Ingested human insulin inhibits the mosquito NF-κB-dependent immune response to Plasmodium falciparum

Infection and Immunity

Volumn 80, Issue 6, 2012, Pages 2141-2149

  Pakpour, Nazzy ^a   Corby Harris, Vanessa ^b   Green, Gabriel P ^a   Smithers, Hannah M ^a   Cheung, Kong W ^a   Riehle, Michael A ^c   Luckhart, Shirley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CARL HAYDEN BEE RESEARCH CENTER   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN INSULIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; SOMATOMEDIN C; INSULIN; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ARTICLE; EMBRYO; ENZYME ACTIVATION; GENE EXPRESSION; IMMUNE RESPONSE; INNATE IMMUNITY; MALARIA; MOSQUITO; NONHUMAN; PARASITE DEVELOPMENT; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; ANOPHELES; CELL CULTURE; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PROMOTER REGION;

ANIMALS; ANOPHELES; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INSULIN; LIPOPOLYSACCHARIDES; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; PLASMODIUM FALCIPARUM; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION;

EID: 85047687055     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00024-12     Document Type: Article

References (59)

1. Ananieva O, et al. 2008. The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat. Immunol. 9:1028 -1036.
2. Barillas-Mury C, et al. 1996. Immune factor Gambif1,x a new rel family member from the human malaria vector,x Anopheles gambiae. EMBO J. 15:4691- 4701.
3. Bayne AC, Mockett RJ, Orr WC, Sohal RS. 2005. Enhanced catabolism of mitochondrial superoxide/hydrogen peroxide and aging in transgenic Drosophila. Biochem. J. 391:277-284.
4. 2020 Reference deleted
5. Cantley LC. 2002. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657.
6. Cargnello M, Roux PP. 2011. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75:50-83.
7. Christophides GK, et al. 2002. Immunity-related genes and gene families in Anopheles gambiae. Science 298:159 -165.
8. Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G. 2010. Mosquito immune defenses against Plasmodium infection. Dev. Comp. Immunol. 34:387-395.
9. Corby-Harris V, et al. 2010. Activation of Akt signaling reduces the prevalence and intensity of malaria parasite infection and lifespan in Anopheles stephensi mosquitoes. PLoS Pathog. 6:e1001003.
10. Cuschieri J, Bulger E, Grinsell R, Garcia I, Maier RV. 2008. Insulin regulates macrophage activation through activin A. Shock 29:285-290.
11. Dandona P, et al. 2001. Insulin inhibits intranuclear nuclear factor κB and stimulates IκB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect? J. Clin. Endocrinol. Metab. 86:3257-3265.
12. 2020 Reference deleted
13. Darby SM, Miller ML, Allen RO, LeBeau M. 2001. A mass spectrometric method for quantitation of intact insulin in blood samples. J. Anal. Toxicol. 25:8 -14.
14. DeVeale B, Brummel T, Seroude L. 2004. Immunity and aging: the enemy within? Aging Cell 3:195-208.
15. DiAngelo JR, Bland ML, Bambina S, Cherry S, Birnbaum MJ. 2009. The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc. Natl. Acad. Sci. U. S. A. 106:20853- 20858.
16. Dionne MS, Pham LN, Shirasu-Hiza M, Schneider DS. 2006. Akt and FOXO dysregulation contribute to infection-induced wasting in Drosophila. Curr. Biol. 16:1977-1985.
17. Dionne MS, Schneider DS. 2008. Models of infectious diseases in the fruit fly Drosophila melanogaster. Dis. Model Mech. 1:43- 49.
18. Dong Y, et al. 2006. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog. 2:e52.
19. Franke TF. 2008. PI3K/Akt: getting it right matters. Oncogene 27:6473- 6488.
20. Frolet C, Thoma M, Blandin S, Hoffmann JA, Levashina EA. 2006. Boosting NF-κB-dependent basal immunity of Anopheles gambiae aborts development of Plasmodium berghei. Immunity 25:677- 685.
21. Fukao T, Koyasu S. 2003. PI3K and negative regulation of TLR signaling. Trends Immunol. 24:358 -363.
22. Fukao T, et al. 2002. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat. Immunol. 3:875- 881.
23. Garver LS, Dong Y, Dimopoulos G. 2009. Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog. 5:e1000335.
24. Guha M, Mackman N. 2002. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277:32124 -32132.
25. Hillyer JF, Estevez-Lao TY. 2010. Nitric oxide is an essential component of the hemocyte-mediated mosquito immune response against bacteria. Dev. Comp. Immunol. 34:141-149.
26. Horton AA, et al. 2011. The mitogen-activated protein kinome from Anopheles gambiae: identification, phylogeny and functional characterization of the ERK, JNK and p38 MAP kinases. BMC Genomics 12:574.
27. Imler JL, Zheng L. 2004. Biology of Toll receptors: lessons from insects and mammals. J. Leukoc. Biol. 75:18 -26.
28. Iwasaki Y, et al. 2009. Insulin exhibits short-term anti-inflammatory but long-term proinflammatory effects in vitro. Mol. Cell Endocrinol. 298: 25-32.
29. Jeschke MG, Klein D, Herndon DN. 2004. Insulin treatment improves the systemic inflammatory reaction to severe trauma. Ann. Surg. 239:553- 560.
30. 2020 Reference deleted
31. Kang MA, Mott TM, Tapley EC, Lewis EE, Luckhart S. 2008. Insulin regulates aging and oxidative stress in Anopheles stephensi. J. Exp. Biol. 211:741-748.
32. Karl S, Davis TM, St Pierre TG. 2010. Parameterization of high magnetic field gradient fractionation columns for applications with Plasmodium falciparum infected human erythrocytes. Malaria J. 9:116.
33. Kim CC, Wilson EB, DeRisi JL. 2010. Improved methods for magnetic purification of malaria parasites and haemozoin. Malaria J. 9:17.
34. Reference deleted
35. Lambros C, Vanderberg JP. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65:418-420.
36. Leffler M, et al. 2007. Insulin attenuates apoptosis and exerts antiinflammatory effects in endotoxemic human macrophages. J. Surg. Res. 143:398-406.
37. Lim J, Gowda DC, Krishnegowda G, Luckhart S. 2005. Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite glycosylphosphatidylinositols. Infect. Immun. 73:2778 -2789.
38. Luckhart S, Riehle MA. 2007. The insulin signaling cascade from nematodes to mammals: insights into innate immunity of Anopheles mosquitoes to malaria parasite infection. Dev. Comp. Immunol. 31:647- 656.
39. Luna C, et al. 2006. Expression of immune responsive genes in cell lines from two different anopheline species. Insect Mol. Biol. 15:721-729.
40. Meister S, et al. 2005. Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc. Natl. Acad. Sci. U. S. A. 102:11420 -11425.
41. Meredith JM, et al. 2006. A novel association between clustered NF-κB and C/EBP binding sites is required for immune regulation of mosquito Defensin genes. Insect Mol. Biol. 15:393- 401.
42. Moret Y, Schmid-Hempel P. 2000. Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166- 1168.
43. Pakpour N, Cheung KW, Souvannaseng L, Concordet JP, Luckhart S. 2010. Transfection and mutagenesis of target genes in mosquito cells by locked nucleic acid-modified oligonucleotides. J. Vis. Exp. pii:e2355.
44. 2020 Reference deleted
45. Richman AM, Dimopoulos G, Seeley D, Kafatos FC. 1997. Plasmodium activates the innate immune response of Anopheles gambiae mosquitoes. EMBO J. 16:6114-6119.
46. Schmid-Hempel P. 2005. Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50:529 -551.
47. Schmid-Hempel P. 2005. Natural insect host-parasite systems show immune priming and specificity: puzzles to be solved. Bioessays 27:1026- 1034.
48. Sinden RE. 1999. Plasmodium differentiation in the mosquito. Parasitologia 41:139 -148.
49. Son MH, Kang KW, Lee CH, Kim SG. 2001. Potentiation of cadmiuminduced cytotoxicity by sulfur amino acid deprivation through activation of extracellular signal-regulated kinase1/2 (ERK1/2) in conjunction with p38 kinase or c-jun N-terminal kinase (JNK): complete inhibition of the potentiated toxicity by U0126 an ERK1/2 and p38 kinase inhibitor. Biochem. Pharmacol. 62:1379 -1390.
50. Surachetpong W, Pakpour N, Cheung KW, Luckhart S. 2011. Reactive oxygen species-dependent cell signaling regulates the mosquito immune response to Plasmodium falciparum. Antioxid. Redox Signal. 14:943-955.
51. Surachetpong W, Singh N, Cheung KW, Luckhart S. 2009. MAPK ERK signaling regulates the TGF- 1-dependent mosquito response to Plasmodium falciparum. PLoS Pathog. 5:e1000366.
52. Traore K, Sharma RB, Burek CL, Trush MA. 2007. Role of ROS and MAPK in TPA-induced ICAM-1 expression in the myeloid ML-1 cell line. J. Cell Biochem. 100:1010 -1021.
53. Unwin N, Gan D, Whiting D. 2010. The IDF Diabetes Atlas: providing evidence, raising awareness, and promoting action. Diabetes Res. Clin. Pract. 87:2-3.
54. Vaid A, Ranjan R, Smythe WA, Hoppe HC, Sharma P. 2010. PfPI3K, a phosphatidylinositol-3 kinase from Plasmodium falciparum, is exported to the host erythrocyte and is involved in hemoglobin trafficking. Blood 115:2500 -2507.
55. Vizioli J, et al. 2000. Cloning and analysis of a cecropin gene from the malaria vector mosquito, Anopheles gambiae. Insect Mol. Biol. 9:75- 84.
56. Vizioli J, et al. 2001. Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. U. S. A. 98:12630 -12635.
57. White NJ, et al. 1983. Severe hypoglycemia and hyperinsulinemia in falciparum malaria. N. Engl. J. Med. 309:61- 66.
58. Whitten MM, Shiao SH, Levashina EA. 2006. Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol. 28:121-130.
59. World Health Organization. 2008. World malaria report 2008. World Health Organization, Geneva, Switzerland.