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Sperm transport in the female reproductive tract
3 To whom correspondence should be addressed at: Department of Biomedical Sciences, T5-002B Veterinary Research Tower, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853, USA. E-mail: sss7@cornell.edu
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Human Reproduction Update , Volume 12, Issue 1, January/February 2006, Pages 23–37, https://doi.org/10.1093/humupd/dmi047
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© The Author 2005. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. for Permissions, please email: journals.permissions@oupjournals.org
© The Author 2005. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. for Permissions, please email: journals.permissions@oupjournals.org
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S.S. Suarez, A. A. Pacey, Sperm transport in the female reproductive tract, Human Reproduction Update , Volume 12, Issue 1, January/February 2006, Pages 23–37, https://doi.org/10.1093/humupd/dmi047
At coitus, human sperm are deposited into the anterior vagina, where, to avoid vaginal acid and immune responses, they quickly contact cervical mucus and enter the cervix. Cervical mucus filters out sperm with poor morphology and motility and as such only a minority of ejaculated sperm actually enter the cervix. In the uterus, muscular contractions may enhance passage of sperm through the uterine cavity. A few thousand sperm swim through the uterotubal junctions to reach the Fallopian tubes (uterine tubes, oviducts) where sperm are stored in a reservoir, or at least maintained in a fertile state, by interacting with endosalpingeal (oviductal) epithelium. As the time of ovulation approaches, sperm become capacitated and hyperactivated, which enables them to proceed towards the tubal ampulla. Sperm may be guided to the oocyte by a combination of thermotaxis and chemotaxis. Motility hyperactivation assists sperm in penetrating mucus in the tubes and the cumulus oophorus and zona pellucida of the oocyte, so that they may finally fuse with the oocyte plasma membrane. Knowledge of the biology of sperm transport can inspire improvements in artificial insemination, IVF, the diagnosis of infertility and the development of contraceptives.
Submitted on July 12, 2005; revised on September 26, 2005; accepted on October 4, 2005
Passage of sperm through the female reproductive tract is regulated to maximize the chance of fertilization and ensure that sperm with normal morphology and vigorous motility will be the ones to succeed.
Oocytes are usually fertilized within hours of ovulation ( Austin, 1957 ; Harper, 1994). On the other hand, in some species, sperm may be inseminated days (horses, cattle and pigs) or even months (some bat species) before the arrival of the oocyte. In humans, there is evidence that fertilization occurs when intercourse takes place up to five days before ovulation (Wilcox et al ., 1995). Because sperm are terminally differentiated cells, deprived of an active transcription and translation apparatus, they must survive in the female without benefit of reparative mechanisms available to many other cells. Sperm are subjected to physical stresses during ejaculation and contractions of the female tract, and they may sustain oxidative damage. Furthermore, because sperm are allogenic to the female, they may encounter the defenses of the female immune system meant for infectious organisms (Menge and Edwards, 1993). Thus, sperm must somehow use their limited resources to maintain their fertility in the face of numerous impediments. As it is, of the millions of sperm inseminated at coitus in humans, only a few thousand reach the Fallopian tubes and, ordinarily, only a single sperm fertilizes an oocyte.
The site of semen deposition is not easy to establish in many species because it must be determined by examining the female immediately after coitus and by considering the anatomy of the penis, vagina and cervix during coitus. However, it has been accomplished for humans, in which semen has been observed pooled in the anterior vagina near the cervical os shortly after coitus. Within minutes of vaginal deposition, human sperm begin to leave the seminal pool and swim into the cervical canal (Sobrero and MacLeod, 1962). In contrast, rodent sperm deposited in the vagina are swept completely through the cervix into the uterus along with seminal plasma within a few minutes (Zamboni, 1972; Bedford and Yanagimachi, 1992 ; Carballada and Esponda, 1997 ). Some species, such as pigs, bypass the vagina altogether and deposit semen directly into the uterine cavity, where sperm may quickly gain access to the oviduct (Hunter, 1981; Roberts, 1986).
Whereas most of the semen of murine rodents is rapidly transported into the uterine cavity, some remains in the vagina where it coagulates to form a copulatory plug. The plug forms a cervical cap that promotes sperm transport into the uterus ( Blandau, 1969 ; Matthews and Adler, 1978; Carballada and Esponda, 1992 ). Ligation of the vesicular and coagulating glands of rats prevented the formation of plugs and the transport of sperm into the uterus ( Blandau, 1945 ). The plugs formed by semen of guinea pigs and mice extend into the cervical canals and thus could form a seal against retrograde sperm loss ( Blandau, 1969 ).
Male mice deficient for the gene encoding the protease inhibitor known as protease nexin-1 (PN-1) show a marked impairment in fertility ( Murer et al ., 2001 ). Vaginal plugs formed in females after mating with PN-1 null males were small, soft and fibrous and did not lodge tightly in the dual cervical canals. No sperm could be found in the uterus 15 min after mating with PN-1 null males, demonstrating the importance of the plug for promoting transport of mouse sperm into the uterus ( Murer et al ., 2001 ).
Human semen coagulates, but it forms a loose gel rather than the compact fibrous plug seen in rodents. The coagulate forms within about a minute of coitus and then is enzymatically degraded in to 1 h (Lilja and Lundwall, 1992). The predominant structural proteins of the gel are the 50 kDa semenogelin I and the 63 kDa semenogelin II, as well as a glycosylated form of semenogelin II, all of which are secreted primarily by the seminal vesicles (Lilja, 1985). The gel is degraded by prostate-specific antigen (PSA), a serine protease secreted by the prostate gland ( Watt et al ., 1986 ). It has been proposed that this coagulum serves to hold the sperm at the cervical os (Harper, 1994) and that it protects sperm against the harsh environment of the vagina (Lundwall et al ., 2003).
Seminal gels are not fully successful at holding sperm at the cervical os. In cattle, several studies have demonstrated loss of sperm from the vagina after mating or insemination (reviewed by Hawk, 1987). The fate of spermatozoa that are ejaculated or inseminated into the vagina, but that do not enter the cervix, has not been studied extensively in humans. However, in a 5 year study of 11 female volunteers Baker and Bellis (1993) examined the characteristics of sperm loss from the vagina following coitus (‘flowback’). They found that flowback occurred in 94% of copulations with the median time to the emergence of ‘flowback’ of 30 min (range 5–120 min). Furthermore they estimated that a median of 35% of spermatozoa were lost through flowback but that in 12% of copulations almost 100% of the sperm inseminated were eliminated. This suggests that less than 1% of sperm might be retained in the female reproductive tract and this supports the notion that only a minority of sperm actually enter cervical mucus and ascend higher into the female reproductive tract.
Like humans, some primates produce semen that forms a soft gel. However, in chimpanzees, a species in which females mate with more than one male in a brief time, the semen coagulates into a compact plug resembling that of rodents (Jensen-Seaman and Li , 2 003; Kingan et al ., 2003). The plug may serve to prevent other males from mating with the female. Some carnivores (e.g. domestic dogs, Canis familiaris ) and some rat and mouse species of the family Cricetidae use the penis as a copulatory plug; i.e. the mating pair remains joined together for a period after coitus ( Dewsbury, 1975 ).
The vagina is open to the exterior and thus to infection, especially at the time of coitus; therefore, it is well equipped with antimicrobial defenses. These defenses include acidic pH and immunological responses and can damage sperm as well as infectious organisms. To enable fertilization to take place, both the female and the male have adopted mechanisms for protecting sperm. In humans, semen is deposited at the external os of the cervix so that sperm can quickly move out of the vagina (Sobrero and MacLeod, 1962).
Human sperm must contend, however briefly, with the acidic pH of vaginal fluid. The vaginal pH of women is normally five or lower, which is microbicidal for many sexually transmitted disease pathogens. Evidence indicates that the acidity is maintained through lactic acid production by anaerobic lactobacilli that feed on glycogen present in shed vaginal epithelial cells ( Boskey et al ., 2001 ). Lowering pH with lactic acid has been demonstrated to immobilize bull sperm ( Acott and Carr, 1984 ; Carr et al ., 1985 ). The pH of seminal plasma ranges from 6.7 to 7.4 in common domestic species (Roberts, 1986) and has the potential to neutralize vaginal acid. Vaginal pH was measured by radio-telemetry in a fertile human couple during coitus. The pH rose from 4.3 to 7.2 within 8 s of the arrival of semen; whereas, no change was detected when the partner used a condom (Fox et al ., 1973). Vaginal washings of women with high levels of detectable seminal antigens had a median pH of 6.1, whereas the median pH of washings lacking detectable antigens was 3.7 ( Bouvet et al ., 1997 ). Contraceptive gel designed to maintain a low vaginal pH after coitus has been shown to immobilize human sperm in vitro and in vivo ( Amaral et al ., 2004 ).
In additions to pH buffers, seminal plasma contains inhibitors of immune responses, including protective components that coat sperm (Suarez and Oliphant, 1982; Dostal et al ., 1997). These are most effective when sperm are bathing in seminal plasma and may be gradually shed when sperm leave the seminal plasma behind.
Males may also overcome female defenses by inseminating many sperm. This strategy is particularly effective for overcoming cellular immune responses. In the rabbit, deposition of semen results in an invasion of neutrophils into the vagina. This invasion takes time, however, to build to an effective level. Numerous leukocytes, many containing ingested sperm, were recovered from vaginas of rabbits 3–24 h post coitus (Phillips and Mahler, 1977a,b). By that time, however, thousands of sperm had already reached the Fallopian tubes (Overstreet et al ., 1978).
In some species, the cervical canal widens under the influence of estrogen. Fluoroscopy and scintigraphy have been used in domestic dogs and cats to examine cervical patency. Opening of the cervix in these species has been correlated with estrus (Silva et al ., 1995; Verstegen et al ., 2001; Chatdarong et al ., 2002 ). Radioopaque fluid and also human serum albumin radiolabelled with technetium 99 could be seen rapidly passing through the cervix and filling the uterine lumen after deposition in the cranial vagina at estrus.
Sperm of humans and cattle enter the cervical canal rapidly where they encounter cervical mucus (Figure 1 A). Under the influence of estrogen the cervix secretes highly hydrated mucus, often exceeding 96% water in women (Katz et al ., 1997). The extent of hydration is correlated with penetrability to sperm (Morales et al ., 1993). Coitus on the day of maximal mucus hydration in women is more closely correlated with incidence of pregnancy than coitus timed with respect to ovulation detected using basal body temperature ( Bigelow et al ., 2004 ).
Human female reproductive tract illustrating stages of gamete transport. ( A ) Sperm entering cervical mucus at external os of cervix. The mucus fills the upper half of the inset. ( B ) Sperm interacting with endosalpingeal epithelium in Fallopian tube. ( C ) Hyperactivated motility of sperm in Fallopian tube. ( D ) Oocyte in cumulus within a transverse section of the tubal ampulla. Artwork by C. Rose Gottlieb.
Cervical mucus presents a greater barrier to abnormal sperm that cannot swim properly or that present a poor hydrodynamic profile than it does to morphologically normal, vigorously motile sperm and is thus thought as one means of sperm selection (Hanson and Overstreet, 1981; Barros et al ., 1984 ; Katz et al ., 1990, 1997).
The greatest barrier to sperm penetration of cervical mucus is at its border, because here the mucus microarchitecture is more compact (Yudin et al ., 1989). Components of seminal plasma may assist sperm in penetrating the mucus border. More human sperm were found to enter cervical mucus in vitro when an inseminate was diluted 1:1 with whole seminal plasma than when it was diluted with Tyrode’s medium, even though the sperm swam faster in the medium (Overstreet et al ., 1980).
Like the vagina, the cervix can mount immune responses. In rabbits and humans, vaginal insemination stimulates the migration of leukocytes, particularly neutrophils and macrophages, into the cervix as well as into the vagina (Tyler, 1977; Pandya and Cohen, 1985). Neutrophils migrate readily through midcycle human cervical mucus (Parkhurst and Saltzman, 1994
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