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Cellular Oncology

, Volume 41, Issue 2, pp 141–157 | Cite as

p53 expression and subcellular survivin localization improve the diagnosis and prognosis of patients with diffuse astrocytic tumors

  • Roberta Soares Faccion
  • Paula Sabbo Bernardo
  • Giselle Pinto Faria de Lopes
  • Leonardo Soares Bastos
  • Cristina Lordello Teixeira
  • José Antonio de Oliveira
  • Priscila Valverde Fernandes
  • Luiz Gustavo Dubois
  • Leila Chimelli
  • Raquel Ciuvalschi Maia
Original Paper

Abstract

Purpose

Diffuse astrocytic tumors are the most frequently occurring primary central nervous system (CNS) tumors. Their histological sub-classification into diffuse astrocytoma (DA), anaplastic astrocytoma (AA) and glioblastoma (GB) is challenging and the available prognostic factors are limited to age and tumor subtype. Biomarkers that may improve the histological sub-classification and/or serve as prognostic factors are, therefore, urgently needed. The relationship between survivin and p53 in diffuse astrocytic tumor progression and survival is currently unclear. Here, we aimed to assess the relevance of these proteins in the accuracy of the histological sub-classification of these tumors and their respective treatment responses.

Methods

One hundred and thirty-three formalin-fixed paraffin-embedded diffuse astrocytic tumor samples were included. The tumor samples were histologically reviewed and subsequently assessed for p53 and survivin expression and the presence of the IDH R132H mutation by immunohistochemistry. p53 expression levels and survivin subcellular localization patterns were correlated with histological classification and clinical outcome.

Results

We found that age and histological subtype were the only features with a prognostic impact. In addition, we found that high p53 expression levels and a nuclear survivin localization correlated with the AA subtype, whereas cytoplasmic survivin localization correlated with the GB subtype. We also found that patients carrying tumors with a high cytoplasmic survivin expression, a high nuclear survivin expression or a high p53 expression, and who did not receive radiotherapy, exhibited poorer short-term and long-term overall survival rates.

Conclusions

Our data suggest that subcellular survivin localization and p53 expression may be employed as valuable tools to improve the accuracy of the histological sub-classification of diffuse astrocytic tumors. Patients whose tumors overexpress these proteins may benefit from radiotherapy, irrespective age and/or histological classification.

Keywords

Astrocytic tumors Survivin p53 Subcellular localization Diagnosis Prognosis 

Notes

Acknowledgements

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação para Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ), Instituto Nacional de Ciência e Tecnologia (INCT) para Controle do Câncer and the Programa de Oncobiologia (Fundação do Câncer and UFRJ). PSB was first supported by a PhD scholarship from FAPERJ and then by a post-doctoral fellowship from the Ministério da Saúde/Instituto Nacional de Câncer. RSF was first supported by a PhD scholarship from CNPq and then by a post-doctoral fellowship from the Ministério da Saúde/Instituto Nacional de Câncer. We would like to thank all patients enrolled in the study and the physicians from the Neurosurgery Service for their participation. We also acknowledge Dr. Mauricio G S Costa from Instituto Oswaldo Cruz (FIOCRUZ) for his help with the artwork.

This work was funded by the Instituto Nacional de Ciência e Tecnologia para o Controle do Câncer [Award number: INCT-573806/2008-0 (FAPERJ-E29/110.278/2010, CNPq-306141/2010-8)], the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (Award number: E-26/103.140/2011) and the Programa de Oncobiologia (Award number: Programa de Oncobiologia/2016 UFRJ/FAF).

Compliance with ethical standards

Conflict of interest

The authors declare to have no conflict of interest.

Research involving human participants and/or animals

The authors declare that our Institutional Ethics Committee approved this study (under the registries 46/04 and 114/08), which was conducted in agreement with the recommendations of the Helsinki Declaration. For retrospective studies informed consent is not required.

Supplementary material

13402_2017_361_MOESM1_ESM.docx (20 kb)
ESM 1 (DOCX 19 kb)

References

  1. 1.
    Q.T. Ostrom, H. Gittleman, J. Fulop, M. Liu, R. Blanda, C. Kromer, Y. Wolinsky, C. Kruchko, J.S. Barnholtz-Sloan, CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the United States in 2008-2012. Neuro-Oncology 17(Suppl 4), iv1–iv62 (2015).  https://doi.org/10.1093/neuonc/nov189 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    D.N. Louis, H. Ohgaki, O.D. Wiestler, W.K. Cavenee, P.C. Burger, A. Jouvet, B.W. Scheithauer, P. Kleihues, The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114, 97–109 (2007).  https://doi.org/10.1007/s00401-007-0243-4
  3. 3.
    D.N. Louis, A. Perry, G. Reifenberger, A. von Deimling, D. Figarella-Branger, W.K. Cavenee, H. Ohgaki, O.D. Wiestler, P. Kleihues, D.W. Ellison, The 2016 World Health Organization classification of tumors of the central nervous system: A summary. Acta Neuropathol 131, 803–820 (2016).  https://doi.org/10.1007/s00401-016-1545-1
  4. 4.
    K. Ichimura, Y. Narita, C.E. Hawkins, Diffusely infiltrating astrocytomas: Pathology, molecular mechanisms and markers. Acta Neuropathol 129, 789–808 (2015).  https://doi.org/10.1007/s00401-015-1439-7
  5. 5.
    M. Weller, M. van den Bent, K. Hopkins, J.C. Tonn, R. Stupp, A. Falini, E. Cohen-Jonathan-Moyal, D. Frappaz, R. Henriksson, C. Balana, O. Chinot, Z. Ram, G. Reifenberger, R. Soffietti, W. Wick, G. European Association for Neuro-Oncology Task Force. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma, Lancet Oncol 15, e395–e403 (2014).  https://doi.org/10.1016/S1470-2045(14)70011-7
  6. 6.
    R. Soffietti, B.G. Baumert, L. Bello, A. von Deimling, H. Duffau, M. Frenay, W. Grisold, R. Grant, F. Graus, K. Hoang-Xuan, M. Klein, B. Melin, J. Rees, T. Siegal, A. Smits, R. Stupp, W. Wick, S. European federation of neurological guidelines on management of low-grade gliomas: Report of an EFNS-EANO task force. Eur J Neurol 17, 1124–1133 (2010).  https://doi.org/10.1111/j.1468-1331.2010.03151.x
  7. 7.
    R. Stupp, W.P. Mason, M.J. van den Bent, M. Weller, B. Fisher, M.J. Taphoorn, K. Belanger, A.A. Brandes, C. Marosi, U. Bogdahn, J. Curschmann, R.C. Janzer, S.K. Ludwin, T. Gorlia, A. Allgeier, D. Lacombe, J.G. Cairncross, E. Eisenhauer, R.O. Mirimanoff, R. European organisation for the treatment of cancer brain, G. Radiotherapy and G. National Cancer Institute of Canada clinical trials. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352, 987–996 (2005).  https://doi.org/10.1056/NEJMoa043330
  8. 8.
    D.N. Louis, A. Perry, P. Burger, D.W. Ellison, G. Reifenberger, A. von Deimling, K. Aldape, D. Brat, V.P. Collins, C. Eberhart, D. Figarella-Branger, G.N. Fuller, F. Giangaspero, C. Giannini, C. Hawkins, P. Kleihues, A. Korshunov, J.M. Kros, M. Beatriz Lopes, H.K. Ng, H. Ohgaki, W. Paulus, T. Pietsch, M. Rosenblum, E. Rushing, F. Soylemezoglu, O. Wiestler, P. Wesseling and N.-H. International Society  of Neuropathology--Haarlem consensus guidelines for nervous system tumor classification and grading. Brain Pathol 24, 429–435 (2014).  https://doi.org/10.1111/bpa.12171
  9. 9.
    N. Cancer Genome Atlas Research, Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455, 1061–1068 (2008).  https://doi.org/10.1038/nature07385
  10. 10.
    E. Gillet, A. Alentorn, B. Doukoure, E. Mundwiller, H.F. van Thuijl, J.C. Reijneveld, J.A. Medina, A. Liou, Y. Marie, K. Mokhtari, K. Hoang-Xuan, M. Sanson, J.Y. Delattre and A. Idbaih. TP53 and p53 statuses and their clinical impact in diffuse low grade gliomas. J Neuro-Oncol 118, 131–139 (2014).  https://doi.org/10.1007/s11060-014-1407-4
  11. 11.
    Y.H. Kim, S. Nobusawa, M. Mittelbronn, W. Paulus, B. Brokinkel, K. Keyvani, U. Sure, K. Wrede, Y. Nakazato, Y. Tanaka, A. Vital, L. Mariani, R. Stawski, T. Watanabe, U. De Girolami, P. Kleihues, H. Ohgaki, Molecular classification of low-grade diffuse gliomas. Am J Pathol 177, 2708–2714 (2010).  https://doi.org/10.2353/ajpath.2010.100680
  12. 12.
    X.Y. Liu, N. Gerges, A. Korshunov, N. Sabha, D.A. Khuong-Quang, A.M. Fontebasso, A. Fleming, D. Hadjadj, J. Schwartzentruber, J. Majewski, Z. Dong, P. Siegel, S. Albrecht, S. Croul, D.T. Jones, M. Kool, M. Tonjes, G. Reifenberger, D. Faury, G. Zadeh, S. Pfister, N. Jabado, Frequent ATRX mutations and loss of expression in adult diffuse astrocytic tumors carrying IDH1/IDH2 and TP53 mutations. Acta Neuropathol 124, 615–625 (2012).  https://doi.org/10.1007/s00401-012-1031-3
  13. 13.
    Y. Okamoto, P.L. Di Patre, C. Burkhard, S. Horstmann, B. Jourde, M. Fahey, D. Schuler, N.M. Probst-Hensch, M.G. Yasargil, Y. Yonekawa, U.M. Lutolf, P. Kleihues, H. Ohgaki, Population-based study on incidence, survival rates, and genetic alterations of low-grade diffuse astrocytomas and oligodendrogliomas. Acta Neuropathol 108, 49–56 (2004).  https://doi.org/10.1007/s00401-004-0861-z
  14. 14.
    R. Ogura, Y. Tsukamoto, M. Natsumeda, M. Isogawa, H. Aoki, T. Kobayashi, S. Yoshida, K. Okamoto, H. Takahashi, Y. Fujii, A. Kakita, Immunohistochemical profiles of IDH1, MGMT and P53: Practical significance for prognostication of patients with diffuse gliomas. Neuropathology 35, 324–335 (2015).  https://doi.org/10.1111/neup.12196
  15. 15.
    K. Wang, Y.Y. Wang, J. Ma, J.F. Wang, S.W. Li, T. Jiang, J.P. Dai, Prognostic value of MGMT promoter methylation and TP53 mutation in glioblastomas depends on IDH1 mutation. Asian Pac J Cancer Prev 15, 10893–10898 (2014)Google Scholar
  16. 16.
    A. Mirza, M. McGuirk, T.N. Hockenberry, Q. Wu, H. Ashar, S. Black, S.F. Wen, L. Wang, P. Kirschmeier, W.R. Bishop, L.L. Nielsen, C.B. Pickett, S. Liu, Human survivin is negatively regulated by wild-type p53 and participates in p53-dependent apoptotic pathway. Oncogene 21, 2613–2622 (2002).  https://doi.org/10.1038/sj.onc.1205353
  17. 17.
    G. Ambrosini, C. Adida, D.C. Altieri, A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 3, 917–921 (1997).  https://doi.org/10.1038/nm0897-917
  18. 18.
    D.P. Banks, J. Plescia, D.C. Altieri, J. Chen, S.H. Rosenberg, H. Zhang, S.C. Ng, Survivin does not inhibit caspase-3 activity. Blood 96, 4002–4003 (2000)Google Scholar
  19. 19.
    S.K. Knauer, W. Mann, R.H. Stauber, Survivin's dual role: An expert's view. Cell Cycle 6, 518–521 (2007).  https://doi.org/10.4161/cc.6.5.3902
  20. 20.
    R.H. Stauber, W. Mann, S.K. Knauer, Nuclear and cytoplasmic survivin: Molecular mechanism, prognostic, and therapeutic potential. Cancer Res 67, 5999–6002 (2007).  https://doi.org/10.1158/0008-5472.CAN-07-0494
  21. 21.
    F. Li, J. Yang, N. Ramnath, M.M. Javle, D. Tan, Nuclear or cytoplasmic expression of survivin: What is the significance? Int J Cancer 114, 509–512 (2005).  https://doi.org/10.1002/ijc.20768
  22. 22.
    S. Lv, C. Dai, Y. Liu, R. Shi, Z. Tang, M. Han, R. Bian, B. Sun, R. Wang, The impact of survivin on prognosis and clinicopathology of glioma patients: A systematic meta-analysis. Mol Neurobiol 51, 1462–1467 (2015).  https://doi.org/10.1007/s12035-014-8823-5
  23. 23.
    L. O'Driscoll, R. Linehan, M. Clynes, Survivin: Role in normal cells and in pathological conditions. Curr Cancer Drug Targets 3, 131–152 (2003).  https://doi.org/10.2174/1568009033482038
  24. 24.
    J.S. Chu, J.Y. Shew, C.S. Huang, Immunohistochemical analysis of survivin expression in primary breast cancers. J Formos Med Assoc 103, 925–931 (2004)Google Scholar
  25. 25.
    A. Chakravarti, E. Noll, P.M. Black, D.F. Finkelstein, D.M. Finkelstein, N.J. Dyson, J.S. Loeffler, Quantitatively determined survivin expression levels are of prognostic value in human gliomas. J Clin Oncol 20, 1063–1068 (2002).  https://doi.org/10.1200/JCO.2002.20.4.1063
  26. 26.
    Y. Gao, L. Li, L. Song, Expression of p16 and survivin in gliomas and their correlation with cell proliferation. Oncol Lett 10, 301–306 (2015).  https://doi.org/10.3892/ol.2015.3180
  27. 27.
    Y. Kajiwara, F. Yamasaki, S. Hama, K. Yahara, H. Yoshioka, K. Sugiyama, K. Arita, K. Kurisu, Expression of survivin in astrocytic tumors: Correlation with malignant grade and prognosis. Cancer 97, 1077–1083 (2003).  https://doi.org/10.1002/cncr.11122
  28. 28.
    T. Sasaki, M.B. Lopes, G.R. Hankins, G.A. Helm, Expression of survivin, an inhibitor of apoptosis protein, in tumors of the nervous system. Acta Neuropathol 104, 105–109 (2002).  https://doi.org/10.1007/s00401-002-0532-x
  29. 29.
    R.K. Varughese, S.H. Torp, Survivin and gliomas: A literature review. Oncol Lett 12, 1679–1686 (2016).  https://doi.org/10.3892/ol.2016.4867
  30. 30.
    K. Shirai, Y. Suzuki, K. Oka, S.E. Noda, H. Katoh, Y. Suzuki, J. Itoh, H. Itoh, S. Ishiuchi, H. Sakurai, M. Hasegawa, T. Nakano, Nuclear survivin expression predicts poorer prognosis in glioblastoma. J Neuro-Oncol 9 3, 353–358 (2009).  https://doi.org/10.1007/s11060-008-9720-4
  31. 31.
    T. Saito, M.T. Arifin, S. Hama, Y. Kajiwara, K. Sugiyama, F. Yamasaki, T. Hidaka, K. Arita, K. Kurisu, Survivin subcellular localization in high-grade astrocytomas: Simultaneous expression in both nucleus and cytoplasm is negative prognostic marker. J Neuro-Oncol 82, 193–198 (2007).  https://doi.org/10.1007/s11060-006-9267-1
  32. 32.
    D. Xie, Y.X. Zeng, H.J. Wang, J.M. Wen, Y. Tao, J.S. Sham, X.Y. Guan, Expression of cytoplasmic and nuclear Survivin in primary and secondary human glioblastoma. Br J Cancer 94, 108–114 (2006).  https://doi.org/10.1038/sj.bjc.6602904
  33. 33.
    R. Rathore, J.E. McCallum, E. Varghese, A.M. Florea, D. Busselberg, Overcoming chemotherapy drug resistance by targeting inhibitors of apoptosis proteins (IAPs). Apoptosis 22, 898–919 (2017).  https://doi.org/10.1007/s10495-017-1375-1
  34. 34.
    R.S. Faccion, L.M. Rezende, O. Romano Sde, S. Bigni Rde, G.L. Mendes, R.C. Maia, Centroblastic diffuse large B cell lymphoma displays distinct expression pattern and prognostic role of apoptosis resistance related proteins. Cancer Investig 30, 404–414 (2012).  https://doi.org/10.3109/07357907.2012.672844
  35. 35.
    F.S. Pardo, D.W. Hsu, R. Zeheb, J.T. Efird, P.G. Okunieff and D.M. Malkin. Mutant, wild type, or overall p53 expression: Freedom from clinical progression in tumours of astrocytic lineage. Br J Cancer 91, 1678–1686 (2004). l  https://doi.org/10.1038/sj.bjc.6602161
  36. 36.
    R.S. Faccion, R.M. Ferreira, M.F. Grabois, T.C. Fonseca, J.A. de Oliveira, R.C. Maia, Lack of prognostic significance of survivin in pediatric medulloblastoma. Pathol Oncol Res 17, 899–908 (2011).  https://doi.org/10.1007/s12253-011-9401-z
  37. 37.
    R Core Team, (R Foundation for Statistical Computing, Vienna, 2015)Google Scholar
  38. 38.
    D.R. Cox, Regression models and life-tables. J R Stat Soc Ser B Methodol 34, 187–220 (1972)Google Scholar
  39. 39.
    P.N. McCullagh, John A. ed., Generalized linear models, Chapters 4 and 5, Second ed. (CRC Press, Boca Raton, 1989)Google Scholar
  40. 40.
    T. Mesti, J. Ocvirk, Malignant gliomas: Old and new systemic treatment approaches. Radiol Oncol 50, 129–138 (2016).  https://doi.org/10.1515/raon-2015-0003
  41. 41.
    M.S. Waitkus, B.H. Diplas, H. Yan, Isocitrate dehydrogenase mutations in gliomas. Neuro-Oncology 18, 16–26 (2016).  https://doi.org/10.1093/neuonc/nov136
  42. 42.
    A.L. Cohen, S.L. Holmen, H. Colman, IDH1 and IDH2 mutations in gliomas. Curr Neurol Neurosci Rep 13, 345 (2013).  https://doi.org/10.1007/s11910-013-0345-4
  43. 43.
    C. Calatozzolo, M. Gelati, E. Ciusani, F.L. Sciacca, B. Pollo, L. Cajola, C. Marras, A. Silvani, L. Vitellaro-Zuccarello, D. Croci, A. Boiardi, A. Salmaggi, Expression of drug resistance proteins Pgp, MRP1, MRP3, MRP5 and GST-pi in human glioma. J Neuro-Oncol 74, 113–121 (2005).  https://doi.org/10.1007/s11060-004-6152-7
  44. 44.
    D.S. Tews, A. Nissen, C. Kulgen, A.K. Gaumann, Drug resistance-associated factors in primary and secondary glioblastomas and their precursor tumors. J Neuro-Oncol 50, 227–237 (2000).  https://doi.org/10.1023/A:1006491405010
  45. 45.
    F.F. Angileri, M. Aguennouz, A. Conti, D. La Torre, S. Cardali, R. Crupi, C. Tomasello, A. Germano, G. Vita, F. Tomasello, Nuclear factor-kappaB activation and differential expression of survivin and Bcl-2 in human grade 2-4 astrocytomas. Cancer 112, 2258–2266 (2008).  https://doi.org/10.1002/cncr.23407
  46. 46.
    M. Seifert, M. Garbe, B. Friedrich, M. Mittelbronn, B. Klink, Comparative transcriptomics reveals similarities and differences between astrocytoma grades. BMC Cancer 15, 952 (2015).  https://doi.org/10.1186/s12885-015-1939-9
  47. 47.
    C. Lopez-Gines, L. Navarro, L. Munoz-Hidalgo, E. Buso, J.M. Morales, R. Gil-Benso, M. Gregori-Romero, J. Megias, P. Roldan, R. Segura-Sabater, J.M. Almerich-Silla, D. Monleon, M. Cerda-Nicolas, Association between epidermal growth factor receptor amplification and ADP-ribosylation factor 1 methylation in human glioblastoma. Cell Oncol 40, 389–399 (2017).  https://doi.org/10.1007/s13402-017-0329-5
  48. 48.
    D. Matias, J. Balca-Silva, L.G. Dubois, B. Pontes, V.P. Ferrer, L. Rosario, A. do Carmo, J. Echevarria-Lima, A.B. Sarmento-Ribeiro, M.C. Lopes, V. Moura-Neto, Dual treatment with shikonin and temozolomide reduces glioblastoma tumor growth, migration and glial-to-mesenchymal transition. Cell Oncol 40, 247–261 (2017).  https://doi.org/10.1007/s13402-017-0320-1
  49. 49.
    M. Staberg, S.R. Michaelsen, R.D. Rasmussen, M. Villingshoj, H.S. Poulsen, P. Hamerlik, Inhibition of histone deacetylases sensitizes glioblastoma cells to lomustine. Cell Oncol 40, 21–32 (2017).  https://doi.org/10.1007/s13402-016-0301-9
  50. 50.
    N. Cancer Genome Atlas Research, D.J. Brat, R.G. Verhaak, K.D. Aldape, W.K. Yung, S.R. Salama, L.A. Cooper, E. Rheinbay, C.R. Miller, M. Vitucci, O. Morozova, A.G. Robertson, H. Noushmehr, P.W. Laird, A.D. Cherniack, R. Akbani, J.T. Huse, G. Ciriello, L.M. Poisson, J.S. Barnholtz-Sloan, M.S. Berger, C. Brennan, R.R. Colen, H. Colman, A.E. Flanders, C. Giannini, M. Grifford, A. Iavarone, R. Jain, I. Joseph, J. Kim, K. Kasaian, T. Mikkelsen, B.A. Murray, B.P. O'Neill, L. Pachter, D.W. Parsons, C. Sougnez, E.P. Sulman, S.R. Vandenberg, E.G. Van Meir, A. von Deimling, H. Zhang, D. Crain, K. Lau, D. Mallery, S. Morris, J. Paulauskis, R. Penny, T. Shelton, M. Sherman, P. Yena, A. Black, J. Bowen, K. Dicostanzo, J. Gastier-Foster, K.M. Leraas, T.M. Lichtenberg, C.R. Pierson, N.C. Ramirez, C. Taylor, S. Weaver, L. Wise, E. Zmuda, T. Davidsen, J.A. Demchok, G. Eley, M.L. Ferguson, C.M. Hutter, K.R. Mills Shaw, B.A. Ozenberger, M. Sheth, H.J. Sofia, R. Tarnuzzer, Z. Wang, L. Yang, J.C. Zenklusen, B. Ayala, J. Baboud, S. Chudamani, M.A. Jensen, J. Liu, T. Pihl, R. Raman, Y. Wan, Y. Wu, A. Ally, J.T. Auman, M. Balasundaram, S. Balu, S.B. Baylin, R. Beroukhim, M.S. Bootwalla, R. Bowlby, C.A. Bristow, D. Brooks, Y. Butterfield, R. Carlsen, S. Carter, L. Chin, A. Chu, E. Chuah, K. Cibulskis, A. Clarke, S.G. Coetzee, N. Dhalla, T. Fennell, S. Fisher, S. Gabriel, G. Getz, R. Gibbs, R. Guin, A. Hadjipanayis, D.N. Hayes, T. Hinoue, K. Hoadley, R.A. Holt, A.P. Hoyle, S.R. Jefferys, S. Jones, C.D. Jones, R. Kucherlapati, P.H. Lai, E. Lander, S. Lee, L. Lichtenstein, Y. Ma, D.T. Maglinte, H.S. Mahadeshwar, M.A. Marra, M. Mayo, S. Meng, M.L. Meyerson, P.A. Mieczkowski, R.A. Moore, L.E. Mose, A.J. Mungall, A. Pantazi, M. Parfenov, P.J. Park, J.S. Parker, C.M. Perou, A. Protopopov, X. Ren, J. Roach, T.S. Sabedot, J. Schein, S.E. Schumacher, J.G. Seidman, S. Seth, H. Shen, J.V. Simons, P. Sipahimalani, M.G. Soloway, X. Song, H. Sun, B. Tabak, A. Tam, D. Tan, J. Tang, N. Thiessen, T. Triche, Jr, DJ Van Den Berg, U Veluvolu, S Waring, DJ Weisenberger, MD Wilkerson, T Wong, J Wu, L Xi, AW Xu, L Yang, TI Zack, J Zhang, BA Aksoy, H Arachchi, C Benz, B Bernard, D Carlin, J Cho, D DiCara, S Frazer, GN Fuller, J Gao, N Gehlenborg, D Haussler, DI Heiman, L Iype, A Jacobsen, Z Ju, S Katzman, H Kim, T Knijnenburg, RB Kreisberg, MS Lawrence, W Lee, K Leinonen, P Lin, S Ling, W Liu, Y Liu, Y Liu, Y Lu, G Mills, S Ng, MS Noble, E Paull, A Rao, S Reynolds, G Saksena, Z Sanborn, C Sander, N Schultz, Y Senbabaoglu, R Shen, I Shmulevich, R Sinha, J Stuart, SO Sumer, Y Sun, N Tasman, BS Taylor, D Voet, N Weinhold, JN Weinstein, D Yang, K Yoshihara, S Zheng, W Zhang, L Zou, T Abel, S Sadeghi, ML Cohen, J Eschbacher, EM Hattab, A Raghunathan, MJ Schniederjan, D Aziz, G Barnett, W Barrett, DD Bigner, L Boice, C Brewer, C Calatozzolo, B Campos, CG Carlotti, Jr, TA Chan, L Cuppini, E Curley, S Cuzzubbo, K Devine, F DiMeco, R Duell, JB Elder, A Fehrenbach, G Finocchiaro, W Friedman, J Fulop, J Gardner, B Hermes, C Herold-Mende, C Jungk, A Kendler, NL Lehman, E Lipp, O Liu, R Mandt, M McGraw, R McLendon, C McPherson, L Neder, P Nguyen, A Noss, R Nunziata, QT Ostrom, C Palmer, A Perin, B Pollo, A Potapov, O Potapova, WK Rathmell, D Rotin, L Scarpace, C Schilero, K Senecal, K Shimmel, V Shurkhay, S Sifri, R Singh, AE Sloan, K Smolenski, SM Staugaitis, R Steele, L Thorne, DP Tirapelli, A Unterberg, M Vallurupalli, Y Wang, R Warnick, F Williams, Y Wolinsky, S Bell, M Rosenberg, C Stewart, F Huang, JL Grimsby, AJ Radenbaugh and J Zhang Comprehensive, Integrative Genomic Analysis of Diffuse Lower-Grade Gliomas N Engl J Med 372, 2481–2498 (2015).  https://doi.org/10.1056/NEJMoa1402121
  51. 51.
    G.P. de Faria, J.A. de Oliveira, J.G. de Oliveira, O. Romano Sde, V.M. Neto, R.C. Maia, Differences in the expression pattern of P-glycoprotein and MRP1 in low-grade and high-grade gliomas. Cancer Investig 26, 883–889 (2008).  https://doi.org/10.1080/07357900801975264
  52. 52.
    M.D. Cykowski, R.A. Allen, A.C. Kanaly, K.M. Fung, R. Marshall, A. Perry, E.D. Stolzenberg, S.T. Dunn, The differential diagnosis of pilocytic astrocytoma with atypical features and malignant glioma: An analysis of 16 cases with emphasis on distinguishing molecular features. J Neuro-Oncol 115, 477–486 (2013).  https://doi.org/10.1007/s11060-013-1249-5
  53. 53.
    X. Hu, W. Miao, Y. Zou, W. Zhang, Y. Zhang, H. Liu, Expression of p53, epidermal growth factor receptor, Ki-67 and O6-methylguanine-DNA methyltransferase in human gliomas. Oncol Lett 6, 130–134 (2013).  https://doi.org/10.3892/ol.2013.1317
  54. 54.
    H. Takami, A. Yoshida, S. Fukushima, H. Arita, Y. Matsushita, T. Nakamura, M. Ohno, Y. Miyakita, S. Shibui, Y. Narita, K. Ichimura, Revisiting TP53 mutations and immunohistochemistry--a comparative study in 157 diffuse gliomas. Brain Pathol 25, 256–265 (2015).  https://doi.org/10.1111/bpa.12173
  55. 55.
    S. Takano, E. Ishikawa, N. Sakamoto, M. Matsuda, H. Akutsu, M. Noguchi, Y. Kato, T. Yamamoto, A. Matsumura, Immunohistochemistry on IDH 1/2, ATRX, p53 and Ki-67 substitute molecular genetic testing and predict patient prognosis in grade III adult diffuse gliomas. Brain Tumor Pathol 33, 107–116 (2016).  https://doi.org/10.1007/s10014-016-0260-x
  56. 56.
    H. Ohgaki, P. Kleihues, The definition of primary and secondary glioblastoma. Clin Cancer Res 19, 764–772 (2013).  https://doi.org/10.1158/1078-0432.CCR-12-3002
  57. 57.
    H. Wakimoto, S. Tanaka, W.T. Curry, F. Loebel, D. Zhao, K. Tateishi, J. Chen, L.K. Klofas, N. Lelic, J.C. Kim, D. Dias-Santagata, L.W. Ellisen, D.R. Borger, S.M. Fendt, M.G. Vander Heiden, T.T. Batchelor, A.J. Iafrate, D.P. Cahill, A.S. Chi, Targetable signaling pathway mutations are associated with malignant phenotype in IDH-mutant gliomas. Clin Cancer Res 20, 2898–2909 (2014).  https://doi.org/10.1158/1078-0432.CCR-13-3052
  58. 58.
    A. Das, W.L. Tan, J. Teo, D.R. Smith, Expression of survivin in primary glioblastomas. J Cancer Res Clin Oncol 128, 302–306 (2002).  https://doi.org/10.1007/s00432-002-0343-4
  59. 59.
    B. Vischioni, P. van der Valk, S.W. Span, F.A. Kruyt, J.A. Rodriguez, G. Giaccone, Nuclear localization of survivin is a positive prognostic factor for survival in advanced non-small-cell lung cancer. Ann Oncol 15, 1654–1660 (2004).  https://doi.org/10.1093/annonc/mdh436
  60. 60.
    A.C. Fields, G. Cotsonis, D. Sexton, R. Santoianni, C. Cohen, Survivin expression in hepatocellular carcinoma: Correlation with proliferation, prognostic parameters, and outcome. Mod Pathol 17, 1378–1385 (2004).  https://doi.org/10.1038/modpathol.3800203
  61. 61.
    D. Ansari, A. Rosendahl, J. Elebro, R. Andersson, Systematic review of immunohistochemical biomarkers to identify prognostic subgroups of patients with pancreatic cancer. Br J Surg 98, 1041–1055 (2011).  https://doi.org/10.1002/bjs.7574
  62. 62.
    A. Del Gobbo, S. Ferrero, Immunohistochemical markers as predictors of histopathologic response and prognosis in rectal cancer treated with preoperative adjuvant therapy: State of the art. Gastroenterol Res Pract 2808235, 2017 (2017).  https://doi.org/10.1155/2017/2808235
  63. 63.
    Q. Li, P. Huang, C. Zheng, J. Wang, M. Ge, Prognostic significance of p53 immunohistochemical expression in adenoid cystic carcinoma of the salivary glands: A meta-analysis. Oncotarget 8, 29458–29473 (2017).  https://doi.org/10.18632/oncotarget.15297
  64. 64.
    H. Lin, Y. Wang, X. Zhang, B. Liu, W. Zhang, J. Cheng, Prognostic significance of kappaB-Ras1 expression in gliomas. Med Oncol 29, 1272–1279 (2012).  https://doi.org/10.1007/s12032-011-9835-x
  65. 65.
    F. Keime-Guibert, O. Chinot, L. Taillandier, S. Cartalat-Carel, M. Frenay, G. Kantor, J.S. Guillamo, E. Jadaud, P. Colin, P.Y. Bondiau, P. Menei, H. Loiseau, V. Bernier, J. Honnorat, M. Barrie, K. Mokhtari, J.J. Mazeron, A. Bissery, J.Y. Delattre, N.-O. Association of French-speaking. Radiotherapy for glioblastoma in the elderly. N Engl J Med 356, 1527–1535 (2007).  https://doi.org/10.1056/NEJMoa065901

Copyright information

© International Society for Cellular Oncology 2018

Authors and Affiliations

  • Roberta Soares Faccion
    • 1
    • 2
  • Paula Sabbo Bernardo
    • 1
    • 3
  • Giselle Pinto Faria de Lopes
    • 1
  • Leonardo Soares Bastos
    • 4
  • Cristina Lordello Teixeira
    • 5
  • José Antonio de Oliveira
    • 6
  • Priscila Valverde Fernandes
    • 7
  • Luiz Gustavo Dubois
    • 8
  • Leila Chimelli
    • 9
  • Raquel Ciuvalschi Maia
    • 1
  1. 1.Laboratório de Hemato-Oncologia Celular e Molecular, Programa de Hemato-Oncologia MolecularHospital do Câncer I, Centro de Pesquisas do Instituto Nacional de Câncer José Alencar Gomes da Silva (INCA)Rio de JaneiroBrazil
  2. 2.Programa de Pós-Graduação em Ciências Biológicas – Fisiologia, Instituto de Biofísica Carlos Chagas Filho, Centro de Ciências da SaúdeUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  3. 3.Programa de Pós-Graduação Stricto Sensu em Oncologia, INCARio de JaneiroBrazil
  4. 4.Programa de Computação Científica (PROCC), Presidência, Fundação Oswaldo Cruz (Fiocruz)Rio de JaneiroBrazil
  5. 5.Serviço de Patologia Clínica, Hospital do Câncer I, INCARio de JaneiroBrazil
  6. 6.Serviço de Neurocirurgia, INCARio de JaneiroBrazil
  7. 7.Divisão de Patologia, INCARio de JaneiroBrazil
  8. 8.Laboratório de Biomedicina do CérebroInstituto Estadual do Cérebro Paulo Niemeyer (IECPN)Rio de JaneiroBrazil
  9. 9.Laboratório de Neuropatologia e Genética MolecularInstituto Estadual do Cérebro Paulo Niemeyer (IECPN)Rio de JaneiroBrazil

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