Molecular Basis for the Heterogeneity of Human Tyrosinase

SHIGEKI SHIBAHARA; YASUSHI TOMITA; HACHIRO TAGAMI; RITA M. MÜLLER; TIRZA COHEN

doi:10.1620/tjem.156.403

SHIGEKI SHIBAHARA, YASUSHI TOMITA, HACHIRO TAGAMI, RITA M. MÜLLER, TIRZA COHEN

Author information

Keywords: tyrosinase, melanin pigment, cDNA, gene, alternative splicing

JOURNAL FREE ACCESS

1988 Volume 156 Issue 4 Pages 403-414

DOI https://doi.org/10.1620/tjem.156.403

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Published: 1988 Received: November 10, 1988 Available on J-STAGE: August 31, 2006 Accepted: November 21, 1988 Advance online publication: - Revised: -
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Date of correction: August 31, 2006 Reason for correction: - Correction: ABSTRACT Details: Wrong : SHIBAHARA, S., TOMITA, Y., TAGAMI, H., MÜLLER, R.M. and COHEN, T. Molecular Basis for the Heterogeneity of Human Tyrosinase. Tohoku J. exp. Med., 1988, 156 (4), 403-414-A cDNA clone, pHT_γ1, representing human tyrosinase mRNA was isolated by screening a melanoma cDNA library with a synthetic oligoriucleotide complementary to a segment of the human tyrosinase cDNA, Pmel 34 [Kwon et al. (1987) Proc. nat. Acad. Sci. USA 84, 7473-7477]. However, there are a number of differences in the nucleotide sequence between two cDNAs, pHT_γ1 and Pmel 34, particularly in the region coding for the carboxyl terminus of the enzyme (putative exon 5). We therefore cloned the genomic DNA segment carrying the exon 5 of the human tyrosinase gene by screening a human placental genomic DNA library with a cloned cDNA probe. The nucleotide sequences of human tyrosinase cDNA as well as a part of its gene were determined. Mature human tyrosinase is composed of 511 amino acids with a molecular weight of 58, 000. We provide evidence for the presence of at least two species of human tyrosinase mRNA generated by alternative splicing in human pigmented melanoma cells.
Right : A cDNA clone, pHTγ1, representing human tyrosinase mRNA was isolated by screening a melanoma cDNA library with a synthetic oligonucleotide complementary to a segment of the human tyrosinase cDNA, Pmel 34 [Kwon et al. (1987) Proc. nat. Acad. Sci. USA 84, 7473-7477]. However, there are a number of differences in the nucleotide sequence between two cDNAs, pHTγ1 and Pmel 34, particularly in the region coding for the carboxyl terminus of the enzyme (putative exon 5). We therefore cloned the genomic DNA segment carrying the exon 5 of the human tyrosinase gene by screening a human placental genomic DNA library with a cloned cDNA probe. The nucleotide sequences of human tyrosinase cDNA as well as a part of its gene were determined. Mature human tyrosinase is composed of 511 amino acids with a molecular weight of 58, 000. We provide evidence for the presence of at least two species of human tyrosinase mRNA generated by alternative splicing in human pigmented melanoma cells.

Date of correction: August 31, 2006 Reason for correction: - Correction: AFFILIATION Details: Wrong :
1) Friedrich Miescher-Institut
2) Department of Applied Physiology, Tohoku University School of Medicine
3) Department of Dermatology, Tohoku University School of Medicine
4) Department of Human Genetics, Hadassah University Hospital

Right :
1) Friedrich Miescher-Institute
2) Department of Applied Physiology, Tohoku University School of Medicine
3) Department of Dermatology, Tohoku University School of Medicine
4) Department of Human Genetics, Hadassah University Hospital

Date of correction: August 31, 2006 Reason for correction: - Correction: CITATION Details: Wrong : 1) Aviv, H.T. & Leder, P. (1972) Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc. nat. Acad. Sci. USA, 69, 1408-1412.
2) Bause, E. (1983) Structural requirements of N-glycosylation of proteins. Biochem. J., 209, 331-336.
3) Brüggen, J., Macher, E. & Sorg, C. (1981) Expression of surface antigens and its relation to parameters of malignancy in human malignant melanoma. Cancer Immunol. Immunother., 10, 121-127.
4) Burnet, J.B., Seiler, H. & Brown, I.V. (1967) Separation and characterization of multiple forms of tyrosinase from mouse melanoma. Cancer Res., 27, 880-889.
5) Feinberg, A.P. & Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem., 132, 6-13.
6) Hearing, V. J., Ekel, T.M. & Montague, P.M. (1981) Mammalian tyrosinase: Isozymic forms of the enzyme. Int. J. Biochem., 13, 99-103.
7) Kwon, B.S., Haq, A.K., Pomerantz, S.H. & Halaban, R. (1987) Isolation and sequence of a c DNA clone for human tyrosinase that maps at the mouse c-albino locus. Proc, nat. Acad. Sci. USA, 84, 7473-7477.
8) Kwon, B.S., Wakulchik, M., Haq, A. K., Halaban, R. & Kestler, D. (1988) Sequence analysis of mouse tyrosinase cDNA and the effect of melanotropin on its gene expression. Biochem. biophys. Res. Commun., 153, 1301-1309.
9) Lerch, K. (1988) Protein and active-site structure of tyrosinase. In: Advances in Pigment Cell Research, edited by J.T. Bagnara, Alan R. Liss, New York, pp. 85-98.
10) Lerner, A.B., Fitzpatrick, T.B., Calkins, E. & Summerson, W.H. (1950) Mammalian tyrosinase: The relationship of copper to enzymic activity. J. biol. Chem., 187, 793-802.
11) Marshall, R.D. (1974) The nature and metabolism of the carbohydrate-peptide linkages of glycoproteins. Biochem. Soc. Symp., 40, 17-26.
12) Maxam, A.M. & Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Meth. Enzymol., 65, 499-560.
13) Müller, G., Ruppert, S., Schmid, E. & Schutz, G. (1988) Functional analysis of alternatively spliced tyrosinase gene transcripts. EMBO J., 7, 2723-2730.
14) Müller, R. M., Taguchi, H. & Shibahara, S. (1987) Nucleotide sequence and organization of the rat heme oxygenasegene. J. biol. Chem., 262, 6795-6802.
15) Nishioka, K. (1978) Particulate tyrosinase of human malignant melanoma. Europ. J. Biochem., 85, 137-146.
16) Ohkura, T., Yamashita, K., Mishima, Y. & Kobata, A. (1984) Purification of hamster melanoma tyrosinase and structural studies of their asparagine-linked sugar chains. Arch. Biochem. byophys., 235, 63-77.
17) Okayama, H. & Berg, P. (1982) High-efficiency cloning of full-length cDNA. Molec. cell. Biol., 2, 161-170.
18) Pomerantz, S.H. (1966) The tyrosine hydroxylase activity of mammalian tyrosinase. J. biol. Chem., 241, 161-168.
19) Pomerantz, S.H. & Li, J. P-C. (1973) Purification and properties of tyrosinase isoenzymes from hamster melanoma. Yale J. biol. Med., 46, 541-552.
20) Ruppert, S., Müller, G., Kwon, B. & Schutz, G. (1988) Multiple transcripts of the mouse tyrosinase gene are generated by alternative splicing. EMBO J., 7, 2715-2722.
21) Shibahara, S., Tomita, Y., Sakakura, T., Nager, C., Chaudhuri, B. & Müller, R. (1986) Cloning and expression of cDNA encoding mouse tyrosinase. Nucleic Acids Res., 14, 2413-2427.
22) Shimao, K. (1962) Partial purification and kinetic studies of mammalian tyrosinase. Biochim. biophys. Acta (Amst.), 62, 205-215.
23) Yamamoto, H., Takeuchi, S., Kudo, T., Makino, K., Nakata, A., Shinoda, T. & Takeuchi, T. (1987) Cloning and sequencing of mouse tyrosinase cDNA. Jap. J. Genet., 62, 271-274.

Right : 1) Aviv, H. T. & Leder, P. (1972) Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc. nat. Acad. Sci. USA, 69, 1408-1412.
2) Bause, E. (1983) Structural requirements of N-glycosylation of proteins. Biochem. J., 209, 331-336.
3) Brüggen, J., Macher, E. & Sorg, C. (1981) Expression of surface antigens and its relation to parameters of malignancy in human malignant melanoma. Cancer Immunol. Immunother., 10, 121-127.
4) Burnet, J. B., Seiler, H. & Brown, I. V. (1967) Separation and characterization of multiple forms of tyrosinase from mouse melanoma. Cancer Res., 27, 880-889.
5) Feinberg, A. P. & Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem., 132, 6-13.
6) Hearing, V. J., Ekel, T. M. & Montague, P. M. (1981) Mammalian tyrosinase: Isozymic forms of the enzyme. Int. J. Biochem., 13, 99-103.
7) Kwon, B. S., Haq, A. K., Pomerantz, S. H. & Halaban, R. (1987) Isolation and sequence of a c DNA clone for human tyrosinase that maps at the mouse c-albino locus. Proc. nat. Acad. Sci. USA, 84, 7473-7477.
8) Kwon, B. S., Wakulchik, M., Haq, A. K., Halaban, R. & Kestler, D. (1988) Sequence analysis of mouse tyrosinase cDNA and the effect of melanotropin on its gene expression. Biochem. biophys. Res. Commun., 153, 1301-1309.
9) Lerch, K. (1988) Protein and active-site structure of tyrosinase. In: Advances in Pigment Cell Research, edited by J. T. Bagnara, Alan R. Liss, New York, pp. 85-98.
10) Lerner, A. B., Fitzpatrick, T. B., Calkins, E. & Summerson, W. H. (1950) Mammalian tyrosinase: The relationship of copper to enzymic activity. J. biol. Chema., 187, 793-802.
11) Marshall, R. D. (1974) The nature and metabolism of the carbohydrate-peptide linkages of glycoproteins. Biochem. Soc. Symp., 40, 17-26.
12) Maxam, A. M. & Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Meth. Enzymol., 65, 499-560.
13) Müller, G., Ruppert, S., Schmid, E. & Schutz, G. (1988) Functional analysis of alternatively spliced tyrosinase gene transcripts. EMBO J., 7, 2723-2730.
14) Müller, R. M., Taguchi, H. & Shibahara, S. (1987) Nucleotide sequence and organization of the rat heme oxygenasegene. J. biol. Chem., 262, 6795-6802.
15) Nishioka, K. (1978) Particulate tyrosinase of human malignant melanoma. Europ. J. Biochem., 85, 137-146.
16) Ohkura, T., Yamashita, K., Mishima, Y. & Kobata, A. (1984) Purification of hamster melanoma tyrosinase and structural studies of their asparagine-linked sugar chains. Arch. Biochem. byophys., 235, 63-77.
17) Okayama, H. & Berg, P. (1982) High-efficiency cloning of full-length cDNA. Molec. cell. Biol., 2, 161-170.
18) Pomerantz, S. H. (1966) The tyrosine hydroxylase activity of mammalian tyrosinase. J. biol. Chem., 241, 161-168.
19) Pomerantz, S. H. & Li, J. P-C. (1973) Purification and properties of tyrosinase isoenzymes from hamster melanoma. Yale J. biol. Med., 46, 541-552.
20) Ruppert, S., Müller, G., Kwon, B. & Schutz, G. (1988) Multiple transcripts of the mouse tyrosinase gene are generated by alternative splicing. EMBO J., 7, 2715-2722.
21) Shibahara, S., Tomita, Y., Sakakura, T., Nager, C., Chaudhuri, B. & Müller, R. (1986) Cloning and expression of cDNA encoding mouse tyrosinase. Nucleic Acids Res., 14, 2413-2427.
22) Shimao, K. (1962) Partial purification and kinetic studies of mammalian tyrosinase. Biochim. biophys. Acta (Amst.), 62, 205-215.
23) Yamamoto, H., Takeuchi, S., Kudo, T., Makino, K., Nakata, A., Shinoda, T. & Takeuchi, T. (1987) Cloning and sequencing of mouse tyrosinase cDNA. Jap. J. Genet., 62, 271-274.

Date of correction: August 31, 2006 Reason for correction: - Correction: PDF FILE Details: -

Date of correction: August 31, 2006 Reason for correction: - Correction: AUTHOR Details: Wrong : SHIGEKI SHIBAHARA¹⁾²⁾, YASUSHI TOMITA³⁾, HACHIRO TAGAMI³⁾, RITA M. MÜLLER¹⁾, TIRZA COHEN⁴⁾
Right : SHIGEKI SHIBAHARA¹⁾²⁾, YASUSHI TOMITA³⁾, HACHIRO TAGAMI³⁾, RITA M. MÜLLER¹⁾, TIRZA COHEN¹⁾⁴⁾

Date of correction: August 31, 2006 Reason for correction: - Correction: CITATION Details: Wrong : 1) Aviv, H. T. & Leder, P. (1972) Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc. nat. Acad. Sci. USA, 69, 1408-1412.
2) Bause, E. (1983) Structural requirements of N-glycosylation of proteins. Biochem. J., 209, 331-336.
3) Brüggen, J., Macher, E. & Sorg, C. (1981) Expression of surface antigens and its relation to parameters of malignancy in human malignant melanoma. Cancer Immunol. Immunother., 10, 121-127.
4) Burnet, J. B., Seiler, H. & Brown, I. V. (1967) Separation and characterization of multiple forms of tyrosinase from mouse melanoma. Cancer Res., 27, 880-889.
5) Feinberg, A. P. & Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem., 132, 6-13.
6) Hearing, V. J., Ekel, T. M. & Montague, P. M. (1981) Mammalian tyrosinase: Isozymic forms of the enzyme. Int. J. Biochem., 13, 99-103.
7) Kwon, B. S., Haq, A. K., Pomerantz, S. H. & Halaban, R. (1987) Isolation and sequence of a c DNA clone for human tyrosinase that maps at the mouse c-albino locus. Proc. nat. Acad. Sci. USA, 84, 7473-7477.
8) Kwon, B. S., Wakulchik, M., Haq, A. K., Halaban, R. & Kestler, D. (1988) Sequence analysis of mouse tyrosinase cDNA and the effect of melanotropin on its gene expression. Biochem. biophys. Res. Commun., 153, 1301-1309.
9) Lerch, K. (1988) Protein and active-site structure of tyrosinase. In: Advances in Pigment Cell Research, edited by J. T. Bagnara, Alan R. Liss, New York, pp. 85-98.
10) Lerner, A. B., Fitzpatrick, T. B., Calkins, E. & Summerson, W. H. (1950) Mammalian tyrosinase: The relationship of copper to enzymic activity. J. biol. Chema., 187, 793-802.
11) Marshall, R. D. (1974) The nature and metabolism of the carbohydrate-peptide linkages of glycoproteins. Biochem. Soc. Symp., 40, 17-26.
12) Maxam, A. M. & Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Meth. Enzymol., 65, 499-560.
13) Müller, G., Ruppert, S., Schmid, E. & Schutz, G. (1988) Functional analysis of alternatively spliced tyrosinase gene transcripts. EMBO J., 7, 2723-2730.
14) Müller, R. M., Taguchi, H. & Shibahara, S. (1987) Nucleotide sequence and organization of the rat heme oxygenasegene. J. biol. Chem., 262, 6795-6802.
15) Nishioka, K. (1978) Particulate tyrosinase of human malignant melanoma. Europ. J. Biochem., 85, 137-146.
16) Ohkura, T., Yamashita, K., Mishima, Y. & Kobata, A. (1984) Purification of hamster melanoma tyrosinase and structural studies of their asparagine-linked sugar chains. Arch. Biochem. byophys., 235, 63-77.
17) Okayama, H. & Berg, P. (1982) High-efficiency cloning of full-length cDNA. Molec. cell. Biol., 2, 161-170.
18) Pomerantz, S. H. (1966) The tyrosine hydroxylase activity of mammalian tyrosinase. J. biol. Chem., 241, 161-168.
19) Pomerantz, S. H. & Li, J. P-C. (1973) Purification and properties of tyrosinase isoenzymes from hamster melanoma. Yale J. biol. Med., 46, 541-552.
20) Ruppert, S., Müller, G., Kwon, B. & Schutz, G. (1988) Multiple transcripts of the mouse tyrosinase gene are generated by alternative splicing. EMBO J., 7, 2715-2722.
21) Shibahara, S., Tomita, Y., Sakakura, T., Nager, C., Chaudhuri, B. & Müller, R. (1986) Cloning and expression of cDNA encoding mouse tyrosinase. Nucleic Acids Res., 14, 2413-2427.
22) Shimao, K. (1962) Partial purification and kinetic studies of mammalian tyrosinase. Biochim. biophys. Acta (Amst.), 62, 205-215.
23) Yamamoto, H., Takeuchi, S., Kudo, T., Makino, K., Nakata, A., Shinoda, T. & Takeuchi, T. (1987) Cloning and sequencing of mouse tyrosinase cDNA. Jap. J. Genet., 62, 271-274.

Right : 1) Aviv, H. T. & Leder, P. (1972) Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc. nat. Acad. Sci. USA, 69, 1408-1412.
2) Bause, E. (1983) Structural requirements of N-glycosylation of proteins. Biochem. J., 209, 331-336.
3) Brüggen, J., Macher, E. & Sorg, C. (1981) Expression of surface antigens and its relation to parameters of malignancy in human malignant melanoma. Cancer Immunol. Immunother., 10, 121-127.
4) Burnet, J. B., Seiler, H. & Brown, I. V. (1967) Separation and characterization of multiple forms of tyrosinase from mouse melanoma. Cancer Res., 27, 880-889.
5) Feinberg, A. P. & Vogelstein, B. (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem., 132, 6-13.
6) Hearing, V. J., Ekel, T. M. & Montague, P. M. (1981) Mammalian tyrosinase: Isozymic forms of the enzyme. Int. J. Biochem., 13, 99-103.
7) Kwon, B. S., Haq, A. K., Pomerantz, S. H. & Halaban, R. (1987) Isolation and sequence of a c DNA clone for human tyrosinase that maps at the mouse c-albino locus. Proc. nat. Acad. Sci. USA, 84, 7473-7477.
8) Kwon, B. S., Wakulchik, M., Haq, A. K., Halaban, R. & Kestler, D. (1988) Sequence analysis of mouse tyrosinase cDNA and the effect of melanotropin on its gene expression. Biochem. biophys. Res. Commun., 153, 1301-1309.
9) Lerch, K. (1988) Protein and active-site structure of tyrosinase. In: Advances in Pigment Cell Research, edited by J. T. Bagnara, Alan R. Liss, New York, pp. 85-98.
10) Lerner, A. B., Fitzpatrick, T. B., Calkins, E. & Summerson, W. H. (1950) Mammalian tyrosinase: The relationship of copper to enzymic activity. J. biol. Chem., 187, 793-802.
11) Marshall, R. D. (1974) The nature and metabolism of the carbohydrate-peptide linkages of glycoproteins. Biochem. Soc. Symp., 40, 17-26.
12) Maxam, A. M. & Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Meth. Enzymol., 65, 499-560.
13) Müller, G., Ruppert, S., Schmid, E. & Schutz, G. (1988) Functional analysis of alternatively spliced tyrosinase gene transcripts. EMBO J., 7, 2723-2730.
14) Müller, R. M., Taguchi, H. & Shibahara, S. (1987) Nucleotide sequence and organization of the rat heme oxygenasegene. J. biol. Chem., 262, 6795-6802.
15) Nishioka, K. (1978) Particulate tyrosinase of human malignant melanoma. Europ. J. Biochem., 85, 137-146.
16) Ohkura, T., Yamashita, K., Mishima, Y. & Kobata, A. (1984) Purification of hamster melanoma tyrosinase and structural studies of their asparagine-linked sugar chains. Arch. Biochem. byophys., 235, 63-77.
17) Okayama, H. & Berg, P. (1982) High-efficiency cloning of full-length cDNA. Molec. cell. Biol., 2, 161-170.
18) Pomerantz, S. H. (1966) The tyrosine hydroxylase activity of mammalian tyrosinase. J. biol. Chem., 241, 161-168.
19) Pomerantz, S. H. & Li, J. P-C. (1973) Purification and properties of tyrosinase isoenzymes from hamster melanoma. Yale J. biol. Med., 46, 541-552.
20) Ruppert, S., Müller, G., Kwon, B. & Schutz, G. (1988) Multiple transcripts of the mouse tyrosinase gene are generated by alternative splicing. EMBO J., 7, 2715-2722.
21) Shibahara, S., Tomita, Y., Sakakura, T., Nager, C., Chaudhuri, B. & Müller, R. (1986) Cloning and expression of cDNA encoding mouse tyrosinase. Nucleic Acids Res., 14, 2413-2427.
22) Shimao, K. (1962) Partial purification and kinetic studies of mammalian tyrosinase. Biochim. biophys. Acta (Amst.), 62, 205-215.
23) Yamamoto, H., Takeuchi, S., Kudo, T., Makino, K., Nakata, A., Shinoda, T. & Takeuchi, T. (1987) Cloning and sequencing of mouse tyrosinase cDNA. Jap. J. Genet., 62, 271-274.

Date of correction: August 31, 2006 Reason for correction: - Correction: PDF FILE Details: -

Abstract

A cDNA clone, pHTγ1, representing human tyrosinase mRNA was isolated by screening a melanoma cDNA library with a synthetic oligonucleotide complementary to a segment of the human tyrosinase cDNA, Pmel 34 [Kwon et al. (1987) Proc. nat. Acad. Sci. USA 84, 7473-7477]. However, there are a number of differences in the nucleotide sequence between two cDNAs, pHTγ1 and Pmel 34, particularly in the region coding for the carboxyl terminus of the enzyme (putative exon 5). We therefore cloned the genomic DNA segment carrying the exon 5 of the human tyrosinase gene by screening a human placental genomic DNA library with a cloned cDNA probe. The nucleotide sequences of human tyrosinase cDNA as well as a part of its gene were determined. Mature human tyrosinase is composed of 511 amino acids with a molecular weight of 58, 000. We provide evidence for the presence of at least two species of human tyrosinase mRNA generated by alternative splicing in human pigmented melanoma cells.

Corresponding author

Correction information

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