DOPA AND THE RED, BROWN AND BLACK PIGMENTS OF HAIR AND FEATHERS*
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1 THE Joume4u. or JNYEBTIGATIYE DERMATOLOGY Copyrigh 1969 by The Williams & Wilkios Co. Vol. 53, No. 4 Prined in U.S.A. DOPA AND THE RED, BROWN AND BLACK PIGMENTS OF HAIR AND FEATHERS* E. M. NICHOLLS, MD. ABSTRACT 1. Pigmens were exraced from mammalian hair and he feahers of domesic poulry by heaing wih hydrochloric acid. 2. Equimolar proporions of dopa and cyseine when aced on by FeCI3 produced pigmens hough o be he same as naurally occurring richosiderins and and black melanins, he proporions of pigmen in any mixure being dependen on he ph of he reacion mixure. 3. Column chromaography and hin layer chromaography were used o produce chromaograms of high resoluion, and hese chromaograms demonsraed a precise agreemen beween pigmens produced a paricular ph levels in he arificial mixure and he pigmens in he hair or feahers of a paricular animal or bird. Sorby in 1878 (1) described he exracion of pigmens from human hair of various colors. Bourquelo and Berrand (2) found yrosine in he oadsool Ru.s.sula nigrican.s in 1895 and demonsraed is imporance in he formaion of black pigmen. Subsequenly he involvemen of yrosine in mammalian melanogenesis was proposed and he chemical pahway from yrosine o melanin was sudied (3). The relaion beween and black melanin has never been clearly defined and he pigmen richosiderin (4 11) and oher pigmens exracable from red hair have no been inegraed ino a general concep of melanogenesis. Flesch and Rohman described richosiderin as a phenolie iron compound lacking sulphur (4). Bold claimed ha riehosiderin conained boh iron and sulphur (7). Proa and Nicolaus (9) saed ha i conained sulphur bu no iron, a view laer acceped by Bold and Hermsed (1). Chromaographic separaion of red melanie pigmen by Proa and Nicolaus (9) suppored previous work in which a number of componens had been demonsraed. They showed ha a mixure of dopa (3-4 dihydroxyphenylalanine), cyseine and poassium ferncyanide in alkaline soluion produced pigmens The auhor is grealy indebed o Professor K. G. Rienis of he School of Biochemisry, Universiy of New Souh Wales, who aced as echnical advisor in he course of his sudy, made many helpful suggesions, and read his paper criically. Received April 1, 1969; acceped for publicaion May 27, * From he School of Human Geneics, Universiy of New Souh Wales, Sydney 32 wih he characerisics of some componens of he naural red pigmen. Cleffmann (12) in 1963 had shown ha gluahione or cyseine added o a culure of hair bulbs from he agoui mouse changed he characer of pigmen produced from or black o yellow bu a his ime lile was known of he chemisry of he red pigmens. Nicholls (13, 14) sudied geneic aspecs of he human red hair phenoype and (15) recorded microspeerophoomery of hair pigmens and showed similariies beween he pigmens in red and human hair. In his paper experimens which were conduced wih a mixure of dopa, cyseine and fernie chloride are described and i is shown ha a number of pigmens may be produced in such a mixure. Two ehromaographio mehods were developed for making comparisons beween pigmens of hair and feahers, and hese arifleally produced pigmens. The deailed agreemen beween pigmenary componens from he wo sources suggess ha he process of melanogenesis in vivo mus bear a close relaionship o he mehod of synhesis described. MATERIALS AND METHOD5 Pigmens of human and mammalian hair of various colors, and of feahers of domesic poulry were sudied. The laer provided a paricularly useful source of maerial. Two mehods of exracion of pigmen were used. In he firs mebod a sample of approximaely 25 gm of hair or feahers was heaed in ion HC1 in a sealed vessel a 5 C for 72 hours. The
2 DOPA AND RED, BROWN AND BLACK PIGMENTS 33 acid digesed he kerain of he sample, some pigmens passed ino soluion, and he remainder became suspended in he acid or formed a precipiae. This mehod ensured an assay of he oal pigmenary saus of a sample alhough he chromaograms obained were much less clear han hose obained by he alernaive mehod. To obain pigmens suiable for specrophoomery following chromaographic separaion, 2 5 gm of red hair or feahers was boiled in 2 ml of.1n HC1 for half an hour. The pigmens obained in soluion were precipiaed a neural PH, colleced by cenrifugaion and washed several imes in disilled waer. The pigmen was finally redissolved in 4N HC1. In his mehod acid soluble red and yellow pigmens were obained in soluion, while much of he acid insoluble pigmen was no exraced. The laer, held in suspension by he concenraed acid, conribued grealy o he indisincness of chromaograms of samples prepared by he firs exracion mehod. Chromaography. Thin layer chromaography (TLC) using Kieselgel G and column chromaography using Biogel P4 were used o effec separaion of pigmen componens. The exracs obained by digesion in ion acid were spoed ono a hin layer plae and, while he spo was sill we wih acid, he chromaogram was developed wih phenol:waer solven (4:1, W:W) a room emperaure. Pigmen exraced by O.IN HC1 and subsequenly redissolved in 4N HC1 was inroduced in 2 ml quaniies o he op of a Biogel column (1.5 cm. diameer and 1 cm. in lengh in acid medium), and 4N HC1 was passed hrough he column under 15 lbs/sq in. pressure. The fracions obained were re-run hrough he column once or wice o purify major componens. For comparisons wih componens seen on TLC, column fracions were concenraed by boiling and applied direc o he hin layer plae as before. The resoluion of TLC was much greaer han ha of he column and fracions from he columns were shown o have several componens. Specro phoomery. The pigmen in fracions from he columns was precipiaed a neural ph, colleced by cenrifugaion, washed in disilled waer, colleced and dissolved in N NaOH,.1N HC1, N HC1 and ion HC1 for specrophoomery in a UNICAM SP8 recording specrophoomeer. The specral curves of minor componens, where i was possible o record hem, were obained by concenraing an appropriae fracion from he Biogel column, separaing he pigmens on TLC, and scraping off he paricular pigmened band. The Kieselgel wih adsorbed pigmen was washed in disilled waer several imes, o remove phenol, and he pigmen was hen recovered by soluion in HC1. Pigmen synhesis. A soluion conaining a concenraion of.oo1m cyseine hydrochloride and.oo1m dopa was prepared. To 1 ml of his soluion 2 ml of O.1M FeCla was added (o give a concenraion of.2m FeCls). Immediaely, a variable quaniy of.1n NaOH (.1 ml incremens in a series of preparaions) was added producing ph values ranging from 2 o 1. ph readings were aken a inervals and he producion of pigmen was observed. Afer 24 hours 2 ml of ion HC1 was added o each soluion and he soluions were boiled. Afer evaporaion o approximaely one quarer of he original volume he pigmened soluions were subjeced o chromaography by he mehods used for naural pigmens. RESULTS Chromaography Naural pigmens. The iniial effec of running phenol-waer solven hrough a highly acid spo of pigmen on TLC was o produce a diffused spo or band of pigmen wih no definable componens. However, afer he solven fron had progressed 3 1 cm disinc bands of pigmen became apparen. These always occupied he same relaive posiions on he plae, perhaps because of differing concenraions of HC1 a differen levels. The disance raveled by a paricular band in any experimen was variable. In Table I he pigmens found o be presen in samples of hair or feahers afer complee digesion in acid are shown. The sequence of pigmens from fases moving o slowes moving on he hin layer plae are numbered The fases moving pigmens, alhough shown in he able as bands, Brown I and Brown 2, usually cause a grea deal of sreaking on he hin layer plae, and end o obscure oher bands seen much more clearly in samples exraced by oher mehods. For he purpose of making comparisons wih arificial preparaions, a visual assessmen of proporions of pigmens has been made, o being variable amouns of pigmen deecable on he plae, while "" represens a race deecable only by concenraing he pigmen from a large volume of exrac. The pigmen soluion passed hrough he Biogel column was divided somewha aribrarily ino six fracions. A small yellow fracion was followed by a large and disinc blue fracion, hen a red purple fracion, hen he larges fracion of red pigmen, and finally yellow red pigmen moving slowly down he column. Brown pigmen remained a he origin unil elued wih.1 N NaOH, when i flowed
3 34 THE JOURNAL OF INVESTIGATIVE DERMATOLOGY TABLE I Thin layer chromaography of pigmens exraced from hair and feahers using 1 N HUl Pigmens irs Rf order, from fases moving o slowes moving Colour of En I En 2 Y I Y 2 Red 1 Y 3 Blue Red 2 Bn 3 Y 4 Bn 4 Bn 5 Black Red feahers Human red hair Red Hereford cow Red dog Human hair Brown dog Human black hair Black dog Black cow Black feahers - -{--J--j- --f----f- Pigmen bands blurred. Much sreaking of pigmen. o : various esimaes of componens deecable on plae. = race deecable only by passage hrough Biogel column, concenraion and TLC. = no clearly idenifiable on TLC bu possibly presen. Bn = Brown Y Yellow freely hrough he column which suggess ha i was originally suspended in he acid raher han presen in rue soluion. The mechanism of he separaion of he soluble fracions did no appear o be rue gel filraion as some small molecules, e.g., FeCl3, ran ahead of he pigmens. The srengh of he acid was imporan in obaining saisfacory separaion and he forces effecing separaion may have been closely analogous o hose operaing in he TLC sysem used. Table II shows he proporions of pigmens (separaed by hin layer chromaography) presen in he fracions obained from he Biogel column, using pigmen exraced from Rhode Island red feahers. Arificial pigmens. The iniial ph of he dopa, cyseine and FeC13 mixure is shown in he firs row of Table III, while he effec of adding.1n NaOH o each 1 ml of soluion is shown in he lower rows. The relaion beween p11 change and amoun of added NaOH is no linear. Small amouns of added NaOH (.1.3 ml) produced a minor ph change. Addiion of.4.6 ml produced a rise o a new plaeau. A seady rise occurred wih.7 and.8 ml, and above.8 ml he soluion became rapidly more alkaline. The color changes a various ph levels were very rapid, much pigmen being produced wihin he firs 15 seconds of reacion. The change in color of he soluions became sabilized o a cerain exen a he end of his ime, and he resulan color is shown in Table III as "immediae color change" and his varied wih he ph. Afer 1 2 minues, in he more acid soluions, he evoluion of color alered qualiaively and a complee change of color occurred wihin 3 minues. Wihin 24 hours much pigmen had precipiaed excep in he
4 DOPA AND RED, BROWN AND BLACK PIGMENTS 35 TABLE II Pigmens in Rhode Island red feahers in fracions from Bio gel column, as demon sraed by hin layer chromaography Pigmens in RI order, from fases moving o slowes moving Yellow Blue Red purple Red Yellow red Brown Ba 1 Bn 2 Y 1 Y 2 Red 1 o Y 3 o Blue o Red 2 o Ba 3 Y 4 Ba 4 Ba 5 Black Mos bands clearly defined. The hird fracion conains a blue band running in fron of "5" a parial spliing ino wo red bands of "5", and anoher blue band running behind "8", no shown in Table or menioned in Tex. Bn = Y yellow mos acid and mos alkaline soluions. The supernaan became paler as he pigmen was precipiaed. The ph readings in each soluion a he end of 24 hours is shown in he Table. Those soluions which had a ph lower han 4 iniially had a greaer final ph, while above ph 4 he siuaion was reversed. TLC of he pigmens produced a each ph level is shown on he righ of Table III. The numbers used o designae pigmens are he same as in Tables I and II (naural pigmens), represening for each number in each able idenical Rf value, and color mached visually and where possible specrophoomerically. The behavior of arificial pigmens on he Biogel column was he same as he behavior of naural pigmens. Figure 1 is a phoograph of a hin layer plae on which four acidic soluions of pigmen have been developed. The L side of he plae has, in order, naural and arificial pigmens from fracion 2 of he Biogel column. The lower compac bands are blue (pigmen 7) in color and run as a single band when placed in apposiion. Yellow bands presen on he plae are no visible in he phoograph. The pigmen seen in fron of he blue band is, he excess amoun in he second sample being due o oxidaion of excess dopa on he plae. The R side of he plae has, in order, naural and arificial pigmens from o fracion 4 of he Biogel column. The lowes band is red (pigmen 8), as also is he nex and broades band (pigmen 5). Brown pigmen, as on he lef of he plae, is parly diffused and parly defined ino wo disinc bands. Despie he closeness of he bands he red and blue fracions remain clearly defined when run ogeher, while yellow and may diffuse and overlap wih oher bands. The resul shown in Figure 1 is ha obained afer a single passage of crude preparaions hrough he column increasingly refined separaion is obained by furher passages, and mos of he pigmen remains a he origin afer 2 3 passages. There is a close similariy beween Table I and he par of Table III from row 4 o row 9. Many alernaive procedures were esed as conrols o he resuls of Table III. Variaion in srengh of main consiuens was unimporan, bu variaion in proporions had an effec in lessening he efficiency of producion of pigmens. The imporance of each consiuen of he reacion mixure was esed by he use of alernaives. Tyrosine could no be subsiued for dopa, oher amino acids1 could no be subsiued for cyseine, subsances 1 The following were esed: glycine, alanine, gluarnic acid, mehionine, cysine, phenylalanine, 2-aminoyrosine, 3-aminoyrosine, N-aceyl yrosine, rypophane, 5-hydroxy rypophane, kynurefine. o o
5 TABLE III Pigmens produced from dopa cy4eine and FeC13 (M/1, M/1, M/5) mixure a various ph levels c Amoun of added.1n NaOH. ml..1 ml..2 ml..3 ml..4 ml..5 ml..6 ml..7 ml..8 ml..9 ml. 1. ml. Iiia1 ph ph in 24 hours Immediae colour change grey green yellow green yellow green yellow dark yellow green dark yellow green grey red red red red Colour 3 mins. Colour 24 hours orange yellow orange yellow orange yellow yellow green green, bik deposi green, blk deposi red, fine deposi red red cloudy red yellow bn, bn deposi pale y bn, bn deposi blue grey, blk deposi blue grey, bik deposi blue grey, bik deposi blue grey, bik deposi BnI Bn2 Yl Pigmens seen on TLC, fases moving pigmens o lef S Y2 Redi Y3 Blue Red2 Bn 3 Y4 Bn4 Bn5 Black Mos bands clearly defined. Some sreaking of pigmens. Amouns of pigmen graded o. = race deecable only afer concenraion. = no clearly idenifiable bu possibly presen. y yellow. bn =. bik = black.
6 DOPA A}D RED, BROWN AND BLACK PIGMENTS 37 LI Fic. 1. Phoograph of hin layer chromaogram of pigmens prepared by mehod described in ex. L half of figure: naural and arificial pigmens, 2nd fracion from Biogel column; R half of figure: naural and arificial pigmens, 4h fracion from Biogel column. wih reducing sulphydryl groups2 could no be subsiued for eyseine, and ferrous or cupric sals could no be subsiued for FeCI,. Specrophoomery. Figures 2(a) and 2(b) presen respecively visible and UV absorpion specra of pigmen "5" (Red 1), he principal red pigmen presen in naural maerials and synheic preparaions. Figures 3(a) and 3(b) are he curves for pigmen "7" (Blue). These curves were prepared using pigmens exraced from Rhode Island red feahers, and idenical curves were subsequenly obained using he arificially produced pigmens. For each pigmen he curves in hree soluions of differing acidiy and in one alkaline soluion are recorded. There is evidence in he curves of pigmens in acid soluion of win peaks or a peak and a shoul-. der, and he laer feaure is accenuaed in he mos acid soluions. The ideniy of shape ' following were esed: gluahione, Cleland's Reagen (dihiohreiol), hioglycollic acid, mercapoehanol. FIG. 2a. Specral absorpion curve of pigmen "5" (Red 1) in acid and alkaline soluions. 1. ion HCl; 2. N HC1; 3. O.1N HCl; 4. N NaOH. Ordinae: opical densiy. Abscissa: wavelengh in millimicrons. Fia. 2b. Specral absorpion curve of pigmen "5" (Red 1) in acid and alkaline soluions. 1. ion HCI; 2. N HCI; 3. O.1N HCl; 4. N NaOH. Ordinae: opical densiy. Abscissa: wavelengh in millimicrons. of he curves for naural and arificial pigmens in soluions of differing acidiy and alkaliniy suppors he chromaographic evidence ha hese pigmens are he same. The curves obained in he UV range have less definie maxima and minima and he absorpion in mos of he ulraviole range is greaer han in he visible range, necessiaing diluion of he pigmen soluions o obain a recording. The pigmens "5" and "7" correspond o he "red purple" and "dark purple" pigmens respecively of Smyh e al. (5). The blue color of pigmen "7" is only seen a high acidiy. Fleseh (11) publishes he curve of he "chromophore-pepide" of he red feaher pigmen. This curve does no differ subsanially from hose presened here and i is clear ha he arificial pigmens do no have a pepide componen.
7 38 THE JOURNAL OF INVESTIGATIVE DERMATOLOGY Fio. 3a. Specral absorpion curve of pigmen "7" (Blue) in acid and alkaline soluions. 1. ion HO; 2. N HO; 3. O.1N HCI; 4. N NaOH. Ordinae: opical densiy. Abscissa: wavelengh in millimicrons. FIG. 3b. Specral absorpion curve of pigmen "7" (Blue) in acid and alkaline soluions. 1. ion HC1; 2. N HO; 3. O.1N HO; 4. N NaOH. Ordinae: opical densiy. Abscissa: wavelengh in millimicrons. DTSCUSSION Geneic sudies of pigmenaion in he pas have been hampered by a lack of undersanding of he relaionship beween red, and black epidermal pigmens. Such phenomena as he abrup change from black pigmenaion o or red on an animal's coa, or of he almos infinie gradaion of color from red o black in some animal species mus be inerpreed in erms of biochemisry as well as of geneics. Wha has been described in his paper is a simple chemical procedure which leads o he producion of a series of pigmens apparenly idenical wih hose found in mammalian hair or he feahers of domesic poulry. The variaion of a single facor in he procedure allows for a qualiaive and quaniaive variaion of pigmen producs which maches ha found in hair or feahers of all colors from red o black. The variable facor in he reacion is he ph and as ye no alernaive mehod of producing he pigmenary variaion has been found. Wheher ph variaion of he degree required by his paricular model occurs physiologically is no known. I mus be expeced ha such variaion, if i occurs, will be confined o a very limied par of he mclanocye, mos likely wihin or immediaely surrounding he melanosome. I seems more likely ha he accurae duplicaion of naural producs in he model reflecs a chemical process which can be produced by some physiological means oher han ph variaion, or a leas by variaion wihin a much narrower range of ph han he required by he model. In favor of he model is he fac ha dopa, cyseinc and ferric ions are all likely o be available o he melanocye. The conversion of yrosine o dopa by yrosinase wihin melanocyes has been acceped for many years and cyseinc is a major componen of kerain. Ferric ions arc more efficien han yrosinasc in he producion of pigmen in viro and i is possible ha he main role of yrosinase in he melanocye is in producing dopa from yrosine, while oher roles a laer sages of melanogenesis are of minor imporance. The work of Proa and his colleagues (9, 16) has clarified he chemisry of he red melanie pigmens alhough here is no clear indicaion from heir work of he physiological mechanisms involved in he producion of hese pigmens. Brumbaugh (17) discusses a mechanism of variaion of pigmens produced in feaher follicles dependen on growh rae of he follicle. This mechanism mus ulimaely be relaed o a biochemical conrol sysem, and i seems possible ha he conclusion from he case which be cies is no applicable in all fields of melanogenesis. The ohromaographie mehod using TLC described in his paper combines speed wih a high degree of resoluion. The efficiency of he mehod is no apparen in sudying crude preparaions obained by he digesion of hair or feahers in concenraed acid because of sreaking by pigmens and perhaps because kerain breakdown producs affec he separaions. However, acid exracs parially purified on a Biogel column and synheic prcparaicns are separaed ino many com-
8 DOPA AND RED, BROWN AND BLACK PIGMENTS 39 ponens. The Biogel column using 4N HC1 as eluen gives greaer resoluion han sephadex bu sill no as grea as he TLC mehod. The wo mehods, Biogel and TLC, used in conjuncion, give he greaes efficiency of separaion. REFERENCES 1. Sorby, H. C.: On he colouring maers found in human hair. J. Anhropol. Ins. G. Bri., 8: 1, Bourquelo and Berrand, Cied by Munro Fox, H. and Vevers, G.: The Naure of Animal Colours. Sidgwick and Jackson, Ld., Raper, H. S.: The aerobic oxidases. Physiol. Rev., 8: 245, Flesch, P. and Rohman, S.: Isolaion of an iron pigmen from human red hair. J. Inves. Derm., 6: 257, Smyh, J. R., Porer, J. W. and Bohren, B. B.: A sudy of pigmens from red,, and buff feahers and hair. Physiol. Zool., 84: 25, Barnico, N. A.: The pigmen, richosiderin, from human red hair. Naure, 177: 528, Bold, P.: Trichosiderin, em Pigmen aus roen Haaren. Naurwissensehafen, 51: 265, Flesch, P., Esoda, E. J. and Kaz, S. A.: The iron pigmen of red hair and feahers. 3. Inves. Derm., 47: 595, Proa, G. and Nicolaus, R. A.: On he biogenesis of phaeomelanins, Advances in he Biology of Skim, Vol. VIII. The Pigmenary Sysem. Eds., Monagna, W. and Hu F., Pergamon Press, Oxford, Bold, P. and Hermsed, E.: Pyrrorichole, eine Gruppe farbiger Verbindungen aus roem Menschenhaar. Zschr. f Naurforsch., 22b: 718, Flesch, P.: The epidermal iron pigmens of red species. J. Inves. Derm., 51: 337, Cleffmann, G.: Agoui pigmen cells in siu and in viro. Ann. N. Y. Aced. Sci., 1: 749, Nicholls, E. M.: Geneic suscepibiliy in he producion of freckles, birhmarks and moles. The Lance, 7533: 71, Nicholls, E. M.: The geneics of red hair. Human Herediy,.19: 36, Nicholls, E. M.: Microspecrophoomery in he sudy of red hair. Ann. Hum. Gene., (Lond.), 38: 15, Faorusso, E., Minale, L., DeSefano, S., Cimino, G., and Nicolaus, R. A.: Sruura e biogenesi delle feomelanine. Noa V Sulla sruura della gallofeomelanina 1. Gazz. Chim. Ial., 98: 1443, Brumbaugh, J. A.: Differeniaion of black-red melanin in he fowl: Ineracion of paern genes and feaher follicle milieu. J. Exp. Zoo!., 166: 11, 1967.
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