Altered Levels of MicroRNA-9,-206, and-132 in Spinal Muscular Atrophy and Their Response to Antisense Oligonucleotide Therapy

Molecular Therapy Nucleic Acids

Volumn 5, Issue 7, 2016, Pages e331-

  Catapano, Francesco ^a   Zaharieva, Irina ^a   Scoto, Mariacristina ^a   Marrosu, Elena ^a   Morgan, Jennifer ^a   Muntoni, Francesco ^a   Zhou, Haiyan ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Antisense oligonucleotides therapy; biomarker; micro RNA; spinal muscular atrophy

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; MICRORNA; MICRORNA 132; MICRORNA 206; MICRORNA 9; PMO 25; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTISENSE THERAPY; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; HUMAN; HUMAN TISSUE; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; SPINAL CORD; SPINAL MUSCULAR ATROPHY;

EID: 84977478368     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2016.47     Document Type: Article

References (53)

1. Shababi, M, Lorson, CL and Rudnik-Schöneborn, SS (2014). Spinal muscular atrophy: a motor neuron disorder or a multi-organ disease J Anat 224: 15-28.
2. Hua, Y, Sahashi, K, Rigo, F, Hung, G, Horev, G, Bennett, CF et al. (2011). Peripheral SMN restoration is essential for long-term rescue of a severe spinal muscular atrophy mouse model. Nature 478: 123-126.
3. Mitrpant, C, Porensky, P, Zhou, H, Price, L, Muntoni, F, Fletcher, S et al. (2013). Improved antisense oligonucleotide design to suppress aberrant SMN2 gene transcript processing: towards a treatment for spinal muscular atrophy. PLoS One 8: e62114.
4. Passini, MA, Bu, J, Richards, AM, Kinnecom, C, Sardi, SP, Stanek, LM et al. (2011). Antisense oligonucleotides delivered to the mouse CNS ameliorate symptoms of severe spinal muscular atrophy. Sci Transl Med 3: 72ra18.
5. Porensky, PN, Mitrpant, C, McGovern, VL, Bevan, AK, Foust, KD, Kaspar, BK et al. (2012). A single administration of morpholino antisense oligomer rescues spinal muscular atrophy in mouse. Hum Mol Genet 21: 1625-1638.
6. Zhou, H, Janghra, N, Mitrpant, C, Dickinson, RL, Anthony, K, Price, L et al. (2013). A novel morpholino oligomer targeting ISS-N1 improves rescue of severe spinal muscular atrophy transgenic mice. Hum Gene Ther 24: 331-342.
7. Dominguez, E, Marais, T, Chatauret, N, Benkhelifa-Ziyyat, S, Duque, S, Ravassard, P et al. (2011). Intravenous scAAV9 delivery of a codon-optimized SMN1 sequence rescues SMA mice. Hum Mol Genet 20: 681-693.
8. Foust, KD, Wang, X, McGovern, VL, Braun, L, Bevan, AK, Haidet, AM et al. (2010). Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat Biotechnol 28: 271-274.
9. Passini, MA, Bu, J, Roskelley, EM, Richards, AM, Sardi, SP, O'Riordan, CR et al. (2010). CNS-targeted gene therapy improves survival and motor function in a mouse model of spinal muscular atrophy. J Clin Invest 120: 1253-1264.
10. Valori, CF, Ning, K, Wyles, M, Mead, RJ, Grierson, AJ, Shaw, PJ et al. (2010). Systemic delivery of scAAV9 expressing SMN prolongs survival in a model of spinal muscular atrophy. Sci Transl Med 2: 35ra42.
11. Naryshkin, NA, Weetall, M, Dakka, A, Narasimhan, J, Zhao, X, Feng, Z et al. (2014). Motor neuron disease. SMN2 splicing modifiers improve motor function and longevity in mice with spinal muscular atrophy. Science 345: 688-693.
12. Palacino, J, Swalley, SE, Song, C, Cheung, AK, Shu, L, Zhang, X et al. (2015). SMN2 splice modulators enhance U1-pre-mRNA association and rescue SMA mice. Nat Chem Biol 11: 511-517
13. Chiriboga, CA, Swoboda, KJ, Darras, BT, Iannaccone, ST, Montes, J, De Vivo, DC et al. (2016). Results from a phase 1 study of nusinersen (ISIS-SMNRx) in children with spinal muscular atrophy. Neurology 86: 890-897.
14. Zaharieva, IT, Calissano, M, Scoto, M, Preston, M, Cirak, S, Feng, L et al. (2013). Dystromirs as serum biomarkers for monitoring the disease severity in Duchenne muscular Dystrophy. PLoS One 8: e80263.
15. Roberts, TC, Blomberg, KE, McClorey, G, El Andaloussi, S, Godfrey, C, Betts, C et al. (2012). Expression analysis in multiple muscle groups and serum reveals complexity in the microRNA transcriptome of the mdx mouse with implications for therapy. Mol Ther Nucleic Acids 1: e39.
16. Roberts, TC, Godfrey, C, McClorey, G, Vader, P, Briggs, D, Gardiner, C et al. (2013). Extracellular microRNAs are dynamic non-vesicular biomarkers of muscle turnover. Nucleic Acids Res 41: 9500-9513.
17. Vignier, N, Amor, F, Fogel, P, Duvallet, A, Poupiot, J, Charrier, S et al. (2013). Distinctive serum miRNA profile in mouse models of striated muscular pathologies. PLoS One 8: e55281.
18. McWhorter, ML, Monani, UR, Burghes, AH and Beattie, CE (2003). Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. J Cell Biol 162: 919-931.
19. Haramati, S, Chapnik, E, Sztainberg, Y, Eilam, R, Zwang, R, Gershoni, N et al. (2010). miRNA malfunction causes spinal motor neuron disease. Proc Natl Acad Sci USA 107: 13111-13116.
20. Dajas-Bailador, F, Bonev, B, Garcez, P, Stanley, P, Guillemot, F and Papalopulu, N (2012). microRNA-9 regulates axon extension and branching by targeting Map1b in mouse cortical neurons. Nat Neurosci 15: 697-699.
21. Wu, D, Raafat, A, Pak, E, Clemens, S and Murashov, AK (2012). Dicer-microRNA pathway is critical for peripheral nerve regeneration and functional recovery in vivo and regenerative axonogenesis in vitro. Exp Neurol 233: 555-565.
22. Magill, ST, Cambronne, XA, Luikart, BW, Lioy, DT, Leighton, BH, Westbrook, GL et al. (2010). microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc Natl Acad Sci USA 107: 20382-20387.
23. Kawashima, H, Numakawa, T, Kumamaru, E, Adachi, N, Mizuno, H, Ninomiya, M et al. (2010). Glucocorticoid attenuates brain-derived neurotrophic factor-dependent upregulation of glutamate receptors via the suppression of microRNA-132 expression. Neuroscience 165: 1301-1311.
24. Clovis, YM, Enard, W, Marinaro, F, Huttner, WB and De Pietri Tonelli, D (2012). Convergent repression of Foxp2 3'UTR by miR-9 and miR-132 in embryonic mouse neocortex: implications for radial migration of neurons. Development 139: 3332-3342.
25. Anand, S, Majeti, BK, Acevedo, LM, Murphy, EA, Mukthavaram, R, Scheppke, L et al. (2010). MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat Med 16: 909-914.
26. Somers, E, Stencel, Z, Wishart, TM, Gillingwater, TH and Parson, SH (2012). Density, calibre and ramification of muscle capillaries are altered in a mouse model of severe spinal muscular atrophy. Neuromuscul Disord 22: 435-442.
27. Somers, E, Lees, RD, Hoban, K, Sleigh, JN, Zhou, H, Muntoni, F et al. (2016). Vascular Defects and Spinal Cord Hypoxia in Spinal Muscular Atrophy. Ann Neurol 79: 217-230.
28. Boyer, JG, Deguise, MO, Murray, LM, Yazdani, A, De Repentigny, Y, Boudreau-Larivière, C et al. (2014). Myogenic program dysregulation is contributory to disease pathogenesis in spinal muscular atrophy. Hum Mol Genet 23: 4249-4259.
29. Bricceno, KV, Martinez, T, Leikina, E, Duguez, S, Partridge, TA, Chernomordik, LV et al. (2014). Survival motor neuron protein deficiency impairs myotube formation by altering myogenic gene expression and focal adhesion dynamics. Hum Mol Genet 23: 4745-4757.
30. Kim, HK, Lee, YS, Sivaprasad, U, Malhotra, A and Dutta, A (2006). Muscle-specific microRNA miR-206 promotes muscle differentiation. J Cell Biol 174: 677-687.
31. Williams, AH, Valdez, G, Moresi, V, Qi, X, McAnally, J, Elliott, JL et al. (2009). MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 326: 1549-1554.
32. Valdez, G, Heyer, MP, Feng, G and Sanes, JR (2014). The role of muscle microRNAs in repairing the neuromuscular junction. PLoS One 9: e93140.
33. Toivonen, JM, Manzano, R, Oliván, S, Zaragoza, P, Garciá-Redondo, A and Osta, R (2014). MicroRNA-206: a potential circulating biomarker candidate for amyotrophic lateral sclerosis. PLoS One 9: e89065.
34. Valsecchi, V, Boido, M, De Amicis, E, Piras, A and Vercelli, A (2015). Expression of muscle-specific MiRNA 206 in the progression of disease in a murine SMA model. PLoS One 10: e0128560.
35. Hsieh-Li, HM, Chang, JG, Jong, YJ, Wu, MH, Wang, NM, Tsai, CH et al. (2000). A mouse model for spinal muscular atrophy. Nat Genet 24: 66-70.
36. Zhou, H, Meng, J, Marrosu, E, Janghra, N, Morgan, J and Muntoni, F (2015). Repeated low doses of morpholino antisense oligomer: an intermediate mouse model of spinal muscular atrophy to explore the window of therapeutic response. Hum Mol Genet 24: 6265-6277.
37. Coolen, M, Katz, S and Bally-Cuif, L (2013). miR-9: a versatile regulator of neurogenesis. Front Cell Neurosci 7: 220.
38. Cogswell, JP, Ward, J, Taylor, IA, Waters, M, Shi, Y, Cannon, B et al. (2008). Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J Alzheimers Dis 14: 27-41.
39. Kim, J, Inoue, K, Ishii, J, Vanti, WB, Voronov, SV, Murchison, E et al. (2007). A MicroRNA feedback circuit in midbrain dopamine neurons. Science 317: 1220-1224.
40. Wang, LT, Chiou, SS, Liao, YM, Jong, YJ and Hsu, SH (2014). Survival of motor neuron protein downregulates miR-9 expression in patients with spinal muscular atrophy. Kaohsiung J Med Sci 30: 229-234.
41. Cacchiarelli, D, Legnini, I, Martone, J, Cazzella, V, D'Amico, A, Bertini, E et al. (2011). miRNAs as serum biomarkers for Duchenne muscular dystrophy. EMBO Mol Med 3: 258-265.
42. Mizuno, H, Nakamura, A, Aoki, Y, Ito, N, Kishi, S, Yamamoto, K et al. (2011). Identification of muscle-specific microRNAs in serum of muscular dystrophy animal models: promising novel blood-based markers for muscular dystrophy. PLoS One 6: e18388.
43. Arroyo, JD, Chevillet, JR, Kroh, EM, Ruf, IK, Pritchard, CC, Gibson, DF et al. (2011). Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108: 5003-5008.
44. Hamilton, G and Gillingwater, TH (2013). Spinal muscular atrophy: going beyond the motor neuron. Trends Mol Med 19: 40-50.
45. Hunter, G, Aghamaleky Sarvestany, A, Roche, SL, Symes, RC and Gillingwater, TH (2014). SMN-dependent intrinsic defects in Schwann cells in mouse models of spinal muscular atrophy. Hum Mol Genet 23: 2235-2250.
46. Hao, le T, Duy, PQ, Jontes, JD and Beattie, CE (2015). Motoneuron development influences dorsal root ganglia survival and Schwann cell development in a vertebrate model of spinal muscular atrophy. Hum Mol Genet 24: 346-360.
47. Araujo, Ap, Araujo, M and Swoboda, KJ (2009). Vascular perfusion abnormalities in infants with spinal muscular atrophy. J Pediatr 155: 292-294.
48. Rudnik-Schöneborn, S, Vogelgesang, S, Armbrust, S, Graul-Neumann, L, Fusch, C and Zerres, K (2010). Digital necroses and vascular thrombosis in severe spinal muscular atrophy. Muscle Nerve 42: 144-147.
49. Sintusek, P, Catapano, F, Angkathunkayul, N, Marrosu, E, Parson, SH, Morgan, JE et al. (2016). Histopathological defects in intestine in severe spinal muscular atrophy mice are improved by systemic antisense oligonucleotide treatment. PLoS One 11: e0155032.
50. Santulli, G (2015). MicroRNAs and endothelial (Dys) function. J Cell Physiol 9999: 1-7.
51. Arunachalam, G, Upadhyay, R, Ding, H and Triggle, CR (2015). MicroRNA signature and cardiovascular dysfunction. J Cardiovasc Pharmacol 65: 419-429.
52. Kato, M and Natarajan, R (2015). MicroRNAs in diabetic nephropathy: functions, biomarkers, and therapeutic targets. Ann N Y Acad Sci 1353: 72-88.
53. Mitchell, PS, Parkin, RK, Kroh, EM, Fritz, BR, Wyman, SK, Pogosova-Agadjanyan, EL et al. (2008). Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105: 10513-10518.