The S100 family of multipurpose calcium-binding proteins

Journal of Cutaneous Pathology

Volumn 25, Issue 10, 1998, Pages 521-529

  McNutt, N Scott ^a,b  

^a NEW YORK PRESBYTERIAN HOSPITAL   (United States)

^b WEILL CORNELL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CALCIUM BINDING PROTEIN; CALCIUM ION; PROTEIN S 100;

CALCIUM METABOLISM; CELL INTERACTION; HUMAN; IMMUNOHISTOCHEMISTRY; PROTEIN FAMILY; REVIEW; SKIN TUMOR;

EID: 0031744189     PISSN: 03036987     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0560.1998.tb01735.x     Document Type: Review

References (109)

1. Zimmer DB, Cornwall EH, Landar A, Song W. The S100 protein family: history, function, and expression. Brain Res Bull 1995: 37: 417.
2. Moore BW. A soluble protein characteristic of the nerve system. Biochem Biophys Res Commun 1965: 19: 739
3. Haimoto H, Hosada S, Kato K. Differential distribution of immunoreactive S100-alpha and S100-beta proteins in normal nonnervous human tissues. Lab Invest 1987: 57: 489.
4. Takahashi K, Isobe T, Ohtsuki Y, Akagi T, Sonobe H, Okoyama T. Immunohistochemical study on the distribution of a and b subunits of S-100 protein in human neoplasms and normal tissues. Virchows Archiv B Cell Pathol 1984: 45: 385.
5. Takahashi K, Isobe T, Ohtsuki Y, Sonobe H, Takeda I, Akagi T. Immunohistochemical localization and distribution of S-100 proteins in the human lymphoreticular system. Am J Pathol 1984: 116: 497.
6. Wick MR, Swanson PE, Rocamora A. Recognition of malignant melanoma by monoclonal antibody HMB-45. An immunohistochemical study of 200 paraffin-embedded cutaneous tumors. J Cutan Pathol 1988: 154: 201.
7. Wick MR, Swanson PE, Ritter JH, Fitzgibbon JF. The immunohistology of cutaneous neoplasia: A practical perspective. J Cutan Pathol 1993: 20: 481.
8. ++-binding proteins S100A6 and S100B in primary cutaneous melanoma. J Cutan Pathol 1997: 24: 76.
9. Ilg EC, Schafer BW, Heizmann CW. Expression pattern of S100 calcium-binding proteins in human tumors. Int J Cancer 1996: 68: 325.
10. Schafer BW, Heizmann CW. The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem Sci (Engl) 1996: 21: 134.
11. Schafer BW, Wicki R, Engelcamp D, Mattei MG, Heizmann CW. Isolation of a YAC clone covering a cluster of nine S100 genes on human chromosome 1q21: rationale for a new nomenclature of the calcium-binding protein family. Genomics 1995: 25: 638.
12. Wicki R, Marenholz I, Mischke D, Schafer BW, Heizmann CW. Characterization of the human S100A12 (calgranulin C, p6, CAAF1, CGRP) gene, a new member of the S100 gene cluster on chromosome 1q21. Cell Calcium (Scotland) 1996: 20: 459.
13. Wicki R, Schafer BW, Erne P, Heizmann CW. Characterization of the human and mouse cDNAs coding for S100A13, a new member of the S100 protein family. Biochem Biophys Res Commun 1996: 227: 594.
14. Marshak DR. S100 beta as a neurotrophic factor. Prog Brain Res 1990: 86: 169.
15. Drohat AC, Amburgey JC, Abildgaard F, Starich MR, Baldisseri D, Weber DJ. Solution structure of rat apo-S100B (beta beta) as determined by NMR spectroscopy. Biochemistry 1996: 35: 11577.
16. Groves P, Finn BE, Kuznicki J, Forsen S. A model for target protein binding to calcium-activated S100 dimers. FEBS Lett 1998: 421: 175.
17. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD. Molecular Biology of the Cell. 3rd edn. New York: Garland Publishing, Inc., 1994.
18. Nakamura Y, Becker LE, Marks A. S100 protein in human chordoma and human and rabbit notochord. Arch Pathol Lab Med 1983: 107: 118.
19. Chaudhuri D, Horrocks WD Jr, Amburgey JC, Weber DJ. Characterization of lanthanide ion binding to the EF-hand protein S100 beta by luminescence spectroscopy. Biochemistry 1997: 36: 9674.
20. 2+/S100 regulation of giant protein kinases. Nature 1996: 380 (6575): 636.
21. Newton RA, Hogg N. The human S100 protein MRP-14 is a novel activator of the beta 2 integrin Mac-1 on neutrophils. J Immunol 1998: 160: 1427.
22. Hunter MJ, Chazin WJ. High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factor-related proteins 8 and 14. J Biol Chem 1998: 273: 12427.
23. Rosai J, Dorfman RF. Sinus histiocytosis with massive lymphadenopathy. A newly recognized benign clinicopathological entity. Arch Pathol 1969: 87: 63.
24. Eisen RN, Buckley PJ, Rosai J. Immunophenotypic characterization of sinus histiocytosis with massive lymphadenopathy (Rosai-Dorfman disease). Semin Diagn Pathol 1990: 7: 74.
25. Foucar E, Rosai J, Dorfman RF. Sinus histiocytosis with massive lymphadenopathy. Arch Dermatol 1988: 124: 1211.
26. Muller H, Takeshita M. In situ immunophenotype of macrophages and lymphocytes in granuloma formation of tuberculous lymphadenitis in HIV-infected and immunocompetent patients. Res Virol 1991: 142: 159.
27. Cuevas-Santos J. Estudio inmunohistoquímico básico de las células del sistema monocito-macrófago, en el espectro inmunopatológico de la lepra. Doctoral Thesis ed. Alcalá de Henares, Spain: University of Alcalá, Facultad de Medicina, 1996.
28. Cuevas-Santos J, Contreras Rubio F, McNutt NS. The role of S100+ macrophages and Factor 13a+ dendritic cells in multibacillary leprosy. J Cutan Pathol 1998: 25: 530.
29. Rammes A, Roth J, Goebeler M, Klempt M, Hartmann M, Sorg C. Myeloid-related protein (MRP) 8 and MRP14, calcium binding proteins of the S100 family, are secreted by activated macrophages via a novel, tubulin dependent pathway. J Biol Chem 1997: 272: 9496.
30. Hu SP, Harrison C, Xu K, Cornish CJ, Geczy CL. Induction of the chemotactic S100 protein, CP-10, in monocytes/ macrophages by lipopolysaccharide. Blood 1996: 87: 3919.
31. Cornish CJ, Devery JM, Poronnik P, Lackmann M, Cook DI, Geczy CL. S100 protein Cp-10 stimulates myeloid cell chemotaxis without activation. J Cell Physiol 1996: 166: 427.
32. Lau W, Devery JM, Geczy CL. A chemotactic S100 peptide enhances scavenger receptor and Mac-1 expression and cholesteryl ester accumulation in murine peritoneal macrophages in vivo. J Clin Invest 1995: 95: 1957.
33. Goebeler M, Roth J, Burwinkel F, Vollmer E, Bocker W, Sorg C. Expression and complex formation of S100-like proteins MRP8 and MRP14 by macrophages during renal allograft rejection. Transplantation 1994: 58: 355.
34. Bhardwaj RS, Zotz C, Zwadlo-Klarwasser G, et al. The calcium-binding proteins MRP8 and MRP14 form a membrane-associated heterodimer in a subset of monocytes macrophages present in acute but absent in chronic inflammatory lesions. Eur J Immunol 1992: 22: 1891.
35. Takenaga K, Nakamura Y, Sakiyama S. Cellular localization of pEL98 protein, an S100-related calcium binding protein, in fibroblasts and its tissue distribution analyzed by monoclonal antibodies. Cell Struct Funct 1994: 19: 133.
36. Loftus B, Loh LC, Curran B, Henry K, Leader M. Mac387: its non-specificity as a tumour marker or marker of histiocytes. Histopathol 1991: 19: 251.
37. Goebeler M, Roth J, Teigelkamp S, Sorg C. The monoclonal antibody MAC387 detects an epitope on the calcium-binding protein MRP14. J Leukoc Biol 1994: 55: 259.
38. Guignard F, Mauel J, Markert M. The monoclonal antibody MAC 387 recognizes three S100 proteins in human neutrophils. Immunol Cell Biol (Australia) 1996: 74: 105.
39. Klingelhofer J, Ambartsumian NS, Lukanidin EM. Expression of the metastasis-associated mts1 gene during mouse development. Dev Dyn 1997: 210: 87.
40. Mrak RE, Sheng JG, Griffin WS. Glial cytokines in Alzheimer's disease: review and pathogenic implications. Hum Pathol 1995: 26: 816.
41. Sheng JG, Ito K, Skinner RD, et al. In vivo and in vitro evidence supporting a role for the inflammatory cytokine interleukin-1 as a driving force in Alzheimer pathogenesis. Neurobiol Aging 1996: 17: 761.
42. Lai F, Williams RS. A prospective study of Alzheimer's disease in Down's syndrome. Arch Neurol 1989: 46: 849
43. Gerlai R, Roder J. Abnormal exploratory behavior in transgenic mice earning multiple copies of the human gene for S100 beta. J Psychiatry Neurosci 1995: 20: 105.
44. Castets F, Griffin WS, Marks A, Van Eldik LJ. Transcriptional regulation of the human S100 beta gene. Brain Res Mol Brain Res 1997: 46: 208.
45. Barger SW, Van Eldik LJ, Mattson MP. S100 beta protects hippocampal neurons from damage induced by glucose deprivation. Brain Res 1995: 677: 167.
46. Hu J, Van Eldik LJ. S100 beta induces apoptotic cell death in cultured astrocytes via a nitric oxide-dependent pathway. Biochim Biophys Acta 1996: 1313: 239.
47. Hu J, Castets F, Guevara JL, Van Eldik LJ. S100 beta stimulates inducible nitric oxide synthase activity and mRNA levels in rat cortical astrocytes. J Biol Chem 1996: 271: 2543.
48. Dumarey CH, Labrousse V, Rastogi N, Vargaftig BB, Bachelet M. Selective mycobacterium avium-induced production of nitric oxide by human monocyte-derived macrophages. J Leukoc Biol 1994: 56: 36.
49. Jeevan A, Bucana CD, Dong Z, et al. Ultraviolet radiation reduces phagocytosis and intracellular killing of mycobacteria and inhibits nitric oxide production by macrophages in mice. J Leukoc Biol 1995: 57: 883.
50. Marcinkiewicz J, Grabowska A, Chain B. Nitric oxide up-regulates the release of inflammatory mediators by mouse macrophages. Eur J Immunol 1995: 25: 947.
51. Barger SW, Van Eldik LJ. S100 beta stimulates calcium fluxes in glial and neuronal cells. J Biol Chem 1992: 267: 9689.
52. Winningham-Major F, Staecker JL, Barger SW, Coats S, Van Eldik LJ. Neurite extension and neuronal survival activities of recombinant S100 beta proteins that differ in the content and position of cysteine residues. J Cell Biol 1989: 109: 3063.
53. ++ in mouse epidermal cells is controlled by E-cadherin. J Cell Biol 1991: 114: 545.
54. Boitano S, Dirksen ER, Evans WH. Sequence-specific antibodies to connexins block intercellular calcium signaling through gap junctions. Cell Calcium (Scotland) 1998: 23: 1.
55. Muyderman H, Nilsson M, Blomstrand F, et al. Modulation of mechanically induced calcium waves in hippocampal astroglial cells. Inhibitory effects of alpha 1-adrenergic stimulation. Brain Res 1998: 793: 127.
56. Frenzel EM, Johnson RG. Gap junction formation between cultured embryonic lens cells is inhibited by antibody to N-cadherin. Dev Biol 1996: 179: 1.
57. Wang Y, Rose B. An inhibition of gap-junctional communication by cadherins. J Cell Sci 1997: 110: 301.
58. Kurata WE, Lau AF. p130gag-fps disrupts gap junctional communication and induces phosphorylation of connexin43 in a manner similar to pp660v-src. Oncogene 1994: 9: 329.
59. Warn-Cramer BJ, Cottrell GT, Burt JM, Lau AF. Regulation of connexin-43 gap junctional intercellular communication by mitogen-activated protein kinase. J Biol Chem 1998: 273: 9188.
60. Torok K, Stauffer K, Evans WH. Connexin 32 of gap junctions contains two cytoplasmic calmodulin-binding domains. Biochem J 1997: 326: 479.
61. Peracchia C, Wang X, Li L, Peracchia LL. Inhibition of calmodulin expression prevents low-pH-induced gap uncoupling in Xenopus oocytes. Pflugers Arch 1996: 431: 379.
62. McNutt NS, Hershberg RA, Weinstein RS. Further observations on the occurrence of nexuses in benign and malignant human cervical epithelium. J Cell Biol 1971: 51: 805.
63. Tada J, Hashimoto K. Ultrastructural localization of gap junction protein connexin 43 in normal human skin, basal cell carcinoma, and squamous cell carcinoma. J Cutan Pathol 1997: 24: 628.
64. Budunova IV, Carbajal S, Viaje A, Slaga TJ. Connexin expression in epidermal cell lines from SENCAR mouse skin tumors. Mol Carcinog 1996: 15: 190.
65. Gibson DF, Bikle DD, Harris J, Goldberg GS. The expression of the gap junctional protein Cx43 is restricted to proliferating and non differentiated normal and transformed keratinocytes. Exp Dermatol 1997: 6: 167.
66. Jansen LA, de Vrije T, Jongen WM. Differences in the calcium-mediated regulation of gap junctional intercellular communication between a cell line consisting of initiated cells and a carcinoma-derived cell line. Carcinogenesis 1996: 17: 2311.
67. Nakatani K, Kawanabe Y, Kato A, Tanaka T. Interaction of propanolol with S100 proteins of the cardiac muscle. Eur J Pharmacol 1996: 315: 335.
68. Hitomi J, Yamaguchi K, Kikuchi Y, Kimura T, Maruyama K, Nagasaki K. A novel calcium-binding protein in amniotic fluid, CAAF1: its molecular cloning and tissue distribution. J Cell Sci 1996: 109: 805.
69. Hitomi J, Maruyama K, Kikuchi Y, Nagasaki K, Yamaguchi K. Characterization of a new calcium-binding protein abundant in amniotic fluid, CAAF2, which is produced by fetal epidermal keratinocytes during embryogenesis. Biochem Biophys Res Commun 1996: 228: 757.
70. Chang E, Dehner L, Wick M. Metastatic melanoma with rhabdoid differentiation: A study of 31 cases. Lab Invest 1992: 66: 31a.
71. Paul E, Cochran AJ, Wen DR. Immunohistochemical demonstration of S-100 protein and melanoma-associated antigens in melanocytic nevi. J Cutan Pathol 1988: 15: 161.
72. Shrestha P, Muramatsu Y, Kudeken W, et al. Localization of Ca (2+)-binding S100 proteins in epithelial tumours of the skin. Virchows Arch Pathol Anal 1998: 432: 53.
73. Ichihara S, Koshikawa T, Nakamura S, Yatabe Y, Kato K. Epithelial hyperplasia of the usual type expresses both S100-alpha and S100-beta in a heterogeneous pattern but ductal carcinoma in situ can express only S100-alpha in a monotonous pattern. Histopathol 1997: 30: 533.
74. Takenaga K, Nakamura Y, Sakiyama S. Expression of antisense RNA to S100A4 gene encoding an S100-related calcium-binding protein suppresses metastatic potential of high-metastatic Lewis lung carcinoma cells. Oncogene 1997: 14: 331.
75. Anbazhagan R, Gusterson RA. Ultrastructure and immunohistochemistry of the embryonicc type of fat identified in the human infant breast. Anat Rec 1995: 241: 129.
76. Wu T, Angus CW, Yao XL, Logun C, Shelhamer JH. P11, a unique member of the S100 family of calcium-binding proteins, interacts with and inhibits the activity of 85-kDa cytosolic phospholipase A2. J Biol Chem 1997: 272: 17145.
77. Landar A, Caddell G, Chesshet J, Zimmer DB. Identification of an S100A1/S100B target protein: phosphoglucomutase. Cell Calcium (Scotland) 1996: 20: 279.
78. Katsumata Y, Ito H, Aoki M, et al. Phosphoglucomutase 1 and 6-phosphogluconate dehydrogenase types in human skin and adipose tissue. J Forensic Sci 1982: 27: 192.
79. Enzinger FM, Weiss SW. Soft Tissue Tumors. 3rd edn. St. Louis, Mo.: C. V. Mosby Co., 1995.
80. Chu P, LeBoit PE. Histologic features of cutaneous sinus histiocytosis (Rosai-Dorfman disease): study of cases both with and without systemic involvement. J Cutan Pathol 1992: 19: 201.
81. Perrin C, Michiels JF, Lacour JP, Chagnon A, Fuzibet JG. Sinus histiocytosis (Rosai-Dorfman disease) clinically limited to the skin. J Cutan Pathol 1993: 20: 368.
82. Hunt SJ, Shin SS. Solitary reticulohistiocytoma in pregnancy: Immunohistochemical and ultrastructural study of a case with unusual immunophenotype. J Cutan Pathol 1995: 22: 177.
83. Tomaszewski M-M, Lupton GP. Unusual expression of S-100 protein in histiocytic neoplasms. J Cutan Pathol 1998: 25: 129.
84. Gagne EJ, Su WPD. Chordoma involving the skin: an immunohistochemical study of 11 cases. J Cutan Pathol. 1992: 19: 469.
85. Imlay SP, Argenvi ZB, Stone MS, McCollough ML, Henghold WB. Cutaneous parachordoma. A light microscopic and immunohistochemical report of two cases and review of the literature. J Cutan Pathol 1998: 25: 279.
86. Wood GS, Haber RS. Novel histiocytoses considered in the context of histiocyte subset differentiation. Arch Dermatol 1993: 129: 210.
87. Wood GS, Turner RR, Shiurba RA, Eng L, Warnke RA. Human dendritic cells and macrophages. In situ immunophenotypic definition of subsets that exhibit specific morphologic and microenvironmental characteristics. Am J Pathol 1985: 119: 73.
88. Sidoroff A, Zelger B, Steiner H, Smith N. Indeterminate cell histiocytosis - a clinicopathological entity with features of both X- and non-X histiocytosis. Br J Dermatol 1996: 134: 525.
89. Hashimoto K, Kagetsu N, Taniguchi Y, Weintraub R, Chapman-Winokur RL, Kasiborski A. Immunohistochemistry and electron microscopy in Langerhans' cell histiocytosis confined to the skin. J Am Acad Dermatol 1991: 25: 1044.
90. Pujol RM, Moreno A, Lopez D, Alomar A, de Moragas JM. Childhood self-healing histiocytosis X. Ped Dermatol 1988: 5: 97.
91. Miracco C, Raffaelli M, Margherita de Santi M, Fimiani M, Tosi P. Solitary cutaneous reticulum cell tumor. Enzyme-immunohistochemical and electron-microscopic analogies with IDRC sarcoma. Am J Dermatopathol 1988: 10: 47.
92. Nakamura S. Interdigitating cell sarcoma (ICS). Evidence of interdigitating cell origin, immunocytochemical studies with monoclonal anti-ICS antibodies. Virchows Arch Pathol Anat 1989: 415: 447.
93. Barrett TL, Skelton HG, Smith KJ, O'Grady TC, Proctor-Shipman L. Ossifying fibromyxoid tumor of soft parts: A case report and review. J Cutan Pathol 1996: 23: 378.
94. Nakayama F, Kuwahara T. Ossifying fibromyxoid tumor of soft parts of the back. J Cutan Pathol 1996: 23: 385.
95. Velasco-Pastor AM, Martinez-Escribiano J, del Pino Gil-Mateo M, Quecedo-Esteganez E, Fortea-Baixauli JM, Aliaga-Boniche A. Ossifying fibromyxoid tumor of soft parts. J Cutan Pathol 1996: 23: 381.
96. Johnson MD, Glick AD, Davis BW. Immunohistochemical evaluation of Leu-7, myelin basic-protein, S100-protein, glial-fibrillary acidic-protein, and LN3 immunoreactivity in nerve sheath tumors and sarcomas. Arch Pathol Lab Med 1988: 112: 155.
97. Diaz-Flores L, Alvarez-Argüelles H, Madrid JF, Varela H, Gonzales MP, Gutierrez R. Perineurial cell tumor (perineurioma) with granular cells. J Cutan Pathol 1997: 24: 575.
98. Smith K, Mezebish D, Williams JP, et al. Cutaneous epithelioid schwannomas: a rare variant of a benign peripheral nerve sheath tumor. J Cutan Pathol 1998: 25: 50.
99. Barnhill RL, Mihm MC Jr. Cellular neurothekeoma. A distinctive variant of neurothekeoma mimicking melanocytic tumors. Am J Surg Pathol 1990: 14: 113.
100. Husain S, Silvers DN, Halperin AJ, McNutt NS. Histologic spectrum of neurothekeoma and the value of immunoperoxidase staining for S-100 protein in distinguishing it from melanoma. Am J Dermatopathol 1994: 16: 496.
101. Lucas DR, Nascimento AG, Sim FH. Clear cell sarcoma of soft tissues. Mayo Clinic experience with 35 cases. Am J Surg Pathol 1992: 16: 1197.
102. Laskin WB, Weiss SW, Bratthauer GL. Epithelioid variant of malignant peripheral nerve sheath tumor (malignant epithelioid schwanoma). Am J Surg Pathol 1991: 15: 1136.
103. Misago N, Ishii Y, Kohda H. Malignant peripheral nerve sheath tumor of the skin: a superficial form of this tumor. J Cutan Pathol 1996: 23: 182.
104. Shimizu S, Teraki Y, Ishiko A, et al. Malignant epithelioid Schwannoma of the skin showing partial HMB-45 positivity. Am J Dermatopathol 1993: 15: 378.
105. Shitabata PK, Ritter JH, Fitzgibbon JF, Dehner LP, Wick MR. Pleomorphic hamartoma of the subcutis. J Cutan Pathol 1995: 22: 269.
106. Penneys NS, Kaiser M. Cylindroma expresses immunohistochemical markers linking it to eccrine coil. J Cutan Pathol 1993: 20: 40.
107. Wiley EL, Milchgrub S, Freeman RG, Kim ES. Sweat gland adenomas: Immunohistochemical study with emphasis on myoepithelial differentiation. J Cutan Pathol 1993: 20: 337.
108. Swanson PE, Cherwitz DL, Neumann MP, Wick MR. Eccrine sweat gland carcinoma: An histologic and immunohistochemical study of 32 cases. J Cutan Pathol 1987: 14: 65.
109. Modlin RL, Rowden G, Taylor CR, Rea TH. Comparison of S-100 and OKT6 antisera in human skin. J Invest Dermatol 1984: 83: 206.