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Intrauterine Growth Retardation (IUGR) as a Novel Condition of Insulin-Like Growth Factor-1 (IGF-1) Deficiency

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Reviews of Physiology, Biochemistry and Pharmacology Vol. 170

Part of the book series: Reviews of Physiology, Biochemistry and Pharmacology ((REVIEWS,volume 170))

Abstract

Insulin-like growth factor 1 (IGF-1) is an anabolic hormone with several biological activities, such as proliferation, mitochondrial protection, cell survival, tissue growth and development, anti-inflammatory, antioxidant, antifibrogenic and antiaging. This hormone plays an important role in embryological and postnatal states, being essential for normal foetal and placental growth and differentiation. During gestation, the placenta is one of the major sources of IGF-1, among other hormones. This intrauterine organ expresses IGF-1 receptors and IGF-1 binding proteins (IGFBPs), which control IGF-1 activities. Intrauterine growth restriction (IUGR) is the second most frequent cause of perinatal morbidity and mortality, defined as the inability to achieve the expected weight for gestational age. Different studies have revealed that IUGR infants have placental dysfunction and low circulating levels of insulin, IGF-1, IGF-2 and IGFBPs. Such data suggest that IGF-1 deficiency in gestational state may be one of the major causes of foetal growth retardation. The aim of this review is to study the epidemiology, physiopathology and possible causes of IUGR. Also, it intends to study the possible role of the placenta as an IGF-1 target organ. The purpose is to establish if IUGR could be considered as a novel condition of IGF-1 deficiency and if its treatment with low doses of IGF-1 could be a suitable therapeutic strategy.

The original version of this chapter was revised: The spelling of the third author's name was corrected. The erratum to this chapter is available at DOI: 10.1007/112_2016_1.

An erratum to this chapter can be found at http://dx.doi.org/10.1007/112_2016_1

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Abbreviations

ALS:

Acid-labile subunit

CG:

Chorionic gonadotropin

CRH:

Corticotropin-releasing hormone

CSF:

Cerebrospinal fluid

CTGF:

Connective tissue growth factor

Cyr61:

Cysteine-rich protein 61

ESM-1:

Endothelial cell-specific molecule

FSH:

Follicle-stimulating hormone

GH:

Growth hormone

GHBP:

Growth hormone binding protein

GHRH:

Growth hormone-releasing hormone

GnRH:

Gonadotropin-releasing hormone

HPA:

Hypothalamus–pituitary–adrenal gland axis

IGF-1:

Insulin-like growth factor 1

IGF-1R:

IGF-1 receptor

IGF-2:

Insulin-like growth factor 2

IGFBP-rPs:

IGFBP-related proteins

IGFBPs:

IGF binding proteins

IGFs:

Insulin-like growth factors

IUGR:

Intrauterine growth restriction

LDL:

Low-density lipoprotein

LH:

Luteinising hormone

MAP:

Mitogen-activated protein

NGAS:

Neonatal growth assessment score

NovH:

Human nephroblastoma overexpression gene

PAPP-A:

Pregnancy-associated plasma protein A

PGAS:

Prenatal growth assessment score

PI3K:

Phosphatidylinositol-3-kinase

PL:

Placental lactogen

PLGF:

Placental growth factor

PSF:

Prostacyclin-stimulating factor

PSG:

Pregnancy-specific β-glycoprotein

TAF:

Tumour adhesion factor

TSC 1:

Tuberous sclerosis protein 1

TSC 2:

Tuberous sclerosis protein 2

References

  • Abu-Amero SN, Ali Z, Bennett P, Vaughan JI, Moore GE (1998) Expression of the insulin-like growth factors and their receptors in term placentas: a comparison between normal and IUGR births. Mol Reprod Dev 49:229–235

    Article  CAS  PubMed  Google Scholar 

  • Adair LS (1989) Low birth weight and intrauterine growth retardation in Filipino infants. Pediatrics 84:613–622

    CAS  PubMed  Google Scholar 

  • Albrecht ED, Pepe GJ (2010) Estrogen regulation of placental angiogenesis and fetal ovarian development during primate pregnancy. Int J Dev Biol 54:397–407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Annenkov A (2009) The insulin-like growth factor (IGF) receptor type 1 (IGF1R) as an essential component of the signalling network regulating neurogenesis. Mol Neurobiol 40:195–215

    Article  CAS  PubMed  Google Scholar 

  • Ashworth CJ, Hoggard N, Thomas L, Mercer JG, Wallace JM, Lea RG (2000) Placental leptin. Rev Reprod 5:18–24

    Article  CAS  PubMed  Google Scholar 

  • Avagliano L, Garò C, Marconi AM (2012) Placental amino acids transport in intrauterine growth restriction. J Pregnancy. doi:10.1155/2012/972562

    PubMed  PubMed Central  Google Scholar 

  • Bach LA (2012) The insulin-like growth factor system in kidney disease and hypertension. Curr Opin Nephrol Hypertens 21:86–91

    Article  CAS  PubMed  Google Scholar 

  • Baker J, Liu JP, Robertson EJ, Efstratiadis A (1993) Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73–82

    Article  CAS  PubMed  Google Scholar 

  • Baker J, Hardy MP, Zhou J, Bondy C, Lupu F, Bellvé AR, Efstratiadis A (1996) Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 10:903–918

    CAS  PubMed  Google Scholar 

  • Baker N, Sharpe P, Culley K et al (2012) Dual regulation of metalloproteinase expression in chondrocytes by Wnt-1-inducible signaling pathway protein 3/CCN6. Arthritis Rheum 64:2289–2299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bamfo JE, Odibo AO (2011) Diagnosis and management of fetal growth restriction. J Pregnancy 2011:640715

    Article  PubMed  PubMed Central  Google Scholar 

  • Baschat AA (2004) Fetal responses to placental insufficiency: an update. BJOG 111:1031–1041

    Article  CAS  PubMed  Google Scholar 

  • Bertherat J, Bluet-Pajot MT, Epelbaum J (1995) Neuroendocrine regulation of growth hormone. Eur J Endocrinol 132:12–24

    Article  CAS  PubMed  Google Scholar 

  • Binoux M, Roghani M, Hossenlopp P, Whitechurch O (1991) Cerebrospinal IGF binding proteins: isolation and characterization. Adv Exp Med Biol 293:161–170

    Article  CAS  PubMed  Google Scholar 

  • Biri A, Bozkurt N, Turp A, Kavutcu M, Himmetoglu Ö, Durak I (2007) Role of oxidative stress in intrauterine growth restriction. Gynecol Obstet Invest 64:187–192

    Article  CAS  PubMed  Google Scholar 

  • Bradham DM, Igarashi A, Potter RL, Grotendorst GR (1991) Connective tissue growth factor: a cysteine-rich mitogen secreted by human vascular endothelial cells is related to the SRC-induced immediate early gene product CEF-10. J Cell Biol 114:1285–1294

    Article  CAS  PubMed  Google Scholar 

  • Brosens JJ, Pijnenborg R, Brosens IA (2002) The myometrial junctional zone spiral arteries in normal and abnormal pregnancies. Am J Obstet Gynecol 187:1416–1423

    Article  PubMed  Google Scholar 

  • Burren CP, Wilson EM, Vivian HWA, Youngman OH, Rosenfeld RG (1999) Binding properties and distribution of insulin-like growth factor binding protein-related protein 3 (IGFBP-rP3/NovH), an additional member of the IGFBP superfamily. J Clin Endocrinol Metab 84:1096–1103

    CAS  PubMed  Google Scholar 

  • Carro E, Trejo JL, Gomez-Isla T, LeRoith D, Torres-Aleman I (2002) Serum insulin-like growth factor I regulates brain amyloid-beta levels. Nat Med 8:1390–1397

    Article  CAS  PubMed  Google Scholar 

  • Carson MJ, Behringer RR, Brinster RL, McMorris FA (1993) Insulin-like growth factor I increases brain growth and central nervous system myelination in transgenic mice. Neuron 10:729–740

    Article  CAS  PubMed  Google Scholar 

  • Carter AM, Nygard K, Mazzuca DM, Han VKM (2006) The expression of insulin-like growth factor and insulin-like growth factor binding protein mRNAs in mouse placenta. Placenta 27:278–290

    Article  CAS  PubMed  Google Scholar 

  • Castilla-Cortazar I, Garcia M, Muguerza B, Quiroga J, Perez R, Santidrian S, Prieto J (1997) Hepatoprotective effects of insulin-like growth factor I in rats with carbon tetrachloride-induced cirrhosis. Gastroenterology 113:1682–1691

    Article  CAS  PubMed  Google Scholar 

  • Castilla-Cortázar I, Aliaga-Montilla MA, Salvador J, García M, Delgado G, González-Barón S, Quiroga J, Prieto J (2001) Insulin-like growth factor-I restores the reduced somatostatinergic tone controlling growth hormone secretion in cirrhotic rats. Liver 21:405–409

    Article  PubMed  Google Scholar 

  • Castilla-Cortázar I, García-Fernández M, Delgado G, Puche JE, Sierra I, Barhoum R, González-Barón S (2011) Hepatoprotection and neuroprotection induced by low doses of IGF-II in aging rats. J Transl Med 9:103

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Caufriez A, Reding P, Urbain D, Golstein J, Copinschi G (1991) Insulin-like growth factor I: a good indicator of functional hepatocellular capacity in alcoholic liver cirrhosis. J Endocrinol Invest 14:317–321

    Article  CAS  PubMed  Google Scholar 

  • Cemborain A, Castilla-Cortázar I, García M, Quirog J, Muguerza B, Picardi A, Santidrián S, Prieto J (1998) Osteopenia in rats with liver cirrhosis: beneficial effects of IGF-I treatment. J Hepatol 28:122–131

    Article  CAS  PubMed  Google Scholar 

  • Chard T (1994) Insulin-like growth factors and their binding proteins in normal and abnormal human fetal growth. Growth Regul 4:91–100

    CAS  PubMed  Google Scholar 

  • Chard T, Macintosh M, Yoong A, Chang TC, Robson SC, Spencer JAD, Steer PJ, Gardosi J, Chang A, Symonds EM (1992) Customised antenatal growth charts. Lancet 339:878–879

    Article  CAS  PubMed  Google Scholar 

  • Chitnis MM, Yuen JSP, Protheroe AS, Pollak M, Macaulay VM (2008) The type 1 insulin-like growth factor receptor pathway. Clin Cancer Res 14:6364–6370

    Article  CAS  PubMed  Google Scholar 

  • Clemmons DR (1997) Insulin-like growth factor binding proteins and their role in controlling IGF actions. Cytokine Growth Factor Rev 8:45–62

    Article  CAS  PubMed  Google Scholar 

  • Clemmons DR (2009) Role of IGF-I in skeletal muscle mass maintenance. Trends Endocrinol Metab 20:349–356

    Article  CAS  PubMed  Google Scholar 

  • Clemmons DR, Underwood LE (1991) Nutritional regulation of IGF-I and IGF binding proteins. Annu Rev Nutr 11:393–412

    Article  CAS  PubMed  Google Scholar 

  • Cohick WS, Clemmons DR (1993) The insulin-like growth factors. Annu Rev Physiol 55:131–153

    Article  CAS  PubMed  Google Scholar 

  • Collins S, Arulkumaran S, Hayes K, Jackson S, Impey L (2013) Oxford handbook of obstetrics and gynaecology. Oxford University Press, Oxford

    Book  Google Scholar 

  • Conchillo M, Prieto J, Quiroga J (2007) Insulin-like growth factor I (IGF-I) and liver cirrhosis. Rev Esp Enferm Dig 99:156–164

    Article  CAS  PubMed  Google Scholar 

  • Crossey PA, Pillai CC, Miell JP (2002) Altered placental development and intrauterine growth restriction in IGF binding protein-1 transgenic mice. J Clin Invest 110:411–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dahlseng MO, Andersen GL, Irgens LM, Skranes J, Vik T (2014) Risk of cerebral palsy in term-born singletons according to growth status at birth. Dev Med Child Neurol 56:53–58

    Article  PubMed  Google Scholar 

  • Daughaday WH, Hall K, Raben MS, Salmon WD, van den Brande JL, van Wyk JJ (1972) Somatomedin: proposed designation for sulphation factor. Nature 235:107

    Article  CAS  PubMed  Google Scholar 

  • De Onis M, Blössner M, Villar J (1998) Levels and patterns of intrauterine growth retardation in developing countries. Eur J Clin Nutr 52(Suppl 1):S5–S15

    PubMed  Google Scholar 

  • De Vrijer B, Davidsen ML, Wilkening RB, Anthony RV, Regnault TRH (2006) Altered placental and fetal expression of IGFS and IGF-binding proteins associated with intrauterine growth restriction in fetal sheep during early and mid-pregnancy. Pediatr Res 60:507–512

    Article  PubMed  CAS  Google Scholar 

  • De Zegher F, Francois I, Van Helvoirt M, Van Den Berghe G (1997) Clinical review 89: small as fetus and short as child - From endogenous to exogenous growth hormone. J Clin Endocrinol Metab 82:2021–2026

    PubMed  Google Scholar 

  • Delafontaine P, Song YH, Li Y (2004) Expression, regulation, and function of IGF-1, IGF-1R, and IGF-1 binding proteins in blood vessels. Arterioscler Thromb Vasc Biol 24:435–444

    Article  CAS  PubMed  Google Scholar 

  • Desbois-Mouthon C, Wendum D, Cadoret A, Rey C, Leneuve P, Blaise A, Housset C, Tronche F, Le Bouc Y, Holzenberger M (2006) Hepatocyte proliferation during liver regeneration is impaired in mice with liver-specific IGF-1R knockout. FASEB J 20:773–775

    CAS  PubMed  Google Scholar 

  • Desoye G, Hartmann M, Jones CJP, Wolf HJ, Kohnen G, Kosanke G, Kaufmann P (1997) Location of insulin receptors in the placenta and its progenitor tissues. Microsc Res Tech 38:63–75

    Article  CAS  PubMed  Google Scholar 

  • Deter RL, Stefos T, Harrist RB, Hill RM (1992) Detection of intrauterine growth retardation in twins using individualized growth assessment. II. Evaluation of third-trimester growth and prediction of growth outcome at birth. J Clin Ultrasound 20:579–585

    Article  CAS  PubMed  Google Scholar 

  • Duan C, Bauchat JR, Hsieh T (2000) Phosphatidylinositol 3-kinase is required for insulin-like growth factor-I-induced vascular smooth muscle cell proliferation and migration. Circ Res 86:15–23

    Article  CAS  PubMed  Google Scholar 

  • Fang J, Furesz TC, Lurent RS, Smith CH, Fant ME (1997) Spatial polarization of insulin-like growth factor receptors on the human syncytiotrophoblast. Pediatr Res 41:258–265

    Article  CAS  PubMed  Google Scholar 

  • Firth SM, Baxter RC (2002) Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23:824–854

    Article  CAS  PubMed  Google Scholar 

  • Florini JR, Ewton DZ, Coolican SA (1996) Growth hormone and the insulin-like growth factor system in myogenesis. Endocr Rev 17:481–517

    CAS  PubMed  Google Scholar 

  • Forbes K, Westwood M (2010) Maternal growth factor regulation of human placental development and fetal growth. J Endocrinol 207:1–16

    Article  CAS  PubMed  Google Scholar 

  • Fowden AL, Forhead AJ (2013) Endocrine interactions in the control of fetal growth. Nestle Nutr Inst Workshop Ser 74:91–102

    Article  PubMed  Google Scholar 

  • Freemark M (2006) Regulation of maternal metabolism by pituitary and placental hormones: roles in fetal development and metabolic programming. Horm Res 65:41–49

    Article  CAS  PubMed  Google Scholar 

  • Freemark M (2010) Placental hormones and the control of fetal growth. J Clin Endocrinol Metab 95:2054–2057

    Article  CAS  PubMed  Google Scholar 

  • Freemark M, Comer M (1989) Purification of a distinct placental lactogen receptor, a new member of the growth hormone/prolactin receptor family. J Clin Invest 83:883–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Froesch ER, Buergi H, Ramseier EB, Bally P, Labhart A (1963) Antibody – suppressible and nonsuppressible insulin-like activities in human serum and their physiologic significance. An insulin assay with adipose tissue of increased precision and specificity. J Clin Invest 42:1816–1834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fryburg DA, Jahn LA, Hill SA, Oliveras DM, Barrett EJ (1995) Insulin and insulin-like growth factor-I enhance human skeletal muscle protein anabolism during hyperaminoacidemia by different mechanisms. J Clin Invest 96:1722–1729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gagné A, Wei SQ, Fraser WD, Julien P (2009) Absorption, transport, and bioavailability of vitamin e and its role in pregnant women. J Obstet Gynaecol Can 31:210–217

    Article  PubMed  Google Scholar 

  • García-Fernández M, Castilla-Cortázar I, Díaz-Sánchez M, Díez Caballero F, Castilla A, Díaz Casares A, Varela-Nieto I, González-Barón S (2003) Effect of IGF-I on total serum antioxidant status in cirrhotic rats. J Physiol Biochem 59:145–146

    Article  PubMed  Google Scholar 

  • García-Fernández M, Castilla-Cortázar I, Díaz-Sanchez M, Navarro I, Puche JE, Castilla A, Casares AD, Clavijo E, González-Barón S (2005) Antioxidant effects of insulin-like growth factor-I (IGF-I) in rats with advanced liver cirrhosis. BMC Gastroenterol 5:7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • García-Fernández M, Delgado G, Puche JE, González-Barón S, Cortázar IC (2008) Low doses of insulin-like growth factor I improve insulin resistance, lipid metabolism, and oxidative damage in aging rats. Endocrinology 149:2433–2442

    Article  PubMed  CAS  Google Scholar 

  • Gheita TA, Gamal SM, El-Kattan E (2011) Uterine–umbilical artery Doppler velocimetry and pregnancy outcome in SLE patients: relation to disease manifestations and activity. Egypt Rheumatol 33:187–193

    Article  Google Scholar 

  • Gibson JM, Aplin JD, White A, Westwood M (2001) Regulation of IGF bioavailability in pregnancy. Mol Hum Reprod 7:79–87

    Article  CAS  PubMed  Google Scholar 

  • Giudice LC (1992) Insulin-like growth factors and ovarian follicular development. Endocr Rev 13:641–669

    CAS  PubMed  Google Scholar 

  • Giudice LC, Saleh W (1995) Growth factors in reproduction. Trends Endocrinol Metab 6:60–69

    Article  CAS  PubMed  Google Scholar 

  • Goldenberg RL, Cliver SP (1997) Small for gestational age and intrauterine growth restriction: definitions and standards. Clin Obstet Gynecol 40:704–714

    Article  CAS  PubMed  Google Scholar 

  • Gómez JM (2008) Growth hormone and insulin-like growth factor-I as an endocrine axis in Alzheimer’s disease. Endocr Metab Immune Disord Drug Targets 8:143–151

    Article  PubMed  Google Scholar 

  • Gómez-Gómez M (2012) Clasificación de los niños recién nacidos. Rev Mex Pediatr 79:32–39

    Google Scholar 

  • Gonzalez R, Merialdi M, Lincetto O, Lauer J, Becerra C, Castro R, García P, Saugstad OD, Villar J (2006) Reduction in neonatal mortality in Chile between 1990 and 2000. Pediatrics 117:e949–e954

    Article  PubMed  Google Scholar 

  • Grammatopoulos DK (2008) Placental corticotrophin-releasing hormone and its receptors in human pregnancy and labour: still a scientific enigma. J Neuroendocrinol 20:433–438

    Article  CAS  Google Scholar 

  • Guntur AR, Rosen CJ (2013) IGF-1 regulation of key signaling pathways in bone. Bonekey Rep 2:437

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hadden JW, Malec PH, Coto J, Hadden EM (1992) Thymic involution in aging: prospects for correction. Ann N Y Acad Sci 673:231–239

    Article  CAS  PubMed  Google Scholar 

  • Han VKM, Carter AM (2001) Control of growth and development of the feto-placental unit. Curr Opin Pharmacol 1:632–640

    Article  CAS  PubMed  Google Scholar 

  • Handwerger S, Freemark M (2000) The roles of placental growth hormone and placental lactogen in the regulation of human fetal growth and development. J Pediatr Endocrinol Metab 13:343–356

    CAS  PubMed  Google Scholar 

  • Harris LK, Crocker IP, Baker PN, Aplin JD, Westwood M (2011) IGF2 actions on trophoblast in human placenta are regulated by the insulin-like growth factor 2 receptor, which can function as both a signaling and clearance receptor. Biol Reprod 84:440–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hattersley AT, Tooke JE (1999) The fetal insulin hypothesis: an alternative explanation of the association of low birthweight with diabetes and vascular disease. Lancet 353:1789–1792

    Article  CAS  PubMed  Google Scholar 

  • Hay WW, Thureen PJ, Anderson MS (2001) Intrauterine growth restriction. NeoReviews 2:129–138

    Article  Google Scholar 

  • Hiden U, Glitzner E, Hartmann M, Desoye G (2009) Insulin and the IGF system in the human placenta of normal and diabetic pregnancies. J Anat 215:60–68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill DJ, Freemark M, Strain AJ, Handwerger S, Milner RD (1988) Placental lactogen and growth hormone receptors in human fetal tissues: relationship to fetal plasma human placental lactogen concentrations and fetal growth. J Clin Endocrinol Metab 66:1283–1290

    Article  CAS  PubMed  Google Scholar 

  • Hills FA, English J, Chard T (1996) Circulating levels of IGF-I and IGF-binding protein-1 throughout pregnancy: relation to birthweight and maternal weight. J Endocrinol 148:303–309

    Article  CAS  PubMed  Google Scholar 

  • Hirschberg R (1996) Insulin-like growth factor I in the kidney. Miner Electrolyte Metab 22:128–132

    CAS  PubMed  Google Scholar 

  • Holbourn KP, Acharya KR, Perbal B (2008) The CCN family of proteins: structure-function relationships. Trends Biochem Sci 33:461–473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossenlopp P, Seurin D, Segovia-Quinson B, Hardouin S, Binoux M (1986) Analysis of serum insulin-like growth factor binding proteins using western blotting: use of the method for titration of the binding proteins and competitive binding studies. Anal Biochem 154:138–143

    Article  CAS  PubMed  Google Scholar 

  • Hu SI, Carozza M, Klein M, Nantermet P, Luk D, Crowl RM (1998) Human HtrA, an evolutionarily conserved serine protease identified as a differentially expressed gene product in osteoarthritic cartilage. J Biol Chem 273:34406–34412

    Article  CAS  PubMed  Google Scholar 

  • Hwa V, Oh Y, Rosenfeld RG (1999) The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr Rev 20:761–787

    CAS  PubMed  Google Scholar 

  • Iliodromiti Z, Antonakopoulos N, Sifakis S, Tsikouras P, Daniilidis A, Dafopoulos K, Botsis D, Vrachnis N (2012) Endocrine, paracrine, and autocrine placental mediators in labor. Hormones 11:397–409

    Article  PubMed  Google Scholar 

  • Isaranurug S, Mo-suwan L, Choprapawon C (2007) A population-based cohort study of effect of maternal risk factors on low birthweight in Thailand. J Med Assoc Thai 90:2559–2564

    PubMed  Google Scholar 

  • Jacobsson B, Ahlin K, Francis A, Hagberg G, Hagberg H, Gardosi J (2008) Cerebral palsy and restricted growth status at birth: population-based case–control study. BJOG 115:1250–1255

    Article  CAS  PubMed  Google Scholar 

  • Jameson JL (1999) Laron Z: Laron syndrome—primary growth hormone resistance. Horm Resist Syndr Contemp Endocrinol 17–37

    Google Scholar 

  • Jaquet D, Vidal H, Hankard R, Czernichow P, Levy-Marchal C (2001) Impaired regulation of glucose transporter 4 gene expression in insulin resistance associated with in utero undernutrition. J Clin Endocrinol Metab 86:3266–3271

    CAS  PubMed  Google Scholar 

  • Jones JI, Clemmons DR (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 16:3–34

    CAS  PubMed  Google Scholar 

  • Juul A (2003) Serum levels of insulin-like growth factor I and its binding proteins in health and disease. Growth Horm IGF Res 13:113–170

    Article  CAS  PubMed  Google Scholar 

  • Kajimura S, Aida K, Duan C (2005) Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proc Natl Acad Sci U S A 102:1240–1245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaludjerovic J, Ward WE (2012) The interplay between estrogen and fetal adrenal cortex. J Nutr Metab. doi:10.1155/2012/837901

    PubMed  PubMed Central  Google Scholar 

  • Karteris E, Grammatopoulos DK, Randeva HS, Hillhouse EW (2001) The role of corticotropin-releasing hormone receptors in placenta and fetal membranes during human pregnancy. Mol Genet Metab 72:287–296

    Article  CAS  PubMed  Google Scholar 

  • Koutsaki M, Sifakis S, Zaravinos A, Koutroulakis D, Koukoura O, Spandidos DA (2011) Decreased placental expression of hPGH, IGF-I and IGFBP-1 in pregnancies complicated by fetal growth restriction. Growth Horm IGF Res 21:31–36

    Article  CAS  PubMed  Google Scholar 

  • Kramer MS, Olivier M, McLean FH, Willis DM, Usher RH (1990) Impact of intrauterine growth retardation and body proportionality on fetal and neonatal outcome. Pediatrics 86:707–713

    CAS  PubMed  Google Scholar 

  • Kumar P, Magon N (2012) Hormones in pregnancy. Niger Med J 53:179–183

    Article  PubMed  PubMed Central  Google Scholar 

  • Lacroix MC, Guibourdenche J, Frendo JL, Muller F, Evain-Brion D (2002) Human placental growth hormone--a review. Placenta 23(Suppl A):S87–S94

    Article  PubMed  Google Scholar 

  • Lamson G, Giudice LC, Rosenfeld RG (1991) Insulin-like growth factor binding proteins: structural and molecular relationships. Growth Factors 5:19–28

    Article  CAS  PubMed  Google Scholar 

  • Landreth KS, Narayanan R, Dorshkind K (1992) Insulin-like growth factor-I regulates pro-B cell differentiation. Blood 80:1207–1212

    CAS  PubMed  Google Scholar 

  • Laron Z (1984) Laron-type dwarfism (hereditary somatomedin deficiency): a review. Ergeb Inn Med Kinderheilkd 51:117–150

    CAS  PubMed  Google Scholar 

  • Laron Z (2001) Insulin-like growth factor 1 (IGF-1): a growth hormone. Mol Pathol 54:311–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laron Z, Pertzelan A, Mannheimer S (1966) Genetic pituitary dwarfism with high serum concentration of growth hormone – a new inborn error of metabolism? Isr J Med Sci 2:152–155

    CAS  PubMed  Google Scholar 

  • Lassalle P, Molet S, Janin A, Van der Heyden J, Tavernier J, Fiers W, Devos R, Tonnel AB (1996) ESM-1 is a novel human endothelial cell-specific molecule expressed in lung and regulated by cytokines. J Biol Chem 271:20458–20464

    Article  CAS  PubMed  Google Scholar 

  • Lawrence JB, Oxvig C, Overgaard MT, Sottrup-Jensen L, Gleich GJ, Hays LG, Yates JR, Conover CA (1999) The insulin-like growth factor (IGF)-dependent IGF binding protein-4 protease secreted by human fibroblasts is pregnancy-associated plasma protein-A. Proc Natl Acad Sci U S A 96:3149–3153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Roith D (1997) Seminars in medicine of the Beth Israel Deaconess Medical Center. Insulin-like growth factors. N Engl J Med 336:633–640

    Article  PubMed  Google Scholar 

  • Lee PD, Conover CA, Powell DR (1993) Regulation and function of insulin-like growth factor-binding protein-1. Proc Soc Exp Biol Med 204:4–29

    Article  CAS  PubMed  Google Scholar 

  • Lee ACC, Katz J, Blencowe H et al (2013) National and regional estimates of term and preterm babies born small for gestational age in 138 low-income and middle-income countries in 2010. Lancet Glob Health. doi:10.1016/S2214-109X(13)70006-8

    PubMed  PubMed Central  Google Scholar 

  • Leonard AJ, Evans IM, Pickard MR, Bandopadhyay R, Sinha AK, Ekins RP (2001) Thyroid hormone receptor expression in rat placenta. Placenta 22:353–359

    Article  CAS  PubMed  Google Scholar 

  • Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A (1993) 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

    CAS  PubMed  Google Scholar 

  • Livingstone C (2013) Insulin-like growth factor-I (IGF-I) and clinical nutrition. Clin Sci 125:265–280

    Article  CAS  PubMed  Google Scholar 

  • Lupu F, Terwilliger JD, Lee K, Segre GV, Efstratiadis A (2001) Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev Biol 229:141–162

    Article  CAS  PubMed  Google Scholar 

  • Majed BH, Khalil RA (2012) Molecular mechanisms regulating the vascular prostacyclin pathways and their adaptation during pregnancy and in the newborn. Pharmacol Rev 64:540–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Markestad T, Bergsjø P, Aakvaag A, Lie RT, Jacobsen G, Hoffman HJ, Bakketeig LS (1997) Prediction of fetal growth based on maternal serum concentrations of human chorionic gonadotropin, human placental lactogen and estriol. Acta Obstet Gynecol Scand Suppl 165:50–55

    CAS  PubMed  Google Scholar 

  • Martin AA, Tomas FM, Owens PC, Knowles SE, Ballard FJ, Read LC (1991) IGF-I and its variant, des-(1–3)IGF-I, enhance growth in rats with reduced renal mass. Am J Physiol 261:F626–F633

    CAS  PubMed  Google Scholar 

  • Maruo T, Murata K, Matsuo H, Samoto T, Mochizuki M (1995) Insulin-like growth factor-I as a local regulator of proliferation and differentiated function of the human trophoblast in early pregnancy. Early Pregnancy 1:54–61

    CAS  PubMed  Google Scholar 

  • Maulik D (2006) Management of fetal growth restriction: an evidence-based approach. Clin Obstet Gynecol 49:320–334

    Article  PubMed  Google Scholar 

  • McCormack SA, Glasser SR (1978) Ontogeny and regulation of a rat placental estrogen receptor. Endocrinology 102:273–280

    Article  CAS  PubMed  Google Scholar 

  • McKinnon T, Chakraborty C, Gleeson LM, Chidiac P, Lala PK (2001) 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 86:3665–3674

    Article  CAS  PubMed  Google Scholar 

  • Miller BH, Takahashi JS (2014) Central circadian control of female reproductive function. Front Endocrinol (Lausanne) 5:1–8

    CAS  Google Scholar 

  • Mitchell EA, Robinson E, Clark PM, Becroft DMO, Glavish N, Pattison NS, Pryor JE, Thompson JMD, Wild CJ (2004) Maternal nutritional risk factors for small for gestational age babies in a developed country: a case–control study. Arch Dis Child Fetal Neonatal Ed 89:F431–F435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muguerza B, Castilla-Cortázar I, García M, Quiroga J, Santidrián S, Prieto J (2001) Antifibrogenic effect in vivo of low doses of insulin-like growth factor-I in cirrhotic rats. Biochim Biophys Acta 1536:185–195

    Article  CAS  PubMed  Google Scholar 

  • Murphy LJ, Friesen HG (1988) Differential effects of estrogen and growth hormone on uterine and hepatic insulin-like growth factor I gene expression in the ovariectomized hypophysectomized rat. Endocrinology 122:325–332

    Article  CAS  PubMed  Google Scholar 

  • Murphy M, Pykett MJ, Harnish P, Zang KD, George DL (1993) Identification and characterization of genes differentially expressed in meningiomas. Cell Growth Differ 4:715–722

    CAS  PubMed  Google Scholar 

  • Murphy VE, Smith R, Giles WB, Clifton VL (2006) Endocrine regulation of human fetal growth: the role of the mother, placenta, and fetus. Endocr Rev 27:141–169

    Article  PubMed  Google Scholar 

  • Muyan M, Boime I (1997) Secretion of chorionic gonadotropin from human trophoblasts. Placenta 18:237–241

    Article  CAS  PubMed  Google Scholar 

  • Myers RB, Rwayitare K, Richey L, Lem J, Castellot JJ (2012) CCN5 expression in mammals. III. Early embryonic mouse development. J Cell Commun Signal 6:217–223

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen TQ, Roestenberg P, van Nieuwenhoven FA et al (2008) CTGF inhibits BMP-7 signaling in diabetic nephropathy. J Am Soc Nephrol 19:2098–2107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nissley P, Lopaczynski W (1991) Insulin-like growth factor receptors. Growth Factors 5:29–43

    Article  CAS  PubMed  Google Scholar 

  • Oh Y, Nagalla SR, Yamanaka Y, Kim HS, Wilson E, Rosenfeld RG (1996) Synthesis and characterization of insulin-like growth factor-binding protein (IGFBP)-7: recombinant human mac25 protein specifically binds IGF-I and -II. J Biol Chem 271:30322–30325

    Article  CAS  PubMed  Google Scholar 

  • Ohlsson C, Mohan S, Sjögren K, Tivesten Å, Isgaard J, Isaksson O, Jansson JO, Svensson J (2009) The role of liver-derived insulin-like growth factor-I. Endocr Rev 30:494–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parraguez VH, Urquieta B, De los Reyes M, Gonzalez-Bulnes A, Astiz S, Munoz A (2013) Steroidogenesis in sheep pregnancy with intrauterine growth retardation by high-altitude hypoxia: effects of maternal altitudinal status and antioxidant treatment. Reprod Fertil Dev 25:639–645

    Article  CAS  PubMed  Google Scholar 

  • Pérez R, García-Fernández M, Díaz-Sánchez M, Puche JE, Delgado G, Conchillo M, Muntané J, Castilla-Cortázar Larrea I (2008) Mitochondrial protection by low doses of insulin-like growth factor-I in experimental cirrhosis. World J Gastroenterol 14:2731–2739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perry HM (1999) The endocrinology of aging. Clin Chem 45:1369–1376

    CAS  PubMed  Google Scholar 

  • Petraglia F (1997) Inhibin, activin and follistatin in the human placenta - a new family of regulatory proteins. Placenta 18:3–8

    Article  CAS  PubMed  Google Scholar 

  • Petraglia F, Calza L, Giardino L, Sutton S, Marrama P, Rivier J, Genazzani AR, Vale W (1989) Identification of immunoreactive neuropeptide-γ in human placenta: localization, secretion, and binding sites. Endocrinology 124:2016–2022

    Article  CAS  PubMed  Google Scholar 

  • Powell-Braxton L, Hollingshead P, Warburton C, Dowd M, Pitts-Meek S, Dalton D, Gillett N, Stewart TA (1993) IGF-I is required for normal embryonic growth in mice. Genes Dev 7:2609–2617

    Article  CAS  PubMed  Google Scholar 

  • Puche JE, Castilla-Cortázar I (2012) Human conditions of insulin-like growth factor-I (IGF-I) deficiency. J Transl Med 10:224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puche JE, García-Fernández M, Muntané J, Rioja J, González-Barón S, Cortazar IC (2008) Low doses of insulin-like growth factor-I induce mitochondrial protection in aging rats. Endocrinology 149:2620–2627

    Article  CAS  PubMed  Google Scholar 

  • Rabinovici J, Goldsmith PC, Librach CL, Jaffe RB (1992) Localization and regulation of the activin-A dimer in human placental cells. J Clin Endocrinol Metab 75:571–576

    CAS  PubMed  Google Scholar 

  • Rajaram S, Baylink DJ, Mohan S (1997) Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocr Rev 18:801–831

    CAS  PubMed  Google Scholar 

  • Randhawa R, Cohen P (2005) The role of the insulin-like growth factor system in prenatal growth. Mol Genet Metab 86:84–90

    Article  CAS  PubMed  Google Scholar 

  • Reece EA, Wiznitzer A, Le E, Homko CJ, Behrman H, Spencer EM (1994) The relation between human fetal growth and fetal blood levels of insulin-like growth factors I and II, their binding proteins, and receptors. Obstet Gynecol 84:88–95

    CAS  PubMed  Google Scholar 

  • Resnik R (2002) Intrauterine growth restriction. Obstet Gynecol 99:490–496

    PubMed  Google Scholar 

  • Riley SC, Leask R, Balfour C, Brennand JE, Groome NP (2000) Production of inhibin forms by the fetal membranes, decidua, placenta and fetus at parturition. Hum Reprod 15:578–583

    Article  CAS  PubMed  Google Scholar 

  • Rinderknecht E, Humbel RE (1976) Polypeptides with nonsuppressible insulin-like and cell-growth promoting activities in human serum: isolation, chemical characterization, and some biological properties of forms I and II. Proc Natl Acad Sci U S A 73:2365–2369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rinderknecht E, Humbel RE (1978a) The amino acid sequence of human insulin-like growth factor I and its structural homology with proinsulin. J Biol Chem 253:2769–2776

    CAS  PubMed  Google Scholar 

  • Rinderknecht E, Humbel RE (1978b) Primary structure of human insulin-like growth factor II. FEBS Lett 89:283–286

    Article  CAS  PubMed  Google Scholar 

  • Romo A, Carceller R, Tobajas J (2009) Intrauterine growth retardation (IUGR): epidemiology and etiology. Pediatr Endocrinol Rev 6:332–336

    PubMed  Google Scholar 

  • Rosenbloom AL (1999) Growth hormone insensitivity: physiologic and genetic basis, phenotype, and treatment. J Pediatr 135:280–289

    Article  CAS  PubMed  Google Scholar 

  • Saglam O, Dai F, Husain S, Zhan Y, Toruner G, Haines GK (2014) Matricellular protein CCN1 (CYR61) expression is associated with high-grade ductal carcinoma in situ. Hum Pathol 45:1269–1275

    Article  CAS  PubMed  Google Scholar 

  • Saleem T, Sajjad N, Fatima S, Habib N, Ali SR, Qadir M (2011) Intrauterine growth retardation – small events, big consequences. Ital J Pediatr 37:41

    Article  PubMed  PubMed Central  Google Scholar 

  • Salmon WD Jr, Daughaday WH (1957) A hormonally controlled serum factor which stimulates sulfate incorporation by cartilage in vitro. J Lab Clin Med 49:825–836

    CAS  PubMed  Google Scholar 

  • Sánchez-Vera I, Bonet B, Viana M, Quintanar A, López-Salva A (2005) Increased low-density lipoprotein susceptibility to oxidation in pregnancies and fetal growth restriction. Obstet Gynecol 106:345–351

    Article  PubMed  Google Scholar 

  • Santos IS, Barros AJD, Matijasevich A, Domingues MR, Barros FC, Victora CG (2011) Cohort profile: the 2004 pelotas (BRAZIL) birth cohort study. Int J Epidemiol 40:1461–1468

    Article  PubMed  PubMed Central  Google Scholar 

  • Sara VR, Hall K (1990) Insulin-like growth factors and their binding proteins. Physiol Rev 70:591–614

    CAS  PubMed  Google Scholar 

  • Schiaffino S, Mammucari C (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 1:4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmiegelow C, Minja D, Oesterholt M et al (2012) Factors associated with and causes of perinatal mortality in northeastern Tanzania. Acta Obstet Gynecol Scand 91:1061–1068

    Article  PubMed  Google Scholar 

  • Setia S, Sridhar MG (2009) Changes in GH/IGF-1 axis in intrauterine growth retardation: consequences of fetal programming? Horm Metab Res 41:791–798

    Article  CAS  PubMed  Google Scholar 

  • Sferruzzi-Perri AN, Owens JA, Pringle KG, Robinson JS, Roberts CT (2006) Maternal insulin-like growth factors-I and -II act via different pathways to promote fetal growth. Endocrinology 147:3344–3355

    Article  CAS  PubMed  Google Scholar 

  • Shah A, Faundes A, Machoki M et al (2008) Methodological considerations in implementing the WHO global survey for monitoring maternal and perinatal health. Bull World Health Organ 86:126–131

    Article  PubMed  PubMed Central  Google Scholar 

  • Shanker YG, Rao AJ (1999) Progesterone receptor expression in the human placenta. Mol Hum Reprod 5:481–486

    Article  CAS  PubMed  Google Scholar 

  • Silva JR, Figueiredo JR, van den Hurk R (2009) Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 71:1193–1208

    Article  CAS  PubMed  Google Scholar 

  • Skrtic S, Wallenius V, Ekberg S, Brenzel A, Gressner AM, Jansson JO (1997) Insulin-like growth factors stimulate expression of hepatocyte growth factor but not transforming growth factor beta1 in cultured hepatic stellate cells. Endocrinology 138:4683–4689

    CAS  PubMed  Google Scholar 

  • Smith GC, Pell JP, Walsh D (2001) Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129,290 births. Lancet 357:2002–2006

    Article  CAS  PubMed  Google Scholar 

  • Sorem KA, Siler-Khodr TM (1997) Effect of IGF-I on placental thromboxane and prostacyclin release in severe intrauterine growth retardation. J Matern Fetal Med 6:341–350

    CAS  PubMed  Google Scholar 

  • Street ME, Seghini P, Feini S, Ziveri MA, Volta C, Martorana D, Viani I, Gramellini D, Bernasconi S (2006) Changes in interleukin-6 and IGF system and their relationships in placenta and cord blood in newborns with fetal growth restriction compared with controls. Eur J Endocrinol 155:567–574

    Article  CAS  PubMed  Google Scholar 

  • Sun IYC, Overgaard MT, Oxvig C, Giudice LC (2002) Pregnancy-associated plasma protein A proteolytic activity is associated with the human placental trophoblast cell membrane. J Clin Endocrinol Metab 87:5235–5240

    Article  CAS  PubMed  Google Scholar 

  • Tahimic CGT, Wang Y, Bikle DD (2013) Anabolic effects of IGF-1 signaling on the skeleton. Front Endocrinol (Lausanne). doi:10.3389/fendo.2013.00006

    Google Scholar 

  • Tzschoppe A, Riedel C, von Kries R et al (2015) Differential effects of low birthweight and intrauterine growth restriction on umbilical cord blood insulin-like growth factor concentrations. Clin Endocrinol (Oxf). doi:10.1111/cen.12844

    Google Scholar 

  • Valsamakis G, Kanaka-Gantenbein C, Malamitsi-Puchner A, Mastorakos G (2006) Causes of intrauterine growth restriction and the postnatal development of the metabolic syndrome. Ann N Y Acad Sci 1092:138–147

    Article  CAS  PubMed  Google Scholar 

  • Vehaskari VM, Aviles DH, Manning J (2001) Prenatal programming of adult hypertension in the rat. Kidney Int 59:238–245

    Article  CAS  PubMed  Google Scholar 

  • Velloso CP (2008) Regulation of muscle mass by growth hormone and IGF-I. Br J Pharmacol 154:557–568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verhaeghe J, Bougoussa M, Van Herck E, De Zegher F, Hennen G, Igout A (2000) Placental growth hormone and IGF-I in a pregnant woman with Pit-1 deficiency. Clin Endocrinol (Oxf) 53:645–647

    Article  CAS  Google Scholar 

  • Victora CG, Barros FC (2006) Cohort profile: the 1982 Pelotas (Brazil) birth cohort study. Int J Epidemiol 35:237–242

    Article  PubMed  Google Scholar 

  • Victora CG, Hallal PC, Araújo CLP, Menezes AMB, Wells JCK, Barros FC (2008) Cohort profile: the 1993 pelotas (Brazil) birth cohort study. Int J Epidemiol 37:704–709

    Article  PubMed  Google Scholar 

  • Villalpando I, López-Olmos V (2003) Insulin-like growth factor I (IGF-I) regulates endocrine activity of the embryonic testis in the mouse. J Steroid Biochem Mol Biol 86:151–158

    Article  CAS  PubMed  Google Scholar 

  • Vincent AM, Feldman EL (2002) Control of cell survival by IGF signaling pathways. Growth Horm IGF Res 12:193–197

    Article  CAS  PubMed  Google Scholar 

  • Voigt HJ, Becker V (1992) Doppler flow measurements and histomorphology of the placental bed in uteroplacental insufficiency. J Perinat Med 20:139–147

    Article  CAS  PubMed  Google Scholar 

  • Vuorela P, Hatva E, Lymboussaki A, Kaipainen A, Joukov V, Persico MG, Alitalo K, Halmesmäki E (1997) Expression of vascular endothelial growth factor and placenta growth factor in human placenta. Biol Reprod 56:489–494

    Article  CAS  PubMed  Google Scholar 

  • Walsh PT, Smith LM, O’Connor R (2002) Insulin-like growth factor-1 activates Akt and Jun N-terminal kinases (JNKs) in promoting the survival of T lymphocytes. Immunology 107:461–471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YP, Walsh SW, Guo JD, Zhang JY (1991) Maternal levels of prostacyclin, thromboxane, vitamin E, and lipid peroxides throughout normal pregnancy. Am J Obstet Gynecol 165:1690–1694

    Article  CAS  PubMed  Google Scholar 

  • Wang S et al (2012) WISP1 (CCN4) autoregulates its expression and nuclear trafficking of β-catenin during oxidant stress with limited effects upon neuronal autophagy. Curr Neurovasc Res 9(2):91–101. doi:10.2174/156720212800410858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weinstock M (2005) The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 19:296–308

    Article  CAS  PubMed  Google Scholar 

  • WHO (2004) Low birthweight: country, regional and global estimates. UNICEF Publications, UNICEF. World Health Organ. http://www.unicef.org/publications/index_24840.html. Accessed 18 May 2015

  • Wolfahrt S, Kleine B, Rossmanith WG (1998) Detection of gonadotrophin releasing hormone and its receptor mRNA in human placental trophoblasts using in-situ reverse transcription-polymerase chain reaction. Mol Hum Reprod 4:999–1006

    Article  CAS  PubMed  Google Scholar 

  • Woods KA, Camacho-Hübner C, Savage MO, Clark AJ (1996) Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N Engl J Med 335:1363–1367

    Article  CAS  PubMed  Google Scholar 

  • Woods KA, van Helvoirt M, Ong KKL, Mohn A, Levy J, de Zegher F, Dunger DB (2002) The somatotropic axis in short children born small for gestational age: relation to insulin resistance. Pediatr Res 51:76–80

    Article  CAS  PubMed  Google Scholar 

  • Wu SM, Arnold LL, Rone J, Trivadi M, Chan WY (1999) Effect of pregnancy-specific beta 1-glycoprotein on the development of preimplantation embryo. Proc Soc Exp Biol Med 220:169–177

    Article  CAS  PubMed  Google Scholar 

  • Wynne F, Ball M, McLellan AS, Dockery P, Zimmermann W, Moore T (2006) Mouse pregnancy-specific glycoproteins: tissue-specific expression and evidence of association with maternal vasculature. Reproduction 131:721–732

    Article  CAS  PubMed  Google Scholar 

  • Yakar S, Courtland HW, Clemmons D (2010) IGF-1 and bone: new discoveries from mouse models. J Bone Miner Res 25:2267–2276

    Article  CAS  Google Scholar 

  • Yu H, Rohan T (2000) Role of the insulin-like growth factor family in cancer development and progression. J Natl Cancer Inst 92:1472–1489

    Article  CAS  PubMed  Google Scholar 

  • Zachariades E, Mparmpakas D, Pang Y, Rand-Weaver M, Thomas P, Karteris E (2012) Changes in placental progesterone receptors in term and preterm labour. Placenta 33:367–372

    Article  CAS  PubMed  Google Scholar 

  • Zapf J, Schoenle E, Froesch ER (1978) Insulin-like growth factors I and II: some biological actions and receptor binding characteristics of two purified constituents of nonsuppressible insulin-like activity of human serum. Eur J Biochem 87:285–296

    Article  CAS  PubMed  Google Scholar 

  • Zepeda-Monreal J, Rodríguez-Balderrama I, Del Carmen Ochoa-Correa E, de la O-Cavazos ME, Ambriz-López R (2012) Risk factors associated with intrauterine growth restriction in newborns attended in a university hospital. Rev Med Inst Mex Seguro Soc 50:173–181

    PubMed  Google Scholar 

  • Zhang X, Sliwowska JH, Weinberg J (2005) Prenatal alcohol exposure and fetal programming: effects on neuroendocrine and immune function. Exp Biol Med (Maywood) 230:376–388

    CAS  Google Scholar 

  • Zhou Y, Xu BC, Maheshwari HG et al (1997) A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse). Proc Natl Acad Sci U S A 94:13215–13220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziyan J, Huaibin R, Xiaotian M, Guangtong S, Xiaoqing C, Zijiang D, Ziyue J, We D, Lizhou S (2010) Regulation of progesterone receptor A and B expression in human preterm, term, and postterm placental villi. Acta Obstet Gynecol Scand 89:705–711

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors would like to express our gratitude to MCs Gabriel Amador Aguirre, Ing. Karl Steinmetz, Dr. Mariano García-Magariño Alonso, Dr. Luis Espinosa Sierra and Joshua S. Williams for their invaluable help. This work was possible thanks to the financial help of “Fundación de Investigación HM Hospitales” and “Tecnológico de Monterrey”.

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Authors and Affiliations

  1. Doctoral Department, Centro de Investigación Transferencia en Salud (CITES), Escuela Nacional de Medicina, Tecnológico de Monterrey, Avenida Morones Prieto No. 3000 Pte, Col. Los Doctores, 64710, Monterrey, NL, Mexico

    I. Martín-Estal, R. G. de la Garza & I. Castilla-Cortázar

  2. Fundación de Investigación HM Hospitales, Plaza Conde Valle Súchil, 2, 28015, Madrid, Spain

    I. Castilla-Cortázar

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  1. I. Martín-Estal
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  2. R. G. de la Garza
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  3. I. Castilla-Cortázar
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Correspondence to I. Castilla-Cortázar .

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  1. KU Leuven, Leuven, Belgium

    Bernd Nilius

  2. Cardiovascular Research Center, Loyola University Chicago, Maywood, Illinois, USA

    Pieter de Tombe

  3. Walther-Straub-Institut für Pharmakologi, München, Germany

    Thomas Gudermann

  4. Department of Neurobiology, Max-Planck-Institute, Göttingen, Germany

    Reinhard Jahn

  5. Department of Cytobiology, University of Marburg, Marburg, Germany

    Roland Lill

  6. Cardiff School of Biosciences, Cardiff University, Cardiff, United Kingdom

    Ole H. Petersen

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Martín-Estal, I., de la Garza, R.G., Castilla-Cortázar, I. (2016). Intrauterine Growth Retardation (IUGR) as a Novel Condition of Insulin-Like Growth Factor-1 (IGF-1) Deficiency. In: Nilius, B., de Tombe, P., Gudermann, T., Jahn, R., Lill, R., Petersen, O. (eds) Reviews of Physiology, Biochemistry and Pharmacology Vol. 170. Reviews of Physiology, Biochemistry and Pharmacology, vol 170. Springer, Cham. https://doi.org/10.1007/112_2015_5001

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