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Role of endothelial cells in bovine mammary gland health and disease

Published online by Cambridge University Press:  25 August 2015

Valerie E. Ryman
Affiliation:
Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824, USA
Nandakumar Packiriswamy
Affiliation:
Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824, USA
Lorraine M. Sordillo*
Affiliation:
Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824, USA
*
* Corresponding author. E-mail: [email protected]

Abstract

The bovine mammary gland is a dynamic and complex organ composed of various cell types that work together for the purpose of milk synthesis and secretion. A layer of endothelial cells establishes the blood–milk barrier, which exists to facilitate the exchange of solutes and macromolecules necessary for optimal milk production. During bacterial challenge, however, endothelial cells divert some of their lactation function to protect the underlying tissue from damage by initiating inflammation. At the onset of inflammation, endothelial cells tightly regulate the movement of plasma components and leukocytes into affected tissue. Unfortunately, endothelial dysfunction as a result of exacerbated or sustained inflammation can negatively affect both barrier integrity and the health of surrounding extravascular tissue. The objective of this review is to highlight the role of endothelial cells in supporting milk production and regulating optimal inflammatory responses. The consequences of endothelial dysfunction and sustained inflammation on milk synthesis and secretion are discussed. Given the important role of endothelial cells in orchestrating the inflammatory response, a better understanding of endothelial function during mastitis may support development of targeted therapies to protect bovine mammary tissue and mammary endothelium.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2015 

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References

Abdul Awal, M, Matsumoto, M, Toyoshima, Y and Nishinakagawa, H (1996). Ultrastructural and morphometrical studies on the endothelial cells of arteries supplying the abdomino-inguinal mammary gland of rats during the reproductive cycle. Journal of Veterinary Medical Science 58: 2934.Google Scholar
Aitken, SL, Corl, CM and Sordillo, LM (2011a). Immunopathology of mastitis: insights into disease recognition and resolution. Journal of Mammary Gland Biology and Neoplasia 16: 291304.CrossRefGoogle ScholarPubMed
Aitken, SL, Corl, CM and Sordillo, LM (2011b). Pro-inflammatory and pro-apoptotic responses of TNF-alpha stimulated bovine mammary endothelial cells. Veterinary Immunology and Immunopathology 140: 282290.Google Scholar
Aleman, G, Lopez, A, Ordaz, G, Torres, N and Tovar, AR (2009). Changes in messenger RNA abundance of amino acid transporters in rat mammary gland during pregnancy, lactation, and weaning. Metabolism 58: 594601.Google Scholar
Anderson, KL, Kindahl, H, Smith, AR, Davis, LE and Gustafsson, BK (1986). Endotoxin-induced bovine mastitis: arachidonic acid metabolites in milk and plasma and effect of flunixin meglumine. American Journal of Veterinary Research 47: 13731377.Google Scholar
Andreotti, CS, Pereyra, EA, Baravalle, C, Renna, MS, Ortega, HH, Calvinho, LF and Dallard, BE (2014). Staphylococcus aureus chronic intramammary infection modifies protein expression of transforming growth factor beta (TGF-beta) subfamily components during active involution. Research in Veterinary Science 96: 514.CrossRefGoogle ScholarPubMed
Andres, AC and Djono, V (2010). The mammary gland vasculature revisited. Journal of Mammary Gland Biology and Neoplasia 15: 319328.CrossRefGoogle ScholarPubMed
Aon, MA, Stanley, BA, Sivakumaran, V, Kembro, JM, O'rourke, B, Paolocci, N and Cortassa, S (2012). Glutathione/thioredoxin systems modulate mitochondrial H2O2 emission: an experimental-computational study. Journal of General Physiology 139: 479491.CrossRefGoogle ScholarPubMed
Atroshi, F, Parantainen, J, Kangasniemi, R and Osterman, T (1987). Milk prostaglandins and electrical conductivity in bovine mastitis. Veterinary Research Communications 11: 1522.CrossRefGoogle ScholarPubMed
Baker, N, O'meara, SJ, Scannell, M, Maderna, P and Godson, C (2009). Lipoxin A4: anti-inflammatory and anti-angiogenic impact on endothelial cells. Journal of Immunology 182: 38193826.Google Scholar
Bannerman, DD, Sathyamoorthy, M and Goldblum, SE (1998). Bacterial lipopolysaccharide disrupts endothelial monolayer integrity and survival signaling events through caspase cleavage of adherens junction proteins. Journal of Biological Chemistry 273: 3537135380.Google Scholar
Bannerman, DD, Paape, MJ, Goff, JP, Kimura, K, Lippolis, JD and Hope, JC (2004a). Innate immune response to intramammary infection with Serratia marcescens and Streptococcus uberis. Veterinary Research 35: 681700.Google Scholar
Bannerman, DD, Paape, MJ, Lee, JW, Zhao, X, Hope, JC and Rainard, P (2004b). Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clinical and Diagnostic Laboratory Immunology 11: 463472.Google Scholar
Bazzoni, G and Dejana, E (2004). Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiological Reviews 84: 869901.Google Scholar
Bjornstedt, M, Xue, J, Huang, W, Akesson, B and Holmgren, A (1994). The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. Journal of Biological Chemistry 269: 2938229384.CrossRefGoogle ScholarPubMed
Blum, J and Fridovich, I (1985). Inactivation of glutathione peroxidase by superoxide radical. Archives of Biochemistry and Biophysics 240: 500508.Google Scholar
Blum, MS, Toninelli, E, Anderson, JM, Balda, MS, Zhou, J, O'donnell, L, Pardi, R and Bender, JR (1997). Cytoskeletal rearrangement mediates human microvascular endothelial tight junction modulation by cytokines. American Journal of Physiology 273: H286H294.Google Scholar
Bombeli, T, Karsan, A, Tait, JF and Harlan, JM (1997). Apoptotic vascular endothelial cells become procoagulant. Blood 89: 24292442.Google Scholar
Bombeli, T, Schwartz, BR and Harlan, JM (1999). Endothelial cells undergoing apoptosis become proadhesive for nonactivated platelets. Blood 93: 38313838.Google Scholar
Boutet, P, Bureau, F, Degand, G and Lekeux, P (2003). Imbalance between lipoxin A4 and leukotriene B4 in chronic mastitis-affected cows. Journal of Dairy Science 86: 34303439.Google Scholar
Bowler, RP, Nicks, M, Tran, K, Tanner, G, Chang, LY, Young, SK and Worthen, GS (2004). Extracellular superoxide dismutase attenuates lipopolysaccharide-induced neutrophilic inflammation. American Journal of Respiratory Cell and Molecular Biology 31: 432439.CrossRefGoogle ScholarPubMed
Breau, WC and Oliver, SP (1985). Accelerated bovine mammary involution induced by infusion of concanavalin A or phytohemagglutinin. American Journal of Veterinary Research 46: 816820.Google ScholarPubMed
Bucci, M, Roviezzo, F, Posadas, I, Yu, J, Parente, L, Sessa, WC, Ignarro, LJ and Cirino, G (2005). Endothelial nitric oxide synthase activation is critical for vascular leakage during acute inflammation in vivo . Proceedings of the National Academy of Sciences of the United States of America 102: 904908.Google Scholar
Busse, R and Mulsch, A (1990). Calcium-dependent nitric oxide synthesis in endothelial cytosol is mediated by calmodulin. FEBS Letters 265: 133136.CrossRefGoogle ScholarPubMed
Cao, YZ, Reddy, CC and Sordillo, LM (2000). Altered eicosanoid biosynthesis in selenium-deficient endothelial cells. Free Radical Biology and Medicine 28: 381389.CrossRefGoogle ScholarPubMed
Cassuto, J, Dou, H, Czikora, I, Szabo, A, Patel, VS, Kamath, V, Belin De Chantemele, E, Feher, A, Romero, MJ and Bagi, Z (2014). Peroxynitrite disrupts endothelial caveolae leading to eNOS uncoupling and diminished flow-mediated dilation in coronary arterioles of diabetic patients. Diabetes 63: 13811393.Google Scholar
Clesham, G, Parsaee, H, Joseph, S, Mcewan, JR and Macdermot, J (1992). Activation of bovine endothelial thromboxane receptors triggers release of prostacyclin but not EDRF. Cardiovascular Research 26: 513517.Google Scholar
Clough, G (1991). Relationship between microvascular permeability and ultrastructure. Progress in Biophysics and Molecular Biology 55: 4769.Google Scholar
Contreras, GA, Mattmiller, SA, Raphael, W, Gandy, JC and Sordillo, LM (2012a). Enhanced n-3 phospholipid content reduces inflammatory responses in bovine endothelial cells. Journal of Dairy Science 95: 71377150.Google Scholar
Contreras, GA, Raphael, W, Mattmiller, SA, Gandy, JC and Sordillo, LM (2012b). Nonesterified fatty acids modify inflammatory response and eicosanoid biosynthesis in bovine endothelial cells. Journal of Dairy Science 95: 50115023.Google Scholar
Conway, EM and Rosenberg, RD (1988). Tumor necrosis factor suppresses transcription of the thrombomodulin gene in endothelial cells. Molecular Cell Biology 8: 55885592.Google Scholar
Corl, CM, Gandy, JC and Sordillo, LM (2008). Platelet activating factor production and proinflammatory gene expression in endotoxin-challenged bovine mammary endothelial cells. Journal of Dairy Science 91: 30673078.Google Scholar
Corl, CM, Contreras, GA and Sordillo, LM (2010). Lipoxygenase metabolites modulate vascular-derived platelet activating factor production following endotoxin challenge. Veterinary Immunology and Immunopathology 136: 98107.Google Scholar
Cromack, DT, Porras-Reyes, B, Purdy, JA, Pierce, GF and Mustoe, TA (1993). Acceleration of tissue repair by transforming growth factor beta 1: identification of in vivo mechanism of action with radiotherapy-induced specific healing deficits. Surgery 113: 3642.Google ScholarPubMed
Crossman, DC, Carr, DP, Tuddenham, EG, Pearson, JD and Mcvey, JH (1990). The regulation of tissue factor mRNA in human endothelial cells in response to endotoxin or phorbol ester. Journal of Biological Chemistry 265: 97829787.Google Scholar
De Caterina, R, Cybulsky, MI, Clinton, SK, Gimbrone, MA Jr and Libby, P (1994). The omega-3 fatty acid docosahexaenoate reduces cytokine-induced expression of proatherogenic and proinflammatory proteins in human endothelial cells. Arteriosclerosis Thrombosis and Vascular Biology 14: 18291836.Google Scholar
De Martin, R, Vanhove, B, Cheng, Q, Hofer, E, Csizmadia, V, Winkler, H and Bach, FH (1993). Cytokine-inducible expression in endothelial cells of an I kappa B alpha-like gene is regulated by NF kappa B. EMBO Journal 12: 27732779.Google Scholar
Djonov, V, Andres, AC and Ziemiecki, A (2001). Vascular remodelling during the normal and malignant life cycle of the mammary gland. Microscopy Research and Technique 52: 182189.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Drake, WT, Lopes, NN, Fenton, JW II and Issekutz, AC (1992). Thrombin enhancement of interleukin-1 and tumor necrosis factor-alpha induced polymorphonuclear leukocyte migration. Laboratory Investigation 67: 617627.Google Scholar
Ereso, AQ, Cureton, EL, Cripps, MW, Sadjadi, J, Dua, MM, Curran, B and Victorino, GP (2009). Lipoxin a(4) attenuates microvascular fluid leak during inflammation. Journal of Surgical Research 156: 183188.Google Scholar
Fei, H, Berliner, JA, Parhami, F and Drake, TA (1993). Regulation of endothelial cell tissue factor expression by minimally oxidized LDL and lipopolysaccharide. Arteriosclerosis Thrombosis and Vascular Biology 13: 17111717.Google Scholar
Ferrari, G, Cook, BD, Terushkin, V, Pintucci, G and Mignatti, P (2009). Transforming growth factor-beta 1 (TGF-beta1) induces angiogenesis through vascular endothelial growth factor (VEGF)-mediated apoptosis. Journal of Cell Physiology 219: 449458.Google Scholar
Fitzpatrick, FA & Soberman, R (2001). Regulated formation of eicosanoids. Journal of Clinical Investigation 107: 13471351.Google Scholar
Fortes, GB, Alves, LS, De Oliveira, R, Dutra, FF, Rodrigues, D, Fernandez, PL, Souto-Padron, T, De Rosa, MJ, Kelliher, M, Golenbock, D, Chan, FK and Bozza, MT (2012). Heme induces programmed necrosis on macrophages through autocrine TNF and ROS production. Blood 119: 23682375.Google Scholar
Friedrichs, B, Toborek, M, Hennig, B, Heinevetter, L, Muller, C and Brigelius-Flohe, R (1999). 13-HPODE and 13-HODE modulate cytokine-induced expression of endothelial cell adhesion molecules differently. Biofactors 9: 6172.Google Scholar
Gamble, JR, Khew-Goodall, Y and Vadas, MA (1993). Transforming growth factor-beta inhibits E-selectin expression on human endothelial cells. Journal of Immunology 150: 44944503.Google Scholar
Goeckeler, ZM and Wysolmerski, RB (1995). Myosin light chain kinase-regulated endothelial cell contraction: the relationship between isometric tension, actin polymerization, and myosin phosphorylation. Journal of Cell Biology 130: 613627.Google Scholar
Haendeler, J, Tischler, V, Hoffmann, J, Zeiher, AM and Dimmeler, S (2004). Low doses of reactive oxygen species protect endothelial cells from apoptosis by increasing thioredoxin-1 expression. FEBS Letters 577: 427433.Google Scholar
Hafezi-Moghadam, A, Noda, K, Almulki, L, Iliaki, EF, Poulaki, V, Thomas, KL, Nakazawa, T, Hisatomi, T, Miller, JW and Gragoudas, ES (2007). VLA-4 blockade suppresses endotoxin-induced uveitis: in vivo evidence for functional integrin up-regulation. FASEB Journals 21: 464474.CrossRefGoogle ScholarPubMed
Haug, A, Hostmark, AT and Harstad, OM (2007). Bovine milk in human nutrition – a review. Lipids in Health and Disease 6: 25.Google Scholar
Holst, BD, Hurley, WL and Nelson, DR (1987). Involution of the bovine mammary gland: histological and ultrastructural changes. Journal of Dairy Science 70: 935944.Google Scholar
Hordijk, PL, Anthony, E, Mul, FP, Rientsma, R, Oomen, LC and Roos, D (1999). Vascular-endothelial-cadherin modulates endothelial monolayer permeability. Journal of Cell Science 112: 19151923.Google Scholar
Ignotz, RA and Massague, J (1986). Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. Journal of Biological Chemistry 261: 43374345.Google Scholar
Ismail, ZA and Dickinson, C (2010). Alterations in coagulation parameters in dairy cows affected with acute mastitis caused by E. coli and S. aureus pathogens. Veterinary Research Communications 34: 533539.CrossRefGoogle ScholarPubMed
Jasper, J and Weary, DM (2002). Effects of ad libitum milk intake on dairy calves. Journal of Dairy Science 85: 30543058.Google Scholar
Jiang, WG, Bryce, RP, Horrobin, DF and Mansel, RE (1998). Regulation of tight junction permeability and occludin expression by polyunsaturated fatty acids. Biochemical and Biophysical Research Communications 244: 414420.CrossRefGoogle ScholarPubMed
Kadl, A and Leitinger, N (2005). The role of endothelial cells in the resolution of acute inflammation. Antioxidants & Redox Signaling 7: 17441754.Google Scholar
Kaplanski, G, Farnarier, C, Tissot, O, Pierres, A, Benoliel, AM, Alessi, MC, Kaplanski, S and Bongrand, P (1993). Granulocyte-endothelium initial adhesion. Analysis of transient binding events mediated by E-selectin in a laminar shear flow. Biophysical Journal 64: 19221933.Google Scholar
Karlsson, A, Markfjall, M, Stromberg, N and Dahlgren, C (1995). Escherichia coli-induced activation of neutrophil NADPH-oxidase: lipopolysaccharide and formylated peptides act synergistically to induce release of reactive oxygen metabolites. Infection and Immunity 63: 46064612.Google Scholar
Knepler, JL Jr, Taher, LN, Gupta, MP, Patterson, C, Pavalko, F, Ober, MD and Hart, CM (2001). Peroxynitrite causes endothelial cell monolayer barrier dysfunction. American Journal of Physiology: Cell Physiology 281: C1064C1075.CrossRefGoogle ScholarPubMed
Kobayashi, M, Shimada, K and Ozawa, T (1990). Human recombinant interleukin-1 beta- and tumor necrosis factor alpha-mediated suppression of heparin-like compounds on cultured porcine aortic endothelial cells. Journal of Cell Physiology 144: 383390.Google ScholarPubMed
Kobayashi, K, Oyama, S, Numata, A, Rahman, MM and Kumura, H (2013). Lipopolysaccharide disrupts the milk-blood barrier by modulating claudins in mammary alveolar tight junctions. PLoS ONE 8: e62187.Google Scholar
Komatsu, T, Itoh, F, Kushibiki, S and Hodate, K (2005). Changes in gene expression of glucose transporters in lactating and nonlactating cows. Journal of Animal Science 83: 557564.Google Scholar
Lacasse, P, Farr, VC, Davis, SR and Prosser, CG (1996). Local secretion of nitric oxide and the control of mammary blood flow. Journal of Dairy Science 79: 13691374.Google Scholar
Levi, M, Van Der Poll, T, Ten Cate, H and Van Deventer, SJ (1997). The cytokine-mediated imbalance between coagulant and anticoagulant mechanisms in sepsis and endotoxaemia. European Journal of Clinical Investigation 27: 39.Google Scholar
Levick, JR and Smaje, LH (1987). An analysis of the permeability of a fenestra. Microvascular Research 33: 233256.Google Scholar
Levkau, B, Kenagy, RD, Karsan, A, Weitkamp, B, Clowes, AW, Ross, R and Raines, EW (2002). Activation of metalloproteinases and their association with integrins: an auxiliary apoptotic pathway in human endothelial cells. Cell Death & Differentiation 9: 13601367.Google Scholar
Ley, K, Bullard, DC, Arbones, ML, Bosse, R, Vestweber, D, Tedder, TF and Beaudet, AL (1995). Sequential contribution of L- and P-selectin to leukocyte rolling in vivo . Journal of Experimental Medicine 181: 669675.Google Scholar
Linzell, JL and Peaker, M (1972). Day-to-day variations in milk composition in the goat and cow as a guide to the detection of subclinical mastitis. British Veterinary Journal 128: 284295.Google Scholar
Lombardo, D, Fanni, T, Pluckthun, A and Dennis, EA (1986). Rate-determining step in phospholipase A2 mechanism. 18 O isotope exchange determined by 13C NMR. Journal of Biological Chemistry 261: 1166311666.Google Scholar
Lubos, E, Kelly, NJ, Oldebeken, SR, Leopold, JA, Zhang, YY, Loscalzo, J and Handy, DE (2011). Glutathione peroxidase-1 deficiency augments proinflammatory cytokine-induced redox signaling and human endothelial cell activation. Journal of Biological Chemistry 286: 3540735417.Google Scholar
Maddox, JF, Aherne, KM, Reddy, CC and Sordillo, LM (1999). Increased neutrophil adherence and adhesion molecule mRNA expression in endothelial cells during selenium deficiency. Journal of Leukocyte Biology 65: 658664.Google Scholar
Matsumoto, M, Nishinakagawa, H, Kurohmaru, M, Hayashi, Y and Otsuka, J (1992). Pregnancy and lactation affect the microvasculature of the mammary gland in mice. Journal of Veterinary Medical Science 54: 937943.Google Scholar
Matsumoto, M, Kurohmaru, M, Hayashi, Y, Nishinakagawa, H and Otsuka, J (1994). Permeability of mammary gland capillaries to ferritin in mice. Journal of Veterinary Medical Science 56: 6570.Google Scholar
Mattmiller, SA, Corl, CM, Gandy, JC, Loor, JJ and Sordillo, LM (2011). Glucose transporter and hypoxia-associated gene expression in the mammary gland of transition dairy cattle. Journal of Dairy Science 94: 29122922.CrossRefGoogle ScholarPubMed
Mavangira, V, Gandy, JC, Zhang, C, Ryman, VE, Jones, AD and Sordillo, LM (2015). Polyunsaturated fatty acids influence differential biosynthesis of oxylipids and other lipid mediators during bovine coliform mastitis. Journal of Dairy Science 98: 62026215.Google Scholar
Mayadas, TN, Johnson, RC, Rayburn, H, Hynes, RO and Wagner, DD (1993). Leukocyte rolling and extravasation are severely compromised in P selectin-deficient mice. Cell 74: 541554.Google Scholar
Mcever, RP, Beckstead, JH, Moore, KL, Marshall-Carlson, L and Bainton, DF (1989). GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel–Palade bodies. Journal of Clinical Investigation 84: 9299.Google Scholar
Michel, CC and Curry, FE (1999). Microvascular permeability. Physiological Review 79: 703761.Google Scholar
Muller, WA, Weigl, SA, Deng, X and Phillips, DM (1993). PECAM-1 is required for transendothelial migration of leukocytes. Journal of Experimental Medicine 178: 449460.Google Scholar
Murata, T, Ushikubi, F, Matsuoka, T, Hirata, M, Yamasaki, A, Sugimoto, Y, Ichikawa, A, Aze, Y, Tanaka, T, Yoshida, N, Ueno, A, Oh-Ishi, S and Narumiya, S (1997). Altered pain perception and inflammatory response in mice lacking prostacyclin receptor. Nature 388: 678682.Google Scholar
Nadjar, A, Tridon, V, May, MJ, Ghosh, S, Dantzer, R, Amedee, T and Parnet, P (2005). NFkappaB activates in vivo the synthesis of inducible Cox-2 in the brain. Journal of Cerebral Blood Flow & Metabolism 25: 10471059.Google Scholar
National Mastitis Council (2004). National Mastitis Council. Madison, WI.Google Scholar
Nawroth, PP and Stern, DM (1986). Modulation of endothelial cell hemostatic properties by tumor necrosis factor. Journal of Experimental Medicine 163: 740745.Google Scholar
Nielsen, MO, Fleet, IR, Jakobsen, K and Heap, RB (1995). The local differential effect of prostacyclin, prostaglandin E2 and prostaglandin F2 alpha on mammary blood flow of lactating goats. Journal of Endocrinology 145: 585591.Google Scholar
Nishida, K, Harrison, DG, Navas, JP, Fisher, AA, Dockery, SP, Uematsu, M, Nerem, RM, Alexander, RW and Murphy, TJ (1992). Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. Journal of Clinical Investigation 90: 20922096.Google Scholar
Nitta, T, Hata, M, Gotoh, S, Seo, Y, Sasaki, H, Hashimoto, N, Furuse, M and Tsukita, S (2003). Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. Journal of Cell Biology 161: 653660.Google Scholar
Niu, XF, Smith, CW and Kubes, P (1994). Intracellular oxidative stress induced by nitric oxide synthesis inhibition increases endothelial cell adhesion to neutrophils. Circulation Research 74: 11331140.Google Scholar
Ohashi, Y, Kawashima, S, Hirata, K, Yamashita, T, Ishida, T, Inoue, N, Sakoda, T, Kurihara, H, Yazaki, Y and Yokoyama, M (1998). Hypotension and reduced nitric oxide-elicited vasorelaxation in transgenic mice overexpressing endothelial nitric oxide synthase. Journal of Clinical Investigation 102: 20612071.Google Scholar
Olson, ST, Richard, B, Izaguirre, G, Schedin-Weiss, S and Gettins, PG (2010). Molecular mechanisms of antithrombin-heparin regulation of blood clotting proteinases. A paradigm for understanding proteinase regulation by serpin family protein proteinase inhibitors. Biochimie 92: 15871596.Google Scholar
Parnham, MJ, Bittner, C and Leyck, S (1987). Changes in glutathione peroxidase activities and the oxidative burst of leukocytes during inflammation in the mouse and rat. Free Radical Research Communications 4: 183188.Google Scholar
Pepper, MS, Baetens, D, Mandriota, SJ, Di Sanza, C, Oikemus, S, Lane, TF, Soriano, JV, Montesano, R and Iruela-Arispe, ML (2000). Regulation of VEGF and VEGF receptor expression in the rodent mammary gland during pregnancy, lactation, and involution. Developmental Dynamics 218: 507524.Google Scholar
Pezeshki, A, Stordeur, P, Wallemacq, H, Schynts, F, Stevens, M, Boutet, P, Peelman, LJ, De Spiegeleer, B, Duchateau, L, Bureau, F and Burvenich, C (2011). Variation of inflammatory dynamics and mediators in primiparous cows after intramammary challenge with Escherichia coli. Veterinary Research 42: 15.Google Scholar
Piotrowska-Tomala, KK, Siemieniuch, MJ, Szostek, AZ, Korzekwa, AJ, Woclawek-Potocka, I, Galvao, AM, Okuda, K and Skarzynski, DJ (2012). Lipopolysaccharides, cytokines, and nitric oxide affect secretion of prostaglandins and leukotrienes by bovine mammary gland epithelial cells. Domestic Animal Endocrinology 43: 278288.Google Scholar
Poutrel, B, Caffin, JP and Rainard, P (1983). Physiological and pathological factors influencing bovine serum albumin content of milk. Journal of Dairy Science 66: 535541.Google Scholar
Predescu, S, Knezevic, I, Bardita, C, Neamu, RF, Brovcovych, V and Predescu, D (2013). Platelet activating factor-induced ceramide micro-domains drive endothelial NOS activation and contribute to barrier dysfunction. PLoS ONE 8: e75846.Google Scholar
Prosser, CG, Davis, SR, Farr, VC and Lacasse, P (1996). Regulation of blood flow in the mammary microvasculature. Journal of Dairy Science 79: 11841197.Google Scholar
Quarrie, LH, Addey, CV and Wilde, CJ (1994). Local regulation of mammary apoptosis in the lactating goat. Biochemical Society Transactions 22: 178s.Google Scholar
Rabot, A, Sinowatz, F, Berisha, B, Meyer, HH and 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: 740748.Google Scholar
Rambeaud, M, Almeida, RA, Pighetti, GM and Oliver, SP (2003). Dynamics of leukocytes and cytokines during experimentally induced Streptococcus uberis mastitis. Veterinary Immunology and Immunopathology 96: 193205.Google Scholar
Ramirez, RA, Lee, A, Schedin, P, Russell, JS and Masso-Welch, PA (2012). Alterations in mast cell frequency and relationship to angiogenesis in the rat mammary gland during windows of physiologic tissue remodeling. Developmental Dynamics 241: 890900.CrossRefGoogle ScholarPubMed
Rao, LV and Rapaport, SI (1987). Studies of a mechanism inhibiting the initiation of the extrinsic pathway of coagulation. Blood 69: 645651.Google Scholar
Rippe, B, Kamiya, A and Folkow, B (1979). Transcapillary passage of albumin, effects of tissue cooling and of increases in filtration and plasma colloid osmotic pressure. Acta Physiologica Scandinavica 105: 171187.Google Scholar
Romer, LH, Mclean, NV, Yan, HC, Daise, M, Sun, J and Delisser, HM (1995). IFN-gamma and TNF-alpha induce redistribution of PECAM-1 (CD31) on human endothelial cells. Journal of Immunology 154: 65826592.Google Scholar
Rossiter, H, Barresi, C, Ghannadan, M, Gruber, F, Mildner, M, Fodinger, D and Tschachler, E (2007). Inactivation of VEGF in mammary gland epithelium severely compromises mammary gland development and function. FASEB Journal 21: 39944004.Google Scholar
Sans, M, Panes, J, Ardite, E, Elizalde, JI, Arce, Y, Elena, M, Palacin, A, Fernandez-Checa, JC, Anderson, DC, Lobb, R and Pique, JM (1999). VCAM-1 and ICAM-1 mediate leukocyte-endothelial cell adhesion in rat experimental colitis. Gastroenterology 116: 874883.Google Scholar
Scalia, R and Lefer, AM (1998). In vivo regulation of PECAM-1 activity during acute endothelial dysfunction in the rat mesenteric microvasculature. Journal of Leukocyte Biology 64: 163169.Google Scholar
Schenkel, AR, Mamdouh, Z, Chen, X, Liebman, RM and Muller, WA (2002). CD99 plays a major role in the migration of monocytes through endothelial junctions. Nature Immunology 3: 143150.Google Scholar
Schmitz, S, Pfaffl, MW, Meyer, HH and Bruckmaier, RM (2004). Short-term changes of mRNA expression of various inflammatory factors and milk proteins in mammary tissue during LPS-induced mastitis. Domestic Animal Endocrinology 26: 111126.Google Scholar
Scholz, D, Devaux, B, Hirche, A, Potzsch, B, Kropp, B, Schaper, W and Schaper, J (1996). Expression of adhesion molecules is specific and time-dependent in cytokine-stimulated endothelial cells in culture. Cell Tissue Research 284: 415423.Google Scholar
Serhan, CN, Gotlinger, K, Hong, S, Lu, Y, Siegelman, J, Baer, T, Yang, R, Colgan, SP and Petasis, NA (2006). Anti-inflammatory actions of neuroprotectin D1/protectin D1 and its natural stereoisomers: assignments of dihydroxy-containing docosatrienes. Journal of Immunology 176: 18481859.Google Scholar
Serhan, CN, Chiang, N and Van Dyke, TE (2008a). Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nature Reviews Immunology 8: 349361.Google Scholar
Serhan, CN, Yacoubian, S and Yang, R (2008b). Anti-inflammatory and pro-resolving lipid mediators. Annual Review of Pathology 3: 279.Google Scholar
Shao, Y, Wellman, TL, Lounsbury, KM and Zhao, FQ (2014). Differential regulation of GLUT1 and GLUT8 expression by hypoxia in mammary epithelial cells. American Journal of Physiology: Regulatory Integrative and Comparative Physiology 307: R237R247.Google Scholar
Shuster, DE, Kehrli, ME Jr, Rainard, P and Paape, M (1997). Complement fragment C5a and inflammatory cytokines in neutrophil recruitment during intramammary infection with Escherichia coli. Infection & Immunity 65: 32863292.Google Scholar
Sordillo, LM, Weaver, JA, Cao, YZ, Corl, C, Sylte, MJ and Mullarky, IK (2005). Enhanced 15-HPETE production during oxidant stress induces apoptosis of endothelial cells. Prostaglandins and other Lipid Mediators 76: 1934.Google Scholar
Sordillo, LM, Streicher, KL, Mullarky, IK, Gandy, JC, Trigona, W and Corl, CM (2008). Selenium inhibits 15-hydroperoxyoctadecadienoic acid-induced intracellular adhesion molecule expression in aortic endothelial cells. Free Radicals Biology & Medicine 44: 3443.Google Scholar
Sordillo, LM, Contreras, GA and Aitken, SL (2009). Metabolic factors affecting the inflammatory response of periparturient dairy cows. Animal Health Research Reviews 10: 5363.CrossRefGoogle ScholarPubMed
Spector, AA (1975). Fatty acid binding to plasma albumin. Journal of Lipid Research 16: 165179.Google Scholar
Stirling, JW and Chandler, JA (1976). The fine structure of the normal, resting terminal ductal-lobular unit of the female breast. Virchows Archives A: Pathology Anatomy & Histology 372: 205226.Google Scholar
Swanson, EW (1965). Comparing continuous milking with sixty-day dry periods in successive lactations. Journal of Dairy Science 48: 12051209.Google Scholar
Tatarczuch, L, Philip, C and Lee, CS (1997). Involution of the sheep mammary gland. Journal of Anatomy 190: 405416.Google Scholar
Thomas, LH, Haider, W, Hill, AW and Cook, RS (1994). Pathologic findings of experimentally induced Streptococcus uberis infection in the mammary gland of cows. American Journal of Veterinary Research 55: 17231728.Google Scholar
Thompson, RD, Noble, KE, Larbi, KY, Dewar, A, Duncan, GS, Mak, TW and Nourshargh, S (2001). Platelet-endothelial cell adhesion molecule-1 (PECAM-1)-deficient mice demonstrate a transient and cytokine-specific role for PECAM-1 in leukocyte migration through the perivascular basement membrane. Blood 97: 18541860.Google Scholar
Trigona, WL, Mullarky, IK, Cao, Y and Sordillo, LM (2006). Thioredoxin reductase regulates the induction of haem oxygenase-1 expression in aortic endothelial cells. Biochemical Journal 394: 207216.Google Scholar
Van Nieuw Amerongen, GP and Van Hinsbergh, VW (2002). Targets for pharmacological intervention of endothelial hyperpermeability and barrier function. Vascular Pharmacology 39: 257272.Google Scholar
Vasquez-Vivar, J, Kalyanaraman, B, Martasek, P, Hogg, N, Masters, BS, Karoui, H, Tordo, P and Pritchard, KA Jr (1998). Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proceedings of the National Academy of Sciences of the United States of America 95: 92209225.CrossRefGoogle ScholarPubMed
Walker, NI, Bennett, RE and Kerr, JF (1989). Cell death by apoptosis during involution of the lactating breast in mice and rats. American Journal of Anatomy 185: 1932.CrossRefGoogle ScholarPubMed
Weaver, JA, Maddox, JF, Cao, YZ, Mullarky, IK and Sordillo, LM (2001). Increased 15-HPETE production decreases prostacyclin synthase activity during oxidant stress in aortic endothelial cells. Free Radical Biology & Medicine 30: 299308.Google Scholar
Weiss, N, Zhang, YY, Heydrick, S, Bierl, C and Loscalzo, J (2001). Overexpression of cellular glutathione peroxidase rescues homocyst(e)ine-induced endothelial dysfunction. Proceedings of the National Academy of Sciences of the United States of America 98: 1250312508.Google Scholar
Wilde, CJ, Addey, CV, Li, P and Fernig, DG (1997). Programmed cell death in bovine mammary tissue during lactation and involution. Experimental Physiology 82: 943953.Google Scholar
Winn, RK and Harlan, JM (2005). The role of endothelial cell apoptosis in inflammatory and immune diseases. Journal of Thrombosis and Haemostasis 3: 18151824.Google Scholar
Wrighton, CJ, Hofer-Warbinek, R, Moll, T, Eytner, R, Bach, FH and De Martin, R (1996). Inhibition of endothelial cell activation by adenovirus-mediated expression of I kappa B alpha, an inhibitor of the transcription factor NF-kappa B. Journal of Experimental Medicine 183: 10131022.Google Scholar
Xia, Y, Tsai, AL, Berka, V and Zweier, JL (1998). Superoxide generation from endothelial nitric-oxide synthase. A Ca2+/calmodulin-dependent and tetrahydrobiopterin regulatory process. Journal of Biological Chemistry 273: 2580425808.Google Scholar
Yasugi, T, Kaido, T and Uehara, Y (1989). Changes in density and architecture of microvessels of the rat mammary gland during pregnancy and lactation. Archives of Histology and Cytology 52: 115122.Google Scholar
Zhang, W, Zheng, S, Storz, P and Min, W (2005). Protein kinase D specifically mediates apoptosis signal-regulating kinase 1-JNK signaling induced by H2O2 but not tumor necrosis factor. Journal of Biological Chemistry 280: 1903619044.Google Scholar
Zhang, X, Wang, T, Gui, P, Yao, C, Sun, W, Wang, L, Wang, H, Xie, W, Yao, S, Lin, Y and Wu, Q (2013). Resolvin D1 reverts lipopolysaccharide-induced TJ proteins disruption and the increase of cellular permeability by regulating IkappaBalpha signaling in human vascular endothelial cells. Oxidative Medicine and Cellular Longevity 2013: 185715.Google Scholar
Zhao, FQ and Keating, AF (2007). Expression and regulation of glucose transporters in the bovine mammary gland. Journal of Dairy Science 90 (suppl. 1): E76E86.Google Scholar
Zia, S, Giri, SN, Cullor, J, Emau, P, Osburn, BI and Bushnell, RB (1987). Role of eicosanoids, histamine, and serotonin in the pathogenesis of Klebsiella pneumoniae-induced bovine mastitis. American Journal of Veterinary Research 48: 16171625.Google Scholar
Zweier, JL, Broderick, R, Kuppusamy, P, Thompson-Gorman, S and Lutty, GA (1994). Determination of the mechanism of free radical generation in human aortic endothelial cells exposed to anoxia and reoxygenation. Journal of Biological Chemistry 269: 2415624162.Google Scholar