Novel localization of OCTN1, an organic cation/carnitine transporter, to mammalian mitochondria

Biochemical and Biophysical Research Communications

Volumn 345, Issue 4, 2006, Pages 1315-1325

  Lamhonwah, Anne Marie ^a   Tein, Ingrid ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Carnitine organic cation transporters; Fatty acid oxidation; Mitochondria; OCTN1

Indexed keywords

ACYLCARNITINE CARNITINE TRANSLOCASE; BIOLOGICAL MARKER; CARNITINE; CELL MARKER; COMPLEMENTARY DNA; ENZYME ANTIBODY; GLUTATHIONE TRANSFERASE ANTIBODY; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; ORGANIC CATION CARNITINE TRANSPORTER 1; ORGANIC CATION TRANSPORTER; PROTEIN ANTIBODY; RABBIT ANTISERUM; RED FLUORESCENT PROTEIN; TRITIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL LINE; CELL TRANSPORT; CELLULAR DISTRIBUTION; EMBRYO; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; HEART; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGOLD LABELING; IMMUNOHISTOCHEMISTRY; INCUBATION TIME; INTRACELLULAR SPACE; MAMMAL; MITOCHONDRION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LOCALIZATION; SKIN FIBROBLAST; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

3T3 CELLS; ADULT; ANIMALS; BLOTTING, WESTERN; CARNITINE; CARNITINE ACYLTRANSFERASES; CELL LINE; CELL LINE, TUMOR; FIBROBLASTS; GENE EXPRESSION PROFILING; GREEN FLUORESCENT PROTEINS; HUMANS; MALE; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; MITOCHONDRIA, HEART; MUTATION; ORGANIC CATION TRANSPORT PROTEINS; RECOMBINANT FUSION PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION;

CAPRA HIRCUS; MAMMALIA; MURINAE; ORYCTOLAGUS CUNICULUS;

EID: 33744801418     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.05.026     Document Type: Article

References (56)

1. Bremer J. Carnitine-metabolism and functions. Physiol. Rev. 63 (1983) 1420-1480
2. Wu X., Prasad P.D., Leibach F.H., and Ganapathy V. cDNA sequence, transport function, and genomic organization of human OCTN2, a new member of the organic cation transporter family. Biochem. Biophys. Res. Commun. 246 (1998) 589-595
3. Tamai I., Ohashi R., Nezu J., Yabuuchi H., Oku A., Shimane M., Sai Y., and Tsuji A. Molecular and functional identification of sodium ion-dependent, high affinity human carnitine transporter OCTN2. J. Biol. Chem. 273 (1998) 20378-20382
4. Lamhonwah A.M., and Tein I. Carnitine uptake defect: frameshift mutations in the human plasmalemmal carnitine transporter gene. Biochem. Biophys. Res. Commun. 252 (1998) 396-401
5. Nezu J., Tamai I., Oku A., Ohashi R., Yabuuchi H., Hashimoto N., Nikaido H., Sai Y., Koizumi A., Shoji Y., Takada G., Matsuishi T., Yoshino M., Kato H., Ohura T., Tsujimoto G., Hayakawa J., Shimane M., and Tsuji A. Primary systemic carnitine deficiency is caused by mutations in a gene encoding sodium ion-dependent carnitine transporter. Nat. Genet. 21 (1999) 91-94
6. Tang N.L., Ganapathy V., Wu X., Hui J., Seth P., Yuen P.M., Wanders R.J., Fok T.F., and Hjelm N.M. Mutations of OCTN2, an organic cation/carnitine transporter, lead to deficient cellular carnitine uptake in primary carnitine deficiency. Hum. Mol. Genet. 8 (1999) 655-660
7. Tein I., De Vivo D.C., Bierman F., Pulver P., De Meirleir L.J., Cvitanovic-Sojat L., Pagon R.A., Bertini E., Dionisi-Vici C., Servidei S., and DiMauro S. Impaired skin fibroblast carnitine uptake in primary systemic carnitine deficiency manifested by childhood carnitine-responsive cardiomyopathy. Pediatr. Res. 28 (1990) 247-255
8. Stanley C.A., DeLeeuw S., Coates P.M., Vianey-Liaud C., Divry P., Bonnefont J.P., Saudubray J.M., Haymond M., Trefz F.K., Breningstall G.N., Wappner R.S., Byrd D.J., Sansaricq C., Tein I., Grover W., Valle D., Rutledge S.L., and Treem W.R. Chronic cardiomyopathy and weakness or acute coma in children with a defect in carnitine uptake. Ann. Neurol. 30 (1991) 709-716
9. Bahl J., Navin T., Manian A., and Bressler R. Carnitine transport in isolated adult rat heart myocytes and the effect of 7,8,-diOH chlorpromazine. Circ. Res. 48 (1981) 378-385
10. Rebouche C.J., and Engel A.G. Carnitine transport in cultured muscle cells and skin fibroblasts from patients with primary systemic carnitine deficiency. In Vitro 18 (1982) 495-500
11. Treem W.R., Stanley C.A., Finegold D.N., Hale D.E., and Coates P.N. Primary carnitine deficiency due to a failure of carnitine transport in kidney, muscle and fibroblasts. N. Engl. J. Med. 319 (1988) 1331-1336
12. Pons R., Carrozzo R., Tein I., Walker W.F., Addonizio L.J., Rhead W., Miranda A.F., DiMauro S., and De Vivo D.C. Deficient muscle carnitine transport in primary carnitine deficiency. Pediatr. Res. 42 (1997) 583-587
13. James M.J., Brooks D.E., and Snoswell A.M. Kinetics of carnitine uptake by rat epididymal cells. Androgen-dependence and lack of stereospecificity. FEBS Lett. 126 (1981) 53-56
14. Hamilton J.W., Li B.U.K., Shug A., and Olsen W.A. Studies of l-carnitine absorption in man. Gastroeneterology 84 (1983) 1180
15. Bieber L.L. Carnitine. Ann. Rev. Biochem. 57 (1988) 261-283
16. Huth P.J., and Shug A. Properties of carnitine transport in rat kidney cortex slices. Biochim. Biophys. Acta 602 (1980) 621-634
17. Shaw R.D., Li B.U., Hamilton J.W., Shug A.L., and Olsen W.A. Carnitine transport in rat small intestine. Am. J. Physiol. 245 (1983) G376-G381
18. Martinuzzi A., Vergani L., Rosa M., and Angelini C. l-carnitine uptake in differentiating human cultured muscle. Biochim. Biophys. Acta 1095 (1991) 217-222
19. Tamai I., Ohashi R., Nezu J.I., Sai Y., Kobayashi D., Oku A., Shimane M., and Tsuji A. Molecular and functional characterization of organic cation/carnitine transporter family in mice. J. Biol. Chem. 275 (2000) 40064-40072
20. Pritchard J.B., and Miller D.S. Mechanisms mediating renal secretion of organic anions and cations. Physiol. Rev. 73 (1983) 765-796
21. Ullrich K.J. Specificity of transporters for 'organic anions' and 'organic cations' in the kidney. Biochim. Biophys. Acta 1197 (1994) 45-62
22. Zevin S., Schaner M.E., Illsley N.P., and Giacomini K.M. Guanidine transport in a human choriocarcinoma cell line (JAR). Pharm. Res. 14 (1997) 401-405
23. Tamai I., Yabuuchi H., Nezu J., Sai Y., Oku A., Shimane M., and Tsuji A. Cloning and characterization of a novel human pH-dependent organic cation transporter, OCTN1. FEBS Lett. 419 (1997) 107-111
24. Yabuuchi H., Tamai I., Nezu J., Sakamoto K., Oku A., Shimane M., Sai Y., and Tsuji A. Novel membrane transporter OCTN1 mediates multispecific, bidirectional, and pH-dependent transport of organic cations. J. Pharm. Exp. Ther. 289 (1999) 768-773
25. Wu X., Huang W., Prasad P.D., Seth P., Rajan D.P., Leibach F.H., Chen J., Conway S.I., and Ganapathy V. Functional characteristics and tissue distribution pattern of organic cation transporter 2 (OCTN2), an organic cation/carnitine transporter. J. Pharm. Exp. Ther. 290 (1999) 1482-1492
26. Ohashi R., Tamai I., Yabuuchi H., Nezu J.I., Oku A., Sai Y., Shimane M., and Tsuji A. Na (+)-dependent carnitine transport by organic cation transporter (OCTN2): its pharmacological and toxicological relevance. J. Pharmacol. Exp. Ther. 291 (1999) 778-784
27. Wu X., George R.L., Huang W., Wang H., Conway S.J., Leibach F.H., and Ganapathy V. Structural and functional characteristics and tissue distribution pattern of rat OCTN1, an organic cation transporter, cloned from placenta. Biochim. Biophys. Acta 1466 (2000) 315-327
28. Tein I., and Xie Z.W. The human plasmalemmal carnitine transporter defect is expressed in cultured lymphoblasts: a new, rapid non-invasive diagnostic method for diagnosis. Clin. Chim. Acta 252 (1996) 201-204
29. Tein I., Bukovac W.S., and Xie Z.W. Characterization of the human plasmalemmal carnitine transporter in cultured skin fibroblasts. Arch. Biochem. Biophys. 329 (1996) 145-155
30. Lamhonwah A.M., and Tein I. GFP-human high-affinity carnitine transporter OCTN2 protein: subcellular localization and functional restoration of carnitine uptake in mutant cell lines with carnitine transporter defect. Biochem. Biophys. Res. Commun. 264 (1999) 909-914
31. Stanley C.A., Hale D.E., Berry G.T., Deleeuw S., Boxer J., and Bonnefont J.P. Brief report: a deficiency of carnitine-acylcarnitine translocase in the inner mitochondrial membrane. N. Engl. J. Med. 327 (1992) 19-23
32. Murthy M.S., and Pande S.V. Malonyl-CoA binding site and the overt carnitine palmitoyl-transferase activity reside on the opposite sides of the outer mitochondrial membrane. Proc. Natl. Acad. Sci. 84 (1987) 378-382
33. Pande S.V., and Parvin R. Carnitine-acylcarnitine translocase catalyzes an equilibrating unidirectional transport as well. J. Biol. Chem. 255 (1980) 2994-3001
34. Ramsay R.R., and Tubbs P.K. The effects of temperature and some inhibitors on the carnitine exchange system of heart mitochondria. Eur. J. Biochem. 69 (1976) 299-303
35. Porter R.K. Mammalian mitochondrial inner membrane cationic and neutral amino acid carriers. Biochim. Biophys. Acta 1459 (2000) 356-362
36. Indiveri C., Tonazzi A., and Palmieri F. Identification and purification of the carnitine carrier from rat liver mitochondria. Biochim. Biophys. Acta 1020 (1990) 81-86
37. Indiveri C., Tonazzi A., and Palmieri F. The reconstituted carnitine carrier from rat liver mitochondria: evidence for a transport mechanism different from that of the other mitochondrial translocators. Biochim. Biophys. Acta 1189 (1994) 65-73
38. Idell-Wenger J.A. Carnitine: acylcarnitine translocase of rat heart mitochondria. Competition for carnitine uptake by carnitine esters. J. Biol. Chem. 256 (1981) 5597-5603
39. Parvin R., and Pande S.V. Enhancement of mitochondrial carnitine and carnitine acylcarnitine translocase-mediated transport of fatty acids into liver mitochondria under ketogenic conditions. J. Biol. Chem. 254 (1979) 5423-5429
40. Huizing M., Iacobazzi V., Ijlst L., Savelkoul P., Ruitenbeek W., van den Heuvel L., Indiveri C., Smeitink J., Trijbels F., Wanders R., and Palmieri F. Cloning of the human carnitine-acylcarnitine carrier cDNA and identification of the molecular defect in a patient. Am. J. Hum. Genet. 61 (1997) 1239-1245
41. Viggiano L., et al. Assignment of the carnitine/acylcarnitine translocase gene (CACT) to human chromosome band 3p21.31 by in situ hybridization. Cytogenet. Cell. Genet. 79 (1997) 62-63
42. Indiveri C., Iacobazzi V., Giangregorio N., and Palmieri F. Bacterial overexpression, purification, and reconstitution of the carnitine/acylcarnitine carrier from rat liver mitochondria. Biochem. Biophys. Res. Commun. 249 (1998) 589-594
43. Pande S.V., Brivet M., Slama A., Demaugre F., Aufrant C., and Saudubray J.M. Carnitine-acylcarnitine translocase deficiency with severe hypoglycemia and auriculo ventricular block: translocase assay in permeabilized fibroblasts. J. Clin. Invest. 91 (1993) 1247-1252
44. Olpin S.E., Bonham J.R., Downing M., Manning N.J., Pollitt R.J., Sharrard M.J., and Tanner M.S. Carnitine-acylcarnitine translocase deficiency-a mild phenotype. J. Inherit. Metab. Dis. 20 (1997) 714-715
45. Stanley C.A. New genetic defects in mitochondrial fatty acid oxidation and carnitine deficiency. Adv. Pediatr. 34 (1987) 59-88
46. Idell-Wenger J.A., Grotyohann L.W., and Neely J.R. Coenzyme A and carnitine distribution in normal and ischemic hearts. J. Biol. Chem. 253 (1978) 4310-4318
47. Brown N.F., Weis B.C., Husti J.E., Foster D.W., and McGarry J.D. Mitochondrial carnitine palmitoyltransferase I isoform switching in the developing rat heart. J. Biol. Chem. 270 (1995) 8952-8957
48. McGarry J.D., and Brown N.F. The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. Eur. J. Biochem. 244 (1997) 1-14
49. Peltekova V.D., Wintle R.F., Rubin L.A., Amos C.I., Huang Q., Gu X., Newman B., Van Oene M., Cescon D., Greenberg G., Griffiths A.M., St. George-Hyslop P.H., and Siminovitch K.A. Functional variants of OCTN cation transporter genes are associated with Crohn disease. Nat. Genet. 36 (2004) 471-475
50. Mootha V.K., Bunkenborg J., Olsen J.V., Hjerrild M., Wisniewski J.R., Stahl E., Bolouri M.S., Ray H.N., Sihag S., Kamal M., Patterson N., Lander E.S., and Mann M. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115 (2003) 629-640
51. Tamai I., Nakanishi T., Kobayashi D., China K., Kosugi Y., Nezu J., Sai Y., and Tsuji A. Involvement of OCTN1 (SLC22A4) in pH-dependent transport of organic cations. Mol. Pharm. 1 (2004) 57-66
52. Moser T.L., Kenan D.J., Ashley T.A., Roy J.A., Goodman M.D., Misra U.K., Cheek D.J., and Pizzo S.V. Endothelial cell surface F1-F0 ATP synthase is active in ATP synthesis and is inhibited by angiostatin. Proc. Natl. Acad. Sci. USA. 98 (2001) 6656-6661
53. Grundemann D., Harlfinger S., Golz S., Geerts A., Lazar A., Berkels R., Jung N., Rubbert A., and Schomig E. Discovery of the ergothioneine transporter. Proc. Natl. Acad. Sci. USA. 102 (2005) 5256-5261
54. Chaudiere J., and Ferrari-Iliou R. Intracellular antioxidants: from chemical to biochemical mechanisms. Food Chem. Toxicol. 37 (1999) 949-962
55. Lamhonwah A.M., Skaug J., Scherer S.W., and Tein I. A third human carnitine/organic cation transporter (OCTN3) as a candidate for the 5q31 Crohn's disease locus (IBD5). Biochem. Biophys. Res. Commun. 301 (2003) 98-101
56. Ramsay R.R. The carnitine acyltransferases: modulators of acyl-CoA-dependent reactions. Biochem. Soc. Trans. 28 (2000) 182-186