Loganin possesses neuroprotective properties, restores SMN protein and activates protein synthesis positive regulator Akt/mTOR in experimental models of spinal muscular atrophy

Pharmacological Research

Volumn 111, Issue , 2016, Pages 58-75

  Tseng, Yu Ting ^a   Chen, Cheng Sheng ^a,c   Jong, Yuh Jyh ^b,c,d   Chang, Fang Rong ^a   Lo, Yi Ching ^a,b  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL CHIAO TUNG UNIVERSITY   (Taiwan)

Author keywords

Akt mTOR; IGF 1; Loganin; Muscular atrophy; Neuroprotection; Survival motor neuron protein

Indexed keywords

ATROGIN 1; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GEMIN2 PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; HELICASE; LOGANIN; MAMMALIAN TARGET OF RAPAMYCIN; MUSCLE RING FINGER 1 PROTEIN; PROTEIN BCL 2; PROTEIN KINASE B; SMALL INTERFERING RNA; SURVIVAL MOTOR NEURON PROTEIN; UNCLASSIFIED DRUG; FBXO32 PROTEIN, MOUSE; INSULIN-LIKE GROWTH FACTOR-1, MOUSE; IRIDOID; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; MUSCLE PROTEIN; NEUROPROTECTIVE AGENT; SMN1 PROTEIN, MOUSE; SOMATOMEDIN C; SURVIVAL MOTOR NEURON PROTEIN 1; TARGET OF RAPAMYCIN KINASE; TRIM63 PROTEIN, MOUSE; TRIPARTITE MOTIF PROTEIN; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; GASTROCNEMIUS MUSCLE; HIND LIMB SUSPENSION TEST; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIFESPAN; MOTOR FUNCTION TEST; MOUSE; MUSCLE PROTECTION; MUSCLE STRENGTH; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS REGULATION; RIGHTING REFLEX TEST; SPINAL MUSCULAR ATROPHY; UPREGULATION; ANIMAL; APOPTOSIS; BIOSYNTHESIS; CELL LINE; CELL PROTECTION; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; FIBROBLAST; GENETIC PREDISPOSITION; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOTONEURON; MOTOR ACTIVITY; MUTATION; NERVE DEGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PHOSPHORYLATION; PROTEIN SYNTHESIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIME FACTOR; TRANSGENIC MOUSE; WEIGHT GAIN;

ANIMALS; APOPTOSIS; CELL LINE; CYTOPROTECTION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROBLASTS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; IRIDOIDS; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; MOTOR NEURONS; MUSCLE PROTEINS; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR ATROPHY, SPINAL; MUTATION; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; PHENOTYPE; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; SURVIVAL OF MOTOR NEURON 1 PROTEIN; TIME FACTORS; TOR SERINE-THREONINE KINASES; TRANSFECTION; TRIPARTITE MOTIF PROTEINS; UBIQUITIN-PROTEIN LIGASES; WEIGHT GAIN;

EID: 84976295564     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2016.05.023     Document Type: Article

References (67)

1. [1] Lefebvre, S.L., Burglen, S., Reboullet, O., Clermont, P., Burlet, L., Viollet, B., Benichou, C., Cruaud, P., Millasseau Zeviani, M., et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80:1 (1995), 155–165.
2. [2] K. Zerresand, K.E. Davies, 59th ENMC International Workshop: Spinal Muscular Atrophies: recent progress and revised diagnostic criteria 17–19 April 1998, Soestduinen, The Netherlands.N euromuscul Disord. 9 (4) (1999) 272–278.
3. [3] Dubowitz, V., Very severe spinal muscular atrophy (SMA type 0): an expanding clinical phenotype. Eur. J. Paediatr. Neurol. 3:2 (1999), 49–51.
4. [4] Russman, B.S., Spinal muscular atrophy: clinical classification and disease heterogeneity. J. Child. Neurol. 22:8 (2007), 946–951.
5. [5] Lunnand, M.R., Wang, C.H., Spinal muscular atrophy. Lancet 371:9630 (2008), 2120–2133.
6. [6] Lefebvre, S., Burlet, P., Liu, Q., Bertrandy, S., Clermont, O., Munnich, A., Dreyfuss, G., Melki, J., Correlation between severity and SMN protein level in spinal muscular atrophy. Nat. Genet. 16:3 (1997), 265–269.
7. [7] Fanand, L., Simard, L.R., Survival motor neuron (SMN) protein: role in neurite outgrowth and neuromuscular maturation during neuronal differentiation and development. Hum. Mol Genet. 11:14 (2002), 1605–1614.
8. [8] Burghesand, A.H., Beattie, C.E., Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick?. Nat. Rev. Neurosci. 10:8 (2009), 597–609.
9. [9] Pearn, J., Classification of spinal muscular atrophies. Lancet 1:8174 (1980), 919–922.
10. [10] Singh, P., Liew, W.K., Darras, B.T., Current advances in drug development in spinal muscular atrophy. Curr. Opin. Pediatr. 25:6 (2013), 682–688.
11. [11] Lorsonand, M.A., Lorson, C.L., SMN-inducing compounds for the treatment of spinal muscular atrophy. Future Med. Chem. 4:16 (2012), 2067–2084.
12. [12] Cauchi, R.J., SMN and Gemins: ‘we are family’ or are we?: insights into the partnership between Gemins and the spinal muscular atrophy disease protein SMN. Bioessays 32:12 (2010), 1077–1089.
13. [13] Paushkin, S., Gubitz, A.K., Massenet, S., Dreyfuss, G., The SMN complex, an assemblyosome of ribonucleoproteins. Curr. Opin. Cell Biol. 14:3 (2002), 305–312.
14. [14] Jablonka, S., Holtmann, B., Meister, G., Bandilla, M., Rossoll, W., Fischer, U., Sendtner, M., Gene targeting of Gemin2 in mice reveals a correlation between defects in the biogenesis of U snRNPs and motoneuron cell death. Proc. Natl. Acad. Sci. U. S. A. 99:15 (2002), 10126–10131.
15. [15] Feng, W., Gubitz, A.K., Wan, L., Battle, D.J., Dostie, J., Golembe, T.J., Dreyfuss, G., Gemins modulate the expression and activity of the SMN complex. Hum. Mol. Genet. 14:12 (2005), 1605–1611.
16. [16] Hsu, Y.Y., Jong, Y.J., Tsai, H.H., Tseng, Y.T., An, L.M., Lo, Y.C., Triptolide increases transcript and protein levels of survival motor neurons in human SMA fibroblasts and improves survival in SMA-like mice. Br. J. Pharmacol. 166:3 (2012), 1114–1126.
17. [17] Cherry, J.J., Osman, E.Y., Evans, M.C., Choi, S., Xing, X., Cuny, G.D., Glicksman, M.A., Lorson, C.L., Androphy, E.J., Enhancement of SMN protein levels in a mouse model of spinal muscular atrophy using novel drug-like compounds. EMBO Mol. Med. 5:7 (2013), 1035–1050.
18. [18] Engvalland, E., Wewer, U.M., The new frontier in muscular dystrophy research: booster genes. FASEB J. 17:12 (2003), 1579–1584.
19. [19] Schiaffino, S., Dyar, K.A., Ciciliot, S., Blaauw, B., Sandri, M., Mechanisms regulating skeletal muscle growth and atrophy. FEBS J. 280:17 (2013), 4294–4314.
20. [20] Millino, C., Fanin, M., Vettori, A., Laveder, P., Mostacciuolo, M.L., Angelini, C., Lanfranchi, G., Different atrophy-hypertrophy transcription pathways in muscles affected by severe and mild spinal muscular atrophy. BMC Med., 7, 2009, 14.
21. [21] Biondi, O., Branchu, J., Sanchez, G., Lancelin, C., Deforges, S., Lopes, P., Pariset, C., Lecolle, S., Cote, J., Chanoine, C., Charbonnier, F., In vivo NMDA receptor activation accelerates motor unit maturation, protects spinal motor neurons, and enhances SMN2 gene expression in severe spinal muscular atrophy mice. J. Neurosci. 30:34 (2010), 11288–11299.
22. [22] Biondi, O., Branchu, J., Ben Salah, A., Houdebine, L., Bertin, L., Chali, F., Desseille, C., Weill, L., Sanchez, G., Lancelin, C., Aid, S., Lopes, P., Pariset, C., Lecolle, S., Cote, J., Holzenberger, M., Chanoine, C., Massaad, C., Charbonnier, F., IGF-1R reduction triggers neuroprotective signaling pathways in spinal muscular atrophy mice. J. Neurosci. 35:34 (2015), 12063–12079.
23. [23] Branchu, J., Biondi, O., Chali, F., Collin, T., Leroy, F., Mamchaoui, K., Makoukji, J., Pariset, C., Lopes, P., Massaad, C., Chanoine, C., Charbonnier, F., Shift from extracellular signal-regulated kinase to AKT/cAMP response element-binding protein pathway increases survival-motor-neuron expression in spinal-muscular-atrophy-like mice and patient cells. J. Neurosci. 33:10 (2013), 4280–4294.
24. [24] Bodine, S.C., Latres, E., Baumhueter, S., Lai, V.K., Nunez, L., Clarke, B.A., Poueymirou, W.T., Panaro, F.J., Na, E., Dharmarajan, K., Pan, Z.Q., Valenzuela, D.M., DeChiara, T.M., Stitt, T.N., Yancopoulos, G.D., Glass, D.J., Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:5547 (2001), 1704–1708.
25. [25] Iyer, C.C., McGovern, V.L., Wise, D.O., Glass, D.J., Burghes, A.H., Deletion of atrophy enhancing genes fails to ameliorate the phenotype in a mouse model of spinal muscular atrophy. Neuromuscul. Disord. 24:5 (2014), 436–444.
26. [26] Liou, S.S., Liu, I.M., Hsu, S.F., Cheng, J.T., Corni fructus as the major herb of Die-Huang-Wan for lowering plasma glucose in Wistar rats. J. Pharm. Pharmacol. 56:11 (2004), 1443–1447.
27. [27] Park, C.H., Tanaka, T., Kim, J.H., Cho, E.J., Park, J.C., Shibahara, N., Yokozawa, T., Hepato-protective effects of loganin, iridoid glycoside from Corni Fructus, against hyperglycemia-activated signaling pathway in liver of type 2 diabetic db/db mice. Toxicology 290:1 (2011), 14–21.
28. [28] Kwon, S.H., Kim, J.A., Hong, S.I., Jung, Y.H., Kim, H.C., Lee, S.Y., Jang, C.G., Loganin protects against hydrogen peroxide-induced apoptosis by inhibiting phosphorylation of JNK, p38, and ERK 1/2 MAPKs in SH-SY5Y cells. Neurochem. Int. 58:4 (2011), 533–541.
29. [29] Babri, S., Hasani Azami, S., Mohaddes, G., Effect of acute administration of loganin on spatial memory in diabetic male rats. Adv. Pharm. Bull. 3:1 (2013), 91–95.
30. [30] Kwon, S.H., Kim, H.C., Lee, S.Y., Jang, C.G., Loganin improves learning and memory impairments induced by scopolamine in mice. Eur. J. Pharmacol. 619:1–3 (2009), 44–49.
31. [31] Jiang, W.L., Zhang, S.P., Hou, J., Zhu, H.B., Effect of loganin on experimental diabetic nephropathy. Phytomedicine 19:3–4 (2012), 217–222.
32. [32] Liu, K., Xu, H., Lv, G., Liu, B., Lee, M.K., Lu, C., Lv, X., Wu, Y., Loganin attenuates diabetic nephropathy in C57BL/6J mice with diabetes induced by streptozotocin and fed with diets containing high level of advanced glycation end products. Life Sci. 123 (2015), 78–85.
33. [33] Lee, C.M., Jung, H.A., Oh, S.H., Park, C.H., Tanaka, T., Yokozawa, T., Choi, J.S., Kinetic and molecular docking studies of loganin and 7-O-galloyl-D-sedoheptulose from Corni Fructus as therapeutic agents for diabetic complications through inhibition of aldose reductase. Arch. Pharm. Res. 38:6 (2015), 1090–1098.
34. [34] Ma, W., Wang, K.J., Cheng, C.S., Yan, G.Q., Lu, W.L., Ge, J.F., Cheng, Y.X., Li, N., Bioactive compounds from Cornus officinalis fruits and their effects on diabetic nephropathy. J. Ethnopharmacol. 153:3 (2014), 840–845.
35. [35] Wen, H.L., Lin, Y.T., Ting, C.H., Lin-Chao, S., Li, H., Hsieh-Li, H.M., Stathmin, a microtubule-destabilizing protein, is dysregulated in spinal muscular atrophy. Hum. Mol. Genet. 19:9 (2010), 1766–1778.
36. [36] Le, T.T., Pham, L.T., Butchbach, M.E., Zhang, H.L., Monani, U.R., Coovert, D.D., Gavrilina, T.O., Xing, L., Bassell, G.J., Burghes, A.H., SMNDelta7, the major product of the centromeric survival motor neuron (SMN2) gene, extends survival in mice with spinal muscular atrophy and associates with full-length SMN. Hum. Mol. Genet. 14:6 (2005), 845–857.
37. [37] Sleigh, J.N., Gillingwater, T.H., Talbot, K., The contribution of mouse models to understanding the pathogenesis of spinal muscular atrophy. Dis. Model Mech. 4:4 (2011), 457–467.
38. [38] Hsu, Y.Y., Tseng, Y.T., Lo, Y.C., Berberine, a natural antidiabetes drug, attenuates glucose neurotoxicity and promotes Nrf2-related neurite outgrowth. Toxicol. Appl. Pharmacol. 272:3 (2013), 787–796.
39. [39] El-Khodor, B.F., Edgar, N., Chen, A., Winberg, M.L., Joyce, C., Brunner, D., Suarez-Farinas, M., Heyes, M.P., Identification of a battery of tests for drug candidate evaluation in the SMNDelta7 neonate model of spinal muscular atrophy. Exp. Neurol. 212:1 (2008), 29–43.
40. [40] Zhang, H., Xing, L., Rossoll, W., Wichterle, H., Singer, R.H., Bassell, G.J., Multiprotein complexes of the survival of motor neuron protein SMN with Gemins traffic to neuronal processes and growth cones of motor neurons. J. Neurosci. 26:33 (2006), 8622–8632.
41. [41] Rathod, R., Havlicek, S., Frank, N., Blum, R., Sendtner, M., Laminin induced local axonal translation of beta-actin mRNA is impaired in SMN-deficient motoneurons. Histochem. Cell Biol. 138:5 (2012), 737–748.
42. [42] Ling, K.K., Lin, M.Y., Zingg, B., Feng, Z., Ko, C.P., Synaptic defects in the spinal and neuromuscular circuitry in a mouse model of spinal muscular atrophy. PLoS One, 5(11), 2010, e15457.
43. [43] Ning, K., Drepper, C., Valori, C.F., Ahsan, M., Wyles, M., Higginbottom, A., Herrmann, T., Shaw, P., Azzouz, M., Sendtner, M., PTEN depletion rescues axonal growth defect and improves survival in SMN-deficient motor neurons. Hum. Mol. Genet. 19:16 (2010), 3159–3168.
44. [44] Klesse, L.J., Meyers, K.A., Marshall, C.J., Parada, L.F., Nerve growth factor induces survival and differentiation through two distinct signaling cascades in PC12 cells. Oncogene 18:12 (1999), 2055–2068.
45. [45] Namikawa, K., Honma, M., Abe, K., Takeda, M., Mansur, K., Obata, T., Miwa, A., Okado, H., Kiyama, H., Akt/protein kinase B prevents injury-induced motoneuron death and accelerates axonal regeneration. J. Neurosci. 20:8 (2000), 2875–2886.
46. [46] Kim, Y., Seger, R., Suresh Babu, C.V., Hwang, S.Y., Yoo, Y.S., A positive role of the PI3-K/Akt signaling pathway in PC12 cell differentiation. Mol. Cells 18:3 (2004), 353–359.
47. [47] Yong, J., Wan, L., Dreyfuss, G., Why do cells need an assembly machine for RNA-protein complexes?. Trends Cell Biol. 14:5 (2004), 226–232.
48. [48] Scott Bitner, R., Cyclic AMP response element-binding protein (CREB) phosphorylation: a mechanistic marker in the development of memory enhancing Alzheimer's disease therapeutics. Biochem. Pharmacol. 83:6 (2012), 705–714.
49. [49] Fujii, M., Sherchan, P., Soejima, Y., Hasegawa, Y., Flores, J., Doycheva, D., Zhang, J.H., Cannabinoid receptor type 2 agonist attenuates apoptosis by activation of phosphorylated CREB-Bcl-2 pathway after subarachnoid hemorrhage in rats. Exp. Neurol. 261 (2014), 396–403.
50. [50] Ozdinlerand, P.H., Macklis, J.D., IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat. Neurosci. 9:11 (2006), 1371–1381.
51. [51] Duan, C., Ren, H., Gao, S., Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: roles in skeletal muscle growth and differentiation. Gen. Comp. Endocrinol. 167:3 (2010), 344–351.
52. [52] Bosch-Marce, M., Wee, C.D., Martinez, T.L., Lipkes, C.E., Choe, D.W., Kong, L., Van Meerbeke, J.P., Musaro, A., Sumner, C.J., Increased IGF-1 in muscle modulates the phenotype of severe SMA mice. Hum. Mol. Genet. 20:9 (2011), 1844–1853.
53. [53] Tsai, L.K., Chen, C.L., Ting, C.H., Lin-Chao, S., Hwu, W.L., Dodge, J.C., Passini, M.A., Cheng, S.H., Systemic administration of a recombinant AAV1 vector encoding IGF-1 improves disease manifestations in SMA mice. Mol. Ther. 22:8 (2014), 1450–1459.
54. [54] Murdocca, M., Malgieri, A., Luchetti, A., Saieva, L., Dobrowolny, G., de Leonibus, E., Filareto, A., Quitadamo, M.C., Novelli, G., Musaro, A., Sangiuolo, F., IPLEX administration improves motor neuron survival and ameliorates motor functions in a severe mouse model of spinal muscular atrophy. Mol. Med. 18 (2012), 1076–1085.
55. [55] Zhang, R., So, B.R., Li, P., Yong, J., Glisovic, T., Wan, L., Dreyfuss, G., Structure of a key intermediate of the SMN complex reveals Gemin2's crucial function in snRNP assembly. Cell 146:3 (2011), 384–395.
56. [56] Naryshkin, N.A., Weetall, M., Dakka, A., Narasimhan, J., Zhao, X., Feng, Z., Ling, K.K., Karp, G.M., Qi, H., Woll, M.G., Chen, G., Zhang, N., Gabbeta, V., Vazirani, P., Bhattacharyya, A., Furia, B., Risher, N., Sheedy, J., Kong, R., Ma, J., Turpoff, A., Lee, C.S., Zhang, X., Moon, Y.C., Trifillis, P., Welch, E.M., Colacino, J.M., Babiak, J., Almstead, N.G., Peltz, S.W., Eng, L.A., Chen, K.S., Mull, J.L., Lynes, M.S., Rubin, L.L., Fontoura, P., Santarelli, L., Haehnke, D., McCarthy, K.D., Schmucki, R., Ebeling, M., Sivaramakrishnan, M., Ko, C.P., Paushkin, S.V., Ratni, H., Gerlach, I., Ghosh, A., Metzger, F., Motor neuron disease SMN2 splicing modifiers improve motor function and longevity in mice with spinal muscular atrophy. Science 345:6197 (2014), 688–693.
57. [57] Monani, U.R., Lorson, C.L., Parsons, D.W., Prior, T.W., Androphy, E.J., Burghes, A.H., McPherson, J.D., A single nucleotide difference that alters splicing patterns distinguishes the SMA gene SMN1 from the copy gene SMN2. Hum. Mol. Genet. 8:7 (1999), 1177–1183.
58. [58] Lorson, C.L., Hahnen, E., Androphy, E.J., Wirth, B., A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc. Natl. Acad. Sci. U. S. A. 96:11 (1999), 6307–6311.
59. [59] Cartegniand, L., Krainer, A.R., Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat. Genet. 30:4 (2002), 377–384.
60. [60] Kashimaand, T., Manley, J.L., A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat. Genet. 34:4 (2003), 460–463.
61. [61] Wishart, T.M., Huang, J.P., Murray, L.M., Lamont, D.J., Mutsaers, C.A., Ross, J., Geldsetzer, P., Ansorge, O., Talbot, K., Parson, S.H., Gillingwater, T.H., SMN deficiency disrupts brain development in a mouse model of severe spinal muscular atrophy. Hum. Mol. Genet. 19:21 (2010), 4216–4228.
62. [62] Bricceno, K.V., Martinez, T., Leikina, E., Duguez, S., Partridge, T.A., Chernomordik, L.V., Fischbeck, K.H., Sumner, C.J., Burnett, B.G., Survival motor neuron protein deficiency impairs myotube formation by altering myogenic gene expression and focal adhesion dynamics. Hum. Mol. Genet. 23:18 (2014), 4745–4757.
63. [63] Rudnik-Schoneborn, S., Heller, R., Berg, C., Betzler, C., Grimm, T., Eggermann, T., Eggermann, K., Wirth, R., Wirth, B., Zerres, K., Congenital heart disease is a feature of severe infantile spinal muscular atrophy. J. Med. Genet. 45:10 (2008), 635–638.
64. [64] Rudnik-Schoneborn, S., Vogelgesang, S., Armbrust, S., Graul-Neumann, L., Fusch, C., Zerres, K., Digital necroses and vascular thrombosis in severe spinal muscular atrophy. Muscle Nerve 42:1 (2010), 144–147.
65. [65] Iyer, C.C., McGovern, V.L., Murray, J.D., Gombash, S.E., Zaworski, P.G., Foust, K.D., Janssen, P.M., Burghes, A.H., Low levels of Survival Motor Neuron protein are sufficient for normal muscle function in the SMNDelta7 mouse model of SMA. Hum. Mol. Genet. 24:21 (2015), 6160–6173.
66. [66] Banerjeeand, A., Guttridge, D.C., Mechanisms for maintaining muscle. Curr. Opin. Support. Palliat Care 6:4 (2012), 451–456.
67. [67] Yuan, L., Han, J., Meng, Q., Xi, Q., Zhuang, Q., Jiang, Y., Han, Y., Zhang, B., Fang, J., Wu, G., Muscle-specific E3 ubiquitin ligases are involved in muscle atrophy of cancer cachexia: an in vitro and in vivo study. Oncol. Rep. 33:5 (2015), 2261–2268.