Marshall, Richard S., Jolliffe, Nicholas A., Ceriotti, Aldo, Snowden, Christopher J., Lord, Mike (J. Mike), Frigerio, Lorenzo and Roberts, Lynne M. . (2009) The role of CDC48 in the retro-translocation of non-ubiquitinated toxin substrates in plant cells. Journal of Biological Chemistry, Vol.283 . pp. 15869-15877. ISSN 0021-9258

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Abstract

When the catalytic A subunits of the castor bean toxins ricin and Ricinus communis agglutinin (denoted as RTA and RCA A, respectively) are delivered into the endoplasmic reticulum (ER) of tobacco protoplasts, they become substrates for ER-associated protein degradation (ERAD). As such, these orphan polypeptides are retro-translocated to the cytosol, where a significant proportion of each protein is degraded by proteasomes. Here we begin to characterise the ERAD pathway in plant cells, showing that retro-translocation of these lysine-deficient glycoproteins requires the ATPase activity of cytosolic CDC48. Lysine polyubiquitination is not obligatory for this step. We also show that while RCA A is found in a mannose-untrimmed form prior to its retro-translocation, a significant proportion of newly synthesised RTA cycles via the Golgi and becomes modified by downstream glycosylation enzymes. Despite these differences, both proteins are similarly retro-translocated.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany
Divisions:	Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH):	Castor beans, Ricin, Endoplasmic reticulum, Tobacco, Plant protoplasts, Plant translocation, Glycoproteins
Journal or Publication Title:	Journal of Biological Chemistry
Publisher:	American Society for Biochemistry and Molecular Biology, Inc.
ISSN:	0021-9258
Date:	6 June 2009
Volume:	Vol.283
Page Range:	pp. 15869-15877
Identification Number:	10.1074/jbc.M709316200
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Leverhulme Trust (LT)
References:	1. Vitale, A. (2001) Plant Cell 13(6), 1260-1262 2. Romisch, K. (2005) Annu Rev Cell Dev Biol 21, 435-456 3. Meusser, B., Hirsch, C., Jarosch, E., and Sommer, T. (2005) Nat Cell Biol 7(8), 766-772 4. Braun, S., Matuschewski, K., Rape, M., Thoms, S., and Jentsch, S. (2002) EMBO J. 21, 615-621. 5. Ye, Y., Meyer, H. H., and Rapoport, T. A. (2001) Nature 414(6864), 652-656 6. Rabinovich, E., Kerem, A., Frohlich, K.-U., Diamant, N., and Bar-Nun, S. (2002) Mol. Cell. Biol. 22, 626-634. 7. Jarosch, E., Taxis, C., Volkwein, C., Bordallo, J., Finley, D., Wolf, D. H., and Sommer, T. (2002) Nat Cell Biol 4(2), 134-139 8. Ye, Y., Meyer, H. H., and Rapoport, T. A. (2003) J Cell Biol 162(1), 71-84 9. Rape, M., Hoppe, T., Gorr, I., Kalocay, M., Richly, H., and Jentsch, S. (2001) Cell 107(5), 667-677 10. Lee, R. J., Liu, C. W., Harty, C., McCracken, A. A., Latterich, M., Romisch, K., DeMartino, G. N., Thomas, P. J., and Brodsky, J. L. (2004) Embo J 23(11), 2206-2215 11. Worthington, Z. E., and Carbonetti, N. H. (2007) Infect Immun 75(6), 2946- 2953 12. Kothe, M., Ye, Y., Wagner, J. S., De Luca, H. E., Kern, E., Rapoport, T. A., and Lencer, W. I. (2005) J Biol Chem 280(30), 28127-28132 13. Ceriotti, A., and Roberts, L. M. (2006) Endoplasmic reticulum-associated protein degradation in plant cells. In: Robinson, D. G. (ed). Plant Cell Mongr (4), Springer Verlag 14. Feiler, H. S., Desprez, T., Santoni, V., Kronenberger, J., Caboche, M., and Traas, J. (1995) Embo J 14(22), 5626-5637 15. Rancour, D. M., Dickey, C. E., Park, S., and Bednarek, S. Y. (2002) Plant Physiol 130(3), 1241-1253 16. Muller, J., Piffanelli, P., Devoto, A., Miklis, M., Elliott, C., Ortmann, B., Schulze-Lefert, P., and Panstruga, R. (2005) Plant Cell 17(1), 149-163 17. Di Cola, A., Frigerio, L., Lord, J. M., Ceriotti, A., and Roberts, L. M. (2001) Proc Natl Acad Sci U S A 98(25), 14726-14731 18. Di Cola, A., Frigerio, L., Lord, J. M., Roberts, L. M., and Ceriotti, A. (2005) Plant Physiol 137(1), 287-296 19. Tabe, L. M., Wardley-Richardson, T., Ceriotti, A., Aryan, A., McNabb, W., Moore, A., and Higgins, T. J. (1995) J Anim Sci 73(9), 2752-2759 20. Hellens, R. P., Edwards, E. A., Leyland, N. R., Bean, S., and Mullineaux, P. M. (2000) Plant Mol Biol 42(6), 819-832 21. Frigerio, L., Vitale, A., Lord, J. M., Ceriotti, A., and Roberts, L. M. (1998) J Biol Chem 273(23), 14194-14199 22. Pedrazzini, E., Giovinazzo, G., Bielli, A., de Virgilio, M., Frigerio, L., Pesca, M., Faoro, F., Bollini, R., Ceriotti, A., and Vitale, A. (1997) Plant Cell 9(10), 1869-1880 23. Hunter, P. R., Craddock, C. P., Di Benedetto, S., Roberts, L. M., and Frigerio, L. (2007) Plant Physiol 24. Chaddock, J. A., and Roberts, L. M. (1993) Protein Eng 6(4), 425-431 25. Jolliffe, N. A., Di Cola, A., Marsden, C. J., Lord, J. M., Ceriotti, A., Frigerio, L., and Roberts, L. M. (2006) J Biol Chem 281(33), 23377-23385 26. Roberts, L. M., Lamb, F. I., Pappin, D. J., and Lord, J. M. (1985) J Biol Chem 260(29), 15682-15686 27. Campbell, R. E., Tour, O., Palmer, A. E., Steinbach, P. A., Baird, G. S., Zacharias, D. A., and Tsien, R. Y. (2002) Proc Natl Acad Sci U S A 99(12), 7877-7882 28. Maliga, P., Sz-Breznovits, A., and Marton, L. (1973) Nat New Biol 244(131), 29-30 29. Denecke, J., Carlsson, L. E., Vidal, S., Hoglund, A. S., Ek, B., van Zeijl, M. J., Sinjorgo, K. M., and Palva, E. T. (1995) Plant Cell 7(4), 391-406 30. Klein, E. M., Mascheroni, L., Pompa, A., Ragni, L., Weimar, T., Lilley, K. S., Dupree, P., and Vitale, A. (2006) Plant J 48(5), 657-673 31. Martinez, I. M., and Chrispeels, M. J. (2003) Plant Cell 15(2), 561-576 32. Allen, S. C. H., Moore, K. A. H., Marsden, C. J., Fulop, V., Moffat, K. G., Lord, J. M., Ladds, G., and Roberts, L. M. (2007) FEBS Journal In press 33. Roberts, L. M., and Lord, J. M. (1981) Eur J Biochem 119(1), 31-41 34. Wojcik, C., Yano, M., and DeMartino, G. N. (2004) J Cell Sci 117(Pt 2), 281- 292 35. Dalal, S., Rosser, M. F., Cyr, D. M., and Hanson, P. I. (2004) Mol Biol Cell 15(2), 637-648 36. Simpson, J. C., Lord, J. M., and Roberts, L. M. (1995) Eur J Biochem 232(2), 458-463 37. Day, P. J., Pinheiro, T. J., Roberts, L. M., and Lord, J. M. (2002) Biochemistry 41(8), 2836-2843 38. Tsai, B., Ye, Y., and Rapoport, T. A. (2002) Nat Rev Mol Cell Biol 3(4), 246- 255 39. Bays, N., Wilhovsky, S., Goradia, A., Hodgkiss-Harlow, K., and Hampton, R. (2001) Mol. Biol. Cell 12, 4114-4128. 40. Denic, V., Quan, E. M., and Weissman, J. S. (2006) Cell 126(2), 349-359 41. Carvalho, P., Goder, V., and Rapoport, T. A. (2006) Cell 126(2), 361-373 42. Swanson, R., Locher, M., and Hochstrasser, M. (2001) Genes Dev 15(20), 2660-2674 43. Deak, P. M., and Wolf, D. H. (2001) J Biol Chem 276(14), 10663-10669 44. Schuberth, C., and Buchberger, A. (2005) Nat Cell Biol 7(10), 999-1006 45. Richly, H., Rape, M., Braun, S., Rumpf, S., Hoege, C., and Jentsch, S. (2005) Cell 120(1), 73-84 46. Yoshida, Y., Chiba, T., Tokunaga, F., Kawasaki, H., Iwai, K., Suzuki, T., Ito, Y., Matsuoka, K., Yoshida, M., Tanaka, K., and Tai, T. (2002) Nature 418(6896), 438-442 47. Yoshida, Y., Tokunaga, F., Chiba, T., Iwai, K., Tanaka, K., and Tai, T. (2003) J Biol Chem 278(44), 43877-43884 48. Wiertz, E., Jones, T., Sun, I., M Bogyo, M., Geuze, H., and Ploegh, H. (1996) Cell 84, 769-779 49. Brandizzi, F., Hanton, S., DaSilva, L. L., Boevink, P., Evans, D., Oparka, K., Denecke, J., and Hawes, C. (2003) Plant J 34(3), 269-281 50. Roberts, L. M., and Smith, D. C. (2004) Toxicon 44(5), 469-472 51. Lord, M. J., Jolliffe, N. A., Marsden, C. J., Pateman, C. S., Smith, D. C., Spooner, R. A., Watson, P. D., and Roberts, L. M. (2003) Toxicol Rev 22(1), 53-64 52. Deeks, E. D., Cook, J. P., Day, P. J., Smith, D. C., Roberts, L. M., and Lord, J. M. (2002) Biochemistry 41(10), 3405-3413 53. Wahlman, J., DeMartino, G. N., Skach, W. R., Bulleid, N. J., Brodsky, J. L., and Johnson, A. E. (2007) Cell 129(5), 943-955 54. Wojcik, C., Rowicka, M., Kudlicki, A., Nowis, D., McConnell, E., Kujawa, M., and DeMartino, G. N. (2006) Mol Biol Cell 17(11), 4606-4618 55. Carlson, E. J., Pitonzo, D., and Skach, W. R. (2006) Embo J 25(19), 4557- 4566 56. Vashist, S., Kim, W., Belden, W. J., Spear, E. D., Barlowe, C., and Ng, D. T. (2001) J Cell Biol 155(3), 355-368 57. Vashist, S., and Ng, D. T. (2004) J Cell Biol 165(1), 41-52 58. Caldwell, S. R., Hill, K. J., and Cooper, A. A. (2001) J Biol Chem 276(26), 23296-23303 59. Schmid, M., Davison, T. S., Henz, S. R., Pape, U. J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D., and Lohmann, J. U. (2005) Nat Genet 37(5), 501- 506 60. Kirst, M. E., Meyer, D. J., Gibbon, B. C., Jung, R., and Boston, R. S. (2005) Plant Physiol 138(1), 218-231 61. Smalle, J., and Vierstra, R. D. (2004) Annu Rev Plant Biol 55, 555-590 62. Carter, C., Pan, S., Zouhar, J., Avila, E. L., Girke, T., and Raikhel, N. V. (2004) Plant Cell 16(12), 3285-3303 63. Contento, A. L., Kim, S. J., and Bassham, D. C. (2004) Plant Physiol 135(4), 2330-2347 64. Pimpl, P., Taylor, J. P., Snowden, C., Hillmer, S., Robinson, D. G., and Denecke, J. (2006) Plant Cell 18(1), 198-211
URI:	http://wrap.warwick.ac.uk/id/eprint/4446

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