Introduction

The current success of assisted reproduction using testicular sperm extraction may give the impression that the human epididymis is not necessary for the development of the fertilising capacity of spermatozoa. However, as all assisted reproduction techniques bypass the epididymal processes refined over millions of years of evolution to permit internal fertilisation naturally (Jones, 2002), this argument is disingenuous (see Cooper, 1990). Certainly, the scarcity of intact human epididymides and the unavailability of biopsies (Schirren, 1982) has delayed research on this organ in comparison with that on the human testis, but organs from autopsies and accident victims and at operations for prostatic carcinoma, radical prostatectomy and organ transplantation have provided information. The human epididymis does not present clear-cut divisions into head (caput), body (corpus) and tail (cauda) as in other species (Fig. 4.1) and the structural complexity of the human epididymal caput (Yeung et al.,1991) and the uncertainty of which regions have been sampled in many studies leave the field less clear than it could be. Unlike the mouse, where the expression is confined to the proximal caput epididymidis (Sonnenberg-Riethmacher et al., 1996), the proto-oncogene c-ros is expressed along the length of the human epididymis (Legare and Sullivan, 2004). Nevertheless, the accumulated data obtained from these studies and reviewed here reveal a pattern of sperm maturation not unlike that found in other animals that have been studied more systematically.

This chapter updates the information relating to the changes that occur to spermatozoa during maturation in the human epididymis that add to our knowledge about the mechanisms by which the epididymis influences the maturing spermatozoa. The application of molecular biology techniques to the human epididymis has provided evidence of many novel proteins over the last 15 years. From this literature it is evident that spermatozoa are subjected to an ever-changing environment in the

Figure 4.1 Photographs of the human epididymis from (A) TG Cooper and CH Yeung, unpublished;

(B) Turner (1997) and (C) Bedford (1991), with kind permission of Springer Science and Business Media. Note the poor demarcation of caput, corpus and cauda, and the distended caput in (C)

Figure 4.1 Photographs of the human epididymis from (A) TG Cooper and CH Yeung, unpublished;

(B) Turner (1997) and (C) Bedford (1991), with kind permission of Springer Science and Business Media. Note the poor demarcation of caput, corpus and cauda, and the distended caput in (C)

epididymis and come sequentially into contact with proteins that have the potential to modify sperm-egg interactions. Recently, observations made on infertile transgenic mice have highlighted the importance of volume regulation in male fertility, a property acquired by spermatozoa within the primate epididymis. This work has suggested new functions for the high concentrations of low-molecular weight organic compounds found in epididymal fluid.

4.2 Sperm maturation in the human epididymis

4.2.1 Sperm transit

Estimates of the time taken for sperm to migrate through the human epididymis vary from a mean of 11 days (range 1-21) by thymidine labelling of spermatozoa (Rowley et al., 1970) to shorter values of 3-4 days (Amann and Howards, 1980; Johnson and Varner, 1988) from measurement of extragonadal sperm reserves. Faster transit (up to 2 days) was estimated for men with large daily sperm production (Johnson and Varner, 1988). Such rapid transit may be caused by the paucity of spermatozoa, as human epididymal fluid is not viscous (Turner and Reich, 1985). Interestingly, rapid transit is also the norm for the chimpanzee (Smithwick et al., 1996) in the very different situation of a large testis size and high sperm production rate.

(A)

0 Normal forms (%)

60 50403020-

10 0

60 50403020-

Motile (%)

(C)

-O- VSL (pm/s) / j

Figure 4.2 Maturation of spermatozoa in the human epididymis. Various functional parameters

(ordinate) are plotted for sperm obtained from different epididymal regions (abscissa): (A) normal forms (Soler et al., 2000); (B) sperm head morphometry (Soler et al., 2000); (C) motility and kinematics (Yeung et al., 1993); (D) sperm-zona binding (Delpech et al., 1988; Moore et al., 1992); (E) acrosome reactions (Yeung et al., 1997a);

S

0 Perimeter (pm) ^

-O" Area (pm2)

(D)

yr Sperm on zona (n)

s 0 Uncapacitated

-O- Capacitated

(H)

j/ Acridine orange

W (% mature)

-O- Aniline blue

(% negative)

(J) VF cycles (%) with pregnancies (P) or fertilisation (F) A

(J) VF cycles (%) with pregnancies (P) or fertilisation (F) A

12345678 12345678 Region of the epididymis

Figure 4.2 Maturation of spermatozoa in the human epididymis. Various functional parameters

(ordinate) are plotted for sperm obtained from different epididymal regions (abscissa): (A) normal forms (Soler et al., 2000); (B) sperm head morphometry (Soler et al., 2000); (C) motility and kinematics (Yeung et al., 1993); (D) sperm-zona binding (Delpech et al., 1988; Moore et al., 1992); (E) acrosome reactions (Yeung et al., 1997a);

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