Skip to main content

Advertisement

SpringerLink
Log in

Comparison of the Neural Differentiation Potential of Human Mesenchymal Stem Cells from Amniotic Fluid and Adult Bone Marrow

  • Short Communication
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Human mesenchymal stem cells (MSCs) are considered a promising tool for cell-based therapies of nervous system diseases. Bone marrow (BM) has been the traditional source of MSCs (BM-MSCs). However, there are some limitations for their clinical use, such as the decline in cell number and differentiation potential with age. Recently, amniotic fluid (AF)-derived MSCs (AF-MSCs) have been shown to express embryonic and adult stem cell markers, and can differentiate into cells of all three germ layers. In this study, we isolated AF-MSCs from second-trimester AF by limiting dilution and compared their proliferative capacity, multipotency, neural differentiation ability, and secretion of neurotrophins to those of BM-MSCs. AF-MSCs showed a higher proliferative capacity and more rapidly formed and expanded neurospheres compared to those of BM-MSCs. Both immunocytochemical and quantitative real-time PCR analyses demonstrated that AF-MSCs showed higher expression of neural stemness markers than those of BM-MSCs following neural stem cell (NSC) differentiation. Furthermore, the levels of brain-derived growth factor and nerve growth factor secreted by AF-MSCs in the culture medium were higher than those of BM-MSCs. In addition, AF-MSCs maintained a normal karyotype in long-term cultures after NSC differentiation and were not tumorigenic in vivo. Our findings suggest that AF-MSCs are a promising and safe alternative to BM-MSCs for therapy of nervous system diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Bieback K, Kern S, Kluter H, Eichler H (2004) Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood. Stem Cells 22:625–634

    Article  PubMed  Google Scholar 

  • Bitsika V, Roubelakis MG, Zagoura D, Trohatou O, Makridakis M, Pappa KI, Marini FC, Vlahou A, Anagnou NP (2012) Human amniotic fluid-derived mesenchymal stem cells as therapeutic vehicles: a novel approach for the treatment of bladder cancer. Stem Cells Dev 21:1097–1111

    Article  PubMed  CAS  Google Scholar 

  • Chen Q, Long Y, Yuan X, Zou L, Sun J, Chen S, Perez-Polo JR, Yang K (2005) Protective effects of bone marrow stromal cell transplantation in injured rodent brain: synthesis of neurotrophic factors. J Neurosci Res 80:611–619

    Article  PubMed  CAS  Google Scholar 

  • De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ, Furth ME, Soker S, Atala A (2007) Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 25:100–106

    Article  PubMed  Google Scholar 

  • Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (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 

  • Ellis P, Fagan BM, Magness ST, Hutton S, Taranova O, Hayashi S, McMahon A, Rao M, Pevny L (2004) SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci 26:148–165

    Article  PubMed  CAS  Google Scholar 

  • Fukuchi Y, Nakajima H, Sugiyama D, Hirose I, Kitamura T, Tsuji K (2004) Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22:649–658

    Article  PubMed  CAS  Google Scholar 

  • Gargett CE, Schwab KE, Zillwood RM, Nguyen HP, Wu D (2009) Isolation and culture of epithelial progenitors and mesenchymal stem cells from human endometrium. Biol Reprod 80:1136–1145

    Article  PubMed  CAS  Google Scholar 

  • Hermann A, Gastl R, Liebau S, Popa MO, Fiedler J, Boehm BO, Maisel M, Lerche H, Schwarz J, Brenner R, Storch A (2004) Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci 117:4411–4422

    Article  PubMed  CAS  Google Scholar 

  • Hermann A, List C, Habisch HJ, Vukicevic V, Ehrhart-Bornstein M, Brenner R, Bernstein P, Fickert S, Storch A (2010) Age-dependent neuroectodermal differentiation capacity of human mesenchymal stromal cells: limitations for autologous cell replacement strategies. Cytotherapy 12:17–30

    Article  PubMed  CAS  Google Scholar 

  • Kaneko Y, Sakakibara S, Imai T, Suzuki A, Nakamura Y, Sawamoto K, Ogawa Y, Toyama Y, Miyata T, Okano H (2000) Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 22:139–153

    Article  PubMed  CAS  Google Scholar 

  • Khoo ML, Tao H, Meedeniya AC, Mackay-Sim A, Ma DD (2011) Transplantation of neuronal-primed human bone marrow mesenchymal stem cells in hemiparkinsonian rodents. PLoS One 6:e19025

    Article  PubMed  CAS  Google Scholar 

  • Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585–595

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Chen J, Chen XG, Wang L, Gautam SC, Xu YX, Katakowski M, Zhang LJ, Lu M, Janakiraman N, Chopp M (2002) Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 59:514–523

    Article  PubMed  CAS  Google Scholar 

  • Liu YW, Roan JN, Wang SP, Hwang SM, Tsai, Chen JH, Hsieh PC (2012) Xenografted human amniotic fluid-derived stem cell as a cell source in therapeutic angiogenesis. Int J Cardiol. doi:10.1016/j.ijcard.2012.09.072

    Google Scholar 

  • Lu P, Jones LL, Snyder EY, Tuszynski MH (2003) Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp Neurol 181:115–129

    Article  PubMed  CAS  Google Scholar 

  • Mareschi K, Rustichelli D, Comunanza V, De Fazio R, Cravero C, Morterra G, Martinoglio B, Medico E, Carbone E, Benedetto C, Fagioli F (2009) Multipotent mesenchymal stem cells from amniotic fluid originate neural precursors with functional voltage-gated sodium channels. Cytotherapy 11:534–547

    Article  PubMed  CAS  Google Scholar 

  • Moorefield EC, McKee EE, Solchaga L, Orlando G, Yoo JJ, Walker S, Furth ME, Bishop CE (2011) Cloned, CD117 selected human amniotic fluid stem cells are capable of modulating the immune response. PLoS One 6:e26535

    Article  PubMed  CAS  Google Scholar 

  • Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D (1994) Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13:1071–1082

    Article  PubMed  CAS  Google Scholar 

  • Mueller SM, Glowacki J (2001) Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J Cell Biochem 82:583–590

    Article  PubMed  CAS  Google Scholar 

  • Park D, Xiang AP, Mao FF, Zhang L, Di CG, Liu XM, Shao Y, Ma BF, Lee JH, Ha KS, Walton N, Lahn BT (2010) Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 28:2162–2171

    Article  PubMed  CAS  Google Scholar 

  • Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147

    Article  PubMed  CAS  Google Scholar 

  • Roubelakis MG, Pappa KI, Bitsika V, Zagoura D, Vlahou A, Papadaki HA, Antsaklis A, Anagnou NP (2007) Molecular and proteomic characterization of human mesenchymal stem cells derived from amniotic fluid: comparison to bone marrow mesenchymal stem cells. Stem cells Dev 16:931–952

    Article  PubMed  CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108

    Article  PubMed  CAS  Google Scholar 

  • Stenderup K, Justesen J, Clausen C, Kassem M (2003) Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33:919–926

    Article  PubMed  Google Scholar 

  • Suzuki S, Namiki J, Shibata S, Mastuzaki Y, Okano H (2010) The neural stem/progenitor cell marker nestin is expressed in proliferative endothelial cells, but not in mature vasculature. J Histochem Cytochem 58:721–730

    Article  PubMed  CAS  Google Scholar 

  • Yi T, Song SU (2012) Immunomodulatory properties of mesenchymal stem cells and their therapeutic applications. Arch Pharm Res 35:213–221

    Article  PubMed  CAS  Google Scholar 

  • Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Natural Science Foundation of China (U0632008, 81100916, 30901774).

Author information

Authors and Affiliations

  1. Neurosurgery Institute, Key Laboratory on Brain Function Repair and Regeneration of Guangdong, Zhujiang Hospital, Southern Medical University, Guangzhou, 510282, China

    Zhong-Jie Yan, Zong-Yu Xiao, Xin-Lin Sun, Ying-Qian Cai & Chang-Chen Hu

  2. Affiliated Bayi Brain Hospital, The Military General Hospital of Beijing PLA, The Bayi Clinical Medical Institute of Southern Medical University, Beijing, 100700, China

    Zhong-Jie Yan, Hong-Tian Zhang, Peng Zhang & Ru-Xiang Xu

  3. Department of Gynecology and Obstetrics, The Affiliated Hexian Memorial Hospital of Southern Medical University, Guangzhou, 511400, China

    Yu-Qin Hu

Authors
  1. Zhong-Jie Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu-Qin Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hong-Tian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zong-Yu Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xin-Lin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ying-Qian Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chang-Chen Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ru-Xiang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ru-Xiang Xu.

Additional information

Zhongjie Yan and Yuqin Hu contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yan, ZJ., Hu, YQ., Zhang, HT. et al. Comparison of the Neural Differentiation Potential of Human Mesenchymal Stem Cells from Amniotic Fluid and Adult Bone Marrow. Cell Mol Neurobiol 33, 465–475 (2013). https://doi.org/10.1007/s10571-013-9922-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-013-9922-y

Keywords

Search

Navigation