Regional adaptations and parallel mutations in Feline panleukopenia virus strains from China revealed by nearly-full length genome analysis

Autoři: Élcio Leal aff001;  Ruiying Liang aff001;  Qi Liu aff001;  Fabiola Villanova aff002;  Lijun Shi aff001;  Lin Liang aff001;  Jinxiang Li aff001;  Steven S. Witkin aff004;  Shangjin Cui aff001
Působiště autorů: Chinese Academy of Agricultural Sciences, Institute of Animal Sciences, Beijing, China aff001;  Federal University of Pará, Belém, Pará, Brazil aff002;  Beijing Observation Station for Veterinary Drug and Veterinary Biotechnology, Ministry of Agriculture, Beijing, China aff003;  Department of Obstetrics and Gynecology, Weill Cornell Medicine, New York, NY, United States of America aff004;  Institute of Tropical Medicine, Sao Paulo, Brazil aff005
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


Protoparvoviruses, widespread among cats and wild animals, are responsible for leukopenia. Feline panleukopenia virus (FPLV) in domestic cats is genetically diverse and some strains may differ from those used for vaccination. The presence of FPLV in two domestic cats from Hebei Province in China was identified by polymerase chain reaction. Samples from these animals were used to isolate FPLV strains in CRFK cells for genome sequencing. Phylogenetic analysis was performed to compare our isolates with available sequences of FPLV, mink parvovirus (MEV) and canine parvovirus (CPV). The isolated strains were closely related to strains of FPLV/MEV isolated in the 1960s. Our analysis also revealed that the evolutionary history of FPLV and MEV is characterized by local adaptations in the Vp2 gene. Thus, it is likely that new FPLV strains are emerging to evade the anti-FPLV immune response.

Klíčová slova:

Amino acid sequence analysis – Carnivory – DNA sequence analysis – Domestic animals – Mammalian genomics – Phylogenetic analysis – Polymerase chain reaction – Parvoviruses


1. Cotmore S.F.; Agbandje-McKenna M.; Chiorini J.A.; Mukha D.V.; Pintel D.J.; Qiu J; et al. The family parvoviridae. Arch Virol 2014, 159, 1239–1247. doi: 10.1007/s00705-013-1914-1 24212889

2. Decaro N.; Camero M.; Greco G.; Zizzo N.; Tinelli A.; Campolo M.; et al. Canine distemper and related diseases: Report of a severe outbreak in a kennel. New Microbiol 2004, 27, 177–181. 15164629

3. Demeter Z.; Gal J.; Palade E.A.; Rusvai M. Feline parvovirus infection in an asian palm civet (paradoxurus hermaphroditus). Vet Rec 2009, 164, 213–216. doi: 10.1136/vr.164.7.213 19218594

4. Guo L.; Yang S.L.; Chen S.J.; Zhang Z.; Wang C.; Hou R.; et al. Identification of canine parvovirus with the q370r point mutation in the vp2 gene from a giant panda (ailuropoda melanoleuca). Virol J 2013, 10, 163. doi: 10.1186/1743-422X-10-163 23706032

5. Kariatsumari T.; Horiuchi M.; Hama E.; Yaguchi K.; Ishigurio N.; Goto H.; et al. Construction and nucleotide sequence analysis of an infectious DNA clone of the autonomous parvovirus, mink enteritis virus. J Gen Virol 1991, 72 (Pt 4), 867–875.

6. Uttenthal A.; Larsen S.; Lund E.; Bloom M.E.; Storgard T.; Alexandersen S. Analysis of experimental mink enteritis virus infection in mink: In situ hybridization, serology, and histopathology. J Virol 1990, 64, 2768–2779. 2159543

7. Yang S.; Wang S.; Feng H.; Zeng L.; Xia Z.; Zhang R.; et al. Isolation and characterization of feline panleukopenia virus from a diarrheic monkey. Vet Microbiol 2010, 143, 155–159. doi: 10.1016/j.vetmic.2009.11.023 20044220

8. Yuan D.; Wang J.; Li Z.; Mao Y.; Sun J.Z.; Xi J.; et al. Establishment of a rescue system for an autonomous parvovirus mink enteritis virus. Virus Res 2014, 183, 1–5. doi: 10.1016/j.virusres.2014.01.012 24463297

9. Zhang R.; Yang S.; Zhang W.; Zhang T.; Xie Z.; Feng H.; et al. Phylogenetic analysis of the vp2 gene of canine parvoviruses circulating in china. Virus Genes 2010, 40, 397–402. doi: 10.1007/s11262-010-0466-7 20217205

10. Zhou L.; Tang Q.; Shi L.; Kong M.; Liang L.; Mao Q.; et al. Full-length genomic characterization and molecular evolution of canine parvovirus in china. Virus Genes 2016, 52, 411–416. doi: 10.1007/s11262-016-1309-y 27038801

11. Christensen J.; Tattersall P. Parvovirus initiator protein ns1 and rpa coordinate replication fork progression in a reconstituted DNA replication system. J Virol 2002, 76, 6518–6531. doi: 10.1128/JVI.76.13.6518-6531.2002 12050365

12. Allison A.B.; Kohler D.J.; Fox K.A.; Brown J.D.; Gerhold R.W.; Shearn-Bochsler V.I.; et al. Frequent cross-species transmission of parvoviruses among diverse carnivore hosts. J Virol 2013, 87, 2342–2347. doi: 10.1128/JVI.02428-12 23221559

13. Allison A.B.; Kohler D.J.; Ortega A.; Hoover E.A.; Grove D.M.; Holmes E.C.; et al. Host-specific parvovirus evolution in nature is recapitulated by in vitro adaptation to different carnivore species. PLoS Pathog 2014, 10, e1004475. doi: 10.1371/journal.ppat.1004475 25375184

14. Canuti M.; Britton A.P.; Graham S.M.; Lang A.S. Epidemiology and molecular characterization of protoparvoviruses infecting wild raccoons (procyon lotor) in british columbia, canada. Virus Res 2017, 242, 85–89. doi: 10.1016/j.virusres.2017.09.015 28947335

15. Horiuchi M.; Yamaguchi Y.; Gojobori T.; Mochizuki M.; Nagasawa H.; Toyoda Y.; et al. Differences in the evolutionary pattern of feline panleukopenia virus and canine parvovirus. Virology 1998, 249, 440–452. doi: 10.1006/viro.1998.9335 9791034

16. Steinel A.; Munson L.; van Vuuren M.; Truyen U. Genetic characterization of feline parvovirus sequences from various carnivores. J Gen Virol 2000, 81, 345–350. doi: 10.1099/0022-1317-81-2-345 10644832

17. Stucker K.M.; Pagan I.; Cifuente J.O.; Kaelber J.T.; Lillie T.D.; Hafenstein S.; et al. The role of evolutionary intermediates in the host adaptation of canine parvovirus. J Virol 2012, 86, 1514–1521. doi: 10.1128/JVI.06222-11 22114336

18. Truyen U.; Gruenberg A.; Chang S.F.; Obermaier B.; Veijalainen P.; Parrish C.R. Evolution of the feline-subgroup parvoviruses and the control of canine host range in vivo. J Virol 1995, 69, 4702–4710. 7609035

19. Truyen U.; Parrish C.R. Feline panleukopenia virus: Its interesting evolution and current problems in immunoprophylaxis against a serious pathogen. Vet Microbiol 2013, 165, 29–32. doi: 10.1016/j.vetmic.2013.02.005 23561891

20. Miranda C.; Thompson G. Canine parvovirus: The worldwide occurrence of antigenic variants. J Gen Virol 2016, 97, 2043–2057. doi: 10.1099/jgv.0.000540 27389721

21. Parrish C.R. Host range relationships and the evolution of canine parvovirus. Vet Microbiol 1999, 69, 29–40. doi: 10.1016/s0378-1135(99)00084-x 10515266

22. Steinel A.; Parrish C.R.; Bloom M.E.; Truyen U. Parvovirus infections in wild carnivores. J Wildl Dis 2001, 37, 594–607. doi: 10.7589/0090-3558-37.3.594 11504234

23. Battilani M.; Scagliarini A.; Ciulli S.; Morganti L.; Prosperi S. High genetic diversity of the vp2 gene of a canine parvovirus strain detected in a domestic cat. Virology 2006, 352, 22–26. doi: 10.1016/j.virol.2006.06.002 16822535

24. Govindasamy L.; Hueffer K.; Parrish C.R.; Agbandje-McKenna M. Structures of host range-controlling regions of the capsids of canine and feline parvoviruses and mutants. J Virol 2003, 77, 12211–12221. doi: 10.1128/JVI.77.22.12211-12221.2003 14581558

25. Parrish C.R.; Aquadro C.F.; Strassheim M.L.; Evermann J.F.; Sgro J.Y.; Mohammed H.O. Rapid antigenic-type replacement and DNA sequence evolution of canine parvovirus. J Virol 1991, 65, 6544–6552. 1942246

26. Hoelzer K.; Parrish C.R. The emergence of parvoviruses of carnivores. Vet Res 2010, 41, 39. doi: 10.1051/vetres/2010011 20152105

27. Pereira C.A.; Leal E.S.; Durigon E.L. Selective regimen shift and demographic growth increase associated with the emergence of high-fitness variants of canine parvovirus. Infect Genet Evol 2007, 7, 399–409. doi: 10.1016/j.meegid.2006.03.007 16716762

28. Shackelton L.A.; Parrish C.R.; Truyen U.; Holmes E.C. High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc Natl Acad Sci U S A 2005, 102, 379–384. doi: 10.1073/pnas.0406765102 15626758

29. Horiuchi M.; Ishiguro N.; Goto H.; Shinagawa M. Characterization of the stage(s) in the virus replication cycle at which the host-cell specificity of the feline parvovirus subgroup is regulated in canine cells. Virology 1992, 189, 600–608. doi: 10.1016/0042-6822(92)90583-b 1322591

30. Leal E.; Villanova F.E.; Lin W.; Hu F.; Liu Q.; Liu Y.; et al. Interclade recombination in porcine parvovirus strains. J Gen Virol 2012, 93, 2692–2704. doi: 10.1099/vir.0.045765-0 22993191

31. Villanova F.; Cui S.; Ai X.; Leal E. Analysis of full-length genomes of porcine teschovirus (ptv) and the effect of purifying selection on phylogenetic trees. Arch Virol 2016, 161, 1199–1208. doi: 10.1007/s00705-015-2744-0 26860913

32. Wang X.; Li T.; Liu H.; Du J.; Zhou F.; Dong Y.; et al. Recombinant feline parvovirus infection of immunized tigers in central china. Emerg Microbes Infect 2017, 6, e42. doi: 10.1038/emi.2017.25 28588292

33. Decaro N.; Desario C.; Miccolupo A.; Campolo M.; Parisi A.; Martella V.; et al.Genetic analysis of feline panleukopenia viruses from cats with gastroenteritis. J Gen Virol 2008, 89, 2290–2298. doi: 10.1099/vir.0.2008/001503-0 18753239

34. Larkin M.A.; Blackshields G.; Brown N.P.; Chenna R.; McGettigan P.A.; McWilliam H.; et al. Clustal w and clustal x version 2.0. Bioinformatics 2007, 23, 2947–2948. doi: 10.1093/bioinformatics/btm404 17846036

35. Kumar S.; Stecher G.; Li M.; Knyaz C.; Tamura K. Mega x: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018, 35, 1547–1549. doi: 10.1093/molbev/msy096 29722887

36. Martin D.P.; Murrell B.; Golden M.; Khoosal A.; Muhire B. Rdp4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 2015, 1, vev003. doi: 10.1093/ve/vev003 27774277

37. Whelan S.; Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001, 18, 691–699. doi: 10.1093/oxfordjournals.molbev.a003851 11319253

38. Liu C.; Liu Y.; Liu D.; Qiu Z.; Tian J.; Guo D.; et al. Complete genome sequence of feline panleukopenia virus strain hrb-cs1, isolated from a domestic cat in northeastern china. Genome Announc 2015, 3.

39. Duarte M.D.; Barros S.C.; Henriques M.; Fernandes T.L.; Bernardino R.; Monteiro M.; et al. Fatal infection with feline panleukopenia virus in two captive wild carnivores (panthera tigris and panthera leo). J Zoo Wildl Med 2009, 40, 354–359. doi: 10.1638/2008-0015.1 19569486

40. Risi E.; Agoulon A.; Allaire F.; Le Drean-Quenec'hdu S.; Martin V.; Mahl P. Antibody response to vaccines for rhinotracheitis, caliciviral disease, panleukopenia, feline leukemia, and rabies in tigers (panthera tigris) and lions (panthera leo). J Zoo Wildl Med 2012, 43, 248–255. doi: 10.1638/2010-0166.1 22779227

Článek vyšel v časopise


2020 Číslo 1
Nejčtenější tento týden