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Instituto Nacional de Salud Pública

2018, Number 1

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salud publica mex 2018; 60 (1)

Ecdysis-related pleiotropic neuropeptides expression during Anopheles albimanus development

Alvarado-Delgado A, Moran-Francia K, Perales-Ortiz G, Rodríguez MH, Lanz-Mendoza H

Language: English
References: 45
Page: 48-55
PDF size: 301.48 Kb.


ABSTRACT

Objective. To analyze the transcription pattern of neuropeptides in the ontogeny of a malaria vector, the mosquito Anopheles albimanus. Materials and methods. The transcription pattern of Crustacean CardioActive peptide (CCAP), corazonin, Ecdysis Triggering Hormone (ETH), allatostatin-A, orcokinin, Insulin Like Peptide 2 (ILP2), Insulin Like Peptide 5 (ILP5) and bursicon was evaluated using qPCR on larvae (1st – 4th instar), pupae and adult mosquitoes. Results. Unlike in other insects, transcripts of CCAP (70.8%), ETH (60.2%) and corazonin (76.5%) were expressed in 4th instar larvae, probably because these three neuropeptides are associated with the beginning of ecdysis. The neuropeptide ILP2 showed higher transcription levels in other stages and orcokinin decreased during the development of the mosquito. Conclusion. The CCAP, corazonin and ETH neuropeptides are potential targets for the design of control strategies aimed at disrupting An. albiamnus larval development.


REFERENCES

  1. Organización Mundial de la Salud. Enfermedades transmitidas por vectores 2016. Ginebra: OMS 2016. Available at: http://www.who.int/ mediacentre/factsheets/fs387/es/

  2. Tercero-Gutiérrez MJ, Olalla-Herbosa R. Enfermedades tropicales transmitidas por vectores. Medidas preventivas y profilaxis. Offarm 2011;30:78-89.

  3. Estevez-Lao TY, Boyce DS, Honegger HW, Hillyer JF. Cardioacceleratory function of the neurohormone CCAP in the mosquito Anopheles gambiae. J Exp Biol 2013;216:601-613. https://doi.org/10.1242/jeb.077164

  4. Wanjala CL, Mbugi JP, Ototo E, Gesuge M, Afrane YA, Atieli HE, et al. Pyrethroid and DDT Resistance and Organophosphate Susceptibility among Anopheles spp. Mosquitoes, Western Kenya. Emerg Infect Dis 2015;21:2178-2181. https://doi.org/10.3201/eid2112.150814

  5. World Health Organization. World Malaria Report 2013. Geneva: WHO, 2013. Available at: http://www.who.int/malaria/publications/world_malaria_ report_2013/en/

  6. Dhadialla TS, Carlson GR, Le DP. New insecticides with ecdysteroidal and juvenile hormone activity. Annual review of entomology 1998;43:545- 569. https://doi.org/10.1146/annurev.ento.43.1.545

  7. Palma L, Munoz D, Berry C, Murillo J, Caballero P. Bacillus thuringiensis toxins: an overview of their biocidal activity. Toxins (Basel) 2014;6(12):3296-3325. https://doi.org/10.3390/toxins6123296

  8. Nassel DR, Winther AM. Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 2010;92(1):42-104. https://doi. org/10.1016/j.pneurobio.2010.04.010

  9. O’Neal ST, Samuel GH, Adelman ZN, Myles KM. Mosquito-borne viruses and suppressors of invertebrate antiviral RNA silencing. Viruses 2014;6(11):4314-4331. https://doi.org/10.3390/v6114314

  10. Stangier J, Hilbich C, Beyreuther K, Keller R. Unusual cardioactive peptide (CCAP) from pericardial organs of the shore crab Carcinus maenas. Proc Natl Acad Sci U S A 1987;84(2):575-579. https://doi.org/10.1073/ pnas.84.2.575

  11. Tublitz N, Brink D, Broadie KS, Loi PK, Sylwester AW. From behavior to molecules: an integrated approach to the study of neuropeptides. Trends in neurosciences 1991;14(6):254-259. https://doi.org/10.1016/0166- 2236(91)90126-F

  12. Donini A, Agricola H, Lange AB. Crustacean cardioactive peptide is a modulator of oviduct contractions in Locusta migratoria. Journal of insect physiology 2001;47(3):277-285. https://doi.org/10.1016/S0022- 1910(00)00112-8

  13. Kim YJ, Zitnan D, Cho KH, Schooley DA, Mizoguchi A, Adams ME. Central peptidergic ensembles associated with organization of an innate behavior. Proc Natl Acad Sci U S A. 2006;103(38):14211-14216. https://doi. org/10.1073/pnas.0603459103

  14. Veenstra JA. Isolation and structure of corazonin, a cardioactive peptide from the American cockroach. FEBS Lett 1989;250(2):231-234. https://doi.org/10.1016/0014-5793(89)80727-6

  15. Tanaka S. Endocrine mechanisms controlling body-color polymorphism in locusts. Arch Insect Biochem Physiol 2001;47(3):139-149. https://doi. org/10.1002/arch.1045

  16. Luo CW, Dewey EM, Sudo S, Ewer J, Hsu SY, Honegger HW, et al. Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2. Proc Natl Acad Sci USA 2005;102(8):2820-2825. https://doi.org/10.1073/ pnas.0409916102

  17. Kim YJ, Spalovska-Valachova I, Cho KH, Zitnanova I, Park Y, Adams ME, et al. Corazonin receptor signaling in ecdysis initiation. Proc Natl Acad Sci USA 2004;101(17):6704-6709. https://doi.org/10.1073/pnas.0305291101

  18. Kruger E, Mena W, Lahr EC, Johnson EC, Ewer J. Genetic analysis of Eclosion hormone action during Drosophila larval ecdysis. Development 2015;142:4279-4287. https://doi.org/10.1242/dev.126995

  19. Baker KD, Thummel CS. Diabetic larvae and obese flies – emerging studies of metabolism in Drosophila. Cell metabolism 2007;6(4):257-266. https://doi.org/10.1016/j.cmet.2007.09.002

  20. Bounias M, Bahjou A, Gourdoux L, Moreau R. Molecular activation of a trehalase purified from the fat body of a coleopteran insect (Tenebrio molitor), by an endogenous insulin-like peptide. Biochem Mol Biol Int 1993;31:249-266.

  21. Slaidina M, Delanoue R, Gronke S, Partridge L, Léopold P. A Drosophila insulin-like peptide promotes growth during nonfeeding states. Dev Cell 2009;17(6):874-884. https://doi.org/10.1016/j.devcel.2009.10.009

  22. Iwami M. Bombyxin: An Insect Brain Peptide that Belongs to the Insulin Family. Zoolog Sci 2000;17(8):1035-1044. https://doi.org/10.2108/ zsj.17.1035

  23. Giannakou ME, Partridge L. Role of insulin-like signalling in Drosophila lifespan. Trends Biochem Sci 2007;32(4):180-188. https://doi.org/10.1016/j. tibs.2007.02.007

  24. Cong X, Wang H, Liu Z, He C, An C, Zhao Z. Regulation of Sleep by Insulin-like Peptide System in Drosophila melanogaster. Sleep 2015;38(7):1075-1083. https://doi.org/10.5665/sleep.4816

  25. Riehle MA, Brown MR. Insulin stimulates ecdysteroid production through a conserved signaling cascade in the mosquito Aedes aegypti. Insect Biochem Mol Biol 1999;29(10):855-860. https://doi.org/10.1016/ S0965-1748(99)00084-3

  26. Stay B, Tobe SS, Bendena WG. Allatostatins: Identification, Primary Structures, Functions and Distribution. In: Evans PD, ed. Advances in Insect Physiology. Volume 25. Oxford UK: Oxford University, 1995:267-337. https://doi.org/10.1016/s0065-2806(08)60066-1

  27. Bendena WG, Donly BC, Tobe SS. Allatostatins: a growing family of neuropeptides with structural and functional diversity. Ann N Y Acad Sci 1999;897:311-329. https://doi.org/10.1111/j.1749-6632.1999.tb07902.x

  28. Yamanaka N, Roller L, Zit ˇnan D, Satake H, Mizoguchi A, Kataoka H, et al. Bombyx orcokinins are brain-gut peptides involved in the neuronal regulation of ecdysteroidogenesis. J Comp Neurol 2011;519(2):238-246. https://doi.org/10.1002/cne.22517

  29. Hofer S, Homberg U. Evidence for a role of orcokinin-related peptides in the circadian clock controlling locomotor activity of the cockroach Leucophaea maderae. J Exp Biol 2006;209:2794-2803. https://doi. org/10.1242/jeb.02307

  30. Ons S, Bellés X, Maestro JL. Orcokinins contribute to the regulation of vitellogenin transcription in the cockroach Blattella germanica. J Insect Physiol 2015;82:129-133. https://doi.org/10.1016/j.jinsphys.2015.10.002

  31. Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH, Gething PW, et al. The dominant Anopheles vectors of human malaria in the Americas: occurrence data, distribution maps and bionomic precis. Parasit Vectors 2010;3:72. https://doi.org/10.1186/1756-3305-3-72

  32. Chomczynski P. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 1993;15:532-537.

  33. Martínez-Barnetche J, Gómez-Barreto RE, Ovilla-Muñoz M, Téllez- Sosa J, García López DE, Dinglasan RR, et al. Transcriptome of the adult female malaria mosquito vector Anopheles albimanus. BMC Genomics 2012;13:207. https://doi.org/10.1186/1471-2164-13-207

  34. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25(4):402-408. https://doi.org/10.1006/meth.2001.1262

  35. Jiang H, Wei Z, Nachman RJ, Kaczmarek K, Zabrocki J, Park Y. Functional characterization of five different PRXamide receptors of the red flour beetle Tribolium castaneum with peptidomimetics and identification of agonists and antagonists. Peptides 2015;68:246-252. https://doi. org/10.1016/j.peptides.2014.11.004

  36. Xie Y, Zhang L, Zhang C, Wu X, Deng X, Yang X, et al. Synthesis, biological activity, and conformational study of N-methylated allatostatin analogues inhibiting juvenile hormone biosynthesis. J Agric Food Chem 2015;63(11):2870-2876. https://doi.org/10.1021/acs.jafc.5b00882

  37. Nachman RJ, Wang XJ, Etzkorn FA, Aziz OB, Davidovitch M, Kaczmarek K, et al. Evaluation of a PK/PBAN analog with an (E)-alkene, trans-Pro isostere identifies the Pro orientation for activity in four diverse PK/ PBAN bioassays. Peptides 2009;30(7):1254-1259. https://doi.org/10.1016/j. peptides.2009.04.017

  38. Nachman RJ, Teal PE, Aziz OB, Davidovitch M, Zubrzak P, Altstein M. An amphiphilic, PK/PBAN analog is a selective pheromonotropic antagonist that penetrates the cuticle of a heliothine insect. Peptides 2009;30(3):616- 621. https://doi.org/10.1016/j.peptides.2008.09.024

  39. Zhang Q, Nachman RJ, Kaczmarek K, Zabrocki J, Denlinger DL. Disruption of insect diapause using agonists and an antagonist of diapause hormone. Proc Natl Acad Sci USA 2011;108(41):16922-16926. https://doi. org/10.1073/pnas.1113863108

  40. Smagghe G, Mahdian K, Zubrzak P, Nachman RJ. Antifeedant activity and high mortality in the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidae) induced by biostable insect kinin analogs. Peptides 2010;31(3):498-505. https://doi.org/10.1016/j.peptides.2009.07.001

  41. Hillyer JF, Estévez-Lao TY, de la Parte LE. Myotropic effects of FMRFamide containing peptides on the heart of the mosquito Anopheles gambiae. Gen Comp Endocrinol 2014;202:15-25. https://doi.org/10.1016/j. ygcen.2014.03.048

  42. Hillyer JF, Estévez-Lao TY, Funkhouser LJ, Aluoch VA. Anopheles gambiae corazonin: gene structure, expression and effect on mosquito heart physiology. Insect Mol Biol 2012;21(3):343-355. https://doi.org/10.1111/ j.1365-2583.2012.01140.x

  43. Honegger HW, Estévez-Lao TY, Hillyer JF. Bursicon-expressing neurons undergo apoptosis after adult ecdysis in the mosquito Anopheles gambiae. J Insect Physiol 2011;57(7):1017-1022. https://doi.org/10.1016/j. jinsphys.2011.04.019

  44. Garczynski SF, Crim JW, Brown MR. Characterization and expression of the short neuropeptide F receptor in the African malaria mosquito, Anopheles gambiae. Peptides 2007;28(1):109-118. https://doi. org/10.1016/j.peptides.2006.09.019

  45. Kaufmann C, Brown MR. Adipokinetic hormones in the African malaria mosquito, Anopheles gambiae: identification and expression of genes for two peptides and a putative receptor. Insect Biochem Mol Biol 2006;36(6):466-481. https://doi.org/10.1016/j.ibmb.2006.03.009




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