Characterization of Wnt/β-catenin and BMP/Smad signaling pathways in an in vitro model of amyotrophic lateral sclerosis

Frontiers in Cellular Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Pinto, Cristina ^a   Cárdenas, Pilar ^b   Osses, Nelson ^b   Henríquez, Juan P ^a  

^a UNIVERSITY OF CONCEPCIÓN   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE VALPARAÍSO   (Chile)

Author keywords

ALS; Beta catenin; BMP; Motor neurons; Smad proteins; Wnt

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; LUCIFERASE; SMAD PROTEIN; WNT PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL ADHESION; CELL COUNT; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOCYTOCHEMISTRY; IMMUNODETECTION; IMMUNOFLUORESCENCE MICROSCOPY; PHASE CONTRAST MICROSCOPY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSIENT TRANSFECTION; WESTERN BLOTTING; WNT SIGNALING PATHWAY;

EID: 84889652725     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00239     Document Type: Article

References (76)

1. Alvarez, A. R., Godoy, J. A., Mullendorff, K., Olivares, G. H., Bronfman, M., and Inestrosa, N. C. (2004). Wnt-3a overcomes beta-amyloid toxicity in rat hippocampal neurons. Exp. Cell Res. 297, 186-196. doi: 10.1016/j.yexcr.2004. 02.028
2. Alvarez Perez, M. A., Guarino, V., Cirillo, V., and Ambrosio, L. (2012). In vitro mineralization and bone osteogenesis in poly(epsilon-caprolactone)/gelatin nanofibers. J. Biomed. Mater. Res. A 100, 3008-3019. doi: 10.1002/jbm.a.34233
3. Arber, S., Han, B., Mendelsohn, M., Smith, M., Jessell, T. M., and Sockanathan, S. (1999). Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23, 659-674. doi: 10.1016/S0896-6273(01) 80026-X
4. Arciello, M., Capo, C. R., D'Annibale, S., Cozzolino, M., Ferri, A., Carri, M. T., et al. (2011). Copper depletion increases the mitochondrial-associated SOD1 in neuronal cells. Biometals 24, 269-278. doi: 10.1007/s10534-010-9392-3
5. Basso, M., Pozzi, S., Tortarolo, M., Fiordaliso, F., Bisighini, C., Pasetto, L., et al. (2013). Mutant copper-zinc superoxide dismutase (SOD1) induces protein secretion pathway alterations and exosome release in astrocytes: implications for disease spreading and motor neuron pathology in amyotrophic lateral sclerosis. J. Biol. Chem. 288, 15699-15711. doi: 10.1074/jbc.M112.425066
6. Bayat, V., Jaiswal, M., and Bellen, H. J. (2011). The BMP signaling pathway at the Drosophila neuromuscular junction and its links to neurodegenerative diseases. Curr. Opin. Neurobiol. 21, 182-188. doi: 10.1016/j.conb.2010.08.014
7. Benavente, F., Pinto, C., Parada, M., Henriquez, J. P., and Osses, N. (2012). Bone morphogenetic protein 2 inhibits neurite outgrowth of motor neuron-like NSC- 34 cells and up-regulates its type II receptor. J. Neurochem. 122, 594-604. doi: 10.1111/j.1471-4159.2012.07795.x
8. Bendotti, C., Marino, M., Cheroni, C., Fontana, E., Crippa, V., Poletti, A., et al. (2012). Dysfunction of constitutive and inducible ubiquitin-proteasome system in amyotrophic lateral sclerosis: implication for protein aggregation and immune response. Prog. Neurobiol. 97, 101-126. doi: 10.1016/j.pneurobio.2011. 10.001
9. Bergemalm, D., Forsberg, K., Srivastava, V., Graffmo, K. S., Andersen, P. M., Brannstrom, T., et al. (2010). Superoxide dismutase-1 and other proteins in inclusions from transgenic amyotrophic lateral sclerosis model mice. J. Neurochem. 114, 408-418. doi: 10.1111/j.1471-4159.2010.06753.x
10. Bragdon, B., Moseychuk, O., Saldanha, S., King, D., Julian, J., and Nohe, A. (2011). Bone morphogenetic proteins: a critical review. Cell. Signal. 23, 609-620. doi:10.1016/j.cellsig.2010.10.003
11. Bruijn, L. I., Houseweart, M. K., Kato, S., Anderson, K. L., Anderson, S. D., Ohama, E., et al. (1998). Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 281, 1851-1854. doi:10.1126/science.281.5384.1851
12. Bruijn, L. I., Miller, T. M., and Cleveland, D. W. (2004). Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27, 723-749. doi: 10.1146/annurev.neuro.27.070203.144244
13. Cashman, N. R., Durham, H. D., Blusztajn, J. K., Oda, K., Tabira, T., Shaw, I. T., et al. (1992). Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev. Dyn. 194, 209-221. doi: 10.1002/aja. 1001940306
14. Cerpa, W., Farias, G. G., Godoy, J. A., Fuenzalida, M., Bonansco, C., and Inestrosa, N. C. (2010). Wnt-5a occludes Abeta oligomer-induced depression of glutamatergic transmission in hippocampal neurons. Mol. Neurodegener. 5, 3. doi: 10.1186/1750-1326-5-3
15. Cerpa, W., Gambrill, A., Inestrosa, N. C., and Barria, A. (2011). Regulation of NMDA-receptor synaptic transmission by Wnt signaling. J. Neurosci. 31, 9466-9471. doi: 10.1523/JNEUROSCI.6311-10.2011
16. Chen, Y., Guan, Y., Zhang, Z., Liu, H., Wang, S., Yu, L., et al. (2012). Wnt signaling pathway is involved in the pathogenesis of amyotrophic lateral sclerosis in adult transgenic mice. Neurol. Res. 34, 390-399. doi: 10.1179/1743132812Y. 0000000027
17. De Ferrari, G. V., Chacon, M. A., Barria, M. I., Garrido, J. L., Godoy, J. A., Olivares, G., et al. (2003). Activation of Wnt signaling rescues neurodegeneration and behavioral impairments induced by beta-amyloid fibrils. Mol. Psychiatry 8, 195-208. doi: 10.1038/sj.mp.4001208
18. Durand, J., Amendola, J., Bories, C., and Lamotte D'Incamps, B. (2006). Early abnormalities in transgenic mouse models of amyotrophic lateral sclerosis. J. Physiol. Paris 99, 211-220. doi: 10.1016/j.jphysparis.2005.12.014
19. Ericson, J., Thor, S., Edlund, T., Jessell, T. M., and Yamada, T. (1992). Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555-1560. doi: 10.1126/science.1350865
20. Garrido, J. L., Godoy, J. A., Alvarez, A., Bronfman, M., and Inestrosa, N. C. (2002). Protein kinase C inhibits amyloid beta peptide neurotoxicity by acting on members of the Wnt pathway. FASEB J. 16, 1982-1984.
21. Ghanevati, M., and Miller, C. A. (2005). Phospho-beta-catenin accumulation in Alzheimer's disease and in aggresomes attributable to proteasome dysfunction. J. Mol. Neurosci. 25, 79-94. doi: 10.1385/JMN:25:1:079
22. Godin, J. D., Poizat, G., Hickey, M. A., Maschat, F., and Humbert, S. (2010). Mutant huntingtin-impaired degradation of beta-catenin causes neurotoxicity in Huntington's disease. EMBO J. 29, 2433-2445. doi: 10.1038/emboj.2010.117
23. Gomes, C., Keller, S., Altevogt, P., and Costa, J. (2007). Evidence for secretion of Cu, Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis. Neurosci. Lett. 428, 43-46. doi: 10.1016/j.neulet.2007.09.024
24. Gomes, C., Palma, A. S., Almeida, R., Regalla, M., Mccluskey, L. F., Trojanowski, J. Q., et al. (2008). Establishment of a cell model of ALS disease: Golgi apparatus disruption occurs independently from apoptosis. Biotechnol. Lett. 30, 603-610. doi: 10.1007/s10529-007-9595-z
25. Goodall, E. F., and Morrison, K. E. (2006). Amyotrophic lateral sclerosis (motor neuron disease): proposed mechanisms and pathways to treatment. Expert Rev. Mol. Med. 8, 1-22. doi: 10.1017/S1462399406010854
26. Gordon, P. H., and Meininger, V. (2011). How can we improve clinical trials in amyotrophic lateral sclerosis? Nat. Rev. Neurol. 7, 650-654. doi: 10.1038/nrneurol.2011.147
27. Gordon, M. D., and Nusse, R. (2006). Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J. Biol. Chem. 281, 22429-22433. doi: 10.1074/jbc.R600015200
28. Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., et al. (1994). Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264, 1772-1775. doi: 10.1126/science.8209258
29. Henriquez, J. P., Krull, C. E., and Osses, N. (2011). The Wnt and BMP families of signaling morphogens at the vertebrate neuromuscular junction. Int. J. Mol. Sci. 12, 8924-8946. doi: 10.3390/ijms12128924
30. Henriquez, J. P., and Salinas, P. C. (2012). Dual roles for Wnt signalling during the formation of the vertebrate neuromuscular junction. Acta Physiol. (Oxf.) 204, 128-136. doi: 10.1111/j.1748-1716.2011.02295.x
31. Hirth, F. (2010). Dro sophila melanogaster in the study of human neurodegeneration. CNS Neurol. Disord. Drug Targets 9, 504-523. doi: 10.2174/187152710791556104
32. Hughes, C. S., Postovit, L. M., and Lajoie, G. A. (2010). Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics 10, 1886-1890. doi: 10.1002/pmic.200900758
33. Inestrosa, N. C., and Arenas, E. (2010). Emerging roles of Wnts in the adult nervous system. Nat. Rev. Neurosci. 11, 77-86. doi: 10.1038/nrn2755
34. Itasaki, N., and Hoppler, S. (2010). Crosstalk between Wnt and bone morphogenic protein signaling: a turbulent relationship. Dev. Dyn. 239, 16-33. doi: 10.1002/dvdy.22009
35. Kim, N. G., Xu, C., and Gumbiner, B. M. (2009). Identification of targets of the Wnt pathway destruction complex in addition to beta-catenin. Proc. Natl. Acad. Sci. U.S.A. 106, 5165-5170. doi: 10.1073/pnas.0810185106
36. Kuo, Y. C., and Chung, C. Y. (2012). Chondrogenesis in scaffolds with surface modification of elastin and poly-L-lysine. Colloids Surf. B Biointerfaces 93, 85-91. doi: 10.1016/j.colsurfb.2011.12.011
37. Lagenaur, C., and Lemmon, V. (1987). An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc. Natl. Acad. Sci. U.S.A. 84, 7753-7757. doi: 10.1073/pnas.84.21.7753
38. Lee, K. W., Kim, H. J., Sung, J. J., Park, K. S., and Kim, M. (2002). Defective neurite outgrowth in aphidicolin/cAMP-induced motor neurons expressing mutant Cu/Zn superoxide dismutase. Int. J. Dev. Neurosci. 20, 521-526. doi: 10.1016/S0736-5748(02)00052-7
39. L'Episcopo, F., Serapide, M. F., Tirolo, C., Testa, N., Caniglia, S., Morale, M. C., et al. (2011). A Wnt1 regulated Frizzled-1/beta-Catenin signaling pathway as a candidate regulatory circuit controlling mesencephalic dopaminergic neuron-astrocyte crosstalk: therapeutical relevance for neuron survival and neuroprotection. Mol. Neurodegener. 6, 49. doi: 10.1186/ 1750-1326-6-49
40. Li, X., Guan, Y., Chen, Y., Zhang, C., Shi, C., Zhou, F., et al. (2013). Expression of Wnt5a and its receptor Fzd2 is changed in the spinal cord of adult amyotrophic lateral sclerosis transgenic mice. Int. J. Clin. Exp. Pathol. 6, 1245-1260.
41. Li, B., Xu, W., Luo, C., Gozal, D., and Liu, R. (2003). VEGF-induced activation of the PI3-K/Akt pathway reduces mutant SOD1-mediated motor neuron cell death. Brain Res. Mol. Brain Res. 111, 155-164. doi: 10.1016/S0169-328X(03)00025-1
42. Lopez-Rovira, T., Chalaux, E., Massague, J., Rosa, J. L., and Ventura, F. (2002). Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J. Biol. Chem. 277, 3176-3185. doi: 10.1074/jbc.M106826200
43. Magrane, J., Hervias, I., Henning, M. S., Damiano, M., Kawamata, H., and Manfredi, G. (2009). Mutant SOD1 in neuronal mitochondria causes toxicity and mitochondrial dynamics abnormalities. Hum. Mol. Genet. 18, 4552-4564. doi:10.1093/hmg/ddp421
44. Maier, O., Bohm, J., Dahm, M., Bruck, S., Beyer, C., and Johann, S. (2013). Differentiated NSC-34 motoneuron-like cells as experimental model for cholinergic neurodegeneration. Neurochem. Int. 62, 1029-1038. doi: 10.1016/j.neuint.2013.03.008
45. Marcellini, S., Henriquez, J. P., and Bertin, A. (2012). Control of osteogenesis by the canonical Wnt and BMP pathways in vivo: cooperation and antagonism between the canonical Wnt and BMP pathways as cells differentiate from osteochondroprogenitors to osteoblasts and osteocytes. Bioessays 34, 953-962. doi: 10.1002/bies.201200061
46. Marchetti, B., L'Episcopo, F., Morale, M. C., Tirolo, C., Testa, N., Caniglia, S., et al. (2013). Uncovering novel actors in astrocyte-neuron crosstalk in Parkinson's disease: the Wnt/beta-catenin signaling cascade as the common final pathway for neuroprotection and self-repair. Eur. J. Neurosci. 37, 1550-1563. doi: 10.1111/ejn.12166
47. Matsuura, I., Taniguchi, J., Hata, K., Saeki, N., and Yamashita, T. (2008). BMP inhibition enhances axonal growth and functional recovery after spinal cord injury. J. Neurochem. 105, 1471-1479. doi: 10.1111/j.1471-4159.2008.05251.x
48. Miyazono, K., Maeda, S., and Imamura, T. (2005). BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth. Factor. Rev. 16, 251-263. doi: 10.1016/j.cytogfr.2005.01.009
49. Mourelatos, Z., Hirano, A., Rosenquist, A. C., and Gonatas, N. K. (1994). Fragmentation of the Golgi apparatus of motor neurons in amyotrophic lateral sclerosis (ALS). Clinical studies in ALS of Guam and experimental studies in deafferented neurons and in beta, beta′-iminodipropionitrile axonopathy. Am. J. Pathol. 144, 1288-1300.
50. Nelson, W. J., and Nusse, R. (2004). Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483-1487. doi: 10.1126/science.1094291
51. Nohe, A., Hassel, S., Ehrlich, M., Neubauer, F., Sebald, W., Henis, Y. I., et al. (2002). The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J. Biol. Chem. 277, 5330-5338. doi:10.1074/jbc.M102750200
52. Pasinelli, P., Borchelt, D. R., Houseweart, M. K., Cleveland, D. W., et al. (1998). Caspase-1 is activated in neural cells and tissue with amyotrophic lateral sclerosisassociated mutations in copper-zinc superoxide dismutase. Proc. Natl. Acad. Sci. U.S.A. 95, 15763-15768. doi: 10.1073/pnas.95.26.15763
53. Pasinelli, P., and Brown, R. H. (2006). Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat. Rev. Neurosci. 7, 710-723. doi: 10.1038/nrn1971
54. Pfaff, S. L., Mendelsohn, M., Stewart, C. L., Edlund, T., and Jessell, T. M. (1996). Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309-320. doi: 10.1016/S0092-8674(00)80985-X
55. Purro, S. A., Dickins, E. M., and Salinas, P. C. (2012). The secreted Wnt antagonist Dickkopf-1 is required for amyloid beta-mediated synaptic loss. J. Neurosci. 32, 3492-3498. doi: 10.1523/JNEUROSCI.4562-11.2012
56. Ratnaparkhi, A., Lawless, G. M., Schweizer, F. E., Golshani, P., and Jackson, G. R. (2008). A Drosophila model of ALS: human ALS-associated mutation in VAP33A suggests a dominant negative mechanism. PLoS ONE 3:e2334. doi:10.1371/journal.pone.0002334
57. Robberecht, W., and Philips, T. (2013). The changing scene of amyotrophic lateral sclerosis. Nat. Rev. Neurosci. 14, 248-264. doi: 10.1038/nrn3430
58. Rosen, D. R. (1993). Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 364, 362. doi:10.1038/362059a0
59. Salinas, P. C. (2012). Wnt signaling in the vertebrate central nervous system: from axon guidance to synaptic function. Cold Spring Harb. Perspect. Biol. 4, pii: a008003 doi: 10.1101/cshperspect.a008003
60. Schymick, J. C., Talbot, K., and Traynor, B. J. (2007). Genetics of sporadic amyotrophic lateral sclerosis. Hum. Mol. Genet. 16(Spec No. 2), R233-R242. doi: 10.1093/hmg/ddm215
61. Shi, Y., and Massague, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113, 685-700. doi: 10.1016/S0092-8674(03)00432-X
62. Sieber, C., Kopf, J., Hiepen, C., and Knaus, P. (2009). Recent advances in BMP receptor signaling. Cytokine Growth. Factor. Rev. 20, 343-355. doi: 10.1016/j.cytogfr.2009.10.007
63. Sundaramoorthy, V., Walker, A. K., Yerbury, J., Soo, K. Y., Farg, M. A., Hoang, V., et al. (2013). Extracellular wildtype and mutant SOD1 induces ER-Golgi pathology characteristic of amyotrophic lateral sclerosis in neuronal cells. Cell. Mol. Life Sci. 70, 4181-4195. doi: 10.1007/s00018-013-1385-2
64. Tanabe, Y., William, C., and Jessell, T. M. (1998). Specification of motor neuron identity by the MNR2 homeodomain protein. Cell 95, 67-80. doi: 10.1016/S0092-8674(00)81783-3
65. Turner, B. J., Atkin, J. D., Farg, M. A., Zang, D. W., Rembach, A., Lopes, E. C., et al. (2005). Impaired extracellular secretion of mutant superoxide dismutase 1 associates with neurotoxicity in familial amyotrophic lateral sclerosis. J. Neurosci. 25, 108-117. doi: 10.1523/JNEUROSCI.4253-04.2005
66. van Zundert, B., Izaurieta, P., Fritz, E., and Alvarez, F. J. (2012). Early pathogenesis in the adult-onset neurodegenerative disease amyotrophic lateral sclerosis. J. Cell. Biochem. 113, 3301-3312. doi: 10.1002/jcb.24234
67. Ventre, M., Causa, F., and Netti, P. A. (2012). Determinants of cell-material crosstalk at the interface: towards engineering of cell instructive materials. J. R. Soc. Interface 9, 2017-2032. doi: 10.1098/rsif.2012.0308
68. Vinals, F., Reiriz, J., Ambrosio, S., Bartrons, R., Rosa, J. L., and Ventura, F. (2004). BMP-2 decreases Mash1 stability by increasing Id1 expression. EMBO J. 23, 3527-3537. doi: 10.1038/sj.emboj.7600360
69. Wang, S., Guan, Y., Chen, Y., Li, X., Zhang, C., Yu, L., et al. (2013). Role of Wnt1 and Fzd1 in the spinal cord pathogenesis of amyotrophic lateral sclerosis-transgenic mice. Biotechnol. Lett. 35, 1199-1207. doi: 10.1007/s10529-013-1199-1
70. Wang, Y. L., Wang, D. Z., Nie, X., Lei, D. L., Liu, Y. P., Zhang, Y. J., et al. (2007). The role of bone morphogenetic protein-2 in vivo in regeneration of peripheral nerves. Br. J. Oral Maxillofac. Surg. 45, 197-202. doi: 10.1016/j.bjoms.2006.06.003
71. Wijesekera, L. C., and Leigh, P. N. (2009). Amyotrophic lateral sclerosis. Orphanet. J. Rare Dis. 4, 3. doi: 10.1186/1750-1172-4-3
72. Wood, J. D., Beaujeux, T. P., and Shaw, P. J. (2003). Protein aggregation in motor neurone disorders. Neuropathol. Appl. Neurobiol. 29, 529-545. doi:10.1046/j.0305-1846.2003.00518.x
73. Yao, X. L., Ye, C. H., Liu, Q., Wan, J. B., Zhen, J., Xiang, A. P., et al. (2013). Motoneuron differentiation of induced pluripotent stem cells from SOD1G93A mice. PLoS ONE 8:e64720. doi: 10.1371/journal.pone.0064720
74. Ying, Q. L., Nichols, J., Chambers, I., and Smith, A. (2003). BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292. doi: 10.1016/S0092-8674(03)00847-X
75. Yu, L., Guan, Y., Wu, X., Chen, Y., Liu, Z., Du, H., et al. (2013). Wnt Signaling is Altered by spinal cord neuronal dysfunction in amyotrophic lateral sclerosis transgenic mice. Neurochem. Res. 38, 1904-1913. doi: 10.1007/s11064-013-1096-y
76. Zhang, J., Ito, H., Wate, R., Ohnishi, S., Nakano, S., and Kusaka, H. (2006). Altered distributions of nucleocytoplasmic transport-related proteins in the spinal cord of a mouse model of amyotrophic lateral sclerosis. Acta Neuropathol. 112, 673-680. doi: 10.1007/s00401-006-0130-4