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Anhydrobiosis: An Unsolved Problem with Applications in Human Welfare

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Book cover Membrane Hydration

Part of the book series: Subcellular Biochemistry ((SCBI,volume 71))

Abstract

Anhydrobiosis (Life Without Water) has been known for millennia, but the underlying mechanisms have not been understood until recent decades, and we have achieved only a partial understanding. One of the chief sites of damage from dehydration is membranes, and we and others have provided evidence that this damage may be obviated by the production of certain sugars, particularly trehalose. The sugar stabilizes membranes by preventing fusion and fluidizing the dry bilayers. The mechanism by which this is accomplished has been controversial, and I review that controversy here. In the past decade evidence is accumulating for a role of stress proteins in addition to or as a substitute for trehalose. Genomic studies on anhydrobiotes are yielding rapid progress. Also in the past decade, numerous uses for trehalose in treating human diseases have been proposed, some of which are in clinical testing. I conclude that the mechanisms underlying anhydrobiosis are more complex than we thought 20 years ago, but progress is being made towards elucidating those mechanisms.

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References

  • Abusharkh SE, Erkut C, Oertel J, Kurzchalia TV, Fahmy K (2014) The role of phospholipid headgroup composition and trehalose in the desiccation tolerance of Caenorhabditis elegans. Langmuir 30:12897–12906

    Article  CAS  PubMed  Google Scholar 

  • Andersen HD, Wanga C, Arleth L, Peters GH, Westh P (2011) Reconciliation of opposing views on membrane–sugar interactions. Proc Natl Acad Sci U S A 108:1874–1878

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Arai C, Kohguchi C, Akamatsu S, Arai N, Yoshizane C, Hasegawa N, Hanaya T, Arai S, Ikeda M, Kuromoto M (2001) Trehalose suppresses lipopolysaccharide-induced osteoclastogenesis bone marrow in mice. Nutr Res 21:993–999

    Article  CAS  PubMed  Google Scholar 

  • Auh J-H, Wolkers WF, Looper SA, Walker NJ, Crowe JH, Tablin F (2004) Calcium mobilization in freeze-dried human platelets. Cell Preserv Technol 2:180–187

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bryant G, Wolfe J (1992) Interfacial forces in cryobiology and anhydrobiology. Cryo-Letters 13:23–36

    Google Scholar 

  • Bryant G, Koster KL, Wolfe J (2001) Membrane behaviour in seeds and other systems at low water content: the various effects of solutes. Seed Sci Res 11:17–25

    Article  CAS  Google Scholar 

  • Čejková J, Ardan T, Čejka Č, Luyckx J (2011) Favorable effects of trehalose on the development of UVB-mediated antioxidant/pro-oxidant imbalance in the corneal epithelium, proinflammatory cytokine and matrix metalloproteinase induction, and heat shock protein 70 expression. Graefes Arch Clin Exp Ophthalmol 249:1185–1194

    Article  PubMed  Google Scholar 

  • Chandrasekhar I, Gaber BP (1988) Stabilization of the biomembrane by small molecules: interaction of trehalose with the phospholipid bilayer. J Biomol Struct Dyn 5:1163–1171

    Article  CAS  PubMed  Google Scholar 

  • Cottone G, Cicotti G, Cordone L (2002) Protein-trehalose-water structures in trehalose coated carboxy-myoglobn. J Cell Phys 117:9862–9866

    CAS  Google Scholar 

  • Couzin J (2004) Huntington’s disease. Unorthodox clinical trials meld science and care. Science 304:816–817

    Article  PubMed  Google Scholar 

  • Crowe JH (1971) Anhydrobiosis: an unsolved problem. Am Nat 105:563–574

    Article  Google Scholar 

  • Crowe JH (2008) Trehalose as a “chemical chaperone”: fact and fantasy. Adv Exp Med Biol 594:143–158

    Article  Google Scholar 

  • Crowe LM, Crowe JH (1991) Solution effects on the thermotropic phase transition of unilamellar liposomes. Biochim et Biophys Acta – Biomembr 1064:267–274

    Article  CAS  Google Scholar 

  • Crowe JH, Crowe LM, Chapman D (1984) Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 1984(223):701–703

    Article  Google Scholar 

  • Crowe JH, Spargo BJ, Crowe LM (1987) Preservation of dry liposomes does not require retention of residual water. Proc Natl Acad Sci U S A 84:1537–1540

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 6:73–103

    Article  Google Scholar 

  • Dupont S, Rapoport A, Gervais P, Beney L (2014) Survival kit of Saccharomyces cerevisiae for anhydrobiosis. Appl Microbiol Biotechnol 98:8821–8834

    Article  CAS  PubMed  Google Scholar 

  • Eleutherio ECA, Araujo PS, Panek AD (1993) Role of the trehalose carrier in dehydration resistance of Saccharomyces cerevisiae. Biochim Biophys Acta 1156:263–266

    Article  CAS  PubMed  Google Scholar 

  • Emanuele E (2014) Can trehalose prevent neurodegeneration? Insights from experimental studies. Curr Drug Targets 15:551–557

    Article  CAS  PubMed  Google Scholar 

  • Erkut C, Penkov S, Khesbak H, Vorkel D, Verbavatz JM, Fahmy K, Kurzchalia TV (2011) Trehalose renders the dauer larva of Caenorhabditis elegans resistant to extreme desiccation. Curr Biol 21:1331–1336

    Article  CAS  PubMed  Google Scholar 

  • Erkut C, Vasilj A, Boland S, Habermann B, Shevchenko A, Kurzchalia TV (2013) Molecular strategies of the Caenorhabditis elegans dauer larva to survive extreme desiccation. PLoS One 8:e82473

    Article  PubMed Central  PubMed  Google Scholar 

  • Förster F, Beisser D, Grohme MA, Liang C, Mali B, Sieg AM, Engelmann JC, Shkumatov AV, Schokraie E (2012) Transcriptome analysis in tardigrade species reveals specific molecular pathways for stress adaptations. Bioinf Biol Insights 2012:69–95

    Google Scholar 

  • Gadducci A, Fanucchi A, Cosio S, Genazzani AR (1997) Hormone replacement therapy and gynecological cancer. Anticancer Res 17:3793–3798

    CAS  PubMed  Google Scholar 

  • Gaff DF, Oliver M (2013) The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct Plant Biol 40:315–328

    Article  Google Scholar 

  • Golovina EA, Golovin A, Hoekstra FA, Faller R (2010) Water replacement hypothesis in atomic details: effect of trehalose on the structure of single dehydrated POPC bilayers. Langmuir 26:11118–11126

    Article  CAS  PubMed  Google Scholar 

  • Hand SC, Menze MA (2015) Molecular approaches for improving desiccation tolerance: insights from the brine shrimp Artemia franciscana. Planta (in press)

    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 447:115–134

    Article  Google Scholar 

  • Hays LM, Crowe JH, Wolkers W (2001) Factors affecting leakage of trapped solutes from phospholipid vesicles during thermotropic phase transitions. Cryobiology 42:88–102

    Article  CAS  PubMed  Google Scholar 

  • Hengherr S, Worland MR, Reuner A, Brümmer F, Schill RO (2009) High-temperature tolerance in anhydrobiotic tardigrades is limited by glass transition. Physiol Biochem Zool 82:749–755

    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 

  • Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438

    Article  CAS  PubMed  Google Scholar 

  • Hovakimyan M, Ramoth T, Löbler M, Schmitz K, Witt M, Guthoff R, Stachs O (2012) Evaluation of protective effects of trehalose on desiccation of epithelial cells in three dimensional reconstructed human corneal epithelium. Curr Eye Res 37(982–989):2012

    Google Scholar 

  • Izawa YT, Matsuo T, Uchida T (2006) Atomic force microscopic observation of trehalose-treated and dried corneal epithelial Surface. Cell Preserv Tech 4:117–122

    Article  CAS  Google Scholar 

  • Keilin D (1959) The problem of anabiosis or latent life: history and current concept. Proc Roy Soc B 150:149–191

    Article  CAS  Google Scholar 

  • Kent B, Hunt T, Darwish TA, Hauß T, Garvey CJ, Bryant G (2014) Localization of trehalose in partially hydrated DOPC bilayers: insights into cryoprotective echanisms. J R Soc Interface 11:20140069

    Article  PubMed Central  PubMed  Google Scholar 

  • Koster KL (2001) Effects of sugars on phospholipid phase transitions: relevance to dehydration tolerance. Cryobiol Cryotechnol 47:26–32

    Google Scholar 

  • Koster KL, Kami AE, Maddocks J, Bryant G (2003) Exclusion of maltodextrins from phosphatidylcholine multilayers during dehydration: effects on membrane phase behavior. Eur Biophys J 32:96–105

    CAS  PubMed  Google Scholar 

  • Krügera UY, Wanga Y, Kumara S, Mandelkowa E (2012) Autophagic degradation of tau in primary neurons and its enhancement by trehalose. Neurobiol Aging 33:2291–2305

    Article  Google Scholar 

  • Lan D, Liu F, Zhao J, Chen Y, Wu J, Ding Z, Yue Z, Ren H, Jiang Y, Wang J (2012) Effect of trehalose on PC12 cells overexpressing wild-type or A53T mutant a-synuclein. Neurochem Res 37:2025–2032

    Article  CAS  PubMed  Google Scholar 

  • Lee CWB, Waugh JS, Griffin RG (1986) Solid-state NMR study of trehalose/1,2-dipalmitoyl-sn-phosphatidylcholine interactions. Biochemistry 25:3737–3742

    Article  CAS  PubMed  Google Scholar 

  • Leidy C, Gousset K, Ricker JV, Crowe JH (2004) Lipid phase behavior and stabilization of domains in membranes of platelets. Cell Biochem Biophys 40:123–135

    Article  CAS  PubMed  Google Scholar 

  • Lenné T, Garvey CJ, Koster KL, Bryant G (2009) Effects of sugars on lipid bilayers during dehydration – SAXS/WAXS measurements and quantitative model. J Phys Chem B 113:2486–2491

    Article  PubMed  Google Scholar 

  • Leprince O, Buitink J (2010) Desiccation tolerance: from genomics to the field. Plant Sci 179:554–564

    Article  CAS  Google Scholar 

  • Li S, Chakraborty N, Borcara 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Lins RD, Pereira CS, Hunenberger PH (2004) Trehalose-protein interactions in aqueous solutions. Proteins 55:177–186

    Article  CAS  PubMed  Google Scholar 

  • Liu R, Barkhordarian H, Emadi S, Park CB, Sierks MR (2005) Trehalose differentially inhibits aggregation and neurotoxicity of beta-amyloid 40 and 42. Neurobiol Dis 20:74–81

    Article  PubMed  Google Scholar 

  • Luyckx J, Baudouin C (2011) Trehalose: an intriguing disaccharide with potential for medical application in ophthalmology. Clin Ophthamol 5:577–581

    CAS  Google Scholar 

  • Luzardo MC, Amalfa F, Nuñez AM, Díaz S, Biondi AC, Disalvo EA (2000) Effect of trehalose and sucrose on the hydration and dipole potential of lipid bilayers. Biophys J 78:2452–2458

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ma X, Jamil K, Macrae TH, Clegg JS, Russell JM, Villeneuve TS, Euloth M, Sun Y, Crowe JH, Tablin F, Oliver AE (2005) A small stress protein acts synergistically with trehalose to confer desiccation tolerance on mammalian cells. Cryobiology 51:15–28

    Article  CAS  PubMed  Google Scholar 

  • Matsuo T (2004) Trehalose versus hyaluronan or cellulose in eye drops for the treatment of dry eye. Jpn J Ophthalmol 48:321–327

    Article  CAS  PubMed  Google Scholar 

  • Mitsumasu K, Kanamori Y, Fujita M, Iwata K, Tanaka D, Kikuta S, Watanabe M, Cornette R, Okuda T, Kikawada T (2010) Enzymatic control of anhydrobiosis related accumulation of trehalose in the sleeping chironomid, Polypedilum vanderplanki. FEBS J 277:4215–4228

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Moiset G, López CA, Bartelds R, Syga L, Rijpkema E, Cukkemane A, Baldus M, Poolman B, Marrink SJ (2014) Disachrides impact the lateral organization of lipid membranes. J Am Chem Soc 136:16167–16175

    Article  CAS  PubMed  Google Scholar 

  • Nakagaki M, Nagase H, Ueda H (1992) Stabilization of the lamellar structure of phosphatidylcholine by complex-formation with trehalose. J Membr Sci 73:173–180

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ricker JV, Tsvetkova NM, Wolkers WF, Crowe JH (2003) Trehalose maintains phase separation in an air-dried binary lipid mixture. Biophys J 84:3045–3051

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rudolph BR, Chandrasekhar I, Gaber BP (1990) Molecular modeling of saccharide-lipid interactions. Chem Phys Lipids 53:243–261

    Article  CAS  Google Scholar 

  • Schebor C, Burin L, del Pilar Bueras M (1999) Stability to hydrolysis and browning of trehalose, sucrose and raffinose in low-moisture systems in relation to their use as protectants of dry biomaterials. Food Sci Technol 32:481–485

    CAS  Google Scholar 

  • Sum AK, Faller R, de Pablo JJ (2003) Molecular simulation of phospholipid bilayers and insights of the interactions with disaccharides. Biophys J 2003(85):2830–2844

    Article  Google Scholar 

  • Takeuchi K, Nakazawa M, Ebina Y, Sato K, Metoki T, Miyagawa Y, Ito T (2010) Inhibitory effects of trehalose on fibroblast proliferation and implications for ocular surgery. Exp Eye Res 91:567–577

    Article  CAS  PubMed  Google Scholar 

  • Tanaka M, Machida Y, Niu S (2004) Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease. Nat Med 2004(10):148–154

    Article  Google Scholar 

  • Tapia H, Koshland DE (2014) Trehalose is a versatile and long-lived chaperone for desiccation tolerance. Curr Biol 24:2758–2766

    Article  CAS  PubMed  Google Scholar 

  • Terrasson E, Buitink J, Righetti K, Vu BY, Pelletier S, Zinsmeister J, Lalanne D, Leprince O (2013) An emerging picture of the seed desiccome: confirmed regulators and newcomers identified using transcriptome comparison. Front Plant Sci 4:497

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tolleter D, Jaquinode M, Mangavel A, Passirani C, Saulnier P, Manon S, Teyssier E, Payet N, Avelange-Macherel MH, Macherel D (2007) Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. Plant Cell 19:1580–1589

    Google Scholar 

  • Tomczak MM, Hincha DK, Estrada SD, Wolkers WF, Crowe LM, Feeney RE, Tablin F, Crowe JH (2002) A mechanism for stabilization of membranes at low temperatures by an antifreeze protein. Biophys J 82:874–881

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Torok Z, Tsvetkova NM, Gabor B, Horváth I, Nagy E, Pénzes Z, Hargitai J, Bensaude O, Csermely P, Crowe JH, Maresca B, Vígh L (2003) Heat shock protein co-inducers specifically modulate the membrane lipid phase. Proc Natl Acad Sci U S A 100:3131–3136

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tsvetkova NM, Phillips BL, Crowe LM, Crowe JH (1998) Effect of sugars on headgroup mobility in freeze-dried dipalmitoylphosphatidylcholine bilayers: solid-state P-31 NMR and FTIR studies. Biophys J 75:2947–2955

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tunnacliffe A, Lapinski J, McGee B (2005) A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546:315–321

    Article  CAS  Google Scholar 

  • Tunnacliffe A, Hincha DK, Leprince O, Macherel D (2010) LEA proteins: versatility of form and function. In: Lubzens E, Cerda J, Clark M (eds) Sleeping beauties: dormancy and resistance in harsh environments. Springer, Berlin, pp 91–108

    Chapter  Google Scholar 

  • Vessey MP (1984) Exogenous hormones in the aetiology of cancer in women. J R Soc Med 77:542–549

    PubMed Central  CAS  PubMed  Google Scholar 

  • Viera LI, Alonso-Romanowski S, Borovyagin V, Feliz MR, Disalvo EA (1993) Properties of gel phase lipid-trehalose bilayers upon rehydration. Biochim Biophys Acta 1145:157–167

    Article  CAS  PubMed  Google Scholar 

  • Villarreal MA, Díaz SB, Disalvo EA, Montich GG (2004) Molecular dynamics simulation study of the interaction of trehalose with lipid membranes. Langmuir 20:7844–7851

    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 

  • Wharton DA (2014) Anhydrobiosis: the model worm as a model. Curr Biol 21:R578

    Article  Google Scholar 

  • Wolkers WF, Oldenhof H, Alberda M, Hoekstra FA (1998) A fourier transform infrared study of sugar glasses: application to anhydrobiotic higher plant cells. Biochim Biophys Acta 1379:83–96

    Article  CAS  PubMed  Google Scholar 

  • Wolkers WF, Walker NJ, Tablin F, Crowe JH (2001) Human platelets loaded with trehalose survive freeze-drying. Cryobiology 42:79–87

    Article  CAS  PubMed  Google Scholar 

  • Zhu S, Jamil K, Ma X, Crowe JH, Oliver AE (2006) Protection of CANARY cells after drying and rehydration correlates with decrease in apoptotic cell death. Cell Preserv Technol 4:67–77

    Article  CAS  Google Scholar 

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  1. Department of Molecular and Cellular Biology, University of California, Davis, CA, 95618, USA

    John H. Crowe

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Correspondence to John H. Crowe .

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  1. Laboratorio de Biointerfases y Sistemas Biomimeticos; Centro de Investigacion y Transferencia de Santiago del Estero, Universidad Nacional de Santiago del Estero-Consejo Nacional de Investigaciones Científicas y Técnicas, El Zanjón, Santiago del Estero, Argentina

    E. Anibal Disalvo

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Crowe, J.H. (2015). Anhydrobiosis: An Unsolved Problem with Applications in Human Welfare. In: Disalvo, E. (eds) Membrane Hydration. Subcellular Biochemistry, vol 71. Springer, Cham. https://doi.org/10.1007/978-3-319-19060-0_11

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