Plasmodium berghei induced priming in Anopheles albimanus independently of bacterial co-infection

Developmental and Comparative Immunology

Volumn 52, Issue 2, 2015, Pages 172-181

  Contreras Garduño, Jorge ^a,b   Rodríguez, María Carmen ^a   Hernández Martínez, Salvador ^a   Martínez Barnetche, Jesús ^a   Alvarado Delgado, Alejandro ^a   Izquierdo, Javier ^a   Herrera Ortiz, Antonia ^a   Moreno García, Miguel ^a   Velazquez Meza, Maria Elena ^a   Valverde, Veronica ^a   Argotte Ramos, Rocio ^a   Rodríguez, Mario Henry ^a   Lanz Mendoza, Humberto ^a  

^a INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^b UNIVERSITY OF GUANAJUATO   (Mexico)

Author keywords

Anopheles albimanus; Insect immune memory; Mosquito immunity; Plasmodium berghei

Indexed keywords

ATTACIN; BROXURIDINE; CECROPIN; GAMBICIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

ANOPHELES; ANOPHELES ALBIMANUS; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DNA SYNTHESIS; ENDOREDUPLICATION; GENE; GENETIC TRANSCRIPTION; HNT GENE; IMMUNE RESPONSE; MALE; MIDGUT; MITOSIS; MIXED INFECTION; MOUSE; NONHUMAN; PLASMODIUM BERGHEI; PRIORITY JOURNAL; ADAPTIVE IMMUNITY; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; DRUG EFFECTS; GASTROINTESTINAL TRACT; HOST PARASITE INTERACTION; IMMUNOLOGY; MICROBIOLOGY; PARASITOLOGY;

ANOPHELES ALBIMANUS; ANOPHELES GAMBIAE; BACTERIA (MICROORGANISMS); HEXAPODA; INVERTEBRATA; PLASMODIUM BERGHEI; VERTEBRATA;

ADAPTIVE IMMUNITY; ANIMALS; ANOPHELES; ANTI-BACTERIAL AGENTS; CELLS, CULTURED; GASTROINTESTINAL TRACT; HOST-PARASITE INTERACTIONS; MALE; MICE, INBRED BALB C; PLASMODIUM BERGHEI;

EID: 84930627438     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2015.05.004     Document Type: Article

References (68)

1. Aguilar R., Jedlicka A.E., Mintz M., Mahairaki V., Scott A.L., Dimopoulos G. Global gene expression analysis of Anopheles gambiae responses to microbial challenge. Insect Biochem. Mol. Biol 2005, 35:709-719.
2. Akira S., Takeda K., Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol 2001, 2:675-680.
3. Bahia A.C., Kubota M.S., Tempone A.J., Araujo H.R., Guedes B.A., Orfano A.S., et al. The JAK-STAT pathway controls Plasmodium vivax load in early stages of Anopheles aquasalis infection. PLoS Negl. Trop. Dis 2011, 5:e1317.
4. Baton L.A., Robertson A., Warr E., Strand M.R., Dimopoulos G. Genome-wide transcriptomic profiling of Anopheles gambiae hemocytes reveals pathogen-specific signatures upon bacterial challenge and Plasmodium berghei infection. BMC Genomics 2009, 10:257.
5. Blandin S., Shiao S.H., Moita L.F., Janse C.J., Waters A.P., Kafatos F.C., et al. Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 2004, 116:661-670.
6. Boman H.G., Steiner H. Humoral immunity in Cecropia pupae. Curr. Top. Microbiol. Immunol 1981, 94-95:75-91.
7. Bravo R., Frank R., Blundell P.A., Macdonald-Bravo H. Cyclin/PCNA is the auxiliary protein of DNA polymerase-delta. Nature 1987, 326:515-517.
8. Brehélin M., Roch P. Specificity, learning and memory in the innate immune response. Invertebr. Surviv. J. 2008, 5:103-109.
9. Chan A.S., Rodriguez M.H., Torres J.A., Rodriguez Mdel C., Villarreal C. Susceptibility of three laboratory strains of Anopheles albimanus (Diptera: Culicidae) to coindigenous Plasmodium vivax in southern Mexico. J. Med. Entomol 1994, 31:400-403.
10. Chen C.C., Laurence B.R. An ultrastructural study on the encapsulation of microfilariae of Brugia pahangi in the haemocoel of Anopheles quadrimaculatus. Int. J. Parasitol 1985, 15:421-428.
11. Cirimotich C.M., Dong Y., Clayton A.M., Sandiford S.L., Souza-Neto J.A., Mulenga M., et al. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 2011, 332:855-858.
12. Contreras-Garduno J., Rodriguez M.C., Rodriguez M.H., Alvarado-Delgado A., Lanz-Mendoza H. Cost of immune priming within generations: trade-off between infection and reproduction. Microbes Infect 2014, 16:261-267.
13. Costa A., Jan E., Sarnow P., Schneider D. The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS ONE 2009, 4:e7436.
14. De Gregorio E., Spellman P.T., Tzou P., Rubin G.M., Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J. 2002, 21:2568-2579.
15. Dimopoulos G., Richman A., Muller H.M., Kafatos F.C. Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:11508-11513.
16. Dimopoulos G., Seeley D., Wolf A., Kafatos F.C. Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. EMBO J. 1998, 17:6115-6123.
17. Dimopoulos G., Muller H.M., Levashina E.A., Kafatos F.C. Innate immune defense against malaria infection in the mosquito. Curr. Opin. Immunol 2001, 13:79-88.
18. Dimopoulos G., Christophides G.K., Meister S., Schultz J., White K.P., Barillas-Mury C., et al. Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:8814-8819.
19. Dong Y., Dimopoulos G. Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J. Biol. Chem 2009, 284:9835-9844.
20. Dong Y., Aguilar R., Xi Z., Warr E., Mongin E., Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2006, 2:e52.
21. Dong Y., Taylor H.E., Dimopoulos G. AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 2006, 4:e229.
22. Dong Y., Manfredini F., Dimopoulos G. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 2009, 5:e1000423.
23. Eyles D.E. A stain for malarial oocysts in temporary preparations. J. Parasitol 1950, 36:501.
24. Franke-Fayard B., Trueman H., Ramesar J., Mendoza J., van der Keur M., van der Linden R., et al. A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol. Biochem. Parasitol 2004, 137:23-33.
25. Garver L.S., Dong Y., Dimopoulos G. Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog 2009, 5:e1000335.
26. Garver L.S., Bahia A.C., Das S., Souza-Neto J.A., Shiao J., Dong Y., et al. Anopheles Imd pathway factors and effectors in infection intensity-dependent anti-Plasmodium action. PLoS Pathog 2012, 8:e1002737.
27. Garver L.S., de Almeida Oliveira G., Barillas-Mury C. The JNK pathway is a key mediator of Anopheles gambiae antiplasmodial immunity. PLoS Pathog 2013, 9:e1003622.
28. Gonzalez-Ceron L., Santillan F., Rodriguez M.H., Mendez D., Hernandez-Avila J.E. Bacteria in midguts of field-collected Anopheles albimanus block Plasmodium vivax sporogonic development. J. Med. Entomol 2003, 40:371-374.
29. Gupta L., Molina-Cruz A., Kumar S., Rodrigues J., Dixit R., Zamora R.E., et al. The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae. Cell Host Microbe 2009, 5:498-507.
30. Hauton C., Smith V.J. Adaptive immunity in invertebrates: a straw house without a mechanistic foundation. Bioessays 2007, 29:1138-1146.
31. Hernández-Martínez S., Barradas-Bautista D., Rodriguez M.H. Diferential DNA synthesis in Anopheles albimanus tissues induced by immune challenge with different microorganisms. Arch. Insect Biochem. Physiol 2013, 84:1-14.
32. Hernandez-Martinez S., Lanz H., Rodriguez M.H., Gonzalez-Ceron L., Tsutsumi V. Cellular-mediated reactions to foreign organisms inoculated into the hemocoel of Anopheles albimanus (Diptera: Culicidae). J. Med. Entomol 2002, 39:61-69.
33. Hernandez-Martinez S., Roman-Martinez U., Martinez-Barnetche J., Garrido E., Rodriguez M.H., Lanz-Mendoza H. Induction of DNA synthesis in Anopheles albimanus tissue cultures in response to a Saccharomyces cerevisiae challenge. Arch. Insect Biochem. Physiol 2006, 63:147-158.
34. Herrera-Ortiz A., Martinez-Barnetche J., Smit N., Rodriguez M.H., Lanz-Mendoza H. The effect of nitric oxide and hydrogen peroxide in the activation of the systemic immune response of Anopheles albimanus infected with Plasmodium berghei. Dev. Comp. Immunol 2011, 35:44-50.
35. Hillyer J.F., Barreau C., Vernick K.D. Efficiency of salivary gland invasion by malaria sporozoites is controlled by rapid sporozoite destruction in the mosquito haemocoel. Int. J. Parasitol 2007, 37:673-681.
36. Hoffmann J.A., Hoffmann D. The inducible antibacterial peptides of dipteran insects. Res. Immunol 1990, 141:910-918.
37. King J.G., Hillyer J.F. Spatial and temporal in vivo analysis of circulating and sessile immune cells in mosquitoes: hemocyte mitosis following infection. BMC Biol 2013, 11:55.
38. Kurtz J. Specific memory within innate immune systems. Trends Immunol 2005, 26:186-192.
39. Kurtz J., Franz K. Innate defence: evidence for memory in invertebrate immunity. Nature 2003, 425:37-38.
40. Little T.J., Kraaijeveld A.R. Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol. Evol 2004, 19:58-60.
41. Marois E. The multifaceted mosquito anti-Plasmodium response. Curr. Opin. Microbiol 2011, 14:429-435.
42. Martinez-Barnetche J., Gomez-Barreto R.E., Ovilla-Munoz M., Tellez-Sosa J., Garcia Lopez D.E., Dinglasan R.R., et al. Transcriptome of the adult female malaria mosquito vector Anopheles albimanus. BMC Genomics 2012, 13:207.
43. Medzhitov R., Janeway C.A. Decoding the patterns of self and nonself by the innate immune system. Science 2002, 296:298-300.
44. Meister S., Kanzok S.M., Zheng X.L., Luna C., Li T.R., Hoa N.T., et al. Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:11420-11425.
45. Michel K., Kafatos F.C. Mosquito immunity against Plasmodium. Insect Biochem. Mol. Biol 2005, 35:677-689.
46. Moret Y., Siva-Jothy M.T. Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc. Biol. Sci 2003, 270:2475-2480.
47. Ng T.H., Chiang Y.A., Yeh Y.C., Wang H.C. Review of Dscam-mediated immunity in shrimp and other arthropods. Dev. Comp. Immunol 2014, 46:129-138.
48. Noden B.H., Vaughan J.A., Pumpuni C.B., Beier J.C. Mosquito ingestion of antibodies against mosquito midgut microbiota improves conversion of ookinetes to oocysts for Plasmodium falciparum, but not P. yoelii. Parasitol. Int 2011, 60:440-446.
49. Oduol F., Xu J., Niare O., Natarajan R., Vernick K.D. Genes identified by an expression screen of the vector mosquito Anopheles gambiae display differential molecular immune response to malaria parasites and bacteria. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:11397-11402.
50. Pham L.N., Dionne M.S., Shirasu-Hiza M., Schneider D.S. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathog 2007, 3:e26.
51. Pike A., Vadlamani A., Sandiford S.L., Gacita A., Dimopoulos G. Characterization of the Rel2-regulated transcriptome and proteome of Anopheles stephensi identifies new anti-Plasmodium factors. Insect Biochem. Mol. Biol 2014, 52:82-93.
52. Pumpuni C.B., Demaio J., Kent M., Davis J.R., Beier J.C. Bacterial population dynamics in three anopheline species: the impact on Plasmodium sporogonic development. Am. J. Trop. Med. Hyg 1996, 54:214-218.
53. Rodrigues J., Brayner F.A., Alves L.C., Dixit R., Barillas-Mury C. Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 2010, 329:1353-1355.
54. Rodriguez M.C., Margos G., Compton H., Ku M., Lanz H., Rodriguez M.H., et al. Plasmodium berghei: routine production of pure gametocytes, extracellular gametes, zygotes, and ookinetes. Exp. Parasitol 2002, 101:73-76.
55. Rolff J., Siva-Jothy M.T. Invertebrate ecological immunology. Science 2003, 301:472-475.
56. Sadd B.M., Schmid-Hempel P. Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr. Biol 2006, 16:1206-1210.
57. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. third ed.
58. Sanders H.R., Foy B.D., Evans A.M., Ross L.S., Beaty B.J., Olson K.E., et al. Sindbis virus induces transport processes and alters expression of innate immunity pathway genes in the midgut of the disease vector, Aedes aegypti. Insect Biochem. Mol. Biol 2005, 35:1293-1307.
59. Schulenburg H., Boehnisch C., Michiels N.K. How do invertebrates generate a highly specific innate immune response?. Mol. Immunol 2007, 44:3338-3344.
60. Smith P.H., Mwangi J.M., Afrane Y.A., Yan G., Obbard D.J., Ranford-Cartwright L.C., et al. Alternative splicing of the Anopheles gambiae Dscam gene in diverse Plasmodium falciparum infections. Malar. J. 2011, 10:156.
61. Sun J., Deng W.M. Hindsight mediates the role of notch in suppressing hedgehog signaling and cell proliferation. Dev. Cell 2007, 12:431-442.
62. Tahar R., Boudin C., Thiery I., Bourgouin C. Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. EMBO J. 2002, 21:6673-6680.
63. Tomas A.M., Margos G., Dimopoulos G., van Lin L.H., de Koning-Ward T.F., Sinha R., et al. P25 and P28 proteins of the malaria ookinete surface have multiple and partially redundant functions. EMBO J. 2001, 20:3975-3983.
64. Vlachou D., Schlegelmilch T., Christophides G.K., Kafatos F.C. Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr. Biol 2005, 15:1185-1195.
65. Warr E., Das S., Dong Y., Dimopoulos G. The Gram-negative bacteria-binding protein gene family: its role in the innate immune system of anopheles gambiae and in anti-Plasmodium defence. Insect Mol. Biol 2008, 17:39-51.
66. Waterhouse R.M., Kriventseva E.V., Meister S., Xi Z., Alvarez K.S., Bartholomay L.C., et al. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007, 316:1738-1743.
67. Winger L.A., Tirawanchai N., Nicholas J., Carter H.E., Smith J.E., Sinden R.E. Ookinete antigens of Plasmodium berghei. Appearance on the zygote surface of an Mr 21 kD determinant identified by transmission-blocking monoclonal antibodies. Parasite Immunol 1988, 10:193-207.
68. Witteveldt J., Cifuentes C.C., Vlak J.M., van Hulten M.C. Protection of Penaeus monodon against white spot syndrome virus by oral vaccination. J. Virol 2004, 78:2057-2061.