REDERIVATION BY EMBRYO TRANSFER IN STRAINS OF LABORATORY MICE AND RATS

Rederivation allows laboratory animal populations to be purged from specified pathogens and thus turns these animals to the SPF (specified pathogens free) status. Results of the rederivation of two unique rat strains selected at the Institute of Cytology and Genetics and one mouse strain are presented. The two rat strains are: tame Norway rats and rats with Inherited Stress Induced Arterial Hypertension (ISIAH strain). The ICR mouse strain has been named as abbreviation of the Institute of Cancer Research wherefrom these mice were distributed to laboratories all over the world. The SPF status of the rats after rederivation was confirmed by the method of indicator animals (sentinel animals). The optimized model of rederivation offered here involves a combination of such embryotechnological methods as freezing/cryopreservation of embryos, their washing through the number of fresh volumes of sterile media, growing in vitro for 48 hours, and subsequent transfer into either one or both uterine horns of recipient females. Application of this model to rederivation of ICR mice yielded 39 pups born in an SPF vivarium. It should be noticed that the effectiveness of the procedure met international standards, and characteristic features of phenotype were retained in all the three strains after rederivation.

1. Амстиславский С.Я. Эмбриотехнологические подходы к сохранению исчезающих видов млекопитающих: Дис. … д-ра биол. наук. Новосибирск, 2006, 265 с.

2. Амстиславский С.Я., Маркель А.Л., Якобсон Г.С. Повышение артериального давления у приемных матерей крыс НИСАГ и Вистар: эффект перекрестного воспитания потомства // Росс. физиол. журн. им. Сеченова. 1999. Т. 85. C. 1496–1502.

3. Амстиславский С.Я., Трукшин И.С. Криобанк эмбрионов млекопитающих: выбор приоритетов и оптимальных репродуктивных технологий // Онтогенез. 2010. № 1. С. 19–31.

4. Брусенцев Е.Ю., Напримеров В.А., Амстиславский С.Я. Редеривация как способ очистки лабораторных животных // Вавилов. журн. генет. и селекции. 2011. Т. 15. № 1. С. 102–113.

5. Карих Т.Л., Молокеев А.В., Никулин Л.Г. Генетическая и биологическая характеристика неинбредных мышей колонии ICR // Генетика. 1999. № 3. С. 366–370.

6. Каркищенко Н.Н., Грачева С.В. Руководство по лабораторным животным и альтернативным моделям в биомедицинских исследованиях. М.: Профиль–2С, 2010. 358 c.

7. Маркель А.Л. Генетическая модель индуцированной стрессом артериальной гипертонии // Изв. Ан. СССР. Сер. биол. 1985. Вып. 3. С. 466–469.

8. Сайфитдинова А.Ф. Двумерная флуоресцентная микроскопия для анализа биологических образцов: Уч.-метод. пособие. СПб.: СОЛО, 2008. 72 с.

9. Abbott A. Genetisists prepare for deluge of mutant mice // Nature. 2004. V. 432. P. 541.

10. Artwohl J.E., Purcell J.E., Fortman J.D. The use of cross-foster rederivation to eliminate murine norovirus, Helicobacter spp., and murine hepatitis virus from a mouse colony // J. Am. Assoc. Lab. Anim. Sci. 2008. V. 47. No. 6. P. 19–24.

11. Baze W.B., Steinbach T.J., Fleetwood M.L. et al. Karyomegaly and intranuclear inclusions in the renal tubules of sentinel ICR mice (Mus musculus) // Comp. Med. 2006. V. 56. No. 5. P. 435–438.

12. Bunag R.D. Measurement of blood pressure in rats // Handbook of Hypertension / Ed. W. De Jong. Amsterdam: Elsevier Science, 1984. V. 4. P. 1–12.

13. Carthew P., Wood M.J., Kirby C. Elimination of Sendai (parainfluenza type 1) virus infection from mice by embryo transfer // J. Reprod. Fertil. 1983. V. 69. No. 1. P. 253–257.

14. Chapin R.E., Gulati D.K., Barnes L.H., Teague J.L. The effects of feed restriction on reproductive function in Sprague-Dawley rats // Fundam. Appl. Toxicol. 1993. V. 20. No. 1. P. 23–29.

15. Dinnyes A., Wallage G.A., Rall W.F. Effect of genotype on the efficiency of mouse embryo cryopreservation by vitrifi cation or slow freezing methods // Mol. Reprod. Dev. 1995. V. 40. P. 429–435.

16. Emiliani S., Van den Bergh M., Vannin A.S. et al. Comparison of ethylene glycol, 1,2-propanediol and glycerol for cryopreservation of slow-cooled mouse zygotes, 4-cell embryos and blastocysts // Hum. Reprod. 2000. V. 15. No. 4. P. 905–910.

17. Festing M. F. The choice of animal model and reduction // Altern. Lab. Anim. 2004. V. 32. Suppl. 2. P. 59–64.

18. Fray M.D., Pickard A.R., Harrison M., Cheeseman M.T. Upgrading mouse health and welfare: direct benefi ts of a large-scale rederivation programme // Lab. Anim. 2008. V. 42. No. 2. P. 127–139.

19. Glage S., Dorsch M., Hedrich H.J., Bleich A. Rederivation of Helicobacter hepaticus-infected Mongolian gerbils by Caesarean section and cross-fostering to rats and mice // Lab. Anim. 2007. V. 41. No. 1. P. 103–110.

20. Han M.S., Niwa K., Kasai M. In vivo development of vitrifi ed rat embryos: effects of timing and sites of transfer to recipient females // Biol. Reprod. 2004. V. 70(2). P. 425–429.

21. Handyside A.H., Hunter S. Cell division and death in the mouse blastocyst before implantation // Roux’s Arch. Dev. Biol. 1986. V. 195. P. 519–526.

22. Hardy K., Spanos S. Growth factor expression and function in the human and mouse preimplantation embryo // J. Endocrinol. 2002. V. 172. P. 221–236.

23. Hardy K., Wright C., Rice S. et al. Future developments in assisted reproduction in humans // Reproduction. 2002. V. 123(2). P. 171–183.

24. Hogan B., Constantiny F., Lacy E. Manipulating the mouse embryo. A laboratory manual. N.Y.: Spring Harbor Laboratory, 1986.

25. Holinka C.F., Carlson A.D. Pup attraction to lactating Sprague-Dawley rats // Behav. Biol. 1976. V. 16. No. 4. P. 489–505.

26. Homberger F.R. Enterotropic mouse hepatitis virus // Lab. Anim. 1997. V. 31. No. 2. P. 97–115.

27. Ike F., Bourgade F., Ohsawa K. et al. Lymphocytic choriomeningitis infection undetected by dirty-bedding sentinel monitoring and revealed after embryo transfer of an inbred strain derived from wild mice // Comp. Med. 2007. V. 57. No. 3. P. 272–281.

28. Jones K.H., Senft J.A. An improved method to determine cell viability by simultaneous staining with fl uorescein diacetate-propidium iodide // J. Histochem. Cytochem. 1985. V. 33(1). P. 77–79.

29. Klug S., Merker H.J., Jäckh R. Effects of ethylene glycol and metabolites on in vitro development of rat embryos during organogenesis // Toxicol. In Vitro. 2001. V. 15(6). P. 635–642.

30. Kolbe T., Palme R., Touma C., Rülicke T. Repeated use of surrogate mothers for embryo transfer in the mouse // Biol. Reprod. 2012. V. 86. No. 1. P. 1–6.

31. Leibo S.P., Songsasen N. Cryopreservation of gametes and embryos of non-domestic species // Theriogenology. 2002. V. 57. P. 303–326.

32. Le Monnier A., Join-Lambert O.F., Jaubert F. et al. Invasion of the placenta during murine listeriosis // Infect. Immun. 2006. V. 74(1). P 663–672.

33. Lindstrom K.E., Carbone L.G., Kellar D.E. et al. Soiled bedding sentinels for the detection of fur mites in mice // J. Am. Assoc. Lab. Anim. Sci. 2011. V. 50. No. 1. P. 54–60.

34. Luo C., Zuсiga J., Edison E. et al. Superovulation strategies for 6 commonly used mouse strains // J. Am. Assoc. Lab. Anim. Sci. 2011. V. 50. No. 4. P. 471–478.

35. Macy J.D. Jr., Weir E.C., Compton S.R. Dual infection with Pneumocystis carinii and Pasteurella pneumotropica in B cell-defi cient mice: diagnosis and therapy // Comp. Med. 2000. V. 50. No. 1. P. 49–55.

36. Mahabir E., Bauer B., Schmidt J. Rodent and germplasm trafficking: risks of microbial contamination in a high-tech biomedical world // ILAR J. 2008. V. 49. No. 3. P. 347–355.

37. Mahabir E., Bulian D., Needham J., Schmidt J. Lack of transmission of mouse minute virus (MMV) from in vitro-produced embryos to recipients and pups due to the presence of cumulus cells during the in vitro fertilization process // Biol. Reprod. 2009. V. 81(3). P. 531–538.

38. Marcotte H., Levesque D., Delanay K. et al. Pneumocystis carinii infection in transgenic B cell-defi cient mice // J. Infect. Dis. 1996. V. 173. No. 4. P. 1034–1037.

39. Markel A.L., Maslova L.N., Shishkina G.T. et al. Developmental Infl uences on Blood Pressure Regulation in ISIAH Rats // Handbook of Hypertension / Eds R. McCarty, D.A. Blizard, R.L. Chevalier. Elsevier Science, 1999. V. 19. P. 493–526.

40. Miyamoto H., Ishibashi T. Survival of frozen-thawed mouse and rat embryos in the presence of ethylene glycol // J. Reprod. Fertil. 1977. V. 50(2). P. 373–375.

41. Mohr L., Trounson A. The use of fl uorescein diacetate to assess embryo viability in the mouse // J. Reprod. Fert. 1980. V. 58. P. 189–196.

42. Moore K., Bonilla A.Q. Cryopreservation of mammalian embryos: the state of the art // Annu. Rev. Biomed. Sci. 2006. V. 8. P. 19–32.

43. Morrell J.M. Techniques of embryo transfer and facility decontamination used to improve the health and welfare of transgenic mice // Lab. Anim. 1999. V. 33. No. 3. P. 201–206.

44. Naumenko E.V., Popova N.K., Nikulina E.M. et al. Behavior, adrenocortical activity, and brain monoamines in Norway rats selected for reduced aggressiveness towards man // Pharmacol. Biochem. Behav. 1989. V. 33. P. 85–91.

45. Nicklas W., Baneux P., Boot R. et al. FELASA (Federation of European Laboratory Animal Science Associations Working Group on Health Monitoring of Rodent and Rabbit Colonies). Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units // Lab. Anim. 2002. V. 36. No. 1. P. 20–42.

46. Omar Farouk F.N., Stott D., Vlad M. Mouse embryo co-culture with autologous cumulus cells and fetal development post-embryo transfer // Anim. Sci. J. 2011. V. 82. No. 3. P. 420–427.

47. Pfaff R.T., Agca Y., Liu J. et al. Cryobiology of rat embryos I: determination of zygote membrane permeability coefficients for water and cryoprotectants, their activation energies, and the development of improved cryopreservation methods // Biol. Reprod. 2000. V. 63(5). P. 1294–302.

48. Plyusnina I.Z., Oskina I.N. Behavioral and adrenocortical responses to open-fi eld test in rats selected for reduced aggressiveness toward humans // Physiol. Behav. 1997. V. 61(3). P. 381–385.

49. Plyusnina I.Z., Oskina I.N., Tibeikina M.A., Popova N.K. Cross-fostering effects on weight, exploratory activity, acoustic startle refl ex and corticosterone stress response in Norway gray rats selected for elimination and for enhancement of aggressiveness towards human // Behav. Genet. 2009. V. 39. P. 202–212.

50. Plyusnina I.Z., Solov’eva M.Y., Oskina I.N. Effect of domestication on aggression in gray Norway rats // Behav. Genet. 2011. V. 41. No. 4. P. 583–592.

51. Rall W.F., Schmidt P.M., Lin X. et al. Factors affecting the effi ciency of embryo cryopreservation and rederivation of rat and mouse models // ILAR J. 2000. V. 41. No. 4. P. 221–227.

52. Rapp J.P. Genetic analysis of inherited hypertension in the rat // Physiol. Rev. 2000. V. 80(1). P. 135–172.

53. Reuter J.D., Dysko R.C. Quality assurance/surveillance monitoring programs for rodent colonies // Laboratory animal medicine and management / Eds J.D. Reuter, M.A. Suckow. www.ivis.org, Ithaca, 2003. N.Y., USA. P. 1–11.

54. Schmidt H.M., Schiewe M.C., Wildt D.E. The genotypic response of mouse embryos to multiple freezing variables // Biol. Reprod. 1987. V. 37. P. 1121–1128.

55. Sheсk W.R. Role of housing modalities on management and surveillance strategies for adventitious agents of rodents // ILAR J. 2008. V. 49. No. 3. P. 316–325.

56. Stringfellow D.A. Recommendation for the sanitary handling of in vivo-derived embryos // Manual of the International Embryo Transfer Society. 1998. P. 79–84.

57. Suzuki H., Yorozu K., Watanabe T. et al. Rederivation of mice by means of in vitro fertilization and embryo transfer // Exp. Anim. 1996. V. 45. No. 1. P. 33–38.

58. Taft R.A. Virtues and limitations of the preimplantation mouse embryo as a model system // Theriogenology. 2008. 69(1). P. 10–16.

59. Van Keuren M.L., Saunders T.L. Rederivation of transgenic and gene-targeted mice by embryo transfer // Transgenic Res. 2004. V. 13. No. 4. P. 363–371.

60. Waterston R., Lindblad-Toh K., Birney E. et al. Initial sequencing and comparative analysis of the mouse genome // Nature. 2002. V. 420. P. 520–562.

61. Watson J., Thompson K.N., Feldman S.H. Successful rederivation of contaminated immunocompetent mice using neonatal transfer with iodine immersion // Comp. Med. 2005. V. 55. No. 5. P. 465–469.

62. Weisbroth S.H., Peters R., Riley L.K., Sheсk W. Microbiological assessment of laboratory rats and mice // ILAR. 1998. V. 39(4). P. 272–290.

63. Wiebold J.L., Becker W.C. Inequality in function of the right and left ovaries and uterine horns of the mouse // J. Reprod. Fert. 1987. V. 79. P. 125–134.

64. Wilkinson J.M., Halley S., Towers P.A. Comparison of male reproductive parameters in three rat strains: Dark Agouti, Sprague-Dawley and Wistar // Lab. Anim. 2000. V. 34. P. 70–75.

65. Williams C., Greenstein G., Kopec A., Hargaden M. Microbiological evaluation of a newly constructed animal facility // Contemp. Top. Lab. Anim. Sci. 2005. V. 44. No. 2. P. 7–11.

66. Yeom S.C., Yu S.A., Choi E.Y. et al. Prevalence of Helicobacter hepaticus, murine norovirus, and Pneumocystis carinii and eradication effi cacy of cross-fostering in genetically engineered mice // Exp. Anim. 2009. V. 58. No. 5. P. 497–504.