Genome-wide analysis of immune activation in human T and B cells reveals distinct classes of alternatively spliced genes

PLoS ONE

Volumn 4, Issue 11, 2009, Pages

  Grigoryev, Yevgeniy A ^a   Kurian, Sunil M ^a   Nakorchevskiy, Aleksey A ^a   Burke, John P ^b   Campbell, Daniel ^a   Head, Steve R ^a   Deng, Jun ^c   Kantor, Aaron B ^c,e   Yates III, John R ^a   Salomon, Daniel R ^a,d  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Biotique Systems Inc   (United States)

^c Pharmaceutical Product Development   (United States)

^d SCRIPPS CLINIC   (United States)

^e Immune Tolerance Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; PURINE; T LYMPHOCYTE RECEPTOR; CD19 ANTIGEN; CD2 ANTIGEN; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELLULAR IMMUNITY; CONTROLLED STUDY; GENE ACTIVATION; GENE EXPRESSION; GENE MAPPING; GENOMICS; HUMAN; HUMAN CELL; PROTEIN METABOLISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; BIOLOGICAL MODEL; BIOSYNTHESIS; CYTOLOGY; DNA MICROARRAY; EXON; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; IMMUNE SYSTEM; LYMPHOCYTE ACTIVATION; METABOLISM;

ALTERNATIVE SPLICING; ANTIGENS, CD19; ANTIGENS, CD2; B-LYMPHOCYTES; EXONS; GENE EXPRESSION PROFILING; GENOME-WIDE ASSOCIATION STUDY; HUMANS; IMMUNE SYSTEM; LYMPHOCYTE ACTIVATION; MODELS, BIOLOGICAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 70949104487     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007906     Document Type: Article

References (72)

1. Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72: 291-336.
2. Blencowe BJ (2006) Alternative splicing: new insights from global analyses. Cell 126: 37-47.
3. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413-1415.
4. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, et al. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature.
5. Argyropoulos C, Nikiforidis GC, Theodoropoulou M, Adamopoulos P, Boubali S, et al. (2004) Mining microarray data to identify transcription factors expressed in naive resting but not activated T lymphocytes. Genes Immun 5: 16-25.
6. Baron U, Floess S, Wieczorek G, Baumann K, Grutzkau A, et al. (2007) DNA demethylation in the human FOXP3 locus discriminates regulatory T cells from activated FOXP3(+) conventional T cells. Eur J Immunol 37: 2378-2389.
7. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
8. Blumerman SL, Herzig CT, Wang F, Coussens PM, Baldwin CL (2007) Comparison of gene expression by co-cultured WC1+ gammadelta and CD4+ alphabeta T cells exhibiting a recall response to bacterial antigen. Mol Immunol 44: 2023-2035.
9. Bunting K, Rao S, Hardy K, Woltring D, Denyer GS, et al. (2007) Genome-wide analysis of gene expression in T cells to identify targets of the NF-kappa B transcription factor c-Rel. J Immunol 178: 7097-7109.
10. Chtanova T, Newton R, Liu SM, Weininger L, Young TR, et al. (2005) Identification of T cell-restricted genes, and signatures for different T cell responses, using a comprehensive collection of microarray datasets. J Immunol 175: 7837-7847.
11. Du ZY, Li XY, Li YC, Wang SY (2003) Analysis of triptolide-regulated gene expression in Jurkat cells by complementary DNA microarray. Acta Pharmacol Sin 24: 864-872.
12. Erickson L, Crews G, Pan F, Kobayashi M, Jiang H (2002) Gene expression profiling of acute rejection and mixed lymphocyte reaction with tacrolimus immunosuppression. Transplant Proc 34: 1385-1386.
13. Ferrando AA, Neuberg DS, Staunton J, Loh ML, Huard C, et al. (2002) Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 1: 75-87.
14. Flechner SM, Kurian SM, Head SR, Sharp SM, Whisenant TC, et al. (2004) Kidney transplant rejection and tissue injury by gene profiling of biopsies and peripheral blood lymphocytes. Am J Transplant 4: 1475-1489.
15. Hansel NN, Hilmer SC, Georas SN, Cope LM, Guo J, et al. (2005) Oligonucleotide-microarray analysis of peripheral-blood lymphocytes in severe asthma. J Lab Clin Med 145: 263-274.
16. Hess K, Yang Y, Golech S, Sharov A, Becker KG, et al. (2004) Kinetic assessment of general gene expression changes during human naive CD4+ T cell activation. Int Immunol 16: 1711-1721.
17. Holm AM, Sivertsen EA, Tunheim SH, Haug T, Bjerkeli V, et al. (2004) Gene expression analysis of peripheral T cells in a subgroup of common variable immunodeficiency shows predominance of CCR7(-) effector-memory T cells. Clin Exp Immunol 138: 278-289.
18. Hutton JJ, Jegga AG, Kong S, Gupta A, Ebert C, et al. (2004) Microarray and comparative genomics-based identification of genes and gene regulatory regions of the mouse immune system. BMC Genomics 5: 82.
19. Lee BP, Mansfield E, Hsieh SC, Hernandez-Boussard T, Chen W, et al. (2005) Expression profiling of murine double-negative regulatory T cells suggest mechanisms for prolonged cardiac allograft survival. J Immunol 174: 4535-4544.
20. Li XD, Essayan DM, Liu MC, Beaty TH, Huang SK (2001) Profiling of differential gene expression in activated, allergen-specific human Th2 cells. Genes Immun 2: 88-98.
21. Li Y, Wong KK, Matsueda S, Efferson CL, Chang DZ, et al. (2006) Mitogen stimulation activates different signaling pathways in early- and late-divided T cells as revealed by cDNA microarray analysis. Int J Mol Med 18: 1127-1139.
22. Lin Z, Fillmore GC, Um TH, Elenitoba-Johnson KS, Lim MS (2003) Comparative microarray analysis of gene expression during activation of human peripheral blood T cells and leukemic Jurkat T cells. Lab Invest 83: 765-776.
23. Lu B, Zagouras P, Fischer JE, Lu J, Li B, et al. (2004) Kinetic analysis of genomewide gene expression reveals molecule circuitries that control T cell activation and Th1/2 differentiation. Proc Natl Acad Sci U S A 101: 3023-3028.
24. Manfredini R, Zini R, Salati S, Siena M, Tenedini E, et al. (2005) The kinetic status of hematopoietic stem cell subpopulations underlies a differential expression of genes involved in self-renewal, commitment, and engraftment. Stem Cells 23: 496-506.
25. Marrack P, Mitchell T, Hildeman D, Kedl R, Teague TK, et al. (2000) Genomic-scale analysis of gene expression in resting and activated T cells. Curr Opin Immunol 12: 206-209.
26. Vinuesa CG, Cook MC, Cooke MP, Maclennan IC, Goodnow CC (2002) Analysis of B cell memory formation using DNA microarrays. Ann N Y Acad Sci 975: 33-45.
27. Zhang X, Chen Z, Huang H, Gordon JR, Xiang J (2002) DNA microarray analysis of the gene expression profiles of naive versus activated tumor-specific T cells. Life Sci 71: 3005-3017.
28. Ip JY, Tong A, Pan Q, Topp JD, Blencowe BJ, et al. (2007) Global analysis of alternative splicing during T-cell activation. Rna 13: 563-572.
29. Raghavan A, Ogilvie RL, Reilly C, Abelson ML, Raghavan S, et al. (2002) Genome-wide analysis of mRNA decay in resting and activated primary human T lymphocytes. Nucleic Acids Res 30: 5529-5538.
30. Xu Q, Modrek B, Lee C (2002) Genome-wide detection of tissue-specific alternative splicing in the human transcriptome. Nucleic Acids Res 30: 3754-3766.
31. Lynch KW (2004) Consequences of regulated pre-mRNA splicing in the immune system. Nat Rev Immunol 4: 931-940.
32. Modrek B, Resch A, Grasso C, Lee C (2001) Genome-wide detection of alternative splicing in expressed sequences of human genes. Nucleic Acids Res 29: 2850-2859.
33. Abdueva D, Wing MR, Schaub B, Triche TJ (2007) Experimental comparison and evaluation of the Affymetrix exon and U133Plus2 GeneChip arrays. PLoS ONE 2: e913.
34. French PJ, Peeters J, Horsman S, Duijm E, Siccama I, et al. (2007) Identification of differentially regulated splice variants and novel exons in glial brain tumors using exon expression arrays. Cancer Res 67: 5635-5642.
35. Gardina PJ, Clark TA, Shimada B, Staples MK, Yang Q, et al. (2006) Alternative splicing and differential gene expression in colon cancer detected by a whole genome exon array. BMC Genomics 7: 325.
36. Huang RS, Duan S, Bleibel WK, Kistner EO, Zhang W, et al. (2007) A genome-wide approach to identify genetic variants that contribute to etoposide-induced cytotoxicity. Proc Natl Acad Sci U S A 104: 9758-9763.
37. Kapur K, Xing Y, Ouyang Z, Wong WH (2007) Exon arrays provide accurate assessments of gene expression. Genome Biol 8: R82.
38. Kwan T, Benovoy D, Dias C, Gurd S, Serre D, et al. (2007) Heritability of alternative splicing in the human genome. Genome Res 17: 1210-1218.
39. Mao X, James SY, Yanez-Munoz RJ, Chaplin T, Molloy G, et al. (2007) Rapid high-resolution karyotyping with precise identification of chromosome breakpoints. Genes Chromosomes Cancer 46: 675-683.
40. Okoniewski MJ, Hey Y, Pepper SD, Miller CJ (2007) High correspondence between Affymetrix exon and standard expression arrays. Biotechniques 42: 181-185.
41. Okoniewski MJ, Yates T, Dibben S, Miller CJ (2007) An annotation infrastructure for the analysis and interpretation of Affymetrix exon array data. Genome Biol 8: R79.
42. Xing Y, Kapur K, Wong WH (2006) Probe selection and expression index computation of Affymetrix Exon Arrays. PLoS ONE 1: e88.
43. Xing Y, Ouyang Z, Kapur K, Scott MP, Wong WH (2007) Assessing the conservation of mammalian gene expression using high-density exon arrays. Mol Biol Evol 24: 1283-1285.
44. Yoshida R, Numata K, Imoto S, Nagasaki M, Doi A, et al. (2006) A statistical framework for genome-wide discovery of biomarker splice variations with GeneChip Human Exon 1.0 ST Arrays. Genome Inform 17: 88-99.
45. Huang RS, Duan S, Kistner EO, Zhang W, Bleibel WK, et al. (2008) Identification of genetic variants and gene expression relationships associated with pharmacogenes in humans. Pharmacogenet Genomics 18: 545-549.
46. Clark TA, Schweitzer AC, Chen TX, Staples MK, Lu G, et al. (2007) Discovery of tissue-specific exons using comprehensive human exon microarrays. Genome Biol 8: R64.
47. Thorsen K, Sorensen KD, Brems-Eskildsen AS, Modin C, Gaustadnes M, et al. (2008) Alternative splicing in colon, bladder, and prostate cancer identified by exon-array analysis. Mol Cell Proteomics.
48. Oberdoerffer S ML, Neems D, Freitas RP, Hacohen N, Rao A (2008) Regulation of CD45 alternative splicing by heterogeneous ribonucleoprotein, hnRNPLL. Science 321: 686-691.
49. Rothrock CR, House AE, Lynch KW (2005) HnRNP L represses exon splicing via a regulated exonic splicing silencer. Embo J 24: 2792-2802.
50. Pan Q, Saltzman AL, Kim YK, Misquitta C, Shai O, et al. (2006) Quantitative microarray profiling provides evidence against widespread coupling of alternative splicing with nonsense-mediated mRNA decay to control gene expression. Genes Dev 20: 153-158.
51. Xi L, Feber A, Gupta V, Wu M, Bergemann AD, et al. (2008) Whole genome exon arrays identify differential expression of alternatively spliced, cancer-related genes in lung cancer. Nucleic Acids Res.
52. Cheung HC, Baggerly KA, Tsavachidis S, Bachinski LL, Neubauer VL, et al. (2008) Global analysis of aberrant pre-mRNA splicing in glioblastoma using exon expression arrays. BMC Genomics 9: 216.
53. Ben-Dov C, Hartmann B, Lundgren J, Valcarcel J (2008) Genome-wide analysis of alternative pre-mRNA splicing. J Biol Chem 283: 1229-1233.
54. Johnson MB, Kawasawa YI, Mason CE, Krsnik Z, Coppola G, et al. (2009) Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 62: 494-509.
55. Zhang J, Bardos T, Li D, Gal I, Vermes C, et al. (2002) Cutting edge: regulation of T cell activation threshold by CD28 costimulation through targeting Cbl-b for ubiquitination. J Immunol 169: 2236-2240.
56. Chambers CA (2001) The expanding world of co-stimulation: the two-signal model revisited. Trends Immunol 22: 217-223.
57. Chambers CA, Allison JP (1999) Costimulatory regulation of T cell function. Curr Opin Cell Biol 11: 203-210.
58. Lane P, Traunecker A, Hubele S, Inui S, Lanzavecchia A, et al. (1992) Activated human T cells express a ligand for the human B cell-associated antigen CD40 which participates in T cell-dependent activation of B lymphocytes. Eur J Immunol 22: 2573-2578.
59. Nonoyama S, Hollenbaugh D, Aruffo A, Ledbetter JA, Ochs HD (1993) B cell activation via CD40 is required for specific antibody production by antigen-stimulated human B cells. J Exp Med 178: 1097-1102.
60. Itoh K, Inoue T, Ito K, Hirohata S (1994) The interplay of interleukin-10 (IL-10) and interleukin-2 (IL-2) in humoral immune responses: IL-10 synergizes with IL-2 to enhance responses of human B lymphocytes in a mechanism which is different from upregulation of CD25 expression. Cell Immunol 157: 478-488.
61. Kindler V, Matthes T, Jeannin P, Zubler RH (1995) Interleukin-2 secretion by human B lymphocytes occurs as a late event and requires additional stimulation after CD40 cross-linking. Eur J Immunol 25: 1239-1243.
62. Rousset F, Peyrol S, Garcia E, Vezzio N, Andujar M, et al. (1995) Long-term cultured CD40-activated B lymphocytes differentiate into plasma cells in response to IL-10 but not IL-4. Int Immunol 7: 1243-1253.
63. Kindler V, Zubler RH (1997) Memory, but not naive, peripheral blood B lymphocytes differentiate into Ig-secreting cells after CD40 ligation and costimulation with IL-4 and the differentiation factors IL-2, IL-10, and IL-3. J Immunol 159: 2085-2090.
64. Schilizzi BM, Boonstra R, The TH, de Leij LF (1997) Effect of B-cell receptor engagement on CD40-stimulated B cells. Immunology. .
65. Baumgarth N (2000) A two-phase model of B-cell activation. Immunol Rev 176: 171-180.
66. Moore MJ, Silver PA (2008) Global analysis of mRNA splicing. Rna 14: 197-203.
67. Washburn MP, Wolters D, Yates JR, 3rd (2001) Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19: 242-247.
68. McCormack AL, Schieltz DM, Goode B, Yang S, Barnes G, et al. (1997) Direct analysis and identification of proteins in mixtures by LC/MS/MS and database searching at the low-femtomole level. Anal Chem 69: 767-776.
69. Wolters DA, Washburn MP, Yates JR, 3rd (2001) An automated multidimensional protein identification technology for shotgun proteomics. Anal Chem 73: 5683-5690.
70. Sadygov RG, Eng J, Durr E, Saraf A, McDonald H, et al. (2002) Code developments to improve the efficiency of automated MS/MS spectra interpretation. J Proteome Res 1: 211-215.
71. Tabb DL, McDonald WH, Yates JR, 3rd (2002) DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 1: 21-26.
72. Joshi T, Chen Y, Alexandrov N, Xu D (2004) Cellular function prediction and biological pathway discovery in Arabidopsis thaliana using microarray data. Conf Proc IEEE Eng Med Biol Soc 4: 2881-2884.