Review ArticleReview

Development of glioblastoma organoids and their applications in personalized therapy

Can Xu, Xiaoye Yuan, Pengyu Hou, Ziru Li, Changsheng Wang, Chuan Fang and Yanli Tan
Cancer Biology & Medicine May 2023, 20 (5) 353-368; DOI: https://doi.org/10.20892/j.issn.2095-3941.2023.0061

References

  1. 1.↵
    2. Ballard DH,
    3. Boyer CJ,
    4. Alexander JS.
    Organoids - preclinical models of human disease. N Engl J Med. 2019; 380: 1981–2.
    OpenUrl
  2. 2.↵
    2. Blue R,
    3. Miranda SP,
    4. Gu BJ,
    5. Chen HI.
    A primer on human brain organoids for the neurosurgeon. Neurosurgery. 2020; 87: 620–9.
    OpenUrl
  3. 3.↵
    2. Xu X,
    3. Li L,
    4. Luo L,
    5. Shu L,
    6. Si X,
    7. Chen Z, et al.
    Opportunities and challenges of glioma organoids. Cell Commun Signal. 2021; 19: 102.
    OpenUrl
  4. 4.↵
    2. Tirosh I,
    3. Suva ML.
    Tackling the many facets of glioblastoma heterogeneity. Cell Stem Cell. 2020; 26: 303–4.
    OpenUrlCrossRef
  5. 5.↵
    2. Tao M,
    3. Wu X.
    The role of patient-derived ovarian cancer organoids in the study of PARP inhibitors sensitivity and resistance: from genomic analysis to functional testing. J Exp Clin Cancer Res. 2021; 40: 338.
    OpenUrl
  6. 6.↵
    2. Chai C,
    3. Ji P,
    4. Xu H,
    5. Tang H,
    6. Wang Z,
    7. Zhang H, et al.
    Targeting cancer drug resistance utilizing organoid technology. Biomed Pharmacother. 2022; 158: 114098.
  7. 7.↵
    2. Lee J,
    3. Kotliarova S,
    4. Kotliarov Y,
    5. Li A,
    6. Su Q,
    7. Donin NM, et al.
    Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006; 9: 391–403.
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    2. Xie Y,
    3. Bergstrom T,
    4. Jiang Y,
    5. Johansson P,
    6. Marinescu VD,
    7. Lindberg N, et al.
    The human glioblastoma cell culture resource: validated cell models representing all molecular subtypes. EBioMedicine. 2015; 2: 1351–63.
    OpenUrl
  9. 9.↵
    2. Stringer BW,
    3. Day BW,
    4. D’Souza RCJ,
    5. Jamieson PR,
    6. Ensbey KS,
    7. Bruce ZC, et al.
    A reference collection of patient-derived cell line and xenograft models of proneural, classical and mesenchymal glioblastoma. Sci Rep. 2019; 9: 4902.
    OpenUrl
  10. 10.↵
    2. Linkous A,
    3. Balamatsias D,
    4. Snuderl M,
    5. Edwards L,
    6. Miyaguchi K,
    7. Milner T, et al.
    Modeling patient-derived glioblastoma with cerebral organoids. Cell Rep. 2019; 26: 3203–11.e5.
    OpenUrlCrossRefPubMed
  11. 11.↵
    2. Musah-Eroje A,
    3. Watson S.
    A novel 3D in vitro model of glioblastoma reveals resistance to temozolomide which was potentiated by hypoxia. J Neurooncol. 2019; 142: 231–40.
    OpenUrlCrossRef
  12. 12.↵
    2. Darrigues E,
    3. Zhao EH,
    4. De Loose A,
    5. Lee MP,
    6. Borrelli MJ,
    7. Eoff RL, et al.
    Biobanked glioblastoma patient-derived organoids as a precision medicine model to study inhibition of invasion. Int J Mol Sci. 2021; 22: 10720.
  13. 13.↵
    2. Lancaster MA,
    3. Renner M,
    4. Martin CA,
    5. Wenzel D,
    6. Bicknell LS,
    7. Hurles ME, et al.
    Cerebral organoids model human brain development and microcephaly. Nature. 2013; 501: 373–9.
    OpenUrlCrossRefPubMedWeb of Science
  14. 14.↵
    2. Lancaster MA,
    3. Knoblich JA.
    Generation of cerebral organoids from human pluripotent stem cells. Nat Protoc. 2014; 9: 2329–40.
    OpenUrlCrossRefPubMed
  15. 15.↵
    2. Park S,
    3. Avera AD,
    4. Kim Y.
    Biomanufacturing of glioblastoma organoids exhibiting hierarchical and spatially organized tumor microenvironment via transdifferentiation. Biotechnol Bioeng. 2022; 119: 3252–74.
    OpenUrl
  16. 16.↵
    2. Joseph JV,
    3. Blaavand MS,
    4. Daubon T,
    5. Kruyt FA,
    6. Thomsen MK.
    Three-dimensional culture models to study glioblastoma - current trends and future perspectives. Curr Opin Pharmacol. 2021; 61: 91–7.
    OpenUrl
  17. 17.↵
    2. Ogawa J,
    3. Pao GM,
    4. Shokhirev MN,
    5. Verma IM.
    Glioblastoma model using human cerebral organoids. Cell Rep. 2018; 23: 1220–9.
    OpenUrlCrossRef
  18. 18.↵
    2. Bian S,
    3. Repic M,
    4. Guo Z,
    5. Kavirayani A,
    6. Burkard T,
    7. Bagley JA, et al.
    Genetically engineered cerebral organoids model brain tumor formation. Nat Methods. 2018; 15: 631–9.
    OpenUrlCrossRefPubMed
  19. 19.↵
    2. Loong HH,
    3. Wong AM,
    4. Chan DT,
    5. Cheung MS,
    6. Chow C,
    7. Ding X, et al.
    Patient-derived tumor organoid predicts drugs response in glioblastoma: a step forward in personalized cancer therapy? J Clin Neurosci. 2020; 78: 400–2.
    OpenUrl
  20. 20.↵
    2. Hwang JW,
    3. Loisel-Duwattez J,
    4. Desterke C,
    5. Latsis T,
    6. Pagliaro S,
    7. Griscelli F, et al.
    A novel neuronal organoid model mimicking glioblastoma (GBM) features from induced pluripotent stem cells (iPSC). Biochim Biophys Acta Gen Subj. 2020; 1864: 129540.
  21. 21.↵
    2. Rybin MJ,
    3. Ivan ME,
    4. Ayad NG,
    5. Zeier Z.
    Organoid models of glioblastoma and their role in drug discovery. Front Cell Neurosci. 2021; 15: 605255.
  22. 22.↵
    2. Hubert CG,
    3. Rivera M,
    4. Spangler LC,
    5. Wu Q,
    6. Mack SC,
    7. Prager BC, et al.
    A three-dimensional organoid culture system derived from human glioblastomas recapitulates the hypoxic gradients and cancer stem cell heterogeneity of tumors found in vivo. Cancer Res. 2016; 76: 2465–77.
    OpenUrlAbstract/FREE Full Text
  23. 23.↵
    2. Jacob F,
    3. Salinas RD,
    4. Zhang DY,
    5. Nguyen PTT,
    6. Schnoll JG,
    7. Wong SZH, et al.
    A patient-derived glioblastoma organoid model and biobank recapitulates inter- and intra-tumoral heterogeneity. Cell. 2020; 180: 188–204.e22.
    OpenUrlCrossRefPubMed
  24. 24.↵
    2. Yang H,
    3. Zhang N,
    4. Liu YC.
    An organoids biobank for recapitulating tumor heterogeneity and personalized medicine. Chin J Cancer Res. 2020; 32: 408–13.
    OpenUrl
  25. 25.↵
    2. Linkous A,
    3. Fine HA.
    Generating patient-derived gliomas within cerebral organoids. STAR Protoc. 2020; 1: 100008.
  26. 26.↵
    2. Liang L,
    3. Cui R,
    4. Zhong S,
    5. Wang Z,
    6. He Z,
    7. Duan H, et al.
    Analysis of the potential role of photocurable hydrogel in patient-derived glioblastoma organoid culture through RNA sequencing. Biomater Sci. 2022; 10: 4902–14.
    OpenUrl
  27. 27.↵
    2. Oudin A,
    3. Baus V,
    4. Barthelemy V,
    5. Fabian C,
    6. Klein E,
    7. Dieterle M, et al.
    Protocol for derivation of organoids and patient-derived orthotopic xenografts from glioma patient tumors. STAR Protoc. 2021; 2: 100534.
  28. 28.↵
    2. Chen CC,
    3. Li HW,
    4. Wang YL,
    5. Lee CC,
    6. Shen YC,
    7. Hsieh CY, et al.
    Patient-derived tumor organoids as a platform of precision treatment for malignant brain tumors. Sci Rep. 2022; 12: 16399.
  29. 29.↵
    2. Golebiewska A,
    3. Hau AC,
    4. Oudin A,
    5. Stieber D,
    6. Yabo YA,
    7. Baus V, et al.
    Patient-derived organoids and orthotopic xenografts of primary and recurrent gliomas represent relevant patient avatars for precision oncology. Acta Neuropathol. 2020; 140: 919–49.
    OpenUrlCrossRef
  30. 30.↵
    2. Zhang L,
    3. Liu F,
    4. Weygant N,
    5. Zhang J,
    6. Hu P,
    7. Qin Z, et al.
    A novel integrated system using patient-derived glioma cerebral organoids and xenografts for disease modeling and drug screening. Cancer Lett. 2021; 500: 87–97.
    OpenUrl
  31. 31.↵
    2. da Silva B,
    3. Mathew RK,
    4. Polson ES,
    5. Williams J,
    6. Wurdak H.
    Spontaneous glioblastoma spheroid infiltration of early-stage cerebral organoids models brain tumor invasion. SLAS Discov. 2018; 23: 862–8.
    OpenUrl
  32. 32.↵
    2. Gomez GA,
    3. Oksdath M,
    4. Brown MP,
    5. Ebert LM.
    New approaches to model glioblastoma in vitro using brain organoids: implications for precision oncology. Transl Cancer Res. 2019; 8: S606–11.
    OpenUrl
  33. 33.↵
    2. Krieger TG,
    3. Tirier SM,
    4. Park J,
    5. Jechow K,
    6. Eisemann T,
    7. Peterziel H, et al.
    Modeling glioblastoma invasion using human brain organoids and single-cell transcriptomics. Neuro Oncol. 2020; 22: 1138–49.
    OpenUrlCrossRef
  34. 34.↵
    2. Fawal MA,
    3. Jungas T,
    4. Davy A.
    Inhibition of DHFR targets the self-renewing potential of brain tumor initiating cells. Cancer Lett. 2021; 503: 129–37.
    OpenUrl
  35. 35.↵
    2. Weth FR,
    3. Peng L,
    4. Paterson E,
    5. Tan ST,
    6. Gray C.
    Utility of the cerebral organoid glioma ‘GLICO’ model for screening applications. Cells. 2022; 12: 153.
    OpenUrl
  36. 36.↵
    2. Gomez-Oliva R,
    3. Dominguez-Garcia S,
    4. Carrascal L,
    5. Abalos-Martinez J,
    6. Pardillo-Diaz R,
    7. Verastegui C, et al.
    Evolution of experimental models in the study of glioblastoma: toward finding efficient treatments. Front Oncol. 2020; 10: 614295.
  37. 37.↵
    2. Ma X,
    3. Liu J,
    4. Zhu W,
    5. Tang M,
    6. Lawrence N,
    7. Yu C, et al.
    3D bioprinting of functional tissue models for personalized drug screening and in vitro disease modeling. Adv Drug Deliv Rev. 2018; 132: 235–51.
    OpenUrl
  38. 38.↵
    2. Yi HG,
    3. Jeong YH,
    4. Kim Y,
    5. Choi YJ,
    6. Moon HE,
    7. Park SH, et al.
    A bioprinted human-glioblastoma-on-a-chip for the identification of patient-specific responses to chemoradiotherapy. Nat Biomed Eng. 2019; 3: 509–19.
    OpenUrl
  39. 39.↵
    2. Hermida MA,
    3. Kumar JD,
    4. Schwarz D,
    5. Laverty KG,
    6. Di Bartolo A,
    7. Ardron M, et al.
    Three dimensional in vitro models of cancer: bioprinting multilineage glioblastoma models. Adv Biol Regul. 2020; 75: 100658.
  40. 40.↵
    2. Xiao W,
    3. Zhang R,
    4. Sohrabi A,
    5. Ehsanipour A,
    6. Sun S,
    7. Liang J, et al.
    Brain-mimetic 3D culture platforms allow investigation of cooperative effects of extracellular matrix features on therapeutic resistance in glioblastoma. Cancer Res. 2018; 78: 1358–70.
    OpenUrlAbstract/FREE Full Text
  41. 41.↵
    2. Maloney E,
    3. Clark C,
    4. Sivakumar H,
    5. Yoo K,
    6. Aleman J,
    7. Rajan SAP, et al.
    Immersion bioprinting of tumor organoids in multi-well plates for increasing chemotherapy screening throughput. Micromachines (Basel). 2020; 11: 208.
    OpenUrl
  42. 42.↵
    2. Tang M,
    3. Xie Q,
    4. Gimple RC,
    5. Zhong Z,
    6. Tam T,
    7. Tian J, et al.
    Three-dimensional bioprinted glioblastoma microenvironments model cellular dependencies and immune interactions. Cell Res. 2020; 30: 833–53.
    OpenUrl
  43. 43.↵
    2. van Pel DM,
    3. Harada K,
    4. Song D,
    5. Naus CC,
    6. Sin WC.
    Modelling glioma invasion using 3D bioprinting and scaffold-free 3D culture. J Cell Commun Signal. 2018; 12: 723–30.
    OpenUrl
  44. 44.↵
    2. Murphy SV,
    3. Atala A.
    3D bioprinting of tissues and organs. Nat Biotechnol. 2014; 32: 773–85.
    OpenUrlCrossRefPubMed
  45. 45.↵
    2. Zhang I,
    3. Lepine P,
    4. Han C,
    5. Lacalle-Aurioles M,
    6. Chen CX,
    7. Haag R, et al.
    Nanotherapeutic modulation of human neural cells and glioblastoma in organoids and monocultures. Cells. 2020; 9: 2434.
    OpenUrl
  46. 46.↵
    2. Shakya S,
    3. Gromovsky AD,
    4. Hale JS,
    5. Knudsen AM,
    6. Prager B,
    7. Wallace LC, et al.
    Altered lipid metabolism marks glioblastoma stem and non-stem cells in separate tumor niches. Acta Neuropathol Commun. 2021; 9: 101.
    OpenUrl
  47. 47.↵
    2. Liu SJ,
    3. Malatesta M,
    4. Lien BV,
    5. Saha P,
    6. Thombare SS,
    7. Hong SJ, et al.
    CRISPRi-based radiation modifier screen identifies long non-coding RNA therapeutic targets in glioma. Genome Biol. 2020; 21: 83.
    OpenUrl
  48. 48.↵
    2. Kim HM,
    3. Lee SH,
    4. Lim J,
    5. Yoo J,
    6. Hwang DY.
    The epidermal growth factor receptor variant type III mutation frequently found in gliomas induces astrogenesis in human cerebral organoids. Cell Prolif. 2021; 54: e12965.
  49. 49.↵
    2. Antonica F,
    3. Santomaso L,
    4. Pernici D,
    5. Petrucci L,
    6. Aiello G,
    7. Cutarelli A, et al.
    A slow-cycling/quiescent cells subpopulation is involved in glioma invasiveness. Nat Commun. 2022; 13: 4767.
    OpenUrl
  50. 50.↵
    2. Tejero R,
    3. Huang Y,
    4. Katsyv I,
    5. Kluge M,
    6. Lin JY,
    7. Tome-Garcia J, et al.
    Gene signatures of quiescent glioblastoma cells reveal mesenchymal shift and interactions with niche microenvironment. EBioMedicine. 2019; 42: 252–69.
    OpenUrl
  51. 51.↵
    2. Zhang K,
    3. Liu X,
    4. Li G,
    5. Chang X,
    6. Li S,
    7. Chen J, et al.
    Clinical management and survival outcomes of patients with different molecular subtypes of diffuse gliomas in China (2011-2017): a multicenter retrospective study from CGGA. Cancer Biol Med. 2022; 19: 1460–76.
    OpenUrlAbstract/FREE Full Text
  52. 52.↵
    2. Bleijs M,
    3. van de Wetering M,
    4. Clevers H,
    5. Drost J.
    Xenograft and organoid model systems in cancer research. EMBO J. 2019; 38: e101654.
  53. 53.↵
    2. Azzarelli R.
    Organoid models of glioblastoma to study brain tumor stem cells. Front Cell Dev Biol. 2020; 8: 220.
    OpenUrl
  54. 54.↵
    2. Zhang C,
    3. Jin M,
    4. Zhao J,
    5. Chen J,
    6. Jin W.
    Organoid models of glioblastoma: advances, applications and challenges. Am J Cancer Res. 2020; 10: 2242–57.
    OpenUrl
  55. 55.↵
    2. Clevers H.
    Modeling development and disease with organoids. Cell. 2016; 165: 1586–97.
    OpenUrlCrossRefPubMed
  56. 56.↵
    2. Wei S,
    3. Yin D,
    4. Yu S,
    5. Lin X,
    6. Savani MR,
    7. Du K, et al.
    Antitumor activity of a mitochondrial-targeted HSP90 inhibitor in gliomas. Clin Cancer Res. 2022; 28: 2180–95.
    OpenUrl
  57. 57.↵
    2. Jermakowicz AM,
    3. Rybin MJ,
    4. Suter RK,
    5. Sarkaria JN,
    6. Zeier Z,
    7. Feng Y, et al.
    The novel BET inhibitor UM-002 reduces glioblastoma cell proliferation and invasion. Sci Rep. 2021; 11: 23370.
  58. 58.↵
    2. Bayat N,
    3. Izadpanah R,
    4. Ebrahimi-Barough S,
    5. Norouzi Javidan A,
    6. Ai A,
    7. Mokhtari Ardakan MM, et al.
    The anti-angiogenic effect of atorvastatin in glioblastoma spheroids tumor cultured in fibrin gel: in 3D in vitro model. Asian Pac J Cancer Prev. 2018; 19: 2553–60.
    OpenUrl
  59. 59.↵
    2. Reed MR,
    3. Lyle AG,
    4. De Loose A,
    5. Maddukuri L,
    6. Learned K,
    7. Beale HC, et al.
    A functional precision medicine pipeline combines comparative transcriptomics and tumor organoid modeling to identify bespoke treatment strategies for glioblastoma. Cells. 2021; 10: 3400.
    OpenUrlCrossRef
  60. 60.↵
    2. Yi C,
    3. Li G,
    4. Ivanov DN,
    5. Wang Z,
    6. Velasco MX,
    7. Hernandez G, et al.
    Luteolin inhibits Musashi1 binding to RNA and disrupts cancer phenotypes in glioblastoma cells. RNA Biol. 2018; 15: 1420–32.
    OpenUrl
  61. 61.↵
    2. Lenin S,
    3. Ponthier E,
    4. Scheer KG,
    5. Yeo ECF,
    6. Tea MN,
    7. Ebert LM, et al.
    A drug screening pipeline using 2D and 3D patient-derived in vitro models for pre-clinical analysis of therapy response in glioblastoma. Int J Mol Sci. 2021; 22: 4322.
    OpenUrl
  62. 62.↵
    2. Urbaniak A,
    3. Reed MR,
    4. Heflin B,
    5. Gaydos J,
    6. Pina-Oviedo S,
    7. Jedrzejczyk M, et al.
    Anti-glioblastoma activity of monensin and its analogs in an organoid model of cancer. Biomed Pharmacother. 2022; 153: 113440.
  63. 63.↵
    2. Jacob F,
    3. Ming GL,
    4. Song H.
    Generation and biobanking of patient-derived glioblastoma organoids and their application in CAR T cell testing. Nat Protoc. 2020; 15: 4000–33.
    OpenUrlCrossRefPubMed
  64. 64.↵
    2. Schnalzger TE,
    3. de Groot MH,
    4. Zhang C,
    5. Mosa MH,
    6. Michels BE,
    7. Roder J, et al.
    3D model for CAR-mediated cytotoxicity using patient-derived colorectal cancer organoids. EMBO J. 2019; 38: e100928.
  65. 65.↵
    2. Balyasnikova IV,
    3. Zannikou M,
    4. Wang G,
    5. Li Y,
    6. Duffy JT,
    7. Levine RN, et al.
    Indocarbocyanine nanoparticles extravasate and distribute better than liposomes in brain tumors. J Control Release. 2022; 349: 413–24.
    OpenUrl
  66. 66.↵
    2. Ruiz-Garcia H,
    3. Alvarado-Estrada K,
    4. Schiapparelli P,
    5. Quinones-Hinojosa A,
    6. Trifiletti DM.
    Engineering three-dimensional tumor models to study glioma cancer stem cells and tumor microenvironment. Front Cell Neurosci. 2020; 14: 558381.
  67. 67.↵
    2. Mariappan A,
    3. Goranci-Buzhala G,
    4. Ricci-Vitiani L,
    5. Pallini R,
    6. Gopalakrishnan J.
    Trends and challenges in modeling glioma using 3D human brain organoids. Cell Death Differ. 2021; 28: 15–23.
    OpenUrl
  68. 68.↵
    2. Benitez JA,
    3. Finlay D,
    4. Castanza A,
    5. Parisian AD,
    6. Ma J,
    7. Longobardi C, et al.
    PTEN deficiency leads to proteasome addiction: a novel vulnerability in glioblastoma. Neuro Oncol. 2021; 23: 1072–86.
    OpenUrl
  69. 69.↵
    2. Goranci-Buzhala G,
    3. Mariappan A,
    4. Ricci-Vitiani L,
    5. Josipovic N,
    6. Pacioni S,
    7. Gottardo M, et al.
    Cilium induction triggers differentiation of glioma stem cells. Cell Rep. 2021; 36: 109656.
  70. 70.↵
    2. Innes JA,
    3. Lowe AS,
    4. Fonseca R,
    5. Aley N,
    6. El-Hassan T,
    7. Constantinou M, et al.
    Phenotyping clonal populations of glioma stem cell reveals a high degree of plasticity in response to changes of microenvironment. Lab Invest. 2022; 102: 172–84.
    OpenUrl
  71. 71.↵
    2. Zhu Z,
    3. Mesci P,
    4. Bernatchez JA,
    5. Gimple RC,
    6. Wang X,
    7. Schafer ST, et al.
    Zika virus targets glioblastoma stem cells through a SOX2-integrin alpha(v)beta(5) axis. Cell Stem Cell. 2020; 26: 187–204.e10.
    OpenUrlCrossRef
  72. 72.↵
    2. Zhao R,
    3. Li B,
    4. Zhang S,
    5. He Z,
    6. Pan Z,
    7. Guo Q, et al.
    The N(6)-methyladenosine-modified pseudogene HSPA7 correlates with the tumor microenvironment and predicts the response to immune checkpoint therapy in glioblastoma. Front Immunol. 2021; 12: 653711.
  73. 73.↵
    2. Majc B,
    3. Novak M,
    4. Lah TT,
    5. Krizaj I.
    Bioactive peptides from venoms against glioma progression. Front Oncol. 2022; 12: 965882.
  74. 74.↵
    2. Ye E,
    3. Lee JE,
    4. Lim YS,
    5. Yang SH,
    6. Park SM.
    Effect of duty cycles of tumor-treating fields on glioblastoma cells and normal brain organoids. Int J Oncol. 2022; 60: 8.
    OpenUrl
  75. 75.↵
    2. Gamboa CM,
    3. Jara K,
    4. Pamarthy S,
    5. Liu L,
    6. Aiken R,
    7. Xiong Z, et al.
    Generation of glioblastoma patient-derived organoids and mouse brain orthotopic xenografts for drug screening. STAR Protoc. 2021; 2: 100345.
  76. 76.↵
    2. Lee CT,
    3. Bendriem RM,
    4. Wu WW,
    5. Shen RF.
    3D brain organoids derived from pluripotent stem cells: promising experimental models for brain development and neurodegenerative disorders. J Biomed Sci. 2017; 24: 59.
    OpenUrl
  77. 77.↵
    2. Kelava I,
    3. Lancaster MA.
    Dishing out mini-brains: current progress and future prospects in brain organoid research. Dev Biol. 2016; 420: 199–209.
    OpenUrlCrossRefPubMed
  78. 78.↵
    2. Silvia N,
    3. Dai G.
    Cerebral organoids as a model for glioblastoma multiforme. Curr Opin Biomed Eng. 2020; 13: 152–9.
    OpenUrl
  79. 79.↵
    2. Cakir B,
    3. Xiang Y,
    4. Tanaka Y,
    5. Kural MH,
    6. Parent M,
    7. Kang YJ, et al.
    Engineering of human brain organoids with a functional vascular-like system. Nat Methods. 2019; 16: 1169–75.
    OpenUrl
  80. 80.↵
    2. Pham MT,
    3. Pollock KM,
    4. Rose MD,
    5. Cary WA,
    6. Stewart HR,
    7. Zhou P, et al.
    Generation of human vascularized brain organoids. Neuroreport. 2018; 29: 588–93.
    OpenUrlCrossRef
  81. 81.↵
    2. Yan HHN,
    3. Siu HC,
    4. Law S,
    5. Ho SL,
    6. Yue SSK,
    7. Tsui WY, et al.
    A comprehensive human gastric cancer organoid biobank captures tumor subtype heterogeneity and enables therapeutic screening. Cell Stem Cell. 2018; 23: 882–97.
    OpenUrlCrossRefPubMed
  82. 82.
    2. Gao D,
    3. Vela I,
    4. Sboner A,
    5. Iaquinta PJ,
    6. Karthaus WR,
    7. Gopalan A, et al.
    Organoid cultures derived from patients with advanced prostate cancer. Cell. 2014; 159: 176–87.
    OpenUrlCrossRefPubMed
  83. 83.
    2. Seino T,
    3. Kawasaki S,
    4. Shimokawa M,
    5. Tamagawa H,
    6. Toshimitsu K,
    7. Fujii M, et al.
    Human pancreatic tumor organoids reveal loss of stem cell niche factor dependence during disease progression. Cell Stem Cell. 2018; 22: 454–67.
    OpenUrlCrossRefPubMed
  84. 84.↵
    2. Broutier L,
    3. Mastrogiovanni G,
    4. Verstegen MM,
    5. Francies HE,
    6. Gavarro LM,
    7. Bradshaw CR, et al.
    Human primary liver cancer-derived organoid cultures for disease modeling and drug screening. Nat Med. 2017; 23: 1424–35.
    OpenUrlCrossRefPubMed
  85. 85.↵
    2. Ham O,
    3. Jin YB,
    4. Kim J,
    5. Lee MO.
    Blood vessel formation in cerebral organoids formed from human embryonic stem cells. Biochem Biophys Res Commun. 2020; 521: 84–90.
    OpenUrlCrossRef
  86. 86.↵
    2. Klein E,
    3. Hau AC,
    4. Oudin A,
    5. Golebiewska A,
    6. Niclou SP.
    Glioblastoma organoids: pre-clinical applications and challenges in the context of immunotherapy. Front Oncol. 2020; 10: 604121.
  87. 87.↵
    2. Maomao C,
    3. He L,
    4. Dianqin S,
    5. Siyi H,
    6. Xinxin Y,
    7. Fan Y, et al.
    Current cancer burden in China: epidemiology, etiology, and prevention. Cancer Biol Med. 2022; 19: 1121–38.
    OpenUrlAbstract/FREE Full Text
  88. 88.↵
    2. Yang H,
    3. Wang Y,
    4. Wang P,
    5. Zhang N,
    6. Wang P.
    Tumor organoids for cancer research and personalized medicine. Cancer Biol Med. 2021; 19: 319–32.
    OpenUrl
  89. 89.↵
    2. Venkatesh HS,
    3. Morishita W,
    4. Geraghty AC,
    5. Silverbush D,
    6. Gillespie SM,
    7. Arzt M, et al.
    Electrical and synaptic integration of glioma into neural circuits. Nature. 2019; 573: 539–45.
    OpenUrlCrossRefPubMed
  90. 90.↵
    2. Schonrock A,
    3. Heinzelmann E,
    4. Steffl B,
    5. Demirdizen E,
    6. Narayanan A,
    7. Krunic D, et al.
    MEOX2 homeobox gene promotes growth of malignant gliomas. Neuro Oncol. 2022; 24: 1911–24.
    OpenUrl
  91. 91.↵
    2. Heinrich MA,
    3. Bansal R,
    4. Lammers T,
    5. Zhang YS,
    6. Michel Schiffelers R,
    7. Prakash J.
    3D-bioprinted mini-brain: a glioblastoma model to study cellular interactions and therapeutics. Adv Mater. 2019; 31: e1806590.
  92. 92.↵
    2. Ruiz-Garcia H,
    3. Zarco N,
    4. Watanabe F,
    5. De Araujo Farias V,
    6. Suarez-Meade P,
    7. Guerrero-Cazares H, et al.
    Development of experimental three-dimensional tumor models to study glioblastoma cancer stem cells and tumor microenvironment. Methods Mol Biol. 2023; 2572: 117–27.
    OpenUrl
  93. 93.↵
    2. Che J,
    3. DePalma TJ,
    4. Sivakumar H,
    5. Mezache LS,
    6. Tallman MM,
    7. Venere M, et al.
    αCT1 peptide sensitizes glioma cells to temozolomide in a glioblastoma organoid platform. Biotechnol Bioeng. 2023; 120: 1108–19.
    OpenUrl
  94. 94.↵
    2. Pernik MN,
    3. Bird CE,
    4. Traylor JI,
    5. Shi DD,
    6. Richardson TE,
    7. McBrayer SK, et al.
    Patient-derived cancer organoids for precision oncology treatment. J Pers Med. 2021; 11: 423.
    OpenUrl
  95. 95.↵
    2. Ratliff M,
    3. Kim H,
    4. Qi H,
    5. Kim M,
    6. Ku B,
    7. Azorin DD, et al.
    Patient-derived tumor organoids for guidance of personalized drug therapies in recurrent glioblastoma. Int J Mol Sci. 2022; 23: 6572.
    OpenUrl
  96. 96.↵
    2. LeBlanc VG,
    3. Trinh DL,
    4. Aslanpour S,
    5. Hughes M,
    6. Livingstone D,
    7. Jin D, et al.
    Single-cell landscapes of primary glioblastomas and matched explants and cell lines show variable retention of inter- and intratumor heterogeneity. Cancer Cell. 2022; 40: 379–92.
    OpenUrl
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