Placental mesenchymal stem cells of fetal origin deposit epigenetic alterations during long-term culture under serum-free condition

Expert Opinion on Biological Therapy

Volumn 15, Issue 2, 2015, Pages 163-180

  Zhu, Yongzhao ^a,b   Song, Xumei ^a   Wang, Jian ^a   Li, Yukui ^a   Yang, Yinxue ^a   Yang, Tingting ^a   Ma, Haibin ^a   Wang, Libin ^a   Zhang, Guangyi ^a   Cho, William C ^c   Liu, Xiaoming ^a,b   Wei, Jun ^a  

^a NINGXIA MEDICAL UNIVERSITY   (China)

^b NINGXIA UNIVERSITY   (China)

^c QUEEN ELIZABETH HOSPITAL   (Hong Kong)

Author keywords

Epigenetic modification; Malignant transformation; Mesenchymal stem cells; Placenta

Indexed keywords

DNA METHYLTRANSFERASE; GENOMIC DNA; CULTURE MEDIUM;

AGING; ANIMAL EXPERIMENT; ARTICLE; CARCINOGENESIS; CARCINOGENICITY; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL PROLIFERATION; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; CULTURE MEDIUM; DEMETHYLATION; DNA METHYLATION; DOWN REGULATION; ENZYME ACTIVITY; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE ONTOLOGY; HUMAN; HUMAN TISSUE; IN VITRO PROPAGATION; IN VITRO STUDY; KARYOTYPING; MALE; MALIGNANT TRANSFORMATION; MESENCHYMAL STEM CELL; MOUSE; MURINE MODEL; NONHUMAN; PLACENTAL MESENCHYMAL STEM CELL; PROMOTER REGION; SCID MOUSE; SENESCENCE; SEVERE COMBINED IMMUNODEFICIENCY; TUMOR GROWTH; ANIMAL; CELL CULTURE; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECTS; FETUS; GENETIC EPIGENESIS; GENETICS; MESENCHYMAL STROMA CELL; PHARMACOLOGY; PHYSIOLOGY; PLACENTA; PREGNANCY; TIME;

MURINAE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FETUS; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MICE; MICE, SCID; PLACENTA; PREGNANCY; PROMOTER REGIONS, GENETIC; TIME FACTORS;

EID: 84920952786     PISSN: 14712598     EISSN: 17447682     Source Type: Journal    
DOI: 10.1517/14712598.2015.960837     Document Type: Article

References (63)

1. Das M, Sundell IB, Koka PS. Adult mesenchymal stem cells and their potency in the cell-based therapy. J Stem Cells 2013;8:1-16
2. Fierabracci A, Del Fattore A, Luciano R, et al. Recent advances in mesenchymal stem cell immunomodulation. the role of microvesicles. Cell Transplant 2013. [Epub ahead of print]
3. Zhang C, Zhai W, Xie Y, et al. Mesenchymal stem cells derived from breast cancer tissue promote the proliferation and migration of the MCF-7 cell line. Oncol Lett 2013;6:1577-82
4. Wagner W, Horn P, Castoldi M, et al. Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 2008;3:e2213
5. Li H, Fan X, Kovi RC, et al. Spontaneous expression of embryonic factors and p53 point mutations in aged mesenchymal stem cells: a model of age-related tumorigenesis in mice. Cancer Res 2007;67:10889-98
6. Miura M, Miura Y, Padilla-Nash HM, et al. Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells 2006;24:1095-103
7. Gou S, Wang C, Liu T, et al. Spontaneous differentiation of murine bone marrow-derived mesenchymal stem cells into adipocytes without malignant transformation after long-term culture. Cells Tissues Organs 2010;191:185-92
8. Tang Q, Chen Q, Lai X, et al. Malignant transformation potentials of human umbilical cord mesenchymal stem cells both spontaneously and via 3-methycholanthrene induction. PLoS One 2013;8:e81844
9. Wang Y, Zhang Z, Chi Y, et al. Long-term cultured mesenchymal stem cells frequently develop genomic mutations but do not undergo malignant transformation. Cell Death Dis 2013;4:e950
10. Redaelli S, Bentivegna A, Foudah D, et al. From cytogenomic to epigenomic profiles: monitoring the biologic behavior of in vitro cultured human bone marrow mesenchymal stem cells. Stem Cell Res Ther 2012;3:47.
11. Schellenberg A, Lin Q, Schuler H, et al. Replicative senescence of mesenchymal stem cells causes DNA-methylation changes which correlate with repressive histone marks. Aging 2011;3:873-88
12. Colosimo A, Russo V, Mauro A, et al. Prolonged in vitro expansion partially affects phenotypic features and osteogenic potential of ovine amniotic fluid-derived mesenchymal stromal cells. Cytotherapy 2013;15:930-50
13. Choi MR, In YH, Park J, et al. Genome-scale DNA methylation pattern profiling of human bone marrow mesenchymal stem cells in long-term culture. Exp Mol Med 2012;44:503-12
14. Binato R, de Souza Fernandez T, Lazzarotto-Silva C, et al. Stability of human mesenchymal stem cells during in vitro culture: considerations for cell therapy. Cell Prolif 2013;46:10-22
15. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002;3:415-28
16. Langevin SM, Kratzke RA, Kelsey KT. Epigenetics of lung cancer. Transl Res 2014. [Epub ahead of print]
17. Mummaneni P, Shord SS. Epigenetics and oncology. Pharmacotherapy 2014;34(5):495-505
18. Bork S, Pfister S, Witt H, et al. DNA methylation pattern changes upon longterm culture and aging of human mesenchymal stromal cells. Aging Cell 2010;9:54-63
19. Teng IW, Hou PC, Lee KD, et al. Targeted methylation of two tumor suppressor genes is sufficient to transform mesenchymal stem cells into cancer stem/initiating cells. Cancer Res 2011;71:4653-63.
20. Kong P, Xie X, Li F, et al. Placenta mesenchymal stem cell accelerates wound healing by enhancing angiogenesis in diabetic Goto-Kakizaki (GK) rats. Biochem Biophys Res Commun 2013;438:410-19
21. Parolini O, Alviano F, Bergwerf I, et al. Toward cell therapy using placentaderived cells: disease mechanisms, cell biology, preclinical studies, and regulatory aspects at the round table. Stem Cells Dev 2010;19:143-54
22. Zhang Y, Li C, Jiang X, et al. Human placenta-derived mesenchymal progenitor cells support culture expansion of longterm culture-initiating cells from cord blood CD34+ cells. Exp Hematol 2004;32:657-64
23. Sabapathy V, Ravi S, Srivastava V, et al. Long-term cultured human term placenta-derived mesenchymal stem cells of maternal origin displays plasticity. Stem Cells Int 2012;2012:174328
24. Zhu Y, Yang Y, Zhang Y, et al. Placental mesenchymal stem cells of fetal and maternal origins demonstrate different therapeutic potentials. Stem Cell Res Ther 2014;5:48.
25. Wang L, Yang Y, Zhu Y, et al. Characterization of placenta-derived mesenchymal stem cells cultured in autologous human cord blood serum. Molecular Med Rep 2012;6:760-6
26. Li CD, Zhang WY, Li HL, et al. Mesenchymal stem cells derived from human placenta suppress allogeneic umbilical cord blood lymphocyte proliferation. Cell Res 2005;15:539-47
27. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45
28. Hwang SM, See CJ, Choi J, et al. The application of an in situ karyotyping technique for mesenchymal stromal cells: a validation and comparison study with classical G-banding. Exp Mol Med 2013;45:e68
29. Barch MJ, Knutsen T, Spurbeck JL. The AGT cytogenetics laboratory manual. Lippincott-Raven; Philadelphia, PA, USA: 1997
30. Gonzalez Garcia JR, Meza-Espinoza JP. Use of the international system for human cytogenetic nomenclature (ISCN). Blood 2006;108:3952-3.
31. Beissbarth T, Speed TP. GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics 2004;20:1464-5
32. Chen AK, Reuveny S, Oh SK. Application of human mesenchymal and pluripotent stem cell microcarrier cultures in cellular therapy: achievements and future direction. Biotechnol Adv 2013;31:1032-46
33. Bellavia M, Altomare R, Cacciabaudo F, et al. Towards an ideal source of mesenchymal stem cell isolation for possible therapeutic application in regenerative medicine. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2013. [Epub ahead of print]
34. Wegmeyer H, Broske AM, Leddin M, et al. Mesenchymal stromal cell characteristics vary depending on their origin. Stem Cells Dev 2013;22:2606-18.
35. Bernardo ME, Zaffaroni N, Novara F, et al. Human bone marrow derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms. Cancer Res 2007;67:9142-9
36. Bonab MM, Alimoghaddam K, Talebian F, et al. Aging of mesenchymal stem cell in vitro. BMC Cell Biol 2006;7:14.
37. Herberts CA, Kwa MS, Hermsen HP. Risk factors in the development of stem cell therapy. J transl Med 2011;9:29
38. Berdasco M, Esteller M. DNA methylation in stem cell renewal and multipotency. Stem Cell Res Ther 2011;2:42
39. Sundin M, Ringden O, Sundberg B, et al. No alloantibodies against mesenchymal stromal cells, but presence of anti-fetal calf serum antibodies, after transplantation in allogeneic hematopoietic stem cell recipients. Haematologica 2007;92:1208-15
40. Tuschong L, Soenen SL, Blaese RM, et al. Immune response to fetal calf serum by two adenosine deaminase-deficient patients after T cell gene therapy. Hum Gene Ther 2002;13:1605-10.
41. Berniakovich I, Giorgio M. Low oxygen tension maintains multipotency, whereas normoxia increases differentiation of mouse bone marrow stromal cells. Int J Mol Sci 2013;14:2119-34
42. Korbut E, Ptak-Belowska A, Brzozowski T. Mechanisms promoting physiological cells progression into tumorigenesis. J Physiol Pharmacol 2012;63:565-70
43. Mark P, Kleinsorge M, Gaebel R, et al. Human mesenchymal stem cells display reduced expression of cd105 after culture in serum-free medium. Stem Cells Int 2013;2013:698076
44. Syeda F, Fagan RL, Wean M, et al. The replication focus targeting sequence (RFTS) domain is a DNA-competitive inhibitor of Dnmt1. J Biol Chem 2011;286:15344-51
45. Lan J, Hua S, He X, et al. DNA methyltransferases and methylbinding proteins of mammals. Acta Biochim Biophys Sin (Shanghai) 2010;42:243-52
46. Bestor TH. The DNA methyltransferases of mammals. Hum Mol Genet 2000;9:2395-402
47. Suetake I, Shinozaki F, Miyagawa J, et al. DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. J Biol Chem 2004;279:27816-23
48. Jin B, Robertson KD. DNA methyltransferases, DNA damage repair, and cancer. Adv Exp Med Biol 2013;754:3-29.
49. Turek-Plewa J, Jagodzinski PP. The role of mammalian DNA methyltransferases in the regulation of gene expression. Cell Mol Biol Lett 2005;10:631-47
50. Dansranjavin T, Krehl S, Mueller T, et al. The role of promoter CpG methylation in the epigenetic control of stem cell related genes during differentiation. Cell Cycle 2009;8:916-24
51. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33(Suppl):245-54
52. Li N, Yang R, Zhang W, et al. Genetically transforming human mesenchymal stem cells to sarcomas: changes in cellular phenotype and multilineage differentiation potential. Cancer 2009;115:4795-806
53. Mohseny AB, Hogendoorn PC. Concise review: mesenchymal tumors: when stem cells go mad. Stem Cells 2011;29:397-403
54. Mohseny AB, Szuhai K, Romeo S, et al. Osteosarcoma originates from mesenchymal stem cells in consequence of aneuploidization and genomic loss of Cdkn2. J Pathol 2009;219:294-305
55. Xiao W, Mohseny AB, Hogendoorn PC, et al. Mesenchymal stem cell transformation and sarcoma genesis. Clin Sarcoma Res 2013;3:10
56. Zhang S, Han Z, Kong Q, et al. Malignant transformation of rat bone marrow-derived mesenchymal stem cells treated with 4-nitroquinoline 1-oxide. Chem Biol Interact 2010;188:119-26
57. Liu J, Zhang Y, Bai L, et al. Rat bone marrow mesenchymal stem cells undergo malignant transformation via indirect cocultured with tumour cells. Cell biochem Funct 2012;30:650-6
58. Sun Y, Yang Y, Zeng S, et al. Identification of proteins related to epigenetic regulation in the malignant transformation of aberrant karyotypic human embryonic stem cells by quantitative proteomics. PLoS One 2014;9:e85823
59. Rosland GV, Svendsen A, Torsvik A, et al. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res 2009;69:5331-9
60. Torsvik A, Rosland GV, Svendsen A, et al. Spontaneous malignant transformation of human mesenchymal stem cells reflects cross-contamination: putting the research field on track-letter. Cancer Res 2010;70:6393-6.
61. Sempere JM, Martinez-Peinado P, Arribas MI, et al. Single-Cell derived clones from human adipose stem cells present different immunomodulatory properties. Clin Exp Immunol 2014;176(2):255-65
62. Poloni A, Maurizi G, Babini L, et al. Human mesenchymal stem cells from chorionic villi and amniotic fluid are not susceptible to transformation after extensive in vitro expansion. Cell Transpl 2011;20:643-54
63. Zhou XG, Yang Y, Yang JS, et al. Granulocyte-macrophage colonystimulating factor and interleukin 4 induce the malignant transformation of the bone marrow-derived human adult mesenchymal stem cells. Chin Med J (Engl) 2011;124:729-33