Defects in motoneuron–astrocyte interactions in spinal muscular atrophy

Journal of Neuroscience

Volumn 36, Issue 8, 2016, Pages 2543-2553

  Zhou, Chunyi ^a   Feng, Zhihua ^a   Ko, Chien Ping ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Astrocytes; Ephrin B2; Motoneurons; Spinal muscular atrophy; Synapses; Synaptic transmission

Indexed keywords

AMPA RECEPTOR ANTAGONIST; EPHRIN A3; EPHRIN A4; EPHRIN B2; EXCITATORY AMINO ACID TRANSPORTER; MESSENGER RNA; NUCLEAR FACTOR; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN S100B; SURVIVAL MOTOR NEURON PROTEIN 1; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR SOX9;

ACTION POTENTIAL AMPLITUDE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CALCIUM SIGNALING; CELL INTERACTION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; EMBRYO; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GENE EXPRESSION REGULATION; IMMUNOCYTOCHEMISTRY; MALE; MOTONEURON; MOUSE; NERVE CELL CULTURE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SPINAL MUSCULAR ATROPHY; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP TECHNIQUE; WHOLE CELL PATCH CLAMP; ANIMAL; CELL CULTURE; CYTOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPINAL CORD; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; FEMALE; MALE; MICE; MICE, TRANSGENIC; MOTOR NEURONS; MUSCULAR ATROPHY, SPINAL; SPINAL CORD;

EID: 84959449603     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3534-15.2016     Document Type: Article

References (60)

1. Allen NJ, Barres BA (2009) Neuroscience: glia-more than just brain glue. Nature 457:675- 677. CrossRef Medline
2. Araque A (2008) Astrocytes process synaptic information. Neuron Glia Biol 4:3-10. CrossRef Medline
3. Ballas N, Lioy DT, Grunseich C, Mandel G (2009) Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat Neurosci 12:311-317. CrossRef Medline
4. Barker AJ, Koch SM, Reed J, Barres BA, Ullian EM (2008) Developmental control of synaptic receptivity. J Neurosci 28:8150-8160. CrossRef Medline
5. Barres BA (2008) The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60:430-440. CrossRef Medline
6. Bezprozvanny I (2009) Calcium signaling and neurodegenerative diseases. Trends Mol Med 15:89 -100. CrossRef Medline
7. Boyer JG, Deguise MO, Murray LM, Yazdani A, De Repentigny Y, Boudreau- Larivière C, Kothary R (2014) Myogenic program dysregulation is contributory to disease pathogenesis in spinal muscular atrophy. Hum Mol Genet 23:4249-4259. CrossRef Medline
8. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28:264 -278. CrossRef Medline
9. Camu W, Henderson CE (1992) Purification of embryonic rat motoneurons by panning on a monoclonal antibody to the low-affinity NGF receptor. J Neurosci Methods 44:59 -70. CrossRef Medline
10. Carmona MA, Murai KK, Wang L, Roberts AJ, Pasquale EB (2009) Glial ephrin-A3 regulates hippocampal dendritic spine morphology and glutamate transport. Proc Natl Acad Sci U S A 106:12524 -12529. CrossRef Medline
11. Christopherson KS, Ullian EM, Stokes CC, Mullowney CE, Hell JW, Agah A, Lawler J, Mosher DF, Bornstein P, Barres BA (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120:421- 433. CrossRef Medline
12. Clarke LE, Barres BA (2013) Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 14:311-321. CrossRef Medline
13. Crawford TO, PardoCA (1996) The neurobiology of childhood spinal muscular atrophy. Neurobiol Dis 3:97-110. CrossRef Medline
14. DiGiorgio FP, Carrasco MA, Siao MC, Maniatis T, EgganK (2007) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cellbased ALS model. Nat Neurosci 10:608-614. CrossRef Medline
15. Du W, Yu W, Huang L, Zhao M, Li X (2012) Ephrin-a4 is involved in retinal neovascularization by regulating the VEGF signaling pathway. Invest Ophthalmol Vis Sci 53:1990 -1998. CrossRef Medline
16. Garcia O, Torres M, Helguera P, Coskun P, Busciglio J (2010) A role for thrombospondin-1 deficits in astrocyte-mediated spine and synaptic pathology in Down's syndrome. PLoS One 5:e14200. CrossRef Medline
17. Gogliotti RG, Quinlan KA, Barlow CB, Heier CR, Heckman CJ, Didonato CJ (2012) Motor neuron rescue in spinal muscular atrophy mice demonstrates that sensory-motor defects are a consequence, not a cause, of motor neuron dysfunction. J Neurosci 32:3818 -3829. CrossRef Medline
18. Graber DJ, Harris BT (2013) Purification and culture of spinal motor neurons from rat embryos. Cold Spring Harb Protoc 2013:319 -326. CrossRef Medline
19. Haidet-Phillips AM, Hester ME, Miranda CJ, Meyer K, Braun L, Frakes A, Song S, Likhite S, Murtha MJ, Foust KD, Rao M, Eagle A, Kammesheidt A, Christensen A, Mendell JR, Burghes AH, Kaspar BK (2011) Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat Biotechnol 29:824-828. CrossRef Medline
20. Hamilton G, Gillingwater TH (2013) Spinal muscular atrophy: going beyond the motor neuron. Trends Mol Med 19:40 -50. CrossRef Medline
21. Haydon PG (2001) GLIA: listening and talking to the synapse. Nat Rev Neurosci 2:185-193. CrossRef Medline
22. Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM (2003) Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 163:1313-1326. CrossRef Medline
23. 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. Hum Mol Genet 23:2235-2250. CrossRef Medline
24. Iascone DM, Henderson CE, Lee JC (2015) Spinal muscular atrophy: from tissue specificity to therapeutic strategies. F1000Prime Rep 7:04. CrossRef Medline
25. Ilieva H, Polymenidou M, ClevelandDW (2009) Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J Cell Biol 187: 761-772. CrossRef Medline
26. Jacobs S, Doering LC (2010) Astrocytes prevent abnormal neuronal development in the fragile X mouse. J Neurosci 30:4508-4514. CrossRef Medline
27. Kawamata H, Ng SK, Diaz N, Burstein S, Morel L, Osgood A, Sider B, Higashimori H, Haydon PG, Manfredi G, Yang Y (2014) Abnormal intracellular calcium signaling and SNARE-dependent exocytosis contributes to SOD1G93A astrocyte-mediated toxicity in amyotrophic lateral sclerosis. J Neurosci 34:2331-2348. CrossRef Medline
28. Kayser MS, McClelland AC, Hughes EG, DalvaMB (2006) Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. J Neurosci 26:12152-12164. CrossRef Medline
29. Környei Z, Szlávik V, Szabó B, Gócza E, Czirók A, Madarász E (2005) Humoral and contact interactions in astroglia/stem cell co-cultures in the course of glia-induced neurogenesis. Glia 49:430-444. CrossRef Medline
30. Lai KO, Ip NY (2009) Synapse development and plasticity: roles of ephrin/ Eph receptor signaling. Curr Opin Neurobiol 19:275-283. CrossRef Medline
31. Le TT, Pham LT, Butchbach ME, Zhang HL, Monani UR, Coovert DD, Gavrilina TO, Xing L, Bassell GJ, Burghes AH (2005) SMNDelta7, the major product of the centromeric survival motor neuron (SMN2) gene, extends survival in mice with spinal muscular atrophy and associates with fulllength SMN. Hum Mol Genet 14:845- 857. CrossRef Medline
32. Lefebvre S, Bürglen L, Reboullet S, Clermont O, Burlet P, Viollet L, Benichou B, Cruaud C, Millasseau P, Zeviani M, et al. (1995) Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80: 155-165. CrossRef Medline
33. 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. CrossRef Medline
34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) Method. Methods 25:402- 408. CrossRef Medline
35. Martinez TL, Kong L, Wang X, Osborne MA, Crowder ME, Van Meerbeke JP, Xu X, Davis C, Wooley J, Goldhamer DJ, Lutz CM, Rich MM, Sumner CJ (2012) Survival motor neuron protein in motor neurons determines synaptic integrity in spinal muscular atrophy. J Neurosci 32:8703- 8715. CrossRef Medline
36. Martinou JC, Martinou I, KatoAC (1992) Cholinergic differentiation factor (CDF/LIF) promotes survival of isolated rat embryonic motoneurons in vitro. Neuron 8:737-744. CrossRef Medline
37. McClelland AC, Sheffler-Collins SI, Kayser MS, Dalva MB (2009) Ephrin-B1 and ephrin-B2 mediate EphB-dependent presynaptic development via syntenin-1. Proc Natl Acad Sci U S A 106:20487-20492. CrossRef Medline
38. McGivern JV, Patitucci TN, Nord JA, Barabas ME, Stucky CL, Ebert AD (2013) Spinal muscular atrophy astrocytes exhibit abnormal calcium regulation and reduced growth factor production. Glia 61:1418 -1428. CrossRef Medline
39. McWhorter ML, Monani UR, Burghes AH, 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. CrossRef Medline
40. Mentis GZ, Blivis D, Liu W, Drobac E, Crowder ME, Kong L, Alvarez FJ, Sumner CJ, O'Donovan MJ (2011) Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron 69:453- 467. CrossRef Medline
41. Molofsky AV, Krenick R, Ullian E, Tsai HH, Deneen B, Richardson WD, Barres BA, Rowitch DH (2012) Astrocytes and disease: a neurodevelopmental perspective. Genes Dev 26:891-907. CrossRef Medline
42. Murai KK, Nguyen LN, Irie F, Yamaguchi Y, Pasquale EB (2003) Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat Neurosci 6:153-160. CrossRef Medline
43. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10:615- 622. CrossRef Medline
44. Nicole S, Desforges B, Millet G, Lesbordes J, Cifuentes-Diaz C, Vertes D, Cao ML, De Backer F, Languille L, Roblot N, Joshi V, Gillis JM, Melki J (2003) Intact satellite cells lead to remarkable protection against Smn gene defect in differentiated skeletal muscle. J Cell Biol 161:571-582. CrossRef Medline
45. O'Leary DD, McLaughlin T (2005) Mechanisms of retinotopic map development: Ephs, ephrins, and spontaneous correlated retinal activity. Prog Brain Res 147:43- 65. CrossRef Medline
46. Ota Y, Zanetti AT, Hallock RM (2013) The role of astrocytes in the regulation of synaptic plasticity and memory formation. Neural Plast 2013: 185463. CrossRef Medline
47. Paez-Colasante X, Seaberg B, Martinez TL, Kong L, Sumner CJ, Rimer M (2013) Improvement of neuromuscular synaptic phenotypes without enhanced survival and motor function in severe spinal muscular atrophy mice selectively rescued in motor neurons. PLoS One 8:e75866. CrossRef Medline
48. 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. J Neurosci 30:12005-12019. CrossRef Medline
49. Perea G, Araque A (2005) Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 25:2192-2203. CrossRef Medline
50. Pickles JO (2003) Expression of Ephs and ephrins in developing mouse inner ear. Hear Res 178:44 -51. CrossRef Medline
51. Rindt H, Feng Z, Mazzasette C, Glascock JJ, Valdivia D, Pyles N, Crawford TO, Swoboda KJ, Patitucci TN, Ebert AD, Sumner CJ, Ko CP, Lorson CL (2015) Astrocytes influence the severity of spinal muscular atrophy. Hum Mol Genet 24:4094-4102. CrossRef Medline
52. Rossoll W, Jablonka S, Andreassi C, Kröning AK, Karle K, Monani UR, Sendtner M (2003) Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J Cell Biol 163:801- 812. CrossRef Medline
53. 2+ homeostasis in nerve terminals of severe spinal muscular atrophy mice. J Neurosci 30:849-857. CrossRef Medline
54. Shababi M, Lorson CL, Rudnik-Schöneborn SS (2014) Spinal muscular atrophy: a motor neuron disorder or a multi-organ disease? J Anat 224:15- 28. CrossRef Medline
55. Tisdale S, Pellizzoni L (2015) Disease mechanisms and therapeutic approaches in spinal muscular atrophy. J Neurosci 35:8691- 8700. CrossRef Medline
56. Ullian EM, Sapperstein SK, Christopherson KS, Barres BA (2001) Control of synapse number by glia. Science 291:657- 661. CrossRef Medline
57. Ullian EM, Harris BT, Wu A, Chan JR, Barres BA (2004) Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture. Mol Cell Neurosci 25:241-251. CrossRef Medline
58. Verkhratsky A (2006) Glial calcium signaling in physiology and pathophysiology. Acta Pharmacol Sin 27:773-780. CrossRef Medline
59. Verkhratsky A, Steinhäuser C (2000) Ion channels in glial cells. Brain Res Brain Res Rev 32:380-412. CrossRef Medline
60. Zhang HM, Robinson N, Gómez-Curet I, Wang W, Harrington MA (2009) Neuronal and network activity in networks of cultured spinal motor neurons. Neuroreport 20:849-854. CrossRef Medline