{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,15]],"date-time":"2026-09-15T05:28:33Z","timestamp":1789450113179,"version":"build-2803163510"},"reference-count":28,"publisher":"Microbiology Society","issue":"5","funder":[{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000769","name":"University of Oxford","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000769","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000837","name":"University of Nottingham","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000837","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000738","name":"University of Leicester","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000738","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000690","name":"RCUK","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000690","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000690","name":"Research Councils UK","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000690","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Higher Education Commission of Pakistan"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2011,5,1]]},"abstract":"<jats:p>\n                    <jats:italic>Neisseria meningitidis<\/jats:italic>\n                    can utilize haem, haemoglobin and haemoglobin\u2013haptoglobin complexes as sources of iron via two TonB-dependent phase variable haemoglobin receptors, HmbR and HpuAB. HmbR is over-represented in disease isolates, suggesting a link between haemoglobin acquisition and meningococcal disease. This study compared the distribution of HpuAB and phase variation (PV) status of both receptors in disease and carriage isolates. Meningococcal disease (\n                    <jats:italic>n<\/jats:italic>\n                    \u200a=\u200a214) and carriage (\n                    <jats:italic>n<\/jats:italic>\n                    \u200a=\u200a305) isolates representative of multiple clonal complexes (CCs) were investigated for the distribution, polyG tract lengths and ON\/OFF status of both haemoglobin receptors, and for the deletion mechanism for HpuAB. Strains with both receptors or only\n                    <jats:italic>hmbR<\/jats:italic>\n                    were present at similar frequencies among meningococcal disease isolates as compared with carriage isolates. However, &gt;90\u200a% of isolates from the three CCs CC5, CC8 and CC11 with the highest disease to carriage ratios contained both receptors. Strains with an\n                    <jats:italic>hpuAB<\/jats:italic>\n                    -only phenotype were under-represented among disease isolates, suggesting selection against this receptor during systemic disease, possibly due to the receptor having a high level of immunogenicity or being inefficient in acquisition of iron during systemic spread. Absence of\n                    <jats:italic>hpuAB<\/jats:italic>\n                    resulted from either complete deletion or replacement by an insertion element. In an examination of PV status, one or both receptors were found in an ON state in 91\u200a% of disease and 71\u200a% of carriage isolates. We suggest that expression of a haemoglobin receptor, either HmbR or HpuAB, is of major importance for systemic spread of meningococci, and that the presence of both receptors contributes to virulence in some strains.\n                  <\/jats:p>","DOI":"10.1099\/mic.0.046946-0","type":"journal-article","created":{"date-parts":[[2011,2,10]],"date-time":"2011-02-10T21:33:44Z","timestamp":1297373624000},"page":"1446-1456","source":"Crossref","is-referenced-by-count":46,"title":["Influence of the combination and phase variation status of the haemoglobin receptors HmbR and HpuAB on meningococcal virulence"],"prefix":"10.1099","volume":"157","author":[{"given":"Isfahan","family":"Tauseef","sequence":"first","affiliation":[{"name":"Department of Genetics, University of Leicester, Leicester LE1 7RH, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Odile B.","family":"Harrison","sequence":"additional","affiliation":[{"name":"The Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3SY, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karl G.","family":"Wooldridge","sequence":"additional","affiliation":[{"name":"Molecular Bacteriology and Immunology Group, University of Nottingham, Nottingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ian M.","family":"Feavers","sequence":"additional","affiliation":[{"name":"National Institute for Biological Standards and Control, Blanche Lane, South Mimms, Hertfordshire EN6 3QG, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Keith R.","family":"Neal","sequence":"additional","affiliation":[{"name":"School of Community Health Sciences, University of Nottingham, Nottingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephen J.","family":"Gray","sequence":"additional","affiliation":[{"name":"Health Protection Agency, Meningococcal Reference Unit, Manchester Royal Infirmary, Manchester M13 9WL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paula","family":"Kriz","sequence":"additional","affiliation":[{"name":"National Reference Laboratory for Meningococcal Infections, National Institute of Public Health, Prague, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David P. J.","family":"Turner","sequence":"additional","affiliation":[{"name":"Molecular Bacteriology and Immunology Group, University of Nottingham, Nottingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dlawer A. A.","family":"Ala\u2019Aldeen","sequence":"additional","affiliation":[{"name":"Molecular Bacteriology and Immunology Group, University of Nottingham, Nottingham, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin C. J.","family":"Maiden","sequence":"additional","affiliation":[{"name":"The Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3SY, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher D.","family":"Bayliss","sequence":"additional","affiliation":[{"name":"Department of Genetics, University of Leicester, Leicester LE1 7RH, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J. G.","family":"Shaw","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"345","reference":[{"key":"r1","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.00395-08."},{"key":"r2","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1128\/JCM.01322-10","article-title":"Persistence, replacement and rapid clonal expansion of meningococcal carriage isolates in a 2008 university student cohort","volume":"49","author":"Bidmos","year":"2011","journal-title":"J Clin Microbiol"},{"key":"r3","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1042\/bj3340269","article-title":"Transferrin-binding protein B isolated from Neisseria meningitidis discriminates between apo and diferric human transferrin","volume":"334","author":"Boulton","year":"1998","journal-title":"Biochem J"},{"key":"r4","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2009.04.061."},{"key":"r5","doi-asserted-by":"publisher","DOI":"10.1007\/PL00008618."},{"key":"r6","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.2000.01701.x."},{"key":"r7","doi-asserted-by":"publisher","DOI":"10.1099\/mic.0.036475-0."},{"key":"r8","doi-asserted-by":"publisher","DOI":"10.1086\/599377."},{"key":"r9","doi-asserted-by":"crossref","first-page":"4492","DOI":"10.1128\/JCM.38.12.4492-4498.2000","article-title":"Carried meningococci in the Czech Republic: a diverse recombining population","volume":"38","author":"Jolley","year":"2000","journal-title":"J Clin Microbiol"},{"key":"r10","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0005198."},{"key":"r11","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1128\/JB.177.5.1299-1306.1995","article-title":"Identification of an iron-regulated outer membrane protein of Neisseria meningitidis involved in the utilization of hemoglobin complexed to haptoglobin","volume":"177","author":"Lewis","year":"1995","journal-title":"J Bacteriol"},{"key":"r12","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1999.01409.x."},{"key":"r13","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.6.3140."},{"key":"r14a","doi-asserted-by":"publisher","DOI":"10.1128\/JCM.02422-06."},{"key":"r14","doi-asserted-by":"publisher","DOI":"10.1128\/JCM.02422-06."},{"key":"r15","doi-asserted-by":"publisher","DOI":"10.1099\/mic.0.27182-0."},{"key":"r16","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.genet.40.110405.090442."},{"key":"r17","doi-asserted-by":"publisher","DOI":"10.3109\/10408419209114559."},{"key":"r18","doi-asserted-by":"publisher","DOI":"10.1099\/mic.0.26448-0."},{"key":"r19","doi-asserted-by":"publisher","DOI":"10.1128\/MMBR.68.1.154-171.2004."},{"key":"r20","doi-asserted-by":"crossref","first-page":"S274","DOI":"10.1097\/01.inf.0000147642.85129.05","article-title":"Global epidemiology of meningococcal disease and vaccine efficacy","volume":"23","author":"Pollard","year":"2004","journal-title":"Pediatr Infect Dis J"},{"key":"r21","doi-asserted-by":"crossref","first-page":"2067","DOI":"10.1128\/JB.181.7.2067-2074.1999","article-title":"HmbR, a hemoglobin-binding outer membrane protein of Neisseria meningitidis, undergoes phase variation","volume":"181","author":"Richardson","year":"1999","journal-title":"J Bacteriol"},{"key":"r22","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.092568699."},{"key":"r23","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.72.5.2494-2506.2004."},{"key":"r24","doi-asserted-by":"crossref","first-page":"674","DOI":"10.3201\/eid1004.030247","article-title":"PorA variable regions of Neisseria meningitidis","volume":"10","author":"Russell","year":"2004","journal-title":"Emerg Infect Dis"},{"key":"r25","doi-asserted-by":"publisher","DOI":"10.1111\/j.1574-6976.2006.00051.x."},{"key":"r26","doi-asserted-by":"publisher","DOI":"10.1099\/mic.0.26131-0."},{"key":"r27","doi-asserted-by":"crossref","first-page":"2928","DOI":"10.1128\/IAI.67.6.2928-2934.1999","article-title":"Deletion of porA by recombination between clusters of repetitive extragenic palindromic sequences in Neisseria meningitidis","volume":"67","author":"van der Ende","year":"1999","journal-title":"Infect Immun"}],"container-title":["Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/micro\/10.1099\/mic.0.046946-0?crawler=true","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,18]],"date-time":"2021-11-18T17:34:41Z","timestamp":1637256881000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/micro\/10.1099\/mic.0.046946-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2011,5,1]]},"references-count":28,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2011,5,1]]}},"URL":"https:\/\/doi.org\/10.1099\/mic.0.046946-0","relation":{},"ISSN":["1350-0872","1465-2080"],"issn-type":[{"value":"1350-0872","type":"print"},{"value":"1465-2080","type":"electronic"}],"subject":[],"published":{"date-parts":[[2011,5,1]]}}}