Molecular control of membrane properties during temperature acclimation. Fatty acid desaturase regulation of membrane fluidity in acclimating Tetrahymena cells

Martin, Charles E.; Hiramitsu, Kayoko; Kitajima, Yasuo; Nozawa, Yoshinori; Skriver, Lars; Thompson, Guy A.

doi:10.1021/bi00669a004

Cited by 161 publications

(80 citation statements)

References 36 publications

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“…The Q10 of the rhythm below 220C was 2.2, and periods of about 40 hr were observed. In contrast, the Q10 of the rhythm above 220C was 1.1, with circadian periods of [18][19][20][21] hr. Thus, cel displayed a threshold temperature or "break point" for the temperature compensation of its rhythm.…”

mentioning

confidence: 78%

“…The possible involvement of membranes as a component ofcircadian rhythmicity was proposed by others (19) in part because of temperature compensation. Membrane "fluidity" is known to be temperature-compensated in a number of systems by means of alteration in fatty acid composition ("homeostasis of membrane fluidity") (20,21). If circadian kinetics were dependent on membrane fluidity, no additional temperature-compensation mechanism would need to be elucidated.…”

Section: Discussionmentioning

confidence: 99%

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Circadian rhythms in Neurospora crassa: a mutation affecting temperature compensation.

Mattern¹,

Forman²,

Brody³

1982

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

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The circadian rhythm of conidiation (spore formation) in Neurospora crassa is known to be temperature compensated, that is, the period is only slightly affected by the incubation temperature. Thus, the Q10 (the relative rate enhancement corresponding to a 10C rise in temperature) of the rhythm of the bd cap strain from 14 to 300C was 1.1, whereas the Q10 of the uncompensated growth rate in the same interval was 2.4. A mutation at the cel locus resulted in loss of the temperature-compensation property in cultures grown below 22TC. The Q10 of the rhythm below 220C was 2.2, and periods of about 40 hr were observed. In contrast, the Q10 of the rhythm above 220C was 1.1, with circadian periods of 18-21 hr. Thus, cel displayed a threshold temperature or "break point" for the temperature compensation of its rhythm. Supplementation of cel strains, which require fatty acids, with unsaturated or short-chain fatty acids raised the threshold temperature to 260C, whereas supplementation with long-chain saturated fatty acids lowered it to 18C. These data suggest a role for fatty acids, as lipid components or as cellular metabolites, in the mechanism of temperature compensation.Circadian rhythms are the most widely studied of the endogenous biological oscillations. Three characteristics are ordinarily used to identify a rhythm as circadian: its period (about 24 hr when free-running); its sensitivity to light (reflecting the ability to adjust its phase to the phase of the environment); and the relative insensitivity of its period to the growth temperature (1). This last characteristic is called temperature compensation (2). Without such a safeguard, daily biological timekeeping would be highly unreliable, running ahead oflocal time in warm situations (summer, noon, thermal springs) and behind in cool ones (winter, midnight, mountain streams). Examples of uncompensated daily rhythms are rare, and are usually confined to tropical species, which live where ambient temperatures are fairly constant (3).Temperature compensation is often quantified in terms ofthe temperature coefficient Q1o, the relative rate enhancement of a process corresponding to a 100C rise in temperature. Ordinary biological growth rates and reactions have Q10s of 2-3 (2). The

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mentioning

confidence: 78%

Section: Discussionmentioning

confidence: 99%

Circadian rhythms in Neurospora crassa: a mutation affecting temperature compensation.

Mattern¹,

Forman²,

Brody³

1982

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

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“…We therefore began our study with an in vivo examination of membrane physical properties as inferred from freeze-fracture electron microscopy. The technique employed involved chilling several aliquots of cells, each to a different test temperature, before fixation with glutaraldehyde (7,9). The resuiting patterns of intramembrane protein particle distribution on the freeze-fracture replicas could be used to determine the temperature at which each membrane underwent initial phase separation of its constituent lipids (7).…”

Section: Tetrahymena Pyriforrnismentioning

confidence: 99%

“…One possibility is through changes in the membrane lipid composition. Much evidence has been accumulated to establish that Tetrahymena can alter its membrane fluidity very rapidly by producing specific lipid species on the endoplasmic reticulum and transferring them to other membranes (6,7,9). We modified one of these earlier experiments to test the ability of food vacuoles to respond to a fluidity-modifying stimulus.…”

Section: Figurementioning

confidence: 99%

Differentiation of food vacuolar membranes during endocytosis in Tetrahymena.

Kitajima¹,

Thompson²

1977

The Journal of Cell Biology

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The origin and differentiation of Tetrahymena pyriformis food vacuolar membranes has been studied by freeze-fracture electron microscopy. By measuring the temperature needed to induce the onset of lipid phase separation (as inferred by the appearance of particle-free regions in replicas) and calculating the changes in average intramembrane particle distribution, a distinct modification of the vacuolar membrane could be observed from the time of its formation from diskshaped vesicles to its maturation before egestion of its indigestible contents. Whereas the nascent vacuolar membrane first showed signs of phase separation at 9~ this temperature rose to 14~ in the completed vacuole and then, after lysosomal fusion, eventually declined to 12~ The average membrane particle density on the PF face increased from 761 -+ 219 to 1,625 _+ 350 per /~m 2 during membrane differentiation. Like other membranes of the cell, the vacuolar membrane underwent adaptive changes in its physical properties in cells maintained for several hours at low temperature. This exposure to low temperature caused an equal effect in vacuoles formed before, during, or after the temperature shift-down. Normal changes in the properties of the vacuolar membrane may have some bearing on its programmed sequence of fusion reactions.

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“…2). It has also been shown that the membranes of Tetrahymena regulate their fluidity in response to changes in the ambient temperature (20,21,27). Thus, on increasing or decreasing the culture temperature, compensatory changes in the lipid composition of the membrane take place, and as a consequence the conformation of the membrane-associated proteins would be expected to change.…”

Section: Discussionmentioning

confidence: 99%

The intrinsic fluorescence of Tetrahymena as a function of temperature

Hill

Zeuthen

1980

Carlsberg Res. Commun.

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Washed suspensions of Tetrahymena pyriformis GL have an intrinsic fluorescence with an excitation maximum at 291 nm and an emission peaking at 358 nm. These wavelengths are characteristic for protein fluorescence. When suitable optical filters are used to eliminate scattered light, a sharp increase in the fluorescence is seen on heating the suspensions. The increase in fluorescence starts at 32 ~ and peaks at 36 ~ with a mid-point at 34 ~ The fluorescence-temperature profile does not change during the cell cycle.On starving the ceils in inorganic medium, the fluorescence decreases markedly within a few hours, but reappears when the cells are transferred to a nutrient medium. Slight shifts in the temperature at which maximal fluorescence is seen were noted as cultures grew denser, and large shifts were observed when the culture temperature was altered. These shifts suggest that the conformation of the proteins responsible for the fluorescence emission is in some way determined by the state of the cell membrane. The local anaesthetic dibucaine was able to titrate out the fluorescence, although cytochalasin B and colchicine had no effect, again suggesting that the fluorescence is controlled by the membrane state.Reversal experiments demonstrated that although the fluorescence was not affected by heating up to 32 ~ it was greatly diminished when the cells were heated above 35 ~ Damaging the cells by other means, e.g. by brief sonication at low power or by shaking the cell suspensions, also resulted in a decrease in the fluorescence.Two other species of Tetrahymena, T. vorax V2S and T. thermophila (Mpr-V) showed similar increases in fluorescence at temperatures a few degrees above their growth temperature. In the latter case, the mid-point of the fluorescence-temperature profile corresponds to the synchrony temperature, as is also the case with T. pyriformis GL.* Deceased on January 10th, 1980.Abbreviation: IM = inorganic medium.

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Molecular control of membrane properties during temperature acclimation. Fatty acid desaturase regulation of membrane fluidity in acclimating Tetrahymena cells

Cited by 161 publications

References 36 publications

Circadian rhythms in Neurospora crassa: a mutation affecting temperature compensation.

Circadian rhythms in Neurospora crassa: a mutation affecting temperature compensation.

Differentiation of food vacuolar membranes during endocytosis in Tetrahymena.

The intrinsic fluorescence of Tetrahymena as a function of temperature

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