Placenta
Volume 29 , Pages 42-47 , March 2008

Distinct Actions of Insulin-Like Growth Factors (IGFs) on Placental Development and Fetal Growth: Lessons from Mice and Guinea Pigs

,Accepted 3 December 2007.

References 

  1. Laws PJ, Grayson N, Sullivan EA. Australia's mothers and babies 2004. Sydney: AIHW National Perinatal Statistics Unit; 2006;
  2. Heard AR, Dekker GA, Chan A, Jacobs DJ, Vreeburg SA, Priest KR. Hypertension during pregnancy in South Australia, Part 1: Pregnancy outcomes. Aust N Z J Obstet Gynaecol. 2004;44:404–409
  3. Gude NM, Roberts CT, Kalionis B, King RG. Growth and function of the normal human placenta. Thromb Res. 2004;114:397–407
  4. Khong TY, Liddell HS, Robertson WB. Defective haemochorial placentation as a cause of miscarriage: a preliminary study. Br J Obstet Gynaecol. 1987;94:649–655
  5. Khong TY, De Wolf F, Robertson WB, Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol. 1986;93:1049–1059
  6. Mayhew TM, Wijesekara J, Baker PN, Ong SS. Morphometric evidence that villous development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by pre-eclampsia. Placenta. 2004;25:829–833
  7. Barker DJP. Mothers, babies and health in later life. London: Churchill Livingstone; 1998;
  8. DeChiara TM, Efstratiadis A, Robertson EJ. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature. 1990;345:78–80
  9. Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. Mice carrying null mutations of the genes encoding insulin- like growth factor-I (Igf-1) and type-1 IGF receptor (Igf1r). Cell. 1993;75:59–72
  10. Denley A, Cosgrove LJ, Booker GW, Wallace JC, Forbes BE. Molecular interactions of the IGF system. Cytokine Growth Factor Rev. 2005;16:421–439
  11. Han VK, Carter AM. Spatial and temporal patterns of expression of messenger RNA for insulin-like growth factors and their binding proteins in the placenta of man and laboratory animals. Placenta. 2000;21:289–305
  12. Han VKM, Bassett N, Walton J, Challis JRG. The expression of insulin-like growth factor (IGF) and IGF-binding protein (IGFBP) genes in the human placenta and membranes: evidence for IGF-IGFBP interactions at the feto-maternal interface. J Clin Endocrinol Metab. 1996;81:2680–2693
  13. Irving JA, Lala PK. Functional role of cell surface integrins on human trophoblast cell migration - regulation by TGF beta, IGF-II and IGFBP-1. Exp Cell Res. 1995;217:419–427
  14. McKinnon T, Chakraborty C, Gleeson LM, Chidiac P, Lala PK. Stimulation of human extravillous trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G protein(s) and phosphorylation of MAPK. J Clin Endocrinol Metab. 2001;86:3665–3674
  15. Lopez MF, Dikkes P, Zurakowski D, Villakomaroff L. Insulin-like growth factor II affects the appearance and glycogen content of glycogen cells in the murine placenta. Endocrinology. 1996;137:2100–2108
  16. Kanai-Azuma M, Kanai Y, Kurohmaru M, Sakai S, Hayashi Y. Insulin-like growth factor (IGF)-I stimulates proliferation and migration of mouse ectoplacental cone cells, while IGF-II transforms them into trophoblastic giant cells in vitro. Biol Reprod. 1993;48:252–261
  17. Pringle KG, Roberts CT. New light on early post-implantation pregnancy in the mouse: roles for insulin-like growth factor-II (IGF-II)?. Placenta. 2007;28:286–297
  18. Redline RW, Chernicky CL, Tan HQ, 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. 1993;36:121–129
  19. Volpert O, Jackson D, Bouck N, Linzer DI. The insulin-like growth factor II/mannose 6-phosphate receptor is required for proliferin-induced angiogenesis. Endocrinology. 1996;137:3871–3876
  20. Zygmunt M, McKinnon T, Herr F, Lala PK, Han VKM. HCG increases trophoblast migration in vitro via the insulin-like growth factor-II/mannose-6 phosphate receptor. Mol Hum Reprod. 2005;11:261–267
  21. Sohlstrom A, Katsman A, Kind KL, Roberts CT, Owens PC, Robinson JS, et al. Food restriction alters pregnancy-associated changes in IGF and IGFBP in the guinea pig. Am J Physiol. 1998;274:E410–E416
  22. Roberts CT, Sohlstrom A, Kind KL, Earl RA, Khong TY, Robinson JS, et al. Maternal food restriction reduces the exchange surface area and increases the barrier thickness of the placenta in the guinea-pig. Placenta. 2001;22:177–185
  23. Roberts CT, Sohlstrom A, Kind KL, Grant PA, Earl RA, Robinson JS, et al. Altered placental structure induced by maternal food restriction in guinea pigs: a role for circulating IGF-II and IGFBP-2 in the mother?. Placenta. 2001;22:S77–S82
  24. Roberts CT, Kind KL, Earl RA, Grant PA, Robinson JS, Sohlstrom A, et al. Circulating insulin-like growth factor (IGF)-I and IGF binding proteins -1 and -3 and placental development in the guinea-pig. Placenta. 2002;23:763–770
  25. Olausson H, Sohlstrom A. Effects of food restriction and pregnancy on the expression of insulin-like growth factors-I and -II in tissues from guinea pigs. J Endocrinol. 2003;179:437–445
  26. Carter AM. Animal models of human placentation—a review. Placenta. 2007;28(Suppl. A):S41–S47
  27. Mess A. The Guinea pig placenta: model of placental growth dynamics. Placenta. 2007;28:812–815
  28. Mess A, Zaki N, Kadyrov M, Korr H, Kaufmann P. Caviomorph placentation as a model for trophoblast invasion. Placenta. 2007;28:1234–1238
  29. Gargosky SE, Owens PC, Walton PE, Owens JA, Robinson JS, Wallace JC, et al. Most of the circulating insulin-like growth factors I and II are present in the 150kDa serum complex during human pregnancy. J Endocrinol. 1991;131:491–497
  30. Sohlstrom A, Katsman A, Kind KL, Grant PA, Owens PC, Robinson JS, et al. Effects of acute and chronic food restriction on the insulin-like growth factor axis in the guinea pig. J Endocr. 1998;157:107–114
  31. Sferruzzi-Perri AN, Owens JA, Pringle KG, Robinson JS, Roberts CT. Maternal insulin-like growth factors-I and -II act via different pathways to promote fetal growth. Endocrinology. 2006;147:3344–3355
  32. Sohlstrom A, Fernberg P, Owens JA, Owens PC. Maternal nutrition affects the ability of treatment with IGF-I and IGF-II to increase growth of the placenta and fetus, in guinea pigs. Growth Horm IGF Res. 2001;11:392–398
  33. Sferruzzi-Perri AN, Owens JA, Standen P, Taylor RL, Robinson JS, Roberts CT. Early pregnancy maternal endocrine insulin-like growth factor I programs the placenta for increased functional capacity throughout gestation. Endocrinology. 2007;148:4362–4370
  34. Sferruzzi-Perri AN, Owens JA, Standen P, Taylor RL, Heinemann GK, Robinson JS, et al. Early treatment of the pregnant guinea pig with IGFs promotes placental transport and nutrient partitioning near term. Am J Physiol Endocrinol Metab. 2007;292:E668–E676
  35. Gargosky SE, Owens JA, Walton PE, Owens PC, Wallace JC, Ballard FJ. Insulin-like growth factor-I, but not growth hormone, increases maternal weight gain in late pregnancy without affecting fetal or placental growth. J Endocrinol. 1991;130:395–400
  36. Gluckman PD, Morel PCH, Ambler BH, Breier HT, McCutcheon SN. Elevating maternal insulin-like growth factor-1 in mice and rats alters the pattern of fetal growth by removing maternal constraint. J Endocrinol. 1992;134:R1–R3
  37. Ong K, Kratzsch J, Kiess W, Costello M, Scott C, Dunger D. Size at birth and cord blood levels of insulin, insulin-like growth factor I (IGF-I), IGF-II, IGF-binding protein-1 (IGFBP-1), IGFBP-3, and the soluble IGF-II/mannose-6-phosphate receptor in term human infants. The ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. J Clin Endocrinol Metab. 2000;85:4266–4269
  38. Morrione A, Valentinis B, Xu SQ, Yumet G, Louvi A, Efstratiadis A, et al. Insulin-like growth factor II stimulates cell proliferation through the insulin receptor. Proc Natl Acad Sci USA. 1997;94:3777–3782
  39. Louvi A, Accili D, Efstratiadis A. Growth-promoting interaction of IGF-II with the insulin receptor during mouse embryonic development. Dev Biol. 1997;189:33–48
  40. Denley A, Bonython ER, Booker GW, Cosgrove LJ, Forbes BE, Ward CW, et al. Structural determinants for high-affinity binding of insulin-like growth factor II to insulin receptor (IR)-A, the exon 11 minus isoform of the IR. Mol Endocrinol. 2004;18:2502–2512
  41. Desoye G, Hartmann M, Jones CJ, Wolf HJ, Kohnen G, Kosanke G, et al. Location of insulin receptors in the placenta and its progenitor tissues. Microsc Res Tech. 1997;38:63–75
  42. Lau MM, Stewart CE, Liu Z, Bhatt H, Rotwein P, Stewart CL. Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev. 1994;8:2953–2963
  43. Ludwig T, Eggenschwiler J, Fisher P, D'Ercole AJ, Davenport ML, Efstratiadis A. Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev Biol. 1996;177:517–535
  44. Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature. 2002;417:945–948
  45. Sibley CP, Coan PM, Ferguson-Smith AC, Dean W, Hughes J, Smith P, et al. Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc Natl Acad Sci USA. 2004;101:8204–8208
  46. Constancia M, Angiolini E, Sandovici I, Smith P, Smith R, Kelsey G, et al. Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proc Natl Acad Sci USA. 2005;102:19219–19224
  47. Carter AM, Kingston MJ, Han KK, Mazzuca DM, Nygard K, Han VK. Altered expression of IGFs and IGF-binding proteins during intrauterine growth restriction in guinea pigs. J Endocrinol. 2005;184:179–189

PII: S0143-4004(07)00291-3

doi: 10.1016/j.placenta.2007.12.002

Placenta
Volume 29 , Pages 42-47 , March 2008