Effects of Heat Stress on Follicular Physiology in Dairy Cows

Follicular organization starts during mid-to-late fetal life with the formation of primordial follicles. The bilateral interplay between the oocyte and adjoining somatic cells during follicular growth and ovulation may be sensitive to heat stress (HS). Mechanisms giving rise to pre-ovulatory temperature gradients across reproductive tissues are mostly regulated by the pre-ovulatory follicle, and because the cooling of the gonads and genital tract depends on a counter-current transfer system of heat, HS may be considered a major factor impairing ovulation, fertilization and early embryo development. There is evidence of a long-lasting influence of HS on oogenesis and final follicular maturation. Follicular stages that are susceptible to HS have not been precisely determined. Therefore, the aim of this review was to describe the influence of HS during the staged follicular development in dairy cattle, from the activation of primordial follicles to ovulation. Some clinical prospects are also considered.

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Kisspeptin level in the aging ovary is regulated by the sympathetic nervous system

Journal of Endocrinology ◽

10.1530/joe-16-0181 ◽

2017 ◽

Vol 232 (1) ◽

pp. 97-105 ◽

Cited By ~ 12

Author(s):

Daniela Fernandois ◽

Gonzalo Cruz ◽

Eun Kyung Na ◽

Hernán E Lara ◽

Alfonso H Paredes

Keyword(s):

Adrenergic Receptor ◽

Follicular Development ◽

Sympathetic Nerves ◽

Female Rats ◽

Reproductive Aging ◽

Beta Adrenergic Receptor ◽

Beta Adrenergic ◽

Primordial Follicles ◽

Follicular Cyst

Previous work has demonstrated that the increase in the activity of sympathetic nerves, which occurs during the subfertility period in female rats, causes an increase in follicular cyst development and impairs follicular development. In addition, the increase in ovarian sympathetic activity of aged rats correlates with an increased expression of kisspeptin (KISS1) in the ovary. This increase in KISS1 could participate in the decrease in follicular development that occurs during the subfertility period. We aimed to determine whether the blockade of ovarian sympathetic tone prevents the increase in KISS1 expression during reproductive aging and improves follicular development. We performed 2 experiments in rats: (1) an in vivo blockade of beta-adrenergic receptor with propranolol (5.0 mg/kg) and (2) an ovarian surgical denervation to modulate the sympathetic system at these ages. We measured Kisspeptin and follicle-stimulating hormone receptor (FSHR) mRNA and protein levels by qRT-PCR and western blot and counted primordial, primary and secondary follicles at 8, 10 and 12 months of age. The results showed that ovarian KISS1 decreased but FSHR increased after both propranolol administration and the surgical denervation in rats of 8, 10 and 12 months of age. An increase in FSHR was related to an increase in the number of smaller secondary follicles and a decreased number of primordial follicles at 8, 10 and 12 months of age. These results suggest that intraovarian KISS1 is regulated by sympathetic nerves via a beta-adrenergic receptor and participates locally in ovarian follicular development in reproductive aging.

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Nutritional programming and the reproductive function of the offspring

Animal Production Science ◽

10.1071/an14470 ◽

2014 ◽

Vol 54 (9) ◽

pp. 1166 ◽

Cited By ~ 9

Author(s):

P. Chavatte-Palmer ◽

C. Dupont ◽

N. Debus ◽

S. Camous

Keyword(s):

Growth Retardation ◽

Intrauterine Growth Retardation ◽

Maternal Nutrition ◽

Reproductive Function ◽

Fetal Life ◽

Ample Evidence ◽

Primordial Follicles ◽

Intrauterine Growth ◽

Maternal Undernutrition ◽

Males And Females

There is ample evidence on the importance of maternal nutrition during pregnancy on fetal and offspring development. In ruminant females, the pool of oocytes is complete and definitive before birth, based on the resting reserve of primordial follicles established during fetal life, which represent the lifespan supply for the female’s fertilisable oocytes, whereas in males, although the production of spermatozoa is a continuous process throughout post-pubertal life. Sertoli cells, which play a central role in the development of a functional testis, proliferate during pre- and post-natal life, coordinating testicular development. Both male and female fertility may, therefore, be affected by the maternal environment, but studies on the effects of developmental nutritional conditions on reproductive function and fertility, both in males and females, are relatively scarce. In humans, intrauterine growth retardation has been associated with abnormal ovarian development, characterised by a decreased volume of primordial follicles in the ovarian cortical tissue in girls, and a higher incidence of cryptorchidism in boys, with subsequent low sperm counts in adulthood. Age at puberty and gonadotropin and inhibin B plasma concentrations are also affected. Animal studies suggest both in males and females that maternal undernutrition during pregnancy may affect pituitary response to GnRH and gonadal development and function, depending on the timing and magnitude of the undernutrition. Excess nutrition, which is often associated with intrauterine growth retardation in domestic species, induces effects on the onset of puberty and both testicular and ovarian function, maybe through the observed reduction in fetal growth. This review addresses the influence of maternal nutrition on offspring reproductive function using examples in humans and animals, with particular focus on ruminants.

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Regulation of Folliculogenesis by Growth Factors in Piglet Ovary Exposed Prenatally to β-Hydroxy-β-Methylbutyrate (HMB)

Annals of Animal Science ◽

10.2478/aoas-2020-0026 ◽

2020 ◽

Vol 20 (3) ◽

pp. 899-917

Author(s):

Monika Hułas-Stasiak ◽

Joanna Jakubowicz-Gil ◽

Piotr Dobrowolski ◽

Małgorzata Grzesiak ◽

Siemowit Muszyński ◽

...

Keyword(s):

Growth Factors ◽

Western Blot ◽

Follicular Development ◽

Animal Husbandry ◽

Dietary Treatment ◽

Western Blot Assay ◽

Primordial Follicles ◽

Morphological Alterations ◽

Newborn Piglets ◽

Kit Ligand

AbstractΒ-hydroxy-β-methylbutyrate (HMB) is one of the leucine metabolites with protein anabolic effects which makes it very popular among athletes. Previously, it was shown that HMB administered during the prenatal period reduced the pool of primordial follicles and increased the proportion of developing follicles in newborn piglets. This work is a further step to understand these morphological alterations. Therefore, the aim of this study was to examine the effect of prenatal HMB treatment on the expression of the Kit ligand, BMP-4, bFGF, and the IGF-1/IGF-1R system which are the main growth factors controlling follicular development. Excised ovaries from 12 newborn piglets, originated from the control (n=6) and HMB-treated (n=6) sows were used for immunohistochemical and western-blot analysis. The tested proteins were localized within egg nests and ovarian follicles. Furthermore, the western-blot assay indicated higher BMP-4, Kit ligand, and IGF-1R expression, while the level of bFGF and IGF-1 proteins decreased after HMB dietary treatment. These findings show that HMB included into sow diet can modulate the expression of growth factors and thereby alter ovarian morphology in offspring. Therefore, this study opens a discussion about the benefits and risks of the diet supplemented with HMB and its potential application in medicine and animal husbandry, and further research is necessary in this area.

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Ovarian development in intrauterine growth-retarded and normally developed piglets originating from the same litter

Reproduction ◽

10.1530/rep.0.1260249 ◽

2003 ◽

pp. 249-258 ◽

Cited By ~ 30

Author(s):

P Da Silva-Buttkus ◽

R van den Hurk ◽

ER te Velde ◽

MA Taverne

Keyword(s):

Body Weight ◽

Ovarian Development ◽

Cell Activity ◽

Follicular Development ◽

Follicle Cell ◽

Epidemiological Studies ◽

Image Analysis System ◽

Ovarian Mass ◽

Primordial Follicles ◽

Intrauterine Growth

Epidemiological studies in humans linking adult disease to growth in utero indicate that prenatal life is a critical period for the appropriate development of the reproductive axis. The aim of this study was to compare ovarian development in intrauterine growth-retarded and normally grown piglets originating from the same litter. Intrauterine growth-retarded piglets (runts) were identified on the basis of statistical analysis of the birth weight distribution within each litter. At birth, ovaries were collected from runt piglets (n=14) and their respective mean weight (normal, n=14) littermates. Ovaries were weighed and fixed, and development of ovarian germ cells was quantified in haematoxylin-eosin-stained paraffin wax sections using an image analysis system. Germ cell loss, using an in situ TdT-mediated dUTP nick-end labelling (TUNEL) assay for DNA fragmentation, and follicle cell activity, using immunohistochemistry to demonstrate vimentin, were studied in ovarian sections. At birth, body weight and absolute ovarian mass were significantly lower in runt piglets compared with their respective normally grown littermates (body weight: 733+/-38.5 versus 1530+/-39.7 g; ovarian mass: 51+/-3.0 versus 108+/-9.6 mg; P<0.001 for both). In the ovary, the proportion of nests of oogonia, the number of oocytes and TUNEL-positive cells, and the localization and intensity of vimentin immunoreactivity were not different between runt and normal littermates. However, runt piglets had more primordial follicles (268+/-18.6 versus 235+/-20.1 per mm(2) of cortex; P<0.05), fewer primary follicles (11+/-2.0 versus 20+/-3.0 per mm(2) of cortex; P<0.001) and no secondary follicles compared with normal piglets. These findings indicate that intrauterine growth retardation delayed follicular development in pig ovaries at birth.

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Heat stress diminishes gonadotropin receptor expression and enhances susceptibility to apoptosis of rat granulosa cells

Reproduction ◽

10.1530/rep.1.00502 ◽

2005 ◽

Vol 129 (4) ◽

pp. 463-472 ◽

Cited By ~ 39

Author(s):

Takashi Shimizu ◽

Izumi Ohshima ◽

Manabu Ozawa ◽

Satoko Takahashi ◽

Atsushi Tajima ◽

...

Keyword(s):

Heat Stress ◽

Granulosa Cells ◽

Follicular Fluid ◽

Follicular Development ◽

Receptor Expression ◽

Female Rats ◽

Aromatase Activity ◽

Mrna Levels ◽

Gonadotropin Receptor ◽

Estradiol Levels

Heat stress inhibits ovarian follicular development in mammalian species. We hypothesized that heat stress inhibits the function of follicular granulosa cells and suppresses follicular development. To test this, immature female rats were injected with pregnant mare serum gonadotropin (PMSG) at 48 h after the start of temperature treatment (control: 25 °C, 50% RH; heat stress: 35 °C, 70% Relative Humidity). The ovaries and granulosa cells of follicles at different developmental stages were analyzed for gonadotropin receptor levels and aromatase activity; estradiol levels were measured in follicular fluid. Before injection, heat stress diminished only the amount of FSH receptor on granulosa cells of antral follicles. During PMSG-stimulated follicular development, heat stress strongly inhibited gonadotropin receptor levels and aromatase activity in granulosa cells, and estradiol levels in the follicular fluid of early antral, antral and preovulatory follicles. To examine apoptosis and mRNA levels of bcl-2 and bax in granulosa cells, follicles harvested 48 h after PMSG injection were cultured in serum-free conditions. Heat-stressed granulosa cells showed a time-dependent increase in apoptosis. The bcl-2 mRNA levels were similar in control and heat-stressed granulosa cells; bax mRNA levels were increased in heat-stressed granulosa cells. According to these results, heat stress inhibits expression of gonadotropin receptors in granulosa cells and attenuates estrogenic activity of growing follicles, granulosa cells of heat-stressed follicles are susceptible to apoptosis, and the bcl2/bax system is not associated with heat-stress-induced apoptosis of granulosa cells. Our study suggests that decreased numbers and function of granulosa cells may cause ovarian dysfunction in domestic animals in summer.

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Climate Change and Livestock Fertility

10.4018/978-1-6684-3686-8.ch061 ◽

2022 ◽

pp. 1256-1277

Author(s):

Vishakha Shrimali ◽

Nibedita Naha ◽

Sukanta Mondal

Keyword(s):

Climate Change ◽

Heat Stress ◽

Greenhouse Gases ◽

Follicular Development ◽

Mitigation Strategies ◽

Adaptation To Climate Change ◽

Oocyte Competence ◽

Livestock Sector ◽

Negative Effect ◽

Global Threat

Climate change is a global threat to livestock sector to so many species and ecosystem in different parts of the world. Climate change, heat stress, and nutritional stress are the major intriguing factors responsible for reduced fertility in farm animals in tropical countries. Heat and nutritional stresses affect the reproductive performance by decreasing the expression of estrous behavior, altering ovarian follicular development and hormonal profiles, compromising oocyte competence, and inhibiting embryonic development in livestock. Climate is changed by greenhouse gases that released into atmosphere through man-made activities. Livestock contribute 18% of the production of greenhouse gases itself and causes climate change including heat stress, which has direct and indirect impact on fertility of the animals as well as reduce milk production. Adaptation to climate change and lowering its negative effect by alteration of animal micro-environment using different essential technologies are the main mitigation strategies to recover heat stress damage in this respect.

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Pentachloronitrobenzene alters progesterone production and primordial follicle recruitment in cultured granulosa cells and rat ovary†

Biology of Reproduction ◽

10.1093/biolre/ioz195 ◽

2019 ◽

Vol 102 (2) ◽

pp. 511-520

Author(s):

Yanrong Kuai ◽

Xiaobo Gao ◽

Huixia Yang ◽

Haiyan Luo ◽

Yang Xu ◽

...

Keyword(s):

Protein Kinase ◽

Granulosa Cells ◽

Crop Production ◽

Follicular Development ◽

Mitogen Activated Protein Kinase ◽

Dependent Manner ◽

Serum Progesterone ◽

Primordial Follicles ◽

Progesterone Production

Abstract Pentachloronitrobenzene (PCNB) is an organochlorine fungicide widely used for crop production and has become an environmental concern. Little is known about the effect of PCNB on ovarian steroidogenesis and follicular development. We found that PCNB stimulated Star expression and progesterone production in cultured rat granulosa cells in a dose-dependent manner. PCNB activated mitogen-activated protein kinase (MAPK3/1) extracellulat regulated kinase (ERK1/2), thus inhibition of either protein kinase A (PKA) or MAPK3/1 signaling pathway significantly attenuated progesterone biosynthesis caused by PCNB, suggesting that PCNB induced progesterone production by activating the cyclic adenosine monophosphate (cAMP/PKA) and MAPK3/1 signaling pathways. Further investigation demonstrated that PCNB induced Star expression and altered MAPK3/1 signaling in ovary tissues of immature SD rats treated with PCNB at the dose of 100, 200, or 300 mg/kg by daily gavage for 7 days, while serum progesterone level was dose-dependently decreased. We demonstrated that PCNB exposure accelerated the recruitment of primordial follicles into the growing follicle pool in ovary tissues, accompanied by increased levels of anti-Mullerian hormone (AMH) in both ovary tissues and serum. Taken together, our data demonstrate for the first time that PCNB stimulated Star expression, altered MAPK3/1 signaling and progesterone production in vivo and in vitro, and accelerated follicular development with a concomitant increase in AMH in ovary tissues and serum. Our findings provide novel insight into the toxicity of PCNB to animal ovary function.

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In vitro development of mouse fetal germ cells into mature oocytes

Reproduction ◽

10.1530/rep-06-0378 ◽

2007 ◽

Vol 134 (2) ◽

pp. 223-231 ◽

Cited By ~ 30

Author(s):

Wei Shen ◽

Lan Li ◽

Zhaodai Bai ◽

Qingjie Pan ◽

Mingxiao Ding ◽

...

Keyword(s):

Genomic Imprinting ◽

Germ Cells ◽

Follicular Development ◽

Germinal Vesicle ◽

Germinal Vesicle Breakdown ◽

Primordial Follicles ◽

Ovarian Cells ◽

Fetal Mice ◽

Vitro Development

Little is known about the mechanisms underlying primordial follicular formation and the acquisition of competence to resume meiosis by growing oocytes. It is therefore important to establish anin vitroexperimental model that allows one to study such mechanisms. Mouse follicular development has been studiedin vitroover the past several years; however, no evidence has been presented showing that mature oocytes can be obtained from mouse fetal germ cells prior to the formation of primordial follicles. In this study, a method has been established to obtain mature oocytes from the mouse fetal germ cells at 16.5 days postcoitum (dpc). From the initiation of primordial follicular formation to the growth of early secondary follicles, ovarian tissues from 16.5 dpc fetal mice were culturedin vitrofor 14 days. Subsequently, 678 intact secondary follicles were isolated from 182 mouse fetal ovaries and cultured for 12 days. A total of 141 oocytes inside antral follicles were maturedin vitro, and 102 oocytes underwent germinal vesicle breakdown. We found that 97 oocytes were fertilized and 15 embryos were able to form morula–blastocysts. We also analyzed various genomic imprinting markers and showed that the erasure of genomic imprinting markers in the parental generation was also imposed on the oocytes that developed from fetal germ cells. Our results demonstrate that mouse fetal germ cells are able to form primordial follicles with ovarian cells, and that oocytes within the growing follicles are able to mature normallyin vitro.

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Follicular dynamics and secretion of inhibin and oestradiol-17β during the oestrous cycle of the hamster

Journal of Endocrinology ◽

10.1677/joe.0.1460169 ◽

1995 ◽

Vol 146 (1) ◽

pp. 169-176 ◽

Cited By ~ 30

Author(s):

H Kishi ◽

K Taya ◽

G Watanabe ◽

S Sasamoto

Keyword(s):

Plasma Levels ◽

Marked Decrease ◽

Plasma Concentrations ◽

Follicular Development ◽

Chorionic Gonadotrophin ◽

Human Chorionic Gonadotrophin ◽

Oestrous Cycle ◽

Antral Follicles ◽

Follicular Maturation ◽

Follicular Dynamics

Abstract Plasma and ovarian levels of inhibin were determined by a radioimmunoassay (RIA) at 3-h intervals throughout the 4-day oestrous cycle of hamsters. Plasma concentrations of FSH, LH, progesterone, testosterone and oestradiol-17β were also determined by RIAs. In addition, hamsters were injected at various times with human chorionic gonadotrophin (hCG) to determine the follicular development. The changes in plasma concentrations of FSH after injection of antisera to oestradiol-17β (oestradiol-AS) and inhibin (inhibin-AS) on the morning of day 2 (day 1=day of ovulation) were also determined. Plasma concentrations of inhibin showed a marked increase on the afternoon of day 1, remained at plateau levels until the morning of day 4, then increased abruptly on the afternoon of day 4 when preovulatory LH and FSH surges were initiated. A marked decrease in plasma concentrations of inhibin occurred during the process of ovulation after the preovulatory gonadotrophin surges. An inverse relationship between plasma levels of FSH and inhibin was observed when the secondary surge of FSH was in progress during the periovulatory period. Plasma concentrations of oestradiol-17β showed three increase phases and these changes differed from those of inhibin. Changes in plasma concentrations of oestradiol-17β correlated well with the maturation and regression of large antral follicles. Follicles capable of ovulating following hCG administration were first noted at 2300 h on day 1. The number of follicles capable of ovulating reached a maximum on the morning of day 3 (24·8± 0·6), and decreased by 0500 h on day 4 (15·0 ± 1·1), corresponding to the number of normal spontaneous ovulations. Plasma concentrations of FSH were dramatically increased within 6 h after inhibin-AS, though no increase in FSH levels was observed after oestradiol-AS. These findings suggest that changes in the plasma levels of inhibin during the oestrous cycle provide a precise indicator of follicular recruitment, and that the changes in plasma concentrations of oestradiol-17β are associated with follicular maturation. These findings also suggest that inhibin may play a major role in the inhibition of FSH secretion during the oestrous cycle of the hamster. Journal of Endocrinology (1995) 146, 169–176

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