Leukotriene B4-like material in scale of psoriatic skin lesions

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1 Br. J. Pharma. (1984), 83, Leukotriene B4-like material in sale of psoriati skin lesions S.D. Brain1, R.D.R. Camp, F.M. Cunningham, P.M. Dowd, M.W. Greaves & A. Kobza Blak Wellome Laboratories for Skin Pharmaology, Institute of Dermatology, St. John's Hospital for Diseases of the Skin, Homerton Grove, London 9 6BX 1 Aidi lipid extrats of sale from the lesions of the skin disease, psoriasis, were purified by straight phase high performane liquid hromatography (h.p.l..). Assay of frations by an agarose mirodroplet hemokinesis method showed the presene of biologially ative material that oeluted with standard leukotriene B4 (LTB4). 2 LTB4-like hemokineti ativity was also deteted in frations olleted on reversed phase h.p.l.. of psoriati sale extrats that were initially purified by straight phase h.p.l.. 3 No LTB4-like ativity was deteted after similar purifiation of sale obtained by abrasion of large areas of normal skin. 4 The LTB4-like material found in extrats of psoriati sale may play a role in the pathogenesis of the neutrophil infiltrate whih haraterizes psoriasis. Introdution The ommon hroni skin disease, psoriasis, is haraterized by epidermal proliferation and inflammatory hanges, inluding intraepidermal neutrophil infiltration whih has been reported to be one of the earliest events in the evolution of lesions (Chowanie et al., 1981). The generation of neutrophil hemoattratants within the epidermis may be important in the indution of this neutrophil infiltrate. Several lipoxygenase metabolites of arahidoni aid exhibit hemotati ativity towards neutrophils in vitro, leukotriene B4 (5S, 12R-dihydroxy-6, 14-is-8, 1- trans-eiosatetraenoi aid, LTB4) being the most potent (Turner et al., 1975; Goetzl & Sun, 1979; Palmer et al., 198). The presene of biologially ative amounts of LTB4- and monohydroxyeiosatetraenoi aid (monoht)-like material in fluid from hambers attahed to abraded psoriati skin lesions has been reported (Brain etal., 1982; 1983a). In addition several monoht ompounds have been onlusively identified by gas hromatographymass spetrometry (g..-m.s.) in extrats of hamber fluid and superfiial sale from lesional psoriati skin (Camp et al., 1983). The present paper onerns the I Present address: Department of Pharmaology, Institute of Basi Medial Sienes, Royal College of Surgeons, Linoln's Inn Fields, London WC2A 3PN. analysis of sale samples from psoriati lesions and from the skin of normal volunteers for LTB4-like material. Part of this work has been ommuniated to the British Pharmaologial Soiety (Brain et al., 1983b). Methods Volunteers Volunteers were patients with untreated plaque psoriasis or healthy Institute staff reeiving no mediation. Volunteers had given informed onsent, and the projet was approved by the Institute thial Committee. The surfae of psoriati lesions or the entire bak of eah normal volunteer was gently abraded with a salpel blade, and the samples so obtained were stored at - 2 C. Sample purifiation In preliminary experiments, 4 lesional psoriati sale (15-16mg) and 5 normal skin sale (1-7mg) samples were eah added to 6 ml ethyl aetate and 6 ml.1 M sodium aetate buffer, ph 3.5 and vortex- () The Mamillan Press Ltd 1984

2 314 S.D. BRAIN etal. mixed. After entrifugation and removal of the upper organi phase, two further partitions with ethyl aetate were arried out. The organi phases were pooled, evaporated and vauum desiated. To remove non-polar material, the residue was partitioned between 4 ml n-heptane and 3 ml methanol. The upper phase was disarded, the lower layer evaporated, and the residue subjeted to straight phase high performane liquid hromatography (h.p.l..). In this system a Nuleosil 5-5 lum silia olumn (25 m x 4.9 mm i.d.) was eluted with hexane/ propan-2-ol/ methanol/aeti aid (88:7:5:.1, by vol.) at lmlmin-1. ffluent frations (lml) were olleted, evaporated and the residues redissolved in.3 ml agle's Minimal ssential Medium (MM) buffered to ph 7.4 with 3 mm N-2- hydroxyethylpiperazine - N'-2-ethanesulphoni aid (HPS) buffer. The hemokineti ativity of eah fration, and a ten-fold dilution, was determined by using an agarose mirodroplet hemokinesis method. Four samples (eah of 75 mg) of lesional psoriati sale were then further purified by onseutive straight and reversed phase h.p.l.., as follows. Aidi lipids in eah sale sample were extrated into ethyl aetate as desribed above, and, following evaporation, eah organi residue was partitioned between a 75r x Y z 2 ml.1 M sodium phosphate buffer, ph 8.5, and 2 ml 1-hlorobutane.Monohydroxy fatty aids and less polar material are preferentially soluble in the hlorobutane layer whilst LTB4 and more polar material remain in the aqueous phase. After a further partition with 2 ml 1-hlorobutane, the aqueous layer was aidified by addition of 2 ml.1 M sodium aetate buffer, ph 3.5, and extrated 3 times with 4 ml ethyl aetate. The pooled ethyl aetate phases were evaporated, vauum desiated and subjeted to straight phase h.p.l.. as desribed above. For eah sample, a fration o-eluting with standard LTB4 was olleted, evaporated and re-purified by reversed phase h.p.l.. on a Spherisorb S5ODS olumn (25 m x 4.9 mm i.d.) eluted with methanol/water/aeti aid (8:2:.1, by vol.) at 1 ml min-. Frations (1 ml) were olleted, evaporated and redissolved in.3 ml MM for assay of hemokineti ativity. The profile of biologial ativity was ompared with that in four 75 mg samples of normal sale purified in an idential manner. In order to obtain the required amount of normal sale, material from a number of volunteers was pooled. To ensure that there was no ontamination of biologial samples with standard LTB4, frations (1 ml) with elution times similar to LTB4 were olleted, evaporated and assayed for hemokineti 5h- b 5r ) GI.2_ U ) -C C..25F n.251- TV1 7 mhf F Fration number Figure 1 Chemokineti ativity in extrats of psoriati sale (15 mg) after purifiation by straight phase h.p.l.. The results of two experiments (a and b) are shown. ah h.p.l.. fration was evaporated and redissolved in.3 ml MM. The profiles shown were obtained when ten fold dilutions were assayed for hemokineti ativity. Ativity has been expressed as the distane moved by PMNs less random movement in the presene of MM alone. The mean of dupliate observations is given for eah h.p.l.. fration. lution times of standard 12-HT (X), 5-HT (Y) and LTB4 (Z) are given.

3 LUKOTRIN B4 IN PSORIASIS 315 ativity, after blank injetion of h.p.l.. solvent. This proedure was performed after eah injetion of standard LTB4, before purifiation of sale extrats. Further haraterization of LTB4-like material in psoriati sale was ahieved by obtaining an ethyl aetate extrat of bulked sale (5 mg) as desribed above. The organi residue was partitioned between n-heptane and methanol, and the evaporated methanol phase purified by the straight phase h.p.l.. system desribed above. A fration orresponding to the elution time of standard LTB4 was olleted, evaporated, vauum desiated and stored in methanol. A portion of the sample was evaporated and redissolved in MM and the hemokineti ativity determined. The remaining methanol solution was then evaporated and suffiient MM added to give a. 75r- biologial ativity orresponding to that of 2.9 x 1-M LTB4. Appropriate dilutions were made and the dose-response urve thus obtained was ompared with that of standard LTB4 (8.9 x 1-11_2.9 x 1-9M; 3-96 pg per well) in the same assay. Chemokinesis assay Chemokineti ativity for human peripheral blood polymorphonulear leuoytes (PMNs) was assayed by the agarose mirodroplet hemokinesis method (Smith & Walker, 198). Chemokineti ativity has been expressed as the distane moved by PMNs (mm) or as LTB4 equivalents when h.p.l.. frations o-eluting with standard LTB4 were assayed against b 75r- U5F 5F C.,_ 25[-.25F 2 FT_ d Fration number Figure 2 Chemokineti ativity in reversed phase h.p.l.. frations after preliminary purifiation of two psoriati sale extrats (a and b) and two normal sale extrats ( and d) by straight phase h.p.l.. ah fration was evaporated, redissolved in.3 ml MM and assayed without further dilution. Ativity has been expressed as the distane moved by PMNs less random movement in the presene of MM alone. The mean of dupliate observations is given for eah h.p.l.. fration. Arrows show the elution times of standard leukotriene B4.

4 316 S.D. BRAIN etal. standardltb4(3. x 1-l'-3. x 1-9M; 1-1pg per well). Materials Organi solvents, 12-HT, 5-HT and materials used in the agarose mirodroplet hemokinesis assay were obtained as desribed (Camp et al., 1983) exept for Indubiose A37 (Unisiene, London, U.K.). LTB4 was a gift from Dr J. Rokah, Merk Frosst, Point-Claire Dorval, Canada. 1-Chlorobutane (h.p.l.. grade) was obtained from Fisons, Loughborough and all other reagents from B.D.H., Poole. Results 1 5r a1).4_1 o 1O _C a) 75 Dilution r After purifiation of 4 lesional psoriati sale samples (15-16 mg) by straight phase h.p.l.., hemokineti ativity was measurable in frations o-eluting with standard LTB4 and the two monohydroxy fatty aids, 12-HT and 5-HT, whih are poorly separated by this system. Figure 1 shows two representative h.p.l.. profiles. Assay of the ative material in h.p.l.. frations o-eluting with LTB4 against standard LTB4, revealed that the 4 psoriati sale samples ontained a mean of 435 pg LTB4 equivalents per 1 mg sale (range 18-8 pg per 1 mg). These values have not been orreted for losses inurred during purifiation. The presene of hemokinetially ative amounts of monohtlike material in straight phase h.p.l.. frations of psoriati sale is also demonstrated in Figure 1, and agrees with published data (Hammarstrom et al., 1975;Camp et al., 1983). The 5 normal sale samples (1-7 mg) were purified by straight phase h.p.l.. and the evaporated frations redissolved in.3 ml MM. Assay of eah fration without further dilution led to variable profiles of hemokineti ativity, and where ative material was seen to elute in the region of LTB4 (in 3 out of 5 samples) broad peaks were obtained whih laked the disrete shape of those seen on purifiation of psoriati samples. In order to larify whether the hemokineti ativity in normal sale ould be attributed to LTB4-like material, 4 samples (75 mg eah) were extrated, partitioned and purified by the 2 h.p.l.. systems desribed. ffluent frations from the seond h.p.l.. system ontained no signifiant hemokineti ativity. In ontrast, 4 psoriati sale samples (75 mg eah), when purified by the same two h.p.l.. systems, all ontained LTB4- like material. Representative profiles of biologial ativity are shown in Figure 2. When the ative frations were assayed against standard LTB4 the mean value of LTB4 equivalents per 1 mg sale was alulated to be 353 pg (range pg). I. I - 5xlo s1 " LTB4 on. (M) Figure 3 Dose-response urves to standard leukotriene B4 (LTB4, 8.9 x 1-II to 2.9 x 1-9 M, ) and the LTB4-like material obtained on purifiation of psoriati sale extrats by straight phase h.p.l.. (A). The onentration of standard LTB4 is given on the lower horizontal axis and the dilution of LTB4-like material from psonati sale on the upper horizontal axis. Results are expressed as mean (n = 4) with s.e.mean shown by vertial lines. After purifiation of a bulked psoriati sale sample (5 mg) by straight phase h.p.l.. and assay of dilutions of the fration o-eluting with LTB4 for hemokineti ativity, as desribed, a log doseresponse urve losely resembling that of standard LTB4 was obtained (Figure 3). Similar results were obtained in a seond suh experiment. Disussion Straight phase h.p.l..-purified extrats of lesional psoriati sale were shown to ontain biologially ative amounts of both LTB4- and monoht- like material (Figure 1). Chemokineti ativity o-eluting with LTB4 was also present after purifiation of psoriati sale extrats by 2 onseutive h.p.l.. systems (Figure 2a and b). Further evidene for the presene of a ompound with similar biologial properties to LTB4 in psoriati sale was provided by the lose similarity between the dose-response urve generated by suh material in straight phase h.p.l..- purified sale extrats, and that generated by standard LTB4 (Figure 3). The identity of the material ausing the variable hemokineti ativity in straight phase h.p.l.. frations of normal sale extrats has not been deter-

5 LUKOTRIN B4 IN PSORIASIS 317 mined. When normal sale was subjeted to partition and purifiation by the two h.p.l.. systems desribed, no hemokineti ativity o-eluting with standard LTB4 was found (Figure 2 and d). This is in ontrast to the results obtained with psoriati sale where LTB4-like material was observed onsistently after both straight phase h.p.l.. and straight phase followed by reversed phase h.p.l.. We have therefore onluded that normal sale does not ontain signifiant amounts of LTB4. The presene of LTB4-like material in extrats of lesional, but not normal sale is onsistent with the possibility that this material plays a role in the pathogenesis of the psoriati neutrophil infiltrate. These results support the previous finding of LTB4- like material in extrats of hamber fluid from abraded psoriati lesions (Brain et al., 1982; 1983a). Topial appliation of 5-5 ng LTB4 to the skin of human volunteers produes loalized erythema and swelling, and histologial examination shows intraepidermal neutrophil miroabsesses with some similarities to those seen in aute pustular psoriasis (Camp et al., 1984). Neutrophils are however apable of produing LTB4 upon stimulation (Borgeat & Samuelsson, 1979), and it is not yet lear whether the release of LTB4-like material in psoriati lesions is a primary phenomenon or ours after neutrophils have infiltrated the skin. In addition, the struture of the LTB4-like material found in extrats of psoriati sale has, as yet, not been onfirmed as being idential to that of authenti LTB4 by physiohemial methods suh as g..-m.s. Analysis by ultraviolet absorbane spetrophotometry or g..-m.s. requires relatively large amounts of material; experiments using the latter tehnique are however in progress. Determination of the exat role of the LTB4-like material in psoriasis must await its strutural identifiation, and the availability of speifi lipoxygenase inhibitors or reeptor antagonists. This work was supported in part by grants from The Wellome (S.D.B. and F.M.C.) and The Dunhill Trust (A.K.B.). We are grateful to S. Mistry, V. MIntosh and J. Isaas for skilled assistane. Referenes BORGAT, P. & SAMULSSON, B. (1979). Arahidoni aid metabolism in polymorphonulear leukoytes: effet of alium ionophore A Pro. natn. Aad. Si. U.S.A., 76, BRAIN, S.D., CAMP, R.D.R., DOWD, P.M., KOBZA BLACK, A., WOOLLARD, P.M., MALLT, A.I. & GRAVS, M.W. (1982). Psoriasis and leukotriene B4 (letter). Lanet, ii, BRAIN, S.D., CAMP, R.D.R., DOWD, P.M., KOBZA BLACK, A., WOOLLARD, P.M., MALLT, A.I. & GRAVS, M.W. (1983a). Release of leukotriene B4 (LTB4) and monohydroxyeiosatetraenoi aids (HTs) from the involved skin of patients with psoriasis. In Leukotrienes and other Lipoxygenase Produts. ed. Piper, P.J. pp Chihester: Wiley. BRAIN, S.D., CAMP, R.D.R., MALLT, A.I., WOOLLARD, P.M. & GRAVS, M.W. (1983b). Hydroxy fatty aid lipoxygenase produts are present in superfiial psoriati sale. Br. J. Pharma., Pro. Suppl. 79, 359P. CAMP, R.D.R., MALLT, A.I., WOOLLARD, P.M., BRAIN, S.D., KOBZA BLACK, A. & GRAVS, M.W. (1983). The identifiation of hydroxy fatty aids in psoriati skin. Prostaglandins, 26, CAMP, R.D.R., RUSSLL JONS, R., BRAIN, S., WOOL- LARD, P. & GRAVS, M.W. (1984). Prodution of intra-epidermal miro-absesses by topial appliation of leukotriene B4. J. Invest. Dermatol., (in press). CHOWANIC, O., JABLONSKA, S., BUTNR,.H., PRO- NIWSKA, M., JARZABK-CHORZLSKA, M. & RZSA, G. (1981). arliest linial and histologial hanges in psoriasis. Dermatologia, 163, GOTZL,.J. & SUN, F.F. (1979). Generation of unique monohydroxyeiosatetraenoi aids from arahidoni aid by neutrophils. J. exp. Med. 15, HAMMARSTROM, S., HAMBRG, M., SAMULSSON, B., DULL,.A., STAWISKI, M. & VOORHS, J. (1975). Inreased onentrations of non-esterified arahidoni aid, 12L-hydroxy-5,8,1,14-eiosatetraenoi aid, prostaglandin 2 and prostaglandin F2a in epidermis of psoriasis. Pro. natn. Aad. Si. U.S.A., 72, PALMR, R.M.J., STPNY, R.J., HIGGS, G.A. & AKINS, K.. (198). Chemokineti ativity of arahidoni aid lipoxygenase produts on leukoytes of different speies. Prostaglandins, 2, SMITH, M.J.H. & WALKR, J.R. (198). The effets of some antirheumati drugs on an in vitro model of human polymorphonulear leuoyte hemokinesis. Br. J. Pharma. 69, TURNR, S.R., TAINR, J.A. & LYNN, W.S. (1975). Biogenesis of hemotati moleules by the arahidonate lipoxygenase system of platelets. Nature, 257, (Reeived Marh 3, 1984.)

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