Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2016, Article ID 5756901, 10 pages
http://dx.doi.org/10.1155/2016/5756901
Research Article

Endurance Exercise Mobilizes Developmentally Early Stem Cells into Peripheral Blood and Increases Their Number in Bone Marrow: Implications for Tissue Regeneration

1Faculty of Biology, University of Environmental and Life Sciences, 50-375 Wroclaw, Poland
2Wroclaw Research Center EIT+, 54-066 Wroclaw, Poland
3Department of Regenerative Medicine, Medical University of Warsaw, 02-091 Warsaw, Poland
4Department of Physiotherapy, University School of Physical Education, 51-617 Wroclaw, Poland
5Stem Cell Biology Program, James Graham Brown Cancer Center, Louisville, KY 40202, USA

Received 18 February 2015; Accepted 26 March 2015

Academic Editor: Irma Virant-Klun

Copyright © 2016 Krzysztof Marycz 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. H. Bonig and T. Papayannopoulou, “Hematopoietic stem cell mobilization: updated conceptual renditions,” Leukemia, vol. 27, no. 1, pp. 24–31, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Z. Ratajczak, T. Jadczyk, D. Pędziwiatr, and W. Wojakowski, “New advances in stem cell research: practical implications for regenerative medicine,” Polskie Archiwum Medycyny Wewnętrznej, vol. 124, pp. 417–426, 2014. View at Google Scholar
  3. M. Z. Ratajczak, K. Marycz, A. Poniewierska-Baran, K. Fiedorowicz, M. Zbucka-Kretowska, and M. Moniuszko, “Very small embryonic-like stem cells as a novel developmental concept and the hierarchy of the stem cell compartment,” Advances in Medical Sciences, vol. 59, no. 2, pp. 273–280, 2014. View at Publisher · View at Google Scholar
  4. T. Lapidot and O. Kollet, “The brain-bone-blood triad: traffic lights for stem-cell homing and mobilization,” Hematology/the Education Program of the American Society of Hematology, vol. 2010, pp. 1–6, 2010. View at Publisher · View at Google Scholar
  5. S. Massberg, P. Schaerli, I. Knezevic-Maramica et al., “Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues,” Cell, vol. 131, no. 5, pp. 994–1008, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. J. M. Baker, M. de Lisio, and G. Parise, “Endurance exercise training promotes medullary hematopoiesis,” The FASEB Journal, vol. 25, no. 12, pp. 4348–4357, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. M. de Lisio and G. Parise, “Characterization of the effects of exercise training on hematopoietic stem cell quantity and function,” Journal of Applied Physiology, vol. 113, no. 10, pp. 1576–1584, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. J. M. Kroepfl, K. Pekovits, I. Stelzer et al., “Exercise increases the frequency of circulating hematopoietic progenitor cells, but reduces hematopoietic colony-forming capacity,” Stem Cells and Development, vol. 21, no. 16, pp. 2915–2925, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. K. A. Volaklis, S. P. Tokmakidis, and M. Halle, “Acute and chronic effects of exercise on circulating endothelial progenitor cells in healthy and diseased patients,” Clinical Research in Cardiology, vol. 102, no. 4, pp. 249–257, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. A. M. Havens, H. Sun, Y. Shiozawa et al., “Human and murine very small embryonic-like cells represent multipotent tissue progenitors, in vitro and in vivo,” Stem Cells and Development, vol. 23, no. 7, pp. 689–701, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Kucia, M. Wysoczynski, J. Ratajczak, and M. Z. Ratajczak, “Identification of very small embryonic like (VSEL) stem cells in bone marrow,” Cell and Tissue Research, vol. 331, no. 1, pp. 125–134, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Z. Ratajczak, D.-M. Shin, R. Liu et al., “Very Small Embryonic/Epiblast-Like stem cells (VSELs) and their potential role in aging and organ rejuvenation—an update and comparison to other primitive small stem cells isolated from adult tissues,” Aging, vol. 4, no. 4, pp. 235–246, 2012. View at Google Scholar · View at Scopus
  13. H. M. Lee, W. Wu, M. Wysoczynski et al., “Impaired mobilization of hematopoietic stem/progenitor cells in C5-deficient mice supports the pivotal involvement of innate immunity in this process and reveals novel promobilization effects of granulocytes,” Leukemia, vol. 23, no. 11, pp. 2052–2062, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Z. Ratajczak, H. Lee, M. Wysoczynski et al., “Novel insight into stem cell mobilization-plasma sphingosine-1-phosphate is a major chemoattractant that directs the egress of hematopoietic stem progenitor cells from the bone marrow and its level in peripheral blood increases during mobilization due to activation of complement cascade/membrane attack complex,” Leukemia, vol. 24, no. 5, pp. 976–985, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Rafii, B. Heissig, and K. Hattori, “Efficient mobilization and recruitment of marrow-derived endothelial and hematopoietic stem cells by adenoviral vectors expressing angiogenic factors,” Gene Therapy, vol. 9, no. 10, pp. 631–641, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Wysoczynski, J. Ratajczak, D. Pedziwiatr, G. Rokosh, R. Bolli, and M. Z. Ratajczak, “Identification of heme oxygenase 1 (HO-1) as a novel negative regulator of mobilization of hematopoietic stem/progenitor cells,” Stem Cell Reviews and Reports, vol. 11, no. 1, pp. 110–118, 2015. View at Publisher · View at Google Scholar
  17. K. Grymula, K. Piotrowska, S. Słuczanowska-Głąbowska et al., “Positive effects of prolonged caloric restriction on the population of very small embryonic-like stem cells—hematopoietic and ovarian implications,” Journal of Ovarian Research, vol. 7, no. 1, article 68, 2014. View at Publisher · View at Google Scholar
  18. M. Suszynska, E. K. Zuba-Surma, M. Maj et al., “The proper criteria for identification and sorting of very small embryonic-like stem cells, and some nomenclature issues,” Stem Cells and Development, vol. 23, no. 7, pp. 702–713, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. S. H. Kassmer, H. Jin, P.-X. Zhang et al., “Very small embryonic-like stem cells from the murine bone marrow differentiate into epithelial cells of the lung,” Stem Cells, vol. 31, no. 12, pp. 2759–2766, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. S. H. Kassmer, E. M. Bruscia, P. X. Zhang, and D. S. Krause, “Nonhematopoietic cells are the primary source of bone marrow-derived lung epithelial cells,” Stem Cells, vol. 30, no. 3, pp. 491–499, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. I. Virant-Klun, N. Zech, P. Rožman et al., “Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes,” Differentiation, vol. 76, no. 8, pp. 843–856, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Bhartiya, S. Kasiviswananthan, and A. Shaikh, “Cellular origin of testis-derived pluripotent stem cells: a case for very small embryonic-like stem cells,” Stem Cells and Development, vol. 21, no. 5, pp. 670–674, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Maredziak, K. Marycz, A. Śmieszek, D. Lewandowski, and N. Y. Toker, “The influence of static magnetic fields on canine and equine mesenchymal stem cells derived from adipose tissue,” In Vitro Cellular & Developmental Biology: Animal, vol. 50, no. 6, pp. 562–571, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Donesz-Sikorska, K. Marycz, A. Śmieszek, J. Grzesiak, K. Kaliński, and J. Krzak-Roś, “Biologically active oxide coatings, produced by the sol-gel method on steel implant,” Przemysł Chemiczny, vol. 92, no. 6, pp. 1110–1116, 2013. View at Google Scholar · View at Scopus
  25. K. Marycz, J. Krzak-Roś, A. Śmieszek, J. Grzesiak, and A. Donesz-Sikorska, “Effect of oxide materials synthesized with sol–gel method on adhesion of mesenchymal stem cells,” Przemysl Chemiczny, vol. 92, no. 6, pp. 1000–1003, 2013. View at Google Scholar · View at Scopus
  26. W. Wojakowski, M. Tendera, M. Kucia et al., “Mobilization of bone marrow-derived Oct-4+ SSEA-4+ very small embryonic-like stem cells in patients with acute myocardial infarction,” Journal of the American College of Cardiology, vol. 53, no. 1, pp. 1–9, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Paczkowska, M. Kucia, D. Koziarska et al., “Clinical evidence that very small embryonic-like stem cells are mobilized into peripheral blood in patients after stroke,” Stroke, vol. 40, no. 4, pp. 1237–1244, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Drukała, E. Paczkowska, M. Kucia et al., “Stem cells, including a population of very small embryonic-like stem cells, are mobilized into peripheral blood in patients after skin burn injury,” Stem Cell Reviews and Reports, vol. 8, no. 1, pp. 184–194, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Grymula, M. Tarnowski, K. Piotrowska et al., “Evidence that the population of quiescent bone marrow-residing very small embryonic/epiblast-like stem cells (VSELs) expands in response to neurotoxic treatment,” Journal of Cellular and Molecular Medicine, vol. 18, no. 9, pp. 1797–1806, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. M. de Lisio, J. M. Baker, and G. Parise, “Exercise promotes bone marrow cell survival and recipient reconstitution post-bone marrow transplantation, which is associated with increased survival,” Experimental Hematology, vol. 41, no. 2, pp. 143–154, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. F. MacAluso and K. H. Myburgh, “Current evidence that exercise can increase the number of adult stem cells,” Journal of Muscle Research and Cell Motility, vol. 33, no. 3-4, pp. 187–198, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Fabel, S. A. Wolf, D. Ehninger, H. Babu, P. Leal-Galicia, and G. Kempermann, “Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice,” Frontiers in Neuroscience, vol. 3, article 50, 2009. View at Publisher · View at Google Scholar
  33. T. Snijders, L. B. Verdijk, J. S. Smeets et al., “The skeletal muscle satellite cell response to a single bout of resistance-type exercise is delayed with aging in men,” Age, vol. 36, no. 4, p. 9699, 2014. View at Publisher · View at Google Scholar
  34. S. Borkowska, M. Suszynska, K. Mierzejewska et al., “Novel evidence that crosstalk between the complement, coagulation and fibrinolysis proteolytic cascades is involved in mobilization of hematopoietic stem/progenitor cells (HSPCs),” Leukemia, vol. 28, pp. 2148–2154, 2014. View at Publisher · View at Google Scholar · View at Scopus