Skip to main content
SpringerLink
Log in

Physicochemical Aspects of the Biological Functions of Trehalose and Group 3 LEA Proteins as Desiccation Protectants

  • Chapter
  • First Online:
Survival Strategies in Extreme Cold and Desiccation

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1081))

Abstract

In this review, we first focus on the mechanism by which the larva of the sleeping chironomid, Polypedilum vanderplanki, survives an extremely dehydrated state and describe how trehalose and probably late embryogenesis abundant (LEA) proteins work as desiccation protectants. Second, we summarize the solid-state and solution properties of trehalose and discuss why trehalose works better than other disaccharides as a desiccation protectant. Third, we describe the structure and function of two model peptides based on group 3 LEA proteins after a short introduction of native LEA proteins themselves. Finally, we present our conclusions and a perspective on the application of trehalose and LEA model peptides to the long-term storage of biological materials.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

BDG:

β-D-galactosidase

G3LEA:

Group 3 late embryogenesis abundant

IDP:

Intrinsically disordered protein

LDH:

Lactate dehydrogenase

MD:

Molecular dynamics

POPC:

1-palmitoyl 2-oleoyl-sn-glycero-3-phosphatidylcholine

References

  • Akao K, Okubo Y, Ikeda T, Inoue Y, Sakurai M (1998) Infrared spectroscopic study on the structural property of a trehalose-water complex. Chem Lett 27:759–760

    Article  Google Scholar 

  • Aldous BJ, Affret AD, Franks F (1995) Crystallisation of hydrates from amorphous carbohydrates. CryoLetters 16:181–186

    CAS  Google Scholar 

  • Banno M, Watanabe HC, Furuta T, Sakurai M (2015) Analysis of free energy and structural change of G3LEA peptide in the binding process to a POPC bilayer. Cryobiol Cryotechol 61:105–109

    Google Scholar 

  • Belton PS, Gil AH (1994) IR and Raman spectroscopic studies of the interaction of trehalose with hen egg white lysozyme. Biopolymers 34:957–961

    Article  CAS  PubMed  Google Scholar 

  • Boswell LC, Menze MA, Hand SC (2014) Group 3 late embryogenesis abundant proteins from embryos of Artemia franciscana: structural properties and protective abilities during desiccation. Physiol Biochem Zool 87:640–651

    Article  PubMed  Google Scholar 

  • Chakrabortee S, Boschetti C, Walton LJ, Sarkar S, Rubinsztein DC, Tunnacliffe A (2007) Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proc Natl Acad Sci U S A 104:18073–18078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakrabortee S, Tripathi R, Watson M, Gabriele S, Schierle K, Kurniawan DP, Kaminski CF, Wise MJ, Tunnacliffe A (2012) Intrinsically disordered proteins as molecular shields. Mol BioSyst 8:210–219

    Article  CAS  PubMed  Google Scholar 

  • Choi Y, Cho KW, Jeong K, Jung S (2006) Molecular dynamics simulations of trehalose as a ‘dynamic reducer’ for solvent water molecules in the hydration shell. Carbohydr Res 341:1020–1028

    Article  CAS  PubMed  Google Scholar 

  • Clegg JS (2001) Cryptobiosis a peculiar state of biological organization. Comp Biochem Physiol 128B:613–624

    Article  CAS  Google Scholar 

  • Crowe LM (2002) Lessons from nature: the role of sugars in anhydrobiosis. Comp Biochem Physiol 131A:505–513

    Article  CAS  Google Scholar 

  • Crowe JH, Hoekstra FA, Crowe L (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599

    Article  CAS  PubMed  Google Scholar 

  • Crowe LM, Reid DS, Crowe JH (1996) Is trehalose special for preserving dry biomaterials? Biophys J 71:2087–2093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crowe JH, Carpenter JF, Crowe L (1998) The role of vitrification in Anhydrobiosis. Annu Rev Physiol 60:73–103

    Article  CAS  PubMed  Google Scholar 

  • Dowd MK, Reilly PJ, French AD (1992) Conformational analysis of trehalose disaccharides and analogues using MM3. J Comput Chem 13:102–114

    Article  CAS  Google Scholar 

  • Dure L III (1993) A repeating 11-mer amino acid motif and plant desiccation. Plant J 3:363–369

    Article  CAS  PubMed  Google Scholar 

  • Dure L III, Greenway SC, Galau GA (1981) Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry 20:4162–4168

    Article  CAS  PubMed  Google Scholar 

  • Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glyocobiology 13:17R–27R

    Article  CAS  Google Scholar 

  • Furuki T, Sakurai M (2014) Group 3 LEA protein model peptides protect liposomes during desiccation. Biochim Biophys Acta 1838:2757–2766

    Article  CAS  PubMed  Google Scholar 

  • Furuki T, Sakurai M (2016) Group 3 LEA protein model peptides protect enzymes against desiccation stress. Biochim Biophys Acta 1864:1237–1243

    Article  CAS  PubMed  Google Scholar 

  • Furuki T, Sakurai M (2017) Protective effect of group 3 LEA model peptides on the thermal denaturation of proteins. Cryobiol Cryotechnol 63:139–142

    Google Scholar 

  • Furuki T, Kishi A, Sakurai M (2005) De- and rehydration behavior of α,α-trehalose dehydrate under humidity-controlled atmospheres. Carbohydr Res 340:429–438

    Article  CAS  PubMed  Google Scholar 

  • Furuki T, Abe R, Kawaji H, Atake T, Sakurai M (2006) Thermodynamic functions of α,α-trehalose dihydrate and of α,β-trehalose monohydrate at temperatures from 13 K to 300 K. J Chem Thermodyn 38:1612–1619

    Article  CAS  Google Scholar 

  • Furuki T, Abe R, Kawaji H, Atake T, Sakurai M (2008) Effect of atmospheric pressure on the phase transitions of a, a-trehalose dehydrate. DTA study of the dehydration behavior in open systems. J Therm Anal Calorim 93:561–567

    Article  CAS  Google Scholar 

  • Furuki T, Ito T, Asakawa N, Inoue Y, Sakurai M (2009) Effects of trehalose on the swelling behavior of hydrogel –visualization of the preferential hydration of disaccharides. Chem Lett 38:264–265

    Article  CAS  Google Scholar 

  • Furuki T, Shimizu T, Kikawada T, Okuda T, Sakurai M (2011) Salt effects on the structural and thermodynamic properties of group 3 late embryogenesis abundant protein model peptides. Biochemistry 50:7093–7103

    Article  CAS  PubMed  Google Scholar 

  • Furuki T, Shimizu T, Cakrabortee S, Yamakawa K, Hatanaka R, Takahashi T, Kikawada T, Okuda T, Mihara H, Tunnacliffe A, Sakurai M (2012) Effects of group-3 LEA protein model peptides on desiccation-induced protein aggregation. Biochim Biophys Acta 1824:891–897

    Article  CAS  PubMed  Google Scholar 

  • Furuki T, Watanabe T, Furuta T, Takano K, Shirakashi R, Sakurai M (2016) The dry preservation of giant vesicles using a Group 3 LEA protein model peptide and its molecular mechanism. Bull Chem Soc Jpn 89:1493–1499

    Article  CAS  Google Scholar 

  • Galema SA, Høiland H (1991) Stereochemical aspects of hydration of carbohydrates in aqueous solutions. 3. Density and ultrasound measurement. J Phys Chem 95:5321–5326

    Article  CAS  Google Scholar 

  • Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J, Tunnacliffe A (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem 278:12977–12984

    Article  CAS  PubMed  Google Scholar 

  • Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grelet J, Benamar A, Teyssier E, Avelange-Macharel M-H, Grunwald D, Macherel D (2005) Identification in pea seed mitochondria of a late embryogenesis abundant protein able to protect enzymes from drying. Plant Physiol 137:157–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gusev O, Suetsugu Y, Cornette R, Kawashima T, Logacheva MD, Kondrashov AS, Penin AA, Hatanaka R, Kikuta S, Shimura S, Kanamori H, Katayose Y, Matsumoto T, Shagimardanova E, Alexeev D, Govorun V, Wisecaver J, Mikheyev A, Koyanagi R, Fujie M, Nishiyama T, Shigenobu S, Shibata TF, Golygina V, Hasebe M, Okuda T, Satoh N, Kikawada T (2014) Comparative genome sequencing reveals genomic signature of extreme desiccation tolerance in the anhydrobiotic midge. Nat Commun 5:4784–4793

    Article  CAS  PubMed  Google Scholar 

  • Hand SC, Menze MA, Toner M, Boswell L, Moore D (2011) LEA proteins during water stress: not just for plants anymore. Annu Rev Physiol 73:115–134

    Article  CAS  PubMed  Google Scholar 

  • Hatanaka R, Hagiwara-Komoda Y, Furuki T, Kanamori Y, Fujita M, Cornette R, Sakurai M, Okuda T, Kikawada T (2013) An abundant LEA protein in the anhydrobiotic midge, PvLEA4, act as a molecular shield by limiting growth of aggregating protein particles. Insect Biochem Mol Biol 43:1055–1067

    Article  CAS  PubMed  Google Scholar 

  • Hatanaka R, Gusev O, Cornette R, Shimura S, Kikuta S, Okada J, Okuda T, Kikawada T (2015) Diversity of the expression profiles of late embryogenesis abundant (LEA) protein encoding genes in the anhydrobiotic midge Polypedilum vanderplanki. Planta 242:451–459

    Article  CAS  PubMed  Google Scholar 

  • Hengherr S, Heyer AG, Köhler H-R, Schill RO (2008) Trehalose and anhydrobiosis in tardigrades – evidence for divergence in responses to dehydration. FEBS J 275:281–288

    Article  CAS  PubMed  Google Scholar 

  • Hincha DK, Thalhammer A (2012) LEA proteins: IDPs with versatile functions in cellular dehydration tolerance. Biochem Soc Trans 40:1000–1003

    Article  CAS  PubMed  Google Scholar 

  • Honjoh K, Matsumoto H, Shimizu H, Ooyama K, Tanaka K, Oda Y, Tanaka R, Joh T, Suga K, Miyamoto T, Ito M, Hatano S (2008) Cryoprotective activities of group 3 late embryogenesis abundant proteins from Chlorella vulgaris C-27. Biosci Biotechnol Biochem 64:1656–1663

    Article  Google Scholar 

  • Irudayam SJ, Berkowitz ML (2012) Binding and reorientation of melittin in a POPC bilayer: computer simulations. Biochim Biophys Acta 1818:2975–2981

    Article  CAS  PubMed  Google Scholar 

  • Jain NK, Roy I (2009) Effect of trehalose on protein structure. Protein Sci 18:24–36

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kawai H, Sakurai M, Inoue Y, Chûjô R (1992) Hydration of oligosaccharides: anomalous hydration ability of trehalose. Cryobiology 29:599–606

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki N, Furuki T, Sakurai M (2006) Molecular dynamics simulation on the glassy states of trehalose and neotrehalose. Cryobiol Cryotechnol 52:121–124

    Google Scholar 

  • Kikawada T, Nakahara Y, Kanamori Y, Iwata K, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochim Biophys Res Comm 384:56–61

    Article  Google Scholar 

  • Kilburn D, Townrow S, Meunier V, Richardson R, Alam A, Ubbink J (2006) Organization and mobility of water in amorphous and crystalline trehalose. Nat Mater 5:632–635

    Article  CAS  PubMed  Google Scholar 

  • Lapinski J, Tunnacliffe A (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett 553:387–390

    Article  CAS  PubMed  Google Scholar 

  • Li S, Chakraborty N, Botcar A, Menze MA, Toner M, Hand SC (2012) Late embryogenesis abundant proteins protect human hepatoma cells during acute desiccation. Proc Natl Acad Sci U S A 109:20859–20864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Zheng Y (2005) PM2, a group 3 LEA protein from soybean, and its 22-mer repeating region confer salt tolerance in Escherichia coli. Biochem Biophys Res Commun 331:325–332

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zheng Y, Zhang Y, Wang W, Li R (2010) Soybean PM2 protein (LEA3) confers the tolerance of Escherichia coli and stabilization of enzyme activity under diverse stresses. Curr Microbiol 60:373–378

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Chakrabortee S, Li R, Zheng Y, Tunnacliffe A (2011) Both plant and animal LEA proteins act as kinetic stabilizers of polyglutamine-dependent protein aggregation. FEBS Lett 585:630–634

    Article  CAS  PubMed  Google Scholar 

  • Magazú S, Villari V, Migliardo P, Maisano G, Telling MTF (2001) Diffusive dynamics of water in the presence of homologous disaccharides: a comparative study by quasi elastic neutron scattering. IV. J Phys Chem B 105:1851–1855

    Article  Google Scholar 

  • 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 1858:104–115

    Article  CAS  PubMed  Google Scholar 

  • Nagase H, Endo T, Ueda H, Nakagaki M (2002) An anhydrous polymorphic form of trehalose. Carbohydr Res 337:167–173

    Article  CAS  PubMed  Google Scholar 

  • Nagase H, Ogawa N, Endo T, Shiro M, Ueda H, Sakurai M (2008) Crystal structure of an anhydrous form of trehalose: structure of water channels of trehalose polymorphism. J Phys Chem B 112:9105–9111

    Article  CAS  PubMed  Google Scholar 

  • Nishimoto T, Furuta T, Sakurai M (2017) Study of desiccation-induced structural changes of G3LEA peptides using replica exchange molecular dynamics simulation. Cryobiol Cryotechnol 63:119–123

    Google Scholar 

  • Ohtake S, Wang YJ (2011) Trehalose: current use and future applications. J Pharm Sci 100:2020–2053

    Article  CAS  PubMed  Google Scholar 

  • Oku K, Watanabe H, Kubota M, Fukuda S, Kurimoto M, Tsujisaka Y, Komori M, Inoue Y, Sakurai M (2003) NMR and quantum chemical study on the OH∙∙∙π and CH∙∙∙O interactions between trehalose and unsaturated fatty acids. Implication for the mechanism of antioxidant function of trehalose. J Am Chem Soc 125:12739–12748

    Article  CAS  PubMed  Google Scholar 

  • Oku K, Kubota M, Fukuda S, Kurimoto M, Tsujisaka Y, Sakurai M (2004) Glass transition temperature of glycosyltrehalose. Cryobiol Cryotechnol 50:97–102

    Google Scholar 

  • Oliver AE, Hinacha DK, Crowe JH (2002) Looking beyond sugars: the role of amphiphilic solutes in preventing adventitious reactions in anhydrobiotes at low water contents. Comp Biochem Biophysiol 131A:515–525

    CAS  Google Scholar 

  • Perić-Hassler L, Hansen HS, Baron R, Hünenberger P (2010) Conformational properties of glucose-based disaccharides investigated using molecular dynamics simulations with local elevation umbrella sampling. Carbohydr Res 345:1781–1801

    Article  PubMed  Google Scholar 

  • Popova AV, Rausch S, Hundertmark M, Gibon Y, Hincha DK (2015) The intrinsically disordered protein LEA7 from Arabidopsis thaliana protects the isolated enzyme lactate dehydrogenase and enzymes in a soluble leaf proteome during freezing and drying. Biochim Biophys Acta 1854:1517–1525

    Article  CAS  PubMed  Google Scholar 

  • Portmann M-O, Birch G (1995) Sweet taste and solution properties of α,α,-trehalose. J Sci Food Agric 69:275–281

    Article  CAS  Google Scholar 

  • Pouchkina-Stantcheva NN, McGee BM, Boschetti C, Tolleter D, Chakrabortee S, Popova AV, Meersman F, Macherel D, Hincha DK, Tunnacliffe A (2007) Functional divergence of former alleles in an ancient asexual invertebrate. Science 318:268–271

    Article  CAS  PubMed  Google Scholar 

  • Sakakura K, Okabe A, Oku K, Sakurai M (2011) Experimental and theoretical study on the intermolecular complex formation between trehalose and benzene compounds in aqueous solution. J Phys Chem B 115:9823–9830

    Article  CAS  PubMed  Google Scholar 

  • Sakurai M (2009) Biological functions of trehalose as a substitute for water. In: Kuwajima K, Goto Y, Hirata F, Kataoka M, Terazima M (eds) Water and biomolecules: physical chemistry of life phenomena. Springer, Berlin, pp 219–241

    Chapter  Google Scholar 

  • Sakurai M, Furuki T, Akao K, Tanaka D, Nakahara Y, Kikawada T, Watanabe M, Okuda T (2008) Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. Proc Natl Acad Sci U S A 105:5093–5098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shih M-D, Hoekstra FA, Hsing YC (2008) Late embryogenesis abundant proteins. Adv Bot Res 48:212–255

    Google Scholar 

  • Shimizu T, Kanamori Y, Furuki T, Kikawada T, Okuda T, Takahashi T, Mihara H, Sakurai M (2010) Desiccation-induced structuralization and glass formation of Group-3 late embryogenesis abundant (G3LEA) protein model peptides. Biochemistry 49:1093–1104

    Article  CAS  PubMed  Google Scholar 

  • Shiraga K, Suzuki T, Kondo N, De Baerdemaeker J, Ogawa Y (2015) Quantitative characterization of hydration state and destructuring effect of monosaccharides and disaccharides on water hydrogen bond network. Carbohydr Res 406:46–54

    Article  CAS  PubMed  Google Scholar 

  • Shrödinger E (1967) What is life? Cambridge University Press, Cambridge, pp 67–75

    Google Scholar 

  • Tolleter D, Hincha DK, Macherel D (2010) A mitochondrial late embryogenesis abundant protein stabilized model membranes in the dry state. Biochim Biophys Acta 1798:1926–1933

    Article  CAS  PubMed  Google Scholar 

  • Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschafften 94:791–812

    Article  CAS  Google Scholar 

  • Tunnacliffe A, Hincha DK, Leprince O, Macherel D (2010) LEA proteins: versatility of form and function. In: Lubzens E, Cerdà J, Clark MS (eds) Dormancy and resistance in harsh environments. Springer-Verlag, Berlin, pp 91–108

    Chapter  Google Scholar 

  • Uedaira H, Ikura M, Uedaira H (1989) Natural-abundance oxygen-17 magnetic relaxation in aqueous solutions of carbohydrates. Bull Chem Soc Jpn 62:1–4

    Article  CAS  Google Scholar 

  • Usui M, Furuki T, Furuta T, Sakuirai M (2014) Analysis of group 3 LEA model peptide-protein interactions by molecular dynamics simulation. Cryobiol Cryotechnol 60:89–92

    Google Scholar 

  • Uversky VN, Gillespie JR, Fink AL (2000) Why are “natively unfolded” proteins unstructured under physiologic conditions? Proteins 41:415–427

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Kikawada T, Minagawa N, Yukuhiro F, Okuda T (2002) Mechanism allowing an insect to survive complete dehydration and extreme temperatures. J Exp Biol 205:2799–2802

    CAS  PubMed  Google Scholar 

  • Watanabe M, Kikawada T, Okuda T (2003) Increase of internal ion concentration triggers trehalose synthesis associated with cryptobiosis in larvae of Polypedilum vanderplanki. J Exp Biol 206:2281–2286

    Article  CAS  PubMed  Google Scholar 

  • Wise J, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9:13–17

    Article  CAS  PubMed  Google Scholar 

  • Wolkers WF, McCready S, Brandt W, Lindsey GG, Hoekstra FA (2001) Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochim Biophys Acta 1544:196–206

    Article  CAS  PubMed  Google Scholar 

  • Yamakawa K, Furuki T, Furuta T, Hatanaka R, Kikawada T, Niwa T, Taguchi H, Furusawa H, Okahata Y, Sakurai M (2013) Experimental study on the mechanism underlying the anti-aggregation function of a group 3 LEA peptide. Cryobiol Cryotechol 59:95–99

    Google Scholar 

Download references

Acknowledgments

This work was supported in part by JSPS KAKENHI JP15H02378.

Author information

Authors and Affiliations

  1. Center for Biological Resources and Informatics, Tokyo Institute of Technology, Yokohama, Japan

    Takao Furuki & Minoru Sakurai

Authors
  1. Takao Furuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Minoru Sakurai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Minoru Sakurai .

Editor information

Editors and Affiliations

  1. Faculty of Agriculture, Kyushu University, Fukuoka, Japan

    Mari Iwaya-Inoue

  2. Center for Biological Resources and Informatics, Tokyo Institute of Technology, Yokohama, Japan

    Minoru Sakurai

  3. United Graduate School of Agricultural Sciences and Department of Plant-biosciences, Faculty of Agriculture, Iwate University, Morioka, Japan

    Matsuo Uemura

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Furuki, T., Sakurai, M. (2018). Physicochemical Aspects of the Biological Functions of Trehalose and Group 3 LEA Proteins as Desiccation Protectants. In: Iwaya-Inoue, M., Sakurai, M., Uemura, M. (eds) Survival Strategies in Extreme Cold and Desiccation. Advances in Experimental Medicine and Biology, vol 1081. Springer, Singapore. https://doi.org/10.1007/978-981-13-1244-1_15

Download citation

Publish with us

Policies and ethics

Search

Navigation