Genomics meets glycomics-the first gwas study of human N-glycome identifies HNF1A as a master regulator of plasma protein fucosylation

PLoS Genetics

Volumn 6, Issue 12, 2010, Pages 1-14

  Lauc, Gordan ^a,b   Essafi, Abdelkader ^c   Huffman, Jennifer E ^c   Hayward, Caroline ^c   Knežević, Ana ^b   Kattla, Jayesh J ^d   Polašek, Ozren ^e,f   Gornik, Olga ^b   Vitart, Veronique ^c   Abrahams, Jodie L ^d   Pučić, Maja ^a   Novokmet, Mislav ^a   Redžić, Irma ^b   Campbell, Susan ^c   Wild, Sarah H ^g   Borovečki, Fran ^f   Wang, Wei ^h,i,j   Kolčić, Ivana ^f   Zgaga, Lina ^f   Gyllensten, Ulf ^k   Wilson, James F ^g   Wright, Alan F ^c   Hastie, Nicholas D ^c   Campbell, Harry ^g   Rudd, Pauline M ^d   Rudan, Igor ^g,j   more..

^a GENOS GLYCOSCIENCE RESEARCH LABORATORY   (Croatia)

^b UNIVERSITY OF ZAGREB   (Croatia)

^c WESTERN GENERAL HOSPITAL   (United Kingdom)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

^e Gen Info Ltd   (Croatia)

^f UNIVERSITY OF ZAGREB   (Croatia)

^g UNIVERSITY OF EDINBURGH   (United Kingdom)

^h CAPITAL MEDICAL UNIVERSITY   (China)

ⁱ UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^j UNIVERSITY OF SPLIT   (Croatia)

^k UPPSALA UNIVERSITY   (Sweden)

more..

Author keywords

[No Author keywords available]

Indexed keywords

FUCOSE; FUCOSYLTRANSFERASE; FUCOSYLTRANSFERASE 10; FUCOSYLTRANSFERASE 11; FUCOSYLTRANSFERASE 3; FUCOSYLTRANSFERASE 5; FUCOSYLTRANSFERASE 6; FUCOSYLTRANSFERASE 8; GLYCAN; GLYCAN DERIVATIVE; GUANOSINE DIPHOSPHATE FUCOSE; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HEPATOCYTE NUCLEAR FACTOR 4; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; COHORT ANALYSIS; CONTROLLED STUDY; EFFECT SIZE; ENZYME REGULATION; ENZYME SYNTHESIS; FUCOSYLATION; GENE EXPRESSION REGULATION; GENOME ANALYSIS; GENOMICS; GLYCOBIOLOGY; GLYCOSYLATION; HIGH THROUGHPUT SCREENING; HUMAN; LIVER CELL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION;

EID: 84975742481     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001256     Document Type: Article

References (58)

1. Marth JD, Grewal PK (2008) Mammalian glycosylation in immunity. Nature Reviews Immunology 8: 874-887.
2. Dennis JW, Lau KS, Demetriou M, Nabi IR (2009) Adaptive Regulation at the Cell Surface by N-Glycosylation. Traffic 10: 1569-1578.
3. Ohtsubo K, Marth JD (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126: 855-867.
4. Apweiler R, Hermjakob H, Sharon N (1999) On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochimica et Biophysica Acta 1473: 4-8.
5. Skropeta D (2009) The effect of individual N-glycans on enzyme activity. Bioorganic & Medicinal Chemistry 17: 2645-2653.
6. Hart GW, Housley MP, Slawson C (2007) Cycling of O-linked beta-Nacetylglucosamine on nucleocytoplasmic proteins. Nature 446: 1017-1022.
7. Crocker PR, Paulson JC, Varki A (2007) Siglecs and their roles in the immune system. Nature Reviews Immunology 7: 255-266.
8. Brown JR, Crawford BE, Esko JD (2007) Glycan antagonists and inhibitors: a fount for drug discovery. Critical reviews in biochemistry and molecular biology 42: 481-515.
9. Jaeken J (2003) Komrower Lecture. Congenital disorders of glycosylation (CDG): it's all in it! J Inherit Metab Dis 26: 99-118.
10. Freeze HH (2006) Genetic defects in the human glycome. Nature Reviews Genetics 7: 537-551.
11. Freeze HH (2002) Human disorders in N-glycosylation and animal models. Biochimica et Biophysica Acta 1573: 388-393.
12. Lauc G, Rudan I, Campbell H, Rudd PM (2010) Complex Genetic Regulation of Protein Glycosylation. Molecular Biosystems 6: 329-335.
13. Royle L, Campbell MP, Radcliffe CM, White DM, Harvey DJ, et al. (2008) HPLC-based analysis of serum N-glycans on a 96-well plate platform with dedicated database software. Analytical Biochemistry 376: 1-12.
14. Rudd PM, Rudan I, Wright AF (2009) High-Throughput Glycome Analysis Is Set To Join High-Throughput Genomics. Journal of Proteome Research 8: 1105-1105.
15. Knežević A, Polašek O, Gornik O, Rudan I, Campbell H, et al. (2009) Variability, Heritability and Environmental Determinants of Human Plasma NGlycome. Journal of Proteome Research 8: 694-701.
16. Gornik O, Wagner J, Pučić M, Knežević A, Redžić I, et al. (2009) Stability of Nglycan profiles in human plasma. Glycobiology 19: 1547-1553.
17. Knežević A, Gornik O, Polašek O, Pučić M, Novokmet M, et al. (2010) Effects of aging, body mass index, plasma lipid profiles, and smoking on human plasma N-glycans. Glycobiology 20: 959-969.
18. Pučić M, Pinto S, Novokmet M, Knežević A, Gornik O, et al. (2010) Common aberrations from normal human N-glycan plasma profile. Glycobiology 20: 970-975.
19. Becker DJ, Lowe JB (2003) Fucose: biosynthesis and biological function in mammals. Glycobiology 13: 41R-53R.
20. Tonetti M, Sturla L, Bisso A, Benatti U, De Flora A (1996) Synthesis of GDP-Lfucose by the human FX protein. Journal of Biological Chemistry 271: 27274-27279.
21. Javaud C, Dupuy F, Maftah A, Julien R, Petit JM (2003) The fucosyltransferase gene family: an amazing summary of the underlying mechanisms of gene evolution. Genetica 118: 157-170.
22. Gornik O, Lauc G (2008) Glycosylation of serum proteins in inflammatory diseases. Disease Markers 25: 267-278.
23. Miyoshi E, Moriwaki K, Nakagawa T (2008) Biological function of fucosylation in cancer biology. Journal of Biochemistry 143: 725-729.
24. Odom DT, Zizlsperger N, Gordon DB, Bell GW, Rinaldi NJ, et al. (2004) Control of pancreas and liver gene expression by HNF transcription factors. Science 303: 1378-1381.
25. Yamagata K, Furuta H, Oda N, Kaisaki PJ, Menzel S, et al. (1996) Mutations in the hepatocyte nuclear factor-4alpha gene in maturity-onset diabetes of the young (MODY1). Nature 384: 458-460.
26. Yamagata K, Oda N, Kaisaki PJ, Menzel S, Furuta H, et al. (1996) Mutations in the hepatocyte nuclear factor-1alpha gene in maturity-onset diabetes of the young (MODY3). Nature 384: 455-458.
27. Elliott P, Chambers JC, Zhang W, Clarke R, Hopewell JC, et al. (2009) Genetic Loci associated with C-reactive protein levels and risk of coronary heart disease. JAMA 302: 37-48.
28. Yuan X, Waterworth D, Perry JR, Lim N, Song K, et al. (2008) Populationbased genome-wide association studies reveal six loci influencing plasma levels of liver enzymes. American Journal of Human Genetics 83: 520-528.
29. Reiner AP, Gross MD, Carlson CS, Bielinski SJ, Lange LA, et al. (2009) Common coding variants of the HNF1A gene are associated with multiple cardiovascular risk phenotypes in community-based samples of younger and older European-American adults: the Coronary Artery Risk Development in Young Adults Study and The Cardiovascular Health Study. Circ Cardiovasc Genet 2: 244-254.
30. Barrett JC, Lee JC, Lees CW, Prescott NJ, Anderson CA, et al. (2009) Genomewide association study of ulcerative colitis identifies three new susceptibility loci, including the HNF4A region. Nature Genetics 41: 1330-1334.
31. Kathiresan S, Willer CJ, Peloso GM, Demissie S, Musunuru K, et al. (2009) Common variants at 30 loci contribute to polygenic dyslipidemia. Nature Genetics 41: 56-65.
32. Vitart V, Rudan I, Hayward C, Gray NK, Floyd J, et al. (2008) SLC2A9 is a newly identified urate transporter influencing serum urate concentration, urate excretion and gout. Nature Genetics 40: 437-442.
33. Taniguchi N, Honke K, Fukuda M, eds (2002) Handbook of glycosyltransferases and related genes. Tokyo: Springer Verlag.
34. Brinkman Van der Linden EC, Mollicone R, Oriol R, Larson G, Van den Eijnden DH, et al. (1996) A missense mutation in the FUT6 gene results in total absence of alpha3-fucosylation of human alpha1-acid glycoprotein. J Biol Chem 271: 14492-14495.
35. Ma B, Simala-Grant JL, Taylor DE (2006) Fucosylation in prokaryotes and eukaryotes. Glycobiology 16: 158R-184R.
36. Higai K, Miyazaki N, Azuma Y, Matsumoto K (2008) Transcriptional regulation of the fucosyltransferase VI gene in hepatocellular carcinoma cells. Glycoconjugate Journal 25: 225-235.
37. Servitja JM, Pignatelli M, Maestro MA, Cardalda C, Boj SF, et al. (2009) Hnf1alpha (MODY3) controls tissue-specific transcriptional programs and exerts opposed effects on cell growth in pancreatic islets and liver. Molecular & Cellular Biology 29: 2945-2959.
38. Boj SF, Petrov D, Ferrer J (2010) Epistasis of transcriptomes reveals synergism between transcriptional activators Hnf1alpha and Hnf4alpha. PLoS Genet 6: e1000970. doi:10.1371/journal.pgen.1000970.
39. Bejerano G, Siepel AC, Kent WJ, Haussler D (2005) Computational screening of conserved genomic DNA in search of functional noncoding elements. Nature Methods 2: 535-545.
40. Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, et al. (2007) Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet 39: 730-732.
41. Loots G, Ovcharenko I (2007) ECRbase: database of evolutionary conserved regions, promoters, and transcription factor binding sites in vertebrate genomes. Bioinformatics 23: 122-124.
42. Boyd M, Bressendorff S, Moller J, Olsen J, Troelsen JT (2009) Mapping of HNF4alpha target genes in intestinal epithelial cells. BMC Gastroenterol 9: 68.
43. Benko S, Fantes JA, Amiel J, Kleinjan DJ, Thomas S, et al. (2009) Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence. Nat Genet 41: 359-364.
44. Essafi A, Fernandez de Mattos S, Hassen YA, Soeiro I, Mufti GJ, et al. (2005) Direct transcriptional regulation of Bim by FoxO3a mediates STI571-induced apoptosis in Bcr-Abl-expressing cells. Oncogene 24: 2317-2329.
45. Withers DA, Hakomori SI (2000) Human alpha (1,3)-fucosyltransferase IV (FUTIV) gene expression is regulated by elk-1 in the U937 cell line. Journal of Biological Chemistry 275: 40588-40593.
46. Erdmann J, Grosshennig A, Braund PS, Konig IR, Hengstenberg C, et al. (2009) New susceptibility locus for coronary artery disease on chromosome 3q22.3. Nature Genetics 41: 280-282.
47. Kel AE, Niehof M, Matys V, Zemlin R, Borlak J (2008) Genome wide prediction of HNF4alpha functional binding sites by the use of local and global sequence context. Genome Biol 9: R36.
48. Brandley BK, Kiso M, Abbas S, Nikrad P, Srivasatava O, et al. (1993) Structurefunction studies on selectin carbohydrate ligands. Modifications to fucose, sialic acid and sulphate as a sialic acid replacement. Glycobiology 3: 633-641.
49. Luhn K, Marquardt T, Harms E, Vestweber D (2001) Discontinuation of fucose therapy in LADII causes rapid loss of selectin ligands and rise of leukocyte counts. Blood 97: 330-332.
50. Klein A (2008) Human total serum N-glycome. Advances in Clinical Chemistry 46: 51-85.
51. Royle L, Radcliffe CM, Dwek RA, Rudd PM (2006) Detailed structural analysis of N-glycans released from glycoproteins in SDS-PAGE gel bands using HPLC combined with exoglycosidase array digestions. Methods Mol Biol 347: 125-143.
52. Campbell MP, Royle L, Radcliffe CM, Dwek RA, Rudd PM (2008) GlycoBase and autoGU: tools for HPLC-based glycan analysis. Bioinformatics 24: 1214-1216.
53. Aulchenko YS, Ripke S, Isaacs A, van Duijn CM (2007) GenABEL: an R library for genome-wide association analysis. Bioinformatics 23: 1294-1296.
54. Chen WM, Abecasis GR (2007) Family-based association tests for genomewide association scans. Am J Hum Genet 81: 913-926.
55. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263-265.
56. Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O'Donnell CJ, et al. (2008) SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 24: 2938-2939.
57. Schaid DJ, Rowland CM, Tines DE, Jacobson RM, Poland GA (2002) Score tests for association between traits and haplotypes when linkage phase is ambiguous. Am J Hum Genet 70: 425-434.
58. Akaike H (1974) New Look at Statistical-Model Identification. Ieee Transactions on Automatic Control AC19: 716-723.