Advertisement

Mass Spectrometry Based Comparative Proteomics Using One Dimensional and Two Dimensional SDS-PAGE of Rat Atria Induced with Obstructive Sleep Apnea

  • Devika ChannaveerappaEmail author
  • Brian K. Panama
  • Costel C. DarieEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1140)

Abstract

Proteomics involves large-scale comprehensive study of specific proteomes which have been widely used in the field of biomarker discovery, drug development, disease diagnosis and therapy. Comprehensive proteomics involve two or more proteomics approaches that are confirmatory, complementary, and/or synergistic. Obstructive sleep apnea (OSA) is a sleep disorder which causes respiratory cessation (due to upper airway collapse). Here we describe a comprehensive MS based label-free quantitative proteomic analysis of the OSA induced rat atria homogenates and matched controls by using 1 dimensional SDS PAGE (1-D PAGE) and 2 dimensional SDS PAGE (2-D PAGE) separation of the proteins, enzymatic digestion and analysis by nanoliquid chromatography tandem-mass spectrometry (LC-MS/MS). The outcomes from the 1D-PAGE and 2D-PAGE studies not only identified dysregulated proteins due to OSA, but also confirmed and complemented each other.

Keywords

Obstructive sleep apnea (OSA) Rats Mass spectrometry Proteomics 

Abbreviations

1-D PAGE

1 dimensional SDS PAGE

2-D PAGE

2 dimensional SDS PAGE

ACN

Acetonitrile

AHI

Apnea-hypopnea index

BCA

Bicinchoninic acid

DTT

Dithiothreitol

ECG

Electrocardiogram

HSP

Heat shock protein

IAA

Iodoacetamide

IEF

Isoelectric focusing

LC-MS/MS

Liquid chromatography mass spectrometry

MS

Mass spectrometry

OSA

Obstructive sleep apnea

pI

Isoelectric points

PLGS

ProteinLynx Global Server

SDS-PAGE

Sodium dodecyl sulfate-polyacrylamide gel electrophoresis

Notes

Acknowledgments

The Authors thank Dr. Babu Suryadevara and Clarkson University’s Center for Advanced Materials Processing (CAMP) for the initial funding on the OSA project. We would also like to thanks Kendrick Laboratories, Inc. for the 2D-PAGE analysis.

References

  1. 1.
    Punjabi, N. M. (2008). The epidemiology of adult obstructive sleep apnea. Proceedings of the American Thoracic Society, 5(2), 136–143.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Channaveerappa, D., Lux, J. C., Wormwood, K. L., Heintz, T. A., McLerie, M., Treat, J. A., et al. (2017). Atrial electrophysiological and molecular remodelling induced by obstructive sleep apnoea. Journal of Cellular and Molecular Medicine, 21(9), 2223–2235.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Crossland, R. F., Durgan, D. J., Lloyd, E. E., Phillips, S. C., Reddy, A. K., Marrelli, S. P., et al. (2013). A new rodent model for obstructive sleep apnea: Effects on ATP-mediated dilations in cerebral arteries. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 305(4), R334–R342.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Lux, J. C., Channaveerappa, D., Aslebagh, R., McLerie, M., Panama, B. K., & Darie, C. C. (2019). Identification of dysregulation of atrial proteins in rats with chronic obstructive apnea using two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Journal of Cellular and Molecular Medicine, 23(4), 3016–3020.PubMedPubMedCentralGoogle Scholar
  5. 5.
    Young, T., Peppard, P. E., & Gottlieb, D. J. (2002). Epidemiology of obstructive sleep apnea: A population health perspective. American Journal of Respiratory and Critical Care Medicine, 165(9), 1217–1239.PubMedGoogle Scholar
  6. 6.
    Ho, M. L., & Brass, S. D. (2011). Obstructive sleep apnea. Neurology International, 3(3), e15.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Piccirillo, J. F., Duntley, S., & Schotland, H. (2000). Obstructive sleep apnea. JAMA, 284(12), 1492–1494.PubMedGoogle Scholar
  8. 8.
    Somers, V., & American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology. American Heart Association Stroke Council. American Heart Association Council on Cardiovascular Nursing. American College of Cardiology Foundation. (2008). Sleep apnea and cardiovascular disease: An American Heart Association/American College Of Cardiology Foundation Scientific Statement from the American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology, Stroke Council, and Council On Cardiovascular Nursing. In collaboration with the National Heart, Lung, and Blood Institute National Center on Sleep Disorders Research (National Institutes of Health). Circulation, 118, 1080–1111.PubMedGoogle Scholar
  9. 9.
    Sin, D. D., Fitzgerald, F., Parker, J. D., Newton, G., Floras, J. S., & Bradley, T. D. (1999). Risk factors for central and obstructive sleep apnea in 450 men and women with congestive heart failure. American Journal of Respiratory and Critical Care Medicine, 160(4), 1101–1106.PubMedGoogle Scholar
  10. 10.
    Young, T., Finn, L., Peppard, P. E., Szklo-Coxe, M., Austin, D., Nieto, F. J., et al. (2008). Sleep disordered breathing and mortality: Eighteen-year follow-up of the Wisconsin sleep cohort. Sleep, 31(8), 1071–1078.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Qureshi, A., Ballard, R. D., & Nelson, H. S. (2003). Obstructive sleep apnea. Journal of Allergy and Clinical Immunology, 112(4), 643–651.PubMedGoogle Scholar
  12. 12.
    Ramos, P., Rubies, C., Torres, M., Batlle, M., Farre, R., Brugada, J., et al. (2014). Atrial fibrosis in a chronic murine model of obstructive sleep apnea: Mechanisms and prevention by mesenchymal stem cells. Respiratory Research, 15(1), 54.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Hohl, M., Linz, B., Bohm, M., & Linz, D. (2014). Obstructive sleep apnea and atrial arrhythmogenesis. Current Cardiology Reviews, 10(4), 362–368.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Iwasaki, Y.-k., Kato, T., Xiong, F., Shi, Y.-F., Naud, P., Maguy, A., et al. (2014). Atrial fibrillation promotion with long-term repetitive obstructive sleep apnea in a rat model. Journal of the American College of Cardiology, 64(19), 2013–2023.PubMedGoogle Scholar
  15. 15.
    Ghias, M., Scherlag, B. J., Lu, Z., Niu, G., Moers, A., Jackman, W. M., et al. (2009). The role of ganglionated plexi in apnea-related atrial fibrillation. Journal of the American College of Cardiology, 54(22), 2075–2083.PubMedGoogle Scholar
  16. 16.
    Linz, D., Schotten, U., Neuberger, H.-R., Böhm, M., & Wirth, K. (2011). Negative tracheal pressure during obstructive respiratory events promotes atrial fibrillation by vagal activation. Heart Rhythm, 8(9), 1436–1443.PubMedGoogle Scholar
  17. 17.
    Carreras, A., Rojas, M., Tsapikouni, T., Montserrat, J. M., Navajas, D., & Farré, R. (2010). Obstructive apneas induce early activation of mesenchymal stem cells and enhancement of endothelial wound healing. Respiratory Research, 11(1), 91.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Carreras, A., Almendros, I., Montserrat, J. M., Navajas, D., & Farré, R. (2010). Mesenchymal stem cells reduce inflammation in a rat model of obstructive sleep apnea. Respiratory Physiology & Neurobiology, 172(3), 210–212.Google Scholar
  19. 19.
    Antzelevitch, C., & Burashnikov, A. (2011). Overview of basic mechanisms of cardiac arrhythmia. Cardiac Electrophysiology Clinics, 3(1), 23–45.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Fujita, M., Mitsuhashi, H., Isogai, S., Nakata, T., Kawakami, A., Nonaka, I., et al. (2012). Filamin C plays an essential role in the maintenance of the structural integrity of cardiac and skeletal muscles, revealed by the medaka mutant zacro. Developmental Biology, 361(1), 79–89.PubMedGoogle Scholar
  21. 21.
    Flix, B., de la Torre, C., Castillo, J., Casal, C., Illa, I., & Gallardo, E. (2013). Dysferlin interacts with calsequestrin-1, myomesin-2 and dynein in human skeletal muscle. The International Journal of Biochemistry & Cell Biology, 45(8), 1927–1938.Google Scholar
  22. 22.
    Capanni, C., Del Coco, R., Squarzoni, S., Columbaro, M., Mattioli, E., Camozzi, D., et al. (2008). Prelamin a is involved in early steps of muscle differentiation. Experimental Cell Research, 314(20), 3628–3637.PubMedGoogle Scholar
  23. 23.
    Araujo-Vilar, D., Lado-Abeal, J., Palos-Paz, F., Lattanzi, G., Bandin, M. A., Bellido, D., et al. (2008). A novel phenotypic expression associated with a new mutation in LMNA gene, characterized by partial lipodystrophy, insulin resistance, aortic stenosis and hypertrophic cardiomyopathy. Clinical Endocrinology, 69(1), 61–68.PubMedGoogle Scholar
  24. 24.
    Knoll, R., Hoshijima, M., Hoffman, H. M., Person, V., Lorenzen-Schmidt, I., Bang, M. L., et al. (2002). The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy. Cell, 111(7), 943–955.PubMedGoogle Scholar
  25. 25.
    Buyandelger, B., Ng, K. E., Miocic, S., Piotrowska, I., Gunkel, S., Ku, C. H., et al. (2011). MLP (muscle LIM protein) as a stress sensor in the heart. Pflügers Archiv, 462(1), 135–142.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Giordano, F. J. (2005). Oxygen, oxidative stress, hypoxia, and heart failure. The Journal of Clinical Investigation, 115(3), 500–508.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Opie, L. H. (2004). Heart physiology: From cell to circulation (4th ed.). Philadelphia: Lippincott Williams & Wilkens.Google Scholar
  28. 28.
    Doenst, T., Nguyen, T. D., & Abel, E. D. (2013). Cardiac metabolism in heart failure: Implications beyond ATP production. Circulation Research, 113(6), 709–724.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K., & Eppenberger, H. M. (1992). Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: The ‘phosphocreatine circuit’ for cellular energy homeostasis. The Biochemical Journal, 281(Pt 1), 21–40.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Brewster, L. M., Mairuhu, G., Bindraban, N. R., Koopmans, R. P., Clark, J. F., & van Montfrans, G. A. (2006). Creatine kinase activity is associated with blood pressure. Circulation, 114(19), 2034–2039.PubMedGoogle Scholar
  31. 31.
    Luo, Y., Pan, Y. Z., Zeng, C., Li, G. L., Lei, X. M., Liu, Z., et al. (2011). Altered serum creatine kinase level and cardiac function in ischemia-reperfusion injury during percutaneous coronary intervention. Medical Science Monitor, 17(9), CR474–CR479.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Lentini, S., Manka, R., Scholtyssek, S., Stoffel-Wagner, B., Luderitz, B., & Tasci, S. (2006). Creatine phosphokinase elevation in obstructive sleep apnea syndrome: An unknown association? Chest, 129(1), 88–94.PubMedGoogle Scholar
  33. 33.
    Cha, Y. M., Dzeja, P. P., Shen, W. K., Jahangir, A., Hart, C. Y., Terzic, A., et al. (2003). Failing atrial myocardium: Energetic deficits accompany structural remodeling and electrical instability. American Journal of Physiology. Heart and Circulatory Physiology, 284(4), H1313–H1320.PubMedGoogle Scholar
  34. 34.
    Smith, C. S., Bottomley, P. A., Schulman, S. P., Gerstenblith, G., & Weiss, R. G. (2006). Altered creatine kinase adenosine triphosphate kinetics in failing hypertrophied human myocardium. Circulation, 114(11), 1151–1158.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Petrash, J. M. (2004). All in the family: Aldose reductase and closely related aldo-keto reductases. Cellular and Molecular Life Sciences, 61(7–8), 737–749.PubMedGoogle Scholar
  36. 36.
    Tang, W. H., Kravtsov, G. M., Sauert, M., Tong, X. Y., Hou, X. Y., Wong, T. M., et al. (2010). Polyol pathway impairs the function of SERCA and RyR in ischemic-reperfused rat hearts by increasing oxidative modifications of these proteins. Journal of Molecular and Cellular Cardiology, 49(1), 58–69.PubMedGoogle Scholar
  37. 37.
    Ananthakrishnan, R., Li, Q., Gomes, T., Schmidt, A. M., & Ramasamy, R. (2011). Aldose reductase pathway contributes to vulnerability of aging myocardium to ischemic injury. Experimental Gerontology, 46(9), 762–767.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Son, N. H., Ananthakrishnan, R., Yu, S., Khan, R. S., Jiang, H., Ji, R., et al. (2012). Cardiomyocyte aldose reductase causes heart failure and impairs recovery from ischemia. PLoS One, 7(9), e46549.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Fillmore, N., Mori, J., & Lopaschuk, G. D. (2014). Mitochondrial fatty acid oxidation alterations in heart failure, ischaemic heart disease and diabetic cardiomyopathy. British Journal of Pharmacology, 171(8), 2080–2090.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Frey, N., & Olson, E. N. (2002). Modulating cardiac hypertrophy by manipulating myocardial lipid metabolism? Circulation, 105(10), 1152–1154.PubMedGoogle Scholar
  41. 41.
    Hopps, E., & Caimi, G. (2015). Obstructive sleep apnea syndrome: Links between pathophysiology and cardiovascular complications. Clinical and Investigative Medicine, 38(6), E362–E370.PubMedGoogle Scholar
  42. 42.
    Somers, V. K., White, D. P., Amin, R., Abraham, W. T., Costa, F., Culebras, A., et al. (2008). Sleep apnea and cardiovascular disease: An American Heart Association/American College of Cardiology Foundation Scientific Statement from the American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology, Stroke Council, and Council on Cardiovascular Nursing in Collaboration with the National Heart, Lung, and Blood Institute National Center on Sleep Disorders Research (National Institutes of Health). Circulation, 118(10), 1080–1111.PubMedGoogle Scholar
  43. 43.
    Taegtmeyer, H., & Overturf, M. L. (1988). Effects of moderate hypertension on cardiac function and metabolism in the rabbit. Hypertension, 11(5), 416–426.PubMedGoogle Scholar
  44. 44.
    Kohno, H., Takahashi, N., Shinohara, T., Ooie, T., Yufu, K., Nakagawa, M., et al. (2007). Receptor-mediated suppression of cardiac heat-shock protein 72 expression by testosterone in male rat heart. Endocrinology, 148(7), 3148–3155.PubMedGoogle Scholar
  45. 45.
    Latchman, D. S. (2001). Heat shock proteins and cardiac protection. Cardiovascular Research, 51(4), 637–646.PubMedGoogle Scholar
  46. 46.
    Torigoe, Y., Takahashi, N., Hara, M., Yoshimatsu, H., & Saikawa, T. (2009). Adrenomedullin improves cardiac expression of heat-shock protein 72 and tolerance against ischemia/reperfusion injury in insulin-resistant rats. Endocrinology, 150(3), 1450–1455.PubMedGoogle Scholar
  47. 47.
    Cao, H., Xue, L., Xu, X., Wu, Y., Zhu, J., Chen, L., et al. (2011). Heat shock proteins in stabilization of spontaneously restored sinus rhythm in permanent atrial fibrillation patients after mitral valve surgery. Cell Stress & Chaperones, 16(5), 517–528.Google Scholar
  48. 48.
    Wakisaka, O., Takahashi, N., Shinohara, T., Ooie, T., Nakagawa, M., Yonemochi, H., et al. (2007). Hyperthermia treatment prevents angiotensin II-mediated atrial fibrosis and fibrillation via induction of heat-shock protein 72. Journal of Molecular and Cellular Cardiology, 43(5), 616–626.PubMedGoogle Scholar
  49. 49.
    Hayashi, M., Fujimoto, K., Urushibata, K., Takamizawa, A., Kinoshita, O., & Kubo, K. (2006). Hypoxia-sensitive molecules may modulate the development of atherosclerosis in sleep apnoea syndrome. Respirology, 11(1), 24–31.PubMedGoogle Scholar
  50. 50.
    Noguchi, T., Chin, K., Ohi, M., Kita, H., Otsuka, N., Tsuboi, T., et al. (1997). Heat shock protein 72 level decreases during sleep in patients with obstructive sleep apnea syndrome. American Journal of Respiratory and Critical Care Medicine, 155(4), 1316–1322.PubMedGoogle Scholar
  51. 51.
    Flink, I. L., Rader, J. H., Banerjee, S. K., & Morkin, E. (1978). Atrial and ventricular cardiac myosins contain different heavy chain species. FEBS Letters, 94(1), 125–130.PubMedGoogle Scholar
  52. 52.
    Reiser, P. J., & Moravec, C. S. (2014). Sex differences in myosin heavy chain isoforms of human failing and nonfailing atria. American Journal of Physiology. Heart and Circulatory Physiology, 307(3), H265–H272.PubMedGoogle Scholar
  53. 53.
    Hydock, D. S., Wonders, K. Y., Schneider, C. M., & Hayward, R. (2009). Voluntary wheel running in rats receiving doxorubicin: Effects on running activity and cardiac myosin heavy chain. Anticancer Research, 29(11), 4401–4407.PubMedGoogle Scholar
  54. 54.
    Miyata, S., Minobe, W., Bristow, M. R., & Leinwand, L. A. (2000). Myosin heavy chain isoform expression in the failing and nonfailing human heart. Circulation Research, 86(4), 386–390.PubMedGoogle Scholar
  55. 55.
    Nakao, K., Minobe, W., Roden, R., Bristow, M. R., & Leinwand, L. A. (1997). Myosin heavy chain gene expression in human heart failure. The Journal of Clinical Investigation, 100(9), 2362–2370.PubMedPubMedCentralGoogle Scholar
  56. 56.
    Balsa, E., Marco, R., Perales-Clemente, E., Szklarczyk, R., Calvo, E., Landazuri, M. O., et al. (2012). NDUFA4 is a subunit of complex IV of the mammalian electron transport chain. Cell Metabolism, 16(3), 378–386.PubMedGoogle Scholar
  57. 57.
    Yoshikawa, S., & Shimada, A. (2015). Reaction mechanism of cytochrome c oxidase. Chemical Reviews, 115(4), 1936–1989.PubMedGoogle Scholar
  58. 58.
    Sharov, V. G., Todor, A. V., Imai, M., & Sabbah, H. N. (2005). Inhibition of mitochondrial permeability transition pores by cyclosporine A improves cytochrome C oxidase function and increases rate of ATP synthesis in failing cardiomyocytes. Heart Failure Reviews, 10(4), 305–310.PubMedGoogle Scholar
  59. 59.
    Wu, C., Yan, L., Depre, C., Dhar, S. K., Shen, Y. T., Sadoshima, J., et al. (2009). Cytochrome c oxidase III as a mechanism for apoptosis in heart failure following myocardial infarction. American Journal of Physiology. Cell Physiology, 297(4), C928–C934.PubMedPubMedCentralGoogle Scholar
  60. 60.
    Kadenbach, B., Ramzan, R., & Vogt, S. (2009). Degenerative diseases, oxidative stress and cytochrome c oxidase function. Trends in Molecular Medicine, 15(4), 139–147.PubMedGoogle Scholar
  61. 61.
    Cox, A. G., Peskin, A. V., Paton, L. N., Winterbourn, C. C., & Hampton, M. B. (2009). Redox potential and peroxide reactivity of human peroxiredoxin 3. Biochemistry, 48(27), 6495–6501.PubMedGoogle Scholar
  62. 62.
    Kumar, V., Kitaeff, N., Hampton, M. B., Cannell, M. B., & Winterbourn, C. C. (2009). Reversible oxidation of mitochondrial peroxiredoxin 3 in mouse heart subjected to ischemia and reperfusion. FEBS Letters, 583(6), 997–1000.PubMedGoogle Scholar
  63. 63.
    Park, A. M., & Suzuki, Y. J. (2007). Effects of intermittent hypoxia on oxidative stress-induced myocardial damage in mice. Journal of Applied Physiology (Bethesda, MD: 1985), 102(5), 1806–1814.Google Scholar
  64. 64.
    Guo, Q., Wang, Y., Li, Q. Y., Li, M., & Wan, H. Y. (2013). Levels of thioredoxin are related to the severity of obstructive sleep apnea: Based on oxidative stress concept. Sleep & Breathing, 17(1), 311–316.Google Scholar
  65. 65.
    Zhao, W., Fan, G. C., Zhang, Z. G., Bandyopadhyay, A., Zhou, X., & Kranias, E. G. (2009). Protection of peroxiredoxin II on oxidative stress-induced cardiomyocyte death and apoptosis. Basic Research in Cardiology, 104(4), 377–389.PubMedGoogle Scholar
  66. 66.
    Park, J. G., Yoo, J. Y., Jeong, S. J., Choi, J. H., Lee, M. R., Lee, M. N., et al. (2011). Peroxiredoxin 2 deficiency exacerbates atherosclerosis in apolipoprotein E-deficient mice. Circulation Research, 109(7), 739–749.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Brandolin, G., Dupont, Y., & Vignais, P. V. (1985). Substrate-induced modifications of the intrinsic fluorescence of the isolated adenine nucleotide carrier protein: Demonstration of distinct conformational states. Biochemistry, 24(8), 1991–1997.PubMedGoogle Scholar
  68. 68.
    Dorner, A., Giessen, S., Gaub, R., Grosse Siestrup, H., Schwimmbeck, P. L., Hetzer, R., et al. (2006). An isoform shift in the cardiac adenine nucleotide translocase expression alters the kinetic properties of the carrier in dilated cardiomyopathy. European Journal of Heart Failure, 8(1), 81–89.PubMedGoogle Scholar
  69. 69.
    Dorner, A., & Schultheiss, H. P. (2007). Adenine nucleotide translocase in the focus of cardiovascular diseases. Trends in Cardiovascular Medicine, 17(8), 284–290.PubMedGoogle Scholar
  70. 70.
    Heger, J., Abdallah, Y., Shahzad, T., Klumpe, I., Piper, H. M., Schultheiss, H. P., et al. (2012). Transgenic overexpression of the adenine nucleotide translocase 1 protects cardiomyocytes against TGFbeta1-induced apoptosis by stabilization of the mitochondrial permeability transition pore. Journal of Molecular and Cellular Cardiology, 53(1), 73–81.PubMedGoogle Scholar
  71. 71.
    Giron-Calle, J., Zwizinski, C. W., & Schmid, H. H. (1994). Peroxidative damage to cardiac mitochondria. II. Immunological analysis of modified adenine nucleotide translocase. Archives of Biochemistry and Biophysics, 315(1), 1–7.PubMedGoogle Scholar
  72. 72.
    Wiegand, G., & Remington, S. J. (1986). Citrate synthase: Structure, control, and mechanism. Annual Review of Biophysics and Biophysical Chemistry, 15, 97–117.PubMedGoogle Scholar
  73. 73.
    Lei, B., Lionetti, V., Young, M. E., Chandler, M. P., d’Agostino, C., Kang, E., et al. (2004). Paradoxical downregulation of the glucose oxidation pathway despite enhanced flux in severe heart failure. Journal of Molecular and Cellular Cardiology, 36(4), 567–576.PubMedGoogle Scholar
  74. 74.
    Garnier, A., Fortin, D., Delomenie, C., Momken, I., Veksler, V., & Ventura-Clapier, R. (2003). Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. The Journal of Physiology, 551(Pt 2), 491–501.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Emelyanova, L., Ashary, Z., Cosic, M., Negmadjanov, U., Ross, G., Rizvi, F., et al. (2016). Selective downregulation of mitochondrial electron transport chain activity and increased oxidative stress in human atrial fibrillation. American Journal of Physiology. Heart and Circulatory Physiology, 311(1), H54–H63.PubMedPubMedCentralGoogle Scholar
  76. 76.
    Montaigne, D., Marechal, X., Lefebvre, P., Modine, T., Fayad, G., Dehondt, H., et al. (2013). Mitochondrial dysfunction as an arrhythmogenic substrate: A translational proof-of-concept study in patients with metabolic syndrome in whom post-operative atrial fibrillation develops. Journal of the American College of Cardiology, 62(16), 1466–1473.PubMedGoogle Scholar
  77. 77.
    Popp, R. L. (2013). Troponin: Messenger or actor? Journal of the American College of Cardiology, 61(6), 611–614.PubMedGoogle Scholar
  78. 78.
    Katus, H. A. (2008). Development of the cardiac troponin T immunoassay. Clinical Chemistry, 54(9), 1576–1577; discussion 1577.PubMedGoogle Scholar
  79. 79.
    Conti, A., Mariannini, Y., Canuti, E., Cerini, G., De Bernardis, N., Gigli, C., et al. (2015). Role of masked coronary heart disease in patients with recent-onset atrial fibrillation and troponin elevations. European Journal of Emergency Medicine, 22(3), 162–169.PubMedGoogle Scholar
  80. 80.
    Conti, A., Angeli, E., Scorpiniti, M., Alesi, A., Trausi, F., Lazzeretti, D., et al. (2015). Coronary atherosclerosis and adverse outcomes in patients with recent-onset atrial fibrillation and troponin rise. The American Journal of Emergency Medicine, 33(10), 1407–1413.PubMedGoogle Scholar
  81. 81.
    Parwani, A. S., & Boldt, L. H. (2014). Atrial fibrillation-induced cardiac troponin I release. International Journal of Cardiology, 172(1), 220.PubMedGoogle Scholar
  82. 82.
    Einvik, G., Rosjo, H., Randby, A., Namtvedt, S. K., Hrubos-Strom, H., Brynildsen, J., et al. (2014). Severity of obstructive sleep apnea is associated with cardiac troponin I concentrations in a community-based sample: Data from the Akershus Sleep Apnea Project. Sleep, 37(6), 1111–1116, 1116A–1116B.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Connelly, A., Findlay, I. N., & Coats, C. J. (2016). Measurement of troponin in cardiomyopathies. Cardiogenetics, 6(1).Google Scholar
  84. 84.
    Barcelo, A., Esquinas, C., Bauca, J. M., Pierola, J., de la Pena, M., Arque, M., et al. (2014). Effect of CPAP treatment on plasma high sensitivity troponin levels in patients with obstructive sleep apnea. Respiratory Medicine, 108(7), 1060–1063.PubMedGoogle Scholar
  85. 85.
    Pietkiewicz, S., Schmidt, J. H., & Lavrik, I. N. (2015). Quantification of apoptosis and necroptosis at the single cell level by a combination of Imaging Flow Cytometry with classical Annexin V/propidium iodide staining. Journal of Immunological Methods, 423, 99–103.PubMedGoogle Scholar
  86. 86.
    Benevolensky, D., Belikova, Y., Mohammadzadeh, R., Trouve, P., Marotte, F., Russo-Marie, F., et al. (2000). Expression and localization of the annexins II, V, and VI in myocardium from patients with end-stage heart failure. Laboratory Investigation, 80(2), 123–133.PubMedGoogle Scholar
  87. 87.
    Wakabayashi, H., Taki, J., Inaki, A., Shiba, K., Matsunari, I., & Kinuya, S. (2015). Correlation between apoptosis and left ventricular remodeling in subacute phase of myocardial ischemia and reperfusion. EJNMMI Research, 5(1), 72.PubMedPubMedCentralGoogle Scholar
  88. 88.
    Sinning, J. M., Losch, J., Walenta, K., Bohm, M., Nickenig, G., & Werner, N. (2011). Circulating CD31+/Annexin V+ microparticles correlate with cardiovascular outcomes. European Heart Journal, 32(16), 2034–2041.PubMedGoogle Scholar
  89. 89.
    Yun, C. H., Jung, K. H., Chu, K., Kim, S. H., Ji, K. H., Park, H. K., et al. (2010). Increased circulating endothelial microparticles and carotid atherosclerosis in obstructive sleep apnea. Journal of Clinical Neurology, 6(2), 89–98.PubMedGoogle Scholar
  90. 90.
    Jia, L., Fan, J., Cui, W., Liu, S., Li, N., Lau, W. B., et al. (2017). Endothelial cell-derived microparticles from patients with obstructive sleep apnea hypoxia syndrome and coronary artery disease increase aortic endothelial cell dysfunction. Cellular Physiology and Biochemistry, 43(6), 2562–2570.PubMedGoogle Scholar
  91. 91.
    Bikov, A., Kunos, L., Pallinger, E., Lazar, Z., Kis, A., Horvath, G., et al. (2017). Diurnal variation of circulating microvesicles is associated with the severity of obstructive sleep apnoea. Sleep & Breathing, 21(3), 595–600.Google Scholar
  92. 92.
    Doubell, A. F., Bester, A. J., & Thibault, G. (1991). Annexins V and VI: Major calcium-dependent atrial secretory granule-binding proteins. Hypertension, 18(5), 648–656.PubMedGoogle Scholar
  93. 93.
    Wang, L., Rahman, M. M., Iida, H., Inai, T., Kawabata, S., Iwanaga, S., et al. (1995). Annexin V is localized in association with Z-line of rat cardiac myocytes. Cardiovascular Research, 30(3), 363–371.PubMedGoogle Scholar
  94. 94.
    Ueng, K. C., Lin, C. S., Yeh, H. I., Wu, Y. L., Liu, R. H., Tsai, C. F., et al. (2008). Downregulated cardiac annexin VI mRNA and protein levels in chronically fibrillating human atria. Cardiology, 109(3), 208–216.PubMedGoogle Scholar
  95. 95.
    Jiao, Q., Bai, Y., Akaike, T., Takeshima, H., Ishikawa, Y., & Minamisawa, S. (2009). Sarcalumenin is essential for maintaining cardiac function during endurance exercise training. American Journal of Physiology. Heart and Circulatory Physiology, 297(2), H576–H582.PubMedPubMedCentralGoogle Scholar
  96. 96.
    Leberer, E., Charuk, J. H., Green, N. M., & MacLennan, D. H. (1989). Molecular cloning and expression of cDNA encoding a lumenal calcium binding glycoprotein from sarcoplasmic reticulum. Proceedings of the National Academy of Sciences of the United States of America, 86(16), 6047–6051.PubMedPubMedCentralGoogle Scholar
  97. 97.
    Minamisawa, S., Uemura, N., Sato, Y., Yokoyama, U., Yamaguchi, T., Inoue, K., et al. (2006). Post-transcriptional downregulation of sarcolipin mRNA by triiodothyronine in the atrial myocardium. FEBS Letters, 580(9), 2247–2252.PubMedGoogle Scholar
  98. 98.
    Zhang, H., Cannell, M. B., Kim, S. J., Watson, J. J., Norman, R., Calaghan, S. C., et al. (2015). Cellular hypertrophy and increased susceptibility to spontaneous calcium-release of rat left atrial myocytes due to elevated afterload. PLoS One, 10(12), e0144309.PubMedPubMedCentralGoogle Scholar
  99. 99.
    Junge, W., & Nelson, N. (2015). ATP synthase. Annual Review of Biochemistry, 84, 631–657.PubMedGoogle Scholar
  100. 100.
    Chen, G., Guo, H., Song, Y., Chang, H., Wang, S., Zhang, M., et al. (2016). Long noncoding RNA AK055347 is upregulated in patients with atrial fibrillation and regulates mitochondrial energy production in myocardiocytes. Molecular Medicine Reports, 14(6), 5311–5317.PubMedGoogle Scholar
  101. 101.
    Li, Z., Wang, X., Wang, W., Du, J., Wei, J., Zhang, Y., et al. (2017). Altered long non-coding RNA expression profile in rabbit atria with atrial fibrillation: TCONS_00075467 modulates atrial electrical remodeling by sponging miR-328 to regulate CACNA1C. Journal of Molecular and Cellular Cardiology, 108, 73–85.PubMedGoogle Scholar
  102. 102.
    Mio, Y., Bienengraeber, M. W., Marinovic, J., Gutterman, D. D., Rakic, M., Bosnjak, Z. J., et al. (2008). Age-related attenuation of isoflurane preconditioning in human atrial cardiomyocytes: Roles for mitochondrial respiration and sarcolemmal adenosine triphosphate-sensitive potassium channel activity. Anesthesiology, 108(4), 612–620.PubMedPubMedCentralGoogle Scholar
  103. 103.
    Ferko, M., Kancirova, I., Jasova, M., Carnicka, S., Murarikova, M., Waczulikova, I., et al. (2014). Remote ischemic preconditioning of the heart: Protective responses in functional and biophysical properties of cardiac mitochondria. Physiological Research, 63(Suppl 4), S469–S478.PubMedGoogle Scholar
  104. 104.
    Dybkova, N., Wagner, S., Backs, J., Hund, T. J., Mohler, P. J., Sowa, T., et al. (2014). Tubulin polymerization disrupts cardiac beta-adrenergic regulation of late INa. Cardiovascular Research, 103(1), 168–177.PubMedPubMedCentralGoogle Scholar
  105. 105.
    Benson, D. W., Wang, D. W., Dyment, M., Knilans, T. K., Fish, F. A., Strieper, M. J., et al. (2003). Congenital sick sinus syndrome caused by recessive mutations in the cardiac sodium channel gene (SCN5A). Journal of Clinical Investigation, 112(7), 1019–1028.PubMedPubMedCentralGoogle Scholar
  106. 106.
    Aquila-Pastir, L. A., DiPaola, N. R., Matteo, R. G., Smedira, N. G., McCarthy, P. M., & Moravec, C. S. (2002). Quantitation and distribution of beta-tubulin in human cardiac myocytes. Journal of Molecular and Cellular Cardiology, 34(11), 1513–1523.PubMedGoogle Scholar
  107. 107.
    Narishige, T., Blade, K. L., Ishibashi, Y., Nagai, T., Hamawaki, M., Menick, D. R., et al. (1999). Cardiac hypertrophic and developmental regulation of the beta-tubulin multigene family. The Journal of Biological Chemistry, 274(14), 9692–9697.PubMedGoogle Scholar
  108. 108.
    Gonzalez-Granillo, M., Grichine, A., Guzun, R., Usson, Y., Tepp, K., Chekulayev, V., et al. (2012). Studies of the role of tubulin beta II isotype in regulation of mitochondrial respiration in intracellular energetic units in cardiac cells. Journal of Molecular and Cellular Cardiology, 52(2), 437–447.PubMedGoogle Scholar
  109. 109.
    Bagur, R., Tanguy, S., Foriel, S., Grichine, A., Sanchez, C., Pernet-Gallay, K., et al. (2016). The impact of cardiac ischemia/reperfusion on the mitochondria-cytoskeleton interactions. Biochimica et Biophysica Acta, 1862(6), 1159–1171.PubMedGoogle Scholar
  110. 110.
    Kuznetsov, A. V., Javadov, S., Guzun, R., Grimm, M., & Saks, V. (2013). Cytoskeleton and regulation of mitochondrial function: The role of beta-tubulin II. Frontiers in Physiology, 4, 82.PubMedPubMedCentralGoogle Scholar
  111. 111.
    Fu, Q., Kim, S., Soto, D., De Arcangelis, V., DiPilato, L., Liu, S., et al. (2014). A long lasting beta1 adrenergic receptor stimulation of cAMP/protein kinase A (PKA) signal in cardiac myocytes. The Journal of Biological Chemistry, 289(21), 14771–14781.PubMedPubMedCentralGoogle Scholar
  112. 112.
    Cserne Szappanos, H., Muralidharan, P., Ingley, E., Petereit, J., Millar, H. A., & Hool, L. C. (2017). Identification of a novel cAMP dependent protein kinase a phosphorylation site on the human cardiac calcium channel. Scientific Reports, 7(1), 15118.PubMedPubMedCentralGoogle Scholar
  113. 113.
    Bobin, P., Varin, A., Lefebvre, F., Fischmeister, R., Vandecasteele, G., & Leroy, J. (2016). Calmodulin kinase II inhibition limits the pro-arrhythmic Ca2+ waves induced by cAMP-phosphodiesterase inhibitors. Cardiovascular Research, 110(1), 151–161.PubMedGoogle Scholar
  114. 114.
    Dhalla, N. S., & Muller, A. L. (2010). Protein kinases as drug development targets for heart disease therapy. Pharmaceuticals (Basel), 3(7), 2111–2145.Google Scholar
  115. 115.
    Wang, P. Y., Yu, J., Lin, J. H., & Tsai, W. B. (2011). Modulation of alignment, elongation and contraction of cardiomyocytes through a combination of nanotopography and rigidity of substrates. Acta Biomaterialia, 7(9), 3285–3293.PubMedGoogle Scholar
  116. 116.
    Goldmann, W. H., & Ingber, D. E. (2002). Intact vinculin protein is required for control of cell shape, cell mechanics, and rac-dependent lamellipodia formation. Biochemical and Biophysical Research Communications, 290(2), 749–755.PubMedGoogle Scholar
  117. 117.
    DeLeon-Pennell, K. Y., & Lindsey, M. L. (2015). Cardiac aging: Send in the vinculin reinforcements. Science Translational Medicine, 7(292), 292fs26.PubMedGoogle Scholar
  118. 118.
    Chinthalapudi, K., Rangarajan, E. S., Brown, D. T., & Izard, T. (2016). Differential lipid binding of vinculin isoforms promotes quasi-equivalent dimerization. Proceedings of the National Academy of Sciences of the United States of America, 113(34), 9539–9544.PubMedPubMedCentralGoogle Scholar
  119. 119.
    Zemljic-Harpf, A. E., Miller, J. C., Henderson, S. A., Wright, A. T., Manso, A. M., Elsherif, L., et al. (2007). Cardiac-myocyte-specific excision of the vinculin gene disrupts cellular junctions, causing sudden death or dilated cardiomyopathy. Molecular and Cellular Biology, 27(21), 7522–7537.PubMedPubMedCentralGoogle Scholar
  120. 120.
    Sun, J., Zhang, D., Zheng, Y., Zhao, Q., Zheng, M., Kovacevic, Z., et al. (2013). Targeting the metastasis suppressor, NDRG1, using novel iron chelators: Regulation of stress fiber-mediated tumor cell migration via modulation of the ROCK1/pMLC2 signaling pathway. Molecular Pharmacology, 83(2), 454–469.PubMedGoogle Scholar
  121. 121.
    Fang, B. A., Kovacevic, Z., Park, K. C., Kalinowski, D. S., Jansson, P. J., Lane, D. J., et al. (2014). Molecular functions of the iron-regulated metastasis suppressor, NDRG1, and its potential as a molecular target for cancer therapy. Biochimica et Biophysica Acta, 1845(1), 1–19.PubMedGoogle Scholar
  122. 122.
    Stein, S., Thomas, E. K., Herzog, B., Westfall, M. D., Rocheleau, J. V., Jackson 2nd, R. S., et al. (2004). NDRG1 is necessary for p53-dependent apoptosis. The Journal of Biological Chemistry, 279(47), 48930–48940.PubMedGoogle Scholar
  123. 123.
    Choi, S. J., Oh, S. Y., Kim, J. H., Sadovsky, Y., & Roh, C. R. (2007). Increased expression of N-myc downstream-regulated gene 1 (NDRG1) in placentas from pregnancies complicated by intrauterine growth restriction or preeclampsia. American Journal of Obstetrics and Gynecology, 196(1), 45 e1–45 e7.Google Scholar
  124. 124.
    Cangul, H. (2004). Hypoxia upregulates the expression of the NDRG1 gene leading to its overexpression in various human cancers. BMC Genetics, 5, 27.PubMedPubMedCentralGoogle Scholar
  125. 125.
    Hartwig, J. H., Thelen, M., Rosen, A., Janmey, P. A., Nairn, A. C., & Aderem, A. (1992). MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature, 356(6370), 618–622.PubMedGoogle Scholar
  126. 126.
    Prieto, D., & Zolessi, F. R. (2017). Functional diversification of the four MARCKS family members in zebrafish neural development. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 328(1–2), 119–138.PubMedGoogle Scholar
  127. 127.
    Stevens, F. C. (1983). Calmodulin: An introduction. Canadian Journal of Biochemistry and Cell Biology, 61(8), 906–910.PubMedGoogle Scholar
  128. 128.
    Heidkamp, M. C., Iyengar, R., Szotek, E. L., Cribbs, L. L., & Samarel, A. M. (2007). Protein kinase Cepsilon-dependent MARCKS phosphorylation in neonatal and adult rat ventricular myocytes. Journal of Molecular and Cellular Cardiology, 42(2), 422–431.PubMedGoogle Scholar
  129. 129.
    McGill, C. J., & Brooks, G. (1997). Expression and regulation of 80K/MARCKS, a major substrate of protein kinase C, in the developing rat heart. Cardiovascular Research, 34(2), 368–376.PubMedGoogle Scholar
  130. 130.
    Li, G. H., Arora, P. D., Chen, Y., McCulloch, C. A., & Liu, P. (2012). Multifunctional roles of gelsolin in health and diseases. Medicinal Research Reviews, 32(5), 999–1025.PubMedGoogle Scholar
  131. 131.
    Hu, W. S., Ho, T. J., Pai, P., Chung, L. C., Kuo, C. H., Chang, S. H., et al. (2014). Gelsolin (GSN) induces cardiomyocyte hypertrophy and BNP expression via p38 signaling and GATA-4 transcriptional factor activation. Molecular and Cellular Biochemistry, 390(1–2), 263–270.PubMedGoogle Scholar
  132. 132.
    Li, G. H., Shi, Y., Chen, Y., Sun, M., Sader, S., Maekawa, Y., et al. (2009). Gelsolin regulates cardiac remodeling after myocardial infarction through DNase I-mediated apoptosis. Circulation Research, 104(7), 896–904.PubMedGoogle Scholar
  133. 133.
    Schrickel, J. W., Fink, K., Meyer, R., Grohe, C., Stoeckigt, F., Tiemann, K., et al. (2009). Lack of gelsolin promotes perpetuation of atrial fibrillation in the mouse heart. Journal of Interventional Cardiac Electrophysiology, 26(1), 3–10.PubMedGoogle Scholar
  134. 134.
    Lader, A. S., Kwiatkowski, D. J., & Cantiello, H. F. (1999). Role of gelsolin in the actin filament regulation of cardiac L-type calcium channels. The American Journal of Physiology, 277(6 Pt 1), C1277–C1283.PubMedGoogle Scholar
  135. 135.
    Pinti, M., Gibellini, L., Liu, Y., Xu, S., Lu, B., & Cossarizza, A. (2015). Mitochondrial Lon protease at the crossroads of oxidative stress, ageing and cancer. Cellular and Molecular Life Sciences, 72(24), 4807–4824.PubMedGoogle Scholar
  136. 136.
    Bota, D. A., Ngo, J. K., & Davies, K. J. (2005). Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radical Biology & Medicine, 38(5), 665–677.Google Scholar
  137. 137.
    Ngo, J. K., Pomatto, L. C., & Davies, K. J. (2013). Upregulation of the mitochondrial Lon protease allows adaptation to acute oxidative stress but dysregulation is associated with chronic stress, disease, and aging. Redox Biology, 1, 258–264.PubMedPubMedCentralGoogle Scholar
  138. 138.
    Hoshino, A., Okawa, Y., Ariyoshi, M., Kaimoto, S., Uchihashi, M., Fukai, K., et al. (2014). Oxidative post-translational modifications develop LONP1 dysfunction in pressure overload heart failure. Circulation. Heart Failure, 7(3), 500–509.PubMedGoogle Scholar
  139. 139.
    Deshaies, R. J., & Joazeiro, C. A. (2009). RING domain E3 ubiquitin ligases. Annual Review of Biochemistry, 78, 399–434.Google Scholar
  140. 140.
    Parry, T. L., & Willis, M. S. (2016). Cardiac ubiquitin ligases: Their role in cardiac metabolism, autophagy, cardioprotection and therapeutic potential. Biochimica et Biophysica Acta, 1862(12), 2259–2269.PubMedPubMedCentralGoogle Scholar
  141. 141.
    Willis, M. S., Bevilacqua, A., Pulinilkunnil, T., Kienesberger, P., Tannu, M., & Patterson, C. (2014). The role of ubiquitin ligases in cardiac disease. Journal of Molecular and Cellular Cardiology, 71, 43–53.PubMedGoogle Scholar
  142. 142.
    Weber, K., & Osborn, M. (1969). The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. Journal of Biological Chemistry, 244(16), 4406–4412.PubMedGoogle Scholar
  143. 143.
    Dunbar, B. S. (2012). Two-dimensional electrophoresis and immunological techniques. New York: Springer Science & Business Media.Google Scholar
  144. 144.
    Schirle, M., Heurtier, M.-A., & Kuster, B. (2003). Profiling core proteomes of human cell lines by one-dimensional PAGE and liquid chromatography-tandem mass spectrometry. Molecular & Cellular Proteomics, 2(12), 1297–1305.Google Scholar
  145. 145.
    Andersen, J. S., & Mann, M. (2006). Organellar proteomics: Turning inventories into insights. EMBO Reports, 7(9), 874–879.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Biochemistry and Proteomics Group, Department of Chemistry and Biomolecular SciencePotsdamUSA
  2. 2.Department of Physiology and Biophysics, Jacobs School of Medicine and Biomedical SciencesSUNY BuffaloBuffaloUSA

Personalised recommendations