Human IGF1 extends lifespan and enhances resistance to Plasmodium falciparum infection in the malaria vector Anopheles stephensi

Journal of Experimental Biology

Volumn 216, Issue 2, 2013, Pages 208-217

  Drexler, Anna ^a   Nuss, Andrew ^b   Hauck, Eric ^a   Glennon, Elizabeth ^a   Cheung, Kong ^a   Brown, Mark ^b   Luckhart, Shirley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Aging; Insulin; Insulin like growth factor; Mosquito; Signal transduction

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR; INSECT PROTEIN; INSULIN; PROTEIN KINASE B; SOMATOMEDIN C;

ANIMAL; ANOPHELES; ARTICLE; CELL LINE; DIGESTIVE SYSTEM; DISEASE CARRIER; DISEASE TRANSMISSION; ERYTHROCYTE; FEMALE; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; HUMAN; MALARIA; METABOLISM; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PLASMODIUM FALCIPARUM; SIGNAL TRANSDUCTION;

ANIMALS; ANOPHELES; CELL LINE; DIGESTIVE SYSTEM; ERYTHROCYTES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HOST-PARASITE INTERACTIONS; HUMANS; INSECT PROTEINS; INSECT VECTORS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; MALARIA; PLASMODIUM FALCIPARUM; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

ANOPHELES STEPHENSI; HEXAPODA; MAMMALIA; PLASMODIUM FALCIPARUM;

EID: 84871818057     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.078873     Document Type: Article

References (49)

1. Antonova, Y., Arik, A. J., Moore, W., Riehle, M. R. and Brown, M. R. (2012). Insulin-like peptides: structure, signaling, and function. In Insect Endocrinology (ed. L. I. Gilbert), pp. 63-92 Boston, MA: Academic Press.
2. Balendran, A., Currie, R., Armstrong, C. G., Avruch, J. and Alessi, D. R. (1999). Evidence that 3-phosphoinositide-dependent protein kinase-1 mediates phosphorylation of p70 S6 kinase in vivo at Thr-412 as well as Thr-252. J. Biol. Chem. 274, 37400-37406
3. Biteau, B., Karpac, J., Supoyo, S., Degennaro, M., Lehmann, R. and Jasper, H. (2010). Lifespan extension by preserving proliferative homeostasis in Drosophila. PLoS Genet. 6, e1001159.
4. Cargnello, M. and Roux, P. P. (2011). Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75, 50-83
5. Corby-Harris, V., Drexler, A., Watkins de Jong, L., Antonova, Y., Pakpour, N., Ziegler, R., Ramberg, F., Lewis, E. E., Brown, J. M., Luckhart, S. 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.
6. Crim, J. W., Garczynski, S. F. and Brown, M. R. (2002). Approaches to radioiodination of insect neuropeptides. Peptides 23, 2045-2051 (Pubitemid 35341614)
7. Darby, S. M., Miller, M. L., Allen, R. O. and LeBeau, M. (2001). A mass spectrometric method for quantitation of intact insulin in blood samples. J. Anal. Toxicol. 25, 8-14 (Pubitemid 32121093)
8. Elased, K. M. and Playfair, J. H. (1994). Hypoglycemia and hyperinsulinemia in rodent models of severe malaria infection. Infect. Immun. 62, 5157-5160 (Pubitemid 24332828)
9. Elased, K. M. and Playfair, J. H. (1996). Reversal of hypoglycaemia in murine malaria by drugs that inhibit insulin secretion. Parasitology 112, 515-521 (Pubitemid 26184529)
10. Giulivi, C., Ross-Inta, C., Horton, A. A. and Luckhart, S. (2008). Metabolic pathways in Anopheles stephensi mitochondria. Biochem. J. 415, 309-316
11. Gomes, C. M., Giannella-Neto, D., Gama, M. E., Pereira, J. C., Campos, M. B. and Corbett, C. E. (2007). Correlation between the components of the insulin-like growth factor I system, nutritional status and visceral leishmaniasis. Trans. R. Soc. Trop. Med. Hyg. 101, 660-667 (Pubitemid 46706151)
12. Grönke, S., Clarke, D. F., Broughton, S., Andrews, T. D. and Partridge, L. (2010). Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet. 6, e1000857.
13. Hansen, I. A., Attardo, G. M., Park, J. H., Peng, Q. and Raikhel, A. S. (2004). Target of rapamycin-mediated amino acid signaling in mosquito anautogeny. Proc. Natl. Acad. Sci. USA 101, 10626-10631 (Pubitemid 38955792)
14. Harada, H., Andersen, J. S., Mann, M., Terada, N. and Korsmeyer, S. J. (2001). p70S6 kinase signals cell survival as well as growth, inactivating the pro-apoptotic molecule BAD. Proc. Natl. Acad. Sci. USA 98, 9666-9670 (Pubitemid 32769360)
15. Idohou-Dossou, N., Wade, S., Guiro, A. T., Sarr, C. S., Diaham, B., Cissé, D., Beau, J. P., Chappuis, P., Hoffman, D. and Lemonnier, D. (2003). Nutritional status of preschool Senegalese children: long-term effects of early severe malnutrition. Br. J. Nutr. 90, 1123-1132 (Pubitemid 37548043)
16. Jensen, M. and De Meyts, P. (2009). Molecular mechanisms of differential intracellular signaling from the insulin receptor. Vitam. Horm. 80, 51-75
17. Kang, M. A., Mott, T. M., Tapley, E. C., Lewis, E. E. and Luckhart, S. (2008). Insulin regulates aging and oxidative stress in Anopheles stephensi. J. Exp. Biol. 211, 741-748 (Pubitemid 351542833)
18. Kaplan, E. L. and Meier, P. (1958). Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 53, 457-481
19. Kenyon, C. J. (2010). The genetics of ageing. Nature 464, 504-512
20. Kenyon, C. J. (2011). The first long-lived mutants: discovery of the insulin/IGF-1 pathway for ageing. Philos. Trans. R. Soc. Lond. B 366, 9-16
21. Kimura, K. D., Tissenbaum, H. A., Liu, Y. and Ruvkun, G. (1997). daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942-946 (Pubitemid 27366677)
22. Lackie, A. M. and Gavin, S. (1989). Uptake and persistence of ingested antibody in the mosquito Anopheles stephensi. Med. Vet. Entomol. 3, 225-230
23. Lambros, C. and Vanderberg, J. P. (1979). Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65, 418-420 (Pubitemid 10222999)
24. Löfqvist, C., Andersson, E., Gelander, L., Rosberg, S., Blum, W. F. and Albertsson Wikland, K. (2001). Reference values for IGF-I throughout childhood and adolescence: a model that accounts simultaneously for the effect of gender, age, and puberty. J. Clin. Endocrinol. Metab. 86, 5870-5876 (Pubitemid 33152637)
25. Luckhart, S. and Riehle, M. A. (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 (Pubitemid 46509795)
26. Luckhart, S., Crampton, A. L., Zamora, R., Lieber, M. J., Dos Santos, P. C., Peterson, T. M., Emmith, N., Lim, J., Wink, D. A. and Vodovotz, Y. (2003). Mammalian transforming growth factor beta1 activated after ingestion by Anopheles stephensi modulates mosquito immunity. Infect. Immun. 71, 3000-3009 (Pubitemid 36637520)
27. Marquez, A. G., Pietri, J. E., Smithers, H. M., Nuss, A., Antonova, Y., Drexler, A. L., Riehle, M. A., Brown, M. R. and Luckhart, S. (2011). Insulin-like peptides in the mosquito Anopheles stephensi: identification and expression in response to diet and infection with Plasmodium falciparum. Gen. Comp. Endocrinol. 173, 303-312
28. Mizushima, Y., Kato, H., Ohmae, H., Tanaka, T., Bobogare, A. and Ishii, A. (1994). Prevalence of malaria and its relationship to anemia, blood glucose levels, and serum somatomedin c (IGF-1) levels in the Solomon Islands. Acta Trop. 58, 207-220
29. Morcavallo, A., Genua, M., Palummo, A., Kletvikova, E., Jiracek, J., Brzozowski, A. M., Iozzo, R. V., Belfiore, A. and Morrione, A. (2012). Insulin and insulin-like growth factor II differentially regulate endocytic sorting and stability of insulin receptor isoform A. J. Biol. Chem. 287, 11422-11436
30. Pakpour, N., Corby-Harris, V., Green, G. P., Smithers, H. M., Cheung, K. W., Riehle, M. A. and Luckhart, S. (2012). Ingested human insulin inhibits the mosquito NF-κB-dependent immune response to Plasmodium falciparum. Infect. Immun. 80, 2141-2149
31. Planche, T., Dzeing, A., Ngou-Milama, E., Kombila, M. and Stacpoole, P. W. (2005). Metabolic complications of severe malaria. Curr. Top. Microbiol. Immunol. 295, 105-136 (Pubitemid 41236513)
32. Renehan, A. G., Jones, J., O'Dwyer, S. T. and Shalet, S. M. (2003). Determination of IGF-I, IGF-II, IGFBP-2, and IGFBP-3 levels in serum and plasma: comparisons using the Bland-Altman method. Growth Horm. IGF Res. 13, 341-346 (Pubitemid 37493325)
33. Riehle, M. A. and Brown, M. R. (2002). Insulin receptor expression during development and a reproductive cycle in the ovary of the mosquito Aedes aegypti. Cell Tissue Res. 308, 409-420 (Pubitemid 34666967)
34. Sajid, W., Kulahin, N., Schluckebier, G., Ribel, U., Henderson, H. R., Tatar, M., Hansen, B. F., Svendsen, A. M., Kiselyov, V. V., Nørgaard, P. et al. (2011). Structural and biological properties of the Drosophila insulin-like peptide 5 show evolutionary conservation. J. Biol. Chem. 286, 661-673
35. Schneider, M., Rudin, W. and Hecker, H. (1986). Absorption and transport of radioactive tracers in the midgut of the malaria mosquito, Anopheles stephensi. J. Ultrastruct. Mol. Struct. Res. 97, 50-63
36. Stephenson, L. S., Holland, C. V. and Cooper, E. S. (2000). The public health significance of Trichuris trichiura. Parasitology 121 Suppl., S73-S95. (Pubitemid 32499890)
37. Suh, Y., Atzmon, G., Cho, M. O., Hwang, D., Liu, B., Leahy, D. J., Barzilai, N. and Cohen, P. (2008). Functionally significant insulin-like growth factor I receptor mutations in centenarians. Proc. Natl. Acad. Sci. USA 105, 3438-3442 (Pubitemid 351723571)
38. Surachetpong, W., Singh, N., Cheung, K. W. and Luckhart, S. (2009). MAPK ERK signaling regulates the TGF-beta1-dependent mosquito response to Plasmodium falciparum. PLoS Pathog. 5, e1000366.
39. Surachetpong, W., Pakpour, N., Cheung, K. W. and Luckhart, S. (2011). Reactive oxygen species-dependent cell signaling regulates the mosquito immune response to Plasmodium falciparum. Antioxid. Redox Signal. 14, 943-955
40. Symons, A., Beinke, S. and Ley, S. C. (2006). MAP kinase kinase kinases and innate immunity. Trends Immunol. 27, 40-48 (Pubitemid 43083563)
41. Taniguchi, C. M., Emanuelli, B. and Kahn, C. R. (2006). Critical nodes in signalling pathways: insights into insulin action. Nat. Rev. Mol. Cell Biol. 7, 85-96 (Pubitemid 43278292)
42. Umbers, A. J., Boeuf, P., Clapham, C., Stanisic, D. I., Baiwog, F., Mueller, I., Siba, P., King, C. L., Beeson, J. G., Glazier, J. et al. (2011). Placental malariaassociated inflammation disturbs the insulin-like growth factor axis of fetal growth regulation. J. Infect. Dis. 203, 561-569
43. Vaughan, J. A., Wirtz, R. A., do Rosario, V. E. and Azad, A. F. (1990). Quantitation of antisporozoite immunoglobulins in the hemolymph of Anopheles stephensi after bloodfeeding. Am. J. Trop. Med. Hyg. 42, 10-16 (Pubitemid 20060505)
44. Wen, Z., Gulia, M., Clark, K. D., Dhara, A., Crim, J. W., Strand, M. R. and Brown, M. R. (2010). Two insulin-like peptide family members from the mosquito Aedes aegypti exhibit differential biological and receptor binding activities. Mol. Cell. Endocrinol. 328, 47-55
45. Weng, Q. P., Kozlowski, M., Belham, C., Zhang, A., Comb, M. J. and Avruch, J. (1998). Regulation of the p70 S6 kinase by phosphorylation in vivo. Analysis using site-specific anti-phosphopeptide antibodies. J. Biol. Chem. 273, 16621-16629 (Pubitemid 28311452)
46. White, N. J., Warrell, D. A., Chanthavanich, P., Looareesuwan, S., Warrell, M. J., Krishna, S., Williamson, D. H. and Turner, R. C. (1983). Severe hypoglycemia and hyperinsulinemia in falciparum malaria. N. Engl. J. Med. 309, 61-66 (Pubitemid 13063587)
47. White, N. J., Miller, K. D., Marsh, K., Berry, C. D., Turner, R. C., Williamson, D. H. and Brown, J. (1987). Hypoglycaemia in African children with severe malaria. Lancet 329, 708-711 (Pubitemid 17036985)
48. World Health Organization Global Malaria Program (2011). World Malaria Report 2011. Geneva: World Health Organization.
49. Yuan, R., Tsaih, S. W., Petkova, S. B., Marin de Evsikova, C., Xing, S., Marion, M. A., Bogue, M. A., Mills, K. D., Peters, L. L., Bult, C. J. et al. (2009). Aging in inbred strains of mice: study design and interim report on median lifespans and circulating IGF1 levels. Aging Cell 8, 277-287