Maternally-inherited Grb10 reduces placental size and efficiency

Developmental Biology

Volumn 337, Issue 1, 2010, Pages 1-8

  Charalambous, Marika ^a,b   Cowley, Michael ^a   Geoghegan, Fleur ^a   Smith, Florentia M ^a   Radford, Elizabeth J ^b   Marlow, Benjamin P ^a   Graham, Christopher F ^c   Hurst, Laurence D ^a   Ward, Andrew ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Adapter protein; Cell signalling; Epigenetics; Genomic imprinting; Growth factor receptor bound protein; Growth regulation; IGF; Insulin like growth factor; Mouse; Placenta

Indexed keywords

GROWTH FACTOR RECEPTOR BOUND PROTEIN 10; SOMATOMEDIN B;

ALLELE; ANIMAL TISSUE; ARTICLE; BIRTH; BODY SIZE; CONTROLLED STUDY; EXTRACHROMOSOMAL INHERITANCE; FETUS GROWTH; GENE DISRUPTION; GENE FUNCTION; GENOME IMPRINTING; GRANDPARENT; MAMMAL; MOUSE; MUTANT; NONHUMAN; ORGAN SIZE; PLACENTA; PLACENTA DEVELOPMENT; PREGNANCY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION;

MAMMALIA; MUS;

EID: 70450224442     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.10.011     Document Type: Article

References (46)

1. Arnaud P., Monk D., Hitchins M., Gordon E., Dean W., Beechey C.V., Peters J., Craigen W., Preece M., Stanier P., Moore G.E., and Kelsey G. Conserved methylation imprints in the human and mouse GRB10 genes with divergent allelic expression suggests differential reading of the same mark. Hum. Mol. Genet. 12 (2003) 1005-1019
2. Bruning J.C., Gautam D., Burks D.J., Gillette J., Schubert M., Orban P.C., Klein R., Krone W., Muller-Wieland D., and Kahn C.R. Role of brain insulin receptor in control of body weight and reproduction. Science 289 (2000) 2122-2125
3. Burks D.J., Font de Mora J., Schubert M., Withers D.J., Myers M.G., Towery H.H., Altamuro S.L., Flint C.L., and White M.F. IRS-2 pathways integrate female reproduction and energy homeostasis. Nature 407 (2000) 377-382
4. Carney E.W., Prideaux V., Lye S.J., and Rossant J. Progressive expression of trophoblast-specific genes during formation of mouse trophoblast giant cells in vitro. Mol. Reprod. Dev. 34 (1993) 357-368
5. Chaddha V., Viero S., Huppertz B., and Kingdom J. Developmental biology of the placenta and the origins of placental insufficiency. Semin. Fetal. Neonatal. Med. 9 (2004) 357-369
6. Charalambous M., Smith F.M., Bennett W.R., Crew T.E., Mackenzie F., and Ward A. Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 8292-8297
7. Chiao E., Fisher P., Crisponi L., Deiana M., Dragatsis I., Schlessinger D., Pilia G., and Efstratiadis A. Overgrowth of a mouse model of the Simpson-Golabi-Behmel syndrome is independent of IGF signaling. Dev. Biol. 243 (2002) 185-206
8. Coan P.M., Angiolini E., Sandovici I., Burton G.J., Constancia M., and Fowden A.L. Adaptations in placental nutrient transfer capacity to meet fetal growth demands depend on placental size in mice. J. Physiol. 586 (2008) 4567-4576
9. Coan P.M., Fowden A.L., Constancia M., Ferguson-Smith A.C., Burton G.J., and Sibley C.P. Disproportional effects of Igf2 knockout on placental morphology and diffusional exchange characteristics in the mouse. J. Physiol. 586 (2008) 5023-5032
10. Constancia M., Angiolini E., Sandovici I., Smith P., Smith R., Kelsey G., Dean W., Ferguson-Smith A., Sibley C.P., Reik W., and Fowden A. Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 19219-19224
11. Constancia M., Hemberger M., Hughes J., Dean W., Ferguson-Smith A., Fundele R., Stewart F., Kelsey G., Fowden A., Sibley C., and Reik W. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417 (2002) 945-948
12. DeChiara T.M., Efstratiadis A., and Robertson E.J. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345 (1990) 78-80
13. Duselis A.R., and Vrana P.B. Assessment and disease comparisons of hybrid developmental defects. Hum. Mol. Genet. 16 (2007) 808-819
14. Efstratiadis A. Genetics of mouse growth. Int. J. Dev. Biol. 42 (1998) 955-976
15. Frank D., Fortino W., Clark L., Musalo R., Wang W., Saxena A., Li C.M., Reik W., Ludwig T., and Tycko B. Placental overgrowth in mice lacking the imprinted gene Ipl. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 7490-7495
16. Guo L., Choufani S., Ferreira J., Smith A., Chitayat D., Shuman C., Uxa R., Keating S., Kingdom J., and Weksberg R. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev. Biol. 320 (2008) 79-91
17. Hager R., and Johnstone R.A. The genetic basis of family conflict resolution in mice. Nature 421 (2003) 533-535
18. Hales C.N., and Barker D.J. The thrifty phenotype hypothesis. Br. Med. Bull. 60 (2001) 5-20
19. Henriksen T. The macrosomic fetus: a challenge in current obstetrics. Acta. Obstet. Gynecol. Scand. 87 (2008) 134-145
20. Hikichi T., Kohda T., Kaneko-Ishino T., and Ishino F. Imprinting regulation of the murine Meg1/Grb10 and human GRB10 genes; roles of brain-specific promoters and mouse-specific CTCF-binding sites. Nucleic Acids Res. 31 (2003) 1398-1406
21. Klammt J., Pfaffle R., Werner H., and Kiess W. IGF signaling defects as causes of growth failure and IUGR. Trends. Endocrinol. Metab. 19 (2008) 197-205
22. Kurz H., Zechner U., Orth A., and Fundele R. Lack of correlation between placenta and offspring size in mouse interspecific crosses. Anat. Embryol. (Berl). 200 (1999) 335-343
23. Liu F., and Roth R.A. Grb-IR: a SH2-domain-containing protein that binds to the insulin receptor and inhibits its function. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 10287-10291
24. Lopez M.F., Dikkes P., Zurakowski D., and Villa-Komaroff L. Insulin-like growth factor II affects the appearance and glycogen content of glycogen cells in the murine placenta. Endocrinology 137 (1996) 2100-2108
25. McLaren A. Genetic and environmental effects on foetal and placental growth in mice. J. Reprod. Fertil. 9 (1965) 79-98
26. McMinn J., Wei M., Schupf N., Cusmai J., Johnson E.B., Smith A.C., Weksberg R., Thaker H.M., and Tycko B. Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta 27 (2006) 540-549
27. Miyoshi N., Kuroiwa Y., Kohda T., Shitara H., Yonekawa H., Kawabe T., Hasegawa H., Barton S.C., Surani M.A., Kaneko-Ishino T., and Ishino F. Identification of the Meg1/Grb10 imprinted gene on mouse proximal chromosome 11, a candidate for the Silver-Russell syndrome gene. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 1102-1107
28. Monami G., Emiliozzi V., and Morrione A. Grb10/Nedd4-mediated multiubiquitination of the insulin-like growth factor receptor regulates receptor internalization. J. Cell. Physiol. 216 (2008) 426-437
29. Monk D., Arnaud P., Frost J., Hills F.A., Stanier P., Feil R., and Moore G.E. Reciprocal imprinting of human GRB10 in placental trophoblast and brain: evolutionary conservation of reversed allelic expression. Hum. Mol. Genet. 18 (2009) 3066-3074
30. Moore T., and Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends. Genet. 7 (1991) 45-49
31. Morrione A., Valentinis B., Li S., Ooi J.Y., Margolis B., and Baserga R. Grb10: a new substrate of the insulin-like growth factor I receptor. Cancer Res. 56 (1996) 3165-3167
32. Neganova I., Al-Qassab H., Heffron H., Selman C., Choudhury A.I., Lingard S.J., Diakonov I., Patterson M., Ghatei M., Bloom S.R., Franks S., Huhtaniemi I., Hardy K., and Withers D.J. Role of central nervous system and ovarian insulin receptor substrate 2 signaling in female reproductive function in the mouse. Biol. Reprod. 76 (2007) 1045-1053
33. Ooi J., Yajnik V., Immanuel D., Gordon M., Moskow J.J., Buchberg A.M., and Margolis B. The cloning of Grb10 reveals a new family of SH2 domain proteins. Oncogene 10 (1995) 1621-1630
34. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. e45 (2001) 29
35. Redline R.W., Chernicky C.L., Tan H.Q., and Ilan J. Differential expression of insulin-like growth factor-II in specific regions of the late (post day 9.5) murine placenta. Mol. Reprod. Dev. 36 (1993) 121-129
36. Reik W., Constancia M., Fowden A., Anderson N., Dean W., Ferguson-Smith A., Tycko B., and Sibley C. Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J. Physiol. 547 (2003) 35-44
37. Rogers J.F., and Dawson W.D. Foetal and placental size in a Peromyscus species cross. J. Reprod. Fert. 21 (1970) 255-262
38. Sibley C., Glazier J., and D'Souza S. Placental transporter activity and expression in relation to fetal growth. Exp. Physiol. 82 (1997) 389-402
39. Sibley C.P., Coan P.M., Ferguson-Smith A.C., Dean W., Hughes J., Smith P., Reik W., Burton G.J., Fowden A.L., and Constancia M. Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 8204-8208
40. Smith F.M., Holt L.J., Garfield A.S., Charalambous M., Koumanov F., Perry M., Bazzani R., Sheardown S.A., Hegarty B.D., Lyons R.J., Cooney G.J., Daly R.J., and Ward A. Mice with a disruption of the imprinted Grb10 gene exhibit altered body composition, glucose homeostasis, and insulin signaling during postnatal life. Mol. Cell. Biol. 27 (2007) 5871-5886
41. Stempien M.M., Fong N.M., Rall L.B., and Bell G.I. Sequence of a placental cDNA encoding the mouse insulin-like growth factor II precursor. DNA 5 (1986) 357-361
42. Takahashi K., Kobayashi T., and Kanayama N. p57(Kip2) regulates the proper development of labyrinthine and spongiotrophoblasts. Mol. Hum. Reprod. 6 (2000) 1019-1025
43. Vrana P.B., Guan X.-J., Ingram R.S., and Tilghman S.M. Genomic imprinting is disrupted in interspecific Peromyscus hybrids. Nat. Genet. 20 (1998) 362-365
44. Wang L., Balas B., Christ-Roberts C.Y., Kim R.Y., Ramos F.J., Kikani C.K., Li C., Deng C., Reyna S., Musi N., Dong L.Q., DeFronzo R.A., and Liu F. Peripheral disruption of the Grb10 gene enhances insulin signaling and sensitivity in vivo. Mol. Cell. Biol. 27 (2007) 6497-6505
45. Wang Z.Q., Fung M.R., Barlow D.P., and Wagner E.F. Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature 372 (1994) 464-467
46. Watson E.D., and Cross J.C. Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20 (2005) 180-193