Secretory cargo composition affects polarized secretion in MDCK epithelial cells

Molecular and Cellular Biochemistry

Volumn 310, Issue 1-2, 2008, Pages 67-75

  Fasciotto, Brigitte H ^a   Kühn, Ulrike ^a,b   Cohn, David V ^a   Gorr, Sven Ulrik ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Apical; Basolateral; Cholesterol; Chromogranin A; Furin; PTH

Indexed keywords

CHOLESTEROL; CHROMOGRANIN A; FURIN; PARATHYROID HORMONE; SECRETORY COMPONENT;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL POLARITY; CELL SELECTION; CELL STRAIN; CONTROLLED STUDY; EPITHELIUM CELL; GENETIC TRANSFECTION; NONHUMAN; PLASMID; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN TARGETING;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CATTLE; CELL LINE; CELL POLARITY; CHOLESTEROL; CHROMOGRANIN A; DOGS; EPITHELIAL CELLS; FURIN; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PARATHYROID HORMONE;

EID: 39949085446     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-007-9666-4     Document Type: Article

References (60)

1. Nelson WJ, Yeaman C (2001) Protein trafficking in the exocytic pathway of polarized epithelial cells. Trends Cell Biol 11:483-486
2. Altschuler Y, Hodson C, Milgram SL (2003) The apical compartment: trafficking pathways, regulators and scaffolding proteins. Curr Opin Cell Biol 15:423-429
3. Vogel LK, Larsen JE (2000) Apical and non-polarized secretion of serpins from MDCK cells. FEBS Lett 473:297-302
4. Archer J, Kennan W, Gould M, Bremel R (1994) Human growth hormone (hGH) secretion in milk of goats after direct transfer of the hGH gene into the mammary gland by using replication-defective retrovirus vectors. Proc Natl Acad Sci USA 91:6840-6844
5. Goldfine ID, German MS, Tseng HC, Wang J, Bolaffi JL, Chen JW, Olson DC, Rothman SS (1997) The endocrine secretion of human insulin and growth hormone by exocrine glands of the gastrointestinal tract. Nat Biotechnol 15:1378-1382
6. Kagami H, O'Connell BC, Baum BJ (1996) Evidence for the systemic delivery of a transgene product from salivary glands. Hum Gene Ther 7:2177-2184
7. Baum BJ, Voutetakis A, Wang J (2004) Salivary glands: Novel target sites for gene therapeutics. Trends Mol Med 10:585-590
8. Baum BJ, Berkman ME, Marmary Y, Goldsmith CM, Baccaglini L, Wang S, Wellner RB, Hoque AT, Atkinson JC, Yamagishi H, Kagami H, Parlow AF, Chao J (1999) Polarized secretion of transgene products from salivary glands in vivo. Hum Gene Ther 10:2789-2797
9. Hoque AT, Baccaglini L, Baum BJ (2001) Hydroxychloroquine enhances the endocrine secretion of adenovirus-directed growth hormone from rat submandibular glands in vivo. Hum Gene Ther 12:1333-1341
10. 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 (2005) Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J Cell Biol 169:491-501
11. Delacour D, Greb C, Koch A, Salomonsson E, Leffler H, Le Bivic A, Jacob R (2007) Apical sorting by galectin-3-dependent glycoprotein clustering. Traffic 8:379-388
12. Martin-Belmonte F, Arvan P, Alonso MA (2001) MAL mediates apical transport of secretory proteins in polarized epithelial Madin-Darby canine kidney cells. J Biol Chem 276:49337-49342
13. 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
14. 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
15. Lafont F, Verkade P, Galli T, Wimmer C, Louvard D, Simons K (1999) Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc Natl Acad Sci USA 96:3734-3738
16. Jacob R, Heine M, Eikemeyer J, Frerker N, Zimmer K-P, Rescher U, Gerke V, Naim HY (2004) Annexin II is required for apical transport in polarized epithelial cells. J Biol Chem 279:3680-3684
17. Heine M, Cramm-Behrens CI, Ansari A, Chu H-P, Ryazanov AG, Naim HY, Jacob R (2005) Alpha-kinase 1, a new component in apical protein transport. J Biol Chem 280:25637-25643
18. Ikonen E, Simons K (1998) Protein and lipid sorting from the trans-Golgi network to the plasma membrane in polarized cells. Semin Cell Dev Biol 9:503-509
19. Schuck S, Simons K (2004) Polarized sorting in epithelial cells: Raft clustering and the biogenesis of the apical membrane. J Cell Sci 117:5955-5964
20. Prydz K, Simons K (2001) Cholesterol depletion reduces apical transport capacity in epithelial Madin-Darby canine kidney cells. Biochem J 357:11-15
21. Keller P, Simons K (1998) Cholesterol is required for surface transport of influenza virus hemagglutinin. J Cell Biol 140:1357-1367
22. Martin-Belmonte F, Alonso MA, Zhang X, Arvan P (2000) Thyroglobulin is selected as luminal protein cargo for apical transport via detergent-resistant membranes in epithelial cells. J Biol Chem 275:41074-41081
23. Zheng X, Sadler JE (2001) Mucin-like domain of enteropeptidase directs apical targeting in Madin-Darby canine kidney cells. J Biol Chem 277:6858-6863
24. Larsen JE, Sjostrom H, Noren O, Vogel LK (2002) Serpins are apically secreted from MDCK cells independently of their raft association. Biochem Biophys Res Commun 299:35-41
25. Potter BA, Hughey RP, Weisz OA (2006) Role of N- and O-glycans in polarized biosynthetic sorting. Am J Physiol Cell Physiol 290:C1-C10
26. Kitagawa Y, Sano Y, Ueda M, Higashio K, Narita H, Okano M, Matsumoto S, Sasaki R (1994) N-glycosylation of erythropoietin is critical for apical secretion by Madin-Darby canine kidney cells. Exp Cell Res 213:449-457
27. Scheiffele P, Peranen J, Simons K (1995) N-glycans as apical sorting signals in epithelial cells. Nature 378:96-98
28. Su T, Cariappa R, Stanley K (1999) N-glycans are not a universal signal for apical sorting of secretory proteins. FEBS Lett 453:391-394
29. Larsen JE, Avvakumov GV, Hammond GL, Vogel LK (1999) N-glycans are not the signal for apical sorting of corticosteroid binding globulin in MDCK cells. FEBS Lett 451:19-22
30. Trischler M, Koch-Brandt C, Ullrich O (2001) Apical transport of osteopontin is independent of N-glycosylation and sialylation. Mol Membr Biol 18:275-281
31. Kuhn U, Cohn D, Gorr S (2000) Polarized secretion of the regulated secretory protein chromogranin A. Biochem Biophys Res Commun 270:631-636
32. Yeaman C, Gall AHL, Baldwin AN, Monlauzeur L, Bivic AL, Rodriguez-Boulan E (1997) The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells. J Cell Biol 139:929-940
33. Castelletti D, Fracasso G, Alfalah M, Cingarlini S, Colombatti M, Naim HY (2006) Apical transport and folding of prostate-specific membrane antigen occurs independent of glycan processing. J Biol Chem 281:3505-3512
34. Uchida S, Horie M, Yanagisawa M, Matsushita Y, Kurokawa K, Ogata E (1991) Polarized secretion of endothelin-1 and big ET-1 in MDCK cells is inhibited by cell Na+ flux and disrupted by NH4Cl. J Cardiovasc Pharmacol 17(Suppl 7):S226-S228
35. Venkatesh SG, Gorr SU (2002) A sulfated proteoglycan is necessary for storage of exocrine secretory proteins in the rat parotid gland. Am J Physiol Cell Physiol 283:C438-C445
36. Venkatesh SG, Tan J, Gorr S-U, Darling DS (2007) Isoproterenol increases sorting of parotid gland cargo proteins to the basolateral pathway. Am J Physiol Cell Physiol 293:C558-C565
37. Ahn TG, Cohn DV, Gorr SU, Ornstein DL, Kashdan MA, Levine MA (1987) Primary structure of bovine pituitary secretory protein I (chromogranin A) deduced from the cDNA sequence. Proc Natl Acad Sci USA 84:5043-5047
38. Gorr SU, Huang XF, Cowley DJ, Kuliawat R, Arvan P (1999) Disruption of disulfide bonds exhibits differential effects on trafficking of regulated secretory proteins. Am J Physiol 277:C121-C131
39. Gorr S-U, Darling DS (1995) An N-terminal hydrophobic peak is the sorting signal of regulated secretory proteins. FEBS Lett 361:8-12
40. Gorr S-U (1996) Differential storage of prolactin, granins (chromogranin B and secretogranin II), and constitutive secretory markers in rat pituitary GH4C1 cells. J Biol Chem 271:3575-3580
41. Cowley DJ, Moore YR, Darling DS, Joyce PB, Gorr SU (2000) N- and C-terminal domains direct cell type-specific sorting of chromogranin A to secretory granules. J Biol Chem 275:7743-7748
42. Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227:680-685
43. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 76:4350-4354
44. van Duijnhoven HL, Creemers JW, Kranenborg MG, Timmer ED, Groeneveld A, van den Ouweland AM, Roebroek AJ, van de Ven WJ (1992) Development and characterization of a panel of monoclonal antibodies against the novel subtilisin-like proprotein processing enzyme furin. Hybridoma 11:71-86
45. Gorr SU (1997) Re-probing of immunoblots after storage for more than a decade. Biotechniques 23:250-252, 254
46. Cohn DV, MacGregor RR (1981) The biosynthesis, intracellular processing, and secretion of parathormone. Endocr Rev 2:1-26
47. Mayer G, Boileau G, Bendayan M (2004) Sorting of furin in polarized epithelial and endothelial cells: Expression beyond the Golgi apparatus. J Histochem Cytochem 52:567-580
48. Simmen T, Nobile M, Bonifacino JS, Hunziker W (1999) Basolateral sorting of furin in MDCK cells requires a phenylalanine-isoleucine motif together with an acidic amino acid cluster. Mol Cell Biol 19:3136-3144
49. Kamerzell TJ, Joshi SB, McClean D, Peplinskie L, Toney K, Papac D, Li M, Middaugh CR (2007) Parathyroid hormone is a heparin/polyanion binding protein: Binding energetics and structure modification. Protein Sci 16:1193-1203
50. Gorr SU, Shioi J, Cohn DV (1989) Interaction of calcium with porcine adrenal chromogranin A (secretory protein-I) and chromogranin B (secretogranin I). Am J Physiol 257:E247-E254
51. Marmorstein AD, Csaky KG, Baffi J, Lam L, Rahaal F, Rodriguez-Boulan E (2000) Saturation of, and competition for entry into, the apical secretory pathway. Proc Natl Acad Sci USA 97:3248-3253
52. Parczyk K, Kondor-Koch C (1989) The influence of pH on the vesicular traffic to the surface of the polarized epithelial cell, MDCK. Eur J Cell Biol 48:353-359
53. Yoo SH (1993) pH-dependent association of chromogranin A with secretory vesicle membrane and a putative membrane binding region of chromogranin A. Biochemistry 32:8213-8219
54. Gottlieb TA, Beaudry G, Rizzolo L, Colman A, Rindler M, Adesnik M, Sabatini DD (1986) Secretion of endogenous and exogenous proteins from polarized MDCK cell monolayers. Proc Natl Acad Sci USA 83:2100-2104
55. Rindler M, Traber M (1988) A specific sorting signal is not required for the polarized secretion of newly synthesized proteins from cultured intestinal epithelial cells. J Cell Biol 107:471-479
56. Hendy GN, Bennett HP, Gibbs BF, Lazure C, Day R, Seidah NG (1995) Proparathyroid hormone is preferentially cleaved to parathyroid hormone by the prohormone convertase furin. A mass spectrometric study. J Biol Chem 270:9517-9525
57. Maruyama M, Kishimoto M, Ishida K, Watanabe Y, Nishikawa M, Masuda S, Sasaki R, Takakura Y (2005) Cholesterol is required for the polarized secretion of erythropoietin in Madin-Darby canine kidney cells. Arch Biochem Biophys 438:174-181
58. Marzolo MP, Bull P, Gonzalez A (1997) Apical sorting of hepatitis B surface antigen (HBsAg) is independent of N-glycosylation and glycosylphosphatidylinositol-anchored protein segregation. Proc Natl Acad Sci USA 94:1834-1839
59. Jain RK, Chang WT, Geetha C, Joyce PB, Gorr SU (2002) In vitro aggregation of the regulated secretory protein chromogranin A. Biochem J 13:605-610
60. Jain RK, Joyce PBM, Gorr S-U (2000) Aggregation chaperones enhance aggregation and storage of secretory proteins in endocrine cells. J Biol Chem 275:27032-27036