Demonstration of heterodimer formation between S100B and S100A6 in the yeast two-hybrid system and human melanoma

Experimental Cell Research

Volumn 246, Issue 2, 1999, Pages 501-509

  Yang, Qiner ^a   O'Hanlon, David ^a   Heizmann, Claus W ^b   Marks, Alexander ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Calcyclin; Confocal microscopy; Melanoma; S100 ; Yeast two hybrid screen

Indexed keywords

CALCIUM BINDING PROTEIN; COMPLEMENTARY DNA; PROTEIN S 100; PROTEIN SUBUNIT;

ARTICLE; CELL CYCLE; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA LIBRARY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MELANOMA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

EID: 0033080449     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1998.4314     Document Type: Article

References (68)

1. Kligman D., Hilt D. C. The S100 protein family. Trends Biochem. Sci. 13:1988;437-443.
2. Zimmer D. B., Cornwall E. H., Landar A., Song W. The S100 protein family: history, function, and expression. Brain Res. Bull. 37:1995;417-429.
3. Schäfer B. W., Heizmann C. W. The S100 family of EF-hand calcium-binding proteins: Functions and pathology. Trends Biochem. Sci. 21:1996;134-140.
4. Wicki R., Marenholz I., Mischke D., Schäfer B. W., Heizmann C. W. Characterization of the human S100A12 (calgranulin C, p6, CAAF1, CGRP) gene, a new member of the S100 gene cluster on chromosome 1q21. Cell Calcium. 20:1996;459-464.
5. Wicki R., Schäfer B. W., Erne P., Heizmann C. W. Characterization of the human and mouse cDNAs coding for S100A13, a new member of the S100 protein family. Biochem. Biophys. Res. Commun. 14:1996;594-599.
6. Schäfer B. W., Wicki R., Engelkamp D., Mattei M-G., Heizmann C. W. Isolation of a YAC clone covering a cluster of nine S100 genes on human chromosome 1q21: Rationale for a new nomenclature of the S100 calcium-binding protein family. Genomics. 25:1995;638-643.
7. Engelkamp D., Schäfer B. W., Mattei M. G., Erne P., Heizmann C. W. Six S100 genes are clustered on human chromosome 1q21: Identification of two genes coding for the two previously unreported calcium-binding proteins S100D and S100E. Proc. Natl. Acad. Sci. USA. 90:1993;6547-6551.
8. Allore R., O'Hanlon D., Price R., Neilson K., Willard H. F., Cox D. R., Marks A., Dunn R. J. Gene encoding the β subunit of S100 protein is on chromosome 21: Implications for Down syndrome. Science. 239:1988;1311-1313.
9. Donato R. Perspectives in S-100 protein biology. CellCalcium. 12:1991;713-726.
10. Krebs J., Quadroni M., Van Eldik L. J. Dance of the dimers. Nature Struct. Biol. 2:1995;711-714.
11. 2+. Nature Struct. Biol. 2:1995;790-796.
12. Drohat A. C., Amburgey J. C., Abildgaard F., Starich M. R., Baldisseri D., Weber D. J. Solution structure of rat apo-S100B (ββ) as determined by NMR spectroscopy. Biochemistry. 35:1996;11577-11588.
13. Kilby P. M., Van Eldik L. J., Roberts G. C. The solution structure of the bovine S100B protein dimer in the calcium-free state. Structure. 15:1996;1041-1052.
14. 9k. Protein Sci. 5:1996;2162-2174.
15. Isobe T., Ishioka N., Masuda T., Takahashi Y., Ganno S., Okuyama T. A rapid separation of S100 subunits by high performance liquid chromatography: The subunit composition of S100 proteins. Biochem. Int. 6:1983;419-426.
16. 2+2+. J. Biol. Chem. 261:1986;8192-8203.
17. 2+. Biochemistry. 27:1988;2728-2736.
18. Donato R. Calcium-sensitivity of brain microtubule proteins in the presence of S100 proteins. Cell Calcium. 6:1985;343-361.
19. Zimmer D. B., Van Eldik L. J. Identification of a molecular target for the calcium-modulated protein S100. J. Biol. Chem. 261:1986;11424-11428.
20. 2+. J. Biol. Chem. 268:1993;12669-12674.
21. Okazaki K., Obata N. H., Inoue S., Hidaka H. S100β is a target protein of neurocalcin δ, an abundant isoform in glial cells. Biochem. J. 306:1995;551-555.
22. Landar A., Caddell G., Chessher J., Zimmer D. B. Identification of an S100A1/S100B target protein: Phosphoglucomutase. Cell Calcium. 20:1996;279-285.
23. Ivanenkov V. V., Jamieson G. A. Jr., Gruenstein E., Dimlich R. V. W. Characterization of S100b binding epitopes: Identification of a novel target, the actin capping protein, Cap Z. J. Biol. Chem. 270:1995;14651-14658.
24. Onions J., Hermann S., Grundström T. Basic helix-loop-helix protein sequences determining differential inhibition by calmodulin and S100 proteins. J. Biol. Chem. 272:1997;23930-23937.
25. Albert K. A., Wu W. C., Nairm A. C., Greengard P. Inhibition by calmodulin of calcium/phospholipid-dependent protein phosphorylation. Proc. Natl. Acad. Sci. USA. 81:1984;3622-3625.
26. Baudier J., Mochly-Rosen D., Newton A., Lee S.-H., Koshlan D. E. Jr., Cole R. D. Comparison of S100b protein with calmodulin: Interactions with melittin and microtubule associatedtautau. Biochemistry. 26:1987;2886-2893.
27. Baudier J., Delphin C., Grunwald D., Khochbin S., Lawrence J. J. Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein. Proc. Natl. Acad. Sci. USA. 89:1992;11627-11631.
28. Sheu F-S., Azmitia E. C., Marshak D. R., Parker P. J., Routtenberg A. Glial-derived S100b protein selectively inhibits recombinant β protein kinase C (PKC) phosphorylation of neuron-specific protein F1/GAP43. Mol. Brain Res. 21:1994;62-66.
29. Chien C.-T., Bartel P. L., Sternglanz R., Fields S. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. USA. 88:1991;9578-9582.
30. 2+. J. Cutan. Pathol. 24:1997;76-80.
31. Calabretta B., Battini R., Kaczmarck L., de Riel J. K., Baserga R. Molecular cloning of the cDNA for a growth factor-inducible gene with strong homology to S100, a calcium binding protein. J. Biol. Chem. 261:1986;12628-12632.
32. Marks A., Petsche D., O'Hanlon D., Kwong P. C., Stead R., Dunn R., Baumal R., Liao S-K. S100 protein expression in human melanoma cells: Comparison of levels of expression among different cell lines and individual cells in different phases of the cell cycle. Exp. Cell Res. 187:1990;59-64.
33. Labourdette G., Marks A. Synthesis of S100 protein in monolayer cultures of rat glial cells. Eur. J. Biochem. 58:1975;73-79.
34. Ilg E. C., Schäfer B. W., Heizmann C. W. Expression pattern of S100 calcium-binding proteins in human tumors. Int. J. Cancer. 68:1996;325-332.
35. Tsoporis J. N., Marks A., Kahn H. J., Butany J. W., Liu P. P., O'Hanlon D., Parker T. G. S100β inhibits the β-protein kinase C signaling pathway associated with hypertrophy in cardiac myocytes. J. Biol. Chem. 272:1997;31915-31921.
36. Friend W. C., Clapoff S., Landry C., Becker L. E., O'Hanlon D., Allore R. J., Brown I. R., Marks A., Roder J., Dunn R. J. Cell-specific expression of high levels of human S100β in transgenic mouse brain is dependent on gene dosage. J. Neurosci. 12:1992;4337-4346.
37. Marks A., O'Hanlon D., Lei M., Percy M. E., Becker L. E. Accumulation of S100β mRNA and protein in cerebellum during infancy in Down syndrome and control subjects. Mol. Brain Res. 36:1996;343-348.
38. Moore B. W. A soluble protein characteristic of the nervous system. Biochem. Biophys. Res. Commun. 19:1965;739-744.
39. Haan E. A., Boss B. D., Cowan W. M. Production and characterization of monoclonal antibodies against the "brain-specific" proteins 14-3-2 and S100. Proc. Natl. Acad. Sci. USA. 79:1982;7585-7589.
40. Kato K., Kimura S. S100ao (α, α) protein is mainly located in the heart and striated muscles. Biochim. Biophys. Acta. 842:1985;146-150.
41. Yang Q., Hamberger H., Khatibi N., Stigbrand T., Haglid K. G. Presence of S100β in cholinergic neurons of the rat hindbrain. NeuroReport. 7:1996;3093-3099.
42. Kahn H., Marks A., Thom R. T., Baumal R. Role of antibody to S100 protein diagnostic in pathology. Am. J. Clin. Pathol. 79:1983;341-347.
43. Kahn H. J., Baumal R., Marks A. The value of immunohistochemical studies using antibody to S100 protein in dermatopathology. Int. J. Dermatopathol. 23:1984;38-44.
44. Kligman D., Marshak D. C. Isolation and characterization of a neurite extension factor from bovine brain. Proc. Natl. Acad. Sci. USA. 82:1985;7136-7139.
45. Winningham-Major F., Staecker J. L., Barger S. W., Coats S., Van Eldik L. J. Neurite extension and neuronal survival activities of recombinant S100β proteins that differ in the content and position of cysteine residues. J. Cell. Biol. 109:1989;3063-3071.
46. Selinfreund R. H., Barger S. W., Pledger W. J., Van Eldik L. J. Neurotrophic protein S100β stimulates glial cell proliferation. Proc. Natl. Acad. Sci. USA. 88:1991;3554-3558.
47. Van Eldik L. J., Christie-Pope B., Balin L. M., Shooter E. M., Whetsell W. O. Jr. Neurotrophic activity of S100β in cultures of dorsal root ganglia from embryonic chick and fetal rat. Brain Res. 542:1991;280-285.
48. Haglid K. G., Yang Q., Hamberger A., Bergman S., Widerberg A., Danielsen N. S100B stimulates neurite outgrowth in the rat sciatic nerve grafted with acellular muscle transplants. Brain Res. 753:1997;196-201.
49. Mely Y., Gérard D. Intra- and interchain disulfide bond generation in S100b protein. J. Neurochem. 55:1990;1100-1106.
50. Barger S. W., Wolchok S. R., Van Eldik L. J. Disulfide-linked S100β dimers and signal transduction. Biochim. Biophys. Acta. 1160:1992;105-112.
51. Hirschhorn R. R., Aller P., Yuan Z-A., Gibson C. W., Baserga R. Cell-cycle-specific cDNAs from mammalian cells temperature sensitive for growth. Proc. Natl. Acad. Sci. USA. 81:1984;6004-6008.
52. 2+. Biochem. J. 247:1987;663-667.
53. Murphy L. C., Murphy L. J., Tsuyuki D., Duckworth M. L., Shiu R. P. C. Cloning and characterization of a cDNA encoding a highly conserved, putative calcium binding protein, identified by an anti-prolactin receptor antiserum. J. Biol. Chem. 263:1988;2397-2401.
54. Filipek A., Heizmann C. W., Kuznicki J. Calcyclin is a calcium and zinc binding protein. FEBS Lett. 264:1990;263-266.
55. Zeng F-Y., Gerke V., Gabius H-J. Identification of annexin II, annexin VI and glycereldehyde-3-phosphate dehydrogenase as calcyclin-binding proteins in bovine heart. Int. J. Biochem. 25:1993;1019-1027.
56. 2+. Biochem. Biophys. Res. Commun. 220:1996;360-365.
57. Filipek A., Wojda U. p30, a novel protein target of mouse calcyclin (S100A6). Biochem. J. 320:1996;585-587.
58. Kuznicki J., Kordowska J., Puzianowska M., Wozniewiecz B. M. Calcyclin as a marker of human epithelial cells and fibroblasts. Exp. Cell. Res. 200:1992;425-430.
59. 2+. NeuroReport. 4:1993;383-386.
60. Gaynor R., Irie R., Morton D., Herschman H. R., Jones P., Cochran A. S100 protein: a marker for human malignant melanomas. Lancet. 1:1981;869-871.
61. Gaynor R., Irie R., Morton D., Herschman H. R. S100 protein is present in cultured human malignant melanomas. Nature. 286:1980;400-401.
62. Weterman M. A. J., Stoopen G. M., Van Muijen G. N. P., Kuznicki J., Ruiter D. J., Bloemers H. P. J. Expression of calcyclin in human melanoma cell lines correlates with metastatic behavior in nude mice. Cancer Res. 52:1992;1291-1296.
63. Cho K. H., Hashimoto K., Taniguchi Y., Pietruk T., Zarbo R. J., An T. Immunohistochemical study of melanocytic nevus and malignant melanoma with monoclonal antibodies against S-100 subunits. Cancer. 66:1990;765-771.
64. Weterman M. A. J., Van Muijen G. N. P., Bloemers H. P. J., Ruiter D. J. Expression of calcyclin in human melanocytic lesions. Cancer Res. 53:1993;6061-6066.
65. Maelandsmo G. M., Florenes V. A., Mellingsaeter T., Hovig E., Kerbel R. S., Fodstad Ø. Differential expression patterns of S100A2, S100A4 and S100A6 during progression of human malignant melanoma. Int. J. Cancer. 74:1997;464-469.
66. 2+. Br. J. Dermatol. 137:1997;39-43.
67. Jensen R., Marshak D. R., Anderson C., Lukas T. J., Watterson D. M. Characterization of human brain S100 protein fraction: Amino acid sequence of S100β J. Neurochem. 45:1985;700-705.
68. Suhy D. A., O'Halloran T. V. Metal-responsive gene regulation and the zinc metalloregulatory model. Metal Ions and Biological Systems. 1996;Dekker, New York. p. 557-578.