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The Lens in Diabetes

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The Lens in Diabetes THE LENS IN DIABETES A. J. BRONl, J. SPARROW2, N. A. P. BROWNl, J. J. HARDINGl and R. BLAKYTNyl Oxford and Bristol SUMMARY are laid down in a series of onion-skin layers, which arch This paper reviews the changes which occur in the human over the equator to meet their opposite numbers at the lens lens in diabetes. They include refractive changes and cat­ sutures. The innermost fibres comprising the nucleus of aract and age-related increases in thickness, curvatures, the lens are free of organelles and show limited metabolic light scattering, autofluorescenceand yellowing. The inci­ activity. The outer fibres comprise the cortex. The most dence of cataract is greatly increased over the age of 50 superficial fibres of the cortex are nucleated and, like the years, slightly more so in women, compared with non­ epithelium, show the normal complement of organelles. diabetics. Experimental models of sugar cataract provide Glucose, which enters the lens by facilitated transport, I is some evidence for the mechanism of the uncommon, but its main energy supply, although energy may also derive morphologically distinct, juvenile form of human dia­ from amino acids? The metabolism of the cortex is chiefly betic cataract, where an osmotic mechanism due to sugar anaerobic, with 70% of the energy supply of the lens alcohol accumulation has been thoroughly studied in dia­ deriving from anaerobic glycolysis. If a lens is incubated betic or galactose-fed rats. The discrepancy between the in nutrient medium in anaerobic conditions with an ready accumulation of sugar alcohol in the lens in model adequate supply of glucose it remains transparent for a systems and the very slow kinetics of aldose reductase number of hours.3.4 The metabolism of the epithelium is (AR) has not been satisfactorily explained and suggests aerobic. New lens fibresarise by cell division in the germi­ that the mechanism of polyol formation is not yet fully native zone in the pre-equatorial region of the lens. understood in mammalian systems. The activity of AR in The epithelium and superficial cortical cells are major the human lens lies mainly in the epithelium and there sites of ion pumps such as Na+,K+-ATPase and Ca2+­ appears to be a marginal expectation that sufficientsorbi­ ATPase, concerned with maintaining the water and ionic tol accumulates in cortical lens fibres to explain the lens environment of the lens,5.6 and there are also ion channels swelling and cataract on an osmotic basis. This is even more so in the cataracts of adult diabetics, which re­ in these cells which cooperate in this regulatory function semble those of age-related non-diabetic cataracts in and additionally conserve cell pH.? Ionic equilibrium is appearance. The very low levels of sorbitol in adult dia­ facilitated by gap junctions present between the cells.8 In betic lenses make an osmotic mechanism for the the human lens, gap junctions occupy a relatively small increased risk of cataract even less likely. Other mech­ fraction of the membrane, compared with that in other spe­ anisms, including glycation and oxidative stress, are dis­ cies. Until recently gap junctions have been thought to be cussed. The occurrence of cataract is a predictor for represented in the lens by the major intrinsic polypeptide increased mortality in the diabetic. (MIP26), although this protein may in fact perform a vol­ ume regulatory function. The lens is protected from oxida­ The diabetic lens is larger than normal, disposed to refrac­ tive damage by a range of scavenger molecules located in tive change and at increased risk of cataract, sometimes of membranes and in the cytosol. These include vitamin E a specific type. This paper discusses the factors involved. within the membranes, reduced glutathione (GSH), and ascorbic acid, superoxide dismutase, catalase, taurine and ANATOMY AND PHYSIOLOGY beta-carotene. The distributions and concentrations avail­ The lens is enclosed in a collagenous capsule containing able vary between species. other matrix proteins and proteoglycans. A monolayer of Thirty-three per cent of the wet weight of the human epithelial cells is interposed between the anterior capsule lens is protein9.lo and over 90% of this is made up of the and the main cellular mass of lens fibres. The lens fibres lens cry stall ins (alpha, beta and gamma) (Fig. 1). This From: 'Department of Ophthalmology and Nuffield Laboratory, high crystallin concentration is responsible for the high University of Oxford, and 2Department of Ophthalmology, University refractive index of the lens. The crystallins exhibit a short of Bristol, UK. range order similar to that of glass.ll This accounts for the Correspondence to: A. J. Bron, Nuffield Laboratory of Ophthalmology, Walton Street, Oxford OX2 6AW, UK. high degree of transparency of the individual lens fibres. Eye (1993)7,260-275 THE LENS IN DIABETES 261 border of which appears as a light-scattering zone (Cl 4 beta). The subjacent zone is a further clear zone (C2), which increases in thickness as the lens grows in sagittal width. The relationship between C 1 and C2 is interesting: as new fibres are added to the outer surface of Cl, the y deeper fibres of C 1 beta show diminished light-scattering properties, and are incorporated into C2.17,18 Deep to C2 is another light-scattering zone, which broadens in width with age and increases its scattering properties from about the age of 45 years. The deepest zone is again clear and is termed C4. Zones Cl and C2 comprise the superficial cor­ tex, and C3 and C4 the deep, or perinuclear, cortex. LENS GROWTH Elution volume The sagittal width of the lens is about 4 mm at birth. Post­ Gel chromatography of bovine lens proteins. Aggre­ Fig. 1. natal growth measured in the sagittal plane shows two dis­ gated protein (HM) is followed by � � . and crystallins. a, W L y, y tinct phases. The lens retains its neonatal width for the first (Beswick and Harding; from Harding _2 with permission.) 20 years while expanding equatorially.19 After this time Other factors responsible for lens transparencyinclude the there is a steady growth in sagittal width at a rate of about orderly arrangement of the lens fibres, the sparseness of 29 Ilm/year20 with relatively little change in equatorial the cellular organelles, the peripheral location of the fibre diameter. Various growth factors, including insulin-like nuclei away from the optic axis, the small extracellular growth factor (IGF), are found in human aqueous and vit­ space (in the region of 1% of the lens volumel2) and the reous21,22 and there are receptors on the lens for insulin and narrowness of the fibre membranes. The transparency of IGF,23 epidermal growth factor (EGF)24,25 and fibroblast the normal young human lens is 90% for incident light in growth factor and (FGF)?6 An unusual feature of lens the wavelength range 500-1000 nm.13 Transparency growth is that while new fibres are added at the surface, decreases with age. certain regions of the lens show a loss of volume, termed Disruption of fibre organisation and integrity (swelling compaction. and breakdown), expansion of the extracellular space and aggregation of lens proteins, particularly the ubiquitous LENS CHANGES IN DIABETES27 crystallins, may lead to the focal increase in light scatter­ The changes seen in the human lens in diabetes are sum­ ing and degradation of the retinal image which charac­ marised in Table I. terise cataract. More diffuse crystallin aggregation may simply reduce light transmission by the lens in the absence Lens Thickness of a focal lens opacity. Lens thickness is greater in diabetics than in normal sub­ The lens crystallins range in size from the monomeric jects, due mainly to cortical thickening.28,29 Other biomet­ gamma crystallin (20 kDa) to alpha crystallin (800 kDa), ric changes include steepening of the front and back which is an aggregate of subunits; beta crystallins are of curvatures of the lens and shallowing of the anterior cham­ intermediate mass. The alpha crystallin aggregates consist ber.30,31 After adjusting for age, these changes are most of two major polypeptides of 20 kDa, and of their phos­ pronounced in insulin-dependent (type 1) diabetics, and phorylated derivatives. The polypeptides of the beta crys­ diabetic duration exerts a powerful independent influence tallins range in size from 21 to 35 kDa. The beta and (Fig. 2). The annual expansion of the sagittal width of the gamma crystallins are highly homologous, and form one lens is accelerated by about 70%.30 The anterior clear zone large superfamily of proteins. They are rich in thiols. The (Cl alpha) is expanded in both type 1 and non-insulin­ complete structures of one gamma and one beta crystallin dependent (type 2) diabetics compared with controls. are now known.14,15 Unlike gamma crystallins, the alpha Among diabetics of both types neither age nor diabetic and beta crystallins have blocked amino-terminal residues duration appear to play a role in this expansion. The pres- and this is thought to have a protective function. Gamma crystallins, such as gamma II, can undergo post-trans­ Table I. Lens changes in diabetes lational modification by sugars such as glucose-6- 6 Lens thickness phosphate.1 Refractive change Sustained THE LENS ZONES Transient In slit-lamp section the adult lens can be seen to be divided Light scattering Chromophore accumulation into zones of differing light-scattering properties. The Fluorescence first, a subcapsular, cortical zone (designated Cl) is a zone Cataract which is of relatively constant width throughout life, the Capsular changes Risk for death greater part of which is clear (Cl alpha) and the posterior 262 A. J. BRON ET AL. 7 � E E � U) U) 6 w z � u i!: 5 U) z W ...J ...J 4 � � 3 +-----�--�-----+----�----�----�--�-----+----� o 10 20 30 40 50 60 70 80 90 AGE (years) Fig.
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