Tumorigenicity analysis of heterogeneous dental stem cells and its self-modification for chromosome instability

References

• Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, Vrana J, Jones K, Grotewold L, Smith A. Nanog safeguards pluripotency and mediates germline development. Nature 2007; 450:1230-4; PMID:18097409; http://dx.doi.org/10.1038/nature06403
   PubMed Web of Science ®Google Scholar
• Hayashi K, Lopes SM, Tang F, Surani MA. Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Sell 2008; 3:391-401; PMID:18940731; http://dx.doi.org/10.1016/j.stem.2008.07.027
   PubMed Web of Science ®Google Scholar
• Singh AM, Hamazaki T, Hankowski KE, Terada N. A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem cells 2007; 25:2534-42; PMID:17615266; http://dx.doi.org/10.1634/stemcells.2007-0126
   PubMed Web of Science ®Google Scholar
• Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 2001; 19:180-92; PMID:11359943; http://dx.doi.org/10.1634/stemcells.19-3-180
   PubMed Web of Science ®Google Scholar
• Graf T, Stadtfeld M. Heterogeneity of embryonic and adult stem cells. Cell Stem Cell 2008; 3:480-3; PMID:18983963; http://dx.doi.org/10.1016/j.stem.2008.10.007
   PubMed Web of Science ®Google Scholar
• Solozobova V, Blattner C. p53 in stem cells. World J Biol Chem 2011; 2:202-14; PMID:21949570; http://dx.doi.org/10.4331/wjbc.v2.i9.202
   PubMedGoogle Scholar
• Valtieri M, Sorrentino A. The mesenchymal stromal cell contribution to homeostasis. J Cell Physiol 2008; 217:296-300; PMID:18615579; http://dx.doi.org/10.1002/jcp.21521
   PubMed Web of Science ®Google Scholar
• Chery L, Lam HM, Coleman I, Lakely B, Coleman R, Larson S, Aguirre-Ghiso JA, Xia J, Gulati R, Nelson PS, et al. Characterization of single disseminated prostate cancer cells reveals tumor cell heterogeneity and identifies dormancy associated pathways. Oncotarget 2014; 5:9939-51; PMID:25301725
   PubMed Web of Science ®Google Scholar
• Boesch M, Zeimet AG, Reimer D, Schmidt S, Gastl G, Parson W, Spoeck F, Hatina J, Wolf D, Sopper S. The side population of ovarian cancer cells defines a heterogeneous compartment exhibiting stem cell characteristics. Oncotarget 2014; 5:7027-39; PMID:25216521
   PubMed Web of Science ®Google Scholar
• Ben-David U, Benvenisty N. The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat Rev Cancer 2011; 11:268-77; PMID:21390058; http://dx.doi.org/10.1038/nrc3034
   PubMed Web of Science ®Google Scholar
• Bolouri H. Network dynamics in the tumor microenvironment. Semin Cancer Biol 2014; 30:52-9; PMID: 24582766; http://dx.doi.org/10.1016/j.semcancer.2014.02.007
   PubMed Web of Science ®Google Scholar
• Biancotti JC, Benvenisty N. Aneuploid human embryonic stem cells: origins and potential for modeling chromosomal disorders. Regenerative Med 2011; 6:493-503; PMID:21749207; http://dx.doi.org/10.2217/rme.11.27
   PubMed Web of Science ®Google Scholar
• Mayshar Y, Ben-David U, Lavon N, Biancotti JC, Yakir B, Clark AT, Plath K, Lowry WE, Benvenisty N. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 2010; 7:521-31; PMID:20887957; http://dx.doi.org/10.1016/j.stem.2010.07.017
   PubMed Web of Science ®Google Scholar
• Miura M, Miura Y, Padilla-Nash HM, Molinolo AA, Fu B, Patel V, Seo BM, Sonoyama W, Zheng JJ, Baker CC, et al. Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells 2006; 24:1095-103; PMID:16282438; http://dx.doi.org/10.1634/stemcells.2005-0403
   PubMed Web of Science ®Google Scholar
• Boveri T. Concerning the origin of malignant tumours by Theodor Boveri. Translated and annotated by Henry Harris. J Cell Sci 2008; 121 Suppl 1:1-84; PMID:18089652; http://dx.doi.org/10.1242/jcs.025742
   PubMedGoogle Scholar
• A SA, H BC, J SS. Application of UV-spectrophotometric methods for estimation of tenofovir disoproxil fumarate in tablets. Pakistan J Pharm Sci 2009; 22:27-9; PMID:19168416;
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j.cell.2011.02.013
   PubMed Web of Science ®Google Scholar
• Moon SH, Kim JS, Park SJ, Lim JJ, Lee HJ, Lee SM, Chung HM. Effect of chromosome instability on the maintenance and differentiation of human embryonic stem cells in vitro and in vivo. Stem Cell Res 2011; 6:50-9; PMID:20920899; http://dx.doi.org/10.1016/j.scr.2010.08.006
   PubMed Web of Science ®Google Scholar
• Colter DC, Sekiya I, Prockop DJ. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci U S A 2001; 98:7841-5; PMID:11427725; http://dx.doi.org/10.1073/pnas.141221698
   PubMed Web of Science ®Google Scholar
• Guo W, Gong K, Shi H, Zhu G, He Y, Ding B, Wen L, Jin Y. Dental follicle cells and treated dentin matrix scaffold for tissue engineering the tooth root. Biomaterials 2012; 33:1291-302; PMID:22088889; http://dx.doi.org/10.1016/j.biomaterials.2011.09.068
   PubMed Web of Science ®Google Scholar
• Muraglia A, Cancedda R, Quarto R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 2000; 113 (Pt 7)1161-6; PMID:10704367;
   PubMed Web of Science ®Google Scholar
• Lee CC, Christensen JE, Yoder MC, Tarantal AF. Clonal analysis and hierarchy of human bone marrow mesenchymal stem and progenitor cells. Exp Hematol 2010; 38:46-54; PMID:19900502; http://dx.doi.org/10.1016/j.exphem.2009.11.001
   PubMed Web of Science ®Google Scholar
• Yoshimura K, Asano Y, Aoi N, Kurita M, Oshima Y, Sato K, Inoue K, Suga H, Eto H, Kato H, et al. Progenitor-enriched adipose tissue transplantation as rescue for breast implant complications. Breast J 2010; 16:169-75; PMID:19912236; http://dx.doi.org/10.1111/j.1524-4741.2009.00873.x
   PubMed Web of Science ®Google Scholar
• Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA, Morgan JE. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 2005; 122:289-301; PMID:16051152; http://dx.doi.org/10.1016/j.cell.2005.05.010
   PubMed Web of Science ®Google Scholar
• Sherwood RI, Christensen JL, Conboy IM, Conboy MJ, Rando TA, Weissman IL, Wagers AJ. Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell 2004; 119:543-54; PMID:15537543; http://dx.doi.org/10.1016/j.cell.2004.10.021
   PubMed Web of Science ®Google Scholar
• Yang R, Chen M, Lee CH, Yoon R, Lal S, Mao JJ. Clones of ectopic stem cells in the regeneration of muscle defects in vivo. PloS One 2010; 5:e13547; PMID: 20975999; http://dx.doi.org/10.1371/journal.pone.0013547
   PubMed Web of Science ®Google Scholar
• Wagner W, Feldmann RE Jr, Seckinger A, Maurer MH, Wein F, Blake J, Krause U, Kalenka A, Burgers HF, Saffrich R, et al. The heterogeneity of human mesenchymal stem cell preparations-evidence from simultaneous analysis of proteomes and transcriptomes. Exp Hematol 2006; 34:536-48; PMID:16569600; http://dx.doi.org/10.1016/j.exphem.2006.01.002
   PubMed Web of Science ®Google Scholar
• Guo W, Chen L, Gong K, Ding B, Duan Y, Jin Y. Heterogeneous dental follicle cells and the regeneration of complex periodontal tissues. Tissue Eng Part A 2012; 18:459-70; PMID:21919800; http://dx.doi.org/10.1089/ten.TEA.2011.0261
   PubMed Web of Science ®Google Scholar
• Hou LT, Liu CM, Chen YJ, Wong MY, Chen KC, Chen J, Thomas HF. Characterization of dental follicle cells in developing mouse molar. Arch Oral Biol 1999; 44:759-70; PMID:10471160;
   PubMed Web of Science ®Google Scholar
• Wu J, Jin F, Tang L, Yu J, Xu L, Yang Z, Wu G, Duan Y, Jin Y. Dentin non-collagenous proteins (dNCPs) can stimulate dental follicle cells to differentiate into cementoblast lineages. Biol Cell/Under Auspices Eur Cell Biol Organ 2008; 100:291-302; PMID:18042041; http://dx.doi.org/10.1042/BC20070092
   PubMed Web of Science ®Google Scholar
• Yao S, Pan F, Prpic V, Wise GE. Differentiation of stem cells in the dental follicle. J Dental Res 2008; 87:767-71; PMID:18650550;
   PubMed Web of Science ®Google Scholar
• Kabir R, Gupta M, Aggarwal A, Sharma D, Sarin A, Kola MZ. Imperative role of dental pulp stem cells in regenerative therapies: a systematic review. Nigerian J Surg: Off Pub Nigerian Surg Res Soc 2014; 20:1-8; PMID:24665194; http://dx.doi.org/10.4103/1117-6806.127092
   PubMedGoogle Scholar
• Lymperi S, Ligoudistianou C, Taraslia V, Kontakiotis E, Anastasiadou E. Dental stem cells and their applications in dental tissue engineering. Open Dent J 2013; 7:76-81; PMID:24009647; http://dx.doi.org/10.2174/1874210601307010076
   PubMedGoogle Scholar
• Insinga A, Cicalese A, Faretta M, Gallo B, Albano L, Ronzoni S, Furia L, Viale A, Pelicci PG. DNA damage in stem cells activates p21, inhibits p53, and induces symmetric self-renewing divisions. Proc Natl Acad Sci U S Am 2013; 110:3931-6; PMID:23417300; http://dx.doi.org/10.1073/pnas.1213394110
   PubMed Web of Science ®Google Scholar
• Udayakumar T, Shareef MM, Diaz DA, Ahmed MM, Pollack A. The E2F1/Rb and p53/MDM2 pathways in DNA repair and apoptosis: understanding the crosstalk to develop novel strategies for prostate cancer radiotherapy. Semin Radiat Oncol 2010; 20:258-66; PMID:20832018; http://dx.doi.org/10.1016/j.semradonc.2010.05.007
   PubMed Web of Science ®Google Scholar
• Schvartzman JM, Duijf PH, Sotillo R, Coker C, Benezra R. Mad2 is a critical mediator of the chromosome instability observed upon Rb and p53 pathway inhibition. Cancer Cell 2011; 19:701-14; PMID:21665145; http://dx.doi.org/10.1016/j.ccr.2011.04.017
   PubMed Web of Science ®Google Scholar
• Ryan SD, Britigan EM, Zasadil LM, Witte K, Audhya A, Roopra A, Weaver BA. Up-regulation of the mitotic checkpoint component Mad1 causes chromosomal instability and resistance to microtubule poisons. Proc Natl Acad Sci U S A 2012; 109:E2205-14; PMID:22778409; http://dx.doi.org/10.1073/pnas.1201911109
   PubMed Web of Science ®Google Scholar
• Schvartzman JM, Sotillo R, Benezra R. Mitotic chromosomal instability and cancer: mouse modelling of the human disease. Nat Rev Cancer 2010; 10:102-15; PMID:20094045; http://dx.doi.org/10.1038/nrc2781
   PubMed Web of Science ®Google Scholar
• El-Sayed KM, Paris S, Graetz C, Kassem N, Mekhemar M, Ungefroren H, Fandrich F, Dorfer C. Isolation and characterisation of human gingival margin-derived STRO-1/MACS and MACS cell populations. Int J Oral Sci 2014; 7:80-8; PMID:25257881; http://dx.doi.org/10.1038/ijos.2014.41
   PubMed Web of Science ®Google Scholar
• Xu J, Wang W, Kapila Y, Lotz J, Kapila S. Multiple differentiation capacity of STRO-1+/CD146+ PDL mesenchymal progenitor cells. Stem Cells Dev 2009; 18:487-96; PMID:18593336; http://dx.doi.org/10.1089/scd.2008.0113
   PubMed Web of Science ®Google Scholar
• Majore I, Moretti P, Hass R, Kasper C. Identification of subpopulations in mesenchymal stem cell-like cultures from human umbilical cord. Cell Commun Signaling: CCS 2009; 7:6; PMID:19302702; http://dx.doi.org/10.1186/1478-811X-7-6
   PubMed Web of Science ®Google Scholar
• Stewart MH, Bosse M, Chadwick K, Menendez P, Bendall SC, Bhatia M. Clonal isolation of hESCs reveals heterogeneity within the pluripotent stem cell compartment. Nat Methods 2006; 3:807-15; PMID:16990813; http://dx.doi.org/10.1038/nmeth939
   PubMed Web of Science ®Google Scholar
• Sengers BG, Dawson JI, Oreffo RO. Characterisation of human bone marrow stromal cell heterogeneity for skeletal regeneration strategies using a two-stage colony assay and computational modelling. Bone 2010; 46:496-503; PMID:19818885; http://dx.doi.org/10.1016/j.bone.2009.10.002
   PubMed Web of Science ®Google Scholar
• Tormin A, Brune JC, Olsson E, Valcich J, Neuman U, Olofsson T, Jacobsen SE, Scheding S. Characterization of bone marrow-derived mesenchymal stromal cells (MSC) based on gene expression profiling of functionally defined MSC subsets. Cytotherapy 2009; 11:114-28; PMID:19242838; http://dx.doi.org/10.1080/14653240802716590
   PubMed Web of Science ®Google Scholar
• Smith JG, Smith AJ, Shelton RM, Cooper PR. Recruitment of dental pulp cells by dentine and pulp extracellular matrix components. Exp Cell Res 2012; 318:2397-406; PMID:22819733; http://dx.doi.org/10.1016/j.yexcr.2012.07.008
   PubMed Web of Science ®Google Scholar
• Freedman DA, Wu L, Levine AJ. Functions of the MDM2 oncoprotein. Cell Mol Life Sci: CMLS 1999; 55:96-107; PMID:10065155
   PubMed Web of Science ®Google Scholar
• Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 2005; 437:1043-7; PMID:16222300; http://dx.doi.org/10.1038/nature04217
   PubMed Web of Science ®Google Scholar
• Heng HH, Bremer SW, Stevens JB, Horne SD, Liu G, Abdallah BY, Ye KJ, Ye CJ. Chromosomal instability (CIN) what it is and why it is crucial to cancer evolution. Cancer Metast Rev 2013; 32:325-40; PMID:23605440; http://dx.doi.org/10.1007/s10555-013-9427-7
   PubMed Web of Science ®Google Scholar
• Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 2007; 8:275-83; PMID:17380161; http://dx.doi.org/10.1038/nrm2147
   PubMed Web of Science ®Google Scholar
• Notterman D, Young S, Wainger B, Levine AJ. Prevention of mammalian DNA reduplication, following the release from the mitotic spindle checkpoint, requires p53 protein, but not p53-mediated transcriptional activity. Oncogene 1998; 17:2743-51; PMID:9840938; http://dx.doi.org/10.1038/sj.onc.1202210
   PubMed Web of Science ®Google Scholar
• Lee J, Hoi CS, Lilja KC, White BS, Lee SE, Shalloway D, Tumbar T. Runx1 and p21 synergistically limit the extent of hair follicle stem cell quiescence in vivo. Proc Natl Acad Sci U S Am 2013; 110:4634-9; PMID:23487742; http://dx.doi.org/10.1073/pnas.1213015110
   PubMed Web of Science ®Google Scholar
• Zielke N, Kim KJ, Tran V, Shibutani ST, Bravo MJ, Nagarajan S, van Straaten M, Woods B, von Dassow G, Rottig C, et al. Control of Drosophila endocycles by E2F and CRL4(CDT2). Nature 2011; 480:123-7; PMID:22037307; http://dx.doi.org/10.1038/nature10579
   PubMed Web of Science ®Google Scholar
• Lin WC, Lin FT, Nevins JR. Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev 2001; 15:1833-44; PMID:11459832
   PubMed Web of Science ®Google Scholar
• Maser RS, Mirzoeva OK, Wells J, Olivares H, Williams BR, Zinkel RA, Farnham PJ, Petrini JH. Mre11 complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol Cell Biol 2001; 21:6006-16; PMID:11486038
   PubMed Web of Science ®Google Scholar
• Liu K, Lin FT, Ruppert JM, Lin WC. Regulation of E2F1 by BRCT domain-containing protein TopBP1. Mol Cell Biol 2003; 23:3287-304; PMID:12697828
   PubMed Web of Science ®Google Scholar
• Guo R, Chen J, Zhu F, Biswas AK, Berton TR, Mitchell DL, Johnson DG. E2F1 localizes to sites of UV-induced DNA damage to enhance nucleotide excision repair. J Biol Chem 2010; 285:19308-15; PMID:20413589; http://dx.doi.org/10.1074/jbc.M110.121939
   PubMed Web of Science ®Google Scholar
• Chen J, Zhu F, Weaks RL, Biswas AK, Guo R, Li Y, Johnson DG. E2F1 promotes the recruitment of DNA repair factors to sites of DNA double-strand breaks. Cell Cycle 2011; 10:1287-94; PMID:21512314; http://dx.doi.org/10.4161/cc.10.8.15341
   PubMed Web of Science ®Google Scholar
• Schuyler SC, Wu YF, Kuan VJ. The Mad1-Mad2 balancing act - a damaged spindle checkpoint in chromosome instability and cancer. J Cell Sci 2012; 125:4197-206; PMID:23093575; http://dx.doi.org/10.1242/jcs.107037
   PubMed Web of Science ®Google Scholar
• Bonizzi G, Cicalese A, Insinga A, Pelicci PG. The emerging role of p53 in stem cells. Trends Mol Med 2012; 18:6-12; PMID:21907001; http://dx.doi.org/10.1016/j.molmed.2011.08.002
   PubMed Web of Science ®Google Scholar
• Gregory CA, Gunn WG, Reyes E, Smolarz AJ, Munoz J, Spees JL, Prockop DJ. How Wnt signaling affects bone repair by mesenchymal stem cells from the bone marrow. Ann New York Acad Sci 2005; 1049:97-106; PMID:15965110; http://dx.doi.org/10.1196/annals.1334.010
   PubMed Web of Science ®Google Scholar
• Rosenbluh J, Wang X, Hahn WC. Genomic insights into WNT/beta-catenin signaling. Trends Pharmacol Sci 2014; 35:103-9; PMID:24365576; http://dx.doi.org/10.1016/j.tips.2013.11.007
   PubMed Web of Science ®Google Scholar
• James AW. Review of signaling pathways governing MSC osteogenic and adipogenic differentiation. Scientifica 2013; 2013:684736; PMID:24416618; http://dx.doi.org/10.1155/2013/684736
   PubMedGoogle Scholar
• Heggebo J, Haasters F, Polzer H, Schwarz C, Saller MM, Mutschler W, Schieker M, Prall WC. Aged human mesenchymal stem cells: the duration of bone morphogenetic protein-2 stimulation determines induction or inhibition of osteogenic differentiation. Orthopedic Rev 2014; 6:5242; PMID:25002931; http://dx.doi.org/10.4081/or.2014.5242
   PubMedGoogle Scholar
• Kevin A. Maupin CJD, Bart O. Williams. A comprehensive overview of skeletal phenotypes associated with alterations in Wnt/β-catenin signaling in humans and mice. Bone Res 2013; 1:27-71; PMID:http://dx.doi.org/10.4248/BR201301004
   PubMed Web of Science ®Google Scholar