Top-down targeted proteomics for deep sequencing of tropomyosin isoforms

Journal of Proteome Research

Volumn 12, Issue 1, 2013, Pages 187-198

  Peng, Ying ^a,b   Chen, Xin ^a,b   Zhang, Han ^a,c   Xu, Qingge ^a,b   Hacker, Timothy A ^d   Ge, Ying ^a,b,c  

^a Human Proteomics Program   (United States)

^b Department of Cell and Regenerative Biology ^*  (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

^d U of WI School of Medicine and Public Health   (United States)

Author keywords

Actin filament; Electron capture dissociation; Mass spectrometry; Muscle contraction; Tropomyosin

Indexed keywords

TROPOMYOSIN;

ACETYLATION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEART MUSCLE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN POLYMORPHISM; PROTEOMICS;

ACTINS; ANIMALS; CELL LINE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MASS SPECTROMETRY; MICE; MICROFILAMENT PROTEINS; MYOCARDIUM; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; SWINE; TROPOMYOSIN;

EID: 84874077075     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr301054n     Document Type: Article

References (64)

1. Gunning, P. W.; Schevzov, G.; Kee, A. J.; Hardeman, E. C. Tropomyosin isoforms: divining rods for actin cytoskeleton function. Trends Cell Biol. 2005, 15 (6), 333-341.
2. Gunning, P., Tropomyosin: introduction and historical perspective. In Tropomyosin; Gunning, P., Ed.; Springer: New York, 2008; pp 1-4.
3. Perry, S. V. Vertebrate tropomyosin: distribution, properties and function. J. Muscle Res. Cell Motil. 2001, 22 (1), 5-49.
4. Gunning, P.; O'Neill, G.; Hardeman, E. Tropomyosin-based regulation of the actin cytoskeleton in time and space. Physiol. Rev. 2008, 88 (1), 1-35.
5. Bailey, K. Tropomyosin: a new asymmetric protein component of muscle. Nature 1946, 157, 368-368.
6. Gordon, A. M.; Homsher, E.; Regnier, M. Regulation of contraction in striated muscle. Physiol. Rev. 2000, 80 (2), 853-924.
7. Kobayashi, T.; Solaro, R. J. Calcium, thin filaments, and the integrative biology of cardiac contractility. Annu. Rev. Physiol. 2005, 67, 39-67.
8. Moss, R. L.; Razumova, M.; Fitzsimons, D. P. Myosin crossbridge activation of cardiac thin filaments-Implications for myocardial function in health and disease. Circ. Res. 2004, 94 (10), 1290-1300.
9. Jagatheesan, G.; Rajan, S.; Wieczorek, D. F. Investigations into tropomyosin function using mouse models. J. Mol. Cell. Cardiol. 2010, 48 (5), 893-898.
10. Jagatheesan, G.; Rajan, S.; Ahmed, R. P. H.; Petrashevskaya, N.; Boivin, G.; Arteaga, G. M.; Tae, H. J.; Liggett, S. B.; Solaro, R. J.; Wieczorek, D. F. Striated muscle tropomyosin isoforms differentially regulate cardiac performance and myofilament calcium sensitivity. J. Muscle Res. Cell Motil. 2010, 31 (3), 227-239.
11. Vrhovski, B. T.; Thiebaud, N., P. Structure and evolution of tropomyosin. In Tropomyosin; Gunning, P., Ed.; Springer Science: New York, 2008; pp 6-23.
12. Denz, C. R.; Narshi, A.; Zajdel, R. W.; Dube, D. K. Expression of a novel cardiac-specific tropomyosin isoform in humans. Biochem. Biophys. Res. Commun. 2004, 320 (4), 1291-1297.
13. Wieczorek, D. F.; Smith, C. W. J.; Nadalginard, B. The rat alphatropomyosin gene generates a minimum of 6 different messenger-RNAs coding for striated, smooth, and non-muscle isoforms by alternative splicing. Mol. Cell. Biol. 1988, 8 (2), 679-694.
14. Nadal-Ginard, B. Muscle cell differentiation and alternative splicing. Curr. Opin. Cell Biol. 1990, 2 (6), 1058-1064.
15. Marston, S. B.; Redwood, C. S. Modulation of thin filament activation by breakdown or isoform switching of thin filament proteins-Physiological and pathological implications. Circ. Res. 2003, 93 (12), 1170-1178.
16. Leesmiller, J. P.; Helfman, D. M. The molecular-basis for tropomyosin isoform diversity. Bioessays 1991, 13 (9), 429-437.
17. Rajan, S.; Jagatheesan, G.; Karam, C. N.; Alves, M. L.; Bodi, I.; Schwartz, A.; Bulcao, C. F.; D'Souza, K. M.; Akhter, S. A.; Boivin, G. P.; Dube, D. K.; Petrashevskaya, N.; Herr, A. B.; Hullin, R.; Liggett, S. B.; Wolska, B. M.; Solaro, R. J.; Wieczorek, D. F. Molecular and functional characterization of a novel cardiac-specific human tropomyosin isoform. Circulation 2010, 121 (3), 410-418.
18. Pittenger, M. F.; Kazzaz, J. A.; Helfman, D. M. Functionalproperties of nonmuscle tropomyosin isoforms. Curr. Opin. Cell Biol. 1994, 6 (1), 96-104.
19. Vrhovski, B.; Schevzov, G.; Dingle, S.; Lessard, J. L.; Gunning, P.; Weinberger, R. P. Tropomyosin isoforms from the gamma genediffering at the C-terminus are spatially and developmentally regulated in the brain. J. Neurosci. Res. 2003, 72 (3), 373-383.
20. Wieczorek, D. F.; Jagatheesan, G.; Rajan, S. The role of tropomyosin in heart disease. In Tropomyosin; Gunning, P., Ed.; Springer Science: New York, 2008; pp 132-139.
21. Franzen, B.; Linder, S.; Uryu, K.; Alaiya, A. A.; Hirano, T.; Kato, H.; Auer, G. Expression of tropomyosin isoforms in benign and malignant human breast lesions. Br. J. Cancer 1996, 73 (7), 909-913.
22. Raval, G. N.; Bharadwaj, S.; Levine, E. A.; Willingham, M. C.; Geary, R. L.; Kute, T.; Prasad, G. Loss of expression of tropomyosin-1, a novel class II tumor suppressor that induces anoikis, in primary breast tumors. Oncogene 2003, 22 (40), 6194-6203.
23. Varga, A. E.; Stourman, N. V.; Zheng, Q.; Safina, A. F.; Quan, L.; Li, X. R.; Sossey-Alaoui, K.; Bakin, A. V. Silencing of the Tropomyosin-1 gene by DNA methylation alters tumor suppressor function of TGF-beta. Oncogene 2005, 24 (32), 5043-5052.
24. Pawlak, G.; McGarvey, T. W.; Nguyen, T. B.; Tomaszewski, J. E.; Puthiyaveettil, R.; Malkowicz, S. B.; Helfman, D. M. Alterations in tropomyosin isoform expression in human transitional cell carcinoma of the urinary bladder. Int. J. Cancer 2004, 110 (3), 368-373.
25. Hughes, J. A. I.; Cooke-Yarborough, C. M.; Chadwick, N. C.; Schevzov, G.; Arbuckle, S. M.; Gunning, P.; Weinberger, R. P. Highmolecular-weight tropomyosins localize to the contractile rings of dividing CNS cells but are absent from malignant pediatric and adult CNS tumors. Glia 2003, 42 (1), 25-35.
26. Galloway, P. G.; Likavec, M. J.; Perry, G. Tropomyosin isoform expression in normal and neoplastic astrocytes. Lab. Invest. 1990, 62 (2), 163-170.
27. Lin, J. L. C.; Geng, X.; Das Bhattacharya, S.; Yu, J. R.; Reiter, R. S.; Sastri, B.; Glazier, K. D.; Mirza, Z. K.; Wang, K. K.; Amenta, P. S.; Das, K. M.; Lin, J. J. C. Isolation and sequencing of a novel tropomyosin isoform preferentially associated with colon cancer. Gastroenterology 2002, 123 (1), 152-162.
28. Zhang, J.; Zhang, H.; Ayaz-Guner, S.; Chen, Y. C.; Dong, X. T.; Xu, Q. G.; Ge, Y. Phosphorylation, but not alternative splicing or proteolytic degradation, is conserved in human and mouse cardiac troponin T. Biochemistry 2011, 50 (27), 6081-6092.
29. Zhang, H.; Ge, Y. Comprehensive analysis of protein modifications by top-down mass spectrometry. Circ.: Cardiovasc. Genet. 2011, 4 (6), 711.
30. Roth, M. J.; Forbes, A. J.; Boyne, M. T.; Kim, Y. B.; Robinson, D. E.; Kelleher, N. L. Precise and parallel characterization of coding polymorphisms, alternative splicing, and modifications in human proteins by mass spectrometry. Mol. Cell. Proteomics 2005, 4 (7), 1002-1008.
31. Sancho Solis, R.; Ge, Y.; Walker, J. W. Single amino acid sequence polymorphisms in rat cardiac troponin revealed by top-down tandem mass spectrometry. J. Muscle Res. Cell Motil. 2008, 29 (6-8), 203-212.
32. Ayaz-Guner, S.; Zhang, J.; Li, L.; Walker, J. W.; Ge, Y. In vivo phosphorylation site mapping in mouse cardiac troponin I by highresolution top-Down electron capture dissociation mass spectrometry: Ser22/23 are the only sites basally phosphorylated. Biochemistry 2009, 48 (34), 8161-8170.
33. Dong, X.; Sumandea, C. A.; Chen, Y.-C.; Garcia-Cazarin, M. L.; Zhang, J.; Balke, C. W.; Sumandea, M. P.; Ge, Y. Augmented phosphorylation of cardiac troponin I in hypertensive heart failure. J. Biol. Chem. 2012, 287 (2), 848-857.
34. Ge, Y.; Rybakova, I. N.; Xu, Q.; Moss, R. L. Top-down highresolution mass spectrometry of cardiac myosin binding protein C revealed that truncation alters protein phosphorylation state. Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (31), 12658-12663.
35. Peng, Y.; Chen, X.; Sato, T.; Rankin, S. A.; Tsuji, R. F.; Ge, Y. Purification and high-resolution top-down mass spectrometric characterization of human salivary alpha-amylase. Anal. Chem. 2012, 84 (7), 3339-3346.
36. Xu, F.; Xu, Q.; Dong, X.; Guy, M.; Guner, H.; Hacker, T. A.; Ge, Y. Top-down high-resolution electron capture dissociation mass spectrometry for comprehensive characterization of post-translational modifications in Rhesus monkey cardiac troponin I. Int. J. Mass Spectrom. 2011, 305 (2-3), 95-102.
37. Zabrouskov, V.; Ge, Y.; Schwartz, J.; Walker, J. W. Unraveling molecular complexity of phosphorylated human cardiac troponin I by top down electron capture dissociation/electron transfer dissociation mass spectrometry. Mol. Cell. Proteomics 2008, 7 (10), 1838-1849.
38. Zhang, J.; Guy, M. J.; Norman, H. S.; Chen, Y.-C.; Xu, Q.; Dong, X.; Guner, H.; Wang, S.; Kohmoto, T.; Young, K. H.; Moss, R. L.; Ge, Y. Top-down quantitative proteomics identified phosphorylation of cardiac troponin I as a candidate biomarker for chronic heart failure. J. Proteome Res. 2011, 10 (9), 4054-4065.
39. Siuti, N.; Kelleher, N. L. Decoding protein modifications using top-down mass spectrometry. Nat. Methods 2007, 4 (10), 817-821.
40. Ryan, C. M.; Souda, P.; Bassilian, S.; Ujwal, R.; Zhang, J.; Abramson, J.; Ping, P.; Durazo, A.; Bowie, J. U.; Hasan, S. S.; Baniulis, D.; Cramer, W. A.; Faull, K. F.; Whitelegge, J. P. Post-translational modifications of integral membrane proteins resolved by top-down Fourier transform mass spectrometry with collisionally activated dissociation. Mol. Cell. Proteomics 2010, 9 (5), 791-803.
41. Thomas, C. E.; Kelleher, N. L.; Mizzen, C. A. Mass spectrometric characterization of human histone H3: A bird's eye view. J. Proteome Res. 2006, 5 (2), 240-247.
42. Guan, S.; Burlingame, A. L. High mass selectivity for top-down proteomics by application of SWIFT technology. J. Am. Soc. Mass Spectrom. 2010, 21 (3), 455-459.
43. Senko, M. W.; Speir, J. P.; Mclafferty, F. W. Collisional activation of large multiply-charged ions using Fourier-transform massspectrometry. Anal. Chem. 1994, 66 (18), 2801-2808.
44. Zubarev, R. A.; Horn, D. M.; Fridriksson, E. K.; Kelleher, N. L.; Kruger, N. A.; Lewis, M. A.; Carpenter, B. K.; McLafferty, F. W. Electron capture dissociation for structural characterization of multiply charged protein cations. Anal. Chem. 2000, 72 (3), 563-573.
45. Neverova, I.; Van Eyk, J. E. Application of reversed phase high performance liquid chromatography for subproteomic analysis of cardiac muscle. Proteomics 2002, 2 (1), 22-31.
46. Horn, D. M.; Zubarev, R. A.; McLafferty, F. W. Automated reduction and interpretation of high-resolution electrospray mass spectra of large molecules. J. Am. Soc. Mass Spectrom. 2000, 11 (4), 320-332.
47. Mann, M.; Ong, S. E.; Gronborg, M.; Steen, H.; Jensen, O. N.; Pandey, A. Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol. 2002, 20 (6), 261-268.
48. Houle, F.; Poirier, A.; Dumaresq, J.; Huot, J. DAP kinase mediates the phosphorylation of tropomyosin-1 downstream of the ERK pathway, which regulates the formation of stress fibers in response to oxidative stress. J. Cell Sci. 2007, 120 (20), 3666-3677.
49. Mak, A.; Smillie, L. B.; Barany, M. Specific phosphorylation at serine-283 of alpha-tropomyosin from from skeletal and rabbit skeletal and cardiac-muscle. Proc. Natl. Acad. Sci. U.S.A. 1978, 75 (8), 3588-3592.
50. Leger, J.; Bouveret, P.; Schwartz, K.; Swynghedauw, B. Comparative-study of skeletal and cardiac tropomyosins-subunits, thiol-group content and biological-activities. Pflugers Arch. 1976, 362 (3), 271-277.
51. Muthuchamy, M.; Boivin, G. P.; Grupp, I. L.; Wieczorek, D. F. beta-tropomyosin overexpression induces severe cardiac abnormalities. J. Mol. Cell. Cardiol. 1998, 30 (8), 1545-1557.
52. Muthuchamy, M.; Grupp, I. L.; Grupp, G.; OToole, B. A.; Kier, A. B.; Boivin, G. P.; Neumann, J.; Wieczorek, D. F. Molecular and physiological effects of overexpressing striated muscle beta-tropomyosin in the adult murine heart. J. Biol. Chem. 1995, 270 (51), 30593-30603.
53. Urbancikova, M.; Hitchcockdegregori, S. E. Requirement of amino-terminal modification for striated muscle alpha-tropomyosin function. J. Biol. Chem. 1994, 269 (39), 24310-24315.
54. Singer, J. M.; Shaw, J. M. Mdm20 protein functions with Nat3 protein to acetylate Tpm1 protein and regulate tropomyosin-actininteractions in budding yeast. Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (13), 7644-7649.
55. Heeley, D. H.; Watson, M. H.; Mak, A. S.; Dubord, P.; Smillie, L. B. Effect of phosphorylation on the interaction and functional properties of rabbit striated muscle alpha alpha-tropomyosin. J. Biol. Chem. 1989, 264 (5), 2424-2430.
56. Vahebi, S.; Ota, A.; Li, M. X.; Warren, C. M.; de Tombe, P. P.; Wang, Y. B.; Solaro, R. J. p38-MAPK induced dephosphorylation of alpha-tropomyosin is associated with depression of myocardial sarcomeric tension and ATPase activity. Circ. Res. 2007, 100 (3), 408-415.
57. Pesavento, J. J.; Mizzen, C. A.; Kelleher, N. L. Quantitative analysis of modified proteins and their positional isomers by tandem mass spectrometry: Human histone H4. Anal. Chem. 2006, 78 (13), 4271-4280.
58. Wu, S.-L.; Huehmer, A. F. R.; Hao, Z.; Karger, B. L. On-line LCMS approach combining collision-induced dissociation (CID), electron-transfer dissociation (ETD), and CID of an isolated chargereduced species for the trace-level characterization of proteins with post-translational modifications. J. Proteome Res. 2007, 6 (11), 4230-4244.
59. Zhang, J. A.; Dong, X. T.; Hacker, T. A.; Ge, Y. Deciphering modifications in swine cardiac troponin I by top-down high-resolution tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 2010, 21 (6), 940-948.
60. Whitelegge, J. P.; Zabrouskov, V.; Halgand, F.; Souda, P.; Bassiliana, S.; Yan, W.; Wolinsky, L.; Loo, J. A.; Wong, D. T. W.; Faull, K. F. Protein-sequence polymorphisms and post-translational modifications in proteins from human saliva using top-down Fouriertransform ion cyclotron resonance mass spectrometry. Int. J. Mass Spectrom. 2007, 268 (2-3), 190-197.
61. Halgand, F.; Zabrouskov, V.; Bassilian, S.; Souda, P.; Loo, J. A.; Faull, K. F.; Wong, D. T.; Whitelegge, J. P. Defining intact protein primary structures from saliva: a step toward the human proteome project. Anal. Chem. 2012, 84 (10), 4383-4395.
62. Ryan, C. M.; Souda, P.; Halgand, F.; Wong, D. T.; Loo, J. A.; Faull, K. F.; Whitelegge, J. P. Confident assignment of intact mass tags to human salivary cystatins using top-down Fourier-transform ion cyclotron resonance mass spectrometry. J. Am. Soc. Mass Spectrom. 2010, 21 (6), 908-917.
63. Tran, J. C.; Zamdborg, L.; Ahlf, D. R.; Lee, J. E.; Catherman, A. D.; Durbin, K. R.; Tipton, J. D.; Vellaichamy, A.; Kellie, J. F.; Li, M.; Wu, C.; Sweet, S. M. M.; Early, B. P.; Siuti, N.; LeDuc, R. D.; Compton, P. D.; Thomas, P. M.; Kelleher, N. L. Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature 2011, 480 (7376), 254-258.
64. Kellie, J. F.; Tran, J. C.; Lee, J. E.; Ahlf, D. R.; Thomas, H. M.; Ntai, I.; Catherman, A. D.; Durbin, K. R.; Zamdborg, L.; Vellaichamy, A.; Thomas, P. M.; Kelleher, N. L. The emerging process of Top Down mass spectrometry for protein analysis: biomarkers, proteintherapeutics, and achieving high throughput. Mol. BioSyst. 2010, 6 (9), 1532-1539.