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FMRF-related peptides in Aedes aegypti midgut: neuromuscular connections and enteric nervous system

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Abstract

FMRFamide-related peptides (FaRPs) are a class of neuropeptides that participate in a variety of physiological processes in invertebrates. They occur in nerves of stomatogastric ganglia and enteroendocrine cells of the insect digestive tract, where they may control muscle functions. However, their direct involvement in muscle function has never been shown in situ. We studied the relationship between FaRPs and midgut muscle during larval–pupal transition of the mosquito Aedes aegypti. In late L4, FaRP-positive neuronal extensions attach to the bundles of the external circular muscle layer, and muscle stem cells start to undergo mitosis in the internal circular layer. Thereafter, the external muscle layer degenerates, disappearing during early pupal development, and is completely absent in the adult mosquito. Our results indicate that FaRP-based neural signals are involved in the reorganization of the muscle fibers of the mosquito midgut during the larval–pupal transition. In addition to confirming FaRP involvement in muscle function, we show that the mosquito midgut muscles are largely innervated, and that circular and longitudinal muscle have specific neuron bodies associated with them.

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References

  • Aghajanian P, Takashima S, Paul M, Younossi-Hartenstein A, Hartenstein V (2016) Metamorphosis of the Drosophila visceral musculature and its role in intestinal morphogenesis and stem cell formation. J Development 420:43–59

    CAS  Google Scholar 

  • Beehler-Evans R, Micchelli CA (2015) Generation of enteroendocrine cell diversity in midgut stem cell lineages. J Development 142:654–664

    Article  CAS  Google Scholar 

  • Bernick EP, Moffett SB, Moffett DF (2007) Organization, ultrastructure, and development of midgut visceral muscle in larval Aedes aegypti. J Tissue Cell 39:277–292

    Article  CAS  Google Scholar 

  • Bernick EP, Moffett SB, Moffett DF (2008) Ultrastructure and morphology of midgut visceral muscle in early pupal Aedes aegypti mosquitoes. J Tissue Cell 40:127–141

    Article  CAS  Google Scholar 

  • Brown MR, Crim JW, Lea AO (1986) FMRFamide-and pancreatic polypeptidelike immunoreactivity of endocrine cells in the midgut of a mosquito. J Tissue Cell 18:419–428

    Article  CAS  Google Scholar 

  • Brown MR, Lea A (1988) FMRFamide-and adipokinetic hormone-Like immunoreactivity in the nervous system of the mosquito, Aedes aegypti. J Comp Neurol 614:606–614

    Article  Google Scholar 

  • Brown MR, Klowden MJ, Crim JW, Young L, Shrouder LA, Lea AO (1994) Endogenous regulation of mosquito host-seeking behavior by a neuropeptide. J Insect Physiol 40:399–406

    Article  CAS  Google Scholar 

  • Bureau I (2015) Novel neuropeptides useful as insecticides Field. The present invention relates to peptide fragments and analogs derived from background of the invention neuropeptides play a key role in the regulation of a variety of physiological’, Israel Patente WO 2015/052701

  • Copenhaver PF (2007) How to innervate a simple gut: familiar themes and unique aspects in the formation of the insect enteric nervous system. J Dev Dyn 236:1841–1864

    Article  CAS  Google Scholar 

  • Cottrell GA (1993) The wide range of actions of the FMRFamide-related peptides and the biological importance of peptidergic messengers. Comparative Molecular Neurobiology, Birkhäuser Basel 279–285

  • Dowling JE (1991) Dopamine release from interplexiform cells in the retina: effects of bicuculline, and enkephalin on horizontal. J Neurosci 11:3034–3046

    Article  PubMed  PubMed Central  Google Scholar 

  • Duttlinger A, Berry K, Nichols R (2002) The different effects of three Drosophila melanogaster dFMRFamide-containing peptides on crop contractions suggest these structurally related peptides do not play redundant functions in gut. J Peptides 23:1953–1957

    Article  CAS  Google Scholar 

  • Elphick MR, Mirabeau O (2014) The evolution and variety of RFamide-type neuropeptides: insights from deuterostomian invertebrates. J Front Endocrinol 5:93

    Google Scholar 

  • Fadda M, Hasakiogullari I, Temmerman L, Beets I, Zels S, Schoofs L (2019) Regulation of feeding and metabolism by neuropeptide F and short neuropeptide F in invertebrates. Front Endocrinol 10:64

    Article  Google Scholar 

  • Fernandes KM, Neves CA, Serrão JE, Martins GF (2014) Aedes aegypti midgut remodeling during metamorphosis. Parasitol Int 63:506–512

    Article  PubMed  Google Scholar 

  • Fónagy A (2007) Insect neuropeptides and their potential application for pest control. Acta phytopathologica et entomologica Hungarica 41:137–152

    Article  Google Scholar 

  • Godoy RSM, Fernandes KM, Martins GF (2015) Midgut of the non-hematophagous mosquito Toxorhynchites theobaldi (Diptera, Culicidae). Sci Rep 5:1–16

    Article  CAS  Google Scholar 

  • Gonzalez-Gaitan M, Jackle H (1995) Invagination centers within the Drosophila stomatogastric nervous system anlage are positioned by Notch-mediated signaling which is spatially controlled through wingless. J Development 121:2313–2325

    Article  CAS  Google Scholar 

  • Hartenstein V (1997) Development of the insect stomatogastric nervous system. J Trends Neurosci 20:421–427

    Article  CAS  Google Scholar 

  • Hao K, Ullah H, Jarwar AR, Nong X, Tu X, Zhang Z (2020) Functional identification of an FMRFamide-related peptide gene on diapause induction of the migratory locust, Locusta migratoria L. Genomics 112:1821–1828

    Article  CAS  PubMed  Google Scholar 

  • Haselton AT, Yin CM, Stoffolano JG (2008) FMRFamide-like immunoreactivity in the central nervous system and alimentary tract of the non-hematophagous blow fly, Phormia regina, and the hematophagous horse fly, Tabanus nigrovittatus. J Insect Sci 8:1–17

    Article  PubMed  Google Scholar 

  • Hill SR, Orchard I (2004) The influence of diet and feeding state on FMRFamide-related peptides in the gut of Locusta migratoria L. J Peptides 25:105–114

    Article  CAS  Google Scholar 

  • Hung RJ, Hu Y, Kirchner R, Liu Y, Xu C, Comjean A, Perrimon N (2020) A cell atlas of the adult Drosophila midgut. Proc Natl Acad Sci 117:1514–1523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JC, Zeve VH (2003) The fine structure of the gastric caeca of Aedes aegypti larvae. J Insect Physiol 14:1567–1575

    Article  Google Scholar 

  • Kingan TG, Shabanowitz J, Hunt D, Witten J (1996) Characterization of two myotrophic neuropeptides in the FMRFamide family from the segmental ganglia of the moth Manduca sexta: candidate neurohormones and neuromodulators. J Exp Biol 199:1095–1104

    Article  CAS  PubMed  Google Scholar 

  • Klapper R (2000) The longitudinal visceral musculature of Drosophila melanogaster persists through metamorphosis. J Mech Dev 95:47–54

    Article  CAS  Google Scholar 

  • Krajniak KG (2013) Invertebrate FMRFamide Related Peptides. J Prot Pept Lett 20:647–670

    Article  CAS  Google Scholar 

  • Lee JS, Shih PY, Schaedel ON, Quintero-Cadena P, Rogers AK, Sternberg PW (2017) FMRFamide-like peptides expand the behavioral repertoire of a densely connected nervous system. J Proc Natl Acad Sci 114:E10726–E10735

    Article  CAS  Google Scholar 

  • Lenaerts C, Cools D, Verdonck R, Verbakel L, Broeck JV, Marchal E (2017) The ecdysis triggering hormone system is essential for successful moulting of a major hemimetabolous pest insect, Schistocerca gregaria. Sci Rep 7:1–14

    Article  CAS  Google Scholar 

  • López-Vera E, Aguilar MB, Heimer de la Cotera EP (2008) FMRFamide and related peptides in the phylum mollusca. Peptides 29:310–317

    Article  PubMed  CAS  Google Scholar 

  • Martin BS, Gomez MR, Landgraf M, Bate M (2001) A distinct set of founders and fusion-competent myoblasts make visceral muscles in the Drosophila embryo. J Development 128:3331–3338

    Article  CAS  Google Scholar 

  • McLachlan IG, Beets I, Bono M, Heiman MG (2018) A neuronal MAP kinase constrains growth of a Caenorhabditis elegans sensory dendrite throughout the life of the organism. J PLoS Gen 14:1–22

    Google Scholar 

  • Micchelli CA, Sudmeier L, Perrimon N, Tang S, Beehler-Evans R (2011) Identification of adult midgut precursors in Drosophila. J Gene Exp Patt 11:12–21

    Article  CAS  Google Scholar 

  • Milakovic M, Ormerod KG, Klose MK, Mercier AJ (2014) Mode of action of a Drosophila FMRFamide in inducing muscle contraction. J Exp Biol 217:1725–1736

    PubMed  Google Scholar 

  • Moffett SB, Moffett DF (2014) Comparison of immunoreactivity to serotonin, FMRFamide and SCPb in the gut and visceral nervous system of larvae, pupae and adults of the yellow fever mosquito Aedes aegypti. J Insect Sci 5:20

    Google Scholar 

  • Nagata S (2016) FMRFamides. In: Handbook of hormones. Academic Press 432–433

  • Nässel DR, Winther ÅM (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42–104

    Article  PubMed  CAS  Google Scholar 

  • Nässel DR, Zandawala M (2019) Recent advances in neuropeptide signaling in Drosophila, from genes to physiology and behavior. Prog Neurobiol 179:101607

    Article  PubMed  CAS  Google Scholar 

  • Nassel RD, Bayraktaroglu E, Dircksen H (1994) Neuropeptides in neurosecretory and efferent neural systems of insect thoracic and abdominal ganglia. J Zool Sci 11:15–31

    Google Scholar 

  • Nichols R, McCormick J, Lim I (1999) Regulation of Drosophila FMRFamide neuropeptide gene expression. J Neurobiology 39:347–358

    Article  CAS  Google Scholar 

  • Nishiura JT, Ho P, Ray K (2003) Methoprene interferes with mosquito midgut remodeling during metamorphosis. J Med Entomol 40:498–507

    Article  CAS  PubMed  Google Scholar 

  • Nishiura JT, Ray K, Murray J (2005) Expression of nuclear receptor-transcription factor genes during Aedes aegypti midgut metamorphosis and the effect of methoprene on expression. Insect Biochem Mol Biol 35:561–573

    Article  CAS  PubMed  Google Scholar 

  • Oliveira AH, Gonçalves WG, Fernandes KM, Barcellos MS, Sampaio WMS, Lopes MP, Martins GF, Serrão JE (2019) Morphology and morphometry of the midgut in the stingless bee Friesella schrottkyi (Hymenoptera: Apidae). J Insects 10:73

    Article  Google Scholar 

  • Onken H, Moffett SB, Moffett DF (2004) The anterior stomach of larval mosquitoes (Aedes aegypti): effects of neuropeptides on transepithelial ion transport and muscular motility. J Exp Biol 207:3731–3739

    Article  CAS  PubMed  Google Scholar 

  • Orchard I, Lange AB, Bendena WG (2001) FMRFamide-related peptides: a multifunctional family of structurally related neuropeptides in insects. Adv Insect Physiol 28:267–329

    Article  CAS  Google Scholar 

  • Parthasarathy R, Palli SR (2007) Stage-and cell-specific expression of ecdysone receptors and ecdysone-induced transcription factors during midgut remodeling in the yellow fever mosquito, Aedes aegypti. J Insect Physiol 53:216–229

    Article  CAS  PubMed  Google Scholar 

  • Peters RS, Meusemann K, Petersen M, Mayer C, Wilbrandt J, Ziesmann T, Donath A, Kjer KM, Aspöck U, Aspöck H (2014) The evolutionary history of holometabolous insects inferred from transcriptome-based phylogeny and comprehensive morphological data. J BMC Evol Biol 14:52

    Article  Google Scholar 

  • Predel R, Neupert S, Garczynski SF, Crim JW, Brown MR, Russell WK, Nachman RJ (2010) Neuropeptidomics of the mosquito Aedes aegypti. J Proteome Res 9:2006–2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price DA, Greenberg MJ (1977a) Purification characterization of a cardioexcitatory neuropeptide from the central ganglia of a bivalve mollusc. J Prep Bioch 7:261–281

    CAS  Google Scholar 

  • Price DA, Greenberg MJ (1977b) Structure of a molluscan cardioexcitatory neuropeptide. J Science 197:670–671

    CAS  Google Scholar 

  • Price DA, Greenberg MJ (2007) The Hunting of the FaRPs: The distribution of FMRFamide-related peptides. J Biol Bull 177:198–205

    Article  Google Scholar 

  • Reiher W, Shirras C, Kahnt J, Baumeister S, Isaac RE, Wegener C (2011) Peptidomics and peptide hormone processing in the Drosophila midgut. J Proteome Res 10:1881–1892

    Article  CAS  PubMed  Google Scholar 

  • Roller L, Čižmár D, Gáliková Z, Bednár B, Daubnerová I, Žitňan D (2016) Molecular cloning, expression and identification of the promoter regulatory region for the neuropeptide trissin in the nervous system of the silkmoth Bombyx mori. Cell Tissue Res 364:499–512

    Article  CAS  PubMed  Google Scholar 

  • Rudolf A, Buttgereit D, Jacobs M, Wolfstetter G, Kesper D, Pütz M, Berger S, Renkawitz-Pohl R, Holz A, Önel SF (2014) Distinct genetic programs guide Drosophila circular and longitudinal visceral myoblast fusion. J BMC Cell Biol 15:27

    Article  CAS  Google Scholar 

  • Scherkenbeck J, Zdobinsky T (2009) Insect neuropeptides: structures, chemical modifications and potential for insect control. J Bioorg Med Chem 17:4071–4084

    Article  CAS  Google Scholar 

  • Schinkmann K, Li C (1992) Localization of FMRFamide-like peptides in Caenorhabditis elegans. J Compar Neurol 316:251–260

    Article  CAS  Google Scholar 

  • Sedra L, Lange AB (2016) Cloning and expression of long neuropeptide F and the role of FMRFamide-like peptides in regulating egg production in the Chagas vector, Rhodnius prolixus. Peptides 82:1–11

    Article  CAS  PubMed  Google Scholar 

  • Seron TJ, Hill J, Linser PJ (2004) A GPI-linked carbonic anhydrase expressed in the larval mosquito midgut. J Exp Biol 207:4559–4572

    Article  CAS  PubMed  Google Scholar 

  • Souza DLL, Zanuncio JC, Serrão JE (2016) FMRFamide-cells in the midgut of Scaptotrigona xanthotricha (Apidae: Meliponini) of different ages and fed different diets. J Apicul Research 55:428–432

    Article  Google Scholar 

  • Stanek DM, Pohl J, Crim JW, Brown MR (2002) Neuropeptide F and its expression in the yellow fever mosquito, Aedes aegypti. Peptides 23:1367–1378

    Article  CAS  PubMed  Google Scholar 

  • Strand MR, Brown MR, Vogel KJ (2016) Mosquito peptide hormones: diversity, production, and function. Adv Insect Physiol 51:145–188

    Article  CAS  Google Scholar 

  • Stracker TH, Thompson S, Grossman GL, Riehle MA, Brown MR (2002) Characterization of the AeaHP gene and its expression in the mosquito Aedes aegypti (Diptera: Culicidae). J Med Entomol 39:331–342

    Article  CAS  PubMed  Google Scholar 

  • Taghert PH, Nitabach MN (2012) Peptide neuromodulation in invertebrate model systems. Neuron 76:82–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarr EA, Fidler BM, Gee KE, Anderson CM, Jager AK, Gallagher NM, Fabian-Fine R (2019) Distribution of FMRFamide-related peptides and co-localization with glutamate in Cupiennius salei, an invertebrate model system. Cell Tissue Res 376:83–96

    Article  CAS  PubMed  Google Scholar 

  • Tune TC, Irving T, Sponberg S (2020) Nanometer-scale structure differences in the myofilament lattice spacing of two two cockroach leg muscles correspond to their different functions. J Exp Biol 9:223

    Google Scholar 

  • Tuthill JC, Wilson RI (2016a) Mechanosensation and adaptive motor control in insects. J Curr Biol 26:R1022–R1038

    Article  CAS  Google Scholar 

  • Tuthill JC, Wilson RI (2016b) Parallel transformation of tactile signals in central circuits of Drosophila. J Cell 164:1046–1059

    Article  CAS  Google Scholar 

  • Veenstra JA, Lau GW, Agricola HJ, Petzel DH (1995) Immunohistological localization of regulatory peptides in the midgut of the female mosquitoAedes aegypti. Histochemistry and Cell Biology 104:337–347

    Article  CAS  PubMed  Google Scholar 

  • Warr E, Aguilar R, Dong Y, Mahairaki V, Dimopoulos G (2007) Spatial and sex-specific dissection of the Anopheles gambiae midgut transcriptome. BMC Genomics 8:1–11

    Article  CAS  Google Scholar 

  • Weetman D, Kamgang B, Badolo A, Moyes CL, Shearer FM, Coulibaly M, Pinto J, Lambrechts L, McCall PJ (2018) Aedes mosquitoes and Aedes-borne arboviruses in Africa: current and future threats. Int J Environ Res Public Health 15:220

    Article  PubMed Central  Google Scholar 

  • Wikgren M, Fagerholm HP (1993) Neuropeptides in sensory structures of nematodes. J Acta Biol Hung 44:133–136

    CAS  Google Scholar 

  • Wu Y, Parthasarathy R, Bai H, Palli SR (2006) Mechanisms of midgut remodeling: juvenile hormone analog methoprene blocks midgut metamorphosis by modulating ecdysone action. Mech Dev 123:530–547

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Cleary L, Byrne J (2018) Identification and characterization of pleural neurons that inhibit tail sensory neurons and motor neurons in Aplysia: correlation with FMRFamide immunoreactivity. J Neuroscience 14:3565–3577

    Article  Google Scholar 

  • Zels S, Dillen S, Crabbé K, Spit J, Nachman RJ, Broeck JV (2015) Sulfakinin is an important regulator of digestive processes in the migratory locust, Locusta migratoria. Insect Biochem Mol Biol 61:8–16

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Yan Z, Li B, Jan LY, Jan YN (2014) Identification of motor neurons and a mechanosensitive sensory neuron in the defecation circuitry of Drosophila larvae. J eLife 3:e03293

    Article  Google Scholar 

  • Žitňan D, Šauman I, Sehnal F (1993) Peptidergic innervation and endocrine cells of insect midgut. J Arch Insect Bioch Physiol 22:113–132

    Article  Google Scholar 

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Acknowledgements

We thank the Núcleo de Microscopia e Microanálise (NMM, UFV) for letting us use the confocal microscope. We are grateful to Nágila Francinete Costa Secundino and Paulo Fillemon Paolucci Pimenta for their support with the reagents and use of scanning electron microscopes at the Instituto René Rachou, Fiocruz, MG.

Funding

This work was supported by the Universidade Federal de Viçosa, Comissão de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—support to RSMG; the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Fapemig; APQ-00560–17)—support to GFM, and by the National Institutes of Health (USA) R01AI031478 and the Bloomberg Philanthropies to MJL.

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  1. Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil

    Raquel S. M. Godoy, Renata C. Barbosa & Gustavo F. Martins

  2. Departamento de Bioquímica e Fisiologia, Universidade Federal de Pernambuco, Recife, Pernambuco, 50670-420, Brazil

    Thamara F. Procópio

  3. Fundação Oswaldo Cruz, Instituto René Rachou, Fiocruz, Belo Horizonte, Minas Gerais, 30190-002, Brazil

    Raquel S. M. Godoy & Breno A. Costa

  4. The W. Harry Feinstone Department of Molecular Microbiology and Immunology and Johns Hopkins Malaria Research Institute, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, 21205, USA

    Marcelo Jacobs-Lorena

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  1. Raquel S. M. Godoy
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  2. Renata C. Barbosa
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Correspondence to Raquel S. M. Godoy.

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This study was performed in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health and the Animal Use Manual (FIOCRUZ, Ministry of Health of Brazil, national decree, no. 3179). The protocol was approved by the Ethics Committee of Universidade Federal de Viçosa (UFV-Protocol 561/2016).

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Supplementary file1 Movie S1 Specificity of the FaRP immunoreactivity (green) in the midgut of late L4 of Aedes aegypti. The grid formed by the external circular muscles (ECMs) fused with the longitudinal muscles (LMs) are shown in a more external position in relation to the midgut epithelium; therefore, they are seen first in the z-stack video. The internal muscle (ICM) layer is more internal and shown above the ECM/LM grid. The FaRP immunoreactivity is inside ring-shaped structures attached to the mid-position of the ECM between two cruciform points (fusion regions of ECM and LM). (MOV 1129 KB)

Supplementary file2 Movie S2 Muscle framework (red) of the anterior midgut of early L4 of Aedes aegypti. The external circular muscle (ECM) layer is shown. (MP4 253 KB)

Supplementary file3 Movie S3. Muscle framework (red) of the anterior midgut of the early pupal Aedes aegypti. The external circular muscle (ECM) layer in the process of degeneration is shown. (MP4 424 KB)

Supplementary file4 Movie S4 Mitotic nuclei (green) in the internal circular muscle layer (ICM) of the early pupal midgut of Aedes aegypti. All labeled nuclei were found in the ICM bundles. No mitosis labeling was observed in the midgut epithelium. Red: midgut muscles; blue: cell nuclei. (MOV 626 KB)

Supplementary file5 Movie S5 Muscle framework (red) of the anterior midgut of adult female Aedes aegypti. The external circular muscle (ECM) layer is not present. (MP4 344 KB)

Supplementary file6 Table S1 List of A. aegypti FaRP genes and their products. (TIFF 14039 KB)

441_2021_3462_MOESM7_ESM.tiff

Supplementary file7 Fig. S1 FaRP and PH3 immunolabeling, neurite and neuron body identifications in immature stages of Aedes aegypti; and the absence of ECM layer in the adult mosquito. (a) FaRP-positive (green) small, rounded points (white arrow) in the posterior midgut of Aedes aegypti early L4. ICM: internal circular muscle layer. Red: midgut muscles; Blue: cell nuclei. (b) Mitotic nuclei (green) of regenerative cells (RCs) from the midgut epithelium in the early L4 of A. aegypti. DC: digestive cell nuclei. (c) 3D view of the FaRP immunoreactivity (green) in the grid formed by the presence of an external circular muscle (ECM) layer fused with the longitudinal muscle (LM) layers in the L4 of A. aegypti. Ring-shaped structures (arrow) are shown in the mid-position of the ECM just between two cruciform points (*) (where ECM fuses with LM). The internal circular muscle (ICM) fibers are shown between two ECM bundles. Red: midgut muscles. (d) Scanning electron microscopy (SEM) of the ring-shaped structures (white arrows) attached to the mid-position of the ECM between two cruciform points (*). Their extensions are also shown (black arrow). (e) FaRP-positive (green) small, rounded points (arrow) lined up and in close association with LM bundles in the anterior midgut of A. aegypti early pupa. (f–h) SEM of the early pupal (f) and early L4 (g, h) midgut, showing the region where the ICM bifurcates (full arrow), close to the two prominent longitudinal muscles (pLMs). (f) In the early pupa, it is difficult to identify the internal neurons using SEM, however, the predicted regions of their presence are shown with the thin arrows. (g, h) In the late L4, both bifurcations of the ICM (full arrow) and the internal neurons (thin arrows) are identified in g. Details of the ICM neurons are shown in h. (i) Midgut muscle organization (red) in the anterior midgut of the adult female of A. aegypti. The pLM; LM; and ICM bundles and their bifurcations (full arrow) are detected in a similar configuration of the larval midgut; however, the ECM is not present (no grids of cruciform regions are detected) (TIFF 5705 KB)

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Godoy, R.S.M., Barbosa, R.C., Procópio, T.F. et al. FMRF-related peptides in Aedes aegypti midgut: neuromuscular connections and enteric nervous system. Cell Tissue Res 385, 585–602 (2021). https://doi.org/10.1007/s00441-021-03462-3

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