Prognostic value of tumor suppressors in osteosarcoma before and after neoadjuvant chemotherapy

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Robl, Bernhard ^a   Pauli, Chantal ^b   Botter, Sander Martijn ^a   Bode Lesniewska, Beata ^b   Fuchs, Bruno ^a  

^a BALGRIST UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Chemotherapy; Osteosarcoma; P16; P53; PTEN; Tissue microarray; Tumor suppressor genes

Indexed keywords

BIOLOGICAL MARKER; BMI1 PROTEIN; KI 67 ANTIGEN; MASPIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P16; PROTEIN P53; TUMOR SUPPRESSOR PROTEIN; ANTINEOPLASTIC AGENT; TUMOR MARKER;

ADOLESCENT; ADULT; ARTICLE; CANCER ADJUVANT THERAPY; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER PROGNOSIS; CANCER SURGERY; CANCER SURVIVAL; CELLULAR DISTRIBUTION; CHILD; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; METASTASIS; OSTEOSARCOMA; OVERALL SURVIVAL; SURVIVAL RATE; SURVIVAL TIME; TISSUE MICROARRAY; ADJUVANT CHEMOTHERAPY; BONE NEOPLASMS; KAPLAN MEIER METHOD; LUNG NEOPLASMS; METABOLISM; MORTALITY; MULTIVARIATE ANALYSIS; NEOADJUVANT THERAPY; PATHOLOGY; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; SECONDARY; TREATMENT OUTCOME; YOUNG ADULT;

ADOLESCENT; ADULT; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; BONE NEOPLASMS; CHEMOTHERAPY, ADJUVANT; CHILD; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MALE; MULTIVARIATE ANALYSIS; NEOADJUVANT THERAPY; OSTEOSARCOMA; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; TREATMENT OUTCOME; TUMOR SUPPRESSOR PROTEINS; YOUNG ADULT;

EID: 85019170134     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1397-4     Document Type: Article

References (71)

1. Mirabello L, Troisi RJ, Savage SA. Osteosarcoma incidence and survival rates from 1973 to 2004: data from the Surveillance, Epidemiology, and End Results Program. Cancer. 2009;115(7):1531-43.
2. Howlader N, Noone AM, Krapcho M, Garshell J, Neyman N, Altekruse SF, et al. Cancer Epidemiology in Older Adolescents and Young Adults 15 to 29 Years of Age, Including SEER Incidence and Survival: 1975-2000. In: Institute NC, editor. NIH Pub No 06-5767. Bethesda, MD: SEER Cancer Statistics Review; 2013. p. 1975-2010.
3. Allison DC, Carney SC, Ahlmann ER, Hendifar A, Chawla S, Fedenko A, et al. A meta-analysis of osteosarcoma outcomes in the modern medical era. Sarcoma. 2012;2012:704872.
4. Picci P. Osteosarcoma (osteogenic sarcoma). Orphanet J Rare Dis. 2007;2:6.
5. Goorin AM, Schwartzentruber DJ, Devidas M, Gebhardt MC, Ayala AG, Harris MB, et al. Presurgical chemotherapy compared with immediate surgery and adjuvant chemotherapy for nonmetastatic osteosarcoma: Pediatric Oncology Group Study POG-8651. J Clin Oncol. 2003;21(8):1574-80.
6. 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(3):776-90.
7. Provisor AJ, Ettinger LJ, Nachman JB, Krailo MD, Makley JT, Yunis EJ, et al. Treatment of nonmetastatic osteosarcoma of the extremity with preoperative and postoperative chemotherapy: a report from the Children's Cancer Group. J Clin Oncol. 1997;15(1):76-84.
8. Hogendoorn PC, Athanasou N, Bielack S, De Alava E, Dei Tos AP, Ferrari S, et al. Bone sarcomas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2010;21 Suppl 5:v204-213.
9. Kaya M, Wada T, Akatsuka T, Kawaguchi S, Nagoya S, Shindoh M, et al. Vascular endothelial growth factor expression in untreated osteosarcoma is predictive of pulmonary metastasis and poor prognosis. Clin Cancer Res. 2000;6(2):572-7.
10. Bajpai J, Sharma M, Sreenivas V, Kumar R, Gamnagatti S, Khan SA, et al. VEGF expression as a prognostic marker in osteosarcoma. Pediatr Blood Cancer. 2009;53(6):1035-9.
11. Lugowska I, Wozniak W, Klepacka T, Michalak E, Szamotulska K. A prognostic evaluation of vascular endothelial growth factor in children and young adults with osteosarcoma. Pediatr Blood Cancer. 2011;57(1):63-8.
12. Khanna C, Wan X, Bose S, Cassaday R, Olomu O, Mendoza A, et al. The membrane-cytoskeleton linker ezrin is necessary for osteosarcoma metastasis. Nat Med. 2004;10(2):182-6.
13. Salas S, Bartoli C, Deville JL, Gaudart J, Fina F, Calisti A, et al. Ezrin and alpha-smooth muscle actin are immunohistochemical prognostic markers in conventional osteosarcomas. Virchows Arch. 2007;451(6):999-1007.
14. Li H, Min D, Zhao H, Wang Z, Qi W, Zheng S, et al. The Prognostic Role of Ezrin Immunoexpression in Osteosarcoma: A Meta-Analysis of Published Data. PLoS One. 2013;8(6), e64513.
15. Jiang L, Tao C, He A. Prognostic significance of p53 expression in malignant bone tumors: a meta-analysis. Tumour Biol. 2013;34(2):1037-43.
16. Mohseny AB, Tieken C, van der Velden PA, Szuhai K, de Andrea C, Hogendoorn PC, et al. Small deletions but not methylation underlie CDKN2A/p16 loss of expression in conventional osteosarcoma. Genes Chromosomes Cancer. 2010;49(12):1095-103.
17. Deng Z, Niu G, Cai L, Wei R, Zhao X. The prognostic significance of CD44V6, CDH11, and beta-catenin expression in patients with osteosarcoma. Biomed Res Int. 2013;2013:496193.
18. Baumhoer D, Smida J, Zillmer S, Rosemann M, Atkinson MJ, Nelson PJ, et al. Strong expression of CXCL12 is associated with a favorable outcome in osteosarcoma. Mod Pathol. 2012;25(4):522-8.
19. Borys D, Canter RJ, Hoch B, Martinez SR, Tamurian RM, Murphy B, et al. P16 expression predicts necrotic response among patients with osteosarcoma receiving neoadjuvant chemotherapy. Hum Pathol. 2012;43(11):1948-54.
20. Baumhoer D, Elsner M, Smida J, Zillmer S, Rauser S, Schoene C, et al. CRIP1 expression is correlated with a favorable outcome and less metastases in osteosarcoma patients. Oncotarget. 2011;2(12):970-5.
21. Urakawa H, Nishida Y, Naruse T, Nakashima H, Ishiguro N. Cyclooxygenase-2 overexpression predicts poor survival in patients with high-grade extremity osteosarcoma: a pilot study. Clin Orthop Relat Res. 2009;467(11):2932-8.
22. Salzer-Kuntschik M, Brand G, Delling G. Determination of the degree of morphological regression following chemotherapy in malignant bone tumors. Pathologe. 1983;4(3):135-41.
23. Rossi B, Schinzari G, Maccauro G, Scaramuzzo L, Signorelli D, Rosa MA, et al. Neoadjuvant multidrug chemotherapy including high-dose methotrexate modifies VEGF expression in osteosarcoma: an immunohistochemical analysis. BMC Musculoskelet Disord. 2010;11:34.
24. Korpi JT, Hagstrom J, Lehtonen N, Parkkinen J, Sorsa T, Salo T, et al. Expression of matrix metalloproteinases-2, -8, -13, -26, and tissue inhibitors of metalloproteinase-1 in human osteosarcoma. Surg Oncol. 2011;20(1):e18-22.
25. Wang YF, Shen JN, Xie XB, Wang J, Huang G. Expression change of ezrin as a prognostic factor in primary osteosarcoma. Med Oncol. 2011;28 Suppl 1:S636-643.
26. Bramer JA, Abudu AA, Tillman RM, Carter SR, Sumathi VP, Grimer RJ. Pre- and post-chemotherapy alkaline phosphatase levels as prognostic indicators in adults with localised osteosarcoma. Eur J Cancer. 2005;41(18):2846-52.
27. Jackson JG, Pant V, Li Q, Chang LL, Quintas-Cardama A, Garza D, et al. p53-mediated senescence impairs the apoptotic response to chemotherapy and clinical outcome in breast cancer. Cancer Cell. 2012;21(6):793-806.
28. Weller M, Rieger J, Grimmel C, Van Meir EG, De Tribolet N, Krajewski S, et al. Predicting chemoresistance in human malignant glioma cells: the role of molecular genetic analyses. Int J Cancer. 1998;79(6):640-4.
29. Ben Shachar B, Feldstein O, Hacohen D, Ginsberg D. The tumor suppressor maspin mediates E2F1-induced sensitivity of cancer cells to chemotherapy. Mol Cancer Res. 2010;8(3):363-72.
30. Oki E, Baba H, Tokunaga E, Nakamura T, Ueda N, Futatsugi M, et al. Akt phosphorylation associates with LOH of PTEN and leads to chemoresistance for gastric cancer. Int J Cancer. 2005;117(3):376-80.
31. May P, May E. Twenty years of p53 research: structural and functional aspects of the p53 protein. Oncogene. 1999;18(53):7621-36.
32. Chen X, Bahrami A, Pappo A, Easton J, Dalton J, Hedlund E, et al. Recurrent somatic structural variations contribute to tumorigenesis in pediatric osteosarcoma. Cell Rep. 2014;7(1):104-12.
33. Slade N, Moll UM. Mutational analysis of p53 in human tumors: immunocytochemistry. Methods Mol Biol. 2003;234:231-43.
34. Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature. 1993;366(6456):704-7.
35. Mohseny AB, Szuhai K, Romeo S, Buddingh EP, Briaire-de Bruijn I, de Jong D, et al. Osteosarcoma originates from mesenchymal stem cells in consequence of aneuploidization and genomic loss of Cdkn2. J Pathol. 2009;219(3):294-305.
36. Barnard NJ, Hall PA, Lemoine NR, Kadar N. Proliferative index in breast carcinoma determined in situ by Ki67 immunostaining and its relationship to clinical and pathological variables. J Pathol. 1987;152(4):287-95.
37. Sorbye SW, Kilvaer TK, Valkov A, Donnem T, Smeland E, Al-Shibli K, et al. Prognostic Impact of Jab1, p16, p21, p62, Ki67 and Skp2 in Soft Tissue Sarcomas. PLoS One. 2012;7(10), e47068.
38. Yerushalmi R, Woods R, Ravdin PM, Hayes MM, Gelmon KA. Ki67 in breast cancer: prognostic and predictive potential. Lancet Oncol. 2010;11(2):174-83.
39. Antonarakis ES, Keizman D, Zhang Z, Gurel B, Lotan TL, Hicks JL, et al. An immunohistochemical signature comprising PTEN, MYC, and Ki67 predicts progression in prostate cancer patients receiving adjuvant docetaxel after prostatectomy. Cancer. 2012;118(24):6063-71.
40. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature. 1999;397(6715):164-8.
41. Wu Z, Min L, Chen D, Hao D, Duan Y, Qiu G, et al. Overexpression of BMI-1 promotes cell growth and resistance to cisplatin treatment in osteosarcoma. PLoS One. 2011;6(2), e14648.
42. Weng LP, Brown JL, Eng C. PTEN coordinates G(1) arrest by down-regulating cyclin D1 via its protein phosphatase activity and up-regulating p27 via its lipid phosphatase activity in a breast cancer model. Hum Mol Genet. 2001;10(6):599-604.
43. Sano T, Lin H, Chen X, Langford LA, Koul D, Bondy ML, et al. Differential expression of MMAC/PTEN in glioblastoma multiforme: relationship to localization and prognosis. Cancer Res. 1999;59(8):1820-4.
44. Kanamori Y, Kigawa J, Itamochi H, Sultana H, Suzuki M, Ohwada M, et al. PTEN expression is associated with prognosis for patients with advanced endometrial carcinoma undergoing postoperative chemotherapy. Int J Cancer. 2002;100(6):686-9.
45. Zou Z, Anisowicz A, Hendrix MJ, Thor A, Neveu M, Sheng S, et al. Maspin, a serpin with tumor-suppressing activity in human mammary epithelial cells. Science. 1994;263(5146):526-9.
46. Lei KF, Liu BY, Jin XL, Guo Y, Ye M, Zhu ZG. Prognostic value of nuclear maspin expression for adjuvant 5-fluorouracil-based chemotherapy in advanced gastric cancer. Exp Ther Med. 2012;3(6):993-8.
47. Triulzi T, Ratti M, Tortoreto M, Ghirelli C, Aiello P, Regondi V, et al. Maspin influences response to doxorubicin by changing the tumor microenvironment organization. Int J Cancer. 2014;134(12):2789-97.
48. Teoh SS, Vieusseux J, Prakash M, Berkowicz S, Luu J, Bird CH, et al. Maspin is not required for embryonic development or tumour suppression. Nat Commun. 2014;5:3164.
49. Fletcher CDM BJ, Hogendoorn PCW, Mertens F, editors. World Health Organization Classification of Tumours of Soft Tissue and Bone. Pathology and Genetics of Tumours of Soft Tissue and Bone. 4th ed. Lyon: IARC Press; 2013.
50. Fuchs N, Bielack SS, Epler D, Bieling P, Delling G, Korholz D, et al. Long-term results of the co-operative German-Austrian-Swiss osteosarcoma study group's protocol COSS-86 of intensive multidrug chemotherapy and surgery for osteosarcoma of the limbs. Ann Oncol. 1998;9(8):893-9.
51. Bielack S, Kempf-Bielack B, Schwenzer D, Birkfellner T, Delling G, Ewerbeck V, et al. Neoadjuvant therapy for localized osteosarcoma of extremities. Results from the Cooperative osteosarcoma study group COSS of 925 patients. Klin Padiatr. 1999;211(4):260-70.
52. Bubendorf L, Nocito A, Moch H, Sauter G. Tissue microarray (TMA) technology: miniaturized pathology archives for high-throughput in situ studies. J Pathol. 2001;195(1):72-9.
53. Emig R, Magener A, Ehemann V, Meyer A, Stilgenbauer F, Volkmann M, et al. Aberrant cytoplasmic expression of the p16 protein in breast cancer is associated with accelerated tumour proliferation. Br J Cancer. 1998;78(12):1661-8.
54. Arifin MT, Hama S, Kajiwara Y, Sugiyama K, Saito T, Matsuura S, et al. Cytoplasmic, but not nuclear, p16 expression may signal poor prognosis in high-grade astrocytomas. J Neurooncol. 2006;77(3):273-7.
55. Zhao N, Ang MK, Yin XY, Patel MR, Fritchie K, Thorne L, et al. Different cellular p16(INK4a) localisation may signal different survival outcomes in head and neck cancer. Br J Cancer. 2012;107(3):482-90.
56. Jang HL, Nam E, Lee KH, Yeom S, Son HJ, Park C. Maspin polymorphism associated with apoptosis susceptibility and in vivo tumorigenesis. Int J Mol Med. 2008;22(3):333-8.
57. Lopez-Guerrero JA, Machado I, Scotlandi K, Noguera R, Pellin A, Navarro S, et al. Clinicopathological significance of cell cycle regulation markers in a large series of genetically confirmed Ewing's sarcoma family of tumors. Int J Cancer. 2011;128(5):1139-50.
58. Sorensen FB, Jensen K, Vaeth M, Hager H, Funder AM, Safwat A, et al. Immunohistochemical Estimates of Angiogenesis, Proliferative Activity, p53 Expression, and Multiple Drug Resistance Have No Prognostic Impact in Osteosarcoma: A Comparative Clinicopathological Investigation. Sarcoma. 2008;2008:874075.
59. Karim RZ, Gerega SK, Yang YH, Spillane A, Carmalt H, Scolyer RA, et al. p16 and pRb immunohistochemical expression increases with increasing tumour grade in mammary phyllodes tumours. Histopathology. 2010;56(7):868-75.
60. Nilsson K, Svensson S, Landberg G. Retinoblastoma protein function and p16INK4a expression in actinic keratosis, squamous cell carcinoma in situ and invasive squamous cell carcinoma of the skin and links between p16INK4a expression and infiltrative behavior. Mod Pathol. 2004;17(12):1464-74.
61. Acs G, Zhang PJ, McGrath CM, Acs P, McBroom J, Mohyeldin A, et al. Hypoxia-inducible erythropoietin signaling in squamous dysplasia and squamous cell carcinoma of the uterine cervix and its potential role in cervical carcinogenesis and tumor progression. Am J Pathol. 2003;162(6):1789-806.
62. Visakorpi T, Kallioniemi OP, Heikkinen A, Koivula T, Isola J. Small subgroup of aggressive, highly proliferative prostatic carcinomas defined by p53 accumulation. J Natl Cancer Inst. 1992;84(11):883-7.
63. Kerns BJ, Jordan PA, Moore MB, Humphrey PA, Berchuck A, Kohler MF, et al. p53 overexpression in formalin-fixed, paraffin-embedded tissue detected by immunohistochemistry. J Histochem Cytochem. 1992;40(7):1047-51.
64. Collier JD, Carpenter M, Burt AD, Bassendine MF. Expression of mutant p53 protein in hepatocellular carcinoma. Gut. 1994;35(1):98-100.
65. Gercel-Taylor C, Scobee JJ, Taylor DD. Effect of chemotherapy on the mutation frequency of ovarian cancer cells at the HPRT locus. Anticancer Res. 2005;25(3B):2113-7.
66. Ottaviano L, Schaefer KL, Gajewski M, Huckenbeck W, Baldus S, Rogel U, et al. Molecular characterization of commonly used cell lines for bone tumor research: a trans-European EuroBoNet effort. Genes Chromosomes Cancer. 2010;49(1):40-51.
67. Freeman SS, Allen SW, Ganti R, Wu J, Ma J, Su X, et al. Copy number gains in EGFR and copy number losses in PTEN are common events in osteosarcoma tumors. Cancer. 2008;113(6):1453-61.
68. Velickovic M, Delahunt B, McIver B, Grebe SK. Intragenic PTEN/MMAC1 loss of heterozygosity in conventional (clear-cell) renal cell carcinoma is associated with poor patient prognosis. Mod Pathol. 2002;15(5):479-85.
69. Durnali A, Alkis N, Cangur S, Yukruk FA, Inal A, Tokluoglu S, et al. Prognostic factors for teenage and adult patients with high-grade osteosarcoma: an analysis of 240 patients. Med Oncol. 2013;30(3):624.
70. Min D, Lin F, Shen Z, Zheng S, Tan L, Yu W, et al. Analysis of prognostic factors in 333 Chinese patients with high-grade osteosarcoma treated by multidisciplinary combined therapy. Asia Pac J Clin Oncol. 2013;9(1):71-9.
71. Whelan JS, Jinks RC, McTiernan A, Sydes MR, Hook JM, Trani L, et al. Survival from high-grade localised extremity osteosarcoma: combined results and prognostic factors from three European Osteosarcoma Intergroup randomised controlled trials. Ann Oncol. 2012;23(6):1607-16.