Gene expression signatures in neutrophils exposed to glucocorticoids: A new paradigm to help explain "neutrophil dysfunction" in parturient dairy cows

Veterinary Immunology and Immunopathology

Volumn 105, Issue 3-4, 2005, Pages 197-219

  Burton, Jeanne L ^a,b   Madsen, Sally A ^a   Chang, Ling Chu ^a   Weber, Patty S D ^a   Buckham, Kelly R ^a   Van Dorp, Renate ^b   Hickey, Mary Clare ^c   Earley, Bernadette ^c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Ctr for Animal Functional Genomics   (United States)

^c GRANGE RESEARCH CENTRE   (Ireland)

Author keywords

Bone marrow cells; cDNA microarray; Cortisol; Dexamethasone; Neutrophils

Indexed keywords

CYTOKINE; DEXAMETHASONE; GLUCOCORTICOID; HYDROCORTISONE;

ANALYTIC METHOD; ANTIMICROBIAL ACTIVITY; BONE MARROW; CELL COUNT; CELL FUNCTION; CELL MATURATION; CELLULAR IMMUNITY; CHILDBIRTH; CORRELATION ANALYSIS; DAIRY CATTLE; DISEASE SEVERITY; DNA MICROARRAY; DOWN REGULATION; FUNCTIONAL GENOMICS; GENE EXPRESSION; GENE EXPRESSION PROFILING; HEMATOPOIESIS; HORMONAL THERAPY; IMMUNE RESPONSE; IMMUNOBIOLOGY; INCIDENCE; INFLAMMATORY DISEASE; LIFESPAN; NEUTROPHIL; NONHUMAN; PHENOTYPE; REGULATOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; STRESS; UPREGULATION; VETERINARY MEDICINE;

EID: 16244423331     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2005.02.012     Document Type: Article

References (111)

1. W.Y. Almawi, and O.K. Melemedjian Negative regulation of nuclear factor-kappaB activation and function by glucocorticoids J. Mol. Endocrinol. 28 2002 69 78
2. F. Andrade, L.A. Casciola-Rosen, and A. Rosen Granzyme B-induced cell death Acta Haematol. 111 2004 28 41
3. C.M. Bamberger, H.M. Schulte, and G.P. Chrousos Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids Endocr. Rev. 17 1996 245 259
4. M. Beato, and J. Klug Steroid hormone receptors: an update Hum. Reprod. Update 6 2000 225 236
5. J.R. Bradley, and J.S. Pober Tumor necrosis factor receptor-associated factors (TRAFs) Oncogene 20 2001 6482 6491
6. J.M. Bowen, L. Chamley, J.A. Keelan, and M.D. Mitchell Cytokines of the placenta and extra-placental membranes: roles and regulation during human pregnancy and parturition Placenta 23 2002 257 273
7. U. Brandt, S. Kerscher, S. Drose, K. Zwicker, and V. Zickermann Proton pumping by NADH:ubiquinone oxidoreductase. A redox driven conformational change mechanism? FEBS Lett. 545 2003 9 17
8. V. Brinkmann, U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, D.S. Weiss, Y. Weinrauch, and A. Zychlinsky Neutrophil extracellular traps kill bacteria Science 303 2004 1532 1535
9. J.L. Burton, and R.J. Erskine Mastitis and immunity: some new ideas for an old disease Vet. Clin. N. Am. Food Anim. Pract. 19 2003 1 45
10. J.L. Burton, and M.E. Kehrli Jr. Regulation of neutrophil adhesion molecules, and shedding of Staphylococcus aureus in milk of cortisol- and dexamethasone-treated cows Am. J. Vet. Res. 56 1995 997 1006
11. J.L. Burton, M.E. Kehrli Jr., S. Kapil, and R.L. Horst Regulation of L-selectin and CD18 on bovine neutrophils by glucocorticoids: effects of cortisol and dexamethasone J. Leukoc. Biol. 57 1995 317 325
12. C. Burvenich, V. Van Merris, J. Mehrzad, A. Diez-Fraile, and L. Duchateau Severity of E. coli mastitis is mainly determined by cow factors Vet. Res. 34 2003 521 564
13. T.-Q. Cai, P.G. Weston, L.A. Lund, B. Brodie, D.J. McKenna, and W.C. Wagner Associations between neutrophil functions and periparturient disorders in cows Am. J. Vet. Res. 55 1994 934 943
14. M.A. Cassatella Production of cytokines by polymorphonuclear neutrophils D.I. Gabrilovich The Neutrophils: New Outlook for Old Cells 1999 Imperial College Press London, UK 151 229 Chapter 5
15. J. Chakir, J. Shannon, S. Molet, M. Fukakusa, J. Elias, M. Laviolette, L.P. Boulet, and Q. Hamid Airway remodeling-associated mediators in moderate to severe asthma: effect of steroids on TGF-beta, IL-11, IL-17, and type I and type III collagen expression J. Allergy Clin. Immunol. 111 2003 1293 1298
16. L.-C. Chang, S.A. Madsen, T. Toelboell, P.S.D. Weber, and J.L. Burton Effects of glucocorticoids on Fas gene expression in bovine blood neutrophils J. Endocrinol. 183 2004 569 583
17. M. Chassagne, J. Barnouin, and J.P. Chacornac Risk factors for stillbirth in Holstein heifers under field conditions in France: a prospective study Theriogenology 51 1999 1477 1488
18. C. Chavatte, G. Brown, J.C. Ousey, M. Silver, C. Cottrill, A.L. Fowden, A.J. McGladdery, and P.D. Rossdale Studies of bone marrow and leucocyte counts in peripheral blood in fetal and newborn foals J. Reprod. Fertil. Suppl. 44 1991 603 608
19. A.I. Chin, J. Shu, C. Shan Shi, Z. Yao, J.H. Kehrl, and G. Cheng TANK potentiates tumor necrosis factor receptor-associated factor-mediated c-Jun N-terminal kinase/stress-activated protein kinase activation through the germinal center kinase pathway Mol. Cell. Biol. 19 1999 6665 6672
20. Eicher, S., Burton, J.L., 2004. Immune system: stress effects. In: Pond, W.C., Bell, A.W. (Eds.), Encyclopedia of Animal Science. Marcel Dekker Publisher, New York, NY, pp. 544-547 (available at http://www.dekker.com).
21. H. Eiler, and F.M. Hopkins Bovine retained placenta: effects of collagenase and hyaluronidase on detachment of placenta Biol. Reprod. 46 1992 580 585
22. N.F. Fanning, H.P. Redmond, and D. Bouchier-Hayes Neutrophils and apoptosis D.I. Gabrilovich The Neutrophils: New Outlook for Old Cells 1999 Imperial College Press London, UK 231 242 Chapter 6
23. S.J. Fortunato, and R. Menon Distinct molecular events suggest different pathways for preterm labor and premature rupture of membranes Am. J. Obstet. Gynecol. 184 2001 1399 1405
24. S.J. Fortunato, and R. Menon Screening of novel matrix metalloproteinases (MMPs) in human fetal membranes J. Assist. Reprod. Genet. 19 2002 483 486
25. M.L. Genova, M.M. Pich, A. Biondi, A. Bernacchia, A. Falasca, C. Bovina, G. Formiggini, G. Parenti Castelli, and G. Lenaz Mitochondrial production of oxygen radical species and the role of Coenzyme Q as an antioxidant Exp. Biol. Med. (Maywood) 228 2003 506 513
26. M. Ghio, L. Ottonello, P. Contini, M. Amelotti, C. Mazzei, F. Indiveri, F. Puppo, and F. Dallegri Transforming growth factor-beta1 in supernatants from stored red blood cells inhibits neutrophil locomotion Blood 102 2003 1100 1107
27. M. Goto, M. Maruyama, K. Kitadate, R. Kirisawa, Y. Obata, M. Koiwa, and H. Iwai Detection of interleukin-1β in sera and colostrum of dairy cattle and in sera of neonates J. Vet. Sci. 59 1997 437 441
28. N.J. Goulding, H.S. Euzger, S.K. Butt, and M. Perretti Novel pathways for glucocorticoid effects on neutrophils in chronic inflammation Inflamm. Res. 47 Suppl. 3 1998 S158 S165
29. P.S. Grutkoski, C.T. Graeber, A. Ayala, and H.H. Simms Paracrine suppression of apoptosis by cytokine-stimulated neutrophils involves divergent regulation of NF-kappaB, Bcl-X(L), and Bak Shock 17 2002 47 54
30. A.J. Guidry, M.J. Paape, and R.E. Pearson Effects of parturition and lactation on blood and milk cell concentrations, corticosteroids, and neutrophil phagocytosis in the cow Am. J. Vet. Res. 37 1976 1195 1200
31. S.J. Heasman, K.M. Giles, C. Ward, A.G. Rossi, C. Haslett, and I. Dransfield Glucocorticoid-mediated regulation of granulocyte apoptosis and macrophage phagocytosis of apoptotic cells: implications for the resolution of inflammation J. Endocrinol. 178 2003 29 36
32. S. Henis-Korenblit, N.L. Strumpf, D. Goldstaub, and A. Kimchi A novel form of DAP5 protein accumulates in apoptotic cells as a result of caspase cleavage and internal ribosome entry site-mediated translation Mol. Cell. Biol. 20 2000 496 506
33. S. Henis-Korenblit, G. Shani, T. Sines, L. Marash, G. Shohat, and A. Kimchi The caspase-cleaved DAP5 protein supports internal ribosome entry site-mediated translation of death proteins Proc. Natl. Acad. Sci. U.S.A. 99 2002 5400 5405
34. A.W. Hill, A.L. Shears, and K.G. Hibbitt The pathogenesis of experimental Escherichia coli mastitis in newly calved dairy cows Res. Vet. Sci. 26 1979 97 101
35. M. Hoedemaker, L.A. Lund, P.G. Weston, and W.C. Wagner Influence of conditioned media from bovine cotyledon tissue cultures on function of bovine neutrophils Am. J. Vet. Res. 53 1992 1530 1533
36. M. Hoedemaker, L.A. Lund, and W.C. Wagner Function of neutrophils and chemoattractant properties of fetal placental tissue during the last month of pregnancy in cows Am. J. Vet. Res. 53 1992 1524 1529
37. S.M. Hollenberg, C. Weinberger, E.S. Ong, G. Cerelli, A. Oro, R. Lebo, E.B. Thompson, M.G. Rosenfeld, and R.M. Evan Primary structure and expression of a functional human glucocorticoid receptor cDNA Nature 318 1985 635 641
38. C.H.E. Homburg, and D. Roos Apoptosis of neutrophils Curr. Opin. Hematol. 3 1996 94 99
39. A.M. Hussain, and R.C.W. Daniel Bovine endometritis: current and future alternative therapy J. Vet. Med. Assoc. 38 1991 641 651
40. A.M. Hussain, and R.C.W. Daniel Phagocytosis by uterine fluid and blood neutrophils and haematological changes in postpartum cows following normal and abnormal parturition Theriogenology 37 1992 1253 1267
41. B. Jilma, P. Stohlawetz, T. Pernerstorfer, H.-G. Eichler, C. Müllner, and S. Kapiotis Glucocorticoids dose-dependently increase plasma levels of granulocyte colony stimulating factor in man J. Clin. Endocrinol. Metab. 83 1998 1037 1040
42. L.C.U. Junqueira, M. Zugaib, G.S. Montes, O.M.S. Toledo, R.M. Krisztán, and K.M. Shigihara Morpholic and histochemical evidence for the occurrence of collagenolysis and for the role of neutrophilic polymorphonuclear leukocytes during cervical dilation Am. J. Obstet. Gynecol. 138 1980 273 281
43. M.E. Kehrli Jr., and J.A. Harp Immunity in the mammary gland Vet. Clin. N. Am. Food Anim. Pract. 17 2001 495 516
44. R.W. Kelly Inflammatory mediators and parturition Rev. Reprod. 1 1996 89 96
45. R.W. Kelly, P. Illingworth, G. Baldie, R. Leask, S. Brouwer, and A.A. Calder Progesterone control of interleukin-8 production in endometrium and chorio-decidual cells underlies the role of the neutrophil in menstruation and parturition Hum. Reprod. 9 1994 253 258
46. M.K. Kerr, and G.A. Churchill Statistical design and the analysis of gene expression microarray data Genet. Res. 77 2001 123 128
47. M.K. Kerr, M. Martin, and G.A. Churchill Analysis of variance for gene expression microarray data J. Comput. Biol. 7 2000 819 837
48. K. Kimura, J.P. Goff, and M.E. Kehrli Jr. 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 1999 2385 2392
49. K. Kimura, J.P. Goff, M.E. Kehrli Jr., and T.A. Reinhardt Decreased neutrophil function as a cause of retained placenta in dairy cattle J. Dairy Sci. 85 2002 544 550
50. T. Kino, R.H. Stauber, J.H. Resau, G.N. Pavlakis, and G.P. Chrousos Pathologic human GR mutant has a transdominant negative effect on the wild-type GR by inhibiting its translocation into the nucleus: importance of the ligand-binding domain for intracellular GR trafficking J. Clin. Endocrinol. Metab. 86 2001 5600 5608
51. W. Klucinski, S.P. Targowski, E. Miernick-Degórska, and A. Winnicka The phagocytic activity of polymorphonuclear leukocytes isolated from normal uterus and that with experimentally induced inflammation in the cow J. Vet. Med. Assoc. 37 1990 506 512
52. M. La, A. Tailor, M. D'Amico, R.J. Flower, and M. Perretti Analysis of the protection afforded by annexin 1 in ischaemia-reperfusion injury: focus on neutrophil recruitment Eur. J. Pharmacol. 429 2001 263 278
53. T. Laakko, and P. Fraker Rapid changes in the lymphopoietic and granulopoietic compartments of the marrow caused by stress levels of corticosterone Immunology 105 2002 111 119
54. G. Li, S. Wang, and T.D. Gelehrter Identification of glucocorticoid receptor domains involved in transrepression of transforming growth factor-beta action J. Biol. Chem. 278 2003 41779 41788
55. -ΔΔCt method Methods 25 2001 402 408
56. L. Luo, T. Ibaragi, M. Nozawa, T. Kasahara, M. Sakai, Y. Sasaki, K. Tanebe, and S. Sait Interleukin-8 levels and granulocyte counts in cervical mucus during pregnancy Am. J. Reprod. Immunol. 43 2000 78 84
57. S.A. Madsen, P.S.D. Weber, and J.L. Burton Altered blood neutrophil gene expression in periparturient dairy cows Vet. Immunol. Immunopathol. 86 2002 159 175
58. S.A. Madsen, L.-C. Chang, M.-C. Hickey, G.J.M. Rosa, P.M. Coussens, and J.L. Burton Microarray analysis of gene expression in blood neutrophils of parturient cows Physiol. Genomics 16 2004 212 221
59. Madsen, S.A., Chang, L.-C., Hickey, M.-C., Coussens, P.M., Rosa, G.J.M., Burton, J.L., 2003a. Gene expression profiling and apoptosis phenotyping indicate that parturient steroids promote survival in bovine blood neutrophils. International Symposium on Animal Functional Genomics, Kellogg Center, Michigan State University, May 9-11, 2003 (abstract viewable at http://www/isafg.msu.edu) .
60. Madsen, S.A., Hickey, M.-C., Burton, J.L., 2003b. Glucocorticoids in parturient serum activate steroid receptors to modulate apoptosis in bovine blood neutrophils. AAVI On-line Newsletter (http://www.cvm.missouri.edu/aavi/ newsletter_3_04/newsletter_3_04.htm#StudentAwards).
61. N.A. Maianski, F.P.J. Mul, J.D. van Buul, D. Roos, and T.W. Kuijpers Granulocyte colony-stimulating factor inhibits the mitochondria-dependent activation of caspase-3 in neutrophils Blood 99 2002 672 679
62. N.A. Maianski, A.N. Maianski, T.W. Kuijpers, and D. Roos Apoptosis of neutrophils Acta Hematol. 111 2004 56 66
63. J.G. Maj, and M. Kankofer Activity of 72-kDa and 92-kDa matrix metalloproteinases in placental tissues of cows with and without retained fetal membranes Placenta 18 1997 683 687
64. T.W. Mak, and W.C. Yeh Signaling for survival and apoptosis in the immune system Arthritis Res. 4 Suppl. 3 2002 243 252
65. L. Mateus, L. Lopes da Costa, H. Carvalho, P. Serra, and R. Silva Blood and intrauterine leukocyte profile and function in dairy cows that spontaneously recovered from postpartum endometritis Reprod. Domest. Anim. 37 2002 176 180
66. F. Mackay, and C. Ambrose The TNF family members BAFF and APRIL: the growing complexity Cytokine Growth Factor Rev. 14 2003 311 324
67. G.R. McCarty, and B. Schwartz Reduced plasma cortisol binding to albumin in ocular hypertension and primary open-angle glaucoma Curr. Eye Res. 18 1999 467 476
68. E. Maymon, R. Romero, P. Pacora, R. Gomez, N. Athayde, S. Edwin, and B.H. Yoon Human neutrophil collagenase (matrix metalloproteinase 8) in parturition, premature rupture of the membranes, and intrauterine infection Am. J. Obstet. Gynecol. 183 2000 94 99
69. J. Mehrzad, H. Dosogne, E. Meyer, R. Heyneman, and C. Burvenich Respiratory burst activity of blood and milk neutrophils in dairy cows during different stages of lactation J. Dairy Res. 68 2001 399 415
70. J. Mehrzad, L. Duchateau, S. Pyörälä, and C. Burvenich Blood and milk neutrophil chemiluminescence and viability in primiparous and pluriparous dairy cows during late pregnancy, around parturition and early lactation J. Dairy Sci. 85 2002 3268 3276
71. D. Mirowska, W. Wicha, A. Czlonkowski, A. Czlonkowska, and F. Weber Increase of matrix metalloproteinase-9 in peripheral blood of multiple sclerosis patients treated with high doses of methylprednisolone J. Neuroimmunol. 146 2004 171 175
72. M. Moilanen, E. Pirila, R. Grenman, T. Sorsa, and T. Salo Expression and regulation of collagenase-2 (MMP-8) in head and neck squamous cell carcinomas J. Pathol. 197 2002 72 81
73. P.K. Narayanan, K. Ragheb, G. Lawler, and J.P. Robinson Defects in intracellular oxidative metabolism of neutrophils undergoing apoptosis J. Leukoc. Biol. 61 1997 481 488
74. P. Newburger, Y.V.B.K. Subrahmanyam, and S.M. Weissman Global analysis of neutrophil gene expression Curr. Opin. Hematol. 7 2000 16 20
75. R. Newton Molecular mechanisms of glucocorticoid action: what is important? Thorax 55 2000 603 613
76. G. Nunez, M.A. Benedict, Y. Hu, and N. Inohara Caspases: the proteases of the apoptotic pathway Oncogene 17 1998 3237 3245
77. I. Osman, A. Young, M.A. Ledingham, A.J. Thomson, F. Jordan, I.A. Greer, and J.E. Norman Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix, and myometrium before and during labour at term Mol. Hum. Reprod. 9 2003 41 45
78. R. Osmers, W. Rath, B.C. Adelmann-Grill, C. Fittkow, M. Kuloczik, M. Szeverényi, H. Tschesche, and W. Kuhn Origin of cervical collagenase during parturition Am. J. Obstet. Gynecol. 166 1992 1455 1460
79. C.A. Owen, Z. Hu, C. Lopez-Otin, and S.D. Shapiro Membrane-bound matrix metalloproteinase-8 on activated polymorphonuclear cells is a potent, tissue inhibitor of metalloproteinase-resistant collagenase and serpinase J. Immunol. 172 2004 7791 7803
80. M.T. Preisler, P.S.D. Weber, R.J. Tempelman, R.J. Erskine, H. Hunt, and J.L. Burton Glucocorticoid receptor down-regulation in neutrophils of periparturient cows Am. J. Vet. Res. 61 2000 14 19
81. J.A. Roth, and M.L. Kaeberle Effect of glucocorticoids on the bovine immune system J. Am. Vet. Med. Assoc. 180 1982 894 901
82. R. Sasson, and A. Amsterdam Pleiotropic anti-apoptotic activity of glucocorticoids in ovarian follicular cells Biochem. Pharmacol. 66 2003 1393 1401
83. J.S. Savill Apoptosis in resolution of inflammation J. Leukoc. Biol. 61 1997 375 380
84. F. Sendo, H. Tsuchida, Y. Takeda, S. Gon, H. Takei, T. Kato, O. Hachiya, and H. Watanabe Regulation of neutrophil apoptosis - its biological significance in inflammation and the immune response Hum. Cell 9 1996 215 222
85. V.B. Shidham, and V.K. Swami Evaluation of apoptotic leukocytes in peripheral blood smears Arch. Pathol. Lab. Med. 124 2000 1291 1294
86. D.E. Shuster, E.-K. Lee, and M.E. Kehrli Jr. Bacterial growth, inflammatory cytokine production, and neutrophil recruitment during coliform mastitis in cows within ten days after calving, compared with cows at midlactation Am. J. Vet. Res. 57 1996 1569 1575
87. J.A. Smith Neutrophils, host defense, and inflammation: a double-edged sword J. Leukoc. Biol. 56 1994 672 686
88. Y.V.B.K. Subrahmanyam, S. Yamaga, Y. Prashar, H.H. Lee, N.P. Hope, Y. Kluger, M. Gerstein, J.D. Goguen, P.E. Newburger, and S.M. Weissma RNA expression patterns change dramatically in human neutrophils exposed to bacteria Blood 97 2001 2457 2468
89. A. Szafarczyk, E. Feuvrier, P. Siaud, G. Rondouin, M. Lacoste, S. Gaillet, F. Malaval, and I. Assenmacher Removal of adrenal steroids from the medium reverses the stimulating effect of catecholamines on corticotropin- releasing hormone neurons in organotypic cultures Neuroendocrinology 61 1995 517 524
90. R.V. Talanian, X.H. Yang, J. Turbov, P. Seth, T. Ghayur, C.A. Casiano, K. Orth, and C.J. Froelich Granule-mediated killing: pathways for granzyme B-initiated apoptosis J. Exp. Med. 186 1997 1323 1331
91. K. Tanji-Matsuba, S.F. van Eeden, Y. Saito, M. Okazawa, M.E. Klut, S. Hayashi, and J.C. Hogg Functional changes in aging polymorphonuclear leukocytes Circulation 97 1998 91 98
92. R.J. Tempelman, P.M. Saama, A.E. Freeman, S.C. Kelm, A.L. Kuck, M.E. Kehrli Jr., and J.L. Burton Genetic variation in bovine neutrophil sensitivity to glucocorticoid challenge Acta Agric. Scand. 52 2002 189 202
93. A.J. Thomson, J.T. Telfer, A. Young, S. Campbell, C.J.R. Stewart, I.T. Cameron, I.A. Greer, and J.E. Norman Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process Hum. Reprod. 14 1999 229 236
94. J.A. Trapani, and V.R. Sutton Granzyme B: pro-apoptotic, antiviral and antitumor functions Curr. Opin. Immunol. 15 2003 533 543
95. A.M. Valencia, K.D. Beharry, J.G. Ang, K. Devarajan, R. Van Woerkom, M. Abrantes, K. Nishihara, E. Chang, J. Waltzman, and H.D. Modanlou Early postnatal dexamethasone influences matrix metalloproteinase-2 and -9, and their tissue inhibitors in the developing rat lung Pediatr. Pulmonol. 35 2003 456 462
96. K. Van Oostveldt, M.J. Paape, H. Dosogne, and C. Burvenich Effect of apoptosis on phagocytosis, respiratory burst and CD18 adhesion receptor expression of bovine neutrophils Domest. Anim. Endocrinol. 22 2002 37 50
97. K.V. Van Oostveldt, F. Vangroenweghe, H. Dosogne, and C. Burvenich Apoptosis and necrosis of blood and milk polymorphonuclear leukocytes in early and midlactating healthy cows Vet. Res. 32 2001 617 622
98. I. Vermes, C. Haanen, H. Steffens-Nakken, and C. Reutelingsperger A novel assay for apoptosis: flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V J. Immunol. Methods 184 1995 39 51
99. C. Wagner, C. Iking-Konert, B. Denefleh, S. Stegmaier, F. Hug, and G.M. Hansch Granzyme B and perforin: constitutive expression in human polymorphonuclear neutrophils Blood 103 2004 1099 1104
100. P.S.D. Weber, S.A. Madsen, G.W. Smith, J.J. Ireland, and J.L. Burton Pre-translational regulation of neutrophil CD62L in glucocorticoid-challenged cattle Vet. Immunol. Immunopathol. 83 2001 213 240
101. P.S.D. Weber, T. Toelboell, L.-C. Chang, J. Durrett Tirrell, P.M. Saama, G.W. Smith, and J.L. Burton Mechanisms of glucocorticoid-induced down regulation of neutrophil L-selectin: evidence for effects at the gene expression level and primarily on blood neutrophils J. Leukoc. Biol. 75 2004 815 827
102. M. Whyte, S. Renshaw, R. Lawson, and C. Bingle Apoptosis and the regulation of neutrophil lifespan Biochem. Soc. Trans. 27 1999 802 807
103. M.K.B. Whyte, L.C. Meagher, J. MacDermot, and C. Haslett Impairment of function in aging neutrophils J. Immunol. 150 1993 5124 5134
104. M. Winkler, D.-C. Fischer, P. Ruck, T. Marx, E. Kaiserling, A. Oberpichler, H. Tschesche, and W. Rath Parturition at term: parallel increases in interleukin-8 and proteinase concentrations and neutrophil count in the lower uterine segment Hum. Reprod. 14 1999 1096 1100
105. M. Winkler, A. Oberpichler, H. Tschesche, P. Ruck, D.-C. Fischer, and W. Rath Collagenolysis in the lower uterine segment during parturition at term: correlations with stage of cervical dilation and duration of labor Am. J. Obstet. Gynecol. 181 1999 153 158
106. M. Winkler, W. Rath, D.-C. Fischer, E. Van de Leur, and H.-D. Haubeck Regulation of interleukin-8 synthesis in human lower uterine segment fibroblasts by cytokines and growth factors Obstet. Gynecol. 95 2000 584 588
107. K.R.H. Winters, E. Meyer, V.M. Van Merris, W.L.M. Van Den Broeck, L. Duchayeau, and C. Burvenich Sex steroids do not influence the oxidative burst activity of polymorphonuclear leukocytes from ovariectomized cows in vitro Steroids 68 2003 397 406
108. R.D. Wolfinger, G. Gibson, E.D. Wolfinger, L. Bennett, H. Hamadeh, P. Bushel, C. Afshari, and R.S. Paules Assessing gene significance from cDNA microarray expression data via mixed models J. Comput. Biol. 8 2001 625 637
109. H. Wu, and J.R. Arron TRAF6, a molecular bridge spanning adaptive immunity, innate immunity and osteoimmunology Bioessays 25 2003 1096 1105
110. Y.H. Yang, S. Dudoit, P. Luu, D.M. Lin, V. Peng, J. Ngai, and T.P. Speed Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation Nucleic Acids Res. 40 2002 e15
111. H. Zerbe, N. Schneider, W. Leibold, T. Wensing, T.A.M. Kruip, and H.J. Schuberth Altered functional and immunophenotypical properties of neutrophilic granulocytes in postpartum cows associated with fatty liver Theriogenology 54 2000 771 786