Wolbachia interferes with ferritin expression and iron metabolism in insects

PLoS Pathogens

Volumn 5, Issue 10, 2009, Pages

  Kremer, Natacha ^a   Voronin, Denis ^b   Charif, Delphine ^a   Mavingui, Patrick ^b   Mollereau, Bertrand ^c   Vavre, Fabrice ^a  

^a UNIVERSITÉ DE LYON   (France)

^b University of Lyon   (France)

^c UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOFERRITIN; FERRITIN; IRON;

AEDES AEGYPTI; ANIMAL CELL; APOPTOSIS; ARTICLE; ASOBARA TABIDA; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BINDING AFFINITY; CELL PROTECTION; CONTROLLED STUDY; DIET; DROSOPHILA MELANOGASTER; DROSOPHILA SIMULANS; ENDOSYMBIONT; FEMALE; HOMEOSTASIS; HOST CELL; HOST PATHOGEN INTERACTION; INSECT DEVELOPMENT; INTRACELLULAR BACTERIUM; IRON METABOLISM; IRON OVERLOAD; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OXIDATIVE STRESS; PARASITISM; PATHOGENESIS; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYMBIONT; SYMBIOSIS; UPREGULATION; WASP; WOLBACHIA; AEDES; ANIMAL; CHROMOSOME MAP; CONFORMATION; DROSOPHILA; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; INSECT; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; RICKETTSIACEAE INFECTION;

AEDES AEGYPTI; ASOBARA TABIDA; BACTERIA (MICROORGANISMS); DROSOPHILA SIMULANS; HEXAPODA; WOLBACHIA;

AEDES; ANIMALS; BASE SEQUENCE; CHROMOSOME MAPPING; DROSOPHILA; FEMALE; FERRITINS; GENE EXPRESSION REGULATION; GENETIC LOCI; HOST-PARASITE INTERACTIONS; INSECTS; IRON; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RICKETTSIACEAE INFECTIONS; SYMBIOSIS; WASPS; WOLBACHIA;

EID: 73449107773     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000630     Document Type: Article

References (75)

1. De Bary H (1879) Die Erscheinung der Symbiose; Vortrag gadVDNuAzC, Trübner RJ, ed.
2. Azad AF, Beard CB (1998) Rickettsial pathogens and their arthropod vectors. Emerg Infect Dis 4: 179-186.
3. Goodrich-Blair H, Clarke DJ (2007) Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol Microbiol 64: 260-268.
4. Hentschel U, Steinert M, Hacker J (2000) Common molecular mechanisms of symbiosis and pathogenesis. Trends in Microbiology 8: 226-231.
5. Goebel W, Gross R (2001) Intracellular survival strategies of mutualistic and parasitic prokaryotes. Trends Microbiol 9: 267-273.
6. Silver AC, Kikuchi Y, Fadl AA, Sha J, Chopra AK, et al. (2007) Interaction between innate immune cells and a bacterial type III secretion system in mutualistic and pathogenic associations. Proc Natl Acad Sci U S A 104: 9481-9486.
7. Visick KL, Ruby EG (2006) Vibrio fischeri and its host: it takes two to tango. Curr Opin Microbiol 9: 632-638.
8. Anselme C, Perez-Brocal V, Vallier A, Vincent-Monegat C, Charif D, et al. (2008) Identification of the weevil immune genes and their expression in the bacteriome tissue. BMC Biol 6: 43.
9. Fortier AH, Leiby DA, Narayanan RB, Asafoadjei E, Crawford RM, et al. (1995) Growth of Francisella tularensis LVS in macrophages: the acidic intracellular compartment provides essential iron required for growth. Infect Immun 63: 1478-1483.
10. Buchmeier NA, Heffron F (1990) Induction of Salmonella stress proteins upon infection of macrophages. Science 248: 730-732.
11. Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42: 587-609.
12. Fenn K, Blaxter M (2004) Are filarial nematode Wolbachia obligate mutualist symbionts? Trends Ecol Evol 19: 163-166.
13. Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, et al. (2001) Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci U S A 98: 6247-6252.
14. Dedeine F, Bouletreau M, Vavre F (2005) Wolbachia requirement for oogenesis: occurrence within the genus Asobara (Hymenoptera, Braconidae) and evidence for intraspecific variation in A. tabida. Heredity 95: 394-400.
15. Pannebakker BA, Loppin B, Elemans CP, Humblot L, Vavre F (2007) Parasitic inhibition of cell death facilitates symbiosis. Proc Natl Acad Sci U S A 104: 213-215.
16. McCall K (2004) Eggs over easy: cell death in the Drosophila ovary. Dev Biol 274: 3-14.
17. Faherty CS, Maurelli AT (2008) Staying alive: bacterial inhibition of apoptosis during infection. Trends Microbiol 16: 173-180.
18. Arosio P, Levi S (2002) Ferritin, iron homeostasis, and oxidative damage. Free Radic Biol Med 33: 457-463.
19. Collins HL (2003) The role of iron in infections with intracellular bacteria. Immunol Lett 85: 193-195.
20. Foster J, Ganatra M, Kamal I, Ware J, Makarova K, et al. (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 3: e121. doi:10.1371/journal.pbio.0030121.
21. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317: 1756-1760.
22. Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I, et al. (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5: e1000368. doi:10.1371/journal.ppat.1000368.
23. Dunkov B, Georgieva T (2006) Insect iron binding proteins: Insights from the genomes. Insect Biochem Mol Biol 36: 300-309.
24. Pham DQ, Shaffer JJ, Chavez CA, Douglass PL (2003) Identification and mapping of the promoter for the gene encoding the ferritin heavy-chain homologue of the yellow fever mosquito Aedes aegypti. Insect Biochem Mol Biol 33: 51-62.
25. Pham DQ, Chavez CA (2005) The ferritin light-chain homologue promoter in Aedes aegypti. Insect Mol Biol 14: 263-270.
26. Missirlis F, Kosmidis S, Brody T, Mavrakis M, Holmberg S, et al. (2007) Homeostatic mechanisms for iron storage revealed by genetic manipulations and live imaging of Drosophila ferritin. Genetics 177: 89-100.
27. Geiser DL, Chavez CA, Flores-Munguia R, Winzerling JJ, Pham DQ (2003) Aedes aegypti ferritin. Eur J Biochem 270: 3667-3674.
28. Georgieva T, Dunkov BC, Harizanova N, Ralchev K, Law JH (1999) Iron availability dramatically alters the distribution of ferritin subunit messages in Drosophila melanogaster. Proc Natl Acad Sci U S A 96: 2716-2721.
29. Lind MI, Ekengren S, Melefors O, Soderhall K (1998) Drosophila ferritin mRNA: alternative RNA splicing regulates the presence of the iron-responsive element. FEBS Lett 436: 476-482.
30. Lawson DM, Treffry A, Artymiuk PJ, Harrison PM, Yewdall SJ, et al. (1989) Identification of the ferroxidase centre in ferritin. FEBS Lett 254: 207-210.
31. Theil EC (1994) Iron regulatory elements (IREs): a family of mRNA non-coding sequences. Biochem J 304 ( Pt 1): 1-11.
32. Strickler-Dinglasan PM, Guz N, Attardo G, Aksoy S (2006) Molecular characterization of iron binding proteins from Glossina morsitans morsitans (Diptera: Glossinidae). Insect Biochem Mol Biol 36: 921-933.
33. Hentze MW, Kuhn LC (1996) Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci U S A 93: 8175-8182.
34. Lind MI, Missirlis F, Melefors O, Uhrigshardt H, Kirby K, et al. (2006) Of two cytosolic aconitases expressed in Drosophila, only one functions as an ironregulatory protein. J Biol Chem 281: 18707-18714.
35. Surdej P, Richman L, Kuhn LC (2008) Differential translational regulation of IRE-containing mRNAs in Drosophila melanogaster by endogenous IRP and a constitutive human IRP1 mutant. Insect Biochem Mol Biol 38: 891-894.
36. Le Brun NE, Andrews SC, Guest JR, Harrison PM, Moore GR, et al. (1995) Identification of the ferroxidase centre of Escherichia coli bacterioferritin. Biochem J 312 ( Pt 2): 385-392.
37. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, et al. (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2: e69. doi:10.1371/journal.pbio.0020069.
38. Klasson L, Westberg J, Sapountzis P, Naslund K, Lutnaes Y, et al. (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci U S A 106: 5725-5730.
39. Klasson L, Walker T, Sebaihia M, Sanders MJ, Quail MA, et al. (2008) Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Mol Biol Evol 25: 1877-1887.
40. Al-Younes HM, Rudel T, Brinkmann V, Szczepek AJ, Meyer TF (2001) Low iron availability modulates the course of Chlamydia pneumoniae infection. Cell Microbiol 3: 427-437.
41. Schaible UE, Collins HL, Priem F, Kaufmann SH (2002) Correction of the iron overload defect in beta-2-microglobulin knockout mice by lactoferrin abolishes their increased susceptibility to tuberculosis. J Exp Med 196: 1507-1513.
42. Bubici C, Papa S, Dean K, Franzoso G (2006) Mutual cross-talk between reactive oxygen species and nuclear factor-kappa B: molecular basis and biological significance. Oncogene 25: 6731-6748.
43. Dunkov BC, Georgieva T, Yoshiga T, Hall M, Law JH (2002) Aedes aegypti ferritin heavy chain homologue: feeding of iron or blood influences message levels, lengths and subunit abundance. J Insect Sci 2: 7.
44. Iwasaki K, Mackenzie EL, Hailemariam K, Sakamoto K, Tsuji Y (2006) Heminmediated regulation of an antioxidant-responsive element of the human ferritin H gene and role of Ref-1 during erythroid differentiation of K562 cells. Mol Cell Biol 26: 2845-2856.
45. Hintze KJ, Theil EC (2005) DNA and mRNA elements with complementary responses to hemin, antioxidant inducers, and iron control ferritin-L expression. Proc Natl Acad Sci U S A 102: 15048-15052.
46. Schaible U, Kaufmann H (2004) Iron and microbial infection. Nature review microbiology 2: 946-953.
47. Bubici C, Papa S, Pham CG, Zazzeroni F, Franzoso G (2006) The NF-kappaBmediated control of ROS and JNK signaling. Histol Histopathol 21: 69-80.
48. Dunkov BC, Georgieva T (1999) Organization of the ferritin genes in Drosophila melanogaster. DNA Cell Biol 18: 937-944.
49. Beck G, Ellis TW, Habicht GS, Schluter SF, Marchalonis JJ (2002) Evolution of the acute phase response: iron release by echinoderm (Asterias forbesi) coelomocytes, and cloning of an echinoderm ferritin molecule. Dev Comp Immunol 26: 11-26.
50. Ong DS, Wang L, Zhu Y, Ho B, Ding JL (2005) The response of ferritin to LPS and acute phase of Pseudomonas infection. J Endotoxin Res 11: 267-280.
51. Li M, Saren G, Zhang S (2008) Identification and expression of a ferritin homolog in amphioxus Branchiostoma belcheri: evidence for its dual role in immune response and iron metabolism. Comp Biochem Physiol B Biochem Mol Biol 150: 263-270.
52. Rao AU, Carta LK, Lesuisse E, Hamza I (2005) Lack of heme synthesis in a free-living eukaryote. Proc Natl Acad Sci U S A 102: 4270-4275.
53. Hajdusek O, Sojka D, Kopacek P, Buresova V, Franta Z, et al. (2009) Knockdown of proteins involved in iron metabolism limits tick reproduction and development. Proc Natl Acad Sci U S A 106: 1033-1038.
54. Nichol H, Law JH, Winzerling JJ (2002) Iron metabolism in insects. Annu Rev Entomol 47: 535-559.
55. Raupach B, Kaufmann SH (2001) Immune responses to intracellular bacteria. Curr Opin Immunol 13: 417-428.
56. Häcker G, Fischer SF (2002) Bacterial anti-apoptotic activities. FEMS Microbiol Lett 211: 1-6.
57. Heussler VT, Kuenzi P, Rottenberg S (2001) Inhibition of apoptosis by intracellular protozoan parasites. Int J Parasitol 31: 1166-1176.
58. Brennan LJ, Keddie BA, Braig HR, Harris HL (2008) The endosymbiont Wolbachia pipientis induces the expression of host antioxidant proteins in an Aedes albopictus cell line. PLoS ONE 3: e2083. doi:10.1371/journal. pone.0002083.
59. Carlyon JA, Ryan D, Archer K, Fikrig E (2005) Effects of Anaplasma phagocytophilum on host cell ferritin mRNA and protein levels. Infect Immun 73: 7629-7636.
60. Mulenga A, Macaluso KR, Simser JA, Azad AF (2003) Dynamics of Rickettsiatick interactions: identification and characterization of differentially expressed mRNAs in uninfected and infected Dermacentor variabilis. Insect Mol Biol 12: 185-193.
61. Joshi S, Francis C, Silverman D, Sahni S (2003) Nuclear factor kappa B protects against host cell apoptosis during Rickettsia rickettsii infection by inhibiting activation of apical and effector caspases and maintaining mitochondrial integrity. Infect Immun 71: 4127-4136.
62. Ge Y, Yoshiie K, Kuribayashi F, Lin M, Rikihisa Y (2005) Anaplasma phagocytophilum inhibits human neutrophil apoptosis via upregulation of bfl-1, maintenance of mitochondrial membrane potential and prevention of caspase 3 activation. Cell Microbiol 7: 29-38.
63. Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou W, et al. (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Mol Biol 29: 153-160.
64. Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 16: 1711-1723.
65. Dedeine F, Vavre F, Shoemaker DD, Bouletreau M (2004) Intra-individual coexistence of a Wolbachia strain required for host oogenesis with two strains inducing cytoplasmic incompatibility in the wasp Asobara tabida. Evolution Int J Org 58: 2167-2174.
66. Kuno G (1983) Cultivation of mosquito cell lines in serum-free media and their effects on dengue virus replication. In Vitro 19: 707-713.
67. Dobson SL, Marsland EJ, Rattanadechakul W (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160: 1087-1094.
68. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int J Neural Syst 8: 581-599.
69. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
70. Noda H, Koizumi Y, Zhang Q, Deng K (2001) Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochem Mol Biol 31: 727-737.
71. Steckel M, Boutros M (2005) Rapid Development of Real-Time RT-PCR Assays Using Universal ProbeLibrary: Applications for Dissecting Signaling Pathways by RNA Interference. Biochemica 3: 17-19.
72. Geiser DL, Zhang D, Winzerling JJ (2006) Secreted ferritin: mosquito defense against iron overload? Insect Biochem Mol Biol 36: 177-187.
73. Pham DQ, Winzerling JJ, Dodson MS, Law JH (1999) Transcriptional control is relevant in the modulation of mosquito ferritin synthesis by iron. Eur J Biochem 266: 236-240.
74. Missirlis F, Holmberg S, Georgieva T, Dunkov BC, Rouault TA, et al. (2006) Characterization of mitochondrial ferritin in Drosophila. Proc Natl Acad Sci U S A 103: 5893-5898.
75. Sanchis A, Latorre A, Gonzalez-Candelas F, Michelena JM (2000) An 18S rDNA-based molecular phylogeny of aphidiinae (Hymenoptera: braconidae). Mol Phylogenet Evol 14: 180-194.