Personalized regulation of glioblastoma cancer stem cells based on biomedical technologies: From theory to experiment (Review)
- Authors:
- Igor Bryukhovetskiy
- Arina Ponomarenko
- Irina Lyakhova
- Sergey Zaitsev
- Yulia Zayats
- Maria Korneyko
- Marina Eliseikina
- Polina Mischenko
- Valerie Shevchenko
- Hari Shanker Sharma
- Aruna Sharma
- Yuri Khotimchenko
-
Affiliations: Far Eastern Federal University, Vladivostok 690091, Russia, National Scientific Center of Marine Biology of Far Eastern Branch of The Russian Academy of Sciences, Vladivostok 690059, Russia, International Experimental CNS Injury & Repair (IECNSIR), Department of Surgical Sciences, Anesthesiology & Intensive Care Medicine, University Hospital, Uppsala University, Uppsala SE‑75185, Sweden - Published online on: May 10, 2018 https://doi.org/10.3892/ijmm.2018.3668
- Pages: 691-702
-
Copyright: © Bryukhovetskiy et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 4.0].
This article is mentioned in:
Abstract
 |
 |
 |
 |
 |
|
Stupp R, Toms SA and Kesari S: Treatment for patients with newly diagnosed glioblastoma-reply. JAMA. 315:2348–2349. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Omuro A and DeAngelis LM: Glioblastoma and other malignant gliomas: A clinical review. JAMA. 310:1842–1850. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P and Ellison DW: The 2016 World Health Organization classification of tumors of the central nervous system: A summary. Acta Neuropathol. 131:803–820. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
DeWitt JC, Mock A and Louis DN: The 2016 WHO classification of central nervous system tumors: What neurologists need to know. Curr Opin Neurol. 30:643–649. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Louis DN, Perry A, Burger P, Ellison DW, Reifenberger G, von Deimling A, Aldape K, Brat D, Collins VP, Eberhart C, et al: International society of Neuropathology-haarlem consensus guidelines for nervous system tumor classification and grading. Brain Pathol. 24:429–435. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Abou-Antoun TJ, Hale JS, Lathia JD and Dombrowski SM: Brain cancer stem cells in adults and children: Cell biology and therapeutic implications. Neurotherapeutics. 14:372–384. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Dirks PB: Cancer: Stem cells and brain tumours. Nature. 444:687–688. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Baba E and Akashi K: The fundamental concept of cancer stem cell and the progress in cancer stem cell research. Nihon Rinsho. 73:721–725. 2015.In Japanese. PubMed/NCBI | |
|
Duesberg P, Mandrioli D, McCormack A and Nicholson JM: Is carcinogenesis a form of speciation. Cell Cycle. 10:2100–2114. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Bryukhovetskiy A, Shevchenko V, Kovalev S, Chekhonin V, Baklaushev V, Bryukhovetskiy I and Zhukova M: To the novel paradigm of proteome-based cell therapy of tumors: Through comparative proteome mapping of tumor stem cells and tissue-specific stem cells of humans. Cell Transplant. 23(Suppl 1): S151–S170. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW and Kleihues P: The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 114:97–109. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al: Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 17:98–110. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Crespo I, Vital AL, Gonzalez-Tablas M, Patino Mdel C, Otero A, Lopes MC, de Oliveira C, Domingues P, Orfao A and Tabernero MD: Molecular and genomic alterations in glioblastoma multiforme. Am J Pathol. 185:1820–1833. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Thakkar JP, Dolecek TA, Horbinski C, Ostrom QT, Lightner DD, Barnholtz-Sloan JS and Villano JL: Epidemiologic and molecular prognostic review of glioblastoma. Cancer Epidemiol Biomarkers Prev. 23:1985–1996. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Rispoli R, Conti C, Celli P, Caroli E and Carletti S: Neural stem cells and glioblastoma. Neuroradiol J. 27:169–174. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Brown DV, Daniel PM, D'Abaco GM, Gogos A, Ng W, Morokoff AP and Mantamadiotis T: Coexpression analysis of CD133 and CD44 identifies proneural and mesenchymal subtypes of glioblastoma multiforme. Oncotarget. 6:6267–6280. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Bradshaw A, Wickremsekera A, Tan ST Peng L, Davis PF and Itinteang T: Cancer stem cell hierarchy in glioblastoma multiforme. Front Surg. 3:212016.PubMed/NCBI | |
|
Bradshaw A, Wickremesekera A, Brasch HD, Chibnall AM, Davis PF, Tan ST and Itinteang T: Cancer stem cells in glioblastoma multiforme. Front Surg. 3:482016.PubMed/NCBI | |
|
Osswald M, Jung E, Sahm F, Solecki G, Venkataramani V, Blaes J, Weil S, Horstmann H, Wiestler B, Syed M, et al: Brain tumour cells interconnect to a functional and resistant network. Nature. 528:93–98. 2015.PubMed/NCBI | |
|
Weil S, Osswald M, Solecki G, Grosch J, Jung E, Lemke D, Ratliff M, Hänggi D, Wick W and Winkler F: Tumor micro-tubes convey resistance to surgical lesions and chemotherapy in gliomas. Neuro Oncol. 19:1316–1326. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Sontheimer H: Brain cancer: Tumour cells on neighbourhood watch. Nature. 528:49–50. 2015.PubMed/NCBI | |
|
Murphy SF, Varghese RT, Lamouille S, Guo S, Pridham KJ, Kanabur P, Osimani AM, Sharma S, Jourdan J, Rodgers CM, et al: Connexin 43 inhibition sensitizes chemoresistant glioblastoma cells to Temozolomide. Cancer Res. 76:139–149. 2016. View Article : Google Scholar : | |
|
Hambardzumyan D and Bergers G: Glioblastoma: Defining tumor Niches. Trends Cancer. 1:252–265. 2015. View Article : Google Scholar | |
|
Milkina EV, Mischenko PV, Zaytsev SV, et al: Features of interaction between hematopoietic stem and tumor cells of different lines in vitro. Gens and Cells. XI:63–71. 2016.In Russian. | |
|
Luo M, Brooks M and Wicha MS: Epithelial-mesenchymal plasticity of breast cancer stem cells: Implications for metastasis and therapeutic resistance. Curr Pharm Des. 21:1301–1310. 2015. View Article : Google Scholar : | |
|
Chow KH, Park HJ, George J, Yamamoto K, Gallup AD, Graber JH, Chen Y, Jiang W, Steindler DA, Neilson EG, et al: S100A4 is a biomarker and regulator of glioma stem cells that is critical for mesenchymal transition in glioblastoma. Cancer Res. 77:5360–5373. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Bryukhovetskiy I and Shevchenko V: Molecular mechanisms of the effect of TGF-β1 on U87 human glioblastoma cells. Oncol Lett. 12:1581–1590. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Li P, Zhou C, Xu L and Xiao H: Hypoxia enhances stemness of cancer stem cells in glioblastoma: An in vitro study. Int J Med Sci. 10:399–407. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Morel AP, Lièvre M, Thomas C, Hinkal G, Ansieau S and Puisieux A: Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One. 3:e28882008. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang N, Hong B, Zhou C, Du X, Chen S, Deng X, Duoerkun S, Li Q, Yang Y and Gong K: Cobalt chloride-induced hypoxia induces epithelial-mesenchymal transition in renal carcinoma cell lines. Ann Clin Lab Sci. 47:40–46. 2017.PubMed/NCBI | |
|
Yang SW, Zhang ZG, Hao YX, Zhao YL, Qian F, Shi Y, Li PA, Liu CY and Yu PW: HIF-1α induces the epithelial-mesenchymal transition in gastric cancer stem cells through the Snail pathway. Oncotarget. 8:9535–9545. 2017.PubMed/NCBI | |
|
Sun LL, Song Z, Li WZ and Tang SY: Hypoxia facilitates epithelial-mesenchymal transition-mediated rectal cancer progress. Genet Mol Res. 15:2016. View Article : Google Scholar | |
|
Li D, Qu C, Ning Z, Wang H, Zang K, Zhuang L, Chen L, Wang P and Meng Z: Radiation promotes epithelial-to-mesenchymal transition and invasion of pancreatic cancer cell by activating carcinoma-associated fibroblasts. Am J Cancer Res. 6:2192–2206. 2016.PubMed/NCBI | |
|
Lehmann S, Te Boekhorst V, Odenthal J, Bianchi R, van Helvert S, Ikenberg K, Ilina O, Stoma S, Xandry J, Jiang L, et al: Hypoxia induces a HIF-1-dependent transition from collective-to-amoeboid dissemination in epithelial cancer cells. Curr Biol. 27:392–400. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Libby CJ, Tran AN, Scott SE, Griguer C and Hjelmeland AB: The pro-tumorigenic effects of metabolic alterations in glioblastoma including brain tumor initiating cells. Biochim Biophys Acta. 1869:175–188. 2018.PubMed/NCBI | |
|
Massagué J: TGFbeta in cancer. Cell. 134:215–230. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Toyonaga T, Yamaguchi S, Hirata K, Kobayashi K, Manabe O, Watanabe S, Terasaka S, Kobayashi H, Hattori N, Shiga T, et al: Hypoxic glucose metabolism in glioblastoma as a potential prognostic factor. Eur J Nucl Med Mol Imaging. 44:611–619. 2017. View Article : Google Scholar | |
|
Bar EE, Lin A, Mahairaki V, Matsui W and Eberhart CG: Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres. Am J Pathol. 177:1491–1502. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Konovalov AN, Potapov AA, Loshakov VA, et al: Standards, options and recommendations in the treatment of CNS tumors. Assoc Neurosurg Russia. 2009.In Russian. | |
|
Scott JG, Berglund A, Schell MJ, Mihaylov I, Fulp WJ, Yue B, Welsh E, Caudell JJ, Ahmed K, Strom TS, et al: A genome-based model for adjusting radiotherapy dose (GARD): A retrospective, cohort-based study. Lancet Oncol. 18:202–211. 2017. View Article : Google Scholar | |
|
Dincoglan F, Beyzadeoglu M, Sager O, Demiral S, Gamsiz H, Uysal B, Ebruli C, Akin M, Oysul K, Sirin S and Dirican B: Management of patients with recurrent glioblastoma using hypofractionated stereotactic radiotherapy. Tumori. 101:179–184. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Wang P, Lan C, Xiong S, Zhao X, Shan Y, Hu R, Wan W, Yu S, Liao B, Li G, et al: HIF1α regulates single differentiated glioma cell dedifferentiation to stem-like cell phenotypes with high tumorigenic potential under hypoxia. Oncotarget. 8:28074–28092. 2017.PubMed/NCBI | |
|
Colwell N, Larion M, Giles AJ, Seldomridge AN, Sizdahkhani S, Gilbert MR and Park DM: Hypoxia in the glioblastoma micro-environment: Shaping the phenotype of cancer stem-like cells. Neuro Oncol. 19:887–896. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Pecchia I, Dini V, Ricci-Vitiani L, Biffoni M, Balduzzi M, Fratini E, Belli M, Campa A, Esposito G, Cirrone G, et al: Glioblastoma stem cells: Radiobiological response to ionising radiations of different qualities. Radiat Prot Dosimetry. 166:374–378. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Jawhari S, Ratinaud MH and Vernier M: Glioblastoma, hypoxia and autophagy: A survival-prone 'ménage-à-trois'. Cell Death Dis. 7:e24342016. View Article : Google Scholar | |
|
Stępień K, Ostrowski RP and Matyja E: Hyperbaric oxygen as an adjunctive therapy in treatment of malignancies, including brain tumours. Med Oncol. 33:1012016. View Article : Google Scholar : | |
|
Sridaran D, Ramamoorthi G, Mahaboob Khan R and Kumpati P: Oxystressed tumor microenvironment potentiates epithelial to mesenchymal transition and alters cellular bioenergetics towards cancer progression. Tumour Biol. 37:13307–13322. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Agnihotri S and Zadeh G: Metabolic reprogramming in glioblastoma: The influence of cancer metabolism on epigenetics and unanswered questions. Neuro Oncol. 18:160–172. 2016. View Article : Google Scholar : | |
|
Choi SA, Lee JY, Phi JH, Wang KC, Park CK, Park SH and Kim SK: Identification of brain tumour initiating cells using the stem cell marker aldehyde dehydrogenase. Eur J Cancer. 50:137–149. 2014. View Article : Google Scholar | |
|
Clark O, Yen K and Mellinghoff IK: Molecular pathways: Isocitrate dehydrogenase mutations in cancer. Clin Cancer Res. 22:1837–1842. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Ojelabi OA, Lloyd KP, Simon AH, De Zutter JK and Carruthers A: WZB117 (2-Fluoro-6-(m- hydroxybenzoyloxy) Phenyl m-Hydroxybenzoate) inhibits GLUT1-mediated sugar transport by binding reversibly at the exofacial sugar binding site. J Biol Chem. 291:26762–26772. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Kathagen A, Schulte A, Balcke G, Phillips HS, Martens T, Matschke J, Günther HS, Soriano R, Modrusan Z, Sandmann T, et al: Hypoxia and oxygenation induce a metabolic switch between pentose phosphate pathway and glycolysis in glioma stem-like cells. Acta Neuropathol. 126:763–780. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Goidts V, Bageritz J, Puccio L, Nakata S, Zapatka M, Barbus S, Toedt G, Campos B, Korshunov A, Momma S, et al: RNAi screening in glioma stem-like cells identifies PFKFB4 as a key molecule important for cancer cell survival. Oncogene. 31:3235–3243. 2012. View Article : Google Scholar | |
|
Jennings RT and Knaus UG: Rho family and Rap GTPase activation assays. Methods Mol Biol. 1124:79–88. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Bejarano L, Schuhmacher AJ, Méndez M, Megías D, Blanco-Aparicio C, Martínez S, Pastor J, Squatrito M and Blasco MA: Inhibition of TRF1 telomere protein impairs tumor initiation and progression in glioblastoma mouse models and patient-derived xenografts. Cancer Cell. 32:590–607. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Huang W, Zhang C, Cui M, Niu J and Ding W: Inhibition of Bevacizumab-induced epithelial-mesenchymal transition by BATF2 overexpression involves the suppression of Wnt/β-catenin signaling in glioblastoma cells. Anticancer Res. 37:4285–4294. 2017.PubMed/NCBI | |
|
Iwadate Y: Epithelial-mesenchymal transition in glioblastoma progression. Oncol Lett. 11:1615–1620. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Clevers H, Loh KM and Nusse R: Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science. 346:12480122014. View Article : Google Scholar : PubMed/NCBI | |
|
Takebe N, Miele L, Harris PJ, Jeong W, Bando H, Kahn M, Yang SX and Ivy SP: Targeting Notch, Hedgehog, and Wnt pathways in cancer stem cells: Clinical update. Nat Rev Clin Oncol. 12:445–464. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Mohammed MK, Shao C, Wang J, Wei Q, Wang X, Collier Z, Tang S, Liu H, Zhang F, Huang J, et al: Wnt/β-catenin signaling plays an ever-expanding role in stem cell self-renewal, tumorigenesis and cancer chemoresistance. Genes Dis. 3:11–40. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Lee J, Kee HJ, Min S, Park KC, Park S, Hwang TH, Ryu DH, Hwang GS and Cheong JH: Integrated omics-analysis reveals Wnt-mediated NAD+ metabolic reprogramming in cancer stem-like cells. Oncotarget. 7:48562–48576. 2016.PubMed/NCBI | |
|
Bae WJ, Lee SH, Rho YS, Koo BS and Lim YC: Transforming growth factor β1 enhances stemness of head and neck squamous cell carcinoma cells through activation of Wnt signaling. Oncol Lett. 12:5315–5320. 2016. View Article : Google Scholar | |
|
Lee Y, Lee JK, Ahn SH, Lee J and Nam DH: WNT signaling in glioblastoma and therapeutic opportunities. Lab Invest. 96:137–150. 2016. View Article : Google Scholar | |
|
Yu QC, Verheyen EM and Zeng YA: Mammary development and breast cancer: A Wnt perspective. Cancers. 8:E652016. View Article : Google Scholar : PubMed/NCBI | |
|
Koval AV, Vlasov P, Shichkova P, Khunderyakova S, Markov Y, Panchenko J, Volodina A, Kondrashov FA and Katanaev VL: Anti-leprosy drug clofazimine inhibits growth of triple-negative breast cancer cells via inhibition of canonical Wnt signaling. Biochem Pharmacol. 87:571–578. 2014. View Article : Google Scholar | |
|
Andersen V and Vogel U: Systematic review: Interactions between aspirin, and other nonsteroidal anti-inflammatory drugs, and polymorphisms in relation to colorectal cancer. Aliment Pharmacol Ther. 40:147–159. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Dovizio M, Tacconelli S, Sostres C, Ricciotti E and Patrignani P: Mechanistic and pharmacological issues of aspirin as an anticancer agent. Pharmaceuticals. 5:1346–1371. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Dovizio M, Bruno A, Tacconelli S and Patrignani P: Mode of action of aspirin as a chemopreventive agent. Recent Results Cancer Res. 191:39–65. 2013. View Article : Google Scholar | |
|
Sareddy GR, Kesanakurti D, Kirti PB and Babu PP: Nonsteroidal anti-inflammatory drugs diclofenac and celecoxib attenuates Wnt/β-catenin/Tcf signaling pathway in human glioblastoma cells. Neurochem Res. 38:2313–2322. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Dharmapuri G, Doneti R, Philip GH and Kalle AM: Celecoxib sensitizes imatinib-resistant K562 cells to imatinib by inhibiting MRP1-5, ABCA2 and ABCG2 transporters via Wnt and Ras signaling pathways. Leuk Res. 39:696–701. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Lin XL, Xu Q, Tang L, Sun L, Han T, Wang LW and Xiao XY: Regorafenib inhibited gastric cancer cells growth and invasion via CXCR4 activated Wnt pathway. PLoS One. 12:e01773352017. View Article : Google Scholar : PubMed/NCBI | |
|
Tumova L, Pombinho AR, Vojtechova M, Stancikova J, Gradl D, Krausova M, Sloncova E, Horazna M, Kriz V, Machonova O, et al: Monensin inhibits canonical Wnt signaling in human colorectal cancer cells and suppresses tumor growth in multiple intestinal neoplasia mice. Mol Cancer Ther. 13:812–822. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Olmez I, Shen W, McDonald H and Ozpolat B: Dedifferentiation of patient-derived glioblastoma multiforme cell lines results in a cancer stem cell-like state with mitogen-independent growth. J Cell Mol Med. 19:1262–1272. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Chen M, Wang J, Lu J, Bond MC, Ren XR, Lyerly HK, Barak LS and Chen W: The anti-helminthic niclosamide inhibits Wnt/Frizzled1 signaling. Biochemistry. 48:10267–10274. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Wieland A, Trageser D, Gogolok S, Reinartz R, Höfer H, Keller M, Leinhaas A, Schelle R, Normann S, Klaas L, et al: Anticancer effects of niclosamide in human glioblastoma. Clin Cancer Res. 19:4124–4136. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Arend RC, Londoño-Joshi AI, Samant RS, Li Y, Conner M, Hidalgo B, Alvarez RD, Landen CN, Straughn JM and Buchsbaum DJ: Inhibition of Wnt/β catenin pathway by niclosamide: A therapeutic target for ovarian cancer. Gynecol Oncol. 134:112–120. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Liu C, Lou W, Armstrong C, Zhu Y, Evans CP and Gao AC: Niclosamide suppresses cell migration and invasion in enzalutamide resistant prostate cancer cells via Stat3-AR axis inhibition. Prostate. 75:1341–1353. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Liu C, Lou W, Zhu Y, Nadiminty N, Schwartz CT, Evans CP and Gao AC: Niclosamide inhibits androgen receptor variants expression and overcomes enzalutamide resistance in castration-resistant prostate cancer. Clin Cancer Res. 20:3198–3210. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Londoño-Joshi AI, Arend RC, Aristizabal L, Lu W, Samant RS, Metge BJ, Hidalgo B, Grizzle WE, Conner M, Forero-Torres A, et al: Effect of niclosamide on basal-like breast cancers. Mol Cancer Ther. 13:800–811. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Liao Z, Nan G, Yan Z, Zeng L, Deng Y, Ye J, Zhang Z, Qiao M, Li R, Denduluri S, et al: The anthelmintic drug niclosamide inhibits the proliferative activity of human osteosarcoma cells by targeting multiple signal pathways. Curr Cancer Drug Targets. 15:726–738. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Lu W, Lin C, King TD, Chen H, Reynolds RC and Li Y: Silibinin inhibits Wnt/β-catenin signaling by suppressing Wnt co-receptor LRP6 expression in human prostate and breast cancer cells. Cell Signal. 24:2291–2296. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang X, Lou Y, Zheng X, Wang H, Sun J, Dong Q and Han B: Wnt blockers inhibit the proliferation of lung cancer stem cells. Drug Des Devel Ther. 9:2399–2407. 2015.PubMed/NCBI | |
|
Bryukhovetskiy IS, Mischenko PV, Tolok EV, Zaitcev SV, Khotimchenko YS and Bryukhovetskiy AS: Directional migration of adult hematopoeitic progenitors to C6 gliom in vitro. Oncol Lett. 9:1839–1844. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Bryukhovetskiy IS, Dyuizen IV, Shevchenko VE, Bryukhovetskiy AS, Mischenko PV, Milkina EV and Khotimchenko YS: Hematopoietic stem cells as a tool for the treatment of glioblastoma multiforme. Mol Med Rep. 14:4511–4520. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Aboody KS, Brown A, Rainov NG, Bower KA, Liu S, Yang W, Small JE, Herrlinger U, Ourednik V, Black PM, et al: Neural stem cells display extensive tropism for pathology in adult brain: Evidence from intracranial gliomas. Proc Natl Acad Sci USA. 97:12846–12851. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Aboody KS, Najbauer J, Metz MZ, D'Apuzzo M, Gutova M, Annala AJ, Synold TW, Couture LA, Blanchard S, Moats RA, et al: Neural stem cell-mediated enzyme/prodrug therapy for glioma: Preclinical studies. Sci Transl Med. 5:184ra592013. View Article : Google Scholar : PubMed/NCBI | |
|
Aboody KS, Najbauer J, Schmidt NO, Yang W, Wu JK, Zhuge Y, Przylecki W, Carroll R, Black PM and Perides G: Targeting of melanoma brain metastases using engineered neural stem/progenitor cell. Neuro Oncol. 8:119–126. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Gutova M, Najbauer J, Frank RT, Kendall SE, Gevorgyan A, Metz MZ, Guevorkian M, Edmiston M, Zhao D, Glackin CA, et al: Urokinase plasminogen activator and urokinase plasminogen activator receptor mediate human stem cell tropism to malignant solid tumors. Stem Cells. 26:1406–1413. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Kucia M, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, Ratajczak J and Ratajczak MZ: Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: Pivotal role of the SDF-1-CXCR4 axis. Stem Cells. 23:879–894. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Gabashvili AN, Baklaushev VP, Grinenko NF, Levinskii AB, Mel'nikov PA, Cherepanov SA and Chekhonin VP: Functionally active gap junctions between connexin 43-positive mesenchymal stem cells and glioma cells. Bull Exp Biol Med. 159:173–179. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Mercapide J, Rappa G and Lorico A: The intrinsic fusogenicity of glioma cells as a factor of transformation and progression in the tumor microenvironment. Int J Cancer. 131:334–43. 2012. View Article : Google Scholar | |
|
Rappa G, Mercapide J and Lorico A: Spontaneous formation of tumorigenic hybrids between breast cancer and multipotent stromal cells is a source of tumor heterogeneity. Am J Pathol. 180:2504–2515. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Mercapide J, Anzanello F, Rappa G and Lorico A: Relationship between tumor cell invasiveness and polyploidization. PLoS One. 7:e533642012. View Article : Google Scholar | |
|
Zimmerlin L, Park TS, Zambidis ET, Donnenberg VS and Donnenberg AD: Mesenchymal stem cell secretome and regenerative therapy after cancer. Biochimie. 95:2235–2245. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
O'Donnell RK, Falcon B, Hanson J, Goldstein WE, Perruzzi C, Rafii S, Aird WC and Benjamin LE: VEGF-A/VEGFR inhibition restores hematopoietic homeostasis in the bone marrow and attenuates tumor growth. Cancer Res. 76:517–524. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Hong JP, Li XM, Li MX and Zheng FL: VEGF suppresses epithelial-mesenchymal transition by inhibiting the expression of Smad3 and miR-192, a Smad3-dependent microRNA. Int J Mol Med. 31:1436–1442. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Treps L, Perret R, Edmond S, Ricard D and Gavard J: Glioblastoma stem-like cells secrete the pro-angiogenic VEGF-A factor in extracellular vesicles. J Extracell Vesicles. 6:13594792017. View Article : Google Scholar : PubMed/NCBI | |
|
Diaz RJ, Ali S, Qadir MG, De La Fuente MI, Ivan ME and Komotar RJ: The role of bevacizumab in the treatment of glioblastoma. J Neurooncol. 133:455–467. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Bryukhovetskiy I, Lyakhova I, Mischenko P, Milkina E, Zaitsev S, Khotimchenko Y, Bryukhovetskiy A, Polevshchikov A, Kudryavtsev I, Khotimchenko M, et al: Alkaloids of fascaplysin are effective conventional chemotherapeutic drugs, inhibiting the proliferation of C6 glioma cells and causing their death in vitro. Oncol Lett. 13:738–746. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Pacioni S, D'Alessandris QG, Giannetti S, Morgante L, Coccè V, Bonomi A, Buccarelli M, Pascucci L, Alessandri G, Pessina A, et al: Human mesenchymal stromal cells inhibit tumor growth in orthotopic glioblastoma xenografts. Stem Cell Res Ther. 8:532017. View Article : Google Scholar : PubMed/NCBI | |
|
Bryukhovetskiy I, Bryukhovetsky A, Khotimchenko Y, Mischenko P, Tolok E and Khotimchenko R: Combination of the multipotent mesenchymal stromal cell transplantation with administration of temozolomide increases survival of rats with experimental glioblastoma. Mol Med Rep. 12:2828–2834. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
English K: Mesenchymal stem cells to promote islet transplant survival. Curr Opin Organ Transplant. 21:568–573. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Vizoso FJ, Eiro N, Cid S, Schneider J and Perez-Fernandez R: Mesenchymal stem cell secretome: Toward cell-free therapeutic strategies in regenerative medicine. Int J Mol Sci. 18:E18522017. View Article : Google Scholar : PubMed/NCBI | |
|
Katakowski M and Chopp M: Exosomes as tools to suppress primary brain tumor. Cell Mol Neurobiol. 36:343–352. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Liu X, Li Q, Niu X, Hu B, Chen S, Song W, Ding J, Zhang C and Wang Y: Exosomes secreted from human-induced pluripotent stem cell-derived mesenchymal stem cells prevent osteonecrosis of the femoral head by promoting angiogenesis. Int J Biol Sci. 13:232–244. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Klopp AH, Gupta A, Spaeth E, Andreeff M and Marini F III: Concise review: Dissecting a discrepancy in the literature: Do mesenchymal stem cells support or suppress tumor growth? Stem Cells. 29:11–19. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Alcayaga-Miranda F, González PL, Lopez-Verrilli A, Varas-Godoy M, Aguila-Díaz C, Contreras L and Khoury M: Prostate tumor-induced angiogenesis is blocked by exosomes derived from menstrual stem cells through the inhibition of reactive oxygen species. Oncotarget. 7:44462–44477. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Bliss SA, Sinha G, Sandiford OA, Williams LM, Engelberth DJ, Guiro K, Isenalumhe LL, Greco SJ, Ayer S, Bryan M, et al: Mesenchymal stem cell-derived exosomes stimulate cycling quiescence and early breast cancer dormancy in bone marrow. Cancer Res. 76:5832–5844. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Reza AM, Choi YJ, Yasuda H and Kim JH: Human adipose mesenchymal stem cell-derived exosomal-miRNAs are critical factors for inducing anti-proliferation signalling to A2780 and SKOV-3 ovarian cancer cells. Sci Rep. 6:384982016. View Article : Google Scholar : PubMed/NCBI | |
|
Baglio SR, Rooijers K, Koppers-Lalic D, Verweij FJ and Pérez Lanzón M: Human bone marrow- and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species. Stem Cell Res Ther. 6:1272015. View Article : Google Scholar : PubMed/NCBI | |
|
Lopatina T, Gai C, Deregibus MC, Kholia S and Camussi G: Cross talk between cancer and mesenchymal stem cells through extracellular vesicles carrying nucleic acids. Front Oncol. 6:1252016. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Z, Gong Q, Li M, Xu J, Zheng Y, Ge P and Chi G: MicroRNA-124 inhibits the proliferation of C6 glioma cells by targeting Smad4. Int J Mol Med. 40:1226–1234. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Mei LL, Wang WJ, Qiu YT, Xie XF, Bai J and Shi ZZ: miR-145-5p suppresses tumor cell migration, invasion and epithelial to mesenchymal transition by regulating the Sp1/NF-κB signaling pathway in esophageal squamous cell carcinoma. Int J Mol Sci. 18:E18332017. View Article : Google Scholar | |
|
Gong Y, Qin Z, Zhou B, Chen H, Shi Z and Zhang J: MicroRNA-200a inhibits transforming growth factor β1-induced proximal tubular epithelial-mesenchymal transition by targeting β-Catenin. Nephron. 137:237–249. 2017. View Article : Google Scholar | |
|
Yan J, Jiang JY, Meng XN, Xiu YL and Zong ZH: MiR-23b targets cyclin G1 and suppresses ovarian cancer tumorigenesis and progression. J Exp Clin Cancer Res. 35:312016. View Article : Google Scholar : PubMed/NCBI | |
|
Liu G, Xu Z and Hao D: MicroRNA-451 inhibits neuroblastoma proliferation, invasion and migration by targeting macrophage migration inhibitory factor. Mol Med Rep. 13:2253–2260. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Zeng T, Peng L, Chao C, Fu B, Wang G, Wang Y and Zhu X: miR-451 inhibits invasion and proliferation of bladder cancer by regulating EMT. Int J Clin Exp Pathol. 7:7653–7662. 2014. | |
|
Xu H, Mei Q, Shi L, Lu J, Zhao J and Fu Q: Tumor-suppressing effects of miR451 in human osteosarcoma. Cell Biochem Biophys. 69:163–168. 2014. View Article : Google Scholar | |
|
Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L, Xiang D, Desano JT, Bommer GT, Fan D, et al: MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One. 4:e68162009. View Article : Google Scholar : PubMed/NCBI | |
|
Alvarado AG, Thiagarajan PS, Mulkearns-Hubert EE, Silver DJ, Hale JS, Alban TJ, Turaga SM, Jarrar A, Reizes O, Longworth MS, et al: Glioblastoma cancer stem cells evade innate immune suppression of self-renewal through reduced TLR4 expression. Cell Stem Cell. 20:450–461.e4. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Sathyanarayanan A, Chandrasekaran KS and Karunagaran D: microRNA-145 downregulates SIP1-expression but differentially regulates proliferation, migration, invasion and Wnt signalling in SW480 and SW620 cells. J Cell Biochem. 119:2022–2035. 2018. View Article : Google Scholar | |
|
Sathyanarayanan A, Chandrasekaran KS and Karunagaran D: microRNA-145 modulates epithelial-mesenchymal transition and suppresses proliferation, migration and invasion by targeting SIP1 in human cervical cancer cells. Cell Oncol. 40:119–131. 2017. View Article : Google Scholar | |
|
Katakowski M, Buller B, Zheng X, Lu Y, Rogers T, Osobamiro O, Shu W, Jiang F and Chopp M: Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett. 335:201–204. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Gopal SK, Greening DW, Rai A, Chen M, Xu R, Shafiq A, Mathias RA, Zhu HJ and Simpson RJ: Extracellular vesicles: Their role in cancer biology and epithelial-mesenchymal transition. Biochem J. 474:21–45. 2017. View Article : Google Scholar | |
|
Ti D, Hao H, Fu X and Han W: Mesenchymal stem cells-derived exosomal microRNAs contribute to wound inflammation. Sci China Life Sci. 59:1305–1312. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Hambardzumyan D, Gutmann DH and Kettenmann H: The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci. 19:20–27. 2016. View Article : Google Scholar : | |
|
Wang Y, Liu T, Yang N, Xu S, Li X and Wang D: Hypoxia and macrophages promote glioblastoma invasion by the CCL4-CCR5 axis. Oncol Rep. 36:3522–3528. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Kondo Y, Katsushima K, Ohka F, Natsume A and Shinjo K: Epigenetic dysregulation in glioma Cancer Sci. 105:363–369. 2014. | |
|
Feng X, Szulzewsky F, Yerevanian A, Chen Z, Heinzmann D, Rasmussen RD, Alvarez-Garcia V, Kim Y, Wang B, Tamagno I, et al: Loss of CX3CR1 increases accumulation of inflammatory monocytes and promotes gliomagenesis. Oncotarget. 6:15077–15094. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Nusblat LM, Carroll MJ and Roth CM: Crosstalk between M2 macrophages and glioma stem cells. Cell Oncol. 40:471–482. 2017. View Article : Google Scholar | |
|
Zhou W, Ke SQ, Huang Z, Flavahan W, Fang X, Paul J, Wu L, Sloan AE, McLendon RE, Li X, et al: Periostea secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat Cell Biol. 17:170–182. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Alifieris C and Trafalis DT: Glioblastoma multiforme: Pathogenesis and treatment. Pharmacol Ther. 152:63–82. 2015. View Article : Google Scholar : PubMed/NCBI |
