microtubule nucleation preventing genomic union, suggesting a novel cause of fertilization failure. Working with rhesus monkey gametes, we have developed a preclinical model for understanding the cell biological basis of intracytoplasmic sperm injection (ICSI). Typically, ICSI results in abnormal nuclear remodeling during sperm decondensation due to the presence of the sperm acrosome and perinuclear theca, structures normally removed at the oolemma during IVF; this is turn causes a delay in the onset of DNA synthesis. These unusual modifications raise concerns that the ICSI procedure itself may result in chromatin damage during DNA decondensation and further highlight the need for a more rigorous assessment of methods of assisted reproduction prior to their global application.

KEYWORD

fertilization - intracytoplasmic sperm injection

REFERENCES

  • 1 Schatten G. The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization.  Dev Biol . 1994;  165 299-335
    CrossrefPubMedGoogle Scholar
  • 2 Simerly C, Wu G, Zoran S. The paternal inheritance of the centrosome, the cell's microtubule-organizing center, in humans and the implications for infertility.  Nat Med . 1995;  1 47-53
    PubMedGoogle Scholar
  • 3 Wu G, Simerly C, Zoran S, Funte L R, Schatten G. Microtubule and chromatin configurations during fertilization and early development in rhesus monkeys, and regulation by intracellular calcium ions.  Biol Reprod . 1996;  55 269-271
    PubMedGoogle Scholar
  • 4 Navara C S, First N L, Schatten G. Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: the role of the sperm aster.  Dev Biol . 1994;  162 29-40
    CrossrefPubMedGoogle Scholar
  • 5 Schatten G, Simerly C, Schatten H. 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 . 1985;  82 4152-4156
    PubMedGoogle Scholar
  • 6 Hewitson L, Haavisto A, Simerly C, Jones J, Schatten G. Microtubule organization and chromatin configurations in hamster oocytes during fertilization and parthenogenetic activation, and after insemination with human sperm.  Biol Reprod . 1997;  57 967-975
    PubMedGoogle Scholar
  • 7 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
    CrossrefPubMedGoogle Scholar
  • 8 Van Steirteghem C A, Nagy Z, Joris H. High fertilization and implantation rates after intracytoplasmic sperm injection.  Hum Reprod . 1993;  8 1061-1066
    PubMedGoogle Scholar
  • 9 Bourne H, Richings N, Liu D Y, Clarke G N, Harari O, Baker H W. The use of intracytoplasmic sperm injection for the treatment of severe and extreme male infertility.  Reprod Fertil Dev . 1995;  7 237-245
    CrossrefPubMedGoogle Scholar
  • 10 Goldstein M, Menendez S, Zaninovic N, Veeck L L, Rosenwaks Z. Testicular sperm extraction with intracytoplasmic sperm injection for nonobstructive azoospermia.  Urology . 1997;  49 435-440
    CrossrefPubMedGoogle Scholar
  • 11 von Zumbusch A, Fiedler K, Mayerhofer A, Jessberger B, Ring J, Vogt H J. Birth of healthy children after intracytoplasmic sperm injection in two couples with male Kartagener's syndrome.  Fertil Steril . 1998;  70 643-646
    CrossrefPubMedGoogle Scholar
  • 12 Liu J, Nagy Z, Joris H, Tournaye H, Devroey P, Van Steirteghem A. Successful fertilization and establishment of pregnancies after intracytoplasmic sperm injection in patients with globozoospermia.  Hum Reprod . 1995;  10 626-629
    PubMedGoogle Scholar
  • 13 Nagy Z P, Liu J, Joris H. The result of intracytoplasmic sperm injection is not related to any of the three basic sperm parameters.  Hum Reprod . 1995;  10 1123-1129
    PubMedGoogle Scholar
  • 14 Tournaye H, Liu J, Nagy Z. Correlation between testicular histology and outcome after intracytoplasmic sperm injection using testicular spermatozoa.  Hum Reprod . 1996;  11 127-132
    PubMedGoogle Scholar
  • 15 In't Velt P, Brandenburg H, Verhoeff A, Dhont M, Los F. Sex chromosomal abnormalities and intracytoplasmic sperm injection.  Lancet . 1995;  773 346
    PubMedGoogle Scholar
  • 16 Silber S J, Nagy Z, Liu J. The use of epididymal and testicular spermatozoa for intracytoplasmic sperm injection: the genetic implications for male infertility.  Hum Reprod . 1995;  10 2031-2043
    PubMedGoogle Scholar
  • 17 Kent-First M G, Kol S, Muallem A. The incidence and possible relevance of Y-linked microdeletions in babies born after intracytoplasmic sperm injection and their infertile fathers.  Mol Hum Reprod . 1996;  2 943-950
    CrossrefPubMedGoogle Scholar
  • 18 Vogt P. Genetic aspects of artificial fertilization.  Hum Reprod . 1995;  10 128-137
    PubMedGoogle Scholar
  • 19 Mulhall J P, Reijo R, Alagappan R. Azoospermic men with deletion of the DAZ gene cluster are capable of completing spermatogenesis: fertilization, normal embryonic development and pregnancy occur when retrieved testicular spermatozoa are used for intracytoplasmic sperm injection.  Hum Reprod . 1997;  12 503-508
    CrossrefPubMedGoogle Scholar
  • 20 Patrizio P. Intracytoplasmic sperm injection (ICSI): potential genetic concerns.  Hum Reprod . 1995;  10 2520-2523
    PubMedGoogle Scholar
  • 21 Cummins J M. Controversies in science: ICSI may foster birth defects.  J NIH Res . 1997;  9 36-40
    PubMedGoogle Scholar
  • 22 Schatten G, Hewitson L, Simerly C, Huszar G. Cell and molecular biological challenges of ICSI: A.R.T. before science?.  J Law Med Ethics . 1998;  26 29-37
    PubMedGoogle Scholar
  • 23 Bonduelle M, Joris H, Hofmans K, Liebaers I, Van Steirteghem A. Mental development of 201 ICSI children at 2 years of age.  Lancet . 1998;  351 1553
    CrossrefPubMedGoogle Scholar
  • 24 Bonduelle M, Aytoz A, Van Assche E, Devroey P, Liebaers I, Van Steirteghem A. Incidence of chromosomal aberrations in children born after assisted reproduction through intracytoplasmic sperm injection.  Hum Reprod . 1998;  13 781-782
    CrossrefPubMedGoogle Scholar
  • 25 Asch R, Simerly C, Ord T, Ord V A, Schatten G. The stages at which human fertilization arrests: microtubule and chromosome configurations in inseminated oocytes which fail to complete fertilization and development in humans.  Hum Reprod . 1995;  10 1897-1906
    PubMedGoogle Scholar
  • 26 Terada Y, Simerly C, 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
    PubMedGoogle Scholar
  • 27 Hewitson L, Simerly C, Tengowski M W. Microtubule and chromatin configurations during rhesus intracytoplasmic sperm injection: successes and failures.  Biol Reprod . 1996;  55 271-280
    PubMedGoogle Scholar
  • 28 Sutovsky P, Hewitson L, Simerly C. Intracytoplasmic sperm injection for rhesus monkey fertilization results in unusual chromatin, cytoskeletal and membrane events, but eventually leads to pronuclear development and sperm aster assembly.  Hum Reprod . 1996;  11 1703-1712
    PubMedGoogle Scholar
  • 29 Compton D A, Cleveland D W. NuMA, a nuclear protein involved in mitosis and nuclear reformation.  Curr Opin Cell Biol . 1994;  6 343-346
    CrossrefPubMedGoogle Scholar
  • 30 Hewitson L, Dominko T, Takahashi D. Unique checkpoints during the first cell cycle of fertilization after intracytoplasmic sperm injection in rhesus monkeys.  Nat Med . 1999;  5 431-433
    PubMedGoogle Scholar
  • 31 Conner S, Leaf D, Wessel G. Members of the SNARE hypothesis are associated with cortical granule exocytosis in the sea urchin egg.  Mol Reprod Dev . 1997;  48 106-118
    CrossrefPubMedGoogle Scholar
  • 32 Ramalho-Santos J, Moreno R D, Sutovsky P. SNAREs in mammalian sperm: possible implications for fertilization.  Dev Biol . 2000;  223 54-69
    CrossrefPubMedGoogle Scholar
  • 33 Sutovsky P, Oko R, Hewitson L, Schatten G. Binding of oocyte microvilli to the perinuclear theca of fertilizing sperm and subsequent theca removal constitute a previously unrecognized step in mammalian fertilization.  Dev Biol . 1997;  188 75-84
    CrossrefPubMedGoogle Scholar
  • 34 Luetjens M, Payne C, Schatten G. Non-random chromosome positioning in human sperm and sex chromosome anomalies following intracytoplasmic sperm injection.  Lancet . 1999;  353 1240
    CrossrefPubMedGoogle Scholar
  • 35 Silva C P, Kommineni K, Oldenbourg R, Keefe D L. The first polar body does not predict accurately the location of the metaphase II meiotic spindle in mammalian oocytes.  Fertil Steril . 1999;  71 719-721
    CrossrefPubMedGoogle Scholar
  • 36 Chan A WS, Luetjens C M, Dominko T. TransgenICSI: foreign DNA transmission by intracytoplasmic sperm injection: injection of sperm bound with exogenous DNA results in embryonic GFP expression and live rhesus births.  Mol Hum Reprod . 1999;  6 26-33
    PubMedGoogle Scholar
      >