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Temporal Coordination of Carbohydrate Metabolism during Mosquito Reproduction


Mosquitoes transmit numerous devastating human diseases due to their obligatory hematophagy that is required for the efficient reproduction. Metabolism must be synchronized with high energetic needs of a female mosquito for host seeking, blood feeding and rapid egg development. Each reproductive cycle is divided into two phases that are sequentially governed by juvenile hormone (JH) and 20-hydroxyecdysone. During the pre-blood meal phase, the JH receptor Methoprene-tolerant (Met) controls carbohydrate metabolism (CM) pathways and its RNA interference (RNAi) silencing caused up-regulation of CM enzymes at the transcript and protein levels activating glycolytic flux and depletion of storage and circulating sugars. During the second, post blood meal phase, CM was regulated by the ecdysone receptor EcR and its RNAi silencing had a dramatic effect opposite to that of Met RNAi. Thus, we show that Met and EcR function as regulatory switches coordinating carbohydrate metabolism with energetic requirements of the female mosquito reproductive cycle.


Vyšlo v časopise: Temporal Coordination of Carbohydrate Metabolism during Mosquito Reproduction. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005309
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005309

Souhrn

Mosquitoes transmit numerous devastating human diseases due to their obligatory hematophagy that is required for the efficient reproduction. Metabolism must be synchronized with high energetic needs of a female mosquito for host seeking, blood feeding and rapid egg development. Each reproductive cycle is divided into two phases that are sequentially governed by juvenile hormone (JH) and 20-hydroxyecdysone. During the pre-blood meal phase, the JH receptor Methoprene-tolerant (Met) controls carbohydrate metabolism (CM) pathways and its RNA interference (RNAi) silencing caused up-regulation of CM enzymes at the transcript and protein levels activating glycolytic flux and depletion of storage and circulating sugars. During the second, post blood meal phase, CM was regulated by the ecdysone receptor EcR and its RNAi silencing had a dramatic effect opposite to that of Met RNAi. Thus, we show that Met and EcR function as regulatory switches coordinating carbohydrate metabolism with energetic requirements of the female mosquito reproductive cycle.


Zdroje

1. Attardo GM, Hansen IA, Raikhel AS (2005) Nutritional regulation of vitellogenesis in mosquitoes: implications for anautogeny. Insect Biochem Mol Biol 35: 661–675. 15894184

2. Matthews KR (2011) Controlling and coordinating development in vector-transmitted parasites. Science 331: 1149–1153. doi: 10.1126/science.1198077 21385707

3. Clements AN (1992) The biology of mosquitoes Volume 1: Development, Nutrition and Reproduction. London: Chapman & Hall. 511 p.

4. Raikhel AS, Kokoza VA, Zhu J, Martin D, Wang SF, et al. (2002) Molecular biology of mosquito vitellogenesis: from basic studies to genetic engineering of antipathogen immunity. Insect Biochem Mol Biol 32: 1275–1286. 12225918

5. Zou Z, Saha TT, Roy S, Shin SW, Backman TW, et al. (2013) Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression. Proc Natl Acad Sci U S A 110: E2173–2181. doi: 10.1073/pnas.1305293110 23633570

6. Lunt SY, Vander Heiden MG (2011) Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 27: 441–464. doi: 10.1146/annurev-cellbio-092910-154237 21985671

7. Nelson DL, Cox MM (2008) Lehninger Principles of Biochemistry 5th. Freeman W H, New York.

8. Tennessen JM, Baker KD, Lam G, Evans J, Thummel CS (2011) The Drosophila estrogen-related receptor directs a metabolic switch that supports developmental growth. Cell Metab 13: 139–148. doi: 10.1016/j.cmet.2011.01.005 21284981

9. Li M, Mead EA, Zhu J (2011) Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad USA 108: 638–643.

10. Hansen IA, Attardo GM, Park JH, Peng Q, Raikhel AS (2004) Target of rapamycin-mediated amino acid signaling in mosquito anautogeny. Proc Natl Acad Sci U S A 101: 10626–10631. 15229322

11. Roy SG, Hansen IA, Raikhel AS (2007) Effect of insulin and 20-hydroxyecdysone in the fat body of the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol 37: 1317–1326. 17967350

12. Gulia-Nuss M, Robertson AE, Brown MR, Strand MR (2011) Insulin-like peptides and the target of rapamycin pathway coordinately regulate blood digestion and egg maturation in the mosquito Aedes aegypti. PLoS One 6: e20401. doi: 10.1371/journal.pone.0020401 21647424

13. Roy SG, Raikhel AS (2011) The small GTPase Rheb is a key component linking amino acid signaling and TOR in the nutritional pathway that controls mosquito egg development. Insect Biochem Mol Biol 41: 62–69. doi: 10.1016/j.ibmb.2010.10.001 21035549

14. Bryant B, Raikhel AS (2011) Programmed autophagy in the fat body of Aedes aegypti is required to maintain egg maturation cycles. PLoS One 6: e25502. doi: 10.1371/journal.pone.0025502 22125592

15. Poelchau MF, Reynolds JA, Elsik CG, Denlinger DL, Armbruster PA (2013) Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proc Biol Sci 280: 20130143. doi: 10.1098/rspb.2013.0143 23516243

16. Stark R, Kibbey RG (2014) The mitochondrial isoform of phosphoenolpyruvate carboxykinase (PEPCK-M) and glucose homeostasis: has it been overlooked? Biochim Biophys Acta 1840: 1313–1330. doi: 10.1016/j.bbagen.2013.10.033 24177027

17. Iijima K, Zhao L, Shenton C, Iijima-Ando K (2009) Regulation of energy stores and feeding by neuronal and peripheral CREB activity in Drosophila. PLoS One 4: e8498. doi: 10.1371/journal.pone.0008498 20041126

18. Patra KC, Hay N (2014) The pentose phosphate pathway and cancer. Trends Biochem Sci 39: 347–354. doi: 10.1016/j.tibs.2014.06.005 25037503

19. Kim JW, Tchernyshyov I, Semenza GL, Dang CV (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3: 177–185. 16517405

20. Bersten DC, Sullivan AE, Peet DJ, Whitelaw ML (2013) bHLH-PAS proteins in cancer. Nat Rev Cancer 13: 827–841. doi: 10.1038/nrc3621 24263188

21. Jindra M, Palli SR, Riddiford LM (2013) The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58: 181–204. doi: 10.1146/annurev-ento-120811-153700 22994547

22. Cui Y, Sui Y, Xu J, Zhu F, Palli SR (2014) Juvenile hormone regulates Aedes aegypti Kruppel homolog 1 through a conserved E box motif. Insect Biochem Mol Biol 52: 23–32. doi: 10.1016/j.ibmb.2014.05.009 24931431

23. Charles JP, Iwema T, Epa VC, Takaki K, Rynes J, et al. (2011) Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc Natl Acad Sci USA 108: 21128–21133. doi: 10.1073/pnas.1116123109 22167806

24. Shin SW, Zou Z, Saha TT, Raikhel AS (2012) bHLH-PAS heterodimer of methoprene-tolerant and Cycle mediates circadian expression of juvenile hormone-induced mosquito genes. Proc Natl Acad Sci USA 109: 16576–16581. doi: 10.1073/pnas.1214209109 23012454

25. Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M, et al. (2012) Transcriptional regulation of juvenile hormone-mediated induction of Kruppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci USA 109: 11729–11734. doi: 10.1073/pnas.1204951109 22753472

26. Attardo GM, Hansen IA, Shiao SH, Raikhel AS (2006) Identification of two cationic amino acid transporters required for nutritional signaling during mosquito reproduction. J Exp Biol 209: 3071–3078. 16888056

27. Chawla A, Repa JJ, Evans RM, Mangelsdorf DJ (2001) Nuclear receptors and lipid physiology: opening the X-files. Science 294: 1866–1870. 11729302

28. Sun G, Zhu J, Chen L, Raikhel AS (2005) Synergistic action of E74B and ecdysteroid receptor in activating a 20-hydroxyecdysone effector gene. Proc Natl Acad Sci U S A 102: 15506–15511. 16230625

29. Cruz J, Mane-Padros D, Zou Z, Raikhel AS (2012) Distinct roles of isoforms of the heme-liganded nuclear receptor E75, an insect ortholog of the vertebrate Rev-erb, in mosquito reproduction. Mol Cell Endocrinol 349: 262–271. doi: 10.1016/j.mce.2011.11.006 22115961

30. Mane-Padros D, Cruz J, Cheng A, Raikhel AS (2012) A critical role of the nuclear receptor HR3 in regulation of gonadotrophic cycles of the mosquito Aedes aegypti. PLoS One 7: e45019. doi: 10.1371/journal.pone.0045019 23049766

31. Hays AR, Raikhel AS (1990) A Novel Protein Produced by the Vitellogenic Fat-Body and Accumulated in Mosquito Oocytes. Rouxs Archives of Developmental Biology 199: 114–121.

32. Bricker DK, Taylor EB, Schell JC, Orsak T, Boutron A, et al. (2012) A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans. Science 337: 96–100. doi: 10.1126/science.1218099 22628558

33. Palanker L, Tennessen JM, Lam G, Thummel CS (2009) Drosophila HNF4 regulates lipid mobilization and beta-oxidation. Cell Metab 9: 228–239. doi: 10.1016/j.cmet.2009.01.009 19254568

34. Ruaud AF, Lam G, Thummel CS (2011) The Drosophila NR4A nuclear receptor DHR38 regulates carbohydrate metabolism and glycogen storage. Mol Endocrinol 25: 83–91. doi: 10.1210/me.2010-0337 21084378

35. Zhu XJ, Dai JQ, Tan X, Zhao Y, Yang WJ (2009) Activation of an AMP-activated protein kinase is involved in post-diapause development of Artemia franciscana encysted embryos. BMC Dev Biol 9: 21. doi: 10.1186/1471-213X-9-21 19284883

36. Martins GF, Serrao JE, Ramalho-Ortigao JM, Pimenta PF (2011) Histochemical and ultrastructural studies of the mosquito Aedes aegypti fat body: effects of aging and diet type. Microsc Res Tech 74: 1032–1039. doi: 10.1002/jemt.20990 21509905

37. Hansen IA, Attardo GM, Roy SG, Raikhel AS (2005) Target of rapamycin-dependent activation of S6 kinase is a central step in the transduction of nutritional signals during egg development in a mosquito. J Biol Chem 280: 20565–20572. 15788394

38. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, et al. (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34: D354–357. 16381885

39. Castillo-Davis CI, Hartl DL (2003) GeneMerge—post-genomic analysis, data mining, and hypothesis testing. Bioinformatics 19: 891–892. 12724301

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Genetika Reprodukčná medicína

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PLOS Genetics


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