Comparative View of Lung Vascular Endothelium of Cattle, Horses, and Water Buffalo

Part of the Advances in Anatomy, Embryology and Cell Biology book series (ADVSANAT, volume 228)


Endothelium plays an important role in maintaining the vascular barrier and physiological homeostasis. Endothelium also is fundamental to the initiation and regulation of inflammation. Endothelium demonstrates phenotypic and functional heterogeneity not only among various organs but also within an organ. One of the striking examples would be the pulmonary endothelium that participates in creating blood–air barrier. Endothelium in large pulmonary blood vessels is distinct in structure and function from that lining of the pulmonary capillaries. This chapter focuses on the comparative aspects of pulmonary endothelium and highlight unique differences such as the presence of pulmonary intravascular macrophages among select species.


  1. Abdi K, Kobzik L, Li X, Mentzer SJ (1995) Expression of membrane glycoconjugates on sheep lung endothelium. Lab Invest 72(4):445–452PubMedGoogle Scholar
  2. Aderem A (2001) Role of Toll-like receptors in inflammatory response in macrophages. Crit Care Med 29(7 Suppl):S16–S18PubMedCrossRefGoogle Scholar
  3. Aharonson-Raz K, Lohmann KL, Townsend HG, Marques F, Singh B (2012) Pulmonary intravascular macrophages as proinflammatory cells in heaves, an asthma-like equine disease. Am J Physiol Lung Cell Mol Physiol 303(3):L189–L198. PubMedCrossRefGoogle Scholar
  4. Alvarez DF, King JA, Weber D, Addison E, Liedtke W, Townsley MI (2006) Transient receptor potential vanilloid 4-mediated disruption of the alveolar septal barrier: a novel mechanism of acute lung injury. Circ Res 99(9):988–995. PubMedPubMedCentralCrossRefGoogle Scholar
  5. Andonegui G, Goyert SM, Kubes P (2002) Lipopolysaccharide-induced leukocyte-endothelial cell interactions: a role for CD14 versus toll-like receptor 4 within microvessels. J Immunol 169(4):2111–2119PubMedCrossRefGoogle Scholar
  6. Andonegui G, Bonder CS, Green F, Mullaly SC, Zbytnuik L, Raharjo E, Kubes P (2003) Endothelium-derived Toll-like receptor-4 is the key molecule in LPS-induced neutrophil sequestration into lungs. J Clin Invest 111(7):1011–1020. PubMedPubMedCentralCrossRefGoogle Scholar
  7. Atwal OS, Saldanha KA (1985) Erythrophagocytosis in alveolar capillaries of goat lung: ultrastructural properties of blood monocytes. Acta Anat (Basel) 124(3-4):245–254CrossRefGoogle Scholar
  8. Atwal OS, Singh B, Staempfli H, Minhas K (1992) Presence of pulmonary intravascular macrophages in the equine lung: some structuro-functional properties. Anat Rec 234(4):530–540. PubMedCrossRefGoogle Scholar
  9. Balachandran Y, Knaus S, Caldwell S, Singh B (2015) Toll-like receptor 10 expression in chicken, cattle, pig, dog, and rat lungs. Vet Immunol Immunopathol 168(3-4):184–192. PubMedCrossRefGoogle Scholar
  10. Bauer S, Wagner H (2002) Bacterial CpG-DNA licenses TLR9. Curr Top Microbiol Immunol 270:145–154PubMedGoogle Scholar
  11. Birch KA, Pober JS, Zavoico GB, Means AR, Ewenstein BM (1992) Calcium/calmodulin transduces thrombin-stimulated secretion: studies in intact and minimally permeabilized human umbilical vein endothelial cells. J Cell Biol 118(6):1501–1510PubMedCrossRefGoogle Scholar
  12. Birch KA, Ewenstein BM, Golan DE, Pober JS (1994) Prolonged peak elevations in cytoplasmic free calcium ions, derived from intracellular stores, correlate with the extent of thrombin-stimulated exocytosis in single human umbilical vein endothelial cells. J Cell Physiol 160(3):545–554. PubMedCrossRefGoogle Scholar
  13. Birks EK, Mathieu-Costello O, Fu Z, Tyler WS, West JB (1994) Comparative aspects of the strength of pulmonary capillaries in rabbit, dog, and horse. Respir Physiol 97(2):235–246PubMedCrossRefGoogle Scholar
  14. Birks EK, Mathieu-Costello O, Fu Z, Tyler WS, West JB (1997) Very high pressures are required to cause stress failure of pulmonary capillaries in thoroughbred racehorses. J Appl Physiol (1985) 82(5):1584–1592CrossRefGoogle Scholar
  15. Bochsler PN, Slauson DO, Chandler SK, Suyemoto MM (1989) Isolation and characterization of equine microvascular endothelial cells in vitro. Am J Vet Res 50(10):1800–1805PubMedGoogle Scholar
  16. Bonfanti R, Furie BC, Furie B, Wagner DD (1989) PADGEM (GMP140) is a component of Weibel-Palade bodies of human endothelial cells. Blood 73(5):1109–1112PubMedGoogle Scholar
  17. Chuang T, Ulevitch RJ (2001) Identification of hTLR10: a novel human Toll-like receptor preferentially expressed in immune cells. Biochim Biophys Acta 1518(1-2):157–161PubMedCrossRefGoogle Scholar
  18. Chung-Welch N, Shepro D, Dunham B, Hechtman HB (1988) Prostacyclin and prostaglandin E2 secretions by bovine pulmonary microvessel endothelial cells are altered by changes in culture conditions. J Cell Physiol 135(2):224–234. PubMedCrossRefGoogle Scholar
  19. Cioffi DL, Moore TM, Schaack J, Creighton JR, Cooper DM, Stevens T (2002) Dominant regulation of interendothelial cell gap formation by calcium-inhibited type 6 adenylyl cyclase. J Cell Biol 157(7):1267–1278. PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cioffi DL, Lowe K, Alvarez DF, Barry C, Stevens T (2009) TRPing on the lung endothelium: calcium channels that regulate barrier function. Antioxid Redox Signal 11(4):765–776. PubMedPubMedCentralCrossRefGoogle Scholar
  21. Costello ML, Mathieu-Costello O, West JB (1992) Stress failure of alveolar epithelial cells studied by scanning electron microscopy. Am Rev Respir Dis 145(6):1446–1455. PubMedCrossRefGoogle Scholar
  22. Cotran RS (1989) Endothelial cells. Textbook of rheumatology, 3rd edn. WB Saunders, Philadelphila, PAGoogle Scholar
  23. Crapo JD, Barry BE, Gehr P, Bachofen M, Weibel ER (1982) Cell number and cell characteristics of the normal human lung. Am Rev Respir Dis 126(2):332–337. PubMedGoogle Scholar
  24. Crapo JD, Young SL, Fram EK, Pinkerton KE, Barry BE, Crapo RO (1983) Morphometric characteristics of cells in the alveolar region of mammalian lungs. Am Rev Respir Dis 128(2 Pt 2):S42–S46. PubMedGoogle Scholar
  25. Demiryurek AT, Wadsworth RM, Kane KA (1991) Effects of hypoxia on isolated intrapulmonary arteries from the sheep. Pulm Pharmacol 4(3):158–164PubMedCrossRefGoogle Scholar
  26. Demiryurek AT, Wadsworth RM, Kane KA, Peacock AJ (1993) The role of endothelium in hypoxic constriction of human pulmonary artery rings. Am Rev Respir Dis 147(2):283–290. PubMedCrossRefGoogle Scholar
  27. Dornan JC, Meban C (1985) The capillary plexus in the gas exchange zone of human neonatal lung: an ultrastructural study. Thorax 40(10):787–792PubMedPubMedCentralCrossRefGoogle Scholar
  28. Egan K, FitzGerald GA (2006) Eicosanoids and the vascular endothelium. Handb Exp Pharmacol 176 Pt 1:189–211CrossRefGoogle Scholar
  29. Elliott AR, Fu Z, Tsukimoto K, Prediletto R, Mathieu-Costello O, West JB (1992) Short-term reversibility of ultrastructural changes in pulmonary capillaries caused by stress failure. J Appl Physiol (1985) 73(3):1150–1158CrossRefGoogle Scholar
  30. Faure E, Equils O, Sieling PA, Thomas L, Zhang FX, Kirschning CJ, Polentarutti N, Muzio M, Arditi M (2000) Bacterial lipopolysaccharide activates NF-kappaB through toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells. Differential expression of TLR-4 and TLR-2 in endothelial cells. J Biol Chem 275(15):11058–11063PubMedCrossRefGoogle Scholar
  31. Fu Z, Costello ML, Tsukimoto K, Prediletto R, Elliott AR, Mathieu-Costello O, West JB (1992) High lung volume increases stress failure in pulmonary capillaries. J Appl Physiol (1985) 73(1):123–133CrossRefGoogle Scholar
  32. Fuchs A, Weibel ER (1966) Morphometric study of the distribution of a specific cytoplasmatic organoid in the rat’s endothelial cells. Zeitschrift fur Zellforschung und mikroskopische Anatomie (Vienna, Austria: 1948) 73(1):1–9CrossRefGoogle Scholar
  33. Furchgott RF, Vanhoutte PM (1989) Endothelium-derived relaxing and contracting factors. FASEB J 3(9):2007–2018PubMedGoogle Scholar
  34. Furchgott RF, Zawadzki JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288(5789):373–376PubMedCrossRefGoogle Scholar
  35. Gillespie JR, Tyler WS (1967) Quantitative electron microscopy of the interalveolar septa of the horse lung. Am Rev Respir Dis 95(3):477–483. PubMedGoogle Scholar
  36. Heltianu C, Simionescu M, Simionescu N (1982) Histamine receptors of the microvascular endothelium revealed in situ with a histamine-ferritin conjugate: characteristic high-affinity binding sites in venules. J Cell Biol 93(2):357–364PubMedCrossRefGoogle Scholar
  37. Jian MY, King JA, Al-Mehdi AB, Liedtke W, Townsley MI (2008) High vascular pressure-induced lung injury requires P450 epoxygenase-dependent activation of TRPV4. Am J Respir Cell Mol Biol 38(4):386–392. PubMedCrossRefGoogle Scholar
  38. Kaiser L, Sparks HV Jr (1986) Mediation of flow-dependent arterial dilation by endothelial cells. Circ Shock 18(2):109–114PubMedGoogle Scholar
  39. Kelly JJ, Moore TM, Babal P, Diwan AH, Stevens T, Thompson WJ (1998) Pulmonary microvascular and macrovascular endothelial cells: differential regulation of Ca2+ and permeability. Am J Physiol 274(5 Pt 1):L810–L819PubMedGoogle Scholar
  40. Kim D, Kim YJ, Koh HS, Jang TY, Park HE, Kim JY (2010) Reactive oxygen species enhance TLR10 expression in the human monocytic cell line THP-1. Int J Mol Sci 11(10):3769–3782. PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kindig CA, Erickson HH, Poole DC (2000) Dissociation of exercise-induced pulmonary hemorrhage and pulmonary artery pressure via nitric oxide synthase inhibition. J Equine Vet Sci 20(11):715–721. CrossRefGoogle Scholar
  42. King J, Hamil T, Creighton J, Wu S, Bhat P, McDonald F, Stevens T (2004) Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes. Microvasc Res 67(2):139–151. PubMedCrossRefGoogle Scholar
  43. Koller A, Sun D, Huang A, Kaley G (1994) Corelease of nitric oxide and prostaglandins mediates flow-dependent dilation of rat gracilis muscle arterioles. Am J Physiol 267(1 Pt 2):H326–H332PubMedGoogle Scholar
  44. Krogmann AO, Lusebrink E, Steinmetz M, Asdonk T, Lahrmann C, Lutjohann D, Nickenig G, Zimmer S (2016) Proinflammatory stimulation of Toll-like receptor 9 with high dose CpG ODN 1826 impairs endothelial regeneration and promotes atherosclerosis in mice. PLoS One 11(1):e0146326. PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kuebler WM, Ying X, Singh B, Issekutz AC, Bhattacharya J (1999) Pressure is proinflammatory in lung venular capillaries. J Clin Invest 104(4):495–502. PubMedPubMedCentralCrossRefGoogle Scholar
  46. Lamar CH, Turek JJ, Bottoms GD, Fessler JF (1986) Equine endothelial cells in vitro. Am J Vet Res 47(4):956–958PubMedGoogle Scholar
  47. Lorant DE, Patel KD, McIntyre TM, McEver RP, Prescott SM, Zimmerman GA (1991) Coexpression of GMP-140 and PAF by endothelium stimulated by histamine or thrombin: a juxtacrine system for adhesion and activation of neutrophils. J Cell Biol 115(1):223–234PubMedCrossRefGoogle Scholar
  48. Lowenstein CJ, Morrell CN, Yamakuchi M (2005) Regulation of Weibel-Palade body exocytosis. Trends Cardiovasc Med 15(8):302–308. PubMedCrossRefGoogle Scholar
  49. Ludwig MG, Seuwen K (2002) Characterization of the human adenylyl cyclase gene family: cDNA, gene structure, and tissue distribution of the nine isoforms. J Recept Signal Transduct Res 22(1-4):79–110. PubMedCrossRefGoogle Scholar
  50. Lundberg JM, Martling CR, Hökfelt T (1988) Airways, oral cavity and salivary glands: classical transmitters and peptides in sensory and autonomic motor neurons. In: Björklund A, Hökfelt T, Owman C (eds) Handbook of chemical neuroanatomy, vol 6. Elsevier Science, New York, NY, pp 391–444Google Scholar
  51. Lymboussaki A, Partanen TA, Olofsson B, Thomas-Crusells J, Fletcher CD, de Waal RM, Kaipainen A, Alitalo K (1998) Expression of the vascular endothelial growth factor C receptor VEGFR-3 in lymphatic endothelium of the skin and in vascular tumors. Am J Pathol 153(2):395–403. PubMedPubMedCentralCrossRefGoogle Scholar
  52. MacEachern KE, Smith GL, Nolan AM (1997) Methods for the isolation, culture and characterisation of equine pulmonary artery endothelial cells. Res Vet Sci 62(2):147–152PubMedCrossRefGoogle Scholar
  53. MacEachern KE, Smith GL, Nolan AM (2004) Characteristics of the in vitro hypoxic pulmonary vasoconstrictor response in isolated equine and bovine pulmonary arterial rings. Vet Anaesth Analg 31(4):239–249. PubMedCrossRefGoogle Scholar
  54. Magee JC, Stone AE, Oldham KT, Guice KS (1994) Isolation, culture, and characterization of rat lung microvascular endothelial cells. Am J Physiol 267(4 Pt 1):L433–L441PubMedGoogle Scholar
  55. Mantovani A, Bussolino F, Dejana E (1992) Cytokine regulation of endothelial cell function. FASEB J 6(8):2591–2599PubMedGoogle Scholar
  56. Marchesi VT (1961) The site of leucocyte emigration during inflammation. Q J Exp Physiol Cogn Med Sci 46:115–118PubMedGoogle Scholar
  57. Michel RP, Hu F, Meyrick BO (1995) Myoendothelial junctional complexes in postobstructive pulmonary vasculopathy: a quantitative electron microscopic study. Exp Lung Res 21(3):437–452PubMedCrossRefGoogle Scholar
  58. Millar FR, Summers C, Griffiths MJ, Toshner MR, Proudfoot AG (2016) The pulmonary endothelium in acute respiratory distress syndrome: insights and therapeutic opportunities. Thorax 71(5):462–473. PubMedCrossRefGoogle Scholar
  59. Minami T, Sugiyama A, Wu SQ, Abid R, Kodama T, Aird WC (2004) Thrombin and phenotypic modulation of the endothelium. Arterioscler Thromb Vasc Biol 24(1):41–53. PubMedCrossRefGoogle Scholar
  60. Muller AM, Nesslinger M, Skipka G, Muller KM (2002) Expression of CD34 in pulmonary endothelial cells in vivo. Pathobiology 70(1):11–17PubMedCrossRefGoogle Scholar
  61. Nishi Y, Kitamura N, Otani M, Hondo E, Taguchi K, Yamada J (2000) Distribution of capsaicin-sensitive substance P- and calcitonin gene-related peptide-immunoreactive nerves in bovine respiratory tract. Ann Anat 182(4):319–326. PubMedCrossRefGoogle Scholar
  62. Ochoa CD, Wu S, Stevens T (2010) New developments in lung endothelial heterogeneity: Von Willebrand factor, P-selectin, and the Weibel-Palade body. Semin Thromb Hemost 36(3):301–308. PubMedPubMedCentralCrossRefGoogle Scholar
  63. Ofori-Acquah SF, King J, Voelkel N, Schaphorst KL, Stevens T (2008) Heterogeneity of barrier function in the lung reflects diversity in endothelial cell junctions. Microvasc Res 75(3):391–402. PubMedCrossRefGoogle Scholar
  64. Pan J, Xia L, McEver RP (1998) Comparison of promoters for the murine and human P-selectin genes suggests species-specific and conserved mechanisms for transcriptional regulation in endothelial cells. J Biol Chem 273(16):10058–10067PubMedCrossRefGoogle Scholar
  65. Parbhakar OP, Duke T, Townsend HG, Singh B (2005) Depletion of pulmonary intravascular macrophages partially inhibits lipopolysaccharide-induced lung inflammation in horses. Vet Res 36(4):557–569. PubMedCrossRefGoogle Scholar
  66. Parker JC, Yoshikawa S (2002) Vascular segmental permeabilities at high peak inflation pressure in isolated rat lungs. Am J Physiol Lung Cell Mol Physiol 283(6):L1203–L1209. PubMedCrossRefGoogle Scholar
  67. Parker JC, Stevens T, Randall J, Weber DS, King JA (2006) Hydraulic conductance of pulmonary microvascular and macrovascular endothelial cell monolayers. Am J Physiol Lung Cell Mol Physiol 291(1):L30–L37. PubMedCrossRefGoogle Scholar
  68. Parthasarathi K, Ichimura H, Monma E, Lindert J, Quadri S, Issekutz A, Bhattacharya J (2006) Connexin 43 mediates spread of Ca2+-dependent proinflammatory responses in lung capillaries. J Clin Invest 116(8):2193–2200. PubMedPubMedCentralCrossRefGoogle Scholar
  69. Pascoe JR, Ferraro GL, Cannon JH, Arthur RM, Wheat JD (1981) Exercise-induced pulmonary hemorrhage in racing thoroughbreds: a preliminary study. Am J Vet Res 42(5):703–707PubMedGoogle Scholar
  70. Pelletier N, Leith DE (1993) Cardiac output but not high pulmonary artery pressure varies with FIO2 in exercising horses. Respir Physiol 91(1):83–97PubMedCrossRefGoogle Scholar
  71. Pober JS, Cotran RS (1990) Cytokines and endothelial cell biology. Physiol Rev 70(2):427–451PubMedCrossRefGoogle Scholar
  72. Pober JS, Sessa WC (2007) Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 7(10):803–815. PubMedCrossRefGoogle Scholar
  73. Prasain N, Stevens T (2009) The actin cytoskeleton in endothelial cell phenotypes. Microvasc Res 77(1):53–63. PubMedCrossRefGoogle Scholar
  74. Prescott SM, Zimmerman GA, McIntyre TM (1984) Human endothelial cells in culture produce platelet-activating factor (1-alkyl-2-acetyl-sn-glycero-3-phosphocholine) when stimulated with thrombin. Proc Natl Acad Sci U S A 81(11):3534–3538PubMedPubMedCentralCrossRefGoogle Scholar
  75. Rees DD, Palmer RM, Moncada S (1989) Role of endothelium-derived nitric oxide in the regulation of blood pressure. Proc Natl Acad Sci U S A 86(9):3375–3378PubMedPubMedCentralCrossRefGoogle Scholar
  76. Sayner S, Stevens T (2006) Soluble adenylate cyclase reveals the significance of compartmentalized cAMP on endothelial cell barrier function. Biochem Soc Trans 34(Pt 4):492–494. PubMedCrossRefGoogle Scholar
  77. Sayner SL, Alexeyev M, Dessauer CW, Stevens T (2006) Soluble adenylyl cyclase reveals the significance of cAMP compartmentation on pulmonary microvascular endothelial cell barrier. Circ Res 98(5):675–681. PubMedCrossRefGoogle Scholar
  78. Schenkel AR, Mamdouh Z, Chen X, Liebman RM, Muller WA (2002) CD99 plays a major role in the migration of monocytes through endothelial junctions. Nat Immunol 3(2):143–150. PubMedCrossRefGoogle Scholar
  79. Schneberger D, Caldwell S, Suri SS, Singh B (2009) Expression of toll-like receptor 9 in horse lungs. Anat Rec (Hoboken) 292(7):1068–1077. CrossRefGoogle Scholar
  80. Schneberger D, Lewis D, Caldwell S, Singh B (2011) Expression of toll-like receptor 9 in lungs of pigs, dogs and cattle. Int J Exp Pathol 92(1):1–7. PubMedPubMedCentralCrossRefGoogle Scholar
  81. Schneberger D, Aharonson-Raz K, Singh B (2012) Pulmonary intravascular macrophages and lung health: what are we missing? Am J Physiol Lung Cell Mol Physiol 302(6):L498–L503. PubMedCrossRefGoogle Scholar
  82. Schneeberger EE (1982) Structure of intercellular junctions in different segments of the intrapulmonary vasculature. Ann N Y Acad Sci 384:54–63PubMedCrossRefGoogle Scholar
  83. Schnitzer JE, Siflinger-Birnboim A, Del Vecchio PJ, Malik AB (1994) Segmental differentiation of permeability, protein glycosylation, and morphology of cultured bovine lung vascular endothelium. Biochem Biophys Res Commun 199(1):11–19PubMedCrossRefGoogle Scholar
  84. Sessa WC (2004) eNOS at a glance. J Cell Sci 117(Pt 12):2427–2429. PubMedCrossRefGoogle Scholar
  85. Sethi RS, Brar RS, Singh O, Singh B (2011) Immunolocalization of pulmonary intravascular macrophages, TLR4, TLR9 and IL-8 in normal and Pasteurella multocida-infected lungs of water buffalo (Bubalus bubalis). J Comp Pathol 144(2–3):135–144. PubMedCrossRefGoogle Scholar
  86. Singh B, Atwal OS (1997) Ultrastructural and immunocytochemical study of the pulmonary intravascular macrophages of Escherichia coli lipopolysaccharide-treated sheep. Anat Rec 247(2):214–224PubMedCrossRefGoogle Scholar
  87. Singh B, de la Concha-Bermejillo A (1998) Gadolinium chloride removes pulmonary intravascular macrophages and curtails the degree of ovine lentivirus-induced lymphoid interstitial pneumonia. Int J Exp Pathol 79(3):151–162PubMedGoogle Scholar
  88. Singh B, Ireland WP, Minhas K, Atwal OS (1995) Surface coat of sheep pulmonary intravascular macrophages: reconstitution, and implication of a glycosyl-phosphatidylinositol anchor. Anat Rec 243(4):466–478. PubMedCrossRefGoogle Scholar
  89. Singh B, Pearce JW, Gamage LN, Janardhan K, Caldwell S (2004) Depletion of pulmonary intravascular macrophages inhibits acute lung inflammation. Am J Physiol Lung Cell Mol Physiol 286(2):L363–L372. PubMedCrossRefGoogle Scholar
  90. Singh Suri S, Janardhan KS, Parbhakar O, Caldwell S, Appleyard G, Singh B (2006) Expression of toll-like receptor 4 and 2 in horse lungs. Vet Res 37(4):541–551. PubMedCrossRefGoogle Scholar
  91. Sirianni FE, Chu FS, Walker DC (2003) Human alveolar wall fibroblasts directly link epithelial type 2 cells to capillary endothelium. Am J Respir Crit Care Med 168(12):1532–1537. PubMedCrossRefGoogle Scholar
  92. Stevens T, Nakahashi Y, Cornfield DN, McMurtry IF, Cooper DM, Rodman DM (1995) Ca(2+)-inhibitable adenylyl cyclase modulates pulmonary artery endothelial cell cAMP content and barrier function. Proc Natl Acad Sci U S A 92(7):2696–2700PubMedPubMedCentralCrossRefGoogle Scholar
  93. Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21:335–376. PubMedCrossRefGoogle Scholar
  94. Townsley MI (2012) Structure and composition of pulmonary arteries, capillaries, and veins. Compr Physiol 2(1):675–709. PubMedPubMedCentralGoogle Scholar
  95. Tsukimoto K, Mathieu-Costello O, Prediletto R, Elliott AR, West JB (1991) Ultrastructural appearances of pulmonary capillaries at high transmural pressures. J Appl Physiol (1985) 71(2):573–582CrossRefGoogle Scholar
  96. Turek JJ, Lamar CH, Fessler JF, Bottoms GD (1987) Ultrastructure of equine endothelial cells exposed to endotoxin and flunixin meglumine and equine neutrophils. Am J Vet Res 48(9):1363–1366PubMedGoogle Scholar
  97. Vrolyk V, Wobeser BK, Al-Dissi AN, Carr A, Singh B (2017) Lung inflammation associated with clinical acute necrotizing pancreatitis in dogs. Vet Pathol 54(1):129–140.
  98. Walker DC, MacKenzie A, Hosford S (1994) The structure of the tricellular region of endothelial tight junctions of pulmonary capillaries analyzed by freeze-fracture. Microvasc Res 48(3):259–281. PubMedCrossRefGoogle Scholar
  99. Walker DC, Behzad AR, Chu F (1995) Neutrophil migration through preexisting holes in the basal laminae of alveolar capillaries and epithelium during streptococcal pneumonia. Microvasc Res 50(3):397–416. PubMedCrossRefGoogle Scholar
  100. Wang JW, Eikenboom J (2010) Von Willebrand disease and Weibel-Palade bodies. Hamostaseologie 30(3):150–155PubMedGoogle Scholar
  101. Wassef A, Janardhan K, Pearce JW, Singh B (2004) Toll-like receptor 4 in normal and inflamed lungs and other organs of pig, dog and cattle. Histol Histopathol 19(4):1201–1208PubMedGoogle Scholar
  102. West JB (2000) Invited review: pulmonary capillary stress failure. J Appl Physiol (1985) 89(6):2483–2489. discussion 2497CrossRefGoogle Scholar
  103. West JB, Mathieu-Costello O, Jones JH, Birks EK, Logemann RB, Pascoe JR, Tyler WS (1993) Stress failure of pulmonary capillaries in racehorses with exercise-induced pulmonary hemorrhage. J Appl Physiol (1985) 75(3):1097–1109CrossRefGoogle Scholar
  104. Winkler GC (1988) Pulmonary intravascular macrophages in domestic animal species: review of structural and functional properties. Am J Anat 181(3):217–234. PubMedCrossRefGoogle Scholar
  105. Wu S, Haynes J Jr, Taylor JT, Obiako BO, Stubbs JR, Li M, Stevens T (2003) Cav3.1 (alpha1G) T-type Ca2+ channels mediate vaso-occlusion of sickled erythrocytes in lung microcirculation. Circ Res 93(4):346–353. PubMedCrossRefGoogle Scholar
  106. Wu S, Jian MY, Xu YC, Zhou C, Al-Mehdi AB, Liedtke W, Shin HS, Townsley MI (2009) Ca2+ entry via alpha1G and TRPV4 channels differentially regulates surface expression of P-selectin and barrier integrity in pulmonary capillary endothelium. Am J Physiol Lung Cell Mol Physiol 297(4):L650–L657. PubMedPubMedCentralCrossRefGoogle Scholar
  107. Xu SF, Wang P, Liang ZX, Sun JP, Zhao XW, Li AM, Chen LA (2011) Investigation of inflammatory responses of pulmonary microvascular endothelial cells induced by lipopolysaccharide and mechanism. Zhonghua Jie He He Hu Xi Za Zhi 34(11):816–820PubMedGoogle Scholar
  108. Yin J, Hoffmann J, Kaestle SM, Neye N, Wang L, Baeurle J, Liedtke W, Wu S, Kuppe H, Pries AR, Kuebler WM (2008) Negative-feedback loop attenuates hydrostatic lung edema via a cGMP-dependent regulation of transient receptor potential vanilloid 4. Circ Res 102(8):966–974. PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Canadian Centre for Health and Safety in AgricultureUniversity of SaskatchewanSaskatoonCanada
  2. 2.School of Animal BiotechnologyGuru Angad Dev Veterinary and Animal Sciences UniversityLudhianaIndia
  3. 3.Faculty of Veterinary MedicineUniversity of CalgaryCalgaryCanada

Personalised recommendations