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Interactions between the bumblebee, Bombus terrestris, and its trypanosome parasite, Crithidia bombi

By Carolyn Riddell

Abstract

Theory predicts that hosts should evolve highly specific immune defences when there are significant fitness costs associated with parasitic infection. Historically, mechanistic studies have defined invertebrate immunity as innate and non-specific. However, recent evidence from ecological studies challenges this view by finding a high degree of specificity between host and parasite and evidence of immune priming, that are indicative of a more complex system. Critics of the ecological perspective assert that without mechanistic evidence, there is no sound reason to assume that these phenomena are generated by innate immunity. To begin bridging the gap between mechanistic and ecological fields of innate immunity, I have examined the molecular basis of specificity and priming in the model Bombus-Crithidia host-parasite system.\ud My studies show that immune gene expression mirrors the interaction effect found with indirect, ecological measures of immunity, providing unequivocal evidence of innate immune specificity in invertebrates. A similar examination of immune priming suggested that the genes I analysed were not involved in this phenomenom and is most likely to be indicative of the relative importance of different arms of immunity in the primed immune response. Finally, I examined more general aspects of the immune response to Crithidia by characterising the temporal dynamics of immune gene expression throughout infection for the first time in this model host-parasite system. I also confirmed that the assumed link between virulence and intensity of Crithidia infection is valid. To conclude, my studies have shown that integration of molecular knowledge into natural host-parasite systems can only serve to enrich our understanding of the wider capabilities of invertebrate innate immunity

Publisher: University of Leicester
Year: 2010
OAI identifier: oai:lra.le.ac.uk:2381/7963

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Citations

  1. (1996). A CONSERVED SIGNALING PATHWAY: The Drosophila Toll-Dorsal Pathway.
  2. (1992). A diphasic immune response against bacteria in the American cockroach.
  3. (2005). A Direct Role for Dual Oxidase in Drosophila Gut Immunity.
  4. (2009). A fibrinogen-related protein from bay scallop Argopecten irradians involved in innate immunity as pattern recognition receptor.
  5. (2006). A genetic module regulates the melanization response of Anopheles to Plasmodium.
  6. (2001). A genome-wide analysis of immune responses in Drosophila.
  7. (2000). A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly.
  8. (2007). A multilayered defense against infection: combinatorial control of insect immune genes.
  9. (1973). A new evolutionary law.
  10. (1996). A novel human serum lectin with collagen-and fibrinogen-like domains that functions as an opsonin.
  11. (2004). A novel lectin with a fibrinogen-like domain and its potential involvement in the innate immune response of Armigeres subalbatus against bacteria.
  12. (1995). A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense.
  13. (2007). A screen for immunity genes evolving under positive selection in Drosophila.
  14. (2002). A serpin mutant links Toll activation to melanization in the host defence of Drosophila.
  15. (2007). A Specific Primed Immune Response in Drosophila Is Dependent on Phagocytes.
  16. (1986). Acquisition and Allocation of Resources - Their Influence on Variation in Life-History Tactics.
  17. (2003). Activation of host constitutive immune defence by an intestinal trypanosome parasite of bumble bees.
  18. (2007). Adaptive immunity in invertebrates: A straw house without a mechanistic foundation.
  19. (2003). Adaptive innate immunity? Responsivemode prophylaxis in the mealworm beetle, Tenerio molitor.
  20. (2003). Adult midgut expressed sequence tags from the tsetse fly Glossina morsitans morsitans and expression analysis of putative immune response genes.
  21. (2006). AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anophles gambiae innate immune system.
  22. (2005). An antimicrobial peptide with trypanocidal activity characterized from Glossina morsitans morsitans.
  23. (2005). An Antioxidant System Required for Host Protection against Gut Infection in Drosophila.
  24. (2006). An essential complementary role of NF-κB pathway to microbicidal oxidants in Drosophila gut immunity.
  25. (2002). An immuneresponsive Serpin regulates the melanization cascade in Drosophila.
  26. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T
  27. (2004). Analysis of Signal-dependent Changes
  28. (2009). Anopheles Fibrinogen-related Proteins Provide Expanded Pattern Recognition Capacity against Bacteria and Malaria Parasites.
  29. (1999). Anopheles gambiae Ag-STAT, a new insect member of the STAT family, is activated in response to bacterial infection.
  30. (2006). Anopheles gambiae Immune Responses to Human and Rodent Plasmodium Parasite Species.
  31. (2008). Antimicrobial Defense and Persistent Infection in Insects.
  32. (2009). Antimicrobial Peptide Evolution in the Asiatic Honey Bee Apis cerana.
  33. (1999). Antimicrobial peptides in insects; structure and function.
  34. (2006). Antimicrobial peptides in the interactions between insects and flagellate parasites.
  35. (2002). Antimicrobial peptides of multicellular organisms.
  36. (2005). Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?
  37. (2005). Antioxidant gene expression in the blood-feeding fly Glossina morsitans morsitans.
  38. (1999). Associations between parasitism and host genotype in natural populations of Daphnia (Crustacea: Cladocera).
  39. (1998). Bacterial lipopolysaccharide binds and stimulates cytokine-producing cells before neutralization by endogenous lipoproteins can occur.
  40. (2004). Behavioural interactions, kin and disease susceptibility in the bumblebee Bombus terrestris.
  41. (2000). Big houses, big cars, superfleas and the costs of reproduction.
  42. (2002). Biological and biomedical implications of the co-evolution of pathogens and their hosts.
  43. (1997). Biological mediators of insect immunity.
  44. (1979). Biology of the Kinetoplastida of arthropods, London,
  45. (1995). Brugia pahangi: the effects of cecropins on microfilariae in vitro and in Aedes aegypti.
  46. (2006). Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information.
  47. (2003). Bumblebee workers from different sire groups vary in susceptibility to parasite infection.
  48. (2003). Bumblebees: Behaviour and Ecology,
  49. (2004). Carbohydrates and glycoconjugates: progress in non-mammalian glycosylation, glycosyltransferases, invertebrate lectins and carbohydrate-carbohydrate interactions.
  50. (1987). Cell-Free Immunity in Insects.
  51. (1999). Cell-surface sialoglycoconjugate structures in wildtype and mutant Crithidia fasciculata.
  52. (2003). Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends in
  53. (2002). Changes of sialomolecules during the dimethylsulfoxide-induced differentiation of Herpetomonas samuelpessoai.
  54. (2009). Characteristics of Novel Insect Defensin-Based Membrane-Disrupting Trypanocidal Peptides.
  55. (2004). Characterization of a defensin from the sand fly Phlebotomus duboscqi induced by challenge with bacteria or the protozoan parasite Leishmania major.
  56. (2008). Circadian regulation in the ability of Drosophila to combat pathogenic infections. Current biology 18,
  57. (2001). Clonal variation and covariation in aphid resistance to parasitoids and a pathogen.
  58. (2001). Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi.
  59. (2008). Cloning and expression profiling of four antibacterial peptide genes from the bumblebee Bombus ignitus. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology,
  60. (1998). Cloning, expression of the polypeptide, and tissue localization.
  61. (2007). Clustering of peptidoglycan recognition protein-SA is required for sensing lysine-type peptidoglycan in insects.
  62. (2006). Coevolutionary interactions between host and parasite genotypes.
  63. (1998). Coevolutionary interactions between host life histories and parasite life cycles.
  64. (2002). Collectins and ficolins: sugar pattern recognition molecules of the mammalian innate immune system. BBAGeneral Subjects,
  65. (1999). Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi.
  66. (2005). Colony-level impacts of immune responsiveness in honey bees, Apis mellifera.
  67. (2004). Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae.
  68. (2000). Condition-dependent expression of virulence in a trypanosome infecting bumblebees.
  69. (2000). Constitutive expression of a complement-like protein in Toll and JAK gain-of-function mutants of Drosophila.
  70. (2002). Constitutive expression of a single antimicrobial peptide can restore wild-type resistance to infection in immunodeficient Drosophila mutants.
  71. (2007). Convergent use of RhoGAP toxins by eukaryotic parasites and bacterial pathogens.
  72. (1988). Crithidia-bombi Sp N. a Flagellated Parasite of a
  73. (2002). Critical evaluation of the role of the Toll-like receptor 18-Wheeler in the host defense of Drosophila.
  74. (2007). Crystal cell rupture after injury in Drosophila requires the JNK pathway, small GTPases and the TNF homolog Eiger.
  75. (2000). Crystallization of antimicrobial pores in membranes: magainin and protegrin.
  76. (2007). Current knowledge of the large RhoGAP family of proteins.
  77. (2002). Cutting Edge: The Toll Pathway Is Required for Resistance to Gram-Positive Bacterial Infections in Drosophila The
  78. (2000). Cytotoxicity and cytotoxic molecules in invertebrates.
  79. (2007). Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans.
  80. (1998). Differential display of peptides induced during the immune response of Drosophila: a matrix-assisted laser desorption ionization time-of-flight mass spectrometry study.
  81. (2005). Differential expression of FREP genes in two strains of Biomphalaria glabrata following exposure to the digenetic trematodes Schistosoma mansoni and Echinostoma paraensei.
  82. (2005). Differential gene expression in queen–worker caste determination in bumble-bees.
  83. (1996). Differential in vitro and in vivo behavior of three strains of Trypanosoma cruzi in the gut and hemolymph of Rhodnius prolixus.
  84. (2009). Differential influence of gp63-like molecules in three distinct Leptomonas species on the adhesion to insect cells.
  85. (2004). Diversification of Ig superfamily genes in an invertebrate.
  86. (2004). Do hosts and parasites coevolve? Empirical support from the Schistosoma system.
  87. (2007). Drosophila Calcineurin Promotes Induction of Innate Immune Responses.
  88. (2000). Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity.
  89. (2007). Drosophila eiger mutants are sensitive to extracellular pathogens.
  90. (2005). Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species.
  91. (1997). Drosophila host defense: Differential induction of antimicrobial peptide genes after infection by various classes of microorganisms.
  92. (1996). Drosophila immunity: a comparative analysis of the Rel proteins dorsal and Dif in the induction of the genes encoding diptericin and cecropin.
  93. (2001). Drosophila immunity: two paths to NF-κB.
  94. (2002). Drosophila innate immunity: an evolutionary perspective.
  95. (2005). Drosophila RNAi Screen Reveals CD36 Family Member Required for Mycobacterial Infection.
  96. (2003). Dual Activation of the Drosophila Toll Pathway by Two Pattern Recognition Receptors.
  97. (1999). Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection.
  98. (2007). Dynamic evolution of the innate immune system in Drosophila.
  99. (2005). Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila.
  100. (1996). Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology.
  101. (1995). Effect of a cecropin-like synthetic peptide (Shiva-3) on the sporogonic development of Plasmodium berghei.
  102. (1989). Effects of magainins and cecropins on the sporogonic development of malaria parasites in mosquitoes.
  103. (2009). Environment can alter selection in host-parasite interactions. Trends in Parasitology.
  104. (2002). Epithelial innate immunity - A novel antimicrobial peptide with antiparasitic activity in the blood-sucking insect Stomoxys calcitrans.
  105. (2003). Evidence for memory in invertebrate immunity.
  106. (2001). Evidence for recurrent paralogous gene conversion and exceptional allelic divergence in the Attacin genes of Drosophila melanogaster.
  107. (2008). Evidence for specificity and memory in the insect innate immune response.
  108. (2008). Evolution and potential function of fibrinogenlike domains across twelve Drosophila species.
  109. (2007). Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes.
  110. (2001). Expression profiles during honeybee caste determination.
  111. (2008). Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata.
  112. (2005). Extensive diversity of IgSuperfamily proteins in the immune system of insects.
  113. (2003). Extracellular release of the surface metalloprotease, gp63, from Leishmania and insect trypanosomatids.
  114. (2000). Female mating frequencies in Bombus spp. from Central Europe.
  115. (1971). Flagellar attachment and detachment of Crithidia fasciculata to the gut wall of Anopheles gambiae.
  116. (1995). Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L.
  117. (2004). Function of the drosophila pattern-recognition receptor PGRP-SD in the detection of Gram-positive bacteria.
  118. (2005). Functional analysis of immune response genes in Drosophila identifies JNK pathway as a regulator of antimicrobial peptide gene expression in S2 cells.
  119. (1993). Functional and chemical characterization of Hymenoptaecin, an antibacterial polypeptide that is infection-inducible in the honeybee (Apis mellifera).
  120. (2003). Functional Diversity of the Drosophila PGRP-LC Gene Cluster in the Response to Lipopolysaccharide and Peptidoglycan.
  121. (2001). Gambicin: A novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae.
  122. (2004). Genetic basis of natural variation in D.melanogaster antibacterial immunity.
  123. (1999). Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi.
  124. (2001). Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection.
  125. (2006). Genetic variation in Drosophila melanogaster pathogen susceptibility.
  126. (2006). Genetic Variation in Drosophila melanogaster Resistance to Infection: A Comparison Across Bacteria.
  127. (2001). Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays.
  128. (1991). Genomic diversity and antigenic variation of HIV-1: links between pathogenesis, epidemiology and vaccine development.
  129. (2008). Genotype-by-Environment Interactions and Adaptation to Local Temperature Affect Immunity and Fecundity in Drosophila melanogaster.
  130. (2007). Genotype-specific interactions and the trade-off between host and parasite fitness.
  131. (1994). Geographic variation in reproductive success of the parasitoid Asobara tabida in larvae of several Drosophila species.
  132. (2000). Gram-negative Bacteria-binding Protein, a Pattern Recognition Receptor for Lipopolysaccharide and beta -1,3-Glucan That Mediates the Signaling for the Induction of Innate Immune Genes in Drosophila melanogaster Cells.
  133. (2005). Growth-phase dependent substrate adhesion in Crithidia fasciculata.
  134. (2002). Heat-shock proteins as activators of the innate immune system.
  135. (1999). Heritable variation in resistance to gastrointestinal nematodes in an unmanaged mammal population.
  136. (2004). Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees.
  137. (2007). Host-parasite 'Red Queen' dynamics archived in pond sediment.
  138. (1998). Host-parasite co-evolution: evidence for rare advantage and time-lagged selection in a natural population.
  139. (2006). Host-parasite interactions for virulence and resistance in a malaria model system.
  140. (1995). Host-parasite interactions: infection of common clones in natural populations of a freshwater snail (Potamopyrgus antipodarum).
  141. (2007). How do invertebrates generate a highly specific innate immune response?
  142. (1996). Identification and characterization of differentially expressed cDNAs of the vector mosquito, Anopheles gambiae.
  143. (2005). Identification and characterization of the fibrinogen-like domain of fibrinogen-related proteins in the mosquito, Anopheles gambiae, and the fruitfly, Drosophila melanogaster, genomes.
  144. (2006). Identification of Drosophila gene products required for phagocytosis of Candida albicans.
  145. (2004). Identification of genes involved in the response of haemocytes of Penaeus japonicus by suppression subtractive hybridization (SSH) following microbial challenge.
  146. (2003). Immune Activation of NF-κB and JNK Requires Drosophila TAK1.
  147. (2006). Immune pathways and defence mechanisms in honey bees Apis mellifera.
  148. (2008). Immune response impairs learning in free-flying bumble-bees.
  149. (2003). Immune response inhibits associative learning in insects.
  150. (2001). Immune response of Drosophila melanogaster to infection with the flagellate parasite Crithidia spp.
  151. (2009). Immune responses of bumblebee workers as a function of individual and colony age: senescence versus plastic adjustment of the immune function.
  152. (1996). Immunity to eukaryotic parasites in vector insects.
  153. (2002). Immunopeptides in the defense reactions of Glossina morsitans to bacterial and Trypanosoma brucei brucei infections.
  154. (2004). In vitro cultivation and cloning of the parasite Crithidia bombi. Department of medical parasitology and infection biology.
  155. (2004). In vivo dynamics of an immune response in the bumble bee Bombus terrestris.
  156. (2004). In vivo dynamics of an immune response in the bumble bee.
  157. (1991). Infectious diseases of humans,
  158. (2007). Inference of parasite local adaptation using two different fitness components.
  159. (2000). Innate immune recognition: mechanisms and pathways.
  160. (2006). Innate immune responses regulate trypanosome parasite infection of the tsetse fly Glossina morsitans morsitans.
  161. (2006). Insect haemocytes: What type of cell is that?
  162. (2008). Insect immune resistance to parasitoids.
  163. (2006). Insect Immunity Shows Specificity in Protection upon Secondary Pathogen Exposure.
  164. (2009). Insect Infection and Immunity: Evolution, Ecology and Mechanisms,
  165. (2006). Insect psychoneuroimmunology: Immune response reduces learning in protein starved bumblebees (Bombus terrestris).
  166. (1989). Interaction of human defensins with Escherichia coli. Mechanism of bactericidal activity.
  167. (2005). Invertebrate immunity and the limits of mechanistic immunology.
  168. (2003). Isolation and characterization of a novel insect defensin from Rhodnius prolixus, a vector of Chagas disease.
  169. (1990). Isolation and characterization of abaecin, a major antibacterial response peptide in the honeybee (Apis mellifera).
  170. (2002). JNK signaling pathway is required for efficient wound healing in Drosophila.
  171. (1998). JNK, cytoskeletal regulator and stress response kinase? A Drosophila perspective.
  172. (2003). Killing of African trypanosomes by antimicrobial peptides.
  173. (2004). Landmark - The road to Toll.
  174. (2005). Ligand-induced dimerization of Drosophila peptidoglycan recognition proteins in vitro.
  175. (2003). Maternal transfer of strain-specific immunity in an invertebrate.
  176. (2004). Memory in the innate and adaptive immune systems.
  177. (2001). Microarray analysis and organization of circadian gene expression in Drosophila.
  178. (1994). Midgut Lectin Activity And Sugar Specificity In Teneral And Fed Tsetse.
  179. (1997). Midgut-specific immune molecules are produced by the blood-sucking insect Stomoxys calcitrans.
  180. (2002). Molecular biology of the cell,
  181. (1993). Molecular flypaper, host defense, and atherosclerosis. Structure, binding properties, and functions of macrophage scavenger receptors.
  182. (2004). Monomeric and polymeric gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway.
  183. (1999). Mosquito-Plasmodium interactions in response to immune activation of the vector.
  184. (2005). Natural insect host-parasite systems show immune priming and specificity: puzzles to be solved.
  185. (2008). Natural selection on the Drosophila antimicrobial immune system.
  186. (2007). Natural variation in the genetic architecture of a host-parasite interaction in the bumblebee Bombus terrestris.
  187. (2003). Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila.
  188. (2001). On the evolutionary ecology of host-parasite SCHMID-HEMPEL, P. (2005a) Evolutionary ecology of insect immune defenses.
  189. (2003). On the evolutionary ecology of specific immune defence.
  190. (2001). On the existence of cytokines in invertebrates.
  191. (2002). Overexpression of a pattern-recognition receptor, peptidoglycan-recognition protein-LE, activates imd/relish-mediated antibacterial defense and the prophenoloxidase cascade in Drosophila larvae.
  192. (2000). Parasite adaptation to locally common host genotypes.
  193. (2008). Parasite immune evasion: a momentous molecular war.
  194. (2006). Parasite-host specificity: experimental studies on the basis of parasite adaptation.
  195. (2001). Parasite-responsive IgSF members in the snail Biomphalaria glabrata: characterization of novel genes with tandemly arranged IgSF domains and a fibrinogen domain.
  196. (2004). Parasite-specific immune response in adult Drosophila melanogaster: a genomic study.
  197. (1991). Parasites delay worker reproduction in bumblebees: consequences for eusociality.
  198. (2002). Pathogenesis of Plasmodium falciparum malaria: the roles of parasite adhesion and antigenic variation.
  199. (1994). Pathogenicity of trypanosomatids on insects.
  200. (1998). Patterns of local adaptation of a protozoan parasite to its bumblebee host.
  201. (2001). Paxillin: a focal adhesion-associated adaptor protein.
  202. (2004). Peptidoglycan Molecular Requirements Allowing Detection by the Drosophila Immune Deficiency Pathway The
  203. (2003). Peptidoglycan Recognition Proteins Involved in 1,3-β -D-Glucandependent Prophenoloxidase Activation System of Insect.
  204. (2006). PGRP-LC and PGRP-LE have essential yet distinct functions in the drosophila immune response to monomeric DAP-type peptidoglycan.
  205. (2008). Phagocytosis and comparative innate immunity: learning on the fly.
  206. (1999). Phylogenetic perspectives in innate immunity.
  207. (2008). Physical stress primes the immune response of Galleria mellonella larvae to infection by Candida albicans.
  208. (1995). Plant defensins: novel antimicrobial peptides as components of the host defense system.
  209. (1998). Plasmodium gallinaceum: differential killing of some mosquito stages of the parasite by insect defensin.
  210. (2006). Plexin-A1 and its interaction with DAP12 in immune responses and bone homeostasis.
  211. (2008). Plexin-A4 negatively regulates T lymphocyte responses.
  212. (2001). Postembryonic hematopoiesis in Drosophila.
  213. (2006). Prevalence of Local Immune Response against Oral Infection in a Drosophila/Pseudomonas Infection Model. Plos Pathogens,
  214. (2005). Profiling early infection responses: Pseudomonas aeruginosa eludes host defenses by suppressing antimicrobial peptide gene expression.
  215. (1984). Prophenoloxidase Activation - Nonself Recognition and Cell Cooperation in Insect Immunity.
  216. (1999). protein.
  217. (1988). Purification of a beta-1, 3-glucan recognition protein in the prophenoloxidase activating system from hemolymph of the silkworm, Bombyx mori.
  218. (2003). Rapid phagocytosis and melanisation of bacteria and Plasmodium sporozoites by hemocytes of the mosquio Aedes aegypti.
  219. (1990). Red Queen hypothesis supported by parasitism in sexual and clonal fish.
  220. (2003). Regulation of JAK-STAT signalling in the immune system.
  221. (2007). Relish regulates expression of antimicrobial peptide genes in the honeybee, Apis mellifera, shown by RNA interference.
  222. (1999). Relish, a central factor in the control of humoral but not cellular immunity in Drosophila.
  223. (2005). Requirements of peptidoglycan structure that allow detection by the Drosophila Toll pathway.
  224. (2007). Rhodnius prolixus: Identification of immune-related genes up-regulated in response to pathogens and parasites using suppressive subtractive hybridization.
  225. (1998). Role of the prophenoloxidase-activating system in invertebrate immunity.
  226. (2006). Self-harm caused by an insect's innate immunity.
  227. (2008). Semaphorins and their receptors in immune cell interactions.
  228. (2006). Sensing of Gram-positive bacteria in Drosophila: GNBP1 is needed to process and present peptidoglycan to PGRP-SA.
  229. (2002). Sequential activation of signaling pathways during innate immune responses in Drosophila.
  230. (1990). Sexual reproduction as an adaptation to resist parasites (a review).
  231. (1994). Shared use of flowers leads to horizontal pathogen transmission.
  232. (1998). Shrimp plasma HDL and β-glucan binding protein (BGBP): comparison of biochemical characteristics.
  233. (2004). Sialoglycans in protozoal diseases: their detection, modes of acquisition and emerging biological roles.
  234. (2009). Sialoglycoconjugates in Herpetomonas megaseliae: role in the adhesion to insect host epithelial cells.
  235. (2003). Signaling role of hemocytes in Drosophila JAK/STATdependent response to septic injury.
  236. (1995). Stage-specific binding of Leishmania donovani to the sand fly vector midgut is regulated by conformational changes in the abundant surface lipophosphoglycan.
  237. (2004). Stochastic yet biased expression of multiple Dscam splice variants by individual cells.
  238. (2008). Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum.
  239. (2003). Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory.
  240. (2007). Structural basis of Dscam isoform specificity.
  241. (1995). Structural organization of the cell surface of pathogenic protozoa.
  242. (2001). Structure of two FREP genes that combine IgSF and fibrinogen domains, with comments on diversity of the FREP gene family in the snail Biomphalaria glabrata.
  243. (2008). Studying immunity at the whole organism level.
  244. (1996). Suppression subtractive hybridization: A method for generating differentially regulated or tissue-specific cDNA probes and libraries.
  245. (2005). Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: Individual variation and fitness consequences.
  246. (2000). Survival for immunity: The price of immune system activation for bumblebee workers.
  247. (2003). Tamo selectively modulates nuclear import in Drosophila. Genes to Cells,
  248. (2001). The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding.
  249. (2000). The cause of parasitic infection in natural populations of Daphnia (Crustacea : Cladocera): the role of host genetics.
  250. (2004). The distribution of genotypes of the trypanosome parasite, Crithidia bombi, in populations of its host, Bombus terrestris.
  251. (1996). The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults.
  252. (2003). The Drosophila immune system detects bacteria through specific peptidoglycan recognition.
  253. (2007). The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections.
  254. (2008). The Dscam homologue of the crustacean Daphnia is diversified by alternative splicing like in insects.
  255. (2008). The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage.
  256. (2008). The evolution of TEP1, an exceptionally polymorphic immunity gene in Anopheles gambiae.
  257. (2000). The evolutionary ecology of resistance to parasitoids by Drosophila.
  258. (2003). The FREP gene family in the snail Biomphalaria glabrata: additional members, and evidence consistent with alternative splicing and FREP retrosequences.
  259. (2007). The Host Defense of Drosophila melanogaster.
  260. (1993). The marine snail, Cerithidea californica, matures at smaller sizes where parasitism is high.
  261. (2004). The organisation and evolution of the Dipteran and Hymeopteran Down syndrome cell adhesion molecule (Dscam) genes.
  262. (2000). The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response.
  263. (2004). The prophenoloxidase-activating system in invertebrates.
  264. (2008). The proPO-system: pros and cons for its role in invertebrate immunity.
  265. (2009). The role of ecological feedbacks in the evolution of host defence: what does theory tell us?
  266. (2003). The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae.
  267. (2004). The roles of JAK/STAT signaling in Drosophila immune responses. Immunological Reviews,
  268. (1999). The roles of Sarcophaga defense molecules in immunity and metamorphosis.
  269. (2008). The stimulation of immune defence accelerates development in the red flour beetle (Tribolium castaneum).
  270. (2001). The TNF and TNF receptor superfamilies integrating mammalian biology.
  271. (2006). The ubiquitous gp63-like metalloprotease from lower trypanosomatids: in the search for a function. Anais da Academia Brasileira de
  272. (2004). Thioester-containing proteins and insect immunity.
  273. (2000). Tissuespecific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia.
  274. (1999). Toll receptor-mediated Drosophila immune response requires Dif, an NF-κB factor.
  275. (2003). Toll-like receptormediated tyrosine phosphorylation of paxillin via MyD88-dependent and -independent pathways.
  276. (2006). Tracking the evolution of alternatively spliced exons within the Dscam family.
  277. (1997). Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster.
  278. (2005). Trans-generational immune priming in a social insect.
  279. (2004). Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae.
  280. (1993). Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects.
  281. (2008). Trypanocidal and leishmanicidal activities of different antimicrobial peptides (AMPs) isolated from aquatic animals.
  282. (2001). Tsetse immune responses and trypanosome transmission: Implications for the development of tsetse-based strategies to reduce trypanosomiasis.
  283. (2007). Variation and Heritability in Immune Gene Expression by Diseased Honeybees.
  284. (2005). Virulence and competitive ability in genetically diverse malaria infections.
  285. (2006). Within-host dynamics of an intestinal pathogen of bumble bees.
  286. (2004). β-1, 3-Glucan recognition protein2 (βGRP-2) from Manduca sexta: an acute-phase protein that binds β-1, 3-glucan and lipoteichoic acid to aggregate fungi and bacteria and stimulate prophenoloxidase activation.

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