International Journal of Hematology

, Volume 90, Issue 2, pp 261–269 | Cite as

Comparison of mesenchymal stem cells derived from arterial, venous, and Wharton’s jelly explants of human umbilical cord

  • Ikuo Ishige
  • Tokiko Nagamura-Inoue
  • Masaki J. Honda
  • Ratanakanit Harnprasopwat
  • Michiko Kido
  • Mitsuhiro Sugimoto
  • Hiromitsu Nakauchi
  • Arinobu Tojo
Original Article

Abstract

We isolated mesenchymal stem cells (MSC) from arteries (UCA), veins (UCV), and Wharton’s jelly (UCWJ) of human umbilical cords (UC) and determined their relative capacities for sustained proliferation and multilineage differentiation. Individual UC components were dissected, diced into 1–2 mm³ fragments, and aligned in explant cultures from which migrating cells were isolated using trypsinization. Preparations from 13 UCs produced 13 UCWJ, 11 UCV, and 10 UCA cultures of fibroblast-like, spindle-shaped cells negative for CD31, CD34, CD45, CD271, and HLA-class II, but positive for CD13, CD29, CD44, CD73, CD90, CD105, and HLA-class I. UCV cells exhibited a significantly higher frequency of colony-forming units fibroblasts than did UCWJ and UCA cells. Individual MSCs could be selectively differentiated into osteoblasts, chondrocytes, and adipocytes. When compared for osteogenic potential, UCWJ cells were the least effective precursors, whereas UCA-derived cells developed alkaline phosphatase activity with or without an osteogenic stimulus. UC components, especially blood vessels, could provide a promising source of MSCs with important clinical applications.

Keywords

Umbilical cord Mesenchymal stem cells Human Wharton's jelly Explants 

References

  1. 1.
    Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–7.PubMedCrossRefGoogle Scholar
  2. 2.
    Gang EJ, Jeong JA, Hong SH, Hwang SH, Kim SW, Yang IH, et al. Skeletal myogenic differentiation of mesenchymal stem cells isolated from human umbilical cord blood. Stem Cells. 2004;22:617–24.PubMedCrossRefGoogle Scholar
  3. 3.
    Rangappa S, Fen C, Lee EH, Bongso A, Sim EK. Transformation of adult mesenchymal stem cells isolated from the fatty tissue into cardiomyocytes. Ann Thorac Surg. 2003;75:775–9.PubMedCrossRefGoogle Scholar
  4. 4.
    Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, et al. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol. 2000;164:247–56.PubMedCrossRefGoogle Scholar
  5. 5.
    Le Blanc K, Rasmusson I, Sundberg B, Götherström C, Hassan M, Uzunel M, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet. 2004;363:1439–41.PubMedCrossRefGoogle Scholar
  6. 6.
    Frank MH, Sayegh MH. Immunomodulatory functions of mesenchymal stem cells. Lancet. 2004;363:1411–2.PubMedCrossRefGoogle Scholar
  7. 7.
    Mueller SM, Glowacki J. Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J Cell Biochem. 2001;82:583–90.PubMedCrossRefGoogle Scholar
  8. 8.
    Barry FP. Biology and clinical applications of mesenchymal stem cells. Birth Defects Res C Embryo Today. 2003;69:250–6.PubMedCrossRefGoogle Scholar
  9. 9.
    Yen BL, Chien CC, Chen YC, Chen JT, Huang JS, Lee FK, et al. Placenta-derived multipotent cells differentiate into neuronal and glial cells in vitro. Tissue Eng Part A. 2008;14:9–17.PubMedCrossRefGoogle Scholar
  10. 10.
    Hu Y, Liao L, Wang Q, Ma L, Ma G, Jiang X, et al. Isolation and identification of mesenchymal stem cells from human fetal pancreas. J Lab Clin Med. 2003;141:342–9.PubMedCrossRefGoogle Scholar
  11. 11.
    In ‘t Anker PS, Scherjon SA, Kleijburg-van der Keur C, de Groot-Swings GM, Claas FH, Fibbe WE, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells. 2004;22:1338–45.PubMedCrossRefGoogle Scholar
  12. 12.
    In ‘t Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, van Bezooijen RL, et al. Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica. 2003;88:845–52.PubMedGoogle Scholar
  13. 13.
    Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood. 2004;103:1669–75.PubMedCrossRefGoogle Scholar
  14. 14.
    Romanov YA, Svintsitskaya VA, Smirnov VN. Searching for alternative sources of postnatal human mesenchymal stem cells: candidate MSC-like cells from umbilical cord. Stem Cells. 2003;21:105–10.PubMedCrossRefGoogle Scholar
  15. 15.
    Mareschi K, Biasin E, Piacibello W, Aglietta M, Madon E, Fagioli F. Isolation of human mesenchymal stem cells: bone marrow versus umbilical cord blood. Haematologica. 2001;86:1099–100.PubMedGoogle Scholar
  16. 16.
    Secco M, Zucconi E, Vieira NM, Fogaça LL, Cerqueira A, Carvalho MD, et al. Multipotent stem cells from umbilical cord: cord is richer than blood. Stem Cells. 2008;26:146–50.PubMedCrossRefGoogle Scholar
  17. 17.
    Wang HS, Hung SC, Peng ST, Huang CC, Wei HM, Guo YJ, et al. Mesenchymal stem cells in the Wharton’s jelly of the human umbilical cord. Stem Cells. 2004;22:1330–7.PubMedCrossRefGoogle Scholar
  18. 18.
    Sarugaser R, Lickorish D, Baksh D, Hosseini MM, Davies JE. Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells. 2005;23:220–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Ingram DA, Mead LE, Tanaka H, Meade V, Fenoglio A, Mortell K, et al. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood. 2004;104:2752–60.PubMedCrossRefGoogle Scholar
  20. 20.
    Lu LL, Liu YJ, Yang SG, Zhao QJ, Wang X, Gong W, et al. Isolation and characterization of human umbilical cord mesenchymal stem cells with hematopoiesis-supportive function and other potentials. Haematologica. 2006;91:1017–26.PubMedGoogle Scholar
  21. 21.
    Mwale F, Stachura D, Roughley P, Antoniou J. Limitations of using aggrecan and type X collagen as markers of chondrogenesis in mesenchymal stem cell differentiation. J Orthop Res. 2006;24:1791–8.PubMedCrossRefGoogle Scholar
  22. 22.
    Honda MJ, Shinohara Y, Sumita Y, Tonomura A, Kagami H, Ueda M. Shear stress facilitates tissue-engineered odontogenesis. Bone. 2006;39:125–33.PubMedCrossRefGoogle Scholar
  23. 23.
    Sumita Y, Honda MJ, Ohara T, Tsuchiya S, Sagara H, Kagami H, et al. Performance of collagen sponge as a 3-D scaffold for tooth-tissue engineering. Biomaterials. 2006;27:3238–48.PubMedCrossRefGoogle Scholar
  24. 24.
    Wharton TW. Adenographia. Translated by S. Freer. Oxford: Oxford Press; 1996. p. 242–8.Google Scholar
  25. 25.
    McElreavey KD, Irvine AI, Ennis KT, McLean WH. Isolation, culture and characterisation of fibroblast-like cells derived from the Wharton’s jelly portion of human umbilical cord. Biochem Soc Trans. 1991;19:29S.PubMedGoogle Scholar
  26. 26.
    Nanaev AK, Kohnen G, Milovanov AP, Domogatsky SP, Kaufmann P. Stromal differentiation and architecture of the human umbilical cord. Placenta. 1997;18:53–64.PubMedCrossRefGoogle Scholar
  27. 27.
    Naughton BA, San Roma J, Liu K. Cells isolated from Wharton’s jelly of the human umbilical cord develop a cartilage phenotype when treated with TGFβ in vitro. FASEB J. 1997;11:A19.Google Scholar
  28. 28.
    Mitchell KE, Weiss ML, Mitchell BM, Martin P, Davis D, Morales L, et al. Matrix cells from Wharton’s jelly form neurons and glia. Stem Cells. 2003;21:50–60.PubMedGoogle Scholar
  29. 29.
    Fauran-Clavel MJ, Oustrin J. Alkaline phosphatase and bone calcium parameters. Bone. 1986;7:95–9.PubMedCrossRefGoogle Scholar
  30. 30.
    Baksh D, Yao R, Tuan RS. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells. 2007;25:1384–92.PubMedCrossRefGoogle Scholar
  31. 31.
    Ushiki T, Abe K. Identification of arterial and venous segments of blood vessels using alkaline phosphatase staining of ink/gelatin injected tissues. Arch Histol Cytol. 1998;61:215–9.PubMedCrossRefGoogle Scholar
  32. 32.
    Rubio D, Garcia-Castro J, Martin MC, de la Fuente R, Ciqudosa JC, Lloyd AC, et al. Spontaneous human adult stem cell transformation. Cancer Res. 2005;65:3035–539.PubMedGoogle Scholar
  33. 33.
    Kadivar M, Khatami S, Mortazavi Y, Shokrgozar MA, Taghikhani M, Soleimani M. In vitro cardiomyogenic potential of human umbilical vein-derived mesenchymal stem cells. Biochem Biophys Res Commun. 2006;340:639–47.PubMedCrossRefGoogle Scholar

Copyright information

© The Japanese Society of Hematology 2009

Authors and Affiliations

  • Ikuo Ishige
    • 1
    • 2
  • Tokiko Nagamura-Inoue
    • 1
  • Masaki J. Honda
    • 3
  • Ratanakanit Harnprasopwat
    • 4
  • Michiko Kido
    • 5
  • Mitsuhiro Sugimoto
    • 5
  • Hiromitsu Nakauchi
    • 2
  • Arinobu Tojo
    • 1
    • 4
  1. 1.Department of Cell Processing and Transfusion, Institute of Medical ScienceUniversity of TokyoTokyoJapan
  2. 2.Division of Stem Cell Therapy, Center for Stem Cell and Regenerative Medicine, The Institute of Medical ScienceUniversity of TokyoTokyoJapan
  3. 3.Department of Anatomy, School of DentistryNihon UniversityTokyoJapan
  4. 4.Division of Molecular of Therapy, Center for Advanced Medical Research, The Institute of Medical ScienceUniversity of TokyoTokyoJapan
  5. 5.Department of ObstetricsJapanese Red Cross Medical CenterTokyoJapan

Personalised recommendations