Cell-to-cell contact and nectin-4 govern spread of measles virus from primary human myeloid cells to primary human airway epithelial cells

Journal of Virology

Volumn 90, Issue 15, 2016, Pages 6808-6817

  Singh, Brajesh K ^a   Li, Ni ^a   Mark, Anna C ^a   Mateo, Mathieu ^b,c,d   Cattaneo, Roberto ^b   Sinna, Patrick L ^a  

^a UNIVERSITY OF IOWA   (United States)

^b MAYO CLINIC   (United States)

^c Institut Pasteur   (France)

^d CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BLOCKING ANTIBODY; NECTIN 4; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; NECTINS; VIRUS RECEPTOR;

ADULT; ARTICLE; BONE MARROW CELL; CELL CONTACT; CELL DIFFERENTIATION; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC CELL; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; MACROPHAGE; MEASLES; MEASLES VIRUS; MONOCYTE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; VIRUS ENTRY; VIRUS TRANSMISSION; CELL CULTURE; CELL FUSION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; RESPIRATORY SYSTEM; VIROLOGY;

CELL ADHESION MOLECULES; CELL FUSION; CELLS, CULTURED; DENDRITIC CELLS; EPITHELIAL CELLS; HUMANS; MACROPHAGES; MEASLES; MEASLES VIRUS; MYELOID CELLS; RECEPTORS, VIRUS; RESPIRATORY SYSTEM; VIRUS INTERNALIZATION;

EID: 84982859275     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00266-16     Document Type: Article

References (46)

1. Griffin DE. 2013. Measles virus, p 1042-1069. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Roizman B (ed), Fields virology, 6th ed. Lippincott Williams and Wilkins, Philadelphia, PA.
2. Blau DM, Compans RW. 1997. Adaptation of measles virus to polarized epithelial cells: alterations in virus entry and release. Virology 231:281-289. http://dx.doi.org/10.1006/viro.1997.8520.
3. Blau DM, Compans RW. 1995. Entry and release of measles virus are polarized in epithelial cells. Virology 210:91-99. http://dx.doi.org/10.1006/viro.1995.1320.
4. Sinn PL, Williams G, Vongpunsawad S, Cattaneo R, McCray PB, Jr. 2002. Measles virus preferentially transduces the basolateral surface of well-differentiated human airway epithelia. J Virol 76:2403-2409. http://dx.doi.org/10.1128/jvi.76.5.2403-2409.2002.
5. Karp PH, Moniger TO, Weber SP, Nesselhauf TS, Launspach JL, Zabner J, Welsh MJ. 2002. An in vitro model of differentiated human airway epithelia. Methods Mol Biol 188:115-137.
6. Leonard VH, Sinn PL, Hodge G, Miest T, Devaux P, Oezguen N, Braun W, McCray PB, Jr, 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. Singh BK, Hornick AL, Krishnamurthy S, Locke AC, Mendoza CA, Mateo M, Miller-Hunt CL, Cattaneo R, Sinn PL. 2015. The nectin-4/ afadin protein complex and intercellular membrane pores contribute to rapid spread of measles virus in primary human airway epithelia. J Virol 89:7089-7096. http://dx.doi.org/10.1128/JVI.00821-15.
8. Mühlebach MD, Mateo M, Sinn PL, Prufer S, Uhlig KM, Leonard VH, Navaratnarajah CK, Frenzke M, Wong XX, Sawatsky B, Ramachandran S, McCray PB, Jr, 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. Pratakpiriya W, Seki F, Otsuki N, Sakai K, Fukuhara H, Katamoto H, Hirai T, Maenaka K, Techangamsuwan S, Lan NT, Takeda M, Yamaguchi R. 2012. Nectin4 is an epithelial cell receptor for canine distemper virus and involved in neurovirulence. J Virol 86:10207-10210. http://dx.doi.org/10.1128/JVI.00824-12.
10. 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. http://dx.doi.org/10.1371/journal.ppat.1002240.
11. Noyce RS, Delpeut S, Richardson CD. 2013. Dog nectin-4 is an epithelial cell receptor for canine distemper virus that facilitates virus entry and syncytia formation. Virology 436:210-220. http://dx.doi.org/10.1016/j.virol.2012.11.011.
12. Tatsuo H, Ono N, Tanaka K, Yanagi Y. 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893-897. http://dx.doi.org/10.1038/35022579.
13. Ferreira CS, Frenzke M, Leonard VH, Welstead GG, Richardson CD, Cattaneo R. 2010. Measles virus infection of alveolar macrophages and dendritic cells precedes spread to lymphatic organs in transgenic mice expressing human signaling lymphocytic activation molecule (SLAM, CD150). J Virol 84:3033-3042. http://dx.doi.org/10.1128/JVI.01559-09.
14. 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. http://dx.doi.org/10.1371/journal.ppat.1001263.
15. 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. http://dx.doi.org/10.1099/vir.0.016428-0.
16. Frenzke M, Sawatsky B, Wong XX, Delpeut S, Mateo M, Cattaneo R, von Messling V. 2013. Nectin-4-dependent measles virus spread to the cynomolgus monkey tracheal epithelium: role of infected immune cells infiltrating the lamina propria. J Virol 87:2526-2534. http://dx.doi.org/10.1128/JVI.03037-12.
17. Ludlow M, Lemon K, de Vries RD, McQuaid S, Millar EL, van Amerongen G, Yuksel S, Verburgh RJ, Osterhaus AD, de Swart RL, Duprex WP. 2013. Measles virus infection of epithelial cells in the macaque upper respiratory tract is mediated by subepithelial immune cells. J Virol 87: 4033-4042. http://dx.doi.org/10.1128/JVI.03258-12.
18. Monto AS. 1999. Interrupting the transmission of respiratory tract infections: theory and practice. Clin Infect Dis 28:200-204. http://dx.doi.org/10.1086/515113.
19. McChesney MB, Miller CJ, Rota PA, Zhu YD, Antipa L, Lerche NW, Ahmed R, Bellini WJ. 1997. Experimental measles. I. Pathogenesis in the normal and the immunized host. Virology 233:74-84.
20. Bohn W, Rutter G, Hohenberg H, Mannweiler K. 1983. Inhibition of measles virus budding by phenothiazines. Virology 130:44-55. http://dx.doi.org/10.1016/0042-6822(83)90116-2.
21. Cathomen T, Naim HY, Cattaneo R. 1998. Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J Virol 72:1224-1234.
22. Sica A, Mantovani A. 2012. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122:787-795. http://dx.doi.org/10.1172/JCI59643.
23. 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.
24. 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. http://dx.doi.org/10.1128/JVI.74.14.6643-6647.2000.
25. Martinez FO, Gordon S, Locati M, Mantovani A. 2006. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 177:7303-7311. http://dx.doi.org/10.4049/jimmunol.177.10.7303.
26. Vermeer PD, Einwalter LA, Moninger TO, Rokhlina T, Kern JA, Zabner J, Welsh MJ. 2003. Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 422:322-326. http://dx.doi.org/10.1038/nature01440.
27. Nakai T, Shand FL, Howatson AF. 1969. Development of measles virus in vitro. Virology 38:50-67. http://dx.doi.org/10.1016/0042-6822(69)90127-5.
28. Rager M, Vongpunsawad S, Duprex WP, Cattaneo R. 2002. Polyploid measles virus with hexameric genome length. EMBO J 21:2364-2372. http://dx.doi.org/10.1093/emboj/21.10.2364.
29. Mothes W, Sherer NM, Jin J, Zhong P. 2010. Virus cell-to-cell transmission. J Virol 84:8360-8368. http://dx.doi.org/10.1128/JVI.00443-10.
30. Sattentau Q. 2008. Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 6:815-826. http://dx.doi.org/10.1038/nrmicro1972.
31. Mateo M, Generous A, Sinn PL, Cattaneo R. 2015. Connections matter-how viruses use cell-cell adhesion components. J Cell Sci 128:431-439. http://dx.doi.org/10.1242/jcs.159400.
32. Birch J, Juleff N, Heaton MP, Kalbfleisch T, Kijas J, Bailey D. 2013. Characterization of ovine Nectin-4, a novel peste des petits ruminants virus receptor. J Virol 87:4756-4761. http://dx.doi.org/10.1128/JVI.02792-12.
33. Mateo M, Navaratnarajah CK, Willenbring RC, Maroun JW, Iankov I, Lopez M, Sinn PL, Cattaneo R. 2014. Different roles of the three loops forming the adhesive interface of nectin-4 in measles virus binding and cell entry, nectin-4 homodimerization, and heterodimerization with nectin-1. J Virol 88:14161-14171. http://dx.doi.org/10.1128/JVI.02379-14.
34. Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG. 1998. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618-1620. http://dx.doi.org/10.1126/science.280.5369.1618.
35. Eisenberg RJ, Atanasiu D, Cairns TM, Gallagher JR, Krummenacher C, Cohen GH. 2012. Herpes virus fusion and entry: a story with many characters. Viruses 4:800-832. http://dx.doi.org/10.3390/v4050800.
36. Sakisaka T, Taniguchi T, Nakanishi H, Takahashi K, Miyahara M, Ikeda W, Yokoyama S, Peng YF, Yamanishi K, Takai Y. 2001. Requirement of interaction of nectin-1alpha/HveC with afadin for efficient cell-cell spread of herpes simplex virus type 1. J Virol 75:4734-4743. http://dx.doi.org/10.1128/JVI.75.10.4734-4743.2001.
37. Mendelsohn CL, Wimmer E, Racaniello VR. 1989. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56:855-865. http://dx.doi.org/10.1016/0092-8674(89)90690-9.
38. Shannon-Lowe C, Rowe M. 2011. Epstein-Barr virus infection of polarized epithelial cells via the basolateral surface by memory B cell-mediated transfer infection. PLoS Pathog 7: e1001338. http://dx.doi.org/10.1371/journal.ppat.1001338.
39. Jaguin M, Houlbert N, Fardel O, Lecureur V. 2013. Polarization profiles of human M-CSF-generated macrophages and comparison of M1-markers in classically activated macrophages from GM-CSF and M-CSF origin. Cell Immunol 281:51-61. http://dx.doi.org/10.1016/j.cellimm.2013.01.010.
40. Fleetwood AJ, Lawrence T, Hamilton JA, Cook AD. 2007. Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J Immunol 178:5245-5252. http://dx.doi.org/10.4049/jimmunol.178.8.5245.
41. Lacey DC, Achuthan A, Fleetwood AJ, Dinh H, Roiniotis J, Scholz GM, Chang MW, Beckman SK, Cook AD, Hamilton JA. 2012. Defining GM-CSF- and macrophage-CSF-dependent macrophage responses by in vitro models. J Immunol 188:5752-5765. http://dx.doi.org/10.4049/jimmunol.1103426.
42. Miest TS, Cattaneo R. 2014. New viruses for cancer therapy: meeting clinical needs. Nat Rev Microbiol 12:23-34.
43. Galanis E, Atherton PJ, Maurer MJ, Knutson KL, Dowdy SC, Cliby WA, Haluska P, Jr, Long HJ, Oberg A, Aderca I, Block MS, Bakkum-Gamez J, Federspiel MJ, Russell SJ, Kalli KR, Keeney G, Peng KW, Hartmann LC. 2015. Oncolytic measles virus expressing the sodium iodide sym-porter to treat drug-resistant ovarian cancer. Cancer Res 75:22-30. http://dx.doi.org/10.1158/0008-5472.CAN-14-2533.
44. Derycke MS, Pambuccian SE, Gilks CB, Kalloger SE, Ghidouche A, Lopez M, Bliss RL, Geller MA, Argenta PA, Harrington KM, Skubitz AP. 2010. Nectin 4 overexpression in ovarian cancer tissues and serum: potential role as a serum biomarker. Am J Clin Pathol 134:835-845. http://dx.doi.org/10.1309/AJCPGXK0FR4MHIHB.
45. Fabre-Lafay S, Garrido-Urbani S, Reymond N, Goncalves A, Dubreuil P, Lopez M. 2005. Nectin-4, a new serological breast cancer marker, is a substrate for tumor necrosis factor-alpha-converting enzyme (TACE)/ ADAM-17. J Biol Chem 280:19543-19550. http://dx.doi.org/10.1074/jbc.M410943200.
46. Takano A, Ishikawa N, Nishino R, Masuda K, Yasui W, Inai K, Nishimura H, Ito H, Nakayama H, Miyagi Y, Tsuchiya E, Kohno N, Nakamura Y, Daigo Y. 2009. Identification of nectin-4 oncoprotein as a diagnostic and therapeutic target for lung cancer. Cancer Res 69:6694-6703. http://dx.doi.org/10.1158/0008-5472.CAN-09-0016.