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The expression of SOX11, cyclin D1, cyclin D2, and cyclin D3 in B-cell lymphocytic proliferative diseases

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Abstract

SOX11 is mainly correlated with embryo neurogenesis and remodeling of tissues. D cyclins (cyclin D1, cyclin D2, and cyclin D3) work in cell transformation. We assessed the expression of SOX11, cyclin D1, cyclin D2, and cyclin D3 mRNA in 152 patients with B-cell lymphocytic proliferative diseases (B-LPD) using qRT-PCR and we detected SOX11 protein using immunohistochemistry in 15 B-LPD patients, to clarify the clinical significance of the four genes in B-LPD. Data showed the transcriptional levels of SOX11 and cyclin D1 were higher for the mantle cell lymphoma (MCL) samples compared with chronic lymphocytic leukemia (CLL), diffuse large B-cell lymphoma (DLBCL), hairy cell leukemia (HCL), splenic marginal zone lymphoma (SMZL), and healthy collators. The expression levels of cyclin D1 and cyclin D2 were both higher in DLBCL than in SMZL. The expression levels of the four genes were highly related to each other. Three of 4 MCL patients showed nuclear staining for SOX11, while other 11 B-LPD examples were negative. Furthermore, we also found the ZAP70-positive CLL patients had higher SOX11 expression levels than ZAP70-negative CLL patients. It was revealed that MCL patients have higher expression levels of SOX11 and cyclin D1 mRNA, specially expressed nuclear SOX11 protein.

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References

  1. Wegner M. From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res. 1999;27:1409–20.

    Article  PubMed  CAS  Google Scholar 

  2. Lefebvre V, Dumitriu B, Penzo-Méndez A, Han Y, Pallavi B. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol. 2007;39:2195–214.

    Article  PubMed  CAS  Google Scholar 

  3. Jay P, Gozé C, Marsollier C, et al. The human SOX11 gene: cloning, chromosomal assignment and tissue expression. Genomics. 1995;29:541–5.

    Article  PubMed  CAS  Google Scholar 

  4. Cheung M, Abu-Elmagd M, Clevers H, Scotting PJ. Roles of Sox4 in central nervous system development. Brain Res Mol Brain Res. 2000;79:180–91.

    Article  PubMed  CAS  Google Scholar 

  5. Ek S, Dictor M, Jerkeman M, Jirström K, Borrebaeck CA. Nuclear expression of the non B-cell lineage Sox11 transcription factor identifies mantle cell lymphoma. Blood. 2008;111:800–5.

    Article  PubMed  CAS  Google Scholar 

  6. Matsushime H, Quelle DE, Shurtleff SA, Shibuya M, Sherr CJ, Kato JY. D-type cyclin-dependent kinase activity in mammalian cells. Mol Cell Biol. 1994;14:2066–76.

    PubMed  CAS  Google Scholar 

  7. Bertoni F, Ponzoni M. The cellular origin of mantle cell lymphoma. Int J Biochem Cell Biol. 2007;39:1747–53.

    Article  PubMed  CAS  Google Scholar 

  8. Wlodarska I, Dierickx D, Vanhentenrijk V, et al. Translocations targeting CCND2, CCND3, and MYCN do occur in t(11;14)-negative mantle cell lymphomas. Blood. 2008;111:5683–90.

    Article  PubMed  CAS  Google Scholar 

  9. Meyerson HJ, MacLennan G, Husel W, et al. D cyclins in CD5+ B-cell lymphoproliferative disorders: cyclin D1 and cyclin D2 identify diagnostic groups and cyclin D1 correlates with ZAP-70 expression in chronic lymphocytic leukemia. Am J Clin Pathol. 2006;125:241–50.

    PubMed  CAS  Google Scholar 

  10. Swerdlow SH, Campo E, Harris NL, et al. WHO classification of tumours of haematopoietic and lymphoid tissues. 4th ed. Lyon: IARC Press; 2008.

    Google Scholar 

  11. Binet JL, Auquier A, Dighiero G, et al. A new prognostic classification of chronic lymphocytic leukemia derived from a multivariate survival analysis. Cancer. 1981;48:198–206.

    Article  PubMed  CAS  Google Scholar 

  12. Fernàndez V, Hartmann E, Ott G, Campo E, Rosenwald A. Pathogenesis of mantle-cell lymphoma: all oncogenic roads lead to dysregulation of cell cycle and DNA damage response pathways. J Clin Oncol. 2005;23:6364–9.

    Article  PubMed  Google Scholar 

  13. Yatabe Y, Suzuki R, Tobinai K, et al. Significance of cyclin D1 overexpression for the diagnosis of mantle cell lymphoma: a clinicopathologic comparison of cyclin D1-positive MCL and cyclin D1-negative MCL-like B-cell lymphoma. Blood. 2000;95:2253–61.

    PubMed  CAS  Google Scholar 

  14. Fu K, Weisenburger DD, Greiner TC, et al. Cyclin D1-negative mantle cell lymphoma: a clinicopathologic study based on gene expression profiling. Blood. 2005;106:4315–21.

    Article  PubMed  CAS  Google Scholar 

  15. Stacey DW. Cyclin D1 serves as a cell cycle regulatory switch in actively proliferating cells. Curr Opin Cell Biol. 2003;15:158–63.

    Article  PubMed  CAS  Google Scholar 

  16. Sinclair AH, Berta P, Palmer MS, et al. A gene from the human sex determining region encodes a protein with homology to a conserved DNA binding motif. Nature. 1990;346:240–4.

    Article  PubMed  CAS  Google Scholar 

  17. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev. 2006;20:3475–86.

    Article  PubMed  CAS  Google Scholar 

  18. Jankowski MP, Cornuet PK, McIlwrath S, Koerber HR, Albers KM. SRY-box containing gene 11 (Sox11) transcription factor is required for neuron survival and neurite growth. Neuroscience. 2006;143:501–14.

    Article  PubMed  CAS  Google Scholar 

  19. Chen YH, Gao J, Fan G, Peterson LC. Nuclear expression of sox11 is highly associated with mantle cell lymphoma but is independent of t(11;14)(q13;q32) in non-mantle cell B-cell neoplasms. Mod Pathol. 2010;23:105–12.

    Article  PubMed  CAS  Google Scholar 

  20. Mozos A, Royo C, Hartmann E, et al. SOX11 expression is highly specific for mantle cell lymphoma and identifies the cyclin D1-negative subtype. Haematologica. 2009;94:1555–62.

    Article  PubMed  CAS  Google Scholar 

  21. Fernàndez V, Salamero O, Espinet B, et al. Genomic and gene expression profiling defines indolent forms of mantle cell lymphoma. Cancer Res. 2010;70:1408–18.

    Article  PubMed  Google Scholar 

  22. Wang X, Asplund AC, Porwit A, et al. The subcellular Sox11 distribution pattern identifies subsets of mantle cell lymphoma: correlation to overall survival. Br J Haematol. 2008;143:248–52.

    Article  PubMed  Google Scholar 

  23. Quintanilla-Martinez L, Slotta-Huspenina J, Koch I, et al. Differential diagnosis of cyclin D2+ mantle cell lymphoma based on fluorescence in situ hybridization and quantitative real-time-PCR. Haematologica. 2009;94:1595–8.

    Article  PubMed  CAS  Google Scholar 

  24. Metcalf RA, Zhao S, Anderson MW, et al. Characterization of D-cyclin proteins in hematolymphoid neoplasms: lack of specificity of cyclin-D2 and D3 expression in lymphoma subtypes. Mod Pathol. 2010;23:420–33.

    Article  PubMed  CAS  Google Scholar 

  25. Watanuki J, Hatakeyama K, Sonoki T, et al. Bone marrow large B cell lymphoma bearing cyclin D3 expression: clinical, morphologic, immunophenotypic, and genotypic analyses of seven patients. Int J Hematol. 2009;90:217–25.

    Article  PubMed  CAS  Google Scholar 

  26. Schroers R, Griesinger F, Trümper L, et al. Combined analysis of ZAP-70 and CD38 expression as a predictor of disease progression in B-cell chronic lymphocytic leukemia. Leukemia. 2005;19:750–8.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by National Natural Science Foundation of China (30871104, 30971295, 30971296), Natural Science Foundation of Jiangsu Province (BK2010584), “Qing Lan” project of Jiangsu Province, and “Liu Da Ren Cai Gao Feng” of Jiangsu Province, University Doctoral Foundation of the Ministry of Education of China (20093234120007, 2009323411001), the Program for Development of Innovative Research Team in the First Affiliated Hospital of NJMU, and Provincial Initiative Program for Excellency Disciplines of Jiangsu Province.

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The authors report no conflicts of interest.

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Authors and Affiliations

  1. Department of Hematology, The First Affiliated Hospital of Nanjing Medical University, Jiangsu Province Hospital, 210029, Nanjing, China

    Xin Cao, Lei Fan, Cheng Fang, Dan-Xia Zhu, Hua-Jie Dong, Dong-Mei Wang, Yin-Hua Wang, Wei Xu & Jian-Yong Li

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  1. Xin Cao
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  2. Lei Fan
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  3. Cheng Fang
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  7. Yin-Hua Wang
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  8. Wei Xu
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Correspondence to Wei Xu.

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Cao, X., Fan, L., Fang, C. et al. The expression of SOX11, cyclin D1, cyclin D2, and cyclin D3 in B-cell lymphocytic proliferative diseases. Med Oncol 29, 1190–1196 (2012). https://doi.org/10.1007/s12032-011-9937-5

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  • DOI: https://doi.org/10.1007/s12032-011-9937-5

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