Heterogeneity and individualized treatment of microenvironment in glioblastoma (Review)
- Authors:
- Wei Kang
- Zhixiao Mo
- Wenshan Li
- Haifeng Ma
- Qiang Zhang
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Affiliations: Department of Neurosurgery, Qinghai Provincial People's Hospital, Xining, Qinghai 810001, P.R. China, Department of Neurosurgery, Qinghai Cardio‑Cerebrovascular Hospital, Xining, Qinghai 810099, P.R. China - Published online on: October 25, 2023 https://doi.org/10.3892/or.2023.8654
- Article Number: 217
-
Copyright: © Kang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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|
Junttila MR and de Sauvage FJ: Influence of tumor micro-environment heterogeneity on therapeutic response. Nature. 501:346–354. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Nawaz S and Yuan Y: Computational pathology: Exploring the spatial dimension of tumor ecology. Cancer Lett. 380:296–303. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Greaves M and Maley CC: Clonal evolution in cancer. Nature. 481:306–313. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J, Cazzato E, Ladewig E, Frattini V, Rosenbloom DI, Zairis S, Abate F, Liu Z, Elliott O, Shin YJ, et al: Clonal evolution of glioblastoma under therapy. Nat Genet. 48:768–476. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Azizi E, Carr AJ, Plitas G, Cornish AE, Konopacki C, Prabhakaran S, Nainys J, Wu K, Kiseliovas V, Setty M, et al: Single-cell map of diverse immune phenotypes in the breast tumor microenvironment. Cell. 174:1293–1308.e36. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Chevrier S, Levine JH, Zanotelli VRT, Silina K, Schulz D, Bacac M, Ries CH, Ailles L, Jewett MAS, Moch H, et al: An immune atlas of clear cell renal cell carcinoma. Cell. 169:736–749.e18. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Costa A, Kieffer Y, Scholer-Dahirel A, Pelon F, Bourachot B, Cardon M, Sirven P, Magagna I, Fuhrmann L, Bernard C, et al: Fibroblast heterogeneity and immunosuppressive environment in human breast cancer. Cancer Cell. 33:463–479.e10. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Jia Q, Wu W, Wang Y, Alexander PB, Sun C, Gong Z, Cheng JN, Sun H, Guan Y, Xia X, et al: Local mutational diversity drives intratumoral immune heterogeneity in non-small cell lung cancer. Nat Commun. 9:53612018. View Article : Google Scholar : PubMed/NCBI | |
|
Salmon H, Remark R, Gnjatic S and Merad M: Host tissue determinants of tumor immunity. Nat Rev Cancer. 19:215–227. 2019.PubMed/NCBI | |
|
Dentro SC, Leshchiner I, Haase K, Tarabichi M, Wintersinger J, Deshwar AG, Yu K, Rubanova Y, Macintyre G, Demeulemeester J, et al: Characterizing genetic intratumor heterogeneity across 2,658 human cancer genomes. Cell. 184:2239–2254.e39. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Kumar S, Warrell J, Li S, McGillivray PD, Meyerson W, Salichos L, Harmanci A, Martinez-Fundichely A, Chan CWY, Nielsen MM, et al: Passenger mutations in more than 2,500 cancer genomes: Overall molecular functional impact and consequences. Cell. 180:915–927.e16. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Rosenthal R, Cadieux EL, Salgado R, Bakir MA, Moore DA, Hiley CT, Lund T, Tanić M, Reading JL, Joshi K, et al: Neoantigen-directed immune escape in lung cancer evolution. Nature. 567:479–485. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Lv Y, Zhang S, Liu Z, Tian Y, Liang N and Zhang J: Prognostic value of preoperative neutrophil to lymphocyte ratio is superior to systemic immune inflammation index for survival in patients with glioblastoma. Clin Neurol Neurosurg. 181:24–27. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Pasqualetti F, Giampietro C, Montemurro N, Giannini N, Gadducci G, Orlandi P, Natali E, Chiarugi P, Gonnelli A, Cantarella M, et al: Old and new systemic immune-inflammation indexes are associated with overall survival of glioblastoma patients treated with radio-chemotherapy. Genes (Basel). 13:10542022. View Article : Google Scholar : PubMed/NCBI | |
|
Montemurro N, Pahwa B, Tayal A, Shukla A, De Jesus Encarnacion M, Ramirez I, Nurmukhametov R, Chavda V and De Carlo A: Macrophages in recurrent glioblastoma as a prognostic factor in the synergistic system of the tumor microenvironment. Neurol Int. 15:595–608. 2023. View Article : Google Scholar : PubMed/NCBI | |
|
Flavahan WA, Gaskell E and Bernstein BE: Epigenetic plasticity and the hallmarks of cancer. Science. 357:eaal23802017. View Article : Google Scholar : PubMed/NCBI | |
|
Marks DL, Olson RL and Fernandez-Zapico ME: Epigenetic control of the tumor microenvironment. Epigenomics. 8:1671–1687. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Ishak CA, Classon M and De Carvalho DD: Deregulation of retroelements as an emerging therapeutic opportunity in cancer. Trends Cancer. 4:583–597. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Dagogo-Jack I and Shaw AT: Tumour heterogeneity and resistance to cancer therapies. Nat Rev Clin Oncol. 15:81–94. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y, Martins I, Ma Y, Kepp O, Galluzzi L and Kroemer G: Autophagy-dependent ATP release from dying cells via lysosomal exocytosis. Autophagy. 9:1624–1625. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Stagg J and Smyth MJ: Extracellular adenosine triphosphate and adenosine in cancer. Oncogene. 29:5346–5358. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Yost KE, Satpathy AT, Wells DK, Qi Y, Wang C, Kageyama R, McNamara KL, Granja JM, Sarin KY, Brown RA, et al: Clonal replacement of tumor-specific T cells following PD-1 blockade. Nat Med. 25:1251–1259. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Zou W, Wolchok JD and Chen L: PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: Mechanisms, response biomarkers, and combinations. Sci Transl Med. 8:328rv42016. View Article : Google Scholar : PubMed/NCBI | |
|
Batlle E and Massagué J: Transforming growth factor-β signaling in immunity and cancer. Immunity. 50:924–940. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Ding R, Liu S, Wang S, Chen H, Wang F, Xu Q, Zhu L, Dong X, Gu Y, Zhang X, et al: Single-cell transcriptome analysis of the heterogeneous effects of differential expression of tumor PD-L1 on responding TCR-T cells. Theranostics. 11:4957–4974. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Lamplugh Z and Fan Y: Vascular microenvironment, tumor Immunity and Immunotherapy. Front Immunol. 12:8114852021. View Article : Google Scholar : PubMed/NCBI | |
|
Fu T, Dai LJ, Wu SY, Xiao Y, Ma D, Jiang YZ and Shao ZM: Spatial architecture of the immune microenvironment orchestrates tumor immunity and therapeutic response. J Hematol Oncol. 14:982021. View Article : Google Scholar : PubMed/NCBI | |
|
Montenegro F and Indraccolo S: Metabolism in the tumor microenvironment. Adv Exp Med Biol. 1263:1–11. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Binnewies M, Roberts EW, Kersten K, Chan V, Fearon DF, Merad M, Coussens LM, Gabrilovich DI, Ostrand-Rosenberg S, Hedrick CC, et al: Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med. 24:541–550. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Joshi K, de Massy MR, Ismail M, Reading JL, Uddin I, Woolston A, Hatipoglu E, Oakes T, Rosenthal R, Peacock T, et al: Spatial heterogeneity of the T cell receptor repertoire reflects the mutational landscape in lung cancer. Nat Med. 25:1549–1559. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Bastola S, Pavlyukov MS, Yamashita D, Ghosh S, Cho H, Kagaya N, Zhang Z, Minata M, Lee Y, Sadahiro H, et al: Glioma-initiating cells at tumor edge gain signals from tumor core cells to promote their malignancy. Nat Commun. 11:46602020. View Article : Google Scholar : PubMed/NCBI | |
|
Lambrechts D, Wauters E, Boeckx B, Aibar S, Nittner D, Burton O, Bassez A, Decaluwé H, Pircher A, Van den Eynde K, et al: Phenotype molding of stromal cells in the lung tumor microenvironment. Nat Med. 24:1277–1289. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Zhu J and Thompson CB: Metabolic regulation of cell growth and proliferation. Nat Rev Mol Cell Biol. 20:436–450. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Sayaman RW, Saad M, Thorsson V, Hu D, Hendrickx W, Roelands J, Porta-Pardo E, Mokrab Y, Farshidfar F, Kirchhoff T, et al: Germline genetic contribution to the immune landscape of cancer. Immunity. 54:367–386.e8. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Maynard A, McCoach CE, Rotow JK, Harris L, Haderk F, Kerr DL, Yu EA, Schenk EL, Tan W, Zee A, et al: Therapy-induced evolution of human lung cancer revealed by single-cell RNA sequencing. Cell. 182:1232–1251.e22. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Bernard V, Semaan A, Huang J, San Lucas FA, Mulu FC, Stephens BM, Guerrero PA, Huang Y, Zhao J, Kamyabi N, et al: Single-cell transcriptomics of pancreatic cancer precursors demonstrates epithelial and microenvironmental heterogeneity as an early event in neoplastic progression. Clin Cancer Res. 25:2194–2205. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Mascaux C, Angelova M, Vasaturo A, Beane J, Hijazi K, Anthoine G, Buttard B, Rothe F, Willard-Gallo K, Haller A, et al: Immune evasion before tumor invasion in early lung squamous carcinogenesis. Nature. 571:570–575. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Riaz N, Havel JJ, Makarov V, Desrichard A, Urba WJ, Sims JS, Hodi FS, Martín-Algarra S, Mandal R, Sharfman WH, et al: Tumor and microenvironment evolution during immunotherapy with nivolumab. Cell. 171:934–949.e16. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Jiang T, Yan Y, Zhou K, Su C, Ren S, Li N, Hou L, Guo X, Zhu W, Zhang H, et al: Characterization of evolution trajectory and immune profiling of brain metastasis in lung adenocarcinoma. NPJ Precis Oncol. 5:62021. View Article : Google Scholar : PubMed/NCBI | |
|
AbdulJabbar K, Raza SEA, Rosenthal R, Jamal-Hanjani M, Veeriah S, Akarca A, Lund T, Moore DA, Salgado R, Al Bakir M, et al: Geospatial immune variability illuminates differential evolution of lung adenocarcinoma. Nat Med. 26:1054–1062. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Gatto L, Franceschi E, Di Nunno V, Tosoni A, Lodi R and Brandes AA: Liquid biopsy in glioblastoma management: From current research to future perspectives. Oncologist. 26:865–878. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Postel M, Roosen A, Laurent-Puig P, Taly V and Wang-Renault SF: Droplet-based digital PCR and next generation sequencing for monitoring circulating tumor DNA: A cancer diagnostic perspective. Expert Rev Mol Diagn. 18:7–17. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Karlin-Neumann G: Improved liquid biopsies with combined digital PCR and next-generation sequencing. Am Lab Mag. 48:17–19. 2016. | |
|
Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, Bartlett BR, Wang H, Luber B, Alani RM, et al: Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med. 6:224ra242014. View Article : Google Scholar : PubMed/NCBI | |
|
Piccioni DE, Achrol AS, Kiedrowski LA, Banks KC, Boucher N, Barkhoudarian G, Kelly DF, Juarez T, Lanman RB, Raymond VM, et al: Analysis of cell-free circulating tumor DNA in 419 patients with glioblastoma and other primary brain tumors. CNS Oncol. 8:CNS342019. View Article : Google Scholar : PubMed/NCBI | |
|
Mair R, Mouliere F, Smith CG, Chandrananda D, Gale D, Marass F, Tsui DWY, Massie CE, Wright AJ, Watts C, et al: Measurement of plasma cell-free mitochondrial tumor DNA improves detection of glioblastoma in patient-derived orthotopic xenograft models. Cancer Res. 79:220–230. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Janjua TI, Rewatkar P, Ahmed-Cox A, Saeed I, Mansfeld FM, Kulshreshtha R, Kumeria T, Ziegler DS, Kavallaris M, Mazzieri R and Popat A: Frontiers in the treatment of glioblastoma: Past, present and emerging. Adv Drug Deliv Rev. 171:108–138. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Wong ET, Lok E and Swanson KD: Clinical benefit in recurrent glioblastoma from adjuvant NovoTTF-100A and TCCC after temozolomide and bevacizumab failure: A preliminary observation. Cancer Med. 4:383–391. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Taal W, Oosterkamp HM, Walenkamp AM, Dubbink HJ, Beerepoot LV, Hanse MC, Buter J, Honkoop AH, Boerman D, de Vos FY, et al: Single-agent bevacizumab or lomustine versus a combination of bevacizumab plus lomustine in patients with recurrent glioblastoma (BELOB trial): A randomised controlled phase 2 trial. Lancet Oncol. 15:943–953. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Cloughesy TF, Mochizuki AY, Orpilla JR, Hugo W, Lee AH, Davidson TB, Wang AC, Ellingson BM, Rytlewski JA, Sanders CM, et al: Neoadjuvant anti-PD-1 immunotherapy promotes a survival benefit with intratumoral and systemic immune responses in recurrent glioblastoma. Nat Med. 25:477–486. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Di Cintio F, Dal Bo M, Baboci L, De Mattia E, Polano M and Toffoli G: The molecular and microenvironmental landscape of glioblastomas: Implications for the novel treatment choices. Front Neurosci. 14:6036472020. View Article : Google Scholar : PubMed/NCBI | |
|
Reardon DA, Desjardins A, Vredenburgh JJ, O'Rourke DM, Tran DD, Fink KL, Nabors LB, Li G, Bota DA, Lukas RV, et al: Rindopepimut with bevacizumab for patients with relapsed EGFRvIII-expressing glioblastoma (ReACT): Results of a double-blind randomized phase II trial. Clin Cancer Res. 26:1586–1594. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Fenstermaker RA, Ciesielski MJ, Qiu J, Yang N, Frank CL, Lee KP, Mechtler LR, Belal A, Ahluwalia MS and Hutson AD: Clinical study of a survivin long peptide vaccine (SurVaxM) in patients with recurrent malignant glioma. Cancer Immunol Immunother. 65:1339–1352. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Y, Mudgal P, Wang L, Wu H, Huang N, Alexander PB, Gao Z, Ji N and Li QJ: T cell receptor repertoire as a prognosis marker for heat shock protein peptide complex-96 vaccine trial against newly diagnosed glioblastoma. Oncoimmunology. 9:17494762020. View Article : Google Scholar : PubMed/NCBI | |
|
Cloughesy TF, Landolfi J, Vogelbaum MA, Ostertag D, Elder JB, Bloomfield S, Carter B, Chen CC, Kalkanis SN, Kesari S, et al: Durable complete responses in some recurrent high-grade glioma patients treated with Toca 511 + Toca FC. Neuro Oncol. 20:1383–1392. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Ene CI, Fueyo J and Lang FF: Delta-24 adenoviral therapy for glioblastoma: Evolution from the bench to bedside and future considerations. Neurosurg Focus. 50:E62021. View Article : Google Scholar : PubMed/NCBI | |
|
Raje N, Berdeja J, Lin Y, Siegel D, Jagannath S, Madduri D, Liedtke M, Rosenblatt J, Maus MV, Turka A, et al: Anti-BCMA CAR T-Cell therapy bb2121 in relapsed or refractory multiple myeloma. N Engl J Med. 380:1726–1737. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Lemoine J, Ruella M and Houot R: Born to survive: How cancer cells resist CAR T cell therapy. J Hematol Oncol. 14:1992021. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang H, Gao L, Liu L, Wang J, Wang S, Gao L, Zhang C, Liu Y, Kong P, Liu J, et al: A Bcma and CD19 bispecific CAR-T for relapsed and refractory multiple myeloma. Blood. 134:31472019. View Article : Google Scholar | |
|
Xie B, Li Z, Zhou J and Wang W: Current status and perspectives of dual-targeting chimeric antigen receptor T-cell therapy for the treatment of hematological malignancies. Cancers (Basel). 14:32302022. View Article : Google Scholar : PubMed/NCBI | |
|
Chen H, Kuhn J, Lamborn KR, Abrey LE, DeAngelis LM, Lieberman F, Robins HI, Chang SM, Yung WKA, Drappatz J, et al: Phase I/II study of sorafenib in combination with erlotinib for recurrent glioblastoma as part of a 3-arm sequential accrual clinical trial: NABTC 05-02. Neurooncol. 2:vdaa1242020. | |
|
Jia Q, Wang A, Yuan Y, Zhu B and Long H: Heterogeneity of the tumor immune microenvironment and its clinical relevance. Exp Hematol Oncol. 11:242022. View Article : Google Scholar : PubMed/NCBI | |
|
Wang H, Tao Z, Feng M, Li X, Deng Z, Zhao G, Yin H, Pan T, Chen G, Feng Z, et al: Dual PLK1 and STAT3 inhibition promotes glioblastoma cells apoptosis through MYC. Biochem Biophys Res Commun. 533:368–375. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Wu J, Yuan Y, Long Priel DA, Fink D, Peer CJ, Sissung TM, Su YT, Pang Y, Yu G, Butler MK, et al: Phase I study of zotiraciclib in combination with temozolomide for patients with recurrent high-grade astrocytomas. Clin Cancer Res. 27:3298–3306. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Weiss T, Puca E, Silginer M, Hemmerle T, Pazahr S, Bink A, Weller M, Neri D and Roth P: Immunocytokines are a promising immunotherapeutic approach against glioblastoma. Sci Transl Med. 12:eabb23112020. View Article : Google Scholar : PubMed/NCBI | |
|
Zang L, Kondengaden SM, Che F, Wang L and Heng X: Potential epigenetic-based therapeutic targets for glioma. Front Mol Neurosci. 11:4082018. View Article : Google Scholar : PubMed/NCBI | |
|
Higuchi F, Nagashima H, Ning J, Koerner MVA, Wakimoto H and Cahill DP: Restoration of temozolomide sensitivity by PARP inhibitors in mismatch repair deficient glioblastoma is independent of base excision repair. Clin Cancer Res. 26:1690–1699. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Kopa P, Macieja A, Gulbas I, Pastwa E and Poplawski T: Inhibition of DNA-PK potentiates the synergistic effect of NK314 and etoposide combination on human glioblastoma cells. Mol Biol Rep. 47:67–76. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Lesueur P, Chevalier F, El-Habr EA, Junier MP, Chneiweiss H, Castera L, Müller E, Stefan D and Saintigny Y: Radiosensitization effect of talazoparib, a PARP inhibitor, on glioblastoma stem cells exposed to low and high linear energy transfer radiation. Sci Rep. 8:36642018. View Article : Google Scholar : PubMed/NCBI | |
|
Shaffer R, Nichol AM, Vollans E, Fong M, Nakano S, Moiseenko V, Schmuland M, Ma R, McKenzie M and Otto K A: A comparison of volumetric modulated arc therapy and conventional intensity-modulated radiotherapy for frontal and temporal high-grade gliomas. Int J Radiat Oncol Biol Phys. 76:1177–1184. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Bunevicius A and Sheehan JP: Radiosurgery for glioblastoma. Neurosurg Clin N Am. 32:117–128. 2021. View Article : Google Scholar : PubMed/NCBI |
