Multiple Biosynthetic Trafficking Routes for Apically Secreted Proteins in MDCK Cells

Traffic

Volumn 13, Issue 3, 2012, Pages 433-442

  Mattila, Polly E ^a   Youker, Robert T ^a   Mo, Di ^a   Bruns, Jennifer R ^a   Cresawn, Kerry O ^a,b   Hughey, Rebecca P ^a   Ihrke, Gudrun ^c   Weisz, Ora A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b JAMES MADISON UNIVERSITY   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Apical recycling endosome; Galectin; Myosin Vb; N glycosylation; Polarity

Indexed keywords

ENSOL; GALECTIN 3; GALECTIN 4; GLYCAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; GROWTH HORMONE; MEMBRANE PROTEIN; MYOSIN V; MYOSIN VB; RAB11 PROTEIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL STRAIN; CONTROLLED STUDY; ENDOSOME; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HORMONE RELEASE; LIPOPROTEIN SECRETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANS GOLGI NETWORK;

ANIMALS; ANTIGENS, CD164; CELL LINE; DOGS; ENDOSOMES; EPITHELIAL CELLS; GROWTH HORMONE; PROTEIN TRANSPORT;

EID: 84856787778     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01315.x     Document Type: Article

References (47)

1. Folsch H, Mattila PE, Weisz OA. Taking the scenic route: biosynthetic traffic to the plasma membrane in polarized epithelial cells. Traffic 2009;10:972-981.
2. Rodriguez-Boulan E, Kreitzer G, Musch A. Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 2005;6:233-247.
3. Jacob R, Naim HY. Apical membrane proteins are transported in distinct vesicular carriers. Curr Biol 2001;11:1444-1450.
4. Cresawn KO, Potter BA, Oztan A, Guerriero CJ, Ihrke G, Goldenring JR, Apodaca G, Weisz OA. Differential involvement of endocytic compartments in the biosynthetic traffic of apical proteins. EMBO J 2007;26:3737-3748.
5. Guerriero CJ, Lai Y, Weisz OA. Differential sorting and Golgi export requirements for raft-associated and raft-independent apical proteins along the biosynthetic pathway. J Biol Chem 2008;283:18040-18047.
6. Brown PS, Wang E, Aroeti B, Chapin SJ, Mostov KE, Dunn KW. Definition of distinct compartments in polarized Madin-Darby canine kidney (MDCK) cells for membrane-volume sorting, polarized sorting and apical recycling. Traffic 2000;1:124-140.
7. Tzaban S, Massol RH, Yen E, Hamman W, Frank SR, Lapierre LA, Hansen SH, Goldenring JR, Blumberg RS, Lencer WI. The recycling and transcytotic pathways for IgG transport by FcRn are distinct and display an inherent polarity. J Cell Biol 2009;185:673-684.
8. Apodaca G, Katz LA, Mostov KE. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J Cell Biol 1994;125:67-86.
9. Lapierre LA, Kumar R, Hales CM, Navarre J, Bhartur SG, Burnette JO, Provance DW Jr, Mercer JA, Bahler M, Goldenring JR. Myosin vb is associated with plasma membrane recycling systems. Mol Biol Cell 2001;12:1843-1857.
10. Ang AL, Taguchi T, Francis S, Folsch H, Murrells LJ, Pypaert M, Warren G, Mellman I. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J Cell Biol 2004;167:531-543.
11. Mattila PE, Kinlough CL, Bruns JR, Weisz OA, Hughey RP. MUC1 traverses apical recycling endosomes along the biosynthetic pathway in polarized MDCK cells. Biol Chem 2009;390:551-556.
12. Kinlough CL, Poland PA, Gendler SJ, Mattila PE, Mo D, Weisz OA, Hughey RP. Core-glycosylated mucin-like repeats from MUC1 are an apical targeting signal. J Biol Chem 2011.
13. Gravotta D, Deora A, Perret E, Oyanadel C, Soza A, Schreiner R, Gonzalez A, Rodriguez-Boulan E. AP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells. Proc Natl Acad Sci U S A 2007;104:1564-1569.
14. Farr GA, Hull M, Mellman I, Caplan MJ. Membrane proteins follow multiple pathways to the basolateral cell surface in polarized epithelial cells. J Cell Biol 2009;186:269-282.
15. Bomsel M, Prydz K, Parton RG, Gruenberg J, Simons K. Endocytosis in filter-grown Madin-Darby canine kidney cells. J Cell Biol 1989;109:3243-3258.
16. Potter BA, Ihrke G, Bruns JR, Weixel KM, Weisz OA. Specific N-glycans direct apical delivery of transmembrane, but not soluble or glycosylphosphatidylinositol-anchored forms of endolyn in Madin-Darby canine kidney cells. Mol Biol Cell 2004;15:1407-1416.
17. Scheiffele P, Peranen J, Simons K. N-glycans as apical sorting signals in epithelial cells. Nature 1995;378:96-98.
18. Ihrke G, Bruns JR, Luzio JP, Weisz OA. Competing sorting signals guide endolyn along a novel route to lysosomes in MDCK cells. EMBO J 2001;20:6256-6264.
19. Wu S, Mehta SQ, Pichaud F, Bellen HJ, Quiocho FA. Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat Struct Mol Biol 2005;12:879-885.
20. Weisz OA, Rodriguez-Boulan E. Apical trafficking in epithelial cells: signals, clusters and motors. J Cell Sci 2009;122:4253-4266.
21. Delacour D, Greb C, Koch A, Salomonsson E, Leffler H, Le Bivic A, Jacob R. Apical sorting by galectin-3-dependent glycoprotein clustering. Traffic 2007;8:379-388.
22. Delacour D, Cramm-Behrens CI, Drobecq H, Le Bivic A, Naim HY, Jacob R. Requirement for galectin-3 in apical protein sorting. Curr Biol 2006;16:408-414.
23. Stechly L, Morelle W, Dessein AF, Andre S, Grard G, Trinel D, Dejonghe MJ, Leteurtre E, Drobecq H, Trugnan G, Gabius HJ, Huet G. Galectin-4-regulated delivery of glycoproteins to the brush border membrane of enterocyte-like cells. Traffic 2009;10:438-450.
24. Delacour D, Gouyer V, Zanetta JP, Drobecq H, Leteurtre E, Grard G, Moreau-Hannedouche O, Maes E, Pons A, Andre S, Le Bivic A, Gabius HJ, Manninen A, Simons K, Huet G. Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J Cell Biol 2005;169:491-501.
25. Barroso M, Sztul ES. 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 1994;124:83-100.
26. Thompson A, Nessler R, Wisco D, Anderson E, Winckler B, Sheff D. Recycling endosomes of polarized epithelial cells actively sort apical and basolateral cargos into separate subdomains. Mol Biol Cell 2007;18:2687-2697.
27. Puthenveedu MA, Lauffer B, Temkin P, Vistein R, Carlton P, Thorn K, Taunton J, Weiner OD, Parton RG, von Zastrow M. Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 2010;143:761-773.
28. Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 2009;10:597-608.
29. Leitinger B, Hille-Rehfeld A, Spiess M. Biosynthetic transport of the asialoglycoprotein receptor H1 to the cell surface occurs via endosomes. Proc Natl Acad Sci U S A 1995;92:10109-10113.
30. Futter CE, Connolly CN, Cutler DF, Hopkins CR. Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface. J Biol Chem 1995;270:10999-11003.
31. Rodriguez-Boulan E, Gonzalez A. Glycans in post-Golgi apical targeting: sorting signals or structural props? Trends Cell Biol 1999;9:291-294.
32. Mo D, Potter BA, Bertrand CA, Hildebrand JD, Bruns JR, Weisz OA. Nucleofection disrupts tight junction fence function to alter membrane polarity of renal epithelial cells. Am J Physiol Renal Physiol 2010.
33. Friedrichs J, Torkko JM, Helenius J, Teravainen TP, Fullekrug J, Muller DJ, Simons K, Manninen A. Contributions of galectin-3 and -9 to epithelial cell adhesion analyzed by single cell force spectroscopy. J Biol Chem 2007;282:29375-29383.
34. Poland PA, Rondanino C, Kinlough CL, Heimburg-Molinaro J, Arthur CM, Stowell SR, Smith DF, Hughey RP. Identification and characterization of endogenous galectins expressed in Madin Darby canine kidney cells. J Biol Chem 2011;286:6780-6790.
35. Thor F, Gautschi M, Geiger R, Helenius A. Bulk flow revisited: transport of a soluble protein in the secretory pathway. Traffic 2009;10:1819-1830.
36. Boll W, Partin JS, Katz AI, Caplan MJ, Jamieson JD. Distinct pathways for basolateral targeting of membrane and secretory proteins in polarized epithelial cells. Proc Natl Acad Sci U S A 1991;88:8592-8596.
37. Musch A, Cohen D, Kreitzer G, Rodriguez-Boulan E. cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network. EMBO J 2001;20:2171-2179.
38. De Almeida JB, Stow JL. Disruption of microtubules alters polarity of basement membrane proteoglycan secretion in epithelial cells. Am J Physiol Cell Physiol 1991;261:C691-C700.
39. Caplan MJ, Stow JL, Newman AP, Madri J, Anderson HC, Farquhar MG, Palade GE, Jamieson JD. Dependence on pH of polarized sorting of secreted proteins. Nature 1987;329:632-635.
40. Tveit H, Akslen LK, Fagereng GL, Tranulis MA, Prydz K. A secretory Golgi bypass route to the apical surface domain of epithelial MDCK cells. Traffic 2009;10:1685-1695.
41. Lapierre LA, Dorn MC, Zimmerman CF, Navarre J, Burnette JO, Goldenring JR. Rab11b resides in a vesicular compartment distinct from Rab11a in parietal cells and other epithelial cells. Exp Cell Res 2003;290:322-331.
42. Henkel JR, Apodaca G, Altschuler Y, Hardy S, Weisz OA. Selective perturbation of apical membrane traffic by expression of influenza M2, an acid-activated ion channel, in polarized Madin-Darby canine kidney cells. Mol Biol Cell 1998;9:2477-2490.
43. Guan JL, Machamer CE, Rose JK. Glycosylation allows cell-surface transport of an anchored secretory protein. Cell 1985;42:489-496.
44. Ihrke G, Martin GV, Shanks MR, Schrader M, Schroer TA, Hubbard AL. Apical plasma membrane proteins and endolyn-78 travel through a subapical compartment in polarized WIF-B hepatocytes. J Cell Biol 1998;141:115-133.
45. Cui S, Guerriero CJ, Szalinski CM, Kinlough CL, Hughey RP, Weisz OA. OCRL1 function in renal epithelial membrane traffic. Am J Physiol Renal Physiol 298:F335-F345.
46. Anderson JM, Stevenson BR, Jesaitis LA, Goodenough DA, Mooseker MS. Characterization of ZO-1, a protein component of the tight junction from mouse liver and Madin-Darby canine kidney cells. J Cell Biol 1988;106:1141-1149.
47. Phair RD, Gorski SA, Misteli T. Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol 2004;375:393-414.