Single-cell sequencing analysis characterizes common and cell-lineage-specific mutations in a muscle-invasive bladder cancer

详细信息    查看全文

• 作者：Yingrui Li (1)
  Xun Xu (1)
  Luting Song (1) (2) (3) (4)
  Yong Hou (1) (5) (6)
  Zesong Li (7) (8) (9)
  Shirley Tsang (10)
  Fuqiang Li (1)
  Kate McGee Im (11)
  Kui Wu (1)
  Hanjie Wu (1) (12)
  Xiaofei Ye (1)
  Guibo Li (1)
  Linlin Wang (1)
  Bo Zhang (1)
  Jie Liang (1)
  Wei Xie (1) (5) (6)
  Renhua Wu (1)
  Hui Jiang (1)
  Xiao Liu (1)
  Chang Yu (1)
  Hancheng Zheng (1)
  Min Jian (1)
  Liping Nie (13)
  Lei Wan (14)
  Min Shi (13)
  Xiaojuan Sun (7) (8) (9)
  Aifa Tang (7) (8) (9)
  Guangwu Guo (1)
  Yaoting Gui (13)
  Zhiming Cai (13) (8) (9)
  Jingxiang Li (1)
  Wen Wang (2)
  Zuhong Lu (5) (6)
  Xiuqing Zhang (1)
  Lars Bolund (1) (15)
  Karsten Kristiansen (1) (16)
  Jian Wang (1)
  Huanming Yang (1)
  Michael Dean (11)
  Jun Wang (1) (16) (17)
  
• 关键词：Single ; cell exome sequencing ; Bladder cancer ; Tumor evolution ; Population genetics
• 刊名：GigaScience
• 出版年：2012
• 出版时间：December 2012
• 年：2012
• 卷：1
• 期：1
• 全文大小：335KB
• 参考文献：1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D: Global cancer statistics. / CA Cancer J Clin 2011,61(2):69鈥?0. CrossRef
  2. Knowles MA: Molecular pathogenesis of bladder cancer. / Int J Clin Oncol 2008,13(4):287鈥?97. CrossRef
  3. Mitra AP, Cote RJ: Molecular pathogenesis and diagnostics of bladder cancer. / Annu Rev Pathol 2009, 4:251鈥?85. CrossRef
  4. Kompier LC, van Tilborg AA, Zwarthoff EC: Bladder cancer: novel molecular characteristics, diagnostic, and therapeutic implications. / Urol Oncol 2010,28(1):91鈥?6. CrossRef
  5. Witjes JA, Hendricksen K: Intravesical pharmacotherapy for non-muscle-invasive bladder cancer: a critical analysis of currently available drugs, treatment schedules, and long-term results. / Eur Urol 2008,53(1):45鈥?2. CrossRef
  6. Gui Y, Guo G, Huang Y, Hu X, Tang A, Gao S, Wu R, Chen C, Li X, Zhou L, He M, Li Z, Sun X, Jia W, Chen J, Yang S, Zhou F, Zhao X, Wan S, Ye R, Liang C, Liu Z, Huang P, Liu C, Jiang H, Wang Y, Zheng H, Sun L, Liu X, Jiang Z, / et al.: Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. / Nat Genet 2011,43(9):875鈥?78. CrossRef
  7. Navin N, Kendall J, Troge J, Andrews P, Rodgers L, McIndoo J, Cook K, Stepansky A, Levy D, Esposito D, Muthuswamy L, Krasnitz A, McCombie WR, Hicks J, Wigler M: Tumour evolution inferred by single-cell sequencing. / Nature 2011,472(7341):90鈥?4. CrossRef
  8. Hou Y, Song L, Zhu P, Zhang B, Tao Y, Xu X, Li F, Wu K, Liang J, Shao D, Wu H, Ye X, Ye C, Wu R, Jian M, Chen Y, Xie W, Zhang R, Chen L, Liu X, Yao X, Zheng H, Yu C, Li Q, Gong Z, Mao M, Yang X, Yang L, Li J, Wang W, / et al.: Single-Cell Exome Sequencing and Monoclonal Evolution of a JAK2-Negative Myeloproliferative Neoplasm. / Cell 2012,148(5):873鈥?85. CrossRef
  9. Xu X, Hou Y, Yin X, Bao L, Tang A, Song L, Li F, Tsang S, Wu K, Wu H, He W, Zeng L, Xing M, Wu R, Jiang H, Liu X, Cao D, Guo G, Hu X, Gui Y, Li Z, Xie W, Sun X, Shi M, Cai Z, Wang B, Zhong M, Li J, Lu Z, Gu N, / et al.: Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor. / Cell 2012,148(5):886鈥?95. CrossRef
  10. Yi X, Liang Y, Huerta-Sanchez E, Jin X, Cuo ZX, Pool JE, Xu X, Jiang H, Vinckenbosch N, Korneliussen TS, Zheng H, Liu T, He W, Li K, Luo R, Nie X, Wu H, Zhao M, Cao H, Zou J, Shan Y, Li S, Yang Q, Asan , Ni P, Tian G, Xu J, Liu X, Jiang T, Wu R, / et al.: Sequencing of 50 human exomes reveals adaptation to high altitude. / Science 2010,329(5987):75鈥?8. CrossRef
  11. Li Y, Xu X, Song L, Hou Y, Li F, Wu K, Wu H, Liang J, Jian M, Li J, Zhang X, Wang J, Yang H, Wang J: Single cell whole-exome sequences of bladder cancer from an individual. / GigaScience 2012. http://dx.doi.org/10.5524/100037
  12. Spits C, Le Caignec C, De Rycke M, Van Haute L, Van Steirteghem A, Liebaers I, Sermon K: Whole-genome multiple displacement amplification from single cells. / Nat Protoc 2006,1(4):1965鈥?970. CrossRef
  13. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP, Evers DJ, Barnes CL, Bignell HR, Boutell JM, Bryant J, Carter RJ, Keira Cheetham R, Cox AJ, Ellis DJ, Flatbush MR, Gormley NA, Humphray SJ, Irving LJ, Karbelashvili MS, Kirk SM, Li H, Liu X, Maisinger KS, Murray LJ, Obradovic B, Ost T, Parkinson ML, Pratt MR, / et al.: Accurate whole human genome sequencing using reversible terminator chemistry. / Nature 2008,456(7218):53鈥?9. CrossRef
  14. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The Sequence Alignment/Map format and SAMtools. / Bioinformatics 2009,25(16):2078鈥?079. CrossRef
  15. Sathirapongsasuti JF, Lee H, Horst BA, Brunner G, Cochran AJ, Binder S, Quackenbush J, Nelson SF: Exome sequencing-based copy-number variation and loss of heterozygosity detection: ExomeCNV. / Bioinformatics 2011,27(19):2648鈥?654. CrossRef
  16. The 1000 Genomes Project Consortium: A map of human genome variation from population-scale sequencing. / Nature 2010,467(7319):1061鈥?073. CrossRef
  17. Stratton MR, Campbell PJ, Futreal PA: The cancer genome. / Nature 2009,458(7239):719鈥?24. CrossRef
  18. Loeb LA, Loeb KR, Anderson JP: Multiple mutations and cancer. / Proc Natl Acad Sci U S A 2003,100(3):776鈥?81. CrossRef
  19. Loeb LA, Bielas JH, Beckman RA: Cancers exhibit a mutator phenotype: clinical implications. / Cancer Res 2008,68(10):3551鈥?557. discussion 3557 CrossRef
  20. Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, Kamiyama M, Hruban RH, Eshleman JR, Nowak MA, Velculescu VE, Kinzler KW, Vogelstein B, Iacobuzio-Donahue CA: Distant metastasis occurs late during the genetic evolution of pancreatic cancer. / Nature 2010,467(7319):1114鈥?117. CrossRef
  21. Tonkin ET, Wang TJ, Lisgo S, Bamshad MJ, Strachan T: NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. / Nat Genet 2004,36(6):636鈥?41. CrossRef
  22. Jahnke P, Xu W, Wulling M, Albrecht M, Gabriel H, Gillessen-Kaesbach G, Kaiser FJ: The Cohesin loading factor NIPBL recruits histone deacetylases to mediate local chromatin modifications. / Nucleic Acids Res 2008,36(20):6450鈥?458. CrossRef
  23. Chi P, Allis CD, Wang GG: Covalent histone modifications鈥搈iswritten, misinterpreted and mis-erased in human cancers. / Nat Rev Cancer 2010,10(7):457鈥?69. CrossRef
  24. Rommens JM, Iannuzzi MC, Kerem B, Drumm ML, Melmer G, Dean M, Rozmahel R, Cole JL, Kennedy D, Hidaka N, / et al.: Identification of the cystic fibrosis gene: chromosome walking and jumping. / Science 1989,245(4922):1059鈥?065. CrossRef
  25. Liang J, Song W, Tromp G, Kolattukudy PE, Fu M: Genome-wide survey and expression profiling of CCCH-zinc finger family reveals a functional module in macrophage activation. / PLoS One 2008,3(8):e2880. CrossRef
  26. Thouennon E, Elkahloun AG, Guillemot J, Gimenez-Roqueplo AP, Bertherat J, Pierre A, Ghzili H, Grumolato L, Muresan M, Klein M, Lefebvre H, Ouafik L, Vaudry H, Plouin PF, Yon L, Anouar Y: Identification of potential gene markers and insights into the pathophysiology of pheochromocytoma malignancy. / J Clin Endocrinol Metab 2007,92(12):4865鈥?872. CrossRef
  27. Zagzag D, Salnikow K, Chiriboga L, Yee H, Lan L, Ali MA, Garcia R, Demaria S, Newcomb EW: Downregulation of major histocompatibility complex antigens in invading glioma cells: stealth invasion of the brain. / Lab Invest 2005,85(3):328鈥?41. CrossRef
  28. Rotman G, Shiloh Y: ATM: from gene to function. / Hum Mol Genet 1998,7(10):1555鈥?563. CrossRef
  29. Branzei D, Foiani M: Regulation of DNA repair throughout the cell cycle. / Nat Rev Mol Cell Biol 2008,9(4):297鈥?08. CrossRef
  30. Smith MJ, Culhane AC, Donovan M, Coffey JC, Barry BD, Kelly MA, Higgins DG, Wang JH, Kirwan WO, Cotter TG, Redmond HP: Analysis of differential gene expression in colorectal cancer and stroma using fluorescence-activated cell sorting purification. / Br J Cancer 2009,100(9):1452鈥?464. CrossRef
  31. Ohlund D, Lundin C, Ardnor B, Oman M, Naredi P, Sund M: Type IV collagen is a tumour stroma-derived biomarker for pancreas cancer. / Br J Cancer 2009,101(1):91鈥?7. CrossRef
  32. Youn A, Simon R: Identifying cancer driver genes in tumor genome sequencing studies. / Bioinformatics 2011,27(2):175鈥?81. CrossRef
  33. Nowell PC: The clonal evolution of tumor cell populations. / Science 1976,194(4260):23鈥?8. CrossRef
  34. Loeb LA: A mutator phenotype in cancer. / Cancer Res 2001,61(8):3230鈥?239.
  35. Heng HH, Stevens JB, Liu G, Bremer SW, Ye KJ, Reddy PV, Wu GS, Wang YA, Tainsky MA, Ye CJ: Stochastic cancer progression driven by non-clonal chromosome aberrations. / J Cell Physiol 2006,208(2):461鈥?72. CrossRef
  36. Hanahan D, Weinberg RA: Hallmarks of cancer: the next generation. / Cell 2011,144(5):646鈥?74. CrossRef
  37. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, Stewart A, Tarpey P, Varela I, Phillimore B, Begum S, McDonald NQ, Butler A, Jones D, Raine K, Latimer C, Santos CR, Nohadani M, Eklund AC, Spencer-Dene B, Clark G, Pickering L, Stamp G, Gore M, Szallasi Z, Downward J, Futreal PA, Swanton C: Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. / N Engl J Med 2012,366(10):883鈥?92. CrossRef
  38. The University of California, Santa Cruz Bioinformatics Sitehttp://genome.ucsc.edu/
  39. Agilent Technologieshttp://www.genomics.agilent.com
  40. The pcaMethods v1.12.0http://rss.acs.unt.edu/Rdoc/library/pcaMethods/
  41. The Perl Package (Left)http://search.cpan.org/dist/Text-NSP/lib/Text/NSP/Measures/2D/Fisher/left.pm
  42. The Perl Package (Right)http://search.cpan.org/dist/Text-NSP/lib/Text/NSP/Measures/2D/Fisher/right.pm
  43. The UniProtKB and Swiss-Prot Databasehttp://www.uniprot.org/
  44. The Kyoto Encyclopedia of Genes and Genomes (KEGG) Databasehttp://www.genome.jp/kegg/
  
• 作者单位：Yingrui Li (1)
  Xun Xu (1)
  Luting Song (1) (2) (3) (4)
  Yong Hou (1) (5) (6)
  Zesong Li (7) (8) (9)
  Shirley Tsang (10)
  Fuqiang Li (1)
  Kate McGee Im (11)
  Kui Wu (1)
  Hanjie Wu (1) (12)
  Xiaofei Ye (1)
  Guibo Li (1)
  Linlin Wang (1)
  Bo Zhang (1)
  Jie Liang (1)
  Wei Xie (1) (5) (6)
  Renhua Wu (1)
  Hui Jiang (1)
  Xiao Liu (1)
  Chang Yu (1)
  Hancheng Zheng (1)
  Min Jian (1)
  Liping Nie (13)
  Lei Wan (14)
  Min Shi (13)
  Xiaojuan Sun (7) (8) (9)
  Aifa Tang (7) (8) (9)
  Guangwu Guo (1)
  Yaoting Gui (13)
  Zhiming Cai (13) (8) (9)
  Jingxiang Li (1)
  Wen Wang (2)
  Zuhong Lu (5) (6)
  Xiuqing Zhang (1)
  Lars Bolund (1) (15)
  Karsten Kristiansen (1) (16)
  Jian Wang (1)
  Huanming Yang (1)
  Michael Dean (11)
  Jun Wang (1) (16) (17)
  
  1. BGI-Shenzhen, Beishan Industrial Zone, Beishan Road, Yantian, Shenzhen, 518083, People鈥檚 Republic of China
  2. CAS-Max Planck Junior Research Group, State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences (CAS), 32# Jiao-chang Road, Kunming, Yunnan, 650223, People鈥檚 Republic of China
  3. Graduate University of the Chinese Academy of Sciences, 19A Yuquanlu, Beijing, 100049, People鈥檚 Republic of China
  4. College of Life Sciences, Wuhan University, Luojia Hill, Wuhan, 430072, People鈥檚 Republic of China
  5. School of Biological Science and Medical Engineering, Southeast University, Sipailou 2#, Nanjing, 210096, People鈥檚 Republic of China
  6. State Key Laboratory of Bioelectronics, Southeast University, Sipailou 2#, Nanjing, 210096, People鈥檚 Republic of China
  7. Shenzhen Key Laboratory of Genitourinary Tumor, Shenzhen Second People鈥檚 Hospital, First Affiliated Hospital of Shenzhen University, Shenzhen, 518035, People鈥檚 Republic of China
  8. Department of Urology, Shenzhen Second People鈥檚 Hospital, Shenzhen, 518035, People鈥檚 Republic of China
  9. The Institute of Urogenital Diseases, Shenzhen University, Shenzhen, 518060, People鈥檚 Republic of China
  10. BioMatrix, LLC, 3029 Windy Knoll Court, Rockville, MD, 20850, USA
  11. Cancer and Inflammation Program, National Cancer Institute at Frederick, Building 560, Frederick, MD, 21702, USA
  12. School of Bioscience and Biotechnology, Guangzhou Higher Education Mega Centre, South China University of Technology, Panyu District, Guangzhou, 510006, People鈥檚 Republic of China
  13. Guangdong and Shenzhen Key Laboratory of Male Reproductive Medicine and Genetics, Institute of Urology, Shenzhen PKU-HKUST Medical Center, Peking University Shenzhen Hospital, 1120 Lian Hua Road, Futian District, Shenzhen, 518036, People鈥檚 Republic of China
  14. Department of Urology, Longgang Central Hospital, Shenhui Road, Longgang Town, Shenzhen, 518116, People鈥檚 Republic of China
  15. Institute of Human Genetics, University of Aarhus, Aarhus, 8100, Denmark
  16. The Novo Nordisk Foundation Center for Basic Metabolic Research, University of Copenhagen, Ole Maal酶es Vej 5, Copenhagen, DK, 2200, Denmark
  17. Department of Biology, University of Copenhagen, Ole Maal酶es Vej 5, Copenhagen, DK, 2200, Denmark
  
• ISSN：2047-217X

文摘

Background Cancers arise through an evolutionary process in which cell populations are subjected to selection; however, to date, the process of bladder cancer, which is one of the most common cancers in the world, remains unknown at a single-cell level. Results We carried out single-cell exome sequencing of 66 individual tumor cells from a muscle-invasive bladder transitional cell carcinoma (TCC). Analyses of the somatic mutant allele frequency spectrum and clonal structure revealed that the tumor cells were derived from a single ancestral cell, but that subsequent evolution occurred, leading to two distinct tumor cell subpopulations. By analyzing recurrently mutant genes in an additional cohort of 99 TCC tumors, we identified genes that might play roles in the maintenance of the ancestral clone and in the muscle-invasive capability of subclones of this bladder cancer, respectively. Conclusions This work provides a new approach of investigating the genetic details of bladder tumoral changes at the single-cell level and a new method for assessing bladder cancer evolution at a cell-population level.