Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Temperature gradients in vivo influence maturing male and female gametes in mammals: evidence from the cow

R. H. F. Hunter A B , F. López-Gatius C D F and O. López-Albors E
+ Author Affiliations
- Author Affiliations

A Sidney Sussex College, University of Cambridge, England.

B Ladfield, Oxnam, Jedburgh TD8 6RJ, Scotland.

C Agrotecnio Center, ETSEA, University of Lleida, 25198 Lleida, Spain.

D Transfer in Bovine Reproduction SLu, 22300 Barbastro, Spain.

E Department of Anatomy and Comparative Pathology, Veterinary Faculty, University of Murcia, Campus Universitario, 7, 30100 Murcia, Spain.

F Corresponding author. Email: lopezgatiusf@gmail.com

Reproduction, Fertility and Development - https://doi.org/10.1071/RD17089
Submitted: 8 March 2017  Accepted: 25 May 2017   Published online: 9 June 2017

Abstract

Since 1980 several reports have indicated that temperatures vary between preovulatory follicles and other ovarian tissues in rabbit, cow, pig and human. However, these observations did not achieve prominence; they were regarded as artefacts due to the use of anaesthetics and open surgery (laparotomy). Recently, without resorting to anaesthesia or surgery, direct measurements of temperature in preovulatory follicles have been performed in the cow by means of a thermistor probe introduced into the antrum under ultrasonic guidance. Such follicles revealed a mean antral (follicular fluid) temperature 0.74°C and 1.54°C cooler than uterine surface and rectal temperatures respectively in ovulating cows, whereas no such temperature differences were detected in non-ovulating cows. Cows are predominantly monovular and preovulatory follicles attain a diameter of 15–22 mm or more. These features and the timescale of response to the preovulatory gonadotrophin surge make them a valuable model for the human preovulatory follicle. Temperature gradients are interpreted primarily in a context of final maturation of gametes immediately before the onset of fertilisation. Preovulatory follicular temperature in women could be assessed by a comparable approach and might become a valuable selection guide for oocyte viability.

Additional keywords: fertilisation, Graafian follicle, ovary, ovulation.


References

Acosta, T. J. (2007). Studies of follicular vascularity associated with follicle selection and ovulation in cattle. J. Reprod. Dev. 53, 39–44.
Studies of follicular vascularity associated with follicle selection and ovulation in cattle.CrossRef | open url image1

Acosta, T. J., Gastal, E. L., Gastal, M. O., Beg, M. A., and Ginther, O. J. (2004). Differential blood flow changes between the future dominant and subordinate follicles precede diameter changes during follicle selection in mares. Biol. Reprod. 71, 502–507.
Differential blood flow changes between the future dominant and subordinate follicles precede diameter changes during follicle selection in mares.CrossRef | 1:CAS:528:DC%2BD2cXmtFWgtbo%3D&md5=56e0a68b5d4ded2f178edc337fdf188cCAS | open url image1

Bahat, A., and Eisenbach, M. (2006). Sperm thermotaxis. Mol. Cell. Endocrinol. 252, 115–119.
Sperm thermotaxis.CrossRef | 1:CAS:528:DC%2BD28XmtlajsLw%3D&md5=d13d930477843e483a81b80270b84327CAS | open url image1

Baker, R. D., and Polge, C. (1973). Sperm penetration of pig eggs in utero. J. Reprod. Fertil. 33, 347–350.
Sperm penetration of pig eggs in utero.CrossRef | 1:STN:280:DyaE3s7osFersQ%3D%3D&md5=aacbd133071260377c170860bf001968CAS | open url image1

Bedford, J. M. (1978). Anatomical evidence for the epididymis as the prime mover in the evolution of the scrotum. Am. J. Anat. 152, 483–507.
Anatomical evidence for the epididymis as the prime mover in the evolution of the scrotum.CrossRef | 1:STN:280:DyaE1c3jt1Ggug%3D%3D&md5=bbcf9b9e61b92cd93cd294aaca13fcc9CAS | open url image1

Berisha, B., Schams, D., Kosmann, M., Amselgruber, W., and Einspanier, R. (2000). Expression and localisation of vascular endothelial growth factor and basic fibroblast growth factor during the final growth of bovine ovarian follicles. J. Endocrinol. 167, 371–382.
Expression and localisation of vascular endothelial growth factor and basic fibroblast growth factor during the final growth of bovine ovarian follicles.CrossRef | 1:CAS:528:DC%2BD3MXjtVCqtg%3D%3D&md5=c4c3e8799eb54754bc32c7ba4dc15714CAS | open url image1

Chang, M. C. (1955). ‘La Fonction Tubaire et Ses Troubles’. pp. 40–52. (Masson & Cie: Paris.) [In French]

Coy, P., and Romar, R. (2002). In vitro production of pig embryos: a point of view. Reprod. Fertil. Dev. 14, 275–286.
In vitro production of pig embryos: a point of view.CrossRef | open url image1

Coy, P., Canovas, S., Mondejar, I., Saavedra, M. D., Romar, R., Grullón, L., Matas, C., and Aviles, M. (2008). Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilisation and contribute to the control of polyspermy. Proc. Natl. Acad. Sci. USA 105, 15809–15814.
Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilisation and contribute to the control of polyspermy.CrossRef | 1:CAS:528:DC%2BD1cXht1yitrjL&md5=9135ab8e9bef20d97b3ab660cc6d4dc0CAS | open url image1

David, A., Vilensky, A., and Nathan, H. (1972). Temperature changes in the different parts of the rabbit’s oviduct. Int. J. Gynaecol. Obstet. 10, 52–56.
Temperature changes in the different parts of the rabbit’s oviduct.CrossRef | open url image1

Eisenbach, M., and Giojalas, L. C. (2006). Sperm guidance in mammals: an unpaved road to the egg. Nat. Rev. Mol. Cell Biol. 7, 276–285.
Sperm guidance in mammals: an unpaved road to the egg.CrossRef | 1:CAS:528:DC%2BD28Xjt12qsLY%3D&md5=d8daeb67c386f52e186bb6bb09cfb847CAS | open url image1

Espey, L. L. (1967). Ultrastructure of the apex of the rabbit Graafian follicle during the ovulatory process. Endocrinology 81, 267–276.
Ultrastructure of the apex of the rabbit Graafian follicle during the ovulatory process.CrossRef | 1:STN:280:DyaK3c7is1Knsg%3D%3D&md5=8781c639f4a5b5d1a9afe5f2d9c2778cCAS | open url image1

Gillet, J. Y., Maillet, R., and Gautier, C. (1980). Blood and lymph supply of the ovary. In ‘Biology of the Ovary’. (Eds P. M. Motta and E. S. E. Hafez.) pp. 86–98. (Martinus Nijhoff Publishers: The Hague.)

Ginther, O. J., Rakesh, H. B., and Hoffman, M. M. (2014). Blood flow to follicles and CL during development of the periovulatory follicular wave in heifers. Theriogenology 82, 304–311.
Blood flow to follicles and CL during development of the periovulatory follicular wave in heifers.CrossRef | 1:STN:280:DC%2BC2cjjsFGmsA%3D%3D&md5=1d2637fd469e50715e400af77b5281b6CAS | open url image1

Glover, T. D., and Nicander, L. (1971). Some aspects of structure and function in the mammalian epididymis. J. Reprod. Fertil. Suppl. 13, 39–50. open url image1

Greve, T., Grøndahl, C., Schmidt, M., Hunter, R. H. F., and Avery, B. (1996). Bovine preovulatory follicular temperature: implications for in vitro production of embryos. Archiv. Tierzucht. Dummerstorf 39, 7–14. open url image1

Grinsted, J., Glendstrup, K., Andreasen, M. P., and Byskov, A. G. (1980). Temperature measurements of rabbit antral follicles. J. Reprod. Fertil. 60, 149–155.
Temperature measurements of rabbit antral follicles.CrossRef | 1:STN:280:DyaL3M%2FkvFamsA%3D%3D&md5=b34c2eb638b4c2e49a792b976fca11f2CAS | open url image1

Grinsted, J., Kjer, J. J., Blendstrup, K., and Pedersen, J. F. (1985). Is low temperature of the follicular fluid prior to ovulation necessary for normal oocyte development? Fertil. Steril. 43, 34–39.
Is low temperature of the follicular fluid prior to ovulation necessary for normal oocyte development?CrossRef | 1:STN:280:DyaL2M%2FnslSnsw%3D%3D&md5=478123ded8856e0c4f15f571b559e4c9CAS | open url image1

Hunter, R. H. F. (1968). Attempted fertilization of hamster eggs following transplantation into the uterus. J. Exp. Zool. 168, 511–516.
Attempted fertilization of hamster eggs following transplantation into the uterus.CrossRef | 1:STN:280:DyaF1M%2FltVGhsw%3D%3D&md5=68ef2c6b8263330293a40c909cb732a9CAS | open url image1

Hunter, R. H. F. (1990). Fertilisation of pig eggs in vivo and in vitro. J. Reprod. Fertil. Suppl. 40, 211–226.
| 1:STN:280:DyaK3c3osF2gtw%3D%3D&md5=9b01927c9e700a581f766520dc944092CAS | open url image1

Hunter, R. H. F. (1997). Sperm dynamics in the female genital tract: interactions with Fallopian tube microenvironments. In ‘Microscopy of Reproduction and Development: a Dynamic Approach’. (Ed. P. M. Motta.) pp. 35–45. (Antonio Delfino Editore: Rome.)

Hunter, R. H. F. (2002). Tubal ectopic pregnancy: a patho-physiological explanation involving endometriosis. Hum. Reprod. 17, 1688–1691.
Tubal ectopic pregnancy: a patho-physiological explanation involving endometriosis.CrossRef | 1:STN:280:DC%2BD38zltVKjsw%3D%3D&md5=784832384c1640f6e2e68c86c4875733CAS | open url image1

Hunter, R. H. F. (2003). ‘Physiology of the Graafian Follicle and Ovulation’. (Cambridge University Press: Cambridge.)

Hunter, R. H. F. (2009). Temperature gradients in female reproductive tissues and their potential significance. Anim. Reprod. 6, 7–15. open url image1

Hunter, R. H. F. (2012). Temperature gradients in female reproductive tissues. Reprod. Biomed. Online 24, 377–380.
Temperature gradients in female reproductive tissues.CrossRef | 1:STN:280:DC%2BC38vksVOgsA%3D%3D&md5=338161965e9339f4be2316a476c5bc90CAS | open url image1

Hunter, R. H. F., and Nichol, R. (1986). A preovulatory temperature gradient between the isthmus and ampulla of pig oviducts during the phase of sperm storage. J. Reprod. Fertil. 77, 599–606.
A preovulatory temperature gradient between the isthmus and ampulla of pig oviducts during the phase of sperm storage.CrossRef | 1:STN:280:DyaL283otFCisg%3D%3D&md5=ff0dd4f25fb1ae80a7bd12cdf13f3247CAS | open url image1

Hunter, R. H. F., Grondahl, C., Greve, T., and Schmidt, M. (1997). Graafian follicles are cooler than neighbouring ovarian tissues and deep rectal temperatures. Hum. Reprod. 12, 95–100.
Graafian follicles are cooler than neighbouring ovarian tissues and deep rectal temperatures.CrossRef | 1:STN:280:DyaK2s7ps1yhsA%3D%3D&md5=6292e87a3ed654a28101ebcb72706c12CAS | open url image1

Hunter, R. H. F., Bogh, I. B., Einer-Jensen, N., Müller, S., and Greve, T. (2000). Preovulatory Graafian follicles are cooler than neighbouring stroma in pig ovaries. Hum. Reprod. 15, 273–283.
Preovulatory Graafian follicles are cooler than neighbouring stroma in pig ovaries.CrossRef | 1:STN:280:DC%2BD3c7it1eksQ%3D%3D&md5=4e3b9e3cbc48c6a252cd8dc687951566CAS | open url image1

Hunter, R. H. F., Einer-Jensen, N., and Greve, T. (2006). Presence and significance of temperature gradients among different ovarian tissues. Microsc. Res. Tech. 69, 501–507.
Presence and significance of temperature gradients among different ovarian tissues.CrossRef | open url image1

Kanzaki, H., Okamura, H., Okuda, Y., Takenaka, A., Morimoto, K., and Nishimura, T. (1982). Scanning electron microscopic study of rabbit follicle microvasculature using resin injection-corrosion casts. J. Anat. 134, 697–704.
| 1:STN:280:DyaL3s%2FjtVGhsg%3D%3D&md5=d725d7d54c2f6650c333d94f358757b3CAS | open url image1

López-Béjar, M. A., López-Gatius, F., Camón, J., Rutllant, J., Valls, X., Labèrnia, J., and Santolaria, P. (1998). Morphological features and effects on reproductive parameters of ovarian cysts of follicular origin in superovulated rabbit does. Reprod. Domest. Anim. 33, 369–378.
Morphological features and effects on reproductive parameters of ovarian cysts of follicular origin in superovulated rabbit does.CrossRef | open url image1

López-Gatius, F., and Hunter, R. H. F. (2011). Intrafollicular insemination for the treatment of infertility in the dairy cow. Theriogenology 75, 1695–1698.
Intrafollicular insemination for the treatment of infertility in the dairy cow.CrossRef | open url image1

López-Gatius, F., and Hunter, R. H. F. (2017). Clinical relevance of preovulatory follicular temperature in heat-stressed lactating dairy cows. Reprod. Domest. Anim. 52, 366–370.
Clinical relevance of preovulatory follicular temperature in heat-stressed lactating dairy cows.CrossRef | open url image1

López-Gatius, F., López-Béjar, M., Fenech, M., and Hunter, R. H. F. (2005). Ovulation failure and double ovulation in dairy cattle: risk factors and effects. Theriogenology 63, 1298–1307.
Ovulation failure and double ovulation in dairy cattle: risk factors and effects.CrossRef | open url image1

Lucena, E., Ruiz, J. A., Mendoza, J. C., Lucena, A., Lucena, C., and Arango, A. (1991). Direct intrafollicular insemination: a case report. J. Reprod. Med. 36, 525–526.
| 1:STN:280:DyaK38%2FksFOhsA%3D%3D&md5=03b9f959921deeb23b26e63f1834a95dCAS | open url image1

Luck, M. R., and Gregson, K. (2000). Mathematical modelling of potential endothermic reactions in cool follicles. J. Reprod. Fertil. Abstr. Ser. 26, 14. open url image1

Luck, M. R., and Griffiths, S. D. (1998). Endothermic response of follicular fluid to aqueous dilution. J. Reprod. Fertil. Abstr. Ser. 22, 12–13. open url image1

Luck, M. R., Nutley, M., and Cooper, A. (1999). Microcalorimetric detection of the endothermic response of follicular fluid to aqueous dilution. J. Reprod. Fertil. Abstr. Ser. 24, 15. open url image1

Luck, M. R., Griffiths, S., Gregson, K., Watson, E., Nutley, M., and Cooper, A. (2001). Follicular fluid responds endothermically to aqueous dilution. Hum. Reprod. 16, 2508–2514.
Follicular fluid responds endothermically to aqueous dilution.CrossRef | 1:CAS:528:DC%2BD38XksleksQ%3D%3D&md5=ddf56ea9d50c8cc42eed20ad0ce7cdf2CAS | open url image1

Mattioli, M., Bacci, M. L., Galeati, G., and Seren, E. (1989). Developmental competence of pig oocytes matured and fertilized in vitro. Theriogenology 31, 1201–1207.
Developmental competence of pig oocytes matured and fertilized in vitro.CrossRef | 1:STN:280:DC%2BD283pvFCjsA%3D%3D&md5=a2b69b6a41316ad298fe31310580d7efCAS | open url image1

Mattioli, M., Barboni, B., Turriani, M., Galeati, G., Zannoni, A., Castellani, G., Berardinelli, P., and Scapolo, P. A. (2001). Follicle activation involves vascular endothelial growth factor production and increased blood vessel extension. Biol. Reprod. 65, 1014–1019.
Follicle activation involves vascular endothelial growth factor production and increased blood vessel extension.CrossRef | 1:CAS:528:DC%2BD3MXnt1Cmsr4%3D&md5=2bbe7364e68435a1c2ed917d8d8c92f7CAS | open url image1

Miyamoto, A., Shirasuna, K., Hayashi, K. G., Kamada, D., Awashima, C., Kaneko, E., Acosta, T. J., and Matsui, M. (2006). A potential use of color ultrasound as a tool for reproductive management: new observations using color ultrasound scanning that were not possible with imaging only in black and white. J. Reprod. Dev. 52, 153–160.
A potential use of color ultrasound as a tool for reproductive management: new observations using color ultrasound scanning that were not possible with imaging only in black and white.CrossRef | open url image1

Motta, P. M., and Makabe, S. (2003). ‘An Atlas of Menopausal Aging’. pp. 18–21. (The Parthenon Publishing Group: Boca Raton, USA.)

Pancarcı, S. M., Gungor, O., Atakisi, O., Cigremis, Y., Ari, U. C., and Bollwein, H. (2011). Changes in follicular blood flow and nitric oxide levels in follicular fluid during follicular deviation in cows. Anim. Reprod. Sci. 123, 149–156.
Changes in follicular blood flow and nitric oxide levels in follicular fluid during follicular deviation in cows.CrossRef | open url image1

Zbella, E. A., Tarantino, S., and Wade, R. (1992). Intrafollicular insemination for male factor infertility. Fertil. Steril. 58, 442–443.
Intrafollicular insemination for male factor infertility.CrossRef | 1:STN:280:DyaK38zjvFKjug%3D%3D&md5=d3b9164a2fc05a996b6aa8d945805c48CAS | open url image1

Zeleznik, A. J., Schuler, H. M., and Reichert, L. E. (1981). Gonadotropin-binding sites in the rhesus monkey ovary: role of the vasculature in the selective distribution of human chorionic gonadotropin to the preovulatory follicle. Endocrinology 109, 356–362.
Gonadotropin-binding sites in the rhesus monkey ovary: role of the vasculature in the selective distribution of human chorionic gonadotropin to the preovulatory follicle.CrossRef | 1:CAS:528:DyaL3MXkvFCkt7k%3D&md5=d841e5dc2da81544ed90fb86e4a7eabfCAS | open url image1

Zimmermann, R. C., Xiao, E., Husami, N., Sauer, M. V., Lobo, R., Kitajewski, J., and Ferin, M. (2001). Short-term administration of antivascular endothelial growth factor antibody in the late follicular phase delays follicular development in the rhesus monkey. J. Clin. Endocrinol. Metab. 86, 768–772.
| 1:CAS:528:DC%2BD3MXht1KntLo%3D&md5=ddcbd7872e80905f95845656003f4a1cCAS | open url image1

Zimmermann, R. C., Xiao, E., Bohlen, P., and Ferin, M. (2002). Administration of antivascular endothelial growth factor receptor 2 antibody in the early follicular phase delays follicular selection and development in the rhesus monkey. Endocrinology 143, 2496–2502.
Administration of antivascular endothelial growth factor receptor 2 antibody in the early follicular phase delays follicular selection and development in the rhesus monkey.CrossRef | 1:CAS:528:DC%2BD38XltVymsL0%3D&md5=fbed5581736b4d1153358702ba1711ddCAS | open url image1



Export Citation