Measles vaccination of nonhuman primates provides partial protection against infection with canine distemper virus

Journal of Virology

Volumn 88, Issue 8, 2014, Pages 4423-4433

  De Vries, Rory D ^a   Ludlow, Martin ^b   Verburgh, R Joyce ^a   van Amerongen, Geert ^a   Yüksel, Selma ^a   Nguyen, D Tien ^a   McQuaid, Stephen ^c   Osterhaus, Albert D M E ^a   Duprex, W Paul ^b   De Swart, Rik L ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD150 ANTIGEN; EPITOPE; GREEN FLUORESCENT PROTEIN; MEASLES VACCINE; NEUTRALIZING ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS MUCOSA; CANINE DISTEMPER; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; DENDRITIC CELL; FEVER; INFECTION PREVENTION; LEUKOCYTE COUNT; LYMPHOCYTOPENIA; MALE; MEASLES VACCINATION; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRAL TROPISM; VIREMIA; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS SHEDDING; VIRUS VIRULENCE;

ANIMALS; ANTIBODIES, VIRAL; CROSS PROTECTION; DISTEMPER; DISTEMPER VIRUS, CANINE; HUMANS; LYMPHOCYTES; MACACA; MALE; MEASLES; MEASLES VACCINE; MEASLES VIRUS; MONKEY DISEASES; VACCINATION;

EID: 84896950906     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03676-13     Document Type: Article

References (56)

1. Blancou J. 2004. Dog distemper: imported into Europe from South America? Hist. Med. Vet. 29:35-41.
2. von Messling V, Milosevic D, Cattaneo R. 2004. Tropism illuminated: lymphocyte-based pathways blazed by lethal morbillivirus through the host immune system. Proc. Natl. Acad. Sci. U. S. A. 101:14216-14421. http://dx.doi.org/10.1073/pnas.0403597101.
3. Beineke A, PuffC, Seehusen F, Baumgartner W. 2009. Pathogenesis and immunopathology of systemic and nervous canine distemper. Vet. Immunol. Immunopathol. 127:1-18. http://dx.doi.org/10.1016/j.vetimm.2008.09.023.
4. Seki F, Ono N, Yamaguchi R, Yanagi Y. 2003. Efficient isolation of wild strains of canine distemper virus in Vero cells expressing canine SLAM (CD150) and their adaptability to marmoset B95a cells. J. Virol. 77:9943-9950. http://dx.doi.org/10.1128/JVI.77.18.9943-9950.2003.
5. Tatsuo H, Ono N, Yanagi Y. 2001. Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J. Virol. 75:5842-5850. http://dx.doi.org/10.1128/JVI.75.13.5842-5850.2001.
6. von Messling V, Svitek N, Cattaneo R. 2006. Receptor (SLAM [CD150]) recognition and the V protein sustain swift lymphocyte-based invasion of mucosal tissue and lymphatic organs by a morbillivirus. J. Virol. 80:6084-6092. http://dx.doi.org/10.1128/JVI.00357-06.
7. 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. http://dx.doi.org/10.1038/nature 10639.
8. 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.
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 the neurovirulence. J. Virol. 86:10207-10210. http://dx.doi.org/10.1128/JVI.00824-12.
10. Sawatsky B, Wong XX, Hinkelmann S, Cattaneo R, von Messling V. 2012. Canine distemper virus epithelial cell infection is required for clinical disease but not for immunosuppression. J. Virol. 86:3658-3666. http://dx.doi.org/10.1128/JVI.06414-11.
11. Leonard VHJ, 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. http://dx.doi.org/10.1172/JCI35454.
12. Ludlow M, Rennick LJ, Nambulli S, De Swart RL, Duprex WP. 2014. Using the ferret model to study morbillivirus entry, spread, transmission and cross-protection. Curr. Opin. Virol. 4:15-23. http://dx.doi.org/10.1016/j.coviro.2013.11.001.
13. Appel MJ, Reggiardo C, Summers BA, Pearce-Kelling S, Mare CJ, Noon TH, Reed RE, Shively JN, Örvell C. 1991. Canine distemper virus infection in javelinas (collared peccaries). Arch. Virol. 119:147-152. http://dx.doi.org/10.1007/BF01314331.
14. Origgi FC, Sattler U, Pilo P, Waldvogel AS. 2013. Fatal combined infection with canine distemper virus and orthopoxvirus in a group of Asian marmots (Marmota caudata). Vet. Pathol. 50:914-920. http://dx.doi.org/10.1177/0300985813476060.
15. Yoshikawa Y, Ochikubo F, Matsubara Y, Tsuruoka H, Ishii M, Shirota K, Nomura Y, Sugiyama M, Yamanouchi K. 1989. Natural infection with canine distemper virus in a Japanese monkey (Macaca fuscata). Vet. Microbiol. 20:193-205. http://dx.doi.org/10.1016/0378-1135(89)90043-6.
16. Qiu W, Zheng Y, Zhang S, Fan Q, Liu H, Zhang F, Wang W, Liao G, Hu R. 2011. Canine distemper outbreak in rhesus monkeys, China. Emerg. Infect. Dis. 17:1541-1543. http://dx.doi.org/10.3201/eid1708.101153.
17. Sakai K, Nagata N, Ami Y, Seki F, Suzaki Y, Iwata-Yoshikawa N, Suzuki T, Fukushi S, Mizutani T, Yoshikawa T, Otsuki N, Kurane I, Komase K, Yamaguchi R, Hasegawa H, Saijo M, Takeda M, Morikawa S. 2013. Lethal canine distemper virus outbreak in cynomolgus monkeys in Japan in 2008. J. Virol. 87:1105-1114. http://dx.doi.org/10.1128/JVI.02419-12.
18. Barrett T. 1999. Morbillivirus infections, with special emphasis on morbilliviruses of carnivores. Vet. Microbiol. 69:3-13. http://dx.doi.org/10.1016/S0378-1135(99)00080-2.
19. Strating A. 1975. Measles vaccine in dogs: efficacy against aerosol challenge with virulent canine distemper virus. J. Am. Vet. Med. Assoc. 167: 59-62.
20. Sanders R, Dabbagh A, Featherstone D. 2011. Risk analysis for measles reintroduction after global certification of eradication. J. Infect. Dis. 204(Suppl 1):S71-S77. http://dx.doi.org/10.1093/infdis/jir133.
21. Drexler JF, Corman VM, Muller MA, Maganga GD, Vallo P, Binger T, Gloza-Rausch F, Rasche A, Yordanov S, Seebens A, Oppong S, Sarkodie YA, Pongombo C, Lukashev AN, Schmidt-Chanasit J, Stocker A, Carneiro AJ, Erbar S, Maisner A, Fronhoffs F, Buettner R, Kalko EK, Kruppa T, Franke CR, Kallies R, Yandoko ER, Herrler G, Reusken C, Hassanin A, Kruger DH, Matthee S, Ulrich RG, Leroy EM, Drosten C. 2012. Bats host major mammalian paramyxoviruses. Nat. Commun. 3:796. http://dx.doi.org/10.1038/ncomms1796.
22. de Swart RL, Ludlow M, De Witte L, Yanagi Y, Van Amerongen G, McQuaid S, Yüksel 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. http://dx.doi.org/10.1371/journal.ppat.0030178.
23. de Vries RD, Lemon K, Ludlow M, McQuaid S, Yüksel 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. http://dx.doi.org/10.1128/JVI.02633-09.
24. Lemon K, de Vries RD, Mesman AW, McQuaid S, Van Amerongen G, Yüksel 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.
25. Ludlow M, Rennick L, 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.
26. Ludlow M, Nguyen DT, Silin D, Lyubomska O, De Vries RD, von Messling V, McQuaid S, De Swart RL, Duprex WP. 2012. Recombinant canine distemper virus strain Snyder Hill expressing green or red fluoresde cent proteins causes meningoencephalitis in the ferret. J. Virol. 86:7508-7519. http://dx.doi.org/10.1128/JVI.06725-11.
27. Nguyen DT, De Vries RD, Ludlow M, van den Hoogen BG, Lemon K, Van Amerongen G, Osterhaus AD, De Swart RL, Duprex WP. 2013. Paramyxovirus infections in ex vivo lung slice cultures of different host species. J. Virol. Methods 193:159-165. http://dx.doi.org/10.1016/j.jviromet.2013.06.016.
28. El Mubarak HS, Yüksel S, Van Amerongen G, Mulder PG, Mukhtar MM, Osterhaus AD, De Swart RL. 2007. Infection of cynomolgus macaques (Macaca fascicularis) and rhesus macaques (Macaca mulatta) with different wild-type measles viruses. J. Gen. Virol. 88:2028-2034. http://dx.doi.org/10.1099/vir.0.82804-0.
29. Reed LJ, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hygiene. 27:493-497.
30. de Swart RL, Vos HW, UytdeHaag FG, Osterhaus AD, Van Binnendijk RS. 1998. Measles virus fusion protein-and hemagglutinin-transfected cell lines are a sensitive tool for the detection of specific antibodies by a FACS-measured immunofluorescence assay. J. Virol. Methods 71:35-44. http://dx.doi.org/10.1016/S0166-0934(97)00188-2.
31. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH. 2005. Well-differentiated human airway epithelial cell cultures. Methods Mol. Med. 107:183-206. http://dx.doi.org/10.1385/1-59259-861-7:183.
32. 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. http://dx.doi.org/10.1111/j.1469-0691.2011.03480.x.
33. van Binnendijk RS, van der Heijden RW, Van Amerongen G, Uytde-Haag FG, Osterhaus AD. 1994. Viral replication and development of specific immunity in macaques after infection with different measles virus strains. J. Infect. Dis. 170:443-448. http://dx.doi.org/10.1093/infdis/170.2.443.
34. de Vries RD, McQuaid S, Van Amerongen G, Yüksel S, Verburgh RJ, Osterhaus AD, Duprex WP, De Swart RL. 2012. Measles immune suppression: lessons from the macaque model. PLoS Pathog. 8:e1002885. http://dx.doi.org/10.1371/journal.ppat.1002885.
35. Ludlow M, Lemon K, De Vries RD, McQuaid S, Millar E, Van Amerongen G, Yüksel 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 sub-epithelial immune cells. J. Virol. 87: 4033-4042. http://dx.doi.org/10.1128/JVI.03258-12.
36. Noyce RS, Richardson CD. 2012. Nectin 4 is the epithelial cell receptor for measles virus. Trends Microbiol. 20:429-439. http://dx.doi.org/10.1016/j.tim.2012.05.006.
37. Racaniello V. 2011. An exit strategy for measles virus. Science 334:1650-1651. http://dx.doi.org/10.1126/science.1217378.
38. Gaskin JM. 1974. Canine distemper virus in domesticated cats and pigs. Adv. Enzymol. Relat. Areas Mol. Biol. 40:803-806.
39. Appel MJ, Summers BA. 1995. Pathogenicity of morbilliviruses for terrestrial carnivores. Vet. Microbiol. 44:187-191. http://dx.doi.org/10.1016/0378-1135(95)00011-X.
40. Harder TC, Kenter M, Vos H, Siebelink K, Huisman W, Van Amerongen G, Örvell C, Barrett T, Appel MJ, Osterhaus AD. 1996. Canine distemper virus from large diseased felids: biological properties and phylogenetic relationships. J. Gen. Virol. 77:397-405. http://dx.doi.org/10.1099/0022-1317-77-3-397.
41. Appel MJ, Yates RA, Foley GL, Bernstein JJ, Santinelli S, Spelman LH, Miller LD, Arp LH, Anderson M, Barr M, Pearce-Kelling S, Summers BA. 1994. Canine distemper epizootic in lions, tigers, and leopards in North America. J. Vet. Diagn. Invest. 6:277-288. http://dx.doi.org/10.1177/104063879400600301.
42. Harder TC, Kenter M, Appel MJ, Roelke-Parker ME, Barrett T, Osterhaus AD. 1995. Phylogenetic evidence of canine distemper virus in Serengeti's lions. Vaccine 13:521-523. http://dx.doi.org/10.1016/0264-410X(95)00024-U.
43. Roelke-Parker ME, Munson L, Packer C, Kock R, Cleaveland S, Carpenter M, O'Brien SJ, Pospischil A, Hofmann-Lehmann R, Lutz H, Mwamengele GL, Mgasa MN, Machange GA, Summers BA, Appel MJ. 1996. A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379:441-445. http://dx.doi.org/10.1038/379441a0.
44. Nagao Y, Nishio Y, Shiomoda H, Tamaru S, Shimojima M, Goto M, Une Y, Sato A, Ikebe Y, Maeda K. 2012. An outbreak of canine distemper virus in tigers (Panthera tigris): possible transmission from wild animals to zoo animals. J. Vet. Med. Sci. 74:699-705. http://dx.doi.org/10.1292/jvms.11-0509.
45. Svansson V, Blixenkrone-Möller M, Skirnisson K, Have P, Heje NI, Nielsen J, Lund E. 1993. Infection studies with canine distemper virus in harbour seals. Arch. Virol. 131:349-359. http://dx.doi.org/10.1007/BF01378637.
46. Osterhaus AD. 1989. A morbillivirus causing mass mortality in seals. Vaccine 7:483-484. http://dx.doi.org/10.1016/0264-410X(89)90265-X.
47. Grachev MA, Kumarev VP, Mamaev LV, Zorin VL, Baranova LV, Denikjna NN, Belikov SI, Petrov EA, Kolesnik VS, Kolesnik RS, Dorofeev VM, Beim AM, Kudelin VN, Nagieva FG, Sidorov VN. 1989. Distemper virus in Baikal seals. Nature 338:209. http://dx.doi.org/10.1038/338209b0.
48. Kennedy S, Kuiken T, Jepson PD, Deaville R, Forsyth M, Barrett T, Van de Bildt MW, Osterhaus AD, Eybatov T, Duck C, Kydyrmanov A, Mitrofanov I, Wilson S. 2000. Mass die-Offof Caspian seals caused by canine distemper virus. Emerg. Infect. Dis. 6:637-639. http://dx.doi.org/10.3201/eid0606.000613.
49. Kuiken T, Kennedy S, Barrett T, Van de Bildt MWG, Borgsteede FH, Brew SD, Codd GA, Duck C, Deaville R, Eybatov T, Forsyth MA, Foster G, Jepson PD, Kydyrmanov A, Mitrofanov I, Ward CJ, Wilson S, Osterhaus AD. 2006. The 2000 canine distemper epidemic in Caspian seals (Phoca caspica): pathology and analysis of contributory factors. Vet. Pathol. 43:321-338. http://dx.doi.org/10.1354/vp.43-3-321.
50. DeLay PD, Stone SS, Karzon DT, Katz S, Enders J. 1965. Clinical and immune response of alien hosts to inoculation with measles, rinderpest, and canine distemper viruses. Am. J. Vet. Res. 26:1359-1373.
51. Imagawa DT, Goret P, Adams JM. 1960. Immunological relationships of measles, distemper, and rinderpest viruses. Proc. Natl. Acad. Sci. U. S. A. 46:1119-1123. http://dx.doi.org/10.1073/pnas.46.8.1119.
52. Sheshberadaran H, Norrby E, McCullough KC, Carpenter WC, Örvell C. 1986. The antigenic relationship between measles, canine distemper and rinderpest viruses studied with monoclonal antibodies. J. Gen. Virol. 67:1381-1392. http://dx.doi.org/10.1099/0022-1317-67-7-1381.
53. Örvell C, Norrby E. 1974. Further studies on the immunological relationships among measles, distemper, and rinderpest viruses. J. Immunol. 113: 1850-1858.
54. Gould EA, Armstrong M, Shirodaria PV, De'Ornellas D. 1981. Examination of the immunological relationship between measles virus and canine distemper virus using monospecific measles antisera. J. Med. Virol. 7:51-60. http://dx.doi.org/10.1002/jmv.1890070106.
55. Moura RA, Warren J. 1961. Subclinical infection of dogs by canineadapted measles virus evidenced by their subsequent immunity to canine distemper virus. J. Bacteriol. 82:702-705.
56. Taylor J, Pincus S, Tartaglia J, Richardson C, Alkhatib G, Briedis D, Appel MJ, Norton E, Paoletti E. 1991. Vaccinia virus recombinants expressing either the measles virus fusion or hemagglutinin glycoprotein protect dogs against canine distemper virus challenge. J. Virol. 65:4263-4274.