Sensory neurons do not induce motor neuron loss in a human stem cell model of spinal muscular atrophy

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Schwab, Andrew J ^a   Ebert, Allison D ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE TRANSPORTER; CALCIUM;

ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL LINE; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOTONEURON; NERVE CELL MEMBRANE STEADY POTENTIAL; NEURITE; PERIKARYON; PLURIPOTENT STEM CELL; SENSORY NERVE CELL; SPINAL MUSCULAR ATROPHY; COCULTURE; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PATHOPHYSIOLOGY; STEM CELL;

CALCIUM; CELL LINE; CELL SURVIVAL; COCULTURE TECHNIQUES; HUMANS; MOTOR NEURONS; MUSCULAR ATROPHY, SPINAL; NEUROGENESIS; SENSORY RECEPTOR CELLS; STEM CELLS;

EID: 84904700148     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103112     Document Type: Article

References (40)

1. Rochette CF, Gilbert N, Simard LR (2001) SMN gene duplication and the emergence of the SMN2 gene occurred in distinct hominids: SMN2 is unique to Homo sapiens. Hum.Genet. 108: 255-266. (Pubitemid 32293674)
2. Fischer U, Liu Q, Dreyfuss G (1997) The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis. Cell 90: 1023-1029. (Pubitemid 27408516)
3. Liu Q, Fischer U, Wang F, Dreyfuss G (1997) The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell 90: 1013-1021. (Pubitemid 27408515)
4. Pellizzoni L, Yong J, Dreyfuss G (2002) Essential role for the SMN complex in the specificity of snRNP assembly. Science 298: 1775-1779. (Pubitemid 35404118)
5. Lorson CL, Androphy EJ (1998) The domain encoded by exon 2 of the survival motor neuron protein mediates nucleic acid binding. Hum.Mol.Genet. 7: 1269-1275. (Pubitemid 28383060)
6. Lorson CL, Hahnen E, Androphy EJ, Wirth B (1999) A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc.Natl.Acad.Sci.U.S.A 96: 6307-6311. (Pubitemid 29256661)
7. Lorson CL, Strasswimmer J, Yao JM, Baleja JD, Hahnen E, et al. (1998) SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat.Genet. 19: 63-66. (Pubitemid 28242025)
8. Monani UR, Lorson CL, Parsons DW, Prior TW, Androphy EJ, et al. (1999) A single nucleotide difference that alters splicing patterns distinguishes the SMA gene SMN1 from the copy gene SMN2. Hum.Mol.Genet. 8: 1177-1183. (Pubitemid 29328985)
9. Lotti F, Imlach WL, Saieva L, Beck ES, Hao le T, et al. (2012) An SMN-dependent U12 splicing event essential for motor circuit function. Cell 151: 440-454.
10. Gogliotti RG, Quinlan KA, Barlow CB, Heier CR, Heckman CJ, et al. (2012) Motor neuron rescue in spinal muscular atrophy mice demonstrates that sensory-motor defects are a consequence, not a cause, of motor neuron dysfunction. The Journal of neuroscience: the official journal of the Society for Neuroscience 32: 3818-3829.
11. Jablonka S, Karle K, Sandner B, Andreassi C, von Au K, et al. (2006) Distinct and overlapping alterations in motor and sensory neurons in a mouse model of spinal muscular atrophy. Human Molecular Genetics 15: 511-518. (Pubitemid 43159902)
12. Ling KK, Lin MY, Zingg B, Feng Z, Ko CP (2010) Synaptic defects in the spinal and neuromuscular circuitry in a mouse model of spinal muscular atrophy. PLoS One 5: e15457.
13. Martinez TL, Kong L, Wang X, Osborne MA, Crowder ME, et al. (2012) Survival motor neuron protein in motor neurons determines synaptic integrity in spinal muscular atrophy. The Journal of neuroscience: the official journal of the Society for Neuroscience 32: 8703-8715.
14. Mentis GZ, Blivis D, Liu W, Drobac E, Crowder ME, et al. (2011) Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron 69: 453-467.
15. Imlach WL, Beck ES, Choi BJ, Lotti F, Pellizzoni L, et al. (2012) SMN is required for sensory-motor circuit function in Drosophila. Cell 151: 427-439.
16. McGivern JV, Patitucci TN, Nord JA, Barabas ME, Stucky CL, et al. (2013) Spinal muscular atrophy astrocytes exhibit abnormal calcium regulation and reduced growth factor production. Glia 61: 1418-1428.
17. Voigt T, Meyer K, Baum O, Schumperli D (2010) Ultrastructural changes in diaphragm neuromuscular junctions in a severe mouse model for Spinal Muscular Atrophy and their prevention by bifunctional U7 snRNA correcting SMN2 splicing. Neuromuscular disorders: NMD 20: 744-752.
18. Murray LM, Beauvais A, Bhanot K, Kothary R (2012) Defects in neuromuscular junction remodelling in the Smn(2B/-) mouse model of spinal muscular atrophy. Neurobiology of Disease 49C: 57-67.
19. Ebert AD, Yu J, Rose FF Jr, Mattis VB, Lorson CL, et al. (2009) Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457: 277-280.
20. Sareen D, Ebert AD, Heins BM, McGivern JV, Ornelas L, et al. (2012) Inhibition of apoptosis blocks human motor neuron cell death in a stem cell model of spinal muscular atrophy. PLoS One 7: e39113.
21. Anagnostou E, Miller SP, Guiot MC, Karpati G, Simard L, et al. (2005) Type I spinal muscular atrophy can mimic sensory-motor axonal neuropathy. Journal of child neurology 20: 147-150. (Pubitemid 40484856)
22. Omran H, Ketelsen UP, Heinen F, Sauer M, Rudnik-Schoneborn S, et al. (1998) Axonal neuropathy and predominance of type II myofibers in infantile spinal muscular atrophy. Journal of child neurology 13: 327-331. (Pubitemid 28367127)
23. Rudnik-Schoneborn S, Goebel HH, Schlote W, Molaian S, Omran H, et al. (2003) Classical infantile spinal muscular atrophy with SMN deficiency causes sensory neuronopathy. Neurology 60: 983-987. (Pubitemid 36348932)
24. Thirumalai V, Behrend RM, Birineni S, Liu W, Blivis D, et al. (2013) Preservation of VGLUT1 synapses on ventral calbindin-immunoreactive interneurons and normal locomotor function in a mouse model of spinal muscular atrophy. Journal of Neurophysiology 109: 702-710.
25. Park GH, Maeno-Hikichi Y, Awano T, Landmesser LT, Monani UR (2010) Reduced survival of motor neuron (SMN) protein in motor neuronal progenitors functions cell autonomously to cause spinal muscular atrophy in model mice expressing the human centromeric (SMN2) gene. The Journal of neuroscience: the official journal of the Society for Neuroscience 30: 12005-12019.
26. Zhang Z, Pinto AM, Wan L, Wang W, Berg MG, et al. (2013) Dysregulation of synaptogenesis genes antecedes motor neuron pathology in spinal muscular atrophy. Proceedings of the National Academy of Sciences of the United States of America 110: 19348-19353.
27. Hultborn H (2006) Spinal reflexes, mechanisms and concepts: from Eccles to Lundberg and beyond. Progress in Neurobiology 78: 215-232.
28. Leveille F, Papadia S, Fricker M, Bell KFS, Soriano FX, et al. (2010) Suppression of the Intrinsic Apoptosis Pathway by Synaptic Activity. Journal of Neuroscience 30: 2623-2635.
29. Catsicas M, Pequignot Y, Clarke PG (1992) Rapid onset of neuronal death induced by blockade of either axoplasmic transport or action potentials in afferent fibers during brain development. The Journal of neuroscience: the official journal of the Society for Neuroscience 12: 4642-4650.
30. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler J, et al. (1999) Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283: 70-74. (Pubitemid 29044848)
31. Tsai LK, Tsai MS, Ting CH, Wang SH, Li H (2008) Restoring Bcl-x(L) levels benefits a mouse model of spinal muscular atrophy. Neurobiology of Disease 31: 361-367.
32. Tsai MS, Chiu YT, Wang SH, Hsieh-Li HM, Lian WC, et al. (2006) Abolishing Bax-dependent apoptosis shows beneficial effects on spinal muscular atrophy model mice. Molecular therapy: the journal of the American Society of Gene Therapy 13: 1149-1155.
33. Kerr DA, Nery JP, Traystman RJ, Chau BN, Hardwick JM (2000) Survival motor neuron protein modulates neuron-specific apoptosis. Proceedings of the National Academy of Sciences of the United States of America 97: 13312-13317.
34. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872. (Pubitemid 350138099)
35. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, et al. (2009) Human induced pluripotent stem cells free of vector and transgene sequences. Science 324: 797-801.
36. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
37. Chambers SM, Qi Y, Mica Y, Lee G, Zhang XJ, et al. (2012) Combined small-molecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors. Nature Biotechnology 30: 715-720.
38. HD iPSC Consortium (2012) Induced Pluripotent Stem Cells from Patients with Huntington's Disease Show CAG Repeat Expansion-Associated Phenotypes. Cell Stem Cell 11: 264-278.
39. Ebert AD, Shelley BC, Hurley AM, Onorati M, Castiglioni V, et al. (2013) EZ spheres: A stable and expandable culture system for the generation of pre-rosette multipotent stem cells from human ESCs and iPSCs. Stem Cell Research 10: 417-427.
40. Hunter G, Aghamaleky Sarvestany A, Roche SL, Symes RC, Gillingwater TH (2014) SMN-dependent intrinsic defects in Schwann cells in mouse models of spinal muscular atrophy. Human Molecular Genetics 23: 2235-2250.