- Email: [email protected]
The cloning and sequencing of a cDNA coding for chick tyrosinase-related protein-1
Biochimica et Biophysica Acta 1395 Ž1998. 7–12
Short sequence-paper
The cloning and sequencing of a cDNA coding for chick tyrosinase-related protein-1 C.S. April a
a,)
, I.J. Jackson b, S.H. Kidson
a
Department of Anatomy and Cell Biology, Medical School, UniÕersity of Cape Town, ObserÕatory, 7925 Cape Town, South Africa b MRC Human Genetics Unit, Western General Hospital, Crewe Road, Edinburgh EH4 2XU, UK Received 2 June 1997; accepted 31 July 1997
Abstract We have cloned a cDNA encoding an avian homologue of the mammalian brownr TYRP1 locus protein. The chick tyrosinase-related protein-1 ŽTRP-1. gene encodes a deduced protein of 535 amino acids, shares ) 65% amino acid sequence identity with fish and mammalian TRP-1 proteins, and spans 5–11 kb of the chick genome. q 1998 Elsevier Science B.V. Keywords: brown Locus; cDNA; Chick; Melanocyte library; TRP-1
In mammals, the tyrosinase-related protein Ž TRP. gene family consists of three members, all of which share significant amino acid sequence similarity, but have evolved distinct functions in the regulation of melanin synthesis w1–3x. The enzymatic functions of tyrosinase and tyrosinase-related protein-2 Ž TRP-2. have been well documented w4,5x, but the specific catalytic role of the third member, TRP-1, remains controversial w6–8x. Apart from its role in contributing towards melanin quality, the TRP-1 molecule has also been associated with certain pathological disorders. In metastatic melanoma, autologous antibodies directed against TRP-1 have been reported in the serum of patients w9x. A point mutation in the coding region of the human TRP-1 gene is responsible for one form of oculocutaneous albinism Ž OCA3. w10x. In addition, autoantibodies from vitiligous Smyth chick-
)
Corresponding author. Fax: Žq27. 21 448 7226; E-mail: [email protected]
ens have been reported to immunoprecipitate mammalian TRP-1 molecules w11x. TRP-1 cDNAs have been cloned from the human w12,13x, mouse w14x, goldfish w15x and axolotl w16x. By contrast, relatively little is known about the TRP gene family in avians w11x. Because we are interested in the genes involved in the regulation of chick melanocyte differentiation, we report here, for the first time, the cloning of a full-length chick TRP-1 cDNA. In order to isolate a full-length chick TRP-1 cDNA, we first used the polymerase chain reaction Ž PCR. to generate a partial chick TRP cDNA fragment. Using degenerate primers that were designed to amplify simultaneously all three known members of the TRP gene family, and a chick melanocyte cDNA library w17x as template DNA, we obtained a ‘‘generic’’ TRP product of 1 kb. The degenerate TRP primers used were 79 M Ž 5X GCACTCGGATr CGATr CCr AGIGAArGIINTGGCC 3X . and 80 M Ž5X CGNGGNTAICCIGTAr GTTAr GGr TCCGAGGAT 3X . w1x. We next screened 8 = 10 5 recombinants of a
0167-4781r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved. PII S 0 1 6 7 - 4 7 8 1 Ž 9 7 . 0 0 1 4 4 - 9
8
C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
chick melanocyte cDNA library w17x with this 1 kb TRP–PCR product. Of the 223 single positive plaque forming units identified, the twelve strongest hybridising ones were selected for further analysis. Five of these twelve inserts Ž1–1.7 kb. cross-hybridised to a 1.6 kb HindIII mouse TRP-1 cDNA w14x probe, and the remaining seven inserts Ž1.8–2.9 kb. cross-hybridised to a 1.75 kb EcoRI mouse TRP-2 cDNA w18x probe on Southern blots Ž results not shown. . Because the partial restriction maps of the five TRP-1 crosshybridising inserts were similar, the longest of these clones, pcTRP-1.6, was selected for further analysis. The nucleotide sequence of the chick TRP-1 ŽcTRP-1. cDNA carried by pcTRP-1.6 was obtained manually using vector, degenerate TRP w1x and custom-designed internal primers. DNA and deduced amino acid sequence analyses were performed using the Genetics Computer Group ŽGCG. program ŽGCG sequence analysis software package, GCG, Madison, WI. and GenBank and EMBL databases. Chick TRP-1 consists of 1771 bp, with 65 bp of 5X untranslated sequence Ž Fig. 1.. The longest open reading frame of 1605 nucleotides begins with the vertebrate translation initiation consensus sequence ArGNCAUG w19x at nucleotide position 66 and ends with a TGA termination codon Ž nucleotides 1671– 1673.. There is a 3X untranslated region of 101 bp, containing a putative polyadenylation signal ŽAATAAA. at nucleotide positions 1752–1757. Chick TRP-1 shows 70.1%, 68.8% and 60.8% nucleotide sequence homology with the human w12x, mouse w14x, and goldfish w15x TRP-1 cDNA sequences respectively. Chick TRP-1 encodes a deduced polypeptide of 535 amino acids with a predicted molecular weight of 60.6 kDa. A signal sequence of 23 amino acid residues, consisting of a hydrophobic core and terminating in alanine w20x, is present at the amino Ž N. terminus. Thus, the predicted mature protein is composed of 512 amino acids with a molecular weight of
9
58 kDa. There are six potential N-glycosylation sites ŽNXTrS. w21x and a possible transmembrane domain near the carboxy ŽC.-terminus. An amino acid alignment of the predicted cTRP-1 protein with other published, full-length TRP-1 proteins ŽFig. 2. was generated using the Pileup GCG command. Chick cTRP-1 encodes a protein of 535 amino acids, whilst the human w12x, mouse w14x and goldfish w15x predicted TRP-1 protein lengths are 527, 537 and 522 amino acids respectively. In addition, cTRP-1 shows 76.2%, 72.8% and 67.6% amino acid sequence identity and 86.1%, 84.5% and 78.6% similarity with the human, mouse and goldfish TRP-1 proteins respectively. From the deduced amino acid sequences in Fig. 2, three conserved protein domains were identified by the Swiss-Prot and Prosite databases. Two of these consensus protein patterns Ž H X 4F Ž L,I,V ,M ,T . X W H RX 2 Ž L,M . X 3E . and ŽDPXFŽL,I,V,M,F,Y,W .X2HX3D. are restricted to members of the TRP gene family and some invertebrate hemocyanins w22x. It is thought that these two histidine-containing motifs bind copper, thus facilitating mono-oxygenase activity w22,3x. The third conserved region is a cysteine-rich ‘‘EGF-like’’ domain ŽCXCX5GX2C. that has been found in several membrane-bound and secreted proteins. This domain is present in all members of the TRP gene family and it has been suggested that this domain may be involved in protein-protein interactions w1x. An additional motif, EXXQPLL, termed the C-terminal consensus sequence Ž CTCS. , has recently been suggested to participate in targeting tyrosinase and TRP-1 to the premelanosome w15,23x. This CTCS is also present in cTRP-1 and previously reported chick tyrosinase cDNA clones w24,17x. Certain mouse brown (b) and human TYRP1 mutant alleles are responsible for the dilution of a black to brown coat colour w25x and OCA3 w10x, respectively. Unlike Black Australorp ŽBA. chicks, which have a black plumage, White Plymouth Rock = Pile
Fig. 1. Nucleotide and deduced amino acid sequence of the pcTRP-1.6 cDNA insert, encoding chick tyrosinase-related protein-1. A putative 23 amino acid residue leader sequence, six N-linked glycosylation sites, a C-terminal hydrophobic membrane-spanning domain, and a polyadenylation signal are all underlined. Asterisks indicate a stop codon. The nucleotide sequence shown here has been deposited in the GenBank database and assigned the accession number AF003631.
10
C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
11
we performed Southern blot analysis using the entire 1.7 kb cTRP-1 cDNA as a probe, on genomic DNA from both BA and WPR = PG fowl breeds. Digestion with DraI, EcoRI, KpnI, PÕuII and XhoI revealed three Ž2.5, 2.1 and 1.2 kb. , three Ž5, 2.6 and 2.2 kb., two Ž6 and 5 kb., two Ž6 and 1.9 kb. and one Ž8 kb. strongly-hybridising bands respectively ŽFig. 3.. Because there are no KpnI, PÕuII and XhoI sites and one EcoRI and two DraI sites in the cTRP-1 cDNA, these results suggest that the chick TRP-1 gene has several introns and may span 5–11 kb. A comparison of the Southern blot analyses of BA and WPR = PG genomic DNA revealed no gross differences Ždeletions or rearrangements. at the chick b r TYRP1 locus. Taken together, these results describe the first molecular cloning of a complete TRP-1 cDNA in an avian species. We are currently sequencing a chick TRP-2 cDNA, which will enable us to further investigate both the developmental expression patterns and evolution of the chick TRP gene family. Thanks to Henry Fortuin for photography and all our colleagues for helpful discussions. This work was supported by Development and Mellon Travel Fellowships ŽCSA. and bursaries from UCT ŽCSA., the United Kingdom MRC ŽIJJ. and grants from South African MRC and UCT Ž SHK. . Fig. 3. Southern blot analysis of the brownr TYRP1 locus in Black Australorp and White Plymouth Rock = Pile Game chicks. Genomic DNA Ž20 mg. prepared from BA ŽB. and WPR = PG ŽW. chick embryos was digested with DraI, EcoRI, KpnI, PÕuII and XhoI and subjected to Southern blot hybridisation w17x using a 1.7 kb cTRP-1 w a-32 PxdCTP random-primed probe. The molecular weight Žkb. marker is l r HindIII.
Game ŽWPR = PG. chicks exhibit a white plumage because of the influence of the dominant white (I) locus w26x. In addition, WPR = PG chicks are homozygous for recessiÕe white at the colour (c) locus w26x. To determine whether there are any large alterations at the b r TYRP1 locus in WPR = PG fowls,
References w1x I.J. Jackson, P. Budd, J.M. Horn, R. Johnson, S. Raymond, K. Steel, Pigment Cell Res. 7 Ž1994. 73–80. w2x I.J. Jackson, Pigment Cell Res. 7 Ž1994. 241–242. w3x R. Morrison, K. Mason, S. Frost-Mason, Pigment Cell Res. 7 Ž1994. 388–393. w4x A. Korner, J. Pawelek, Science 217 Ž1982. 1163–1165. ¨ w5x K. Tsukamoto, I.J. Jackson, K. Urabe, P.M. Montague, V.J. Hearing, EMBO J. 11 Ž1992. 519–526. w6x H. Zhao, Y. Zhao, J.J. Nordlund, R.E. Boissy, Pigment Cell Res. 7 Ž1994. 131–140. w7x T. Kobayashi, K. Urabe, A. Winder, K. Tsukamoto, T. Brewington, G. Imokawa, B. Potterf, V.J. Hearing, Pigment Cell Res. 7 Ž1994. 227–234.
Fig. 2. Amino acid alignment of TRP-1 proteins from human ŽHtrp1. w12x, mouse ŽMtrp1. w14x, chick ŽChtrp1. and goldfish ŽGftrp1. w15x. The protein sequences are represented in one-letter code. Dots Ž... have been introduced for optimal alignment. An N-terminal EGF-like domain, two copper-binding domains, and a C-terminal consensus sequence are all underlined.
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C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
w8x A.J. Winder, A. Wittbjer, G. Odh, E. Rosengren, H. Rorsman, Pigment Cell Res. 7 Ž1994. 305–310. w9x S. Vijayasaradhi, B. Bouchard, A.N. Houghton, J. Exp. Med. 171 Ž1990. 1375–1380. w10x R.E. Boissy, H. Zhao, W.S. Oetting, L.M. Austin, S.C. Wildenberg, Y.L. Boissy, Y. Zhao, R.A. Sturm, V.J. Hearing, R.A. King, J.J. Nordlund, Am. J. Hum. Genet. 58 Ž1996. 1145–1156. w11x L.M. Austin, R.E. Boissy, Am. J. Pathol. 146 Ž1995. 1529– 1541. w12x T. Cohen, R.M. Muller, Y. Tomita, S. Shibahara, Nucleic Acids Res. 18 Ž1990. 2807–2808. w13x C.D. Chintamaneni, M. Ramsay, M.-A. Colman, M.F. Fox, R.T. Pickard, B.S. Kwon, Biochem. Biophys. Res. Commun. 178 Ž1991. 227–235. w14x S. Shibahara, Y. Tomita, T. Sakakura, C. Nager, B. Chaudhuri, R. Muller, Nucleic Acids Res. 14 Ž1986. 2413–2427. ¨ w15x G. Peng, J.D. Taylor, T.T. Tchen, Pigment Cell Res. 7 Ž1994. 9–16. w16x K.A. Mason, S.K. Mason, Pigment Cell Res. 8 Ž1995. 46–52.
w17x C.S. April, T. Franz, S.H. Kidson, Exp. Cell Res. 224 Ž1996. 372–378. w18x I.J. Jackson, D.M. Chambers, K. Tsukamoto, N.G. Copeland, D.J. Gilbert, N.A. Jenkins, V. Hearing, EMBO J. 11 Ž1992. 527–535. w19x D.R. Cavener, S.C. Ray, Nucleic Acids Res. 19 Ž1991. 3185–3192. w20x G. von Heijne, Eur. J. Biochem. 133 Ž1983. 17–21. w21x E. Bause, Biochem. J. 209 Ž1983. 331–336. w22x K. Lerch, in: J.T. Bagnara, ŽEd.., Advances in Pigment Cell Research, Alan R. Liss, New York, 1988, pp. 85–98. w23x F. Beermann, S.J. Orlow, R.E. Boissy, A. Schmidt, Y.L. Boissy, M.L. Lamoreux, Exp. Eye Res. 61 Ž1995. 599–607. w24x M. Mochii, A. Iio, H. Yamamoto, T. Takeuchi, G. Eguchi, Pigment Cell Res. 5 Ž1992. 162–167. w25x E. Zdarsky, J. Favor, I.J. Jackson, Genetics 126 Ž1990. 443–449. w26x J.R. Smyth, in: R.D. Crawford ŽEd.., Poultry Breeding and Genetics, Elsevier, New York, 1990, pp. 109–167.
Short sequence-paper
The cloning and sequencing of a cDNA coding for chick tyrosinase-related protein-1 C.S. April a
a,)
, I.J. Jackson b, S.H. Kidson
a
Department of Anatomy and Cell Biology, Medical School, UniÕersity of Cape Town, ObserÕatory, 7925 Cape Town, South Africa b MRC Human Genetics Unit, Western General Hospital, Crewe Road, Edinburgh EH4 2XU, UK Received 2 June 1997; accepted 31 July 1997
Abstract We have cloned a cDNA encoding an avian homologue of the mammalian brownr TYRP1 locus protein. The chick tyrosinase-related protein-1 ŽTRP-1. gene encodes a deduced protein of 535 amino acids, shares ) 65% amino acid sequence identity with fish and mammalian TRP-1 proteins, and spans 5–11 kb of the chick genome. q 1998 Elsevier Science B.V. Keywords: brown Locus; cDNA; Chick; Melanocyte library; TRP-1
In mammals, the tyrosinase-related protein Ž TRP. gene family consists of three members, all of which share significant amino acid sequence similarity, but have evolved distinct functions in the regulation of melanin synthesis w1–3x. The enzymatic functions of tyrosinase and tyrosinase-related protein-2 Ž TRP-2. have been well documented w4,5x, but the specific catalytic role of the third member, TRP-1, remains controversial w6–8x. Apart from its role in contributing towards melanin quality, the TRP-1 molecule has also been associated with certain pathological disorders. In metastatic melanoma, autologous antibodies directed against TRP-1 have been reported in the serum of patients w9x. A point mutation in the coding region of the human TRP-1 gene is responsible for one form of oculocutaneous albinism Ž OCA3. w10x. In addition, autoantibodies from vitiligous Smyth chick-
)
Corresponding author. Fax: Žq27. 21 448 7226; E-mail: [email protected]
ens have been reported to immunoprecipitate mammalian TRP-1 molecules w11x. TRP-1 cDNAs have been cloned from the human w12,13x, mouse w14x, goldfish w15x and axolotl w16x. By contrast, relatively little is known about the TRP gene family in avians w11x. Because we are interested in the genes involved in the regulation of chick melanocyte differentiation, we report here, for the first time, the cloning of a full-length chick TRP-1 cDNA. In order to isolate a full-length chick TRP-1 cDNA, we first used the polymerase chain reaction Ž PCR. to generate a partial chick TRP cDNA fragment. Using degenerate primers that were designed to amplify simultaneously all three known members of the TRP gene family, and a chick melanocyte cDNA library w17x as template DNA, we obtained a ‘‘generic’’ TRP product of 1 kb. The degenerate TRP primers used were 79 M Ž 5X GCACTCGGATr CGATr CCr AGIGAArGIINTGGCC 3X . and 80 M Ž5X CGNGGNTAICCIGTAr GTTAr GGr TCCGAGGAT 3X . w1x. We next screened 8 = 10 5 recombinants of a
0167-4781r98r$19.00 q 1998 Elsevier Science B.V. All rights reserved. PII S 0 1 6 7 - 4 7 8 1 Ž 9 7 . 0 0 1 4 4 - 9
8
C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
chick melanocyte cDNA library w17x with this 1 kb TRP–PCR product. Of the 223 single positive plaque forming units identified, the twelve strongest hybridising ones were selected for further analysis. Five of these twelve inserts Ž1–1.7 kb. cross-hybridised to a 1.6 kb HindIII mouse TRP-1 cDNA w14x probe, and the remaining seven inserts Ž1.8–2.9 kb. cross-hybridised to a 1.75 kb EcoRI mouse TRP-2 cDNA w18x probe on Southern blots Ž results not shown. . Because the partial restriction maps of the five TRP-1 crosshybridising inserts were similar, the longest of these clones, pcTRP-1.6, was selected for further analysis. The nucleotide sequence of the chick TRP-1 ŽcTRP-1. cDNA carried by pcTRP-1.6 was obtained manually using vector, degenerate TRP w1x and custom-designed internal primers. DNA and deduced amino acid sequence analyses were performed using the Genetics Computer Group ŽGCG. program ŽGCG sequence analysis software package, GCG, Madison, WI. and GenBank and EMBL databases. Chick TRP-1 consists of 1771 bp, with 65 bp of 5X untranslated sequence Ž Fig. 1.. The longest open reading frame of 1605 nucleotides begins with the vertebrate translation initiation consensus sequence ArGNCAUG w19x at nucleotide position 66 and ends with a TGA termination codon Ž nucleotides 1671– 1673.. There is a 3X untranslated region of 101 bp, containing a putative polyadenylation signal ŽAATAAA. at nucleotide positions 1752–1757. Chick TRP-1 shows 70.1%, 68.8% and 60.8% nucleotide sequence homology with the human w12x, mouse w14x, and goldfish w15x TRP-1 cDNA sequences respectively. Chick TRP-1 encodes a deduced polypeptide of 535 amino acids with a predicted molecular weight of 60.6 kDa. A signal sequence of 23 amino acid residues, consisting of a hydrophobic core and terminating in alanine w20x, is present at the amino Ž N. terminus. Thus, the predicted mature protein is composed of 512 amino acids with a molecular weight of
9
58 kDa. There are six potential N-glycosylation sites ŽNXTrS. w21x and a possible transmembrane domain near the carboxy ŽC.-terminus. An amino acid alignment of the predicted cTRP-1 protein with other published, full-length TRP-1 proteins ŽFig. 2. was generated using the Pileup GCG command. Chick cTRP-1 encodes a protein of 535 amino acids, whilst the human w12x, mouse w14x and goldfish w15x predicted TRP-1 protein lengths are 527, 537 and 522 amino acids respectively. In addition, cTRP-1 shows 76.2%, 72.8% and 67.6% amino acid sequence identity and 86.1%, 84.5% and 78.6% similarity with the human, mouse and goldfish TRP-1 proteins respectively. From the deduced amino acid sequences in Fig. 2, three conserved protein domains were identified by the Swiss-Prot and Prosite databases. Two of these consensus protein patterns Ž H X 4F Ž L,I,V ,M ,T . X W H RX 2 Ž L,M . X 3E . and ŽDPXFŽL,I,V,M,F,Y,W .X2HX3D. are restricted to members of the TRP gene family and some invertebrate hemocyanins w22x. It is thought that these two histidine-containing motifs bind copper, thus facilitating mono-oxygenase activity w22,3x. The third conserved region is a cysteine-rich ‘‘EGF-like’’ domain ŽCXCX5GX2C. that has been found in several membrane-bound and secreted proteins. This domain is present in all members of the TRP gene family and it has been suggested that this domain may be involved in protein-protein interactions w1x. An additional motif, EXXQPLL, termed the C-terminal consensus sequence Ž CTCS. , has recently been suggested to participate in targeting tyrosinase and TRP-1 to the premelanosome w15,23x. This CTCS is also present in cTRP-1 and previously reported chick tyrosinase cDNA clones w24,17x. Certain mouse brown (b) and human TYRP1 mutant alleles are responsible for the dilution of a black to brown coat colour w25x and OCA3 w10x, respectively. Unlike Black Australorp ŽBA. chicks, which have a black plumage, White Plymouth Rock = Pile
Fig. 1. Nucleotide and deduced amino acid sequence of the pcTRP-1.6 cDNA insert, encoding chick tyrosinase-related protein-1. A putative 23 amino acid residue leader sequence, six N-linked glycosylation sites, a C-terminal hydrophobic membrane-spanning domain, and a polyadenylation signal are all underlined. Asterisks indicate a stop codon. The nucleotide sequence shown here has been deposited in the GenBank database and assigned the accession number AF003631.
10
C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
11
we performed Southern blot analysis using the entire 1.7 kb cTRP-1 cDNA as a probe, on genomic DNA from both BA and WPR = PG fowl breeds. Digestion with DraI, EcoRI, KpnI, PÕuII and XhoI revealed three Ž2.5, 2.1 and 1.2 kb. , three Ž5, 2.6 and 2.2 kb., two Ž6 and 5 kb., two Ž6 and 1.9 kb. and one Ž8 kb. strongly-hybridising bands respectively ŽFig. 3.. Because there are no KpnI, PÕuII and XhoI sites and one EcoRI and two DraI sites in the cTRP-1 cDNA, these results suggest that the chick TRP-1 gene has several introns and may span 5–11 kb. A comparison of the Southern blot analyses of BA and WPR = PG genomic DNA revealed no gross differences Ždeletions or rearrangements. at the chick b r TYRP1 locus. Taken together, these results describe the first molecular cloning of a complete TRP-1 cDNA in an avian species. We are currently sequencing a chick TRP-2 cDNA, which will enable us to further investigate both the developmental expression patterns and evolution of the chick TRP gene family. Thanks to Henry Fortuin for photography and all our colleagues for helpful discussions. This work was supported by Development and Mellon Travel Fellowships ŽCSA. and bursaries from UCT ŽCSA., the United Kingdom MRC ŽIJJ. and grants from South African MRC and UCT Ž SHK. . Fig. 3. Southern blot analysis of the brownr TYRP1 locus in Black Australorp and White Plymouth Rock = Pile Game chicks. Genomic DNA Ž20 mg. prepared from BA ŽB. and WPR = PG ŽW. chick embryos was digested with DraI, EcoRI, KpnI, PÕuII and XhoI and subjected to Southern blot hybridisation w17x using a 1.7 kb cTRP-1 w a-32 PxdCTP random-primed probe. The molecular weight Žkb. marker is l r HindIII.
Game ŽWPR = PG. chicks exhibit a white plumage because of the influence of the dominant white (I) locus w26x. In addition, WPR = PG chicks are homozygous for recessiÕe white at the colour (c) locus w26x. To determine whether there are any large alterations at the b r TYRP1 locus in WPR = PG fowls,
References w1x I.J. Jackson, P. Budd, J.M. Horn, R. Johnson, S. Raymond, K. Steel, Pigment Cell Res. 7 Ž1994. 73–80. w2x I.J. Jackson, Pigment Cell Res. 7 Ž1994. 241–242. w3x R. Morrison, K. Mason, S. Frost-Mason, Pigment Cell Res. 7 Ž1994. 388–393. w4x A. Korner, J. Pawelek, Science 217 Ž1982. 1163–1165. ¨ w5x K. Tsukamoto, I.J. Jackson, K. Urabe, P.M. Montague, V.J. Hearing, EMBO J. 11 Ž1992. 519–526. w6x H. Zhao, Y. Zhao, J.J. Nordlund, R.E. Boissy, Pigment Cell Res. 7 Ž1994. 131–140. w7x T. Kobayashi, K. Urabe, A. Winder, K. Tsukamoto, T. Brewington, G. Imokawa, B. Potterf, V.J. Hearing, Pigment Cell Res. 7 Ž1994. 227–234.
Fig. 2. Amino acid alignment of TRP-1 proteins from human ŽHtrp1. w12x, mouse ŽMtrp1. w14x, chick ŽChtrp1. and goldfish ŽGftrp1. w15x. The protein sequences are represented in one-letter code. Dots Ž... have been introduced for optimal alignment. An N-terminal EGF-like domain, two copper-binding domains, and a C-terminal consensus sequence are all underlined.
12
C.S. April et al.r Biochimica et Biophysica Acta 1395 (1998) 7–12
w8x A.J. Winder, A. Wittbjer, G. Odh, E. Rosengren, H. Rorsman, Pigment Cell Res. 7 Ž1994. 305–310. w9x S. Vijayasaradhi, B. Bouchard, A.N. Houghton, J. Exp. Med. 171 Ž1990. 1375–1380. w10x R.E. Boissy, H. Zhao, W.S. Oetting, L.M. Austin, S.C. Wildenberg, Y.L. Boissy, Y. Zhao, R.A. Sturm, V.J. Hearing, R.A. King, J.J. Nordlund, Am. J. Hum. Genet. 58 Ž1996. 1145–1156. w11x L.M. Austin, R.E. Boissy, Am. J. Pathol. 146 Ž1995. 1529– 1541. w12x T. Cohen, R.M. Muller, Y. Tomita, S. Shibahara, Nucleic Acids Res. 18 Ž1990. 2807–2808. w13x C.D. Chintamaneni, M. Ramsay, M.-A. Colman, M.F. Fox, R.T. Pickard, B.S. Kwon, Biochem. Biophys. Res. Commun. 178 Ž1991. 227–235. w14x S. Shibahara, Y. Tomita, T. Sakakura, C. Nager, B. Chaudhuri, R. Muller, Nucleic Acids Res. 14 Ž1986. 2413–2427. ¨ w15x G. Peng, J.D. Taylor, T.T. Tchen, Pigment Cell Res. 7 Ž1994. 9–16. w16x K.A. Mason, S.K. Mason, Pigment Cell Res. 8 Ž1995. 46–52.
w17x C.S. April, T. Franz, S.H. Kidson, Exp. Cell Res. 224 Ž1996. 372–378. w18x I.J. Jackson, D.M. Chambers, K. Tsukamoto, N.G. Copeland, D.J. Gilbert, N.A. Jenkins, V. Hearing, EMBO J. 11 Ž1992. 527–535. w19x D.R. Cavener, S.C. Ray, Nucleic Acids Res. 19 Ž1991. 3185–3192. w20x G. von Heijne, Eur. J. Biochem. 133 Ž1983. 17–21. w21x E. Bause, Biochem. J. 209 Ž1983. 331–336. w22x K. Lerch, in: J.T. Bagnara, ŽEd.., Advances in Pigment Cell Research, Alan R. Liss, New York, 1988, pp. 85–98. w23x F. Beermann, S.J. Orlow, R.E. Boissy, A. Schmidt, Y.L. Boissy, M.L. Lamoreux, Exp. Eye Res. 61 Ž1995. 599–607. w24x M. Mochii, A. Iio, H. Yamamoto, T. Takeuchi, G. Eguchi, Pigment Cell Res. 5 Ž1992. 162–167. w25x E. Zdarsky, J. Favor, I.J. Jackson, Genetics 126 Ž1990. 443–449. w26x J.R. Smyth, in: R.D. Crawford ŽEd.., Poultry Breeding and Genetics, Elsevier, New York, 1990, pp. 109–167.