Mesenchymal stem cells (MSCs) are multipotent progenitor cells that adhere to plastic; express the specific markers CD29, CD44, CD73, CD90, and CD105; and produce cytokines and growth factors supporting and regulating hematopoiesis. MSCs have capacity for differentiating into osteocytes, chondrocytes, adipocytes, and myocytes. They are useful for research toward better understanding the pathogenic potential of the infectious bursal disease virus, mineralization during osteogenesis, and interactions between MSCs as a feeder layer to other cells. MSCs are also important for immunomodulatory cell therapy, can provide a suitable strategy model for coculture with pathogens causing dermatitis disorders in chickens, can be cultured in vitro with probiotics and prebiotics with a view to eliminate the feeding of antibiotic growth promoters, and offer cell-based meat production. Moreover, bone marrow-derived MSCs (BM-MSCs) in coculture with hematopoietic progenitor/stem cells (HPCs/HSCs) can support expansion and regulation of the hematopoiesis process using the 3D-culture system in future research in chickens. MSCs' several advantages, including ready availability, strong proliferation, and immune modulatory properties make them a suitable model in the field of stem cell research. This review summarizes current knowledge about the general characterization of MSCs and their application in chicken as a model organism.

Department of Animal Morphology Physiology and Genetics Faculty of AgriSciences Mendel University in Brno 613 00 Brno Czech Republic

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Mir N.A., Rafiq A., Kumar F., Singh V., Shukla V. Determinants of broiler chicken meat quality and factors affecting them: A review. J. Food Sci. Technol. 2017;54:2997–3009. doi: 10.1007/s13197-017-2789-z. PubMed DOI PMC

Fornari M.B., Zanella R., Ibelli A.M., Fernandes L.T., Cantão M.E., Thomaz-Soccol V., Ledur M.C., Peixoto J.O. Unraveling the associations of osteoprotegerin gene with production traits in a paternal broiler line. SpringerPlus. 2014;3:1–8. doi: 10.1186/2193-1801-3-682. PubMed DOI PMC

Prockop D.J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276:71–74. doi: 10.1126/science.276.5309.71. PubMed DOI

Crigler L., Kazhanie A., Yoon T.J., Zakhari J., Anders J., Taylor B., Virador V.M. Isolation of a mesenchymal cell population from murine dermis that contains progenitors of multiple cell lineages. FASEB J. 2007;21:2050–2063. doi: 10.1096/fj.06-5880com. PubMed DOI PMC

Dumas A., Le Drévo M.A., Moreau M.F., Guillet C., Baslé M.F., Chappard D. Isolation of osteoprogenitors from murine bone marrow by selection of CD11b negative cells. Cytotechnology. 2008;58:163. doi: 10.1007/s10616-009-9184-1. PubMed DOI PMC

Kar S., Mitra S., Banerjee E.R. Isolation and culture of embryonic stem cells, mesenchymal stem cells, and dendritic cells from humans and mice. Methods. Mol. Biol. 2015;1516:145–152. doi: 10.1007/7651_2015_315. PubMed DOI

Kumar K., Agarwal P., Das K., Mili B., Madhusoodan A.P., Kumar A., Bag S. Isolation and characterization of mesenchymal stem cells from caprine umbilical cord tissue matrix. Tissue Cell. 2016;48:653–658. doi: 10.1016/j.tice.2016.06.004. PubMed DOI

Li H., Ghazanfari R., Zacharaki D., Lim H.C., Scheding S. Isolation and characterization of primary bone marrow mesenchymal stromal cells. Ann. N. Y. Acad. Sci. 2016;1370:109–118. doi: 10.1111/nyas.13102. PubMed DOI

Krešić N., Šimić I., Lojkić I., Bedeković T. Canine adipose derived mesenchymal stem cells transcriptome composition alterations: A step towards standardizing therapeutic. Stem Cells Int. 2017 doi: 10.1155/2017/4176292. PubMed DOI PMC

Nakamura M., Nishida H., Yoshizaki K., Akiyoshi H., Hatoya S., Sugiura K., Inaba T. Canine mesenchymal stromal cell-conditioned medium promotes survival and neurite outgrowth of neural stem cells. J. Vet. Med. Sci. 2020 doi: 10.1292/jvms.19-0141. PubMed DOI PMC

Munoz J.L., Greco S.J., Patel S.A., Sherman L.S., Bhatt S., Bhatt R.S., Shrensel J.A., Guan Y.Z., Xie G., Ye J.H., et al. Feline bone marrow-derived mesenchymal stromal cells (MSCs) show similar phenotype and functions with regards to neuronal differentiation as human MSCs. Differentiation. 2012;84:214–222. doi: 10.1016/j.diff.2012.07.002. PubMed DOI PMC

Dominici M.L.B.K., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F.C., Krause D.S., Horwitz E.M. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–317. doi: 10.1080/14653240600855905. PubMed DOI

Majumdar M.K., Thiede M.A., Mosca J.D., Moorman M., Gerson S.L. Phenotypic and functional comparison of cultures of marrow--derived mesenchymal stem cells (MSCs) and stromal cells. J. Cell. Physiol. 1998;176:57–66. doi: 10.1002/(SICI)1097-4652(199807)176:1<57::AID-JCP7>3.0.CO;2-7. PubMed DOI

Eleuteri S., Fierabracci A. Insights into the secretome of mesenchymal stem cells and its potential applications. Inter. J. Mol. Sci. 2020;20:4597. doi: 10.3390/ijms20184597. PubMed DOI PMC

Fu X., Liu G., Halim A., Ju Y., Luo Q., Song G. Mesenchymal stem cell migration and tissue repair. Cells. 2019;8:784. doi: 10.3390/cells8080784. PubMed DOI PMC

Zannetti A., Benga G., Brunetti A., Napolitano F., Avallone L., Pelagalli A. Role of Aquaporins in the Physiological Functions of Mesenchymal Stem Cells. Cells. 2020;9:2678. doi: 10.3390/cells9122678. PubMed DOI PMC

Khatri M., Sharma J.M. Susceptibility of chicken mesenchymal stem cells to infectious bursal disease virus. J. Virol. Methods. 2009;160:197–199. doi: 10.1016/j.jviromet.2009.05.008. PubMed DOI

Adhikari R., Chen C., Waters E., West F.D., Kim W.K. Isolation and differentiation of mesenchymal stem cells from broiler chicken compact bones. Front. Physiol. 2019;9:1892. doi: 10.3389/fphys.2018.01892. PubMed DOI PMC

Bai C., Hou L., Ma Y., Chen L., Zhang M., Guan W. Isolation and characterization of mesenchymal stem cells from chicken bone marrow. Cell Tissue Bank. 2013;14:437–451. doi: 10.1007/s10561-012-9347-8. PubMed DOI

Wang X., Wang J.J., Ji H., Guan W., Zhao Y. Isolation, culture, and characterization of chicken lung-derived mesenchymal stem cells. Can. J. Vet. Res. 2018;82:225–235. PubMed PMC

Teresa Conconi M., Di Liddo R., Tommasini M., Calore C., Paolo Parnigotto P. Phenotype and differentiation potential of stromal populations obtained from various zones of human umbilical cord: An overview. J. Tissue Eng. Regen. Med. 2011;4:6–20. doi: 10.2174/1875043501104010006. DOI

Lin C.S., Xin Z.C., Dai J., Lue T.F. Commonly used mesenchymal stem cell markers and tracking labels: Limitations and challenges. Histol. Histopathol. 2013;28:1109. doi: 10.14670/HH-28.1109. PubMed DOI PMC

Cruz F.F., Rocco P.R.M. The potential of mesenchymal stem cell therapy for chronic lung disease. Expert. Rev. Respir. Med. 2020;14:31–39. doi: 10.1080/17476348.2020.1679628. PubMed DOI

Nichols J., Zevnik B., Anastassiadis K., Niwa H., Klewe-Nebenius D., Chambers I., Schöler H., Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell. 1998;95:379–391. doi: 10.1016/S0092-8674(00)81769-9. PubMed DOI

Chambers I., Colby D., Robertson M., Nichols J., Lee S., Tweedie S., Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003;113:643–655. doi: 10.1016/S0092-8674(03)00392-1. PubMed DOI

Avilion A.A., Nicolis S.K., Pevny L.H., Perez L., Vivian N., Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003;17:126–140. doi: 10.1101/gad.224503. PubMed DOI PMC

Lavial F., Acloque H., Bertocchini F., MacLeod D.J., Boast S., Bachelard E., Montillet G., Thenot S., Sang H.M., Stern C.D., et al. The Oct4 homologue PouV and Nanog regulate pluripotency in chicken embryonic stem cells. Development. 2007;134:3549–3563. doi: 10.1242/dev.006569. PubMed DOI

Khatri M., O’Brien T.D., Goyal S.M., Sharma J.M. Isolation and characterization of chicken lung mesenchymal stromal cells and their susceptibility to avian influenza virus. Dev. Comp. Immunol. 2010;34:474–479. doi: 10.1016/j.dci.2009.12.008. PubMed DOI PMC

Bai C., Li X., Hou L., Zhang M., Guan W., Ma Y. Biological characterization of chicken mesenchymal stem/progenitor cells from umbilical cord Wharton’s jelly. Mol. Cell. Biochem. 2013;376:95–102. doi: 10.1007/s11010-012-1553-y. PubMed DOI

Krampera M., Glennie S., Dyson J., Scott D., Laylor R., Simpson E., Dazzi F. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood. 2003;101:3722–3729. doi: 10.1182/blood-2002-07-2104. PubMed DOI

Maitra B., Szekely E., Gjini K., Laughlin M.J., Dennis J., Haynesworth S.E., Koç O.N. Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplant. 2004;33:597–604. doi: 10.1038/sj.bmt.1704400. PubMed DOI

Beyth S., Borovsky Z., Mevorach D., Liebergall M., Gazit Z., Aslan G.E., Rachmilewitz J. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood. 2005;105:2214–2219. doi: 10.1182/blood-2004-07-2921. PubMed DOI

Groh M.E., Maitra B., Szekely E., Koç O.N. Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Ex. Hematol. 2005;33:928–934. doi: 10.1016/j.exphem.2005.05.002. PubMed DOI

Meisel R., Zibert A., Laryea M., Göbel U., Däubener W., Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2, 3-dioxygenase–mediated tryptophan degradation. Blood. 2004;103:4619–4621. doi: 10.1182/blood-2003-11-3909. PubMed DOI

Parhami F., Morrow A.D., Balucan J., Leitinger N., Watson A.D., Tintut Y., Berliner J.A., Demer L.L. Lipid oxidation products have opposite effects on calcifying vascular cell and bone cell differentiation: A possible explanation for the paradox of arterial calcification in osteoporotic patients. Arterioscler. Tthromb. Vasc. Biol. 1997;17:680–687. doi: 10.1161/01.ATV.17.4.680. PubMed DOI

Kocamaz E., Gok D., Cetinkaya A., Tufan A.C. Implication of C-type natriuretic peptide-3 signaling in glycosaminoglycan synthesis and chondrocyte hypertrophy during TGF-β1 induced chondrogenic differentiation of chicken bone marrow-derived mesenchymal stem cells. J. Mol. His. 2012;43:497–508. doi: 10.1007/s10735-012-9430-2. PubMed DOI

Kyurkchiev D., Bochev I., Ivanova-Todorova E., Mourdjeva M., Oreshkova T., Belemezova K., Belemezova K., Kyurkchiev S. Secretion of immunoregulatory cytokines by mesenchymal stem cells. World J. Stem Cells. 2014;6:552–570. doi: 10.4252/wjsc.v6.i5.552. PubMed DOI PMC

Mazzoni A., Bronte V., Visintin A., Spitzer J.H., Apolloni E., Serafini P., Zanovello P., Segal D.M. Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J. Immunol. 2002;168:689–695. doi: 10.4049/jimmunol.168.2.689. PubMed DOI

Mais A., Klein T., Ullrich V., Schudt C., Lauer G. Prostanoid pattern and iNOS expression during chondrogenic differentiation of human mesenchymal stem cells. J. Cell. Biochem. 2006;98:798–809. doi: 10.1002/jcb.20786. PubMed DOI

Glennie S., Soeiro I., Dyson P.J., Lam E.W.F., Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood. 2005;105:2821–2827. doi: 10.1182/blood-2004-09-3696. PubMed DOI

Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., Risso M., Gualandi F., Luigi G., Pistoia M.V., et al. Human mesenchymal stem cells modulate B-cell functions. Blood. 2006;107:367–372. doi: 10.1182/blood-2005-07-2657. PubMed DOI

Djouad F., Plence P., Bony C., Tropel P., Apparailly F., Sany J., Jorgensen C. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003;102:3837–3844. doi: 10.1182/blood-2003-04-1193. PubMed DOI

Adams G.B., Scadden D.T. The hematopoietic stem cell in its place. Nat. Immunol. 2006;7:333–337. doi: 10.1038/ni1331. PubMed DOI

Wagner W., Roderburg C., Wein F., Diehlmann A., Frankhauser M., Schubert R., Eckstein V., Ho A.D. Molecular and secretory profiles of human mesenchymal stromal cells and their abilities to maintain primitive hematopoietic progenitors. Stem Cells. 2007;25:2638–2647. doi: 10.1634/stemcells.2007-0280. PubMed DOI

Leisten I., Kramann R., Ferreira M.S.V., Bovi M., Neuss S., Ziegler P., Wagner W., Knüchel R., Schneider R.K. 3D co-culture of hematopoietic stem and progenitor cells and mesenchymal stem cells in collagen scaffolds as a model of the hematopoietic niche. Biomaterials. 2012;33:1736–1747. doi: 10.1016/j.biomaterials.2011.11.034. PubMed DOI

Walenda T., Bokermann G., Ferreira M.S.V., Piroth D.M., Hieronymus T., Neuss S., Zenke M., Ho A.D., Müller A.M., Wagner W. Synergistic effects of growth factors and mesenchymal stromal cells for expansion of hematopoietic stem and progenitor cells. Exp. Hematol. 2011;39:617–628. doi: 10.1016/j.exphem.2011.02.011. PubMed DOI

Walenda T., Bork S., Horn P., Wein F., Saffrich R., Diehlmann A., Eckstein V., Ho A.D., Wagner W. Co--culture with mesenchymal stromal cells increases proliferation and maintenance of haematopoietic progenitor cells. J. Cell Mol. Med. 2010;14:337–350. doi: 10.1111/j.1582-4934.2009.00776.x. PubMed DOI PMC

Rustad K.C., Wong V.W., Sorkin M., Glotzbach J.P., Major M.R., Rajadas J., Longaker M.T., Gurtner G.C. Enhancement of mesenchymal stem cell angiogenic capacity and stemness by a biomimetic hydrogel scaffold. Biomaterials. 2012;33:80–90. doi: 10.1016/j.biomaterials.2011.09.041. PubMed DOI PMC

Li Z., Tian X., Yuan Y., Song Z., Zhang L., Wang X., Li T. Effect of cell culture using chitosan membranes on stemness marker genes in mesenchymal stem cells. Mol. Med. Rep. 2013;7:1945–1949. doi: 10.3892/mmr.2013.1423. PubMed DOI

Su N., Gao P.L., Wang K., Wang J.Y., Zhong Y., Luo Y. Fibrous scaffolds potentiate the paracrine function of mesenchymal stem cells: A new dimension in cell-material interaction. Biomaterials. 2017;141:74–85. doi: 10.1016/j.biomaterials.2017.06.028. PubMed DOI

Qian C., Zhou Z., Han H., Zhao C., Jin X., Zhao H., Zhang Y., Chen W., Yang N., Li Z. Influence of microgravity on the concentration of circulating primordial germ cells in Silky chicken offspring. J. Poult. Sci. 2009;47:65–70. doi: 10.2141/jpsa.009036. DOI

Naeemipour M., Dehghani H., Bassami M., Bahrami A. Expression dynamics of pluripotency genes in chicken primordial germ cells before and after colonization of the genital ridges. Mol. Reprod. Dev. 2013;80:849–861. doi: 10.1002/mrd.22216. PubMed DOI

Tonus C., Cloquette K., Ectors F., Piret J., Gillet L., Antoine N., Grobet L. Long term-cultured and cryopreserved primordial germ cells from various chicken breeds retain high proliferative potential and gonadal colonisation competency. Reprod. Fertil. Dev. 2016;28:628–639. doi: 10.1071/RD14194. PubMed DOI

Li D., Chen Z., Chen S., Ji H., Zhan X., Luo D., Luo H., Wang B. Chicken Mesenchymal Stem Cells as Feeder Cells Facilitate the Cultivation of Primordial Germ Cells from Circulating Blood and Gonadal Ridge. Stem Cell Discov. 2019;9:1–14. doi: 10.4236/scd.2019.91001. DOI

Xie H., Sun L., Zhang L., Liu T., Chen L., Zhao A., Gao F., Zou P., Li Q., Guo A.J., et al. Mesenchymal stem cell-derived microvesicles support ex vivo expansion of cord blood-derived CD34+ cells. Stem Cells. 2016 doi: 10.1155/2016/6493241. PubMed DOI PMC

Iacono M.L., Anzalone R., La Rocca G., Baiamonte E., Maggio A., Acuto S. Wharton’s jelly mesenchymal stromal cells as a feeder layer for the ex vivo expansion of hematopoietic stem and progenitor cells: A review. Stem. Cell. Rev. Rep. 2017;13:35–49. doi: 10.1007/s12015-016-9702-4. PubMed DOI

Chang Y.H., Chu T.Y., Ding D.C. WNT/β-Catenin signaling pathway regulates non-tumorigenesis of human embryonic stem cells co-cultured with human umbilical cord mesenchymal stem cells. Sci. Rep. 2017;7:1–10. doi: 10.1038/srep41913. PubMed DOI PMC

Zmrhal V., Slama P. Current knowledge about interactions between avian dendritic cells and poultry pathogens. Dev. Comp. Immunol. 2020;104:103565. doi: 10.1016/j.dci.2019.103565. PubMed DOI

Tippenhauer M., Heller D.E., Weigend S., Rautenschlein S. The host genotype influences infectious bursal disease virus pathogenesis in chickens by modulation of T cells responses and cytokine gene expression. Dev. Comp. Immunol. 2013;40:1–10. doi: 10.1016/j.dci.2012.10.013. PubMed DOI

Dey S., Pathak D.C., Ramamurthy N., Maity H.K., Chellappa M.M. Infectious bursal disease virus in chickens: Prevalence, impact, and management strategies. Vet. Med. Res. Rep. 2019;10:85. doi: 10.2147/VMRR.S185159. PubMed DOI PMC

Elankumaran S., Heckert R.A., Moura L. Pathogenesis and tissue distribution of a variant strain of infectious bursal disease virus in commercial broiler chickens. Avian Dis. 2002;46:169–176. doi: 10.1637/0005-2086(2002)046[0169:PATDOA]2.0.CO;2. PubMed DOI

Kabell S., Handberg K.J., Kusk M., Bisgaard M. Detection of infectious bursal disease virus in various lymphoid tissues of experimentally infected specific pathogen free chickens by different reverse transcription polymerase chain reaction assays. Avian Dis. 2005;49:534–539. doi: 10.1637/7370-042905R.1. PubMed DOI

Kim I.J., You S.K., Kim H., Yeh H.Y., Sharma J.M. Characteristics of bursal T lymphocytes induced by infectious bursal disease virus. J. Virol. 2000;74:8884–8892. doi: 10.1128/JVI.74.19.8884-8892.2000. PubMed DOI PMC

Rautenschlein S., Yeh H.Y., Njenga M.K., Sharma J.M. Role of intrabursal T cells in infectious bursal disease virus (IBDV) infection: T cells promote viral clearance but delay follicular recovery. Arch. Virol. 2002;147:285–304. doi: 10.1007/s705-002-8320-2. PubMed DOI

Ruby T., Whittaker C., Withers D.R., Chelbi-Alix M.K., Morin V., Oudin A., Young J.R., Zoorob R. Transcriptional profiling reveals a possible role for the timing of the inflammatory response in determining susceptibility to a viral infection. J. Virol. 2006;80:9207–9216. doi: 10.1128/JVI.00929-06. PubMed DOI PMC

Eldaghayes I., Rothwell L., Williams A., Withers D., Balu S., Davison F., Kaiser P. Infectious bursal disease virus: Strains that differ in virulence differentially modulate the innate immune response to infection in the chicken bursa. Viral Immunol. 2006;19:83–91. doi: 10.1089/vim.2006.19.83. PubMed DOI

Liu H., Zhang M., Han H., Yuan J., Li Z. Comparison of the expression of cytokine genes in the bursal tissues of the chickens following challenge with infectious bursal disease viruses of varying virulence. Virol. J. 2010;7:1–9. doi: 10.1186/1743-422X-7-364. PubMed DOI PMC

Heo Y.T., Lee S.H., Yang J.H., Kim T., Lee H.T. Bone marrow cell-mediated production of transgenic chickens. Lab. Investig. 2011:1229–1240. doi: 10.1038/labinvest.2011.53. PubMed DOI PMC

Rath N.C., Huff G.R., Huff W.E., Balog J.M. Factors regulating bone maturity and strength in poultry. Poult. Sci. 2000;79:1024–1032. doi: 10.1093/ps/79.7.1024. PubMed DOI

Yahyaei B., Gilanpour H., Veshkini A. Study of the ossification centers and skeletal development of pelvic limb in quail after hatching. Adv. Environ. Biol. 2013:2074–2081.

Iqbal M., Zhang H., Mehmood K., Li A., Jiang X., Wang Y., Zhang J., Iqbal M.K., Rehman M.U., Yao W., et al. Icariin: A potential compound for the recovery of Tibial Dyschondroplasia affected chicken via up-regulating BMP-2 expression. Biol. Proced. 2018;20:1–7. doi: 10.1186/s12575-018-0080-y. PubMed DOI PMC

Fleming R.H., McCormack H.A., McTeir L., Whitehead C.C. Incidence, pathology and prevention of keel bone deformities in the laying hen. Brit. Poult. Sci. 2004;45:320–330. doi: 10.1080/00071660410001730815. PubMed DOI

Rodenburg T.B., Tuyttens F.A.M., De Reu K., Herman L., Zoons J., Sonck B. Welfare assessment of laying hens in furnished cages and non-cage systems: An on-farm comparison. Anim. Welf. 2008;17:363–373.

Käppeli S., Gebhardt-Henrich S.G., Fröhlich E., Pfulg A., Stoffel M.H. Prevalence of keel bone deformities in Swiss laying hens. Br. Poult. Sci. 2011;52:531–536. doi: 10.1080/00071668.2011.615059. PubMed DOI

Wilkins L.J., McKinstry J.L., Avery N.C., Knowles T.G., Brown S.N., Tarlton J., Nicol C.J. Influence of housing system and design on bone strength and keel bone fractures in laying hens. Vet. Rec. 2011;169:414. doi: 10.1136/vr.d4831. PubMed DOI

Petrik M.T., Guerin M.T., Widowski T.M. On-farm comparison of keel fracture prevalence and other welfare indicators in conventional cage and floor-housed laying hens in Ontario, Canada. Poult. Sci. 2015;94:579–585. doi: 10.3382/ps/pev039. PubMed DOI

Toscano M.J., Dunn I.C., Christensen J.P., Petow S., Kittelsen K., Ulrich R. Explanations for keel bone fractures in laying hens: Are there explanations in addition to elevated egg production? Poult. Sci. 2020;99:4183–4194. doi: 10.1016/j.psj.2020.05.035. PubMed DOI PMC

Chen F.P., Lee N., Wang K.C., Soong Y.K., Huang K.E. Effect of estrogen and 1α, 25 (OH) 2-vitamin D3 on the activity and growth of human primary osteoblast-like cells in vitro. Fertil. Steril. 2002;77:1038–1043. doi: 10.1016/S0015-0282(02)03065-0. PubMed DOI

Jørgensen N.R., Henriksen Z., Sørensen O.H., Civitelli R. Dexamethasone, BMP-2, and 1, 25-dihydroxyvitamin D enhance a more differentiated osteoblast phenotype: Validation of an in vitro model for human bone marrow-derived primary osteoblasts. Steroids. 2004;69:219–226. doi: 10.1016/j.steroids.2003.12.005. PubMed DOI

Li X., Liu H., Niu X., Yu B., Fan Y., Feng Q., Cui F., Watari F. The use of carbon nanotubes to induce osteogenic differentiation of human adipose-derived MSCs in vitro and ectopic bone formation in vivo. Biomaterials. 2012;33:4818–4827. doi: 10.1016/j.biomaterials.2012.03.045. PubMed DOI

Tourkova I.L., Liu L., Sutjarit N., Larrouture Q.C., Luo J., Robinson L.J., Blair H.C. Adrenocorticotropic hormone and 1, 25-dihydroxyvitamin D 3 enhance human osteogenesis in vitro by synergistically accelerating the expression of bone-specific genes. Lab. Investig. 2017;97:1072–1083. doi: 10.1038/labinvest.2017.62. PubMed DOI PMC

Harrison J.R., Petersen D.N., Lichtler A.C., Mador A.T., Rowe D.W., Kream B.E. 1, 25-Dihydroxyvitamin D3 inhibits transcription of type I collagen genes in the rat osteosarcoma cell line ROS 17/2.8. Endocrinology. 1989;125:327–333. doi: 10.1210/endo-125-1-327. PubMed DOI

Kim H.T., Chen T.L. 1, 25-Dihydroxyvitamin D3 interaction with dexamethasone and retinoic acid: Effects on procollagen messenger ribonucleic acid levels in rat osteoblast-like cells. Mol. Endocrinol. 1989;3:97–104. doi: 10.1210/mend-3-1-97. PubMed DOI

Van Driel M., Van Leeuwen J.P. Vitamin D endocrine system and osteoblasts. Bonekey Rep. 2014;3:493. doi: 10.1038/bonekey.2013.227. PubMed DOI PMC

Chen J., Dosier C.R., Park J.H., De S., Guldberg R.E., Boyan B.D., Schwartz Z. Mineralization of three--dimensional osteoblast cultures is enhanced by the interaction of 1α, 25--dihydroxyvitamin D3 and BMP2 via two specific vitamin D receptors. J. Tissue. Eng. Regen. Med. 2016;10:40–51. doi: 10.1002/term.1770. PubMed DOI

Kim J.H., Seong S., Kim K., Kim I., Jeong B.C., Kim N. Downregulation of Runx2 by 1, 25-dihydroxyvitamin D3 induces the transdifferentiation of osteoblasts to adipocytes. Int. J. Mol. Sci. 2016;17:770. doi: 10.3390/ijms17050770. PubMed DOI PMC

Xiong Y., Zhang Y., Xin N., Yuan Y., Zhang Q., Gong P., Wu Y. 1α, 25-Dihydroxyvitamin D3 promotes osteogenesis by promoting Wnt signaling pathway. J. Steroid. Biochem. Mol. Biol. 2017;174:153–160. doi: 10.1016/j.jsbmb.2017.08.014. PubMed DOI

Broess M., Riva A., Gerstenfeld L.C. Inhibitory effects of 1, 25 (OH) 2 vitamin D3 on collagen type I, osteopontin, and osteocalcin gene expression in chicken osteoblasts. J. Cell. Bibiochem. 1995;57:440–451. doi: 10.1002/jcb.240570310. PubMed DOI

Pande V.V., Chousalkar K.C., Bhanugopan M.S., Quinn J.C. Super pharmacological levels of calcitriol (1, 25-(OH) 2 D3) inhibits mineral deposition and decreases cell proliferation in a strain dependent manner in chicken mesenchymal stem cells undergoing osteogenic differentiation in vitro. Poult. Sci. 2015;94:2784–2796. doi: 10.3382/ps/pev284. PubMed DOI PMC

Gil A., Plaza-Diaz J., Mesa M.D. Vitamin D: Classic and novel actions. Ann. Nutr. Metab. 2018;72:87–95. doi: 10.1159/000486536. PubMed DOI

Milford A.B., Le Mouël C., Bodirsky B.L., Rolinski S. Drivers of meat consumption. Appetite. 2019;141:104313. doi: 10.1016/j.appet.2019.06.005. PubMed DOI

Basu S. The transitional dynamics of caloric ecosystems: Changes in the food supply around the world. Crit. Public Health. 2015;25:248–264. doi: 10.1080/09581596.2014.931568. PubMed DOI PMC

Al-Khalaifa H., Al-Nasser A., Al-Surayee T., Al-Kandari S., Al-Enzi N., Al-Sharrah T., Ragheb G., Al-Qalaf S., Mohammed A. Effect of dietary probiotics and prebiotics on the performance of broiler chickens. Poult. Sci. 2019;98:4465–4479. doi: 10.3382/ps/pez282. PubMed DOI

Sohail M.U., Hume M.E., Byrd J.A., Nisbet D.J., Ijaz A., Sohail A., Shabbir M.Z., Rehman H. Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poult. Sci. 2012;91:2235–2240. doi: 10.3382/ps.2012-02182. PubMed DOI

Alavi S.A.N., Zakeri A., Kamrani B., Pourakbari Y. Effect of prebiotics, probiotics, acidfire, growth promoter antibiotics and synbiotic on humural immunity of broiler chickens. Global Vet. 2012;8:612–617.

Maiorano G., Stadnicka K., Tavaniello S., Abiuso C., Bogucka J., Bednarczyk M. In ovo validation model to assess the efficacy of commercial prebiotics on broiler performance and oxidative stability of meat. Poult. Sci. 2017;96:511–518. doi: 10.3382/ps/pew311. PubMed DOI

Carrade D.D., Borjesson D.L. Immunomodulation by mesenchymal stem cells in veterinary species. Com. Med. 2013;63:207–217. PubMed PMC

Lotfinegad P. Immunomodulatory nature and site specific affinity of mesenchymal stem cells: A hope in cell therapy. Adv. Pharm. Bull. 2014;4:5. doi: 10.5681/apb.2014.002. PubMed DOI PMC

Zimmermann K., Haas A., Oxenius A. Systemic antibody responses to gut microbes in health and disease. Gut Microbes. 2012;3:42–47. doi: 10.4161/gmic.19344. PubMed DOI

Li G., Lillehoj H.S., Lee K.W., Jang S.I., Marc P., Gay C.G., Ritter G.D., Bautista D.A., Phillips K., Neumann A.P., et al. An outbreak of gangrenous dermatitis in commercial broiler chickens. Avian Path. 2010;39:247–253. doi: 10.1080/03079457.2010.487517. PubMed DOI

McDevitt R.M., Brooker J.D., Acamovic T., Sparks N.H.C. Necrotic enteritis; a continuing challenge for the poultry industry. World’s Poul. Sci. J. 2006;62:221–247. doi: 10.1079/WPS200593. DOI

Mataragas M., Skandamis P.N., Drosinos E.H. Risk profiles of pork and poultry meat and risk ratings of various pathogen/product combinations. Int. J. Food Microbiol. 2008;126:1–12. doi: 10.1016/j.ijfoodmicro.2008.05.014. PubMed DOI

Cooper K.K., Songer J.G. Necrotic enteritis in chickens: A paradigm of enteric infection by Clostridium perfringens type A. Anaerobe. 2009;15:55–60. doi: 10.1016/j.anaerobe.2009.01.006. PubMed DOI

Van Immerseel F., Rood J.I., Moore R.J., Titball R.W. Rethinking our understanding of the pathogenesis of necrotic enteritis in chickens. Trends Microbiol. 2009;17:32–36. doi: 10.1016/j.tim.2008.09.005. PubMed DOI

Gornatti-Churria C.D., Crispo M., Shivaprasad H.L., Uzal F.A. Gangrenous dermatitis in chickens and turkeys. J. Vet. Diag. Investig. 2018;30:188–196. doi: 10.1177/1040638717742435. PubMed DOI PMC

Shivaprasad H.L. Clostridial Diseases of Animals. Wiley-Blackwell; Ames, IA, USA: 2016. Gangrenous dermatitis in poultry; pp. 255–264.

Dinev I., Denev S., Vashin I., Kanakov D., Rusenova N. Pathomorphological investigations on the prevalence of contact dermatitis lesions in broiler chickens. J. Appl. Anim. Res. 2019;47:129–134. doi: 10.1080/09712119.2019.1584105. DOI

Li G., Lillehoj H.S., Lee K.W., Lee S.H., Park M.S., Jang S.I., Bauchan G.R., Gay C.G., Ritter G.D., Bautista D.A., et al. Immunopathology and cytokine responses in commercial broiler chickens with gangrenous dermatitis. Avian Pathol. 2010;39:255–264. doi: 10.1080/03079457.2010.495382. PubMed DOI

Golchin A., Farahany T.Z., Khojasteh A., Soleimanifar F., Ardeshirylajimi A. The clinical trials of mesenchymal stem cell therapy in skin diseases: An update and concise review. Curr. Stem Cell Res. Ther. 2019;14:22–33. doi: 10.2174/1574888X13666180913123424. PubMed DOI

Steinfeld H., Gerber P., Wassenaar T.D., Castel V., Rosales M., Rosales M., de Haan C. Livestock’s Long Shadow: Environmental Issues and Options. Food Agriculture Organization; Rome, Italy: 2006.

Hoekstra A.Y., Chapagain A.K. Integrated Assessment of Water Resources and Global Change. Springer; Dordrecht, The Netherlands: 2006. Water footprints of nations: Water use by people as a function of their consumption pattern; pp. 35–48.

Fiala N. Meeting the demand: An estimation of potential future greenhouse gas emissions from meat production. Ecol. Econom. 2008;67:412–419. doi: 10.1016/j.ecolecon.2007.12.021. DOI

Sutton T.C. The pandemic threat of emerging H5 and H7 avian influenza viruses. Viruses. 2018;10:461. doi: 10.3390/v10090461. PubMed DOI PMC

Park S.E. Epidemiology, virology, and clinical features of severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2; Coronavirus Disease-19) Clin. Exp. Pediatr. 2020;63:119. doi: 10.3345/cep.2020.00493. PubMed DOI PMC

Stanton M.M., Tzatzalos E., Donne M., Kolundzic N., Helgason I., Ilic D. Prospects for the use of induced pluripotent stem cells in animal conservation and environmental protection. Stem Cells Transl. Med. 2019;8:7–13. doi: 10.1002/sctm.18-0047. PubMed DOI PMC

Datar I., Betti M. Possibilities for an in vitro meat production system. Innov. Food. Sci. Emerg. Technol. 2010;11:13–22. doi: 10.1016/j.ifset.2009.10.007. DOI

Arshad M.S., Javed M., Sohaib M., Saeed F., Imran A., Amjad Z. Tissue engineering approaches to develop cultured meat from cells: A mini review. Cogent Food Agric. 2017;3:1320814. doi: 10.1080/23311932.2017.1320814. DOI

Bhat Z.F., Kumar S., Fayaz H. In Vitro meat production: Challenges and benefits over conventional meat production. J. Integr. Agric. 2015;14:241–248. doi: 10.1016/S2095-3119(14)60887-X. DOI

Will K., Schering L., Albrecht E., Kalbe C., Maak S. Differentiation of bovine satellite cell-derived myoblasts under different culture conditions. In Vitro. Cell. Dev. Biol. Animal. 2015;51:885–889. doi: 10.1007/s11626-015-9916-9. PubMed DOI

Ostrovidov S., Ahadian S., Ramon--Azcon J., Hosseini V., Fujie T., Parthiban S.P., Khademhosseini A. Three–dimensional co--culture of C2C12/PC12 cells improves skeletal muscle tissue formation and function. J. Tissue Eng. Regen. Med. 2017;11:582–595. doi: 10.1002/term.1956. PubMed DOI

Mehta F., Theunissen R., Post M.J. Myogenesis. Humana Press; New York, NY, USA: 2019. Adipogenesis from bovine precursors; pp. 111–125. PubMed DOI

Cremonesi F., Corradetti B., Consiglio A.L. Fetal adnexa derived stem cells from domestic animal: Progress and perspectives. Theriogenology. 2001;75:1400–1415. doi: 10.1016/j.theriogenology.2010.12.032. PubMed DOI

Wang Y., Han Z.B., Song Y.P., Han Z.C. Safety of mesenchymal stem cells for clinical application. Stem Cells Int. 2012:652034. doi: 10.1155/2012/652034. PubMed DOI PMC

Bai C., Li C., Jin D., Guo Y., Guan W., Ma Y., Zhao Q. Establishment and characterization of a fibroblast line from landrace. Artif. Cell Blood Sub. 2010;38:129–135. doi: 10.3109/10731191003670525. PubMed DOI

Na R.S., Zhao Q.J., Su X.H., Chen X.W., Guan W.J., Ma Y.H. Establishment and biological characteristics of Ujumqin sheep fibroblast line. Cytotechnology. 2010;62:43–52. doi: 10.1007/s10616-010-9260-6. PubMed DOI PMC