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1 J Clin Pthol 1983;36: Incresed erythrocyte superoxide dismutse ctivities in f3 -thlssemi/hemoglobin E nd in hemoglobin H diseses P YENCHITSOMNUS, P WSI From the Thlssemi Centre, Fculty of Grdute Studies, nd Division ofhemtology, Deprtment of Medicine, Fculty ofmedicine Sirirj Hospitl, Mhidol University, Bngkok 7, Thilnd SUMMRY Erythrocyte superoxide dismutse ctivities were mesured in 45 subjects, 15 ech of 39-thlssemi/hemoglobin (Hb) E disese, Hb H disese, nd norml. The erythrocyte superoxide dismutse ctivities were significntly higher in the ptients with -thlssemi/hb E nd Hb H diseses thn in the norml subjects. The increse of erythrocyte superoxide dismutse ctivities is most likely due to bnormlities specific to thlssemic red cells rther thn n incresed number of younger red cells for reticulocytes nd nucleted red blood cells did not ffect the enzyme ctivity. Ptients with P.'-thlssemi/Hb E disese with lower hemoglobin concentrtion hd significntly higher superoxide dismutse ctivities. In ll 45 subjects hemoglobin concentrtions nd super6xide dismutse ctivities were inversely correlted (r = -- 6 (p < O- 1)). This indictes tht the mounts of superoxide generted in the red cells my, t lest prtly, determine severity of red cell dmge nd thus severity of disese; the incresed superoxide dismutse ctivity in thlssemi is response to superoxide generted in greter mounts becuse of ccumultion of excessive globin chins nd iron in the red cells. The superoxide dismutse ctivities in Hb H disese, n -thlssemic disese, were found to be strikingly incresed, higher thn in I -thlssemic disese or other conditions. In lrge number of ptients with 8,,-thlssemi/ hemoglobin (Hb) E disese (in untrnsfused stte) hemoglobin concentrtions vry between 3 nd 13 g/dl (men = 7 g/dl). Why ptients with the sme genotype differ so much in severity of disese is interesting nd importnt. One spect which we hve investigted concerns the reltion between erythrocyte superoxide dismutse ctivity nd severity of thlssemi. In the red blood cell, superoxide dismutse is n enzyme tht protects the cell from the deleterious effect of the superoxide free rdicl (-). ' It ctlyses the brekdown of superoxide ccording to the rection: 2 + 2H+ -+ H The hydrogen peroxide (H22) is less dngerous thn superoxide nd is further reduced to wter nd oxygen by ctlse nd glutthione peroxidse. 'I3 The superoxide is thought to be generted in the red blood cell by utoxidtion of hemoglobin. It hs been found tht the utoxidtion of oxyhemoglobins ccepted for publiction 3 June 1982 or isolted oxyhemoglobin chins produces superoxide."6 utoxidtion of unstble hemoglobins or isolted nd,b chins, however, releses superoxide t greter rte thn utoxidtion of Hb. '7 ccumultion of excessive or f8-globin chins is typicl finding in thlssemic red blood cells.8 Therefore, the superoxide is suspected to be generted more esily nd/or in lrger mount in the thlssemic thn in the norml red blood cells. It is thus importnt to mesure the erythrocyte superoxide dismutse ctivity in thlssemi nd exmine its reltion to severity of the disese. ny reltion between erythrocyte superoxide dismutse ctivity nd the severity of thlssemi should revel whether superoxide dismutse ctivity determines the severity of the disese or not. Subjecs ll thlssemic subjects were ptients of Division of Hemtology, Deprtment of Medicine, Fculty of 329
2 33 Medicine Sirirj Hospitl nd norml subjects were hospitl personnel. ltogether 45 subjects were exmined, 15 ech from 13-thlssemi/Hb E disese, Hb H disese nd norml. In the group of (3 -thlssemi/hb E disese five ptients hd hd splenectomy. This group cn be divided into two subgroups of different severity. Group 1 with hemoglobin concentrtions > 8 g/dl consisted of six ptients, ll with spleens intct; group 2 with hemoglobin concentrtions < 8 g/dl consisted of nine ptients, five of whom hd hd splenectomies. Seven ptients with Hb H disese hd the -thlssemi '1/-thlssemi 2 genotype, nd eight hd the,-thlssemi 1/Hb Constnt Spring (Hb CS) genotype. Dignostic criteri for these thlssemic diseses were ccording to previous reports.9 1 Mteril nd methods Riboflvin nd nitroblue tetrzolium (NBT) were purchsed from Sigm Chemicl Co. Beckmn DB-G grting spectrophotometer ws used in the study. bout 5-6 ml of venous blood were drwn both into EDT nd into heprinised tubes. EDT blood ws used for routine complete blood count nd hemoglobin typing nd the heprinised blood ws used for superoxide dismutse study. HEMTOLOGICL STUDIES ND HEMOGLOBIN TYPING Red blood cell count (RBC), men corpusculr volume (MCV), hemtocrit (HCT) nd white blood cell count (WBC) were determined in Coulter Counter model ZF 6. Hemoglobin concentrtions were mesured on Coulter Hemoglobinometer. Hemoglobin types were chrcterised by strch gel electrophoresis in Tris-EDT-Borte buffer, ph ERYTHROCYTE SUPEROXIDE DISMUTSE SSY The heprinised blood ws centrifuged; plsm nd buffy cot were removed by spirtion. Pcked red cells were wshed three times with norml sline. Erythrocyte superoxide dismutse ctivities in chloroform-ethnol extrct were mesured by Tble 1 Yenchitsomnus, Wsi following the method of Winterbourn et l.3 This method depends on the bility of the enzyme to inhibit the reduction of NBT by superoxide, which is generted by the rection of photoreduced riboflvin nd oxygen. Results Results re summrised in Tble 1 nd illustrted in Figs. 1 nd 2. Thlssemic erythrocytes hd higher superoxide dismutse ctivities thn the norml erythrocytes, both on the bsis of U/g Hb nd U/cell. In Hb H disese superoxide dismutse ctivities were strikingly higher thn in (3-thlssemi/Hb E disese. Differences between norml nd, -thlssemi/hb E, norml nd Hb H disese, nd 9 8 m I 7 _ 6o l V :2 x1 " 2 4, 3-1- I\oe ((~C * t I %Ip>'" ~~,Irlll '$ m Non-sp(enec o Sptenec c-thl I/c-thl 2 oc-thll/hb CS Fig. 1 Erythrocyte superoxie dismutse ctivities s UIg Hb ofnorml subjects ndptients with -thlssemilhb E nd with Hb H diseses. Men + SD ofhemoglobin concentrtions nd erythrocyte superoxide dismutse ctivities Norml f -thlssemil Hb H disese (n = 15) Hb E (n = 15) (n = 15) Hemoglobin(g/dl) Superoxide dismutse U/gHb 2563 ± ± ± 1169 U/cell(x 1r) 83± ± ± 2-34 C
3 Incresed erythrocyte superoxide dismutse ctivities in thlssemic diseses Tble 2 Hemtologicl dt nd erythrocyte superoxide dismutse ctivities ofmild nd more severe,b( -thlssemi/hb E disese Hb HCT RBC MCV Superoxide dismutse (gldl) (%) (x / 2/1) (f) U/g Hb xjo- U/cell Group 1 Mild,3-thlssemi/Hb E Men (n = 6) SD Group 2 More severe (-thlssemi/hb E Men (n = 9) SD p<o-oo1 p< -5 Go U :- c 2 1 -x 15-.' ci 4 2 ED n ED. 5 + * * I * Non-sspenec I o Splenec oc-thl I /c-thol 2 & cc-thl I/ Hb CS Fig. 2 Erythrocyte superoxide dismutse ctivities s U/cell ofthe sme three groups ofsubjects s shown in Fig. 1. (3-thlssemi/Hb E nd Hb H disese were ll sttisticlly significnt (p < 1). Hemtologicl dt nd erythrocyte superoxide dismutse ctivity of the mild (group 1) nd the more severe (group 2) (3 -thlssemi/hb E re shown in Tble 2. The group 2 ptients (more severe) hd significntly higher superoxide dismutse ctivities thn the ptients in group 1 (mild) (p < 1 for U/g Hb nd p < 5 for U/cell). To test whether the higher superoxide dismutse ctivity in the ptients with more severe disese ws ttributble to greter reticulocytosis superoxide dismutse ctivity ws lso mesured in the Tble 3 Superoxide dismutse ctivities in top nd bottom lyers ofred blood cellsfrom threeptients with utoimmune hemolytic nemi Subject Renculocyte Superoxide (%) dismutse (U/g Hb) Cse I (Hb = 1 gldl) Whole blood 1-8 Top lyer Bottom lyer Cse II (Hb = 1 gldl) Whole blood 6-6 Top lyer Bottom lyer Cse III (Hb = 5 4 gldl) Whole blood 19 Top lyer Bottom lyer reticulocyte-rich nd reticulocyte-poor frctions of red blood cells from three ptients with utoimmune hemolytic nemi. The results re shown in Tble 3. Discussion 331 The erythrocyte superoxide dismutse ctivities in our thlssemic ptients were significntly higher thn norml. With the exception of one vlue the distribution of superoxide dismutse ctivities in -thlssemi/hb E disese did not overlp with tht of norml, when clculted s U/g Hb. When clculted s U/cell two vlues of (83-thlssemi/ Hb E ptients cme within the norml rnge. One unusully high vlue in the control red cells ws probbly due to error in red cell counting. The erythrocyte superoxide dismutse ctivities in Hb H disese were in generl higher thn in (3othlssemi/Hb E disese. There hve been only three reports on erythrocyte superoxide dismutse ctivity in thlssemi nd their results conflict. Concetti et ll4 nd Gerli et l'5 reported no significnt difference in erythrocyte superoxide dismutse vlues between homozymous (-
4 332 Yenchitsomnus, Wsi Tble 4 Superoxide dismutse ctivities in splenectomised nd non-splenectomised ptients (ll mens + SD) Hb (gidl) WBC(x19/l) NRC* (19/l) Superoxide dismutse ctivity x 1-8 U/cell.UIg Hb Splenectomised (n = 5) ± ± 1-45 Non-splenectomised (n = 1) 8-5± ± ± ± ± 2 9 p>>o-5 p>.4 *Nucleted red cells (NRC) were clculted from totl nucleted cell counts (WBC + NRC) nd NRC/WBC rtios in the blood smer. thlssemi subjects nd norml controls. Vnell et l'6, however, observed significnt differences in erythrocyte superoxide dismutse ctivities between similr groups of subjects. It should be pointed out tht the ptients in these three series hd received blood trnsfusion shortly before the studies. Most of our ptients received no blood trnsfusion lthough few hd been trnsfused severl months before superoxide dismutse mesurement. Thus the superoxide dismutse ctivities found in our study represented truer picture of this enzyme ctivity in thlssemic red cells. There is question whether rised erythrocyte superoxide dismutse ctivities re due to bnormlities specific to thlssemi or due to n increse in the proportion of younger red cells. In generl erythrocyte enzyme ctivities re greter in younger red cell popultions. 7 Thlssemic diseses re usully ssocited with reticulocytosis nd lso often with the presence of nucleted red cells. We checked the effect of reticulocytosis on the erythrocyte superoxide dismutse ctivities in three ptients with utoimmune hemolytic nemi s shown in Tble 3. The red cells were seprted into reticulocyte-rich top lyer nd reticulocyte-poor lyer nd superoxide dismutse ctivities were determined. In spite of reticulocyte counts between the two lyers differing by s much s 14 times, the superoxide dismutse ctivities were not significntly different. Furthermore the erythrocyte superoxide dismutse ctivity in splenectomised ptients with 13-thlssemi/Hb E did not differ from tht of the non-splenectomised ones, lthough the former hd numerous NRC (Tble 4). Thus the incresed erythrocyte superoxide dismutse ctivities in thlssemi found in our study were unlikely to be due to reticulocytosis or reticulocytosis lone. Most likely it ws cused by incresed production of Tble 5 Correltion between superoxide dismutse ctivities nd hemoglobin concentrtions ofll 45 subjects Correlton (y) p Hb v superoxide dismutse (U/g Hb) Hb v superoxide dismutse (U/cell) <-1 <-1 superoxide in thlssemic red cells. In thlssemic red cells there re lwys excessive globin chins. Isolted hemoglobin subunits hve been shown to generte superoxide.67 lso lipid membrne peroxidtion of thlssemic red cells is incresed.'8 These indicte tht superoxide nd other free rdicls re generted in incresed mounts in thlssemic red cells nd re probbly importnt fctors cusing red cell membrne dmge in this disese. The incresed superoxide dismutse ctivity in thlssemic red blood cells my be response to the increse of the free rdicls. Defective globin chin synthesis in thlssemi leds to decresed hem synthesis."' This results in ccumultion of non-hem iron in the red cells s indicted by the presence of sideroblst nd incresed erythrocyte ferritin nd hemosiderin.2i22 Iron is strong oxidnt; together with hemoglobin it leds to superoxide genertion by stimulting hemoglobin utoxidtion. ' Excessive mount of iron in the thlssemic red cells my be nother contributory fctor in incresed superoxide production. Erythrocyte superoxide dismutse ctivities in the splenectomised nd non-splenectomised ptients did not significntly differ (Tble 4). Splenectomised ptients hd numerous nucleted red cells. The presence of nucleted red cells did not seem significntly to ffect the erythrocyte superoxide dismutse ctivities. Splenectomy in thlssemi is usully ssocited with incresed proportion of red cells with excessive hemoglobin chins which pper s inclusion bodies.23 These inclusion bodies my be expected to generte more superoxide but perhps not enough to result in significntly incresed superoxide dismutse ctivities. s shown in Tble 2 the group of ptients with hemoglobin <8 g/dl hd significntly higher erythrocyte superoxide dismutse ctivities (p < O- 1 nd p < O 5) thn the group with hemoglobin >8 g/dl. The erythrocyte superoxide dismutse ctivities showed inverse correltion with hemoglobin concentrtions with correltion coefficient of - 6 (Tble 5). Whether rised erythrocyte superoxide dismutse ctivity determines the severity of the thlssemic disese or not is interesting. If the
5 Incresed erythrocyte superoxide dismutse ctivities in thlssemic diseses erythrocyte superoxide dismutse ctivity is independent to severity of the disese one would expect tht thlssemic ptients with higher erythrocyte superoxide dismutse ctivities would run milder course, for superoxide would be neutrlised to lrger extent nd would therefore be less deleterious to red cells. However, the opposite ws observed in this study-tht is, higher erythrocyte superoxide dismutse ctivities were ssocited with more severe disese. This indictes tht incresed erythrocyte superoxide dismutse ctivities in thlssemi is rection to or compenstes for the increse in superoxide. In Hb H disese the erythrocyte superoxide dismutse ctivities were strikingly high, probbly highest mong conditions so fr reported. This hs not been known before. This is probbly due to the presence of excessive (3-chins generting incresed mounts of superoxide in red blood cells. The red blood cells of ptients with Hb H disese hve lso been found to show remrkble increse in glutthione peroxidse ctivity.24 The most likely explntion is tht erythrocytes with Hb H, which is n unstble hemoglobin, generte superoxide in incresed mounts leding to incresed superoxide dismutse ctivities which ctlyse the brekdown of superoxide into hydrogen peroxide resulting in high ctivities of glutthione peroxidse, n enzyme prticipting in conversion of hydrogen peroxide to wter nd oxygen. This investigtion ws supported by US Public Helth Service reserch grnt M 985 from the Ntionl Institute of rthritis, Metbolism, nd Digestive Diseses. References 'Crrell RW, Winterboum CC, Rchnmilewitz E. nnottion: ctivted oxygen nd hemolysis. Br J Hemtol 1975;3: Fridovich I. Superoxide dismutse. nn Rev Biochem 1975;44: Fridovich I. The biology of oxygen rdicls. Science 1978;21: Misr HP, Fridovich I. The genertion of superoxide rdicl during the utoxidtion of hemoglobin. J Biol Chem s 1972;247: Wever R, Oudeg B, Vn Gelder BF. Genertion of superoxide rdicls during the utoxidtion of mmmlin oxyhemoglobin. Biochim Biophys ct 1973;32: Brunori M, Flcioni G, Fioretti E, Girdin B, Rotilio G. 333 Formtion of superoxide in the utoxidtion of the isolted nd.8 chins of humn hemoglobin nd its involvement in hemichrome ittion. EurJ Biochem 1975;53: Winterbourn CC, M th BM, Crreil RW. Rections involving superoxide nd norml nd unstble hemogbbins. Biochem i 1976;1SS: Wetherll DJ, Clegg JB. The lnoemi syndromes. 3rd ed. Oxford: Blckwell Scientifc Publictions, 'Wsi P, N-Nkom S, Pootrkul S, et l. lph- nd betthlssemi in Thilnd. nn NYcd Sci 1969;1K5:6-82. ' Wsi P, N-Nkorn S, Pootrkul S. Tne thlssemis. Clin Hemtol 1974;3: "Smithies. Zone eectrophoresis in strch gels. Group vritions in the serum proteins of norml humn dults. Biochem J 1955,61: Boyer SH, Finer DC, Nughton M. Myoglobin: inherited structurl vrint in mn. Science 1963;14: Winterbourn CC, Hwkins RE, Brin M, Crrell RW. The estimtion of red celi superoxide dismutse ctivity. J Lb Clin Med 1975;85: Concetti, Mssei P, Rotilio G, Brunori M, Rchmilewitz E. Superoxide dismutse in red blood ceils: method of ssy nd enzyme content in norml subjects nd in ptients with 8 - thlssemi (mjor nd intermedi). J Lb Clin Med 1976;87: Gerli GC, Berett L, Binchi M, Pellegtt, gostoni. Erythrocyte superoxide dismutse, ctlse nd glutthione peroxidse ctivities in 9 -thlssemi (mjor nd minor). Scnd JHemtol 198;25: Vnell, Rizz V, Li Volti S, Pinturo R, Musumeci S, Mollic F. Effect of polymines on utohemolysis: studies on norml nd thlssemic children. ct Hemtol 198;63: Wintrobe MM, Lee GR, Boggs DR, Bitheli TC, thens IW, Foerster J. Clinicl hemtology. 7th ed. Phildelphi: Le & Febiger, 1974: " Rchmilewitz E, Lubin BH, Shohet SB. Lipid membrnce peroxidtion in bet thlssemi mjor. Blood 1976;47: "9 Bnnermn RM. bnormlities of heme nd pyrrole metbolism in thlssemi. nn NYcd Sci 1964;119: Pollick, Rchmilewitz E. Ultrstucturl studies in i3-thlssei mjor. BrJHemtol 1973;24: Buminger ER, Cohen SG, Ofer S, Rchmilewitz E. Quntittive studies of ferritinlike iron in erythrocytes of thlssemi, sickle-ceil nemi, nd hemoglobin Hmmersmith with M6ssbuer spectroscopy. Proc Nd cd Sci US 1979;76: Jcobs, Peters SW, Buminger ER, Eikelboom J, Ofer S, Rchmilewitz E. Ferritin concentrtion in norml nd bnorml erythrocytes mesured by immunordiometric ssy with ntibodies to hert nd spleen ferritin nd Mbssbuer spectroscopy. Brl Hemtol 1981;49: Fesss P. IndCusions of hemoglobin in erythroblsts nd erythrocytes of thlssemi. Blood 1963;21: Beutler E, Mtsumoto F, Powrs D, Wrner J. Incresed glutthione peroxidse ctivity in -thlssemi. Blood 1977;5: Requests for reprints to: Professor P Wsi, Division of Hemtology, Sirirj Hospitl, Bngkok, Thilnd.
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