Rare genetic variants in SMAP1, B3GAT2, and RIMS1 contribute to pediatric venous thromboembolism

Blood

Volumn 129, Issue 6, 2017, Pages 783-790

  Rühle, Frank ^a   Witten, Anika ^a   Barysenka, Andrei ^a   Huge, Andreas ^a   Arning, Astrid ^a   Heller, Christine ^b   Krümpel, Anne ^c   Mesters, Rolf ^c   Franke, Andre ^d   Lieb, Wolfgang ^d   Riemenschneider, Mona ^a   Hiersche, Milan ^a   Limperger, Verena ^e   Nowak Göttl, Ulrike ^c,e   Stoll, Monika ^a,f  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^d UNIVERSITY OF KIEL   (Germany)

^e UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^f MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; BETA 1,3 GLUCORONYLTRANSFERASE 2; CARRIER PROTEINS AND BINDING PROTEINS; GENOMIC DNA; RAB 3 INTERACTING MOLECULE; SMALL ARF GAP1; TRANSFERASE; UNCLASSIFIED DRUG; B3GAT2 PROTEIN, HUMAN; GLUCURONOSYLTRANSFERASE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MEMBRANE PROTEIN; NERVE PROTEIN; RIMS1 PROTEIN, HUMAN; SMAP1 PROTEIN, HUMAN;

ARTICLE; CARDIOEMBOLIC STROKE; CHILD; CHILDHOOD DISEASE; CHROMOSOME 6; CONTROLLED STUDY; EXON; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENOTYPE; HAPLOTYPE; HUMAN; INDEL MUTATION; MAJOR CLINICAL STUDY; NEXT GENERATION SEQUENCING; PARADOXICAL EMBOLISM; PRIORITY JOURNAL; REPLICATION STUDY; SINGLE NUCLEOTIDE POLYMORPHISM; VENOUS THROMBOEMBOLISM; ADOLESCENT; CHEMISTRY; CHROMOSOMAL MAPPING; COHORT ANALYSIS; FEMALE; GENE LOCUS; GENETIC PREDISPOSITION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HIGH THROUGHPUT SEQUENCING; INFANT; MALE; MUTATION; PATHOLOGY; PRESCHOOL CHILD; SIBLING;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, PAIR 6; COHORT STUDIES; FEMALE; GENETIC LOCI; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; GLUCURONOSYLTRANSFERASE; GTP-BINDING PROTEINS; GTPASE-ACTIVATING PROTEINS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFANT; MALE; MEMBRANE PROTEINS; MUTATION; NERVE TISSUE PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; SIBLINGS; VENOUS THROMBOEMBOLISM;

EID: 85014811384     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-07-728840     Document Type: Article

References (42)

1. Kenet G, Lütkhoff LK, Albisetti M, et al. Impact of thrombophilia on risk of arterial ischemic stroke or cerebral sinovenous thrombosis in neonates and children: a systematic review and meta-analysis of observational studies. Circulation. 2010;121(16):1838-1847.
2. Caruso V, Iacoviello L, Di Castelnuovo A, et al. Thrombotic complications in childhood acute lymphoblastic leukemia: a meta-analysis of 17 prospective studies comprising 1752 pediatric patients. Blood. 2006;108(7):2216-2222.
3. Haywood S, Liesner R, Pindora S, Ganesan V. Thrombophilia and first arterial ischaemic stroke: a systematic review. Arch Dis Child. 2005;90(4):402-405.
4. Nowak-Göttl U, Kurnik K, Krümpel A, Stoll M. Thrombophilia in the young. Hamostaseologie. 2008;28(1-2):16-20.
5. Uitte de Willige S, de Visser MC, Houwing-Duistermaat JJ, Rosendaal FR, Vos HL, Bertina RM. Genetic variation in the fibrinogen gamma gene increases the risk for deep venous thrombosis by reducing plasma fibrinogen gamma' levels. Blood. 2005;106(13):4176-4183.
6. Nowak-Göttl U, Weiler H, Hernandez I, et al. Fibrinogen alpha and gamma genes and factor VLeiden in children with thromboembolism: results from 2 family-based association studies. Blood. 2009;114(9):1947-1953.
7. Trégouët DA, Heath S, Saut N, et al. Common susceptibility alleles are unlikely to contribute as strongly as the FV and ABO loci to VTE risk: results from a GWAS approach. Blood. 2009;113(21):5298-5303.
8. Morange P-E, Bezemer I, Saut N, et al. A follow-up study of a genome-wide association scan identifies a susceptibility locus for venous thrombosis on chromosome 6p24.1. Am J Hum Genet. 2010;86(4):592-595.
9. Heit JA, Armasu SM, Asmann YW, et al. A genome-wide association study of venous thromboembolism identifies risk variants in chromosomes 1q24.2 and 9q. J Thromb Haemost. 2012;10(8):1521-1531.
10. Germain M, Chasman DI, de Haan H, et al; Cardiogenics Consortium. Meta-analysis of 65,734 individuals identifies TSPAN15 and SLC44A2 as two susceptibility loci for venous thromboembolism. Am J Hum Genet. 2015;96(4):532-542.
11. Germain M, Saut N, Greliche N, et al. Genetics of venous thrombosis: insights from a new genome wide association study. PLoS One. 2011;6(9):e25581.
12. Arning A, Hiersche M, Witten A, et al. A genome-wide association study identifies a gene network of ADAMTS genes in the predisposition to pediatric stroke. Blood. 2012;120(26):5231-5236.
13. Krawczak M, Nikolaus S, von Eberstein H, Croucher PJ, El Mokhtari NE, Schreiber S. PopGen: population-based recruitment of patients and controls for the analysis of complex genotype-phenotype relationships. Community Genet. 2006;9(1):55-61.
14. Purcell S, Neale B, Todd-Brown K, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81(3):559-575.
15. Delaneau O, Marchini J, Zagury JF. A linear complexity phasing method for thousands of genomes. Nat Methods. 2011;9(2):179-181.
16. Howie BN, Donnelly P, Marchini J. A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet. 2009;5(6):e1000529.
17. Spielman RS, Ewens WJ. The TDT and other family-based tests for linkage disequilibrium and association. Am J Hum Genet. 1996;59(5):983-989.
18. Fisher RA. Statistical Methods for Research Workers. London, England: Oliver and Boyed; 1946.
19. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-1760.
20. DePristo MA, Banks E, Poplin R, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43(5):491-498.
21. McKenna A, Hanna M, Banks E, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9):1297-1303.
22. Van der Auwera GA, Carneiro MO, Hartl C, et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinformatics. 2013;43:11.101-33.
23. Cingolani P, Platts A, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin). 2012;6(2):80-92.
24. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38(16):e164.
25. Horvath S, Laird NM. A discordant-sibship test for disequilibrium and linkage: no need for parental data. Am J Hum Genet. 1998;63(6):1886-1897.
26. De G, Yip WK, Ionita-Laza I, Laird N. Rare variant analysis for family-based design. PLoS One. 2013;8(1):e48495.
27. Laird NM, Horvath S, Xu X. Implementing a unified approach to family-based tests of association. Genet Epidemiol. 2000;19(Suppl 1): S36-S42.
28. Uricchio LH, Zaitlen NA, Ye CJ, Witte JS, Hernandez RD. Selection and explosive growth alter genetic architecture and hamper the detection of causal rare variants. Genome Res. 2016;26(7):863-873.
29. Gamara J, Chouinard F, Davis L, Aoudjit F, Bourgoin SG. Regulators and effectors of Arf GTPases in neutrophils. J Immunol Res. 2015; 2015:235170.
30. Huang Y, Joshi S, Xiang B, et al. Arf6 controls platelet spreading and clot retraction via integrin aIIbb3 trafficking. Blood. 2016;127(11):1459-1467.
31. Kon S, Minegishi N, Tanabe K, et al. Smap1 deficiency perturbs receptor trafficking and predisposes mice to myelodysplasia. J Clin Invest. 2013;123(3):1123-1137.
32. Imiya K, Ishizaki T, Seiki T, et al. cDNA cloning, genomic structure and chromosomal mapping of the mouse glucuronyltransferase-S involved in the biosynthesis of the HNK-1 carbohydrate epitope. Gene. 2002;296(1-2):29-36.
33. Marcos I, Galán JJ, Borrego S, Antiñolo G. Cloning, characterization, and chromosome mapping of the human GlcAT-S gene. J Hum Genet. 2002;47(12):677-680.
34. Bhatnagar P, Purvis S, Barron-Casella E, et al. Genome-wide association study identifies genetic variants influencing F-cell levels in sickle-cell patients. J Hum Genet. 2011;56(4):316-323.
35. Key NS, Slungaard A, Dandelet L, et al. Whole blood tissue factor procoagulant activity is elevated in patients with sickle cell disease. Blood. 1998;91(11):4216-4223.
36. Austin H, Key NS, Benson JM, et al. Sickle cell trait and the risk of venous thromboembolism among blacks. Blood. 2007;110(3):908-912.
37. Nowak-Göttl U, Kurnik K, Manner D, Kenet G. Thrombophilia testing in neonates and infants with thrombosis. Semin Fetal Neonatal Med. 2011; 16(6):345-348.
38. Mittelstaedt T, Alvaréz-Baron E, Schoch S. RIM proteins and their role in synapse function. Biol Chem. 2010;391(6):599-606.
39. Schoch S, Castillo PE, Jo T, et al. RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature. 2002;415(6869):321-326.
40. Gandini MA, Sandoval A, González-Ramírez R, Mori Y, de Waard M, Felix R. Functional coupling of Rab3-interacting molecule 1 (RIM1) and L-type Ca2+ channels in insulin release. J Biol Chem. 2011;286(18):15757-15765.
41. Ren Q, Ye S, Whiteheart SW. The platelet release reaction: just when you thought platelet secretion was simple. Curr Opin Hematol. 2008;15(5):537-541.
42. Mollinedo F, Calafat J, Janssen H, et al. Combinatorial SNARE complexes modulate the secretion of cytoplasmic granules in human neutrophils. J Immunol. 2006;177(5):2831-2841.