Receptor Tyrosine Kinases as Candidate Prognostic Biomarkers and Therapeutic Targets in Meningioma
Abstract
:1. Introduction
2. Molecular Changes and Novel Molecularly Targeted Therapeutic Strategies
Potential Role for Anti-Angiogenic, Hormone, and Immune-Based Therapeutical Modalities in MGM
3. Current and Candidate Biomarkers in MGM
4. RTKs as Candidate Prognostic Biomarkers in MGM
5. Concluding Remarks
Author Contributions
Funding
Conflicts of Interest
References
- Ostrom, Q.T.; Gittleman, H.; Truitt, G.; Boscia, A.; Kruchko, C.; Barnholtz-Sloan, J. CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2011–2015. Neuro-Oncol. 2018, 20, iv1–iv86. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Louis, D.N.; Perry, A.; Reifenberger, G.; von Deimling, A.; Figarella-Branger, D.; Cavenee, W.K.; Ohgaki, H.; Wiestler, O.D.; Kleihues, P.; Ellison, D.W. The 2016 World Health Organization Classification of Tumors of the Central Nervous System: A summary. Acta Neuropathol. 2016, 131, 803–820. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huntoon, K.; Toland, A.M.S.; Dahiya, S. Meningioma: A Review of Clinicopathological and Molecular Aspects. Front. Oncol. 2020, 10, 579599. [Google Scholar] [CrossRef] [PubMed]
- Slot, K.M.; Verbaan, D.; Buis, D.R.; Schoonmade, L.J.; Berckel, B.N.M.; Vandertop, W.P. Prediction of Meningioma WHO Grade Using PET Findings: A Systematic Review and Meta-Analysis. J. Neuroimaging 2020, 31, 6–19. [Google Scholar] [CrossRef] [PubMed]
- Magill, S.T.; Vasudevan, H.N.; Seo, K.; Villanueva-Meyer, J.E.; Choudhury, A.; Liu, S.J.; Pekmezci, M.; Findakly, S.; Hilz, S.; Lastella, S.; et al. Multiplatform genomic profiling and magnetic resonance imaging identify mechanisms underlying intratumor heterogeneity in meningioma. Nat. Commun. 2020, 11, 1–15. [Google Scholar] [CrossRef]
- Birzu, C.; Peyre, M.; Sahm, F. Molecular alterations in meningioma: Prognostic and therapeutic perspectives. Curr. Opin. Oncol. 2020, 32, 613–622. [Google Scholar] [CrossRef]
- Delgado-López, P.D.; Cubo-Delgado, E.; González-Bernal, J.J.; Martín-Alonso, J. A Practical Overview on the Molecular Biology of Meningioma. Curr. Neurol. Neurosci. Rep. 2020, 20, 1–12. [Google Scholar] [CrossRef]
- Kalamarides, M.; O Stemmerrachamimov, A.; Kawakita, M.; Chareyre, F.; Taranchon, E.; Han, Z.-Y.; Martinelli, C.; A Lusis, E.; Hegedus, B.; Gutmann, D.; et al. Identification of a progenitor cell of origin capable of generating diverse meningioma histological subtypes. Oncogene 2011, 30, 2333–2344. [Google Scholar] [CrossRef] [Green Version]
- Tohma, Y.; Yamashima, T.; Yamashita, J. Immunohistochemical localization of cell adhesion molecule epithelial cadherin in human arachnoid villi and meningiomas. Cancer Res. 1992, 52. [Google Scholar]
- Shao, Z.; Liu, L.; Zheng, Y.; Tu, S.; Pan, Y.; Yan, S.; Wei, Q.; Shao, A.; Zhang, J. Molecular Mechanism and Approach in Progression of Meningioma. Front. Oncol. 2020, 10. [Google Scholar] [CrossRef]
- Shivapathasundram, G.; Wickremesekera, A.C.; Tan, S.T.; Itinteang, T. Tumour stem cells in meningioma: A review. J. Clin. Neurosci. 2017, 47, 66–71. [Google Scholar] [CrossRef]
- Apra, C.; Peyre, M.; Kalamarides, M. Current treatment options for meningioma. Expert Rev. Neurother. 2018, 18, 241–249. [Google Scholar] [CrossRef]
- Brastianos, P.K.; Galanis, E.; Butowski, N.; Chan, J.W.; Dunn, I.F.; Goldbrunner, R.; Herold-Mende, C.; Ippen, F.M.; Mawrin, C.; McDermott, M.W.; et al. Advances in multidisciplinary therapy for meningiomas. Neuro-Oncol. 2019, 21, i18–i31. [Google Scholar] [CrossRef] [Green Version]
- Gardner, P.A.; Kassam, A.B.; Thomas, A.; Snyderman, C.H.; Carrau, R.L.; Mintz, A.H.; Prevedello, D.M. ENDOSCOPIC ENDONASAL RESECTION OF ANTERIOR CRANIAL BASE MENINGIOMAS. Neurosurgery 2008, 63, 36–54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mirimanoff, R.O.; Dosoretz, D.E.; Linggood, R.M.; Ojemann, R.G.; Martuza, R.L. Meningioma: Analysis of recurrence and progression following neurosurgical resection. J. Neurosurg. 1985, 62, 18–24. [Google Scholar] [CrossRef] [PubMed]
- Karsy, M.; Azab, M.A.; Abou-Al-Shaar, H.; Guan, J.; Eli, I.; Jensen, R.L.; Ormond, D.R. Clinical potential of meningioma genomic insights: A practical review for neurosurgeons. Neurosurg. Focus 2018, 44, E10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Preusser, M.; Brastianos, P.; Mawrin, C. Advances in meningioma genetics: Novel therapeutic opportunities. Nat. Rev. Neurol. 2018, 14, 106–115. [Google Scholar] [CrossRef]
- Shaikh, N.; Dixit, K.; Raizer, J. Recent advances in managing/understanding meningioma. F1000Research 2018, 7, 490. [Google Scholar] [CrossRef]
- Pećina-Šlaus, N.; Kafka, A.; Lechpammer, M. Molecular Genetics of Intracranial Meningiomas with Emphasis on Canonical Wnt Signalling. Cancers 2016, 8, 67. [Google Scholar] [CrossRef] [Green Version]
- E Leone, P.; Bello, M.J.; De Campos, J.M.; Vaquero, J.; Sarasa, J.L.; Pestaña, A.; A Rey, J. NF2 gene mutations and allelic status of 1p, 14q and 22q in sporadic meningiomas. Oncogene 1999, 18, 2231–2239. [Google Scholar] [CrossRef] [Green Version]
- Al-Rashed, M.; Foshay, K.; Abedalthagafi, M. Recent Advances in Meningioma Immunogenetics. Front. Oncol. 2020, 9. [Google Scholar] [CrossRef] [PubMed]
- Sahm, F.; Schrimpf, D.; Olar, A.; Koelsche, C.; E Reuss, D.; Bissel, J.; Kratz, A.; Capper, D.; Schefzyk, S.; Hielscher, T.; et al. TERT Promoter Mutations and Risk of Recurrence in Meningioma. J. Natl. Cancer Inst. 2015, 108. [Google Scholar] [CrossRef]
- Juratli, T.A.; McCabe, D.; Nayyar, N.; Williams, E.A.; Silverman, I.; Tummala, S.S.; Fink, A.L.; Baig, A.; Martinez-Lage, M.; Selig, M.K.; et al. DMD genomic deletions characterize a subset of progressive/higher-grade meningiomas with poor outcome. Acta Neuropathol. 2018, 136, 779–792. [Google Scholar] [CrossRef]
- Ferluga, S.; Baiz, D.; A Hilton, D.; Adams, C.; Ercolano, E.; Dunn, J.; Bassiri, K.; Kurian, K.M.; O Hanemann, C. Constitutive activation of the EGFR–STAT1 axis increases proliferation of meningioma tumor cells. Neuro-Oncol. Adv. 2020, 2, vdaa008. [Google Scholar] [CrossRef] [Green Version]
- Tuchen, M.; Wilisch-Neumann, A.; Daniel, E.A.; Baldauf, L.; Pachow, D.; Scholz, J.; Angenstein, F.; Stork, O.; Kirches, E.; Mawrin, C. Receptor tyrosine kinase inhibition by regorafenib/sorafenib inhibits growth and invasion of meningioma cells. Eur. J. Cancer 2017, 73, 9–21. [Google Scholar] [CrossRef]
- Kaley, T.J.; Wen, P.; Schiff, D.; Ligon, K.; Haidar, S.; Karimi, S.; Lassman, A.B.; Nolan, C.P.; DeAngelis, L.M.; Gavrilovic, I.; et al. Phase II trial of sunitinib for recurrent and progressive atypical and anaplastic meningioma. Neuro-Oncol. 2014, 17, 116–121. [Google Scholar] [CrossRef] [Green Version]
- Raheja, A.; Colman, H.; Palmer, C.A.; Couldwell, W.T. Dramatic radiographic response resulting in cerebrospinal fluid rhinorrhea associated with sunitinib therapy in recurrent atypical meningioma: Case report. J. Neurosurg. 2017, 127, 965–970. [Google Scholar] [CrossRef]
- Raizer, J.J.; Grimm, S.A.; Rademaker, A.; Chandler, J.P.; Muro, K.; Helenowski, I.; Rice, L.; McCarthy, K.; Johnston, S.K.; Mrugala, M.M.; et al. A phase II trial of PTK787/ZK 222584 in recurrent or progressive radiation and surgery refractory meningiomas. J. Neuro-Oncol. 2014, 117, 93–101. [Google Scholar] [CrossRef]
- Horak, P.; Woehrer, A.; Hassler, M.; Hainfellner, J.; Preusser, M.; Marosi, C. Imatinib mesylate treatment of recurrent meningiomas in preselected patients: A retrospective analysis. J. Neuro-Oncol. 2012, 109, 323–330. [Google Scholar] [CrossRef] [PubMed]
- Pachow, D.; Andrae, N.; Kliese, N.; Angenstein, F.; Stork, O.; Wilisch-Neumann, A.; Kirches, E.; Mawrin, C. mTORC1 Inhibitors Suppress Meningioma Growth in Mouse Models. Clin. Cancer Res. 2013, 19, 1180–1189. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beauchamp, R.L.; Erdin, S.; Witt, L.; Jordan, J.T.; Plotkin, S.R.; Gusella, J.F.; Ramesh, V. mTOR kinase inhibition disrupts neuregulin 1-ERBB3 autocrine signaling and sensitizes NF2-deficient meningioma cellular models to IGF1R inhibition. J. Biol. Chem. 2021, 296, 100157. [Google Scholar] [CrossRef]
- Graillon, T.; Sanson, M.; Campello, C.; Idbaih, A.; Peyre, M.; Peyrière, H.; Basset, N.; Autran, D.; Roche, C.; Kalamarides, M.; et al. Everolimus and Octreotide for Patients with Recurrent Meningioma: Results from the Phase II CEVOREM Trial. Clin. Cancer Res. 2020, 26, 552–557. [Google Scholar] [CrossRef]
- Lamszus, K.; Lengler, U.; Schmidt, N.O.; Stavrou, D.; Ergün, S.; Westphal, M. Vascular Endothelial Growth Factor, Hepatocyte Growth Factor/Scatter Factor, Basic Fibroblast Growth Factor, and Placenta Growth Factor in Human Meningiomas and Their Relation to Angiogenesis and Malignancy. Neurosurgery 2000, 46, 938–948. [Google Scholar] [CrossRef]
- Cardona, A.F.; Ruiz-Patiño, A.; Zatarain-Barrón, Z.L.; Hakim, F.; Jiménez, E.; Mejía, J.A.; Ramón, J.F.; Useche, N.; Bermúdez, S.; Pineda, D.; et al. Systemic management of malignant meningiomas: A comparative survival and molecular marker analysis between Octreotide in combination with Everolimus and Sunitinib. PLoS ONE 2019, 14, e0217340. [Google Scholar] [CrossRef]
- Lou, E.; Sumrall, A.L.; Turner, S.; Peters, K.B.; Desjardins, A.; Vredenburgh, J.J.; McLendon, R.E.; Herndon, J.E.; McSherry, F.; Norfleet, J.; et al. Bevacizumab therapy for adults with recurrent/progressive meningioma: A retrospective series. J. Neuro-Oncol. 2012, 109, 63–70. [Google Scholar] [CrossRef] [Green Version]
- Nayak, L.; Iwamoto, F.M.; Rudnick, J.D.; Norden, A.D.; Lee, E.Q.; Drappatz, J.; Omuro, A.; Kaley, T.J. Atypical and anaplastic meningiomas treated with bevacizumab. J. Neuro-Oncol. 2012, 109, 187–193. [Google Scholar] [CrossRef]
- Nigim, F.; Wakimoto, H.; Kasper, E.M.; Ackermans, L.; Temel, Y. Emerging Medical Treatments for Meningioma in the Molecular Era. Biomedicines 2018, 6, 86. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shih, K.C.; Chowdhary, S.; Rosenblatt, P.; Weir, A.B.; Shepard, G.C.; Williams, J.T.; Shastry, M.; Burris, H.A.; Hainsworth, J.D.; Iii, A.B.W. A phase II trial of bevacizumab and everolimus as treatment for patients with refractory, progressive intracranial meningioma. J. Neuro-Oncol. 2016, 129, 281–288. [Google Scholar] [CrossRef] [PubMed]
- Kotecha, R.; Tonse, R.; Appel, H.; Odia, Y.; Kotecha, R.; Rabinowits, G.; Mehta, M. Regression of Intracranial Meningiomas Following Treatment with Cabozantinib. Curr. Oncol. 2021, 28, 1537–1543. [Google Scholar] [CrossRef] [PubMed]
- Du, Z.; Abedalthagafi, M.; Aizer, A.A.; McHenry, A.R.; Sun, H.H.; Bray, M.-A.; Viramontes, O.; Machaidze, R.; Brastianos, P.; Reardon, D.A.; et al. Increased expression of the immune modulatory molecule PD-L1 (CD274) in anaplastic meningioma. Oncotarget 2014, 6, 4704–4716. [Google Scholar] [CrossRef] [Green Version]
- Hsu, D.W.; Efird, J.T.; Hedley-Whyte, E.T. Progesterone and estrogen receptors in meningiomas: Prognostic considerations. J. Neurosurg. 1997, 86, 113–120. [Google Scholar] [CrossRef]
- Touat, M.; Lombardi, G.; Farina, P.; Kalamarides, M.; Sanson, M. Successful treatment of multiple intracranial meningiomas with the antiprogesterone receptor agent mifepristone (RU486). Acta Neurochir. 2014, 156, 1831–1835. [Google Scholar] [CrossRef]
- Ji, Y.; Rankin, C.J.; Grunberg, S.M.; Sherrod, A.E.; Ahmadi, J.; Townsend, J.J.; Feun, L.G.; Fredericks, R.K.; Russell, C.A.; Kabbinavar, F.F.; et al. Double-Blind Phase III Randomized Trial of the Antiprogestin Agent Mifepristone in the Treatment of Unresectable Meningioma: SWOG S9005. J. Clin. Oncol. 2015, 33, 4093–4098. [Google Scholar] [CrossRef]
- Sofela, A.A.; McGavin, L.; Whitfield, P.C.; Hanemann, C.O. Biomarkers for differentiating grade II meningiomas from grade I: A systematic review. Br. J. Neurosurg. 2021, 1–7. [Google Scholar] [CrossRef]
- Schmidt, M.; Möck, A.; Jungk, C.; Sahm, F.; Ull, A.T.; Warta, R.; Lamszus, K.; Gousias, K.; Ketter, R.; Roesch, S.; et al. Transcriptomic analysis of aggressive meningiomas identifies PTTG1 and LEPR as prognostic biomarkers independent of WHO grade. Oncotarget 2016, 7, 14551–14568. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barkhoudarian, G.; Whitelegge, J.P. Proteomics Analysis of Brain Meningiomas in Pursuit of Novel Biomarkers of the Aggressive Behavior. J. Proteom. Bioinform. 2016, 09, 53–57. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abbritti, R.V.; Polito, F.; Cucinotta, M.; Giudice, C.L.; Caffo, M.; Tomasello, C.; Germanò, A.; Aguennouz, M. Meningiomas and Proteomics: Focus on New Potential Biomarkers and Molecular Pathways. Cancer Genom. Proteom. 2016, 13, 369–380. [Google Scholar]
- Kim, J.H.; Lee, S.K.; Yoo, Y.C.; Park, N.H.; Park, D.B.; Yoo, J.S.; An, H.J.; Park, Y.M.; Cho, K.G. Proteome analysis of human cerebrospinal fluid as a diagnostic biomarker in patients with meningioma. Med Sci. Monit. 2012, 18, BR450–BR460. [Google Scholar] [CrossRef] [Green Version]
- Nazem, A.A.; Ruzevick, J.; Jr, M.J.F. Advances in meningioma genomics, proteomics, and epigenetics: Insights into biomarker identification and targeted therapies. Oncotarget 2020, 11, 4544–4553. [Google Scholar] [CrossRef]
- Gousias, K.; Niehusmann, P.; Gielen, G.H.; Simon, M. Karyopherin a2 and chromosome region maintenance protein 1 expression in meningiomas: Novel biomarkers for recurrence and malignant progression. J. Neuro-Oncol. 2014, 118, 289–296. [Google Scholar] [CrossRef]
- Menke, J.R.; Raleigh, D.R.; Gown, A.M.; Thomas, S.; Perry, A.; Tihan, T. Somatostatin receptor 2a is a more sensitive diagnostic marker of meningioma than epithelial membrane antigen. Acta Neuropathol. 2015, 130, 441–443. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Osbun, J.W.; Tatman, P.D.; Kaur, S.; Parada, C.A.; Busald, T.; Gonzalez-Cuyar, L.; Shi, M.; Born, D.E.; Zhang, J.; Ferreira, M. Comparative Proteomic Profiling Using Two-Dimensional Gel Electrophoresis and Identification via LC-MS/MS Reveals Novel Protein Biomarkers to Identify Aggressive Subtypes of WHO Grade I Meningioma. J. Neurol. Surg. Part B Skull Base 2017, 78, 371–379. [Google Scholar] [CrossRef] [PubMed]
- Alamir, H.; AlOmari, M.; Salwati, A.A.A.; Saka, M.; Bangash, M.; Baeesa, S.; Alghamdi, F.; Carracedo, A.; Schulten, H.-J.; Chaudhary, A.; et al. In situ characterization of stem cells-like biomarkers in meningiomas. Cancer Cell Int. 2018, 18, 77. [Google Scholar] [CrossRef] [PubMed]
- Erkan, E.P.; Ströbel, T.; Dorfer, C.; Sonntagbauer, M.; Weinhäusel, A.; Saydam, N.; Saydam, O. Circulating Tumor Biomarkers in Meningiomas Reveal a Signature of Equilibrium Between Tumor Growth and Immune Modulation. Front. Oncol. 2019, 9, 1031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Samal, S.; Patnaik, A.; Purkait, S.; Sahu, F. Altered expression of epigenetic modifiers EZH2, H3K27me3, and DNA methyltransferases in meningiomas—Prognostic biomarkers for routine practice. Folia Neuropathol. 2020, 58, 133–142. [Google Scholar] [CrossRef]
- Collord, G.; Tarpey, P.; Kurbatova, N.; Martincorena, I.; Moran, S.; Castro, M.; Nagy, T.; Bignell, G.; Maura, F.; Young, M.D.; et al. An integrated genomic analysis of anaplastic meningioma identifies prognostic molecular signatures. Sci. Rep. 2018, 8, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Mittal, P.; Roberts, C.W.M. The SWI/SNF complex in cancer—Biology, biomarkers and therapy. Nat. Rev. Clin. Oncol. 2020, 17, 435–448. [Google Scholar] [CrossRef]
- Liu, Z.Y.; Wang, J.Y.; Liu, H.H.; Ma, X.M.; Wang, C.L.; Zhang, X.P.; Tao, Y.Q.; Lu, Y.C.; Liao, J.C.; Hu, G.H. Retinoblastoma protein-interacting zinc-finger gene 1 (RIZ1) dysregulation in human malignant meningiomas. Oncogene 2012, 32, 1216–1222. [Google Scholar] [CrossRef]
- Jun, P.; Hong, C.; Lal, A.; Wong, J.M.; McDermott, M.W.; Bollen, A.W.; Plass, C.; Held, W.A.; Smiraglia, D.J.; Costello, J.F. Epigenetic silencing of the kinase tumor suppressor WNK2 is tumor-type and tumor-grade specific. Neuro-Oncol. 2009, 11, 414–422. [Google Scholar] [CrossRef] [Green Version]
- Sahm, F.; Schrimpf, D.; Stichel, D.; Jones, D.T.W.; Hielscher, T.; Schefzyk, S.; Okonechnikov, K.; Koelsche, C.; E Reuss, D.; Capper, D.; et al. DNA methylation-based classification and grading system for meningioma: A multicentre, retrospective analysis. Lancet Oncol. 2017, 18, 682–694. [Google Scholar] [CrossRef] [Green Version]
- Bi, W.L.; Abedalthagafi, M.; Horowitz, P.; Agarwalla, P.K.; Mei, Y.; Aizer, A.A.; Brewster, R.; Dunn, G.P.; Al-Mefty, O.; Alexander, B.M.; et al. Genomic landscape of intracranial meningiomas. J. Neurosurg. 2016, 125, 525–535. [Google Scholar] [CrossRef] [Green Version]
- Negroni, C.; Hilton, D.A.; Ercolano, E.; Adams, C.L.; Kurian, K.M.; Baiz, D.; Hanemann, C. GATA-4, a potential novel therapeutic target for high-grade meningioma, regulates miR-497, a potential novel circulating biomarker for high-grade meningioma. EBioMedicine 2020, 59, 102941. [Google Scholar] [CrossRef] [PubMed]
- El-Gewely, M.R.; Andreassen, M.; Walquist, M.; Ursvik, A.; Knutsen, E.; Nystad, M.; Coucheron, D.H.; Myrmel, K.S.; Hennig, R.; Johansen, S.D. Differentially Expressed MicroRNAs in Meningiomas Grades I and II Suggest Shared Biomarkers with Malignant Tumors. Cancers 2016, 8, 31. [Google Scholar] [CrossRef] [PubMed]
- Zhi, F.; Shao, N.; Li, B.; Xue, L.; Deng, D.; Xu, Y.; Lan, Q.; Peng, Y.; Yang, Y. A serum 6-miRNA panel as a novel non-invasive biomarker for meningioma. Sci. Rep. 2016, 6, 32067. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arteaga, C.L.; Engelman, J.A. ERBB Receptors: From Oncogene Discovery to Basic Science to Mechanism-Based Cancer Therapeutics. Cancer Cell 2014, 25, 282–303. [Google Scholar] [CrossRef] [Green Version]
- de Bono, J.S.; Rowinsky, E.K. The ErbB receptor family: A therapeutic target for cancer. Trends Mol. Med. 2002, 8, S19–S26. [Google Scholar] [CrossRef]
- Mishra, R.; Hanker, A.; Garrett, J.T. Genomic alterations of ERBB receptors in cancer: Clinical implications. Oncotarget 2017, 8, 114371–114392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dahabreh, I.J.; Linardou, H.; Siannis, F.; Kosmidis, P.; Bafaloukos, D.; Murray, S. Somatic EGFR Mutation and Gene Copy Gain as Predictive Biomarkers for Response to Tyrosine Kinase Inhibitors in Non-Small Cell Lung Cancer. Clin. Cancer Res. 2009, 16, 291–303. [Google Scholar] [CrossRef] [Green Version]
- Brennan, C.W.; Verhaak, R.G.; McKenna, A.; Campos, B.; Noushmehr, H.; Salama, S.; Zheng, S.; Chakravarty, D.; Sanborn, J.Z.; Berman, S.H.; et al. The Somatic Genomic Landscape of Glioblastoma. Cell 2013, 155, 462–477. [Google Scholar] [CrossRef]
- Shinojima, N.; Tada, K.; Shiraishi, S.; Kamiryo, T.; Kochi, M.; Nakamura, H.; Makino, K.; Saya, H.; Hirano, H.; Kuratsu, J.-I.; et al. Prognostic value of epidermal growth factor receptor in patients with glioblastoma multiforme. Cancer Res. 2003, 63, 6962–6970. [Google Scholar]
- Saadeh, F.S.; Mahfouz, R.; Assi, H.I. EGFR as a clinical marker in glioblastomas and other gliomas. Int. J. Biol. Markers 2017, 33, 22–32. [Google Scholar] [CrossRef] [Green Version]
- Arnli, M.B.; Backer-Grøndahl, T.; Ytterhus, B.; Granli, U.S.; Lydersen, S.; Gulati, S.; Torp, S.H. Expression and clinical value of EGFR in human meningiomas. PeerJ 2017, 5, e3140. [Google Scholar] [CrossRef] [Green Version]
- Wernicke, A.G.; Dicker, A.P.; Whiton, M.; Ivanidze, J.; Hyslop, T.; Hammond, E.H.; Perry, A.; Andrews, D.W.; Kenyon, L. Assessment of Epidermal Growth Factor Receptor (EGFR) expression in human meningioma. Radiat. Oncol. 2010, 5, 46. [Google Scholar] [CrossRef] [Green Version]
- Everson, R.G.; Hashimoto, Y.; Freeman, J.L.; Hodges, T.R.; Huse, J.; Zhou, S.; Xiu, J.; Spetzler, D.; Sanai, N.; Kim, L.; et al. Multiplatform profiling of meningioma provides molecular insight and prioritization of drug targets for rational clinical trial design. J. Neuro-Oncol. 2018, 139, 469–478. [Google Scholar] [CrossRef]
- Lusis, E.A.; Chicoine, M.R.; Perry, A. High throughput screening of meningioma biomarkers using a tissue microarray. J. Neuro-Oncol. 2005, 73, 219–223. [Google Scholar] [CrossRef]
- Maxwell, M.; Galanopoulos, T.; Antoniades, H. Coexpression of EGF receptor and TGF alpha mRNA and protein occurs in primary meningiomas. Int. J. Oncol. 1996, 9. [Google Scholar] [CrossRef] [PubMed]
- Johnson, M.D.; Horiba, M.; Winnier, A.R.; Arteaga, C.L. The epidermal growth factor receptor is associated with phospholipase C-γ1 in meningiomas. Hum. Pathol. 1994, 25, 146–153. [Google Scholar] [CrossRef]
- Caltabiano, R.; Barbagallo, G.M.V.; Castaing, M.; Cassenti, A.; Senetta, R.; Cassoni, P.; Albanese, V.; Lanzafame, S. Prognostic value of EGFR expression in de novo and progressed atypical and anaplastic meningiomas: An immunohistochemical and fluorescence in situ hybridization pilot study. J. Neurosurg. Sci. 2013, 57, 139–151. [Google Scholar]
- Arnli, M.B.; Meta, R.; Lydersen, S.; Torp, S.H. HER3 and HER4 are highly expressed in human meningiomas. Pathol. Res. Pr. 2019, 215, 152551. [Google Scholar] [CrossRef] [PubMed]
- Mahzouni, P.; Movahedipour, M. An immunohistochemical study of HER2 expression in meningioma and its correlation with tumor grade. Pathol. Res. Pr. 2012, 208, 221–224. [Google Scholar] [CrossRef]
- Andersson, U.; Guo, D.; Malmer, B.; Bergenheim, A.T.; Henriksson, R. Epidermal growth factor receptor family (EGFR, ErbB2?4) in gliomas and meningiomas. Acta Neuropathol. 2004, 108, 135–142. [Google Scholar] [CrossRef]
- Loussouarn, D.; Brunon, J.; Avet-Loiseau, H.; Campone, M.; Mosnier, J.-F. Prognostic value of HER2 expression in meningiomas: An immunohistochemical and fluorescence in situ hybridization study. Hum. Pathol. 2006, 37, 415–421. [Google Scholar] [CrossRef] [PubMed]
- Arnli, M.B.; Winther, T.L.; Lydersen, S.; Torp, S.H. Prognostic value of ErbB2/HER2 in human meningiomas. PLoS ONE 2018, 13, e0205846. [Google Scholar] [CrossRef]
- Vasudevan, H.N.; Braunstein, S.E.; Phillips, J.J.; Pekmezci, M.; Tomlin, B.A.; Wu, A.; Reis, G.F.; Magill, S.T.; Zhang, J.; Feng, F.Y.; et al. Comprehensive Molecular Profiling Identifies FOXM1 as a Key Transcription Factor for Meningioma Proliferation. Cell Rep. 2018, 22, 3672–3683. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nakada, S.; Sasagawa, Y.; Tachibana, O.; Iizuka, H.; Kurose, N.; Shioya, A.; Guo, X.; Yamada, S.; Nojima, T. The clinicopathological analysis of receptor tyrosine kinases in meningiomas: The expression of VEGFR-2 in meningioma was associated with a higher WHO grade and shorter progression-free survival. Brain Tumor Pathol. 2018, 36, 7–13. [Google Scholar] [CrossRef] [PubMed]
- Saini, M.; Jha, A.N.; Abrari, A.; Ali, S. Expression of proto-oncogene KIT is up-regulated in subset of human meningiomas. BMC Cancer 2012, 12, 212. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martínez-Rumayor, A.; Arrieta, O.; Guevara, P.; Escobar, E.; Rembao, D.; Salina, C.; Sotelo, J. Coexpression of hepatocyte growth factor/scatter factor (HGF/SF) and its receptor cMET predict recurrence of meningiomas. Cancer Lett. 2004, 213, 117–124. [Google Scholar] [CrossRef] [PubMed]
- Barker, P.E. Cancer Biomarker Validation: Standards and Process. Ann. N. Y. Acad. Sci. 2003, 983, 142–150. [Google Scholar] [CrossRef]
- Sun, X.; Li, S.; Shen, B. Identification of Disease States and Response to Therapy in Humans by Utilizing the Biomarker EGFR for Targeted Molecular Imaging. Curr. Protein Pept. Sci. 2016, 17, 534–542. [Google Scholar] [CrossRef]
- Jelski, W.; Mroczko, B. Molecular and Circulating Biomarkers of Brain Tumors. Int. J. Mol. Sci. 2021, 22, 7039. [Google Scholar] [CrossRef]
Experimental Model | Main Findings | References |
---|---|---|
MGM tumor specimens and primary cell culture | High levels of pEGFR are found in both MGM tumor lysates and MGM cells. Signaling by EGFR mediates aberrant STAT1 activation, and EGFR inhibition impairs cell proliferation and reduces the levels of cyclin D1, phosphorylated AKT, and phosphorylated extracellular signal-regulated kinase (ERK)1/2 | [24] |
Cultured IOMM-Lee MGM cells | RTK inhibitors sorafenib and regorafenib impair PDGF receptor (PDGFR)-mediated signaling and inhibit MGM cell proliferation through PDGFR downregulation and inhibition of p44/42 ERK | [25] |
Orthotropic xenograft model in mice that received bilateral infusions of IOMM-Lee MGM cells into the subarachnoidal space | Treatment for 5 days a week with regorafenib inhibits intracranial MGM cell growth and cell growth and increases survival time of treated mice. In contrast, the group treated with sorafenib showed no statistically significant benefit in survival compared to controls | [25] |
Thirty-six patients with either histologically proven MGM, hemangiopericytoma, hemangioblastoma, or radiographic features of a surgically inaccessible MGM, and recurrence despite radiotherapy | Treatment with sunitinib 50 mg daily for days 1–28 of 42 (one cycle), until disease progression or intolerable toxicity, resulted in 42% of patients being alive and progression-free at 6 months. Considerable toxicity was observed | [25] |
Thirty-nine-year-old woman who had undergone surgeries and courses of radiotherapy over 11 years for recurrent cranial and spinal MGM. | Treatment with sunitinib resulted in a radiographic response with marked reduction in tumor volume and reduction in brainstem vasogenic edema | [27] |
Patients with recurrent MGM tumors refractory to surgery and radiation | Treatment with the multi-RTK inhibitor PTK787/ZK 222584 (PTK787) led to a progression-free survival at 6 months of 64.3%, a median progression-free survival of 6.5 months, and an overall survival of 26.0 months in patients with grade II MGM, and a progression-free survival at 6 months of 37.5%, median progression-free survival of 3.6 months, and overall survival of 23 months in patients with grade III MGM | [28] |
Eighteen patients with recurrent MGM | A retrospective analysis of 9 patients with PDGFR-positive MGM tumors treated with imatinib showed that 7 patients had stable disease and 2 patients had progressed at the first scan after three months. No complete or partial responses were observed. Median progression-free survival was 16 months | [29] |
Experimental Model | Main Findings | References |
---|---|---|
MGM specimens and primary cell cultures obtained from 36 tumors | High levels of pEGFR expression across tumor samples and cultured cells | [24] |
Set of 186 archived primary MGM tumors | Tissue microarrays obtained from the set of tumors and analyzed by immunohistochemistry show EGFR overexpression and activation Reduced survival and recurrence in association with high staining of the EGFR extracellular domain | [72] |
Set of 113 MGM specimens from 89 patients | Benign and atypical MGM tumors show intermediate to marked staining percentage score for EGFR expression, whereas all the malignant MGM samples show low staining percentage score | [73] |
Set of 115 MGM tumor specimens | Tumor investigation with next-generation sequencing, immunohistochemistry, and fluorescent and chromogenic in situ hybridization shows EGFR expression in 93% of samples | [74] |
Tissue microarray from set of 41 MGMs of various grades and two subsets of atypical MGMs | Analysis by high throughput TMA-IHC show differential EGFR expression in symptomatic, surgically resected MGMs versus incidental MGMs, whereas PDGFRβ helps distinguish anaplastic MGMs from hemangiopericytomas | [75] |
Set of 115 primary MGM tumors | Analysis with Northern blot shows EGFR mRNA expression in 9 (82%) tumors Expression at the EGFR protein level is confirmed by immunocytochemistry | [74] |
Set of 19 MGM tumors | EGFR expression detected by immunoblot in 6 of 9 MGM tumors (67%) Immunohistochemical analysis show EGFR in 13 of 19 (68%) tumors | [77] |
Set of malignant MGM tumors that progressed or not from lower grade tumors | Immunohistochemical analysis and gene amplification by FISH show that an increased EGFR expression is associated with progression from benign to atypical or anaplastic MGM tumors EGFR expression is not associated with overall survival or recurrence-free survival | [78] |
Set of 186 primary MGM tumors | High expressions of HER3 and HER4 in most tumor samples of all grades, both in the cytoplasm and cell membrane, and also in the nucleus for HER4. Absence of immunoreaction in non-neoplastic meningeal tissue | [79] |
Set of 72 MGM tumor samples | Immunohistochemical analysis shows HER2 expression in 45% of samples, being 55% grade II/III, and 38.5% of grade I No differences between grade I and grade II/III MGMs, primary and recurrent tumors, or males and females | [80] |
Set of 26 MGM tumor samples | The mRNA expressions of EGFR, HER2, and HER4, and high protein content of HER2 in most tumors | [81] |
Set of 35 MGM tumor samples | HER2 overexpression in 5 atypical/anaplastic MGMs and 5 classic MGMs; Increased HER2 gene copy number in 4 of 10 HER2-positive MGMs; Increased tumor recurrence in patients with MGMs showing HER2 overexpression | [82] |
Set of of 186 MGM tumor samples of different grades | The content of activated HER2 receptors significantly correlated with increased risk for recurrence or death | [83] |
Data sets derived from 42 aggressive MGM tumors | Higher levels of expressions of ErbB2 (HER2) and ErbB3 (HER3) compared to all other members of the ErbB receptor family High levels of expressions of TGFA, AREG, EPGN, and NRG3 in a subset of patients High levels of expressions of HB-EGF and NRG4 in a higher density of MGM patients | Present paper based on data from [84] |
Set of 81 MGM tumors from 74 patients | Immunohistochemical analysis reveals 29 grade I (45%), 10 grade II (77%), and 4 grade III (100%) tumors positive for VEGFR2 Expression of VEGFR2 significantly correlates with tumor grade | [85] |
Thirty-four tumor specimens collected from 34 patients | High expression of KIT in 20.6% of MGMs, likely through upregulation of KIT transcription | [86] |
Seventeen recurrent and 25 non-recurrent MGM tumors | Significant association of coexpression of cMET and HGF/SF with cell proliferation and recurrence | [87] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Roesler, R.; Souza, B.K.; Isolan, G.R. Receptor Tyrosine Kinases as Candidate Prognostic Biomarkers and Therapeutic Targets in Meningioma. Int. J. Mol. Sci. 2021, 22, 11352. https://doi.org/10.3390/ijms222111352
Roesler R, Souza BK, Isolan GR. Receptor Tyrosine Kinases as Candidate Prognostic Biomarkers and Therapeutic Targets in Meningioma. International Journal of Molecular Sciences. 2021; 22(21):11352. https://doi.org/10.3390/ijms222111352
Chicago/Turabian StyleRoesler, Rafael, Barbara Kunzler Souza, and Gustavo R. Isolan. 2021. "Receptor Tyrosine Kinases as Candidate Prognostic Biomarkers and Therapeutic Targets in Meningioma" International Journal of Molecular Sciences 22, no. 21: 11352. https://doi.org/10.3390/ijms222111352