The mitochondrial respiratory chain is essential for haematopoietic stem cell function (original) (raw)

• Chandel, N. S., Jasper, H., Ho, T. T. & Passegue, E. Metabolic regulation of stem cell function in tissue homeostasis and organismal ageing. Nat. Cell Biol. 18, 823–832 (2016).
  Article CAS PubMed Google Scholar
• Ito, K. & Suda, T. Metabolic requirements for the maintenance of self-renewing stem cells. Nat. Rev. Mol. Cell Biol. 15, 243–256 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Takubo, K. et al. Regulation of glycolysis by pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell 12, 49–61 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Adelman, D. M., Maltepe, E. & Simon, M. C. Multilineage embryonic hematopoiesis requires hypoxic ARNT activity. Genes Dev. 13, 2478–2483 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Simsek, T. et al. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 7, 380–390 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Norddahl, G. L. et al. Accumulating mitochondrial DNA mutations drive premature hematopoietic aging phenotypes distinct from physiological stem cell aging. Cell Stem Cell 8, 499–510 (2011).
  Article CAS PubMed Google Scholar
• Parmar, K., Mauch, P., Vergilio, J.-A., Sackstein, R. & Down, J. D. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc. Natl Acad. Sci. USA 104, 5431–5436 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Spencer, J. A. et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 508, 269–273 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Tothova, Z. et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128, 325–339 (2007).
  Article CAS PubMed Google Scholar
• Ito, K. et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat. Med. 12, 446–451 (2006).
  Article CAS PubMed Google Scholar
• Chen, C. et al. TSC–mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J. Experim. Med. 205, 2397–2408 (2008).
  Article CAS Google Scholar
• Jung, H. et al. TXNIP maintains the hematopoietic cell pool by switching the function of p53 under oxidative stress. Cell Metab. 18, 75–85 (2013).
  Article CAS PubMed Google Scholar
• Ito, K. et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431, 997–1002 (2004).
  Article CAS PubMed Google Scholar
• Maryanovich, M. et al. The ATM-BID pathway regulates quiescence and survival of haematopoietic stem cells. Nat. Cell Biol. 14, 535–541 (2012).
  Article CAS PubMed Google Scholar
• Ahlqvist, K. J. et al. Somatic progenitor cell vulnerability to mitochondrial DNA mutagenesis underlies progeroid phenotypes in Polg mutator mice. Cell Metab. 15, 100–109 (2012).
  Article CAS PubMed Google Scholar
• Maryanovich, M. et al. An MTCH2 pathway repressing mitochondria metabolism regulates haematopoietic stem cell fate. Nat. Commun. 6, 7901 (2015).
  Article CAS PubMed Google Scholar
• Yu, W.-M. et al. Metabolic regulation by the mitochondrial phosphatase PTPMT1 is required for hematopoietic stem cell differentiation. Cell Stem Cell 12, 62–74 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Gan, B. et al. Lkb1 regulates quiescence and metabolic homeostasis of haematopoietic stem cells. Nature 468, 701–704 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Gurumurthy, S. et al. The Lkb1 metabolic sensor maintains haematopoietic stem cell survival. Nature 468, 659–663 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Nakada, D., Saunders, T. L. & Morrison, S. J. Lkb1 regulates cell cycle and energy metabolism in haematopoietic stem cells. Nature 468, 653–658 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Sena, L. A. et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38, 225–236 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Ema, H. & Nakauchi, H. Expansion of hematopoietic stem cells in the developing liver of a mouse embryo. Blood 95, 2284–2288 (2000).
  Article CAS PubMed Google Scholar
• Larsson, N. G. et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 18, 231–236 (1998).
  Article CAS PubMed Google Scholar
• Martinez-Reyes, I. et al. TCA cycle and mitochondrial membrane potential are necessary for diverse biological functions. Mol. Cell 61, 199–209 (2016).
  Article CAS PubMed Google Scholar
• Orkin, S. H. & Zon, L. I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132, 631–644 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• McDonnell, E. et al. Lipids reprogram metabolism to become a major carbon source for histone acetylation. Cell Rep. 17, 1463–1472 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Losman, J. A. & Kaelin, W. G. Jr What a difference a hydroxyl makes: mutant IDH, (R)-2-hydroxyglutarate, and cancer. Genes Dev. 27, 836–852 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Xu, W. et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of α-ketoglutarate-dependent dioxygenases. Cancer Cell 19, 17–30 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Xiao, M. et al. Inhibition of α-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors. Genes Dev. 26, 1326–1338 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Sullivan, L. B. et al. The proto-oncometabolite fumarate binds glutathione to amplify ROS-dependent signaling. Mol. Cell 51, 236–248 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Sciacovelli, M. et al. Fumarate is an epigenetic modifier that elicits epithelial-to-mesenchymal transition. Nature 537, 544–547 (2016).
  Article CAS PubMed PubMed Central Google Scholar
• Engqvist, M. K., Esser, C., Maier, A., Lercher, M. J. & Maurino, V. G. Mitochondrial 2-hydroxyglutarate metabolism. Mitochondrion 19B, 275–281 (2014).
  Article CAS Google Scholar
• Oldham, W. M., Clish, C. B., Yang, Y. & Loscalzo, J. Hypoxia-mediated increases in l-2-hydroxyglutarate coordinate the metabolic response to reductive stress. Cell Metab. 22, 291–303 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Chowdhury, R. et al. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep. 12, 463–469 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Birsoy, K. et al. An essential role of the mitochondrial electron transport chain in cell proliferation is to enable aspartate synthesis. Cell 162, 540–551 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Sullivan, L. B. et al. Supporting aspartate biosynthesis is an essential function of respiration in proliferating cells. Cell 162, 552–563 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Chandel, N. S. Evolution of mitochondria as signaling organelles. Cell Metab. 22, 204–206 (2015).
  Article CAS PubMed Google Scholar
• Tormos, K. V. et al. Mitochondrial complex III ROS regulate adipocyte differentiation. Cell Metab. 14, 537–544 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Hamanaka, R. B. et al. Mitochondrial reactive oxygen species promote epidermal differentiation and hair follicle development. Sci. Signal. 6, ra8 (2013).
  Article PubMed PubMed Central CAS Google Scholar
• Owusu-Ansah, E. & Banerjee, U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461, 537–541 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, J. et al. UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J. 30, 4860–4873 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Mullen, A. R. et al. Oxidation of α-ketoglutarate is required for reductive carboxylation in cancer cells with mitochondrial defects. Cell Rep. 7, 1679–1690 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Shim, E. H. et al. L-2-Hydroxyglutarate: an epigenetic modifier and putative oncometabolite in renal cancer. Cancer Discov. 4, 1290–1298 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Weinberg, F. et al. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc. Natl Acad. Sci. USA 107, 8788–8793 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Wheaton, W. W. et al. Metformin inhibits mitochondrial complex I of cancer cells to reduce tumorigenesis. eLife 3, e02242 (2014).
  Article PubMed PubMed Central CAS Google Scholar
• Evans, D. R. & Guy, H. I. Mammalian pyrimidine biosynthesis: fresh insights into an ancient pathway. J. Biol. Chem. 279, 33035–33038 (2004).
  Article CAS PubMed Google Scholar
• Mullen, A. R. et al. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 481, 385–388 (2012).
  Article CAS Google Scholar
• Liu, X. et al. Regulation of mitochondrial biogenesis in erythropoiesis by mTORC1-mediated protein translation. Nat. Cell Biol. http://dx.doi.org/10.1038/ncb3527 (2017).
• Sena, L. A. et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38, 225–236 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105–1111 (2009).
  CAS PubMed PubMed Central Google Scholar
• Anders, S., Pyl, P. T. & Huber, W. HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).
  CAS PubMed Google Scholar
• Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511–515 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Lu, W. et al. Metabolomic analysis via reversed-phase ion-pairing liquid chromatography coupled to a stand alone orbitrap mass spectrometer. Anal. Chem. 82, 3212–3221 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Garcia, B. A. et al. Chemical derivatization of histones for facilitated analysis by mass spectrometry. Nat. Protoc. 2, 933–938 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Zheng, Y., Tipton, J. D., Thomas, P. M., Kelleher, N. L. & Sweet, S. M. Site-specific human histone H3 methylation stability: fast K4me3 turnover. Proteomics 14, 2190–2199 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Zheng, Y., Thomas, P. M. & Kelleher, N. L. Measurement of acetylation turnover at distinct lysines in human histones identifies long-lived acetylation sites. Nat. Commun. 4, 2203 (2013).
  Article PubMed CAS Google Scholar
• MacLean, B. et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966–968 (2010).
  Article CAS PubMed PubMed Central Google Scholar