Affinage

BOLL

Protein boule-like · UniProt Q8N9W6

Length
283 aa
Mass
31.3 kDa
Annotated
2026-06-09
100 papers in source corpus 18 papers cited in narrative 18 extracted findings
Cross-family judge vs UniProt: Affinage preferred faithfulness: 6/6 claims corpus-supported (100%)

Mechanistic narrative

Synthesis pass · prose summary of the discoveries below

BOLL (BOULE) encodes a germ-cell-specific RNA-binding protein that acts as a post-transcriptional regulator of meiotic progression and gamete differentiation, with a function conserved from insects to humans (PMID:10559904, PMID:9486791, PMID:12499397). Its core meiotic activity is translational control of CDC25-family phosphatases: Drosophila Boule promotes Twine translation to drive the G2-to-M meiotic transition (PMID:10559904), and human BOLL directly binds a 21-nucleotide U-rich element in the CDC25A 3'UTR to stimulate CDC25A translation without affecting mRNA stability, a mechanism whose disruption co-reduces BOLL and CDC25A in testes with meiotic arrest (PMID:19417033). BOLL forms homodimers and complexes with PUMILIO-2 (PUM2), thereby directing PUM2 to a distinct subset of RNA targets (PMID:15806553), and in mammalian testis it assembles into SDS-resistant amyloid-like aggregates that bind numerous spermatogenesis-related mRNAs (PMID:35965435). Functionally, BOLL acts at later germ-cell stages than its paralog DAZL: it promotes haploid gamete formation in human ES-derived germ cells (PMID:19865085) and is required for post-meiotic differentiation, since mouse Boule knockouts complete meiosis but arrest spermatid development at step 6 (PMID:20335278) and porcine BOLL deletion causes defective acrosome formation (PMID:32975846). Gonad-specific expression of BOLL is controlled by DNA methylation of its core promoter, with promoter hypermethylation repressing transcription and associating with infertility (PMID:27358391, PMID:26030766). In humans, reduced BOULE expression accompanies spermatogenic failure and meiotic arrest (PMID:19417033, PMID:17114206).

Mechanistic history

Synthesis pass · year-by-year structured walk · 8 steps
  1. 1998 Medium

    Established where Boule acts within the germ cell and its biochemical class, framing it as a cytoplasmic RNA-binding regulator of meiosis rather than a transcription factor.

    Evidence Immunolocalization and Y-chromosome deletion analysis in Drosophila testis; in vitro RNA-binding assay and cross-species transgenic rescue of Xenopus Xdazl in Drosophila boule mutants

    PMID:9486791 PMID:9882490

    Open questions at the time
    • Direct RNA targets not identified at this stage
    • Cytoplasmic mechanism (stability vs translation) inferred, not demonstrated
  2. 1999 High

    Identified the essential meiotic target of Boule, showing it controls the G2-to-M transition by promoting translation of the Cdc25 phosphatase Twine.

    Evidence Genetic epistasis and heterologous Twine rescue with protein quantification in Drosophila boule mutants

    PMID:10559904

    Open questions at the time
    • Direct RNA binding of Boule to twine mRNA not demonstrated in this study
    • Mechanism of translational activation unresolved
  3. 2003 High

    Demonstrated that human BOULE function is conserved across phyla, validating the fly model as relevant to human meiosis.

    Evidence Transgenic rescue of Drosophila boule mutant meiosis by human BOULE cDNA

    PMID:12499397

    Open questions at the time
    • Human RNA targets not addressed
    • Rescue does not establish endogenous human mechanism
  4. 2005 Medium

    Revealed the protein-interaction basis for target selection, showing BOLL homodimerizes and partners with PUM2 to define a distinct set of regulated RNAs.

    Evidence Co-immunoprecipitation, deletion-based domain mapping, and RNA target identification of the BOL-PUM2 complex

    PMID:15806553

    Open questions at the time
    • Single lab without reciprocal in vivo validation
    • Functional consequence of BOL-PUM2 target binding not measured
  5. 2009 High

    Defined the direct human molecular target and stage of action, distinguishing BOLL (later meiosis/haploid gametes) from DAZL (PGC formation).

    Evidence RNA-binding/IP mapping of a 21-nt CDC25A 3'UTR site, in vitro translation and mRNA-stability assays, clinical testis correlation; knockdown/overexpression in human ES-derived germ cells

    PMID:19417033 PMID:19865085

    Open questions at the time
    • Translational activation mechanism on CDC25A not structurally resolved
    • Full target repertoire beyond CDC25A undefined
  6. 2010 High

    Uncovered a post-meiotic role distinct from the canonical meiotic-entry function, showing Boule is required for spermatid differentiation in mice.

    Evidence Boule knockout mouse with stage-specific histology and Western blot for spermiogenesis regulators

    PMID:20335278

    Open questions at the time
    • The 'novel pathway' downstream of Boule in spermiogenesis unidentified
    • Spermiogenic RNA targets not defined
  7. 2016 Medium

    Established epigenetic control of BOULE, showing core-promoter DNA methylation represses transcription and underlies gonad-specific expression and infertility.

    Evidence Bisulfite sequencing across species, in vitro methylation and luciferase reporter assays, 5-Aza-dC treatment, and infertility correlation in human and bovine systems

    PMID:26030766 PMID:27358391

    Open questions at the time
    • Trans-acting factors reading the methylation state unidentified
    • Causality in human infertility is correlative
  8. 2022 Medium

    Showed BOULE adopts an amyloid-like aggregated state in testis that binds a broad set of spermatogenesis mRNAs, linking its biophysical behavior to RNA regulation.

    Evidence SDS-resistance assays, knockout validation, in vitro aggregation domain mapping, temperature dependence, and eCLIP-seq of testis aggregates

    PMID:35965435

    Open questions at the time
    • Functional consequence of aggregation on translation not established
    • Single lab; physiological role of temperature dependence unclear

Open questions

Synthesis pass · forward-looking unresolved questions
  • How BOLL mechanistically promotes translation of CDC25A and its spermiogenic targets, and how homodimerization, PUM2 partnering, and amyloid-like aggregation are integrated into a single regulatory mechanism, remains unresolved.
  • No structural model of BOLL on its U-rich RNA element
  • Spermiogenic target downstream of mouse Boule unidentified
  • Relationship between aggregated state and active translational control unknown

Mechanism profile

Synthesis pass · controlled-vocabulary classification · explore literature graph →
Molecular activity
GO:0003723 RNA binding 4 GO:0045182 translation regulator activity 2
Localization
GO:0005829 cytosol 1
Pathway
R-HSA-1474165 Reproduction 3 R-HSA-1640170 Cell Cycle 2 R-HSA-8953854 Metabolism of RNA 2
Partners

Evidence

Reading pass · 18 per-paper findings extracted from the source corpus
Year Finding Method Journal Conf PMIDs
1999 Drosophila Boule (ortholog of human BOLL/BOULE) post-transcriptionally regulates Twine (a Cdc25-type phosphatase) translation: boule mutations markedly reduce Twine protein expression from twine mRNA, and heterologous expression of Twine rescues the boule meiotic-entry defect, establishing that the essential function of Boule at the G2-to-M transition in meiosis is translational control of Twine. Genetic epistasis (double mutant analysis), rescue experiment (heterologous Twine expression in boule mutant flies), quantitative protein expression analysis Nature Cell Biology High 10559904
1998 Drosophila Boule protein undergoes biphasic subcellular localization during spermatogenesis: it localizes premeiotically to a perinucleolar region and then translocates to the cytoplasm at the onset of meiosis. Deletion of the Y chromosome ks-1 fertility locus eliminates Boule nuclear localization without perturbing meiotic entry, suggesting Boule acts in the cytoplasm to regulate mRNA stability or translation of an essential meiotic factor. Immunolocalization/subcellular fractionation in Drosophila testis; genetic deletion analysis (Y chromosome ks-1 locus) Developmental Biology Medium 9882490
1998 Xdazl (Xenopus DAZ-like, ortholog of BOLL/BOULE family) functions as an RNA-binding protein in vitro, and its cDNA rescues the boule meiotic entry phenotype in Drosophila boule mutant flies (restoring spindle formation, histone H3 phosphorylation, and meiotic cell division completion), demonstrating functional conservation of the meiotic RNA-binding role across species. In vitro RNA-binding assay; transgenic rescue of Drosophila boule mutant phenotype Development High 9486791
2003 Human BOULE transgene advances meiosis in infertile Drosophila boule mutant flies, demonstrating that human BOULE protein functionally substitutes for Drosophila Boule in regulating meiotic progression and that this function is conserved from flies to humans. Transgenic rescue experiment: human BOULE cDNA introduced into boule mutant Drosophila; meiotic progression assessed Human Molecular Genetics High 12499397
2009 Human DAZL functions in primordial germ-cell formation from human embryonic stem cells, whereas human BOULE (BOLL) promotes later stages of meiosis and development of haploid gametes, as established by silencing and overexpression of these genes in a germ-cell reporter system. Gene silencing (knockdown) and overexpression in human ES cell-derived germ cells; germ cell reporter quantification and isolation; flow cytometry Nature High 19865085
2010 Mouse Boule knockout reveals a novel role for Boule in spermiogenesis (differentiation of round spermatids into mature spermatozoa) rather than meiosis: meiosis completes normally in Boule-/- mice and haploid round spermatids form, but round spermatids arrest at step 6 and fail to differentiate into mature sperm; expression of key regulators of spermiogenesis is unaffected, suggesting Boule acts through a novel pathway. Knockout mouse generation (Boule-/- mice); histological analysis of spermatogenesis stages; Western blot for spermiogenesis regulators Human Molecular Genetics High 20335278
2009 Human BOLL protein specifically binds a 21-nucleotide region of the CDC25A 3'UTR (with a critical U-rich sequence within it), stimulates CDC25A translation without altering mRNA stability, and CDC25A and BOLL protein levels are co-reduced in human testes with spermatogenic failure/meiotic arrest, establishing post-transcriptional translational control of CDC25A by BOLL as a conserved fertility mechanism. RNA immunoprecipitation/binding assay (identification of 21-nt binding site in CDC25A 3'UTR); in vitro translation assay; mRNA stability assay; protein/mRNA expression correlation in human testis biopsies Journal of Clinical Endocrinology and Metabolism High 19417033
2005 Human BOL (BOULE) forms homodimers and interacts with PUMILIO homolog PUM2; the domain of BOL required for dimerization and PUM2 interaction was mapped. BOL and PUM2 form a complex on a subset of PUM2 RNA targets distinct from targets bound by PUM2-DAZL complexes, suggesting that BOL determines RNA target specificity of PUM2 through protein-protein interaction. Co-immunoprecipitation; domain mapping by deletion/mutagenesis; RNA-binding assays to identify RNA targets of BOL-PUM2 complex Molecular Reproduction and Development Medium 15806553
2008 In Drosophila, an isoform of Boule is expressed in the nervous system (not only testis), and forced overexpression of Boule in mushroom body gamma neurons inhibits developmental axon pruning. This activity requires both the RNA-binding domain and the conserved DAZ domain. Genetic analysis indicates Boule functions in the Cdc25 phosphatase (Twine) pathway in the nervous system as well as the germline. Genomic microarray (expression profiling); forced expression in mushroom body neurons; genetic epistasis (Boule overexpression + twine loss-of-function); domain deletion analysis Journal of Neuroscience Medium 18550751
2004 A nervous-system-expressed isoform of Drosophila Boule, when overexpressed, causes mutant phenotypes in neural communication (eye receptor-to-laminar cell signaling), altered larval locomotion, and reduced viability. Genetic studies indicate Boule functions via the Cdc25 phosphatase (Twine) pathway in the nervous system, and a twine loss-of-function mutation in a Boule-overexpression background reveals a role for Twine Cdc25 in the adult nervous system. Isoform-specific overexpression in Drosophila nervous system; electrophysiological/behavioral phenotypic analysis; genetic epistasis (Boule overexpression + twine loss-of-function) Journal of Neurogenetics Medium 15370196
2016 Promoters of BOULE and DAZL exhibit differential DNA methylation consistent with their gonad-specific expression; low promoter methylation in testicular tissue is attributed to spermatogenic cells; this conserved differential methylation is present in orthologous promoters of diverse species including mammals, chicken, and fish. Hypermethylation of BOULE promoter in human sperm is associated with human infertility, establishing epigenetic (DNA methylation) regulation as a mechanism controlling gonad-specific BOULE expression. Bisulfite sequencing; methylation analysis of testicular cell subpopulations; comparative genomics across species; correlation of promoter methylation with infertility phenotype FASEB Journal Medium 27358391
2022 Mouse BOULE forms SDS-resistant amyloid-like aggregates in testis during spermatogenesis; aggregate formation correlates with spermatogenic developmental stage and is absent in Boule knockout testis. A small region immediately downstream of the DAZ repeats is essential for in vitro aggregation, and aggregation positively correlates with temperature. Enhanced UV cross-linking immunoprecipitation of BOULE aggregates from mouse testes shows they bind numerous spermatogenesis-related mRNAs. SDS-PAGE resistance assay for aggregates; Boule knockout validation; domain mapping (in vitro aggregation with deletion constructs); temperature dependence assay; eCLIP-seq (enhanced UV cross-linking immunoprecipitation) of BOULE aggregates Journal of Biomedical Research Medium 35965435
2006 Three isoforms of human BOULE (B1, B2, B3) were identified, differing only in N-terminal sequences encoded by alternatively spliced exon 1. All three isoforms are exclusively expressed in human testes. Altered B1/B2 and B1/B3 transcript ratios correlate with reduced meiotic capacity of spermatocytes. BOULE mRNA reduction in meiotic arrest biopsies parallels absence of BOULE protein. RT-PCR identification of isoforms; quantitative RT-PCR in testis biopsies from infertile men; flow cytometry for meiotic capacity; immunohistochemistry for BOULE protein Molecular Human Reproduction Medium 17114206
2015 In Athalia rosae (haploid hymenopteran), Ar bol (boule ortholog) is exclusively expressed in testis when maturation divisions occur, and knockdown of all bol transcripts arrests the cell cycle before maturation divisions (shown by flow cytometry), prevents mature sperm formation, and blocks sperm differentiation. This is genetically upstream of Ar cdc25, as cdc25 knockdown alone permits partial sperm elongation. Thus boule is essential for meiotic entry and progression via cdc25 regulation even in haploid males. RNAi knockdown; flow cytometry for cell cycle analysis; stage-specific expression analysis; epistasis between bol and cdc25 knockdowns Developmental Biology Medium 25592223
2020 Deletion of porcine BOLL gene (55 kb deletion encompassing the BOLL locus) in Yorkshire boars in the homozygous state causes defective acrosome formation in sperm and subfertility, revealing a novel role for BOLL in acrosome formation during spermatogenesis in pigs. Genome sequencing; read depth/copy number analysis identifying 55 kb deletion; association mapping; phenotypic characterization of acrosome defects Animal Genetics Medium 32975846
2014 IGF1 increases BOULE mRNA expression in mouse testis via ERK1/2 signaling in a testosterone-independent pathway; antiandrogen flutamide abolished testosterone-induced BOULE mRNA increase but not IGF1-induced increase; ERK1/2 inhibitor U0126 prevented IGF1-induction of both BOULE and CDC25A mRNAs, placing IGF1-ERK1/2 signaling upstream of BOULE and CDC25A expression during spermatogenesis. In vitro testis incubation with hormones/inhibitors; RT-PCR/qPCR for BOULE and CDC25A mRNA; pharmacological inhibition (flutamide, U0126); immunohistochemical localization Reproductive Biology Low 25726377
2015 In vitro methylation of the bovine Boule core promoter by M.SssI methylase significantly decreases promoter activity; treatment of bovine cells with the methyltransferase inhibitor 5-Aza-dC dramatically increases bBoule transcription; the core promoter region of bBoule (107 bp) is hypermethylated in infertile cattle-yak hybrids with low bBoule expression, establishing that DNA methylation of the core promoter mechanistically represses bBoule transcription. In vitro methylation assay with M.SssI; luciferase reporter assay; 5-Aza-dC treatment; bisulfite sequencing PloS One Medium 26030766
2013 BOLL protein is expressed in the human fetal ovary at a developmental stage later than and almost mutually exclusive with DAZL, corresponding to later stages of meiotic prophase I; BOLL is subsequently downregulated as primordial follicles form and DAZL is re-expressed. In fetal mouse ovary, Boll is co-expressed with Dazl during oogenesis, showing species differences. This establishes BOLL as a meiotic-stage-specific protein in human female germ cells. Immunofluorescence/immunohistochemistry with stage markers in human and mouse fetal ovary; quantification of co-expression with meiosis markers PloS One Medium 24086306

Source papers

Stage 0 corpus · 100 papers · ranked by NIH iCite citations
Year Title Journal Citations PMID
2009 Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature 390 19865085
1998 A Xenopus DAZ-like gene encodes an RNA component of germ plasm and is a functional homologue of Drosophila boule. Development (Cambridge, England) 209 9486791
1999 Post-transcriptional regulation of the meiotic Cdc25 protein Twine by the Dazl orthologue Boule. Nature cell biology 134 10559904
2003 Human BOULE gene rescues meiotic defects in infertile flies. Human molecular genetics 104 12499397
1996 A SPGY copy homologous to the mouse gene Dazla and the Drosophila gene boule is autosomal and expressed only in the human male gonad. Human molecular genetics 95 8968755
2016 Construction of a high-density genetic map by specific locus amplified fragment sequencing (SLAF-seq) and its application to Quantitative Trait Loci (QTL) analysis for boll weight in upland cotton (Gossypium hirsutum.). BMC plant biology 82 27067834
1993 Cholesterol oxidase: a potent insecticidal protein active against boll weevil larvae. Biochemical and biophysical research communications 74 8250897
2014 Waterlogging during flowering and boll forming stages affects sucrose metabolism in the leaves subtending the cotton boll and its relationship with boll weight. Plant science : an international journal of experimental plant biology 72 24767118
2010 A novel requirement in mammalian spermatid differentiation for the DAZ-family protein Boule. Human molecular genetics 70 20335278
1998 Biphasic subcellular localization of the DAZL-related protein boule in Drosophila spermatogenesis. Developmental biology 70 9882490
1992 The boll weevil vitellogenin gene: nucleotide sequence, structure, and evolutionary relationship to nematode and vertebrate vitellogenin genes. Journal of molecular evolution 68 1593641
2009 Boule is present in fish and bisexually expressed in adult and embryonic germ cells of medaka. PloS one 67 19564913
1984 Olfaction in the boll weevil,Anthonomus grandis Boh. (Coleoptera: Curculionidae): Electroantennogram studies. Journal of chemical ecology 61 24318432
2020 Circular RNAs from BOULE play conserved roles in protection against stress-induced fertility decline. Science advances 58 33177084
2010 Widespread presence of human BOULE homologs among animals and conservation of their ancient reproductive function. PLoS genetics 53 20657660
2017 Nucleases as a barrier to gene silencing in the cotton boll weevil, Anthonomus grandis. PloS one 51 29261729
2012 Similar genetic basis of resistance to Bt toxin Cry1Ac in Boll-selected and diet-selected strains of pink bollworm. PloS one 47 22530065
2011 Differential conservation and divergence of fertility genes boule and dazl in the rainbow trout. PloS one 45 21253610
2016 Relationship between potassium fertilization and nitrogen metabolism in the leaf subtending the cotton (Gossypium hirsutum L.) boll during the boll development stage. Plant physiology and biochemistry : PPB 43 26874296
2008 Genomic analysis of Drosophila neuronal remodeling: a role for the RNA-binding protein Boule as a negative regulator of axon pruning. The Journal of neuroscience : the official journal of the Society for Neuroscience 43 18550751
2002 Molecular cloning and characterization of the cathepsin B-like proteinase from the cotton boll worm, Helicoverpa armigera. Insect molecular biology 43 12421414
2013 Transcriptome analysis in cotton boll weevil (Anthonomus grandis) and RNA interference in insect pests. PloS one 42 24386449
2017 Transgenic cotton expressing Cry10Aa toxin confers high resistance to the cotton boll weevil. Plant biotechnology journal 38 28081289
2011 Boule-like genes regulate male and female gametogenesis in the flatworm Macrostomum lignano. Developmental biology 36 21740899
2006 Association of three isoforms of the meiotic BOULE gene with spermatogenic failure in infertile men. Molecular human reproduction 34 17114206
2005 Interaction of the conserved meiotic regulators, BOULE (BOL) and PUMILIO-2 (PUM2). Molecular reproduction and development 33 15806553
2017 Carbohydrate metabolism in the subtending leaf cross-acclimates to waterlogging and elevated temperature stress and influences boll biomass in cotton (Gossypium hirsutum). Physiologia plantarum 31 28581029
2011 Improving Cry8Ka toxin activity towards the cotton boll weevil (Anthonomus grandis). BMC biotechnology 31 21906288
2007 Susceptibility of Anthonomus grandis (cotton boll weevil) and Spodoptera frugiperda (fall armyworm) to a cry1ia-type toxin from a Brazilian Bacillus thuringiensis strain. Journal of biochemistry and molecular biology 31 17927912
2014 Transcriptome analysis of Gossypium hirsutum flower buds infested by cotton boll weevil (Anthonomus grandis) larvae. BMC genomics 30 25280771
2007 Role of Pantoea agglomerans in opportunistic bacterial seed and boll rot of cotton (Gossypium hirsutum) grown in the field. Journal of applied microbiology 30 17184328
2013 Expression pattern of Boule in dairy goat testis and its function in promoting the meiosis in male germline stem cells (mGSCs). Journal of cellular biochemistry 28 22930651
2003 Molecular cloning of alpha-amylases from cotton boll weevil, Anthonomus grandis and structural relations to plant inhibitors: an approach to insect resistance. Journal of protein chemistry 28 12744224
2004 Messenger RNA transcripts of the meiotic regulator BOULE in the testis of azoospermic men and their application in predicting the success of sperm retrieval. Human reproduction (Oxford, England) 27 15591084
2010 Midgut GPI-anchored proteins with alkaline phosphatase activity from the cotton boll weevil (Anthonomus grandis) are putative receptors for the Cry1B protein of Bacillus thuringiensis. Insect biochemistry and molecular biology 26 20079436
2008 Recombinant Cry1Ia protein is highly toxic to cotton boll weevil (Anthonomus grandis Boheman) and fall armyworm (Spodoptera frugiperda). Journal of applied microbiology 24 18248369
2008 Cloning and characterization of the gene encoding the bovine BOULE protein. Molecular genetics and genomics : MGG 24 18987886
2021 Foliar melatonin stimulates cotton boll distribution characteristics by modifying leaf sugar metabolism and antioxidant activities during drought conditions. Physiologia plantarum 23 34405415
2016 Transgenic Cotton Plants Expressing Cry1Ia12 Toxin Confer Resistance to Fall Armyworm (Spodoptera frugiperda) and Cotton Boll Weevil (Anthonomus grandis). Frontiers in plant science 23 26925081
2013 A developmental stage-specific switch from DAZL to BOLL occurs during fetal oogenesis in humans, but not mice. PloS one 23 24086306
1997 Characterization and partial cloning of ecdysteroid receptor from a cotton boll weevil embryonic cell line. Archives of insect biochemistry and physiology 23 9131780
2015 The boule gene is essential for spermatogenesis of haploid insect male. Developmental biology 22 25592223
2015 Differential expression of fertility genes boule and dazl in Chinese sturgeon (Acipenser sinensis), a basal fish. Cell and tissue research 22 25592848
2016 Vitellogenin knockdown strongly affects cotton boll weevil egg viability but not the number of eggs laid by females. Meta gene 20 27419079
2006 Diversity of boll weevil populations in South America: a phylogeographic approach. Genetica 20 16636929
2006 Molecular genetic variation of boll weevil populations in North America estimated with microsatellites: implications for patterns of dispersal. Genetica 20 16850220
2005 Toxicity to cotton boll weevil Anthonomus grandis of a trypsin inhibitor from chickpea seeds. Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology 20 15649779
2004 Genetic structuring of boll weevil populations in the US based on RAPD markers. Insect molecular biology 20 15157230
2016 Highly conserved epigenetic regulation of BOULE and DAZL is associated with human fertility. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 19 27358391
2010 Histone and ribosomal RNA repetitive gene clusters of the boll weevil are linked in a tandem array. Insect molecular biology 19 20456508
2009 Posttranscriptional regulation of CDC25A by BOLL is a conserved fertility mechanism essential for human spermatogenesis. The Journal of clinical endocrinology and metabolism 19 19417033
2016 Overexpression of STRA8, BOULE, and DAZL Genes Promotes Goat Bone Marrow-Derived Mesenchymal Stem Cells In Vitro Transdifferentiation Toward Putative Male Germ Cells. Reproductive sciences (Thousand Oaks, Calif.) 18 27342271
2001 Replication of Chilo iridescent virus in the cotton boll weevil, Anthonomus grandis, and development of an infectivity assay. Archives of virology 18 11402862
2016 Germline Defects Caused by Smed-boule RNA-Interference Reveal That Egg Capsule Deposition Occurs Independently of Fertilization, Ovulation, Mating, or the Presence of Gametes in Planarian Flatworms. PLoS genetics 17 27149082
2011 CDY1 and BOULE transcripts assessed in the same biopsy as predictive markers for successful testicular sperm retrieval. Fertility and sterility 17 21474125
2004 Nervous system function for the testis RNA-binding protein boule in Drosophila. Journal of neurogenetics 16 15370196
2002 A hexamerin protein, AgSP-1, is associated with diapause in the boll weevil(1). Journal of insect physiology 16 12770051
1993 Proteolytic processing of the vitellogenin precursor in the boll weevil, Anthonomus grandis. Archives of insect biochemistry and physiology 16 8347856
2020 RNAi-Mediated Suppression of Laccase2 Impairs Cuticle Tanning and Molting in the Cotton Boll Weevil (Anthonomus grandis). Frontiers in physiology 15 33329040
2019 Induction of goat bone marrow mesenchymal stem cells into putative male germ cells using mRNA for STRA8, BOULE and DAZL. Cytotechnology 14 30767091
2016 Effect of Different Lignocellulosic Diets on Bacterial Microbiota and Hydrolytic Enzyme Activities in the Gut of the Cotton Boll Weevil (Anthonomus grandis). Frontiers in microbiology 14 28082962
2009 Isolation and characterization of farnesyl diphosphate synthase from the cotton boll weevil, Anthonomus grandis. Archives of insect biochemistry and physiology 14 19309001
2006 Evolutionary comparison of the reproductive genes, DAZL and BOULE, in primates with and without DAZ. Development genes and evolution 14 16425031
2021 Field-evolved resistance to beta-cyfluthrin in the boll weevil: Detection and characterization. Pest management science 13 33991055
2016 A premeiotic function for boule in the planarian Schmidtea mediterranea. Proceedings of the National Academy of Sciences of the United States of America 13 27330085
2014 Differential expression of boule and dazl in adult germ cells of the Asian seabass. Gene 13 25084124
2011 Boule and the Evolutionary Origin of Metazoan Gametogenesis: A Grandpa's Tale. International journal of evolutionary biology 13 21755049
2004 A diverse family of serine proteinase genes expressed in cotton boll weevil (Anthonomus grandis): implications for the design of pest-resistant transgenic cotton plants. Insect biochemistry and molecular biology 13 15350610
2019 Histomorphological Comparisons and Expression Patterns of BOLL Gene in Sheep Testes at Different Development Stages. Animals : an open access journal from MDPI 12 30901845
2009 Nitrophenolates spray can alter boll abscission rate in cotton through enhanced peroxidase activity and increased ascorbate and phenolics levels. Journal of plant physiology 12 19647335
2005 Mutations in the human BOULE gene are not a major cause of impaired spermatogenesis. Fertility and sterility 12 15705409
2003 Effect of ULV malathion use in boll weevil (Coleoptera: Curculionidae) eradication on resistance in the tarnished plant bug (Heteroptera: Miridae). Journal of economic entomology 12 12852634
2015 Epigenetic regulation of bovine spermatogenic cell-specific gene boule. PloS one 11 26030766
2024 Integrated analysis of the transcriptome and metabolome reveals the molecular mechanism regulating cotton boll abscission under low light intensity. BMC plant biology 10 38475753
2021 Direct reprogramming of human Sertoli cells into male germline stem cells with the self-renewal and differentiation potentials via overexpressing DAZL/DAZ2/BOULE genes. Stem cell reports 10 34653405
2020 Midgut Genes Knockdown by Oral dsRNA Administration Produces a Lethal Effect on Cotton Boll Weevil. Neotropical entomology 10 33025569
2018 Nitrogen (N) Application Gradually Enhances Boll Development and Decreases Boll Shell Insecticidal Protein Content in N-Deficient Cotton. Frontiers in plant science 10 29441082
2014 Cloning and expression of boule and dazl in the Nile tilapia (Oreochromis niloticus). Gene 10 24607036
2014 Identification and characterization of yak (Bos grunniens) b-Boule gene and its alternative splice variants. Gene 10 25149018
2014 IGF1 regulation of BOULE and CDC25A transcripts via a testosterone-independent pathway in spermatogenesis of adult mice. Reproductive biology 10 25726377
2023 Lint percentage and boll weight QTLs in three excellent upland cotton (Gossypium hirsutum): ZR014121, CCRI60, and EZ60. BMC plant biology 9 37020180
2023 Molecular Mechanism of Circ_0088300-BOLL Interaction Regulating Mitochondrial Metabolic Reprogramming and Involved in Gastric Cancer Growth and Metastasis. Journal of proteome research 9 37953520
2015 The Complexity of Posttranscriptional Small RNA Regulatory Networks Revealed by In Silico Analysis of Gossypium arboreum L. Leaf, Flower and Boll Small Regulatory RNAs. PloS one 9 26070200
2013 Expression of miR-34c in response to overexpression of Boule and Stra8 in dairy goat male germ line stem cells (mGSCs). Cell biochemistry and function 9 23508548
2019 Nicotiana benthamiana is a suitable transient system for high-level expression of an active inhibitor of cotton boll weevil α-amylase. BMC biotechnology 8 30849970
2015 Oncogenic Role of BOLL in Colorectal Cancer. Digestive diseases and sciences 8 25605553
1989 Receptor chirality and behavioral specificity of the boll weevil,Anthonomus grandis Boh. (Coleoptera: Curculionidae), for its pheromone, (+)-grandisol. Journal of chemical ecology 8 24271795
2023 Simultaneous silencing of juvenile hormone metabolism genes through RNAi interrupts metamorphosis in the cotton boll weevil. Frontiers in molecular biosciences 7 36950526
2022 RNA binding protein BOULE forms aggregates in mammalian testis. Journal of biomedical research 7 35965435
2021 Population genomics and phylogeography of the boll weevil, Anthonomus grandis Boheman (Coleoptera: Curculionidae), in the United States, northern Mexico, and Argentina. Evolutionary applications 7 34295363
2017 Selection of Bacillus thuringiensis strains toxic to cotton boll weevil (Anthonomus grandis, Coleoptera: Curculionidae) larvae. Revista Argentina de microbiologia 7 28495035
2015 Constitutively overexpressing a tomato fructokinase gene (LeFRK1) in cotton (Gossypium hirsutum L. cv. Coker 312) positively affects plant vegetative growth, boll number and seed cotton yield. Functional plant biology : FPB 7 32480732
2012 Field evaluation of Bt cotton crop impact on nontarget pests: cotton aphid and boll weevil. Neotropical entomology 7 23949719
2004 Molecular cloning of a cysteine proteinase cDNA from the cotton boll weevil Anthonomus grandis (Coleoptera: Curculionidae). Bioscience, biotechnology, and biochemistry 7 15215586
2023 A novel picorna-like virus identified in the cotton boll weevil Anthonomus grandis (Coleoptera: Curculionidae). Archives of virology 6 36598610
2020 Deletion of porcine BOLL is associated with defective acrosomes and subfertility in Yorkshire boars. Animal genetics 6 32975846
2018 Goat Boule: Isoforms identification, mRNA expression in testis and functional study and promoter methylation profiles. Theriogenology 6 29778921
2015 Stable integration and expression of a cry1Ia gene conferring resistance to fall armyworm and boll weevil in cotton plants. Pest management science 6 26558603
2012 Combining ability analysis for within-boll yield components in upland cotton (Gossypium hirsutum L.). Genetics and molecular research : GMR 6 23007974
2009 Phenotypic expression of partial AZFc deletions is independent of the variations in DAZL and BOULE in a Han population. Journal of andrology 6 19342699

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