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

Biology of Reproduction

Volumn 81, Issue 3, 2009, Pages 531-538

  Mahabir, Esther ^a   Bulian, D ^a   Needham, J ^b,c   Schmidt, J ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b Microbiology Laboratories   (United Kingdom)

^c NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Assisted reproductive technology; Embryo; In vitro fertilization; Mouse; Mouse minute virus

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CUMULUS CELL; EMBRYO; EMBRYO TRANSFER; ENZYME ASSAY; FERTILIZATION IN VITRO; IN VITRO STUDY; MOUSE; NONHUMAN; OOCYTE; PARVOVIRUS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PUP (RODENT); RECIPIENT; SCANNING ELECTRON MICROSCOPY; SEROLOGY; TISSUE CULTURE; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; CUMULUS CELLS; EMBRYO TRANSFER; EMBRYO, MAMMALIAN; FEMALE; FERTILIZATION IN VITRO; MALE; MICE; MICE, INBRED C3H; MINUTE VIRUS OF MICE; MODELS, BIOLOGICAL; PARVOVIRIDAE INFECTIONS; PREGNANCY; TRANSPLANTATION; TREATMENT OUTCOME; VIRUS REPLICATION;

MINUTE VIRUS OF MICE; MURINAE; MUS;

EID: 69849096476     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.077024     Document Type: Article

References (48)

1. Marschall S, Huffstadt U, Balling R, Hrabe de Angelis M. Reliable recovery of inbred mouse lines using cryopreserved spermatozoa. Mamm Genome 1999; 10:773-776. (Pubitemid 29390552)
2. Glenister PH, Whittingham DG, Wood MJ. Genome cryopreservation: a valuable contribution to mammalian genetic research. Genet Res 1990; 56: 253-258.
3. Shaw JM, Nakagata N. Cryopreservation of transgenic mouse lines. Methods Mol Biol 2002; 180:207-228.
4. Suzuki H, Yorozu K, Watanabe T, Nakura M, Adachi J. Rederivation of mice by means of in vitro fertilization and embryo transfer. Exp Anim 1996; 45:33-38. (Pubitemid 126419606)
5. Sztein JM, Farley JS, Mobraaten LE. In vitro fertilization with cryopreserved inbred mouse sperm. Biol Reprod 2000; 63:1774-1780.
6. Crawford LV. A minute virus of mice. Virology 1966; 29:605-612.
7. Parker JC, Collins MJ Jr, Cross SS, Rowe WP. Minute virus of mice, II: prevalence, epidemiology, and occurrence as a contaminant of transplanted tumors. J Natl Cancer Inst 1970; 45:305-310.
8. Harris RE, Coleman PH, Morahan PS. Stability of minute virus of mice to chemical and physical agents. Appl Microbiol 1974; 28:351-354.
9. Boschetti N, Wyss K, Mischler A, Hostettler T, Kempf C. Stability of minute virus of mice against temperature and sodium hydroxide. Biologicals 2003; 31:181-185. (Pubitemid 37006336)
10. Neighbour PA. Studies on the susceptibility of the mouse preimplantation embryo to infection with cytomegalovirus. J Reprod Fertil 1978; 54:15-20.
11. Reetz IC, Wullenweber-Schmidt M, Kraft V, Hedrich HJ. Rederivation of inbred strains of mice by means of embryo transfer. Lab Anim Sci 1988; 38:696-701.
12. Carthew P, Wood MJ, Kirby C. Pathogenicity of mouse hepatitis virus for preimplantation mouse embryos. J Reprod Fertil 1985; 73:207-213. (Pubitemid 15150586)
13. Zeichner SL, Plotkin SA. Mechanisms and pathways of congenital infections. Clin Perinatol 1988; 15:163-188.
14. Vanroose G, Nauwynck H, Van Soom A, Vanopdenbosch E, de Kruif A. Replication of cytopathic and noncytopathic bovine viral diarrhea virus in zona-free and zona-intact in vitro-produced bovine embryos and the effect on embryo quality. Biol Reprod 1998; 58:857-866. (Pubitemid 28117088)
15. Vanroose G, Nauwynck H, Van Soom A, Vanopdenbosch E, de Kruif A. Effect of bovine herpesvirus-1 or bovine viral diarrhea virus on development of in vitro-produced bovine embryos. Mol Reprod Dev 1999; 54:255-263. (Pubitemid 29463425)
16. Van Keuren ML, Saunders TL. Rederivation of transgenic and genetargeted mice by embryo transfer. Transgenic Res 2004; 13:363-371.
17. Stringfellow DA, Seidel SM (eds.). Manual of the International Embryo Transfer Society. Savoy: International Embryo Transfer Society; 1998.
18. Mahabir E, Bulian D, Needham J, Mayer A, Mateusen B, Soom AV, Nauwynck H, Schmidt J. Transmission of mouse minute virus (MMV) but not mouse hepatitis virus (MHV) following embryo transfer with experimentally exposed in vivo-derived embryos. Biol Reprod 2007; 76: 189-197. (Pubitemid 46219332)
19. Spearman C. The method of 'right and wrong cases' (constant stimuli) without Gauss's formulae. Br J Psychol 1908; 2:227-242.
20. Kaerber G. Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Arch Exp Pathol Pharmakol 1931; 162:480-483.
21. Nicklas W, Baneux P, Boot R, Decelle T, Deeny AA, Fumanelli M, Illgen- Wilcke B. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab Anim 2002; 36: 20-42. (Pubitemid 34073119)
22. Kraft V, Blanchet HM, Boot R, Deeny A, Hansen AK, Hem A, van Herck H, Kunstyr I, Needham JR, Nicklas W, Perrot A, Rehbinder C, et al. Recommendations for the health monitoring of mouse, rat, hamster, guineapig and rabbit breeding colonies: report of the Federation of European Laboratory Animal Science Associations (FELASA) Working Group on Animal Health accepted by the FELASA Board of Management November 1992. Lab Anim 1994; 28:1-12. (Pubitemid 24040203)
23. Quinn P, Kerin JF, Warnes GM. Improved pregnancy rate in human in vitro fertilization with the use of a medium based on the composition of human tubal fluid. Fertil Steril 1985; 44:493-498. (Pubitemid 16214173)
24. Lawitts JA, Biggers JD. Overcoming the 2-cell block by modifying standard components in a mouse embryo culture medium. Biol Reprod 1991; 45:245-251.
25. Nagy A, Gertsenstein M, Vintersten K, Behringer R. Manipulating the mouse embryo. New York: Cold Spring Harbor Laboratory Press; 2003.
26. Mahabir E, Jacobsen K, Brielmeier M, Peters D, Needham J, Schmidt J. Mouse antibody production test: can we do without it? J Virol Methods 2004; 120:239-245.
27. Bootz F, Sieber I, Popovic D, Tischhauser M, Homberger FR. Comparison of the sensitivity of in vivo antibody production tests with in vitro PCRbased methods to detect infectious contamination of biological materials. Lab Anim 2003; 37:341-351. (Pubitemid 37297044)
28. Mahabir E, Bulian D, Schmoller R, Needham J, Schmidt J. Production of virus-free seronegative pups from murine embryos arising from in vitro fertilization with mouse minute virus-exposed spermatozoa. Biol Reprod 2008; 78:53-58.
29. Besselsen DG, Romero-Aleshire MJ, Munger SJ, Marcus EC, Henderson KS, Wagner AM. Embryo transfer rederivation of C.B-17/Icr-Prkdc(scid) mice experimentally infected with mouse parvovirus 1. Comp Med 2008; 58:353-359.
30. Nogues C, Ponsa M, Vidal F, Boada M, Egozcue J. Effects of aging on the zona pellucida surface of mouse oocytes. J In Vitro Fert Embryo Transf 1988; 5:225-229. (Pubitemid 18245786)
31. Cortez Romero C, Fieni F, Roux C, Russo P, Guibert JM, Guiguen F, Chebloune Y, Pepin M, Pellerin JL. Detection of ovine lentivirus in the cumulus cells, but not in the oocytes or follicular fluid, of naturally infected sheep. Theriogenology 2006; 66:1131-1139. (Pubitemid 44232939)
32. Ali Al Ahmad MZ, Fieni F, Martignat L, Chatagnon G, Baril G, Bouvier F, Chebloune Y. Proviral DNA of caprine arthritis encephalitis virus (CAEV) is detected in cumulus oophorus cells but not in oocytes from naturally infected goats. Theriogenology 2005; 64:1656-1666. (Pubitemid 41338631)
33. Fray MD, Prentice H, Clarke MC, Charleston B. Immunohistochemical evidence for the localization of bovine viral diarrhea virus, a single-stranded RNA virus, in ovarian oocytes in the cow. Vet Pathol 1998; 35: 253-259. (Pubitemid 128473340)
34. Tsuboi T, Kanazawa Y, Syoji T, Tokuhisa S. Growth activity of bovid herpesvirus 1 in bovine follicular oocytes with cumulus cells. J Vet Med Sci 1992; 54:1179-1181.
35. Agca Y, Bauer BA, Johnson DK, Critser JK, Riley LK. Detection of mouse parvovirus in Mus musculus gametes, embryos, and ovarian tissues by polymerase chain reaction assay. Comp Med 2007; 57:51-56. (Pubitemid 46328519)
36. Mahabir E, Bauer B, Schmidt J. Rodent and germplasm trafficking: risks of microbial contamination in a high-tech biomedical world. ILAR J 2008; 49:347-355.
37. Joyce CL, Mack SR, Anderson RA, Zaneveld LJ. Effect of hyaluronidase, beta-glucuronidase and beta-N-acetylglucosaminidase inhibitors on sperm penetration of the mouse oocyte. Biol Reprod 1986; 35:336-346.
38. Lin Y, Mahan K, Lathrop WF, Myles DG, Primakoff P. A hyaluronidase activity of the sperm plasma membrane protein PH-20 enables sperm to penetrate the cumulus cell layer surrounding the egg. J Cell Biol 1994; 125:1157-1163. (Pubitemid 24177217)
39. Cross PC, Brinster RL. In vitro development of mouse oocytes. Biol Reprod 1970; 3:298-307.
40. Pavlok A, McLaren A. The role of cumulus cells and the zona pellucida in fertilization of mouse eggs in vitro. J Reprod Fertil 1972; 29:91-97.
41. Stanger JD, Quinn P. Fertilization of cumulus-free, zona-intact mouse ova in vitro at high and low sperm concentrations. Gamete Res 1982; 5:61-70.
42. Cox JF, Hormazabal J, Santa Maria A. Effect of the cumulus on in vitro fertilization of bovine matured oocytes. Theriogenology 1993; 40:1259-1267. (Pubitemid 2017706)
43. Tao T, Robichaud A, Nadeau S, Savoie R, Gallant B, Ouellette R. Effect of cumulus cell removal on the fertilization and the day 3 embryo quality in human IVF. In: Grundy K (ed.), Proceedings of the 18th World Congress on Fertility and Sterility (IFFS 2004), Montreal, Canada 23-28 May 2004. Amsterdam: Elsevier; 2004:135-138. International Congress Series 1271.
44. Hashlamoun LA, Killian GJ. Effects of timing of ovum recovery, cumulus cells, sperm preincubation time, and pH on in vitro fertilization in C57BL/ 6 mice. Arch Androl 1985; 15:159-171.
45. Vergara GJ, Irwin MH, Moffatt RJ, Pinkert CA. In vitro fertilization in mice: strain differences in response to superovulation protocols and effect of cumulus cell removal. Theriogenology 1997; 47:1245-1252.
46. Kim E, Yamashita M, Kimura M, Honda A, Kashiwabara S, Baba T. Sperm penetration through cumulus mass and zona pellucida. Int J Dev Biol 2008; 52:677-682.
47. Vanderhyden BC, Armstrong DT. Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol Reprod 1989; 40:720-728.
48. Galeati G, Modina S, Lauria A, Mattioli M. Follicle somatic cells influence pig oocyte penetrability and cortical granule distribution. Mol Reprod Dev 1991; 29:40-46.