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Mechanisms of regulated unconventional protein secretion

Nature Reviews Molecular Cell Biology volume 10, pages 148–155 (2009)Cite this article

An Erratum to this article was published on 01 March 2009

Abstract

Most eukaryotic proteins are secreted through the conventional endoplasmic reticulum (ER)–Golgi secretory pathway. However, cytoplasmic, nuclear and signal-peptide-containing proteins have been shown to reach the cell surface by non-conventional transport pathways. The mechanisms and molecular components of unconventional protein secretion are beginning to emerge, including a role for caspase 1 and for the peripheral Golgi protein GRASP, which could function as a plasma membrane tether for membrane compartments during specific stages of development.

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Figure 1: Unconventional transport of signal-peptide-containing proteins.
Figure 2: Unconventional secretion of soluble cytoplasmic proteins.
Figure 3: Proposed roles for caspase 1 in the unconventional secretion of cytokines.
Figure 4: Proposed roles for GRASP in unconventional protein secretion.

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References

  1. Osborne, A. R., Rapoport, T. A. & van den Berg, B. Protein translocation by the Sec61/SecY channel. Annu. Rev. Cell Dev. Biol. 21, 529–550 (2005).

    Article  CAS  PubMed  Google Scholar 

  2. Lee, M. C., Miller, E. A., Goldberg, J., Orci, L. & Schekman, R. Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20, 87–123 (2004).

    Article  CAS  PubMed  Google Scholar 

  3. Trombetta, E. S. & Parodi, A. J. Quality control and protein folding in the secretory pathway. Annu. Rev. Cell Dev. Biol. 19, 649–676 (2003).

    Article  CAS  PubMed  Google Scholar 

  4. Nickel, W. & Seedorf, M. Unconventional mechanisms of protein transport to the cell surface of eukaryotic cells. Annu. Rev. Cell Dev. Biol. 24, 287–308 (1992).

    Article  CAS  Google Scholar 

  5. Fatal, N., Karhinen, L., Jokitalo, E. & Makarow, M. Active and specific recruitment of a soluble cargo protein for endoplasmic reticulum exit in the absence of functional COPII component Sec24p. J. Cell Sci. 117, 1665–1673 (2004).

    Article  CAS  PubMed  Google Scholar 

  6. Yoo, J. S. et al. Non-conventional trafficking of the cystic fibrosis transmembrane conductance regulator through the early secretory pathway. J. Biol. Chem. 277, 11401–11409 (2002).

    Article  CAS  PubMed  Google Scholar 

  7. Baldwin, T. A. & Ostergaard, H. L. The protein-tyrosine phosphatase CD45 reaches the cell surface via Golgi-dependent and -independent pathways. J. Biol. Chem. 277, 50333–50340 (2002).

    Article  CAS  PubMed  Google Scholar 

  8. Juschke, C., Wachter, A., Schwappach, B. & Seedorf, M. SEC18/NSF-independent, protein-sorting pathway from the yeast cortical ER to the plasma membrane. J. Cell Biol. 169, 613–622 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Schotman, H., Karhinen, L. & Rabouille, C. dGRASP-mediated noncanonical integrin secretion is required for Drosophila epithelial remodeling. Dev. Cell 14, 171–182 (2008).

    Article  CAS  PubMed  Google Scholar 

  10. Engling, A. et al. Biosynthetic FGF-2 is targeted to non-lipid raft microdomains following translocation to the extracellular surface of CHO cells. J. Cell Sci. 115, 3619–3631 (2002).

    Article  CAS  PubMed  Google Scholar 

  11. Florkiewicz, R. Z., Majack, R. A., Buechler, R. D. & Florkiewicz, E. Quantitative export of FGF-2 occurs through an alternative, energy-dependent, non-ER/Golgi pathway. J. Cell. Physiol. 162, 388–399 (1995).

    Article  CAS  PubMed  Google Scholar 

  12. Nickel, W. The mystery of nonclassical protein secretion. Eur. J. Biochem. 270, 2109–2119 (2003).

    Article  CAS  PubMed  Google Scholar 

  13. Trudel, C., Faure-Desire, V., Florkiewicz, R. Z. & Baird, A. Translocation of FGF2 to the cell surface without release into conditioned media. J. Cell. Physiol. 185, 260–268 (2000).

    Article  CAS  PubMed  Google Scholar 

  14. Cho, M. & Cummings, R. D. Galectin-1, a β-galactoside-binding lectin in Chinese hamster ovary cells. II. Localization and biosynthesis. J. Biol. Chem. 270, 5207–5212 (1995).

    Article  CAS  PubMed  Google Scholar 

  15. Hughes, R. C. Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim. Biophys. Acta 1473, 172–185 (1999).

    Article  CAS  PubMed  Google Scholar 

  16. Cooper, D. N. & Barondes, S. H. Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J. Cell Biol. 110, 1681–1691 (1990).

    Article  CAS  PubMed  Google Scholar 

  17. Seelenmeyer, C. et al. Cell surface counter receptors are essential components of the unconventional export machinery of galectin-1. J. Cell Biol. 171, 373–381 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Rubartelli, A., Cozzolino, F., Talio, M. & Sitia, R. A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J. 9, 1503–1510 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Nickel, W. Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6, 607–614 (2005).

    Article  CAS  PubMed  Google Scholar 

  20. Bonaldi, T. et al. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22, 5551–5560 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Gardella, S. et al. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep. 3, 995–1001 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Scaffidi, P., Misteli, T. & Bianchi, M. E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418, 191–195 (2002).

    Article  CAS  PubMed  Google Scholar 

  23. Dupont, E., Prochiantz, A. & Joliot, A. Identification of a signal peptide for unconventional secretion. J. Biol. Chem. 282, 8994–9000 (2007).

    Article  CAS  PubMed  Google Scholar 

  24. Joliot, A. et al. Identification of a signal sequence necessary for the unconventional secretion of Engrailed homeoprotein. Curr. Biol. 8, 856–863 (1998).

    Article  CAS  PubMed  Google Scholar 

  25. Maizel, A., Bensaude, O., Prochiantz, A. & Joliot, A. A short region of its homeodomain is necessary for engrailed nuclear export and secretion. Development 126, 3183–3190 (1999).

    Article  CAS  PubMed  Google Scholar 

  26. Maizel, A. et al. Engrailed homeoprotein secretion is a regulated process. Development 129, 3545–3553 (2002).

    Article  CAS  PubMed  Google Scholar 

  27. Kinseth, M. A. et al. The Golgi-associated protein GRASP is required for unconventional protein secretion during development. Cell 130, 524–534 (2007).

    Article  CAS  PubMed  Google Scholar 

  28. Barr, F. A., Puype, M., Vandekerckhove, J. & Warren, G. GRASP65, a protein involved in the stacking of Golgi cisternae. Cell 91, 253–262 (1997).

    Article  CAS  PubMed  Google Scholar 

  29. Shorter, J. et al. GRASP55, a second mammalian GRASP protein involved in the stacking of Golgi cisternae in a cell-free system. EMBO J. 18, 4949–4960 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Fatal, N., Suntio, T. & Makarow, M. Selective protein exit from yeast endoplasmic reticulum in absence of functional COPII coat component Sec13p. Mol. Biol. Cell 13, 4130–4140 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Karhinen, L., Bastos, R. N., Jokitalo, E. & Makarow, M. Endoplasmic reticulum exit of a secretory glycoprotein in the absence of sec24p family proteins in yeast. Traffic 6, 562–574 (2005).

    Article  CAS  PubMed  Google Scholar 

  32. Hasdemir, B., Fitzgerald, D. J., Prior, I. A., Tepikin, A. V. & Burgoyne, R. D. Traffic of Kv4 K+ channels mediated by KChIP1 is via a novel post-ER vesicular pathway. J. Cell Biol. 171, 459–469 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Ichimura, Y. et al. In vivo and in vitro reconstitution of Atg8 conjugation essential for autophagy. J. Biol. Chem. 279, 40584–40592 (2004).

    Article  CAS  PubMed  Google Scholar 

  34. Cali, T., Galli, C., Olivari, S. & Molinari, M. Segregation and rapid turnover of EDEM1 by an autophagy-like mechanism modulates standard ERAD and folding activities. Biochem. Biophys. Res. Commun. 371, 405–410 (2008).

    Article  CAS  PubMed  Google Scholar 

  35. Helms, J. B. & Rothman, J. E. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 360, 352–354 (1992).

    Article  CAS  PubMed  Google Scholar 

  36. Rabouille, C. & Klumperman, J. The maturing role of COPI vesicles in intra-Golgi transport. Nature Rev. Mol. Cell Biol. 6, 812–817 (2005).

    Article  CAS  Google Scholar 

  37. Pelham, H. R. & Rothman, J. E. The debate about transport in the Golgi—two sides of the same coin? Cell 102, 713–719 (2000).

    Article  CAS  PubMed  Google Scholar 

  38. Baldwin, T. A. & Ostergaard, H. L. Developmentally regulated changes in glucosidase II association with, and carbohydrate content of, the protein tyrosine phosphatase CD45. J. Immunol. 167, 3829–3835 (2001).

    Article  CAS  PubMed  Google Scholar 

  39. Jourdan, N. et al. Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J. Virol. 71, 8268–8278 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Toyokawa, K., Carling, S. J. & Ott, T. L. Cellular localization and function of the antiviral protein, ovine Mx1 (oMx1): I. Ovine Mx1 is secreted by endometrial epithelial cells via an 'unconventional' secretory pathway. Am. J. Reprod. Immunol. 57, 13–22 (2007).

    Article  CAS  PubMed  Google Scholar 

  41. Wang, X. et al. COPII-dependent export of cystic fibrosis transmembrane conductance regulator from the ER uses a di-acidic exit code. J. Cell Biol. 167, 65–74 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Pelham, H. R. SNAREs and the specificity of membrane fusion. Trends Cell Biol. 11, 99–101 (2001).

    Article  CAS  PubMed  Google Scholar 

  43. Jahn, R. & Scheller, R. H. SNAREs — engines for membrane fusion. Nature Rev. Mol. Cell Biol. 7, 631–643 (2006).

    Article  CAS  Google Scholar 

  44. Sollner, T. H. Intracellular and viral membrane fusion: a uniting mechanism. Curr. Opin. Cell Biol. 16, 429–435 (2004).

    Article  CAS  PubMed  Google Scholar 

  45. Becker, T., Volchuk, A. & Rothman, J. E. Differential use of endoplasmic reticulum membrane for phagocytosis in J774 macrophages. Proc. Natl Acad. Sci. USA 102, 4022–4026 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Desjardins, M. ER-mediated phagocytosis: a new membrane for new functions. Nature Rev. Immunol. 3, 280–291 (2003).

    Article  CAS  Google Scholar 

  47. Juschke, C., Ferring, D., Jansen, R. P. & Seedorf, M. A novel transport pathway for a yeast plasma membrane protein encoded by a localized mRNA. Curr. Biol. 14, 406–411 (2004).

    Article  CAS  PubMed  Google Scholar 

  48. Prudovsky, I. et al. Secretion without Golgi. J. Cell. Biochem. 103, 1327–1343 (2007).

    Article  CAS  Google Scholar 

  49. Temmerman, K. et al. A direct role for phosphatidylinositol-4,5-bisphosphate in unconventional secretion of fibroblast growth factor 2. Traffic 9, 1204–1217 (2008).

    Article  CAS  PubMed  Google Scholar 

  50. Zehe, C., Engling, A., Wegehingel, S., Schäfer, T. & Nickel, W. Cell-surface heparan sulfate proteoglycans are essential components of the unconventional export machinery of FGF-2. Proc. Natl Acad. Sci. USA 103, 15479–15484 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Pellegrini, L. Role of heparan sulfate in fibroblast growth factor signalling: a structural view. Curr. Opin. Struct. Biol. 11, 629–634 (2001).

    Article  CAS  PubMed  Google Scholar 

  52. Nickel, W. Unconventional secretion: an extracellular trap for export of fibroblast growth factor 2. J. Cell Sci. 120, 2295–2299 (2007).

    Article  CAS  PubMed  Google Scholar 

  53. Schäfer, T. et al. Unconventional secretion of fibroblast growth factor 2 is mediated by direct translocation across the plasma membrane of mammalian cells. J. Biol. Chem. 279, 6244–6251 (2004).

    Article  PubMed  CAS  Google Scholar 

  54. Andrei, C. et al. The secretory route of the leaderless protein interleukin 1β involves exocytosis of endolysosome-related vesicles. Mol. Biol. Cell 10, 1463–1475 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Andrei, C. et al. Phospholipases C and A2 control lysosome-mediated IL-1β secretion: implications for inflammatory processes. Proc. Natl Acad. Sci. USA 101, 9745–9750 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. MacKenzie, A. et al. Rapid secretion of interleukin-1β by microvesicle shedding. Immunity 15, 825–835 (2001).

    Article  CAS  PubMed  Google Scholar 

  57. Pelegrin, P., Barroso-Gutierrez, C. & Surprenant, A. P2X7 receptor differentially couples to distinct release pathways for IL-1β in mouse macrophage. J. Immunol. 180, 7147–7157 (2008).

    Article  CAS  PubMed  Google Scholar 

  58. Gruenberg, J. & Stenmark, H. The biogenesis of multivesicular endosomes. Nature Rev. Mol. Cell Biol. 5, 317–323 (2004).

    Article  CAS  Google Scholar 

  59. Piper, R. C. & Katzmann, D. J. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23, 519–547 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wegehingel, S., Zehe, C. & Nickel, W. Rerouting of fibroblast growth factor 2 to the classical secretory pathway results in post-translational modifications that block binding to heparan sulfate proteoglycans. FEBS Lett. 582, 2387–2392 (2008).

    Article  CAS  PubMed  Google Scholar 

  61. Thornberry, N. A. et al. A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature 356, 768–774 (1992).

    Article  CAS  PubMed  Google Scholar 

  62. Burns, K., Martinon, F. & Tschopp, J. New insights into the mechanism of IL-1β maturation. Curr. Opin. Immunol. 15, 26–30 (2003).

    Article  CAS  PubMed  Google Scholar 

  63. Ogura, Y., Sutterwala, F. S. & Flavell, R. A. The inflammasome: first line of the immune response to cell stress. Cell 126, 659–662 (2006).

    Article  CAS  PubMed  Google Scholar 

  64. Petrilli, V., Dostert, C., Muruve, D. A. & Tschopp, J. The inflammasome: a danger sensing complex triggering innate immunity. Curr. Opin. Immunol. 19, 615–622 (2007).

    Article  CAS  PubMed  Google Scholar 

  65. Dostert, C. et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320, 674–677 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Eisenbarth, S. C., Colegio, O. R., O'Connor, W., Sutterwala, F. S. & Flavell, R. A. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453, 1122–1126 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Halle, A. et al. The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nature Immunol. 9, 857–865 (2008).

    Article  CAS  Google Scholar 

  68. Hornung, V. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nature Immunol. 9, 847–856 (2008).

    Article  CAS  Google Scholar 

  69. Muruve, D. A. et al. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 452, 103–107 (2008).

    Article  CAS  PubMed  Google Scholar 

  70. Feldmeyer, L. et al. The inflammasome mediates UVB-induced activation and secretion of interleukin-1β by keratinocytes. Curr. Biol. 17, 1140–1145 (2007).

    Article  CAS  PubMed  Google Scholar 

  71. Keller, M., Ruegg, A., Werner, S. & Beer, H. D. Active caspase-1 is a regulator of unconventional protein secretion. Cell 132, 818–831 (2008).

    Article  CAS  PubMed  Google Scholar 

  72. Wang, Y., Satoh, A. & Warren, G. Mapping the functional domains of the Golgi stacking factor GRASP65. J. Biol. Chem. 280, 4921–4928 (2005).

    Article  CAS  PubMed  Google Scholar 

  73. Duran, J. M. et al. The role of GRASP55 in Golgi fragmentation and entry of cells into mitosis. Mol. Biol. Cell 19, 2579–2587 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Feinstein, T. N. & Linstedt, A. D. GRASP55 regulates Golgi ribbon formation. Mol. Biol. Cell 19, 2696–2707 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Puthenveedu, M. A., Bachert, C., Puri, S., Lanni, F. & Linstedt, A. D. GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi-enzyme distribution. Nature Cell Biol. 8, 238–248 (2006).

    Article  CAS  PubMed  Google Scholar 

  76. Sutterlin, C., Hsu, P., Mallabiabarrena, A. & Malhotra, V. Fragmentation and dispersal of the pericentriolar Golgi complex is required for entry into mitosis in mammalian cells. Cell 109, 359–369 (2002).

    Article  CAS  PubMed  Google Scholar 

  77. Rabouille, C. & Kondylis, V. Golgi ribbon unlinking: an organelle-based G2/M checkpoint. Cell Cycle 6, 2723–2729 (2007).

    Article  CAS  PubMed  Google Scholar 

  78. Behnia, R., Barr, F. A., Flanagan, J. J., Barlowe, C. & Munro, S. The yeast orthologue of GRASP65 forms a complex with a coiled-coil protein that contributes to ER to Golgi traffic. J. Cell Biol. 176, 255–261 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Kondylis, V., Spoorendonk, K. M. & Rabouille, C. dGRASP localization and function in the early exocytic pathway in Drosophila S2 cells. Mol. Biol. Cell 16, 4061–4072 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kuo, A., Zhong, C., Lane, W. S. & Derynck, R. Transmembrane transforming growth factor-α tethers to the PDZ domain-containing, Golgi membrane-associated protein p59/GRASP55. EMBO J. 19, 6427–6439 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Anjard, C. & Loomis, W. F. Peptide signaling during terminal differentiation of Dictyostelium. Proc. Natl Acad. Sci. USA 102, 7607–7611 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Filimonenko, M. et al. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J. Cell Biol. 179, 485–500 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Miller, E. A. et al. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114, 497–509 (2003).

    Article  CAS  PubMed  Google Scholar 

  84. Barlowe, C. Molecular recognition of cargo by the COPII complex: a most accommodating coat. Cell 114, 395–397 (2003).

    Article  CAS  PubMed  Google Scholar 

  85. Otte, S. & Barlowe, C. Sorting signals can direct receptor-mediated export of soluble proteins into COPII vesicles. Nature Cell Biol. 6, 1189–1194 (2004).

    Article  CAS  PubMed  Google Scholar 

  86. Mellman, I. & Warren, G. The road taken: past and future foundations of membrane traffic. Cell 100, 99–112 (2000).

    Article  CAS  PubMed  Google Scholar 

  87. McGrath, J. P. & Varshavsky, A. The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein. Nature 340, 400–404 (1989).

    Article  CAS  PubMed  Google Scholar 

  88. Pamer, E. & Cresswell, P. Mechanisms of MHC class I—restricted antigen processing. Annu. Rev. Immunol. 16, 323–358 (1998).

    Article  CAS  PubMed  Google Scholar 

  89. Borst, P., Zelcer, N. & van Helvoort, A. ABC transporters in lipid transport. Biochim. Biophys. Acta 1486, 128–144 (2000).

    Article  CAS  PubMed  Google Scholar 

  90. Flieger, O. et al. Regulated secretion of macrophage migration inhibitory factor is mediated by a non-classical pathway involving an ABC transporter. FEBS Lett. 551, 78–86 (2003).

    Article  CAS  PubMed  Google Scholar 

  91. Qu, Y., Franchi, L., Nunez, G. & Dubyak, G. R. Nonclassical IL-1β secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 179, 1913–1925 (2007).

    Article  CAS  PubMed  Google Scholar 

  92. Anjard, C. & Loomis, W. F. GABA induces terminal differentiation of Dictyostelium through a GABAB receptor. Development 133, 2253–2261 (2006).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to F. Reggiori, J. Klumperman and V. Malhotra for critically reading the manuscript.

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  1. Walter Nickel is at the Heidelberg University Biochemistry Center, Im Neuenheimer Feld 328, 69120 Heidelberg, Germany.,

    Walter Nickel

  2. Department of Cell Biology, Catherine Rabouille is at the Cell Microscopy Center, UMC Utrecht, Heidelberglaan 100, 3584 CX Utrecht, The Netherlands. walter.nickel@bzh.uni-heidelberg.de; C.rabouille@umcutrecht.nl,

    Catherine Rabouille

  3. C.rabouille@umcutrecht.nl,

    Catherine Rabouille

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Nickel, W., Rabouille, C. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol 10, 148–155 (2009). https://doi.org/10.1038/nrm2617

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