The monocarboxylate transporter family-Structure and functional characterization

IUBMB Life

Volumn 64, Issue 1, 2012, Pages 1-9

  Halestrap, Andrew P ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

basigin; embigin; lactate; MCT1; MCT2; MCT3; MCT4; MCT8; metabolism; pyruvate; thyroid hormone

Indexed keywords

4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; AROMATIC AMINO ACID; CD147 ANTIGEN; IMMUNOGLOBULIN; MONOCARBOXYLATE TRANSPORTER 1; MONOCARBOXYLATE TRANSPORTER 10; MONOCARBOXYLATE TRANSPORTER 2; MONOCARBOXYLATE TRANSPORTER 3; MONOCARBOXYLATE TRANSPORTER 4; MONOCARBOXYLATE TRANSPORTER 8; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL MEMBRANE; HUMAN; HYDROPHOBICITY; IMMUNOFLUORESCENCE MICROSCOPY; MUTAGENESIS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS;

ANIMALS; CARBOXYLIC ACIDS; CELL MEMBRANE; HUMANS; MONOCARBOXYLIC ACID TRANSPORTERS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

MAMMALIA;

EID: 84855444042     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.573     Document Type: Review

References (51)

1. Poole, R. C., and, Halestrap, A. P., (1993) Transport of lactate and other monocarboxylates across mammalian plasma membranes. Am. J. Physiol. 264, C761-C782. (Pubitemid 23118095)
2. Halestrap, A. P., and, Meredith, D., (2004) The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch. 447, 619-628. (Pubitemid 38241446)
3. Halestrap, A. P., and, Price, N. T., (1999) The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem. J. 343, 281-299. (Pubitemid 29511759)
4. Meredith, D., and, Christian, H. C., (2008) The SLC16 monocaboxylate transporter family. Xenobiotica 38, 1072-1106.
5. Kim, D. K., Kanai, Y., Chairoungdua, A., Matsuo, H., Cha, S. H., and, Endou, H., (2001) Expression cloning of a Na+-independent aromatic amino acid transporter with structural similarity to H+/monocarboxylate transporters. J. Biol. Chem. 276, 17221-17228.
6. Friesema, E. C. H., Ganguly, S., Abdalla, A., Manning Fox, J. E., Halestrap, A. P., and, Visser, T. J., (2003) Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J. Biol. Chem. 278, 40128-40135. (Pubitemid 37248580)
7. Ganapathy, V., Thangaraju, M., Gopal, E., Martin, P., Itagaki, S., et al. (2008) Sodium-coupled monocarboxylate transporters in normal tissues and in cancer. AAPS J. 10, 193-199.
8. Halestrap, A. P., and, Wilson, M. C., (2011) The monocarboxylate transporter family-role and regulation. IUBMB Life, following review.
9. Halestrap, A. P., and, Denton, R. M., (1974) Specific inhibition of pyruvate transport in rat liver mitochondria and human erythrocytes by α-cyano-4-hydroxycinnamate. Biochem. J. 138, 313-316.
10. Deuticke, B., (1982) Monocarboxylate transport in erythrocytes. J. Membr. Biol. 70, 89-103. (Pubitemid 13224951)
11. Poole, R. C., and, Halestrap, A. P., (1994) N-Terminal protein sequence analysis of the rabbit erythrocyte lactate transporter suggests identity with the cloned monocarboxylate transport protein MCT1. Biochem. J. 303, 755-759. (Pubitemid 24326007)
12. Kim-Garcia, C., Goldstein, J. L., Pathak, R. K., Anderson, R. G. W., and, Brown, M. S., (1994) Molecular characterization of a membrane transporter for lactate, pyruvate, and other monocarboxylates-implications for the Cori cycle. Cell 76, 865-873. (Pubitemid 24085324)
13. Carpenter, L., and, Halestrap, A. P., (1994) The kinetics, substrate and inhibitor specificity of the lactate transporter of Ehrlich-Lettre tumour cells studied with the intracellular pH indicator BCECF. Biochem. J. 304, 751-760.
14. Bröer, S., Schneider, H. P., Bröer, A., Rahman, B., Hamprecht, B., and, Deitmer, J. W., (1998) Characterization of the monocarboxylate transporter 1 expressed in Xenopus laevis oocytes by changes in cytosolic pH. Biochem. J. 333, 167-174. (Pubitemid 28342506)
15. Manning Fox, J. E., Meredith, D., and, Halestrap, A. P., (2000) Characterisation of human monocarboxylate transporter 4 substantiates its role in lactic acid efflux from skeletal muscle. J. Physiol. 529, 285-293. (Pubitemid 32040847)
16. Yoon, H. Y., Fanelli, A., Grollman, E. F., and, Philp, N. J., (1997) Identification of a unique monocarboxylate transporter (MCT3) in retinal pigment epithelium. Biochem. Biophys. Res. Commun. 234, 90-94. (Pubitemid 27267538)
17. Murray, C. M., Hutchinson, R., Bantick, J. R., Belfield, G. P., Benjamin, A. D., et al. (2005) Monocarboxylate transporter MCT1 is a target for immunosuppression. Nat. Chem. Biol. 1, 371-376.
18. Guile, S. D., Banticka, J. R., Cheshire, D. R., Cooper, M. E., Davis, A. M., et al. (2006) Potent blockers of the monocarboxylate transporter MCT1: novel immunomodulatory compounds. Bioorg. Medicinal. Chem. Lett. 16, 2260-2265. (Pubitemid 43351091)
19. Ovens, M. J., Manoharan, C., Wilson, M. C., Murray, C. M., and, Halestrap, A. P., (2010) The inhibition of monocarboxylate transporter 2 (MCT2) by AR-C155858 is modulated by the associated ancillary protein. Biochem. J. 431, 217-225.
20. Vinnakota, K. C., and, Beard, D. A., (2011) Kinetic analysis and design of experiments to identify the catalytic mechanism of the monocarboxylate transporter isoforms 4 and 1. Biophys. J. 100, 369-380.
21. Manoharan, C., Wilson, M. C., Sessions, R. B., and, Halestrap, A. P., (2006) The role of charged residues in the TMs of monocarboxylate transporter 1 and its ancillary protein basigin in determining plasma membrane expression and catalytic activity. Mol. Membr. Biol. 23, 486-498. (Pubitemid 44837734)
22. Wilson, M. C., Meredith, D., Bunnun, C., Sessions, R. B., and, Halestrap, A. P., (2009) Studies on the DIDS binding site of monocarboxylate transporter 1 suggest a homology model of the open conformation and a plausible translocation cycle. J. Biol. Chem. 284, 20011-20021.
23. Edlund, G. L., and, Halestrap, A. P., (1988) The kinetics of transport of lactate and pyruvate into rat hepatocytes. Evidence for the presence of a specific carrier similar to that in erythrocytes. Biochem. J. 249, 117-126.
24. Poole, R. C., Halestrap, A. P., Price, S. J., and, Levi, A. J., (1989) The kinetics of transport of lactate and pyruvate into isolated cardiac myocytes from guinea pig-kinetic evidence for the presence of a carrier distinct from that in erythrocytes and hepatocytes. Biochem. J. 264, 409-418. (Pubitemid 20024509)
25. Garcia, C. K., Brown, M. S., Pathak, R. K., and, Goldstein, J. L., (1995) cDNA cloning of MCT2, a second monocarboxylate transporter expressed in different cells than MCT1. J. Biol. Chem. 270, 1843-1849.
26. Bröer, S., Bröer, A., Schneider, H.-P., Stegen, C., Halestrap, A. P., and, Deitmer, J. W., (1999) Characterisation of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes. Biochem. J. 341, 529-535. (Pubitemid 29389181)
27. Wilson, M. C., Meredith, D., Manning Fox, J. E., Manoharan, C., Davies, A. J., and, Halestrap, A. P., (2005) Basigin (CD147) is the target for organomercurial inhibition of monocarboxylate transporter isoforms 1 and 4-the ancillary protein for the insensitive MCT2 is embigin (Gp70). J. Biol. Chem. 280, 27213-27221. (Pubitemid 41040760)
28. Jackson, V. N., Price, N. T., Carpenter, L., and, Halestrap, A. P., (1997) Cloning of the monocarboxylate transporter isoform MCT2 from rat testis provides evidence that expression in tissues is species-specific and may involve post-transcriptional regulation. Biochem. J. 324, 447-453. (Pubitemid 27267986)
29. Bergersen, L., Waerhaug, O., Helm, J., Thomas, M., Laake, P., et al. (2001) A novel postsynaptic density protein: the monocarboxylate transporter MCT2 is co-localized with delta-glutamate receptors in postsynaptic densities of parallel fiber-Purkinje cell synapses. Exp. Brain Res. 136, 523-534. (Pubitemid 32193853)
30. Bergersen, L. H., (2007) Is lactate food for neurons? Comparison of monocarboxylate transporter subtypes in brain and muscle. Neuroscience 145, 11-19. (Pubitemid 46237686)
31. Grollman, E. F., Philp, N. J., McPhie, P., Ward, R. D., and, Sauer, B., (2000) Determination of transport kinetics of chick MCT3 monocarboxylate transporter from retinal pigment epithelium by expression in genetically modified yeast. Biochemistry 39, 9351-9357. (Pubitemid 30626326)
32. Philp, N., Chu, P., Pan, T. C., Zhang, R. Z., Chu, M. L., et al. (1995) Developmental expression and molecular cloning of REMP, a novel retinal epithelial membrane protein. Exp. Cell Res. 219, 64-73.
33. Philp, N. J., Yoon, H., and, Grollman, E. F., (1998) Monocarboxylate transporter MCT1 is located in the apical membrane and MCT3 in the basal membrane of rat RPE-rapid communication. Am. J. Physiol. 43, R1824-R1828.
34. Bergersen, L., Johannsson, E., Veruki, M. L., Nagelhus, E. A., Halestrap, A., et al. (1999) Cellular and subcellular expression of monocarboxylate transporters in the pigment epithelium and retina of the rat. Neuroscience 90, 319-331. (Pubitemid 29096476)
35. Price, N. T., Jackson, V. N., and, Halestrap, A. P., (1998) Cloning and sequencing of four new mammalian monocarboxylate transporter (MCT) homologues confirms the existence of a transporter family with an ancient past. Biochem. J. 329, 321-328. (Pubitemid 28040795)
36. Wilson, M. C., Jackson, V. N., Heddle, C., Price, N. T., Pilegaard, H., et al. (1998) Lactic acid efflux from white skeletal muscle is catalyzed by the monocarboxylate transporter isoform MCT3. J. Biol. Chem. 273, 15920-15926. (Pubitemid 28311355)
37. Hatta, H., Tonouchi, M., Miskovic, D., Wang, Y. X., Heikkila, J. J., and, Bonen, A., (2001) Tissue-specific and isoform-specific changes in MCT1 and MCT4 in heart and soleus muscle during a 1-yr period. Am. J. Physiol. 281, E749-E756.
38. Dimmer, K. S., Friedrich, B., Lang, F., Deitmer, J. W., and, Bröer, S., (2000) The low-affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells. Biochem. J. 350, 219-227.
39. Lafreniere, R. G., Carrel, L., and, Willard, H. F., (1994) A novel transmembrane transporter encoded by the XPCT gene in Xq13.2. Hum. Mol. Genet. 3, 1133-1139. (Pubitemid 24211959)
40. Friesema, E. C., Ganguly, S., Abdalla, A., Manning Fox, J. E., Halestrap, A. P., and, Visser, T. J., (2003) Identification of monocarboxylate transporter 8 as a specific thyroid hormone transporter. J. Biol. Chem. 278, 40128-40135. (Pubitemid 37248580)
41. Visser, W. E., Friesema, E. C., and, Visser, T. J., (2011) Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol. Endocrinol. 25, 1-14.
42. Friesema, E. C., Grueters, A., Biebermann, H., Krude, H., von Moers, A., et al. (2004) Association between mutations in a thyroid hormone transporter and severe X-linked psychomotor retardation. Lancet 364, 1435-1437. (Pubitemid 39370719)
43. Poole, R. C., Sansom, C. E., and, Halestrap, A. P., (1996) Studies of the membrane topology of the rat erythrocyte H+/lactate cotransporter (MCT1) Biochem. J. 320, 817-824. (Pubitemid 27013796)
44. Poole, R. C., and, Halestrap, A. P., (1997) Interaction of the erythrocyte lactate transporter (monocarboxylate transporter 1) with an integral 70-kDa membrane glycoprotein of the immunoglobulin superfamily. J. Biol. Chem. 272, 14624-14628. (Pubitemid 27251724)
45. Galic, S., Schneider, H. P., Bröer, A., Deitmer, J. W., and, Bröer, S., (2003) The loop between helix 4 and helix 5 in the monocarboxylate transporter MCT1 is important for substrate selection and protein stability. Biochem. J. 376, 413-422. (Pubitemid 38010526)
46. Zhou, Y., Guan, L., Freites, J. A., and, Kaback, H. R., (2008) Opening and closing of the periplasmic gate in lactose permease. Proc. Natl. Acad. Sci. USA 105, 3774-3778. (Pubitemid 351723474)
47. Iacono, K. T., Brown, A. L., Greene, M. I., and, Saouaf, S. J., (2007) CD147 immunoglobulin superfamily receptor function and role in pathology. Exp. Mol. Pathol. 83, 283-295. (Pubitemid 350087035)
48. Kirk, P., Wilson, M. C., Heddle, C., Brown, M. H., Barclay, A. N., and, Halestrap, A. P., (2000) CD147 is tightly associated with lactate transporters MCT1 and MCT4 and facilitates their cell surface expression. EMBO J. 19, 3896-3904. (Pubitemid 30608530)
49. Zhao, C., Wilson, M. C., Schuit, F., Halestrap, A. P., and, Rutter, G. A., (2001) Expression and distribution of lactate/monocarboxylate transporter isoforms in pancreatic islets and the exocrine pancreas. Diabetes 50, 361-366. (Pubitemid 32127293)
50. Philp, N. J., Ochrietor, J. D., Rudoy, C., Muramatsu, T., and, Linser, P. J., (2003) Loss of MCT1, MCT3, and MCT4 expression in the retinal pigment epithelium and neural retina of the 5A11/basigin-null mouse. Invest. Ophthalmol. Vis. Sci. 44, 1305-1311. (Pubitemid 36297854)
51. Wilson, M. C., Meredith, D., and, Halestrap, A. P., (2002) Fluorescence resonance energy transfer studies on the interaction between the lactate transporter MCT1 and CD147 provide information on the topology and stoichiometry of the complex in situ. J. Biol. Chem. 277, 3666-3672. (Pubitemid 34953240)