Pelletier, R.‐M. and Byers, S. (1992). The blood–testis barrier and Sertoli cell junctions: structural considerations. Microsc. Res. Tech. 20: 3–33.44 44 Meng, J., Holdcraft, R., Shima, J. et al. (2005). Androgens regulate the permeability of the blood–testis barrier. PNAS 102: 16696–16700.
45 45 Madara, J. (1998). Regulation of the movement of solutes across tight junctions. Annu. Rev. Physiol. 60: 143–159.
46 46 Setchell, B. (1980). The functional significance of the blood–testis barrier. J. Androl. 1: 3–10.
47 47 Dejucq, N., Chousterman, S., and Jégou, B. (1997). The testicular antiviral defense system: localization, expression, and regulation of 2′ 5′ oligoadenylate synthetase, double‐stranded RNA‐activated protein kinase, and Mx proteins in the rat seminiferous tubule. J. Cell Biol. 139: 865–873.
48 48 Beach, S. and Vogl, A. (1999). Spermatid translocation in the rat seminiferous epithelium: coupling membrane trafficking machinery to a junction plaque. Biol. Reprod. 60: 1036–1046.
49 49 O'Donnell, L., Nicholls, P., O'Bryan, M. et al. (2011). Spermiation: the process of sperm release. Spermatogenesis 1: 14–35.
50 50 Carr, I., Clegg, E., and Meek, G. (1968). Sertoli cells as phagocytes: an electron microscopic study. J. Anat. 102: 501–509.
51 51 Clermont, Y., Morales, C., and Hermo, L. (1987). Endocytic activities of Sertoli cells in the rat. Ann. N. Y. Acad. Sci. 513: 1–15.
52 52 Monsees, T., Schill, W., and Miska, W. (1997). Protease–Protease Inhibitor Interactions in Sertoli Cell–Germ Cell Crosstalk. The Fate of the Male Germ Cell. Boston, MA: Springer.
53 53 Tsuruta, J., O'Brien, D., and Griswold, M. (1993). Sertoli cell and germ cell cystatin C: stage‐dependent expression of two distinct messenger ribonucleic acid transcripts in rat testes. Biol. Reprod. 49: 1045–1054.
54 54 Jutte, N., Jansen, R., Grootegoed, J. et al. (1983). FSH stimulation of the production of pyruvate and lactate by rat Sertoli cells may be involved in hormonal regulation of spermatogenesis. J. Reprod. Fertil. 68: 219–226.
55 55 Jutte, N., Jansen, R., Grootegoed, J. et al. (1982). Regulation of survival of rat pachytene spermatocytes by lactate supply from Sertoli cells. J. Reprod. Fertil. 65: 431–438.
56 56 Ritzen, E., Boitani, C., Parvinen, M. et al. (1982). Stage‐dependent secretion of ABP by rat seminiferous tubules. Mol. Cell. Endocrinol. 25: 25–33.
57 57 Gilmont, R., Senger, P., Sylvester, S. et al. (1990). Seminal transferrin and spermatogenic capability in the bull. Biol. Reprod. 43: 151–157.
58 58 Rivarola, M., Sanchez, P., and Saez, J. (1985). Stimulation of ribonucleic acid and deoxyribonucleic acid synthesis in spermatogenic cells by their coculture with Sertoli cells. Endocrinology 117: 1796–1802.
59 59 Rato, L., Meneses, M., Silva, B. et al. (2016). New insights on hormones and factors that modulate Sertoli cell metabolism. Histol. Histopathol. 31: 499–513.
60 60 Berndtson, W., Igboeli, G., and Parker, W. (1987). The numbers of Sertoli cells in mature Holstein bulls and their relationship to quantitative aspects of spermatogenesis. Biol. Reprod. 37: 60–67.
61 61 Berndtson, W., Igboeli, G., and Pickett, B. (1987). Relationship of absolute numbers of Sertoli cells to testicular size and spermatogenesis in young beef bulls. J. Anim. Sci. 64: 241–246.
62 62 Berndtson, W. and Igboeli, G. (1989). Numbers of Sertoli cells, quantitative rates of sperm production, and the efficiency of spermatogenesis in relation to the daily sperm output and seminal quality of young beef bulls. Am. J. Vet. Res. 50: 1193–1197.
63 63 Hochereau‐de Reviers, M., Monet‐Kuntz, C., and Courot, M. (1987). Spermatogenesis and Sertoli cell numbers and function in rams and bulls. J. Reprod. Fertil. Suppl. 34: 101–114.
64 64 Johnson, L. and Tatum, M. (1989). Temporal appearance of seasonal changes in numbers of Sertoli cells, Leydig cells, and germ cells in stallions. Biol. Reprod. 40: 994–999.
4 Thermoregulation of the Testes
John P. Kastelic and Guilherme Rizzoto
Department of Production Animal Health, Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada
Introduction
Since one bull may be responsible for breeding twenty (by natural service in one breeding season) to thousands (artificial insemination) of females, bull fertility is critically important. Although sterile bulls (total inability to reproduce) are uncommon, there can be a wide range in bull fertility, particularly in the absence of selection for fertility [1]. It is well established that a bull's testes must be 2–6 °C cooler than core body temperature for fertile sperm to be produced; consequently, increased testicular temperature, regardless of cause, reduces semen quality [2]. Although the underlying cause of infertility in bulls is frequently unknown, we speculate that it is often increased testicular temperature.
Anatomy and Physiology
Regulation of testicular temperature is dependent on several features. Scrotal skin is typically thin, with minimal hair and an extensive subcutaneous vasculature, facilitating heat loss by radiation [3]. The scrotal neck is the warmest part of the scrotum; a long distinct scrotal neck (and pendulous scrotum) reduces testicular temperature by increasing the area for radiation and enabling the testes to move away from the body. The tunica dartos, a thin sheet of smooth muscle under the scrotal skin, is controlled by sympathetic nerves and contracts and relaxes in cold and warm environments, respectively [4]. The cremaster muscle also contracts to draw the testes closer to the body under cold ambient conditions [4]. Dorsal to the testis is the testicular vascular cone [5], consisting of the highly coiled testicular artery surrounded by the pampiniform plexus, a complex venous network. The testicular vascular cone functions as a classic countercurrent heat exchanger, transferring heat from the artery to the vein, contributing to testicular cooling. Characteristics of scrotal surface temperatures and the testicular vascular cone in bulls aged 0.5–3 years were reported [6]. As bulls age, testicular vascular cone diameter increased; furthermore, increases in testicular vascular cone diameter and a shorter distance between arterial and venous blood in this structure were associated with increased percentage of normal sperm and fewer sperm with defects [7]. In a comparative study of semen quality and scrotal/testicular thermoregulation in Bos indicus, Bos taurus, and B. indicus/B. taurus crossbred bulls, there were significant differences among these genotypes in the vascular arrangement, characteristics of the testicular artery (e.g. wall thickness), and thickness of the tunica albuginea; overall, B. indicus bulls had the best thermoregulatory capacity whereas B. taurus bulls had the worst, with crossbred bulls intermediate [8].
Sweating and whole‐body responses also contribute to testicular cooling. In bulls, sweat gland density is highest in the scrotal skin [9]. In rams, apocrine sweat glands in the scrotum discharge simultaneously (up to 10 times per hour) when scrotal surface temperature is ~35.5 °C [10]. In these animals, respiration rate increases in association with scrotal surface temperature, reaching 200 breaths per minute when scrotal surface temperature is 38–40 °C [11].
Surface and Internal Temperatures
In beef bulls, average temperatures
