Cited by 536Growth Hormone and Insulin-like Growth FactorsFibroblast Growth Factor ResearchLiver physiology and pathology

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Insulin-like Growth Factor Binding Protein-1: Recent Findings and New Directions

Lee, P. D. K., Giudice, L. C., Conover, C. A., Powell, D. R.·1997·Experimental Biology and Medicine

DOI 10.3181/00379727-216-44182

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Abstract

In 1988, insulin-like growth factor-binding protein-1 (IGFBP-1) became the first characterized member of a group of structurally related soluble proteins which specifically bind and modulate the actions of the IGFs. Since then, a wealth of information has accumulated regarding the physiology of this dynamic serum protein. In this review, we update our 1993 summary (Lee PDK et al. Proc Soc Exp Biol Med 204:4-29) of the status of IGFBP-1 research. The IGFBP-1 protein sequence contains 12 N-terminal and 6 C-terminal cysteine residues which are conserved in other mammalian IGFBP-1 sequences and amongst other IGFBPs; both of the cysteine-rich regions are required for optimal IGF binding. The nonconserved IGFBP-1 midregion may act as both a hinge which defines ligand binding characteristics and as a specific target for protease activity. Integrin-binding and phosphorylation sites within the IGFBP-1 sequence have functional significance in vitro, but their physiologic relevance in vivo have not been defined. The human IGFBP-1 and IGFBP-3 genes are contiguous and located in close proximity to the homeobox A (HOXA) gene cluster on chromosome 7. The other IGFBP genes, located on chromosomes 2, 12, and 17, are also associated with HOX clusters, suggesting evolutionary linkage of the IGFBP and HOX gene families. Similarities between the hlGFBP-1 and phosphoenolpyruvate kinase (PEPCK) promoters, including regions conferring insulin, glucocorticoid, and cyclic adenosine-monophosphate responses, are consistent with our previous hypothesis that IGFBP-1 is involved in regulation of glucose metabolism. The tissue-specific patterns of IGFBP-1 gene expression in liver, kidney, decidua, and ovary may be due to stimulation of IGFBP-1 transcription by hepatic nuclear factor 1 (HNF1) proteins. Clinical and basic studies of IGFBP-1 physiology have been aided by several recently developed assay methods. Numerous investigations have confirmed that insulin, via inhibition of IGFBP-1 transcription, is the primary determinant of IGFBP-1 expression both in vitro and in viva IGF-I and IGF-II also have specific inhibitory effects on IGFBP-1 expression. Glucocorticoids and cAMP stimulate IGFBP-1 transcription, but these effects are observed only in conditions of low or absent insulin effect. Other stimulants of IGFBP-1 expression include thyroid hormones and epidermal growth factor. Phorbol ester stimulation of IGFBP-1 expression can supersede the effects of insulin in vitro; however, the mechanism and in vivo correlates of this effect have not been determined. Cytokines and, perhaps, growth hormones may affect IGFBP-1 expression, perhaps by altering the regulatory actions of insulin; this effect may have important clinical relevance. IGFBP-1 expression is upregulated in liver and (nonhuman) kidney during postinjury regeneration. The IGF-inhibitory actions of IGFBP-1 has been confirmed by numerous in vitro studies and several in vivo animal investigations, including administration of recombinant IGFBP-1 and IGFBP-1 transgenic models. IGFBP-1 has been shown to inhibit somatic linear growth, weight gain, tissue growth, and glucose metabolism. Moreover, IGFBP-1 appears to be a primary determinant of free IGF-I levels in serum. Excess levels of IGFBP-1 may contribute to growth failure in intrauterine growth restriction and in pediatric chronic renal failure, while low IGFBP-1 levels are associated with obesity and with cardiovascular risk factors in insulin resistance syndromes. Serum IGFBP-1 measurements may be useful biochemical marker in these pathologic conditions. IGFBP-1 is expressed in decidualized stromal cells of the uterine endometrium and in ovarian granulosa cells. IGFBP-1, together with IGFs, insulin, ovarian steroids, cytokines, and other factors, is involved in a complex system which regulates menstrual cycles, ovulation, decidualization, blastocyst implantation, and fetal growth. Models for the role of IGFBP-1 in female reproductive physiology are presented, and evidence for pathophysiologic roles in pre-eclampsia, polycystic ovarian syndrome, and uterine malignancy are reviewed. Very recent data indicates that IGFBP-1 undergoes regulated expression in human osteoblasts. Limited information also suggests that IGFBP-1 may be present in peripheral neurons, and that serum IGFBP-1 may increase during exercise and in critical ilIness. In summary, two major roles for IGFBP-1 in normal physiology can be constructed from current data: (i) As an “endocrine” factor, IGFBP-1 regulates the bio-availability of serum IGF-I, thereby modulating IGF-mediated tissue metabolism. The dominant regulation of IGFBP-1 expression by meal-related changes in hepatic insulin concentrations provides a dynamic link to substrate availability. (ii) As an autocrine/paracrine factor, IGFBP-1 appears to play a crucial role in the female reproductive system and, in particular, the sequence of events leading from ovulation to implantation to successful fetal outcom

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“Possibly indirect induction by thyroid hormones and catecholamines have been reported (Lee et al. 1997).”
Background
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“IGFBP-1 is mainly produced by the liver (5) and largely regulated by inhibitory effects of insulin (12).”
Background
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BackgroundInfluential
Insulin-Like Growth Factors and Insulin-Like Growth Factor Binding Proteins in Adult Patients with Severe Liver Disease before and after Orthotopic Liver Transplantation
Weber, M. M., Auernhammer, C. J., Lee, P., Engelhardt, D., & Zachoval, R. (2002) · Hormone Research in Paediatrics · doi:10.1159/000057960 · Cited by 39
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“IGF BP1 gene expression is known to be regulated by glucocorticoids (19).”
BackgroundSelf-citation
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Background
Increased Pulsatility, Process Irregularity, and Nocturnal Trough Concentrations of Growth Hormone in Amenorrheic Compared to Eumenorrheic Athletes
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Background
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Background
Peptide self-aggregation and peptide complementarity as bases for the evolution of peptide receptors: a review
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“…and glucagon are members of larger families of insulin-like and glucagon-like peptides (reviewed in Navarro et al., 1999; Plisetskaya, 1998; Reinecke and Collet, 1998; Chang et al., 2002; Lee et al., 1997), for which the same complementary relationships should exist in their respective receptors.”
Background
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Background
High insulinlike growth factor binding protein 1 level predicts incident congestive heart failure in the elderly
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BackgroundInfluential
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Background
Insulin‐like growth factor binding protein 1 ameliorates lipid accumulation and inflammation in nonalcoholic fatty liver disease
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“IGFBP-1 increased from early to midgestation, but was lower in wk 24–34, when all samples were collected after glucose challenge, probably a reflection of the negative regulation of insulin on total IGFBP-1 (10, 22).”
BackgroundSelf-citation
Effects of Estradiol and Exogenous Insulin-Like Growth Factor I (IGF-I) on the IGF-I Axis during Growth Hormone Inhibition and Antagonism1
Wilson, M. E. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.11.5279 · Cited by 32
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The associations of anthropometric, behavioural and sociodemographic factors with circulating concentrations of IGF‐I, IGF‐II, IGFBP‐1, IGFBP‐2 and IGFBP‐3 in a pooled analysis of 16,024 men from 22 studies
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“or bioavailable fraction of IGF-I (14, 15).”
Insulin growth factor binding proteins as therapeutic targets in type 2 diabetes
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“The notion is supported by several studies; the hepatic gene transcription and synthesis of IGFBP-1 is rapidly inhibited by the meal-stimulated increase in insulin and, conversely, stimulated by both glucagon and cortisol [87-91].”
Result
Effects of hormone replacement therapy on insulin-like growth factor (IGF)-I, IGF-II and IGF binding protein (IGFBP)-1 to IGFBP-4: Implications for cardiovascular risk
Heald, A. H., Kaushal, K., Anderson, S. G., Redpath, M., Durrington, P. N., Selby, P. L., & Gibson, M. (2005) · Gynecological Endocrinology · doi:10.1080/09513590400027406 · Cited by 30
“In contrast, the acute metabolic actions of the IGFs are thought to be modulated principally by lower-molecular-weight binding proteins, in particular IGFBP-1 [17].”
Background
Glucose regulation of the IGF response system in chondrocytes: induction of an IGF-I-resistant state
Kelley, K. M., Johnson, T. R., Ilan, J., et al. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.276.4.r1164 · Cited by 30
“IGFBP-1, in particular, is increased substantially in diabetic serum (20) and has been shown to inhibit IGF-I-mediated proliferation and [35S]PG synthesis when added to chick embryonic cartilage explants cultures (2).”
Background
Polymorphisms in igf -Binding Protein 1 Are Associated With Impaired Renal Function in Type 2 Diabetes
Stephens, R. H., McElduff, P., Heald, A. H., New, J. P., Worthington, J., Ollier, W., & Gibson, M. (2005) · Diabetes · doi:10.2337/diabetes.54.12.3547 · Cited by 29
Homeostasis model assessment and related simplified evaluations of insulin sensitivity from fasting insulin and glucose.
Brun, J. ‐., de Mauverger, É. R., & Mercier, J. G. (2000) · Diabetes Care · doi:10.2337/diacare.23.7.1037 · Cited by 29
AUUUA Sequences Compromise Human Insulin-like Growth Factor Binding Protein-1 mRNA Stability
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IGFBP‐1 levels in adult women born small for gestational age suggest insulin resistance in spite of normal BMI
Kistner, A., Jacobson, S., Celsi, G., Vanpée, M., & Brismar, K. (2004) · Journal of Internal Medicine · doi:10.1046/j.0954-6820.2003.01257.x · Cited by 30
Dexamethasone effects on cortisol secretion in Alzheimer’s disease: Some clinical and hormonal features in suppressor and nonsuppressor patients
Murialdo, G., Barreca, A., Nobili, F. M., Rollero, A., Timossi, G., Gianelli, M. V., Copello, F., Rodriguez, G., & POLLERI, A. (2000) · Journal of Endocrinological Investigation · doi:10.1007/bf03343703 · Cited by 28
CONTROLLING THE SUGAR BOWL
Haymond, M. W., & Sunehag, A. L. (1999) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(05)70096-7 · Cited by 28
Insulin-Like Growth Factor-I Stimulates Histone H3 and H4 Acetylation in the Brainin Vivo
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“Because of its capacity to avidly bind IGFs, IGFBP-1, when present in molar excess, is capable of inhibiting IGF-I action (19,20).”
Background
Expression of insulin-like growth factor binding protein-1 (IGFBP-1) mRNA in the ovine uterus throughout the oestrous cycle and early pregnancy
Osgerby, J., Gadd, T., & Wathes, D. C. (1999) · Journal of Endocrinology · doi:10.1677/joe.0.1620279 · Cited by 28
“This may be attributed to the tripeptide sequence at the COOH terminal domain of IGFBP-1, permitting integrin receptor binding at the surface of target cells (Lee et al. 1993, 1997).”
Background
Chronic pulsatile infusion of growth hormone to growth-restricted fetal sheep increases circulating fetal insulin-like growth factor-I levels but not fetal growth
Bauer, M., Breier, B. H., Bloomfield, F. H., et al. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1770083 · Cited by 27
“We found an increase in plasma IGFBP-1 and IGFBP-2 in IUGR+GH fetuses and both IGFBPs have been implicated in the regulation of tissue distribution and the amount of biologically active IGF-I (Baxter 1993, Lee et al. 1997).”
Background
Hypoxia Increases IGFBP-1 Phosphorylation Mediated by mTOR Inhibition
Damerill, I., Biggar, K. K., Shehab, M. A., Li, S. S. ‐., Jansson, T., & Gupta, M. B. (2015) · Molecular Endocrinology · doi:10.1210/me.2015-1194 · Cited by 27
Human Transcriptional Coactivator with PDZ-Binding Motif (TAZ) Is Downregulated During Decidualization1
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“It is believed that its core function in decidual cells is the regulation of IGF-I and IGF-II availability on the maternal-fetal interface [45].”
Background
Elevated insulin, proinsulin and insulin-like growth factor-binding protein-1 in liver disease
Hwang, D., Huang, S.-P., Lan, W.-S., et al. (2003) · Growth Hormone & IGF Research · doi:10.1016/s1096-6374(03)00042-x · Cited by 26
Self-citation
Hypoglycemia and pulmonary edema: a forgotten association.
Ortega, E., Wägner, A. M., Caixàs, A., Barcons, M., & Corcoy, R. (2000) · Diabetes Care · doi:10.2337/diacare.23.7.1023 · Cited by 26
Regulation of insulin-like growth factor binding protein-1 expression during aging
Rutkute, K., & Nikolova‐Karakashian, M. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.06.079 · Cited by 25
“Insulin-like growth factor (IGF)-binding proteins (IGFBPs) are serum proteins that bind IGFI and regulate its turnover, transport and tissue availability [1].”
Background
Isolation stress for 30 days alters hepatic gene expression profiles, especially with reference to lipid metabolism in mice
Motoyama, K., Nakai, Y., Miyashita, T., Fukui, Y., Morita, M., Sanmiya, K., Sakakibara, H., Matsumoto, I., Abe, K., Yakabe, T., et al. (2008) · Physiological Genomics · doi:10.1152/physiolgenomics.90358.2008 · Cited by 25
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“When we consider that the IGFBP-1 promoter contains a glucocorticoid response element (17) and that the glucocorticoids are intimately involved in glucose counterregulation, this is an attractive possibility.”
BackgroundInfluential
Low IGF1 and high IGFBP1 predict diabetes onset in prediabetic patients
Meyer, N. M. T., Kabisch, S., Dambeck, U., Honsek, C., Kemper, M., Gerbracht, C., Arafat, A. M., Birkenfeld, A. L., Schwarz, P. E. H., Machann, J., et al. (2022) · European Journal of Endocrinology · doi:10.1530/eje-22-0034 · Cited by 24
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Use of the Ligand Immunofunctional Assay for Human Insulin-Like Growth Factor (IGF) Binding Protein-3 (IGFBP-3) to Analyze IGFBP-3 Proteolysis and IGF-I Bioavailability in Healthy Adults, GH-Deficient and Acromegalic Patients, and Diabetics
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“In particular, differences in peripheral and hepatic insulin resistance may be important, when looking at circulating IGFBP-1, which is directly regulated by hepatic insulin action (Lee et al., 1997).”
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Regulation of Insulin-Like Growth Factor-Binding Protein 1 by Hypoxia and 3′,5′-Cyclic Adenosine Monophosphate Is Additive in HepG2 Cells1
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Self-citation
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Network Analysis of Hepatic Genes Responded to High-Fat Diet in C57BL/6J Mice: Nutrigenomics Data Mining from Recent Research Findings
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Background

Authors: Lee, P. D. K., Giudice, L. C., Conover, C. A., & Powell, D. R.
Affiliations: Mayo Clinic (US)
ORCID: Lee, P. D. K.
Giudice, L. C.
Conover, C. A.
Powell, D. R.
Venue: Experimental Biology and Medicine
Publisher: Frontiers Media SA
Published: 1997-12-01
Volume: 216
Issue: 3
Pages: 319-357
ISSN: 0071-3384 (ISSN-L)
1535-3702
1535-3699
DOI: 10.3181/00379727-216-44182
OpenAlex: W2036466897
Cited by: 523
References: 0
Citations by year: 2026: 1 · 2025: 4 · 2024: 8 · 2023: 4 · 2022: 6 · 2021: 10 · 2020: 8 · 2019: 11 · 2018: 10 · 2017: 19 · 2016: 16 · 2015: 16 · 2014: 11 · 2013: 17 · 2012: 14
FWCI: 16.84
Type: journal article
Language: en
Open access: closed
Locations: Experimental Biology and Medicine (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fibroblast Growth Factor Research
Health Sciences › Medicine › Hepatology › Liver physiology and pathology
Keywords: IGFBP-1, insulin-like growth factor, IGF binding, cysteine-rich region, protease cleavage, integrin binding, phosphorylation sites, IGFBP-3, chromosome 7, glucose metabolism, glucocorticoids, cyclic AMP, tissue-specific gene expression
MeSH terms: Amino Acid Sequence, Animals, Bone and Bones, Cartilage, Connective Tissue, Female, Gene Expression Regulation, Genitalia, Female, Genitalia, Male, Humans, Kidney, Liver, Male, Molecular Sequence Data, Organ Specificity, Substrate Specificity, Insulin-Like Growth Factor Binding Protein 1, Evolution, Molecular

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Insulin-like Growth Factor Binding Protein-1: Recent Findings and New Directions

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