Genome-wide Trans-ethnic Meta-analysis Identifies Seven Genetic Loci Influencing Erythrocyte Traits and a Role for RBPMS in Erythropoiesis

American Journal of Human Genetics

Volumn 100, Issue 1, 2017, Pages 51-63

  van Rooij, Frank J A ^a   Qayyum, Rehan ^b   Smith, Albert V ^c,d   Zhou, Yi ^e,f   Trompet, Stella ^g   Tanaka, Toshiko ^h   Keller, Margaux F ^h   Chang, Li Ching ⁱ   Schmidt, Helena ^j   Yang, Min Lee ^k   Chen, Ming Huei ^l,m   Hayes, James ⁿ   Johnson, Andrew D ^m   Yanek, Lisa R ^b   Mueller, Christian ^o,z   Lange, Leslie ^p   Floyd, James S ^q   Ghanbari, Mohsen ^a,r   Zonderman, Alan B ^h   Jukema, J Wouter ^g   Hofman, Albert ^a,s   van Duijn, Cornelia M ^a   Desch, Karl C ^k   Saba, Yasaman ^j   Ozel, Ayse B ^k   Snively, Beverly M ^t   Wu, Jer Yuarn ^i,u   Schmidt, Reinhold ^j   Fornage, Myriam ^v   Klein, Robert J ⁿ   Fox, Caroline S ^m   Matsuda, Koichi ^w   Kamatani, Naoyuki ^x   Wild, Philipp S ^y,z   Stott, David J ^aa   Ford, Ian ^aa   Slagboom, P Eline ^g   Yang, Jaden ^ab   Chu, Audrey Y ^ac   Lambert, Amy J ^ad   Uitterlinden, André G ^a   Franco, Oscar H ^a   Hofer, Edith ^j   Ginsburg, David ^k   Hu, Bella ^e,f   Keating, Brendan ^ae,af   Schick, Ursula M ^n,ag   Brody, Jennifer A ^q   Li, Jun Z ^k   Chen, Zhao ^ah   Zeller, Tanja ^o,z   Guralnik, Jack M ^ai   Chasman, Daniel I ^ac   Peters, Luanne L ^ad   Kubo, Michiaki ^x   Becker, Diane M ^b   Li, Jin ^ab   Eiriksdottir, Gudny ^d   Rotter, Jerome I ^aj   Levy, Daniel ^m   Grossmann, Vera ^y   Patel, Kushang V ^h   Chen, Chien Hsiun ^i,u   Ridker, Paul M ^ac   Tang, Hua ^ab   Launer, Lenore J ^h   Rice, Kenneth M ^q   Li Gao, Ruifang ^g   Ferrucci, Luigi ^h   Evans, Michelle K ^h   Choudhuri, Avik ^e,f   Trompouki, Eirini ^f,ak   Abraham, Brian J ^al   Yang, Song ^e,f   Takahashi, Atsushi ^x   Kamatani, Yoichiro ^x   Kooperberg, Charles ^ag   Harris, Tamara B ^h   Jee, Sun Ha ^am   Coresh, Josef ^an   Tsai, Fuu Jen ^u   Longo, Dan L ^h   Chen, Yuan Tsong ⁱ   Felix, Janine F ^a   Yang, Qiong ^m,ao   Psaty, Bruce M ^q,ap   Boerwinkle, Eric ^v   Becker, Lewis C ^b   Mook Kanamori, Dennis O ^g,aq   Wilson, James G ^ar   Gudnason, Vilmundur ^c,d   O'Donnell, Christopher J ^m   Dehghan, Abbas ^a,as   Cupples, L Adrienne ^m,ao   Nalls, Michael A ^h   Morris, Andrew P ^at,au   Okada, Yukinori ^x,av   Reiner, Alexander P ^q,ag   Zon, Leonard I ^e,f   Ganesh, Santhi K ^k   more..

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ICELAND   (Iceland)

^d ICELANDIC HEART ASSOCIATION   (Iceland)

^e HARVARD UNIVERSITY   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^h NATIONAL INSTITUTE ON AGING   (United States)

ⁱ INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^j MEDICAL UNIVERSITY OF GRAZ   (Austria)

^k UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^l BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

ⁿ MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^o UNIVERSITY HEART CENTER HAMBURG   (Germany)

^p UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^q UNIVERSITY OF WASHINGTON   (United States)

^r MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^s HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^t WAKE FOREST SCHOOL OF MEDICINE   (United States)

^u CHINA MEDICAL UNIVERSITY   (Taiwan)

^v UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^w UNIVERSITY OF TOKYO   (Japan)

^x RIKEN Center for Integrative Medical Sciences   (Japan)

^y UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^z DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^aa UNIVERSITY OF GLASGOW   (United Kingdom)

^ab STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^ac BRIGHAM AND WOMEN S HOSPITAL   (United States)

^ad JACKSON LABORATORY   (United States)

^ae CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^af UNIVERSITY OF PENNSYLVANIA   (United States)

^ag Fred Hutchinson Cancer Research Center   (United States)

^ah UNIVERSITY OF ARIZONA   (United States)

^ai UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^aj HARBOR UCLA MEDICAL CENTER   (United States)

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

^al WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^am Yonsei University   (South Korea)

^an JOHNS HOPKINS UNIVERSITY   (United States)

^ao BOSTON UNIVERSITY SCHOOL OF PUBLIC HEALTH   (United States)

^ap CENTER FOR HEALTH STUDIES   (United States)

^aq KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^ar UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^as IMPERIAL COLLEGE LONDON   (United Kingdom)

^at UNIVERSITY OF LIVERPOOL   (United Kingdom)

^au UNIVERSITY OF OXFORD   (United Kingdom)

^av OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

RBPMS PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; RBPMS PROTEIN, HUMAN; RNA BINDING PROTEIN;

AFRICAN; ANCESTRY GROUP; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; EAST ASIAN; EMBRYO; ERYTHROCYTE; ERYTHROPOIESIS; ETHNIC DIFFERENCE; EUROPEAN; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENE MAPPING; GENE REPLICATION; GENETIC IDENTIFICATION; GENOME-WIDE ASSOCIATION STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MEAN CORPUSCULAR HEMOGLOBIN; MEAN CORPUSCULAR VOLUME; MOUSE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; ZEBRA FISH; AFRICA; ALLELE; ANIMAL; BAYES THEOREM; ETHNIC GROUP; ETHNOLOGY; EUROPE; FAR EAST; FEMALE; GENETICS; MALE; META ANALYSIS; METABOLISM;

AFRICA; ALLELES; ANIMALS; BAYES THEOREM; CONTINENTAL POPULATION GROUPS; ERYTHROCYTES; ERYTHROPOIESIS; ETHNIC GROUPS; EUROPE; FAR EAST; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LINKAGE DISEQUILIBRIUM; MALE; RNA-BINDING PROTEINS; ZEBRAFISH;

EID: 85009756485     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.11.016     Document Type: Article

References (67)

1. 1 Koury, M.J., Abnormal erythropoiesis and the pathophysiology of chronic anemia. Blood Rev. 28 (2014), 49–66.
2. 2 Whitfield, J.B., Martin, N.G., Genetic and environmental influences on the size and number of cells in the blood. Genet. Epidemiol. 2 (1985), 133–144.
3. 3 Evans, D.M., Frazer, I.H., Martin, N.G., Genetic and environmental causes of variation in basal levels of blood cells. Twin Res. 2 (1999), 250–257.
4. 4 Lin, J.-P., O'Donnell, C.J., Jin, L., Fox, C., Yang, Q., Cupples, L.A., Evidence for linkage of red blood cell size and count: genome-wide scans in the Framingham Heart Study. Am. J. Hematol. 82 (2007), 605–610.
5. 5 Guindo, A., Fairhurst, R.M., Doumbo, O.K., Wellems, T.E., Diallo, D.A., X-linked G6PD deficiency protects hemizygous males but not heterozygous females against severe malaria. PLoS Med., 4, 2007, e66.
6. 6 Tishkoff, S.A., Varkonyi, R., Cahinhinan, N., Abbes, S., Argyropoulos, G., Destro-Bisol, G., Drousiotou, A., Dangerfield, B., Lefranc, G., Loiselet, J., et al. Haplotype diversity and linkage disequilibrium at human G6PD: recent origin of alleles that confer malarial resistance. Science 293 (2001), 455–462.
7. 7 Lo, K.S., Wilson, J.G., Lange, L.A., Folsom, A.R., Galarneau, G., Ganesh, S.K., Grant, S.F.A., Keating, B.J., McCarroll, S.A., Mohler, E.R. 3rd, et al. Genetic association analysis highlights new loci that modulate hematological trait variation in Caucasians and African Americans. Hum. Genet. 129 (2011), 307–317.
8. 8 Ganesh, S.K., Zakai, N.A., van Rooij, F.J.A., Soranzo, N., Smith, A.V., Nalls, M.A., Chen, M.-H., Kottgen, A., Glazer, N.L., Dehghan, A., et al. Multiple loci influence erythrocyte phenotypes in the CHARGE Consortium. Nat. Genet. 41 (2009), 1191–1198.
9. 9 Soranzo, N., Spector, T.D., Mangino, M., Kühnel, B., Rendon, A., Teumer, A., Willenborg, C., Wright, B., Chen, L., Li, M., et al. A genome-wide meta-analysis identifies 22 loci associated with eight hematological parameters in the HaemGen consortium. Nat. Genet. 41 (2009), 1182–1190.
10. 10 van der Harst, P., Zhang, W., Mateo Leach, I., Rendon, A., Verweij, N., Sehmi, J., Paul, D.S., Elling, U., Allayee, H., Li, X., et al. Seventy-five genetic loci influencing the human red blood cell. Nature 492 (2012), 369–375.
11. 11 Kamatani, Y., Matsuda, K., Okada, Y., Kubo, M., Hosono, N., Daigo, Y., Nakamura, Y., Kamatani, N., Genome-wide association study of hematological and biochemical traits in a Japanese population. Nat. Genet. 42 (2010), 210–215.
12. 12 Chen, Z., Tang, H., Qayyum, R., Schick, U.M., Nalls, M.A., Handsaker, R., Li, J., Lu, Y., Yanek, L.R., Keating, B., et al. BioBank Japan Project, CHARGE Consortium. Genome-wide association analysis of red blood cell traits in African Americans: the COGENT Network. Hum. Mol. Genet. 22 (2013), 2529–2538.
13. 13 Franceschini, N., van Rooij, F.J.A., Prins, B.P., Feitosa, M.F., Karakas, M., Eckfeldt, J.H., Folsom, A.R., Kopp, J., Vaez, A., Andrews, J.S., et al., LifeLines Cohort Study. Discovery and fine mapping of serum protein loci through transethnic meta-analysis. Am. J. Hum. Genet. 91 (2012), 744–753.
14. 14 Nalls, M.A., Couper, D.J., Tanaka, T., van Rooij, F.J.A., Chen, M.-H., Smith, A.V., Toniolo, D., Zakai, N.A., Yang, Q., Greinacher, A., et al. Multiple loci are associated with white blood cell phenotypes. PLoS Genet., 7, 2011, e1002113.
15. 15 Chen, P., Takeuchi, F., Lee, J.-Y., Li, H., Wu, J.-Y., Liang, J., Long, J., Tabara, Y., Goodarzi, M.O., Pereira, M.A., et al., CHARGE Hematology Working Group. Multiple nonglycemic genomic loci are newly associated with blood level of glycated hemoglobin in East Asians. Diabetes 63 (2014), 2551–2562.
16. 16 Wild, P.S., Zeller, T., Beutel, M., Blettner, M., Dugi, K.A., Lackner, K.J., Pfeiffer, N., Münzel, T., Blankenberg, S., Die Gutenberg Gesundheitsstudie. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 55 (2012), 824–829.
17. 17 Desch, K.C., Ozel, A.B., Siemieniak, D., Kalish, Y., Shavit, J.A., Thornburg, C.D., Sharathkumar, A.A., McHugh, C.P., Laurie, C.C., Crenshaw, A., et al. Linkage analysis identifies a locus for plasma von Willebrand factor undetected by genome-wide association. Proc. Natl. Acad. Sci. USA 110 (2013), 588–593.
18. 18 de Mutsert, R., den Heijer, M., Rabelink, T.J., Smit, J.W.A., Romijn, J.A., Jukema, J.W., de Roos, A., Cobbaert, C.M., Kloppenburg, M., le Cessie, S., et al. The Netherlands Epidemiology of Obesity (NEO) study: study design and data collection. Eur. J. Epidemiol. 28 (2013), 513–523.
19. 19 Ridker, P.M., JUPITER Study Group. Rosuvastatin in the primary prevention of cardiovascular disease among patients with low levels of low-density lipoprotein cholesterol and elevated high-sensitivity C-reactive protein: rationale and design of the JUPITER trial. Circulation 108 (2003), 2292–2297.
20. 20 Qayyum, R., Snively, B.M., Ziv, E., Nalls, M.A., Liu, Y., Tang, W., Yanek, L.R., Lange, L., Evans, M.K., Ganesh, S., et al. A meta-analysis and genome-wide association study of platelet count and mean platelet volume in african americans. PLoS Genet., 8, 2012, e1002491.
21. 21 Reiner, A.P., Lettre, G., Nalls, M.A., Ganesh, S.K., Mathias, R., Austin, M.A., Dean, E., Arepalli, S., Britton, A., Chen, Z., et al. Genome-wide association study of white blood cell count in 16,388 African Americans: the continental origins and genetic epidemiology network (COGENT). PLoS Genet., 7, 2011, e1002108.
22. 22 Willer, C.J., Li, Y., Abecasis, G.R., METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 26 (2010), 2190–2191.
23. 23 Devlin, B., Roeder, K., Wasserman, L., Genomic control, a new approach to genetic-based association studies. Theor. Popul. Biol. 60 (2001), 155–166.
24. 24 Morris, A.P., Transethnic meta-analysis of genomewide association studies. Genet. Epidemiol. 35 (2011), 809–822.
25. 25 Han, B., Eskin, E., Random-effects model aimed at discovering associations in meta-analysis of genome-wide association studies. Am. J. Hum. Genet. 88 (2011), 586–598.
26. 26 Li, J., Ji, L., Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix. Heredity (Edinb) 95 (2005), 221–227.
27. 27 Wang, X., Chua, H.-X., Chen, P., Ong, R.T.-H., Sim, X., Zhang, W., Takeuchi, F., Liu, X., Khor, C.-C., Tay, W.-T., et al. Comparing methods for performing trans-ethnic meta-analysis of genome-wide association studies. Hum. Mol. Genet. 22 (2013), 2303–2311.
28. 28 Maller, J.B., McVean, G., Byrnes, J., Vukcevic, D., Palin, K., Su, Z., Howson, J.M., Auton, A., Myers, S., Morris, A., et al., Wellcome Trust Case Control Consortium. Bayesian refinement of association signals for 14 loci in 3 common diseases. Nat. Genet. 44 (2012), 1294–1301.
29. 29 The ENCODE Project Consortium. A user's guide to the Encyclopedia of DNA Elements (ENCODE). PLoS Biol., 2011, 10.1371/journal.pbio.1001046 Published online April 19, 2011.
30. 30 Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., Schilling, T.F., Stages of embryonic development of the zebrafish. Dev. Dyn. 203 (1995), 253–310.
31. 31 Huang, H.-T., Kathrein, K.L., Barton, A., Gitlin, Z., Huang, Y.-H., Ward, T.P., Hofmann, O., Dibiase, A., Song, A., Tyekucheva, S., et al. A network of epigenetic regulators guides developmental haematopoiesis in vivo. Nat. Cell Biol. 15 (2013), 1516–1525.
32. 32 Lee, T.I., Johnstone, S.E., Young, R.A., Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 1 (2006), 729–748.
33. 33 Trompouki, E., Bowman, T.V., Lawton, L.N., Fan, Z.P., Wu, D.-C., DiBiase, A., Martin, C.S., Cech, J.N., Sessa, A.K., Leblanc, J.L., et al. Lineage regulators direct BMP and Wnt pathways to cell-specific programs during differentiation and regeneration. Cell 147 (2011), 577–589.
34. 34 Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L., Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, 2009, R25.
35. 35 Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., Liu, X.S., Model-based analysis of ChIP-Seq (MACS). Genome Biol., 9, 2008, R137.
36. 36 Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., Mesirov, J.P., Integrative genomics viewer. Nat. Biotechnol. 29 (2011), 24–26.
37. 37 Thorvaldsdóttir, H., Robinson, J.T., Mesirov, J.P., Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14 (2013), 178–192.
38. 38 Peters, L.L., Shavit, J.A., Lambert, A.J., Tsaih, S.-W., Li, Q., Su, Z., Leduc, M.S., Paigen, B., Churchill, G.A., Ginsburg, D., Brugnara, C., Sequence variation at multiple loci influences red cell hemoglobin concentration. Blood 116 (2010), e139–e149.
39. 39 Broman, K.W., Wu, H., Sen, S., Churchill, G.A., R/qtl: QTL mapping in experimental crosses. Bioinformatics 19 (2003), 889–890.
40. 40 Cox, A., Ackert-Bicknell, C.L., Dumont, B.L., Ding, Y., Bell, J.T., Brockmann, G.A., Wergedal, J.E., Bult, C., Paigen, B., Flint, J., et al. A new standard genetic map for the laboratory mouse. Genetics 182 (2009), 1335–1344.
41. 41 Churchill, G.A., Doerge, R.W., Empirical threshold values for quantitative trait mapping. Genetics 138 (1994), 963–971.
42. 42 Sen, S., Churchill, G.A., A statistical framework for quantitative trait mapping. Genetics 159 (2001), 371–387.
43. 43 Chambers, J.C., Zhang, W., Li, Y., Sehmi, J., Wass, M.N., Zabaneh, D., Hoggart, C., Bayele, H., McCarthy, M.I., Peltonen, L., et al. Genome-wide association study identifies variants in TMPRSS6 associated with hemoglobin levels. Nat. Genet. 41 (2009), 1170–1172.
44. 44 Ding, K., de Andrade, M., Manolio, T.A., Crawford, D.C., Rasmussen-Torvik, L.J., Ritchie, M.D., Denny, J.C., Masys, D.R., Jouni, H., Pachecho, J.A., et al. Genetic variants that confer resistance to malaria are associated with red blood cell traits in African-Americans: an electronic medical record-based genome-wide association study. G3 (Bethesda) 3 (2013), 1061–1068.
45. 45 Kullo, I.J., Ding, K., Jouni, H., Smith, C.Y., Chute, C.G., A genome-wide association study of red blood cell traits using the electronic medical record. PLoS ONE, 5, 2010, e13011.
46. 46 Li, J., Glessner, J.T., Zhang, H., Hou, C., Wei, Z., Bradfield, J.P., Mentch, F.D., Guo, Y., Kim, C., Xia, Q., et al. GWAS of blood cell traits identifies novel associated loci and epistatic interactions in Caucasian and African-American children. Hum. Mol. Genet. 22 (2013), 1457–1464.
47. 47 Pistis, G., Okonkwo, S.U., Traglia, M., Sala, C., Shin, S.-Y., Masciullo, C., Buetti, I., Massacane, R., Mangino, M., Thein, S.-L., et al., CHARGE Consortium Hematology Working. Genome wide association analysis of a founder population identified TAF3 as a gene for MCHC in humans. PLoS ONE, 8, 2013, e69206.
48. 48 CHARGE Consortium Hematology Working Group. Meta-analysis of rare and common exome chip variants identifies S1PR4 and other loci influencing blood cell traits. Nat. Genet. 48 (2016), 867–876.
49. 49 Richardson, K., Louie-Gao, Q., Arnett, D.K., Parnell, L.D., Lai, C.-Q., Davalos, A., Fox, C.S., Demissie, S., Cupples, L.A., Fernandez-Hernando, C., Ordovas, J.M., The PLIN4 variant rs8887 modulates obesity related phenotypes in humans through creation of a novel miR-522 seed site. PLoS ONE, 6, 2011, e17944.
50. 50 Williams, Z., Ben-Dov, I.Z., Elias, R., Mihailovic, A., Brown, M., Rosenwaks, Z., Tuschl, T., Comprehensive profiling of circulating microRNA via small RNA sequencing of cDNA libraries reveals biomarker potential and limitations. Proc. Natl. Acad. Sci. USA 110 (2013), 4255–4260.
51. 51 Shimamoto, A., Kitao, S., Ichikawa, K., Suzuki, N., Yamabe, Y., Imamura, O., Tokutake, Y., Satoh, M., Matsumoto, T., Kuromitsu, J., et al. A unique human gene that spans over 230 kb in the human chromosome 8p11-12 and codes multiple family proteins sharing RNA-binding motifs. Proc. Natl. Acad. Sci. USA 93 (1996), 10913–10917.
52. 52 Ascano, M., Hafner, M., Cekan, P., Gerstberger, S., Tuschl, T., Identification of RNA-protein interaction networks using PAR-CLIP. Wiley Interdiscip. Rev. RNA 3 (2012), 159–177.
53. 53 Trakarnsanga, K., Wilson, M.C., Griffiths, R.E., Toye, A.M., Carpenter, L., Heesom, K.J., Parsons, S.F., Anstee, D.J., Frayne, J., Qualitative and quantitative comparison of the proteome of erythroid cells differentiated from human iPSCs and adult erythroid cells by multiplex TMT labelling and nanoLC-MS/MS. PLoS ONE, 9, 2014, e100874.
54. 54 Kingsley, P.D., Greenfest-Allen, E., Frame, J.M., Bushnell, T.P., Malik, J., McGrath, K.E., Stoeckert, C.J., Palis, J., Ontogeny of erythroid gene expression. Blood 121 (2013), e5–e13.
55. 55 Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R.C., Melton, D.A., “Stemness”: transcriptional profiling of embryonic and adult stem cells. Science 298 (2002), 597–600.
56. 56 Georgantas, R.W. 3rd, Tanadve, V., Malehorn, M., Heimfeld, S., Chen, C., Carr, L., Martinez-Murillo, F., Riggins, G., Kowalski, J., Civin, C.I., Microarray and serial analysis of gene expression analyses identify known and novel transcripts overexpressed in hematopoietic stem cells. Cancer Res. 64 (2004), 4434–4441.
57. 57 Wagner, W., Ansorge, A., Wirkner, U., Eckstein, V., Schwager, C., Blake, J., Miesala, K., Selig, J., Saffrich, R., Ansorge, W., Ho, A.D., Molecular evidence for stem cell function of the slow-dividing fraction among human hematopoietic progenitor cells by genome-wide analysis. Blood 104 (2004), 675–686.
58. 58 Sun, Y., Ding, L., Zhang, H., Han, J., Yang, X., Yan, J., Zhu, Y., Li, J., Song, H., Ye, Q., Potentiation of Smad-mediated transcriptional activation by the RNA-binding protein RBPMS. Nucleic Acids Res. 34 (2006), 6314–6326.
59. 59 He, W., Dorn, D.C., Erdjument-Bromage, H., Tempst, P., Moore, M.A.S., Massagué, J., Hematopoiesis controlled by distinct TIF1γ and Smad4 branches of the TGFbeta pathway. Cell 125 (2006), 929–941.
60. 60 Shin, S.-Y., Fauman, E.B., Petersen, A.-K., Krumsiek, J., Santos, R., Huang, J., Arnold, M., Erte, I., Forgetta, V., Yang, T.-P., et al., Multiple Tissue Human Expression Resource (MuTHER) Consortium. An atlas of genetic influences on human blood metabolites. Nat. Genet. 46 (2014), 543–550.
61. 61 Comuzzie, A.G., Cole, S.A., Laston, S.L., Voruganti, V.S., Haack, K., Gibbs, R.A., Butte, N.F., Novel genetic loci identified for the pathophysiology of childhood obesity in the Hispanic population. PLoS ONE, 7, 2012, e51954.
62. 62 Nalls, M.A., Plagnol, V., Hernandez, D.G., Sharma, M., Sheerin, U.M., Saad, M., Simón-Sánchez, J., Schulte, C., Lesage, S., Sveinbjörnsdóttir, S., et al., International Parkinson Disease Genomics Consortium. Imputation of sequence variants for identification of genetic risks for Parkinson's disease: a meta-analysis of genome-wide association studies. Lancet 377 (2011), 641–649.
63. 63 Otsuki, M., Fukami, K., Kohno, T., Yokota, J., Takenawa, T., Identification and characterization of a new phospholipase C-like protein, PLC-L(2). Biochem. Biophys. Res. Commun. 266 (1999), 97–103.
64. 64 Sankaran, V.G., Ludwig, L.S., Sicinska, E., Xu, J., Bauer, D.E., Eng, J.C., Patterson, H.C., Metcalf, R.A., Natkunam, Y., Orkin, S.H., et al. Cyclin D3 coordinates the cell cycle during differentiation to regulate erythrocyte size and number. Genes Dev. 26 (2012), 2075–2087.
65. 65 Keller, M.F., Reiner, A.P., Okada, Y., van Rooij, F.J.A., Johnson, A.D., Chen, M.-H., Smith, A.V., Morris, A.P., Tanaka, T., Ferrucci, L., et al. CHARGE Hematology COGENT, BioBank Japan Project (RIKEN) Working Groups. Trans-ethnic meta-analysis of white blood cell phenotypes. Hum. Mol. Genet. 23 (2014), 6944–6960.
66. 66 Dastani, Z., Hivert, M.-F., Timpson, N., Perry, J.R.B., Yuan, X., Scott, R.A., Henneman, P., Heid, I.M., Kizer, J.R., Lyytikäinen, L.-P., et al. DIAGRAM+ Consortium MAGIC Consortium GLGC Investigators MuTHER Consortium DIAGRAM Consortium GIANT Consortium Global B Pgen Consortium Procardis Consortium MAGIC investigators, GLGC Consortium. Novel loci for adiponectin levels and their influence on type 2 diabetes and metabolic traits: a multi-ethnic meta-analysis of 45,891 individuals. PLoS Genet., 8, 2012, e1002607.
67. 67 Liu, C.-T., Buchkovich, M.L., Winkler, T.W., Heid, I.M., Borecki, I.B., Fox, C.S., Mohlke, K.L., North, K.E., Adrienne Cupples, L. African Ancestry Anthropometry Genetics Consortium, GIANT Consortium. Multi-ethnic fine-mapping of 14 central adiposity loci. Hum. Mol. Genet. 23 (2014), 4738–4744.