Exploring the host transcriptome for mechanisms underlying protective immunity and resistance to nematode infections in ruminants

Veterinary Parasitology

Volumn 190, Issue 1-2, 2012, Pages 1-11

  Li, Robert W ^a   Choudhary, Ratan K ^a   Capuco, Anthony V ^a   Urban Jr , Joseph F ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Nematode; Parasite; Pathways; Resistance; Ruminant; Transcriptome

Indexed keywords

ALPHA 1,3 FUCOSYLTRANSFERASE; CELL ADHESION MOLECULE; INTERLEUKIN 13; INTERLEUKIN 25; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 9; STEM CELL FACTOR; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA;

ADAPTIVE IMMUNITY; BOVIDS; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GASTROINTESTINAL INFECTION; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; NEMATODIASIS; NONHUMAN; PARASITE CONTROL; PARASITE IMMUNITY; PATHOGEN LOAD; PROTEIN EXPRESSION; QUANTITATIVE TRAIT LOCUS; REGULATOR GENE; REVIEW; RNA SEQUENCE; RUMINANT STOMACH; SMALL INTESTINE; TH2 CELL; TRANSCRIPTION REGULATION;

ANIMALS; DISEASE RESISTANCE; DISEASE SUSCEPTIBILITY; GENE REGULATORY NETWORKS; GENOMICS; HOST-PARASITE INTERACTIONS; INTESTINAL DISEASES, PARASITIC; NEMATODA; NEMATODE INFECTIONS; QUANTITATIVE TRAIT LOCI; RUMINANTS; TRANSCRIPTOME;

ANIMALIA; PROTOZOA;

EID: 84867142122     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2012.06.021     Document Type: Review

References (120)

1. Albers G.A., Gray G.D., Piper L.R., Barker J.S., Le Jambre L.F., Barger I.A. The genetics of resistance and resilience to Haemonchus contortus infection in young merino sheep. Int. J. Parasitol. 1987, 17:1355-1363.
2. Almería S., Canals A., Zarlenga D.S., Gasbarre L.C. Isolation and phenotypic characterization of abomasal mucosal lymphocytes in the course of a primary Ostertagia ostertagi infection in calves. Vet. Immunol. Immunopathol. 1997, 57:87-98.
3. Amarante A.F., Craig T., Ramsey W., El-Sayed N., Desouki A., Bazer F. Comparison of naturally acquired parasite burdens among Florida Native. Rambouillet and crossbreed ewes. Vet. Parasitol. 1999, 85:61-69.
4. Andronicos N., Hunt P., Windon R. Expression of genes in gastrointestinal and lymphatic tissues during parasite infection in sheep genetically resistant or susceptible to Trichostrongylus colubriformis and Haemonchus contortus. Int. J. Parasitol. 2010, 40:417-429.
5. Anthony R.M., Urban J.F., Alem F., Hamed H.A., Rozo C.T., Boucher J.L., Van R.N., Gause W.C. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 2006, 12:955-960.
6. Araujo R.N., Padilha T., Zarlenga D., Sonstegard T., Connor E.E., Van Tassel C., Lima W.S., Nascimento E., Gasbarre L.C. Use of a candidate gene array to delineate gene expression patterns in cattle selected for resistance or susceptibility to intestinal nematodes. Vet. Parasitol. 2009, 162:106-115.
7. Artis D., Grencis R.K. The intestinal epithelium: sensors to effectors in nematode infection. Mucosal Immunol. 2008, 1:252-264.
8. Artis D., Wang M.L., Keilbaugh S.A., He W., Brenes M., Swain G.P., Knight P.A., Donaldson D.D., Lazar M.A., Miller H.R., Schad G.A., Scott P., Wu G.D. RELMbeta/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13596-13600.
9. Athanasiadou S., Jones L.A., Burgess S.T., Kyriazakis I., Pemberton A.D., Houdijk J.G., Huntley J.F. Genome-wide transcriptomic analysis of intestinal tissue to assess the impact of nutrition and a secondary nematode challenge in lactating rats. PLoS One 2011, 6:e20771.
10. Athanasiadou S., Pemberton A., Jackson F., Inglis N., Miller H.R., Thévenod F., Mackellar A., Huntley J.F. Proteomic approach to identify candidate effector molecules during the in vitro immune exclusion of infective Teladorsagia circumcincta in the abomasum of sheep. Vet. Res. 2008, 39:58.
11. Baldwin R.L., Wu S., Li W., Li C., Bequette B.J., Li R.W. Quantification of transcriptome responses of the rumen epithelium to butyrate infusion using RNA-seq technology. Gene Regul. Syst. Biol. 2012, 6:67-80.
12. Barger I.A., Gibbs H.C. Milk production of cows infected experimentally with trichostrongylid parasites. Vet. Parasitol. 1981, 9:69-73.
13. Bassetto C.C., Silva B.F., Newlands G.F.J., Smith W.D., Amarante A.F.T. Protection of calves against Haemonchus placei and Haemonchus contortus after immunization with gut membrane proteins from H. contortus. Parasite Immunol. 2011, 33:377-381.
14. Bell L.V., Else K.J. Mechanisms of leucocyte recruitment to the inflamed large intestine: redundancy in integrin and addressin usage. Parasite Immunol. 2008, 30:163-170.
15. Beraldi D., McRae A.F., Gratten J., Pilkington J.G., Slate J., Visscher P.M., Pemberton J.M. Quantitative trait loci (QTL) mapping of resistance to strongyles and coccidia in the free-living Soay sheep (Ovis aries). Int. J. Parasitol. 2007, 37:121-129.
16. Bogdan C. Nitric oxide and the immune response. Nat. Immunol. 2001, 2:907-916.
17. Bolormaa S., van der Werf J.H.J., Walkden-Brown S.W., Marshall K., Ruvinsky A. A quantitative trait locus for faecal worm egg and blood eosinophil counts on chromosome 23 in Australian goats. J. Anim. Breed. Genet. 2010, 127:207-214.
18. Brady M.T., O'Neill S.M., Dalton J.P., Mills K.H. Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infect. Immun. 1999, 67:5372-5378.
19. Brailsford T.J., Behnke J.M. The dynamics of trickle infections with Heligmosomoides polygyrus in syngeneic strains of mice. Int. J. Parasitol. 1992, 22:351-359.
20. Bricarello P.A., Zaros L.G., Coutinho L.L., Rocha R.A., Kooyman F.N.J., De Vries E., Gonçalves J.R.S., Lima L.G., Pires A.V., Amarante A.F.T. Field study on nematode resistance in Nellore-breed cattle. Vet. Parasitol. 2007, 148:272-278.
21. Burke J., Miller J. Relative resistance to gastrointestinal nematode parasites in Dorper, Katahdin, and St. Croix lambs under conditions encountered in the southeastern region of the United States. Small Ruminant Res. 2004, 54:43-51.
22. Canals A., Zarlenga D.S., Almeria S., Gasbarre L.C. Cytokine profile induced by a primary infection with Ostertagia ostertagi in cattle. Vet. Immunol. Immunopathol. 1997, 58:63-75.
23. Charlier J., Claerebout E., Duchateau L., Vercruysse J. A survey to determine relationships between bulk tank milk antibodies against Ostertagia ostertagi and milk production parameters. Vet. Parasitol. 2005, 129:67-75.
24. Charlier J., Höglund J., von Samson-Himmelstjerna G., Dorny P., Vercruysse J. Gastrointestinal nematode infections in adult dairy cattle: impact on production, diagnosis and control. Vet. Parasitol. 2009, 164:70-79.
25. Chen C.C., Louie S., McCormick B.A., Walker W.A., Shi H.N. Helminth-primed dendritic cells alter the host response to enteric bacterial infection. J. Immunol. 2006, 176:472-483.
26. Chen F., Liu Z., Wu W., Rozo C., Bowdridge S., Millman A., Van R.N., Urban J.F., Wynn T.A., Gause W.C. An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection. Nat. Med. 2012, 18:260-266.
27. Claerebout E., Vercauteren I., Geldhof P., Olbrechts A., Zarlenga D.S., Goddeeris B.M., Vercruysse J. Cytokine responses in immunized and non-immunized calves after Ostertagia ostertagi infection. Parasite Immunol. 2005, 27:325-331.
28. Cliffe L.J., Humphreys N.E., Lane T.E., Potten C.S., Booth C., Grencis R.K. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 2005, 308:1463-1465.
29. Colditz I.G. Six costs of immunity to gastrointestinal nematode infections. Parasite Immunol. 2008, 30:63-70.
30. Coop R.L., Sykes A.R., Angus K.W. The pathogenicity of daily intakes of Cooperia oncophora larvae in growing calves. Vet. Parasitol. 1979, 5:261-269.
31. Coop R.L., Kyriazakis I. Nutrition-parasite interaction. Vet. Parasitol. 1999, 84:187-204.
32. Coppieters W., Mes T.H.M., Druet T., Farnir F., Tamma N., Schrooten C., Cornelissen A.W.C.A., Georges M., Ploeger H.W. Mapping QTL influencing gastrointestinal nematode burden in Dutch Holstein-Friesian dairy cattle. BMC Genomics 2009, 10:96.
33. Cox M.P., Peterson D.A., Biggs P.J. SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform. 2010, 11:485.
34. Crawford A.M., Paterson K.A., Dodds K.G., Diez Tascon C., Williamson P.A., Roberts Thomson M., Bisset S.A., Beattie A.E., Greer G.J., Green R.S., et al. Discovery of quantitative trait loci for resistance to parasitic nematode infection in sheep: I. Analysis of outcross pedigrees. BMC Genomics 2006, 7:178.
35. de la Fuente A. From 'differential expression' to 'differential networking'-identification of dysfunctional regulatory networks in diseases. Trends Genet. 2010, 26:326-333.
36. Dervishi E., Uriarte J., Valderrábano J., Calvo J.H. Structural and functional characterisation of the ovine interferon gamma (IFNG) gene: its role in nematode resistance in Rasa Aragonesa ewes. Vet. Immunol. Immunopathol. 2011, 141:100-108.
37. deSchoolmeester M.L., Manku H., Else K.J. The innate immune responses of colonic epithelial cells to Trichuris muris are similar in mouse strains that develop a type 1 or type 2 adaptive immune response. Infect. Immun. 2006, 74:6280-6286.
38. Diez-Tascón C., Keane O.M., Wilson T., Zadissa A., Hyndman D.L., Baird D.B., McEwan J.C., Crawford A.M. Microarray analysis of selection lines from outbred populations to identify genes involved with nematode parasite resistance in sheep. Physiol. Genomics 2005, 21:59-69.
39. Dominik S., Hunt P.W., McNally J., Murrell A., Hall A., Purvis I.W. Detection of quantitative trait loci for internal parasite resistance in sheep. I. Linkage analysis in a Romney×Merino sheep backcross population. Parasitology 2010, 137:1275-1282.
40. Dubois P.C., Trynka G., Franke L., Hunt K.A., Romanos J., Curtotti A., Zhernakova A., Heap G.A., Adany R., Aromaa A., Bardella M.T., van den Berg L.H., Bockett N.A., de la Concha E.G., Dema B., Fehrmann R.S., Fernandez-Arquero M., Fiatal S., Grandone E., Green P.M., Groen H.J., Gwilliam R., Houwen R.H., Hunt S.E., Kaukinen K., Kelleher D., Korponay-Szabo I., Kurppa K., MacMathuna P., Maki M., Mazzilli M.C., McCann O.T., Mearin M.L., Mein C.A., Mirza M.M., Mistry V., Mora B., Morley K.I., Mulder C.J., Murray J.A., Nunez C., Oosterom E., Ophoff R.A., Polanco I., Peltonen L., Platteel M., Rybak A., Salomaa V., Schweizer J.J., Sperandeo M.P., Tack G.J., Turner G., Veldink J.H., Verbeek W.H., Weersma R.K., Wolters V.M., Urcelay E., Cukrowska B., Greco L., Neuhausen S.L., McManus R., Barisani D., Deloukas P., Barrett J.C., Saavalainen P., Wijmenga C., van Heel D.A. Multiple common variants for celiac disease influencing immune gene expression. Nat. Genet. 2010, 42:295-302.
41. Dunphy J.L., Balic A., Barcham G.J., Horvath A.J., Nash A.D., Meeusen E.N. Isolation and characterization of a novel inducible mammalian galectin. J. Biol. Chem. 2000, 275:32106-32113.
42. Dynes R.A., Poppi D.P., Barrell G.K., Sykes A.R. Elevation of feed intake in parasite-infected lambs by central administration of a cholecystokinin receptor antagonist. Br. J. Nutr. 1998, 79:47-54.
43. Else K.J., Hultner L., Grencis R.K. Cellular immune responses to the murine nematode parasite Trichuris muris, II. Differential induction of TH-cell subsets in resistant versus susceptible mice. Immunology 1992, 75:232-237.
44. Emery D.L., McClure S.J., Wagland B.M. Production of vaccines against gastrointestinal nematodes of livestock. Immunol. Cell Biol. 1993, 71(Pt 5):463-472.
45. FAO technical co-operation project in Malaysia TCP/MAL/0065 (T) Biological Control of Nematode Parasites of Small Ruminants in Asia 2002, http://cnia.inta.gov.ar/helminto/pdf%20alternativos/FAO_TCP_MAL_0065%28T%291.pdf.
46. Finkelman F.D., Urban J.F. The other side of the coin: the protective role of the TH2 cytokines. J. Allergy Clin. Immunol. 2001, 107:772-780.
47. Finkelman F.D., Shea-Donohue T., Morris S.C., Gildea L., Strait R., Madden K.B., Schopf L., Urban J.F. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 2004, 201:139-155.
48. French A.T., Bethune J.A., Knight P.A., McNeilly T.N., Wattegedera S., Rhind S., Miller H.R., Pemberton A.D. The expression of intelectin in sheep goblet cells and upregulation by interleukin-4. Vet. Immunol. Immunopathol. 2007, 120:41-46.
49. French A.T., Knight P.A., Smith W.D., Pate J.A., Miller H.R., Pemberton A.D. Expression of three intelectins in sheep and response to a Th2 environment. Vet. Res. 2009, 40:53.
50. Gasbarre L.C. Effects of gastrointestinal nematode infection on the ruminant immune system. Vet. Parasitol. 1997, 72:327-337.
51. Gasbarre L.C., Leighton E.A., Davies C.J. Influence of host genetics upon antibody responses against gastrointestinal nematode infections in cattle. Vet. Parasitol. 1993, 46:81-91.
52. Gasbarre L.C., Leighton E.A., Sonstegard T. Role of the bovine immune system and genome in resistance to gastrointestinal nematodes. Vet. Parasitol. 2001, 98:51-64.
53. Gasbarre L.C., Smith L.L., Hoberg E., Pilitt P.A. Further characterization of a cattle nematode population with demonstrated resistance to current anthelmintics. Vet. Parasitol. 2009, 166:275-280.
54. Gibson J.P. Strategies for Utilizing Molecular Marker Data for Livestock Genetic Improvement in the Developing World. Electronic Forum on Biotechnology in Food and Agriculture-Marker Assisted Selection: A Fast Track to Increase Genetic Gain in Plant and Animal Breeding 2005, http://www.fao.org/biotech/Torino.htm2005.
55. Gupta G., Surolia A. Collectins: sentinels of innate immunity. Bioessays 2007, 29:452-464.
56. Hansen S., Holm D., Moeller V., Vitved L., Bendixen C., Reid K.B., Skjoedt K., Holmskov U. CL-46, a novel collectin highly expressed in bovine thymus and liver. J. Immunol. 2002, 169:5726-5734.
57. Hasnain S.Z., Evans C.M., Roy M., Gallagher A.L., Kindrachuk K.N., Barron L., Dickey B.F., Wilson M.S., Wynn T.A., Grencis R.K., Thornton D.J. Muc5ac: a critical component mediating the rejection of enteric nematodes. J. Exp. Med. 2011, 208:893-900.
58. Hein W.R., Pernthaner A., Piedrafita D., Meeusen E.N. Immune mechanisms of resistance to gastrointestinal nematode infections in sheep. Parasite Immunol. 2010, 32:541-548.
59. Holtenius K., Persson Waller K., Essén-Gustavsson B., Holtenius P., Hallén S.C. Metabolic parameters and blood leukocyte profiles in cows from herds with high or low mastitis incidence. Vet. J. 2004, 168:65-73.
60. Hoorens P., Rinaldi M., Mihi B., Dreesen L., Grit G., Meeusen E., Li R.W., Geldhof P. Galectin-11 induction in the gastrointestinal tract of cattle following nematode and protozoan infections. Parasite Immunol. 2011, 33:669-678.
61. Hoste H., Torres-Acosta J.F., Aguilar-Caballero A.J. Nutrition-parasite interactions in goats: is immunoregulation involved in the control of gastrointestinal nematodes?. Parasite Immunol. 2008, 30:79-88.
62. Hoste H., Torres-Acosta J.F. Non chemical control of helminths in ruminants: adapting solutions for changing worms in a changing world. Vet. Parasitol. 2011, 180:144-154.
63. Hughes P.L., McKenna P.B., Dowling A.F. A survey of the prevalence of emerging macrocyclic lactone resistance and of benzimidazole resistance in sheep nematodes in the lower North Island of New Zealand. N. Z. Vet. J. 2005, 53:87-90.
64. Ingham A., Reverter A., Windon R., Hunt P., Menzies M. Gastrointestinal nematode challenge induces some conserved gene expression changes in the gut mucosa of genetically resistant sheep. Int. J. Parasitol. 2008, 38:431-442.
65. Jackson J.A., Turner J.D., Kamal M., Wright V., Bickle Q., Else K.J., Ramsan M., Bradley J.E. Gastrointestinal nematode infection is associated with variation in innate immune responsiveness. Microbes Infect. 2006, 8:487-492.
66. Johnston C.E., Bradley J.E., Behnke J.M., Matthews K.R., Else K.J. Isolates of Trichuris muris elicit different adaptive immune responses in their murine host. Parasite Immunol. 2005, 27:69-78.
67. Kadarmideen H.N., Watson-Haigh N.S., Andronicos N.M. Systems biology of ovine intestinal parasite resistance: disease gene modules and biomarkers. Mol. Biosyst. 2011, 7:235-246.
68. Keane O.M., Zadissa A., Wilson T., Hyndman D.L., Greer G.J., Baird D.B., McCulloch A.F., Crawford A.M., McEwan J.C. Gene expression profiling of naive sheep genetically resistant and susceptible to gastrointestinal nematodes. BMC Genomics 2006, 7:42-53.
69. Khan I.A., Hakak R., Eberle K., Sayles P., Weiss L.M., Urban J.F. Coinfection with Heligmosomoides polygyrus fails to establish CD8+ T-cell immunity against Toxoplasma gondii. Infect. Immun. 2008, 76:1305-1313.
70. Khodoun M., Strait R., Orekov T., Hogan S., Karasuyama H., Herbert D.R., Kohl J., Finkelman F.D. Peanuts can contribute to anaphylactic shock by activating complement. J. Allergy Clin. Immunol. 2009, 123:342-351.
71. Kijas J.W., Lenstra J.A., Hayes B., Boitard S., Porto Neto L.R., San C.M., Servin B., McCulloch R., Whan V., Gietzen K., Paiva S., Barendse W., Ciani E., Raadsma H., McEwan J., Dalrymple B. Genome-wide analysis of the world's sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biol. 2012, 10:e1001258.
72. Knight J.S., Baird D.B., Hein W.R., Pernthaner A. The gastrointestinal nematode Trichostrongylus colubriformis down-regulates immune gene expression in migratory cells in afferent lymph. BMC Immunol. 2010, 11:51.
73. Lasky L.A. Lectin cell adhesion molecules (LEC-CAMs): a new family of cell adhesion proteins involved with inflammation. J. Cell. Biochem. 1991, 45:139-146.
74. LeJambre L.F., Windon R.G., Smith W.D. Vaccination against Haemonchus contortus: performance of native parasite gut membrane glycoproteins in Merino lambs grazing contaminated pasture. Vet. Parasitol. 2008, 153:302-312.
75. Li R.W., Sonstegard T.S., Van Tassell C.P., Gasbarre L.C. Local inflammation as a possible mechanism of resistance to gastrointestinal nematodes in Angus heifers. Vet. Parasitol. 2007, 145:100-107.
76. Li R.W., Gasbarre L.C. A temporal shift in regulatory networks and pathways in the bovine small intestine during Cooperia oncophora infection. Int. J. Parasitol. 2009, 39:813-824.
77. Li R.W., Hou Y., Li C., Gasbarre L.C. Localized complement activation in the development of protective immunity against Ostertagia ostertagi infections in cattle. Vet. Parasitol. 2010, 174:247-256.
78. Li R.W., Gasbarre L.C. Gene expression in the bovine gastrointestinal tract during nematode infection. Veterinary Parasitology 2010, 157-178. Nova, New York. G.V. LaMann (Ed.).
79. Li R.W., Rinaldi M., Capuco A.V. Characterization of the abomasal transcriptome for mechanisms of resistance to gastrointestinal nematodes in cattle. Vet. Res. 2011, 42:114.
80. Li R.W., Li C.J., Gasbarre L.C. The vitamin D receptor and inducible nitric oxide synthase associated pathways in acquired resistance to Cooperia oncophora infection in cattle. Vet. Res. 2011, 42:48. 10.1186/1297-9716-42-48.
81. Li R.W., Schroeder S.G. Cytoskeleton remodeling and alterations in smooth muscle contractility in the bovine jejunum during nematode infection. Funct. Integr. Genomics 2012, 12:35-44.
82. Maizels R.M., Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 2003, 3:733-744.
83. Mandonnet N., Aumont G., Fleury J., Arquet R., Varo H., Gruner L., Bouix J., Khang J.V. Assessment of genetic variability of resistance to gastrointestinal nematode parasites in Creole goats in the humid tropics. J. Anim. Sci. 2001, 79:1706-1712.
84. Marshall K., Maddox J.F., Lee S.H., Zhang Y., Kahn L., Graser H.-U., Gondro C., Walkden-Brown S.W., van der Werf J.H.J. Genetic mapping of quantitative trait loci for resistance to Haemonchus contortus in sheep. Anim. Genet. 2009, 40:262-272.
85. McDermott J.R., Leslie F.C., D'Amato M., Thompson D.G., Grencis R.G., McLaughlin.J.T. Immune control of food intake: enteroendocrine cells are regulated by CD4+ T lymphocytes during small intestinal inflammation. Gut 2006, 55:492-497.
86. Meeusen E.N., Balic A., Bowles V. Cells, cytokines and other molecules associated with rejection of gastrointestinal nematode parasites. Vet. Immunol. Immunopathol. 2005, 108:121-125.
87. Michaelson J.J., Loguercio S., Beyer A. Detection and interpretation of expression quantitative trait loci (eQTL). Methods 2009, 48:265-276.
88. Miller J.E., Horohov D.W. Immunological aspects of nematode parasite control in sheep. J. Anim. Sci. 2006, 84(Suppl):E124-E132.
89. Montgomery S.B., Dermitzakis E.T. From expression QTLs to personalized transcriptomics. Nat. Rev. Genet. 2011, 12:277-282.
90. Moran A.P. Relevance of fucosylation and Lewis antigen expression in the bacterial gastroduodenal pathogen Helicobacter pylori. Carbohydr. Res. 2008, 343:1952-1965.
91. Mortensen L.L., Williamson L.H., Terrill T.H., Kircher R.A., Larsen M., Kaplan R.M. Evaluation of prevalence and clinical implications of anthelmintic resistance in gastrointestinal nematodes in goats. J. Am. Vet. Med. Assoc. 2003, 223:495-500.
92. Musson M.C., Jepeal L.I., Finnerty J.R., Wolfe M.M. Evolutionary expression of glucose-dependent-insulinotropic polypeptide (GIP). Regul. Pept. 2011, 171:26-34.
93. Muturi K.N., Scaife J.R., Lomax M.A., Jackson F., Huntley J., Coop R.L. The effect of dietary polyunsaturated fatty acids (PUFA) on infection with the nematodes Ostertagia ostertagi and Cooperia oncophora in calves. Vet. Parasitol. 2005, 129:273-283.
94. Nagaraj S.H., Harsha H.C., Reverter A., Colgrave M.L., Sharma R., Andronicos N., Hunt P., Menzies M., Lees M.S., Sekhar N.R., Pandey A., Ingham A. Proteomic analysis of the abomasal mucosal response following infection by the nematode, Haemonchus contortus, in genetically resistant and susceptible sheep. J. Proteomics 2012, 75:2141-2152.
95. Nair M.G., Guild K.J., Du Y., Zaph C., Yancopoulos G.D., Valenzuela D.M., Murphy A., Stevens S., Karow M., Artis D. Goblet cell-derived resistin-like molecule beta augments CD4+ T cell production of IFN-gamma and infection-induced intestinal inflammation. J. Immunol. 2008, 181:4709-4715.
96. Nakayama F., Nishihara S., Iwasaki H., Kudo T., Okubo R., Kaneko M., Nakamura M., Karube M., Sasaki K., Narimatsu H. CD15 expression in mature granulocytes is determined by alpha 1,3-fucosyltransferase IX, but in promyelocytes and monocytes by alpha 1,3-fucosyltransferase IV. J. Biol. Chem. 2001, 276:16100-16106.
97. Noland G.S., Urban J.F., Fried B., Kumar N. Counter-regulatory anti-parasite cytokine responses during concurrent Plasmodium yoelii and intestinal helminth infections in mice. Exp. Parasitol. 2008, 119:272-278.
98. Nsoso S.J., Machete J.B., Molatole M., Ndebele R.T., Lebani N.N., Chabo R.G., Kalake A.M., Jacyna L., Segadimo B.W., Mine O.M. The impact of traditional management on seasonal internal parasite burdens and productivity of indigenous Tswana goats in southern Botswana. Onderstepoort J. Vet. Res. 2001, 68:101-104.
99. Pemberton A.D., Knight P.A., Gamble J., Colledge W.H., Lee J.K., Pierce M., Miller H.R. Innate BALB/c enteric epithelial responses to Trichinella spiralis: inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. J. Immunol. 2004, 173:1894-1901.
100. Pennock J.L., Grencis R.K. The mast cell and gut nematodes: damage and defence. Chem. Immunol. Allergy 2006, 90:128-140.
101. Pomroy W.E., Lambert M.G., Betteridge K. Comparison of faecal strongylate egg counts of goats and sheep on the same pasture. N. Z. Vet. J. 1986, 34:36-37.
102. Porto A.F., Santos S.B., Muniz A.L., Basilio V., Rodrigues W., Neva F.A., Dutra W.O., Gollob K.J., Jacobson S., Carvalho E.M. Helminthic infection down-regulates type 1 immune responses in human T cell lymphotropic virus type 1 (HTLV-1) carriers and is more prevalent in HTLV-1 carriers than in patients with HTLV-1-associated myelopathy/tropical spastic paraparesis. J. Infect. Dis. 2005, 191:612-618.
103. Rinaldi M., Dreesen L., Hoorens P.R., Li R.W., Claerebout E., Goddeeris B., Vercruysse J., Van Den Broek W., Geldhof P. Infection with the gastrointestinal nematode Ostertagia ostertagi in cattle affects mucus biosynthesis in the abomasum. Vet. Res. 2011, 42:61.
104. Rowe A., Gondro C., Emery D., Sangster N. Sequential microarray to identify timing of molecular responses to Haemonchus contortus infection in sheep. Vet. Parasitol. 2009, 161:76-87.
105. Ruiz A., Molina J.M., González J.F., Conde M.M., Martín S., Hernández Y.I. Immunoprotection in goats against Haemonchus contortus after immunization with cysteine protease enriched protein fractions. Vet. Res. 2004, 35:565-572.
106. Sanchez J., Dohoo I. A bulk tank milk survey of Ostertagia ostertagi antibodies in dairy herds in Prince Edward Island and their relationship with herd management factors and milk yield. Can. Vet. J. 2002, 43:454-459.
107. Sanchez J., Dohoo I., Carrier J., Carrier J., DesCôteaux L. A meta-analysis of the milk-production response after anthelmintic treatment in naturally infected adult dairy cows. Prev. Vet. Med. 2004, 63:237-256.
108. Shakya K.P., Miller J.E., Horohov D.W. A Th2 type of immune response is associated with increased resistance to Haemonchus contortus in naturally infected Gulf Coast Native lambs. Vet. Parasitol. 2009, 163:57-66.
109. Shea-Donohue T., Urban J.F. Gastrointestinal parasite and host interactions. Curr. Opin. Gastroenterol. 2004, 20:3-9.
110. Stear M.J., Boag B., Cattadori I., Murphy L. Genetic variation in resistance to mixed, predominantly Teladorsagia circumcincta nematode infections of sheep: from heritabilities to gene identification. Parasite Immunol. 2009, 31:274-282.
111. Sykes A.R. Manipulating host immunity to improve nematode parasite control-quo vadit. Parasite Immunol. 2008, 30:71-77.
112. Taylor M.A. SCOPS and COWS-'worming it out of UK farmers'. Vet. Parasitol. 2012, 186:65-69. 10.1016/j.vetpar.2011.11.047.
113. Terefe G., Lacroux C., Andreoletti O., Grisez C., Prevot F., Bergeaud J.P., Penicaud J., Rouillon V., Gruner L., Brunel J.C., et al. Immune response to Haemonchus contortus infection in susceptible (INRA 401) and resistant (Barbados Black Belly) breeds of lambs. Parasite Immunol. 2007, 29:415-424.
114. Trapnell C., Pachter L., Salzberg S.L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
115. Trapnell C., Williams B.A., Pertea G., Mortazavi A., Kwan G., van Baren M.J., Salzberg S.L., Wold B.J., Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010, 28:511-515.
116. Valentine B.A., Cebra C.K., Taylor G.H. Fatal gastrointestinal parasitism in goats: 31 cases (2001-2006). J. Am. Vet. Med. Assoc. 2007, 231:1098-1103.
117. Wagland B.M., Steel J.W., Windon R.G., Dineen J.K. The response of lambs to vaccination and challenge with Trichostrongylus colubriformis: effect of plane of nutrition on, and the inter-relationship between, immunological responsiveness and resistance. Int. J. Parasitol. 1984, 14:39-44.
118. Zaiss D.M., Yang L., Shah P.R., Kobie J.J., Urban J.F., Mosmann T.R. Amphiregulin, a TH2 cytokine enhancing resistance to nematodes. Science 2006, 314:1746.
119. Zaros L.G., Bricarello P.A., Amarante A.F.T., Rocha R.A., Kooyman F.N.J., De Vries E., Coutinho L.L. Cytokine gene expression in response to Haemonchus placei infections in Nellore cattle. Vet. Parasitol. 2010, 171:68-73.
120. Zhao A., Urban J.F., Anthony R.M., Sun R., Stiltz J., Van R.N., Wynn T.A., Gause W.C., Shea-Donohue T. Th2 cytokine-induced alterations in intestinal smooth muscle function depend on alternatively activated macrophages. Gastroenterology 2008, 135:217-225.