Advertisement

Cell and Tissue Research

, Volume 363, Issue 3, pp 599–608 | Cite as

Induction of apoptosis, stimulation of cell-cycle arrest and inhibition of angiogenesis make human amnion-derived cells promising sources for cell therapy of cancer

  • Hassan Niknejad
  • Ghasem Yazdanpanah
  • Abolhassan Ahmadiani
Mini Review

Abstract

Amniotic membrane (AM), the nearest layer of fetal membranes to the fetus, contains two types of cells with unique characteristics that make them excellent candidates for clinical applications. Amniotic epithelial and mesenchymal cells have low immunogenicity, anti-inflammation, anti-fibrosis and anti-bacterial properties and no ethical issues. Although amniotic cells have stem cell properties and express transcription factors specific for pluripotent stem cells, they are not tumorigenic after transplantation. In the last decade, a new line of research has been initiated with a focus on the anti-proliferative effects of amniotic epithelial and mesenchymal cells on tumor growth. Amnion-derived epithelial and mesenchymal cells inhibit tumor growth and invasion through three pathways: the induction of apoptosis, the stimulation of cell-cycle arrest and the inhibition of angiogenesis. In this review, the various aspects of the anti-cancer properties of amnion-derived cells and the underlying mechanisms are discussed with emphasis on the translation of the cell therapy of cancer from experimental into clinical practice.

Keywords

Amniotic membrane Apoptosis Angiogenesis Cancer Cell therapy 

Notes

Acknowledgments

The authors thank Prof. H. Peirovi for his critical comments.

References

  1. Alviano F, Fossati V, Marchionni C, Arpinati M, Bonsi L, Franchina M, Lanzoni G, Cantoni S, Cavallini C, Bianchi F, Tazzari PL, Pasquinelli G, Foroni L, Ventura C, Grossi A, Bagnara GP (2007) Term amniotic membrane is a high throughput source for multipotent mesenchymal stem cells with the ability to differentiate into endothelial cells in vitro. BMC Dev Biol 7:11PubMedCentralCrossRefPubMedGoogle Scholar
  2. Banerjee A, Weidinger A, Hofer M, Steinborn R, Lindenmair A, Hennerbichler-Lugscheider S, Eibl J, Redl H, Kozlov AV, Wolbank S (2015) Different metabolic activity in placental and reflected regions of the human amniotic membrane. Placenta 36:1329–1332CrossRefPubMedGoogle Scholar
  3. Barboni B, Russo V, Curini V, Martelli A, Berardinelli P, Mauro A, Mattioli M, Marchisio M, Bonassi Signoroni P, Parolini O, Colosimo A (2014) Gestational stage affects amniotic epithelial cells phenotype, methylation status, immunomodulatory and stemness properties. Stem Cell Rev 10:725–741PubMedCentralCrossRefPubMedGoogle Scholar
  4. Bauer D, Wasmuth S, Hennig M, Baehler H, Steuhl KP, Heiligenhaus A (2009) Amniotic membrane transplantation induces apoptosis in T lymphocytes in murine corneas with experimental herpetic stromal keratitis. Invest Ophthalmol Vis Sci 50:3188–3198CrossRefPubMedGoogle Scholar
  5. Bauer D, Hennig M, Wasmuth S, Baehler H, Busch M, Steuhl KP, Thanos S, Heiligenhaus A (2012) Amniotic membrane induces peroxisome proliferator-activated receptor-gamma positive alternatively activated macrophages. Invest Ophthalmol Vis Sci 53:799–810CrossRefPubMedGoogle Scholar
  6. Bourcier T, Becmeur PH, Mutter D (2015) Robotically assisted amniotic membrane transplant surgery. JAMA Ophthalmol 133:213–214CrossRefPubMedGoogle Scholar
  7. de Weerd L, Weum S, Sjavik K, Acharya G, Hennig RO (2013) A new approach in the repair of a myelomeningocele using amnion and a sensate perforator flap. J Plast Reconstr Aesthet Surg 66:860–863CrossRefPubMedGoogle Scholar
  8. Diaz-Prado S, Muinos-Lopez E, Hermida-Gomez T, Rendal-Vazquez ME, Fuentes-Boquete I, de Toro FJ, Blanco FJ (2010) Multilineage differentiation potential of cells isolated from the human amniotic membrane. J Cell Biochem 111:846–857CrossRefPubMedGoogle Scholar
  9. Garfias Y, Zaga-Clavellina V, Vadillo-Ortega F, Osorio M, Jimenez-Martinez MC (2011) Amniotic membrane is an immunosuppressor of peripheral blood mononuclear cells. Immunol Invest 40:183–196CrossRefPubMedGoogle Scholar
  10. Hao Y, Ma DH, Hwang DG, Kim WS, Zhang F (2000) Identification of antiangiogenic and antiinflammatory proteins in human amniotic membrane. Cornea 19:348–352CrossRefPubMedGoogle Scholar
  11. Hemphill C, Stavoe K, Khalpey Z (2014) First in man: amniotic stem cell injection promotes scar remodeling and healing processes in late-stage fibrosis. Int J Cardiol 174:442–443CrossRefPubMedGoogle Scholar
  12. Henley SA, Dick FA (2012) The retinoblastoma family of proteins and their regulatory functions in the mammalian cell division cycle. Cell Div 7:10PubMedCentralCrossRefPubMedGoogle Scholar
  13. Hupfeld J, Gorr IH, Schwald C, Beaucamp N, Wiechmann K, Kuentzer K, Huss R, Rieger B, Neubauer M, Wegmeyer H (2014) Modulation of mesenchymal stromal cell characteristics by microcarrier culture in bioreactors. Biotechnol Bioeng 111:2290–2302CrossRefPubMedGoogle Scholar
  14. Hwang JH, Shim SS, Seok OS, Lee HY, Woo SK, Kim BH, Song HR, Lee JK, Park YK (2009) Comparison of cytokine expression in mesenchymal stem cells from human placenta, cord blood, and bone marrow. J Korean Med Sci 24:547–554PubMedCentralCrossRefPubMedGoogle Scholar
  15. Ilancheran S, Michalska A, Peh G, Wallace EM, Pera M, Manuelpillai U (2007) Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol Reprod 77:577–588CrossRefPubMedGoogle Scholar
  16. Jablonski EM, Mattocks MA, Sokolov E, Koniaris LG, Hughes FM Jr, Fausto N, Pierce RH, McKillop IH (2007) Decreased aquaporin expression leads to increased resistance to apoptosis in hepatocellular carcinoma. Cancer Lett 250:36–46PubMedCentralCrossRefPubMedGoogle Scholar
  17. Jiang YJ, Kim P, Lu YF, Feingold KR (2011) PPARgamma activators stimulate aquaporin 3 expression in keratinocytes/epidermis. Exp Dermatol 20:595–599PubMedCentralCrossRefPubMedGoogle Scholar
  18. Jiang H, He D, Xu H, Liu J, Qu L, Tong S (2015) Cullin-1 promotes cell proliferation via cell cycle regulation and is a novel in prostate cancer. Int J Clin Exp Pathol 8:1575–1583PubMedCentralPubMedGoogle Scholar
  19. Jiao H, Guan F, Yang B, Li J, Song L, Hu X, Du Y (2012) Human amniotic membrane derived-mesenchymal stem cells induce C6 glioma apoptosis in vivo through the Bcl-2/caspase pathways. Mol Biol Rep 39:467–473CrossRefPubMedGoogle Scholar
  20. Kakavand M, Yazdanpanah G, Ahmadiani A, Niknejad H (2015) Blood compatibility of human amniotic membrane compared with heparin-coated ePTFE for vascular tissue engineering. J Tissue Eng Regen Med. doi: 10.1002/term.2064 PubMedGoogle Scholar
  21. Kang JW, Koo HC, Hwang SY, Kang SK, Ra JC, Lee MH, Park YH (2012a) Immunomodulatory effects of human amniotic membrane-derived mesenchymal stem cells. J Vet Sci 13:23–31PubMedCentralCrossRefPubMedGoogle Scholar
  22. Kang NH, Yi BR, Lim SY, Hwang KA, Baek YS, Kang KS, Choi KC (2012b) Human amniotic membrane-derived epithelial stem cells display anticancer activity in BALB/c female nude mice bearing disseminated breast cancer xenografts. Int J Oncol 40:2022–2028PubMedGoogle Scholar
  23. Khalpey Z, Marsh KM, Ferng A, Riaz IB, Friedman M, Indik J, Avery R, Jokerst C, Oliva I (2015) First in man: amniotic patch reduces postoperative inflammation. Am J Med 128:e5–e6CrossRefPubMedGoogle Scholar
  24. Klein JD, Fauza DO (2011) Amniotic and placental mesenchymal stem cell isolation and culture. Methods Mol Biol 698:75–88CrossRefPubMedGoogle Scholar
  25. Koike C, Zhou K, Takeda Y, Fathy M, Okabe M, Yoshida T, Nakamura Y, Kato Y, Nikaido T (2014) Characterization of amniotic stem cells. Cell Reprogram 16:298–305PubMedCentralCrossRefPubMedGoogle Scholar
  26. Kubo M, Sonoda Y, Muramatsu R, Usui M (2001) Immunogenicity of human amniotic membrane in experimental xenotransplantation. Invest Ophthalmol Vis Sci 42:1539–1546PubMedGoogle Scholar
  27. Lalier L, Pedelaborde F, Braud C, Menanteau J, Vallette FM, Olivier C (2011) Increase in intracellular PGE2 induces apoptosis in Bax-expressing colon cancer cell. BMC Cancer 11:153PubMedCentralCrossRefPubMedGoogle Scholar
  28. Li H, Niederkorn JY, Neelam S, Mayhew E, Word RA, McCulley JP, Alizadeh H (2005) Immunosuppressive factors secreted by human amniotic epithelial cells. Invest Ophthalmol Vis Sci 46:900–907CrossRefPubMedGoogle Scholar
  29. Magatti M, De Munari S, Vertua E, Parolini O (2012) Amniotic membrane-derived cells inhibit proliferation of cancer cell lines by inducing cell cycle arrest. J Cell Mol Med 16:2208–2218PubMedCentralCrossRefPubMedGoogle Scholar
  30. Magatti M, Caruso M, De Munari S, Vertua E, De D, Manuelpillai U, Parolini O (2015) Human amniotic membrane-derived mesenchymal and epithelial cells exert different effects on monocyte-derived dendritic cell differentiation and function. Cell Transplant 24:1733–1752CrossRefPubMedGoogle Scholar
  31. Malumbres M, Barbacid M (2009) Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer 9:153–166CrossRefPubMedGoogle Scholar
  32. Mamede AC, Laranjo M, Carvalho MJ, Abrantes AM, Pires AS, Brito AF, Moura P, Maia CJ, Botelho MF (2014) Effect of amniotic membrane proteins in human cancer cell lines: an exploratory study. J Membr Biol 247:357–360CrossRefPubMedGoogle Scholar
  33. Mamede AC, Guerra S, Laranjo M, Carvalho MJ, Oliveira RC, Goncalves AC, Alves R, Prado Castro L, Sarmento-Ribeiro AB, Moura P, Abrantes AM, Maia CJ, Botelho MF (2015) Selective cytotoxicity and cell death induced by human amniotic membrane in hepatocellular carcinoma. Med Oncol 32:257CrossRefPubMedGoogle Scholar
  34. Masiero M, Simoes FC, Han HD, Snell C, Peterkin T, Bridges E, Mangala LS, Wu SY, Pradeep S, Li D, Han C, Dalton H, Lopez-Berestein G, Tuynman JB, Mortensen N, Li JL, Patient R, Sood AK, Banham AH, Harris AL, Buffa FM (2013) A core human primary tumor angiogenesis signature identifies the endothelial orphan receptor ELTD1 as a key regulator of angiogenesis. Cancer Cell 24:229–241PubMedCentralCrossRefPubMedGoogle Scholar
  35. Miki T, Lehmann T, Cai H, Stolz DB, Strom SC (2005) Stem cell characteristics of amniotic epithelial cells. Stem Cells 23:1549–1559CrossRefPubMedGoogle Scholar
  36. Mogami H, Keller PW, Shi H, Word RA (2014) Effect of thrombin on human amnion mesenchymal cells, mouse fetal membranes, and preterm birth. J Biol Chem 289:13295–13307PubMedCentralCrossRefPubMedGoogle Scholar
  37. Moore RM, Mansour JM, Redline RW, Mercer BM, Moore JJ (2006) The physiology of fetal membrane rupture: insight gained from the determination of physical properties. Placenta 27:1037–1051CrossRefPubMedGoogle Scholar
  38. Niknejad H, Yazdanpanah G (2014a) Anticancer effects of human amniotic membrane and its epithelial cells. Med Hypotheses 82:488–489CrossRefPubMedGoogle Scholar
  39. Niknejad H, Yazdanpanah G (2014b) Opposing effect of amniotic membrane on angiogenesis originating from amniotic epithelial cells. J Med Hypotheses Ideas 8:39–41CrossRefGoogle Scholar
  40. Niknejad H, Peirovi H, Jorjani M, Ahmadiani A, Ghanavi J, Seifalian AM (2008) Properties of the amniotic membrane for potential use in tissue engineering. Eur Cell Mater 15:88–99PubMedGoogle Scholar
  41. Niknejad H, Deihim T, Solati-Hashjin M, Peirovi H (2011) The effects of preservation procedures on amniotic membrane’s ability to serve as a substrate for cultivation of endothelial cells. Cryobiology 63:145–151CrossRefPubMedGoogle Scholar
  42. Niknejad H, Khayat-Khoei M, Peirovi H (2012) Inhibition of MMPs might increase anticancer properties of amniotic epithelial cells. Med Hypotheses 78:690–691CrossRefPubMedGoogle Scholar
  43. Niknejad H, Deihim T, Peirovi H, Abolghasemi H (2013a) Serum-free cryopreservation of human amniotic epithelial cells before and after isolation from their natural scaffold. Cryobiology 67:56–63CrossRefPubMedGoogle Scholar
  44. Niknejad H, Paeini-Vayghan G, Tehrani FA, Khayat-Khoei M, Peirovi H (2013b) Side dependent effects of the human amnion on angiogenesis. Placenta 34:340–345CrossRefPubMedGoogle Scholar
  45. Niknejad H, Yazdanpanah G, Mirmasoumi M, Abolghasemi H, Peirovi H, Ahmadiani A (2013c) Inhibition of HSP90 could be possible mechanism for anti-cancer property of amniotic membrane. Med Hypotheses 81:862–865CrossRefPubMedGoogle Scholar
  46. Niknejad H, Khayat-Khoei M, Peirovi H, Abolghasemi H (2014) Human amniotic epithelial cells induce apoptosis of cancer cells: a new anti-tumor therapeutic strategy. Cytotherapy 16:33–40CrossRefPubMedGoogle Scholar
  47. Niknejad H, Yazdanpanah G, Kakavand M (2015) Extract of fetal membrane would inhibit thrombosis and hemolysis. Med Hypotheses 85:197–202CrossRefPubMedGoogle Scholar
  48. Pavan B, Paganetto G, Dalpiaz A, Biondi C, Lunghi L (2011) Estrogen metabolites in the release of inflammatory mediators from human amnion-derived cells. Life Sci 88:551–558CrossRefPubMedGoogle Scholar
  49. Peirovi H, Rezvani N, Hajinasrollah M, Mohammadi SS, Niknejad H (2012) Implantation of amniotic membrane as a vascular substitute in the external jugular vein of juvenile sheep. J Vasc Surg 56:1098–1104CrossRefPubMedGoogle Scholar
  50. Penny H, Rifkah M, Weaver A, Zaki P, Young A, Meloy G, Flores R (2015) Dehydrated human amnion/chorion tissue in difficult-to-heal DFUs: a case series. J Wound Care 24:104–111CrossRefPubMedGoogle Scholar
  51. Pianta S, Bonassi Signoroni P, Muradore I, Rodrigues MF, Rossi D, Silini A, Parolini O (2015) Amniotic membrane mesenchymal cells-derived factors skew T cell polarization toward Treg and downregulate Th1 and Th17 cells subsets. Stem Cell Rev 11:394–407PubMedCentralCrossRefPubMedGoogle Scholar
  52. Qi X, Wang J, Sun D, Zhou Q, Xie L (2014) Postoperative changes in amniotic membrane as a carrier for allogeneic cultured limbal epithelial transplantation. Am J Ophthalmol 158:e1191CrossRefGoogle Scholar
  53. Secchiero P, Zorzet S, Tripodo C, Corallini F, Melloni E, Caruso L, Bosco R, Ingrao S, Zavan B, Zauli G (2010) Human bone marrow mesenchymal stem cells display anti-cancer activity in SCID mice bearing disseminated non-Hodgkin’s lymphoma xenografts. PLoS One 5:e11140PubMedCentralCrossRefPubMedGoogle Scholar
  54. Seo JH, Kim YH, Kim JS (2008) Properties of the amniotic membrane may be applicable in cancer therapy. Med Hypotheses 70:812–814CrossRefPubMedGoogle Scholar
  55. Singh R, Chacharkar MP (2011) Dried gamma-irradiated amniotic membrane as dressing in burn wound care. J Tissue Viability 20:49–54CrossRefPubMedGoogle Scholar
  56. Stenqvist AC, Nagaeva O, Baranov V, Mincheva-Nilsson L (2013) Exosomes secreted by human placenta carry functional Fas ligand and TRAIL molecules and convey apoptosis in activated immune cells, suggesting exosome-mediated immune privilege of the fetus. J Immunol 191:5515–5523CrossRefPubMedGoogle Scholar
  57. Tan SL, Sulaiman S, Pingguan-Murphy B, Selvaratnam L, Tai CC, Kamarul T (2011) Human amnion as a novel cell delivery vehicle for chondrogenic mesenchymal stem cells. Cell Tissue Bank 12:59–70CrossRefPubMedGoogle Scholar
  58. Tehrani FA, Ahmadiani A, Niknejad H (2013) The effects of preservation procedures on antibacterial property of amniotic membrane. Cryobiology 67:293–298CrossRefPubMedGoogle Scholar
  59. Wirt SE, Sage J (2010) p107 in the public eye: an Rb understudy and more. Cell Div 5:9PubMedCentralCrossRefPubMedGoogle Scholar
  60. Yazdanpanah G, Paeini-Vayghan G, Asadi S, Niknejad H (2015) The effects of cryopreservation on angiogenesis modulation activity of human amniotic membrane. Cryobiology 71:413–418CrossRefPubMedGoogle Scholar
  61. Yu X, Su B, Ge P, Wang Z, Li S, Huang B, Gong Y, Lin J (2015) Human adipose derived stem cells induced cell apoptosis and S phase arrest in bladder tumor. Stem Cells Int 2015:1–12CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Hassan Niknejad
    • 1
  • Ghasem Yazdanpanah
    • 1
  • Abolhassan Ahmadiani
    • 2
  1. 1.Department of Tissue Engineering and Regenerative Medicine, School of Advanced Technologies in MedicineShahid Beheshti University of Medical SciencesTehranIran
  2. 2.Neuroscience Research CenterShahid Beheshti University of Medical SciencesTehranIran

Personalised recommendations