Diverse roles for the p24 family of proteins in eukaryotic cells

Biomolecular Concepts

Volumn 3, Issue 6, 2012, Pages 561-570

  Schuiki, Irmgard ^a   Volchuk, Allen ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Endoplasmic reticulum; Golgi; p24 proteins; Protein transport; Secretory pathway

Indexed keywords

EID: 84954307884     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/bmc-2012-0028     Document Type: Review

References (96)

1. Nickel W, Rabouille C. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 2009; 10: 148-55.
2. Pfeffer SR. Unsolved mysteries in membrane traffic. Annu Rev Biochem 2007; 76: 629-45.
3. Spang A. On vesicle formation and tethering in the ER-Golgi shuttle. Curr Opin Cell Biol 2009; 21: 531-6.
4. Szul T, Sztul E. COPII and COPI traffic at the ER-Golgi interface. Physiology (Bethesda) 2011; 26: 348-64.
5. Jensen D, Schekman R. COPII-mediated vesicle formation at a glance. J Cell Sci 2011; 124: 1-4.
6. Dancourt J, Barlowe C. Protein sorting receptors in the early secretory pathway. Annu Rev Biochem 2010; 79: 777-802.
7. Strating JR, Hafmans TG, Martens GJ. Functional diversity among p24 subfamily members. Biol Cell 2009; 101: 207-19.
8. Strating JR, Martens GJ. The p24 family and selective transport processes at the ER-Golgi interface. Biol Cell 2009; 101: 495-509.
9. Carney GE, Bowen NJ. p24 proteins, intracellular trafficking, and behavior: Drosophila melanogaster provides insights and opportunities. Biol Cell 2004; 96: 271-8.
10. Springer S, Chen E, Duden R, Marzioch M, Rowley A, Hamamoto S, Merchant S, Schekman R. The p24 proteins are not essential for vesicular transport in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2000; 97: 4034-9.
11. Strating JRPM, van Bakel NHM, Leunissen JAM, Martens GJM. A comprehensive overview of the vertebrate p24 family: identification of a novel tissue-specifically expressed member. Mol Biol Evol 2009; 26: 1707-14.
12. Belden WJ, Barlowe C. Erv25p, a component of COPII-coated vesicles, forms a complex with Emp24p that is required for efficient endoplasmic reticulum to Golgi transport. J Biol Chem 1996; 271: 26939-46.
13. Marzioch M, Henthorn DC, Herrmann JM, Wilson R, Thomas DY, Bergeron JJM, Solari RCE, Rowley A. Erp1p and Erp2p, partners for Emp24p and Erv25p in a yeast p24 complex. Mol Biol Cell 1999; 10: 1923-38.
14. Schimmoller F, Singer-Kruger B, Schroder S, Kruger U, Barlowe C, Riezman H. The absence of Emp24p, a component of ER-derived COPII-coated vesicles, causes a defect in transport of selected proteins to the Golgi. EMBO J 1995; 14: 1329-39.
15. Dominguez M, Dejgaard K, Fullekrug J, Dahan S, Fazel A, Paccaud J-P, Thomas DY, Bergeron JJM, Nilsson T. gp25L/emp24/p24 protein family members of the cis-Golgi network bind both COPI and II coatomer. J Cell Biol 1998; 140: 751-65.
16. Gayle MA, Slack JL, Bonnert TP, Renshaw BR, Sonoda G, Taguchi T, Testa JR, Dower SK, Sims JE. Cloning of a putative ligand for the T1/ST2 receptor. J Biol Chem 1996; 271: 5784-9.
17. Sohn K, Orci L, Ravazzola M, Amherdt M, Bremser M, Lottspeich F, Fiedler K, Helms JB, Wieland FT. A major transmembrane protein of Golgi-derived COPI-coated vesicles involved in coatomer binding. J Cell Biol 1996; 135: 1239-48.
18. Stamnes MA, Craighead MW, Hoe MH, Lampen N, Geromanos S, Tempst P, Rothman JE. An integral membrane component of coatomer-coated transport vesicles defines a family of proteins involved in budding. Proc Natl Acad Sci USA 1995; 92: 8011-5.
19. Wada I, Rindress D, Cameron PH, Ou WJ, Doherty JJ II, Louvard D, Bell AW, Dignard D, Thomas DY, Bergeron JJ. SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem 1991; 266: 19599-610.
20. Strating JR, Bouw G, Hafmans TG, Martens GJ. p24 Proteins from the same subfamily are functionally nonredundant. Biochimie 2011; 93: 528-32.
21. Chen J, Qi X, Zheng H. Subclass-specific localization and trafficking of Arabidopsis p24 proteins in the ER-Golgi interface. Traffic 2012; 13: 400-15.
22. Montesinos JC, Sturm S, Langhans M, Hillmer S, Marcote MJ, Robinson DG, Aniento F. Coupled transport of Arabidopsis p24 proteins at the ER-Golgi interface. J Expt Bot 2012; 63: 4343-61.
23. Anantharaman V, Aravind L. The GOLD domain, a novel protein module involved in Golgi function and secretion. Genome Biol 2002; 3: research0023.
24. Ciufo LF, Boyd A. Identification of a lumenal sequence specifying the assembly of Emp24p into p24 complexes in the yeast secretory pathway. J Biol Chem 2000; 275: 8382-8.
25. Jenne N, Frey K, Brugger B, Wieland FT. Oligomeric state and stoichiometry of p24 proteins in the early secretory pathway. J Biol Chem 2002; 277: 46504-11.
26. Bethune J, Kol M, Hoffmann J, Reckmann I, Brugger B, Wieland F. Coatomer, the coat protein of COPI transport vesicles, discriminates endoplasmic reticulum residents from p24 proteins. Mol Cell Biol 2006; 26: 8011-21.
27. Contreras I, Yang Y, Robinson DG, Aniento F. Sorting signals in the cytosolic tail of plant p24 proteins involved in the interaction with the COPII coat. Plant Cell Physiol 2004; 45: 1779-86.
28. Zhao L, Helms JB, Brunner J, Wieland FT. GTP-dependent binding of ARF to coatomer in close proximity to the binding site for dilysine retrieval motifs and p23. J Biol Chem 1999; 274: 14198-203.
29. Gommel D, Orci L, Emig EM, Hannah MJ, Ravazzola M, Nickel W, Helms JB, Wieland FT, Sohn K. p24 and p23, the major transmembrane proteins of COPI-coated transport vesicles, form hetero-oligomeric complexes and cycle between the organelles of the early secretory pathway. FEBS Lett 1999; 447: 179-85.
30. Emery G, Rojo M, Gruenberg J. Coupled transport of p24 family members. J Cell Sci 2000; 113: 2507-16.
31. Denzel A, Otto F, Girod A, Pepperkok R, Watson R, Rosewell I, Bergeron JJM, Solari RCE, Owen MJ. The p24 family member p23 is required for early embryonic development. Curr Biol 2000; 10: 55-8.
32. Jerome-Majewska LA, Achkar T, Luo L, Lupu F, Lacy E. The trafficking protein Tmed2/p24beta(1) is required for morphogenesis of the mouse embryo and placenta. Dev Biol 2010; 341: 154-66.
33. Takida S, Maeda Y, Kinoshita T. Mammalian GPI-anchored proteins require p24 proteins for their efficient transport from the ER to the plasma membrane. Biochem J 2008; 409: 555-62.
34. Vetrivel KS, Gong P, Bowen JW, Cheng H, Chen Y, Carter M, Nguyen PD, Placanica L, Wieland FT, Li Y-M, Kounnas MZ, Thinakaran G. Dual roles of the transmembrane protein p23/TMP21 in the modulation of amyloid precursor protein metabolism. Mol Neurodegen 2007; 2: 1-12.
35. Zhang L, Volchuk A. p24 family type 1 transmembrane proteins are required for insulin biosynthesis and secretion in pancreatic beta-cells. FEBS Lett 2010; 584: 2298-304.
36. Bouw G, Van Huizen R, Jansen EJ, Martens GJ. A cell-specific transgenic approach in Xenopus reveals the importance of a functional p24 system for a secretory cell. Mol Biol Cell 2004; 15: 1244-53.
37. Strating JR, Bouw G, Hafmans TG, Martens GJ. Disparate effects of p24alpha and p24delta on secretory protein transport and processing. PLoS One 2007; 2: e704.
38. Contreras F-X, Ernst AM, Haberkant P, Bjorkholm P, Lindahl E, Gonen B, Tischer C, Elofsson A, von Heijne G, Thiele C, Pepperkok R, Wieland F, Brugger B. Molecular recognition of a single sphingolipid species by a protein's transmembrane domain. Nature 2012; 481: 525-9.
39. Blum R, Lepier A. The luminal domain of p23 (Tmp21) plays a critical role in p23 cell surface trafficking. Traffic 2008; 9: 1530-50.
40. Hosaka M, Watanabe T, Yamauchi Y, Sakai Y, Suda M, Mizutani S, Takeuchi T, Isobe T, Izumi T. A subset of p23 localized on secretory granules in pancreatic beta-cells. J Histochem Cytochem 2007; 55: 235-45.
41. Kaiser C. Thinking about p24 proteins and how transport vesicles select their cargo. Proc Natl Acad Sci USA 2000; 97: 3783-5.
42. Zakariyah A, Hou W, Slim R, Jerome-Majewska L. TMED2/p24beta1 is expressed in all gestational stages of human placentas and in choriocarcinoma cell lines. Placenta 2012; 33: 214-9.
43. Langhans M, Marcote MJ, Pimpl P, Virgili-Lopez G, Robinson DG, Aniento F. In vivo trafficking and localization of p24 proteins in plant cells. Traffic 2008; 9: 770-85.
44. Kurbatova E, Otzen M, van der Klei IJ. p24 proteins play a role in peroxisome proliferation in yeast. FEBS Lett 2009; 583: 3175-80.
45. Barr FA, Preisinger C, Kopajtich R, Korner R. Golgi matrix proteins interact with p24 cargo receptors and aid their efficient retention in the Golgi apparatus. J Cell Biol 2001; 155: 885-91.
46. Blum R, Feick P, Puype M, Vandekerckhove J, Klengel R, Nastainczyk W, Schulz I. Tmp21 and p24A, two type 1 proteins enriched in pancreatic microsomal membranes, are members of a protein family involved in vesicular trafficking. J Biol Chem 1996; 271: 17183-9.
47. Kuiper RP, Waterham HR, Rotter J, Bouw G, Martens GJ. Differential induction of two p24delta putative cargo receptors upon activation of a prohormone-producing cell. Mol Biol Cell 2000; 11: 131-40.
48. Rotter J, Kuiper RP, Bouw G, Martens GJ. Cell-type-specific and selectively induced expression of members of the p24 family of putative cargo receptors. J Cell Sci 2002; 115: 1049-58.
49. Bartoszewski S, Luschnig S, Desjeux I, Grosshans J, Nusslein-Volhard C. Drosophila p24 homologues eclair and baiser are necessary for the activity of the maternally expressed Tkv receptor during early embryogenesis. Mech Dev 2004; 121: 1259-73.
50. Boltz KA, Ellis LL, Carney GE. Drosophila melanogaster p24 genes have developmental, tissue-specific, and sex-specific expression patterns and functions. Dev Dyn 2007; 236: 544-55.
51. Carney GE, Taylor BJ. Logjam encodes a predicted EMP24/GP25 protein that is required for Drosophila oviposition behavior. Genetics 2003; 164: 173-86.
52. Hetz C, Martinon F, Rodriguez D, Glimcher LH. The unfolded protein response: integrating stress signals through the stress sensor IRE1a. Physiol Rev 2011; 91: 1219-43.
53. Hartley T, Siva M, Lai E, Teodoro T, Zhang L, Volchuk A. Endoplasmic reticulum stress response in an INS-1 pancreatic beta-cell with inducible expression of a folding-deficient proinsulin. BMC Cell Biol 2010; 11: 59.
54. Fox RM, Hanlon CD, Andrew DJ. The CrebA/Creb3-like transcription factors are major and direct regulators of secretory capacity. J Cell Biol 2010; 191: 479-92.
55. Asada R, Kanemoto S, Kondo S, Saito A, Imaizumi K. The signalling from the endoplasmic reticulum-resident bZIP transcription factors involved in diverse cellular physiology. J Biochem 2011; 149: 507-18.
56. Bailey D, O'Hare P. Transmembrane bZIP transcription factors in ER stress signaling and the unfolded protein response. Antioxid Redox Signal 2007; 9: 2305-21.
57. Kondo S, Saito A, Asada R, Kanemoto S, Imaizumi K. Physiological unfolded protein response regulated by OASIS family members, transmembrane bZIP transcription factors. IUBMB Life 2011; 63: 233-9.
58. Murakami T, Saito A, Hino S, Kondo S, Kanemoto S, Chihara K, Sekiya H, Tsumagari K, Ochiai K, Yoshinaga K, Saitoh M, Nishimura R, Yoneda T, Kou I, Furuichi T, Ikegawa S, Ikawa M, Okabe M, Wanaka A, Imaizumi K. Signalling mediated by the endoplasmic reticulum stress transducer OASIS is involved in bone formation. Nat Cell Biol 2009; 11: 1205-11.
59. Vellanki RN, Zhang L, Guney MA, Rocheleau JV, Gannon M, Volchuk A. OASIS/CREB3L1 induces expression of genes involved in extracellular matrix production but not classical endoplasmic reticulum response genes in pancreatic beta-cells. Endocrinology 2010; 151: 4146-57.
60. Aguilera-Romero A, Kaminska J, Spang A, Riezman H, Muniz M. The yeast p24 complex is required for the formation of COPI retrograde transport vesicles from the Golgi apparatus. J Cell Biol 2008; 180: 713-20.
61. Saleem S, Schwedes CC, Ellis LL, Grady ST, Adams RL, Johnson N, Whittington JR, Carney GE. Drosophila melanogaster p24 trafficking proteins have vital roles in development and reproduction. Mech Dev 2012; 129: 177-91.
62. Fiedler K, Veit M, Stamnes MA, Rothman JE. Bimodal interaction of coatomer with the p24 family of putative cargo receptors. Science 1996; 273: 1396-9.
63. Gommel DU, Memon AR, Heiss A, Lottspeich F, Pfannstiel J, Lechner J, Reinhard C, Helms JB, Nickel W, Wieland FT. Recruitment to Golgi membranes of ADP-ribosylation factor 1 is mediated by the cytoplasmic domain of p23. EMBO J 2001; 20: 6751-60.
64. Kuehn MJ, Herrmann JM, Schekman R. COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 1998; 391: 187-90.
65. Muniz M, Nuoffer C, Hauri HP, Riezman H. The Emp24 complex recruits a specific cargo molecule into endoplasmic reticulum-derived vesicles. J Cell Biol 2000; 148: 925-30.
66. Namekawa M, Muriel MP, Janer A, Latouche M, Dauphin A, Debeir T, Martin E, Duyckaerts C, Prigent A, Depienne C, Sittler A, Brice A, Ruberg M. Mutations in the SPG3A gene encoding the GTPase atlastin interfere with vesicle trafficking in the ER/Golgi interface and Golgi morphogenesis. Mol Cell Neurosci 2007; 35: 1-13.
67. Wen C, Greenwald I. p24 proteins and quality control of LIN-12 and GLP-1 trafficking in Caenorhabditis elegans. J Cell Biol 1999; 145: 1165-75.
68. Beck R, Rawet M, Wieland F, Cassel D. The COPI system: molecular mechanisms and function. FEBS Lett 2009; 583: 2701-9.
69. Bremser M, Nickel W, Schweikert M, Ravazzola M, Amherdt M, Hughes CA, Sollner TH, Rothman JE, Wieland FT. Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors. Cell 1999; 96: 495-506.
70. Majoul I, Straub M, Hell SW, Duden R, Soling HD. KDEL-cargo regulates interactions between proteins involved in COPI vesicle traffic: measurements in living cells using FRET. Dev Cell 2001; 1: 139-53.
71. Harter C, Wieland FT. A single binding site for dilysine retrieval motifs and p23 within the gamma subunit of coatomer. Proc Natl Acad Sci USA 1998; 95: 11649-54.
72. Langer JD, Roth CM, Bethune J, Stoops EH, Brugger B, Herten DP, Wieland FT. A conformational change in the alpha-subunit of coatomer induced by ligand binding to gamma-COP revealed by single-pair FRET. Traffic 2008; 9: 597-607.
73. Reinhard C, Harter C, Bremser M, Brugger B, Sohn K, Helms JB, Wieland F. Receptor-induced polymerization of coatomer. Proc Natl Acad Sci USA 1999; 96: 1224-8.
74. Goldberg J. Decoding of sorting signals by coatomer through a GTPase switch in the COPI coat complex. Cell 2000; 100: 671-9.
75. Lanoix J, Ouwendijk J, Stark A, Szafer E, Cassel D, Dejgaard K, Weiss M, Nilsson T. Sorting of Golgi resident proteins into different subpopulations of COPI vesicles: a role for ArfGAP1. J Cell Biol 2001; 155: 1199-212.
76. Miller EA, Beilharz TH, Malkus PN, Lee MC, Hamamoto S, Orci L, Schekman R. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 2003; 114: 497-509.
77. Matsuoka K, Orci L, Amherdt M, Bednarek SY, Hamamoto S, Schekman R, Yeung T. COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 1998; 93: 263-75.
78. Copic A, Latham CF, Horlbeck MA, D' Arcangelo JG, Miller EA. ER cargo properties specify a requirement for COPII coat rigidity mediated by Sec13p. Science 2012; 335: 1359-62.
79. Castillon GA, Aguilera-Romero A, Manzano-Lopez J, Epstein S, Kajiwara K, Funato K, Watanabe R, Riezman H, Muniz M. The yeast p24 complex regulates GPI-anchored protein transport and quality control by monitoring anchor remodeling. Mol Biol Cell 2011; 22: 2924-36.
80. Castillon GA, Watanabe R, Taylor M, Schwabe TM, Riezman H. Concentration of GPI-anchored proteins upon ER exit in yeast. Traffic 2009; 10: 186-200.
81. Bonnon C, Wendeler MW, Paccaud JP, Hauri HP. Selective export of human GPI-anchored proteins from the endoplasmic reticulum. J Cell Sci 2010; 123: 1705-15.
82. Maeda Y, Kinoshita T. Structural remodeling, trafficking and functions of glycosylphosphatidylinositol-anchored proteins. Prog Lipid Res 2011; 50: 411-24.
83. Fujita M, Watanabe R, Jaensch N, Romanova-Michaelides M, Satoh T, Kato M, Riezman H, Yamaguchi Y, Maeda Y, Kinoshita T. Sorting of GPI-anchored proteins into ER exit sites by p24 proteins is dependent on remodeled GPI. J Cell Biol 2011; 194: 61-75.
84. Buechling T, Chaudhary V, Spirohn K, Weiss M, Boutros M. p24 proteins are required for secretion of Wnt ligands. EMBO Rep 2011; 12: 1265-72.
85. Port F, Hausmann G, Basler K. A genome-wide RNA interference screen uncovers two p24 proteins as regulators of Wingless secretion. EMBO Rep 2011; 12: 1144-52.
86. Luo W, Wang Y, Reiser G. p24A, a type I transmembrane protein, controls ARF1-dependent resensitization of protease-activated receptor-2 by influence on receptor trafficking. J Biol Chem 2007; 282: 30246-55.
87. Luo W, Wang Y, Reiser G. Proteinase-activated receptors, nucleotide P2Y receptors, and mu-opioid receptor-1B are under the control of the type I transmembrane proteins p23 and p24A in post-Golgi trafficking. J Neurochem 2011; 117: 71-81.
88. Wang H, Kazanietz MG. Chimaerins, novel non-protein kinase C phorbol ester receptors, associate with Tmp21-I (p23): evidence for a novel anchoring mechanism involving the chimaerin C1 domain. J Biol Chem 2002; 277: 4541-50.
89. Hasegawa H, Liu L, Nishimura M. Dilysine retrieval signalcontaining p24 proteins collaborate in inhibiting gamma-cleavage of amyloid precursor protein. J Neurochem 2010; 115: 771-81.
90. Blum R, Pfeiffer F, Feick P, Nastainczyk W, Kohler B, Schafer KH, Schulz I. Intracellular localization and in vivo trafficking of p24A and p23. J Cell Sci 1999; 112: 537-48.
91. Rojo M, Emery G, Marjomaki V, McDowall AW, Parton RG, Gruenberg J. The transmembrane protein p23 contributes to the organization of the Golgi apparatus. J Cell Sci 2000; 113: 1043-57.
92. Gong P, Roseman J, Fernandez CG, Vetrivel KS, Bindokas VP, Zitzow LA, Kar S, Parent AT, Thinakaran G. Transgenic neuronal overexpression reveals that stringently regulated p23 expression is critical for coordinated movement in mice. Mol Neurodegener 2011; 6: 87.
93. Mitrovic S, Ben-Tekaya H, Koegler E, Gruenberg J, Hauri HP. The cargo receptors Surf4, endoplasmic reticulum-Golgi intermediate compartment (ERGIC)-53, and p25 are required to maintain the architecture of ERGIC and Golgi. Mol Biol Cell 2008; 19: 1976-90.
94. Belden WJ, Barlowe C. Deletion of yeast p24 genes activates the unfolded protein response. Mol Biol Cell 2001; 12: 957-69.
95. Shevchenko A, Keller P, Scheiffele P, Mann M, Simons K. Identification of components of trans-Golgi network-derived transport vesicles and detergent-insoluble complexes by nanoelectrospray tandem mass spectrometry. Electrophoresis 1997; 18: 2591-600.
96. Chen F, Hasegawa H, Schmitt-Ulms G, Kawarai T, Bohm C, Katayama T, Gu Y, Sanjo N, Glista M, Rogaeva E, Wakutani Y, Pardossi-Piquard R, Ruan X, Tandon A, Checler F, Marambaud P, Hansen K, Westaway D, St George-Hyslop P, Fraser P. TMP21 is a presenilin complex component that modulates gamma-secretase but not epsolon-secretase activity. Nature 2006; 440: 1208-12.