A comparative survey of steroids and steroidogenic pathways throughout the vertebrates

Abstract

Corticosteroid hormone biosynthesis has been demonstrated in most classes of vertebrates, both Agnatha and Gnathostomata. Though comparative steroid endocrinology is still a young discipline, it is possible to group, tentatively, the different classes of animals according to the chemical nature of the corticosteroid hormones elaborated. In many instances these results were obtained in vitro and only on a limited number of representatives of a class. Thus our classification is only preliminary. Group I. Animals that secrete both 17-hydroxylated (e.g., cortisol, cortisone, 11-deoxycortisol) and 17-deoxycorticosteroids (e.g., corticosterone, 11-deoxycorticosterone, 18-hydroxycorticosterone, aldosterone). Most mammals investigated belong to this group, including subeutherian and eutherian orders. Notable exceptions from this endocrine pattern are found in the order of Rodentia, and some amphibians, both urodeles ( Amphiuma) and anurans ( Bufo), can be included in this group. Group II. Animals that secrete only 17-deoxycorticosteroids. The group comprises Aves, Reptilia, amphibians (Ranidae), and the rat and mouse (Order Rodentia). Group III. Animals that secrete only 17α-hydroxycorticosteroids. The few orders of Osteichthyes investigated can be classified in this group, but with some reservations, as both corticosterone and aldosterone were reported in bony fishes. Group IV. This chemically heterogeneous group comprises mostly chondrichthians. In this class adrenocortical secretion seems to vary from order to order. Thus, in the genus Raja the main, and possibly only, secretory product is 1-α-hydroxycorticosterone; the elaboration of cortisol was reported in the ratfish ( Hydrolagus), and of corticosterone in dogfishes ( Squalus and Mustelus). This tentative classification demonstrates that for adrenocortical secretion the same chemical building-blocks are used throughout the vertebrates. No quantitative classification has been attempted. Studies on the biosynthesis of steroid hormones in mammalian adrenals are numerous, but few reports exist on biosynthetic routes operating in the adrenals of nonmammalian vertebrates. The pathway acetate-cholesterol corticosteroids was shown to exist in birds, and the route cholesterol-corticosteroids in one species of bony fish ( Anguilla). Pregnenolone and progesterone are precursors of both 17-hydroxy and 17-deoxycorticosteroids in all four groups. Aldosterone is biosynthesized from corticosterone in all aldosterone-producing species; it is accompanied in most instances by the production of 18-hydroxycorticosterone. On the intracellular level, adrenal mitochondria were shown to be the main source of steroid 18-oxygenating enzymes in Mammalia, Aves, and Amphibia. These synthetic routes are found in mammalian adrenals as well. Thus there seems to be a basic uniformity in steroid biochemistry in all hormone-producing adrenal cells. The adrenal itself shows progressive evolution from the scattered secretory cells in fishes to the encapsulated and zonated organ in mammals, but no evolutionary trend is yet apparent in the chemical nature of adrenocortical secretion. Nor can obvious connections be seen between the type of hormone synthesized and the habitat of the animal. The full potential of steroid hormone biosynthesis may have been acquired with the development of an inner supporting structure, and from this pool of possible reactions each class, order, or genus may have adopted biosynthetic routes to solve its adaptive and metabolic problems.