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1. Author Correction: Nuclear Translocation of Glutaminase GLS2 in Human Cancer Cells Associates with Proliferation Arrest and Differentiation

Author

Amada R. López de la Oliva, José A. Campos-Sandoval, María C. Gómez-García, Carolina Cardona, Mercedes Martín-Rufián, Fernando J. Sialana, Laura Castilla, Narkhyun Bae, Carolina Lobo, Ana Peñalver, Marina García-Frutos, David Carro, Victoria Enrique, José C. Paz, Raghavendra G. Mirmira, Antonia Gutiérrez, Francisco J. Alonso, Juan A. Segura, José M. Matés, Gert Lubec, and Javier Márquez

Subjects
Medicine, Science
Abstract

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Published
2021
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2. Nuclear Translocation of Glutaminase GLS2 in Human Cancer Cells Associates with Proliferation Arrest and Differentiation

Author

María C. Gómez-García, David Carro, Carolina Lobo, Francisco J. Alonso, Narkhyun Bae, José A. Campos-Sandoval, Raghavendra G. Mirmira, Laura Castilla, Carolina Cardona, José C. Paz, Antonia Gutierrez, Gert Lubec, Ana Peñalver, José M. Matés, Amada R. López de la Oliva, Juan A. Segura, Victoria Enrique, Mercedes Martín-Rufián, Marina García-Frutos, Javier Márquez, Fernando J. Sialana, [López de la Oliva,AR, Gómez-García,MC, Cardona,C, Castilla,L, Peñalver,A, García-Frutos,M, Carro,D, Enrique,V, Paz,JC, Alonso,FJ, Segura,JA, Matés,JM, Márquez,J] Departamento de Biología Molecular y Bioquímica, Canceromics Lab, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain and Instituto de Investigación Biomédica de Málaga (IBIMA), Málaga, Spain. [Campos-Sandoval,JA, Martín-Rufián,M, Lobo,C] Proteomics Lab, Central Facility Core, University of Málaga, Málaga, Spain. [Sialana,FJ, Lubec,G] Private Medical University of Salzburg, Salzburg, Austria. [Bae,N] Institute of Science and Technology Austria, Klosterneuburg, Austria. [Mirmira,RG] Department of Pediatrics, Indiana University School of Medicine, Indianapolis, USA. [Gutiérrez,A] Departamento de Biología Celular, Genética y Fisiología, Facultad de Ciencias, Universidad de Málaga, Instituto de Investigación Biomédica de Málaga (IBIMA). Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Málaga, Spain., and This research was financed by Grant SAF2015-64501-R from the Spanish Ministry of Economy, Industry and Competitivity (to JM and JMM).

Subjects
Proteomics, Anatomy::Cells::Cells, Cultured::Cell Line::Cell Line, Tumor [Medical Subject Headings], Phenomena and Processes::Cell Physiological Phenomena::Cell Physiological Processes::Cell Differentiation [Medical Subject Headings], Cell cycle checkpoint, Carcinogenesis, Ciclo celular, lcsh:Medicine, medicine.disease_cause, Organisms::Eukaryota::Animals::Chordata::Vertebrates::Mammals::Primates::Haplorhini::Catarrhini::Hominidae::Humans [Medical Subject Headings], Neoplasms, Chlorocebus aethiops, Organisms::Eukaryota::Animals [Medical Subject Headings], lcsh:Science, Mitocondrias, Cancer, Multidisciplinary, Glutaminase, Chemistry, Cell Differentiation, Hep G2 Cells, Diseases::Neoplasms::Neoplastic Processes::Carcinogenesis [Medical Subject Headings], Diseases::Neoplasms [Medical Subject Headings], Cancer metabolism, Cell biology, Mitochondria, Translocación genética, COS Cells, Anatomy::Cells::Cells, Cultured::Tumor Cells, Cultured::Cell Line, Tumor::Hep G2 Cells [Medical Subject Headings], Proliferación celular, Translocation, Cell cycle, Phenomena and Processes::Cell Physiological Phenomena::Cell Physiological Processes::Cell Cycle::Cell Cycle Checkpoints [Medical Subject Headings], Article, Downregulation and upregulation, Cell Line, Tumor, medicine, Glutaminasa, Animals, Humans, Author Correction, Phenomena and Processes::Cell Physiological Phenomena::Cell Physiological Processes::Cell Growth Processes::Cell Proliferation [Medical Subject Headings], Cell Proliferation, Nucleoplasm, Anatomy::Cells::Cells, Cultured::Cell Line::Cell Line, Transformed::COS Cells [Medical Subject Headings], Oncogene, Cell growth, lcsh:R, Cell Cycle Checkpoints, Cancer cell, lcsh:Q, Chemicals and Drugs::Enzymes and Coenzymes::Enzymes::Hydrolases::Amidohydrolases::Glutaminase [Medical Subject Headings]
Abstract

Glutaminase (GA) catalyzes the first step in mitochondrial glutaminolysis playing a key role in cancer metabolic reprogramming. Humans express two types of GA isoforms: GLS and GLS2. GLS isozymes have been consistently related to cell proliferation, but the role of GLS2 in cancer remains poorly understood. GLS2 is repressed in many tumor cells and a better understanding of its function in tumorigenesis may further the development of new therapeutic approaches. We analyzed GLS2 expression in HCC, GBM and neuroblastoma cells, as well as in monkey COS-7 cells. We studied GLS2 expression after induction of differentiation with phorbol ester (PMA) and transduction with the full-length cDNA of GLS2. In parallel, we investigated cell cycle progression and levels of p53, p21 and c-Myc proteins. Using the baculovirus system, human GLS2 protein was overexpressed, purified and analyzed for posttranslational modifications employing a proteomics LC-MS/MS platform. We have demonstrated a dual targeting of GLS2 in human cancer cells. Immunocytochemistry and subcellular fractionation gave consistent results demonstrating nuclear and mitochondrial locations, with the latter being predominant. Nuclear targeting was confirmed in cancer cells overexpressing c-Myc- and GFP-tagged GLS2 proteins. We assessed the subnuclear location finding a widespread distribution of GLS2 in the nucleoplasm without clear overlapping with specific nuclear substructures. GLS2 expression and nuclear accrual notably increased by treatment of SH-SY5Y cells with PMA and it correlated with cell cycle arrest at G2/M, upregulation of tumor suppressor p53 and p21 protein. A similar response was obtained by overexpression of GLS2 in T98G glioma cells, including downregulation of oncogene c-Myc. Furthermore, human GLS2 was identified as being hypusinated by MS analysis, a posttranslational modification which may be relevant for its nuclear targeting and/or function. Our studies provide evidence for a tumor suppressor role of GLS2 in certain types of cancer. The data imply that GLS2 can be regarded as a highly mobile and multilocalizing protein translocated to both mitochondria and nuclei. Upregulation of GLS2 in cancer cells induced an antiproliferative response with cell cycle arrest at the G2/M phase.

Published
2020

3. Author Correction: Nuclear Translocation of Glutaminase GLS2 in Human Cancer Cells Associates with Proliferation Arrest and Differentiation

Author

Marina García-Frutos, David Carro, Raghavendra G. Mirmira, Antonia Gutierrez, José A. Campos-Sandoval, María C. Gómez-García, Laura Castilla, Amada R. López de la Oliva, José M. Matés, Gert Lubec, Carolina Cardona, José C. Paz, Juan A. Segura, Carolina Lobo, Javier Márquez, Fernando J. Sialana, Narkhyun Bae, Mercedes Martín-Rufián, Ana Peñalver, Victoria Enrique, and Francisco J. Alonso

Subjects
Multidisciplinary, Glutaminase, Science, Cancer research, Medicine, Biology, Human cancer, Nuclear translocation
Abstract

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Published
2021

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