Insulin-like growth factors in embryonic and fetal growth and skeletal development (Review)
- Authors:
- Georgios D. Agrogiannis
- Stavros Sifakis
- Efstratios S. Patsouris
- Anastasia E. Konstantinidou
-
Affiliations: 1st Department of Pathology, School of Medicine, University of Athens, Athens, Greece, Department of Obstetrics and Gynecology, University Hospital of Heraklion, Crete, Greece - Published online on: May 21, 2014 https://doi.org/10.3892/mmr.2014.2258
- Pages: 579-584
This article is mentioned in:
Abstract
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Jones JI and Clemmons DR: Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev. 16:3–34. 1995.PubMed/NCBI | |
|
LeRoith D, Werner H, Beitner-Johnson and Roberts CT Jr: Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr Rev. 16:143–163. 1995. View Article : Google Scholar | |
|
Kornfeld S: Structure and function of the mannose-6-phosphate/insulin-like growth factor II receptors. Annu Rev Biochem. 61:307–330. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Efstratiadis A: Genetics of mouse growth. Int J Dev Biol. 42:955–976. 1998. | |
|
Davies SM: Developmental regulation of genomic imprinting of the Igf2 gene in human liver. Cancer Res. 54:2560–2562. 1994.PubMed/NCBI | |
|
Vetter U, Zapf J, Heit W, et al: Human fetal and adult chondrocytes. Effect of insulin-like growth factors I and II, insulin, and growth hormone on clonal growth. J Clin Invest. 77:1903–1908. 1986. View Article : Google Scholar : PubMed/NCBI | |
|
Bhaumick B and Bala RM: Differential effects of insulin-like growth factors I and II on growth, differentiation and glucoregulation in differentiating chondrocyte cells in culture. Acta Endocrinol (Copenh). 125:201–211. 1991.PubMed/NCBI | |
|
Lorenzo M, Valverde AM, Ternel T and Benito M: IGF-I is a mitogen involved in differentiation-related gene expression in fetal rat brown adipocytes. J Cell Biol. 123:1567–1575. 1993. View Article : Google Scholar : PubMed/NCBI | |
|
Harvey MB and Kaye PL: Insulin-like growth factor-1 stimulates growth of mouse preimplantation embryos in vitro. Mol Reprod Dev. 31:195–199. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Canalis E, McCarthy T and Centrella M: Isolation and characterization of insulin-like growth factor I (somatomedin-C) from cultures of fetal rat calvariae. Endocrinology. 122:22–27. 1988. View Article : Google Scholar : PubMed/NCBI | |
|
D’Ercole AJ, Applewhite GT and Underwood LE: Evidence that somatomedin is synthesized by multiple tissues in the fetus. Dev Biol. 75:315–328. 1980.PubMed/NCBI | |
|
DeChiara TM, Efstratiadis A and Robertson EJ: A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature. 345:78–80. 1990. View Article : Google Scholar : PubMed/NCBI | |
|
Liu J-P, Baker J, Perkins AS, Roberson EJ and Efstratiadis A: Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell. 75:59–72. 1993. | |
|
Baker J, Liu J-P, Robertson EJ and Efstratiadis A: Role of insulin-like growth factors in embryonic and postnatal growth. Cell. 75:73–82. 1993. View Article : Google Scholar : PubMed/NCBI | |
|
Wajnrajch MP, Gertner JM, Harbison MD, Chua SC Jr and Leibel RL: Nonsense mutation in the human growth hormone-releasing hormone receptor causes growth failure analogous to the little (lit) mouse. Nat Genet. 12:88–90. 1996. View Article : Google Scholar : PubMed/NCBI | |
|
Savage MO, Blum WF, Ranke MB, et al: Clinical features and endocrine status in patients with growth hormone insensitivity (Laron syndrome). J Clin Endocrinol Metab. 77:1465–1471. 1993.PubMed/NCBI | |
|
Sanders EJ and Harvey S: Growth hormone as an early embryonic growth and differentiation factor. Anat Embryol (Berl). 209:1–9. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Walenkamp MJ, Karperien M, Pereira AM, et al: Homozygous and heterozygous expression of a novel insulin-like growth factor-I mutation. J Clin Endocrinol Metab. 90:2855–2864. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Bhakta KY, Marlin SJ, Shen JJ and Fernandes CJ: Terminal deletion of chromosome 15q26.1: case report and brief literature review. J Perinatol. 25:429–432. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Gluckman PD and Butler JH: Parturition-related changes in insulin-like growth factors-I and -II in the perinatal lamb. J Endocrinol. 99:223–232. 1983. View Article : Google Scholar : PubMed/NCBI | |
|
Holland MD, Hossner KL, Williams SE, Wallace CR, Niswender GD and Odde KG: Serum concentrations of insulin-like growth factors and placental lactogen during gestation in cattle. Domest Anim Endocrinol. 14:231–239. 1997. View Article : Google Scholar | |
|
Lee CY, Chung CS and Simmen FA: Ontogeny of the porcine insulin-like growth factor system. Mol Cell Endocrinol. 93:71–80. 1993. View Article : Google Scholar : PubMed/NCBI | |
|
Moses AC, Nissley SP, Short PA, et al: Increased levels of multiplication-stimulating activity, an insulin-like growth factor, in fetal rat serum. Proc Natl Acad Sci USA. 77:3649–3653. 1980. View Article : Google Scholar : PubMed/NCBI | |
|
Daughaday WH, Parker KA, Borowsky S, Trivedi B and Kapadia M: Measurement of somatomedin-related peptides in fetal, neonatal, and maternal rat serum by insulin-like growth factor (IGF) I radioimmunoassay, IGF-II radioreceptor assay (RRA), and multiplication-stimulating activity RRA after acid-ethanol extraction. Endocrinology. 110:575–581. 1982. View Article : Google Scholar | |
|
Lund PK, Moats-Staats BM, Hynes MA, et al: Somatomedin-C/insulin-like growth factor-I and insulin-like growth factor-II mRNAs in rat fetal and adult tissues. J Biol Chem. 261:14539–14544. 1986.PubMed/NCBI | |
|
Gluckman PD, Johnson-Barrett JJ, Butler JH, Edgar BW and Gunn TR: Studies of insulin-like growth factor-I and -II by specific radioligand assays in umbilical cord blood. Clin Endocrinol (Oxf). 19:405–413. 1983. View Article : Google Scholar : PubMed/NCBI | |
|
Lassarre C, Hardouin S, Daffos F, Forestier F, Frankenne F and Binoux M: Serum insulin-like growth factors and insulin-like growth factor binding proteins in the human fetus. Relationships with growth in normal subjects and in subjects with intrauterine growth retardation. Pediatr Res. 29:219–225. 1991. View Article : Google Scholar | |
|
Verhaeghe J, Van Bree R, Van Herck E, Laureys J, Bouillon R and van Assche FA: C-peptide, the insulin-like growth factors-I and -II, and IGF-binding protein I in umbilical cord serum: correlations with birthweight. Am J Obstet Gynecol. 169:89–97. 1993. View Article : Google Scholar : PubMed/NCBI | |
|
Giudice LC, de Zegher F, Gargosky SE, et al: Insulin-like growth factors and their binding proteins in the term and preterm human fetus and neonate with normal and extremes of intrauterine growth. J Clin Endocrinol Metab. 80:1548–1555. 1995.PubMed/NCBI | |
|
Sifakis S, Akolekar R, Kappou D, Mantas N and Nicolaides KH: Maternal serum insulin like growth factor-I (IGF-I) at 11–13 weeks in preeclampsia. Prenat Diagn. 30:1026–1031. 2010. | |
|
Sifakis S, Akolekar R, Kappou D, Mantas N and Nicolaides KH: Maternal serum insulin-like growth factor binding protein-1 (IGFBP-1) at 11–13 weeks in preeclampsia. Prenat Diagn. 31:196–201. 2011.PubMed/NCBI | |
|
Sifakis S, Akolekar R, Kappou D, Mantas N and Nicolaides KH: Maternal serum insulin-like growth factor binding protein-3 (IGFBP-3) at 11–13 weeks in preeclampsia. J Hum Hypertens. 26:253–258. 2012.PubMed/NCBI | |
|
Sifakis S, Akolekar R, Kappou D, Mantas N and Nicolaides KH: Maternal serum insulin like growth factor (IGF-I) and binding proteins IGFBP-1 and IGFBP-3 at 11–13 weeks’ gestation in pregnancies delivering small for gestational age neonates. Eur J Obstet Gynecol Reprod Biol. 161:30–33. 2012. | |
|
Koutsaki M, Sifakis S, Zaravinos A, Koutroulakis D, Koukoura O and Spandidos DA: Decreased placental expression of hPGH, IGF-I and IGFBP-1 in pregnancies complicated by fetal growth restriction. Growth Horm IGF Res. 21:31–36. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Koukoura O, Sifakis S, Zaravinos A, et al: Aberrant methylation of IGF2 is associated with loss of imprinting in placentas from pregnancies complicated with fetal growth restriction. Int J Mol Med. 28:481–487. 2011.PubMed/NCBI | |
|
Watson AJ, Hogan A, Hahnel A, Wiemer KE and Schultz GA: Expression of growth factor ligand and receptor genes in the preimplantation bovine embryo. Mol Reprod Dev. 31:87–95. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Watson AJ, Watson PH, Arcellana-Panlilio M, et al: A growth factor phenotype map for ovine preimplantation development. Biol Reprod. 50:725–733. 1994. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang X, Kidder GM, Watson AJ, Schultz GA and Armstrong DT: Possible roles of insulin and insulin-like growth factors in rat preimplantation development: investigation of gene expression by reverse transcription-polymerase chain reaction. J Reprod Fertil. 100:375–380. 1994. View Article : Google Scholar | |
|
Lighten AD, Hardy K, Winston RM and Moore GE: Expression of mRNA for the insulin-like growth factors and their receptors in human preimplantation embryos. Mol Reprod Dev. 47:134–139. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Rotwein P, Pollock KM, Watson M and Milbrandt JD: Insulin-like growth factor gene expression during rat embryonic development. Endocrinology. 121:2141–2144. 1987. View Article : Google Scholar : PubMed/NCBI | |
|
Schlegel W, Halbauer D, Raimann A, et al: IGF expression patterns and regulation in growth plate chondrocytes. Mol Cell Endocrinol. 327:65–71. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y, Cheng Z, Elalieh HZ, et al: IGF1R signaling in chondrocytes modulates growth plate development by interacting with the PTHrP/Ihhpathway. J Bone Miner Res. 26:1437–46. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Parker EA, Hegde A, Buckley M, Barnes KM, Baron J and Nilsson O: Spatial and temporal regulation of GH-IGF-related gene expression in growth plate cartilage. J Endocrinol. 194:31–40. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Sadler TW: Limbs. Langman’s Medical Embryology. Lippincott Williams and Wilkins; Philadephia, PA: 12th edition. pp. 151–152 | |
|
Sifakis S, Basel D, Ianakiev P, Kilpatrick M and Tsipouras P: Distal limb malformations: underlying mechanisms and clinical associations. Clin Genet. 60:165–172. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Kaplowitz PB, D’Ercole AJ and Underwood LE: Stimulation of embryonic mouse limb bud mesenchymal cell growth by peptide growth factors. J Cell Physiol. 112:353–359. 1982. View Article : Google Scholar : PubMed/NCBI | |
|
Bhaumick B and Bala RM: Receptors for insulin-like growth factors I and II in developing embryonic mouse limb bud. Bioch Bioph Acta. 927:117–128. 1987. View Article : Google Scholar : PubMed/NCBI | |
|
Geduspan JS and Solursh M: Effects of the mesonephros and insulin-like growth factor I on chondrogenesis of limb explants. Dev Biol. 156:500–508. 1993. View Article : Google Scholar : PubMed/NCBI | |
|
Streck RD, Wood TL, Hsu MS and Pintar JE: Insulin-like growth factor I and II and insulin-like growth factor binding protein 2 RNAs are expressed in adjacent tissues within rat embryonic and fetal limbs. Dev Biol. 151:586–596. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Ralphs JR, Wylie L and Hill DJ: Distribution of insulin-like growth factor peptides in the developing chick embryo. Development. 109:51–58. 1990.PubMed/NCBI | |
|
Geduspan JS, Padanilam BJ and Solursh M: Coordinate expression of IGF-I and its receptor during limb outgrowth. Dev Dyn. 195:67–73. 1992. View Article : Google Scholar : PubMed/NCBI | |
|
Mc Queeney K and Dealy CN: Roles of insulin-like growth factor-I (IGF-I) and IGF-I binding protein-2 (IGFBP2) and -5 (IGFBP5) in developing chick limbs. Growth Horm IGF Res. 11:346–363. 2001.PubMed/NCBI | |
|
van Kleffens M, Groffen C, Rosato RR, et al: mRNA expression patterns of the IGF system during mouse limb bud development determined by whole mount in situ hybridization. Mol Cell Endocrinol. 138:151–161. 1998.PubMed/NCBI | |
|
Wang E, Wang J, Chin E, Zhou J and Bondy CA: Cellular patterns of insulin-like growth factor system gene expression in murine chondrogenesis and osteogenesis. Endocrinology. 136:2741–2751. 1995.PubMed/NCBI | |
|
Allan GJ, Flint DJ, Darling SM, Geh J and Patel K: Altered expression of insulin-like growth factor 1 and insulin-like growth factor binding proteins 2 and 5 in the mouse mutant Hypodactyly (Hd) correlates with sites of apoptotic activity. Anat Embryol (Berl). 202:1–11. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Lok F, Owens JA, Mundy L, Robinson JS and Owens PC: Insulin-like growth factor I promotes growth selectively in fetal sheep in late gestation. Am J Physiol. 270:R1148–R1155. 1996.PubMed/NCBI | |
|
Mathews LS, Hammer RE, Behringer RR, et al: Growth enhancement of transgenic mice expressing human insulin-like growth factor I. Endocrinology. 123:2827–2833. 1988. View Article : Google Scholar : PubMed/NCBI | |
|
Dealy CN and Kosher RA: Studies on insulin-like growth factor-I and insulin in chick limb morphogenesis. Dev Dyn. 202:67–79. 1995. View Article : Google Scholar : PubMed/NCBI | |
|
Mesiano S, Young IR, Baxter RC, Hintz RL, Browne CA and Thorburn GD: Effect of hypophysectomy with and without thyroxine replacement on growth and circulating concentrations of insulin-like growth factors I and II in the fetal lamb. Endocrinology. 120:1821–1830. 1987. View Article : Google Scholar | |
|
Bikle D, Majumdar S, Laib A, et al: The skeletal structure of insulin-like growth factor I-deficient mice. J Bone Miner Res. 16:2320–2329. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Burghardt AJ, Wang Y, Elalieh H, et al: Evaluation of fetal bone structure and mineralization in IGF-I deficient mice using synchrotron radiation microtomography and Fourier transform infrared spectroscopy. Bone. 40:160–168. 2007. View Article : Google Scholar | |
|
Woods KA, Camacho-Hübner C, Barter D, Clark AJL and Savage MO: Insulin-like growth factor I gene deletion causing intrauterine growth retardation an severe short stature. Acta Paediatr Suppl. 423:39–45. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Netchine I, Azzi S, Housang M, et al: Partial primary deficiency of insulin-like growth factor (IGF)-I activity associated with IGF1 mutation demonstrates its critical role in growth and brain development. J Clin Endocrinol Metab. 94:3913–3921. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Bonapace G, Concolino D, Formicola S and Strisciuglio P: A novel mutation in a patient with insulin-like growth factor 1 (IGF1) deficiency. J Med Genet. 40:913–917. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Coutinho DC, Coletta RR, Costa EM, et al: Polymorphisms identified in the upstream core polyadenylation signal of IGF1 gene exon 6 do not cause pre- and postnatal growth impairment. J Clin Endocrinol Metab. 92:4889–4892. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
van Duyvenvoorde HA, van Setten PA, Walenkamp MJE, et al: Short stature associated with a novel heterozygous mutation in the insulin-like growth factor 1 gene. J Clin Endocrinol Metab. 95:E363–E367. 2010.PubMed/NCBI | |
|
van Duyvenvoorde HA, van Doorn J, Koenig J, et al: The severe short stature in two siblings with a heterozygous IGF1 mutation is not caused by a dominant negative effect of the putative truncated protein. Growth Hormone IGF Res. 21:44–50. 2011.PubMed/NCBI | |
|
Abuzzahab MJ, Schneider A, Goddard A, et al: IGF-I receptor mutations resulting in intrauterine and postnatal growth retardation. N Engl J Med. 349:2211–2222. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Kawashima Y, Kanzaki S, Yang F, et al: Mutation at cleavage site of insulin-like growth factor receptor in a short-stature child born with intrauterine growth retardation. J Clin Endocrinol Metab. 90:4679–4687. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Raile K, Klammt J, Schneider A, et al: Clinical and functional characteristics of the human Arg59Ter insulin-like growth factor I receptor (IGF1R) mutation: implication for a gene dosage effect of the human IGF1R. J Clin Endocrinol Metab. 91:2264–2271. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Walenkamp MJ, van der Kamp HJ, Pereira AM, et al: A variable degree of intrauterine and postnatal growth retardation in a family with a missense mutation in the insulin-like growth factor I receptor. J Clin Endocrinol Metab. 91:3062–3070. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Inagaki K, Tiulpakov A, Rubtsov P, et al: A familial insulin-like growth factor I receptor mutant leads to short stature: clinical and biochemical characterization. J Clin Endocrinol Metab. 92:1542–1548. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Kruis T, Klammt J, Galli-Tsinopoulou A, et al: Heterozygous mutation within a kinase-conserved motif of the insulin-like growth factor I receptor causes intrauterine and postnatal growth retardation. J Clin Endocrinol Metab. 95:1137–1142. 2010. View Article : Google Scholar | |
|
Wallborn T, Wüller S, Klammt J, et al: A heterozygous mutation of the insulin-like growth factor-I receptor causes retention of the nascent protein in the endoplasmic reticulum and results in intrauterine and postnatal growth retardation. J Clin Endocrinol Metab. 95:2316–2324. 2010. View Article : Google Scholar | |
|
Choi JH, Kang M, Kim GH, et al: Clinical and functional characteristics of a novel heterozygous mutation of the IGF1R gene and IGF1R haploinsufficiency due to terminal 15q26.2->qter deletion in patients with intrauterine growth retardation and postnatal catch-up growth failure. J Clin Endocrinol Metab. 96:E130–E134. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Roback EW, Barakat AJ, Dev VG, Mbikay M, Chrétien M and Butler MG: An infant with deletion of the distal long arm of chromosome 15 (q26.1 - qter) and loss of insulin-like growth factor I receptor gene. Am J Med Genet. 38:74–79. 1991. View Article : Google Scholar : PubMed/NCBI | |
|
Walemkamp MJ, de Muinck Keizer-Schrama SM, de Mos M, et al: Successful long-term growth hormone therapy in a girl with haploinsufficiency in the insulin-like growth factor-I receptor due to a terminal 15q26.2->qter deletion detected by multiplex ligation probe amplification. J Clin Endocrinol Metab. 93:2421–2425. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Fang P, Schwartz ID, Johnson BD, et al: Familial short stature caused by haploinsufficiency of the insulin-like growth factor I receptor due to nonsense-mediated messenger ribonucleic acid decay. J Clin Endocrinol Metab. 94:1740–1747. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Ester WA, van Duyvenvoorde HA, de Wit CC, et al: Two short children born small for gestational age with insulin-like growth factor 1 receptor haploinsufficiency illustrate the heterogeneity of its phenotype. J Clin Endocrinol Metab. 94:4717–4727. 2009. View Article : Google Scholar : PubMed/NCBI |
