#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Genetic Evidence for Function of the bHLH-PAS Protein Gce/Met As a Juvenile Hormone Receptor


Juvenile hormones (JHs) play critical roles in the development of arthropods, comprising half the animal biomass of the oceans and over a million insect species, which have an enormous impact on ecosystems, agriculture (pollinators and pests) and health of mankind (disease vectors). Despite decades of research, a receptor for these unique sesquiterpenoid hormones has remained elusive. Here, we provide definitive genetic evidence establishing that the essential biological function of the Gce/Met protein during insect development is critically dependent on its ability to bind JH, in effect functionally defining a JH receptor. Unequivocal identification of a JH receptor has profound implications for our understanding of arthropod biology. It also defines a molecular target for development of environmentally friendly, safer insecticides.


Vyšlo v časopise: Genetic Evidence for Function of the bHLH-PAS Protein Gce/Met As a Juvenile Hormone Receptor. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005394
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005394

Souhrn

Juvenile hormones (JHs) play critical roles in the development of arthropods, comprising half the animal biomass of the oceans and over a million insect species, which have an enormous impact on ecosystems, agriculture (pollinators and pests) and health of mankind (disease vectors). Despite decades of research, a receptor for these unique sesquiterpenoid hormones has remained elusive. Here, we provide definitive genetic evidence establishing that the essential biological function of the Gce/Met protein during insect development is critically dependent on its ability to bind JH, in effect functionally defining a JH receptor. Unequivocal identification of a JH receptor has profound implications for our understanding of arthropod biology. It also defines a molecular target for development of environmentally friendly, safer insecticides.


Zdroje

1. Nijhout H (1994) Insect hormones. Princeton: Princeton University Press. 267 p.

2. Cusson M, Yagi KJ, Ding Q, Duve H, Thorpe A, et al. (1991) Biosynthesis and release of juvenile hormone and its precursors in insects and crustaceans: the search for a unifying arthropod endocrinology. Insect Biochem 21: 1–6.

3. Laufer H, Biggers WJ (2001) Unifying concepts learned from methyl farnesoate for invertebrate reproduction and post-embryonic development. Am Zool 41: 442–457.

4. Raikhel AS, Brown MR, Bellés X (2005) Hormonal control of reproductive processes. In: Gilbert LI, Iatrou K, Gill SS, editors. Comprehensive molecular insect science. Amsterdam: Elsevier/Pergamon. pp. 433–491.

5. 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

6. Dubrovsky EB, Bernardo TJ (2014) The juvenile hormone receptor and molecular mechanisms of juvenile hormone action. Adv Insect Physiol 46: 305–388.

7. Röller H, Dahm KH, Sweeley CC, Trost BM (1967) Die Struktur des Juvenilhormones. Angew Chemie 4: 190–191.

8. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schütz G, et al. (1995) The nuclear receptor superfamily: the second decade. Cell 83: 835–839. 8521507

9. King-Jones K, Thummel CS (2005) Nuclear receptors–a perspective from Drosophila. Nat Rev Genet 6: 311–323. 15803199

10. Hill RJ, Billas IML, Bonneton F, Graham LD, Lawrence MC (2013) Ecdysone receptors: from the Ashburner model to structural biology. Annu Rev Entomol 58: 251–271. doi: 10.1146/annurev-ento-120811-153610 23072463

11. Jones G, Sharp PA (1997) Ultraspiracle: an invertebrate nuclear receptor for juvenile hormones. Proc Natl Acad Sci USA 94: 13499–13503. 9391054

12. Jones G, Jones D, Teal P, Sapa A, Wozniak M (2006) The retinoid-X receptor ortholog, ultraspiracle, binds with nanomolar affinity to an endogenous morphogenetic ligand. FEBS J 273: 4983–4996. 17064257

13. Jones G, Teal P, Henrich VC, Krzywonos A, Sapa A, et al. (2013) Ligand binding pocket function of Drosophila USP is necessary for metamorphosis. Gen Comp Endocrinol 182: 73–82. doi: 10.1016/j.ygcen.2012.11.009 23211750

14. Jones D, Jones G, Teal P (2013) Sesquiterpene action, and morphogenetic signaling through the ortholog of retinoid X receptor, in higher Diptera. Gen Comp Endocrinol 194: 326–335. doi: 10.1016/j.ygcen.2013.09.021 24120505

15. Heyman RA, Mangelsdorf DJ, Dyck JA, Stein RB, Eichele G, et al. (1992) 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68: 397–406. 1310260

16. Yao TP, Segraves WA, Oro AE, McKeown M, Evans RM (1992) Drosophila ultraspiracle modulates ecdysone receptor function via heterodimer formation. Cell 71: 63–72. 1327536

17. Thomas HE, Stunnenberg HG, Stewart AF (1993) Heterodimerization of the Drosophila ecdysone receptor with retinoid X receptor and ultraspiracle. Nature 362: 471–475. 8385270

18. Nowickyj SM, Chithalen JV, Cameron D, Tyshenko MG, Petkovich M, et al. (2008) Locust retinoid X receptors: 9-cis-retinoic acid in embryos from a primitive insect. Proc Natl Acad Sci USA 105: 9540–9545. doi: 10.1073/pnas.0712132105 18606996

19. Ren B, Peat TS, Streltsov VA, Pollard M, Fernley R, et al. (2014) Unprecedented conformational flexibility revealed in the ligand-binding domains of the Bovicola ovis ecdysone receptor (EcR) and ultraspiracle (USP) subunits. Acta Crystallogr D Biol Crystallogr 70: 1954–1964. doi: 10.1107/S1399004714009626 25004972

20. Wilson TG, Fabian J (1986) A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev Biol 118: 190–201. 3095161

21. Konopova B, Jindra M (2007) Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. Proc Natl Acad Sci USA 104: 10488–10493. 17537916

22. Abdou MA, He Q, Wen D, Zyaan O, Wang J, et al. (2011) Drosophila Met and Gce are partially redundant in transducing juvenile hormone action. Insect Biochem Mol Biol 41: 938–945. doi: 10.1016/j.ibmb.2011.09.003 21968404

23. Riddiford LM, Truman JW, Mirth CK, Shen YC (2010) A role for juvenile hormone in the prepupal development of Drosophila melanogaster. Development 137: 1117–1126. doi: 10.1242/dev.037218 20181742

24. Baumann A, Fujiwara Y, Wilson TG (2010) Evolutionary divergence of the paralogs Methoprene tolerant (Met) and germ cell expressed (gce) within the genus Drosophila. J Insect Physiol 56: 1445–1455. doi: 10.1016/j.jinsphys.2010.05.001 20457161

25. Ashok M, Turner C, Wilson TG (1998) Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proc Natl Acad Sci USA 95: 2761–2766. 9501163

26. Denison MS, Soshilov AA, He G, DeGroot DE, Zhao B (2011) Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol Sci 124: 1–22. doi: 10.1093/toxsci/kfr218 21908767

27. Stockinger B, Di Meglio P, Gialitakis M, Duarte JH (2014) The aryl hydrocarbon receptor: multitasking in the immune system. Annu Rev Immunol 32: 403–432. doi: 10.1146/annurev-immunol-032713-120245 24655296

28. Miura K, Oda M, Makita S, Chinzei Y (2005) Characterization of the Drosophila Methoprene-tolerant gene product. FEBS J 272: 1169–1178. 15720391

29. Charles J-P, 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

30. Li M, Liu P, Wiley JD, Ojani R, Bevan DR, et al. (2014) A steroid receptor coactivator acts as the DNA-binding partner of the methoprene-tolerant protein in regulating juvenile hormone response genes. Mol Cell Endocrinol 394: 47–58. doi: 10.1016/j.mce.2014.06.021 25004255

31. Li M, Mead EA, Zhu J (2011) Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad Sci USA 108: 638–643. doi: 10.1073/pnas.1013914108 21187375

32. Zhang Z, Xu J, Sheng Z, Sui Y, Palli SR (2011) Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, methoprene tolerant. J Biol Chem 286: 8437–8447. doi: 10.1074/jbc.M110.191684 21190938

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

34. He Q, Wen D, Jia Q, Cui C, Wang J, et al. (2014) Heat shock protein 83 (Hsp83) facilitates Methoprene-tolerant (Met) nuclear import to modulate juvenile hormone signaling. J Biol Chem 289: 27874–27885. doi: 10.1074/jbc.M114.582825 25122763

35. Zou Z, Saha TT, Roy S, Shin SW, Backman TWH, et al. (2013) Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression. Proc Natl Acad Sci USA 110: E2173–E2181. doi: 10.1073/pnas.1305293110 23633570

36. Lozano J, Kayukawa T, Shinoda T, Bellés X (2014) A role for taiman in insect metamorphosis. PLoS Genet 10: e1004769. doi: 10.1371/journal.pgen.1004769 25356827

37. Smykal V, Bajgar A, Provaznik J, Fexova S, Buricova M, et al. (2014) Juvenile hormone signaling during reproduction and development of the linden bug, Pyrrhocoris apterus. Insect Biochem Mol Biol 45: 69–76. doi: 10.1016/j.ibmb.2013.12.003 24361539

38. Guo W, Wu Z, Song J, Jiang F, Wang Z, et al. (2014) Juvenile hormone-receptor complex acts on mcm4 and mcm7 to promote polyploidy and vitellogenesis in the migratory locust. PLoS Genet 10: e1004702. doi: 10.1371/journal.pgen.1004702 25340846

39. Wen D, Rivera-Perez C, Abdou M, Jia Q, He Q, et al. (2015) Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis. PLoS Genet 11: e1005038. doi: 10.1371/journal.pgen.1005038 25774983

40. Ishaaya I, Horowitz AR (1995) Pyriproxyfen, a novel insect growth regulator for controlling whiteflies: mechanisms and resistance management. Pestic Sci 43: 227–232.

41. Nagaraju GPC (2011) Reproductive regulators in decapod crustaceans: an overview. J Exp Biol 214: 3–16. doi: 10.1242/jeb.047183 21147963

42. Miyakawa H, Toyota K, Sumiya E, Iguchi T (2014) Comparison of JH signaling in insects and crustaceans. Curr Opin Insect Sci 1: 81–87.

43. Miyakawa H, Toyota K, Hirakawa I, Ogino Y, Miyagawa S, et al. (2013) A mutation in the receptor Methoprene-tolerant alters juvenile hormone response in insects and crustaceans. Nat Commun 4: 1856. doi: 10.1038/ncomms2868 23673641

44. Groth AC, Fish M, Nusse R, Calos MP (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166: 1775–1782. 15126397

45. Pecasse F, Beck Y, Ruiz C, Richards G (2000) Krüppel-homolog, a stage-specific modulator of the prepupal ecdysone response, is essential for Drosophila metamorphosis. Dev Biol 221: 53–67. 10772791

46. Baumann A, Barry J, Wang S, Fujiwara Y, Wilson TG (2010) Paralogous genes involved in juvenile hormone action in Drosophila melanogaster. Genetics 185: 1327–1336. doi: 10.1534/genetics.110.116962 20498297

47. Wilson TG, Ashok M (1998) Insecticide resistance resulting from an absence of target-site gene product. Proc Natl Acad Sci USA 95: 14040–14044. 9826649

48. Valenta T, Lukas J, Korinek V (2003) HMG box transcription factor TCF-4's interaction with CtBP1 controls the expression of the Wnt target Axin2/Conductin in human embryonic kidney cells. Nucleic Acids Res 31: 2369–2380. 12711682

49. Bischof J, Maeda RK, Hediger M, Karch F, Basler K (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci USA 104: 3312–3317. 17360644

50. Bai J, Uehara Y, Montell DJ (2000) Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 103: 1047–1058. 11163181

51. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415. 8223268

52. Riddiford LM, Ashburner M (1991) Effects of juvenile hormone mimics on larval development and metamorphosis of Drosophila melanogaster. Gen Comp Endocrinol 82: 172–183. 1906823

53. Külshammer E, Uhlirova M (2013) The actin cross-linker Filamin/Cheerio mediates tumor malignancy downstream of JNK signaling. J Cell Sci 126: 927–938. doi: 10.1242/jcs.114462 23239028

54. Struhl G, Basler K (1993) Organizing activity of wingless protein in Drosophila. Cell 72: 527–540. 8440019

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 7
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#