Stem and Cancer Stem Cell_Markers: Comparison
Please note this is a comparison between Version 2 by Peter Tang and Version 1 by Olatz Crende.

The conversion of healthy stem cells into cancer stem cells (CSCs) is believed to underlie tumor relapse after surgical removal and fuel tumor growth and invasiveness. CSCs often arise from the malignant transformation of resident multipotent stem cells, which are present in most human tissues. Some organs, such as the gut and the brain, can give rise to very aggressive types of cancers, contrary to the dental pulp, which is a tissue with a very remarkable resistance to oncogenesis.

  • stem cells
  • cancer stem cells
  • dental pulp stem cells
  • glioma
  • colorectal cancer
  • cell markers
  • telomerase
  • alternative lengthening of telomeres
  • pluripotency core factors
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References

  1. Williams, J.M.; Duckworth, C.A.; Burkitt, M.D.; Watson, A.J.M.; Campbell, B.J.; Pritchard, D.M. Epithelial cell shedding and barrier function: A matter of life and death at the small intestinal villus tip. Vet. Pathol. 2015, 52, 445–455.
  2. Umar, S. Intestinal Stem Cells. Curr. Gastroenterol. Rep. 2010, 12, 340–348.
  3. Cliffe, L.J.; Humphreys, N.E.; Lane, T.E.; Potten, C.S.; Booth, C.; Grencis, R.K. Accelerated intestinal epithelial cell turnover: A new mechanism of parasite expulsion. Science 2005, 308, 1463–1465.
  4. Paredes, M.F.; Sorrells, S.F.; Cebrian-Silla, A.; Sandoval, K.; Qi, D.; Kelley, K.W.; James, D.; Mayer, S.; Chang, J.; Auguste, K.I.; et al. Does Adult Neurogenesis Persist in the Human Hippocampus? Cell Stem Cell 2018, 23, 780–781.
  5. Moreno-Jiménez, E.P.; Flor-García, M.; Terreros-Roncal, J.; Rábano, A.; Cafini, F.; Pallas-Bazarra, N.; Ávila, J.; Llorens-Martín, M. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat. Med. 2019, 25, 554–560.
  6. Scoville, W.B.; Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 1957, 20, 11–21.
  7. Rusznák, Z.; Henskens, W.; Schofield, E.; Kim, W.S.; Fu, Y. Adult Neurogenesis and Gliogenesis: Possible Mechanisms for Neurorestoration. Exp. Neurobiol. 2016, 25, 103–112.
  8. Arvidsson, A.; Collin, T.; Kirik, D.; Kokaia, Z.; Lindvall, O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 2002, 8, 963–970.
  9. Robel, S.; Berninger, B.; Götz, M. The stem cell potential of glia: Lessons from reactive gliosis. Nat. Rev. Neurosci. 2011, 12, 88–104.
  10. Sierra, A.; Martin-Suarez, S.; Valcarcel-Martin, R.; Pascual-Brazo, J.; Aelvoet, S.A.; Abiega, O.; Deudero, J.J.; Brewster, A.L.; Bernales, I.; Anderson, A.E.; et al. Neuronal hyperactivity accelerates depletion of neural stem cells and impairs hippocampal neurogenesis. Cell Stem Cell 2015, 16, 488–503.
  11. Brenner, H.; Kloor, M.; Pox, C.P. Colorectal cancer. Lancet 2014, 383, 1490–1502.
  12. Seo, Y.-S.; Ko, I.O.; Park, H.; Jeong, Y.J.; Park, J.-A.; Kim, K.S.; Park, M.-J.; Lee, H.-J. Radiation-Induced Changes in Tumor Vessels and Microenvironment Contribute to Therapeutic Resistance in Glioblastoma. Front. Oncol. 2019, 9, 1259.
  13. Wang, D.; Wang, C.; Wang, L.; Chen, Y. A comprehensive review in improving delivery of small-molecule chemotherapeutic agents overcoming the blood-brain/brain tumor barriers for glioblastoma treatment. Drug Deliv. 2019, 26, 551–565.
  14. Stupp, R.; Hegi, M.E.; Mason, W.P.; van den Bent, M.J.; Taphoorn, M.J.B.; Janzer, R.C.; Ludwin, S.K.; Allgeier, A.; Fisher, B.; Belanger, K.; et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009, 10, 459–466.
  15. Visvader, J.E.; Lindeman, G.J. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat. Rev. Cancer 2008, 8, 755–768.
  16. Sell, S. Stem cell origin of cancer and differentiation therapy. Crit. Rev. Oncol. Hematol. 2004, 51, 1–28.
  17. Wang, K.; Wu, X.; Wang, J.; Huang, J. Cancer stem cell theory: Therapeutic implications for nanomedicine. Int. J. Nanomed. 2013, 8, 899–908.
  18. Kleinsmith, L.J.; Pierce, G.B. MULTIPOTENTIALITY OF SINGLE EMBRYONAL CARCINOMA CELLS. Cancer Res. 1964, 24, 1544–1551.
  19. Neuhaus, K.W. Teeth: Malignant neoplasms in the dental pulp? Lancet Oncol. 2007, 8, 75–78.
  20. Neuhaus, K.W. Dental Pulp Neoplasms. In Encyclopedia of Cancer; Schwab, M., Ed.; Springer: Berlin/Heidelberg, Germany, 2011; pp. 1084–1086. ISBN 978-3-642-16483-5.
  21. Gronthos, S.; Mankani, M.; Brahim, J.; Robey, P.G.; Shi, S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc. Natl. Acad. Sci. USA 2000, 97, 13625–13630.
  22. Mitsiadis, T.A.; Woloszyk, A. Odyssey of human dental pulp stem cells and their remarkable ability to survive in extremely adverse conditions. Front. Physiol. 2015, 6.
  23. Shi, S.; Gronthos, S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J. Bone Miner. Res. 2003, 18, 696–704.
  24. Kaukua, N.; Shahidi, M.K.; Konstantinidou, C.; Dyachuk, V.; Kaucka, M.; Furlan, A.; An, Z.; Wang, L.; Hultman, I.; Ahrlund-Richter, L.; et al. Glial origin of mesenchymal stem cells in a tooth model system. Nature 2014, 513, 551–554.
  25. Yoshida, S.; Wada, N.; Hasegawa, D.; Miyaji, H.; Mitarai, H.; Tomokiyo, A.; Hamano, S.; Maeda, H. Semaphorin 3A Induces Odontoblastic Phenotype in Dental Pulp Stem Cells. J. Dent. Res. 2016, 95, 1282–1290.
  26. Yang, X.; Zhang, S.; Fan, M.; Li, X.; Liu, T.; Yao, Y. Effects of interleukin-1β on mineralization potential of dental pulp stem cells. Zhonghua Kou Qiang Yi Xue Za Zhi 2011, 46, 406–411.
  27. Rombouts, C.; Jeanneau, C.; Bakopoulou, A.; About, I. Dental Pulp Stem Cell Recruitment Signals within Injured Dental Pulp Tissue. Dent. J. 2016, 4, 8.
  28. Ullah, I.; Subbarao, R.B.; Rho, G.J. Human mesenchymal stem cells—Current trends and future prospective. Biosci. Rep. 2015, 35.
  29. Huang, G.T.-J.; Gronthos, S.; Shi, S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: Their biology and role in regenerative medicine. J. Dent. Res. 2009, 88, 792–806.
  30. Ducimetière, F.; Lurkin, A.; Ranchère-Vince, D.; Decouvelaere, A.-V.; Péoc’h, M.; Istier, L.; Chalabreysse, P.; Muller, C.; Alberti, L.; Bringuier, P.-P.; et al. Incidence of Sarcoma Histotypes and Molecular Subtypes in a Prospective Epidemiological Study with Central Pathology Review and Molecular Testing. PLoS ONE 2011, 6.
  31. Burningham, Z.; Hashibe, M.; Spector, L.; Schiffman, J.D. The Epidemiology of Sarcoma. Clin. Sarcoma Res. 2012, 2, 14.
  32. Lv, F.-J.; Tuan, R.S.; Cheung, K.M.C.; Leung, V.Y.L. Concise review: The surface markers and identity of human mesenchymal stem cells. Stem Cells 2014, 32, 1408–1419.
  33. Snippert, H.J.; van Es, J.H.; van den Born, M.; Begthel, H.; Stange, D.E.; Barker, N.; Clevers, H. Prominin-1/CD133 marks stem cells and early progenitors in mouse small intestine. Gastroenterology 2009, 136, 2187–2194.e1.
  34. Todaro, M.; Perez Alea, M.; Scopelliti, A.; Medema, J.P.; Stassi, G. IL-4-mediated drug resistance in colon cancer stem cells. Cell Cycle 2008, 7, 309–313.
  35. Pfenninger, C.V.; Roschupkina, T.; Hertwig, F.; Kottwitz, D.; Englund, E.; Bengzon, J.; Jacobsen, S.E.; Nuber, U.A. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res. 2007, 67, 5727–5736.
  36. Jang, T.J.; Park, J.B.; Lee, J.I. The Expression of CD10 and CD15 Is Progressively Increased during Colorectal Cancer Development. Korean J. Pathol. 2013, 47, 340–347.
  37. Daynac, M.; Tirou, L.; Faure, H.; Mouthon, M.-A.; Gauthier, L.R.; Hahn, H.; Boussin, F.D.; Ruat, M. Hedgehog Controls Quiescence and Activation of Neural Stem Cells in the Adult Ventricular-Subventricular Zone. Stem Cell Rep. 2016, 7, 735–748.
  38. Son, M.J.; Woolard, K.; Nam, D.-H.; Lee, J.; Fine, H.A. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 2009, 4, 440–452.
  39. Singh, S.K.; Clarke, I.D.; Terasaki, M.; Bonn, V.E.; Hawkins, C.; Squire, J.; Dirks, P.B. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003, 63, 5821–5828.
  40. Mao, X.-G.; Zhang, X.; Xue, X.-Y.; Guo, G.; Wang, P.; Zhang, W.; Fei, Z.; Zhen, H.-N.; You, S.-W.; Yang, H. Brain Tumor Stem-Like Cells Identified by Neural Stem Cell Marker CD15. Transl. Oncol. 2009, 2, 247–257.
  41. Uribe-Etxebarria, V.; Luzuriaga, J.; Garcia-Gallastegui, P.; Agliano, A.; Unda, F.; Ibarretxe, G. Notch/Wnt cross-signalling regulates stemness of dental pulp stem cells through expression of neural crest and core pluripotency factors. Eur. Cell Mater. 2017, 34, 249–270.
  42. Fu, L.; Zhu, L.; Huang, Y.; Lee, T.D.; Forman, S.J.; Shih, C.-C. Derivation of Neural Stem Cells from Mesenchymal Stem Cells: Evidence for a Bipotential Stem Cell Population. Stem Cells Dev. 2008, 17, 1109–1121.
  43. Hiraoka, K.; Hayashi, T.; Kaneko, R.; Nasu-Nishimura, Y.; Koyama-Nasu, R.; Kawasaki, Y.; Akiyama, T. SOX9-mediated upregulation of LGR5 is important for glioblastoma tumorigenicity. Biochem. Biophys. Res. Commun. 2015, 460, 216–221.
  44. Ibarretxe, G.; Crende, O.; Aurrekoetxea, M.; García-Murga, V.; Etxaniz, J.; Unda, F. Neural crest stem cells from dental tissues: A new hope for dental and neural regeneration. Stem Cells Int. 2012, 2012, 103503.
  45. Yu, Y.; Moberly, A.H.; Bhattarai, J.P.; Duan, C.; Zheng, Q.; Li, F.; Huang, H.; Olson, W.; Luo, W.; Wen, T.; et al. The Stem Cell Marker Lgr5 Defines a Subset of Postmitotic Neurons in the Olfactory Bulb. J. Neurosci. 2017, 37, 9403–9414.
  46. Wang, F.; Scoville, D.; He, X.C.; Mahe, M.M.; Box, A.; Perry, J.M.; Smith, N.R.; Lei, N.Y.; Davies, P.S.; Fuller, M.K.; et al. Isolation and characterization of intestinal stem cells based on surface marker combinations and colony-formation assay. Gastroenterology 2013, 145, 383–395.e1–21.
  47. Levin, T.G.; Powell, A.E.; Davies, P.S.; Silk, A.D.; Dismuke, A.D.; Anderson, E.C.; Swain, J.R.; Wong, M.H. Characterization of the intestinal cancer stem cell marker CD166 in the human and mouse gastrointestinal tract. Gastroenterology 2010, 139, 2072–2082.e5.
  48. Kijima, N.; Hosen, N.; Kagawa, N.; Hashimoto, N.; Nakano, A.; Fujimoto, Y.; Kinoshita, M.; Sugiyama, H.; Yoshimine, T. CD166/activated leukocyte cell adhesion molecule is expressed on glioblastoma progenitor cells and involved in the regulation of tumor cell invasion. Neuro-Oncology 2012, 14, 1254–1264.
  49. Ho, S.-Y.; Ling, T.-Y.; Lin, H.-Y.; Liou, J.T.-J.; Liu, F.-C.; Chen, I.-C.; Lee, S.-W.; Hsu, Y.; Lai, D.-M.; Liou, H.-H. SDF-1/CXCR4 Signaling Maintains Stemness Signature in Mouse Neural Stem/Progenitor Cells. Stem Cells Int. 2017, 2017, 2493752.
  50. Yi, L.; Zhou, X.; Li, T.; Liu, P.; Hai, L.; Tong, L.; Ma, H.; Tao, Z.; Xie, Y.; Zhang, C.; et al. Notch1 signaling pathway promotes invasion, self-renewal and growth of glioma initiating cells via modulating chemokine system CXCL12/CXCR4. J. Exp. Clin. Cancer Res. 2019, 38, 339.
  51. Zhang, Q.; Yi, D.-Y.; Xue, B.-Z.; Wen, W.-W.; Lu, Y.-P.; Abdelmaksou, A.; Sun, M.-X.; Yuan, D.-T.; Zhao, H.-Y.; Xiong, N.-X.; et al. CD90 determined two subpopulations of glioma-associated mesenchymal stem cells with different roles in tumour progression. Cell Death Dis. 2018, 9, 1101.
  52. Luzuriaga, J.; Pineda, J.R.; Irastorza, I.; Uribe-Etxebarria, V.; García-Gallastegui, P.; Encinas, J.M.; Chamero, P.; Unda, F.; Ibarretxe, G. BDNF and NT3 Reprogram Human Ectomesenchymal Dental Pulp Stem Cells to Neurogenic and Gliogenic Neural Crest Progenitors Cultured in Serum-Free Medium. Cell. Physiol. Biochem. 2019, 52, 1361–1380.
  53. Zhang, S.; Han, Z.; Jing, Y.; Tao, S.; Li, T.; Wang, H.; Wang, Y.; Li, R.; Yang, Y.; Zhao, X.; et al. CD133(+)CXCR4(+) colon cancer cells exhibit metastatic potential and predict poor prognosis of patients. BMC Med. 2012, 10, 85.
  54. Uribe-Etxebarria, V.; Agliano, A.; Unda, F.; Ibarretxe, G. Wnt signaling reprograms metabolism in dental pulp stem cells. J. Cell. Physiol. 2019, 234, 13068–13082.
  55. Uribe-Etxebarria, V.; García-Gallastegui, P.; Pérez-Garrastachu, M.; Casado-Andrés, M.; Irastorza, I.; Unda, F.; Ibarretxe, G.; Subirán, N. Wnt-3a Induces Epigenetic Remodeling in Human Dental Pulp Stem Cells. Cells 2020, 9, 652.
  56. Aurrekoetxea, M.; Garcia-Gallastegui, P.; Irastorza, I.; Luzuriaga, J.; Uribe-Etxebarria, V.; Unda, F.; Ibarretxe, G. Dental pulp stem cells as a multifaceted tool for bioengineering and the regeneration of craniomaxillofacial tissues. Front. Physiol. 2015, 6.
  57. Asadi, M.H.; Khalifeh, K.; Mowla, S.J. OCT4 spliced variants are highly expressed in brain cancer tissues and inhibition of OCT4B1 causes G2/M arrest in brain cancer cells. J. Neurooncol. 2016, 130, 455–463.
  58. D’ Alimonte, I.; Nargi, E.; Mastrangelo, F.; Falco, G.; Lanuti, P.; Marchisio, M.; Miscia, S.; Robuffo, I.; Capogreco, M.; Buccella, S.; et al. Vascular endothelial growth factor enhances in vitro proliferation and osteogenic differentiation of human dental pulp stem cells. J. Biol. Regul. Homeost. Agents 2011, 25, 57–69.
  59. Jing, F.; Kim, H.J.; Kim, C.H.; Kim, Y.J.; Lee, J.H.; Kim, H.R. Colon cancer stem cell markers CD44 and CD133 in patients with colorectal cancer and synchronous hepatic metastases. Int. J. Oncol. 2015, 46, 1582–1588.
  60. Luzuriaga, J.; Pastor-Alonso, O.; Encinas, J.M.; Unda, F.; Ibarretxe, G.; Pineda, J.R. Human Dental Pulp Stem Cells Grown in Neurogenic Media Differentiate Into Endothelial Cells and Promote Neovasculogenesis in the Mouse Brain. Front. Physiol. 2019, 10, 347.
  61. Zhang, M.; Xu, C.; Wang, H.-Z.; Peng, Y.-N.; Li, H.-O.; Zhou, Y.-J.; Liu, S.; Wang, F.; Liu, L.; Chang, Y.; et al. Soft fibrin matrix downregulates DAB2IP to promote Nanog-dependent growth of colon tumor-repopulating cells. Cell Death Dis. 2019, 10, 151.
  62. Gregorian, C.; Nakashima, J.; Le Belle, J.; Ohab, J.; Kim, R.; Liu, A.; Smith, K.B.; Groszer, M.; Garcia, A.D.; Sofroniew, M.V.; et al. Pten deletion in adult neural stem/progenitor cells enhances constitutive neurogenesis. J. Neurosci. 2009, 29, 1874–1886.
  63. Groszer, M.; Erickson, R.; Scripture-Adams, D.D.; Lesche, R.; Trumpp, A.; Zack, J.A.; Kornblum, H.I.; Liu, X.; Wu, H. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 2001, 294, 2186–2189.
  64. He, X.C.; Yin, T.; Grindley, J.C.; Tian, Q.; Sato, T.; Tao, W.A.; Dirisina, R.; Porter-Westpfahl, K.S.; Hembree, M.; Johnson, T.; et al. PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat. Genet. 2007, 39, 189–198.
  65. Shen, W.-C.; Lai, Y.-C.; Li, L.-H.; Liao, K.; Lai, H.-C.; Kao, S.-Y.; Wang, J.; Chuong, C.-M.; Hung, S.-C. Methylation and PTEN activation in dental pulp mesenchymal stem cells promotes osteogenesis and reduces oncogenesis. Nat. Commun. 2019, 10, 2226.
  66. Pagella, P.; Miran, S.; Neto, E.; Martin, I.; Lamghari, M.; Mitsiadis, T.A. Human dental pulp stem cells exhibit enhanced properties in comparison to human bone marrow stem cells on neurites outgrowth. FASEB J. 2020.
  67. Fan, L.-F.; Dong, W.-G.; Jiang, C.-Q.; Xia, D.; Liao, F.; Yu, Q.-F. Expression of putative stem cell genes Musashi-1 and beta1-integrin in human colorectal adenomas and adenocarcinomas. Int. J. Colorectal Dis. 2010, 25, 17–23.
  68. Paschall, A.V.; Yang, D.; Lu, C.; Redd, P.S.; Choi, J.-H.; Heaton, C.M.; Lee, J.R.; Nayak-Kapoor, A.; Liu, K. CD133+CD24lo defines a 5-Fluorouracil-resistant colon cancer stem cell-like phenotype. Oncotarget 2016, 7, 78698–78712.
  69. Duan, S.; Yuan, G.; Liu, X.; Ren, R.; Li, J.; Zhang, W.; Wu, J.; Xu, X.; Fu, L.; Li, Y.; et al. PTEN deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell-like phenotype. Nat. Commun. 2015, 6, 10068.
  70. Kaneko, Y.; Sakakibara, S.; Imai, T.; Suzuki, A.; Nakamura, Y.; Sawamoto, K.; Ogawa, Y.; Toyama, Y.; Miyata, T.; Okano, H. Musashi1: An evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev. Neurosci. 2000, 22, 139–153.
  71. Carmon, K.S.; Lin, Q.; Gong, X.; Thomas, A.; Liu, Q. LGR5 interacts and cointernalizes with Wnt receptors to modulate Wnt/β-catenin signaling. Mol. Cell. Biol. 2012, 32, 2054–2064.
  72. Lundberg, I.V.; Edin, S.; Eklöf, V.; Öberg, Å.; Palmqvist, R.; Wikberg, M.L. SOX2 expression is associated with a cancer stem cell state and down-regulation of CDX2 in colorectal cancer. BMC Cancer 2016, 16, 471.
  73. Chiou, G.-Y.; Yang, T.-W.; Huang, C.-C.; Tang, C.-Y.; Yen, J.-Y.; Tsai, M.-C.; Chen, H.-Y.; Fadhilah, N.; Lin, C.-C.; Jong, Y.-J. Musashi-1 promotes a cancer stem cell lineage and chemoresistance in colorectal cancer cells. Sci. Rep. 2017, 7, 2172.
  74. Sakakibara, S.; Imai, T.; Hamaguchi, K.; Okabe, M.; Aruga, J.; Nakajima, K.; Yasutomi, D.; Nagata, T.; Kurihara, Y.; Uesugi, S.; et al. Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev. Biol. 1996, 176, 230–242.
  75. Hattermann, K.; Flüh, C.; Engel, D.; Mehdorn, H.M.; Synowitz, M.; Mentlein, R.; Held-Feindt, J. Stem cell markers in glioma progression and recurrence. Int. J. Oncol. 2016, 49, 1899–1910.
  76. Chen, H.-Y.; Lin, L.-T.; Wang, M.-L.; Laurent, B.; Hsu, C.-H.; Pan, C.-M.; Jiang, W.-R.; Chen, P.-Y.; Ma, H.-I.; Chen, Y.-W.; et al. Musashi-1 Enhances Glioblastoma Cell Migration and Cytoskeletal Dynamics through Translational Inhibition of Tensin3. Sci. Rep. 2017, 7, 8710.
  77. Beckervordersandforth, R.; Tripathi, P.; Ninkovic, J.; Bayam, E.; Lepier, A.; Stempfhuber, B.; Kirchhoff, F.; Hirrlinger, J.; Haslinger, A.; Lie, D.C.; et al. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 2010, 7, 744–758.
  78. Lin, J.-C.; Tsai, J.-T.; Chao, T.-Y.; Ma, H.-I.; Liu, W.-H. Musashi-1 Enhances Glioblastoma Migration by Promoting ICAM1 Translation. Neoplasia 2019, 21, 459–468.
  79. Schwartz, P.H.; Bryant, P.J.; Fuja, T.J.; Su, H.; O’Dowd, D.K.; Klassen, H. Isolation and characterization of neural progenitor cells from post-mortem human cortex. J. Neurosci. Res. 2003, 74, 838–851.
  80. Bakopoulou, A.; Apatzidou, D.; Aggelidou, E.; Gousopoulou, E.; Leyhausen, G.; Volk, J.; Kritis, A.; Koidis, P.; Geurtsen, W. Isolation and prolonged expansion of oral mesenchymal stem cells under clinical-grade, GMP-compliant conditions differentially affects “stemness” properties. Stem Cell Res. Ther. 2017, 8, 247.
  81. Hill, R.; Wu, H. PTEN, Stem Cells, and Cancer Stem Cells. J. Biol. Chem. 2009, 284, 11755–11759.
  82. Li, L.; Liu, F.; Ross, A.H. PTEN regulation of neural development and CNS stem cells. J. Cell Biochem. 2003, 88, 24–28.
  83. Amiri, A.; Cho, W.; Zhou, J.; Birnbaum, S.G.; Sinton, C.M.; McKay, R.M.; Parada, L.F. Pten Deletion in Adult Hippocampal Neural Stem/Progenitor Cells Causes Cellular Abnormalities and Alters Neurogenesis. J. Neurosci. 2012, 32, 5880–5890.
  84. Schoumacher, M.; Goldman, R.D.; Louvard, D.; Vignjevic, D.M. Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J. Cell Biol. 2010, 189, 541–556.
  85. Kumar, A.; Bhanja, A.; Bhattacharyya, J.; Jaganathan, B.G. Multiple roles of CD90 in cancer. Tumour Biol. 2016, 37, 11611–11622.
  86. Shafaei, S.; Sharbatdaran, M.; Kamrani, G.; Khafri, S. The association between CD166 detection rate and clinicopathologic parameters of patients with colorectal cancer. Caspian J. Intern. Med. 2013, 4, 768–772.
  87. Chen, J.; Li, Y.; Yu, T.-S.; McKay, R.M.; Burns, D.K.; Kernie, S.G.; Parada, L.F. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012, 488, 522–526.
  88. Li, J.; Wang, R.; Yang, L.; Wu, Q.; Wang, Q.; Nie, Z.; Yu, Y.; Ma, J.; Pan, Q. Knockdown of Nestin inhibits proliferation and migration of colorectal cancer cells. Int. J. Clin. Exp. Pathol. 2015, 8, 6377–6386.
  89. Gervois, P.; Struys, T.; Hilkens, P.; Bronckaers, A.; Ratajczak, J.; Politis, C.; Brone, B.; Lambrichts, I.; Martens, W. Neurogenic maturation of human dental pulp stem cells following neurosphere generation induces morphological and electrophysiological characteristics of functional neurons. Stem Cells Dev. 2015, 24, 296–311.
  90. Martens, W.; Sanen, K.; Georgiou, M.; Struys, T.; Bronckaers, A.; Ameloot, M.; Phillips, J.; Lambrichts, I. Human dental pulp stem cells can differentiate into Schwann cells and promote and guide neurite outgrowth in an aligned tissue-engineered collagen construct in vitro. FASEB J. 2014, 28, 1634–1643.
  91. Parry, P.V.; Engh, J.A. CD90 is identified as a marker for cancer stem cells in high-grade gliomas using tissue microarrays. Neurosurgery 2012, 70, N23–N24.
  92. Yang, X.H.; Wu, Q.L.; Yu, X.B.; Xu, C.X.; Ma, B.F.; Zhang, X.M.; Li, S.N.; Lahn, B.T.; Xiang, A.P. Nestin expression in different tumours and its relevance to malignant grade. J. Clin. Pathol. 2008, 61, 467–473.
  93. Lv, D.; Lu, L.; Hu, Z.; Fei, Z.; Liu, M.; Wei, L.; Xu, J. Nestin Expression Is Associated with Poor Clinicopathological Features and Prognosis in Glioma Patients: An Association Study and Meta-analysis. Mol. Neurobiol. 2017, 54, 727–735.
  94. Ariza, A.; López, D.; Castellà, E.M.; Muñoz, C.; Zújar, M.J.; Mate, J.L. Expression of CD15 in normal and metaplastic Paneth cells of the digestive tract. J. Clin. Pathol. 1996, 49, 474–477.
  95. Park, D.; Xiang, A.P.; Mao, F.F.; Zhang, L.; Di, C.-G.; Liu, X.-M.; Shao, Y.; Ma, B.-F.; Lee, J.-H.; Ha, K.-S.; et al. Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 2010, 28, 2162–2171.
  96. Yadav, V.N.; Zamler, D.; Baker, G.J.; Kadiyala, P.; Erdreich-Epstein, A.; DeCarvalho, A.C.; Mikkelsen, T.; Castro, M.G.; Lowenstein, P.R. CXCR4 increases in-vivo glioma perivascular invasion, and reduces radiation induced apoptosis: A genetic knockdown study. Oncotarget 2016, 7, 83701–83719.
  97. Wu, W.; Cao, J.; Ji, Z.; Wang, J.; Jiang, T.; Ding, H. Co-expression of Lgr5 and CXCR4 characterizes cancer stem-like cells of colorectal cancer. Oncotarget 2016, 7, 81144–81155.
  98. Xiu, G.; Li, X.; Yin, Y.; Li, J.; Li, B.; Chen, X.; Liu, P.; Sun, J.; Ling, B. SDF-1/CXCR4 Augments the Therapeutic Effect of Bone Marrow Mesenchymal Stem Cells in the Treatment of Lipopolysaccharide-Induced Liver Injury by Promoting Their Migration Through PI3K/Akt Signaling Pathway. Cell Transplant. 2020, 29, 963689720929992.
  99. Potdar, P.D.; Jethmalani, Y.D. Human dental pulp stem cells: Applications in future regenerative medicine. World J. Stem Cells 2015, 7, 839–851.
  100. Kim, J.-H.; Jeon, M.; Song, J.-S.; Lee, J.-H.; Choi, B.-J.; Jung, H.-S.; Moon, S.J.; DenBesten, P.K.; Kim, S.-O. Distinctive genetic activity pattern of the human dental pulp between deciduous and permanent teeth. PLoS ONE 2014, 9, e102893.
  101. Hermann, A.; Gastl, R.; Liebau, S.; Popa, M.O.; Fiedler, J.; Boehm, B.O.; Maisel, M.; Lerche, H.; Schwarz, J.; Brenner, R.; et al. Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J. Cell. Sci. 2004, 117, 4411–4422.
  102. Shmelkov, S.V.; Butler, J.M.; Hooper, A.T.; Hormigo, A.; Kushner, J.; Milde, T.; St Clair, R.; Baljevic, M.; White, I.; Jin, D.K.; et al. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J. Clin. Investig. 2008, 118, 2111–2120.
  103. Choi, D.; Lee, H.-W.; Hur, K.-Y.; Kim, J.-J.; Park, G.-S.; Jang, S.-H.; Song, Y.-S.; Jang, K.-S.; Paik, S.-S. Cancer stem cell markers CD133 and CD24 correlate with invasiveness and differentiation in colorectal adenocarcinoma. World J. Gastroenterol. 2009, 15, 2258–2264.
  104. Glumac, P.M.; LeBeau, A.M. The role of CD133 in cancer: A concise review. Clin. Transl. Med. 2018, 7, 18.
  105. Uchida, N.; Buck, D.W.; He, D.; Reitsma, M.J.; Masek, M.; Phan, T.V.; Tsukamoto, A.S.; Gage, F.H.; Weissman, I.L. Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. USA 2000, 97, 14720–14725.
  106. Florek, M.; Haase, M.; Marzesco, A.-M.; Freund, D.; Ehninger, G.; Huttner, W.B.; Corbeil, D. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res. 2005, 319, 15–26.
  107. Virant-Klun, I.; Skerl, P.; Novakovic, S.; Vrtacnik-Bokal, E.; Smrkolj, S. Similar Population of CD133+ and DDX4+ VSEL-Like Stem Cells Sorted from Human Embryonic Stem Cell, Ovarian, and Ovarian Cancer Ascites Cell Cultures: The Real Embryonic Stem Cells? Cells 2019, 8, 706.
  108. Lottaz, C.; Beier, D.; Meyer, K.; Kumar, P.; Hermann, A.; Schwarz, J.; Junker, M.; Oefner, P.J.; Bogdahn, U.; Wischhusen, J.; et al. Transcriptional profiles of CD133+ and CD133- glioblastoma-derived cancer stem cell lines suggest different cells of origin. Cancer Res. 2010, 70, 2030–2040.
  109. Viña-Almunia, J.; Mas-Bargues, C.; Borras, C.; Gambini, J.; El Alami, M.; Sanz-Ros, J.; Peñarrocha, M.; Vina, J. Influence of Partial O₂ Pressure on the Adhesion, Proliferation, and Osteogenic Differentiation of Human Dental Pulp Stem Cells on β-Tricalcium Phosphate Scaffold. Int. J. Oral. Maxillofac. Implants 2017, 32, 1251–1256.
  110. Bonnamain, V.; Thinard, R.; Sergent-Tanguy, S.; Huet, P.; Bienvenu, G.; Naveilhan, P.; Farges, J.-C.; Alliot-Licht, B. Human dental pulp stem cells cultured in serum-free supplemented medium. Front. Physiol 2013, 4.
  111. Lee, T.-C.; Lee, T.-H.; Huang, Y.-H.; Chang, N.-K.; Lin, Y.-J.; Chien, P.-W.C.; Yang, W.-H.; Lin, M.H.-C. Comparison of surface markers between human and rabbit mesenchymal stem cells. PLoS ONE 2014, 9, e111390.
  112. Feng, B.-H.; Liu, A.-G.; Gu, W.-G.; Deng, L.; Cheng, X.-G.; Tong, T.-J.; Zhang, H.-Z. CD133+ subpopulation of the HT1080 human fibrosarcoma cell line exhibits cancer stem-like characteristics. Oncol. Rep. 2013, 30, 815–823.
  113. Irollo, E.; Pirozzi, G. CD133: To be or not to be, is this the real question? Am. J. Transl Res. 2013, 5, 563–581.
  114. Silvestre, D.C.; Pineda, J.R.; Hoffschir, F.; Studler, J.M.; Mouthon, M.A.; Pflumio, F.; Junier, M.P.; Chneiweiss, H.; Boussin, F.D. Alternative lengthening of telomeres in human glioma stem cells. Stem Cells 2011, 29, 440–451.
  115. Hadaegh, Y.; Niknam, M.; Attar, A.; Maharlooei, M.K.; Tavangar, M.S.; Aarabi, A.M.; Monabati, A. Characterization of stem cells from the pulp of unerupted third molar tooth. Indian J. Dent. Res. 2014, 25, 14–21.
  116. Sokol, S.Y. Maintaining embryonic stem cell pluripotency with Wnt signaling. Development 2011, 138, 4341–4350.
  117. Barraud, P.; Stott, S.; Møllgård, K.; Parmar, M.; Björklund, A. In vitro characterization of a human neural progenitor cell coexpressing SSEA4 and CD133. J. Neurosci. Res. 2007, 85, 250–259.
  118. Patru, C.; Romao, L.; Varlet, P.; Coulombel, L.; Raponi, E.; Cadusseau, J.; Renault-Mihara, F.; Thirant, C.; Leonard, N.; Berhneim, A.; et al. CD133, CD15/SSEA-1, CD34 or side populations do not resume tumor-initiating properties of long-term cultured cancer stem cells from human malignant glio-neuronal tumors. BMC Cancer 2010, 10, 66.
  119. Kahlert, U.D.; Bender, N.O.; Maciaczyk, D.; Bogiel, T.; Bar, E.E.; Eberhart, C.G.; Nikkhah, G.; Maciaczyk, J. CD133/CD15 defines distinct cell subpopulations with differential in vitro clonogenic activity and stem cell-related gene expression profile in in vitro propagated glioblastoma multiforme-derived cell line with a PNET-like component. Folia Neuropathol. 2012, 50, 357–368.
  120. Friedman, G.K.; Moore, B.P.; Nan, L.; Kelly, V.M.; Etminan, T.; Langford, C.P.; Xu, H.; Han, X.; Markert, J.M.; Beierle, E.A.; et al. Pediatric medulloblastoma xenografts including molecular subgroup 3 and CD133+ and CD15+ cells are sensitive to killing by oncolytic herpes simplex viruses. Neuro-Oncology 2016, 18, 227–235.
  121. Yudoh, K.; Matsui, H.; Tsuji, H. Nitric oxide induced by tumor cells activates tumor cell adhesion to endothelial cells and permeability of the endothelium in vitro. Clin. Exp. Metastasis 1997, 15, 557–567.
  122. Satoh, J.; Obayashi, S.; Tabunoki, H.; Wakana, T.; Kim, S.U. Stable expression of neurogenin 1 induces LGR5, a novel stem cell marker, in an immortalized human neural stem cell line HB1.F3. Cell. Mol. Neurobiol. 2010, 30, 415–426.
  123. Xu, L.; Lin, W.; Wen, L.; Li, G. Lgr5 in cancer biology: Functional identification of Lgr5 in cancer progression and potential opportunities for novel therapy. Stem Cell Res. Ther. 2019, 10, 219.
  124. Barker, N.; Clevers, H. Tracking down the stem cells of the intestine: Strategies to identify adult stem cells. Gastroenterology 2007, 133, 1755–1760.
  125. de Sousa e Melo, F.; Kurtova, A.V.; Harnoss, J.M.; Kljavin, N.; Hoeck, J.D.; Hung, J.; Anderson, J.E.; Storm, E.E.; Modrusan, Z.; Koeppen, H.; et al. A distinct role for Lgr5+ stem cells in primary and metastatic colon cancer. Nature 2017, 543, 676–680.
  126. Barker, N.; van Es, J.H.; Kuipers, J.; Kujala, P.; van den Born, M.; Cozijnsen, M.; Haegebarth, A.; Korving, J.; Begthel, H.; Peters, P.J.; et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449, 1003–1007.
  127. Snyder, J.C.; Rochelle, L.K.; Marion, S.; Lyerly, H.K.; Barak, L.S.; Caron, M.G. Lgr4 and Lgr5 drive the formation of long actin-rich cytoneme-like membrane protrusions. J. Cell Sci. 2015, 128, 1230–1240.
  128. Lin, W.; Xu, L.; Lin, S.; Shi, L.; Wang, B.; Pan, Q.; Lee, W.Y.W.; Li, G. Characterisation of multipotent stem cells from human peripheral blood using an improved protocol. J. Orthop. Translat. 2019, 19, 18–28.
  129. Rot, S.; Taubert, H.; Bache, M.; Greither, T.; Würl, P.; Eckert, A.W.; Schubert, J.; Vordermark, D.; Kappler, M. A novel splice variant of the stem cell marker LGR5/GPR49 is correlated with the risk of tumor-related death in soft-tissue sarcoma patients. BMC Cancer 2011, 11, 429.
  130. Ganju, R.K.; Brubaker, S.A.; Meyer, J.; Dutt, P.; Yang, Y.; Qin, S.; Newman, W.; Groopman, J.E. The alpha-chemokine, stromal cell-derived factor-1alpha, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways. J. Biol. Chem. 1998, 273, 23169–23175.
  131. Li, M.; Sun, X.; Ma, L.; Jin, L.; Zhang, W.; Xiao, M.; Yu, Q. SDF-1/CXCR4 axis induces human dental pulp stem cell migration through FAK/PI3K/Akt and GSK3β/β-catenin pathways. Sci. Rep. 2017, 7, 40161.
  132. Su, W.; Foster, S.C.; Xing, R.; Feistel, K.; Olsen, R.H.J.; Acevedo, S.F.; Raber, J.; Sherman, L.S. CD44 Transmembrane Receptor and Hyaluronan Regulate Adult Hippocampal Neural Stem Cell Quiescence and Differentiation. J. Biol. Chem. 2017, 292, 4434–4445.
  133. Nishikawa, M.; Inoue, A.; Ohnishi, T.; Kohno, S.; Ohue, S.; Matsumoto, S.; Suehiro, S.; Yamashita, D.; Ozaki, S.; Watanabe, H.; et al. Significance of Glioma Stem-Like Cells in the Tumor Periphery That Express High Levels of CD44 in Tumor Invasion, Early Progression, and Poor Prognosis in Glioblastoma. Stem Cells Int. 2018, 2018, 5387041.
  134. Rimkus, T.K.; Carpenter, R.L.; Sirkisoon, S.; Zhu, D.; Pasche, B.C.; Chan, M.D.; Lesser, G.J.; Tatter, S.B.; Watabe, K.; Debinski, W.; et al. Truncated Glioma-Associated Oncogene Homolog 1 (tGLI1) Mediates Mesenchymal Glioblastoma via Transcriptional Activation of CD44. Cancer Res. 2018, 78, 2589–2600.
  135. Wang, H.-H.; Liao, C.-C.; Chow, N.-H.; Huang, L.L.-H.; Chuang, J.-I.; Wei, K.-C.; Shin, J.-W. Whether CD44 is an applicable marker for glioma stem cells. Am. J. Transl Res. 2017, 9, 4785–4806.
  136. Macrin, D.; Alghadeer, A.; Zhao, Y.T.; Miklas, J.W.; Hussein, A.M.; Detraux, D.; Robitaille, A.M.; Madan, A.; Moon, R.T.; Wang, Y.; et al. Metabolism as an early predictor of DPSCs aging. Sci. Rep. 2019, 9, 2195.
  137. Singh, S.K.; Hawkins, C.; Clarke, I.D.; Squire, J.A.; Bayani, J.; Hide, T.; Henkelman, R.M.; Cusimano, M.D.; Dirks, P.B. Identification of human brain tumour initiating cells. Nature 2004, 432, 396–401.
  138. Ehrmann, J.; Kolár, Z.; Mokry, J. Nestin as a diagnostic and prognostic marker: Immunohistochemical analysis of its expression in different tumours. J. Clin. Pathol. 2005, 58, 222–223.
  139. Amoh, Y.; Yang, M.; Li, L.; Reynoso, J.; Bouvet, M.; Moossa, A.R.; Katsuoka, K.; Hoffman, R.M. Nestin-linked green fluorescent protein transgenic nude mouse for imaging human tumor angiogenesis. Cancer Res. 2005, 65, 5352–5357.
  140. Potten, C.S.; Booth, C.; Tudor, G.L.; Booth, D.; Brady, G.; Hurley, P.; Ashton, G.; Clarke, R.; Sakakibara, S.; Okano, H. Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation 2003, 71, 28–41.
  141. Wang, Y.; Jiang, C.-Q.; Fan, L.-F. Correlation of Musashi-1, Lgr5, and pEGFR expressions in human small intestinal adenocarcinomas. Tumour Biol. 2015, 36, 6075–6082.
  142. Padial-Molina, M.; de Buitrago, J.G.; Sainz-Urruela, R.; Abril-Garcia, D.; Anderson, P.; O’Valle, F.; Galindo-Moreno, P. Expression of Musashi-1 During Osteogenic Differentiation of Oral MSC: An In Vitro Study. Int. J. Mol. Sci. 2019, 20, 2171.
  143. Zhang, S.; Cui, W. Sox2, a key factor in the regulation of pluripotency and neural differentiation. World J. Stem Cells 2014, 6, 305–311.
  144. Wen, K.; Fu, Z.; Wu, X.; Feng, J.; Chen, W.; Qian, J. Oct-4 is required for an antiapoptotic behavior of chemoresistant colorectal cancer cells enriched for cancer stem cells: Effects associated with STAT3/Survivin. Cancer Lett. 2013, 333, 56–65.
  145. Vincent, P.H.; Benedikz, E.; Uhlén, P.; Hovatta, O.; Sundström, E. Expression of Pluripotency Markers in Nonpluripotent Human Neural Stem and Progenitor Cells. Stem Cells Dev. 2017, 26, 876–887.
  146. Liu, T.; Xu, H.; Huang, M.; Ma, W.; Saxena, D.; Lustig, R.A.; Alonso-Basanta, M.; Zhang, Z.; O’Rourke, D.M.; Zhang, L.; et al. Circulating Glioma Cells Exhibit Stem Cell-like Properties. Cancer Res. 2018, 78, 6632–6642.
  147. Schubert, M.; Holland, L.Z. The Wnt Gene Family and the Evolutionary Conservation of Wnt Expression; Landes Bioscience: Austin, TX, USA, 2013.
  148. González-Sancho, J.M.; Aguilera, O.; García, J.M.; Pendás-Franco, N.; Peña, C.; Cal, S.; García de Herreros, A.; Bonilla, F.; Muñoz, A. The Wnt antagonist DICKKOPF-1 gene is a downstream target of beta-catenin/TCF and is downregulated in human colon cancer. Oncogene 2005, 24, 1098–1103.
  149. Jung, Y.-S.; Park, J.-I. Wnt signaling in cancer: Therapeutic targeting of Wnt signaling beyond β-catenin and the destruction complex. Exp. Mol. Med. 2020, 52, 183–191.
  150. Duchartre, Y.; Kim, Y.-M.; Kahn, M. The Wnt signaling pathway in cancer. Crit. Rev. Oncol. Hematol. 2016, 99, 141–149.
  151. Zhang, L.; Shay, J.W. Multiple Roles of APC and its Therapeutic Implications in Colorectal Cancer. J. Natl. Cancer Inst. 2017, 109.
  152. de Roo, J.J.D.; Breukel, C.; Chhatta, A.R.; Linssen, M.M.; Vloemans, S.A.; Salvatori, D.; Mikkers, H.M.M.; Verbeek, S.J.; Staal, F.J.T. Axin2-mTurquoise2: A novel reporter mouse model for the detection of canonical Wnt signalling. Genesis 2017, 55.
  153. Kim, B.-M.; Mao, J.; Taketo, M.M.; Shivdasani, R.A. Phases of canonical Wnt signaling during the development of mouse intestinal epithelium. Gastroenterology 2007, 133, 529–538.
  154. Haegebarth, A.; Clevers, H. Wnt signaling, lgr5, and stem cells in the intestine and skin. Am. J. Pathol. 2009, 174, 715–721.
  155. Kahlert, U.D.; Mooney, S.M.; Natsumeda, M.; Steiger, H.-J.; Maciaczyk, J. Targeting cancer stem-like cells in glioblastoma and colorectal cancer through metabolic pathways. Int. J. Cancer 2017, 140, 10–22.
  156. Lie, D.-C.; Colamarino, S.A.; Song, H.-J.; Désiré, L.; Mira, H.; Consiglio, A.; Lein, E.S.; Jessberger, S.; Lansford, H.; Dearie, A.R.; et al. Wnt signalling regulates adult hippocampal neurogenesis. Nature 2005, 437, 1370–1375.
  157. Zhou, F.; Cao, W.; Xu, R.; Zhang, J.; Yu, T.; Xu, X.; Zhi, T.; Yin, J.; Cao, S.; Liu, N.; et al. MicroRNA-206 attenuates glioma cell proliferation, migration, and invasion by blocking the WNT/β-catenin pathway via direct targeting of Frizzled 7 mRNA. Am. J. Transl Res. 2019, 11, 4584–4601.
  158. Augustin, I.; Goidts, V.; Bongers, A.; Kerr, G.; Vollert, G.; Radlwimmer, B.; Hartmann, C.; Herold-Mende, C.; Reifenberger, G.; von Deimling, A.; et al. The Wnt secretion protein Evi/Gpr177 promotes glioma tumourigenesis. EMBO Mol. Med. 2012, 4, 38–51.
  159. Yu, J.M.; Jun, E.S.; Jung, J.S.; Suh, S.Y.; Han, J.Y.; Kim, J.Y.; Kim, K.W.; Jung, J.S. Role of Wnt5a in the proliferation of human glioblastoma cells. Cancer Lett. 2007, 257, 172–181.
  160. Zuccarini, M.; Giuliani, P.; Ziberi, S.; Carluccio, M.; Iorio, P.D.; Caciagli, F.; Ciccarelli, R. The Role of Wnt Signal in Glioblastoma Development and Progression: A Possible New Pharmacological Target for the Therapy of This Tumor. Genes 2018, 9, 105.
  161. Shevchenko, V.; Arnotskaya, N.; Korneyko, M.; Zaytsev, S.; Khotimchenko, Y.; Sharma, H.; Bryukhovetskiy, I. Proteins of the Wnt signaling pathway as targets for the regulation of CD133+ cancer stem cells in glioblastoma. Oncol. Rep. 2019, 41, 3080–3088.
  162. Gonçalves, C.S.; Vieira de Castro, J.; Pojo, M.; Martins, E.P.; Queirós, S.; Chautard, E.; Taipa, R.; Pires, M.M.; Pinto, A.A.; Pardal, F.; et al. WNT6 is a novel oncogenic prognostic biomarker in human glioblastoma. Theranostics 2018, 8, 4805–4823.
  163. Portela, M.; Venkataramani, V.; Fahey-Lozano, N.; Seco, E.; Losada-Perez, M.; Winkler, F.; Casas-Tintó, S. Glioblastoma cells vampirize WNT from neurons and trigger a JNK/MMP signaling loop that enhances glioblastoma progression and neurodegeneration. PLoS Biol. 2019, 17, e3000545.
  164. Rajakulendran, N.; Rowland, K.J.; Selvadurai, H.J.; Ahmadi, M.; Park, N.I.; Naumenko, S.; Dolma, S.; Ward, R.J.; So, M.; Lee, L.; et al. Wnt and Notch signaling govern self-renewal and differentiation in a subset of human glioblastoma stem cells. Genes Dev. 2019, 33, 498–510.
  165. Oskarsson, T.; Batlle, E.; Massagué, J. Metastatic stem cells: Sources, niches, and vital pathways. Cell Stem Cell 2014, 14, 306–321.
  166. Valdor, R.; García-Bernal, D.; Riquelme, D.; Martinez, C.M.; Moraleda, J.M.; Cuervo, A.M.; Macian, F.; Martinez, S. Glioblastoma ablates pericytes antitumor immune function through aberrant up-regulation of chaperone-mediated autophagy. Proc. Natl. Acad. Sci. USA 2019, 116, 20655–20665.
  167. Sakaki-Yumoto, M.; Katsuno, Y.; Derynck, R. TGF-β family signaling in stem cells. Biochim. Biophys. Acta 2013, 1830, 2280–2296.
  168. Weiss, A.; Attisano, L. The TGFbeta superfamily signaling pathway. Wiley Interdiscip Rev. Dev. Biol. 2013, 2, 47–63.
  169. Daynac, M.; Pineda, J.R.; Chicheportiche, A.; Gauthier, L.R.; Morizur, L.; Boussin, F.D.; Mouthon, M.-A. TGFβ lengthens the G1 phase of stem cells in aged mouse brain. Stem Cells 2014, 32, 3257–3265.
  170. Pineda, J.R.; Daynac, M.; Chicheportiche, A.; Cebrian-Silla, A.; Sii Felice, K.; Garcia-Verdugo, J.M.; Boussin, F.D.; Mouthon, M.-A. Vascular-derived TGF-β increases in the stem cell niche and perturbs neurogenesis during aging and following irradiation in the adult mouse brain. EMBO Mol. Med. 2013, 5, 548–562.
  171. Mani, S.A.; Guo, W.; Liao, M.-J.; Eaton, E.N.; Ayyanan, A.; Zhou, A.Y.; Brooks, M.; Reinhard, F.; Zhang, C.C.; Shipitsin, M.; et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133, 704–715.
  172. Flanders, K.C.; Ren, R.F.; Lippa, C.F. Transforming growth factor-betas in neurodegenerative disease. Prog. Neurobiol. 1998, 54, 71–85.
  173. Derynck, R.; Goeddel, D.V.; Ullrich, A.; Gutterman, J.U.; Williams, R.D.; Bringman, T.S.; Berger, W.H. Synthesis of messenger RNAs for transforming growth factors alpha and beta and the epidermal growth factor receptor by human tumors. Cancer Res. 1987, 47, 707–712.
  174. TGFβ Promotes Immune Evasion to Limit the Efficacy of Anti-PD-1/PD-L1. Cancer Discov 2018, 8, OF10.
  175. Platten, M.; Wick, W.; Weller, M. Malignant glioma biology: Role for TGF-beta in growth, motility, angiogenesis, and immune escape. Microsc. Res. Tech. 2001, 52, 401–410.
  176. Derynck, R.; Akhurst, R.J.; Balmain, A. TGF-beta signaling in tumor suppression and cancer progression. Nat. Genet. 2001, 29, 117–129.
  177. Bellomo, C.; Caja, L.; Moustakas, A. Transforming growth factor β as regulator of cancer stemness and metastasis. Br. J. Cancer 2016, 115, 761–769.
  178. Vallier, L.; Mendjan, S.; Brown, S.; Chng, Z.; Teo, A.; Smithers, L.E.; Trotter, M.W.B.; Cho, C.H.-H.; Martinez, A.; Rugg-Gunn, P.; et al. Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development 2009, 136, 1339–1349.
  179. Liu, J.; Jin, T.; Chang, S.; Ritchie, H.H.; Smith, A.J.; Clarkson, B.H. Matrix and TGF-beta-related gene expression during human dental pulp stem cell (DPSC) mineralization. In Vitro Cell. Dev. Biol. Anim. 2007, 43, 120–128.
  180. Qi, Z.; Li, Y.; Zhao, B.; Xu, C.; Liu, Y.; Li, H.; Zhang, B.; Wang, X.; Yang, X.; Xie, W.; et al. BMP restricts stemness of intestinal Lgr5+ stem cells by directly suppressing their signature genes. Nat. Commun. 2017, 8, 13824.
  181. Ahmadi, A.; Najafi, M.; Farhood, B.; Mortezaee, K. Transforming growth factor-β signaling: Tumorigenesis and targeting for cancer therapy. J. Cell. Physiol. 2019, 234, 12173–12187.
  182. Zhou, X.; Geng, L.; Wang, D.; Yi, H.; Talmon, G.; Wang, J. R-Spondin1/LGR5 Activates TGFβ Signaling and Suppresses Colon Cancer Metastasis. Cancer Res. 2017, 77, 6589–6602.
  183. Calon, A.; Espinet, E.; Palomo-Ponce, S.; Tauriello, D.V.F.; Iglesias, M.; Céspedes, M.V.; Sevillano, M.; Nadal, C.; Jung, P.; Zhang, X.H.-F.; et al. Dependency of colorectal cancer on a TGF-β-driven program in stromal cells for metastasis initiation. Cancer Cell 2012, 22, 571–584.
  184. Ulaner, G.A.; Hu, J.F.; Vu, T.H.; Giudice, L.C.; Hoffman, A.R. Telomerase activity in human development is regulated by human telomerase reverse transcriptase (hTERT) transcription and by alternate splicing of hTERT transcripts. Cancer Res. 1998, 58, 4168–4172.
  185. Chen, K.; Chen, L.; Li, L.; Qu, S.; Yu, B.; Sun, Y.; Wan, F.; Chen, X.; Liang, R.; Zhu, X. A positive feedback loop between Wnt/β-catenin signaling and hTERT regulates the cancer stem cell-like traits in radioresistant nasopharyngeal carcinoma cells. J. Cell. Biochem. 2020.
  186. Park, J.-I.; Venteicher, A.S.; Hong, J.Y.; Choi, J.; Jun, S.; Shkreli, M.; Chang, W.; Meng, Z.; Cheung, P.; Ji, H.; et al. Telomerase modulates Wnt signalling by association with target gene chromatin. Nature 2009, 460, 66–72.
  187. Saha, A.; Shree Padhi, S.; Roy, S.; Banerjee, B. HCT116 colonospheres shows elevated expression of hTERT and β-catenin protein—A short report. J. Stem Cells 2014, 9, 243–251.
  188. Kerem Terali, K. On the Far Side of Telomeres: The Many Roles of Telomerase in the Acquisition and Retention of Cancer Stemness. In Telomere—A Complex End of a Chromosome; Intechopen: London, UK, 2016; pp. 1–28. ISBN 978-953-51-2753-6.
  189. Rhyu, M.S. Telomeres, telomerase, and immortality. J. Natl. Cancer Inst. 1995, 87, 884–894.
  190. Beck, S.; Jin, X.; Sohn, Y.-W.; Kim, J.-K.; Kim, S.-H.; Yin, J.; Pian, X.; Kim, S.-C.; Nam, D.-H.; Choi, Y.-J.; et al. Telomerase Activity-Independent Function of TERT Allows Glioma Cells to Attain Cancer Stem Cell Characteristics by Inducing EGFR Expression. Mol. Cells 2011, 31, 9–15.
  191. Gunes, C.; Avila, A.I.; Rudolph, K.L. Telomeres in cancer. Differentiation 2018, 99, 41–50.
  192. Tanaka, K.; Hirota, T. Chromosomal instability: A common feature and a therapeutic target of cancer. Biochim. Biophys. Acta 2016, 1866, 64–75.
  193. McClelland, S.E. Role of chromosomal instability in cancer progression. Endocr. Relat. Cancer 2017, 24, T23–T31.
  194. Ishaq, A.; Hanson, P.S.; Morris, C.M.; Saretzki, G. Telomerase Activity is Downregulated Early During Human Brain Development. Genes 2016, 7, 27.
  195. Hiyama, E.; Hiyama, K. Telomere and telomerase in stem cells. Br. J. Cancer 2007, 96, 1020–1024.
  196. Schepers, A.G.; Vries, R.; van den Born, M.; van de Wetering, M.; Clevers, H. Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes. EMBO J. 2011, 30, 1104–1109.
  197. Ninagawa, N.; Murakami, R.; Isobe, E.; Tanaka, Y.; Nakagawa, H.; Torihashi, S. Mesenchymal stem cells originating from ES cells show high telomerase activity and therapeutic benefits. Differentiation 2011, 82, 153–164.
  198. Horibe, H.; Murakami, M.; Iohara, K.; Hayashi, Y.; Takeuchi, N.; Takei, Y.; Kurita, K.; Nakashima, M. Isolation of a stable subpopulation of mobilized dental pulp stem cells (MDPSCs) with high proliferation, migration, and regeneration potential is independent of age. PLoS ONE 2014, 9, e98553.
  199. Jeon, B.-G.; Kang, E.-J.; Kumar, B.M.; Maeng, G.-H.; Ock, S.-A.; Kwack, D.-O.; Park, B.-W.; Rho, G.-J. Comparative analysis of telomere length, telomerase and reverse transcriptase activity in human dental stem cells. Cell Transplant. 2011, 20, 1693–1705.
  200. Caporaso, G.L.; Lim, D.A.; Alvarez-Buylla, A.; Chao, M.V. Telomerase activity in the subventricular zone of adult mice. Mol. Cell Neurosci. 2003, 23, 693–702.
  201. Ferrón, S.; Mira, H.; Franco, S.; Cano-Jaimez, M.; Bellmunt, E.; Ramírez, C.; Fariñas, I.; Blasco, M.A. Telomere shortening and chromosomal instability abrogates proliferation of adult but not embryonic neural stem cells. Development 2004, 131, 4059–4070.
  202. Ferrón, S.R.; Marqués-Torrejón, M.A.; Mira, H.; Flores, I.; Taylor, K.; Blasco, M.A.; Fariñas, I. Telomere shortening in neural stem cells disrupts neuronal differentiation and neuritogenesis. J. Neurosci. 2009, 29, 14394–14407.
  203. Liu, M.-Y.; Nemes, A.; Zhou, Q.-G. The Emerging Roles for Telomerase in the Central Nervous System. Front. Mol. Neurosci. 2018, 11, 160.
  204. Miura, T.; Katakura, Y.; Yamamoto, K.; Uehara, N.; Tsuchiya, T.; Kim, E.H.; Shirahata, S. Neural stem cells lose telomerase activity upon differentiating into astrocytes. Cytotechnology 2001, 36, 137–144.
  205. Kim, N.W.; Piatyszek, M.A.; Prowse, K.R.; Harley, C.B.; West, M.D.; Ho, P.L.; Coviello, G.M.; Wright, W.E.; Weinrich, S.L.; Shay, J.W. Specific association of human telomerase activity with immortal cells and cancer. Science 1994, 266, 2011–2015.
  206. Zhao, S.; Wang, F.; Liu, L. Alternative Lengthening of Telomeres (ALT) in Tumors and Pluripotent Stem Cells. Genes 2019, 10, 1030.
  207. Arnoult, N.; Karlseder, J. ALT telomeres borrow from meiosis to get moving. Cell 2014, 159, 11–12.
  208. Farooqi, A.; Yang, J.; Sharin, V.; Ezhilarasan, R.; Danussi, C.; Alvarez, C.; Dharmaiah, S.; Irvin, D.; Huse, J.; Sulman, E.P. Identification of patient-derived glioblastoma stem cell (GSC) lines with the alternative lengthening of telomeres phenotype. Acta Neuropathol. Commun 2019, 7, 76.
  209. Lafferty-Whyte, K.; Cairney, C.J.; Will, M.B.; Serakinci, N.; Daidone, M.-G.; Zaffaroni, N.; Bilsland, A.; Keith, W.N. A gene expression signature classifying telomerase and ALT immortalization reveals an hTERT regulatory network and suggests a mesenchymal stem cell origin for ALT. Oncogene 2009, 28, 3765–3774.
  210. Pompili, L.; Maresca, C.; Dello Stritto, A.; Biroccio, A.; Salvati, E. BRCA2 Deletion Induces Alternative Lengthening of Telomeres in Telomerase Positive Colon Cancer Cells. Genes 2019, 10, 697.
  211. Heaphy, C.M.; Subhawong, A.P.; Hong, S.-M.; Goggins, M.G.; Montgomery, E.A.; Gabrielson, E.; Netto, G.J.; Epstein, J.I.; Lotan, T.L.; Westra, W.H.; et al. Prevalence of the Alternative Lengthening of Telomeres Telomere Maintenance Mechanism in Human Cancer Subtypes. Am. J. Pathol. 2011, 179, 1608–1615.
  212. Lawlor, R.T.; Veronese, N.; Pea, A.; Nottegar, A.; Smith, L.; Pilati, C.; Demurtas, J.; Fassan, M.; Cheng, L.; Luchini, C. Alternative lengthening of telomeres (ALT) influences survival in soft tissue sarcomas: A systematic review with meta-analysis. BMC Cancer 2019, 19, 232.
  213. Venturini, L.; Motta, R.; Gronchi, A.; Daidone, M.; Zaffaroni, N. Prognostic relevance of ALT-associated markers in liposarcoma: A comparative analysis. BMC Cancer 2010, 10, 254.
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