Trade-off between immune stimulation and expression of storage protein genes

Archives of Insect Biochemistry and Physiology

Volumn 71, Issue 2, 2009, Pages 70-87

  Lourenĉo, Anete P ^a,b   Martins, Juliana R ^a   Bitondi, Márcia M G ^a   Simões, Zilá L P ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSIDADE FEDERAL DOS VALES DO JEQUITINHONHA E MUCURI   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPHORIN III; APOLIPOPROTEIN; CATECHOL OXIDASE; DEFENSIN; ENZYME PRECURSOR; INSECT PROTEIN; MESSENGER RNA; PRO PHENOLOXIDASE; PRO-PHENOLOXIDASE; RNA; STORAGE PROTEINS, INSECTA; VITELLOGENIN;

ANIMAL; ARTICLE; BACTERIAL INFECTION; BEE; COMPARATIVE STUDY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HEMOLYMPH; IMMUNOLOGY; METABOLISM; PHYSIOLOGICAL STRESS; SPECIES DIFFERENCE;

ANIMALS; APOLIPOPROTEINS; BACTERIAL INFECTIONS; BEES; CATECHOL OXIDASE; DEFENSINS; ENZYME PRECURSORS; FEMALE; GENE EXPRESSION REGULATION; HEMOLYMPH; INSECT PROTEINS; RNA; RNA, MESSENGER; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL; VITELLOGENINS;

APIS MELLIFERA; APOIDEA; BACTERIA (MICROORGANISMS); HEXAPODA;

EID: 67649743348     PISSN: 07394462     EISSN: 15206327     Source Type: Journal    
DOI: 10.1002/arch.20301     Document Type: Article

References (58)

1. Ahmed AM, Hurd H. 2006. Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes Infect 8:308-315.
2. Ahmed AM, Taylor P, Maingon R, Romans P, Hurd H. 2001. Effects of malaria infection on vitellogenesis in Anopheles gambiae during two gonotrophic cycles. Insect Mol Biol 10:347-356. Amdam GV, Simões ZLP, Hagen A, Norberg K, Schroder K, Mikkelsen O, Kirkwood TBL,
3. Omholt SW. 2004. Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp Gerontol 39:767-773.
4. Ashida M, Brey PT. 1998. Recent advances in research on the insect prophenoloxidase cascade. In: Brey PT, Hultmark D, editors. Molecular mechanisms of immune responses in insects. London: Chapman and Hall. p 135-172.
5. Baker ME. 1988. Invertebrate vitellogenin is homologous to human von Willebrand factor. Biochem J 256:1059-1063.
6. Beresford PJ, Basinski-Gray JM, Chiu JK, Chadwick JS, Aston WP. 1997. Characterization of hemolytic and cytotoxic Gallysins: a relationship with arylphorins. Dev Comp Immunol 21:253-266.
7. Bitondi MMG, Simões ZLP. 1996. The relationship between level of pollen in the diet, vitellogenin and juvenile hormone titers in Africanized Apis mellifera workers. J Apicult Res 35:27-36.
8. Braun RP, Wyatt GW. 1996. Sequence of the hexameric juvenile hormone-binding protein from the hemolymph of Locusta migratoria. J Biol Chem 6:31756-31762.
9. Bulet P, Hetru C, Dimarcq JL, Hoffmann D. 1999. Antimicrobial peptides in insects; structure and function. Dev Comp Immunol 23:329-344.
10. Burmester T. 1999. Evolution and function of the insect hexamerins. Eur J Entomol 96:213-225.
11. Casteels-Josson K, ZhangW, Capaci T, Casteels P, Tempst P. 1994. Acute transcriptional response of the honeybee peptide-antibiotics gene repertoire and required post-translational conversion of the precursor structures. J Biol Chem 296:28569-28575.
12. Cheon HM, Shin SW, Bian G, Park JH, Raikhel AS. 2006. Regulation of lipid metabolism genes, lipid carrier protein lipophorin, and its receptor during immune challenge in the mosquito Aedes aegypti. J Biol Chem 281:8426-8435. Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT,
13. Collins FH, Danielli A, Dimopoulos G, Hetru C, Hoa NT, Hoffmann JA, Kanzok SM, Letunic I, Levashina EA, Loukeris TG, Lycett G, Meister S, Michel K, Moita LF, Müller HM, Osta MA, Paskewitz SM, Reichhart JM, Rzhetsky A, Troxler L, Vernick KD, Vlachou D, Volz J, von Mering C, Xu J, Zheng L, Bork P, Kafatos FC. 2002. Immunity-related genes and gene families in Anopheles gambiae. Science 298:159-165.
14. Cociancich S, Ghazi A, Hetru C, Hoffmann JA, Letellier L. 1993. Insect defensin, an inducible antibacterial peptide, forms voltage dependent channels in Micrococcus luteus. J Biol Chem 268:19239-19245.
15. Danty E, Arnold G, Burmester T, Huet JC, Huet D, Pernollet JC, Masson C. 1998. Identification and developmental profiles of hexamerins in antenna and hemolymph of the honeybee, Apis mellifera. Insect Biochem Mol Biol 28:387-397.
16. Engels W, Kaatz H, Zillikens A, Simões ZLP, Trube A, Braun R, Dittrich F. 1990. Honey bee reproduction: vitellogenin and caste-specific regulation of fertility. Adv Inv Reprod 5:495-502.
17. Evans JD, Aronstein K, Chen YP, Hetru C, Imler J-L, Jiang H, Kanost M, Thompson G, Zhou C, Hultmark D. 2006. Immune pathways and defense mechanisms in honey bees, Apis mellifera. Insect Mol Biol 15:645-656.
18. Guidugli KR, Piulachs MD, Belles X, Lourenc-o AP, Simões ZL. 2005. Vitellogenin expression in queen ovaries and in larvae of both sexes of Apis mellifera. Arch Insect Biochem Physiol 59:211-218.
19. Guntur KVP, Velasquez D, Chadwell L, Carroll C, Weintraub S, Cassill JA, Renthal R. 2004. Apolipophorin-III-like protein expressed in the antenna of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). Arch Insect Biochem Physiol 57:101-110.
20. Hall M, Wang R, Van Antwerpen R, Sottrup-Jensen L, Soderhall K. 1999. The crayfish plasma clotting protein: a vitellogenin-related protein responsible for clot formation in crustacean blood. Proc Natl Acad Sci USA 96:1965-1970.
21. Halwani AE, Niven DF, Dunphy GB. 2000. Apolipophorin-III and the interactions of lipoteichoic acids with the immediate immune responses of Galleria mellonella. J Invertebr Pathol 76:233-241.
22. Hetru C, Hoffmann D, Bulet P. 1998. Antimicrobial peptides from insects. In: Brey PT, Hultmark D, editors. Molecular mechanisms of immune responses in insects. London: Chapman and Hall. p 40-66.
23. Hultmark D. 1993. Immune reactions in Drosophila and other insects: a model for innate immunity. Trends Genet 9:178-183.
24. Kato Y, Motoi Y, Taniai K, Kadonookuda K, Yamamoto M, Higashino Y, Shimabukuro M, Chowdhury S, Xu J, Sugiyama M, Hiramatsu M, Yamakawa, M. 1994. Lipopolysaccharidelipophorin complex formation in insect hemolymph: a common pathway of lipopolysaccharide detoxification both in insects and in mammals. Insect Biochem Mol Biol 24:547-555.
25. Kim HJ, Je HJ, Park SY, Lee IH, Jin BR, Yun HK, Yun CY, Han YS, Kang YJ, Seo SJ. 2004. Immune activation of apolipophorin-III and its distribution in hemocytes from Hyphantria cunea. Insect Biochem Mol Biol 34:1011-1023.
26. Klaudiny J, Albert S, Bachanova K, Kopernicky J, Simuth J. 2005. Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee Apis mellifera. Insect Biochem Mol Biol 35:11-22.
27. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
28. Lemaitre B, Hoffmann J. 2007. The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697-743.
29. Lourenc-o AP, Zufelato MS, Bitondi MMG, Simões ZLP. 2005. Molecular characterization of a cDNA encoding the prophenoloxidase and its expression in Apis mellifera. Insect Biochem Mol Biol 35:541-552.
30. Lourenc-o AP, Mackert A, Cristino A dos S, Simões ZLP. 2008. Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie 39:372-385.
31. Ma G, Hay D, Li D, Asgari S, Schmidt O. 2006. Recognition and inactivation of LPS by lipophorin particles. Dev Comp Immunol 30:619-626.
32. Magee J, Kraynack N, Massey Jr HC, Telfer WH. 1994. Properties and significance of a riboflavin-binding hexamerin in the hemolymph of Hyalophora cecropia. Arch Insect Biochem Physiol 25:137-157.
33. Martins JR, Nunes FM, Simões ZLP, Bitondi MMG. 2008. A honeybee storage protein gene, hex 70a, expressed in developing gonads and nutritionally regulated in adult fat body. J Insect Physiol 54:867-877.
34. Mason HS. 1965. Oxidases. Ann Rev Biochem 34:595-634.
35. Pan ML, Telfer H. 1999. Equivalence of riboflavin-binding hexamerin and arylphorin as reserves for adult development in two saturniid moths. Arch Insect Biochem Physiol 42:138-146.
36. Peter MG, Scheller K. 1991. The physiology of insect epidermis. In: Retnakaran A, Binnington K, editors. North Carolina, Australia: Inkata Press. p 115-124.
37. Robbs SL, Ryan RO, Schmidt JO, Keim PS, Law JH. 1985. Lipophorin of the larval honeybee, Apis mellifera L. J Lipid Res 26:241-247.
38. Rodenburg KW, Van der Horst DJ. 2005. Lipoprotein-mediated lipid transport in insects: analogy to the mammalian lipid carrier system and novel concepts for the functioning of LDL receptor family members. Biochim Biophys Acta 1736:10-29.
39. Scharlaken B, de Graaf DC, Memmi S, Devreese B, Van Beeumen J, Jacobs FJ. 2007. Differential protein expression in the honey bee head after a bacterial challenge. Arch Insect Biochem Physiol 65:223-237.
40. Scharlaken B, de Graaf DC, Goossens K, Peelman LJ, Jacobs FJ. 2008. Differential gene expression in the honeybee head after a bacterial challenge. Dev Comp Immunol 32: 883-889.
41. Scherfer C, Karlsson C, Loseva O, Bidla G, Goto A, Havemann J, Dushay MS, Theopold U. 2004. Isolation and characterization of hemolymph clotting factors in Drosophila melanogaster by a pullout method. Curr Biol 14:625-629.
42. Schmid-Hempel P. 2005. Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50:529-551.
43. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. 1985. Measurement of protein using bicinchoninic acid. Anal Biochem 150:76-85.
44. Söderhäll K, Cerenius L. 1998. Role of prophenoloxidase- activating system in invertebrate immunity. Curr Op Immunol 10:23-28.
45. Strand MR. 2008. The insect cellular immune response. Insect Science 15:1-14.
46. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599.
47. Telfer WH, Kunkel JG. 1991. The function and evolution of insect storage hexamers. Ann Rev Entomol 36:205-228.
48. Theopold U, Li D, Fabbri M, Scherfer C, Schmidt O. 2002. The coagulation of insect hemolymph. Cell Mol Life Sci 59:363-372.
49. Theopold U, Schmidt O, Söderhäll K, Dushay MS. 2004. Coagulation in arthropods: defence, wound closure and healing. Trends Immunol 25:289-294.
50. Vilcinskas A, Kopacek P, Jegorov A, Vey A, Matha V. 1997. Detection of lipophorin as the major cyclosporine-binding protein in the hemolymph of the greater wax moth Galleria mellonella. Comp Biochem Physiol-C Comp Pharm Toxi 117:41-45.
51. Weers PMM, Ryan RO. 2003. Apolipophorin III: a lipid-triggered molecular switch. Insect Biochem Mol Biol 33:1249-1260.
52. Weers PMM, Ryan RO. 2006. Apolipophorin III: role model apolipoprotein. Insect Biochem Mol Biol 36:231-240.
53. Whitten MMA, Tew IF, Lee BL, Ratcliffe NA. 2004. A novel role for an insect apolipoprotein (apolipophorin III) in beta-1,3-glucan pattern recognition and cellular encapsulation reactions. J Immunol 172:2177-2185.
54. Wiesner A, Losen S, Kopa'cek P, Gotz P. 1997. Isolated apolipophorin III from Galleria mellonella stimulates the immune reactions of this insect. J Insect Physiol 43:383-391.
55. Yamauchi H. 2001. Two novel insect defensins from larvae of the cupreous chafer, Anomala cuprea: purification, amino acid sequences and antibacterial activity. Insect Biochem Mol Biol 32:75-78.
56. Zerofsky M, Harel E, Silverman N, Tatar M. 2005. Aging of the innate immune response in Drosophila melanogaster. Aging Cell 4:103-108.
57. Zhou XG, Oi FM, Scharf ME. 2006. Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc Natl Acad Sci USA 103:4499-4504.
58. Zou Z, Lopez DL, Kanost MR, Evans JD, Jiang H. 2006. Comparative analysis of serine proteaserelated genes in the honey bee genome: possible involvement in embryonic development and innate immunity. Insect Mol Biol 15:603-614.