{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,21]],"date-time":"2025-02-21T03:11:32Z","timestamp":1740107492477,"version":"3.37.3"},"reference-count":32,"publisher":"Springer Science and Business Media LLC","issue":"11","license":[{"start":{"date-parts":[[2024,11,1]],"date-time":"2024-11-01T00:00:00Z","timestamp":1730419200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2024,11,1]],"date-time":"2024-11-01T00:00:00Z","timestamp":1730419200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32273029 and 31972700"],"award-info":[{"award-number":["32273029 and 31972700"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Parasitol Res"],"published-print":{"date-parts":[[2024,11]]},"DOI":"10.1007\/s00436-024-08405-9","type":"journal-article","created":{"date-parts":[[2024,11,18]],"date-time":"2024-11-18T08:03:09Z","timestamp":1731916989000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Dense granule protein 41 of Neospora caninum modulates tachyzoite egress by regulating microneme secretion"],"prefix":"10.1007","volume":"123","author":[{"given":"Jing","family":"Yang","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yanqun","family":"Pei","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xianmei","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhu","family":"Ying","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zifu","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qun","family":"Liu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7309-0340","authenticated-orcid":false,"given":"Jing","family":"Liu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2024,11,18]]},"reference":[{"issue":"4","key":"8405_CR1","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1007\/s11259-007-9033-7","volume":"32","author":"JH Behrendt","year":"2008","unstructured":"Behrendt JH, Taubert A, Zahner H, Hermosilla C (2008) Studies on synchronous egress of coccidian parasites (Neospora caninum, Toxoplasma gondii, Eimeria bovis) from bovine endothelial host cells mediated by calcium ionophore A23187. Vet Res Commun 32(4):325\u201332. https:\/\/doi.org\/10.1007\/s11259-007-9033-7","journal-title":"Vet Res Commun"},{"issue":"10","key":"8405_CR2","doi-asserted-by":"publisher","first-page":"2071","DOI":"10.1084\/jem.20130103","volume":"210","author":"L Braun","year":"2013","unstructured":"Braun L, Brenier-Pinchart MP, Yogavel M, Curt-Varesano A, Curt-Bertini RL, Hussain T, Kieffer-Jaquinod S, Coute Y, Pelloux H, Tardieux I, Sharma A, Belrhali H, Bougdour A, Hakimi MA (2013) A Toxoplasma dense granule protein, GRA24, modulates the early immune response to infection by promoting a direct and sustained host p38 MAPK activation. J Exp Med 210(10):2071\u20132086. https:\/\/doi.org\/10.1084\/jem.20130103","journal-title":"J Exp Med"},{"issue":"4","key":"8405_CR3","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1016\/j.chom.2013.03.002","volume":"13","author":"A Bougdour","year":"2013","unstructured":"Bougdour A, Durandau E, Brenier-Pinchart MP, Ortet P, Barakat M, Kieffer S, Curt-Varesano A, Curt-Bertini RL, Bastien O, Coute Y, Pelloux H, Hakimi MA (2013) Host cell subversion by Toxoplasma GRA16, an exported dense granule protein that targets the host cell nucleus and alters gene expression. Cell Host Microbe 13(4):489\u2013500. https:\/\/doi.org\/10.1016\/j.chom.2013.03.002","journal-title":"Cell Host Microbe"},{"issue":"3","key":"8405_CR4","doi-asserted-by":"publisher","first-page":"e00375","DOI":"10.1128\/mBio.00375-17","volume":"8","author":"KM Brown","year":"2017","unstructured":"Brown KM, Long S, Sibley LD (2017) Plasma membrane association by N-acylation governs PKG function in Toxoplasma gondii. mBio 8(3):e00375-17. https:\/\/doi.org\/10.1128\/mBio.00375-17","journal-title":"mBio"},{"issue":"6","key":"8405_CR5","doi-asserted-by":"publisher","first-page":"804","DOI":"10.1016\/j.chom.2018.10.015","volume":"24","author":"KM Brown","year":"2018","unstructured":"Brown KM, Sibley LD (2018) Essential cGMP signaling in Toxoplasma is initiated by a hybrid P-type ATPase-guanylate cyclase. Cell Host Microbe 24(6):804-816.e6. https:\/\/doi.org\/10.1016\/j.chom.2018.10.015","journal-title":"Cell Host Microbe"},{"issue":"5","key":"8405_CR6","doi-asserted-by":"publisher","first-page":"e1007670","DOI":"10.1371\/journal.ppat.1007670","volume":"15","author":"HE Bullen","year":"2019","unstructured":"Bullen HE, Bisio H, Soldati-Favre D (2019) The triumvirate of signaling molecules controlling Toxoplasma microneme exocytosis: cyclic GMP, calcium, and phosphatidic acid. PLoS Pathog 15(5):e1007670. https:\/\/doi.org\/10.1371\/journal.ppat.1007670","journal-title":"PLoS Pathog"},{"issue":"3","key":"8405_CR7","doi-asserted-by":"publisher","first-page":"420","DOI":"10.1038\/s41564-018-0339-8","volume":"4","author":"H Bisio","year":"2019","unstructured":"Bisio H, Lunghi M, Brochet M, Soldati-Favre D (2019) Phosphatidic acid governs natural egress in Toxoplasma gondii via a guanylate cyclase receptor platform. Nat Microbiol 4(3):420\u2013428. https:\/\/doi.org\/10.1038\/s41564-018-0339-8","journal-title":"Nat Microbiol"},{"key":"8405_CR8","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1146\/annurev-micro-020518-120235","volume":"73","author":"H Bisio","year":"2019","unstructured":"Bisio H, Soldati-Favre D (2019) Signaling cascades governing entry into and exit from host cells by Toxoplasma gondii. Annu Rev Microbiol 73:579\u2013599. https:\/\/doi.org\/10.1146\/annurev-micro-020518-120235","journal-title":"Annu Rev Microbiol"},{"issue":"7","key":"8405_CR9","doi-asserted-by":"publisher","first-page":"1007","DOI":"10.1016\/s0020-7519(98)00076-9","volume":"28","author":"JF Dubremetz","year":"1998","unstructured":"Dubremetz JF, Garcia-R\u00e9guet N, Conseil V, Fourmaux MN (1998) Apical organelles and host-cell invasion by Apicomplexa. Int J Parasitol 28(7):1007\u20131013. https:\/\/doi.org\/10.1016\/s0020-7519(98)00076-9","journal-title":"Int J Parasitol"},{"issue":"4","key":"8405_CR10","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1016\/j.chom.2015.09.007","volume":"18","author":"S Das","year":"2015","unstructured":"Das S, Hertrich N, Perrin AJ, Withers-Martinez C, Collins CR, Jones ML, Watermeyer JM, Fobes ET, Martin SR, Saibil HR, Wright GJ, Treeck M, Epp C, Blackman MJ (2015) Processing of Plasmodium falciparum merozoite surface protein MSP1 activates a spectrin-binding function enabling parasite egress from RBCs. Cell Host Microbe 18(4):433\u2013444. https:\/\/doi.org\/10.1016\/j.chom.2015.09.007","journal-title":"Cell Host Microbe"},{"key":"8405_CR11","doi-asserted-by":"publisher","first-page":"e27480","DOI":"10.7554\/eLife.27480","volume":"6","author":"SK Dogga","year":"2017","unstructured":"Dogga SK, Mukherjee B, Jacot D, Kockmann T, Molino L, Hammoudi PM, Hartkoorn RC, Hehl AB, Soldati-Favre D (2017) A druggable secretory protein maturase of Toxoplasma essential for invasion and egress. Elife 6:e27480. https:\/\/doi.org\/10.7554\/eLife.27480","journal-title":"Elife"},{"issue":"6065","key":"8405_CR12","doi-asserted-by":"publisher","first-page":"218","DOI":"10.1126\/science.1210829","volume":"335","author":"A Farrell","year":"2012","unstructured":"Farrell A, Thirugnanam S, Lorestani A, Dvorin JD, Eidell KP, Ferguson DJ, Anderson-White BR, Duraisingh MT, Marth GT, Gubbels MJ (2012) A DOC2 protein identified by mutational profiling is essential for apicomplexan parasite exocytosis. Science 335(6065):218\u2013221. https:\/\/doi.org\/10.1126\/science.1210829","journal-title":"Science"},{"issue":"5","key":"8405_CR13","doi-asserted-by":"publisher","first-page":"642","DOI":"10.1016\/j.chom.2015.04.003","volume":"17","author":"DA Gold","year":"2015","unstructured":"Gold DA, Kaplan AD, Lis A, Bett GC, Rosowski EE, Cirelli KM, Bougdour A, Sidik SM, Beck JR, Lourido S, Egea PF, Bradley PJ, Hakimi MA, Rasmusson RL, Saeij JP (2015) The Toxoplasma dense granule proteins GRA17 and GRA23 mediate the movement of small molecules between the host and the parasitophorous vacuole. Cell Host Microbe 17(5):642\u2013652. https:\/\/doi.org\/10.1016\/j.chom.2015.04.003","journal-title":"Cell Host Microbe"},{"issue":"1","key":"8405_CR14","doi-asserted-by":"publisher","first-page":"e00851","DOI":"10.1128\/mSphere.00851-19","volume":"5","author":"RB Guevara","year":"2020","unstructured":"Guevara RB, Fox BA, Bzik DJ (2020) Toxoplasma gondii parasitophorous vacuole membrane-associated dense granule proteins regulate maturation of the cyst wall. mSphere 5(1):e00851-19. https:\/\/doi.org\/10.1128\/mSphere.00851-19","journal-title":"mSphere"},{"issue":"1","key":"8405_CR15","doi-asserted-by":"publisher","first-page":"23","DOI":"10.2741\/e593","volume":"5","author":"A Hemphill","year":"2013","unstructured":"Hemphill A, Debache K, Monney T, Schorer M, Guionaud C, Alaeddine F, Mueller N, Mueller J (2013) Proteins mediating the Neospora caninum-host cell interaction as targets for vaccination. Front Biosci (Elite Ed) 5(1):23\u201336. https:\/\/doi.org\/10.2741\/e593","journal-title":"Front Biosci (Elite Ed)"},{"issue":"12","key":"8405_CR16","doi-asserted-by":"publisher","first-page":"1792","DOI":"10.1111\/j.1462-5822.2010.01509.x","volume":"12","author":"V Lagal","year":"2010","unstructured":"Lagal V, Binder EM, Huynh MH, Kafsack BF, Harris PK, Diez R, Chen D, Cole RN, Carruthers VB, Kim K (2010) Toxoplasma gondii protease TgSUB1 is required for cell surface processing of micronemal adhesive complexes and efficient adhesion of tachyzoites. Cell Microbiol 12(12):1792\u20131808. https:\/\/doi.org\/10.1111\/j.1462-5822.2010.01509.x","journal-title":"Cell Microbiol"},{"issue":"24","key":"8405_CR17","doi-asserted-by":"publisher","first-page":"4524","DOI":"10.1038\/emboj.2012.299","volume":"31","author":"S Lourido","year":"2012","unstructured":"Lourido S, Tang K, Sibley LD (2012) Distinct signalling pathways control Toxoplasma egress and host-cell invasion. EMBO J 31(24):4524\u20134534. https:\/\/doi.org\/10.1038\/emboj.2012.299","journal-title":"EMBO J"},{"doi-asserted-by":"publisher","unstructured":"LaFavers KA, M\u00e1rquez-Nogueras KM, Coppens I, Moreno SNJ, Arrizabalaga G (2017) A novel dense granule protein, GRA41, regulates timing of egress and calcium sensitivity in Toxoplasma gondii. Cell Microbiol 19(9). https:\/\/doi.org\/10.1111\/cmi.12749","key":"8405_CR18","DOI":"10.1111\/cmi.12749"},{"issue":"1","key":"8405_CR19","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/j.cvfa.2019.11.004","volume":"36","author":"DS Lindsay","year":"2020","unstructured":"Lindsay DS, Dubey JP (2020) Neosporosis, toxoplasmosis, and sarcocystosis in ruminants: an update. Vet Clin North Am Food Anim Pract 36(1):205\u2013222. https:\/\/doi.org\/10.1016\/j.cvfa.2019.11.004","journal-title":"Vet Clin North Am Food Anim Pract"},{"issue":"6","key":"8405_CR20","doi-asserted-by":"publisher","first-page":"978","DOI":"10.3201\/eid1406.071128","volume":"14","author":"CM McCann","year":"2008","unstructured":"McCann CM, Vyse AJ, Salmon RL, Thomas D, Williams DJ, McGarry JW, Pebody R, Trees AJ (2008) Lack of serologic evidence of Neospora caninum in humans, England. Emerg Infect Dis 14(6):978\u2013980. https:\/\/doi.org\/10.3201\/eid1406.071128","journal-title":"Emerg Infect Dis"},{"issue":"12","key":"8405_CR21","doi-asserted-by":"publisher","first-page":"e1003066","DOI":"10.1371\/journal.ppat.1003066","volume":"8","author":"JM McCoy","year":"2012","unstructured":"McCoy JM, Whitehead L, van Dooren GG, Tonkin CJ (2012) TgCDPK3 regulates calcium-dependent egress of Toxoplasma gondii from host cells. PLoS Pathog 8(12):e1003066. https:\/\/doi.org\/10.1371\/journal.ppat.1003066","journal-title":"PLoS Pathog"},{"issue":"2","key":"8405_CR22","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1016\/j.pt.2014.12.002","volume":"31","author":"C Mercier","year":"2015","unstructured":"Mercier C, Cesbron-Delauw MF (2015) Toxoplasma secretory granules: one population or more? Trends Parasitol 31(2):60\u201371. https:\/\/doi.org\/10.1016\/j.pt.2014.12.002","journal-title":"Trends Parasitol"},{"issue":"5","key":"8405_CR23","doi-asserted-by":"publisher","first-page":"e00784","DOI":"10.1128\/IAI.00784-18","volume":"87","author":"S Nava","year":"2019","unstructured":"Nava S, White AC Jr, Castellanos-Gonz\u00e1lez A (2019) Cryptosporidium parvum subtilisin-like serine protease (SUB1) is crucial for parasite egress from host cells. Infect Immun 87(5):e00784-e818. https:\/\/doi.org\/10.1128\/IAI.00784-18","journal-title":"Infect Immun"},{"issue":"1\u20132","key":"8405_CR24","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1016\/j.molbiopara.2013.04.005","volume":"189","author":"T Okada","year":"2013","unstructured":"Okada T, Marmansari D, Li ZM, Adilbish A, Canko S, Ueno A, Shono H, Furuoka H, Igarashi M (2013) A novel dense granule protein, GRA22, is involved in regulating parasite egress in Toxoplasma gondii. Mol Biochem Parasitol 189(1\u20132):5\u201313. https:\/\/doi.org\/10.1016\/j.molbiopara.2013.04.005","journal-title":"Mol Biochem Parasitol"},{"issue":"1","key":"8405_CR25","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1186\/s13071-016-1620-4","volume":"9","author":"I Pastor-Fern\u00e1ndez","year":"2016","unstructured":"Pastor-Fern\u00e1ndez I, Regidor-Cerrillo J, \u00c1lvarez-Garc\u00eda G, Marug\u00e1n-Hern\u00e1ndez V, Garc\u00eda-Lunar P, Hemphill A, Ortega-Mora LM (2016) The tandemly repeated NTPase (NTPDase) from Neospora caninum is a canonical dense granule protein whose RNA expression, protein secretion and phosphorylation coincides with the tachyzoite egress. Parasit Vectors 9(1):352. https:\/\/doi.org\/10.1186\/s13071-016-1620-4","journal-title":"Parasit Vectors"},{"key":"8405_CR26","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/j.ijpara.2012.10.022","volume":"43","author":"MP Reichel","year":"2013","unstructured":"Reichel MP, Alejandra Ayanegui-Alc\u00e9rreca M, Gondim LF, Ellis JT (2013) What is the global economic impact of Neospora caninum in cattle - the billion dollar question. Int J Parasitol 43:133\u2013142. https:\/\/doi.org\/10.1016\/j.ijpara.2012.10.022","journal-title":"Int J Parasitol"},{"issue":"1","key":"8405_CR27","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1084\/jem.20100717","volume":"208","author":"EE Rosowski","year":"2011","unstructured":"Rosowski EE, Lu D, Julien L, Rodda L, Gaiser RA, Jensen KD, Saeij JP (2011) Strain-specific activation of the NF-kappaB pathway by GRA15, a novel Toxoplasma gondii dense granule protein. J Exp Med 208(1):195\u2013212. https:\/\/doi.org\/10.1084\/jem.20100717","journal-title":"J Exp Med"},{"issue":"1","key":"8405_CR28","doi-asserted-by":"publisher","first-page":"e00073","DOI":"10.1128\/mSphereDirect.00073-18","volume":"3","author":"AJ Schultz","year":"2018","unstructured":"Schultz AJ, Carruthers VB (2018) Toxoplasma gondii LCAT primarily contributes to tachyzoite egress. mSphere 3(1):e00073-18. https:\/\/doi.org\/10.1128\/mSphereDirect.00073-18","journal-title":"mSphere"},{"issue":"9","key":"8405_CR29","doi-asserted-by":"publisher","first-page":"e2005642","DOI":"10.1371\/journal.pbio.2005642","volume":"16","author":"AD Uboldi","year":"2018","unstructured":"Uboldi AD, Wilde ML, McRae EA, Stewart RJ, Dagley LF, Yang L, Katris NJ, Hapuarachchi SV, Coffey MJ, Lehane AM, Botte CY, Waller RF, Webb AI, McConville MJ, Tonkin CJ (2018) Protein kinase A negatively regulates Ca2+ signalling in Toxoplasma gondii. PLoS Biol 16(9):e2005642. https:\/\/doi.org\/10.1371\/journal.pbio.2005642","journal-title":"PLoS Biol"},{"issue":"2","key":"8405_CR30","doi-asserted-by":"publisher","first-page":"201","DOI":"10.3390\/pathogens10020201","volume":"10","author":"X Wang","year":"2021","unstructured":"Wang X, Tang D, Wang F, Jin G, Wang L, Liu Q, Liu J (2021) Microneme protein 6 is involved in invasion and egress by Neospora caninum. Pathogens 10(2):201. https:\/\/doi.org\/10.3390\/pathogens10020201","journal-title":"Pathogens"},{"issue":"1","key":"8405_CR31","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1128\/IAI.00734-15","volume":"84","author":"CS Yang","year":"2015","unstructured":"Yang CS, Yuk JM, Lee YH, Jo EK (2015) Toxoplasma gondii GRA7-induced TRAF6 activation contributes to host protective immunity. Infect Immun 84(1):339\u2013350. https:\/\/doi.org\/10.1128\/IAI.00734-15","journal-title":"Infect Immun"},{"key":"8405_CR32","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/j.vetpar.2018.03.018","volume":"64","author":"C Yang","year":"2018","unstructured":"Yang C, Liu J, Ma L, Zhang X, Zhang X, Zhou B, Zhu X, Liu Q (2018) NcGRA17 is an important regulator of parasitophorous vacuole morphology and pathogenicity of Neospora caninum. Vet Parasitol 64:26\u201334. https:\/\/doi.org\/10.1016\/j.vetpar.2018.03.018","journal-title":"Vet Parasitol"}],"container-title":["Parasitology Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00436-024-08405-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00436-024-08405-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00436-024-08405-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,5]],"date-time":"2024-12-05T11:09:53Z","timestamp":1733396993000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00436-024-08405-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,11]]},"references-count":32,"journal-issue":{"issue":"11","published-print":{"date-parts":[[2024,11]]}},"alternative-id":["8405"],"URL":"https:\/\/doi.org\/10.1007\/s00436-024-08405-9","relation":{},"ISSN":["0932-0113","1432-1955"],"issn-type":[{"type":"print","value":"0932-0113"},{"type":"electronic","value":"1432-1955"}],"subject":[],"published":{"date-parts":[[2024,11]]},"assertion":[{"value":"12 August 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 November 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 November 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The mice used in this study were handled in compliance with the recommendations outlined in the \u201cGuidelines for the Care and Use of Laboratory Animals\u201d of the Ministry of Science and Technology of China. Additionally, our research protocol received approval from the Laboratory Animal Welfare and Animal Experimental Ethical Committee of China Agricultural University (Certificate No.: CAU-AW31901202-2\u20131).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval"}},{"value":"Done and confirmed.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to participate"}},{"value":"Not applicable.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare no competing interests.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"386"}}