CoChat
Sign Up
Cited by 29

The DOI matches its Crossref record.

Structural basis of prostaglandin efflux by MRP4

Pourmal, Sergei, Green, Evan, Bajaj, Ruchika, Chemmama, Ilan E., Knudsen, Giselle M., Gupta, Meghna, Sali, Andrej, Cheng, Yifan, Craik, Charles S., Kroetz, Deanna L., Stroud, Robert M.·2024·Nature Structural & Molecular Biology
DOI 10.1038/s41594-023-01176-4

Published version of a preprint

Open this paper in CoChat — free account

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41594-023-01176-4

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 70

  1. Chabowski, D. S., Cohen, K. E., Abu-Hatoum, O., Gutterman, D. D. & Freed, J. K. Crossing signals: bioactive lipids in the microvasculature. Am. J. Physiol. Heart Circ. Physiol. 318, H1185–H1197 (2020). · DOI
  2. Harizi, H. & Gualde, N. The impact of eicosanoids on the crosstalk between innate and adaptive immunity: the key roles of dendritic cells. Tissue Antigens 65, 507–514 (2005). · DOI
  3. Martens, M. D., Fernando, A. S. & Gordon, J. W. A new trick for an old dog? Myocardial-specific roles for prostaglandins as mediators of ischemic injury and repair. Am. J. Physiol. Heart Circ. Physiol. 320, H2169–H2184 (2021). · DOI
  4. Mitchell, J. A. & Kirkby, N. S. Eicosanoids, prostacyclin and cyclooxygenase in the cardiovascular system. Br. J. Pharmacol. 176, 1038–1050 (2019). · DOI
  5. Oyesola, O. O. & Tait Wojno, E. D. Prostaglandin regulation of type 2 inflammation: from basic biology to therapeutic interventions. Eur. J. Immunol. 51, 2399–2416 (2021). · DOI
  6. Vannuccini, S., Bocchi, C., Severi, F. M., Challis, J. R. & Petraglia, F. Endocrinology of human parturition. Ann. Endocrinol. 77, 105–113 (2016). · DOI · Paper page
  7. Zeilhofer, H. U. Prostanoids in nociception and pain. Biochem. Pharmacol. 73, 165–174 (2007). · DOI
  8. Biringer, R. G. The enzymology of the human prostanoid pathway. Mol. Biol. Rep. 47, 4569–4586 (2020). · DOI
  9. Johnson, A. M., Kleczko, E. K. & Nemenoff, R. A. Eicosanoids in cancer: new roles in immunoregulation. Front Pharm. 11, 595498 (2020). · DOI
  10. Mitchell, J. A. et al. Cyclooxygenases and the cardiovascular system. Pharmacol. Ther. 217, 107624 (2021). · DOI
  11. Wang, D., Cabalag, C. S., Clemons, N. J. & DuBois, R. N. Cyclooxygenases and prostaglandins in tumor immunology and microenvironment of gastrointestinal cancer. Gastroenterology 161, 1813–1829 (2021). · DOI
  12. Beaman, J., Prifti, C., Schwarz, E. B. & Sobota, M. Medication to manage abortion and miscarriage. J. Gen. Intern Med 35, 2398–2405 (2020). · DOI
  13. Klimko, P. G. & Sharif, N. A. Discovery, characterization and clinical utility of prostaglandin agonists for the treatment of glaucoma. Br. J. Pharmacol. 176, 1051–1058 (2019). · DOI
  14. Lang, I. M. & Gaine, S. P. Recent advances in targeting the prostacyclin pathway in pulmonary arterial hypertension. Eur. Respir. Rev. 24, 630–641 (2015). · DOI
  15. Lee, O. Y. et al. A comparative study of DA-9601 and misoprostol for prevention of NSAID-associated gastroduodenal injury in patients undergoing chronic NSAID treatment. Arch. Pharm. Res 37, 1308–1316 (2014). · DOI
  16. Stephenson, M. L. & Wing, D. A. Misoprostol for induction of labor. Semin Perinatol. 39, 459–462 (2015). · DOI
  17. Reid, G. et al. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc. Natl Acad. Sci. USA 100, 9244–9249 (2003). · DOI · Paper page
  18. Wen, J. et al. The pharmacological and physiological role of multidrug-resistant protein 4. J. Pharmacol. Exp. Ther. 354, 358–375 (2015). · DOI
  19. Rius, M., Thon, W. F., Keppler, D. & Nies, A. T. Prostanoid transport by multidrug resistance protein 4 (MRP4/ABCC4) localized in tissues of the human urogenital tract. J. Urol. 174, 2409–2414 (2005). · DOI
  20. Tanaka, N., Kawai, J., Hirasawa, N., Mano, N. & Yamaguchi, H. ATP-Binding cassette transporter C4 is a prostaglandin D2 exporter in HMC-1 cells. Prostaglandins Leukot. Ess. Fat. Acids 159, 102139 (2020). · DOI
  21. Kalinski, P. Regulation of immune responses by prostaglandin E2. J. Immunol. 188, 21–28 (2012). · DOI
  22. Kochel, T. J., Reader, J. C., Ma, X., Kundu, N. & Fulton, A. M. Multiple drug resistance-associated protein (MRP4) exports prostaglandin E2 (PGE2) and contributes to metastasis in basal/triple negative breast cancer. Oncotarget 8, 6540–6554 (2017). · DOI
  23. Zelcer, N. et al. Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem. J. 371, 361–367 (2003). · DOI · Paper page
  24. Chen, Z. S., Lee, K. & Kruh, G. D. Transport of cyclic nucleotides and estradiol 17-b-d-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine. J. Biol. Chem. 276, 33747–33754 (2001). · DOI
  25. Hara, Y. et al. Inhibition of MRP4 prevents and reverses pulmonary hypertension in mice. J. Clin. Invest. 121, 2888–2897 (2011). · DOI
  26. Decouture, B. et al. Impaired platelet activation and cAMP homeostasis in MRP4-deficient mice. Blood 126, 1823–1830 (2015). · DOI
  27. Li, C. et al. Spatiotemporal coupling of cAMP transporter to CFTR chloride channel function in the gut epithelia. Cell 131, 940–951 (2007). · DOI
  28. Moon, C. et al. Compartmentalized accumulation of cAMP near complexes of multidrug resistance protein 4 (MRP4) and cystic fibrosis transmembrane conductance regulator (CFTR) contributes to drug-induced diarrhea. J. Biol. Chem. 290, 11246–11257 (2015). · DOI
  29. Chen, Z. S. et al. Analysis of methotrexate and folate transport by multidrug resistance protein 4 (ABCC4): MRP4 is a component of the methotrexate efflux system. Cancer Res. 62, 3144–3150 (2002).
  30. Ci, L. et al. Involvement of MRP4 (ABCC4) in the luminal efflux of ceftizoxime and cefazolin in the kidney. Mol. Pharmacol. 71, 1591–1597 (2007). · DOI
  31. Imaoka, T. et al. Functional involvement of multidrug resistance-associated protein 4 (MRP4/ABCC4) in the renal elimination of the antiviral drugs adefovir and tenofovir. Mol. Pharmacol. 71, 619–627 (2007). · DOI
  32. Kohler, J. J. et al. Tenofovir renal proximal tubular toxicity is regulated by OAT1 and MRP4 transporters. Lab. Invest. 91, 852–858 (2011). · DOI
  33. Ray, A. S. et al. Mechanism of active renal tubular efflux of tenofovir. Antimicrob. Agents Chemother. 50, 3297–3304 (2006). · DOI
  34. Rius, M., Hummel-Eisenbeiss, J., Hofmann, A. F. & Keppler, D. Substrate specificity of human ABCC4 (MRP4)-mediated cotransport of bile acids and reduced glutathione. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G640–G649 (2006). · DOI · Paper page
  35. Rius, M., Hummel-Eisenbeiss, J. & Keppler, D. ATP-dependent transport of leukotrienes B4 and C4 by the multidrug resistance protein ABCC4 (MRP4). J. Pharmacol. Exp. Ther. 324, 86–94 (2008). · DOI
  36. Rius, M., Nies, A. T., Hummel-Eisenbeiss, J., Jedlitschky, G. & Keppler, D. Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology 38, 374–384 (2003). · DOI · Paper page
  37. Vogt, K. et al. Release of platelet-derived sphingosine-1-phosphate involves multidrug resistance protein 4 (MRP4/ABCC4) and Is inhibited by statins. Thromb. Haemost. 118, 132–142 (2018). · DOI
  38. Hagmann, W. et al. Purification of the human apical conjugate export pump MRP2 reconstitution and functional characterization as substrate-stimulated ATPase. Eur. J. Biochem. 265, 281–289 (1999). · DOI
  39. Mao, Q., Leslie, E. M., Deeley, R. G. & Cole, S. P. ATPase activity of purified and reconstituted multidrug resistance protein MRP1 from drug-selected H69AR cells. Biochim. Biophys. Acta 1461, 69–82 (1999). · DOI
  40. Shapiro, A. B. & Ling, V. ATPase activity of purified and reconstituted P-glycoprotein from Chinese hamster ovary cells. J. Biol. Chem. 269, 3745–3754 (1994). · DOI
  41. Sauna, Z. E., Nandigama, K. & Ambudkar, S. V. Multidrug resistance protein 4 (ABCC4)-mediated ATP hydrolysis: effect of transport substrates and characterization of the post-hydrolysis transition state. J. Biol. Chem. 279, 48855–48864 (2004). · DOI
  42. Berthier, J., Arnion, H., Saint-Marcoux, F. & Picard, N. Multidrug resistance-associated protein 4 in pharmacology: overview of its contribution to pharmacokinetics, pharmacodynamics and pharmacogenetics. Life Sci. 231, 116540 (2019). · DOI
  43. Stockner, T., Gradisch, R. & Schmitt, L. The role of the degenerate nucleotide binding site in type I ABC exporters. FEBS Lett. 594, 3815–3838 (2020). · DOI
  44. Copsel, S. et al. Multidrug resistance protein 4 (MRP4/ABCC4) regulates cAMP cellular levels and controls human leukemia cell proliferation and differentiation. J. Biol. Chem. 286, 6979–6988 (2011). · DOI
  45. Hayashi, H. et al. Sorting nexin 27 interacts with multidrug resistance-associated protein 4 (MRP4) and mediates internalization of MRP4. J. Biol. Chem. 287, 15054–15065 (2012). · DOI
  46. Payen, L. F., Gao, M., Westlake, C. J., Cole, S. P. & Deeley, R. G. Role of carboxylate residues adjacent to the conserved core Walker B motifs in the catalytic cycle of multidrug resistance protein 1 (ABCC1). J. Biol. Chem. 278, 38537–38547 (2003). · DOI
  47. Johnson, Z. L. & Chen, J. Structural basis of substrate recognition by the multidrug resistance protein MRP1. Cell 168, 1075–1085 e9 (2017). · DOI · Paper page
  48. Mi, W. et al. Structural basis of MsbA-mediated lipopolysaccharide transport. Nature 549, 233–237 (2017). · DOI
  49. Hofmann, S. et al. Conformation space of a heterodimeric ABC exporter under turnover conditions. Nature 571, 580–583 (2019). · DOI
  50. Sedzicki, J. et al. Mechanism of cyclic beta-glucan export by ABC transporter Cgt of Brucella. Nat. Struct. Mol. Biol. 29, 1170–1177 (2022). · DOI
  51. Choudhury, H. G. et al. Structure of an antibacterial peptide ATP-binding cassette transporter in a novel outward occluded state. Proc. Natl Acad. Sci. USA 111, 9145–9150 (2014). · DOI
  52. Olsen, J. A., Alam, A., Kowal, J., Stieger, B. & Locher, K. P. Structure of the human lipid exporter ABCB4 in a lipid environment. Nat. Struct. Mol. Biol. 27, 62–70 (2020). · DOI
  53. Lee, K. P. K., Chen, J. & MacKinnon, R. Molecular structure of human KATP in complex with ATP and ADP. eLife 6, e32481 (2017). · DOI
  54. El-Sheikh, A. A., van den Heuvel, J. J., Krieger, E., Russel, F. G. & Koenderink, J. B. Functional role of arginine 375 in transmembrane helix 6 of multidrug resistance protein 4 (MRP4/ABCC4). Mol. Pharmacol. 74, 964–971 (2008). · DOI
  55. Wittgen, H. G. et al. Phenylalanine 368 of multidrug resistance-associated protein 4 (MRP4/ABCC4) plays a crucial role in substrate-specific transport activity. Biochem. Pharmacol. 84, 366–373 (2012). · DOI
  56. Schuetz, J. D. et al. MRP4: a previously unidentified factor in resistance to nucleoside-based antiviral drugs. Nat. Med. 5, 1048–1051 (1999). · DOI
  57. van Aubel, R. A., Smeets, P. H., Peters, J. G., Bindels, R. J. & Russel, F. G. The MRP4/ABCC4 gene encodes a novel apical organic anion transporter in human kidney proximal tubules: putative efflux pump for urinary cAMP and cGMP. J. Am. Soc. Nephrol. 13, 595–603 (2002). · DOI
  58. Kawahara, K., Hohjoh, H., Inazumi, T., Tsuchiya, S. & Sugimoto, Y. Prostaglandin E2-induced inflammation: relevance of prostaglandin E receptors. Biochim. Biophys. Acta 1851, 414–421 (2015). · DOI · Paper page
  59. Barnett, R. E. Effect of monovalent cations on the ouabain iniibition of the sodium and potassium ion activated adenosine triphosphatase. Biochemistry 9, 4644–4648 (1970). · DOI
  60. Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017). · DOI
  61. Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017). · DOI · Paper page
  62. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D. Biol. Crystallogr. 66, 486–501 (2010). · DOI · Paper page
  63. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D. Biol. Crystallogr. 66, 213–221 (2010). · DOI · Paper page
  64. Croll, T. I. ISOLDE: a physically realistic environment for model building into low-resolution electron-density maps. Acta Crystallogr. D. Struct. Biol. 74, 519–530 (2018). · DOI
  65. Sanchez-Garcia, R. et al. DeepEMhancer: a deep learning solution for cryo-EM volume post-processing. Commun. Biol. 4, 874 (2021). · DOI
  66. Pettersen, E. F. et al. UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004). · DOI
  67. Pravda, L. et al. MOLEonline: a web-based tool for analyzing channels, tunnels and pores (2018 update). Nucleic Acids Res. 46, W368–W373 (2018). · DOI
  68. Voss, N. R. & Gerstein, M. 3V: cavity, channel and cleft volume calculator and extractor. Nucleic Acids Res. 38, W555–W562 (2010). · DOI
  69. Laskowski, R. A. & Swindells, M. B. LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J. Chem. Inf. Model. 51, 2778–2786 (2011). · DOI
  70. Pintilie, G. et al. Measurement of atom resolvability in cryo-EM maps with Q-scores. Nat. Methods 17, 328–334 (2020). · DOI

Cited by

Sorted by citations

See all 29

Metadata

Authors
Pourmal, S., Green, E., Bajaj, R., Chemmama, I. E., Knudsen, G. M., Gupta, M., Sali, A., Cheng, Y., Craik, C. S., Kroetz, D. L., & Stroud, R. M.
Venue
Nature Structural & Molecular Biology
Publisher
Springer Science and Business Media LLC
Published
2024-01-12
Volume
31
Issue
4
Pages
621-632
ISSN
  • 1545-9993
  • 1545-9985
DOI
10.1038/s41594-023-01176-4
Cited by
29
References
0
Language
en
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review