Bovine spermatozoa react to in vitro heat stress by activating the mitogen-activated protein kinase 14 signalling pathway (original) (raw)
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Impact of Heat Stress on Bovine Sperm Quality and Competence
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Global warming has negatively influenced animal production performance, in addition to animal well-being and welfare, consequently impairing the economic sustainability of the livestock industry. Heat stress impact on male fertility is complex and multifactorial, with the fertilizing ability of spermatozoa affected by several pathways. Among the most significative changes are the increase in and accumulation of reactive oxygen species (ROS) causing lipid peroxidation and motility impairment. The exposure of DNA during the cell division of spermatogenesis makes it vulnerable to both ROS and apoptotic enzymes, while the subsequent post-meiotic DNA condensation makes restoration impossible, harming later embryonic development. Mitochondria are also susceptible to the loss of membrane potential and electron leakage during oxidative phosphorylation, lowering their energy production capacity under heat stress. Although cells are equipped with defense mechanisms against heat stress, heat i...
Heat stress effects on bovine sperm cells: a chronological approach to early findings
International Journal of Biometeorology, 2020
Testicular heat stress affects sperm quality and fertility. However, the chronology of these effects is not yet fully understood. This study aimed to establish the early sequential effects of heat stress in bull sperm quality. Semen and blood samples of Nellore breed bulls were collected and distributed into control and testicular heat stress (scrotal bags/96 h) groups. Semen samples were evaluated for sperm motility, abnormalities, plasma membrane integrity, acrosomal membrane integrity, mitochondrial membrane potential, sperm lipid peroxidation, seminal plasma lipid peroxidation, and DNA fragmentation. Blood plasma was also evaluated for lipid peroxidation. An increase in sperm abnormalities was observed 7 days following heat stress. After 14 days, sperm lipid peroxidation increased and mitochondrial membrane function, sperm motility, and plasma membrane integrity decreased. Heat stress effects were still observed after 21 days following heat stress. An increase in sperm DNA fragmentation was observed as a late effect after 28 days. Thus, the initial effects of heat stress (i.e., increasing sperm abnormalities and lipid peroxidation) suggest the presence of oxidative stress in the semen that alters mitochondrial function, sperm motility, plasma membrane integrity, and belatedly, DNA fragmentation. Although sperm abnormalities persisted and increased over time, sperm lipid peroxidation, in turn, increased only until 21 days after heat stress. In this regard, these findings provide a greater understanding of the chronological effects of experimentally induced heat stress on bovine sperm, providing valuable insights about spermatogenesis during the first 28 days following heat stress.
Pathogenesis of Heat-Induced Infertility in Male Mammals
2020
Testicular temperature must be 3-5 ºC below body temperature for physiological spermatogenesis and testicular function. Therefore, increased testicular temperatures, either the entire body or just the testes, reduce sperm quality and fertility. Our understanding regarding the pathophysiology of testicular heat stress is unclear. There is a long-standing dogma that as testicular temperature increases, there is no change in blood flow, and the testes, which are regarded as physiologically functioning on the brink of hypoxia, undergo frank hypoxia. However, recent data challenged this dogma, indicating that temperature itself was the major pathological agent. Therefore, this thesis was developed to further investigate the subject. In a series of five studies, the overall aim was to investigate changes in testicular blood flow in response to testicular heat stress and its pathophysiology on testes and testicular function. In the first two studies, we investigated how heat stress and hypoxia affect testicular blood flow and metabolism in rams; both treatments increased testicular blood flow which supported metabolic needs, with no indications of hypoxia. The third study was a comparison of responses between Bos indicus and Bos taurus bulls to increased testicular temperature. Once again, testicular blood flow significantly increased, supporting metabolic needs, with no indications of hypoxia. These three studies provided new knowledge to debunk the previous dogma and to support the new understanding that temperature itself was the main pathological factor of testicular heat stress. In the last two studies, we investigated how heat stress modulates gene expression in bull and mouse testes. Heat stress caused modulation of gene P53 and components of the P53-dependent apoptotic pathway, also upregulation of genes associated with the antioxidant (GPX1) and chaperone systems (Hsp70) and downregulation of the StAR gene and reduced testosterone concentrations (impaired steroidogenesis). Collectively, these studies provided novel information iii regarding testicular vascular physiology under local heat stress and described several factors associated with its pathophysiology in the testes. Lastly, it is expected that these findings will serve as a strong base for new studies in this area, to elucidate in more detail, how heat stress affects reproduction in male mammals.
Acute mild heat stress alters gene expression in testes and reduces sperm quality in mice
Theriogenology, 2020
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Comparative proteomic analysis of heat stress proteins associated with rat sperm maturation
Molecular medicine reports, 2016
Heat stress is demonstrated to have an effect on the function of the male testis, however, limited information has been reported on its effects on sperm maturation. In the present study, a comparative proteomic analysis was performed on the rat caput epididymal fluids responsible for sperm maturation, to identify key heat‑stress‑associated sperm maturation proteins. The results demonstrated 21 proteins corresponding to 29 differential protein spots, including 10 downregulated and 11 upregulated proteins in the heat treatment group. Functional analysis demonstrated that these proteins were primarily involved in enriched reproduction and antioxidant activity. Analysis of western blot and immunohistochemical analysis demonstrated that the expression of antioxidant proteins peroxiredoxin 6 and clusterin were downregulated, and the expression of superoxide dismutase upregulated, in the heat treatment group. Morphological and TUNEL experiments demonstrated that altered nucleus activity oc...
Causes, effects and molecular mechanisms of testicular heat stress
The process of spermatogenesis is temperature-dependent and occurs optimally at temperatures slightly lower than that of the body. Adequate thermoregulation is imperative to maintain testicular temperatures at levels lower than that of the body core. Raised testicular temperature has a detrimental effect on mammalian spermatogenesis and the resultant spermatozoa. Therefore, thermoregulatory failure leading to heat stress can compromise sperm quality and increase the risk of infertility. In this paper, several different types of external and internal factors that may contribute towards testicular heat stress are reviewed. The effects of heat stress on the process of spermatogenesis, the resultant epididymal spermatozoa and on germ cells, and the consequent changes in the testis are elaborated upon. We also discuss the molecular response of germ cells to heat exposure and the possible mechanisms involved in heat-induced germ cell damage, including apoptosis, DNA damage and autophagy. Further, the intrinsic and extrinsic pathways that are involved in the intricate mechanism of germ cell apoptosis are explained. Ultimately, these complex mechanisms of apoptosis lead to germ cell death.
Amelioration of heat stress-induced damage to testes and sperm quality
Theriogenology, 2020
Heat stress (HS) occurs when temperatures exceed a physiological range, overwhelming compensatory mechanisms. Most mammalian testes are~4e5 C cooler than core body temperature. Systemic HS or localized warming of the testes affects all types of testicular cells, although germ cells are more sensitive than either Sertoli or Leydig cells. Increased testicular temperature has deleterious effects on sperm motility, morphology and fertility, with effects related to extent and duration of the increase. The major consequence of HS on testis is destruction of germ cells by apoptosis, with pachytene spermatocytes, spermatids and epididymal sperm being the most susceptible. In addition to the involvement of various transcription factors, HS triggers production of reactive oxygen species (ROS), which cause apoptosis of germ cells and DNA damage. Effects of HS on testes can be placed in three categories: testicular cells, sperm quality, and ability of sperm to fertilize oocytes and support development. Various substances have been given to animals, or added to semen, in attempts to ameliorate heat stress-induced damage to testes and sperm. They have been divided into various groups according to their composition or activity, as follows: amino acids, antibiotics, antioxidant cocktails, enzyme inhibitors, hormones, minerals, naturally produced substances, phenolic compounds, traditional herbal medicines, and vitamins. Herein, we summarized those substances according to their actions to mitigate HS' three main mechanisms: oxidative stress, germ cell apoptosis, and sperm quality deterioration and testicular damage. The most promising approaches are to use substances that overcome these mechanisms, namely reducing testicular oxidative stress, reducing or preventing apoptosis and promoting recovery of testicular tissue and restoring sperm quality. Although some of these products have considerable promise, further studies are needed to clarify their ability to preserve or restore fertility following HS; these may include more advanced sperm analysis techniques, e.g. sperm epigenome or proteome, or direct assessment of fertilization and development, including in vitro fertilization or breeding data (either natural service or artificial insemination).
Toxicology and industrial health, 2013
Scrotal hyperthermia has been known as a cause of male infertility but the exact mechanism leading to impaired spermatogenesis is unknown. This work was aimed to investigate the role of scrotal hyperthermia on cell proliferation and apoptosis in testes. The rats were randomly allotted into one of the four experimental groups: A (control), B (1 day after scrotal hyperthermia), C (14 days after scrotal hyperthermia), and D (35 days after scrotal hyperthermia); each group comprised 7 animals. Scrotal hyperthermia was carried out in a thermostatically controlled water bath at 43°C for 30 min once daily for 6 consecutive days. Control rats were treated in the same way, except the testes were immersed in a water bath maintained at 22°C. Hyperthermia-exposed rats were killed under 50 mg/kg ketamine anaesthesia and tissue samples were obtained for biochemical and histopathological investigations. Hyperthermia treatment significantly decreased the testicular antioxidant system, including dec...
Effects of whole-body heat on male germ cell development and sperm motility in the laboratory mouse
Reproduction, fertility, and development, 2014
This study investigated the effects of high temperatures on male germ cell development and epididymal sperm motility of laboratory mice. In Experiment 1, adult males (n ¼ 16) were exposed to whole-body heat of 37-388C for 8 h day À1 for 3 consecutive days, whereas controls (n ¼ 4) were left at 23-248C. In Experiment 2, adult mice (n ¼ 6) were exposed to 37-388C for a single 8-h period with controls (n ¼ 6) left at 23-248C. Experiment 2 was conducted as a continuation of previous study that showed changes in spermatozoa 16 h after exposure to heat of 37-388C for 8 h day À1 for 3 consecutive days. In the present study, in Experiment 1, high temperature reduced testes weights 16 h and 14 days after exposure, whereas by Day 21 testes weights were similar to those in the control group (P ¼ 0.18). At 16 h, 7 and 14 days after exposure, an increase in germ cell apoptosis was noticeable in early and late stages (I-VI and XI-XII) of the cycle of the seminiferous epithelium. However, apoptosis in intermediate stages (VII-X) was evident 16 h after heat exposure (P , 0.05), without any change at other time periods. By 21 days, there were no significant differences between heattreated groups and controls. Considerably more caspase-3-positive germ cells occurred in heat-treated mice 16 h after heat exposure compared with the control group (P , 0.0001), whereas 8 h after heat in Experiment 2, sperm motility was reduced with a higher percentage of spermatozoa showing membrane damage. In conclusion, the present study shows that whole-body heat of 37-388C induces stage-specific germ cell apoptosis and membrane changes in spermatozoa; this may result in reduced fertility at particular times of exposure after heating.
Theriogenology, 2019
We tested the hypothesis that hypoxia replicates effects of hyperthermia on reducing number and quality of sperm produced, whereas hyperoxia mitigates effects of hyperthermia. Ninety-six CD-1 mice (~50 d old), inspired air with 13, 21, or 95% O 2 and were exposed to ambient temperatures of 20 or 36 o C (3 x 2 factorial, six groups) twice for 12 h (separated by 12 h at 20 0 C and 21% O 2), with euthanasia 14 or 20 d after first exposure. Combined for both post-exposure intervals, there were primarily main effects of temperature; mice exposed to 20 vs 36 0 C had differences in testis weight (110.2 vs 96.9 mg, respectively; P<0.0001), daily sperm production (24.7 vs 21.1 x 10 6 sperm/g testes, P<0.03), motile sperm (54.5 vs 41.5%, P<0.002), morphologically normal sperm (59.9 vs 45.4%, P<0.002), morphologically abnormal heads (7.3 vs 22.0%, P<0.0001), seminiferous tubule diameter (183.4 vs 176.3 μm, P<0.004) and altered elongated spermatids (2.2 vs 15.9, P<0.001). Increasing O 2 (from 13 to 95%) affected morphologically abnormal heads (15.4, 10.8 and 17.6%, respectively; P<0.03), seminiferous tubule diameter (175.7, 185.6 and 178.4 μm, P<0.003) and total altered spermatids (8.3, 3.3 and 15.2, P<0.05). Our hypothesis was not supported; hypoxia did not replicate effects of hyperthermia with regards to reducing number and quality of sperm produced and hyperoxia did not mitigate effects of hyperthermia. We concluded that hyperthermia per se and not secondary hypoxia was the fundamental cause of heat-induced effects on spermatogenesis and sperm. These findings are of interest to develop evidence-based efforts to mitigate effects of testicular hyperthermia, as efforts should be focused on hyperthermia per se and not on hyperthermia-induced hypoxia.