Aberrant glycosylation in the left ventricle and plasma of rats with cardiac hypertrophy and heart failure

PLoS ONE

Volumn 11, Issue 6, 2016, Pages

  Nagai Okatani, Chiaki ^a,b   Minamino, Naoto ^a  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA LEVO FUCOSIDASE; ATRIAL NATRIURETIC FACTOR; CYSTEINE AND GLYCINE RICH PROTEIN 3; GLYCAN; GLYCOSIDASE; GLYCOSYLTRANSFERASE; MUCIN; PEPTIDE; PROTEIN; UNCLASSIFIED DRUG; GLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C1GALT1 GENE; C1GALT1C1 GENE; CONTROLLED STUDY; DAHL SALT SENSITIVE RAT; DOWN REGULATION; ENZYME ACTIVITY; FUCA1 GENE; FUCA2 GENE; FUCOSYLATION; FUT8 GENE; GALNT1 GENE; GALNT2 GENE; GALNT7 GENE; GENE; GENE EXPRESSION; GLB1 GENE; HEART FAILURE; HEART FUNCTION; HEART LEFT VENTRICLE; HEART VENTRICLE HYPERTROPHY; LECTIN MICROARRAY; MALE; MICROARRAY ANALYSIS; NONHUMAN; OLIGOMERIZATION; PLASMA; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN GLYCOSYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; RAT; UPREGULATION; ANIMAL; CARDIOMEGALY; DAHL RAT; GENE EXPRESSION PROFILING; GENETICS; GLYCOSYLATION; HEART VENTRICLE; HYPERTENSION; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; PATHOPHYSIOLOGY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; CARDIOMEGALY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION PROFILING; GLYCOPROTEINS; GLYCOSYLATION; HEART FAILURE; HEART VENTRICLES; HYPERTENSION; MALE; PROTEOMICS; RATS; RATS, INBRED DAHL; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84975815576     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0150210     Document Type: Article

References (55)

1. Nishikimi T, Kuwahara K, Nakao K. Current biochemistry, molecular biology, and clinical relevance of natriuretic peptides. J Cardiol. 2011; 57: 131-140. doi: 10.1016/j.jjcc.2011.01.002 PMID: 21296556
2. Gaggin HK, Januzzi JL. Biomarkers and diagnostics in heart failure. Biochim Biophys Acta. 2013; 1832: 2442-2450. doi: 10.1016/j.bbadis.2012.12.014 PMID: 23313577
3. Chowdhury P, Kehl D, Choudhary R, Maisel A. The use of biomarkers in the patient with heart failure. Curr Cardiol Rep. 2013; 15: 372. doi: 10.1007/s11886-013-0372-4 PMID: 23644993
4. van Kimmenade RR, and Januzzi JL Jr. Emerging biomarkers in heart failure. Clin Chem. 2012; 58: 127-138. doi: 10.1373/clinchem.2011.165720 PMID: 22086968
5. Mann M, Jensen ON. Proteomic analysis of post-translational modifications. Nat Biotechnol. 2003; 21: 255-261. PMID: 12610572
6. Rifai N, Gillette MA, Carr SA. Protein biomarker discovery and validation: the long and uncertain path to clinical utility. Nat Biotechnol. 2006; 24: 971-983. PMID: 16900146
7. Van Eyk JE. Overview: the maturing of proteomics in cardiovascular research. Circ Res. 2011; 108: 490-498. doi: 10.1161/CIRCRESAHA.110.226894 PMID: 21335431
8. Kuzmanov U, Kosanam H, Diamandis EP. The sweet and sour of serological glycoprotein tumor biomarker quantification. BMC Med. 2013; 11: 31. doi: 10.1186/1741-7015-11-31 PMID: 23390961
9. Ufret-Vincenty CA, Baro DJ, Lederer WJ, Rockman HA, Quinones LE, Santana LF. Role of sodium channel deglycosylation in the genesis of cardiac arrhythmias in heart failure. J Biol Chem. 2001; 276: 28197-28203. PMID: 11369778
10. Michele DE, Kabaeva Z, Davis SL, Weiss RM, Campbell KP. Dystroglycan matrix receptor function in cardiac myocytes is important for limiting activity-induced myocardial damage. Circ Res. 2009; 105: 984-993. doi: 10.1161/CIRCRESAHA.109.199489 PMID: 19797173
11. Crossman DJ, Ruygrok PN, Ruygrok PR, Soeller C, Cannell MB. Changes in the organization of excitation-contraction coupling structures in failing human heart. PLoS One. 2011; 6: e17901. doi: 10.1371/journal.pone.0017901 PMID: 21408028
12. Nishikimi T, Yoshihara F, Horinaka S, Kobayashi N, Mori Y, Tadokoro K, et al. Chronic administration of adrenomedullin attenuates transition from left ventricular hypertrophy to heart failure in rats. Hypertension. 2003; 42: 1034-1041. PMID: 14568998
13. Kuno A, Itakura Y, Toyoda M. Development of a data-mining system for differential profiling of cell glycoproteins based on lectin microarray. J Proteomics Bioinform. 2008; 1: 68-72.
14. Tateno H, Kuno A, Itakura Y, Hirabayashi J. A versatile technology for cellular glycomics using lectin microarray. Methods Enzymol. 2010; 478: 181-195. doi: 10.1016/S0076-6879(10)78008-3 PMID: 20816480
15. Hirabayashi J, Yamada M, Kuno A, Tateno H. Lectin microarrays: concept, principle and applications. Chem Soc Rev. 2013; 42: 4443-4458. doi: 10.1039/c3cs35419a PMID: 23443201
16. Nakagawa T, Uozumi N, Nakano M, Mizuno-Horikawa Y, Okuyama N, Taguchi T, et al. Fucosylation of N-glycans regulates the secretion of hepatic glycoproteins into bile ducts. J Biol Chem. 2006; 281: 29797-806. PMID: 16899455
17. Ju T, Xia B, Aryal RP, Wang W, Wang Y, Ding X, et al. A novel fluorescent assay for T-synthase activity. Glycobiology. 2011; 21: 352-362. doi: 10.1093/glycob/cwq168 PMID: 20959392
18. Wood S. A sensitive fluorometric assay for alpha-kl-fucosidase. Clin Chim Acta. 1975; 58: 251-256. PMID: 234314
19. Nagai C, Minamino N. Direct chemiluminescent enzyme immunoassay for atrial natriuretic peptide in mammalian plasma using a PEGylated antibody. Anal Biochem. 2014; 461: 10-16. doi: 10.1016/j.ab.2014.05.022 PMID: 24907507
20. Aburaya M, Minamino N, Hino J, Kangawa K, Matsuo H. Distribution and molecular forms of brain natriuretic peptide in the central nervous system, heart and peripheral tissue of rat. Biochem Biophys Res Commun. 1989; 165: 880-887. PMID: 2532011
21. Katafuchi T, Kikumoto K, Hamano K, Kangawa K, Matsuo H, Minamino N. Calcitonin receptor-stimulating peptide, a new member of the calcitonin gene-related peptide family. Its isolation from porcine brain, structure, tissue distribution, and biological activity. J Biol Chem. 2003; 278: 12046-12054. PMID: 12556539
22. Matsumura K, Higashida K, Ishida H, Hata Y, Yamamoto K, Shigeta M, et al. Carbohydrate binding specificity of a fucose-specific lectin from Aspergillus oryzae: a novel probe for core fucose. J Biol Chem. 2007; 282: 15700-15708. PMID: 17383961
23. Rinderle SJ, Goldstein IJ, Matta KL, Ratcliffe RM. Isolation and characterization of amaranthin, a lectin present in the seeds of Amaranthus caudatus, that recognizes the T- (or cryptic T)-antigen. J Biol Chem. 1989; 264: 16123-16131. PMID: 2777780
24. Sikora E, Arendt T, Bennett M, Narita M. Impact of cellular senescence signature on ageing research. Ageing Res Rev. 2011; 10: 146-152. doi: 10.1016/j.arr.2010.10.002 PMID: 20946972
25. Lunde IG, Aronsen JM, Kvaløy H, Qvigstad E, Sjaastad I, Tønnessen T, et al. Cardiac O-GlcNAc signaling is increased in hypertrophy and heart failure. Physiol Genomics. 2012; 44: 162-172. doi: 10.1152/physiolgenomics.00016.2011 PMID: 22128088
26. Liddy KA, White MY, Cordwell SJ. Functional decorations: post-translational modifi cations and heart disease delineated by targeted proteomics. Genome Med. 2013; 5: 20. doi: 10.1186/gm424 PMID: 23445784
27. Bennett EP, Mandel U, Clausen H, Gerken T a, Fritz T a, Tabak L a. Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology. 2012; 22: 736-756. doi: 10.1093/glycob/cwr182 PMID: 22183981
28. Gerken TA, Ten Hagen KG, Jamison O. Conservation of peptide acceptor preferences between Drosophila and mammalian polypeptide-GalNAc transferase ortholog pairs. Glycobiology. 2008; 18: 861-870. doi: 10.1093/glycob/cwn073 PMID: 18669915
29. Bennett E, Hassan H, Hollingsworth M, Clausen H. A novel human UDP-N-acetyl-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase, GalNAc-T7, with specificity for partial GalNAc-glycosylated acceptor substrates. FEBS Lett. 1999; 460: 226-230. PMID: 10544240
30. Wang Y, Ju T, Ding X, Xia B, Wang W, Xia L, et al. Cosmc is an essential chaperone for correct protein O-glycosylation. Proc Natl Acad Sci U S A. 2010; 107: 9228-9233. doi: 10.1073/pnas.0914004107 PMID: 20439703
31. Tian E, Stevens SR, Guan Y, Springer DA, Anderson SA, Starost MF, et al. Galnt1 is required for normal heart valve development and cardiac function. PLoS One. 2015; 10: e0115861. doi: 10.1371/journal.pone.0115861 PMID: 25615642
32. Yu H, Zhu M, Qin Y, Zhong Y, Yan H, Wang Q, et al. Analysis of glycan-related genes expression and glycan profiles in mice with liver fibrosis. J Proteome Res. 2012; 11: 5277-5285. doi: 10.1021/pr300484j PMID: 23043565
33. Kessler EL, Boulaksil M, van Rijen HVM, Vos MA, van Veen TAB. Passive ventricular remodeling in cardiac disease: focus on heterogeneity. Front Physiol. 2014; 5: 482. doi: 10.3389/fphys.2014.00482 PMID: 25566084
34. Doi R, Masuyama T, Yamamoto K, Doi Y, Mano T, Sakata Y, et al. Development of different phenotypes of hypertensive heart failure: systolic versus diastolic failure in Dahl salt-sensitive rats. J Hypertens. 2000; 18: 111-120. PMID: 10678551
35. Vafiadaki E, Arvanitis DA, Sanoudou D. Muscle LIM Protein: Master regulator of cardiac and skeletal muscle functions. Gene. 2015; 566: 1-7. doi: 10.1016/j.gene.2015.04.077 PMID: 25936993
36. Boateng SY, Belin RJ, Geenen DL, Margulies KB, Martin JL, Hoshijima M, et al. Cardiac dysfunction and heart failure are associated with abnormalities in the subcellular distribution and amounts of oligomeric muscle LIM protein. Am J Physiol Heart Circ Physiol. 2007; 292: H259-269. PMID: 16963613
37. Boateng SY, Senyo SE, Qi L, Goldspink PH, Russell B. Myocyte remodeling in response to hypertrophic stimuli requires nucleocytoplasmic shuttling of muscle LIM protein. J Mol Cell Cardiol. 2009; 47: 426-435. doi: 10.1016/j.yjmcc.2009.04.006 PMID: 19376126
38. Steentoft C, Vakhrushev SY, Joshi HJ, Kong Y, Vester-Christensen MB, Schjoldager KT-BG, et al. Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J. 2013; 32: 1478-1488. doi: 10.1038/emboj.2013.79 PMID: 23584533
39. Papalouka V, Arvanitis DA, Vafiadaki E, Mavroidis M, Papadodima SA, Spiliopoulou CA, et al. Muscle LIM protein interacts with cofilin 2 and regulates F-actin dynamics in cardiac and skeletal muscle. Mol Cell Biol. 2009; 29: 6046-6058. doi: 10.1128/MCB.00654-09 PMID: 19752190
40. Heineke J, Ruetten H, Willenbockel C, Gross SC, Naguib M, Schaefer A, et al. Attenuation of cardiac remodeling after myocardial infarction by muscle LIM protein-calcineurin signaling at the sarcomeric Z-disc. Proc Natl Acad Sci U S A. 2005; 102: 1655-1660. PMID: 15665106
41. Agrawal P, Kurcon T, Pilobello KT, Rakus JF, Koppolu S, Liu Z, et al. Mapping posttranscriptional regulation of the human glycome uncovers microRNA defining the glycocode. Proc Natl Acad Sci U S A. 2014; 111: 4338-4343. doi: 10.1073/pnas.1321524111 PMID: 24591635
42. Kasper BT, Koppolu S, Mahal LK. Insights into miRNA regulation of the human glycome. Biochem Biophys Res Commun. 2014; 445: 774-779. doi: 10.1016/j.bbrc.2014.01.034 PMID: 24463102
43. Gaziel-Sovran A, Segura MF, Di Micco R, Collins MK, Hanniford D, Vega-Saenz de Miera E, et al. miR-30b/30d regulation of GalNAc transferases enhances invasion and immunosuppression during metastasis. Cancer Cell. 2011; 20: 104-118. doi: 10.1016/j.ccr.2011.05.027 PMID: 21741600
44. Kannagi R, Sakuma K, Miyazaki K, Lim K-T, Yusa A, Yin J, et al. Altered expression of glycan genes in cancers induced by epigenetic silencing and tumor hypoxia: clues in the ongoing search for new tumor markers. Cancer Sci. 2010; 101: 586-593. doi: 10.1111/j.1349-7006.2009.01455.x PMID: 20085584
45. Mi R, Song L, Wang Y, Ding X, Zeng J, Lehoux S, et al. Epigenetic silencing of the chaperone Cosmc in human leukocytes expressing tn antigen. J Biol Chem. 2012; 287: 41523-41533. doi: 10.1074/jbc.M112.371989 PMID: 23035125
46. Ogihara T, Asano T, Ando K, Sakoda H, Anai M, Shojima N, et al. High-salt diet enhances insulin signaling and induces insulin resistance in Dahl salt-sensitive rats. Hypertension. 2002; 40: 83-89. PMID: 12105143
47. Schellenberger U, O'Rear J, Guzzetta A. The precursor to B-type natriuretic peptide is an O-linked glycoprotein. Arch Biochem Biophys. 2006; 451: 160-166. PMID: 16750161
48. Semenov AG, Postnikov AB, Tamm NN, Seferian KR, Karpova NS, Bloshchitsyna MN, et al. Processing of pro-brain natriuretic peptide is suppressed by O-glycosylation in the region close to the cleavage site. Clin Chem. 2009; 55: 489-498. doi: 10.1373/clinchem.2008.113373 PMID: 19168558
49. Schjoldager KT-BG, Vester-Christensen MB, Bennett EP, Levery SB, Schwientek T, Yin W, et al. O-glycosylation modulates proprotein convertase activation of angiopoietin-like protein 3: possible role of polypeptide GalNAc-transferase-2 in regulation of concentrations of plasma lipids. J Biol Chem. 2010; 285: 36293-36303. doi: 10.1074/jbc.M110.156950 PMID: 20837471
50. Zhao Y-P, Xu X-Y, Fang M, Wang H, You Q, Yi C-H, et al. Decreased core-fucosylation contributes to malignancy in gastric cancer. PLoS One. 2014; 9: e94536. doi: 10.1371/journal.pone.0094536 PMID: 24732908
51. Wang X, Inoue S, Gu J, Miyoshi E. Dysregulation of TGF-beta1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc Natl Acad Sci U S A. 2005; 102: 15791-15796. PMID: 16236725
52. Wang X, Gu J, Ihara H, Miyoshi E. Core fucosylation regulates epidermal growth factor receptor-mediated intracellular signaling. J Biol Chem. 2006; 281: 2572-2577. PMID: 16316986
53. Makki N, Thiel KW, Miller FJ. The epidermal growth factor receptor and its ligands in cardiovascular disease. Int J Mol Sci. 2013; 14: 20597-20613. doi: 10.3390/ijms141020597 PMID: 24132149
54. Rosenkranz S. TGF-beta1 and angiotensin networking in cardiac remodeling. Cardiovasc Res. 2004; 63: 423-432. PMID: 15276467
55. Stefaniuk P, Cianciara J, Wiercinska-Drapalo A. Present and future possibilities for early diagnosis of hepatocellular carcinoma. World J Gastroenterol. 2010; 16: 418-424. PMID: 20101765