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Wharton’s Jelly Derived Mesenchymal Stem Cells: Comparing Human and Horse

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Abstract

Wharton’s jelly (WJ) is an important source of mesenchymal stem cells (MSCs) both in human and other animals. The aim of this study was to compare human and equine WJMSCs. Human and equine WJMSCs were isolated and cultured using the same protocols and culture media. Cells were characterized by analysing morphology, growth rate, migration and adhesion capability, immunophenotype, differentiation potential and ultrastructure. Results showed that human and equine WJMSCs have similar ultrastructural details connected with intense synthetic and metabolic activity, but differ in growth, migration, adhesion capability and differentiation potential. In fact, at the scratch assay and transwell migration assay, the migration ability of human WJMSCs was higher (P < 0.05) than that of equine cells, while the volume of spheroids obtained after 48 h of culture in hanging drop was larger than the volume of equine ones (P < 0.05), demonstrating a lower cell adhesion ability. This can also revealed in the lower doubling time of equine cells (3.5 ± 2.4 days) as compared to human (6.5 ± 4.3 days) (P < 0.05), and subsequently in the higher number of cell doubling after 44 days of culture observed for the equine (20.3 ± 1.7) as compared to human cells (8.7 ± 2.4) (P < 0.05), and to the higher (P < 0.05) ability to form fibroblast colonies at P3. Even if in both species tri-lineage differentiation was achieved, equine cells showed an higher chondrogenic and osteogenic differentiation ability (P < 0.05). Our findings indicate that, although the ultrastructure demonstrated a staminal phenotype in human and equine WJMSCs, they showed different properties reflecting the different sources of MSCs.

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References

  1. Dominici, M., Le Blanc, K., Mueller, I., et al. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8, 315–317.

    Article  PubMed  CAS  Google Scholar 

  2. Vangsness, C. T. Jr., Sternberg, H., & Harris, L. (2015). Umbilical cord tissue offers the greatest number of harvestable mesenchymal stem cells for research and clinical application: a literature review of different harvest sites. Arthroscopy, 31, 1836–1843.

    Article  PubMed  Google Scholar 

  3. Iacono, E., Rossi, B., & Merlo, B. (2015). Stem cells from foetal adnexa and fluid in domestic animals: an update on their features and clinical application. Reproduction in Domestic Animals, 50, 353–364.

    Article  PubMed  CAS  Google Scholar 

  4. Troyer, D. L., & Weiss, M. L. (2008). Wharton’s jelly-derived cells are a primitive stromal cell population. Stem Cells, 26, 591–599.

    Article  PubMed  Google Scholar 

  5. Harding, J., Roberts, R. M., & Mirochnitchenko, O. (2013). Large animal models for stem cell therapy. Stem Cell Research & Therapy, 4, 23.

    Article  Google Scholar 

  6. Rainaldi, G., Pinto, B., Piras, A., Vatteroni, L., Simi, S., & Citti, L. (1991). Reduction of proliferative heterogeneity of CHEF18 Chinese hamster cell line during the progression toward tumorigenicity. In Vitro Cellular & Development Biology, 27, 949–952.

    Article  Google Scholar 

  7. Piccinini, F., Tesei, A., Arienti, C., & Bevilacqua, A. (2015). Cancer multicellular spheroids: volume assessment from a single 2D projection. Computer Methods and Programs in Biomedicine, 118, 95–106.

    Article  PubMed  Google Scholar 

  8. De Schauwer, C., Piepers, S., Van de Walle, G. R., et al. (2012). In search for cross-reactivity to immunophenotype equine mesenchymal stromal cells by multicolor flow cytometry. Cytometry Part A, 81, 312–323.

    Article  Google Scholar 

  9. Ibrahim, S., & Steinbach, F. (2012). Immunoprecipitation of equine CD molecules using anti-human MABs previously analyzed by flow cytometry and immunohistochemistry. Veterinary Immunology and Immunopathology, 145, 7–13.

    Article  PubMed  CAS  Google Scholar 

  10. Iacono, E., Merlo, B., Romagnoli, N., Rossi, B., Ricci, F., & Spadari, A. (2015). Equine bone marrow and adipose tissue mesenchymal stem cells: cytofluorimetric characterization, in vitro differentiation, and clinical application. Journal of Equine Veterinary Science, 35, 130–140.

    Article  Google Scholar 

  11. Patterson-Kane, J. C., Becker, D. L., & Rich, T. (2012). The pathogenesis of tendon microdamage in athletes: the horse as a natural model for basic cellular research. Journal of Comparative Pathology, 147, 227–247.

    Article  PubMed  CAS  Google Scholar 

  12. Smith, R. K. W. (2008). Mesenchymal stem cell therapy for equine tendinopathy. Disability and Rehabilitation, 30, 1752–1758.

    Article  PubMed  Google Scholar 

  13. Crovace, A., Lacitignola, L., Rossi, G., & Francioso, E. (2010). Histological and immunohistochemical evaluation of autologous cultured bone marrow mesenchymal stem cells and bone marrow mononucleated cells in collagenase-induced tendinitis of equine superficial digital flexor tendon. Veterinary Medicine International, 250978.

  14. Godwin, E. E., Young, N. J., Dudhia, J., Beamish, I. C., & Smith, R. K. (2012). Implantation of bone marrow-derived mesenchymal stem cells demonstrates improved outcome in horses with overstrain injury of the superficial digital flexor tendon. Equine Veterinary Journal, 44, 25–32.

    Article  PubMed  CAS  Google Scholar 

  15. Pasquinelli, G., Tazzari, P., Ricci, F., et al. (2007). Ultrastructural characteristics of human mesenchymal stromal (stem) cells derived from bone marrow and term placenta. Ultrastructural Pathology, 31, 23–31.

    Article  PubMed  Google Scholar 

  16. Orsolic, I., Jurada, D., Pullen, N., Oren, M., Eliopoulos, A. G., & Volarevic, S. (2016). The relationship between the nucleolus and cancer: current evidence and emerging paradigms. Seminars in Cancer Biology, 37–38, 36–50.

    Article  PubMed  CAS  Google Scholar 

  17. Pascucci, L., Mercati, F., Marini, C., et al. (2010). Ultrastructural morphology of equine adipose-derived mesenchymal stem cells. Histology and Histopathology, 25, 1277–1285.

    PubMed  Google Scholar 

  18. Teti, G., Cavallo, C., Grigolo, B., et al. (2012). Ultrastructural analysis of human bone marrow mesenchymal stem cells during in vitro osteogenesis and chondrogenesis. Microscopy Research and Technique, 75, 596–604.

    Article  PubMed  Google Scholar 

  19. García-Prat, L., Martínez-Vicente, M., & Muñoz-Cánoves, P. (2016). Autophagy: a decisive process for stemness. Oncotarget, 7, 12286–12288.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Sbrana, F. V., Cortini, M., Avnet, S., et al. (2016). The role of autophagy in the maintenance of stemness and differentiation of mesenchymal stem cells. Stem Cell Reviews, 12, 621–633.

    Article  PubMed  CAS  Google Scholar 

  21. Iacono, E., Brunori, L., Pirrone, A., et al. (2012). Isolation, characterization and differentiation of mesenchymal stem cells from amniotic fluid, umbilical cord blood and Wharton’s jelly in the horse. Reproduction, 143, 455–468.

    Article  PubMed  CAS  Google Scholar 

  22. Mattioli-Belmonte, M., Teti, G., Salvatore, V., et al. (2015). Stem cell origin differently affects bone tissue engineering strategies. Frontiers in Physiology, 6, 266.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Li, G., Zhang, X. A., Wang, H., et al. (2009). Comparative proteomic analysis of mesenchymal stem cells derived from human bone marrow, umbilical cord, and placenta: Implication in the migration. Proteomics, 9, 20–30.

    Article  PubMed  CAS  Google Scholar 

  24. Sart, S., Tsai, A. C., Li, Y., & Ma, T. (2014). Three-dimensional aggregates of mesenchymal stem cells: cellular mechanism, biological properties, and applications. Tissue Engineering Part B Reviews, 20, 365–380.

    Article  PubMed  Google Scholar 

  25. Wang, W., Itaka, K., Ohba, S., et al. (2009). 3D spheroid culture system on micropatterned substrates for improved differentiation efficiency of multipotent mesenchymal stem cells. Biomaterials, 30, 2705–2715.

    Article  PubMed  CAS  Google Scholar 

  26. Suzuki, S., Muneta, T., Tsuji, K., et al. (2012). Properties and usefulness of aggregates of synovial mesenchymal stem cells as a source for cartilage regeneration. Arthritis Research & Therapy, 14, R136.

    Article  CAS  Google Scholar 

  27. Mizuno, H., & Hyakusoku, H. (2003). Mesengenic potential and future clinical perspective of human processed lipospirated cells. Journal of Nippon Medical School, 70, 300–306.

    Article  PubMed  Google Scholar 

  28. Janderova, L., McNeil, M., Murrell, A. N., Mynatt, R. L., & Smith, S. R. (2003). Human mesenchymal stem cells as an in vitro model for human adipogenesis. Obesity Research, 11, 65–74.

    Article  PubMed  CAS  Google Scholar 

  29. De Schauwer, C., Meyer, E., Van de Walle, G. R., & Van Soom, A. (2011). Markers of stemness in equine mesenchymal stem cells: a plea for uniformity. Theriogenology, 75, 1431–1443.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The author wish to thank Mirella Falconi, manager of “Laboratorio di morfologia e biologia cellulare e tissutale” (Department for Biomedical and Neuromotor Sciences). This research was funded by RFO (Ricerca Fondamentale Orientata), University of Bologna.

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Correspondence to Barbara Merlo.

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Merlo, B., Teti, G., Mazzotti, E. et al. Wharton’s Jelly Derived Mesenchymal Stem Cells: Comparing Human and Horse. Stem Cell Rev and Rep 14, 574–584 (2018). https://doi.org/10.1007/s12015-018-9803-3

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  • DOI: https://doi.org/10.1007/s12015-018-9803-3

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