Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid

Kikawada, Takahiro; Nakahara, Yuko; Kanamori, Yasushi; Iwata, Ken-ichi; Watanabe, Masahiko; McGee, Brian; Tunnacliffe, Alan; Okuda, Takashi

doi:10.1016/j.bbrc.2006.07.003

Cited by 182 publications

(118 citation statements)

References 14 publications

Supporting

Mentioning

115

Contrasting

Order By: Relevance

“…Expression of Tret1 also was induced by hypersalinity, supporting our hypothesis that salinity stress can mimic desiccation in its effects on larval gene transcription (26). The extraordinarily high values for both K m and V max for trehalose are physiologically reasonable because TRET1 can retain a high capacity for transport activity even when trehalose is highly concentrated in the dehydrating larval body during the final stage of entry into anhydrobiosis (23)(24)(25).…”

Section: Discussionmentioning

confidence: 52%

“…Candidates for trehalose transporter genes were identified in our original P. vanderplanki EST (Pv-EST) database by using total RNA from larvae desiccated for 0, 12, or 36 h (26). We then identified a subset of six EST clones that form a single cluster annotated as a sugar transporter [supporting information (SI) Fig.…”

Section: Molecular Cloning Of the Tret1mentioning

confidence: 99%

“…In the Pv-EST database (26), six EST clones annotated as sugar transporter-like genes were assembled into one cluster designated as Tret1 (SI Fig. 8).…”

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells

Kikawada

Saito

Kanamori

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

218

211

View full text Add to dashboard Cite

Trehalose is potentially a useful cryo-or anhydroprotectant molecule for cells and biomolecules such as proteins and nucleotides. A major obstacle to application is that cellular membranes are impermeable to trehalose. In this study, we isolated and characterized the functions of a facilitated trehalose transporter [trehalose transporter 1 (TRET1)] from an anhydrobiotic insect, Polypedilum vanderplanki. Tret1 cDNA encodes a 504-aa protein with 12 predicted transmembrane structures. Tret1 expression was induced by either desiccation or salinity stress. Expression was predominant in the fat body and occurred concomitantly with the accumulation of trehalose, indicating that TRET1 is involved in transporting trehalose synthesized in the fat body into the hemolymph. Functional expression of TRET1 in Xenopus oocytes showed that transport activity was stereochemically specific for trehalose and independent of extracellular pH (between 4.0 and 9.0) and electrochemical membrane potential. These results indicate that TRET1 is a trehalose-specific facilitated transporter and that the direction of transport is reversible depending on the concentration gradient of trehalose. The extraordinarily high values for apparent K m (>100 mM) and Vmax (>500 pmol/min per oocyte) for trehalose both indicate that TRET1 is a high-capacity transporter of trehalose. Furthermore, TRET1 was found to function in mammalian cells, suggesting that it confers trehalose permeability on cells, including those of vertebrates as well as insects. These characteristic features imply that TRET1 in combination with trehalose has high potential for basic and practical applications in vivo.anhydrobiosis ͉ insect ͉ trehalose transport ͉ Polypedilum vanderplanki dessication-inducible gene

show abstract

Section: Discussionmentioning

confidence: 52%

Section: Molecular Cloning Of the Tret1mentioning

confidence: 99%

See 1 more Smart Citation

Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells

Kikawada

Saito

Kanamori

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

218

211

View full text Add to dashboard Cite

show abstract

“…Among these, we isolated three cDNA-encoding proteins (PvLEA1, PvLEA2, and PvLEA3) with highly significant matches to group 3 LEA proteins. Both mRNA and protein levels of all three candidates were increased by dehydration stress imposed by either desiccation or hypersalinity (48). Further characterization of these LEA proteins showed that all of them did not aggregate after boiling treatment.…”

Section: Late Embryogenesis Abundant Proteinsmentioning

confidence: 98%

The induction of anhydrobiosis in the sleeping chironomid: Current status of our knowledge

2011

Self Cite

View full text Add to dashboard Cite

An African chironomid, Polypedilum vanderplanki, is the only insect known to be capable of extreme desiccation tolerance, or anhydrobiosis. In the 1950s and 1960s, Hinton strenuously studied anhydrobiosis in this insect from a physiological standpoint; however, nobody has afterward investigated the phenomenon. In 2000, research on mechanisms underlying anhydrobiosis was resumed due to successful establishment of a rearing system for P. vanderplanki. This review is focused on the latest findings on the physiological and molecular mechanisms underlying the induction of anhydrobiosis in P. vanderplanki. Early experiments demonstrated that the induction of anhydrobiosis was possible in isolated tissues and independent from the control of central nervous system. However, to achieve successful anhydrobiosis, larvae need a slow regime of desiccation, allowing them to synthesize molecules, which will protect cells and tissues against the deleterious effects of dehydration. Trehalose, a nonreducing disaccharide, which accumulates in P. vanderplanki larvae up to 20% of the dry body mass, is thought to replace the water in its tissues. Similarly, highly hydrophilic proteins called the late embryogenesis abundant (LEA) proteins are expressed in huge quantities and act as a molecular shield to protect biological molecules against aggregation and denaturation. This function is shared by heat shock proteins, which are also upregulated during the desiccation process. At the same time, desiccating larvae express various antioxidant molecules and enzymes, to cope with the massive oxidative stress, which is responsible for general damage to membranes, proteins, and DNA in dehydrating cells. Finally, specific water channels, called aquaporins, accelerate dehydration, and trehalose together with LEA proteins forms a glassy matrix, which protects the biological molecules and the structural integrity of larvae in the anhydrobiotic state. © 2011 IUBMB IUBMB Life, 63(6): 419–429, 2011

show abstract

“…LEA proteins were first discovered in maturing plant seeds (Dure et al 1981) and have since been found in desiccation-tolerant cyanobacter (Close and Lammers 1993), bacteria and Archaea (Campos et al 2013), nematodes (Browne et al 2002;Gal et al 2004;Goyal et al 2005a;Erkut et al 2013), rotifers (Tunnacliffe et al 2005), an insect (Kikawada et al 2006;Hatanaka et al 2013), and a crustacean (Hand et al 2007;Sharon et al 2009). LEA proteins are induced by and mediate the effects of dehydration/ rehydration (Gal et al 2004;Tunnacliffe et al 2005;Kikawada et al 2006), osmotic stress (Close and Lammers 1993; Gal et al 2004;Kikawada et al 2006), temperature fluctuation (Gal et al 2004), and freezing-thawing (Hand et al 2011;Campos et al 2013;Toxopeus et al 2014). Protein aggregation is inhibited by LEA proteins, either by chaperoning (Grelet et al 2005) or more probably by molecular shielding, the formation of electrostatic and/or physical barriers that prevent protein interactions (Goyal et al 2005b;Chakrabortee et al 2011;Hatanaka et al 2013).…”

Section: Lea Proteins and Desiccation Tolerance In Artemia Cystsmentioning

confidence: 99%

Stress tolerance during diapause and quiescence of the brine shrimp, Artemia

MacRae

2016

Cell Stress and Chaperones

View full text Add to dashboard Cite

Oviparously developing embryos of the brine shrimp, Artemia, arrest at gastrulation and are released from females as cysts before entering diapause, a state of dormancy and stress tolerance. Diapause is terminated by an external signal, and growth resumes if conditions are permissible. However, if circumstances are unfavorable, cysts enter quiescence, a dormant stage that continues as long as adverse conditions persist. Artemia embryos in diapause and quiescence are remarkably resistant to environmental and physiological stressors, withstanding desiccation, cold, heat, oxidation, ultraviolet radiation, and years of anoxia at ambient temperature when fully hydrated. Cysts have adapted to stress in several ways; they are surrounded by a rigid cell wall impermeable to most chemical compounds and which functions as a shield against ultraviolet radiation. Artemia cysts contain large amounts of trehalose, a non-reducing sugar thought to preserve membranes and proteins during desiccation by replacing water molecules and/or contributing to vitrification. Late embryogenesis abundant proteins similar to those in seeds and other anhydrobiotic organisms are found in cysts, and they safeguard cell organelles and proteins during desiccation. Artemia cysts contain abundant amounts of p26, a small heat shock protein, and artemin, a ferritin homologue, both ATPindependent molecular chaperones important in stress tolerance. The evidence provided in this review supports the conclusion that it is the interplay of these protective elements that make Artemia one of the most stress tolerant of all metazoan organisms.

show abstract

Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid

Cited by 182 publications

References 14 publications

Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells

Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells

The induction of anhydrobiosis in the sleeping chironomid: Current status of our knowledge

Stress tolerance during diapause and quiescence of the brine shrimp, Artemia

Contact Info

Product

Resources

About