Overexpression of Plasmodium berghei ATG8 by liver forms leads to cumulative defects in organelle dynamics and to generation of noninfectious merozoites

mBio

Volumn 7, Issue 3, 2016, Pages

  Voss, Christiane ^a   Ehrenman, Karen ^a   Mlambo, Godfree ^a   Mishra, Satish ^a,b   Kumar, Kota Arun ^c   Sacci, John B ^d   Sinnis, Photini ^a   Coppens, Isabelle ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b CENTRAL DRUG RESEARCH INSTITUTE   (India)

^c UNIVERSITY OF HYDERABAD   (India)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL CARRIER PROTEIN; ATG8 PROTEIN; GOLGI REASSEMBLY AND STACKING PROTEIN; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG; VACUOLAR PROTEIN SORTING 4; AUTOPHAGY RELATED PROTEIN 8 FAMILY; MEMBRANE PROTEIN;

3' UNTRANSLATED REGION; AMPHISOME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APICOPLAST; ARTICLE; AUTOPHAGOSOME; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; HEPATITIS; HUMAN; HUMAN CELL; LIVER CELL; MEROZOITE; MICRONEME; MOUSE; NONHUMAN; PARASITE CLEARANCE; PARASITE DEVELOPMENT; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; ULTRASTRUCTURE; ANIMAL; AUTOPHAGY; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; MALARIA; METABOLISM; MUTATION; PARASITOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ACYL CARRIER PROTEIN; ANIMALS; APICOPLASTS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 8 FAMILY; HEPATOCYTES; HUMANS; LIVER; MALARIA; MEMBRANE PROTEINS; MEROZOITES; MICE, TRANSGENIC; MUTATION; ORGANELLES; PLASMODIUM BERGHEI; PROTOZOAN PROTEINS;

EID: 84979086771     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00682-16     Document Type: Article

References (91)

1. Ejigiri I, Sinnis P. 2009. Plasmodium sporozoite-host interactions from the dermis to the hepatocyte. Curr Opin Microbiol 12: 401-407. http:// dx.doi.org/10.1016/j.mib.2009.06.006.
2. Kaushansky A, Kappe SH. 2015. Selection and refinement: the malaria parasite’s infection and exploitation of host hepatocytes. Curr Opin Microbiol 26: 71-78. http://dx.doi.org/10.1016/j.mib.2015.05.013.
3. Jayabalasingham B, Bano N, Coppens I. 2010. Metamorphosis of the malaria parasite in the liver is associated with organelle clearance. Cell Res 20: 1043-1059. http://dx.doi.org/10.1038/cr.2010.88.
4. Zaffagnini G, Martens S. 2016. Mechanisms of selective autophagy. J Mol Biol 428: 1714-1724. http://dx.doi.org/10.1016/j.jmb.2016.02.004.
5. Coppens I. 2011. Metamorphoses of malaria: the role of autophagy in parasite differentiation. Essays Biochem 51: 127-136. http://dx.doi.org/10.1042/bse0510127.
6. Duszenko M, Ginger ML, Brennand A, Gualdrón-López M, Colombo MI, Coombs GH, Coppens I, Jayabalasingham B, Langsley G, de Castro SL, Menna-Barreto R, Mottram JC, Navarro M, Rigden DJ, Romano PS, Stoka V, Turk B, Michels PA. 2011. Autophagy in protists. Autophagy 7: 127-158. http://dx.doi.org/10.4161/auto.7.2.13310.
7. Brennand A, Gualdrón-López M, Coppens I, Rigden DJ, Ginger ML, Michels PA. 2011. Autophagy in parasitic protists: unique features and drug targets. Mol Biochem Parasitol 177: 83-99. http://dx.doi.org/10.1016/j.molbiopara.2011.02.003.
8. Nakatogawa H, Ichimura Y, Ohsumi Y. 2007. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130: 165-178. http://dx.doi.org/10.1016/ j.cell.2007.05.021.
9. Cervantes S, Bunnik EM, Saraf A, Conner CM, Escalante A, Sardiu ME, Ponts N, Prudhomme J, Florens L, Le Roch KG. 2014. The multifunctional autophagy pathway in the human malaria parasite, Plasmodium falciparum. Autophagy 10: 80-92. http://dx.doi.org/10.4161/auto.26743.
10. Jayabalasingham B, Voss C, Ehrenman K, Romano JD, Smith ME, Fidock DA, Bosch J, Coppens I. 2014. Characterization of the ATG8-conjugation system in 2 Plasmodium species with special focus on the liver stage: possible linkage between the apicoplastic and autophagic systems? Autophagy 10: 269-284. http://dx.doi.org/10.4161/auto.27166.
11. Eickel N, Kaiser G, Prado M, Burda PC, Roelli M, Stanway RR, Heussler VT. 2013. Features of autophagic cell death in Plasmodium liverstage parasites. Autophagy 9: 568-580. http://dx.doi.org/10.4161/ auto.23689.
12. Tawk L, Chicanne G, Dubremetz JF, Richard V, Payrastre B, Vial HJ, Roy C, Wengelnik K. 2010. Phosphatidylinositol 3-phosphate, an essential lipid in Plasmodium, localizes to the food vacuole membrane and the apicoplast. Eukaryot Cell 9: 1519-1530. http://dx.doi.org/10.1128/ EC.00124-10.
13. Raiborg C, Schink KO, Stenmark H. 2013. Class III phosphatidylinositol 3-kinase and its catalytic product PtdIns3P in regulation of endocytic membrane traffic. FEBS J 280: 2730-2742. http://dx.doi.org/10.1111/ febs.12116.
14. Tooze SA, Yoshimori T. 2010. The origin of the autophagosomal membrane. Nat Cell Biol 12: 831-835. http://dx.doi.org/10.1038/ncb0910-831.
15. Militello RD, Colombo MI. 2011. A membrane is born: origin of the autophagosomal compartment. Curr Mol Med 11: 197-203. http:// dx.doi.org/10.2174/156652411795243441.
16. Rubinsztein DC, Shpilka T, Elazar Z. 2012. Mechanisms of autophagosome biogenesis. Curr Biol 22: R29-R34. http://dx.doi.org/10.1016/ j.cub.2011.11.034.
17. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T. 2004. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 117: 2805-2812. http://dx.doi.org/10.1242/jcs.01131.
18. Lévêque MF, Berry L, Cipriano MJ, Nguyen HM, Striepen B, Besteiro S. 2015. Autophagy-related protein ATG8 has a noncanonical function for apicoplast inheritance in Toxoplasma gondii. mBio 6: e01446-15. http:// dx.doi.org/10.1128/mBio.01446-15.
19. Sacci JB, Jr, Alam U, Douglas D, Lewis J, Tyrrell DL, Azad AF, Kneteman NM. 2006. Plasmodium falciparum infection and exoerythrocytic development in mice with chimeric human livers. Int J Parasitol 36: 353-360. http://dx.doi.org/10.1016/j.ijpara.2005.10.014.
20. Sattabongkot J, Yimamnuaychoke N, Leelaudomlipi S, Rasameesoraj M, Jenwithisuk R, Coleman RE, Udomsangpetch R, Cui L, Brewer TG. 2006. Establishment of a human hepatocyte line that supports in vitro development of the exo-erythrocytic stages of the malaria parasites Plasmodium falciparum and P. vivax. Am J Trop Med Hyg 74: 708-715.
21. Stanway RR, Witt T, Zobiak B, Aepfelbacher M, Heussler VT. 2009. GFP-targeting allows visualization of the apicoplast throughout the life cycle of live malaria parasites. Biol Cell 101: 415-430. http://dx.doi.org/10.1042/BC20080202.
22. Jahreiss L, Menzies FM, Rubinsztein DC. 2008. The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic 9: 574-587. http://dx.doi.org/10.1111/j.1600-0854.2008.00701.x.
23. Ravikumar B, Futter M, Jahreiss L, Korolchuk VI, Lichtenberg M, Luo S, Massey DCO, Menzies FM, Narayanan U, Renna M, Jimenez-Sanchez M, Sarkar S, Underwood B, Winslow A, Rubinsztein DC. 2009. Mammalian macroautophagy at a glance. J Cell Sci 122: 1707-1711. http:// dx.doi.org/10.1242/jcs.031773.
24. Koga H, Kaushik S, Cuervo AM. 2010. Altered lipid content inhibits autophagic vesicular fusion. FASEB J 24: 3052-3065. http://dx.doi.org/10.1096/fj.09-144519.
25. Mehrpour M, Esclatine A, Beau I, Codogno P. 2010. Overview of macroautophagy regulation in mammalian cells. Cell Res 20: 748-762. http:// dx.doi.org/10.1038/cr.2010.82.
26. Fader CM, Colombo MI. 2009. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ 16: 70-78. http://dx.doi.org/10.1038/cdd.2008.168.
27. Duran JM, Anjard C, Stefan C, Loomis WF, Malhotra V. 2010. Unconventional secretion of Acb1 is mediated by autophagosomes. J Cell Biol 188: 527-536. http://dx.doi.org/10.1083/jcb.200911154.
28. Cabral M, Anjard C, Malhotra V, Loomis WF, Kuspa A. 2010. Unconventional secretion of AcbA in Dictyostelium discoideum through a vesicular intermediate. Eukaryot Cell 9: 1009-1017. http://dx.doi.org/10.1128/ EC.00337-09.
29. Ushio H, Ueno T, Kojima Y, Komatsu M, Tanaka S, Yamamoto A, Ichimura Y, Ezaki J, Nishida K, Komazawa-Sakon S, Niyonsaba F, Ishii T, Yanagawa T, Kominami E, Ogawa H, Okumura K, Nakano H. 2011. Crucial role for autophagy in degranulation of mast cells. J Allergy Clin Immunol 127: 1267-1276. http://dx.doi.org/10.1016/j.jaci.2010.12.1078.
30. Manjithaya R, Subramani S. 2011. Autophagy: a broad role in unconventional protein secretion? Trends Cell Biol 21: 67-73. http://dx.doi.org/10.1016/j.tcb.2010.09.009.
31. Chua CE, Lim YS, Lee MG, Tang BL. 2012. Non-classical membrane trafficking processes galore. J Cell Physiol 227: 3722-3730. http:// dx.doi.org/10.1002/jcp.24082.
32. Betin VM, Singleton BK, Parsons SF, Anstee DJ, Lane JD. 2013. Autophagy facilitates organelle clearance during differentiation of human erythroblasts: evidence for a role for ATG4 paralogs during autophagosome maturation. Autophagy 9: 881-893. http://dx.doi.org/10.4161/ auto.24172.
33. Giuliani F, Grieve A, Rabouille C. 2011. Unconventional secretion: a stress on GRASP. Curr Opin Cell Biol 23: 498-504. http://dx.doi.org/10.1016/j.ceb.2011.04.005.
34. Vinke FP, Grieve AG, Rabouille C. 2011. The multiple facets of the Golgi reassembly stacking proteins. Biochem J 433: 423-433. http://dx.doi.org/10.1042/BJ20101540.
35. Kinseth MA, Anjard C, Fuller D, Guizzunti G, Loomis WF, Malhotra V. 2007. The Golgi-associated protein GRASP is required for unconventional protein secretion during development. Cell 130: 524-534. http:// dx.doi.org/10.1016/j.cell.2007.06.029.
36. Manjithaya R, Anjard C, Loomis WF, Subramani S. 2010. Unconventional secretion of Pichia pastoris Acb1 is dependent on GRASP protein, peroxisomal functions, and autophagosome formation. J Cell Biol 188: 537-546. http://dx.doi.org/10.1083/jcb.200911149.
37. Struck NS, Herrmann S, Langer C, Krueger A, Foth BJ, Engelberg K, Cabrera AL, Haase S, Treeck M, Marti M, Cowman AF, Spielmann T, Gilberger TW. 2008. Plasmodium falciparum possesses two GRASP proteins that are differentially targeted to the Golgi complex via a higher-and lower-eukaryote-like mechanism. J Cell Sci 121: 2123-2129. http:// dx.doi.org/10.1242/jcs.021154.
38. Hanson PI, Cashikar A. 2012. Multivesicular body morphogenesis. Annu Rev Cell Dev Biol 28: 337-362. http://dx.doi.org/10.1146/annurev-cellbio-092910-154152.
39. Yang M, Coppens I, Wormsley S, Baevova P, Hoppe HC, Joiner KA. 2004. The Plasmodium falciparum Vps4 homolog mediates multivesicular body formation. J Cell Sci 117: 3831-3838. http://dx.doi.org/10.1242/ jcs.01237.
40. Branda CS, Dymecki SM. 2004. Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev Cell 6: 7-28. http://dx.doi.org/10.1016/S1534-5807(03)00399-X.
41. Combe A, Giovannini D, Carvalho TG, Spath S, Boisson B, Loussert C, Thiberge S, Lacroix C, Gueirard P, Ménard R. 2009. Clonal conditional mutagenesis in malaria parasites. Cell Host Microbe 5: 386-396. http:// dx.doi.org/10.1016/j.chom.2009.03.008.
42. Falae A, Combe A, Amaladoss A, Carvalho T, Menard R, Bhanot P. 2010. Role of Plasmodium berghei cGMP-dependent protein kinase in late liver stage development. J Biol Chem 285: 3282-3288. http:// dx.doi.org/10.1074/jbc.M109.070367.
43. Panneerselvam P, Bawankar P, Kulkarni S, Patankar S. 2011. In silico prediction of evolutionarily conserved GC-rich elements associated with antigenic proteins of Plasmodium falciparum. Evol Bioinform Online 7: 235-255. http://dx.doi.org/10.4137/EBO.S8162.
44. Waller KL, Muhle RA, Ursos LM, Horrocks P, Verdier-Pinard D, Sidhu AB, Fujioka H, Roepe PD, Fidock DA. 2003. Chloroquine resistance modulated in vitro by expression levels of the Plasmodium falciparum chloroquine resistance transporter. J Biol Chem 278: 33593-33601. http:// dx.doi.org/10.1074/jbc.M302215200.
45. Sebastian S, Brochet M, Collins MO, Schwach F, Jones ML, Goulding D, Rayner JC, Choudhary JS, Billker O. 2012. A Plasmodium calciumdependent protein kinase controls zygote development and transmission by translationally activating repressed mRNAs. Cell Host Microbe 12: 9-19. http://dx.doi.org/10.1016/j.chom.2012.05.014.
46. Klein RJ, Misulovin Z, Eddy SR. 2002. Noncoding RNA genes identified in AT-rich hyperthermophiles. Proc Natl Acad Sci U S A 99: 7542-7547. http://dx.doi.org/10.1073/pnas.112063799.
47. Militello KT, Dodge M, Bethke L, Wirth DF. 2004. Identification of regulatory elements in the Plasmodium falciparum genome. Mol Biochem Parasitol 134: 75-88. http://dx.doi.org/10.1016/j.molbiopara.2003.11.004.
48. Sturm A, Graewe S, Franke-Fayard B, Retzlaff S, Bolte S, Roppenser B, Aepfelbacher M, Janse C, Heussler V. 2009. Alteration of the parasite plasma membrane and the parasitophorous vacuole membrane during exo-erythrocytic development of malaria parasites. Protist 160: 51-63. http://dx.doi.org/10.1016/j.protis.2008.08.002.
49. Baer K, Klotz C, Kappe SH, Schnieder T, Frevert U. 2007. Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLoS Pathog 3: e171. http://dx.doi.org/10.1371/journal.ppat.0030171.
50. Cowman AF, Crabb BS. 2006. Invasion of red blood cells by malaria parasites. Cell 124: 755-766. http://dx.doi.org/10.1016/j.cell.2006.02.006.
51. Garcia JE, Puentes A, Patarroyo ME, Puentes A, Patarroyo ME. 2006. Developmental biology of sporozoite-host interactions in Plasmodium falciparum malaria: implications for vaccine design. Clin Microbiol Rev 19: 686-707. http://dx.doi.org/10.1128/CMR.00063-05.
52. Nyalwidhe J, Lingelbach K. 2006. Proteases and chaperones are the most abundant proteins in the parasitophorous vacuole of Plasmodium falciparum-infected erythrocytes. Proteomics 6: 1563-1573. http:// dx.doi.org/10.1002/pmic.200500379.
53. Fader CM, Colombo MI. 2006. Multivesicular bodies and autophagy in erythrocyte maturation. Autophagy 2: 122-125. http://dx.doi.org/10.4161/auto.2.2.2350.
54. Betin VM, Singleton BK, Parsons SF, Anstee DJ, Lane JD. 2013. Autophagy facilitates organelle clearance during differentiation of human erythroblasts: evidence for a role for ATG4 paralogs during autophagosome maturation. Autophagy 9: 881-893. http://dx.doi.org/10.4161/ auto.24172.
55. Zhang J, Randall MS, Loyd MR, Dorsey FC, Kundu M, Cleveland JL, Ney PA. 2009. Mitochondrial clearance is regulated by Atg7-dependent and-independent mechanisms during reticulocyte maturation. Blood 114: 157-164. http://dx.doi.org/10.1182/blood-2008-04-151639.
56. Schweers RL, Zhang J, Randall MS, Loyd MR, Li W, Dorsey FC, Kundu M, Opferman JT, Cleveland JL, Miller JL, Ney PA. 2007. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci U S A 104: 19500-19505. http://dx.doi.org/10.1073/ pnas.0708818104.
57. Mariño G, Uría JA, Puente XS, Quesada V, Bordallo J, López-Otín C. 2003. Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J Biol Chem 278: 3671-3678. http://dx.doi.org/10.1074/jbc.M208247200.
58. Fujita N, Hayashi-Nishino M, Fukumoto H, Omori H, Yamamoto A, Noda T, Yoshimori T. 2008. An Atg4B mutant hampers the lipidation of LC3 paralogues and causes defects in autophagosome closure. Mol Biol Cell 19: 4651-4659. http://dx.doi.org/10.1091/mbc.E08-03-0312.
59. Dupont N, Jiang S, Pilli M, Ornatowski W, Bhattacharya D, Deretic V. 2011. Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1_. EMBO J 30: 4701-4711. http://dx.doi.org/10.1038/ emboj.2011.398.
60. Loomis WF, Behrens MM, Williams ME, Anjard C. 2010. Pregnenolone sulfate and cortisol induce secretion of acyl-CoA-binding protein and its conversion into endozepines from astrocytes. J Biol Chem 285:-21359-21365. http://dx.doi.org/10.1074/jbc.M110.105858.
61. Ejlerskov P, Rasmussen I, Nielsen TT, Bergström AL, Tohyama Y, Jensen PH, Vilhardt F. 2013. Tubulin polymerization-promoting protein (TPPP/p25_) promotes unconventional secretion of_-synuclein through exophagy by impairing autophagosome-lysosome fusion. J Biol Chem 288: 17313-17335. http://dx.doi.org/10.1074/jbc.M112.401174.
62. Sirois I, Groleau J, Pallet N, Brassard N, Hamelin K, Londono I, Pshezhetsky AV, Bendayan M, Hébert MJ. 2012. Caspase activation regulates the extracellular export of autophagic vacuoles. Autophagy 8: 927-937. http://dx.doi.org/10.4161/auto.19768.
63. Pallet N, Sirois I, Bell C, Hanafi LA, Hamelin K, Dieudé M, Rondeau C, Thibault P, Desjardins M, Hebert MJ. 2013. A comprehensive characterization of membrane vesicles released by autophagic human endothelial cells. Proteomics 13: 1108-1120. http://dx.doi.org/10.1002/ pmic.201200531.
64. Jackson WT. 2015. Viruses and the autophagy pathway. Virology 479-480: 450-456. http://dx.doi.org/10.1016/j.virol.2015.03.042.
65. Tanida I, Sou YS, Ezaki J, Minematsu-Ikeguchi N, Ueno T, Kominami E. 2004. HsAtg4B/HsApg4B/autophagin-1 cleaves the carboxyl termini of three human Atg8 homologues and delipidates microtubule-associated protein light chain 3-and GABAA receptor-associated proteinphospholipid conjugates. J Biol Chem 279: 36268-36276. http:// dx.doi.org/10.1074/jbc.M401461200.
66. Opperdoes FR, Borst P. 1977. Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome. FEBS Lett 80: 360-364. http://dx.doi.org/10.1016/0014-5793(77)80476-6.
67. Van Grinsven KW, Van Den Abbeele J, Van den Bossche P, Van Hellemond JJ, Tielens AG. 2009. Adaptations in the glucose metabolism of procyclic Trypanosoma brucei isolates from tsetse flies and during differentiation of bloodstream forms. Eukaryot Cell 8: 1307-1311. http:// dx.doi.org/10.1128/EC.00091-09.
68. Brennand A, Rico E, Rigden DJ, Van Der Smissen P, Courtoy PJ, Michels PA. 2015. ATG24 Represses autophagy and differentiation and is essential for homeostasy of the flagellar pocket in Trypanosoma brucei. PLoS One 10: e0130365. http://dx.doi.org/10.1371/journal.pone.0130365.
69. Waller RF, Reed MB, Cowman AF, McFadden GI. 2000. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 19: 1794-1802. http://dx.doi.org/10.1093/emboj/19.8.1794.
70. Heiny SR, Pautz S, Recker M, Przyborski JM. 2014. Protein traffic to the Plasmodium falciparum apicoplast: evidence for a sorting branch point at the Golgi. Traffic 15: 1290-1304. http://dx.doi.org/10.1111/tra.12226.
71. Jia W, He YW. 2011. Temporal regulation of intracellular organelle homeostasis in T lymphocytes by autophagy. J Immunol 186: 5313-5322. http://dx.doi.org/10.4049/jimmunol.1002404.
72. Ralph SA, van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, Foth BJ, Tonkin CJ, Roos DS, McFadden GI. 2004. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2: 203-216. http://dx.doi.org/10.1038/ nrmicro843.
73. Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Türbachova I, Eberl M, Zeidler J, Lichtenthaler HK, Soldati D, Beck E. 1999. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285: 1573-1576. http:// dx.doi.org/10.1126/science.285.5433.1573.
74. Dahl EL, Rosenthal PJ. 2007. Multiple antibiotics exert delayed effects against the Plasmodium falciparum apicoplast. Antimicrob Agents Chemother 51: 3485-3490. http://dx.doi.org/10.1128/AAC.00527-07.
75. Fichera ME, Roos DS. 1997. A plastid organelle as a drug target in apicomplexan parasites. Nature 390: 407-409. http://dx.doi.org/10.1038/37132.
76. Yu M, Kumar TR, Nkrumah LJ, Coppi A, Retzlaff S, Li CD, Kelly BJ, Moura PA, Lakshmanan V, Freundlich JS, Valderramos JC, Vilcheze C, Siedner M, Tsai JH, Falkard B, Sidhu AB, Purcell LA, Gratraud P, Kremer L, Waters AP, Schiehser G, Jacobus DP, Janse CJ, Ager A, Jacobs WR, Jr, Sacchettini JC, Heussler V, Sinnis P, Fidock DA. 2008. The fatty acid biosynthesis enzyme FabI plays a key role in the development of liver-stage malarial parasites. Cell Host Microbe 4: 567-578. http://dx.doi.org/10.1016/j.chom.2008.11.001.
77. Vaughan AM, O’Neill MT, Tarun AS, Camargo N, Phuong TM, Aly AS, Cowman AF, Kappe SH. 2009. Type II fatty acid synthesis is essential only for malaria parasite late liver stage development. Cell Microbiol 11: 506-520. http://dx.doi.org/10.1111/j.1462-5822.2008.01270.x.
78. Pei Y, Tarun AS, Vaughan AM, Herman RW, Soliman JM, Erickson-Wayman A, Kappe SH. 2010. Plasmodium pyruvate dehydrogenase activity is only essential for the parasite’s progression from liver infection to blood infection. Mol Microbiol 75: 957-971. http://dx.doi.org/10.1111/ j.1365-2958.2009.07034.x.
79. Haussig JM, Matuschewski K, Kooij TW. 2011. Inactivation of a Plasmodium apicoplast protein attenuates formation of liver merozoites. Mol Microbiol 81: 1511-1525. http://dx.doi.org/10.1111/j.1365-2958.2011.07787.x.
80. Striepen B, Crawford MJ, Shaw MK, Tilney LG, Seeber F, Roos DS. 2000. The plastid of Toxoplasma gondii is divided by association with the centrosomes. J Cell Biol 151: 1423-1434. http://dx.doi.org/10.1083/jcb.151.7.1423.
81. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT. 2008. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182: 685-701. http://dx.doi.org/10.1083/jcb.200803137.
82. Dall’Armi C, Devereaux KA, Di Paolo G. 2013. The role of lipids in the control of autophagy. Curr Biol 23: R33-R45. http://dx.doi.org/10.1016/ j.cub.2012.10.041.
83. Vaid A, Ranjan R, Smythe WA, Hoppe HC, Sharma P. 2010. PfPI3K, a phosphatidylinositol-3 kinase from Plasmodium falciparum, is exported to the host erythrocyte and is involved in hemoglobin trafficking. Blood 115: 2500-2507. http://dx.doi.org/10.1182/blood-2009-08-238972.
84. Jiang P, Mizushima N. 2014. Autophagy and human diseases. Cell Res 24: 69-79. http://dx.doi.org/10.1038/cr.2013.161.
85. Goldberg DE, Slater AF, Cerami A, Henderson GB. 1990. Hemoglobin degradation in the malaria parasite Plasmodium falciparum: an ordered process in a unique organelle. Proc Natl Acad Sci U S A 87: 2931-2935. http://dx.doi.org/10.1073/pnas.87.8.2931.
86. Gaviria D, Paguio MF, Turnbull LB, Tan A, Siriwardana A, Ghosh D, Ferdig MT, Sinai AP, Roepe PD. 2013. A process similar to autophagy is associated with cytocidal chloroquine resistance in Plasmodium falciparum. PLoS One 8: e79059. http://dx.doi.org/10.1371/ journal.pone.0079059.
87. Tomlins AM, Ben-Rached F, Williams RA, Proto WR, Coppens I, Ruch U, Gilberger TW, Coombs GH, Mottram JC, Müller S, Langsley G. 2013. Plasmodium falciparum ATG8 implicated in both autophagy and apicoplast formation. Autophagy 9: 1540-1552. http://dx.doi.org/10.4161/auto.25832.
88. Struck NS, Herrmann S, Schmuck-Barkmann I, de Souza Dias S, Haase S, Cabrera AL, Treeck M, Bruns C, Langer C, Cowman AF, Marti M, Spielmann T, GilbergerTW. 2008. Spatial dissection of the cis-and trans-Golgi compartments in the malaria parasite Plasmodium falciparum. Mol Microbiol 67: 1320-1330. http://dx.doi.org/10.1111/j.1365-2958.2008.06125.x.
89. Kaiser K, Camargo N, Kappe SH. 2003. Transformation of sporozoites into early exoerythrocytic malaria parasites does not require host cells. J Exp Med 197: 1045-1050. http://dx.doi.org/10.1084/jem.20022100.
90. Janse CJ, Ramesar J, Waters AP. 2006. High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc 1: 346-356. http:// dx.doi.org/10.1038/nprot.2006.53.
91. Janse CJ, Franke-Fayard B, Waters AP. 2006. Selection by flow-sorting of genetically transformed, GFP-expressing blood stages of the rodent malaria parasite, Plasmodium berghei. Nat Protoc 1: 614-623. http:// dx.doi.org/10.1038/nprot.2006.88.