A dynamic basal complex modulates mammalian sperm movement

A dynamic basal complex modulates mammalian sperm movement | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article A dynamic basal complex modulates mammalian sperm movement Sushil Khanal, Miguel Leung, Abigail Royfman, Emily Fishman, Barbara Saltzman, and 3 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-136145/v2 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 21 Jun, 2021 Read the published version in Nature Communications → Version 2 posted You are reading this latest preprint version Show more versions Abstract Reproductive success depends on efficient sperm movement driven by dynein-mediated microtubule sliding in the axoneme 1-3. Models predict sliding at the base of the tail – the centriole – but such sliding has never been observed 4,5. Centrioles are evolutionarily-ancient organelles with a conserved architecture 6-8, and their rigidity is thought to restrict microtubule sliding 1. Here, we show that, in mammalian sperm, the atypical distal centriole (DC) and its surrounding atypical pericentriolar matrix 9,10 form a dynamic basal complex (DBC) that facilitates a cascade of internal sliding deformations, coupling tail beating with asymmetric head kinking. During asymmetric tail beating, the DC’s right side and its surroundings slide ~300 nm rostrally relative to the left side. This deformation is transmitted through the DBC to the head-tail junction; as a result, the head tilts to the left, generating a kinking motion. These findings suggest that the DBC evolved to act as a mechanotransducer, coupling sperm head and tail into a single self-coordinated system. The DBC may act as a morphological computer 11, regulating tail beating from external feedback imparted to the head during sperm navigation. We anticipate our findings will enable studies of coordinated motion in sperm and cilia in many contexts. General Cell Biology & Physiology mammalian sperm movement dynamic basal complex (DBC) Figures Figure 1 Figure 2 Figure 3 Full Text Additional Declarations There is NO Competing Interest. Supplementary Files 20210112TARKhanaletalSupplementrytext.pdf SUPPLEMENTARY INFO Cite Share Download PDF Status: Published Journal Publication published 21 Jun, 2021 Read the published version in Nature Communications → Version 2 posted You are reading this latest preprint version Show more versions Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Communications","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"ejp","reportingPortfolio":"Nature Communications","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":9068173,"identity":"16559361-fd72-4378-96bd-15560c299a5f","order_by":0,"name":"Sushil Khanal","email":"","orcid":"","institution":"University of Toledo","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Sushil","middleName":"","lastName":"Khanal","suffix":""},{"id":9068174,"identity":"574a7465-95ff-47a1-9051-8f815ed8d566","order_by":1,"name":"Miguel Leung","email":"","orcid":"","institution":"The University of Oxford","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Miguel","middleName":"","lastName":"Leung","suffix":""},{"id":9068175,"identity":"5c0426e0-76dc-40bf-a545-5ef046ef5d33","order_by":2,"name":"Abigail Royfman","email":"","orcid":"","institution":"University of Toledo","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Abigail","middleName":"","lastName":"Royfman","suffix":""},{"id":9068176,"identity":"5cd8829f-6362-4008-b052-41d061dad689","order_by":3,"name":"Emily Fishman","email":"","orcid":"","institution":"University of Toledo","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Emily","middleName":"","lastName":"Fishman","suffix":""},{"id":9068177,"identity":"1af38177-e445-4b5d-9105-b559e65a8300","order_by":4,"name":"Barbara Saltzman","email":"","orcid":"","institution":"University of Toledo","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Barbara","middleName":"","lastName":"Saltzman","suffix":""},{"id":9068178,"identity":"a7bf7941-1d0b-48d8-b389-3d3e04c62c64","order_by":5,"name":"Hermes Bloomfield-Gadêlha","email":"","orcid":"","institution":"University of Bristol","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Hermes","middleName":"","lastName":"Bloomfield-Gadêlha","suffix":""},{"id":9068179,"identity":"d47e2132-4a67-445e-b0e3-441b9392928a","order_by":6,"name":"Tzvya Zeev Ben Mordehai","email":"","orcid":"https://orcid.org/0000-0002-2571-550X","institution":"Cryo-Electron Microscopy, Bijvoet Center for Biomolecular Research, Utrecht University, 3584 CH Utrecht, The Netherlands","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Tzvya","middleName":"Zeev Ben","lastName":"Mordehai","suffix":""},{"id":9068180,"identity":"b38652f3-0a7d-4303-9782-1c619ddf3c91","order_by":7,"name":"Tomer Avidor-Reiss","email":"data:image/png;base64,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","orcid":"https://orcid.org/0000-0003-0918-526X","institution":"University of Toledo","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Tomer","middleName":"","lastName":"Avidor-Reiss","suffix":""}],"badges":[],"createdAt":"2020-12-25 17:35:28","currentVersionCode":2,"declarations":"","doi":"10.21203/rs.3.rs-136145/v2","doiUrl":"https://doi.org/10.21203/rs.3.rs-136145/v2","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1038/s41467-021-24011-0","type":"published","date":"2021-06-21T04:00:00+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":5281220,"identity":"ea2fab49-2078-4512-8f24-a1f45c06e889","added_by":"auto","created_at":"2021-01-19 00:21:53","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":325650,"visible":true,"origin":"","legend":"The DC is Asymmetric.\na) Schematics illustrating sperm cell asymmetries (top) with a magnification of the neck (bottom). Note that sperm beating occurs in one plane, while head and neck asymmetry provide a basis for orientation in all figures, such that the top is rostral and the left side is on the left.\nb-e) Rod proteins and microtubules are asymmetric in the DC of bovine spermatozoa, as observed using 3D-STORM. Side view (left two panels); top view (right two panels). All sizes are in mean ± sd nm. The colors represent depths of 1178 nm in the Z-plane, with red on the bottom (bott.) in all figures. Statistical is shown in Extended Data Fig. 2e\nf-g) A computational slice (left) and corresponding 3D segmentation (right) of a Volta phase plate cryo-tomogram of a bovine sperm neck (f). A digital zoom of a cryo-tomogram illustrating bar asymmetry, complexity, and intimate association with the central pair (g). Scale bars, 250 nm.Throughout the paper, labels and their colors are the same: N, nucleus; IF, Implantation fossa; Bp, basal plate; Ca, capitulum; SC, striated column, grey; PC, Proximal centriole, yellow; DC, distal centriole, green; Ax, axoneme, red; M, mitochondria, brown; L, left side; R, right side; r, rod, C, central microtubules; B, bars, light yellow; CP, central pair, pink; Mts., microtubules, green in DC and red in axoneme.","description":"","filename":"figure1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-149166/v1/729b8b7057fe1276b7e3214b.jpg"},{"id":5281223,"identity":"d83ee83f-3dfa-4025-9f16-736e80ab44f1","added_by":"auto","created_at":"2021-01-19 00:24:53","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":236414,"visible":true,"origin":"","legend":"The DC's Rods and Lateral Side Microtubules Slide in Correlation with Tail Beating.\na-b) The four types of sperm tail bending oriented according to COSA. Staining with FAM161A (a), and tubulin (b) in chemically fixed sperm. Orange dotted line marks the neck midline.\nc-d) Zoom-in on the neck from panels a and b shows the location difference in the DC rod (c) and microtubule (d) edges. Arrowhead marks the central microtubules (d). Lines mark the edges on left (L, green) and right (R, red).\ne-f) Rotated neck to align along the neck midline. The white arrow shows the head is bending to the left during tail beating to the left.\ng-h) Zoom in on neck from the panels e and f. The orange dotted line mark the neck/DC and PC midline. +d and –d is the distance of right-side rod and microtubule edge relative to left side rod and microtubules edge.\ni-) Rostral (purple) and caudal (magenta) DC rod distance (dist.) and rostral DC microtubule distance (green) during tail beating. The schematic at left side of each graph represents the measurement scheme shown in Y-Axis of the graph. ****p\u003c0.0001, ***p\u003c0.001, **p\u003c0.01.\nj) Scatter plot of rod and microtubule rostral distance against flagellar beating amplitude (y̅) (X-axis). The R in each scatter plot represents correlation and R2 represents regression value. The solid orange line in scatter plots represents regression line. Correlation is statistically significant at ****P\u003c0.0001. Scale bars, 250 nm","description":"","filename":"figure2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-149166/v1/ed4838153579a53e7b7a0aeb.jpg"},{"id":5281225,"identity":"37575f3c-70b2-4f1b-b912-3bad0835f828","added_by":"auto","created_at":"2021-01-19 00:27:53","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":269464,"visible":true,"origin":"","legend":"The sperm tail beating, neck deformation, and head kinking are coordinated.\na) Computational slices through cryo-tomograms of sperm with varying extents of tail bending (upper panels) and corresponding three-dimensional segmentations (lower panels). The arrow marks the area where the SCs bend when the head kinks to the left.\nb) Tail beating coordinates head kinking. Correlation analysis between head-neck angle with flagella curvature (κ̅, upper panel) and DC microtubules (Mts.) rostral distance (dist., lower panel). Correlation analysis ****p\u003c0.0001\nc) Model of the coordinated change in sperm internal structure during asymmetric sperm head kinking.","description":"","filename":"figure3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-149166/v1/72798ec0d2ed6a3d933cc9e8.jpg"},{"id":15781841,"identity":"b73b1dfb-9e77-4cd6-8028-56a8fd6ffad0","added_by":"auto","created_at":"2021-11-22 15:47:03","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1408183,"visible":true,"origin":"","legend":"","description":"","filename":"20210113SKKhanaletal.pdf","url":"https://assets-eu.researchsquare.com/files/rs-136145/v2_covered.pdf"},{"id":13576578,"identity":"4ad863bf-0159-4fe0-b373-3d6795981675","added_by":"auto","created_at":"2021-09-17 04:08:16","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1403344,"visible":true,"origin":"","legend":"","description":"","filename":"20210113SKKhanaletal.pdf","url":"https://assets-eu.researchsquare.com/files/rs-136145/v2_covered.pdf"},{"id":5281218,"identity":"79826878-c412-421d-b7bb-2ac1105a8181","added_by":"auto","created_at":"2021-01-19 00:31:02","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1249428,"visible":true,"origin":"","legend":"","description":"","filename":"20210113SKKhanaletal.pdf","url":"https://assets-eu.researchsquare.com/files/rs-149166/v1_stamped.pdf"},{"id":5281219,"identity":"5d643549-b4da-4b9c-93c3-827928ca13e0","added_by":"auto","created_at":"2021-01-19 00:27:53","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":3294817,"visible":true,"origin":"","legend":"SUPPLEMENTARY INFO","description":"","filename":"20210112TARKhanaletalSupplementrytext.pdf","url":"https://assets-eu.researchsquare.com/files/rs-149166/v1/0a4c5a7c64032180b0057c34.pdf"}],"financialInterests":"There is \u003cb\u003eNO\u003c/b\u003e Competing Interest.","formattedTitle":"A dynamic basal complex modulates mammalian sperm movement","fulltext":[{"header":"Full Text","content":"\u003cp\u003eThis preprint is available for \u003ca href='/article/rs-136145/latest.pdf' target='_blank'\u003edownload as a PDF\u003c/a\u003e.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":true,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"nature-portfolio","isNatureJournal":true,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"","title":"Nature Portfolio","twitterHandle":"","acdcEnabled":false,"dfaEnabled":false,"editorialSystem":"ejp","reportingPortfolio":"","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"mammalian sperm movement, dynamic basal complex (DBC)","lastPublishedDoi":"10.21203/rs.3.rs-136145/v2","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-136145/v2","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"Reproductive success depends on efficient sperm movement driven by dynein-mediated microtubule sliding in the axoneme 1-3. Models predict sliding at the base of the tail – the centriole – but such sliding has never been observed 4,5. Centrioles are evolutionarily-ancient organelles with a conserved architecture 6-8, and their rigidity is thought to restrict microtubule sliding 1. Here, we show that, in mammalian sperm, the atypical distal centriole (DC) and its surrounding atypical pericentriolar matrix 9,10 form a dynamic basal complex (DBC) that facilitates a cascade of internal sliding deformations, coupling tail beating with asymmetric head kinking. During asymmetric tail beating, the DC’s right side and its surroundings slide ~300 nm rostrally relative to the left side. This deformation is transmitted through the DBC to the head-tail junction; as a result, the head tilts to the left, generating a kinking motion. These findings suggest that the DBC evolved to act as a mechanotransducer, coupling sperm head and tail into a single self-coordinated system. The DBC may act as a morphological computer 11, regulating tail beating from external feedback imparted to the head during sperm navigation. We anticipate our findings will enable studies of coordinated motion in sperm and cilia in many contexts.","manuscriptTitle":"A dynamic basal complex modulates mammalian sperm movement","msid":"","msnumber":"","nonDraftVersions":[{"code":2,"date":"2021-01-19 00:21:51","doi":"10.21203/rs.3.rs-136145/v2","editorialEvents":[],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"nature-communications","isNatureJournal":true,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"NCOMMS","sideBox":"Learn more about [Nature Communications](http://www.nature.com/ncomms/)","snPcode":"","submissionUrl":"https://mts-ncomms.nature.com/","title":"Nature Communications","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"ejp","reportingPortfolio":"Nature Communications","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"9bb2aa77-27af-4af1-8699-b804dd8e17d0","owner":[],"postedDate":"January 19th, 2021","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[{"id":2090317,"name":"General Cell Biology \u0026 Physiology"}],"tags":[],"updatedAt":"2021-11-22T15:40:12+00:00","versionOfRecord":{"articleIdentity":"rs-136145","link":"https://doi.org/10.1038/s41467-021-24011-0","journal":{"identity":"nature-communications","isVorOnly":false,"title":"Nature Communications"},"publishedOn":"2021-06-21 04:00:00","publishedOnDateReadable":"June 21st, 2021"},"versionCreatedAt":"2021-01-19 00:21:51","video":"","vorDoi":"10.1038/s41467-021-24011-0","vorDoiUrl":"https://doi.org/10.1038/s41467-021-24011-0","workflowStages":[]},"version":"v2","identity":"rs-136145","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-136145","identity":"rs-136145","version":["v2"]},"buildId":"7rjqhiLT3MXkJMwkYKINL","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}