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PMID: 18324337 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Production of CFTR-null and CFTR-DeltaF508 heterozygous pigs by adeno-associated virus-mediated gene targeting and somatic cell nuclear transfer.

The Journal of clinical investigation ·Vol. 118 ·No. 4 ·2008-04-00 ·Pages 1571-7

Rogers CS, Hao Y, Rokhlina T, Samuel M, Stoltz DA, Li Y, Petroff E, Vermeer DW, Kabel AC, Yan Z, Spate L, Wax D, Murphy CN, Rieke A, Whitworth K, Linville ML, Korte SW, Engelhardt JF, Welsh MJ, Prather RS

Abstract

Progress toward understanding the pathogenesis of cystic fibrosis (CF) and developing effective therapies has been hampered by lack of a relevant animal model. CF mice fail to develop the lung and pancreatic disease that cause most of the morbidity and mortality in patients with CF. Pigs may be better animals than mice in which to model human genetic diseases because their anatomy, biochemistry, physiology, size, and genetics are more similar to those of humans. However, to date, gene-targeted mammalian models of human genetic disease have not been reported for any species other than mice. Here we describe the first steps toward the generation of a pig model of CF. We used recombinant adeno-associated virus (rAAV) vectors to deliver genetic constructs targeting the CF transmembrane conductance receptor (CFTR) gene to pig fetal fibroblasts. We generated cells with the CFTR gene either disrupted or containing the most common CF-associated mutation (DeltaF508). These cells were used as nuclear donors for somatic cell nuclear transfer to porcine oocytes. We thereby generated heterozygote male piglets with each mutation. These pigs should be of value in producing new models of CF. In addition, because gene-modified mice often fail to replicate human diseases, this approach could be used to generate models of other human genetic diseases in species other than mice.

MeSH Terms
Alleles Animals Animals, Genetically Modified Cystic Fibrosis Transmembrane Conductance Regulator/deficiency,genetics,metabolism Dependovirus/genetics Fibroblasts Gene Expression Regulation Gene Targeting/methods Genetic Vectors/genetics Genome/genetics Heterozygote Mutation/genetics Nuclear Transfer Techniques Phenylalanine/genetics,metabolism RNA, Messenger/genetics Swine
Chemicals
RNA, Messenger Cystic Fibrosis Transmembrane Conductance Regulator Phenylalanine
Authors & Affiliations
20 authors, click to expand affiliations / ORCID
Rogers Christopher S
Department of Internal Medicine, University of Iowa Carver College of Medicine, Iowa City, Iowa, USA.
Hao Yanhong
Rokhlina Tatiana
Samuel Melissa
Stoltz David A
Li Yuhong
Petroff Elena
Vermeer Daniel W
Kabel Amanda C
Yan Ziying
Spate Lee
Wax David
Murphy Clifton N
Rieke August
Whitworth Kristin
Linville Michael L
Korte Scott W
Engelhardt John F
Welsh Michael J
Prather Randall S
References (63)
63 references, click to expand
  1. Defects in processing and trafficking of the cystic fibrosis transmembrane conductance regulator.
    Kidney Int. 2000 Mar;57(3):825-31 PMID: 10720935
  2. Analysis of cystic fibrosis gener product (CFTR) function in patients with pancreas divisum and recurrent acute pancreatitis.
    Am J Gastroenterol. 2004 Aug;99(8):1557-62 PMID: 15307877
  3. In vitro development of preimplantation porcine nuclear transfer embryos cultured in different media and gas atmospheres.
    Theriogenology. 2004 Apr 15;61(6):1125-35 PMID: 15037000
  4. Choose your target.
    Nat Genet. 2000 Oct;26(2):159-61 PMID: 11017070
  5. Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning.
    Science. 2002 Feb 8;295(5557):1089-92 PMID: 11778012
  6. Pathophysiology of gene-targeted mouse models for cystic fibrosis.
    Physiol Rev. 1999 Jan;79(1 Suppl):S193-214 PMID: 9922382
  7. High frequency targeting of genes to specific sites in the mammalian genome.
    Cell. 1986 Feb 14;44(3):419-28 PMID: 3002636
  8. Mutation of R555 in CFTR-delta F508 enhances function and partially corrects defective processing.
    Recept Channels. 1996;4(1):63-72 PMID: 8723647
  9. Generation of fertile cloned rats by regulating oocyte activation.
    Science. 2003 Nov 14;302(5648):1179 PMID: 14512506
  10. Gene targeting and somatic cell genetics--a rebirth or a coming of age?
    Trends Genet. 1999 Mar;15(3):88-90 PMID: 10203800
  11. Cystic fibrosis mouse models.
    Am J Respir Cell Mol Biol. 2007 Jan;36(1):1-7 PMID: 16888286
  12. CFTR chloride channel drug discovery--inhibitors as antidiarrheals and activators for therapy of cystic fibrosis.
    Curr Pharm Des. 2006;12(18):2235-47 PMID: 16787252
  13. Cystic fibrosis: genotypic and phenotypic variations.
    Annu Rev Genet. 1995;29:777-807 PMID: 8825494
  14. Production of cloned pigs by using somatic cells as donors.
    Cloning Stem Cells. 2003;5(4):233-41 PMID: 14733743
  15. Production of gene-targeted sheep by nuclear transfer from cultured somatic cells.
    Nature. 2000 Jun 29;405(6790):1066-9 PMID: 10890449
  16. Morphometric characterization of the airway and vascular systems of the lung of the domestic pig, Sus scrofa: comparison of the airway, arterial and venous systems.
    Comp Biochem Physiol A Mol Integr Physiol. 2001 Nov;130(4):781-98 PMID: 11691614
  17. Pharmacologic approaches to correcting the basic defect in cystic fibrosis.
    N Engl J Med. 2003 Oct 9;349(15):1401-4 PMID: 14534332
  18. Dogs cloned from adult somatic cells.
    Nature. 2005 Aug 4;436(7051):641 PMID: 16079832
  19. Zero-stress state of intra- and extraparenchymal airways from human, pig, rabbit, and sheep lung.
    J Appl Physiol (1985). 2002 Mar;92(3):1261-6 PMID: 11842066
  20. A mouse model for the delta F508 allele of cystic fibrosis.
    J Clin Invest. 1995 Oct;96(4):2051-64 PMID: 7560099
  21. The respiratory immune system of pigs.
    Vet Immunol Immunopathol. 1996 Nov;54(1-4):191-5 PMID: 8988865
  22. Cystic fibrosis.
    Am J Respir Crit Care Med. 1996 Nov;154(5):1229-56 PMID: 8912731
  23. Functional disruption of the prion protein gene in cloned goats.
    J Gen Virol. 2006 Apr;87(Pt 4):1019-1027 PMID: 16528053
  24. Influence of DNA delivery method on gene targeting frequencies in human cells.
    Somat Cell Mol Genet. 1999 Jan;25(1):27-31 PMID: 10925701
  25. Cloned rabbits produced by nuclear transfer from adult somatic cells.
    Nat Biotechnol. 2002 Apr;20(4):366-9 PMID: 11923842
  26. Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive.
    Nature. 1992 Aug 27;358(6389):761-4 PMID: 1380673
  27. Production of cattle lacking prion protein.
    Nat Biotechnol. 2007 Jan;25(1):132-8 PMID: 17195841
  28. Generation of cloned transgenic pigs rich in omega-3 fatty acids.
    Nat Biotechnol. 2006 Apr;24(4):435-6 PMID: 16565727
  29. Processing and function of CFTR-DeltaF508 are species-dependent.
    Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15370-5 PMID: 17873061
  30. Hyposecretion of beta-adrenergically induced sweating in cystic fibrosis heterozygotes.
    Pediatr Res. 1987 Sep;22(3):271-6 PMID: 2889182
  31. Targeted transgene insertion into human chromosomes by adeno-associated virus vectors.
    Nat Biotechnol. 2002 Jul;20(7):735-8 PMID: 12089561
  32. Human gene targeting by viral vectors.
    Nat Genet. 1998 Apr;18(4):325-30 PMID: 9537413
  33. Efficient gene targeting mediated by adeno-associated virus and DNA double-strand breaks.
    Mol Cell Biol. 2003 May;23(10):3558-65 PMID: 12724414
  34. Sequential targeting of the genes encoding immunoglobulin-mu and prion protein in cattle.
    Nat Genet. 2004 Jul;36(7):775-80 PMID: 15184897
  35. Viable offspring derived from fetal and adult mammalian cells.
    Nature. 1997 Feb 27;385(6619):810-3 PMID: 9039911
  36. Somatic cell nuclear transfer.
    Nature. 2002 Oct 10;419(6907):583-6 PMID: 12374931
  37. Ubiquitination of both adeno-associated virus type 2 and 5 capsid proteins affects the transduction efficiency of recombinant vectors.
    J Virol. 2002 Mar;76(5):2043-53 PMID: 11836382
  38. CFTR is a conductance regulator as well as a chloride channel.
    Physiol Rev. 1999 Jan;79(1 Suppl):S145-66 PMID: 9922379
  39. Cloned ferrets produced by somatic cell nuclear transfer.
    Dev Biol. 2006 May 15;293(2):439-48 PMID: 16584722
  40. Sex identification in mammals with polymerase chain reaction and its use to examine sex effects on diameter of day-10 or -11 pig embryos.
    J Anim Sci. 1995 May;73(5):1408-15 PMID: 7665371
  41. Production of nuclear transfer-derived swine that express the enhanced green fluorescent protein.
    Anim Biotechnol. 2001 Nov;12(2):173-81 PMID: 11808633
  42. Expression of the cystic fibrosis transmembrane conductance regulator gene in the respiratory tract of normal individuals and individuals with cystic fibrosis.
    Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6565-9 PMID: 1713683
  43. Gene targeting in mice: functional analysis of the mammalian genome for the twenty-first century.
    Nat Rev Genet. 2005 Jun;6(6):507-12 PMID: 15931173
  44. Will the pig solve the transplantation backlog?
    Annu Rev Med. 2002;53:133-47 PMID: 11818467
  45. Production of goats by somatic cell nuclear transfer.
    Nat Biotechnol. 1999 May;17(5):456-61 PMID: 10331804
  46. Variable reduction in beta-adrenergic sweat secretion in cystic fibrosis heterozygotes.
    J Lab Clin Med. 1988 May;111(5):511-8 PMID: 2896223
  47. Altered chloride ion channel kinetics associated with the delta F508 cystic fibrosis mutation.
    Nature. 1991 Dec 19-26;354(6354):526-8 PMID: 1722027
  48. Cloned pigs produced by nuclear transfer from adult somatic cells.
    Nature. 2000 Sep 7;407(6800):86-90 PMID: 10993078
  49. Cloned transgenic calves produced from nonquiescent fetal fibroblasts.
    Science. 1998 May 22;280(5367):1256-8 PMID: 9596577
  50. Manipulating the mammalian genome by homologous recombination.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8403-10 PMID: 11459982
  51. High-fidelity correction of mutations at multiple chromosomal positions by adeno-associated virus vectors.
    J Virol. 1999 Sep;73(9):7376-80 PMID: 10438827
  52. Complete activation of porcine oocytes induced by the sulfhydryl reagent, thimerosal.
    Biol Reprod. 1997 Nov;57(5):1123-7 PMID: 9369179
  53. Some functional consequences of species differences in lung anatomy.
    Adv Vet Sci Comp Med. 1982;26:1-33 PMID: 6758536
  54. Evaluation of gene targeting by homologous recombination in ovine somatic cells.
    Mol Reprod Dev. 2003 Oct;66(2):115-25 PMID: 12950098
  55. Mutations in the cystic fibrosis transmembrane regulator gene and in vivo transepithelial potentials.
    Am J Respir Crit Care Med. 2006 Oct 1;174(7):787-94 PMID: 16840743
  56. Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei.
    Nature. 1998 Jul 23;394(6691):369-74 PMID: 9690471
  57. Targeted disruption of the alpha1,3-galactosyltransferase gene in cloned pigs.
    Nat Biotechnol. 2002 Mar;20(3):251-5 PMID: 11875425
  58. Generation and characterization of a delta F508 cystic fibrosis mouse model.
    Nat Genet. 1995 Aug;10(4):445-52 PMID: 7545494
  59. Adeno-associated virus-targeted disruption of the CFTR gene in cloned ferrets.
    J Clin Invest. 2008 Apr;118(4):1578-83 PMID: 18324338
  60. Uncertainty in the diagnosis of cystic fibrosis: possible role of in vivo nasal potential difference measurements.
    J Pediatr. 1998 Apr;132(4):596-9 PMID: 9580755
  61. Gene targeting in livestock.
    Reprod Suppl. 2003;61:495-508 PMID: 14635957
  62. The immune system of the respiratory tract in pigs.
    Vet Immunol Immunopathol. 1994 Oct;43(1-3):151-6 PMID: 7856047
  63. Gene targeting with viral vectors.
    Mol Ther. 2005 Jul;12(1):9-17 PMID: 15932801
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
2008-04-00
Pages
1571-7
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC2265103
Subset
IM
Grants
NHLBI NIH HHS · P01 HL051670 · United States
NHLBI NIH HHS · T32 HL007638 · United States
Howard Hughes Medical Institute · United States
NIDDK NIH HHS · DK54759 · United States
NHLBI NIH HHS · HL51670 · United States
NIDDK NIH HHS · P30 DK054759 · United States
NIDDK NIH HHS · R37 DK047967 · United States
NHLBI NIH HHS · HL07638 · United States
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