The mechanoreceptor Piezo is required for spermatogenesis in Bombyx mori.
Bombyx mori
Piezo
Ale fertility
Permatogenesis
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
20 May 2024
20 May 2024
Historique:
received:
15
12
2023
accepted:
10
05
2024
medline:
21
5
2024
pubmed:
21
5
2024
entrez:
20
5
2024
Statut:
epublish
Résumé
The animal sperm shows high diversity in morphology, components, and motility. In the lepidopteran model insect, the silkworm Bombyx mori, two types of sperm, including nucleate fertile eupyrene sperm and anucleate unfertile apyrene sperm, are generated. Apyrene sperm assists fertilization by facilitating the migration of eupyrene spermatozoa from the bursa copulatrix to the spermatheca. During spermatogenesis, eupyrene sperm bundles extrude the cytoplasm by peristaltic squeezing, while the nuclei of the apyrene sperm bundles are discarded with the same process, forming matured sperm. In this study, we describe that a mechanoreceptor BmPiezo, the sole Piezo ortholog in B. mori, plays key roles in larval feeding behavior and, more importantly, is essential for eupyrene spermatogenesis and male fertility. CRISPR/Cas9-mediated loss of BmPiezo function decreases larval appetite and subsequent body size and weight. Immunofluorescence analyses reveal that BmPiezo is intensely localized in the inflatable point of eupyrene sperm bundle induced by peristaltic squeezing. BmPiezo is also enriched in the middle region of apyrene sperm bundle before peristaltic squeezing. Cytological analyses of dimorphic sperm reveal developmental arrest of eupyrene sperm bundles in BmPiezo mutants, while the apyrene spermatogenesis is not affected. RNA-seq analysis and q-RT-PCR analyses demonstrate that eupyrene spermatogenic arrest is associated with the dysregulation of the actin cytoskeleton. Moreover, we show that the deformed eupyrene sperm bundles fail to migrate from the testes, resulting in male infertility due to the absence of eupyrene sperm in the bursa copulatrix and spermatheca. In conclusion, our studies thus uncover a new role for Piezo in regulating spermatogenesis and male fertility in insects.
Sections du résumé
BACKGROUND
BACKGROUND
The animal sperm shows high diversity in morphology, components, and motility. In the lepidopteran model insect, the silkworm Bombyx mori, two types of sperm, including nucleate fertile eupyrene sperm and anucleate unfertile apyrene sperm, are generated. Apyrene sperm assists fertilization by facilitating the migration of eupyrene spermatozoa from the bursa copulatrix to the spermatheca. During spermatogenesis, eupyrene sperm bundles extrude the cytoplasm by peristaltic squeezing, while the nuclei of the apyrene sperm bundles are discarded with the same process, forming matured sperm.
RESULTS
RESULTS
In this study, we describe that a mechanoreceptor BmPiezo, the sole Piezo ortholog in B. mori, plays key roles in larval feeding behavior and, more importantly, is essential for eupyrene spermatogenesis and male fertility. CRISPR/Cas9-mediated loss of BmPiezo function decreases larval appetite and subsequent body size and weight. Immunofluorescence analyses reveal that BmPiezo is intensely localized in the inflatable point of eupyrene sperm bundle induced by peristaltic squeezing. BmPiezo is also enriched in the middle region of apyrene sperm bundle before peristaltic squeezing. Cytological analyses of dimorphic sperm reveal developmental arrest of eupyrene sperm bundles in BmPiezo mutants, while the apyrene spermatogenesis is not affected. RNA-seq analysis and q-RT-PCR analyses demonstrate that eupyrene spermatogenic arrest is associated with the dysregulation of the actin cytoskeleton. Moreover, we show that the deformed eupyrene sperm bundles fail to migrate from the testes, resulting in male infertility due to the absence of eupyrene sperm in the bursa copulatrix and spermatheca.
CONCLUSIONS
CONCLUSIONS
In conclusion, our studies thus uncover a new role for Piezo in regulating spermatogenesis and male fertility in insects.
Identifiants
pubmed: 38769528
doi: 10.1186/s12915-024-01916-y
pii: 10.1186/s12915-024-01916-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
118Subventions
Organisme : National Science Foundation of China
ID : 31925007
Organisme : National Science Foundation of China
ID : 32000336
Organisme : National Science Foundation of China
ID : 32000339
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20231249
Organisme : Jiangsu Provincial Association for Science and Technology Young Scientific and Technological Talents Trusteeship Project
ID : T-2022-045
Informations de copyright
© 2024. The Author(s).
Références
Murthy SE, Dubin AE, Patapoutian A. Piezos thrive under pressure: mechanically activated ion channels in health and disease. Nat Rev Mol Cell Biol. 2017;18(12):771–83.
pubmed: 28974772
doi: 10.1038/nrm.2017.92
Wu J, Lewis AH, Grandl J. Touch, tension, and transduction - the function and regulation of Piezo ion channels. Trends Biochem Sci. 2017;42(1):57–71.
pubmed: 27743844
doi: 10.1016/j.tibs.2016.09.004
Coste B, Mathur J, Schmidt M, Earley TJ, Ranade S, Petrus MJ, et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science. 2010;330(6000):55–60.
pubmed: 20813920
pmcid: 3062430
doi: 10.1126/science.1193270
Ranade SS, Qiu Z, Woo SH, Hur SS, Murthy SE, Cahalan SM, et al. Piezo1, a mechanically activated ion channel, is required for vascular development in mice. Proc Natl Acad Sci U S A. 2014;111(28):10347–52.
pubmed: 24958852
pmcid: 4104881
doi: 10.1073/pnas.1409233111
Ranade SS, Woo SH, Dubin AE, Moshourab RA, Wetzel C, Petrus M, et al. Piezo2 is the major transducer of mechanical forces for touch sensation in mice. Nature. 2014;516(7529):121–5.
pubmed: 25471886
pmcid: 4380172
doi: 10.1038/nature13980
Mousavi SAR, Dubin AE, Zeng WZ, Coombs AM, Do K, Ghadiri DA, et al. PIEZO ion channel is required for root mechanotransduction in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2021;118(20):e2102188118.
pubmed: 33975957
pmcid: 8158017
doi: 10.1073/pnas.2102188118
Bai X, Bouffard J, Lord A, Brugman K, Sternberg PW, Cram EJ, et al. Caenorhabditis elegans PIEZO channel coordinates multiple reproductive tissues to govern ovulation. Elife. 2020;9:e53603.
pubmed: 32490809
pmcid: 7340503
doi: 10.7554/eLife.53603
Kim SE, Coste B, Chadha A, Cook B, Patapoutian A. The role of Drosophila Piezo in mechanical nociception. Nature. 2012;483(7388):209–12 pmid: 22343891.
pubmed: 22343891
pmcid: 3297676
doi: 10.1038/nature10801
Douguet D, Patel A, Xu A, Vanhoutte PM, Honoré E. Piezo iIon channels in cardiovascular mechanobiology. Trends Pharmacol Sci. 2019;40(12):956–70.
pubmed: 31704174
doi: 10.1016/j.tips.2019.10.002
Kefauver JM, Ward AB, Patapoutian A. Discoveries in structure and physiology of mechanically activated ion channels. Nature. 2020;587(7835):567–76.
pubmed: 33239794
pmcid: 8477435
doi: 10.1038/s41586-020-2933-1
Ikeda R, Cha M, Ling J, Jia Z, Coyle D, Gu JG. Merkel cells transduce and encode tactile stimuli to drive Aβ-afferent impulses. Cell. 2014;157(3):664–75.
pubmed: 24746027
pmcid: 4003503
doi: 10.1016/j.cell.2014.02.026
Marshall KL, Saade D, Ghitani N, Coombs AM, Szczot M, Keller J, et al. PIEZO2 in sensory neurons and urothelial cells coordinates urination. Nature. 2020;588(7837):290–5.
pubmed: 33057202
pmcid: 7725878
doi: 10.1038/s41586-020-2830-7
Wang F, Knutson K, Alcaino C, Linden DR, Gibbons SJ, Kashyap P, et al. Mechanosensitive ion channel Piezo2 is important for enterochromaffin cell response to mechanical forces. J Physiol. 2017;595(1):79–91.
pubmed: 27392819
doi: 10.1113/JP272718
Zarychanski R, Schulz VP, Houston BL, Maksimova Y, Houston DS, Smith B, et al. Mutations in the mechanotransduction protein PIEZO1 are associated with hereditary xerocytosis. Blood. 2012;120(9):1908–15.
pubmed: 22529292
pmcid: 3448561
doi: 10.1182/blood-2012-04-422253
Albuisson J, Murthy SE, Bandell M, Coste B, Louis-Dit-Picard H, Mathur J, et al. Dehydrated hereditary stomatocytosis linked to gain-of-function mutations in mechanically activated PIEZO1 ion channels. Nat Commun. 2013;4:1884.
pubmed: 23695678
doi: 10.1038/ncomms2899
Bae C, Gnanasambandam R, Nicolai C, Sachs F, Gottlieb PA. Xerocytosis is caused by mutations that alter the kinetics of the mechanosensitive channel PIEZO1. Proc Natl Acad Sci U S A. 2013;110(12):E1162–8.
pubmed: 23487776
pmcid: 3606986
doi: 10.1073/pnas.1219777110
Ma S, Cahalan S, LaMonte G, Grubaugh ND, Zeng W, Murthy SE, et al. Common PIEZO1 allele in African populations vauses RBC dehydration and attenuates plasmodium infection. Cell. 2018;173(2):443–455.e12.
pubmed: 29576450
pmcid: 5889333
doi: 10.1016/j.cell.2018.02.047
Ma S, Dubin AE, Zhang Y, Mousavi SAR, Wang Y, Coombs AM, et al. A role of PIEZO1 in iron metabolism in mice and humans. Cell. 2021;184(4):969–982.e13.
pubmed: 33571427
pmcid: 7927959
doi: 10.1016/j.cell.2021.01.024
Lukacs V, Mathur J, Mao R, Bayrak-Toydemir P, Procter M, Cahalan SM, et al. Impaired PIEZO1 function in patients with a novel autosomal recessive congenital lymphatic dysplasia. Nat Commun. 2015;6:8329.
pubmed: 26387913
doi: 10.1038/ncomms9329
Fotiou E, Martin-Almedina S, Simpson MA, Lin S, Gordon K, Brice G, et al. Novel mutations in PIEZO1 cause an autosomal recessive generalized lymphatic dysplasia with non-immune hydrops fetalis. Nat Commun. 2015;6:8085.
pubmed: 26333996
doi: 10.1038/ncomms9085
McMillin MJ, Beck AE, Chong JX, Shively KM, Buckingham KJ, Gildersleeve HI, et al. Mutations in PIEZO2 cause Gordon syndrome, Marden-Walker syndrome, and distal arthrogryposis type 5. Am J Hum Genet. 2014;94(5):734–44.
pubmed: 24726473
pmcid: 4067551
doi: 10.1016/j.ajhg.2014.03.015
Ma S, Dubin AE, Romero LO, Loud M, Salazar A, Chu S, et al. Excessive mechanotransduction in sensory neurons causes joint contractures. Science. 2023;379(6628):201–6.
pubmed: 36634173
pmcid: 10163824
doi: 10.1126/science.add3598
Chesler AT, Szczot M, Bharucha-Goebel D, Čeko M, Donkervoort S, Laubacher C, et al. The role of PIEZO2 in human mechanosensation. N Engl J Med. 2016;375(14):1355–64.
pubmed: 27653382
pmcid: 5911918
doi: 10.1056/NEJMoa1602812
Szczot M, Liljencrantz J, Ghitani N, Barik A, Lam R, Thompson JH, et al. PIEZO2 mediates injury-induced tactile pain in mice and humans. Sci Transl Med. 2018;10(462):eaat9892.
pubmed: 30305456
pmcid: 6875774
doi: 10.1126/scitranslmed.aat9892
Song Y, Li D, Farrelly O, Miles L, Li F, Kim SE, et al. The mechanosensitive ion channel piezo inhibits axon regeneration. Neuron. 2019;102(2):373–389.e6.
pubmed: 30819546
pmcid: 6487666
doi: 10.1016/j.neuron.2019.01.050
Wang P, Jia Y, Liu T, Jan YN, Zhang W. Visceral mechano-sensing neurons control Drosophila feeding by using Piezo as a sensor. Neuron. 2020;108(4):640–650.e4.
pubmed: 32910893
pmcid: 8386590
doi: 10.1016/j.neuron.2020.08.017
Min S, Oh Y, Verma P, Whitehead SC, Yapici N, Van Vactor D, et al. Control of feeding by Piezo-mediated gut mechanosensation in Drosophila. Elife. 2021;10:e63049.
pubmed: 33599608
pmcid: 7920550
doi: 10.7554/eLife.63049
Oh Y, Lai JS, Min S, Huang HW, Liberles SD, Ryoo HD, et al. Periphery signals generated by Piezo-mediated stomach stretch and nNeuromedin-mediated glucose load regulate the Drosophila brain nutrient sensor. Neuron. 2021;109(12):1979–1995.e6.
pubmed: 34015253
pmcid: 8611812
doi: 10.1016/j.neuron.2021.04.028
Yamanouchi HM, Tanaka R, Kamikouchi A. Piezo-mediated mechanosensation contributes to stabilizing copulation posture and reproductive success in Drosophila males. iScience. 2023;26(5):106617.
pubmed: 37250311
pmcid: 10214400
doi: 10.1016/j.isci.2023.106617
Zechini L, Amato C, Scopelliti A, Wood W. Piezo acts as a molecular brake on wound closure to ensure effective inflammation and maintenance of epithelial integrity. Curr Biol. 2022;32(16):3584–3592.e4.
pubmed: 35835122
pmcid: 9616804
doi: 10.1016/j.cub.2022.06.041
Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015;10(6):845–58.
pubmed: 25950237
pmcid: 5298202
doi: 10.1038/nprot.2015.053
Li Z, You L, Zeng B, Ling L, Xu J, Chen X, et al. Ectopic expression of ecdysone oxidase impairs tissue degeneration in Bombyx mori. Proc Biol Sci. 1809;2015(282):20150513.
Phillips DM. Morphogenesis of the lacinate appendages of lepidopteran spermatozoa. J Ultrastruct Res. 1971;34(5):567–85.
pubmed: 5555018
doi: 10.1016/S0022-5320(71)80064-3
Sahara K, Kawamura N. Roles of actin networks in peristaltic squeezing of sperm bundles in Bombyx mori. J Morphol. 2004;259(1):1–6.
pubmed: 14666520
doi: 10.1002/jmor.10168
Georgiadou M, Ivaska J. Tensins: bridging AMP-activated protein kinase with integrin activation. Trends Cell Biol. 2017;27(10):703–11.
pubmed: 28698049
doi: 10.1016/j.tcb.2017.06.004
Sallee JL, Wittchen ES, Burridge K. Regulation of cell adhesion by protein-tyrosine phosphatases: II. Cell-cell adhesion J Biol Chem. 2006;281(24):16189–92.
pubmed: 16497667
Bulgakova NA, Klapholz B, Brown NH. Cell adhesion in Drosophila: versatility of cadherin and integrin complexes during development. Curr Opin Cell Biol. 2012;24(5):702–12.
pubmed: 22938782
doi: 10.1016/j.ceb.2012.07.006
Hutter H, Vogel BE, Plenefisch JD, Norris CR, Proenca RB, Spieth J, et al. Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science. 2000;287(5455):989–94.
pubmed: 10669422
doi: 10.1126/science.287.5455.989
Katsuno S. Studies on eupyrene and apyrene spermatozoa in the silkworm, Bombyx mori L.(Lepidoptera: Bombycidae): I. The intratesticular behaviour of the spermatozoa at various stages from the 5th-instar to the adult. Appl Entomol Zool. 1977;12(2):142–53.
doi: 10.1303/aez.12.142
Chen S, Liu Y, Yang X, Liu Z, Luo X, Xu J, et al. Dysfunction of dimorphic sperm impairs male fertility in the silkworm. Cell Discov. 2020;6:60.
pubmed: 32963806
pmcid: 7477584
doi: 10.1038/s41421-020-00194-6
He L, Si G, Huang J, Samuel ADT, Perrimon N. Mechanical regulation of stem-cell differentiation by the stretch-activated Piezo channel. Nature. 2018;555(7694):103–6.
pubmed: 29414942
pmcid: 6101000
doi: 10.1038/nature25744
Servin-Vences MR, Lam RM, Koolen A, Wang Y, Saade DN, Loud M, et al. PIEZO2 in somatosensory neurons controls gastrointestinal transit. Cell. 2023;186(16):3386–3399.e15.
pubmed: 37541196
pmcid: 10501318
doi: 10.1016/j.cell.2023.07.006
Lam RM, von Buchholtz LJ, Falgairolle M, Osborne J, Frangos E, Servin-Vences MR, et al. PIEZO2 and perineal mechanosensation are essential for sexual function. Science. 2023;381(6660):906–10.
pubmed: 37616369
doi: 10.1126/science.adg0144
Hughes K, Shah A, Bai X, Adams J, Bauer R, Jackson J, et al. Distinct mechanoreceptor pezo-1 isoforms modulate food intake in the nematode Caenorhabditis elegans. G3 (Bethesda). 2022;12(3):jkab429.
pubmed: 35100363
doi: 10.1093/g3journal/jkab429
Lemaitre B, Miguel-Aliaga I. The digestive tract of Drosophila melanogaster. Annu Rev Genet. 2013;47:377–404.
pubmed: 24016187
doi: 10.1146/annurev-genet-111212-133343
Chen K, Chen S, Xu J, Yu Y, Liu Z, Tan A, et al. Maelstrom regulates spermatogenesis of the silkworm. Bombyx mori Insect Biochem Mol Biol. 2019;109:43–51.
pubmed: 30970276
doi: 10.1016/j.ibmb.2019.03.012
Yang X, Chen D, Zheng S, Yi M, Wang S, Liu Y, et al. The Prmt5-Vasa module is essential for spermatogenesis in Bombyx mori. PLoS Genet. 2023;19(1): e1010600.
pubmed: 36634107
pmcid: 9876381
doi: 10.1371/journal.pgen.1010600
Sakai H, Oshima H, Yuri K, Gotoh H, Daimon T, Yaginuma T, et al. Dimorphic sperm formation by Sex-lethal. Proc Natl Acad Sci U S A. 2019;116(21):10412–7.
pubmed: 31036645
pmcid: 6535010
doi: 10.1073/pnas.1820101116
Yang D, Xu J, Chen K, Liu Y, Yang X, Tang L, et al. BmPMFBP1 regulates the development of eupyrene sperm in the silkworm, Bombyx mori. PLoS Genet. 2022;18(3): e1010131.
pubmed: 35312700
pmcid: 8970482
doi: 10.1371/journal.pgen.1010131
Yang X, Chen D, Zheng S, Yi M, Liu Z, Liu Y, et al. BmHen1 is essential for eupyrene sperm development in Bombyx mori but PIWI proteins are not. Insect Biochem Mol Biol. 2022;151: 103874.
pubmed: 36375757
doi: 10.1016/j.ibmb.2022.103874
Kawamura N, Yamashiki N, Saitoh H, Sahara K. Peristaltic squeezing of sperm bundles at the late stage of spermatogenesis in the silkworm. Bombyx mori J Morphol. 2000;246(2):53–8.
pubmed: 11074574
Pontes B, Monzo P, Gauthier NC. Membrane tension: aA challenging but universal physical parameter in cell biology. Semin Cell Dev Biol. 2017;71:30–41.
pubmed: 28851599
doi: 10.1016/j.semcdb.2017.08.030
Xu J, Chen S, Zeng B, James AA, Tan A, Huang Y. Bombyx mori P-element somatic inhibitor (BmPSI) is a key auxiliary factor for silkworm male sex determination. PLoS Genet. 2017;13(1): e1006576.
pubmed: 28103247
pmcid: 5289617
doi: 10.1371/journal.pgen.1006576
Zhang Z, Liu X, Shiotsuki T, Wang Z, Xu X, Huang Y, et al. Depletion of juvenile hormone esterase extends larval growth in Bombyx mori. Insect Biochem Mol Biol. 2017;81:72–9.
pubmed: 28057597
doi: 10.1016/j.ibmb.2017.01.001