Germ cells are essential to sexual reproduction. Across the animal kingdom, extracellular signaling isoprenoids, such as retinoic acids (RAs) in vertebrates and juvenile hormones (JHs) in invertebrates, facilitate multiple processes in reproduction. Here we investigated the role of these potent signaling molecules in embryonic germ cell development, using JHs in Drosophila melanogaster as a model system. In contrast to their established endocrine roles during larval and adult germline development, we found that JH signaling acts locally during embryonic development. Using an in vivo biosensor, we observed active JH signaling first within and near primordial germ cells (PGCs) as they migrate to the developing gonad. Through in vivo and in vitro assays, we determined that JHs are both necessary and sufficient for PGC migration. Analysis into the mechanisms of this newly uncovered paracrine JH function revealed that PGC migration was compromised when JHs were decreased or increased, suggesting that specific titers or spatiotemporal JH dynamics are required for robust PGC colonization of the gonad. Compromised PGC migration can impair fertility and cause germ cell tumors in many species, including humans. In mammals, retinoids have many roles in development and reproduction. We found that like JHs in Drosophila, RA was sufficient to impact mouse PGC migration in vitro. Together, our study reveals a previously unanticipated role of isoprenoids as local effectors of pre-gonadal PGC development and suggests a broadly shared mechanism in PGC migration.

Department of Biological Sciences and Biomolecular Sciences Institute Florida International University 11200 SW 8 Street Miami FL 33199 USA; Department of Parasitology University of South Bohemia 37005 České Budějovice Czech Republic

Department of Biological Sciences and Biomolecular Sciences Institute Florida International University 11200 SW 8 Street Miami FL 33199 USA; Institute of Parasitology Biology Centre CAS 37005 Ceske Budejovice Czech Republic

Department of Cell Biology Skirball Institute of Biomolecular Medicine and Howard Hughes Medical Institute NYU Grossman School of Medicine 540 1st Avenue New York NY 10016 USA

Department of Cell Biology Skirball Institute of Biomolecular Medicine and Howard Hughes Medical Institute NYU Grossman School of Medicine 540 1st Avenue New York NY 10016 USA; Department of Neuroscience Developmental and Regenerative Biology University of Texas at San Antonio One UTSA Circle San Antonio TX 78249 USA

Department of Cell Biology Skirball Institute of Biomolecular Medicine and Howard Hughes Medical Institute NYU Grossman School of Medicine 540 1st Avenue New York NY 10016 USA; Whitehead Institute for Biomedical Research and Department of Biology Massachusetts Institute of Technology 455 Main Street Cambridge MA 02142 USA

Sanford 1 Weill Department of Medicine Weill Cornell Medicine 413 E 69th Street New York NY USA

Komentář v

Curr Biol. 2024 Feb 5;34(3):R84-R86. doi: 10.1016/j.cub.2023.12.026. PubMed

Zobrazit více v PubMed

Saitou M, and Hayashi K (2021). Mammalian in vitro gametogenesis. Science 374, eaaz6830. 10.1126/science.aaz6830. PubMed DOI

Misawa N, Takemura M, and Maoka T (2021). Carotenoid Biosynthesis in Animals: Case of Arthropods. Adv Exp Med Biol 1261, 217–220. 10.1007/978-981-15-7360-6_19. PubMed DOI

Finger DS, Whitehead KM, Phipps DN, and Ables ET (2021). Nuclear receptors linking physiology and germline stem cells in Drosophila. Vitam Horm 116, 327–362. 10.1016/bs.vh.2020.12.008. PubMed DOI PMC

Banisch TU, Slaidina M, Gupta S, Ho MG, Gilboa L, and Lehmann R (2021). A transitory signaling center controls timing of primordial germ cell differentiation. Dev Cell 56, 1742–+. 10.1016/j.devcel.2021.05.008. PubMed DOI PMC

Bai JW, Uehara Y, and Montell DJ (2000). Regulation of invasive cell behavior by taiman, a Drosophila protein related to AlB1, a steroid receptor coactivator amplified in breast cancer. Cell 103, 1047–1058. Doi 10.1016/S0092-8674(00)00208-7. PubMed DOI

Hodin J, and Riddiford LM (1998). The ecdysone receptor and ultraspiracle regulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis. Dev Genes Evol 208, 304–317. DOI 10.1007/s004270050186. PubMed DOI

Olmstead AW, and Leblanc GA (2002). Juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna. J Exp Zool 293, 736–739. 10.1002/jez.10162. PubMed DOI

Roy S, Saha TT, Zou Z, and Raikhel AS (2018). Regulatory Pathways Controlling Female Insect Reproduction. Annu Rev Entomol 63, 489–511. 10.1146/annurev-ento-020117-043258. PubMed DOI

Santos CG, Humann FC, and Hartfelder K (2019). Juvenile hormone signaling in insect oogenesis. Curr Opin Insect Sci 31, 43–48. 10.1016/j.cois.2018.07.010. PubMed DOI

Luo W, Veeran S, Wang J, Li S, Li K, and Liu SN (2020). Dual roles of juvenile hormone signaling during early oogenesis in Drosophila. Insect Sci 27, 665–674. 10.1111/1744-7917.12698. PubMed DOI

Easwaran S, Van Ligten M, Kui M, and Montell DJ (2022). Enhanced germline stem cell longevity in Drosophila diapause. Nat Commun 13, 711. 10.1038/s41467-022-28347-z. PubMed DOI PMC

Hiruma K, and Kaneko Y (2013). Hormonal Regulation of Insect Metamorphosis with Special Reference to Juvenile Hormone Biosynthesis. Curr Top Dev Biol 103, 73–100. 10.1016/B978-0-12-385979-2.00003-4. PubMed DOI

Riddiford LM (2020). Rhodnius, Golden Oil, and Met: A History of Juvenile Hormone Research. Front Cell Dev Biol 8, 679. 10.3389/fcell.2020.00679. PubMed DOI PMC

Jindra M, Tumova S, Milacek M, and Bittova L (2021). A decade with the juvenile hormone receptor. Adv Insect Physiol 60, 37–85. 10.1016/bs.aiip.2021.03.001. DOI

Abdou MA, He QY, Wen D, Zyaan O, Wang J, Xu JJ, Baumann AA, Joseph J, Wilson TG, Li S, and Wang J (2011). Drosophila Met and Gce are partially redundant in transducing juvenile hormone action. Insect Biochem Molec 41, 938–945. 10.1016/j.ibmb.2011.09.003. PubMed DOI

Jindra M, Uhlirova M, Charles JP, Smykal V, and Hill RJ (2015). Genetic Evidence for Function of the bHLH-PAS Protein Gce/Met As a Juvenile Hormone Receptor. PLoS Genet 11, e1005394. 10.1371/journal.pgen.1005394. PubMed DOI PMC

Jindra M, Belles X, and Shinoda T (2015). Molecular basis of juvenile hormone signaling. Curr Opin Insect Sci 11, 39–46. 10.1016/j.cois.2015.08.004. PubMed DOI

Niwa R, Niimi T, Honda N, Yoshiyama M, Itoyama K, Kataoka H, and Shinoda T (2008). Juvenile hormone acid O-methyltransferase in Drosophila melanogaster. Insect Biochem Molec 38, 714–720. 10.1016/j.ibmb.2008.04.003. PubMed DOI

Van Doren M, Broihier HT, Moore LA, and Lehmann R (1998). HMG-CoA reductase guides migrating primordial germ cells. Nature 396, 466–469. 10.1038/24871. PubMed DOI

Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, and Page DC (2006). Retinoic acid regulates sex-specific timing of meiotic initiation in mice. P Natl Acad Sci USA 103, 2474–2479. 10.1073/pnas.0510813103. PubMed DOI PMC

Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro K, Chawengsaksophak K, Wilson MJ, Rossant J, et al. (2006). Retinoid signaling determines germ cell fate in mice. Science 312, 596–600. 10.1126/science.1125691. PubMed DOI

Bowles J, Feng CW, Miles K, Ineson J, Spiller C, and Koopman P (2016). ALDH1A1 provides a source of meiosis-inducing retinoic acid in mouse fetal ovaries. Nature Communications 7. ARTN 10845 10.1038/ncomms10845. PubMed DOI PMC

Noriega FG, Shah DK, and Wells MA (1997). Juvenile hormone controls early trypsin gene transcription in the midgut of Aedes aegypti. Insect Mol Biol 6, 63–66. DOI 10.1046/j.1365-2583.1997.00154.x. PubMed DOI

Ramirez CE, Nouzova M, Michalkova V, Fernandez-Lima F, and Noriega FG (2020). Common structural features facilitate the simultaneous identification and quantification of the five most common juvenile hormones by liquid chromatography-tandem mass spectrometry. Insect Biochem Mol Biol 116, 103287. 10.1016/j.ibmb.2019.103287. PubMed DOI PMC

Wen D, Rivera-Perez C, Abdou M, Jia Q, He Q, Liu X, Zyaan O, Xu J, Bendena WG, Tobe SS, et al. (2015). Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis. PLoS Genet 11, e1005038. 10.1371/journal.pgen.1005038. PubMed DOI PMC

Burtenshaw SM, Su PP, Zhang JR, Tobe SS, Dayton L, and Bendena WG (2008). A putative farnesoic acid O-methyltransferase (FAMeT) orthologue in Drosophila melanogaster (CG10527): relationship to juvenile hormone biosynthesis? Peptides 29, 242–251. 10.1016/j.peptides.2007.10.030. PubMed DOI

Zhang H, Tian L, Tobe S, Xiong Y, Wang S, Lin X, Liu Y, Bendena W, Li S, and Zhang YQ (2010). Drosophila CG10527 mutants are resistant to juvenile hormone and its analog methoprene. Biochem Biophys Res Commun 401, 182–187. 10.1016/j.bbrc.2010.09.019. PubMed DOI

Kenwrick K, Mukherjee A, and Renault AD (2019). Hmgcr promotes a long-range signal to attract Drosophila germ cells independently of Hedgehog. J Cell Sci 132. 10.1242/jcs.232637. PubMed DOI

Santos AC, and Lehmann R (2004). Isoprenoids control germ cell migration downstream of HMGCoA reductase. Dev Cell 6, 283–293. 10.1016/s1534-5807(04)00023-1. PubMed DOI

Ricardo S, and Lehmann R (2009). An ABC transporter controls export of a Drosophila germ cell attractant. Science 323, 943–946. 10.1126/science.1166239. PubMed DOI PMC

Yamamoto R, Bai H, Dolezal AG, Amdam G, and Tatar M (2013). Juvenile hormone regulation of Drosophila aging. BMC Biol 11, 85. 10.1186/1741-7007-11-85. PubMed DOI PMC

Liu P, Peng HJ, and Zhu J (2015). Juvenile hormone-activated phospholipase C pathway enhances transcriptional activation by the methoprene-tolerant protein. Proceedings of the National Academy of Sciences of the United States of America 112, E1871–1879. 10.1073/pnas.1423204112. PubMed DOI PMC

Wilson TG, Wang S, Beno M, and Farkas R (2006). Wide mutational spectrum of a gene involved in hormone action and insecticide resistance in Drosophila melanogaster. Mol Genet Genomics 276, 294–303. 10.1007/s00438-006-0138-4. PubMed DOI

Luo W, Liu SN, Zhang WQ, Yang L, Huang JH, Zhou ST, Feng QL, Palli SR, Wang J, Roth S, and Li S (2021). Juvenile hormone signaling promotes ovulation and maintains egg shape by inducing expression of extracellular matrix genes. P Natl Acad Sci USA 118. ARTN e2104461118 10.1073/pnas.2104461118. PubMed DOI PMC

Bensaude O (2011). Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity? Transcription 2, 103–108. 10.4161/trns.2.3.16172. PubMed DOI PMC

Clagett-Dame M, and Knutson D (2011). Vitamin A in reproduction and development. Nutrients 3, 385–428. 10.3390/nu3040385. PubMed DOI PMC

Busada JT, Chappell VA, Niedenberger BA, Kaye EP, Keiper BD, Hogarth CA, and Geyer CB (2015). Retinoic acid regulates Kit translation during spermatogonial differentiation in the mouse. Dev Biol 397, 140–149. 10.1016/j.ydbio.2014.10.020. PubMed DOI PMC

Ghyselinck NB, and Duester G (2019). Retinoic acid signaling pathways. Development 146. 10.1242/dev.167502. PubMed DOI PMC

Harmon MA, Boehm MF, Heyman RA, and Mangelsdorf DJ (1995). Activation of mammalian retinoid X receptors by the insect growth regulator methoprene. Proceedings of the National Academy of Sciences of the United States of America 92, 6157–6160. PubMed PMC

Knaut H, Werz C, Geisler R, Nusslein-Volhard C, and Tubingen Screen C (2003). A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 421, 279–282. 10.1038/nature01338. PubMed DOI

Doitsidou M, Reichman-Fried M, Stebler J, Koprunner M, Dorries J, Meyer D, Esguerra CV, Leung T, and Raz E (2002). Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111, 647–659. 10.1016/s0092-8674(02)01135-2. PubMed DOI

Molyneaux KA, Zinszner H, Kunwar PS, Schaible K, Stebler J, Sunshine MJ, O’Brien W, Raz E, Littman D, Wylie C, and Lehmann R (2003). The chemokine SDF1/CXCL12 and its receptor CXCR4 regulate mouse germ cell migration and survival. Development 130, 4279–4286. 10.1242/dev.00640. PubMed DOI

Koshimizu U, Watanabe M, and Nakatsuji N (1995). Retinoic acid is a potent growth activator of mouse primordial germ cells in vitro. Developmental biology 168, 683–685. 10.1006/dbio.1995.1113. PubMed DOI

Campos-Ortega JA, and Hartenstein V (1997). The embryonic development of Drosophila melanogaster, 2nd Edition (Springer; ).

De Velasco B, Shen J, Go S, and Hartenstein V (2004). Embryonic development of the Drosophila corpus cardiacum, a neuroendocrine gland with similarity to the vertebrate pituitary, is controlled by sine oculis and glass. Dev Biol 274, 280–294. 10.1016/j.ydbio.2004.07.015. PubMed DOI

Pecasse F, Beck Y, Ruiz C, and Richards G (2000). Kruppel-homolog, a stage-specific modulator of the prepupal ecdysone response, is essential for Drosophila metamorphosis. Dev Biol 221, 53–67. 10.1006/dbio.2000.9687. PubMed DOI

Graveley BR, Brooks AN, Carlson JW, Duff MO, Landolin JM, Yang L, Artieri CG, van Baren MJ, Boley N, Booth BW, et al. (2011). The developmental transcriptome of Drosophila melanogaster. Nature 471, 473–479. 10.1038/nature09715. PubMed DOI PMC

Rahman MM, Franch-Marro X, Maestro JL, Martin D, and Casali A (2017). Local Juvenile Hormone activity regulates gut homeostasis and tumor growth in adult Drosophila. Sci Rep-Uk 7. ARTN 1167710.1038/s41598-017-11199-9. PubMed DOI PMC

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

Tomancak P, Beaton A, Weiszmann R, Kwan E, Shu S, Lewis SE, Richards S, Ashburner M, Hartenstein V, Celniker SE, and Rubin GM (2002). Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol 3, RESEARCH0088. 10.1186/gb-2002-3-12-research0088. PubMed DOI PMC

Tomancak P, Berman BP, Beaton A, Weiszmann R, Kwan E, Hartenstein V, Celniker SE, and Rubin GM (2007). Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol 8, R145. 10.1186/gb-2007-8-7-r145. PubMed DOI PMC

Hammonds AS, Bristow CA, Fisher WW, Weiszmann R, Wu S, Hartenstein V, Kellis M, Yu B, Frise E, and Celniker SE (2013). Spatial expression of transcription factors in Drosophila embryonic organ development. Genome Biol 14, R140. 10.1186/gb-2013-14-12-r140. PubMed DOI PMC

Qu Z, Bendena WG, Nong W, Siggens KW, Noriega FG, Kai ZP, Zang YY, Koon AC, Chan HYE, Chan TF, et al. (2017). MicroRNAs regulate the sesquiterpenoid hormonal pathway in Drosophila and other arthropods. Proc Biol Sci 284. 10.1098/rspb.2017.1827. PubMed DOI PMC

Zhang J, Wen D, Li EY, Palli SR, Li S, Wang J, and Liu S (2021). MicroRNA miR-8 promotes cell growth of corpus allatum and juvenile hormone biosynthesis independent of insulin/IGF signaling in Drosophila melanogaster. Insect Biochem Mol Biol 136, 103611. 10.1016/j.ibmb.2021.103611. PubMed DOI

Ilenchuk TT, and Davey KG (1987). The Development of Responsiveness to Juvenile-Hormone in the Follicle Cells of Rhodnius-Prolixus. Insect Biochem 17, 525–529. Doi 10.1016/0020-1790(87)90050-3. DOI

Yamamoto K, Chadarevian A, and Pellegrini M (1988). Juvenile-Hormone Action Mediated in Male Accessory-Glands of Drosophila by Calcium and Kinase-C. Science 239, 916–919. DOI 10.1126/science.3124270. PubMed DOI

Sevala VL, and Davey KG (1989). Action of Juvenile-Hormone on the Follicle Cells of Rhodnius-Prolixus - Evidence for a Novel Regulatory Mechanism Involving Protein Kinase-C. Experientia 45, 355–356. Doi 10.1007/Bf01957476. DOI

Pszczolkowski MA, Peterson A, Srinivasan A, and Ramaswamy SB (2005). Pharmacological analysis of ovarial patency in Heliothis virescens. J Insect Physiol 51, 445–453. 10.1016/j.jinsphys.2005.01.008. PubMed DOI

Zheng H, Wang N, Yun J, Xu H, Yang J, and Zhou S (2022). Juvenile hormone promotes paracellular transport of yolk proteins via remodeling zonula adherens at tricellular junctions in the follicular epithelium. PLoS Genet 18, e1010292. 10.1371/journal.pgen.1010292. PubMed DOI PMC

Cai MJ, Liu W, Pei XY, Li XR, He HJ, Wang JX, and Zhao XF (2014). Juvenile hormone prevents 20-hydroxyecdysone-induced metamorphosis by regulating the phosphorylation of a newly identified broad protein. J Biol Chem 289, 26630–26641. 10.1074/jbc.M114.581876. PubMed DOI PMC

Jing YP, An H, Zhang S, Wang N, and Zhou S (2018). Protein kinase C mediates juvenile hormone-dependent phosphorylation of Na(+)/K(+)-ATPase to induce ovarian follicular patency for yolk protein uptake. J Biol Chem 293, 20112–20122. 10.1074/jbc.RA118.005692. PubMed DOI PMC

Ojani R, Liu P, Fu X, and Zhu J (2016). Protein kinase C modulates transcriptional activation by the juvenile hormone receptor methoprene-tolerant. Insect Biochem Mol Biol 70, 44–52. 10.1016/j.ibmb.2015.12.001. PubMed DOI PMC

Lin B, Luo J, and Lehmann R (2020). Collectively stabilizing and orienting posterior migratory forces disperses cell clusters in vivo. Nat Commun 11, 4477. 10.1038/s41467-020-18185-2. PubMed DOI PMC

Leyria J, Orchard I, and Lange AB (2022). Impact of JH Signaling on Reproductive Physiology of the Classical Insect Model, Rhodnius prolixus. Int J Mol Sci 23. 10.3390/ijms232213832. PubMed DOI PMC

Leyria J, Benrabaa S, Nouzova M, Noriega FG, Tose LV, Fernandez-Lima F, Orchard I, and Lange AB (2022). Crosstalk between Nutrition, Insulin, Juvenile Hormone, and Ecdysteroid Signaling in the Classical Insect Model, Rhodnius prolixus. Int J Mol Sci 24. 10.3390/ijms24010007. PubMed DOI PMC

Hammal F, de Langen P, Bergon A, Lopez F, and Ballester B (2022). ReMap 2022: a database of Human, Mouse, Drosophila and Arabidopsis regulatory regions from an integrative analysis of DNA-binding sequencing experiments. Nucleic Acids Res 50, D316–D325. 10.1093/nar/gkab996. PubMed DOI PMC

Liu S, Li K, Gao Y, Liu X, Chen W, Ge W, Feng Q, Palli SR, and Li S (2018). Antagonistic actions of juvenile hormone and 20-hydroxyecdysone within the ring gland determine developmental transitions in Drosophila. Proc Natl Acad Sci U S A 115, 139–144. 10.1073/pnas.1716897115. PubMed DOI PMC

Zhang T, Song W, Li Z, Qian W, Wei L, Yang Y, Wang W, Zhou X, Meng M, Peng J, et al. (2018). Kruppel homolog 1 represses insect ecdysone biosynthesis by directly inhibiting the transcription of steroidogenic enzymes. Proc Natl Acad Sci U S A 115, 3960–3965. 10.1073/pnas.1800435115. PubMed DOI PMC

Riddiford LM, Truman JW, and Nern A (2018). Juvenile hormone reveals mosaic developmental programs in the metamorphosing optic lobe of Drosophila melanogaster. Biol Open 7. 10.1242/bio.034025. PubMed DOI PMC

Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, and Song SY (2004). Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527–538. 10.1016/j.immuni.2004.08.011. PubMed DOI

Kim MH, Taparowsky EJ, and Kim CH (2015). Retinoic Acid Differentially Regulates the Migration of Innate Lymphoid Cell Subsets to the Gut. Immunity 43, 107–119. 10.1016/j.immuni.2015.06.009. PubMed DOI PMC

Irie N, Lee SM, Lorenzi V, Xu H, Chen J, Inoue M, Kobayashi T, Sancho-Serra C, Drousioti E, Dietmann S, et al. (2023). DMRT1 regulates human germline commitment. Nat Cell Biol 25, 1439–1452. 10.1038/s41556-023-01224-7. PubMed DOI PMC

Al Tanoury Z, Piskunov A, and Rochette-Egly C (2013). Vitamin A and retinoid signaling: genomic and nongenomic effects. J Lipid Res 54, 1761–1775. 10.1194/jlr.R030833. PubMed DOI PMC

Rand CD, Spencer GE, and Carlone RL (2017). Retinoic acid as a chemoattractant for cultured embryonic spinal cord neurons of the African Clawed Frog, Xenopus laevis. Can J Zool 95, 653–661. 10.1139/cjz-2016-0279. DOI

Farrar NR, Dmetrichuk JM, Carlone RL, and Spencer GE (2009). A Novel, Nongenomic Mechanism Underlies Retinoic Acid-Induced Growth Cone Turning. J Neurosci 29, 14136–14142. 10.1523/Jneurosci.2921-09.2009. PubMed DOI PMC

Vesprini ND, Dawson TF, Yuan Y, Bruce D, and Spencer GE (2015). Retinoic acid affects calcium signaling in adult molluscan neurons. J Neurophysiol 113, 172–181. 10.1152/jn.00458.2014. PubMed DOI PMC

Johnson A, Nasser TIN, and Spencer GE (2019). Inhibition of Rho GTPases in Invertebrate Growth Cones Induces a Switch in Responsiveness to Retinoic Acid. Biomolecules 9. ARTN 460 10.3390/biom9090460. PubMed DOI PMC

de Hoog E, Lukewich MK, and Spencer GE (2019). Retinoid receptor-based signaling plays a role in voltage-dependent inhibition of invertebrate voltage-gated Ca2+ channels. J Biol Chem 294, 10076–10093. 10.1074/jbc.RA118.006444. PubMed DOI PMC

Casper AL, and Van Doren M (2009). The establishment of sexual identity in the Drosophila germline. Development 136, 3821–3830. 10.1242/dev.042374. PubMed DOI PMC

Gramates LS, Agapite J, Attrill H, Calvi BR, Crosby MA, dos Santos G, Goodman JL, Goutte-Gattat D, Jenkins VK, Kaufman T, et al. (2022). FlyBase: a guided tour of highlighted features. Genetics 220. ARTN iyac035 10.1093/genetics/iyac035. PubMed DOI PMC

Taylor SC, Nadeau K, Abbasi M, Lachance C, Nguyen M, and Fenrich J (2019). The Ultimate qPCR Experiment: Producing Publication Quality, Reproducible Data the First Time. Trends Biotechnol 37, 761–774. 10.1016/j.tibtech.2018.12.002. PubMed DOI

Moore LA, Broihier HT, Van Doren M, Lunsford LB, and Lehmann R (1998). Identification of genes controlling germ cell migration and embryonic gonad formation in Drosophila. Development 125, 667–678. PubMed

Sano H, Renault AD, and Lehmann R (2005). Control of lateral migration and germ cell elimination by the Drosophila melanogaster lipid phosphate phosphatases Wunen and Wunen 2. J Cell Biol 171, 675–683. 10.1083/jcb.200506038. PubMed DOI PMC

Baumann AA, Texada MJ, Chen HM, Etheredge JN, Miller DL, Picard S, Warner R, Truman JW, and Riddiford LM (2017). Genetic tools to study juvenile hormone action in Drosophila. Sci Rep 7, 2132. 10.1038/s41598-017-02264-4. PubMed DOI PMC

Restifo LL, and Wilson TG (1998). A juvenile hormone agonist reveals distinct developmental pathways mediated by ecdysone-inducible broad complex transcription factors. Dev Genet 22, 141–159. 10.1002/(SICI)1520-6408(1998)22:2<141::AID-DVG4>3.0.CO;2-6. PubMed DOI

Yoshimizu T, Sugiyama N, De Felice M, Yeom YI, Ohbo K, Masuko K, Obinata M, Abe K, Scholer HR, and Matsui Y (1999). Germline-specific expression of the Oct-4/green fluorescent protein (GFP) transgene in mice. Dev Growth Differ 41, 675–684. 10.1046/j.1440-169x.1999.00474.x. PubMed DOI

Lecuyer E, Necakov AS, Caceres L, and Krause HM (2008). High-resolution fluorescent in situ hybridization of Drosophila embryos and tissues. CSH Protoc 2008, pdb prot5019. 10.1101/pdb.prot5019. PubMed DOI

Barton LJ, Duan T, Ke W, Luttinger A, Lovander KE, Soshnev AA, and Geyer PK (2018). Nuclear lamina dysfunction triggers a germline stem cell checkpoint. Nat Commun 9, 3960. 10.1038/s41467-018-06277-z. PubMed DOI PMC

Celniker SE, Dillon LA, Gerstein MB, Gunsalus KC, Henikoff S, Karpen GH, Kellis M, Lai EC, Lieb JD, MacAlpine DM, et al. (2009). Unlocking the secrets of the genome. Nature 459, 927–930. 10.1038/459927a. PubMed DOI PMC

The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis

Differential gene expression and microRNA profile in corpora allata-corpora cardiaca of Aedes aegypti mosquitoes with weak juvenile hormone signalling

The embryonic role of juvenile hormone in the firebrat, Thermobia domestica, reveals its function before its involvement in metamorphosis