Tail-anchored membrane proteins: Exploring the complex diversity of tail-anchored-protein targeting in plant cells

Plant Cell Reports

Volumn 30, Issue 2, 2011, Pages 137-151

  Abell, Ben M ^a   Mullen, Robert T ^b  

^a SHEFFIELD HALLAM UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Biogenesis; Membrane; Organelle; Protein trafficking; Tail anchored

Indexed keywords

MAMMALIA;

EID: 78651420040     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-010-0925-6     Document Type: Review

References (117)

1. Abell BM, Jung M, Oliver JD, Knight BC, Tyedmers J, Zimmermann R, High S (2003) Tail-anchored and signal-anchored proteins utilize overlapping pathways during membrane insertion. J Biol Chem 278: 5669-5678.
2. Abell BM, Hahn M, Holbrook LA, Moloney MM (2004) Membrane topology and sequence requirements for oil body targeting of oleosin. Plant J 37: 461-470.
3. Abell BM, Rabu C, Leznicki P, Young JC, High S (2007) Post-translational integration of tail-anchored proteins is facilitated by defined molecular chaperones. J Cell Sci 120: 1743-1751.
4. Annis MG, Soucie EL, Dlugosz PJ, Cruz-Aguado JA, Penn LZ, Leber B, Andrews DW (2005) Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J 24: 2096-2103.
5. Aung K, Zhang X, Hu J (2010) Peroxisome division and proliferation in plants. Biochem Soc Trans 38: 817-822.
6. Bae W, Lee YJ, Kim DH, Lee J, Kim S, Sohn EJ, Hwang I (2008) AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nat Cell Biol 10: 220-227.
7. Bailly A, Sovero V, Geisler M (2006) The twisted dwarf's ABC: how immunophilins regulate auxin transport. Plant Signal Behav 1: 277-280.
8. Barbante A, Irons S, Hawes C, Frigerio L, Vitale A, Pedrazzini E (2008) Anchorage to the cytosolic face of the endoplasmic reticulum membrane: a new strategy to stabilize a cytosolic recombinant antigen in plants. Plant Biotechnol J 6: 560-575.
9. Bassham DC, Blatt MR (2008) SNAREs: cogs and coordinators in signaling and development. Plant Physiol 147: 1504-1515.
10. Beilharz T, Egan B, Silver PA, Hofmann K, Lithgow T (2003) Bipartite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae. J Biol Chem 278: 8219-8223.
11. Blobel G (1980) Intracellular protein topogenesis. Proc Natl Acad Sci USA 77: 1496-1500.
12. Borgese N, Fasana E (2010) Targeting pathways of C-tail-anchored proteins. Biochim Biophys Acta. doi: 10. 1016/j. bbamem. 2010. 07. 10.
13. Borgese N, Righi M (2010) Remote origins of tail-anchored proteins. Traffic 11: 877-885.
14. Borgese N, Colombo S, Pedrazzini E (2003) The tale of tail-anchored proteins: coming from the cytosol and looking for a membrane. J Cell Biol 161: 1013-1019.
15. Borgese N, Brambillasca S, Colombo S (2007) How tails guide tail-anchored proteins to their destinations. Curr Opin Cell Biol 19: 368-375.
16. Bozkurt G, Stjepanovic G, Vilardi F, Amlacher S, Wild K, Bange G, Favaloro V, Rippe K, Hurt E, Dobberstein B, Sinning I (2009) Structural insights into tail-anchored protein binding and membrane insertion by Get3. Proc Natl Acad Sci USA 106: 21131-21136.
17. Brambillasca S, Yabal M, Soffientini P, Stefanovic S, Makarow M, Hegde RS, Borgese N (2005) Transmembrane topogenesis of a tail-anchored protein is modulated by membrane lipid composition. EMBO J 24: 2533-2542.
18. Brambillasca S, Yabal M, Makarow M, Borgese N (2006) Unassisted translocation of large polypeptide domains across phospholipid bilayers. J Cell Biol 175: 767-777.
19. Brkljacic J, Zhao Q, Meier I (2009) WPP-domain proteins mimic the activity of the HSC70-1 chaperone in preventing mistargeting of RanGAP1-anchoring protein WIT1. Plant Physiol 151: 142-154.
20. Chang YW, Chuang YC, Ho YC, Cheng MY, Sun YJ, Hsiao CD, Wang C (2010) Crystal structure of Get4-Get5 complex and its interactions with Sgt2, Get3, and Ydj1. J Biol Chem 285: 9962-9970.
21. Chartron JW, Suloway CJ, Zaslaver M, Clemons WM Jr (2010) Structural characterization of the Get4/Get5 complex and its interaction with Get3. Proc Natl Acad Sci USA 107: 12127-12132.
22. Choi SB, Wang C, Muench DG, Ozawa K, Franceschi VR, Wu Y, Okita TW (2000) Messenger RNA targeting of rice seed storage proteins to specific ER subdomains. Nature 407: 765-767.
23. Colombo SF, Longhi R, Borgese N (2009) The role of cytosolic proteins in the insertion of tail-anchored proteins into phospholipid bilayers. J Cell Sci 122: 2383-2392.
24. 5 is required for full activity of flavonoid 3′, 5′-hydroxylase, a cytochrome P450 involved in the formation of blue flower colors. Proc Natl Acad Sci USA 96: 778-783.
25. del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53: 1255-1272.
26. Delille HK, Schrader M (2008) Targeting of hFis1 to peroxisomes is mediated by Pex19p. J Biol Chem 283: 31107-31115.
27. Dhanoa PK, Richardson LG, Smith MD, Gidda SK, Henderson MP, Andrews DW, Mullen RT (2010) Distinct pathways mediate the sorting of tail-anchored proteins to the plastid outer envelope. PLoS One 5: e10098.
28. Donaldson RP (2002) Peroxisomal membrane enzymes. In: Baker A, Graham IA (eds) Plant peroxisomes: biochemistry, cell biology, and biotechnological applications. Kluwer Academic Publishers, Dordrecht, pp 259-278.
29. Fagarasanu A, Fagarasanu M, Rachubinski RA (2007) Maintaining peroxisome populations: a story of division and inheritance. Annu Rev Cell Dev Biol 23: 321-344.
30. 5 to regulate their affinity for substrate sugars. Plant Physiol 150: 1880-1901.
31. Flanagan JJ, Chen JC, Miao Y, Shao Y, Lin J, Bock PE, Johnson AE (2003) Signal recognition particle binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J Biol Chem 278: 18628-18637.
32. Freiin Loeffelholz von Colberg CO, Kriechbaumer V, Ewan RA, Jonczyk R, Lehmann S, Young JC, Abell BM (2010) OEP61 is a novel chaperone receptor at the chloroplast outer envelope in Arabidopsis. Manuscript in preparation.
33. Grudnik P, Bange G, Sinning I (2009) Protein targeting by the signal recognition particle. Biol Chem 390: 775-782.
34. Gutensohn M, Schulz B, Nicolay P, Flugge UI (2000) Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. Plant J 23: 771-783.
35. Halbach A, Landgraf C, Lorenzen S, Rosenkranz K, Volkmer-Engert R, Erdmann R, Rottensteiner H (2006) Targeting of the tail-anchored peroxisomal membrane proteins PEX26 and PEX15 occurs through C-terminal PEX19-binding sites. J Cell Sci 119: 2508-2517.
36. Henderson MP, Billen LP, Kim PK, Andrews DW (2007a) Cell-free analysis of tail-anchor protein targeting to membranes. Methods 41: 427-438.
37. 5 confers endoplasmic reticulum specificity by preventing spontaneous insertion into membranes. Biochem J 401: 701-709.
38. High S, Abell BM (2004) Tail-anchored protein biosynthesis at the endoplasmic reticulum: the same but different. Biochem Soc Trans 32: 659-662.
39. Hofmann NR, Theg SM (2005) Chloroplast outer membrane protein targeting and insertion. Trends Plant Sci 10: 450-457.
40. Honsbein A, Sokolovski S, Grefen C, Campanoni P, Pratelli R, Paneque M, Chen Z, Johansson I, Blatt MR (2009) A tripartite SNARE-K+ channel complex mediates in channel-dependent K+ nutrition in Arabidopsis. Plant Cell 21: 2859-2877.
41. 5 to either endoplasmic reticulum or mitochondria. Plant Cell 16: 3002-3019.
42. Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72: 1143-1154.
43. Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102: 5280-5285.
44. Janiak F, Leber B, Andrews DW (1994) Assembly of Bcl-2 into microsomal and outer mitochondrial membranes. J Biol Chem 269: 9842-9849.
45. Jarvis P, Chen LJ, Li H, Peto CA, Fankhauser C, Chory J (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282: 100-103.
46. Jespersen HM, Kjaersgard IV, Ostergaard L, Welinder KG (1997) From sequence analysis of three novel ascorbate peroxidases from Arabidopsis thaliana to structure, function and evolution of seven types of ascorbate peroxidase. Biochem J 326(Pt 2): 305-310.
47. Kajander T, Sachs JN, Goldman A, Regan L (2009) Electrostatic interactions of Hsp-organizing protein tetratricopeptide domains with Hsp70 and Hsp90: computational analysis and protein engineering. J Biol Chem 284: 25364-25374.
48. Kalbfleisch T, Cambon A, Wattenberg BW (2007) A bioinformatics approach to identifying tail-anchored proteins in the human genome. Traffic 8: 1687-1694.
49. Karnik SK, Trelease RN (2005) Arabidopsis peroxin 16 coexists at steady state in peroxisomes and endoplasmic reticulum. Plant Physiol 138: 1967-1981.
50. Karyotou K, Donaldson RP (2005) Ascorbate peroxidase, a scavenger of hydrogen peroxide in glyoxysomal membranes. Arch Biochem Biophys 434: 248-257.
51. Kaur N, Hu J (2009) Dynamics of peroxisome abundance: a tale of division and proliferation. Curr Opin Plant Biol 12: 781-788.
52. Kemper C, Habib SJ, Engl G, Heckmeyer P, Dimmer KS, Rapaport D (2008) Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components. J Cell Sci 121: 1990-1998.
53. Kessler F, Schnell D (2009) Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Curr Opin Cell Biol 21: 494-500.
54. Kim SG, Park CM (2007a) Membrane-mediated salt stress signaling in flowering time control. Plant Signal Behav 2: 517-518.
55. Kim YS, Park CM (2007b) Membrane regulation of cytokinin-mediated cell division in Arabidopsis. Plant Signal Behav 2: 15-16.
56. Kim PK, Janiak-Spens F, Trimble WS, Leber B, Andrews DW (1997) Evidence for multiple mechanisms for membrane binding and integration via carboxyl-terminal insertion sequences. Biochemistry 36: 8873-8882.
57. Kim PK, Hollerbach C, Trimble WS, Leber B, Andrews DW (1999) Identification of the endoplasmic reticulum targeting signal in vesicle-associated membrane proteins. J Biol Chem 274: 36876-36882.
58. Kim PK, Annis MG, Dlugosz PJ, Leber B, Andrews DW (2004) During apoptosis bcl-2 changes membrane topology at both the endoplasmic reticulum and mitochondria. Mol Cell 14: 523-529.
59. Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18: 3132-3144.
60. Kriechbaumer V, Shaw R, Mukherjee J, Bowsher CG, Harrison AM, Abell BM (2009) Subcellular distribution of tail-anchored proteins in Arabidopsis. Traffic 10: 1753-1764.
61. Kutay U, Hartmann E, Rapoport TA (1993) A class of membrane proteins with a C-terminal anchor. Trends Cell Biol 3: 72-75.
62. Lee J, Wang F, Schnell DJ (2009) Toc receptor dimerization participates in the initiation of membrane translocation during protein import into chloroplasts. J Biol Chem 284: 31130-31141.
63. Leznicki P, Clancy A, Schwappach B, High S (2010) Bat3 promotes the membrane integration of tail-anchored proteins. J Cell Sci 123: 2170-2178.
64. Li H, Chen LJ (1997) A novel chloroplastic outer membrane-targeting signal that functions at both termini of passenger polypeptides. J Biol Chem 272: 10968-10974.
65. Li J, Qian X, Hu J, Sha B (2009) Molecular chaperone Hsp70/Hsp90 prepares the mitochondrial outer membrane translocon receptor Tom71 for preprotein loading. J Biol Chem 284: 23852-23859.
66. Lindner R, Naim HY (2009) Domains in biological membranes. Exp Cell Res 315: 2871-2878.
67. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Llorente F, Molina A, Parker J, Somerville S, Schulze-Lefert P (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180-1183.
68. Lipka V, Kwon C, Panstruga R (2007) SNARE-ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 23: 147-174.
69. Lisenbee CS, Heinze M, Trelease RN (2003) Peroxisomal ascorbate peroxidase resides within a subdomain of rough endoplasmic reticulum in wild-type Arabidopsis cells. Plant Physiol 132: 870-882.
70. Lisenbee CS, Lingard MJ, Trelease RN (2005) Arabidopsis peroxisomes possess functionally redundant membrane and matrix isoforms of monodehydroascorbate reductase. Plant J 43: 900-914.
71. Lister R, Carrie C, Duncan O, Ho LH, Howell KA, Murcha MW, Whelan J (2007) Functional definition of outer membrane proteins involved in preprotein import into mitochondria. Plant Cell 19: 3739-3759.
72. Macasev D, Newbigin E, Whelan J, Lithgow T (2000) How do plant mitochondria avoid importing chloroplast proteins? Components of the import apparatus Tom20 and Tom22 from Arabidopsis differ from their fungal counterparts. Plant Physiol 123: 811-816.
73. Macasev D, Whelan J, Newbigin E, Silva-Filho MC, Mulhern TD, Lithgow T (2004) Tom22', an 8-kDa trans-site receptor in plants and protozoans, is a conserved feature of the TOM complex that appeared early in the evolution of eukaryotes. Mol Biol Evol 21: 1557-1564.
74. 5 in plants: a comparative study using different isoforms from rabbit and Arabidopsis. J Exp Bot 58: 1365-1379.
75. Mateja A, Szlachcic A, Downing ME, Dobosz M, Mariappan M, Hegde RS, Keenan RJ (2009) The structural basis of tail-anchored membrane protein recognition by Get3. Nature 461: 361-366.
76. Matsuzono Y, Fujiki Y (2006) In vitro transport of membrane proteins to peroxisomes by shuttling receptor Pex19p. J Biol Chem 281: 36-42.
77. May T, Soll J (2000) 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12: 53-64.
78. Michaud M, Marechal-Drouard L, Duchene AM (2010) RNA trafficking in plant cells: targeting of cytosolic mRNAs to the mitochondrial surface. Plant Mol Biol 73: 697-704.
79. Motz C, Martin H, Krimmer T, Rassow J (2002) Bcl-2 and porin follow different pathways of TOM-dependent insertion into the mitochondrial outer membrane. J Mol Biol 323: 729-738.
80. Mullen RT, Trelease RN (2000) The sorting signals for peroxisomal membrane-bound ascorbate peroxidase are within its C-terminal tail. J Biol Chem 275: 16337-16344.
81. Mullen RT, Trelease RN (2006) The ER-peroxisome connection in plants: development of the "ER semi-autonomous peroxisome maturation and replication" model for plant peroxisome biogenesis. Biochim Biophys Acta 1763: 1655-1668.
82. Mullen RT, Lisenbee CS, Miernyk JA, Trelease RN (1999) Peroxisomal membrane ascorbate peroxidase is sorted to a membranous network that resembles a subdomain of the endoplasmic reticulum. Plant Cell 11: 2167-2185.
83. Nyathi Y, Baker A (2006) Plant peroxisomes as a source of signalling molecules. Biochim Biophys Acta 1763: 1478-1495.
84. Obara K, Sumi K, Fukuda H (2002) The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts. Plant Cell Physiol 43: 697-705.
85. Otera H, Taira Y, Horie C, Suzuki Y, Suzuki H, Setoguchi K, Kato H, Oka T, Mihara K (2007) A novel insertion pathway of mitochondrial outer membrane proteins with multiple transmembrane segments. J Cell Biol 179: 1355-1363.
86. Paquette SM, Jensen K, Bak S (2009) A web-based resource for the Arabidopsis P450, cytochromes b5, NADPH-cytochrome P450 reductases, and family 1 glycosyltransferases (http://www. P450. kvl. dk). Phytochemistry 70: 1940-1947.
87. Paulick MG, Bertozzi CR (2008) The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 47: 6991-7000.
88. Pedrazzini E (2009) Tail-anchored proteins in plants. J Plant Biol 52: 1226-9239.
89. Qbadou S, Tien R, Soll J, Schleiff E (2003) Membrane insertion of the chloroplast outer envelope protein, Toc34: constrains for insertion and topology. J Cell Sci 116: 837-846.
90. Qbadou S, Becker T, Mirus O, Tews I, Soll J, Schleiff E (2006) The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO J 25: 1836-1847.
91. Rabu C, Wipf P, Brodsky JL, High S (2008) A precursor-specific role for Hsp40/Hsc70 during tail-anchored protein integration at the endoplasmic reticulum. J Biol Chem 283: 27504-27513.
92. Rabu C, Schmid V, Schwappach B, High S (2009) Biogenesis of tail-anchored proteins: the beginning for the end? J Cell Sci 122: 3605-3612.
93. Rosenblad MA, Larsen N, Samuelsson T, Zwieb C (2009) Kinship in the SRP RNA family. RNA Biol 6: 508-516.
94. Rudhe C, Chew O, Whelan J, Glaser E (2002) A novel in vitro system for simultaneous import of precursor proteins into mitochondria and chloroplasts. Plant J 30: 213-220.
95. Sanchez-Vallet A, Ramos B, Bednarek P, Lopez G, Pislewska-Bednarek M, Schulze-Lefert P, Molina A (2010) Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. Plant J 63: 115-127.
96. Schrader M, Yoon Y (2007) Mitochondria and peroxisomes: are the 'big brother' and the 'little sister' closer than assumed? Bioessays 29: 1105-1114.
97. Schuldiner M, Collins SR, Thompson NJ, Denic V, Bhamidipati A, Punna T, Ihmels J, Andrews B, Boone C, Greenblatt JF, Weissman JS, Krogan NJ (2005) Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123: 507-519.
98. Schuldiner M, Metz J, Schmid V, Denic V, Rakwalska M, Schmitt HD, Schwappach B, Weissman JS (2008) The GET complex mediates insertion of tail-anchored proteins into the ER membrane. Cell 134: 634-645.
99. Seedorf M, Waegemann K, Soll J (1995) A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J 7: 401-411.
100. Seo PJ, Kim SG, Park CM (2008) Membrane-bound transcription factors in plants. Trends Plant Sci 13: 550-556.
101. Setoguchi K, Otera H, Mihara K (2006) Cytosolic factor- and TOM-independent import of C-tail-anchored mitochondrial outer membrane proteins. EMBO J 25: 5635-5647.
102. Shen G, Kuppu S, Venkataramani S, Wang J, Yan J, Qiu X, Zhang H (2010) ANKYRIN REPEAT-CONTAINING PROTEIN 2A is an essential molecular chaperone for peroxisomal membrane-bound ASCORBATE PEROXIDASE3 in Arabidopsis. Plant Cell 22: 811-831.
103. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53: 1305-1319.
104. Stefanovic S, Hegde RS (2007) Identification of a targeting factor for posttranslational membrane protein insertion into the ER. Cell 128: 1147-1159.
105. Stojanovski D, Guiard B, Kozjak-Pavlovic V, Pfanner N, Meisinger C (2007) Alternative function for the mitochondrial SAM complex in biogenesis of alpha-helical TOM proteins. J Cell Biol 179: 881-893.
106. Tabak HF, van der Zand A, Braakman I (2008) Peroxisomes: minted by the ER. Curr Opin Cell Biol 20: 393-400.
107. Teixeira FK, Menezes-Benavente L, Galvao VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224: 300-314.
108. Titorenko VI, Rachubinski RA (2009) Spatiotemporal dynamics of the ER-derived peroxisomal endomembrane system. Int Rev Cell Mol Biol 272: 191-244.
109. Tsai LY, Tu SL, Li HM (1999) Insertion of atToc34 into the chloroplastic outer membrane is assisted by at least two proteinaceous components in the import system. J Biol Chem 274: 18735-18740.
110. van den Berg B, Clemons WM Jr, Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA (2004) X-ray structure of a protein-conducting channel. Nature 427: 36-44.
111. van der Zand A, Braakman I, Tabak HF (2010) Peroxisomal membrane proteins insert into the endoplasmic reticulum. Mol Biol Cell 21: 2057-2065.
112. 5, its functions, structure and membrane topology. Biochimie 77: 604-620.
113. Wattenberg B, Lithgow T (2001) Targeting of C-terminal (tail)-anchored proteins: understanding how cytoplasmic activities are anchored to intracellular membranes. Traffic 2: 66-71.
114. Werhahn W, Niemeyer A, Jansch L, Kruft V, Schmitz UK, Braun H (2001) Purification and characterization of the preprotein translocase of the outer mitochondrial membrane from Arabidopsis. Identification of multiple forms of TOM20. Plant Physiol 125: 943-954.
115. Xu XM, Meulia T, Meier I (2007) Anchorage of plant RanGAP to the nuclear envelope involves novel nuclear-pore-associated proteins. Curr Biol 17: 1157-1163.
116. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9: 47-59.
117. Zhao Q, Brkljacic J, Meier I (2008) Two distinct interacting classes of nuclear envelope-associated coiled-coil proteins are required for the tissue-specific nuclear envelope targeting of Arabidopsis RanGAP. Plant Cell 20: 1639-1651.