Effects of bacterial toxins on endothelial tight junction in vitro: A mechanism-based investigation

Toxicology Mechanisms and Methods

Volumn 17, Issue 6, 2007, Pages 331-347

  Singh, Ashok K ^a,b   Jiang, Yin ^a   Gupta, Shveta ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Apoptosis; Blood Brain Barrier; Endothelial Tight Junction; Lipopolysaccharide; Lipoteichoic Acid; NF B

Indexed keywords

BACTERIAL TOXIN; CASPASE 8; CYTOKINE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; OCCLUDIN; PROTEIN; PROTEIN P50; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ZONULA OCCLUDENS 1 PROTEIN;

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL CULTURE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; RAT; TIGHT JUNCTION;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

EID: 34547155721     PISSN: 15376516     EISSN: 15376524     Source Type: Journal    
DOI: 10.1080/15376510601077029     Document Type: Article

References (80)

1. Adams, J. K., and Tepperman, B. L. 2001. Colonic production and expression of IL-4, IL-6, and IL-10 in neonatal suckling rats after LPS challenge. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G755-G762.
2. Ahishali, B., Kaya, M., Kalayci, R., Uzun, H., Bilgic, B., Arican, N., Elmas, I., Aydin, S., and Kucuk, M. 2005. Effects of lipopolysaccharide on the blood-brain barrier permeability in prolonged nitric oxide blockade-induced hypertensive rats. Int. J. Neurosci. 115:151-168.
3. Arthur, F. E., Shivers, R. R., and Bowman, P. D. 1987. Astrocyte-mediated induction of tight junctions in brain capillary endothelium: an efficient in vitro model. Dev. Brain Res. 36:155-159.
4. Badger, J. L., and Kim, K. S. 1998. Environmental growth conditions influence the ability of Escherichia coli K1 to invade brain microvascular endothelial cells and confer serum resistance. Infect. Immunity 66:5692-5707.
5. Badger, J. L., Wass, C. A., and Kim, K. S. 2000. Identification of Escherichia coli K1 genes contributing to human brainmicrovascular endothelial cell invasion by differential fluorescence induction. Mol. Microbiol. 36:174-182.
6. Bailey, D. P., Kashyap, M., Bouton, L. A., Murray, P. J., and Ryan, J. J. 2006. Interleukin IL-10 induces apoptosis in developing mast cells and macrophases. J. Leuk. Biol. 80:581-589.
7. Bazzoni, G., Martinez-Estrada, O-M., Orsenigo, F., Cordenonsi, M., Citi, S., and Dejana, S. 2000. Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and OCLg. J. Biol. Chem. 275:20520-20526.
8. Bermpohl, D., Halle, A., Freyer, D., Dagand, E., Braun, J. S., Bechmann, I., Schroder, N. W., and Weber, J. R. 2005. Bacterial programmed cell death of cerebral endothelial cells involves dual death pathways. J. Clin. Invest 115:1607-1615.
9. Beutler, B., and Rietschel, E. T. 2003. Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol. 3:169-176.
10. Blasig,, I. E., Winkler, L., Lassowski, B., Mueller, S. L., Zuleger, N., Krause, E., Krause, G., Gast, K., Kolbe, M., and Piontek, J. 2006. On the self-association potential of transmembrane tight junction proteins. Cell. Mol. Life Sci. 63:505-514.
11. Bouton, L. A., Ramirez, C. D., Bailey, D. P., Yeatman, C. F., Yue, J., Wright, H. V., Domen, J., Rosato, R. R., Grant, S., Fischer-Stenger, K., and Ryan, J. J. 2004. Costimulation with interleukin-4 and interleukin-10 induces mast cell apoptosis and cell-cycle arrest: the role of p53 and the mitochondrion. Exp. Hematol. 32:1137-1145.
12. Boveri, M., Kinsner, A., Berezowski, V., Lenfant, A. M., Draing, C., Cecchelli, R., Dehouck, M. P., Hartung, T., Prieto, P., and Bal-Price, A. 2006. Highly purified lipoteichoic acid from gram-positive bacteria induces in vitro blood-brain barrier disruption through glia activation: role of pro-inflammatory cytokines and nitric oxide. Neuroscience 137:1193-1209.
13. Brown, R. C., and Davis, T. 2002. Calcium modulation of adherens and tight junction function. Stroke 33:1706-1711.
14. Brown, R. C., Mark, K. S., Egleton, R. D., Huber, J. D., Burroughs, A. R., and Davis, T. P. 2003. Protection against hypoxia-induced increase in blood-brain barrier permeability: role of tight junction proteins and NFkappaB. J Cell Sci. 116:693-700.
15. Cai, Z., Pan, Z-L., Pang, Y., Evans, O. B., and Rhodes, P. G. 2000. Cytokine induction in fetal rat brain and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr. Res. 47:64-72.
16. Cartmell, T., Luheshi, G. N., and Rothwell, N. J. 1999. Brain sites of action of endogenous interleukin-1 in the febrile response to localized inflammation in the rat. J. Physiol. 518:585-594.
17. Ching, S., Zhang, H., Lai, W., and Quan, N. 2006. Peripheral injection of lipopolysaccharide prevents brain recruitment of leukocytes induced by central injection of interleukin-1. Neuroscience 137:717-726.
18. Chio, C. C., Baba, T., and Black, K. L. 1992. Selective blood-tumor barrier disruption by leukotrienes. J. Neurosurg. 77:407-410.
19. Chomczynski, P., and Sacchi, N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
20. Cucullo, L., Aumayr, B., Rapp, E., and Janigro, D. 2005. Drug delivery and in vitro models of the blood-brain barrier. Curr. Opin. Drug. Disc. Dev. 8:89-99.
21. Cucullo, L., McAllister, M. S., Kight, K., Krizanac-Bengez, L., Marroni, M., Mayberg, M. R., Stanness, K. A., and Janigro, D. 2002. A new dynamic in vitro model for the multidimensional study of astrocyte-endothelial cell interactions at the blood-brain barrier. Br. Res. 951:243-254.
22. Deli,, M. A., Abraham, C. S., Kataoka, Y., and Niwa, M. 2005. Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell. Mol. Neurobiol. 25:59-127.
23. Doran,, K. S., Engelson, E. J., Khosravi, A., Maisey, H. C., Fedtke, I., Equils, O., Michelsen, K. S., Arditi, M., Peschel, A., and Nizet, V. 2005. Blood-brain barrier invasion by group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J. Clin. Invest. 115:2499-2507.
24. Dziarski, R., Tapping, R. I., and Tobias, P. S. 1998. Binding of bacterial peptidoglycan to CD14. J. Biol. Chem. 273:8680-8690.
25. Fan, T.-J., Han, L.-H., Cong, R.-S., and Liang, J. 2005. Caspase family and apoptosis. Acta Bioche. Biophys. Sinica 37:719-727.
26. Fanning, A. S., Ma, T. Y., and Anderson, J. M. 2002. Isolation and functional characterization of the actin binding region in the tight junction protein ZO-1. FASEB J. 16:1835-1837.
27. Fanning, A. S., Mitic, L. L., and Anderson, J. M. 1999. Transmembrane proteins in the tight junction barrier. J. Am. Soc. Nephrol. 10:1337-1345.
28. Fenstermacher, J. D. 1980. Comparative aspects of blood-brain exchange. Fed. Proc. 39:3201-3206.
29. Franke, H., Ringelstein, E. B., and Stogbauer, F. 2005. Electromagnetic fields (GSM 1800) do not alter blood-brain barrier permeability to sucrose in models in vitro with high barrier tightness. Bioelectromagnetics 26:529-535.
30. Fu, Y., and Galan, J. E. 1999. A Salmonella protein antagonizes Rac-1 and CDC42 to mediate host cell recovery after bacterial invasion. Nature 401:293-297.
31. Gabeller, M. M., Griffais, R., Fillion, G., and Haour, F. 1995. Expression of interleukin 1 alpha, interleukin 1 beta and interleukin 1 receptor antagonist mRNA in mouse brain: regulation by bacterial lipopolysaccharide (LPS) treatment. Brain Res. Mol. Br. Res. 31:122-130.
32. Gaillard, P. J., Voorwinden, L. H., Nielsen, J. L., Ivanov, A., Atsumi, R., Engman, H., Ringbom, C., de Boer, A. G., and Breimer, D. D. 2001. Establishment and functional characterization of an in vitro model of the blood-brain barrier, comprising a co-culture of brain capillary endothelial cells and astrocytes. Eur. J. Pharmac. Sci. 12:215-222.
33. Gerhart, D. Z., Broderius, M. A., and Drewes, L. R. 1988. Cultured human and canine endothelial cells from brain microvessels. Brain Res. Bull. 21:785-793.
34. Gutierrez-Venegas, G., Kawasaki-Cardenas, P., Cruz-Arroyo, S. R., Perez-Garzon, M., and Maldonado-Frias, S. 2006. Actinobacillus actinomycetemcomitans lipopolysaccharide stimulates the phosphorylation of p44 and p42 MAP kinases through CD14 and TLR-4 receptor activation in human gingival fibroblasts. Life Sci. 78:2577-2583.
35. Harry, G. J., Billingsley, M., Bruinink, A., Campbell, I. L., Classen, W., Dorman, D. C., Galli, C., Ray, D., Smith, R. A., and Tilson, H. A. 1998. In vitro techniques for the assessment of neurotoxicity. Environ. Health Persp. 106(Supp1):131-158.
36. Hartz, A. M., Bauer, B., Fricker, G., and Miller, D. S. 2006. Rapid modulation of P-glycoprotein-mediated transport at the blood-brain barrier by tumor necrosis factor-alpha and lipopolysaccharide. Mol. Pharmacol. 69:462-470.
37. Haskins, J., Gu, L., Wittchen, E. S., Hibbard, J., and Stevenson, B. R. 1998. ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J. Cell Biol. 141:199-208.
38. Hermann, C., Spreitzer, I., Schroder, N. W., Morath, S., Lehner, M. D., Fischer, W., Schutt, C., Schumann, R. R., and Hartung, T. 2002. Cytokine induction by purified lipoteichoic acids from various bacterial species-role of LBP, sCD14, CD14 and failure to induce IL-12 and subsequent IFN-gamma release. Eur. J. Immunol. 32:541-551.
39. Hetman, M., and Kharebava, G. 2006. Survival signaling pathways activated by NMDA receptors. Curr. Topics Med. Chem. 6:787-799.
40. Hirase, T., Staddon, J. M., Saitou, M., Ando-Akatsuka, Y., Itoh, M., Furuse, M., Fujimoto, K., Tsukita, S., and Rubin, L. L. 1997. Occludin as a possible determinant of tight junction permeability in endothelial cells. J. Cell Sci. 110:1603-1613.
41. Hurst, R. D., Azam, S., Hurst, A., and Clark, J. B. 2001. Nitric-oxide-induced inhibition of glyceraldehyde-3-phosphate dehydrogenase may mediate reduced endothelial cell monolayer integrity in an in vitro model blood-brain barrier. Br. Res. 894:181-188.
42. Isowa, N., Xavier, A. M., Dziak, E., Opas, M., McRitchie, D. I., Slutsky, A. S., Keshavjee, S. H., and Liu, M. 1999. LPS-induced depolymerization of cytoskeleton and its role in TNF-α production by rat pneumocytes. Am. J. Physiol. Lung Cell. Mol. Physiol. 277:L606-L615.
43. Kim, B. Y., Kang, J., and Kim, K. S. 2005. Invasion processes of pathogenic Escherichia coli. Int. J. Med. Microbiol. 295:463-470.
44. Kinsner, A., Pilotto, V., Deininger, S., Brown, G. C., Coecke, S., Hartung, T., and Bal-Price, A. 2005. Inflammatory neurodegeneration induced by lipoteichoic acid from Staphylococcus aureus is mediated by glia activation, nitrosative and oxidative stress, and caspase activation. J. Neurochem. 95:1132-1143.
45. Kneisel, U., and Wolburg, H. 2000. Tight junctions of the blood-brain barrier. Cell. Mol. Neurobiol. 20:57-76.
46. Krizbai, I. A., Bauer, H., Bresgen, N., Eckl, P. M., Farkas, A., Szatmari, E., Traweger, A., Wejksza, K., and Bauer, H. C. 2005. Effect of oxidative stress on the junctional proteins of cultured cerebral endothelial cells. Cell. Mol. Neurobiol. 25:129-139.
47. Lai, C. H., Kuo, K. H., and Leo, J. M. 2005. Critical role of actin in modulating BBB permeability. Br. Res. Br. Res. Rev. 50:7-13.
48. Lai, C. H., and Kuo, K. H. 2005. The critical component to establish in vitro BBB model. Br. Res. Br. Res. Rev. 50:258-265.
49. Li, S-H., Lam, S., Cheng, A. L., and Li, X-J. 2000. Intranuclear huntingtin increases the expression of caspase-1 and induces apoptosis. Human Mol. Genet. 9:2859-2867.
50. Loucks, F. A., Le, S. S., Zimmermann, A. K., Ryan, K. R., Barth, H., Aktories, K., and Linseman, D. A. 2006. Rho family GTPase inhibition reveals opposing effects of mitogen-activated protein kinase kinase/extracellular signal-regulated kinase and Janus kinase/signal transducer and activator of transcription signaling cascades on neuronal survival. J. Neurochem. 97:957-667.
51. Madara, J. L., Barenberg, D., and Carlson, S. 1986. Effects of cytochalasin D on occluding junctions of intestinal absorptive cells: further evidence that the cytoskeleton may influence paracellular permeability and junctional change selectivity. J. Cell Biol. 102:2125-2136.
52. Maslin, C. L., Kedzierska, K., Webster, N. L., Muller, W. A., and Crowe, S. M. 2005. Transendothelial migration of monocytes: the underlying molecular mechanisms and consequences of HIV-1 infection. Curr. HIV Res. 3:303-317.
53. McClenahan, D. J., Sotos, J. P., and Czuprynski, C. J. 2005. Cytokine response of bovine mammary gland epithelial cells to Escherichia coli, coliform culture filtrate, or lipopolysaccharide. Am. J. Vet. Res. 66:1590-1597.
54. Miller, D. J., Eckert, J. J., Lazzari, G., Duranthon-Richoux, V., Sreenan, J., Morris, D., Galli, C., Jean-Paul Renard, J.P., and Flemming, T. P. 2003. Tight junction messenger RNA expression levels in bovine embryos are dependent upon the ability to compact and in vitro culture methods. Biol. Reprod. 68:1394-1402.
55. Morita, K., Itoh, M., Saitou, M., Ando-Akatsuka, Y., Furuse, M., Yoneda, K., Imamura, S., Fujimoto, K., and Tsukita, S. 1998. Subcellular distribution of tight junction-associated proteins (occludin, ZO-1, ZO-2) in rodent skin. J. Invest. Dermatol. 110:862-866.
56. Pardridge, W. M. 1981. Transport of nutrients and hormones through the blood-brain barrier. Diabetologia 20:246-254.
57. Persidsky, Y., Ghorpade, A., Rasmussen, J., Limoges, J., Juan-Liu, X., Stins Milan Fiala, M., Way, D., Sik Kim, K., Witte, M. H., Weinand, M., Carhart, L. R., and Gendelman, H. E. 1999. Microglial and astrocyte chemokines regulate monocyte migration through the blood-brain barrier in human immunodeficiency virus-1 encephalitis. Am. J. Pathol. 155:1599-1611.
58. Philpott, D. J., Mckay, D. M., Sherman, P. M., and Perdue, M. H. 1996. Infection of T84 intestinal epithelial cells with enteropathogenic Escherichia coli alters barrier and transport functions. Am. J. Physiol. 270:G634-G645.
59. Pialoux, G., Fournier, S., Moulignier, A., Poveda, J. D., Clavel, F., and Dupont, B. 1997. Central nervous system as a sanctuary for HIV-1 infection despite treatment with zidovudine, lamivudine and indinavir. AIDS 11:1302-1303.
60. Ponting, C. P., Phillips, C., Davies, K. E., and Blake, D. J. 1997. PDZ domains: targeting signalling molecules to sub-membranous sites. Bioassays 19:469-479.
61. Prieto, P., Blaauboer, B. J., de Boer, A. G., Boveri, M., Cecchelli, R., Clemedson, C., Coecke, S., Forsby, A., Galla, H. J., Garberg, P., Greenwood, J., Price, A., and Tahti, H. 2004. European Centre for the Validation of Alternative Methods. Blood-brain barrier in vitro models and their application in toxicology. The report and recommendations of ECVAM Workshop 49. ATLA-Alternatives to Lab Animals 32:37-50.
62. Quan, N., He, L., and Lai, W. 2003. Endothelial activation is an intermediate step for peripheral lipopolysaccharide induced activation of paraventricular nucleus. Br. Res. Bull. 59:447-452.
63. Ring, A., Weiser,, J. N., and Tuomanen, E. I. 1998. Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway. J. Clin. Invest. 102:347-360.
64. Schirmacher,, A., Winters, S., Fischer, S., Goeke, J., Galla, H. J., Kullnick, U., Ringelstein, E. B., and Stogbauer, F. 2000. Electromagnetic fields (1.8 GHz) increase the permeability to sucrose of the blood-brain barrier in vitro. Bioelectromagnetics 21:338-345.
65. Schroder, N. W., Morath, S., Alexander, C., Hamann, L., Hartung, T., Zahringer, U., Gobel, U. B., Weber, J. R., and Schumann, R. R. 2003. Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide- binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J. Biol. Chem. 278:15587-15594.
66. Si, Q., Nakamura, Y., and Kataoka, K. 2000. A serum factor enhances production of nitric oxide and tumor necrosis factor-alpha from cultured microglia. Exp. Neurol. 162:89-97.
67. Singh, A. K., and Jiang, Y. 2004a. How does peripheral lipopolysaccharide induce gene expression in the brain of rats?. Toxicology 201:197-207.
68. Singh, A. K., and Jiang, Y. 2004b. Differential activation of NFκB/RelA-p50 and NFκB/p50-p50 in control and alcohol-drinking rats subjected to carrageenin-induced pleurisy. Mediators Inflamm. 13:255-262.
69. Stanness, K. A., Neumaier, J. F., Sexton, T. J., Grant, G. A., Emmi, A., Maris, D. O., and Janigro, D. 1999. A new model of the blood-brain barrier: co-culture of neuronal, endothelial and glial cells under dynamic conditions. Neuroreport 10:3725-3731.
70. Stanness, K. A., Westrum, L. E., Fornaciari, E., Mascagni, P., Nelson, J. A., Stenglein, S. G., Myers, T., and Janigro, D. 1997. Morphological and functional characterization of an in vitro blood-brain barrier model. Br. Res. 771:329-342.
71. Stins, M. F., Badger, J., and Sik Kim, K. 2001. Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb. Pathol. 30:19-28.
72. Strelow, L., Janigro, D., and Nelson, J. A. 2002. Persistent SIV infection of a blood-brain barrier model. J. Neurovirol. 8:270-280.
73. Tafazoli, F. C. Q., Zeng, M. K., Estes, K.-E., Magnusson, K., and Svensson, L. 2001. NSP4 enterotoxin of Rotavirus induces paracellular leakage in polarized epithelial cells. J. Virol 75:1540-1546.
74. Wolburg, H., and Lippoldt, A. 2002. Tight junctions of the blood-brain barrier: development, composition and regulation. Vas. Pharmacol. 38:323-337.
75. Wong, D., Dorovini-Zis, K., and Vincent, S. R. 2004. Cytokines, nitric oxide, and cGMP modulate the permeability of an in vitro model of the human blood-brain barrier. Exp. Neurol. 190:446-455.
76. Xaio, H., Banks, W. A., Niehoff, W. A., and Morley, J. E. 2001. Effects of LPS in the permeability of the blood-brain barrier for insulin. Br. Res. 896:36-42.
77. Yan, E., Castillo-Melendez, M., Nicholls, T., Hirst, J., and Walker, D. 2004a. Cerebrovascular responses in the fetal sheep brain to low-dose endotoxin. Pediatr. Res. 55:855-863.
78. Yan, S. R., Qing, G., Byers, D. M., Stadnyk, A. W., Al-Hertani, W., and Bortolussi, R. 2004b. Role of MyD88 in diminished tumor necrosis factor alpha production by newborn mononuclear cells in response to lipopolysaccharide. Infect. Immunity 72:1223-1229.
79. Youakim, A., and Ahdieh, M. 1999. Interferon-γ decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin. Am. J. Physiol. Gastrointest. Liver Physiol. 276:G1279-G1288.
80. Zysk, G., Schneider-Wald, B. K., Hwang, J. H., Bejo, L., Kim, K. S., Mitchell, T. J., Hakenbeck, R., and Heinz, H. P. 2001. Pneumolysin is the main inducer of cytotoxicity to brain microvascular endothelial cells caused by Streptococcus pneumoniae. Infect. Immunity. 69:845-852.