A review of glucose transport in the lens
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- Noreen Taylor
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1 A revew of glucose transport n the lens John W. Patterson T The transport of glucose nto the lens s revewed aganst a background of data on glucose transport n muscle and the red blood cell. In muscle, sorbtol does not penetrate tle cell membrane and s lmted to the extracellular space. On the other hand, 3-0-methjlglucose s dstrbuted n most of the tssue water. Smlar results are obtaned n lens. The glucose that s found n muscle and lens can be accounted for on the bass of the glucose that would be expected to be n the extracelhdar space. Thus, transport s a lmtng step n glucose metabolsm and the rate of utlzaton of glucose may be equated wth the rate of nward transport. Medated transport s consdered as takng place at the fber membrane. The knetcs of glucose transport n the lens are smlar to those n muscle and the red blood cell. All three have Km values of about 7.0 mm. and Qw values of 2.0. Glucose competes wth 3-0-methylglucose for the transport system n the lens. Glucose transport n the lens, as t s n muscle, s enhanced by respratory posons and nhbted by glycolytc posons and phlorzn. It s concluded that the process of glucose transport n the lens s smlar to that n tssues such as muscle and the red blood cell. -he nature of the process by whch sugars -Lh pass across the cell membrane has been studed extensvely n red blood cells ' 2 and muscle. 3 " 6 The lterature on the subject of the entry of sugars nto the lens s much smaller n volume and not as well authentcated. Therefore, n ths paper, materal on the transport of glucose nto the lens wll be presented aganst a background of establshed observatons on the transport of sugars n other tssues. For the most part, comparsons wll be made wth muscle, snce the technques of study for lens and muscle are smlar. In the tssues that are under consderaton, and under ordnary crcumstances, the net passage of glucose s n the drecton of the concentraton gradent. There- From the Unversty of Connectcut, Storrs, Conn. Supported n part by Research Grant AM from the Natonal Insttute of Arthrts and Metabolc Dseases, Unted States Publc Health Servce, Bethesda, Md. 667 fore, as an ntal hypothess the transport process mght be consdered as smple dffuson through the pores of a membrane. Accumulated evdence, however, ndcates that the process s more complex 7 ' S and that the membrane behaves n a selectve manner. Therefore, the terms facltated dffuson and medated transport have been developed to ndcate an nteracton between the membrane and the transported substances. The term actve transport s reserved for phenomena n whch an energy contrbuton s essental. 30 The more general term transport s used wthout prejudce as to the mechansm of permeaton. There are three structural components of the lens whch must be consdered n any dscusson of the transport of glucose from outsde the lens nto the fbers the capsule, the epthelum, and the fber membranes. The capsule of the lens s an acellular structure made up of collagen-lke materal. It s permeable to small molecules
2 668 Patterson Investgatve Ophthalmology August 965 but mpermeable to large protens. 2 Recently, Becker 3 has demonstrated that caton transport s unaffected by the removal of the capsule wth collagenase. There s no evdence that the capsule plays a role n glucose transport. The lens epthelum s nterposed between the aqueous humor and the anteror porton of the lens fbers. It has a specal role n the actve transport of catons and amno acds nto the lens. Followng exposure of the lens to radoactve rubdum, whch behaves lke potassum, the hghest concentratons are found at the epthelal surface. 4 Amno acds and catons 5 are actvely transported and concentrated n the lens from fluds exposed to the anteror epthelal surface of the lens. Passage across the posteror surface s by passve dffuson. 5 Removal of the epthelum by decapsulaton elmnates actve transport of amno acds 5 ' G and catons. 5 ' T Glucose uptake s not affected n the same way. After decapsulaton, even though there s some njury to the remanng fbers, glucose uptake may be as hgh as 83 per cent of that n the ntact lens. ls The methylated glucose dervatve, 3-0-methylglucose, whch s not metabolzed but transported n a manner smlar to that of glucose, 9 enters the lens at the same rate from the posteror surface as t does from the anteror epthelal surface. 20 Although the epthelum plays a role n the actve transport of amno acds and catons, there s no evdence to ndcate that t should be assgned a specal functon n the transport of sugars n the solated lens. Wthn the lens, ndvdual fbers have membranes 2 whch separate the lens nto ntracellular and extracellular compartments n the same manner as the cell membranes of other tssues. Measurements of the dstrbuton of Na, K-ATPase n the lens, 22 of electrcal potentals across the lens surface, 23 and of the dstrbuton of sodum wthn the lens 24 support the concept that the lens fber membranes, as well as the epthelum, serve as stes of caton transport.- 5 Fber membranes retan the polyhydroxy alcohols that are produced by the reducton of sugars, 20 and they prevent the entry of substances such as sucrose nto the fbers. 27 Ths s consstent wth the behavor of other cell membranes, and by analogy and by the process of elmnaton one may suggest that the fber membranes are the ste of glucose transport n the solated lens. The concluson that the fber membrane s the structure that s beng studed when glucose transport s measured n solated lenses has three mportant mplcatons: () the lenses should be small so that the dstance substances must move to reach the ste wll be mnmal; (2) the lenses should be young so that there wll be a homogeneous fber mass; and (3) the extracellular space should be taken nto consderaton when results are nterpreted. The extracellular space whch potentally exsts n the capsule between epthelum and fbers and between ndvdual fbers can be measured by determnng the content wthn the lens of a substance whch does not penetrate through cell membranes. For purposes of comparson, t s common to determne the hypothetcal "space" or volume of tssue flud that would be occuped by a substance f t were present n the same concentraton that occurs n the bathng medum. It s calculated by dvdng the concentraton of the substance n the tssue by ts concentraton n the medum and multplyng by 00. The "space" of the substance, therefore, represents a volume of lens flud per unt of lens weght (mcrolters per 00 mg.), or approxmately the per cent of the wet weght that would be occuped by the substance f t were present n the same concentraton that exsts n the surroundng flud. Snce a substance that freely dffuses nto the extracellular space can have the same concentraton n the extracellular flud that occurs n the surroundng medum, a "space" for a substance that s less than or equal to the extracellular space ndcates an extracellular dstrbuton of the substance. A "space" that s greater than the extracellular space
3 Volume 4 Number 4 Glucose transport n lens 669 MUSCLE LENS INCUBATION TIME (mn.) 20 24C Fg.. The sorbtol space and 3-0-methylglucose space after dfferent tmes of ncubaton. In muscle, sorbtol s lmted to the extracellular space 5 and 3-0-methylglucose s dstrbuted n most of the tssue water. 9 In lens 33 the results are smlar. In order of ncreasng ncubaton tme the ponts for sorbtol represent the mean values for 30, 20, 0, 30, and 0 lenses, respectvely, and for 3-0-methylglucose, the mean values for 2, 6, 2, 3, and 9 lenses, respectvely. ndcates that the substance s also n the ntracellular compartment. The sodum space of rabbt lens determned by sacrfcng the anmals followng the njecton of radoactve sodum was found to be 6. yu. per 00 mg. by Langham and Davson. 27 A smlar study by Huggert 2S showed a sodum space of 9 to 2.6 /\ per 00 mg. n the lens cortex and 3.3 to 7.3 p per 00 mg. n the lens nucleus for rabbts rangng from 3 weeks to 3 years n age. On the bass of ther estmates of the dstrbuton of weght between cortex and nucleus, the average sodum space estmated for the whole lens s 7 to 0 p per 00 mg. Snce the dstrbuton of sodum s accepted as beng extracellular, these values are accepted as reasonable estmates of the extracellular space n rabbt lenses. Determnatons made followng ncubaton of lens n artfcal meda are generally hgher. Bromde and sodum spaces of 29 to 36 p per 00 mg. for the whole lenses, to 30 p\ per 00 mg. for lens cortex, 2<J and 2 to 20 /J per 00 mg. for the lens nucleus have been reported. Followng ncubaton under smlar crcumstances, the lenses of sheep had a sucrose space of 3.5 p per 00 mg. Several types of studes n muscle have contrbuted to an understandng of the mechansm of glucose transport. These nclude:. Dfferences n permeablty of glucose and structurally related molecules. 2. The knetcs of glucose transport. 3. Competton for transport between glucose and related substances. 4. Induced counterflow of sugars aganst a concentraton gradent. 5. The effects of metabolc posons. A consderaton of each of these tems provdes a bass for revewng the transport of glucose n the lens. The permeablty of membranes to dfferent substances may be estmated by measurng the accumulaton of the substance n the tssue followng a perod of ncubaton. The permeablty s ndcated by the extent to whch the "space" occuped by the substance exceeds the extracellular space. Sorbtol does not penetrate cell membranes ' 3 and s used to measure extracellular space n muscle. 32 The sugar dervatve, 3-0-methylglucose s not metabolzed by tssue and dstrbutes tself n the ntracellular and extracellular space. 9 The
4 670 Patterson Inooxtgulve Ophthalmology August 965 Table I. Glucose space and sorbtol space determned smultaneously n rat lenses at 37 C. and 5 C. after 2 hour ncubaton n Tyrode's soluton contanng 00 mg. per 00 ml. of each of glucose and sorbtol 4 No. of lenses 2 2 "Corrected for ntracellular sorbtol. Temperature (C. ) 37 l5 Glucose space (fl/loomg.) Range Mean Sorbtol space 9 (d/00 mg.) Range Mean behavor of these substances n the rat lens s smlar (Fg. I). 33 The sorbtol space was determned wth trtum-labeled sorbtol n the presence of,000 mg. per 00 ml. of glucose. The value of 3.5 /xl per 00 mg. s a lttle hgher than the n vvo results of 6 to 0 /A per 00 mg. that was presented earler for the sodum space of lenses from rabbts. Inasmuch as n vtro determnatons yeld hgher results, the fndng may be accepted as a measure of the extracellular space of rat lens and as a demonstraton that sorbtol does not penetrate through the fber membrane. The 3-0- methylglucose space was determned by usng a radoactvely labeled compound. Ths space ncreases wth tme and equals 40 [xl per 00 mg. of lens n 4 hours. The specfcty of the membranes of muscle and lens as ndcated by the permeablty of these two dervatves of glucose s representatve of the behavor of other substances. In muscle, D-galactose 34 and D- glucose 0 enter the cell and ther L-forms are excluded. Ths selectvty by the cell membrane demonstrates that the transport process s lmted to substances wth specfc molecular confguratons, and that there s a barrer n the lens to the passage of certan dervatves of glucose. The net rate of glucose transport s equal to the rate of utlzaton plus the rate of ntracellular accumulaton. The net rate of transport s equal to the dfference between nward transport and outward transport whch n turn are related, respectvely, to the concentraton of glucose outsde and nsde the membrane. The lower the level of ntracellular glucose, the more closely the net rate of transport equals the rate of nward transport. Thus, f t can be shown that the concentraton of ntracellular glucose s very low, the values for the rate of nward transport, the rate of uptake, and the rate of utlzaton become the same. In lenses from normal rats, the rate of utlzaton has been shown to be equal to the rate of glucose uptake. 35 The glucose space of lenses from normal rats s what would be expected for the extracellular space. Kuck, 3G Knoshta,- G and Lennan, 37 respectvely, found glucose concentratons of 8.4, 9.0, and 9. mg. per 00 Gm. of normal rat lens. Knoshta reported an average blood glucose level of 00 mg. per 00 ml. and Kuck reported a blood glucose level of 02 mg. per 00 ml. and an aqueous glucose level of 04 mg. per 00 ml. n the anmals from whch the lenses were obtaned. The glucose space s thus 8 to 9 /xl per 00 mg. and n the same range as the 6 to 0 [xl per 00 mg. found for the n vvo extracellular space of rabbts. The fact that ntracellular glucose s very low under these crcumstances s confrmed by a smultaneous determnaton of the glucose space and sorbtol space followng ncubaton of rat lenses n Tyrode's medum contanng 00 mg. per 00 ml. each of glucose and sorbtol (Tables I and II). Thus, n lenses from normal rats, there does not appear to be an apprecable amount of ntracellular glucose, and the rate of utlzaton may be accepted as a measure of the rate of nward transport. There s an apparent contradcton to ths concluson whch must be consdered. Harrs, Hauschldt, and Nordqust s have
5 Volume 4 Number 4 Glucose transport n lens 67 Table II. Rato of glucose space to extracellular space at dfferent temperatures Organ Temperature Rato Daphragm" Lens "Calculated from glucose space data of Park, Bornsten, and Post 0 and the extracellular space data of Kpns. 4 shown that glucose accumulates (more than 0 per cent) n rabbt lenses ncubated n meda contanng over 00 mg. per 00 ml. of glucose. Ths has also been demonstrated for rat lenses by Patterson and Buntng. 83 In rat lenses, the crtcal concentraton s just under 200 mg. per 00 ml. of glucose. The glucose space, however, does not exceed the sorbtol space f the ncubaton tme s less than 30 mnutes even though the glucose concentratons range up to,000 mg. per 00 ml. The accumulaton of glucose n the lens n the presence of hgh concentratons of glucose and prolonged ncubaton perods must be the result of an ncrease n the rate of transport of glucose nto the fber or the result of a decrease n the rate of utlzaton of glucose. The sorbtol space s not ncreased wth prolonged ncubaton tmes n the presence of,000 mg. per 00 ml. of glucose (Fg. ) and the rate of accumulaton of 3-0-methylglucose s decreased rather than ncreased n the presence of,000 mg. per 00 ml. of glucose (Fg. 4). Therefore, t appears unlkely that the rate of glucose transport s ncreased. On the other hand, when ntact lenses are ncubated n meda contanng 400 mg. per 00 ml. of glucose, the utlzaton of glucose decreases as the ncubaton tme ncreases. 33 Ths phenomenon s apparently secondary to a decrease n glycolyss, nasmuch as glucose utlzaton n unfortfed lens homogenates, after dfferent tmes of prencubaton of the ntact lenses, also decreases wth ncreasng tmes of prencubaton (Table III). Ths observaton, ndcatng that hgh concentratons of glucose soon have a deleterous effect on glucose utlzaton, helps to explan two earler observatons. Frst, t explans the glucose "toxcty" at concentratons above 200 mg. per 00 ml. of glucose that was observed by Harrs, Hauschldt, and Nordqust 3S n ther studes of the reversble caton shft, and, second, t explans the anomalous results for glucose uptake that were obtaned by Farkas Ivory, and Patterson 39 when 25 mg. rat lenses were ncubated for two hours n medum contanng over 200 mg. per 00 ml. glucose. On the bass of studes on glucose accumulaton, t may be concluded that glucose does not accumulate n rat lenses n the presence of a glucose concentraton of less than 200 mg. per 00 ml. but wll gradually accumulate at hgher concentratons of glucose. Therefore, f the rate of nward glucose transport s to be determned by measurng the rate of glucose utlzaton, t s essental that the ncubaton perods be short. In heart muscle, the rate of nward glu- Table III. Glucose utlzaton by an unfortfed homogenate of a rat lens (9 ± 2 mg.) plus 0 /A of glucose soluton, after prencubaton of the ntact lens n Tyrode's soluton contanng 400 mg. per 00 ml. of glucose 04 No. of experments* Length of prencubaton (hours) Glucose concentraton n homogenate (mg./looml.) Range Mean Glucose utlzaton (mg./gm./hr.) Range Mean "Each experment ncluded 5 lenses for zero tme and 5 lenses that were ncubated for 30 mnutes
6 672 Patterson Investgatve Ophthalmology August 965 MUSCLE LENS MEDIUM GLUCOSE mg/00 ml. 400 Fg. 2. Glucose uptake at dfferent concentratons of glucose for muscle 32 and lens. 33 The curve labeled no membrane for muscle was calculated on the bass of the levels of ntracellular glucose that are found n the presence of nsuln. The ponts on the curve for ntact lenses represent, n order of ncreasng concentraton, the mean value for 0, 9, 8, 32, and 32 lenses, respectvely. The no membrane curve for lens was determned on homogenates of a lens (about 20 mg.) plus 0 "l of sugar soluton. One lens of a par was analyzed at zero tme and the other after 30 mnutes of ncubaton. Each pont represents 20 or more pars of lenses. cose transport at dfferent glucose concentratons s measured by determnng the rate of glucose dsappearance from the medum. 3 '- Apprecable amounts of free glucose do not accumulate wthn the cells except n the presence of anoxa or nsuln. The fact that free ntracellular glucose accumulates under these condtons provdes a bass for calculatng the rate of glucose uptake for dfferent concentratons of ntracellular glucose wthout worryng about the lmtng effects of a membrane. The results for glucose uptake n the presence and absence of a membrane are shown n Fg. 2. The dfference between the two curves ndcates the degree to whch the cell membrane lmts glucose utlzaton under normal aerobc condtons. The rate of nward transport of glucose nto the lens fber s measured n 9 ± 2 mg. rat lenses by determnng the dsappearance of glucose from the total system of lens plus medum durng a 30 mnute ncubaton perod. 33 The glucose uptake for lenses wthout membranes s estmated by homogenzng a seres of lenses n 0 /xl of water contanng dfferent amounts of added glucose. One lens of a par s analyzed at zero tme and the second after 30 mnutes of ncubaton at 37 C. The dfference n the glucose levels n the two lenses along wth the average sugar concentraton durng the ncubaton perod provdes the data for the calculatons. 33 The estmates for glucose uptake n lenses wth and wthout membranes s shown n Fg. 2. The results are smlar to those n muscle. In both nstances, glucose transport through the membrane appears to be the lmtng factor n glucose utlzaton, and n both nstances the transport system becomes saturated at hgher external glucose concentratons. The transport of glucose nto the lens conforms wth Mchaels-Menten knetcs and gves a straght lne n a Lneweaver- Burk plot. 33 The apparent Km for transport s 6.7 ram. and the maxmum rate of transport s 4 mg. per gram of lens per hour. The Km for glucose utlzaton n concentrated unfortfed lens homogenates s 0.7 mm. and the maxmum uptake s
7 Volume 4 Number 4 Glucose transport n lens 673 Table IV. Km of glucose transport n rats Intact cells Heart muscle* Lens Wthout membrane Heart muscle" Lens Km (mm.) (mg./gm./ hr.) "Data from Morgan, Henderson, Regen, and Park mg. per gram per hour. These fndngs are compared wth those for rat heart muscle n Table IV. The values for the Km of glucose transport n red blood cells fall between 4 and 0 mm. 3 Glucose uptake has been measured at dfferent temperatures n rat muscle' 0 and n rat lens. The latter data were suppled by Dr. T. G. Farkas who made avalable the manuscrpt of a paper submtted for publcaton. Wth a decrease n temperature, n muscle and lens, the rate of glucose metabolsm decreases more rapdly than the rate of transport. Therefore, at lower temperatures, ntracellular glucose accumulates (Table I). A plot of the logarthm of the rate of glucose transport MUSCLE aganst the recprocal of the absolute temperature usng the method of least squares permts an estmate of the Q 0 for the transport of glucose n muscle and lens (Fg. 3). The values are 2.0 and.8, respectvely. They are n agreement wth a Q 0 of 2.0 reported for red blood cells." On the bass of knetc studes the Km and Q 0 of glucose for transport n muscle, red blood cells, and lens are the same. The values are consstent wth those of an enzymelke system. The measurement of 3-0-methylglucose space wth dfferent tmes of ncubaton n the presence and absence of glucose provdes a smple method of measurng the competton between 3-0-methylglucose and glucose. The results for rat heart muscle 9 and rat lens 33 are shown n Fg. 4. The results are qualtatvely smlar and demonstrate that these two substances nterfere wth each other's passage through the membrane. Induced counterflow has been demonstrated n muscle 9 (Fg. 5) and n red blood cells. 42 The phenomena may be explaned as follows. If a tssue s loaded wth a sugar dervatve that s not metabolzed, such as 3-0-methylglucose, the con- LENS Fg. 3. The logarthm of the rate of glucose uptake plotted aganst the recprocal of the absolute temperature for muscle 40 and for lens. The latter s calculated from data n a manuscrpt that was made avalable by Dr. T. G. Farkas. The straght lnes are calculated by the method of least squares.
8 674 Patterson Investgatve Ophthalmology August 965 MUSCLE LENS NCUBATION TIME (mn.) Fg. 4. The 3-0-methylglucose space after dfferent tmes of ncubaton n the absence and presence of glucose. The rate of penetraton s much faster n heart muscle 9 than t s n lens. 33 The curve for lens wthout glucose s the same as n Fg.. The ponts on the curve n the presence of glucose each represent four determnatons. MUSCLE LENS a N0 GLUCOSE NO GLUCOSE GLUCOSE ADDED 9 mm AT 0 mn //, / / t I 5 30 INCUBATION TIME (mn.) f * s ' GLUCOSE ADDED 56 mm AT 30 mm Fg. 5. The 3-0-methylglucose space as t s changed by the addton of glucose after there has been some ntracellular loadng. The dotted lnes reproduce the data of Fg. 4. The addton of glucose s made vvtlout alterng the concentraton of 3-0-methylglucose n the medum. In muscle 9 the 3-0-methylglucose moves out aganst a concentraton gradent untl t reaches a new equlbrum. In lens a3 the same process seems to occur but the change does not demonstrate "counterflow." centraton of ths substance n the cell s determned by the relatve rates of nward and outward transport. The concentraton nsde the cell wll approach that of the outsde but t wll not surpass t. If a hgh concentraton of a compettve sugar that s readly metabolzed, such as glucose, s then ntroduced on the outsde wthout changng the concentraton of the 3-0- methylglucose, a compettve stuaton s created for nward transport. Because the glucose s metabolzed and does not accumulate n the cell, the stuaton for outward transport remans the same. Under
9 Volume 4 Number 4 Glucose transport n lens A H R C, M H E A R T L b S ANOXIA NaCN DNP M3F «DNP DNP ONP ANOXIA NdCN DNP IAA Nap GLUCOSE TRANSPORT PERCENT OF NORMAL mn. 30 mn mm mm rtm*o.25 mm 0.25 mm ] 3 :.O mm 0 JmM 50 mm 25 JmM Fg. 6. The effects of posons on the rate of glucose uptake n rat daphragm, 45 rat heart muscle,' G and rabbt lens. s approprate condtons the rate of nflux of 3-0-methylglucose may be reduced below the rate of efflux wth the net effect beng a temporary (untl a new equlbrum s reached) efflux of 3-0-methylglucose aganst ts concentraton gradent. An attempt to demonstrate counterflow n rat lenses dd result n the demonstraton of competton and dd shft the uptake of 3-0-methylglucose to a new equlbrum poston (Fg. 5) but, wth condtons that were used, counterflow aganst a concentraton gradent was not shown. 33 These experments demonstrate that n muscle and the red blood cell, the process for nward and the process for outward transport are saturated on an ndependent bass. There are three types of posons that affect glucose transport. The frst type s ds- I trbuted n the extracellular space, acts on the cell membrane, and decreases transport. Phlorzn, N-ethylmalemde, and p- chloromercurbenzoate are examples of ths type. 43 The second type of poson nhbts the respratory enzymes, stmulates glycolyss secondarly through the Pasteur effect, and ncreases glucose transport. Ths type ncludes cyande, salcylate, arsente, and dntrophenol. 46 " 47 Anoxa has an effect smlar to that of these posons. 44 The thrd type of poson nhbts glycolyss and nhbts glucose transport. It ncludes fluorde, 45 odoacetate, 47 and acetoacetate. 4S The effects of phlorzn are shown n Tables V and VI. The effects on glucose transport of the nhbton of respraton by anoxa and cyande and the nhbton of glycolyss by fluorde and odoacetate are shown n Fg. 6. The effect of dntrophenol seems to depend on the condtons under whch t s employed. It has been suggested that t nhbts glycolyss as a secondary effect. 40 The nhbtory effect of odoacetate on glucose transport nto the lens was also shown by Mller. 49 The effects of fluorde and odoacetate are mnmal n red blood cells 47 and fluorde has only a small effect on xylose transport nto muscle. 50 Phenylethylbguande (DBI) acts as a respratory poson 5 and ncreases glucose uptake n muscle 5 and rabbt lens. 52 Randle and Morgan 0 have been mpressed by the effects of posons on glucose transport and more partcularly by the stmulatng effect of anoxa and the nhbtory effect of fatty acd metaboltes, such as acetoacetate, on the rate of glycolyss. Table V. Effect of phlorzn on glucose utlzaton of ntact rat lenses ncubated for 30 mnutes at 37 C. n Tyrode's soluton contanng 00 mg. per 00 ml. glucose 04 No. of lenses 0 0 Phlorzn concentraton (mm.) "Uptake from lens plus medum. Glucose utlzaton 0 (mg./gm./hr.) Range Mean
10 676 Patterson Investgatve Ophthalmology August 965 Snce the rate of glucose transport seems to parallel the rate of some of the phosphorylaton steps n glycolyss, there s a possble mechansm for the control of glucose transport on the bass of metabolc need. The parallel behavor of glucose and ts dervatves n muscle and lens supports the vew that the nature of the transport process s the same n these two tssues. The smlartes between muscle and red blood cells are well known, and the demonstraton that another tssue behaves n the same way gves further authentcty to the lmted observatons n lens. The absence of demonstrable ntracellular glucose n the lens ndcates that the rate of transport of glucose s equal to the rate of glucose utlzaton. The qualtatve and quanttatve agreement of the knetcs of glucose utlzaton n lens wth the knetcs of glucose transport n muscle and the red blood cell supports the concluson that the transport process s the same n the membranes of the three tssues. It could be argued, however, that the Km and Q t0 of glucose utlzaton n the lens are reflectons of glucose metabolsm rather than transport and that the quanttatve agreement wth the transport values n other tssues s fortutous. The lmtaton of the dstrbuton of sorbtol n the lens does demonstrate the exstence of a barrer consstent wth the fber membranes, and the lmtaton n the dstrbuton of 3-0-methylglucose by the addton of glucose can be explaned by competton at the membrane level, whereas t cannot be explaned at a metabolc level. Smlarly, the observaton that the accumulaton of glucose, under condtons of glucose "toxcty," s decreased 8 n lenses bathed n meda contanng glycolytc posons, whch can also decrease transport, s readly explaned on the bass of an nhbton of transport at the fber membrane. It cannot be explaned, solely, on the bass of an nhbton of glucose metabolsm. Thus, the complete data on the lens are best explaned by the concept that the fber membrane lmts the access of glucose to the cell, and that the transport of glucose across the membrane takes place by a process smlar to that whch occurs n muscle and red blood cells. As a result of the types of evdence that have been presented for the transport of glucose n tssues such as muscle and red blood cells, there s lttle doubt that glucose nteracts wth the membrane durng the transport process. The nature of the process of medated transport, however, s stll beng debated. A model nvolvng a moble carrer for the transport of glucose across the membrane has ganed great support. 7 ' S 9> 53 ' 54 Recently another model, based on the formaton of a dmer of glucose whch passes through the lpd layer of the membrane to reform the monomer on the other sde, has been suggested. 55 Each of these models s supported by mathematcal treatments whch explan the complex aspects of sugar transport that occur under specal crcumstances. It s clamed, however, that the observed phenomena can also be explaned, on a mathematcal bass, f a fxed membrane carrer s used as a model. ' 5G Danell 0 has suggested that the problem wll not be solved untl more s known about the molecular bass of transport. Recently, Keston 57 has suggested that the enzyme mutarotase may be nvolved n the transport process: The Km of the enzyme s about the same as that for transport; the enzyme s nhbted by phlorzn n a manner smlar to transport, and the rate of glucose utlzaton n varous organs parallels the actvty of mutarotase. Concevably, the formaton of the open chan form of the sugar, as dstnct from the pyranose rng form, mght be a necessary step n transport. Mutarotase has been demon- Table VI. Per cent nhbton of glucose utlzaton by 3 ram. phlorzn n the rat Organ Daphragm Heart muscle Lens Per cent nhbton Reference
11 Volume 4 Number 4 Glucose transport n lens 677 strated n lenses from cattle, rabbts, dogs, and rats. 58 The Km of glucose for rabbt lens s 4 mm. The enzyme s nhbted by galactose and xylose and by sugar alcohols. Clarfcaton of the role of mutarotase n glucose transport must, however, awat further studes. Wlbrandt 2 faled to fnd mutarotase n red blood cells and Crane and Krane 50 seem to dffer wth Keston G0 on the nterpretaton of the results obtaned wth -deoxyglucose, a sugar dervatve whch s not capable of mutarotatng. In ths presentaton, the effects of nsuln on glucose transport have not been consdered. The effect of nsuln on glucose transport n muscle has been studed extensvely. 0 The data on lens, however, are less conclusve. Insuln labeled wth radoactve odne does not enter the aqueous, 0 and nsuln does not stmulate glucose utlzaton n the ntact lens. ls> G2 However, t s reported to have some effect n the decapsulated lens. TS> G3 Insuln njected n a rat pror to sacrfce s reported to ncrease the glucose uptake n the solated lens. 39 Ths work, however, has lacked confrmaton. Further studes, wth dfferent approaches, need to be made. In the meantme, t may be assumed that, under physologcal condtons, nsuln does not have a drect effect on glucose transport n the lens. In concluson, t may be stated that the process of glucose transport n the lens s smlar to the process for the transport of glucose n tssues such as muscle and the red blood cell. If advances are made n our understandng of the transport process n any of these tssues, the results wll probably also apply to the transport of glucose n the lens. REFERENCES. Lefevre, P. G.: The evdence for actve transport of monosacchardes across the red cell membrane, n Brown, R., and Danell, J. F., edtors: Actve Transport and Secreton, New York, 954, Academc Press, Inc., pp Wlbrandt, W.: The sugar transport across the red cell membrane, n Klenzeller, A., and Kotyk, A., edtors: Symposum on Membrane Transport and Metabolsm, Praha, 96, Publshng House of Czechoslovak Academy of Scence, pp Henderson, M. J.: The uptake of glucose nto cells and the role of nsuln n glucose transport, Canad. J. Bochem. 42: 933, Kpns, D. M.: Regulaton of glucose uptake by muscle: Functonal sgnfcance of permeablty and phosphorylatng actvty, Ann. New York Acad. Sc. 82: 354, Park, C. R., Morgan, H. E., Henderson, M. J., Regen, D. M., Cadenas, E., and Post, R. L.: The regulaton of glucose uptake n muscle as studed n the perfused rat heart, n Pncus, C, edtor: Recent Progress n Hormone Research, New York, 96, Academc Press, Inc., pp Randle, P. J., and Morgan, H. E.: Regulaton of glucose uptake by muscle, n Harrs, R. S., and Wool, I. C, edtors: Vtamns and Hormones, New York, 962, Academc Press, Inc., vol. 20, pp Lefevre, P. G., and McGnns, G. F.: Tracer exchange vs. net uptake of glucose through human red cell surface, J. Gen. Physol. 44: 87, Rosenberg, T., and Wlbrandt, W.: The knetcs of membrane transports nvolvng chemcal reactons, Exper. Cell. Res. 9: 49, Wddas, W. F.: Facltated transfer of hexoses across the human erythrocyte membrane, J. Physol. 25: 63, Danell, J. F.: Structure of the cell surface, Crculaton 26: 63, Pre, A.: Composton of the ox lens capsule, Bochem. J. 48: 368, Fredenwald, J. S.: Permeablty of the lens capsule: Wth specal reference to the etology of senle cataract, Arch. Ophth. 3: 82, Becker, B.: Paper presented at IX Conference on Ophthalmc Bochemstry, Dedham, Mass., Feb. 2-23, Becker, B., and Cotler, E.: Dstrbuton of rubdum-86 accumulated n the rabbt lens, INVEST. OPHTH. : 642, 962. ' 5. Knsey, V. E., and Reddy, D. V. N.: Studes on the crystallne lens. XI. The relatve role of epthelum and capsule n transport, IN- VEST. OPHTH. 3: 243, Knsey, V. E., and Reddy, D. V. N.: Studes on the crystallne lens. X. Transport of amno acds. INVEST. OPHTH. 2: 229, Harrs, J. E., and Cruber, L.: The electroylte and water balance of the lens, Exper. Eye Res. : 372, Harrs, J. E., Hauschldt, J. D., and Nordqust, L. T.: Transport of glucose across the
12 67S Patterson Invcstgutoe Ophthalmology August 965 lens surfaces, Am. J. Ophth. 39: (Part II) 6, Morgan, H. E., Regen, D. M., and Park, C. R.: Identfcaton of a moble carrer-medated sugar transport system n muscle, J. Bol. Chem. 239: 369, Knsey, V. E.: Personal communcaton. 2. Cogan, D.: Anatomy of lens and pathology of cataracts, Exper. Eye Res. : 29, Bontng, S. L., Caravaggo, L. L., and Hawkns, N. M.: Studes on sodum-potassum actvated adenosnetrphosphatase. VI. Its role dn caton transport n the lens of cat, calf and rabbt, Arch. Bochem. & Bophys. 0: 47, Sperelaks, N., and Potts, A. M.: Addtonal observatons on the boelectrc potentals of the lens, Am. J. Ophth. 47: 395, Amoore, J. E., Bartley, W., and van Heynngen, R.: Dstrbuton of sodum and potassum wthn cattle lens, Bochem. J. 72: 26, Knoshta, J. H.: Selected topcs n ophthalmc bochemstry, Arch. Ophth. 70: 558, Knoshta, J. H., Merola, L. O., and Dkmak, E.: Osmotc changes n expermental galactose cataracts, Exper. Eye Res. : 405, Langham, M., and Davson, M.: Studes on the lens, Bochem. J. 44: 467, Huggert, A.: Studes on the water of the crystallne lens. 4. The sodum space of rabbt lens n vvo, Acta ophth. 37: 522, Huggert, A.: Studes on the water of the crystallne lens. 2. The extracellular space of the cattle lens measured n vtro, Acta ophth. 37: 26, Wck, A. N., and Drury, D. R.: Acton of nsuln on permeablty of cells to sorbtol, Am. J. Physol. 66: 42, Fsher, R. B., and Lndsay, D. B.: The acton of nsuln on the penetraton of sugars nto the perfused heart, J. Physol. 3: 526, Morgan, H. E., Henderson, M. J.: Regen, D. M., and Park, C. R.:. The effects of nsuln and anoxa on glucose transport and phosphorylaton n the solated, perfused heart of normal rats, J. Bol. Chem. 236: 253, Patterson, J. W., and Buntng, K. W.: Glucose transport n rat lens, Am. J. Physol. In press. 34. Park, C. R., Renwen, D., Henderson, M. J., Cardenas, E., and Morgan, H. E.: The acton of nsuln on the transport of glucose through the cell membrane, Am. J. Med. 26: 674, Farkas, T. C, and Patterson, J. W.: Insuln and the lens, Am. J. Ophth. 44: (Part II) 34, Kuck, J. F. R.: Sugar and sugar alcohol levels n the agng rat lens, INVEST. OPHTH. 2: 607, Lerman, S.: Metabolc pathways n expermental dabetc cataract, INVEST. OPHTH. : 507, Harrs, J. E., Hauschldt, J. D., and Nordqust, L. T.: Lens metabolsm as studed wth the reversble caton shft. I. The role of glucose, Am. J. Ophth. 38: (Part II) 4, Farkas, T. C, Ivory, R. F., and Patterson, J. W.: Glucose uptake and utlzaton of solated lenses for normal and dabetc rats followng nsuln njecton, Anal. Rec. 38: 235, Park, C. R., Bornsten, J., and Post, R. L.: Effect of nsuln on free glucose content of rat daphragm n vtro, Am. J. Physol. 82: 2, Brtton, H. G.: Permeablty of the human red cell to labelled glucose, J. Physol. 70:, Rosenberg, T., and Wlbrandt, W.: Uphll transport nduced by counterflow, J. Gen. Physol. 4: 289, Battagla, F. C., and Randle, P. J.: Regulaton of glucose uptake by muscle. 4. The specfcty of monosaccharde transport systems n rat-daphragm muscle, Bochem. J. 73: 408, Randle, P. J., and Smth, G. H.: Regulaton of the uptake of glucose by the solated rat daphragm, Bochm. et bophys. acta 25: 442, Randle, P. J., and Smth, G. H.: Regulaton of glucose by muscle. 2. The effects of nsuln, anaeroboss, and cell posons on the penetraton of solated rat daphragms by sugars, Bochem. J. 70: 50, Morgan, H. E., Randle, P. J., and Regen, D. M.: Regulaton of glucose uptake by muscle. 3. The effect of nsuln, anoxa, salcylate and 2, 4 dntrophenol on membrane transport and ntracellular phosphorylaton of glucose n the solated rat heart, Bochem. J. 73: 573, Lars, P. C: Permeablty and utlzaton of glucose n mammalan erythrocytes, J. Cell. & Comp. Physol. 5: 273, Ottoway, J. H.: The effects of growth hormone and ketone bodes on carbohydrate metabolsm n daphragm from normal and hypophysectomzed rats, J. Endocrnol. 2: 443, Mller, H. K.: Ueber de resorpton von glucose und askorbnsaure n de lnse, Arch, f. Ophth. 40: 258, Forbath, N., and Clarke, D. W.: Factors nfluencng the dstrbuton of pentoses n the solated rat daphragm, Canad. J. Bochem. Physol. 38: 3, Stener, D. F., and Wllams, R. H.: Actons
13 Volume 4 Ntmber 4 Glucose transport n lens 679 of phenylethylbguande and related compounds, Dabetes 8: 54, Cles, K. M., and Harrs, J. E.: The accumulaton of C u from unformly labeled glucose by the normal and dabetc rabbt lens, Am. J. Ophth. 48: (Part II) 508, Lacko, L., and Burger, M.: Knetc comparson of exchange transport of sugars wth nonexchange transport n human erythrocytes, J. Bol. Chem. 238: 3478, Lefevre, P. G., and Habch, K. I.: Absence of rapd exchange component n a low affnty carrer transport, J. Gen. Physol. 46: 72, Sten, W. D.: Dmer formaton and glucose transfer across the membrane of the red blood cell, Nature 9: 277, Brtton, H. G.: Induced uphll and downhll transport: Relatonshp to the Ussng crteron, Nature 98: 90, Keston, A. S.: Knetcs and dstrbuton of mutarotases and ther relaton to sugar transport, J. Bol. Chem. 239: 324, Keston, A. S.: Inhbton of acton of lens mutarotase on glucose by cataractogenc sugars and correspondng polyols, Arch. Bochem. & Bophys. 02: 306, Crane, R. K., and Krane, S. M.: On the mechansm of ntestnal absorpton of sugars, Bochm. et bophys. acta 20: , Keston, A. S.: Mutarotase nhbton by - deoxyglucose, Scence 43: 698, Gles, K. M., and Harrs, J. E.: Radoelectrophoretc patterns of aqueous and plasma: After ntravenous njecton of I 3 labeled nsuln nto rabbts, Am. J. Ophth. 46: (Part II) 96, Macntyre, M. N., Polt, S. S., and Patterson, J. W.: Glucose uptake by solated normal and dabetc rat lenses, Am. J. Physol. 86: 406, Ross, E. J.: Insuln and the permeablty of cell membranes to glucose, Nature 7: 25, Patterson, J. W., and Buntng, K. W.: Unpublshed data.
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