The kinesin KIF16B mediates apical transcytosis of transferrin receptor in AP-1B-deficient epithelia

EMBO Journal

Volumn 32, Issue 15, 2013, Pages 2125-2139

  Perez Bay, Andres E ^a   Schreiner, Ryan ^a   Mazzoni, Francesca ^a   Carvajal Gonzalez, Jose M ^a   Gravotta, Diego ^a   Perret, Emilie ^a   Lehmann Mantaras, Gullermo ^a   Zhu, Yuan Shan ^a   Rodriguez Boulan, Enrique J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

AP 1B; KIF16B; rab11a; RPE; transferrin receptor

Indexed keywords

CLATHRIN; KIF16B PROTEIN; KINESIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; APICAL MEMBRANE; APICAL RECYCLING ENDOSOME; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOSOME; EPITHELIUM CELL; FEMALE; MDCK CELL; MICROTUBULE; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCYTOSIS;

ADAPTOR PROTEIN COMPLEX 1; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DOGS; ENDOSOMES; EPITHELIAL CELLS; HUMANS; KINESIN; MADIN DARBY CANINE KIDNEY CELLS; MICROTUBULES; RAB GTP-BINDING PROTEINS; RECEPTORS, TRANSFERRIN; TRANSCYTOSIS;

EID: 84881480879     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.130     Document Type: Article

References (54)

1. Apodaca G, Katz LA, Mostov KE (1994) Receptor-mediated trans-cytosis of IgA in MDCK cells is via apical recycling endosomes. J Cell Biol 125: 67-86
2. Babbey CM, Ahktar N, Wang E, Chen CC, Grant BD, Dunn KW (2006) Rab10 regulates membrane transport through early endo-somes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 17: 3156-3175
3. Barroso M, Sztul ES (1994) Basolateral to apical transcytosis in polarized cells is indirect and involves BFA and trimeric G protein sensitive passage through the apical endosome. J Cell Biol 124: 83-100
4. Bomsel M, Prydz K, Parton RG, Gruenberg J, Simons K (1989) Endocytosis in filter-grown Madin-Darby canine kidney cells. J Cell Biol 109: 3243-3258
5. Brown PS, Wang E, Aroeti B, Chapin SJ, Mostov KE, Dunn KW (2000) Definition of distinct compartments in polarized Madin-Darby canine kidney (MDCK) cells for membrane-volume sorting, polarized sorting and apical recycling. Traffic 1: 124-140
6. Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, Woodrum JE, Altschuler Y, Ray GS, Goldenring JR (1999) Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol Biol Cell 10: 47-61
7. Chabin-Brion K, Marceiller J, Perez F, Settegrana C, Drechou A, Durand G, Pous C (2001) The Golgi complex is a microtubule-organizing organelle. Mol Biol Cell 12: 2047-2060
8. Cheong KH, Zacchetti D, Schneeberger EE, Simons K (1999) VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells. Proc Natl Acad Sci USA 96: 6241-6248
9. Cresawn KO, Potter BA, Oztan A, Guerriero CJ, Ihrke G, Goldenring JR, Apodaca G, Weisz OA (2007) Differential involvement of endocytic compartments in the biosynthetic traffic of apical proteins. EMBO J 26: 3737-3748
10. Daro E, van der Sluijs P, Galli T, Mellman I (1996) Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling. Proc Natl Acad Sci USA 93: 9559-9564
11. Datta A, Bryant DM, Mostov KE (2011) Molecular regulation of lumen morphogenesis. Curr Biol 21: R126-R136
12. Deborde S, Perret E, Gravotta D, Deora A, Salvarezza S, Schreiner R, Rodriguez-Boulan E (2008) Clathrin is a key regulator of baso-lateral polarity. Nature 452: 719-723
13. Deora AA, Diaz F, Schreiner R, Rodriguez-Boulan E (2007) Efficient electroporation of DNA and protein into confluent and differentiated epithelial cells in culture. Traffic 8: 1304-1312
14. Diaz F, Gravotta D, Deora A, Schreiner R, Schoggins J, Falck-Pedersen E, Rodriguez-Boulan E (2009) Clathrin adaptor AP1B controls adenovirus infectivity of epithelial cells. Proc Natl Acad Sci USA 106: 11143-11148
15. Folsch H, Ohno H, Bonifacino JS, Mellman I (1999) A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 99: 189-198
16. Folsch H, Pypaert M, Maday S, Pelletier L, Mellman I (2003) The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains. J Cell Biol 163: 351-362
17. Fuller SD, Simons K (1986) Transferrin receptor polarity and recycling accuracy in "tight" and "leaky" strains of Madin-Darby canine kidney cells. J Cell Biol 103: 1767-1779
18. Gan Y, McGraw TE, Rodriguez-Boulan E (2002) The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane. Nat Cell Biol 4: 605-609
19. Garcia-Castineiras S (2010) Iron, the retina and the lens: a focused review. Exp Eye Res 90: 664-678
20. Golachowska MR, Hoekstra D, van ISC (2010) Recycling endosomes in apical plasma membrane domain formation and epithelial cell polarity. Trends Cell Biol 20: 618-626
21. Gravotta D, Carvajal-Gonzalez JM, Mattera R, Deborde S, Banfelder JR, Bonifacino JS, Rodriguez-Boulan E (2012) The clathrin adaptor AP-1A mediates basolateral polarity. Dev Cell 22: 811-823
22. Gravotta D, Deora A, Perret E, Oyanadel C, Soza A, Schreiner R, Gonzalez A, Rodriguez-Boulan E (2007) AP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells. Proc Natl Acad Sci USA 104: 1564-1569
23. He X, Hahn P, Iacovelli J, Wong R, King C, Bhisitkul R, Massaro-Giordano M, Dunaief JL (2007) Iron homeostasis and toxicity in retinal degeneration. Prog Retin Eye Res 26: 649-673
24. Hoepfner S, Severin F, Cabezas A, Habermann B, Runge A, Gillooly D, Stenmark H, Zerial M (2005) Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121: 437-450
25. Hopkins CR (1983) Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells. Cell 35: 321-330
26. Hughson EJ, Hopkins CR (1990) Endocytic pathways in polarized Caco-2 cells: identification of an endosomal compartment accessible from both apical and basolateral surfaces. J Cell Biol 110: 337-348
27. Hunziker W, Male P, Mellman I (1990) Differential microtubule requirements for transcytosis in MDCK cells. EMBO J 9: 3515-3525
28. Jaulin F, Xue X, Rodriguez-Boulan E, Kreitzer G (2007) Polarization-dependent selective transport to the apical membrane by KIF5B in MDCK cells. Dev Cell 13: 511-522
29. Kitt KN, Hernandez-Deviez D, Ballantyne SD, Spiliotis ET, Casanova JE, Wilson JM (2008) Rab14 regulates apical targeting in polarized epithelial cells. Traffic 9: 1218-1231
30. Lapierre LA, Dorn MC, Zimmerman CF, Navarre J, Burnette JO, Goldenring JR (2003) Rab11b resides in a vesicular compartment distinct from Rab11a in parietal cells and other epithelial cells. Exp Cell Res 290: 322-331
31. Leung SM, Ruiz WG, Apodaca G (2000) Sorting of membrane and fluid at the apical pole of polarized Madin-Darby canine kidney cells. Mol Biol Cell 11: 2131-2150
32. Li HC, Li EY, Neumeier L, Conforti L, Soleimani M (2007) Identification of a novel signal in the cytoplasmic tail of the Na+:HCO3-cotransporter NBC1 that mediates basolateral targeting. Am J Physiol Renal Physiol 292: F1245-F1255
33. Li Y, Roy BD, Wang W, Zhang L, Sampson SB, Yang Y, Lin DT (2012) Identification of two functionally distinct endosomal recycling pathways for dopamine D(2) receptor. J Neurosci 32: 7178-7190
34. Luton F, Hexham MJ, Zhang M, Mostov KE (2009) Identification of a cytoplasmic signal for apical transcytosis. Traffic 10: 1128-1142
35. Maxfield FR, McGraw TE (2004) Endocytic recycling. Nat Rev Mol Cell Biol 5: 121-132
36. McGraw TE, Greenfield L, Maxfield FR (1987) Functional expression of the human transferrin receptor cDNA in Chinese hamster ovary cells deficient in endogenous transferrin receptor. J Cell Biol 105: 207-214
37. Mohrmann K, Leijendekker R, Gerez L, van Der Sluijs P (2002) rab4 regulates transport to the apical plasma membrane in Madin-Darby canine kidney cells. J Biol Chem 277: 10474-10481
38. Odorizzi G, Trowbridge IS (1997) Structural requirements for baso-lateral sorting of the human transferrin receptor in the biosyn-thetic and endocytic pathways of Madin-Darby canine kidney cells. J Cell Biol 137: 1255-1264
39. Ohno H, Tomemori T, Nakatsu F, Okazaki Y, Aguilar RC, Foelsch H, Mellman I, Saito T, Shirasawa T, Bonifacino JS (1999) Mu1B, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett 449: 215-220
40. Perret E, Lakkaraju A, Deborde S, Schreiner R, Rodriguez-Boulan E (2005) Evolving endosomes: how many varieties and why? Curr Opin Cell Biol 17: 423-434
41. Puertollano R, Martin-Belmonte F, Millan J, de Marco MC, Albar JP, Kremer L, Alonso MA (1999) The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. J Cell Biol 145: 141-151
42. Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD (1998) Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci USA 95: 6187-6192
43. Rodriguez-Boulan E, Kreitzer G, Musch A (2005) Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 6: 233-247
44. Roush DL, Gottardi CJ, Naim HY, Roth MG, Caplan MJ (1998) Tyrosine-based membrane protein sorting signals are differentially interpreted by polarized Madin-Darby canine kidney and LLC-PK1 epithelial cells. J Biol Chem 273: 26862-26869
45. Schreiner R, Frindt G, Diaz F, Carvajal-Gonzalez JM, Perez Bay AE, Palmer LG, Marshansky V, Brown D, Philp NJ, Rodriguez-Boulan E (2010) The absence of a clathrin adapter confers unique polarity essential to proximal tubule function. Kidney Int 78: 382-388
46. Simons K, Fuller SD (1985) Cell surface polarity in epithelia. Annu Rev Cell Biol 1: 243-288
47. Strauss O (2005) The retinal pigment epithelium in visual function. Physiol Rev 85: 845-881
48. Ueno H, Huang X, Tanaka Y, Hirokawa N (2011) KIF16B/Rab14 molecular motor complex is critical for early embryonic development by transporting FGF receptor. Dev Cell 20: 60-71
49. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericentriolar recycling endo-some. J Cell Biol 135: 913-924
50. Wang X, Kumar R, Navarre J, Casanova JE, Goldenring JR (2000) Regulation of vesicle trafficking in madin-darby canine kidney cells by Rab11a and Rab25. J Biol Chem 275: 29138-29146
51. Weisz OA, Rodriguez-Boulan E (2009) Apical trafficking in epithelial cells: signals, clusters and motors. J Cell Sci 122: 4253-4266
52. Yamashiro DJ, Tycko B, Fluss SR, Maxfield FR (1984) Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37: 789-800
53. Yefimova MG, Jeanny JC, Guillonneau X, Keller N, Nguyen-Legros J, Sergeant C, Guillou F, Courtois Y (2000) Iron, ferritin, trans-ferrin, and transferrin receptor in the adult rat retina. Invest Ophthalmol Vis Sci 41: 2343-2351
54. Zacchi P, Stenmark H, Parton RG, Orioli D, Lim F, Giner A, Mellman I, Zerial M, Murphy C (1998) Rab17 regulates membrane trafficking through apical recycling endosomes in polarized epithelial cells. J Cell Biol 140: 1039-1053