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Reproduction Biotechnology in Pigs

  • Birbal SinghEmail author
  • Gorakh Mal
  • Sanjeev K. Gautam
  • Manishi Mukesh
Chapter
  • 540 Downloads

Abstract

Pig is an important livestock species used for pork and as valuable model animal for biomedical sciences. Adoption of reproduction biotechniques has vividly transformed the way pig has been raised for clinical research. Nuclear transfer cloning, in vitro embryo production, stem cell biology and engineering, and production of transgenic pigs for producing therapeutics, and organs for transplantation are the remarkable achievements. Pig as model animals is important for research on metabolic and lifestyle diseases and regenerative medicine.
  • Highlights

  • Pigs are the main sources of animal origin meat and as a model animal in biomedical sciences

  • Besides, genetically modified pig is used to generate cells, tissue, and organs for human xenotransplantation.

Keywords

Reproduction biotechnology Transgenic pigs Xenotransplantation Biomedical applications 

References

  1. Betthauser J, Forsberg E, Augenstein M, Childs L, Eilertsen K, Enos J, Forsythe T, Golueke P, Jurgella G, Koppang R, Lesmeister T, Mallon K, Mell G, Misica P, Pace M, Pfister-Genskow M, Strelchenko N, Voelker G, Watt S, Thompson S, Bishop M (2000) Production of cloned pigs from in vitro systems. Nat Biotechnol 18(10):1055–1059PubMedCrossRefGoogle Scholar
  2. Bharti D, Shivakumar SB, Subbarao RB, Rho GJ (2016) Research advancements in porcine derived mesenchymal stem cells. Curr Stem Cell Res Ther 11(1):78–93 (Review)CrossRefGoogle Scholar
  3. Callesen MM, Árnadóttir SS, Lyskjaer I, Ørntoft MW, Høyer S, Dagnaes-Hansen F, Liu Y, Li R, Callesen H, Rasmussen MH, Berthelsen MF, Thomsen MK, Schweiger PJ, Jensen KB, Laurberg S, Ørntoft TF, Elverløv-Jakobsen JE, Andersen CL (2017) A genetically inducible porcine model of intestinal cancer. Mol Oncol. 11(11):1616–1629.  https://doi.org/10.1002/1878-0261.12136 (Epub 2017 Oct 10)PubMedPubMedCentralCrossRefGoogle Scholar
  4. Chang F, Fang R, Wang M, Zhao X, Chang W, Zhang Z, Li N, Meng Q (2017) The transgenic expression of human follistatin-344 increases skeletal muscle mass in pigs. Transgenic Res 26(1):25–36.  https://doi.org/10.1007/s11248-016-9985-x (Epub 2016 Oct 27)PubMedCrossRefGoogle Scholar
  5. Cheng W, Zhao H, Yu H, Xin J, Wang J, Zeng L, Yuan Z, Qing Y, Li H, Jia B, Yang C, Shen Y, Zhao L, Pan W, Zhao HY, Wang W, Wei HJ (2016) Efficient generation of GGTA1-null Diannan miniature pigs using TALENs combined with somatic cell nuclear transfer. Reprod Biol Endocrinol 14(1):77PubMedPubMedCentralCrossRefGoogle Scholar
  6. Cho B, Kim SJ, Lee EJ, Ahn SM, Lee JS, Ji DY, Lee K, Kang JT (2018) Generation of insulin-deficient piglets by disrupting INS gene using CRISPR/Cas9 system. Transgenic Res 27(3):289–300.  https://doi.org/10.1007/s11248-018-0074-1 (Epub 2018 Apr 24)PubMedCrossRefGoogle Scholar
  7. Chou CJ, Peng SY, Wu MH, Yang CC, Lin YS, Cheng WT, Wu SC, Lin YP (2014) Generation and characterization of a transgenic pig carrying a DsRed-monomer reporter gene. PLoS One 9(9):e106864.  https://doi.org/10.1371/journal.pone.0106864 (eCollection 2014)PubMedPubMedCentralCrossRefGoogle Scholar
  8. Cuello C, Berthelot F, Martinat-Botté F, Venturi E, Guillouet P, Vázquez JM, Roca J, Martínez EA (2005) Piglets born after non-surgical deep intrauterine transfer of vitrified blastocysts in gilts. Anim Reprod Sci 85(3–4):275–286PubMedCrossRefGoogle Scholar
  9. del Olmo D, Parrilla I, Gil MA, Maside C, Tarantini T, Angel MA, Roca J, Martinez EA, Vazquez JM (2013) Handling of boar spermatozoa during and after flow cytometric sex-sorting process to improve their in vitro fertilizing ability. Theriogenology 80(4):350–356.  https://doi.org/10.1016/j.theriogenology.2013.04.022 (Epub 2013 Jun 7)PubMedCrossRefGoogle Scholar
  10. Dutton AQ, Choong PF, Goh JC, Lee EH, Hui JH (2010) Enhancement of meniscal repair in the avascular zone using mesenchymal stem cells in a porcine model. J Bone Joint Surg Br 92(1):169–175.  https://doi.org/10.1302/0301-620X.92B1.22629PubMedCrossRefGoogle Scholar
  11. Dobrinsky JR, Pursel VG, Long CR, Johnson LA (2000) Birth of piglets after transfer of embryos cryopreserved by cytoskeletal stabilization and vitrification. Biol Reprod 62(3):564–570PubMedCrossRefGoogle Scholar
  12. Du Y, Kragh PM, Zhang Y, Li J, Schmidt M, Bøgh IB, Zhang X, Purup S, Jørgensen AL, Pedersen AM, Villemoes K, Yang H, Bolund L, Vajta G (2007a) Piglets born from handmade cloning, an innovative cloning method without micromanipulation. Theriogenology 68(8):1104–1110 (Epub 2007 Sep 21)PubMedCrossRefGoogle Scholar
  13. Du Y, Li J, Kragh PM, Zhang Y, Schmidt M, Bøgh IB, Zhang X, Purup S, Kuwayama M, Jørgensen AL, Pedersen AM, Villemoes K, Yang H, Bolund L, Vajta G (2007b) Piglets born from vitrified cloned blastocysts produced with a simplified method of delipation and nuclear transfer. Cloning Stem Cells 9(4):469–476PubMedCrossRefGoogle Scholar
  14. Du Y, Zhang Y, Li J, Kragh PM, Kuwayama M, Ieda S, Zhang X, Schmidt M, Bøgh IB, Purup S, Pedersen AM, Villemoes K, Yang H, Bolund L, Vajta G (2007c) Simplified cryopreservation of porcine cloned blastocysts. Cryobiology 54(2):181–187 (Epub 2007 Jan 27)PubMedCrossRefGoogle Scholar
  15. Eirin A, Zhu XY, Krier JD, Tang H, Jordan KL, Grande JP, Lerman A, Textor SC, Lerman LO (2012) Adipose tissue-derived mesenchymal stem cells improve revascularization outcomes to restore renal function in swine atherosclerotic renal artery stenosis. Stem Cells 30(5):1030–1041.  https://doi.org/10.1002/stem.1047PubMedPubMedCentralCrossRefGoogle Scholar
  16. Eirin A, Zhu XY, Jonnada S, Lerman A, van Wijnen AJ, Lerman LO (2018) Mesenchymal stem cell-derived extracellular vesicles improve the renal microvasculature in metabolic renovascular disease in swine. Cell Transplant 27(7):1080–1095.  https://doi.org/10.1177/0963689718780942 (Epub 2018 Jun 28)PubMedPubMedCentralCrossRefGoogle Scholar
  17. Evans MJ, Notarianni E, Laurie S, Moor RM (1990) Derivation and preliminary characterization of pluripotent cell lines from porcine and bovine blastocysts. Theriogenology. 33, 125–128 CrossRefGoogle Scholar
  18. Faast R, Harrison SJ, Beebe LF, McIlfatrick SM, Ashman RJ, Nottle MB (2006) Use of adult mesenchymal stem cells isolated from bone marrow and blood for somatic cell nuclear transfer in pigs. Cloning Stem Cells 8(3):166–173PubMedCrossRefGoogle Scholar
  19. Fan N, Chen J, Shang Z, Dou H, Ji G, Zou Q, Wu L, He L, Wang F, Liu K, Liu N, Han J, Zhou Q, Pan D, Yang D, Zhao B, Ouyang Z, Liu Z, Zhao Y, Lin L, Zhong C, Wang Q, Wang S, Xu Y, Luan J, Liang Y, Yang Z, Li J, Lu C, Vajta G, Li Z, Ouyang H, Wang H, Wang Y, Yang Y, Liu Z, Wei H, Luan Z, Esteban MA, Deng H, Yang H, Pei D, Li N, Pei G, Liu L, Du Y, Xiao L, Lai L (2013) Piglets cloned from induced pluripotent stem cells. Cell Res 23(1):162–166.  https://doi.org/10.1038/cr.2012.176 (Epub 2012 Dec 18. No abstract available)PubMedPubMedCentralCrossRefGoogle Scholar
  20. Fischer K, Kraner-Scheiber S, Petersen B, Rieblinger B, Buermann A, Flisikowska T, Flisikowski K, Christan S, Edlinger M, Baars W, Kurome M, Zakhartchenko V, Kessler B, Plotzki E, Szczerbal I, Switonski M, Denner J, Wolf E, Schwinzer R, Niemann H, Kind A, Schnieke A (2016) Efficient production of multi-modified pigs for xenotransplantation by ‘combineering’, gene stacking and gene editing. Sci Rep. 29(6):29081.  https://doi.org/10.1038/srep29081CrossRefGoogle Scholar
  21. Flisikowska T, Kind A, Schnieke A (2014) Genetically modified pigs to model human diseases. J Appl Genet 55:53–64PubMedCrossRefGoogle Scholar
  22. Fowler KE, Mandawala AA, Griffin DK, Walling GA, Harvey SC (2018) The production of pig preimplantation embryos in vitro: Current progress and future prospects. Reprod Biol 18(3):203–211.  https://doi.org/10.1016/j.repbio.2018.07.001 (Epub 2018 Jul 7. Review)PubMedCrossRefGoogle Scholar
  23. Fujimura T1, Takahagi Y, Shigehisa T, Nagashima H, Miyagawa S, Shirakura R, Murakami H (2008) Production of alpha 1,3-galactosyltransferase gene-deficient pigs by somatic cell nuclear transfer: a novel selection method for gal alpha 1,3-Gal antigen-deficient cells. Mol Reprod Dev 75(9):1372–1378.  https://doi.org/10.1002/mrd.20890PubMedCrossRefGoogle Scholar
  24. Galli C, Perota A, Brunetti D, Lagutina I, Lazzari G, Lucchini F (2010) Genetic engineering including superseding microinjection: new ways to make GM pigs. Xenotransplantation 17(6):397–410.  https://doi.org/10.1111/j.1399-3089.2010.00590.x (Review)PubMedCrossRefGoogle Scholar
  25. Garcia-Vazquez FA, Ruiz S, Matas C, Izquierdo-Rico MJ, Grullon LA, De Ondiz A, Vieira L, Aviles-Lopez K, Gutierrez-Adán A, Gadea J (2010) Production of transgenic piglets using ICSI-sperm-mediated gene transfer in combination with recombinase RecA. Reproduction 140:259–272PubMedCrossRefGoogle Scholar
  26. Gerlach M, Kraft T, Brenner B, Petersen B, Niemann H, Montag J (2018) Efficient knock-in of a point mutation in porcine fibroblasts using the CRISPR/Cas9-GMNN Fusion Gene Genes (Basel) 9(6). pii: E296.  https://doi.org/10.3390/genes9060296PubMedCentralCrossRefGoogle Scholar
  27. Gil MA, Martinez CA, Nohalez A, Parrilla I, Roca J, Wu J, Ross PJ, Cuello C, Izpisua JC, Martinez EA (2017a) Developmental competence of porcine genome-edited zygotes. Mol Reprod Dev 84(9):814–821.  https://doi.org/10.1002/mrd.22829 (Epub 2017 Jun 8)PubMedCrossRefGoogle Scholar
  28. Gil MA, Martinez CA, Nohalez A, Parrilla I, Roca J, Wu J, Ross PJ, Cuello C, Izpisua JC, Martinez EA (2017) Developmental competence of porcine genome-edited zygotes. Mol Reprod Dev 84(9):814–821.  https://doi.org/10.1002/mrd.22829 (Epub 2017 Jun 8. Review)PubMedCrossRefGoogle Scholar
  29. Gupta MK, Das ZC, Heo YT, Joo JY, Chung HJ, Song H, Kim JH, Kim NH, Lee HT, Ko DH, Uhm SJ (2013) Transgenic chicken, mice, cattle, and pig embryos by somatic cell nuclear transfer into pigoocytes. Cell Reprogram. 15(4):322–328.  https://doi.org/10.1089/cell.2012.0074 (Epub 2013 Jun 28)PubMedPubMedCentralCrossRefGoogle Scholar
  30. Gutierrez K, Dicks N, Glanzner WG, Agellon LB, Bordignon V (2015) Efficacy of the porcine species in biomedical research. Front Genet 6:293.  https://doi.org/10.3389/fgene.2015.00293 (eCollection 2015)
  31. Hammer RE, Pursel VG, Rexroad CE Jr, Wall RJ, Bolt DJ, Ebert KM, Palmiter RD, Brinster RL (1985) Production of transgenic rabbits, sheep and pigs by microinjection. Nature 315(6021):680–683PubMedCrossRefGoogle Scholar
  32. Hisamatsu S, Sakaue M, Takizawa A, Kato T, Kamoshita M, Ito J, Kashiwazaki N (2015) Knockout of targeted gene in porcine somatic cells using zinc-finger nuclease. Anim Sci J 86(2):132–137.  https://doi.org/10.1111/asj.12259 (Epub 2014 Sep 3)PubMedCrossRefGoogle Scholar
  33. Hofmann A, Kessler B, Ewerling S, Weppert M, Vogg B, Ludwig H, Stojkovic M, Boelhauve M, Brem G, Wolf E, Pfeifer A (2003) Efficient transgenesis in farm animals by lentiviral vectors. EMBO Rep 4(11):1054–1060 (Epub 2003 Oct 17)PubMedPubMedCentralCrossRefGoogle Scholar
  34. Hwang SU, Eun K, Yoon JD, Kim H, Hyun SH (2018) Production of transgenic pigs using a pGFAP-CreERT2/EGFP LoxP inducible system for central nervous system disease models. J Vet Sci 19(3):434–445.  https://doi.org/10.4142/jvs.2018.19.3.434PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hyun S, Lee G, Kim D, Kim H, Lee S, Nam D, Jeong Y, Kim S, Yeom S, Kang S, Han J, Lee B, Hwang W (2003) Production of nuclear transfer-derived piglets using porcine fetal fibroblasts transfected with the enhanced green fluorescent protein. Biol Reprod 69(3):1060–1068 (Epub 2003 May 28)PubMedCrossRefGoogle Scholar
  36. Ivics Z, Garrels W, Mátés L, Yau TY, Bashir S, Zidek V, Landa V, Geurts A, Pravenec M, Rülicke T, Kues WA, Izsvák Z (2014) Germline transgenesis in pigs by cytoplasmic microinjection of Sleeping Beauty transposons. Nat Protoc 9(4):810–827.  https://doi.org/10.1038/nprot.2014.010 (Epub 2014 Mar 13)PubMedCrossRefGoogle Scholar
  37. Knox RV (2014) Impact of swine reproductive technologies on pig and global food production. Adv Exp Med Biol 752:131–160.  https://doi.org/10.1007/978-1-4614-8887-3_7 (Review)Google Scholar
  38. Knox RV, Rodriguez Zas SL, Sloter NL, McNamara KA, Gall TJ, Levis DG, Safranski TJ, Singleton WL (2013) An analysis of survey data by size of the breeding herd for the reproductive management practices of North American sow farms. J Anim Sci 91(1):433–445PubMedCrossRefGoogle Scholar
  39. Kues WA, Schwinzer R, Wirth D, Verhoeyen E, Lemme E, Herrmann D, Barg-Kues B, Hauser H, Wonigeit H, Niemann H (2006) Epigenetic silencing and tissue independent expression of a novel tetracycline inducible system in double-transgenic pigs. FASEB J 20:E1–E10CrossRefGoogle Scholar
  40. Lai L, Kolber-Simonds D, Park KW, Cheong HT, Greenstein JL, Im GS, Samuel M, Bonk A, Rieke A, Day BN, Murphy CN, Carter DB, Hawley RJ, Prather RS (2002) Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science 295(5557):1089–1092 (Epub 2002 Jan 3)PubMedCrossRefGoogle Scholar
  41. Laroye C, Lemarié J, Boufenzer A, Labroca P, Cunat L, Alauzet C, Groubatch F, Cailac C, Jolly L, Bensoussan D, Reppel L, Gibot S (2018) Clinical-grade mesenchymal stem cells derived from umbilical cord improve septic shock in pigs. Intensive Care Med Exp 6(1):24.  https://doi.org/10.1186/s40635-018-0194-1PubMedPubMedCentralCrossRefGoogle Scholar
  42. Lee GS, Kim HS, Hyun SH, Lee SH, Jeon HY, Nam DH, Jeong YW, Kim S, Kim JH, Han JY, Ahn C, Kang SK, Lee BC, Hwang WS (2005) Production of transgenic cloned piglets from genetically transformed fetal fibroblasts selected by green fluorescent protein. Theriogenology 63(4):973–991PubMedCrossRefGoogle Scholar
  43. Li GP, Tan JH, Sun QY, Meng QG, Yue KZ, Sun XS, Li ZY, Wang HB, Xu LB (2000) Cloned piglets born after nuclear transplantation of embryonic blastomeres into porcine oocytes matured in vivo. Cloning 2(1):45–52PubMedCrossRefGoogle Scholar
  44. Li M, Zhang D, Hou Y, Jiao L, Zheng X, Wang WH (2003) Isolation and culture of embryonic stem cells from porcine blastocysts. Mol Reprod Dev 65(4):429–434PubMedCrossRefGoogle Scholar
  45. Li Z, Zeng F, Meng F, Xu Z, Zhang X, Huang X, Tang F, Gao W, Shi J, He X, Liu D, Wang C, Urschitz J, Moisyadi S, Wu Z (2014) Generation of transgenic pigs by cytoplasmic injection of piggyBac transposase-based pmGENIE-3 plasmids. Biol Reprod 90(5):93.  https://doi.org/10.1095/biolreprod.113.116905 (Print 2014 May)
  46. Lin YS, Yang CC, Hsu CC, Hsu JT, Wu SC, Lin CJ, Cheng WT (2015) Establishment of a novel, eco-friendly transgenic pig model using porcine pancreatic amylase promoter-driven fungal cellulase transgenes. Transgenic Res 24(1):61–71.  https://doi.org/10.1007/s11248-014-9817-9 (Epub 2014 Jul 26)PubMedCrossRefGoogle Scholar
  47. Liu W, Wu LH, Yue M, Nashun B, Tang H, Chen Y, Chen BZ, Yuan J, Xiao D, Gu WW (2017) Generation of DKK1 transgenic Tibet minipigs by somatic cell nuclear transfer (SCNT) Oncotarget 8(43):74331–74339.  https://doi.org/10.18632/oncotarget.20604 (eCollection 2017 Sep 26)
  48. Lutz AJ, Li P, Estrada JL, Sidner RA, Chihara RK, Downey SM, Burlak C, Wang ZY, Reyes LM, Ivary B, Yin F, Blankenship RL, Paris LL, Tector AJ (2013) Double knockout pigs deficient in N-glycolylneuraminic acid and galactose α-1,3-galactose reduce the humoral barrier to xenotransplantation. Xenotransplantation 20(1):27–35.  https://doi.org/10.1111/xen.12019PubMedCrossRefGoogle Scholar
  49. Maehara M, Matsunari H, Honda K, Nakano K, Takeuchi Y, Kanai T, Matsuda T, Matsumura Y, Hagiwara Y, Sasayama N, Shirasu A, Takahashi M, Watanabe M, Umeyama K, Hanazono Y, Nagashima H (2012) Hollow fiber vitrification provides a novel method for cryopreserving in vitro maturation/fertilization-derived porcine embryos. Biol Reprod 87(6):133.  https://doi.org/10.1095/biolreprod.112.100339 (Print 2012 Jun)
  50. Maes D, Van Soom A, Appeltant R, Arsenakis I, Nauwynck H (2016) Porcine semen as a vector for transmission of viral pathogens. Theriogenology 85(1):27–38.  https://doi.org/10.1016/j.theriogenology.2015.09.046 (Epub 2015 Sep 26. Review)PubMedCrossRefGoogle Scholar
  51. Martinez EA, Caamaño JN, Gil MA, Rieke A, McCauley TC, Cantley TC, Vazquez JM, Roca J, Vazquez JL, Didion BA, Murphy CN, Prather RS, Day BN (2004) Successful nonsurgical deep uterine embryo transfer in pigs. Theriogenology 61(1):137–146PubMedCrossRefGoogle Scholar
  52. Matsunari H, Maehara M, Nakano K, Ikezawa Y, Hagiwara Y, Sasayama N, Shirasu A, Ohta H, Takahashi M, Nagashima H (2012) Hollow fiber vitrification: a novel method for vitrifying multiple embryos in a single device. J Reprod Dev 58(5):599–608 (Epub 2012 Jul 4)PubMedCrossRefGoogle Scholar
  53. McCreath KJ, Howcroft J, Campbell KH, Colman A, Schnieke AE, Kind AJ (2000) Production of gene-targeted sheep by nuclear transfer from cultured somatic cells. Nature 405(6790):1066–1069 (Erratum in: Nature 2000 Nov 2;408(6808):120)PubMedCrossRefGoogle Scholar
  54. Mei SH, McCarter SD, Deng Y, Parker CH, Liles WC, Stewart DJ (2007) Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. PLoS Med. 4(9):e269PubMedPubMedCentralCrossRefGoogle Scholar
  55. Meidinger RG, Ajakaiye A, Fan MZ, Zhang J, Phillips JP, Forsberg CW (2013) Digestive utilization of phosphorus from plant-based diets in the Cassie line of transgenic Yorkshire pigs that secrete phytase in the saliva. J Anim Sci 91(3):1307–1320.  https://doi.org/10.2527/jas.2012-5575 (Epub 2013 Jan 7)PubMedCrossRefGoogle Scholar
  56. Mendicino M, Ramsoondar J, Phelps C, Vaught T, Ball S, LeRoith T, Monahan J, Chen S, Dandro A, Boone J, Jobst P, Vance A, Wertz N, Bergman Z, Sun XZ, Polejaeva I, Butler J, Dai Y, Ayares D, Wells K (2011) Generation of antibody- and B cell-deficient pigs by targeted disruption of the J-region gene segment of the heavy chain locus. Transgenic Res 20(3):625–641.  https://doi.org/10.1007/s11248-010-9444-z (Epub 2010 Sep 26)PubMedCrossRefGoogle Scholar
  57. Miernik K, Karasinski J (2012) Porcine uterus contains a population of mesenchymal stem cells. Reproduction 143(2):203–209.  https://doi.org/10.1530/REP-11-0202 (Epub 2011 Nov 7)PubMedCrossRefGoogle Scholar
  58. Müller M, Brenig B, Winnacker EL, Brem G (1992) Transgenic pigs carrying cDNA copies encoding the murine Mx1 protein which confers resistance to influenza virus infection. Gene 121(2):263–270PubMedCrossRefGoogle Scholar
  59. Onishi A, Iwamoto M, Akita T, Mikawa S, Takeda K, Awata T, Hanada H, Perry AC (2000) Pig cloning by microinjection of fetal fibroblast nuclei. Science 289(5482):1188–1190PubMedCrossRefGoogle Scholar
  60. Ozawa M, Himaki T, Ookutsu S, Mizobe Y, Ogawa J, Miyoshi K, Yabuki A, Fan J, Yoshida M (2015) Production of cloned miniature pigs expressing high levels of human apolipoprotein(a) in plasma. PLoS One 10(7):e0132155.  https://doi.org/10.1371/journal.pone.0132155 (eCollection 2015)PubMedPubMedCentralCrossRefGoogle Scholar
  61. Phelps CJ, Koike C, Vaught TD, Boone J, Wells KD, Chen SH, Ball S, Specht SM, Polejaeva IA, Monahan JA, Jobst PM, Sharma SB, Lamborn AE, Garst AS, Moore M, Demetris AJ, Rudert WA, Bottino R, Bertera S, Trucco M, Starzl TE, Dai Y, Ayares DL (2003) Production of alpha 1,3-galactosyltransferase-deficient pigs. Science 299(5605):411–414 (Epub 2002 Dec 19)PubMedPubMedCentralCrossRefGoogle Scholar
  62. Petersen B, Frenzel A, Lucas-Hahn A, Herrmann D, Hassel P, Klein S, Ziegler M, Hadeler KG, Niemann H (2016) Efficient production of biallelic GGTA1 knockout pigs by cytoplasmic microinjection of CRISPR/Cas9 into zygotes. Xenotransplantation 23(5):338–346.  https://doi.org/10.1111/xen.12258 (Epub 2016 Sep 9)PubMedCrossRefGoogle Scholar
  63. Polejaeva IA, Chen SH, Vaught TD, Page RL, Mullins J, Ball S, Dai Y, Boone J, Walker S, Ayares DL, Colman A, Campbell KH (2000) Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407(6800):86–90CrossRefGoogle Scholar
  64. Reyes LM, Estrada JL, Wang ZY, Blosser RJ, Smith RF, Sidner RA, Paris LL, Blankenship RL, Ray CN, Miner AC, Tector M, Tector AJ (2014) Creating class I MHC-null pigs using guide RNA and the Cas9 endonuclease. J Immunol. 193(11):5751–5757.  https://doi.org/10.4049/jimmunol.1402059 (Epub 2014 Oct 22)PubMedPubMedCentralCrossRefGoogle Scholar
  65. Roca J, Parrilla I, Bolarin A, Martinez EA, Rodriguez-Martinez H (2016) Will AI in pigs become more efficient? Theriogenology 86(1):187–193.  https://doi.org/10.1016/j.theriogenology.2015.11.026 (Epub 2015 Dec 2. Review)PubMedCrossRefGoogle Scholar
  66. Schulze M, Bortfeldt R, Schäfer J, Jung M, Fuchs-Kittowski F (2018) Effect of vibration emissions during shipping of artificial insemination doses on boar semen quality. Anim Reprod Sci. 192:328–334.  https://doi.org/10.1016/j.anireprosci.2018.03.035 (Epub 2018 Mar 31)PubMedCrossRefGoogle Scholar
  67. Sheets TP, Park CH, Park KE, Powell A, Donovan DM, Telugu BP (2016) Somatic cell nuclear transfer followed by CRIPSR/Cas9 microinjection results in highly efficient genome editing in cloned pigs. Int J Mol Sci 17(12). pii: E2031Google Scholar
  68. Shim H, Gutiérrez-Adán A, Chen LR, BonDurant RH, Behboodi E, Anderson GB (1997) Isolation of pluripotent stem cells from cultured porcine primordial germ cells. Biol Reprod 57(5):1089–1095PubMedCrossRefGoogle Scholar
  69. Sommer JR, Estrada JL, Collins EB, Bedell M, Alexander CA, Yang Z, Hughes G, Mir B, Gilger BC, Grob S, Wei X, Piedrahita JA, Shaw PX, Petters RM, Zhang K (2011) Production of ELOVL4 transgenic pigs: a large animal model for Stargardt-like macular degeneration. Br J Ophthalmol 95(12):1749–1754.  https://doi.org/10.1136/bjophthalmol-2011-300417 (Epub 2011 Aug 26)PubMedCrossRefGoogle Scholar
  70. Tanihara F, Takemoto T, Kitagawa E, Rao S, Do LT, Onishi A, Yamashita Y, Kosugi C, Suzuki H, Sembon S, Suzuki S, Nakai M, Hashimoto M, Yasue A, Matsuhisa M, Noji S, Fujimura T, Fuchimoto D, Otoi T (2016) Somatic cell reprogramming-free generation of genetically modified pigs. Sci Adv 2(9):e1600803.  https://doi.org/10.1126/sciadv.1600803 (eCollection 2016 Sep)PubMedPubMedCentralCrossRefGoogle Scholar
  71. Wang Y, Du Y, Zhou X, Wang L, Li J, Wang F, Huang Z, Huang X, Wei H (2016) Efficient generation of B2 m-null pigs via injection of zygote with TALENs. Sci Rep 16(6):38854.  https://doi.org/10.1038/srep38854CrossRefGoogle Scholar
  72. West FD, Terlouw SL, Dobrinsky JR, Lu Y, Jordan ET, Stice SL (2015) Generation of chimeras from porcine induced pluripotent stem cells. Meth Mol Biol 1330:153–167.  https://doi.org/10.1007/978-1-4939-2848-4_14CrossRefGoogle Scholar
  73. Wu Z, Chen J, Ren J, Bao L, Liao J, Cui C, Rao L, Li H, Gu Y, Dai H, Zhu H, Teng X, Cheng L, Xiao L (2009) Generation of pig induced pluripotent stem cells with a drug-inducible system. J Mol Cell Biol. 1(1):46–54.  https://doi.org/10.1093/jmcb/mjp003 (Epub 2009 Jun 3)PubMedCrossRefGoogle Scholar
  74. Yang J, Zhao Q, Wang K, Ma C, Liu H, Liu Y, Guan W (2018) Isolation, culture and biological characteristics of multipotent porcine tendon-derived stem cells. Int J Mol Med 41(6):3611–3619.  https://doi.org/10.3892/ijmm.2018.3545 (Epub 2018 Mar 7)PubMedCrossRefGoogle Scholar
  75. Yang Z, Vajta G, Xu Y, Luan J, Lin M, Liu C, Tian J, Dou H, Li Y, Liu T, Zhang Y, Li L, Yang W, Bolund L, Yang H, Du Y (2016) Production of pigs by hand-made cloning using mesenchymal stem cells and fibroblasts. Cell Reprogram 18(4):256–263.  https://doi.org/10.1089/cell.2015.0072PubMedCrossRefGoogle Scholar
  76. Yu H, Long W, Zhang X, Xu K, Guo J, Zhao H, Li H, Qing Y, Pan W, Jia B, Zhao HY, Huang X, Wei HJ (2018) Generation of GHR-modified pigs as Laron syndrome models via a dual-sgRNAs/Cas9 system and somatic cell nuclear transfer. J Transl Med 16(1):41.  https://doi.org/10.1186/s12967-018-1409-7PubMedPubMedCentralCrossRefGoogle Scholar
  77. Zeyland J, Gawrońska B, Juzwa W, Jura J, Nowak A, Słomski R, Smorąg Z, Szalata M, Woźniak A, Lipiński D (2013) Transgenic pigs designed to express human α-galactosidase to avoid humoral xenograft rejection. J Appl Genet. 54(3):293–303.  https://doi.org/10.1007/s13353-013-0156-y (Epub 2013 Jun 19)PubMedPubMedCentralCrossRefGoogle Scholar
  78. Zhang X, Li Z, Yang H, Liu D, Cai G, Li G, Mo J, Wang D, Zhong C, Wang H, Sun Y, Shi J, Zheng E, Meng F, Zhang M, He X, Zhou R, Zhang J, Huang M, Zhang R, Li N, Fan M, Yang J, Wu Z (2018) Novel transgenic pigs with enhanced growth and reduced environmental impact. Elife 7. pii: e34286.  https://doi.org/10.7554/elife.34286
  79. Zhao D, Li Y, Zhou X, Yang Z (2018) Peripheral blood mesenchymal stem cells combined with modified demineralized bone matrix promote pig cartilage defect repair. Cells Tissues Organs 1–9.  https://doi.org/10.1159/000493210 (Epub ahead of print)PubMedCrossRefGoogle Scholar
  80. Zhou X, Wang L, Du Y, Xie F, Li L, Liu Y, Liu C, Wang S, Zhang S, Huang X, Wang Y, Wei H (2016) Efficient generation of gene-modified pigs harboring precise orthologous human mutation via CRISPR/Cas9-induced homology-directed repair in zygotes. Hum Mutat 37(1):110–118.  https://doi.org/10.1002/humu.22913 (Epub 2015 Oct 23)PubMedCrossRefGoogle Scholar
  81. Zhou X, Xin J, Fan N, Zou Q, Huang J, Ouyang Z, Zhao Y, Zhao B, Liu Z, Lai S, Yi X, Guo L, Esteban MA, Zeng Y, Yang H, Lai L (2015) Generation of CRISPR/Cas9-mediated gene-targeted pigs via somatic cell nuclear transfer. Cell Mol Life Sci 72(6):1175–1184.  https://doi.org/10.1007/s00018-014-1744-7 (Epub 2014 Oct 2)PubMedCrossRefGoogle Scholar
  82. Zhu XX, Zhong YZ, Ge YW, Lu KH1, Lu SS (2018) Generation of transgenic-cloned Huanjiang Xiang pigs systemically expressing enhanced green fluorescent protein. Reprod Domest Anim.  https://doi.org/10.1111/rda.13301 (Epub ahead of print)PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Birbal Singh
    • 1
    Email author
  • Gorakh Mal
    • 1
  • Sanjeev K. Gautam
    • 2
  • Manishi Mukesh
    • 3
  1. 1.ICAR-Indian Veterinary Research Institute, Regional StationPalampurIndia
  2. 2.Department of BiotechnologyKurukshetra UniversityKurukshetraIndia
  3. 3.Department of Animal BiotechnologyICAR-National Bureau of Animal Genetic ResourcesKarnalIndia

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