Melatonin potentially acts directly on swine ovary by modulating granulosa cell function and angiogenesis
Giuseppina Basini A B , Simona Bussolati A , Roberta Ciccimarra A and Francesca Grasselli AA Dipartimento di Scienze Medico-Veterinarie, Università degli Studi di Parma, Via del Taglio 10, 43126 Parma, Italy.
B Corresponding author. Email: basini@unipr.it
Reproduction, Fertility and Development 29(12) 2305-2312 https://doi.org/10.1071/RD16513
Submitted: 26 September 2016 Accepted: 7 March 2017 Published: 3 April 2017
Abstract
Melatonin exerts well-known reproductive effects, mainly acting on hypothalamic gonadotrophin-releasing hormone release. More recent data suggest that melatonin acts directly at the ovarian level, even if, at present, these aspects have been only partly investigated. Swine follicular fluid contains melatonin and its concentration is significantly reduced during follicular growth. Therefore, the present study was undertaken to examine the effects of melatonin, used at physiological concentrations, on cultured swine granulosa cells collected from small (<3 mm) and large (>5 mm) follicles on the main parameters of granulosa cell function such as proliferation and steroidogenesis, namely oestradiol 17β and progesterone (P4) production. Moreover, the effects of melatonin on superoxide anion and nitric oxide (NO) generation by swine granulosa cells were also investigated. Finally, since angiogenesis is crucial for follicle growth, the effects of melatonin on new vessel growth were studied. Collected data indicate that melatonin interferes with cultured granulosa cell proliferation and steroidogenesis, specifically in terms of P4 production and NO output. In addition, the events of physiological follicular angiogenesis were stimulated by melatonin as evidenced by angiogenesis bioassay. Therefore, we suggest that physiological melatonin concentrations could potentially be involved in local modulation of swine ovarian follicle function.
Additional keywords: nitric oxide, ovarian follicle, oestradiol 17β, progesterone, superoxide anion.
References
Amir Aslani, B. A., and Ghobadi, S. (2016). Studies on oxidants and antioxidants with a brief glance at their relevance to the immune system. Life Sci. 146, 163–173.| Studies on oxidants and antioxidants with a brief glance at their relevance to the immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtF2qsLw%3D&md5=576833892f486b74abfd079be55ac6a5CAS |
Basini, G., and Grasselli, F. (2015). Nitric oxide in follicle development and oocyte competence. Reproduction 150, R1–R9.
| Nitric oxide in follicle development and oocyte competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsV2ktLrN&md5=58436ed42eaf93e7561eae183473e1ceCAS |
Basini, G., and Tamanini, C. (2000). Selenium stimulates estradiol production in bovine granulosa cells: possible involvement of nitric oxide. Domest. Anim. Endocrinol. 18, 1–17.
| Selenium stimulates estradiol production in bovine granulosa cells: possible involvement of nitric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtFalsr8%3D&md5=7c3994fcc94042eb421aa3b8e25904d5CAS |
Basini, G., Baratta, M., Ponderato, N., Bussolati, S., and Tamanini, C. (1998). Is nitric oxide an autocrine modulator of bovine granulosa cell function? Reprod. Fertil. Dev. 10, 471–478.
| Is nitric oxide an autocrine modulator of bovine granulosa cell function?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvV2msrw%3D&md5=1c939f0ea41e1afdd93473af22b77666CAS |
Basini, G., Grasselli, F., Bianco, F., Tirelli, M., and Tamanini, C. (2004). Effect of reduced oxygen tension on reactive oxygen species production and activity of antioxidant enzymes in swine granulosa cells. Biofactors 20, 61–69.
| Effect of reduced oxygen tension on reactive oxygen species production and activity of antioxidant enzymes in swine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmslOmsLw%3D&md5=37dceee792446acad5a01cadd44f27c4CAS |
Basini, G., Bussolati, S., Santini, S. E., and Grasselli, F. (2008a). Reactive oxygen species and anti-oxidant defences in swine follicular fluids. Reprod. Fertil. Dev. 20, 269–274.
| Reactive oxygen species and anti-oxidant defences in swine follicular fluids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXislyquro%3D&md5=1d0ae31c4b7bfbe0fcd3b372b8df9e59CAS |
Basini, G., Bussolati, S., Santini, S. E., Bianchi, F., Careri, M., Mangia, A., Musci, M., and Grasselli, F. (2008b). Hydroxyestrogens inhibit angiogenesis in swine ovarian follicles. J. Endocrinol. 199, 127–135.
| Hydroxyestrogens inhibit angiogenesis in swine ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtleiurvI&md5=1b547c292ce16a0746a7c88f0a042f24CAS |
Basini, G., Bussolati, S., Baioni, L., and Grasselli, F. (2009). Gossypol, a polyphenolic aldehyde from cotton plant, interferes with swine granulosa cell function. Domest. Anim. Endocrinol. 37, 30–36.
| Gossypol, a polyphenolic aldehyde from cotton plant, interferes with swine granulosa cell function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntVyqsL4%3D&md5=070a5fba442f7ac3a99fa24f26cd930dCAS |
Basini, G., Baioni, L., Bussolati, S., Grolli, S., and Grasselli, F. (2014a). Prolactin is a potential physiological modulator of swine ovarian follicle function. Regul. Pept. 189, 22–30.
| Prolactin is a potential physiological modulator of swine ovarian follicle function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXns1CktLs%3D&md5=3dc61822fcca84771dca69cc0d98e9c6CAS |
Basini, G., Falasconi, I., Bussolati, S., Grolli, S., Ramoni, R., and Grasselli, F. (2014b). Isolation of endothelial cells and pericytes from swine corpus luteum. Domest. Anim. Endocrinol. 48, 100–109.
| Isolation of endothelial cells and pericytes from swine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvFGht7o%3D&md5=dc0f5c62b58b535a249025787c90cd34CAS |
Basini, G., Spatafora, C., Tringali, C., Bussolati, S., and Grasselli, F. (2014c). Effects of a ferulate-derived dihydrobenzofuran neolignan on angiogenesis, steroidogenesis, and redox status in a swine cell model. J. Biomol. Screen. 19, 1282–1289.
| Effects of a ferulate-derived dihydrobenzofuran neolignan on angiogenesis, steroidogenesis, and redox status in a swine cell model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXisFSqtL4%3D&md5=005cd60163e6e8ce50bcadd1c192c6cfCAS |
Basini, G., Falasconi, I., Bussolati, S., Grolli, S., Di Lecce, R., and Grasselli, F. (2016). Swine granulosa cells show typical endothelial cell characteristics. Reprod. Sci. 23, 630–637.
| Swine granulosa cells show typical endothelial cell characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1ens7fF&md5=10e3a25e96af858ba0747a7dea534eceCAS |
Benov, L., and Fridovich, I. (2002). Is reduction of the sulfonated tetrazolium 2,3-bis (2-methoxy-4-nitro-5-sulfophenyl)-2-tetrazolium 5-carboxanilide a reliable measure of intracellular superoxide production? Anal. Biochem. 310, 186–190.
| Is reduction of the sulfonated tetrazolium 2,3-bis (2-methoxy-4-nitro-5-sulfophenyl)-2-tetrazolium 5-carboxanilide a reliable measure of intracellular superoxide production?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotlKis7k%3D&md5=7d61dae114da13f3d9e55cdee4c7bd5fCAS |
Blask, D. E., Sauer, L. A., Dauchy, R. T., Holowachuk, E. W., and Ruhoff, M. S. (1999). New insights into melatonin regulation of cancer growth. Adv. Exp. Med. Biol. 460, 337–343.
| New insights into melatonin regulation of cancer growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltV2qu7o%3D&md5=1f0d5e8f9c8ce53f8fcaa1d8b22685c5CAS |
Brzezinski, A., Seibel, M. M., Lynch, H. J., Deng, M. H., and Wurtman, R. J. (1987). Melatonin in human preovulatory follicular fluid. J. Clin. Endocrinol. Metab. 64, 865–867.
| Melatonin in human preovulatory follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhvV2mtrY%3D&md5=e73e008b94f38afb265b3f1b403ea044CAS |
Chu, E. W., Wurtman, R. J., and Axelrod, J. (1964). An inhibitory effect of melatonin on the estrous phase of the estrous cycle of the rodent. Endocrinology 75, 238–242.
| An inhibitory effect of melatonin on the estrous phase of the estrous cycle of the rodent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2cXktlGntLw%3D&md5=24153917dd5f3389f0572db7c2562fafCAS |
Claustrat, B., and Leston, J. (2015). Melatonin: physiological effects in humans. Neurochirurgie 61, 77–84.
| Melatonin: physiological effects in humans.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2MjnsV2gtA%3D%3D&md5=bd0a0a38d42c8b4de11d2b415b1a112dCAS |
Cruz, M. H., Leal, C. L., da Cruz, J. F., Tan, D. X., and Reiter, R. J. (2014a). Role of melatonin on production and preservation of gametes and embryos: a brief review. Anim. Reprod. Sci. 145, 150–160.
| Role of melatonin on production and preservation of gametes and embryos: a brief review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivFCksb8%3D&md5=575bfcba00eea671323bf6959bb0291eCAS |
Cruz, M. H. C., Leal, C. L. V., Cruz, J. F., Tan, D. X., and Reiter, R. J. (2014b). Essential actions of melatonin in protecting the ovary from oxidative damage. Theriogenology 82, 925–932.
| Essential actions of melatonin in protecting the ovary from oxidative damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlCjsbbK&md5=29b47f5db701ab46488b9185ad2e500dCAS |
Dong, Y. L., and Yallampalli, C. (1996). Interaction between nitric oxide and prostaglandin E2 pathways in pregnant rat uteri. Am. J. Physiol. 270, E471–E476.
| 1:CAS:528:DyaK28XitVajtb0%3D&md5=da90149708de252cef825ec222fa71c6CAS |
Drazen, D. L., Bilu, D., Bilbo, S. D., and Nelson, R. J. (2001). Melatonin enhancement of splenocyte proliferation is attenuated by luzindole, a melatonin receptor antagonist. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R1476–R1482.
| 1:CAS:528:DC%2BD3MXjsVequrk%3D&md5=edb8ef9d349a280b9558ab85c73d2ef2CAS |
González, A., Martínez-Campa, C., Mediavilla, M. D., Alonso-González, C., Sánchez-Barceló, E. J., and Cos, S. (2007). Inhibitory effects of pharmacological doses of melatonin on aromatase activity and expression in rat glioma cells. Br. J. Cancer 97, 755–760.
| Inhibitory effects of pharmacological doses of melatonin on aromatase activity and expression in rat glioma cells.Crossref | GoogleScholarGoogle Scholar |
Graham, J. D., and Clarke, C. L. (1997). Physiological action of progesterone in target tissues. Endocr. Rev. 18, 502–519.
| 1:CAS:528:DyaK2sXlvV2hu7o%3D&md5=30233e3741b6f29f502610e76a6ebec0CAS |
Grasselli, F., Baratta, M., and Tamanini, C. (1993). Effects of a GnRH analogue (buserelin) infused via osmotic minipumps on pituitary and ovarian activity of prepubertal heifers. Anim. Reprod. Sci. 32, 153–161.
| Effects of a GnRH analogue (buserelin) infused via osmotic minipumps on pituitary and ovarian activity of prepubertal heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXps1ChsQ%3D%3D&md5=9b50be531584ac5ebdc8278c098edacfCAS |
Grasselli, F., Ponderato, N., Basini, G., and Tamanini, C. (2001). Nitric oxide synthase expression and nitric oxide/cyclic GMP pathway in swine granulosa cells. Domest. Anim. Endocrinol. 20, 241–252.
| Nitric oxide synthase expression and nitric oxide/cyclic GMP pathway in swine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtV2lsrk%3D&md5=d2fb349bc0eb68edba9bbf1a3c98ec31CAS |
Hoffman, R. A., and Reiter, R. J. (1965a). Pineal gland: influence on gonads of male hamsters. Science 148, 1609–1611.
| Pineal gland: influence on gonads of male hamsters.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2M%2Fpt1Wrsw%3D%3D&md5=8c36c602b248bf6f8f450a00f1656702CAS |
Hoffman, R. A., and Reiter, R. J. (1965b). Influence of compensatory mechanisms and the pineal upon light-induced gonadal atrophy in hamsters. Nature 207, 658–659.
| Influence of compensatory mechanisms and the pineal upon light-induced gonadal atrophy in hamsters.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF287jslWktg%3D%3D&md5=669fb20f74cd7f18b49752cadc946250CAS |
Hornedo-Ortega, R., Cerezo, A. B., Troncoso, A. M., Garcia-Parrilla, M. C., and Mas, A. (2016). Melatonin and other tryptophan metabolites produced by yeasts: implications in cardiovascular and neurodegenerative diseases. Front. Microbiol. 6, 1565.
| Melatonin and other tryptophan metabolites produced by yeasts: implications in cardiovascular and neurodegenerative diseases.Crossref | GoogleScholarGoogle Scholar |
Huebner, O. (1898). Tumor des Glandula pinealis. Dtsch. Med. Wochenschr. 24, 214–215.
Itoh, M. T., Ishizuka, B., Kuribayashi, Y., Amemiya, A., and Sumi, Y. (1999). Melatonin, its precursors, and synthesizing enzyme activities in the human ovary. Mol. Hum. Reprod. 5, 402–408.
| Melatonin, its precursors, and synthesizing enzyme activities in the human ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtl2hs7k%3D&md5=c8214a3f44c7b94cf25ba1aa9dcf0029CAS |
Kang, J. T., Koo, O. J., Kwon, D. K., Park, H. J., Jang, G., Kang, S. K., and Lee, B. C. (2009). Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells. J. Pineal Res. 46, 22–28.
| Effects of melatonin on in vitro maturation of porcine oocyte and expression of melatonin receptor RNA in cumulus and granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsV2rtQ%3D%3D&md5=46f93934abb79891ac558ce9cb3532eaCAS |
Lerner, A. B., Case, J. D., Takahashi, Y., Lee, T. H., and Mori, W. (1958). Isolation of melatonin, the pineal gland factor that lightens melanocytes. J. Am. Chem. Soc. 80, 2587.
| Isolation of melatonin, the pineal gland factor that lightens melanocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1cXhtFGmsLc%3D&md5=5c64572672f27d77630df373ae37a5e2CAS |
Lima, G. N., Maganhin, C. C., Simões, R. S., Baracat, M. C., Sasso, G. R., Fuchs, L. F., Simões Mde, J., Baracat, E. C., and Soares Júnior, J. M. (2015). Steroidogenesis-related gene expression in the rat ovary exposed to melatonin supplementation. Clinics (Sao Paulo) 70, 144–151.
| Steroidogenesis-related gene expression in the rat ovary exposed to melatonin supplementation.Crossref | GoogleScholarGoogle Scholar |
Reiter, R. J., Tan, D. X., Tamura, H., Cruz, M. H., and Fuentes-Broto, L. (2014). Clinical relevance of melatonin in ovarian and placental physiology: a review. Gynecol. Endocrinol. 30, 83–89.
| Clinical relevance of melatonin in ovarian and placental physiology: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlCmt70%3D&md5=35dab0ea3c8659bf7a6c3dbbc459e792CAS |
Rönnberg, L., Kauppila, A., Leppäluoto, J., Martikainen, H., and Vakkuri, O. (1990). Circadian and seasonal variation in human preovulatory follicular fluid melatonin concentration. J. Clin. Endocrinol. Metab. 71, 493–496.
| Circadian and seasonal variation in human preovulatory follicular fluid melatonin concentration.Crossref | GoogleScholarGoogle Scholar |
Roth, J. A., Rosenblatt, T., Lis, A., and Bucelli, R. (2001). Melatonin-induced suppression of PC12 cell growth is mediated by its Gi coupled transmembrane receptors. Brain Res. 919, 139–146.
| Melatonin-induced suppression of PC12 cell growth is mediated by its Gi coupled transmembrane receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvFCktrw%3D&md5=9db7ab4291102ca16187b4bf4525a56cCAS |
Sainz, R. M., Mayo, J. C., Rodriguez, C., Tan, D. X., Lopez-Burillo, S., and Reiter, R. J. (2003). Melatonin and cell death: differential actions on apoptosis in normal and cancer cells. Cell. Mol. Life Sci. 60, 1407–1426.
| Melatonin and cell death: differential actions on apoptosis in normal and cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms1Witr0%3D&md5=c8d2cd1276f3eaec29b594dcdfe52775CAS |
Shi, J. M., Tian, X. Z., Zhou, G. B., Wang, L., Gao, C., Zhu, S. E., Zeng, S. M., Tian, J. H., and Liu, G. S. (2009). Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes. J. Pineal Res. 47, 318–323.
| Melatonin exists in porcine follicular fluid and improves in vitro maturation and parthenogenetic development of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlOqtLnP&md5=0b2a97885b94eb203f9a63b1571f9afaCAS |
Sugino, N., Takiguchi, S., Kashida, S., Takayama, H., Yamagata, Y., Nakamura, Y., and Kato, H. (1999). Suppression of intracellular superoxide dismutase activity by antisense oligonucleotides causes inhibition of progesterone production by rat luteal cells. Biol. Reprod. 61, 1133–1138.
| Suppression of intracellular superoxide dismutase activity by antisense oligonucleotides causes inhibition of progesterone production by rat luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlajtLo%3D&md5=5cf8eebaaed58c623320adde358a1599CAS |
Tamura, H., Nakamura, Y., Korkmaz, A., Manchester, L. C., Tan, D. X., Sugino, N., and Reiter, R. J. (2009). Melatonin and the ovary: physiological and pathophysiological implications. Fertil. Steril. 92, 328–343.
| Melatonin and the ovary: physiological and pathophysiological implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFWisLrP&md5=62ac97cb9eaadd25a2be6f0a30713db9CAS |
Tamura, H., Takasaki, A., Taketani, T., Tanabe, M., Kizuka, F., Lee, L., Tamura, I., Maekawa, R., Aasada, H., Yamagata, Y., and Sugino, N. (2012). The role of melatonin as an antioxidant in the follicle. J. Ovarian Res. 5, 5.
| The role of melatonin as an antioxidant in the follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFertLk%3D&md5=b714e8e4b4137e03b811616533f99af8CAS |
Tamura, H., Takasaki, A., Taketani, T., Tanabe, M., Lee, L., Tamura, I., Maekawa, R., Aasada, H., Yamagata, Y., and Sugino, N. (2014). Melatonin and female reproduction. J. Obstet. Gynaecol. Res. 40, 1–11.
| Melatonin and female reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtVagsA%3D%3D&md5=80f565357d920f70c9fb51a7f1d50ef4CAS |
Tan, D. X., Zheng, X., Kong, J., Manchester, L. C., Hardeland, R., Kim, S. J., Xu, X., and Reiter, R. J. (2014). Fundamental issues related to the origin of melatonin and melatonin isomers during evolution: relation to their biological functions. Int. J. Mol. Sci. 15, 15858–15890.
| Fundamental issues related to the origin of melatonin and melatonin isomers during evolution: relation to their biological functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVaqtLjJ&md5=5cc0e66628363cd437b2317da14ffaa3CAS |
Tanavde, V. S., and Maitra, A. (2003). In vitro modulation of steroidogenesis and gene expression by melatonin: a study with porcine antral follicles. Endocr. Res. 29, 399–410.
| In vitro modulation of steroidogenesis and gene expression by melatonin: a study with porcine antral follicles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovVOnsLg%3D&md5=dfc8c2ce8e12c238405b38747366de73CAS |
Ukeda, H., Shimamura, T., Tsubouchi, M., Harada, Y., Nakai, Y., and Sawamura, M. (2002). Spectrophotometric assay of superoxide anion formed in Maillard reaction based on highly water-soluble tetrazolium salt. Anal. Sci. 18, 1151–1154.
| Spectrophotometric assay of superoxide anion formed in Maillard reaction based on highly water-soluble tetrazolium salt.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotFGrsL4%3D&md5=ce5f84ada568b205aedb2bdea89dfac6CAS |
Vriend, J., and Reiter, R. J. (2016). Melatonin and the von Hippel-Lindau/HIF-1 oxygen sensing mechanism: a review. Biochim. Biophys. Acta 1865, 176–183.
| 1:CAS:528:DC%2BC28XjtVCht74%3D&md5=28f9f73ea4362ddee20ec2bffe3b6992CAS |
Wang, S. J., Liu, W. J., Wu, C. J., Ma, F. H., Ahmad, S., Liu, B. R., Han, L., Jiang, X. P., Zhang, S. J., and Yang, L. G. (2012). Melatonin suppresses apoptosis and stimulates progesterone production by bovine granulosa cells via its receptors (MT1 and MT2). Theriogenology 78, 1517–1526.
| Melatonin suppresses apoptosis and stimulates progesterone production by bovine granulosa cells via its receptors (MT1 and MT2).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGntr7I&md5=e9a9f7be0cedede806818bc8d6ec74ddCAS |
Zwirska-Korczala, K., Jochem, J., Adamczyk-Sowa, M., Sowa, P., Polaniak, R., Birkner, E., Latocha, M., Pilc, K., and Suchanek, R. (2005). Influence of melatonin on cell proliferation, antioxidative enzyme activities and lipid peroxidation in 3T3–L1 preadipocytes – an in vitro study. J. Physiol. Pharmacol. 56, 91–99.