Organic cation transporter-mediated ergothioneine uptake in mouse neural progenitor cells suppresses proliferation and promotes differentiation into neurons

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Ishimoto, Takahiro ^a   Nakamichi, Noritaka ^a   Hosotani, Hiroshi ^a   Masuo, Yusuke ^a   Sugiura, Tomoko ^a   Kato, Yukio ^a  

^a KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BETA TUBULIN; BETA3 TUBULIN; CARNITINE TRANSPORTER 1; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; NESTIN; NORPHENAZONE; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; THIONEINE; UNCLASSIFIED DRUG; ANTIOXIDANT; CARNITINE; CARRIER PROTEIN; MEMBRANE PROTEIN; ORGANIC CATION TRANSPORTER; SLC22A4 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; CARCINOMA CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE; GENETIC TRANSFECTION; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; MATH1 GENE; MOUSE; NEURAL STEM CELL; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; DOWN REGULATION; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; STEM CELL; TUMOR CELL LINE;

ANIMALS; ANTIOXIDANTS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARNITINE; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; DOWN-REGULATION; ERGOTHIONEINE; GLIAL FIBRILLARY ACIDIC PROTEIN; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; NEURONS; ORGANIC CATION TRANSPORT PROTEINS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; STEM CELLS; UP-REGULATION;

EID: 84896071197     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089434     Document Type: Article

References (66)

1. Reynolds BA, Weiss S (1996) Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic precursor is a stem cell. Dev Biol 175: 1-13. (Pubitemid 26150042)
2. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, et al. (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25-34. (Pubitemid 29044150)
3. Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70: 687-702.
4. Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, et al (2010) Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One 5: e8809.
5. Horner PJ, Gage FH (2000) Regenerating the damaged central nervous system. Nature 407: 963-970.
6. Hilliard MA (2009) Axonal degeneration and regeneration: a mechanistic tug-of-war. J Neurochem 108: 23-32.
7. Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85: 523-569. (Pubitemid 40404636)
8. Menezes JR, Luskin MB (1994) Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci 14: 5399-5416. (Pubitemid 24279060)
9. Hsieh J, Schneider JW (2013) Neuroscience. Neural stem cells, excited. Science 339: 1534-1535.
10. Yamamoto A, Shofuda T, Islam MO, Nakamura Y, Yamasaki M, et al. (2009) ABCB1 is predominantly expressed in human fetal neural stem/progenitor cells at an early development stage. J Neurosci Res 87: 2615-2623.
11. Islam MO, Kanemura Y, Tajria J, Mori H, Kobayashi S, et al. (2005) Functional expression of ABCG2 transporter in human neural stem progenitor cells. Neurosci Res 52: 75-82. (Pubitemid 40461874)
12. Schumacher T, Krohn M, Hofrichter J, Lange C, Stenzel J, et al. (2012) ABC transporters B1, C1 and G2 differentially regulate neuroregeneration in mice. PLoS One 7: e35613.
13. Gilley JA, Kernie SG (2011) Excitatory amino acid transporter 2 and excitatory amino acid transporter 1 negatively regulate calcium-dependent proliferation of hippocampal neural progenitor cells and are persistently upregulated after injury. Eur J Neurosci 34: 1712-1723.
14. Ogura M, Kakuda T, Takarada T, Nakamichi N, Fukumori R, et al. (2012) Promotion of both proliferation and neuronal differentiation in pluripotent P19 cells with stable overexpression of the glutamine transporter slc38a1. PLoS One 7: e48270.
15. Gründemann D, Harlfinger S, Golz S, Geerts A, Lazar A, et al. (2005) Discovery of the ergothioneine transporter. Proc Natl Acad Sci U S A 102: 5256-5261.
16. Nikodemus D, Lazic D, Bach M, Bauer T, Pfeiffer C, et al. (2011) Paramount levels of ergothioneine transporter SLC22A4 mRNA in boar seminal vesicles and cross-species analysis of ergothioneine and glutathione in seminal plasma. J Physiol Pharmacol 62: 411-419.
17. Gründemann D (2012) The ergothioneine transporter controls and indicates ergothioneine activity - a review. Prev Med 54: Suppl: S71-74.
18. Tamai I, Yabuuchi H, Nezu J, Sai Y, Oku A, et al. (1997) Cloning and characterization of a novel human pH-dependent organic cation transporter, OCTN1. FEBS Lett 419: 107-111. (Pubitemid 28011227)
19. Meier Y, Eloranta JJ, Darimont J, Ismair MG, Hiller C, et al. (2007) Regional distribution of solute carrier mRNA expression along the human intestinal tract. Drug Metab Dispos 35: 590-594. (Pubitemid 46513261)
20. Taubert D, Jung N, Goeser T, Schömig E (2009) Increased ergothioneine tissue concentrations in carriers of the Crohn's disease risk-associated 503F variant of the organic cation transporter OCTN1. Gut 58: 312-314.
21. Grigat S, Harlfinger S, Pal S, Striebinger R, Golz S, et al. (2007) Probing the substrate specificity of the ergothioneine transporter with methimazole, hercynine, and organic cations. Biochem Pharmacol 74: 309-16. (Pubitemid 46890822)
22. Bacher P, Giersiefer S, Bach M, Fork C, Schömig E, et al. (2009) Substrate discrimination by ergothioneine transporter SLC22A4 and carnitine transporter SLC22A5: gain-of-function by interchange of selected amino acids. Biochim Biophys Acta 1788: 2594-2602.
23. Jong NN, Nakanishi T, Liu JJ, Tamai I, McKeage MJ (2011) Oxaliplatin transport mediated by organic cation/carnitine transporters OCTN1 and OCTN2 in overexpressing human embryonic kidney 293 cells and rat dorsal root ganglion neurons. J Pharmacol Exp Ther 338: 537-547.
24. Pochini L, Scalise M, Galluccio M, Pani G, Siminovitch KA, et al. (2011) The human OCTN1 (SLC22A4) reconstituted in liposomes catalyzes acetylcholine transport which is defective in the mutant L503F associated to the Crohn's disease. Biochim Biophys Acta. 1818: 559-565.
25. Kato Y, Kubo Y, Iwata D, Kato S, Sudo T, et al. (2010) Gene knockout and metabolome analysis of carnitine/organic cation transporter OCTN1. Pharm Res 27: 832-840.
26. Sugiura T, Kato S, Shimizu T, Wakayama T, Nakamichi N, et al. (2010) Functional expression of carnitine/organic cation transporter OCTN1/SLC22A4 in mouse small intestine and liver. Drug Metab Dispos 38: 1665-1672.
27. Nakamichi N, Taguchi T, Hosotani H, Wakayama T, Shimizu T, et al. (2012) Functional expression of carnitine/organic cation transporter OCTN1 in mouse brain neurons: possible involvement in neuronal differentiation. Neurochem Int 61: 1121-1132.
28. Inazu M, Takeda H, Maehara K, Miyashita K, Tomoda A, et al. (2006) Functional expression of the organic cation/carnitine transporter 2 in rat astrocytes. J Neurochem 97: 424-434.
29. Okura T, Hattori A, Takano Y, Sato T, Hammarlund-Udenaes M, et al. (2008) Involvement of the pyrilamine transporter, a putative organic cation transporter, in blood-brain barrier transport of oxycodone. Drug Metab Dispos 36: 2005-2013.
30. Yoneyama M, Kawada K, Gotoh Y, Shiba T, Ogita K (2010) Endogenous reactive oxygen species are essential for proliferation of neural stem/progenitor cells. Neurochem Int 56: 740-746.
31. Nakamura Y, Nakamichi N, Takarada T, Ogita K, Yoneda Y (2012) Transferrin receptor-1 suppresses neurite outgrowth in neuroblastoma Neuro2A cells. Neurochem Int 60: 448-457.
32. Khunweeraphong N, Nagamori S, Wiriyasermkul P, Nishinaka Y, Wongthai P, et al. (2012) Establishment of stable cell lines with high expression of heterodimers of human 4F2hc and human amino acid transporter LAT1 or LAT2 and delineation of their differential interaction with α-alkyl moieties. J Pharmacol Sci 119: 368-380.
33. Nakamichi N, Kambe Y, Oikawa H, Ogura M, Takano K, et al. (2005) Protection by exogenous pyruvate through a mechanism related to monocarboxylate transporters against cell death induced by hydrogen peroxide in cultured rat cortical neurons. J Neurochem 93: 84-93. (Pubitemid 40463518)
34. Shuto M, Seko K, Kuramoto N, Sugiyama C, Kawada K, et al. (2009) Activation of c-Jun N-terminal kinase cascades is involved in part of the neuronal degeneration induced by trimethyltin in cortical neurons of mice. J Pharmacol Sci 109: 60-70.
35. Abe K, Matsuki N (2000) Measurement of cellular 3-(4,5-dimethylthiazol-2- yl)-2,5-diphenyltetrazolium bromide (MTT) reduction activity and lactate dehydrogenase release using MTT. Neurosci Res 38: 325-329. (Pubitemid 32063338)
36. Sugiura T, Otake T, Shimizu T, Wakayama T, Silver DL, et al. (2010) PDZK1 regulates organic anion transporting polypeptide Oatp1a in mouse small intestine. Drug Metab Pharmacokinet 25: 588-598.
37. Paul BD, Snyder SH (2010) The unusual amino acid L-ergothioneine is a physiologic cytoprotectant. Cell Death Differ 17: 1134-1140.
38. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, et al. (2011) Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependent manner. Cell Stem Cell 8: 59-71.
39. Haines DD, Lekli I, Teissier P, Bak I, Tosaki A (2012) Role of haeme oxygenase-1 in resolution of oxidative stress-related pathologies: focus on cardiovascular, lung, neurological and kidney disorders. Acta Physiol (Oxf) 204: 487-501.
40. Lewerenz J, Maher P, Methner A (2012) Regulation of xCT expression and system xCT function in neuronal cells. Amino Acids 42: 171-179.
41. Lange C, Huttner WB, Calegari F (2009) Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5: 320-331.
42. Oppel F, Müller N, Schackert G, Hendruschk S, Martin D (2011) SOX2-RNAi attenuates S-phase entry and induces RhoA-dependent switch to protease-independent amoeboid migration in human glioma cells. Mol Cancer 10: 137.
43. Lao CL, Lu CS, Chen JC (2013) Dopamine D(3) receptor activation promotes neural stem/progenitor cell proliferation through AKT and ERK1/2 pathways and expands type-B and -C cells in adult subventricular zone. Glia 61: 475-489.
44. Zhao L, Jiao Q, Chen X, Yang P, Zhao B, et al. (2012) mGluR5 is involved in proliferation of rat neural progenitor cells exposed to hypoxia with activation of mitogen-activated protein kinase signaling pathway. J Neurosci Res 90: 447-460.
45. Nakamichi N, Takarada T, Yoneda Y (2009) Neurogenesis mediated by gamma-aminobutyric acid and glutamate signaling. J Pharmacol Sci 110: 133-149.
46. Bunk EC, König HG, Bonner HP, Kirby BP, Prehn JH (2010) NMDA-induced injury of mouse organotypic hippocampal slice cultures triggers delayed neuroblast proliferation in the dentate gyrus: an in vitro model for the study of neural precursor cell proliferation. Brain Res 1359: 22-32.
47. Yoneyama M, Nakamichi N, Fukui M, Kitayama T, Georgiev DD, et al. (2008) Promotion of neuronal differentiation through activation of N-methyl-D-aspartate receptors transiently expressed by undifferentiated neural progenitor cells in fetal rat neocortex. J Neurosci Res 86: 2392-2402.
48. Nakamichi N, Yoshida K, Ishioka Y, Makanga JO, Fukui M, et al. (2008) Group III metabotropic glutamate receptor activation suppresses self-replication of undifferentiated neocortical progenitor cells. J Neurochem 105: 1996-2012. (Pubitemid 351678510)
49. Takarada T, Nakamichi N, Kitajima S, Fukumori R, Nakazato R, et al. (2012) Promoted neuronal differentiation after activation of alpha4/beta2 nicotinic acetylcholine receptors in undifferentiated neural progenitors. PLoS One 7: e46177.
50. Zhou C, Wen ZX, Shi DM, Xie ZP (2004) Muscarinic acetylcholine receptors involved in the regulation of neural stem cell proliferation and differentiation in vitro. Cell Biol Int 28: 63-67. (Pubitemid 38169016)
51. A receptors in undifferentiated neural progenitors of fetal mouse brain. J Neurosci Res 86: 2615-2623.
52. Kitayama T, Yoneyama M, Yoneda Y (2003) Possible regulation by N-methyl-D-aspartate receptors of proliferative progenitor cells expressed in adult mouse hippocampal dentate gyrus. J Neurochem 84: 767-780. (Pubitemid 36176935)
53. Koepsell H, Lips K, Volk C (2007) Polyspecific organic cation transporters: structure, function, physiological roles, and biopharmaceutical implications. Pharm Res 24: 1227-1251. (Pubitemid 46876495)
54. Motohashi H, Inui K (2013) Multidrug and toxin extrusion family SLC47: Physiological, pharmacokinetic and toxicokinetic importance of MATE1 and MATE2-K. Mol Aspects Med 34: 661-668.
55. Duan H, Wang J (2010) Selective transport of monoamine neurotransmitters by human plasma membrane monoamine transporter and organic cation transporter 3. J Pharmacol Exp Ther 335: 743-753.
56. Yoneda Y, Ogita K, Azuma Y, Kuramoto N, Manabe T, et al. (1999) Predominant expression of nuclear activator protein-1 complex with DNA binding activity following systemic administration of N-methyl-D-aspartate in dentate granule cells of murine hippocampus. Neuroscience 93: 19-31. (Pubitemid 29290683)
57. Wang DD, Krueger DD, Bordey A (2003) GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J Physiol 550: 785-800. (Pubitemid 37010063)
58. Lamhonwah AM, Hawkins CE, Tam C, Wong J, Mai L (2008) Expression patterns of the organic cation/carnitine transporter family in adult murine brain. Brain Dev 30: 31-42. (Pubitemid 350296742)
59. Cheah IK, Halliwell B (2012) Ergothioneine; antioxidant potential, physiological function and role in disease. Biochim Biophys Acta 1822: 784-793.
60. Contestabile A (2008) Regulation of transcription factors by nitric oxide in neurons and in neural-derived tumor cells. Prog Neurobiol 84: 317-328.
61. Lee SH, Na SI, Heo JS, Kim MH, Kim YH, et al. (2009) Arachidonic acid release by H2O2 mediated proliferation of mouse embryonic stem cells: involvement of Ca2+/PKC and MAPKs-induced EGFR transactivation. J Cell Biochem 106: 787-797.
62. Wegner F, Kraft R, Busse K, Härtig W, Ahrens J, et al. (2012) Differentiated human midbrain-derived neural progenitor cells express excitatory strychnine-sensitive glycine receptors containing a2b subunits. PLoS One 7: e36946.
63. Sharma M, Celver J, Kovoor A (2011) Regulator of G protein signaling 9-2 (RGS9-2) mRNA is up regulated during neuronal differentiation of mouse embryonic stem cells. Neurosci Lett 502: 123-128.
64. Elkouby YM, Polevoy H, Gutkovich YE, Michaelov A, Frank D (2012) A hindbrain-repressive Wnt3a/Meis3/Tsh1 circuit promotes neuronal differentiation and coordinates tissue maturation. Development 139: 1487-1497.
65. Kageyama R, Ohtsuka T (1999) The Notch-Hes pathway in mammalian neural development. Cell Res 9: 179-188. (Pubitemid 129623500)
66. Ito H, Nakajima A, Nomoto H, Furukawa S (2003) Neurotrophins facilitate neuronal differentiation of cultured neural stem cells via induction of mRNA expression of basic helix-loop-helix transcription factors Mash1 and Math1. J Neurosci Res 71: 648-658. (Pubitemid 36255349)