Cryopreservation of chicken primordial germ cells by vitrification and slow-freezing: a comparative study

chicken primordial germ cells; cryopreservation; slow freezing; aseptic vitrification; genetic resources preservation; male and female germplasm; cellules germinales primordiales; poulet; cryopréservation; Congélation lente; vitrification aseptique; préservation des ressources génétiques

Abstract :

[en] In the present study, we compare a classical slow freezing method and an aseptic vitrification technique to cryopreserve a stable Primordial Gem Cells (PGCs) line issued from the Ardennaise chicken breed. Viability immediately after warming was close to 80% and did not differ between the two cryopreservation methods. Proliferation tended to be slower for both cryopreservation methods compared to controls, but the difference was significant only for vitrification. No difference was found between the two methods after flow cytometry analysis of SSEA-1 expression and RT-PCR on several factors related to PGCs phenotype. After one week in culture, all cryopreserved cells reached controls main morphological and expanding (viability/proliferation) features. However, slow freezing generated more unwanted cells clusters than vitrification. After injection of the PGCs into recipient embryos, vitrified PGCs showed a clear, yet not significant, tendency to colonize the gonad at a higher rate than slow frozen PGCs. Slow freezing in cryovials remains simple, inexpensive and less technically demanding than vitrification. Nevertheless, the intrinsic advantages of our aseptic vitrification method and the present study suggest that this should be considered as safer than classical slow freezing for cryopreserving chicken PGCs.

Research Center/Unit :

FARAH - Fundamental and Applied Research for Animals and Health - ULiège

Disciplines :

Anatomy (cytology, histology, embryology...) & physiology
Veterinary medicine & animal health
Biotechnology

Author, co-author :

Tonus, Céline ^✱; Université de Liège > Département de morphologie et pathologie (DMP) > Embryologie

Connan, Delphine ^✱; Université de Liège > Département de morphologie et pathologie (DMP) > Embryologie

Waroux, Olivier ^✱; Université de Liège > Département de morphologie et pathologie (DMP) > Département de morphologie et pathologie (DMP)

Vandenhove, Benoit ; Université de Liège - ULiège > Département de morphologie et pathologie (DMP) > Embryologie

Wayet, Jérome ; Université de Liège - ULiège > Département de morphologie et pathologie (DMP) > Embryologie

Gillet, Laurent ; Université de Liège > Département des maladies infectieuses et parasitaires (DMI) > Vaccinologie vétérinaire

Desmecht, Daniel ; Université de Liège > Département de morphologie et pathologie (DMP) > Pathologie spéciale et autopsies

Antoine, Nadine ; Université de Liège > Département de morphologie et pathologie (DMP) > Histologie

Ectors, Fabien ; Université de Liège > GIGA-Technology platforms : Plate-forme transgénique

Grobet, Luc ; Université de Liège > Département de morphologie et pathologie (DMP) > Embryologie

^✱ These authors have contributed equally to this work.

Language :

English

Title :

Cryopreservation of chicken primordial germ cells by vitrification and slow-freezing: a comparative study

Publication date :

15 January 2017

Journal title :

Theriogenology

ISSN :

0093-691X

eISSN :

1879-3231

Publisher :

Elsevier, New York, United States - New York

Volume :

Pages :

197-206

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Région wallonne : DGO6

Available on ORBi :

since 22 September 2016

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Bibliography

[1] Blesbois, E., Seigneurin, F., Grasseau, I., Limouzin, C., Besnard, J., Gourichon, D., et al. Semen cryopreservation for ex situ management of genetic diversity in chicken: creation of the French avian cryobank. Poult Sci 86 (2007), 555–564.
[2] Santiago-Moreno, J., Castano, C., Toledano-Diaz, A., Coloma, M.A., Lopez-Sebastian, A., Prieto, M.T., et al. Semen cryopreservation for the creation of a Spanish poultry breeds cryobank: optimization of freezing rate and equilibration time. Poult Sci 90 (2011), 2047–2053.
[3] Saint Jalme, M., Lecoq, R., Seigneurin, F., Blesbois, E., Plouzeau, E., Cryopreservation of semen from endangered pheasants: the first step towards a cryobank for endangered avian species. Theriogenology 59 (2003), 875–888.
[4] Long, J.A., Bongalhardo, D.C., Pelaez, J., Saxena, S., Settar, P., O'Sullivan, N.P., et al. Rooster semen cryopreservation: effect of pedigree line and male age on postthaw sperm function. Poult Sci 89 (2010), 966–973.
[5] Blesbois, E., Grasseau, I., Seigneurin, F., Mignon-Grasteau, S., Saint Jalme, M., Mialon-Richard, M.M., Predictors of success of semen cryopreservation in chickens. Theriogenology 69 (2008), 252–261.
[6] Liu, J., Song, Y., Cheng, K.M., Silversides, F.G., Production of donor-derived offspring from cryopreserved ovarian tissue in Japanese quail (Coturnix japonica). Biol Reprod 83 (2010), 15–19.
[7] Song, Y., Silversides, F.G., Long-term production of donor-derived offspring from chicken ovarian transplants. Poult Sci 87 (2008), 1818–1822.
[8] Silversides, F.G., Robertson, M.C., Liu, J., Cryoconservation of avian gonads in Canada. Poult Sci 92 (2013), 2613–2617.
[9] van de Lavoir, M.-C., Diamond, J.H., Leighton, P.A., Mather-Love, C., Heyer, B.S., Bradshaw, R., et al. Germline transmission of genetically modified primordial germ cells. Nature 441 (2006), 766–769.
[10] Tonus, C., Cloquette, K., Ectors, F., Piret, J., Gillet, L., Antoine, N., et al. Long term-cultured and cryopreserved primordial germ cells from various chicken breeds retain high proliferative potential and gonadal colonisation competency. Reprod Fertil Dev 28 (2016), 628–639.
[11] Nandi, S., Whyte, J., Taylor, L., Sherman, A., Nair, V., Kaiser, P., et al. Cryopreservation of specialized chicken lines using cultured primordial germ cells. Poult Sci 95 (2016), 1905–1911.
[12] Nakamura, Y., Poultry genetic resource conservation using primordial germ cells. J Reprod Dev, 2016, 10.1262/jrd.2016-052.
[13] Nakamura, Y., Yamamoto, Y., Usui, F., Mushika, T., Ono, T., Setioko, A.R., et al. Migration and proliferation of primordial germ cells in the early chicken embryo. Poult Sci 86 (2007), 2182–2193.
[14] Hamburger, V., Hamilton, H.L., A series of normal stages in the development of the chick embryo. J Morphol 88 (1951), 49–92.
[15] Naito, M., Tajima, A., Tagami, T., Yasuda, Y., Kuwana, T., Preservation of chick primordial germ cells in liquid nitrogen and subsequent production of viable offspring. J Reprod Fertil 102 (1994), 321–325.
[16] Moore, D.T., Purdy, P.H., Blackburn, H.D., A method for cryopreserving chicken primordial germ cells. Poult Sci 85 (2006), 1784–1790.
[17] Setioko, A.R., Tagami, T., Tase, H., Nakamura, Y., Takeda, K., Nirasawa, K., Cryopreservation of primordial germ cells (PGCs) from White Leghorn embryos using commercial cryoprotectants. J Poult Sci 44 (2007), 73–77.
[18] Nakamura, Y., Usui, F., Miyahara, D., Mori, T., Watanabe, H., Ono, T., et al. Viability and functionality of primordial germ cells after freeze-thaw in chickens. J Poult Sci 48 (2011), 57–63.
[19] Nakamura, Y., Tasai, M., Takeda, K., Nirasawa, K., Tagami, T., Production of functional gametes from cryopreserved primordial germ cells of the Japanese quail. J Reprod Dev 59 (2013), 580–587.
[20] Kohara, Y., Kanai, Y., Tajima, A., Cryopreservation of gonadal germ cells (GGCs) from the domestic chicken using vitrification. J Poult Sci 45 (2008), 57–61.
[21] Tajima, A., Naito, M., Yasuda, Y., Kuwana, T., Production of germ-line chimeras by transfer of cryopreserved gonadal primordial germ cells (gPGCs) in chicken. J Exp Zool 280 (1998), 265–267.
[22] Smith, G.D., Serafini, P.C., Fioravanti, J., Yadid, I., Coslovsky, M., Hassun, P., et al. Prospective randomized comparison of human oocyte cryopreservation with slow-rate freezing or vitrification. Fertil Steril 94 (2010), 2088–2095.
[23] Rienzi, L., Cobo, A., Paffoni, A., Scarduelli, C., Capalbo, A., Vajta, G., et al. Consistent and predictable delivery rates after oocyte vitrification: an observational longitudinal cohort multicentric study. Hum Reprod 27 (2012), 1606–1612.
[24] Vanderzwalmen, P., Ectors, F., Grobet, L., Prapas, Y., Panagiotidis, Y., Vanderzwalmen, S., et al. Aseptic vitrification of blastocysts from infertile patients, egg donors and after IVM. Reprod Biomed Online 19 (2009), 700–707.
[25] Li, L., Zhang, X., Zhao, L., Xia, X., Wang, W., Comparison of DNA apoptosis in mouse and human blastocysts after vitrification and slow freezing. Mol Reprod Dev 79 (2012), 229–236.
[26] Vanderzwalmen, P., Zech, N.H., Ectors, F., Stecher, A., Lejeune, B., Vanderzwalmen, S., et al. Blastocyst transfer after aseptic vitrification of zygotes: an approach to overcome an impaired uterine environment. Reprod Biomed Online 25 (2012), 591–599.
[27] Reubinoff, B.E., Pera, M.F., Vajta, G., Trounson, A.O., Effective cryopreservation of human embryonic stem cells by the open pulled straw vitrification method. Hum Reprod 16 (2001), 2187–2194.
[28] Li, T., Mai, Q., Gao, J., Zhou, C., Cryopreservation of human embryonic stem cells with a new bulk vitrification method. Biol Reprod 82 (2010), 848–853.
[29] Li, Y., Tan, J.C., Li, L.S., Comparison of three methods for cryopreservation of human embryonic stem cells. Fertil Steril 93 (2010), 999–1005.
[30] Nakao, K., Nakagata, N., Katsuki, M., Simple and efficient vitrification procedure for cryopreservation of mouse embryos. Exp Anim 46 (1997), 231–234.
[31] Kim, S.W., Ko, Y.-G., Byun, M., Do, Y.J., Han, J.Y., Kim, D.H., et al. Comparison of vitrification and slow freezing for the cryopreservation of chicken primordial germ cell (Ogye). J Anim Sci Technol 55 (2013), 417–425.
[32] Sawicka, D., Chojnacka-Puchta, L., Brzezinska, J., Lakota, P., Bednarczyk, M., Cryoconservation of chicken blastodermal cells: effects of slow freezing, vitrification, cryoprotectant type and thawing method during in vitro processing. Folia Biol 63 (2015), 129–134.
[33] Isachenko, V., Montag, M., Isachenko, E., Zaeva, V., Krivokharchenko, I., Shafei, R., et al. Aseptic technology of vitrification of human pronuclear oocytes using open-pulled straws. Hum Reprod 20 (2005), 492–496.
[34] Choi, J.W., Kim, S., Kim, T.M., Kim, Y.M., Seo, H.W., Park, T.S., et al. Basic fibroblast growth factor activates MEK/ERK cell signaling pathway and stimulates the proliferation of chicken primordial germ cells. PLoS One, 5, 2010, e12968.
[35] Wang, Y., Hou, L., Li, C., Guan, W., Chen, L., Li, X., et al. Isolation, culture and biological characteristics of primordial germ cells from Beijing fatty chicken. J Reprod Dev 56 (2010), 303–308.
[36] Lavial, F., Acloque, H., Bachelard, E., Nieto, M.A., Samarut, J., Pain, B., Ectopic expression of Cvh (Chicken Vasa homologue) mediates the reprogramming of chicken embryonic stem cells to a germ cell fate. Dev Biol 330 (2009), 73–82.
[37] Swanberg, S.E., Payne, W.S., Hunt, H.D., Dodgson, J.B., Delany, M.E., Telomerase activity and differential expression of telomerase genes and c-myc in chicken cells in vitro. Dev Dyn 231 (2004), 14–21.
[38] Motono, M., Ohashi, T., Nishijima, K., Iijima, S., Analysis of chicken primordial germ cells. Cytotechnology 57 (2008), 199–205.
[39] Vanderzwalmen, P., Connan, D., Grobet, L., Wirleitner, B., Remy, B., Vanderzwalmen, S., et al. Lower intracellular concentration of cryoprotectants after vitrification than after slow freezing despite exposure to higher concentration of cryoprotectant solutions. Hum Reprod 28 (2013), 2101–2110.
[40] Seki, S., Mazur, P., The dominance of warming rate over cooling rate in the survival of mouse oocytes subjected to a vitrification procedure. Cryobiology 59 (2009), 75–82.
[41] Sawicka, D., Chojnacka-Puchta, L., Zielinski, M., Plucienniczak, G., Plucienniczak, A., Bednarczyk, M., Flow cytometric analysis of apoptosis in cryoconserved chicken primordial germ cells. Cell Mol Biol Lett 20 (2015), 143–159.
[42] Heng, B.C., Ye, C.P., Liu, H., Toh, W.S., Rufaihah, A.J., Yang, Z., et al. Loss of viability during freeze-thaw of intact and adherent human embryonic stem cells with conventional slow-cooling protocols is predominantly due to apoptosis rather than cellular necrosis. J Biomed Sci 13 (2006), 433–445.
[43] Naaldijk, Y., Staude, M., Fedorova, V., Stolzing, A., Effect of different freezing rates during cryopreservation of rat mesenchymal stem cells using combinations of hydroxyethyl starch and dimethylsulfoxide. BMC Biotechnol, 12, 2012, 49.
[44] Song, Y., Duraisamy, S., Ali, J., Kizhakkayil, J., Jacob, V.D., Mohammed, M.A., et al. Characteristics of long-term cultures of avian primordial germ cells and gonocytes. Biol Reprod, 90, 2014, 15.
[45] Riesco, M.F., Robles, V., Cryopreservation causes genetic and epigenetic changes in zebrafish genital ridges. PLoS One, 8, 2013, e67614.
[46] Aramaki, S., Kubota, K., Soh, T., Yamauchi, N., Hattori, M., Chicken dead end homologue protein is a nucleoprotein of germ cells including primordial germ cells. J Reprod Dev 55 (2009), 214–218.
[47] Aramaki, S., Sato, F., Kato, T., Soh, T., Kato, Y., Hattori, M., Molecular cloning and expression of dead end homologue in chicken primordial germ cells. Cell Tissue Res 330 (2007), 45–52.
[48] Kedde, M., Strasser, M.J., Boldajipour, B., Oude Vrielink, J.A., Slanchev, K., le Sage, C., et al. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131 (2007), 1273–1286.
[49] Zhu, R., Iacovino, M., Mahen, E., Kyba, M., Matin, A., Transcripts that associate with the RNA binding protein, DEAD-END (DND1), in embryonic stem (ES) cells. BMC Mol Biol, 12, 2011, 37.
[50] Yang, C.X., Wright, E.C., Ross, J.W., Expression of RNA-binding proteins DND1 and FXR1 in the porcine ovary, and during oocyte maturation and early embryo development. Mol Reprod Dev 79 (2012), 541–552.
[51] Wirleitner, B., Vanderzwalmen, P., Bach, M., Baramsai, B., Neyer, A., Schwerda, D., et al. The time aspect in storing vitrified blastocysts: its impact on survival rate, implantation potential and babies born. Hum Reprod 28 (2013), 2950–2957.
[52] Sanchez-Osorio, J., Cuello, C., Gil, M.A., Parrilla, I., Alminana, C., Caballero, I., et al. In vitro postwarming viability of vitrified porcine embryos: effect of cryostorage length. Theriogenology 74 (2010), 486–490.