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Published Online: 9 January 2013

The Cystine/Glutamate Antiporter System xc in Health and Disease: From Molecular Mechanisms to Novel Therapeutic Opportunities

Publication: Antioxidants & Redox Signaling
Volume 18, Issue Number 5

Abstract

The antiporter system xc imports the amino acid cystine, the oxidized form of cysteine, into cells with a 1:1 counter-transport of glutamate. It is composed of a light chain, xCT, and a heavy chain, 4F2 heavy chain (4F2hc), and, thus, belongs to the family of heterodimeric amino acid transporters. Cysteine is the rate-limiting substrate for the important antioxidant glutathione (GSH) and, along with cystine, it also forms a key redox couple on its own. Glutamate is a major neurotransmitter in the central nervous system (CNS). By phylogenetic analysis, we show that system xc is a rather evolutionarily new amino acid transport system. In addition, we summarize the current knowledge regarding the molecular mechanisms that regulate system xc, including the transcriptional regulation of the xCT light chain, posttranscriptional mechanisms, and pharmacological inhibitors of system xc. Moreover, the roles of system xc in regulating GSH levels, the redox state of the extracellular cystine/cysteine redox couple, and extracellular glutamate levels are discussed. In vitro, glutamate-mediated system xc inhibition leads to neuronal cell death, a paradigm called oxidative glutamate toxicity, which has successfully been used to identify neuroprotective compounds. In vivo, xCT has a rather restricted expression pattern with the highest levels in the CNS and parts of the immune system. System xc is also present in the eye. Moreover, an elevated expression of xCT has been reported in cancer. We highlight the diverse roles of system xc in the regulation of the immune response, in various aspects of cancer and in the eye and the CNS. Antioxid. Redox Signal. 18, 522–555.

Abstract

I. Introduction
A. Oxidative stress and antioxidant defense
B. GSH metabolism
C. Glutamate: neurotransmission and neurotoxicity
II. The Cystine/Glutamate Antiporter System xc
A. Functional and pharmacological characteristics of system xc
B. The molecular biology of system xc
C. The phylogeny of xCT, the specific subunit of system xc
D. Regulation of system xc by transcriptional regulation of its specific subunit xCT
E. Regulation of system xc activity by protein trafficking and protein modification
F. Regulation of system xc activity by substrate availability
III. Expression of System xcIn Vitro and In Vivo and Its Functional Consequences
A. In the absence of disease, system xc shows a rather restricted expression pattern in vivo
B. System xc is induced in most cultured cells
C. The role of system xc in the regulation of GSH synthesis, the extracellular redox milieu, and extracellular glutamate levels
D. Oxidative glutamate toxicity—an in vitro paradigm for neuronal death induced by system xc inhibition
1. The cell death pathway in oxidative glutamate toxicity
2. Using oxidative glutamate toxicity to identify neuroprotective pathways
3. Using oxidative glutamate toxicity to screen for neuroprotective drugs
4. Oxidative glutamate toxicity in vivo
IV. The Role of System xc in Health and Disease
A. System xcin vivo—lessons from xCT-deficient mice
B. The role of system xc in the immune system and inflammation
C. The role of system xc in cancer and resistance against anti-cancer drugs
1. System xc is regulated by potentially oncogenic pathways
2. System xc mediates the infection of cells by oncogenic Kaposi's sarcoma herpesvirus
3. System xc plays an important role in the multidrug resistance of cancers
4. Inhibition of system xc reduces cancer cell replication, tissue invasion, and metastasis
5. System xc expressed in tumor cells may be used as a target for anticancer drug delivery
6. Up-regulation of system xc in normal cells provides protection against carcinogenesis—a possible role in cancer prevention
7. Synopsis of the role of system xc in cancer and resistance against anti-cancer drugs
D. System xc and diseases of the eye
1. Studies of system xc in the retina
2. Studies of system xc in the lens and cornea
3. Synopsis and future directions for system xc and diseases of the eye
E. The role of system xc in diseases of the CNS
F. The role of system xc activity in memory and behavior
V. Conclusion

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Published In

cover image Antioxidants & Redox Signaling
Antioxidants & Redox Signaling
Volume 18Issue Number 5February 10, 2013
Pages: 522 - 555
PubMed: 22667998

History

Published in print: February 10, 2013
Published online: 9 January 2013
Published ahead of print: 3 August 2012
Published ahead of production: 5 June 2012
Accepted: 5 June 2012
Revision received: 19 May 2012
Received: 2 November 2011

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Jan Lewerenz
Department of Neurology, University of Ulm, Ulm, Germany.
Sandra J. Hewett
Program in Neuroscience, Department of Biology, Syracuse University, Syracuse, New York.
Ying Huang
Center for the Advancement of Drug Research and Evaluation, College of Pharmacy, Western University of Health Sciences, Pomona, California.
Maria Lambros
Center for the Advancement of Drug Research and Evaluation, College of Pharmacy, Western University of Health Sciences, Pomona, California.
Peter W. Gout
Department of Experimental Therapeutics, BC Cancer Agency, Vancouver, British Columbia, Canada.
Peter W. Kalivas
Department of Neurosciences, Medical University of South Carolina, Charleston, South Carolina.
Ann Massie
Department of Pharmaceutical Biotechnology and Molecular Biology, Vrije Universiteit Brussel, Brussels, Belgium.
Ilse Smolders
Department of Pharmaceutical Chemistry and Drug Analysis, Center for Neuroscience, Vrije Universiteit Brussel, Brussels, Belgium.
Axel Methner
Department of Neurology, Heinrich-Heine-University Duesseldorf, Duesseldorf, Germany.
Mathias Pergande
Department of Neurology, Heinrich-Heine-University Duesseldorf, Duesseldorf, Germany.
Sylvia B. Smith
Department of Cellular Biology and Anatomy, Medical College of Georgia, Augusta, Georgia.
Vadivel Ganapathy
Department of Biochemistry and Molecular Biology, Medical College of Georgia, Augusta, Georgia.
Pamela Maher
Cellular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, California.

Notes

Address correspondence to:Dr. Jan LewerenzDepartment of NeurologyUniversity of UlmOberer Eselsberg 4589081 UlmGermany
E-mail: [email protected]
Reviewing Editors: Markus Conrad, Miriam Cortese-Krott, Giovanni Li Volti, Doug Lobner, Carlos Matute, Hugo Monteiro, Osamu Nagano, Chris Norris, Hideyo Sato, and Oren Tirosh

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