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BioMed Research International
Volume 2017, Article ID 2403072, 9 pages
https://doi.org/10.1155/2017/2403072
Research Article

Expression of C4.4A in an In Vitro Human Tissue-Engineered Skin Model

1The Finsen Laboratory, Copenhagen University Hospital (Rigshospitalet), Copenhagen Biocenter, Copenhagen, Denmark
2Biotech Research and Innovation Centre (BRIC), University of Copenhagen, Copenhagen, Denmark
3Centre de Recherche du CHU de Québec-Université Laval, Department of Surgery, Faculty of Medicine, Université Laval and Centre de Recherche en Organogénèse Expérimentale de l’Université Laval (LOEX), Québec, QC, Canada

Correspondence should be addressed to Danielle Larouche; ac.lavalu@2.ehcuoral.elleinad and Lucie Germain; ac.lavalu.demf@niamreg.eicul

Received 27 March 2017; Accepted 18 July 2017; Published 7 September 2017

Academic Editor: Xin-yuan Guan

Copyright © 2017 Benedikte Jacobsen 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. M. Kjaergaard, L. V. Hansen, B. Jacobsen, H. Gardsvoll, and M. Ploug, “Structure and ligand interactions of the urokinase receptor (uPAR),” Frontiers in Bioscience, vol. 13, no. 14, pp. 5441–5461, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. C. L. Loughner, E. A. Bruford, M. S. McAndrews, E. E. Delp, S. Swamynathan, and S. K. Swamynathan, “Organization, evolution and functions of the human and mouse Ly6/uPAR family genes,” Human Genomics, vol. 10, no. 1, article 10, 2016. View at Publisher · View at Google Scholar
  3. R. A. Brodsky, “Complement in hemolytic anemia,” Blood, vol. 126, no. 22, pp. 2459–2465, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Ploug, “Structure-driven design of radionuclide tracers for non-invasive imaging of uPAR and targeted radiotherapy. The tale of a synthetic peptide antagonist,” Theranostics, vol. 3, no. 7, pp. 467–476, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Mysling, K. K. Kristensen, M. Larsson et al., “The angiopoietin-like protein ANGPTL4 catalyzes unfolding of the hydrolase domain in lipoprotein lipase and the endothelial membrane protein GPIHBP1 counteracts this unfolding,” eLife, vol. 5, Article ID e20958, 18 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Mysling, K. K. Kristensen, M. Larsson et al., “The acidic domain of the endothelial membrane protein GPIHBP1 stabilizes lipoprotein lipase activity by preventing unfolding of its catalytic domain,” eLife, vol. 5, Article ID e12095, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. Y. Fujihara, K. Tokuhiro, Y. Muro et al., “Expression of TEX101, regulated by ACE, is essential for the production of fertile mouse spermatozoa,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 20, pp. 8111–8116, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. Z. Wu, R. Liang, T. Ohnesorg et al., “Heterogeneity of human neutrophil CD177 expression results from CD177P1 pseudogene conversion,” PLoS Genetics, vol. 12, no. 5, Article ID e1006067, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. O. Adeyo, B. B. Allan, R. H. Barnes II et al., “Palmoplantar keratoderma along with neuromuscular and metabolic phenotypes in slurp1-deficient mice,” Journal of Investigative Dermatology, vol. 134, no. 6, pp. 1589–1598, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Perez and A. Khachemoune, “Mal de Meleda: a focused review,” American Journal of Clinical Dermatology, vol. 17, no. 1, pp. 63–70, 2016. View at Publisher · View at Google Scholar · View at Scopus
  11. M. C. Kriegbaum, M. Persson, L. Haldager et al., “Rational targeting of the urokinase receptor (uPAR): Development of antagonists and non-invasive imaging probes,” Current Drug Targets, vol. 12, no. 12, pp. 1711–1728, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. M. C. Kriegbaum, B. Jacobsen, A. Hald, and M. Ploug, “Expression of C4.4A, a structural uPAR homolog, reflects squamous epithelial differentiation in the adult mouse and during embryogenesis,” Journal of Histochemistry and Cytochemistry, vol. 59, no. 2, pp. 188–201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Gårdsvoll, M. C. Kriegbaum, E. P. Hertz, W. Alpízar-Alpízar, and M. Ploug, “The urokinase receptor homolog Haldisin is a novel differentiation marker of stratum granulosum in squamous epithelia,” Journal of Histochemistry and Cytochemistry, vol. 61, no. 11, pp. 802–813, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Jacobsen and M. Ploug, “The urokinase receptor and its structural homologue C4.4A in human cancer: Expression, prognosis and pharmacological inhibition,” Current Medicinal Chemistry, vol. 15, no. 25, pp. 2559–2573, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. L. V. Hansen, H. Gårdsvoll, B. S. Nielsen et al., “Structural analysis and tissue localization of human C4.4A: A protein homologue of the urokinase receptor,” Biochemical Journal, vol. 380, no. 3, pp. 845–857, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Rösel, C. Claas, S. Seiter, M. Herlevsen, and M. Zöller, “Cloning and functional characterization of a new phosphatidyl-inositol anchored molecule of a metastasizing rat pancreatic tumor,” Oncogene, vol. 17, no. 15, pp. 1989–2002, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. L. V. Hansen, B. G. Skov, M. Ploug, and H. Pappot, “Tumour cell expression of C4.4A, a structural homologue of the urokinase receptor, correlates with poor prognosis in non-small cell lung cancer,” Lung Cancer, vol. 58, no. 2, pp. 260–266, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Jacobsen, M. C. Kriegbaum, E. Santoni-Rugiu, and M. Ploug, “C4.4A as a biomarker in pulmonary adenocarcinoma and squamous cell carcinoma,” World Journal of Clinical Oncology, vol. 5, no. 4, pp. 621–632, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Jacobsen, E. Santoni-Rugiu, M. Illemann, M. C. Kriegbaum, O. D. Lærum, and M. Ploug, “Expression of C4.4A in precursor lesions of pulmonary adenocarcinoma and squamous cell carcinoma,” International Journal of Cancer, vol. 130, no. 11, pp. 2734–2739, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. B. Jacobsen, T. Muley, M. Meister et al., “Ly6/upar-related protein c4.4a as a marker of solid growth pattern and poor prognosis in lung adenocarcinoma,” Journal of Thoracic Oncology, vol. 8, no. 2, pp. 152–160, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. L. V. Hansen, O. D. Lærum, M. Illemann, B. S. Nielsen, and M. Ploug, “Altered expression of the urokinase receptor homologue, C4.4A, in invasive areas of human esophageal squamous cell carcinoma,” International Journal of Cancer, vol. 122, no. 4, pp. 734–741, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Ohtsuka, H. Yamamoto, T. Masuzawa et al., “C4.4A expression is associated with a poor prognosis of esophageal squamous cell carcinoma,” Annals of Surgical Oncology, vol. 20, no. 8, pp. 2699–2705, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Konishi, H. Yamamoto, K. Mimori et al., “Expression of C4.4A at the invasive front is a novel prognostic marker for disease recurrence of colorectal cancer,” Cancer Science, vol. 101, no. 10, pp. 2269–2277, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. M. C. Kriegbaum, O. P. F. Clausen, O. D. Lærum, and M. Ploug, “Expression of the Ly6/uPAR-domain proteins C4.4A and Haldisin in non-invasive and invasive skin lesions,” Journal of Histochemistry and Cytochemistry, vol. 63, no. 2, pp. 142–154, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. M. C. Kriegbaum, B. Jacobsen, A. Füchtbauer et al., “C4.4A gene ablation is compatible with normal epidermal development and causes modest overt phenotypes,” Scientific Reports, vol. 6, Article ID 25833, 2016. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Michel, N. L'Heureux, R. Pouliot, W. Xu, F. A. Auger, and L. Germain, “Characterization of a new tissue-engineered human skin equivalent with hair,” In Vitro Cellular and Developmental Biology—Animal, vol. 35, no. 6, pp. 318–326, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Pouliot, D. Larouche, F. A. Auger et al., “Reconstructed human skin produced in vitro and grafted on athymic mice,” Transplantation, vol. 73, no. 11, pp. 1751–1757, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Dubé, O. Rochette-Drouin, P. Lévesque et al., “Restoration of the transepithelial potential within tissue-engineered human skin in vitro and during the wound healing process in vivo,” Tissue Engineering Part A, vol. 16, no. 10, pp. 3055–3063, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Robitaille, C. Simard-Bisson, D. Larouche, R. M. Tanguay, R. Blouin, and L. Germain, “The small heat-shock protein Hsp27 undergoes ERK-dependent phosphorylation and redistribution to the cytoskeleton in response to dual leucine zipper-bearing kinase expression,” Journal of Investigative Dermatology, vol. 130, no. 1, pp. 74–85, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Germain, M. Rouabhia, R. Guignard, L. Carrier, V. Bouvard, and F. A. Auger, “Improvement of human keratinocyte isolation and culture using thermolysin,” Burns, vol. 19, no. 2, pp. 99–104, 1993. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Bisson, É. Rochefort, A. Lavoie et al., “Irradiated human dermal fibroblasts are as efficient as mouse fibroblasts as a feeder layer to improve human epidermal cell culture lifespan,” International Journal of Molecular Sciences, vol. 14, no. 3, pp. 4684–4704, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Larouche, C. Paquet, J. Fradette, P. Carrier, F. A. Auger, and L. Germain, “Regeneration of skin and cornea by tissue engineering,” Methods in Molecular Biology, vol. 482, pp. 233–256, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. A. F. Laplante, L. Germain, F. A. Auger, and V. Moulin, “Mechanisms of wound reepithelialization: hints from a tissue-engineered reconstructed skin to long-standing questions,” The FASEB Journal, vol. 15, no. 13, pp. 2377–2389, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Gårdsvoll, L. V. Hansen, T. J. D. Jørgensen, and M. Ploug, “A new tagging system for production of recombinant proteins in Drosophila S2 cells using the third domain of the urokinase receptor,” Protein Expression and Purification, vol. 52, no. 2, pp. 384–394, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. I. Royal, A. Grenier, D. Mailhot, and N. Marceau, “Polyomavirus middle T selective action on cytokeratin 14 gene expression in liver nonparenchymal epithelial cells,” Experimental Cell Research, vol. 220, no. 1, pp. 171–177, 1995. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Larouche, L. Cantin-Warren, M. Desgagné et al., “Improved methods to produce tissue-engineered skin substitutes suitable for the permanent closure of full-thickness skin injuries,” BioResearch Open Access, vol. 5, no. 1, pp. 320–329, 2016. View at Publisher · View at Google Scholar
  37. R. Moll, W. W. Franke, D. L. Schiller, B. Geiger, and R. Krepler, “The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells,” Cell, vol. 31, no. 1, pp. 11–24, 1982. View at Publisher · View at Google Scholar · View at Scopus
  38. M. D. Hertle, M.-D. Kubler, I. M. Leigh, and F. M. Watt, “Aberrant integrin expression during epidermal wound healing and in psoriatic epidermis,” Journal of Clinical Investigation, vol. 89, no. 6, pp. 1892–1901, 1992. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Hanson, “The histogenesis of the epidermis in the rat and mouse,” Journal of Anatomy, vol. 81, no. 2, pp. 174–197, 1947. View at Google Scholar · View at Scopus
  40. C. Blanpain and E. Fuchs, “Epidermal homeostasis: a balancing act of stem cells in the skin,” Nature Reviews Molecular Cell Biology, vol. 10, no. 3, pp. 207–217, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Fuchs, “Finding One's Niche in the Skin,” Cell Stem Cell, vol. 4, no. 6, pp. 499–502, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. J. R. Bickenbach, J. M. Greer, D. S. Bundman, J. A. Rothnagel, and D. R. Roop, “Loricrin expression is coordinated with other epidermal proteins and the appearance of lipid lamellar granules in development,” Journal of Investigative Dermatology, vol. 104, no. 3, pp. 405–410, 1995. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Byrne, M. Tainsky, and E. Fuchs, “Programming gene expression in developing epidermis,” Development, vol. 120, no. 9, pp. 2369–2383, 1994. View at Google Scholar · View at Scopus
  44. F. Fries, I. Nazarenko, J. Hess, A. Claas, P. Angel, and M. Zöller, “CEBPβ, JunD and c-Jun contribute to the transcriptional activation of the metastasis-associated C4.4A gene,” International Journal of Cancer, vol. 120, no. 10, pp. 2135–2147, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. W.-Y. Yu, J. M. W. Slack, and D. Tosh, “Conversion of columnar to stratified squamous epithelium in the developing mouse oesophagus,” Developmental Biology, vol. 284, no. 1, pp. 157–170, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. R. E. Leube and T. J. Rustad, “Squamous cell metaplasia in the human lung: molecular characteristics of epithelial stratification,” Virchows Archiv B Cell Pathology Including Molecular Pathology, vol. 61, no. 1, pp. 227–253, 1992. View at Publisher · View at Google Scholar · View at Scopus
  47. P. Stosiek, M. Kasper, and R. Moll, “Changes in cytokeratin expression accompany squamous metaplasia of the human respiratory epithelium,” Virchows Archiv A Pathological Anatomy and Histopathology, vol. 421, no. 2, pp. 133–141, 1992. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Paret, M. Bourouba, A. Beer et al., “Ly6 family member C4.4A binds laminins 1 and 5, associates with Galectin-3 and supports cell migration,” International Journal of Cancer, vol. 115, no. 5, pp. 724–733, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Nieminen, A. Kuno, J. Hirabayashi, and S. Sato, “Visualization of galectin-3 oligomerization on the surface of neutrophils and endothelial cells using fluorescence resonance energy transfer,” Journal of Biological Chemistry, vol. 282, no. 2, pp. 1374–1383, 2007. View at Publisher · View at Google Scholar · View at Scopus