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TNFα-mediated plasminogen activation on neutrophils is involved in the high plasmin activity in mammary secretion of drying-off cows

Published online by Cambridge University Press:  29 July 2009

Wen K Chou ,
Ting C Yu ,
Shuen E Chen ,
Ho C Peh ,
Wen B Liu ,
Ming T Chen ,
Hajime Nagahata  and
Chai J Chang
Wen K Chou
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan ROC
Ting C Yu
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan ROC
Shuen E Chen
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan ROC
Ho C Peh
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan ROC
Wen B Liu
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan ROC
Ming T Chen
Affiliation:
Department of Bioindustry Technology, Da Yeh University, Chung Hwa 555, Taiwan ROC
Hajime Nagahata
Affiliation:
Department of Animal Health, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Hokkaido 069-8501, Japan
Chai J Chang*
Affiliation:
Department of Animal Science, National Chung Hsing University, Taichung 402, Taiwan ROC
*
*For correspondence; e-mail: [email protected]
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Abstract

Interactions between inflammatory cytokines and plasminogen (Pg) activation system on immune cells are yet to be established. In previous studies we reported a somatic cell-associated elevation of proteolytic activity in mammary secretion of drying-off goats and cows. The purposes of the present study were to examine the role of TNF-α in polymorphonuclear neutrophil (PMN)-associated Pg activation, and the significance of this activation pathway for overall plasmin (Pm) activity in mammary secretion of drying-off cows. Results of experiments in vitro showed that the spontaneous Pg activation observed on fresh preparations of bovine blood PMN was completely blocked by anti bovine TNF-α antibody, and was further up-regulated by exogenous bovine TNF-α. Monitoring the parameters of mammary secretion of drying-off cows revealed that both somatic cell counts and differential PMN ratio was significantly elevated at weeks 1, 2 and 3 of milk stasis. Nevertheless, specific activity of soluble Pm in mammary secretion increased and the level of 17-kDa TNF-α decreased immediately following milk stasis. Iimmunoblotting revealed that although both 26-kDa pro-TNF-α and 17-kDa TNF-α were consistently present in somatic cells of mammary secretion collected at weeks 0, 1, 2 and 3 of milk stasis, only 26-kDa pro-TNF-α was present in somatic cells of milk during lactation. In-vitro assay indicated that cell-free mammary secretion of drying-off cows exerted no Pg activation bioactivity towards bovine blood PMN. Altogether, the current study suggests the existence of an active TNF-α-Pg-Pm autocrine/paracrine loop on the massively infiltrated PMN inside udders of drying-off cows, which involves extensive binding and internalization of 17-kDa TNF-α on PMN and consequently activation of Pg, resulting in high Pm activity and low 17-kDa TNF-α level in mammary secretion. These coordinated mechanisms may play a role in the defence of drying-off mammary gland.

Keywords

Plasminogen activationTNF-αPMNmammary secretiondry cows
Type
Research Article
Information
Journal of Dairy Research , Volume 76 , Issue 4 , November 2009 , pp. 459 - 468
Copyright
Copyright © Proprietors of Journal of Dairy Research 2009

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References

Athie, F, Bachman, KC, Head, HH, Hayen, MJ & Wilcox, CJ 1997 Milk plasmin during bovine mammary involution that has been accelerated by estrogen. Journal of Dairy Science 80 1561–1568CrossRefGoogle ScholarPubMed
Andronicos, NM & Ranson, M 2001 The topology of plasminogen binding and activation on the surface of human breast cancer cells. British Journal of Cancer 85 909–916CrossRefGoogle ScholarPubMed
Annen, EL, Collier, RJ, McGuire, MA & Vicini, JL 2004 Effects of dry period length on milk yield and mammary epithelial cells. Journal of Dairy Science 87 E66–E76CrossRefGoogle Scholar
Andreasen, PA, Kjoller, L, Christensen, L & Duffy, MJ 1997 The urokinase-type plasminogen activator system in cancer metastasis: a review. International Journal of Cancer 72 1–223.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Blasi, F 1997 uPA, uPAR, PAI-1: key intersection of proteolytic adhesive and chemotactic highways? Immunology Today 18 415–417CrossRefGoogle ScholarPubMed
Blasi, F & Carmeliet, P 2002 uPAR: a versatile signaling orchestrator. National Review of Molecular Cell Biology 3 932–943CrossRefGoogle ScholarPubMed
Bradford, MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 248–254CrossRefGoogle ScholarPubMed
Burvenich, C & Van Merris, V 2003 Severity of E. Coli mastitis is mainly determined by cow factors. Veterinary Research 34 521–564CrossRefGoogle ScholarPubMed
Capuco, AV, Akers, RM & Smith, JJ 1997 Mammary growth in Holstein cows during the dry period: Quantification of nucleic acids and histology. Journal of Dairy Science 80 477–487CrossRefGoogle ScholarPubMed
Chen, WY, Weng, MH, Chen, SE, Peh, HC, Liu, WB, Yu, TC, Huang, MC, Chen, MT, Nagahata, H & Chang, CJ 2007 Profile of gelatinolytic capacity in raw goat milk and the implication for milk quality. Journal of Dairy Science 90 4954–4965CrossRefGoogle ScholarPubMed
Gong, Y, Kim, S, Felez, J, Grella, DK, Castellino, FJ & Miles, LA 2001 Conversion of Glu-plasminogen to Lys-plasminogen is necessary for optimal stimulation of plasminogen activation on the endothelial cell surface. Journal of Biological Chemistry 276 19078–19083CrossRefGoogle ScholarPubMed
Grummer, RR & Rastani, RR 2004 Why re-evaluate dry period length? Journal of Dairy Science 87 E77–E85CrossRefGoogle Scholar
Horrevoets, AJG, Smilde, AE, Fredenburgh, JC, Pannekock, H & Nesheim, ME 1995 The activation-resistant conformation of recombinant human plasminogen is stabilized by basic residues in the amino-terminal hinge region. Journal of Biological Chemistry 270 15770–15776CrossRefGoogle ScholarPubMed
Lee, CS, Wooding, FB & Kemp, P 1980 Identification, properties, and differential counts of cell populations using electron microscopy of dry cow secretion, colostrums and milk from normal cows. Journal of Dairy Research 47 39–50CrossRefGoogle ScholarPubMed
Le Roux, Y, Laurent, F & Moussaoui, F 2003 Polymorphonuclear proteolytic activity and milk composition change. Veterinary Research 34 629–645CrossRefGoogle ScholarPubMed
Levi, M, van der Poll, T & Buller, HR 2004 Bidirectional relation between inflammation and coagulation. Circulation 109 2698–2704CrossRefGoogle ScholarPubMed
Mehrzad, J, Dosogne, H, Meyer, E, Heyneman, R & Burvenich, C 2001 Respiratory burst activity of blood and milk neutrohils in dairy cows during different stages of lactation. Journal of Dairy Research 68 399–415CrossRefGoogle Scholar
Mehrzad, J, Desrosiers, C, Lauzon, K, Robitaille, G, Zhao, X & Lacasse, P 2005 Proteases involved in mammary tissue damage during endotoxin-induced mastitis in dairy cows. Journal of DairyScience 88 211–222CrossRefGoogle ScholarPubMed
Moller, LB 1993 Structure and function of the urokinase receptor. Blood Coaguation and Fibrinolysis 4 293–303CrossRefGoogle ScholarPubMed
Murray, RZ, Kay, JG, Sangermani, DG & Stow, JL 2005 A role for the phasosome in cytokine secretion. Science 310 1492–1495CrossRefGoogle ScholarPubMed
Pezeshki, A, Mehrzad, J, Ghorbani, GR, Rahman, HR, Collier, RJ & Burvenich, C 2007 Effects of short dary periods on performance and metabolic status in Holstein dairy cows. Journal of Dairy Science 90 5531–5541CrossRefGoogle Scholar
Plesner, T, Behrendt, N & Ploug, M 1997 Structure, function and expression on blood and bone marrow cells of the urokinase-type plasminogen activator receptor, uPAR. Stem Cell 15 398–408CrossRefGoogle ScholarPubMed
Rabot, A, Sinowatz, F, Berisha, B, Meyer, HHD & Schams, D 2007 Expression and localization of extracellular matrix-degrading proteinases and their inhibitors in the bovine mammary gland during development, function, and involution. Journal of Dairy Science 90 740–748CrossRefGoogle ScholarPubMed
Rhee, JS, Santoso, S & Herrmann, M 2003 New aspects of integrin-mediated leukocyte adhesion in inflammation: regulation by haemostatic factors and bacterial products. Current Molecular Medicine 3 387–392CrossRefGoogle ScholarPubMed
Riollet, C, Rainard, P & Poutrel, B 2001 Cell subpopulations and cytokine expression in cow milk in response to chronic Staphylococcus aureus infection. Journal of Dairy Science 84 1077–1084CrossRefGoogle ScholarPubMed
Pluskota, E, Soloviev, DA, Bdeir, K, Cines, DB & Plow, EF 2004 Integrin αMβ2 orchestrates and accelerates plasminogen activation and fibrinolysis by neutrophils. Journal of Biological Chemistry 279 18063–18072CrossRefGoogle ScholarPubMed
Prager, GW, Breuss, JM, Steurer, S, Mihaly, J & Binder, BR 2004 Vascular endothelial growth factor (VEGF) induces rapid prourokinase (pro-uPA) activation on the surface of endothelial cells. Blood 103 955–962CrossRefGoogle ScholarPubMed
SAS Institute 2003 SAS/STAT User's Guide. Release 6.12. SAS Institute Inc.; Cary NC, USAGoogle Scholar
Shurety, W, Merino-Trigo, A, Brown, D, Hume, DA & Stow, JL 2000 Localization and post-Golgi trafficking of tumor necrosis factor-alphs in macrophages. Journal of Interferon and Cytokine Research 20 427–438CrossRefGoogle ScholarPubMed
Smiley, ST, King, JA & Hancock, WW 2001 Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. Journal of Immunology 167 2887–2894CrossRefGoogle ScholarPubMed
Solomon, KA, Pesti, N, Wu, G & Newton, RC 1999 Cutting edge: a dominant negative form of TNF-alpha converting enzyme inhibits proTNF and TNFRII secretion. Journal of Immunology 163 4105–4108CrossRefGoogle Scholar
Stillfried, GE, Saunders, DN & Ranson, M 2007 Plasminogen binding and activation at the breast cancer cell surface: the integral role of urokinase activity. Breast Cancer Research 9 14–24CrossRefGoogle ScholarPubMed
Syrovets, T, Jendrach, M, Rohwedder, A, Schule, A & Simmet, T 2001 Plasmin-induced expression of cytokines and tissue factor in human monocytes involves AP-1 and IKK beta-mediated NF-kappa B activation. Blood 97 3941–3950CrossRefGoogle Scholar
Szaba, FM & Smiley, ST 2002 Roles for thrombin and fibrin(ogen) in cytokine/chemokine production and macrophage adhesion in vivo. Blood 99 1053–1059CrossRefGoogle ScholarPubMed
Tian, SZ, Chang, CJ, Chiang, CC, Peh, HC, Huang, MC, Lee, JW & Zhao, X 2005 Comparison of morphology, viability and function between blood and milk neutrophils from peak lactating goats. Canadian Journal of Veterinary Research 69 39–45Google ScholarPubMed
Vandeputte-Van Mesom, G, Burvenich, C, Roets, E, Massart-Leen, AM, Heyneman, R, Kremer, WD & Brand, A 1993 Classification of newly calved cows into moderate and severe responders to experimentally induced Escherichia coli mastitis. Journal of Dairy Research 60 19–29CrossRefGoogle Scholar
van Ijzendoorn, SC 2006 Recycling endosomes. Journal of Cell Science 119 1679–1681CrossRefGoogle ScholarPubMed
Vassalli, P 1996 The tumor necrosis factor ligand and receptor families. New England Journal of Medicine 334 1717–1725Google Scholar
Wedlock, DN, McCarthy, AR, Doolin, EE, Lacy-Hulbert, SJ, Woolford, MW & Buddle, BM 2004 Effect of recombinant cytokines on leucocytes and physiological changes in bovine mammary glands during early involution. Journal of Dairy Research 71 154–161CrossRefGoogle ScholarPubMed
Weng, MH, Chang, CJ, Chen, WY, Chou, WK, Peh, HC, Huang, MC, Chen, MT & Nagahata, H 2006 Contribution of somatic cell-associated activation of plasminogen to caseinolysis within the goat mammary gland. Journal of Dairy Science 89 2025–2037CrossRefGoogle ScholarPubMed
Weng, MH, Yu, TC, Chen, SE, Peh, HC, Liu, WB, Chen, MT, Nagahata, H & Chang, CJ 2008 Regional accretion of gelatinase B in mammary gland during gradual and acute involution of dairy animals. Journal of Dairy Research 75 202–210CrossRefGoogle ScholarPubMed
Yang, WL, Godwin, AK & Xu, XX 2004 Tumor necrosis factor-α-induced matrix proteolytic enzyme production and basement membrane remodeling by human ovarian surface epithelial cells: molecular basis linking ovulation and cancer risk. Cancer Research 64 1534–1540CrossRefGoogle ScholarPubMed