Measles virus infection of epithelial cells in the macaque upper respiratory tract is mediated by subepithelial immune cells

Journal of Virology

Volumn 87, Issue 7, 2013, Pages 4033-4042

  Ludlow, Martin ^a   Lemon, Ken ^b   de Vries, Rory D ^c   McQuaid, Stephen ^b,d   Millar, Emma L ^c   Van Amerongen, Geert ^c   Yüksel, Selma ^c   Verburgh, R Joyce ^c   Osterhaus, Albert D M E ^c   de Swart, Rik L ^c   Duprexa, W Paul ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d ROYAL GROUP OF HOSPITALS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN PVRL4; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; LYMPHOID CELL; MACACA; MEASLES; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; TRACHEA; UPPER RESPIRATORY TRACT; VIRUS RECOMBINANT; VIRUS TRANSMISSION; WILD TYPE;

ANIMALS; B-LYMPHOCYTES; CELL ADHESION MOLECULES; CERCOPITHECUS AETHIOPS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; MEASLES; MEASLES VIRUS; RESPIRATORY MUCOSA; VERO CELLS; VIRUS INTERNALIZATION; VIRUS REPLICATION;

MACACA; MEASLES VIRUS;

EID: 84875549968     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03258-12     Document Type: Article

References (26)

1. Moss WJ, Griffin DE. 2006. Global measles elimination. Nat. Rev. Microbiol. 4:900 -908.
2. ECDC. 21 February 2012. Surveillance report. European monthly measles monitoring (EMMO). Issue 8. European Centre for Disease Prevention and Control, Stockholm, Sweden. http://ecdc.europa.eu/en/publications /publications/sur_emmo_European-monthly-measles-monitoring -february-2012.pdf.
3. Simons E, Ferrari M, Fricks J, Wannemuehler K, Anand A, Burton A, Strebel P. 2012. Assessment of the 2010 global measles mortality reduction goal: results from a model of surveillance data. Lancet 379:2173- 2178.
4. Tahara M, Takeda M, Shirogane Y, Hashiguchi T, Ohno S, Yanagi Y. 2008. Measles virus infects both polarized epithelial and immune cells by using distinctive receptor-binding sites on its hemagglutinin. J. Virol. 82: 4630-4637.
5. Ludlow M, Rennick LJ, Sarlang S, Skibinski G, McQuaid S, Moore T, de Swart RL, Duprex WP. 2010. Wild-type measles virus infection of primary epithelial cells occurs via the basolateral surface without syncytium formation or release of infectious virus. J. Gen. Virol. 91:971-979.
6. Leonard VH, Sinn PL, Hodge G, Miest T, Devaux P, Oezguen N, Braun W, McCray PB, McChesney MB, Cattaneo R. 2008. Measles virus blind to its epithelial cell receptor remains virulent in rhesus monkeys but cannot cross the airway epithelium and is not shed. J. Clin. Invest. 118:2448- 2458.
7. Noyce RS, Bondre DG, Ha MN, Lin LT, Sisson G, Tsao MS, Richardson CD. 2011. Tumor cell marker PVRL4 (nectin 4) is an epithelial cell receptor for measles virus. PLoS Pathog. 7:e1002240. doi:10.1371/journal.ppat .1002240.
8. Muhlebach MD, Mateo M, Sinn PL, Prufer S, Uhlig KM, Leonard VH, Navaratnarajah CK, Frenzke M, Wong XX, Sawatsky B, Ramachandran S, McCray PB, Cichutek K, von Messling V, Lopez M, Cattaneo R. 2011. Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 480:530 -533.
9. Lemon K, de Vries RD, Mesman AW, McQuaid S, van Amerongen G, Yuksel S, Ludlow M, Rennick LJ, Kuiken T, Rima BK, Geijtenbeek TB, Osterhaus AD, Duprex WP, de Swart RL. 2011. Early target cells of measles virus after aerosol infection of non-human primates. PLoS Pathog. 7:e1001263. doi:10.1371/journal.ppat.1001263.
10. de Swart RL, Ludlow M, de Witte L, Yanagi Y, van Amerongen G, McQuaid S, Yuksel S, Geijtenbeek TB, Duprex WP, Osterhaus AD. 2007. Predominant infection of CD150+lymphocytes and dendritic cells during measles virus infection of macaques. PLoS Pathog. 3:e178. doi:10 .1371/journal.ppat.0030178.
11. Mesman AW, de Vries RD, McQuaid S, Duprex WP, de Swart RL, Geijtenbeek TB. 2012. A prominent role for DC-SIGN+dendritic cells in initiation and dissemination of measles virus infection in non-human primates. PLoS One 7:e49573. doi:10.1371/journal.pone.0049573.
12. de Vries RD, McQuaid S, van Amerongen G, Yuksel S, Verburgh RJ, Osterhaus AD, Duprex WP, de Swart RL. 2012. Measles immune suppression: lessons from the macaque model. PLoS Pathog. 8:e1002885. doi: 10.1371/journal.ppat.1002885.
13. de Vries RD, Lemon K, Ludlow M, McQuaid S, Yuksel S, van Amerongen G, Rennick LJ, Rima BK, Osterhaus AD, de Swart RL, Duprex WP. 2010. In vivo tropism of attenuated and pathogenic measles virus expressing green fluorescent protein in macaques. J. Virol. 84:4714 - 4724.
14. Reed LJ, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. (Lond.) 27:493- 497.
15. Verkaik NJ, Nguyen DT, de Vogel CP, Moll HA, Verbrugh HA, Jaddoe VW, Hofman A, van Wamel WJ, van den Hoogen BG, Buijs-Offerman RM, Ludlow M, de Witte L, Osterhaus AD, van Belkum A, de Swart RL. 2011. Streptococcus pneumoniae exposure is associated with human metapneumovirus seroconversion and increased susceptibility to in vitro HMPV infection. Clin. Microbiol. Infect. 17:1840 -1844.
16. Takeda M, Takeuchi K, Miyajima N, Kobune F, Ami Y, Nagata N, Suzaki Y, Nagai Y, Tashiro M. 2000. Recovery of pathogenic measles virus from cloned cDNA. J. Virol. 74:6643- 6647.
17. Takeda M, Tahara M, Hashiguchi T, Sato TA, Jinnouchi F, Ueki S, Ohno S, Yanagi Y. 2007. A human lung carcinoma cell line supports efficient measles virus growth and syncytium formation via a SLAM- and CD46-independent mechanism. J. Virol. 81:12091-12096.
18. Frenzke M, Sawatsky B, Wong XX, Delpeut S, Mateo M, Cattaneo R, von Messling V. 19 December 2012. Nectin-4 dependent measles virus spread to the cynomolgus monkey tracheal epithelium: role of infected immune cells infiltrating the lamina propria. J. Virol. [Epub ahead of print.] doi:10.1128/JVI.03037-12.
19. Duprex WP, McQuaid S, Hangartner L, Billeter MA, Rima BK. 1999. Observation of measles virus cell-to-cell spread in astrocytoma cells by using a green fluorescent protein-expressing recombinant virus. J. Virol. 73:9568 -9575.
20. Racaniello V. 2011. Virology. An exit strategy for measles virus. Science. 334:1650 -1651.
21. Hall CB, Douglas RG, Jr, Schnabel KC, Geiman JM. 1981. Infectivity of respiratory syncytial virus by various routes of inoculation. Infect. Immun. 33:779 -783.
22. Eccles R. 2005. Understanding the symptoms of the common cold and influenza. Lancet Infect. Dis. 5:718 -725.
23. Lu R, Yu X, Wang W, Duan X, Zhang L, Zhou W, Xu J, Xu L, Hu Q,Lu J, Ruan L, Wang Z, Tan W. 2012. Characterization of human coronavirus etiology in Chinese adults with acute upper respiratory tract infection by real-time RT-PCR assays. PLoS One 7:e38638. doi:10.1371 /journal.pone.0038638.
24. Burke CW, Mason JN, Surman SL, Jones BG, Dalloneau E, Hurwitz JL, Russell CJ. 2011. Illumination of parainfluenza virus infection and transmission in living animals reveals a tissue-specific dichotomy. PLoS Pathog. 7:e1002134. doi:10.1371/journal.ppat.1002134.
25. van Riel D, den Bakker MA, Leijten LM, Chutinimitkul S, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T. 2010. Seasonal and pandemic human influenza viruses attach better to human upper respiratory tract epithelium than avian influenza viruses. Am. J. Pathol. 176:1614 -1618.
26. van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T. 2006. H5N1 virus attachment to lower respiratory tract. Science. 312:399. doi:10.1126/science.1125548.