Publications

Agis-Balboa, R. C., Arcos-Diaz, D., Wittnam, J., Govindarajan, N., Blom, K., Burkhardt, S., Haladyniak, U., Agbemenyah, H. Y., Zovoilis, A., Salinas-Riester, G., Opitz, L., Sananbenesi, F., & Fischer, A. (2011). A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. The EMBO journal, 30(19), 4071–4083. https://doi.org/10.1038/emboj.2011.293

Chen, D. Y., Stern, S. A., Garcia-Osta, A., Saunier-Rebori, B., Pollonini, G., Bambah-Mukku, D., Blitzer, R. D., & Alberini, C. M. (2011). A critical role for IGF-II in memory consolidation and enhancement. Nature, 469(7331), 491–497. https://doi.org/10.1038/nature09667

Alfimova, M. V., Lezheĭko, T. V., Gritsenko, I. K., & Golimbet, V. E. (2012). Genetika, 48(8), 993–998. PMID: 23035551

Stern, S. A., Chen, D. Y., & Alberini, C. M. (2014). The effect of insulin and insulin-like growth factors on hippocampus- and amygdala-dependent long-term memory formation. Learning & memory (Cold Spring Harbor, N.Y.), 21(10), 556–563. https://doi.org/10.1101/lm.029348.112

Stern, S. A., Kohtz, A. S., Pollonini, G., & Alberini, C. M. (2014). Enhancement of memories by systemic administration of insulin-like growth factor II. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology, 39(9), 2179–2190. https://doi.org/10.1038/npp.2014.69   

Duan, Q., Huang, F. L., Li, S. J., Chen, K. Z., Gong, L., Qi, J., Yang, Z. H., Yang, T. L., Li, F., & Li, C. Q. (2020). BET proteins inhibitor JQ-1 impaired the extinction of remote auditory fear memory: An effect mediated by insulin like growth factor 2. Neuropharmacology, 177, 108255. https://doi.org/10.1016/j.neuropharm.2020.108255

Yu, X. W., Pandey, K., Katzman, A. C., & Alberini, C. M. (2020). A role for CIM6P/IGF2 receptor in memory consolidation and enhancement. eLife, 9, e54781. https://doi.org/10.7554/eLife.54781

Concina, G., Renna, A., Milano, L., Manassero, E., Stabile, F., & Sacchetti, B. (2021). Expression of IGF-2 Receptor in the Auditory Cortex Improves the Precision of Recent Fear Memories and Maintains Detailed Remote Fear Memories Over Time. Cerebral cortex (New York, N.Y. : 1991), 31(12), 5381–5395. https://doi.org/10.1093/cercor/bhab165

Luo, Y., Liu, Z., Luo, S., Wang, X., & Tao, L. (2020). The developmental and experience-dependent expression of IGF-2 in mice visual cortex. Neuroscience letters, 721, 134828. https://doi.org/10.1016/j.neulet.2020.134828 

Steinmetz, A. B., Johnson, S. A., Iannitelli, D. E., Pollonini, G., & Alberini, C. M. (2016). Insulin-like growth factor 2 rescues aging-related memory loss in rats. Neurobiology of aging, 44, 9–21. https://doi.org/10.1016/j.neurobiolaging.2016.04.006

Lim, P. H., Wert, S. L., Tunc-Ozcan, E., Marr, R., Ferreira, A., & Redei, E. E. (2018). Premature hippocampus-dependent memory decline in middle-aged females of a genetic rat model of depression. Behavioural brain research, 353, 242–249. https://doi.org/10.1016/j.bbr.2018.02.030 

Pardo, M., Cheng, Y., Velmeshev, D., Magistri, M., Eldar-Finkelman, H., Martinez, A., Faghihi, M. A., Jope, R. S., & Beurel, E. (2017). Intranasal siRNA administration reveals IGF2 deficiency contributes to impaired cognition in Fragile X syndrome mice. JCI insight, 2(6), e91782. https://doi.org/10.1172/jci.insight.91782

Steinmetz, A. B., Stern, S. A., Kohtz, A. S., Descalzi, G., & Alberini, C. M. (2018). Insulin-Like Growth Factor II Targets the mTOR Pathway to Reverse Autism-Like Phenotypes in Mice. The Journal of neuroscience : the official journal of the Society for Neuroscience, 38(4), 1015–1029. https://doi.org/10.1523/JNEUROSCI.2010-17.2017

Cruz, E., Descalzi, G., Steinmetz, A., Scharfman, H. E., Katzman, A., & Alberini, C. M. (2021). CIM6P/IGF-2 Receptor Ligands Reverse Deficits in Angelman Syndrome Model Mice. Autism research : official journal of the International Society for Autism Research, 14(1), 29–45. https://doi.org/10.1002/aur.2418

Aria, F., Pandey, K., & Alberini, C. M. (2023). Excessive Protein Accumulation and Impaired Autophagy in the Hippocampus of Angelman Syndrome Modeled in Mice. Biological psychiatry, 94(1), 68–83. https://doi.org/10.1016/j.biopsych.2022.11.016

Cummings K. A. (2023). Protein Accumulation and Impaired Autophagy Underlie Cognitive Dysfunction in Angelman Syndrome. Biological psychiatry, 94(1), e1–e3. https://doi.org/10.1016/j.biopsych.2023.04.015

Pizzarelli, R., Pimpinella, D., Jacobs, C., Tartacca, A., Kullolli, U., Monyer, H., Alberini, C.M., Griguoli, M. (2023). Insulin-like growth factor 2 (IGF-2) rescues social deficits in NLG3 -/y mouse model of ASDs. (2023). Frontiers in Cellular Neuroscience.  7. https://www.frontiersin.org/articles/10.3389/fncel.2023.1332179/abstract    

García-Huerta, P., Troncoso-Escudero, P., Wu, D., Thiruvalluvan, A., Cisternas-Olmedo, M., Henríquez, D. R., Plate, L., Chana-Cuevas, P., Saquel, C., Thielen, P., Longo, K. A., Geddes, B. J., Lederkremer, G. Z., Sharma, N., Shenkman, M., Naphade, S., Sardi, S. P., Spichiger, C., Richter, H. G., Court, F. A., … Hetz, C. (2020). Insulin-like growth factor 2 (IGF2) protects against Huntington's disease through the extracellular disposal of protein aggregates. Acta neuropathologica, 140(5), 737–764. https://doi.org/10.1007/s00401-020-02183-1

Troncoso-Escudero, P., Vidal, RL. (2021). Insulin-like Growth Factor 2: Beyond its Role in Hippocampal-dependent Memory.  J Cell Immunol, 3(1), 46-52. https://www.scientificarchives.com/journal/journal-of-cellular-immunology 

Tham, A., Nordberg, A., Grissom, F. E., Carlsson-Skwirut, C., Viitanen, M., & Sara, V. R. (1993). Insulin-like growth factors and insulin-like growth factor binding proteins in cerebrospinal fluid and serum of patients with dementia of the Alzheimer type. Journal of neural transmission. Parkinson's disease and dementia section, 5(3), 165–176. https://doi.org/10.1007/BF02257671 

Rivera, E. J., Goldin, A., Fulmer, N., Tavares, R., Wands, J. R., & de la Monte, S. M. (2005). Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine. Journal of Alzheimer's disease : JAD, 8(3), 247–268. https://doi.org/10.3233/jad-2005-8304

Kar, S., Poirier, J., Guevara, J., Dea, D., Hawkes, C., Robitaille, Y., & Quirion, R. (2006). Cellular distribution of insulin-like growth factor-II/mannose-6-phosphate receptor in normal human brain and its alteration in Alzheimer's disease pathology. Neurobiology of aging, 27(2), 199–210. https://doi.org/10.1016/j.neurobiolaging.2005.03.005

Amritraj, A., Hawkes, C., Phinney, A. L., Mount, H. T., Scott, C. D., Westaway, D., & Kar, S. (2009). Altered levels and distribution of IGF-II/M6P receptor and lysosomal enzymes in mutant APP and APP + PS1 transgenic mouse brains. Neurobiology of aging, 30(1), 54–70. https://doi.org/10.1016/j.neurobiolaging.2007.05.004

Hertze, J., Nägga, K., Minthon, L., & Hansson, O. (2014). Changes in cerebrospinal fluid and blood plasma levels of IGF-II and its binding proteins in Alzheimer's disease: an observational study. BMC neurology, 14, 64. https://doi.org/10.1186/1471-2377-14-64 

Mellott, T. J., Pender, S. M., Burke, R. M., Langley, E. A., & Blusztajn, J. K. (2014). IGF2 ameliorates amyloidosis, increases cholinergic marker expression and raises BMP9 and neurotrophin levels in the hippocampus of the APPswePS1dE9 Alzheimer's disease model mice. PloS one, 9(4), e94287. https://doi.org/10.1371/journal.pone.0094287

Pascual-Lucas, M., Viana da Silva, S., Di Scala, M., Garcia-Barroso, C., González-Aseguinolaza, G., Mulle, C., Alberini, C. M., Cuadrado-Tejedor, M., & Garcia-Osta, A. (2014). Insulin-like growth factor 2 reverses memory and synaptic deficits in APP transgenic mice. EMBO molecular medicine, 6(10), 1246–1262. https://doi.org/10.15252/emmm.201404228

Åberg, D., Johansson, P., Isgaard, J., Wallin, A., Johansson, J. O., Andreasson, U., Blennow, K., Zetterberg, H., Åberg, N. D., & Svensson, J. (2015). Increased Cerebrospinal Fluid Level of Insulin-like Growth Factor-II in Male Patients with Alzheimer's Disease. Journal of Alzheimer's disease : JAD, 48(3), 637–646. https://doi.org/10.3233/JAD-150351

Liou, C. J., Tong, M., Vonsattel, J. P., & de la Monte, S. M. (2019). Altered Brain Expression of Insulin and Insulin-Like Growth Factors in Frontotemporal Lobar Degeneration: Another Degenerative Disease Linked to Dysregulation of Insulin Metabolic Pathways. ASN neuro, 11, 1759091419839515. https://doi.org/10.1177/1759091419839515  

Xia, L., Zhu, X., Zhao, Y., Yang, G., Zuo, X., Xie, P., Chen, C., & Han, Q. (2019). Genome-wide RNA sequencing analysis reveals that IGF-2 attenuates memory decline, oxidative stress and amyloid plaques in an Alzheimer's disease mouse model (AD) by activating the PI3K/AKT/CREB signaling pathway. International psychogeriatrics, 31(7), 947–959. https://doi.org/10.1017/S1041610219000383

Fertan, E., Gendron, W. H., Wong, A. A., Hanson, G. M., Brown, R. E., & Weaver, I. C. G. (2023). Noncanonical regulation of imprinted gene Igf2 by amyloid-beta 1-42 in Alzheimer's disease. Scientific reports, 13(1), 2043. https://doi.org/10.1038/s41598-023-29248-x

Fitzgerald, G. S., Chuchta, T. G., & McNay, E. C. (2023). Insulin-like growth factor-2 is a promising candidate for the treatment and prevention of Alzheimer's disease. CNS neuroscience & therapeutics, 29(6), 1449–1469. https://doi.org/10.1111/cns.14160

Claros, S., Cabrera, P., Valverde, N., Romero-Zerbo, S. Y., López-González, M. V., Shumilov, K., Rivera, A., Pavia, J., Martín-Montañez, E., & Garcia-Fernandez, M. (2021). Insulin-like Growth Factor II Prevents MPP+ and Glucocorticoid Mitochondrial-Oxidative and Neuronal Damage in Dopaminergic Neurons. Antioxidants (Basel, Switzerland), 11(1), 41. https://doi.org/10.3390/antiox11010041

Sepúlveda, D., Grunenwald, F., Vidal, A., Troncoso-Escudero, P., Cisternas-Olmedo, M., Villagra, R., Vergara, P., Aguilera, C., Nassif, M., & Vidal, R. L. (2022). Insulin-like growth factor 2 and autophagy gene expression alteration arise as potential biomarkers in Parkinson's disease. Scientific reports, 12(1), 2038. https://doi.org/10.1038/s41598-022-05941-1  

Zhang, H. Y., Jiang, Y. C., Li, J. R., Yan, J. N., Wang, X. J., Shen, J. B., Ke, K. F., & Gu, X. S. (2023). Neuroprotective effects of insulin-like growth factor-2 in 6-hydroxydopamine-induced cellular and mouse models of Parkinson's disease. Neural regeneration research, 18(5), 1099–1106. https://doi.org/10.4103/1673-5374.355815

Martín-Montañez, E., Valverde, N., Ladrón de Guevara-Miranda, D., Lara, E., Romero-Zerbo, Y. S., Millon, C., Boraldi, F., Ávila-Gámiz, F., Pérez-Cano, A. M., Garrido-Gil, P., Labandeira-Garcia, J. L., Santin, L. J., Pavia, J., & Garcia-Fernandez, M. (2021). Insulin-like growth factor II prevents oxidative and neuronal damage in cellular and mice models of Parkinson's disease. Redox biology, 46, 102095. https://doi.org/10.1016/j.redox.2021.102095

Arcos, J., Grunenwald, F., Sepulveda, D., Jerez, C., Urbina, V., Huerta, T., Troncoso-Escudero, P., Tirado, D., Perez, A., Diaz-Espinoza, R., Nova, E., Kubitscheck, U., Rodriguez-Gatica, J. E., Hetz, C., Toledo, J., Ahumada, P., Rojas-Rivera, D., Martín-Montañez, E., Garcia-Fernandez, M., & Vidal, R. L. (2023). IGF2 prevents dopaminergic neuronal loss and decreases intracellular alpha-synuclein accumulation in Parkinson's disease models. Cell death discovery, 9(1), 438. https://doi.org/10.1038/s41420-023-01734-1 

Chao, X. L., Jiang, S. Z., Xiong, J. W., Zhan, J. Q., Wei, B., Chen, C. N., & Yang, Y. J. (2020). Changes of Serum Insulin-like Growth Factor-2 Response to Negative Symptom Improvements in Schizophrenia Patients Treated with Atypical Antipsychotics. Current medical science, 40(3), 563–569. https://doi.org/10.1007/s11596-020-2214-0

Yang, Y. J., Luo, T., Zhao, Y., Jiang, S. Z., Xiong, J. W., Zhan, J. Q., Yu, B., Yan, K., & Wei, B. (2020). Altered insulin-like growth factor-2 signaling is associated with psychopathology and cognitive deficits in patients with schizophrenia. PloS one, 15(3), e0226688. https://doi.org/10.1371/journal.pone.0226688 

Vafaee, F., Zarifkar, A., Emamghoreishi, M., Namavar, M. R., Shirzad, S., Ghazavi, H., & Mahdavizadeh, V. (2020). Insulin-Like Growth Factor 2 (IGF-2) Regulates Neuronal Density and IGF-2 Distribution Following Hippocampal Intracerebral Hemorrhage. Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association, 29(10), 105128. https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105128

Åberg, D., Åberg, N. D., Jood, K., Redfors, P., Blomstrand, C., Isgaard, J., Jern, C., & Svensson, J. (2021). Insulin-Like Growth Factor-II and Ischemic Stroke-A Prospective Observational Study. Life (Basel, Switzerland), 11(6), 499. https://doi.org/10.3390/life11060499 

Martín-Montañez, E., Millon, C., Boraldi, F., Garcia-Guirado, F., Pedraza, C., Lara, E., Santin, L. J., Pavia, J., & Garcia-Fernandez, M. (2017). IGF-II promotes neuroprotection and neuroplasticity recovery in a long-lasting model of oxidative damage induced by glucocorticoids. Redox biology, 13, 69–81. https://doi.org/10.1016/j.redox.2017.05.012 

Guan, S. Z., Fu, Y. J., Zhao, F., Liu, H. Y., Chen, X. H., Qi, F. Q., Liu, Z. H., & Ng, T. B. (2021). The mechanism of enriched environment repairing the learning and memory impairment in offspring of prenatal stress by regulating the expression of activity-regulated cytoskeletal-associated and insulin-like growth factor-2 in hippocampus. Environmental health and preventive medicine, 26(1), 8. https://doi.org/10.1186/s12199-020-00929-7

Vafaee, F., Zarifkar, A., Emamghoreishi, M., Namavar, M. R., Shirzad, S., Ghazavi, H., & Mahdavizadeh, V. (2020). Insulin-Like Growth Factor 2 (IGF-2) Regulates Neuronal Density and IGF-2 Distribution Following Hippocampal Intracerebral Hemorrhage. Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association, 29(10), 105128. https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105128   

Mackay, K. B., Loddick, S. A., Naeve, G. S., Vana, A. M., Verge, G. M., & Foster, A. C. (2003). Neuroprotective effects of insulin-like growth factor-binding protein ligand inhibitors in vitro and in vivo. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism, 23(10), 1160–1167. https://doi.org/10.1097/01.WCB.0000087091.01171.AE  

Guan, J., Williams, C. E., Skinner, S. J., Mallard, E. C., & Gluckman, P. D. (1996). The effects of insulin-like growth factor (IGF)-1, IGF-2, and des-IGF-1 on neuronal loss after hypoxic-ischemic brain injury in adult rats: evidence for a role for IGF binding proteins. Endocrinology, 137(3), 893–898. https://doi.org/10.1210/endo.137.3.8603600

Li, Y., Chen, Y., Gao, X., & Zhang, Z. (2017). The behavioral deficits and cognitive impairment are correlated with decreased IGF-II and ERK in depressed mice induced by chronic unpredictable stress. The International journal of neuroscience, 127(12), 1096–1103. https://doi.org/10.1080/00207454.2017.1337014 

Poggini, S., Golia, M. T., Alboni, S., Milior, G., Sciarria, L. P., Viglione, A., Matte Bon, G., Brunello, N., Puglisi-Allegra, S., Limatola, C., Maggi, L., & Branchi, I. (2019). Combined Fluoxetine and Metformin Treatment Potentiates Antidepressant Efficacy Increasing IGF2 Expression in the Dorsal Hippocampus. Neural plasticity, 2019, 4651031. https://doi.org/10.1155/2019/4651031  

Guo, D., Xu, Y., Liu, Z., Wang, Y., Xu, X., Li, C., Li, S., Zhang, J., Xiong, T., Cao, W., & Liang, J. (2023). IGF2 inhibits hippocampal over-activated microglia and alleviates depression-like behavior in LPS- treated male mice. Brain research bulletin, 194, 1–12. https://doi.org/10.1016/j.brainresbull.2023.01.001 

Allodi, I., Comley, L., Nichterwitz, S., Nizzardo, M., Simone, C., Benitez, J. A., Cao, M., Corti, S., & Hedlund, E. (2016). Differential neuronal vulnerability identifies IGF-2 as a protective factor in ALS. Scientific reports, 6, 25960. https://doi.org/10.1038/srep25960

Osborn, T. M., Beagan, J., & Isacson, O. (2018). Increased motor neuron resilience by small molecule compounds that regulate IGF-II expression. Neurobiology of disease, 110, 218–230. https://doi.org/10.1016/j.nbd.2017.11.002 

Near, S. L., Whalen, L. R., Miller, J. A., & Ishii, D. N. (1992). Insulin-like growth factor II stimulates motor nerve regeneration. Proceedings of the National Academy of Sciences of the United States of America, 89(24), 11716–11720. https://doi.org/10.1073/pnas.89.24.11716  

Glazner, G. W., Lupien, S., Miller, J. A., & Ishii, D. N. (1993). Insulin-like growth factor II increases the rate of sciatic nerve regeneration in rats. Neuroscience, 54(3), 791–797. https://doi.org/10.1016/0306-4522(93)90248-e 

Hedlund, E., Karlsson, M., Osborn, T., Ludwig, W., & Isacson, O. (2010). Global gene expression profiling of somatic motor neuron populations with different vulnerability identify molecules and pathways of degeneration and protection. Brain : a journal of neurology, 133(Pt 8), 2313–2330. https://doi.org/10.1093/brain/awq167 

Martin-Montañez, E., Pavia, J., Santin, L. J., Boraldi, F., Estivill-Torrus, G., Aguirre, J. A., & Garcia-Fernandez, M. (2014). Involvement of IGF-II receptors in the antioxidant and neuroprotective effects of IGF-II on adult cortical neuronal cultures. Biochimica et biophysica acta, 1842(7), 1041–1051. https://doi.org/10.1016/j.bbadis.2014.03.010 

Pardo, M., Cheng, Y., Sitbon, Y. H., Lowell, J. A., Grieco, S. F., Worthen, R. J., Desse, S., & Barreda-Diaz, A. (2019). Insulin growth factor 2 (IGF2) as an emergent target in psychiatric and neurological disorders. Review. Neuroscience research, 149, 1–13. https://doi.org/10.1016/j.neures.2018.10.012  

Wang, Y., MacDonald, R. G., Thinakaran, G., & Kar, S. (2017). Insulin-Like Growth Factor-II/Cation-Independent Mannose 6-Phosphate Receptor in Neurodegenerative Diseases. Molecular neurobiology, 54(4), 2636–2658. https://doi.org/10.1007/s12035-016-9849-7 

Beletskiy, A., Chesnokova, E., & Bal, N. (2021). Insulin-Like Growth Factor 2 As a Possible Neuroprotective Agent and Memory Enhancer-Its Comparative Expression, Processing and Signaling in Mammalian CNS. International journal of molecular sciences, 22(4), 1849. https://doi.org/10.3390/ijms22041849  

Alberini C. M. (2023). IGF2 in memory, neurodevelopmental disorders, and neurodegenerative diseases. Trends in neurosciences, 46(6), 488–502. https://doi.org/10.1016/j.tins.2023.03.007