Quantitative N-linked glycoproteomics of myocardial ischemia and reperfusion injury reveals early remodeling in the extracellular environment

Molecular and Cellular Proteomics

Volumn 10, Issue 8, 2011, Pages

  Parker, Benjamin L ^a   Palmisano, Giuseppe ^b   Edwards, Alistair V G ^a   White, Melanie Y ^a   Engholm Keller, Kasper ^b   Lee, Albert ^c   Scott, Nichollas E ^a   Kolarich, Daniel ^c   Hambly, Brett D ^a   Packer, Nicolle H ^c   Larsen, Martin R ^b   Cordwell, Stuart J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c MACQUARIE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; GLYCOPEPTIDE; PROTEINASE; GLYCOPROTEIN; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; POLYSACCHARIDE; PROTEOME; SCLEROPROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; EXTRACELLULAR MATRIX; GLYCOBIOLOGY; GLYCOSYLATION; HEART INFARCTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE ISCHEMIA; ISOLATED HEART; ISOTOPE LABELING; LIQUID CHROMATOGRAPHY; MALE; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEOMICS; QUANTITATIVE ANALYSIS; RAT; REPERFUSION INJURY; ANIMAL; CARBOHYDRATE ANALYSIS; CHEMISTRY; HEART; HEART MUSCLE; HEART VENTRICLE REMODELING; HEMODYNAMICS; IN VITRO STUDY; ION EXCHANGE CHROMATOGRAPHY; ISOLATION AND PURIFICATION; LEWIS RAT; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN DEGRADATION; TANDEM MASS SPECTROMETRY;

RATTUS;

ANIMALS; CARBOHYDRATE SEQUENCE; CHROMATOGRAPHY, ION EXCHANGE; EXTRACELLULAR MATRIX PROTEINS; GLYCOPROTEINS; HEART; HEMODYNAMICS; MALE; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; PEPTIDE FRAGMENTS; POLYSACCHARIDES; PROTEOLYSIS; PROTEOME; PROTEOMICS; RATS; RATS, INBRED LEW; TANDEM MASS SPECTROMETRY; VENTRICULAR REMODELING;

EID: 80051655470     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.006833     Document Type: Article

References (70)

1. Ohtsubo, K., and Marth, J. D. (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126, 855-867 (Pubitemid 44310784)
2. Rudd, P. M., Elliott, T., Cresswell, P., Wilson, I. A., and Dwek, R. A. (2001) Glcosylation and the immune system. Science 291, 2370-2376
3. Helenius, A., and Aebi, M. (2001) Intracellular functions of N-linked glycans. Science 291, 2364-2369 (Pubitemid 32231791)
4. Lowe, J. B. (2001) Glycosylation, immunity and autoimmunity. Cell 104, 809-812
5. Ohtsubo, K., Takamatsu, S., Minowa, M. T., Yoshida, A., Takeuchi, M., and Marth, J. D. (2005) Dietary and genetic control of glucose transporter 2 glycosylation promotes insulin secretion in suppressing diabetes. Cell 123, 1307-1321 (Pubitemid 41821787)
6. Thomas, P. (1996) Cell surface sialic acid as a mediator of metastatic potential in colorectal cancer. Cancer J. 9, 32-36
7. Cordwell, S. J., and Thingholm, T. (2010) Technologies for plasma membrane proteomics. Proteomics 10, 1-17
8. Ghosh, D., Beavis, R. C., and Wilkins, J. A. (2008) The identification and characterization of membranome components. J. Proteome Res. 7, 1572-1583
9. Lee, A., Kolarich, D., Haynes, P. A., Jensen, P. H., Baker, M. S., and Packer, N. H. (2009) Rat liver membrane glycoproteome: enrichment by phase partitioning and glycoprotein capture. J. Proteome Res. 8, 770-781
10. Gundry, R. L., Raginski, K., Tarasova, Y., Tchernyshyov, I., Bausch-Fluck, D., Elliott, S. T., Boheler, K. R., Van Eyk, J. E., and Wollscheid, B. (2009) The mouse C2C12 myoblast cell surface N-linked glycoproteome: identification, glycosite occupancy, and membrane orientation. Mol. Cell. Proteomics 8, 2555-2569
11. Wollscheid, B., Bausch-Fluck, D., Henderson, C., O'Brien, R., Bibel, M., Schiess, R., Aebersold, R., and Watts, J. D. (2009) Mass spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat. Biotechnol. 27, 378-386
12. McDonald, C. A., Yang, J. Y., Marathe, V., Yen, T. Y., and Macher, B. A. (2009) Combining results from lectin affinity chromatography and glycocapture approaches substantially improves the coverage of the glycoproteome. Mol. Cell. Proteomics 8, 287-301
13. Larsen, M. R., Jensen, S. S., Jakobsen, L. A., and Heegaard, N. H. H. (2007) Exploring the sialiome using titanium dioxide chromatography and mass spectrometry. Mol. Cell. Proteomics 6, 1778-1787 (Pubitemid 350031679)
14. Scott, N. E., Parker, B. L., Connolly, A. M., Paulech, J., Edwards, A. V. G., Crossett, B., Falconer, L., Kolarich, D., Djordjevic, S. P., Højrup, P., Packer, N. H., Larsen, M. R., and Cordwell, S. J. (2011) Simultaneous glycan-peptide characterization using hydrophilic interaction chromatography and parallel fragmentation by CID, HCD and ETD-MS applied to the N-linked glycoproteome of Campylobacter jejuni. Mol. Cell. Proteomics 10, M000031MCP201
15. Kaji, H., Yamauchi, Y., Takahashi, N., and Isobe, T. (2006) Mass spectrometric identification of N-linked glycopeptides using lectin-mediated affinity capture and glycosylation site-specific stable isotope tagging. Nat. Protoc. 1, 3019-3027
16. Zielinska, D. F., Gnad, F., Wiśniewski, J. R., and Mann, M. (2010) Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897-907
17. Zhang, H., Li, X., Martin, D. B., and Aebersold, R. (2003) Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat. Biotechnol. 21, 660-666 (Pubitemid 36638093)
18. Tian, Y., Zhou, Y., Elliott, S., Aebersold, R., and Zhang, H. (2007) Solid-phase extraction of N-linked glycopeptides. Nat. Protoc. 2, 334-339 (Pubitemid 47040048)
19. Hägglund, P., Bunkenborg, J., Elortza, F., Jensen, O. N., and Roepstorff, P. (2004) A new strategy for identification of N-glycosylated proteins and unambiguous assignment of their glycosylation sites using HILIC enrichment and partial deglycosylation. J. Proteome Res. 3, 556-566 (Pubitemid 39207360)
20. Ding, W., Nothaft, H., Szymanski, C. M., and Kelly, J. (2009) Identification and quantification of glycoproteins using ion-pairing normal-phase liquid chromatography and mass spectrometry. Mol. Cell. Proteomics 8, 2170-2185
21. Post, J. A. (1992) Removal of sarcolemmal sialic acid residues results in a loss of sarcolemmal functioning and integrity. Am. J. Physiol. 263, H147-52
22. Splawski, I., Timothy, K. W., Tateyama, M., Clancy, C. E., Malhotra, A., Beggs, A. H., Cappuccio, F. P., Sagnella, G. A., Kass, R. S., and Keating, M. T. (2002) Variant of SCN5A sodium channel implicated in risk of cardiac arrhythmia. Science 297, 1333-1336 (Pubitemid 34913168)
23. Montpetit, M. L., Stocker, P. J., Schwetz, T. A., Harper, J. M., Norring, S. A., Schaffer, L., North, S. J., Jang-Lee, J., Gilmartin, T., Head, S. R., Haslam, S. M., Dell, A., Marth, J. D., and Bennett, E. S. (2009) Regulated and aberrant glycosylation modulate cardiac electrical signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 16517-16522
24. Ufret-Vincenty, C. A., Baro, D. J., Lederer, W. J., Rockman, H. A., Quinones, L. E., and Santana, L. F. (2001) Role of sodium channel deglycosylation in the genesis of cardiac arrhythmias in heart failure. J. Biol. Chem. 276, 28197-28203
25. Wang, Y., and Sun, Z. (2009) Current understanding of klotho. Ageing Res. Rev. 8, 43-51
26. Bolli R., and Marban E. (1999) Molecular and cellular mechanisms of myocardial stunning. Physiol. Revs. 79, 609-634 (Pubitemid 29210931)
27. Banerjee, I., Yekkala, K., Borg, T. K., and Baudino, T. A. (2006) Dynamic interactions between myocytes, fibroblasts, and extracellular matrix. Ann. N.Y. Acad. Sci. 1080, 76-84 (Pubitemid 44955414)
28. Zamilpa, R., and Lindsey, M. L. (2010) Extracellular matrix turnover and signaling during cardiac remodeling following MI: causes and consequences. J. Mol. Cell. Cardiol. 48, 558-563
29. Dobaczewski, M., Gonzalez-Quesada, C., and Frangogiannis, N. G. (2010) The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J. Mol. Cell. Cardiol. 48, 504-511
30. Dobaczewski, M., Bujak, M., Zymek, P., Ren, G., Entman, M. L., and Frangogiannis, N. G. (2006) Extracellular matrix remodeling in canine and mouse myocardial infarcts. Cell Tissue Res. 324, 475-488 (Pubitemid 43673489)
31. Spinale, F. G. (2007) Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Revs. 87, 1285-1342
32. Boersema, P. J., Raijmakers, R., Lemeer, S., Mohammed, S., and Heck, A. J. (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat. Protoc. 4, 484-494
33. Palmisano, G., Lendal, S. E., Engholm-Keller, K., Leth-Larsen, R., Parker, B. L., and Larsen, M. R. (2010) Selective enrichment of sialic acid-containing glycopeptides using titanium dioxide chromatography with analysis by HILIC and mass spectrometry. Nat. Protoc. 5, 1974-1982
34. Mysling, S., Palmisano, G., Højrup, P., and Thaysen-Andersen, M. (2010) Utilizing ion-pairing hydrophilic interaction chromatography solid phase extraction for efficient glycopeptide enrichment in glycoproteomics. Anal. Chem. 82, 5598-5609
35. Boersema, P. J., Divecha, N., Heck, A. J., and Mohammed, S. (2007) Evaluation and optimization of ZIC-HILIC-RP as an alternative MudPIT strategy. J. Proteome Res. 6, 937-946 (Pubitemid 46480458)
36. Gilar, M., Olivova, P., Daly, A. E., and Gebler, J. C. (2005) Orthogonality of separation in two-dimensional liquid chromatography. Anal. Chem. 77, 6426-6434 (Pubitemid 41436983)
37. Mortensen, P., Gouw, J. W., Olsen, J. V., Ong, S. E., Rigbolt, K. T., Bunkenborg, J., Cox, J., Foster, L. J., Heck, A. J., Blagoev, B., Andersen, J. S., and Mann, M. (2010) MSQuant, an open source platform for mass spectrometry-based quantitative proteomics. J. Proteome Res. 9, 393-403
38. van Breukelen, B., van den Toorn, H. W., Drugan, M. M., and Heck, A. J. (2009) StatQuant: a post-quantification analysis toolbox for improving quantitative mass spectrometry. Bioinformatics 25, 1472-1473
39. Lee, A., Chick, J. M., Kolarich, D., Haynes, P. A., Robertson, G. R., Tsoli, M., Jankova, L., Clarke, S. J., Packer, N. H., and Baker, M. S. (2010) Liver membrane proteome glycosylation changes in mice bearing an extrahepatic tumour. Mol. Cell. Proteomics [Epub ahead of print Feb 18]
40. Chen, R., Jiang, X., Sun, D., Han, G., Wang, F., Ye, M., Wang, L., and Zou, H. (2009) Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. J. Proteome Res. 8, 651-661
41. Wright, H. T. (1991) Sequence and structure determinants of the nonenzymatic deamidation of asparagine and glutamine residues in proteins. Protein Eng. 4, 283-294
42. White, M. Y., Cordwell, S. J., McCarron, H. C., Tchen, A. S., Hambly, B. D., and Jeremy, R. W. (2003) Modifications of myosin-regulatory light chain correlate with function of stunned myocardium. J. Mol. Cell. Cardiol. 35, 833-840 (Pubitemid 36773596)
43. Robinson, N. E. (2002) Protein deamidation. Proc. Natl. Acad. Sci. U.S.A. 99, 5283-5288
44. Cohn, J. N., Ferrari, R., Sharpe, N. Int. Forum Cardiac Remodeling (2000) Cardiac remodeling - concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. J. Am. Coll. Cardiol. 35, 569-582 (Pubitemid 30167013)
45. Shaw, S. Y. (2009) Molecular imaging in cardiovascular disease: targets and opportunities. Nat. Rev. Cardiol. 6, 569-579
46. Dewald, O., Ren, G., Duerr, G. D., Zoerlein, M., Klemm, C., Gersch, C., Tincey, S., Michael, L. H., Entman, M. L., and Frangogiannis, N. G. (2004) Of mice and dogs: species-specific differences in the inflammatory response following myocardial infarction. Am. J. Pathol. 164, 665-677 (Pubitemid 38364680)
47. Villarreal, F., Omens, J., Dillmann, W., Risteli, J., Nguyen, J., and Covell, J. (2004) Early degradation and serum appearance of type I collagen fragments after myocardial infarction. J. Mol. Cell. Cardiol. 36, 597-601 (Pubitemid 38469950)
48. Mukherjee, R., Brinsa, T. A., Dowdy, K. B., Scott, A. A., Baskin, J. M., Deschamps, A. M., Lowry, A. S., Escobar, G. P., Lucas, D. G., Yarbrough, W. M., Zile, M. R., and Spinale, F. G. (2003) Myocardial infarct expansion and matrix metalloproteinase inhibition. Circulation 107, 618-625 (Pubitemid 36176814)
49. Chancey, A. L., Brower, G. L., and Janicki, J. S. (2002) Cardiac mast cell-mediated activation of gelatinase and alteration of ventricular diastolic function. Am. J. Physiol. Heart Circ. Physiol. 282, H2152-H2158 (Pubitemid 34663025)
50. Wolters, P. J., Pham, C. T., Muilenburg, D. J., Ley, T. J., and Caughey, G. H. (2001) Dipeptidyl peptidase I is essential for activation of mast cell chymases, but not tryptases, in mice. J. Biol. Chem. 276, 18551-18556
51. Henningsson, F., Wolters, P., Chapman, H. A., Caughey, G. H., and Pejler, G. (2003) Mast cell cathepsins C and S control levels of carboxypeptidase A and the chymase, mouse mast cell protease 5. Biol. Chem. 384, 1527-1531 (Pubitemid 37508656)
52. Judd, J. T., and Wexler, B. C. (1975) Prolyl hydroxylase and collagen metabolism after experimental myocardial infarction. Am. J. Physiol. 228, 212-216
53. Wei, S., Chow, L. T., Shum, I. O., Qin, L., and Sanderson, J. E. (1999) Left and right ventricular collagen type I/III ratios and remodeling post-myocardial infarction. J. Cardiac Fail. 5, 117-126 (Pubitemid 29297804)
54. Herrmann, K. L., McCulloch, A. D., and Omens, J. H. (2003) Glycated collagen cross-linking alters cardiac mechanics in volume-overload hypertrophy. Am. J. Physiol.Heart Circ. Physiol. 284, H1277-H1284 (Pubitemid 36348591)
55. McCurdy, S., Baicu, C. F., Heymans, S., and Bradshaw, A. D. (2010) Cardiac extracellular matrix remodeling: fibrillar collagens and secreted protein acidic and rich in cysteine (SPARC). J. Mol. Cell. Cardiol. 48, 544-549
56. Wu, R. X., Laser, M., Han, H., Varadarajulu, J., Schuh, K., Hallhuber, M., Hu, K., Ertl, G., Hauck, C. R., and Ritter, O. (2006) Fibroblast migration after myocardial infarction is regulated by transient SPARC expression. J. Mol. Med. 84, 241-252 (Pubitemid 43291013)
57. Schellings, M. W., Vanhoutte, D., Swinnen, M., Cleutjens, J. P., Debets, J., van Leeuwen, R. E., d'Hooge, J., Van de Werf, F., Carmeliet, P., Pinto, Y. M., Sage, E. H., and Heymans, S. (2009) Absence of SPARC results in increased cardiac rupture and dysfunction after acute myocardial infarction. J. Exp. Med. 206, 113-123
58. Visconti, R. P., and Markwald, R. R. (2006) Recruitment of new cells into the postnatal heart: potential modification of phenotype by periostin. Ann. N.Y. Acad. Sci. 1080, 19-33 (Pubitemid 44955410)
59. Oka, T., Xu, J., Kaiser, R. A., Melendez, J., Hambleton, M., Sargent, M. A., Lorts, A., Brunskill, E. W., Dorn, G. W., 2nd, Conway, S. J., Aronow, B. J., Robbins, J., and Molkentin, J. D. (2007) Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ. Res. 101, 313-321 (Pubitemid 47351119)
60. Shimazaki, M., Nakamura, K., Kii, I., Kashima, T., Amizuka, N., Li, M., Saito, M., Fukuda, K., Nishiyama, T., Kitajima, S., Saga, Y., Fukayama, M., Sata, M., and Kudo, A. (2008) Periostin is essential for cardiac healing after acute myocardial infarction. J. Exp. Med. 205, 295-303 (Pubitemid 351281595)
61. Dinh, W., Bansemir, L., Füth, R., Nickl, W., Stasch, J. P., Coll-Barroso, M., Lapp, H., Bufe, A., Wolfertz, J., Scheffold, T., and Lankisch, M. (2009) Increased levels of laminin and collagen type VI may reflect early remodelling in patients with acute myocardial infarction. Acta Cardiol. 64, 329-334
62. Shai, S. Y., Harpf, A. E., Babbitt, C. J., Jordan, M. C., Fishbein, M. C., Chen, J., Omura, M., Leil, T. A., Becker, K. D., Jiang, M., Smith, D. J., Cherry, S. R., Loftus, J. C., and Ross, R. S. (2002) Cardiac myocyte-specific excision of the beta-1 integrin gene results in myocardial fibrosis and cardiac failure. Circ. Res. 90, 458-464 (Pubitemid 34633916)
63. Brooks, P. C., Clark, R. A., and Cheresh, D. A. (1994) Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264, 569-571
64. Yue, W., Sun, Q., Landreneau, R., Wu, C., Siegfried, J. M., Yu, J., and Zhang, L. (2009) Fibulin-5 suppresses lung cancer invasion by inhibiting matrix metalloproteinase-7 expression. Cancer Res. 69, 6339-6346
65. + channels in the developing mouse heart. J. Physiol. 564, 683-696
66. Roberts, R. H., and Barchi, R. L. (1987) The voltage-sensitive sodium channel from rabbit skeletal muscle. Chemical characterization of subunits. J. Biol. Chem. 262, 2298-2303
67. Jones, S. P., Zachara, N. E., Ngoh, G. A., Hill, B. G., Teshima, Y., Bhatnagar, A., Hart, G. W., and Marbán, E. (2008) Cardioprotection by Nacetylglucosamine linkage to cellular proteins. Circulation 117, 1172-1182 (Pubitemid 351544067)
68. Langer, G. A., Frank, J. S., Nudd, L. M., and Seraydarian, K. (1976) Sialic acid: effect of removal on calcium exchange-abililty of cultured heart cells. Science 193, 1013-1015
69. Frank, J. S., Langer, G. A., Nudd, L. M., and Seraydarian, K. (1977) The myocardial cell surface, its histochemistry, and the effect of sialic acid and calcium removal on its stucture and cellular ionic exchange. Circ. Res. 41, 702-714 (Pubitemid 8216882)
70. Yee, H. F., Jr., Kuwata, J. H., and Langer, G. A. (1991) Effects of neuraminidase on cellular calcium and contraction in cultured cardiac myocytes. J. Mol. Cell. Cardiol. 23, 175-185