Three Dimensional Neuronal Cell Cultures More Accurately Model Voltage Gated Calcium Channel Functionality in Freshly Dissected Nerve Tissue

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Lai, Yinzhi ^a   Cheng, Ke ^a   Kisaalita, William ^a  

^a University of Georgia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; MESSENGER RNA; TRANSCRIPTASE; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CALCIUM CELL LEVEL; CELL STRUCTURE; CONTROLLED STUDY; CULTURE TECHNIQUE; GENE EXPRESSION; INTERMETHOD COMPARISON; LIPID RAFT; MEMBRANE STRUCTURE; MOUSE; NERVE CELL CULTURE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; THREE DIMENSIONAL CELL CULTURE;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CAVEOLAE; CAVEOLIN 1; CELL CULTURE TECHNIQUES; COATED MATERIALS, BIOCOMPATIBLE; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION; ION CHANNEL GATING; LACTIC ACID; MICE; MOLECULAR IMAGING; POLYMERS; POLYSTYRENES; SUPERIOR CERVICAL GANGLION; TISSUE SCAFFOLDS;

MUS;

EID: 84866694776     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045074     Document Type: Article

References (69)

1. Mueller-Klieser W, (1997) Three-dimensional cell cultures: from molecular mechanisms to clinical applications. Am J Physiol 273: C1109-1123.
2. Weaver VM, Petersen OW, Wang F, Larabell CA, Briand P, et al. (1997) Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 137: 231-245.
3. Abbott A, (2003) Cell culture: biology's new dimension. Nature 424: 870-872.
4. Jessup JM, Goodwin TJ, Spaulding G, (1993) Prospects for use of microgravity-based bioreactors to study three-dimensional host-tumor interactions in human neoplasia. J Cell Biochem 51: 290-300.
5. Lewis ML, Moriarity DM, Campbell PS, (1993) Use of microgravity bioreactors for development of an in vitro rat salivary gland cell culture model. J Cell Biochem 51: 265-273.
6. Desai A, Kisaalita WS, Keith C, Wu ZZ, (2006) Human neuroblastoma (SH-SY5Y) cell culture and differentiation in 3-D collagen hydrogels for cell-based biosensing. Biosens Bioelectron 21: 1483-1492.
7. Mao C, Kisaalita WS, (2004) Characterization of 3-D collagen hydrogels for functional cell-based biosensing. Biosens Bioelectron 19: 1075-1088.
8. O'Connor SM, Andreadis JD, Shaffer KM, Ma W, Pancrazio JJ, et al. (2000) Immobilization of neural cells in three-dimensional matrices for biosensor applications. Biosens Bioelectron 14: 871-881.
9. Albrecht DR, Underhill GH, Wassermann TB, Sah RL, Bhatia SN, (2006) Probing the role of multicellular organization in three-dimensional microenvironments. Nat Methods 3: 369-375.
10. Freed LE, (1994) Biodegradable polymer scaffolds for tissue engineering. Nature Biotechnology 12: 689-693.
11. Mikos AG, Sarakinos G, Leite SM, Vacanti JP, Langer R, (1993) Laminated three-dimensional biodegradable foams for use in tissue engineering. Biomaterials 14: 323-330.
12. Zhang S, (2004) Beyond the Petri dish. Nat Biotechnol 22: 151-152.
13. Powers MJ, Domansky K, Kaazempur-Mofrad MR, Kalezi A, Capitano A, et al. (2002) A microfabricated array bioreactor for perfused 3D liver culture. Biotechnol Bioeng 78: 257-269.
14. Freyman TM, Yannas IV, Gibson LJ, (2001) Cellular materials as porous scaffolds for tissue engineering. Progr Mater Sci 46: 273-282.
15. Cheng K, Lai Y, Kisaalita WS, (2008) Three-dimensional polymer scaffolds for high throughput cell-based assay systems. Biomaterials 29: 2802-2812.
16. Wang L, Kisaalita WS, (2010) Characterization of micropatterned nanofibrous scaffolds for neural network activity readout for high-throughput screening. J Biomed Mater Res B Appl Biomater 94: 238-249.
17. Kisaalita WS (2009) 3-D Cell-Based Biosensors in Drug Discovery Programs: Taylor and Francis, 2009. 386 p.
18. Cosford ND, Meinke PT, Stauderman KA, Hess SD, (2002) Recent advances in the modulation of voltage-gated ion channels for the treatment of epilepsy. Curr Drug Targets CNS Neurol Disord 1: 81-104.
19. Triggle DJ, Gopalakrishnan M, Rampe D, Zheng W (2006) Voltage-Gated Ion Channels as Drug Targets; Mannhold R, Kubinyi H, Folkers G, editors: Wiley-VCH, 2006. 479 p.
20. Nam YS, Yoon JJ, Park TG, (2000) A novel fabrication method of macroporous biodegradable polymer scaffolds using gas foaming salt as a porogen additive. J Biomed Mater Res 53: 1-7.
21. Mains RE, Patterson PH, (1973) Primary cultures of dissociated sympathetic neurons. I. Establishment of long-term growth in culture and studies of differentiated properties. J Cell Biol 59: 329-345.
22. Belletti S, Orlandini G, Vettori MV, Mutti A, Uggeri J, et al. (2002) Time course assessment of methylmercury effects on C6 glioma cells: submicromolar concentrations induce oxidative DNA damage and apoptosis. J Neurosci Res 70: 703-711.
23. Cheng K, Lai Y, Kisaalita WS, (2008) Three-dimensional polymer scaffolds for high throughput cell-based assay systems. Biomaterials 29: 2802-2812.
24. Wu ZZ, Zhao Y, Kisaalita WS, (2006) Interfacing SH-SY5Y human neuroblastoma cells with SU-8 microstructures. Colloids Surf B Biointerfaces 52: 14-21.
25. Wu ZZ, Zhao YP, Kisaalita WS, (2006) A packed Cytodex microbead array for three-dimensional cell-based biosensing. Biosens Bioelectron 22: 685-693.
26. Martinez-Pinna J, Lamas JA, Gallego R, (2002) Calcium current components in intact and dissociated adult mouse sympathetic neurons. Brain Res 951: 227-236.
27. Cukierman E, Pankov R, Stevens DR, Yamada KM, (2001) Taking cell-matrix adhesions to the third dimension. Science 294: 1708-1712.
28. Saino T, Satoh Y, (2004) Application of real-time confocal laser scanning microscopy to observe living cells in tissue specimens. J Electron Microsc (Tokyo) 53: 49-56.
29. Dolphin AC, (2006) A short history of voltage-gated calcium channels. Br J Pharmacol 147Suppl 1: S56-62.
30. Yamakage M, Namiki A, (2002) Calcium channels-basic aspects of their structure, function and gene encoding; anesthetic action on the channels-a review. Can J Anaesth 49: 151-164.
31. Dolphin AC, (1999) L-type calcium channel modulation. Adv Second Messenger Phosphoprotein Res 33: 153-177.
32. Benitah JP, Alvarez JL, Gomez AM, (2010) L-type Ca(2+) current in ventricular cardiomyocytes. J Mol Cell Cardiol 48: 26-36.
33. Lipscombe D, Helton TD, Xu W, (2004) L-type calcium channels: the low down. J Neurophysiol 92: 2633-2641.
34. Ertel E, Godfraind T, (2004) Calcium channel blockers and calcium channels. In: Calcium Channel Blockers: Birkhäuser Godfraind T, editor. 2004: P26-28.
35. Meier K, Knepel W, Schofl C, (1988) Potassium depolarization elevates cytosolic free calcium concentration in rat anterior pituitary cells through 1,4-dihydropyridine-sensitive, omega-conotoxin-insensitive calcium channels. Endocrinology 122: 2764-2770.
36. Joshi DC, Singh M, Krishnamurthy K, Joshi PG, Joshi NB, (2011) AMPA induced Ca(2+) influx in motor neurons occurs through voltage gated Ca(2+) channel and Ca(2+) permeable AMPA receptor. Neurochem Int 59(6): 913-921.
37. Shitaka Y, Matsuki N, Saito H, Katsuki H, (1996) Basic fibroblast growth factor increases functional L-type Ca2+ channels in fetal rat hippocampal neurons: implications for neurite morphogenesis in vitro. J Neurosci 16: 6476-6489.
38. Lohn M, Furstenau M, Sagach V, Elger M, Schulze W, et al. (2000) Ignition of calcium sparks in arterial and cardiac muscle through caveolae. Circ Res 87: 1034-1039.
39. O'Connell KM, Martens JR, Tamkun MM, (2004) Localization of ion channels to lipid Raft domains within the cardiovascular system. Trends Cardiovasc Med 14: 37-42.
40. Berridge MJ, (2006) Calcium microdomains: organization and function. Cell Calcium 40: 405-412.
41. Taverna E, Saba E, Rowe J, Francolini M, Clementi F, et al. (2004) Role of lipid microdomains in P/Q-type calcium channel (Cav2.1) clustering and function in presynaptic membranes. J Biol Chem 279: 5127-5134.
42. Maguy A, Hebert TE, Nattel S, (2006) Involvement of lipid rafts and caveolae in cardiac ion channel function. Cardiovasc Res 69: 798-807.
43. Calder PC, Yaqoob P, (2007) Lipid rafts-composition, characterization, and controversies. J Nutr 137: 545-547.
44. Tsui-Pierchala BA, Encinas M, Milbrandt J, Johnson EM Jr, (2002) Lipid rafts in neuronal signaling and function. Trends Neurosci 25: 412-417.
45. Leitinger B, Hogg N, (2002) The involvement of lipid rafts in the regulation of integrin function. J Cell Sci 115: 963-972.
46. Pani B, Singh BB, (2009) Lipid rafts/caveolae as microdomains of calcium signaling. Cell Calcium 45: 625-633.
47. Kiselyov K, Wang X, Shin DM, Zang W, Muallem S, (2006) Calcium signaling complexes in microdomains of polarized secretory cells. Cell Calcium 40: 451-459.
48. Jacob SN, Choe CU, Uhlen P, DeGray B, Yeckel MF, et al. (2005) Signaling microdomains regulate inositol 1,4,5-trisphosphate-mediated intracellular calcium transients in cultured neurons. J Neurosci 25: 2853-2864.
49. Blackstone C, Sheng M, (2002) Postsynaptic calcium signaling microdomains in neurons. Front Biosci 7: d872-885.
50. Blackstone C, Sheng M, (1999) Protein targeting and calcium signaling microdomains in neuronal cells. Cell Calcium 26: 181-192.
51. Liu P, Rudick M, Anderson RG, (2002) Multiple functions of caveolin-1. J Biol Chem 277: 41295-41298.
52. Volonte D, Galbiati F, Lisanti MP, (1999) Visualization of caveolin-1, a caveolar marker protein, in living cells using green fluorescent protein (GFP) chimeras. The subcellular distribution of caveolin-1 is modulated by cell-cell contact. FEBS Lett 445: 431-439.
53. Dunn GA, Heath JP, (1976) A new hypothesis of contact guidance in tissue cells. Exp Cell Res 101: 1-14.
54. Kunz-Schughart LA, Kreutz M, Knuechel R, (1998) Multicellular spheroids: a three-dimensional in vitro culture system to study tumor biology. Int J Exp Pathol 79: 1-23.
55. Wang SS, Good TA, (2001) Effect of culture in a rotating wall bioreactor on the physiology of differentiated neuron-like PC12 and SH-SY5Y cells. J Cell Biochem 83: 574-584.
56. Webb K, Li W, Hitchcock RW, Smeal RM, Gray SD, et al. (2003) Comparison of human fibroblast ECM-related gene expression on elastic three-dimensional substrates relative to two-dimensional films of the same material. Biomaterials 24: 4681-4690.
57. Mochida S, Westenbroek RE, Yokoyama CT, Itoh K, Catterall WA, (2003) Subtype-selective reconstitution of synaptic transmission in sympathetic ganglion neurons by expression of exogenous calcium channels. Proc Natl Acad Sci USA100: 2813-2818.
58. Regan LJ, Sah DWY, Bean BP, (1991) Ca2+ channels in rat central and peripheral neurons - high-threshold current resistant to dihydropyridine blockers and omega-conotoxin. Neuron 6: 269-280.
59. Mintz IM, Adams ME, Bean BP, (1991) P-type calcium channels in rat central and peripheral neurons. Neuron 9: 85-95.
60. Catterall WA, (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3(8): a003947.
61. Fabiato A, (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245(1): C1-14.
62. Kim S, Yun HM, Baik JH, Chung KC, Nah SY, et al. (2007) Functional interaction of neuronal Cav1.3 L-type calcium channel with ryanodine receptor type 2 in the rat hippocampus. J Biol Chem 282(45): 32877-89.
63. Hell JW, Westenbroek RE, Warner C, Ahlijanian MK, Prystay W,et al. 1993) Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits. J Cell Biol 123(4): 949-62.
64. Yang L, Wang Z, Wang B, Justice NJ, Zheng H, (2009) Amyloid precursor protein regulates Cav1.2 L-type calcium channel levels and function to influence GABAergic short-term plasticity. J Neurosci 29(50): 15660-8.
65. Cheng ZJ, Singh RD, Marks DL, Pagano RE, (2006) Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids. Mol Membr Biol 23: 101-110.
66. Shu L, Lee L, Chang Y, Holzman LB, Edwards CA, et al. (2000) Caveolar structure and protein sorting are maintained in NIH 3T3 cells independent of glycosphingolipid depletion. Arch Biochem Biophys 373: 83-90.
67. Zhang JH, Chung TD, Oldenburg KR, (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J Biomol Screen 4: 67-73.
68. Lai Y, Kisaalita W, (2012) Performance evaluation of 3D polystyrene 96-well plates with human stem cells and the calcium assay. Journal Lab Autom 17(4): 284-292.
69. Denyer J, Worley J, Cox B, Allenby G, Banks M, (1998) HTS approaches to voltage-gated ion channel drug discovery. Drug Discov Today 3: 323-332.