Characterization of the Constitutive Pig Ovary Heat Shock Chaperone Machinery and Its Response to Acute Thermal Stress or to Seasonal Variations1

Abstract

Reduced oocyte competence causes the lower fertility reported in domestic sows during the warm months of the year. Somatic cells express heat shock proteins (HSPs) to protect themselves from damage caused by thermal stress. HSPs are classified as molecular chaperones and control the correct folding of newly synthesized or damaged proteins. The present work performed a comprehensive survey of the different components of the heat shock chaperone machinery in the pig ovary, which included the HSP40, HSP70, HSP90, and HSP110 families, as well as heat shock factors (HSF) 1 and 2. Pig ovarian follicles constitutively expressed different members of these families; therefore, we examined their ability to respond to heat stress. In order to take into account the role of the complex follicular architecture, whole pig ovaries were exposed to 41.5°C for 1 h. This exposure significantly disrupted oocyte maturation and determined the upregulation of the HSP70, HSP40, HSPH1, HSPA4, HSPA4L, HSF1, and HFS2 genes, whereas expression levels of HSP90A and HSP90B, as well as those of genes unrelated to heat stress were not altered. Unexpectedly HSP and HSF expression levels changed only in oocytes but not in cumulus cells. Cumulus-oocyte complexes isolated from ovaries collected in summer showed the same pattern as those collected in winter. We conclude that the HSP chaperone machinery is constitutively fully operational in the pig ovary. However, following thermal stimuli or seasonal variations, cumulus cell HS-related gene expression remains unchanged, and only oocytes activate a response, suggesting why this mechanism is insufficient to preserve their competence both in vitro and in vivo.

Summer heat stress affects prostaglandin synthesis in the bovine oviduct

“…The expressions of HSP90AA1 and PTGES3 mRNAs in the ampullary oviduct were higher in summer than in winter, whereas there was no difference in them in the isthmic oviduct in summer and winter. It has been reported that the expression of HSPs is higher in porcine oocytes in summer than in winter, although there are no seasonal changes in porcine cumulus cell (Pennarossa et al 2012). Therefore, it is possible that the expressions of HSP90AA1 and PTGES3 in the isthmic oviduct are not affected by different seasonal conditions in contrast to those in the ampullary oviduct.…”

Developmental competence and expression profile of genes in buffalo (Bubalus bubalis) oocytes and embryos collected under different environmental stress

“…A study reported that exposure of COCs to elevated temperature increased HSP-70.1 mRNA in cumulus cells and some adverse effects of heat stress on oocytes were intervened through cumulus cells (Payton et al 2011). Besides, exposure of buffalo oocytes to elevated temperature (41.5°C) for 1 h greatly disrupted oocyte maturation and resulted in upregulation of HSP-70.1 mRNA expression at 8-to 16-cell and blastocyst (Pennarossa et al 2012). It suggests that heat stress can promote HSP-70.1 mRNA synthesis in buffalo and this could be used as marker of biological effect of heat stress in buffalo.…”

Physiological consequences of heat stress in pigs

“…How exactly heat impacts female fertility is not well understood, although it most likely involves compromised production of gametes and embryos capable of development. Heat stress has been associated with reduced developmental competence, and induction of apoptosis in in vitro fertilised and parthenogenetically activated pig embryos (Isom et al 2007b;Bertoldo et al 2010;Pennarossa et al 2012). Although the heat shock protein (HSP) machinery is constitutively expressed in the somatic cells of the ovary, there is only a change in abundance in the oocyte in response to whole-ovary heat stress (Pennarossa et al 2012), suggesting that regulation in response to hyperthermia may occur within the porcine oocyte.…”