Elsevier

Theriogenology

Volume 130, May 2019, Pages 103-110
Theriogenology

Oocyte quality and heat shock proteins in oocytes from bovine breeds adapted to the tropics under different conditions of environmental thermal stress

https://doi.org/10.1016/j.theriogenology.2019.02.039Get rights and content

Abstract

In order to evaluate the influence of thermal stress on physiological parameters, and the oocyte quality of Girolando (n = 12) and adapted Pantaneira (n = 12) cattle, twelve sessions of ultrasound guided follicular aspiration (OPU) were performed, between January and November 2014 (during dry (May–September) and rainy season (October–April) in Brazil). The recovered cumulus-oocyte complexes (COCs) were selected and classified, according to quality, immediately after OPU. The oocytes were then stored in 3% paraformaldehyd before conducting immunofluorescence analysis under confocal microscopy to identify HSP70 and 90 proteins. Before each OPU session, the rectal temperature (RT) and respiratory frequency (RF) of each animal were measured. The black globe humidity index (BGHI) was calculated on the day of the OPUs and 90 days before each OPU session, and related to the thermal stress of the animals. The quality of oocytes from Girolando cattle, but not Pantaneira, showed a negative relationship with BGHI of 90 days before OPU. RT of both breeds did not exceed normal values for cattle below BGHI 95. BGHI variation on the day of OPU did not affect RF of the adapted Pantaneira breed (p = 0.3221). On the other hand, Girolando cattle showed a positive relationship between RF and BGHI (p = 0.0103). With increasing BGHI, the amount of HSP70 increased in Girolando oocytes, however, decreased in the Pantaneira breed. We have not observed a relationship between HSP 90 and BGHI, however Girolando cattle produced a greater amount of this protein in relation to the Pantaneira breed. In conclusion, higher BGHIs, 90 days before OPU session, negatively affect oocyte quality of Girolando cattle and positively affect oocyte quality of the Pantaneira breed. Higher BGHIs on the day of the OPU session negatively affected the respiratory frequency of the Girolando breed, and lead to a higher recruitment of HSP70 to protect oocyte maturation. The opposite pattern was observed for Pantaneira. In addition, Pantaneira cattle produced twice as much as HSP70 as Girolando cattle, suggesting that a natural higher production of this protein could be involved in the mechanisms of adaptation to heat conditions.

Introduction

Cattle are homeothermic animals, maintaining a constant body temperature through heat flow, determined by processes that depend on the temperature and humidity of the environment. When animals are in the thermoneutral zone (TZ), physiological imbalances are minimal, and productivity is increased. However, the understanding of the relationship between animals and their interactions with the environment becomes difficult to evaluate, due to the intrinsic characteristics of each animal, such as breed, age and sex [1].

One way to measure environmental parameters (i.e., temperature and humidity), is the black globe humidity index (BGHI). This index considers the effects of dry bulb temperature, humidity and air movement, and the radiation level in a single value. BGHI is the preferred index for investigating the impact of environmental factors on grazing animals [2]. The resulting values can be interpreted as comfort or stress, and depending on the stress intensity, thermal discomfort can be rated as alert, dangerous or critical [2].

High humidity combined with high temperatures leads to changes in the physiological behavior of the animal, which promotes greater energy expenditure to maintain its homeostasis [3], interfering with food consumption [[4], [5], [6]], weight gain [7], milk production [5,8], and reproductive rates [9,10]. These may influence folliculogenesis, oogenesis, and maintenance of gestation, resulting in the reduction of productive and reproductive indexes [11].

In this way, the deleterious effect of thermal stress can promote damage to oocytes and consequently to embryos. Oocytes are protected from stress by heat shock proteins (HSPs), representing primary cellular protection responses [12]. In adverse situations, HSP levels are increased, thus assisting the synthesis and maturation of new proteins, which will replace those affected by metabolic stress [13,14].

Breeds adapted to regions of warm climate have provided an alternative to handle the effects of thermal caloric stress (TCS) on animal production. However, it was demonstrated that Bos taurus indicus, considered to be more thermotolerant, may also suffer injury in production and reproduction when in TCS [15]. Girolando cattle are considered a well-adapted breed for milk production in the warm regions of Brazil. In the Pantanal, the native Pantaneira breed is favored, as it resisted intense climate changes over hundreds of years. This breed is currently being rescued from extinction in order to improve animal production in critical climate regions [16]. Reproduction programs for these breeds may be supported by a better understanding regarding the response of oocyte development of heat-adapted cows under different stress conditions [17]. This study aims to evaluate the influence of thermal stress on physiological parameters, oocyte quality, and the presence of HSP70 and HSP90 in oocytes of breeds adapted to the tropics.

Section snippets

Animals

Girolando (Bos taurus x Bos indicus, Holstein 3/4; n = 12) and Pantaneira (an adapted Bos taurus taurus; n = 12) cattle were selected according to their clinical-reproductive characteristics. Donor cattle were vaccinated against mandatory calendar diseases and reproductive diseases (Cattle Master®; Zoetis). The immunization was performed at least 60 days before the first session of ultrasound-guided follicular aspiration (OPU). The cattle were non-pregnant, all aged 48 ± 12 months, and had a

Results

The present study was carried out in a tropical region, categorized by high air temperatures. In 2014, the average temperature in the day was lower than 25 °C only in the months between May and August. The relative air humidity (RH) was, in general, high, but showed great variation during the warmer months. In the hottest months of the year BGHI was greater than 80. Seven OPU sessions were performed with BGHI above 80 on the day of the session (session: 1–4, 10–12). Among session 1 and 6 BGHI

Discussion

In all OPU sessions, conditions of comfort and thermal stress were observed, clearly demonstrating the climatic conditions to which animals are subjected for most of the year. The climatic conditions of the Brazilian high wetland are characterized by temperatures that can reach up to 42 °C with an average annual temperature of 25 °C [20]. Such characteristics require the use of well-adapted animals, and strategies that enable greater productivity without compromising animal welfare. The search

Acknowledgment

This work was carried out with the support of the Coordination of Improvement of Higher Education Personnel - Brazil (CAPES) - Financing Code 001 and 88881.068117/2014-01 and Foundation for the development of teaching, science and technology in Mato Grosso do Sul (FUNDECT).

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