Glycosome turnover in Leishmania major is mediated by autophagy

References

• den Boer M, Argaw D, Jannin J, Alvar J. Leishmaniasis impact and treatment access. Clin Microbiol Infect 2011; 17 (10):1471-7; PMID:21933305; http://dx.doi.org/10.1111/j.1469-0691.2011.03635.x
   PubMed Web of Science ®Google Scholar
• Kaye P, Scott P. Leishmaniasis: complexity at the hostpathogen interface. Nat Rev Micro 2011; 9 (8):604-15; PMID:21747391; http://dx.doi.org/10.1038/nrmicro2608
   PubMed Web of Science ®Google Scholar
• Besteiro S, Williams RAM, Coombs GH, Mottram JC. Protein turnover and differentiation in Leishmania. Int J Parasitol 2007; 37 (10):1063-75; PMID:17493624; http://dx.doi.org/10.1016/j.ijpara.2007.03.008
   PubMed Web of Science ®Google Scholar
• Huete-Pérez JA, Engel JC, Brinen LS, Mottram JC, McKerrow JH. Protease trafficking in two primitive eukaryotes is mediated by a prodomain protein motif. J Biol Chem 1999; 274 (23):16249-56; PMID:10347181; http://dx.doi.org/10.1074/jbc.274.23.16249
   PubMed Web of Science ®Google Scholar
• Besteiro S, Coombs G, Mottram J. The SNARE protein family of Leishmania major. BMC Genomics 2006; 7 (1):250; PMID:17026746; http://dx.doi.org/10.1186/1471-2164-7-250
   PubMed Web of Science ®Google Scholar
• Mullin KA, Foth BJ, Ilgoutz SC, Callaghan JM, Zawadzki JL, McFadden GI, McConville MJ. Regulated degradation of an endoplasmic reticulum membrane protein in a tubular lysosome in Leishmania mexicana. Mol Biol Cell 2001; 12 (8):2364-77; PMID:11514622; http://dx.doi.org/10.1091/mbc.12.8.2364
   PubMed Web of Science ®Google Scholar
• Coombs GH, Tetley L, Moss VA, Vickerman K. Three dimensional structure of the leishmania amastigote as revealed by computer-aided reconstruction from serial sections. Parasitology 1986; 92 (01):13-23; PMID:3754324; http://dx.doi.org/10.1017/S0031182000063411
   PubMed Web of Science ®Google Scholar
• Ueda-Nakamura T, Attias M, de Souza W. Megasome biogenesis in Leishmania amazonensis: a morphometric and cytochemical study. Parasitol Res 2001; 87 (2):89-97; PMID:11206117; http://dx.doi.org/10.1007/s004360000319
   PubMed Web of Science ®Google Scholar
• Brooks DR, Denise H, Westrop GD, Coombs GH, Mottram JC. The stage-regulated expression of Leishmania mexicana CPB cysteine proteases is mediated by an intercistronic sequence element. J Biol Chem 2001; 276 (50):47061-9; PMID:11592967; http://dx.doi.org/10.1074/jbc.M108498200
   PubMed Web of Science ®Google Scholar
• Ueda-Nakamura T, da Conceição Rocha Sampaio M, Cunha-e-Silva NL, Traub-Cseko Y, de Souza W. Expression and processing of megasome cysteine proteinases during Leishmania amazonensis differentiation. Parasitol Res 2002; 88 (4):332-7; PMID:11999020; http://dx.doi.org/10.1007/s00436-001-0516-0
   PubMed Web of Science ®Google Scholar
• Dice JF. Chaperone-mediated autophagy. Autophagy 2007; 3 (4):295-9; PMID:17404494; http://dx.doi.org/10.4161/auto.4144
   PubMed Web of Science ®Google Scholar
• Mijaljica D, Prescott M, Devenish RJ. Microautophagy in mammalian cells: Revisiting a 40-year-old conundrum. Autophagy 2011; 7 (7):673-82; PMID:21646866; http://dx.doi.org/10.4161/auto.7.7.14733
   PubMed Web of Science ®Google Scholar
• Kraft C, Reggiori F, Peter M. Selective types of autophagy in yeast. Biochim Biophys Acta 2009; 1793 (9):1404-12; PMID:19264099; http://dx.doi.org/10.1016/j.bbamcr.2009.02.006
   PubMed Web of Science ®Google Scholar
• Cebollero E, Reggiori F, Kraft C. Reticulophagy and ribophagy: regulated degradation of protein production factories. Int J Cell Biol 2012; 2012:182834; PMID:22481944; http://dx.doi.org/10.1155/2012/182834
   PubMedGoogle Scholar
• Lamark T, Johansen T. Aggrephagy: selective disposal of protein aggregates by macroautophagy. Int J Cell Biol 2012; 2012:736905; PMID:22518139; http://dx.doi.org/10.1155/2012/736905
   PubMedGoogle Scholar
• Wang K, Klionsky DJ. Mitochondria removal by autophagy. Autophagy 2011; 7 (3):297-300; PMID:21252623; http://dx.doi.org/10.4161/auto.7.3.14502
   PubMed Web of Science ®Google Scholar
• Mostowy S, Sancho-Shimizu V, Hamon MA, Simeone R, Brosch R, Johansen T, Cossart P. p62 and NDP52 proteins target intracytosolic Shigella and Listeria to different autophagy pathways. J Biol Chem 2011; 286 (30):26987-95; PMID:21646350; http://dx.doi.org/10.1074/jbc.M111.223610
   PubMed Web of Science ®Google Scholar
• Sumpter R, Levine B. Selective autophagy and viruses. Autophagy 2011; 7 (3):260-5; PMID:21150267; http://dx.doi.org/10.4161/auto.7.3.14281
   PubMed Web of Science ®Google Scholar
• Brennand A, Gualdrón-López M, Coppens I, Rigden DJ, Ginger ML, Michels PAM. Autophagy in parasitic protists: unique features and drug targets. Mol Biochem Parasitol 2011; 177 (2):83-99; PMID:21315770; http://dx.doi.org/10.1016/j.molbiopara.2011.02.003
   PubMed Web of Science ®Google Scholar
• Williams RA, Tetley L, Mottram JC, Coombs GH. Cysteine peptidases CPA and CPB are vital for autophagy and differentiation in Leishmania mexicana. Mol Microbiol 2006; 61 (3):655-74; PMID:16803590; http://dx.doi.org/10.1111/j.1365-2958.2006.05274.x
   PubMed Web of Science ®Google Scholar
• Besteiro S, Williams RAM, Morrison LS, Coombs GH, Mottram JC. Endosome sorting and autophagy are essential for differentiation and virulence of Leishmania major. J Biol Chem 2006; 281 (16):11384-96; PMID:16497676; http://dx.doi.org/10.1074/jbc.M512307200
   PubMed Web of Science ®Google Scholar
• Williams RAM, Smith TK, Cull B, Mottram JC, Coombs GH. ATG5 is essential for ATG8-dependent autophagy and mitochondrial homeostasis in Leishmania major. PLoS Pathog 2012; 8 (5):e1002695; PMID:22615560; http://dx.doi.org/10.1371/journal.ppat.1002695
   PubMed Web of Science ®Google Scholar
• Michels PAM, Bringaud F, Herman M, Hannaert V. Metabolic functions of glycosomes in trypanosomatids. Biochimica et Biophysica Acta (BBA) - Mol Cell Res 2006; 1763 (12):1463-77; PMID:17023066; http://dx.doi.org/10.1016/j.bbamcr.2006.08.019
   PubMed Web of Science ®Google Scholar
• Haanstra JR, van Tuijl A, Kessler P, Reijnders W, Michels PAM, Westerhoff HV, Parsons M, Bakker BM. Compartmentation prevents a lethal turbo-explosion of glycolysis in trypanosomes. Proc Natl Acad Sci USA 2008; 105 (46):17718-23; PMID:19008351; http://dx.doi.org/10.1073/pnas.0806664105
   PubMed Web of Science ®Google Scholar
• Guerra-Giraldez C, Quijada L, Clayton CE. Compartmentation of enzymes in a microbody, the glycosome, is essential in Trypanosoma brucei. J Cell Sci 2002; 115 (13):2651-8; PMID:12077356
   PubMed Web of Science ®Google Scholar
• Plewes KA, Barr SD, Gedamu L. Iron superoxide dismutases targeted to the glycosomes of Leishmania chagasi are important for survival. Infect Immun 2003; 71 (10):5910-20; PMID:14500512; http://dx.doi.org/10.1128/IAI.71.10.5910-5920.2003
   PubMed Web of Science ®Google Scholar
• Naderer T, Ellis MA, Sernee MF, De Souza DP, Curtis J, Handman E, McConville MJ. Virulence of Leishmania major in macrophages and mice requires the gluconeogenic enzyme fructose-1,6-bisphosphatase. Proc Natl Acad Sci USA 2006; 103 (14):5502-7; PMID:16569701; http://dx.doi.org/10.1073/pnas.0509196103
   PubMed Web of Science ®Google Scholar
• Kumar R, Gupta S, Srivastava R, Sahasrabuddhe AA, Gupta CM. Expression of a PTS2-truncated hexokinase produces glucose toxicity in Leishmania donovani. Mol Biochem Parasitol 2010; 170 (1):41-4; PMID:19925831; http://dx.doi.org/10.1016/j.molbiopara.2009.11.002
   PubMed Web of Science ®Google Scholar
• da Silva MFL, Zampieri RA, Muxel SM, Beverley SM, Floeter-Winter LM. Leishmania amazonensis arginase compartmentalization in the glycosome is important for parasite infectivity. PLoS One 2012; 7 (3):e34022; PMID:22479507; http://dx.doi.org/10.1371/journal.pone.0034022
   PubMedGoogle Scholar
• Herman M, Perez-Mora D, Schtickzelle N, Michels PAM. Turnover of glycosomes during life-cycle differentiation of Trypanosoma brucei. Autophagy 2008; 4 (3):294-308; PMID:18365344; http://dx.doi.org/10.4161/auto.5443
   PubMed Web of Science ®Google Scholar
• Hart DT, Coombs GH. Leishmania mexicana: energy metabolism of amastigotes and promastigotes. Exp Parasitol 1982; 54 (3):397-409; PMID:7151947; http://dx.doi.org/10.1016/0014-4894(82)90049-2
   PubMed Web of Science ®Google Scholar
• Brotherton MC, Racine G, Foucher AL, Drummelsmith J, Papadopoulou B, Ouellette M. Analysis of stage-specific expression of basic proteins in Leishmania infantum. J Proteome Res 2010; 9 (8):3842-53; PMID:20583757; http://dx.doi.org/10.1021/pr100048m
   PubMed Web of Science ®Google Scholar
• Rosenzweig D, Smith D, Opperdoes F, Stern S, Olafson RW, Zilberstein D. Retooling Leishmania metabolism: from sand fly gut to human macrophage. FASEB J 2008; 22 (2):590-602; PMID:17884972; http://dx.doi.org/10.1096/fj.07-9254com
   PubMed Web of Science ®Google Scholar
• Dunn WA, Cregg JM, Kiel JAKW, van der Klei IJ, Oku M, Sakai Y, Sibirny AA, Stasyk OV, Veenhuis M. Pexophagy - the selective autophagy of peroxisomes. Autophagy 2005; 1 (2):75-83; PMID:16874024; http://dx.doi.org/10.4161/auto.1.2.1737
   PubMed Web of Science ®Google Scholar
• Sommer JM, Cheng QL, Keller GA, Wang CC. In vivo import of firefly luciferase into the glycosomes of Trypanosoma brucei and mutational analysis of the C-terminal targeting signal. Mol Biol Cell 1992; 3 (7):749-59; PMID:1515676; http://dx.doi.org/10.1091/mbc.3.7.749
   PubMed Web of Science ®Google Scholar
• Hart DT, Opperdoes FR. The occurrence of glycosomes (microbodies) in the promastigote stage of four major Leishmania species. Mol Biochem Parasitol 1984; 13 (2):159-72; PMID:6440018; http://dx.doi.org/10.1016/0166-6851(84)90110-5
   PubMed Web of Science ®Google Scholar
• Köchl R, Hu XW, Chan EYW, Tooze SA. Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 2006; 7 (2):129-45; PMID:16420522; http://dx.doi.org/10.1111/j.1600-0854.2005.00368.x
   PubMed Web of Science ®Google Scholar
• Kanki T, Wang K, Baba M, Bartholomew CR, Lynch-Day MA, Du Z, Geng J, Mao K, Yang Z, Yen WL, et al. A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol Biol Cell 2009; 20 (22):4730-8; PMID:19793921; http://dx.doi.org/10.1091/mbc.E09-03-0225
   PubMed Web of Science ®Google Scholar
• Zalila H, González IJ, El Fadili AK, Delgado MB, Desponds C, Schaff C, Fasel N. Processing of metacaspase into a cytoplasmic catalytic domain mediating cell death in Leishmania major. Mol Microbiol 2011; 79 (1):222-39; PMID:21166905; http://dx.doi.org/10.1111/j.1365-2958.2010.07443.x
   PubMed Web of Science ®Google Scholar
• Moreno SNJ, Docampo R. The role of acidocalcisomes in parasitic protists. J Eukaryot Microbiol 2009; 56 (3):208-13; PMID:19527347; http://dx.doi.org/10.1111/j.1550-7408.2009.00404.x
   PubMed Web of Science ®Google Scholar
• Besteiro S, Tonn D, Tetley L, Coombs GH, Mottram JC. The AP3 adaptor is involved in the transport of membrane proteins to acidocalcisomes of Leishmania. J Cell Sci 2008; 121 (5):561-70; PMID:18252798; http://dx.doi.org/10.1242/jcs.022574
   PubMed Web of Science ®Google Scholar
• Vickerman K. The fine structure of Trypanosoma congolense in its bloodstream phase. J Eukaryot Microbiol 1969; 16 (1):54-69; PMID:4896668
   PubMed Web of Science ®Google Scholar
• Sakai Y, Oku M, van der Klei IJ, Kiel JAKW. Pexophagy: autophagic degradation of peroxisomes. Biochim Biophys Acta 2006; 1763 (12):1767-75; PMID:17005271; http://dx.doi.org/10.1016/j.bbamcr.2006.08.023
   PubMed Web of Science ®Google Scholar
• Krick R, Muehe Y, Prick T, Bremer S, Schlotterhose P, Eskelinen EL, Millen J, Goldfarb DS, Thumm M. Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol Biol Cell 2008; 19 (10):4492-505; PMID:18701704; http://dx.doi.org/10.1091/mbc.E08-04-0363
   PubMed Web of Science ®Google Scholar
• Kissová I, Salin B, Schaeffer J, Bhatia S, Manon S, Camougrand N. Selective and non-selective autophagic degradation of mitochondria in yeast. Autophagy 2007; 3 (4):329-36; PMID:17377488; http://dx.doi.org/10.4161/auto.4034
   PubMed Web of Science ®Google Scholar
• Müller O, Sattler T, Flötenmeyer M, Schwarz H, Plattner H, Mayer A. Autophagic tubes: vacuolar invaginations involved in lateral membrane sorting and inverse vesicle budding. J Cell Biol 2000; 151 (3):519-28; PMID:11062254; http://dx.doi.org/10.1083/jcb.151.3.519
   PubMed Web of Science ®Google Scholar
• Sattler T, Mayer A. Cell-free reconstitution of microautophagic vacuole invagination and vesicle formation. J Cell Biol 2000; 151 (3):529-38; PMID:11062255; http://dx.doi.org/10.1083/jcb.151.3.529
   PubMed Web of Science ®Google Scholar
• Kim I, Lemasters JJ. Mitochondrial degradation by autophagy (mitophagy) in GFP-LC3 transgenic hepatocytes during nutrient deprivation. Am J Physiol - Cell Physiol 2011; 300 (2):C308-C317; PMID:21106691; http://dx.doi.org/10.1152/ajpcell.00056.2010
   PubMed Web of Science ®Google Scholar
• Rodriguez-Rocha H, Garcia-Garcia A, Panayiotidis MI, Franco R. DNA damage and autophagy. Mutat Res 2011; 711 (1-2):158-66; PMID:21419786; http://dx.doi.org/10.1016/j.mrfmmm.2011.03.007
   PubMed Web of Science ®Google Scholar
• Stauffert I, Paulini H, Steinmann U, Sippel H, Estler CJ. Investigations on mutagenicity and genotoxicity of pentamidine and some related trypanocidal diamidines. Mutat Res 1990; 245 (2):93-8; PMID:2215556; http://dx.doi.org/10.1016/0165-7992(90)90006-6
   PubMed Web of Science ®Google Scholar
• Williams RAM, Mottram JC, Coombs GH. Distinct roles in autophagy and importance in infectivity of the two ATG4 cysteine peptidases of Leishmania major. J Biol Chem 2013; 288:3678-90; PMID:23166325; http://dx.doi.org/10.1074/jbc.M112.415372
   PubMed Web of Science ®Google Scholar
• Xie Z, Nair U, Geng J, Szefler MB, Rothman ED, Klionsky DJ. Indirect estimation of the area density of Atg8 on the phagophore. Autophagy 2009; 5 (2):217-20; PMID:19088501; http://dx.doi.org/10.4161/auto.5.2.7201
   PubMed Web of Science ®Google Scholar
• Takeshige K, Baba M, Tsuboi S, Noda T, Ohsumi Y. Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol 1992; 119 (2):301-11; PMID:1400575; http://dx.doi.org/10.1083/jcb.119.2.301
   PubMed Web of Science ®Google Scholar
• Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, Elazar Z. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 2010; 29 (11):1792-802; PMID:20418806; http://dx.doi.org/10.1038/emboj.2010.74
   PubMed Web of Science ®Google Scholar
• Twig G, Elorza A, Molina AJA, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 2008; 27 (2):433-46; PMID:18200046; http://dx.doi.org/10.1038/sj.emboj.7601963
   PubMed Web of Science ®Google Scholar
• Rambold AS, Kostelecky B, Elia N, Lippincott-Schwartz J. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci USA 2011; 108 (25):10190-5; PMID:21646527; http://dx.doi.org/10.1073/pnas.1107402108
   PubMed Web of Science ®Google Scholar
• Gomes LC, Benedetto GD, Scorrano L. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 2011; 13 (5):589-98; PMID:21478857; http://dx.doi.org/10.1038/ncb2220
   PubMed Web of Science ®Google Scholar
• Rigden DJ, Michels P, Ginger ML. Autophagy in protists: examples of secondary loss, lineage-specific innovations, and the conundrum of remodeling a single mitochondrion. Autophagy 2009; 5 (6):784-94; PMID:19483474; http://dx.doi.org/10.4161/auto.8838
   PubMed Web of Science ®Google Scholar
• Soubannier V, McLelland GL, Zunino R, Braschi E, Rippstein P, Fon EA, McBride HM. A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr Biol 2012; 22 (2):135-41; PMID:22226745; http://dx.doi.org/10.1016/j.cub.2011.11.057
   PubMed Web of Science ®Google Scholar
• Heo JM, Livnat-Levanon N, Taylor EB, Jones KT, Dephoure N, Ring J, Xie J, Brodsky JL, Madeo F, Gygi SP, et al. A stress-responsive system for mitochondrial protein degradation. Mol Cell 2010; 40 (3):465-80; PMID:21070972; http://dx.doi.org/10.1016/j.molcel.2010.10.021
   PubMed Web of Science ®Google Scholar
• Kristensen AR, Schandorff S, Hoyer-Hansen M, Nielsen MO, Jaattela M, Dengjel J, Andersen JS. Ordered organelle degradation during starvation-induced autophagy. Mol Cell Proteomics 2008; 7 (12):2419-28; PMID:18687634; http://dx.doi.org/10.1074/mcp.M800184-MCP200
   PubMed Web of Science ®Google Scholar
• Sacks DL, Hieny S, Sher A. Identification of cell surface carbohydrate and antigenic changes between noninfective and infective developmental stages of Leishmania major promastigotes. J Immunol 1985; 135 (1):564-9; PMID:2582050
   PubMed Web of Science ®Google Scholar
• Tetaud E, Lecuix I, Sheldrake T, Baltz T, Fairlamb AH. A new expression vector for Crithidia fasciculata and Leishmania. Mol Biochem Parasitol 2002; 120 (2):195-204; PMID:11897125; http://dx.doi.org/10.1016/S0166-6851(02)00002-6
   PubMed Web of Science ®Google Scholar
• Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 2006; 224:213-32; PMID:17210054; http://dx.doi.org/10.1111/j.1365-2818.2006.01706.x
   PubMed Web of Science ®Google Scholar