Wild-type measles virus is intrinsically dual-tropic

Frontiers in Microbiology

Volumn 2, Issue JAN, 2012, Pages

  Takeda, Makoto ^a   Tahara, Maino ^a   Nagata, Noriyo ^a   Seki, Fumio ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Dual tropic; Measles virus; Nectin4; Receptor; Slam

Indexed keywords

MEASLES VIRUS;

EID: 84866167093     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00279     Document Type: Review

References (54)

1. Bellini, W. J., Rota, J. S., Lowe, L. E., Katz, R. S., Dyken, P. R., Zaki, S. R., Shieh, W. J., and Rota, P. A. (2005). Subacute sclerosing panencephalitis: more cases of this fatal disease are prevented by measles immunization than was previously recognized. J. Infect. Dis. 192, 1686-1693.
2. Brancati, F., Fortugno, P., Bottillo, I., Lopez, M., Josselin, E., Boudghene-Stambouli, O., Agolini, E., Bernardini, L., Bellacchio, E., Iannicelli, M., Rossi, A., Dib-Lachachi, A., Stuppia, L., Palka, G., Mundlos, S., Stricker, S., Kornak, U., Zambruno, G., and Dallapiccola, B. (2010). Mutations in PVRL4, encoding cell adhesion molecule nectin-4, cause ectodermal dysplasia-syndactyly syndrome. Am. J. Hum. Genet. 87, 265-273.
3. Cannons, J. L., Tangye, S. G., and Schwartzberg, P. L. (2011). SLAM family receptors and SAP adaptors in immunity. Annu. Rev. Immunol. 29, 665-705.
4. Corry, D., Kulkarni, P., and Lipscomb, M. F. (1984). The migration ofbron-choalveolar macrophages into hilar lymph nodes. Am. J. Pathol. 115, 321-328.
5. Craighead, J. E. (2000). "Rubeola (Measles)," in Pathology and Pathogenesis of Human Viral Disease, ed. J. E. Craighead (Philadelphia, PA: Elsevier Inc.), 397-410.
6. de Swart, R. L., Ludlow, M., de Witte, L., Yanagi, Y., Van Amerongen, G., Mcquaid, S., Yuksel, S., Geijtenbeek, T. B., Duprex, W. P., and Oster-haus, A. D. (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
7. de Vries, R. D., Lemon, K., Ludlow, M., Mcquaid, S., Yuksel, S., Van Amerongen, G., Rennick, L. J., Rima, B. K., Osterhaus, A. D., de Swart, R. L., and Duprex, W. P. (2010). In vivo tropism of attenuated and pathogenic measles virus expressing green fluorescent protein in macaques. J. Virol. 84, 4714-4724.
8. de Witte, L., Abt, M., Schneider-Schaulies, S., Van Kooyk, Y., and Geijtenbeek, T. B. (2006). Measles virus targets DC-SIGN to enhance dendritic cell infection. J. Virol. 80, 3477-3486.
9. de Witte, L., de Vries, R. D., Van Der Vlist, M., Yuksel, S., Litjens, M., de Swart, R. L., and Gei-jtenbeek, T. B. (2008). DC-SIGN and CD 150 have distinct roles in transmission of measles virus from dendritic cells to T-lymphocytes. PLoS Pathog. 4, e1000049. doi:10.1371/journal.ppat.1000049
10. Derycke, M. S., Pambuccian, S. E., Gilks, C. B., Kalloger, S. E., Ghidouche, A., Lopez, M., Bliss, R. L., Geller, M. A., Argenta, P. A., Harrington, K. M., and Skubitz, A. P. (2010). Nectin 4 overexpression in ovarian cancer tissues and serum: potential role as a serum biomarker.Am.J. Clin. Pathol. 134, 835-845.
11. Detre, C., Keszei, M., Romero, X., Tsokos, G. C., and Terhorst, C. (2010). SLAM family receptors and the SLAM-associated protein (SAP) modulate T cell functions. Semin. Immunopathol. 32, 157-171.
12. Devaux, P., Hodge, G., Mcchesney, M. B., and Cattaneo, R. (2008). Attenuation of V- or C-defective measles viruses: infection control by the inflammatory and interferon responses of rhesus monkeys. J. Virol. 82, 5359-5367.
13. Devaux, P., Hudacek, A. W., Hodge, G., Reyes-Del Valle, J., Mcchesney, M. B., and Cattaneo, R. (2011). A recombinant measles virus unable to antagonize STAT1 function cannot control inflammation and is attenuated in rhesus monkeys. J. Virol. 85, 348-356.
14. Dong, Z., and Veillette, A. (2010). How do SAP family deficiencies compromise immunity? TrendsImmunol. 31, 295-302.
15. Dorig, R. E., Marcil, A., Chopra, A., and Richardson, C. D. (1993). The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75,295-305.
16. Fabre, S., Reymond, N., Cocchi, E, Menotti, L., Dubreuil, P., Campadelli-Fiume, G., and Lopez, M. (2002). Prominent role of the Ig-like V domain in trans-interactions of nectins. Nectin3 and nectin 4 bind to the predicted C-C′-C″-D beta-strands of the nectin1 V domain. J. Biol. Chem. 277, 27006-27013.
17. Fabre-Lafay, S., Monville, F., Garrido-Urbani, S., Berruyer-Pouyet, C., Ginestier, C., Reymond, N., Finetti, P., Sauvan, R., Adelaide, J., Geneix, J., Lecocq, E., Popovici, C., Dubreuil, P., Viens, P., Goncalves, A., Charafe-Jauffret, E., Jacquemier, J., Birn-baum, D., and Lopez, M. (2007). Nectin-4 is a new histological and serological tumor associated marker for breast cancer. BMC Cancer 7, 73. doi:10.1186/1471-2407-7-73
18. Griffin, D. E. (2007). "Measles virus," in Fields Virology, 5th Edn, eds D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (Philadelphia: Lippincott Williams and Wilkins), 1551-1585.
19. Griffin, D. E., and Ward, B. J. (1993). Differential CD4 T cell activation in measles. J. Infect. Dis. 168,275-281.
20. Hashimoto, K., Ono, N., Tatsuo, H., Minagawa, H., Takeda, M., Takeuchi, K., and Yanagi, Y. (2002). SLAM (CD 150)-independent measles virus entry as revealed by recombinant virus expressing green fluorescent protein. J. Virol. 76, 6743-6749.
21. Jelani, M., Chishti, M. S., and Ahmad, W. (2011). Mutation in PVRL4 gene encoding nectin-4 underlies ecto dermal-dysplasia-syndactyly syndrome (EDSS1). J. Hum. Genet. 56, 352-357.
22. Kobune, F., Sakata, H., and Sugiura, A. (1990). Marmoset lymphoblas-toid cells as a sensitive host for isolation of measles virus. J. Virol. 64, 700-705.
23. Kobune, F., Takahashi, H., Terao, K., Ohkawa, T., Ami, Y., Suzaki, Y., Nagata, N., Sakata, H., Yamanouchi, K., and Kai, C. (1996). Nonhuman primate models of measles. Lab. Anim. Sci. 46, 315-320.
24. Lehmann, C., Wilkening, A., Leiber, D., Markus, A., Krug, N., Pabst, R., and Tschernig, T. (2001). Lymphocytes in the bronchoalveolar space reen-ter the lung tissue by means of the alveolar epithelium, migrate to regional lymph nodes, and subsequently rejoin the systemic immune system. Anat. Rec. 264, 229-236.
25. Lemon, K., de Vries, R. D., Mesman, A. W., Mcquaid, S., Van Amerongen, G., Yuksel, S., Ludlow, M., Rennick, L. J., Kuiken, T., Rima, B. K., Geijtenbeek, T. B., Osterhaus, A. D., Duprex, W. P., and de Swart, R. L. (2011). Early target cells of measles virus after aerosol infection of non-human primates. PLoS Pathog. 7, e1001263. doi:10.1371/journal.ppat. 1001263
26. Leonard, V H., Sinn, P. L., Hodge, G., Miest, T., Devaux, P., Oezguen, N., Braun, W., Mccray, P. B., Mcchesney, M. B., and 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.
27. Lightwood, R., and Nolan, R. (1970). Epithelial giant cells in measles as an acid in diagnosis. J. Pediatr. 77, 59-64.
28. Ludlow, M., Rennick, L. J., Sarlang, S., Skibinski, G., Mcquaid, S., Moore, T., de Swart, R. L., and Duprex, W P. (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.
29. Ma, C. S., and Deenick, E. K. (2011). The role of SAP and SLAM family molecules in the humoral immune response. Ann. N. Y. Acad. Sci. 1217, 32-44.
30. Makhortova, N. R., Askovich, P., Patterson, C. E., Gechman, L. A., Gerard, N. P., and Rall, G. F. (2007). Neurokinin-1 enables measles virus trans-synaptic spread in neurons. Virology 362, 235-244.
31. Moench, T. R., Griffin, D. E., Obriecht, C R., Vaisberg, A. J., and Johnson, R. T. (1988). Acute measles in patients with and without neuro logical involvement: distribution of measles virus antigen and RNA. J. Infect. Dis. 158,433-442.
32. Mühlebach, M. D., Mateo, M., Sinn, P. L., Prufer, S., Uhlig, K. M., Leonard, V H., Navaratnarajah, C. K., Fren-zke, M., Wong, X. X., Sawatsky, B., Ramachandran, S., Mccray, P. B., Cichutek, K., Von Messling, V., Lopez, M., and Cattaneo, R. (2011). Adherens junction protein nectin-4 is the epithelial receptor for measles virus. Nature 480, 530-533.
33. Nakatsu, Y., Takeda, M., Ohno, S., Shirogane, Y., Iwasaki, M., and Yanagi, Y (2008). Measles virus circumvents the host interferon response by different actions of the C and V proteins. J. Virol. 82, 8296-8306.
34. Naniche, D., Varior-Krishnan, G., Cer-voni, F., Wild, T. F., Rossi, B., Rabourdin-Combe, C., and Gerlier, D. (1993). Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J. Virol. 67,6025-6032.
35. Nii, S., Kamahora, J., Mori, Y., Takahashi, M., Nishimura, S., and Okuno, Y. (1964). Experimental pathology of measles in monkeys. Biken J. 6, 271-297.
36. Noyce, R. S., Bondre, D. G., Ha, M. N., Lin, L. T., Sisson, G., Tsao, M. S., and Richardson, C. D. (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
37. Olding-Stenkvist, E., and Bjorvatn, B. (1976). Rapid detection of measles virus in skin rashes by immunofluroescence. J. Infect. Dis. 134,463-469.
38. Reymond, N., Fabre, S., Lecocq, E., Adelaide, J., Dubreuil, P., and Lopez, M. (2001). Nectin4/PRR4, a new afadin-associated member of the nectin family that trans-interacts with nectin1/PRR1 through V domain interaction. J. Biol. Chem. 276, 43205-43215.
39. Schneider-Schaulies, S., and Schneider-Schaulies, J. (2009). Measles virus-induced immunosuppression. Curr. Top. Microbiol. Immunol. 330, 243-269.
40. Seki, F., Yamada, K., Nakatsu, Y., Oka-mura, K., Yanagi, Y., Nakayama, T., Komase, K., and Takeda, M. (2011). The si strain of measles virus derived from a patient with subacute sclerosing panencephalitis possesses typical genome alterations and unique amino acid changes that modulate receptor specificity and reduce membrane fusion activity. J. Virol. 85, 11871-11882.
41. Tahara, M., Takeda, M., Shirogane, Y., Hashiguchi, T., Ohno, S., and 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.
42. Takai, Y., Ikeda, W., Ogita, H., and Rikitake, Y (2008a). The immunoglobulin-like cell adhesion molecule nectin and its associated protein afadin. Annu. Rev. Cell Dev. Biol. 24, 309-342.
43. Takai, Y., Miyoshi, J., Ikeda, W., and Ogita, H. (2008b). Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat. Rev. Mol. Cell Biol. 9,603-615.
44. 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., and Daigo, Y. (2009). Identification of nectin-4 oncoprotein as a diagnostic and therapeutic target for lung cancer. Cancer Res. 69, 6694-6703.
45. Takasu, T., Mgone, J. M., Mgone, C. S., Miki, K., Komase, K., Namae, H., Saito,Y., Kokubun,Y., Nishimura, T., Kawanishi, R., Mizutani, T., Markus, T. J., Kono, J., Asuo, P. G., and Alpers, M. P. (2003). A continuing high incidence of subacute sclerosing panencephalitis (SSPE) in the Eastern Highlands of Papua New Guinea. Epidemiol. Infect. 131, 887-898.
46. Takeda, M., Kato, A., Kobune, F., Sakata, H., Li, Y., Shioda, T., Sakai, Y., Asakawa, M., and Nagai, Y (1998). Measles virus attenuation associated with transcriptional impediment and a few amino acid changes in the polymerase and accessory proteins. J. Virol. 72, 8690-8696.
47. Takeda, M., Tahara, M., Hashiguchi, T., Sato, T. A., Jinnouchi, F., Ueki, S., Ohno, S., and Yanagi, Y. (2007). A human lung carcinoma cell line supports efficient measles virus growth and syn-cytium formation via a SLAM- and CD46-independent mechanism. J. Virol. 81,12091-12096.
48. Takeda, M., Takeuchi, K., Miyajima, N., Kobune, F., Ami, Y., Nagata, N., Suzaki, Y., Nagai, Y., and Tashiro, M. (2000). Recovery of pathogenic measles virus from cloned cDNA. J. Virol. 74, 6643-6647.
49. Takeuchi, K., Miyajima, N., Nagata, N., Takeda, M., and Tashiro, M. (2003). Wild-type measles virus induces large syncytium formation in primary human small airway epithelial cells by a SLAM(CD150)-independent mechanism. Virus Res. 94, 11-16.
50. Takeuchi, K., Takeda, M., Miyajima, N., Ami, Y., Nagata, N., Suzaki, Y., Shahnewaz, J., Kadota, S., and Nagata, K. (2005). Stringent requirement for the C protein of wild-type measles virus for growth both in vitro and in macaques. J. Virol. 79, 7838-7844.
51. Tatsuo, H., Ono, N., Tanaka, K., and Yanagi, Y (2000). SLAM (CDw150) is a cellular receptor for measles virus. Nature 406, 893-897.
52. Veillette, A. (2010). SLAM-family receptors: immune regulators with or without SAP-family adaptors. Cold Spring Harb. Perspect. Biol. 2, a002469.
53. WHO. (2009). Global reductions in measles mortality 2000-2008 and the risk of measles resurgence. Wkly. Epidemiol. Rec. 84, 509-516.
54. Yanagi, Y., Takeda, M., Ohno, S., and Hashiguchi, T. (2009). Measles virus receptors. Curr. Top. Microbiol. Immunol. 329, 13-30.