Advertisement

Cell and Tissue Research

, Volume 366, Issue 3, pp 523–531 | Cite as

Role of stem cell factor in the placental niche

  • Elahe Khodadi
  • Saeid Shahrabi
  • Mohammad Shahjahani
  • Saeed Azandeh
  • Najmaldin Saki
Review

Abstract

Stem cell factor (SCF) is a cytokine found in hematopoietic stem cells (HSCs) and causes proliferation and differentiation of cells by binding to its receptor (c-kit). It is produced in the yolk sac, fetal liver and bone marrow during the development of the fetus and, together with its signaling pathway, plays an important role in the development of these cells. The placenta, an important hematopoiesis site before the entry of cells into the liver, is rich in HSCs, with definitive hematopoiesis in a variety of HSC types and embryonic stem cells. Chorionic-plate-derived mesenchymal stem cells (CP-MSCs) isolated from the placenta show stem cell markers such as CD41 and cause the self-renewal of cells under hypoxic conditions. In contrast, hypoxia can result in apoptosis and autophagy via oxidative stress in stem cells. As a hypoxia-induced factor, SCF causes a balance between cell survival and death by autophagy in CP-MSCs. Stromal cells and MSCs have a crucial function in the development of HSCs in the placenta via SCF expression in the placental vascular niche. Defects in hematopoietic growth factors (such as SCF and its signaling pathways) lead to impaired hematopoiesis, resulting in fetal death and abortion. Therefore, an awareness of the role of the SCF/c-kit pathway in the survival, apoptosis and development of stem cells can significantly contribute to the exploration of stem cell production pathways during the embryonic period and in malignancies and in the further generation of these cells to facilitate therapeutic approaches. In this review, we discuss the role of SCF in the placental niche.

Keywords

Stem cell factor Placental niche Hematopoietic stem cells Mesenchymal stem cells Hematopoiesis 

Notes

Acknowledgments

We wish to thank all our colleagues at Shafa Hospital and Allied Health Sciences School, Ahvaz Jundishapur University of Medical Sciences.

Authors’ contributions

N.S. conceived the manuscript and revised it; E.K, S.A. and M.Sh. wrote the manuscript; N.S. and E.K. prepared the table and figure.

Compliance with ethical standards

Conflict of interest

None

References

  1. Alvarez-Silva M, Belo-Diabangouaya P, Salaün J, Dieterlen-Lièvre F (2003) Mouse placenta is a major hematopoietic organ. Development 130:5437–5444CrossRefPubMedGoogle Scholar
  2. Ankrum J, Karp JM (2010) Mesenchymal stem cell therapy: two steps forward, one step back. Trends Mol Med 16:203–209CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ashman LK (1999) The biology of stem cell factor and its receptor C-kit. Int J Biochem Cell Biol 31:1037–1051CrossRefPubMedGoogle Scholar
  4. Bashamboo A, Taylor AH, Samuel K, Panthier J-J, Whetton AD, Forrester LM (2006) The survival of differentiating embryonic stem cells is dependent on the SCF-KIT pathway. J Cell Sci 119:3039–3046CrossRefPubMedGoogle Scholar
  5. Broudy VC (1997) Stem cell factor and hematopoiesis. Blood 90:1345–1364PubMedGoogle Scholar
  6. Carson WE, Haldar S, Baiocchi RA, Croce CM, Caligiuri MA (1994) The c-kit ligand suppresses apoptosis of human natural killer cells through the upregulation of bcl-2. Proc Natl Acad Sci 91:7553–7557CrossRefPubMedPubMedCentralGoogle Scholar
  7. Castrechini N, Murthi P, Gude N, Erwich J, Gronthos S, Zannettino A, Kalionis B (2010) Mesenchymal stem cells in human placental chorionic villi reside in a vascular niche. Placenta 31:203–212CrossRefPubMedGoogle Scholar
  8. Chhabra A, Lechner AJ, Ueno M, Acharya A, Van Handel B, Wang Y, Mikkola HK (2012) Trophoblasts regulate the placental hematopoietic niche through PDGF-B signaling. Dev Cell 22:651–659CrossRefPubMedPubMedCentralGoogle Scholar
  9. Corbel C, Vaigot P, Salaun J (2005) Alpha IIb integrin, a novel marker for hemopoietic progenitor cells. Int J Dev Biol 49:279–284CrossRefPubMedGoogle Scholar
  10. Crisan M, Yap S, Casteilla L, Chen C-W, Corselli M, Park TS, Zhang L (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313CrossRefPubMedGoogle Scholar
  11. Cross J, Baczyk D, Dobric N, Hemberger M, Hughes M, Simmons D, Kingdom J (2003) Genes, development and evolution of the placenta. Placenta 24:123–130CrossRefPubMedGoogle Scholar
  12. Cumano A, Dieterlen-Lievre F, Godin I (1996) Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 86:907–916CrossRefPubMedGoogle Scholar
  13. Danet GH, Pan Y, Luongo JL, Bonnet DA, Simon MC (2003) Expansion of human SCID-repopulating cells under hypoxic conditions. J Clin Invest 112:126–135CrossRefPubMedPubMedCentralGoogle Scholar
  14. de Bruijn MF, Ma X, Robin C, Ottersbach K, Sanchez M-J, Dzierzak E (2002) Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 16:673–683CrossRefPubMedGoogle Scholar
  15. Diaz-Flores L, Gutierrez R, Lopez-Alonso A, Gonzalez R, Varela H (1992) Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin Orthop Relat Res 275:280–286Google Scholar
  16. Ding L, Saunders TL, Enikolopov G, Morrison SJ (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481:457–462CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dolci S, Williams DE, Ernst MK, Resnick JL, Brannan CI, Lock LF, Donovan PJ (1991) Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature 352:809–811CrossRefPubMedGoogle Scholar
  18. Downs K (2002) Early placental ontogeny in the mouse. Placenta 23:116–131CrossRefPubMedGoogle Scholar
  19. Downs KM, Gardner RL (1995) An investigation into early placental ontogeny: allantoic attachment to the chorion is selective and developmentally regulated. Development 121:407–416PubMedGoogle Scholar
  20. Dubreuil P, Forrester L, Rottapel R, Reedijk M, Fujita J, Bernstein A (1991) The c-fms gene complements the mitogenic defect in mast cells derived from mutant W mice but not mi (microphthalmia) mice. Proc Natl Acad Sci U S A 88:2341–2345CrossRefPubMedPubMedCentralGoogle Scholar
  21. Dvorak AM, Seder RA, Paul WE, Morgan ES, Galli SJ (1994) Effects of interleukin-3 with or without the c-kit ligand, stem cell factor, on the survival and cytlopasmic granule formation of mouse basophils and mast cells in vitro. Am J Pathol 144:160PubMedPubMedCentralGoogle Scholar
  22. Dzierza KE, Speck NA (2008) Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol 9:129–136CrossRefGoogle Scholar
  23. Eliasson P, Jönsson JI (2010) The hematopoietic stem cell niche: low in oxygen but a nice place to be. J Cell Physiol 222:17–22CrossRefPubMedGoogle Scholar
  24. Elmasri H, Ghelfi E, Yu C-w, Traphagen S, Cernadas M, Cao H, Hotamisligil G (2012) Endothelial cell-fatty acid binding protein 4 promotes angiogenesis: role of stem cell factor/c-kit pathway. Angiogenesis 15:457–468CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ezashi T, Das P, Roberts RM (2005) Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci U S A 102:4783–4788CrossRefPubMedPubMedCentralGoogle Scholar
  26. Ferkowicz MJ, Yoder MC (2005) Blood island formation: longstanding observations and modern interpretations. Exp Hematol 33:1041–1047CrossRefPubMedGoogle Scholar
  27. Ferkowicz MJ, Starr M, Xie X, Li W, Johnson SA, Shelley WC, Yoder MC (2003) CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development 130:4393–4403CrossRefPubMedGoogle Scholar
  28. Gekas C, Dieterlen-Lièvre F, Orkin SH, Mikkola HK (2005) The placenta is a niche for hematopoietic stem cells. Dev Cell 8:365–375CrossRefPubMedGoogle Scholar
  29. Gordon-Keylock S, Sobiesiak M, Rybtsov S, Moore K, Medvinsky A (2013) Mouse extraembryonic arterial vessels harbor precursors capable of maturing into definitive HSCs. Blood 122:2338–2345CrossRefPubMedPubMedCentralGoogle Scholar
  30. Green DR, Kroemer G (2005) Pharmacological manipulation of cell death: clinical applications in sight? J Clin Invest 115:2610–2617CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gustafsson ÅB, Gottlieb RA (2008) Eat your heart out: role of autophagy in myocardial ischemia/reperfusion. Autophagy 4:416–421CrossRefPubMedPubMedCentralGoogle Scholar
  32. Han Z-B, Ren H, Zhao H, Chi Y, Chen K, Zhou B, Liu B (2008) Hypoxia-inducible factor (HIF)-1α directly enhances the transcriptional activity of stem cell factor (SCF) in response to hypoxia and epidermal growth factor (EGF). Carcinogenesis 29:1853–1861CrossRefPubMedGoogle Scholar
  33. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432:625–630CrossRefPubMedGoogle Scholar
  34. Ji L, Liu YX, Yang C, Yue W, Shi SS, Bai CX, Pei XT (2009) Self-renewal and pluripotency is maintained in human embryonic stem cells by co-culture with human fetal liver stromal cells expressing hypoxia inducible factor 1α. J Cell Physiol 221:54–66CrossRefPubMedGoogle Scholar
  35. Kim MJ, Shin KS, Jeon JH, Lee DR, Shim SH, Kim JK, Kim GJ (2011) Human chorionic-plate-derived mesenchymal stem cells and Wharton’s jelly-derived mesenchymal stem cells: a comparative analysis of their potential as placenta-derived stem cells. Cell Tissue Res 346:53–64CrossRefPubMedGoogle Scholar
  36. Kissel H, Timokhina I, Hardy MP, Rothschild G, Tajima Y, Soares V, Besmer P (2000) Point mutation in kit receptor tyrosine kinase reveals essential roles for kit signaling in spermatogenesis and oogenesis without affecting other kit responses. EMBO J 19:1312–1326CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kumaravelu P, Hook L, Morrison AM, Ure J, Zhao S, Zuyev S, Medvinsky A (2002) Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development 129:4891–4899PubMedGoogle Scholar
  38. Lee Y, Jung J, Cho KJ, Lee SK, Park JW, Oh IH, Kim GJ (2013) Increased SCF/c-kit by hypoxia promotes autophagy of human placental chorionic plate-derived mesenchymal stem cells via regulating the phosphorylation of mTOR. J Cell Biochem 114:79–88CrossRefPubMedGoogle Scholar
  39. Lennartsson J, Rönnstrand L (2012) Stem cell factor receptor/c-Kit: from basic science to clinical implications. Physiol Rev 92:1619–1649CrossRefPubMedGoogle Scholar
  40. Majmundar AJ, Wong WJ, Simon MC (2010) Hypoxia-inducible factors and the response to hypoxic stress. Mol Cell 40:294–309CrossRefPubMedPubMedCentralGoogle Scholar
  41. Matsui J, Wakabayashi T, Asada M, Yoshimatsu K, Okada M (2004) Stem cell factor/c-kit signaling promotes the survival, migration, and capillary tube formation of human umbilical vein endothelial cells. J Biol Chem 279:18600–18607CrossRefPubMedGoogle Scholar
  42. Miao Z, Jin J, Chen L, Zhu J, Huang W, Zhao J, Zhang X (2006) Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol Int 30:681–687CrossRefPubMedGoogle Scholar
  43. Mikkola HK, Fujiwara Y, Schlaeger TM, Traver D, Orkin SH (2003) Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood 101:508–516CrossRefPubMedGoogle Scholar
  44. Mikkola HK, Gekas C, Orkin SH, Dieterlen-Lievre F (2005) Placenta as a site for hematopoietic stem cell development. Exp Hematol 33:1048–1054CrossRefPubMedGoogle Scholar
  45. Mitjavila-Garcia MT, Cailleret M, Godin I, Nogueira MM, Cohen-Solal K, Schiavon V, Vainchenker W (2002) Expression of CD41 on hematopoietic progenitors derived from embryonic hematopoietic cells. Development 129:2003–2013PubMedGoogle Scholar
  46. Mohyeldin A, Garzón-Muvdi T, Quiñones-Hinojosa A (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 7:150–161CrossRefPubMedGoogle Scholar
  47. Nekanti U, Dastidar S, Venugopal P, Totey S, Ta M (2010) Increased proliferation and analysis of differential gene expression in human Wharton’s jelly-derived mesenchymal stromal cells under hypoxia. Int J Biol Sci 6:499–512CrossRefPubMedPubMedCentralGoogle Scholar
  48. Orr-Urtreger A, Avivi A, Zimmer Y, Givol D, Yarden Y, Lonai P (1990) Developmental expression of c-kit, a proto-oncogene encoded by the W locus. Development 109:911–923PubMedGoogle Scholar
  49. Osawa M, Hanada K-I, Hamada H, Nakauchi H (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273:242–245CrossRefPubMedGoogle Scholar
  50. Ottersbach K, Dzierzak E (2005) The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev Cell 8:377–387CrossRefPubMedGoogle Scholar
  51. Palacios R, Nishikawa SL (1992) Developmentally regulated cell surface expression and function of c-kit receptor during lymphocyte ontogeny in the embryo and adult mice. Development 115:1133–1147PubMedGoogle Scholar
  52. Palmqvist L, Glover CH, Hsu L, Lu M, Bossen B, Piret JM, Helgason CD (2005) Correlation of murine embryonic stem cell gene expression profiles with functional measures of pluripotency. Stem Cells 23:663–680CrossRefPubMedGoogle Scholar
  53. Raynaud CM, Butler JM, Halabi NM, Ahmad FS, Ahmed B, Rafii S, Rafii A (2013) Endothelial cells provide a niche for placental hematopoietic stem/progenitor cell expansion through broad transcriptomic modification. Stem Cell Res 11:1074–1090CrossRefPubMedGoogle Scholar
  54. Rhodes KE, Gekas C, Wang Y, Lux CT, Francis CS, Chan DN, Mikkola HK (2008) The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell 2:252–263CrossRefPubMedPubMedCentralGoogle Scholar
  55. Robin C, Ottersbach K, Durand C, Peeters M, Vanes L, Tybulewicz V, Dzierzak E (2006) An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells. Dev Cell 11:171–180CrossRefPubMedGoogle Scholar
  56. Robin C, Bollerot K, Mendes S, Haak E, Crisan M, Cerisoli F, Vermeulen M (2009) Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development. Cell Stem Cell 5:385–395CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rossant J, Cross JC (2001) Placental development: lessons from mouse mutants. Nat Rev Genet 2:538–548CrossRefPubMedGoogle Scholar
  58. Rybtsov S, Sobiesiak M, Taoudi S, Souilhol C, Senserrich J, Liakhovitskaia A, Medvinsky A (2011) Hierarchical organization and early hematopoietic specification of the developing HSC lineage in the AGM region. J Exp Med 208:1305–1315CrossRefPubMedPubMedCentralGoogle Scholar
  59. Rybtsov S, Batsivari A, Bilotkach K, Paruzina D, Senserrich J, Nerushev O, Medvinsky A (2014) Tracing the origin of the HSC hierarchy reveals an SCF-dependent, IL-3-independent CD43− embryonic precursor. Stem cell Rep 3:489–501CrossRefGoogle Scholar
  60. Sasaki T, Mizuochi C, Horio Y, Nakao K, Akashi K, Sugiyama D (2010) Regulation of hematopoietic cell clusters in the placental niche through SCF/Kit signaling in embryonic mouse. Development 137:3941–3952CrossRefPubMedGoogle Scholar
  61. Shi S, Gronthos S (2003) Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18:696–704CrossRefPubMedGoogle Scholar
  62. Sugiyama D, Tsuji K (2006) Definitive hematopoiesis from endothelial cells in the mouse embryo; a simple guide. Trends Cardiovasc Med 16:45–49CrossRefPubMedGoogle Scholar
  63. Tanaka S, Kunath T, Hadjantonakis A-K, Nagy A, Rossant J (1998) Promotion of trophoblast stem cell proliferation by FGF4. Science 282:2072–2075CrossRefPubMedGoogle Scholar
  64. Taoudi S, Gonneau C, Moore K, Sheridan JM, Blackburn CC, Taylor E, Medvinsky A (2008) Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin+ CD45+ pre-definitive HSCs. Cell Stem Cell 3:99–108CrossRefPubMedGoogle Scholar
  65. Williams DE, Eisenman J, Baird A, Rauch C, Van Ness K, March CJ, Boswell HS (1990) Identification of a ligand for the c-kit proto-oncogene. Cell 63:167–174CrossRefPubMedGoogle Scholar
  66. Zannettino A, Paton S, Arthur A, Khor F, Itescu S, Gimble J, Gronthos S (2008) Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 214:413–421CrossRefPubMedGoogle Scholar
  67. Zovein AC, Iruela-Arispe ML (2009) Time to cut the cord: placental HSCs grow up. Cell Stem Cell 5:351–352CrossRefPubMedGoogle Scholar
  68. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Hedrick MH (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Elahe Khodadi
    • 1
  • Saeid Shahrabi
    • 2
  • Mohammad Shahjahani
    • 1
  • Saeed Azandeh
    • 3
  • Najmaldin Saki
    • 1
  1. 1.Health Research Institute, Thalassemia & Hemoglobinopathy Research CenterAhvaz Jundishapur University of Medical SciencesAhvazIran
  2. 2.Department of Biochemistry and Hematology, Faculty of MedicineSemnan University of Medical SciencesSemnanIran
  3. 3.Cellular and Molecular Research Center, Department of Anatomical ScienceAhvaz Jundishapur University of Medical SciencesAhvazIran

Personalised recommendations