High content screening of cortical neurons identifies novel regulators of axon growth

Molecular and Cellular Neuroscience

Volumn 44, Issue 1, 2010, Pages 43-54

  Blackmore, Murray G ^a   Moore, Darcie L ^b,c   Smith, Robin P ^a,b   Goldberg, Jeffrey L ^b,c   Bixby, John L ^a,b   Lemmon, Vance P ^a,b  

^a UNIVERSITY OF MIAMI   (United States)

^b UNIVERSITY OF MIAMI   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Axon regeneration; Corticospinal tract; Development; Doublecortin; High content analysis; Kruppel like transcription factor

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CHIMERIN; DOUBLECORTIN; FRUCTOSE BISPHOSPHATE ALDOLASE; GROWTH INHIBITOR; GUANOSINE TRIPHOSPHATASE; KRUPPEL LIKE FACTOR 6; ORGANIC CATION TRANSPORTER 3;

ANALYTIC METHOD; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOANALYSIS; BRAIN NERVE CELL; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETIC CODE; GROWTH REGULATION; MICROTUBULE; MOLECULAR DYNAMICS; NERVE FIBER GROWTH; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; UPREGULATION;

ANIMALS; BIOLOGICAL ASSAY; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL CORTEX; FRUCTOSE-BISPHOSPHATE ALDOLASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH CONES; GROWTH INHIBITORS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICROTUBULE-ASSOCIATED PROTEINS; NERVE GROWTH FACTORS; NERVE REGENERATION; NEURITES; NEUROGENESIS; NEURONAL PLASTICITY; NEUROPEPTIDES; PROTO-ONCOGENE PROTEINS; PYRAMIDAL TRACTS; RATS;

EID: 77950339970     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.02.002     Document Type: Article

References (58)

1. Arlotta P., Molyneaux B.J., Chen J., Inoue J., Kominami R., Macklis J.D. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 2005, 45:207-221.
2. Barres B.A., Silverstein B.E., Corey D.P., Chun L.L. Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron 1988, 1:791-803.
3. Benson M.D., Romero M.I., Lush M.E., Lu Q.R., Henkemeyer M., Parada L.F. Ephrin-B3 is a myelin-based inhibitor of neurite outgrowth. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10694-10699.
4. Bielas S.L., Serneo F.F., Chechlacz M., Deerinck T.J., Perkins G.A., Allen P.B., Ellisman M.H., Gleeson J.G. Spinophilin facilitates dephosphorylation of doublecortin by PP1 to mediate microtubule bundling at the axonal wrist. Cell 2007, 129:579-591.
5. Blackmore M., Letourneau P.C. Changes within maturing neurons limit axonal regeneration in the developing spinal cord. J. Neurobiol. 2006, 66:348-360.
6. Bregman B.S., Kunkel-Bagden E., McAtee M., O'Neill A. Extension of the critical period for developmental plasticity of the corticospinal pathway. J. Comp. Neurol. 1989, 282:355-370.
7. Brown M., Jacobs T., Eickholt B., Ferrari G., Teo M., Monfries C., Qi R.Z., Leung T., Lim L., Hall C. Alpha2-chimaerin, cyclin-dependent Kinase 5/p35, and its target collapsin response mediator protein-2 are essential components in semaphorin 3A-induced growth-cone collapse. J. Neurosci. 2004, 24:8994-9004.
8. Buchser W.J., Pardinas J.R., Shi Y., Bixby J.L., Lemmon V.P. 96-well electroporation method for transfection of mammalian central neurons. Biotechniques 2006, 41:619-624.
9. Canete-Soler R., Reddy K.S., Tolan D.R., Zhai J. Aldolases a and C are ribonucleolytic components of a neuronal complex that regulates the stability of the light-neurofilament mRNA. J. Neurosci. 2005, 25:4353-4364.
10. Case L.C., Tessier-Lavigne M. Regeneration of the adult central nervous system. Curr. Biol. 2005, 15:R749-R753.
11. Chen D.F., Jhaveri S., Schneider G.E. Intrinsic changes in developing retinal neurons result in regenerative failure of their axons. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:7287-7291.
12. Cohen D., Segal M., Reiner O. Doublecortin supports the development of dendritic arbors in primary hippocampal neurons. Dev. Neurosci. 2008, 30:187-199.
13. De Hoop M.J., Meyn L., Dotti C.G. Culturing hippocampal neurons and astrocytes from fetal rodent brain 1998, Academic, San Diego.
14. Deuel T.A., Liu J.S., Corbo J.C., Yoo S.Y., Rorke-Adams L.B., Walsh C.A. Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 2006, 49:41-53.
15. Dusart I., Airaksinen M.S., Sotelo C. Purkinje cell survival and axonal regeneration are age dependent: an in vitro study. J. Neurosci. 1997, 17:3710-3726.
16. Erturk A., Hellal F., Enes J., Bradke F. Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J. Neurosci. 2007, 27:9169-9180.
17. Fink C.C., Bayer K.U., Myers J.W., Ferrell J.E., Schulman H., Meyer T. Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII. Neuron 2003, 39:283-297.
18. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., Denoulet P., Chelly J. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 1999, 23:247-256.
19. Gdalyahu A., Ghosh I., Levy T., Sapir T., Sapoznik S., Fishler Y., Azoulai D., Reiner O. DCX, a new mediator of the JNK pathway. Embo J. 2004, 23:823-832.
20. Gerhard D.S., Wagner L., Feingold E.A., Shenmen C.M., Grouse L.H., Schuler G., Klein S.L., Old S., Rasooly R., Good P., Guyer M., Peck A.M., Derge J.G., Lipman D., Collins F.S., Jang W., Sherry S., Feolo M., Misquitta L., Lee E., Rotmistrovsky K., Greenhut S.F., Schaefer C.F., Buetow K., Bonner T.I., Haussler D., Kent J., Kiekhaus M., Furey T., Brent M., Prange C., Schreiber K., Shapiro N., Bhat N.K., Hopkins R.F., Hsie F., Driscoll T., Soares M.B., Casavant T.L., Scheetz T.E., Brown-stein M.J., Usdin T.B., Toshiyuki S., Carninci P., Piao Y., Dudekula D.B., Ko M.S., Kawakami K., Suzuki Y., Sugano S., Gruber C.E., Smith M.R., Simmons B., Moore T., Waterman R., Johnson S.L., Ruan Y., Wei C.L., Mathavan S., Gunaratne P.H., Wu J., Garcia A.M., Hulyk S.W., Fuh E., Yuan Y., Sneed A., Kowis C., Hodgson A., Muzny D.M., McPherson J., Gibbs R.A., Fahey J., Helton E., Ketteman M., Madan A., Rodrigues S., Sanchez A., Whiting M., Madari A., Young A.C., Wetherby K.D., Granite S.J., Kwong P.N., Brinkley C.P., Pearson R.L., Bouffard G.G., Blakesly R.W., Green E.D., Dickson M.C., Rodriguez A.C., Grimwood J., Schmutz J., Myers R.M., Butterfield Y.S., Griffith M., Griffith O.L., Krzywinski M.I., Liao N., Morin R., Palmquist D., et al. The status, quality, and expansion of the NIH full-length cDNA project: the Mammalian Gene Collection (MGC). Genome Res 2004, 14:2121-2127.
21. Gleeson J.G., Lin P.T., Flanagan L.A., Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999, 23:257-271.
22. Goldberg J.L., Klassen M.P., Hua Y., Barres B.A. Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 2002, 296:1860-1864.
23. Hafidi A., Grumet M., Sanes D.H. In vitro analysis of mechanisms underlying age-dependent failure of axon regeneration. J. Comp. Neurol. 2004, 470:80-92.
24. Hasan S.J., Keirstead H.S., Muir G.D., Steeves J.D. Axonal regeneration contributes to repair of injured brainstem-spinal neurons in embryonic chick. J. Neurosci. 1993, 13:492-507.
25. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., Speed T.P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
26. Kawano H., Li H.P., Sango K., Kawamura K., Raisman G. Inhibition of collagen synthesis overrides the age-related failure of regeneration of nigrostriatal dopaminergic axons. J. Neurosci. Res. 2005, 80:191-202.
27. Kawauchi T., Hoshino M. Molecular pathways regulating cytoskeletal organization and morphological changes in migrating neurons. Dev. Neurosci. 2008, 30:36-46.
28. Koizumi H., Tanaka T., Gleeson J.G. Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 2006, 49:55-66.
29. Lee E.J., Kim I.B., Lee E., Kwon S.O., Oh S.J., Chun M.H. Differential expression and cellular localization of doublecortin in the developing rat retina. Eur. J. Neurosci. 2003, 17:1542-1548.
30. Loh S.H., Francescut L., Lingor P., Bahr M., Nicotera P. Identification of new kinase clusters required for neurite outgrowth and retraction by a loss-of-function RNA interference screen. Cell Death Differ. 2008, 15:283-298.
31. Meyer-Franke A., Kaplan M.R., Pfrieger F.W., Barres B.A. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 1995, 15:805-819.
32. Moore D.L., Blackmore M.G., Hu Y., Kaestner K.H., Bixby J.L., Lemmon V.P., Goldberg J.L. KLF family members regulate intrinsic axon regeneration ability. Science 2009, 326:298-301.
33. Niclou S.P., Ehlert E.M., Verhaagen J. Chemorepellent axon guidance molecules in spinal cord injury. J. Neurotrauma 2006, 23:409-421.
34. Nothias F., Boyne L., Murray M., Tessler A., Fischer I. The expression and distribution of tau proteins and messenger RNA in rat dorsal root ganglion neurons during development and regeneration. Neuroscience 1995, 66:707-719.
35. Pak C.W., Flynn K.C., Bamburg J.R. Actin-binding proteins take the reins in growth cones. Nat. Rev. Neurosci. 2008, 9:136-147.
36. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
37. Sahin M., Greer P.L., Lin M.Z., Poucher H., Eberhart J., Schmidt S., Wright T.M., Shamah S.M., O'Connell S., Cowan C.W., Hu L., Goldberg J.L., Debant A., Corfas G., Krull C.E., Greenberg M.E. Eph-dependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse. Neuron 2005, 46:191-204.
38. Saunders N.R., Kitchener P., Knott G.W., Nicholls J.G., Potter A., Smith T.J. Development of walking, swimming and neuronal connections after complete spinal cord transection in the neonatal opossum, Monodelphis domestica. J. Neurosci. 1998, 18:339-355.
39. Schaar B.T., Kinoshita K., McConnell S.K. Doublecortin microtubule affinity is regulated by a balance of kinase and phosphatase activity at the leading edge of migrating neurons. Neuron 2004, 41:203-213.
40. Senut M.C., Tuszynski M.H., Raymon H.K., Suhr S.T., Liou N.H., Jones K.R., Reichardt L.F., Gage F.H. Regional differences in responsiveness of adult CNS axons to grafts of cells expressing human neurotrophin 3. Exp. Neurol. 1995, 135:36-55.
41. Sepp K.J., Hong P., Lizarraga S.B., Liu J.S., Mejia L.A., Walsh C.A., Perrimon N. Identification of neural outgrowth genes using genome-wide RNAi. PLoS Genet. 2008, 4:e1000111.
42. Shamah S.M., Lin M.Z., Goldberg J.L., Estrach S., Sahin M., Hu L., Bazalakova M., Neve R.L., Corfas G., Debant A., Greenberg M.E. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 2001, 105:233-244.
43. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N., Palmer A.E., Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 2004, 22:1567-1572.
44. Shi L., Fu W.Y., Hung K.W., Porchetta C., Hall C., Fu A.K., Ip N.Y. Alpha2-chimaerin interacts with EphA4 and regulates EphA4-dependent growth cone collapse. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:16347-16352.
45. Shmueli A., Gdalyahu A., Sapoznik S., Sapir T., Tsukada M., Reiner O. Site-specific dephosphorylation of doublecortin (DCX) by protein phosphatase 1 (PP1). Mol. Cell. Neurosci. 2006, 32:15-26.
46. Sivasankaran R., Pei J., Wang K.C., Zhang Y.P., Shields C.B., Xu X.M., He Z. PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat. Neurosci. 2004, 7:261-268.
47. So K.F., Schneider G.E., Ayres S. Lesions of the brachium of the superior colliculus in neonate hamsters: correlation of anatomy with behavior. Exp. Neurol. 1981, 72:379-400.
48. Stefanizzi I., Canete-Soler R. Coregulation of light neurofilament mRNA by poly(A)-binding protein and aldolase C: implications for neurodegeneration. Brain Res. 2007, 1139:15-28.
49. Tanaka T., Serneo F.F., Tseng H.C., Kulkarni A.B., Tsai L.H., Gleeson J.G. Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 2004, 41:215-227.
50. Tint I., Jean D., Baas P.W., Black M.M. Doublecortin associates with microtubules preferentially in regions of the axon displaying actin-rich protrusive structures. J. Neurosci. 2009, 29:10995-11010.
51. Tsukada M., Prokscha A., Oldekamp J., Eichele G. Identification of neurabin II as a novel doublecortin interacting protein. Mech. Dev. 2003, 120:1033-1043.
52. Tsukada M., Prokscha A., Ungewickell E., Eichele G. Doublecortin association with actin filaments is regulated by neurabin II. J. Biol. Chem. 2005, 280:11361-11368.
53. Vreugdenhil E., Kolk S.M., Boekhoorn K., Fitzsimons C.P., Schaaf M., Schouten T., Sarabdjitsingh A., Sibug R., Lucassen P.J. Doublecortin-like, a microtubule-associated protein expressed in radial glia, is crucial for neuronal precursor division and radial process stability. Eur. J. Neurosci. 2007, 25:635-648.
54. Wayman G.A., Kaech S., Grant W.F., Davare M., Impey S., Tokumitsu H., Nozaki N., Banker G., Soderling T.R. Regulation of axonal extension and growth cone motility by calmodulin-dependent protein kinase I. J. Neurosci. 2004, 24:3786-3794.
55. Wayman G.A., Lee Y.S., Tokumitsu H., Silva A., Soderling T.R. Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 2008, 59:914-931.
56. Yamada S., Uchimura E., Ueda T., Nomura T., Fujita S., Matsumoto K., Funeriu D.P., Miyake M., Miyake J. Identification of twinfilin-2 as a factor involved in neurite outgrowth by RNAi-based screen. Biochem. Biophys. Res. Commun. 2007, 363:926-930.
57. Yiu G., He Z. Glial inhibition of CNS axon regeneration. Nat. Rev. Neurosci. 2006, 7:617-627.
58. Zhou F.Q., Snider W.D. Intracellular control of developmental and regenerative axon growth. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:1575-1592.