Implications of Concurrent IDH1 and IDH2 Mutations on Survival in Glioma—A Case Report and Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Genomic Database Interrogation
2.2. Data Sources and Search Strategy
- Pubmed (from 1966)
- Ovid MEDLINE (from 1950)
- Ovid Embase (from 1974)
2.3. Selection Criteria and Process
2.4. Data Extraction
3. Results
3.1. Case Presentation
3.2. Genomic Database Interrogation Did Not Yield a Co-occurring IDH1 and IDH2 Mutation in Glioma Datasets
3.3. Systematic Review of the Literature Shows Rare Co-occurring IDH1 and IDH2 SNVs in Cancer
3.3.1. Acute Myeloid Leukaemia
3.3.2. Chondrosarcoma
3.3.3. Glioma
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- 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]
- Parker, S.J.; Metallo, C.M. Metabolic consequences of oncogenic IDH mutations. Pharmacol. Ther. 2015, 152, 54–62. [Google Scholar] [CrossRef] [Green Version]
- Yan, H.; Parsons, D.W.; Jin, G.; McLendon, R.; Rasheed, B.A.; Yuan, W.; Kos, I.; Batinic-Haberle, I.; Jones, S.; Riggins, G.J.; et al. IDH1 and IDH2 Mutations in Gliomas. N. Engl. J. Med. 2009, 360, 765–773. [Google Scholar] [CrossRef] [PubMed]
- Brat, D.J.; Aldape, K.; Bridge, J.A.; Canoll, P.; Colman, H.; Hameed, M.R.; Harris, B.T.; Hattab, E.M.; Huse, J.T.; Jenkins, R.B.; et al. Molecular Biomarker Testing for the Diagnosis of Diffuse Gliomas. Arch. Pathol. Lab. Med. 2022, 146, 547–574. [Google Scholar] [CrossRef] [PubMed]
- Eckel-Passow, J.E.; Lachance, D.H.; Molinaro, A.M.; Walsh, K.M.; Decker, P.A.; Sicotte, H.; Pekmezci, M.; Rice, T.; Kosel, M.L.; Smirnov, I.V.; et al. Glioma Groups Based on 1p/19q, IDH, and TERT Promoter Mutations in Tumors. N. Engl. J. Med. 2015, 372, 2499–2508. [Google Scholar] [CrossRef] [Green Version]
- Parsons, D.W.; Jones, S.; Zhang, X.; Lin, J.C.-H.; Leary, R.J.; Angenendt, P.; Mankoo, P.; Carter, H.; Siu, I.-M.; Gallia, G.L.; et al. An Integrated Genomic Analysis of Human Glioblastoma Multiforme. Science 2008, 321, 1807–1812. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cancer Genome Atlas Research Network. Comprehensive, Integrative Genomic Analysis of Diffuse Lower-Grade Gliomas. N. Engl. J. Med. 2015, 372, 2481–2498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mondesir, J.; Willekens, C.; Touat, M.; de Botton, S. IDH1 and IDH2 mutations as novel therapeutic targets: Current perspectives. J. Blood Med. 2016, 7, 171–180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, K.; Ouyang, L.; He, M.; Luo, M.; Cai, W.; Tu, Y.; Pi, R.; Liu, A. IDH1 R132H mutation regulates glioma chemosensitivity through Nrf2 pathway. Oncotarget 2017, 8, 28865–28879. [Google Scholar] [CrossRef] [Green Version]
- Tesileanu, C.M.S.; Vallentgoed, W.R.; Sanson, M.; Taal, W.; Clement, P.M.; Wick, W.; Brandes, A.A.; Baurain, J.F.; Chinot, O.L.; Wheeler, H.; et al. Non-IDH1-R132H IDH1/2 mutations are associated with increased DNA methylation and improved survival in astrocytomas, compared to IDH1-R132H mutations. Acta Neuropathol. 2021, 141, 945–957. [Google Scholar] [CrossRef]
- Zhao, S.; Lin, Y.; Xu, W.; Jiang, W.; Zha, Z.; Wang, P.; Yu, W.; Li, Z.; Gong, L.; Peng, Y.; et al. Glioma-Derived Mutations in IDH1 Dominantly Inhibit IDH1 Catalytic Activity and Induce HIF-1α. Science 2009, 324, 261–265. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Clark, O.; Yen, K.; Mellinghoff, I.K. Molecular Pathways: Isocitrate Dehydrogenase Mutations in Cancer. Clin. Cancer Res. 2016, 22, 1837–1842. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Avellaneda Matteo, D.; Grunseth, A.J.; Gonzalez, E.R.; Anselmo, S.L.; Kennedy, M.A.; Moman, P.; Scott, D.A.; Hoang, A.; Sohl, C.D. Molecular mechanisms of isocitrate dehydrogenase 1 (IDH1) mutations identified in tumors: The role of size and hydrophobicity at residue 132 on catalytic efficiency. J. Biol. Chem. 2017, 292, 7971–7983. [Google Scholar] [CrossRef] [Green Version]
- Dang, L.; White, D.W.; Gross, S.; Bennett, B.D.; Bittinger, M.A.; Driggers, E.M.; Fantin, V.R.; Jang, H.G.; Jin, S.; Keenan, M.C.; et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2009, 462, 739–744. [Google Scholar] [CrossRef] [Green Version]
- Xu, W.; Yang, H.; Liu, Y.; Yang, Y.; Wang, P.; Kim, S.-H.; Ito, S.; Yang, C.; Wang, P.; Xiao, M.-T.; et al. Oncometabolite 2-Hydroxyglutarate Is a Competitive Inhibitor of α-Ketoglutarate-Dependent Dioxygenases. Cancer Cell 2011, 19, 17–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rakheja, D.; Medeiros, L.J.; Bevan, S.; Chen, W. The Emerging Role of D-2-Hydroxyglutarate as an Oncometabolite in Hematolymphoid and Central Nervous System Neoplasms. Front. Oncol. 2013, 3, 169. [Google Scholar] [CrossRef] [Green Version]
- Reiter-Brennan, C.; Semmler, L.; Klein, A. The effects of 2-hydroxyglutarate on the tumorigenesis of gliomas. Contemp. Oncol. 2018, 22, 215–222. [Google Scholar] [CrossRef]
- Yalaza, C.; Ak, H.; Cagli, M.S.; Ozgiray, E.; Atay, S.; Aydin, H.H. R132H Mutation in IDH1 Gene is Associated with Increased Tumor HIF1-Alpha and Serum VEGF Levels in Primary Glioblastoma Multiforme. Ann. Clin. Lab. Sci. 2017, 47, 362–364. [Google Scholar]
- Cohen, A.L.; Holmen, S.L.; Colman, H. IDH1 and IDH2 Mutations in Gliomas. Curr. Neurol. Neurosci. Rep. 2013, 13, 345. [Google Scholar] [CrossRef] [Green Version]
- Page, M.J.; Moher, D.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. PRISMA 2020 explanation and elaboration: Updated guidance and exemplars for reporting systematic reviews. BMJ 2021, 372, n160. [Google Scholar] [CrossRef]
- Cerami, E.; Gao, J.; Dogrusoz, U.; Gross, B.E.; Sumer, S.O.; Aksoy, B.A.; Jacobsen, A.; Byrne, C.J.; Heuer, M.L.; Larsson, E.; et al. The cBio cancer genomics portal: An open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012, 2, 401–404. [Google Scholar] [CrossRef] [PubMed]
- Platt, M.Y.; Fathi, A.T.; Borger, D.R.; Brunner, A.M.; Hasserjian, R.P.; Balaj, L.; Lum, A.; Yip, S.; Dias-Santagata, D.; Zheng, Z.; et al. Detection of Dual IDH1 and IDH2 Mutations by Targeted Next-Generation Sequencing in Acute Myeloid Leukemia and Myelodysplastic Syndromes. J. Mol. Diagn. 2015, 17, 661–668. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Naya, U.A.; Podder, S.; Ray, R.; Chattopadhyay, A.; Bhatt. Prevalence of IDH mutations in acute myeloid leukemia and its clinicopathological characteristics. Indian J. Hematol. Blood Transfus. 2017, 33 (Suppl. 1), S36–S37. [Google Scholar]
- Petrova, L.; Vrbacky, F.; Lanska, M.; Zavrelova, A.; Zak, P.; Hrochova, K. IDH1 and IDH2 mutations in patients with acute myeloid leukemia: Suitable targets for minimal residual disease monitoring? Clin Biochem. 2018, 61, 34–39. [Google Scholar] [CrossRef] [PubMed]
- Meggendorfer, M.; Cappelli, L.V.; Walter, W.; Haferlach, C.; Kern, W.; Falini, B.; Haferlach, T. IDH1R132, IDH2R140 and IDH2R172 in AML: Different genetic landscapes correlate with outcome and may influence targeted treatment strategies. Leukemia 2018, 32, 1249–1253. [Google Scholar] [CrossRef] [PubMed]
- Lugowska, I.; Teterycz, P.; Mikula, M.; Kulecka, M.; Kluska, A.; Balabas, A.; Piatkowska, M.; Wagrodzki, M.; Pienkowski, A.; Rutkowski, P.; et al. IDH1/2 Mutations Predict Shorter Survival in Chondrosarcoma. J. Cancer 2018, 9, 998–1005. [Google Scholar] [CrossRef] [Green Version]
- Hartmann, C.; Meyer, J.; Balss, J.; Capper, D.; Mueller, W.; Christians, A.; Felsberg, A.; Wolter, M.; Mawrin, C.; Wick, W.; et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: A study of 1010 diffuse gliomas. Acta Neuropathol. 2009, 118, 469–474. [Google Scholar] [CrossRef] [Green Version]
- Louis, D.N.; Perry, A.; Wesseling, P.; Brat, D.J.; Cree, I.A.; Figarella-Branger, D.; Hawkins, C.; Ng, H.K.; Pfister, S.M.; Reifenberger, G.; et al. The 2021 WHO Classification of Tumors of the Central Nervous System: A summary. Neuro Oncol. 2021, 23, 1231–1251. [Google Scholar] [CrossRef]
- Campo, E.; Harris, N.L.; Jaffe, E.S.; Pileri, S.A.; Stein, H.; Thiele, J. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues; Swerdlow, S.H., Ed.; International Agency for Research on Cancer: Lyon, France, 2017; Available online: https://publications.iarc.fr/Book-And-Report-Series/Who-Classification-Of-Tumours/WHO-Classification-Of-Tumours-Of-Haematopoietic-And-Lymphoid-Tissues-2017 (accessed on 30 August 2022).
- Noushmehr, H.; Weisenberger, D.J.; Diefes, K.; Phillips, H.S.; Pujara, K.; Berman, B.P.; Pan, F.; Pelloski, C.E.; Sulman, E.P.; Bhat, K.P.; et al. Identification of a CpG Island Methylator Phenotype that Defines a Distinct Subgroup of Glioma. Cancer Cell 2010, 17, 510–522. [Google Scholar] [CrossRef] [Green Version]
- Wise, D.R.; Ward, P.S.; Shay, J.E.S.; Cross, J.R.; Gruber, J.J.; Sachdeva, U.M.; Platt, J.M.; DeMatteo, R.G.; Simon, M.C.; Thompson, C.B. Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of α-ketoglutarate to citrate to support cell growth and viability. Proc. Natl. Acad. Sci. USA 2011, 108, 19611–19616. [Google Scholar] [CrossRef] [Green Version]
- Pessôa, I.A.; Amorim, C.K.; Ferreira, W.A.S.; Sagica, F.; Brito, J.R.; Othman, M.; Meyer, B.; Liehr, T.; de Oliveira, E.H.C. Detection and Correlation of Single and Concomitant TP53, PTEN, and CDKN2A Alterations in Gliomas. Int. J. Mol. Sci. 2019, 20, 2658. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wick, W.; Meisner, C.; Hentschel, B.; Platten, M.; Schilling, A.; Wiestler, B.; Sabel, M.C.; Koeppen, S.; Ketter, R.; Weiler, M.; et al. Prognostic or predictive value of MGMT promoter methylation in gliomas depends on IDH1 mutation. Neurology 2013, 81, 1515–1522. [Google Scholar] [CrossRef] [PubMed]
- Filipp, F.V.; Scott, D.A.; Ronai, Z.A.; Osterman, A.L.; Smith, J.W. Reverse TCA cycle flux through isocitrate dehydrogenases 1 and 2 is required for lipogenesis in hypoxic melanoma cells. Pigment Cell Melanoma Res. 2012, 25, 375–383. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Metallo, C.M.; Gameiro, P.A.; Bell, E.L.; Mattaini, K.R.; Yang, J.; Hiller, K.; Jewell, C.M.; Johnson, Z.R.; Irvine, D.J.; Guarente, L.; et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 2011, 481, 380–384. [Google Scholar] [CrossRef] [Green Version]
- Mullen, A.R.; Wheaton, W.W.; Jin, E.S.; Chen, P.-H.; Sullivan, L.B.; Cheng, T.; Yang, Y.; Linehan, W.M.; Chandel, N.S.; DeBerardinis, R.J. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 2011, 481, 385–388. [Google Scholar] [CrossRef] [Green Version]
- Grassian, A.R.; Parker, S.J.; Davidson, S.M.; Divakaruni, A.S.; Green, C.R.; Zhang, X.; Slocum, K.L.; Pu, M.; Lin, F.; Vickers, C.; et al. IDH1 mutations alter citric acid cycle metabolism and increase dependence on oxidative mitochondrial metabolism. Cancer Res. 2014, 74, 3317–3331. [Google Scholar] [CrossRef] [Green Version]
- Gupta, R.; Flanagan, S.; Li, C.C.; Lee, M.; Shivalingham, B.; Maleki, S.; Wheeler, H.R.; Buckland, M.E. Expanding the spectrum of IDH1 mutations in gliomas. Mod. Pathol. 2013, 26, 619–625. [Google Scholar] [CrossRef]
Study | Malignancy Type | Proportion with IDH1/2 Co-Mutation | Method of Genomic Testing | Associated Mutations | Clinical Outcomes |
---|---|---|---|---|---|
Meggendorfer et al. [28] | AML | 7/1394 (0.5%) | NGS | Not reported | Not reported |
Platt et al. [27] | AML | 3/53 (5.7%) | NGS | FLT3 | 1 patient remains alive and well 24 months post allogeneic transplant, 1 patient surviving for 14 months post diagnosis and 1 patient surviving three months post diagnosis |
CEBPA | |||||
NPM1 | |||||
Petrova et al. [29] | AML | 1/90 (1.1%) | NGS | Not reported | Not reported |
Nayak et al. [26] | AML | 1/33 (3.0%) | Sanger | Not reported | Not reported |
sequencing | |||||
Lugowska et al. [30] | CS | 3/80 (3.8%) | NGS | Not reported | Not reported |
Hartman et al. [31] | A | 1/228 (0.4%) | NGS | Not reported | Not reported |
O | 1/174 (0.6%) | ||||
OA | 2/177 (1.1%) |
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Yuile, A.; Satgunaseelan, L.; Wei, J.; Kastelan, M.; Back, M.F.; Lee, M.; Wei, H.; Buckland, M.E.; Lee, A.; Wheeler, H.R. Implications of Concurrent IDH1 and IDH2 Mutations on Survival in Glioma—A Case Report and Systematic Review. Curr. Issues Mol. Biol. 2022, 44, 5117-5125. https://doi.org/10.3390/cimb44100348
Yuile A, Satgunaseelan L, Wei J, Kastelan M, Back MF, Lee M, Wei H, Buckland ME, Lee A, Wheeler HR. Implications of Concurrent IDH1 and IDH2 Mutations on Survival in Glioma—A Case Report and Systematic Review. Current Issues in Molecular Biology. 2022; 44(10):5117-5125. https://doi.org/10.3390/cimb44100348
Chicago/Turabian StyleYuile, Alexander, Laveniya Satgunaseelan, Joe Wei, Marina Kastelan, Michael F. Back, Maggie Lee, Heng Wei, Michael E. Buckland, Adrian Lee, and Helen R. Wheeler. 2022. "Implications of Concurrent IDH1 and IDH2 Mutations on Survival in Glioma—A Case Report and Systematic Review" Current Issues in Molecular Biology 44, no. 10: 5117-5125. https://doi.org/10.3390/cimb44100348