Host Reticulocytes Provide Metabolic Reservoirs That Can Be Exploited by Malaria Parasites

PLoS Pathogens

Volumn 11, Issue 6, 2015, Pages

  Srivastava, Anubhav ^a,b   Creek, Darren J ^a,b,c   Evans, Krystal J ^d   De Souza, David ^e   Schofield, Louis ^d,f   Müller, Sylke ^b   Barrett, Michael P ^a,b   McConville, Malcolm J ^e,g   Waters, Andrew P ^a,b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c MONASH UNIVERSITY   (Australia)

^d WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f JAMES COOK UNIVERSITY   (Australia)

^g UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBON METABOLISM; CELL INVASION; CELL PROLIFERATION; DISEASE TRANSMISSION; DOWN REGULATION; ERYTHROCYTE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LIQUID CHROMATOGRAPHY; MASS FRAGMENTOGRAPHY; MASS SPECTROMETRY; METABOLOMICS; MOUSE; NONHUMAN; PHENOTYPE; PLASMODIUM BERGHEI; PYRIMIDINE SYNTHESIS; RAT; RETICULOCYTE; SPECIES DIFFERENCE; UPREGULATION; ANIMAL; HOST PARASITE INTERACTION; MALARIA; METABOLISM; PARASITOLOGY; PHYSIOLOGY;

MUS; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; RODENTIA;

ANIMALS; ERYTHROCYTES; HOST-PARASITE INTERACTIONS; HUMANS; MALARIA; MICE; RATS; RETICULOCYTES;

EID: 84936791319     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004882     Document Type: Article

References (75)

1. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, et al. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1: E5. 12929205
2. Llinas M, del Portillo HA, (2005) Mining the malaria transcriptome. Trends Parasitol 21: 350–352. 15979411
3. Khan SM, Franke-Fayard B, Mair GR, Lasonder E, Janse CJ, et al. (2005) Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell 121: 675–687. 15935755
4. Hall N, Karras M, Raine JD, Carlton JM, Kooij TW, et al. (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307: 82–86. 15637271
5. Olszewski KL, Morrisey JM, Wilinski D, Burns JM, Vaidya AB, et al. (2009) Host-parasite interactions revealed by Plasmodium falciparum metabolomics. Cell Host Microbe 5: 191–199. doi: 10.1016/j.chom.2009.01.004 19218089
6. Kafsack BF, Llinas M, (2010) Eating at the table of another: metabolomics of host-parasite interactions. Cell Host Microbe 7: 90–99. doi: 10.1016/j.chom.2010.01.008 20159614
7. Macrae JI, Dixon MW, Dearnley MK, Chua HH, Chambers JM, et al. (2013) Mitochondrial metabolism of sexual and asexual blood stages of the malaria parasite Plasmodium falciparum. BMC Biol 11: 67. doi: 10.1186/1741-7007-11-67 23763941
8. Sana TR, Gordon DB, Fischer SM, Tichy SE, Kitagawa N, et al. (2013) Global mass spectrometry based metabolomics profiling of erythrocytes infected with Plasmodium falciparum. PLoS One 8: e60840. doi: 10.1371/journal.pone.0060840 23593322
9. Booden T, Hull RW, (1973) Nucleic acid precursor synthesis by Plasmodium lophurae parasitizing chicken erythrocytes. Exp Parasitol 34: 220–228. 4744840
10. Sherman IW, (1977) Amino acid metabolism and protein synthesis in malarial parasites. Bull World Health Organ 55: 265–276. 338183
11. Homewood CA, (1977) Carbohydrate metabolism of malarial parasites. Bull World Health Organ 55: 229–235. 338181
12. Oppenheim RD, Creek DJ, Macrae JI, Modrzynska KK, Pino P, et al. (2014) BCKDH: The Missing Link in Apicomplexan Mitochondrial Metabolism Is Required for Full Virulence of Toxoplasma gondii and Plasmodium berghei. PLoS Pathog 10: e1004263. doi: 10.1371/journal.ppat.1004263 25032958
13. Holz GG, Jr. (1977) Lipids and the malarial parasite. Bull World Health Organ 55: 237–248. 412602
14. Dechamps S, Shastri S, Wengelnik K, Vial HJ, (2010) Glycerophospholipid acquisition in Plasmodium—a puzzling assembly of biosynthetic pathways. Int J Parasitol 40: 1347–1365. doi: 10.1016/j.ijpara.2010.05.008 20600072
15. Barrett MP, (1997) The pentose phosphate pathway and parasitic protozoa. Parasitol Today 13: 11–16. 15275160
16. Hyde JE, (2007) Targeting purine and pyrimidine metabolism in human apicomplexan parasites. Curr Drug Targets 8: 31–47. 17266529
17. Macedo CS, Schwarz RT, Todeschini AR, Previato JO, Mendonca-Previato L, (2010) Overlooked post-translational modifications of proteins in Plasmodium falciparum: N- and O-glycosylation—a review. Mem Inst Oswaldo Cruz 105: 949–956. 21225189
18. Landfear SM, (2011) Nutrient transport and pathogenesis in selected parasitic protozoa. Eukaryot Cell 10: 483–493. doi: 10.1128/EC.00287-10 21216940
19. Martin RE, Ginsburg H, Kirk K, (2009) Membrane transport proteins of the malaria parasite. Mol Microbiol 74: 519–528. doi: 10.1111/j.1365-2958.2009.06863.x 19796339
20. Maier AG, Duraisingh MT, Reeder JC, Patel SS, Kazura JW, et al. (2003) Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat Med 9: 87–92. 12469115
21. Duraisingh MT, Maier AG, Triglia T, Cowman AF, (2003) Erythrocyte-binding antigen 175 mediates invasion in Plasmodium falciparum utilizing sialic acid-dependent and-independent pathways. Proc Natl Acad Sci U S A 100: 4796–4801. 12672957
22. Mayer DC, Cofie J, Jiang L, Hartl DL, Tracy E, et al. (2009) Glycophorin B is the erythrocyte receptor of Plasmodium falciparum erythrocyte-binding ligand, EBL-1. Proc Natl Acad Sci U S A 106: 5348–5352. doi: 10.1073/pnas.0900878106 19279206
23. Crosnier C, Bustamante LY, Bartholdson SJ, Bei AK, Theron M, et al. (2011) Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 480: 534–537. doi: 10.1038/nature10606 22080952
24. Tham WH, Healer J, Cowman AF, (2012) Erythrocyte and reticulocyte binding-like proteins of Plasmodium falciparum. Trends Parasitol 28: 23–30. doi: 10.1016/j.pt.2011.10.002 22178537
25. Harvey KL, Gilson PR, Crabb BS, (2012) A model for the progression of receptor-ligand interactions during erythrocyte invasion by Plasmodium falciparum. Int J Parasitol 42: 567–573. doi: 10.1016/j.ijpara.2012.02.011 22710063
26. Wright GJ, Rayner JC, (2014) Plasmodium falciparum erythrocyte invasion: combining function with immune evasion. PLoS Pathog 10: e1003943. doi: 10.1371/journal.ppat.1003943 24651270
27. Pasvol G, Weatherall DJ, Wilson RJ, (1980) The increased susceptibility of young red cells to invasion by the malarial parasite Plasmodium falciparum. Br J Haematol 45: 285–295. 7002199
28. Galinski MR, Medina CC, Ingravallo P, Barnwell JW, (1992) A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Cell 69: 1213–1226. 1617731
29. Barnwell JW, Nichols ME, Rubinstein P, (1989) In vitro evaluation of the role of the Duffy blood group in erythrocyte invasion by Plasmodium vivax. J Exp Med 169: 1795–1802. 2469769
30. Malleret B, Li A, Zhang R, Tan KS, Suwanarusk R, et al. (2014) Plasmodium vivax: restricted tropism and rapid remodelling of CD71 positive reticulocytes. Blood.
31. Cromer D, Evans KJ, Schofield L, Davenport MP, (2006) Preferential invasion of reticulocytes during late-stage Plasmodium berghei infection accounts for reduced circulating reticulocyte levels. Int J Parasitol 36: 1389–1397. 16979643
32. Janse CJ, Waters AP, (1995) Plasmodium berghei: the application of cultivation and purification techniques to molecular studies of malaria parasites. Parasitol Today 11: 138–143. 15275357
33. Chen K, Liu J, Heck S, Chasis JA, An X, et al. (2009) Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. Proc Natl Acad Sci U S A 106: 17413–17418. doi: 10.1073/pnas.0909296106 19805084
34. Gronowicz G, Swift H, Steck TL, (1984) Maturation of the reticulocyte in vitro. J Cell Sci 71: 177–197. 6097593
35. Liu J, Guo X, Mohandas N, Chasis JA, An X, (2010) Membrane remodeling during reticulocyte maturation. Blood 115: 2021–2027. doi: 10.1182/blood-2009-08-241182 20038785
36. Chapman RG, Hennessey MA, Waltersdorph AM, Huennekens FM, Gabrio BW, (1962) Erythrocyte metabolism. V. Levels of glycolytic enzymes and regulation of glycolysis. J Clin Invest 41: 1249–1256. 13878200
37. Stromme JH, Eldjarn L, (1962) The role of the pentose phosphate pathway in the reduction of methaemoglobin in human erythrocytes. Biochem J 84: 406–410. 13917855
38. Dajani RM, Orten JM, (1958) [A study of the citric acid cycle in erythrocytes]. J Biol Chem 231: 913–924. 13539026
39. Malleret B, Xu F, Mohandas N, Suwanarusk R, Chu C, et al. (2013) Significant biochemical, biophysical and metabolic diversity in circulating human cord blood reticulocytes. PLoS One 8: e76062. doi: 10.1371/journal.pone.0076062 24116088
40. Darghouth D, Koehl B, Madalinski G, Heilier JF, Bovee P, et al. (2011) Pathophysiology of sickle cell disease is mirrored by the red blood cell metabolome. Blood 117: e57–66. doi: 10.1182/blood-2010-07-299636 21135259
41. Douay L, Giarratana MC, (2009) Ex vivo generation of human red blood cells: a new advance in stem cell engineering. Methods Mol Biol 482: 127–140. doi: 10.1007/978-1-59745-060-7_8 19089353
42. Storm J, Sethia S, Blackburn GJ, Chokkathukalam A, Watson DG, et al. (2014) Phosphoenolpyruvate carboxylase identified as a key enzyme in erythrocytic Plasmodium falciparum carbon metabolism. PLoS Pathog 10: e1003876. doi: 10.1371/journal.ppat.1003876 24453970
43. Ginsburg H, (2006) Progress in in silico functional genomics: the malaria Metabolic Pathways database. Trends Parasitol 22: 238–240. 16707276
44. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498–511. 12368864
45. Valentine WN, Paglia DE, (1980) Erythrocyte disorders of purine and pyrimidine metabolism. Hemoglobin 4: 669–681. 6254919
46. Rebouche CJ, Paulson DJ, (1986) Carnitine metabolism and function in humans. Annu Rev Nutr 6: 41–66. 3524622
47. Bulusu V, Jayaraman V, Balaram H, (2011) Metabolic fate of fumarate, a side product of the purine salvage pathway in the intraerythrocytic stages of Plasmodium falciparum. J Biol Chem 286: 9236–9245. doi: 10.1074/jbc.M110.173328 21209090
48. Wrenger C, Muller IB, Schifferdecker AJ, Jain R, Jordanova R, et al. (2011) Specific inhibition of the aspartate aminotransferase of Plasmodium falciparum. J Mol Biol 405: 956–971. doi: 10.1016/j.jmb.2010.11.018 21087616
49. Hino A, Hirai M, Tanaka TQ, Watanabe Y, Matsuoka H, et al. (2012) Critical roles of the mitochondrial complex II in oocyst formation of rodent malaria parasite Plasmodium berghei. Journal of biochemistry 152: 259–268. doi: 10.1093/jb/mvs058 22628552
50. van Dijk MR, Janse CJ, Thompson J, Waters AP, Braks JA, et al. (2001) A central role for P48/45 in malaria parasite male gamete fertility. Cell 104: 153–164. 11163248
51. Cassera MB, Zhang Y, Hazleton KZ, Schramm VL, (2011) Purine and pyrimidine pathways as targets in Plasmodium falciparum. Curr Top Med Chem 11: 2103–2115. 21619511
52. Gujjar R, Marwaha A, El Mazouni F, White J, White KL, et al. (2009) Identification of a metabolically stable triazolopyrimidine-based dihydroorotate dehydrogenase inhibitor with antimalarial activity in mice. J Med Chem 52: 1864–1872. doi: 10.1021/jm801343r 19296651
53. Phillips MA, Gujjar R, Malmquist NA, White J, El Mazouni F, et al. (2008) Triazolopyrimidine-based dihydroorotate dehydrogenase inhibitors with potent and selective activity against the malaria parasite Plasmodium falciparum. J Med Chem 51: 3649–3653. doi: 10.1021/jm8001026 18522386
54. Rathod PK, Khatri A, Hubbert T, Milhous WK, (1989) Selective activity of 5-fluoroorotic acid against Plasmodium falciparum in vitro. Antimicrob Agents Chemother 33: 1090–1094. 2675756
55. Hekmat-Nejad M, Rathod PK, (1996) Kinetics of Plasmodium falciparum thymidylate synthase: interactions with high-affinity metabolites of 5-fluoroorotate and D1694. Antimicrob Agents Chemother 40: 1628–1632. 8807052
56. Pattanakitsakul SN, Ruenwongsa P, (1984) Characterization of thymidylate synthetase and dihydrofolate reductase from Plasmodium berghei. Int J Parasitol 14: 513–520. 6392123
57. Pasini EM, Kirkegaard M, Mortensen P, Lutz HU, Thomas AW, et al. (2006) In-depth analysis of the membrane and cytosolic proteome of red blood cells. Blood 108: 791–801. 16861337
58. Pasini EM, Kirkegaard M, Salerno D, Mortensen P, Mann M, et al. (2008) Deep coverage mouse red blood cell proteome: a first comparison with the human red blood cell. Mol Cell Proteomics 7: 1317–1330. doi: 10.1074/mcp.M700458-MCP200 18344233
59. Martin RE, Kirk K, (2007) Transport of the essential nutrient isoleucine in human erythrocytes infected with the malaria parasite Plasmodium falciparum. Blood 109: 2217–2224. 17047158
60. Berger LC, Wilson J, Wood P, Berger BJ, (2001) Methionine regeneration and aspartate aminotransferase in parasitic protozoa. J Bacteriol 183: 4421–4434. 11443076
61. Downie MJ, Kirk K, Mamoun CB, (2008) Purine salvage pathways in the intraerythrocytic malaria parasite Plasmodium falciparum. Eukaryot Cell 7: 1231–1237. doi: 10.1128/EC.00159-08 18567789
62. Cassera MB, Hazleton KZ, Riegelhaupt PM, Merino EF, Luo M, et al. (2008) Erythrocytic adenosine monophosphate as an alternative purine source in Plasmodium falciparum. J Biol Chem 283: 32889–32899. doi: 10.1074/jbc.M804497200 18799466
63. Quashie NB, Ranford-Cartwright LC, de Koning HP, (2010) Uptake of purines in Plasmodium falciparum-infected human erythrocytes is mostly mediated by the human equilibrative nucleoside transporter and the human facilitative nucleobase transporter. Malar J 9: 36. doi: 10.1186/1475-2875-9-36 20113503
64. Desai SA, Krogstad DJ, McCleskey EW, (1993) A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362: 643–646. 7681937
65. Parker MD, Hyde RJ, Yao SY, McRobert L, Cass CE, et al. (2000) Identification of a nucleoside/nucleobase transporter from Plasmodium falciparum, a novel target for anti-malarial chemotherapy. Biochem J 349: 67–75. 10861212
66. Frame IJ, Merino EF, Schramm VL, Cassera MB, Akabas MH, (2012) Malaria parasite type 4 equilibrative nucleoside transporters (ENT4) are purine transporters with distinct substrate specificity. Biochem J 446: 179–190. doi: 10.1042/BJ20112220 22670848
67. Majerus PW, Brauner MJ, Smith MB, Minnich V, (1971) Glutathione synthesis in human erythrocytes. II. Purification and properties of the enzymes of glutathione biosynthesis. The Journal of clinical investigation 50: 1637–1643. 5097571
68. Muller S, (2004) Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Molecular microbiology 53: 1291–1305. 15387810
69. Patzewitz EM, Wong EH, Muller S, (2012) Dissecting the role of glutathione biosynthesis in Plasmodium falciparum. Molecular microbiology 83: 304–318. doi: 10.1111/j.1365-2958.2011.07933.x 22151036
70. Pastrana-Mena R, Dinglasan RR, Franke-Fayard B, Vega-Rodriguez J, Fuentes-Caraballo M, et al. (2010) Glutathione reductase-null malaria parasites have normal blood stage growth but arrest during development in the mosquito. The Journal of biological chemistry 285: 27045–27056. doi: 10.1074/jbc.M110.122275 20573956
71. Vega-Rodriguez J, Franke-Fayard B, Dinglasan RR, Janse CJ, Pastrana-Mena R, et al. (2009) The glutathione biosynthetic pathway of Plasmodium is essential for mosquito transmission. PLoS pathogens 5: e1000302. doi: 10.1371/journal.ppat.1000302 19229315
72. Walliker D, Sanderson A, Yoeli M, Hargreaves BJ, (1976) A genetic investigation of virulence in a rodent malaria parasite. Parasitology 72: 183–194. 1264490
73. 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. 17406255
74. Sinha A, Hughes KR, Modrzynska KK, Otto TD, Pfander C, et al. (2014) A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature 507: 253–257. doi: 10.1038/nature12970 24572359
75. Ponzi M, Siden-Kiamos I, Bertuccini L, Curra C, Kroeze H, et al. (2009) Egress of Plasmodium berghei gametes from their host erythrocyte is mediated by the MDV-1/PEG3 protein. Cell Microbiol 11: 1272–1288. doi: 10.1111/j.1462-5822.2009.01331.x 19438517