TY - JOUR
T1 - Increased mitochondrial activity in a novel IDH1-R132H mutant human oligodendroglioma xenograft model
T2 - In situ detection of 2-HG and α-KG
AU - Navis, Anna C.
AU - Niclou, Simone P.
AU - Fack, Fred
AU - Stieber, Daniel
AU - van Lith, Sanne
AU - Verrijp, Kiek
AU - Wright, Alan
AU - Stauber, Jonathan
AU - Tops, Bastiaan
AU - Otte-Holler, Irene
AU - Wevers, Ron A.
AU - van Rooij, Arno
AU - Pusch, Stefan
AU - von Deimling, Andreas
AU - Tigchelaar, Wikky
AU - van Noorden, Cornelis J.F.
AU - Wesseling, Pieter
AU - Leenders, William P.J.
N1 - Funding Information:
This work was supported by a grant from the Hersenstichting (grant 2010(1)-01) and by the CORE grant ESCAPE (C10/BM/784322) from the FNR in Luxembourg. ACN was supported by a RUNMC grant. We thank Jeroen Mooren for excellent technical assistance with xenograft transplantations and Nathalie Nicot from the Genomics Research Unit of CRP-Santé for expert technical assistance in genomics analysis.
Publisher Copyright:
© 2013 Navis et al.; licensee BioMed Central Ltd.
PY - 2014/1/27
Y1 - 2014/1/27
N2 - Background: Point mutations in genes encoding NADP+-dependent isocitrate dehydrogenases (especially IDH1) are common in lower grade diffuse gliomas and secondary glioblastomas and occur early during tumor development. The contribution of these mutations to gliomagenesis is not completely understood and research is hampered by the lack of relevant tumor models. We previously described the development of the patient-derived high-grade oligodendroglioma xenograft model E478 that carries the commonly occurring IDH1-R132H mutation. We here report on the analyses of E478 xenografts at the genetic, histologic and metabolic level. Results: LC-MS and in situ mass spectrometric imaging by LESA-nano ESI-FTICR revealed high levels of the proposed oncometabolite D-2-hydroxyglutarate (D-2HG), the product of enzymatic conversion of α-ketoglutarate (α-KG) by IDH1-R132H, in the tumor but not in surrounding brain parenchyma. α-KG levels and total NADP+-dependent IDH activity were similar in IDH1-mutant and -wildtype xenografts, demonstrating that IDH1-mutated cancer cells maintain α-KG levels. Interestingly, IDH1-mutant tumor cells in vivo present with high densities of mitochondria and increased levels of mitochondrial activity as compared to IDH1-wildtype xenografts. It is not yet clear whether this altered mitochondrial activity is a driver or a consequence of tumorigenesis. Conclusions: The oligodendroglioma model presented here is a valuable model for further functional elucidation of the effects of IDH1 mutations on tumor metabolism and may aid in the rational development of novel therapeutic strategies for the large subgroup of gliomas carrying IDH1 mutations.
AB - Background: Point mutations in genes encoding NADP+-dependent isocitrate dehydrogenases (especially IDH1) are common in lower grade diffuse gliomas and secondary glioblastomas and occur early during tumor development. The contribution of these mutations to gliomagenesis is not completely understood and research is hampered by the lack of relevant tumor models. We previously described the development of the patient-derived high-grade oligodendroglioma xenograft model E478 that carries the commonly occurring IDH1-R132H mutation. We here report on the analyses of E478 xenografts at the genetic, histologic and metabolic level. Results: LC-MS and in situ mass spectrometric imaging by LESA-nano ESI-FTICR revealed high levels of the proposed oncometabolite D-2-hydroxyglutarate (D-2HG), the product of enzymatic conversion of α-ketoglutarate (α-KG) by IDH1-R132H, in the tumor but not in surrounding brain parenchyma. α-KG levels and total NADP+-dependent IDH activity were similar in IDH1-mutant and -wildtype xenografts, demonstrating that IDH1-mutated cancer cells maintain α-KG levels. Interestingly, IDH1-mutant tumor cells in vivo present with high densities of mitochondria and increased levels of mitochondrial activity as compared to IDH1-wildtype xenografts. It is not yet clear whether this altered mitochondrial activity is a driver or a consequence of tumorigenesis. Conclusions: The oligodendroglioma model presented here is a valuable model for further functional elucidation of the effects of IDH1 mutations on tumor metabolism and may aid in the rational development of novel therapeutic strategies for the large subgroup of gliomas carrying IDH1 mutations.
KW - D-2-hydroxyglutarate
KW - Glioma
KW - IDH mutations
KW - Mitochondria: LESA-nano ESI-FTICR
KW - Xenograft
KW - α-ketoglutarate
UR - https://www.scopus.com/pages/publications/85005848045
U2 - 10.1186/2051-5960-1-18
DO - 10.1186/2051-5960-1-18
M3 - Article
C2 - 24252742
AN - SCOPUS:85005848045
SN - 2051-5960
VL - 2
JO - Acta Neuropathologica Communications
JF - Acta Neuropathologica Communications
IS - 1
M1 - 18
ER -