Sorting of membrane proteins to vacuoles in plant cells

Plant Science

Volumn 146, Issue 2, 1999, Pages 55-67

  Jiang, Liwen ^a   Rogers, John C ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Cytoplasmic tail; Integral membrane protein; Organelle; Reporter protein; Transmembrane domain; Transport vesicle

Indexed keywords

MEMBRANE PROTEIN;

CELL TRANSPORT; CELL VACUOLE; NONHUMAN; PLANT CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; SHORT SURVEY;

EID: 0033618851     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-9452(99)00069-2     Document Type: Article

References (90)

1. Okita T.W., Rogers J.C. Compartmentation of proteins in the endomembrane system of plant cells. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:1996;327-350.
2. Staehelin L. The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J. 11:1997;1151-1165.
3. Neuhaus J.-M., Rogers J.C. Sorting of proteins to vacuoles in plant cells. Plant Mol. Biol. 38:1998;127-144.
4. Paris N., Stanley C.M., Jones R.L., Rogers J.C. Plant cells contain two functionally distinct vacuolar compartments. Cell. 85:1996;563-572.
5. Robinson D.G., Hoh B., Hinz G., Jeong B.-K. One vacuole or two vacuoles: do protein storage vacuoles arise de novo during pea cotyledon development? J. Plant Physiol. 145:1995;654-664.
6. Jauh G.Y., Fisher A.M., Grimes H.G., Ryan C.A., Rogers J.C. Delta-tonoplast intrinsic protein defines unique plant vacuole function. Proc. Natl. Acad. Sci. USA. 95:1998;12995-12999.
7. G.Y. Jauh, T.E. Philips, J.C. Rogers, Tonoplast intrinsic protein isoforms as markers for vacuolar functions, Plant Cell 11 (1999) in press.
8. Matsuoka K., Bassham D.C., Raikhel N., Nakamura K. Different sensitivity to wortmannin of two vacuolar sorting signals indicates the presence of distinct sorting machineries in tobacco cells. J. Cell. Biol. 130:1995;1307-1318.
9. DiSansebastiano G.P., Paris N., MarcMartin S., Neuhaus J.M. Specific accumulation of GFP in a non-acidic vacuolar compartment via a C-terminal propeptide-mediated sorting pathway. Plant J. 15:1998;449-457.
10. Jiang L., Rogers J.C. Integral membrane protein sorting to vacuoles in plant cells: evidence for two pathways. J. Cell Biol. 143:1998;1183-1199.
11. Schroeder M.R., Borkhsenious O.N., Matsuoka K., Nakamura K., Raikhel N.V. Colocalization of barley lectin and sporamin in vacuoles of transgenic tobacco plants. Plant Physiol. 101:1993;451-458.
12. Paris N., Rogers S.W., Jiang L. et al. Molecular cloning and further characterization of a probable plant vacuolar sorting receptor. Plant Physiol. 115:1997;29-39.
13. Robinson D.G., Bäumer M., Hinz G., Hohl I. Vesicle transfer of storage proteins to the vacuole: the role of the Golgi apparatus and multivesicular bodies. J. Plant Physiol. 152:1998;659-667.
14. Chrispeels M.J., Raikhel N.V. Short peptide domains target proteins to plant vacuoles. Cell. 68:1992;613-616.
15. Nakamura K., Matsuoka K. Protein targeting to the vacuole in plant cells. Plant Physiol. 101:1993;1-6.
16. Robinson D.G., Hinz G., Holstein S.E.H. The molecular characterization of transport vesicles. Plant Mol. Biol. 38:1998;49-76.
17. Weimbs T., Low S.H., Chapin S.J., Mostov K.E., Bucher P., Hofmann K. A conserved domain is present in different families of vesicular fusion proteins: a new superfamily. Proc. Natl. Acad. Sci. USA. 94:1997;3046-3051.
18. Pfeffer S.R. Transport vesicle docking: SNAREs and associates. Annu. Rev. Cell Dev. Biol. 12:1996;441-461.
19. Schekman R., Orci L. Coat proteins and vesicle budding. Science. 271:1996;1526-1533.
20. Sollner J., Bennett M.K., Whiteheart S.W., Schelcer R.H., Rothman J.E. A protein assembly disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation and fusion. Cell. 75:1993;409-418.
21. Sollner T., Whiteheart S.W., Brunner M. et al. SNAP receptors implicated in vesicle targeting and fusion. Nature. 362:1993;318-324.
22. Holthuis J.C.M., Nichols B.J., Dhruvakumar S., Pelham H.R.B. Two syntaxin homologues in the TGN/endosomal system of yeast. EMBO J. 17:1998;113-126.
23. Nichols B.J., Pelham H.R.B. SNAREs and membrane fusion in the Golgi apparatus. Biochim. Biophys. Acta. 1404:1998;9-31.
24. Becherer K.A., Reider S., Emr S.D., Jones E.W. Novel syntaxin homologue, Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast. Mol. Biol. Cell. 7:1996;579-594.
25. Bassham D.C., Gal S., Conceicao A.S., Raikhel N.V. An Arobidopsis syntaxin homologue isolated by functional complementation of a yeast Pep12p mutant. Proc. Natl. Acad. Sci. USA. 92:1995;7262-7266.
26. Conceicao A., Marty-Mazars D., Bassham D.C., Sanderfoot A.A., Marty F., Raikhel N.V. The syntaxin homologue AtPEP12p resides on a late post-Golgi compartment in plants. Plant Cell. 9:1997;571-582.
27. Lukowitz W., Mayer U., Jurgens G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell. 84:1996;61-71.
28. Sato M.H., Nakamura N., Ohsumi Y. et al. The AtVAM3 encodes a syntaxin-related molecule implicated in the vacuolar assembly in Arabidopsis thaliana. J. Biol. Chem. 272:1997;24530-24535.
29. Darsow T., Rieder S.E., Emr S.D. A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J. Cell Biol. 138:1997;517-529.
30. Cowles C.R., Odorizzi G., Payne G.S., Emr S.D. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell. 91:1997;109-118.
31. Darsow T., Burd C.G., Emr S.D. Acidic di-leucine motif essential for AP-3-dependent sorting and restriction of the functional specificity of the Vam3p vacuolar t-SNARE. J. Cell Biol. 142:1998;913-922.
32. Yeh K.W., Chen J.C., Lin M.I., Chen Y.M., Lin C.Y. Functional activity of sporamin from sweet potato (Ipomoea batatas Lam.): a tuber storage protein with trypsin inhibitory activity. Plant Mol. Biol. 33:1997;565-570.
33. Hohl I., Robinson D.G., Chrispeels M.C., Hinz G. Transport of storage proteins to the vacuole is mediated by vesicles without a clathrin coat. J. Cell Sci. 109:1996;2539-2550.
34. Hara-Nishimura I., Shimada T., Hatano K., Takeuchi Y., Nishimura M. Transport of storage proteins to protein storage vacuoles is mediated by large precursor-accumulating vesicles. Plant Cell. 10:1998;825-836.
35. Kirchhausen T., Bonifacino J.S., Riezman H. Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol. 9:1997;488-495.
36. Ohno H., Stewart J., Fournier M.-C. et al. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science. 269:1995;1872-1875.
37. Bryant N.J., Piper R.C., Weisman L.S., Stevens T.H. Retrograde traffic out of the yeast vacuole to the TGN occurs via the prevacuole/endosome compartment. J. Cell Biol. 142:1998;651-663.
38. Cereghino J.L., Marcusson E.G., Emr S.D. The cytoplasmic tail domain of the vacuolar protein sorting receptor Vps10p and a subset of VPS gene products regulate receptor stability, function, and localization. Mol. Biol. Cell. 6:1995;1089-1102.
39. Cooper A.A., Stevens T.H. Vps10p cycles between the late-Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolyses. J. Cell Biol. 133:1996;529-541.
40. Kirsch T., Paris N., Butler J.M., Beevers L., Rogers J.C. Purification and initial characterization of a potential plant vacuolar targeting receptor. Proc Natl. Acad. Sci. USA. 91:1994;3403-3407.
41. Butler J.M., Kirsch T., Watson B., Paris N., Rogers J.C., Beevers L. Interaction of the vacuolar targeting receptor BP-80 with clathrin adaptors. Plant Physiol. 114:1997;237.
42. Ahmed S.U., Bar-Peled M., Raikhel N.V. Cloning and subcellular location of an Arabidopsis receptor-like protein that shares common features with protein-sorting receptors of eukaryotic cells. Plant Physiol. 114:1997;325-336.
43. Sanderfoot A.A., Ahmed S.U., Marty-Mazars D. et al. A putative vacuolar cargo receptor partially colocalizes with AtPEP12p on a prevacuolar compartment in Arabidopsis roots. Proc. Natl. Acad. Sci. USA. 95:1998;9920-9925.
44. Matsuoka K., Matsumoto S., Hattori T., Machida Y., Nakamura K. Vacuolar targeting and posttranslational processing of the precursor to the sweet potato tuberous root storage protein in heterologous plant cells. J. Biol. Chem. 265:1990;19750-19757.
45. Hoh B., Hinz G., Jeong B.-K., Robinson D.G. Protein storage vacuoles form de novo during pea cotyledon development. J. Cell Sci. 108:1995;299-310.
46. Hara-Nishimura I., Nishimura M., Akazawa T. Biosynthesis and intracellular transport of 11S globulin in developing pumpkin cotyledons. Plant Physiol. 77:1985;747-752.
47. Hara-Nishimura I., Shimada T., Hiraiwa N., Nishimura M. Vacuolar processing enzyme responsible for maturation of seed proteins. J. Plant Physiol. 145:1995;632-640.
48. Hara-Nishimura I., Takeuchi Y., Inoue K., Nishimura M. Vesicle transport and processing of the precursor to 2S albumin. Plant J. 4:1993;783-800.
49. Levanony H., Rubin R., Altschuler Y., Galili G. Evidence for a novel route of wheat storage proteins to vacuoles. J. Cell Biol. 119:1992;1117-1128.
50. Johnson K.D., Herman E.M., Chrispeels M.J. An abundant, highly conserved tonoplast protein in seeds. Plant Physiol. 91:1989;1006-1013.
51. Johnson K.D., Höfte H., Chrispeels M.J. An intrinsic tonoplast protein of protein storage vacuoles in seeds is structurally related to a bacterial solute transporter (GlpF). Plant Cell. 2:1990;525-532.
52. Höfte H., Chrispeels M.J. Protein sorting to the vacuolar membrane. Plant Cell. 4:1992;995-1004.
53. Gomez L., Chrispeels M.J. Tonoplast and soluble vacuolar proteins are targeted by different mechanisms. Plant Cell. 5:1993;1113-1124.
54. Klausner R.D., Donaldson J.G., Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116:1992;1071-1080.
55. Nothwehr S.F., Conibear E., Stevens T.H. Golgi and vacuolar membrane proteins reach the vacuole in vps1 mutant yeast cells via the plasma membrane. J. Cell Biol. 129:1995;35-46.
56. S.F. Nothwehr, C.J. Roberts, T.H. Stevens, Membrane protein retention in the yeast Golgi apparatus: dipeptidyl aminopeptidase A is retained by a cytoplasmic signal containing aromatic residues, J. Cell Biol. 121 (1993).
57. Nothwehr S.F., Stevens T.H. Sorting of membrane proteins in the yeast secretory pathway. J. Biol. Chem. 269:1994;10185-10188.
58. Lauriér M., Lauriér M.C., Chrispeels M.J., Johnson K.D., Sturm A. Characterization of a xylose-specific antiserum that reacts with the complex asparagine-linked glycans of extracellular and vacuolar glycoproteins. Plant Physiol. 90:1989;1182-1188.
59. Germain D., Zollinger L., Racine C. et al. The yeast Kex2-processing endoprotease is active in the Golgi apparatus of transfected NIH 3T3 fibroblasts. Mol. Endocrinol. 4:1990;1572-1579.
60. Thomas G., Thorne B.A., Thomas L. et al. Yeast KEX2 endopeptidase correctly cleaves a neuroendocrine prohormone in mammalian cells. Science. 241:1988;226-230.
61. Kinal H., Park C.-M., Berry J.O., Koltin Y., Bruenn J.A. Processing and secretion of a virally encoded antifungal toxin in transgenic tobacco plants: evidence for a Kex2p pathway in plants. Plant Cell. 7:1995;677-688.
62. Jiang L., Rogers J.C. Functional analysis of a Golgi-localized Kex2p-like protease in tobacco suspension culture cells. Plant J. 18:1999;23-32.
63. Roberts C.J., Nothwehr S.F., Stevens T.H. Membrane protein sorting in the yeast secretory pathway: evidence that the vacuole may be the default compartment. J. Cell Biol. 119:1992;63-83.
64. Bryant N.J., Stevens T.H. Vacuole biogenesis in Saccharomyces cerevisiae: protein transport pathways to the yeast vacuole. Microbiol. Mol. Biol. Rev. 62:1998;230-247.
65. Piper R.C., Bryant N.J., Stevens T.H. The membrane protein alkaline phosphatase is delivered to the vacuole by a route that is distinct from the VPS-dependent pathway. J. Cell Biol. 138:1997;531-545.
66. Honing S., Sandoval I.V., von Figura K. A di-leucine-based motif in the cytoplasmic tail of LIMP-II and tyrosinase mediates selective binding of AP-3. EMBO J. 17:1998;1304-1314.
67. Lanier L.L., Corliss B.C., Wu J., Leong C., Phillips J.H. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature. 391:1998;703-707.
68. +-pyrophosphatase by N,N′-dicyclohexylcarbodiimide. J. Biol. Chem. 272:1997;22340-22348.
69. Rayner J.C., Pelham H.R.B. Transmembrane domain-dependent sorting of proteins to the ER and plasma membrane in yeast. EMBO J. 16:1997;1832-1841.
70. Neuhaus J.-M., Sticher L., Meins F., Boller T. A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc. Natl. Acad. Sci. USA. 88:1991;10362-10366.
71. +-ATPase. Plant Physiol. 118:1998;137-147.
72. +-ATPase in a nonvacuolar organelle is required for the sorting of soluble vacuolar protein precursors in tobacco cells. Plant Cell. 9:1997;533-546.
73. +-ATPase in mutants lacking one subunit of the enzyme. J. Biol. Chem. 268:1993;16845-16851.
74. +-ATPase subunit required for activity but not assembly of the enzyme complex in Saccharomyces cerevisiae. J. Biol. Chem. 268:1993;18286-18292.
75. Kane P.M., Kuehn M.C., Howaldstevenson I., Stevens T.H. Assembly and targeting of peripheral and integral membrane subunits of the yeast vacuolar H+-ATPase. J. Biol. Chem. 267:1992;447-454.
76. +-ATPase occurs in the endoplasmic reticulum and requires a Vma12p/Vma22p assembly complex. J. Cell Biol. 142:1998;39-49.
77. +-ATPase from oat seedling. Plant Cell. 10:1998;119-130.
78. +-ATPases are associated with the endoplasmic reticulum and provacuoles of root tip cells. Plant Physiol. 106:1994;1313-1324.
79. Oberbeck K., Drucker M., Robinson D.G. V-type ATPase and pyrophosphatase in endomembranes of maize roots. J. Exp. Bot. 45:1994;235-244.
80. Kim E.J., Zhen R.G., Rea P.A. Heterologous expression of plant vacuolar pyrophosphatase in yeast demonstrates sufficiency of substrate-binding subunit for transport. Proc. Natl. Acad. Sci. USA. 91:1994;6128-6132.
81. +-translocating pyrophosphatase is induced by anoxia of chilling in seedlings of rice. Plant Physiol. 108:1995;641-649.
82. +-pyrophosphatase in tonoplast vesicles from maize coleoptiles and seeds. Plant Physiol. 116:1998;1487-1495.
83. Maeshima M. Characterization of the major integral protein of vacuolar membrane. Plant Physiol. 98:1992;1248-1254.
84. +-ATPase during reformation of the central vacuole in germinating pumpkin seeds. Plant Physiol. 106:1994;61-69.
85. Rad M.R., Katz H. Retention of a co-translational translocated mutant protein of carboxypeptidase Y of Saccharomyces cerevisiae in endoplasmic reticulum. MS Microbiol. Lett. 111:1993;165-170.
86. Robinson D.G., Haschke H.-P., Hinz G., Hoh B., Maeshima M., Marty F. Immunological detection of tonoplast polypeptides in the plasma membrane of pea cotyledons. Planta. 198:1996;95-103.
87. Jefferson R.A., Kavanaugh T.A., Bevan M.W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6:1987;3901-3907.
88. Holwerda B.C., Galvin N.J., Baranski T.J., Rogers J.C. In vitro processing of aleurain, a barley vacuolar thiol protease. Plant Cell. 2:1990;1091-1106.
89. Holwerda B.C., Padgett H.S., Rogers J.C. Proaleurain vacuolar targeting is mediated by short contiguous peptide interactions. Plant Cell. 4:1992;307-318.
90. Robinson D.G., Bäumer M., Hinz G., Hohl I. Vesicle transfer of storage proteins to the vacoule: the role of the Golgi apparatus and multivesicular bodies. J. Plant Physiol. 152:1998;659-667.