Fertilization-induced K63-linked ubiquitylation mediates clearance of maternal membrane proteins

Development (Cambridge)

Volumn 141, Issue 6, 2014, Pages 1324-1331

  Sato, Miyuki ^a   Konuma, Ryosuke ^a   Sato, Katsuya ^a   Tomura, Kotone ^a   Sato, Ken ^a  

^a GUNMA UNIVERSITY   (Japan)

Author keywords

Endocytosis; K63 linked ubiquitin chains; Multivesicular body (MVB) pathway; Oocyte to zygote transition; Ubc13

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CAVEOLIN 1; CAVEOLIN 1 GREEN FLUORESCENT FUSION PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; K63 LINKED POLYUBIQUITIN; LIGASE; MATERNAL MEMBRANE PROTEIN; MEMBRANE PROTEIN; POLYUBIQUITIN; UBIQUITIN CONJUGATING ENZYME 13; UBIQUITIN CONJUGATING ENZYME E2; UEV 1 LIGASE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BIOACCUMULATION; CAENORHABDITIS ELEGANS; CELL CYCLE; CELL MEMBRANE; CELL SELECTION; CELL SURFACE; CONTROLLED STUDY; EMBRYO; ENDOSOME; FEMALE; FERTILIZATION; INTERNALIZATION; MEIOSIS; MULTIVESICULAR BODY; MUTANT; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN CLEARANCE; PROTEIN METABOLISM; UBIQUITINATION;

ENDOCYTOSIS; K63-LINKED UBIQUITIN CHAINS; MULTIVESICULAR BODY (MVB) PATHWAY; OOCYTE-TO-ZYGOTE TRANSITION; UBC13;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CAVEOLINS; ENDOCYTOSIS; FEMALE; FERTILIZATION; GENES, HELMINTH; MALE; MEMBRANE PROTEINS; MUTATION; OOCYTES; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION; ZYGOTE;

EID: 84896850176     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.103044     Document Type: Article

References (49)

1. Al Rawi, S., Louvet-Vallée, S., Djeddi, A., Sachse, M., Culetto, E., Hajjar, C., Boyd, L., Legouis, R. and Galy, V. (2011). Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334, 1144-1147.
2. Audhya, A., McLeod, I. X., Yates, J. R. and Oegema, K. (2007). MVB-12, a fourth subunit of metazoan ESCRT-I, functions in receptor downregulation. PLoS ONE 2, e956.
3. Balklava, Z., Pant, S., Fares, H. and Grant, B. D. (2007). Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 9, 1066-1073.
4. Barriere, H., Nemes, C., Du, K. and Lukacs, G. L. (2007). Plasticity of polyubiquitin recognition as lysosomal targeting signals by the endosomal sorting machinery. Mol. Biol. Cell 18, 3952-3965.
5. Bowerman, B. and Kurz, T. (2006). Degrade to create: developmental requirements for ubiquitin-mediated proteolysis during early C. elegans embryogenesis. Development 133, 773-784.
6. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
7. Deng, L., Wang, C., Spencer, E., Yang, L., Braun, A., You, J., Slaughter, C., Pickart, C. and Chen, Z. J. (2000). Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 103, 351-361.
8. Eddins, M. J., Carlile, C. M., Gomez, K. M., Pickart, C. M. and Wolberger, C. (2006). Mms2-Ubc13 covalently bound to ubiquitin reveals the structural basis of linkagespecific polyubiquitin chain formation. Nat. Struct. Mol. Biol. 13, 915-920.
9. Erpapazoglou, Z., Dhaoui, M., Pantazopoulou, M., Giordano, F., Mari, M., Léon, S., Raposo, G., Reggiori, F. and Haguenauer-Tsapis, R. (2012). A dual role for K63-linked ubiquitin chains in multivesicular body biogenesis and cargo sorting. Mol. Biol. Cell 23, 2170-2183.
10. Fukushima, T., Matsuzawa, S., Kress, C. L., Bruey, J. M., Krajewska, M., Lefebvre, S., Zapata, J. M., Ronai, Z. and Reed, J. C. (2007). Ubiquitin-conjugating enzyme Ubc13 is a critical component of TNF receptor-associated factor (TRAF)-mediated inflammatory responses. Proc. Natl. Acad. Sci. USA 104, 6371-6376.
11. Goto, E., Yamanaka, Y., Ishikawa, A., Aoki-Kawasumi, M., Mito-Yoshida, M., Ohmura-Hoshino, M., Matsuki, Y., Kajikawa, M., Hirano, H. and Ishido, S. (2010). Contribution of lysine 11-linked ubiquitination to MIR2-mediated major histocompatibility complex class I internalization. J. Biol. Chem. 285, 35311-35319.
12. Grant, B. and Hirsh, D. (1999). Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10, 4311-4326.
13. Haglund, K. and Dikic, I. (2012). The role of ubiquitylation in receptor endocytosis and endosomal sorting. J. Cell Sci. 125, 265-275.
14. Hofmann, R. M. and Pickart, C. M. (1999). Noncanonical MMS2-encoded ubiquitinconjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96, 645-653.
15. Huang, F., Kirkpatrick, D., Jiang, X., Gygi, S. and Sorkin, A. (2006). Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol. Cell 21, 737-748.
16. Johnston, W. L. and Dennis, J. W. (2012). The eggshell in the C. elegans oocyte-toembryo transition. Genesis 50, 333-349.
17. Johnston, W. L., Krizus, A. and Dennis, J. W. (2010). Eggshell chitin and chitininteracting proteins prevent polyspermy in C. elegans. Curr. Biol. 20, 1932-1937.
18. Kadandale, P., Stewart-Michaelis, A., Gordon, S., Rubin, J., Klancer, R., Schweinsberg, P., Grant, B. D. and Singson, A. (2005). The egg surface LDL receptor repeat-containing proteins EGG-1 and EGG-2 are required for fertilization in Caenorhabditis elegans. Curr. Biol. 15, 2222-2229.
19. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
20. Kerscher, O., Felberbaum, R. and Hochstrasser, M. (2006). Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159-180.
21. Kramer, L. B., Shim, J., Previtera, M. L., Isack, N. R., Lee, M. C., Firestein, B. L. and Rongo, C. (2010). UEV-1 is an ubiquitin-conjugating enzyme variant that regulates glutamate receptor trafficking in C. elegans neurons. PLoS ONE 5, e14291.
22. L'Hernault, S. W. (2006). Spermatogenesis. In WormBook (ed. The C. elegans Research Community). doi/10.1895/wormbook.1.85.1, http://www.wormbook.org.
23. Lauwers, E., Jacob, C. and André, B. (2009). K63-linked ubiquitin chains as a specific signal for protein sorting into the multivesicular body pathway. J. Cell Biol. 185, 493-502.
24. Lauwers, E., Erpapazoglou, Z., Haguenauer-Tsapis, R. and André, B. (2010). The ubiquitin code of yeast permease trafficking. Trends Cell Biol. 20, 196-204.
25. Lin, R. (2003). A gain-of-function mutation in oma-1, a C. elegans gene required for oocyte maturation, results in delayed degradation of maternal proteins and embryonic lethality. Dev. Biol. 258, 226-239.
26. Maruyama, R., Velarde, N. V., Klancer, R., Gordon, S., Kadandale, P., Parry, J. M., Hang, J. S., Rubin, J., Stewart-Michaelis, A., Schweinsberg, P. et al. (2007). EGG-3 regulates cell-surface and cortex rearrangements during egg activation in Caenorhabditis elegans. Curr. Biol. 17, 1555-1560.
27. Mayers, J. R., Wang, L., Pramanik, J., Johnson, A., Sarkeshik, A., Wang, Y., Saengsawang, W., Yates, J. R., III and Audhya, A. (2013). Regulation of ubiquitindependent cargo sorting by multiple endocytic adaptors at the plasma membrane. Proc. Natl. Acad. Sci. USA 110, 11857-11862.
28. McCarter, J., Bartlett, B., Dang, T. and Schedl, T. (1999). On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 205, 111-128.
29. Mukhopadhyay, D. and Riezman, H. (2007). Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315, 201-205.
30. Newton, K., Matsumoto, M. L., Wertz, I. E., Kirkpatrick, D. S., Lill, J. R., Tan, J., Dugger, D., Gordon, N., Sidhu, S. S., Fellouse, F. A. et al. (2008). Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies. Cell 134, 668-678.
31. Pellettieri, J., Reinke, V., Kim, S. K. and Seydoux, G. (2003). Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Dev. Cell 5, 451-462.
32. Pickart, C. M. and Fushman, D. (2004). Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 8, 610-616.
33. Praitis, V., Casey, E., Collar, D. and Austin, J. (2001). Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217-1226.
34. Raiborg, C. and Stenmark, H. (2009). The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452.
35. Sato, M. and Sato, K. (2011). Degradation of paternal mitochondria by fertilizationtriggered autophagy in C. elegans embryos. Science 334, 1141-1144.
36. Sato, M. and Sato, K. (2013). Dynamic regulation of autophagy and endocytosis for cell remodeling during early development. Traffic 14, 479-486.
37. Sato, M., Sato, K., Fonarev, P., Huang, C. J., Liou, W. and Grant, B. D. (2005). Caenorhabditis elegans RME-6 is a novel regulator of RAB-5 at the clathrin-coated pit. Nat. Cell Biol. 7, 559-569.
38. Sato, K., Sato, M., Audhya, A., Oegema, K., Schweinsberg, P. and Grant, B. D. (2006). Dynamic regulation of caveolin-1 trafficking in the germ line and embryo of Caenorhabditis elegans. Mol. Biol. Cell 17, 3085-3094.
39. Sato, M., Grant, B. D., Harada, A. and Sato, K. (2008). Rab11 is required for synchronous secretion of chondroitin proteoglycans after fertilization in Caenorhabditis elegans. J. Cell Sci. 121, 3177-3186.
40. Spike, C. A. and Strome, S. (2003). Germ plasm: protein degradation in the soma. Curr. Biol. 13, R837-R839.
41. Stiernagle, T. (1999). Maintenance of C. elegans. In C. elegans; A Practical Approach (ed. I. A. Hope), pp. 51-67. Oxford: Oxford University Press.
42. Stitzel, M. L. and Seydoux, G. (2007). Regulation of the oocyte-to-zygote transition. Science 316, 407-408.
43. Stitzel, M. L., Cheng, K. C. and Seydoux, G. (2007). Regulation of MBK-2/Dyrk kinase by dynamic cortical anchoring during the oocyte-to-zygote transition. Curr. Biol. 17, 1545-1554.
44. Stringer, D. K. and Piper, R. C. (2011). A single ubiquitin is sufficient for cargo protein entry into MVBs in the absence of ESCRT ubiquitination. J. Cell Biol. 192, 229-242.
45. Traub, L. M. and Lukacs, G. L. (2007). Decoding ubiquitin sorting signals for clathrindependent endocytosis by CLASPs. J. Cell Sci. 120, 543-553.
46. Tsukamoto, S., Hara, T., Yamamoto, A., Ohta, Y., Wada, A., Ishida, Y., Kito, S., Nishikawa, T., Minami, N., Sato, K. et al. (2013). Functional analysis of lysosomes during mouse preimplantation embryo development. J. Reprod. Dev. 59, 33-39.
47. Wu, X., Yamamoto, M., Akira, S. and Sun, S. C. (2009). Regulation of hematopoiesis by the K63-specific ubiquitin-conjugating enzyme Ubc13. Proc. Natl. Acad. Sci. USA 106, 20836-20841.
48. Yamamoto, M., Okamoto, T., Takeda, K., Sato, S., Sanjo, H., Uematsu, S., Saitoh, T., Yamamoto, N., Sakurai, H., Ishii, K. J. et al. (2006). Key function for the Ubc13 E2 ubiquitin-conjugating enzyme in immune receptor signaling. Nat. Immunol. 7, 962-970.
49. Ye, Y. and Rape, M. (2009). Building ubiquitin chains: E2 enzymes at work. Nat. Rev. Mol. Cell Biol. 10, 755-764.