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. 2006 Apr 5;9(1):1–19. doi: 10.1111/j.1750-3639.1999.tb00205.x

Supratentorial Pilocytic Astrocytomas, Astrocytomas, Anaplastic Astrocytomas and Glioblastomas are Characterized by a Differential Expression of S100 Proteins

Isabelle Camby 1, Nathalie Nagy 2, Maria‐Beatriz Lopes 3, Beat W Schäfer 4, Claude‐Alain Maurage 5, Marie‐Magdeleine Ruchoux 5, Petra Murmann 4, Roland Pochet 1, Claus W Heizmann 4, Jacques Brotchi 6, Isabelle Salmon 2, Robert Kiss 1,, Christine Decaestecker 1
PMCID: PMC8098381  PMID: 9989446

Abstract

The levels of expression of the S100A1, S100A2, S100A3, S100A4, S100A5, S100A6 and S100B proteins were immunohistochemically assayed and quantitatively determined in a series of 95 astrocytic tumors including 26 World Health Organization (WHO) grade I (pilocytic astrocytomas), 23 WHO grade II (astrocytomas), 25 WHO grade III (anaplastic astrocytomas) and 21 WHO grade IV (glioblastomas) cases. The level of the immunohistochemical expression of the S100 proteins was quantitatively determined in the solid tumor tissue (tumor mass). In addition twenty blood vessel walls and their corresponding perivascular tumor astrocytes were also immunohistochemically assayed for 10 cases chosen at random from each of the four histopathological groups. The data showed modifications in the level of S100A3 protein expression; these modifications clearly identified the pilocytic astrocytomas from WHO grade II‐IV astrocytic tumors as a distinct biological group. Modifications in the level of S100A6 protein expression enabled a clear distinction to be made between low (WHO grade I and II) and high (WHO grade III and IV) grade astrocytic tumors. Very significant modifications occurred in the level of S100A1 protein expression (and, to a lesser extent, in their of the S100A4 and S100B proteins) in relation to the increasing levels of malignancy. While the S100A5 protein was significantly expressed in all the astrocytic tumors (but without any significant modifications in the levels of malignancy), the S100A2 protein was never expressed in these tumors. These data thus indicate that several S100 proteins play major biological roles in human astrocytic tumors.

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References

  • 1. Barraglough R (1998). Calcium‐binding protein S100A4 in health and disease. Biochem Biophys Acta (in press). [DOI] [PubMed] [Google Scholar]
  • 2. Baudier J, Delphin C, Grunwald D, Khochbin S, Lawrence JJ (1992). Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100B‐binding protein. Proc Natl Acad Sci USA 89:11627–11631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3. Bianchi R, Giambanco I, Donato R (1993). S‐100 protein, but not calmodulin, binds to the glial fibrillary acidic protein and inhibits its polymerization in a Ca2+‐dependent manner. J Biol Chem 268:12669–12674. [PubMed] [Google Scholar]
  • 4. Bianchi R, Verzini M, Garbuglia M, Giambanco I, Donato R (1994). Mechanism of S100 protein‐dependent inhibition of glial fibrillary acidic protein (GFAP) polymerization. Biochim Biophys Acta 1223:354–360. [DOI] [PubMed] [Google Scholar]
  • 5. Bigner SH, Humphrey PA, Wong AJ, Vogelstein B, Mark J, Friedman HS, Bigner DD (1990). Characterization of the epidermal growth factor receptor in human glioma cell lines and xenografts. Cancer Res 50:8017–8022. [PubMed] [Google Scholar]
  • 6. Bigner SH, Schrock E (1998). Molecular cytogenetics of brain tumors. J Neuropathol Exp Neurol 56:1173–1181. [DOI] [PubMed] [Google Scholar]
  • 7. Boni R, Burg G, Doguoglu A, IIg EC, Schäfer BW, Müller B, Heizmann CW (1997). Immunohistochemical localization of the Ca2+‐binding S100 proteins in normal human skin and melanocytic lesions. Br J Dermatol 137:39–43. [PubMed] [Google Scholar]
  • 8. Burger PC, Scheithauer BW (1994). Tumors of the central nervous system. Atlas of tumor pathology. Armed Forces Institute of Pathology. Washington , DC , 1994. [Google Scholar]
  • 9. Burger PC, Scheithauer BW, Vogel FS, eds (1991). Surgical pathology of the nervous system and its coverings, 3rd Edition, Churchill Livingstone: New York . [Google Scholar]
  • 10. Burger PC, Shibata T, Kleihues P (1986). The use of the monoclonal antibody Ki‐67 for the identification of proliferating cells: application to surgical neuropathology. Am J Surg Pathol 10:611–617. [DOI] [PubMed] [Google Scholar]
  • 11. Burger PC, Vogel FS, Green SB, Strike TA (1985). Glioblastoma multiforme and anaplastic astrocytoma. Pathologic criteria and prognostic implications. Cancer 56:1106–1111. [DOI] [PubMed] [Google Scholar]
  • 12. Calabretta B, Battini R, Kaczmarek L, De Riel JK, Baserga R (1986). Molecular cloning of the cDNA for a growth factor‐inducible gene with strong homology to S‐100, a calcium binding protein. J Biol Chem 261:12628–12632. [PubMed] [Google Scholar]
  • 13. Collins VP (1995). Gene amplification in human gliomas. GLIA 15:289–296. [DOI] [PubMed] [Google Scholar]
  • 14. Collins VP, James CD (1993). Gene and chromosome alterations associated with the development of human gliomas. FASEB J 7:926–930. [DOI] [PubMed] [Google Scholar]
  • 15. Coons SW, Johnson BW (1993). Regional heterogeneity in the proliferative activity of human gliomas as measured by the Ki‐67 labeling index. J Neuropathol Exp Neurol 52:609–618. [DOI] [PubMed] [Google Scholar]
  • 16. Decaestecker C, Camby I, Nagy N, Brotchi J, Kiss R, Salmon I (1998). Improving morphology‐based malignancy grading schemes in astrocytic tumors by means of computer‐assisted techniques. Brain Pathol 8:29–38. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17. Decaestecker C, Salmon I, Camby I, DeWitte O, Pasteels JL, Brotchi J, Van Ham Ph, Kiss R (1995). Identification of high versus lower risk clinical subgroups in a group of adult patients with supratentorial anaplastic astrocytomas. J. Neuropathol. Exp. Neurol 54:371–384. [DOI] [PubMed] [Google Scholar]
  • 18. Decaestecker C, Salmon I, DeWitte O, Camby I, Van Ham Ph, Pasteels JL, Brotchi J, Kiss R (1997). Nearest‐neighbour classification for the identification of aggressive versus non‐aggressive low‐grade astrocytic tumors by means of image‐cytometry‐generated variables. J Neurosurg 86:532–537. [DOI] [PubMed] [Google Scholar]
  • 19. DeHauwer C, Camby I, Darro F, Decaestecker C, Gras T, Salmon I, Kiss R, VanHam Ph (1997). Dynamic characterization of glioblastoma cell motility. Biochem Biophys Res Commun 232:267–272. [DOI] [PubMed] [Google Scholar]
  • 20. DeHauwer C, Camby I, Darro F, Migeotte I, Decaestecker C, Verbeek C, Danguy A, Brotchi J, Salmon I, Van Ham Ph, Kiss R (1998). Gastrin inhibits motility, decreases cell death and increases cell proliferation in human glioblastoma cell lines. J Neurobiol 37:373–382. [DOI] [PubMed] [Google Scholar]
  • 21. Donato R (1991). Perspectives in S100 protein biology. Cell Calcium 12:713–726. [DOI] [PubMed] [Google Scholar]
  • 22. Engelkamp D, Schafer BW, Mattei MG, Erne P, Heizmann CW (1993). Six S100 genes are clustered on human chromosome 1q21: identification of two previously unreported calcium‐binding proteins S100D and S100E. Proc Natl Acad Sci USA 90:6547–6551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23. Europath Project, available in http://www.europath.imag.fr/EUROPATH/.
  • 24. Fan K (1982). S‐100 Protein synthesis in cultured glioma cells is G1‐phase of cell cycle dependent. Brain Res 237:498–503. [DOI] [PubMed] [Google Scholar]
  • 25. Filipek A, Puzianowska M, Cieslak B, Kuznicki J (1993). Calcyclin‐Ca2+‐binding protein homologous to glial S‐100B is present in neurones. NeuroReport 4:383–386. [DOI] [PubMed] [Google Scholar]
  • 26. Föhr UG, Heizmann CW, Engelkamp D, Schafer BW, Cox JA (1995). Purification and cation binding properties of the recombinant human S100 calcium‐binding protein A3, an EF‐hand motif protein with high affinity for zinc. J Biol Chem 270:21056–21061. [DOI] [PubMed] [Google Scholar]
  • 27. Folkman J (1995). Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1:27–31. [DOI] [PubMed] [Google Scholar]
  • 28. Forsyth PA, Shaw EG, Scheithauer BW, O'Fallon JR, Lay‐ton DD Jr, Katzmann JA (1993). Supratentorial pilocytic astrocytomas. A clinicopathologic, prognostic, and flow cytometric study of 51 patients. Cancer 72:1335–1342. [DOI] [PubMed] [Google Scholar]
  • 29. Franz C, Durussel I, Cox JA, Schäfer BW, Heizmann CW (1998). Binding of Ca2+ and Zn2+ to human nuclear S100A2 and mutant proteins. J Biol Chem 273:18826–18834. [DOI] [PubMed] [Google Scholar]
  • 30. Giannini G, Scheithauer BW (1997). Classification and grading of low‐grade astrocytic tumors in children. Brain Pathol 7:785–798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31. Glenney JR, Kindy MS, Zokas L (1989). Isolation of a new member of the S100 protein family: amino acid sequence, tissue, and subcellular distribution. J Cell Biol 108:569–578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32. Goldschmidt D, Decaestecker C, Berthe JV, Gordower L, Remmelink M, Danguy A, Pasteels JL, Salmon I, Kiss R (1996). The contribution of computer‐assistaged methods for histopathological classification of adipose tumors. Lab Invest 75:295–306. [PubMed] [Google Scholar]
  • 33. Haddad SH, Moore SA, Schelper RL, Goeken JA (1992). Vascular smooth muscle hyperplasia underlies the formation of glomeruloid vascular structures of glioblastoma multiforme. J Neuropathol Exp Neurol 51:488–492. [DOI] [PubMed] [Google Scholar]
  • 34. Heizmann CW, Braun K (1995). Calcium regulation by calcium‐binding proteins in neurodegenerative disorders. Neuroscience Intelligence Unit. RC Landes Company: Austin , USA , and Springer Verlag: Heidelberg , Germany . [Google Scholar]
  • 35. Heizmann CW, Cox JA (1998). New perspectives on S100 proteins: a multifunctional Ca2+‐, Zn2+‐ and Cu2+‐bind‐ing protein family. Biometals (in press). [DOI] [PubMed] [Google Scholar]
  • 36. Ho DM, Wong TT, Hsu CY, Ting LT, Chiang H (1998). MIB‐1 labeling index in nonpilocytic astrocytomas of childhood: a study of 101 cases. Cancer 82:2459–2466. [DOI] [PubMed] [Google Scholar]
  • 37. Huang JW, Ming Z, Shrestha P, Mori M, IIg E, Schafer BW, Heizmann CW (1996). Immunohistochemical evaluation of the Ca2+‐binding S‐100 proteins S‐100A1, S‐100A2, S‐100A4, S‐100A6 and S‐100B in salivary gland tumors. J Oral Pathol Med 25:547–555. [DOI] [PubMed] [Google Scholar]
  • 38. Humphrey PA, Gangarosa LM, Wong AJ, Archer GE, Lund‐Johansen M, Bjerkvig R, Laerum OD, Friedman HS, Bigner DD (1991). Deletion‐mutant epidermal growth factor receptor in human gliomas: effects of type II mutation on receptor function. Biochem Biophys Res Commun 178:1413–1420. [DOI] [PubMed] [Google Scholar]
  • 39. IIg EC, Schafer BW, Heizmann CW (1996). Expression pattern of S100 calcium‐binding proteins in human tumors. Int J Cancer 68:325–332. [DOI] [PubMed] [Google Scholar]
  • 40. Ishii N, Sawamura Y, Tada M, Daub DM, Janzer RC, Meagher‐Villemure M, De Tribolet N, Van Meir EG (1998). Absence of p53 gene mutations in a tumor panel representative of pilocytic astrocytoma diversity using a p53 functional assay. Int J Cancer 76:797–800. [DOI] [PubMed] [Google Scholar]
  • 41. Jen J, Harper W, Bigner SH, Bigner DD, Papadopoulos N, Markowitz S, Willsson JK, Kinzler KW, Vogelstein B (1994). Deletion of p16 and p15 genes in brain tumors. Cancer Res 54:6353–6358. [PubMed] [Google Scholar]
  • 42. Kayama T, Tominaga T, Yoshimoto T (1996). Management of pilocytic astrocytoma. Neurosurg Rev 19:217–220. [DOI] [PubMed] [Google Scholar]
  • 43. Kizawa K, Uchiwa H, Murakami U (1996). Highly‐expressed S100A3, a calcium‐binding protein, in human hair cuticle. Biochim Biophys Acta 1312:94–98. [DOI] [PubMed] [Google Scholar]
  • 44. Kleihues P, Burger PC, Scheithauer BW (1993). The new WHO classification of brain tumours. Brain Pathol 3:255–268. [DOI] [PubMed] [Google Scholar]
  • 45. Kleihues P, Burger PC, Scheithauer BW, eds. (1993). His‐tological typing of tumours of the central nervous system, World Health Organisation International Histological Classification of Tumours, 2nd Edition, Springer Verlag: Berlin . [Google Scholar]
  • 46. Kleihues P, Cavenee WK, eds (1997). Pathology and genetics of tumours of the nervous system. International Agency for Research on Cancer (IARC) Who Health Organisation. Oxford : Oxford Press. [Google Scholar]
  • 47. Kleihues P, Soylemezoglu F, Schauble B, Scheithauer BW, Burger PC (1995). Histopathology, classification, and grading of gliomas. GLIA 15: 211–221. [DOI] [PubMed] [Google Scholar]
  • 48. Kriajevska M, Tarabykina S, Bronstein I, Maitland N, Lomonosov M, Hansen K, Georgiev G, Lukanidin E (1998). Metastasis‐associated Mts1 (S100A4) protein modulates protein kinase C phosphorylation of the heavy chain of nonmuscle myosin. J Biol Chem 273:9852–9856. [DOI] [PubMed] [Google Scholar]
  • 49. Krieger MD, Gonzalez‐Gomez I, Levy ML, McComb JG (1997). Recurrence patterns and anaplastic change in a long‐term study of pilocytic astrocytomas. Pediatr Neurosurg 27:1–11. [DOI] [PubMed] [Google Scholar]
  • 50. Kriho VK, Yang HY, Moskal JR, Skalli O (1997). Keratin expression in astrocytomas: an immunofluorescent and biochemical reassessment. Virchows Arch 431:139–147. [DOI] [PubMed] [Google Scholar]
  • 51. Lakshmi MS, Parker C, Sherbet GV (1993). Metastasis associated MTS1 and NM23 genes affect tubulin polymerization in B16 melanomas: a possible mechanism of their regulation of metastatic behavior of tumors. Anti-cancer Res 13:299–304. [PubMed] [Google Scholar]
  • 52. Lee SW, Tomasetto C, Swisshelm K, Keyomarsi K, Sager R (1992). Down‐regulation of a member of the S100gene family in mammary carcinoma cells and reexpression by azadeoxycytidine treatment. Proc Natl Acad Sci USA 89:2504–2508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53. Litofsky NS, Hinton D, Raffel C (1994). The lack of a role for p53 in astrocytomas in pediatric patients. Neurosurgery 34:967–972. [DOI] [PubMed] [Google Scholar]
  • 54. Lloyd BH, Ruddell C, Rudland PS, Barraclough R (1996). S100A3 mRNA expression displays an inverse correlation to breast cancer progression. Biochem Soc Trans 24:340S. [DOI] [PubMed] [Google Scholar]
  • 55. Louis DN (1997). A molecular genetic model of astrocytoma histopathology. Brain Pathol 7:755–764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56. Marks A, Petsche D, O'Hanlon D, Kwong PC, Stead R, Dunn R, Baumal R, Liao SK (1990). 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 187:59–64. [DOI] [PubMed] [Google Scholar]
  • 57. McKeever PE, Ross DA, Strawderman MS, Brunberg JA, Greenberg HS, Junck L (1997). A comparison of the predictive power for survival in gliomas provided by MIB‐1, bromodeoxyuridine and proliferating cell nuclear antigen with histopathologic and clinical parameters. J Neuropatho. Exp Neurol 56:798–805. [PubMed] [Google Scholar]
  • 58. Millward TA, Heizmann CW, Schafer BW, Hemmings BA (1998). Calcium regulation of Ndr protein kinase mediated by S100 calcium‐binding proteins. EMBO J (in press). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59. Murphy LC, Murphy LJ, Tsuyuki D, Duckworth ML, Shiu R (1988). Cloning and characterization of a cDNA encoding a highly conserved, putative calcium binding protein, identified by an anti‐prolactin receptor antiserum. J Biol Chem 263:2397–2401. [PubMed] [Google Scholar]
  • 60. Patt S, Gries H, Giraldo M, Cervos‐Navarro J, Martin H, Janisch W, Brockmoller J (1996). p53 gene mutations in human astrocytic brain tumors including pilocytic astrocytomas. Hum Pathol 27:586–589. [DOI] [PubMed] [Google Scholar]
  • 61. Plate KH, Breier G, Risau W (1994). Molecular mechanisms of developmental and tumor angiogenesis. Brain Pathol 4:207–218. [DOI] [PubMed] [Google Scholar]
  • 62. Reeves RH, Yao J, Crowley MR, Buck S, Zhang X, Yarowsky P, Gearhart JD, Hilt DC (1994). Astrocytosis and axonal proliferation in the hippocampus of S100B transgenic mice. Proc Natl Acad Sci USA 91:5359–5363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 63. Revesz T, Alsanjari N, Darling JL, Scaravilli F, Lane DP, Thomas DG (1993). Proliferating cell nuclear antigen (PCNA): expression in samples of human astrocytic gliomas. Neuropathol Appl Neurobiol 19:152–158. [DOI] [PubMed] [Google Scholar]
  • 64. Robertson PL (1998). Pediatric brain tumors. Prim Care 25:323–339. [DOI] [PubMed] [Google Scholar]
  • 65. Rutka JT, Murakami M, Dirks PB, Hubbard SL, Becker LE, Fukuyama K, Jung S, Tsugu A, Matsuzawa K (1997). Role of glial filaments in cells and tumors of glial origin: A review. J Neurosurg 87:420–430. [DOI] [PubMed] [Google Scholar]
  • 66. Salmon I, Levivier M, Camby I, Rombaut K, Gras T, Pas‐teels JI, Brotchi J, Kiss R (1993). Assessment of nuclear size, nuclear DNA content and proliferation index in stereotaxic biopsies from brain tumours. Neuropathol Appl Neurobiol 19:507–518. [DOI] [PubMed] [Google Scholar]
  • 67. Salmon I, Rorive S, Camby I, Decaestecker C, Pirotte B, Rombaut K, Haot J, Pasteels JL, Brotchi J, Kiss R (1995). Stereotactic biopsies from astrocytic tumors: Diagnostic information contributed by the quantitative chromatin pattern description. Anal Quant Cytol Histol 17:332–343. [PubMed] [Google Scholar]
  • 68. Schäfer BW, Heizmann CW (1996). The S100 family of EF‐hand calcium‐binding proteins: functions and pathology. TIBS 21:134–140. [DOI] [PubMed] [Google Scholar]
  • 69. Saussez S, Marchant H, Nagy N, Decaestecker C, Hassid S, Jortay A, Schüring M, Gabius HJ, Danguy A, Salmon I, Kiss R (1998). Quantitative glycohistochemistry defines new prognostic markers in cancers of the oral cavity. Cancer 82:252–60. [PubMed] [Google Scholar]
  • 70. Schiffer D (1997). Brain Tumors. Biology, Pathology, and Clinical References. Springer‐Verlag. Berlin , Heidelberg , New York , p 58. [Google Scholar]
  • 71. Schmidt EE, Ichimura K, Reifenberger G, Collins VP (1994). CDKN2 (p16/MTS1) gene deletion or CDK4 amplification occurs in the majority of glioblastomas. Cancer Res 54:6321–6324. [PubMed] [Google Scholar]
  • 72. Selinfreund RH, Barger SW, Pledger WJ, Van Eldik LJ (1991). Neurotrophic protein S100B stimulates glial cell proliferation. Proc Natl Acad Sci USA 88:3554–3558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73. Selinfreund RH, Barger SW, Welsh MJ, Van Eldik LJ (1990). Antisense inhibition of glial S100B production results in alterations in cell morphology, cytoskeletal organization, and cell proliferation. J Cell Biol 111:2021–2028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74. Shaw EG, Scheithauer BW, O'Fallon JR (1997). Supratentorial gliomas: a comparative study by grade and histologic type. J Neurooncol 31:273–278. [DOI] [PubMed] [Google Scholar]
  • 75. Silbergeld DL, Chicoine MR (1997). Isolation and characterization of human malignant glioma cells from histologically normal brain. J Neurosurg 86:525–531. [DOI] [PubMed] [Google Scholar]
  • 76. Takenaga K, Nakamura Y, Sakiyama S (1997). 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 14:331–337. [DOI] [PubMed] [Google Scholar]
  • 77. Tohma Y, Gratas C, Van Meir EG, Desbaillets I, Tenan M, Tachibana O, Kleihues P, Ohgaki H (1998). Necrogenesis and Fas/APO‐1 (CD95) expression in primary (de novo) and secondary glioblastomas. J Neuropathol Exp Neurol 57:239–245. [DOI] [PubMed] [Google Scholar]
  • 78. VandenBerg SR (1992). Current diagnostic concepts of astrocytic tumors. J Neuropathol Exp Neurol 51:644–657. [DOI] [PubMed] [Google Scholar]
  • 79. von Deimling A, Louis DN, Wiestler OD (1995). Molecular pathways in the formation of gliomas. GLIA 15:328–338. [DOI] [PubMed] [Google Scholar]
  • 80. Walker DG, Duan W, Popovic EA, Kaye AH, Tomlinson FH, Lavin M (1995). Homozygous deletions of the multiple tumor suppressor gene 1 in the progression of human astrocytomas. Cancer Res 55:20–23. [PubMed] [Google Scholar]
  • 81. Weller M, Kleihues P, Dichgans J, Ohgaki H (1998). CD95 ligand: lethal weapon against malignant glioma Brain Pathol 8:285–293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82. Wesseling P, Van der Laak JAWM, Link M, Teepen HLJM, Ruiter DJ (1998). Quantitative analysis of microvascular changes in diffuse astrocytic neoplasms with increasing grade of malignancy. Hum Pathol 29:352–358. [DOI] [PubMed] [Google Scholar]
  • 83. Wicki R, Franz C, Scholl FA, Heizmann CW, Schafer BW (1997). Repression of the candidate tumor suppressor gene S100A2 in breast cancer is mediated by site‐specific hypermethylation. Cell Calcium 22:243–254. [DOI] [PubMed] [Google Scholar]
  • 84. Yamashita N, Kosaka K, IIg EC, Schafer BW, Heizmann CW, Kosaka T (1997). Selective association of S100A6 (calcyclin)‐immunoreactive astrocytes with the tangential migration pathway of subventricular zone cells in the rat. Brain Res 778:388–392. [DOI] [PubMed] [Google Scholar]
  • 85. Yamashita N, Kosaka K, IIg EC, Schafer BW, Heizmann CW, Kosaka T (1998). Distribution of a specific Ca2+‐binding protein of the S100 protein family, S100A6 (calcy‐clin), in subpopulations of neurons and glial cells of the dult rat nervous system. J Comp Neurol (in press). [PubMed] [Google Scholar]
  • 86. Zimmer DB, Cornwall EH, Landar A, Song W (1995). The S100 protein family: history, function and expression. Brain Res Bull 37:417–429. [DOI] [PubMed] [Google Scholar]

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