Sampling the contents of the male reproductive tract: a tribute to Josef K. Voglmayr (1929 – 2019)

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Authors:

Andrzej Bartke, Terry T. Turner

Southern Illinois University School of Medicine

Consider This: 

Spermatozoa develop in the seminiferous tubules of the testis and mature during their passage through a very long duct folded into a seemingly compact organ, the epididymis. During the processes of development and maturation, spermatozoa remain in a milieu that is unique, regionally specific within the epididymis, and distinct from circulating blood, lymph, or interstitial fluid. While within the testis, sperm are effectively isolated by the blood-testis barrier, reminiscent of the better known blood-brain barrier. Consequently, mechanisms controlling sperm development and maturation are impossible to understand without characterizing their immediate liquid environment within the male reproductive tract. Unfortunately, both testicular and epididymal fluid are relatively inaccessible and amounts needed for detailed analysis are difficult to obtain from surgical specimens or autopsy material. In experimental studies, this difficulty can be partially circumvented by placing ligatures at various levels of the reproductive tracts and collecting fluid accumulated above (“upstream”) of the suture some time later, for example, on the next day. One of us used this approach to collect rat seminiferous tubules fluid after ligating the efferent ducts [1]. Collecting the fluid in this manner allowed for comparison of testicular testosterone levels in the lumen of the seminiferous tubules to the levels measured in peripheral blood and in testicular venous outflow in the same animal under various experimental conditions [2, 3]. However, this approach did not allow time course (longitudinal) studies or measurements in conscious animals.

 A real breakthrough in this area of study was provided in the 1960s by development of a surgical procedure for cannulation of the rete testis in the ram by Josef K. Voglmayr, working in Australia with Drs. Setchell and Waites [4, 5]. This procedure allowed continued collection of rete testis fluid (fluid flowing into this region of the testis from the seminiferous tubules) in conscious, lightly restrained animals. Multiple studies followed that would have been impossible without the cannulation procedure, including studies of sperm metabolism, changes of ram sperm plasma membrane during maturation, and responses to heating the testis [5-9]. In these studies, the cannulation procedure was adapted for the bull rete testis [10] and the epididymis.

Other methodological developments allowed pioneering studies in smaller animals which facilitated further insights into epididymal function and sperm maturation. Encouraged by the successes of Drs. Voglmayr, Setchell, and colleagues in collecting fluids from single sites, and Levine and Marsh [11] in collecting seminiferous and epididymal fluid by micropuncture, Howards and Turner [12, 13] developed further procedures for collecting intraluminal fluids by in vivo micropuncture. Other labs developed similar techniques [14, 15], supporting a variety of works characterizing the microenvironment of the developing sperm and investigating the physiological processes that support it.  All of these later studies were built upon the preceding works of Drs. Voglmayr, Setchell, and colleagues who were early in realizing the importance of understanding the physiology and cell biology of the male tract tubules. 

Dr. Voglmayr made significant contributions in important works ranging from the early physiological demonstration of the blood-testis barrier [7] to detailing the sperm membrane transitions during epididymal transit [9] to elucidating the role of inhibin in testicular regulation [16]. His work has stood the test of time and reflects well on himself and the field of reproductive biology. Innovations like his ultimately led, step by step, to clinical advances like Testicular Sperm Extraction (TESE) and Micorsurgical Epididymal Sperm Aspiration (MESA), among others. Moreover, measurements of androgen levels in fluids collected from different compartments of the male reproductive tract provided conceptual basis for the ongoing efforts to develop hormonal contraception for men [17].

References: 

1.         Harris, M.E. and A. Bartke, Concentration of testosterone in testis fluid of the rat. Endocrinology, 1974. 95(3): p. 701-6.

2.         Harris, M.E. and A. Bartke, Maintenance of rate testis fluid testosterone and dihydrotestosterone levels by pregnenolone and other C21 steroids in hypophysectomized rats. Endocrinology, 1975. 96(6): p. 1396-402.

3.         Harris, M.E., et al., Effects of testosterone and dihydrotestosterone on spermatogenesis, rete testis fluid, and peripheral androgen levels in hypophysectomized rats. Fertil Steril, 1977. 28(10): p. 1113-7.

4.         Voglmayr, J.K., G.M. Waites, and B.P. Setchell, Studies on spermatozoa and fluid collected directly from the testis of the conscious ram. Nature, 1966. 210(5038): p. 861-3.

5.         Voglmayr, J.K., et al., Metabolism of testicular spermatozoa and characteristics of testicular fluid collected from conscious rams. J Reprod Fertil, 1967. 14(1): p. 87-99.

6.         Setchell, B.P., et al., Amino acids in ram testicular fluid and semen and their metabolism by spermatozoa. Biochem J, 1967. 105(3): p. 1061-5.

7.         Setchell, B.P., J.K. Voglmayr, and G.M. Waites, A blood-testis barrier restricting passage from blood into rete testis fluid but not into lymph. J Physiol, 1969. 200(1): p. 73-85.

8.         Voglmayr, J.K., et al., The effect of heating the testis on the metabolism of testicular spermatozoa and on the rete testis fluid. J Reprod Fertil, 1970. 21(2): p. 365-6.

9.         Voglmayr, J.K., R.F. Sawyer, Jr., and J.L. Dacheux, Glycoproteins: a variable factor in surface transformation of ram spermatozoa during epididymal transit. Biol Reprod, 1985. 33(1): p. 165-76.

10.       Voglmayr, J.K., et al., A modified technique for cannulating the rete testis of the bull. J Reprod Fertil, 1972. 31(2): p. 291-4.

11.       Levine, N. and D.J. Marsh, Micropuncture studies of the electrochemical aspects of fluid and electrolyte transport in individual seminiferous tubules, the epididymis and the vas deferens in rats. J Physiol, 1971. 213(3): p. 557-70.

12.       Howards, S.S., A. Johnson, and S. Jessee, Micropuncture and microanalytic studies of the rat testis and epididymis. Fertil Steril, 1975. 26(1): p. 13-9.

13.       Turner, T.T., P.K. Hartmann, and S.S. Howards, In vivo sodium, potassium, and sperm concentrations in the rat epididymis. Fertil Steril, 1977. 28(2): p. 191-4.

14.       Hinton, B.T., A.M. Snoswell, and B.P. Setchell, The concentration of carnitine in the luminal fluid of the testis and epididymis of the rat and some other mammals. J Reprod Fertil, 1979. 56(1): p. 105-11.

15.       Djakiew, D. and R.C. Jones, Sperm maturation, fluid transport, and secretion and absorption of protein in the epididymis of the echidna, Tachyglossus aculeatus. J Reprod Fertil, 1983. 68(2): p. 445-56.

16.       Sanford, L.M., et al., Sexual maturational changes circulatory inhibin concentration in relation to FSH concentration and testicular size in Suffolk and DLS rams. Theriogenology, 2000. 54(5): p. 719-30.

17.       Anawalt, B.D., et al., Combined nestorone-testosterone gel suppresses serum gonadotropins to concentrations associated with effective hormonal contraception in men. Andrology, 2019.

Fertility and Sterility

Editorial Office, American Society for Reproductive Medicine

Fertility and Sterility® is an international journal for obstetricians, gynecologists, reproductive endocrinologists, urologists, basic scientists and others who treat and investigate problems of infertility and human reproductive disorders. The journal publishes juried original scientific articles in clinical and laboratory research relevant to reproductive endocrinology, urology, andrology, physiology, immunology, genetics, contraception, and menopause. Fertility and Sterility® encourages and supports meaningful basic and clinical research, and facilitates and promotes excellence in professional education, in the field of reproductive medicine.

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