Actin polymerization controls the activation of multidrug efflux at fertilization by translocation and fine-scale positioning of ABCB1 on microvilli

Molecular Biology of the Cell

Volumn 23, Issue 18, 2012, Pages 3663-3672

  Whalen, Kristen ^a   Reitzel, Adam M ^b   Hamdoun, Amro ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; MULTIDRUG RESISTANCE PROTEIN 1A; RAB11 PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; FERTILIZATION; FLUORESCENCE MICROSCOPY; MICROVILLUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SEA URCHIN;

ACTINS; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELL MEMBRANE; CYTOCHALASIN D; DEPSIPEPTIDES; EMBRYO, NONMAMMALIAN; FEMALE; FERTILIZATION; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MICROVILLI; OVUM; P-GLYCOPROTEIN; PHYLOGENY; POLYMERIZATION; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SEA URCHINS; THIAZOLIDINES;

ECHINOIDEA;

EID: 84866380361     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-06-0438     Document Type: Article

References (46)

1. Abascal F, Zardoya R, Posada D (2005). ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105. (Pubitemid 40668057)
2. Acharya P, Tran TT, Polli JW, Ayrton A, Ellens H, Bentz J (2006). P-glycoprotein (P-gp) expressed in a confluent monolayer of hMDR1-MDCKII cells has more than one efflux pathway with cooperative binding sites. Biochemistry 45, 15505-15519. (Pubitemid 46032474)
3. Annilo T, Chen Z-Q, Shulenin S, Costantino J, Thomas L, Lou H, Stefanov S, Dean M (2006). Evolution of the vertebrate ABC gene family: analysis of gene birth and death. Genomics 88, 1-11. (Pubitemid 43851178)
4. Begg DA, Rebhun LI, Hyatt H (1982). Structural organization of actin in the sea urchin egg cortex: microvillar elongation in the absence of actin filament bundle formation. J Cell Biol 93, 24-32. (Pubitemid 12117037)
5. Bonder EM, Fishkind DJ, Cotran NM, Begg DA (1989). The cortical actin-membrane cytoskeleton of unfertilized sea urchin eggs: analysis of the spatial organization and relationship of filamentous actin, nonfilamentous actin, and egg spectrin. Dev Biol 134, 327-341. (Pubitemid 19201052)
6. Callaghan R, Crowley E, Potter S, Kerr ID (2008). P-glycoprotein: so many ways to turn it on. J Clin Pharmacol 48, 365-378.
7. Campanale JP, Hamdoun A (2012). Programmed reduction of ABC transporter activity in sea urchin germline progenitors. Development 139, 783-792.
8. Conner SD, Wessel GM (1998). rab3 mediates cortical granule exocytosis in the sea urchin egg. Dev Biol 203, 334-344.
9. Conner SD, Wessel GM (2000). A rab3 homolog in sea urchin functions in cell division. FASEB J 14, 1559-1566. (Pubitemid 30636560)
10. Dillon C, Goda Y (2005). The actin cytoskeleton: integrating form and function at the synapse. Annu Rev Neurosci 28, 25-55. (Pubitemid 41098898)
11. Edgar R (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792-1797.
12. Epel D (1972). Activation of an Na+-dependent amino acid transport system upon fertilization of sea urchin eggs. Exp Cell Res 72, 74-89.
13. Epel D (1975). The program of and mechanisms of fertilization in the echinoderm egg. Integr Comp Biol 15, 507-522.
14. Evans GL, Ni B, Hrycyna CA, Chen D, Ambudkar SV, Pastan I, Germann UA, Gottesman MM (1995). Heterologous expression systems for P-glycoprotein: E. coli, yeast, and baculovirus. J Bioenerg Biomembr 27, 43-52.
15. Fu D, Arias IM (2012). Intracellular trafficking of P-glycoprotein. Int J Biochem Cell Biol 44, 461-464.
16. Fu D, Roufogalis BD (2007). Actin disruption inhibits endosomal traffic of P-glycoprotein-EGFP and resistance to daunorubicin accumulation. Am J Physiol Cell Physiol 292, C1543-C1552. (Pubitemid 46631739)
17. Goldstone JV, Hamdoun A, Cole BJ, Howard-Ashby M, Nebert DW, Scally M, Dean M, Epel D, Hahn ME, Stegeman JJ (2006). The chemical defensome: environmental sensing and response genes in the Strongylocentrotus purpuratus genome. Dev Biol 300, 366-384. (Pubitemid 44827001)
18. Guggino WB, Stanton BA (2006). New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat Rev Mol Cell Biol 7, 426-436. (Pubitemid 44050096)
19. Hamdoun AM (2009). Reduced intracellular accumulation of calcein by overexpression of fluorescent protein fusions of the multidrug transporter Sp-ABCB1a, in sea urchin (Strongylocentrotus purpuratus) embryos. Mount Desert Island Biol Lab Bull 48, 59-62.
20. Hamdoun AM, Cherr GN, Roepke TA, Epel D (2004). Activation of multidrug efflux transporter activity at fertilization in sea urchin embryos (Strongylocentrotus purpuratus). Dev Biol 276, 452-462. (Pubitemid 39592406)
21. Kipp H, Arias IM (2002). Trafficking of canalicular ABC transporters in hepatocytes. Annu Rev Physiol 64, 595-608. (Pubitemid 34259242)
22. Lange K, Gartzke J (2001). Microvillar cell surface as a natural defense system against xenobiotics: a new interpretation of multidrug resistance. Am J Physiol Cell Physiol 281, C369-C385.
23. Loo TW, Clarke DM (1997). Correction of defective protein kinesis of human p-glycoprotein mutants by substrates and modulators. J Biol Chem 272, 709-712. (Pubitemid 27034553)
24. Loo TW, Clarke DM (2008). Mutational analysis of ABC proteins. Arch Biochem Biophys 476, 51-64.
25. McConnell RE, Higginbotham JN, Shifrin DA, Jr., Tabb DL, Coffey RJ, Tyska M (2009). The enterocyte microvillus is a vesicle-generating organelle. J Cell Biol 185, 1285-1298.
26. Nicolaou M, Andress EJ, Zolnerciks JK, Dixon PH, Williamson C, Linton KJ (2011). Canalicular ABC transporters and liver disease. J Pathol 226, 300-315.
27. Otto JJ, Kane RE, Bryan J (1980). Redistribution of actin and fascin in sea urchin eggs after fertilization. Cell Motil 1, 31-40. (Pubitemid 12233332)
28. Polyak K, Weinberg RA (2009). Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9, 265-273.
29. Putnam NH et al. (2007). Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86-94. (Pubitemid 47056460)
30. Revenu C et al. (2011). A new role for the architecture of the microvillar actin bundles in apical retention of membrane proteins. Mol Biol Cell 23, 324-336.
31. Schroeder TE (1979). Surface area change at fertilization: resorption of the mosaic membrane. Dev Biol 70, 306-326.
32. Schroeder TE (1988). Contact-independent polarization of the cell surface and cortex of free sea urchin blastomeres. Dev Biol 125, 255-264.
33. Shi Z et al. (2009). Inhibiting the function of ABCB1 and ABCG2 by the EGFR tyrosine kinase inhibitor AG1478. Biochem Pharmacol 77, 781-793.
34. Shipp LE, Hamdoun A (2012). ATP-binding cassette (ABC) transporter expression and localization in sea urchin development. Dev Dyn 241, 1111-1124.
35. Singer II et al. (2001). CCR5, CXCR4, and CD4 are clustered and closely apposed on microvilli of human macrophages and T cells. J Virol 75, 3779-3790. (Pubitemid 32246387)
36. Spudich A, Spudich JA (1979). Actin in triton-treated cortical preparations of unfertilized and fertilized sea urchin eggs. J Cell Biol 82, 212-226.
37. Spudich A, Wrenn JT, Wessells NK (1988). Unfertilized sea urchin eggs contain a discrete cortical shell of actin that is subdivided into two organizational states. Cell Motil Cytoskeleton 9, 85-96. (Pubitemid 18053107)
38. Srivastava M et al. (2010). The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466, 720-726.
39. Stamatakis A (2006). Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690.
40. Sturm A, Cunningham P, Dean M (2009). The ABC transporter gene family of Daphnia pulex. BMC Genomics 10, 170.
41. Tran TT, Mittal A, Aldinger T, Polli JW, Ayrton A, Ellens H, Bentz J (2005). The elementary mass action rate constants of P-gp transport for a confluent monolayer of MDCKII-hMDR1 cells. Biophys J 88, 715-738. (Pubitemid 40070714)
42. Vacquier VD (1981). Dynamic changes of the egg cortex. Dev Biol 84, 1-26.
43. von Andrian UH, Hasslen SR, Nelson RD, Erlandsen SL, Butcher EC (1995). A central role for microvillous receptor presentation in leukocyte adhesion under flow. Cell 82, 989-999.
44. Wakabayashi Y, Dutt P, Lippincott-Schwartz J, Arias IM (2005). Rab11a and myosin Vb are required for bile canalicular formation in WIF-B9 cells. Proc Natl Acad Sci USA 102, 15087-15092. (Pubitemid 41513339)
45. Wang L, Soroka CJ, Boyer JL (2002). The role of bile salt export pump mutations in progressive familial intrahepatic cholestasis type II. J Clin Invest 110, 965-972.
46. Weigmann A, Corbeil D, Hellwig A, Huttner WB (1997). Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci USA 94, 12425-12430. (Pubitemid 27492544)