{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T22:20:36Z","timestamp":1793312436356,"version":"4.5.0"},"reference-count":33,"publisher":"Springer Science and Business Media LLC","issue":"9","license":[{"start":{"date-parts":[[2020,3,4]],"date-time":"2020-03-04T00:00:00Z","timestamp":1583280000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2020,3,4]],"date-time":"2020-03-04T00:00:00Z","timestamp":1583280000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"funder":[{"name":"the National Key R&D Program","award":["2017YFD0501103"],"award-info":[{"award-number":["2017YFD0501103"]}]},{"name":"the Special Fund for Scientific Research and Development of Henan Academy of Agricultural Sciences","award":["[2017]76-21"],"award-info":[{"award-number":["[2017]76-21"]}],"id":[{"id":"https:\/\/ror.org\/00vdyrj80","id-type":"ROR","asserted-by":"crossref"}]},{"name":"\u201c1125 talent gathering plan\u201d of Zhengzhou"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Appl Microbiol Biotechnol"],"published-print":{"date-parts":[[2020,5]]},"DOI":"10.1007\/s00253-020-10483-5","type":"journal-article","created":{"date-parts":[[2020,3,4]],"date-time":"2020-03-04T01:14:54Z","timestamp":1583284494000},"page":"3847-3857","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Large-scale manufacture of VP2 VLP vaccine against porcine parvovirus in Escherichia coli with high-density fermentation"],"prefix":"10.1007","volume":"104","author":[{"given":"Jucai","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunchao","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yumei","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aiping","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiang","family":"Wei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dongmin","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9630-8397","authenticated-orcid":false,"given":"Gaiping","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,3,4]]},"reference":[{"issue":"26","key":"10483_CR1","doi-asserted-by":"publisher","first-page":"5481","DOI":"10.1016\/j.vaccnie.2006.03.089","volume":"24","author":"AF Antonis","year":"2006","unstructured":"Antonis AF, Bruschke CJ, Rueda P, Maranga L, Casal JI, Vela C, Hilgers LA, Belt PB, Weerdmeester K, Carrondo MJ, Langeveld JP (2006) A novel recombinant virus-like particle vaccine for prevention of porcine parvovirus-induced reproductive failure. Vaccine 24(26):5481\u20135490. https:\/\/doi.org\/10.1016\/j.vaccnie.2006.03.089","journal-title":"Vaccine"},{"issue":"1\u20132","key":"10483_CR2","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1016\/j.jviromet.2008.10.029","volume":"156","author":"HY Chen","year":"2009","unstructured":"Chen HY, Li XK, Cui BA, Wei ZY, Li XS, Wang YB, Zhao L, Wang ZY (2009) A TaqMan-based real-time polymerase chain reaction for the detection of porcine parvovirus. J Virol Methods 156(1\u20132):84\u201388. https:\/\/doi.org\/10.1016\/j.jviromet.2008.10.029","journal-title":"J Virol Methods"},{"issue":"2","key":"10483_CR3","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1101\/cshperspect.a012989","volume":"5","author":"SF Cotmore","year":"2013","unstructured":"Cotmore SF, Tattersall P (2013) Parvovirus diversity and DNA damage responses. Cold Spring Harb Perspect Biol 5(2):152\u2013158. https:\/\/doi.org\/10.1101\/cshperspect.a012989","journal-title":"Cold Spring Harb Perspect Biol"},{"issue":"33","key":"10483_CR4","doi-asserted-by":"publisher","first-page":"3327","DOI":"10.1016\/j.vaccine.2013.05.078","volume":"31","author":"P Dar","year":"2013","unstructured":"Dar P, Kalaivanan R, Sied N, Mamo B, Kishore S, Suryanarayana VV, Kondabattula G (2013) Montanide ISA 201 adjuvanted FMD vaccine induces improved immune responses and protection in cattle. Vaccine 31(33):3327\u20133332. https:\/\/doi.org\/10.1016\/j.vaccine.2013.05.078","journal-title":"Vaccine"},{"issue":"10","key":"10483_CR5","first-page":"6","volume":"45","author":"ZG Duan","year":"2017","unstructured":"Duan ZG, Zhu CH, Zhang J, Fan DD (2017) Endotoxin removal from human-like collagen using triton X-114 two-phase extraction and affinity chromatography resin. Chem Eng 45(10):6\u201311","journal-title":"Chem Eng"},{"issue":"1","key":"10483_CR6","doi-asserted-by":"publisher","first-page":"e79575","DOI":"10.1371\/journal.pone.0079575","volume":"9","author":"H Feng","year":"2014","unstructured":"Feng H, Hu G, Wang H, Liang M, Liang H, Guo H, Zhao P, Yang Y, Zheng X, Zhang Z (2014) Canine parvovirus VP2 protein expressed in silkworm pupae self-assembles into virus-like particles with high immunogenicity. PLoS One 9(1):e79575. https:\/\/doi.org\/10.1371\/journal.pone.0079575","journal-title":"PLoS One"},{"issue":"6","key":"10483_CR7","doi-asserted-by":"publisher","first-page":"1408","DOI":"10.1099\/jgv.0.000446","volume":"97","author":"T Foerster","year":"2016","unstructured":"Foerster T, Streck AF, Speck S, Selbitz HJ, Lindner T, Truyen U (2016) An inactivated whole-virus porcine parvovirus vaccine protects pigs against disease but does not prevent virus shedding even after homologous virus challenge. J Gen Virol 97(6):1408\u20131413. https:\/\/doi.org\/10.1099\/jgv.0.000446","journal-title":"J Gen Virol"},{"issue":"7","key":"10483_CR8","doi-asserted-by":"publisher","first-page":"1258","DOI":"10.1016\/j.carbon.2005.10.038","volume":"44","author":"VM Gun\u2019Ko","year":"2006","unstructured":"Gun\u2019Ko VM, Betz WR, Patel S, Murphy MC, Mikhalovsky SV (2006) Adsorption of lipopolysaccharide on carbon sieves. Carbon 44(7):1258\u20131262","journal-title":"Carbon"},{"issue":"5","key":"10483_CR9","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1007\/s00705-013-1907-0","volume":"159","author":"C Guo","year":"2014","unstructured":"Guo C, Zhong Z, Huang Y (2014) Production and immunogenicity of VP2 protein of porcine parvovirus expressed in Pichia pastoris. Arch Virol 159(5):963\u2013970. https:\/\/doi.org\/10.1007\/s00705-013-1907-0","journal-title":"Arch Virol"},{"issue":"1","key":"10483_CR10","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1002\/bit.22886","volume":"108","author":"Y Hou","year":"2011","unstructured":"Hou Y, Jiang C, Shukla AA, Cramer SM (2011) Improved process analytical technology for protein a chromatography using predictive principal component analysis tools. Biotechnol Bioeng 108(1):59\u201368. https:\/\/doi.org\/10.1002\/bit.22886","journal-title":"Biotechnol Bioeng"},{"issue":"10","key":"10483_CR11","doi-asserted-by":"publisher","first-page":"1189","DOI":"10.14202\/vetworld.2015.1189-1198","volume":"8","author":"S Ibrahim Eel","year":"2015","unstructured":"Ibrahim Eel S, Gamal WM, Hassan AI, Mahdy Sel D, Hegazy AZ, Abdel-Atty MM (2015) Comparative study on the immunopotentiator effect of ISA 201, ISA 61, ISA 50, ISA 206 used in trivalent foot and mouth disease vaccine. Vet World 8(10):1189\u20131198. https:\/\/doi.org\/10.14202\/vetworld.2015.1189-1198","journal-title":"Vet World"},{"key":"10483_CR12","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1016\/j.antiviral.2017.01.003","volume":"139","author":"P Ji","year":"2017","unstructured":"Ji P, Liu Y, Chen Y, Wang A, Jiang D, Zhao B, Wang J, Chai S, Zhou E, Zhang G (2017) Porcine parvovirus capsid protein expressed in Escherichia coli self-assembles into virus-like particles with high immunogenicity in mice and guinea pigs. Antivir Res 139:146\u2013152. https:\/\/doi.org\/10.1016\/j.antiviral.2017.01.003","journal-title":"Antivir Res"},{"issue":"Pt 10","key":"10483_CR13","doi-asserted-by":"publisher","first-page":"2437","DOI":"10.1099\/vir.0.012054-0","volume":"90","author":"A Jozwik","year":"2009","unstructured":"Jozwik A, Manteufel J, Selbitz HJ, Truyen U (2009) Vaccination against porcine parvovirus protects against disease, but does not prevent infection and virus shedding after challenge infection with a heterologous virus strain. J Gen Virol 90(Pt 10):2437\u20132441. https:\/\/doi.org\/10.1099\/vir.0.012054-0","journal-title":"J Gen Virol"},{"issue":"1","key":"10483_CR14","first-page":"8","volume":"17","author":"A Khorasani","year":"2016","unstructured":"Khorasani A, Madadgar O, Soleimanjahi H, Keyvanfar H, Mahravani H (2016) Evaluation of the efficacy of a new oil-based adjuvant ISA 61 VG FMD vaccine as a potential vaccine for cattle. Iran J Vet Res 17(1):8\u201312","journal-title":"Iran J Vet Res"},{"issue":"4","key":"10483_CR15","first-page":"491","volume":"139","author":"C Lahariya","year":"2014","unstructured":"Lahariya C (2014) A brief history of vaccines & vaccination in India. Indian J Med Res 139(4):491\u2013511","journal-title":"Indian J Med Res"},{"issue":"6","key":"10483_CR16","doi-asserted-by":"publisher","first-page":"1497","DOI":"10.1002\/btpr.1961","volume":"30","author":"AS London","year":"2014","unstructured":"London AS, Mackay K, Lihon M, He Y, Alabi BR (2014) Gel filtration chromatography as a method for removing bacterial endotoxin from antibody preparations. Biotechnol Prog 30(6):1497\u20131501. https:\/\/doi.org\/10.1002\/btpr.1961","journal-title":"Biotechnol Prog"},{"issue":"899","key":"10483_CR17","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1007\/978-1-61779-921-1_17","volume":"899","author":"AJ Lowe","year":"2012","unstructured":"Lowe AJ, Bardliving CL, Batt CA (2012) Methods for chromatographic removal of endotoxin. Methods Mol Biol 899(899):265\u2013275. https:\/\/doi.org\/10.1007\/978-1-61779-921-1_17","journal-title":"Methods Mol Biol"},{"issue":"3","key":"10483_CR18","first-page":"388","volume":"10","author":"PO Magalhaes","year":"2007","unstructured":"Magalhaes PO, Lopes AM, Mazzola PG, Rangel-Yagui C, Penna TC, Pessoa A Jr (2007) Methods of endotoxin removal from biological preparations: a review. J Pharm Pharm Sci 10(3):388\u2013404","journal-title":"J Pharm Pharm Sci"},{"issue":"1","key":"10483_CR19","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1007\/s00253-002-0976-x","volume":"59","author":"L Maranga","year":"2002","unstructured":"Maranga L, Rueda P, Antonis AF, Vela C, Langeveld JP, Casal JI, Carrondo MJ (2002) Large scale production and downstream processing of a recombinant porcine parvovirus vaccine. Appl Microbiol Biotechnol 59(1):45\u201350. https:\/\/doi.org\/10.1007\/s00253-002-0976-x","journal-title":"Appl Microbiol Biotechnol"},{"key":"10483_CR20","doi-asserted-by":"publisher","unstructured":"Meszaros I, Olasz F, Csagola A, Tijssen P, Zadori Z (2017) Biology of porcine parvovirus (Ungulate parvovirus 1). Viruses 9(12). https:\/\/doi.org\/10.3390\/v9120393","DOI":"10.3390\/v9120393"},{"key":"10483_CR21","doi-asserted-by":"publisher","unstructured":"Oh WT, Kim RY, Nguyen VG, Chung HC, Park BK (2017) Perspectives on the evolution of porcine parvovirus. Viruses 9(8). https:\/\/doi.org\/10.3390\/v9080196","DOI":"10.3390\/v9080196"},{"issue":"8","key":"10483_CR22","doi-asserted-by":"publisher","first-page":"1261","DOI":"10.1128\/CVI.05057-11","volume":"18","author":"T Opriessnig","year":"2011","unstructured":"Opriessnig T, Shen HG, Pal N, Ramamoorthy S, Huang YW, Lager KM, Beach NM, Halbur PG, Meng XJ (2011) A live-attenuated chimeric porcine circovirus type 2 (PCV2) vaccine is transmitted to contact pigs but is not upregulated by concurrent infection with porcine parvovirus (PPV) and porcine reproductive and respiratory syndrome virus (PRRSV) and is efficacious in a PCV2b-PRRSV-PPV challenge model. Clin Vaccine Immunol 18(8):1261\u20131268. https:\/\/doi.org\/10.1128\/CVI.05057-11","journal-title":"Clin Vaccine Immunol"},{"issue":"2\u20133","key":"10483_CR23","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/s0168-1656(99)00185-6","volume":"76","author":"D Petsch","year":"2000","unstructured":"Petsch D, Anspach FB (2000) Endotoxin removal from protein solutions. J Biotechnol 76(2\u20133):97\u2013119. https:\/\/doi.org\/10.1016\/s0168-1656(99)00185-6","journal-title":"J Biotechnol"},{"issue":"4","key":"10483_CR24","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1023\/A:1023426906756","volume":"11","author":"RT Rymerson","year":"2003","unstructured":"Rymerson RT, Babiuk L, Menassa R, Vanderbeld B, Brandle JE (2003) Immunogenicity of the capsid protein VP2 from porcine parvovirus expressed in low alkaloid transgenic tobacco. Mol Breed 11(4):267\u2013276","journal-title":"Mol Breed"},{"issue":"24","key":"10483_CR25","doi-asserted-by":"publisher","first-page":"9700","DOI":"10.1016\/j.biortech.2010.07.072","volume":"101","author":"AD Smith","year":"2010","unstructured":"Smith AD, Holtzapple MT (2010) Investigation of nutrient feeding strategies in a countercurrent mixed-acid multi-staged fermentation: development of segregated-nitrogen model. Bioresour Technol 101(24):9700\u20139709. https:\/\/doi.org\/10.1016\/j.biortech.2010.07.072","journal-title":"Bioresour Technol"},{"key":"10483_CR26","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1186\/1743-422X-7-353","volume":"7","author":"C Song","year":"2010","unstructured":"Song C, Zhu C, Zhang C, Cui S (2010) Detection of porcine parvovirus using a taqman-based real-time pcr with primers and probe designed for the NS1 gene. Virol J 7:353\u2013354. https:\/\/doi.org\/10.1186\/1743-422X-7-353","journal-title":"Virol J"},{"issue":"37","key":"10483_CR27","doi-asserted-by":"publisher","first-page":"3872","DOI":"10.1016\/j.vaccine.2013.06.062","volume":"31","author":"C Sumana","year":"2013","unstructured":"Sumana C, Angelica MS, Doris C, Mary S, Terika S, Brito LA, Pu Z, Gillis O, Mandl CW, Mason PW (2013) Generation of a parvovirus B19 vaccine candidate. Vaccine 31(37):3872\u20133878. https:\/\/doi.org\/10.1016\/j.vaccine.2013.06.062","journal-title":"Vaccine"},{"issue":"3","key":"10483_CR28","doi-asserted-by":"publisher","first-page":"e0173778","DOI":"10.1371\/journal.pone.0173778","volume":"12","author":"M Teodorowicz","year":"2017","unstructured":"Teodorowicz M, Perdijk O, Verhoek I, Govers C, Savelkoul HF, Tang Y, Wichers H, Broersen K (2017) Optimized Triton X-114 assisted lipopolysaccharide (LPS) removal method reveals the immunomodulatory effect of food proteins. PLoS One 12(3):e0173778. https:\/\/doi.org\/10.1371\/journal.pone.0173778","journal-title":"PLoS One"},{"key":"10483_CR29","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1186\/1297-9716-42-105","volume":"42","author":"SJ van Beurden","year":"2011","unstructured":"van Beurden SJ, Leroy B, Wattiez R, Haenen OL, Boeren S, Vervoort JJ, Peeters BP, Rottier PJ, Engelsma MY, Vanderplasschen AF (2011) Identification and localization of the structural proteins of anguillid herpesvirus 1. Vet Res 42:105. https:\/\/doi.org\/10.1186\/1297-9716-42-105","journal-title":"Vet Res"},{"issue":"2","key":"10483_CR30","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1016\/S0034-5288(18)31968-4","volume":"36","author":"AE Wrathall","year":"1984","unstructured":"Wrathall AE, Wells DE, Cartwright SF, Frerichs GN (1984) An inactivated, oil-emulsion vaccine for the prevention of porcine parvovirus-induced reproductive failure. Res Vet Sci 36(2):136\u2013143","journal-title":"Res Vet Sci"},{"key":"10483_CR31","doi-asserted-by":"publisher","first-page":"366","DOI":"10.1186\/1743-422X-7-366","volume":"7","author":"H Zhou","year":"2010","unstructured":"Zhou H, Yao G, Cui S (2010) Production and purification of VP2 protein of porcine parvovirus expressed in an insect-baculovirus cell system. Virol J 7:366. https:\/\/doi.org\/10.1186\/1743-422X-7-366","journal-title":"Virol J"},{"issue":"1","key":"10483_CR32","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.pep.2012.06.016","volume":"85","author":"Y Zhou","year":"2012","unstructured":"Zhou Y, Ma X, Hou Z, Xue X, Meng J, Li M, Jia M, Luo X (2012) High cell density cultivation of recombinant Escherichia coli for prodrug of recombinant human GLPs production. Protein Expr Purif 85(1):38\u201343. https:\/\/doi.org\/10.1016\/j.pep.2012.06.016","journal-title":"Protein Expr Purif"},{"issue":"4","key":"10483_CR33","doi-asserted-by":"publisher","first-page":"1545","DOI":"10.1007\/s00253-017-8700-z","volume":"102","author":"Y Zhou","year":"2018","unstructured":"Zhou Y, Lu Z, Wang X, Selvaraj JN, Zhang G (2018) Genetic engineering modification and fermentation optimization for extracellular production of recombinant proteins using Escherichia coli. Appl Microbiol Biotechnol 102(4):1545\u20131556. https:\/\/doi.org\/10.1007\/s00253-017-8700-z","journal-title":"Appl Microbiol Biotechnol"}],"container-title":["Applied Microbiology and Biotechnology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00253-020-10483-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00253-020-10483-5\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00253-020-10483-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,3,3]],"date-time":"2021-03-03T19:28:02Z","timestamp":1614799682000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00253-020-10483-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,4]]},"references-count":33,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2020,5]]}},"alternative-id":["10483"],"URL":"https:\/\/doi.org\/10.1007\/s00253-020-10483-5","relation":{},"ISSN":["0175-7598","1432-0614"],"issn-type":[{"value":"0175-7598","type":"print"},{"value":"1432-0614","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,3,4]]},"assertion":[{"value":"12 November 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"9 February 2020","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 February 2020","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 March 2020","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare that they have no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"All animal experiments were approved by the Animal Experiment Committee of Henan Academy of Agricultural Sciences with the approval number (LLSC1009605 and LLSC1009618). All the animals received humane care in compliance with good animal practice according to the animal ethics procedures and guidelines of the Institutional Animal Care and Use Committee (IACUC). All efforts were made to alleviate and minimize animal suffering.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical statement"}}]}}