Cancer Letters
Volume 229, Issue 1 , Pages 135-148 , 8 November 2005

Increased expression of S100A6 is associated with decreased metastasis and inhibition of cell migration and anchorage independent growth in human osteosarcoma

  • Hue H. Luu

      Affiliations

    • Molecular Oncology Laboratory, Department of Surgery, The University of Chicago Medical Center, Chicago, IL, USA
    • ,
  • Lan Zhou

      Affiliations

    • Molecular Oncology Laboratory, Department of Surgery, The University of Chicago Medical Center, Chicago, IL, USA
    • Department of Biomedical Engineering, Chongqing University of Medical Sciences, Chongqing, China
    • ,
  • Rex C. Haydon

      Affiliations

    • Molecular Oncology Laboratory, Department of Surgery, The University of Chicago Medical Center, Chicago, IL, USA
    • ,
  • Andrea T. Deyrup

      Affiliations

    • Department of Pathology and Laboratory Medicine, Emory University, Atlanta, GA, USA
    • ,
  • Anthony G. Montag

      Affiliations

    • Molecular Oncology Laboratory, Department of Surgery, The University of Chicago Medical Center, Chicago, IL, USA
    • Department of Pathology, The University of Chicago Medical Center, Chicago, IL, USA
    • ,
  • Dezheng Huo

      Affiliations

    • Department of Health Studies, The University of Chicago, Chicago, IL, USA
    • ,
  • Robert Heck

      Affiliations

    • Department of Orthopaedic Surgery, Campbell Clinic, Germantown, TN, USA
    • ,
  • Claus W. Heizmann

      Affiliations

    • Division of Clinical Chemistry and Biochemistry, Department of Pediatrics, University of Zurich, Zurich, Switzerland
    • ,
  • Terrance D. Peabody

      Affiliations

    • Molecular Oncology Laboratory, Department of Surgery, The University of Chicago Medical Center, Chicago, IL, USA
    • ,
  • Michael A. Simon

      Affiliations

    • Molecular Oncology Laboratory, Department of Surgery, The University of Chicago Medical Center, Chicago, IL, USA
    • ,
  • Tong-Chuan He

      Affiliations

    • Molecular Oncology Laboratory, Department of Surgery, The University of Chicago Medical Center, Chicago, IL, USA
    • Corresponding Author InformationCorresponding author. Address: Molecular Oncology Laboratory, Department of Surgery, The University of Chicago Medical Center, 5841 South Maryland Avenue, MC3079, Chicago, IL 60637, USA. Tel.: +1 773 702 7169; fax: +1 773 834 4598.

Received 10 November 2004 ,Revised 27 January 2005 ,Accepted 12 February 2005.

References 

  1. Murphey MD, Robbin MR, McRae GA, Flemming DJ, Temple HT, Kransdorf MJ. The many faces of osteosarcoma. Radiographics. 1997;17:1205–1231
  2. Whelan JS. Osteosarcoma. Eur. J. Cancer. 1997;33:1611–1618discussion 1618–1619
  3. Bentzen SM, Poulsen HS, Kaae S, Jensen OM, Johansen H, Mouridsen HT, et al. Prognostic factors in osteosarcomas. A regression analysis. Cancer. 1988;62:194–202
  4. Davis AM, Bell RS, Goodwin PJ. Prognostic factors in osteosarcoma: a critical review. J. Clin. Oncol. 1994;12:423–431
  5. Link MP, Goorin AM, Miser AW, Green AA, Pratt CB, Belasco JB, et al. The effect of adjuvant chemotherapy on relapse-free survival in patients with osteosarcoma of the extremity. N. Engl. J. Med. 1986;314:1600–1606
  6. Ward WG, Mikaelian K, Dorey F, Mirra JM, Sassoon A, Holmes EC, et al. Pulmonary metastases of stage IIB extremity osteosarcoma and subsequent pulmonary metastases. J. Clin. Oncol. 1994;12:1849–1858
  7. Kaste SC, Pratt CB, Cain AM, Jones-Wallace DJ, Rao BN. Metastases detected at the time of diagnosis of primary pediatric extremity osteosarcoma at diagnosis: imaging features. Cancer. 1999;86:1602–1608
  8. Yonemoto T, Tatezaki S, Ishii T, Satoh T, Kimura H, Iwai N. Prognosis of osteosarcoma with pulmonary metastases at initial presentation is not dismal. Clin. Orthop. 1998;194–199
  9. Ferguson WS, Goorin AM. Current treatment of osteosarcoma. Cancer Invest. 2001;19:292–315
  10. Letson GD, Muro-Cacho CA. Genetic and molecular abnormalities in tumors of the bone and soft tissues. Cancer Control. 2001;8:239–251
  11. Ragland BD, Bell WC, Lopez RR, Siegal GP. Cytogenetics and molecular biology of osteosarcoma. Lab. Invest. 2002;82:365–373
  12. Fuchs B, Pritchard DJ. Etiology of osteosarcoma. Clin. Orthop. 2002;40–52
  13. Bridge JA, Nelson M, McComb E, McGuire MH, Rosenthal H, Vergara G, et al. Cytogenetic findings in 73 osteosarcoma specimens and a review of the literature. Cancer Genet. Cytogenet. 1997;95:74–87
  14. Forus A, Berner JM, Meza-Zepeda LA, Saeter G, Mischke D, Fodstad O, et al. Molecular characterization of a novel amplicon at 1q21-q22 frequently observed in human sarcomas. Br. J. Cancer. 1998;78:495–503
  15. Ozaki T, Schaefer KL, Wai D, Buerger H, Flege S, Lindner N, et al. Genetic imbalances revealed by comparative genomic hybridization in osteosarcomas. Int. J. Cancer. 2002;102:355–365
  16. Schafer BW, Heizmann CW. The S100 family of EF-hand calcium-binding proteins: functions and pathology. Trends Biochem. Sci. 1996;21:134–140
  17. Lewit-Bentley A, Rety S. EF-hand calcium-binding proteins. Curr. Opin. Struct. Biol. 2000;10:637–643
  18. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int. J. Biochem. Cell Biol. 2001;33:637–668
  19. Heizmann CW, Fritz G, Schafer BW. S100 proteins: structure, functions and pathology. Front. Biosci. 2002;7:d1356–d1368
  20. Marenholz I, Heizmann CW, Fritz G. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem. Biophys. Res. Commun. 2004;322:1111–1122
  21. Moore BW. A soluble protein characteristic of the nervous system. Biochem. Biophys. Res. Commun. 1965;19:739–744
  22. Mani RS, McCubbin WD, Kay CM. Calcium-dependent regulation of caldesmon by an 11-kDa smooth muscle calcium-binding protein, caltropin. Biochemistry. 1992;31:11896–11901
  23. Sorci G, Agneletti AL, Bianchi R, Donato R. Association of S100B with intermediate filaments and microtubules in glial cells. Biochim. Biophys. Acta. 1998;1448:277–289
  24. Garbuglia M, Verzini M, Sorci G, Bianchi R, Giambanco I, Agneletti AL, et al. The calcium-modulated proteins, S100A1 and S100B, as potential regulators of the dynamics of type III intermediate filaments. Braz. J. Med. Biol. Res. 1999;32:1177–1185
  25. Golitsina NL, Kordowska J, Wang CL, Lehrer SS. Ca2+-dependent binding of calcyclin to muscle tropomyosin. Biochem. Biophys. Res. Commun. 1996;220:360–365
  26. Garbuglia M, Verzini M, Donato R. Annexin VI binds S100A1 and S100B and blocks the ability of S100A1 and S100B to inhibit desmin and GFAP assemblies into intermediate filaments. Cell Calcium. 1998;24:177–191
  27. Maelandsmo GM, Florenes VA, Mellingsaeter T, Hovig E, Kerbel RS, Fodstad O. Differential expression patterns of S100A2, S100A4 and S100A6 during progression of human malignant melanoma. Int. J. Cancer. 1997;74:464–469
  28. Lauriola L, Michetti F, Maggiano N, Galli J, Cadoni G, Schafer BW, et al. Prognostic significance of the Ca(2+) binding protein S100A2 in laryngeal squamous-cell carcinoma. Int. J. Cancer. 2000;89:345–349
  29. Liu D, Rudland PS, Sibson DR, Platt-Higgins A, Barraclough R. Expression of calcium-binding protein S100A2 in breast lesions. Br. J. Cancer. 2000;83:1473–1479
  30. El-Rifai W, Moskaluk CA, Abdrabbo MK, Harper J, Yoshida C, Riggins GJ, et al. Gastric cancers overexpress S100A calcium-binding proteins. Cancer Res. 2002;62:6823–6826
  31. Kimura K, Endo Y, Yonemura Y, Heizmann CW, Schafer BW, Watanabe Y, et al. Clinical significance of S100A4 and E-cadherin-related adhesion molecules in non-small cell lung cancer. Int. J. Oncol. 2000;16:1125–1131
  32. Pedersen KB, Nesland JM, Fodstad O, Maelandsmo GM. Expression of S100A4, E-cadherin, alpha- and beta-catenin in breast cancer biopsies. Br. J. Cancer. 2002;87:1281–1286
  33. Takenaga K. Suppression of metastasis-associated S100A4 gene expression by gamma- interferon in human colon adenocarcinoma cells. Br. J. Cancer. 1999;80:127–132
  34. Ninomiya I, Ohta T, Fushida S, Endo Y, Hashimoto T, Yagi M, et al. Increased expression of S100A4 and its prognostic significance in esophageal squamous cell carcinoma. Int. J. Oncol. 2001;18:715–720
  35. Ben-Izhak O, Stark P, Levy R, Bergman R, Lichtig C. Epithelial markers in malignant melanoma. A study of primary lesions and their metastases. Am. J. Dermatopathol. 1994;16:241–246
  36. Ilg EC, Schafer BW, Heizmann CW. Expression pattern of S100 calcium-binding proteins in human tumors. Int. J. Cancer. 1996;68:325–332
  37. Barrett AW, Scully C. S100 protein in oral biology and pathology. J. Oral. Pathol. Med. 1994;23:433–440
  38. Mathisen B, Lindstad RI, Hansen J, El-Gewely SA, Maelandsmo GM, Hovig E, et al. S100A4 regulates membrane induced activation of matrix metalloproteinase-2 in osteosarcoma cells. Clin. Exp. Metastasis. 2003;20:701–711
  39. Fullen DR, Reed JA, Finnerty B, McNutt NS. S100A6 expression in fibrohistiocytic lesions. J. Cutan. Pathol. 2001;28:229–234
  40. Haydon RC, Deyrup A, Ishikawa A, Heck R, Jiang W, Zhou L, et al. Cytoplasmic and/or nuclear accumulation of the beta-catenin protein is a frequent event in human osteosarcoma. Int. J. Cancer. 2002;102:338–342
  41. Deyrup AT, Haydon RC, Huo D, Ishikawa A, Peabody TD, He TC, et al. Myoid differentiation and prognosis in adult pleomorphic sarcomas of the extremity: an analysis of 92 cases. Cancer. 2003;98:805–813
  42. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc. Natl Acad. Sci. USA. 1998;95:2509–2514
  43. Peng Y, Kang Q, Luo Q, Jiang W, Si W, Liu BA, et al. Inhibitor of DNA binding/differentiation helix-loop-helix proteins mediate bone morphogenetic protein-induced osteoblast differentiation of mesenchymal stem cells. J. Biol. Chem. 2004;279:32941–32949
  44. Luo Q, Kang Q, Si W, Jiang W, Park JK, Peng Y, et al. Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J. Biol. Chem. 2004;279:55958–55968
  45. Muramatsu Y, Kamegai A, Shiba T, Shrestha P, Takai Y, Mori M, et al. Histochemical characteristics of calcium binding S100 proteins and bone morphogenetic proteins in chondro-osseous tumors. Oncol. Rep. 1997;49–53
  46. Komatsu K, Kobune-Fujiwara Y, Andoh A, Ishiguro S, Hunai H, Suzuki N, et al. Increased expression of S100A6 at the invading fronts of the primary lesion and liver metastasis in patients with colorectal adenocarcinoma. Br. J. Cancer. 2000;83:769–774
  47. Komatsu K, Murata K, Kameyama M, Ayaki M, Mukai M, Ishiguro S, et al. Expression of S100A6 and S100A4 in matched samples of human colorectal mucosa, primary colorectal adenocarcinomas and liver metastases. Oncology. 2002;63:192–200
  48. Rhim JS, Putman DL, Arnstein P, Huebner RJ, McAllister RM. Characterization of human cells transformed in vitro by N-methyl-N′-nitro-N-nitrosoguanidine. Int. J. Cancer. 1977;19:505–510
  49. Hensler PJ, Annab LA, Barrett JC, Pereira-Smith OM. A gene involved in control of human cellular senescence on human chromosome 1q. Mol. Cell. Biol. 1994;14:2291–2297
  50. Rehman I, Cross SS, Azzouzi AR, Catto JW, Deloulme JC, Larre S, et al. S100A6 (Calcyclin) is a prostate basal cell marker absent in prostate cancer and its precursors. Br. J. Cancer. 2004;91:739–744
  51. Breen EC, Tang K. Calcyclin (S100A6) regulates pulmonary fibroblast proliferation, morphology, and cytoskeletal organization in vitro. J. Cell. Biochem. 2003;88:848–854
  52. Pawlak G, Helfman DM. Cytoskeletal changes in cell transformation and tumorigenesis. Curr. Opin. Genet. Dev. 2001;11:41–47
  53. Prasad GL, Fuldner RA, Cooper HL. Expression of transduced tropomyosin 1 cDNA suppresses neoplastic growth of cells transformed by the ras oncogene. Proc. Natl Acad. Sci. USA. 1993;90:7039–7043
  54. Prasad GL, Masuelli L, Raj MH, Harindranath N. Suppression of src-induced transformed phenotype by expression of tropomyosin-1. Oncogene. 1999;18:2027–2031
  55. Janssen RA, Mier JW. Tropomyosin-2 cDNA lacking the 3′ untranslated region riboregulator induces growth inhibition of v-Ki-ras-transformed fibroblasts. Mol. Biol. Cell. 1997;8:897–908
  56. Tu Q, Pi M, Quarles LD. Calcyclin mediates serum response element (SRE) activation by an osteoblastic extracellular cation-sensing mechanism. J. Bone Miner. Res. 2003;18:1825–1833
  57. Hwang R, Lee EJ, Kim MH, Li SZ, Jin YJ, Rhee Y, et al. Calcyclin, a Ca2+ ion-binding protein, contributes to the anabolic effects of simvastatin on bone. J. Biol. Chem. 2004;279:21239–21247
  58. Komatsu K, Andoh A, Ishiguro S, Suzuki N, Hunai H, Kobune-Fujiwara Y, et al. Increased expression of S100A6 (Calcyclin), a calcium-binding protein of the S100 family, in human colorectal adenocarcinomas. Clin. Cancer Res. 2000;6:172–177
  59. Bielack SS, Kempf-Bielack B, Delling G, Exner GU, Flege S, Helmke K, et al. Prognostic factors in high-grade osteosarcoma of the extremities or trunk: an analysis of 1,702 patients treated on neoadjuvant cooperative osteosarcoma study group protocols. J. Clin. Oncol. 2002;20:776–790

PII: S0304-3835(05)00175-8

doi: 10.1016/j.canlet.2005.02.015

Cancer Letters
Volume 229, Issue 1 , Pages 135-148 , 8 November 2005

Article Tools

* Image Usage & Resolution