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      Glutaminases as a Novel Target for SDHB-Associated Pheochromocytomas/Paragangliomas

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          Abstract

          Pheochromocytoma/paragangliomas (Pheo/PGL) are rare endocrine cancers with strong genetic background. Mutations in the SDHB subunit of succinate dehydrogenase (SDH) predispose patients to malignant disease with limited therapeutic options and poor prognosis. Using a host of cellular and molecular biology techniques in 2D and 3D cell culture formats we show that SDH inhibition had cell line specific biological and biochemical consequences. Based on our studies performed on PC12 (rat chromaffin cell line), Hela (human cervix epithelial cell line), and H295R (human adrenocortical cell line) cells, we demonstrated that chromaffin cells were not affected negatively by the inhibition of SDH either by siRNA directed against SDHB or treatment with SDH inhibitors (itaconate and atpenin A5). Cell viability and intracellular metabolite measurements pointed to the cell line specific consequences of SDH impairment and to the importance of glutamate metabolism in chromaffin cells. A significant increase in glutaminase-1 (GLS-1) expression after SDH impairment was observed in PC12 cells. GLS-1 inhibitor BPTES was capable of significantly decreasing proliferation of SDH impaired PC12 cells. Glutaminase-1 and SDHB expressions were tested in 35 Pheo/PGL tumor tissues. Expression of GLS1 was higher in the SDHB low expressed group compared to SDHB high expressed tumors. Our data suggest that the SDH-associated malignant potential of Pheo/PGL is strongly dependent on GLS-1 expression and glutaminases may be novel targets for therapy.

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          Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of α-ketoglutarate to citrate to support cell growth and viability.

          Citrate is a critical metabolite required to support both mitochondrial bioenergetics and cytosolic macromolecular synthesis. When cells proliferate under normoxic conditions, glucose provides the acetyl-CoA that condenses with oxaloacetate to support citrate production. Tricarboxylic acid (TCA) cycle anaplerosis is maintained primarily by glutamine. Here we report that some hypoxic cells are able to maintain cell proliferation despite a profound reduction in glucose-dependent citrate production. In these hypoxic cells, glutamine becomes a major source of citrate. Glutamine-derived α-ketoglutarate is reductively carboxylated by the NADPH-linked mitochondrial isocitrate dehydrogenase (IDH2) to form isocitrate, which can then be isomerized to citrate. The increased IDH2-dependent carboxylation of glutamine-derived α-ketoglutarate in hypoxia is associated with a concomitant increased synthesis of 2-hydroxyglutarate (2HG) in cells with wild-type IDH1 and IDH2. When either starved of glutamine or rendered IDH2-deficient by RNAi, hypoxic cells are unable to proliferate. The reductive carboxylation of glutamine is part of the metabolic reprogramming associated with hypoxia-inducible factor 1 (HIF1), as constitutive activation of HIF1 recapitulates the preferential reductive metabolism of glutamine-derived α-ketoglutarate even in normoxic conditions. These data support a role for glutamine carboxylation in maintaining citrate synthesis and cell growth under hypoxic conditions.
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            Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma.

            Hereditary paraganglioma (PGL) is characterized by the development of benign, vascularized tumors in the head and neck. The most common tumor site is the carotid body (CB), a chemoreceptive organ that senses oxygen levels in the blood. Analysis of families carrying the PGL1 gene, described here, revealed germ line mutations in the SDHD gene on chromosome 11q23. SDHD encodes a mitochondrial respiratory chain protein-the small subunit of cytochrome b in succinate-ubiquinone oxidoreductase (cybS). In contrast to expectations based on the inheritance pattern of PGL, the SDHD gene showed no evidence of imprinting. These findings indicate that mitochondria play an important role in the pathogenesis of certain tumors and that cybS plays a role in normal CB physiology.
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              Targeting mitochondrial glutaminase activity inhibits oncogenic transformation.

              Rho GTPases impact a number of activities important for oncogenesis. We describe a small molecule inhibitor that blocks oncogenic transformation induced by various Rho GTPases in fibroblasts, and the growth of human breast cancer and B lymphoma cells, without affecting normal cells. We identify the target of this inhibitor to be the metabolic enzyme glutaminase, which catalyzes the hydrolysis of glutamine to glutamate. We show that transformed fibroblasts and breast cancer cells exhibit elevated glutaminase activity that is dependent on Rho GTPases and NF-κB activity, and is blocked by the small molecule inhibitor. These findings highlight a previously unappreciated connection between Rho GTPase activation and cellular metabolism and demonstrate that targeting glutaminase activity can inhibit oncogenic transformation. Copyright © 2010 Elsevier Inc. All rights reserved.
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                Author and article information

                Journal
                Cancers (Basel)
                Cancers (Basel)
                cancers
                Cancers
                MDPI
                2072-6694
                05 March 2020
                March 2020
                : 12
                : 3
                : 599
                Affiliations
                [1 ]2nd Department of Internal Medicine, Semmelweis University, 1088 Budapest, Hungary; sarkadi.balazs2@ 123456med.semmelweis-univ.hu (B.S.); sarazakarias@ 123456gmail.com (S.Z.); igaz.peter@ 123456med.semmelweis-univ.hu (P.I.)
                [2 ]Hereditary Tumours Research Group, Hungarian Academy of Sciences and Semmelweis University, 1085 Budapest, Hungary; kati.balla@ 123456gmail.com (K.M.); krokker.lilla@ 123456gmail.com (L.K.); butz.henriett@ 123456med.semmelweis-univ.hu (H.B.); otto.darvasi@ 123456gmail.com (O.D.)
                [3 ]Department of Laboratory Medicine, Semmelweis University, 1089 Budapest, Hungary
                [4 ]Bionics Innovation Center, 1088 Budapest, Hungary; sebestyen.anna@ 123456med.semmelweis-univ.hu
                [5 ]1st Department of Pathology and Experimental Cancer, Semmelweis University, 1085 Budapest, Hungary; krencz.ildiko@ 123456med.semmelweis-univ.hu (I.K.); barna.gabor@ 123456med.semmelweis-univ.hu (G.B.); papay.judit@ 123456med.semmelweis-univ.hu (J.P.); zoltan.hujber56@ 123456gmail.com (Z.H.)
                [6 ]Department of Experimental and Clinical Biomedical Sciences “Mario Serio”, University of Florence, 50139 Florence, Italy; letizia.canu@ 123456unifi.it (L.C.); Luconi.michaela.luconi@ 123456unifi.it (M.L.)
                [7 ]Department of Molecular Genetics, National Institute of Oncology, 1122 Budapest, Hungary
                [8 ]Molecular Medicine Research Group, Hungarian Academy of Sciences and Semmelweis University, 1085 Budapest, Hungary
                [9 ]Department of Medical Biochemistry, Semmelweis University, 1094 Budapest, Hungary; doczi.judit@ 123456med.semmelweis-univ.hu (J.D.); chinopoulos.christos@ 123456med.semmelweis-univ.hu (C.C.)
                Author notes
                [* ]Correspondence: patocs.attila@ 123456med.semmelweis-univ.hu ; Tel.: +36-1-266-0926; Fax: +36-1-266-0816
                Author information
                https://orcid.org/0000-0003-4995-8108
                https://orcid.org/0000-0003-2192-554X
                https://orcid.org/0000-0003-0183-4149
                Article
                cancers-12-00599
                10.3390/cancers12030599
                7139890
                32150977
                6f2d8d77-adc6-490b-a3f5-414beaaf542f
                © 2020 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 ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 05 February 2020
                : 01 March 2020
                Categories
                Article

                succinate,sdh,sdhb,pheochromocytoma,paraganglioma,gls-1
                succinate, sdh, sdhb, pheochromocytoma, paraganglioma, gls-1

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