CSK regulatory polymorphism is associated with systemic lupus. erythematosus and influences B cell signaling and activation
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1 Supplementary Information for CSK regulatory polymorphism is associated with systemic lupus erythematosus and influences B cell signaling and activation Nataly Manjarrez-Orduño 1,2, Emiliano Marasco 1, Sharon A. Chung 3, Matthew S. Katz 2, Jenna F. Kiridly 2, Kim R. Simpfendorfer 2, Jan Freudenberg 2, David H. Ballard 2, Emil Nashi 1 *, Thomas J. Hopkins 2, Deborah S Cunninghame Graham 4, Annette T. Lee 2, Marieke J. H. Coenen 5, Barbara Franke 5, Dorine W. Swinkels 6, Robert R. Graham 7, Robert P. Kimberly 8, Patrick M. Gaffney 9, Timothy J. Vyse 4, Timothy W. Behrens 7, Lindsey A. Criswell 3, Betty Diamond 1, Peter K. Gregersen Center for Autoimmune and Musculoskeletal Disorders, The Feinstein Institute for Medical Research, North Shore-LIJ, Manhasset, NY Robert S. Boas Center for Genomics and Human Genetics, The Feinstein Institute for Medical Research, North Shore-LIJ, Manhasset, NY Rosalind Russell Medical Research Center for Arthritis, Department of Medicine, University of California, San Francisco, CA Department of Medical and Molecular Genetics, Division of Genetics and Molecular Medicine, School of Medicine, King's College London, London SE1 9RT, United Kingdom. Department of Human Genetics, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands. Department of Laboratory Medicine, Laboratory of Genetic Endocrine and Metabolic Diseases, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands. Department of Human Genetics, Genentech, South San Francisco, CA Department of Medicine, University of Alabama at Birmingham, AL Arthritis and Immunology Research Program, Oklahoma Medical Research Foundation, Oklahoma City, OK Jointly directed this work. * Current address: Division of Clinical Immunology, McGill University Health Centre. Montreal, Canada. 1
2 Supplementary Table 1. Summary of genetic variants found by sequencing of selected CSK regions in the discovery dataset 1. Region Variants 2 Counts (Frequency) 1 Intron 1 Chr15: G>T G/T:1 (0.042) Intron 2 rs G>A G/G:1 (0.042); G/A:12 (0.5); A/A:11 (0.458) Intron 2 Chr15: A>G A/G:1 (0.042) Exon 14 rs T>G T/T: 19 (0.792); T/G 5 (0.208) 1 24 SLE-affected subjects homozygous for the B haplotype. 2 Positions in hg19. 2
3 Supplementary Table 2. Cohorts and genotyping platforms used in this study. Analytic group I II III Platform for GWAS data HapMap550 Iselect Immunochip Exome chip Disease status Cohort Ref N SLE ABCoN 320 SLE MADGC Controls NYCP SLE U. Minnesota SLE UAB Controls NYCP SLE UCSF SLE UK SLE Controls GaP at FIMR 428 Controls GaP at UAB 800 SLE OMRF Controls Nijmegen Ancestry informative markers (N) 5,899 Markers in the CSK gene Markers used for imputation , ,
4 Supplementary Table 3. Markers genotyped or imputed in each platform and analytic group. Marker Chr Position 1 HapMap550 Iselect Immunochip Exomechip rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped 4
5 rs Imputed Imputed Imputed rs Imputed Genotyped rs Imputed Imputed rs Genotyped Genotyped rs Imputed rs Imputed Imputed rs Imputed Imputed rs Imputed Imputed rs Imputed rs Imputed Imputed Imputed rs Genotyped Imputed Genotyped rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed rs Imputed Imputed rs Genotyped rs Imputed Imputed Imputed rs Genotyped Imputed Genotyped rs Imputed rs Imputed Imputed Imputed rs Imputed rs Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed rs Imputed rs Imputed rs Imputed Imputed Imputed rs Imputed Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed Genotyped rs Imputed rs Imputed Imputed Imputed rs , Genotyped Imputed Imputed Imputed rs Imputed rs Imputed Imputed Imputed rs Imputed rs Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed rs Imputed Genotyped Imputed rs Imputed rs Imputed rs Imputed Imputed Imputed Imputed rs Imputed Genotyped Imputed rs Genotyped rs Imputed Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed Imputed rs Genotyped Genotyped Genotyped rs Genotyped Genotyped Genotyped Genotyped rs Imputed Genotyped Imputed rs Imputed Imputed Genotyped Imputed rs Genotyped Imputed Imputed Imputed rs Imputed Imputed Imputed 5
6 rs Imputed Imputed Imputed Imputed rs Imputed Genotyped Imputed rs Imputed Imputed Imputed rs Genotyped Imputed Imputed Imputed rs Imputed Imputed Imputed Imputed rs Imputed Imputed Imputed Imputed rs Genotyped rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Genotyped Imputed Imputed Imputed rs Imputed Genotyped rs Imputed Genotyped Imputed Imputed rs Genotyped rs Imputed Imputed Genotyped Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Genotyped rs Imputed Imputed Imputed Imputed rs Imputed Imputed Imputed Imputed rs Imputed Imputed Genotyped Imputed rs Genotyped rs Imputed Imputed Imputed rs Imputed Imputed Imputed Imputed rs Imputed Imputed Imputed Imputed rs Imputed Genotyped Genotyped Imputed rs Imputed Imputed Imputed rs Imputed Imputed Genotyped Imputed rs Genotyped rs Imputed rs Imputed Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed Imputed rs Genotyped rs Imputed Imputed rs Genotyped Genotyped Genotyped rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed Imputed rs Imputed Imputed rs Imputed Imputed Genotyped rs Imputed Imputed rs Imputed rs Imputed Imputed Imputed rs Genotyped Imputed rs Imputed Imputed Imputed rs Imputed Genotyped Genotyped rs Imputed Imputed rs Genotyped rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed rs Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed rs Imputed Imputed Imputed 6
7 rs Imputed rs Imputed rs Imputed Imputed rs Genotyped rs Imputed Imputed Imputed rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped rs Genotyped 1 The positions shadowed in gray highlight the span of CSK transcription. 2 The markers shadowed in green are shown in figure 1. 3 rs was genotyped in all the cohorts and is shown highlighted in yellow. 4 Markers that were genotyped in some cohorts and imputed in others are shown in orange. 5 Markers that were imputed in all the cohorts are shown in blue. 7
8 Supplementary Table 4. Primers used for genotyping of rs by pyrosequencing. Forward Reverse Sequencing CCTGGCCTGGCTCAGATGA CCAGAGGAGAGGGGGAAGG AGGGGGAAGGGAGGCAGT 8
9 Supplementary Figure 1 Supplementary Figure 1. The Csk risk allele is associated with increased plyn508 in resting naïve B cells. (A) Gating strategy employed to analyze naïve B cells, data shown also in figure 3. (B) Lyn508 phosphorylation (red line) and isotype control (blue line) as measured in one single flow cytometry experiment in ten healthy subjects homozygous for the B haplotype. (C) plyn508 median fluorescence intensity (MFI) of the same samples, (p<0.05, Mann-Whitney test). 9
10 Supplementary Figure 2 Supplementary figure 2. The CSK risk allele is associated with expansion of late transitional B cells in umbilical cord blood. (a) Transitional B cells were defined by a CD19+ gate, and subsequently as CD38 hi, CD10 hi, as in figure 4; and (b) further classified into CD21 low (early) and CD21 hi (late) transitional cells as described 10. (Kruskal-Wallis test). 10
11 References 1. Hom, G., et al. Association of Systemic Lupus Erythematosus with C8orf13 BLK and ITGAM ITGAX. NEJM 358, (2008). 2. Criswell, L.A., et al. Analysis of Families in the Multiple Autoimmune Disease Genetics Consortium (MADGC) Collection: the PTPN22 620W Allele Associates with Multiple Autoimmune Phenotypes. Am J Hum Genet 76, (2005). 3. Plenge, R.M., et al. TRAF1 C5 as a Risk Locus for Rheumatoid Arthritis A Genomewide Study. NEJM 357, (2007). 4. Graham, R.R., et al. A common haplotype of interferon regulatory factor 5 (IRF5) regulates splicing and expression and is associated with increased risk of systemic lupus erythematosus. Nat Genet 38, (2006). 5. Nath, S.K., et al. A nonsynonymous functional variant in integrin-[alpha]m (encoded by ITGAM) is associated with systemic lupus erythematosus. Nat Genet 40, (2008). 6. Gregersen, P.K., et al. REL, encoding a member of the NF-[kappa]B family of transcription factors, is a newly defined risk locus for rheumatoid arthritis. Nat Genet 41, (2009). 7. Thorburn, C.M., et al. Association of PDCD1 genetic variation with risk and clinical manifestations of systemic lupus erythematosus in a multiethnic cohort. Genes Immun 8, (2007). 8. Cunninghame Graham, D.S., et al. Association of NCF2, IKZF1, IRF8, IFIH1, and TYK2 with Systemic Lupus Erythematosus. PLoS Genet 7, e (2011). 9. Wetzels, J.F.M., Kiemeney, L.A.L.M., Swinkels, D.W., Willems, H.L. & Heijer, M.d. Age- and gender-specific reference values of estimated GFR in Caucasians: The Nijmegen Biomedical Study. Kidney Int 72, (2007). 10. Suryani, S., et al. Differential expression of CD21 identifies developmentally and functionally distinct subsets of human transitional B cells. Blood 115, (2010). 11
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