The Association between Glycosylation of Immunoglobulin G and Hypertension

Medicine (United States)

Volumn 95, Issue 17, 2016, Pages

  Wang, Youxin ^a,d   Klarić, Lucija ^b,c   Yu, Xinwei ^a,d   Thaqi, Kujtim ^b   Dong, Jing ^e   Novokmet, Mislav ^b   Wilson, Jim ^f   Polasek, Ozren ^g   Liu, Youqin ^e   Krištić, Jasminka ^b   Ge, Siqi ^a,d   Pučić Baković, Maja ^b   Wu, Lijuan ^a   Zhou, Yong ^h   Ugrina, Ivo ^b   Song, Manshu ^a   Zhang, Jie ^a   Guo, Xiuhua ^a   Zeng, Qiang ⁱ   Rudan, Igor ^f   Campbell, Harry ^f   Aulchenko, Yurii ^j,k   Lauc, Gordan ^b,g   Wang, Wei ^a,d   more..

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b GENOS GLYCOSCIENCE RESEARCH LABORATORY   (Croatia)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d EDITH COWAN UNIVERSITY   (Australia)

^e CAPITAL MEDICAL UNIVERSITY   (China)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

^g UNIVERSITY OF ZAGREB   (Croatia)

^h CAPITAL MEDICAL UNIVERSITY   (China)

ⁱ CHINESE PLA GENERAL HOSPITAL   (China)

^j INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

^k NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; IMMUNOGLOBULIN G; POLYSACCHARIDE;

ADOLESCENT; ADULT; AGED; ARTICLE; BLOOD SAMPLING; CROATIAN (CITIZEN); CROSS-SECTIONAL STUDY; DIASTOLIC BLOOD PRESSURE; FEMALE; HAN CHINESE; HUMAN; HYDROPHILIC INTERACTION CHROMATOGRAPHY; HYPERTENSION; IMMUNOPATHOGENESIS; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PREHYPERTENSION; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; SCOTSMAN; SYSTOLIC BLOOD PRESSURE; BLOOD; CHINA; COMPARATIVE STUDY; CROATIA; CULTURAL FACTOR; ETHNOLOGY; GLYCOSYLATION; IMMUNOLOGY; SCOTLAND; STATISTICS; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; CHINA; CROATIA; CROSS-CULTURAL COMPARISON; CROSS-SECTIONAL STUDIES; FEMALE; GLYCOSYLATION; HUMANS; HYPERTENSION; IMMUNOGLOBULIN G; MALE; MIDDLE AGED; POLYSACCHARIDES; PREHYPERTENSION; SCOTLAND; STATISTICS AS TOPIC; YOUNG ADULT;

EID: 84978230478     PISSN: 00257974     EISSN: 15365964     Source Type: Journal    
DOI: 10.1097/MD.0000000000003379     Document Type: Article

References (68)

1. Kearney PM, Whelton M, Reynolds K, et al. Global burden of hypertension: analysis of worldwide data. Lancet. 2005;365:217-223.
2. Writing Group MembersLloyd-Jones D, Adams RJ, Brown TM, et al. Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation. 2010;121:e46-e215.
3. Vasan RS, Beiser A, Seshadri S, et al. Residual lifetime risk for developing hypertension in middle-aged women and men: The Framingham Heart Study. JAMA. 2002;287:1003-1010.
4. International Consortium for Blood Pressure Genome-Wide Association StudiesEhret GB, Munroe PB, Rice KM, et al. Genetic variants in novel pathways influence blood pressure and cardiovascular disease risk. Nature. 2011;478:103-109.
5. Lifton RP, Gharavi AG, Geller DS. Molecular mechanisms of human hypertension. Cell. 2001;104:545-556.
6. He FJ, MacGregor GA. A comprehensive review on salt and health and current experience of worldwide salt reduction programmes. J Hum Hypert. 2009;23:363-384.
7. He FJ, Li J, Macgregor GA. Effect of longer term modest salt reduction on blood pressure: Cochrane systematic review and meta-analysis of randomised trials. BMJ. 2013;346:f1325.
8. Dickinson HO, Mason JM, Nicolson DJ, et al. Lifestyle interventions to reduce raised blood pressure: a systematic review of randomized controlled trials. J Hypertens. 2006;24:215-233.
9. Haslam DW, James WP. Obesity. Lancet. 2005;366:1197-1209.
10. Whelton PK, He J, Appel LJ, et al. Primary prevention of hypertension: clinical and public health advisory from The National High Blood Pressure Education Program. JAMA. 2002;288:1882-1888.
11. Mesas AE, Leon-Munuoz LM, Rodriguez-Artalejo F, et al. The effect of coffee on blood pressure and cardiovascular disease in hypertensive individuals: a systematic review and meta-analysis. Am J Clin Nutr. 2011;94:1113-1126.
12. Vaidya A, Forman JP. Vitamin D and hypertension: current evidence and future directions. Hypertension. 2010;56:774-779.
13. Lawlor DA, Smith GD. Early life determinants of adult blood pressure. Curr Opin Nephrol Hypertens. 2005;14:259-264.
14. Marshall IJ, Wolfe CD, McKevitt C. Lay perspectives on hypertension and drug adherence: systematic review of qualitative research. BMJ. 2012;345:e3953.
15. Lauc G. Sweet secret of multicellular life. Biochim Biophys Acta. 2006;1760:525-526.
16. Apweiler R, Hermjakob H, Sharon N. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim Biophys Acta. 1999;1473:4-8.
17. Marek KW, Vijay IK, Marth JD. A recessive deletion in the GlcNAc-1-phosphotransferase gene results in peri-implantation embryonic lethality. Glycobiology. 1999;9:1263-1271.
18. Parekh RB, Dwek RA, Sutton BJ, et al. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature. 1985;316:452-457.
19. Varki A, Baum L, Bellis S, et al. Working group report: the roles of glycans in hemostasis, inflammation and vascular biology. Glyco-biology. 2008;18:747-749.
20. Junqueira LC, Carneiro J. Basic Histology. McGraw-Hill, 2003: ISBN 0838505902.
21. Wright A, Morrison SL. Effect of glycosylation on antibody function: implications for genetic engineering. Trends Biotechnol. 1997;15:26-32.
22. Jefferis R. Antibody therapeutics: isotype and glycoform selection. Expert Opin Biol Ther. 2007;7:1401-1413.
23. Miyoshi E, Shinzaki S, Fujii H, et al. Role of aberrant IgG glycosylation in the pathogenesis of inflammatory bowel disease. Proteomics Clin Appl. 2016;10:384-390.
24. van Timmeren MM, van der Veen BS, Stegeman CA, et al. IgG glycan hydrolysis attenuates ANCA-mediated glomerulonephritis. J Am Soc Nephrol. 2010;21:1103-1114.
25. Trbojević Akmacić I, Ventham NT, Theodoratou E, et al. Inflammatory bowel disease associates with proinflammatory potential of the immunoglobulin G glycome. Inflamm Bowel Dis. 2015;21:1237-1247.
26. Vucković F, Kristić J, Gudelj I, et al. Association of systemic lupus erythematosus with decreased immunosuppressive potential of the IgG glycome. Arthritis Rheumatol. 2015;67:2978-2989.
27. Lundström SL, Yang H, Lyutvinskiy Y, et al. Blood plasma IgG Fc glycans are significantly altered in Alzheimer's disease and progressive mild cognitive impairment. J Alzheimers Dis. 2014;38:567-579.
28. Kaneshige H. Nonenzymatic glycosylation of serum IgG and its effect on antibody activity in patients with diabetes mellitus. Diabetes. 1987;36:822-828.
29. Pucić M, Knezević A, Vidic J, et al. High throughput isolation and glycosylation analysis of IgG-variability and heritability of the IgG glycome in three isolated human populations. Mol Cell Proteomics. 2011;10:M111.010090.
30. Nikolac Perkovic M, Pucic Bakovic M, Kristic J, et al. The association between galactosylation of immunoglobulin G and body mass index. Prog Neuropsychopharmacol Biol Psychiatry. 2014;48:20-25.
31. Lu JP, Knezevic A, Wang YX, et al. Screening novel biomarkers for metabolic syndrome by profiling human plasma N-glycans in Chinese Han and Croatian populations. J Proteome Res. 2011;10:4959-4969.
32. Rudan I, Campbell H, Rudan P. Genetic epidemiological studies of eastern Adriatic Island isolates, Croatia: objective and strategies. Coll Antropol. 1999;23:531-546.
33. Rudan I, Biloglav Z, Vorko-Jovic A, et al. Effects of inbreeding, endogamy, genetic admixture, and outbreeding on human health: a (1001 Dalmatians) study. Croat Med J. 2006;47:601-610.
34. Rudan I, Marusic A, Jankovic S, et al. "10001 Dalmatians:" Croatia launches its national biobank. Croat Med J. 2009;50:4-6.
35. McQuillan R, Leutenegger AL, Abdel-Rahman R, et al. Runs of homozygosity in European populations. Am J Hum Genet. 2008;83:359-372.
36. Chobanian AV, Bakris GL, Black HR, et al. Seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure. Hypertension. 2003;42:1206-1252.
37. Ruhaak LR, Steenvoorden E, Koeleman CA, et al. 2-Picoline-borane: a non-toxic reducing agent for oligosaccharide labeling by reductive amination. Proteomics. 2010;10:2330-2336.
38. Ruhaak LR, Hennig R, Huhn C, et al. Optimized workflow for preparation of APTS-labeled N-glycans allowing high-throughput analysis of human plasma glycomes using 48-channelmultiplexed CGE-LIF. J Proteome Res. 2010;9:6655-6664.
39. Royle L, Campbell MP, Radcliffe CM, et al. HPLC-based analysis of serum N-glycans on a 96-well plate platform with dedicated database software. Anal Biochem. 2008;376:1-12.
40. Pucic M, Knezevic A, Vidic J, et al. High throughput isolation and glycosylation analysis of IgG-variability and heritability of the IgG glycome in three isolated human populations. Mol Cell Proteomics. 2011;10:010090.
41. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biosta-tistics. 2007;8:118-127.
42. Leek JT, Johnson WE, Parker HS, et al. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics. 2012;28:882-883.
43. Aulchenko YS, de Koning DJ, Haley C. Genome wide rapid association using mixed model and regression: a fast and simple method for genome wide pedigree-based quantitative trait loci association analysis. Genetics. 2007;177:577-585.
44. Lauc G, Huffman JE, Pucic M, et al. Loci associated with N-glycosylation of human immunoglobulin G show pleiotropy with autoimmune diseases and haematological cancers. PLoS Genet. 2013;9:e1003225.
45. Aulchenko YS, Ripke S, Isaacs A, et al. GenABEL: an R library for genome-wide association analysis. Bioinformatics. 2007;23:1294-1296.
46. R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. Accessed at April 11, 2014.
47. Kristic J, Vuckovic F, Menni C, et al. Glycans are a novel biomarker of chronological and biological ages. J Gerontol A Biol Sci Med Sci. 2014;69:779-789.
48. Menni C, Keser T, Mangino M, et al. Glycosylation of Immunoglobulin G: role of genetic and epigenetic influences. PLoS One. 2013;8:e82558.
49. Ebringer A, Doyle AE. Raised serum IgG levels in hypertension. Br Med J. 1970;2:146-148.
50. Ohara N, Hanyu O, Hirayama S, et al. Hypertension increases urinary excretion of immunoglobulin G, ceruloplasmin and transferrin in normoalbuminuric patients with type 2 diabetes mellitus. J Hypertens. 2014;32:432-438.
51. Zabay JM, Marco J, Soler J, et al. Association of HLA-DRB3∗0202 and serum IgG antibodies to Chlamydia pneumoniae with essential hypertension in a highly homogeneous population from Majorca (Balearic Islands, Spain). J Hum Hypertens. 2005;19:615-622.
52. White FN, Grollman A. Autoimmune factors associated with infarction of the kidney. Nephron. 1964;204:93-102.
53. Guzik TJ, Hoch NE, Brown KA, et al. Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med. 2007;204:2449-2460.
54. Marvar PJ, Thabet SR, Guzik TJ, et al. Central and peripheral mechanisms of T-lymphocyte activation and vascular inflammation produced by angiotensin II-induced hypertension. Circ Res. 2010;107:263-270.
55. Crowley SD, Song YS, Lin EE, et al. Lymphocyte responses exacerbate angiotensin II-dependent hypertension. Am J Physiol Regul Integr Comp Physiol. 2010;298:R1089-1097.
56. Tran LT, MacLeod KM, McNeill JH. Chronic etanercept treatment prevents the development of hypertension in fructose-fed rats. Mol Cell Biochem. 2009;330:219-228.
57. Venegas-Pont M, Manigrasso MB, Grifoni SC, et al. Tumor necrosis factor-alpha antagonist etanercept decreases blood pressure and protects the kidney in a mouse model of systemic lupus erythemato-sus. Hypertension. 2010;56:643-649.
58. Schrader LI, Kinzenbaw DA, Johnson AW, et al. IL-6 deficiency protects against angiotensin II induced endothelial dysfunction and hypertrophy. Arterioscler Thromb Vasc Biol. 2007;27: 2576-2581.
59. Brands MW, Banes-Berceli AK, Inscho EW, et al. Interleukin 6 knockout prevents angiotensin II hypertension: role of renal vaso-constriction and janus kinase 2/signal transducer and activator of transcription 3 activation. Hypertension. 2010;56:879-884.
60. Harrison DG, Guzik TJ, Lob HE, et al. Inflammation, immunity, and hypertension. Hypertension. 2011;57:132-140.
61. Montecucco F, Pende A, Quercioli A, et al. Inflammation in the pathophysiology of essential hypertension. J Nephrol. 2011;24:23-34.
62. Basta M, Branch DR. 7(th) International Immunoglobulin Conference: Mechanisms of Action. Clin Exp Immunol. 2014;178(Suppl 1):111.
63. Anthony RM, Wermeling F, Ravetch JV. Novel roles for the IgG Fc glycan. Ann NY Acad Sci. 2012;1253:170-180.
64. Karsten CM, Pandey MK, Figge J, et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcgRIIB and dectin-1. Nat Med. 2012;18:1401-1406.
65. Kapur R, Kustiawan I, Vestrheim A, et al. A prominent lack of IgG1-Fc fucosylation of platelet alloantibodies in pregnancy. Blood. 2014;123:471-480.
66. Kaneko Y, Nimmerjahn F, Ravetch JV. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science. 2006;313:670-673.
67. Anthony RM, Nimmerjahn F, Ashline DJ, et al. Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc. Science. 2008;320:373-376.
68. Anthony RM, Ravetch JV. A novel role for the IgG Fc glycan: the anti-inflammatory activity of sialylated IgG Fcs. J Clin Immunol. 2010;30(Suppl 1):S9-S14.