Proteinaceous sperm motility inhibitory factor from the female Indian garden lizard Calotes versicolor
Goutham Shankar A E , Shubhashree Uppangala B , Satish K. Adiga B , Belinda Willard C , Bhadravathi K. C. Sagar D , Ruth S. K. Titus E and Gopal K. Marathe A F
+ Author Affiliations
- Author Affiliations
A Department of Studies in Biochemistry, University of Mysore, Manasagangotri, Mysuru 570006, Karnataka, India.
B Division of Clinical Embryology, Kasturba Medical College, Manipal University, Manipal 576104, Karnataka, India.
C Research Core Services, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, OH 44195, USA.
D Department of Neuropathology, National Institute of Mental Health and Neurosciences (Institute of National Importance), Bengaluru 560029, Karnataka, India.
E Department of Zoology, St. Philomena’s College, Bannimantap, Mysuru 570015, Karnataka, India.
F Corresponding author. Email: marathe1962@gmail.com
Reproduction, Fertility and Development 30(5) 744-751 https://doi.org/10.1071/RD17292
Submitted: 3 June 2017 Accepted: 28 September 2017 Published: 15 November 2017
Abstract
Female sperm storage is an intriguing adaptation exhibited by a wide array of both vertebrates and invertebrates. The mechanisms underlying female sperm storage have remained elusive. Using the Indian garden lizard Calotes versicolor as a model organism, we investigated the role of low and high molecular weight factors in this phenomenon. Previously, we demonstrated three distinct phases of the reproductive cycle in this animal with live, motile spermatozoa recovered from the uterovaginal region during the reproductive phase. In the present study, we analysed the uterovaginal contents using sodium dodecyl sulfate–polyacrylamide gel electrophoresis and identified an abundant protein band corresponding to ~55 kDa regardless of the phase of the reproductive cycle. Analysis of the purified protein by liquid chromatography–tandem mass spectrometry suggested a unique protein without any homology to the National Center for Biotechnology Information database. Exogenous addition of this protein to washed spermatozoa derived from the epididymis reversibly inhibited sperm motility in a concentration- and time-dependent manner, suggesting it plays a key role in sperm storage. These studies are likely to offer new avenues to unravel the secrets of female sperm storage seen across the animal taxa and may have novel applications not only in reproductive biology, but also in general cell storage and preserving endangered animal species.
Additional keywords: lactic acid, sperm storage tubule, uterovaginal flushing.
References
Abe, H., Sendai, Y., Satoh, T., and Hoshi, H. (1995). Bovine oviduct-specific glycoprotein: a potent factor for maintenance of viability and motility of bovine spermatozoa in vitro. Mol. Reprod. Dev. 42, 226–232.| Bovine oviduct-specific glycoprotein: a potent factor for maintenance of viability and motility of bovine spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXosVWqtr8%3D&md5=db4d5261a19d97626a4b76881ae962c7CAS |
Akbarsha, M. A., and Meeran, M. M. (1995). Occurrence of ampulla in the ductus deferens of the Indian garden lizard Calotes versicolor Daudin. J. Morphol. 225, 261–268.
| Occurrence of ampulla in the ductus deferens of the Indian garden lizard Calotes versicolor Daudin.Crossref | GoogleScholarGoogle Scholar |
Avila, F. W., Bloch-Qazi, M. C., Rubinstein, C. D., and Wolfner, M. F. (2012). A requirement for the neuromodulators octopamine and tyramine in Drosophila melanogaster female sperm storage. Proc. Natl Acad. Sci. USA 109, 4562–4567.
| A requirement for the neuromodulators octopamine and tyramine in Drosophila melanogaster female sperm storage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvF2mtL8%3D&md5=2c3ed1afae06f4155a4679029766ccebCAS |
Avila, F. W., Mattei, A. L., and Wolfner, M. F. (2015). Sex peptide receptor is required for the release of stored sperm by mated Drosophila melanogaster females. J. Insect Physiol. 76, 1–6.
| Sex peptide receptor is required for the release of stored sperm by mated Drosophila melanogaster females.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXksF2ntbg%3D&md5=7742801caa89c6b092c2b0c63e2689f8CAS |
Baer, B., Armitage, S. A., and Boomsma, J. J. (2006). Sperm storage induces an immunity cost in ants. Nature 441, 872–875.
| Sperm storage induces an immunity cost in ants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvVGlsbk%3D&md5=8dd69cf2192ffb89be186706043a6566CAS |
Bakst, M. R. (1985). Zinc reduces turkey sperm oxygen uptake in vitro. Poult. Sci. 64, 564–566.
| Zinc reduces turkey sperm oxygen uptake in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhs1Cjt78%3D&md5=114ad477d8880e3272addc09c3fe37b6CAS |
Bakst, M. R., and Richards, M. P. (1985). Concentrations of selected cations in turkey serum and oviductal mucosae. Poult. Sci. 64, 555–563.
| Concentrations of selected cations in turkey serum and oviductal mucosae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhs1CjsL0%3D&md5=d923e1cd735e7e2d0a10cb967dd75ddeCAS |
Bernasconi, G., Hellriegel, B., Heyland, A., and Ward, P. I. (2002). Sperm survival in the female reproductive tract in the fly Scathophaga stercoraria (L.). J. Insect Physiol. 48, 197–203.
| Sperm survival in the female reproductive tract in the fly Scathophaga stercoraria (L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsFagtLc%3D&md5=a5a5b15e0031b159827149f55fea4e92CAS |
Birkhead, T. R., and Moller, A. P. (1993). Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biol. J. Linn. Soc. Lond. 50, 295–311.
| Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals.Crossref | GoogleScholarGoogle Scholar |
Björndahl, L., Söderlund, I., and Kvist, U. (2003). Evaluation of the one-step eosin–nigrosin staining technique for human sperm vitality assessment. Hum. Reprod. 18, 813–816.
| Evaluation of the one-step eosin–nigrosin staining technique for human sperm vitality assessment.Crossref | GoogleScholarGoogle Scholar |
Collins, A. M., Williams, V., and Evans, J. D. (2004). Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera. Insect Mol. Biol. 13, 141–146.
| Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1GktLo%3D&md5=57df88fca3c1a746ebf13521933add66CAS |
Coy, P., Garcia-Vazquez, F. A., Visconti, P. E., and Aviles, M. (2012). Roles of the oviduct in mammalian fertilization. Reproduction 144, 649–660.
| Roles of the oviduct in mammalian fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVOitb%2FP&md5=65824a7cc0281d28c9e7043a5f946df7CAS |
Crichton, E. G., Krutzsch, P. H., and Chvapil, M. (1982). Studies on prolonged spermatozoa survival in chiroptera – II. The role of zinc in the spermatozoa storage phenomenon. Comp. Biochem. Physiol. 71, 71–77.
| Studies on prolonged spermatozoa survival in chiroptera – II. The role of zinc in the spermatozoa storage phenomenon.Crossref | GoogleScholarGoogle Scholar |
Das, S., Saha, S., Majumder, G. C., and Dungdung, S. R. (2010). Purification and characterization of a sperm motility inhibiting factor from caprine epididymal plasma. PLoS One 5, e12039.
| Purification and characterization of a sperm motility inhibiting factor from caprine epididymal plasma.Crossref | GoogleScholarGoogle Scholar |
den Boer, S. P., Boomsma, J. J., and Baer, B. (2009). Honey bee males and queens use glandular secretions to enhance sperm viability before and after storage. J. Insect Physiol. 55, 538–543.
| Honey bee males and queens use glandular secretions to enhance sperm viability before and after storage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsVektbw%3D&md5=d6d147ce683b82d1ef20f4b235186d6aCAS |
Figenschou, D. L., and Marais, J. P. (1991). Spectrophotometric method for the determination of microquantities of lactic acid in biological material. Anal. Biochem. 195, 308–312.
| Spectrophotometric method for the determination of microquantities of lactic acid in biological material.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXks1Oku7k%3D&md5=6334fff673555a01b9f4d3fa4a26f73fCAS |
Frasca, J. M., and Parks, V. R. (1965). A routine technique for double-staining ultrathin sections using uranyl and lead salts. J. Cell Biol. 25, 157–161.
| A routine technique for double-staining ultrathin sections using uranyl and lead salts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2M%2Fptl2nsw%3D%3D&md5=e8982c1339978afc57b8b7fd0e3e4ccbCAS |
Girons, H. S. (1982). Reproductive cycles of male snakes and their relationships with climate and female reproductive cycles. Herpetologica 38, 5–16.
Hiyama, G., Matsuzaki, M., Mizushima, S., Dohra, H., Ikegami, K., Yoshimura, T., Shiba, K., Inaba, K., and Sasanami, T. (2014). Sperm activation by heat shock protein 70 supports the migration of sperm released from sperm storage tubules in Japanese quail (Coturnix japonica). Reproduction 147, 167–178.
| Sperm activation by heat shock protein 70 supports the migration of sperm released from sperm storage tubules in Japanese quail (Coturnix japonica).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisFart7o%3D&md5=e041dc3083dd37acb68a17178eda93c2CAS |
Holm, L., Ekwall, H., Wishart, G. J., and Ridderstrale, Y. (2000). Localization of calcium and zinc in the sperm storage tubules of chicken, quail and turkey using X-ray microanalysis. J. Reprod. Fertil. 118, 331–336.
| 1:CAS:528:DC%2BD3cXitlCqurs%3D&md5=de0c69fd98356ec3ec1d2c3179baf3b9CAS |
Holt, W. V., and Fazeli, A. (2010). The oviduct as a complex mediator of mammalian sperm function and selection. Mol. Reprod. Dev. 77, 934–943.
| The oviduct as a complex mediator of mammalian sperm function and selection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVCktrnL&md5=a153db3359488c82e1122b285cf3772bCAS |
Holt, W. V., and Lloyd, R. E. (2010). Sperm storage in the vertebrate female reproductive tract: how does it work so well? Theriogenology 73, 713–722.
| Sperm storage in the vertebrate female reproductive tract: how does it work so well?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7ot1Wqsw%3D%3D&md5=990c2d98592b8875fcdbe9061f4a5f12CAS |
Iwamoto, T., Tsang, A., Luterman, M., Dickson, J., de Lamirande, E., Okuno, M., Mohri, H., and Gagnon, C. (1992). Purification and characterization of a sperm motility-dynein ATPase inhibitor from boar seminal plasma. Mol. Reprod. Dev. 31, 55–62.
| Purification and characterization of a sperm motility-dynein ATPase inhibitor from boar seminal plasma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xht1eksLo%3D&md5=3fdc0d27a474742088d5d63eee93a739CAS |
Jones, J. M., and Bavister, B. D. (2000). Acidification of intracellular pH in bovine spermatozoa suppresses motility and extends viable life. J. Androl. 21, 616–624.
| 1:STN:280:DC%2BD3M%2Fnsl2qtQ%3D%3D&md5=fbb763735245b9cb44ec0bdfd55badf3CAS |
Kareskoski, M., and Katila, T. (2008). Components of stallion seminal plasma and the effects of seminal plasma on sperm longevity. Anim. Reprod. Sci. 107, 249–256.
| Components of stallion seminal plasma and the effects of seminal plasma on sperm longevity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXoslWkt7Y%3D&md5=4b1b646df15c97e163c121cd979bb22eCAS |
Kawano, N., Araki, N., Yoshida, K., Hibino, T., Ohnami, N., Makino, M., Kanai, S., Hasuwa, H., Yoshida, M., Miyado, K., and Umezawa, A. (2014). Seminal vesicle protein SVS2 is required for sperm survival in the uterus. Proc. Natl Acad. Sci. USA 111, 4145–4150.
| Seminal vesicle protein SVS2 is required for sperm survival in the uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtlylt7Y%3D&md5=32000b55e90d8475a89decead12ba667CAS |
King, R. S., Anderson, S. H., and Killian, G. J. (1994). Effect of bovine oviductal estrus-associated protein on the ability of sperm to capacitate and fertilize oocytes. J. Androl. 15, 468–478.
| 1:CAS:528:DyaK2MXitFGhur4%3D&md5=2e047c75ffde5b5b2a7e7c38494ef692CAS |
King, M., Eubel, H., Millar, A. H., and Baer, B. (2011). Proteins within the seminal fluid are crucial to keep sperm viable in the honeybee Apis mellifera. J. Insect Physiol. 57, 409–414.
| Proteins within the seminal fluid are crucial to keep sperm viable in the honeybee Apis mellifera.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFKjtrk%3D&md5=47c5d466befd85b844cc0d3f1781f562CAS |
Kuehnel, S., and Kupfer, A. (2012). Sperm storage in the caecilian amphibians. Front. Zool. 9, 12.
| Sperm storage in the caecilian amphibians.Crossref | GoogleScholarGoogle Scholar |
Kumari, T. R. S., Sarkar, H. B. D., and Shivanandappa, T. (1990). Histology and histochemistry of the oviductal sperm storage pockets of the agamid lizard, Calotes versicolor. J. Morphol. 203, 97–106.
| Histology and histochemistry of the oviductal sperm storage pockets of the agamid lizard, Calotes versicolor.Crossref | GoogleScholarGoogle Scholar |
Lee, K. M., Daubnerová, I., Isaac, R. E., Zhang, C., Choi, S., Chung, J., and Kim, Y. J. (2015). A neuronal pathway that controls sperm ejection and storage in female Drosophila. Curr. Biol. 25, 790–797.
| A neuronal pathway that controls sperm ejection and storage in female Drosophila.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjt1amtrw%3D&md5=35454fb2098664b6ee5922e61a90ff10CAS |
Liu, T., Chu, X., Huang, Y., Yang, P., Li, Q., Hu, L., Chen, H., and Chen, Q. (2016). Androgen-related sperm storage in oviduct of Chinese soft-shelled turtle in vivo during annual cycle. Sci. Rep. 6, 20456.
| Androgen-related sperm storage in oviduct of Chinese soft-shelled turtle in vivo during annual cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xitlyht7w%3D&md5=df7bbb9e4af7f6c89e45b259e553c683CAS |
Maillo, V., Sánchez-Calabuig, M. J., Lopera-Vasquez, R., Hamdi, M., Gutierrez-Adan, A., Lonergan, P., and Rizos, D. (2016). Oviductal response to gametes and early embryos in mammals. Reproduction 152, R127–R141.
| Oviductal response to gametes and early embryos in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhslyrtLbL&md5=5b2fc1589ef0c4ba71c5e8fe5e5e24b8CAS |
Matsuzaki, M., Mizushima, S., Hiyama, G., Hirohashi, N., Shiba, K., Inaba, K., Suzuki, T., Dohra, H., Ohnishi, T., Sato, Y., Kohsaka, T., Ichikawa, Y., Atsumi, Y., Yoshimura, T., and Sasanami, T. (2015). Lactic acid is a sperm motility inactivation factor in the sperm storage tubules. Sci. Rep. 5, 17643.
| Lactic acid is a sperm motility inactivation factor in the sperm storage tubules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvFGntbnO&md5=b359ae2ff19d59bd0f5f946e296b126dCAS |
McNutt, T., Rogowski, L., Vasilatos-Younken, R., and Killian, G. (1992). Adsorption of oviductal fluid proteins by the bovine sperm membrane during in vitro capacitation. Mol. Reprod. Dev. 33, 313–323.
| Adsorption of oviductal fluid proteins by the bovine sperm membrane during in vitro capacitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslSksQ%3D%3D&md5=baf9a424e62afebbf2423604df454f93CAS |
Mohan, J., Saini, M., and Joshi, P. (1995). Isolation of a spermatozoa motility inhibiting factor from chicken seminal plasma with antibacterial property. Biochim. Biophys. Acta 1245, 407–413.
| Isolation of a spermatozoa motility inhibiting factor from chicken seminal plasma with antibacterial property.Crossref | GoogleScholarGoogle Scholar |
Novo, M., Fernández, R., Granado-Yela, C., López, M. G., and Cosín, D. J. D. (2013). Does the order of copulation matter? Experimental paternity analyses in the earthworm Hormogaster elisae (Annelida: Hormogastridae). Pedobiologia (Jena) 56, 97–104.
| Does the order of copulation matter? Experimental paternity analyses in the earthworm Hormogaster elisae (Annelida: Hormogastridae).Crossref | GoogleScholarGoogle Scholar |
Ribou, A. C., and Reinhardt, K. (2012). Reduced metabolic rate and oxygen radicals production in stored insect sperm. Proc. Biol. Sci. 279, 2196–2203.
| Reduced metabolic rate and oxygen radicals production in stored insect sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsFOgtL4%3D&md5=095d4d200958cf19f381f5aad72a46b2CAS |
Roy, V. K., and Krishna, A. (2011). Sperm storage in the female reproductive tract of Scotophilus heathii: role of androgen. Mol. Reprod. Dev. 78, 477–487.
| Sperm storage in the female reproductive tract of Scotophilus heathii: role of androgen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptVahtrs%3D&md5=54c2132c009cac62cea1bdf4e1c81fe7CAS |
Satoh, T., Kobayashi, K., Yamashita, S., Kikuchi, M., Sendai, Y., and Hoshi, H. (1994). Tissue inhibitor of metalloproteinases (TIMP-1) produced by granulosa and oviduct cells enhances in vitro development of bovine embryo. Biol. Reprod. 50, 835–844.
| Tissue inhibitor of metalloproteinases (TIMP-1) produced by granulosa and oviduct cells enhances in vitro development of bovine embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFemsb0%3D&md5=aedb3ceefa24a007eaa18216343b8b36CAS |
Satoh, T., Abe, H., Sendai, Y., Iwata, H., and Hoshi, H. (1995). Biochemical characterization of a bovine oviduct-specific sialo-glycoprotein that sustains sperm viability in vitro. Biochim. Biophys. Acta 1266, 117–123.
| Biochemical characterization of a bovine oviduct-specific sialo-glycoprotein that sustains sperm viability in vitro.Crossref | GoogleScholarGoogle Scholar |
Schuett, G. W. (1992). Is long-term sperm storage an important component of the reproductive biology of temperate pit vipers? In ‘Biology of the Pit Vipers’. (Eds J. A. Campbell and E. D. Brodie Jr.) pp. 169–184. (Selva: Tyler, TX.)
Sever, D. M. (1992). Spermiophagy by the spermathecal epithelium of the salamander Eurycea cirrigera. J. Morphol. 212, 281–290.
| Spermiophagy by the spermathecal epithelium of the salamander Eurycea cirrigera.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zntlOkuw%3D%3D&md5=b45b8373f574a6461a361887d28a7238CAS |
Shanbhag, B. A. (2002). Reproductive biology of Indian reptiles. Proc. Indian Natn. Sci. Acad. 6, 497–528.
Shanbhag, B. A., and Prasad, B. S. K. (1993). Induction of ovulation, fertilization and development of embryo in captivity in the garden lizard, Calotes versicolor. J. Herpetol. 27, 480–481.
| Induction of ovulation, fertilization and development of embryo in captivity in the garden lizard, Calotes versicolor.Crossref | GoogleScholarGoogle Scholar |
Shankar, G., Sagar, B. K. C., Kumari, T. R. S., and Marathe, G. K. (2015). Ultrastructural features of sperm storage tubules in the oviduct of the Indian garden lizard, Calotes versicolor. Anat. Rec. (Hoboken) 298, 1932–1937.
| Ultrastructural features of sperm storage tubules in the oviduct of the Indian garden lizard, Calotes versicolor.Crossref | GoogleScholarGoogle Scholar |
Shaw, W. R., Teodori, E., Mitchell, S. N., Baldini, F., Gabrieli, P., Rogers, D. W., and Catteruccia, F. (2014). Mating activates the heme peroxidase HPX15 in the sperm storage organ to ensure fertility in Anopheles gambiae. Proc. Natl Acad. Sci. USA 111, 5854–5859.
| Mating activates the heme peroxidase HPX15 in the sperm storage organ to ensure fertility in Anopheles gambiae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtlaju7k%3D&md5=f7efb2cca4e9b155157470f7e89fa5aaCAS |
Suarez, S. S. (2010). How do sperm get to the egg? Bioengineering expertise needed! Exp. Mech. 50, 1267–1274.
| How do sperm get to the egg? Bioengineering expertise needed!Crossref | GoogleScholarGoogle Scholar |
Tse, P. K., Tse, P. K., Lee, Y. L., Chow, W. N., Luk, J. M., Lee, K. F., and Yeung, W. S. (2008). Preimplantation embryos cooperate with oviductal cells to produce embryotrophic inactivated complement-3b. Endocrinology 149, 1268–1276.
| Preimplantation embryos cooperate with oviductal cells to produce embryotrophic inactivated complement-3b.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVaqtLs%3D&md5=3c616943ea3b0c3c29e2e82c198994bdCAS |
Willaert, B., Suyesh, R., Garg, S., Giri, V. B., Bee, M. A., and Biju, S. D. (2016). A unique mating strategy without physical contact during fertilization in Bombay night frogs (Nyctibatrachus humayuni) with the description of a new form of amplexus and female call. PeerJ 4, e2117.
| A unique mating strategy without physical contact during fertilization in Bombay night frogs (Nyctibatrachus humayuni) with the description of a new form of amplexus and female call.Crossref | GoogleScholarGoogle Scholar |
Wolfner, M. F. (2011). Precious essences: female secretions promote sperm storage in Drosophila. PLoS Biol. 9, e1001191.
| Precious essences: female secretions promote sperm storage in Drosophila.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKhsr%2FF&md5=564614d8759a9a228f8eebf4fefc9239CAS |
