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Quantitative analysis of Northern bobwhite (Colinus virginianus) cytokines and TLR expression to eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula) glycoproteins

  • Aravindan Kalyanasundaram
  • Kendall R. Blanchard
  • Brett J. Henry
  • Cassandra Henry
  • Matthew Z. Brym
  • Ronald J. KendallEmail author
Immunology and Host-Parasite Interactions - Original Paper

Abstract

Helminth parasites have been a popular research topic due to their global prevalence and adverse effects on livestock and game species. The Northern bobwhite (Colinus virginianus), a popular game bird in the USA, is one species subject to helminth infection and has been experiencing a decline of > 4% annually over recent decades. In the Rolling Plains Ecoregion of Texas, the eyeworm (Oxyspirura petrowi) and caecal worm (Aulonocephalus pennula) helminths are found to be highly prevalent in bobwhite. While there have been increasing studies on the prevalence, pathology, and phylogeny of the eyeworm and caecal worm, there is still a need to investigate the bobwhite immune response to infection. This study utilizes previously sequenced bobwhite cytokines and toll-like receptors to develop and optimize qPCR primers and measure gene expression in bobwhite intramuscularly challenged with eyeworm and caecal worm glycoproteins. For the challenge experiments, separate treatments of eyeworm and caecal worm glycoproteins were administered to bobwhite on day 1 and day 21. Measurements of primary and secondary immune responses were taken at day 7 and day 28, respectively. Using the successfully optimized qPCR primers for TLR7, IL1β, IL6, IFNα, IFNγ, IL10, and β-actin, the gene expression analysis from the challenge experiments revealed that there was a measurable immune reaction in bobwhite in response to the intramuscular challenge of eyeworm and caecal worm glycoproteins.

Keywords

Bobwhite Caecal Eyeworm Cytokine qPCR TLR 

Notes

Funding information

This research received funding and support form Park Cities Quail Coalition and the Rolling Plains Quail Research Foundation.

Compliance with ethical standards

This study contains no conflicts of interest. This experiment was approved by Texas Tech University Animal Care and Use Committee under protocol number 18044-05 and 16071-08 for bobwhite collection. All bobwhites were trapped and handled according to Texas Parks and Wildlife permit SPR-0715-095.

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Abdul-Cader MS, Amarasinghe A, Abdul-Careem MF (2016) Activation of toll-like receptor signaling pathways leading to nitric oxide-mediated antiviral responses. Arch Virol 161:2075–2086CrossRefGoogle Scholar
  2. Abdul-Cader MS, Senapathi UDS, Nagy E, Sharif S, Abdul-Careem MF (2018) Antiviral response elicited against avian influenza virus infection following activation of toll-like receptor (TLR)7 signaling pathway is attributable to interleukin (IL)-1β production. BMC Res Notes 11:859CrossRefGoogle Scholar
  3. Addison EM, Anderson RC (1969) A review of eye worms of the genus Oxyspirura (Nematoda: Spiruroidea). J Wildl Dis 55:1–58Google Scholar
  4. Albonico M, Allen H, Chitsulo L, Engels D, Gabrielli A-F, Savioli L (2008) Controlling soil-transmitted helminthiasis in pre-school-age children through preventive chemotherapy. PLoS Negl Trop Dis 2:e126CrossRefGoogle Scholar
  5. Alves CR, Silva FS, Oliveira-Junior FO, Pereira BAS, Pires FA, MCS P (2012) Affinity-based methods for the separation of parasite proteins. In: Magdeldin S (ed) Affinity Chromatography. InTech, Rijeka, Croatia, pp 333–356Google Scholar
  6. Alzabin S, Kong P, Medghalchi M, Palfreeman A, Williams R, Sacre S (2012) Investigation of the role of endosomal toll-like receptors in murine collagen-induced arthritis reveals a potential role for TLR7 in disease maintenance. Arthritis Res Ther 14:R142CrossRefGoogle Scholar
  7. Amrani DL, Mauzy-Melitz D, Mosesson MW (1986) Effect of hepatocyte-stimulating factor and glucocorticoids on plasma fibronectin levels. Biochem J 238:365–371CrossRefGoogle Scholar
  8. Appleton JA, Bell RG, Homan W, Van Knapen F (1991) Consensus on Trichinella spiralis antigens and antibodies. Parasitol Today 7:190–192CrossRefGoogle Scholar
  9. Babu S, Nutman TB (2003) Proinflammatory cytokines dominate the early immune response to filarial parasites. J Immunol 171:6723–6732CrossRefGoogle Scholar
  10. Barua P, Barua N, Hazarika NK, Das S (2005) Loa loa in the anterior chamber of the eye: a case report. Indian J Med Microbiol 23:59–60CrossRefGoogle Scholar
  11. Behnke JM, Barnard CJ, Wakelin D (1992) Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. Int J Parasitol 22:861–907CrossRefGoogle Scholar
  12. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367:1521–1532CrossRefGoogle Scholar
  13. Bruno A, Fedynich AM, Smith-Herron A, Rollins D (2015) Pathological response of Northern bobwhites to Oxyspirura petrowi infections. J Parasitol 101:364–368CrossRefGoogle Scholar
  14. Bruno A, Fedynich AM, Rollins D, Wester DB (2018) Helminth communities and host dynamics in Northern bobwhites from the Rolling Plains Ecoregion, USA. J. Helminthol 29:1–7Google Scholar
  15. Brym MZ, Henry C, Kendall RJ (2018) Elevated parasite burdens as a potential mechanism affecting Northern bobwhite (Colinus virginianus) population dynamics in the Rolling Plains of West Texas. Parasitol Res 117:1683–1688CrossRefGoogle Scholar
  16. Chandler AC (1935) A new genus and species of Subulurinae (Nematodes). Trans Am Microsc Soc 54:33–35CrossRefGoogle Scholar
  17. Charlier J, Soenen K, De Roeck E, Hantson W, Ducheyne E, Van Coillie F, De Wulf R, Hendrickx G, Vercruysse J (2014) Longitudinal study on the temporal and micro-spatial distribution of Galba truncatula in four farms in Belgium as a base for small-scale risk mapping of Fasciola hepatica. Parasit Vectors 7:528CrossRefGoogle Scholar
  18. Christe P, Møller AP, de Lope F (1998) Immuno-competence and nestling survival in the house martin: the tasty chick hypothesis. Oikos 83:175–179CrossRefGoogle Scholar
  19. Commons KA, Blanchard KR, Brym MZ, Henry C, Kalyanasundaram A, Skinner K, Kendall RJ (2019) Monitoring Northern bobwhite (Colinus virginianus) populations in the Rolling Plains of Texas: Implications of parasitic infection. Rangeland Ecology and Management.  https://doi.org/10.1016/j.rama.2019.04.004
  20. Cram EB (1937) A review of the genus Oxyspirura, with a morphological study of O. petrowi Skrjabin 1929, recently discovered in galliform birds of the Northern United States. In Papers on Helminthology Published in Commemoration of the 30 Year Jubileum of K. I. Skrjabin and of the 15th Anniversary of the All-Union Institute of Helminthology, Moscow, pp 89–98Google Scholar
  21. Cummings RD, Nyame AK (1996) Glycobiology of schistosomiasis. The FASEB J 10:838–848CrossRefGoogle Scholar
  22. van Die I, Cummings RD (2010) Glycan gimmickry by parasitic helminths: a strategy for modulating the host immune response? Glycobiology 20:2–12CrossRefGoogle Scholar
  23. Dunham NR, Soliz LA, Fedynich AM, Rollins D, Kendall RJ (2014) Evidence of an Oxyspirura petrowi epizootic in Northern bobwhites (Colinus virginianus). J Wildl Dis 50:552–558CrossRefGoogle Scholar
  24. Dunham NR, Bruno A, Almas S, Rollins D, Fedynich AM, Presley SM, Kendall RJ (2016) Eyeworms (Oxyspirura petrowi) in Northern bobwhite (Colinus virginianus) from the Rolling Plains of Texas and Oklahoma, 2011–2013. J Wildl Dis 52:562–567CrossRefGoogle Scholar
  25. Dunham NR, Peper ST, Downing C, Brake E, Rollins D, Kendall RJ (2017a) Infection levels of eyeworm Oxyspirura petrowi and caecal worm Aulonocephalus pennula in the Northern bobwhite and scaled quail from the Rolling Plains of Texas. J Helminthol 91:569–577CrossRefGoogle Scholar
  26. Dunham NR, Henry C, Brym M, Rollins D, Helman RG, Kendall RJ (2017b) Caecal worm, Aulonocephalus pennula, infection in the Northern bobwhite quail, Colinus virginianus. Int J Parasitol Parasites Wildl 6:35–38CrossRefGoogle Scholar
  27. Greter H, Cowan N, Ngandolo BN, Kessely H, Alfaroukh IO, Utzinger J, Keiser J, Zinsstag J (2017) Treatment of human and livestock helminth infections in a mobile pastoralist setting at Lake Chad: Attitudes to health and analysis of active pharmaceutical ingredients of locally available anthelminthic drugs. Acta Trop 175:91–99CrossRefGoogle Scholar
  28. Guthery FS (2002) The technology of bobwhite management. Iowa State Press, AmesGoogle Scholar
  29. Halley YA, Dowd SE, Decker JE, Seabury PM, Bhattarai E (2014) A draft de novo genome assembly for the Northern bobwhite (Colinus virginianus) reveals evidence for a rapid decline in effective population size beginning in the late Pleistocene. PLoS One 9:e90240CrossRefGoogle Scholar
  30. Haslam SM, Khoo KH, Houston KM, Harnett W, Morris HR, Dell A (1997) Characterisation of the phosphorylcholine-containing N-linked oligosaccharides in the excretory-secretory 62 kDa glycoprotein of Acanthocheilonema viteae. Mol Biochem Parasitol 85:53–66CrossRefGoogle Scholar
  31. Henry C, Brym MZ, Kendall RJ (2017) Oxyspirura petrowi and Aulonocephalus pennula infection in wild Northern bobwhite quail in the Rolling Plains Ecoregion, Texas: possible evidence of a die-off. Arch Parasitol 1:2Google Scholar
  32. Hernández F, Guthery FS, Kuvlesky WP Jr (2002) The legacy of bobwhite research in south Texas. J Wildl Manag 66:1–18CrossRefGoogle Scholar
  33. Hernández F, Brennan LA, DeMaso SJ, Sands JP, Wester DB (2013) On reversing the Northern bobwhite population decline: 20 years later. Wildl Soc Bull 37:177–188CrossRefGoogle Scholar
  34. Hewitson JP, Grainger JR, Maizels RM (2009) Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 167:1–11CrossRefGoogle Scholar
  35. Hoerauf A, Mand S, Adjei O, Fleischer B, Buttner DW (2001) Depletion of Wolbachia endobacteria in Onchocerca volvulus by doxycycline and microfilaridermia after ivermectin treatment. Lancet 357:1415–1416CrossRefGoogle Scholar
  36. Holly FJ, Lemp MA (1977) Tear physiology and dry eyes. Surv Ophthalmol 22:69–87CrossRefGoogle Scholar
  37. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J (2008) Helminth infections: the great neglected tropical diseases. J Clin Invest 118:1311–1321CrossRefGoogle Scholar
  38. Hudson PJ, Newborn D, Dobson AP (1992) Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. I. Monitoring and parasite reduction experiments. J Anim Ecol 61:477–486Google Scholar
  39. Jackson AS (1969) Quail management handbook for West Texas Rolling Plains. Bulletin Number 48. Texas Parks and Wildlife Department, AustinGoogle Scholar
  40. Johnson JL, Rollins D, Reyna KS (2012) What’s a quail worth? A longitudinal assessment of quail hunter demographics, attitudes, and spending habits in Texas. Proc Nat Quail Sym 7:294–299Google Scholar
  41. Kaiser P, Balic A (2015) The avian immune system. In: Scanes CG (ed) Sturkie’s Avian Physiology. Academic Press, USA, pp 403–418CrossRefGoogle Scholar
  42. Kaiser P, Stäheli P (2014) Avian Cytokines and Chemokines. In: Schat KA, Kaspers B, Kaiser P (eds) Avian Immunology, 2nd edn. Academic Press, Amsterdam, pp 189–204CrossRefGoogle Scholar
  43. Kaiser P, Rothwell L, Galyov EE, Barrow PA, Burnside J, Wigley P (2000) Differential cytokine expression in avian cells in response to invasion by Salmanella typhimurium, Salmonella enteritidis, and Salmonella gallinarum. Microbiology 12:3217–3226CrossRefGoogle Scholar
  44. Kalyanasundaram A, Blanchard KR, Kendall RJ (2017) Molecular identification and characterization of partial COX1 gene from caecal worm (Aulonocephalus pennula) in Northern bobwhite (Colinus virginianus) from the Rolling Plains Ecoregion of Texas. Int J Parasitol Parasites Wildl 6:195–201CrossRefGoogle Scholar
  45. Kalyanasundaram A, Blanchard KR, Henry C, Brym MZ, Kendall RJ (2018) Phylogenetic analysis of eyeworm (Oxyspirura petrowi) in Northern bobwhite quail (Colinus virginianus) based on the nuclear 18S rDNA and mitochondrial cytochrome oxidase 1 gene (COX1). Parasitology Open 15:65–70Google Scholar
  46. Kamal SM, Khalifa KES (2006) Immune modulation by helminthic infections: worms and viral infections. Parasite Immunol 28:483–496CrossRefGoogle Scholar
  47. Kellogg FE, Prestwood AE (1968) Gastrointestinal helminths from wild and pen-raised bobwhite. J Wildl Manag 32:468–475CrossRefGoogle Scholar
  48. Killpack TL, Karasov WH (2012) Ontogeny of adaptive antibody response to a model antigen in captive altricial zebra finches. PLoS One 7:e47294CrossRefGoogle Scholar
  49. King CH (2007) Lifting the burden of schistosomiasis – defining elements of infection–associated disease and the benefits of anti-parasite treatment. J Infect Dis 196:653–655CrossRefGoogle Scholar
  50. King CL, Mahanty S, Kumaraswami V, Abrams SS, Regunathan J, Ottesen EA, Nutman TB (1993) Cytokine control of parasite-specific anergy in human lymphatic filariasis. Preferential induction of a regulatory T helper type 2 lymphocyte subset. J Clin Invest 92:1667–1673CrossRefGoogle Scholar
  51. Kishimoto T, Akira S, Narazaki M, Taga T (1995) Interleukin-6 family of cytokines and gp130. Blood 86:1243–1254Google Scholar
  52. Kistler WM, Parlos JA, Peper ST, Dunham NR, Kendall RJ (2016) A quantitative PCR protocol for detection of Oxyspirura petrowi in Northern bobwhites (Colinus virginianus). PLoS One 11:e0166309CrossRefGoogle Scholar
  53. Kopko SH, Martin DS, Barta JR (2000) Responses of chickens to a recombinant refractile body antigen of Eimeria tenella administered using various immunizing strategies. Poult Sci 79:336–342CrossRefGoogle Scholar
  54. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRefGoogle Scholar
  55. Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immuno-competence in Northern bobwhite chicks. Auk 110:503–510CrossRefGoogle Scholar
  56. Lung NP, Thompson JP, Kollias GV Jr, Olsen JH, Zdziarski JM, Klein PA (1996) Maternal immunoglobulin G antibody transfer and development of immunoglobulin G antibody responses in blue and gold macaw (Ara ararauna) chicks. Am J Vet Res 57:1162–1167Google Scholar
  57. Lynagh GR, Bailey M, Kaiser P (2000) Interleukin-6 is produced during both murine and avian Eimeria infections. Vet Immunol Immunopathol 76:89–102CrossRefGoogle Scholar
  58. Maizels RM, Yazdanbakhsh M (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Rev. Immunol 3:733–744CrossRefGoogle Scholar
  59. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE (2004) Helminth parasites: masters of regulation. Immunol Rev. 201:89–116CrossRefGoogle Scholar
  60. McClure HE (1949) The eyeworm, Oxyspirura petrowi, in Nebraska pheasants. J Wildl Manag 13:304–307CrossRefGoogle Scholar
  61. Mogensen TH (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev. 22:240–273CrossRefGoogle Scholar
  62. Mosser DM, Karp CL (1999) Receptor mediated subversion of macrophage cytokine production by intracellular pathogens. Curr Opin Immunol 11:406–411CrossRefGoogle Scholar
  63. Muhsin M, Ajendra J, Gentil K, Berbudi A, Neumann AL, Klaas L, Schmidt KE, Hoerauf A, Hübner MP (2018) IL-6 is required for protective immune responses against early filarial infection. Int J Parasitol 48:925–935CrossRefGoogle Scholar
  64. Munn EA, Greenwood CA, Coadwell WJ (1987) Vaccination of young lambs by means of a protein fraction extracted from adult Haemonchus contortus. Parasitol 94:385–397CrossRefGoogle Scholar
  65. Nayak B, Sinha S, Nayak L (2016) Loa loa in the vitreous cavity of the eye. BMJ Case Rep.  https://doi.org/10.1136/bcr-2015-213,879
  66. Nordling D, Andersson M, Zohari S, Gustafsson L (1998) Reproductive effort reduces specific immune response and parasite resistance. Proc R Soc Lond B 265:1291–1298CrossRefGoogle Scholar
  67. Oldeschulte DL, Halley YA, Wilson ML, Bhattarai EK, Brashear W, Hill J, Metz RP, Johnson CD, Rollins D, Peterson MJ, Bickhart DM, Decker JE, Sewell JF, Seabury CM (2017) Annotated draft genome assemblies for the Northern bobwhite (Colinus virginianus) and the Scaled quail (Callipepla squamata) reveal disparate estimates of modern genome diversity and historic effective population size. G3 (Bethesda) 7:3047–3058CrossRefGoogle Scholar
  68. Payne AP (1994) The Harderian gland: a tercentennial review. J Anat 185:1–49Google Scholar
  69. Pei J, Sekellick MJ, Marcus PI, Choi IS, Collisson EW (2001) Chicken interferon type I inhibits infectious bronchitis virus replication and associated respiratory illness. J Interferon Cytokine Res 21:1071–1077CrossRefGoogle Scholar
  70. Pence DB (1972) The genus Oxyspirura (Nematoda:Thelaziidae) from birds in Louisiana. Proc Helminthol Soc Wash 39:23–28Google Scholar
  71. Philibin VJ, Iqbal M, Boyd Y, Goodchild MJ, Beal RK, Bumstead N, Young J, Smith AL (2005) Identification and characterization of a functional, alternatively spliced toll-like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunology 114:507–521CrossRefGoogle Scholar
  72. Robel RJ, Walker TL, Hagen CA, Ridley RK, Kemp KE, Applegate RD (2003) Helminth parasites of the lesser prairie-chicken in southwestern Kansas: incidence, burdens, and effects. Wild Biol 9:341–350CrossRefGoogle Scholar
  73. Rollins D (1980) Comparative ecology of bobwhite and scaled quail in mesquite grassland habitats. M. S. Thesis Oklahoma State University, Stillwater, Oklahoma, USAGoogle Scholar
  74. Saino N, Calza S, Møller AP (1997) Immuno-competence of nestling barn swallows in relation to brood size and parental effort. J Anim Ecol 66:827–836CrossRefGoogle Scholar
  75. Sauer JR, Link WA, Fallon JE, Pardieck KL, Ziolkowski DJ Jr (2013) The North American breeding bird survey 1966–2011: summary analysis and species accounts. N Am Fauna 79:1–32CrossRefGoogle Scholar
  76. Saunders GB (1935) Michigan’s studies of sharp-tailed grouse. In Transactions of the American Game Conference 21:342–344Google Scholar
  77. Schmid-Hempel P (2009) Immune defence, parasite evasion strategies and their relevance for macroscopic phenomena such as virulence. Philos Trans R Soc Lond B Biol Sci 364:85–98CrossRefGoogle Scholar
  78. Smith KA, Maizels RM (2014) IL-6 controls susceptibility to helminth infection by impeding Th2 responsiveness and altering the Treg phenotype in vivo. Eur J Immunol 44:150–161CrossRefGoogle Scholar
  79. Turner PV, Brabb T, Pekow C, Vasbinder MA (2011) Administration of substances to laboratory animals: routes of administration and factors to consider. J Am Assoc Lab Anim Sci 50:600–613Google Scholar
  80. Uematsu S, Akira S (2006) Toll-like receptors and innate immunity. J Mol Med 84:712–725CrossRefGoogle Scholar
  81. Umar S, Arif M, Shah MAA, Munir MT, Yaqoob M, Ahmed S, Khan MI, Younus M, Shahzad M (2015) Application of avian cytokines as immuno-modulating agents. World Poultry Sci J 71:643–653CrossRefGoogle Scholar
  82. Whelan M, Harnett MM, Houston KM, Patel V, Harnett W, Rigley KP (2000) A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J Immunol 164:6453–6460CrossRefGoogle Scholar
  83. Wigley P, Kaiser P (2003) Avian cytokines in health and disease. Brazilian J Poult Sci 5:1–14CrossRefGoogle Scholar
  84. Yu AT, Blackburn BG (2019) Soil-transmitted helminths: Ascaris, Trichurus, and hookworm infections. In: Selendy JMH, Farmer P, Fawzi W (eds) Water and sanitation-related diseases and changing environment: challenges, interventions, and preventative measures, 2nd edn. Wiley, New York, pp 95–110Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.The Wildlife Toxicology LaboratoryTexas Tech UniversityLubbockUSA

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