Cell type specific gene expression analysis of prostate needle biopsies resolves tumor tissue heterogeneity

Oncotarget

Volumn 6, Issue 2, 2015, Pages 1302-1314

  Krönig, Malte ^a   Walter, Max ^a   Drendel, Vanessa ^a   Werner, Martin ^a   Jilg, Cordula A ^a   Richter, Andreas S ^b,c   Backofen, Rolf ^b   McGarry, David ^a   Follo, Marie ^a   Schultze Seemann, Wolfgang ^a   Schüle, Roland ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

Gene expression; Living cells; Needle biopsy; Prostate cancer; RNA detection; Tumor heterogeneity

Indexed keywords

2 METHYLACYL COENZYME A RACEMASE; CD45 ANTIGEN; EPITHELIAL CELL ADHESION MOLECULE; ALPHA-METHYLACYL-COA RACEMASE; CELL ADHESION MOLECULE; ISOMERASE; TUMOR ANTIGEN; TUMOR MARKER; TUMOR-ASSOCIATED ANTIGEN GA733;

AMACR GENE; ARTICLE; CELL HETEROGENEITY; CELL SPECIFICITY; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOCYTIC INFILTRATION; MALE; MESENCHYME CELL; NEEDLE BIOPSY; PROSTATE BIOPSY; PROSTATE CANCER; PROTEIN EXPRESSION; TUMOR CELL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETIC HETEROGENEITY; GENETICS; METABOLISM; PATHOLOGY; PROCEDURES; PROGNOSIS; PROSTATE; PROSTATE TUMOR; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE;

ANTIGENS, CD45; ANTIGENS, NEOPLASM; BIOMARKERS, TUMOR; BIOPSY, NEEDLE; CELL ADHESION MOLECULES; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC HETEROGENEITY; HUMANS; MALE; PROGNOSIS; PROSTATE; PROSTATIC NEOPLASMS; RACEMASES AND EPIMERASES; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR CELLS, CULTURED;

EID: 84921721635     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2744     Document Type: Article

References (50)

1. Howlader N NA, Krapcho M, Garshell J, Miller D, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z Mariotto, A Lewis, DR Chen, HS Feuer, EJ Cronin KA (eds). SEER Cancer Statistics Review. National Cancer Institute. 2011;1975-2011.
2. Schroder FH, Hugosson J, Roobol MJ, Tammela TL, Ciatto S, Nelen V, Kwiatkowski M, Lujan M, Lilja H, Zappa M, Denis LJ, Recker F, Paez A, Maattanen L, Bangma CH, Aus G, et al. Prostate-cancer mortality at 11 years of follow-up. N Engl J Med. 2012; 366:981-990.
3. D'Amico AV, Whittington R, Malkowicz SB, Schultz D, Blank K, Broderick GA, Tomaszewski JE, Renshaw AA, Kaplan I, Beard CJ, Wein A. Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA. 1998; 280:969-974.
4. Tuxhorn JA, Ayala GE, Smith MJ, Smith VC, Dang TD, Rowley DR. Reactive stroma in human prostate cancer: induction of myofibroblast phenotype and extracellular matrix remodeling. Clin Cancer Res. 2002; 8:2912-2923.
5. Markert EK, Mizuno H, Vazquez A, Levine AJ. Molecular classification of prostate cancer using curated expression signatures. Proc Natl Acad Sci USA. 2011; 108:21276-21281.
6. Prensner JR, Iyer MK, Balbin OA, Dhanasekaran SM, Cao Q, Brenner JC, Laxman B, Asangani IA, Grasso CS, Kominsky HD, Cao X, Jing X, Wang X, Siddiqui J, Wei JT, Robinson D, et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat Biotechnol. 2011; 29:742-749.
7. Boyd LK, Mao X, Lu YJ. The complexity of prostate cancer: genomic alterations and heterogeneity. Nat Rev Urol. 2012; 9:652-664.
8. Sahu A, Iyer MK, Chinnaiyan AM. Insights into Chinese prostate cancer with RNA-seq. Cell Res. 2012; 22:786-788.
9. Joseph A, Gnanapragasam VJ. Laser-capture microdissection and transcriptional profiling in archival FFPE tissue in prostate cancer. Methods Mol Biol. 2011; 755:291-300.
10. Seferos DS, Giljohann DA, Hill HD, Prigodich AE, Mirkin CA. Nano-flares: probes for transfection and mRNA detection in living cells. J Am Chem Soc. 2007; 129:15477-15479.
11. Jiang Z, Wu CL, Woda BA, Dresser K, Xu J, Fanger GR, Yang XJ. P504S/alpha-methylacyl-CoA racemase: a useful marker for diagnosis of small foci of prostatic carcinoma on needle biopsy. Am J Surg Pathol. 2002; 26:1169-1174.
12. Rubin MA, Zhou M, Dhanasekaran SM, Varambally S, Barrette TR, Sanda MG, Pienta KJ, Ghosh D, Chinnaiyan AM. alpha-Methylacyl coenzyme A racemase as a tissue biomarker for prostate cancer. JAMA. 2002; 287:1662-1670.
13. Zhou M, Chinnaiyan AM, Kleer CG, Lucas PC, Rubin MA. Alpha-Methylacyl-CoA racemase: a novel tumor marker over-expressed in several human cancers and their precursor lesions. Am J Surg Pathol. 2002; 26:926-931.
14. Epstein JI. Diagnosis of limited adenocarcinoma of the prostate. Histopathology. 2012; 60:28-40.
15. Zhou M, Jiang Z, Epstein JI. Expression and diagnostic utility of alpha-methylacyl-CoA-racemase (P504S) in foamy gland and pseudohyperplastic prostate cancer. Am J Surg Pathol. 2003; 27:772-778.
16. Dalerba P, Kalisky T, Sahoo D, Rajendran PS, Rothenberg ME, Leyrat AA, Sim S, Okamoto J, Johnston DM, Qian D, Zabala M, Bueno J, Neff NF, Wang J, Shelton AA, Visser B, et al. Single-cell dissection of transcriptional heterogeneity in human colon tumors. Nat Biotechnol. 2011; 29:1120-1127.
17. Dominguez MH, Chattopadhyay PK, Ma S, Lamoreaux L, McDavid A, Finak G, Gottardo R, Koup RA, Roederer M. Highly multiplexed quantitation of gene expression on single cells. J Immunol Methods. 2013; 391:133-145.
18. Sanchez-Freire V, Ebert AD, Kalisky T, Quake SR, Wu JC. Microfluidic single-cell real-time PCR for comparative analysis of gene expression patterns. Nat Protoc. 2012; 7:829-838.
19. Ramskold D, Luo S, Wang YC, Li R, Deng Q, Faridani OR, Daniels GA, Khrebtukova I, Loring JF, Laurent LC, Schroth GP, Sberg R. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat Biotechnol. 2012; 30:777-782.
20. Romanuik TL, Ueda T, Le N, Haile S, Yong TM, Thomson T, Vessella RL, Sadar MD. Novel biomarkers for prostate cancer including noncoding transcripts. Am J Pathol. 2009; 175:2264-2276.
21. Gery S, Sawyers CL, Agus DB, Said JW, Koeffler HP. TMEFF2 is an androgen-regulated gene exhibiting antiproliferative effects in prostate cancer cells. Oncogene. 2002; 21:4739-4746.
22. Holt SK, Kwon EM, Lin DW, Ostrander EA, Stanford JL. Association of hepsin gene variants with prostate cancer risk and prognosis. Prostate. 2010; 70:1012-1019.
23. Ramachandran S, Liu P, Young AN, Yin-Goen Q, Lim SD, Laycock N, Amin MB, Carney JK, Marshall FF, Petros JA, Moreno CS. Loss of HOXC6 expression induces apoptosis in prostate cancer cells. Oncogene. 2005; 24:188-198.
24. Massie CE, Lynch A, Ramos-Montoya A, Boren J, Stark R, Fazli L, Warren A, Scott H, Madhu B, Sharma N, Bon H, Zecchini V, Smith DM, Denicola GM, Mathews N, Osborne M, et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 2011; 30:2719-2733.
25. Ho LL, Kench JG, Handelsman DJ, Scheffer GL, Stricker PD, Grygiel JG, Sutherland RL, Henshall SM, Allen JD, Horvath LG. Androgen regulation of multidrug resistance-associated protein 4 (MRP4/ABCC4) in prostate cancer. Prostate. 2008; 68:1421-1429.
26. Oosterhoff JK, Penninkhof F, Brinkmann AO, Anton Grootegoed J, Blok LJ. REPS2/POB1 is downregulated during human prostate cancer progression and inhibits growth factor signalling in prostate cancer cells. Oncogene. 2003; 22:2920-2925.
27. Sathyanarayana UG, Padar A, Suzuki M, Maruyama R, Shigematsu H, Hsieh JT, Frenkel EP, Gazdar AF. Aberrant promoter methylation of laminin-5-encoding genes in prostate cancers and its relationship to clinicopathological features. Clin Cancer Res. 2003; 9:6395-6400.
28. Saleem M, Kweon MH, Johnson JJ, Adhami VM, Elcheva I, Khan N, Bin Hafeez B, Bhat KM, Sarfaraz S, Reagan-Shaw S, Spiegelman VS, Setaluri V, Mukhtar H. S100A4 accelerates tumorigenesis and invasion of human prostate cancer through the transcriptional regulation of matrix metalloproteinase 9. Proc Natl Acad Sci USA. 2006; 103:14825-14830.
29. Chang L, Schwarzenbach H, Meyer-Staeckling S, Brandt B, Mayr GW, Weitzel JM, Windhorst S. Expression Regulation of the Metastasis-Promoting Protein InsP3-Kinase-A in Tumor Cells. Mol Cancer Res. 2011; 9:497.
30. Nguyen AH, Tremblay M, Haigh K, Koumakpayi IH, Paquet M, Pandolfi PP, Mes-Masson AM, Saad F, Haigh JJ, Bouchard M. Gata3 antagonizes cancer progression in Pten-deficient prostates. Hum Mol Genet. 2013; 22:2400-2410.
31. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, Waldvogel B, Vannier C, Darling D, zur Hausen A, Brunton VG, Morton J, Sansom O, Schuler J, Stemmler MP, Herzberger C, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol. 2009; 11:1487-1495.
32. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010; 29:4741-4751.
33. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003; 17:126-140.
34. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, Itzkovitz S, Noske A, Zurrer-Hardi U, Bell G, Tam WL, Mani SA, van Oudenaarden A, Weinberg RA. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell. 2012; 148:1015-1028.
35. Nishida S, Hirohashi Y, Torigoe T, Kitamura H, Takahashi A, Masumori N, Tsukamoto T, Sato N. Gene expression profiles of prostate cancer stem cells isolated by aldehyde dehydrogenase activity assay. J Urol. 2012; 188:294-299.
36. Siddique HR, Saleem M. Role of BMI1, a stem cell factor, in cancer recurrence and chemoresistance: preclinical and clinical evidences. Stem Cells. 2012; 30:372-378.
37. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126:663-676.
38. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006; 6:392-401.
39. Teicher BA, Fricker SP. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res. 2010; 16:2927-2931.
40. Altin JG, Sloan EK. The role of CD45 and CD45-associated molecules in T cell activation. Immunol Cell Biol. 1997; 75:430-445.
41. Stanbrough M, Bubley GJ, Ross K, Golub TR, Rubin MA, Penning TM, Febbo PG, Balk SP. Increased expression of genes converting adrenal androgens to testosterone in androgen-independent prostate cancer. Cancer Res. 2006; 66:2815-2825.
42. Goldstein AS, Huang J, Guo C, Garraway IP, Witte ON. Identification of a cell of origin for human prostate cancer. Science. 2010; 329:568-571.
43. Kannan K, Wang L, Wang J, Ittmann MM, Li W, Yen L. Recurrent chimeric RNAs enriched in human prostate cancer identified by deep sequencing. Proc Natl Acad Sci USA. 2011; 108:9172-9177.
44. Anders S, Pyl PT, Huber W. HTSeq –, A Python framework to work with high-throughput sequencing data. 2014.
45. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014; 15:178-196.
46. Evans AJ. Alpha-methylacyl CoA racemase (P504S): overview and potential uses in diagnostic pathology as applied to prostate needle biopsies. J Clin Pathol. 2003; 56:892-897.
47. Picelli S, Bjorklund AK, Faridani OR, Sagasser S, Winberg G, Sberg R. Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat Methods. 2013; 10:1096-1098.
48. Madar S, Goldstein I, Rotter V. 'Cancer associated fibroblasts'-more than meets the eye. Trends Mol Med. 2013; 19:447-453.
49. Gooden MJ, de Bock GH, Leffers N, Daemen T, Nijman HW. The prognostic influence of tumour-infiltrating lymphocytes in cancer: a systematic review with meta-analysis. Br J Cancer. 2011; 105:93-103.
50. Bishoff JT, Freedland SJ, Gerber L, Tennstedt P, Reid J, Welbourn W, Graefen M, Sangale Z, Tikishvili E, Park J, Younus A, Gutin A, Lanchbury JS, Sauter G, Brawer M, Stone S, et al. Prognostic utility of the cell cycle progression score generated from biopsy in men treated with prostatectomy. J Urol. 2014; 192:409-414.