How applicable is the general adaptation syndrome to the unicellular Tetrahymena?

Abstract

Hormone receptors, hormones and signal transduction pathways characteristic of higher vertebrates can be observed also in the unicellular Tetrahymena. Previous work showed that stress conditions (starvation, high temperature, high salt concentration, formaldehyde or alcohol treatment) elevated the intracellular level of four hormones (ACTH, endorphin, serotonin and T 3 ). Here, the effect of other stressors (CuSO4 poisoning, tryptophan hydroxylase inhibitor parachlorphenylalanine (PCPA) treatment) on the same and other hormones (epinephrine, insulin, histamine) was studied, using immunocytochemistry and flow cytometric analysis. It was found, that each effect increased the intracellular hormone contents, but some hormones (histamine, T 3 ) were less reactive. Insulin-which is a life-saving factor for Tetrahymena-itself provoked elevation of hormone amounts in association with a stressor, further increased the level of hormones. It was concluded that the ancestor of Selye's General Adaptation Syndrome (GAS) can be found already at unicellular level, and this possibly has a life saving function. Copyright # 2008 John Wiley & Sons, Ltd.key words -hormones; stress; general adaptation syndrome; GAS; Tetrahymena pyriformis INTRODUCTIONIt was demonstrated more than 30 years ago that the unicellular ciliate, Tetrahymena has binding sites (receptors) for hormones characteristic of higher ranked multicellular animals [1][2][3][4][5][6] and it also contains these hormones. 7-10 Some of these receptors are similar to those of the mammalian ones 10-14 and the hormones are not only cytochemically but also functionally similar to the hormones of mammals. 15The signal transduction pathways also can be found. [16][17][18] The hormones can transmit information within the Tetrahymena population even if they are present in an extremely small concentration. 19In earlier experiments it was demonstrated that stress conditions stimulate hormone production by Tetrahymena. Thermal or osmotic stress as well as starvation increased the cells' hormone (ACTH, endorphin, triiodothyronone (T 3 ) and serotonin) concentration, [20][21][22] suggesting that the General Adaptation Syndrome (GAS) of Selye 23 can be applied at a unicellular level. However, it was not clear how broad is the spectrum of hormones which are activated by stress, especially for epinephrine, which is a key-hormone in mammalian GAS, and whether insulin, which is a life-saving factor for Tetrahymena is also involved or not? In the present experiments we decided to study this problem. In addition the effect of other stressors and the effect of a stressor þ insulin combination are studied here, for testing the generality of GAS theory in unicellular organisms. MATERIALS AND METHODS Cells and culturingTetrahymena pyriformis GL strain was used in the logarithmic phase of growth. The cells were cultured at 288C in tryptone medium (Sigma, St. Louis, USA) containing 0.1% yeast extract, for 24 h. The density of Tetrahymena cultures studied was 10 4 cell mL À1 . TreatmentsStudy of osm...

Effect of stress and stress hormones on the hormone (insulin) binding of Tetrahymena

“…However, it is also possible that the unicellular organisms had also an evolution with similar steps of signal reception and Tetrahymena, which is a top-level organism considering the unicellular realm, shows the similarities to the higher ranked animals. The elevation of hormone content as a consequence of any stress 20,21 is also similar to the event which is characteristic to mammals. The elevation of hormone binding during and after stress means that not only the amount of signal molecules are growing but also the possibility of signalreception, perhaps by the co-ordination of hormone and receptor genes.…”

“…23 As the reaction was universal and in each case ACTH level was found also elavated, [19][20][21] it was supposed that a GAS-like phenomenon is present at unicellular level. In the present experiments the hormone binding (receptor) capacity of Tetrahymena was studied, influenced by different stressors.…”

“…20,21 If we suppose that hormones have a life-saving function 17 during stress conditions, the parallel elevation of hormone production and hormone binding seems to be plausible. However, insulin given during stress did not influence the hormone (insulin) binding, rather serotonin and histamine had such an effect.…”

“…This system could be used for giving information for the members of the Tetrahymena population as well as for receiving information, for example, in the presence of useful molecules (e.g., nourishment) or in the case of danger. In earlier experiments [19][20][21] the effect of stressors (starvation, high concentration of salts, higher temperature, formaldehyde, CuSO 4 poisoning) to the hormone (ACTH, endorphin, serotonin, histamine, triiodothyronine (T 3 ), epinephrine, insulin) content of these cells was studied and a significant elevation of them was found. It was concluded that the ancestor of Selye's General Adaptation Syndrome (GAS) 22 is present already at unicellular level and this possibly has a life-saving function.…”

Biogenic amines at a low level of evolution: Production, functions and regulation in the unicellular Tetrahymena

“…almost doubled the serotonin concentration inside the cells [82]. This is right also to epinephrine and histamine, however, the latter was the less reactive [83]. Heat stress for 1 h increased the serotonin and histamine level for two weeks [84].…”