High yield derivation of enriched glutamatergic neurons from suspension-cultured mouse ESCs for neurotoxicology research

BMC Neuroscience

Volumn 13, Issue 1, 2012, Pages

  Hubbard, Kyle S ^a   Gut, Ian M ^a   Lyman, Megan E ^a   Tuznik, Kaylie M ^a   Mesngon, Mariano T ^b   McNutt, Patrick M ^a  

^a US ARMY MEDICAL RESEARCH INSTITUTE OF CHEMICAL DEFENSE   (United States)

^b MADIGAN ARMY MEDICAL CENTER   (United States)

Author keywords

BoNT; Glutamate; In vitro modeling; LTX; Mouse embryonic stem cells; Neurotoxicity

Indexed keywords

ALPHA LATROTOXIN; BOTULINUM TOXIN; GLUTAMIC ACID;

ANIMAL CELL; ARTICLE; BRAIN FUNCTION; CALCIUM TRANSPORT; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MEMBRANE DEPOLARIZATION; CELL POPULATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; EXCITOTOXICITY; GENE EXPRESSION; GLUTAMATERGIC NERVE CELL; IN VITRO STUDY; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROTOXICOLOGY; NONHUMAN; STEM CELL;

ANIMALS; BOTULINUM TOXINS, TYPE A; CALCIUM; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; GLUTAMIC ACID; MICE; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; NEUROTOXINS; SPIDER VENOMS; TOXICOLOGY;

EID: 84867666644     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-13-127     Document Type: Article

References (45)

1. Eubanks LM, Hixon MS, Jin W, Hong S, Clancy CM, Tepp WH, Baldwin MR, Malizio CJ, Goodnough MC, Barbieri JT, et al. An in vitro and in vivo disconnect uncovered through high-throughput identification of botulinum neurotoxin A antagonists. Proc Natl Acad Sci U S A 2007, 104(8):2602-2607. 10.1073/pnas.0611213104, 1815229, 17293454.
2. Purkiss JR, Friis LM, Doward S, Quinn CP. Clostridium botulinum neurotoxins act with a wide range of potencies on SH-SY5Y human neuroblastoma cells. Neurotoxicology 2001, 22(4):447-453. 10.1016/S0161-813X(01)00042-0, 11577803.
3. Durham HD, Dahrouge S, Cashman NR. Evaluation of the spinal cord neuron X neuroblastoma hybrid cell line NSC-34 as a model for neurotoxicity testing. Neurotoxicology 1993, 14(4):387-395.
4. Clementi E, Raichman M, Meldolesi J. Heterogeneity of NGF-induced differentiation in PC12 cells investigated in a battery of isolated cell clones. Funct Neurol 1993, 8(2):109-113.
5. NIAID Summary of the NIAID expert panel on botulinum neurotoxins therapeutics. NIAID expert panel on botulinum neurotoxins therapeutics 2004, National Institute of Allergy and Infectious Diseases, Bethesda, MD, NIAID.
6. Bain G, Kitchens D, Yao M, Huettner JE, Gottlieb DI. Embryonic stem cells express neuronal properties in vitro. Dev Biol 1995, 168(2):342-357. 10.1006/dbio.1995.1085, 7729574.
7. Gaspard N, Bouschet T, Herpoel A, Naeije G, van den Ameele J, Vanderhaeghen P. Generation of cortical neurons from mouse embryonic stem cells. Nat Protoc 2009, 4(10):1454-1463. 10.1038/nprot.2009.157, 19798080.
8. Jones-Villeneuve EM, McBurney MW, Rogers KA, Kalnins VI. Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J Cell Biol 1982, 94(2):253-262. 10.1083/jcb.94.2.253, 2112882, 7107698.
9. Okabe S, Forsberg-Nilsson K, Spiro AC, Segal M, McKay RD. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech Dev 1996, 59(1):89-102. 10.1016/0925-4773(96)00572-2, 8892235.
10. Stavridis MP, Smith AG. Neural differentiation of mouse embryonic stem cells. Biochem Soc Trans 2003, 31(Pt 1):45-49.
11. Bibel M, Richter J, Schrenk K, Tucker KL, Staiger V, Korte M, Goetz M, Barde YA. Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat Neurosci 2004, 7(9):1003-1009. 10.1038/nn1301, 15332090.
12. Bibel M, Richter J, Lacroix E, Barde YA. Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat Protoc 2007, 2(5):1034-1043. 10.1038/nprot.2007.147, 17546008.
13. Smith AG. Embryo-derived stem cells: of mice and men. Annu Rev Cell Dev Biol 2001, 17:435-462. 10.1146/annurev.cellbio.17.1.435, 11687496.
14. McNutt P, Celver J, Hamilton T, Mesngon M. Embryonic stem cell-derived neurons are a novel, highly sensitive tissue culture platform for botulinum research. Biochem Biophys Res Commun 2011, 405(1):85-90. 10.1016/j.bbrc.2010.12.132, 21215258.
15. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5(7):621-628. 10.1038/nmeth.1226, 18516045.
16. da Huang W, Sherman BT, Tan Q, Collins JR, Alvord WG, Roayaei J, Stephens R, Baseler MW, Lane HC, Lempicki RA. The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol 2007, 8(9):R183. 10.1186/gb-2007-8-9-r183, 2375021, 17784955.
17. Huang da W, Sherman BT, Zheng X, Yang J, Imamichi T, Stephens R, Lempicki RA. Extracting biological meaning from large gene lists with DAVID. Curr Protoc Bioinformatics 2009, Chapter 13:Unit 13 11.
18. Choi DW. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1988, 1(8):623-634. 10.1016/0896-6273(88)90162-6, 2908446.
19. Choi DW, Koh JY, Peters S. Pharmacology of glutamate neurotoxicity in cortical cell culture: attenuation by NMDA antagonists. J Neurosci 1988, 8(1):185-196.
20. Nicholls DG. Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr Mol Med 2004, 4(2):149-177. 10.2174/1566524043479239, 15032711.
21. Zhang Y, Bhavnani BR. Glutamate-induced apoptosis in primary cortical neurons is inhibited by equine estrogens via down-regulation of caspase-3 and prevention of mitochondrial cytochrome c release. BMC Neurosci 2005, 6:13. 10.1186/1471-2202-6-13, 555946, 15730564.
22. Lidwell K, Griffiths R. Possible role for the FosB/JunD AP-1 transcription factor complex in glutamate-mediated excitotoxicity in cultured cerebellar granule cells. J Neurosci Res 2000, 62(3):427-439. 10.1002/1097-4547(20001101)62:3<427::AID-JNR13>3.0.CO;2-O, 11054812.
23. Yu X, Sun L, Luo X, Xu Z, An L. Investigation of the neuronal death mode induced by glutamate treatment in serum-, antioxidant-free primary cultured cortical neurons. Brain Res Dev Brain Res 2003, 145(2):263-268. 10.1016/j.devbrainres.2003.08.008, 14604766.
24. Silva JP, Suckling J, Ushkaryov Y. Penelope's web: using alpha-latrotoxin to untangle the mysteries of exocytosis. J Neurochem 2009, 111(2):275-290. 10.1111/j.1471-4159.2009.06329.x, 3145131, 19682210.
25. Mesngon M, McNutt PM. Alpha-Latrotoxin Rescues SNAP-25 from BoNT/A-Mediated Proteolysis in Embryonic Stem Cell-Derived Neurons. Toxins 2011, 3(4):489-503. 3202834, 22069721.
26. Deak F, Liu X, Khvotchev M, Li G, Kavalali ET, Sugita S, Sudhof TC. Alpha-latrotoxin stimulates a novel pathway of Ca2+-dependent synaptic exocytosis independent of the classical synaptic fusion machinery. J Neurosci 2009, 29(27):8639-8648. 10.1523/JNEUROSCI.0898-09.2009, 2739239, 19587270.
27. Li G, Lee D, Wang L, Khvotchev M, Chiew SK, Arunachalam L, Collins T, Feng ZP, Sugita S. N-terminal insertion and C-terminal ankyrin-like repeats of alpha-latrotoxin are critical for Ca2+-dependent exocytosis. J Neurosci 2005, 25(44):10188-10197. 10.1523/JNEUROSCI.3560-05.2005, 16267226.
28. Simpson LL. Identification of the major steps in botulinum toxin action. Annu Rev Pharmacol Toxicol 2004, 44:167-193. 10.1146/annurev.pharmtox.44.101802.121554, 14744243.
29. Foran PG, Mohammed N, Lisk GO, Nagwaney S, Lawrence GW, Johnson E, Smith L, Aoki KR, Dolly JO. Evaluation of the therapeutic usefulness of botulinum neurotoxin B, C1, E, and F compared with the long lasting type A. Basis for distinct durations of inhibition of exocytosis in central neurons. J Biol Chem 2003, 278(2):1363-1371. 10.1074/jbc.M209821200, 12381720.
30. Keller JE, Neale EA, Oyler G, Adler M. Persistence of botulinum neurotoxin action in cultured spinal cord cells. FEBS Lett 1999, 456(1):137-142. 10.1016/S0014-5793(99)00948-5, 10452545.
31. Mandell JW, Banker GA. Microtubule-associated proteins, phosphorylation gradients, and the establishment of neuronal polarity. Perspect Dev Neurobiol 1996, 4(2-3):125-135.
32. Caceres A, Mautino J, Kosik KS. Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron 1992, 9(4):607-618. 10.1016/0896-6273(92)90025-9, 1389180.
33. Ahmari SE, Buchanan J, Smith SJ. Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 2000, 3(5):445-451. 10.1038/74814, 10769383.
34. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, Garner CC. Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 2001, 29(1):131-143. 10.1016/S0896-6273(01)00185-4, 11182086.
35. Sytnyk V, Leshchyns'ka I, Dityatev A, Schachner M. Trans-Golgi network delivery of synaptic proteins in synaptogenesis. J Cell Sci 2004, 117(Pt 3):381-388.
36. Kraszewski K, Mundigl O, Daniell L, Verderio C, Matteoli M, De Camilli P. Synaptic vesicle dynamics in living cultured hippocampal neurons visualized with CY3-conjugated antibodies directed against the lumenal domain of synaptotagmin. J Neurosci 1995, 15(6):4328-4342.
37. Manev H, Favaron M, Guidotti A, Costa E. Delayed increase of Ca2+ influx elicited by glutamate: role in neuronal death. Mol Pharmacol 1989, 36(1):106-112.
38. Ushkaryov YA, Volynski KE, Ashton AC. The multiple actions of black widow spider toxins and their selective use in neurosecretion studies. Toxicon 2004, 43(5):527-542. 10.1016/j.toxicon.2004.02.008, 15066411.
39. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A 1993, 90(18):8424-8428. 10.1073/pnas.90.18.8424, 47369, 8378314.
40. Adams LD, Choi L, Xian HQ, Yang A, Sauer B, Wei L, Gottlieb DI. Double lox targeting for neural cell transgenesis. Brain Res Mol Brain Res 2003, 110(2):220-233. 10.1016/S0169-328X(02)00651-4, 12591158.
41. Brook FA, Gardner RL. The origin and efficient derivation of embryonic stem cells in the mouse. Proc Natl Acad Sci U S A 1997, 94(11):5709-5712. 10.1073/pnas.94.11.5709, 20843, 9159137.
42. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 2009, 6(12):875-881. 10.1038/nmeth.1398, 2858873, 19898485.
43. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25(14):1754-1760. 10.1093/bioinformatics/btp324, 2705234, 19451168.
44. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinforma 2011, 12:323.
45. Bullard JH, Purdom E, Hansen KD, Dudoit S. Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments. BMC Bioinforma 2010, 11:94.