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Archives of Andrology
Journal of Reproductive Systems
Volume 53, 2007 - Issue 4
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REVIEW ARTICLE

In vivo Gene Transfer into Testis and Sperm: Developments and Future Application

, &
Pages 187-197 | Received 02 Feb 2007, Accepted 03 Mar 2007, Published online: 09 Jul 2009

REFERENCES

  • Ambasudhan, R., Singh, K., Agarwal, J. K., Singh, S. K., Khanna, A., Sah, R. K., Singh, I., and Raman, R. (2003) Idiopathic cases of male infertility from a region in India show low incidence of Y-chromosome microdeletion. J Biosci 28:605–612.
  • Arezzo, F. (1989) Sea Urchin sperm as a vector of foreign genetic information. Cell Biol Int Rep 13:391–404.
  • Bachiller, D., Schellander, K., Peli, J., and Ruther, U. (1991) Liposome-mediated DNA uptake by sperm cells. Mol Reprod Dev 30:194–200.
  • Birnstiel, M. L. and Busslinger, M. (1989) Dangerous liaisons: Spermatozoa as natural vectors for foreign DNA? Cell 57:701–702.
  • Blanchard, K. T. and Boekelheide, K. (1997) Adenovirus-mediated gene transfer to rat testis in vivo. Biol Reprod 56:495–500.
  • Bondioli, K. R., Biery, K. A., Hill, K. G., Jones, K. B., and DeMayo, F. J. (1991) Production of transgenic cattle by pronuclear injection. Biotechnology 16:265–273.
  • Brackett, B. G., Baranska, W., Sawicki, W., and Koprowski, H. (1971) Uptake of heterologous genome by mammalian spermatozoa and its transfer to ova through fertilization. Proc Natl Acad Sci USA 68:353–357.
  • Brinster, R. L., Sandgren, E. P., Behringer, R. R., and Palmiter, R. D. (1989) No simple solution for making transgenic mice. Cell 59:239–241.
  • Camaioni, A., Russo, M. A., Odorisio, T., Gandolfi, F., Fazio, V. M., and Siracusa, G. (1992) Uptake of exogenous DNA by mammalian spermatozoa: Specific localization of DNA on sperm heads. J Reprod Fertil 961:203–212.
  • Capecchi, M. R. (1989) Altering the genome by homologous recombination. Science 244:1288–1292.
  • Celebi, C., Auvray, P., Benvegnu, T., Plusquellec, D., Jegou, B., and Guillaudeux, T. (2002) Transient transmission of a transgene in mouse offspring following in vivo transfection of male germ cells. Mol Reprod Dev 62:477–482.
  • Celebi, C., Guillaudeux, T., Auvray, P., Vallet-Erdtmann, V., and Jegou, B. (2003) The making of “transgenic spermatozoa”. Biol Reprod 68:1477–1483.
  • Chan, A. W., Luetjens, C. M., Dominko, T., Ramalho-Santos, J., Simerly, C. R., Hewitson, L., and Schatten, G. (2000) Foreign DNA transmission by ICSI: Injection of spermatozoa bound with exogenous DNA results in embryonic GFP expression and live rhesus monkey births. Mol Hum Reprod 6:26–33.
  • Chang, K. T., Ikeda, A., Hayashi, K., Furuhata, Y., Nishihara, M., Ohta, A., Ogawa, S., and Takahashi, M. (1999a) Production of transgenic rats and mice by the testis-mediated gene transfer. J Reprod Dev 45:29–36.
  • Chang, K. T., Ikeda, A., Hayashi, K., Furuhata, Y., Banai, M., Nishihara, M., Ohta, A., Ogawa, S., and Takahashi, M. (1999b) Possible mechanisms for the testis-mediated gene transfer as a new method for producing transgenic animals. J Reprod Dev 45:37–42.
  • Chen, T. M. and Chen, Y. H. (1996) Transgenic sperm or deadly missiles? Fertil Steril 66:167–169.
  • Coward, K., Kubota, H., Hibbit, O., McIlhinney, J., Kohri, K., and Parrington, J. (2006) Expression of a fluorescent recombinant form of sperm protein phospholipase C zeta in mouse epididymal sperm by in vivo gene transfer into the testis. Fertil Steril 85:1281–1289.
  • De Miguel, M. P. and Donovan, P. J. (2003) Determinants of retroviral-mediated gene delivery to mouse spermatogonia. Biol Reprod 68:860–866.
  • Ding, S., Wu, X., Li, G., Han, M., Zhuang, Y., and Xu, T. (2005) Efficient transposition of the piggyBac (PB) transposon in mammalian cells and mice. Cell 122:473–484.
  • Dobashi, M., Goda, K., Maruyama, H., and Fujisawa, M. (2005) Erythropoietin gene transfer into rat testes by in vivo electroporation may reduce the risk of germ cell loss caused by cryptorchidism. Asian J Androl 7:369–373.
  • Eiges, R. (2006) Genetic manipulation of human embryonic stem cells by transfection. Methods Mol Biol. 331:221–239.
  • Escalier, D. (2001) Impact of genetic engineering on the understanding of spermatogenesis. Hum Reprod Update 7:191–210.
  • Francolini, M., Lavitrano, M., Lamia, C. L., French, D., Frat, i L., Cotelli, F., and Spadafora, C. (1993) Evidence for nuclear internalization of exogenous DNA into mammalian sperm cells. Mol Reprod Dev 34:133–139.
  • Gagné, M. B., Pothier, F., and Sirard, M. A. (1991) Electroporation of bovine spermatozoa to carry foreign DNA in oocytes. Mol Reprod Dev 29:6–15.
  • Gordon, J. W., Scangos, G. A., Plotkin, D. J., Barbosa, J. A., and Ruddle, F. H. (1980) Genetic transformation of mouse embryos by microinjection of purified DNA. Proc Natl Acad Sci USA 77:7380–7384.
  • Hall, S. J., Bar-Charma, N., Ta, S., and Gordon, J. W. (2000). Direct exposure of mouse spermatogenic cells to high doses of adenovirus gene therapy vector does not result in germ cell transduction. Hum Gene Ther 11:1705–1712.
  • Hamaguchi, I., Woods, N. B., Panagopoulos, I., Andersson, E., Mikkola, H., Fahlman, C., Zufferey, R., Carlsson, L., Trono, D., and Karlsson, S. (2000) Lentivirus vector gene expression during ES cell-derived hematopoietic development in vitro. J Virol 74:10778–10784.
  • Hammer, R. E., Maika, S. D., Richardson, J. A., Tang, J. P., and Taurog, J. D. (1990) Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human beta 2 m: An animal model of HLA-B27-associated human disorders. Cell 63:1099–1112.
  • Hamra, F. K., Gatlin, J., Chapman, K. M., Grellhesl, D. M., Garcia, J. V., Hammer, R. E., and Garbers, D. L. (2002) Production of transgenic rats by lentiviral transduction of male germ-line stem cells. Proc Natl Acad Sci USA 99:14931–14936.
  • Hibbit, O., Coward, K., Kubota, H., Prathalingham, N., Holt, W., Kohri, K., and Parrington, J. (2006) In vivo gene transfer by electroporation allows expression of a fluorescent transgene in hamster testis and epididymal sperm and has no adverse effects upon testicular integrity or sperm quality. Biol Reprod 74:95–101.
  • Hitt, M., Bett, A., Addison, C., Prevec, L., and Graham, F. (1995) Techniques for human adenovirus vector construction and characterization. Methods Mol Genet 7:13–30.
  • Hogan, B., Beddington, R., Constantin, F., and Lacy, E. (1994) Manipulating the mouse embryo. New York: Cold Spring Harbor Laboratory.
  • Horan, R., Powell, R., Bird, J. M., Gannon, F., and Houghton, J. A. (1992) Effects of electropermeabilization on the association of foreign DNA with pig sperm. Arch Androl 28:105–114.
  • Huang, Z., Tamura, M., Sakurai, T., Chuma, S., Saito, T., and Nakatsuji, N. (2000) In vivo transfection of testicular germ cells and transgenesis by using the mitochondrially localized jellyfish fluorescent protein gene. FEBS Lett 487:248–251.
  • Ikawa, M., Tergaonkar, V., Ogura, A., Ogonuki, N., Inoue, K., and Verma, I. M. (2002) Restoration of spermatogenesis by lentiviral gene transfer: Offspring from infertile mice. Proc Natl Acad Sci USA 99:7524–7529.
  • Ikawa, M., Tanaka, N., Kao, W. W., and Verma, I. M. (2003) Generation of transgenic mice using lentiviral vectors: A novel preclinical assessment of lentiviral vectors for gene therapy. Mol Ther 8:666–673.
  • Ike, A., Ohta, H., Onishi, M., Iguchi, N., Nishimune, Y., and Nozaki, M. (2004) Transient expression analysis of the mouse ornithine decarboxylase antizyme haploid-specific promoter using in vivo electroporation. FEBS Lett 559:159–164.
  • Jahner, D., Haase, K., Mulligan, R., and Jaenisch, R. (1985) Insertion of the bacterial gpt gene into the germ line of mice by retroviral infection. Proc Natl Acad Sci USA 82:6927–6931.
  • Jonak, J. (2000) Sperm-mediated preparation of transgenic Xenopus laevis and transmission of transgenic DNA to the next generation. Mol Reprod Dev 56:298–300.
  • Kanatsu-Shinohara, M., Ogura, A., Ikegawa, M., Inoue, K., Ogonuki, N., Tashiro, K., Toyokuni. S., Honjo, T., and Shinohara, T. (2002) Adenovirus-mediated gene delivery and in vitro microinsemination produce offspring from infertile male mice. Proc Natl Acad Sci USA 99:1383–1388.
  • Kanatsu-Shinohara, M., Toyokuni, S., and Shinohara, T. (2004) Transgenic mice produced by retroviral transduction of male germ line stem cells in vivo. Biol Reprod 71:1202–1207.
  • Kanatsu-Shinohara, M., Ikawa, M., Takehashi, M., Ogonuki, N., Miki, H., Inoue, K., Kazuki, Y., Lee, J., Toyokuni, S., Oshimura, M., Ogura, A., and Shinohara, T. (2006) Production of knockout mice by random or targeted mutagenesis in spermatogonial stem cells. Proc Natl Acad Sci USA 103:8018–8023.
  • Kaneko, T., Moisyadi, S., Suganuma, R., Hohn, B., Yanagimachi, R., and Pelczarlpar;2005) Recombinase-mediated mouse transgenesis by intracytoplasmic sperm injection. Theriogenology 64:1704–1715.
  • Khoo, H. W. (2000) Sperm-mediated gene transfer studies on zebrafish in Singapore. Mol Reprod Dev 56:278–280.
  • Kroll, K. L. and Amaya, E. (1996) Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. Development 122:3173–3183.
  • Kubota, H., Hayashi, Y., Kubota, Y., Coward, K., and Parrington, J. (2005) Comparison of two methods of in vivo gene transfer by electroporation. Fertil Steril 83:1310–1318.
  • Kurita, K., Burgess, S. M., and Sakai, N. (2004) Transgenic zebrafish produced by retroviral infection of in vitro-cultured sperm. Proc Natl Acad Sci USA 101:1263–1267.
  • Kuznetsov, A. V. and Kuznetsova, I. V. (1995) The binding of exogenous DNA pRK31acZ by rabbit spermatozoa, its transfer to oocytes and expression in preimplantation embryos. Ontogenez 26:300–309.
  • Lai, L., Sun, Q., Wu, G., Murphy, C. N., Kuhholzer, B., Park, K. W., Bonk, A. J., Day, B. N., and Prather, R. S. (2001) Development of porcine embryos and offspring after intracytoplasmic sperm injection with liposome transfected or non-transfected sperm into in vitro matured oocytes. Zygote 9:339–346.
  • Lavitrano, M., Camaioni, A., Fazio, V. M., Dolci, S., Farace, M. G., and Spadafora, C. (1989) Sperm cells as vectors for introducing foreign DNA into eggs; genetic transformation of mice. Cell 57:717–723.
  • Lavitrano, M., French, D., Zani, M., Frati, L., and Spadafora, C. (1992) The interaction between exogenous DNA and sperm cells. Mol Reprod Dev 31:161–169.
  • Lavitrano, M., Maione, B., Forte, E., Francolini, M., Sperandio, S., Testi, R., and Spadafora, C. (1997) The interaction of sperm cells with exogenous DNA: A role of CD4 and major histocompatibility complex class II molecules. Exp Cell Res 233:56–62.
  • Lavitrano, M., Bacci, M. L., Forni, M., Lazzereschi, D., Di Stefano, C., Fioretti, D., Giancotti, P., Marfe, G., Pucci, L., Renzi, L., ., et al, 2002) Efficient production by sperm-mediated gene transfer of human decay accelerating factor (hDAF) transgenic pigs for xenotransplantation. Proc Natl Acad Sci USA 99:14230–14235.
  • Lavitrano, M., Busnelli, M., Cerrito, M. G., Giovannoni, R., Manzini, S., and Vargiolu, A. (2006) Sperm-mediated gene transfer. Reprod Fertil Dev 18:19–23.
  • Lois, C., Hong, E. J., Pease, S., Brown, E. J., and Baltimore, D. (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868–872.
  • Maione, B., Lavitrano, M., Spadafora, C., and Kiessling, A. A. (1998) Sperm-mediated gene transfer in mice. Mol Reprod Dev 50:406–409.
  • Mancheno-Corvo, P. and Martin-Duque, P. (2006) Viral gene therapy. Clin Transl Oncol 8:858–867.
  • McLachlan, R. I., Mallidis, C., Ma, K., Bhasin, S., and de Kretser, D. M. (1998) Genetic disorders and spermatogenesis. Reprod Fertil Dev 10:97–104.
  • Moreira, P. N., Giraldo, P., Cozar, P., Pozueta, J., Jimenez, A., Montoliu, L., and Gutierrez-Adan, A. (2004). Efficient generation of transgenic mice with intact yeast artificial chromosomes by intracytoplasmic sperm injection. Biol Reprod 71:1943–1947.
  • Moreira, P. N., Perez-Crespon, M., Ramirez, M. A., Pozueta, J., Montoliu, L., and Gutierrez-Adan, A. (2007) Effect of transgene concentration, flanking matrix attachment regions, and RecA-coating on the efficiency of mouse transgenesis mediated by intracytoplasmic sperm injection. Biol Reprod 76:336–343.
  • Muramatsu, T., Shibata, O., Ryoki, S., Ohmori, Y., and Okumura, J. (1997) Foreign gene expression in the mouse testis by localized in vivo gene transfer. Biochem Biophys Res Commun 233:45–49.
  • Nagano, M., Shinohara, T., Avarbock, M. R., and Brinster, R. L. (2000) Retrovirus-mediated gene delivery into male germ line stem cells. FEBS Lett 475:7–10.
  • Nagano, M., Watson, D. J., Ryu, B. Y., Wolfe, J. H., and Brinster, R. L. (2002) Lentiviral vector transduction of male germ line stem cells in mice. FEBS Lett 524:111–115.
  • Nagafuchi, S., Namiki, M., Nakahori, Y., Kondoh, N., Okuyama, A., and Nakagome, Y. A. (1993) Minute deletion of the Y chromosome in men with azoospermia. J Urol 150:1155–1157.
  • Nakanishi, A. and Iritani, A. (1993) Gene transfer in the chicken by sperm-mediated methods. Mol Reprod Dev 36:258–261.
  • Naldini, L., Blomer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F. H., Verma, I. M., and Trono, D. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263–267.
  • Ogawa, S., Hayashi, K., Tada, N., Sato, M., Kurihara, T., and Iwaya, M. (1995) Gene expression in blastocysts following direct injection of DNA into testis. J Reprod Dev 41:379–382.
  • Orwig, K. E., Avarbock, M. R., and Brinster, R. L. (2002) Retrovirus-mediated modification of male germline stem cells in rats. Biol Reprod 67:874–879.
  • Osada, T., Toyoda, A., Moisyadi, S., Akutsu, H., Hattori, M., Sakaki, Y., and Yanagimachi, R. (2005) Production of inbred and hybrid transgenic mice carrying large (> 200 kb) foreign DNA fragments by intracytoplasmic sperm injection. Mol Reprod Dev 72:329–335.
  • Parks, J. E., Lee, D. R., Huang, S., and Kaproth, M. T. (2003) Prospects for spermatogenesis in vitro. Theriogenology 59:73–86.
  • Patil, J. G. and Khoo, H. W. (1996) Nuclear internalization of foreign DNA by zebrafish spermatozoa and its enhancement by electroporation. J Exp Zool 274:121–129.
  • Perry, A. C., Wakayama, T., Kishikawa, H., Kasai, T., Okabe, M., Toyoda, Y., and Yanagimachi, R. (1999) Mammalian transgenesis by intracytoplasmic sperm injection. Science 284:1180–1183.
  • Pfeifer, A. (2004). Lentiviral transgenesis. Transgenic Res 13:513–522.
  • Pirity, M., Hadjantonakis, A. K., and Nagy, A. (1998) Embryonic stem cells, creating transgenic animals. Methods Cell Biol 57:279–293.
  • Rieth, A., Pothier, F., and Sirard, M. A. (2000) Electroporation of bovine spermatozoa to carry DNA containing highly repetitive sequences into oocytes and detection of homologous recombination events. Mol Reprod Dev 57:338–345.
  • Robertson, E., Bradley, A., Kuehn, M., and Evans, M. (1986) Germ-line transmission of genes introduced into cultured pluripotential cells by retroviral vector. Nature 323:445–448.
  • Robinson, S. D., Wilson, S., and Hodivala-Dilke, K. M. (2006) Generation of genetically modified embryonic stem cells for the development of knockout mouse animal model systems. Methods Mol Med 120:465–477.
  • Rottmann, O. J., Antes, R., Hofer, P., and Maierhofer, G. (1992) Liposome mediated gene transfer via spermatozoa into avian egg cells. J Anim Breed Genet 109:64–70.
  • Ruggiu, M., Speed, R., Taggart, M., McKay, S. J., Kilanowski, F., Saunders, P., Dorin, J., and Cooke, H. J. (1997) The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 1997 389:73–77.
  • Sasaki, S., Kojima, Y., Kubota, H., Tatsura, H., Hayashi, Y., and Kohri, K. (2000) Effects of the gene transfer into sperm mediated by liposomes on sperm motility and fertilization in vitro. Hinyokika Kiyo 46:591–595.
  • Sato, M., Iwase, R., Kasai, K., and Tada, N. (1994) Direct injection of foreign DNA into mouse testis as a possible alternative of sperm-mediated gene transfer. Animal Biotech 5:19–31.
  • Sato, M., Gotoh, K., and Kimura, M.: (1999a) Sperm-mediated gene transfer by direct injection of foreign DNA into mouse testis. Transgenics 2:357–369.
  • Sato, M., Yabuki, K., Watanabe, T., and Kimura, M. (1999b) Testis-mediated gene transfer (TMGT) in mice: Successful transmission of introduced DNA from F0 to F2 generations. Transgenics 3:11–22.
  • Sato, M., Ishikawa, A., and Kimura, M. (2002) Direct injection of foreign DNA into mouse testis as a possible in vivo gene transfer system via epididymal spermatozoa. Mol Reprod Dev 61:49–56.
  • Shemesh, M., Gurevich, M., Harel-Markowitz, E., Benvenisti, L., Shore, L. S., and Stram, Y. (2000) Gene integration into bovine sperm genome and its expression in transgenic offspring. Mol Reprod Dev 56:306–308.
  • Shen, W., Li, L., Pan, Q., Min, L., Dong, H., and Deng, J. (2006) Efficient and simple production of transgenic mice and rabbits using the new DMSO-sperm mediated exogenous DNA transfer method. Mol Reprod Dev 73:589–594.
  • Shoji, M., Chuma, S., Yoshida, K., Morita, T., and Nakatsuji, N. (2005) RNA interference during spermatogenesis in mice. Dev Biol 282:524–534.
  • Simoni, M. (1994) Transgenic animals in male reproduction research. Exp Clin Endocrinol 102:419–433.
  • Smith, K. R. (2004) Gene therapy: Gene Therapy: The Potential Applicability of Gene Transfer Technology to the Human Germline. Int J Med Sci 1:76–91.
  • Smith, K. and Spadafora, C. (2005) Sperm-mediated gene transfer: Applications and implications. BioEssays 27:551–562.
  • Somboonthum, P., Ohta, H., Yamada, S., Onishi, M., Ike, A., Nishimune, Y., and Nozaki, M. (2005) cAMP-responsive element in TATA-less core promoter is essential for haploid-specific gene expression in mouse testis. Nucleic Acids Res 33:3401–3411.
  • Spadafora, C. (1998) Sperm cells and foreign DNA: A controversial relation. Bioessays 20:955–964.
  • Suganuma, R., Pelczar, P., Spetz, J. F., Hohn, B., Yanagimachi, R., and Moisyadi, S. (2005) Tn5 transposase-mediated mouse transgenesis. Biol Reprod 73:1157–1163.
  • Szczygiel, M. A., Moisyadi, S., and Ward, M. S. (2003) Expression of foreign DNA is associated with paternal chromosome degradation in intracytoplasmic sperm injection-mediated transgenesis in the mouse. Biol Reprod 68:1903–1910.
  • Tsai, H. J. (2000) Electroporated sperm mediation of a gene transfer system for finfish and shellfish. Mol Reprod Dev 56:281–284.
  • Umemoto, Y., Sasaki, S., Kojima, Y., Kubota, H., Kaneko, T., Hayashi, Y., and Kohri, K. (2005) Gene transfer to mouse testes by electroporation and its influence on spermatogenesis. J Androl 26:264–271.
  • van der Putten, H., Botteri, F. M., Miller, A. D., Rosenfeld, M. G., Fan, H., Evans, R. M., and Verma, I. M. (1985) Efficient insertion of genes into the mouse germ line via retroviral vectors. Proc Natl Acad Sci USA 82:6148–6152.
  • Vogt, P. H., Edelmann, A., Hirschmann, P., and Kohler, M. R. (1995) The azoospermia factor (AZF) of the human Y chromosome in Yq11: Function and analysis in spermatogenesis. Reprod Fertil Dev 7:685–693.
  • Wall, R. J. (2001) Pronuclear microinjection. Cloning Stem Cells 3:209–220.
  • Wall, R. J. (2002) New gene transfer methods. Theriogenol 57:189–201.
  • Wang, H. J., Lin, A. X., Zhang, Z. C., and Chen, Y. F.: (2001) Expression of porcine growth hormone gene in transgenic rabbits as reported by green fluorescent protein. Anim Biotechnol 12:101–110.
  • Wang, H. J., Lin, A. X., and Chen, Y. F. (2003) Association of rabbit sperm cells with exogenous DNA. Anim Biotechnol 14:155–165.
  • Wheeler, M. B., Walters, E. M., and Clark, S. G. (2003) Transgenic animals in biomedicine and agriculture: Outlook for the future. Anim Reprod Sci. 79:265–289.
  • Wilson, M. H., Coates, C. J., and George, A. L. Jr.: (2007) PiggyBac transposon-mediated gene transfer in human cells. Mol Ther 15:139–145.
  • Yamazaki, Y., Fujimoto, H., Ando, H., Ohyama, T., Hirota, Y., and Noce, T. (1998) In vivo gene transfer to mouse spermatogenic cells by deoxyribonucleic acid injection into seminiferous tubules and subsequent electroporation. Biol Reprod 59:1439–1444.
  • Yamazaki, Y., Yagi, T., Ozaki, T., and Imoto, K. (2000) In vivo gene transfer to mouse spermatogenic cells using green fluorescent protein as a marker. J Exp Zool 286:212–218.
  • Yang, C. C., Chang, H. S., Lin, C. J., Hsu, C. C., Cheung, J. I., Hwu, L., and Cheng W. T. K. (2004) Cock spermatozoa serve as the gene vector for generation of transgenic chicken (Gallus gallus). Asian Austral J Anim Sci 17:885–891.
  • Yomogida, K., Yagura, Y., and Nishimune, Y. (2002) Electroporated transgene-rescued spermatogenesis in infertile mutant mice with a sertoli cell defect. Biol Reprod 67:712–717.
  • Yonezawa, T., Furuhata, Y., Hirabayashi, K., Suzuki, S., Takahashi, M., and Nishihara, M. (2001) Detection of transgene in progeny at different developmental stages following testis-mediated gene transfer. Mol Reprod Dev 60:196–201.
  • Yonezawa, T., Furuhata, Y., Hirabayashi, K., Suzuki, M., Yamanouchi, K., and Nishihara, M. (2002) Protamine-derived synthetic peptide enhances the efficiency of sperm-mediated gene transfer using liposome-peptide-DNA complex. J Reprod Dev 48:281–286.
  • Zani, M., Lavitrano, M., French, D., Lulli, V., Maione, B., Sperandio, S., and Spadafora, C. (1995) The mechanism of binding of exogenous DNA to sperm cells: Factors controlling the DNA uptake. Exp Cell Res 217:57–64.

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