{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T06:30:29Z","timestamp":1790749829966,"version":"4.1.0"},"reference-count":108,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2017,3,29]],"date-time":"2017-03-29T00:00:00Z","timestamp":1490745600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/501100004920","name":"Royan Institute","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004920","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003968","name":"Iran National Science Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100003968","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biotechnology Journal"],"published-print":{"date-parts":[[2017,5]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Chick embryos are a significant historical research model in basic and applied sciences. The embryonated eggs have been used for virus inoculation in order to vaccine production for nearly a century. Recently, avian eggs and cell lines derived from embryonated eggs have found wide application in biotechnology. This review will discuss about the unique characteristics of avian eggs in terms of safety, large scale and economical production of recombinant proteins. This system also provides the human\u2010like glycosylation on target proteins and therefore can be considered as a suitable host for biomanufacturing of humanized monoclonal antibodies and therapeutic proteins. Avian derived cell lines are an alternative for rapid vaccine manufacturing during a pandemic. Based on the latest knowledge in cell and animal transgenesis, the currently available germ cell\u2010mediated gene transfer system provides a more efficient strategy in gene targeting and creation of transgenic birds that lead to advancements in industrial, biotechnology, and biological research applications. This review covers the recent development of avian fertilized eggs and related cell lines in a variety of human biopharmaceuticals and viral vaccine manufacturing.<\/jats:p>","DOI":"10.1002\/biot.201600598","type":"journal-article","created":{"date-parts":[[2017,3,29]],"date-time":"2017-03-29T03:52:55Z","timestamp":1490759575000},"source":"Crossref","is-referenced-by-count":42,"title":["Avian embryos and related cell lines: A convenient platform for recombinant proteins and vaccine production"],"prefix":"10.1002","volume":"12","author":[{"given":"Maryam","family":"Farzaneh","sequence":"first","affiliation":[{"name":"Department of Stem Cells and Developmental Biology, Cell Science Research Center Royan Institute for Stem Cell Biology and Technology, ACECR  Tehran Iran"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seyedeh\u2010Nafiseh","family":"Hassani","sequence":"additional","affiliation":[{"name":"Department of Stem Cells and Developmental Biology, Cell Science Research Center Royan Institute for Stem Cell Biology and Technology, ACECR  Tehran Iran"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Mozdziak","sequence":"additional","affiliation":[{"name":"Graduate Physiology Program Campus Box 7608\/321 Scott Hall  Raleigh NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hossein","family":"Baharvand","sequence":"additional","affiliation":[{"name":"Department of Stem Cells and Developmental Biology, Cell Science Research Center Royan Institute for Stem Cell Biology and Technology, ACECR  Tehran Iran"},{"name":"Department of Developmental Biology University of Science and Culture  Tehran Iran"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2017,3,29]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"crossref","unstructured":"Hornblower S. Spawforth A. Eidinow E. The Oxford Companion to Classical Civilization OUP Oxford2014.","DOI":"10.1093\/acref\/9780198706779.001.0001"},{"key":"e_1_2_8_3_1","doi-asserted-by":"publisher","DOI":"10.1002\/dvdy.24093"},{"key":"e_1_2_8_4_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.74.1919.371"},{"key":"e_1_2_8_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.devcel.2004.11.018"},{"key":"e_1_2_8_6_1","doi-asserted-by":"publisher","DOI":"10.1111\/asj.12620"},{"key":"e_1_2_8_7_1","doi-asserted-by":"publisher","DOI":"10.1093\/ilar.51.4.353"},{"key":"e_1_2_8_8_1","first-page":"419","article-title":"The avian EB66\u00ae cell line, application to vaccines, and therapeutic protein production","volume":"64","author":"Brown S. W.","year":"2010","journal-title":"PDA J. Pharm. Sci. Technol."},{"key":"e_1_2_8_9_1","unstructured":"Guehenneux F. Moreau K. Esnault M. Mehtali M. Generation of duck cell lines.US\u2010Patent 9260694 B2 2016."},{"key":"e_1_2_8_10_1","doi-asserted-by":"publisher","DOI":"10.1002\/1098-2795(200008)56:4<475::AID-MRD5>3.0.CO;2-M"},{"key":"e_1_2_8_11_1","doi-asserted-by":"publisher","DOI":"10.4103\/1008-682X.148073"},{"key":"e_1_2_8_12_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature04831"},{"key":"e_1_2_8_13_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11427-012-4426-4"},{"key":"e_1_2_8_14_1","doi-asserted-by":"publisher","DOI":"10.1089\/scd.2011.0499"},{"key":"e_1_2_8_15_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2011.08.122"},{"key":"e_1_2_8_16_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2009.05.083"},{"key":"e_1_2_8_17_1","doi-asserted-by":"publisher","DOI":"10.1186\/1753-6561-5-S8-P52"},{"key":"e_1_2_8_18_1","doi-asserted-by":"publisher","DOI":"10.14348\/molcells.2015.0225"},{"key":"e_1_2_8_19_1","doi-asserted-by":"publisher","DOI":"10.1002\/biot.201500579"},{"key":"e_1_2_8_20_1","doi-asserted-by":"publisher","DOI":"10.1002\/biot.201600105"},{"key":"e_1_2_8_21_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10295-011-1082-9"},{"key":"e_1_2_8_22_1","first-page":"75","article-title":"Making recombinant proteins in filamentous fungi\u2010are we expecting too much?","volume":"5","author":"Nevalainen H.","year":"2014","journal-title":"Front. Microbiol."},{"key":"e_1_2_8_23_1","doi-asserted-by":"publisher","DOI":"10.4161\/bioe.22856"},{"key":"e_1_2_8_24_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrg1177"},{"key":"e_1_2_8_25_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00253-011-3758-5"},{"key":"e_1_2_8_26_1","doi-asserted-by":"publisher","DOI":"10.1002\/biot.201400647"},{"key":"e_1_2_8_27_1","doi-asserted-by":"publisher","DOI":"10.4161\/mabs.2.5.12720"},{"key":"e_1_2_8_28_1","doi-asserted-by":"publisher","DOI":"10.1002\/biot.201400765"},{"key":"e_1_2_8_29_1","doi-asserted-by":"publisher","DOI":"10.1385\/MB:34:2:225"},{"key":"e_1_2_8_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cimid.2007.11.005"},{"key":"e_1_2_8_31_1","doi-asserted-by":"publisher","DOI":"10.1111\/dgd.12032"},{"key":"e_1_2_8_32_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11248-011-9511-0"},{"key":"e_1_2_8_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jbiosc.2013.11.010"},{"key":"e_1_2_8_34_1","doi-asserted-by":"publisher","DOI":"10.1038\/nbt1132"},{"key":"e_1_2_8_35_1","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.f.202"},{"key":"e_1_2_8_36_1","doi-asserted-by":"publisher","DOI":"10.1080\/19420862.2015.1117719"},{"key":"e_1_2_8_37_1","first-page":"44","article-title":"Glycosylation variations with expression systems","volume":"1","author":"Raju S.","year":"2003","journal-title":"Bioprocess Int."},{"key":"e_1_2_8_38_1","doi-asserted-by":"publisher","DOI":"10.1002\/biot.201400388"},{"key":"e_1_2_8_39_1","doi-asserted-by":"publisher","DOI":"10.3892\/ijmm.2015.2397"},{"key":"e_1_2_8_40_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M210665200"},{"key":"e_1_2_8_41_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0167-7799(02)00009-4"},{"key":"e_1_2_8_42_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.copbio.2004.08.006"},{"key":"e_1_2_8_43_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ymeth.2013.08.005"},{"key":"e_1_2_8_44_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1359-6446(04)03317-3"},{"key":"e_1_2_8_45_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tibtech.2006.01.004"},{"key":"e_1_2_8_46_1","doi-asserted-by":"publisher","DOI":"10.1023\/A:1025854217349"},{"key":"e_1_2_8_47_1","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.79.17.10864-10874.2005"},{"key":"e_1_2_8_48_1","doi-asserted-by":"publisher","DOI":"10.3382\/ps.2013-03223"},{"key":"e_1_2_8_49_1","doi-asserted-by":"publisher","DOI":"10.5483\/BMBRep.2013.46.8.251"},{"key":"e_1_2_8_50_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11248-009-9327-3"},{"key":"e_1_2_8_51_1","doi-asserted-by":"publisher","DOI":"10.1096\/fj.14-264739"},{"key":"e_1_2_8_52_1","doi-asserted-by":"publisher","DOI":"10.1038\/nbt0216-117"},{"key":"e_1_2_8_53_1","doi-asserted-by":"publisher","DOI":"10.1586\/erv.09.128"},{"key":"e_1_2_8_54_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2015.06.110"},{"key":"e_1_2_8_55_1","first-page":"4I","article-title":"Growth and maintenance of chick embryo fibroblasts (CEF)","author":"Hernandez R.","year":"2010","journal-title":"Curr. Protoc. Microbiol."},{"key":"e_1_2_8_56_1","doi-asserted-by":"publisher","DOI":"10.3382\/ps.2012-02582"},{"key":"e_1_2_8_57_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.122.8.2339"},{"key":"e_1_2_8_58_1","unstructured":"Mehtali M. Champion\u2010Arnaud P. Leon A. Production of viral vaccines in suspension on avian embryonic derived stem cell lines.US\u2010Patent 20150275186 A1 2015."},{"key":"e_1_2_8_59_1","doi-asserted-by":"publisher","DOI":"10.4161\/mabs.12350"},{"key":"e_1_2_8_60_1","unstructured":"Petitte J. N. Yang Z. Method of producing an avian embryonic stem cell culture and the avian embryonic stem cell culture produced by the process.U.S. Patent 07884423 1992."},{"key":"e_1_2_8_61_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0069893"},{"key":"e_1_2_8_62_1","first-page":"2854","article-title":"Stem cell theory for the pathogenesis of endometriosis","volume":"4","author":"Maruyama T.","year":"2012","journal-title":"Front. Biosci. (Elite Ed.)"},{"key":"e_1_2_8_63_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biologicals.2015.09.002"},{"key":"e_1_2_8_64_1","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.71.4.3005-3012.1997"},{"key":"e_1_2_8_65_1","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6822(87)90334-5"},{"key":"e_1_2_8_66_1","doi-asserted-by":"publisher","DOI":"10.1038\/nbt0194-60"},{"key":"e_1_2_8_67_1","doi-asserted-by":"publisher","DOI":"10.1038\/srep23980"},{"key":"e_1_2_8_68_1","doi-asserted-by":"publisher","DOI":"10.1093\/ps\/84.9.1477"},{"key":"e_1_2_8_69_1","doi-asserted-by":"publisher","DOI":"10.1038\/225072a0"},{"key":"e_1_2_8_70_1","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1242\/dev.108.1.185","article-title":"Production of somatic and germline chimeras in the chicken by transfer of early blastodermal cells","volume":"108","author":"Petitte J.","year":"1990","journal-title":"Development"},{"key":"e_1_2_8_71_1","first-page":"69","article-title":"Embryonic expression of beta\u2010actin\u2010lacZ hybrid gene injected into the fertilized ovum of the domestic fowl","volume":"35","author":"Naito M.","year":"1991","journal-title":"The International J. Dev. Biol."},{"key":"e_1_2_8_72_1","doi-asserted-by":"publisher","DOI":"10.1002\/mrd.1080370207"},{"key":"e_1_2_8_73_1","doi-asserted-by":"publisher","DOI":"10.1006\/cbir.1997.0173"},{"key":"e_1_2_8_74_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1098-2795(199712)48:4<501::AID-MRD11>3.0.CO;2-W"},{"key":"e_1_2_8_75_1","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1050880104"},{"key":"e_1_2_8_76_1","doi-asserted-by":"publisher","DOI":"10.1016\/0012-1606(76)90178-0"},{"key":"e_1_2_8_77_1","doi-asserted-by":"publisher","DOI":"10.1002\/jez.1401470308"},{"key":"e_1_2_8_78_1","doi-asserted-by":"publisher","DOI":"10.3382\/ps.0680999"},{"key":"e_1_2_8_79_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.117.2.669"},{"key":"e_1_2_8_80_1","doi-asserted-by":"publisher","DOI":"10.1002\/mrd.1080390206"},{"key":"e_1_2_8_81_1","doi-asserted-by":"publisher","DOI":"10.1159\/000016701"},{"key":"e_1_2_8_82_1","doi-asserted-by":"publisher","DOI":"10.1089\/scd.2008.0223"},{"key":"e_1_2_8_83_1","doi-asserted-by":"publisher","DOI":"10.3382\/ps.2010-01011"},{"key":"e_1_2_8_84_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.mod.2005.10.002"},{"key":"e_1_2_8_85_1","doi-asserted-by":"publisher","DOI":"10.3382\/ps.2009-00413"},{"key":"e_1_2_8_86_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.dci.2009.12.008"},{"key":"e_1_2_8_87_1","doi-asserted-by":"publisher","DOI":"10.3724\/SP.J.1005.2013.00365"},{"key":"e_1_2_8_88_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1118715109"},{"key":"e_1_2_8_89_1","first-page":"e33","article-title":"Isolation and biological characterization of chicken amnion epithelial cells. Eur","volume":"56","author":"Gao Y.","year":"2012","journal-title":"J. Histochem."},{"key":"e_1_2_8_90_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1410555111"},{"key":"e_1_2_8_91_1","first-page":"1","article-title":"Generation of chickens expressing Cre recombinase","author":"Leighton P. A.","year":"2016","journal-title":"Transgenic Res."},{"key":"e_1_2_8_92_1","doi-asserted-by":"publisher","DOI":"10.1534\/g3.116.027706"},{"key":"e_1_2_8_93_1","doi-asserted-by":"publisher","DOI":"10.1038\/sj.embor.7400171"},{"key":"e_1_2_8_94_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0610401104"},{"key":"e_1_2_8_95_1","doi-asserted-by":"publisher","DOI":"10.1093\/ps\/86.10.2221"},{"key":"e_1_2_8_96_1","doi-asserted-by":"publisher","DOI":"10.1002\/mrd.20860"},{"key":"e_1_2_8_97_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.109.081687"},{"key":"e_1_2_8_98_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0118626"},{"key":"e_1_2_8_99_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0127922"},{"key":"e_1_2_8_100_1","first-page":"349","article-title":"Characterization of stage\u2010specific embryonic antigen\u20101 (SSEA\u20101) expression during early development of the turkey embryo","volume":"43","author":"D'Costa S.","year":"2004","journal-title":"Int. J. Dev. Biol."},{"key":"e_1_2_8_101_1","doi-asserted-by":"publisher","DOI":"10.2141\/jpsa.010102"},{"key":"e_1_2_8_102_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.113.113381"},{"key":"e_1_2_8_103_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.theriogenology.2015.04.032"},{"key":"e_1_2_8_104_1","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.00036"},{"key":"e_1_2_8_105_1","doi-asserted-by":"publisher","DOI":"10.1242\/dev.006569"},{"key":"e_1_2_8_106_1","doi-asserted-by":"publisher","DOI":"10.1634\/stemcells.2004-0208"},{"key":"e_1_2_8_107_1","doi-asserted-by":"publisher","DOI":"10.1089\/cell.2014.0028"},{"key":"e_1_2_8_108_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0015518"},{"key":"e_1_2_8_109_1","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.102.006825"}],"container-title":["Biotechnology Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fbiot.201600598","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/analyticalsciencejournals.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/biot.201600598","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T15:45:34Z","timestamp":1759938334000},"score":1,"resource":{"primary":{"URL":"https:\/\/analyticalsciencejournals.onlinelibrary.wiley.com\/doi\/10.1002\/biot.201600598"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,3,29]]},"references-count":108,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2017,5]]}},"alternative-id":["10.1002\/biot.201600598"],"URL":"https:\/\/doi.org\/10.1002\/biot.201600598","archive":["Portico"],"relation":{},"ISSN":["1860-6768","1860-7314"],"issn-type":[{"value":"1860-6768","type":"print"},{"value":"1860-7314","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,3,29]]},"article-number":"1600598"}}