Exogenous long-term treatment with 17β-oestradiol alters the innervation pattern in pig ovary
Marlena Koszykowska A , Jarosław Całka B , Aleksandra Nidzgorska B and Barbara Jana A C
+ Author Affiliations
- Author Affiliations
A Division of Biology Reproduction, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences, Olsztyn 10-747, Tuwima 10, Poland.
B Division of Clinical Physiology, Faculty of Veterinary Medicine, University of Warmia and Mazury, Olsztyn 10-718, Oczapowskiego 13, Poland.
C Corresponding author. Email: b.jana@pan.olsztyn.pl
Reproduction, Fertility and Development 25(4) 661-673 https://doi.org/10.1071/RD11271
Submitted: 25 October 2011 Accepted: 18 May 2012 Published: 17 July 2012
Abstract
The aim of the present study was to determine the effect of long-term 17β-oestradiol (E2) exposure, a simulation of pathological states that occur with oestrogen overproduction, on the innervation patterns of ovaries in adult gilts. The intraovarian distribution and density of nerve fibres immunoreactive (IR) to protein gene product (PGP) 9.5 and containing dopamine-β-hydroxylase (DBH), neuropeptide Y (NPY), somatostatin (SOM) and galanin (GAL) were determined. From Day 4 of the first oestrous cycle to Day 20 of the second cycle studied, experimental gilts were injected with E2 (1000 μg every 12 h) whereas control gilts were injected with corn oil. After E2 administration, there was an increase in the number of PGP9.5-, DBH-, NPY- and GAL-IR fibres. Numerous PGP9.5-IR terminals were observed within the ground plexus around secondary follicles and small or medium tertiary follicles. Long-term E2 treatment increased the density of DBH- and NPY-IR fibres in the cortical part of the ground plexus, DBH- and GAL-IR fibres in the medullary part of the ground plexus, DBH-IR fibres near small and medium tertiary follicles and NPY-IR fibres around medullary arteries. The data indicate that long-term exposure of gilts to E2 increases the total number of intraovarian fibres, including sympathetic fibres. These results suggest that elevated E2 levels that occur during pathological states may affect the innervation patterns of ovaries and their function(s).
Additional keywords: follicles, gilts, hyperoestrogenism.
References
Andreani, C. L., Lazzarin, N., Pierro, E., Lanzone, A., and Mancuso, S. (1995). Somatostatin action on rat ovarian steroidogenesis. Hum. Reprod. 10, 1968–1973.| 1:CAS:528:DyaK2MXptFOitro%3D&md5=cce97b6dd68b9489249a0a603826e00dCAS | 8567824PubMed |
Anesetti, G., Lombide, P., and Chávez-Genaro, R. (2009). Prepubertal estrogen exposure modifies neurotrophin receptor expression in celiac neurons and alters ovarian innervation. Auton. Neurosci. 145, 35–43.
| Prepubertal estrogen exposure modifies neurotrophin receptor expression in celiac neurons and alters ovarian innervation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVersQ%3D%3D&md5=48b72fd2657c4d15189f9c0e50448fddCAS | 19036644PubMed |
Barboni, B., Martelli, A., Berardinelli, P., Russo, V., Turriani, M., Bernabò, N., Lucidi, P., and Mattioli, M. (2004). Ovarian follicle vascularization in fasted pig. Theriogenology 62, 943–957.
| Ovarian follicle vascularization in fasted pig.Crossref | GoogleScholarGoogle Scholar | 15251245PubMed |
Barreca, A., Valli, B., Cesarone, A., Arvigo, M., Balasini, M., Battista La Sala, G., Garrone, S., Minuto, F., and Giordano, G. (1998). Effects of the neuropeptide Y on estradiol and progesterone secretion by human granulosa cells in culture. Fertil. Steril. 70, 320–325.
| Effects of the neuropeptide Y on estradiol and progesterone secretion by human granulosa cells in culture.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czlvFCitQ%3D%3D&md5=c882cd7e3acc89d646f5a709a823643dCAS | 9696228PubMed |
Blacklock, A. D., and Smith, P. G. (2004). Estrogen increases calcitonin gene-related peptide-immunoreactive sensory innervation of rat mammary gland. J. Neurobiol. 59, 192–204.
| Estrogen increases calcitonin gene-related peptide-immunoreactive sensory innervation of rat mammary gland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt1Shsrc%3D&md5=c9a0319edc3b7991799340be8ba61817CAS | 15085537PubMed |
Blacklock, A. D., Cauveren, J. A., and Smith, P. G. (2004). Estrogen selectively increases sensory nociceptor innervation of arterioles in the female rat. Brain Res. 1018, 55–65.
| Estrogen selectively increases sensory nociceptor innervation of arterioles in the female rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsl2itr0%3D&md5=81c67cfe0f2e199c8186065b8fc88ec8CAS | 15262205PubMed |
Crawley, J. N. (1995). Biological actions of galanin. Regul. Pept. 59, 1–16.
| Biological actions of galanin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotFCqtL0%3D&md5=59101f3c1ce6e45a25c0a9fc4e5c2bfbCAS | 12506409PubMed |
Curry, T. E., , Lawrence, I. E., and Burden, H. W. (1984). Ovarian sympathectomy in the guinea pig. I. Effects on follicular development during the estrous cycle. Cell Tissue Res. 236, 257–263.
Demont, F., Fourquet, F., Rogers, M., and Lansac, J. (2001). Epidemiology of apparently benign ovarian cysts. J. Gynecol. Obstet. Biol. Reprod. 30, 8–11.
Dickerson, S. M., and Gore, A. C. (2007). Estrogenic environmental endocrine-disrupting chemical effects on reproductive neuroendocrine function and dysfunction across the life cycle. Rev. Endocr. Metab. Disord. 8, 143–159.
| Estrogenic environmental endocrine-disrupting chemical effects on reproductive neuroendocrine function and dysfunction across the life cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVGmsL%2FE&md5=319c8c4f18508185be00acc45345c1a7CAS | 17674209PubMed |
Dziadkowiec, J., Danilczuk, H., and Rembiesa, R. (1982). Biosynthesis of progesterone in rat placenta. Endokrynol. Pol. 33, 201–207.
| 1:CAS:528:DyaL3sXls12ru7c%3D&md5=f35a2078410f2fafe33799e32d01a247CAS |
Dziadkowiec, J., Warchoł, A., and Rembiesa, R. (1982). Biosynthesis of estrogens in pregnant rats. Endokrynol. Pol. 33, 4–6.
Hiroi, H., Osuga, Y., Tarumoto, Y., Shimokama, T., Yano, T., Yokota, H., and Taketani, Y. (2002). A case of estrogen-producing Brenner tumor with a stromal component as a potential source for estrogen. Oncology 63, 201–204.
| A case of estrogen-producing Brenner tumor with a stromal component as a potential source for estrogen.Crossref | GoogleScholarGoogle Scholar | 12239457PubMed |
Hotchkiss, J., Aitkinson, L. E., and Knobil, E. (1971). Time course of serum estrogen and luteinizing hormone (LH) concentration during the menstrual cycle of the rhesus monkey. Endocrinology 89, 177–183.
| Time course of serum estrogen and luteinizing hormone (LH) concentration during the menstrual cycle of the rhesus monkey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXkslertL0%3D&md5=778c7fe3498a048859a3a8044e4c766bCAS | 4995997PubMed |
Huang, E. J., and Reichardt, L. F. (2001). Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677–736.
| Neurotrophins: roles in neuronal development and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXls1ShsL4%3D&md5=fbe179b35e61f7fe40b33d1b8eb6636cCAS | 11520916PubMed |
Jana, B., and Kozłowska, A. (2008). Nerve growth factor: its expression and participation in the functioning of reproductive organs in females. Med. Welt 64, 520–524.
Jana, B., and Majewski, M. (2007). Influence of the peripheral nervous system on ovarian function. Med. Welt 63, 1163–1167.
Keator, C. S., Custer, E. E., Hoagland, T. A., Schreiber, D. T., Mah, K., Lawsom, A. M., Slayden, O. D., and McCraken, J. A. (2010). Evidence for a potential role of neuropeptide Y in ovine corpus luteum function. Domest. Anim. Endorcinol. 38, 103–114.
| Evidence for a potential role of neuropeptide Y in ovine corpus luteum function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosFSq&md5=d8910e604d152482fe7473ccec1ec1ecCAS |
Kengaku, K., Tanaka, T., and Kamomae, H. (2007). Changes in the peripheral concentrations of inhibin, follicle-stimulating hormone, luteinizing hormone, progesterone and estradiol-17beta during turnover of cystic follicles in dairy cows with spontaneous follicular cysts. J. Reprod. Dev. 53, 987–993.
| Changes in the peripheral concentrations of inhibin, follicle-stimulating hormone, luteinizing hormone, progesterone and estradiol-17beta during turnover of cystic follicles in dairy cows with spontaneous follicular cysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlOls7nL&md5=3ea59f0a73983c42ed884d3f55b27d5eCAS | 17690530PubMed |
Koszykowska, M., Całka, J., Szwajca, P., and Jana, B. (2011a). Long-term estradiol-17β administration decreases the number of neurons in the caudal mesenteric ganglion innervating the ovary in sexually mature gilts. J. Reprod. Dev. 57, 62–71.
| Long-term estradiol-17β administration decreases the number of neurons in the caudal mesenteric ganglion innervating the ovary in sexually mature gilts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkt1Cgu7g%3D&md5=f6bd71921289d56b222983154976e258CAS | 20881351PubMed |
Koszykowska, M., Całka, J., Gańko, M., and Jana, B. (2011b). Long-term estradiol-17β administration reduces population of neurons in the sympathetic chain ganglia supplying the ovary in adult gilts. Exp. Mol. Pathol. 91, 353–361.
| Long-term estradiol-17β administration reduces population of neurons in the sympathetic chain ganglia supplying the ovary in adult gilts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptVyksr4%3D&md5=a5d26f2f4bf8944ddd33ac5bf92a912eCAS | 21545801PubMed |
Kozłowska, A. (2009). The innervation and steroidogenic activity of cystic porcine ovaries. Ph.D. Thesis, Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences in Olsztyn.
Krizsan-Agbas, D., Pedchenko, T., Hasan, W., and Smith, P. G. (2003). Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus. Eur. J. Neurosci. 18, 2760–2768.
| Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3srns1Olsw%3D%3D&md5=95c6c5347ccad7cd86c664a88a944451CAS | 14656325PubMed |
Krizsan-Agbas, D., Pedchenko, T., and Smith, P. G. (2008). Neurotrimin is an estrogen-regulated determinant of peripheral sympathetic innervation. J. Neurosci. Res. 86, 3086–3095.
| Neurotrimin is an estrogen-regulated determinant of peripheral sympathetic innervation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVaitbvM&md5=fca55e70c075e8f8a20d76234f37aa7dCAS | 18627025PubMed |
Kucharski, J., Jana, B., and Zezula-Szpyra, A. (2002). Effect of the gonadotrophins treatment on morphological alterations in ovary and peripheral plasma concentrations of steroid hormones in gilts. Pol. J. Vet. Sci. 5, 7–15.
| 1:CAS:528:DC%2BD38Xks1ensb8%3D&md5=9719d29b1d5278037b1e778e503f3b69CAS | 11944587PubMed |
Lakomy, M., Kaleczyc, J., and Całka, J. (1986a). The effect of oestradiolum benzoicum and progesterone on AChE activity in the nerves of the female reproductive system of immature pigs. Gegenbaurs Morphol. Jahrb. 132, 333–348.
| 1:STN:280:DyaL28zgtFOltg%3D%3D&md5=729c4afc6fa78dbf0c85f2c62eff3199CAS | 3743996PubMed |
Lakomy, M., Kotwica, J., Całka, J., and Kaleczyc, J. (1986b). The effect of oestradiolum benzoicum and progesterone on the noradrenaline content in organs of the female reproductive system of sexually immature pigs. Gegenbaurs Morphol. Jahrb. 132, 129–143.
| 1:STN:280:DyaL283itFGrug%3D%3D&md5=0dd856bd8fa7538f381243f1950dd664CAS | 3710109PubMed |
Lara, H. E., Ferruz, J. L., Luza, S., Bustamante, D. A., Borges, Y., and Ojeda, S. R. (1993). Activation of ovarian sympathetic nerves in polycystic ovary syndrome. Endocrinology 133, 2690–2695.
| Activation of ovarian sympathetic nerves in polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXnsVOrtg%3D%3D&md5=fb931bd819ee7f86eac03c7b1d05c77dCAS | 7902268PubMed |
Lara, H. E., Dissen, G. A., Leyton, V., Paredes, A., Fuenzalida, H., Fiedler, J. L., and Ojeda, S. R. (2000). An increased intraovarian synthesis of nerve growth factor and its low affinity receptor is a principal component of steroid-induced polycystic ovary in the rat. Endocrinology 141, 1059–1072.
| An increased intraovarian synthesis of nerve growth factor and its low affinity receptor is a principal component of steroid-induced polycystic ovary in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFOrsbg%3D&md5=c3c6d2f38a775561df262d51a813171bCAS | 10698182PubMed |
Majewski, M. (1997). Afferent and efferent innervation of the porcine ovary: sources of origin and chemical coding. Acta Acad. Agric. Tech. Olst. Vet. Suppl. B 24, 3–125.
Majewski, M., and Heym, C. (1991). The origin of ovarian neuropeptide Y (NPY)-immunoreactive nerve fibres from the inferior mesenteric ganglion in the pig. Cell Tissue Res. 266, 591–596.
| The origin of ovarian neuropeptide Y (NPY)-immunoreactive nerve fibres from the inferior mesenteric ganglion in the pig.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383kvVKmtA%3D%3D&md5=4788ddc9e3c92aa2de16f6e015765462CAS | 1687453PubMed |
Markiewicz, W., Jaroszewski, J. J., Barszczewska, B., and Sienkiewicz, W. (2003). Localization of neuropeptide Y and norepinephrine in the porcine ovarian artery and their influence on the local blood pressure. Folia Histochem. Cytobiol. 41, 73–81.
| 1:CAS:528:DC%2BD3sXjs1akt7w%3D&md5=12df8e7771fae15fe0fdb00c427e33c3CAS | 12722792PubMed |
Matias-Guiu, X. (2010). Endocrine ovaries. In ‘Endocrine Pathology: Differential Diagnosis and Molecular Advances’. (Ed. R.V. Lloyd.) pp. 307–331. (Humana Press: New York.)
Miyamoto, A., Brückmann, A., von Lützow, H., and Schams, D. (1993). Multiple effects of neuropeptide Y, substance P and vasoactive intestinal polypeptide on progesterone and oxytocin release from bovine corpus luteum in vitro. J. Endocrinol. 138, 451–458.
| Multiple effects of neuropeptide Y, substance P and vasoactive intestinal polypeptide on progesterone and oxytocin release from bovine corpus luteum in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsVKq&md5=15adc3244bc4de97ab859dd1ba5cba9dCAS | 7506290PubMed |
Nalbandov, A. V. (1952). Anatomic and endocrine causes of sterility in female swine. Fertil. Steril. 3, 100–120.
| 1:STN:280:DyaG38%2Fls1yntQ%3D%3D&md5=85b52a70a3da1a765d777ec657bcc917CAS | 14926737PubMed |
Nestorović, N., Manojlović-Stojanoski, M., Ristić, N., Sekulić, M., Sošić-Jurjević, B., Filipović, B., and Milošević, V. (2008). Somatostatin-14 influences pituitary–ovarian axis in peripubertal rats. Histochem. Cell Biol. 130, 699–708.
| Somatostatin-14 influences pituitary–ovarian axis in peripubertal rats.Crossref | GoogleScholarGoogle Scholar | 18493786PubMed |
Pasterkamp, R. J., Peschon, J. J., Spriggs, M. K., and Kolodkin, A. L. (2003). Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature 424, 398–405.
| Semaphorin 7A promotes axon outgrowth through integrins and MAPKs.Crossref | GoogleScholarGoogle Scholar | 12879062PubMed |
Pessina, M. A., Hoyt, R. F.,, Goldstein, I., and Traish, A. M. (2006). Differential effects of estradiol, progesterone, and testosterone on vaginal structural integrity. Endocrinology 147, 61–69.
| Differential effects of estradiol, progesterone, and testosterone on vaginal structural integrity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptFaj&md5=8a129b6412ff7373646c0634c9440cd8CAS | 16210369PubMed |
Pitzel, L., Jarry, H., and Wuttke, W. (1991). Effects of substance-P and neuropeptide-Y on in vitro steroid release by porcine granulosa and luteal cells. Endocrinology 129, 1059–1065.
| Effects of substance-P and neuropeptide-Y on in vitro steroid release by porcine granulosa and luteal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltVKrtL4%3D&md5=fdff8b1b8e0e3e57a14b528640b49bd0CAS | 1713157PubMed |
Richeri, A., Chalar, C., Bianchimano, P., Greif, G., and Brauer, M. M. (2007). Oestrogen regulation of semaphorin expression in the rat uterus. In ‘Proceedings of the 7th IBRO World Congress of Neuroscience, Melbourne’. (Ed. E. M. McLachlan.) p. 343. (The Australian Neuroscience Society: Melbourne.)
Rosa-e-Silva, A., Guimaraes, M. A., Padmanabhan, V., and Lara, H. E. (2003). Prepubertal administration of estradiol valerate disrupts cyclicity and leads to cystic ovarian morphology during adult life in the rat: role of sympathetic innervation. Endocrinology 144, 4289–4297.
| Prepubertal administration of estradiol valerate disrupts cyclicity and leads to cystic ovarian morphology during adult life in the rat: role of sympathetic innervation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1SrtL0%3D&md5=1da62df02bc41d4494d0326b5f679827CAS | 12960066PubMed |
Shinohara, Y., Matsumoto, A., and Mori, T. (1998). Effects of prenatal exposure to diethylstilbestrol on the sympathetic nervous system in the rat ovary. Neurosci. Lett. 255, 123–126.
| Effects of prenatal exposure to diethylstilbestrol on the sympathetic nervous system in the rat ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmvFWmur8%3D&md5=9388e591d44af61faa2bced73820b620CAS | 9832188PubMed |
Shinohara, Y., Matsumoto, A., Hayashi, S., and Mori, T. (2000). Prenatal exposure to diethylstilbestrol decreases the number of estrogen receptor alpha-containing neurons innervating the ovary in rat celiac ganglion. Neuroscience 101, 779–783.
| Prenatal exposure to diethylstilbestrol decreases the number of estrogen receptor alpha-containing neurons innervating the ovary in rat celiac ganglion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosFemtL0%3D&md5=c529a15a08de045306e3cb5f37dbb3d7CAS | 11113326PubMed |
Słomczyńska, M., and Woźniak, J. (2001). Differential distribution of estrogen receptor-beta and estrogen receptor-alpha in the porcine ovary. Exp. Clin. Endocrinol. Diabetes 109, 238–244.
| Differential distribution of estrogen receptor-beta and estrogen receptor-alpha in the porcine ovary.Crossref | GoogleScholarGoogle Scholar | 11453037PubMed |
Smith, P. G., George, M., and Bradshaw, S. (2009). Estrogen promotes sympathetic nerve regeneration in rat proximal urethra. Urology 73, 1392–1396.
| Estrogen promotes sympathetic nerve regeneration in rat proximal urethra.Crossref | GoogleScholarGoogle Scholar | 19362354PubMed |
Sosa, Z. Y., Casais, M., Rastrilla, A. M., and Aguado, L. (2000). Adrenergic influences on coeliac ganglion affect the release of progesterone from cycling ovaries: characterization of an in vitro system. J. Endocrinol. 166, 307–318.
| Adrenergic influences on coeliac ganglion affect the release of progesterone from cycling ovaries: characterization of an in vitro system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFOqt78%3D&md5=3966a667348a8318218d5af896d9e2e4CAS | 10927620PubMed |
Sotomayor-Zárate, R., Dorfman, M., Paredes, A., and Lara, H. E. (2008). Neonatal exposure to estradiol valerate programs ovarian sympathetic innervation and follicular development in the adult rat. Biol. Reprod. 78, 673–680.
| Neonatal exposure to estradiol valerate programs ovarian sympathetic innervation and follicular development in the adult rat.Crossref | GoogleScholarGoogle Scholar | 18077802PubMed |
Swindle, M. M., Moody, D. C., and Phillips, L. D. (1992). ‘Swine as Models in Biomedical Research.’ (Iowa State University Press: Ames.)
Szafranska, B., Ziecik, A. J., and Okrasa, S. (2002). Primary antisera against selected steroids or proteins and secondary antisera against γ-globulins: an available tool for studies of reproductive processes. Reprod. Biol. 5, 187–203.
Szatkowska, C., and Łakomy, M. (1987). Adrenergic innervation of swine ovaries in various periods of pregnancy Pol. Arch. Weter. 27, 73–80.
| 1:STN:280:DyaL1czitVSqsw%3D%3D&md5=21aaa521fde71fa8e5f061661ecb8199CAS | 3454964PubMed |
Tanaka, Y. O., Saida, T. S., Minami, R., Yagi, T., Tsunoda, H., Yoshikawa, H., and Minami, M. (2007). MR findings of ovarian tumors with hormonal activity, with emphasis on tumors other than sex cord-stromal tumors. Eur. J. Radiol. 62, 317–327.
| MR findings of ovarian tumors with hormonal activity, with emphasis on tumors other than sex cord-stromal tumors.Crossref | GoogleScholarGoogle Scholar | 17403591PubMed |
Ting, A. Y., Blacklock, A. D., and Smith, P. G. (2004). Estrogen regulates vaginal sensory and autonomic nerve density in the rat. Biol. Reprod. 71, 1397–1404.
| Estrogen regulates vaginal sensory and autonomic nerve density in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVGqurc%3D&md5=4c5e1a87d433043232580f77f646190dCAS | 15189832PubMed |
Traurig, H. H., and Papka, R. E. (1993). Autonomic efferent and visceral sensory innervation of the female reproductive system: special reference to the functional roles of nerves in reproductive organs. In ‘Nervous Control of the Urogenital System’. (Ed. C. A. Maggi.) pp. 103–141. (Harwood Academic Press: Chur.)
Wulff, C., Wilson, H., Wiegand, S. J., Rudge, J. S., and Fraser, H. M. (2002). Prevention of thecal angiogenesis, antral follicular growth, and ovulation in the primate by treatment with vascular endothelial growth factor trap R1R2. Endocrinology 143, 2797–2807.
| Prevention of thecal angiogenesis, antral follicular growth, and ovulation in the primate by treatment with vascular endothelial growth factor trap R1R2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltVymtL8%3D&md5=9ed60f3c2ed3adddc26e0a878dac3597CAS | 12072415PubMed |
Xu, X. J., Hao, J. X., Wiesenfeld-Hallin, Z., Håkanson, R., Folkers, K., and Hökfelt, T. (1991). Spantide II, a novel tachykinin antagonist, and galanin inhibit plasma extravasation induced by antidromic C-fiber stimulation in rat hindpaw. Neuroscience 42, 731–737.
| Spantide II, a novel tachykinin antagonist, and galanin inhibit plasma extravasation induced by antidromic C-fiber stimulation in rat hindpaw.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFWnsr8%3D&md5=02c94eb119c0f71e94bdca534194efdfCAS | 1720225PubMed |
Ziecik, A. J., Britt, H. J., and Esbenshade, K. L. (1988). Short loop feedback of estrogen-induced luteinizing hormone surge in pigs. Endocrinology 122, 1658–1662.
| Short loop feedback of estrogen-induced luteinizing hormone surge in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhvVSntLc%3D&md5=3a38717c7d89e4f10d664b794e0e78efCAS | 3126042PubMed |
Zoubina, E. V., and Smith, P. G. (2001). Sympathetic hyperinnervation of the uterus in the estrogen receptor alpha knock-out mouse. Neuroscience 103, 237–244.
| Sympathetic hyperinnervation of the uterus in the estrogen receptor alpha knock-out mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXislaqsL0%3D&md5=6a43e10bb7b93c8e1084cba4561ac171CAS | 11311804PubMed |
