Insulin-like growth factor 1 and related compounds in the treatment of childhood-onset neurodevelopmental disorders

Frontiers in Neuroscience

Volumn 10, Issue SEP, 2016, Pages

  Vahdatpour, Cyrus ^a   Dyer, Adam H ^a   Tropea, Daniela ^b  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Autism spectrum disorders; Fragile X Syndrome; IGF 1; Phelan Mcdermid Syndrome; Rett Syndrome

Indexed keywords

RECOMBINANT SOMATOMEDIN C; SOMATOMEDIN C; TROFINETIDE;

AUTISM; BLOOD BRAIN BARRIER; CLINICAL EFFECTIVENESS; DISEASE ASSOCIATION; DRUG EFFICACY; FRAGILE X SYNDROME; HUMAN; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NONHUMAN; ONSET AGE; PHELAN-MCDERMID SYNDROME; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETT SYNDROME; SHORT SURVEY; SIGNAL TRANSDUCTION; TREATMENT DURATION; TREATMENT PLANNING;

EID: 84992028003     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2016.00450     Document Type: Short Survey

References (75)

1. Aberg, N. D., Brywe, K. G., and Isgaard, J. (2006). Aspects of growth hormone and insulin-like growth factor-I related to neuroprotection, regeneration, and functional plasticity in the adult brain. ScientificWorldJournal 6, 53-80. doi: 10.1100/tsw.2006.22
2. Anlar, B., Oktem, F., Bakkaloglu, B., Haliloglu, M., Oguz, H., Unal, F., et al. (2007). Urinary epidermal and insulin-like growth factor excretion in autistic children. Neuropediatrics 38, 151-153. doi: 10.1055/s-2007-990282
3. Armstrong, D. D. (2005). Neuropathology of Rett syndrome. J. Child Neurol. 20, 747-753. doi: 10.1177/08830738050200082401
4. Bach, M. A., Shen-Orr, Z., Lowe, W. L. Jr., Roberts, C. T. Jr., and LeRoith, D. (1991). Insulin-like growth factor I mRNA levels are developmentally regulated in specific regions of the rat brain. Brain Res. Mol. Brain Res. 10, 43-48. doi: 10.1016/0169-328X(91)90054-2
5. Banerjee, A., Castro, J., and Sur, M. (2012). Rett syndrome: genes, synapses, circuits, and therapeutics. Front. Psychiatry 3:34. doi: 10.3389/fpsyt.2012.00034
6. Bartlett, W. P., Li, X. S., and Williams, M. (1992). Expression of IGF-1 mRNA in the murine subventricular zone during postnatal development. Brain Res. Mol. Brain Res. 12, 285-291. doi: 10.1016/0169-328X(92)90131-T
7. Beck, K. D., Powell-Braxton, L., Widmer, H. R., Valverde, J., and Hefti, F. (1995). Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 14, 717-730. doi: 10.1016/0896-6273(95)90216-3
8. Bhakar, A. L., Dölen, G., and Bear, M. F. (2012). The pathophysiology of fragile X (and what it teaches us about synapses). Annu. Rev. Neurosci. 35, 417-443. doi: 10.1146/annurev-neuro-060909-153138
9. Bondy, C. A., and Lee, W. H. (1993). Patterns of insulin-like growth factor and IGF receptor gene expression in the brain. Functional implications. Ann. N.Y. Acad. Sci. 692, 33-43.
10. Bozdagi, O., Sakurai, T., Papapetrou, D., Wang, X., Dickstein, D. L., Takahashi, N., et al. (2010). Haploinsufficiency of the autism-associated Shank3 gene leads to deficits in synaptic function, social interaction, and social communication. Mol. Autism 1:15. doi: 10.1186/2040-2392-1-15
11. Bozdagi, O., Tavassoli, T., and Buxbaum, J. D. (2013). Insulin-like growth factor-1 rescues synaptic and motor deficits in a mouse model of autism and developmental delay. Mol. Autism 4:9. doi: 10.1186/2040-2392-4-9
12. Cahrour, M., and Zoghbi, H. Y. (2007). The story of Rett syndrome: from clinic to neurobiology. Neuron 56, 422-437. doi: 10.1016/j.neuron.2007.10.001
13. Castro, J., Garcia, R. I., Kwok, S., Banerjee, A., Petravicz, J., Woodson, J., et al. (2014). Functional recovery with recombinant human IGF1 treatment in a mouse model of Rett Syndrome. Proc. Natl. Acad. Sci. U.S.A. 111, 9941-9946. doi: 10.1073/pnas.1311685111
14. Centers for Disease Control Prevention (2012). Prevalence and Characteristics of Autism Spectrum Disorder Among Children Aged 8 Years-Autism and Developmental Disabilities Monitoring Network, 11 Sites, United States, 2012. Available online at: http://www.cdc.gov/mmwr/volumes/65/ss/ss6503a1.htm (Accessed on: September 26, 2016).
15. Chahrour, M., Jung, S. Y., Shaw, C., Zhou, Z., Wong, S. T., Qin, J., et al. (2008). MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320, 1224-1229. doi: 10.1126/science.1153252
16. Chang, Q., Khare, G., Dani, V., Nelson, S., and Jaenisch, R. (2006). The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49, 341-348. doi: 10.1016/j.neuron.2005.12.027
17. Chapleau, C. A., Calfa, G. D., Lane, M. C., Albertson, A. J., Larimore, J. L., Kudo, S., et al. (2009). Dendritic spine pathologies in hippocampal pyramidal neurons from Rett syndrome brain and after expression of Rett-associated MECP2 mutations. Neurobiol. Dis. 35, 219-233. doi: 10.1016/j.nbd.2009.05.001
18. Chen, M. J., and Russo-Neustadt, A. A. (2007). Running exercise-and antidepressant-induced increases in growth and survival-associated signaling molecules are IGF-dependent. Growth Factors 25, 118-131. doi: 10.1080/08977190701602329
19. Clemmons, D. R. (1998). Role of insulin-like growth factor binding proteins in the control of IGF actions. Mol. Cell. Endocrinol. 140, 19-24.
20. Corvin, A. P., Molinos, I., Little, G., Donohoe, G., Gill, M., Morris, D. W., et al. (2012). Insulin-like growth factor 1 (IGF1) and its active peptide (1-3)IGF1 enhance the expression of synaptic markers in neuronal circuits through different cellular mechanisms. Neurosci. Lett. 520, 51-56. doi: 10.1016/j.neulet.2012.05.029
21. Costales, J. L., and Kolevzon, A. (2015). The therapeutic potential of insulin-like growth factor-1 in central nervous system disorders. Neurotherapeutics 12, 620-630. doi: 10.1007/s13311-015-0352-z
22. Curia, G., Gualtieri, F., Bartolomeo, R., Vezzalo, R., and Biagini, G. (2013). Resilience to audiogenic seizures is associated with p-ERK1/2 dephosphorylation in the subiculum of Fmr1 knockout mice. Front. Cell. Neurosci. 25:46. doi: 10.3389/fncel.2013.00046
23. Dani, V. S., Chang, Q., Maffei, A., Turrigiano, G. G., Jaenisch, R., Nelson, S. B., et al. (2005). Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. U.S.A. 102, 12560-12565. doi: 10.1073/pnas.0506071102
24. Deacon, R. M., Glass, L., Snape, M., Hurley, M. J., Altimiras, F. J., Biekofsky, R. R., et al. (2015). NNZ-2566, a novel analog of (1-3) IGF-1, as a potential therapeutic agent for fragile X syndrome. Neuromol. Med. 17, 71-82. doi: 10.1007/s12017-015-8341-2
25. Della Sala, G., Putignano, E., Chelini, G., Melani, R., Calcagno, E., Michele Ratto, G., et al. (2016). Dendritic spine instability in a mouse model of CDKL5 disorder is rescued by insulin-like growth factor 1. Mol. Psychiatry. 80, 302-311. doi: 10.1016/j.biopsych.2015.08.028
26. Deng, P. Y., Rotman, Z., Blundon, J. A., Cho, Y., Cui, J., Cavalli, V., et al. (2013). FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron 77, 696-711. doi: 10.1016/j.neuron.2012.12.018
27. De Rubeis, S., He, X., Goldberg, A. P., Poultney, C. S., Samocha, K., Cicek, A. E., et al. (2014). Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 515, 209-215. doi: 10.1038/nature13772
28. Ding, Q., Vaynman, S., Akhavan, M., Ying, Z., and Gomez-Pinilla, F. (2006). Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 140, 823-833. doi: 10.1016/j.neuroscience.2006.02.084
29. Durand, S., Patrizi, A., Quast, K. B., Hachingian, L., Pavlyuk, R., and Saxena, A. (2012). NMDA receptor regulation prevents regression of visual cortical function in the absence of Mecp2. Neuron 76, 1078-10790. doi: 10.1016/j.neuron.2012.12.004
30. Dyer, A. H., Vahdatpour, C., Sanfeliu, A., and Tropea, D. (2016). The role of Insulin-Like Growth Factor 1 (IGF-1) in brain development, maturation and neuroplasticity. Nueroscience 325, 89-99. doi: 10.1016/j.neuroscience.2016.03.056
31. Fernandez, A. M., and Torres-Alemán, I. (2012). The many faces of insulin-like peptide signalling in the brain. Nat. Rev. Neurosci. 13, 225-239. doi: 10.1038/nrn3209
32. Firth, S. M., and Baxter, R. C. (2002). Cellular actions of the insulin-like growth factor binding proteins. Endocr. Rev. 23, 824-854. doi: 10.1210/er.2001-0033
33. Freitag, C. M. (2007). The genetics of autistic disorders and its clinical relevance: a review of the literature. Mol. Psychiatry 12, 2-22. doi: 10.1038/sj.mp.4001896
34. Garber, K. B., Visootsak, J., and Warren, S. T. (2008). Fragile X syndrome. Eur. J. Hum. Genet. 16, 666-6672. doi: 10.1586/14737159.2016.1135739
35. Gross, C., Nakamoto, M., Yao, X., Chan, C. B., Yim, S. Y., Ye, K., et al. (2010). Excess phosphoinositide 3-kinase subunit synthesis and activity as a novel therapeutic target in fragile X syndrome. J. Neurosci. 30, 10624-10638. doi: 10.1523/JNEUROSCI.0402-10.2010
36. Guan, J., Waldvogel, H. J., Faull, R. L., Gluckman, P. D., and Williams, C. E. (1999). The effects of the N-terminal tripeptide of insulin-like growth factor-1, glycine-proline-glutamate in different regions following hypoxic-ischemic brain injury in adult rats. Neuroscience 89, 649-659. doi: 10.1016/S0306-4522(98)00338-8
37. Hagberg, B. (2002). Clinical manifestations and stages of Rett syndrome. Ment. Retard. Disabil. Res. Rev. 8, 61-65. doi: 10.1002/mrdd.10020
38. Hagerman, R. J. (1997). Fragile X syndrome. molecular and clinical insights and treatment issues. West J. Med. 166, 129-137.
39. Huat, T. J., Khan, A. A., Pati, S., Mustafa, Z., Abdullah, J. M., and Jaafar, H. (2014). IGF-1 enhances cell proliferation and survival during early differentiation of mesenchymal stem cells to neural progenitor-like cells. BMC Neurosci. 15:91. doi: 10.1186/1471-2202-15-91
40. Hussman, J. P., Chung, R. H., Griswold, A. J., Jaworski, J. M., Salyakina, D., Ma, D., et al. (2011). A noise-reduction GWAS analysis implicates altered regulation of neurite outgrowth and guidance in autism. Mol. Autism 2:1. doi: 10.1186/2040-2392-2-1
41. Hwa, V., Oh, Y., and Rosenfeld, R. G. (1999). The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev. 20, 761-787. doi: 10.1210/er.20.6.761
42. Itoh, M., Ide, S., Takashima, S., Kudo, S., Nomura, Y., Segawa, M., et al. (2007). Methyl CpG-binding protein 2 (a mutation of which causes Rett syndrome) directly regulates insulin-like growth factor binding protein 3 in mouse and human brains. Neuropathol. Exp. Neurol. 66, 117-123. doi: 10.1097/nen.0b013e3180302078
43. Julu, P. O., Kerr, A. M., Apartopoulos, F., Al-Rawas, S., Engerstrom, I. W., Engerström, L., et al. (2001). Characterisation of breathing and associated central autonomic dysfunction in the Rett disorder. Arch. Dis. Child. 85, 29-37. doi: 10.1136/adc.85.1.29
44. Katz, D. M., Bird, A., Coenraads, M., Gray, S. J., Menon, D. U., Philpot, B. D., et al. (2016). Rett syndrome: crossing the threshold to clinical translation. Trends Neurosci. 39, 100-113. doi: 10.1016/j.tins.2015.12.008
45. Kaufmann, W. E., Johnston, M. V., and Blue, M. E. (2005). MeCP2 expression and function during brain development: implications for Rett syndrome's pathogenesis and clinical evolution. Brain Dev. 27(Suppl. 1), S77-S87. doi: 10.1016/j.braindev.2004.10.008
46. Khwaja, O. S., Ho, E., Barnes, K. V., O'Leary, H. M., Pereira, L. M., and Finkelstein, Y. (2014). Safety, pharmacokinetics, and preliminary assessment of efficacy of mecasermin (recombinant human IGF-1) for the treatment of Rett syndrome. Proc. Natl. Acad. Sci. U.S.A. 111, 4596-4601. doi: 10.1073/pnas.1311141111
47. Kolevzon, A., Bush, L., Wang, A. T., Halpern, D., Frank, Y., Grodberg, D., et al. (2014). A pilot controlled trial of insulin-like growth factor-1 in children with Phelan-McDermid syndrome. Mol. Autism 5:54. doi: 10.1186/2040-2392-5-54
48. Llorens-Martín, M., Torres-Alemán, I., and Trejo, J. L. (2009). Mechanisms mediating brain plasticity: IGF1 and adult hippocampal neurogenesis. Neuroscientist 15, 134-148. doi: 10.1177/1073858408331371
49. Marchetto, M. C., Belinson, H., Tian, Y., Freitas, B. C., Fu, C., Vadodaria, K. C., et al. (2016). Altered proliferation and networks in neural cells derived from idiopathic autistic individuals. Mol. Psychiatry. doi: 10.1038/mp.2016.95. [Epub ahead of print].
50. Mills, J. L., Hediger, M. L., Molloy, C. A., Chrousos, G. P., Manning-Courtney, P., Yu, K. F., et al. (2007). Elevated levels of growth-related hormones in autism and autism spectrum disorder. Clin. Endocrinol. 67, 230-237. doi: 10.1111/j.1365-2265.2007.02868.x
51. Netchine, I., Azzi, S., Le Bouc, Y., and Savage, M. O. (2011). IGF1 molecular anomalies demonstrate its critical role in fetal, postnatal growth and brain development. Best Pract. Res. Clin. Endocrinol. Metab. 25, 181-190. doi: 10.1016/j.beem.2010.08.005
52. Ocrant, I., Fay, C. T., and Parmelee, J. T. (1990). Characterization of insulin-like growth factor binding proteins produced in the rat central nervous system. Endocrinology 127, 1260-1267. doi: 10.1210/endo-127-3-1260
53. O'Kusky, J., and Ye, P. (2012). Neurodevelopmental effects of insulin-like growth factor signaling. Front. Neuroendocrinol. 33, 230-251. doi: 10.1016/j.yfrne.2012.06.002
54. Pan, W., Banks, W. A., Fasold, M. B., Bluth, J., and Kastin, A. J. (1998). Transport of brain-derived neurotrhophic factor across the blood brain barrier. Nueropharmacology 37, 1553-1561. doi: 10.1016/S0028-3908(98)00141-5
55. Pardridge, W. M., Kang, Y. S., and Buckiak, J. L. (1994). Transport of human recombinant brain-derived neurotrophic factor (BDNF) through the rat blood-brain barrier in vivo using vector-mediated peptide drug delivery. Pharm. Res. 11, 738-746. doi: 10.1023/A:1018940732550
56. Percy, A. K., and Lane, J. B. (2004). Rett syndrome: clinical and molecular update. Curr. Opin. Paediatr. 16, 670-677. doi: 10.1097/01.mop.0000143693.59408.ce
57. Phelan, K., and McDermid, H. E. (2012). The 22q13.3 deletion syndrome (Phelan-McDermid syndrome). Mol. Syndromol. 2, 186-201. doi: 10.1159/000334260
58. Pini, G., Congiu, L., Benicasa, A., DiMarco, P., Bigoni, S., Dyer, A. H., et al. (2016). Illness severity, social and cognitive ability, and EEG analysis of ten patients with rett syndrome treated with mecasermin (recombinant human IGF-1). Autism Res. Treat. 2016:5073078. doi: 10.1155/2016/5073078
59. Pini, G., Scusa, M. F., Benincasa, A., Bottliglioni, I., Congiu, L., Vahdatpour, C., et al. (2014). Repeated insulin-like growth factor 1 treatment in a patient with rett syndrome: a single case study. Front. Paediatry 2:52. doi: 10.3389/fped.2014.00052
60. Pini, G., Scusa, M. F., Congiu, L., Benincasa, A., Morescalchi, P., Bottliglioni, I., et al. (2012). IGF1 as a potential treatment for rett syndrome: safety assessment in six rett patients. Autism Res. Treat. 2012:679801. doi: 10.1155/2012/679801
61. Poduslo, J. F., and Curran, G. L. (1996). Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF. Brain Res. Mol. Brain Res. 36, 280-286. doi: 10.1016/0169-328X(95)00250-V
62. Popken, G. J., Hodge, R. F., Ye, P., Zhang, J., Ng, W., O'Kusky, J. R., et al. (2004). In vivo effects of insulin-like growth factor-I (IGF-I) on prenatal and early postnatal development of the central nervous system. Eur. J. Neurosci. 19, 2056-2068. doi: 10.1111/j.0953-816X.2004.03320.x
63. Riikonen, R., Turpeinen, U., and Riikonen, R. (2001). Cerebrospinal fluid insulin-like growth factors IGF-1 and IGF-2 in infantile autism. Dev. Med. Chlild Neurol. 43, 614-616. doi: 10.1017/S0012162201001116
64. Roussignol, G., Ango, F., Romorini, S., Tu, J. C., Sala, C., Worley, P. F., et al. (2005). Shank expression is sufficient to induce functional dendritic spine synapses in aspiny neurons. J. Neurosci. 25, 3560-3570. doi: 10.1523/jneurosci.4354-04.2005
65. Shcheglovitov, A., Shcheglovitova, O., Yazawa, M., Portmann, T., Shu, R., Sebastino, V., et al. (2013). SHANK3 and IGF1 restore synaptic deficits in neurons from 22q13 deletion syndrome patients. Nature 503, 267-271. doi: 10.1038/nature12618
66. Supeno, N. E., Pati, S., Hadi, R. A., Ghani, A. R., Mustafa, Z., Abdullah, J. M., et al. (2013). IGF-1 acts as controlling switch for long-term proliferation and maintenance of EGF/FGF-responsive striatal neural stem cells. Int. J. Med. Sci. 10, 522-531. doi: 10.7150/ijms.5325
67. Tropea, D., Diacometti, E., Wilson, N. R., Beard, C., McCurry, C., Fu, D. D., et al. (2009). Partial reversal of Rett Syndrome-like symptoms in MeCP2 mutant mice. Proc. Natl. Acad. Sci. U.S.A. 106, 2029-2034. doi: 10.1073/pnas.0812394106
68. Tropea, D., Mortimer, N., Bellini, S., Molinos, I., Sanfeliu, A., Shovlin, S., et al. (2016). Expression of nuclear Methyl-CpG binding protein 2 (Mecp2) is dependent on neuronal stimulation and application of Insulin-like growth factor 1. Neurosci. Lett. 621, 111-116. doi: 10.1016/j.neulet.2016.04.024
69. Vanhala, R., Turpeinen, U., and Riikonen, R. (2006). Low levels of insulin-like growth factor-I in cerebrospinal fluid in children with autism. Dev. Med. Child Neurol. 48, 751-755. doi: 10.1017/S0012162206001605
70. Wang, H., and Doering, L. C. (2015). Autism spectrum disorders: emerging mechanisms and mechanism-based treatment. Front. Cell Neursci. 9:183. doi: 10.3389/fncel.2015.00183
71. Wang, K., Zhang, H., Ma, D., Bucan, M., Glessner, J. T., Abrahams, B. S., et al. (2009). Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature 459, 528-533. doi: 10.1038/nature07999
72. Weng, N., Weller, I. J., Sumis, A., Berry-Kravis, E., and Greenough, W. T. (2008). Early-phase ERK activation as a biomarker for metabolic status in fragile X syndrome. Am. J. Med. Genet. B Neuropsychiatr. Genet. 147B, 1253-1257. doi: 10.1002/ajmg.b.30765
73. Woods, K. A., Camacho-Hübner, C., Savage, M. O., and Clark, A. J. (1996). Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N. Engl. J. Med. 335, 1363-1367. doi: 10.1056/NEJM199610313351805
74. Zhang, J., Moats-Staats, B. M., Ye, P., and D'Ercole, A. J. (2007). Expression of insulin-like growth factor system genes during the early postnatal neurogenesis in the mouse hippocampus. J. Neurosci. Res. 85, 1618-1627. doi: 10.1002/jnr.21289
75. Zhou, Z., Hong, E. J., Cohen, S., Zhao, W. N., Ho, H. Y., and Schmidt, L. (2006). Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255-269. doi: 10.1016/j.neuron.2006.09.037