Inactivation of Caenorhabditis elegans aminopeptidase DNPP-1 restores endocytic sorting and recycling in tat-1 mutants

Molecular Biology of the Cell

Volumn 24, Issue 8, 2013, Pages 1163-1175

  Li, Xin ^a,b   Chen, Baohui ^b   Yoshina, Sawako ^c   Cai, Tanxi ^d   Yang, Fuquan ^d   Mitani, Shohei ^c   Wang, Xiaochen ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^c TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^d INSTITUTE OF BIOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINOPEPTIDASE DNPP 1; ASPARTYL AMINOPEPTIDASE; FUNGAL ENZYME; GLUCOSE TRANSPORTER 1; MUTANT PROTEIN; RAB PROTEIN; TAT 1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BASOLATERAL MEMBRANE; CAENORHABDITIS ELEGANS; CELL MEMBRANE; CELL VACUOLE; EMBRYO DEVELOPMENT; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; ENZYME INACTIVATION; INTESTINE CELL; INTRACELLULAR MEMBRANE; LYSOSOME; MEMBRANE LEAFLET; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN METABOLISM; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SURFACE CHARGE;

AMINOPEPTIDASES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL MEMBRANE; ENDOCYTOSIS; ENDOSOMES; INTESTINES; KINETICS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; ORGAN SPECIFICITY; PHOSPHATIDYLSERINES; PHOSPHOLIPID TRANSFER PROTEINS; PROTEIN TRANSPORT; PROTEOLYSIS;

CAENORHABDITIS ELEGANS;

EID: 84876565480     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-10-0730     Document Type: Article

References (37)

1. Babbey CM, Ahktar N, Wang E, Chen CC, Grant BD, Dunn KW (2006). Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 17, 3156-3175. (Pubitemid 43993517)
2. Cadel S, Pierotti AR, Foulon T, Creminon C, Barre N, Segretain D, Cohen P (1995). Aminopeptidase-B in the rat testes: isolation, functional properties and cellular localization in the seminiferous tubules. Mol Cell Endocrinol 110, 149-160.
3. Chen B, Jiang Y, Zeng S, Yan J, Li X, Zhang Y, Zou W, Wang X (2010). Endocytic sorting and recycling require membrane phosphatidylserine asymmetry maintained by TAT-1/CHAT-1. PLoS Genet 6, e1001235.
4. Chen CC, Schweinsberg PJ, Vashist S, Mareiniss D P, Lambie EJ, Grant BD (2006). RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol Biol Cell 17, 1286-1297. (Pubitemid 43376549)
5. Chen Y, Farquhar ER, Chance MR, Palczewski K, Kiser PD (2012). Insights into substrate specifcity and metal activation of mammalian tetrahedral aspartyl aminopeptidase. J Biol Chem 287, 13356-13370.
6. Darland-Ransom M, Wang X, Sun CL, Mapes J, Gengyo-Ando K, Mitani S, Xue D (2008). Role of C. elegans TAT-1 protein in maintaining plasma membrane phosphatidylserine asymmetry. Science 320, 528-531. (Pubitemid 351590665)
7. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, McMahon HT (2007). Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449, 923-927. (Pubitemid 47598607)
8. Grant B, Hirsh D (1999). Receptor-mediated endocytosis in the Caenorhab-ditis elegans oocyte. Mol Biol Cell 10, 4311-4326.
9. Grant B, Zhang Y, Paupard MC, Lin SX, Hall DH, Hirsh D (2001). Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat Cell Biol 3, 573-579. (Pubitemid 32536854)
10. Grant BD, Caplan S (2008). Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffc 9, 2043-2052.
11. Grant BD, Donaldson JG (2009). Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10, 597-608.
12. Gruenberg J (2001). The endocytic pathway: a mosaic of domains. Nat Rev Mol Cell Biol 2, 721-730. (Pubitemid 33679834)
13. Harford J, Bridges K, Ashwell G, Klausner RD (1983). Intracellular dissociation of receptor-bound asialoglycoproteins in cultured hepatocytes. A pH-mediated nonlysosomal event. J Biol Chem 258, 3191-3197.
14. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006). PI(3, 4, 5)P3 and PI(4, 5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461. (Pubitemid 44871952)
15. Hersh LB, Aboukhair N, Watson S (1987). Immunohistochemical localization of aminopeptidase M in rat brain and periphery: relationship of enzyme localization and enkephalin metabolism. Peptides 8, 523-532. (Pubitemid 17119188)
16. Jovic M, Sharma M, Rahajeng J, Caplan S (2010). The early endosome: a busy sorting station for proteins at the crossroads. Histol Histopathol 25, 99-112.
17. Kamath RS, Ahringer J (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321. (Pubitemid 36793968)
18. Kelly JA, Neidle EL, Neidle A (1983). An aminopeptidase from mouse brain cytosol that cleaves N-terminal acidic amino acid residues. J Neurochem 40, 1727-1734. (Pubitemid 13106955)
19. Kostich M, Fire A, Fambrough DM (2000). Identifcation and molecular-genetic characterization of a LAMP/CD68-like protein from Caenorhabditis elegans. J Cell Sci 113, 2595-2606. (Pubitemid 30599411)
20. Maxfeld FR, McGraw TE (2004). Endocytic recycling. Nat Rev Mol Cell Biol 5, 121-132. (Pubitemid 38160255)
21. McGowan S et al. (2009). Structural basis for the inhibition of the essential Plasmodium falciparum M1 neutral aminopeptidase. Proc Natl Acad Sci USA 106, 2537-2542.
22. McLaughlin S, Murray D (2005). Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438, 605-611. (Pubitemid 41740564)
23. McMahon HT, Gallop JL (2005). Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596. (Pubitemid 41740562)
24. Mukherjee S, Ghosh RN, Maxfeld FR (1997). Endocytosis. Physiol Rev 77, 759-803. (Pubitemid 27328740)
25. Nilsson L, Conradt B, Ruaud AF, Chen CC, Hatzold J, Bessereau JL, Grant BD, Tuck S (2008). Caenorhabditis elegans num-1 negatively regulates endocytic recycling. Genetics 179, 375-387.
26. Nilsson L, Jonsson E, Tuck S (2011). Caenorhabditis elegans numb inhibits endocytic recycling by binding TAT-1 aminophospholipid translocase. Traffc 12, 1839-1849.
27. Pant S, Sharma M, Patel K, Caplan S, Carr CM, Grant BD (2009). AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat Cell Biol 11, 1399-1410.
28. Roy MO, Leventis R, Silvius JR (2000). Mutational and biochemical analysis of plasma membrane targeting mediated by the farnesylated, polybasic carboxy terminus of K-ras4B. Biochemistry 39, 8298-8307. (Pubitemid 30460982)
29. Ruaud AF, Nilsson L, Richard F, Larsen MK, Bessereau JL, Tuck S (2009). The C. elegans P4-ATPase TAT-1 regulates lysosome biogenesis and endocy-tosis. Traffc 10, 88-100.
30. Sano H, Eguez L, Teruel MN, Fukuda M, Chuang TD, Chavez JA, Lienhard GE, McGraw TE (2007). Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab 5, 293-303. (Pubitemid 46477855)
31. Shi A, Liu O, Koenig S, Banerjee R, Chen CC, Eimer S, Grant BD (2012). RAB-10-GTPase-mediated regulation of endosomal phosphatidylinosi-tol-4, 5-bisphosphate. Proc Natl Acad Sci USA 109, E2306-E2315.
32. Sim MK, Choo MH, Qiu XS (1994). Degradation of angiotensin I to [des-Asp1]angiotensin I by a novel aminopeptidase in the rat hypothalamus. Biochem Pharmacol 48, 1043-1046. (Pubitemid 24285183)
33. Sune A, Bienvenue A (1988). Relationship between the transverse distribution of phospholipids in plasma membrane and shape change of human platelets. Biochemistry 27, 6794-6800.
34. Taylor A (1993). Aminopeptidases: structure and function. FASEB J 7, 290-298. (Pubitemid 23067779)
35. Wilk S, Wilk E, Magnusson RP (1998). Purifcation, characterization, and cloning of a cytosolic aspartyl aminopeptidase. J Biol Chem 273, 15961-15970. (Pubitemid 28311361)
36. Wilk S, Wilk E, Magnusson RP (2002). Identifcation of histidine residues important in the catalysis and structure of aspartyl aminopeptidase. Arch Biochem Biophys 407, 176-183. (Pubitemid 35341045)
37. Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, Grinstein S (2008). Membrane phosphatidylserine regulates surface charge and protein localization. Science 319, 210-213.