A new role for an old antimicrobial: Lysozyme c-1 can function to protect malaria parasites in Anopheles mosquitoes

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Kajla, Mayur K ^a   Shi, Lei ^a,b   Li, Bin ^a,c   Luckhart, Shirley ^d   Li, Jianyong ^e   Paskewitz, Susan M ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; LYSOZYME; LYSOZYME C 1; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; ANTIBODY; ANTIINFECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOPHELES GAMBIAE; ANOPHELES STEPHENSI; ARTICLE; CONTROLLED STUDY; ENZYME ANALYSIS; FEMALE; GENE SILENCING; HOST PARASITE INTERACTION; IMMUNOHISTOCHEMISTRY; MICROBIOLOGICAL PHENOMENA AND FUNCTIONS; MIDGUT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYST; OOKINETE; PARASITE DEVELOPMENT; PARASITE MELANIZATION; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; AMINO ACID SEQUENCE; ANIMAL; ANOPHELES; BACTERIAL COUNT; BACTERIUM; CHEMISTRY; CYTOLOGY; DIGESTIVE SYSTEM; DRUG EFFECT; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; HUMAN; MALARIA; METABOLISM; MOLECULAR GENETICS; PARASITE; PARASITOLOGY; PHYSIOLOGY; PIGMENTATION;

ANOPHELES (GENUS); ANOPHELES GAMBIAE; ANOPHELES STEPHENSI; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES; ANTI-INFECTIVE AGENTS; ANTIBODIES; BACTERIA; COLONY COUNT, MICROBIAL; DIGESTIVE SYSTEM; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HUMANS; MALARIA; MOLECULAR SEQUENCE DATA; MURAMIDASE; OOCYSTS; PARASITES; PIGMENTATION; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM;

EID: 79955808831     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019649     Document Type: Article

References (40)

1. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661-670.
2. Osta MA, Christophides GK, Kafatos FC, (2004) Effects of mosquito genes on Plasmodium development. Science 303: 2030-2032.
3. Vlachou D, Schlegelmilch T, Christophides GK, Kafatos FC, (2005) Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Current Biol 15: 1185-1195.
4. Kotsyfakis M, Ehret-Sabatier L, Siden-Kiamos I, Mendoza J, Sinden RE, et al. (2005) Plasmodium berghei ookinetes bind to Anopheles gambiae and Drosophila melanogaster annexins. Mol Microbiol 57: 171-179.
5. Arrighi RBG, Lycett G, Mahairaki V, Siden-Kiamos I, Louis C, (2005) Laminin and the malaria parasite's journey through the mosquito midgut. J Exp Biol 208: 2497-2502.
6. Nacer A, Walker K, Hurd H, (2008) Localisation of laminin within Plasmodium berghei oocysts and the midgut epithelial cells of Anopheles stephensi. Parasit Vectors 1: 33.
7. Nakimbugave D, Masschalck B, Atanassova M, Zewdie-Bosüher A, Michiels CW, (2006) Comparison of bactericidal activity of six lysozymes at atmospheric pressure and under high hydrostatic pressure. Int J Food Microbiol 108: 355-363.
8. Clark A, Dupont C, (1992) O-acetylated peptidoglycan: its occurrence, pathological significance and biosynthesis. Can J Microbiol 38: 85-91.
9. Yu KH, Kim KN, Lee JH, Lee HS, Kim SH, et al. (2002) Comparative study on characteristics of lysozymes from the hemolymph of three lepidopteran larvae, Galleria mellonella, Bombyx mori, Agrius convolvuli. Dev Comp Immunol 26: 707-713.
10. Gandhe AS, Janardhan G, Nagaraju J, (2007) Immune upregulation of novel antibacterial proteins from silkmoths (Lepidoptera) that resemble lysozymes but lack muramidase activity. Insect Biochem Mol Biol 37: 655-666.
11. Callewaert L, Michiels CW, (2010) Lysozymes in the animal kingdom. J Biosci 35: 127-160.
12. Hultmark D, (1996) Insect lysozymes. Lysozymes: Model enzymes in biochemistry and biology Birkhauser Verlag Basel pp. 87-102.
13. Gao Y, Fallon AM, (2000) Immune activation upregulates lysozyme gene expression in Aedes aegypti mosquito cell culture. Insect Mol Biol 9: 553-558.
14. Ursic Bedoya RJ, Mitzey AM, Obraztsova M, Lowenberger C, (2005) Molecular cloning and transcriptional activation of lysozyme-encoding cDNAs in the mosquito Aedes aegypti. Insect Mol Biol 14: 89-94.
15. Li B, Calvo E, Marinotti O, James AA, Paskewitz SM, (2005) Characterization of the c-type lysozyme gene family in Anopheles gambiae. Gene 360: 131-139.
16. Li B, Paskewitz SM, (2006) A role for lysozyme in melanization of Sephadex beads in Anopheles gambiae. J Insect Physiol 52: 936-942.
17. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, et al. (2006) Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2: e52.
18. Dong Y, Manfredini F, Dimopoulos G, (2009) Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog 5: e1000423.
19. Kajla MK, Andreeva O, Gilbreath TM 3rd, Paskewitz SM, (2010) Characterization of expression, activity and role in antibacterial immunity of Anopheles gambiae lysozyme c-1. Comp Biochem Physiol B Biochem Mol Biol 155: 201-209.
20. Chun J, Riehle M, Paskewitz SM, (1995) Effect of mosquito age and reproductive status on melanization of sephadex beads in Plasmodium-refractory and-susceptible strains of lysozyme c-1 Anopheles gambiae. J Invertebr Pathol 66: 11-17.
21. Paskewitz SM, Riehle M, (1998) A factor preventing melanization of sephadex CM C-25 beads in Plasmodium-susceptible and refractory Anopheles gambiae. Exp Parasitol 90: 34-41.
22. Collins FH, Sakai RK, Vernick KD, Paskewitz SM, Seeley DC, et al. Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae.
23. Castillo JC, Robertson AE, Strand MR, (2006) Characterization of hemocytes from the mosquitoes Anopheles gambiae and Aedes aegypti. Insect Biochem Mol Biol 36: 891-903.
24. Meis JF, Pool G, van Gemert GJ, Lensen AH, Ponnudurai T, Meuwissen JH, (1989) Plasmodium falciparum ookinetes migrate intercellularly through Anopheles stephensi midgut epithelium. Parasitol Res 76: 13-19.
25. Adini A, Warburg A, (1999) Interaction of Plasmodium gallinaceum ookinetes and oocysts with extracellular matrix proteins. Parasitol 119: 331-336.
26. Dessens JT, Siden-Kiamos I, Mendoza J, Mahairaki V, Khater E, et al. (2003) SOAP, a novel malaria ookinetes protein involved in mosquito midgut invasion and oocyst development. Mol Microbiol 49: 319-329.
27. Vlachou D, Lycett G, Sidén-Kiamos I, Blass C, Sinden RE, et al. (2001) Anopheles gambiae laminin interacts with the P25 surface protein of Plasmodium berghei ookinetes. Mol Biochem Parasitol 112: 229-237.
28. Mahairaki V, Voyatzi T, Sidén-Kiamos I, Louis C, (2005) The Anopheles gambiae gamma1 laminin directly binds the Plasmodium berghei circumsporozoite and TRAP-related protein (CTRP). Mol Biochem Parasitol 140: 119-121.
29. Moss JM, Van Damme MPI, Murphy WH, Preston BN, (1997) Dependence of salt concentration on glycosaminoglycan-lysozyme interactions in cartilage. Arch Biochem Biophys 348: 49-55.
30. Park PW, Biedermann K, Mecham L, Bissett DL, Mecham RP, (1996) Lysozyme binds to elastin and protects elastin from elastase-mediated degradation. J Invest Dermatol 106: 1075-1080.
31. Ahmed AM, Maingon BR, Hurd H, (2002) The costs of mounting of an immune response are reflected in the reproductive fitness of the mosquito Anopheles gambiae. OIKOS 97: 371-377.
32. Reddy JT, Locke M, (1990) The size limited penetration of gold particles through insect basal laminae. J Insect Physiol 36: 397-408.
33. Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C, (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 5997: 1353-1355.
34. Paskewitz SM, Reese-Stardy SR, Gorman MJ, (1999) An easter-like serine protease from Anopheles gambiae exhibits changes in transcript abundance following immune challenge. Insect Mol Biol 8: 329-337.
35. Malaria Research and Reference Reagent Resource Center (MR4) (http://www.mr4.org/).
36. Franke-Fayard B, Trueman H, Ramesar J, Mendoza J, van der Keur M, et al. (2004) A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol Biochem Parasitol 137: 23-33.
37. Surachetpong W, Singh N, Cheung KW, Luckhart S, (2009) MAPK ERK signaling regulates the TGF-beta1-dependent mosquito response to Plasmodium falciparum. PLoS Pathog 4: 1000366.
38. Winger LA, Tirawanchai N, Nicholas J, Carter HE, Smith JE, et al. (1988) Ookinete antigens of Plasmodium berghei. Appearance on the zygote surface of an Mr 21 kD determinant identified by transmission-blocking monoclonal antibodies. Parasite Immunol 10: 193-207.
39. Han YS, Thompson J, Kafatos FC, Barillas-Mury C, (2000) Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinetes invasion of mosquitoes. EMBO J 19: 6030-6040.
40. Salazar CE, Mills-Hamm D, Kumar V, Collins FH, (1993) Sequence of a cDNA from the mosquito Anopheles gambiae encoding a homologue of human ribosomal protein S7. Nucleic Acids Res 21: 4147.