Membrane transport of sepiapterin and dihydrobiopterin by equilibrative nucleoside transporters: A plausible gateway for the salvage pathway of Tetrahydrobiopterin biosynthesis

Molecular Genetics and Metabolism

Volumn 102, Issue 1, 2011, Pages 18-28

  Ohashi, Akiko ^a   Sugawara, Yuko ^b   Mamada, Kaori ^a   Harada, Yoshinori ^b   Sumi, Tomomi ^b   Anzai, Naohiko ^c   Aizawa, Shin ^a   Hasegawa, Hiroyuki ^a  

^a NIHON UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b TEIKYO UNIVERSITY OF SCIENCE   (Japan)

^c KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

BH4 responsive PKU; Dihydrobiopterin; Endothelial cell; Equilibrative nucleoside transporter; NO synthesis; Salvage pathway; Sepiapterin; Supplement; Tetrahydrobiopterin

Indexed keywords

DIHYDROBIOPTERIN; NITROBENZYLTHIOINOSINE; NUCLEOSIDE TRANSPORTER; SEPIAPTERIN; TETRAHYDROBIOPTERIN;

ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CELL LEVEL; CELL MEMBRANE; ENDOTHELIUM CELL; GENE EXPRESSION SYSTEM; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; RAT; URINARY EXCRETION; XENOPUS;

ANIMALS; BIOPTERIN; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; EQUILIBRATIVE NUCLEOSIDE TRANSPORT PROTEINS; FEMALE; HELA CELLS; HUMANS; MICE; MICE, INBRED C57BL; OOCYTES; PTERINS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; THIOINOSINE; XENOPUS LAEVIS;

MUS; RATTUS;

EID: 78650857261     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2010.09.005     Document Type: Article

References (58)

1. Kaufman S. The structure of the phenylalanine-hydroxylation cofactor. Proc. Natl. Acad. Sci. U. S. A. 1963, 50:1085-1093.
2. Nagatsu T., Levitt M., Udenfriend S. Tyrosine hydroxylase. the initial step in norepinephrine biosynthesis. J. Biol. Chem. 1964, 239:2910-2917.
3. Lovenberg W., Jequier E., Sjoerdsma A. Tryptophan hydroxylation: measurement in pineal gland, brainstem, and carcinoid tumor. Science 1967, 155:217-219.
4. Kwon N.S., Nathan C.F., Stuehr D.J. Reduced biopterin as a cofactor in the generation of nitrogen oxides by murine macrophages. J. Biol. Chem. 1989, 264:20496-20501.
5. Baek K.J., Thiel B.A., Lucas S., Stuehr D.J. Macrophage nitric oxide synthase subunits. Purification, characterization, and role of prosthetic groups and substrate in regulating their association into a dimeric enzyme. J. Biol. Chem. 1993, 268:21120-21129.
6. Nichol C.A., Smith G.K., Duch D.S. Biosynthesis and metabolism of tetrahydrobiopterin and molybdopterin. Annu. Rev. Biochem. 1985, 54:729-764.
7. Thony B., Auerbach G., Blau N. Tetrahydrobiopterin biosynthesis, regeneration and functions. Biochem. J. 2000, 347(Pt 1):1-16.
8. Werner-Felmayer G., Golderer G., Werner E.R. Tetrahydrobiopterin biosynthesis, utilization and pharmacological effects. Curr. Drug Metab. 2002, 3:159-173.
9. Kaufman S. Studies on the structure of the primary oxidation product formed from tetrahydropteridines during phenylalamine hydroxylation. J. Biol. Chem. 1964, 239:332-338.
10. Kato S. Sepiapterin reductase from horse liver: purification and properties of the enzyme. Arch. Biochem. Biophys. 1971, 146:202-214.
11. Kaufman S. Metabolism of the phenylalanine hydroxylation cofactor. J. Biol. Chem. 1967, 242:3934-3943.
12. Abelson H.T., Spector R., Gorka C., Fosburg M. Kinetics of tetrahydrobiopterin synthesis by rabbit brain dihydrofolate reductase. Biochem. J. 1978, 171:267-268.
13. Matsubara M., Akino M. On the presence of sepiapterin reductase different from folate and dihydrofolate reductase in chicken liver. Experientia 1964, 20:574-575.
14. Matsubara M., Katoh S., Akino M., Kaufman S. Sepiapterin reductase. Biochim. Biophys. Acta 1966, 122:202-212.
15. Fukushima T. Biosynthesis of pteridines in the tadpole of the bullfrog, Rana catesbeiana. Arch. Biochem. Biophys. 1970, 139:361-369.
16. Nichol C.A., Lee C.L., Edelstein M.P., Chao J.Y., Duch D.S. Biosynthesis of tetrahydrobiopterin by de novo and salvage pathways in adrenal medulla extracts, mammalian cell cultures, and rat brain in vivo. Proc. Natl. Acad. Sci. U. S. A. 1983, 80:1546-1550.
17. Sawabe K., Wakasugi K.O., Hasegawa H. Tetrahydrobiopterin uptake in supplemental administration: elevation of tissue tetrahydrobiopterin in mice following uptake of the exogenously oxidized product 7, 8-dihydrobiopterin and subsequent reduction by an anti-folate-sensitive process. J. Pharmacol. Sci. 2004, 96:124-133.
18. Sawabe K., Yamamoto K., Harada Y., Ohashi A., Sugawara Y., Matsuoka H., Hasegawa H. Cellular uptake of sepiapterin and push-pull accumulation of tetrahydrobiopterin. Mol. Genet. Metab. 2008, 94:410-416.
19. Griffith D.A., Jarvis S.M. Nucleoside and nucleobase transport systems of mammalian cells. Biochim. Biophys. Acta 1996, 1286:153-181.
20. Young J.D., Yao S.Y., Sun L., Cass C.E., Baldwin S.A. Human equilibrative nucleoside transporter (ENT) family of nucleoside and nucleobase transporter proteins. Xenobiotica 2008, 38:995-1021.
21. L. Bianchi and M. Driscoll, Heterologous expression of C. elegans ion channels in Xenopus oocytes. in: T.C.e.R. Community, (Ed.), WormBook, WormBook, 2006, pp. 1-16.
22. Sawabe K., Saeki Y., Ohashi A., Mamada K., Wakasugi K.O., Matsuoka H., Hasegawa H. Tetrahydrobiopterin in intestinal lumen: its absorption and secretion in the small intestine and the elimination in the large intestine. J. Inherit. Metab. Dis. 2008, 32:79-85.
23. Fukushima T., Nixon J.C. Analysis of reduced forms of biopterin in biological tissues and fluids. Anal. Biochem. 1980, 102:176-188.
24. Yao S.Y., Ng A.M., Vickers M.F., Sundaram M., Cass C.E., Baldwin S.A., Young J.D. Functional and molecular characterization of nucleobase transport by recombinant human and rat equilibrative nucleoside transporters 1 and 2. Chimeric constructs reveal a role for the ENT2 helix 5-6 region in nucleobase translocation. J. Biol. Chem. 2002, 277:24938-24948.
25. Baldwin S.A., Beal P.R., Yao S.Y., King A.E., Cass C.E., Young J.D. The equilibrative nucleoside transporter family, SLC29. Pflugers Arch. 2004, 447:735-743.
26. Lu H., Chen C., Klaassen C. Tissue distribution of concentrative and equilibrative nucleoside transporters in male and female rats and mice. Drug Metab. Dispos. 2004, 32:1455-1461.
27. Damaraju V.L., Damaraju S., Young J.D., Baldwin S.A., Mackey J., Sawyer M.B., Cass C.E. Nucleoside anticancer drugs: the role of nucleoside transporters in resistance to cancer chemotherapy. Oncogene 2003, 22:7524-7536.
28. Zhang J., Visser F., King K.M., Baldwin S.A., Young J.D., Cass C.E. The role of nucleoside transporters in cancer chemotherapy with nucleoside drugs. Cancer Metastasis Rev. 2007, 26:85-110.
29. Hoshiga M., Hatakeyama K., Watanabe M., Shimada M., Kagamiyama H. Autoradiographic distribution of [14C]tetrahydrobiopterin and its developmental change in mice. J. Pharmacol. Exp. Ther. 1993, 267:971-978.
30. Shinozaki K., Kashiwagi A., Masada M., Okamura T. Stress and vascular responses: oxidative stress and endothelial dysfunction in the insulin-resistant state. J. Pharmacol. Sci. 2003, 91:187-191.
31. Alp N.J., Channon K.M. Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler. Thromb. Vasc. Biol. 2004, 24:413-420.
32. Schmidt T.S., Alp N.J. Mechanisms for the role of tetrahydrobiopterin in endothelial function and vascular disease. Clin. Sci. (Lond.) 2007, 113:47-63.
33. Hasegawa H., Sawabe K., Nakanishi N., Wakasugi O.K. Delivery of exogenous tetrahydrobiopterin (BH4) to cells of target organs: role of salvage pathway and uptake of its precursor in effective elevation of tissue BH4. Mol. Genet. Metab. 2005, 86(Suppl 1):S2-S10.
34. Sawabe K., Suetake Y., Wakasugi K.O., Hasegawa H. Accumulated BH4 in mouse liver caused by administration of either 6R- or 6SBH4 consisted solely of the 6R-diastereomer: evidence of oxidation to BH2 and enzymic reduction. Mol. Genet. Metab. 2005, 86(Suppl 1):S145-S147.
35. Sawabe K., Suetake Y., Nakanishi N., Wakasugi K.O., Hasegawa H. Cellular accumulation of tetrahydrobiopterin following its administration is mediated by two different processes; direct uptake and indirect uptake mediated by a methotrexate-sensitive process. Mol. Genet. Metab. 2005, 86(Suppl 1):S133-S138.
36. Bonafe L., Thony B., Penzien J.M., Czarnecki B., Blau N. Mutations in the sepiapterin reductase gene cause a novel tetrahydrobiopterin-dependent monoamine-neurotransmitter deficiency without hyperphenylalaninemia. Am. J. Hum. Genet. 2001, 69:269-277.
37. Zorzi G., Redweik U., Trippe H., Penzien J.M., Thony B., Blau N. Detection of sepiapterin in CSF of patients with sepiapterin reductase deficiency. Mol. Genet. Metab. 2002, 75:174-177.
38. Hama T., Obika M. On the nature of some fluorescent substances of pterin type in the adult skin of toad, Bufo vulgaris formosus. Experientia 1958, 14:182-184.
39. Hama T. The relation between the chromatophores and pterin compounds. Ann. N Y Acad. Sci. 1963, 100:977-986.
40. Gross S.S., Jaffe E.A., Levi R., Kilbourn R.G. Cytokine-activated endothelial cells express an isotype of nitric oxide synthase which is tetrahydrobiopterin-dependent, calmodulin-independent and inhibited by arginine analogs with a rank-order of potency characteristic of activated macrophages. Biochem. Biophys. Res. Commun. 1991, 178:823-829.
41. Barnes K., Dobrzynski H., Foppolo S., Beal P.R., Ismat F., Scullion E.R., Sun L., Tellez J., Ritzel M.W., Claycomb W.C., Cass C.E., Young J.D., Billeter-Clark R., Boyett M.R., Baldwin S.A. Distribution and functional characterization of equilibrative nucleoside transporter-4, a novel cardiac adenosine transporter activated at acidic pH. Circ. Res. 2006, 99:510-519.
42. Bone D.B., Hammond J.R. Nucleoside and nucleobase transporters of primary human cardiac microvascular endothelial cells: characterization of a novel nucleobase transporter. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H3325-H3332.
43. Tsutsui M., Milstien S., Katusic Z.S. Effect of tetrahydrobiopterin on endothelial function in canine middle cerebral arteries. Circ. Res. 1996, 79:336-342.
44. Chalupsky K., Cai H. Endothelial dihydrofolate reductase: critical for nitric oxide bioavailability and role in angiotensin II uncoupling of endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9056-9061.
45. Sugiyama T., Levy B.D., Michel T. Tetrahydrobiopterin recycling, a key determinant of endothelial nitric-oxide synthase-dependent signaling pathways in cultured vascular endothelial cells. J. Biol. Chem. 2009, 284:12691-12700.
46. Kaufman S. Dihydropteridine reductase from sheep liver. Methods Enzymol. 1987, 142:97-103.
47. Hasegawa H., Nakanishi N. Dihydropteridine reductase from bovine liver. Methods Enzymol 1987, 142:103-110.
48. Vasquez-Vivar J., Kalyanaraman B., Martasek P., Hogg N., Masters B.S., Karoui H., Tordo P., Pritchard K.A. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:9220-9225.
49. Crabtree M.J., Smith C.L., Lam G., Goligorsky M.S., Gross S.S. Ratio of 5, 6, 7, 8-tetrahydrobiopterin to 7, 8-dihydrobiopterin in endothelial cells determines glucose-elicited changes in NO vs. superoxide production by eNOS. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H1530-H1540.
50. Crabtree M.J., Tatham A.L., Al-Wakeel Y., Warrick N., Hale A.B., Cai S., Channon K.M., Alp N.J. Quantitative regulation of intracellular endothelial nitric-oxide synthase (eNOS) coupling by both tetrahydrobiopterin-eNOS stoichiometry and biopterin redox status: insights from cells with tet-regulated GTP cyclohydrolase I expression. J. Biol. Chem. 2009, 284:1136-1144.
51. Azumagawa K., Suzuki S., Mino M. Developmental changes of tetrahydrobiopterin in rat and human erythrocytes. J. Nutr. Sci. Vitaminol. (Tokyo) 1995, 41:607-617.
52. Hayashi T., Ogata A., Takehisa M., Komoriya K., Ohnuma N. Studies on metabolism and disposition of Sapropterin hydrochloride (SUN 0588) l-erythro-tetrahydrobiopterin hydrochloride in rats. Kiso to Rinsho 1992, 26:3471-3495.
53. Kure S., Hou D.C., Ohura T., Iwamoto H., Suzuki S., Sugiyama N., Sakamoto O., Fujii K., Matsubara Y., Narisawa K. Tetrahydrobiopterin-responsive phenylalanine hydroxylase deficiency. J. Pediatr. 1999, 135:375-378.
54. Kapatos G., Katoh S., Kaufman S. Biosynthesis of biopterin by rat brain. J. Neurochem. 1982, 39:1152-1162.
55. Brand M.P., Hyland K., Engle T., Smith I., Heales S.J. Neurochemical effects following peripheral administration of tetrahydropterin derivatives to the hph-1 mouse. J. Neurochem. 1996, 66:1150-1156.
56. Kapatos G., Hirayama K., Hasegawa H. Tetrahydrobiopterin turnover in cultured rat sympathetic neurons: developmental profile, pharmacologic sensitivity, and relationship to norepinephrine synthesis. J. Neurochem. 1992, 59:2048-2055.
57. Hasegawa H., Sawabe K., Sugawara Y., Maruyama S., Matsuoka H., Nakanishi N., Wakasugi K.O. Recent studies on sepiapterin and biopterin transport in mammalian cells. Chemistry and Biology of Pteridines and Folates 2007, 254-268. SPS Publications, Heilbronn. G. Jansen, G. Peters (Eds.).
58. Watabe S. Purification and characterization of tetrahydrofolate protein complex in bovine liver. J. Biol. Chem. 1978, 253:6673-6679.