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Disease Markers
Volume 2016 (2016), Article ID 3695454, 11 pages
http://dx.doi.org/10.1155/2016/3695454
Research Article

Detection of Soluble ED-A+ Fibronectin and Evaluation as Novel Serum Biomarker for Cardiac Tissue Remodeling

1Jena University Hospital, Department of Internal Medicine I, 07747 Jena, Germany
2Swiss Federal Institute of Technology, Department of Chemistry and Applied Biosciences, 8093 Zurich, Switzerland
3Jena University Hospital, Department of Internal Medicine III, 07747 Jena, Germany
4Medical Faculty, Division of Cardiology, Pulmonology, and Vascular Medicine, University of Duesseldorf, 40225 Duesseldorf, Germany
5Jena University Hospital, Institute of Pathology, 07743 Jena, Germany

Received 9 April 2016; Accepted 10 July 2016

Academic Editor: Dennis W. T. Nilsen

Copyright © 2016 Barbara Ziffels et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Global Burden of Disease Study 2013 Collaborators, “Global, regional, and national incidence, prevalence, and years lived with disability for 301 acute and chronic diseases and injuries in 188 countries, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013,” The Lancet, vol. 386, no. 9995, pp. 743–800, 2013. View at Publisher · View at Google Scholar
  2. A. González, S. Ravassa, J. Beaumont, B. López, and J. Díez, “New targets to treat the structural remodeling of the myocardium,” Journal of the American College of Cardiology, vol. 58, no. 18, pp. 1833–1843, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Tarone, J.-L. Balligand, J. Bauersachs et al., “Targeting myocardial remodelling to develop novel therapies for heart failure: a position paper from the Working Group on Myocardial Function of the European Society of Cardiology,” European Journal of Heart Failure, vol. 16, no. 5, pp. 494–508, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. A. K. Schroer and W. D. Merryman, “Mechanobiology of myofibroblast adhesion in fibrotic cardiac disease,” Journal of Cell Science, vol. 128, no. 10, pp. 1865–1875, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. S. L. K. Bowers, I. Banerjee, and T. A. Baudino, “The extracellular matrix: at the center of it all,” Journal of Molecular and Cellular Cardiology, vol. 48, no. 3, pp. 474–482, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. B. R. Freedman, N. D. Bade, C. N. Riggin et al., “The (dys)functional extracellular matrix,” Biochimica et Biophysica Acta (BBA)—Molecular Cell Research, vol. 1853, no. 11, pp. 3153–3164, 2015. View at Publisher · View at Google Scholar · View at Scopus
  7. J. E. Schwarzbauer, “Fibronectin: from gene to protein,” Current Opinion in Cell Biology, vol. 3, no. 5, pp. 786–791, 1991. View at Publisher · View at Google Scholar · View at Scopus
  8. J. E. Schwarzbauer, “Alternative splicing of fibronectin: three variants, three functions,” BioEssays, vol. 13, no. 10, pp. 527–533, 1991. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Borsi, E. Balza, B. Gaggero, G. Allemanni, and L. Zardi, “The alternative splicing pattern of the tenascin-C pre-mRNA is controlled by the extracellular pH,” The Journal of Biological Chemistry, vol. 270, no. 11, pp. 6243–6245, 1995. View at Publisher · View at Google Scholar · View at Scopus
  10. U. Gabler, A. Berndt, H. Kosmehl et al., “Matrix remodelling in dilated cardiomyopathy entails the occurrence of oncofetal fibronectin molecular variants,” Heart, vol. 75, no. 4, pp. 358–362, 1996. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Imanaka-Yoshida, K.-I. Matsumoto, M. Hara, T. Sakakura, and T. Yoshida, “The dynamic expression of tenascin-C and tenascin-X during early heart development in the mouse,” Differentiation, vol. 71, no. 4-5, pp. 291–298, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. I. E. M. G. Willems, J.-W. Arends, and M. J. A. P. Daemen, “Tenascin and fibronectin expression in healing human myocardial scars,” The Journal of Pathology, vol. 179, no. 3, pp. 321–325, 1996. View at Google Scholar · View at Scopus
  13. M. Franz, C. Jung, A. Lauten, H. R. Figulla, and A. Berndt, “Tenascin-C in cardiovascular remodeling: potential impact for diagnosis, prognosis estimation and targeted therapy,” Cell Adhesion and Migration, vol. 9, no. 1-2, pp. 90–95, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Franz, D. Neri, and A. Berndt, “Chronic cardiac allograft rejection: critical role of ED-A+ fibronectin and implications for targeted therapy strategies,” The Journal of Pathology, vol. 226, no. 4, pp. 557–561, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. J.-N. Rybak, E. Trachsel, J. Scheuermann, and D. Neri, “Ligand-based vascular targeting of disease,” ChemMedChem, vol. 2, no. 1, pp. 22–40, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Aso, A. Tamura, and M. Nasu, “Circulating tenascin-C levels in patients with idiopathic dilated cardiomyopathy,” The American Journal of Cardiology, vol. 94, no. 11, pp. 1468–1470, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Franz, A. Berndt, A. Altendorf-Hofmann et al., “Serum levels of large tenascin-C variants, matrix metalloproteinase-9, and tissue inhibitors of matrix metalloproteinases in concentric versus eccentric left ventricular hypertrophy,” European Journal of Heart Failure, vol. 11, no. 11, pp. 1057–1062, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Franz, A. Berndt, K. Grün et al., “Serum levels of tenascin-C variants in congestive heart failure patients: comparative analysis of ischemic, dilated, and hypertensive cardiomyopathy,” Clinical Laboratory, vol. 60, no. 6, pp. 1007–1013, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Fujimoto, K. Onishi, A. Sato et al., “Incremental prognostic values of serum tenascin-c levels with blood B-type natriuretic peptide testing at discharge in patients with dilated cardiomyopathy and decompensated heart failure,” Journal of Cardiac Failure, vol. 15, no. 10, pp. 898–905, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. M. H. M. Hessel, G. B. Bleeker, J. J. Bax et al., “Reverse ventricular remodelling after cardiac resynchronization therapy is associated with a reduction in serum tenascin-C and plasma matrix metalloproteinase-9 levels,” European Journal of Heart Failure, vol. 9, no. 10, pp. 1058–1063, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. K. Imanaka-Yoshida, M. Hiroe, Y. Yasutomi et al., “Tenascin-C is a useful marker for disease activity in myocarditis,” The Journal of Pathology, vol. 197, no. 3, pp. 388–394, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Tamaoki, K. Imanaka-Yoshida, K. Yokoyama et al., “Tenascin-C regulates recruitment of myofibroblasts during tissue repair after myocardial injury,” The American Journal of Pathology, vol. 167, no. 1, pp. 71–80, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. F. Terasaki, H. Okamoto, K. Onishi et al., “Higher serum tenascin-C levels reflect the severity of heart failure, left ventricular dysfunction and remodeling in patients with dilated cardiomyopathy,” Circulation Journal, vol. 71, no. 3, pp. 327–330, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Nozato, A. Sato, H. Hikita et al., “Impact of serum tenascin-C on the aortic healing process during the chronic stage of type B acute aortic dissection,” International Journal of Cardiology, vol. 191, pp. 97–99, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Baldinger, B. R. Brehm, P. Richter et al., “Comparative analysis of oncofetal fibronectin and tenascin-C expression in right atrial auricular and left ventricular human cardiac tissue from patients with coronary artery disease and aortic valve stenosis,” Histochemistry and Cell Biology, vol. 135, no. 5, pp. 427–441, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Franz, A. Berndt, K. Grün et al., “Expression of extra domain A containing fibronectin in chronic cardiac allograft rejection,” The Journal of Heart and Lung Transplantation, vol. 30, no. 1, pp. 86–94, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Franz, A. Berndt, D. Neri et al., “Matrix metalloproteinase-9, tissue inhibitor of metalloproteinase-1, B+ tenascin-C and ED-A+ fibronectin in dilated cardiomyopathy: potential impact on disease progression and patients' prognosis,” International Journal of Cardiology, vol. 168, no. 6, pp. 5344–5351, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Franz, B. R. Brehm, P. Richter et al., “Changes in extra cellular matrix remodelling and re-expression of fibronectin and tenascin-C splicing variants in human myocardial tissue of the right atrial auricle: implications for a targeted therapy of cardiovascular diseases using human SIP format antibodies,” Journal of Molecular Histology, vol. 41, no. 1, pp. 39–50, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Franz, K. Grün, P. Richter et al., “Extra cellular matrix remodelling after heterotopic rat heart transplantation: gene expression profiling and involvement of ED-A+ fibronectin, alpha-smooth muscle actin and B+ tenascin-C in chronic cardiac allograft rejection,” Histochemistry and Cell Biology, vol. 134, no. 5, pp. 503–517, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Franz, M. Matusiak-Brückner, P. Richter et al., “De novo expression of fetal ED-A+ fibronectin and B+ tenascin-C splicing variants in human cardiac allografts: potential impact for targeted therapy of rejection,” Journal of Molecular Histology, vol. 45, no. 5, pp. 519–532, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Franz, I. Hilger, K. Grün et al., “Selective imaging of chronic cardiac rejection using a human antibody specific to the alternatively spliced EDA domain of fibronectin,” Journal of Heart and Lung Transplantation, vol. 32, no. 6, pp. 641–650, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Franz, F. Doll, K. Grün et al., “Targeted delivery of interleukin-10 to chronic cardiac allograft rejection using a human antibody specific to the extra domain A of fibronectin,” International Journal of Cardiology, vol. 195, pp. 311–322, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Erturk, E. Cure, Z. Ozkurt, E. Parlak, and M. C. Cure, “Serum fibronectin levels in acute and chronic viral hepatitis patients,” The Malaysian Journal of Medical Sciences, vol. 21, no. 1, pp. 29–36, 2014. View at Google Scholar · View at Scopus
  34. C. Wang, Y.-Y. Li, X. Li et al., “Serum complement C4b, fibronectin, and prolidase are associated with the pathological changes of pulmonary tuberculosis,” BMC Infectious Diseases, vol. 14, article 52, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Selmer, H. Eriksen, and I. Clemmensen, “Native and degraded fibronectin: new immunological methods for distinction,” Scandinavian Journal of Clinical and Laboratory Investigation, vol. 44, no. 1, pp. 57–63, 1984. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Schulte, M. Weidig, P. Balzer et al., “Expression of the E-cadherin repressors Snail, Slug and Zeβ1 in urothelial carcinoma of the urinary bladder: relation to stromal fibroblast activation and invasive behaviour of carcinoma cells,” Histochemistry and Cell Biology, vol. 138, no. 6, pp. 847–860, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. E. S. White, F. E. Baralle, and A. F. Muro, “New insights into form and function of fibronectin splice variants,” The Journal of Pathology, vol. 216, no. 1, pp. 1–14, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Pankov and K. M. Yamada, “Fibronectin at a glance,” Journal of Cell Science, vol. 115, no. 20, pp. 3861–3863, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Borsi, B. Carnemolla, P. Castellani et al., “Monoclonal antibodies in the analysis of fibronectin isoforms generated by alternative splicing of mRNA precursors in normal and transformed human cells,” The Journal of Cell Biology, vol. 104, no. 3, pp. 595–600, 1987. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Carnemolla, L. Borsi, L. Zardi, R. J. Owens, and F. E. Baralle, “Localization of the cellular-fibronectin-specific epitope recognized by the monoclonal antibody IST-9 using fusion proteins expressed in E. coli,” FEBS Letters, vol. 215, no. 2, pp. 269–273, 1987. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Ylätupa, P. Mertaniemi, C. Haglund, and P. Partanen, “An improved method for quantification of extra domain A-containing cellular fibronectin (EDAcFN) in different body fluids,” Clinica Chimica Acta, vol. 234, no. 1-2, pp. 79–90, 1995. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Ylatupa, C. Haglund, P. Mertaniemi, E. Vahtera, and P. Partanen, “Cellular fibronectin in serum and plasma: a potential tumour marker?” British Journal of Cancer, vol. 71, no. 3, pp. 578–582, 1995. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Kropf and A. M. Gressner, “Two sensitive time-resolved fluoroimmunoassays for cellular fibronectin,” Clinical Chemistry, vol. 41, no. 9, pp. 1283–1287, 1995. View at Google Scholar · View at Scopus
  44. A. E. Voskuyl, J. J. Emeis, J. M. W. Hazes, R. A. van Hogezand, I. Biemond, and F. C. Breedveld, “Levels of circulating cellular fibronectin are increased in patients with rheumatoid vasculitis,” Clinical and Experimental Rheumatology, vol. 16, no. 4, pp. 429–434, 1998. View at Google Scholar · View at Scopus
  45. S. D. J. M. Kanters, J.-D. Banga, A. Algra, R. C. J. M. Frijns, J. J. Beutler, and R. Fijnheer, “Plasma levels of cellular fibronectin in diabetes,” Diabetes Care, vol. 24, no. 2, pp. 323–327, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Kimura, T. Kanzaki, K. Tahara et al., “Identification of citrullinated cellular fibronectin in synovial fluid from patients with rheumatoid arthritis,” Modern Rheumatology, vol. 24, no. 5, pp. 766–769, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. R. W. Powers, R. W. Evans, R. B. Ness, W. R. Crombleholme, and J. M. Roberts, “Homocysteine and cellular fibronectin are increased in preeclampsia, not transient hypertension of pregnancy,” Hypertension in Pregnancy, vol. 20, no. 1, pp. 69–77, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Hegele, A. Heidenreich, Z. Varga et al., “Cellular fibronectin in patients with transitional cell carcinoma of the bladder,” Urological Research, vol. 30, no. 6, pp. 363–366, 2003. View at Google Scholar · View at Scopus
  49. A. Hegele, A. Heidenreich, J. Kropf et al., “Plasma levels of cellular fibronectin in patients with localized and metastatic renal cell carcinoma,” Tumor Biology, vol. 25, no. 3, pp. 111–116, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. U. M. Warawdekar, S. M. Zingde, K. S. N. Iyer, P. Jagannath, A. R. Mehta, and N. G. Mehta, “Elevated levels and fragmented nature of cellular fibronectin in the plasma of gastrointestinal and head and neck cancer patients,” Clinica Chimica Acta, vol. 372, no. 1-2, pp. 83–93, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Castellanos, T. Sobrino, M. Millan et al., “Serum cellular fibronectin and matrix metalloproteinase-9 as screening biomarkers for the prediction of parenchymal hematoma after thrombolytic therapy in acute ischemic stroke: a multicenter confirmatory study,” Stroke, vol. 38, pp. 1855–1859, 2007. View at Google Scholar
  52. A. Hegele, R. Hofmann, B. Kosche, and J. Kropf, “Evaluation of cellular fibronectin plasma levels as a useful staging tool in different stages of transitional cell carcinoma of the bladder and renal cell carcinoma,” Biomarker Insights, vol. 2, pp. 1–7, 2007. View at Google Scholar
  53. J. K. van Keulen, D. P. de Kleijn, M. M. O. Nijhuis et al., “Levels of extra domain A containing fibronectin in human atherosclerotic plaques are associated with a stable plaque phenotype,” Atherosclerosis, vol. 195, no. 1, pp. e83–e91, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Serini, M.-L. Bochaton-Piallat, P. Ropraz et al., “The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-β1,” The Journal of Cell Biology, vol. 142, no. 3, pp. 873–881, 1998. View at Publisher · View at Google Scholar · View at Scopus
  55. A. J. Booth, S. C. Wood, A. M. Cornett et al., “Recipient-derived EDA fibronectin promotes cardiac allograft fibrosis,” The Journal of Pathology, vol. 226, no. 4, pp. 609–618, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. Y. Okamura, M. Watari, E. S. Jerud et al., “The extra domain A of fibronectin activates Toll-like receptor 4,” The Journal of Biological Chemistry, vol. 276, no. 13, pp. 10229–10233, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Kelsh, R. You, C. Horzempa, M. Zheng, and P. J. McKeown-Longo, “Regulation of the innate immune response by fibronectin: synergism between the III-1 and EDA domains,” PLoS ONE, vol. 9, no. 7, Article ID e102974, 2014. View at Publisher · View at Google Scholar · View at Scopus
  58. J. P. McFadden, B. S. Baker, A. V. Powles, and L. Fry, “Psoriasis and extra domain A fibronectin loops,” The British Journal of Dermatology, vol. 163, no. 1, pp. 5–11, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. S.-I. Morimoto, K. Imanaka-Yoshida, S. Hiramitsu et al., “Diagnostic utility of tenascin-C for evaluation of the activity of human acute myocarditis,” Journal of Pathology, vol. 205, no. 4, pp. 460–467, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. H.-C. Yao, Q.-F. Han, A.-P. Zhao, D.-K. Yao, and L.-X. Wang, “Prognostic values of serum tenascin-C in patients with ischaemic heart disease and heart failure,” Heart, Lung & Circulation, vol. 22, no. 3, pp. 184–187, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Golledge, P. Clancy, J. Maguire, L. Lincz, and S. Koblar, “The role of tenascin C in cardiovascular disease,” Cardiovascular Research, vol. 92, no. 1, pp. 19–28, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Singh, C. Carraher, and J. E. Schwarzbauer, “Assembly of fibronectin extracellular matrix,” Annual Review of Cell and Developmental Biology, vol. 26, pp. 397–419, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. F. Doll, K. Schwager, T. Hemmerle, and D. Neri, “Murine analogues of etanercept and of F8-IL10 inhibit the progression of collagen-induced arthritis in the mouse,” Arthritis Research and Therapy, vol. 15, no. 5, article R138, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Villa, E. Trachsel, M. Kaspar et al., “A high-affinity human monoclonal antibody specific to the alternatively spliced EDA domain of fibronectin efficiently targets tumor neo-vasculature in vivo,” International Journal of Cancer, vol. 122, no. 11, pp. 2405–2413, 2008. View at Publisher · View at Google Scholar · View at Scopus