Antibody response in snakes with boid inclusion body disease


Autoři: Katharina Windbichler aff001;  Eleni Michalopoulou aff002;  Pia Palamides aff001;  Theresa Pesch aff001;  Christine Jelinek aff001;  Olli Vapalahti aff003;  Anja Kipar aff001;  Udo Hetzel aff001;  Jussi Hepojoki aff001
Působiště autorů: Institute of Veterinary Pathology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland aff001;  Department of Veterinary Pathology and Public Health, Institute of Veterinary Science, University of Liverpool, Liverpool, United Kingdom aff002;  University of Helsinki, Faculty of Veterinary Medicine, Department of Veterinary Biosciences, Helsinki, Finland aff003;  University of Helsinki, Faculty of Medicine, Medicum, Department of Virology, Helsinki, Finland aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0221863

Souhrn

Boid Inclusion Body Disease (BIBD) is a potentially fatal disease reported in captive boid snakes worldwide that is caused by reptarenavirus infection. Although the detection of intracytoplasmic inclusion bodies (IB) in blood cells serves as the gold standard for the ante mortem diagnosis of BIBD, the mechanisms underlying IB formation and the pathogenesis of BIBD are unknown. Knowledge on the reptile immune system is sparse compared to the mammalian counterpart, and in particular the response towards reptarenavirus infection is practically unknown. Herein, we investigated a breeding collection of 70 Boa constrictor snakes for BIBD, reptarenavirus viraemia, anti-reptarenavirus IgM and IgY antibodies, and population parameters. Using NGS and RT-PCR on pooled blood samples of snakes with and without BIBD, we could identify three different reptarenavirus S segments in the collection. The examination of individual samples by RT-PCR indicated that the presence of University of Giessen virus (UGV)-like S segment strongly correlates with IB formation. We could also demonstrate a negative correlation between BIBD and the presence of anti-UGV NP IgY antibodies. Further evidence of an association between antibody response and BIBD is the finding that the level of anti-reptarenavirus antibodies measured by ELISA was lower in snakes with BIBD. Furthermore, female snakes had a significantly lower body weight when they had BIBD. Taken together our findings suggest that the detection of the UGV-/S6-like S segment and the presence of anti-reptarenavirus IgY antibodies might serve as a prognostic tool for predicting the development of BIBD.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Animals – Vertebrates – Amniotes – Reptiles – Squamates – Snakes – Molecular biology – Molecular biology techniques – Artificial gene amplification and extension – Polymerase chain reaction – Reverse transcriptase-polymerase chain reaction – Physiology – Antibodies – Antibody response – Biochemistry – Proteins – Immune system proteins – Cell biology – Cellular types – Animal cells – Blood cells – Research and analysis methods – Immunologic techniques – Immunoassays – Enzyme-linked immunoassays – Medicine and health sciences – Immune physiology – Immunology – Immune response


Zdroje

1. Keller S, Hetzel U, Sironen T, Korzyukov Y, Vapalahti O, Kipar A, et al. Co-infecting Reptarenaviruses Can Be Vertically Transmitted in Boa Constrictor. PLoS Pathog. 2017; 13: e1006179. doi: 10.1371/journal.ppat.1006179 28114434

2. Schumacher J, Jacobson ER, Homer BL, Gaskin JM. Inclusion Body Disease in Boid Snakes. Journal of Zoo and Wildlife Medicine. 1994; 25: 511–524.

3. Chang L-W, Jacobson E. Inclusion Body Disease, A Worldwide Infectious Disease of Boid Snakes: A Review. Journal of Exotic Pet Medicine. 2010; 19.

4. Wozniak E, McBride J, DeNardo D, Tarara R, Wong V, Osburn B. Isolation and characterization of an antigenically distinct 68-kd protein from nonviral intracytoplasmic inclusions in Boa constrictors chronically infected with the inclusion body disease virus (IBDV: Retroviridae). Vet Pathol. 2000; 37: 449–459. doi: 10.1354/vp.37-5-449 11055868

5. Bodewes R, Kik MJL, Raj VS, Schapendonk CME, Haagmans BL, Smits SL, et al. Detection of novel divergent arenaviruses in boid snakes with inclusion body disease in The Netherlands. J Gen Virol. 2013; 94: 1206–1210. doi: 10.1099/vir.0.051995-0 23468423

6. Stenglein MD, Sanders C, Kistler AL, Ruby JG, Franco JY, Reavill DR, et al. Identification, characterization, and in vitro culture of highly divergent arenaviruses from boa constrictors and annulated tree boas: candidate etiological agents for snake inclusion body disease. MBio. 2012; 3: e00180–12. doi: 10.1128/mBio.00180-12 22893382

7. Hetzel U, Sironen T, Laurinmaki P, Liljeroos L, Patjas A, Henttonen H, et al. Isolation, identification, and characterization of novel arenaviruses, the etiological agents of boid inclusion body disease. J Virol. 2013; 87: 10918–10935. doi: 10.1128/JVI.01123-13 23926354

8. Stenglein MD, Sanchez-Migallon Guzman D, Garcia VE, Layton ML, Hoon-Hanks LL, Boback SM, et al. Differential Disease Susceptibilities in Experimentally Reptarenavirus-Infected Boa Constrictors and Ball Pythons. J Virol. 2017; 91.

9. Maes P, Adkins S, Alkhovsky SV, Avsic-Zupanc T, Ballinger MJ, Bente DA, et al. Taxonomy of the order Bunyavirales: second update 2018. Arch Virol. 2019; 164: 927–941. doi: 10.1007/s00705-018-04127-3 30663021

10. Hepojoki J, Hepojoki S, Smura T, Szirovicza L, Dervas E, Prahauser B, et al. Characterization of Haartman Institute snake virus-1 (HISV-1) and HISV-like viruses-The representatives of genus Hartmanivirus, family Arenaviridae. PLoS Pathog. 2018; 14: e1007415. doi: 10.1371/journal.ppat.1007415 30427944

11. Hepojoki J, Salmenpera P, Sironen T, Hetzel U, Korzyukov Y, Kipar A, et al. Arenavirus Coinfections Are Common in Snakes with Boid Inclusion Body Disease. J Virol. 2015; 89: 8657–8660. doi: 10.1128/JVI.01112-15 26041290

12. Stenglein MD, Jacobson ER, Chang L-W, Sanders C, Hawkins MG, Guzman DS-M, et al. Widespread recombination, reassortment, and transmission of unbalanced compound viral genotypes in natural arenavirus infections. PLoS Pathog. 2015; 11: e1004900. doi: 10.1371/journal.ppat.1004900 25993603

13. Chang L-W. Development of molecular diagnostic tests for Inclusion body disease in boid snakes. PhD Thesis, University of Florida. 2012. Available: http://ufdc.ufl.edu/UFE0045011/00001.

14. Korzyukov Y, Hetzel U, Kipar A, Vapalahti O, Hepojoki J. Generation of Anti-Boa Immunoglobulin Antibodies for Serodiagnostic Applications, and Their Use to Detect Anti-Reptarenavirus Antibodies in Boa Constrictor. PLoS One. 2016; 11: e0158417. doi: 10.1371/journal.pone.0158417 27355360

15. Martinez-Sobrido L, Giannakas P, Cubitt B, Garcia-Sastre A, de la Torre Juan Carlos. Differential inhibition of type I interferon induction by arenavirus nucleoproteins. J Virol. 2007; 81: 12696–12703. doi: 10.1128/JVI.00882-07 17804508

16. Martinez-Sobrido L, Zuniga EI, Rosario D, Garcia-Sastre A, de la Torre Juan Carlos. Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J Virol. 2006; 80: 9192–9199. doi: 10.1128/JVI.00555-06 16940530

17. Fan L, Briese T, Lipkin WI. Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J Virol. 2010; 84: 1785–1791. doi: 10.1128/JVI.01362-09 20007272

18. Meyer B, Ly H. Inhibition of Innate Immune Responses Is Key to Pathogenesis by Arenaviruses. J Virol. 2016; 90: 3810–3818. doi: 10.1128/JVI.03049-15 26865707

19. Borden KL, Campbell Dwyer EJ, Salvato MS. An arenavirus RING (zinc-binding) protein binds the oncoprotein promyelocyte leukemia protein (PML) and relocates PML nuclear bodies to the cytoplasm. J Virol. 1998; 72: 758–766. 9420283

20. Salomoni P, Pandolfi PP. The role of PML in tumor suppression. Cell. 2002; 108: 165–170. doi: 10.1016/s0092-8674(02)00626-8 11832207

21. Zimmerman LM, Vogel LA, Bowden RM. Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol. 2010; 213: 661–671. doi: 10.1242/jeb.038315 20154181

22. Jaffredo T, Fellah JS, Dunon D. Immunology of Birds and Reptiles; 2006.

23. Galabov AS, Velichikova EH. Interferon production in tortoise peritoneal cells. J Gen Virol. 1975; 28: 259–263. doi: 10.1099/0022-1317-28-2-259 1100778

24. Mondal S, Rai U. In vitro effect of temperature on phagocytic and cytotoxic activities of splenic phagocytes of the wall lizard, Hemidactylus flaviviridis. Comp Biochem Physiol A Mol Integr Physiol. 2001; 129: 391–398. 11423311

25. Mondal S, Rai U. In vitro effect of sex steroids on cytotoxic activity of splenic macrophages in wall lizard (Hemidactylus flaviviridis). Gen Comp Endocrinol. 2002; 125: 264–271. doi: 10.1006/gcen.2001.7744 11884072

26. Shang S, Zhong H, Wu X, Wei Q, Zhang H, Chen J, et al. Genomic evidence of gene duplication and adaptive evolution of Toll like receptors (TLR2 and TLR4) in reptiles. International Journal of Biological Macromolecules. 2018; 109: 698–703. doi: 10.1016/j.ijbiomac.2017.12.123 29292152

27. Voogdt CGP, Bouwman LI, Kik MJL, Wagenaar JA, van Putten, Jos P. M. Reptile Toll-like receptor 5 unveils adaptive evolution of bacterial flagellin recognition. Scientific Reports. 2016; 6: 19046 EP -. doi: 10.1038/srep19046 26738735

28. Zhou Y, Liang Q, Li W, Gu Y, Liao X, Fang W, et al. Characterization and functional analysis of toll-like receptor 4 in Chinese soft-shelled turtle Pelodiscus sinensis. Developmental & Comparative Immunology. 2016; 63: 128–135.

29. Merchant M, Williams S, Trosclair PL3, Elsey RM, Mills K. Febrile response to infection in the American alligator (Alligator mississippiensis). Comp Biochem Physiol A Mol Integr Physiol. 2007; 148: 921–925. doi: 10.1016/j.cbpa.2007.09.016 17977038

30. Kluger MJ, Ringler DH, Anver MR. Fever and survival. Science. 1975; 188: 166–168. 1114347

31. A Farag M, El Ridi R. Mixed leucocyte reaction (MLR) in the snake Psammophis sibilans. Immunology. 1985; 55.

32. El Ridi R, Zada S, Afifi A, El Deeb S, El Rouby S, Farag M, et al. Cyclic changes in the differentiation of lymphoid cells in reptiles. Cell Differentiation. 1988; 24: 1–8. 3044615

33. Munoz FJ, La Fuente M de. The effect of the seasonal cycle on the splenic leukocyte functions in the turtle Mauremys caspica. Physiol Biochem Zool. 2001; 74: 660–667. doi: 10.1086/323033 11517451

34. Ansar Ahmed S, Penhale WJ, Talal N. Sex hormones, immune responses, and autoimmune diseases. Mechanisms of sex hormone action. Am J Pathol. 1985; 121: 531–551. 3907369

35. Klein SL. Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol. 2004; 26: 247–264. doi: 10.1111/j.0141-9838.2004.00710.x 15541029

36. Saad AH. Sex-associated differences in the mitogenic responsiveness of snake blood lymphocytes. Developmental & Comparative Immunology. 1989; 13: 225–229.

37. Gambon-Deza F, Sanchez-Espinel C, Mirete-Bachiller S, Magadan-Mompo S. Snakes antibodies. Developmental & Comparative Immunology. 2012; 38: 1–9.

38. Warr GW, Magor KE, Higgins DA. IgY: clues to the origins of modern antibodies. Immunol Today. 1995; 16: 392–398. doi: 10.1016/0167-5699(95)80008-5 7546196

39. Coe JE, Leong D, Portis JL, Thomas LA. Immune response in the garter snake (Thamnophis ordinoides). Immunology. 1976; 31: 417–424. 1027724

40. Kendall Salanitro S. Immune Response of Snakes. Copeia. 1973; 1973: 504–515.

41. Chang L-W, Fu A, Wozniak E, Chow M, Duke DG, Green L, et al. Immunohistochemical detection of a unique protein within cells of snakes having inclusion body disease, a world-wide disease seen in members of the families Boidae and Pythonidae. PLoS One. 2013; 8: e82916. doi: 10.1371/journal.pone.0082916 24340066

42. Cohen J. A Coefficient of Agreement for Nominal Scales. Educational and Psychological Measurement. 1960; 20: 37–46.

43. Hepojoki J, Kipar A, Korzyukov Y, Bell-Sakyi L, Vapalahti O, Hetzel U, et al. Replication of Boid Inclusion Body Disease-Associated Arenaviruses Is Temperature Sensitive in both Boid and Mammalian Cells. J Virol. 2015; 89: 1119. doi: 10.1128/JVI.03119-14 25378485

44. Elliott R. Jacobson. Infectious Diseases and Pathology of Reptiles: Color Atlas and Text. 1st ed. Boca Raton: CRC Press Inc; 2007.

45. Ujvari B, Madsen T. Do natural antibodies compensate for humoral immunosenescence in tropical pythons. Functional Ecology. 2011; 25: 813–817.

46. Holodick NE, Rodríguez-Zhurbenko N, Hernández AM. Defining Natural Antibodies. Frontiers in immunology. 2017; 8: 872. doi: 10.3389/fimmu.2017.00872 28798747

47. Mims CA. Vertical transmission of viruses. Microbiol Rev. 1981; 45: 267–286. 6790919

48. HOTCHIN J WEIGAN DH. Studies of lymphocytic choriomeningitis in mice. I. The relationship between age at inoculation and outcome of infection. J Immunol. 1961; 86: 392–400. 13716107

49. Zhou X, Ramachandran S, Mann M, Popkin DL. Role of lymphocytic choriomeningitis virus (LCMV) in understanding viral immunology: past, present and future. Viruses. 2012; 4: 2650–2669. doi: 10.3390/v4112650 23202498

50. Thomsen AR, Volkert M, Marker O. Different isotype profiles of virus-specific antibodies in acute and persistent lymphocytic choriomeningitis virus infection in mice. Immunology. 1985; 55: 213–223. 4007926

51. Sevilla N, Kunz S, McGavern D, Oldstone MBA. Infection of dendritic cells by lymphocytic choriomeningitis virus. Curr Top Microbiol Immunol. 2003; 276: 125–144. 12797446

52. Cao W, Henry MD, Borrow P, Yamada H, Elder JH, Ravkov EV, et al. Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science. 1998; 282: 2079–2081. doi: 10.1126/science.282.5396.2079 9851928

53. Borrow P, Evans CF, Oldstone MB. Virus-induced immunosuppression: immune system-mediated destruction of virus-infected dendritic cells results in generalized immune suppression. J Virol. 1995; 69: 1059–1070. 7815484

54. Doyle MV, Oldstone MB. Interactions between viruses and lymphocytes. I. In vivo replication of lymphocytic choriomeningitis virus in mononuclear cells during both chronic and acute viral infections. J Immunol. 1978; 121: 1262–1269. 308960

55. Chang L, Fu D, Stenglein MD, Hernandez JA, DeRisi JL, Jacobson ER. Detection and prevalence of boid inclusion body disease in collections of boas and pythons using immunological assays. Vet J. 2016; 218: 13–18. doi: 10.1016/j.tvjl.2016.10.006 27938703

56. Aubert RD, Kamphorst AO, Sarkar S, Vezys V, Ha S-J, Barber DL, et al. Antigen-specific CD4 T-cell help rescues exhausted CD8 T cells during chronic viral infection. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108: 21182–21187. doi: 10.1073/pnas.1118450109 22160724

57. Oxenius A, Zinkernagel RM, Hengartner H. Comparison of activation versus induction of unresponsiveness of virus-specific CD4+ and CD8+ T cells upon acute versus persistent viral infection. Immunity. 1998; 9: 449–457. 9806631

58. Borrow P, Martinez-Sobrido L, de la Torre, Juan Carlos. Inhibition of the type I interferon antiviral response during arenavirus infection. Viruses. 2010; 2: 2443–2480. doi: 10.3390/v2112443 21994626

59. Chang L, Fu D, Stenglein MD, Hernandez JA, DeRisi JL, Jacobson ER. Detection and prevalence of boid inclusion body disease in collections of boas and pythons using immunological assays. Vet J. 2016; 218: 13–18. doi: 10.1016/j.tvjl.2016.10.006 27938703

60. Dervas E, Hepojoki J, Laimbacher A, Romero-Palomo F, Jelinek C, Keller S, et al. Nidovirus-Associated Proliferative Pneumonia in the Green Tree Python (Morelia viridis). J Virol. 2017.

61. Hepojoki J, Kipar A, Korzyukov Y, Bell-Sakyi L, Vapalahti O, Hetzel U, et al. Replication of Boid Inclusion Body Disease-Associated Arenaviruses Is Temperature Sensitive in both Boid and Mammalian Cells. J Virol. 2015; 89: 1119 doi: 10.1128/JVI.03119-14 25378485


Článok vyšiel v časopise

PLOS One


2019 Číslo 9

Najčítanejšie v tomto čísle

Tejto téme sa ďalej venujú…


Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Faktory ovlivňující léčbu levotyroxinem
nový kurz

Kurz originály vs. generika

Autori: MUDr. Petr Výborný, CSc., FEBO

Autori: MUDr. Jiří Horažďovský, Ph.D

Klinická farmakokinetika betablokátorů

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa