Role of insulin-like growth factors in embryonic and postnatal growth

A developmental analysis of growth kinetics in mouse embryos carrying null mutations of the genes encoding insulin-like growth factor I (IGF-I), IGF-II, and the type 1 IGF receptor (IGF1R), alone or in combination, defined the onset of mutational effects leading to growth deficiency and indicated that between embryonic days 11.0 and 12.5, IGF1R serves only the in vivo mitogenic signaling of IGF-II. From E13.5 onward, IGF1R interacts with both IGF-I and IGF-II, while IGF-II recognizes an additional unknown receptor (XR). In contrast with the embryo proper, placental growth is served exclusively by an IGF-II-XR interaction. Additional genetic data suggested that the type 2IGF/mannose 6-phosphate receptor is an unlikely candidate for XR. Postnatal growth curves indicated that surviving Igf-1(-/-) mutants, which are infertile and exhibit delayed bone development, continue to grow with a retarded rate after birth in comparison with wild-type littermates and become 30% of normal weight as adults.

[1]  R. Hammer,et al.  Relative growth of the skull and postcranium in giant transgenic mice. , 1990, Genetical research.

[2]  P. Payne,et al.  Growth of the Foetus , 1967, Nature.

[3]  H. Green,et al.  A dual effector theory of growth-hormone action. , 1985, Differentiation; research in biological diversity.

[4]  M. Watson,et al.  Insulin-like growth factor gene expression during rat embryonic development. , 1987, Endocrinology.

[5]  M. Czech,et al.  Direct demonstration of rapid insulin-like growth factor II Receptor internalization and recycling in rat adipocytes. Insulin stimulates 125I-insulin-like growth factor II degradation by modulating the IGF-II receptor recycling process. , 1985, The Journal of biological chemistry.

[6]  P. D. Gluckman,et al.  7 – THE REGULATION OF FETAL GROWTH , 1986 .

[7]  G. Bell,et al.  Growth hormone stimulates sequential induction of c-myc and insulin-like growth factor I expression in vivo. , 1987, Endocrinology.

[8]  Tyler Sa,et al.  Dynamics of normal growth. , 1965 .

[9]  A. Huggett,et al.  The relationship between mammalian foetal weight and conception age , 1951, The Journal of physiology.

[10]  R. Humbel,et al.  Insulin-like growth factors I and II. , 1990, European journal of biochemistry.

[11]  A. Mclaren,et al.  GENETIC AND ENVIRONMENTAL EFFECTS ON FOETAL AND PLACENTAL GROWTH IN MICE. , 1965, Journal of reproduction and fertility.

[12]  G. Schultz,et al.  Expression of genes for insulin and insulin‐like growth factors and receptors in early postimplantation mouse embryos and embryonal carcinoma cells , 1990, Molecular reproduction and development.

[13]  T. Chard.  Hormonal control of growth in the human fetus. , 1989, The Journal of endocrinology.

[14]  R. Baserga,et al.  Cell cycle and growth control. , 1993, Critical reviews in eukaryotic gene expression.

[15]  J. Baker,et al.  Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r) , 1993, Cell.

[16]  R. Hammer,et al.  Growth allometry of the organs in giant transgenic mice. , 1987, Endocrinology.

[17]  E. Macdowell,et al.  THE PRENATAL GROWTH OF THE MOUSE , 1927, The Journal of general physiology.

[18]  W. Sly,et al.  Binding of insulin-like growth factor II (IGF-II) by human cation-independent mannose 6-phosphate receptor/IGF-II receptor expressed in receptor-deficient mouse L cells. , 1990, Cell regulation.

[19]  W. Beamer,et al.  New mouse dw allele: genetic location and effects on lifespan and growth hormone levels. , 1980, The Journal of heredity.

[20]  Sikov Mr,et al.  Prenatal growth of the rat. , 1970 .

[21]  D. Johnson.  Further observations on the hairpin-tail ( T hp ) mutation in the mouse , 1974 .

[22]  A. Bartke,et al.  Etiology of growth hormone deficiency in little, Ames, and Snell dwarf mice. , 1983, Endocrinology.

[23]  James M. Roberts,et al.  Cyclin-dependent regulation of G1 in mammalian fibroblasts. , 1993, Science.

[24]  V. Sara,et al.  Expression of IGF-I and -II mRNA in the brain and craniofacial region of the rat fetus. , 1991, Development.

[25]  Anita B. Roberts,et al.  Peptide Growth Factors and Their Receptors I , 1990, Springer Study Edition.

[26]  G. Snell.  DWARF, A NEW MENDELIAN RECESSIVE CHARACTER OF THE HOUSE MOUSE. , 1929, Proceedings of the National Academy of Sciences of the United States of America.

[27]  P. Tam,et al.  Retarded development of XO conceptuses during early pregnancy in the mouse. , 1983, Journal of reproduction and fertility.

[28]  M. Winick,et al.  Quantitative changes in DNA, RNA, and protein during prenatal and postnatal growth in the rat. , 1965, Developmental biology.

[29]  Larry W. Swanson,et al.  Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene pit-1 , 1990, Nature.

[30]  Nancy A. Jenkins,et al.  GHRH receptor of little mice contains a missense mutation in the extracellular domain that disrupts receptor function , 1993, Nature Genetics.

[31]  G. Bell,et al.  Tissue distribution of insulin-like growth factor I and II messenger ribonucleic acid in the adult rat. , 1987, Endocrinology.

[32]  W. Daughaday,et al.  A hormonally controlled serum factor which stimulates sulfate incorporation by cartilage in vitro. , 1957, The Journal of laboratory and clinical medicine.

[33]  A. Pardee.  G1 events and regulation of cell proliferation. , 1989, Science.

[34]  C. M. Osborn,et al.  A STUDY OF NATURAL GROWTH AND OSSIFICATION IN HEREDITARY DWARF MICE1 , 1938 .

[35]  M. Rosenfeld,et al.  Anterior pituitary development: Short tales from dwarf mice , 1992, Cell.

[36]  A. Efstratiadis,et al.  Parental imprinting of the mouse insulin-like growth factor II gene , 1991, Cell.

[37]  J. Pintar,et al.  The embryonic pattern of rat insulin-like growth factor-I gene expression suggests a role in induction and early growth of the liver. , 1992, Endocrinology.

[38]  R. Palmiter,et al.  Regulation of insulin-like growth factor I gene expression by growth hormone. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[39]  A. Dahlström,et al.  Regulation by growth hormone of number of chondrocytes containing IGF-I in rat growth plate. , 1986, Science.

[40]  S. Camper,et al.  The Pit-1 transcription factor gene is a candidate for the murine Snell dwarf mutation. , 1990, Genomics.

[41]  D. James.  Some effects of immunological factors on gestation in mice. , 1967, Journal of reproduction and fertility.

[42]  A G Cock,et al.  Genetical Aspects of Metrical Growth and Form in Animals , 1966, The Quarterly Review of Biology.

[43]  L. Harrison,et al.  Delineation of atypical insulin receptors from classical insulin and type I insulin-like growth factor receptors in human placenta. , 1989, The Biochemical journal.

[44]  P. J. Brooks,et al.  Growth hormone dependence of somatomedin-C/insulin-like growth factor-I and insulin-like growth factor-II messenger ribonucleic acids. , 1987, Molecular endocrinology.

[45]  D. Evain-Brion.  Hormonal regulation of fetal growth. , 1994, Hormone research.

[46]  C. P. Leblond,et al.  Increase in Cell Number as a Factor in the Growth of the Organs and Tissues of the Young Male Rat , 1962 .

[47]  W. Daughaday.  A Personal History of the Origin of the Somatomedin Hypothesis and Recent Challenges to Its Validity , 2015, Perspectives in biology and medicine.

[48]  A. Louvi,et al.  Rescue of the T-associated maternal effect in mice carrying null mutations in Igf-2 and Igf2r, two reciprocally imprinted genes. , 1993, Development.

[49]  C. Roberts,et al.  Growth hormone regulates the abundance of insulin-like growth factor I RNA in adult rat liver. , 1986, The Journal of biological chemistry.

[50]  D. Johnson.  Hairpin-tail: a case of post-reductional gene action in the mouse egg. , 1974, Genetics.

[51]  E. Froesch,et al.  Recombinant human insulin-like growth factor I stimulates growth and has distinct effects on organ size in hypophysectomized rats. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[52]  C. Bondy,et al.  Insulin-like growth factor-II and its binding proteins in placental development. , 1992, Endocrinology.

[53]  Insulin-Like Growth Factors , 1991 .

[54]  A. Lindahl,et al.  Effects of growth hormone and insulin-like growth factor-I on colony formation of rabbit epiphyseal chondrocytes at different stages of maturation. , 1987, Journal of Endocrinology.

[55]  G. Bell,et al.  Identification, characterization, and regulation of a rat complementary deoxyribonucleic acid which encodes insulin-like growth factor-I. , 1987, Endocrinology.

[56]  J. Goedbloed.  The embryonic and postnatal growth of rat and mouse. II. The growth of the whole animal during the first 24 days after birth in two inbred mouse strains (CPB-S and DBA-2). , 1972, Acta anatomica.

[57]  J. Pintar,et al.  Pattern of the insulin-like growth factor II gene expression during early mouse embryogenesis. , 1990, Development.

[58]  R. Rugh,et al.  The mouse; its reproduction and development , 1968 .

[59]  W. J. Brammar,et al.  Expression of the IGF-II/mannose-6-phosphate receptor mRNA and protein in the developing rat. , 1990, Development.

[60]  R. Baserga,et al.  The role of the IGF1 receptor in the regulation of cdc2 mRNA levels in fibroblasts. , 1992, Experimental cell research.

[61]  A. Ullrich,et al.  Expression of a type I insulin-like growth factor receptor with low affinity for insulin-like growth factor II. , 1992, The Biochemical journal.

[62]  S. Nissley,et al.  Somatomedin activity in sera of genetically small mice. , 1980, Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme.

[63]  A. D'ercole,et al.  Ontogeny of somatomedin during development in the mouse. Serum concentrations, molecular forms, binding proteins, and tissue receptors. , 1980, Developmental biology.

[64]  G. Tregear,et al.  Histochemical localization of IGF-I and -II mRNA in the developing rat embryo. , 1987, Development.

[65]  D. Rappolee,et al.  Insulin-like growth factor II acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. , 1992, Genes & development.

[66]  Birgitta,et al.  An antibody that blocks insulin-like growth factor (IGF) binding to the type II IGF receptor is neither an agonist nor an inhibitor of IGF-stimulated biologic responses in L6 myoblasts. , 1987, The Journal of biological chemistry.

[67]  J. V. Van Wyk,et al.  Tissue and development specific regulation of a complex family of rat insulin-like growth factor I messenger ribonucleic acids. , 1988, Molecular endocrinology.

[68]  D. Barlow,et al.  The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus , 1991, Nature.

[69]  W. Beamer,et al.  Inherited ateliotic dwarfism in mice. Characteristics of the mutation, little, on chromosome 6. , 1976, The Journal of heredity.

[70]  A. Mclaren,et al.  PLACENTAL WEIGHT LOSS IN LATE PREGNANCY , 1965 .

[71]  B. Moats-Staats,et al.  Somatomedin-C/insulin-like growth factor-I and insulin-like growth factor-II mRNAs in rat fetal and adult tissues. , 1986, The Journal of biological chemistry.

[72]  F. Mailland,et al.  Effect of dihydroergocristine administration on serum prolactin and growth hormone levels in normal, hyperprolactinaemic, and acromegalic subjects: further evidence for pituitary dopamine deficiency in these conditions. , 1983, Acta endocrinologica.

[73]  A. Efstratiadis,et al.  A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting , 1990, Nature.

[74]  K. Hall,et al.  Insulin-like growth factors and their binding proteins. , 1990, Physiological reviews.