Research Article
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Pilot study on cardiogenic differentiation capability of rabbit mesenchymal stem cells

Year 2020, , 407 - 412, 01.09.2020
https://doi.org/10.33988/auvfd.682682

Abstract

Cardiovascular diseases are still one of the most common reasons for mortality in humans. Mesenchymal stem cells (MSCs) are preferable in cardiac regeneration cell-based therapies because of their allogeneic and high proliferative potential. The electrophysiological properties of the rabbit heard is closer to human than the mouse. The current study aimed to trace mRNA expression changes of two stemness/cardiogenic differentiation ability-related transcriptionala factors OCT4 and GATA4 in rabbit MSCs during early stages of induced cardiomyocyte differentiation in vitro. The mesenchymal stem cell originated from different anatomical areas-subcutaneous, visceral, bone marrow and pericardial tissue. The cardiac differentiation protocol for mouse embryonic stem cells in hanging drop was adopted in rabbit MSCs. The best formed embryonal bodies (EBs) like structures were collected and cultivated on gelatin-coated plates. The total mRNA was obtained before cardiac differentiation and on the 6th day after it. SYBER based real-time PCR was performed to evaluate the mRNA expression fold-changes of OCT4 and GATA4. The cultivation of MSCs in hanging drops during cardiac differentiation induced EBs formation, without any contractile activity up to the 6th day of the differentiation in all cell types. The applied differentiation protocol significantly downregulated GATA4 expression in ADSCs - EBs, while in BMSCs, both target genes were significantly upregulated. In conclusion, the adopted cardiac differentiation protocol from mouse embryonic stem cells could be a useful approach for rabbit bone marrow mesenchymal stem cells. Since the rest of the cells revealed weak cardiogenic capability at this early stage, some modifications of induction protocols should be considered.

References

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  • 3. Baer PC, Geiger H (2012): Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells Int, 2012, 812693.
  • 4. Baer PC, Griesche N, Luttmann W, et al (2010): Human adipose-derived mesenchymal stem cells in vitro: evaluation of an optimal expansion medium preserving stemness. Cytotherapy, 12, 96-106.
  • 5. Burridge P, Keller G, Gold JD, et al (2012): Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell, 10, 16-28.
  • 6. Choi YS, Dusting GJ, Stubbs S, et al (2010): Differentiation of human adipose-derived stem cells into beating cardiomyocytes. J Cell Mol Med, 14, 878-889.
  • 7. Conrad C, Huss R (2005): Adult stem cell lines in regenerative medicine and reconstructive surgery. J Surg Res, 124, 201-208.
  • 8. Dulak J, Szade K, Szade A, et al (2015): Adult stem cells: hopes and hypes of regenerative medicine. Acta Biochim Pol, 62, 329-37
  • 9. Ejaz A, Hatzmann FM, Hammerle S, et al (2019): Fibroblast feeder layer supports adipogenic differentiation of human adipose stromal/progenitor cells. Adipocyte, 8, 178-189.
  • 10. Ferroni L, Gardin C, Bellin G, et al (2019): Bovine pericardium membrane as new tool for mesenchymal stem cells commitment. J Tissue Eng Regen Med, 13, 1805-1814.
  • 11. Gaetani R, Yin C, Srikumar N, et al (2016): Cardiac-derived extracellular matrix enhances cardiogenic properties of human cardiac progenitor cells. Cell Transplantation, 25, 1653-1663.
  • 12. Greco SJ, Liu K, Rameshwar P (2007): Functional similarities among genes regulated by OCT4 in human mesenchymal and embryonic stem cells. Stem Cells, 25, 3143-3154.
  • 13. Iacobellis G, Corradi D, Sharma AM (2005): Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nature Clinical Practice Cardiovascular Medicine, 2, 5365-43.
  • 14. Khorramirouz R, Go JL, Noble C, et al (2019): In vivo response of acellular porcine pericardial for tissue engineered transcatheter aortic valves. Sci Rep, 9, 1094.
  • 15. Kocan B, Maziarz A, Tabarkiewicz J, et al (2017): Trophic activity and phenotype of adipose tissue-derived mesenchymal stem cells as a background of their regenerative potential. Stem Cells Int, 2017, 1653254.
  • 16. Ladage D, Turnbull IC, Ishikawa K, et al (2011): Delivery of gelfoam-enabled cells and vectors into the pericardial space using a percutaneous approach in a porcine model. Gene Therapy, 18, 979-985.
  • 17. Limana F, Bertolami C, Mangoni A, et al (2010): Myocardial infarction induces embryonic reprogramming of epicardial c-kit(+) cells: role of the pericardial fluid. J Mol Cell Cardiol, 48, 609-618.
  • 18. Major P, Baczkó I, Hiripi L, et al (2016): A novel transgenic rabbit model with reduced repolarization reserve: long QT syndrome caused by a dominant-negative mutation of the KCNE1 gene. B J Pharmacol, 173, 2046-61.
  • 19. Maraghechi P, Hiripi L, Tóth G, et al (2013): Discovery of pluripotency-associated microRNAs in rabbit preimplantation embryos and embryonic stem-like cells. Reproduction, 145, 421-37.
  • 20. Minteer D, Marra KG, Rubin JP (2013): Adipose-derived mesenchymal stem cells: biology and potential applications. Adv Biochem Eng Biotechnol, 129, 59-71.
  • 21. Naderi N, Combellack EJ, Griffin M, et al (2017): The regenerative role of adipose‐derived stem cells (ADSC) in plastic and reconstructive surgery. Int Wound J, 14, 112-124.
  • 22. Navarrete SA, Ramin N, Tonack S, et al (2008): Cell lineagespecific signaling of insulin and insulin-like growth factor I in rabbit blastocysts. Endocrinology, 149, 515–524.
  • 23. Nerbonne JM (2004): Studying cardiac arrhythmias in the mouse—a reasonable model for probing mechanisms? Trends Cardiovasc Med, 14, 83-93.
  • 24. Nerbonne JM, Kass RS (2005): Molecular physiology of cardiac repolarization. Physiol Rev, 85, 1205-1253.
  • 25. Pekkanen-Mattila M, Ojala M, Kerkelä E, et al (2012): The effect of human and mouse fibroblast feeder cells on cardiac differentiation of human pluripotent stem cells. Stem Cells Int, 2012, 875059.
  • 26. Perrino C, Rockman HA (2006): GATA4 and the two sides of gene expression reprogramming. Circ Res, 98, 715-6.
  • 27. Pierantozzi E, Gava B, Manini I, et al (2011): Pluripotency regulators in human mesenchymal stem cells: expression of NANOG but not of OCT-4 and SOX-2. Stem Cells, 20, 915-23.
  • 28. Sacks HS, Fain JN (2007): Human epicardial adipose tissue: a review. Am Heart J, 153, 907-917.
  • 29. Sanina C, Hare JM (2015): Mesenchymal stem cells as a biological drug for heart disease: where are we with cardiac cell-based therapy? Circ Res, 117, 229-233.
  • 30. Vachkova E, Bosnakovski D, Yonkova P, et al (2016): Adipogenic potential of stem cells derived from rabbit subcutaneous and visceral adipose tissue in vitro. In Vitro Cell Dev Biol Anim, 52, 829-837.
  • 31. Wobus AM, Holzhausen H, Jäkel P, et al (1984): Characterization of a pluripotent stem cell line derived from a mouse embryo. Exp Cell Res, 152, 212-219.
  • 32. Wystrychowski W, Patlolla B, Zhuge Y, et al (2016): Multipotency and cardiomyogenic potential of human adipose-derived stem cells from epicardium, pericardium, and omentum. Stem Cell Res Ther, 7, 84.
  • 33. Yannarelli G, Pacienza N, Montanari S, et al (2017): OCT4 expression mediates partial cardiomyocyte reprogramming of mesenchymal stromal cells. PLoS One, 12, 1-20.
  • 34. Zhang J, Wu Z, Fan Z, et al (2018): Pericardial application as a new route for implanting stem-cell cardiospheres to treat myocardial infarction. J Physiol, 596, 2037-2054.
  • 35. Zhang Y, Wu J, King JH, et al (2014): Measurement and interpretation of electrocardiographic QT intervals in murine hearts. Am J Physiol Heart Circ Physiol, 306, 1553-1557.
  • 36. Zhu Y, Liu T, Song K, et al (2008): Adipose-derived stem cell: a better stem cell than BMSC. Cell Res, 18, 165.
Year 2020, , 407 - 412, 01.09.2020
https://doi.org/10.33988/auvfd.682682

Abstract

References

  • 1. Anonymous (2017):World Health Organization (WHO). Available at: https://www.who.int/en/news-room/fact-sheets/detail/cardiovascular-diseases-(cvds). (Accessed 17 May 2017).
  • 2. Baer PC (2014): Adipose-derived mesenchymal stromal/stem cells: An update on their phenotype in vivo and in vitro. World J Stem Cells, 6, 256-65.
  • 3. Baer PC, Geiger H (2012): Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells Int, 2012, 812693.
  • 4. Baer PC, Griesche N, Luttmann W, et al (2010): Human adipose-derived mesenchymal stem cells in vitro: evaluation of an optimal expansion medium preserving stemness. Cytotherapy, 12, 96-106.
  • 5. Burridge P, Keller G, Gold JD, et al (2012): Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell, 10, 16-28.
  • 6. Choi YS, Dusting GJ, Stubbs S, et al (2010): Differentiation of human adipose-derived stem cells into beating cardiomyocytes. J Cell Mol Med, 14, 878-889.
  • 7. Conrad C, Huss R (2005): Adult stem cell lines in regenerative medicine and reconstructive surgery. J Surg Res, 124, 201-208.
  • 8. Dulak J, Szade K, Szade A, et al (2015): Adult stem cells: hopes and hypes of regenerative medicine. Acta Biochim Pol, 62, 329-37
  • 9. Ejaz A, Hatzmann FM, Hammerle S, et al (2019): Fibroblast feeder layer supports adipogenic differentiation of human adipose stromal/progenitor cells. Adipocyte, 8, 178-189.
  • 10. Ferroni L, Gardin C, Bellin G, et al (2019): Bovine pericardium membrane as new tool for mesenchymal stem cells commitment. J Tissue Eng Regen Med, 13, 1805-1814.
  • 11. Gaetani R, Yin C, Srikumar N, et al (2016): Cardiac-derived extracellular matrix enhances cardiogenic properties of human cardiac progenitor cells. Cell Transplantation, 25, 1653-1663.
  • 12. Greco SJ, Liu K, Rameshwar P (2007): Functional similarities among genes regulated by OCT4 in human mesenchymal and embryonic stem cells. Stem Cells, 25, 3143-3154.
  • 13. Iacobellis G, Corradi D, Sharma AM (2005): Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nature Clinical Practice Cardiovascular Medicine, 2, 5365-43.
  • 14. Khorramirouz R, Go JL, Noble C, et al (2019): In vivo response of acellular porcine pericardial for tissue engineered transcatheter aortic valves. Sci Rep, 9, 1094.
  • 15. Kocan B, Maziarz A, Tabarkiewicz J, et al (2017): Trophic activity and phenotype of adipose tissue-derived mesenchymal stem cells as a background of their regenerative potential. Stem Cells Int, 2017, 1653254.
  • 16. Ladage D, Turnbull IC, Ishikawa K, et al (2011): Delivery of gelfoam-enabled cells and vectors into the pericardial space using a percutaneous approach in a porcine model. Gene Therapy, 18, 979-985.
  • 17. Limana F, Bertolami C, Mangoni A, et al (2010): Myocardial infarction induces embryonic reprogramming of epicardial c-kit(+) cells: role of the pericardial fluid. J Mol Cell Cardiol, 48, 609-618.
  • 18. Major P, Baczkó I, Hiripi L, et al (2016): A novel transgenic rabbit model with reduced repolarization reserve: long QT syndrome caused by a dominant-negative mutation of the KCNE1 gene. B J Pharmacol, 173, 2046-61.
  • 19. Maraghechi P, Hiripi L, Tóth G, et al (2013): Discovery of pluripotency-associated microRNAs in rabbit preimplantation embryos and embryonic stem-like cells. Reproduction, 145, 421-37.
  • 20. Minteer D, Marra KG, Rubin JP (2013): Adipose-derived mesenchymal stem cells: biology and potential applications. Adv Biochem Eng Biotechnol, 129, 59-71.
  • 21. Naderi N, Combellack EJ, Griffin M, et al (2017): The regenerative role of adipose‐derived stem cells (ADSC) in plastic and reconstructive surgery. Int Wound J, 14, 112-124.
  • 22. Navarrete SA, Ramin N, Tonack S, et al (2008): Cell lineagespecific signaling of insulin and insulin-like growth factor I in rabbit blastocysts. Endocrinology, 149, 515–524.
  • 23. Nerbonne JM (2004): Studying cardiac arrhythmias in the mouse—a reasonable model for probing mechanisms? Trends Cardiovasc Med, 14, 83-93.
  • 24. Nerbonne JM, Kass RS (2005): Molecular physiology of cardiac repolarization. Physiol Rev, 85, 1205-1253.
  • 25. Pekkanen-Mattila M, Ojala M, Kerkelä E, et al (2012): The effect of human and mouse fibroblast feeder cells on cardiac differentiation of human pluripotent stem cells. Stem Cells Int, 2012, 875059.
  • 26. Perrino C, Rockman HA (2006): GATA4 and the two sides of gene expression reprogramming. Circ Res, 98, 715-6.
  • 27. Pierantozzi E, Gava B, Manini I, et al (2011): Pluripotency regulators in human mesenchymal stem cells: expression of NANOG but not of OCT-4 and SOX-2. Stem Cells, 20, 915-23.
  • 28. Sacks HS, Fain JN (2007): Human epicardial adipose tissue: a review. Am Heart J, 153, 907-917.
  • 29. Sanina C, Hare JM (2015): Mesenchymal stem cells as a biological drug for heart disease: where are we with cardiac cell-based therapy? Circ Res, 117, 229-233.
  • 30. Vachkova E, Bosnakovski D, Yonkova P, et al (2016): Adipogenic potential of stem cells derived from rabbit subcutaneous and visceral adipose tissue in vitro. In Vitro Cell Dev Biol Anim, 52, 829-837.
  • 31. Wobus AM, Holzhausen H, Jäkel P, et al (1984): Characterization of a pluripotent stem cell line derived from a mouse embryo. Exp Cell Res, 152, 212-219.
  • 32. Wystrychowski W, Patlolla B, Zhuge Y, et al (2016): Multipotency and cardiomyogenic potential of human adipose-derived stem cells from epicardium, pericardium, and omentum. Stem Cell Res Ther, 7, 84.
  • 33. Yannarelli G, Pacienza N, Montanari S, et al (2017): OCT4 expression mediates partial cardiomyocyte reprogramming of mesenchymal stromal cells. PLoS One, 12, 1-20.
  • 34. Zhang J, Wu Z, Fan Z, et al (2018): Pericardial application as a new route for implanting stem-cell cardiospheres to treat myocardial infarction. J Physiol, 596, 2037-2054.
  • 35. Zhang Y, Wu J, King JH, et al (2014): Measurement and interpretation of electrocardiographic QT intervals in murine hearts. Am J Physiol Heart Circ Physiol, 306, 1553-1557.
  • 36. Zhu Y, Liu T, Song K, et al (2008): Adipose-derived stem cell: a better stem cell than BMSC. Cell Res, 18, 165.
There are 36 citations in total.

Details

Primary Language English
Subjects Veterinary Surgery
Journal Section Research Article
Authors

Natalia Grıgorova 0000-0001-5749-7773

Elen Gócza 0000-0001-7720-4720

Ekaterina Vachkova 0000-0002-9291-332X

Publication Date September 1, 2020
Published in Issue Year 2020

Cite

APA Grıgorova, N., Gócza, E., & Vachkova, E. (2020). Pilot study on cardiogenic differentiation capability of rabbit mesenchymal stem cells. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 67(4), 407-412. https://doi.org/10.33988/auvfd.682682
AMA Grıgorova N, Gócza E, Vachkova E. Pilot study on cardiogenic differentiation capability of rabbit mesenchymal stem cells. Ankara Univ Vet Fak Derg. September 2020;67(4):407-412. doi:10.33988/auvfd.682682
Chicago Grıgorova, Natalia, Elen Gócza, and Ekaterina Vachkova. “Pilot Study on Cardiogenic Differentiation Capability of Rabbit Mesenchymal Stem Cells”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 67, no. 4 (September 2020): 407-12. https://doi.org/10.33988/auvfd.682682.
EndNote Grıgorova N, Gócza E, Vachkova E (September 1, 2020) Pilot study on cardiogenic differentiation capability of rabbit mesenchymal stem cells. Ankara Üniversitesi Veteriner Fakültesi Dergisi 67 4 407–412.
IEEE N. Grıgorova, E. Gócza, and E. Vachkova, “Pilot study on cardiogenic differentiation capability of rabbit mesenchymal stem cells”, Ankara Univ Vet Fak Derg, vol. 67, no. 4, pp. 407–412, 2020, doi: 10.33988/auvfd.682682.
ISNAD Grıgorova, Natalia et al. “Pilot Study on Cardiogenic Differentiation Capability of Rabbit Mesenchymal Stem Cells”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 67/4 (September 2020), 407-412. https://doi.org/10.33988/auvfd.682682.
JAMA Grıgorova N, Gócza E, Vachkova E. Pilot study on cardiogenic differentiation capability of rabbit mesenchymal stem cells. Ankara Univ Vet Fak Derg. 2020;67:407–412.
MLA Grıgorova, Natalia et al. “Pilot Study on Cardiogenic Differentiation Capability of Rabbit Mesenchymal Stem Cells”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 67, no. 4, 2020, pp. 407-12, doi:10.33988/auvfd.682682.
Vancouver Grıgorova N, Gócza E, Vachkova E. Pilot study on cardiogenic differentiation capability of rabbit mesenchymal stem cells. Ankara Univ Vet Fak Derg. 2020;67(4):407-12.