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The synthesis of diapause-specific molecular chaperones in embryos of Artemia franciscana is determined by the quantity and location of heat shock factor 1 (Hsf1)

  • Jiabo Tan
  • Thomas H. MacRaeEmail author
Original Paper
  • 18 Downloads

Abstract

The crustacean, Artemia franciscana, displays a complex life history in which embryos either arrest development and undertake diapause as cysts or they develop into swimming nauplii. Diapause entry is preceded during embryogenesis by the synthesis of specific molecular chaperones, namely the small heat shock proteins p26, ArHsp21, and ArHsp22, and the ferritin homolog, artemin. Maximal synthesis of diapause-specific molecular chaperones is dependent on the transcription factor, heat shock factor 1 (Hsf1), found in similar amounts in cysts and nauplii newly released from females. This investigation was performed to determine why, if cysts and nauplii contain comparable amounts of Hsf1, only cyst-destined embryos synthesize diapause-specific molecular chaperones. Quantification by qPCR and immunoprobing of Western blots, respectively, demonstrated that hsf1 mRNA and Hsf1 peaked by day 2 post-fertilization in embryos that were developing into cysts and then declined. hsf1 mRNA and Hsf1 were present in nauplii-destined embryos on day 2 post-fertilization, but in much smaller amounts than in cyst-destined embryos, and they increased in quantity until release of nauplii from females. Immunofluorescent staining revealed that the amount of Hsf1 in nuclei was greatest on day 4 post-fertilization in cyst-destined embryos but could not be detected in nuclei of nauplius-destined embryos at this time. The differences in quantity and location of Hsf1 explain why embryos fated to become cysts and eventually enter diapause synthesize p26, ArHsp21, ArHsp22, and artemin, whereas nauplius-destined embryos do not produce these molecular chaperones.

Keywords

Heat shock factor 1 Transcription factor Molecular chaperone Diapause Artemia franciscana 

Notes

Funding information

The work was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant (Number RGPIN/04882-2016) to THM and by a scholarship from the Chinese Scholarship Council to JT.

Compliance with ethical standards

The research described in this paper was performed in accordance with the ethical guidelines provided by the Canadian Council on Animal Care (CCAC). The University Committee on Laboratory Animals (UCLA) of Dalhousie University approved the research and assigned Protocol Number 117-36.

References

  1. Barna J, Princz A, Kosztelnik M, Hargitai B, Takács-Vellai K, Vellai T (2012) Heat shock factor-1 intertwines insulin/IGF-1, TGF-β and cGMP signaling to control development and aging. BMC Dev Biol 12:32CrossRefGoogle Scholar
  2. Barna J, Csermely P, Vellai T (2018) Roles of heat shock factor 1 beyond the heat shock response. Cell Mol Life Sci 75:2897–2916CrossRefGoogle Scholar
  3. Brunquell J, Morris S, Lu Y, Cheng F, Westerheide SD (2016) The genome-wide role of HSF-1 in the regulation of gene expression in Caenorhabditis elegans. BMC Genomics 17:559CrossRefGoogle Scholar
  4. Chen T, Amons R, Clegg JS, Warner AH, MacRae TH (2003) Molecular characterization of artemin and ferritin from Artemia franciscana. Eur J Biochem 270:137–145CrossRefGoogle Scholar
  5. Chen T, Villeneuve TS, Garant KA, Amons R, MacRae TH (2007) Functional characterization of artemin, a ferritin homolog synthesized in Artemia embryos during encystment and diapause. FEBS J 274:1093–1101CrossRefGoogle Scholar
  6. Clegg JS (1965) The origin of trehalose and its significance during the formation of encysted dormant embryos of Artemia salina. Comp Biochem Physiol 14:135–143CrossRefGoogle Scholar
  7. Clegg JS (1997) Embryos of Artemia franciscana survive four years of contibuous anoxia: the case for complete metabolic rate depression. J Exp Biol 200:467–475Google Scholar
  8. Clegg JS (2011) Stress-related proteins compared in diapause and in activated, anoxic encysted embryos of the animal extremophile, Artemia franciscana. J Insect Physiol 57:660–664CrossRefGoogle Scholar
  9. Clegg JS, Drinkwater LE, Sorgeloos P (1996) The metabolic status of diapause embryos of Artemia franciscna (SFB). Physiol Zool 69:49–66CrossRefGoogle Scholar
  10. Dai L, Chen D-F, Liu Y-L, Zhao Y, Yang F, Yang J-S, Yang W-J (2011) Extracellular matrix peptides of Artemia cyst shell participate in protecting encysted embryos from extreme environments. PLoS One 6(6):e20187CrossRefGoogle Scholar
  11. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122CrossRefGoogle Scholar
  12. Gomez-Pastor R, Burchfiel ET, Thiele DJ (2018) Regulation of heat shock transcription factors and their roles in physiology and disease. Nat Rev Mol Cell Biol 19:4–19CrossRefGoogle Scholar
  13. Gusev O, Cornette R, Kikawada T, Okuda T (2011) Expression of heat shock protein-coding genes associated with anhydrobiosis in an African chironomid Polypedilum vanderplanki. Cell Stress Chaperones 16:81–90CrossRefGoogle Scholar
  14. Jackson SA, Clegg JS (1996) Ontogeny of low molecular weight stress protein p26 during early development of the brine shrimp, Artemia franciscana. Develop Growth Differ 38:153–160CrossRefGoogle Scholar
  15. Kihara F, Niimi T, Yamashita O, Yaginuma T (2011) Heat shock factor binds to heat shock elements upstream of heat shock protein 70a and Samui genes to confer transcriptional activity in Bombyx mori diapause eggs exposed to 5 °C. Insect Biochem Mol Biol 41:843–851CrossRefGoogle Scholar
  16. King AM, MacRae TH (2012) The small heat shock protein p26 aids development of encysting Artemia embryos, prevents spontaneous diapause termination and protects against stress. PLoS One 7(8):e43723CrossRefGoogle Scholar
  17. King AM, Toxopeus J, MacRae TH (2013) Functional differentiation of small heat shock proteins in diapause-destined Artemia embryos. FEBS J 280:4761–4772CrossRefGoogle Scholar
  18. King AM, Toxopeus J, MacRae TH (2014) Artemin, a diapause-specific chaperone, contributes to the stress tolerance of Artemia franciscana cysts and influences their release from females. J Exp Biol 217:1719–1724CrossRefGoogle Scholar
  19. Koštál V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127CrossRefGoogle Scholar
  20. Koštál V, Štĕtina T, Poupardin R, Korbelová J, Bruce AW (2017) Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling. Proc Natl Acad Sci U S A 114:8532–8537CrossRefGoogle Scholar
  21. Li J, Chauve L, Phelps G, Brielmann RM, Morimoto RI (2016) E2F coregulates an essential HSF developmental program that is distinct from the heat shock response. Genes Dev 30:2062–2075CrossRefGoogle Scholar
  22. Li J, Labbadia J, Morimoto RI (2017) Rethinking HSF1 in stress, development, and organismal health. Trends Cell Biol 27:895–905CrossRefGoogle Scholar
  23. Liang P, MacRae TH (1999) The synthesis of a small heat shock/α-crystallin protein in Artemia and its relationship to stress tolerance during development. Dev Biol 207:445–456CrossRefGoogle Scholar
  24. Liang P, Amons R, Clegg JS, MacRae TH (1997) Molecular characterization of a small heat shock/α-crystallin protein in encysted Artemia embryos. J Biol Chem 272:19051–19058CrossRefGoogle Scholar
  25. Ma W-M, Li H-W, Dai Z-M, Yang J-S, Yang F, Yang W-J (2013) Chitin-binding proteins of Artemia diapause cysts participate in formation of the embryonic cuticle layer of cyst shells. Biochem J 449:285–294CrossRefGoogle Scholar
  26. MacRae TH (2003) Molecular chaperones, stress resistance and development in Artemia franciscana. Semin Cell Dev Biol 14:251–258CrossRefGoogle Scholar
  27. MacRae TH (2005) Diapause: diverse states of development and metabolic arrest. J Biol Res 3:3–14Google Scholar
  28. MacRae TH (2010) Gene expression, metabolic regulation and stress tolerance during diapause. Cell Mol Life Sci 67:2405–2424CrossRefGoogle Scholar
  29. MacRae TH (2016) Stress tolerance during diapause and quiescence of the brine shrimp, Artemia. Cell Stress Chaperones 21:9–18CrossRefGoogle Scholar
  30. Mahat DB, Salamanca HH, Duarte FM, Danko CG, Lis JT (2016) Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation. Mol Cell 62:63–78CrossRefGoogle Scholar
  31. Moore DS, Hansen R, Hand SC (2016) Liposomes with diverse compositions are protected during desiccation by LEA proteins from Artemia franciscana and trehalose. Biochim Biophys Acta 1858:104–115CrossRefGoogle Scholar
  32. Nair R, Shariq M, Dhamgaye S, Mukhopadhyay CK, Shaikh S, Prasad R (2017) Non-heat shock responsive roles of HSF1 in Candida albicans are essential under iron deprivation and drug defense. Biochim Biophys Acta 1864:345–354CrossRefGoogle Scholar
  33. Neudegger T, Verghese J, Hayer-Hartl M, Hartl FU, Bracher A (2016) Structure of human heat-shock transcription factor 1 in complex with DNA. Nat Struct Mol Biol 23:140–146CrossRefGoogle Scholar
  34. Qiu Z, MacRae TH (2008a) ArHsp21, a developmentally regulated small heat-shock protein synthesized in diapausing embryos of Artemia franciscana. Biochem J 411:605–611CrossRefGoogle Scholar
  35. Qiu Z, MacRae TH (2008b) ArHsp22, a developmentally regulated small heat shock protein produced in diapause-destined Artemia embryos, is stress inducible in adults. FEBS J 275:3556–3566CrossRefGoogle Scholar
  36. Reznik SYA, Voinovich ND (2016) Diapause induction in Trichogramma telengai: the dynamics of maternal thermosensitivity. Physiol Entomol 41:335–343CrossRefGoogle Scholar
  37. Robbins HM, Van Stappen G, Sorgeloos P, Sung YY, MacRae TH, Bossier P (2010) Diapause termination and development of encysted Artemia embryos: roles for nitric oxide and hydrogen peroxide. J Exp Biol 213:1464–1470CrossRefGoogle Scholar
  38. Takii R, Fujimoto M, Matsuura Y, Wu F, Oshibe N, Takaki E, Katiyar A, Akashi H, Makino T, Kawata M, Naka A (2017) HSF1 and HSF3 cooperatively regulate the heat shock response in lizards. PLoS One 12(7):e0180776CrossRefGoogle Scholar
  39. Tan J, MacRae TH (2018) Stress tolerance in diapausing embryos of Artemia franciscana is dependent on heat shock factor 1 (Hsf1). PLoS One 13(7):e0200153CrossRefGoogle Scholar
  40. Toxopeus J, Warner AH, MacRae TH (2014) Group 1 LEA proteins contribute to the desiccation and freeze tolerance of Artemia franciscana embryos during diapause. Cell Stress Chaperones 19:939–948CrossRefGoogle Scholar
  41. Wang Z, Lindquist S (1998) Developmentally regulated nuclear transport of transcription factors in Drosophila embryos enable the heat shock response. Development 125:4841–4850Google Scholar
  42. Warner AH, Miroshnychenko O, Kozarova A, Vacratsis PO, MacRae TH, Kim J, Clegg JS (2010) Evidence for multiple group 1 late embryogenesis abundant proteins in encysted embryos of Artemia and their organelles. J Biochem 148:581–592CrossRefGoogle Scholar
  43. Xiang H, MacRae TH (1995) Production and utilization of detyrosinated tubulin in developing Artemia larvae: evidence for α tubulin-reactive carboxypeptidase. Biochem Cell Biol 73:673–685CrossRefGoogle Scholar
  44. Zhang G, Storey JM, Storey KB (2011) Chaperone proteins and winter survival by a freeze tolerant insect. J Insect Physiol 57:1115–1122CrossRefGoogle Scholar
  45. Zhang G, Storey JM, Storey KB (2018) Elevated chaperone proteins are a feature of winter freeze avoidance by larvae of the goldenrod gall moth, Epiblema scudderiana. J Insect Physiol 106:106–113CrossRefGoogle Scholar

Copyright information

© Cell Stress Society International 2019

Authors and Affiliations

  1. 1.Department of BiologyDalhousie UniversityHalifaxCanada

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