Age-Specific Gene Expression Signatures for Breast Tumors and Cross-Species Conserved Potential Cancer Progression Markers in Young Women

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Colak, Dilek ^a   Nofal, Asmaa ^a   AlBakheet, AlBandary ^a   Nirmal, Maimoona ^a   Jeprel, Hatim ^a   Eldali, Abdelmoneim ^a   AL Tweigeri, Taher ^a   Tulbah, Asma ^a   Ajarim, Dahish ^a   Malik, Osama Al ^a   Inan, Mehmet S ^a   Kaya, Namik ^a   Park, Ben H ^b   Bin Amer, Suad M ^a  

^a KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE A1 RECEPTOR; AQUAPORIN 3; BETA DEFENSIN 1; BETA4 INTEGRIN; CHEMOKINE RECEPTOR CXCR4; COMPLEMENT COMPONENT C2; EPHRIN RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; GLYCINE RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN LAMBDA CHAIN; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 6; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROSTACYCLIN SYNTHASE; PROTEIN KINASE B; REELIN; RETINOL DEHYDROGENASE; RIBOSOME PROTEIN; SERINE PROTEINASE INHIBITOR; SQUALENE SYNTHASE; TETRASPANIN; TRANSFORMING GROWTH FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA;

AGE; ARTICLE; BIRC5 GENE; BREAST CANCER; BREAST TUMOR; CANCER GROWTH; CARCINOGENESIS; CCNB1 GENE; CCNB2 GENE; CEP55 GENE; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; COPY NUMBER VARIATION; DEPDC1 GENE; DNA BASE COMPOSITION; ETHNICITY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC CONSERVATION; HELLS GENE; HUMAN; IMMUNOHISTOCHEMISTRY; INTRADUCTAL CARCINOMA; KIAA0101 GENE; KIF4A GENE; MICROARRAY ANALYSIS; MIDDLE EASTERN; NUSAP1 GENE; PTTG1 GENE; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RRM2 GENE; SHCBP1 GENE; SIGNAL TRANSDUCTION; TOP2A GENE; TPX2 GENE; TUMOR GENE; UBE2C GENE; UBE2T GENE;

ADULT; AGING; ANIMALS; BREAST NEOPLASMS; CARCINOGENESIS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, INTRADUCTAL, NONINFILTRATING; COHORT STUDIES; COMPUTATIONAL BIOLOGY; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; GENES, NEOPLASM; GENOME, HUMAN; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MIDDLE AGED; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCIBILITY OF RESULTS; SPECIES SPECIFICITY; TRANSCRIPTOME; TUMOR MARKERS, BIOLOGICAL; YOUNG ADULT;

EID: 84877933653     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063204     Document Type: Article

References (98)

1. Kamangar F, Dores GM, Anderson WF, (2006) Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol 24: 2137-2150.
2. Arabia CRoS (2009) Cancer Incidence Report Saudi Arabia 2005.
3. Society AC (2010) Breast Cancer Facts & Figures 2009-2010. Atlanta: American Cancer Society, Inc.
4. Chung M, Chang HR, Bland KI, Wanebo HJ, (1996) Younger women with breast carcinoma have a poorer prognosis than older women. Cancer 77: 97-103.
5. Maggard MA, O'Connell JB, Lane KE, Liu JH, Etzioni DA, et al. (2003) Do young breast cancer patients have worse outcomes? J Surg Res 113: 109-113.
6. Adami HO, Malker B, Holmberg L, Persson I, Stone B, (1986) The relation between survival and age at diagnosis in breast cancer. N Engl J Med 315: 559-563.
7. Anders CK, Hsu DS, Broadwater G, Acharya CR, Foekens JA, et al. (2008) Young age at diagnosis correlates with worse prognosis and defines a subset of breast cancers with shared patterns of gene expression. J Clin Oncol 26: 3324-3330.
8. Bleyer A, Barr R, Hayes-Lattin B, Thomas D, Ellis C, et al. (2008) The distinctive biology of cancer in adolescents and young adults. Nat Rev Cancer 8: 288-298.
9. Nixon AJ, Neuberg D, Hayes DF, Gelman R, Connolly JL, et al. (1994) Relationship of patient age to pathologic features of the tumor and prognosis for patients with stage I or II breast cancer. J Clin Oncol 12: 888-894.
10. El Saghir NS, Seoud M, Khalil MK, Charafeddine M, Salem ZK, et al. (2006) Effects of young age at presentation on survival in breast cancer. BMC Cancer 6: 194.
11. Holli K, Isola J, (1997) Effect of age on the survival of breast cancer patients. Eur J Cancer 33: 425-428.
12. Aebi S, Gelber S, Castiglione-Gertsch M, Gelber RD, Collins J, et al. (2000) Is chemotherapy alone adequate for young women with oestrogen-receptor-positive breast cancer? Lancet 355: 1869-1874.
13. Elkum N, Dermime S, Ajarim D, Al-Zahrani A, Alsayed A, et al. (2007) Being 40 or younger is an independent risk factor for relapse in operable breast cancer patients: the Saudi Arabia experience. BMC Cancer 7: 222.
14. Bombonati A, Sgroi DC, (2011) The molecular pathology of breast cancer progression. J Pathol 223: 307-317.
15. Ma XJ, Salunga R, Tuggle JT, Gaudet J, Enright E, et al. (2003) Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci U S A 100: 5974-5979.
16. Chin K, de Solorzano CO, Knowles D, Jones A, Chou W, et al. (2004) In situ analyses of genome instability in breast cancer. Nat Genet 36: 984-988.
17. Burstein HJ, Polyak K, Wong JS, Lester SC, Kaelin CM, (2004) Ductal carcinoma in situ of the breast. N Engl J Med 350: 1430-1441.
18. Amari M, Moriya T, Ishida T, Harada Y, Ohnuki K, et al. (2003) Loss of heterozygosity analyses of asynchronous lesions of ductal carcinoma in situ and invasive ductal carcinoma of the human breast. Jpn J Clin Oncol 33: 556-562.
19. Castro NP, Osorio CA, Torres C, Bastos EP, Mourao-Neto M, et al. (2008) Evidence that molecular changes in cells occur before morphological alterations during the progression of breast ductal carcinoma. Breast Cancer Res 10: R87.
20. Ma XJ, Dahiya S, Richardson E, Erlander M, Sgroi DC, (2009) Gene expression profiling of the tumor microenvironment during breast cancer progression. Breast Cancer Res 11: R7.
21. Peeper D, Berns A, (2006) Cross-species oncogenomics in cancer gene identification. Cell 125: 1230-1233.
22. Gaspar C, Cardoso J, Franken P, Molenaar L, Morreau H, et al. (2008) Cross-species comparison of human and mouse intestinal polyps reveals conserved mechanisms in adenomatous polyposis coli (APC)-driven tumorigenesis. Am J Pathol 172: 1363-1380.
23. Paoloni M, Davis S, Lana S, Withrow S, Sangiorgi L, et al. (2009) Canine tumor cross-species genomics uncovers targets linked to osteosarcoma progression. BMC Genomics 10: 625.
24. Sweet-Cordero A, Mukherjee S, Subramanian A, You H, Roix JJ, et al. (2005) An oncogenic KRAS2 expression signature identified by cross-species gene-expression analysis. Nat Genet 37: 48-55.
25. Graeber TG, Sawyers CL, (2005) Cross-species comparisons of cancer signaling. Nat Genet 37: 7-8.
26. Ellwood-Yen K, Graeber TG, Wongvipat J, Iruela-Arispe ML, Zhang J, et al. (2003) Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 4: 223-238.
27. Colak D, Chishti MA, Al-Bakheet AB, Al-Qahtani A, Shoukri MM, et al. (2010) Integrative and comparative genomics analysis of early hepatocellular carcinoma differentiated from liver regeneration in young and old. Mol Cancer 9: 146.
28. Gonzalez-Angulo AM, Hennessy BT, Mills GB, (2010) Future of personalized medicine in oncology: a systems biology approach. J Clin Oncol 28: 2777-2783.
29. Zender L, Spector MS, Xue W, Flemming P, Cordon-Cardo C, et al. (2006) Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125: 1253-1267.
30. Comprehensive molecular portraits of human breast tumours. Nature 490: 61-70.
31. Kadota M, Sato M, Duncan B, Ooshima A, Yang HH, et al. (2009) Identification of novel gene amplifications in breast cancer and coexistence of gene amplification with an activating mutation of PIK3CA. Cancer Res 69: 7357-7365.
32. Haverty PM, Fridlyand J, Li L, Getz G, Beroukhim R, et al. (2008) High-resolution genomic and expression analyses of copy number alterations in breast tumors. Genes Chromosomes Cancer 47: 530-542.
33. Pollack JR, Sorlie T, Perou CM, Rees CA, Jeffrey SS, et al. (2002) Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors. Proc Natl Acad Sci U S A 99: 12963-12968.
34. Patil MA, Chua MS, Pan KH, Lin R, Lih CJ, et al. (2005) An integrated data analysis approach to characterize genes highly expressed in hepatocellular carcinoma. Oncogene 24: 3737-3747.
35. Garraway LA, Widlund HR, Rubin MA, Getz G, Berger AJ, et al. (2005) Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436: 117-122.
36. Ala U, Piro RM, Grassi E, Damasco C, Silengo L, et al. (2008) Prediction of human disease genes by human-mouse conserved coexpression analysis. PLoS Comput Biol 4: e1000043.
37. Kretschmer C, Sterner-Kock A, Siedentopf F, Schoenegg W, Schlag PM, et al. (2011) Identification of early molecular markers for breast cancer. Mol Cancer 10: 15.
38. Bennett CN, Green JE, (2008) Unlocking the power of cross-species genomic analyses: identification of evolutionarily conserved breast cancer networks and validation of preclinical models. Breast Cancer Res 10: 213.
39. Collins LC, Marotti JD, Gelber S, Cole K, Ruddy K, et al. (2012) Pathologic features and molecular phenotype by patient age in a large cohort of young women with breast cancer. Breast Cancer Res Treat 131: 1061-1066.
40. Li C, Hung Wong W, (2001) Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol 2: RESEARCH0032.
41. Li C, Wong WH, (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98: 31-36.
42. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, et al. (2006) TM4 microarray software suite. Methods Enzymol 411: 134-193.
43. Saeed AI, Sharov V, White J, Li J, Liang W, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378.
44. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
45. Wu Z, Irizarry RA (2004) Preprocessing of oligonucleotide array data. Nat Biotechnol 22: 656-658; author reply 658.
46. Wu Z, Irizarry RA, (2005) Stochastic models inspired by hybridization theory for short oligonucleotide arrays. J Comput Biol 12: 882-893.
47. Pavlidis P, (2003) Using ANOVA for gene selection from microarray studies of the nervous system. Methods 31: 282-289.
48. Thomas PD, Kejariwal A, Guo N, Mi H, Campbell MJ, et al. (2006) Applications for protein sequence-function evolution data: mRNA/protein expression analysis and coding SNP scoring tools. Nucleic Acids Res 34: W645-650.
49. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA, (2003) Identifying biological themes within lists of genes with EASE. Genome Biol 4: R70.
50. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, et al. (2001) Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 29: 365-371.
51. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, et al. (2010) An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat 123: 725-731.
52. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, et al. (2007) Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res 13: 3207-3214.
53. Zhang Y, Sieuwerts AM, McGreevy M, Casey G, Cufer T, et al. (2009) The 76-gene signature defines high-risk patients that benefit from adjuvant tamoxifen therapy. Breast Cancer Res Treat 116: 303-309.
54. Miller LD, Smeds J, George J, Vega VB, Vergara L, et al. (2005) An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc Natl Acad Sci U S A 102: 13550-13555.
55. Culhane AC, Schroder MS, Sultana R, Picard SC, Martinelli EN, et al. (2012) GeneSigDB: a manually curated database and resource for analysis of gene expression signatures. Nucleic Acids Res 40: D1060-1066.
56. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, et al. (2012) The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2: 401-404.
57. Reiner A, Yekutieli D, Benjamini Y, (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19: 368-375.
58. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
59. Rubinstein R, Simon I, (2005) MILANO-custom annotation of microarray results using automatic literature searches. BMC Bioinformatics 6: 12.
60. Psyrri A, Kalogeras KT, Kronenwett R, Wirtz RM, Batistatou A, et al. (2012) Prognostic significance of UBE2C mRNA expression in high-risk early breast cancer. A Hellenic Cooperative Oncology Group (HeCOG) Study. Ann Oncol 23: 1422-1427.
61. Waligorska-Stachura J, Jankowska A, Wasko R, Liebert W, Biczysko M, et al. (2012) Survivin-prognostic tumor biomarker in human neoplasms-review. Ginekol Pol 83: 537-540.
62. Stav D, Bar I, Sandbank J, (2007) Usefulness of CDK5RAP3, CCNB2, and RAGE genes for the diagnosis of lung adenocarcinoma. Int J Biol Markers 22: 108-113.
63. Olson JE, Wang X, Goode EL, Pankratz VS, Fredericksen ZS, et al. (2010) Variation in genes required for normal mitosis and risk of breast cancer. Breast Cancer Res Treat 119: 423-430.
64. Chen Z, Zhang C, Wu D, Chen H, Rorick A, et al. (2011) Phospho-MED1-enhanced UBE2C locus looping drives castration-resistant prostate cancer growth. EMBO J 30: 2405-2419.
65. Albertson DG, Collins C, McCormick F, Gray JW, (2003) Chromosome aberrations in solid tumors. Nat Genet 34: 369-376.
66. Zhao X, Weir BA, LaFramboise T, Lin M, Beroukhim R, et al. (2005) Homozygous deletions and chromosome amplifications in human lung carcinomas revealed by single nucleotide polymorphism array analysis. Cancer Res 65: 5561-5570.
67. Pharoah PD, Day NE, Caldas C, (1999) Somatic mutations in the p53 gene and prognosis in breast cancer: a meta-analysis. Br J Cancer 80: 1968-1973.
68. Anders CK, Acharya CR, Hsu DS, Broadwater G, Garman K, et al. (2008) Age-specific differences in oncogenic pathway deregulation seen in human breast tumors. PLoS One 3: e1373.
69. Fredholm H, Eaker S, Frisell J, Holmberg L, Fredriksson I, et al. (2009) Breast cancer in young women: poor survival despite intensive treatment. PLoS One 4: e7695.
70. Xu J, Chen Y, Olopade OI, (2010) MYC and Breast Cancer. Genes Cancer 1: 629-640.
71. Corzo C, Corominas JM, Tusquets I, Salido M, Bellet M, et al. (2006) The MYC oncogene in breast cancer progression: from benign epithelium to invasive carcinoma. Cancer Genet Cytogenet 165: 151-156.
72. Park BK, Zhang H, Zeng Q, Dai J, Keller ET, et al. (2007) NF-kappaB in breast cancer cells promotes osteolytic bone metastasis by inducing osteoclastogenesis via GM-CSF. Nat Med 13: 62-69.
73. Buck MB, Knabbe C, (2006) TGF-beta signaling in breast cancer. Ann N Y Acad Sci 1089: 119-126.
74. Katsuno Y, Lamouille S, Derynck R, (2013) TGF-beta signaling and epithelial-mesenchymal transition in cancer progression. Curr Opin Oncol 25: 76-84.
75. Tokunaga E, Kimura Y, Mashino K, Oki E, Kataoka A, et al. (2006) Activation of PI3K/Akt signaling and hormone resistance in breast cancer. Breast Cancer 13: 137-144.
76. McAuliffe PF, Meric-Bernstam F, Mills GB, Gonzalez-Angulo AM, (2010) Deciphering the role of PI3K/Akt/mTOR pathway in breast cancer biology and pathogenesis. Clin Breast Cancer 10Suppl 3: S59-65.
77. D'Errico A, Barozzi C, Fiorentino M, Carella R, Di Simone M, et al. (2000) Role and new perspectives of transforming growth factor-alpha (TGF-alpha) in adenocarcinoma of the gastro-oesophageal junction. Br J Cancer 82: 865-870.
78. Hantschmann P, Jeschke U, Friese K, (2005) TGF-alpha, c-erbB-2 expression and neoangiogenesis in vulvar squamous cell carcinoma. Anticancer Res 25: 1731-1737.
79. Hartley MC, McKinley BP, Rogers EA, Kalbaugh CA, Messich HS, et al. (2006) Differential expression of prognostic factors and effect on survival in young (< or = 40) breast cancer patients: a case-control study. Am Surg 72: 1189-1194; discussion 1194-1185.
80. Agrup M, Stal O, Olsen K, Wingren S, (2000) C-erbB-2 overexpression and survival in early onset breast cancer. Breast Cancer Res Treat 63: 23-29.
81. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, et al. (1989) Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244: 707-712.
82. Pantschenko AG, Pushkar I, Anderson KH, Wang Y, Miller LJ, et al. (2003) The interleukin-1 family of cytokines and receptors in human breast cancer: implications for tumor progression. Int J Oncol 23: 269-284.
83. Grimm C, Kantelhardt E, Heinze G, Polterauer S, Zeillinger R, et al. (2009) The prognostic value of four interleukin-1 gene polymorphisms in Caucasian women with breast cancer: a multicenter study. BMC Cancer 9: 78.
84. Graziano F, Ruzzo A (2005) Role of the interleukin-1 receptor antagonist gene polymorphism (IL-1RN*2) in early gastric cancer. J Clin Oncol 23: 5272; author reply 5272-5273.
85. Saijo Y, Tanaka M, Miki M, Usui K, Suzuki T, et al. (2002) Proinflammatory cytokine IL-1 beta promotes tumor growth of Lewis lung carcinoma by induction of angiogenic factors: in vivo analysis of tumor-stromal interaction. J Immunol 169: 469-475.
86. Elaraj DM, Weinreich DM, Varghese S, Puhlmann M, Hewitt SM, et al. (2006) The role of interleukin 1 in growth and metastasis of human cancer xenografts. Clin Cancer Res 12: 1088-1096.
87. Honma S, Shimodaira K, Shimizu Y, Tsuchiya N, Saito H, et al. (2002) The influence of inflammatory cytokines on estrogen production and cell proliferation in human breast cancer cells. Endocr J 49: 371-377.
88. Jin L, Yuan RQ, Fuchs A, Yao Y, Joseph A, et al. (1997) Expression of interleukin-1beta in human breast carcinoma. Cancer 80: 421-434.
89. Connelly L, Barham W, Onishko HM, Sherrill T, Chodosh LA, et al. (2011) Inhibition of NF-kappa B activity in mammary epithelium increases tumor latency and decreases tumor burden. Oncogene 30: 1402-1412.
90. Stebel A, Brachetti C, Kunkel M, Schmidt M, Fritz G, (2009) Progression of breast tumors is accompanied by a decrease in expression of the Rho guanine exchange factor Tiam1. Oncol Rep 21: 217-222.
91. Cantrell VA, Jessen JR, (2010) The planar cell polarity protein Van Gogh-Like 2 regulates tumor cell migration and matrix metalloproteinase-dependent invasion. Cancer Lett 287: 54-61.
92. Bennett CN, Green JE, (2010) Genomic analyses as a guide to target identification and preclinical testing of mouse models of breast cancer. Toxicol Pathol 38: 88-95.
93. Langerod A, Zhao H, Borgan O, Nesland JM, Bukholm IR, et al. (2007) TP53 mutation status and gene expression profiles are powerful prognostic markers of breast cancer. Breast Cancer Res 9: R30.
94. Rossner P Jr, Gammon MD, Zhang YJ, Terry MB, Hibshoosh H, et al. (2009) Mutations in p53, p53 protein overexpression and breast cancer survival. J Cell Mol Med 13: 3847-3857.
95. Martelli AM, Cocco L, Capitani S, Miscia S, Papa S, et al. (2007) Nuclear phosphatidylinositol 3,4,5-trisphosphate, phosphatidylinositol 3-kinase, Akt, and PTen: emerging key regulators of anti-apoptotic signaling and carcinogenesis. Eur J Histochem 51Suppl 1: 125-131.
96. Bosco EE, Knudsen ES, (2007) RB in breast cancer: at the crossroads of tumorigenesis and treatment. Cell Cycle 6: 667-671.
97. Sloan KE, Eustace BK, Stewart JK, Zehetmeier C, Torella C, et al. (2004) CD155/PVR plays a key role in cell motility during tumor cell invasion and migration. BMC Cancer 4: 73.
98. Pende D, Spaggiari GM, Marcenaro S, Martini S, Rivera P, et al. (2005) Analysis of the receptor-ligand interactions in the natural killer-mediated lysis of freshly isolated myeloid or lymphoblastic leukemias: evidence for the involvement of the Poliovirus receptor (CD155) and Nectin-2 (CD112). Blood 105: 2066-2073.