A simple method for effective cryopreservation of antlerogenic periosteum of sika deer.
antlerogenic periosteum
cell proliferation
cell viability
cryopreservation
xenogeneic antler
Journal
Journal of experimental zoology. Part A, Ecological and integrative physiology
ISSN: 2471-5646
Titre abrégé: J Exp Zool A Ecol Integr Physiol
Pays: United States
ID NLM: 101710204
Informations de publication
Date de publication:
12 2023
12 2023
Historique:
revised:
13
08
2023
received:
11
06
2023
accepted:
16
08
2023
medline:
6
11
2023
pubmed:
28
8
2023
entrez:
28
8
2023
Statut:
ppublish
Résumé
Antlerogenic periosteum (AP) is the unique tissue type that gives rise to antlers and their antecedents, the pedicles. Deer antlers are the only mammalian organ that can fully regenerate. Efficient investigation of the mechanism of antler formation and regeneration requires year-round availability of AP, but naturally AP can only be obtained less than two months in a year. In the present study we took the cryopreservation approach to store the sampled AP in ultra-low temperature to overcome the limited period of availability. First, we evaluated the suitability of vitrification and cell cryopreservation method for cryopreservation of AP, cell migration status of the AP tissue pieces confirmed that vitrification methods did not work as the only few AP cells migrated out, whereas migrated cell numbers in the cell-cryo group (conventional method for cryopreservation of cells) were comparable to those of the fresh AP group. To further evaluate the suitability of cell cryopreservation method for AP tissue, AP samples were allocated into three groups based on the different ratios of cryopreservation reagents (dimethyl sulfoxide [DMSO], dulbecco's modified eagle's medium [DMEM] and fetal bovine serum [FBS]): AP-Cell-1 (1:4:5), AP-Cell-2 (1:2:7) and AP-Cell-3 (1:0:9), the results showed that migrated cell number were again comparable to the fresh AP group. There was no significant difference between the cell-cryo groups (AP-Cell-1 and AP-Cell-3) and the fresh group: (1) in viability (p > 0.05) through trypan blue staining (91.2%, 90.8%, and 92.4%, respectively); (2) in the attachment day, and all on Day 5 after cell seeding; (3) in cell proliferation rate (p > 0.05) through Cell Counting kit 8 (CCK8) measurement; and (4) in number of the formed clones (Clonogenicity). In the in vivo trials, there was no visible difference in temporal differentiation sequence of the formed xenogeneic antlers between the fresh AP and cryopreserved AP (AP-Cell-1 and AP-Cell-3). Overall, we found that the AP tissue was well cryopreserved just using the conventional freezing and thawing methods for cells, and their viability and developmental potential comparable to the fresh AP both in vitro and in vivo. The long-term preservation of the AP tissue is of great significance for the study of the periosteum biology in general and the mechanism underlying xenogeneic generation and regeneration of deer antlers in specific.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1017-1025Subventions
Organisme : Wellcome Trust
ID : 202306
Pays : United Kingdom
Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Bubenik, G., & Bubenik, A. H. (1990). Horns, Pronghorns, and Antlers. Evolution, Morphology, Physiology, and Social Significance. George A. Bubenik and Anthony B. Bubenik, Eds. Springer-Verlag, New York, 1990. xii, 562 pp., illus. $89. Science, 250(4986), 1458.
Gao, Z., Yang, F., McMahon, C., & Li, C. (2012). Mapping the morphogenetic potential of antler fields through deleting and transplanting subregions of antlerogenic periosteum in sika deer (Cervus nippon): Morphogenetic potential of antler field. Journal of Anatomy, 220(2), 131-143.
Goss, R. J. (1983). Deer antlers. Regeneration, function and evolution. Academic Press.
Goss, R. J., & Powel, R. S. (1985). Induction of deer antlers by transplanted periosteum. I. Graft size and shape. Journal of Experimental Zoology, 235(3), 359-373.
Hartwig, H., & Schrudde, J. (1974). Experimentelle untersuchungen zur bildung der primären stirnauswüchse beim reh (Capreolus capreolus L.). Zeitschrift für Jagdwissenschaft, 20, 1-13.
Kierdorf, H., Kierdorf, U., Szuwart, T., Gath, U., & Clemen, G. (1994). Light microscopic observations on the ossification process in the early developing pedicle of fallow deer (Dama dama). Annals of Anatomy - Anatomischer Anzeiger, 176(3), 243-249.
Kierdorf, U., Li, C., & Price, J. S. (2009). Improbable appendages: Deer antler renewal as a unique case of mammalian regeneration. Seminars in Cell & Developmental Biology, 20(5), 535-542.
Kierdorf, U., Stoffels, E., Stoffels, D., Kierdorf, H., Szuwart, T., & Clemen, G. (2003). Histological studies of bone formation during pedicle restoration and early antler regeneration in roe deer and fallow deer. The Anatomical Record, 273(2), 741-751.
Kreder, H. J., Keeley, F. W., & Salter, R. (1993). Cryopreservation of periosteum for transplantation. Cryobiology, 30(2), 107-115.
Leonel, E. C. R., Corral, A., Risco, R., Camboni, A., Taboga, S. R., Kilbride, P., Vazquez, M., Morris, J., Dolmans, M. M., & Amorim, C. A. (2019). Stepped vitrification technique for human ovarian tissue cryopreservation. Scientific Reports, 9(1), 20008.
Li, C. (2013). Histogenetic aspects of deer antler development. Frontiers in Bioscience, 5(2), 479-489.
Li, C. (2017). Custom-built tools for the study of deer antler biology. Frontiers in Bioscience, 22, 1622-1633.
Li, C., Gao, X., Yang, F., Martin, S. K., Haines, S. R., Deng, X., Schofield, J., & Stanton, J. A. L. (2009). Development of a nude mouse model for the study of antlerogenesis--mechanism of tissue interactions and ossification pathway. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 312(2), 118-135.
Li, C., Harris, A. J., & Suttie, J. M. (1988). Autoradiographic localization of androgen-binding in the antlerogenic periosteum of red deer (Cervus elaphus). In J. A. Milne (Ed.), Recent development in biology of deer Scotland: Edinburgh.
Li, C., Harris, A. J., & Suttie, J. M. (2001). Tissue interactions and antlerogenesis: New findings revealed by a xenograft approach. Journal of Experimental Zoology, 290(1), 18-30.
Li, C., Littlejohn, R. P., Corson, I. D., & Suttie, J. M. (2003). Effects of testosterone on pedicle formation and its transformation to antler in castrated Male, freemartin and normal female red deer (Cervus elaphus). General and Comparative Endocrinology, 131(1), 21-31.
Li, C., Littlejohn, R. P., & Suttie, J. M. (1999). Effects of insulin-like growth factor 1 and testosterone on the proliferation of antlerogenic cells in vitro. Journal of Experimental Zoology, 284(1), 82-90.
Li, C., & Suttie, J. M. (1994). Light microscopic studies of pedicle and early first antler development in red deer (Cervus elaphus). The Anatomical Record, 239(2), 198-215.
Li, C., & Suttie, J. M. (2001). Deer antlerogenic periosteum: A piece of postnatally retained embryonic tissue? Anatomy and Embryology, 204(5), 375-388.
Li, C., & Suttie, J. M. (2003). Tissue collection methods for antler research. European Journal of Morphology, 41(1), 23-30.
Li, C., Suttie, J. M., & Clark, D. E. (2005). Histological examination of antler regeneration in red deer (Cervus elaphus), Anat Rec A Discov Mol Cell Evol Biol, 282(2), 163-174.
Li, C., Yang, F., Haines, S., Zhao, H., Wang, W., Xing, X., Sun, H., Chu, W., Lu, X., Liu, L., & McMahon, C. (2010). Stem cells responsible for deer antler regeneration are unable to recapitulate the process of first antler development-revealed through intradermal and subcutaneous tissue transplantation. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 314(7), 552-570.
Li, C., Yang, F., & Sheppard, A. (2009). Adult stem cells and mammalian epimorphic regeneration-insights from studying annual renewal of deer antlers. Current stem cell research & therapy, 4(3), 237-251.
Li, C., Yang, F., Xing, X., Gao, X., Deng, X., Mackintosh, C., & Suttie, J. M. (2008). Role of heterotypic tissue interactions in deer pedicle and first antler formation-revealed via a membrane insertion approach. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 310(3), 267-277.
Li, C., Zhao, H., Liu, Z., & McMahon, C. (2014). Deer antler-a novel model for studying organ regeneration in mammals. The International Journal of Biochemistry & Cell Biology, 56, 111-122.
Mase, J., Mizuno, H., Okada, K., Sakai, K., Mizuno, D., Usami, K., Kagami, H., & Ueda, M. (2006). Cryopreservation of cultured periosteum: Effect of different cryoprotectants and pre-incubation protocols on cell viability and osteogenic potential. Cryobiology, 52(2), 182-192.
Qin, Y. (2018). Research on vitrification cryopreservation of rabbit ovarian. tissueJournal of Reproductive Medicine, 10(27), 994-999.
Shen, H. P., Ding, C. M., Chi, Z. Y., Kang, Z. Z., & Tan, W. S. (2003). [Effects of different cooling rates on cryopreservation of hematopoietic stem cells from cord blood]. Sheng wu gong cheng xue bao = Chinese journal of biotechnology, 19(19), 489-492.
Shi, Q., Xie, Y., Wang, Y., & Li, S. (2017). Vitrification versus slow freezing for human ovarian tissue cryopreservation: A systematic review and meta-anlaysis. Scientific Reports, 7(1), 8538.
Sun, H., Sui, Z., Wang, D., Ba, H., Zhao, H., Zhang, L., & Li, C. (2020). Identification of interactive molecules between antler stem cells and dermal papilla cells using an in vitro co-culture system. Journal of Molecular Histology, 51(1), 15-31.
Wang, D., Wang, X., Ba, H., Ren, J., Wang, Z., & Sun, H. (2022). Chimeric blood vessels sustained development of the xenogeneic antler: A unique model for xenogeneic organ generation.