In vivo oocyte IGF-1 priming increases inner cell mass proliferation of in vitro-formed bovine blastocysts

Theriogenology

Volumn 78, Issue 3, 2012, Pages 517-527

  Velazquez, M A ^a,b,d   Hadeler, K G ^a   Herrmann, D ^a   Kues, W A ^a   Remy B ^c   Beckers, J F ^c   Niemann, H ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b UNIVERSIDAD AUTÓNOMA DE CAMPECHE   (Mexico)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Cellular allocation; Growth factor; Preimplantation embryo; Superovulation

Indexed keywords

GLUCOSE TRANSPORTER; MESSENGER RNA; PROTEIN P53; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR;

ANIMAL; ANIMAL DISEASE; ARTICLE; BLASTOCYST; CATTLE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; DRUG EFFECT; EMBRYO CULTURE; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION; GENETICS; MORULA; OOCYTE; OVARY; PRENATAL DEVELOPMENT;

ANIMALS; BLASTOCYST; CATTLE; CELL PROLIFERATION; EMBRYO CULTURE TECHNIQUES; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; INSULIN-LIKE GROWTH FACTOR I; MORULA; OOCYTES; OVARY; RECEPTOR, IGF TYPE 1; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEIN P53;

BOVINAE;

EID: 84863481564     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2012.02.034     Document Type: Article

References (58)

1. Laron Z. Insulin-like growth factor-1 (IGF-1): a growth hormone. J Clin Pathol Mol Pathol 2001, 54:311-316.
2. Chan S.J., Cao Q.P., Steiner D.F. Evolution of the insulin superfamily: cloning of a hybrid insulin/insulin-like growth factor cDNA from amphioxus. Proc Natl Acad Sci U S A 1990, 87:9319-9323.
3. Velazquez M.A., Zaraza J., Oropeza A., Webb R., Niemann H. The role of IGF1 in the in vivo production of bovine embryos from superovulated donors. Reproduction 2009, 137:161-180.
4. Benito M., Valverde A.M., Lorenzo M. IGF-I: a mitogen also involved in differentiation processes in mammalian cells. Int J Biochem Cell Biol 1996, 28:499-510.
5. Vincent A.M., Feldman E.L. Control of cell survival by IGF signaling pathways. Growth Horm IGF Res 2002, 12:193-197.
6. Velazquez M.A., Hermann D., Kues W.A., Niemann H. Increased apoptosis in bovine blastocysts exposed to high levels of IGF1 is not associated with downregulation of the IGF1 receptor. Reproduction 2011, 141:91-103.
7. Oropeza A., Wrenzycki C., Herrmann D., Hadeler K.G., Niemann H. Improvement of the developmental capacity of oocytes from prepubertal cattle by intraovarian insulin-like growth factor-I application. Biol Reprod 2004, 70:1634-1643.
8. Zaraza J., Oropeza A., Velazquez M.A., Korsawe K., Herrmann D., Carnwath J.W., et al. Developmental competence and mRNA expression of preimplantation in vitro-produced embryos from prepubertal and postpubertal cattle and their relationship with apoptosis after intraovarian administration of IGF-1. Theriogenology 2010, 74:75-89.
9. Velazquez M.A., Hadeler K.G., Herrmann D., Kues W.A., Ulbrich S.E., Meyer H.H.D., et al. In vivo oocyte developmental competence is reduced in lean but not in obese superovulated dairy cows after intraovarian administration of IGF1. Reproduction 2011, 142:41-52.
10. Rizos D., Ward F., Duffy P., Boland M.P., Lonergan P. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev 2002, 61:234-248.
11. Siddiqui M.A., Gastal E.L., Gastal M.O., Almamun M., Beg M.A., Ginther O.J. Relationship of vascular perfusion of the wall of the preovulatory follicle to in vitro fertilisation and embryo development in heifers. Reproduction 2009, 137:689-697.
12. Wang T.H., Chang C.L., Wu H.M., Chiu Y.M., Chen C.K., Wang H.S. Insulin-like growth factor-II (IGF-II), IGF-binding proteins-3 (IGFBP-3), and IGFBP-4 in follicular fluid are associated with oocyte maturation and embryo development. Fertil Steril 2006, 86:1392-1401.
13. Lloyd R.E., Romar R., Matás C., Gutiérrez-Adán A., Holt W.V., Coy P. Effects of oviductal fluid on the development, quality, and gene expression of porcine blastocysts produced in vitro. Reproduction 2009, 137:679-687.
14. Niemann H., Wrenzycki C., Lucas-Hahn A., Brambrink T., Kues W.A., Carnwath J.W. Gene expression patterns in bovine in vitro-produced and nuclear transfer-derived embryos and their implications for early development. Cloning Stem Cells 2002, 4:29-38.
15. Schaetzlein S., Lucas-Hahn A., Lemme E., Kues W.A., Dorsch M., Manns M.P., et al. Telomere length is reset during early mammalian embryogenesis. Proc Natl Acad Sci U S A 2004, 101:8034-8038.
16. Thomas F.H., Campbell B.K., Armstrong D.G., Telfer E.E. Effects of IGF-I bioavailability on bovine preantral follicular development in vitro. Reproduction 2007, 133:1121-1128.
17. Chi M.M., Schlein A.L., Moley K.H. High insulin-like growth factor 1 (IGF-1) and insulin concentrations trigger apoptosis in the mouse blastocyst via down-regulation of the IGF-1 receptor. Endocrinology 2000, 141:4784-4792.
18. Pinto A.B., Schlein A.L., Moley K.H. Preimplantation exposure to high insulin-like growth factor I concentrations results in increased resorption rates in vivo. Hum Reprod 2002, 17:457-462.
19. Eng G.S., Sheridan R.A., Wyman A., Chi M.M., Bibee K.P., Jungheim E.S., et al. AMP kinase activation increases glucose uptake, decreases apoptosis, and improves pregnancy outcome in embryos exposed to high IGF-I concentrations. Diabetes 2007, 56:2228-2234.
20. Stringfellow D.A., Seidel S.M. Manual of the international embryo transfer society 1998, 172. International Embryo Transfer Society (IETS), Savoy, IL, USA.
21. Kues A., Sudheer S., Herrmann D., Carnwath J.W., Havlicek V., Besenfelder U., et al. Genome-wide expression profiling reveals distinct clusters of transcriptional regulation during bovine preimplantation development in vivo. Proc Natl Acad Sci U S A 2008, 105:19768-19773.
22. Niemann H., Carnwath J.W., Herrmann D., Wieczorek G., Lemme E., Lucas-Hahn A., et al. DNA methylation patterns reflect epigenetic reprogramming in bovine embryos. Cell Reprog 2010, 12:33-42.
23. Block J., Wrenzycki C., Niemann H., Herrmann D., Hansen P.J. Effects of insulin-like growth factor-1 on cellular and molecular characteristics of bovine blastocysts produced in vitro. Mol Reprod Dev 2008, 75:895-903.
24. Lighten A.D., Moore G.E., Winston R.M., Hardy K. Routine addition of human insulin-like growth factor-I ligand could benefit clinical in-vitro fertilization culture. Hum Reprod 1998, 13:3144-3150.
25. Kim S., Lee G.S., Lee S.H., Kim H.S., Jeong Y.W., Kim J.H., et al. Embryotropic effect of insulin-like growth factor (IGF)-I and its receptor on development of porcine preimplantation embryos produced by in vitro fertilization and somatic cell nuclear transfer. Mol Reprod Dev 2005, 72:88-97.
26. Smith R.M., Garside W.T., Aghayan M., Shi C.Z., Shah N., Jarett L., et al. Mouse preimplantation embryos exhibit receptor-mediated binding and transcytosis of maternal insulin-like growth factor I. Biol Reprod 1993, 49:1-12.
27. Leppens-Luisier G., Urner F., Sakkas D. Facilitated glucose transporters play a crucial role throughout mouse preimplantation embryo development. Hum Reprod 2001, 16:1229-1236.
28. Purcell S.H., Moley K.H. Glucose transporters in gametes and preimplantation embryos. Trends Endocrinol Metab 2009, 20:483-489.
29. Augustin R., Pocar P., Navarrete-Santos A., Wrenzycki C., Gandolfi F., Niemann H., et al. Glucose transporter expression is developmentally regulated in in vitro derived bovine preimplantation embryos. Mol Reprod Dev 2001, 60:370-376.
30. Zheng P., Vassena R., Latham K.E. Effects of in vitro oocyte maturation and embryo culture on the expression of glucose transporters, glucose metabolism and insulin signaling genes in rhesus monkey oocytes and preimplantation embryos. Mol Hum Reprod 2007, 13:361-371.
31. Carayannopoulos M.O., Chi M.M., Cui Y., Pingsterhaus J.M., McKnight R.A., Mueckler M., et al. GLUT8 is a glucose transporter responsible for insulin-stimulated glucose uptake in the blastocyst. Proc Natl Acad Sci U S A 2000, 97:7313-7318.
32. Pinto A.B., Carayannopoulos M.O., Hoehn A., Dowd L., Moley K.H. Glucose transporter 8 expression and translocation are critical for murine blastocyst survival. Biol Reprod 2002, 66:1729-1733.
33. Choi Y.S., Kim S.H., Ku S.Y., Jee B.C., Suh C.S., Choi Y.M., et al. Efficacy of ER-α polymorphisms and the intrafollicular IGF system for predicting pregnancy in IVF-ET patients. Gynecol Obstet Invest 2009, 67:73-80.
34. Fried G., Remaeus K., Harlin J., Krog E., Csemiczky G., Aanesen A., et al. Inhibin B predicts oocyte number and the ratio IGF-I/IGFBP-1 may indicate oocyte quality during ovarian hyperstimulation for in vitro fertilization. J Assist Reprod Genet 2003, 20:167-176.
35. Koo D.B., Kang Y.K., Choi Y.H., Park J.S., Kim H.N., Oh K.B., et al. Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biol Reprod 2002, 67:487-492.
36. Amarnath D., Kato Y., Tsunoda Y. Cryopreservation of bovine somatic cell nuclear-transferred blastocysts: effect of developmental stage. J Reprod Dev 2004, 50:593-598.
37. Li G.P., Bunch T.D., White K.L., Aston K.I., Meerdo L.N., Pate B.J., et al. Development, chromosomal composition, and cell allocation of bovine cloned blastocyst derived from chemically assisted enucleation and cultured in conditioned media. Mol Reprod Dev 2004, 68:189-197.
38. Byrne A.T., Southgate J., Brison D.R., Leese H.J. Regulation of apoptosis in the bovine blastocyst by insulin and the insulin-like growth factor (IGF) superfamily. Mol Reprod Dev 2002, 62:489-495.
39. Stadtmauer L.A., Toma S.K., Riehl R.M., Talbert L.M. Metformin treatment of patients with polycystic ovary syndrome undergoing in vitro fertilization improves outcomes and is associated with modulation of the insulin-like growth factors. Fertil Steril 2001, 75:505-509.
40. Choi Y.S., Ku S.Y., Jee B.C., Suh C.S., Choi Y.M., Kim J.G., et al. Comparison of follicular fluid IGF-I, IGF-II, IGFBP-3, IGFBP-4 and PAPP-A concentrations and their ratios between GnRH agonist and GnRH antagonist protocols for controlled ovarian stimulation in IVF-embryo transfer patients. Hum Reprod 2006, 21:2015-2021.
41. Ferrari B., Pezzuto A., Barusi L., Coppola F. Gonadotropin-releasing hormone antagonists increase follicular fluid insulin-like growth factor-I and vascular endothelial growth factor during ovarian stimulation cycles. Gynecol Endocrinol 2006, 22:289-296.
42. Hidalgo C., Díez C., Duque P., Prendes J.M., Rodríguez A., Goyache F., et al. Oocytes recovered from cows treated with retinol become unviable as blastocysts produced in vitro. Reproduction 2005, 129:411-421.
43. Watkins A.J., Fleming T.P. Blastocyst environment and its influence on offspring cardiovascular health: the heart of the matter. J Anat 2009, 215:52-59.
44. Zhang S., Rattanatray L., McMillen I.C., Suter C.M., Morrison J.L. Periconceptional nutrition and the early programming of a life of obesity or adversity. Prog Biophys Mol Biol 2011, 106:307-314.
45. Williams C.L., Teeling J.L., Perry V.H., Fleming T.P. Mouse maternal systemic inflammation at the zygote stage causes blunted cytokine responsiveness in lipopolysaccaride-challenged adult offspring. BMC Biol 2011, 9:49.
46. Koch J.M., Wilmoth T.A., Wilson M.E. Periconceptional growth hormone treatment alters fetal growth and development in lambs. J Anim Sci 2010, 88:1619-1625.
47. Costine B.A., Inskeep E.K., Wilson M.E. Growth hormone at breeding modifies conceptus development and postnatal growth in sheep. J Anim Sci 2005, 83:810-815.
48. Melnik B.C. Milk-the promoter of chronic western diseases. Med Hypotheses 2009, 72:631-639.
49. Key T.J. Diet, insulin-like growth factor-1 and cancer risk. Proc Nutr Soc 2011, 70:385-388.
50. Melnik B.C., John S.M., Schmitz G. Over-stimulation of insulin/IGF-1 signaling by western diet may promote diseases of civilization: lessons learnt from Laron syndrome. Nutr Metab 2011, 8:41.
51. Adams G.P., Pierson R.A. Bovine model for study of ovarian follicular dynamics in humans. Theriogenology 1995, 43:113-120.
52. Campbell B.K., Souza C., Gong J., Webb R., Kendall N., Marsters P., et al. Domestic ruminants as models for the elucidation of the mechanisms controlling ovarian follicle development in humans. Reprod 2003, 61(Suppl):429-443.
53. Mihm M., Evans A.C.O. Mechanisms for dominant follicle selection in monovulatory species: a comparison of morphological, endocrine and intraovarian events in cows, mares and women. Reprod Domest Anim 2008, 43(Suppl 2):48-56.
54. Adjaye J., Herwig R., Brink T.C., Herrmann D., Greber B., Sudheer S., et al. Conserved molecular portraits of bovine and human blastocysts as a consequence of the transition from maternal to embryonic control of gene expression. Physiol Genomics 2007, 31:315-327.
55. Xie D., Chen C.C., Ptaszek L.M., Xiao S., Cao X., Fang F., et al. Rewirable gene regulatory networks in the preimplantation embryonic development of three mammalian species. Genome Res 2010, 20:804-815.
56. Ménézo Y.J., Hérubel F. Mouse and bovine models for human IVF. Reprod Biomed Online 2002, 4:170-175.
57. Bianchi P.Hd.M., Serafini P., da Rocha A.M., Hassun P.A., da Motta E.L.A., Baruselli P.S., Baracat E.C. Follicular waves in the human ovary: a new physiological paradigm for novel ovarian stimulation protocols. Reprod Sci 2010, 17:1067-1076.
58. Baerwald A.R., Adams G.P., Pierson R.A. Ovarian antral folliculogenesis during the human menstrual cycle: a review. Hum Reprod Update 2012, 18:73-91.