Recent Progress on Skin-Derived Mesenchymal Stem Cells in Pigs

  • Kumar, B. Mohana (Department of OBS/Theriogenology and Biotechnology, College of Veterinary Medicine,Gyeongsang National University) ;
  • Patil, Rajreddy (Department of OBS/Theriogenology and Biotechnology, College of Veterinary Medicine,Gyeongsang National University) ;
  • Lee, Sung-Lim (Department of OBS/Theriogenology and Biotechnology, College of Veterinary Medicine,Gyeongsang National University) ;
  • Rho, Gyu-Jin (Department of OBS/Theriogenology and Biotechnology, College of Veterinary Medicine,Gyeongsang National University)
  • Received : 2012.12.14
  • Accepted : 2012.12.14
  • Published : 2012.12.31

Abstract

Skin serves as an easily accessible source of multipotent stem cells with potential for cellular therapies. In pigs, stem cells from skin tissues of fetal and adult origins have been demonstrated as either floating spheres (cell aggregates) or adherent spindle-shaped mesenchymal stem cell (MSC)-like cells depending on culture conditions. The cells isolated from the epidermis and dermis of porcine skin showed plastic adherent growth in the presence of serum and positively expressed a range of surface and intracellular markers that are considered to be specific for MSCs. The properties of primitive stem cells have been observed with the expression of alkaline phosphatase and markers related to pluripotency. Further, studies have shown the ability of skin-derived MSCs to differentiate in vitro along mesodermal, neuronal and germ-line lineages. Moreover, preclinical studies have also been performed to assess their in vivo potential, and the findings appear to be effective in tissue regeneration at the defected site after transplantation. The present review describes the recent progress on the biological features of porcine skin-derived MSCs as adherent cells, and summarizes their potential in advancing stem cell based therapies.

Keywords

References

  1. Barnabé GF, Schwindt TT, Calcagnotto ME, Motta FL, Martinez G Jr, de Olivera AC, Keim LM, D'Almeida V, Mendez-Otero R, Mello LE (2009): Chemically- induced RAT mesenchymal stem cells adopt molecular properties of neuron-like cells but do not have basic neuronal functional properties. PLoS ONE 4:e5222. https://doi.org/10.1371/journal.pone.0005222
  2. Bosch P, Pratt SL, Stice SL (2006): Isolation, characterization, gene modification, and nuclear reprogramming of porcine mesenchymal stem cells. Biol Reprod 74:46-57.
  3. Carlin R, Davis D, Weiss M, Schultz B, Troyer D (2006): Expression of early transcription factors Oct-4, Sox-2 and Nanog by porcine umbilical cord (PUC) matrix cells. Reprod Biol Endocrinol 4:8. https://doi.org/10.1186/1477-7827-4-8
  4. Carpenter JE, Hankenson KD (2004): Animal models of tendon and ligament injuries for tissue engineering applications. Biomaterials 25:1715-1722. https://doi.org/10.1016/S0142-9612(03)00507-6
  5. Chen J, Lu Z, Cheng D, Peng S, Wang H (2011): Isolation and characterization of porcine amniotic fluid- derived multipotent stem cells. PLoS ONE 6:e-19964.
  6. Danner S, Kajahn J, Klink E, Kruse C (2007): Derivation of oocyte-like cells from a clonal pancreatic stem cell line. Mol Hum Reprod 13:11-20.
  7. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E (2006): Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315-317. https://doi.org/10.1080/14653240600855905
  8. Dyce PW, Zhu H, Craig J, Li J (2004): Stem cells with multilineage potential derive from porcine skin. Biochem Biophys Res Commun 316:651-658. https://doi.org/10.1016/j.bbrc.2004.02.093
  9. Dyce PW, Wen L, Li J (2006): In vitro germline potential of stem cells derived from fetal porcine skin. Nat Cell Biol 8:384-390. https://doi.org/10.1038/ncb1388
  10. Dyce PW, Shen W, Huynh E, Shao H, Villagómez DA, Kidder GM, King WA, Li J (2011): Analysis of oocyte-like cells differentiated from porcine fetal skinderived stem cells. Stem Cells Dev 20:809-819. https://doi.org/10.1089/scd.2010.0395
  11. Faast R, Harrison SJ, Beebe LF, McIlfatrick SM, Ashman RJ, Nottle MB (2006): Use of adult mesenchymal stem cells isolated from bone marrow and blood for somatic cell nuclear transfer in pigs. Cloning Stem Cells 8:166-173. https://doi.org/10.1089/clo.2006.8.166
  12. Gregory CA, Prockup DJ, Spees JL (2005): Non-hematopoietic bone marrow stem cells: Molecular control of expansion and differentiation. Exp Cell Res 306:330-335. https://doi.org/10.1016/j.yexcr.2005.03.018
  13. Huang T, He D, Kleiner G, Kuluz J (2007): Neuron- like differentiation of adipose-derived stem cells from infant piglets in vitro. J Spinal Cord Med 30 (Suppl 1):S35-40.
  14. Johnson J, Bagley J, Skaznik-Wikiel M, Lee HJ, Adams GB, Niikura Y, Tschudy KS, Tilly JC, Cortes ML, Forkert R, Spitzer T, Iacomini J, Scadden DT, Tilly JL (2005): Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell 122:303-315. https://doi.org/10.1016/j.cell.2005.06.031
  15. Kang EJ, Byun JH, Choi YJ, Maeng GH, Lee SL, Kang DH, Lee JS, Rho GJ, Park BW (2010): In vitro and in vivo osteogenesis of porcine skin-derived mesenchymal stem cell-like cells with a demineralized bone and fibrin scaffold. Tissue Eng Part A 16:815-827. https://doi.org/10.1089/ten.tea.2009.0439
  16. Kang EJ, Lee YH, Kim MJ, Lee YM, Kumar BM, Jeon BG, Ock SA, Kim HJ, Rho GJ (2011): Transplantation of porcine umbilical cord matrix mesenchymal stem cells in a mouse model of Parkinson's disease. J Tissue Eng Regen Med. doi: 10.1002/term.504. [Epub ahead of print].
  17. Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, Gudas LJ, Mongan NP (2009): Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the Nanog, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 18:1093-1108. https://doi.org/10.1089/scd.2009.0113
  18. Kellner S, Kikyo N (2010): Transcriptional regulation of the Oct4 gene, a master gene for pluripotency. Histol Histopathol 25:405-412.
  19. Kues WA, Petersen B, Mysegades W, Carnwath JW, Niemann H (2005): Isolation of murine and porcine fetal stem cells from somatic tissue. Biol Reprod 72: 1020-1028. https://doi.org/10.1095/biolreprod.104.031229
  20. Kumar BM, Yoo JG, Ock SA, Kim JG, Song HJ, Kang EJ, Cho SK, Lee SL, Cho JH, Balasubramanian S, Rho GJ (2007): In vitro differentiation of mesenchymal progenitor cells derived from porcine umbilical cord blood. Molecules and Cells 24, 343-350.
  21. Kumar BM, Maeng GH, Lee YM, Kim TH, Lee JH, Jeon BG, Ock SA, Yoo JG, Rho GJ (2012): Neurogenic and cardiomyogenic differentiation of mesenchymal stem cells isolated from minipig bone marrow. Res Vet Sci 93:749-757. https://doi.org/10.1016/j.rvsc.2011.09.012
  22. Lermen D, Gorjup E, Dyce PW, von Briesen H, Muller P (2010): Neuro-muscular differentiation of adult porcine skin derived stem cell-like cells. PLoS ONE 5:e8968. https://doi.org/10.1371/journal.pone.0008968
  23. Linher K, Dyce P, Li J (2009): Primordial germ celllike cells differentiated in vitro from skin-derived stem cells. PLoS ONE 4:e8263. https://doi.org/10.1371/journal.pone.0008263
  24. Lorenz K, Sicker M, Schmelzer E, Rupf T, Salvetter J, Schulz-Siegmund M, Bader A (2008): Multilineage differentiation potential of human dermal skin-derived fibroblasts. Exp Dermatol 17:925-932. https://doi.org/10.1111/j.1600-0625.2008.00724.x
  25. Moscoso I, Centeno A, Lopez E, Rodriguez-Barbosa JI, Santamarina I, Filgueira P, Sanchez MJ, Dominguez- Perles R, Penuelas-Rivas G, Domenech N (2005): Differentiation in vitro of primary and immortalized porcine mesenchymal stem cells into cardiomyocytes for cell transplantation. Transplant Proc 37:481-482. https://doi.org/10.1016/j.transproceed.2004.12.247
  26. Ock SA, Jeon BG, Rho GJ (2010): Comparative characterization of porcine mesenchymal stem cells derived from bone marrow extract and skin tissues. Tissue Eng Part C Methods 16:1481-1491. https://doi.org/10.1089/ten.tec.2010.0149
  27. Park BW, Kang DH, Kang EJ, Byun JH, Lee JS, Maeng GH, Rho GJ (2012): Peripheral nerve regeneration using autologous porcine skin-derived mesenchymal stem cells. J Tissue Eng Regen Med 6:113-124. https://doi.org/10.1002/term.404
  28. Rho GJ, Kumar BM, Balasubramanian S (2009): Porcine mesenchymal stem cells- Current technological status and future perspective. Front Biosci 14:3942-3961.
  29. Ringe J, Kaps C, Schmitt B, Buscher K, Bartel J, Smolian H, Schultz O, Burmester GR, Haupl T, Sittinger M (2002): Porcine mesenchymal stem cells- Induction of distinct mesenchymal cell lineages. Cell Tissue Res 307:321-327. https://doi.org/10.1007/s00441-002-0525-z
  30. Shukla D, Box GN, Edwards RA, Tyson DR (2008): Bone marrow stem cells for urologic tissue engineering. World J Urol 26:341-349. https://doi.org/10.1007/s00345-008-0311-y
  31. Song SH, Kumar BM, Kang EJ, Lee YM, Kim TH, Ock SA, Lee SL, Jeon BG, Rho GJ (2011): Characterization of porcine multipotent stem/stromal cells derived from skin, adipose, and ovarian tissues and their differentiation in vitro into putative oocyte-like cells. Stem Cells Dev 20:1359-1370. https://doi.org/10.1089/scd.2010.0203
  32. Toma JG, Akhavan M, Fernandes KJ, Barnabé-Heider F, Sadikot A, Kaplan DR, Miller FD (2001): Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3:778-784. https://doi.org/10.1038/ncb0901-778
  33. Toma JG, McKenzie IA, Bagli D, Miller FD (2005): Isolation and characterization of multipotent skinderived precursors from human skin. Stem Cells 23:727-737. https://doi.org/10.1634/stemcells.2004-0134
  34. Vishnubalaji R, Al-Nbaheen M, Kadalmani B, Aldahmash A, Ramesh T (2012): Skin-derived multipotent stromal cells-an archrival for mesenchymal stem cells. Cell Tissue Res 350:1-12. https://doi.org/10.1007/s00441-012-1471-z
  35. Wang X, Dai J (2010): Isoforms of Oct4 contribute to the confusing diversity in stem cell biology. Stem Cells 28:885-893.
  36. Woodbury D, Reynolds K, Black IB (2002): Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal gene prior to neurogenesis. J Neurosci Res 96:908-917.
  37. Zhao M, Isom SC, Lin H, Hao Y, Zhang Y, Zhao J, Whyte JJ, Dobbs KB, Prather RS (2009): Tracing the stemness of porcine skin-derived progenitors (pSKP) back to specific marker gene expression. Cloning Stem Cells 11:111-122. https://doi.org/10.1089/clo.2008.0071
  38. Zhao MT, Prather RS (2011): The multi-potentiality of skin-derived stem cells in pigs. Theriogenology 75:1372-1380. https://doi.org/10.1016/j.theriogenology.2010.06.010