ZIPCO, a putative metal ion transporter, is crucial for Plasmodium liver-stage development

EMBO Molecular Medicine

Volumn 6, Issue 11, 2014, Pages 1387-1397

  Sahu, Tejram ^a,b   Boisson, Bertrand ^a,c   Lacroix, Céline ^a,d   Bischoff, Emmanuel ^a   Richier, Quentin ^a   Formaglio, Pauline ^a   Thiberge, Sabine ^a   Dobrescu, Irina ^a   Ménard, Robert ^a   Baldacci, Patricia ^a  

^a INSTITUT PASTEUR   (France)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

Author keywords

Iron; Liver stage; Plasmodium; Transporter; ZIP

Indexed keywords

CARRIER PROTEIN; IRON; METAL ION; METALLOPROTEIN; UNCLASSIFIED DRUG; ZINC; ZIP DOMAIN CONTAINING PROTEIN; ION;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; FEMALE; GENE INACTIVATION; HEPG2 CELL LINE; HUMAN; HUMAN CELL; ION TRANSPORT; IRON DEPLETION; IRON METABOLISM; IRON TRANSPORT; LIVER DEVELOPMENT; MALE; MINERAL SUPPLEMENTATION; MOSQUITO; NONHUMAN; PLASMODIUM (LIFE CYCLE STAGE); PLASMODIUM BERGHEI; PROTEIN TRANSPORT; RAT; ZINC METABOLISM; AMINO ACID SEQUENCE; ANIMAL; ANOPHELES; C57BL MOUSE; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; LIVER CELL; MALARIA; METABOLISM; MOLECULAR GENETICS; MOUSE; PARASITOLOGY; PHYLOGENY; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES; FEMALE; GENE KNOCKOUT TECHNIQUES; HEP G2 CELLS; HEPATOCYTES; HUMANS; IONS; IRON; LIVER; MALARIA; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMODIUM BERGHEI; SEQUENCE HOMOLOGY, AMINO ACID; ZINC;

EID: 84910629448     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201403868     Document Type: Article

References (49)

1. Boisson B, Lacroix C, Bischoff E, Gueirard P, Bargieri DY, Franke-Fayard B, Janse CJ, Menard R, Baldacci P (2011) The novel putative transporter NPT1 plays a critical role in early stages of Plasmodium berghei sexual development. Mol Microbiol 81: 1343-1357
2. Carey AF, Menard R, Bargieri DY (2013) Scoring sporozoite motility. Methods Mol Biol 932: 371-383
3. Cassat JE, Skaar EP (2013) Iron in infection and immunity. Cell Host Microbe 13: 509-519
4. Crouch ML, Castor M, Karlinsey JE, Kalhorn T, Fang FC (2008) Biosynthesis and IroC-dependent export of the siderophore salmochelin are essential for virulence of Salmonella enterica serovar Typhimurium. Mol Microbiol 67: 971-983
5. Drakesmith H, Prentice AM (2012) Hepcidin and the iron-infection axis. Science 338: 768-772
6. Eide DJ (2006) Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 1763: 711-722
7. Eng BH, Guerinot ML, Eide D, Saier MH Jr (1998) Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J Membr Biol 166: 1-7
8. Fisher RA (1932) Statistical Methods for Research Workers, 4th edn. London: Oliver and Boyd
9. Fritsch G, Treumer J, Spira DT, Jung A (1985) Plasmodium vinckei: suppression of mouse infections with desferrioxamine B. Exp Parasitol 60: 171-174
10. Ganz T (2011) Hepcidin and iron regulation, 10 years later. Blood 117: 4425-4433
11. Gara SN, Madaki AJ, Thacher TD (2010) A comparison of iron and folate with folate alone in hematologic recovery of children treated for acute malaria. Am J Trop Med Hyg 83: 843-847
12. Giovannini D, Spath S, Lacroix C, Perazzi A, Bargieri D, Lagal V, Lebugle C, Combe A, Thiberge S, Baldacci P et al (2011) Independent roles of apical membrane antigen 1 and rhoptry neck proteins during host cell invasion by apicomplexa. Cell Host Microbe 10: 591-602
13. Gordeuk V, Thuma P, Brittenham G, McLaren C, Parry D, Backenstose A, Biemba G, Msiska R, Holmes L, McKinley E et al (1992) Effect of iron chelation therapy on recovery from deep coma in children with cerebral malaria. New Engl J Med 327: 1473-1477
14. Graewe S, Rankin KE, Lehmann C, Deschermeier C, Hecht L, Froehlke U, Stanway RR, Heussler V (2011) Hostile takeover by Plasmodium: reorganization of parasite and host cell membranes during liver stage egress. PLoS Pathog 7: e1002224
15. Graewe S, Stanway RR, Rennenberg A, Heussler VT (2012) Chronicle of a death foretold: Plasmodium liver stage parasites decide on the fate of the host cell. FEMS Microbiol Rev 36: 111-130
16. Guerinot ML (2000) The ZIP family of metal transporters. Biochim Biophys Acta 1465: 190-198
17. Hershko C, Gordeuk VR, Thuma PE, Theanacho EN, Spira DT, Hider RC, Peto TE, Brittenham GM (1992) The antimalarial effect of iron chelators: studies in animal models and in humans with mild falciparum malaria. J Inorg Biochem 47: 267-277
18. Huynh C, Sacks DL, Andrews NW (2006) A Leishmania amazonensis ZIP family iron transporter is essential for parasite replication within macrophage phagolysosomes. J Exp Med 203: 2363-2375
19. Huynh C, Andrews NW (2008) Iron acquisition within host cells and the pathogenicity of Leishmania. Cell Microbiol 10: 293-300
20. Ishino T, Boisson B, Orito Y, Lacroix C, Bischoff E, Loussert C, Janse C, Menard R, Yuda M, Baldacci P (2009) LISP1 is important for the egress of Plasmodium berghei parasites from liver cells. Cell Microbiol 11: 1329-1339
21. Jacques I, Andrews NW, Huynh C (2010) Functional characterization of LIT1, the Leishmania amazonensis ferrous iron transporter. Mol Biochem Parasitol 170: 28-36
22. Janse CJ, Franke-Fayard B, Waters AP (2006a) Selection by flow-sorting of genetically transformed, GFP-expressing blood stages of the rodent malaria parasite, Plasmodium berghei. Nat Protoc 1: 614-623
23. Janse CJ, Franke-Fayard B, Mair GR, Ramesar J, Thiel C, Engelmann S, Matuschewski K, van Gemert GJ, Sauerwein RW, Waters AP (2006b) High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Mol Biochem Parasitol 145: 60-70
24. Kabyemela ER, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE (2008) Decreased susceptibility to Plasmodium falciparum infection in pregnant women with iron deficiency. J Infect Dis 198: 163-166
25. Kambe T, Yamaguchi-Iwai Y, Sasaki R, Nagao M (2004) Overview of mammalian zinc transporters. Cell Mol Life Sci 61: 49-68
26. de Koning-Ward TF, O'Donnell RA, Drew DR, Thomson R, Speed TP, Crabb BS (2003) A new rodent model to assess blood stage immunity to the Plasmodium falciparum antigen merozoite surface protein 119 reveals a protective role for invasion inhibitory antibodies. J Exp Med 198: 869-875
27. Lacroix C, Giovannini D, Combe A, Bargieri DY, Spath S, Panchal D, Tawk L, Thiberge S, Carvalho TG, Barale JC et al (2011) FLP/FRT-mediated conditional mutagenesis in pre-erythrocytic stages of Plasmodium berghei. Nat Protoc 6: 1412-1428
28. Liuzzi JP, Cousins RJ (2004) Mammalian zinc transporters. Annu Rev Nutr 24: 151-172
29. Marvin RG, Wolford JL, Kidd MJ, Murphy S, Ward J, Que EL, Mayer ML, Penner-Hahn JE, Haldar K, O'Halloran TV (2012) Fluxes in "free" and total zinc are essential for progression of intraerythrocytic stages of Plasmodium falciparum. Chem Biol 19: 731-741
30. Murray MJ, Murray AB, Murray MB, Murray CJ (1978) The adverse effect of iron repletion on the course of certain infections. Br Med J 2: 1113-1115
31. Pollack S, Rossan RN, Davidson DE, Escajadillo A (1987) Desferrioxamine suppresses Plasmodium falciparum in Aotus monkeys. Proc Soc Exp Biol Med 184: 162-164
32. Portugal S, Carret C, Recker M, Armitage AE, Goncalves LA, Epiphanio S, Sullivan D, Roy C, Newbold CI, Drakesmith H et al (2011) Host-mediated regulation of superinfection in malaria. Nat Med 17: 732-737
33. Prentice AM, Ghattas H, Doherty C, Cox SE (2007) Iron metabolism and malaria. Food Nutr Bull 28: S524-S539
34. Prentice AM (2011) Hepcidin and iron-mediated resistance to malaria. EMBO Mol Med 3: 620-622
35. R Development Core team. (2011) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing
36. Raventos-Suarez C, Pollack S, Nagel RL (1982) Plasmodium falciparum: inhibition of in vitro growth by desferrioxamine. Am J Trop Med Hyg 31: 919-922
37. Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci USA 97: 12356-12360
38. Sanvisens N, Bano MC, Huang M, Puig S (2011) Regulation of ribonucleotide reductase in response to iron deficiency. Mol Cell 44: 759-769
39. Sazawal S, Black RE, Ramsan M, Chwaya HM, Stoltzfus RJ, Dutta A, Dhingra U, Kabole I, Deb S, Othman MK et al (2006) Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomised, placebo-controlled trial. Lancet 367: 133-143
40. Schaible UE, Kaufmann SH (2004) Iron and microbial infection. Nat Rev Microbiol 2: 946-953
41. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675
42. Schrettl M, Bignell E, Kragl C, Joechl C, Rogers T, Arst HN Jr, Haynes K, Haas H (2004) Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J Exp Med 200: 1213-1219
43. Seifert M, Nairz M, Schroll A, Schrettl M, Haas H, Weiss G (2008) Effects of the Aspergillus fumigatus siderophore systems on the regulation of macrophage immune effector pathways and iron homeostasis. Immunobiology 213: 767-778
44. Stahel E, Mazier D, Guillouzo A, Miltgen F, Landau I, Mellouk S, Beaudoin RL, Langlois P, Gentilini M (1988) Iron chelators: in vitro inhibitory effect on the liver stage of rodent and human malaria. Am J Trop Med Hyg 39: 236-240
45. 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
46. Thiberge S, Blazquez S, Baldacci P, Renaud O, Shorte S, Menard R, Amino R (2007) In vivo imaging of malaria parasites in the murine liver. Nat Protoc 2: 1811-1818
47. Weinberg ED, Moon J (2009) Malaria and iron: history and review. Drug Metab Rev 41: 644-662
48. Wu Y, Brosh RM Jr (2012) DNA helicase and helicase-nuclease enzymes with a conserved iron-sulfur cluster. Nucleic Acids Res 40: 4247-4260
49. Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig V, Aikawa M (1980) Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207: 71-73