Insulin-like growth factor 1 and 2 (IGF1, IGF2) expression in human microglia: differential regulation by inflammatory mediators
Open accessAbstract
BACKGROUND: Recent studies in experimental animals show that insulin-like growth factor 1 (IGF1) plays a trophic role during development and tissue injury and that microglia are important sources of IGF1. However, little information is available regarding the expression, regulation, and function of IGF1 and related proteins in human brain cells. In the current study, we examined the expression of IGF1 and IGF2 in human microglia in vivo and in vitro. METHODS: Expression of IGF1 and IGF2 was examined by immunohistochemistry in post-mortem human brain sections derived from HIV+ and HIV- brains. In primary cultures of human fetal microglia, IGF1 and IGF2 mRNA and protein expression was examined by Q-PCR, ELISA, and Western blot analysis. Additionally, the role of IGF1 and IGF2 in neuroprotection was examined in primary human neuronal glial cultures. RESULTS: Immunohistochemistry of human brain tissues showed that nonparenchymal cells (vessels and meninges), as well as parenchymal microglia and macrophages were positive for IGF1, in both HIV encephalitis and control brains, while IGF2 was undetectable. Cultured microglia expressed IGF1 mRNA and produced pg/ml levels of IGF1 protein; this was significantly suppressed by proinflammatory mediators, such as lipopolysaccharide (LPS), poly(I:C), and IFNγ. The Th2 cytokines IL-4 and IL-13 had no significant effect, but the cAMP analog (dibutyryl cAMP) significantly increased IGF1 production. In contrast, microglial IGF2 mRNA and protein (determined by Western blot) were upregulated by LPS. IGF1 receptor (IGF1R) immunoreactivity was predominantly expressed by neurons, and both IGF1 and IGF2 significantly protected neurons from cytokine (IL-1/IFNγ) induced death. CONCLUSIONS: Our study in human brain tissues and cells indicates that microglia are important sources of neurotrophic growth factors IGF1 and IGF2, and that microglial activation phenotypes can influence the growth factor expression. Importantly, our results suggest that chronic neuroinflammation and upregulation of proinflammatory cytokines could lead to neurodegeneration by suppressing the production of microglia-derived neuronal growth factors, such as IGF1.
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M2 microglia can release anti-inflammatory cytokines including IL-4, IL-13, IL-10, TGF-β and neurotrophic factors such as IGF-1 to assist inflammation resolution and promote neuron survival.
“These cells can release anti-inflammatory cytokines including IL-4, IL-13, IL-10, TGF-β and neurotrophic factors, such as insulin-like growth factor 1 (IGF-1) to assist inflammation resolution and promote neuron survival (Suh et al., 2013; Tang and Le, 2016).”
From The role of microglia in retinal neurodegeneration: Alzheimer’s disease, parkinson, and glaucoma. (2017) · cites this paper as Suh et al., 2013
Igf1 expression is inhibited by pro-inflammatory stimuli and enhanced in anti-inflammatory environments.
“Our findings, in line with previous studies (59,68–71), show that Igf1 expression is inhibited by pro-inflammatory stimuli and enhanced in anti-inflammatory environments.”
From <i>Trem2</i> promotes anti-inflammatory responses in microglia and is suppressed under pro-inflammatory conditions (2020) · cites this paper as [69]
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Alternative activation of macrophages
Gordon, S. (2003) · Nature Reviews Immunology · doi:10.1038/nri978 · Cited by 6,189 · see citing works
ATP mediates rapid microglial response to local brain injury in vivo
Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., Littman, D. R., Dustin, M. L., & Gan, W.-B. (2005) · Nature Neuroscience · doi:10.1038/nn1472 · Cited by 3,913 · see citing works
Microglia: Active sensor and versatile effector cells in the normal and pathologic brain
Hanisch, U.-K., & Kettenmann, H. (2007) · Nature Neuroscience · doi:10.1038/nn1997 · Cited by 3,676 · see citing works
Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool
Ajami, B., Bennett, J. L., Krieger, C., McNagny, K. M., & Rossi, F. M. V. (2011) · Nature Neuroscience · doi:10.1038/nn.2887 · Cited by 1,061 · see citing works
Selective Ablation of Proliferating Microglial Cells Exacerbates Ischemic Injury in the Brain
Lalancette-Hébert, M., Gowing, G., Simard, A., Weng, Y. C., & Kriz, J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5360-06.2007 · Cited by 874 · see citing works
The many faces of insulin-like peptide signalling in the brain
Fernandez, A. M., & Torres-Alemán, I. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3209 · Cited by 872 · see citing works
Cellular Localization of Somatomedin (Insulin-Like Growth Factor) Messenger RNA in the Human Fetus
Han, V. K. M., D’Ercole, A. J., & Lund, P. K. (1987) · Science · doi:10.1126/science.3563497 · Cited by 660 · see citing works
The Insulin-Like Growth Factor System and Its Pleiotropic Functions in Brain
Russo, V. C., Gluckman, P. D., Feldman, E. L., & Werther, G. A. (2005) · Endocrine Reviews · doi:10.1210/er.2004-0024 · Cited by 488 · see citing works
Differential expression of insulin-like growth factor genes in rat central nervous system.
Rotwein, P. S., Burgess, S. K., Milbrandt, J., & Krause, J. E. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.1.265 · Cited by 474 · see citing works
Carson, M. J., Behringer, R. R., Brinster, R. L., & McMorris, F. A. (1993) · Neuron · doi:10.1016/0896-6273(93)90173-o · Cited by 474 · see citing works
Serum insulin-like growth factor I regulates brain amyloid-β levels
Carro, E., Trejo, J. L., Gómez‐Isla, T., LeRoith, D., & Torres‐Alemán, I. (2002) · Nature Medicine · doi:10.1038/nm793 · Cited by 448 · see citing works
Serum insulin-like growth factor I regulates brain amyloid-β levels
Carro, E., Jl, T., Gómez‐Isla, T., LeRoith, D., & Torres‐Alemán, I. (2002) · Nature Medicine · doi:10.1038/nm1202-793 · Cited by 442 · see citing works
Molecular interactions of the IGF system
Denley, A., Cosgrove, L. J., Booker, G. W., Wallace, J. C., & Forbes, B. E. (2005) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2005.04.004 · Cited by 438 · see citing works
A critical role for IGF-II in memory consolidation and enhancement
Chen, D. Y., Stern, S. A., García‐Osta, A., Saunier-Rebori, B., Pollonini, G., Bambah-Mukku, D., Blitzer, R. D., & Alberini, C. M. (2011) · Nature · doi:10.1038/nature09667 · Cited by 421 · see citing works
Bondy, C. A., Werner, H., Roberts, C. T., & LeRoith, D. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90193-6 · Cited by 372 · see citing works
Ginderachter, J. A. V., Movahedi, K., Ghassabeh, G. H., Meerschaut, S., Beschin, A., Raes, G., & BAETSELIER, P. D. (2006) · Immunobiology · doi:10.1016/j.imbio.2006.06.002 · Cited by 370 · see citing works
Signaling by insulin-like growth factor 1 in brain
Bondy, C. A., & Cheng, C. M. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.02.042 · Cited by 323 · see citing works
Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells
Raes, G., Van den Bergh, R., De Baetselier, P., & Ghassabeh, G. H. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.11.6561 · Cited by 302 · see citing works
Serum TNF-alpha levels are increased and correlate negatively with free IGF-I in Alzheimer disease
Álvarez, A., Cacabelos, R., Sanpedro, C., García-Fantini, M., & Aleixandre, M. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.02.012 · Cited by 278 · see citing works
Human monocytes/macrophages: NO or no NO?
Denis, M. (1994) · Journal of Leukocyte Biology · doi:10.1002/jlb.55.5.682 · Cited by 274 · see citing works
Butovsky, O. (2006) · Journal of Clinical Investigation · doi:10.1172/jci26836 · Cited by 261 · see citing works
Neumann, J. H. L., Sauerzweig, S., Rönicke, R., Gunzer, F., Dinkel, K., Ullrich, O., Gunzer, M., & Reymann, K. G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0060-08.2008 · Cited by 255 · see citing works
Cosenza;, M. A., Zhao;, M., Si;, Q., & Lee, S. C. (2002) · Brain Pathology · doi:10.1111/j.1750-3639.2002.tb00461.x · Cited by 238 · see citing works
Self-citationMyelination Is Altered in Insulin-Like Growth Factor-I Null Mutant Mice
Ye, P., Li, L., Richards, R. G., DiAugustine, R. P., & D'Ercole, A. J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-14-06041.2002 · Cited by 225 · see citing works
Komoly, S., Hudson, L. D., Webster, H. D., & Bondy, C. A. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.5.1894 · Cited by 223 · see citing works
Noradrenergic regulation of inflammatory gene expression in brain
Feinstein, D. L., Heneka, M. T., Gavrilyuk, V., Russo, C. D., Weinberg, G. L., & Galea, E. (2002) · Neurochemistry International · doi:10.1016/s0197-0186(02)00049-9 · Cited by 221 · see citing works
Progranulin in frontotemporal lobar degeneration and neuroinflammation
Ahmed, Z., Mackenzie, I. R., Hutton, M. L., & Dickson, D. W. (2007) · Journal of Neuroinflammation · doi:10.1186/1742-2094-4-7 · Cited by 220 · see citing works
Siddappa, R., Martens, A. C., Doorn, J., Mentink-Leusink, A., Olivo, C., Licht, R., van Rijn, L., Gaspar, C., Fodde, R., Janssen, F., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711190105 · Cited by 219 · see citing works
An antagomir to microRNA Let7f promotes neuroprotection in an ischemic stroke model
Selvamani, A., Sathyan, P., Miranda, R. C., & Sohrabji, F. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032662 · Cited by 217 · see citing works
Haselbacher, G. K., Schwab, M. E., Pasi, A., & HUMBEL, R. E. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.7.2153 · Cited by 205 · see citing works
Batchelor, P. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2002.1185 · Cited by 199 · see citing works
Thissen, J., & Verniers, J. (1997) · Endocrinology · doi:10.1210/endo.138.3.4966 · Cited by 182 · see citing works
Krause, D., Suh, H.-S., Tarassishin, L., Cui, Q., Durafourt, B. A., Choi, N., Bauman, A., Cosenza-Nashat, M. A., Antel, J. P., Zhao, M., et al. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.05.048 · Cited by 176 · see citing works
Self-citationTarassishin, L., Suh, H.-S., & Lee, S. C. (2011) · Journal of Neuroinflammation · doi:10.1186/1742-2094-8-187 · Cited by 169 · see citing works
Self-citationHawkes, C. A., & Kar, S. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2003.11.002 · Cited by 159 · see citing works
Downen, M., Amaral, T. D., Hua, L. L., Zhao, M., & Lee, S. C. (1999) · Glia · doi:10.1002/(sici)1098-1136(199911)28:2 · Cited by 157 · see citing works
Self-citationSpecifying the cellular responses to IGF signals: roles of IGF-binding proteins
Duan, C. (2002) · Journal of Endocrinology · doi:10.1677/joe.0.1750041 · Cited by 151 · see citing works
Lee, S. C., Liu, W., Brosnan, C. F., & Dickson, D. W. (1992) · PubMed · Cited by 149 · see citing works
Self-citationA hippocampal insulin‐growth factor 2 pathway regulates the extinction of fear memories
Agís‐Balboa, R. C., Arcos-Díaz, D. P., Wittnam, J. L., Govindarajan, N., Blom, K., Burkhardt, S., Haladyniak, U., Agbemenyah, H. Y., Zovoilis, A., Salinas-Riester, G., et al. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.293 · Cited by 145 · see citing works
IGF‐I and microglia/macrophage proliferation in the ischemic mouse brain
O'Donnell, S. L., Frederick, T. J., Krady, J. K., Vannucci, S. J., & Wood, T. L. (2002) · Glia · doi:10.1002/glia.10081 · Cited by 139 · see citing works
TLR3 Ligation Activates an Antiviral Response in Human Fetal Astrocytes: A Role for Viperin/cig5
Rivieccio, M. A., Suh, H.-S., Zhao, Y., Zhao, M., Chin, K. C., Lee, S. C., & Brosnan, C. F. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.7.4735 · Cited by 135 · see citing works
Self-citationSuh, H.-S., Choi, N., Tarassishin, L., & Lee, S. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035115 · Cited by 135 · see citing works
Self-citationInsulin-like growth factors in the response to cerebral ischemia
Lee, W., Clemens, J. A., & Bondy, C. A. (1992) · Molecular and Cellular Neuroscience · doi:10.1016/1044-7431(92)90006-n · Cited by 115 · see citing works
Induction of macrophage insulin-like growth factor-I expression by the Th2 cytokines IL-4 and IL-13
Wynes, M. W., & Riches, D. W. H. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.7.3550 · Cited by 105 · see citing works
Huang, G. S., Brouwer‐Visser, J., Ramirez, M. J., et al. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-3233 · Cited by 98 · see citing works
Suh, H.-S., Zhao, M., Rivieccio, M. A., Choi, S., Connolly, E. C., Zhao, Y., Takikawa, O., Brosnan, C. F., & Lee, S. C. (2007) · Journal of Virology · doi:10.1128/jvi.00792-07 · Cited by 98 · see citing works
Self-citationSuh, H.-S., Kim, M.-O., & Lee, S. C. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.5.2712 · Cited by 88 · see citing works
Self-citationThomas, M. J., Umayahara, Y., Shu, H., Rotwein, P. S., & McCarthy, T. L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.36.21835 · Cited by 82 · see citing works
Arkins, S., Rebeiz, N., Brunke-Reese, D., Biragyn, A., & Kelley, K. W. (1995) · Molecular Endocrinology · doi:10.1210/mend.9.3.7776981 · Cited by 77 · see citing works
Mouse model for ablation of proliferating microgliain acute CNS injuries
Gowing, G., Vallières, L., & Julien, J. (2005) · Glia · doi:10.1002/glia.20288 · Cited by 71 · see citing works
Lee, S. C., Collins, M., Vanguri, P., & Shin, M. L. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.11.3391 · Cited by 71 · see citing works
Self-citationBilić, E., Bilić, E., Rudan, I., Kuŝec, V., Zurak, N., Delimar, D., & Žagar, M. (2006) · European Journal of Neurology · doi:10.1111/j.1468-1331.2006.01503.x · Cited by 71 · see citing works
Bellini, M. J., Hereñú, C. B., Goya, R. G., & García‐Segura, L. M. (2011) · Journal of Neuroinflammation · doi:10.1186/1742-2094-8-21 · Cited by 66 · see citing works
Fournier, T., Riches, D. W. H., Winston, B. W., Rose, D. M., Young, S. K., Noble, P. W., Lake, F., & Henson, P. M. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.155.4.2123 · Cited by 62 · see citing works
From hormones to immunity: the physiology of immunology
Kelley, K. W. (2003) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2003.10.003 · Cited by 58 · see citing works
Kang, Y., Digicaylioglu, M. H., Russo, R., Kaul, M., Achim, C. L., Fletcher, L., Masliah, E., & Lipton, S. A. (2010) · Annals of Neurology · doi:10.1002/ana.22070 · Cited by 57 · see citing works
Kaur, C., Sivakumar, V., Dheen, S. T., & Ling, E. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.12.025 · Cited by 48 · see citing works
Microglia and monocytes: 'tis plain the twain meet in the brain
Ransohoff, R. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2917 · Cited by 44 · see citing works
CD45 Isoform Expression in Microglia and Inflammatory Cells in HIV‐1 Encephalitis
Cosenza‐Nashat, M. A., Kim, M., Zhao, M., Suh, H., & Lee, S. C. (2006) · Brain Pathology · doi:10.1111/j.1750-3639.2006.00027.x · Cited by 43 · see citing works
Self-citationMultiple levels of control of insulin-like growth factor gene expression
Zarrilli, R., Bruni, C. B., & Riccio, A. (1994) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(94)90253-4 · Cited by 39 · see citing works
Neuroprotective Effects of IGF-I against TNFα-Induced Neuronal Damage in HIV-Associated Dementia
Wang, J. Y., Peruzzi, F., Lassak, A., Valle, L. D., Radhakrishnan, S., Rappaport, J., Khalili, K., Amini, S., & Krzysztof Reiss, F. (2002) · Virology · doi:10.1006/viro.2002.1690 · Cited by 38 · see citing works
Insulin-Like Growth Factor (IGF)-I Gene Deletion
Camacho‐Hübner, C., Woods, K. A., Clark, A., & Savage, M. O. (2002) · Reviews in Endocrine and Metabolic Disorders · doi:10.1023/a:1020957809082 · Cited by 36 · see citing works
Hatey, F., Langlois, I., Mulsant, P., et al. (1992) · Molecular and Cellular Endocrinology · doi:10.1016/0303-7207(92)90145-v · Cited by 36 · see citing works
Suh, H.-S., Cosenza-Nashat, M. A., Choi, N., et al. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.100399 · Cited by 31 · see citing works
Self-citationMonitoring insulin-like growth factors in HIV infection and AIDS
Congote, L. F. (2005) · Clinica Chimica Acta · doi:10.1016/j.cccn.2005.05.001 · Cited by 24 · see citing works
Zhou, Y., Zhang, Y., Li, J., Lv, F.-Y., Zhao, Y., Duan, D., & Xu, Q. (2012) · Journal of Neurochemistry · doi:10.1111/jnc.12010 · Cited by 20 · see citing works
Kihira, T., Suzuki, A., Kubo, T., Miwa, H., & Kondo, T. (2007) · Neuropathology · doi:10.1111/j.1440-1789.2007.00776.x · Cited by 16 · see citing works
Strickler, H. D., Fazzari, M. J., Kovács, A., et al. (2008) · The Journal of Infectious Diseases · doi:10.1086/524848 · Cited by 10 · see citing works
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- Authors
- Suh, H.-S., Zhao, M.-L., Derico, L., Choi, N., & Lee, S. C.
- Affiliations
- Albert Einstein College of Medicine (US)
- Corresponding author
- Suh, Hyeon-Sook
- Lee, Sunhee C
- Venue
- Journal of Neuroinflammation
- Published
- 2013-03-12
- Volume
- 10
- Issue
- 1
- Pages
- 37-37
- ISSN
- 1742-2094 (ISSN-L)
- PMC
- PMC3607995
- OpenAlex
- W2138293945
- Cited by
- 226
- References
- 68
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 23 · 2023: 20 · 2022: 26 · 2021: 30 · 2020: 17 · 2019: 15 · 2018: 12 · 2017: 20 · 2016: 15 · 2015: 15 · 2014: 14 · 2013: 7
- FWCI
- 9.54
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal of Neuroinflammation (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH055477, KO1MH084705, R01 MH 55477, K01MH084705)
- National Institute of Allergy and Infectious Diseases (P30AI051519)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- insulin-like growth factor I, insulin-like growth factor II, microglia, neuroinflammation, HIV-associated encephalitis, neuroprotection, IGF-1 receptor, inflammatory cytokines, lipopolysaccharide, interferon-gamma, cAMP signaling, neurodegeneration, human brain, neuronal growth factors, microglial activation, macrophages
- MeSH terms
- Cells, Cultured, Gene Expression Regulation, Humans, Insulin-Like Growth Factor I, Insulin-Like Growth Factor II, Neuroglia, Neurons, Phenotype, Microglia, Inflammation Mediators, Coculture Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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