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Biochemistry of Hyperthyroidism and Hypothyroidism* FREDERIC L

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Biochemistry of Hyperthyroidism and Hypothyroidism* FREDERIC L Postgrad. med. J. (May 1968) 44, 347-362. Postgrad Med J: first published as 10.1136/pgmj.44.511.347 on 1 May 1968. Downloaded from Biochemistry of hyperthyroidism and hypothyroidism* FREDERIC L. HOCH B.S., M.S., M.D. Biophysics Research Division, Institute ofScience and Technology, The University of Michigan, Ann Arbor, Michigan 48104 Summary effect. The preponderance of evidence at present The thyroid hormones act directly on mito- supports the first hypothesis. It seems feasible chondria, and thereby control the transformation therefore to attempt to reduce the complex of the energy derived from oxidations into a form pathologic pictures to subcellular phenomena utilizable by the cell. Through their direct actions and their consequences. on mitochondria, the hormones also control in- Recent advances in the understanding of where directly the rate of protein synthesis and thereby and how the thyroid hormones act in the cell the amount of oxidative apparatus in the cell. A support a simplification of thyrotoxicosis and rationale for the effects of thyroid hormone excess hypothyroidism, although our understanding is or deficiency is based upon studies of the not as yet so far advanced as to permit a final mechanism of thyroid hormone action. In hypo- 'explanation' of the diseases in molecular terms. thyroidism, slow fuel consumption leads to a low A brief history of the evolution of studies on Protected by copyright. output of utilizable energy. In hyperthyroidism, the mechanism of thyroid hormone action serves rapid fuel consumption leads to a high energy to outline the present state of knowledge, the output, but as efficiency decreases, the utilizable areas in which future advances may be made, energy produced decreases. Many of the chemical and a basis for a rationale of hyperthyroidism and physical features of these diseases can be and hypothyroidism. reduced to changes in available energy. Actions and effects of thyroid hormones Introduction Ever since Magnus-Levy (1895) showed that Excess or deficiency in the amount of thyroid the thyroid gland controlled the rate of oxygen hormones in humans produces clinical and consumption in mammals, attention has been chemical manifestations that involve a number fixed on oxidative processes as a target of the of organ and metabolic systems. Variations of hormone. Kendall (1929) showed the structure of thyroid hormone concentrations in vivo change thyroxine and suggested the hormone might be http://pmj.bmj.com/ oxygen consumption, temperature regulation, a component or coenzyme of an oxidative growth and development, the response to other enzyme, undergoing a redox cycle between the hormones, nerve function, and the metabolism of phenol and semiquinone forms. No evidence proteins, fats, carbohydrates, nucleic acids, vita- has as yet been found to support Kendall's hypo- mins, and inorganic anions and cations. On the thesis conclusively. In the years 1940-50 it be- other hand, thyroxine and triiodothyronine are came clear that 90% or more of the cell's relatively simple molecules, and their small size oxygen was consumed via processes occurring on September 30, 2021 by guest. and limited number of reactive groups suggest in mitochondria, and experiments were done either that the variety of the effects they pro- with thyroid hormones in vivo and in vitro to duce are due to a few types of primary inter- determine their effects on mitochondria. actions at the molecular level, or that the hor- One should differentiate, in considering these mones are changed in the body to analogues studies, between actions of the hormones and each having a different and specific physiologic effects of the hormones. Actions may be defined as those functional or structural changes that *Abbreviations: L-T,, L-thyroxine; L-T,, L-triiodo- are primary and depend upon the presence of thyronine; Triac, triiodothyroacetic acid; ATP, ADP and the hormone at a site where it interacts with a AMP, adenosine tri-, di- and mono-phosphate; P1, inorganic molecule in the cellular apparatus. Because hor- phosphate; NADH and NADPH, reduced nicotinamide- mones are effective in small amounts we adenine dinucleotide and dinucleotide phosphate; DNP, may 2,4-dinitrophenol; BMR, basal metabolic rate (0O con- assume that their primary molecular interactions sumption). are reversible, so that the hormones are not 348 Frederic L. Hoch Postgrad Med J: first published as 10.1136/pgmj.44.511.347 on 1 May 1968. Downloaded from used up. Effects may be defined as those func- 1966), then increases in ribosomal RNA-content tional, structural, or compositional changes that and aggregation (about 40 hr) (Tata, 1967). How- are secondary and do not depend upon the pres- ever, although all these phenomena showed an ence of the hormone; they should not be important relationship between the thyroid hor- reversed if the hormone is removed after acting. mones and the processes supplying information The differentiation between actions and effects to and controlling the rate of protein synthesis, makes no judgement on their relative importance they did not show the primary locus of hormone in the cell. The thyroid hormones are peculiarly action. When L-T3 was added to isolated nuclei, suitable for the resolution of primary actions RNA-metabolism was not stimulated (Widnell & from secondary effects, because their iodine Tata, 1963; Tata & Widnell, 1966; Sokoloff, moieties can be used experimentally as a tracer Francis & Campbell, 1964). Tata's conclusions for quantitative analysis. Methods for detecting are diagrammed in Fig. 1. other hormones not possessing this useful pro- perty are less specific or more tedious. As will be detailed below, the thyroid hor- T- -/- Nucleus -:> Ribosome = Protein > Mitochondrion mones were shown to affect mitochondria as synthesis 2,4-dinitrophenol did: both agents increased mitochondrial respiration, and the energy lib- 3-16 40 48 70-90 erated was transformed into heat rather than Time(hr) /i vivo into the normal utilizable form, the high-energy phosphate bond. This toxic, catabolic, energy- FIG. 1. Sequence of events after injecting hypothyroid wasting effect served as a rationale for thyro- rats with thyroid hormone (T = L-T,), according to toxicosis (Hoch, 1962a), but not for the anabolic Tata and co-workers. energy-conserving effects that the smaller doses Protected by copyright. of thyroid hormones exerted in euthyroid or The studies of Sokoloff (Sokoloff & Kaufman, hypothyroid subjects (Hoch, 1962b). Nor was 1959, 1961; Sokoloff et al., 1963, 1964) have hypothyroidism made more understandable by recently drawn attention back to the mitochon- the 'uncoupling' hypothesis. Accordingly, atten- drion as a site of action of the hormone (Fig. 2). tion was directed away from the mitochrondrion in the search for the mechanism. o2 In the early 1960s the groups of Tata and of ASH.2 t-RNA-AA showed that hormones affected T Mitochondrion =>xn > Sokoloff thyroid ATP Ribosomez= Protein synthesis protein synthesis. It had been demonstrated GTP earlier by Dutoit (1952) that protein was syn- 5min Time 2hr: thesized abnormally slowly in the livers of hypo- in vitro in vivo thyroid rats. L-T3 given in vivo accelerated FIG. 2. Sequence of events after injecting hypothyroid http://pmj.bmj.com/ the synthesis of proteins by ribosomes after rats with thyroid hormone, or after addition of thyroid about 48 hr after injection; the doses necessary hormone to mitochondria (T - L-T,), according to were small and physiologic, smaller than those Sokoloff and co-workers. producing uncoupling in mitochondria, and the effect of the hormone was obviously anabolic Adding L-T3 to a homogenate in vitro stimu- (see Tata, 1967). Puromycin and actinomycin D, lated ribosomal synthesis of proteins. The pro- agents that block protein synthesis by acting on cesses whereby t-RNA-amino-acyl complexes nucleic acids, blocked the calorigenic action of interacted with the ribosomes were the locus of on September 30, 2021 by guest. thyroid hormones (Tata, 1963; Weiss & Sokoloff, the stimulation. Mitochondria oxidizing a sub- 1963). No changes were observed in mitochon- strate were necessary, and they apparently pro- drial respiratory control after hormone injec- duced a substance that accelerated the ribosomal tion (Tata et al., 1963). Respiratory acceleration translation; adding ATP, GTP or glutathione did could be demonstrated in mitochondria 70-90 not replace the effect of hormone-treated mito- hr after hormone injections, but it was due to chondria. What it is that mitochondria produce increases in the number of depleted respira- to control ribosomal protein synthesis is not yet tory assemblies in the mitochondria of hypo- clear; studies by Bronk (1963) have suggested thyroid rats (Tata et al., 1963; Roodyn, Freeman that mitochondrial non-phosphorylated, high- & Tata, 1965), and so represented the specific energy intermediates may support protein syn- results of earlier protein synthesis. Increases in thesis. nuclear RNA-metabolism were shown early (3- Our recent studies have shown that L-T4 in- 16 hr) after hormone injection (Tata & Widnell, jected in vivo can act rapidly and directly on Biochemistry of hyperthyroidism and hypothyroidism 349 Postgrad Med J: first published as 10.1136/pgmj.44.511.347 on 1 May 1968. Downloaded from mitochondria (Hoch, 1968a). Bronk (1966) has not yet clear, the rate of translation of t-RNA- also shown a very short latent period for L-T8. amino-acyl complexes by ribosomes to synthesize In hypothyroid rats, a subcalorigenic dose of proteins. Among the proteins synthesized are L-T4 (at least fifty times less than those used the enzymatic components of the mitochondrial to stimulate protein synthesis) partly corrected respiratory chain. The nucleus is also involved the excessive respiratory control in liver mito- early, but the relation between the rises in nuclear chondria 3 hr after injection (Hoch, 1966). A RNA-metabolism and the earlier changes in larger dose did the same when the rats were mitochondrial function, as well as the later killed 2 min after injection (Hoch, 1967, 1968b).
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