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

A quantitative study of rat uterine sympathetic innervation during pregnancy and post partum

R. Chávez-Genaro A D , P. Lombide A B and G. Anesetti A C
+ Author Affiliations
- Author Affiliations

A Departamento de Histología y Embriología, Facultad de Medicina, General Flores 2125, CP 11800, Montevideo, Uruguay.

B Sección Biología Celular, Departamento de Biología Celular y Molecular, Instituto de Biología, Facultad de Ciencias, Iguá 4245, CP 11400, Montevideo, Uruguay.

C Area de Histología y Embriología, Facultad de Veterinaria, Las Places 1550, CP 11600, Montevideo, Uruguay.

D Corresponding author. Email: rchavez@fmed.edu.uy

Reproduction, Fertility and Development 18(5) 525-531 https://doi.org/10.1071/RD05053
Submitted: 9 May 2005  Accepted: 26 February 2006   Published: 16 May 2006

Abstract

In mammals, pregnancy induces a transient and extensive degeneration of uterine sympathetic innervation. We used the models of unilateral oviduct ligation and in oculo myometrium transplant in pregnant rats to address the role of stretching forces and/or hormone milieu in the loss of sympathetic innervation. The sympathetic fibres of the uterine horn and in oculo myometrial transplants were quantified on tissue sections processed by the glyoxylic acid technique. In normal pregnant rats, the density of uterine horn innervation was significantly reduced at late pregnancy and recovery took place during post partum. The empty horn of pregnant rats showed no significant changes in density of myometrial innervation during pregnancy or post partum. In oculo myometrial transplants were organotypically reinnervated in virgin animals. When the transplants were exposed to gestational hormonal milieu, few or no fibres were observed to the end of pregnancy; however, a significant increase at post partum was observed. Results showed that both the effects of stretching and the hormone milieu derived from the fetus–placenta complex play a role as inductors of changes on sympathetic myometrial innervation during pregnancy and support the idea that immature muscular uterine fibres are more susceptible to the effects of pregnancy than those originating from adult animals.

Extra keywords: sympathetic nerves, transplant, uterus.


Acknowledgments

The authors would like to thank Dr M. M. Brauer and the Cell Biology Division of the Instituto de Investigaciones Biológicas Clemente Estable (IIBCE), Montevideo, Uruguay, for access to the equipment laboratory and animal facilities.


References

Adham, H. , and Schenk, E. A. (1969). Autonomic innervation of the rat vagina, cervix and uterus and its cyclic variations. Am. J. Obstet. Gynecol. 104, 508–516.
PubMed |

Alm, P. , Lundberg, L. M. , Wharton, J. , and Polak, J. M. (1988). Effects of pregnancy on the extrinsic innervation of the guinea pig uterus. A histochemical, immunohistochemical and ultrastructural study. Histochem. J. 20, 414–426.
CrossRef | PubMed |

Bell, C. , and Malcolm, S. J. (1978). Observations of the loss of catecholamine fluorescence from intrauterine adrenergic nerves during pregnancy in the guinea pig. J. Reprod. Fertil. 73, 51–58.


Brauer, M. M. , Lincoln, J. , Blundell, D. , and Corbacho, A. (1992). Posnatal development of noradrenaline-containing nerves of the rat uterus. J. Auton. Nerv. Syst. 39, 37–50.
CrossRef | PubMed |

Brauer, M. M. , Corbacho, A. , and Burnstock, G. (1995). Effects of chronic and acute oestrogen treatment on the development of noradrenaline-containing nerves of the rat uterus. Int. J. Dev. Neurosci. 13, 791–798.
CrossRef | PubMed |

Brauer, M. M. , Burnstock, G. , Thrasivoulou, C. , and Cowen, T. (1998). In oculo transplants of myometrium from postpartum guinea pigs fail to support sympathetic reinnervation. J. Anat. 193, 509–517.
CrossRef | PubMed |

Brauer, M. M. , Llodra, J. , Scorza, C. , Chávez-Genaro, R. , Burnstock, G. , Thrasivoulou, C. , and Cowen, T. (1999). Differential effects of prepubertal chronic estrogen treatment on the synthesis of noradrenaline in uterine myometrial and perivascular sympathetic nerves. Int. J. Dev. Neurosci. 17, 295–303.
CrossRef | PubMed |

Brauer, M. M. , Shockley, K. P. , Chávez-Genaro, R. , Richeri, A. , Cowen, T. , and Crutcher, K. A. (2000a). The role of NGF in pregnancy-induced degeneration and regeneration of sympathetic nerves in the guinea pig uterus. J. Auton. Nerv. Syst. 79, 19–27.
CrossRef | PubMed |

Brauer, M. M. , Chávez-Genaro, R. , Llodrá, J. , Richeri, A. , and Scorza, M. C. (2000b). Effects of chronic oestrogen treatment are not selective for uterine sympathetic nerves: a transplantation study. J. Anat. 196, 347–355.
CrossRef | PubMed |

Chávez-Genaro, R. , Crutcher, K. , Viettro, L. , Richeri, A. , Coirolo, N. , Burnstock, G. , Cowen, T. , and Brauer, M. M. (2002). Differential effects of oestrogen on developing and mature uterine sympathetic nerves. Cell Tissue Res. 308, 61–73.
CrossRef | PubMed |

de la Torre, J. C. , and Surgeon, J. W. (1976). A methodological approach to rapid and sensitive monoamine histofluorescence using a modified glyoxylic acid technique: the SPG method. Histochemistry 49, 81–93.
CrossRef | PubMed |

Haase, E. B. , Buchman, J. , Tietz, A. E. , and Schramm, L. P. (1997). Pregnancy-induced uterine neuronal degeneration in the rat. Cell Tissue Res. 288, 293–306.
CrossRef | PubMed |

Klukovits, A. , Gaspar, R. , Santha, P. , Jancso, C. , and Falkay, G. (2002). Functional and histochemical characterization of a uterine denervation process in pregnant rats. Biol. Reprod. 67, 1013–1017.
CrossRef | PubMed |

Lindzey J., and Korach K. S. (1998). Estrogen action on the female reproductive tract. In ‘Encyclopedia of Reproduction’. (Eds E. Knobil and J. D. Neill.) pp. 79–86. (Academic Press: San Diego, CA, USA.)

Lobos, E. , Gebhardt, C. , Kluge, A. , and Spanel-Borowski, K. (2005). Expression of nerve growth factor isoforms in the rat uterus during pregnancy: accumulation of precursor proNGF. Endocrinology 146, 1922–1929.
CrossRef | PubMed |

Marshall, J. M. (1981). Effects of ovarian steroids and pregnancy on adrenergic nerves of uterus and oviduct. Am. J. Physiol. 240, C165–C174.
PubMed |

Melo, R. C. , and Machado, C. R. (1993). Noradrenergic and acetylcholinesterase-positive nerve fibres of the uterus in sexually immature and cycling rats. Histochem. J. 25, 213–218.
CrossRef | PubMed |

Naves, J. F. , Vazquez, M. T. , San Jose, I. , Martinez-Almagro, A. , and Vega, J. A. (1998). Pregnancy-induced denervation of the human uterine artery correlates with local decrease of NGF and TrkA. Ital. J. Anat. Embryol. 103, 279–290.
PubMed |

Olson, L. , and Malmfors, T. (1970). Growth characteristics of adrenergic nerves in the adult rat. Acta Physiol. Scand. 348(Suppl.), 1–112.


Owman C. (1981). Pregnancy induces degenerative and regenerative changes in the autonomic innervation of the female reproductive tract. In ‘Developmental of the Autonomic Nervous System’. (Eds K. Elliot and G. Lawrenson.) Ciba Foundation Symposium 83. pp. 252–279. (Pitman Medical: London, UK.)

Owman C., and Stjernquist M. (1988). Origin, distribution and functional aspects of aminergic and peptidergic nerves in the male and female genital tracts. In ‘Handbook of Chemical Neuroanatomy’. (Eds A. Björklund, T. Hökfelt and C. Owman.) pp. 445–544. (Elsevier Science Publishers: Amsterdam, the Netherlands.)

Papka, R. E. , Cotton, J. P. , and Traurig, H. H. (1985). Comparative distribution of neuropeptide tyrosine-, vasoactive intestinal polypeptide-, and noradrenergic nerves in the reproductive tract of the female rat. Cell Tissue Res. 242, 475–490.
CrossRef | PubMed |

Robbins, A. , Sato, Y. , Hotta, H. , and Berkley, K. J. (1990). Responses of hypogastric nerve afferent fibres to uterine distension in oestrous or metaestrous rats. Neurosci. Lett. 110, 82–85.
CrossRef | PubMed |

Sporrong, B. , Alm, P. , Owman, C. , Sjöberg, N. O. , and Thorbert, G. (1981). Pregnancy is associated with extensive adrenergic nerve degeneration in the uterus. An electronmicroscopic study in the guinea pig. Neuroscience 6, 1119–1126.
CrossRef | PubMed |

Sumida, C. , and Pasqualini, J. R. (1981). Regulation of estrogen action in the uterus of the guinea-pig foetus. J. Steroid Biochem. 15, 137–143.
CrossRef | PubMed |

Thorbert, G. (1978). Regional changes in structure and function of adrenergic nerves in the guinea pig uterus during pregnancy. Acta Obstet. Gynecol. Scandinavica 79(Suppl.), 5–32.


Varol, F. , Duchemin, A. , Neff, N. , and Hadjiconstantinou, M. (2000). Nerve growth factor (NGF) and NGF mRNA change in rat uterus during pregnancy. Neurosci. Lett. 294, 58–62.
CrossRef | PubMed |

Wiesel, O. , Toth, I. E. , Boldogkoi, Z. , Hornyak, A. , Bokor, V. , Halasz, B. , and Gerendai, I. (2004). Comparison of transsynaptic viral labelling of central nervous system structures from the uterine horn in virgin, pregnant, and lactating rats. Microsc. Res. Tech. 63, 244–252.
CrossRef | PubMed |

Yamada, M. (1988). Changes in the innervation of the uterus during pregnancy and following parturition: histochemical and electron microscopic observations in the rat and man. Nippon Sanka Fujinka Gakkai Zasshi 40, 145–152.
PubMed |

Zoubina, E. V. , and Smith, P. G. (2000). Axonal degeneration and regeneration in the rat uterus during oestrous cycle. Auton. Neurosci. – Basic 84, 176–185.
CrossRef |

Zoubina, E. V. , Fan, Q. , and Smith, P. G. (1998). Variation in uterine innervation during the oestrous cycle. J. Comp. Neurol. 397, 561–571.
CrossRef | PubMed |

Zoubina, E. V. , Mize, A. L. , Alper, R. H. , and Smith, P. G. (2001). Acute and chronic oestrogen supplementation decreases uterine sympathetic innervation in ovariectomised adult virgin rats. Histol. Histopathol. 16, 989–996.
PubMed |



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