Reprogramming malignant cancer cells toward a benign phenotype following exposure to human embryonic stem cell microenvironment

PLoS ONE

Volumn 12, Issue 1, 2017, Pages

  Zhou, Shufeng ^a,b   Abdouh, Mohamed ^a   Arena, Vincenzo ^c   Arena, Manuel ^d   Arena, Goffredo Orazio ^a,e  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MONTREAL GENERAL HOSPITAL   (Canada)

^c Santo Bambino Hospital   (Italy)

^d UNIVERSITY OF CATANIA   (Italy)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; CONDITIONED MEDIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BENIGN NEOPLASM; BREAST CARCINOMA; CANCER CELL; CANCER CELL LINE; CANCER GROWTH; CANCER INHIBITION; CANCER STAGING; CARCINOGENICITY; CELL ISOLATION; CELL PROLIFERATION; CELL REPROGRAMMING TECHNIQUE; COLORECTAL CARCINOMA; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYONIC STEM CELL; EXOSOME; EXPOSURE; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; TUMOR VOLUME; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; APOPTOSIS; CANCER GRADING; CELL COMMUNICATION; CELL CYCLE; CELL TRANSDIFFERENTIATION; CELL TRANSFORMATION; CONDITIONED MEDIUM; DRUG EFFECTS; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; NUCLEAR REPROGRAMMING; PHARMACOLOGY; SIGNAL TRANSDUCTION; STEM CELL NICHE; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; CELL COMMUNICATION; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; CELLULAR REPROGRAMMING; CULTURE MEDIA, CONDITIONED; EXOSOMES; FEMALE; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; NEOPLASM GRADING; PHENOTYPE; SIGNAL TRANSDUCTION; STEM CELL NICHE;

EID: 85009074627     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0169899     Document Type: Article

References (51)

1. Hendrix MJ, Seftor EA, Seftor RE, Kasemeier-Kulesa J, Kulesa PM, Postovit LM. Reprogramming metastatic tumour cells with embryonic microenvironments. Nat Rev Cancer. 2007; 7(4):246-55. doi: 10. 1038/nrc2108 PMID: 17384580
2. Bailey CM, Kulesa PM. Dynamic interactions between cancer cells and the embryonic microenvironment regulate cell invasion and reveal EphB6 as a metastasis suppressor. Mol Cancer Res. 2014; 12 (9):1303-13. PubMed Central PMCID: PMCPMC4498260. doi: 10.1158/1541-7786.MCR-13-0673 PMID: 24836890
3. Joel M, Sandberg CJ, Boulland JL, Vik-Mo EO, Langmoen IA, Glover JC. Inhibition of tumor formation and redirected differentiation of glioblastoma cells in a xenotypic embryonic environment. Dev Dyn. 2013; 242(9):1078-93. doi: 10.1002/dvdy.24001 PMID: 23780720
4. Mintz B, Illmensee K. Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc Natl Acad Sci U S A. 1975; 72(9):3585-9. PubMed Central PMCID: PMCPMC433040. PMID: 1059147
5. Illmensee K, Mintz B. Totipotency and normal differentiation of single teratocarcinoma cells cloned by injection into blastocysts. Proc Natl Acad Sci U S A. 1976; 73(2):549-53. PubMed Central PMCID: PMCPMC335947. PMID: 1061157
6. Diez-Torre A, Andrade R, Eguizabal C, Lopez E, Arluzea J, Silio M, et al. Reprogramming of melanoma cells by embryonic microenvironments. Int J Dev Biol. 2009; 53(8-10):1563-8. doi: 10.1387/ijdb. 093021ad PMID: 19924629
7. Lee LM, Seftor EA, Bonde G, Cornell RA, Hendrix MJ. The fate of human malignant melanoma cells transplanted into zebrafish embryos: assessment of migration and cell division in the absence of tumor formation. Dev Dyn. 2005; 233(4):1560-70. doi: 10.1002/dvdy.20471 PMID: 15968639
8. Kulesa PM, Kasemeier-Kulesa JC, Teddy JM, Margaryan NV, Seftor EA, Seftor RE, et al. Reprogramming metastatic melanoma cells to assume a neural crest cell-like phenotype in an embryonic microenvironment. Proc Natl Acad Sci U S A. 2006; 103(10):3752-7. PubMed Central PMCID: PMCPMC1450149. doi: 10.1073/pnas.0506977103 PMID: 16505384
9. Fonsato V, Collino F, Herrera MB, Cavallari C, Deregibus MC, Cisterna B, et al. Human liver stem cellderived microvesicles inhibit hepatoma growth in SCID mice by delivering antitumor microRNAs. Stem Cells. 2012; 30(9):1985-98. PubMed Central PMCID: PMCPMC3468738. doi: 10.1002/stem.1161 PMID: 22736596
10. Bruno S, Collino F, Deregibus MC, Grange C, Tetta C, Camussi G. Microvesicles derived from human bone marrow mesenchymal stem cells inhibit tumor growth. Stem Cells Dev. 2013; 22(5):758-71. doi: 10.1089/scd.2012.0304 PMID: 23034046
11. Schatten G, Smith J, Navara C, Park JH, Pedersen R. Culture of human embryonic stem cells. Nat Methods. 2005; 2(6):455-63. doi: 10.1038/nmeth0605-455 PMID: 16170868
12. Xu RH, Peck RM, Li DS, Feng X, Ludwig T, Thomson JA. Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods. 2005; 2(3):185-90. doi: 10.1038/nmeth744 PMID: 15782187
13. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998; 282(5391):1145-7. PMID: 9804556
14. Pera MF, Reubinoff B, Trounson A. Human embryonic stem cells. J Cell Sci. 2000; 113 (Pt 1):5-10.
15. Postovit LM, Margaryan NV, Seftor EA, Kirschmann DA, Lipavsky A, Wheaton WW, et al. Human embryonic stem cell microenvironment suppresses the tumorigenic phenotype of aggressive cancer cells. Proc Natl Acad Sci U S A. 2008; 105(11):4329-34. PubMed Central PMCID: PMCPMC2393795. doi: 10.1073/pnas.0800467105 PMID: 18334633
16. Postovit LM, Seftor EA, Seftor RE, Hendrix MJ. A three-dimensional model to study the epigenetic effects induced by the microenvironment of human embryonic stem cells. Stem Cells. 2006; 24(3):501-5. doi: 10.1634/stemcells.2005-0459 PMID: 16293574
17. Khalkhali-Ellis Z, Galat V, Galat Y, Gilgur A, Seftor EA, Hendrix MJC. Lefty Glycoproteins in Human Embryonic Stem Cells: Extracellular Delivery Route and Posttranslational Modification in Differentiation. Stem Cells Dev. September 2016; [Epub ahead of print].
18. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007; 9(6):654-9. doi: 10.1038/ncb1596 PMID: 17486113
19. Abbott DE, Bailey CM, Postovit LM, Seftor EA, Margaryan N, Seftor RE, et al. The epigenetic influence of tumor and embryonic microenvironments: how different are they? Cancer Microenviron. 2008; 1 (1):13-21. PubMed Central PMCID: PMCPMC2654360. doi: 10.1007/s12307-008-0004-5 PMID: 19308681
20. Giuffrida D, Rogers IM, Nagy A, Calogero AE, Brown TJ, Casper RF. Human embryonic stem cells secrete soluble factors that inhibit cancer cell growth. Cell Prolif. 2009; 42(6):788-98. doi: 10.1111/j. 1365-2184.2009.00640.x PMID: 19732065
21. Lykke-Andersen S, Brodersen DE, Jensen TH. Origins and activities of the eukaryotic exosome. J Cell Sci. 2009; 122(Pt 10):1487-94. doi: 10.1242/jcs.047399 PMID: 19420235
22. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia. 2006; 20(9):1487-95. doi: 10.1038/sj.leu.2404296 PMID: 16791265
23. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 2006; 20(5):847-56. doi: 10.1038/sj.leu.2404132 PMID: 16453000
24. Zhang S, Chu WC, Lai RC, Lim SK, Hui JH, Toh WS. Exosomes derived from human embryonic mesenchymal stem cells promote osteochondral regeneration. Osteoarthritis Cartilage. 2016.
25. Lai RC, Yeo RW, Padmanabhan J, Choo A, de Kleijn DP, Lim SK. Isolation and Characterization of Exosome from Human Embryonic Stem Cell-Derived C-Myc-Immortalized Mesenchymal Stem Cells. Methods Mol Biol. 2016; 1416:477-94. doi: 10.1007/978-1-4939-3584-0-29 PMID: 27236691
26. Khan M, Nickoloff E, Abramova T, Johnson J, Verma SK, Krishnamurthy P, et al. Embryonic stem cellderived exosomes promote endogenous repair mechanisms and enhance cardiac function following myocardial infarction. Circ Res. 2015; 117(1):52-64. PubMed Central PMCID: PMCPMC4482130. doi: 10.1161/CIRCRESAHA.117.305990 PMID: 25904597
27. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013; 200(4):373-83. PubMed Central PMCID: PMCPMC3575529. doi: 10.1083/jcb.201211138 PMID: 23420871
28. Kastelowitz N, Yin H. Exosomes and microvesicles: identification and targeting by particle size and lipid chemical probes. Chembiochem. 2014; 15(7):923-8. PubMed Central PMCID: PMCPMC4098878. doi: 10.1002/cbic.201400043 PMID: 24740901
29. Hosseini-Beheshti E, Pham S, Adomat H, Li N, Tomlinson Guns ES. Exosomes as biomarker enriched microvesicles: characterization of exosomal proteins derived from a panel of prostate cell lines with distinct AR phenotypes. Mol Cell Proteomics. 2012; 11(10):863-85. PubMed Central PMCID: PMCPMC3494141. doi: 10.1074/mcp.M111.014845 PMID: 22723089
30. Malumbres M. Cyclin-dependent kinases. Genome Biol. 2014; 15(6):122. PubMed Central PMCID: PMCPMC4097832. doi: 10.1186/gb4184 PMID: 25180339
31. Peurala E, Koivunen P, Haapasaari KM, Bloigu R, Jukkola-Vuorinen A. The prognostic significance and value of cyclin D1, CDK4 and p16 in human breast cancer. Breast Cancer Res. 2013; 15(1):R5. PubMed Central PMCID: PMCPMC3672746. doi: 10.1186/bcr3376 PMID: 23336272
32. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma. 1997; 106 (6):348-60. PMID: 9362543
33. Van Hooser A, Goodrich DW, Allis CD, Brinkley BR, Mancini MA. Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J Cell Sci. 1998; 111 (Pt 23):3497-506.
34. Li X, Pei D, Zheng H. Transitions between epithelial and mesenchymal states during cell fate conversions. Protein Cell. 2014; 5(8):580-91. PubMed Central PMCID: PMCPMC4130923. doi: 10.1007/s13238-014-0064-x PMID: 24805308
35. De Toro J, Herschlik L, Waldner C, Mongini C. Emerging roles of exosomes in normal and pathological conditions: new insights for diagnosis and therapeutic applications. Front Immunol. 2015; 6:203. PubMed Central PMCID: PMCPMC4418172. doi: 10.3389/fimmu.2015.00203 PMID: 25999947
36. Azmi AS, Bao B, Sarkar FH. Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev. 2013; 32(3-4):623-42. PubMed Central PMCID: PMCPMC3843988. doi: 10.1007/s10555-013-9441-9 PMID: 23709120
37. Ciardiello C, Cavallini L, Spinelli C, Yang J, Reis-Sobreiro M, de Candia P, et al. Focus on Extracellular Vesicles: New Frontiers of Cell-to-Cell Communication in Cancer. Int J Mol Sci. 2016; 17(2):175. PubMed Central PMCID: PMCPMC4783909. doi: 10.3390/ijms17020175 PMID: 26861306
38. Desrochers LM, Bordeleau F, Reinhart-King CA, Cerione RA, Antonyak MA. Microvesicles provide a mechanism for intercellular communication by embryonic stem cells during embryo implantation. Nat Commun. 2016; 7:11958. PubMed Central PMCID: PMCPMC4912619. doi: 10.1038/ncomms11958 PMID: 27302045
39. Medema JP. Cancer stem cells: the challenges ahead. Nat Cell Biol. 2013; 15(4):338-44. doi: 10.1038/ncb2717 PMID: 23548926
40. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet. 2000; 24(4):372-6. doi: 10.1038/74199 PMID: 10742100
41. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003; 113(5):643-55. PMID: 12787505
42. Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell. 2012; 10(6):717-28. doi: 10.1016/j.stem.2012.05.007 PMID: 22704512
43. Herreros-Villanueva M, Bujanda L, Billadeau DD, Zhang JS. Embryonic stem cell factors and pancreatic cancer. World J Gastroenterol. 2014; 20(9):2247-54. PubMed Central PMCID: PMCPMC3942830. doi: 10.3748/wjg.v20.i9.2247 PMID: 24605024
44. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006; 126(4):663-76. doi: 10.1016/j.cell.2006.07.024 PMID: 16904174
45. Kumar SM, Liu S, Lu H, Zhang H, Zhang PJ, Gimotty PA, et al. Acquired cancer stem cell phenotypes through Oct4-mediated dedifferentiation. Oncogene. 2012; 31(47):4898-911. PubMed Central PMCID: PMCPMC3343184. doi: 10.1038/onc.2011.656 PMID: 22286766
46. Lin YL, Han ZB, Xiong FY, Tian LY, Wu XJ, Xue SW et al. Malignant transformation of 293 cells induced by ectopic expressionof human Nanog. Mol Cell Biochem. 2011; 351:109-116. Epub 2011 Jan 19 doi: 10.1007/s11010-011-0717-5 PMID: 21246261
47. Kim J, Zaret KS. Reprogramming of human cancer cells to pluripotency for models of cancer progression. EMBO J. 2015; 34(6):739-47. PubMed Central PMCID: PMCPMC4369311. doi: 10.15252/embj. 201490736 PMID: 25712212
48. Slack JM. Origin of stem cells in organogenesis. Science. 2008; 322(5907):1498-501. doi: 10.1126/science.1162782 PMID: 19056975
49. Ohlsson LB, Varas L, Kjellman C, Edvardsen K, Lindvall M. Mesenchymal progenitor cell-mediated inhibition of tumor growth in vivo and in vitro in gelatin matrix. Exp Mol Pathol. 2003; 75(3):248-55. PMID: 14611816
50. Khakoo AY, Pati S, Anderson SA, Reid W, Elshal MF, Rovira, II, et al. Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J Exp Med. 2006; 203(5):1235-47. PubMed Central PMCID: PMCPMC2121206. doi: 10.1084/jem.20051921 PMID: 16636132
51. Qiao L, Xu Z, Zhao T, Zhao Z, Shi M, Zhao RC, et al. Suppression of tumorigenesis by human mesenchymal stem cells in a hepatoma model. Cell Res. 2008; 18(4):500-7. doi: 10.1038/cr.2008.40 PMID: 18364678