The role of a novel Wo l b a c h i a (Rickettsiales: Anaplasmataceae) synthetic peptide, WolFar, in regulating prostaglandin levels in the hemolymph of Acheta domesticus (Orthoptera: Gryllidae)
Prostaglandins and other eicosanoids are known as regulating agents for cellular immune responses to pathogen threats in an insect?s hemolymph. A novel synthetic peptide, WolFar, was customized from a conserved region of the Wolbachia surface protein (WSP), isolated from an economically important endoparasitoid species, Fopius arisanus. WolFar consists of nine amino acids (SYY VRL QYN) and was tested on the house cricket, Acheta domesticus. Three concentrations of peptides, 0.83 mmol/L (100%), 0.63 mmol/L (75%), and 0.42 mmol/L (50%), were injected and observed for 72 h. The regulation of prostaglandin E2 (PGE2) in the hemolymph of A. domesticus was determined using ELISA and by observation of nodules in the internal system of A. domesticus. The results showed that there were significant increases in PGE2 in response to peptide injection at 24, 48, and 72 h after treatment. Furthermore, higher concentrations of peptide were directly proportional to the level of PGE2 activity. These findings were supported by the abundance of nodules that formed in the internal system and fat body of A. domesticus, detectable at 72 h into the treatment. This indicates that WolFar is able to stimulate the immune system of insects and can be further developed as a potential biopesticide.
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- Adamo SA (1999). Evidence for adaptive changes in egg laying in
crickets exposed to bacteria and parasites. Anim Behav 57:
117-124.
- Asgharian H, Chang PL, Mazzoglio PJ, Negri I (2014).
Wolbachia
is not all about sex: male-feminizing
Wolbachia
alters the
leafhopper
Zyginidia pullula
transcriptome in a mainly sex-
independent manner. Front Microbiol 5: 430.
- Azad AF, Beard CB (1998). Rickettsial pathogens and their arthropod
vectors. Emerg Infect Diseases 4: 179.
- Bali GK, Kaur S (2013). Phenoloxidase activity in haemolymph of
Spodoptera litura
(Fabricius) mediating immune responses
challenge with entomopathogenic fungus,
Beauveria bassiana
(Balsamo) Vuillmin. J Entomol Zool Stud 1: 118-123.
- Baldo L, Lo N, Werren JH (2005). Mosaic nature of the Wolbachia
surface protein. J Bacteriol 187: 5406-5418.
- Bazzocchi C, Ceciliani F, McCall JW, Ricci I, Genchi C, Bandi C (2000).
Antigenic role of the endosymbionts of filarial nematodes: IgG
response against the
Wolbachia
surface protein in cats infected
with
Dirofilaria immitis
. Proc R Soc Lond B Biol Sci 267: 2511-
2516.
- Billingsley PF, Lehane MJ (1996). Structure and ultrastructure of the
insect midgut. In: Billingsley P, Lehane MJ, editors. Biology of
the Insect Midgut. Berlin, Germany: Springer, pp. 3-30.
- Bordenstein SR, Werren JH (2007). Bidirectional incompatibility
among divergent
Wolbachia
and incompatibility level differences
among closely related
Wolbachia
in
Nasonia
. Heredity 99: 278.
- Braig HR, Zhou W, Dobson SL, O’Neill SL (1998). Cloning and
characterization of a gene encoding the major surface protein
of the bacterial endosymbiont
Wolbachia pipientis
. J Bacteriol
180: 2373-2378.
- Brattig NW, Bazzocchi C, Kirschning CJ, Reiling N, Büttner DW,
Ceciliani F, Geisinger F, Hochrein H, Ernst M, Wagner H et al.
(2004). The major surface protein of
Wolbachia
endosymbionts
in filarial nematodes elicits immune responses through TLR2
and TLR4. J Immunol 173:437-445.
- Brattig NW, Rathjens U, Ernst M, Geisinger F, Renz A, Tischendorf
FW (2000). Lipopolysaccharide-like molecules derived from
Wolbachia
endobacteria of the filaria
Onchocerca volvulus
are candidate mediators in the sequence of inflammatory and
antiinflammatory responses of human monocytes. Microbes
Infect 2: 1147-1157.
- Brelsfoard CL, Dobson SL (2009).
Wolbachia
-based strategies to
control insect pests and disease vectors. Asia Pac J Mol Biol
Biotechnol 17: 55-63.
- Bulet P, Cociancich S, Dimarcq JL, Lambert J, Reichhart JM, Hoffmann
D, Hetru C, Hoffmann JA (1991). Insect immunity. Isolation
from a coleopteran insect of a novel inducible antibacterial
peptide and of new members of the insect defensin family. J Biol
Chem 266: 24520-24525.
- Büyükgüzel E (2012). Eicosanoids mediate cellular immune response
and phenoloxidase reaction to viral infection in adult
Pimpla
turionellae
. Arch Insect Biochem Physiol 81: 20-33.
- Büyükgüzel E, Tunaz H, Stanley D, Büyükgüzel K (2007). Eicosanoids
mediate
Galleria mellonella
cellular immune response to viral
infection. J Insect Physiol 53: 99-105.
- Cherng JY, Liu CC, Shen CR, Lin HH, Shih MF (2010) Beneficial effects
of
Chlorella
-11 peptide on blocking LPS-induced macrophage
activation and alleviating thermal injury-induced inflammation
in rats. Int J Immunopathol Pharmacol 23: 811-820.
- Clifford CW, Woodring JP (1990). Methods for rearing the house
cricket,
Acheta domesticus
(L.), along with baseline values
for feeding rates, growth rates, development times, and blood
composition. J Appl Entomol 109: 1-14.
- Clifford CW, Roe RM, Woodring JP (1977). Rearing methods for
obtaining house crickets,
Acheta domesticus
, of known age, sex,
and instar. Ann Entomol Soc Am 70: 69-74.
- Cytryńska M, Zdybicka-Barabas A, Jakubowicz T (2006). Studies on
the role of protein kinase A in humoral immune response of
Galleria mellonella
larvae. J Insect Physiol 52: 744-753.
- Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, Nazzi F,
Gargiulo G, Pennacchio F (2013). Neonicotinoid clothianidin
adversely affects insect immunity and promotes replication of a
viral pathogen in honey bees. P Natl Acad Sci USA 110: 18466-
18471.
- Dorrah MA (2009). Phenoloxidase and lysozyme activity in naive
and immune-responsive larvae
Parasarcophaga hertipes
.
EFFlatounia 9: 10-17.
- Ebrahimi L, Niknam G, Dunphy GB, Toorchi M (2014). Side effects
of immune response of Colorado potato beetle,
Leptinotarsa
decemlineata
against the entomopathogenic nematode,
Steinernema carpocapsae
infection. Invert Surviv J 11: 132-142.
- Eleftherianos I, Xu M, Yadi H, Reynolds SE (2009). Plasmatocyte-
spreading peptide (PSP) plays a central role in insect cellular
immune defenses against bacterial infection. J Exp Biol 212:
1840-1848.
- Fang Q, Wang L, Zhu J, Li Y, Song Q, Stanley DW, Akhtar ZR, Ye G
(2010). Expression of immune-response genes in lepidopteran
host is suppressed by venom from an endoparasitoid,
Pteromalus puparum
. BMC Genomics 11: 484.
- Flores-Villegas AL, Cabrera-Bravo M, Toriello C, Bucio-Torres MI,
Salazar-Schettino PM, Córdoba-Aguilar A (2016). Survival and
immune response of the Chagas vector
Meccus pallidipennis
(Hemiptera: Reduviidae) against two entomopathogenic
fungi,
Metarhizium anisopliae
and
Isaria fumosorosea
. Parasit
Vectors 9: 176.
- Fruttero LL, Moyetta NR, Uberti AF, Grahl MVC, Lopes FC, Broll
V, Feder D, Carlini CR (2016). Humoral and cellular immune
responses induced by the urease-derived peptide Jaburetox in
the model organism
Rhodnius prolixus
. Parasit Vectors 9: 412.
- Fu G, Lees RS, Nimmo D, Aw D, Jin L, Gray P, Berendonk TU, White-
Cooper H, Scaife S, Phuc HK et al. (2010). Female-specific
flightless phenotype for mosquito control. P Natl Acad Sci
USA 107: 4550-4554.
- Gandhe AS, John SH, Nagaraju J (2007). Noduler, a novel immune
up-regulated protein mediates nodulation response in insects. J
Immunol 179: 6943-6951.
- Hallem EA, Dillman AR, Hong AV, Zhang Y, Yano JM, DeMarco
SF, Sternberg PW (2011). A sensory code for host seeking in
parasitic nematodes. Curr Biol 21: 377-383.
- Hardy MC, Daly NL, Mobli M, Morales RA, King GF (2013).
Isolation of an orally active insecticidal toxin from the venom
of an Australian tarantula. PLoS One 8: e73136.
- Ishii K, Hamamoto H, Kamimura M, Nakamura Y, Noda H, Imamura
K, Mita K, Sekimizu K (2010). Insect cytokine paralytic peptide
(PP) induces cellular and humoral immune responses in the
silkworm
Bombyx mori
. J Biol Chem 285: 28635-28642.
- Johnson KN (2015). The impact of
Wolbachia
on virus infection in
mosquitoes. Viruses 7: 5705-5717.
- Joubert DA, O’Neill SL (2017). Comparison of stable and transient
Wolbachia
infection models in
Aedes aegypti
to block dengue
and West Nile viruses. PLoS Negl Trop Dis 11: e0005275.
- Jurenka RA, Miller JS, Pedibhotla VK, Rana RL, Stanley-Samuelson D
(1997). Eicosanoids mediate microaggregation and nodulation
responses to bacterial infections in black cutworms,
Agrotis
ipsilon
, and true armyworms,
Pseudaletia unipuncta
. J Insect
Physiol 43: 125-133.
- Jurenka RA, Pedibhotla VK, Stanley DW (1999). Prostaglandin
production in response to a bacterial infection in true armyworm
larvae. Arch Insect Biochem Physiol 41: 225-232.
- La Fauce K, Owens L (2013). Suppression of
Penaeus merguiensis
densovirus following oral delivery of live bacteria expressing
dsRNA in the house cricket (
Acheta domesticus
) model. J
Invertebr Pathol 112: 162-165.
- Lee S, Peterson CJ, Coats JR (2003). Fumigation toxicity of
monoterpenoids to several stored product insects. J Stored Prod
Res 39: 77-85.
- Lemaitre B, Hoffmann J (2007). The host defense of
Drosophila
melanogaster
. Annu Rev Immunol 25: 697-743.
- Liu K, Li Y, Jousset FX, Zadori Z, Szelei J, Yu Q, Pham HT, Lépine F,
Bergoin M, Tijssen P (2011). The
Acheta domesticus
densovirus,
isolated from the European house cricket, has evolved an
expression strategy unique among parvoviruses. J Virol 85:
10069-10078.
- Mandato CA, Diehl-Jones WL, Moore SJ, Downer RG (1997).
The effects of eicosanoid biosynthesis inhibitors on
prophenoloxidase activation, phagocytosis and cell spreading in
Galleria mellonella
. J Insect Physiol 43: 1-8.
- McFarlane JE, Distler MHW (1982). The effect of rutin on growth,
fecundity and food utilization in
Acheta domesticus
(L.). J Insect
Physiol 28: 85-88.
- Mohammed MA, Aman‐Zuki A, Yusof S, Md‐Zain BM, Yaakop S
(2017). Prevalence and evolutionary history of endosymbiont
Wolbachia
(Rickettsiales: Anaplasmataceae) in parasitoids
(Hymenoptera: Braconidae) associated with
Bactrocera
fruit
flies (Diptera: Tephritidae) infesting carambola. Entomol Sci 20:
382-395.
- Nakagaki BJ, Defoliart GR (1991). Comparison of diets for mass-
rearing
Acheta domesticus
(Orthoptera: Gryllidae) as a novelty
food, and comparison of food conversion efficiency with values
reported for livestock. J Econ Entomol 84: 891-896.
- Park C, Kim SI, Ahn YJ (2003). Insecticidal activity of asarones
identified in
Acorus gramineus
rhizome against three coleopteran
stored-product insects. J Stored Prod Res 39: 333-342.
- Park S, Hahm KB, Oh TY, Jin JH, Choue R (2004). Preventive effect
of the flavonoid, wogonin, against ethanol-induced gastric
mucosal damage in rats. Dig Dis Sci 49: 384-394.
- Patton RL (1978). Growth and development parameters for
Acheta
domesticus
. Ann Entomol Soc Am 71: 40-42.
- Pinto SB, Mariconti M, Bazzocchi C, Bandi C, Sinkins SP (2012).
Wolbachia
surface protein induces innate immune responses in
mosquito cells. BMC Microbiol 12: 11.
- Rasgon JL (2012).
Wolbachia
induces male-specific mortality in the
mosquito
Culex pipiens
(LIN strain). PLoS One 7: e30381.
- Ryder JJ (2007). Temporal dynamics of the encapsulation response
towards a synthetic immune challenge in
Acheta domesticus
.
Physiol Entomol 32: 240-245.
- Saridaki A, Bourtzis K (2009).
Wolbachia
-induced reproductive
parasitism and applications. Entomol Hellenica 18: 3-16.
- Sheppard R (2003). The fluorenylmethoxycarbonyl group in solid
phase synthesis. J Pept Sci 9: 545-552.
- Silva CCD (2002). Activation of prophenoloxidase and removal of
Bacillus subtilis
from the hemolymph of
Acheta domesticus
(L.)
(Orthoptera: Gryllidae). Neotrop Entomol 31: 487-491.
- Simpson AJG, Reinach FC, Arruda P, Abreu FA, Acencio M,
Alvarenga R, Alves LC, Araya JE, Baia GS, Baptista CS et al.
(2000). The genome sequence of the plant pathogen
Xylella
fastidiosa
. Nature 406: 151-158.
- Srikanth K, Park J, Stanley DW, Kim Y (2011). Plasmatocyte‐spreading
peptide influences hemocyte behavior via eicosanoids. Arch
Insect Biochem Physiol 78: 145-160.
- Srygley RB, Jaronski ST (2011). Immune response of Mormon
crickets that survived infection by
Beauveria
bassiana
. Psyche
2011: 849038.
- Stanley D, Kim Y (2011). Prostaglandins and their receptors in insect
biology. Front Endocrinol 2: 105.
- Stanley D, Kim Y (2014). Eicosanoid signaling in insects: from
discovery to plant protection. CRC Crit Rev Plant Sci 33: 20-63.
- Stanley D, Haas E, Miller J (2012). Eicosanoids: exploiting insect
immunity to improve biological control programs. Insects 3:
492-510.
- Strand MR (2008). The insect cellular immune response. Insect
Sci 15: 1-14.
- Szelei J, Woodring J, Goettel MS, Duke G, Jousset FX, Liu KY, Zadori
Z, Li Y, Styer E, Boucias DG et al. (2011). Susceptibility of
North-American and European crickets to
Acheta domesticus
densovirus (AdDNV) and associated epizootics. J Invertebr
Pathol 106: 394-399.
- Tunaz H, Bedick JC, Miller JS, Hoback WW, Rana RL, Stanley
DW (1999). Eicosanoids mediate nodulation reactions to
bacterial infections in adults of two 17-year periodical cicadas,
Magicicada septendecim
and
M. cassini
. J Insect Physiol 45:
923-931.
- Turner JD, Langley RS, Johnston KL, Gentil K, Ford L, Wu B, Graham
M, Sharpley F, Slatko B, Pearlman E et al. (2009).
Wolbachia
lipoprotein stimulates innate and adaptive immunity through
Toll-like receptors 2 and 6 to induce disease manifestations of
filariasis. J Biol Chem 284: 22364-22378.
- Wang C, Leger RJS (2006). A collagenous protective coat enables
Metarhizium anisopliae
to evade insect immune responses. P
Natl Acad Sci USA 103: 6647-6652.
- Wang Y, Gaugler R, Cui L (1994). Variations in immune response
of
Popillia japonica
and
Acheta domesticus
to
Heterorhabditis
bacteriophora
and
Steinernema
species. J Nematol 26: 11.
- Watanabe M, Kageyama D, Miura K (2013). Transfer of a
parthenogenesis-inducing
Wolbachia
endosymbiont
derived from
Trichogramma dendrolimi
into
Trichogramma
evanescens
. J Invertebr Pathol 112: 83-87.
- Wigglesworth VB (1972). The Principles of Insect Physiology. Berlin,
Germany: Springer.
- Windley MJ, Herzig V, Dziemborowicz SA, Hardy MC, King
GF, Nicholson GM (2012). Spider-venom peptides as
bioinsecticides. Toxins 4: 191-227.
- Xi Z, Khoo CC, Dobson SL (2006). Interspecific transfer of
Wolbachia
into the mosquito disease vector
Aedes albopictus
. Proc Royal
Soc B 273: 1317-1322.
- Yokoyama A, Hamaguchi K, Ohtsu K, Ishihara S, Kobara Y,
Horio T, Endo S (2009). A method for mass-rearing
caddisfly,
Cheumatopsyche brevilineata
(Iwata) (Trichoptera:
Hydropsychidae), as a new test organism for assessing the
impact of insecticides on riverine insects. Appl Entomol Zool
44: 195-201.
- Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C, Savakis
C, Bourtzis K (2004).
Wolbachia
-induced cytoplasmic
incompatibility as a means for insect pest population control. P
Natl Acad Sci USA 101: 15042-15045.
- Zhao F, Stanley D, Wang Y, Zhu F, Lei CL (2009). Eicosanoids mediate
nodulation reactions to a mollicute bacterium in larvae of the
blowfly,
Chrysomya megacephala
. J Insect Physiol 55: 192-196.