Novel approach for biomaterial assessment: utilizing the Ex Ovo quail cam assay for biocompatibility pre-screening

. 2024 Nov 21 ; 49 (1) : 24. [epub] 20241121

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39570443
Odkazy

PubMed 39570443
PubMed Central PMC11582168
DOI 10.1007/s11259-024-10574-y
PII: 10.1007/s11259-024-10574-y
Knihovny.cz E-zdroje

In recent years, the chorioallantoic membrane (CAM) has emerged as a crucial component of biocompatibility testing for biomaterials designed for regenerative strategies and tissue engineering applications. This study explores angiogenic potential of an innovative acellular and porous biopolymer scaffold, based on polyhydroxybutyrate and chitosan (PHB/CHIT), using the ex ovo quail CAM assay as an alternative to the conventional chick CAM test. On embryonic day 6 (ED6), we placed the tested biomaterials on the CAM alone or soaked them with various substances, including vascular endothelial growth factor (VEGF-A), saline, or the endogenous angiogenesis inhibitor Angiostatin. After 72 h (ED9), we analyzed blood vessels formation, a sign of ongoing angiogenesis, in the vicinity of the scaffold and within its pores. We employed marker for cell proliferation (PHH3), embryonic endothelium (WGA, SNA), myofibroblasts (α-SMA), and endothelial cells (QH1) for morphological and histochemical analysis. Our findings demonstrated the robust angiogenic potential of the untreated scaffold without additional influence from the angiogenic factor VEGF-A. Furthermore, gene expression analysis revealed an upregulation of pro-angiogenic growth factors, including VEGF-A, ANG-2, and VE-Cadherin after 5 days of implantation, indicative of a pro-angiogenic microenvironment. These results underscore the inherent angiogenic potential of the PHB/CHIT composite. Additionally, monitoring of CAM microvilli growing to the scaffold provides a methodology for investigating the biocompatibility of materials using the ex ovo quail CAM assay as a suitable alternative model compared to the chicken CAM platform. This approach offers a rapid screening method for biomaterials in the field of tissue repair/regeneration and engineering.

Zobrazit více v PubMed

Abhinand CS, Raju R, Soumya SJ et al (2016) VEGF-A/VEGFR2 signaling network in endothelial cells relevant to angiogenesis. J Cell Commun Signal 10:347–354. 10.1007/s12079-016-0352-8 PubMed PMC

Ainsworth SJ, Stanley RL, Evans DJR (2010) Developmental stages of the Japanese quail. J Anat 216:3–15. 10.1111/j.1469-7580.2009.01173.x PubMed PMC

Akwii RG, Sajib MS, Zahra FT et al (2019) Role of Angiopoietin-2 in vascular physiology and pathophysiology. 10.3390/cells8050471. Cells 8 PubMed PMC

Aleem AR, Shahzadi L, Tehseen S et al (2019) Amino acids loaded chitosan/collagen based new membranes stimulate angiogenesis in chorioallantoic membrane assay. Int J Biol Macromol 140:401–406. 10.1016/j.ijbiomac.2019.08.095 PubMed

Bai J, Pang Y, Zhang X et al (2016) Study on the Morphological Development of Quail Embryos. Rev Bras Cienc Avic 18:91–93. 10.1590/1806-9061-2015-0177

Cattalini JP, Roether J, Hoppe A et al (2016) Nanocomposite scaffolds with tunable mechanical and degradation capabilities: co-delivery of bioactive agents for bone tissue engineering. Biomed Mater 11:065003. 10.1088/1748-6041/11/6/065003 PubMed

Colman H, Giannini C, Huang L et al (2006) Assessment and Prognostic significance of Mitotic Index using the mitosis marker phospho-histone H3 in low and intermediate-grade infiltrating Astrocytomas. Am J Surg Pathol 30:657–664. 10.1097/01.pas.0000202048.28203.25 PubMed

Dejana E, Bazzoni G, Lampugnani MG (1999) Vascular endothelial (VE)-Cadherin: only an intercellular glue? Exp Cell Res 252:13–19. 10.1006/excr.1999.4601 PubMed

Demcisakova Z, Luptakova L, Tirpakova Z et al (2022) Evaluation of Angiogenesis in an Acellular Porous Biomaterial based on Polyhydroxybutyrate and Chitosan using the Chicken Ex Ovo Chorioallantoic membrane model. Cancers (Basel) 14:4194. 10.3390/cancers14174194 PubMed PMC

Doyle C, Tanner ET, Bonfield W (1991) In vitro and in vivo evaluation of polyhydroxybutyrate and of polyhydroxybutyrate reinforced with hydroxyapatite. Biomaterials 12:841–847. 10.1016/0142-9612(91)90072-I PubMed

Dünker N, Jendrossek V (2019) Implementation of the Chick Chorioallantoic membrane (CAM) model in Radiation Biology and Experimental Radiation Oncology Research. Cancers (Basel) 11:1499. 10.3390/cancers11101499 PubMed PMC

Duong CN, Vestweber D (2020) Mechanisms ensuring endothelial junction integrity beyond VE-Cadherin. Front Physiol 11. 10.3389/fphys.2020.00519. PubMed PMC

Dvořánková B, Lacina L, Smetana K (2018) Isolation of normal fibroblasts and their Cancer-Associated counterparts (CAFs) for Biomedical Research. In: Turksen K (ed) Skin stem cells. Methods in Molecular Biology. Humana, New York, pp 393–406. 10.1007/7651_2018_137 PubMed

Ellermann E, Meyer N, Cameron RE et al (2023) In vitro angiogenesis in response to biomaterial properties for bone tissue engineering: a review of the state of the art. Regen Biomater 10. 10.1093/rb/rbad027 PubMed PMC

Ezdakova MI, Matveeva DK, Andreeva ER (2022) Short-term interaction with endothelial cells enhances angiogenic activity of growth-arrested mesenchymal stromal cells in vitro and in Ovo. Bull Exp Biol Med 174:125–130. 10.1007/s10517-022-05660-7 PubMed

Felcht M, Luck R, Schering A et al (2012) Angiopoietin-2 differentially regulates angiogenesis through TIE2 and integrin signaling. J Clin Invest 122:1991–2005. 10.1172/JCI58832 PubMed PMC

Félétou M (2011) The endothelium, part I: multiple functions of the endothelial cells -- Focus on Endothelium-Derived Vasoactive mediators. Colloquium Ser Integr Syst Physiology: Molecule Function 3:1–306. 10.4199/C00031ED1V01Y201105ISP019

Gentile LB, Piva B, Diaz BL (2011) Hypertonic stress induces VEGF production in human Colon Cancer Cell Line Caco-2: inhibitory role of Autocrine PGE2. PLoS ONE 6:e25193. 10.1371/journal.pone.0025193 PubMed PMC

Giretova M, Medvecky L, Stulajterova R et al (2016) Effect of enzymatic degradation of chitosan in polyhydroxybutyrate/chitosan/calcium phosphate composites on in vitro osteoblast response. J Mater Sci Mater Med 27:181. 10.1007/s10856-016-5801-7 PubMed

Giretova M, Medvecky L, Petrovova E et al (2019) Polyhydroxybutyrate/Chitosan 3D scaffolds promote in Vitro and in Vivo Chondrogenesis. Appl Biochem Biotechnol 189:556–575. 10.1007/s12010-019-03021-1 PubMed

Guillén-Carvajal K, Valdez-Salas B, Beltrán-Partida E et al (2023) Chitosan, gelatin, and Collagen Hydrogels for bone regeneration. Polym (Basel) 15:2762. 10.3390/polym15132762 PubMed PMC

Hessenauer MET, Lauber K, Zuchtriegel G et al (2018) Vitronectin promotes the vascularization of porous polyethylene biomaterials. Acta Biomater 82:24–33. 10.1016/j.actbio.2018.10.004 PubMed

Karageorgiou V, Kaplan D (2005) Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 26:5474–5491. 10.1016/j.biomaterials.2005.02.002 PubMed

Klueh U, Dorsky DI, Moussy F et al (2003) Ex Ova chick chorioallantoic membrane as a novel model for evaluation of tissue responses to biomaterials and implants. J Biomed Mater Res A 67A:838–843. 10.1002/jbm.a.10059 PubMed

Kundeková B, Máčajová M, Meta M et al (2021) Chorioallantoic membrane models of various avian species: differences and applications. Biology (Basel) 10:301. 10.3390/biology10040301 PubMed PMC

Lazarovici P, Gazit A, Staniszewska I et al (2006) Nerve growth factor (NGF) promotes angiogenesis in the Quail Chorioallantoic membrane. Endothelium 13:51–59. 10.1080/10623320600669053 PubMed

Lee HJ, Hong YJ, Kim M (2021) Angiogenesis in chronic inflammatory skin disorders. Int J Mol Sci 22:12035. 10.3390/ijms222112035 PubMed PMC

Liu M, Xie S, Zhou J (2018) Use of animal models for the imaging and quantification of angiogenesis. Exp Anim 67:1–6. 10.1538/expanim.17-0054 PubMed PMC

Lobov IB, Brooks PC, Lang RA (2002) Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Nat Acad Sci 99:11205–11210 PubMed PMC

Macajova M, Cavarga I, Sykorova M et al (2020) Modulation of angiogenesis by topical application of leptin and high and low molecular heparin using the Japanese quail chorioallantoic membrane model. Saudi J Biol Sci 27:1488–1493. 10.1016/j.sjbs.2020.04.013 PubMed PMC

Máčajová M, Huntošová V, Meta M et al (2022) Quail Chorioallantoic membrane - A Tool for photodynamic diagnosis and therapy. J Visualized Experiments. 10.3791/63422 PubMed

Mahapatra C, Kumar P, Paul MK et al (2022) Angiogenic stimulation strategies in bone tissue regeneration. Tissue Cell 79:101908. 10.1016/j.tice.2022.101908 PubMed

Maksimov VF, Korostyshevskaya IM, Kurganov SA (2006) Functional morphology of chorioallantoic vascular network in chicken. Bull Exp Biol Med 142:367–371. 10.1007/s10517-006-0368-9 PubMed

Mangir N, Dikici S, Claeyssens F et al (2019) Using ex Ovo Chick Chorioallantoic membrane (CAM) assay to evaluate the biocompatibility and angiogenic response to Biomaterials. ACS Biomater Sci Eng 5:3190–3200. 10.1021/acsbiomaterials.9b00172 PubMed

Marew T, Birhanu G (2021) Three dimensional printed nanostructure biomaterials for bone tissue engineering. Regen Ther 18:102–111. 10.1016/j.reth.2021.05.001 PubMed PMC

Medvecky L, Giretova M, Stulajterova R (2014) Properties and in vitro characterization of polyhydroxybutyrate–chitosan scaffolds prepared by modified precipitation method. J Mater Sci Mater Med 25:777–789. 10.1007/s10856-013-5105-0 PubMed

Nan W, He Y, Wang S et al (2023) Molecular mechanism of VE-cadherin in regulating endothelial cell behaviour during angiogenesis. Front Physiol 14:1234104. 10.3389/fphys.2023.1234104 PubMed PMC

Naňka O, Peumans WJ, Van Damme EJM et al (2001) Lectin histochemistry of microvascular endothelium in chick and quail musculature. Anat Embryol (Berl) 204:407–411. 10.1007/s004290100212 PubMed

Neuhaus W, Reininger-Gutmann B, Rinner B et al (2022) The current status and work of three rs centres and platforms in Europe*. Altern Lab Anim 50:381–413. 10.1177/02611929221140909 PubMed

Papoutsi M, Tomarev SI, Eichmann A et al (2001) Endogenous origin of the lymphatics in the avian chorioallantoic membrane. Dev Dyn 222:238–251. 10.1002/dvdy.1187 PubMed

Pardanaud L, Altmann C, Kitos P et al (1987) Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100:339–349. 10.1242/dev.100.2.339 PubMed

Parsons-Wingerter P, Lwai B, Yang MC et al (1998) A Novel assay of Angiogenesis in the Quail Chorioallantoic membrane: stimulation by bFGF and inhibition by Angiostatin according to Fractal Dimension and Grid Intersection. Microvasc Res 55:201–214. 10.1006/mvre.1998.2073 PubMed

Petrovova E, Giretova M, Kvasilova A et al (2019) Preclinical alternative model for analysis of porous scaffold biocompatibility in bone tissue engineering. Altex 36:121–130. 10.14573/altex.1807241 PubMed

Petrovova E, Tomco M, Holovska K et al (2021) PHB/CHIT Scaffold as a Promising Biopolymer in the treatment of Osteochondral Defects—An experimental animal study. Polym (Basel) 13:1232. 10.3390/polym13081232 PubMed PMC

Ribatti D (2016) The chick embryo chorioallantoic membrane (CAM). A multifaceted experimental model. Mech Dev 141:70–77. 10.1016/j.mod.2016.05.003 PubMed

Ribatti D (2017) The chick embryo chorioallantoic membrane (CAM) assay. Reprod Toxicol 70:97–101. 10.1016/j.reprotox.2016.11.004 PubMed

Ribatti D, Nico B, Vacca A et al (2006) The gelatin sponge–chorioallantoic membrane assay. Nat Protoc 1:85–91. 10.1038/nprot.2006.13 PubMed

Ribatti D, Annese T, Tamma R (2020) The use of the chick embryo CAM assay in the study of angiogenic activiy of biomaterials. Microvasc Res 131:104026. 10.1016/j.mvr.2020.104026 PubMed

Schneider-Stock R, Flügen G (2023) Editorial for special issue: the Chorioallantoic membrane (CAM) model—traditional and state-of-the art applications: the 1st International CAM Conference. Cancers (Basel) 15:772. 10.3390/cancers15030772 PubMed PMC

Scholz A, Plate KH, Reiss Y (2015) Angiopoietin-2: a multifaceted cytokine that functions in both angiogenesis and inflammation. Ann N Y Acad Sci 1347:45–51. 10.1111/nyas.12726 PubMed

Sun Z, Li X, Massena S et al (2012) VEGFR2 induces c-Src signaling and vascular permeability in vivo via the adaptor protein TSAd. J Exp Med 209:1363–1377. 10.1084/jem.20111343 PubMed PMC

Tetzlaff MT, Curry JL, Ivan D et al (2013) Immunodetection of phosphohistone H3 as a surrogate of mitotic figure count and clinical outcome in cutaneous melanoma. Mod Pathol 26:1153–1160. 10.1038/modpathol.2013.59 PubMed

Vargas GE, Haro Durand LA, Cadena V et al (2013) Effect of nano-sized bioactive glass particles on the angiogenic properties of collagen based composites. J Mater Sci Mater Med 24:1261–1269. 10.1007/s10856-013-4892-7 PubMed

Wallez Y, Vilgrain I, Huber P (2006) Angiogenesis: the VE-Cadherin switch. Trends Cardiovasc Med 16:55–59. 10.1016/j.tcm.2005.11.008 PubMed

Wang X, Bove AM, Simone G et al (2020) Molecular bases of VEGFR-2-Mediated physiological function and pathological role. Front Cell Dev Biol 8. 10.3389/fcell.2020.599281 PubMed PMC

Woloszyk A, Mitsiadis TA (2017) Angiogenesis within stem cell–Seeded Silk scaffolds cultured on the Chorioallantoic membrane and visualized by 3D imaging. Curr Protoc Stem Cell Biol 41. 10.1002/cpsc.27 PubMed

Zhu P, Zhang C-B, Yang P et al (2016) Phosphohistone H3 (pHH3) is a prognostic and epithelial to mesenchymal transition marker in diffuse gliomas. Oncotarget 7:45005–45014. 10.18632/oncotarget.7154 PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...