Chaperone proteins and winter survival by a freeze tolerant insect

Zhang, Guijun; Storey, Janet M.; Storey, Kenneth B.

doi:10.1016/j.jinsphys.2011.02.016

Cited by 66 publications

(45 citation statements)

References 48 publications

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“…HSP members were subsequently shown to have integral roles in stabilizing the proteome of all cells including folding of new Significantly different from the corresponding September value as determined by analysis of variance followed by a two-tailed Dunnett's t-test, P , 0.01; b P , 0.05. Reprinted with permission from Zhang et al 74 Photograph by JM Storey. proteins, rescue of malfolded or unfolded proteins, control of protein aggregation, and guiding protein translocation to subcellular sites.…”

Section: Resultsmentioning

confidence: 99%

“…Protein levels of Hsp110, Hsp70, and Hsp40 (recall that these three work together) all rose over the late autumn and winter in the larvae, reaching 1.5-to 2.0-fold higher than September values. 74 Interestingly, levels of the mitochondrial Hsp60 decreased by about 50% during the winter in E. solidaginis. This correlates with comparable reductions in mitochondrial DNA content and activities of mitochondrial enzymes in this freeze-tolerant species that indicate winter degradation of these organelles.…”

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confidence: 98%

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Heat shock proteins and hypometabolism: adaptive strategy for proteome preservation

Storey¹,

Storey²

2011

RRB

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Abstract:To survive under harsh environmental conditions many organisms retreat into hypometabolic states where metabolic rate may be reduced by 80% or more and energy use is reprioritized to emphasize key functions that sustain viability and provide cytoprotection. ATP-expensive activities, such as gene expression, protein turnover (synthesis and degradation), and the cell cycle, are largely shut down. As a consequence, mechanisms that stabilize the existing cellular proteome can become critical for long-term survival. Heat shock proteins (HSPs) are well-known for their actions as chaperones that act to fold new proteins or refold proteins that are damaged. Indeed, they are part of the "minimal stress proteome" that appears to be a ubiquitous response by all cells as they attempt, successfully or unsuccessfully, to deal with stress. The present review summarizes evidence that HSPs are also a conserved feature of natural animal hypometabolism including the phenomena of estivation, hibernation, diapause, cold-hardiness, anaerobiosis, and anhydrobiosis. That is, organisms that retreat into dormant or torpid states in anticipation that environmental conditions may become too difficult for normal life also integrate the use of HSPs to protect their proteome while hypometabolic. Multiple studies show a common upregulation of expression of hsp genes and/or HSP proteins prior to or during hypometabolism in organisms as diverse as ground squirrels, turtles, land snails, insects, and brine shrimp and in situations of both preprogrammed dormancies (eg, seasonal or life stage specific) and opportunistic hypometabolism (eg, triggered by desiccation or lack of oxygen). Hence, HSPs are not just a "shock" response that attempts to rescue cells from damaging stress but are a key protective strategy that is an integral component of natural states of torpor and dormancy.

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Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 98%

Heat shock proteins and hypometabolism: adaptive strategy for proteome preservation

Storey¹,

Storey²

2011

RRB

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“…Another possibility is rapid upregulation of chaperone proteins or heat shock proteins (Hsps). Zhang et al (Zhang et al, 2011) reported elevation of various Hsps during autumn and winter in E. solidaginis larvae. Hsps are upregulated in some species during rapid cold-hardening (RCH) (Li and Denlinger, 2008;Kostál and Tollarová-Borovanská, 2009), but have not been reported in E. solidaginis as part of the RCH response.…”

Section: Discussionmentioning

confidence: 99%

Mild desiccation rapidly increases freeze tolerance of the goldenrod gall fly, Eurosta solidaginis: evidence for drought-induced RCH

Levis

Lee

2012

Journal of Experimental Biology

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SUMMARYOverwintering insects may experience extreme cold and desiccation stress. Both freezing and desiccation require cells to tolerate osmotic challenge as solutes become concentrated in the hemolymph. Not surprisingly, physiological responses to low temperature and desiccation share common features and may confer cross-tolerance against these stresses. Freeze-tolerant larvae of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae), experience extremely dry and cold conditions in winter. To determine whether mild desiccation can improve freeze tolerance at organismal and cellular levels, we assessed survival, hemolymph osmolality and glycerol levels of control and desiccated larvae. Larvae that lost only 6-10% of their body mass, in as little as 6h, had markedly higher levels of freeze tolerance. Mild, rapid desiccation increased freezing tolerance at -15°C in September-collected larvae (33.3±6.7 to 73.3±12%) and at -20°C in October-collected larvae (16.7±6.7 to 46.7±3.3%). Similarly, 6h of desiccation improved in vivo survival by 17-43% in fat body, Malpighian tubule, salivary gland and tracheal cells at -20°C. Desiccation also enhanced intrinsic levels of cold tolerance in midgut cells frozen ex vivo (38.7±4.6 to 89.2±5.5%). Whereas hemolymph osmolality increased significantly with desiccation treatment from 544±16 to 720±26mOsm, glycerol levels did not differ between control and desiccated groups. The rapidity with which a mild desiccation stress increased freeze tolerance closely resembles the rapid cold-hardening response, which occurs during brief sub-lethal chilling, and suggests that drought stress can induce rapid cold-hardening.

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“…Hsp70, Hsp40, and other HSPs are elevated in coldadapted larvae of the gall fly, Eurosta solidaginis, suggesting that these molecular chaperones contribute to protein preservation during stress (Zhang et al 2011). The mRNA for Hsp40, among several other molecular chaperones, is upregulated during recovery from cold stress in Drosophila melanogaster, implying that Hsp40 works in concert with other chaperones to repair protein chilling injury (Colinet et al 2010), just as it could during recovery from heat shock and from stresses associated with diapause and quiescence.…”

Section: Discussionmentioning

confidence: 99%

ArHsp40, a type 1 J-domain protein, is developmentally regulated and stress inducible in post-diapause Artemia franciscana

Jiang

Rowarth

Panchakshari

et al. 2016

Cell Stress and Chaperones

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Upon diapause termination and exposure to favorable environmental conditions, cysts of the crustacean Artemia franciscana reinitiate development, a process dependent on the resumption of metabolic activity and the maintenance of protein homeostasis. The objective of the work described herein was to characterize molecular chaperones during post-diapause growth of A. franciscana. An Hsp40 complementary DNA (cDNA) termed ArHsp40 was cloned and shown to encode a protein with an amino-terminal J-domain containing a conserved histidine, proline, and aspartic acid (HPD) motif. Following the J-domain was a Gly/Phe (G/F) rich domain, a zinc-binding domain which contained a modified CXXCXGXG motif, and the carboxyl-terminal substrate binding region, all characteristics of type I Hsp40. Multiple alignment and protein modeling showed that ArHsp40 is comparable to Hsp40s from other eukaryotes and likely to be functionally similar. qRT-PCR revealed that during postdiapause development, ArHsp40 messenger RNA (mRNA) varied slightly until the E2/E3 stage and decreased significantly upon hatching. The immunoprobing of Western blots demonstrated that ArHsp40 was also relatively constant until E2/ E3 and then declined dramatically. The drop in ArHsp40 when metabolism and protein synthesis were increasing was unexpected and demonstrated developmental regulation. The reduction in ArHsp40 at such an active life history stage indicates, as one possibility, that A. franciscana possesses additional Hsp40s, one or more of which replaces ArHsp40 as development progresses. Increased synthesis upon heat shock established that in addition to being developmentally regulated, ArHsp40 is stress inducible and, because it is found in mature cysts, ArHsp40 has the potential to contribute to stress tolerance during diapause.

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Chaperone proteins and winter survival by a freeze tolerant insect

Cited by 66 publications

References 48 publications

Heat shock proteins and hypometabolism: adaptive strategy for proteome preservation

Heat shock proteins and hypometabolism: adaptive strategy for proteome preservation

Mild desiccation rapidly increases freeze tolerance of the goldenrod gall fly, Eurosta solidaginis: evidence for drought-induced RCH

ArHsp40, a type 1 J-domain protein, is developmentally regulated and stress inducible in post-diapause Artemia franciscana

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