Direct imaging of Rab27b-enriched secretory vesicle biogenesis in lacrimal acinar cells reveals origins on a nascent vesicle budding site

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Chiang, Lilian ^a   Karvar, Serhan ^b   Hamm Alvarez, Sarah F ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; GUANINE NUCLEOTIDE BINDING PROTEIN; MOLECULAR MOTOR; MYOSIN 5C; NOCODAZOLE; PROTEIN RAB27B; UNCLASSIFIED DRUG; HYBRID PROTEIN; MYOSIN; RAB PROTEIN;

ACINAR CELL; ANIMAL CELL; ARTICLE; BIOGENESIS; CELL ORGANELLE; CONTROLLED STUDY; CYTOPLASM; FEMALE; FLUORESCENCE MICROSCOPY; GENE AMPLIFICATION; NONHUMAN; PROTEIN LOCALIZATION; RABBIT; SECRETORY VESICLE; TRANS GOLGI NETWORK; VIRUS RECOMBINANT; ANIMAL; BIOLOGICAL MODEL; CELL COMPARTMENTALIZATION; CYTOLOGY; GOLGI COMPLEX; LACRIMAL APPARATUS; METABOLISM; METHODOLOGY; MICROTUBULE; PROTEIN BINDING; THREE DIMENSIONAL IMAGING; TRANSPORT AT THE CELLULAR LEVEL;

ACINAR CELLS; ANIMALS; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; FEMALE; GOLGI APPARATUS; IMAGING, THREE-DIMENSIONAL; LACRIMAL APPARATUS; MICROTUBULES; MODELS, BIOLOGICAL; MYOSINS; PROTEIN BINDING; RAB GTP-BINDING PROTEINS; RABBITS; RECOMBINANT FUSION PROTEINS; SECRETORY VESICLES;

EID: 84857401098     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031789     Document Type: Article

References (71)

1. Fullard RJ, Snyder C, (1990) Protein levels in nonstimulated and stimulated tears of normal human subjects. Invest Ophthalmol Vis Sci 31: 1119-1126.
2. de Souza GA, Godoy LM, Mann M, (2006) Identification of 491 proteins in the tear fluid proteome reveals a large number of proteases and protease inhibitors. Genome Biol 7: R72.
3. Sanghi S, Kumar R, Lumsden A, Dickinson D, Klepeis V, et al. (2001) cDNA and genomic cloning of lacritin, a novel secretion enhancing factor from the human lacrimal gland. J Mol Biol 310: 127-139.
4. van Setten GB, Viinikka L, Tervo T, Pesonen K, Tarkkanen A, et al. (1989) Epidermal growth factor is a constant component of normal human tear fluid. Graefes Arch Clin Exp Ophthalmol 227: 184-187.
5. Jerdeva GV, Wu K, Yarber FA, Rhodes CJ, Kalman D, et al. (2005a) Actin and non-muscle myosin II facilitate apical exocytosis of tear proteins in rabbit lacrimal acinar epithelial cells. J Cell Sci 118: 4797-4812.
6. Marchelletta RR, Jacobs DT, Schechter JE, Cheney RE, Hamm-Alvarez SF, (2008) The Class V myosin motor, Myosin 5c, localizes to mature secretory vesicles and facilitates exocytosis in lacrimal acini. Am J Physiol Cell Physiol 295: C13-28.
7. Jedd G, Richardson C, Litt R, Segev N, (1995) The Ypt1 GTPase is essential for the first two steps of the yeast secretory pathway. J Cell Biol 131: 583-590.
8. Baker D, Wuestehube L, Schekman R, Botstein D, Segev N, (1990) GTP-binding Ypt1 protein and Ca2+ function independently in a cell-free protein transport reaction. Proc Natl Acad Sci U S A 87: 355-359.
9. Wang Y, Jerdeva G, Yarber FA, da Costa SR, Xie J, et al. (2003) Cytoplasmic dynein participates in apically targeted stimulated secretory traffic in primary rabbit lacrimal acinar epithelial cells. J Cell Sci 116: 2051-2065.
10. Valentijn JA, Valentijn K, Pastore LM, Jamieson JD, (2000) Actin coating of secretory granules during regulated exocytosis correlates with the release of rab3D. Proc Natl Acad Sci U S A 97: 1091-1095.
11. Yoshie S, Imai A, Nashida T, Shimomura H, (2000) Expression, characterization, and localization of Rab26, a low molecular weight GTP-binding protein, in the rat parotid gland. Histochem Cell Biol 113: 259-263.
12. Pickett JA, Edwardson JM, (2006) Compound exocytosis: mechanisms and functional significance. Traffic 7: 109-116.
13. Apodaca G, (2001) Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2: 149-159.
14. Valentijn KM, Gumkowski FD, Jamieson JD, (1999) The subapical actin cytoskeleton regulates secretion and membrane retrieval in pancreatic acinar cells. J Cell Sci 112 (Pt 1): 81-96.
15. D'Souza-Schorey C, Chavrier P, (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7: 347-358.
16. Davidson HW, Balch WE, (1993) Differential inhibition of multiple vesicular transport steps between the endoplasmic reticulum and trans Golgi network. J Biol Chem 268: 4216-4226.
17. Miserey-Lenkei S, Chalancon G, Bardin S, Formstecher E, Goud B, et al. Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat Cell Biol 12: 645-654.
18. da Costa SR, Yarber FA, Zhang L, Sonee M, Hamm-Alvarez SF, (1998) Microtubules facilitate the stimulated secretion of beta-hexosaminidase in lacrimal acinar cells. J Cell Sci 111 (Pt 9): 1267-1276.
19. Fath KR, Trimbur GM, Burgess DR, (1994) Molecular motors are differentially distributed on Golgi membranes from polarized epithelial cells. J Cell Biol 126: 661-675.
20. Wu K, Jerdeva GV, da Costa SR, Sou E, Schechter JE, et al. (2006) Molecular mechanisms of lacrimal acinar secretory vesicle exocytosis. Exp Eye Res 83: 84-96.
21. Wu X, Bowers B, Wei Q, Kocher B, Hammer JA 3rd, (1997) Myosin V associates with melanosomes in mouse melanocytes: evidence that myosin V is an organelle motor. J Cell Sci 110 (Pt 7): 847-859.
22. Lapierre LA, Goldenring JR, (2005) Interactions of myosin vb with rab11 family members and cargoes traversing the plasma membrane recycling system. Methods Enzymol 403: 715-723.
23. Lise MF, Wong TP, Trinh A, Hines RM, Liu L, et al. (2006) Involvement of myosin Vb in glutamate receptor trafficking. J Biol Chem 281: 3669-3678.
24. Nedvetsky PI, Stefan E, Frische S, Santamaria K, Wiesner B, et al. (2007) A Role of myosin Vb and Rab11-FIP2 in the aquaporin-2 shuttle. Traffic 8: 110-123.
25. Jacobs DT, Weigert R, Grode KD, Donaldson JG, Cheney RE, (2009) Myosin Vc is a molecular motor that functions in secretory granule trafficking. Mol Biol Cell 20: 4471-4488.
26. Pereira-Leal JB, Seabra MC, (2001) Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 313: 889-901.
27. Seabra MC, Mules EH, Hume AN, (2002) Rab GTPases, intracellular traffic and disease. Trends Mol Med 8: 23-30.
28. Wu H, Rossi G, Brennwald P, (2008) The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends Cell Biol 18: 397-404.
29. Seabra MC, Coudrier E, (2004) Rab GTPases and myosin motors in organelle motility. Traffic 5: 393-399.
30. Grosshans BL, Ortiz D, Novick P, (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 103: 11821-11827.
31. Schluter OM, Khvotchev M, Jahn R, Sudhof TC, (2002) Localization versus function of Rab3 proteins. Evidence for a common regulatory role in controlling fusion. J Biol Chem 277: 40919-40929.
32. Evans E, Zhang W, Jerdeva G, Chen CY, Chen X, et al. (2008) Direct interaction between Rab3D and the polymeric immunoglobulin receptor and trafficking through regulated secretory vesicles in lacrimal gland acinar cells. Am J Physiol Cell Physiol 294: C662-674.
33. Riedel D, Antonin W, Fernandez-Chacon R, Alvarez de Toledo G, Jo T, et al. (2002) Rab3D is not required for exocrine exocytosis but for maintenance of normally sized secretory granules. Mol Cell Biol 22: 6487-6497.
34. Chen X, Edwards JA, Logsdon CD, Ernst SA, Williams JA, (2002) Dominant negative Rab3D inhibits amylase release from mouse pancreatic acini. J Biol Chem 277: 18002-18009.
35. Nguyen D, Jones A, Ojakian GK, Raffaniello RD, (2003) Rab3D redistribution and function in rat parotid acini. J Cell Physiol 197: 400-408.
36. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, et al. (2010) Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12: 19-30; sup pp 11-13.
37. Chen D, Guo J, Miki T, Tachibana M, Gahl WA, (1997) Molecular cloning and characterization of rab27a and rab27b, novel human rab proteins shared by melanocytes and platelets. Biochem Mol Med 60: 27-37.
38. Chen X, Li C, Izumi T, Ernst SA, Andrews PC, et al. (2004) Rab27b localizes to zymogen granules and regulates pancreatic acinar exocytosis. Biochem Biophys Res Commun 323: 1157-1162.
39. Imai A, Yoshie S, Nashida T, Shimomura H, Fukuda M, (2004) The small GTPase Rab27B regulates amylase release from rat parotid acinar cells. J Cell Sci 117: 1945-1953.
40. Imai A, Yoshie S, Nashida T, Fukuda M, Shimomura H, (2009) Redistribution of small GTP-binding protein, Rab27B, in rat parotid acinar cells after stimulation with isoproterenol. Eur J Oral Sci 117: 224-230.
41. Chiang L, Ngo J, Schechter JE, Karvar S, Tolmachova T, et al. (2011) Rab27b regulates exocytosis of secretory vesicles in acinar epithelial cells from the lacrimal gland. Am J Physiol Cell Physiol 301: C507-521.
42. Tolmachova T, Abrink M, Futter CE, Authi KS, Seabra MC, (2007) Rab27b regulates number and secretion of platelet dense granules. Proc Natl Acad Sci U S A 104: 5872-5877.
43. Gomi H, Mori K, Itohara S, Izumi T, (2007) Rab27b is expressed in a wide range of exocytic cells and involved in the delivery of secretory granules near the plasma membrane. Mol Biol Cell 18: 4377-4386.
44. Jerdeva GV, Yarber FA, Trousdale MD, Rhodes CJ, Okamoto CT, et al. (2005b) Dominant-negative PKC-epsilon impairs apical actin remodeling in parallel with inhibition of carbachol-stimulated secretion in rabbit lacrimal acini. Am J Physiol Cell Physiol 289: C1052-1068.
45. Kraemer J, Schmitz F, Drenckhahn D, (1999) Cytoplasmic dynein and dynactin as likely candidates for microtubule-dependent apical targeting of pancreatic zymogen granules. Eur J Cell Biol 78: 265-277.
46. Vaughan KT, (2005) Microtubule plus ends, motors, and traffic of Golgi membranes. Biochim Biophys Acta 1744: 316-324.
47. Gill SR, Schroer TA, Szilak I, Steuer ER, Sheetz MP, et al. (1991) Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J Cell Biol 115: 1639-1650.
48. Qian L, Xie J, Rose CM, Sou E, Zeng H, et al. (2004) Altered traffic to the lysosome in an ex vivo lacrimal acinar cell model for chronic muscarinic receptor stimulation. Exp Eye Res 79: 665-675.
49. Busson-Mabillot S, Chambaut-Guerin AM, Ovtracht L, Muller P, Rossignol B, (1982) Microtubules and protein secretion in rat lacrimal glands: localization of short-term effects of colchicine on the secretory process. J Cell Biol 95: 105-117.
50. Robin P, Rossignol B, Raymond MN, (1995) Effect of microtubule network disturbance by nocodazole and docetaxel (Taxotere) on protein secretion in rat extraorbital lacrimal and parotid glands. Eur J Cell Biol 67: 227-237.
51. Goud B, Gleeson PA, (2010) TGN golgins, Rabs and cytoskeleton: regulating the Golgi trafficking highways. Trends Cell Biol 20: 329-336.
52. Pfeffer SR, (2007) Unsolved mysteries in membrane traffic. Annu Rev Biochem 76: 629-645.
53. Yoshino A, Bieler BM, Harper DC, Cowan DA, Sutterwala S, et al. (2003) A role for GRIP domain proteins and/or their ligands in structure and function of the trans Golgi network. J Cell Sci 116: 4441-4454.
54. Wong DH, Brodsky FM, (1992) 100-kD proteins of Golgi- and trans-Golgi network-associated coated vesicles have related but distinct membrane binding properties. J Cell Biol 117: 1171-1179.
55. Derby MC, van Vliet C, Brown D, Luke MR, Lu L, et al. (2004) Mammalian GRIP domain proteins differ in their membrane binding properties and are recruited to distinct domains of the TGN. J Cell Sci 117: 5865-5874.
56. Kogel T, Gerdes HH, (2010) Maturation of secretory granules. Results Probl Cell Differ 50: 1-20.
57. White T, Bennett EP, Takio K, Sorensen T, Bonding N, et al. (1995) Purification and cDNA cloning of a human UDP-N-acetyl-alpha-D-galactosamine:polypeptide N-acetylgalactosaminyltransferase. J Biol Chem 270: 24156-24165.
58. Rottger S, White J, Wandall HH, Olivo JC, Stark A, et al. (1998) Localization of three human polypeptide GalNAc-transferases in HeLa cells suggests initiation of O-linked glycosylation throughout the Golgi apparatus. J Cell Sci 111 (Pt 1): 45-60.
59. Hume AN, Collinson LM, Rapak A, Gomes AQ, Hopkins CR, et al. (2001) Rab27a regulates the peripheral distribution of melanosomes in melanocytes. J Cell Biol 152: 795-808.
60. Hume AN, Tarafder AK, Ramalho JS, Sviderskaya EV, Seabra MC, (2006) A coiled-coil domain of melanophilin is essential for Myosin Va recruitment and melanosome transport in melanocytes. Mol Biol Cell 17: 4720-4735.
61. Izumi T, Gomi H, Kasai K, Mizutani S, Torii S, (2003) The roles of Rab27 and its effectors in the regulated secretory pathways. Cell Struct Funct 28: 465-474.
62. Kuroda TS, Itoh T, Fukuda M, (2005) Functional analysis of slac2-a/melanophilin as a linker protein between Rab27A and myosin Va in melanosome transport. Methods Enzymol 403: 419-431.
63. Wu X, Rao K, Bowers MB, Copeland NG, Jenkins NA, et al. (2001) Rab27a enables myosin Va-dependent melanosome capture by recruiting the myosin to the organelle. J Cell Sci 114: 1091-1100.
64. Fukuda M, (2006) Distinct Rab27A binding affinities of Slp2-a and Slac2-a/melanophilin: Hierarchy of Rab27A effectors. Biochem Biophys Res Commun 343: 666-674.
65. Vilalta PM, Zhang L, Hamm-Alvarez SF, (1998) A novel taxol-induced vimentin phosphorylation and stabilization revealed by studies on stable microtubules and vimentin intermediate filaments. J Cell Sci 111 (Pt 13): 1841-1852.
66. Gierow JP, Yang T, Bekmezian A, Liu N, Norian JM, et al. (1996) Na-K-ATPase in lacrimal gland acinar cell endosomal system: correcting a case of mistaken identity. Am J Physiol 271: C1685-1698.
67. Gierow JP, Lambert RW, Mircheff AK, (1995) Fluid phase endocytosis by isolated rabbit lacrimal gland acinar cells. Exp Eye Res 60: 511-525.
68. da Costa SR, Andersson S, Arber F, Okamoto C, Hamm-Alvarez S, (2002) Cytoskeletal participation in stimulated secretion and compensatory apical plasma membrane retrieval in lacrimal gland acinar cells. Adv Exp Med Biol 506: 199-205.
69. Suda J, Zhu L, Okamoto C, Karvar S, (2010) (in press)) Cellular distribution and functional importance of Rab27b in gastric parietal cells. Gastroenterology.
70. Rodriguez OC, Cheney RE, (2002) Human myosin-Vc is a novel class V myosin expressed in epithelial cells. J Cell Sci 115: 991-1004.
71. Xie J, Chiang L, Contreras J, Wu K, Garner JA, et al. (2006) Novel fiber-dependent entry mechanism for adenovirus serotype 5 in lacrimal acini. J Virol 80: 11833-11851.