Gene expression analysis of whole blood, peripheral blood mononuclear cells, and lymphoblastoid cell lines from the Framingham Heart Study

Physiological Genomics

Volumn 44, Issue 1, 2012, Pages 59-75

  Joehanes, Roby ^a,b   Johnson, Andrew D ^a,b   Barb, Jennifer J ^c   Raghavachari, Nalini ^b   Liu, Poching ^b   Woodhouse, Kimberly A ^b   O'Donnell, Christopher J ^a,b   Munson, Peter J ^c   Levy, Daniel ^a,b  

^a FRAMINGHAM HEART STUDY   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c Division of Computational Bioscience   (United States)

Author keywords

Biomarker discovery; Cardiovascular disease; Data normalization; Fingerprinting genes; Microarray; System biology; X linked expression

Indexed keywords

BIOLOGICAL MARKER; HIGH DENSITY LIPOPROTEIN CHOLESTEROL;

ADULT; AGE DISTRIBUTION; ARTICLE; BLOOD; CARDIOVASCULAR DISEASE; CELL LINE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; HUMAN; LEUKOCYTE DIFFERENTIAL COUNT; LYMPHOBLASTOID CELL; MAJOR CLINICAL STUDY; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; RISK FACTOR; RNA FINGERPRINTING; RNA TRANSCRIPTION; SEX DIFFERENCE; SMOKING; Y CHROMOSOME;

ADULT; BIOLOGICAL MARKERS; BLOOD; CARDIOVASCULAR DISEASES; CELL LINE; COHORT STUDIES; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTES; MALE; MASSACHUSETTS; MICROARRAY ANALYSIS; MIDDLE AGED; PILOT PROJECTS;

EID: 84856021920     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00130.2011     Document Type: Article

References (80)

1. Affymetrix. Transcript assignment for NetAffx(TM) Annotations [online]. http://www.affymetrix.com/support/technical/byproduct.affx?product_huexon-st, 2006.
2. Affymetrix. Quality Assessment of Exon and Gene Arrays, 2007.
3. Affymetrix. GeneChip Whole Transcript (WT) Sense Target Labeling Assay Manual [online]. http://www.affymetrix.com/support/downloads/manuals/wt_sensetarget_label_manual.pdf
4. Affymetrix. Affymetrix Power Tools [online]. http://www.affymetrix-.com/partners_programs/programs/developer/tools/powertools.affx
5. Amos CI, Wu X, Broderick P, Gorlov IP, Gu J, Eisen T, Dong Q, Zhang Q, Gu X, Vijayakrishnan J, Sullivan K, Matakidou A, Wang Y, Mills G, Doheny K, Tsai YY, Chen WV, Shete S, Spitz MR, Houlston RS. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat Genet 40: 616-622, 2008.
6. Asare AL, Kolchinsky SA, Gao Z, Wang R, Raddassi K, Bourcier K, Seyfert-Margolis V. Differential gene expression profiles are dependent upon method of peripheral blood collection and RNA isolation. BMC Genomics 9: 474, 2008.
7. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29, 2000.
8. Avent ND, Reid ME. The Rh blood group system: a review. Blood 95: 375-387, 2000.
9. Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, Shark KB, Grande WJ, Hughes KM, Kapur V, Gregersen PK, Behrens TW. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci USA 100: 2610-2615, 2003.
10. Barr TL, Conley Y, Ding J, Dillman A, Warach S, Singleton A, Matarin M. Genomic biomarkers and cellular pathways of ischemic stroke by RNA gene expression profiling. Neurology 75: 1009-1014, 2010.
11. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B 57: 289-300, 1995.
12. Birkenbach M, Josefsen K, Yalamanchili R, Lenoir G, Kieff E. Epstein-Barr virus-induced genes: first lymphocyte-specific G proteincoupled peptide receptors. J Virol 67: 2209-2220, 1993.
13. Blumenfeld OO, Huang CH. Molecular genetics of the glycophorin gene family, the antigens for MNSs blood groups: multiple gene rearrangements and modulation of splice site usage result in extensive diversification. Hum Mutat 6: 199-209, 1995.
14. Boldrick JC, Alizadeh AA, Diehn M, Dudoit S, Liu CL, Belcher CE, Botstein D, Staudt LM, Brown PO, Relman DA. Stereotyped and specific gene expression programs in human innate immune responses to bacteria. Proc Natl Acad Sci USA 99: 972-977, 2002.
15. Bourke E, Cassetti A, Villa A, Fadlon E, Colotta F, Mantovani A. IL-1 beta scavenging by the type II IL-1 decoy receptor in human neutrophils. J Immunol 170: 5999-6005, 2003.
16. Cain CE, Blekhman R, Marioni JC, Gilad Y. Gene expression differences among primates are associated with changes in a histone epigenetic modification. Genetics 187: 1225-1234, 2011.
17. Caradec J, Sirab N, Keumeugni C, Moutereau S, Chimingqi M, Matar C, Revaud D, Bah M, Manivet P, Conti M, Loric S. "Desperate house genes": the dramatic example of hypoxia. Br J Cancer 102: 1037-1043, 2010.
18. Casabonne D, Reina O, Benavente Y, Becker N, Maynadié M, Foretová L, Cocco P, González-Neira A, Nieters A, Boffetta P, Middeldorp JM, de Sanjose S. Single nucleotide polymorphisms of matrix metalloproteinase 9 (MMP9) and tumor protein 73 (TP73) interact with Epstein-Barr virus in chronic lymphocytic leukemia: results from the European case-control study EpiLymph. Haematologica 96: 323-327, 2011.
19. CDC. Understanding Your Complete Blood Count [online]. http://www.cc.nih.gov/ccc/patient_education/pepubs/cbc97.pdf, 2008.
20. Chen PW, Lin SJ, Tsai SC, Lin JH, Chen MR, Wang JT, Lee CP, Tsai CH. Regulation of microtubule dynamics through phosphorylation on stathmin by Epstein-Barr virus kinase BGLF4. J Biol Chem 285: 10053-10063, 2010.
21. Choy E, Yelensky R, Bonakdar S, Plenge RM, Saxena R, De Jager PL, Shaw SY, Wolfish CS, Slavik JM, Cotsapas C, Rivas M, Dermitzakis ET, Cahir-McFarland E, Kieff E, Hafler D, Daly MJ, Altshuler D. Genetic analysis of human traits in vitro: drug response and gene expression in lymphoblastoid cell lines. PLoS Genet 4: e1000287, 2008.
22. Conboy JG. Structure, function, and molecular genetics of erythroid membrane skeletal protein 4.1 in normal and abnormal red blood cells. Semin Hematol 30: 58-73, 1993.
23. Cox TC, Sadlon TJ, Schwarz QP, Matthews CS, Wise PD, Cox LL, Bottomley SS, May BK. The major splice variant of human 5-aminolevulinate synthase-2 contributes significantly to erythroid heme biosynthesis. Int J Biochem Cell Biol 36: 281-295, 2004.
24. Dawber TR, Meadors GF, Moore FE Jr. Epidemiological approaches to heart disease: the Framingham Study. Am J Public Health Nations Health 41: 279-281, 1951.
25. Debey S, Schoenbeck U, Hellmich M, Gathof BS, Pillai R, Zander T, Schultze JL. Comparison of different isolation techniques prior gene expression profiling of blood derived cells: impact on physiological responses, on overall expression and the role of different cell types. Pharmacogenomics J 4: 193-207, 2004.
26. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48, 2009.
27. Feinleib M, Kannel WB, Garrison RJ, McNamara PM, Castelli WP. The Framingham Offspring Study. Prev Med 4: 518-525, 1975.
28. Fujita K, Horikawa I, Mondal AM, Jenkins LMM, Appella E, Vojtesek B, Bourdon JC, Lane DP, Harris CC. Positive feedback between p53 and TRF2 during telomere-damage signalling and cellular senescence. Nat Cell Biol 12: 1205-1212, 2010.
29. Govindaraju DR, Larson MG, Yin X, Benjamin EJ, Rao MB, Vasan RS. Association between SNP heterozygosity and quantitative traits in the Framingham Heart Study. Ann Hum Genet 73: 465-473, 2009.
30. Grünblatt E, Bartl J, Zehetmayer S, Ringel TM, Bauer P, Riederer P, Jacob CP. Gene expression as peripheral biomarkers for sporadic Alzheimer's disease. J Alzheimers Dis 16: 627-634, 2009.
31. Higgs DR, Vickers MA, Wilkie AO, Pretorius IM, Jarman AP, Weatherall DJ. A review of the molecular genetics of the human alpha-globin gene cluster. Blood 73: 1081-1104, 1989.
32. Hindle AK, Edwards C, McCaffrey T, Fu SW, Brody F. Reactivation of adiponectin expression in obese patients after bariatric surgery. Surg Endosc 24: 1367-1373, 2010.
33. Huang RS, Chen P, Wisel S, Duan S, Zhang W, Cook EH, Das S, Cox NJ, Dolan ME. Population-specific GSTM1 copy number variation. Hum Mol Genet 18: 366-372, 2009.
34. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264, 2003.
35. Isensee J, Witt H, Pregla R, Hetzer R, Regitz-Zagrosek V, Noppinger PR. Sexually dimorphic gene expression in the heart of mice and men. J Mol Med 86: 61-74, 2008.
36. Iyoda T, Ushida M, Kimura Y, Minamino K, Hayuka A, Yokohata S, Ehara H, Inaba K. Invariant NKT cell anergy is induced by a strong TCR-mediated signal plus co-stimulation. Int Immunol 22: 905-913, 2010.
37. Jacobsen LC, Sørensen OE, Cowland JB, Borregaard N, Theilgaard-Mönch K. The secretory leukocyte protease inhibitor (SLPI) and the secondary granule protein lactoferrin are synthesized in myelocytes, colocalize in subcellular fractions of neutrophils, and are coreleased by activated neutrophils. J Leukoc Biol 83: 1155-1164, 2008.
38. Jeon JP, Kim JW, Park B, Nam HY, Shim SM, Lee MH, Han BG. Identification of tumor necrosis factor signaling-related proteins during Epstein-Barr virus-induced B cell transformation. Acta Virol 52: 151-159, 2008.
39. Jison ML, Munson PJ, Barb JJ, Suffredini AF, Talwar S, Logun C, Raghavachari N, Beigel JH, Shelhamer JH, Danner RL, Gladwin MT. Blood mononuclear cell gene expression profiles characterize the oxidant, hemolytic, and inflammatory stress of sickle cell disease. Blood 104: 270-280, 2004.
40. Johnson AD, O'Donnell CJ. An open access database of genome-wide association results. BMC Med Genet 10: 6, 2009.
41. Kashuba E, Yurchenko M, Yenamandra SP, Snopok B, Szekely L, Bercovich B, Ciechanover A, Klein G. Epstein-Barr virus-encoded EBNA-5 forms trimolecular protein complexes with MDM2 and p53 and inhibits the transactivating function of p53. Int J Cancer 128: 817-825, 2011.
42. Khanna-Gupta A, Zibello T, Idone V, Sun H, Lekstrom-Himes J, Berliner N. Human neutrophil collagenase expression is C/EBP-dependent during myeloid development. Exp Hematol 33: 42-52, 2005.
43. Kostylina G, Simon D, Fey MF, Yousefi S, Simon HU. Neutrophil apoptosis mediated by nicotinic acid receptors (GPR109A). Cell Death Differ 15: 134-142, 2008.
44. Lane HC, Anand AR, Ganju RK. Cbl and Akt regulate CXCL8-induced and CXCR1-and CXCR2-mediated chemotaxis. Int Immunol 18: 1315-1325, 2006.
45. Larousserie F, Bardel E, Coulomb L'Herminé A, Canioni D, Brousse N, Kastelein RA, Devergne O. Variable expression of Epstein-Barr virus-induced gene 3 during normal B-cell differentiation and among B-cell lymphomas. J Pathol 209: 360-368, 2006.
46. Li CY, Zhan YQ, Xu CW, Xu WX, Wang SY, Lv J, Zhou Y, Yue PB, Chen B, Yang XM. EDAG regulates the proliferation and differentiation of hematopoietic cells and resists cell apoptosis through the activation of nuclear factor-kappa B. Cell Death Differ 11: 1299-1308, 2004.
47. Malossini A, Blanzieri E, Ng RT. Assessment of SVM reliability of microarrays data analysis. 14th Dutch-Belgian Conference of Machine Learning. WP05-03, 2005.
48. Mason CC, Hanson RL, Ossowski V, Bian L, Baier LJ, Krakoff J, Bogardus C. Bimodal distribution of RNA expression levels in human skeletal muscle tissue. BMC Genomics 12: 98, 2011.
49. McLaren JE, Zuo J, Grimstead J, Poghosyan Z, Bell AI, Rowe M, Brennan P. STAT1 contributes to the maintenance of the latency III viral programme observed in Epstein-Barr virus-transformed B cells and their recognition by CD8 T cells. J Gen Virol 90: 2239-2250, 2009.
50. Min JL, Barrett A, Watts T, Pettersson FH, Lockstone HE, Lindgren CM, Taylor JM, Allen M, Zondervan KT, McCarthy MI. Variability of gene expression profiles in human blood and lymphoblastoid cell lines. BMC Genomics 11: 96, 2010.
51. Mohan J, Dement-Brown J, Maier S, Ise T, Kempkes B, Tolnay M. Epstein-Barr virus nuclear antigen 2 induces FcRH5 expression through CBF1. Blood 107: 4433-4439, 2006.
52. Munson PJ. A consistency test for determining the significance of gene expression changes on replicate samples and two convenient variancestabilizing transformations [online]. GeneLogic Workshop on Low Level Analysis of Affymetrix GeneChip Data. http://stat-www.berkeley.edu/ users/terry/zarray/Affy/GL_Workshop/genelogic2001.html.
53. Murtagh F. Multidimensional Clustering Algorithms. Würzburg: Physica-Verlag, 1985.
54. O'Donnell CJ, Elosua R. Cardiovascular risk factors. Insights from Framingham Heart Study. Rev Esp Cardiol 61: 299-310, 2008.
55. Oppenheimer GM. Becoming the Framingham Study 1947-1950. Am J Public Health 95: 602-610, 2005.
56. Palikhe NS, Kim JH, Park HS. Biomarkers predicting isocyanateinduced asthma. Allergy Asthma Immunol Res 3: 21-26, 2011.
57. Park JY, Matsuo K, Suzuki T, Ito H, Hosono S, Kawase T, Watanabe M, Oze I, Hida T, Yatabe Y, Mitsudomi T, Takezaki T, Tajima K, Tanaka H. Impact of smoking on lung cancer risk is stronger in those with the homozygous aldehyde dehydrogenase 2 null allele in a Japanese population. Carcinogenesis 31: 660-665, 2010.
58. Pickrell JK, Marioni JC, Pai AA, Degner JF, Engelhardt BE, Nkadori E, Veyrieras JB, Stephens M, Gilad Y, Pritchard JK. Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464: 768-772, 2010.
59. Pinheiro J, Bates D. Mixed-effects Models in S and S-PLUS. New York: Springer, 2009.
60. Provan S, Angel K, Semb AG, Atar D, Kvien TK. NT-proBNP predicts mortality in patients with rheumatoid arthritis: results from 10-year follow-up of the EURIDISS study. Ann Rheum Dis 69: 1946-1950, 2010.
61. QIAGEN. RNeasy Plus Handbook [online]. http://www.qiagen.com/literature/render.aspx?id_103686.
62. QIAGEN. PAXgene Blood RNA Kit Handbook Version 2 [online]. http://www.qiagen.com/literature/render.aspx?id_104458.
63. R Development Core Team. R: A Language and Environment for Statistical Computing [online]. http://www.R-project.org.
64. Raghavachari N, Xu X, Harris A, Villagra J, Logun C, Barb J, Solomon MA, Suffredini AF, Danner RL, Kato G, Munson PJ, Morris SM Jr, Gladwin MT. Amplified expression profiling of platelet transcriptome reveals changes in arginine metabolic pathways in patients with sickle cell disease. Circulation 115: 1551-1562, 2007.
65. Rana AP, Ruff P, Maalouf GJ, Speicher DW, Chishti AH. Cloning of human erythroid dematin reveals another member of the villin family. Proc Natl Acad Sci USA 90: 6651-6655, 1993.
66. Rockett JC, Burczynski ME, Fornace AJ, Herrmann PC, Krawetz SA, Dix DJ. Surrogate tissue analysis: monitoring toxicant exposure and health status of inaccessible tissues through the analysis of accessible tissues and cells. Toxicol Appl Pharmacol 194: 189-199, 2004.
67. Rollins B, Martin MV, Morgan L, Vawter MP. Analysis of whole genome biomarker expression in blood and brain. Am J Med Genet B Neuropsychiatr Genet 153B: 919-936, 2010.
68. Rowe M, Lear AL, Croom-Carter D, Davies AH, Rickinson AB. Three pathways of Epstein-Barr virus gene activation from EBNA1-positive latency in B lymphocytes. J Virol 66: 122-131, 1992.
69. Rybicki AC, Musto S, Schwartz RS. Identification of a band-3 binding site near the N-terminus of erythrocyte membrane protein 4.2. Biochem J 309: 677-681, 1995.
70. Schaniel C, Rolink AG, Melchers F. Attractions and migrations of lymphoid cells in the organization of humoral immune responses. Adv Immunol 78: 111-168, 2001.
71. Splansky GL, Corey D, Yang Q, Atwood LD, Cupples LA, Benjamin EJ, D'Agostino RB, Fox CS, Larson MG, Murabito JM, O'Donnell CJ, Vasan RS, Wolf PA, Levy D. The third generation cohort of the National Heart, Lung, and Blood Institute's Framingham Heart Study: design, recruitment, and initial examination. Am J Epidemiol 165: 1328-1335, 2007.
72. Stamm S, Riethoven JJ, Le Texier V, Gopalakrishnan C, Kumanduri V, Tang Y, Barbosa-Morais NL, Thanaraj TA. ASD: a bioinformatics resource on alternative splicing. Nucleic Acids Res 34: D46-D55, 2006.
73. Stanietsky N, Mandelboim O. Paired NK cell receptors controlling NK cytotoxicity. FEBS Lett 584: 4895-4900, 2010.
74. Tanner MJ. Molecular and cellular biology of the erythrocyte anion exchanger (AE1). Semin Hematol 30: 34-57, 1993.
75. Twine NC, Stover JA, Marshall B, Dukart G, Hidalgo M, Stadler W, Logan T, Dutcher J, Hudes G, Dorner AJ, Slonim DK, Trepicchio WL, Burczynski ME. Disease-associated expression profiles in peripheral blood mononuclear cells from patients with advanced renal cell carcinoma. Cancer Res 63: 6069-6075, 2003.
76. Venables WN, Ripley BD. Modern Applied Statistics With S (4th ed.). New York: Springer, 2002.
77. Wallace AE, Sales KJ, Catalano RD, Anderson RA, Williams ARW, Wilson MR, Schwarze J, Wang H, Rossi AG, Jabbour HN. Prostaglandin F2alpha-F-prostanoid receptor signaling promotes neutrophil chemotaxis via chemokine (C-X-C motif) ligand 1 in endometrial adenocarcinoma. Cancer Res 69: 5726-5733, 2009.
78. Waterworth DM, Ricketts SL, Song K, Chen L, Zhao JH, Ripatti S, Aulchenko YS, Zhang W, Yuan X, Lim N, Luan J, Ashford S, Wheeler E, Young EH, Hadley D, Thompson JR, Braund PS, Johnson T, Struchalin M, Surakka I, Luben R, Khaw KT, Rodwell SA, Loos RJF, Boekholdt SM, Inouye M, Deloukas P, Elliott P, Schlessinger D, Sanna S, Scuteri A, Jackson A, Mohlke KL, Tuomilehto J, Roberts R, Stewart A, Kesäniemi YA, Mahley RW, Grundy SM, McArdle W, Cardon L, Waeber G, Vollenweider P, Chambers JC, Boehnke M, Abecasis GR, Salomaa V, Järvelin MR, Ruokonen A, Barroso I, Epstein SE, Hakonarson HH, Rader DJ, Reilly MP, Witteman JCM, Hall AS, Samani NJ, Strachan DP, Barter P, van Duijn CM, Kooner JS, Peltonen L, Wareham NJ, McPherson R, Mooser V, Sandhu MS. Genetic variants influencing circulating lipid levels and risk of coronary artery disease. Arterioscler Thromb Vasc Biol 30: 2264-2276, 2010.
79. West M, Blanchette C, Dressman H, Huang E, Ishida S, Spang R, Zuzan H, Olson JA Jr, Marks JR, Nevins JR. Predicting the clinical status of human breast cancer by using gene expression profiles. Proc Natl Acad Sci USA 98: 11462-11467, 2001.
80. Whitney AR, Diehn M, Popper SJ, Alizadeh AA, Boldrick JC, Relman DA, Brown PO. Individuality and variation in gene expression patterns in human blood. Proc Natl Acad Sci USA 100: 1896-1901, 2003.