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Stem Cells International
Volume 2017, Article ID 9717353, 9 pages
https://doi.org/10.1155/2017/9717353
Research Article

Mesenchymal Stromal Cells Accelerate Epithelial Tight Junction Assembly via the AMP-Activated Protein Kinase Pathway, Independently of Liver Kinase B1

1Groupe Interdisciplinaire de Génoprotéomique Appliquée (GIGA), Cardiovascular Sciences, University of Liège (ULg), Liège, Belgium
2Division of Nephrology, University of Liège Hospital (ULg CHU), Liège, Belgium
3Centre de Recherche en Cancérologie de Marseille, Aix Marseille Université UM105, Institut Paoli Calmettes, UMR7258 CNRS, U1068 INSERM, Cell Polarity, Cell Signalling and Cancer “Equipe Labellisée Ligue Contre le Cancer”, Marseille, France

Correspondence should be addressed to F. Jouret; eb.ca.glu@teruoj.siocnarf

Received 30 March 2017; Accepted 21 May 2017; Published 11 July 2017

Academic Editor: Bruno Christ

Copyright © 2017 P. Rowart 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. J. Caplan, P. Seo-Mayer, and L. Zhang, “Epithelial junctions and polarity: complexes and kinases,” Current Opinion in Nephrology and Hypertension, vol. 17, no. 5, pp. 506–512, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Hou, “The kidney tight junction (review),” International Journal of Molecular Medicine, vol. 34, no. 6, pp. 1451–1457, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Gonzalezmariscal, “Tight junction proteins,” Progress in Biophysics and Molecular Biology, vol. 81, no. 1, pp. 1–44, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. E. McNeil, C. T. Capaldo, and I. G. Macara, “Zonula occludens-1 function in the assembly of tight junctions in Madin-Darby canine kidney epithelial cells,” Molecular Biology of the Cell, vol. 17, no. 4, pp. 1922–1932, 2006. View at Google Scholar
  5. A. S. Fanning and J. M. Anderson, “Zonula occludens-1 and -2 are cytosolic scaffolds that regulate the assembly of cellular junctions,” Annals of the New York Academy of Sciences, vol. 1165, no. 1, pp. 113–120, 2009. View at Google Scholar
  6. R. G. Contreras, J. H. Miller, M. Zamora, L. Gonzalez-Mariscal, and M. Cereijido, “Interaction of calcium with plasma membrane of epithelial (MDCK) cells during junction formation,” The American Journal of Physiology, vol. 263, Part 1, no. 2, pp. C313–C318, 1992. View at Google Scholar
  7. L. Gonzalez-Mariscal, B. Chávez de Ramírez, and M. Cereijido, “Tight junction formation in cultured epithelial cells (MDCK),” The Journal of Membrane Biology, vol. 86, no. 2, pp. 113–125, 1985. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Meldolesi, G. Castiglioni, R. Parma, N. Nassivera, and P. De Camilli, “Ca++-dependent disassembly and reassembly of occluding junctions in guinea pig pancreatic acinar cells. Effect of drugs,” The Journal of Cell Biology, vol. 79, no. 1, pp. 156–172, 1978. View at Publisher · View at Google Scholar
  9. C. E. Palant, M. E. Duffey, B. K. Mookerjee, S. Ho, and C. J. Bentzel, “Ca2+ regulation of tight-junction permeability and structure in Necturus gallbladder,” The American Journal of Physiology, vol. 245, no. 3, pp. C203–C212, 1983. View at Google Scholar
  10. L. Gonzalez-Mariscal, R. G. Contreras, J. J. Bolívar, A. Ponce, B. Chávez De Ramirez, and M. Cereijido, “Role of calcium in tight junction formation between epithelial cells,” The American Journal of Physiology, vol. 259, Part 1, no. 6, pp. C978–C986, 1990. View at Google Scholar
  11. L. Zhang, J. Li, L. H. Young, and M. J. Caplan, “AMP-activated protein kinase regulates the assembly of epithelial tight junctions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 46, pp. 17272–17277, 2006. View at Google Scholar
  12. L. Zhang, F. Jouret, J. Rinehart et al., “AMP-activated protein kinase (AMPK) activation and glycogen synthase kinase-3β (GSK-3β) inhibition induce Ca2+-independent deposition of tight junction components at the plasma membrane,” The Journal of Biological Chemistry, vol. 286, no. 19, pp. 16879–16890, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. F. Jouret, J. Wu, M. Hull et al., “Activation of the Ca(2)+−sensing receptor induces deposition of tight junction components to the epithelial cell plasma membrane,” Journal of Cell Science, vol. 126, Part 22, pp. 5132–5142, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Chen and M. Zhang, “The Par3/Par6/aPKC complex and epithelial cell polarity,” Experimental Cell Research, vol. 319, no. 10, pp. 1357–1364, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. N. Aznar, A. Patel, C. C. Rohena et al., “AMP-activated protein kinase fortifies epithelial tight junctions during energetic stress via its effector GIV/Girdin,” eLife, vol. 5, article e71, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. J. H. Lee, H. Koh, M. Kim et al., “Energy-dependent regulation of cell structure by AMP-activated protein kinase,” Nature, vol. 447, no. 7147, pp. 1017–1020, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. D. G. Hardie, “AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function,” Genes & Development, vol. 25, no. 18, pp. 1895–1908, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Zheng and L. C. Cantley, “Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 3, pp. 819–822, 2007. View at Google Scholar
  19. R. J. Shaw, M. Kosmatka, N. Bardeesy et al., “The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 10, pp. 3329–3335, 2004. View at Google Scholar
  20. S. A. Hawley, D. A. Pan, K. J. Mustard et al., “Calmodulin-dependent protein kinase kinase-β is an alternative upstream kinase for AMP-activated protein kinase,” Cell Metabolism, vol. 2, no. 1, pp. 9–19, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. D. G. Hardie, F. A. Ross, and S. A. Hawley, “AMPK: a nutrient and energy sensor that maintains energy homeostasis,” Nature Reviews. Molecular Cell Biology, vol. 13, no. 4, pp. 251–262, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Sebbagh, S. Olschwang, M.-J. Santoni, and J.-P. Borg, “The LKB1 complex-AMPK pathway: the tree that hides the forest,” Familial Cancer, vol. 10, no. 3, pp. 415–424, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Carling, M. J. Sanders, and A. Woods, “The regulation of AMP-activated protein kinase by upstream kinases,” International Journal of Obesity, vol. 32, pp. S55–S59, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Sebbagh, M.-J. Santoni, B. Hall, J.-P. Borg, and M. A. Schwartz, “Regulation of LKB1/STRAD localization and function by E-cadherin,” Current Biology, vol. 19, no. 1, pp. 37–42, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Oligschlaeger, M. Miglianico, D. Chanda et al., “The recruitment of AMP-activated protein kinase to glycogen is regulated by autophosphorylation,” The Journal of Biological Chemistry, vol. 290, no. 18, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Ooshio, R. Kobayashi, W. Ikeda et al., “Involvement of the interaction of afadin with ZO-1 in the formation of tight junctions in Madin-Darby canine kidney cells,” The Journal of Biological Chemistry, vol. 285, no. 7, pp. 5003–5012, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Castanares-Zapatero, C. Bouleti, C. Sommereyns et al., “Connection between cardiac vascular permeability, myocardial edema, and inflammation during sepsis,” Critical Care Medicine, vol. 41, no. 12, pp. e411–e422, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. P. W. Seo-Mayer, G. Thulin, L. Zhang et al., “Preactivation of AMPK by metformin may ameliorate the epithelial cell damage caused by renal ischemia,” American Journal of Physiology. Renal Physiology, vol. 301, no. 6, pp. F1346–F1357, 2011. View at Google Scholar
  29. J. Lempiäinen, P. Finckenberg, J. Levijoki, and E. Mervaala, “AMPK activator AICAR ameliorates ischaemia reperfusion injury in the rat kidney,” British Journal of Pharmacology, vol. 166, no. 6, pp. 1905–1915, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. V. Cantaluppi, L. Biancone, A. Quercia, M. C. Deregibus, G. Segoloni, and G. Camussi, “Rationale of mesenchymal stem cell therapy in kidney injury,” American Journal of Kidney Diseases, vol. 61, no. 2, pp. 300–309, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. P. Erpicum, O. Detry, L. Weekers et al., “Mesenchymal stromal cell therapy in conditions of renal ischaemia/reperfusion,” Nephrology Dialysis Transplantation, vol. 29, no. 8, pp. 1487–1493, 2014, Oxford University Press. View at Publisher · View at Google Scholar · View at Scopus
  32. P. Rowart, P. Erpicum, O. Detry et al., “Mesenchymal stromal cell therapy in ischemia/reperfusion injury,” Journal of Immunology Research, vol. 2015, Article ID 602597, 8 pages, 2015. View at Google Scholar
  33. M. Franquesa, M. J. Hoogduijn, M. E. Reinders et al., “Mesenchymal stem cells in solid organ transplantation (MiSOT) fourth meeting: lessons learned from first clinical trials,” Transplantation, vol. 96, no. 3, pp. 234–238, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Souidi, M. Stolk, and M. Seifert, “Ischemia–reperfusion injury: beneficial effects of mesenchymal stromal cells,” Current Opinion in Organ Transplantation, vol. 18, no. 1, pp. 34–43, 2013. View at Google Scholar
  35. S. Winkler, M. Hempel, S. Brückner, H.-M. Tautenhahn, R. Kaufmann, and B. Christ, “Identification of pathways in liver repair potentially targeted by secretory proteins from human mesenchymal stem cells,” International Journal of Molecular Sciences, vol. 17, no. 7, p. 1099, 2016. View at Publisher · View at Google Scholar · View at Scopus
  36. W. Broekman, G. D. Amatngalim, Y. de Mooij-Eijk et al., “TNF-alpha and IL-1beta-activated human mesenchymal stromal cells increase airway epithelial wound healing in vitro via activation of the epidermal growth factor receptor,” Respiratory Research, vol. 17, no. 1, p. 3, 2016. View at Google Scholar
  37. K. M. Akram, S. Samad, M. A. Spiteri, and N. R. Forsyth, “Mesenchymal stem cells promote alveolar epithelial cell wound repair in vitro through distinct migratory and paracrine mechanisms,” Respiratory Research, vol. 14, no. 1, p. 9, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. A. I. Caplan and J. E. Dennis, “Mesenchymal stem cells as trophic mediators,” Journal of Cellular Biochemistry, vol. 98, no. 5, pp. 1076–1084, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. G. Raposo and W. Stoorvogel, “Extracellular vesicles: exosomes, microvesicles, and friends,” The Journal of Cell Biology, vol. 200, no. 4, pp. 373–383, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Camussi, M. C. Deregibus, S. Bruno, V. Cantaluppi, and L. Biancone, “Exosomes/microvesicles as a mechanism of cell-to-cell communication,” Kidney International, vol. 78, no. 9, pp. 838–848, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. J. V. Bonventre, “Microvesicles from mesenchymal stromal cells protect against acute kidney injury,” Journal of the American Society of Nephrology, vol. 20, no. 5, pp. 927-928, 2009. View at Google Scholar
  42. M. Dominici, K. Le Blanc, I. Mueller et al., “Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement,” Cytotherapy, vol. 8, no. 4, pp. 315–317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. X. X. Tang, H. Chen, S. Yu, L. Zhang, M. J. Caplan, and H. C. Chan, “Lymphocytes accelerate epithelial tight junction assembly: role of AMP-activated protein kinase (AMPK),” PloS One, vol. 5, no. 8, article e12343, 2010. View at Google Scholar
  44. L. Ho, L. Tsang, Y. Chung, and H. Chan, “Establishment of a mouse primary co-culture of endometrial epithelial cells and peripheral blood leukocytes: effect on epithelial barrier function and leukocyte survival,” Cell Biology International, vol. 30, no. 12, pp. 977–982, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. C. De Meester, A. D. Timmermans, M. Balteau et al., “Role of AMP-activated protein kinase in regulating hypoxic survival and proliferation of mesenchymal stem cells,” Cardiovascular Research, vol. 101, no. 1, pp. 20–29, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. X.-Y. Zhu, V. Urbieta-Caceres, J. D. Krier, S. C. Textor, A. Lerman, and L. O. Lerman, “Mesenchymal stem cells and endothelial progenitor cells decrease renal injury in experimental swine renal artery stenosis through different mechanisms,” Stem Cells, vol. 31, no. 1, pp. 117–125, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Hardie and S. Hawley, “AMP-activated protein kinase: the energy charge hypothesis revisited,” BioEssays, vol. 23, no. 12, pp. 1112–1119, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. G. R. Steinberg and B. E. Kemp, “AMPK in health and disease,” Physiological Reviews, vol. 89, no. 3, pp. 1025–1078, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Cantó and J. Auwerx, “AMP-activated protein kinase and its downstream transcriptional pathways,” Cellular and Molecular Life Sciences, vol. 67, no. 20, pp. 3407–3423, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. J. D. Matthews, C. M. Weight, and C. A. Parkos, “Leukocyte-epithelial interactions and mucosal homeostasis,” Toxicologic Pathology, vol. 42, no. 1, pp. 91–98, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. K. Bäsler and J. M. Brandner, “Tight junctions in skin inflammation,” Pflügers Archiv-European Journal of Physiology, vol. 1, no. 1, pp. 3–14, 2016. View at Google Scholar
  52. A. M. Dimarino, A. I. Caplan, and T. L. Bonfield, “Mesenchymal stem cells in tissue repair,” Frontiers in Immunology, vol. 4, p. 201, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Morigi and A. Benigni, “Mesenchymal stem cells and kidney repair,” Nephrology, Dialysis, Transplantation, vol. 28, no. 4, pp. 788–793, 2013. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Biancone, S. Bruno, M. C. Deregibus, C. Tetta, and G. Camussi, “Therapeutic potential of mesenchymal stem cell-derived microvesicles,” Nephrology, Dialysis, Transplantation, vol. 27, no. 8, pp. 3037–3042, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. J. He, Y. Wang, S. Sun et al., “Bone marrow stem cells-derived microvesicles protect against renal injury in the mouse remnant kidney model,” Nephrology (Carlton, Vic.), vol. 17, no. 5, pp. 493–500, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Rao, Y. Zhang, Q. Li et al., “AMPK-dependent and independent effects of AICAR and compound C on T-cell responses,” Oncotarget, vol. 7, no. 23, pp. 33783–33795, 2014. View at Google Scholar