CcpA is important for growth and virulence of Enterococcus faecium

The collagen adhesin Acm was the first virulence determinant reported to be important for the pathogenesis of Enterococcus faecium in a rat infective endocarditis model. We had previously reported that there was a slight growth delay associated with acm allelic replacement (cat) mutant strain TX6051...

Celý popis

Uloženo v:
Podrobná bibliografie
Vydáno v:Infection and immunity Ročník 82; číslo 9; s. 3580
Hlavní autoři: Somarajan, Sudha R, Roh, Jung H, Singh, Kavindra V, Weinstock, George M, Murray, Barbara E
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States 01.09.2014
Témata:
ISSN:1098-5522, 1098-5522
On-line přístup:Zjistit podrobnosti o přístupu
Tagy: Přidat tag
Žádné tagy, Buďte první, kdo vytvoří štítek k tomuto záznamu!
Abstract The collagen adhesin Acm was the first virulence determinant reported to be important for the pathogenesis of Enterococcus faecium in a rat infective endocarditis model. We had previously reported that there was a slight growth delay associated with acm allelic replacement (cat) mutant strain TX6051 used in that study. Recently, we generated a nonpolar markerless acm deletion mutant and did not observe a delay in growth. We therefore performed comparative genome sequence analysis of wild-type strain TX82 and TX6051 and found a single mutation, a nonsense mutation in the ccpA gene of TX6051. After correcting this mutation, the growth defect of TX6051 was abolished, implicating a role for CcpA in the growth of E. faecium. To confirm this, we created a ccpA deletion mutant of TX82, which also exhibited a slight delay in growth. Furthermore, the ccpA deletion mutant was attenuated (P = 0.0024) in a mixed-inoculum (TX82 plus TX82 ΔccpA) rat endocarditis model and also in an in vitro competitive growth assay; a ccpA-complemented strain showed neither reduced growth nor reduced virulence. We also found attenuation in the endocarditis model with the new acm deletion mutant although not as great as that previously observed with TX6051 carrying the ccpA mutation. Taken together, our data confirm the role of Acm in the pathogenesis of endocarditis. We also show that CcpA affects the growth of E. faecium, that an intact ccpA gene is important for full virulence, and that a ccpA mutation was partly responsible for the highly attenuated phenotype of TX6051.
AbstractList The collagen adhesin Acm was the first virulence determinant reported to be important for the pathogenesis of Enterococcus faecium in a rat infective endocarditis model. We had previously reported that there was a slight growth delay associated with acm allelic replacement (cat) mutant strain TX6051 used in that study. Recently, we generated a nonpolar markerless acm deletion mutant and did not observe a delay in growth. We therefore performed comparative genome sequence analysis of wild-type strain TX82 and TX6051 and found a single mutation, a nonsense mutation in the ccpA gene of TX6051. After correcting this mutation, the growth defect of TX6051 was abolished, implicating a role for CcpA in the growth of E. faecium. To confirm this, we created a ccpA deletion mutant of TX82, which also exhibited a slight delay in growth. Furthermore, the ccpA deletion mutant was attenuated (P = 0.0024) in a mixed-inoculum (TX82 plus TX82 ΔccpA) rat endocarditis model and also in an in vitro competitive growth assay; a ccpA-complemented strain showed neither reduced growth nor reduced virulence. We also found attenuation in the endocarditis model with the new acm deletion mutant although not as great as that previously observed with TX6051 carrying the ccpA mutation. Taken together, our data confirm the role of Acm in the pathogenesis of endocarditis. We also show that CcpA affects the growth of E. faecium, that an intact ccpA gene is important for full virulence, and that a ccpA mutation was partly responsible for the highly attenuated phenotype of TX6051.
The collagen adhesin Acm was the first virulence determinant reported to be important for the pathogenesis of Enterococcus faecium in a rat infective endocarditis model. We had previously reported that there was a slight growth delay associated with acm allelic replacement (cat) mutant strain TX6051 used in that study. Recently, we generated a nonpolar markerless acm deletion mutant and did not observe a delay in growth. We therefore performed comparative genome sequence analysis of wild-type strain TX82 and TX6051 and found a single mutation, a nonsense mutation in the ccpA gene of TX6051. After correcting this mutation, the growth defect of TX6051 was abolished, implicating a role for CcpA in the growth of E. faecium. To confirm this, we created a ccpA deletion mutant of TX82, which also exhibited a slight delay in growth. Furthermore, the ccpA deletion mutant was attenuated (P = 0.0024) in a mixed-inoculum (TX82 plus TX82 ΔccpA) rat endocarditis model and also in an in vitro competitive growth assay; a ccpA-complemented strain showed neither reduced growth nor reduced virulence. We also found attenuation in the endocarditis model with the new acm deletion mutant although not as great as that previously observed with TX6051 carrying the ccpA mutation. Taken together, our data confirm the role of Acm in the pathogenesis of endocarditis. We also show that CcpA affects the growth of E. faecium, that an intact ccpA gene is important for full virulence, and that a ccpA mutation was partly responsible for the highly attenuated phenotype of TX6051.The collagen adhesin Acm was the first virulence determinant reported to be important for the pathogenesis of Enterococcus faecium in a rat infective endocarditis model. We had previously reported that there was a slight growth delay associated with acm allelic replacement (cat) mutant strain TX6051 used in that study. Recently, we generated a nonpolar markerless acm deletion mutant and did not observe a delay in growth. We therefore performed comparative genome sequence analysis of wild-type strain TX82 and TX6051 and found a single mutation, a nonsense mutation in the ccpA gene of TX6051. After correcting this mutation, the growth defect of TX6051 was abolished, implicating a role for CcpA in the growth of E. faecium. To confirm this, we created a ccpA deletion mutant of TX82, which also exhibited a slight delay in growth. Furthermore, the ccpA deletion mutant was attenuated (P = 0.0024) in a mixed-inoculum (TX82 plus TX82 ΔccpA) rat endocarditis model and also in an in vitro competitive growth assay; a ccpA-complemented strain showed neither reduced growth nor reduced virulence. We also found attenuation in the endocarditis model with the new acm deletion mutant although not as great as that previously observed with TX6051 carrying the ccpA mutation. Taken together, our data confirm the role of Acm in the pathogenesis of endocarditis. We also show that CcpA affects the growth of E. faecium, that an intact ccpA gene is important for full virulence, and that a ccpA mutation was partly responsible for the highly attenuated phenotype of TX6051.
Author Murray, Barbara E
Singh, Kavindra V
Weinstock, George M
Somarajan, Sudha R
Roh, Jung H
Author_xml – sequence: 1
  givenname: Sudha R
  surname: Somarajan
  fullname: Somarajan, Sudha R
  organization: Division of Infectious Diseases, Department of Internal Medicine, University of Texas Medical School at Houston, Houston, Texas, USA
– sequence: 2
  givenname: Jung H
  surname: Roh
  fullname: Roh, Jung H
  organization: Division of Infectious Diseases, Department of Internal Medicine, University of Texas Medical School at Houston, Houston, Texas, USA
– sequence: 3
  givenname: Kavindra V
  surname: Singh
  fullname: Singh, Kavindra V
  organization: Division of Infectious Diseases, Department of Internal Medicine, University of Texas Medical School at Houston, Houston, Texas, USA Center for the Study of Emerging and Re-Emerging Pathogens, University of Texas Medical School at Houston, Houston, Texas, USA
– sequence: 4
  givenname: George M
  surname: Weinstock
  fullname: Weinstock, George M
  organization: Jackson Laboratory for Genomic Medicine, Farmington, Connecticut, USA
– sequence: 5
  givenname: Barbara E
  surname: Murray
  fullname: Murray, Barbara E
  email: bem.asst@uth.tmc.edu
  organization: Division of Infectious Diseases, Department of Internal Medicine, University of Texas Medical School at Houston, Houston, Texas, USA Center for the Study of Emerging and Re-Emerging Pathogens, University of Texas Medical School at Houston, Houston, Texas, USA Department of Microbiology and Molecular Genetics, University of Texas Medical School at Houston, Houston, Texas, USA bem.asst@uth.tmc.edu
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24914215$$D View this record in MEDLINE/PubMed
BookMark eNpNj01LxDAURYOMOB-6cy1ZuumYlyaTdDkOoxYG3Oi6pK-JVtqkJq3iv1dwBDf3nsXlwF2SmQ_eEnIJbA3A9U25LdcMCoAMxAlZACt0JiXns388J8uU3hgDIYQ-I3MuChAc5ILc7nDY0jbRth9CHI0fqQuRvsTwOb5S4xv60capsx4tDY7u_WhjwIA4JeqMxXbqz8mpM12yF8dekee7_dPuITs83pe77SFDAWrMGmQ507XLEViNiFpJ6TZK58aBbFTthANmdG4FU8qopqmtkmjzGjQqu1F8Ra5_vUMM75NNY9W3CW3XGW_DlCqQMs85FD-xIlfH6VT3tqmG2PYmflV_v_k3Z-9a-w
CitedBy_id crossref_primary_10_1016_j_idc_2016_02_006
crossref_primary_10_1128_microbiolspec_GPP3_0055_2018
crossref_primary_10_1128_MMBR_00076_15
crossref_primary_10_1155_2018_1435820
crossref_primary_10_1038_srep32442
crossref_primary_10_1093_femsmc_xtae027
crossref_primary_10_1038_s41598_018_32558_0
crossref_primary_10_1093_femsmc_xtae018
crossref_primary_10_2478_am_2023_0014
crossref_primary_10_3389_fcimb_2021_667327
crossref_primary_10_1080_1062936X_2024_2434934
crossref_primary_10_1128_IAI_00885_15
crossref_primary_10_1093_infdis_jiw108
crossref_primary_10_1099_mgen_0_001160
crossref_primary_10_1128_JB_02288_14
crossref_primary_10_1038_s42003_023_04994_w
crossref_primary_10_3389_fcimb_2019_00411
crossref_primary_10_1128_spectrum_03724_23
crossref_primary_10_1128_spectrum_01289_25
crossref_primary_10_1016_j_jprot_2018_05_017
crossref_primary_10_1093_femsle_fnz256
ContentType Journal Article
Copyright Copyright © 2014, American Society for Microbiology. All Rights Reserved.
Copyright_xml – notice: Copyright © 2014, American Society for Microbiology. All Rights Reserved.
DBID CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1128/IAI.01911-14
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE
MEDLINE - Academic
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Medicine
Biology
EISSN 1098-5522
ExternalDocumentID 24914215
Genre Journal Article
Research Support, N.I.H., Extramural
GrantInformation_xml – fundername: NIAID NIH HHS
  grantid: R01 AI067861
– fundername: NHGRI NIH HHS
  grantid: U54 HG004968
GroupedDBID ---
-DZ
-~X
.55
.GJ
0R~
18M
29I
2WC
39C
3O-
4.4
41~
53G
5GY
5RE
5VS
85S
ABOCM
ACGFO
ADBBV
AENEX
AGCDD
AGVNZ
AI.
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BAWUL
BTFSW
C1A
CGR
CS3
CUY
CVF
D0S
DIK
DU5
E3Z
EBS
ECM
EIF
EJD
F5P
FRP
GX1
H13
HYE
HZ~
H~9
IH2
J5H
KQ8
L7B
MVM
NEJ
NPM
O9-
OHT
OK1
P2P
RHI
RNS
RPM
RSF
SJN
TR2
TWZ
UPT
VH1
W2D
W8F
WH7
WHG
WOQ
X7M
Y6R
ZGI
ZXP
~KM
7X8
AAGFI
ID FETCH-LOGICAL-c417t-dc0308bf3c10bccc8755f6783af15d7bf4f10a83e4077a7ddbe75ce3b18c7e672
IEDL.DBID 7X8
ISICitedReferencesCount 24
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000341932700007&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1098-5522
IngestDate Thu Sep 04 17:59:14 EDT 2025
Thu Apr 03 07:10:17 EDT 2025
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 9
Language English
License Copyright © 2014, American Society for Microbiology. All Rights Reserved.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c417t-dc0308bf3c10bccc8755f6783af15d7bf4f10a83e4077a7ddbe75ce3b18c7e672
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
OpenAccessLink https://iai.asm.org/content/iai/82/9/3580.full.pdf
PMID 24914215
PQID 1553321933
PQPubID 23479
ParticipantIDs proquest_miscellaneous_1553321933
pubmed_primary_24914215
PublicationCentury 2000
PublicationDate 2014-09-01
PublicationDateYYYYMMDD 2014-09-01
PublicationDate_xml – month: 09
  year: 2014
  text: 2014-09-01
  day: 01
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Infection and immunity
PublicationTitleAlternate Infect Immun
PublicationYear 2014
References 21299645 - Mol Microbiol. 2011 Feb;79(4):882-99
21266081 - BMC Microbiol. 2011;11(1):20
15292123 - J Bacteriol. 2004 Aug;186(16):5221-9
18947320 - Infect Control Hosp Epidemiol. 2008 Nov;29(11):996-1011
18591238 - Infect Immun. 2008 Sep;76(9):4110-9
16996131 - Plasmid. 2007 Mar;57(2):131-44
18832325 - Microbiology. 2008 Oct;154(Pt 10):3199-211
18223086 - J Bacteriol. 2008 Apr;190(7):2340-9
12552437 - J Infect Dis. 2003 Feb 1;187(3):508-12
9753005 - FEMS Immunol Med Microbiol. 1998 Aug;21(4):323-31
21109532 - Nucleic Acids Res. 2011 Jan;39(Database issue):D225-9
23447698 - J Infect Dis. 2013 Jun 1;207(11):1780-6
23974022 - J Bacteriol. 2013 Oct;195(20):4761-8
23963180 - MBio. 2013;4(4). pii: e00534-13. doi: 10.1128/mBio.00534-13
23274986 - J Microbiol. 2012 Dec;50(6):994-1002
24606170 - FEMS Microbiol Lett. 2014 Apr;353(2):151-6
7699051 - J Clin Microbiol. 1995 Jan;33(1):24-7
17257059 - PLoS Pathog. 2007 Jan;3(1):e7
18347047 - Infect Immun. 2008 May;76(5):2044-50
12622825 - Mol Microbiol. 2003 Mar;47(6):1733-47
21899450 - N Engl J Med. 2011 Sep 8;365(10):892-900
22421879 - Nat Rev Microbiol. 2012 Apr;10(4):266-78
20072611 - PLoS Pathog. 2010 Jan;6(1):e1000716
11004180 - J Bacteriol. 2000 Oct;182(20):5799-806
22989714 - Nucleic Acids Res. 2012 Nov;40(21):10701-18
14665673 - Microbiol Mol Biol Rev. 2003 Dec;67(4):475-90
22856458 - J Proteome Res. 2012 Sep 7;11(9):4654-61
18591236 - Infect Immun. 2008 Sep;76(9):4120-8
20971911 - J Bacteriol. 2011 Jan;193(1):52-62
15155680 - Infect Immun. 2004 Jun;72(6):3658-63
10706902 - N Engl J Med. 2000 Mar 9;342(10):710-21
19821720 - J Infect Dis. 2009 Nov 15;200(10):1566-73
21964732 - Microbiology. 2011 Dec;157(Pt 12):3458-68
12618459 - J Bacteriol. 2003 Mar;185(6):1951-7
18230719 - Proc Natl Acad Sci U S A. 2008 Feb 5;105(5):1698-703
16321938 - J Bacteriol. 2005 Dec;187(24):8340-9
23209408 - PLoS Pathog. 2012;8(11):e1003033
19193843 - J Clin Microbiol. 2009 Apr;47(4):896-901
16569828 - Antimicrob Agents Chemother. 2006 Apr;50(4):1183-94
16391062 - Appl Environ Microbiol. 2006 Jan;72(1):334-45
18765726 - Infect Immun. 2008 Nov;76(11):4944-51
23882129 - Genome Biol Evol. 2013;5(8):1524-35
9003306 - Mol Gen Genet. 1996 Nov 27;253(1-2):217-24
11265956 - Lancet. 2001 Mar 17;357(9259):853-5
23447697 - J Infect Dis. 2013 Jun 1;207(11):1633-6
References_xml – reference: 19821720 - J Infect Dis. 2009 Nov 15;200(10):1566-73
– reference: 21964732 - Microbiology. 2011 Dec;157(Pt 12):3458-68
– reference: 15155680 - Infect Immun. 2004 Jun;72(6):3658-63
– reference: 21266081 - BMC Microbiol. 2011;11(1):20
– reference: 7699051 - J Clin Microbiol. 1995 Jan;33(1):24-7
– reference: 12622825 - Mol Microbiol. 2003 Mar;47(6):1733-47
– reference: 17257059 - PLoS Pathog. 2007 Jan;3(1):e7
– reference: 21899450 - N Engl J Med. 2011 Sep 8;365(10):892-900
– reference: 14665673 - Microbiol Mol Biol Rev. 2003 Dec;67(4):475-90
– reference: 23447698 - J Infect Dis. 2013 Jun 1;207(11):1780-6
– reference: 18832325 - Microbiology. 2008 Oct;154(Pt 10):3199-211
– reference: 22989714 - Nucleic Acids Res. 2012 Nov;40(21):10701-18
– reference: 10706902 - N Engl J Med. 2000 Mar 9;342(10):710-21
– reference: 16321938 - J Bacteriol. 2005 Dec;187(24):8340-9
– reference: 18765726 - Infect Immun. 2008 Nov;76(11):4944-51
– reference: 24606170 - FEMS Microbiol Lett. 2014 Apr;353(2):151-6
– reference: 9753005 - FEMS Immunol Med Microbiol. 1998 Aug;21(4):323-31
– reference: 18230719 - Proc Natl Acad Sci U S A. 2008 Feb 5;105(5):1698-703
– reference: 23209408 - PLoS Pathog. 2012;8(11):e1003033
– reference: 16569828 - Antimicrob Agents Chemother. 2006 Apr;50(4):1183-94
– reference: 23882129 - Genome Biol Evol. 2013;5(8):1524-35
– reference: 22856458 - J Proteome Res. 2012 Sep 7;11(9):4654-61
– reference: 23274986 - J Microbiol. 2012 Dec;50(6):994-1002
– reference: 18591238 - Infect Immun. 2008 Sep;76(9):4110-9
– reference: 18591236 - Infect Immun. 2008 Sep;76(9):4120-8
– reference: 23963180 - MBio. 2013;4(4). pii: e00534-13. doi: 10.1128/mBio.00534-13
– reference: 11004180 - J Bacteriol. 2000 Oct;182(20):5799-806
– reference: 16391062 - Appl Environ Microbiol. 2006 Jan;72(1):334-45
– reference: 23974022 - J Bacteriol. 2013 Oct;195(20):4761-8
– reference: 22421879 - Nat Rev Microbiol. 2012 Apr;10(4):266-78
– reference: 12618459 - J Bacteriol. 2003 Mar;185(6):1951-7
– reference: 18347047 - Infect Immun. 2008 May;76(5):2044-50
– reference: 21299645 - Mol Microbiol. 2011 Feb;79(4):882-99
– reference: 9003306 - Mol Gen Genet. 1996 Nov 27;253(1-2):217-24
– reference: 19193843 - J Clin Microbiol. 2009 Apr;47(4):896-901
– reference: 12552437 - J Infect Dis. 2003 Feb 1;187(3):508-12
– reference: 20072611 - PLoS Pathog. 2010 Jan;6(1):e1000716
– reference: 18223086 - J Bacteriol. 2008 Apr;190(7):2340-9
– reference: 15292123 - J Bacteriol. 2004 Aug;186(16):5221-9
– reference: 20971911 - J Bacteriol. 2011 Jan;193(1):52-62
– reference: 23447697 - J Infect Dis. 2013 Jun 1;207(11):1633-6
– reference: 21109532 - Nucleic Acids Res. 2011 Jan;39(Database issue):D225-9
– reference: 16996131 - Plasmid. 2007 Mar;57(2):131-44
– reference: 11265956 - Lancet. 2001 Mar 17;357(9259):853-5
– reference: 18947320 - Infect Control Hosp Epidemiol. 2008 Nov;29(11):996-1011
SSID ssj0014448
Score 2.2570221
Snippet The collagen adhesin Acm was the first virulence determinant reported to be important for the pathogenesis of Enterococcus faecium in a rat infective...
SourceID proquest
pubmed
SourceType Aggregation Database
Index Database
StartPage 3580
SubjectTerms Adhesins, Bacterial - genetics
Adhesins, Bacterial - metabolism
Amino Acid Sequence
Animals
Bacterial Adhesion - genetics
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Biofilms - growth & development
Endocarditis, Bacterial
Enterococcus faecium - genetics
Enterococcus faecium - metabolism
Molecular Sequence Data
Rats
Sequence Deletion - genetics
Virulence - genetics
Title CcpA is important for growth and virulence of Enterococcus faecium
URI https://www.ncbi.nlm.nih.gov/pubmed/24914215
https://www.proquest.com/docview/1553321933
Volume 82
WOSCitedRecordID wos000341932700007&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpZ3PS8MwFMeDOhUv_pi_5i8ieK1rm7RJTzKHwx02dlDYbSRpoj2snWs78L_3pe3YSRC89BYoj-Tl8_K-yRehBy0pdeModICOmUMjGTlcQTIM_NAIrXwdi9psgo3HfDqNJs2BW97IKtc5sUrUcabsGXnX-tsQWF6EPC2-HOsaZburjYXGNmoRQBkr6WLTTReBUlpfhYu4EwBorIXvPu8Oe8NHoBur56K_w2W1yQyO_vt7x-iwwUvcq-fDCdrSaRvt1YaT3220P2pa6afoua8WPZzkOJlXCJ4WGPgVf0BZXnxikcZ4lSzL6koSzgyuxAMZZE9V5tjGNynnZ-h98PLWf3UaQwVHUY8VTqzs6zTSEOW5UikFtUpgYLciwnhBzKShxnMFJxqqPCZYHEvNAqWJ9LhiOmT-OdpJs1RfImzzEg-iiMqQUCk0UE1gmK80dwPuCreD7tdxmsGEtV0IkeqszGebSHXQRR3s2aJ-WWMGtaBHAUKu_jD6Gh0AvNBa73WDWgaWq75Fu2pVJPnyrpoJ8B1PRj-rqbxV
linkProvider ProQuest
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=CcpA+is+important+for+growth+and+virulence+of+Enterococcus+faecium&rft.jtitle=Infection+and+immunity&rft.au=Somarajan%2C+Sudha+R&rft.au=Roh%2C+Jung+H&rft.au=Singh%2C+Kavindra+V&rft.au=Weinstock%2C+George+M&rft.date=2014-09-01&rft.eissn=1098-5522&rft.volume=82&rft.issue=9&rft.spage=3580&rft_id=info:doi/10.1128%2FIAI.01911-14&rft_id=info%3Apmid%2F24914215&rft_id=info%3Apmid%2F24914215&rft.externalDocID=24914215
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1098-5522&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1098-5522&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1098-5522&client=summon