Type III Protein Secretion Systems in Bacterial Pathogens of Animals and Plants

Microbiology and Molecular Biology Reviews - Tập 62 Số 2 - Trang 379-433 - 1998
Christoph J. Hueck1
1Lehrstuhl für Mikrobiologie, Biozentrum der Universität Würzburg, 97074 Würzburg, Germany

Tóm tắt

SUMMARY

Various gram-negative animal and plant pathogens use a novel, sec-independent protein secretion system as a basic virulence mechanism. It is becoming increasingly clear that these so-called type III secretion systems inject (translocate) proteins into the cytosol of eukaryotic cells, where the translocated proteins facilitate bacterial pathogenesis by specifically interfering with host cell signal transduction and other cellular processes. Accordingly, some type III secretion systems are activated by bacterial contact with host cell surfaces. Individual type III secretion systems direct the secretion and translocation of a variety of unrelated proteins, which account for species-specific pathogenesis phenotypes. In contrast to the secreted virulence factors, most of the 15 to 20 membrane-associated proteins which constitute the type III secretion apparatus are conserved among different pathogens. Most of the inner membrane components of the type III secretion apparatus show additional homologies to flagellar biosynthetic proteins, while a conserved outer membrane factor is similar to secretins from type II and other secretion pathways. Structurally conserved chaperones which specifically bind to individual secreted proteins play an important role in type III protein secretion, apparently by preventing premature interactions of the secreted factors with other proteins. The genes encoding type III secretion systems are clustered, and various pieces of evidence suggest that these systems have been acquired by horizontal genetic transfer during evolution. Expression of type III secretion systems is coordinately regulated in response to host environmental stimuli by networks of transcription factors. This review comprises a comparison of the structure, function, regulation, and impact on host cells of the type III secretion systems in the animal pathogens Yersinia spp., Pseudomonas aeruginosa, Shigella flexneri, Salmonella typhimurium, enteropathogenic Escherichia coli, and Chlamydia spp. and the plant pathogens Pseudomonas syringae, Erwinia spp., Ralstonia solanacearum, Xanthomonas campestris, and Rhizobium spp.

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Tài liệu tham khảo

10.1016/0022-2836(85)90402-4

10.1083/jcb.129.2.367

10.1002/j.1460-2075.1996.tb00696.x

10.1111/j.1365-2958.1989.tb00210.x

10.1046/j.1365-2958.1996.344874.x

10.1128/jb.173.11.3573-3579.1991

10.1046/j.1365-2958.1996.415946.x

10.1128/iai.61.5.1707-1714.1993

10.1111/j.1365-2958.1992.tb00885.x

10.1111/j.1365-2958.1995.mmi_17030461.x

10.1128/jb.174.23.7661-7669.1992

10.1111/j.1365-2958.1993.tb01097.x

10.1128/jb.177.15.4230-4237.1995

10.1111/j.1365-2958.1995.mmi_18020343.x

10.1128/jb.176.15.4534-4542.1994

10.1128/iai.63.11.4456-4462.1995

10.1111/j.1365-2958.1993.tb01100.x

10.1016/S0022-2836(05)80360-2

10.1126/science.278.5340.1140

10.1111/j.1365-2958.1996.tb02546.x

10.1128/iai.59.6.1997-2005.1991

10.1128/iai.60.8.3287-3295.1992

10.1128/iai.63.4.1541-1551.1995

Arakawa E. Kato J.-I. Ito K.-I. Watanabe H. Comparison and high conservation of nucleotide sequences of spa-mxi regions between S. sonnei and S. flexneri—identification of a new gene coding plausible membrane protein. 1995GenBank accession no. D50601

10.1094/MPMI-5-187

10.1002/j.1460-2075.1994.tb06292.x

10.1111/j.1365-2958.1995.mmi_18040715.x

10.1046/j.1365-2958.1996.d01-1718.x

10.1126/science.276.5313.726

10.1128/iai.59.5.1599-1604.1991

10.1128/jb.172.8.4661-4671.1990

10.1016/0882-4010(88)90062-9

Baudry B. Maurelli A. T. Clerc P. Sadoff J. C. Sansonetti P. J. Localization of plasmid loci necessary for the entry of Shigella flexneri into HeLa cells, and characterization of one locus encoding four immunogenic polypeptides.J. Gen. Microbiol.133198734033413

10.1094/MPMI-8-0484

10.1016/S0966-842X(97)01082-2

10.1073/pnas.93.1.279

10.1128/iai.65.6.2254-2259.1997

10.1128/jb.175.14.4475-4484.1993

10.1016/0147-619X(81)90019-6

10.1128/jb.176.9.2619-2626.1994

10.1128/jb.173.5.1607-1616.1991

10.1128/jb.172.11.6274-6281.1990

10.1139/m92-138

10.1128/iai.63.4.1270-1277.1995

10.1128/iai.62.11.4900-4908.1994

10.1111/j.1365-2958.1992.tb01448.x

10.1128/jb.174.12.4017-4025.1992

10.1093/emboj/16.10.2730

10.1128/iai.63.2.681-685.1995

10.1084/jem.176.6.1625

10.1073/pnas.88.4.1187

10.1128/iai.62.2.606-614.1994

10.1093/clinids/5.2.279

10.1046/j.1365-2958.1996.5731077.x

10.1128/jb.178.6.1720-1730.1996

10.1002/j.1460-2075.1996.tb00904.x

10.1128/iai.56.2.343-348.1988

10.1128/iai.48.1.234-240.1985

10.1111/j.1365-2958.1988.tb00025.x

Bonas U. hrp genes of phytopathogenic bacteria.Curr. Top. Microbiol. Immunol.19219947998

10.1094/MPMI-4-081

10.1128/jb.169.12.5626-5632.1987

10.1128/jb.179.6.1985-1991.1997

10.1016/0092-8674(92)90530-P

10.1016/0922-3371(90)90048-2

Burrows T. Bacon G. A. The basis of virulence in Pasteurella pestis: an antigen determinig virulence.Br. J. Exp. Pathol.371956481493

10.1128/jb.169.6.2561-2569.1987

10.1016/0882-4010(90)90047-T

10.1111/j.1365-2958.1993.tb01164.x

10.1016/0378-1119(93)90014-T

10.1084/jem.139.5.1189

10.1128/jb.179.12.3866-3874.1997

10.1126/science.274.5295.2115

10.1046/j.1365-2958.1996.471410.x

10.1002/j.1460-2075.1996.tb00759.x

10.1046/j.1365-2958.1997.3831750.x

10.1128/jb.178.4.1232-1236.1996

10.1126/science.7716514

10.1016/0923-2508(94)90031-0

Coburn J. Pseudomonas aeruginosa exoenzyme S.Curr. Top. Microbiol. Immunol.1751992133143

10.1016/S0021-9258(18)38137-7

10.1128/iai.64.9.3524-3531.1996

10.1046/j.1365-2958.1997.3781740.x

10.1111/j.1365-2958.1995.tb02218.x

Collmer A. Bauer D. W. Erwinia chrysanthemi and Pseudomonas syringae: plant pathogens trafficking in extracellular virulence proteins.Curr. Top. Microbiol. Immunol.19219944378

10.1093/clinids/9.1.64

10.1128/jb.171.1.254-262.1989

10.1016/0882-4010(86)90067-7

10.1016/0882-4010(87)90078-7

Cornelis G. R. Personal communication.

10.1111/j.1365-2958.1989.tb00129.x

10.1111/j.1365-2958.1991.tb01875.x

10.1128/iai.64.12.5075-5084.1996

10.1002/j.1460-2075.1995.tb07244.x

10.1111/j.1365-2958.1994.tb01262.x

10.1016/S0021-9258(18)71517-2

10.1111/j.1365-2958.1992.tb01489.x

Donaldson R. M. J. The relation of enteric bacterial populations to gastrointestinal function and disease Gastrointestinal disease: pathophysiology diagnosis and management. Sleisinger M. H. Fordtran J. S. 1978 79 92 The W. B. Saunders Co. Philadelphia Pa

10.1111/j.1365-2958.1993.tb00930.x

10.1128/iai.58.6.1565-1571.1990

10.1128/IAI.59.12.4310-4317.1991

10.1128/iai.60.10.3953-3961.1992

10.1016/S0966-842X(97)01000-7

10.1016/S0378-1119(96)00581-1

10.1128/jb.175.15.4670-4680.1993

10.1111/j.1365-2958.1992.tb00879.x

10.1038/344789a0

10.1016/0022-2836(90)90063-R

10.1128/jb.176.15.4501-4510.1994

Eichelberg K. Kaniga K. Galán J. E. Transcriptional regulation of Salmonella secreted virulence determinants abstr. B-40.Abstracts of the 96th General Meeting of the American Society for Microbiology 1996.1996American Society for MicrobiologyWashington D.C

10.1073/pnas.86.13.5173

10.1128/iai.58.6.2014-2016.1990

Falkow S. Personal communication.

10.1128/iai.63.8.3117-3124.1995

10.1074/jbc.271.50.31981

10.1128/mr.57.4.995-1017.1993

10.1094/MPMI-5-390

10.1094/MPMI-8-0845

10.1128/iai.31.2.839-841.1981

10.1128/jb.176.3.569-579.1994

10.1073/pnas.83.14.5189

10.1046/j.1365-2958.1997.4891851.x

10.1016/0300-9084(88)90271-4

10.1128/mmbr.61.2.136-169.1997

10.1128/iai.60.6.2541-2543.1992

10.1242/jcs.99.2.283

10.1111/j.1365-2958.1988.tb00087.x

10.1016/S0021-9258(19)86105-7

10.1146/annurev.py.09.090171.001423

10.1016/0882-4010(87)90104-5

10.1111/j.1365-2958.1991.tb00773.x

10.1111/j.1365-2958.1988.tb00013.x

10.1128/jb.172.3.1547-1555.1990

10.1128/iai.62.7.3038-3040.1994

10.1084/jem.179.3.993

10.1111/j.1365-2958.1992.tb01765.x

10.1046/j.1365-2958.1997.6251991.x

10.1128/jb.173.20.6460-6468.1991

10.1128/iai.62.2.554-563.1994

10.1111/j.1365-2958.1993.tb01709.x

10.1038/387394a0

10.1046/j.1365-2958.1997.5411905.x

10.1111/j.1365-2958.1995.tb02426.x

10.1073/pnas.90.6.2320

10.1073/pnas.86.16.6383

10.1128/iai.58.6.1879-1885.1990

10.1128/iai.59.9.2901-2908.1991

10.1128/jb.174.13.4338-4349.1992

Galán J. E. Sansonetti P. J. Molecular and cellular bases of Salmonella and Shigella interactions with host cells Escherichia coli and Salmonella: cellular and molecular biology 2nd ed. Neidhardt F. C. Curtiss R. III Ingraham J. L. Lin E. C. C. Low K. B. Magasanik B. Riley M. Reznikoff W. S. Schaechter M. Umbarger H. E. 1996 2757 2773 ASM Press Washington D.C

10.1093/nar/21.4.807

10.1038/361730a0

10.1128/jb.176.15.4543-4548.1994

10.1111/j.1365-2958.1997.mmi525.x

10.1016/S0092-8674(00)81003-X

10.1128/iai.27.2.682-685.1980

10.1128/iai.28.3.1044-1047.1980

10.1111/j.1365-2958.1992.tb01764.x

10.1073/pnas.89.13.5976

10.1128/iai.63.2.729-732.1995

10.1016/0092-8674(94)90510-X

10.1128/iai.65.4.1267-1272.1997

10.1128/jb.160.3.842-848.1984

10.1128/iai.63.5.1767-1776.1995

Gopalan S. Bauer D. W. Alfano J. R. Loniello A. O. He S. Y. Collmer A. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death.Plant Cell8199610951105

10.1094/MPMI-5-384

10.1016/S0968-0004(96)30040-6

10.1016/S0021-9258(17)41945-4

10.1111/j.1365-2958.1995.tb02230.x

10.1128/jb.171.9.5031-5038.1989

10.1002/j.1460-2075.1993.tb06056.x

10.1126/science.2166336

10.1046/j.1365-2958.1997.3101672.x

10.1016/S0966-842X(97)01061-5

10.1128/jb.174.14.4820-4828.1992

10.1128/iai.61.1.71-80.1993

10.1046/j.1365-2958.1996.5251051.x

10.1002/j.1460-2075.1996.tb00968.x

10.1128/iai.50.3.620-629.1985

10.1128/iai.40.1.340-350.1983

10.1126/science.3291115

10.1128/iai.57.3.673-678.1989

10.1128/iai.59.3.1106-1111.1991

10.1002/j.1460-2075.1996.tb00434.x

10.1046/j.1365-2958.1996.01539.x

10.1073/pnas.94.18.9887

10.1128/iai.37.3.1295-1298.1982

10.1111/j.1365-2958.1994.tb00408.x

10.1128/iai.62.10.4445-4453.1994

10.1128/jb.172.4.1905-1915.1990

10.1016/0092-8674(93)90354-S

He X.-T. Krishnan H. B. Pueppke S. G. Genes controlling cultivar-specific nodulation of soybean by Rhizobium fredii are homologous genes encoding type III secretion systems in other bacteria. 1997GenBank accession no. L12251

10.1128/iai.46.1.105-110.1984

10.1128/iai.54.2.561-567.1986

10.1111/j.1574-6968.1987.tb01978.x

10.1093/infdis/147.1.107

Hensel M. Personal communication.

10.1128/jb.179.4.1105-1111.1997

10.1126/science.7618105

10.1046/j.1365-2958.1997.3271699.x

10.1111/j.1365-2958.1995.mmi_17040781.x

10.1016/0092-8674(88)90470-9

10.1111/j.1365-2958.1990.tb00559.x

10.1002/j.1460-2075.1992.tb05253.x

10.1128/jb.77.3.317-321.1959

10.1128/jb.176.17.5439-5449.1994

10.1111/j.1365-2958.1993.tb01949.x

10.1128/jb.174.13.4275-4286.1992

10.1046/j.1365-2958.1997.3211681.x

10.1128/iai.63.6.2269-2276.1995

Hook E. W. Salmonella species (including typhoid fever) Principles and practice and infectious diseases 3rd ed. Mandell G. L. Douglas R. G. Jr. Bennett J. E. 1990 1700 1716 Churchill Livingstone Inc. New York N.Y

10.1128/jb.177.15.4427-4436.1995

10.1128/iai.57.10.2963-2970.1989

10.1111/j.1365-2958.1992.tb01385.x

10.1046/j.1365-2958.1997.4701834.x

10.1128/jb.174.21.6878-6885.1992

10.1094/MPMI-8-0733

10.1128/jb.170.10.4748-4756.1988

10.1094/MPMI-6-515

10.1111/j.1365-2958.1995.mmi_18030479.x

10.1126/science.8235660

10.1016/0092-8674(90)90458-Q

10.1128/jb.174.6.1923-1931.1992

10.1016/0092-8674(92)90115-S

10.1073/pnas.75.7.3211

10.1128/jb.175.15.4859-4869.1993

10.1073/pnas.92.17.7996

Jepson M. A. Personal communication.

10.1128/iai.59.11.3869-3875.1991

10.1073/pnas.87.20.7839

10.1046/j.1365-2958.1996.d01-1719.x

10.1128/iai.62.9.3745-3752.1994

10.1084/jem.180.1.15

10.1128/jb.171.7.3890-3900.1989

10.1128/jb.172.3.1327-1339.1990

10.1046/j.1365-2958.1997.4311793.x

10.1111/j.1365-2958.1994.tb00450.x

10.1128/jb.177.24.7078-7085.1995

10.1128/jb.177.14.3965-3971.1995

10.1111/j.1365-2958.1996.tb02571.x

10.1128/iai.57.5.1391-1398.1989

10.1006/jmbi.1994.1280

10.1128/iai.65.7.2606-2612.1997

10.1016/S0092-8674(00)80437-7

10.1073/pnas.92.17.7991

10.1128/iai.65.7.2528-2536.1997

10.1111/j.1365-2958.1996.tb02619.x

10.1128/jb.171.6.3247-3257.1989

10.1128/jb.179.5.1690-1697.1997

Klement Z. Hypersensitivity Phythopathogenic prokaryotes. Mount M. S. Lacy G. H. 1982 149 177 Academic Press Inc. New York N.Y

10.1128/jb.168.1.22-30.1986

10.1128/jb.173.22.7142-7150.1991

10.1128/iai.57.4.1290-1298.1989

10.1111/j.1348-0421.1986.tb03055.x

10.1111/j.1365-2958.1994.tb01268.x

10.1016/0022-2836(92)90958-M

10.1128/jb.179.3.813-817.1997

10.1016/S0021-9258(17)34078-4

10.1128/jb.166.3.1007-1012.1986

10.1128/jb.76.1.120-121.1958

10.1128/jb.176.24.7625-7629.1994

10.1073/pnas.86.13.4953

10.1128/jb.88.5.1503-1518.1964

10.1128/iai.65.6.2211-2217.1997

10.1016/0092-8674(94)90106-6

10.1111/j.1365-2958.1992.tb01483.x

Lawton W. D. Erdman R. L. Surgalla M. J. Biosynthesis and purification of V and W antigen in Pasteurella pestis.J. Immunol.911963179184

10.1128/iai.63.8.2854-2858.1995

10.1016/S0966-842X(97)01029-9

10.1073/pnas.87.11.4304

10.1073/pnas.89.5.1847

10.1073/pnas.93.26.15497

10.1128/iai.58.10.3262-3271.1990

10.1128/jb.171.9.4623-4632.1989

10.1093/oxfordjournals.epirev.a036274

10.1073/pnas.92.16.7252

10.1128/jb.174.6.1742-1749.1992

10.1073/pnas.91.2.489

10.1094/MPMI-7-0488

10.1016/0264-410X(93)90014-O

10.1128/jb.168.2.512-522.1986

10.1016/0966-842X(93)90088-9

10.1073/pnas.91.16.7573

10.1146/annurev.ge.26.120192.001023

Macnab R. M. Flagella and motility Escherichia coli and Salmonella: cellular and molecular biology 2nd ed. Neidhardt F. C. Curtiss R. III Ingraham J. L. Lin E. C. C. Low K. B. Magasanik B. Riley M. Reznikoff W. S. Schaechter M. Umbarger H. E. 1996 123 145 ASM Press Washington D.C

10.1128/iai.59.12.4465-4472.1991

10.1128/jb.176.1.189-197.1994

10.1128/jb.171.5.2728-2734.1989

10.1128/iai.65.1.110-115.1997

10.1016/0140-6736(92)90340-9

10.1128/iai.64.10.4182-4187.1996

10.1126/science.7902614

10.1111/j.1365-2958.1993.tb01744.x

10.1006/jmbi.1996.0109

10.1128/iai.49.1.164-171.1985

Maurelli A. T. Hromockyj A. E. Bernardini M. L. Environmental regulation of Shigella virulence.Curr. Top. Microbiol. Immunol.180199295116

10.1146/annurev.mi.42.100188.001015

10.1073/pnas.85.8.2820

10.1128/iai.48.3.676-685.1985

10.1128/iai.63.6.2302-2309.1995

10.1073/pnas.92.5.1664

10.1046/j.1365-2958.1997.2311591.x

10.1016/0167-4781(94)90040-X

10.1111/j.1365-2958.1993.tb01665.x

10.1016/0966-842X(96)10039-1

10.1073/pnas.93.3.1254

10.1002/j.1460-2075.1994.tb06863.x

10.1016/0092-8674(94)90260-7

10.1128/JB.175.18.5899-5906.1993

10.1016/0882-4010(88)90006-X

10.1128/jb.173.5.1677-1685.1991

10.1128/jb.173.16.4994-5009.1991

10.1128/iai.58.9.2840-2849.1990

Miller S. I. Personal communication.

Miller S. I. Hohmann E. L. Pegues D. A. Salmonella (including Salmonella typhi) Principles and practice of infectious diseases Mandell G. L. Bennett J. E. Raphael D. 2 1995 2013 2033 Churchill Livingstone, Inc. New York, N.Y

10.1073/pnas.86.13.5054

10.1128/jb.172.5.2485-2490.1990

10.1111/j.1365-2958.1995.tb02382.x

10.1073/pnas.94.23.12638

10.1128/jb.176.24.7630-7637.1994

10.1073/pnas.93.18.9833

10.1128/iai.41.3.1340-1351.1983

10.1128/iai.62.10.4192-4201.1994

10.1128/iai.64.10.4313-4318.1996

10.1128/mr.55.1.143-190.1991

10.1128/iai.65.2.774-782.1997

10.1128/iai.57.8.2534-2541.1989

Mullan P. B. A. V. Gautier M. W. Wood M. H. Edwards B. V. Jones and E. E. Galyov. Sip invasins of Salmonella dublin are involved in macrophage cytotoxicity and mouse virulence. GenBank accession no. U66877

Murphy C. K. Beckwith J. Export of proteins to the cell envelope in Escherichia coli Escherichia coli and Salmonella: cellular and molecular biology 2nd ed. Neidhardt F. C. Curtiss R. III Ingraham J. L. Lin E. C. C. Low K. B. Magasanik B. Riley M. Reznikoff W. S. Schaechter M. Umbarger H. E. 1996 967 978 ASM Press Washington D.C

10.1128/iai.61.1.23-31.1993

10.1128/iai.63.8.3021-3029.1995

10.1128/jb.177.17.5062-5069.1995

10.1093/infdis/152.4.716

10.1139/m85-074

10.1128/jb.179.4.1307-1316.1997

10.1128/iai.53.1.57-63.1986

10.1128/iai.25.2.513-520.1979

Ochman H. Lawrence J. G. Pholygenetics and the amelioration of bacterial genomes Escherichia coli and Salmonella: cellular and molecular biology 2nd ed. Neidhardt F. C. Curtiss R. III Ingraham J. L. Lin E. C. C. Low K. B. Magasanik B. Riley M. Reznikoff W. S. Schaechter M. Umbarger H. E. 1996 2627 2637 ASM Press Washington D.C

10.1073/pnas.93.15.7800

10.1046/j.1365-2958.1997.4901850.x

10.1016/S0966-842X(00)88937-4

10.1016/S0968-0004(97)01089-X

10.1111/j.1365-2958.1995.tb02301.x

Parsot C. Sansonetti P. J. Invasion and the pathogenesis of Shigella infections.Curr. Top. Microbiol. Immunol.20919962542

10.1111/j.1365-2958.1995.mmi_17010169.x

10.1046/j.1365-2958.1997.3741745.x

10.1172/JCI117015

10.1084/jem.180.4.1307

10.1128/iai.54.2.428-434.1986

10.1093/emboj/16.9.2307

10.1111/j.1365-2958.1995.mmi_18010135.x

10.1126/science.273.5279.1231

Petterson J. Nordfelth R. Wolf-Watz H. Contact with eukaryotic cells: a new signal triggering bacterial gene expression. Response to G. R. Cornelis. 1997Trends Microbiol. 5: 44–45.

10.1094/MPMI-9-0252

10.1128/jb.173.22.7293-7303.1991

10.1128/jb.175.11.3536-3545.1993

10.1128/jb.177.13.3843-3854.1995

10.1128/iai.63.9.3642-3648.1995

Popoff M. Personal communication.

10.1128/jb.176.13.4187-4191.1994

10.1093/infdis/148.2.297

10.1128/iai.31.2.775-782.1981

10.1128/iai.43.1.108-114.1984

10.1094/MPMI-8-0717

10.1128/jb.173.8.2649-2657.1991

10.1128/jb.171.10.5646-5653.1989

10.1128/iai.57.5.1491-1498.1989

10.1111/j.1365-2958.1996.tb02491.x

10.1128/MR.57.1.50-108.1993

10.1094/MPMI.1997.10.2.247

10.1006/mpat.1996.0051

10.1128/jb.173.2.575-586.1991

10.1128/jb.174.11.3499-3507.1992

10.1038/347685a0

10.1128/iai.60.12.5242-5252.1992

10.1126/science.8438166

10.1128/jb.174.10.3355-3363.1992

10.1046/j.1365-2958.1997.3371700.x

10.1111/j.1365-2958.1995.tb02371.x

10.1111/j.1365-2958.1994.tb01008.x

10.1073/pnas.94.7.3459

Rooney P. J. T. L. Yahr and D. W. Frank. Genbank accession no. AF010151

10.1002/j.1460-2075.1992.tb05438.x

10.1128/iai.64.3.966-973.1996

10.1002/j.1460-2075.1996.tb00621.x

10.1128/iai.56.8.2139-2143.1988

10.1128/iai.59.12.4562-4569.1991

10.1111/j.1365-2958.1990.tb00635.x

10.1002/j.1460-2075.1995.tb00092.x

10.1002/j.1460-2075.1994.tb06341.x

10.1016/0882-4010(86)90047-1

10.1111/j.1365-2958.1994.tb01296.x

10.1016/S0966-842X(00)88929-5

10.1128/jb.175.13.3998-4007.1993

10.1128/iai.54.2.395-402.1986

10.1111/j.1365-2958.1988.tb00067.x

10.1007/BF00281595

10.1016/0968-0004(93)90080-7

10.1016/0882-4010(87)90057-X

10.1128/iai.64.7.2752-2764.1996

10.1016/S0769-2609(83)80056-8

10.1128/iai.39.3.1392-1402.1983

10.1128/iai.34.1.75-83.1981

10.1128/iai.35.3.852-860.1982

10.1128/iai.51.2.461-469.1986

10.1111/j.1365-2958.1989.tb00269.x

10.1128/jb.170.6.2480-2484.1988

10.1128/jb.175.8.2334-2346.1993

10.1128/iai.54.1.32-36.1986

10.1128/iai.45.2.534-536.1984

10.1128/jb.178.24.7227-7233.1996

10.1128/iai.59.1.437-440.1991

10.1128/jb.176.2.368-377.1994

10.1128/iai.64.6.2106-2113.1996

10.1126/science.274.5295.2063

10.1152/physrev.1988.68.1.177

10.1073/pnas.93.6.2593

10.1016/0966-842X(96)81501-0

10.1128/iai.58.3.841-845.1990

10.1128/jb.175.11.3520-3528.1993

10.1128/jb.177.9.2530-2542.1995

10.1128/iai.47.1.183-190.1985

10.1128/iai.56.10.2743-2748.1988

10.1128/iai.56.10.2749-2752.1988

10.1126/science.1439793

10.1002/pro.5560030314

10.1073/pnas.92.26.11998

10.1111/j.1365-2958.1994.tb02191.x

10.1046/j.1365-2958.1997.6281995.x

Staley T. E. Jones E. W. Corley L. D. Attachment and penetration of Escherichia coli into intestinal epithelium of the ileum in newborn pigs.Am. J. Pathol.561969371392

10.1126/science.7732374

Stock J. B. Surette M. G. Levit M. Park P. Two-component signal transduction systems: structure-function relationships and mechanisms of catalysis Two-component signal transduction. Hoch J. A. Silhavy T. J. 1995 25 51 ASM Press Washington D.C

10.1128/jb.174.12.3945-3952.1992

10.1093/cid/10.Supplement_2.S323

10.1073/pnas.78.2.1224

10.1128/iai.57.4.1200-1210.1989

10.1111/j.1365-2958.1993.tb01644.x

10.1128/iai.61.8.3105-3110.1993

10.1016/0092-8674(93)90047-T

10.1038/326607a0

Takeuchi A. Electron microscopic studies of experimental Salmonella infection I. Penetration into the intestinal epithelium by Salmonella typhimurium.Am. J. Pathol.501967109136

Takeuchi A. Formal S. B. Sprinz H. Experimental acute colitis in the rhesus monkey following peroral infection with Shigella flexneri. An electron microscope study.Am. J. Pathol.521968503529

10.1126/science.274.5295.2060

10.1128/iai.65.2.787-793.1997

10.1111/j.1365-2958.1991.tb00762.x

10.1046/j.1365-2958.1996.531415.x

10.1128/jb.175.19.6142-6149.1993

10.1128/jb.177.4.1094-1097.1995

10.1093/emboj/16.10.2717

10.1111/j.1365-2958.1995.mmi_17020241.x

10.1016/0022-2836(92)90216-7

10.1006/jmbi.1994.1164

10.1016/S0092-8674(00)81825-5

10.1016/0966-842X(93)90087-8

10.1111/j.1365-2958.1995.tb02284.x

10.1128/AAC.16.6.743

10.1073/pnas.85.23.9317

10.1093/nar/18.6.1648

10.1128/jb.174.6.1990-2001.1992

10.1016/0092-8674(93)90135-D

10.1128/jb.172.6.3152-3162.1990

10.1099/00221287-143-3-693

10.1128/jb.173.11.3564-3572.1991

10.1016/0304-4173(84)90003-X

10.1002/j.1460-2075.1982.tb01276.x

Wandersman C. Secretion across the bacterial outer membrane Escherichia coli and Salmonella: cellular and molecular biology 2nd ed. Neidhardt F. C. Curtiss R. III Ingraham J. L. Lin E. C. C. Low K. B. Magasanik B. Riley M. Reznikoff W. S. Schaechter M. Umbarger H. E. 1996 955 966 ASM Press Washington D.C

10.1128/iai.57.3.858-863.1989

10.1128/jb.172.2.619-629.1990

10.1084/jem.183.3.991

10.1084/jem.185.2.281

10.1002/j.1460-2075.1995.tb07243.x

10.1073/pnas.92.11.4927

10.1073/pnas.91.22.10493

10.1111/j.1365-2958.1993.tb01209.x

10.1128/jb.176.13.3878-3884.1994

10.1111/j.1365-2958.1996.tb02614.x

10.1128/jb.175.24.7958-7967.1993

10.1128/jb.177.21.6201-6210.1995

10.1126/science.1621099

10.1128/jb.174.6.1875-1882.1992

Weksler B. B. Platelets Inflammation: basic principles and clinical correlates. Gallin J. I. Goldstein I. M. Snyderman R. 1988 543 557 Raven Press New York N.Y

10.1111/j.1365-2958.1991.tb00723.x

10.1128/jb.178.12.3462-3469.1996

10.1128/jb.178.4.1061-1069.1996

10.1094/MPMI-9-0704

10.1094/MPMI-6-616

10.1128/jb.178.10.2960-2970.1996

10.1016/0966-842X(96)81513-7

10.1128/jb.176.6.1561-1569.1994

10.1111/j.1365-2958.1996.tb02645.x

10.1128/iai.48.1.241-243.1985

10.1046/j.1365-2958.1996.00116.x

Wu H. C. Tokunaga M. Biogenesis of lipoproteins in bacteria.Curr. Top. Microbiol. Immunol.1251986127157

10.1128/jb.176.4.1025-1036.1994

10.1128/jb.176.10.3089-3091.1994

10.1128/jb.174.6.1734-1741.1992

10.1128/jb.176.13.3832-3838.1994

10.1046/j.1365-2958.1996.01554.x

10.1128/jb.177.5.1169-1178.1995

10.1128/jb.179.22.7165-7168.1997

10.1111/j.1365-2958.1991.tb02151.x

10.1128/iai.60.3.1163-1169.1992

10.1016/S0021-9258(18)33981-4

10.1128/jb.165.2.443-447.1986

10.1128/jb.164.2.704-711.1985

10.1128/jb.178.21.6399-6402.1996

10.1128/jb.139.3.792-799.1979

10.1016/S0021-9258(18)35903-9

10.1006/jmbi.1996.0452

10.1006/jmbi.1995.0443

10.1016/0092-8674(95)90208-2

10.1038/283224a0

10.1172/JCI117452

10.1111/j.1365-2958.1994.tb00341.x

10.1111/j.1749-6632.1994.tb44249.x

10.1038/358167a0

10.1128/iai.64.12.5357-5365.1996