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Endocrine and Paracrine Regulation of Birth at Term and Preterm¹

Departments of Physiology (J.R.G.C., S.G.M., W.G., S.J.L.) and of Obstetrics and Gynaecology (J.R.G.C., S.G.M., S.J.L.), University of Toronto, Toronto, Ontario, Canada M55 1A8; Program in Development and Fetal Health (J.R.G.C., S.J.L.), Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada M5G 1X5; MRC Group in Fetal and Neonatal Health and Development (J.R.G.C., S.J.L.); Department of Obstetrics and Gynaecology, and Cellular and Molecular Medicine (W.G.), University of Ottawa, Ottawa, Ontario, Canada K1H 8L6

We have examined factors concerned with the maintenance of uterine quiescence during pregnancy and the onset of uterine activity at term in an animal model, the sheep, and in primate species. We suggest that in both species the fetus exerts a critical role in the processes leading to birth, and that activation of the fetal hypothalamic-pituitary-adrenal axis is a central mechanism by which the fetal influence on gestation length is exerted. Increased cortisol output from the fetal adrenal gland is a common characteristic across animal species. In primates, there is, in addition, increased output of estrogen precursor from the adrenal in late gestation. The end result, however, in primates and in sheep is similar: an increase in estrogen production from the placenta and intrauterine tissues. We have revised the pathway by which endocrine events associated with parturition in the sheep come about and suggest that fetal cortisol directly affects placental PGHS expression. In human pregnancy we suggest that cortisol increases PGHS expression, activity, and PG output in human fetal membranes in a similar manner. Simultaneously, cortisol contributes to decreases in PG metabolism and to a feed-forward loop involving elevation of CRH production from intrauterine tissues. In human pregnancy, there is no systemic withdrawal of progesterone in late gestation. We have argued that high circulating progesterone concentrations are required to effect regionalization of uterine activity, with predominantly relaxation in the lower uterine segment, allowing contractions in the fundal region to precipitate delivery. This new information, arising from basic and clinical studies, should further the development of new methods of diagnosing the patient at risk of preterm labor, and the use of scientifically based strategies specifically for the management of this condition, which will improve the health of the newborn.

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				J. C. Havelock, P. Keller, N. Muleba, B. A. Mayhew, B. M. Casey, W. E. Rainey, and R. A. Word Human Myometrial Gene Expression Before and During Parturition Biol Reprod, March 1, 2005; 72(3): 707 - 719. [Abstract] [Full Text] [PDF]

				C. E. Wood Estrogen/Hypothalamus-Pituitary-Adrenal Axis Interactions in the Fetus: the Interplay Between Placenta and Fetal Brain Reproductive Sciences, February 1, 2005; 12(2): 67 - 76. [Abstract] [PDF]

				M. Elmes, L. R. Green, K. Poore, J. Newman, D. Burrage, D. R. E. Abayasekara, Z. Cheng, M. A. Hanson, and D. C. Wathes Raised dietary n-6 polyunsaturated fatty acid intake increases 2-series prostaglandin production during labour in the ewe J. Physiol., January 15, 2005; 562(2): 583 - 592. [Abstract] [Full Text] [PDF]

				B G White, S J Williams, K Highmore, and D J MacPhee Small heat shock protein 27 (Hsp27) expression is highly induced in rat myometrium during late pregnancy and labour Reproduction, January 1, 2005; 129(1): 115 - 126. [Abstract] [Full Text] [PDF]

				S. D. Tardif, T. E. Ziegler, M. Power, and D. G. Layne Endocrine Changes in Full-Term Pregnancies and Pregnancy Loss Due to Energy Restriction in the Common Marmoset (Callithrix jacchus) J. Clin. Endocrinol. Metab., January 1, 2005; 90(1): 335 - 339. [Abstract] [Full Text] [PDF]

				V. Kumarasamy, M. D. Mitchell, F. H. Bloomfield, M. H. Oliver, M. E Campbell, J. R. G. Challis, and J. E. Harding Effects of periconceptional undernutrition on the initiation of parturition in sheep Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2005; 288(1): R67 - R72. [Abstract] [Full Text] [PDF]

				F. H. Bloomfield, M. H. Oliver, P. Hawkins, A. C. Holloway, M. Campbell, P. D. Gluckman, J. E. Harding, and J. R. G. Challis Periconceptional Undernutrition in Sheep Accelerates Maturation of the Fetal Hypothalamic-Pituitary-Adrenal Axis in Late Gestation Endocrinology, September 1, 2004; 145(9): 4278 - 4285. [Abstract] [Full Text] [PDF]

				S. Bittrich, C. Philipona, H. M. Hammon, V. Rome, P. Guilloteau, and J. W. Blum Preterm as Compared with Full-Term Neonatal Calves Are Characterized by Morphological and Functional Immaturity of the Small Intestine J Dairy Sci, June 1, 2004; 87(6): 1786 - 1795. [Abstract] [Full Text] [PDF]

				B.S.J. Yuen, P.C. Owens, M.E. Symonds, D.H. Keisler, J.R. McFarlane, K.G. Kauter, and I.C. McMillen Effects of Leptin on Fetal Plasma Adrenocorticotropic Hormone and Cortisol Concentrations and the Timing of Parturition in the Sheep Biol Reprod, June 1, 2004; 70(6): 1650 - 1657. [Abstract] [Full Text] [PDF]

				J. C. Condon, P. Jeyasuria, J. M. Faust, and C. R. Mendelson Surfactant protein secreted by the maturing mouse fetal lung acts as a hormone that signals the initiation of parturition PNAS, April 6, 2004; 101(14): 4978 - 4983. [Abstract] [Full Text] [PDF]

				M. A. Kutzler, E. K Ruane, T. Coksaygan, S. E. Vincent, and P. W. Nathanielsz Effects of Three Courses of Maternally Administered Dexamethasone at 0.7, 0.75, and 0.8 of Gestation on Prenatal and Postnatal Growth in Sheep Pediatrics, February 1, 2004; 113(2): 313 - 319. [Abstract] [Full Text] [PDF]

				J. W. Ward, F. B. P. Wooding, and A. L. Fowden Ovine feto-placental metabolism J. Physiol., January 15, 2004; 554(2): 529 - 541. [Abstract] [Full Text] [PDF]

				H.A. Rodriguez, L. Kass, J. Varayoud, J.G. Ramos, H.H. Ortega, M. Durando, M. Munoz-de-Toro, and E.H. Luque Collagen remodelling in the guinea-pig uterine cervix at term is associated with a decrease in progesterone receptor expression Mol. Hum. Reprod., December 1, 2003; 9(12): 807 - 813. [Abstract] [Full Text] [PDF]

				K. Sun and L. Myatt Enhancement of Glucocorticoid-Induced 11{beta}-Hydroxysteroid Dehydrogenase Type 1 Expression by Proinflammatory Cytokines in Cultured Human Amnion Fibroblasts Endocrinology, December 1, 2003; 144(12): 5568 - 5577. [Abstract] [Full Text] [PDF]

				R. Marttila, R. Haataja, S. Guttentag, and M. Hallman Surfactant Protein A and B Genetic Variants in Respiratory Distress Syndrome in Singletons and Twins Am. J. Respir. Crit. Care Med., November 15, 2003; 168(10): 1216 - 1222. [Abstract] [Full Text] [PDF]

				M. I. Muniz-Junqueira, L. M. F. Pecanha, V. L. da Silva-Filho, M. C. de Almeida Cardoso, and C. E. Tosta Novel Microtechnique for Assessment of Postnatal Maturation of the Phagocytic Function of Neutrophils and Monocytes Clin. Vaccine Immunol., November 1, 2003; 10(6): 1096 - 1102. [Abstract] [Full Text] [PDF]

				M. Mlynarczyk, T. Imamura, H. Umezaki, K.M. Kaushal, L. Zhang, and C.A. Ducsay Long-Term Hypoxia Changes Myometrial Responsiveness and Oxytocin Receptors in the Pregnant Ewe: Differential Effects on Longitudinal Versus Circular Smooth Muscle Biol Reprod, November 1, 2003; 69(5): 1500 - 1505. [Abstract] [Full Text] [PDF]