Literature DB >> 16968769

Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect.

Joseph P Rinehart1, Scott A L Hayward, Michael A Elnitsky, Luke H Sandro, Richard E Lee, David L Denlinger.   

Abstract

Antarctica's terrestrial environment is a challenge to which very few animals have adapted. The largest, free-living animal to inhabit the continent year-round is a flightless midge, Belgica antarctica. Larval midges survive the lengthy austral winter encased in ice, and when the ice melts in summer, the larvae complete their 2-yr life cycle, and the wingless adults form mating aggregations while subjected to surprisingly high substrate temperatures. Here we report a dichotomy in survival strategies exploited by this insect at different stages of its life cycle. Larvae constitutively up-regulate their heat shock proteins (small hsp, hsp70, and hsp90) and maintain a high inherent tolerance to temperature stress. High or low temperature exposure does not further up-regulate these genes nor does it further enhance thermotolerance. Such "preemptive" synthesis of hsps is sufficient to prevent irreversible protein aggregation in response to a variety of common environmental stresses. Conversely, adults exhibit no constitutive up-regulation of their hsps and have a lower intrinsic tolerance to high temperatures, but their hsps can be thermally activated, resulting in enhanced thermotolerance. Thus, the midge larvae, but not the adults, have adopted the unusual strategy of expressing hsps continuously, possibly to facilitate proper protein folding in a cold habitat that is more thermally stable than that of the adults but a habitat subjected frequently to freeze-thaw episodes and bouts of pH, anoxic, and osmotic stress.

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Year:  2006        PMID: 16968769      PMCID: PMC1599938          DOI: 10.1073/pnas.0606840103

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  16 in total

1.  Developmental upregulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Ssarcophaga crassipalpis.

Authors:  J P Rinehart; G D Yocum; D L Denlinger
Journal:  Insect Biochem Mol Biol       Date:  2000-06       Impact factor: 4.714

2.  Stress proteins and stress tolerance in an Antarctic, psychrophilic yeast, Candida psychrophila.

Authors:  M L Deegenaars; K Watson
Journal:  FEMS Microbiol Lett       Date:  1997-06-15       Impact factor: 2.742

3.  Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae.

Authors:  R A Krebs; M E Feder
Journal:  Cell Stress Chaperones       Date:  1997-03       Impact factor: 3.667

4.  Gene expression of heat-shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata.

Authors:  Shin-Ichiro Tachibana; Hideharu Numata; Shin G Goto
Journal:  J Insect Physiol       Date:  2005-01-22       Impact factor: 2.354

5.  Temporal variation in overwintering gene expression and respiration in the solitary bee Megachile rotundata.

Authors:  G D Yocum; W P Kemp; J Bosch; J N Knoblett
Journal:  J Insect Physiol       Date:  2005-01-07       Impact factor: 2.354

6.  Role of trehalose phosphate synthase in anoxia tolerance and development in Drosophila melanogaster.

Authors:  Qiaofang Chen; Enbo Ma; Kevin L Behar; Tian Xu; Gabriel G Haddad
Journal:  J Biol Chem       Date:  2001-11-21       Impact factor: 5.157

7.  Heat shock causes protein aggregation and reduced protein solubility at the centrosome and other cytoplasmic locations.

Authors:  C A Vidair; R N Huang; S J Doxsey
Journal:  Int J Hyperthermia       Date:  1996 Sep-Oct       Impact factor: 3.914

8.  Protein aggregation as primary and characteristic cell reaction to various stresses.

Authors:  A E Kabakov; V L Gabai
Journal:  Experientia       Date:  1993-08-15

9.  Heat-shock protein 90 is down-regulated during pupal diapause in the flesh fly, Sarcophaga crassipalpis, but remains responsive to thermal stress.

Authors:  J P Rinehart; D L Denlinger
Journal:  Insect Mol Biol       Date:  2000-12       Impact factor: 3.585

10.  Differential expression of two HSP70 transcripts in response to cold shock, thermoperiod, and adult diapause in the Colorado potato beetle.

Authors:  G D. Yocum
Journal:  J Insect Physiol       Date:  2001-09       Impact factor: 2.354

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  43 in total

1.  Thermotolerance and hsp70 heat shock response in the cold-stenothermal chironomid Pseudodiamesa branickii (NE Italy).

Authors:  Paola Bernabò; Lorena Rebecchi; Olivier Jousson; Jose Luis Martínez-Guitarte; Valeria Lencioni
Journal:  Cell Stress Chaperones       Date:  2010-12-28       Impact factor: 3.667

2.  Molecular mechanisms underlying thermal adaptation of xeric animals.

Authors:  M B Evgen'ev; D G Garbuz; V Y Shilova; O G Zatsepina
Journal:  J Biosci       Date:  2007-04       Impact factor: 1.826

3.  Up-regulation of heat shock proteins is essential for cold survival during insect diapause.

Authors:  Joseph P Rinehart; Aiqing Li; George D Yocum; Rebecca M Robich; Scott A L Hayward; David L Denlinger
Journal:  Proc Natl Acad Sci U S A       Date:  2007-05-23       Impact factor: 11.205

4.  Dehydration, rehydration, and overhydration alter patterns of gene expression in the Antarctic midge, Belgica antarctica.

Authors:  Giancarlo Lopez-Martinez; Joshua B Benoit; Joseph P Rinehart; Michael A Elnitsky; Richard E Lee; David L Denlinger
Journal:  J Comp Physiol B       Date:  2009-01-06       Impact factor: 2.200

Review 5.  How insects survive the cold: molecular mechanisms-a review.

Authors:  Melody S Clark; M Roger Worland
Journal:  J Comp Physiol B       Date:  2008-06-27       Impact factor: 2.200

6.  Upregulation of heat-shock proteins in larvae, but not adults, of the flesh fly during hot summer days.

Authors:  Eri Harada; Shin G Goto
Journal:  Cell Stress Chaperones       Date:  2017-06-08       Impact factor: 3.667

7.  Heat shock protein expression enhances heat tolerance of reptile embryos.

Authors:  Jing Gao; Wen Zhang; Wei Dang; Yi Mou; Yuan Gao; Bao-Jun Sun; Wei-Guo Du
Journal:  Proc Biol Sci       Date:  2014-09-22       Impact factor: 5.349

8.  Identification and expression analysis of multiple small heat shock protein genes in spruce budworm, Choristoneura fumiferana (L.).

Authors:  Guoxing Quan; Jun Duan; Tim Ladd; Peter J Krell
Journal:  Cell Stress Chaperones       Date:  2017-07-28       Impact factor: 3.667

9.  Is cold the new hot? Elevated ubiquitin-conjugated protein levels in tissues of Antarctic fish as evidence for cold-denaturation of proteins in vivo.

Authors:  Anne E Todgham; Elizabeth A Hoaglund; Gretchen E Hofmann
Journal:  J Comp Physiol B       Date:  2007-08-21       Impact factor: 2.200

10.  Exploration of the mechanisms of protein quality control and osmoregulation in gills of Chromis viridis in response to reduced salinity.

Authors:  Cheng-Hao Tang; Ming-Yih Leu; Wen-Kai Yang; Shu-Chuan Tsai
Journal:  Fish Physiol Biochem       Date:  2014-05-08       Impact factor: 2.794

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