Human ABCB6 localizes to both the outer mitochondrial membrane and the plasma membrane

Biochemistry

Volumn 46, Issue 33, 2007, Pages 9443-9452

  Paterson, Jill K ^a   Shukla, Suneet ^a   Black, Chelsea M ^a   Tachiwada, Tokushi ^b   Garfield, Susan ^a   Wincovitch, Stephen ^a   Ernst, David N ^c   Agadir, Anissa ^c   Li, Xuelin ^c   Ambudkar, Suresh V ^a   Szakacs, Gergely ^d   Akiyama, Shin Ichi ^b   Gottesman, Michael M ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b KAGOSHIMA UNIVERSITY   (Japan)

^c BD BIOSCIENCES   (United States)

^d INSTITUTE OF ENZYMOLOGY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ATP-BINDING CASSETTE TRANSPORTERS; CYTOTOXIC AGENTS; MITOCHONDRIA;

ADENOSINETRIPHOSPHATE; CONFOCAL MICROSCOPY; PHYSIOLOGY; PORPHYRINS;

CELL MEMBRANES;

ABC TRANSPORTER; ABC TRANSPORTER B6; ABC TRANSPORTER B6 ANTIBODY; CISPLATIN; CYCLOPHOSPHAMIDE; CYTOTOXIC AGENT; DIGITONIN; EPIRUBICIN; FLUOROURACIL; HEMIN; IRON; PACLITAXEL; PHEOPHORBIDE A; PORPHYRIN; PRAZOSIN DERIVATIVE; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ANTIBODY SPECIFICITY; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CENTRIFUGATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIFFERENTIAL CENTRIFUGATION; DRUG CYTOTOXICITY; HOMEOSTASIS; HUMAN; HUMAN CELL; IRON TRANSPORT; MITOCHONDRIAL MEMBRANE; MOLECULAR WEIGHT; PORPHYRIN METABOLISM; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SOLUBILIZATION; TITRIMETRY; WESTERN BLOTTING;

ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TUMOR; CELL MEMBRANE; GLYCOSYLATION; HUMANS; MITOCHONDRIAL MEMBRANES; PROTEIN BINDING;

EID: 34548095406     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700015m     Document Type: Article

References (71)

1. Holland, I. B., Cole, Susan P. C., Kuchler, K., and Higgins, C. F. (2003) ABC Proteins, From Bacteria to Man, Academic Press/Elsevier Science, New York.
2. Dean, M., Rzhetsky, A., and Allikmets, R. (2001) The human ATP-binding cassette (ABC) transporter superfamily, Genome Res. 11, 1156-1166.
3. Gottesman, M. M., and Ambudkar, S. V. (2001) Overview: ABC transporters and human disease, J. Bioenerg. Biomembr. 33, 453-458.
4. Szakacs, G., Paterson, J. K., Ludwig, J. A., Booth-Genthe, C., and Gottesman, M. M. (2006) Targeting multidrug resistance in cancer, Nat. Rev. Drug Discovery 5, 219-234.
5. Dean, M., Fojo, T., and Bates, S. (2005) Tumour stem cells and drug resistance, Nat. Rev. Cancer 5, 275-284.
6. Szakacs, G., Annereau, J. P., Lababidi, S., Shankavaram, U., Arciello, A., Bussey, K. J., Reinhold, W., Guo, Y., Kruh, G. D., Reimers, M., Weinstein, J. N., and Gottesman, M. M. (2004) Predicting drug sensitivity and resistance: profiling ABC transporter genes in cancer cells, Cancer Cell 6, 129-137.
7. Annereau, J. P., Szakacs, G., Tucker, C. J., Arciello, A., Cardarelli, C., Collins, J., Grissom, S., Zeeberg, B. R., Reinhold, W., Weinstein, J. N., Pommier, Y., Paules, R. S., and Gottesman, M. M. (2004) Analysis of ATP-binding cassette transporter expression in drug-selected cell lines by a microarray dedicated to multidrug resistance, Mol. Pharmacol. 66, 1397-1405.
8. Yasui, K., Mihara, S., Zhao, C., Okamoto, H., Saito-Ohara, F., Tomida, A., Funato, T., Yokomizo, A., Naito, S., Imoto, I., Tsuruo, T., and Inazawa, J. (2004) Alteration in copy numbers of genes as a mechanism for acquired drug resistance, Cancer Res. 64, 1403-1410.
9. Park, S., Shimizu, C., Shimoyama, T., Takeda, M., Ando, M., Kohno, T., Katsumata, N., Kang, Y. K., Nishio, K., and Fujiwara, Y. (2006) Gene expression profiling of ATP-binding cassette (ABC) transporters as a predictor of the pathologic response to neoadjuvant chemotherapy in breast cancer patients, Breast Cancer Res. Treat. 99, 9-17.
10. Emadi-Konjin, H. P., Zhang, H., Anandan, V., Sun, D., Schuetz, J., and Furuya, K. N. (2002) Isolation of a genomic clone containing the promoter region of the human ATP binding cassette (ABC) transporter, ABCB6, Biochim. Biophys. Acta 1574, 117-130.
11. Mitsuhashi, N., Miki, T., Senbongi, H., Yokoi, N., Yano, H., Miyazaki, M., Nakajima, N., Iwanaga, T., Yokoyama, Y., Shibata, T., and Seino, S. (2000) MTABC3, a novel mitochondrial ATP-binding cassette protein involved in iron homeostasis, J. Biol. Chem. 275, 17536-17540.
12. Kispal, G., Csere, P., Guiard, B., and Lill, R. (1997) The ABC transporter Atm1p is required for mitochondrial iron homeostasis, FEBS Lett. 418, 346-350.
13. Leighton, J., and Schatz, G. (1995) An ABC transporter in the mitochondrial inner membrane is required for normal growth of yeast, EMBO J. 14, 188-195.
14. Kispal, G., Csere, P., Prohl, C., and Lill, R. (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins, EMBO J. 18, 3981-3989.
15. Krishnamurthy, P. C., Du, G., Fukuda, Y., Sun, D., Sampath, J., Mercer, K. E., Wang, J., Sosa-Pineda, B., Murti, K. G., and Schuetz, J. D. (2006) Identification of a mammalian mitochondrial porphyrin transporter, Nature 443, 586-589.
16. Akiyama, S., Fojo, A., Hanover, J. A., Pastan, I., and Gottesman, M. M. (1985) Isolation and genetic characterization of human KB cell lines resistant to multiple drugs, Somatic Cell Mol. Genet. 11, 117-126.
17. Kornblith, P. L., Smith, B. H., and Leonard, L. A. (1981) Response of cultured human brain tumors to nitrosoureas: correlation with clinical data, Cancer 47, 255-265.
18. Bullard, D. E., Schold, S. C., Jr., Bigner, S. H., and Bigner, D. D. (1981) Growth and chemotherapeutic response in athymic mice of tumors arising from human glioma-derived cell lines, J. Neuropathol. Exp. Neurol. 40, 410-427.
19. Hackett, A. J., Smith, H. S., Springer, E. L., Owens, R. B., Nelson-Rees, W. A., Riggs, J. L., and Gardner, M. B. (1977) Two syngeneic cell lines from human breast tissue: the aneuploid mammary epithelial (Hs578T) and the diploid myoepithelial (Hs578Bst) cell lines, J. Natl. Cancer Inst. 58, 1795-1806.
20. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid, Anal. Biochem. 150, 76-85.
21. Chearwae, W., Anuchapreeda, S., Nandigama, K., Ambudkar, S. V., and Limtrakul, P. (2004) Biochemical mechanism of modulation of human P-glycoprotein (ABCB1) by curcumin I, II, and III purified from turmeric powder, Biochem. Pharmacol. 68, 2043-2052.
22. Paterson, J. K., and Gottesman, M. M. (2007) P-Glycoprotein is not present in mitochondrial membranes, Exp. Cell Res, in press.
23. Storrie, B., and Madden, E. A. (1990) Isolation of subcellular organelles, Methods Enzymol. 182, 203-225.
24. Attardi, G., and Ching, E. (1979) Biogenesis of mitochondrial proteins in HeLa cells, Methods Enzymol. 56, 66-79.
25. Shukla, S., Saini, P., Smriti, Jha, S., Ambudkar, S. V., and Prasad, R. (2003) Functional characterization of Candida albicans ABC transporter Cdr1p, Eukaryotic Cell 2, 1361-1375.
26. Stanley, S., Dias, J. A., D'Arcangelis, D., and Mannella, C. A. (1995) Peptide-specific antibodies as probes of the topography of the voltage-gated channel in the mitochondrial outer membrane of Neurospora crassa, J. Biol. Chem. 270, 16694-16700.
27. Notario, B., Manchado, C., Zamora, M., Mampel, T., and Vinas, O. (2003) Assessment of membrane-bound mammal mitochondrial adenine nucleotide translocase topography by experimental antibodies, Biochemistry 42, 820-828.
28. De Pinto, V., al Jamal, J. A., Benz, R., Genchi, G., and Palmieri, F. (1991) Characterization of SH groups in porin of bovine heart mitochondria. Porin cysteines are localized in the channel walls, Eur. J. Biochem. 202, 903-911.
29. Poot, M., Zhang, Y. Z., Kramer, J. A., Wells, K. S., Jones, L. J., Hanzel, D. K., Lugade, A. G., Singer, V. L., and Haugland, R. P. (1996) Analysis of mitochondrial morphology and function with novel fixable fluorescent stains, J. Histochem. Cytochem. 44, 1363-1372.
30. Clarke, S. (1976) Protein asymmetry in the inner membrane of rat liver mitochondria, J. Biol. Chem. 251, 1354-1363.
31. Dorner, M., Altmann, M., Paabo, S., and Morl, M. (2001) Evidence for import of a lysyl-tRNA into marsupial mitochondria, Mol. Biol. Cell 12, 2688-2698.
32. Dolder, M., Zeth, K., Tittmann, P., Gross, H., Welte, W., and Wallimann, T. (1999) Crystallization of the human, mitochondrial voltage-dependent anion-selective channel in the presence of phospholipids, J. Struct. Biol. 127, 64-71.
33. Song, J., Midson, C., Blachly-Dyson, E., Forte, M., and Colombini, M. (1998) The topology of VDAC as probed by biotin modification, J. Biol. Chem. 273, 24406-24413.
34. Robey, R. W., Steadman, K., Polgar, O., Morisaki, K., Blayney, M., Mistry, P., and Bates, S. E. (2004) Pheophorbide a is a specific probe for ABCG2 function and inhibition, Cancer Res. 64, 1242-1246.
35. Goffeau, A., Park, J., Paulsen, I. T., Jonniaux, J. L., Dinh, T., Mordant, P., and Saier, M. H., Jr. (1997) Multidrug-resistant transport proteins in yeast: complete inventory and phylogenetic characterization of yeast open reading frames with the major facilitator superfamily, Yeast 13, 43-54.
36. Young, L., Leonhard, K., Tatsuta, T., Trowsdale, J., and Langer, T. (2001) Role of the ABC transporter Mdl1 in peptide export from mitochondria, Science 291, 2135-2138.
37. Shirihai, O. S., Gregory, T., Yu, C., Orkin, S. H., and Weiss, M. J. (2000) ABC-me: a novel mitochondrial transporter induced by GATA-1 during erythroid differentiation, EMBO J. 19, 2492-2502.
38. Benz, R. (1985) Porin from bacterial and mitochondrial outer membranes, CRC Crit. Rev. Biochem. 19, 145-190.
39. Csere, P., Lill, R., and Kispal, G. (1998) Identification of a human mitochondrial ABC transporter, the functional orthologue of yeast Atmlp, FEBS Lett. 441, 266-270.
40. Bekri, S., Kispal, G., Lange, H., Fitzsimons, E., Tolmie, J., Lill, R., and Bishop, D. F. (2000) Human ABC7 transporter: gene structure and mutation causing X-linked sideroblastic anemia with ataxia with disruption of cytosolic iron-sulfur protein maturation, Blood 96, 3256-3264.
41. Chloupkova, M., LeBard, L. S., and Koeller, D. M. (2003) MDL1 is a high copy suppressor of ATM1: evidence for a role in resistance to oxidative stress, J. Mol. Biol. 331, 155-165.
42. Shimada, Y., Okuno, S., Kawai, A., Shinomiya, H., Saito, A., Suzuki, M., Omori, Y., Nishino, N., Kanemoto, N., Fujiwara, T., Horie, M., and Takahashi, E. (1998) Cloning and chromosomal mapping of a novel ABC transporter gene (hABC7), a candidate for X-linked sideroblastic anemia with spinocerebellar ataxia, J. Hum. Genet. 43, 115-122.
43. Allikmets, R., Raskind, W. H., Hutchinson, A., Schueck, N. D., Dean, M., and Koeller, D. M. (1999) Mutation of a putative mitochondrial iron transporter gene (ABC7) in X-linked sideroblastic anemia and ataxia (XLSA/A), Hum. Mol. Genet. 8, 743-749.
44. Low, T. Y., Seow, T. K., and Chung, M. C. (2002) Separation of human erythrocyte membrane associated proteins with one-dimensional and two-dimensional gel electrophoresis followed by identification with matrix-assisted laser desorption/ionization-time of flight mass spectrometry, Proteomics 2, 1229-1239.
45. Kakhniashvili, D. G., Bulla, L. A., Jr., and Goodman, S. R. (2004) The human erythrocyte proteome: analysis by ion trap mass spectrometry, Mol Cell Proteomics 3, 501-509.
46. Jitsukawa, K., Suizu, R., and Hidano, A. (1984) Chlorella photosensitization. New phytophotodermatosis, Int. J. Dermatol. 23, 263-268.
47. Millard, T. P., and Hawk, J. L. (2002) Photosensitivity disorders: cause, effect and management, Am. J. Clin. Dermatol. 3, 239-246.
48. Beier, R. C. (1990) Natural pesticides and bioactive components in foods, Rev. Environ. Contam. Toxicol. 113, 47-137.
49. Bowers, A. G. (1999) Phytophotodermatitis, Am. J. Contact Dermatitis 10, 89-93.
50. Jonker, J. W., Buitelaar, M., Wagenaar, E., Van Der, Valk, M. A., Scheffer, G. L., Scheper, R. J., Plosch, T., Kuipers, F., Elferink, R. P., Rosing, H., Beijnen, J. H., and Schinkel, A. H. (2002) The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria, Proc. Natl. Acad. Sci. U.S.A. 99, 15649-15654.
51. Lecha, M. (2003) Erythropoietic protoporphyria, Photodermatol. Photoimmunol. Photomed. 19, 142-146.
52. Sarkany, R. P. (2002) Erythropoietic protoporphyria (EPP) at 40. Where are we now? Photodermatol. Photoimmunol. Photomed. 18, 147-152.
53. Thunell, S., Harper, P., and Bran, A. (2000) Porphyrins, porphyrin metabolism and porphyrias. IV. Pathophysiology of erythyropoietic protoporphyria - diagnosis, care and monitoring of the patient, Scand. J. Clin. Lab. Invest. 60, 581-604.
54. Lill, R., and Neupert, W. (1996) Mechanisms of protein import across the mitochondrial outer membrane, Trends Cell Biol. 6, 56-61.
55. Neupert, W. (1997) Protein import into mitochondria, Annu. Rev. Biochem. 66, 863-917.
56. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence, J. Mol. Biol. 300, 1005-1016.
57. Bannai, H., Tamada, Y., Maruyama, O., Nakai, K., and Miyano, S. (2002) Extensive feature detection of N-terminal protein sorting signals, Bioinformatics 18, 298-305.
58. Hogue, D. L., Liu, L., and Ling, V. (1999) Identification and characterization of a mammalian mitochondrial ATP-binding cassette membrane protein, J. Mol. Biol. 285, 379-389.
59. Graf, S. A., Haigh, S. E., Corson, E. D., and Shirihai, O. S. (2004) Targeting, import, and dimerization of a mammalian mitochondrial ATP binding cassette (ABC) transporter, ABCB10 (ABC-me), J. Biol. Chem. 279, 42954-42963.
60. Rapaport, D. (2003) Finding the right organelle. Targeting signals in mitochondrial outer-membrane proteins, EMBO Rep. 4, 948-952.
61. Rapaport, D., and Neupert, W. (1999) Biogenesis of Tom40, core component of the TOM complex of mitochondria, J. Cell Biol. 146, 321-331.
62. Court, D. A., Kleene, R., Neupert, W., and Lill, R. (1996) Role of the N- and C-termini of porin in import into the outer membrane of Neurospora mitochondria, FEBS Lett. 390, 73-77.
63. Shore, G. C., McBride, H. M., Millar, D. G., Steenaart, N. A., and Nguyen, M. (1995) Import and insertion of proteins into the mitochondrial outer membrane, Eur. J. Biochem. 227, 9-18.
64. Wattenberg, B., and Lithgow, T. (2001) Targeting of C-terminal (tail)-anchored proteins: understanding how cytoplasmic activities are anchored to intracellular membranes, Traffic 2, 66-71.
65. Fritz, S., Rapaport, D., Klanner, E., Neupert, W., and Westermann, B. (2001) Connection of the mitochondrial outer and inner membranes by Fzo1 is critical for organellar fusion, J. Cell Biol. 152, 683-692.
66. Mannella, C. A., Neuwald, A. F., and Lawrence, C. E. (1996) Detection of likely transmembrane beta strand regions in sequences of mitochondrial pore proteins using the Gibbs sampler, J. Bioenerg. Biomembr. 28, 163-169.
67. Tusnady, G. E., and Simon, I. (1998) Principles governing amino acid composition of integral membrane proteins: application to topology prediction, J. Mol. Biol. 283, 489-506.
68. Rost, B. (1996) Predicting one-dimensional protein structure by profile based neural networks, Methods Enzymol. 266, 525-539.
69. Hirokawa, T., Boon-Chieng, S., and Mitaku, S. (1998) SOSUI: classification and secondary structure prediction system for membrane proteins, Bioinformatics 14, 378-379.
70. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes, J. Mol. Biol. 305, 567-580.
71. Ambudkar, S. V., Kim, I. W., Xia, D., and Sauna, Z. E. (2006) The A-loop, a novel conserved aromatic acid subdomain upstream of the Walker A motif in ABC transporters, is critical for ATP binding, FEBS Lett. 580, 1049-1055.