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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BackgroundSelf-citation
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Background
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Background
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Background
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Background
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BackgroundResult
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Background
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BackgroundInfluential
2,3,7,8-Tetrachlorodibenzo-p-dioxin Induces Insulin-Like Growth Factor Binding Protein-1 Gene Expression and Counteracts the Negative Effect of Insulin
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BackgroundInfluential
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“IGFBP-1 is considered to be the principal acute regulator of IGF-I bioactivity and plays an important role in the development of diabetes and complications [11].”
Background
Effects of an endurance cycling competition on resting serum insulin-like growth factor I (IGF-I) and its binding proteins IGFBP-1 and IGFBP-3
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Background
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“The GCT stimulates insulin secretion, and the down-regulation of IGFBP-1 by insulin and IGF-I is well documented (7).”
Background
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“IGFBP-1 is an IGF-binding protein that typically reduces IGF-1 action (Lee et al., 1997).”
Background
The role of insulin-like growth factor-I and growth factor-associated signal transduction pathways in estradiol and progesterone facilitation of female reproductive behaviors
Etgen, A. M., González‐Flores, O., & Todd, B. J. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2006.06.001 · Cited by 51
Cross Talk Between Growth and Immunity: Coupling of the IGF Axis to Conserved Cytokine Pathways in Rainbow Trout
Alzaid, A., Castro, R., Wang, T., et al. (2016) · Endocrinology · doi:10.1210/en.2015-2024 · Cited by 50
Hormonal and Metabolic Defects in a Prader-Willi Syndrome Mouse Model with Neonatal Failure to Thrive
Stefan, M., Ji, H. L., Simmons, R. A., Cummings, D. E., Ahima, R. S., Friedman, M. I., & Nicholls, R. D. (2005) · Endocrinology · doi:10.1210/en.2005-0371 · Cited by 49
Maternal plasma concentrations of IGF-1, IGFBP-1, and C-peptide in early pregnancy and subsequent risk of gestational diabetes mellitus
Qiu, C., Vadachkoria, S., Meryman, L., Frederick, I. O., & Williams, M. A. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2005.04.015 · Cited by 50
Insulin-like growth factor binding protein-1 induces decidualization of human endometrial stromal cells via 5 1 integrin
Matsumoto, H., Sakai, K., & Iwashita, M. (2008) · Molecular Human Reproduction · doi:10.1093/molehr/gan038 · Cited by 50
“Although physiological significance of IGFBP-1 produced in decidua is not fully understood, it has been presumed that decidual IGFBP-1 negatively controls the trophoblast invasion into uterine myometrium (Lee et al., 1997).”
BackgroundInfluential
Effect of Short-Term Prednisone Use on Blood Flow, Muscle Protein Metabolism, and Function
Short, K. R., Nygren, J., Bigelow, M. L., & Nair, K. S. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0908 · Cited by 50
Hoxa5 overexpression correlates with IGFBP1 upregulation and postnatal dwarfism: evidence for an interaction between Hoxa5 and Forkhead box transcription factors
Foucher, I., Volovitch, M., Frain, M., et al. (2002) · Development · doi:10.1242/dev.129.17.4065 · Cited by 50
Transcriptomic analysis of human placenta in intrauterine growth restriction
Madeleneau, D., Buffat, C., Mondon, F., Grimault, H., Rigourd, V., Tsatsaris, V., Letourneur, F., Vaiman, D., Barbaux, S., & Gascoin-Lachambre, G. (2015) · Pediatric Research · doi:10.1038/pr.2015.40 · Cited by 49
Patterns of gene expression in pig adipose tissue: Insulin-like growth factor system proteins, neuropeptide Y (NPY), NPY receptors, neurotrophic factors and other secreted factors
Hausman, G. J., Barb, C. R., & Dean, R. G. (2008) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2008.01.004 · Cited by 50
A comprehensive analysis of common IGF1, IGFBP1 and IGFBP3 genetic variation with prospective IGF-I and IGFBP-3 blood levels and prostate cancer risk among Caucasians †
Schumacher, F. R., Cheng, I. C., Freedman, M. L., Mucci, L. A., Allen, N. E., Pollak, M., Hayes, R. B., Stram, D. O., Canzian, F., Henderson, B. E., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq210 · Cited by 50
“Circulating levels of IGF-I derive mostly from the liver; more than 90% is complexed with IGF-binding protein 3 (IGFBP-3) and an acidlabile subunit thus reducing bioavailability (12,13).”
Absence of the Full-Length Breast Cancer–Associated Gene-1 Leads to Increased Expression of Insulin-Like Growth Factor Signaling Axis Members
Shukla, V., Coumoul, X., Cao, L., Wang, R.-H., Xiao, C., Xu, X., Andò, S., Yakar, S., LeRoith, D., & Deng, C. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-4570 · Cited by 49
ACUTE EFFECTS OF GROWTH HORMONE IN ALCOHOL-FED RATS
Lang, C. H. (2000) · Alcohol and Alcoholism · doi:10.1093/alcalc/35.2.148 · Cited by 49
Concentrations of IGF-I and IGFBP-3 and pancreatic cancer risk in the European Prospective Investigation into Cancer and Nutrition
Rohrmann, S., Grote, V. A., Becker, S., et al. (2012) · British Journal of Cancer · doi:10.1038/bjc.2012.19 · Cited by 48
Glycogen Synthase Kinase-3 regulates IGFBP-1 gene transcription through the Thymine-rich Insulin Response Element
Finlay, D. K., Patel, S., Dickson, L. M., Shpiro, N., Márquez, R., Rhodes, C. J., & Sutherland, C. D. (2004) · BMC Molecular Biology · doi:10.1186/1471-2199-5-15 · Cited by 47
The influence of dietary intake on the insulin-like growth factor (IGF) system across three ethnic groups: a population-based study
Heald, A. H., Cade, J. E., Cruickshank, J. K., Anderson, S. G., White, A. E., & Gibson, M. (2003) · Public Health Nutrition · doi:10.1079/phn2002414 · Cited by 48
Lack of association between adipose tissue distribution and IGF-1 and IGFBP-3 in men and women.
Schoen, R. E., Schragin, J. G., Weissfeld, J. L., Thaete, F. L., Evans, R. G., Rosen, C. J., & Kuller, L. H. (2002) · PubMed · Cited by 48
IGF-I Bioactivity in an Elderly Population
Brugts, M. P., van Duijn, C. M., Hofland, L. J., Witteman, J. C. M., Lamberts, S. W. J., & Janssen, J. A. M. J. L. (2010) · Diabetes · doi:10.2337/db09-0583 · Cited by 47
“Because individuals with the metabolic syndrome are chronically exposed to high circulating insulin levels, the increase in IGF-I bioactivity in subjects with one to three components of the metabolic syndrome may be due to an insulinmediated suppression of IGFBP-1 levels (24).”
Background
Effects of losartan or enalapril on hemoglobin, circulating erythropoietin, and insulin-like growth factor-1 in patients with and without posttransplant erythrocytosis
Wang, A. Y., Yu, A. W. Y., Lam, C. W. K., et al. (2002) · American Journal of Kidney Diseases · doi:10.1053/ajkd.2002.31404 · Cited by 47
Metabolic, Anthropometric, and Nutritional Factors as Predictors of Circulating Insulin-Like Growth Factor Binding Protein-1 Levels in Middle-Aged and Elderly Men
Wolk, K., Larsson, S. C., Vessby, B. O., et al. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031349 · Cited by 47
“Numerous investigations have confirmed that insulin, through inhibition of IGFBP-1 transcription, is the primary determinant of IGFBP-1 expression both in vitro and in vivo (28).”
Background
Glomerulosclerosis in mice transgenic for human insulin-like growth factor-binding protein-1
Doublier, S., Seurin, D., Fouqueray, B. L., et al. (2000) · Kidney International · doi:10.1046/j.1523-1755.2000.00090.x · Cited by 47
Nutritional status and growth hormone regulate insulin-like growth factor binding protein (igfbp) transcripts in Mozambique tilapia
Breves, J. P., Tipsmark, C. K., Stough, B. A., Seale, A. P., Flack, B. R., Moorman, B. P., Lerner, D. T., & Grau, E. G. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.04.034 · Cited by 46
“A strong association between elevated plasma Igfbp1 and fasting conditions appears to be conserved from teleosts to mammals (Lee et al., 1997; Siharath et al., 1996).”
Insulin-like growth factor binding protein-1 in PCOS: a systematic review and meta-analysis
Kelly, C. J., Stenton, S. R., & Lashen, H. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmq027 · Cited by 46
“The reference sections of five recent review articles on IGFBP-1 were hand-searched (Poretsky, 1991; Poretsky et al., 1999; Lee et al., 1997; Fowler et al., 2000; Wang and Wang, 2003).”
BackgroundMethod
Salmon serum 22 kDa insulin-like growth factor-binding protein (IGFBP) is IGFBP-1
Shimizu, M., Dickey, J. T., Fukada, H., & Dickhoff, W. W. (2005) · Journal of Endocrinology · doi:10.1677/joe.1.05880 · Cited by 46
“IGFBP-1 is one of the best-9 characterized IGFBPs (for reviews, Lee et al., 1993, 1997).”
Background
Endoplasmic Reticulum Stress Induction of Insulin-like Growth Factor-binding Protein-1 Involves ATF4
Marchand, A., Tomkiewicz, C., Magne, L., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602157200 · Cited by 46
Haplotype-Based Association Studies of IGFBP1 and IGFBP3 with Prostate and Breast Cancer Risk: The Multiethnic Cohort
Cheng, I. C., Penney, K. L., Stram, D. O., et al. (2006) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-06-0361 · Cited by 46
“IGFBP1 is inversely regulated by insulin and acutely mediates IGF-I bioavailability (6).”
Background
IGFBP-1 in cancer: expression, molecular mechanisms, and potential clinical implications.
Lin, Y.-W., Weng, X., Huang, B.-L., Guo, H., Xu, Y., & Peng, Y. (2021) · PubMed Central · Cited by 45
Insulin-like growth factor binding protein-1 inhibits cancer cell invasion and is associated with poor prognosis in hepatocellular carcinoma.
Dai, B., Ruan, B., Wu, J., Wang, J., Shang, R., Sun, W., Li, X., Dou, K., Wang, D., & Li, Y. (2014) · PubMed Central · Cited by 45
Structure and Properties of the C-terminal Domain of Insulin-like Growth Factor-binding Protein-1 Isolated from Human Amniotic Fluid
Sala, A., Capaldi, S., Campagnoli, M., Faggion, B., Labò, S., Perduca, M., Romano, A., Carrizo, M. E., Valli, M., Visai, L., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m504304200 · Cited by 45
Purification of a 41-kDa insulin-like growth factor binding protein from serum of chinook salmon, Oncorhynchus tshawytscha
Shimizu, M., Swanson, P., Hara, A., et al. (2003) · General and Comparative Endocrinology · doi:10.1016/s0016-6480(03)00052-2 · Cited by 45
Decreased IGF-I bioavailability after ethanol abuse in alcoholics: partial restitution after short-term abstinence
Röjdmark, S., & Brismar, K. (2001) · Journal of Endocrinological Investigation · doi:10.1007/bf03343879 · Cited by 44
Genetic Variants, Prediagnostic Circulating Levels of Insulin-like Growth Factors, Insulin, and Glucose and the Risk of Colorectal Cancer: The Multiethnic Cohort Study
Ollberding, N. J., Cheng, I. C., Wilkens, L. R., Henderson, B. E., Pollak, M., Kolonel, L. N., & Marchand, L. L. (2012) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-1105 · Cited by 45
“cell proliferation and aberrant crypt foci in the colon (9, 10) and to inhibit the transcriptionof IGFBP-1 (11).”
Influential
Multiple Hormonal Dysregulation as Determinant of Low Physical Performance and Mobility in Older Persons
Maggio, M. G., Lauretani, F., Vita, F., Basaria, S. S., Lippi, G., Buttò, V., Luci, M., Cattabiani, C., Ceresini, G., Verzicco, I., et al. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113196660062 · Cited by 46
“IGFBPs have also independent biological actions [102].”
Reproductive Abnormalities in Human Insulin-Like Growth Factor-Binding Protein-1 Transgenic Male Mice
Froment, P., Staub, C., Hembert, S., Pisselet, C., Magistrini, M., Delaleu, B., Seurin, D., Levine, J. E., Johnson, L. W., Binoux, M., et al. (2004) · Endocrinology · doi:10.1210/en.2003-0956 · Cited by 44
“cocorticoids and is inhibited by insulin and GH (15, 16).”
Background
The Role of Insulin-like Growth Factors and Binding Proteins in Bone Cell Biology
Conover, C. A., & Rosen, C. J. (2002) · Elsevier eBooks · doi:10.1016/b978-012098652-1.50147-5 · Cited by 50
Self-citation
Human Insulin-Like Growth Factor (IGF) Binding Protein-1 Inhibits IGF-I-Stimulated Body Growth but Stimulates Growth of the Kidney in Snell Dwarf Mice
van Buul-Offers, S. C., Kleffens, M. D.-V., Koster, J. G., Lindenbergh-Kortleve, D. J., Gresnigt, M. G., Drop, S. L. S., Hoogerbrugge, C. M., Bloemen, R. J., KOEDAM, J. A., & van Neck, J. W. (2000) · Endocrinology · doi:10.1210/endo.141.4.7418 · Cited by 43
Hypoxia and Leucine Deprivation Induce Human Insulin-Like Growth Factor Binding Protein-1 Hyperphosphorylation and Increase Its Biological Activity
Seferovic, M. D., Ali, R., Kamei, H., Liu, S., Khosravi, J. M., Nazarian, S. H., Han, V. K. M., Duan, C., & Gupta, M. B. (2008) · Endocrinology · doi:10.1210/en.2008-0657 · Cited by 43
Polycystic Ovary Syndrome
Sood, M., Zweig, S. B., Tolentino, M. C., Strizhevsky, M., & Poretsky, L. (2017) · Springer eBooks · doi:10.1007/978-3-319-18741-9_33 · Cited by 43
Diagnostic Value of the Acid-Labile Subunit in Acromegaly: Evaluation in Comparison with Insulin-Like Growth Factor (IGF) I, and IGF-Binding Protein-1, -2, and -31
Arosio, M., Garrone, S., Bruzzi, P., et al. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.3.7288 · Cited by 43
“The observation that IGFBP-1 levels were lower in acromegaly than in normal subjects is in agreement with previous reports (33, 40, 41) and with the known inhibition of this parameter by insulin (38).”
BackgroundResult
Inhibition of FASN suppresses migration, invasion and growth in hepatoma carcinoma cells by deregulating the HIF-1α/IGFBP1 pathway
Gong, J., Shen, S., Yang, Y., et al. (2017) · International Journal of Oncology · doi:10.3892/ijo.2017.3867 · Cited by 42
“However, in contrast to other proteins of this family, the expression of IGFBP-1 is markedly altered by changes in metabolic state (24).”
IGFBP1 and Follistatin-like 3 Genes are Significantly Up-regulated in Expression Profiles of the IUGR Placenta
Okamoto, A., Endo, H., Kalionis, B., et al. (2005) · Placenta · doi:10.1016/j.placenta.2004.12.007 · Cited by 42
Impaired brain development and hydrocephalus in a line of transgenic mice with liver-specific expression of human insulin-like growth factor binding protein-1
Doublier, S., Duyckaerts, C. J., Seurin, D., & Binoux, M. (2000) · Growth Hormone & IGF Research · doi:10.1054/ghir.2000.0168 · Cited by 41

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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