Complexity of Human Cytomegalovirus Infection in South African HIV-Exposed Infants with Pneumonia
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
P 31503
Austrian Science Fund FWF - Austria
MC_UU_12014/3
Medical Research Council - United Kingdom
PubMed
35632596
PubMed Central
PMC9147013
DOI
10.3390/v14050855
PII: v14050855
Knihovny.cz E-zdroje
- Klíčová slova
- HIV, compartmentalization, genotype, human cytomegalovirus, multiple-strain infections, pneumonia, whole genome sequence,
- MeSH
- cytomegalovirové infekce * epidemiologie MeSH
- Cytomegalovirus genetika MeSH
- HIV infekce * komplikace MeSH
- kojenec MeSH
- lidé MeSH
- pneumonie * MeSH
- Check Tag
- kojenec MeSH
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Jihoafrická republika epidemiologie MeSH
Human cytomegalovirus (HCMV) can cause significant end-organ diseases such as pneumonia in HIV-exposed infants. Complex viral factors may influence pathogenesis including: a large genome with a sizeable coding capacity, numerous gene regions of hypervariability, multiple-strain infections, and tissue compartmentalization of strains. We used a whole genome sequencing approach to assess the complexity of infection by comparing high-throughput sequencing data obtained from respiratory and blood specimens of HIV-exposed infants with severe HCMV pneumonia with those of lung transplant recipients and patients with hematological disorders. There were significantly more specimens from HIV-exposed infants showing multiple HCMV strain infection. Some genotypes, such as UL73 G4B and UL74 G4, were significantly more prevalent in HIV-exposed infants with severe HCMV pneumonia. Some genotypes were predominant in the respiratory specimens of several patients. However, the predominance was not statistically significant, precluding firm conclusions on anatomical compartmentalization in the lung.
Center for Virology Medical University of Vienna 1090 Vienna Austria
Medical Research Council University of Glasgow Centre for Virus Research Bearsden Glasgow G61 1QH UK
Zobrazit více v PubMed
Mocarski E.S. Cytomegaloviruses. In: Knipe D.M., editor. Fields Virology. Volume 2. Lippincott Williams and Wilkins; Philadelphia, PA, USA: 2007. pp. 2702–2772.
Manicklal S., van Niekerk A.M., Kroon S.M., Hutto C., Novak Z., Pati S.K., Chowdhury N., Hsiao N.Y., Boppana S.B. Birth prevalence of congenital cytomegalovirus among infants of HIV-infected women on prenatal antiretroviral prophylaxis in South Africa. Clin. Infect. Dis. 2014;58:1467–1472. doi: 10.1093/cid/ciu096. PubMed DOI
Mwaanza N., Chilukutu L., Tembo J., Kabwe M., Musonda K., Kapasa M., Chabala C., Sinyangwe S., Mwaba P., Zumla A., et al. High rates of congenital cytomegalovirus infection linked with maternal HIV infection among neonatal admissions at a large referral center in sub-Saharan Africa. Clin. Infect. Dis. 2014;58:728–735. doi: 10.1093/cid/cit766. PubMed DOI
Manicklal S., Emery V.C., Lazzarotto T., Boppana S.B., Gupta R.K. The “silent” global burden of congenital cytomegalovirus. Clin. Microbiol. Rev. 2013;26:86–102. doi: 10.1128/CMR.00062-12. PubMed DOI PMC
Kaye S., Miles D., Antoine P., Burny W., Ojuola B., Kaye P., Rowland-Jones S., Whittle H., van der Sande M., Marchant A. Virological and immunological correlates of mother-to-child transmission of cytomegalovirus in The Gambia. J. Infect. Dis. 2008;197:1307–1314. doi: 10.1086/586715. PubMed DOI
Richardson B.A., John-Stewart G., Atkinson C., Nduati R., Asbjornsdottir K., Boeckh M., Overbaugh J., Emery V., Slyker J.A. Vertical Cytomegalovirus Transmission From HIV-Infected Women Randomized to Formula-Feed or Breastfeed Their Infants. J. Infect. Dis. 2016;213:992–998. doi: 10.1093/infdis/jiv515. PubMed DOI PMC
Garcia-Knight M.A., Nduati E., Hassan A.S., Nkumama I., Etyang T.J., Hajj N.J., Gambo F., Odera D., Berkley J.A., Rowland-Jones S.L., et al. Cytomegalovirus viraemia is associated with poor growth and T-cell activation with an increased burden in HIV-exposed uninfected infants. Aids. 2017;31:1809–1818. doi: 10.1097/QAD.0000000000001568. PubMed DOI PMC
Filteau S., Rowland-Jones S. Cytomegalovirus Infection May Contribute to the Reduced Immune Function, Growth, Development, and Health of HIV-Exposed, Uninfected African Children. Front. Immunol. 2016;7:257. doi: 10.3389/fimmu.2016.00257. PubMed DOI PMC
Gompels U.A., Larke N., Sanz-Ramos M., Bates M., Musonda K., Manno D., Siame J., Monze M., Filteau S., Group C.S. Human cytomegalovirus infant infection adversely affects growth and development in maternally HIV-exposed and unexposed infants in Zambia. Clin. Infect. Dis. 2012;54:434–442. doi: 10.1093/cid/cir837. PubMed DOI PMC
Gronborg H.L., Jespersen S., Honge B.L., Jensen-Fangel S., Wejse C. Review of cytomegalovirus coinfection in HIV-infected individuals in Africa. Rev. Med. Virol. 2017;27:e1907. doi: 10.1002/rmv.1907. PubMed DOI
Slyker J.A., Lohman-Payne B.L., Rowland-Jones S.L., Otieno P., Maleche-Obimbo E., Richardson B., Farquhar C., Mbori-Ngacha D., Emery V.C., John-Stewart G.C. The detection of cytomegalovirus DNA in maternal plasma is associated with mortality in HIV-1-infected women and their infants. AIDS. 2009;23:117–124. doi: 10.1097/QAD.0b013e32831c8abd. PubMed DOI PMC
Arnold M., Itzikowitz R., Young B., Machoki S.M., Hsiao N.Y., Pillay K., Alexander A. Surgical manifestations of gastrointestinal cytomegalovirus infection in children: Clinical audit and literature review. J. Pediatr. Surg. 2015;50:1874–1879. doi: 10.1016/j.jpedsurg.2015.06.018. PubMed DOI
Goussard P., Kling S., Gie R.P., Nel E.D., Heyns L., Rossouw G.J., Janson J.T. CMV pneumonia in HIV-infected ventilated infants. Pediatr. Pulmonol. 2010;45:650–655. doi: 10.1002/ppul.21228. PubMed DOI
Zampoli M., Morrow B., Hsiao N.Y., Whitelaw A., Zar H.J. Prevalence and outcome of cytomegalovirus-associated pneumonia in relation to human immunodeficiency virus infection. Pediatr. Infect. Dis. J. 2011;30:413–417. doi: 10.1097/INF.0b013e3182065197. PubMed DOI
Bates M., Shibemba A., Mudenda V., Chimoga C., Tembo J., Kabwe M., Chilufya M., Hoelscher M., Maeurer M., Sinyangwe S., et al. Burden of respiratory tract infections at post mortem in Zambian children. BMC Med. 2016;14:99. doi: 10.1186/s12916-016-0645-z. PubMed DOI PMC
Jeena P.M., Govender K., Parboosing R., Adhikari M. The significance of cytomegalovirus in children with pneumonia admitted for mechanical ventilation. Int. J. Tuberc. Lung Dis. 2017;21:1230–1236. doi: 10.5588/ijtld.17.0026. PubMed DOI
Griffiths P., Reeves M. Pathogenesis of human cytomegalovirus in the immunocompromised host. Nat. Rev. Microbiol. 2021;19:759–773. doi: 10.1038/s41579-021-00582-z. PubMed DOI PMC
Govender K., Msomi N., Moodley P., Parboosing R. Cytomegalovirus pneumonia of infants in Africa: A narrative literature review. Future Microbiol. 2021;16:1401–1414. doi: 10.2217/fmb-2021-0147. PubMed DOI
Puchhammer-Stöckl E., Görzer I. Human cytomegalovirus: An enormous variety of strains and their possible clinical significance in the human host. Future Virol. 2011;6:259–271. doi: 10.2217/fvl.10.87. DOI
Arav-Boger R. Strain Variation and Disease Severity in Congenital Cytomegalovirus Infection: In Search of a Viral Marker. Infect. Dis. Clin. N. Am. 2015;29:401–414. doi: 10.1016/j.idc.2015.05.009. PubMed DOI PMC
Renzette N., Gibson L., Jensen J.D., Kowalik T.F. Human cytomegalovirus intrahost evolution-a new avenue for understanding and controlling herpesvirus infections. Curr. Opin. Virol. 2014;8:109–115. doi: 10.1016/j.coviro.2014.08.001. PubMed DOI PMC
Meyer-Konig U., Vogelberg C., Bongarts A., Kampa D., Delbruck R., Wolff-Vorbeck G., Kirste G., Haberland M., Hufert F.T., von Laer D. Glycoprotein B genotype correlates with cell tropism in vivo of human cytomegalovirus infection. J. Med. Virol. 1998;55:75–81. doi: 10.1002/(SICI)1096-9071(199805)55:1<75::AID-JMV12>3.0.CO;2-Z. PubMed DOI
Pang J., Slyker J.A., Roy S., Bryant J., Atkinson C., Cudini J., Farquhar C., Griffiths P., Kiarie J., Morfopoulou S., et al. Mixed cytomegalovirus genotypes in HIV-positive mothers show compartmentalization and distinct patterns of transmission to infants. eLife. 2020;9:e63199. doi: 10.7554/eLife.63199. PubMed DOI PMC
Slyker J., Farquhar C., Atkinson C., Asbjornsdottir K., Roxby A., Drake A., Kiarie J., Wald A., Boeckh M., Richardson B., et al. Compartmentalized cytomegalovirus replication and transmission in the setting of maternal HIV-1 infection. Clin. Infect. Dis. 2014;58:564–572. doi: 10.1093/cid/cit727. PubMed DOI PMC
Coaquette A., Bourgeois A., Dirand C., Varin A., Chen W., Herbein G. Mixed cytomegalovirus glycoprotein B genotypes in immunocompromised patients. Clin. Infect. Dis. 2004;39:155–161. doi: 10.1086/421496. PubMed DOI
Govender K., Jeena P., Parboosing R. Clinical utility of bronchoalveolar lavage cytomegalovirus viral loads in the diagnosis of cytomegalovirus pneumonitis in infants. J. Med. Virol. 2017;89:1080–1087. doi: 10.1002/jmv.24730. PubMed DOI PMC
Bates M., Monze M., Bima H., Kapambwe M., Kasolo F.C., Gompels U.A., CIGNIS Study Group High human cytomegalovirus loads and diverse linked variable genotypes in both HIV-1 infected and exposed, but uninfected, children in Africa. Virology. 2008;382:28–36. doi: 10.1016/j.virol.2008.09.001. PubMed DOI
Wang H.Y., Valencia S.M., Pfeifer S.P., Jensen J.D., Kowalik T.F., Permar S.R. Common Polymorphisms in the Glycoproteins of Human Cytomegalovirus and Associated Strain-Specific Immunity. Viruses. 2021;13:1106. doi: 10.3390/v13061106. PubMed DOI PMC
Hage E., Wilkie G.S., Linnenweber-Held S., Dhingra A., Suarez N.M., Schmidt J.J., Kay-Fedorov P.C., Mischak-Weissinger E., Heim A., Schwarz A., et al. Characterization of Human Cytomegalovirus Genome Diversity in Immunocompromised Hosts by Whole-Genome Sequencing Directly From Clinical Specimens. J. Infect. Dis. 2017;215:1673–1683. doi: 10.1093/infdis/jix157. PubMed DOI
Suarez N.M., Musonda K.G., Escriva E., Njenga M., Agbueze A., Camiolo S., Davison A.J., Gompels U.A. Multiple-Strain Infections of Human Cytomegalovirus With High Genomic Diversity Are Common in Breast Milk From Human Immunodeficiency Virus-Infected Women in Zambia. J. Infect. Dis. 2019;220:792–801. doi: 10.1093/infdis/jiz209. PubMed DOI PMC
Kalser J., Adler B., Mach M., Kropff B., Puchhammer-Stockl E., Gorzer I. Differences in Growth Properties among Two Human Cytomegalovirus Glycoprotein O Genotypes. Front. Microbiol. 2017;8:1609. doi: 10.3389/fmicb.2017.01609. PubMed DOI PMC
Tanaka N., Kimura H., Iida K., Saito Y., Tsuge I., Yoshimi A., Matsuyama T., Morishima T. Quantitative analysis of cytomegalovirus load using a real-time PCR assay. J. Med. Virol. 2000;60:455–462. doi: 10.1002/(SICI)1096-9071(200004)60:4<455::AID-JMV14>3.0.CO;2-Q. PubMed DOI
Suarez N.M., Wilkie G.S., Hage E., Camiolo S., Holton M., Hughes J., Maabar M., Vattipally S.B., Dhingra A., Gompels U.A., et al. Human Cytomegalovirus Genomes Sequenced Directly From Clinical Material: Variation, Multiple-Strain Infection, Recombination, and Gene Loss. J. Infect. Dis. 2019;220:781–791. doi: 10.1093/infdis/jiz208. PubMed DOI PMC
Camiolo S., Suarez N.M., Chalka A., Venturini C., Breuer J., Davison A.J. GRACy: A tool for analysing human cytomegalovirus sequence data. Virus Evol. 2021;7:veaa099. doi: 10.1093/ve/veaa099. PubMed DOI PMC
Langmead B., Salzberg S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012;9:357–359. doi: 10.1038/nmeth.1923. PubMed DOI PMC
Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., Kulikov A.S., Lesin V.M., Nikolenko S.I., Pham S., Prjibelski A.D., et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 2012;19:455–477. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC
Silva G.G., Dutilh B.E., Matthews T.D., Elkins K., Schmieder R., Dinsdale E.A., Edwards R.A. Combining de novo and reference-guided assembly with scaffold_builder. Source Code Biol. Med. 2013;8:23. doi: 10.1186/1751-0473-8-23. PubMed DOI PMC
Milne I., Stephen G., Bayer M., Cock P.J., Pritchard L., Cardle L., Shaw P.D., Marshall D. Using Tablet for visual exploration of second-generation sequencing data. Brief. Bioinform. 2013;14:193–202. doi: 10.1093/bib/bbs012. PubMed DOI
Marti-Carreras J., Maes P. Human cytomegalovirus genomics and transcriptomics through the lens of next-generation sequencing: Revision and future challenges. Virus Genes. 2019;55:138–164. doi: 10.1007/s11262-018-1627-3. PubMed DOI PMC
Musonda K.G., Nyonda M., Filteau S., Kasonka L., Monze M., Gompels U.A. Increased Cytomegalovirus Secretion and Risks of Infant Infection by Breastfeeding Duration From Maternal Human Immunodeficiency Virus Positive Compared to Negative Mothers in Sub-Saharan Africa. J. Pediatric Infect. Dis. Soc. 2016;5:138–146. doi: 10.1093/jpids/piw015. PubMed DOI PMC
Sowmya P., Madhavan H.N. Analysis of mixed infections by multiple genotypes of human cytomegalovirus in immunocompromised patients. J. Med. Virol. 2009;81:861–869. doi: 10.1002/jmv.21459. PubMed DOI
Jiang X.J., Zhang J., Xiong Y., Jahn G., Xiong H.R., Yang Z.Q., Liu Y.Y. Human cytomegalovirus glycoprotein polymorphisms and increasing viral load in AIDS patients. PLoS ONE. 2017;12:e0176160. doi: 10.1371/journal.pone.0176160. PubMed DOI PMC
Shikhagaie M., Merce-Maldonado E., Isern E., Muntasell A., Alba M.M., Lopez-Botet M., Hengel H., Angulo A. The human cytomegalovirus-specific UL1 gene encodes a late-phase glycoprotein incorporated in the virion envelope. J. Virol. 2012;86:4091–4101. doi: 10.1128/JVI.06291-11. PubMed DOI PMC
Choi H.J., Park A., Kang S., Lee E., Lee T.A., Ra E.A., Lee J., Lee S., Park B. Human cytomegalovirus-encoded US9 targets MAVS and STING signaling to evade type I interferon immune responses. Nat. Commun. 2018;9:125. doi: 10.1038/s41467-017-02624-8. PubMed DOI PMC
Ourahmane A., Cui X., He L., Catron M., Dittmer D.P., Al Qaffasaa A., Schleiss M.R., Hertel L., McVoy M.A. Inclusion of Antibodies to Cell Culture Media Preserves the Integrity of Genes Encoding RL13 and the Pentameric Complex Components During Fibroblast Passage of Human Cytomegalovirus. Viruses. 2019;11:221. doi: 10.3390/v11030221. PubMed DOI PMC
Nguyen C.C., Kamil J.P. Pathogen at the Gates: Human Cytomegalovirus Entry and Cell Tropism. Viruses. 2018;10:704. doi: 10.3390/v10120704. PubMed DOI PMC
Kabanova A., Marcandalli J., Zhou T., Bianchi S., Baxa U., Tsybovsky Y., Lilleri D., Silacci-Fregni C., Foglierini M., Fernandez-Rodriguez B.M., et al. Platelet-derived growth factor-alpha receptor is the cellular receptor for human cytomegalovirus gHgLgO trimer. Nat. Microbiol. 2016;1:16082. doi: 10.1038/nmicrobiol.2016.82. PubMed DOI PMC
Endale M., Ahlfeld S., Bao E., Chen X., Green J., Bess Z., Weirauch M.T., Xu Y., Perl A.K. Temporal, spatial, and phenotypical changes of PDGFRalpha expressing fibroblasts during late lung development. Dev. Biol. 2017;425:161–175. doi: 10.1016/j.ydbio.2017.03.020. PubMed DOI PMC
Gouveia L., Betsholtz C., Andrae J. Expression analysis of platelet-derived growth factor receptor alpha and its ligands in the developing mouse lung. Physiol. Rep. 2017;5:e13092. doi: 10.14814/phy2.13092. PubMed DOI PMC
Bons E., Regoes R.R. Virus dynamics and phyloanatomy: Merging population dynamic and phylogenetic approaches. Immunol. Rev. 2018;285:134–146. doi: 10.1111/imr.12688. PubMed DOI
Suarez N.M., Blyth E., Li K., Ganzenmueller T., Camiolo S., Avdic S., Withers B., Linnenweber-Held S., Gwinner W., Dhingra A., et al. Whole-Genome Approach to Assessing Human Cytomegalovirus Dynamics in Transplant Patients Undergoing Antiviral Therapy. Front. Cell Infect. Microbiol. 2020;10:267. doi: 10.3389/fcimb.2020.00267. PubMed DOI PMC
UNAIDS FACT SHEET. [(accessed on 7 April 2022)]. Available online: https://www.unaids.org/sites/default/files/media_asset/UNAIDS_FactSheet_en.pdf.