Advertisement

Mammalian Cell-Based Sensor System

  • Pratik Banerjee
  • Briana Franz
  • Arun K. Bhunia
Chapter
Part of the Advances in Biochemical Engineering / Biotechnology book series (ABE, volume 117)

Abstract

Use of living cells or cellular components in biosensors is receiving increased attention and opens a whole new area of functional diagnostics. The term “mammalian cell-based biosensor” is designated to biosensors utilizing mammalian cells as the biorecognition element. Cell-based assays, such as high-throughput screening (HTS) or cytotoxicity testing, have already emerged as dependable and promising approaches to measure the functionality or toxicity of a compound (in case of HTS); or to probe the presence of pathogenic or toxigenic entities in clinical, environmental, or food samples. External stimuli or changes in cellular microenvironment sometimes perturb the “normal” physiological activities of mammalian cells, thus allowing CBBs to screen, monitor, and measure the analyte-induced changes. The advantage of CBBs is that they can report the presence or absence of active components, such as live pathogens or active toxins. In some cases, mammalian cells or plasma membranes are used as electrical capacitors and cell–cell and cell–substrate contact is measured via conductivity or electrical impedance. In addition, cytopathogenicity or cytotoxicity induced by pathogens or toxins resulting in apoptosis or necrosis could be measured via optical devices using fluorescence or luminescence. This chapter focuses mainly on the type and applications of different mammalian cell-based sensor systems.

Keywords

Biosensor Pathogens Toxins Cytotoxicity Rapid detection 

Notes

Acknowledgments

Research in the authors’ laboratory was supported through a cooperative agreement with the Agricultural Research Service of the US Department of Agriculture (USDA) project number 1935-42000-035, the Center for Food Safety and Engineering at Purdue University, and USDA-NRI (2005-35603-16338). BF is supported by the USDA National Needs Fellowship.

References

  1. 1.
    Pancrazio JJ, Whelan JP, Borkholder DA, Ma W, Stenger DA (1999) Development and application of cell-based biosensors. Ann Biomed Eng 27:697–711Google Scholar
  2. 2.
    Banerjee P, Bhunia AK (2009) Mammalian cell-based biosensors for pathogens and toxins. Trends Biotechnol 27(3):179–188Google Scholar
  3. 3.
    Banerjee P, Lenz D, Robinson JP, Rickus JL, Bhunia AK (2008) A novel and simple cell-based detection system with a collagen-encapsulated B-lymphocyte cell line as a biosensor for rapid detection of pathogens and toxins. Lab Invest 88:196–206Google Scholar
  4. 4.
    Bhunia AK, Banada PP, Banerjee P, Valadez A, Hirleman ED (2007) Light scattering, fiber optic-and cell-based sensors for sensitive detection of foodborne pathogens. J Rapid Methods Autom Microbiol 15:121–145Google Scholar
  5. 5.
    Stenger DA, Gross GW, Keefer EW, Shaffer KM, Andreadis JD, Ma W, Pancrazio JJ (2001) Detection of physiologically active compounds using cell-based biosensors. Trends Biotechnol 19:304–309Google Scholar
  6. 6.
    Ziegler C (2000) Cell-based biosensors. Fresenius' J Anal Chem 366:552–559Google Scholar
  7. 7.
    Rawson DM, Willmer AJ, Turner AP (1989) Whole-cell biosensors for environmental monitoring. Biosensors 4:299–311Google Scholar
  8. 8.
    Deng J, Schoenbach KH, Buescher ES, Hair PS, Fox PM, Beebe SJ (2003) The effects of intense submicrosecond electrical pulses on cells. Biophys J 84:2709–2714Google Scholar
  9. 9.
    Giaever I, Keese CR (1993) A morphological biosensor for mammalian cells. Nature 366:591–592Google Scholar
  10. 10.
    Bhakdi S, Bayley H, Valeva A, Walev I, Walker B, Kehoe M, Palmer M (1996) Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch Microbiol 165:73–79Google Scholar
  11. 11.
    Gilbert RJ (2002) Pore-forming toxins. Cell Mol Life Sci 59:832–844Google Scholar
  12. 12.
    Bhunia AK, Westbrook DG (1998) Alkaline phosphatase release assay to determine cytotoxicity for Listeria species. Lett Appl Microbiol 26:305–310Google Scholar
  13. 13.
    Low MG, Finean JB (1978) Specific release of plasma membrane enzymes by a phosphatidylinositol-specific phospholipase C. Biochim Biophys Acta 508:565–570Google Scholar
  14. 14.
    Moss DW (1994) Release of membrane-bound enzymes from cells and the generation of isoforms. Clin Chim Acta 226:131–142Google Scholar
  15. 15.
    Hardy SP, Lund T, Granum PE (2001) CytK toxin of Bacillus cereus forms pores in planar lipid bilayers and is cytotoxic to intestinal epithelia. FEMS Microbiol Lett 197:47–51Google Scholar
  16. 16.
    Sekiya K, Futaesaku Y (1998) Characterization of the damage to membranes caused by bacterial cytolysins. J Electron Microsc (Tokyo) 47:543–552Google Scholar
  17. 17.
    Banerjee P, Morgan MT, Rickus JL, Ragheb K, Corvalan C, Robinson JP, Bhunia AK (2007) Hybridoma Ped-2E9 cells cultured under modified conditions can sensitively detect Listeria monocytogenes and Bacillus cereus. Appl Microbiol Biotechnol 73:1423–1434Google Scholar
  18. 18.
    Gray KM, Bhunia AK (2005) Specific detection of cytopathogenic Listeria monocytogenes using a two-step method of immunoseparation and cytotoxicity analysis. J Microbiol Methods 60:259–268Google Scholar
  19. 19.
    Gray KM, Banada PP, O'Neal E, Bhunia AK (2005) Rapid Ped-2E9 cell-based cytotoxicity analysis and genotyping of Bacillus species. J Clin Microbiol 43:5865–5872Google Scholar
  20. 20.
    Lee JH, Mitchell RJ, Kim BC, Cullen DC, Gu MB (2005) A cell array biosensor for environmental toxicity analysis. Biosens Bioelectron 21:500–507Google Scholar
  21. 21.
    Hertzberg RP, Pope AJ (2000) High-throughput screening: new technology for the 21st century. Curr Opin Chem Biol 4:445–451Google Scholar
  22. 22.
    Aravanis AM, DeBusschere BD, Chruscinski AJ, Gilchrist KH, Kobilka BK, Kovacs GT (2001) A genetically engineered cell-based biosensor for functional classification of agents. Biosens Bioelectron 16:571–577Google Scholar
  23. 23.
    Bousse L (1996) Whole cell biosensors. Sens Actuators B Chem 34:270–275Google Scholar
  24. 24.
    Rabinowitz P, Gordon Z, Chudnov D, Wilcox M, Odofin L, Liu A, Dein J (2006) Animals as sentinels of bioterrorism agents. Emerg Infect Dis 12:647–652Google Scholar
  25. 25.
    Gubernot DM, Boyer BL, Moses MS (2008) Animal as early detectors of bioevents: veterinary tools and a framework for animal-human integrated zoonotic disease surveillance. Public Health Rep 123:300–315Google Scholar
  26. 26.
    van der Schalie WH, Gardner HS, Bantle JA, De Rosa CT, Finch RA, Reif JS, Reuter RH, Backer LC, Burger J, Folmar LC, Stokes WS (1999) Animals as sentinels of human health hazards of environmental chemicals. Environ Health Perspect 107:309–315Google Scholar
  27. 27.
    Li N, Tourovskaia A, Folch A (2003) Biology on a chip: microfabrication for studying the behavior of cultured cells. Crit Rev Biomed Eng 31:423–488Google Scholar
  28. 28.
    O’Shaughnessy TJ, Pancrazio JJ (2007) Broadband detection of environmental neurotoxicants. Anal Chem 79:8838–8845Google Scholar
  29. 29.
    Slaughter GE, Hobson R (2009) An impedimetric biosensor based on PC 12 cells for the monitoring of exogenous agents. Biosens Bioelectron 24:1153–1158Google Scholar
  30. 30.
    Benderitter M, Vincent-Genod L, Pouget JP, Voisin P (2003) The cell membrane as a biosensor of oxidative stress induced by radiation exposure: a multiparameter investigation. Radiat Res 159:471–483Google Scholar
  31. 31.
    Kintzios S, Bem F, Mangana O, Nomikou K, Markoulatos P, Alexandropoulos N, Fasseas C, Arakelyan V, Petrou AL, Soukouli K, Moschopoulou G, Yialouris C, Simonian A (2004) Study on the mechanism of Bioelectric Recognition Assay: evidence for immobilized cell membrane interactions with viral fragments. Biosens Bioelectron 20:907–916Google Scholar
  32. 32.
    Kintzios S, Makri O, Pistola E, Matakiadis T, Shi HP, Economou A (2004) Scale-up production of puerarin from hairy roots of Pueraria phaseoloides in an airlift bioreactor. Biotechnol Lett 26:1057–1059Google Scholar
  33. 33.
    Yamazaki V, Sirenko O, Schafer RJ, Nguyen L, Gutsmann T, Brade L, Groves JT (2005) Cell membrane array fabrication and assay technology. BMC Biotechnol 5:18Google Scholar
  34. 34.
    Alves ID, Salgado GF, Salamon Z, Brown MF, Tollin G, Hruby VJ (2005) Phosphatidylethanolamine enhances rhodopsin photoactivation and transducin binding in a solid supported lipid bilayer as determined using plasmon-waveguide resonance spectroscopy. Biophys J 88:198–210Google Scholar
  35. 35.
    Minic J, Grosclaude J, Aioun J, Persuy MA, Gorojankina T, Salesse R, Pajot-Augy E, Hou Y, Helali S, Jaffrezic-Renault N, Bessueille F, Errachid A, Gomila G, Ruiz O, Samitier J (2005) Immobilization of native membrane-bound rhodopsin on biosensor surfaces. Biochim Biophys Acta 1724:324–332Google Scholar
  36. 36.
    Vo-Dinh T, Cullum B (2000) Biosensors and biochips: advances in biological and medical diagnostics. Fresenius' J Anal Chem 366:540–551Google Scholar
  37. 37.
    Lehmann M, Riedel K, Adler K, Kunze G (2000) Amperometric measurement of copper ions with a deputy substrate using a novel Saccharomyces cerevisiae sensor. Biosens Bioelectron 15:211–219Google Scholar
  38. 38.
    Mattiasson B (1997) Cell-based biosensors for environmental monitoring with special reference to heavy metal analysis. Res Microbiol 148:533Google Scholar
  39. 39.
    Sanders CA, Rodriguez M Jr, Greenbaum E (2001) Stand-off tissue-based biosensors for the detection of chemical warfare agents using photosynthetic fluorescence induction. Biosens Bioelectron 16:439–446Google Scholar
  40. 40.
    Smutok O, Dmytruk K, Gonchar M, Sibirny A, Schuhmann W (2007) Permeabilized cells of flavocytochrome b(2) over-producing recombinant yeast Hansenula polymorpha as biological recognition element in amperometric lactate biosensors. Biosens Bioelectron 23:599–605Google Scholar
  41. 41.
    Immonen N, Karp M (2007) Bioluminescence-based bioassays for rapid detection of nisin in food. Biosens Bioelectron 22:1982–1987Google Scholar
  42. 42.
    Schmidt A, StandfussGabisch C, Bilitewski U (1996) Microbial biosensor for free fatty acids using an oxygen electrode based on thick film technology. Biosens Bioelectron 11:1139–1145Google Scholar
  43. 43.
    Jiang YQ, Xiao LL, Zhao L, Chen X, Wang XR, Wong KY (2006) Optical biosensor for the determination of BOD in seawater. Talanta 70:97–103Google Scholar
  44. 44.
    Lin L, Xiao LL, Huang S, Zhao L, Cui JS, Wang XH, Chen X (2006) Novel BOD optical fiber biosensor based on co-immobilized microorganisms in ormosils matrix. Biosens Bioelectron 21:1703–1709Google Scholar
  45. 45.
    Neufeld T, Biran D, Popovtzer R, Erez T, Ron EZ, Rishpon J (2006) Genetically engineered pfabA pfabR bacteria: an electrochemical whole cell biosensor for detection of water toxicity. Anal Chem 78:4952–4956Google Scholar
  46. 46.
    Sakaguchi T, Kitagawa K, Ando T, Murakami Y, Morita Y, Yamamura A, Yokoyama K, Tamiya E (2003) A rapid BOD sensing system using luminescent recombinants of Escherichia coli. Biosens Bioelectron 19:115–121Google Scholar
  47. 47.
    Sakaguchi T, Morioka Y, Yamasaki M, Iwanaga J, Beppu K, Maeda H, Morita Y, Tamiya E (2007) Rapid and onsite BOD sensing system using luminous bacterial cells-immobilized chip. Biosens Bioelectron 22:1345–1350Google Scholar
  48. 48.
    Chambers J, Ames RS, Bergsma D, Muir A, Fitzgerald LR, Hervieu G, Dytko GM, Foley JJ, Martin J, Liu WS, Park J, Ellis C, Ganguly S, Konchar S, Cluderay J, Leslie R, Wilson S, Sarau HM (1999) Melanin-concentrating hormone is the cognate ligand for the orphan G-protein-coupled receptor SLC-1. Nature 400:261–265Google Scholar
  49. 49.
    Pietrangelo A (2002) Mechanism of iron toxicity. Adv Exp Med Biol 509:19–43Google Scholar
  50. 50.
    Pietrangelo A, Montosi G, Garuti C, Contri M, Giovannini F, Ceccarelli D, Masini A (2002) Iron-induced oxidant stress in nonparenchymal liver cells: mitochondrial derangement and fibrosis in acutely iron-dosed gerbils and its prevention by silybin. J Bioenerg Biomembr 34:67–79Google Scholar
  51. 51.
    Rudolph AS, Reasor J (2001) Cell and tissue based technologies for environmental detection and medical diagnostics. Biosens Bioelectron 16:429–431Google Scholar
  52. 52.
    Sacco MG, Amicone L, Cato EM, Filippini D, Vezzoni P, Tripodi M (2004) Cell-based assay for the detection of chemically induced cellular stress by immortalized untransformed transgenic hepatocytes. BMC Biotechnol 4:5Google Scholar
  53. 53.
    Bhunia AK, Steele PJ, Westbrook DG, Bly LA, Maloney TP, Johnson MG (1994) A six-hour in vitro virulence assay for Listeria monocytogenes using myeloma and hybridoma cells from murine and human sources. Microb Pathog 16:99–110Google Scholar
  54. 54.
    Bhunia AK, Westbrook DG, Story R, Johnson MG (1995) Frozen stored murine hybridoma cells can be used to determine the virulence of Listeria monocytogenes. J Clin Microbiol 33:3349–3351Google Scholar
  55. 55.
    Meister M, Pine J, Baylor DA (1994) Multi-neuronal signals from the retina: acquisition and analysis. J Neurosci Methods 51:95–106Google Scholar
  56. 56.
    Segev R, Goodhouse J, Puchalla J, Berry MJ 2nd (2004) Recording spikes from a large fraction of the ganglion cells in a retinal patch. Nat Neurosci 7:1154–1161Google Scholar
  57. 57.
    Hafner F (2000) Cytosensor Microphysiometer: technology and recent applications. Biosens Bioelectron 15:149–158Google Scholar
  58. 58.
    Wang P, Xu GX, Qin LF, Xu Y, Li Y, Li R (2005) Cell-based biosensors and its application in biomedicine. Sens Actuators B Chem 108:576–584Google Scholar
  59. 59.
    Liu Q, Cai H, Xu Y, Xiao L, Yang M, Wang P (2007) Detection of heavy metal toxicity using cardiac cell-based biosensor. Biosens Bioelectron 22:3224–3229Google Scholar
  60. 60.
    Gilchrist KH, Giovangrandi L, Whittington RH, Kovacs GT (2005) Sensitivity of cell-based biosensors to environmental variables. Biosens Bioelectron 20:1397–1406Google Scholar
  61. 61.
    Whittington RH, Chen MQ, Giovangrandi L, Kovacs GA (2006) Temporal resolution of stimulation threshold: a tool for electrophysiologic analysis. Conf Proc IEEE Eng Med Biol Soc 1:3891–3894Google Scholar
  62. 62.
    Gilchrist KH (2003) Characterization and validation of cell-based biosensors. PhD dissertation, Stanford University, United States–California Retrieved January 13, 2008, from ProQuest Digital Dissertations database (Publication No. AAT 3104228), pp 3–6Google Scholar
  63. 63.
    Keefer EW, Gramowski A, Stenger DA, Pancrazio JJ, Gross GW (2001) Characterization of acute neurotoxic effects of trimethylolpropane phosphate via neuronal network biosensors. Biosens Bioelectron 16:513–525Google Scholar
  64. 64.
    Pancrazio JJ, Keefer EW, Ma W, Stenger DA, Gross GW (2001) Neurophysiologic effects of chemical agent hydrolysis products on cortical neurons in vitro. Neurotoxicology 22:393–400Google Scholar
  65. 65.
    Pancrazio JJ, Gray SA, Shubin YS, Kulagina N, Cuttino DS, Shaffer KM, Eisemann K, Curran A, Zim B, Gross GW, O'Shaughnessy TJ (2003) A portable microelectrode array recording system incorporating cultured neuronal networks for neurotoxin detection. Biosens Bioelectron 18:1339–1347Google Scholar
  66. 66.
    Selinger JV, Pancrazio JJ, Gross GW (2004) Measuring synchronization in neuronal networks for biosensor applications. Biosens Bioelectron 19:675–683Google Scholar
  67. 67.
    Bhunia AK (2008) Biosensors and bio-based methods for the separation and detection of foodborne pathogens. In: Taylor S (ed) Advances in food and nutrition research. Elsevier, San Diego, Vol 54, pp 1–44Google Scholar
  68. 68.
    Ehret R, Baumann W, Brischwein M, Schwinde A, Stegbauer K, Wolf B (1997) Monitoring of cellular behaviour by impedance measurements on interdigitated electrode structures. Biosens Bioelectron 12:29–41Google Scholar
  69. 69.
    Ehret R, Baumann W, Brischwein M, Schwinde A, Wolf B (1998) On-line control of cellular adhesion with impedance measurements using interdigitated electrode structures. Med Biol Eng Comput 36:365–370Google Scholar
  70. 70.
    Tiruppathi C, Malik AB, Del Vecchio PJ, Keese CR, Giaever I (1992) Electrical method for detection of endothelial cell shape change in real time: assessment of endothelial barrier function. Proc Natl Acad Sci USA 89:7919–7923Google Scholar
  71. 71.
    Kowolenko M, Keese CR, Lawrence DA, Giaever I (1990) Measurement of macrophage adherence and spreading with weak electric fields. J Immunol Methods 127:71–77Google Scholar
  72. 72.
    Borkholder DA, Bao J, Maluf NI, Perl ER, Kovacs GT (1997) Microelectrode arrays for stimulation of neural slice preparations. J Neurosci Methods 77:61–66Google Scholar
  73. 73.
    Pancrazio JJ, Bey PP Jr, Loloee A, Manne S, Chao HC, Howard LL, Gosney WM, Borkholder DA, Kovacs GT, Manos P, Cuttino DS, Stenger DA (1998) Description and demonstration of a CMOS amplifier-based-system with measurement and stimulation capability for bioelectrical signal transduction. Biosens Bioelectron 13:971–979Google Scholar
  74. 74.
    Lebrun M, Mengaud J, Ohayon H, Nato F, Cossart P (1996) Internalin must be on the bacterial surface to mediate entry of Listeria monocytogenes into epithelial cells. Mol Microbiol 21:579–592Google Scholar
  75. 75.
    Lundstrom I, Svensson S (1998) Biosensing with G-protein coupled receptor systems. Biosens Bioelectron 13:689–695Google Scholar
  76. 76.
    Subrahmanyam S, Piletsky SA, Turner AP (2002) Application of natural receptors in sensors and assays. Anal Chem 74:3942–3951Google Scholar
  77. 77.
    Wijesuriya DC, Rechnitz GA (1993) Biosensors based on plant and animal tissues. Biosens Bioelectron 8:155–160Google Scholar
  78. 78.
    Golden RJ, Noller KL, Titus-Ernstoff L, Kaufman RH, Mittendorf R, Stillman R, Reese EA (1998) Environmental endocrine modulators and human health: an assessment of the biological evidence. Crit Rev Toxicol 28:109–227Google Scholar
  79. 79.
    Haga T (1995) Receptor biochemistry. In: Meyers RA (ed) Molecular biology and biotechnology, a comprehensive desk reference. VCH, New YorkGoogle Scholar
  80. 80.
    Connolly CN, Wafford KA (2004) The Cys-loop superfamily of ligand-gated ion channels: the impact of receptor structure on function. Biochem Soc Trans 32:529–534Google Scholar
  81. 81.
    Whitaker RD, Walt DR (2007) Multianalyte single-cell analysis with multiple cell lines using a fiber-optic array. Anal Chem 79:9045–9053Google Scholar
  82. 82.
    Robinson DR, Wu YM, Lin SF (2000) The protein tyrosine kinase family of the human genome. Oncogene 19:5548–5557Google Scholar
  83. 83.
    Kaczmarski RS, Mufti GJ (1991) The cytokine receptor superfamily. Blood Rev 5:193–203Google Scholar
  84. 84.
    Milev P, Monnerie H, Popp S, Margolis RK, Margolis RU (1998) The core protein of the chondroitin sulfate proteoglycan phosphacan is a high-affinity ligand of fibroblast growth factor-2 and potentiates its mitogenic activity. J Biol Chem 273:21439–21442Google Scholar
  85. 85.
    Hauck CR, Agerer F, Muenzner P, Schmitter T (2006) Cellular adhesion molecules as targets for bacterial infection. Eur J Cell Biol 85:235–242Google Scholar
  86. 86.
    Weiss AA, Iyer SS (2007) Glycomics aims to interpret the third molecular language of cells. Microbe 2:489–497Google Scholar
  87. 87.
    Hauck CR (2002) Cell adhesion receptors – signaling capacity and exploitation by bacterial pathogens. Med Microbiol Immunol 191:55–62Google Scholar
  88. 88.
    Patti JM, Allen BL, McGavin MJ, Hook M (1994) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48:585–617Google Scholar
  89. 89.
    Schwarz-Linek U, Werner JM, Pickford AR, Gurusiddappa S, Kim JH, Pilka ES, Briggs JA, Gough TS, Hook M, Campbell ID, Potts JR (2003) Pathogenic bacteria attach to human fibronectin through a tandem beta-zipper. Nature 423:177–181Google Scholar
  90. 90.
    Frankel G, Lider O, Hershkoviz R, Mould AP, Kachalsky SG, Candy DC, Cahalon L, Humphries MJ, Dougan G (1996) The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to beta1 integrins. J Biol Chem 271:20359–20364Google Scholar
  91. 91.
    Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, Finlay BB (1997) Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511–520Google Scholar
  92. 92.
    Kenny B (1999) Phosphorylation of tyrosine 474 of the enteropathogenic Escherichia coli (EPEC) Tir receptor molecule is essential for actin nucleating activity and is preceded by additional host modifications. Mol Microbiol 31:1229–1241Google Scholar
  93. 93.
    Hauck CR, Meyer TF (2003) 'Small' talk: Opa proteins as mediators of Neisseria-host-cell communication. Curr Opin Microbiol 6:43–49Google Scholar
  94. 94.
    Steinberg MS, McNutt PM (1999) Cadherins and their connections: adhesion junctions have broader functions. Curr Opin Cell Biol 11:554–560Google Scholar
  95. 95.
    Pertz O, Bozic D, Koch AW, Fauser C, Brancaccio A, Engel J (1999) A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J 18:1738–1747Google Scholar
  96. 96.
    Bierne H, Sabet C, Personnic N, Cossart P (2007) Internalins: a complex family of leucine-rich repeat-containing proteins in Listeria monocytogenes. Microbes Infect 9:1156–1166Google Scholar
  97. 97.
    Braun L, Ghebrehiwet B, Cossart P (2000) gC1q-R/p32, a C1q-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J 19:1458–1466Google Scholar
  98. 98.
    Shen Y, Naujokas M, Park M, Ireton K (2000) InIB-dependent internalization of Listeria is mediated by the Met receptor tyrosine kinase. Cell 103:501–510Google Scholar
  99. 99.
    Gaillard JL, Berche P, Frehel C, Gouin E, Cossart P (1991) Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from Gram-positive cocci. Cell 65:1127–1141Google Scholar
  100. 100.
    Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P (1996) E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84:923–932Google Scholar
  101. 101.
    Dramsi S, Cossart P (1998) Intracellular pathogens and the actin cytoskeleton. Annu Rev Cell Dev Biol 14:137–166Google Scholar
  102. 102.
    Lasa I, Cossart P (1996) Actin-based bacterial motility: towards a definition of the minimal requirements. Trends Cell Biol 6:109–114Google Scholar
  103. 103.
    Pandiripally VK, Westbrook DG, Sunki GR, Bhunia AK (1999) Surface protein p104 is involved in adhesion of Listeria monocytogenes to human intestinal cell line, Caco-2. J Med Microbiol 48:117–124Google Scholar
  104. 104.
    Santiago NI, Zipf A, Bhunia AK (1999) Influence of temperature and growth phase on expression of a 104-kilodalton Listeria adhesion protein in Listeria monocytogenes. Appl Environ Microbiol 65:2765–2769Google Scholar
  105. 105.
    Wampler JL, Kim KP, Jaradat Z, Bhunia AK (2004) Heat shock protein 60 acts as a receptor for the Listeria adhesion protein in Caco-2 cells. Infect Immun 72:931–936Google Scholar
  106. 106.
    Jaradat ZW, Bhunia AK (2003) Adhesion, invasion, and translocation characteristics of Listeria monocytogenes serotypes in Caco-2 cell and mouse models. Appl Environ Microbiol 69:3640–3645Google Scholar
  107. 107.
    Kim KP, Jagadeesan B, Burkholder KM, Jaradat ZW, Wampler JL, Lathrop AA, Morgan MT, Bhunia AK (2006) Adhesion characteristics of Listeria adhesion protein (LAP)-expressing Escherichia coli to Caco-2 cells and of recombinant LAP to eukaryotic receptor Hsp60 as examined in a surface plasmon resonance sensor. FEMS Microbiol Lett 256:324–332Google Scholar
  108. 108.
    Campadelli-Fiume G (2000) Virus receptor arrays, CD46 and human herpesvirus 6. Trends Microbiol 8:436–438Google Scholar
  109. 109.
    Gruenheid S, Gatzke L, Meadows H, Tufaro F (1993) Herpes simplex virus infection and propagation in a mouse L cell mutant lacking heparan sulfate proteoglycans. J Virol 67:93–100Google Scholar
  110. 110.
    Ugolini S, Mondor I, Sattentau QJ (1999) HIV-1 attachment: another look. Trends Microbiol 7:144–149Google Scholar
  111. 111.
    Spear PG, Shieh MT, Herold BC, WuDunn D, Koshy TI (1992) Heparan sulfate glycosaminoglycans as primary cell surface receptors for herpes simplex virus. Adv Exp Med Biol 313:341–353Google Scholar
  112. 112.
    Berger EA, Murphy PM, Farber JM (1999) Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 17:657–700Google Scholar
  113. 113.
    Schroeder K, Neagle B (1996) FLIPR: a new instrument for accurate, high throughput optical screening. J Biomol Screen 1:75Google Scholar
  114. 114.
    Gonzalez JE, Oades K, Leychkis Y, Harootunian A, Negulescu PA (1999) Cell-based assays and instrumentation for screening ion-channel targets. Drug Discov Today 4:431–439Google Scholar
  115. 115.
    Kiss L, Bennett PB, Uebele VN, Koblan KS, Kane SA, Neagle B, Schroeder K (2003) High throughput ion-channel pharmacology: planar-array-based voltage clamp. Assay Drug Dev Technol 1:127–135Google Scholar
  116. 116.
    Zuck P, Lao Z, Skwish S, Glickman JF, Yang K, Burbaum J, Inglese J (1999) Ligand-receptor binding measured by laser-scanning imaging. Proc Natl Acad Sci USA 96:11122–11127Google Scholar
  117. 117.
    Lee JY, Miraglia S, Yan X, Swartzman E, Cornell-Kennon S, Mellentin-Michelotti J, Bruseo C, France DS (2003) Oncology drug discovery applications using the FMAT 8100 HTS system. J Biomol Screen 8:81–88Google Scholar
  118. 118.
    Conway BR, Minor LK, Xu JZ, Gunnet JW, DeBiasio R, D'Andrea MR, Rubin R, DeBiasio R, Giuliano K, Zhou LB, Demarest KT (1999) Quantification of G-protein coupled receptor internalization using G-protein coupled receptor-green fluorescent protein conjugates with the ArrayScan (TM) high-content screening system. J Biomol Screen 4:75–86Google Scholar
  119. 119.
    Gasparri F, Mariani M, Sola F, Galvani A (2004) Quantification of the proliferation index of human dermal fibroblast cultures with the ArrayScan high-content screening reader. J Biomol Screen 9:232–243Google Scholar
  120. 120.
    Trask OJ Jr, Baker A, Williams RG, Nickischer D, Kandasamy R, Laethem C, Johnston PA, Johnston PA (2006) Assay development and case history of a 32K-biased library high-content MK2-EGFP translocation screen to identify p38 mitogen-activated protein kinase inhibitors on the ArrayScan 3.1 imaging platform. Methods Enzymol 414:419–439Google Scholar
  121. 121.
    Williams RG, Kandasamy R, Nickischer D, Trask OJ Jr, Laethem C, Johnston PA, Johnston PA (2006) Generation and characterization of a stable MK2-EGFP cell line and subsequent development of a high-content imaging assay on the Cellomics ArrayScan platform to screen for p38 mitogen-activated protein kinase inhibitors. Methods Enzymol 414:364–389Google Scholar
  122. 122.
    Liu Q, Huang H, Cai H, Xu Y, Li Y, Li R, Wang P (2007) Embryonic stem cells as a novel cell source of cell-based biosensors. Biosens Bioelectron 22:810–815Google Scholar
  123. 123.
    May KML, Wang Y, Bachas LG, Anderson KW (2004) Development of a whole-cell-based biosensor for detecting histamine as a model toxin. Anal Chem 76:4156–4161Google Scholar
  124. 124.
    Davila JC, Cezar GG, Thiede M, Strom S, Miki T, Trosko J (2004) Use and application of stem cells in toxicology. Toxicol Sci 79:214–223Google Scholar
  125. 125.
    Raucy JL, Mueller L, Duan K, Allen SW, Strom S, Lasker JM (2002) Expression and induction of CYP2C P450 enzymes in primary cultures of human hepatocytes. J Pharmacol Exp Ther 302:475–482Google Scholar
  126. 126.
    Lavon N, Benvenisty N (2003) Differentiation and genetic manipulation of human embryonic stem cells and the analysis of the cardiovascular system. Trends Cardiovasc Med 13:47–52Google Scholar
  127. 127.
    Rambhatla L, Chiu CP, Kundu P, Peng Y, Carpenter MK (2003) Generation of hepatocyte-like cells from human embryonic stem cells. Cell Transplant 12:1–11Google Scholar
  128. 128.
    Trosko JE (2003) The role of stem cells and gap junctional intercellular communication in carcinogenesis. J Biochem Mol Biol 36:43–48Google Scholar
  129. 129.
    Hanson GT, Hanson BJ (2008) Fluorescent probes for cellular assays. Comb Chem High Throughput Screen 11:505–513Google Scholar
  130. 130.
    Wang H-Y, Bao N, Lu C (2008) A microfluidic cell array with individually addressable culture chambers. Biosens Bioelectron 24:613–617Google Scholar
  131. 131.
    Lee RM, Choi H, Shin J-S, Kim K, Yoo K-H (2009) Distinguishing between apoptosis and necrosis using a capacitance sensor. Biosens Bioelectron 24(8):2586–2591Google Scholar
  132. 132.
    Tong C, Shi B, Xiao X, Liao H, Zheng Y, Shen G, Tang D, Liu X (2009) An annexin V based biosensor for quantitatively detecting early apoptotic cells. Biosens Bioelectron 24(6):1777–1782Google Scholar
  133. 133.
    Gil GC, Mitchell RJ, Chang ST, Gu MB (2000) A biosensor for the detection of gas toxicity using a recombinant bioluminescent bacterium. Biosens Bioelectron 15:23–30Google Scholar
  134. 134.
    Hay AG, Rice JF, Applegate BM, Bright NG, Sayler GS (2000) A bioluminescent whole-cell reporter for detection of 2,4-dichlorophenoxyacetic acid and 2,4-dichlorophenol in soil. Appl Environ Microbiol 66:4589–4594Google Scholar
  135. 135.
    Rider TH, Petrovick MS, Nargi FE, Harper JD, Schwoebel ED, Mathews RH, Blanchard DJ, Bortolin LT, Young AM, Chen J, Hollis MA (2003) A B cell-based sensor for rapid identification of pathogens. Science 301:213–215Google Scholar
  136. 136.
    Shingleton JT, Applegate BA, Baker AJ, Sayler GS, Bienkowski PR (2001) Quantification of toluene dioxygenase induction and kinetic modeling of TCE cometabolism by Pseudomonas putida TVA8. Biotechnol Bioeng 76:341–350Google Scholar
  137. 137.
    O’Riordan TC, Buckley D, Ogurtsov V, O'Connor R, Papkovsky DB (2000) A cell viability assay based on monitoring respiration by optical oxygen sensing. Anal Biochem 278:221–227Google Scholar
  138. 138.
    Sturzl M, Konrad A, Sander G, Wies E, Neipel F, Naschberger E, Reipschlager S, Gonin-Laurent N, Horch RE, Kneser U, Hohenberger W, Erfle H, Thurau M (2008) High throughput screening of gene functions in mammalian cells using reversely transfected cell arrays: review and protocol. Comb Chem High Throughput Screen 11:159–172Google Scholar
  139. 139.
    Durick K, Negulescu P (2001) Cellular biosensors for drug discovery. Biosens Bioelectron 16:587–592Google Scholar
  140. 140.
    Kumar HS, Karunasagar I, Teizou T, Shima K, Yamasaki S (2004) Characterisation of Shiga toxin-producing Escherichia coli (STEC) isolated from seafood and beef. FEMS Microbiol Lett 233:173–178Google Scholar
  141. 141.
    Noda M, Yutsudo T, Nakabayashi N, Hirayama T, Takeda Y (1987) Purification and some properties of Shiga-like toxin from Escherichia coli 0157:H7 that is immunologically identical to Shiga toxin. Microb Pathog 2:339–349Google Scholar
  142. 142.
    Picot L, Chevalier S, Mezghani-Abdelmoula S, Merieau A, Lesouhaitier O, Leroux P, Cazin L, Orange N, Feuilloley MG (2003) Cytotoxic effects of the lipopolysaccharide from Pseudomonas fluorescens on neurons and glial cells. Microb Pathog 35:95–106Google Scholar
  143. 143.
    Ngamwongsatit P, Banada PP, Panbangred W, Bhunia AK (2008) WST-1-based cell cytotoxicity assay as a substitute for MTT-based assay for rapid detection of toxigenic Bacillus species using CHO cell line. J Microbiol Methods 73:211–215Google Scholar
  144. 144.
    Sakurazawa T, Ohkusa T (2005) Cytotoxicity of organic acids produced by anaerobic intestinal bacteria on cultured epithelial cells. J Gastroenterol 40:600–609Google Scholar
  145. 145.
    Saliba AM, de Assis MC, Nishi R, Raymond B, Marques Ede A, Lopes UG, Touqui L, Plotkowski MC (2006) Implications of oxidative stress in the cytotoxicity of Pseudomonas aeruginosa ExoU. Microbes Infect 8:450–459Google Scholar
  146. 146.
    Lee J, Cuddihy MJ, Kotov NA (2008) Three-dimensional cell culture matrices: state of the art. Tissue Eng Part B Rev 14:61–86Google Scholar
  147. 147.
    Liu J, Kuznetsova LA, Edwards GO, Xu J, Ma M, Purcell WM, Jackson SK, Coakley WT (2007) Functional three-dimensional HepG2 aggregate cultures generated from an ultrasound trap: comparison with HepG2 spheroids. J Cell Biochem 102:1180–1189Google Scholar
  148. 148.
    Pampaloni F, Reynaud EG, Stelzer EHK (2007) The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol 8:839–845Google Scholar
  149. 149.
    Yamada KM, Cukierman E (2007) Modeling tissue morphogenesis and cancer in 3D. Cell 130:601–610Google Scholar
  150. 150.
    Nickerson C, Richter E, Ott C (2007) Studying host–pathogen interactions in 3-D: organotypic models for infectious disease and drug development. J Neuroimmune Pharmacol 2:26–31Google Scholar
  151. 151.
    Smith YC, Grande KK, Rasmussen SB, O'Brien AD (2006) Novel three-dimensional organoid model for evaluation of the interaction of uropathogenic Escherichia coli with terminally differentiated human urothelial cells. Infect Immun 74:750–757Google Scholar
  152. 152.
    Curtis T, Naal RMZG, Batt C, Tabb J, Holowka D (2008) Development of a mast cell-based biosensor. Biosens Bioelectron 23:1024–1031Google Scholar
  153. 153.
    Straub TM, KHz B, Orosz-Coghlan P, Dohnalkova A, Mayer BK, Bartholomew RA, Valdez CO, Bruckner-Lea CJ, Gerba CP, Abbaszadegan M, Nickerson CA (2007) In vitro cell culture infectivity assay for human Noroviruses. Emerg Infect Dis 13:396–403Google Scholar
  154. 154.
    Lee M-Y, Kumar RA, Sukumaran SM, Hogg MG, Clark DS, Dordick JS (2008) Three-dimensional cellular microarray for high-throughput toxicology assays. Proc Nat Acad Sci USA 105:59–63Google Scholar
  155. 155.
    Campbell CE, Laane MM, Haugarvoll E, Giaever I (2007) Monitoring viral-induced cell death using electric cell-substrate impedance sensing. Biosens Bioelectron 23:536–542Google Scholar
  156. 156.
    Moschopoulou G, Vitsa K, Bem F, Vassilakos N, Perdikaris A, Blouhos P, Yialouris C, Frosyniotis D, Anthopoulos I, Mangana O, Nomikou K, Rodeva V, Kostova D, Grozeva S, Michaelides A, Simonian A, Kintzios S (2008) Engineering of the membrane of fibroblast cells with virus-specific antibodies: a novel biosensor tool for virus detection. Biosens Bioelectron 24:1033–1036Google Scholar
  157. 157.
    Relman DA (2003) Shedding light on microbial detection. N Engl J Med 349:2162–2163Google Scholar
  158. 158.
    Shroyer ML, Bhunia AK (2003) Development of a rapid 1-h fluorescence-based cytotoxicity assay for Listeria species. J Microbiol Methods 55:35–40Google Scholar
  159. 159.
    Zhao J, Jedlicka SS, Lannu JD, Bhunia AK, Rickus JL (2006) Liposome-doped nanocomposites as artificial cell-based biosensors: detection of listeriolysin O. Biotechnol Prog 22:32–37Google Scholar
  160. 160.
    Barak LS, Salahpour A, Zhang X, Masri B, Sotnikova TD, Ramsey AJ, Violin JD, Lefkowitz RJ, Caron MG, Gainetdinov RR (2008) Pharmacological characterization of membrane-expressed human trace amine-associated receptor 1 (TAAR1) by a bioluminescence resonance energy transfer cAMP biosensor. Mol Pharmacol 74:585–594Google Scholar
  161. 161.
    Rogers KR, Valdes JJ, Eldefrawi ME (1991) Effects of receptor concentration, media pH and storage on nicotinic receptor-transmitted signal in a fiber-optic biosensor. Biosens Bioelectron 6:1–8Google Scholar
  162. 162.
    Hanslick JL, Lau K, Noguchi KK, Olney JW, Zorumski CF, Mennerick S, Farber NB (2009) Dimethyl sulfoxide (DMSO) produces widespread apoptosis in the developing central nervous system. Neurobiol Dis 34(1):1–10Google Scholar
  163. 163.
    Korbutt GS, Rayat GR, Ezekowitz J, Rajotte RV (1997) Cryopreservation of rat pancreatic islets: effect of ethylene glycol on islet function and cellular composition. Transplantation 64:1065–1070Google Scholar
  164. 164.
    Gilchrist KH, Barker VN, Fletcher LE, DeBusschere BD, Ghanouni P, Giovangrandi L, Kovacs GT (2001) General purpose, field-portable cell-based biosensor platform. Biosens Bioelectron 16:557–564Google Scholar
  165. 165.
    Baust JM, Van B, Baust JG (2000) Cell viability improves following inhibition of cryopreservation-induced apoptosis. In Vitro Cell Dev Biol Anim 36:262–270Google Scholar
  166. 166.
    Nakagawa T, Yamaguchi M (2005) Overexpression of regucalcin suppresses apoptotic cell death in cloned normal rat kidney proximal tubular epithelial NRK52E cells: change in apoptosis-related gene expression. J Cell Biochem 96:1274–1285Google Scholar
  167. 167.
    Kovacs GT (2003) Electronic sensors with living cellular components. Proc IEEE 91:915–929Google Scholar
  168. 168.
    Keusgen M (2002) Biosensors: new approaches in drug discovery. Naturwissenschaften 89:433–444Google Scholar
  169. 169.
    Burrell GA, Seibert FM (1916) Gases found in coal mines. Miners’ Circ 14Google Scholar
  170. 170.
    Schwabe CW (1984) Animals as monitors of the environment. Veterinary Medicine and Human Health, 3rd ed. Williams and Wilkins, Baltimore, MD, USA, pp 562–578Google Scholar
  171. 171.
    Veterinarian (1874) The effects of the fog on cattle in London. Veterinarian 47:1–4Google Scholar
  172. 172.
    Veterinarian (1874) The effects of the recent fog on the Smithfield Show and the London dairies. Veterinarian 47:32–33Google Scholar
  173. 173.
    Haring CM, Meyer KF (1915) Investigations of livestock conditions with horses in the Selby smoke zone. Calif Hurrau Mines Bull 98Google Scholar
  174. 174.
    Holm LW, Wheat JD, Rhode EA, Firch G (1953) Treatment of chronic lead poisoning in horses with calcium disodium ethylenediaminetetreacetate. J Am Vet Assoc 123:383–388Google Scholar
  175. 175.
    Kurland LT, Faro SN, Siedler H (1960) Minamata disease. World Neurol 1:370–395Google Scholar
  176. 176.
    Kuratsune M, Yoshimura T, Matsuzaka J, Yamaguchi A (1972) Epidemiologic study on Yusho, a poisoning caused by ingestion of rice oil contaminated with a commercial brand of polychlorinated biphenyls. Environ Health Perspect 1:119–128Google Scholar
  177. 177.
    Van Kampen KR, James LF, Rasmussen J, Huffaker RH, Fawcett MO (1969) Organic phosphate poisoning of sheep in Skull Valley, Utah. J Am Vet Med Asso 154:623–630Google Scholar
  178. 178.
    Case AA, Coffman JR (1973) Waste oil: toxic for horses. Vet Clin North Am 3:273–277Google Scholar
  179. 179.
    Carter CD, Kimbrough RD, Liddle JA (1975) Tetrachlorodibenzodioxin: an accidental poisoning episode in horse arenas. Science 188:738–740Google Scholar
  180. 180.
    Jackson TF, Halbert FL (1974) A toxic syndrome associated with the feeding of polybrominated biphenyl-contaminated protein concentrate to dairy cattle. J Am Vet Med Asso 165:437–439Google Scholar
  181. 181.
    Welborn JA, Allen R, Byker G, DeGrow S, Hertel J, Noordhoek R, Koons D (1975) The contamination crisis in Michigan: polybrominated biphenyls. Senate Special Investigating Committee, Lansing, MIGoogle Scholar
  182. 182.
    Guillette LJ Jr, Gross TS, Masson GR, Matter JM, Percival HF, Woodward AR (1994) Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ Health Perspect 102:680–688Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Pratik Banerjee
    • 1
  • Briana Franz
    • 1
  • Arun K. Bhunia
    • 2
  1. 1.Laboratory of Food Microbiology & Immunochemistry, Department of Food & Animal SciencesAlabama A&M UniversityNormalUSA
  2. 2.Molecular Food Microbiology Laboratory, Center for Food Safety EngineeringPurdue UniversityWest LafayetteUSA

Personalised recommendations