The avian heterophil

Developmental and Comparative Immunology

Volumn 41, Issue 3, 2013, Pages 334-340

  Genovese, Kenneth J ^a   He, Haiqi ^a   Swaggerty, Christina L ^a   Kogut, Michael H ^a  

^a SOUTHERN PLAINS AGRICULTURAL RESEARCH CENTER   (United States)

Author keywords

Avian; Granulocyte; Heterophil; Innate immunity; Poultry

Indexed keywords

CHEMOKINE; CYTOKINE; DNA; HISTONE;

ARTICLE; CAMPYLOBACTER JEJUNI; CELL FUNCTION; CHICKEN; CYTOKINE RELEASE; DEGRANULATION; DISEASE RESISTANCE; EIMERIA TENELLA; ENTEROCOCCUS GALLINARUM; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENETIC SELECTION; GRANULOCYTE; HETEROPHIL; HOST; INFECTION SENSITIVITY; INNATE IMMUNITY; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REGULATORY MECHANISM; RESPIRATORY BURST; SALMONELLA ENTERITIDIS; SIGNAL TRANSDUCTION;

AVES;

AVIAN; GRANULOCYTE; HETEROPHIL; INNATE IMMUNITY; POULTRY;

ADAPTIVE IMMUNITY; ANIMALS; CELL DEGRANULATION; CHICKENS; CYTOKINES; DNA; GENE EXPRESSION REGULATION; HISTONES; IMMUNITY, INNATE; NEUTROPHILS; PHAGOCYTOSIS; RECEPTORS, COMPLEMENT; RESPIRATORY BURST; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 84883053861     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2013.03.021     Document Type: Article

References (99)

1. Akira S. Toll-like receptors and innate immunity. Adv Immunol 2001, 78:1-56.
2. Barletta K.E., Ley K., Mehrad B. Regulation of neutrophil function by adenosine. Arterioscler. Thromb. Vasc. Biol. 2012, 32:856-864.
3. Bischoff K.M., Pishko E.J., Genovese K.J., Crippen T.L., Holtzapple C.K., Stanker L.H., Nisbet D.J., Kogut M.H. Chicken mim-1 protein, P33, is a heterophil chemotactic factor present in Salmonella enteritidis immune lymphokine. J. Food Prot. 2001, 64:1503-1509.
4. Borregaard N., Sorensen O.E., Theilgaard-Monch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 2007, 28:340-345.
5. Brinkmann V., Reichard U., Goosemann C., Fauler B., Uhlemann Y., Weiss D.S., Weinrauch Y., Zychlinsky A. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535.
6. Brinkmann V., Zychlinsky A. Beneficial suicide: why neutrophils die to make NETS. Nat. Rev. Microbiol. 2007, 5:577-582.
7. Brockus C.W., Jackwood M.W., Harmon B.G. Characterization of beta-defensin prepropeptide mRNA from chicken and turkey bone marrow. Anim. Genet. 1998, 29:283-289.
8. Brownlie R., Zhu J., Allan B., Mutwiri G.K., Babiuk L.A., Potter A., Griebel P. Chicken TLR21 acts as a functional homologue to mammalian TLR9 in the recognition of CpG oligodeoxynucleotides. Mol. Immunol. 2009, 46:3163-3170.
9. Brune K., Spitznagel J.K. Peroxidaseless chicken leukocytes: isolation and characterization of antibacterial granules. J. Infect. Dis. 1973, 127:84-94.
10. Chiang H.I., Swaggerty C.L., Kogut M.H., Dowd S.E., Li X., Pevzner I.Y., Zhou H. Gene expression profiling in chicken heterophils with Salmonella enteritidis stimulation using a chicken 44 K agilent microarray. BMC Genomics 2008, 9:1-11.
11. Chuammitri P., Ostojić J., Andreasen C.B., Redmond S.B., Lamont S.J., Palić D. Chicken heterophil extracellular traps (HETs): novel defense mechanism of chicken heterophils. Vet. Immunol. Immunopathol. 2009, 129:126-131.
12. Chuammitri P., Redmond S.B., Kimura K., Andreasen C.B., Lamont S.J., Palić D. Vet Immunol Immunopathol. 2011, 142:219-227.
13. Cloutier A., Ear T., Blais-Charron E., Dubois C.M. Differential involvement of NF-kB and MAP kinase pathways in the generation of inflammatory cytokines by human neutrophils. J. Leukocyte Biol. 2007, 81:567-577.
14. Daimon T., Caxton-Martins A. Electron microscopic and enzyme cytochemical studies on granules of mature chicken granular leucocytes. J. Anat. 1977, 123:553-562.
15. Evans E.W., Beach G.G., Wunderlich J., Harmon B.G. Isolation of antimicrobial peptides from avian heterophils. J. Leukocyte Biol. 1994, 56:661-665.
16. Evans E.W., Beach F.G., Moore K.M., Jackwood M.W., Glisson J.R., Harmon B.G. Antimicrobial activity of chicken and turkey heterophil peptides CHP1, CHP2, THP1, and THP3. Vet. Microbiol. 1995, 47:295-303.
17. Ermert D., Urban C.F., Laube B., Goosmann C., Zychlinsky A., Brinkmann V. Mouse neutrophil extracellular traps in microbial infections. J. Innate Immun. 2009, 1:181-193.
18. Farnell M.B., He H., Genovese K., Kogut M.H. Pharmacological analysis of signal transduction pathways required for oxidative burst in chicken heterophils stimulated by a Toll-like receptor 2 agonist. Int. Immunopharmacol. 2003, 3:1677-1684.
19. Farnell M.B., Donoghue A.M., de Los Santos F.S., Blore P.J., Hargis B.M., Tellez G., Donoghue D.J. Upregulation of oxidative burst and degranulation in chicken heterophils stimulated with probiotic bacteria. Poult. Sci. 2006, 85:1900-1906.
20. Ferro P.J., Swaggerty C.L., Kaiser P., Pevzner I.Y., Kogut M.H. Heterophils isolated from chickens resistant to extraintestinal Salmonella enteritidis infection express higher levels of pro-inflammatory cytokine mRNA following infection than heterophils from susceptible chickens. Epidemiol. Infect. 2004, 132:1029-1037.
21. Flannagan R.S., Jaumouille V., Grinstein S. The cell biology of phagocytosis. Annu. Rev. Pathol. 2012, 7:61-98.
22. Fuchs T.A., Abed U., Goosemann C., Hurwitz R., Schulze I., Wahn V., Weinreich Y., Brinkmann V., Zychlinsky A. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 2007, 176:231-241.
23. Fujimori K., Yamada M., Imai K. Distribution of neutral and acid alpha-glucosidases of granule fractions from chicken heterophil leucocytes. Cell Mol. Biol. Incl. Cyto. Enzymol. 1978, 23:391-402.
24. Genovese K.J., Moyes R.B., Genovese L.L., Lowry V.K., Kogut M.H. Resistance to Salmonella enteritidis organ invasion in day-old turkeys and chickens by transformed t cell line produced lymphokines. Avian Diseases 1998, 42:545-553.
25. Genovese L.L., Lowry V.K., Genovese K.J., DeLoach J.R., Kogut M.H. Enhancement of phagocytosis and bacterial killing by heterophils from neonatal chicks after administration of Salmonella enteritidis-immune lymphokines. Vet. Microbiol. 1999, 65:133-143.
26. Genovese L.L., Lowry V.K., Genovese K.J., Kogut M.H. Longevity of augmented phagocytic activity of heterophils in neonatal chickens following administration of Salmonella enteritidis-immune lymphokines to chickens. Avian Pathology 2000, 29:117-122.
27. Genovese K.J., He H., Lowry V.K., Kogut M.H. Comparison of MAP and tyrosine kinase signaling in heterophils from commercial and wild-type turkeys. Dev. Comp. Immunol. 2007, 31:927-933.
28. Genovese K.J., He H., Lowry V.K., Swaggerty C.L., Kogut M.H. Comparison of heterophil functions of modern commercial and wild-type Rio Grande turkeys. Avian Pathol. 2006, 35:217-223.
29. Gerilechaogetu H.A., Abe A., Kondo Y. Extracellular signal-regulated kinase (ERK) activation in chicken heterophils stimulated with phorbol 12-myristate 13-acetate (PMA), formyl-methionylleucyl-phenylalanine (fMLP) and lipopolysaccharide (LPS). Anim. Sci. 2009, 80:577-584.
30. Gupta A., Hasler P., Gebhardt S., Holzgreve W., Hahn S. Occurrence of neutrophil extracellular DNA traps (NETS) in pre-eclampsia: a link with elevated levels of cell-free DNA?. Ann. NY Acad. Sci. 2006, 1075:118-122.
31. Gupta A., Hasler P., Gebhardt S., Holzgreve W., Hahn S. Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum. Immunol. 2005, 66:1146-1154.
32. Harmon B.G. Avian heterophils in inflammation and disease resistance. Poult. Sci. 1998, 77:972-977.
33. Harwig S.S., Swiderek K.M., Kokryakov V.N., Tan L., Lee T.D., Panyutich E.A., Aleshina G.M., Shamova O.V., Lehrer R.I. Gallinacins: cysteine-rich antimicrobial peptides of chicken leukocytes. FEBS Lett. 1994, 342:281-285.
34. Higgs R., Cormican P., Cahalane S., Allan B., Lloyd A.T., Meade K., James T., Lynn D.J., Babiuk L.A., O'Farrelly C. Induction of a novel chicken Toll-like receptor following Salmonella enterica Serovar Typhimurium infection. Infect. Immun. 2006, 74:1692-1698.
35. He H., Farnell M.B., Kogut M.H. Inflammatory agonist stimulation and signal pathway of oxidative burst in neonatal chicken heterophils. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2003, 135:177-184.
36. He H., Lowry V.K., Swaggerty C.L., Ferro P.J., Kogut M.H. In vitro activation of chicken leukocytes and in vivo protection against Salmonella enteritidis organ invasion and peritoneal S. enteritidis infection-induced mortality in neonatal chickens by immunostimulatory CpG oligodeoxynucleotide. FEMS Immunol. Med. Microbiol. 2005, 43:81-89.
37. He H., Genovese K.J., Lowry V.K., Nisbet D.J., Kogut M.H. Response of nitric oxide production to CpG oligodeoxynucleotides in turkey and chicken peripheral blood monocytes. FEMS Immunol. Med. Microbiol. 2006, 48:99-106.
38. He H., Genovese K.J., Swaggerty C.L., Nisbet D.J., Kogut M.H. In vivo priming heterophil innate immune functions and increasing resistance to Salmonella enteritidis infection in neonatal chickens by immune stimulatory CpG oligodeoxynucleotides. Vet. Immunol. Immunopathol. 2007, 117:275-283.
39. He H., Genovese K.J., Swaggerty C.L., Nisbet D.J., Kogut M.H. Differential induction of nitric oxide, degranulation, and oxidative burst activities in response to microbial agonist stimulations in monocytes and heterophils from young commercial turkeys. Vet. Immunol. Immunopathol. 2008, 123:177-185.
40. He H., MacKinnon K.M., Genovese K.J., Nerren J.R., Swaggerty C.L., Nisbet D.J., Kogut M.H. Chicken scavenger receptors and their ligand-induced cellular immune responses. Mol. Immunol. 2009, 46:2218-2225.
41. Iqbal M., Philbin V.J., Smith A.L. Expression patterns of chicken Toll-like receptor mRNA in tissues, immune cell subsets and cell lines. Vet. Immunol. Immunopathol. 2005, 104:117-127.
42. Janeway C.A., Medzhitov R. Innate immune recognition. Annual Review of Immunology 2002, 20:197-216.
43. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
44. Klebanoff S.J. Myeloperoxidase: friend and foe. J. Leukocyte Biol. 2005, 77:598-625.
45. Kogut M.H., McGruder E.D., Hargis B.M., Corrier D.E., DeLoach J.R. Dynamics of the avian inflammatory response to Salmonella-immune lymphokines. Changes in avian blood leukocyte populations. Inflammation 1994, 18:373-388.
46. Kogut M.H., McGruder E.D., Hargis B.M., Corrier D.E., DeLoach J.R. In vivo activation of heterophil function in chickens following injection with Salmonella enteritidis-immune lymphokines. J. Leukocyte Biol. 1995, 57:56-62.
47. Kogut M.H., McGruder E.D., Hargis B.M., Corrier D.E., DeLoach J.R. Characterization of the pattern of inflammatory cell influx in chicks following the intraperitoneal administration of live Salmonella enteritidis and Salmonella enteritidis-immune lymphokines. Poult. Sci. 1995, 74:8-17.
48. Kogut M.H., Holtzapple C., Lowry V.K., Genovese K., Stanker L.H. Functional responses of neonatal chicken and turkey heterophils following stimulation by inflammatory agonists. Am. J. Vet. Res. 1998, 59:1404-1408.
49. Kogut M.H., Lowry V.K., Moyes R.B., Bowden L.L., Bowden R., Genovese K., Deloach J.R. Lymphokine-augmented activation of avian heterophils. Poult. Sci. 1998, 77:964-971.
50. Kogut M.H., Pishko E.J., Kaspers B., Weining K.C. Modulation of functional activities of chicken heterophils by recombinant chicken IFN-gamma. J. Interferon Cytokine Res. 2001, 21:85-92.
51. Kogut M.H., Genovese K.J., Lowry V.K. Differential activation of signal transduction pathways mediating phagocytosis, oxidative burst, and degranulation by chicken heterophils in response to stimulation with opsonized Salmonella enteritidis. Inflammation 2001, 25:7-15.
52. Kogut M.H., Rothwell L., Kaiser P. Differential regulation of cytokine gene expression by avian heterophils during receptor-mediated phagocytosis of opsonized and nonopsonized Salmonella enteritidis. J. Interferon Cytokine Res. 2003, 23:319-327.
53. Kogut M.H., Rothwell L., Kaiser P. Priming by recombinant chicken interleukin-2 induces selective expression of IL-8 and IL-18 mRNA in chicken heterophils during receptor-mediated phagocytosis of opsonized and nonopsonized Salmonella enterica serovar enteritidis. Mol. Immunol. 2003, 40:603-610.
54. Kogut M.H., Iqbal M., He H., Philbin V., Kaiser P., Smith A. Expression and function of Toll-like receptors in chicken heterophils. Dev. Comp. Immunol. 2005, 29:791-807.
55. Kogut M.H., Rothwell L., Kaiser P. IFN-gamma priming of chicken heterophils upregulates the expression of proinflammatory and Th1 cytokine mRNA following receptor-mediated phagocytosis of Salmonella enterica serovar enteritidis. J. Interferon Cytokine Res. 2005, 25:73-81.
56. Kogut M.H., Swaggerty C., He H., Pevzner I., Kaiser P. Toll-like receptor agonists stimulate differential functional activation and cytokine and chemokine gene expression in heterophils isolated from chickens with differential innate responses. Microbes Infect. 2006, 8:1866-1874.
57. Kogut M.H., Genovese K.J., He H., Li M.A., Jiang Y.W. The effects of the BT/TAMUS 2032 cationic peptides on innate immunity and susceptibility of young chickens to extraintestinal Salmonella enterica serovar Enteritidis infection. Int. Immunopharmacol. 2007, 7:912-919.
58. Kogut M.H., Genovese K.J., He H., Kaiser P. Flagellin and lipopolysaccharide up-regulation of IL-6 and CXCLi2 gene expression in chicken heterophils is mediated by ERK1/2-dependent activation of AP-1 and NF-kappaB signaling pathways. Innate Immun. 2008, 14:213-222.
59. Kogut M.H., He H., Genovese K.J., Jiang Y.W. Feeding the BT cationic peptides to chickens at hatch reduces cecal colonization by Salmonella enterica serovar Enteritidis and primes innate immune cell functional activity. Foodborne. Pathog. Dis. 2010, 7:23-30.
60. Kogut M.H., Genovese K.J., He H., Swaggerty C.L., Jiang Y.W. BT cationic peptides: small peptides that modulate innate immune responses of chicken heterophils and monocytes. Vet. Immunol. Immunopathol. 2012, 145:151-158.
61. Kogut M.H., Chiang H.I., Swaggerty C.L., Pevzner I.Y., Zhou H. Gene expression analysis of Toll-like receptor pathways in heterophils from genetic chicken lines that differ in their susceptibility to Salmonella enteritidis. Front. Genet. 2012, 3:121.
62. Kogut M.H., Genovese K.J., Nerren J.R., He H. Effects of avian triggering receptor expressed on myeloid cells (TREM-A1) activation on heterophil functional activities. Dev. Comp. Immunol. 2012, 36:157-165.
63. Kogut M.H., Chiang H.-I., Swaggerty C.L., Pevzner I.Y., Zhou H. Gene expression analysis of Toll-like receptor pathways in heterophils from genetic chicken lines that differ in their susceptibility to Salmonella enteritidis. Front. Epigenomics 2012, 3:1-10.
64. Li X., Swaggerty C.L., Kogut M.H., Chiang H., Wang Y., Genovese K.J., He H., Stern N.J., Pevzner I.Y., Zhou H. The paternal effect of Campylobacter jejuni colonization in ceca in broilers. Poult. Sci. 2008, 87:1742-1747.
65. Lippolis J.D., Reinhardt T.A., Goff J.P., Horst R.L. Neutrophil extracellular trap formation by bovine neutrophils is not inhibited milk. Vet. Immunol. Immunopathol. 2006, 113:248-255.
66. Liu Y., Shepherd E.G., Nelin L.D. MAPK phosphatases - regulating the immune response. Nat. Rev. Immunol. 2007, 7:202-212.
67. Lowry V.K., Genovese K.J., Bowden L.L., Kogut M.H. Ontogeny of the phagocytic and bactericidal activities of turkey heterophils and their potentiation by Salmonella enteritidis-immune lymphokines. FEMS Immunol. Med. Microbiol. 1997, 19:95-100.
68. Lowry V.K., Farnell M.B., Ferro P.J., Swaggerty C.L., Bahl A., Kogut M.H. Purified B- glucan as an abiotic feed additive up-regulates the innate immune response in immature chickens against Salmonella enterica serovars Enteritidis. Int. J. Food Microbiol. 2005, 98:309-318.
69. Mackinnon K.M., He H., Swaggerty C.L., McReynolds J.L., Genovese K.J., Duke S.E., Nerren J.R., Kogut M.H. In ovo treatment with CpG oligodeoxynucleotides decreases colonization of Salmonella enteriditis in broiler chickens. Vet. Immunol. Immunopathol. 2009, 127(3-4):371-375.
70. Macrae E.K., Spitznagel J.K. Ultrastructural localization of cationic proteins in cytoplasmic granules of chicken and rabbit polymorphonuclear leukocytes. J. Cell Sci. 1975, 17:79-94.
71. Maxwell M.H. The distribution and localisation of acid trimetaphosphatase in developing heterophils and eosinophils in the bone marrow of the fowl and the duck. Cell Tissue Res. 1984, 235:171-176.
72. Maxwell M.H., Robertson G.W. The avian heterophil leucocyte: a review. World's Poult. Sci. J. 1998, 54:155-178.
73. Nerren J.R., Swaggerty C.L., MacKinnon K.M., Genovese K.J., He H., Pevzner I., Kogut M.H. Differential mRNA expression of the avian-specific toll-like receptor 15 between heterophils from Salmonella-susceptible and -resistant chickens. Immunogenetics 2009, 61:71-77.
74. Nerren J.R., Kogut M.H. The selective Dectin-1 agonist, curdlan, induces an oxidative burst response in chicken heterophils and peripheral blood mononuclear cells. Vet. Immunol. Immunopathol. 2009, 127:162-166.
75. Nixon J.B., McPhail L.C. Protein kinase C (PKC) isoforms translocate to Triton-insoluble fractions in stimulated human neutrophils: correlation of conventional PKC with activation of NADPH oxidase. J. Immunol. 1999, 163:4574-4582.
76. Osculati F. Fine structural localization of acid phosphatase and arylsulfatase in the chick heterophil leucocytes. Z. Zellforsch. Mikrosk. Anat. 1970, 109:398-406.
77. Philbin V.J., Iqbal M., Boyd Y., Goodchild M.J., Beal R.K., Bumstead N., Young J., Smith A.L. Identification and characterization of a functional, alternatively spliced Toll-like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunology 2005, 114:507-521.
78. Palic D., Ostojic J., Andreason C.B., Roth J.A. Fish cast NETs: neutrophil extracellular traps are released from fish neutrophils. Dev. Comp. Immunol. 2007, 31:805-816.
79. Pinard-Van Der Laan M.H., Monvoisin J.L., Pery P., Hamet N., Thomas M. Comparison of outbred lines of chickens for resistance to experimental infection with Coccidiosis (Eimeria tenella). Poult. Sci. 1998, 77:185-191.
80. Redmond S.B., Chuammitri P., Andreasen C.B., Palic D., Lamont S.J. Chicken heterophils from commercially selected and non-selected genetic lines express cytokines differently after in vitro exposure to Salmonella enteritidis. Vet. Immunol. Immunopathol. 2009, 132:129-134.
81. Redmond S.B., Chuammitri P., Andreasen C.B., Palic D., Lamont S.J. Genetic control of chicken heterophil function in advanced intercross lines: associations with novel and with known Salmonella resistance loci and a likely mechanism for cell death in extracellular trap production. Immunogenetics 2011, 63:449-458.
82. Redmond S.B., Chuammitri P., Andreasen C.B., Palic D., Lamont S.J. Proportion of circulating chicken heterophils and CXCLi2 expression in response to Salmonella enteritidis are affected by genetic line and immune modulating diet. Vet. Immunol. Immunopathol. 2011, 140:323-328.
83. Smith E.J., Crittenden L.B. Genetic cellular resistance to subgroup E avian leukosis virus in slow-feathering dams reduces congenital transmission of an endogenous retrovirus encoded at locus ev 21. Poult. Sci. 1998, 67:1668-1673.
84. Stabler J.G., McCormick T.W., Powell K.C., Kogut M.H. Avian heterophils and monocytes: phagocytic and bactericidal activities against Salmonella enteritidis. Vet. Microbiol. 1994, 38:293-305.
85. Stringfellow K., Caldwell D., Lee J., Mohnl M., Beltran R., Schatzmayr G., Fitz-Coy S., Broussard C., Farnell M. Evaluation of probiotic administration on the immune response of coccidiosis-vaccinated broilers. Poult. Sci. 2011, 90:1652-1658.
86. Swaggerty C.L., Pevzner I.Y., Ferro P.J., Crippen T.L., Kogut M.H. Association between in vitro heterophil function and the feathering gene in commercial broiler chickens. Avian Pathol. 2003, 32:483-488.
87. Swaggerty C.L., Pevzner I.Y., Lowry V.K., Farnell M.B., Kogut M.H. Functional comparison of heterophils isolated from commercial broiler chickens. Avian Pathol. 2003, 32:95-102.
88. Swaggerty C.L., Kogut M.H., Ferro P.J., Rothwell L., Pevzner I.Y., Kaiser P. Differential cytokine mRNA expression in heterophils isolated from Salmonella -resistant and -susceptible chickens. Immunology 2004, 113:139-148.
89. Swaggerty C.L., Ferro P.J., Pevzner I.Y., Kogut M.H. Heterophils are associated with resistance to systemic Salmonella enteritidis infection in genetically distinct lines of chickens. FEMS Immunol. Med. Microbiol. 2005, 43:149-154.
90. Swaggerty C.L., Lowry V.K., Ferro P.J., Pevzner I.Y., Kogut M.H. Disparity in susceptibility to vancomycin-resistant Enterococcus organ invasion in commercial broiler chickens that differ in innate immune responsiveness. Food Agric. Immunol. 2005, 16:1-15.
91. Swaggerty C.L., He H., Genovese K.J., Kaiser P., Pevzner I.Y., Kogut M.H. The feathering gene is linked to degranulation and oxidative burst not cytokine/chemokine mRNA expression levels or Salmonella enteritidis organ invasion in broilers. Avian Pathol. 2006, 35:465-470.
92. Swaggerty C.L., Kaiser P., Rothwell L., Pevzner I.Y., Kogut M.H. Heterophil cytokine mRNA profiles from genetically distinct lines of chickens with differential heterophil-mediated innate immune responses. Avian Pathol. 2006, 35:102-108.
93. Swaggerty C.L., Genovese K.J., He H., Duke S.E., Pevzner I.Y., Kogut M.H. Broiler breeders with an efficient innate immune response are more resistant to Eimeria tenella. Poult. Sci. 2011, 90:1014-1019.
94. Swaggerty C.L., He H., Genovese K.J., Pevzner I.Y., Kogut M.H. Protein tyrosine kinase and mitogen-activated protein kinase signaling pathways contribute to differences in heterophil-mediated innate immune responsiveness between two lines of broilers. Avian Pathol. 2011, 40:289-297.
95. van Dijk A., Veldhuizen E.J., Haagsman H.P. Avian defensins. Vet. Immunol. Immunopathol. 2008, 124:1-18.
96. van Dijk A., Tersteeg-Zijderveld M.H., Tjeerdsma-van Bokhoven J.L., Jansman A.J., Veldhuizen E.J., Haagsman H.P. Chicken heterophils are recruited to the site of Salmonella infection and release antibacterial mature Cathelicidin-2 upon stimulation with LPS. Mol. Immunol. 2009, 46:1517-1526.
97. Wells L.L., Lowry V.K., DeLoach J.R., Kogut M.H. Age-dependent phagocytosis and bactericidal activities of the chicken heterophil. Dev. Comp. Immunol. 1998, 22:103-109.
98. Vitiello M., D'Isanto M., Galdiero M., Raieta K., Tortora A., Rotondo P., Peluso L. Interleukin-8 production by THP-1 cells stimulated by Salmonella enterica serovar Typhimurium porins is mediated by AP-1, NF-[kappa]B and MAPK pathways. Cytokine 2004, 27:15-24.
99. Winterbourn C.C., Kettle A.J. Redox reactions and microbial killing in the neutrophil phagosome. Antioxid. Redox Signal 2012, 10.1089/ars.2012.4827.