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Monosaccharide Transport A Arch Dis Child: first published as 10.1136/adc.42.224.341 on 1 August 1967. Downloaded from Review Article Arch. Dis. Childh., 1967, 42, 341. Sugar Malabsorption Due to Deficiencies of Disaccharidase Activities and of Monosaccharide Transport A. HOLZEL From the Department of Child Health, University of Manchester In many societies including our own, carbo- maltase, were secreted by unspecified cells of the hydrates play a major part in the total calorie supply. intestinal mucosa into the lumen of the gut where According to the National Food survey figures the hydrolytic process took place. But studies in (Greaves and Hollingsworth, 1964), the average man during the past decade (Borgstrom, Dahlqvist, daily diet of adults contains nearly 350 g. of this Lundh, and Sjovall, 1957; Dahlqvist and Borgstrom, constituent. Diets of course vary with eating 1961) demonstrated that disaccharidase activity in habits and social class, but the dietary carbohydrates the intestinal lumen was extremely limited and did are largely ingested as poly-, oligo-, and disaccha- not account for the amount of carbohydrate rides. In the very young, however, the carbo- absorbed. They further indicated that the majority hydrate intake may consist almost entirely of of disaccharides were absorbed unhydrolysed and disaccharides, though this phase is now getting split intracellularly, a fact that accorded well with progressively shorter. As the rapid decrease in experimental findings (Cajori, 1933; Fridhandler breast-feeding has been followed by the early and Quastel, 1955). copyright. introduction of cereals into the cow's milk formulae, The problem of localization of the sugar-splitting even the infant of only a few weeks of age has also enzymes was brought nearer its solution by Miller to digest polysaccharides. and Crane (1961), who were able to separate the The percentage of calories derived from carbo- brush-border from the rest of the intestinal mucosa hydrate increases from 40% in infancy to well over of the hamster, and found that the whole of the 50% later in life. The polysaccharides, starch and enzyme activity of the mucosa was accounted for by glycogen, are hydrolysed by salivary and pancreatic this layer. (-galactosidase (lactase) activity had amylase to maltose and small quantities of isomal- been localized in the microsomes ofthe rat intestinal http://adc.bmj.com/ tose and glucose. The common disaccharides in mucosa by Doell and Kretchmer (1962), while our food are lactose and sucrose. The amount of Dahlqvist and Brun (1962), employing histochemi- lactose depends on the milk intake, as this is its main cal methods for the recognition of invertase and source. The human intestinal mucosa has there- trehalase in various animal tissues, associated their fore the task of absorbing large quantities of the activity with cytoplasmic granules. As yet there is disaccharides, maltose, isomaltose, sucrose, and no definite information concerning the possible lactose. For a long time surprisingly little attention relationship of the elements of fine structure of the was paid to this important absorptive function of the microvillus with its absorptive and digestive on September 26, 2021 by guest. Protected small intestine, but during recent years physiologists, functions. However, two related fractions have biochemists, and paediatricians have discovered been obtained by density gradient centrifugation of much of interest, and clinical observations have tris-disrupted brush-borders from hamster intesti- revealed a number of disorders associated with nal mucosa, and have been identified as the micro- sugar malabsorption. villus cores and their surrounding membranous coats (Overton, Eichholz, and Crane, 1965; Physiology of Disaccharide Absorption Eichholz and Crane, 1965). Until a few years ago it had been accepted that hydrolysis of the disaccharides into their component Specificity of human intestinal disacchari- monosaccharides had to precede their absorption dases. The belief that each enzyme has its and entry into the further stages of metabolism, and corresponding specific substrate has been modified that the disaccharidases, lactase, sucrase, and in so far as experimental and practical experience 341 Arch Dis Child: first published as 10.1136/adc.42.224.341 on 1 August 1967. Downloaded from 342 A. Holzel has shown that synthetic sugars which have the to slightly different conclusions, and thus to some- same glycosidic linkage as naturally occurring what differing nomenclature. Dahlqvist recognizes products will be split by the same enzyme. four maltases, while Auricchio and colleagues The following human intestinal disaccharidases separate five (Table I). have been identified by heat inactivation experi- ments (Dahlqvist, 1962; Dahlqvist, Auricchio, TABLE I Semenza, and Prader, 1963), gel-filtration on Classification of Maltases Sephadex and chromatography (Auricchio, Semenza, and Rubino, 1965c; Semenza, Auricchio, and Dahlqvist (1964a) Auricchio et al. (1965c) Enzyme Substrate Enzyme Rubino, 1965a). The maltases or ao-glycosidases Maltase Ia Isomaltose Maltase 5 hydrolyse maltose, isomaltose, sucrose, and palati- (isomaltase palatinase) Palatinose (isomaltase palatinase) Maltose nose. Trehalase exerts its activity on trehalose, a Maltase Ib Sucrose Maltase 3 (sucrase) (sucrase: invertase) Maltose Maltase 4 rare disaccharide that occurs in certain mushrooms. Maltase II Maltose Maltase 2 The 3-glycosidase lactase (P-galactosidase) attacks Maltase III Maltose Maltase I cellobiose, in addition to lactose. Cellobiose is a disaccharide resulting from the digestion of cellulose, which consists of two molecules of Maltase 5 (in the latter classification) hydrolyses glucose with a 1-4 3 linkage similar to that which maltose, isomaltose, and palatinose, a synthetic sugar joins the glucose and galactose molecules in consisting of one molecule glucose and one molecule lactose (Fig. 1). Although cellobiose plays little fructose in 1-6o0 linkage. Since palatinose and isomaltose have the same glycosidic bond, they are , galoctosi dase split by the same disaccharidase (Fig. 2). Palatinose can therefore be used to demonstrate isomaltase * *I * a~~ activity (Auricchio, Prader, Murset, and Witt, 1961) when isomaltose is in short supply (Fig. 2). * 0 *4 * * * 0 0 0 MALTASES copyright. Lactose Cellobiose Invertase Isomaltose FIG. 1.-f-galactosidase hydrolyses two disaccharides of different molecular composition but with the same * *ff<2 S glycosidic linkage. 0 0 * * 4 * 0 0 * 0 0 0 0 part in human nutrition, since cellulose cannot be * 0 0 6 0 6 0 0 hydrolysed in the small intestine, the sugar can be *Sucrose0 somaltose *0Polotinose: Maltose used as an additional substrate to verify lactase FIG. 2.-Isomaltase hydrolyses in addition to isomaltose http://adc.bmj.com/ activity. The presence of two intestinal lactases palatinose, a synthetic disaccharide. was demonstrated by Heilskov (1956) for the calf, and for the rat and rabbit by Doell and Kretchmer Distribution of disaccharidases along the (1962), who found one lactase associated with the small intestine. Comparison of a number of particulate fraction which hydrolyses two substrates, published animal and human investigations reveals namely lactose and ortho-nitrophenyl-3-galactoside, the presence of species differences. In the rat, while the enzyme the latter. lactose is in the middle of the soluble splits only activity stronger part on September 26, 2021 by guest. Protected Since ortho-nitrophenyl-3-galactoside is an artificial small intestine than in its proximal or distal regions, compound, the true function of the second enzyme maltase activity is uniformly distributed, while is unknown. Two lactases have also been postula- sucrase (invertase) and isomaltase are strongest in ted for the human intestinal mucosa (Semenza et al., the proximal areas. In the adult pig, the trehalase, 1965a). These authors have been able to show that lactase, and cellobiase activities are strongest in the the two 3-galactosidases in the mucosa of the proximal part, while the maltases are most active in human jejunum and ileum are not the result of an the distal part (Dahlqvist, 1964a). In adult man, artefact, and that the ratio of cellobiase activity according to Auricchio, Rubino, and Miirset (1965a), remains constant in relation to that of each of the enzyme assays on mucosal specimens obtained by lactases, further indicating that cellobiase and peroral intestinal biopsy indicate that sucrase, lactase activity are due to the same enzyme molecule. isomaltase, and lactase are less active in the first part With regard to the multiplicity of human maltases, than in the remainder of the duodenum; in the Dahlqvist (1964a) and Auricchio et al. (1965c) come upper jejunum and the last segments of the ileum Arch Dis Child: first published as 10.1136/adc.42.224.341 on 1 August 1967. Downloaded from Sugar Malabsorption 343 disaccharidase activities are of the same order of decreases gradually to its lowest level in the adult magnitude. Taking the rate of absorption as a specimen. In other animals such as mice, rabbits, measure of disaccharidase activity, Gray and and guinea-pigs, the P-galactosidase activity may Ingelfinger (1965) found, with the aid of infusion decrease at different rates in the jejunum and ileum experiments, that sucrose absorption was about (Koldovsky, Heringova, Jirsova, Chytil, and twice as rapid in the human jejunum as in the ileum. Hoskova, 1966) according to the pH. In rats and Ingested sucrose was almost completely absorbed
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