Anatomy and Cell Biology

Korean Association of Anatomists (대한해부학회)
권호 표지
DOI QR코드

DOI QR Code

Genomics and proteomics in stem cell research: the road ahead

  • Ahn, Sung-Min (LCDI-BRC Joint Genome Center, Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science) ;
  • Simpson, Richard (Joint Proteomics Laboratory, Ludwig Institute for Cancer Research & The Walter and Eliza Hall Institute of Medical Research, University of Melbourne) ;
  • Lee, Bong-Hee (Center for Genomics and Proteomics & Stem Cell Core Facility, Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science)
  • Received : 2010.02.01
  • Accepted : 2010.03.04
  • Published : 2010.03.30
⟨ Previous Next ⟩

Abstract

Stem cell research has been widely studied over the last few years and has attracted increasing attention from researchers in all fi elds of medicine due to its potential to treat many previously incurable diseases by replacing damaged cells or tissues. As illustrated by hematopoietic stem research, understanding stem cell differentiation at molecular levels is essential for both basic research and for clinical applications of stem cells. Although multiple integrative analyses, such as genomics, epigenomics, transcriptomics and proteomics, are required to understand stem cell biology, proteomics has a unique position in stem cell research. For example, several major breakthroughs in HSC research were due to the identifi cation of proteins such as colony-stimulating factors (CSFs) and cell-surface CD molecules. In 2007, the Human Proteome Organization (HUPO) and the International Society for Stem Cell Research (ISSCR) launched the joint Proteome Biology of Stem Cells Initiative. A systematic proteomics approach to understanding stem cell differentiation will shed new light on stem cell biology and accelerate clinical applications of stem cells.

Keywords

Acknowledgement

Supported by : Korean Government (MOEHRD)

References

  1. Agaton C, Galli J, Höidén Guthenberg I, et al. (2003). Affinity proteomics for systematic protein profiling of chromosome 21 gene products in human tissues. Mol Cell Proteomics 2: 405-414 https://doi.org/10.1074/mcp.M300022-MCP200
  2. Ahmad K, Henikoff S. (2002). Th e histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Molecular cell 9: 1191-1200 https://doi.org/10.1016/S1097-2765(02)00542-7
  3. Alberts B. (2002). Molecular biology of the cell, 4th edn (New York, Garland Science)
  4. Arney KL, Fisher AG. (2004). Epigenetic aspects of diff erentiation. J Cell Sci 117: 4355-4363 https://doi.org/10.1242/jcs.01390
  5. Arrell DK, Niederlander NJ, Faustino RS, Behfar A, Terzic A. (2008). Cardioinductive network guiding stem cell differentiation revealed by proteomic cartography of tumor necrosis factor alpha-primed endodermal secretome. Stem Cells 26: 387-400 https://doi.org/10.1634/stemcells.2007-0599
  6. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. (2003). Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17: 126-140 https://doi.org/10.1101/gad.224503
  7. Baba M, Hasegawa H, Nakayabu M, et al. (1995). Establishment and characteristics of a gastric cancer cell line (HuGC-OOHIRA) producing high levels of G-CSF, GM-CSF, and IL-6: the presence of autocrine growth control by G-CSF. Am J Hematol 49: 207-215 https://doi.org/10.1002/ajh.2830490306
  8. Bannister AJ, Zegerman P, Partridge JF, et al. (2001). Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410: 120-124 https://doi.org/10.1038/35065138
  9. Bartel DP. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297 https://doi.org/10.1016/S0092-8674(04)00045-5
  10. Bartel DP, Chen CZ. (2004). Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 5: 396-400
  11. Baudino TA, Cleveland JL. (2001). The Max network gone mad. Mol Cell Biol 21: 691-702 https://doi.org/10.1128/MCB.21.3.691-702.2001
  12. Bentley GA, Boulot G, Chitarra V. (1994). Cross-reactivity in antibody-antigen interactions. Res Immunol 145: 45-48 https://doi.org/10.1016/S0923-2494(94)80042-1
  13. Bernstein BE, Mikkelsen TS, Xie X, et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326 https://doi.org/10.1016/j.cell.2006.02.041
  14. Bhutani N, Brady JJ, Damian M, Sacco A, Corbel SY, Blau HM. (2010). Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463: 1042-1047 https://doi.org/10.1038/nature08752
  15. Bird A. (2002). DNA methylation patterns and epigenetic memory. Genes Development 16: 6-21 https://doi.org/10.1101/gad.947102
  16. Black DL. (2003). Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72: 291-336 https://doi.org/10.1146/annurev.biochem.72.121801.161720
  17. Blanchette M, Bataille AR, Chen X, et al. (2006). Genomewide computational prediction of transcriptional regulatory modules reveals new insights into human gene expression. Genome Res 16; 656-668 https://doi.org/10.1101/gr.4866006
  18. Boyer LA, Lee TI, Cole MF, et al. (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956 https://doi.org/10.1016/j.cell.2005.08.020
  19. Bradley TR, Metcalf D. (1966). The growth of mouse bone marrow cells in vitro. Aust J Exp Biol Med Sci 44: 287-299 https://doi.org/10.1038/icb.1966.28
  20. Burns CE, Zon LI. (2002). Portrait of a stem cell. Dev Cell 3: 612-613 https://doi.org/10.1016/S1534-5807(02)00329-5
  21. Byrne JA, Pedersen DA, Clepper LL, et al. (2007) Producing primate embryonic stem cells by somatic cell nuclear transfer. Nature 450: 497-502 https://doi.org/10.1038/nature06357
  22. Cai J, Weiss ML, Rao MS. (2004). In search of "stemness". Exp Hematol 32: 585-598 https://doi.org/10.1016/j.exphem.2004.03.013
  23. Chambers I, Silva J, Colby D, et al. (2007). Nanog safeguards pluripotency and mediates germline development. Nature 450: 1230-1234 https://doi.org/10.1038/nature06403
  24. Chang HY, Th omson JA, Chen X. (2006) Microarray analysis of stem cells and differentiation. Methods Enzymol 420: 225-254 https://doi.org/10.1016/S0076-6879(06)20010-7
  25. Chen CZ, Li L, Lodish HF, Bartel DP. (2004). MicroRNAs modulate hematopoietic lineage differentiation. Science 303: 83-86 https://doi.org/10.1126/science.1091903
  26. Cheng LC, Tavazoie M, Doetsch F. (2005). Stem cells: from epigenetics to microRNAs. Neuron 46: 363-367 https://doi.org/10.1016/j.neuron.2005.04.027
  27. Clarke MF, Fuller M. (2006). Stem cells and cancer: two faces of eve. Cell 124: 1111-1115 https://doi.org/10.1016/j.cell.2006.03.011
  28. Cui Q, Yu Z, Purisima EO, Wang E. (2006). Principles of microRNA regulation of a human cellular signaling network. Mol Syst Biol 2: 46
  29. Davidson EH. (2006). Th e regulatory genome: gene regulatory networks in development and evolution, New edn (Oxford Boston, Elsevier / Academic Press)
  30. Dou Y, Gorovsky MA. (2000). Phosphorylation of linker histone H1 regulates gene expression in vivo by creating a charge patch. Molecular Cell 6: 225-231 https://doi.org/10.1016/S1097-2765(00)00024-1
  31. Dover J, Schneider J, Tawiah-Boateng MA, et al. (2002). Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J Biol Chem 277: 28368-28371 https://doi.org/10.1074/jbc.C200348200
  32. Draper JS, Smith K, Gokhale P, et al. (2004). Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat Biotechnol 22: 53-54 https://doi.org/10.1038/nbt922
  33. Edman P. (1960). Phenylthiohydantoins in protein analysis. Ann N Y Acad Sci 88: 602-610
  34. Elliott RL, Blobe GC. (2005). Role of transforming growth factor Beta in human cancer. J Clin Oncol 23: 2078-2093 https://doi.org/10.1200/JCO.2005.02.047
  35. Elliott ST, Crider DG, Garnham CP, Boheler KR, Van Eyk JE. (2004). Two-dimensional gel electrophoresis database of murine R1 embryonic stem cells. Proteomics 4: 3813-3832 https://doi.org/10.1002/pmic.200300820
  36. Feinberg AP, Ohlsson R, Henikoff S. (2006). The epigenetic progenitor origin of human cancer. Nat Rev Genet 7: 21-33 https://doi.org/10.1038/nrg1748
  37. Feldman N, Gerson A, Fang J, et al. (2006). G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat Cell Biol 8: 188-194 https://doi.org/10.1038/ncb1353
  38. Fischle W, Wang Y, Allis CD. (2003) Binary switches and modification cassettes in histone biology and beyond. Nature 425: 475-479 https://doi.org/10.1038/nature02017
  39. Fortunel NO, Otu HH, Ng HH, et al. (2003). Comment on " 'Stemness': transcriptional profiling of embryonic and adult stem cells" and "a stem cell molecular signature". Science 302: 393
  40. Gandhi TK, Zhong J, Mathivanan S, et al. (2006). Analysis of the human protein interactome and comparison with yeast, worm and fly interaction datasets. Nat Genet 38: 285-293 https://doi.org/10.1038/ng1747
  41. Garcia BA, Pesavento JJ, Mizzen CA, Kelleher NL. (2007). Pervasive combinatorial modification of histone H3 in human cells. Nat Methods 4: 487-489 https://doi.org/10.1038/nmeth1052
  42. Gasson JC, Weisbart RH, Kaufman SE, et al. (1984). Purifi ed human granulocyte-macrophage colony-stimulating factor: direct action on neutrophils. Science 226: 1339-1342 https://doi.org/10.1126/science.6390681
  43. He L, He X, Lim LP, et al. (2007). A microRNA component of the p53 tumour suppressor network. Nature 447: 1130-1134 https://doi.org/10.1038/nature05939
  44. Heck AJ, Mummery C, Whetton AD, et al. (2007). Proteome biology of stem cells. Stem Cell Res 1: 7-8 https://doi.org/10.1016/j.scr.2007.08.001
  45. Hopkins AL, Groom CR. (2002). Th e druggable genome. Nat Rev Drug Discov 1: 727-730 https://doi.org/10.1038/nrd892
  46. Howard ML, Davidson EH. (2004). cis-Regulatory control circuits in development. Dev Biol 271: 109-118 https://doi.org/10.1016/j.ydbio.2004.03.031
  47. Hunt DF, Yates JR 3rd, Shabanowitz J, Winston S, Hauer CR. (1986). Protein sequencing by tandem mass spectrometry. Proc Natl Acad Sci U S A 83: 6233-6237 https://doi.org/10.1073/pnas.83.17.6233
  48. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR. (2002). A stem cell molecular signature. Science 298: 601-604 https://doi.org/10.1126/science.1073823
  49. Jacobs JM, Waters KM, Kathmann LE, et al. (2008). The mammary epithelial cell secretome and its regulation by signal transduction pathways. J Proteome Res 7: 558-569 https://doi.org/10.1021/pr0704377
  50. Jenuwein T, Allis CD. (2001). Translating the histone code. Science 293: 1074-1080 https://doi.org/10.1126/science.1063127
  51. Johnston RJ Jr, Chang S, Etchberger JF, Ortiz CO, Hobert O. (2005). MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision. Proc Natl Acad Sci U S A 102: 12449-12454 https://doi.org/10.1073/pnas.0505530102
  52. Jones PA, Takai D. (2001). The role of DNA methylation in mammalian epigenetics. Science 293: 1068-1070 https://doi.org/10.1126/science.1063852
  53. Judson RL, Babiarz JE, Venere M, Blelloch R. (2009). Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat Biotechnol 27: 459-461 https://doi.org/10.1038/nbt.1535
  54. Kang DJ, Oh SO, Ahn SM, Lee BH, Moon MH. (2008). Proteomic analysis of exosomes from human neural stem cells by fl ow fi eld-fl ow fractionation and nanofl ow liquid chromatography-tandem mass spectrometry. J Proteome Res 7: 3475-3480 https://doi.org/10.1021/pr800225z
  55. Kang YK, Koo DB, Park JS, et al. (2001). Aberrant methylation of donor genome in cloned bovine embryos. Nat Genet 28: 173-177 https://doi.org/10.1038/88903
  56. Khwaja FW, Svoboda P, Reed M, Pohl J, Pyrzynska B, Van Meir EG. (2006). Proteomic identifi cation of the wt-p53-regulated tumor cell secretome. Oncogene 25: 7650-7661 https://doi.org/10.1038/sj.onc.1209969
  57. Kim H, Hahn M, Grabowski P, et al. (2006). The Bacillus subtilis spore coat protein interaction network. Mol Microbiol 59: 487-502, https://doi.org/10.1111/j.1365-2958.2005.04968.x
  58. Kim J, Lo L, Dormand E, Anderson DJ. (2003). SOX10 maintains multipotency and inhibits neuronal diff erentiation of neural crest stem cells. Neuron 38: 17-31 https://doi.org/10.1016/S0896-6273(03)00163-6
  59. Klose RJ, Sarraf SA, Schmiedeberg L, McDermott SM, Stancheva I, Bird AP. (2005). DNA binding selectivity of MeCP2 due to a requirement for A/T sequences adjacent to methyl-CpG. Mol Cell 19: 667-678 https://doi.org/10.1016/j.molcel.2005.07.021
  60. Kratchmarova I, Blagoev B, Haack-Sorensen M, Kassem M, Mann M. (2005). Mechanism of divergent growth factor eff ects in mesenchymal stem cell diff erentiation. Science 308: 1472-1477 https://doi.org/10.1126/science.1107627
  61. Krijgsveld J, Whetton AD, Lee BH, et al. (2008). Proteome biology of stem cells: a new joint HUPO and ISSCR initiative. Mol Cell Proteomics 7: 204-205 https://doi.org/10.1074/mcp.H800001-MCP200
  62. Krishna RG, Wold F. (1993). Post-translational modifi cation of proteins. Adv Enzymol Relat Areas Mol Biol 67: 265-298
  63. Lee JH, Hart SRL, Skalnik DG. (2004). Histone deacetylase activity is required for embryonic stem cell diff erentiation. Genesis 38: 32-38 https://doi.org/10.1002/gene.10250
  64. Levchenko A. (2005). Proteomics takes stem cell analyses to another level. Nat Biotechnol 23: 828-830 https://doi.org/10.1038/nbt0705-828
  65. Lim LP, Lau NC, Garrett-Engele P, et al. (2005). Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773 https://doi.org/10.1038/nature03315
  66. Liu C, Zhao X. (2009). MicroRNAs in adult and embryonic neurogenesis. Neuromolecular Med 11: 141-152 https://doi.org/10.1007/s12017-009-8077-y
  67. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. (1997). Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260 https://doi.org/10.1038/38444
  68. Luzi E, Marini F, Carbonell SS, Tognarini I, Galli G, Brandi ML. (2008). Osteogenic diff erentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting the SMAD1 transcription factor. J Bone Miner Res 23: 287-295
  69. Maitra A, Arking DE, Shivapurkar N, et al. (2005). Genomic alterations in cultured human embryonic stem cells. Nat Genet 37: 1099-1103 https://doi.org/10.1038/ng1631
  70. Margueron R, Trojer P, Reinberg D. (2005). The key to development: interpreting the histone code? Curr Opin Genet Dev 15: 163-176 https://doi.org/10.1016/j.gde.2005.01.005
  71. Marx J. (2003). Cancer research. Mutant stem cells may seed cancer. Science 301: 1308-1310 https://doi.org/10.1126/science.301.5638.1308
  72. Mattick JS, Makunin IV. (2006). Non-coding RNA. Hum Mol Genet 15 Spec No 1: R17-29 https://doi.org/10.1093/hmg/ddl046
  73. Metcalf D. (1991). The Florey Lecture, 1991. The colonystimulating factors: discovery to clinical use. Philos Trans R Soc Lond B Biol Sci 333: 147-173 https://doi.org/10.1098/rstb.1991.0065
  74. Nichols J, Zevnik B, Anastassiadis K, et al. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95: 379-391 https://doi.org/10.1016/S0092-8674(00)81769-9
  75. Nightingale KP, O'Neill LP, Turner BM. (2006). Histone modifi cations: signalling receptors and potential elements of a heritable epigenetic code. Curr Opin Genet Dev 16: 125-136 https://doi.org/10.1016/j.gde.2006.02.015
  76. Nomura H, Imazeki I, Oheda M, et al. (1986). Purification and characterization of human granulocyte colonystimulating factor (G-CSF). EMBO J 5: 871-876
  77. Ong SE, Mittler G, Mann M. (2004). Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat Methods 1: 119-126 https://doi.org/10.1038/nmeth715
  78. O'Shea JJ, Gadina M, Schreiber RD. (2002). Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 109(Suppl): S121-131 https://doi.org/10.1016/S0092-8674(02)00701-8
  79. Pardal R, Clarke MF, Morrison SJ. (2003). Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3: 895-902 https://doi.org/10.1038/nrc1232
  80. Pasquinelli AE, Hunter S, Bracht J. (2005). MicroRNAs: a developing story. Curr Opin Genet Dev 15: 200-205 https://doi.org/10.1016/j.gde.2005.01.002
  81. Pesavento JJ, Kim YB, Taylor GK, Kelleher NL. (2004). Shotgun annotation of histone modifications: a new approach for streamlined characterization of proteins by top down mass spectrometry. J Am Chem Soc 126: 3386-3387 https://doi.org/10.1021/ja039748i
  82. Plasterk RH. (2006). Micro RNAs in animal development. Cell 124: 877-881 https://doi.org/10.1016/j.cell.2006.02.030
  83. Poy MN, Eliasson L, Krutzfeldt J, et al. (2004). A pancreatic islet-specific microRNA regulates insulin secretion. Nature 432: 226-230 https://doi.org/10.1038/nature03076
  84. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. (2002). "Stemness": transcriptional profi ling of embryonic and adult stem cells. Science 298: 597-600 https://doi.org/10.1126/science.1072530
  85. Reik W. (2007). Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447: 425-432 https://doi.org/10.1038/nature05918
  86. Reinders J, Sickmann A. (2005). State-of-the-art in phosphoproteomics. Proteomics 5: 4052-4061 https://doi.org/10.1002/pmic.200401289
  87. Rubio D, Garcia-Castro J, Martín MC, et al. (2005). Spontaneous human adult stem cell transformation. Cancer Res 65: 3035-3039 https://doi.org/10.1158/0008-5472.CAN-04-4194
  88. Russo VEA, Martienssen RA, Riggs AD. (1996). Epigenetic mechanisms of gene regulation (Plainview, N.Y., Cold Spring Harbor Laboratory Press)
  89. Sanosaka T, Namihira M, Nakashima K. (2009). Epigenetic mechanisms in sequential differentiation of neural stem cells. Epigenetics 4: 89-92 https://doi.org/10.4161/epi.4.2.8233
  90. Schwartz BE, Ahmad K. (2005). Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19: 804-814 https://doi.org/10.1101/gad.1259805
  91. Shalgi R, Lieber D, Oren M, Pilpel Y. (2007). Global and Local Architecture of the Mammalian microRNA-Transcription Factor Regulatory Network. PLoS Comput Biol 3: e131 https://doi.org/10.1371/journal.pcbi.0030131
  92. Sharan R, Ulitsky I, Shamir R. (2007). Network-based prediction of protein function. Mol Syst Biol 3: 88
  93. Stark A, Brennecke J, Russell RB , Cohen SM. (2003). Identification of Drosophila MicroRNA targets. PLoS Biol 1: E60 https://doi.org/10.1371/journal.pbio.0000060
  94. Stein LD. (2004). Human genome: end of the beginning. Nature 431: 915-916 https://doi.org/10.1038/431915a
  95. Stolt CC, Rehberg S, Ader M, et al. (2002). Terminal diff erentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10. Genes Dev 16: 165-170 https://doi.org/10.1101/gad.215802
  96. Tai MH, Chang CC, Kiupel M, Webster JD, Olson LK, Trosko JE. (2005). Oct4 expression in adult human stem cells: evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis 26: 495-502
  97. Takahashi K, Tanabe K, Ohnuki M, et al. (2007). Induction of pluripotent stem cells from adult human fi broblasts by defi ned factors. Cell 131: 861-872 https://doi.org/10.1016/j.cell.2007.11.019
  98. Takahashi K, Yamanaka S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defi ned factors. Cell 126: 663-676 https://doi.org/10.1016/j.cell.2006.07.024
  99. Taverna SD, Ueberheide BM, Liu Y, et al. (2007). Longdistance combinatorial linkage between methylation and acetylation on histone H3 N termini. Proc Natl Acad Sci U S A 104: 2086-2091 https://doi.org/10.1073/pnas.0610993104
  100. Tay YM, Tam WL, Ang YS, et al. (2008). MicroRNA-134 modulates the differentiation of mouse embryonic stem cells where it causes post-transcriptional attenuation of nanog and LRH1. Stem Cells 26: 17-29 https://doi.org/10.1634/stemcells.2007-0295
  101. Taylor CJ, Bolton EM, Pocock S, Sharples LD, Pedersen RA, Bradley JA. (2005). Banking on human embryonic stem cells: estimating the number of donor cell lines needed for HLA matching. Lancet 366: 2019-2025 https://doi.org/10.1016/S0140-6736(05)67813-0
  102. The ENCODE Project Consortium. (2004). The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306: 636-640 https://doi.org/10.1126/science.1105136
  103. Thomas CE, Kelleher NL, Mizzen CA. (2006). Mass spectrometric characterization of human histone H3: a bird's eye view. J Proteome Res 5: 240-247 https://doi.org/10.1021/pr050266a
  104. Uhlen M, Bjorling E, Agaton C, et al. (2005). A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol Cell Proteomics 4: 1920-1932 https://doi.org/10.1074/mcp.M500279-MCP200
  105. Uhlen M, Ponten F. (2005). Antibody-based proteomics for human tissue profi ling. Mol Cell Proteomics 4: 384-393 https://doi.org/10.1074/mcp.R500009-MCP200
  106. Unwin RD, Smith DL, Blinco D, et al. (2006). Quantitative proteomics reveals posttranslational control as a regulatory factor in primary hematopoietic stem cells. Blood 107: 4687-4694 https://doi.org/10.1182/blood-2005-12-4995
  107. Van Hoof D, Muñoz J, Braam SR, et al. (2009). Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 5: 214-226 https://doi.org/10.1016/j.stem.2009.05.021
  108. Vogel G. (2005). Cell biology. Ready or not? Human ES cells head toward the clinic. Science 308: 1534-1538 https://doi.org/10.1126/science.308.5728.1534
  109. Wade PA. (2001). Methyl CpG binding proteins: coupling chromatin architecture to gene regulation. Oncogene 20: 3166-3173 https://doi.org/10.1038/sj.onc.1204340
  110. Wallin E, von Heijne G. (1998). Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7: 1029-1038
  111. Walsh C. (2006). Posttranslational modification of proteins: expanding nature's inventory (Englewood, Colo., Roberts and Co. Publishers)
  112. Wang ZX, Teh CH, Chan CM, et al. (2008). The transcription factor Zfp281 controls embryonic stem cell pluripotency by direct activation and repression of target genes Stem Cells 26: 2791-2799 https://doi.org/10.1634/stemcells.2008-0443
  113. Watt F, Molloy PL. (1988). Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev 2: 1136-1143 https://doi.org/10.1101/gad.2.9.1136
  114. Wenick AS, Hobert O. (2004). Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specifi c gene battery in C. elegans. Dev Cell 6: 757-770 https://doi.org/10.1016/j.devcel.2004.05.004
  115. Wienholds E, Kloosterman WP, Miska E, et al. (2005). MicroRNA expression in zebrafi sh embryonic development. Science 309: 310-311 https://doi.org/10.1126/science.1114519
  116. Wienholds E, Plasterk RH. (2005). MicroRNA function in animal development. FEBS Lett 579: 5911-5922 https://doi.org/10.1016/j.febslet.2005.07.070
  117. Wissmuller S, Kosian T, Wolf M, Finzsch M, Wegner M. (2006). The high-mobility-group domain of Sox proteins interacts with DNA-binding domains of many transcription factors. Nucleic Acids Res 34: 1735-1744 https://doi.org/10.1093/nar/gkl105
  118. Woolfson A, Ellmark P, Chrisp JS, A Scott M, Christopherson RI. (2006). Th e application of CD antigen proteomics to pharmacogenomics. Pharmacogenomics 7: 759-771 https://doi.org/10.2217/14622416.7.5.759
  119. Wu CC, MacCoss MJ, Howell KE , Yates JR 3rd. (2003). A method for the comprehensive proteomic analysis of membrane proteins. Nat Biotechnol 21: 532-538 https://doi.org/10.1038/nbt819
  120. Wu CC, Yates JR 3rd. (2003). The application of mass spectrometry to membrane proteomics. Nat Biotechnol 21: 262-267. https://doi.org/10.1038/nbt0303-262
  121. Xiao C, Calado DP, Galler G, et al. (2007). MiR-150 controls B cell diff erentiation by targeting the transcription factor c-Myb. Cell 131: 146-159 https://doi.org/10.1016/j.cell.2007.07.021
  122. Xu P, Guo M, Hay BA. (2004). MicroRNAs and the regulation of cell death. Trends Genet 20: 617-624 https://doi.org/10.1016/j.tig.2004.09.010
  123. Yoo AS, Greenwald I. (2005). LIN-12/Notch activation leads to microRNA-mediated down-regulation of Vav in C. elegans. Science 310: 1330-1333 https://doi.org/10.1126/science.1119481
  124. Yu J, Vodyanik MA, Smuga-Otto K, et al. (2007). Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells. Science 318: 1917-1920 https://doi.org/10.1126/science.1151526
  125. Yu L, Gaskell SJ, Brookman JL. (1998). Epitope mapping of monoclonal antibodies by mass spectrometry: identification of protein antigens in complex biological systems. J Am Soc Mass Spectrom 9: 208-215 https://doi.org/10.1016/S1044-0305(97)00250-X
  126. Zola H, Swart B, Nicholson I, et al. (2005). CD molecules 2005: human cell differentiation molecules. Blood 106: 3123-3126 https://doi.org/10.1182/blood-2005-03-1338
  127. Zola H, Swart BW. (2003). Human leucocyte differentiation antigens. Trends Immunol 24: 353-354 https://doi.org/10.1016/S1471-4906(03)00140-6

Cited by

  1. Improving the outcomes: developing cancer therapeutics vol.8, pp.1, 2010, https://doi.org/10.2217/fon.11.136
  2. Germ Cells are Made Semiotically Competent During Evolution vol.9, pp.1, 2010, https://doi.org/10.1007/s12304-016-9258-3
  3. An integrated network analysis approach to identify potential key genes, transcription factors, and microRNAs regulating human hematopoietic stem cell aging vol.17, pp.6, 2010, https://doi.org/10.1039/d1mo00199j