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Articles

2008 Landis Award Lecture Inflammation and the Autodigestion Hypothesis

Pages 289-306 | Received 28 Dec 2008, Published online: 20 Apr 2009

References

  • Abraham CR, Potter H. The protease inhibitor, alpha 1-antichymotrypsin, is a component of the brain amyloid deposits in normal aging and Alzheimer's disease. Ann Med 1989; 21: 77–81
  • Acosta JA, Hoyt DB, Schmid-Schönbein GW, Hugli TE, Anjaria DJ, Frankel DA, Coimbra R. Intraluminal pancreatic serine protease activity, mucosal permeability, and shock: a review. Shock 2006; 26: 3–9
  • Adams CA, Jr, Xu DZ, Lu Q, Deitch EA. Factors larger than 100 kd in post-hemorrhagic shock mesenteric lymph are toxic for endothelial cells. Surgery 2001; 129: 351–363
  • Ahmad E, Steinberg SM, Goldin L, Hess CJ, Caporaso N, Kreitman RJ, Wiestner A, Wilson W, White T, Marti G, Stetler-Stevenson M. Immunophenotypic features distinguishing familial chronic lymphocytic leukemia from sporadic chronic lymphocytic leukemia. Cytom B Clin Cytom 2008; 74: 221–226
  • Arndt H, Smith CW, Granger DN. Leukocyte-endothelial cell adhesion in spontaneously hypertensive and normotensive rats. Hypertension 1993; 21: 667–673
  • Arroyo AG, Genis L, Gonzalo P, Matias-Roman S, Pollan A, Galvez BG. Matrix metalloproteinases: new routes to the use of MT1-MMP as a therapeutic target in angiogenesis-related disease. Curr Pharm Des 2007; 13: 1787–1802
  • Beaudeux JL, Giral P, Bruckert E, Foglietti MJ, Chapman MJ. Matrix metalloproteinases, inflammation, and atherosclerosis: therapeutic perspectives. Clin Chem Lab Med 2004; 42: 121–131
  • Biffl WL, Moore EE, Moore FA. Gut-derived mediators of multiple organ failure: platelet-activating factor and interleukin-6. Br J Hosp Med 1995; 54: 134–138
  • Boonacker E, Van Noorden CJ. Enzyme cytochemical techniques for metabolic mapping in living cells, with special reference to proteolysis. J Histochem Cytochem 2001; 49: 1473–1486
  • Brundula V, Rewcastle NB, Metz LM, Bernard CC, Yong VW. Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain 2002; 125: 1297–1308
  • Bursztyn M, Ben-Ishay D, Gutman A. Insulin resistance in spontaneously hypertensive rats but not in deoxycorticosterone-salt or renal vascular hypertension. J Hypertens 1992; 10: 137–142
  • Bush KT, Tsukamoto T, Nigam SK. Selective degradation of E-cadherin and dissolution of E-cadherin-catenin complexes in epithelial ischemia. Am J Physiol Renal Physiol 2000; 278: F847–F852
  • Chang TW. Improvement of survival from hemorrhagic shock by enterectomy in rats: finding to implicate the role of the gut for irreversibility of hemorrhagic shock. J Trauma 1997; 42: 223–230
  • Childs EW, Udobi KF, Hunter FA. Hypothermia reduces microvascular permeability and reactive oxygen species expression after hemorrhagic shock. J Trauma 2005; 58: 271–277
  • Cho KO, La HO, Cho YJ, Sung KW, Kim SY. Minocycline attenuates white matter damage in a rat model of chronic cerebral hypoperfusion. J Neurosci Res 2006; 83: 285–291
  • Chung AW, Booth AD, Rose C, Thompson CR, Levin A, van Breemen C. Increased matrix metalloproteinase 2 activity in the human internal mammary artery is associated with ageing, hypertension, diabetes, and kidney dysfunction. J Vasc Res 2008; 45: 357–362
  • Coimbra, R, Hoyt, D, Winchell, R, Simons, R, Fortlage, D, Garcia, J. 1996. The ongoing challenge of retroperitoneal vascular injuries. Am J Surg, 172:541–544; discussion, 545.
  • Curry S, Brick P, Franks NP. Fatty acid binding to human serum albumin: new insights from crystallographic studies. Biochim Biophys Acta 1999; 1441: 131–140
  • Dayal, SD, Hauser, CJ, Feketeova, E, Fekete, Z, Adams, JM, Lu, Q, Xu, DZ, Zaets, S, Deitch, EA. 2002. Shock mesenteric lymph-induced rat polymorphonuclear neutrophil activation and endothelial cell injury is mediated by aqueous factors. J Trauma, 52:1048–1055; discussion, 1055.
  • Deitch ED, Shi HP, Lu Q, Feketeova E, Xu DZ. Serine proteases are involved in the pathogenesis of trauma-hemorrhagic shoch-induced gut and lung injury. Shock 2003; 19: 452–456
  • del Zoppo GJ, Milner R, Mabuchi T, Hung S, Wang X, Berg GI, Koziol JA. Microglial activation and matrix protease generation during focal cerebral ischemia. Stroke 2007; 38: 646–651
  • DeLano FA, Balete R, Schmid-Schönbein GW. Control of oxidative stress in microcirculation of spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 2005; 288: H805–H812
  • DeLano, FA, Hoyt, DB, Schmid-Schönbein, GW. 2007. The auto-digestion hypothesis: blockade of pancreatic digestive enzymes in the lumen of the intestine during hemorrhagic shock reduces mortality. FASEB J, 21:421, (Abstract).
  • DeLano FA, Parks DA, Ruedi JM, Babior BM, Schmid-Schönbein GW. Microvascular display of xanthine oxidase and NADPH oxidase in the spontaneously hypertensive rat. Microcirculation 2006; 13: 551–566
  • DeLano FA, Schmid-Schönbein GW. Proteinase activity and receptor cleavage: mechanism for insulin resistance in the spontaneously hypertensive rat. Hypertension 2008; 52: 415–423
  • Emerit I, Garban F, Vassy J, Levy A, Filipe P, Freitas J. Superoxide-mediated clastogenesis and anticlastogenic effects of exogenous superoxide dismutase. Proc Natl Acad Sci U S A 1996; 93: 12799–12804
  • Eppihimer MJ, Granger DN. Ischemia/reperfusion-induced leukocyte-endothelial interactions in postcapillary venules. Shock 1997; 8: 16–25
  • Fitzal F, Delano FA, Young C, Rosario HS, Junger WG, Schmid-Schönbein GW. Pancreatic enzymes sustain systemic inflammation after an initial endotoxin challenge. Surgery 2003; 134: 446–456
  • Fitzal F, DeLano FA, Young C, Rosario HS, Schmid-Schönbein GW. Pancreatic protease inhibition during shock attenuates cell activation and peripheral inflammation. J Vasc Res 2002; 39: 320–329
  • Fitzal F, DeLano FA, Young C, Schmid-Schönbein GW. Improvement in early symptoms of shock by delayed intestinal protease inhibition. Arch Surg 2004; 139: 1008–1016
  • Fitzal, F, Kistler, E, Mitsuoka, H, Hugli, TE, Schmid-Schönbein, GW. (2005). A new hypothesis for the origin of shock: Self-digestion of the ischemic intestine by pancreatic enzymes. In: JA Pitzer, Progress in Inflammation. Nova Science Pub.
  • Fruchterman TM, Spain DA, Wilson MA, Harris PD, Garrison RN. Selective microvascular endothelial cell dysfunction in the small intestine following resuscitated hemorrhagic shock. Shock 1998; 10: 417–422
  • Fukuda S, Fini CA, Mabuchi T, Koziol JA, Eggleston LL, Jr, del Zoppo GJ. Focal cerebral ischemia induces active proteases that degrade microvascular matrix. Stroke 2004; 35: 998–1004
  • Fukuda T, Hata N. Mechanisms of endotoxin shock in rats and the anti-endotoxic effect of glucocorticoids and endotoxin-conditioning. Jap J Physiol 1969; 19: 509–520
  • Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res 2002; 90: 251–262
  • Garcia RA, Pantazatos DP, Gessner CR, Go KV, Woods VL, Jr, Villarreal FJ. Molecular interactions between matrilysin and the matrix metalloproteinase inhibitor doxycycline investigated by deuterium exchange mass spectrometry. Mol Pharmacol 2005; 67: 1128–1136
  • Garcia Soriano F, Liaudet L, Marton A, Hasko G, Batista Lorigados C, Deitch EA, Szabo C. Inosine improves gut permeability and vascular reactivity in endotoxic shock. Crit Care Med 2001; 29: 703–708
  • Gasche Y, Soccal PM, Kanemitsu M, Copin JC. Matrix metalloproteinases and diseases of the central nervous system with a special emphasis on ischemic brain. Front Biosci 2006; 11: 1289–1301
  • George SK, Meyer TN, Abdeen O, Bush KT, Nigam SK. Tunicamycin preserves intercellular junctions, cytoarchitecture, and cell-substratum interactions in ATP-depleted epithelial cells. Biochem Biophys Res Commun 2004; 322: 223–231
  • Glenn TM, Herlihy BL, Ferfuson WW, Lefer AM. Protective effect of pancreatic duct ligation in splanchnic ischemia shock. Am J Physiol 1972; 222: 1278–1284
  • Go VLW, Dimagno EP, Gardner JD, Lebenthal E, Reber HA, Scheele GA. The Pancreas. Biology, Pathobiology, and Disease. Raven Press, New York 1993; 1–1176
  • Griffin MO, Jinno M, Miles LA, Villarreal FJ. Reduction of myocardial infarct size by doxycycline: a role for plasmin inhibition. Mol Cell Biochem 2005; 270: 1–11
  • Harlan JM, Winn RK. Leukocyte-endothelial interactions: clinical trials of anti-adhesion therapy. Crit Care Med 2002; 30: S214–S219
  • Healey MA, Samphire J, Hoyt DB, Liu F, Davis R, Loomis WH. Irreversible shock is not irreversible: a new model of massive hemorrhage and resuscitation. J Trauma 2001; 50: 826–834
  • Hinshaw LB. Sepsis/septic shock: participation of the microcirculation: an abbreviated review. Crit Care Med 1996; 24: 1072–1078
  • Hulman S, Falkner B, Freyvogel N. Insulin resistance in the conscious spontaneously hypertensive rat: euglycemic hyperinsulinemic clamp study. Metab Clin Exp 1993; 42: 14–18
  • Jarrar D, Wang P, Cioffi WG, Bland KI, Chaudry IH. Critical role of oxygen radicals in the initiation of hepatic depression after trauma hemorrhage. J Trauma 2000; 49: 879–885
  • Kaiser, VL, Sifri, ZC, Senthil, M, Dikdan, GS, Lu, Q, Xu, DZ, Deitch, EA. 2005. Albumin peptide: a molecular marker for trauma/hemorrhagic-shock in rat mesenteric lymph. Peptides, 26:2491–2499. Epub 2005 Jun 8.
  • Kien ND, Antognini JF, Reilly DA, Moore PG. Small-volume resuscitation using hypertonic saline improves organ perfusion in burned rats. Anesth Analges 1996; 83: 782–788
  • Kistler EB, Hugli TE, Schmid-Schönbein GW. The pancreas as a source of cardiovascular cell activating factors. Microcirculation 2000; 7: 183–192
  • Kistler EB, Lefer AM, Hugli TE, Schmid-Schönbein GW. Plasma activation during splanchnic arterial occlusion shock. Shock 2000; 14: 30–34
  • Kolev K, Skopal J, Simon L, Csonka E, Machovich R, Nagy Z. Matrix metalloproteinase-9 expression in post-hypoxic human brain capillary endothelial cells: H2O2 as a trigger and NF-kappaB as a signal transducer. Thromb Haemost 2003; 90: 528–537
  • Korhonen H, Pihlanto A. Food-derived bioactive peptides—opportunities for designing future foods. Curr Pharm Des 2003; 9: 1297–1308
  • Kramp WJ, Waldo S, Schmid-Schönbein GW, Hoyt D, Coimbra R, Hugli TE. Characterization of two classes of pancreatic shock factors: functional differences exhibited by hydrophilic and hydrophobic shock factors. Shock 2003; 20: 356–362
  • Labat-Robert J, Kern P, Robert L. Biomarkers of connective tissue aging: biosynthesis of fibronectin, collagen type III, and elastase. Ann N Y Acad Sci 1992; 673: 16–22
  • Lee CZ, Yao JS, Huang Y, Zhai W, Liu W, Guglielmo BJ, Lin E, Yang GY, Young WL. Dose-response effect of tetracyclines on cerebral matrix metalloproteinase-9 after vascular endothelial growth factor hyperstimulation. J Cereb Blood Flow Metab 2006; 26: 1157–1164
  • Lefer AM. Myocardial depressant factor and circulatory shock. Klinische Wochenschrift 1974; 52: 358–370
  • Lefer AM. Role of a myocardial depressant factor in the pathogenesis of circulatory shock. Fed Proc 1970; 29: 1836–1847
  • Lehoux S, Lemarie CA, Esposito B, Lijnen HR, Tedgui A. Pressure-induced matrix metalloproteinase-9 contributes to early hypertensive remodeling. Circulation 2004; 109: 1041–1047
  • Leonardo CC, Eakin AK, Ajmo JM, Collier LA, Pennypacker KR, Strongin AY, Gottschall PE. Delayed administration of a matrix metalloproteinase inhibitor limits progressive brain injury after hypoxia-ischemia in the neonatal rat. J Neuroinflammation 2008; 5: 34
  • Ley K, Gaehtgens P. Microcirculation disorders in shock]. Klin Anasthesiol Intensivther 1987; 33: 19–36
  • Lijnen HR. Extracellular proteolysis in the development and progression of atherosclerosis. Biochem Soc Trans 2002; 30: 163–167
  • Lim HH, DeLano FA, Schmid-Schönbein GW. Life and death cell labeling in the microcirculation of the spontaneously hypertensive rat. J Vasc Res 2001; 38: 228–236
  • Luttun A, Dewerchin M, Collen D, Carmeliet P. The role of proteinases in angiogenesis, heart development, restenosis, atherosclerosis, myocardial ischemia, and stroke: insights from genetic studies. Curr Atheroscler Rep 2000; 2: 407–416
  • Manabe T, Suzuki T, Honjo I. Role of the pancreas in organ blood flow during shock. Surg Gynecol Obstet 1978; 146: 577–582
  • Martin MA, Monnnai M, Otani H. Isolation and characterization of a cytotoxic pentapeptide, k-casecidin, from bovine K-casein digested with bovine trypsin. Anim Sci J 2000; 71: 197–207
  • Martin MA, Otani H. Antimicrobial and cytotoxic peptides released from milk proteins by the action of mammalian gastrointestinal proteinases. Curr Res Adv Agric Biol Chem 2001; 1: 23–36
  • Mathison JC, Wolfson E, Ulevitch RJ. Participation of tumor necrosis factor in the mediation of Gram-negative bacterial lipopolysaccharide-induced injury in rabbits. J Clin Invest 1988; 81: 1925–1937
  • McCord JM, Fridovich I. Superoxide dismutase: an enzymatic function for erthryocuprein (hemocuprein). J Biol Chem 1969; 244: 6049–6055
  • McCuskey RS. Hepatic and splanchnic microvascular responses to inflammation and shock. Hepato-Gastroenterol 1999; 46(Suppl 2)1464–1467
  • McMillen MA, Huribal M, Sumpio B. Common pathway of endothelial-leukocyte interaction in shock, ischemia, and reperfusion. Am J Surg 1993; 166: 557–562
  • Meisel H, FitzGerald RJ. Biofunctional peptides from milk proteins: mineral binding and cytomodulatory effects. Curr Pharm Des 2003; 9: 1289–1295
  • Migeotte I, Riboldi E, Franssen JD, Gregoire F, Loison C, Wittamer V, Detheux M, Robberecht P, Costagliola S, Vassart G, Sozzani S, Parmentier M, Communi D. Identification and characterization of an endogenous chemotactic ligand specific for FPRL2. J Exp Med 2005; 201: 83–93
  • Mitsuoka H, Kistler EB, Schmid-Schönbein GW. Generation of in vivo activating factors in the ischemic intestine by pancreatic enzymes. Proc Natl Acad Sci U S A 2000; 97: 1772–1777
  • Mitsuoka H, Kistler EB, Schmid-Schönbein GW. Protease inhibition in the intestinal lumen: attenuation of systemic inflammation and early indicators of multiple organ failure in shock. Shock 2002; 17: 205–209
  • Mota-Filipe H, McDonald MC, Cuzzocrea S, Thiemermann C. A membrane-permeable radical scavenger reduces the organ injury in hemorrhagic shock. Shock 1999; 12: 255–261
  • Newby AC. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev 2005; 85: 1–31
  • O'Connor DT, Takiyyuddin MA, Printz MP, Dinh TQ, Barbosa JA, Rozansky DJ, Mahata SK, Wu H, Kennedy BP, Ziegler MG, Wright FA, Schlager G, Parmer RJ. Catecholamine storage vesicle protein expression in genetic hypertension. Blood Press 1999; 8: 285–295
  • Ooyama, T, Sakamato, H. 1995. Elastase in the prevention of arterial aging and the treatment of atherosclerosis. Ciba Found Symp, 192:307–317; discussion, 318–320.
  • Otani H, Hata I. Inhibition of proliferative responses of mouse spleen lymphocytes and rabbit Peyer's patch cells by bovine milk caseins and their digests. J Dairy Res 1995; 62: 339–348
  • Parker F, Migliore-Samour D, Floc'h F, Zerial A, Werner GH, Jolles J, Casaretto M, Zahn H, Jolles P. Immunostimulating hexapeptide from human casein: amino acid sequence, synthesis, and biological properties. Eur J Biochem 1984; 145: 677–682
  • Peitzman AB, Billiar TR, Harbrecht BG, Kelly E, Udekwu AO, Simmons RL. Hemorrhagic shock. Curr Prob Surg 1995; 32: 925–1002
  • Penn, AH. (2005). Digestive enzymes in the generation of cytotoxic mediators during shock. University of California–San Diego, Ph.D. Thesis.
  • Penn AH, Hugli TE, Schmid-Schönbein GW. Pancreatic enzymes generate cytotoxic mediators in the intestine. Shock 2007; 27: 296–304
  • Penn AH, Schmid-Schönbein GW. The intestine as source of cytotoxic mediators in shock: free fatty acids and degradation of lipid-binding proteins. Am J Physiol Heart Circ Physiol 2008; 294: H1779–H1792
  • Pillai S, Oresajo C, Hayward J. Ultraviolet radiation and skin aging: roles of reactive oxygen species, inflammation and protease activation, and strategies for prevention of inflammation-induced matrix degradation—a review. Int J Cosmet Sci 2005; 27: 17–34
  • Prewitt RL, Cardoso SS, Wood WB. Prevention of arteriolar rarefaction in the spontaneously hypertensive rat by exposure to simulated high altitude. J Hypertens 1986; 4: 735–740
  • Raffetto JD, Khalil RA. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem Pharmacol 2008; 75: 346–359
  • Roghanian A, Sallenave JM. Neutrophil elastase (NE) and NE inhibitors: canonical and noncanonical functions in lung chronic inflammatory diseases (cystic fibrosis and chronic obstructive pulmonary disease). J Aerosol Med Pulm Drug Deliv 2008; 21: 125–144
  • Rollwagen FM, Li YY, Pacheco ND, Dick EJ, Kang YH. Microvascular effects of oral interleukin-6 on ischemia/reperfusion in the murine small intestine. Am J Pathol 2000; 156: 1177–1182
  • Romero-Perez D, Fricovsky E, Yamasaki KG, Griffin M, Barraza-Hidalgo M, Dillmann W, Villarreal F. Cardiac uptake of minocycline and mechanisms for in vivo cardioprotection. J Am Coll Cardiol 2008; 52: 1086–1094
  • Rosario HS, Waldo SW, Becker SA, Schmid-Schönbein GW. Pancreatic trypsin increases matrix metalloproteinase-9 accumulation and activation during acute intestinal ischemia-reperfusion in the rat. Am J Pathol 2004; 164: 1707–1716
  • Roumen RM, Hendriks T, Wevers RA, Goris JA. Intestinal permeability after severe trauma and hemorrhagic shock is increased without relation to septic complications. Arch Surg 1993; 128: 453–457
  • Rubanyi GM. Nitric oxide and circulatory shock. Adv Exp Med Biol 1998; 454: 165–172
  • Russell DH, Barreto JC, Klemm K, Miller TA. Hemorrhagic shock increases gut macromolecular permeability in the rat. Shock 1995; 4: 50–55
  • Scheidler, N. (2007). The Impact of Endothelial Mechanotransduction on Capillary Network Perfusion. University of California–San Diego, Ph.D. Thesis.
  • Schmid-Schönbein GW. Analysis of inflammation. Annu Rev Biomed Eng 2006; 8: 93–131
  • Schmid-Schönbein GW, Hugli TE, Kistler EB, Sofianos A, Mitsuoka H. Pancreatic enzymes and microvascular cell activation in multiorgan failure. Microcirculation 2001; 8: 5–14
  • Schmid-Schönbein GW, Kistler EB, Hugli TE. Mechanisms for cell activation and its consequences for biorheology and microcirculation: multi-organ failure in shock. Biorheology 2001; 38: 185–201
  • Schmid-Schönbein GW, Seiffge D, DeLano FA, Shen K, Zweifach BW. Leukocyte counts and activation in spontaneously hypertensive and normotensive rats. Hypertension 1991; 17: 323–330
  • Schober M, Howe PR, Sperk G, Fischer-Colbrie R, Winkler H. An increased pool of secretory hormones and peptides in adrenal medulla of stroke-prone spontaneously hypertensive rats. Hypertension 1989; 13: 469–474
  • Sechi LA, Griffin CA, Giacchetti G, Zingaro L, Catena C, Bartoli E, Schambelan M. Abnormalities of insulin receptors in spontaneously hypertensive rats. Hypertension 1996; 27: 955–961
  • Shen K, Sung KL, Whittemore DE, DeLano FA, Zweifach BW, Schmid-Schönbein GW. Properties of circulating leukocytes in spontaneously hypertensive rats. Biochem Cell Biol 1995; 73: 491–500
  • Smedegård G, Cui LX, Hugli TE. Endotoxin-induced shock in the rat. A role for C5a. Am J Pathol 1989; 135: 489–497
  • Spinale FG. Matrix metalloproteinases: regulation and dysregulation in the failing heart. Circ Res 2002; 90: 520–530
  • Suematsu M, Suzuki H, Delano FA, Schmid-Schönbein GW. The inflammatory aspect of the microcirculation in hypertension: oxidative stress, leukocytes/endothelial interaction, apoptosis. Microcirculation 2002; 9: 259–276
  • Suematsu M, Suzuki H, Tamatani T, Iigou Y, DeLano FA, Miyasaka M, Forrest MJ, Kannagi R, Zweifach BW, Ishimura Y, Schmid-Schönbein GW. Impairment of selectin-mediated leukocyte adhesion to venular endothelium in spontaneously hypertensive rats. J Clin Invest 1995; 96: 2009–2016
  • Suzuki H, DeLano FA, Jamshidi N, Katz D, Mori M, Kosaki K, Gottlieb RA, Ishii H, Schmid-Schönbein GW. Enhanced DNA fragmentation in the thymus of spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol 1999; 276: H2135–H2140
  • Suzuki H, Schmid-Schönbein GW, Suematsu M, DeLano FA, Forrest MJ, Miyasaka M, Zweifach BW. Impaired leukocyte-endothelial cell interaction in spontaneously hypertensive rats. Hypertension 1994; 24: 719–727
  • Suzuki H, Swei A, Zweifach BW, Schmid-Schönbein GW. In vivo evidence for microvascular oxidative stress in spontaneously hypertensive rats. Hydroethidine microfluorography. Hypertension 1995; 25: 1083–1089
  • Suzuki T, Motoyama T, Sato R. Periarteritis nodosa in spontaneously hypertensive rats. Acta Pathol Jpn 1980; 30: 907–912
  • Takiyyuddin MA, De Nicola L, Gabbai FB, Dinh TQ, Kennedy B, Ziegler MG, Sabban EL, Parmer RJ, O'Connor DT. Catecholamine secretory vesicles. Augmented chromogranins and amines in secondary hypertension. Hypertension 1993; 21: 674–679
  • Thiagarajan RR, Winn RK, Harlan JM. The role of leukocyte and endothelial adhesion molecules in ischemia-reperfusion injury. Thromb Haemost 1997; 78: 310–314
  • Tompkins SD, Gregory S, Hoyt DB, Ozkan AN. In vitro inhibition of IL-2 biosynthesis in activated human peripheral blood mononuclear cells by a trauma-induced glycopeptide. Immunol Lett 1990; 23: 205–209
  • Tran, ED, Schmid-Schönbein, GW. 2007. An in-vivo analysis of capillary stasis and endothelial apoptosis in a model of hypertension. Microcirculation. 1–12.
  • Uchiba M, Okajima K, Murakami K, Okabe H, Takatsuki K. Endotoxin-induced pulmonary vascular injury is mainly mediated by activated neutrophils in rats. Thromb Res 1995; 78: 117–125
  • Vender RL. Therapeutic potential of neutrophil-elastase inhibition in pulmonary disease. J Invest Med 1996; 44: 531–539
  • Vollmar B. Microcirculation and oxygen supply to the liver in hemorrhagic shock and sepsis]. Anasthesiol Intensivmed Notfallmed Schmerzther 1995; 30(Suppl 1)S52–S54
  • Waldo SW, Rosario HS, Penn AH, Schmid-Schönbein GW. Pancreatic digestive enzymes are potent generators of mediators for leukocyte activation and mortality. Shock 2003; 20: 138–143
  • Wang Y, Luo W, Reiser G. Trypsin and trypsin-like proteases in the brain: proteolysis and cellular functions. Cell Mol Life Sci 2008; 65: 237–252
  • Watanabe N, Ikeda U. Matrix metalloproteinases and atherosclerosis. Curr Atheroscler Rep 2004; 6: 112–120
  • Wattanasirichaigoon S, Menconi MJ, Delude RL, Fink MP. Effect of mesenteric ischemia and reperfusion or hemorrhagic shock on intestinal mucosal permeability and ATP content in rats. Shock 1999; 12: 127–133
  • Waxman K. Shock: ischemia, reperfusion, and inflammation. New Horiz 1996; 4: 153–160
  • Wettstein R, Tsai AG, Erni D, Winslow RM, Intaglietta M. Resuscitation with polyethylene glycol-modified human hemoglobin improves microcirculatory blood flow and tissue oxygenation after hemorrhagic shock in awake hamsters. Crit Care Med 2003; 31: 1824–1830
  • Winn RK, Mihelicic D, Vedder NB, Sharar SR, Harlan JM. Monoclonal antibodies to leukocyte and endothelial adhesion molecules attenuate ischemia-reperfusion injury. Behring Institute Mitteilungen 1993; 119: 229–237
  • Winn, RK, Sharar, SR, Vedder, NB, Harlan, JM. 1995. Leukocyte and endothelial adhesion molecules in ischaemia/reperfusion injuries. Ciba Found Symp, 189:63–71; discussion, 72–76, 77–78.
  • Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS-binding protein. Science 1990; 249: 1431–1433
  • Yong VW, Zabad RK, Agrawal S, Goncalves Dasilva A, Metz LM. Elevation of matrix metalloproteinases (MMPs) in multiple sclerosis and impact of immunomodulators. J Neurol Sci 2007; 259: 79–84
  • Zimmet P, Magliano D, Matsuzawa Y, Alberti G, Shaw J. The metabolic syndrome: a global public health problem and a new definition. J Atheroscler Thromb 2005; 12: 295–300
  • Zweifach BW, Kovalcheck S, DeLano F, Chen P. Micropressure-flow relationships in a skeletal muscle of spontaneously hypertensive rats. Hypertension 1981; 3: 601–614
  • Zweifach BW, Lipowsky HH. Pressure-flow relations in blood and lymph microcirculation. Handbook of Physiology, Section 2: The Cardiovascular System, EM Renkin, CC Michel. American Physiological Society, Bethesda, MarylandUSA 1984; 251–307

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