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Cytolytic assessment of hyperacute rejection and production of nuclear transfer embryos using hCD46-transgenic porcine embryonic germ cells

Published online by Cambridge University Press:  01 May 2009

Ji Young Won ,
Kwang Sung Ahn ,
Alice M. Sorrell ,
Susa Shin ,
Soon Young Heo ,
Jee Hyun Kang ,
Jin-Ki Park ,
Won-Kyong Chang  and
Hosup Shim
Ji Young Won
Affiliation:
Department of Physiology, Dankook University School of Medicine, Cheonan, Korea.
Kwang Sung Ahn
Affiliation:
Department of Physiology, Dankook University School of Medicine, Cheonan, Korea.
Alice M. Sorrell
Affiliation:
Department of Physiology, Dankook University School of Medicine, Cheonan, Korea. Metabolic Research Laboratories, Institute of Metabolic Science, University of Cambridge, Addenbrooke's Treatment Centre, Addenbrooke's Hospital, Hills Road, Cambridge, CB2 0QQ, UK.
Susa Shin
Affiliation:
Department of Physiology, Dankook University School of Medicine, Cheonan, Korea.
Soon Young Heo
Affiliation:
Department of Physiology, Dankook University School of Medicine, Cheonan, Korea.
Jee Hyun Kang
Affiliation:
Department of Physiology, Dankook University School of Medicine, Cheonan, Korea.
Jin-Ki Park
Affiliation:
Animal Biotechnology Division, National Institute of Animal Science, Suwon, Korea.
Won-Kyong Chang
Affiliation:
Animal Biotechnology Division, National Institute of Animal Science, Suwon, Korea.
Hosup Shim*
Affiliation:
Department of Physiology, Dankook University School of Medicine, San 29 Anseo-dong, Cheonan, Chungnam 330–714, South Korea. Department of Physiology, Dankook University School of Medicine, Cheonan, Korea.
*
All correspondence to: Hosup Shim. Department of Physiology, Dankook University School of Medicine, San 29 Anseo-dong, Cheonan, Chungnam 330–714, South Korea. Tel: +82 41 550 3865. Fax: +82 41 565 6167. e-mail: [email protected]
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Summary

Human complement regulatory protein hCD46 may reduce the hyperacute rejection (HAR) in pig-to-human xenotransplantation. In this study, an hCD46 gene was introduced into porcine embryonic germ (EG) cells. Treatment of human serum did not affect the survival of hCD46-transgenic EG cells, whereas the treatment significantly reduced the survival of non-transgenic EG cells (p < 0.01). The transgenic EG cells presumably capable of alleviating HAR were transferred into enucleated oocytes. Among 235 reconstituted oocytes, 35 (14.9%) developed to the blastocyst stage. Analysis of individual embryos indicated that 80.0% (28/35) of embryos contained the transgene hCD46. The result of the present study demonstrates resistance of hCD46-transgenic EG cells against HAR, and the usefulness of the transgenic approach may be predicted by this cytolytic assessment prior to actual production of transgenic pigs. Subsequently performed EG cell nuclear transfer gave rise to hCD46-transgenic embryos. Further study on the transfer of these embryos to recipients may produce hCD46-transgenic pigs.

Keywords

Embryonic germ cellhCD46Hyperacute rejectionNuclear transferTransgenic
Type
Research Article
Information
Zygote , Volume 17 , Issue 2 , May 2009 , pp. 101 - 108
Copyright
Copyright © Cambridge University Press 2008

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References

Ahn, K.S., Won, J.Y., Heo, S.Y., Kang, J.H., Yang, H.S. & Shim, H. (2007). Transgenesis and nuclear transfer using porcine embryonic germ cells. Cloning Stem Cells 9, 461–8.CrossRefGoogle ScholarPubMed
Bach, F.H. (1998). Xenotransplantation: problems and prospects. Annu. Rev. Med. 49, 301–10.CrossRefGoogle Scholar
Chen, R.H., Naficy, S., Logan, J.S., Diamond, L.E. & Adams, D.H. (1999). Hearts from transgenic pigs constructed with CD59/DAF genomic clones demonstrate improved survival in primates. Xenotransplantation 6, 194–200.CrossRefGoogle ScholarPubMed
Cozzi, E., Bosio, E., Seveso, M., Vadori, M. & Ancona, E. (2006). Xenotransplantation-current status and future perspectives. Br. Med. Bull. 75–76, 99–114.Google ScholarPubMed
Dai, Y., Vaught, T.D., Boone, J., Chen, S.H., Phelps, C.J., Ball, S., Monahan, J.A., Jobst, P.M., McCreath, K.J., Lamborn, A.E., Cowell-Lucero, J.L., Wells, K.D., Colman, A., Polejaeva, I.A. & Ayares, D.L. (2002). Targeted disruption of the alpha1,3-galactosyltransferase gene in cloned pigs. Nat. Biotechnol. 20, 251–5.CrossRefGoogle ScholarPubMed
Faast, R., Harrison, S.J., Beebe, L.F., McIlfatrick, S.M., Ashman, R.J. & Nottle, M.B. (2006). Use of adult mesenchymal stem cells isolated from bone marrow and blood for somatic cell nuclear transfer in pigs. Cloning Stem Cells 8, 166–73.CrossRefGoogle ScholarPubMed
Fujimura, T., Kurome, M., Murakami, H., Takahagi, Y., Matsunami, K., Shimanuki, S., Suzuki, K., Miyagawa, S., Shirakura, R., Shigehisa, T. & Nagashima, H. (2004). Cloning of the transgenic pigs expressing human decay accelerating factor and N-acetylglucosaminyl transferase III. Cloning Stem Cells 6, 294–301.CrossRefGoogle Scholar
Galli, C., Duchi, R., Moor, R.M. & Lazzari, G. (1999). Mammalian leukocytes contain all the genetic information necessary for the development of a new individual. Cloning 1, 161–70.CrossRefGoogle ScholarPubMed
Gibbons, J., Arat, S., Rzucidlo, J., Miyoshi, K., Waltenburg, R., Respess, D., Venable, A. & Stice, S. (2002). Enhanced survivability of cloned calves derived from roscovitine-treated adult somatic cells. Biol. Reprod. 66, 895–900.CrossRefGoogle ScholarPubMed
Gordon, J.W., Scangos, G.A., Plotkin, D.J., Barbosa, J.A. & Ruddle, F.H. (1980). Genetic transformation of mouse embryos by microinjection of purified DNA. Proc. Natl. Acad. Sci. USA 77, 7380–4.CrossRefGoogle ScholarPubMed
Harrison, S., Boquest, A., Grupen, C., Faast, R., Guildolin, A., Giannakis, C., Crocker, L., McIlfatrick, S., Ashman, R., Wengle, J., Lyons, I., Tolstoshev, P., Cowan, P., Robins, A., O'Connell, P., D'Apice, A.J. & Nottle, M. (2004). An efficient method for producing alpha(1,3)-galactosyltransferase gene knockout pigs. Cloning Stem Cells 6, 327–31.CrossRefGoogle ScholarPubMed
Hill, J.R., Winger, Q.A., Long, C.R., Looney, C.R., Thompson, J.A. & Westhusin, M.E. (2000). Development rates of male bovine nuclear transfer embryos derived from adult and fetal cells. Biol. Reprod. 62, 1135–40.CrossRefGoogle ScholarPubMed
Hochedlinger, K. & Jaenisch, R. (2002). Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 415, 1035–8.CrossRefGoogle ScholarPubMed
Huang, J., Gou, D., Zhen, C., Jiang, D., Mao, X., Li, W., Chen, S. & Cai, C. (2001). Protection of xenogeneic cells from human complement-mediated lysis by the expression of human DAF, CD59 and MCP. FEMS Immunol. Med. Microbiol. 31, 203–9.CrossRefGoogle ScholarPubMed
Kasinathan, P., Knott, J.G., Wang, Z., Jerry, D.J. & Robl, J.M. (2001). Production of calves from G1 fibroblasts. Nat. Biotechnol. 19, 1176–8.CrossRefGoogle ScholarPubMed
Kato, Y., Tani, T. & Tsunoda, Y. (2000). Cloning of calves from various somatic cell types of male and female adult, newborn and fetal cows. J. Reprod. Fertil. 120, 231–7.CrossRefGoogle ScholarPubMed
Khalpey, Z., Koch, C.A. & Platt, J.L. (2004). Xenograft transplantation. Anesthesiol. Clin. North America 22, 871–5.CrossRefGoogle ScholarPubMed
Labosky, P.A., Barlow, D.P. & Hogan, B.L.M. (1994). Mouse embryonic germ (EG) cell lines: transmission through the germline and differences in the methylation imprint of insulin-like growth factor w receptor (Igf2r) gene compared with embryonic stem (ES) cell lines. Development 120, 3197–204.CrossRefGoogle Scholar
Lai, L., Kolber-Simonds, D., Park, K.W., Cheong, H.T., Greenstein, J.L., Im, G.S., Samuel, M., Bonk, A., Rieke, A., Day, B.N., Murphy, C.N., Carter, D.B., Hawley, R.J. & Prather, R.S. (2002). Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science 295, 1089–92.CrossRefGoogle ScholarPubMed
Lee, J.H., Lee, H.J., Nahm, K.M., Jeon, H.Y., Hwang, W.S., Paik, N.W. & Rho, H.M. (2006). Effects of combined expression of human complement regulatory proteins and H-transferase on the inhibition of complement-mediated cytolysis in porcine embryonic fibroblasts. Transplant Proc. 38, 1618–21.CrossRefGoogle ScholarPubMed
Liszewski, M.K., Farries, T.C., Lublin, D.M., Rooney, I.A. & Atkinson, J.P. (1996). Control of the complement system. Adv. Immunol. 61, 201–83.Google ScholarPubMed
Macháty, Z., Bondioli, K.R., Ramsoondar, J.J. & Fodor, W.L. (2002). The use of nuclear transfer to produce transgenic pigs. Cloning Stem Cells 4, 21–7.CrossRefGoogle ScholarPubMed
Liu, L., Shin, T., Pryor, J.H., Kraemer, D. & Westhusin, M. (2001). Regenerated bovine fetal fibroblasts support high blastocyst development following nuclear transfer. Cloning 3, 51–8.CrossRefGoogle ScholarPubMed
Matsui, Y., Zsebo, K. & Hogan, B.L. (1992). Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70, 841–7.CrossRefGoogle ScholarPubMed
McCurry, K.R., Kooyman, D.L., Alvarado, C.G., Cotterell, A.H., Martin, M.J., Logan, J.S. & Platt, J.L. (1995). Human complement regulatory proteins protect swine-to-primate cardiac xenografts from humoral injury. Nat. Med. 1, 423–7.CrossRefGoogle ScholarPubMed
Mir, B., Tanner, N., Chowdhary, B.P. & Piedrahita, J.A. (2003). UP1 extends life of primary porcine fetal fibroblasts in culture. Cloning Stem Cells 5, 143–8.CrossRefGoogle ScholarPubMed
Miyashita, N., Shiga, K., Yonai, M., Kaneyama, K., Kobayashi, S., Kojima, T., Goto, Y., Kishi, M., Aso, H., Suzuki, T., Sakaguchi, M. & Nagai, T. (2002). Remarkable differences in telomere lengths among cloned cattle derived from different cell types. Biol. Reprod. 66, 1649–55.CrossRefGoogle ScholarPubMed
Niemann, H. (2001). Current status and perspectives for the generation of transgenic pigs for xenotransplantation. Ann. Transplant. 6, 6–9.Google ScholarPubMed
Nottle, M.B., Beebe, L.F., Harrison, S.J., McIlfatrick, S.M., Ashman, R.J., O'Connell, P.J., Salvaris, E.J., Fisicaro, N., Pommey, S., Cowan, P.J. & d'Apice, A.J. (2007). Production of homozygous alpha-1,3-galactosyltransferase knockout pigs by breeding and somatic cell nuclear transfer. Xenotransplantation 14, 339–44.CrossRefGoogle ScholarPubMed
Ogura, A., Inoue, K., Ogonuki, N., Noguchi, A., Takano, K., Nagano, R., Suzuki, O., Lee, J., Ishino, F. & Matsuda, J. (2000). Production of male cloned mice from fresh, cultured, and cryopreserved immature Sertoli cells. Biol. Reprod. 62, 1579–84.CrossRefGoogle ScholarPubMed
Piedrahita, J.A. & Mir, B. (2004). Cloning and transgenesis in mammals: implications for xenotransplantation. Am. J. Transplant. 4 (Suppl. 6), 43–50.CrossRefGoogle Scholar
Piedrahita, J.A., Moore, K., Oetama, B., Lee, C.K., Scales, N., Ramsoondar, J., Bazer, F.W. & Ott, T. (1998). Generation of transgenic porcine chimeras using primordial germ cell-derived colonies. Biol. Reprod. 58, 1321–9.CrossRefGoogle ScholarPubMed
Pino-Chavez, G. (2001). Differentiating acute humoral from acute cellular rejection histopathologically. Graft 4, 60–3.CrossRefGoogle Scholar
Ramsoondar, J.J., Macháty, Z., Costa, C., Williams, B.L., Fodor, W.L. & Bondioli, K.R. (2003). Production of alpha 1,3-galactosyltransferase-knockout cloned pigs expressing human alpha 1,2-fucosylosyltransferase. Biol. Reprod. 69, 437–45.CrossRefGoogle Scholar
Resnick, J.L., Bixter, L.S., Cheng, L. & Donovan, P.J. (1992). Long-term proliferation of mouse primordial germ cells in culture. Nature 359, 550–1.CrossRefGoogle ScholarPubMed
Rideout, W.M. 3rd, Wakayama, T., Wutz, A., Eggan, K., Jackson-Grusby, L., Dausman, J., Yanagimachi, R. & Jaenisch, R. (2000). Generation of mice from wild type and targeted ES cells by nuclear cloning. Nat. Genet. 24, 109–10.CrossRefGoogle ScholarPubMed
Rui, R., Qiu, Y., Hu, Y. & Fan, B. (2006). Establishment of porcine transgenic embryonic germ cell lines expressing enhanced green fluorescent protein. Theriogenology 65, 713–20.CrossRefGoogle ScholarPubMed
Schuurman, H.J., Pino-Chavez, G., Phillips, M.J., Thomas, L., White, D.J. & Cozzi, E. (2002). Incidence of hyperacute rejection in pig-to-primate transplantation using organs from hDAF-transgenic donors. Transplantation 73, 1146–51.CrossRefGoogle ScholarPubMed
Shim, H., Gutierrez-Adan, A., Chen, L.R., BonDurant, R.H., Behboodi, E. & Anderson, G.B. (1997). Isolation of pluripotent stem cells from cultured porcine primordial germ cells. Biol. Reprod. 57, 1089–95.CrossRefGoogle ScholarPubMed
Takahagi, Y., Fujimura, T., Miyagawa, S., Nagashima, H., Shigehisa, T., Shirakura, R. & Murakami, H. (2005). Production of alpha 1,3-galactosyltransferase gene knockout pigs expressing both human decay-accelerating factor and N-acetylglucosaminyltransferase III. Mol. Reprod. Dev. 71, 331–8.CrossRefGoogle ScholarPubMed
Takeuchi, Y., Magre, S. & Patience, C. (2005). The potential hazards of xenotransplantation: an overview. Rev. Sci. Tech. 24, 323–34.CrossRefGoogle ScholarPubMed
Tian, X.C., Xu, J. & Yang, X. (2000). Normal telomere lengths found in cloned cattle. Nat. Genet. 26, 272–3.CrossRefGoogle ScholarPubMed
Van Den Bogaerde, J. & White, D. J. (1997). Xenogeneic transplantation. Br. Med. Bull. 53, 904–20.CrossRefGoogle ScholarPubMed
Wakayama, T., Rodriguez, I., Perry, A.C.F., Yanagimachi, R. & Mombaerts, P. (1999). Mice cloned from embryonic stem cells. Proc. Natl. Acad. Sci. USA 96, 14984–9.CrossRefGoogle ScholarPubMed
Wells, D.N., Laible, G., Tucker, F.C., Miller, A.L., Oliver, J.E., Xiang, T., Forsyth, J.T., Berg, M.C., Cockrem, K., L'Huillier, P.J., Tervit, H.R. & Oback, B. (2003). Coordination between donor cell type and cell cycle stage improves nuclear cloning efficiency in cattle. Theriogenology 59, 45–59.CrossRefGoogle ScholarPubMed
Yang, Y.G. & Sykes, M. (2007). Xenotransplantation: current status and a perspective on the future. Nat. Rev. Immunol. 7, 519–31.CrossRefGoogle Scholar
Zakhartchenko, V., Alberio, R., Stojkovic, M., Prelle, K., Schernthaner, W., Stojkovic, P., Wenigerkind, H., Wanke, R., Duchler, M., Steinborn, R., Mueller, M. & Brem, G.E. (1999). Adult cloning in cattle: potential of nuclei from a permanent cell line and from primary cultures. Mol. Reprod. Dev. 54, 264–72.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed