Cell and Tissue Research

, Volume 371, Issue 3, pp 617–637 | Cite as

Bovine neutrophils in health and disease



Bovine neutrophils have similarities to those of other species with respect to mechanisms of their activation and migration into tissue, modulation of immune responses and the balance between microbial killing and host tissue damage. However, bovine neutrophils have biochemical and functional differences from those of other species, which may yield insights about the comparative biology of neutrophils. Neutrophils play protective and harmful roles in the infectious diseases of cattle that occur at times of transition: respiratory disease in beef calves recently arrived to feedlots and mastitis and other diseases of postparturient dairy cows. An important research focus is the mechanisms by which risk factors for these diseases affect neutrophil function and thereby lead to disease and the prospect of genetic or pharmacologic improvement of disease resistance. Further, in keeping with the One Health paradigm, cattle can be considered a model for studying the role of neutrophils in naturally occurring diseases caused by host-adapted pathogens and are thus an intermediary between studies of mouse models and investigations of human disease. Finally, the study of bovine neutrophils is important for agriculture, to understand the pathogenesis of these production-limiting diseases and to develop novel methods of disease prevention that improve animal health and reduce the reliance on antimicrobial use.


Cattle Neutrophils Polymorphonuclear leukocytes Bovine respiratory disease Mastitis 



This work was supported by research grants to J Caswell from the Natural Sciences and Engineering Research Council of Canada (CRDPJ 476331–14; RGPIN-2017-03872), Beef Farmers of Ontario (17–02; 13–05) and the Ontario Ministry of Agriculture, Food and Rural Affairs (2013–1488).

Compliance with ethical standards

Conflict of interest

Dr. Caswell receives research and consulting funding from Zoetis Inc.


  1. Ackermann MR, Kehrli ME, Laufer JA, Nusz LT (1996) Alimentary and respiratory tract lesions in eight medically fragile holstein cattle with bovine leukocyte adhesion deficiency (BLAD). Vet Pathol 33:273–281PubMedCrossRefGoogle Scholar
  2. Alarcón P, Conejeros I, Carretta MD, Concha C, Jara E, Tadich N, Hidalgo MA, Burgos RA (2011) D-lactic acid interferes with the effects of platelet activating factor on bovine neutrophils. Vet Immunol Immunopathol 144:68–78PubMedCrossRefGoogle Scholar
  3. Aleri JW, Hine BC, Pyman MF, Mansell PD, Wales WJ, Mallard B, Fisher AD (2016) Periparturient immunosuppression and strategies to improve dairy cow health during the periparturient period. Res Vet Sci 108:8–17PubMedCrossRefGoogle Scholar
  4. Aoki Y, Magata F, Miyamoto A, Kawashima C, Hojo T, Okuda K, Shirasuna K, Shimizu (2014) The effect of single nucleotide polymorphisms in the tumor necrosis factor-α gene on reproductive performance and immune function in dairy cattle. J Reprod Dev 60:173–178PubMedPubMedCentralCrossRefGoogle Scholar
  5. Aulik, Hellenbrand, Klos, Czuprynski (2010) Mannheimia haemolytica and Its Leukotoxin Cause Neutrophil Extracellular Trap Formation by Bovine Neutrophils. Infect Immun 78:4454–4466PubMedPubMedCentralCrossRefGoogle Scholar
  6. Baggiolini M, Horisberger U, Gennaro R, Dewald B (1985) Identification of three types of granules in neutrophils of ruminants. Ultrastructure of circulating and maturing cells. Lab Investig J Technol Methods Pathol 52:151–158Google Scholar
  7. Bagheri M, Moradi-Sharhrbabak M, Miraie-Ashtiani R, Safdari-Shahroudi M, Abdollahi-Arpanahi R (2016) Case–control approach application for finding a relationship between candidate genes and clinical mastitis in Holstein dairy cattle. J Appl Genet 57:107–112PubMedCrossRefGoogle Scholar
  8. Baumann A, Kiener MS, Haigh B, Perreten V, Summerfield A (2017) Differential ability of bovine antimicrobial Cathelicidins to mediate nucleic acid sensing by epithelial cells. Front Immunol.
  9. Beecher C, Daly M, Ross RP, Flynn J, McCarthy TV, Giblin L (2012) Characterization of the bovine innate immune response in milk somatic cells following intramammary infection with streptococcus dysgalactiae subspecies dysgalactiae. J Dairy Sci 95:5720–5729PubMedCrossRefGoogle Scholar
  10. Behrendt JH, Ruiz A, Zahner H, Taubert A, Hermosilla C (2010) Neutrophil extracellular trap formation as innate immune reactions against the apicomplexan parasite Eimeria bovis. Vet Immunol Immunopathol 133:1–8PubMedCrossRefGoogle Scholar
  11. Benincasa M, Scocchi M, Pacor S, Tossi A, Nobili D, Basaglia G, Busetti M, Gennaro R (2006) Fungicidal activity of five cathelicidin peptides against clinically isolated yeasts. J Antimicrob Chemother 58:950–959PubMedCrossRefGoogle Scholar
  12. Berenji HSN (1997) Lysozyme content of bovine neutrophils. In: J Fac Vet Med Univ Tehran. Accessed 29 Nov 2017
  13. Beveridge JD, Mitchell GB, Brewer D, Clark ME, Caswell JL (2008) Altered protein expression in neutrophils of calves treated with dexamethasone. Can J Vet Res 72:249–252PubMedPubMedCentralGoogle Scholar
  14. Bordignon M, Da Dalt L, Marinelli L, Gabai G (2014) Advanced oxidation protein products are generated by bovine neutrophils and inhibit free radical production in vitro. Vet J Lond Engl 1997 199:162–168Google Scholar
  15. Breider MA, Walker RD, Hopkins FM, Schultz TW, Bowersock TL (1988) Pulmonary lesions induced by Pasteurella haemolytica in neutrophil sufficient and neutrophil deficient calves. Can J Vet Res 52:205–209PubMedPubMedCentralGoogle Scholar
  16. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303:1532–1535PubMedCrossRefGoogle Scholar
  17. Brown GB, Roth JA (1991) Comparison of the response of bovine and human neutrophils to various stimuli. Vet Immunol Immunopathol 28:201–218PubMedCrossRefGoogle Scholar
  18. Buckham Sporer KR, Burton JL, Earley B, Crowe MA (2007) Transportation stress in young bulls alters expression of neutrophil genes important for the regulation of apoptosis, tissue remodeling, margination, and anti-bacterial function. Vet Immunol Immunopathol 118:19–29PubMedCrossRefGoogle Scholar
  19. Burgos RA, Conejeros I, Hidalgo MA, Werling D, Hermosilla C (2011) Calcium influx, a new potential therapeutic target in the control of neutrophil-dependent inflammatory diseases in bovines. Vet Immunol Immunopathol 143:1–10PubMedCrossRefGoogle Scholar
  20. Cai TQ, Weston PG, Lund LA, Brodie B, McKenna DJ, Wagner WC (1994) Association between neutrophil functions and periparturient disorders in cows. Am J Vet Res 55:934–943PubMedGoogle Scholar
  21. Carretta MD, Hidalgo AI, Burgos J, Opazo L, Castro L, Hidalgo MA, Figueroa CD, Taubert A, Hermosilla C, Burgos RA (2016) Butyric acid stimulates bovine neutrophil functions and potentiates the effect of platelet activating factor. Vet Immunol Immunopathol 176:18–27PubMedCrossRefGoogle Scholar
  22. Caswell (2013) Failure of respiratory defenses in the pathogenesis of bacterial pneumonia of cattle. Vet Pathol 51:393–409PubMedCrossRefGoogle Scholar
  23. Caswell JL, Middleton DM, Sorden SD, Gordon JR (1998) Expression of the Neutrophil Chemoattractant Interleukin-8 in the lesions of bovine pneumonic Pasteurellosis. Vet Pathol 35:124–131PubMedCrossRefGoogle Scholar
  24. Caswell JL, Middleton DM, Gordon JR (1999) Production and functional characterization of recombinant bovine interleukin-8 as a specific neutrophil activator and chemoattractant. Vet Immunol Immunopathol 67:327–340PubMedCrossRefGoogle Scholar
  25. Caswell JL, Middleton DM, Gordon JR (2001) The importance of interleukin-8 as a neutrophil chemoattractant in the lungs of cattle with pneumonic pasteurellosis. Can J Vet Res 65:229–232PubMedPubMedCentralGoogle Scholar
  26. Cerone SI, Sansinanea AS, García MC (2007) Effects of beta-hydroxybutyric acid on bovine milk leukocytes function in vitro. Gen Physiol Biophys 26:14–19PubMedGoogle Scholar
  27. Chang L-C, Madsen SA, Toelboell T, Weber PSD, Burton JL (2004) Effects of glucocorticoids on Fas gene expression in bovine blood neutrophils. J Endocrinol 183:569–583PubMedCrossRefGoogle Scholar
  28. Chen R, Yang Z, Ji D, Mao Y, Chen Y, Zhang Y, Hamza, Wang X, Li Y (2011) SNPs of CXCR1 gene and its associations with somatic cell score in Chinese Holstein cattle. Anim Biotechnol 22:133–142PubMedCrossRefGoogle Scholar
  29. Chin AC, Lee WD, Murrin KA, Morck DW, Merrill JK, Dick P, Buret AG (2000) Tilmicosin induces apoptosis in bovine peripheral neutrophils in the presence or in the absence of Pasteurella haemolytica and promotes neutrophil phagocytosis by macrophages. Antimicrob Agents Chemother 44:2465–2470PubMedPubMedCentralCrossRefGoogle Scholar
  30. Conejeros I, Patterson R, Burgos RA, Hermosilla C, Werling D (2011) Induction of reactive oxygen species in bovine neutrophils is CD11b, but not dectin-1-dependent. Vet Immunol Immunopathol 139:308–312PubMedCrossRefGoogle Scholar
  31. Conejeros I, Jara E, Carretta MD, Alarcón P, Hidalgo MA, Burgos RA (2012) 2-Aminoethoxydiphenyl borate (2-APB) reduces respiratory burst, MMP-9 release and CD11b expression, and increases l-selectin shedding in bovine neutrophils. Res Vet Sci 92:103–110PubMedCrossRefGoogle Scholar
  32. Conejeros I, Gibson AJ, Werling D, Muñoz-Caro T, Hermosilla C, Taubert A, Burgos RA (2015) Effect of the synthetic toll-like receptor ligands LPS, Pam3CSK4, HKLM and FSL-1 in the function of bovine polymorphonuclear neutrophils. Dev Comp Immunol 52:215–225PubMedCrossRefGoogle Scholar
  33. Cooray R, Petersson CG, Holmberg O (1993) Isolation and purification of bovine myeloperoxidase from neutrophil granules. Vet Immunol Immunopathol 38:261–272PubMedCrossRefGoogle Scholar
  34. Cortjens B, de Boer OJ, de Jong R, Antonis AF, Sabogal Piñeros YS, Lutter R, van Woensel JB, Bem RA (2016) Neutrophil extracellular traps cause airway obstruction during respiratory syncytial virus disease. J Pathol 238:401–411PubMedCrossRefGoogle Scholar
  35. Craven N (1986) Chemotactic factors for bovine neutrophils in relation to mastitis. Comp Immunol Microbiol Infect Dis 9:29–36PubMedCrossRefGoogle Scholar
  36. Crookenden MA, Heiser A, Murray A, Dukkipati VSR, Kay JK, Loor JJ, Meier S, Mitchell MD, Moyes KM, Walker CG, Roche JR (2016) Parturition in dairy cows temporarily alters the expression of genes in circulating neutrophils. J Dairy Sci 99:6470–6483PubMedCrossRefGoogle Scholar
  37. Cudd L, Clarke C, Clinkenbeard K (2003) Mannheimia haemolytica leukotoxin-induced increase in leukotriene B4 production by bovine neutrophils is mediated by a sustained and excessive increase in intracellular calcium concentration. FEMS Microbiol Lett 224:85–90PubMedCrossRefGoogle Scholar
  38. Cullor JS, Smith W, Zinkl JG, Dellinger JD, Boone T (1992) Hematologic and bone marrow changes after short- and long-term Administration of two Recombinant Bovine Granulocyte Colony-Stimulating Factors. Vet Pathol 29:521–527PubMedCrossRefGoogle Scholar
  39. Deniset JF, Kubes P (2016) Recent advances in understanding neutrophils. F1000Research.
  40. Dhabhar FS (2014) Effects of stress on immune function: the good, the bad, and the beautiful. Immunol Res 58:193–210PubMedCrossRefGoogle Scholar
  41. Diez-Fraile A, Meyer E, Burvenich C (2002) Regulation of adhesion molecules on circulating neutrophils during coliform mastitis and their possible immunomodulation with drugs. Vet Immunol Immunopathol 86:1–10PubMedCrossRefGoogle Scholar
  42. Diez-Fraile A, Meyer E, Duchateau L, Paape MJ, Burvenich C (2004a) In vitro regulation of Mac-1 expression on bovine polymorphonuclear leukocytes by endotoxin and tumor necrosis factor-α at different stages of lactation. Can J Vet Res 68:232–235PubMedPubMedCentralGoogle Scholar
  43. Diez-Fraille A, Mehrzad J, Meyer E, Duchateau L, Burvenich C (2004b) Comparison of L-selectin and Mac-1 expression on blood and milk neutrophils during experimental Escherichia Coli-induced mastitis in cows. Am J Vet Res 65:1164–1171PubMedCrossRefGoogle Scholar
  44. Duquette SC, Fischer CD, Feener TD, Muench GP, Morck DW, Barreda DR, Nickerson JG, Buret AG (2014) Anti-inflammatory effects of retinoids and carotenoid derivatives on caspase-3-dependent apoptosis and efferocytosis of bovine neutrophils. Am J Vet Res 75:1064–1075PubMedCrossRefGoogle Scholar
  45. Earley B, Buckham Sporer K, Gupta S (2017) Invited review: relationship between cattle transport, immunity and respiratory disease. Animal 11:486–492PubMedCrossRefGoogle Scholar
  46. Fischer CD, Beatty JK, Zvaigzne CG, Morck DW, Lucas MJ, Buret AG (2011) Anti-inflammatory benefits of antibiotic-induced neutrophil apoptosis: tulathromycin induces caspase-3-dependent neutrophil programmed cell death and inhibits NF-kappaB signaling and CXCL8 transcription. Antimicrob Agents Chemother 55:338–348PubMedCrossRefGoogle Scholar
  47. Fischer CD, Beatty JK, Duquette SC, Morck DW, Lucas MJ, Buret AG (2013) Direct and indirect anti-inflammatory effects of tulathromycin in bovine macrophages: inhibition of CXCL-8 secretion, induction of apoptosis, and promotion of efferocytosis. Antimicrob Agents Chemother 57:1385–1393PubMedPubMedCentralCrossRefGoogle Scholar
  48. Fischer D, Renaux F, Morck H, Lucas B (2014) Tulathromycin exerts Proresolving effects in bovine Neutrophils by inhibiting Phospholipases and altering Leukotriene B4, prostaglandin E2, and Lipoxin A4 production. Antimicrob Agents Chemother 58:4298–4307PubMedPubMedCentralCrossRefGoogle Scholar
  49. Fjell CD, Jenssen H, Fries P, Aich P, Griebel P, Hilpert K, Hancock REW, Cherkasov A (2008) Identification of novel host defense peptides and the absence of alpha-defensins in the bovine genome. Proteins 73:420–430PubMedCrossRefGoogle Scholar
  50. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A (2007) Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176:231–241PubMedPubMedCentralCrossRefGoogle Scholar
  51. Galvão KN, Pighetti GM, Cheong SH, Nydam DV, Gilbert RO (2011) Association between interleukin-8 receptor-α (CXCR1) polymorphism and disease incidence, production, reproduction, and survival in Holstein cows. J Dairy Sci 94:2083–2091PubMedCrossRefGoogle Scholar
  52. Garcia M, Elsasser TH, Qu Y, Zhu X, Moyes KM (2015) Glucose supplementation has minimal effects on blood neutrophil function and gene expression in vitro. J Dairy Sci 98:6139–6150PubMedCrossRefGoogle Scholar
  53. Gennaro R, Schneider C, de Nicola G, Cian F, Romeo D (1978) Biochemical properties of bovine granulocytes. Proc Soc Exp Biol Med 157:342–347PubMedCrossRefGoogle Scholar
  54. Gennaro R, Dewald B, Horisberger U, Gubler HU, Baggiolini M (1983) A novel type of cytoplasmic granule in bovine neutrophils. J Cell Biol 96:1651–1661PubMedCrossRefGoogle Scholar
  55. George JW, Snipes J, Lane VM (2010) Comparison of bovine hematology reference intervals from 1957 to 2006. Vet Clin Pathol 39:138–148PubMedCrossRefGoogle Scholar
  56. Goertz I, Baes C, Weimann C, Reinsch N, Erhardt G (2009) Association between single nucleotide polymorphisms in the CXCR1 gene and somatic cell score in Holstein dairy cattle. J Dairy Sci 92:4018–4022PubMedCrossRefGoogle Scholar
  57. Gondaira S, Higuchi H, Nishi K, Iwano H, Nagahata H (2017) Mycoplasma bovis escapes bovine neutrophil extracellular traps. Vet Microbiol 199:68–73PubMedCrossRefGoogle Scholar
  58. Graugnard DE, Bionaz M, Trevisi E, Moyes KM, Salak-Johnson JL, Wallace RL, Drackley JK, Bertoni G, Loor JJ (2012) Blood immunometabolic indices and polymorphonuclear neutrophil function in peripartum dairy cows are altered by level of dietary energy prepartum. J Dairy Sci 95:1749–1758PubMedCrossRefGoogle Scholar
  59. Greenlee-Wacker MC (2016) Clearance of apoptotic neutrophils and resolution of inflammation. Immunol Rev 273:357–370PubMedPubMedCentralCrossRefGoogle Scholar
  60. Grinberg N, Elazar S, Rosenshine I, Shpigel NY (2008) β-Hydroxybutyrate abrogates formation of bovine Neutrophil extracellular traps and bactericidal activity against mammary pathogenic Escherichia Coli. Infect Immun 76:2802–2807PubMedPubMedCentralCrossRefGoogle Scholar
  61. Hammon DS, Evjen IM, Dhiman TR, Goff JP, Walters JL (2006) Neutrophil function and energy status in Holstein cows with uterine health disorders. Vet Immunol Immunopathol 113:21–29PubMedCrossRefGoogle Scholar
  62. Heidel JR, Taylor SM, Laegreid WW, Silflow RM, Liggitt HD, Leid RW (1989) In vivo chemotaxis of bovine neutrophils induced by 5-lipoxygenase metabolites of arachidonic and eicosapentaenoic acid. Am J Pathol 134:671–676PubMedPubMedCentralGoogle Scholar
  63. Hellenbrand KM, Forsythe KM, Rivera-Rivas JJ, Czuprynski CJ, Aulik NA (2013) Histophilus somni causes extracellular trap formation by bovine neutrophils and macrophages. Microb Pathog 54:67–75PubMedCrossRefGoogle Scholar
  64. Hidalgo MA, Ojeda F, Eyre P, LaBranche TP, Smith C, Hancke JL, Burgos RA (2004) Platelet-activating factor increases pH(i) in bovine neutrophils through the PI3K-ERK1/2 pathway. Br J Pharmacol 141:311–321PubMedCrossRefGoogle Scholar
  65. Hidalgo MA, Loncomán CA, Hidalgo AI, Andrade V, Carretta MD, Burgos RA (2014) Decreased cyclooxygenase-2 gene expression and lactoferrin release in blood neutrophils of heifers during the calving period. Vet Immunol Immunopathol 160:139–144PubMedCrossRefGoogle Scholar
  66. Hoeben D, Heyneman R, Burvenich C (1997) Elevated levels of beta-hydroxybutyric acid in periparturient cows and in vitro effect on respiratory burst activity of bovine neutrophils. Vet Immunol Immunopathol 58:165–170PubMedCrossRefGoogle Scholar
  67. Hoedemaker M, Lund LA, Wagner WC (1992) Influence of arachidonic acid metabolites and steroids on function of bovine polymorphonuclear neutrophils. Am J Vet Res 53:1534–1539PubMedGoogle Scholar
  68. Huang JM, Wang XG, Jiang Q, Sun Y, Yang CH, Ju ZH, Hao HS, Wang CF, Zhong JF, Zhu HB (2016) Identification of CD14 transcript in blood polymorphonuclear neutrophil leukocytes and functional variation in Holsteins. Genet Mol Res.
  69. Hughes HD, Carroll JA, Burdick Sanchez NC, Roberts SL, Broadway PR, May ND, Ballou MA, Richeson JT (2017) Effects of dexamethasone treatment and respiratory vaccination on rectal temperature, complete blood count, and functional capacities of neutrophils in beef steers. J Anim Sci 95:1502–1511PubMedGoogle Scholar
  70. Hulbert LE, Carroll JA, Burdick NC, Randel RD, Brown MS, Ballou MA (2011) Innate immune responses of temperamental and calm cattle after transportation. Vet Immunol Immunopathol 143:66–74PubMedCrossRefGoogle Scholar
  71. Hussen J, Koy M, Petzl W, Schuberth H-J (2016) Neutrophil degranulation differentially modulates phenotype and function of bovine monocyte subsets. Innate Immun 22:124–137PubMedCrossRefGoogle Scholar
  72. Ibeagha-Awemu EM, Lee J-W, Ibeagha AE, Zhao X (2008) Bovine CD14 gene characterization and relationship between polymorphisms and surface expression on monocytes and polymorphonuclear neutrophils. BMC Genet.
  73. Ingvartsen KL, Moyes K (2013) Nutrition, immune function and health of dairy cattle. Animal 7:112–122PubMedCrossRefGoogle Scholar
  74. Ingvartsen KL, Moyes KM (2015) Factors contributing to immunosuppression in the dairy cow during the periparturient period. Jpn J Vet Res 63(Suppl 1):S15–S24PubMedGoogle Scholar
  75. Jerjomiceva N, Seri H, Völlger L, Wang Y, Zeitouni N, Naim HY, von Köckritz-Blickwede M (2014) Enrofloxacin enhances the formation of neutrophil extracellular traps in bovine granulocytes. J Innate Immun 6:706–712PubMedPubMedCentralCrossRefGoogle Scholar
  76. Kawasaki Y, Aoki Y, Magata F, et al. (2014) The effect of single nucleotide polymorphisms in the tumor necrosis factor-α gene on reproductive performance and immune function in dairy cattle. J Reprod Dev 60:173–178PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kehrli ME, Nonnecke BJ, Roth JA (1989) Alterations in bovine neutrophil function during the periparturient period. Am J Vet Res 50:207–214PubMedGoogle Scholar
  78. Keller SL, Jefferson BJ, Jacobs RM, Wood RD (2006) Effects of noncytopathic type 2 bovine viral diarrhea virus on the proliferation of bone marrow progenitor cells. Can J Vet Res 70:20–27PubMedPubMedCentralGoogle Scholar
  79. Kimura K, Goff JP, Kehrli ME (1999) Effects of the presence of the mammary gland on expression of Neutrophil adhesion molecules and Myeloperoxidase activity in Periparturient dairy cows. J Dairy Sci 82:2385–2392PubMedCrossRefGoogle Scholar
  80. Kimura K, Goff JP, Kehrli ME, Reinhardt TA (2002) Decreased neutrophil function as a cause of retained placenta in dairy cattle. J Dairy Sci 85:544–550PubMedCrossRefGoogle Scholar
  81. Kimura K, Goff JP, Canning P, Wang C, Roth JA (2014) Effect of recombinant bovine granulocyte colony-stimulating factor covalently bound to polyethylene glycol injection on neutrophil number and function in periparturient dairy cows. J Dairy Sci 97:4842–4851PubMedCrossRefGoogle Scholar
  82. Kolaczkowska E, Kubes P (2013) Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13:159–175PubMedCrossRefGoogle Scholar
  83. Lahouassa H, Rainard P, Caraty A, Riollet C (2008) Identification and characterization of a new interleukin-8 receptor in bovine species. Mol Immunol 45:1153–1164PubMedCrossRefGoogle Scholar
  84. Lamote I, Meyer E, Duchateau L, Burvenich C (2004) Influence of 17β-Estradiol, progesterone, and Dexamethasone on Diapedesis and viability of bovine blood Polymorphonuclear leukocytes. J Dairy Sci 87:3340–3349PubMedCrossRefGoogle Scholar
  85. LeBlanc SJ, Lissemore KD, Kelton DF, Duffield TF, Leslie KE (2006) Major advances in disease prevention in dairy cattle. J Dairy Sci 89:1267–1279PubMedCrossRefGoogle Scholar
  86. Lee J-W, Paape MJ, Elsasser TH, Zhao X (2003a) Recombinant soluble CD14 reduces severity of intramammary infection by Escherichia Coli. Infect Immun 71:4034–4039PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lee J-W, Paape MJ, Elsasser TH, Zhao X (2003b) Elevated milk soluble CD14 in bovine mammary glands challenged with Escherichia Coli Lipopolysaccharide. J Dairy Sci 86:2382–2389PubMedCrossRefGoogle Scholar
  88. Lee WD, Flynn AN, LeBlanc JM, Merrill JK, Dick P, Morck DW, Buret AG (2004) Tilmicosin-induced bovine neutrophil apoptosis is cell-specific and downregulates spontaneous LTB4 synthesis without increasing Fas expression. Vet Res 35:213–224PubMedCrossRefGoogle Scholar
  89. Leite F, O’Brien S, Sylte MJ, Page T, Atapattu D, Czuprynski CJ (2002) Inflammatory cytokines enhance the interaction of Mannheimia haemolytica leukotoxin with bovine peripheral blood neutrophils in vitro. Infect Immun 70:4336–4343PubMedPubMedCentralCrossRefGoogle Scholar
  90. Leite F, Atapattu D, Kuckleburg C, Schultz R, Czuprynski CJ (2005) Incubation of bovine PMNs with conditioned medium from BHV-1 infected peripheral blood mononuclear cells increases their susceptibility to Mannheimia haemolytica leukotoxin. Vet Immunol Immunopathol 103:187–193PubMedCrossRefGoogle Scholar
  91. Leyva-Baca I, Pighetti G, Karrow NA (2008a) Genotype-specific IL8RA gene expression in bovine neutrophils in response to Escherichia Coli lipopolysaccharide challenge. Anim Genet 39:298–300PubMedCrossRefGoogle Scholar
  92. Leyva-Baca I, Schenkel F, Martin J, Karrow NA (2008b) Polymorphisms in the 5′ upstream region of the CXCR1 chemokine receptor gene, and their association with somatic cell score in Holstein cattle in Canada. J Dairy Sci 91:407–417PubMedCrossRefGoogle Scholar
  93. Li F, Zhang X, Mizzi C, Gordon JR (2002) CXCL8(3-73)K11R/G31P antagonizes the neutrophil chemoattractants present in pasteurellosis and mastitis lesions and abrogates neutrophil influx into intradermal endotoxin challenge sites in vivo. Vet Immunol Immunopathol 90:65–77PubMedCrossRefGoogle Scholar
  94. Lippolis JD, Reinhardt TA (2005) Proteomic survey of bovine neutrophils. Vet Immunol Immunopathol 103:53–65PubMedCrossRefGoogle Scholar
  95. Lippolis JD, Peterson-Burch BD, Reinhardt TA (2006a) Differential expression analysis of proteins from neutrophils in the periparturient period and neutrophils from dexamethasone-treated dairy cows. Vet Immunol Immunopathol 111:149–164PubMedCrossRefGoogle Scholar
  96. Lippolis JD, Reinhardt TA, Goff JP, Horst RL (2006b) Neutrophil extracellular trap formation by bovine neutrophils is not inhibited by milk. Vet Immunol Immunopathol 113:248–255PubMedCrossRefGoogle Scholar
  97. Lohuis JA, Van Leeuwen W, Verheijden JH et al (1988) Effect of dexamethasone on experimental Escherichia Coli mastitis in the cow. J Dairy Sci 71:2782–2789PubMedCrossRefGoogle Scholar
  98. Loiselle MC, Ster C, Talbot BG, Zhao X, Wagner GF, Boisclair YR, Lacasse P (2009) Impact of postpartum milking frequency on the immune system and the blood metabolite concentration of dairy cows. J Dairy Sci 92:1900–1912PubMedCrossRefGoogle Scholar
  99. Lu T, Kobayashi SD, Quinn MT, DeLeo FR (2012) A NET Outcome. Front Immunol.
  100. Lynch EM, Earley B, McGee M, Doyle S (2010) Effect of abrupt weaning at housing on leukocyte distribution, functional activity of neutrophils, and acute phase protein response of beef calves. BMC Vet Res 6:39. PubMedPubMedCentralCrossRefGoogle Scholar
  101. Madsen-Bouterse SA, Rosa GJM, Burton JL (2006) Glucocorticoid modulation of Bcl-2 family members A1 and Bak during delayed spontaneous apoptosis of bovine blood Neutrophils. Endocrinology 147:3826–3834PubMedCrossRefGoogle Scholar
  102. Malazdrewich C, Thumbikat P, Maheswaran SK (2004) Protective effect of dexamethasone in experimental bovine pneumonic mannheimiosis. Microb Pathog 36:227–236PubMedCrossRefGoogle Scholar
  103. Mantovani A, Cassatella MA, Costantini C, Jaillon S (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11:519–531PubMedCrossRefGoogle Scholar
  104. Martinez N, Risco CA, Lima FS, Bisinotto RS, Greco LF, Ribeiro ES, Maunsell F, Galvão K, Santos JEP (2012) Evaluation of peripartal calcium status, energetic profile, and neutrophil function in dairy cows at low or high risk of developing uterine disease. J Dairy Sci 95:7158–7172PubMedCrossRefGoogle Scholar
  105. Martinez N, Sinedino LDP, Bisinotto RS, Ribeiro ES, Gomes GC, Lima FS, Greco LF, Risco CA, Galvão KN, Taylor-Rodriguez D, Driver JP, Thatcher WW, Santos JEP (2014) Effect of induced subclinical hypocalcemia on physiological responses and neutrophil function in dairy cows. J Dairy Sci 97:874–887PubMedCrossRefGoogle Scholar
  106. McClenahan DJ, Evanson OA, Weiss DJ (2002) In vitro evaluation of the role of platelet-activating factor and interleukin-8 in Mannheimia haemolytica-induced bovine pulmonary endothelial cell injury. Am J Vet Res 63:394–401PubMedCrossRefGoogle Scholar
  107. McDougall S, LeBlanc SJ, Heiser A (2017) Effect of prepartum energy balance on neutrophil function following pegbovigrastim treatment in periparturient cows. J Dairy Sci.
  108. Mehrzad J, Duchateau L, Burvenich C (2004) Viability of milk Neutrophils and severity of bovine Coliform mastitis. J Dairy Sci 87:4150–4162PubMedCrossRefGoogle Scholar
  109. Melendez P, Marin MP, Robles J, Rios C, Duchens M, Archbald L (2009) Relationship between serum nonesterified fatty acids at calving and the incidence of periparturient diseases in Holstein dairy cows. Theriogenology 72:826–833PubMedCrossRefGoogle Scholar
  110. Mitchell GB, Albright BN, Caswell JL (2003) Effect of interleukin-8 and granulocyte colony-stimulating factor on priming and activation of bovine neutrophils. Infect Immun 71:1643–1649PubMedPubMedCentralCrossRefGoogle Scholar
  111. Mitchell GB, Clark ME, Siwicky M, Caswell JL (2008) Stress alters the cellular and proteomic compartments of bovine bronchoalveolar lavage fluid. Vet Immunol Immunopathol 125:111–125PubMedCrossRefGoogle Scholar
  112. Moya SL, Gómez MA, Boyle LA, Mee JF, O’Brien B, Arkins S (2008) Effects of milking frequency on phagocytosis and oxidative burst activity of phagocytes from primiparous and multiparous dairy cows during early lactation. J Dairy Sci 91:587–595PubMedCrossRefGoogle Scholar
  113. Moyes KM, Drackley JK, Salak-Johnson JL, Morin DE, Hope JC, Loor JJ (2009a) Dietary-induced negative energy balance has minimal effects on innate immunity during a streptococcus uberis mastitis challenge in dairy cows during midlactation. J Dairy Sci 92:4301–4316PubMedCrossRefGoogle Scholar
  114. Moyes KM, Larsen T, Friggens NC, Drackley JK, Ingvartsen KL (2009b) Identification of potential markers in blood for the development of subclinical and clinical mastitis in dairy cattle at parturition and during early lactation. J Dairy Sci 92:5419–5428PubMedCrossRefGoogle Scholar
  115. Muñoz-Caro T, Hermosilla C, Silva LMR, Cortes H, Taubert A (2014) Neutrophil extracellular traps as innate immune reaction against the emerging Apicomplexan parasite Besnoitia besnoiti. PLoS ONE 9:e91415. PubMedPubMedCentralCrossRefGoogle Scholar
  116. Muñoz-Caro T, Lendner M, Daugschies A, Hermosilla C, Taubert A (2015a) NADPH oxidase, MPO, NE, ERK1/2, p38 MAPK and Ca2+ influx are essential for Cryptosporidium Parvum-induced NET formation. Dev Comp Immunol 52:245–254PubMedCrossRefGoogle Scholar
  117. Muñoz-Caro T, Mena Huertas SJ, Conejeros I, Alarcón P, Hidalgo MA, Burgos RA, Hermosilla C, Taubert A (2015b) Eimeria bovis-triggered neutrophil extracellular trap formation is CD11b-, ERK 1/2-, p38 MAP kinase- and SOCE-dependent. Vet Res 46:23. PubMedPubMedCentralCrossRefGoogle Scholar
  118. Muñoz-Caro T, Rubio RMC, Silva LMR, Magdowski G, Gärtner U, McNeilly TN, Taubert A, Hermosilla C (2015c) Leucocyte-derived extracellular trap formation significantly contributes to Haemonchus contortus larval entrapment. Parasit Vectors 8:607. PubMedPubMedCentralCrossRefGoogle Scholar
  119. Nagahata H (2004) Bovine leukocyte adhesion deficiency (BLAD): a review. J Vet Med Sci 66:1475–1482PubMedCrossRefGoogle Scholar
  120. Nagahata H, Masuyama A, Masue M, Yuki M, Higuchi H, Ohtsuka H, Kurosawa T, Sato H, Noda H (1997) Leukocyte emigration in normal calves and calves with leukocyte adhesion deficiency. J Vet Med Sci 59:1143–1147PubMedCrossRefGoogle Scholar
  121. Nauseef WM (2014) Myeloperoxidase in human neutrophil host defense. Cell Microbiol 16:1146–1155PubMedPubMedCentralCrossRefGoogle Scholar
  122. Nemali S, Siemsen DW, Nelson LK, Bunger PL, Faulkner CL, Rainard P, Gauss KA, Jutila MA, Quinn MT (2008) Molecular analysis of the bovine anaphylatoxin C5a receptor. J Leukoc Biol 84:537–549PubMedPubMedCentralCrossRefGoogle Scholar
  123. Nemchinov LG, Paape MJ, Sohn EJ, Bannerman DD, Zarlenga DS, Hammond RW (2006) Bovine CD14 receptor produced in plants reduces severity of intramammary bacterial infection. FASEB J 20:1345–1351PubMedCrossRefGoogle Scholar
  124. Nunes JS, Lawhon SD, Rossetti CA, Khare S, Figueiredo JF, Gull T, Burghardt RC, Bäumler AJ, Tsolis RM, Andrews-Polymenis HL, Adams LG (2010) Morphologic and cytokine profile characterization of salmonella enterica serovar typhimurium infection in calves with bovine leukocyte adhesion deficiency. Vet Pathol 47:322–333PubMedCrossRefGoogle Scholar
  125. O’Loughlin A, McGee M, Waters SM, Doyle S, Earley B (2011) Examination of the bovine leukocyte environment using immunogenetic biomarkers to assess immunocompetence following exposure to weaning stress. BMC Vet Res.
  126. O’Loughlin A, McGee M, Doyle S, Earley B (2014) Biomarker responses to weaning stress in beef calves. Res Vet Sci 97:458–463PubMedCrossRefGoogle Scholar
  127. Paape MJ, Lilius EM, Wiitanen PA, Kontio MP, Miller RH (1996) Intramammary defense against infections induced by Escherichia Coli in cows. Am J Vet Res 57:477–482PubMedGoogle Scholar
  128. Paape MJ, Bannerman DD, Zhao X, Lee J-W (2003) The bovine neutrophil: structure and function in blood and milk. Vet Res 34:597–627PubMedCrossRefGoogle Scholar
  129. Pawlik A, Sender G, Kapera M, Korwin-Kossakowska A (2015) Association between interleukin 8 receptor α gene (CXCR1) and mastitis in dairy cattle. Cent-Eur J Immunol 40:153–158. PubMedPubMedCentralCrossRefGoogle Scholar
  130. Pechous RD (2017) With friends like these: the complex role of Neutrophils in the progression of severe pneumonia. Front Cell Infect Microbiol 7:160. PubMedPubMedCentralCrossRefGoogle Scholar
  131. Prince LR, Whyte MK, Sabroe I, Parker LC (2011) The role of TLRs in neutrophil activation. Curr Opin Pharmacol 11:397–403PubMedCrossRefGoogle Scholar
  132. Rahman MM, Miranda-Ribera A, Lecchi C, Bronzo V, Sartorelli P, Franciosi F, Ceciliani F (2008) Alpha1-acid glycoprotein is contained in bovine neutrophil granules and released after activation. Vet Immunol Immunopathol 125:71–81PubMedCrossRefGoogle Scholar
  133. Rainard P, Riollet C, Poutrel B, Paape MJ (2000) Phagocytosis and killing of Staphylococcus Aureus by bovine neutrophils after priming by tumor necrosis factor-alpha and the des-arginine derivative of C5a. Am J Vet Res 61:951–959PubMedCrossRefGoogle Scholar
  134. Rainard P, Riollet C, Berthon P, Cunha P, Fromageau A, Rossignol C, Gilbert FB (2008) The chemokine CXCL3 is responsible for the constitutive chemotactic activity of bovine milk for neutrophils. Mol Immunol 45:4020–4027PubMedCrossRefGoogle Scholar
  135. Rambeaud M, Pighetti GM (2005) Impaired neutrophil migration associated with specific bovine CXCR2 genotypes. Infect Immun 73:4955–4959PubMedPubMedCentralCrossRefGoogle Scholar
  136. Rambeaud M, Pighetti GM (2007) Differential calcium signaling in dairy cows with specific CXCR1 genotypes potentially related to interleukin-8 receptor functionality. Immunogenetics 59:53–58PubMedCrossRefGoogle Scholar
  137. Rambeaud M, Clift R, Pighetti GM (2006) Association of a bovine CXCR2 gene polymorphism with neutrophil survival and killing ability. Vet Immunol Immunopathol 111:231–238PubMedCrossRefGoogle Scholar
  138. Rastani RR, Andrew SM, Zinn SA, Sniffen CJ (2001) Body Composition and Estimated Tissue Energy Balance in Jersey and Holstein Cows During Early Lactation1. J Dairy Sci 84:1201–1209PubMedCrossRefGoogle Scholar
  139. Rausch PG, Moore TG (1975) Granule enzymes of polymorphonuclear neutrophils: a phylogenetic comparison. Blood 46:913–919PubMedGoogle Scholar
  140. Rinaldi M, Ceciliani F, Lecchi C, Moroni P, Bannerman DD (2008a) Differential effects of alpha1-acid glycoprotein on bovine neutrophil respiratory burst activity and IL-8 production. Vet Immunol Immunopathol 126:199–210PubMedCrossRefGoogle Scholar
  141. Rinaldi M, Moroni P, Paape MJ, Bannerman DD (2008b) Differential alterations in the ability of bovine neutrophils to generate extracellular and intracellular reactive oxygen species during the periparturient period. Vet J 178:208–213PubMedCrossRefGoogle Scholar
  142. Rivera-Rivas JJ, Kisiela D, Czuprynski CJ (2009) Bovine herpesvirus type 1 infection of bovine bronchial epithelial cells increases neutrophil adhesion and activation. Vet Immunol Immunopathol 131:167–176PubMedCrossRefGoogle Scholar
  143. Roth JA, Kaeberle ML (1981) Effects of in vivo dexamethasone administration on in vitro bovine polymorphonuclear leukocyte function. Infect Immun 33:434–441.PubMedPubMedCentralGoogle Scholar
  144. Ruiz R, Tedeschi LO, Sepúlveda A (2017) Investigation of the effect of pegbovigrastim on some periparturient immune disorders and performance in Mexican dairy herds. J Dairy Sci 100:3305–3317PubMedCrossRefGoogle Scholar
  145. Russell CD, Widdison S, Leigh JA, Coffey TJ (2012) Identification of single nucleotide polymorphisms in the bovine toll-like receptor 1 gene and association with health traits in cattle. Vet Res 43:17. PubMedPubMedCentralCrossRefGoogle Scholar
  146. Sample AK, Czuprynski CJ (1991) Priming and stimulation of bovine neutrophils by recombinant human interleukin-1 alpha and tumor necrosis factor alpha. J Leukoc Biol 49:107–115PubMedCrossRefGoogle Scholar
  147. Sandoval AJ, Riquelme JP, Carretta MD, Hancke JL, Hidalgo MA, Burgos RA (2007) Store-operated calcium entry mediates intracellular alkalinization, ERK1/2, and Akt/PKB phosphorylation in bovine neutrophils. J Leukoc Biol 82:1266–1277PubMedCrossRefGoogle Scholar
  148. Scalia D, Lacetera N, Bernabucci U, Demeyere K, Duchateau L, Burvenich C (2006) In vitro effects of nonesterified fatty acids on bovine neutrophils oxidative burst and viability. J Dairy Sci 89:147–154PubMedCrossRefGoogle Scholar
  149. Scocchi M, Skerlavaj B, Romeo D, Gennaro R (1992) Proteolytic cleavage by neutrophil elastase converts inactive storage proforms to antibacterial bactenecins. Eur J Biochem 209:589–595PubMedCrossRefGoogle Scholar
  150. Selsted ME, Tang YQ, Morris WL, McGuire PA, Novotny MJ, Smith W, Henschen AH, Cullor JS (1993) Purification, primary structures, and antibacterial activities of beta-defensins, a new family of antimicrobial peptides from bovine neutrophils. J Biol Chem 268:6641–6648PubMedGoogle Scholar
  151. Shimizu T, Kawasaki Y, Aoki Y, Magata F, Kawashima C, Miyamoto A (2017) Effect of single nucleotide polymorphisms of toll-like receptor 4 (TLR 4) on reproductive performance and immune function in dairy cows. Biochem Genet 55:212–222PubMedCrossRefGoogle Scholar
  152. Siebert L, Headrick S, Lewis M, Gillespie B, Young C, Wojakiewicz L, Kerro-Dego O, Prado ME, Almeida R, Oliver SP, Pighetti GM (2017) Genetic variation in CXCR1 haplotypes linked to severity of streptococcus uberis infection in an experimental challenge model. Vet Immunol Immunopathol 190:45–52PubMedCrossRefGoogle Scholar
  153. Silva LMR, Muñoz-Caro T, Burgos RA, Hidalgo MA, Taubert A, Hermosilla C (2016) Far beyond Phagocytosis: phagocyte-derived extracellular traps act efficiently against protozoan parasites in vitro and in vivo. Mediat Inflamm 2016:5898074. Google Scholar
  154. Singh, Ritchey, Confer (2010) Mannheimia haemolytica: bacterial-host interactions in bovine pneumonia. Vet Pathol 48:338–348PubMedCrossRefGoogle Scholar
  155. Sládek Z, Rysánek D (2001) Neutrophil apoptosis during the resolution of bovine mammary gland injury. Res Vet Sci 70:41–46PubMedCrossRefGoogle Scholar
  156. Sladek Z, Rysanek D (2006) The role of CD14 during resolution of experimentally induced Staphylococcus Aureus and streptococcus uberis mastitis. Comp Immunol Microbiol Infect Dis 29:243–262PubMedCrossRefGoogle Scholar
  157. Sladek Z, Rysanek D (2011) Cell death and CD14 expression in resident and inflammatory polymorphonuclear leukocytes from virgin bovine mammary gland. Res Vet Sci 90:226–234PubMedCrossRefGoogle Scholar
  158. Sládek Z, Rysánek D, Faldyna M (2002) Activation of phagocytes during initiation and resolution of mammary gland injury induced by lipopolysaccharide in heifers. Vet Res 33:191–204PubMedCrossRefGoogle Scholar
  159. Sladek Z, Rysanek D, Ryznarova H, Faldyna M (2005) Neutrophil apoptosis during experimentally induced Staphylococcus Aureus mastitis. Vet Res 36:629–643PubMedCrossRefGoogle Scholar
  160. Slocombe RF, Malark J, Ingersoll R, Derksen FJ, Robinson NE (1985) Importance of neutrophils in the pathogenesis of acute pneumonic pasteurellosis in calves. Am J Vet Res 46:2253–2258PubMedGoogle Scholar
  161. Smits E, Burvenich C, Guidry AJ, Roets E (1998) In vitro expression of adhesion receptors and Diapedesis by Polymorphonuclear Neutrophils during experimentally induced streptococcus uberis mastitis. Infect Immun 66:2529–2534PubMedPubMedCentralGoogle Scholar
  162. Sohn EJ, Paape MJ, Bannerman DD, Connor EE, Fetterer RH, Peters RR (2007) Shedding of sCD14 by bovine neutrophils following activation with bacterial lipopolysaccharide results in down-regulation of IL-8. Vet Res 38:95–108PubMedCrossRefGoogle Scholar
  163. Sordillo LM (2016) Nutritional strategies to optimize dairy cattle immunity. J Dairy Sci 99:4967–4982PubMedCrossRefGoogle Scholar
  164. Sordillo LM, Raphael W (2013) Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders. Vet Clin North Am Food Anim Pract 29:267–278PubMedCrossRefGoogle Scholar
  165. Ster C, Loiselle M-C, Lacasse P (2012) Effect of postcalving serum nonesterified fatty acids concentration on the functionality of bovine immune cells. J Dairy Sci 95:708–717PubMedCrossRefGoogle Scholar
  166. Stevens MGH, Peelman LJ, De Spiegeleer B, Pezeshki A, Van De Walle GR, Duchateau L, Burvenich C (2011a) Differential gene expression of the toll-like receptor-4 cascade and neutrophil function in early- and mid-lactating dairy cows. J Dairy Sci 94:1277–1288PubMedCrossRefGoogle Scholar
  167. Stevens MGH, Van Poucke M, Peelman LJ, Rainard P, De Spiegeleer B, Rogiers C, Van de Walle GR, Duchateau L, Burvenich C (2011b) Anaphylatoxin C5a-induced toll-like receptor 4 signaling in bovine neutrophils. J Dairy Sci 94:152–164PubMedCrossRefGoogle Scholar
  168. Stojkovic B, McLoughlin RM, Meade KG (2016) In vivo relevance of polymorphic interleukin 8 promoter haplotype for the systemic immune response to LPS in Holstein-Friesian calves. Vet Immunol Immunopathol 182:1–10PubMedCrossRefGoogle Scholar
  169. Storici P, Tossi A, Lenarcic B, Romeo D (1996) Purification and structural characterization of bovine cathelicidins, precursors of antimicrobial peptides. Eur J Biochem 238:769–776PubMedCrossRefGoogle Scholar
  170. Suriyasathaporn W, Daemen AJ, Noordhuizen-Stassen EN, Dieleman SJ, Nielen M, Schukken YH (1999) Beta-hydroxybutyrate levels in peripheral blood and ketone bodies supplemented in culture media affect the in vitro chemotaxis of bovine leukocytes. Vet Immunol Immunopathol 68:177–186PubMedCrossRefGoogle Scholar
  171. Swain SD, Bunger PL, Sipes KM, Nelson LK, Jutila KL, Boylan SM, Quinn MT (1998) Platelet-activating factor induces a concentration-dependent spectrum of functional responses in bovine neutrophils. J Leukoc Biol 64:817–827PubMedCrossRefGoogle Scholar
  172. Swain SD, Jutila KL, Quinn MT (2000) Cell-surface lactoferrin as a marker for degranulation of specific granules in bovine neutrophils. Am J Vet Res 61:29–37PubMedCrossRefGoogle Scholar
  173. Swain SD, Siemsen DW, Hanson AJ, Quinn MT (2001) Activation-induced mobilization of secretory vesicles in bovine neutrophils. Am J Vet Res 62:1776–1781PubMedCrossRefGoogle Scholar
  174. Tan X, Li W-W, Guo J, Zhou J-Y (2012) Down-regulation of NOD1 in neutrophils of periparturient dairy cows. Vet Immunol Immunopathol 150:133–139PubMedCrossRefGoogle Scholar
  175. Tan X, Wei L-J, Fan G-J, Jiang Y-N, Yu X-P (2015) Effector responses of bovine blood neutrophils against Escherichia Coli: role of NOD1/NF-κB signalling pathway. Vet Immunol Immunopathol 168:68–76PubMedCrossRefGoogle Scholar
  176. Thomas CJ, Schroder K (2013) Pattern recognition receptor function in neutrophils. Trends Immunol 34:317–328PubMedCrossRefGoogle Scholar
  177. Tomasinsig L, Scocchi M, Di Loreto C, Artico D, Zanetti M (2002) Inducible expression of an antimicrobial peptide of the innate immunity in polymorphonuclear leukocytes. J Leukoc Biol 72:1003–1010PubMedGoogle Scholar
  178. Tomasinsig L, De Conti G, Skerlavaj B, Piccinini R, Mazzilli M, D’Este F, Tossi A, Zanetti M (2010) Broad-Spectrum activity against bacterial mastitis pathogens and activation of mammary epithelial cells support a protective role of Neutrophil Cathelicidins in bovine mastitis. Infect Immun 78:1781–1788PubMedPubMedCentralCrossRefGoogle Scholar
  179. Tydell CC, Yount N, Tran D, et al. (2002) Isolation, Characterization, and Antimicrobial Properties of Bovine Oligosaccharide-binding Protein a microbicidal granule protein of eosinophils and neutrophils. J Biol Chem 277:19658–19664PubMedCrossRefGoogle Scholar
  180. Tydell CC, Yuan J, Tran P, Selsted ME (2006) Bovine Peptidoglycan recognition protein-S: antimicrobial activity, localization, secretion, and binding properties. J Immunol 176:1154–1162PubMedCrossRefGoogle Scholar
  181. Valli VE, Hulland TJ, McSherry BJ, Robinson GA, Gilman JP (1971) The kinetics of haematopoiesis in the calf. I. An autoradiographical study of myelopoiesis in normal, anaemic and endotoxin treated calves. Res Vet Sci 12:535–550PubMedGoogle Scholar
  182. van Abel RJ, Tang YQ, Rao VS, Dobbs CH, Tran D, Barany G, Selsted ME (1995) Synthesis and characterization of indolicidin, a tryptophan-rich antimicrobial peptide from bovine neutrophils. Int J Pept Protein Res 45:401–409PubMedCrossRefGoogle Scholar
  183. Van Oostveldt K, Vangroenweghe F, Dosogne H, Burvenich C (2001) Apoptosis and necrosis of blood and milk polymorphonuclear leukocytes in early and midlactating healthy cows. Vet Res 32:617–622PubMedCrossRefGoogle Scholar
  184. Verbeke J, Piepers S, Peelman L, Van Poucke M, De Vliegher S (2012) Pathogen-group specific association between CXCR1 polymorphisms and subclinical mastitis in dairy heifers. J Dairy Res 79:341–351PubMedCrossRefGoogle Scholar
  185. Verbeke J, Piepers S, Peelman L, Van Poucke M, De Vliegher S (2014a) Association of CXCR1 polymorphisms with apoptosis, necrosis and concentration of milk neutrophils in early lactating dairy heifers. Res Vet Sci 97:55–59PubMedCrossRefGoogle Scholar
  186. Verbeke J, Van Poucke M, Peelman L, Piepers S, De Vliegher S (2014b) Associations between CXCR1 polymorphisms and pathogen-specific incidence rate of clinical mastitis, test-day somatic cell count, and test-day milk yield. J Dairy Sci 97:7927–7939PubMedCrossRefGoogle Scholar
  187. Verbeke J, Boulougouris X, Rogiers C, Burvenich C, Peelman L, De Spiegeleer B, De Vliegher S (2015a) Reactive oxygen species generation by bovine blood neutrophils with different CXCR1 (IL8RA) genotype following Interleukin-8 incubation. BMC Vet Res.
  188. Verbeke J, Piccart K, Piepers S, Van Poucke M, Peelman L, De Visscher A, De Vliegher S (2015b) Somatic cell count and milk neutrophil viability of dairy heifers with specific CXCR1 genotypes following experimental intramammary infection with staphylococcus chromogenes originating from milk. Vet J Lond Engl 204:322–326Google Scholar
  189. Verbeke J, Van Poucke M, Peelman L, De Vliegher S (2015c) Differential expression of CXCR1 and commonly used reference genes in bovine milk somatic cells following experimental intramammary challenge. BMC Genet.
  190. Villagra-Blanco R, Silva LMR, Muñoz-Caro T, Yang Z, Li J, Gärtner U, Taubert A, Zhang X, Hermosilla C (2017) Bovine Polymorphonuclear Neutrophils cast Neutrophil extracellular traps against the abortive parasite Neospora caninum. Front Immunol.
  191. Wang Y, Zarlenga DS, Paape MJ, Dahl GE (2002) Recombinant bovine soluble CD14 sensitizes the mammary gland to lipopolysaccharide. Vet Immunol Immunopathol 86:115–124PubMedCrossRefGoogle Scholar
  192. Wang Y, Zarlenga DS, Paape MJ, Dahl GE, Tomita GM (2003) Functional analysis of recombinant bovine CD14. Vet Res 34:413–421PubMedCrossRefGoogle Scholar
  193. Wang X, Xu S, Gao X, Ren H, Chen J (2007) Genetic polymorphism of TLR4 gene and Correlation with mastitis in cattle. J Genet Genomics 34:406–412PubMedCrossRefGoogle Scholar
  194. Wang J, Zhou X, Pan B, Yang L, Yin X, Xu B, Zhao D (2013) Investigation of the effect of Mycobacterium Bovis infection on bovine neutrophils functions. Tuberculosis 93:675–687PubMedCrossRefGoogle Scholar
  195. Watson GL, Slocombe RF, Robinson NE, Sleight SD (1995) Enzyme release by bovine neutrophils. Am J Vet Res 56:1055–1061PubMedGoogle Scholar
  196. Weber PSD, Toelboell T, Chang L-C, Tirrell JD, Saama PM, Smith GW, Burton JL (2004) Mechanisms of glucocorticoid-induced down-regulation of neutrophil L-selectin in cattle: evidence for effects at the gene-expression level and primarily on blood neutrophils. J Leukoc Biol 75:815–827PubMedCrossRefGoogle Scholar
  197. Weber PSD, Madsen-Bouterse SA, Rosa GJM, Sipkovsky S, Ren X, Almeida PE, Kruska R, Halgren RG, Barrick JL, Burton JL (2006) Analysis of the bovine neutrophil transcriptome during glucocorticoid treatment. Physiol Genomics 28:97–112PubMedCrossRefGoogle Scholar
  198. Wei L-J, Tan X, Fan G-J, Jiang Y-N, Shah QA (2016) Role of the NOD1/NF-κB pathway on bovine neutrophil responses to crude lipopolysaccharide. Vet J 214:24–31PubMedCrossRefGoogle Scholar
  199. Weiss DJ, Bauer MC, Whiteley LO, Maheswaran SK, Ames TR (1991) Changes in blood and bronchoalveolar lavage fluid components in calves with experimentally induced pneumonic pasteurellosis. Am J Vet Res 52:337–344PubMedGoogle Scholar
  200. Weiss DJ, Wardrop KJ, Schalm OW (2010) Schalm’s veterinary hematology, 6th ed. In: DJ Weiss, KJ Wardrop. Ames, Wiley-BlackwellGoogle Scholar
  201. Wessely-Szponder J (2008) The influence of TNFalpha and IL-8 on secretory action of neutrophils isolated from heifers in the course of bovine respiratory disease. Acta Vet Hung 56:187–196PubMedCrossRefGoogle Scholar
  202. Whale TA, Beskorwayne TK, Babiuk LA, Griebel PJ (2006a) Bovine polymorphonuclear cells passively acquire membrane lipids and integral membrane proteins from apoptotic and necrotic cells. J Leukoc Biol 79:1226–1233PubMedCrossRefGoogle Scholar
  203. Whale TA, Wilson HL, Tikoo SK, Babiuk LA, Griebel PJ (2006b) Pivotal advance: passively acquired membrane proteins alter the functional capacity of bovine polymorphonuclear cells. J Leukoc Biol 80:481–491PubMedCrossRefGoogle Scholar
  204. Winters KRH, Meyer E, Van Merris VM, Van Den Broeck WLM, Duchateau L, Burvenich C (2003) Sex steroid hormones do not influence the oxidative burst activity of polymorphonuclear leukocytes from ovariectomized cows in vitro. Steroids 68:397–406PubMedCrossRefGoogle Scholar
  205. Worku M, Morris A (2009) Binding of different forms of lipopolysaccharide and gene expression in bovine blood neutrophils. J Dairy Sci 92:3185–3193PubMedCrossRefGoogle Scholar
  206. Yagi Y, Shiono H, Chikayama Y, Ohnuma A, Nakamura I, Yayou K-I (2004) Transport stress increases somatic cell counts in milk, and enhances the migration capacity of peripheral blood neutrophils of dairy cows. J Vet Med Sci 66:381–387PubMedCrossRefGoogle Scholar
  207. Yildiz K, Gokpinar S, Gazyagci AN, Babur C, Sursal N, Azkur AK (2017) Role of NETs in the difference in host susceptibility to Toxoplasma gondii between sheep and cattle. Vet Immunol Immunopathol 189:1–10PubMedCrossRefGoogle Scholar
  208. Youngerman SM, Saxton AM, Oliver SP, Pighetti GM (2004) Association of CXCR2 polymorphisms with subclinical and clinical mastitis in dairy cattle. J Dairy Sci 87:2442–2448PubMedCrossRefGoogle Scholar
  209. Yount NY, Yuan J, Tarver A, Castro T, Diamond G, Tran PA, Levy JN, McCullough C, Cullor JS, Bevins CL, Selsted ME (1999) Cloning and expression of bovine Neutrophil β-Defensins biosynthetic profile during neutrophilic maturation and localization of mature peptide to novel cytoplasmic dense granules. J Biol Chem 274:26249–26258PubMedCrossRefGoogle Scholar
  210. Youssef SA, Clark ME, Caswell JL (2004) Effect of bovine granulocyte Colony-stimulating factor on the development of pneumonia caused by Mannheimia haemolytica. Vet Pathol Online 41:649–657CrossRefGoogle Scholar
  211. Zanetti M, Litteri L, Gennaro R, Horstmann H, Romeo D (1990) Bactenecins, defense polypeptides of bovine neutrophils, are generated from precursor molecules stored in the large granules. J Cell Biol 111:1363–1371PubMedCrossRefGoogle Scholar
  212. Zhang G, Young JR, Tregaskes CA, Sopp P, Howard CJ (1995) Identification of a novel class of mammalian Fc gamma receptor. J Immunol 155:1534–1541PubMedGoogle Scholar
  213. Zhang H, Zhao G, Guo Y, Menghwar H, Chen Y, Chen H, Guo A (2016) Mycoplasma bovis MBOV_RS02825 encodes a Secretory nuclease associated with Cytotoxicity. Int J Mol Sci.

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PathobiologyUniversity of GuelphGuelphCanada

Personalised recommendations