Effects of three stabilizing agents—Proline, betaine, and trehalose—on membrane phospholipids

Rudolph, Alan S.; Crowe, John H.; Crowe, Lois M.

doi:10.1016/0003-9861(86)90197-9

Cited by 250 publications

(117 citation statements)

References 21 publications

Supporting

Mentioning

110

Contrasting

Unclassified

Order By: Relevance

“…Proline can also stabilize the native structure of protein monomers in aquaeous solutions and protect oligomeric protein complexes from denaturation and dissociation caused by low temperatures and freeze/thaw cycles (32,33). In addition, proline molecules can intercalate between the headgroups of membrane phospholipids during freeze dehydration and alleviate mechanical stresses in the membranes or can disturb the membranes, making them less prone to the liquid crystallineto-gel transition (34,35).…”

Section: Feeding Larvae Proline-augmented Diet Results In Accumulatiomentioning

confidence: 99%

Conversion of the chill susceptible fruit fly larva ( Drosophila melanogaster ) to a freeze tolerant organism

Košťál

Šimek

Zahradníčková

et al. 2012

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

138

View full text Add to dashboard Cite

Among vertebrates, only a few species of amphibians and reptiles tolerate the formation of ice crystals in their body fluids. Freeze tolerance is much more widespread in invertebrates, especially in overwintering insects. Evolutionary adaptations for freeze tolerance are considered to be highly complex. Here we show that surprisingly simple laboratory manipulations can change the chill susceptible insect to the freeze tolerant one. Larvae of Drosophila melanogaster, a fruit fly of tropical origin with a weak innate capacity to tolerate mild chilling, can survive when approximately 50% of their body water freezes. To achieve this goal, synergy of two fundamental prerequisites is required: (i) shutdown of larval development by exposing larvae to low temperatures (dormancy) and (ii) incorporating the free amino acid proline in tissues by feeding larvae a proline-augmented diet (cryopreservation).insect cold tolerance | long-term storage | metabolomics | cryoprotection | quiescence T he vast majority of insect lineages and species evolved, diversified, and recently live in warm lowland tropics, where seasonal and daily temperatures fluctuate little. This scenario is also true for the genus Drosophila, which contains almost 1,500 described species (1) including a common model of modern biology, the fruit fly Drosophila (Sophophora) melanogaster (Meigen, 1830) (fruit fly in further text). The ancestral members of this genus were adapted to warm temperatures (2), and most of the extant species still have tropical and/or subtropical distributions and are chill susceptible (3). The immature development of D. melanogaster halts at temperatures below 10°C (4), chill injury occurs below 6°C (5), and all developmental stages die when chilled (supercooled) below −5°C for just a few hours (6). The ability to tolerate freezing; i.e., formation of ice crystals in body fluids, is unknown in any Drosophila species (2, 5).Numerous insect lineages, including some drosophilid flies, colonized colder environments in higher altitudes or temperate and polar regions. Such lineages had to overcome selection pressures of shorter growing season, exaggerated daily temperature fluctuations, and seasonal drop of temperatures below the physiological thresholds for activity, growth, and development (7). It is now widely accepted that cold adaptation in insects is highly complex and requires adjustments at all levels of biological organization (8-16). Supercooling and freeze tolerance are two main strategies that help insects to cope with the risk of water freezing in a cryothermic state. While the capacity for supercooling seems to be basal in cold-adapted arthropod lineages, freeze tolerance probably converged in several groups in response to either severe Arctic winters or unpredictable subzero temperature events typical of cold habitats in the southern hemisphere (17, 18). For example, larvae of subarctic drosophilid fly, Chymomyza costata (Zetterstedt, 1838) are extremely freeze tolerant and may even survive after submergence in liquid nitro...

show abstract

Section: Feeding Larvae Proline-augmented Diet Results In Accumulatiomentioning

confidence: 99%

Conversion of the chill susceptible fruit fly larva ( Drosophila melanogaster ) to a freeze tolerant organism

Košťál

Šimek

Zahradníčková

et al. 2012

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

138

View full text Add to dashboard Cite

show abstract

“…64 Trehalose is also thought to increase the cytoplasmic viscosity, thus decreasing the possibility of formation of intracellular ice crystals which are often fatal. 65 …”

Section: Glass Transition Temperaturementioning

confidence: 99%

Effect of trehalose on protein structure

Jain¹,

Roy²

2008

Protein Science

714

576

View full text Add to dashboard Cite

Trehalose is a ubiquitous molecule that occurs in lower and higher life forms but not in mammals. Till about 40 years ago, trehalose was visualized as a storage molecule, aiding the release of glucose for carrying out cellular functions. This perception has now changed dramatically. The role of trehalose has expanded, and this molecule has now been implicated in a variety of situations. Trehalose is synthesized as a stress-responsive factor when cells are exposed to environmental stresses like heat, cold, oxidation, desiccation, and so forth. When unicellular organisms are exposed to stress, they adapt by synthesizing huge amounts of trehalose, which helps them in retaining cellular integrity. This is thought to occur by prevention of denaturation of proteins by trehalose, which would otherwise degrade under stress. This explanation may be rational, since recently, trehalose has been shown to slow down the rate of polyglutamine-mediated protein aggregation and the resultant pathogenesis by stabilizing an aggregation-prone model protein. In recent years, trehalose has also proved useful in the cryopreservation of sperm and stem cells and in the development of a highly reliable organ preservation solution. This review aims to highlight the changing perception of the role of trehalose over the last 10 years and to propose common mechanisms that may be involved in all the myriad ways in which trehalose stabilizes protein structures. These will take into account the structure of trehalose molecule and its interactions with its environment, and the explanations will focus on the role of trehalose in preventing protein denaturation.

show abstract

“…Betaine is a stabilizing or salting-in agent (Yancey et al 1982), and it might act by preventing the aggregation of cellular proteins and, hence, maintaining their solubility or by altering the physical properties of cellular membranes, or both. In an artificial membrane system, 1 kmol m -3 betaine lowered the temperature of the phase transition from a liquid-crystalline state to the gel state (Rudolph, Crowe & Crowe 1986;Rudolph & Goins 1991). …”

mentioning

confidence: 98%

Transformation with a gene for choline oxidase enhances the cold tolerance of Arabidopsis during germination and early growth

Alia¹,

Hayashi

Chen

et al. 1998

Plant Cell & Environment

View full text Add to dashboard Cite

We transformed Arabidopsis thaliana with the codA gene from Arthrobacter globiformis. This gene encodes choline oxidase, the enzyme that converts choline to glycinebetaine. The presence of choline oxidase and glycinebetaine in seeds of transformed lines was confirmed by Western blotting and nuclear magnetic resonance (NMR) spectrometry, respectively. The transformation with the codA gene significantly enhanced the tolerance of seeds to low temperatures, such as 0°C, during imbibition. The transformation accelerated the germination and growth of seedlings at 10 and 15°C. It appears that the presence of glycinebetaine in transformed plants enhances their ability to tolerate low-temperature stress during the imbibition and germination of seeds and the growth of seedlings.Key-words: Arabidopsis thaliana; chilling injury; choline oxidase; germination; glycinebetaine; imbibition; tolerance to low temperature. INTRODUCTIONPlants are often exposed to environmental stresses that lead to interruptions or perturbations of normal homeostatic processes and can affect plant growth and development at various stages in the life of the plant (Boyer 1982;Tarczynski, Jensen & Bohnert 1993). Low temperature is one of the adverse environmental conditions that limit the geographical distribution of plants and it is responsible for significant reductions in the yield and quality of agriculturally important crops (Levitt 1980 and references therein). Because tolerance to low temperature is controlled by many genes and is inherited as a quantitative trait, progress in the development of cold-tolerant crops by traditional breeding methods has been slow (Guy 1990). Therefore considerable attention has been paid, in recent years, to the possible genetic engineering of tolerance to low temperature in plants (Murata et al. 1992;Wolter, Schmidt & Heinz 1992;Hayashi et al. 1997). However, such studies have focused on the tolerance to low temperature of vegetative tissues of transgenic plants. The effects of transgenes on the imbibition and germination of seeds and on the growth of seedlings at low temperatures have not previously been examined.Plants have evolved a vast diversity of acclimation and avoidance strategies to cope with adverse environmental conditions (Levitt 1980). One common cellular mechanism of acclimation in plants is the accumulation of osmotically active, low-molecular-weight, non-toxic compounds (Wyn Jones & Storey 1981;Yancey et al. 1982;Le Rudulier et al. 1984;Tarczynski et al. 1993;Bohnert & Jensen 1996), known collectively as osmoprotectants. Glycinebetaine (hereafter referred to as betaine) is an important osmoprotectant that is accumulated in bacteria, algae and higher plants, as well as in animals (Papageorgiou & Murata 1995). In addition to its role in osmoregulation, betaine stabilizes macromolecules by protecting them against damage induced by various types of stress (Papageorgiou & Murata 1995).The role of betaine in tolerance to low temperature has been demonstrated in bacteria as well as in higher plants (Coug...

show abstract

Effects of three stabilizing agents—Proline, betaine, and trehalose—on membrane phospholipids

Cited by 250 publications

References 21 publications

Conversion of the chill susceptible fruit fly larva ( Drosophila melanogaster ) to a freeze tolerant organism

Conversion of the chill susceptible fruit fly larva ( Drosophila melanogaster ) to a freeze tolerant organism

Effect of trehalose on protein structure

Transformation with a gene for choline oxidase enhances the cold tolerance of Arabidopsis during germination and early growth

Contact Info

Product

Resources

About