Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-26T07:05:08.276Z Has data issue: false hasContentIssue false
  • English
  • Français

Biofluid mechanics of the human reproductive process: modelling of the complex interaction and pathway to the oocytes

Published online by Cambridge University Press:  01 November 2008

Jong Yong Abdiel Foo  and
Chu Sing Lim
Jong Yong Abdiel Foo*
Affiliation:
Division of Research, Singapore General Hospital, 31 Hospital Avenue, Bowyer Block A Level 3, Outram Road, Singapore169608. Biomedical & Pharmaceutical Engineering Cluster, Nanyang Technological University, 50 Nanyang Drive, Research Techno Plaza, 6th Storey, Xfrontiers Block, Singapore637553. Singapore Institute for Clinical Sciences, Agency for Science, Technology and Research (A* STAR), Brenner Centre for Molecular Medicine, 30 Medical Drive, Singapore117609.
Chu Sing Lim
Affiliation:
Singapore Institute for Clinical Sciences, Agency for Science, Technology and Research (A* STAR), Brenner Centre for Molecular Medicine, 30 Medical Drive, Singapore117609. School of Mechanical and Aerospace Engineering, Nanyang Technological University, 50 Nanyang Avenue, Singapore639798.
*
All correspondence to: Jong Foo. Division of Research, Singapore General Hospital, 31 Hospital Avenue, Bowyer Block A Level 3, Outram Road, Singapore169608. Tel: +65 6326 5295. Fax: +65 6326 5612. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Recent revelations in the human reproductive process have fuelled much interest in this field of study. In particular, the once prevailing view of large numbers of ejaculated sperms racing towards the egg has been refuted recently. This is opposed to the current views derived from numerous clinical findings that state that only a very small number of sperms will ever enter the oviduct. It is believed that these few sperms must have been guided to make the long, tedious and obstructed journey to the egg. For a mature spermatozoon, its hyperactivated swimming motility upon capacitation plays an important role in the fertilization of a mature egg. Likewise, the female genital tract also provides guiding mechanisms to complement the survival of normal hydrodynamic profile sperms and thus promotes an eventual sperm–egg interaction. Understanding these mechanisms can be essential for the derivation of assisted conception techniques especially those in vitro. With the aid of computational models and simulation, suitability and effectiveness of novel assisted conception methodology can be assessed, particularly for those yet to be ready for clinical trials. This review discusses the possible bioengineering models and the mechanisms by which human spermatozoa are guided to the egg.

Keywords

CapacitationChemotaxisFemale genital tractMuscular contractionsSperm motilityThermotaxis
Type
Research Article
Information
Zygote , Volume 16 , Issue 4 , November 2008 , pp. 343 - 354
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aitken, R.J. (2006). Sperm function tests and fertility. Int. J. Androl. 29, 69–75.Google Scholar
Andrietti, F. & Bernardini, G. (1994). The movement of spermatozoa with helical head, theoretical analysis and experimental results. Biophys. J. 67, 1767–74.CrossRefGoogle ScholarPubMed
Bahat, A. & Eisenbach, M. (2006). Sperm thermotaxis. Mol. Cell Endocrinol. 252, 115–9.Google Scholar
Bahat, A., Tur-Kaspa, I., Gakamsky, A., Giojalas, L.C., Breitbart, H. & Eisenbach, M. (2003). Thermotaxis of mammalian sperm cells, a potential navigation mechanism in the female genital tract. Nature Med. 9, 149–50.Google Scholar
Bahat, A., Eisenbach, M. & Tur-Kaspa, I. (2005). Periovulatory increase in temperature difference within the rabbit oviduct. Hum. Reprod. 20, 2118–21.CrossRefGoogle ScholarPubMed
Bastias, M.C., Kamijo, H. & Osteen, K.G. (1993). Assessment of human sperm functional changes after in-vitro coincubation with cells retrieved from the human female reproductive tract. Hum. Reprod. 8, 1670–77.CrossRefGoogle ScholarPubMed
Ben-Yosef, D., Oron, Y. & Shalgi, R. (1996). Intracellular pH is not affected by fertilisation and the resulting calcium oscillations. Biol. Reprod. 55, 461–8.Google Scholar
Bergqvist, A.S., Ballester, J., Johannisson, A., Hernandez, M., Lundeheim, N. & Rodriguez-Martinez, H. (2006). In vitro capacitation of bull spermatozoa by oviductal fluid and its components. Zygote 14, 259–73.CrossRefGoogle ScholarPubMed
Bianchi, P.G., De Agostini, A., Fournier, J., Guidetti, C., Tarozzi, N., Bizzaro, D. & Manicardi, G.C. (2004). Human cervical mucus can act in vitro as a selective barrier against spermatozoa carrying fragmented DNA and chromatin structural abnormalities. J. Assist. Reprod. Genet. 21, 97–102.CrossRefGoogle ScholarPubMed
Brawley, S.H. (1991). The fast block against polyspermy in fucoid algae is an electrical block. Dev. Biol. 144, 94–106.Google Scholar
Brewis, I.A., Moore, H.D., Fraser, L.R., Holt, W.V., Baldi, E., Luconi, M., Gadella, B.M., Ford, W.C. & Harrison, R.A. (2005). Molecular mechanisms during sperm capacitation. Hum. Fertil. 8, 253–61.Google Scholar
Brokaw, C.J. (2001). Simulating the effects of fluid viscosity on the behavior of sperm flagella. Math. Meth. Appl. Sci. 24, 1351–65.Google Scholar
Chretien, F.C. (2003). Involvement of the glycoproteic meshwork of cervical mucus in the mechanism of sperm orientation. Acta Obstet. Gynecol. Scand. 82, 449–61.Google Scholar
Cicinelli, E., Einer-Jensen, N., Barba, B., Luisi, D., Alfonso, R. & Tartagni, M. (2004). Blood to the cornual area of the uterus is mainly supplied from the ovarian artery in the follicular phase and from the uterine artery in the luteal phase. Hum. Reprod. 19, 1003–8.CrossRefGoogle Scholar
Cohen-Dayag, A., Tur-Kaspa, I., Dor, J., Mashiach, S. & Eisenbach, M. (1995). Sperm capacitation in humans is transient and correlates with chemotactic responsiveness to follicular factors. Proc. Natl. Acad. Sci. USA 92, 11039–43.Google Scholar
Cortez, R., Fauci, L. & Medovikov, A. (2005). The method of regularized Stokeslets in three dimensions, analysis, validation and application to helical swimming. Phys. Fluids 17, 031504–1-14.CrossRefGoogle Scholar
Dale, B., Menezo, Y., Cohen, J., DiMatteo, L. & Wilding, M. (1998). Intracellular pH regulation in the human oocyte. Hum. Reprod. 13, 964–70.Google Scholar
Dale, P. & Monroy, A. (1981). How is polyspermy prevented? Gamete Res. 4, 151–69.CrossRefGoogle Scholar
David, A., Vilensky, A. & Nathan, H. (1972). Temperature changes in the different parts of the rabbit's oviduct. Int. J. Gynaecol. Obstet. 10, 52–6.Google Scholar
Dunson, D.B., Bigelow, J.L. & Colombo, B. (2005). Reduced fertilization rates in older men when cervical mucus is suboptimal. Obstet. Gynecol. 105, 788–93.Google Scholar
Eddy, E.M., Toshimori, K. & O'Brien, D.A. (2003). Fibrous sheath of mammalian spermatozoa. Microsc. Res. Tech. 61, 103–15.CrossRefGoogle ScholarPubMed
Egydio de Carvalho, C., Tanaka, H., Iguchi, N., Ventela, S., Nojima, H. & Nishimune, Y. (2002). Molecular cloning and characterization of a complementary DNA encoding sperm tail protein SHIPPO 1. Biol. Reprod. 66, 785–95.Google Scholar
Eisenbach, M. & Giojalas, L.C. (2006). Sperm guidance in mammals—an unpaved road to the egg. Nat. Rev. Mol. Cell. Biol. 7, 276–85.Google Scholar
Eisenbach, M. & Tur-Kaspa, I. (1999). Do human eggs attract spermatozoa? Bioessays 21, 203–10.Google Scholar
Elder, K. & Dale, B. (2000). In Vitro Fertilization, 2nd edn. Cambridge: Cambridge University Press.Google Scholar
Eriksen, G.V., Carlstedt, I., Uldbjerg, N. & Ernst, E. (1998). Cervical mucins affect the motility of human spermatozoa in vitro. Fertil. Steril. 70, 350–4.CrossRefGoogle ScholarPubMed
Eytan, O. & Elad, D. (1999). Analysis of intra-uterine fluid motion induced by uterine contractions. Bull. Math. Biol. 61, 221–38.Google Scholar
Fauci, L. & Dillon, R. (2006). Biofluid mechanics of reproduction. Annu. Rev. Fluid Mech. 38, 371–94.CrossRefGoogle Scholar
Fulford, G.R., Katz, D.F. & Powell, R.L. (1998). Swimming of spermatozoa in a linear viscoelastic fluid. Biorheology 35, 295–309.Google Scholar
Gaddum-Rosse, P. (1985). Mammalian gamete interactions, what can be gained from observations on living eggs? Am. J. Anat. 174, 347–56.Google Scholar
Giojalas, L.C., Rovasio, R.A., Fabro, G., Gakamsky, A. & Eisenbach, M. (2004). Timing of sperm capacitation appears to be programmed according to egg availability in the female genital tract. Fertil. Steril. 82, 247–9.CrossRefGoogle ScholarPubMed
Hunter, R.H.F. & Nichol, R. (1986). A preovulatory temperature gradient between the isthmus and the ampulla of pig oviducts during the phase of sperm storage. J. Reprod. Fert. 77, 599–606.CrossRefGoogle ScholarPubMed
Ishijima, S., Baba, S.A., Mohri, H. & Suarez, S.S. (2002). Quantitative analysis of flagellar movement in hyperactivated and acrosome-reacted golden hamster spermatozoa. Mol. Reprod. Dev. 61, 376–84.CrossRefGoogle ScholarPubMed
Jaiswal, B.S., Cohen-Dayag, A., Tur-Kaspa, I. & Eisenbach, M. (1998). Sperm capacitation is, after all, a prerequisite for both partial and complete acrosome reaction. FEBS Lett. 427, 309–13.Google Scholar
Jaiswal, B.S., Tur-Kaspa, I., Dor, J., Mashiach, S. & Eisenbach, M. (1999). Human sperm chemotaxis, is progesterone a chemoattractant? Biol. Reprod. 60, 1314–9.CrossRefGoogle ScholarPubMed
Katz, D.F. & Berger, S.A. (1980). Flagellar propulsion of human sperm in cervical mucus. Biorheology 17, 169–75.Google Scholar
Katz, D.F., Slade, D.A. & Nakajima, S.T. (1997). Analysis of pre-ovulatory changes in cervical mucus hydration and sperm penetrability. Adv. Contracept. 13, 143–51.CrossRefGoogle ScholarPubMed
Kirichok, Y., Navarro, B. & Clapham, D.E. (2006). Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel. Nature 439, 737–40.CrossRefGoogle ScholarPubMed
Kunz, G., Beil, D., Deiniger, H., Einspanier, A., Mall, G. & Leyendecker, G. (1997). The uterine peristaltic pump. Normal and impeded sperm transport within the female genital tract. Adv. Exp. Med. Biol. 424, 267–77.CrossRefGoogle ScholarPubMed
Kunz, G., Beil, D., Huppert, P. & Leyendecker, G. (2000). Structural abnormalities of the uterine wall in women with endometriosis and infertility visualized by vaginal sonography and magnetic resonance imaging. Hum. Reprod. 15, 76–82.Google Scholar
Leyendecker, G., Kunz, G., Wildt, L., Beil, D. & Deininger, H. (1996). Uterine hyperperistalsis and dysperistalsis as dysfunctions of the mechanism of rapid sperm transport in patients with endometriosis and infertility, Hum. Reprod. 11, 1542–51.CrossRefGoogle ScholarPubMed
Luconi, M., Forti, G. & Baldi, E. (2006). Pathophysiology of sperm motility. Front. Biosci. 11, 1433–47.CrossRefGoogle ScholarPubMed
Lyons, E.A., Taylor, P.J., Zheng, X.H., Ballard, G., Levi, C.S. & Kredentser, J.V. (1991). Characterization of subendometrial myometrial contractions throughout the menstrual cycle in normal fertile women. Fertil. Steril. 55, 771–4.Google Scholar
Marquez, B. & Suarez, S.S. (2004). Different signaling pathways in bovine sperm regulate capacitation and hyperactivation. Biol. Reprod. 70, 1626–33.CrossRefGoogle ScholarPubMed
Mittal, R. & Iaccarino, G. (2005). Immersed boundary methods. Annu. Rev. Fluid. Mech. 37, 239–61.Google Scholar
Nishino, M., Togashi, K., Nakai, A., Hayakawa, K., Kanao, S., Iwasaku, K. & Fujii, S. (2005). Uterine contractions evaluated on cine MR imaging in patients with uterine leiomyomas. Eur. J. Radiol. 53, 142–6.CrossRefGoogle ScholarPubMed
Ohl, D.A., Menge, A.C. & Jarow, J.P. (1999). Seminal vesicle aspiration in spinal cord injured men, insight into poor sperm quality. J. Urol. 162, 2048–51.CrossRefGoogle ScholarPubMed
Petersen, C., Fuzesi, L. & Hoyer-Fender, S. (1999). Outer dense fibre proteins from human sperm tail, molecular cloning and expression analyses of two cDNA transcripts encoding proteins of approximately 70 kDa. Mol. Hum. Reprod. 5, 627–35.Google Scholar
Ralt, D., Manor, M., Cohen-Dayag, A., Tur-Kaspa, I., Ben-Shlomo, I., Makler, A., Yuli, I., Dor, J., Blumberg, S. & Mashiach, S. (1994). Chemotaxis and chemokinesis of human spermatozoa to follicular factors. Biol. Reprod. 50, 774–85.Google Scholar
Schuel, H., Burkman, L.J., Lippes, J., Crickard, K., Forester, E., Piomelli, D. & Giuffrida, A. (2002). N-Acylethanolamines in human reproductive fluids. Chem. Phys. Lipids 121, 211–27.Google Scholar
Scott, M.A. (2000). A glimpse at sperm function in vivo, sperm transport and epithelial interaction in the female reproductive tract. Anim. Reprod. Sci. 60–1, 337–48.Google Scholar
Snyder, M.G. & Zaneveld, L.J. (1985). Treatment of cervical mucus with lectins, effect on sperm migration. Fertil. Steril. 44, 633–7.CrossRefGoogle ScholarPubMed
Spehr, M., Schwane, K., Riffell, J.A., Barbour, J., Zimmer, R.K., Neuhaus, E.M. & Hatt, H. (2004). Particulate adenylate cyclase plays a key role in human sperm olfactory receptor-mediated chemotaxis. J. Biol. Chem. 279, 40194–203.CrossRefGoogle Scholar
Suarez, S.S. & Ho, H.C. (2003). Hyperactivation of mammalian sperm. Cell. Mol. Biol. 49, 351–6.Google ScholarPubMed
Suarez, S.S. & Pacey, A.A. (2006). Sperm transport in the female reproductive tract. Hum. Reprod. Update 12, 23–37.Google Scholar
Sun, F., Bahat, A., Gakamsky, A., Girsh, E., Katz, N., Giojalas, L.C., Tur-Kaspa, I. & Eisenbach, M. (2005). Human sperm chemotaxis, both the oocyte and its surrounding cumulus cells secrete sperm chemoattractants. Hum. Reprod. 20, 761–77.Google Scholar
Taylor, G.I. (1951). Analysis of the swimming of microscopic organisms. Proc. R. Soc. Lond. A 209, 447–61.Google Scholar
Tollner, T.L., Yudin, A.I., Cherr, G.N. & Overstreet, J.W. (2003). Real-time observations of individual macaque sperm undergoing tight binding and the acrosome reaction on the zona pellucida. Biol. Reprod. 68, 664–72.Google Scholar
Turner, R.M. (2003). Tales from the tail, what do we really know about sperm motility? J. Androl. 24, 790–803.CrossRefGoogle ScholarPubMed
Turner, R.M. (2006). Moving to the beat, a review of mammalian sperm motility regulation. Reprod. Fertil. Dev. 18, 25–38.Google Scholar
Wang, W.H., Day, B.N. & Wu, G.M. (2003). How does polyspermy happen in mammalian oocytes? Microsc. Res. Tech. 61, 335–41.CrossRefGoogle ScholarPubMed
Welch, J.E., Brown, P.L., O'Brien, D.A., Magyar, P.L., Bunch, D.O., Mori, C. & Eddy, E.M. (2000). Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells. J. Androl. 21, 328–38.Google Scholar
Wilding, M., Di Matteo, L. & Dale, B. (2005). The maternal age effect, a hypothesis based on oxidative phosphorylation. Zygote 13, 317–23.Google Scholar
Wildt, L., Kissler, S., Licht, P. & Becker, W. (1998). Sperm transport in the human female genital tract and its modulation by oxytocin as assessed by hysterosalpingoscintigraphy, hysterosonography, electrohysterography and Doppler sonography. Hum. Reprod. Update 4, 655–66.CrossRefGoogle Scholar
Williams, M., Hill, C.J., Scudamore, I., Dunphy, B., Cooke, I.D. & Barratt, C.L. (1993). Sperm numbers and distribution within the human fallopian tube around ovulation. Hum. Reprod. 8, 2019–26.Google Scholar
Wong, J.L. & Wessel, G.M. (2006). Defending the zygote, search for the ancestral animal block to polyspermy. Curr. Top. Dev. Biol. 72, 1–151.Google Scholar
Yanagimachi, R. (2005). Intracytoplasmic injection of spermatozoa and spermatogenic cells, its biology and applications in humans and animals. Reprod. Biomed. Online 10, 247–88.CrossRefGoogle Scholar
Yaniv, S., Elad, D., Jaffa, A.J. & Eytan, O. (2003). Biofluid aspects of embryo transfer. Ann. Biomed. Eng. 31, 1255–62.Google Scholar
Yu, Y., Oko, R. & Miranda-Vizuete, A. (2002). Developmental expression of spermatid-specific thioredoxin-1 protein, transient association to the longitudinal columns of the fibrous sheath during sperm tail formation. Biol. Reprod. 67, 1546–54.Google Scholar