Sensory denervation with capsaicin reduces ovarian follicular development and delays the onset of puberty in guinea pigs

DOI: 10.4236/arsci.2013.13005   PDF   HTML   XML   3,843 Downloads   8,095 Views   Citations

Abstract

Introduction: It has been documented that mammalian ovaries receive sympathetic, parasympathetic and sensory nerve fibers. The aim of this work was to investigate the effects of sensory denervation with capsaicin at the first vaginal opening (FVO) on follicular development and the expression of TRPV1 receptors in ovary cells as well as in the dorsal root ganglia (DRGs) and lumbar dorsal spinal cord neurons of guinea pigs. The DRGs and lumbar dorsal spinal cord neurons serve as a nerve connection from the ovaries to the CNS. Materials and Methods: Female guinea pigs received a subcutaneous injection of capsaicin (30 mM) at 10 days of age (P10), while control animals were injected with vehicle. Using light microscopy, we counted healthy preantral follicles (HPF), healthy antral follicles (HAF), atretic preantral follicles (APF), and atretic antral follicles (AAF) in the ovaries at the FVO, and the numbers of TRPV1-positive cells were counted in the ovarian follicles, DRGs, and lumbar dorsal spinal cord (L2-L4) neurons by immunohistochemistry. Results: Guinea pigs treated with capsaicin showed a significant delay of FVO in comparison with the control animals (36 vs. 44 days). In the ovaries, the number of preantral and antral follicles decreased significantly. Additionally, the number of TRPV1-positive thecainterstitial cells of the antral follicles was reduced significantly, and the number of TRPV1-positive neurons in the DRGs and lumbar dorsal spinal cord (L2-L4) decreased. Thus, we showed that TRPV1 receptors throughout the sensory fibers modulate ovarian follicular development and the onset of puberty in guinea pigs. Conclusion: Sensory denervation decreases ovarian follicular development and delays the onset of puberty of guinea pigs. Our data support the idea that through TRPV1 receptors, ovarian afferent fibers sense local stimuli that are sent to the CNS.

Share and Cite:

Alatriste, V. , Herrera-Camacho, I. , I. Martínez, M. , D. Limón, I. , González-Flores, O. and Luna, F. (2013) Sensory denervation with capsaicin reduces ovarian follicular development and delays the onset of puberty in guinea pigs. Advances in Reproductive Sciences, 1, 29-37. doi: 10.4236/arsci.2013.13005.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Burden, H.W., Leonard, M., Smith, C.O. and Lawrence Jr. I.E. (1983) The sensory innervation of the ovary: A horseradish peroxidase study in the rat. Anatomical Record, 207, 623-627. http://dx.doi.org/10.1002/ar.1092070410
[2] Klein, C.M. and Burden, H.W. (1988) Anatomical localization of afferent and postganglionic sympathetic neurons innervating the ovary. Neuroscience Letters, 85, 217- 222. http://dx.doi.org/10.1016/0304-3940(88)90354-0
[3] Gerendai, I., Tóth, I.E., Boldogk?i, Z., Medveczky, I. and Halász, B. (2000) CNS structures presumably involved in vagal control of ovarian function. Journal of the Autonomic Nervous System, 80, 40-45. http://dx.doi.org/10.1016/S0165-1838(00)00071-0
[4] Burden, H.W. and Zary, J.T. (2002) Localization of calretinin in the rat ovary and in relation to nerve cell bodies in dorsal root and paravertebral ganglia projecting to the ovary. Microscopy Research and Technique, 59, 490-494. http://dx.doi.org/10.1002/jemt.10226
[5] Jana, B., Lata, M., Bulc, M. and Ca?ka, J. (2012) Long term estradiol-17β administration changes population of the dorsal root ganglia neurons innervating the ovary in the sexually mature gilts. Neuropeptides, 46, 157-165. http://dx.doi.org/10.1016/j.npep.2012.05.001
[6] Majewski, M., Sienkiewicz, W., Kaleczyc, J., Mayer, B., Czaja, K. and ?akomy, M. (1995) The distribution and co-localization of imunoreactivity to nitric oxide synthase, vasoactive intestinal polypeptide and substance P within nerve fibres supplying bovine and porcine genital organs. Cell and Tissue Research, 281, 445-464. http://dx.doi.org/10.1007/BF00417862
[7] Shadiack, A.M., Sun, Y. and Zigmod, R.E. (2001) Nerve growth factor antiserum induces axotomy-like changes in neuropeptide expression in intact sympathetic and sensory neurons. The Journal of Neuroscience, 21, 363-371.
[8] Lara, H.E., Hill, D.F., Katz, K.H. and Ojeda, S.R. (1990) The gene encoding nerve growth factor is expressed in the immature rat ovary: Effect of denervation and hormo- nal treatment. Endocrinology, 126, 357-363. http://dx.doi.org/10.1210/endo-126-1-357
[9] Gerendai, I. and Halász, B. (1997) Neuroendocrine asymmetry. Frontiers in Neuroendocrinology, 18, 354-381. http://dx.doi.org/10.1006/frne.1997.0154
[10] Kim, J.C., Kim, D.B., Seo, S.I., Park, Y.H. and Hwang, T.K. (2004) Nerve growth factor and vanilloid receptor expression, and detrusor instability, after relieving bladder outlet obstruction in rats. BJU International, 94, 915-918. http://dx.doi.org/10.1111/j.1464-4096.2003.05059.x
[11] Dissen, G.A., Hill, D.F., Costa, M.E., Dees, W.L., Lara, H.E. and Ojeda, S.R. (1996) A role for trkA nerve growth factor receptors in mammalian ovulation. Endocrinology, 137, 198-209. http://dx.doi.org/10.1210/en.137.1.198
[12] Dissen, G.A., Lara, H.E., Leyton, V., Paredes, A., Hill, D.F., Costa, M.E., et al. (2000) Intraovarian excess of nerve growth factor increases androgen secretion and disrupts estrous cyclicity in the rat. Endocrinology, 141, 1073-1082. http://dx.doi.org/10.1210/en.141.3.1073
[13] Lara, H.E., Dissen, G.A., Leyton, V., Paredes, A., Fuenzalida, H., Fiedler, J.L., et al. (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. http://dx.doi.org/10.1210/en.141.3.1059
[14] Lara, H.E., McDonald, J.K. and Ojeda, S.R. (1990) Involvement of nerve growth factor in female sexual development. Endocrinology, 126, 364-375. http://dx.doi.org/10.1210/endo-126-1-364
[15] Urbán, L., Willetts, J., Randi?, M. and Papka, R.E. (1985) The acute and chronic effects of capsaicin on slow excitatory transmission in rat dorsal horn. Brain Research, 330, 390-396. http://dx.doi.org/10.1016/0006-8993(85)90705-X
[16] Morán, C., Morales, L., Razo, R.S., Apolonio, J., Quiróz, U., Chavira R, et al. (2003) Effects of sensorial denervation induced by capsaicin injection at birth or on day three of life, on puberty, induced ovulation and pregnancy. Life Science, 73, 2113-2125. http://dx.doi.org/10.1016/S0024-3205(03)00598-8
[17] Trujillo, A., Morales, L., Vargas, X., Alba, L. and Domínguez, R. (2004) Effects of capsaicin treatment on the regulation of ovarian compensatory hypertrophy and compensatory ovulation. Endocrine, 25, 155-162. http://dx.doi.org/10.1385/ENDO:25:2:155
[18] Dissen, G.A., Hill, D.F., Costa, M.E., Ma, Y.J. and Ojeda, S.R. (1991) Nerve growth factor receptors in the peripubertal rat ovary. Molecular Endocrinology, 5, 1642-1650. http://dx.doi.org/10.1210/mend-5-11-1642
[19] Calka, J., McDonald, J. K. and Ojeda, S.R. (1988) The innervation of the immature rat ovary by calcitonin generelated peptide. Biology of Reproduction, 39, 1215-1223. http://dx.doi.org/10.1095/biolreprod39.5.1215
[20] Koz?owska, A., Wojtkiewicz, J., Majewski, M. and Jana, B. (2011) Localization of substance P, calcitonin gene related peptide and galanin in the nerve fibers of porcine cystic ovaries. Folia Histochemica et Cytobiologica, 49, 622-630.
[21] Tokushige, N., Russell, P. and Black, K. (2010) Nerve fibers in ovarian endometriomas. Fertility Sterility, 94, 1944-1947. http://dx.doi.org/10.1016/j.fertnstert.2009.12.074
[22] Yu, S.Q. and Wang, D.H. (2011) Intrathecal injection of TRPV1 shRNA leads to increases in blood pressure in rats. Acta Physiologica (Oxford England), 203, 139-147. http://dx.doi.org/10.1111/j.1748-1716.2011.02285.x
[23] Liu, J., Liu, X., Duan, K., Zhang, Y. and Guo, S.W. (2012) The expression and functionality of transient receptor potential vanilloid 1 in ovarian endometriomas. Reproductive Sciences, 19, 1110-1124. http://dx.doi.org/10.1177/1933719112443876
[24] Dawson, L.F., Phillips, J.K., Finch, P.M., Inglis, J.J. and Drummond, P.D. (2011) Expression of α1-adrenoceptors on peripheral nociceptive neurons. Neuroscience, 175, 300- 314. http://dx.doi.org/10.1016/j.neuroscience.2010.11.064
[25] Christianson, J.A., Traub, R.J. and Davis, B.M. (2006) Differences in spinal distribution and neurochemical phenotype of colonic afferents in mouse and rat. The Journal of Comparative Neurology, 494, 246-259. http://dx.doi.org/10.1002/cne.20816
[26] Ji, R.R., Samad, T.A., Jin, S.X., Schmoll, R. and Woolf, C.J. (2002) p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron, 36, 57-68. http://dx.doi.org/10.1016/S0896-6273(02)00908-X
[27] Bonnington, J.K. and McNaughton, P.A. (2003) Signalling pathways involved in the sensitisation of mouse nociceptive neurones by nerve growth factor. The Journal of Physiology, 551, 433-446. http://dx.doi.org/10.1113/jphysiol.2003.039990
[28] Gopinath, P., Wan, E., Holdcroft, A., Facer, P., Davis, J.B., Smith, G.D., et al. (2005) Increased capsaicin receptor TRPV1 in skin nerve fibres and related vanilloid recaptors TRPV3 and TRPV4 in keratinocytes in human breast pain. BMC Womens Health, 5, 2. http://dx.doi.org/10.1186/1472-6874-5-2
[29] Tingaker, B.K., Ekman-Ordeberg, G., Facer, P., Irestedt, L. and Anand, P. (2008) Influence of pregnancy and labor on the occurrence of nerve fibers expressing the capsaicin receptor TRPV1 in human corpus and cervix uteri. Reproductive Biology and Endocrinology: RB&E, 6, 8. http://dx.doi.org/10.1186/1477-7827-6-8
[30] Alatriste, V., Herrera-Camacho, I., Torres-Soto, M., Gomez-Camarillo, M.A., Gonzalez-Flores, O., Limon, I.D., et al. (2011) Differential development of TRPV1-expressing reproductive gland and sensory nerves; ovary, dorsal root ganglion, and lumbar spinal cord of the guinea pig. Neuroscience Meeting, Washington DC.
[31] Kroemer, G., ElDeiry, W.S., Golstein, P., Peter, M.E., Vaux, D., Vandenabeele, P., et al. (2005) Classification of cell death: Recommendations of the Nomenclature Committee on Cell Death. Cell Death and Differentiation, 12, 1463-1467. http://dx.doi.org/10.1038/sj.cdd.4401724
[32] Wang, W., Liu, H.L., Tian, W., Zhang, F.F., Gong, Y., Chen, J.W., et al. (2010) Morphologic observation and classification criteria of atretic follicles in guinea pigs. Journal of Zhejiang University, Science B, 11, 307-314. http://dx.doi.org/10.1631/jzus.B0900391
[33] Metz, W. and Forssmann, W.G. (1980) Innervation of the liver in guinea pig and rat. Anatomy and Embryology, 160, 239-252. http://dx.doi.org/10.1007/BF00305105
[34] Nikkinen, A., Uusitalo, H., Lehtosalo, J.I. and Palkama, A. (1985) Distribution of adrenergic nerves in the lacrimal glands of guinea-pig and rat. Experimental Eye Research, 40, 751-756. http://dx.doi.org/10.1016/0014-4835(85)90144-7
[35] Birmingham, A.T. (1970) Sympathetic denervation of the smooth muscle of the vas deferens. The Journal of Physiology, 206, 645-661.
[36] Dissen, G.A., Hirshfield, A.N., Malamed, S. and Ojeda, S.R. (1995) Expression of neurotrophins and their recaptors in the mammalian ovary is developmentally regulated: Changes at the time of folliculogenesis. Endocrinology, 136, 4681-4692. http://dx.doi.org/10.1210/en.136.10.4681
[37] Romero, C., Paredes, A., Dissen, G.A. and Ojeda S.R. (2002) Nerve growth factor induces the expression of functional FSH receptors in newly formed follicles of the rat ovary. Endocrinology, 143, 1485-1494. http://dx.doi.org/10.1210/en.143.4.1485
[38] Teerds, K.J. and Dorrington, J.H. (1993) Immunohisto-chemical localization of 3 beta-hydroxysteroid dehydrogenase in the rat ovary during follicular development and atresia. Biology of Reproduction, 49, 989-996. http://dx.doi.org/10.1095/biolreprod49.5.989
[39] Kumazawa, T. and Perl, E.R. (1978) Excitation of marginal and substantia gelatinosa neurons in the primate spinal cord: Indications of their place in dorsal horn functional organization. The Journal of Comparative Neurology, 177, 417-434. http://dx.doi.org/10.1002/cne.901770305
[40] Yoshimura, M. and Jessell, T.M. (1989) Primary afferent-evoked synaptic responses and slow potential generation in rat substantia gelat-inosa neurons in vitro. Journal of Neurophysiology, 62, 96-108.
[41] Fonseca, B.M., Correia-da-Silva, G., Taylor, A.H., Konje, J.C., Bell, S.C. and Teixeira, N.A. (2009) Spatio-temporal expression patterns of anandamide-binding receptors in rat implantation sites: evidence for a role of the endocannabinoid system during the period of placental development. Reproductive Biology and Endocrinology, 7, 121. http://dx.doi.org/10.1186/1477-7827-7-121
[42] Giannantoni, A., Conte, A., Farfariello, V., Proietti, S., Vianello, A., Nardicchi, V., et al. (2013) Onabotulinumtoxin-A intradetrusorial injections modulate bladder expression of NGF, TrkA, p75 and TRPV1 in patients with detrusor overactivity. Pharmacological Research, 68, 118-124. http://dx.doi.org/10.1016/j.phrs.2012.11.009
[43] Leonelli, M., Martins, D.O. and Britto, L.R. (2011) TRPV1 receptors modulate retinal development. International Journal of Developmental Neuroscience, 29, 405- 413. http://dx.doi.org/10.1016/j.ijdevneu.2011.03.002
[44] Martin, E., Dahan, D., Cardouat, G., Gillibert-Duplantier, J., Marthan, R., Savineau, J.P., et al. (2012) Involvement of TRPV1 and TRPV4 channels in migration of rat pulmonary arterial smooth muscle cells. Pflügers Archiv, 464, 261-272. http://dx.doi.org/10.1007/s00424-012-1136-5
[45] Kobayashi, K., Fukuoka, T., Obata, K., Yamanaka, H., Dai, Y., Tokunaga, A., et al. (2005) Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. The journal of comparative neurology, 493, 596-606. http://dx.doi.org/10.1002/cne.20794
[46] Jankowski, M.P. and Koerber, H.R. (2010) Neurotrophic factors and nociceptor sensitization. In: Kruger, L. and Light, A.R., Eds., Translational Pain Research: From Mouse to Man, CRC Press, Boca Raton. http://www.ncbi.nlm.nih.gov/books/NBK57265/
[47] Donnerer, J., Liebmann, I. and Schicho, R. (2005) Differential regulation of 3-beta-hydroxysteroid dehydrogenase and vanilloid receptor TRPV1 mRNA in sensory neurons by capsaicin and NGF. Pharmacology, 73, 97-101. http://dx.doi.org/10.1159/000081625
[48] Obreja, O., Ring-kamp, M., Turnquist, B., Hirth, M., Forsch, E., Rukwied, R., et al. (2011) Nerve growth factor selectively decreases activity-dependent conduction slowing in mechano-insensitive Cnociceptors. Pain, 152, 2138-2146. http://dx.doi.org/10.1016/j.pain.2011.05.021
[49] Li, D., Ren, Y., Xu, X., Zou, X., Fang, L. and Lin, Q. (2008) Sensitization of primary afferent nociceptors induced by intradermal capsaicin involves the peripheral release of calcitonin generelated Peptide driven by dorsal root reflexes. Journal of Pain, 9, 1155-1168. http://dx.doi.org/10.1016/j.jpain.2008.06.011
[50] Ye, Y., Dang, D., Zhang, J., Viet, C.T., Lam, D.K., Dolan, J.C., et al. (2011) Nerve growth factor links oral cancer progression, pain, and cachexia. Molecular Cancer Therapeutics, 10, 1667-1676. http://dx.doi.org/10.1158/1535-7163.MCT-11-0123

  
comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.