Stem cells in carcinogenesis of glioblastoma multiforme

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Glioblastoma multiforme is a malignant primary brain tumor with a very poor prognosis. Neural stem and progenitor cells of the adult brain, as well as other types of stem cells are considered by carcinogenesis researchers the most likely source of malignant gliomas. This is evidenced by common genes regulating key processes of life, uniform proteomic profiles and identical immunophenotypical cell surface markers. These cells are highly proliferative, multipotent, able to independently migrate to the damaged area and have extensive replicative potential. However, antitumor properties of the stem cells (SCs) are also confirmed. The bodies of adult mammals and humans have genetically fixed mechanisms of control over their populations and multiple levels of antitumor protection. So far, the role of autologous SCs in a tumor patient is not clear. On the one hand, they fail to fulfill their anti-tumor and regulatory functions, and instead of organizing anti-tumor response become one of the key elements of carcinogenesis contributing to the development of neoplastic tumor vascular network and modulating the processes of neurogenesis, which is the main source of its pathological reinnervation, and therefore, a pain. On the other hand, autologous stem cells trigger powerful proliferative processes in the tumor tissue becoming the driving force of neoplastic growth. Apparently, due to the interaction of tumor cells with autologous stem cells, general and local interstitial patterns of autoregulation and sanogenesis are disturbed making tumor growth possible in principle. From this perspective, the technology that directly affects the population of cancer stem cells seems the most promising.

Full Text

Restricted Access

About the authors

IS. S Bryukhovetskyi

A.V. Zhirmunsky Institute of Marine Biology of the FEB RAS, Vladivostok

A. S. Bryukhovetskyia

Federal Research Centre of Specialized Types of Medical Care and Technologies of the FMBA of Russia, Moscow

V. V Kumeiko

Far Eastern Federal University, Vladivostok

P. V Mischenko

Far Eastern Federal University, Vladivostok

Y. S Khotimchenko

Far Eastern Federal University, Vladivostok

References

  1. Баклаушев В.П., Гриненко Н.Ф., Савченко Е.А. и др. Нейральные предшественники и гемопоэтические стволовые клетки подавляют рост низкодифференцированной глиомы. Клеточные технологии в биологии и медицине 2011; 4: 183-90.
  2. Walzlein J.H., Synowitz B., Engels В. et al. The antitumorigenic response of neural precursors depends on subventricular proliferation and age. Stem Cells 2008; 26: 2945-54.
  3. Берсенев А.В. Применение модифицированных нейральных стволовых клеток приводит к эрадикации метастатической нейро-бластомы в эксперименте. Клеточная трансплантология и тканевая инженерия 2007; 2(1): 21.
  4. Altman J. Are new neurons formed in the brains of adult mammals? Science 1962; 135(3509): 1127-8.
  5. Викторов И.В. Стволовые клетки мозга млекопитающих: биология стволовых клеток in vivo и in vitro. Известия РАН. Серия биологическая 2001; 6: 646-55.
  6. Weissman L.L. Translating stem and progenitor cell biology to the clinic: barriers and opportunities. Science 2000; 287(5457): 1442-6.
  7. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255(5052): 1707-10.
  8. Eriksson P.S., Perfilieva E., Bjork-Eriksson T. et al. Neurogenesis in the adult human hippocampus. Nature Medicine 1998; 4(11): 1313-7.
  9. Doetsch F., Garcia-Verdugo J.M., Alvarez-Buylla A. Regeneration of a germinal layer in the adult mammalian brain. PNAS USA 1999; 96(20): 11619-24.
  10. Doetsch F., Caille I., Lim D.A.et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain.Cell 1999; 97(6): 703-16.
  11. Kempermann G., Chesler E.J., Lu L. et al. Natural variation and genetic covariance in adult hippocampal neurogenesis. PNAS USA 2006; 103(3): 780-85.
  12. Soltanian S., Matin M.M. Cancer stem cells and cancer therapy.Tumour Biology 2011; 32(3): 425-40.
  13. Andreu-Agullo C., Maurin T., Thompson C. B.et al. Ars2 maintains neural stem-cell identity through direct transcriptional activation of Sox2. Nature 2012; 481(7380): 195-8.
  14. Kirshenbaum B., Doetsch F., Lois C.et al. Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J. Neuroscience 1999; 19(6): 2171-80.
  15. Bass A.J., Wang T.C. An inflammatory situation: SOX2 and STAT3 cooperate in squamous cell carcinoma initiation. Cell Stem Cell 2013; 12(3): 266-8.
  16. Sher C.J., Roberts J.M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes and development 1999; 13(12): 1501-12.
  17. Binda E.,Visioli A., Reynolds B. et al. Heterogeneity of cancer-initiating cells within glioblastoma. Frontiers in bioscience (Scholar Edition) 2012; 4: 1235-48.
  18. Gage F.H. Mammalian neural stem cells. Science 2000; 287(5457): 1433-8.
  19. Huang Z., Cheng L., Gurianova O.A. et al. Cancer stem cells in glioblastoma molecular signaling and therapeutic targeting. Protein and cell 2010; 1(7): 638-55.
  20. Annovazzi L., Mellai M., Caldera V. et al. SOX2 expression and amplification in gliomas and glioma cell lines. Cancer genomics and Proteomics 2011; 8(3): 139-47.
  21. Omari K.M., Dorovini-Zis К. CD40 expressed by human brain endothelial cells regulates CD34+ T cell adhesion to endothelium. J. Neuroimmunol 2003; 134(1-2): 166-78.
  22. Wang Y., Yang J., Zheng H. et al. Expression of mutant p53 proteins implicates a lineage relationship between neural stem cells and malignant astrocytesglioma in a murine model. Cancer Cell 2009; 15(6): 514-26.
  23. Zheng H, Ying H, Yan H, Kimmelman A.C.et al. P53 and PTEN control neural and glioma stem/progenitor cell renewal and differentiation. Nature 2008; 455(7216): 1129-33.
  24. Holland E.C., Celestino J., Dai C. et al. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nature genetics 2000; 25(1): 55-7.
  25. Spits C., Mateizel I., Geens M. et al. Recurrent chromosomal abnormalities in human embryonic stem cells. Nature biotechnology 2008; 26(12): 1361-63.
  26. Sareen D., McMillan E., Ebert A.D.et al. Chromosome 7 and 19 trisomy in cultured human neural progenitor cells. PLoSone 2009; 4(10): e7630.
  27. Kuroda T., Yasuda S., Sato Y. Tumorigenicity studies for human pluripotent stem cell-derived products. Biological and pharmaceutical bulletin 2013; 36(2): 189-92.
  28. Vredenburgh J.J., Desjardins A., Reardon D.A. et al. Experience with irinotecan for the treatment of malignant glioma. Neuro-oncology 2009; 11(1): 80-91.
  29. Брюховецкий А.С. Клеточные технологии в нейроонкологии: циторегуляторная терапия глиальных опухолей головного мозга. М.: Издательская группа РОНЦ; 2011.
  30. Vescovi A.L., Galli R., Reynolds B.A. Brain tumor stem cells. Nature review. Cancer 2006; 6: 425-36.
  31. Piccirillo S.G., Binda E., Fiocco R.et al. Brain cancer stem cells. J. Mol. Med. (Berlin, Germany) 2009; 87(11): 1087-95.
  32. Chen R., Nishimura M.C., Bumbaca S.M. et al. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell 2010; 17(4): 362-75.
  33. Barrett L.E., Granot Z., Coker C. et al. Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma. Cancer Cell 2012; 21(1): 11-24.
  34. Dahlrot R.H., Hermansen S.K., Hansen S. et al. What is the clinical value of cancer stem cell markers in gliomas? International journal of clinical and experimental pathology 2013; 6(3): 334-48.
  35. Jin X., Jin X., Jung J.E. et al. Cell surface Nestin is a biomarker for glioma stem cells. Biochemical and biophysical research communications 2013; 433(4): 496-501.
  36. Коржевский Д.Э., Петрова Е.С., Кирик О.В. и др. Нейральные маркеры, используемые при изучении дифференцировки стволовых клеток. Клеточная трансплантология и тканевая инженерия 2010; 5(3): 57-63.
  37. Liu J., Albrecht A.M., Ni X. et al. Glioblastoma tumor initiating cells: therapeutic strategies targeting apoptosis and microRNA pathways. Curr. Mol. Med. 2013; 13(3): 352-7.
  38. Aboody K.S., Broun A., Rainbov N.G. et al. Neural stem cells display extensive tropism for pathology in adult brain: Evidence from intracranial gliomas. PNAS USA 2000; 97(23): 12846-51.
  39. Glass R., Synowitz M., Kronenberg G.et al. Glioblastoma-induced attraction of endogenous neural precursor cells is associated with improved survival. J. Neuroscience 2005; 25(10): 2637-46.
  40. Robin A. M., Zhang Z. G., Wang L. et al. Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. J. Cerebr. Blood Flow Metabol. 2006; 26(1): 125-34.
  41. Mohle R., Bautz F., Rafii S. et al. The chemokine receptor CXCR-4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates trans endothelial migration induced by stromal cell-derived factor-1. Blood 1998; 91(12): 4523-30.
  42. Yin D., Zhang Z., Gao S.et al. The role of chemokine receptor CXCR4 and its ligand CXCL12 in the process of proliferation and migration of oral squamous cell carcinoma. West China J. Stomatol. 2013; 31(1): 8-12.
  43. Greenbaum A., Hsu Y.M., Day R.B. et al. CXCL12 in early mesenchymal progenitors is required for hematopoietic stem-cell maintenance. Nature 2013; 495(7440): 227-30.
  44. Imitola J., Comabella M., Chandraker A.K.et al. Neural stem/ progenitor cells express costimulatory molecules that are differentially regulated by inflammatory and apoptotic stimuli. Amer. J. Pathol. 2004; 164(5): 1615-25.
  45. Sahin A.O., Buitenhuis M. Molecular mechanisms underlying adhesion and migration of hematopoietic stem cells. Cell Adhes. Migrat. 2012; 6(1): 39-48.
  46. Yip S., Aboody K.S., Burns M. et al. Neural stem cell biology may be well suited for improving brain tumor therapies. Cancer 2003; 9(3): 189-204.
  47. Пальцев М.А., Иванов А.А., Северин С.Е. Межклеточное взаимодействие. М.: Медицина 2003.
  48. Ермаков А.В., Конькова М.С., Костюк С.В. и др. Развитие эффекта свидетеля в мезенхимальных стволовых клетках человека после воздействия рентгеновского излучения в адаптирующей дозе. Радиационная биология и радиоэкология 2010; 50 (1): 42-51.
  49. Buckner J.C., Brown P.D., O'Neill B.P. et al. Central nervous system tumors. Mayo Clinic proceedings. Mayo Clinic 2007; 82(10): 1271-86.
  50. Bajeto A., Barbieri F., Dorcaratto A. et al. Expression of CXC chemokine receptor 1-5and their ligands in human glioma tissues: Role of CXCR4 and SDF1 in glioma cells proliferation and migration. Neurochemistry International 2006; 49(5): 423-32.
  51. Mirisola V., Zuccarino A., Bachmeier B.E. et al. CXCL12/SDF1 expression by breast cancers is an independent prognostic marker of disease-free and overall survival. European J. Cancer 2009; (14): 2579-87.
  52. Zhou Y., Larsen P.Y., Hao C.et al.CXCR4 is a major chemokine receptor onglioma cells and mediates their survival. J. Biol. Chem. 2002; 227 (51): 49481-7.
  53. Voermans C., Anthoni E.C., Mul E. et al. SDF-1 induced actin polymerization and migration in human hematopoietic progenitor cells. Exper. Hematol. 2001; 29(12): 1456-64.
  54. Великанов Г.А., Леванов В.Ю., Белова Л.П. и др. Регулируемое русло для диффузии между вакуолями соседних клеток: ва-куолярный симпласт. Успехи современной биологии 2012; 132(1): 36-50.
  55. Tang W., Duan J., Zhang J.G. et al. Subtyping glioblastoma by combining miRNA and mRNA expression data using compressed sensing-based approach. EURASIP J. Bioinform. Syst. Biol.; 2013(1): 2.
  56. Marsden C.G., Wright M.J., Pochampally R. et al. Breast tumor-initiatingcells isolated from patient core biopsies for study of hormone action. Method. Mol. Biol. 2009; 590: 363-75.
  57. Manoranjan B., Venugopal C., McFarlane N.et al. Medullo-blastoma stem cells: where development and cancer cross pathways. Pediatric research 2012; 71(4 Pt 2): 516-22.
  58. Ding L., Morrison S.J. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 2013; 495(7440): 231-5.
  59. Ratajczak M.Z., Kim C., Ratajczak J. et al. Innate immunity as orchestrator of bone marrow homing for hematopoietic stem/ progenitor cells. Advanc. Experimen. Med. Biol. 2013; 735: 219-32.
  60. Dougherty J.D., Fomchenko E.I., Akuffo A.A. et al. Candidate pathways for promoting differentiation or quiescence of oligodendrocyte progenitor-like cells in glioma. Cancer Research 2012; 72(18): 4856-68.
  61. Piccirillo S.G., Binda E., Fiocco R. et al. Brain cancer stem cells. J. Mol. Med. (Berlin, Germany) 2009; 87(11): 1087-95.
  62. Tang W., Huang Y., Chen L. et al. Small intestinal tubular adenoma in a pediatric patient with Turner syndrome. World J. Gastroenterol. 2013; 19(13): 2122-25.
  63. Anbalagan M., Ali A., Jones R.K. et al. Peptidomimetic Src/ pretubulin inhibitor KX-01 alone and in combination with paclitaxel suppresses growth, metastasis in human ER/PR/HER2-negative tumor xenografts. Mol. Cancer Therap. 2012; 11(9): 1936-47.
  64. Fukuda S., Broxmeyer H.E., Pelus L.M. Flt3 ligand and the Flt3 receptor regulate hematopoietic cell migration by modulating the SDF-1alpha (CXCL12)/CXCR4 axis. Blood 2005; 105(8): 3117-26.
  65. He J., Liu Y., Zhu T.S. et al. Glycoproteomic analysis of glioblastoma stem cell differentiation. J. Proteome Research 2011; 10(1): 330—8.
  66. Ceyhan G.O., Giese N.A., Erkan M. et al. The neurotrophic factor artemin promotes pancreatic cancer invasion. Ann. Surgery 2006; 244(2): 274—81.
  67. Ceyhan G.O., Bergmann F., Kadihasanoglu M. et al. Theneurotrophic factor artemin influences the extent of neural damage and growth in chronic pancreatitis. Gut. 2007; 56(4): 534—44.
  68. Strizzi L., Bianco C, Raafat A. et al. Netrin-1 regulates invasion and migration of mouse mammary epithelial cells overexpressing Cripto-1 in vitro and in vivo. J. Cell Sci. 2005; 118(Pt 20): 4633—43.
  69. Ohira K., Homma K.J., Hirai H. et al. TrkB-T1 regulates the RhoA signaling and actin cytoskeleton in glioma cells. Biochem. Biophys. Res. Comm. 2006; 342(3): 867—74.
  70. Bajetto A., Porcile C., Pattarozzi A. et al. Differential role of EGF and BFGF in human GBM-TIC proliferation: relationship to EGFR-tyrosine kinase inhibitor sensibility. J. Biol. Regul. Homeost. Agents. 2013; 27(1): 143—54.
  71. Adini A., Adini I., Ghosh K. et al. The stemcell marker prominin-1/CD133 interacts with vascular endothelial growth factor and potentiates its action. Angiogenesis 2013; 16(2): 405—16.
  72. Arien-Zakay H., Lecht S., Nagler A. et al. Neuroprotection by human umbilical cord blood-derived progenitors in ischemic brain injuries. Arch. Italien. Biol. 2011; 149(2): 233—45.
  73. Varner J.A. Stem cells and neurogenesis in tumors. Progress in experimental tumor research 2007; 39: 122—9.
  74. Halvorson K.G., Sevcik M.A., Ghilardi J.R. et al. Intravenous ibandronate rapidly reduces pain, neurochemical indices of central sensitization, tumor burden, and skeletal destruction in a mouse model of bone cancer. J. Pain Sympt. Manag. 2008; 36(3): 289—303.
  75. Jimenez-Andrade J.M., Martin C.D., Koewler N.J. et al. Nerve growth factor sequestering therapy attenuates non-malignant skeletal pain following fracture. Pain 2007; 133(1—3): 183—96.
  76. Basile J.R., Castilho R.M., Williams V.P. et al. Semaphorin 4D provides a link between axon guidance processes and tumor-induced angiogenesis. PNAS USA 2006; 103(24): 9017—22.
  77. Nakamura K., Yashiro M., Matsuoka T. et al. A novel molecular targeting compound as K-samII/FGF-R2 phosphorylation inhibitor, Ki23057, for Scirrhous gastric cancer. Gastroenterol. 2006; 131(5): 1530—41.
  78. Yazdani U., Terman J.R. The semaphorins. Genome biology 2006; 7(3): 211.
  79. Ellis L.M. Mechanisms of action of bevacizumab as a component of therapy for metastatic colorectal cancer. Seminaries in oncology 2006; 33: S1—7.
  80. Ellis L.M. The role of neuropilins in cancer. Mol. Canc. Ther. 2006; 5(5): 1099—107.
  81. Spicer J.A. New small-molecule inhibitors of mitogen-activated protein kinase. Expert Opin.n Drug Discov. 2008; 3(7): 801—17.
  82. Zhou H., Binmadi N.O., Yang Y.H. et al. Semaphorin 4D cooperates with VEGF to promote angiogenesis and tumor progression. Angiogenesis 2012; 15(3): 391—407.
  83. Sakurai A., Gavard J., Annas-Linhares Y. et al. Semaphorin 3E initiates antiangiogenic signaling through plexin D1 by regulating Arf6 and R-Ras. Mol. Cell. Biol. 2010; 30(12): 3086—98.
  84. Garmy-Susini B., Varner J.A. Circulating endothelial progenitor cells. British J. Cancer 2005; 93(8): 855—8.
  85. Manoranjan B., Venugopal C., McFarlane N. et al. Medulloblastoma stem cells: where development and cancer cross pathways. Pediat. Res. 2012; 71(4 Pt 2): 516—22.
  86. Wang X., Venugopal C., Manoranjan B. Sonic hedgehog regulates Bmi1 in human medulloblastoma brain tumor-initiating cells. Oncogene 2012; 31(2): 187—99.
  87. Martinez-Ferre A., Navarro-Garberi M., Bueno C. et al. Wnt Signal Specifies the Intrathalamic Limit and Its Organizer Properties by Regulating Shh Induction in the Alar Plate. J. Neurosci. 2013; 33(9): 3967—80.
  88. Hu J., Huang X., Hong X. et al. Arsenic trioxide inhibits the proliferation of myeloma cell line through notch signaling pathway. Canc. Cell Inter. 2013; 13(1): 25.
  89. Устьянцева И.М. Апоптоз и воспалительный ответ. Политравма 2007; 1:74—80.
  90. Leong S.Y., Faux C.H., Turbic A.et al. The Rho kinase pathway regulates mouse adult neural precursor cell migration. Stem cells 2011; 29(2): 332—43.
  91. Hirschmann -Jax C., Foster A.E., Wulf G.G. et al. A distinct «side population» of cells with high drug efflux capacity in human tumor cells. PNAS USA 2004; 101: 14228—33.
  92. Hegi M.E., Diserens A.C., Gorlia T. et al. MGMT gene silencing and benefit from temozolamide in glioblastoma. New Eng. J. Med. 2005; 352: 997—1003.
  93. Bao S., Wu Q., McLendon R.E. et al. Glioma stem cell promotes radioresistance by preferential activation of DNA damage response. Nature 2006; 444: 756—60.
  94. Bach P., Abel T., Hoffmann C. et al. Specific elimination of CD133+ tumor cells with targeted oncolytic measles virus. Canc. Res. 2013; 73(2): 865—74.
  95. Manning G., Whyte D.B., Martinez R. et al. The protein kinase complement of the human genome. Science 2002; 298(5600): 1912—34.
  96. Stricker S.H., Feber A., Engstrom P.G. et al. Widespread resetting of DNA methylation in glioblastoma-initiating cells suppresses malignant cellular behavior in a lineage-dependent manner. Gen. Develop. 2013; 27(6): 654—69.
  97. Xie L.Q., Sun H.P., Wang T. et al. Reprogramming of adult human neural stem cells into induced pluripotent stem cells. Chinese Med. J.2013; 126(6): 1138—43.
  98. Bo Y., Guo G., Yao W. miRNA-mediated tumor specific delivery of TRAIL reduced glioma growth. J. Neurooncol. 2013; 112(1): 27—37.
  99. Prior H.M., Walter M.A. SOX genes: architects of development. Mol. Med. 1996; 2(4): 405—12.
  100. Bazzoli E., Pulvirenti T., Oberstadt M.C. et al. MEF promotes stemness in the pathogenesis of gliomas. Cell Stem Cell 2012; 11(6): 836—44.
  101. Murphy A.M., Rabkin S.D. Current status of gene therapy for brain tumors. Transl. Res. 2013; 161(4): 339—54.
  102. Snapyan M., Lemasson M., Brill M.S. et al. Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J. Neurosci. 2009; 29(13): 4172—88.
  103. Teramoto T., Qiu J., Plumier J. C. et al. EGF amplifies the replacement of parvalbumin-expressing striatal interneurons after ischemia. J. Clin. Invest. 2003; 111: 1125—32.
  104. Ben-Hur T., Ben-Menachem O., Furer V. et al. Effects of proin flammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol. Cell. Neurosci. 2003; 24(3): 623—31.
  105. Kobayashi N., Navarro-Alvares N., Soto-Gutieres A. et al. Cancer stem cell research; current situation and problem. Cell Transpl. 2008; 17(1-2): 19—25.
  106. Shi N., Pardridge W.M. Noninvasive gene targeting to the brain. PNAS USA 2000; 97(13): 7567—72.
  107. Navarro-Alvarez N., Kondo E., Kawamoto H.et al. Isolation and propagation of a human CD133(-) colon tumor-derived cell line with tumorigenic and angiogenic properties. Cell Transpl. 2010; 19(6): 865—77.
  108. Cheng L., Alexander R., Zhang S. et al. The clinical and therapeutic implications of cancer stem cell biology. Expert Rev. Anticanc.Ther. 2011; 11(7): 1131—43.
  109. Tabatabai G., Bahr O., Mohle R. et al. Lessons from the bone marrow: how malignant glioma cells attract adult hematopoietic progenitor cells. Brain 2005; 128(9): 2200—11.
  110. Брюховецкий А.С., Чехонин В.П., Семенова А.В. и др. Противоопухолевое средство на основе иммунолипосомальной биологической конструкции, способ его получения и векторной доставки в центральную нервную систему при опухолевом процессе. Патент РФ на изобретение № 2336901 от 27.10.2008.
  111. Khurana B., Goyal A.K., Budhiraja A. et al. Lipoplexes versus nanoparticles: pDNA/siRNA delivery. Drug delivery 2013; 20(2): 57—64.
  112. Duman B.B., Sahin B., Acikalin A. et al. PTEN, Akt, MAPK, p53 and p95 expression to predict trastuzumab resistance in HER2 positive breast cancer. J. B.U.ON 2013; 18(1): 44—50.
  113. Ortensi B., Setti M., Osti D. et al. Cancer stem cell contribution to glioblastoma invasiveness. Stem Cell Res. Ther. 2013; 4(1): 18.
  114. Peled A., Tavor S. Role of CXCR4 in the pathogenesis of acute myeloid leukemia. Theranostics 2013; 3(1): 34—9.
  115. Lin C.Y., Wang L., Than K. et al. Cancer stem cell markers: what is their diagnostic value? Expert Opin. Med. Diagnost. 2010; 4(6): 473—81.
  116. Tarnowski M., Liu R., Wysoczynski M.et al. CXCR7: a new SDF-1-binding receptor in contrast to normal CD34( + ) progenitors is functional and is expressed at higher level in human malignant hematopoietic cells. Euro. J. Haematol. 2010; 85(6): 472—83.
  117. Tang Y., Shah K., MesserliS. M. et al. In vivo tracking of neural progenitor cell migration to glioblastomas. Human gene therapy 2003; 14(13): 1247—54.
  118. Foubert P., Varner J.A. Integrin's in tumor angiogenesis and lymphangiogenesis. Meth. Mol. Biol. 2012; 757: 471—86.
  119. Zalatimo O., Zoccoli C.M. Patel A. et al. Impact of genetic targets on primary brain tumor therapy: what's ready for prime time? Advanc. Inexper. Med. Biol. 2013; 779: 267—89.
  120. Holland E.C. Gliomagenesis: genetic alterations and mouse models. Genetics 2001; 2: 120—9.
  121. Reya T., Morrison S.J., Clarke M.F.et al. Stem cell, cancer, and cancer stem cell. Nature 2001; 423: 409—14.
  122. Charles N.A., Holland E.C., Gilbertson R. et al. The brain tumor microenvironment. Glia 2012; 60(3): 502—14.
  123. Dvorak P., Dvorakova D., Hampl A. Fibroblast growth factor signaling in embryonic and cancer stem cells. FEBS Letters 2006; 580(12): 2869—74.
  124. Jiang W., Peng J., Zhang Y. et al. The implications of cancer stem cells for cancer therapy. Inter. J. Mol. Sci. 2012; 13(12): 16636—57.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2013 Eco-Vector


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: 

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies