Participation of the subventricular zone of the brain in the development of brain glioma

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Abstract

Glioblastoma (GBM) is a malignant tumor with an average survival rate of 15–16 months with standard treatment; however, cases of successful treatment provide hope that a better understanding of the pathology will improve prognosis. Glial tumors contain clonogenic cells (cells capable of forming colonies in a culture medium) with a high proliferative potential, and their descendants have a wide range of possible differentiation; these clonogenic cells are currently considered as glioma stem cells (GSCs). In normal and pathological conditions, there are zones in the adult brain that contain proliferating neural stem cells (NSCs) and their descendants – progenitor cells that have begun to differentiate. One such zone lying on the lateral wall of the lateral ventricle, called the subventricular zone of the lateral ventricle (SVZ), has attracted much attention due to its importance for gliomagenesis. Numerous studies have shown that the intense exchange of signaling molecules and cells between the GBM and the SVZ leads to accelerated tumor growth and an increased risk of relapse. Research results indicate the possibility of developing new, more effective strategies to combat this dangerous disease, taking into account knowledge about the role of SVZ in the development of this pathology.

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About the authors

A. V. Revishchin

Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences

Author for correspondence.
Email: revishchin@mail.ru
Russian Federation, Moscow

G. V. Pavlova

Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences; N.N. Burdenko National Medical Research Center of Neurosurgery, Ministry of Healthcare of Russia; Sechenov First Moscow State Medical University

Email: revishchin@mail.ru
Russian Federation, Moscow; Moscow; Moscow

References

  1. Корочкин Л. И., Ревищин A. B., Охотин В. Е. Нейральные стволовые клетки, их значение в восстановительных процессах в нервной системе. Морфология. 2005. 127 (3): 7–16.
  2. Павлова Г. В., Охотин В. Е., Корочкин Л. И., Ревищин А. В. Геномная регуляция судьбы нейральных стволовых клеток млекопитающих. Генетика. 2008. 44 (3): 293–299.
  3. Aboody K. S., Brown A., Rainov N. G., Bower K. A., Liu S., Yang W., Small J. E., Herrlinger U., Ourednik V., Black P. M., Breakefield X. O., and Snyder E. Y. Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. Proc Natl Acad Sci U S A. 2000. 97(23): 12846–12851.
  4. Adeberg S., Bostel T., Konig L., Welzel T., Debus J., and Combs S. E. A comparison of long-term survivors and short-term survivors with glioblastoma, subventricular zone involvement: a predictive factor for survival? Radiat Oncol. 2014. 9 (95).
  5. Ahmadipour Y., Krings J. I., Rauschenbach L., Gembruch O., Chihi M., Darkwah Oppong M., Pierscianek D., Jabbarli R., Sure U., and El Hindy N. The influence of subventricular zone involvement in extent of resection and tumor growth pattern of glioblastoma. Innov Surg Sci. 2020. 5 (3–4): 127–132.
  6. Allport J. R., Shinde Patil V. R., and Weissleder R. Murine neuronal progenitor cells are preferentially recruited to tumor vasculature via alpha4-integrin and SDF-1alpha-dependent mechanisms. Cancer Biol Ther. 2004. 3 (9): 838–844.
  7. Bergmann O., Liebl J., Bernard S., Alkass K., Yeung M. S., Steier P., Kutschera W., Johnson L., Landen M., Druid H., Spalding K. L., and Frisen J. The age of olfactory bulb neurons in humans. Neuron. 2012. 74 (4): 634–639.
  8. Bexell D., Gunnarsson S., Nordquist J., and Bengzon J. Characterization of the subventricular zone neurogenic response to rat malignant brain tumors. Neuroscience, 2007. 147 (3): 824–832.
  9. Burns M. J., and Weiss W. Targeted therapy of brain tumors utilizing neural stem and progenitor cells. Front Biosci. 2003. 8: 228–234.
  10. Cao F., Hata R., Zhu P., Ma Y. J., Tanaka J., Hanakawa Y., Hashimoto K., Niinobe M., Yoshikawa K., and Sakanaka M. Overexpression of SOCS3 inhibits astrogliogenesis and promotes maintenance of neural stem cells. J Neurochem. 2006. 98 (2): 459–470.
  11. Chen L., Guerrero-Cazares H., Ye X., Ford E., McNutt T., Kleinberg L., Lim M., Chaichana K., Quinones-Hinojosa A., and Redmond K. Increased subventricular zone radiation dose correlates with survival in glioblastoma patients after gross total resection. Int J Radiat Oncol Biol Phys. 2013. 86 (4): 616–622.
  12. Doetsch F., Caille I., Lim D. A., Garcia-Verdugo J.M., and Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999. 97 (6): 703–716.
  13. Ehtesham M., Winston J. A., Kabos P., and Thompson R. C. CXCR4 expression mediates glioma cell invasiveness. Oncogene. 2006. 25 (19): 2801–2806.
  14. Ehtesham M., Yuan X., Kabos P., Chung N. H., Liu G., Akasaki Y., Black K. L., and Yu J. S. Glioma tropic neural stem cells consist of astrocytic precursors and their migratory capacity is mediated by CXCR4. Neoplasia. 2004. 6 (3): 287–293.
  15. Ellingson B. M., Lai A., Harris R. J., Selfridge J. M., Yong W. H., Das K., Pope W. B., Nghiemphu P. L., Vinters H. V., Liau L. M., Mischel P. S., and Cloughesy T. F. Probabilistic radiographic atlas of glioblastoma phenotypes. AJNR Am J Neuroradiol. 2013. 34 (3): 533–540.
  16. Eriksson P. S., Perfilieva E., Bjork-Eriksson T., Alborn A. M., Nordborg C., Peterson D. A., and Gage F. H. Neurogenesis in the adult human hippocampus. Nat Med. 1998. 4 (11): 1313–1317.
  17. Ernst A., Alkass K., Bernard S., Salehpour M., Perl S., Tisdale J., Possnert G., Druid H., and Frisen J. Neurogenesis in the striatum of the adult human brain. Cell. 2014. 156 (5): 1072–1083.
  18. Furth J., Kahn M. C., and Breedis C. The Transmission of Leukemia of Mice with a Single Cell. Am Journal Cancer. 1937. 31: (276–282.
  19. Gage F. H., Ray J., and Fisher L. J. Isolation, characterization, and use of stem cells from the CNS. Annu Rev Neurosci. 1995. 18: 159–192.
  20. Glass R., Synowitz M., Kronenberg G., Walzlein J. H., Markovic D. S., Wang L. P., Gast D., Kiwit J., Kempermann G., and Kettenmann H. Glioblastoma-induced attraction of endogenous neural precursor cells is associated with improved survival. J Neurosci. 2005. 25 (10): 2637–2646.
  21. Gleeson J. G., Lin P. T., Flanagan L. A., and Walsh C. A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron. 1999. 23 (2): 257–271.
  22. Goffart N., Kroonen J., Di Valentin E., Dedobbeleer M., Denne A., Martinive P., and Rogister B. Adult mouse subventricular zones stimulate glioblastoma stem cells specific invasion through CXCL12/CXCR4 signaling. Neuro Oncol. 2015. 17 (1): 81–94.
  23. Goffart N., Lombard A., Lallemand F., Kroonen J., Nassen J., Di Valentin E., Berendsen S., Dedobbeleer M., Willems E., Robe P., Bours V., Martin D., Martinive P., Maquet P., and Rogister B. CXCL12 mediates glioblastoma resistance to radiotherapy in the subventricular zone. Neuro Oncol. 2017. 19 (1): 66–77.
  24. Gollapalli K., Ghantasala S., Kumar S., Srivastava R., Rapole S., Moiyadi A., Epari S., and Srivastava S. Subventricular zone involvement in Glioblastoma – A proteomic evaluation and clinicoradiological correlation. Sci Rep. 2017. 7 (1): 1449.
  25. Gupta T., Nair V., Paul S. N., Kannan S., Moiyadi A., Epari S., and Jalali R. Can irradiation of potential cancer stem-cell niche in the subventricular zone influence survival in patients with newly diagnosed glioblastoma? J Neurooncol. 2012. 109 (1): 195–203.
  26. Hira V. V.V., Molenaar R. J., Breznik B., Lah T., Aronica E., and Van Noorden C. J.F. Immunohistochemical Detection of Neural Stem Cells and Glioblastoma Stem Cells in the Subventricular Zone of Glioblastoma Patients. J Histochem Cytochem. 2021. 69 (5): 349–364.
  27. Ichimura K., Ohgaki H., Kleihues P., and Collins V. P. Molecular pathogenesis of astrocytic tumours. J Neurooncol. 2004. 70 (2): 137–160.
  28. Ignatova T. N., Kukekov V. G., Laywell E. D., Suslov O. N., Vrionis F. D., and Steindler D. A. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia. 2002. 39 (3): 193–206.
  29. Jafri N. F., Clarke J. L., Weinberg V., Barani I. J., and Cha S. Relationship of glioblastoma multiforme to the subventricular zone is associated with survival. Neuro Oncol. 2013. 15 (1): 91–96.
  30. Kam M., Curtis M. A., McGlashan S.R., Connor B., Nannmark U., and Faull R. L. The cellular composition and morphological organization of the rostral migratory stream in the adult human brain. J Chem Neuroanat. 2009. 37 (3): 196–205.
  31. Kim J. E., Park J. E., Park S. Y., Kim Y. H., Hong C. K., Kim J. H., and Kim H. S. Defining subventricular zone involvement to predict the survival of patients in isocitrate dehydrogenase-wild type glioblastoma: validation in a prospective registry. Eur Radiol. 2023. 33 (9): 6448– 6458.
  32. Kimura M., Lee Y., Miller R., and Castillo M. Glioblastoma multiforme: relationship to subventricular zone and recurrence. Neuroradiol J. 2013. 26 (5): 542–547.
  33. Kornack D. R., and Rakic P. The generation, migra tion, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci U S A. 2001. 98 (8): 4752–4757.
  34. Kroonen J., Nassen J., Boulanger Y. G., Provenzano F., Capraro V., Bours V., Martin D., Deprez M., Robe P., and Rogister B. Human glioblastoma-initiating cells invade specifically the subventricular zones and olfactory bulbs of mice after striatal injection. Int J Cancer. 2011. 129 (3): 574–585.
  35. Kucia M., Reca R., Miekus K., Wanzeck J., Wojakowski W., Janowska-Wieczorek A., Ratajczak J., and Ratajczak M. Z. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: pivotal role of the SDF-1CXCR4 axis. Stem Cells. 2005. 23 (7): 879–894.
  36. Levison S. W., and Goldman J. E. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron. 1993. 10 (2): 201–212.
  37. Liu Q., Sanai N., Jin W. N., La Cava A., Van Kaer L., and Shi F. D. Neural stem cells sustain natural killer cells that dictate recovery from brain inflammation. Nat Neurosci. 2016. 19 (2): 243–252.
  38. MacLeod G., Bozek D. A., Rajakulendran N., Monteiro V., Ahmadi M., Steinhart Z., Kushida M. M., Yu H., Coutinho F. J., Cavalli F. M.G., Restall I., Hao X., Hart T., Luchman H. A., Weiss S., Dirks P. B., and Angers S. Genome-Wide CRISPRCas9 Screens Expose Genetic Vulnerabilities and Mechanisms of Temozolomide Sensitivity in Glioblastoma Stem Cells. Cell Rep. 2019. 27 (3): 971–986 e979.
  39. Matarredona E. R., and Pastor A. M. Neural Stem Cells of the Subventricular Zone as the Origin of Human Glioblastoma Stem Cells. Therapeutic Implications. Front Oncol. 2019. 9: 779.
  40. Mattei V, Santilli F, Martellucci S, Delle Monache S, Fabrizi J, Colapietro A, Angelucci A, Festuccia C. The Importance of Tumor Stem Cells in Glioblastoma Resistance to Therapy. Int J Mol Sci. 2021. 22 (8): 3863. doi: 10.3390/ijms22083863.
  41. Morshead C. M., Craig C. G., and van der Kooy D. In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development. 1998. 125 (12): 2251–2261.
  42. Pavlova G., Kolesnikova V., Samoylenkova N., Drozd S., Revishchin A., Shamadykova D., Usachev D. Y., and Kopylov A. A Combined Effect of G-Quadruplex and Neuro-Inducers as an Alternative Approach to Human Glioblastoma Therapy. Front Oncol. 2022. 12: 880740.
  43. Quinones-Hinojosa A., Sanai N., Soriano-Navarro M., Gonzalez-Perez O., Mirzadeh Z., Gil-Perotin S., Romero-Rodriguez R., Berger M. S., Garcia-Verdugo J.M., and Alvarez-Buylla A. Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol. 2006. 494 (3): 415–434.
  44. Rempel S. A., Dudas S., Ge S., and Gutierrez J. A. Identification and localization of the cytokine SDF1 and its receptor, CXC chemokine receptor 4, to regions of necrosis and angiogenesis in human glioblastoma. Clin Cancer Res. 2000. 6 (1): 102–111.
  45. Revishchin A. V., Korochkin L. I., Okhotin V. E., Pavlova G. V. Neural stem cells in the mammalian brain. Int Rev Cytol. 2008. 265: 55–109.
  46. Ripari L. B., Norton E. S., Bodoque-Villar R., Jeanneret S., Lara-Velazquez M., Carrano A., Zarco N., Vazquez-Ramos C.A., Quinones-Hinojosa A., de la Rosa-Prieto C., and Guerrero-Cazares H. Glioblastoma Proximity to the Lateral Ventricle Alters Neurogenic Cell Populations of the Subventricular Zone. Front Oncol. 2021. 11: 650316.
  47. Rizzo A. E., Yu J., Suh J., Emch T., Murphy E., Ahluwalia M., Reddy C., and S. Chao. Investigating the Relationship Between Radiation Dose to Neural Stem Cell Niches and Survival in GBM. Int J Radiat Oncol 2014. 90 (1S): S283-S284.
  48. Rousselot P., Lois C., and Alvarez-Buylla A. Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J Comp Neurol. 1995. 351(1): 51–61.
  49. Sanai N., Alvarez-Buylla A., and Berger M. S. Neural stem cells and the origin of gliomas. N Engl J Med. 2005. 353 (8): 811–822.
  50. Sanai N., Berger M. S., Garcia-Verdugo J.M., and Alvarez-Buylla A. Comment on “Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension”. Science. 2007. 318 (5849): 393; author reply 393.
  51. Sanai N., Tramontin A. D., Quinones-Hinojosa A., Barbaro N. M., Gupta N., Kunwar S., Lawton M. T., McDermott M.W., Parsa A. T., Manuel-Garcia Verdugo J., Berger M. S., and Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature. 2004. 427 (6976): 740–744.
  52. Staflin K., Honeth G., Kalliomaki S., Kjellman C., Edvardsen K., and Lindvall M. Neural progenitor cell lines inhibit rat tumor growth in vivo. Cancer Res. 2004. 64 (15): 5347–5354.
  53. Susman S., Leucuta D. C., Kacso G., and Florian S. I. High dose vs low dose irradiation of the subventricular zone in patients with glioblastoma-a systematic review and meta-analysis. Cancer Manag Res. 2019. 11: 6741–6753.
  54. Wang C., Liu F., Liu Y.Y., Zhao C.H., You Y., Wang L., Zhang J., Wei B., Ma T., Zhang Q., Zhang Y., Chen R., Song H., Yang Z. Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res. 2011. 21 (11): 1534–1550.
  55. Wang C., You Y., Qi D., Zhou X., Wang L., Wei S., Zhang Z., Huang W., Liu Z., Liu F., Ma L., and Yang Z. Human and monkey striatal interneurons are derived from the medial ganglionic eminence but not from the adult subventricular zone. J Neurosci. 2014. 34 (33): 10906–10923.
  56. Weinstein D. E., Shelanski M. L., and Liem R. K. C17, a retrovirally immortalized neuronal cell line, inhibits the proliferation of astrocytes and astrocytoma cells by a contact-mediated mechanism. Glia. 1990. 3 (2): 130–139.
  57. Yip S., Aboody K. S., Burns M., Imitola J., Boockvar J. A., Allport J., Park K. I., Teng Y. D., Lachyankar M., McIntosh T., O’Rourke D.M., Khoury S., Weissleder R., Black P. M., Weiss W., and Snyder E. Y. Neural stem cell biology may be well suited for improving brain tumor therapies. Cancer J. 2003. 9 (3): 189–204.
  58. Zhang J., Sarkar S., and Yong V. W. The chemokine stromal cell derived factor-1 (CXCL12) promotes glioma invasiveness through MT2-matrix metalloproteinase. Carcinogenesis. 2005. 26 (12): 2069–2077.
  59. Zhang S., and Cui W. Sox2, a key factor in the regulation of pluripotency and neural differentiation. World J Stem Cells. 2014. 6 (3): 305–311.
  60. Zhang S., Zhao F., Zhou T., Liu D., Yao X., Fu W., Liu Z., Lan C., Lai Z., Liu C., Li H., Li Y., Hu S., Yin Y., Tan L., Li W., Li F., Hu R., and Feng H. Combination of the Distance From Tumor Edge to Subventricular Zone and IDH Mutation Predicts Prognosis of Patients With Glioma. Front Oncol. 2021. 11: 693693.

Supplementary files

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2. Fig. 1. Diagram of the location of the subventricular zone (SVZ) and fascia dentata of the hippocampus on a frontal section of the human brain. The drawing was made using the BioRender resource https://ikt-masterilki.ru/ biorender/

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3. Fig. 2. Diagram of the arrangement of cells in the subventricular zone of the adult human brain. The positions of the layers are indicated at the top: I – monolayer of ependymal cells, II – intermediate hypocellular layer, III – strip of astrocyte bodies IV – transition zone. The drawing was made using the BioRender resource https://ikt-masterilki.ru/biorender/

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