Uncoupling protein 2 and 4 expression pattern during stem cell differentiation provides new insight into their putative function

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Rupprecht, Anne ^a,b   Sittner, Dana ^b,c   Smorodchenko, Alina ^a,b   Hilse, Karolina E ^a   Goyn, Justus ^b,d   Moldzio, Rudolf ^a   Seiler, Andrea E M ^c   Bräuer, Anja U ^b   Pohl, Elena E ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^d Microbiological Quality Control Unit   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLECORTIN; MESSENGER RNA; NEURON SPECIFIC NUCLEAR PROTEIN; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3; UNCOUPLING PROTEIN 4;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CELL MATURATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SUBVENTRICULAR ZONE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; ION CHANNELS; LYMPHOCYTES; MACROPHAGES; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MITOCHONDRIAL PROTEINS; NEURONS;

EID: 84895752271     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088474     Document Type: Article

References (56)

1. Palmieri F, Pierri CL (2010) Mitochondrial metabolite transport. Essays Biochem 47: 37-52.
2. Klingenberg M, Winkler E, Echtay K (2001) Uncoupling protein, H+ transport and regulation. Biochem Soc Trans 29: 806-811.
3. Esteves TC, Brand MD (2005) The reactions catalysed by the mitochondrial uncoupling proteins UCP2 and UCP3. Biochim Biophys Acta 1709: 35-44. (Pubitemid 41096089)
4. Krauss S, Zhang CY, Lowell BB (2005) The mitochondrial uncoupling-protein homologues. Nat Rev Mol Cell Biol 6: 248-261. (Pubitemid 40314925)
5. Jaburek M, Varecha M, Gimeno RE, Dembski M, Jezek P, et al. (1999) Transport function and regulation of mitochondrial uncoupling proteins 2 and 3. J Biol Chem 274: 26003-26007.
6. Hoang T, Smith MD, Jelokhani-Niaraki M (2012) Toward understanding the mechanism of ion transport activity of neuronal uncoupling proteins UCP2, UCP4, and UCP5. Biochemistry 51: 4004-4014.
7. Beck V, Jaburek M, Breen EP, Porter RK, Jezek P, et al. (2006) A new automated technique for the reconstitution of hydrophobic proteins into planar bilayer membranes. Studies of human recombinant uncoupling protein 1. Biochim Biophys Acta 1757: 474-479. (Pubitemid 43993844)
8. Rupprecht A, Sokolenko EA, Beck V, Ninnemann O, Jaburek M, et al. (2010) Role of the transmembrane potential in the membrane proton leak. Biophys J 98: 1503-1511.
9. Nicholls DG (2001) A history of UCP1. Biochem Soc Trans 29: 751-755.
10. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84: 277-359. (Pubitemid 38054374)
11. Fleury C, Neverova M, Collins S, Raimbault S, Champigny O, et al. (1997) Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 15: 269-272. (Pubitemid 27098720)
12. Rupprecht A, Brauer AU, Smorodchenko A, Goyn J, Hilse KE, et al. (2012) Quantification of uncoupling protein 2 reveals its main expression in immune cells and selective up-regulation during T-cell proliferation. PLoS ONE 7: e41406.
13. Pecqueur C, Alves-Guerra MC, Gelly C, Levi-Meyrueis C, Couplan E, et al. (2001) Uncoupling protein 2, in vivo distribution, induction upon oxidative stress, and evidence for translational regulation. J Biol Chem 276: 8705-8712.
14. Rousset S, Mozo J, Dujardin G, Emre Y, Masscheleyn S, et al. (2007) UCP2 is a mitochondrial transporter with an unusual very short half-life. FEBS Lett 581: 479-482. (Pubitemid 46149624)
15. Yu WM, Liu X, Shen J, Jovanovic O, Pohl EE, et al. (2013) Metabolic regulation by the mitochondrial phosphatase PTPMT1 is required for hematopoietic stem cell differentiation. Cell Stem Cell 12: 62-74.
16. Smorodchenko A, Rupprecht A, Sarilova I, Ninnemann O, Brauer AU, et al. (2009) Comparative analysis of uncoupling protein 4 distribution in various tissues under physiological conditions and during development. Biochim Biophys Acta 1788: 2309-2319.
17. Smorodchenko A, Rupprecht A, Fuchs J, Gross J, Pohl EE (2011) Role of mitochondrial uncoupling protein 4 in rat inner ear. Mol Cell Neurosci 47: 244-253.
18. Rousset S, Emre Y, Join-Lambert O, Hurtaud C, Ricquier D, et al. (2006) The uncoupling protein 2 modulates the cytokine balance in innate immunity. Cytokine 35: 135-142. (Pubitemid 44666428)
19. Elorza A, Hyde B, Mikkola HK, Collins S, Shirihai OS (2008) UCP2 modulates cell proliferation through the MAPK/ERK pathway during erythropoiesis and has no effect on heme biosynthesis. J Biol Chem 283: 30461-30470.
20. Zhang J, Khvorostov I, Hong JS, Oktay Y, Vergnes L, et al. (2011) UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J 30: 4860-4873.
21. Pecqueur C, Alves-Guerra C, Ricquier D, Bouillaud F (2009) UCP2, a metabolic sensor coupling glucose oxidation to mitochondrial metabolism? IUBMB Life 61: 762-767.
22. Samudio I, Fiegl M, McQueen T, Clise-Dwyer K, Andreeff M (2008) The warburg effect in leukemia-stroma cocultures is mediated by mitochondrial uncoupling associated with uncoupling protein 2 activation. Cancer Res 68: 5198-5205.
23. Horimoto M, Resnick MB, Konkin TA, Routhier J, Wands JR, et al. (2004) Expression of uncoupling protein-2 in human colon cancer. Clin Cancer Res 10: 6203-6207. (Pubitemid 39287527)
24. Simon-Areces J, Dietrich MO, Hermes G, Garcia-Segura LM, Arevalo MA, et al. (2012) UCP2 induced by natural birth regulates neuronal differentiation of the hippocampus and related adult behavior. PLoS ONE 7: e42911.
25. Alves-Guerra MC, Aheng C, Pecqueur C, Masscheleyn S, Tharaux PL, et al. (2012) Analysis of uncoupling protein 2-deficient mice upon anaesthesia and sedation revealed a role for UCP2 in locomotion. PLoS ONE 7: e41846.
26. Cardoso S, Santos MS, Moreno A, Moreira PI (2013) UCP2 and ANT differently modulate proton-leak in brain mitochondria of long-term hyperglycemic and recurrent hypoglycemic rats. J Bioenerg Biomembr 45: 397-407.
27. Suski JM, Schonfeld P, Bonora M, Shabalina I, Pinton P, et al. (2012) Guanosine diphosphate exerts a lower effect on superoxide release from mitochondrial matrix in the brains of uncoupling protein-2 knockout mice: new evidence for a putative novel function of uncoupling proteins as superoxide anion transporters. Biochem Biophys Res Commun 428: 234-238.
28. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87: 27-45. (Pubitemid 15029925)
29. Seiler AE, Spielmann H (2011) The validated embryonic stem cell test to predict embryotoxicity in vitro. Nat Protoc 6: 961-978.
30. Visan A, Hayess K, Sittner D, Pohl EE, Riebeling C, et al. (2012) Neural differentiation of mouse embryonic stem cells as a tool to assess developmental neurotoxicity in vitro. Neurotoxicology 33: 1135-1146.
31. Bonfanti L, Peretto P (2011) Adult neurogenesis in mammals - a theme with many variations. Eur J Neurosci 34: 930-950.
32. Curtis MA, Low VF, Faull RL (2012) Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation. Dev Neurobiol 72: 990-1005.
33. Pecqueur C, Bui T, Gelly C, Hauchard J, Barbot C, et al. (2008) Uncoupling protein-2 controls proliferation by promoting fatty acid oxidation and limiting glycolysis-derived pyruvate utilization. FASEB J 22: 9-18.
34. Macintyre AN, Rathmell JC (2013) Activated lymphocytes as a metabolic model for carcinogenesis. Cancer and Metabolism 1.
35. Zhou W, Choi M, Margineantu D, Margaretha L, Hesson J, et al. (2012) HIF1alpha induced switch from bivalent to exclusively glycolytic metabolism during ESC-to-EpiSC/hESC transition. EMBO J 31: 2103-2116.
36. Shyh-Chang N, Daley GQ, Cantley LC (2013) Stem cell metabolism in tissue development and aging. Development 140: 2535-2547.
37. Shetty PK, Galeffi F, Turner DA (2012) Cellular Links between Neuronal Activity and Energy Homeostasis. Front Pharmacol 3: 43.
38. Belanger M, Allaman I, Magistretti PJ (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14: 724-738.
39. Pfeiffer T, Schuster S, Bonhoeffer S (2001) Cooperation and competition in the evolution of ATP-producing pathways. Science 292: 504-507. (Pubitemid 32335953)
40. Mao W, Yu XX, Zhong A, Li W, Brush J, et al. (1999) UCP4, a novel brain-specific mitochondrial protein that reduces membrane potential in mammalian cells. FEBS Lett 443: 326-330. (Pubitemid 29080820)
41. Liu D, Chan SL, Souza-Pinto NC, Slevin JR, Wersto RP, et al. (2006) Mitochondrial UCP4 mediates an adaptive shift in energy metabolism and increases the resistance of neurons to metabolic and oxidative stress. Neuromolecular Med 8: 389-414.
42. Lunt SY, Vander Heiden MG (2011) Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 27: 441-464.
43. Munyon WH, Merchant DJ (1959) The relation between glucose utilization, lactic acid production and utilization and the growth cycle of L strain fibroblasts. Exp Cell Res 17: 490-498.
44. Shimasaki Y, Pan N, Messina LM, Li C, Chen K, et al. (2013) Uncoupling Protein 2 Impacts Endothelial Phenotype via p53-Mediated Control of Mitochondrial Dynamics. Circ Res.
45. Alves-Guerra MC, Rousset S, Pecqueur C, Mallat Z, Blanc J, et al. (2003) Bone marrow transplantation reveals the in vivo expression of the mitochondrial uncoupling protein 2 in immune and nonimmune cells during inflammation. J Biol Chem 278: 42307-42312. (Pubitemid 37310499)
46. Ayyasamy V, Owens KM, Desouki MM, Liang P, Bakin A, et al. (2011) Cellular model of Warburg effect identifies tumor promoting function of UCP2 in breast cancer and its suppression by genipin. PLoS ONE 6: e24792.
47. Derdak Z, Mark NM, Beldi G, Robson SC, Wands JR, et al. (2008) The mitochondrial uncoupling protein-2 promotes chemoresistance in cancer cells. Cancer Res 68: 2813-2819. (Pubitemid 351556280)
48. Derdak Z, Fulop P, Sabo E, Tavares R, Berthiaume EP, et al. (2006) Enhanced colon tumor induction in uncoupling protein-2 deficient mice is associated with NF-kappaB activation and oxidative stress. Carcinogenesis 27: 956-961.
49. Liu Y, Chen L, Xu X, Vicaut E, Sercombe R (2009) Both ischemic preconditioning and ghrelin administration protect hippocampus from ischemia/reperfusion and upregulate uncoupling protein-2. BMC Physiol 9: 17.
50. Della-Morte D, Dave KR, DeFazio RA, Bao YC, Raval AP, et al. (2009) Resveratrol pretreatment protects rat brain from cerebral ischemic damage via a sirtuin 1-uncoupling protein 2 pathway. Neuroscience 159: 993-1002.
51. Haines BA, Mehta SL, Pratt SM, Warden CH, Li PA (2010) Deletion of mitochondrial uncoupling protein-2 increases ischemic brain damage after transient focal ischemia by altering gene expression patterns and enhancing inflammatory cytokines. J Cereb Blood Flow Metab 30: 1825-1833.
52. Bechmann I, Diano S, Warden CH, Bartfai T, Nitsch R, et al. (2002) Brain mitochondrial uncoupling protein 2 (UCP2): a protective stress signal in neuronal injury. Biochem Pharmacol 64: 363-367. (Pubitemid 34874838)
53. Mattiasson G, Shamloo M, Gido G, Mathi K, Tomasevic G, et al. (2003) Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma. Nat Med 9: 1062-1068. (Pubitemid 37021787)
54. Diano S, Matthews RT, Patrylo P, Yang L, Beal MF, et al. (2003) Uncoupling protein 2 prevents neuronal death including that occurring during seizures: a mechanism for preconditioning. Endocrinology 144: 5014-5021. (Pubitemid 37378417)
55. Sullivan PG, Dube C, Dorenbos K, Steward O, Baram TZ (2003) Mitochondrial uncoupling protein-2 protects the immature brain from excitotoxic neuronal death. Ann Neurol 53: 711-717. (Pubitemid 36622507)
56. Vogler S, Pahnke J, Rousset S, Ricquier D, Moch H, et al. (2006) Uncoupling protein 2 has protective function during experimental autoimmune encephalomyelitis. Am J Pathol 168: 1570-1575.