Hsp70 and larval thermotolerance in Drosophila melanogaster: how much is enough and when is more too much?

Abstract

Heat shock proteins (Hsps) and other molecular chaperones perform diverse cellular roles (e.g., inducible thermotolerance) whose functional consequences are concentration dependent. We manipulated Hsp70 concentration quantitatively in intact larvae of Drosophila melanogaster to examine its effect on survival, developmental time and tissue damage after heat shock. Larvae of an extra-copy strain, which has 22 hsp70 copies, produced Hsp70 more rapidly and to higher concentrations than larvae of a control strain, which has the wild-type 10 copies of the gene. Increasing the magnitude and duration of pretreatment increased Hsp70 concentrations, improved tolerance of more severe stress, and reduced delays in development. Pretreatment, however, did not protect against acute tissue damage. For larvae provided a brief or mild intensity pretreatment, faster expression of Hsp70 in the extra-copy strain improved survival to adult and reduced tissue damage 21h after heat shock. Negative effects on survival ensued in extra-copy larvae pretreated most intensely, but their overexpression of Hsp70 did not increase tissue damage. Because rapid expression to yield a low Hsp70 concentration benefits larvae but overexpression harms them, natural selection may balance benefits and costs of high and low expression levels in natural populations.

Differences in heat shock protein 70 expression during larval and early spat development in the Eastern oyster, Crassostrea virginica (Gmelin, 1791)

“…In the red flour beetle, the lowest levels of a constitutively expressed HSP 70 gene were seen in pupae just prior to metamorphosis. While increases in expression of HSP 70 can be explained as a form of cell level defense during stress-sensitive phases of development, detrimental effects of HSP overexpression in the cells are likely to account for the lower expression of this protein during other phases of development (Krebs and Feder 1998;Feder and Hofmann 1999). Feder and Hofmann (1999) proposed that one of the possible explanations for the negative effects of HSPs is the reduction in overall cellular energy budget because of high energetic costs of synthesis/degradation of HSPs.…”

Response of heat shock protein genes of the oriental fruit moth under diapause and thermal stress reveals multiple patterns dependent on the nature of stress exposure

“…This may reflect the role of molecular chaperons in the first line of defense of an insect to prevent irreversible denaturation of proteins and vital enzymes (Arrigo 2013;King and MacRae 2015). GmHsp70/ 90 were also highly expressed in the fat body, suggesting a role of chaperone function in stress signal detection in tissue during development (Krebs and Feder 1998), but these functional roles remain speculative in the absence of additional data including changes in protein levels.…”

“…Both copies of GmHsp70 were good indicators of stressful conditions given that they were expressed at a much lower base level than GmHsp90, which may associate with stress signal detection in tissue during development (Krebs and Feder 1998). On the other hand, GmHsp90 may be a biomarker of diapause in OFM, being downregulated specifically when entering diapause.…”

Embryo stability and vulnerability in an always changing world

“…In contrast, HSPs are not induced in response to stress during early cleavage stages of the orphan embryos (41). This strategy may be in part because overexpression of these proteins in embryos inhibits development (42), possibly by interfering with mitosis or signaling (43,44). Instead the strategy is to have adequate, but not excessive, HSP present in the egg at fertilization.…”