Emerging new paradigms for ABCG transporters

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1791, Issue 7, 2009, Pages 584-593

  Tarr, Paul T ^a   Tarling, Elizabeth J ^b   Bojanic, Dragana D ^b   Edwards, Peter A ^b,c   Baldán, Ángel ^d  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ABC transporter; ABCG; Atherosclerosis; Multidrug resistance; Sitosterolemia; Sterol transporter

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER G1; ABC TRANSPORTER G4; ABC TRANSPORTER G5; ABC TRANSPORTER G8; BREAST CANCER RESISTANCE PROTEIN; CALNEXIN; CARRIER PROTEIN; REGULATOR PROTEIN; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG;

APOPTOSIS; ATHEROSCLEROSIS; BACTERIUM; CELL ORGANELLE; CELL SURVIVAL; CYTOPLASM; DIABETES MELLITUS; EUKARYOTE; GENE CONTROL; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HYPOXIA; INFLAMMATION; LIPID MEMBRANE; MULTIDRUG RESISTANCE; NONHUMAN; NUTRIENT SUPPLY; OBESITY; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; STEROL METABOLISM; VASOCONSTRICTION; VASODILATATION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; LIPOPROTEINS; MICE; MICE, KNOCKOUT;

EUKARYOTA; HOMO SAPIENS; PROKARYOTA;

EID: 67649269578     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.01.007     Document Type: Review

References (115)

1. Higgins C.F. ABC transporters: from microorganisms to man. Annu. Rev. Cell. Biol. 8 (1992) 67-113
2. Dean M., and Allikmets R. Evolution of ATP-binding cassette transporter genes. Curr. Opin. Genet. Dev. 5 (1995) 779-785
3. Dawson R.J., and Locher K.P. Structure of a bacterial multidrug ABC transporter. Nature 443 (2006) 180-185
4. Borst P., and Elferink R.O. Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 71 (2002) 537-592
5. Savary S., Denizot F., Luciani M., Mattei M., and Chimini G. Molecular cloning of a mammalian ABC transporter homologous to Drosophila white gene. Mamm. Genome 7 (1996) 673-676
6. Chen H., Rossier C., Lalioti M.D., Lynn A., Chakravarti A., Perrin G., and Antonarakis S.E. Cloning of the cDNA for a human homologue of the Drosophila white gene and mapping to chromosome 21q22.3. Am. J. Hum. Genet. 59 (1996) 66-75
7. Croop J.M., Tiller G.E., Fletcher J.A., Lux M.L., Raab E., Goldenson D., Son D., Arciniegas S., and Wu R.L. Isolation and characterization of a mammalian homolog of the Drosophila white gene. Gene 185 (1997) 77-85
8. Baldan A., Tarr P., Lee R., and Edwards P.A. ATP-binding cassette transporter G1 and lipid homeostasis. Curr. Opin. Lipidol. 17 (2006) 227-232
9. Venkateswaran A., Laffitte B.A., Joseph S.B., Mak P.A., Wilpitz D.C., Edwards P.A., and Tontonoz P. Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXR alpha. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 12097-12102
10. Venkateswaran A., Repa J.J., Lobaccaro J.M., Bronson A., Mangelsdorf D.J., and Edwards P.A. Human white/murine ABC8 mRNA levels are highly induced in lipid-loaded macrophages. A transcriptional role for specific oxysterols. J. Biol. Chem. 275 (2000) 14700-14707
11. Ulven S.M., Dalen K.T., Gustafsson J.A., and Nebb H.I. Tissue-specific autoregulation of the LXRalpha gene facilitates induction of apoE in mouse adipose tissue. J. Lipid Res. 45 (2004) 2052-2062
12. Nakamura K., Kennedy M.A., Baldan A., Bojanic D.D., Lyons K., and Edwards P.A. Expression and regulation of multiple murine ATP-binding cassette transporter G1 mRNAs/isoforms that stimulate cellular cholesterol efflux to high density lipoprotein. J. Biol. Chem. 279 (2004) 45980-45989
13. Klucken J., Buchler C., Orso E., Kaminski W.E., Porsch-Ozcurumez M., Liebisch G., Kapinsky M., Diederich W., Drobnik W., Dean M., Allikmets R., and Schmitz G. ABCG1 (ABC8), the human homolog of the Drosophila white gene, is a regulator of macrophage cholesterol and phospholipid transport. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 817-822
14. Sabol S.L., Brewer Jr. H.B., and Santamarina-Fojo S. The human ABCG1 gene: identification of LXR response elements that modulate expression in macrophages and liver. J. Lipid Res. 46 (2005) 2151-2167
15. Kennedy M.A., Venkateswaran A., Tarr P.T., Xenarios I., Kudoh J., Shimizu N., and Edwards P.A. Characterization of the human ABCG1 gene: liver X receptor activates an internal promoter that produces a novel transcript encoding an alternative form of the protein. J. Biol. Chem. 276 (2001) 39438-39447
16. Kennedy M.A., Barrera G.C., Nakamura K., Baldan A., Tarr P.T., Fishbein M.C., Frank J.S., Francone O., and Edwards P.A. ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation. Cell. Metab. 1 (2005) 121-131
17. Vaughan A.M., and Oram J.F. ABCG1 redistributes cell cholesterol to domains removable by high density lipoprotein but not by lipid-depleted apolipoproteins. J. Biol. Chem. 280 (2005) 30150-30157
18. Kobayashi A., Takanezawa Y., Hirata T., Shimizu Y., Misasa K., Kioka N., Arai H., Ueda K., and Matsuo M. Efflux of sphingomyelin, cholesterol, and phosphatidylcholine by ABCG1. J. Lipid. Res. 47 (2006) 1791-1802
19. Gelissen I.C., Harris M., Rye K.A., Quinn C., Brown A.J., Kockx M., Cartland S., Packianathan M., Kritharides L., and Jessup W. ABCA1 and ABCG1 synergize to mediate cholesterol export to apoA-I. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 534-540
20. Lorkowski S., Kratz M., Wenner C., Schmidt R., Weitkamp B., Fobker M., Reinhardt J., Rauterberg J., Galinski E.A., and Cullen P. Expression of the ATP-binding cassette transporter gene ABCG1 (ABC8) in Tangier disease. Biochem. Biophys. Res. Commun. 283 (2001) 821-830
21. Engel T., Kannenberg F., Fobker M., Nofer J.R., Bode G., Lueken A., Assmann G., and Seedorf U. Expression of ATP binding cassette-transporter ABCG1 prevents cell death by transporting cytotoxic 7beta-hydroxycholesterol. FEBS Lett. 581 (2007) 1673-1680
22. Tarr P.T., and Edwards P.A. ABCG1 and ABCG4 are coexpressed in neurons and astrocytes of the CNS and regulate cholesterol homeostasis through SREBP-2. J. Lipid Res. 49 (2008) 169-182
23. Wang N., Ranalletta M., Matsuura F., Peng F., and Tall A.R. LXR-induced redistribution of ABCG1 to plasma membrane in macrophages enhances cholesterol mass efflux to HDL. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 1310-1316
24. Xie Q., Engel T., Schnoor M., Niehaus J., Hofnagel O., Buers I., Cullen P., Seedorf U., Assmann G., and Lorkowski S. Cell surface localization of ABCG1 does not require LXR activation. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 143-144 [author reply e145]
25. Wang N., Lan D., Chen W., Matsuura F., and Tall A.R. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 9774-9779
26. Sankaranarayanan S., Oram J.F., Asztalos B.F., Vaughan A.M., Lund-Katz S., Adorni M.P., Phillips M.C., and Rothblat G.H. Effects of acceptor composition and mechanism of ABCG1-mediated cellular free cholesterol efflux. J. Lipid Res. (2008)
27. Vaughan A.M., and Oram J.F. ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL. J. Lipid Res. 47 (2006) 2433-2443
28. Baldan A., Tarr P., Vales C.S., Frank J., Shimotake T.K., Hawgood S., and Edwards P.A. Deletion of the transmembrane transporter ABCG1 results in progressive pulmonary lipidosis. J. Biol. Chem. 281 (2006) 29401-29410
29. Burgess B.L., Parkinson P.F., Racke M.M., Hirsch-Reinshagen V., Fan J., Wong C., Stukas S., Theroux L., Chan J.Y., Donkin J., Wilkinson A., Balik D., Christie B., Poirier J., Lutjohann D., Demattos R.B., and Wellington C.L. ABCG1 influences the brain cholesterol biosynthetic pathway but does not affect amyloid precursor protein or apolipoprotein E metabolism in vivo. J. Lipid Res. 49 (2008) 1254-1267
30. Terasaka N., Yu S., Yvan-Charvet L., Wang N., Mzhavia N., Langlois R., Pagler T., Li R., Welch C.L., Goldberg I.J., and Tall A.R. ABCG1 and HDL protect against endothelial dysfunction in mice fed a high-cholesterol diet. J. Clin. Invest. 118 (2008) 3701-3713
31. Karten B., Campenot R.B., Vance D.E., and Vance J.E. Expression of ABCG1, but not ABCA1, correlates with cholesterol release by cerebellar astroglia. J. Biol. Chem. 281 (2005) 4049-4057
32. Out R., Jessup W., Le Goff W., Hoekstra M., Gelissen I.C., Zhao Y., Kritharides L., Chimini G., Kuiper J., Chapman M.J., Huby T., Van Berkel T.J., and Van Eck M. Coexistence of foam cells and hypocholesterolemia in mice lacking the ABC transporters A1 and G1. Circ. Res. 102 (2008) 113-120
33. Out R., Hoekstra M., Habets K., Meurs I., de Waard V., Hildebrand R.B., Wang Y., Chimini G., Kuiper J., Van Berkel T.J., and Van Eck M. Combined deletion of macrophage ABCA1 and ABCG1 leads to massive lipid accumulation in tissue macrophages and distinct atherosclerosis at relatively low plasma cholesterol levels. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 258-264
34. Yvan-Charvet L., Ranalletta M., Wang N., Han S., Terasaka N., Li R., Welch C., and Tall A.R. Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J. Clin. Invest. 117 (2007) 3900-3908
35. Adorni M.P., Zimetti F., Billheimer J.T., Wang N., Rader D.J., Phillips M.C., and Rothblat G.H. The roles of different pathways in the release of cholesterol from macrophages. J. Lipid Res. 48 (2007) 2453-2462
36. Wang X., Collins H.L., Ranalletta M., Fuki I.V., Billheimer J.T., Rothblat G.H., Tall A.R., and Rader D.J. Macrophage ABCA1 and ABCG1, but not SR-BI, promote macrophage reverse cholesterol transport in vivo. J. Clin. Invest. 117 (2007) 2216-2224
37. Baldan A., Gomes A.V., Ping P., and Edwards P.A. Loss of ABCG1 results in chronic pulmonary inflammation. J. Immunol. 180 (2008) 3560-3568
38. Wojcik A.J., Skaflen M.D., Srinivasan S., and Hedrick C.C. A critical role for ABCG1 in macrophage inflammation and lung homeostasis. J. Immunol. 180 (2008) 4273-4282
39. Terkeltaub R., Banka C.L., Solan J., Santoro D., Brand K., and Curtiss L.K. Oxidized LDL induces monocytic cell expression of interleukin-8, a chemokine with T-lymphocyte chemotactic activity. Arterioscler. Thromb. 14 (1994) 47-53
40. Wang N., Tabas I., Winchester R., Ravalli S., Rabbani L.E., and Tall A. Interleukin 8 is induced by cholesterol loading of macrophages and expressed by macrophage foam cells in human atheroma. J. Biol. Chem. 271 (1996) 8837-8842
41. Li Y., Schwabe R.F., DeVries-Seimon T., Yao P.M., Gerbod-Giannone M.C., Tall A.R., Davis R.J., Flavell R., Brenner D.A., and Tabas I. Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-alpha and interleukin-6: model of NF-kappaB- and map kinase-dependent inflammation in advanced atherosclerosis. J. Biol. Chem. 280 (2005) 21763-21772
42. Yvan-Charvet L., Welch C., Pagler T.A., Ranalletta M., Lamkanfi M., Han S., Ishibashi M., Li R., Wang N., and Tall A.R. Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation 118 (2008) 1837-1847
43. Zhu X., Lee J.Y., Timmins J.M., Brown J.M., Boudyguina E., Mulya A., Gebre A.K., Willingham M.C., Hiltbold E.M., Mishra N., Maeda N., and Parks J.S. Increased cellular free cholesterol in macrophage-specific Abca1 knock-out mice enhances pro-inflammatory response of macrophages. J. Biol. Chem. 283 (2008) 22930-22941
44. Jury E.C., Flores-Borja F., and Kabouridis P.S. Lipid rafts in T cell signalling and disease. Semin. Cell Dev. Biol. 18 (2007) 608-615
45. Bensinger S.J., Bradley M.N., Joseph S.B., Zelcer N., Janssen E.M., Hausner M.A., Shih R., Parks J.S., Edwards P.A., Jamieson B.D., and Tontonoz P. LXR signaling couples sterol metabolism to proliferation in the acquired immune response. Cell 134 (2008) 97-111
46. Baldan A., Pei L., Lee R., Tarr P., Tangirala R.K., Weinstein M.M., Frank J., Li A.C., Tontonoz P., and Edwards P.A. Impaired development of atherosclerosis in hyperlipidemic Ldlr-/- and ApoE-/- mice transplanted with Abcg1-/- bone marrow. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 2301-2307
47. Terasaka N., Wang N., Yvan-Charvet L., and Tall A.R. High-density lipoprotein protects macrophages from oxidized low-density lipoprotein-induced apoptosis by promoting efflux of 7-ketocholesterol via ABCG1. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 15093-15098
48. Devries-Seimon T., Li Y., Yao P.M., Stone E., Wang Y., Davis R.J., Flavell R., and Tabas I. Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J. Cell Biol. 171 (2005) 61-73
49. Out R., Hoekstra M., Hildebrand R.B., Kruit J.K., Meurs I., Li Z., Kuipers F., Van Berkel T.J., and Van Eck M. Macrophage ABCG1 deletion disrupts lipid homeostasis in alveolar macrophages and moderately influences atherosclerotic lesion development in LDL receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 2295-2300
50. Ranalletta M., Wang N., Han S., Yvan-Charvet L., Welch C., and Tall A.R. Decreased atherosclerosis in low-density lipoprotein receptor knockout mice transplanted with Abcg1-/- bone marrow. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 2308-2315
51. Curtiss L.K. Is two out of three enough for ABCG1?. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 2175-2177
52. Basso F., Amar M.J., Wagner E.M., Vaisman B., Paigen B., Santamarina-Fojo S., and Remaley A.T. Enhanced ABCG1 expression increases atherosclerosis in LDLr-KO mice on a western diet. Biochem. Biophys. Res. Commun. 351 (2006) 398-404
53. Burgess B., Naus K., Chan J., Hirsch-Reinshagen V., Tansley G., Matzke L., Chan B., Wilkinson A., Fan J., Donkin J., Balik D., Tanaka T., Ou G., Dyer R., Innis S., McManus B., Lutjohann D., and Wellington C. Overexpression of human ABCG1 does not affect atherosclerosis in fat-fed ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 1731-1737
54. Out R., Hoekstra M., Meurs I., de Vos P., Kuiper J., Van Eck M., and Van Berkel T.J. Total body ABCG1 expression protects against early atherosclerotic lesion development in mice. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 594-599
55. Hassan H.H., Denis M., Krimbou L., Marcil M., and Genest J. Cellular cholesterol homeostasis in vascular endothelial cells. Can. J. Cardiol. 22 Suppl. B (2006) 35B-40B
56. Mauldin J.P., Srinivasan S., Mulya A., Gebre A., Parks J.S., Daugherty A., and Hedrick C.C. Reduction in ABCG1 in Type 2 diabetic mice increases macrophage foam cell formation. J. Biol. Chem. 281 (2006) 21216-21224
57. Mauldin J.P., Nagelin M.H., Wojcik A.J., Srinivasan S., Skaflen M.D., Ayers C.R., McNamara C.A., and Hedrick C.C. Reduced expression of ATP-binding cassette transporter G1 increases cholesterol accumulation in macrophages of patients with type 2 diabetes mellitus. Circulation 117 (2008) 2785-2792
58. Zhou H., Tan K.C., Shiu S.W., and Wong Y. Determinants of leukocyte adenosine triphosphate-binding cassette transporter G1 gene expression in type 2 diabetes mellitus. Metabolism 57 (2008) 1135-1140
59. Li C., Xu M., and Gu Q. ATP binding cassette transporter G1 gene expression is reduced in type 2 diabetic patients. Endocr. J. (2008)
60. Buchmann J., Meyer C., Neschen S., Augustin R., Schmolz K., Kluge R., Al-Hasani H., Jurgens H., Eulenberg K., Wehr R., Dohrmann C., Joost H.G., and Schurmann A. Ablation of the cholesterol transporter adenosine triphosphate-binding cassette transporter G1 reduces adipose cell size and protects against diet-induced obesity. Endocrinology 148 (2007) 1561-1573
61. Thomassen M.J., Barna B.P., Malur A.G., Bonfield T.L., Farver C.F., Malur A., Dalrymple H., Kavuru M.S., and Febbraio M. ABCG1 is deficient in alveolar macrophages of GM-CSF knockout mice and patients with pulmonary alveolar proteinosis. J. Lipid Res. 48 (2007) 2762-2768
62. Doyle L.A., Yang W., Abruzzo L.V., Krogmann T., Gao Y., Rishi A.K., and Ross D.D. A multidrug resistance transported from human MCF-7 breast cancer cells. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 15665-15670
63. Hardwick L.J., Velamakanni S., and van Veen H.W. The emerging pharmacotherapeutic significance of the breast cancer resistance protein (ABCG2). Br. J. Pharmacol. 151 (2007) 163-174
64. Sarkadi B., Homolya L., Szakacs G., and Varadi A. Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system. Physiol. Rev. 86 (2006) 1179-1236
65. Krishnamurthy P., and Schuetz J.D. Role of ABCG2/BCRP in biology and medicine. Annu. Rev. Pharmacol. Toxicol. 46 (2006) 381-410
66. Bhatia A., Schafer H.J., and Hrycyna C.A. Oligomerization of the human ABC transporter ABCG2: evaluation of the native protein and chimeric dimers. Biochemistry 44 (2005) 10893-10904
67. Xu J., Liu Y., Yang Y., Bates S., and Zhang J.T. Characterization of oligomeric human half-ABC transporter ATP-binding cassette G2. J. Biol. Chem. 279 (2004) 19781-19789
68. Robey R.W., Polgar O., Deeken J., To K.W., and Bates S.E. ABCG2: determining its relevance in clinical drug resistance. Cancer Metastasis Rev. 26 (2007) 39-57
69. Assaraf Y.G. The role of multidrug resistance efflux transporters in antifolate resistance and folate homeostasis. Drug Resist. Updat. 9 (2006) 227-246
70. Zhou S., Morris J.J., Barnes Y., Lan L., Schuetz J.D., and Sorrentino B.P. Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 12339-12344
71. Kim M., Turnquist H., Jackson J., Sgagias M., Yan Y., Gong M., Dean M., Sharp J.G., and Cowan K. The multidrug resistance transporter ABCG2 (breast cancer resistance protein 1) effluxes Hoechst 33342 and is overexpressed in hematopoietc stem cells. Ciln. Cancer Res. 8 (2002) 22-28
72. Scharenberg C.W., Harkey M.A., and Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 99 (2002) 507-512
73. Lechner A., Leech C.A., Abraham E.J., Nolan A.L., and Habener J.F. Nestin-positive progenitor cells derived from adult human pancreatic islets of Langerhans contain side population (SP) cells defined by expression of the ABCG2 (BCRP1) ATP-binding cassette transporter. Biochem. Biophys. Res. Commun. 293 (2002) 670-674
74. Benchaouir R., Rameau P., Decraene C., Dreyfus P., Israeli D., Piétu G., Danos O., and Garcia L. Evidence for a resident subset of cells with SP phenotype in the C2C12 myogenic line: a tool to explore muscle stem cell biology. Exp. Cell Res. 294 (2004) 254-268
75. Zhou S., Zong Y., Ney P.A., Nair G., Stewart C.F., and Sorrentino B.P. Increased expression of the Abcg2 transporter during erythroid maturation plays a role in decreasing cellular protoporphyrin IX levels. Blood 105 (2005) 2571-2576
76. Shane B. Folate chemistry and metabolism. In: Bailey L.B. (Ed). Folate in health and disease (1995), Marcel Dekker, New York 1-22
77. Chen Z.S., Robey R.W., Belinsky M.G., Shchaveleva I., Ren X.Q., Sugimoto Y., Ross D.D., Bates S.E., and Kruh G.D. Transport of methotrexate, methotrexate polyglutamates and 17beta-estradiol 17-(beta-d-glucuronide) by ABCG2: effects of acquired mutations at R482 on methotrexate transport. Cancer Res. 63 (2003) 4048-4054
78. Ifergan I., Shafran A., Jansen G., Hooijberg J.H., Scheffer G.L., and Assaraf Y.G. Folate deprivation results in the loss of breast cancer resistance protein (BCRP/ABCG2) expression. A role for BCRP in cellular folate homeostasis. J. Biol. Chem. 279 (2004) 25527-25534
79. Krishnamurthy P., Ross D.D., Nakanishi T., Bailey-Dell K., Zhou S., Mercer K.E., Sarkadi B., Sorrentino B.P., and Schuetz J.D. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J. Biol. Chem. 279 (2004) 24218-24225
80. Gottesman M.M., Fojo T., and Bates S.E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev., Cancer 2 (2002) 48-58
81. Ross D.D., Karp J.E., Chen T.T., and Doyle L.A. Expression of breast cancer resistance protein in blast cells from patients with acute leukemia. Blood 96 (2000) 365-368
82. Annilo T., Tammur J., Hutchinson A., Rzhetsky A., Dean M., and Allikmets R. Human and mouse orthologs of a new ATP-binding cassette gene, ABCG4. Cytogenet. Cell Genet. 94 (2001) 196-201
83. Oldfield S., Lowry C., Ruddick J., and Lightman S. ABCG4: a novel human white family ABC-transporter expressed in the brain and eye. Biochim. Biophys. Acta 1591 (2002) 175-179
84. Wang N., Yvan-Charvet L., Lutjohann D., Mulder M., Vanmierlo T., Kim T.W., and Tall A.R. ATP-binding cassette transporters G1 and G4 mediate cholesterol and desmosterol efflux to HDL and regulate sterol accumulation in the brain. FASEB J. 22 (2008) 1073-1082
85. Tachikawa M., Watanabe M., Hori S., Fukaya M., Ohtsuki S., Asashima T., and Terasaki T. Distinct spatio-temporal expression of ABCA and ABCG transporters in the developing and adult mouse brain. J. Neurochem. 95 (2005) 294-304
86. Koshiba S., Ito T., Shiota A., Wakabayashi K., Ueda M., Ichinose H., and Ishikawa T. Development of polyclonal antibodies specific to ATP-binding cassette transporters human ABCG4 and mouse Abcg4: site-specific expression of mouse Abcg4 in brain. J. Exp. Ther. Oncol. 6 (2007) 321-333
87. Cserepes J., Szentpetery Z., Seres L., Ozvegy-Laczka C., Langmann T., Schmitz G., Glavinas H., Klein I., Homolya L., Varadi A., Sarkadi B., and Elkind N.B. Functional expression and characterization of the human ABCG1 and ABCG4 proteins: indications for heterodimerization. Biochem. Biophys. Res. Commun. 320 (2004) 860-867
88. Uehara Y., Yamada T., Baba Y., Miura S., Abe S., Kitajima K., Higuchi M.A., Iwamoto T., and Saku K. ATP-binding cassette transporter G4 is highly expressed in microglia in Alzheimer's brain. Brain Res. 1217 (2008) 239-246
89. Berge K.E., Tian H., Graf G.A., Yu L., Grishin N.V., Schultz J., Kwiterovich P., Shan B., Barnes R., and Hobbs H.H. Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. [Comment In: Science. 2000 Dec 1;290(5497):1709-11 UI: 20559920]. Science 290 (2000) 1771-1775
90. Graf G.A., Li W.P., Gerard R.D., Gelissen I., White A., Cohen J.C., and Hobbs H.H. Coexpression of ATP-binding cassette proteins ABCG5 and ABCG8 permits their transport to the apical surface. J. Clin. Invest. 110 (2002) 659-669
91. Graf G.A., Yu L., Li W.-P., Gerard R., Tuma P.L., Cohen J.C., and Hobbs H.H. ABCG5 and ABCG8 are obligate heterodimers for protein trafficking and biliary cholesterol excretion. J. Biol. Chem. 278 (2003) 48275-48282
92. Gaudet R., and Wiley D.C. Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J. 20 (2001) 4964-4972
93. Zhang D.W., Graf G.A., Gerard R.D., Cohen J.C., and Hobbs H.H. Functional asymmetry of nucleotide-binding domains in ABCG5 and ABCG8. J. Biol. Chem. 281 (2006) 4507-4516
94. Yu L., Li-Hawkins J., Hammer R.E., Berge K.E., Horton J.D., Cohen J.C., and Hobbs H.H. Overexpression of ABCG5 and ABCG8 promotes biliary cholesterol secretion and reduces fractional absorption of dietary cholesterol. J. Clin. Invest. 110 (2002) 671-680
95. Yu L., Hammer R.E., Li-Hawkins J., Von Bergmann K., Lutjohann D., Cohen J.C., and Hobbs H.H. Disruption of Abcg5 and Abcg8 in mice reveals their crucial role in biliary cholesterol secretion. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 16237-16242
96. Wilund K.R., Yu L., Xu F., Hobbs H.H., and Cohen J.C. High-level expression of ABCG5 and ABCG8 attenuates diet-induced hypercholesterolemia and atherosclerosis in Ldlr-/- mice. J. Lipid Res. 45 (2004) 1429-1436
97. Biddinger S.B., Haas J.T., Yu B.B., Bezy O., Jing E., Zhang W., Unterman T.G., Carey M.C., and Kahn C.R. Hepatic insulin resistance directly promotes formation of cholesterol gallstones. Nat. Med. 14 (2008) 778-782
98. Wang J., Sun F., Zhang D.W., Ma Y., Xu F., Belani J.D., Cohen J.C., Hobbs H.H., and Xie X.S. Sterol transfer by ABCG5 and ABCG8: in vitro assay and reconstitution. J. Biol. Chem. 281 (2006) 27894-27904
99. Wang J., Zhang D.W., Lei Y., Xu F., Cohen J.C., Hobbs H.H., and Xie X.S. Purification and reconstitution of sterol transfer by native mouse ABCG5 and ABCG8. Biochemistry 47 (2008) 5194-5204
100. Morgan T.H. Sex-limited inheritance in Drosophila. Science 32 (1910) 120-122
101. Sullivan D.T., and Sullivan M.C. Transport defects as the physiological basis for eye color mutants of Drosophila melanogaster. Biochem. Genet. 13 (1975) 603-613
102. Ewart G.D., and Howells A.J. ABC transporters involved in transport of eye pigment precursors in Drosophila melanogaster. Methods Enzymol. 292 (1998) 213-224
103. Sullivan D.T., Bell L.A., Paton D.R., and Sullivan M.C. Purine transport by malpighian tubules of pteridine-deficient eye color mutants of Drosophila melanogaster. Biochem. Genet. 17 (1979) 565-573
104. Sullivan D.T., Bell L.A., Paton D.R., and Sullivan M.C. Genetic and functional analysis of tryptophan transport in Malpighian tubules of Drosophila. Biochem. Genet. 18 (1980) 1109-1130
105. Zhang S.D., and Odenwald W.F. Misexpression of the white (w) gene triggers male-male courtship in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 5525-5529
106. Lloyd V.K., Sinclair D.A., Alperyn M., and Grigliatti T.A. Enhancer of garnet/deltaAP-3 is a cryptic allele of the white gene and identifies the intracellular transport system for the white protein. Genome 45 (2002) 296-312
107. Sanchez-Fernandez R., Davies T.G., Coleman J.O., and Rea P.A. The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J. Biol. Chem. 276 (2001) 30231-30244
108. Verrier P.J., Bird D., Burla B., Dassa E., Forestier C., Geisler M., Klein M., Kolukisaoglu U., Lee Y., Martinoia E., Murphy A., Rea P.A., Samuels L., Schulz B., Spalding E.J., Yazaki K., and Theodoulou F.L. Plant ABC proteins-a unified nomenclature and updated inventory. Trends Plant Sci. 13 (2008) 151-159
109. Bird D., Beisson F., Brigham A., Shin J., Greer S., Jetter R., Kunst L., Wu X., Yephremov A., and Samuels L. Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J. 52 (2007) 485-498
110. Panikashvili D., Savaldi-Goldstein S., Mandel T., Yifhar T., Franke R.B., Hofer R., Schreiber L., Chory J., and Aharoni A. The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol. 145 (2007) 1345-1360
111. P.T. Tarr, Identification of a novel function for the ATP binding cassette transporters G1 and G4 in regulating intracellular cholesterol homeostasis, PhD Thesis, UCLA (2008) pp 165-168.
112. Heringa J. Two strategies for sequence comparison: profile-preprocessed and secondary structure-induced multiple alignment. Comput. Chem. 23 (1999) 341-364
113. Pearson W.R. Effective protein sequence comparison. Methods Enzymol. 266 (1996) 227-258
114. Campanella J.J., Bitincka L., and Smalley J. MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4 (2003) 29
115. Ronquist F., and Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003) 1572-1574