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Expression profile of genes encoding allatoregulatory neuropeptides in females of the spider Parasteatoda tepidariorum (Araneae, Theridiidae)


Autoři: Marta Katarzyna Sawadro aff001;  Agata Wanda Bednarek aff001;  Agnieszka Ewa Molenda aff001;  Agnieszka Izabela Babczyńska aff001
Působiště autorů: Department of Animal Physiology and Ecotoxicology, University of Silesia in Katowice, Bankowa, Katowice, Poland aff001
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222274

Souhrn

Allatoregulatory neuropeptides are multifunctional proteins that take part in the synthesis and secretion of juvenile hormones. In insects, allatostatins are inhibitors of juvenile hormone biosynthesis in the corpora allata while allatotropins, act as stimulators. By quantitative real-time PCR, we analyzed the gene expression of allatostatin A (PtASTA), allatostatin B (PtASTB), allatostatin C (PtASTC), allatotropin (PtAT) and their receptors (PtASTA-R, PtASTB-R, PtASTC-R, PtAT-R) in various tissues in different age groups of female spiders. In the presented manuscript, the presence of allatostatin A, allatostatin C, and allatotropin are reported in females of the spider P. tepidariorum. The obtained results indicated substantial differences in gene expression levels for allatoregulatory neuropeptides and their receptors in the different tissues. Additionally, the gene expression levels also varied depending on the female age. Strong expression was observed coinciding with sexual maturation in the neuroendocrine and nervous system, and to a lower extent in the digestive tissues and ovaries. Reverse trends were observed for the expression of genes encoding the receptors of these neuropeptides. In conclusion, our study is the first hint that the site of synthesis and secretion is fulfilled by similar structures as observed in other arthropods. In addition, the results of the analysis of spider physiology give evidence that the general functions like regulation of the juvenile hormone synthesis, regulation of the digestive tract and ovaries action, control of vitellogenesis process by the neuropeptides seem to be conserved among arthropods and are the milestone to future functional studies.

Klíčová slova:

Biology and life sciences – Biochemistry – Neurochemistry – Neurochemicals – Neuropeptides – Hormones – Peptide hormones – Neuroscience – Genetics – Gene expression – Anatomy – Nervous system – Reproductive system – Ovaries – Organisms – Eukaryota – Animals – Invertebrates – Arthropoda – Arachnida – Spiders – Insects – Medicine and health sciences – Research and analysis methods – Database and informatics methods – Bioinformatics – Sequence analysis – Sequence motif analysis


Zdroje

1. Marciniak P, Szymczak M, Rosiński G. Hormony peptydowe owadów–przegląd najważniejszych rodzin. Post Biol Komórki. 2011;38: 43–63.

2. Sarkar NRS, Tobe SS, Orchard I. The distribution and effects of Dippu-allatostatin-like peptides in the blood-feeding bug, Rhodnius prolixus. Peptides. 2003;24: 1553–1563. doi: 10.1016/j.peptides.2003.07.015 14706534

3. Nassel DR. Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Prog Neurobiol. 2002;68: 1–84. 12427481

4. Dickinson PS, Wiwatpanit T, Gabranski ER, Ackerman RJ, Stevens JS, Cashman CR, et al.Identification of SYWKQCAFNAVSCFamide: a broadly conserved crustacean C-type allatostatin-like peptide with both neuromodulatory and cardioactive properties. J Experimental Biology. 2009;212: 1140–1152.

5. Christie AE, Pascual MG. Peptidergic signaling in the crab Cancer borealis: Tapping the power of transcriptomics for neuropeptidome expansion. Gen Comp Endocrino. 2016;237: 53–67.

6. Christie AE. Expansion of the neuropeptidome of the globally invasive marine crab Carcinus maenas. Gen Comp Endocrino. 2016;235: 150–169.

7. Christie AE, Pascual MG, Yu A. Peptidergic signaling in the tadpole shrimp Triops newberryi: A potential model for investigating the roles played by peptide paracrines/hormones in adaptation to environmental change. Mar Genomics. 2018;39: 45–63. doi: 10.1016/j.margen.2018.01.005 29526397

8. Duve H, Johnsen A, Scott AG, Thorpe A. Allatostatins of the tiger prawn, Penaeus monodon (Crustacea: Penaeidea). Peptides. 2002;23: 1039–1051. doi: 10.1016/s0196-9781(02)00035-9 12126730

9. Christie AE, Miller A, Fernandez R, Dickinson ES, Jordan A, Kohn J, et al. Non-amidated and amidated members of the C-type allatostatin (AST-C) family are differentially distributed in the stomatogastric nervous system of the American lobster, Homarus americanus. Invert Neurosci. 2018;18: 2. doi: 10.1007/s10158-018-0206-6 29332202

10. Ahn SJ, Martin R, Rao S, Choi MY. Neuropeptides predicted from the transcriptome analysis of the gray garden slug Deroceras reticulatum. Peptides. 2017;93: 51–65. doi: 10.1016/j.peptides.2017.05.005 28502716

11. Sawadro M, Bednarek A, Babczyńska A. The current state of knowledge on the neuroactive compounds that affect the development, mating and reproduction of spiders (Araneae) compared to insects. Invert Neurosci. 2017;17: 4. doi: 10.1007/s10158-017-0197-8 28421370

12. Smart D, Johnston CF, Curry WJ, Williamson R, Maule AG, Skuce PJ, et al. Peptides related to the Diploptera punctata allatostatins in nonarthropod invertebrates: An immunocytochemical survey. J Comp Neurol. 1994; 347: 426–432. doi: 10.1002/cne.903470308 7822491

13. Alzugaray ME, Hernández-Martínez S, Ronderos JR. Somatostatin signaling system as an ancestral mechanism: Myoregulatory activity of an Allatostatin-C peptide in Hydra. Peptides. 2016;82: 67–75. doi: 10.1016/j.peptides.2016.05.011 27288244

14. Laufer H, Borst D, Baker FC, Reuter CC, Tsai LW, Schooley DA, et al. Identification of a juvenile hormone–like compound in a crustacean. Science. 1987;235: 202–205. doi: 10.1126/science.235.4785.202 17778635

15. Laufer H, Landau M, Borst D, Homola E. The synthesis and regulation of methyl farnesoate, a new juvenile hormone for crustacean reproduction. Adv Inver Reprod. 1986;4: 135–143.

16. Gonçalves SC, Carvalho HF, Hartfelder K. Juvenile hormone signaling in insect oogenesis. Curr Opin Insect Sci. 2019;31: 43–48. doi: 10.1016/j.cois.2018.07.010 31109672

17. Harshini S, Nachman RJ, Sreekumar S. Inhibition of digestive enzyme release by neuropeptides in larvae of Opisina arenosella (Lepidoptera: Cryptophasidae). Comp Biochem Physiol. B. 2002;132: 353–358. 12031460

18. Marciniak P, Rosiński G. Aktualny stan badań nad neuropeptydami miotropowymi owadów: tachykininy, sulfakininy i FMRFa-pokrewne peptydy. Post Biol Komórki. 2007;34: 241–249.

19. Bendena WG. Neuropeptide physiology in Insects. Neuropeptide systems as targets for parasite and pest control. Adv Exp Med Biol. 2010;692: 166–191. doi: 10.1007/978-1-4419-6902-6_9 21189679

20. Gade G, Hoffmann KH. Neuropeptides regulating development and reproduction in insects. Physiol Entomol. 2005;30: 103–121.

21. Zhu XX, Oliver JH. Cockroach allatostatin–like immunoreactivity in the synganglion of the American dog tick Dermacentor variabilis (Acari: Ixodidae). Exp Appl Acarol. 2001;25: 1005–1013. 12465854

22. Neupert S, Russell WK, Predel R, Russell DH, Strey OF, Teel PD, et al. The neuropeptidomics of Ixodes scapularis synganglion. J Proteome Res. 2009;72: 1040–1045.

23. Loesel R, Seyfarth EA, Bräunig P, Agricola HJ. Neuroarchitecture of the arcuate body in the brain of the spider Cupiennius salei (Araneae, Chelicerata) revealed by allatostatin–, proctolin–, and CCAP–immunocytochemistry and its evolutionary implications. Arthropod Struct Dev. 2011;40: 210–220. doi: 10.1016/j.asd.2011.01.002 21256976

24. De Loof A, Hoffmann KH. Neuropeptides in insect development and reproduction. Arch Insect Biochem Physiol. 2001;47: 127–128. doi: 10.1002/arch.1043 11418930

25. Bednarek A, Sawadro M, Babczyńska A. Modulation of the response to stress factors of Xerolycosa nemoralis (Lycosidae) spiders living in contaminated environments. Ecotoxicol Environ Saf. 2016;131: 1–6. doi: 10.1016/j.ecoenv.2016.04.027 27162128

26. Turnbull AL. 1973. Ecology of the true spiders (Araneomorphae). Annu Rev Entomol. 1973;18: 305–348.

27. Wise DH. Spiders in Ecological Webs. Cambridge University Press, Cambridge, UK. 1993.

28. Ekschmitt K, Wolters V, Weber M. Spiders, carabids, and staphylinids: the ecological potential of predatory macroarthropods. In: Benckiser G. editor. Fauna in Soil Ecosystems., New York: Marcel Dekker; 1997. p. 307–362.

29. Bonaric JC. Contribution a l'etude de la biofogie de developpement chez l'araignee Pisaura mirabilis (Clerck., 1758). Approche physiologique des phenomenes de mue et de diapause hivemale. Montpellier, PhD. 1980.

30. Bonaric JC. Effets des ecdysones et de l'hormone juvénile sur ladurée du cycle de mue chez l'araignée Pisaura mirabilis (Araneae, Pisauridae). Rev Arachn. 1979;2: 205–207.

31. Bonaric JC. Juberthie UEC. Ultrastructure of the Retrocerebral Neuroendocrine Complex in Pisaura mirabilis Cl. (Araneae, Pisauridae). Zool Jahrb. Abt allg Zool Physiol Tiere. 1983;87: 55–64.

32. Bonaric JC. Le systeme neuroendocrine retrocerebral des Araignees: structure et function. In: Ruzicka V. editor. Proceedings of the 15th European Colloquium of Arachnology. Ceske Budejovice: Institute of Entomology; 1995. p. 27–34.

33. Bonaric JC. Moulting Hormones. In: Nentwig W. editor. Ecophysiology of spiders. Berlin: Springer-Verlag; 1986. p. 111–118.

34. Bonaric JC, Emerit M, Legendre R. Le complexe neuroendocrine rétrocérébral et la «glande de mue» de Filistata insidiatrix Forskôl (Araneae, Filistatidae). Rev Arch. 5;1984: 301–310.

35. Miyashita K. Development and egg sac production of Achaearanea tepidariorum (CL Koch) (Araneae, Theridiidae) under long and short photoperiods. J Arachn. 1987;15: 51–58.

36. NCBI Protein database in National Library of Medicine (US), 2017. National Center for Biotechnology Information [Internet]. Available: https://www.ncbi.nlm.nih.gov/gene/. Accesses: 20 May 2017.

37. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215: 403–410. doi: 10.1016/S0022-2836(05)80360-2 2231712

38. Pearson WR. An Introduction to Sequence and Series. Int J Res. 2014;1: 1286–1292.

39. Jones P, Binns D, Chang H-Y, Fraser M, Weizhong LW, McAnulla C, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30: 1236–1240. doi: 10.1093/bioinformatics/btu031 24451626

40. Ouedraogo M, Bettembourg C, Bretaudeau A, Sallou O, Diot C, Demeure O, et al. 2012.The duplicated genes database: identification and functional annotation of co-localised duplicated genes across genomes. PLoS One. 2012;7(11):e50653. doi: 10.1371/journal.pone.0050653 23209799

41. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol. 2018;35: 1547–1549. doi: 10.1093/molbev/msy096 29722887

42. Wong ML, Medrano JF. Real-time PCR for mRNA quantitation. BioTechniques. 2005;39: 1–11.

43. Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4: 406–425. doi: 10.1093/oxfordjournals.molbev.a040454 3447015

44. Chomczyński P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-choloroform extraction. Anal Biochem. 1987;162: 156–159. doi: 10.1006/abio.1987.9999 2440339

45. Bookout AL, Cummins CL, Mangelsdorf DJ. High-throughput real-time quantitative reverse transcription PCR. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, et al., editors. Current Protocols in Molecular Biology. Michigan: Wiley; 2005. p. 2363–2383.

46. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution. 1985;39: 783–791. doi: 10.1111/j.1558-5646.1985.tb00420.x 28561359

47. Schoofs L, Holman GM, Hayes TK, Nachman RJ, De Loof A. Isolation, identification and synthesis of locusta-myoinhibiting peptide (Lom-MIP), a novel biologically active neuropeptide from Locusta migratoria. Regul Pept. 1991;36: 111–119. doi: 10.1016/0167-0115(91)90199-q 1796179

48. Blackburn MB, Wagner RM, Kochansky JP, Harrison DJ, Thomas-Laemont P, Raina AK. The identification of two myoinhibitory peptides, with sequence similarities to the galanins, isolated from the ventral nerve cord of Manduca sexta. Regul Pept. 1995;57: 213–219. doi: 10.1016/0167-0115(95)00034-9 7480870

49. Lorenz MW, Kellner R, Hoffmann KH, Gade G. Identification of multiple peptide homologous to cockroach and cricket allatostatins in the stick insect, Carausius morosus. Insect Biochem Mol Biol. 2000;30: 711–718. 10876114

50. Williamson M, Lenz C, Winther AME, Nassel DR, Grimmelikhuijzen CJP. Molecular cloning, genomic organization, and expression of a B–type (cricket–type) allatostatin preprohormone from Drosophila melanogaster. Biochem Biophys Res Commun. 2001;281: 544–550. doi: 10.1006/bbrc.2001.4402 11181081

51. Wang J. Isolation and characterization of the B–type allatostatin gene of Gryllus bimaculatus de Geer (Ensifera, Gryllidae). PhD. 2004.

52. Lorenz MW, Gäde G, Hoffmann KH. Interspecific actions of allatostatins. Mitt Dtsch Ges Allg Angew Entomol. 1997;11: 549–553.

53. Posnien N, Zeng V, Schwager EE, Pechmann M, Hilbrant M, Keefe JD, et al. A comprehensive reference transcriptome resource for the common house spider Parasteatoda tepidariorum. PLoS One. 2014;9(8):e104885. doi: 10.1371/journal.pone.0104885 25118601

54. Schwager EE, Sharma PP, Clarke T, Leite DJ, Wierschin T, Pechmann M, et al. The house spider genome reveals an ancient whole-genome duplication during arachnid evolution. BMC Biol. 2017;15: 62. doi: 10.1186/s12915-017-0399-x 28756775

55. Stay B, Sereg Bachmann JA, Stoltzmann CA, Fairbairn SE, Yu CG, Tobe SS. Factors affecting allatostatin release in a cockroach (Diploptera punctata): Nerve section, juvenile hormone analog and ovary. J Insect Physiol. 1994;50: 365–372.

56. Witek GK, Hoffmann H. Immunological evidence for FGLamide- and w2w9-allatostatins in the ovary of Gryllus bimaculatus (Ensifera, Gryllidae). Physiol Entomol. 2001;26: 49–57.

57. Abdel-Latief M, Hoffmann KH, Functional activity of allatotropin and allatostatin in the pupal stage of a holometablous insect, Tribolium castaneum (Coleoptera, Tenebrionidae). Peptides. 2014;53: 172–184. doi: 10.1016/j.peptides.2013.10.007 24140809

58. Yamanaka N, Yamamoto S, Zitnan D, Watanabe K1, Kawada T, Satake H, et al. Neuropeptide Receptor Transcriptome Reveals Unidentified Neuroendocrine Pathways. PLoS ONE. 2008;3(8): e3048. doi: 10.1371/journal.pone.0003048 18725956

59. Nouzova M, Rivera-Perez C, Noriega FG. Allatostatin-C reversibly blocks the transport of citrate out of the mitochondria and inhibits juvenile hormone synthesis in mosquitoes. Insect Biochem Mol Biol. 2015;57: 20–26. doi: 10.1016/j.ibmb.2014.12.003 25500428

60. Lenz C, Williamson M, Grimmelikhuijzen CJ. Molecular cloning and genomic organization of a second probable allatostatin receptor from Drosophila melanogaster. Biochem Biophys Res Commun. 2000;273: 571–577. doi: 10.1006/bbrc.2000.2964 10873647

61. Urlacher E, Soustelle L, Parmentier ML, Verlinden H, Gherardi MJ, Fourmy D, et al. Honey Bee Allatostatins Target Galanin/ Somatostatin-Like Receptors and Modulate Learning: A Conserved Function? PLoS ONE. 2016;11(1): e0146248. doi: 10.1371/journal.pone.0146248 26741132

62. Kreienkamp HJ, Larusson HJ, Witte I, Roeder T, Birgül N, Honck HH, et al. Functional annotation of two orphan G-proteincoupled receptors, Drostar1 and -2, from Drosophila melanogaster and their ligands by reverse pharmacology. J Biol Chem. 2002;277: 39937–39943. doi: 10.1074/jbc.M206931200 12167655

63. Lange AB, Chan KK, Stay B. 1993. Effect of allatostatin and proctolin on antennal pulsatile organ and hindgut muscle in the cockroach, Diploptera punctata. Arch Insect Biochem Physiol. 1993;24: 79–92. doi: 10.1002/arch.940240203 7902139

64. Yu CG, Hayes TK, Strey A, Bendena WG, Tobe SS. Identification and partial characterization of receptors for allatostatins in brain and corpora allata of the cockroach Diploptera punctata using a binding assay and photoaffinity labeling. Regul Pept. 1995;57: 347–358. doi: 10.1016/0167-0115(95)00048-G 7480884

65. Secher T, Lenz C, Cazzamali G, Sorensen G, Williamson M, Hansen GN, et al. Molecular cloning of a functional allatostatin gut/brain receptor and an allatostatin preprohormone from the silkworm Bombyx mori. J Biol Chem. 2001;276: 47052–47060. doi: 10.1074/jbc.M106675200 11590150

66. Meyering-Vos M, Merz S, Sertkol M, Hoffmann KH. Functional analysis of the allatostatin-A type gene in the cricket Gryllus bimaculatus and the armyworm Spodoptera frugiperda. Insect Biochem Mol Biol. 2006;36: 492–504. doi: 10.1016/j.ibmb.2006.03.008 16731345

67. Lungchukiet P, Donly BC, Zhang J, Tobe SS, Bendena WG. Molecular cloning and characterization of an allatostatin-like receptor in the cockroach Diploptera punctata. Peptides. 2008;29: 276–285. doi: 10.1016/j.peptides.2007.10.029 18237821

68. Duve H, Wren P, Thorpe A. Innervation of the foregut of the cockroach Leucophaea maderae and inhibition of spontaneous contractile activity by allatostatin neuropeptides. Physiol Entomol. 1995;20: 33–44.

69. Aguilar R., Maestro JL, Vilaplana L, Pascual N, Piulachs MD, Belles X. Allatostatin gene expression in brain and midgut, and activity of synthetic allatostatins on feeding-related processes in the cockroach Blattella germanica. Regul Pept. 2003;115: 171–177. doi: 10.1016/s0167-0115(03)00165-4 14556958

70. Fuse M, Zhang JR, Partridge E, Nachman RJ, Orchard I, Bendena WG, et al. Effects of an allatostatin and a myosuppressin on midgut carbohydrate enzyme activity in the cockroach Diploptera punctata. Peptides. 1999;20: 1285–1293. doi: 10.1016/s0196-9781(99)00133-3 10612442

71. Martin D, Piulachs MD, Bell X. Inhibition of vitellogenin production by allatostatin in the German cockroach. Mol Cell Endocrinol. 1996;121: 191–196. doi: 10.1016/0303-7207(96)03864-6 8892320

72. Woodhead AP, Thompson ME, Chan KK, Stay B. Allatostatin in ovaries, oviducts, and young embryos in the cockroach Diploptera punctata. J Insect Physiol. 2003;49: 1103–1114. 14624882

73. Lorenz MW. Neuropeptides regulating developmental, reproductive, and metabolic events in crickets: structures and modes of action. J Insect Biotechnol Sericol. 2001;70: 69–93.

74. Lorenz JI, Lorenz MW, Hoffmann KH. Regulators of ovarian ecdysteroid release display opposite effects in the cricket Gryllus bimaculatus and the cockroach Blaptica dubia. Mitt Dtsch Ges Allg Angew Entomol. 2004;14: 447–450.

75. Sawadro M, Bednarek A, Molenda A, Babczyńska A. Allatoregulatory neuropeptides role in vitellogenesis process of Parasteatoda tepidariorum (Araneae, Theridiidae) spider females. Conference paper. 31st European Congress of Arachnology. 2018.

76. Sawadro M, Bednarek A, Molenda A, Babczyńska A, Metabolizm energetyczny samic Parasteatoda tepidariorum (Araneae, Theridiidae) po iniekcji neuropeptydów allatoregulujących. Conference paper. VII Ogólnopolska Konferencja Młodych Naukowców–ARTHROPOD. 2018.

77. Bednarek A, Sawadro M, Nicewicz Ł, Babczyńska A. Vitellogenins in the spider Parasteatoda tepidariorum–expression profile and putative hormonal regulation of vitellogenesis. BMC Dev Biol. 2019;19: 4. doi: 10.1186/s12861-019-0184-x 30849941

78. Riddiford LM. Cellular and molecular actions of juvenile hormone I. General considerations and premetamorphic actions. Adv In Insect Phys. 1994;24: 213–227.

79. Smykal V, Daimon T, Kayukawa T, Takaki K, Shinoda T, Jindra M. Importance of juvenile hormone signaling arises with competence of insect larvae to metamorphose. Dev Biol. 2014;390: 221–230. doi: 10.1016/j.ydbio.2014.03.006 24662045

80. Bednarek A, Sawadro M, Nicewicz Ł, Babczyńska A. Ekspresja genów kodujących enzym epox CYP15A1 oraz receptory hormonów juwenilnych w jajnikach samic pająka Parasteatoda tepidariorum (Araneae, Theridiidae). Conference paper. VII Ogólnopolska Konferencja Młodych Naukowców–ARTHROPOD. 2018.

81. Garside CS, Koladich PM, Bendena WG, Tobe SS. Expression of allatostatin in the oviducts of the cockroach Diploptera punctata. Insect Biochem Mol Biol. 2002;32: 1089–1099. 12213245


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