Skip to main content
Log in

Transverse and tangential orientation of predicted transmembrane fragments 4 and 10 from the human multidrug resistance protein (hMRP1/ABCC1) in membrane mimics

  • Original Paper
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

The human multidrug-resistance-associated protein 1 (hMRP1/ABCC1) belongs to the large ATP-binding cassette transporter superfamily. In normal tissues, hMRP1 is involved in tissue defense, whereas, in cancer cells, it is overproduced and contributes to resistance to chemotherapy. We previously investigated the folding properties of the predicted transmembrane fragments (TM) TM16, and TM17 from membrane-spanning domain 2 (MSD2). These TMs folded only partially as an α-helix and were located in the polar headgroup region of detergent micelles used as membrane mimics (Vincent et al. in Biochim Biophys Acta 1768:538–552, 2007; de Foresta et al. in Biochim Biophys Acta 1798:401–414, 2010). We have now extended these studies to TM4 and TM10, from MSD0 and MSD1, respectively. TM10 may be involved in the substrate translocation pathway whereas the role of TM4 is less predictable, because few studies have focused on MSD0, a domain present in some hMRP1 homologs only. Each TM contained a single Trp residue (W142 or W553) acting as an intrinsic fluorescent probe. The location and dynamics of the TMs in dodecylphosphocholine (DPC) or n-dodecyl-β-d-maltoside (DDM) micelles were studied by Trp steady-state and time-resolved fluorescence, including quenching experiments. Overall TM structure was analyzed by far-UV circular dichroism studies in detergent micelles and TFE. TM10 behaved similarly to TM16 and TM17, with an interfacial location in micelles consistent with a possible role in lining the transport pore. By contrast, TM4 behaved like a classical TM fragment with a high α-helical content, and its transmembrane insertion did not require its interaction with other TMs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Scheme 1
Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

hMRP1 (or ABCC1):

Human multidrug-resistance protein 1

BCRP (or ABCG2):

Breast cancer-resistance protein

LTC4 :

Cysteinyl leukotriene C4

E217βG:

Estradiol 17-(β-d-glucuronide)

GSH:

Reduced glutathione

DDM:

n-dodecyl-β-d-maltoside

BrDDM (BrDM in our previous papers):

7,8-Dibromododecylmaltoside

BrUM:

10,11-Dibromoundecanoylmaltoside

DPC:

Dodecylphosphocholine

Cmc:

Critical micellar concentration

NATA:

N-acetyltryptophanamide

TOE:

Tryptophan octyl ester

DMSO:

Dimethylsulfoxide

TFE:

Trifluoroethanol

TFA:

Trifluoroacetic acid

MSD:

Membrane-spanning domain

TM:

Transmembrane fragment

NBD:

Nucleotide-binding domain

MEM:

Maximum entropy method

CD:

Circular dichroism

FWHM:

Full width at half maximum

P3:

K2WL9AL9K2A

P5:

K2CLWL7AL9K2A

P7:

K2CL3WL5AL9K2A

P9:

K2CL5WL3AL9K2A

P11:

K2CL7WLAL9K2A

P13:

K2CL9WL9K2A

TM16:

A1195NRWLAVRLECVGNCIVLFAALFAV1219

mTM16:

A1195NRWLAVRLESVGNSIVLFAALFAV1219

TM17:

A1227GLVGLSVSYSLQVTTYLNWLVRMS1251

mTM17:

K1227GLVGLSVSYSLQVTTYLNWLVRMS1251

TM4:

V132QSSGIMLTFWLVALVCALAILRSK156

mTM4:

V132QSSGIMLTFWLVALVSALAILRSK156

TM10:

S546AVGTFTWVCTPFLVALCTFAVYVT570

mTM10:

S546AVGTFTWVSTPFLVALSTFAVYVT570

(all synthetic peptides were Ac– and –Am)

References

  • Ababou A, Bombarda E (2001) On the involvement of electron transfer reactions in the fluorescence decay kinetics heterogeneity of proteins. Protein Sci 10:2102–2113

    Article  PubMed  CAS  Google Scholar 

  • Abel S, Dupradeau FY, Raman EP, MacKerell AD Jr, Marchi M (2010) Molecular simulations of dodecyl-β-maltoside micelles in water: influence of the headgroup conformation and force field parameters. J Phys Chem B 115:487–499

    Article  PubMed  CAS  Google Scholar 

  • Adams PD, Chen Y, Ma K, Zagorski MG, Sönnichsen FD, McLaughlin ML, Barkley MD (2002) Intramolecular quenching of tryptophan fluorescence by the peptide bond in cyclic hexapeptides. J Am Chem Soc 124:9278–9286

    Article  PubMed  CAS  Google Scholar 

  • Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, Harrell PM, Trinh YT, Zhang Q, Urbatsch IL, Chang G (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323:1718–1722

    Article  PubMed  CAS  Google Scholar 

  • Ambudkar SV, Kimchi-Sarfaty C, Sauna ZE, Gottesman MM (2003) P-glycoprotein: from genomics to mechanism. Oncogene 22:7468–7485

    Article  PubMed  CAS  Google Scholar 

  • Babenko AP, Bryan J (2003) Sur domains that associate with and gate KATP pores define a novel gatekeeper. J Biol Chem 278:41577–41580

    Article  PubMed  CAS  Google Scholar 

  • Bakos E, Evers R, Szakacs G, Tusnady GE, Welker E, Szabo K, de Haas M, van Deemter L, Borst P, Varadi A, Sarkadi B (1998) Functional multidrug resistance protein (MRP1) lacking the N-terminal transmembrane domain. J Biol Chem 273:32167–32175

    Article  PubMed  CAS  Google Scholar 

  • Bernsel A, Viklund H, Falk J, Lindahl E, von Heijne G, Elofsson A (2008) Prediction of membrane-protein topology from first principles. Proc Natl Acad Sci USA 105:7177–7181

    Article  PubMed  CAS  Google Scholar 

  • Bordag N, Keller S (2010) Alpha-helical transmembrane peptides: a “divide and conquer” approach to membrane proteins. Chem Phys Lipids 163:1–26

    Article  PubMed  CAS  Google Scholar 

  • Borst P, Elferink RO (2002) Mammalian ABC transporters in health and disease. Annu Rev Biochem 71:537–592

    Article  PubMed  CAS  Google Scholar 

  • Borst P, Zelcer N, van de Wetering K, Poolman B (2006) On the putative co-transport of drugs by multidrug resistance proteins. FEBS Lett 580:1085–1093

    Article  PubMed  CAS  Google Scholar 

  • Bouhss A, Vincent M, Munier H, Gilles AM, Takahashi M, Bârzu O, Danchin A, Gallay J (1996) Conformational transitions within the calmodulin-binding site of Bordetella pertussis adenylate cyclase studied by time-resolved fluorescence of Trp242 and circular dichroism. Eur J Biochem 237:619–628

    Article  PubMed  CAS  Google Scholar 

  • Bowie JU (2005) Solving the membrane protein folding problem. Nature 438:581–589

    Article  PubMed  CAS  Google Scholar 

  • Buck M (1998) Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q Rev Biophys 31:297–355

    Article  PubMed  CAS  Google Scholar 

  • Chan KW, Zhang H, Logothetis DE (2003) N-terminal transmembrane domain of the SUR controls trafficking and gating of Kir6 channel subunits. EMBO J 22:3833–3843

    Article  PubMed  CAS  Google Scholar 

  • Chang XB (2010) Molecular mechanism of ATP-dependent solute transport by multidrug resistance-associated protein 1. Methods Mol Biol 596:223–249

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Liu B, Barkley MD (1995) Trifluoroethanol quenches indole fluorescence by excited-state proton-transfer. J Am Chem Soc 117:5608–5609

    Article  CAS  Google Scholar 

  • Chen Q, Yang Y, Li L, Zhang JT (2006) The amino terminus of the human multidrug resistance transporter ABCC1 has a U-shaped folding with a gating function. J Biol Chem 281:31152–31163

    Article  PubMed  CAS  Google Scholar 

  • Chenal A, Guijarro JI, Raynal B, Delepierre M, Ladant D (2009) RTX calcium binding motifs are intrinsically disordered in the absence of calcium: implication for protein secretion. J Biol Chem 284:1781–1789

    Article  PubMed  CAS  Google Scholar 

  • Coïc YM, Vincent M, Gallay J, Baleux F, Mousson F, Beswick V, Neumann JM, de Foresta B (2005) Single-spanning membrane protein insertion in membrane mimetic systems: role and localization of aromatic residues. Eur Biophys J 35:27–39

    Article  PubMed  CAS  Google Scholar 

  • Cole SP, Deeley RG (2006) Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol Sci 27:438–446

    Article  PubMed  CAS  Google Scholar 

  • Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AM, Deeley RG (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258:1650–1654

    Article  PubMed  CAS  Google Scholar 

  • Dawson RJ, Locher KP (2006) Structure of a bacterial multidrug ABC transporter. Nature 443:180–185

    Article  PubMed  CAS  Google Scholar 

  • Dawson RJ, Locher KP (2007) Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett 581:935–938

    Article  PubMed  CAS  Google Scholar 

  • de Foresta B, Legros N, Plusquellec D, le Maire M, Champeil P (1996) Brominated detergents as tools to study protein-detergent interactions. Eur J Biochem 241:343–354

    Article  PubMed  Google Scholar 

  • de Foresta B, Gallay J, Sopkova J, Champeil P, Vincent M (1999) Tryptophan octyl ester in detergent micelles of dodecylmaltoside: fluorescence properties and quenching by brominated detergent analogs. Biophys J 77:3071–3084

    Article  PubMed  Google Scholar 

  • de Foresta B, Tortech L, Vincent M, Gallay J (2002) Location and dynamics of tryptophan in transmembrane alpha-helix peptides: a fluorescence and circular dichroism study. Eur Biophys J 31:185–197

    Article  PubMed  CAS  Google Scholar 

  • de Foresta B, Vincent M, Gallay J, Garrigos M (2010) Interaction with membrane mimics of transmembrane fragments 16 and 17 from the human multidrug resistance ABC transporter 1 (hMRP1/ABCC1) and two of their tryptophan variants. Biochim Biophys Acta 1798:401–414

    Article  PubMed  CAS  Google Scholar 

  • Dean M, Allikmets R (2001) Complete characterization of the human ABC gene family. J Bioenerg Biomembr 33:475–479

    Article  PubMed  CAS  Google Scholar 

  • Deeley RG, Cole SP (2006) Substrate recognition and transport by multidrug resistance protein 1 (ABCC1). FEBS Lett 580:1103–1111

    Article  PubMed  CAS  Google Scholar 

  • Deeley RG, Westlake C, Cole SP (2006) Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 86:849–899

    Article  PubMed  CAS  Google Scholar 

  • DeGorter MK, Conseil G, Deeley RG, Campbell RL, Cole SP (2008) Molecular modeling of the human multidrug resistance protein 1 (MRP1/ABCC1). Biochem Biophys Res Commun 365:29–34

    Article  PubMed  CAS  Google Scholar 

  • Di Bartolo ND, Hvorup RN, Locher KP, Booth PJ (2011) In Vitro folding and assembly of the Escherichia coli ATP-binding cassette transporter, BtuCD. J Biol Chem 286:18807–18815

    Google Scholar 

  • Dupuy C, Auvray X, Petipas C, Rico-Lattes I, Lattes A (1997) Anomeric effects on the structure of micelles of alkyl maltosides in water. Langmuir 13:3965–3967

    Article  CAS  Google Scholar 

  • East JM, Lee AG (1982) Lipid selectivity of the calcium and magnesium ion dependent adenosinetriphosphatase, studied with fluorescence quenching by a brominated phospholipid. Biochemistry 21:4144–4151

    Article  PubMed  CAS  Google Scholar 

  • Eftink MR (1991) Fluorescence techniques for studying protein structure. Methods Biochem Anal 35:127–205

    Article  PubMed  CAS  Google Scholar 

  • Engelman DM, Chen Y, Chin CN, Curran AR, Dixon AM, Dupuy AD, Lee AS, Lehnert U, Matthews EE, Reshetnyak YK, Senes A, Popot JL (2003) Membrane protein folding: beyond the two stage model. FEBS Lett 555:122–125

    Article  PubMed  CAS  Google Scholar 

  • Fagerberg L, Jonasson K, von Heijne G, Uhlen M, Berglund L (2010) Prediction of the human membrane proteome. Proteomics 10:1141–1149

    Article  PubMed  CAS  Google Scholar 

  • Faggad A, Darb-Esfahani S, Wirtz R, Sinn B, Sehouli J, Konsgen D, Lage H, Noske A, Weichert W, Buckendahl AC, Budczies J, Muller BM, Elwali NE, Dietel M, Denkert C (2009) Expression of multidrug resistance-associated protein 1 in invasive ovarian carcinoma: implication for prognosis. Histopathology 54:657–666

    Article  PubMed  Google Scholar 

  • Fiedler S, Broecker J, Keller S (2010) Protein folding in membranes. Cell Mol Life Sci 67:1779–1798

    Article  PubMed  CAS  Google Scholar 

  • Flanagan SE, Patch AM, Mackay DJ, Edghill EL, Gloyn AL, Robinson D, Shield JP, Temple K, Ellard S, Hattersley AT (2007) Mutations in ATP-sensitive K+ channel genes cause transient neonatal diabetes and permanent diabetes in childhood or adulthood. Diabetes 56:1930–1937

    Article  PubMed  CAS  Google Scholar 

  • Fletcher JI, Haber M, Henderson MJ, Norris MD (2010) ABC transporters in cancer: more than just drug efflux pumps. Nat Rev Cancer 10:147–156

    Article  PubMed  CAS  Google Scholar 

  • Grant CE, Gao M, DeGorter MK, Cole SP, Deeley RG (2008) Structural determinants of substrate specificity differences between human multidrug resistance protein (MRP) 1 (ABCC1) and MRP3 (ABCC3). Drug Metab Dispos 36:2571–2581

    Article  PubMed  CAS  Google Scholar 

  • Haimeur A, Conseil G, Deeley RG, Cole SP (2004) The MRP-related and BCRP/ABCG2 multidrug resistance proteins: biology, substrate specificity and regulation. Curr Drug Metab 5:21–53

    Article  PubMed  CAS  Google Scholar 

  • Hedin LE, Ojemalm K, Bernsel A, Hennerdal A, Illergard K, Enquist K, Kauko A, Cristobal S, von Heijne G, Lerch-Bader M, Nilsson I, Elofsson A (2010) Membrane insertion of marginally hydrophobic transmembrane helices depends on sequence context. J Mol Biol 396:221–229

    Article  PubMed  CAS  Google Scholar 

  • Hipfner DR, Almquist KC, Leslie EM, Gerlach JH, Grant CE, Deeley RG, Cole SP (1997) Membrane topology of the multidrug resistance protein (MRP). A study of glycosylation-site mutants reveals an extracytosolic NH2 terminus. J Biol Chem 272:23623–23630

    Article  PubMed  CAS  Google Scholar 

  • Holland IB, Blight MA (1999) ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. J Mol Biol 293:381–399

    Article  PubMed  CAS  Google Scholar 

  • Holland IB, Cole SPC, Kuchler K, Higgins CF (2003) ABC proteins: from bacteria to man. Academic Press, London

  • Hollenstein K, Dawson RJ, Locher KP (2007) Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol 17:412–418

    Article  PubMed  CAS  Google Scholar 

  • Hunt JF, Earnest TN, Bousche O, Kalghatgi K, Reilly K, Horvath C, Rothschild KJ, Engelman DM (1997) A biophysical study of integral membrane protein folding. Biochemistry 36:15156–15176

    Article  PubMed  CAS  Google Scholar 

  • Ito K, Olsen SL, Qiu W, Deeley RG, Cole SP (2001) Mutation of a single conserved tryptophan in multidrug resistance protein 1 (MRP1/ABCC1) results in loss of drug resistance and selective loss of organic anion transport. J Biol Chem 276:15616–15624

    Article  PubMed  CAS  Google Scholar 

  • Jasanoff A, Fersht AR (1994) Quantitative determination of helical propensities from trifluoroethanol titration curves. Biochemistry 33:2129–2135

    Article  PubMed  CAS  Google Scholar 

  • Jones PM, O’Mara ML, George AM (2009) ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem Sci 34:520–531

    Article  PubMed  CAS  Google Scholar 

  • Karwatsky J, Daoud R, Cai J, Gros P, Georges E (2003) Binding of a photoaffinity analogue of glutathione to MRP1 (ABCC1) within two cytoplasmic regions (L0 and L1) as well as transmembrane domains 10–11 and 16–17. Biochemistry 42:3286–3294

    Article  PubMed  CAS  Google Scholar 

  • Kast C, Gros P (1997) Topology mapping of the amino-terminal half of multidrug resistance-associated protein by epitope insertion and immunofluorescence. J Biol Chem 272:26479–26487

    Article  PubMed  CAS  Google Scholar 

  • Kast C, Gros P (1998) Epitope insertion favors a six transmembrane domain model for the carboxy-terminal portion of the multidrug resistance-associated protein. Biochemistry 37:2305–2313

    Article  PubMed  CAS  Google Scholar 

  • Kerr ID, Jones PM, George AM (2010) Multidrug efflux pumps: the structures of prokaryotic ATP-binding cassette transporter efflux pumps and implications for our understanding of eukaryotic P-glycoproteins and homologues. Febs J 277:550–563

    Article  PubMed  CAS  Google Scholar 

  • Kinosita K Jr, Kawato S, Ikegami A (1977) A theory of fluorescence polarization decay in membranes. Biophys J 20:289–305

    Article  PubMed  CAS  Google Scholar 

  • Koike K, Oleschuk CJ, Haimeur A, Olsen SL, Deeley RG, Cole SP (2002) Multiple membrane-associated tryptophan residues contribute to the transport activity and substrate specificity of the human multidrug resistance protein, MRP1. J Biol Chem 277:49495–49503

    Article  PubMed  CAS  Google Scholar 

  • Koike K, Conseil G, Leslie EM, Deeley RG, Cole SP (2004) Identification of proline residues in the core cytoplasmic and transmembrane regions of multidrug resistance protein 1 (MRP1/ABCC1) important for transport function, substrate specificity, and nucleotide interactions. J Biol Chem 279:12325–12336

    Article  PubMed  CAS  Google Scholar 

  • Lakowicz JR (2006) Principles of fluorescence spectroscopy, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Lauterwein J, Bösch C, Brown LR, Wüthrich K (1979) Physicochemical studies of the protein-lipid interactions in melittin-containing micelles. Biochim Biophys Acta 556:244–264

    Article  PubMed  CAS  Google Scholar 

  • Le Lan C, Gallay J, Vincent M, Neumann JM, de Foresta B, Jamin N (2010) Structural and dynamic properties of juxta-membrane segments of caveolin-1 and caveolin-2 at the membrane interface. Eur Biophys J 39:307–325

    Article  PubMed  CAS  Google Scholar 

  • Lequin O, Ladram A, Chabbert L, Bruston F, Convert O, Vanhoye D, Chassaing G, Nicolas P, Amiche M (2006) Dermaseptin S9, an alpha-helical antimicrobial peptide with a hydrophobic core and cationic termini. Biochemistry 45:468–480

    Article  PubMed  CAS  Google Scholar 

  • Leslie EM, Deeley RG, Cole SP (2005) Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204:216–237

    Article  PubMed  CAS  Google Scholar 

  • Li SC, Deber CM (1994) A measure of helical propensity for amino acids in membrane environments. Nat Struct Biol 1:368–373

    Article  PubMed  CAS  Google Scholar 

  • Liao MJ, London E, Khorana HG (1983) Regeneration of the native bacteriorhodopsin structure from two chymotryptic fragments. J Biol Chem 258:9949–9955

    PubMed  CAS  Google Scholar 

  • Liu YH, Di YM, Zhou ZW, Mo SL, Zhou SF (2010) Multidrug resistance-associated proteins and implications in drug development. Clin Exp Pharmacol Physiol 37:115–120

    Article  PubMed  CAS  Google Scholar 

  • Livesey AK, Brochon JC (1987) Analyzing the distribution of decay constants in pulse-fluorimetry using the maximum entropy method. Biophys J 52:693–706

    Article  PubMed  CAS  Google Scholar 

  • Locher KP (2009) Review. Structure and mechanism of ATP-binding cassette transporters. Philos Trans R Soc Lond B Biol Sci 364:239–245

    Article  PubMed  CAS  Google Scholar 

  • Loe DW, Almquist KC, Deeley RG, Cole SP (1996) Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J Biol Chem 271:9675–9682

    Article  PubMed  CAS  Google Scholar 

  • London E, Feigenson GW (1981) Fluorescence quenching in model membranes. 1. Characterization of quenching caused by a spin-labeled phospholipid. Biochemistry 20:1932–1938

    Article  PubMed  CAS  Google Scholar 

  • Lundin C, Kim H, Nilsson I, White SH, von Heijne G (2008) Molecular code for protein insertion in the endoplasmic reticulum membrane is similar for N(in)-C(out) and N(out)-C(in) transmembrane helices. Proc Natl Acad Sci USA 105:15702–15707

    Article  PubMed  CAS  Google Scholar 

  • Marquez B, Van Bambeke F (2010) ABC multidrug transporters: target for modulation of drug pharmacokinetics and drug–drug interactions. Curr Drug Targets (in press)

  • Møller JV, le Maire M (1993) Detergent binding as a measure of hydrophobic surface area of integral membrane proteins. J Biol Chem 268:18659–18672

    PubMed  Google Scholar 

  • Montserret R, Aubert-Foucher E, McLeish MJ, Hill JM, Ficheux D, Jaquinod M, van der Rest M, Deleage G, Penin F (1999) Structural analysis of the heparin-binding site of the NC1 domain of collagen XIV by CD and NMR. Biochemistry 38:6479–6488

    Article  PubMed  CAS  Google Scholar 

  • Pace CN, Vajdos F, Fee L, Grimsley G, Gray T (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci 4:2411–2423

    Article  PubMed  CAS  Google Scholar 

  • Pan CP, Barkley MD (2004) Conformational effects on tryptophan fluorescence in cyclic hexapeptides. Biophys J 86:3828–3835

    Article  PubMed  CAS  Google Scholar 

  • Popot JL, Engelman DM (1990) Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29:4031–4037

    Article  PubMed  CAS  Google Scholar 

  • Popot JL, Engelman DM (2000) Helical membrane protein folding, stability, and evolution. Annu Rev Biochem 69:881–922

    Article  PubMed  CAS  Google Scholar 

  • Powl AM, East JM, Lee AG (2005) Heterogeneity in the binding of lipid molecules to the surface of a membrane protein: hot spots for anionic lipids on the mechanosensitive channel of large conductance MscL and effects on conformation. Biochemistry 44:5873–5883

    Article  PubMed  CAS  Google Scholar 

  • Rappa G, Lorico A, Flavell RA, Sartorelli AC (1997) Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res 57:5232–5237

    PubMed  CAS  Google Scholar 

  • Rath A, Tulumello DV, Deber CM (2009) Peptide models of membrane protein folding. Biochemistry 48:3036–3045

    Article  PubMed  CAS  Google Scholar 

  • Rees DC, Johnson E, Lewinson O (2009) ABC transporters: the power to change. Nat Rev Mol Cell Biol 10:218–227

    Article  PubMed  CAS  Google Scholar 

  • Reiersen H, Rees AR (2000) Trifluoroethanol may form a solvent matrix for assisted hydrophobic interactions between peptide side chains. Protein Eng 13:739–743

    Article  PubMed  CAS  Google Scholar 

  • Robey RW, To KK, Polgar O, Dohse M, Fetsch P, Dean M, Bates SE (2009) ABCG2: a perspective. Adv Drug Deliv Rev 61:3–13

    Article  PubMed  CAS  Google Scholar 

  • Roccatano D, Colombo G, Fioroni M, Mark AE (2002) Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: a molecular dynamics study. Proc Natl Acad Sci USA 99:12179–12184

    Article  PubMed  CAS  Google Scholar 

  • Rosenberg MF, Oleschuk CJ, Wu P, Mao Q, Deeley RG, Cole SP, Ford RC (2010) Structure of a human multidrug transporter in an inward-facing conformation. J Struct Biol 170:540–547

    Article  PubMed  CAS  Google Scholar 

  • Rothnie A, Conseil G, Lau AY, Deeley RG, Cole SP (2008) Mechanistic differences between GSH transport by multidrug resistance protein 1 (MRP1/ABCC1) and GSH modulation of MRP1-mediated transport. Mol Pharmacol 74:1630–1640

    Article  PubMed  CAS  Google Scholar 

  • Rouvière N, Vincent M, Craescu CT, Gallay J (1997) Immunosuppressor binding to the immunophilin FKBP59 affects the local structural dynamics of a surface β-strand: time-resolved fluorescence study. Biochemistry 36:7339–7352

    Article  PubMed  Google Scholar 

  • Sharom FJ (2008) ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 9:105–127

    Article  PubMed  CAS  Google Scholar 

  • Sillen A, Engelborghs Y (1998) The correct use of “average” fluorescence parameters. Photochem Photobiol 67:475–486

    CAS  Google Scholar 

  • Situ D, Haimeur A, Conseil G, Sparks KE, Zhang D, Deeley RG, Cole SP (2004) Mutational analysis of ionizable residues proximal to the cytoplasmic interface of membrane spanning domain 3 of the multidrug resistance protein, MRP1 (ABCC1): glutamate 1204 is important for both the expression and catalytic activity of the transporter. J Biol Chem 279:38871–38880

    Article  PubMed  CAS  Google Scholar 

  • Stanley AM, Fleming KG (2008) The process of folding proteins into membranes: challenges and progress. Arch Biochem Biophys 469:46–66

    Article  PubMed  CAS  Google Scholar 

  • Szabo AG, Rayner DM (1980) Fluorescence Decay of Tryptophan Conformers in Aqueous-Solution. J Am Chem Soc 102:554–563

    Article  CAS  Google Scholar 

  • Tortech L, Jaxel C, Vincent M, Gallay J, de Foresta B (2001) The polar headgroup of the detergent governs the accessibility to water of tryptophan octyl ester in host micelles. Biochim Biophys Acta 1514:76–86

    Article  PubMed  CAS  Google Scholar 

  • Tusnady GE, Sarkadi B, Simon I, Varadi A (2006) Membrane topology of human ABC proteins. FEBS Lett 580:1017–1022

    Article  PubMed  CAS  Google Scholar 

  • Vincent M, Gallay J (1991) The interactions of horse heart apocytochrome c with phospholipid vesicles and surfactant micelles: time-resolved fluorescence study of the single tryptophan residue (Trp-59). Eur Biophys J 20:183–191

    Article  PubMed  CAS  Google Scholar 

  • Vincent M, Brochon JC, Merola F, Jordi W, Gallay J (1988) Nanosecond dynamics of horse heart apocytochrome c in aqueous solution as studied by time-resolved fluorescence of the single tryptophan residue (Trp-59). Biochemistry 27:8752–8761

    Article  PubMed  CAS  Google Scholar 

  • Vincent M, Gallay J, Demchenko AP (1995) Solvent relaxation around the excited state of indole: analysis of fluorescence lifetime distributions and spectral shift. J Phys Chem 99:14931–14941

    Article  CAS  Google Scholar 

  • Vincent M, Gilles AM, Li de la Sierra IM, Briozzo P, Barzu O, Gallay J (2000) Nanosecond fluorescence dynamic Stokes shift of tryptophan in a protein matrix. J Phys Chem B 104:11286–11295

    Article  CAS  Google Scholar 

  • Vincent M, Gallay J, Jamin N, Garrigos M, de Foresta B (2007) The predicted transmembrane fragment 17 of the human multidrug resistance protein 1 (MRP1) behaves as an interfacial helix in membrane mimics. Biochim Biophys Acta 1768:538–552

    Article  PubMed  CAS  Google Scholar 

  • Ward A, Reyes CL, Yu J, Roth CB, Chang G (2007) Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc Natl Acad Sci USA 104:19005–19010

    Article  PubMed  CAS  Google Scholar 

  • Westlake CJ, Cole SP, Deeley RG (2005) Role of the NH2-terminal membrane spanning domain of multidrug resistance protein 1/ABCC1 in protein processing and trafficking. Mol Biol Cell 16:2483–2492

    Article  PubMed  CAS  Google Scholar 

  • White SH, von Heijne G (2005) Transmembrane helices before, during, and after insertion. Curr Opin Struct Biol 15:378–386

    Article  PubMed  CAS  Google Scholar 

  • White SH, Wimley WC (1999) Membrane protein folding and stability: physical principles. Annu Rev Biophys Biomol Struct 28:319–365

    Article  PubMed  CAS  Google Scholar 

  • Whitmore L, Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acid Res 32:W668–W673

    Article  PubMed  CAS  Google Scholar 

  • Whitmore L, Wallace BA (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89:392–400

    Article  PubMed  CAS  Google Scholar 

  • Willis KJ, Neugebauer W, Sikorska M, Szabo AG (1994) Probing α-helical secondary structure at a specific site in model peptides via restriction of tryptophan side-chain rotamer conformation. Biophys J 66:1623–1630

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Chen Q, Zhang JT (2002) Structural and functional consequences of mutating cysteine residues in the amino terminus of human multidrug resistance-associated protein 1. J Biol Chem 277:44268–44277

    Article  PubMed  CAS  Google Scholar 

  • Zhang DW, Cole SP, Deeley RG (2002) Determinants of the substrate specificity of multidrug resistance protein 1: role of amino acid residues with hydrogen bonding potential in predicted transmembrane helix 17. J Biol Chem 277:20934–20941

    Article  PubMed  CAS  Google Scholar 

  • Zhang DW, Nunoya K, Vasa M, Gu HM, Cole SP, Deeley RG (2006) Mutational analysis of polar amino acid residues within predicted transmembrane helices 10 and 16 of multidrug resistance protein 1 (ABCC1): effect on substrate specificity. Drug Metab Dispos 34:539–546

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Béatrice de Foresta or Jacques Gallay.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 257 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Foresta, B., Vincent, M., Garrigos, M. et al. Transverse and tangential orientation of predicted transmembrane fragments 4 and 10 from the human multidrug resistance protein (hMRP1/ABCC1) in membrane mimics. Eur Biophys J 40, 1043–1060 (2011). https://doi.org/10.1007/s00249-011-0721-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-011-0721-4

Keywords

Navigation