Transgenic rabbit models for biomedical research: Current status, basic methods and future perspectives

Pathology International

Volumn 49, Issue 7, 1999, Pages 583-594

  Fan, Jianglin ^a   Challah, Mireille ^a   Watanabe, Teruo ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Animal model; Atherosclerosis; Bioreactor; Cloning; Gene targeting; Lipid metabolism; Rabbit; Transgene; Transgenic

Indexed keywords

APOLIPOPROTEIN; CD4 ANTIGEN; DNA; GROWTH HORMONE; LIPID; LIPOPROTEIN; LIVER TRIACYLGLYCEROL LIPASE; MESSENGER RNA; PROTEIN; RECOMBINANT DNA;

ANIMAL MODEL; ATHEROSCLEROSIS; BIOREACTOR; GENE EXPRESSION; GENE TARGETING; LIPID METABOLISM; MEDICAL RESEARCH; NONHUMAN; PRIORITY JOURNAL; RABBIT; RECOMBINANT DNA TECHNOLOGY; REVIEW; TRANSGENE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; GENE TARGETING; RABBITS; RESEARCH;

EID: 0032858383     PISSN: 13205463     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1440-1827.1999.00923.x     Document Type: Review

References (93)

1. Hogan T, Constantini F, Lacy E, eds. Manipulating the Mouse Embryo, 2nd edn. Cold Spring Harbor Laboratory, New York, 1994.
2. Gordon J, Scangos G, Plotkin D, Barbosa J, Ruddle F. Genetic transformation of mouse embryos by microinjection of purified DNA. Proc. Natl Acad. Sci. USA 1980; 77: 7380-7384.
3. Jaenisch R. Transgenic animals. Science 1988; 240: 1468-1474.
4. Wight DC, Wagner TE. Transgenic mice: A decade of progress in technology and research. Mutat. Res. 1994; 307: 429-440.
5. Hammer RE, Pursel VG, Rexroad Jr CE et al. Production of transgenic rabbits, sheep and pigs by microinjection. Nature 1985; 315: 680-683.
6. Taylor MJ, Fan J. Transgenic rabbit models for the study of atherosclerosis. Front. Biosci. 1997; 2: 298-308.
7. Hammer RE, Pursel VG, Rexroad Jr CE et al. Genetic engineering of mammalian embryos. J. Anim. Sci. 1986; 63: 269-278.
8. Brinster R, Chen H, Trumbauer M, Yagle K, Palmiter R. Factors affecting the efficiency of introducing foreign DNA into mice by microinjecting eggs. Proc. Natl Acad. Sci. USA 1985; 82: 4438-4442.
9. Wassarman PM, DePamphilis ML, eds. Guide to Techniques in Mouse Development, Academic Press Inc., San Diego, 1993.
10. Chiesa G, Hobbs HH, Koschinsky ML, Lawn RM, Maika SD, Hammer RE. Reconstitution of lipoprotein (a) by infusion of human low density lipoprotein into transgenic mice expressing human apolipoprotein (a). J. Biol. Chem. 1992; 267: 24 369-24 374.
11. Rouy D, Duverger N, Lin SD et al. Apolipoprotein (a) yeast artificial chromosome transgenic rabbits. Lipoprotein (a) assembly with human and rabbit apolipoprotein B. J. Biol. Chem. 1998; 273: 1247-1251.
12. Fan J, Araki M, Wu L et al. Transgenic rabbits expressing human apolipoprotein (a). Circulation 1998; 98 (Suppl.): 1-390 (Abstract).
13. Fan J, Araki M, Wu L et al. Assembly of lipoprotein (a) in transgenic rabbits expressing human apolipoprotein (a). Biochem. Biophys. Res. Commun. 1999; 255: 639-644.
14. Duff GL. Experimental cholesterol arteriosclerosis and its relationship to human arteriosclerosis. Arch. Pathol. 1935; 20: 81-304.
15. Paigen B, Ishida BY, Verstuyft J, Winters RB, Albee D. Atherosclerosis susceptibility differences among progenitors of recombinant inbred strains of mice. Arteriosclerosis 1990; 10: 316-323.
16. Tall AR. Plasma cholesteryl ester transfer protein. J. Lipid Res. 1986; 27: 361-367.
17. Chapman MJ. Animal lipoproteins: Chemistry, structure and comparative aspects. J. Lipid Res. 1980; 21: 789-853.
18. Yamanaka S, Balestra ME, Ferrell LD et al. Apolipoprotein B mRNA-editing protein induces hepatocellular carcinoma and dysplasia in transgenic animals. Proc. Natl Acad. Sci. USA 1995; 92: 8483-8487.
19. Watanabe Y. Serial inbreeding of rabbits with hereditary hyperlipidemia (WHHL-rabbit). Atherosclerosis 1980; 36: 261-268.
20. La Ville A, Turner PR, Pittilo RM et al. Hereditary hyperlipidemia in the rabbit due to overproduction of lipoproteins. I. Biochemical studies. Arteriosclerosis 1987; 7: 105-112.
21. Seddon AM, Woolf N, La Ville A et al. Hereditary hyperlipidemia and atherosclerosis in the rabbit due to overproduction of lipoproteins. II. Preliminary report of arterial pathology. Arteriosclerosis 1987; 7: 113-124.
22. Fan J, Wang J, Bensadoun A et al. Overexpression of hepatic lipase in transgenic rabbits leads to a marked reduction of plasma high density lipoproteins and intermediate density lipoproteins. Proc. Natl Acad. Sci. USA 1994; 91: 8724-8728.
23. Fan J, Mahley RW, Taylor JM. Transgenic rabbits that overexpress hepatic lipase have a marked reduction of plasma high density lipoproteins and intermediate density lipoproteins. In: Woodford FP, Davignon J, Sniderman A, eds. Atherosclerosis X. Elsevier, Amsterdam, 1995; 666-669.
24. Warren RJ, Ebert DL, Mitchell A, Barter PJ. Rabbit hepatic lipase cDNA sequence: Low activity is associated with low messenger RNA levels. J. Lipid Res. 1991; 32: 1333-1339.
25. Taylor M. Transgenic rabbit models for the study of atherosclerosis. Ann. NY Acad. Sci. 1997; 811: 146-151.
26. Sanan DA, Fan J, Bensadoun A, Taylor JM. Hepatic lipase is abundant on both hepatocyte and endothelial cell surfaces in the liver. J. Lipid Res. 1997; 38: 1002-1013.
27. Fan J, McCormick SP, Krauss RM et al. Overexpression of human apolipoprotein B-100 in transgenic rabbits results in increased levels of LDL and decreased levels of HDL. Arterioscler. Thromb. Vasc. Biol. 1995; 15: 1889-1899.
28. Fan J, Ji Z-S, Huang Y et al. Increased expression of apolipoprotein E in transgenic rabbits results in reduced levels of very low density lipoproteins and an accumulation of low density lipoproteins in plasma. J. Clin. Invest. 1998; 101: 2151-2164.
29. Huang Y, Schwendner SW, Rall SC, Sanan D, Mahley RW. Apolipoprotein E2 transgenic rabbits. J. Biol. Chem. 1997; 272: 22 685-22 694.
30. Shen J, Kuhn H, Petho-Shramm A, Chan L. Transgenic rabbits with the integrated human 15-lipoxygenase gene driven by a lysozyme promoter: Macrophage-specific expression and variable positional specificity of the transgenic enzyme. FASEB J. 1995; 9: 1623-1631.
31. Shen J, Herderick E, Cornhill JF et al. Macrophage-mediated 15-lipoxygenase expression protects against atherosclerosis development. J. Clin. Invest. 1996; 98: 2201-2208.
32. Brousseau ME, Santamarina-Fojo S, Zech LA et al. Hyperalphalipoproteinemia in human lecithin cholesterol acyltransferase transgenic rabbits. In vivo apolipoprotein A-I catabolism is delayed in a gene dose-dependent manner. J. Clin. Invest. 1996; 97: 1844-1851.
33. Hoeg JM, Vaisman BL, Demosky Jr SJ et al. Lecithin: cholesterol acyltransferase overexpression generates hyperalpha-lipoproteinemia and a nonatherogenic lipoprotein pattern in transgenic rabbits. J. Biol. Chem. 1996; 271: 4396-4402.
34. Hoeg JM, Santamarina-Fojo S, Berard AM et al. Overexpression of lecithin:cholesterol acyltransferase in transgenic rabbits prevents diet-induced atherosclerosis. Proc. Natl Acad. Sci. USA 1996; 93: 11 448-11 453.
35. Duverger N, Viglietta C, Berthou L et al. Transgenic rabbits expressing human apolipoprotein A-I in the liver. Arterioscler. Thromb. Vasc. Biol. 1996; 16: 1424-1429.
36. Duverger N, Kruth H, Emmanuel F et al. Inhibition of atherosclerosis development in cholesterol-fed human apolipoprotein A-I-transgenic rabbits. Circulation 1996; 94: 713-717.
37. Lebuffe G, Boullier A, Tailleux A et al. Endothelial derived vasorelaxation is impaired in human APO A-I transgenic rabbits. Biochem. Biophys. Res. Commun. 1997; 241: 205-211.
38. Barbagallo C, Fan J, Taylor M, Krauss R. Triglyceride-rich lipoprotein subfractions in cholesterol-fed transgenic rabbits overexpressing human hepatic lipase and apoE. Circulation 1995; 92 (Suppl.): 1-495.
39. Barbagallo C, Fan J, Blanche P, Rizzo M, Taylor J, Krauss R. Overexpression of human hepatic lipase and Apo E in transgenic rabbits attenuates response to dietary cholesterol and alters lipoprotein subclass distributions. Arterioscler. Thromb. Vascul. Biol. 1999; 19: 625-632.
40. Hoeg JM, Kauffman RD, Herderick E, Demonsky Jr SJ, Evans W, Brousseau M. Lecithin:cholesterol acyltransferase requires functional LDL receptors to prevent atherosclerosis. Circulation 1998; 98 (Suppl.): 1-464 (Abstract).
41. Brousseau M, Jian W, Demonsky Jr SJ et al. Correction of hypoalphalipoproteinemia in LDL receptor-deficient rabbits by lecithin:cholesterol acyltransferase. J. Lipid Res. 1998; 39: 1558-1567.
42. James JM, Klevitsky R, Robbins J. Use of the mouse myosin heavy chain promoters in transgenic rabbits. Circulation 1998; 98 (Suppl.): 1-235.
43. Watanabe T, Tokunaga O, Fan J, Shimokama T. Atherosclerosis and macrophages. Acta Pathol. Jpn. 1989; 39: 473-486.
44. Araki M, Fan J, Watanabe T. Immunohistochemical localization of lipoprotein lipase and apolipoprotein E in human atherosclerotic lesions. Acta Histochem. Cytochem. 1998; 31: 485-492.
45. Matsumoto S, Kobayashi T, Katoh M et al. Expression and localization of matrix metalloproteinase-12 in the aorta of cholesterol-fed rabbits. Am. J. Pathol. 1998; 153: 109-119.
46. Libby P. Molecular bases of the acute coronary syndromes. Circulation 1995; 91: 2844-2850.
47. Horvai A, Palinski W, Wu H, Moulton KS, Kalla K, Glass CK. Scavenger receptor A gene regulatory elements target gene expression to macrophages and to foam cells of atherosclerotic lesions. Proc. Natl Acad. Sci. USA 1995; 92: 5391-5395.
48. Bellosta S, Mahley RW, Sanan DA et al. Macrophage-specific expression of human apolipoprotein E reduces atherosclerosis in hypercholesterolemic apolipoprotein E-null mice. J. Clin. Invest. 1995; 96: 2170-2179.
49. Yamamura Y, Kotani M, Chowdhury IH et al. Infection of human CD4+ rabbit cells with HIV: The possibility of the rabbit as model for HIV-1 infection. Int. Immunol. 1991; 3: 1183-1187.
50. Speck RF, Penn ML, Wimmer J et al. Rabbit cells expressing human CD4 and human CCR5 are highly permissive for human immunodeficiency virus type 1 infection. J. Virol. 1998; 72: 5728-5734.
51. Snyder BW, Vitale J, Milos P et al. Developmental and tissue-specific expression of human CD4 in transgenic rabbits. Mol. Reprod. Dev. 1995; 40: 419-428.
52. Dunn CS, Mehtali M, Houdebine LM, Gut JP, Kirn A, Aubertin AM. Human immunodeficiency virus type 1 infection of human CD4-transgenic rabbits. J. Gen. Virol. 1995; 76: 1327-1336.
53. Leno M, Hague BF, Teller R, Kindt TJ. HIV-1 mediates rapid apoptosis of lymphocytes from human CD4 transgenic but not normal rabbits. Virology 1995; 213: 450-454.
54. Knight KL, Spieker-Polet H, Kazdin DS, Oi VT. Transgenic rabbits with lymphocytic leukemia induced by the c-myc oncogene fused with the immunoglobulin heavy chain enhancer. Proc. Natl Acad. Sci. USA 1988; 85: 3130-3134.
55. Sethupathi P, Spieker-Polet H, Polet H, Yam PC, Tunyaplin C, Knight KL. Lymphoid and non-lymphoid tumors in E kappa-myc transgenic rabbits. Leukemia 1994; 8: 2144-2155.
56. Peng X, Olson RO, Christian CB, Lang CM, Kreider JW. Papillomas and carcinomas in transgenic rabbits carrying EJ-ras DNA and cottontail rabbit papillomavirus DNA. J. Virol. 1993; 67: 1698-1701.
57. Peng X, Lang CM, Kreider JW. Methylation of cottontail rabbit papillomavirus DNA and tissue-specific expression in transgenic rabbits. Virus Res. 1995; 35: 101-108.
58. Costa C, Solanes G, Visa J, Bosch F. Transgenic rabbits overexpressing growth hormone develop acromegaly and diabetes mellitus. FASEB J. 1998; 12: 1455-1460.
59. Massoud M, Bischoff R, Dalemans W et al. Production of human proteins in the blood of transgenic animals. Comptes Rendus L Academie Des Sci. Serie III 1990; 311: 275-280.
60. Massoud M, Bischoff R, Dalemans W et al. Expression of active recombinant human alpha 1-antitrypsin in transgenic rabbits. J. Biotech. 1991; 18: 193-203.
61. Buhler TA, Bruyere T, Went DF, Stranzinger G, Burki K. Rabbit beta-casein promoter directs secretion of human interleukin-2 into the milk of transgenic rabbits. Biotechnology 1990; 8: 140-143.
62. Reigo E, Limonta J, Aguilar A et al. Production of transgenic mice and rabbits that carry and express the human tissue plasminogen activator cDNA under the control of a bovine alpha S1 casein promoter. Theriogenology 1993; 39: 1173-1185.
63. Rodriguez A, Castro FO, Aguilar A et al. Expression of active human erythropoietin in the mammary gland of lactating transgenic mice and rabbits. Biol. Res. 1995; 28: 141-153.
64. Massoud M, Attal J, Thepot D et al. The deleterious effects of human erythropoietin gene driven by the rabbit whey acidic protein gene promoter in transgenic rabbits. Reprod. Nutr. Dev. 1996; 36: 555-563.
65. Korhonen VP, Tolvanen M, Hyttinen JM et al. Expression of bovine beta-lactoglobulin human erythropoietin fusion protein in the milk of transgenic mice and rabbits. Eur. J. Biochem. 1997; 245: 482-489.
66. Brem G, Hartl P, Besenfelder U, Wolf E, Zinovieva N, Pfaller R. Expression of synthetic cDNA sequences encoding human insulin-like growth factor-1 (IGF-1) in the mammary gland of transgenic rabbits. Gene 1994; 149: 351-355.
67. Wolf E, Jehle PM, Weber MM et al. Human insulin-like growth factor I (IGF-I) produced in the mammary glands of transgenic rabbits: Yield, receptor binding, mitogenic activity, and effects on IGF-binding proteins. Endocrinology 1997; 138: 307-313.
68. Brem G, Brenig B, Goodman HM et al. Production of transgenic mice, rabbits, and pigs by microinjection into pronuclei. Zychthygience 1985; 20: 251-252.
69. Limonta JM, Castro FO, Martinez R et al. Transgenic rabbits as bioreactors for the production of human growth hormone. J. Biotech. 1995; 40: 49-58.
70. Stromqvist M, Houdebine M, Andersson JO et al. Recombinant human extracellular superoxide dismutase produced in milk of transgenic rabbits. Transgenic Res. 1997; 6: 271-278.
71. McKee C, Gibson A, Dalrymple M, Emslie L, Garner I, Cottingham I. Production of biologically active salmon calcitonin in the milk of transgenic rabbits. Nat. Biotechnol. 1998; 16: 647-651.
72. Weidle UH, Lenz H, Brem G. Genes encoding a mouse monoclonal antibody are expressed in transgenic mice, rabbits and pigs. Gene 1991; 98: 185-191.
73. Spieker-Polet H, Sethupathi P, Yam PC, Knight KL. Rabbit monoclonal antibodies: Generating a fusion partner to produce rabbit-rabbit hybridomas. Proc. Natl Acad. Sci. USA 1995; 92: 9348-9352.
74. Aigner B, Besenfelder U, Seregi J, Frenyo LV, Sahin-Toth T, Brem G. Expression of the murine wild-type tyrosinase gene in transgenic rabbits. Transgenic Res. 1996; 5: 405-411.
75. Brem G, Besenfelder U, Aigner B et al. YAC transgenesis in farm animals: Rescue of albinism in rabbits. Mol. Reprod. Dev. 1996; 44: 56-62.
76. Jeffery G, Brem G, Montoliu L. Correction of retinal abnormalities found in albinism by introduction of a functional tyrosinase gene in transgenic mice and rabbits. Dev. Brain Res. 1997; 99: 95-102.
77. Aigner B, Brem G. Tyrosinase as marker gene and model for screening transgenes in mice and rabbits. Theriogenology 1993; 39: 177.
78. Hafez ESE. Structural and developmental anomalies of rabbit ova. Int. J. Fertil. 1961; 6: 393-407.
79. Hafez ESE. In vitro and in vivo survival of morphologically atypical embryos in rabbits. Nature 1962; 196: 1226-1227.
80. Adams CE. Studies on prenatal mortality in the rabbit, Oryctolagus cuniculus: The effect of transferring varying numbers of eggs. J. Endocrinol. 1962; 24: 471-490.
81. Hafez ESE. Effects of over-crowding in utero on implantation and fetal development in the rabbit. J. Exp. Zool. 1964; 156: 269-287.
82. Manning PJ, Ringler DH, Newcomer CE, eds. The Biology of the Laboratory Rabbits, 2nd edn. Academic Press Inc., San Diego, 1994.
83. Adams CE. The influence of advanced maternal age on embryo survival in the rabbit. In: 5th Internal Congress on Animal Reproduction and Artificial Insemination. Trento, Italy, 1964; 305-308.
84. Moreadith RW, Radford NB. Gene targeting in embryonic stem cells: The new physiology and metabolism. J. Mol Med. 1997; 75: 208-216.
85. Graves KH, Moreadith RW. Derivation and characterization of putative pluripotential embryonic stem cells from preimplantation rabbit embryos. Mot. Reprod. Dev. 1993; 36: 424-433.
86. Du F, Giles JR, Foote RH, Graves KH, Yang X, Moreadith RW. Nuclear transfer of putative rabbit embryonic stem cells leads to normal blastocyst development. J. Reprod. Fertil. 1995; 104: 219-223.
87. Schoonjans L, Albright GM, Li JL, Collen D, Moreadith RW. Pluripotential rabbit embryonic stem (ES) cells are capable of forming overt coat color chimeras following injection into blastocysts. Mol. Reprod. Dev. 1996; 45: 439-443.
88. Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. Viable offspring derived from fetal and adult mammalian cells. Nature 1997; 385: 810-813.
89. Wakayama T, Perry AC, Zuccotti M, Johnson KR, Yanagimachi R. Full-term development of mice from nucleated oocytes injected with cumulus cell nuclei. Nature 1998; 394: 369-374.
90. Kato Y, Tani T, Sotomaru Y et al. Eight calves cloned from somatic cells of a single adult. Science 1998; 282: 2095-2098.
91. Schnieke AE, Kind AJ, Ritchie WA et al. Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science 1997; 278: 2130-2133.
92. Cibelli JB, Stice SL, Golueke PJ et al. Transgenic bovine chimeric offspring produced from somatic cell-derived stem-like cells. Nat. Biotechnol. 1998; 16: 642-646.
93. Yang X, Jiang S, Kovacs A, Foots RH. Nuclear totipotency of cultured rabbit morulae to support full-term development following nuclear transfer. Biol. Reprod. 1992; 47: 636-643.