Abstract
Leukocyte recruitment is a hallmark feature of the inflammatory response. This review summarizes the generally accepted paradigm of leukocyte recruitment based on studies using intravital microscopy to visualize the microcirculation. The role of selectins and α4‐integrin in rolling as well as integrin‐mediated adhesion is discussed. However, it is becoming increasingly clear that the recruitment cascade within organs differs and therefore the review also attempts to highlight what is and is not known regarding leukocyte recruitment into the brain microvasculature. In the second part of this review, we provide some discussion of mechanisms by which the inflammatory response may be terminated. Particular emphasis on nuclear factor NfκB and how IL10, IL13 and secreted leukocyte protease inhibitor (SLPI) may impact upon the NfκB‐dependent inflammatory response is presented.
Full Text
The Full Text of this article is available as a PDF (73.8 KB).
References
- 1. Abbassi O, Kishimoto TK, McIntire LV, Anderson DC, Smith CW (1993) E‐selectin supports neutrophil rolling in vitro under conditions of flow. J Clin Invest 92: 2719–2730. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Albelda SM, Smith CW, Ward PA (1994) Adhesion molecules and inflammatory injury. FASEB J 8: 504–512. [PubMed] [Google Scholar]
- 3. Alon R, Kassner PD, Carr MW, Finger EB, Hemler ME, Springer TA (1995) The integrin VLA‐4 supports tethering and rolling in flow on VCAM‐1. J Cell Biol 128: 1243–1253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. Akopov S, Sercombe R, Seylaz J (1996) Cerebrovascular reactivity: role of endothelium/platelet/leukocyte interactions. Cerebrovasc Brain Metab Rev 8: 11–94. [PubMed] [Google Scholar]
- 5. Arbones ML, Ord DC, Ley K, Ratech H, Maynard‐Curry C, Otten G, Capon DJ, Tedder TF (1994) Lymphocyte homing and leukocyte rolling and migration are impaired in L‐selectin‐deficient mice. Immunity 1: 247–260. [DOI] [PubMed] [Google Scholar]
- 6. Barkalow FJ, Goodman MJ, Gerritsen ME, Mayadas TN (1996) Brain endothelium lack one of two pathways of P‐selectin‐mediated neutrophil adhesion. Blood 88: 4585–4593. [PubMed] [Google Scholar]
- 7. Bednar MM, Gross CE, Russel SR, Fuller SP, Ellenberger CL, Schindler E, Klingbeil C, Vexler V (1998) Humanized anti‐L‐selectin monoclonal antibody DREG200 therapy in acute thromboembolic stroke. Neurol Res 20: 403–408. [DOI] [PubMed] [Google Scholar]
- 8. Berlin C, Bargatze RF, Campbell JJ, Von Andrian UH, Szabo MC, Hasslen SR, Nelson RD, Berg EL, Erlandsen SL, Butcher EC (1995) a4 integrins mediate lymphocyte attachment and rolling under physiologic flow. Cell 80: 413–422. [DOI] [PubMed] [Google Scholar]
- 9. Bevilacqua MP, Pober JS, Mendrick DL, Cotran RS, Gimbrone MA (1987) Identification of an inducible endothelial‐leukocyte adhesion molecule. Proc Natl Acad Sci USA 84: 9238–9242. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Bowes MP, Zivin JA, Rothlein R (1993) Monoclonal antibody to the ICAM‐1 adhesion site reduces neurological damage in a rabbit cerebral embolism stroke model. Exp Neurol 119: 215–219. [DOI] [PubMed] [Google Scholar]
- 11. Brass LF (1998) The Biochemistry of Platelet Activation. Hermostasis and Thrombosis 1176–1197.
- 12. Carvalho‐Tavares J, Fox‐Robichaud A, Kubes P (1999) Assessment of the mechanism of juxtacrine activation and adhesion of leukocytes in liver microcirculation. Am J Physiol 276: G828–834. [DOI] [PubMed] [Google Scholar]
- 13. Carvalho‐Tavares J, Kubes P (1999) Molecular mechanisms underlying leukocyte recruitment in brain microvasculature. FASEB J In Press. [Google Scholar]
- 14. Catalina MD, Carroll MC, Arizpe H, Takashima A, Estess P, Siegelman MH (1996) The route of antigen entry determines the requirement for L‐selectin during immune responses. J Exp Med 184: 2341–2351. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T (1995) Transcriptional regulation of endothelial cell adhesion molecules: NF‐ kappa B and cytokine‐inducible enhancers. FASEB J 9: 899–909. [PubMed] [Google Scholar]
- 16. Connolly ES Jr., Winfree CJ, Prestigiacomo CJ, Kim SC, Choudhri TF, Hoh BL, Naka Y, Solomon RA, Pinsky DJ (1997) Exacerbation of cerebral injury in mice that express the P‐selectin gene: identification of P‐selectin blockade as a new target for the treatment of stroke. Circ Res 81: 304–310. [DOI] [PubMed] [Google Scholar]
- 17. Connolly ES Jr., Winfree CJ, Springer TA, Naka Y, Liao H, Yan SD, Stern DM, Solomon RA, Gutierrez‐Ramos JC, Pinsky DJ (1996) Cerebral protection in homozygous null ICAM‐1 mice after middle cerebral artery occlusion. Role of neutrophil adhesion in the pathogenesis of stroke. J Clin Invest 97: 209–216. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Davenpeck KL, Gauthier TW, Albertine KH, Lefer AM (1994) Role of P‐selectin in microvascular leukocyte‐endothelial interaction in splanchnic ischemia‐reperfusion. Am J Physiol 267: H622–H630. [DOI] [PubMed] [Google Scholar]
- 19. Diamond MS, Springer TA (1994) The dynamic regulation of integrin adhesiveness. Current Biology 4: 506–517. [DOI] [PubMed] [Google Scholar]
- 20. Engelhardt B, Vestweber D, Hallmann R, Schulz R (1997) E‐ and P‐selectin are not involved in the recruitment of inflammatory cells across the blood‐brain barrier in experimental autoimmune encephalomyelitis. Blood 90: 4459–4472. [PubMed] [Google Scholar]
- 21. Eppihimer MJ, Wolitzky B, Anderson DC, Labow MA, Granger DN (1996) Heterogeneity of expression of E‐ and P‐selectins in vivo . Circ Res 79: 560–569. [DOI] [PubMed] [Google Scholar]
- 22. Gallatin WM, Weissman IL, Butcher EC (1983) A surface molecule involved in organ‐specific homing of lymphocytes. Nature 3044: 30–34. [DOI] [PubMed] [Google Scholar]
- 23. Garcia JH, Liu KF, Yoshida Y, Lian J, Chen S, del Zoppo GJ (1994) Influx of leukocytes and platelets in an evolving brain infarct (Wistar Rat). Am J Pathol 144: 188–199. [PMC free article] [PubMed] [Google Scholar]
- 24. Garcia‐Criado FJ, Toledo‐Pereyra LH, Lopez‐Neblina F, Phillips ML, Paez‐Rollys A, Misawa K (1995) Role of P‐selectin in total hepatic ischemia and reperfusion. Journal of American College of Surgeons 181: 327–334. [PubMed] [Google Scholar]
- 25. Geng J‐G, Bevilacqua MP, Moore KL, McIntyre TM, Prescott SM, Kim JM, Bliss GA, Zimmerman GA, McEver RP (1990) Rapid neutrophil adhesion to activated endothelium mediated by GMP‐140. Nature 343: 757–760. [DOI] [PubMed] [Google Scholar]
- 26. Ghosh S, May MJ, Kopp EB (1998) NF‐kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annual Review of Immunology 16: 225–260. [DOI] [PubMed] [Google Scholar]
- 27. Gipson TS, Bless NM, Shanley TP, Crouch LD, Bleavins MR, Younkin EM, Sarma V, Gibbs DF, Tefera W, McConnell PC, Mueller WT, Johnson KJ, Ward PA (1999) Regulatory effects of endogenous protease inhibitors in acute lung inflammatory injury. J Immunol 162: 3653–3662. [PubMed] [Google Scholar]
- 28. Hemler ME (1990) VLA proteins in the integrin family: structures, functions, and their role on leukocytes. Annual Review of Immunology 8: 365–400. [DOI] [PubMed] [Google Scholar]
- 29. Hickey MJ, Granger DN, Kubes P (1999) Molecular mechanisms underlying IL‐4‐induced leukocyte recruitment in vivo: a critical role for the a4 integrin. J Immunol 163: 3441–3448. [PubMed] [Google Scholar]
- 30. Hickey MJ, Kanwar S, McCafferty D‐M, Granger DN, Eppihimer MJ, Kubes P (1999) Varying roles of E‐selectin and P‐selectin in different microvascular beds in response to antigen. J Immunol 162: 1137–1143. [PubMed] [Google Scholar]
- 31. Hickey MJ, Reinhardt PH, Ostrovsky L, Jones WM, Jutila MA, Payne D, Elliott J, Kubes P (1997) Tumor necrosis factor‐a induces leukocyte recruitment by different mechanisms in vivo and in vitro . J Immunol 158: 3391–3400. [PubMed] [Google Scholar]
- 32. Hogg JC, Doerschuk CM (1995) Leukocyte traffic in the lung. Annu Rev Physiol 57: 97–114. [DOI] [PubMed] [Google Scholar]
- 33. Jaeschke H, Farhood A, Bautista AP, Spolarics Z, Spitzer JJ, Smith CW (1993) Functional inactivation of neutrophils with a Mac‐1 (CD11b/CD18) monoclonal antibody protects against ischemia‐reperfusion injury in rat liver. Hepatology 17: 915–923. [PubMed] [Google Scholar]
- 34. Jin FNCRDDA (1997) Secretory leukocyte protease inhibitor: a macrophage product induced by and antagonistic to bacterial lipopolysaccharide. Cell 88: 417–426. [DOI] [PubMed] [Google Scholar]
- 35. Jones DA, Abbassi O, McIntire LV, McEver RP, Smith CW (1993) P‐selectin mediates neutrophil rolling on histamine‐stimulated endothelial cells. Biophysical Journal 65: 1560–1569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36. Johnson KJ, Ward PA (1974) Acute immunologic pulmonary alveolitis. J Clin Invest 54: 349–357. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37. Johnston B, Issekutz TB, Kubes P (1996) The a4‐integrin supports leukocyte rolling and adhesion in chronically inflamed postcapillary venules in vivo . J Exp Med 181: 1995–2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38. Johnston B, Walter UM, Issekutz AC, Issekutz TB, Anderson DC, Kubes P (1997) Differential roles of selectins and the a4‐integrin in acute, subacute, and chronic leukocyte recruitment in vivo . J Immunol 159: 4514–4523. [PubMed] [Google Scholar]
- 39. Kanda T, Yamawaki M, Ariga T, Yu RK (1995) Interleukin 1 beta up‐regulates the expression of sulfoglucuronosyl paragloboside, a ligand for L‐selectin, in brain microvascular endothelial cells. Proc Natl Acad Sci USA 92: 7897–7901. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40. Kanwar S, Bullard DC, Hickey MJ, Smith CW, Beaudet AL, Wolitzky BA, Kubes P (1997) The association between a4‐integrin, P‐selectin, and E‐selectin in an allergic model of inflammation. J Exp Med 185: 1–11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41. Kanwar S, Johnston B, Kubes P (1995) Leukotriene C4/D4 induces P‐selectin and sialyl lewisx‐dependent alterations in leukocyte kinetics in vivo . Circ Res 77: 879–887. [DOI] [PubMed] [Google Scholar]
- 42. Kanwar S, Smith CW, Kubes P (1998) An absolute requirement for P‐selectin in ischemia/reperfusion‐induced leukocyte recruitment in cremaster muscle. Microcirculation 5: 281–287. [PubMed] [Google Scholar]
- 43. Kanwar S, Steeber DA, Tedder TF, Hickey MJ, Kubes P (1999) Overlapping roles for L‐selectin and P‐selectin in antigen‐induced immune responses in the microvasculature. J Immunol 162: 2709–2716. [PubMed] [Google Scholar]
- 44. Kanwar S, Woodman RC, Poon M‐C, Murohara T, Lefer AM, Davenpeck KL, Kubes P (1995) Desmopressin induces endothelial P‐selectin expression and leukocyte rolling in post‐capillary venules. Blood 86: 2760–2766. [PubMed] [Google Scholar]
- 45. Kubes P, Jutila M, Payne D (1995) Therapeutic potential of inhibiting leukocyte rolling in ischemia/reperfusion. J Clin Invest 95: 2510–2519. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46. Kubes P, Kanwar S (1994) Histamine induces leukocyte rolling in post‐capillary venules: A P‐selectin‐mediated event. J Immunol 152: 3570–3577. [PubMed] [Google Scholar]
- 47. Kunkel EJ, Ley K (1996) Distinct phenotype of E‐selectin‐deficient mice. E‐selectin is required for slow leukocyte rolling in vivo . Circ Res 79: 1196–1204. [DOI] [PubMed] [Google Scholar]
- 48. Lawrence MB, Springer TA (1991) Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 65: 859–873. [DOI] [PubMed] [Google Scholar]
- 49. Lawrence MB, Springer TA (1993) Neutrophils roll on E‐selectin. J Immunol 151: 6338–6346. [PubMed] [Google Scholar]
- 50. Lentsch AB, Jordan JA, Czermak BJ, Diehl KM, Younkin EM, Sarma V, Ward PA (1999) Inhibition of NF‐kappaB activation and augmentation of IkappaBbeta by secretory leukocyte protease inhibitor during lung inflammation. Am J Pathol 154: 239–247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51. Lentsch AB, Shanley TP, Sarma V, Ward PA (1997) In vivo suppression of NF‐kappa B and preservation of I kappa B alpha by interleukin‐10 and interleukin‐13. J Clin Invest 100: 2443–2448. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52. 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: 223–234. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53. Luscinskas FW, Ding H, Lichtman AH (1995) P‐selectin and vascular cell adhesion molecule 1 mediate rolling and arrest, respectively, of CD4+ T lymphocytes on tumor necrosis factor a‐activated vascular endothelium under flow. J Exp Med 181: 1179–1186. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54. Luscinskas FW, Ding H, Tan P, Cumming D, Tedder TF, Gerritsen ME (1996) L‐ and P‐selectins, but not CD49d (VLA‐4) integrins, mediate monocyte initial attachment to TNF‐a‐activated vascular endothelium under flow in vitro . J Immunol 156: 326–335. [PubMed] [Google Scholar]
- 55. Ma X‐L, Weyrich AS, Lefer DJ, Buerke M, Albertine KH, Kishimoto TK, Lefer AM (1993) Monoclonal antibody to L‐selectin attenuates neutrophil accumulation and protects ischemic reperfused cat myocardium. Circulation 88: 649–658. [DOI] [PubMed] [Google Scholar]
- 56. Matsuo Y, Onodera H, Shiga Y, Shozuhara H, Ninomiya M, Kihara T, Tamatani T, Miyasaka M, Kogure K (1994) Role of cell adhesion molecules in brain injury after transient middle cerebral artery occlusion in the rat. Brain Res 656: 344–352. [DOI] [PubMed] [Google Scholar]
- 57. Meng H, Tonnesen MG, Marchese MJ, Clark RAF, Bahou WF, Bruber BL (1995) Mast cells are potent regulators of endothelial cell adhesion molecule ICAM‐1 and VCAM‐1 expression. Journal of Cellular Physiology 165: 40–53. [DOI] [PubMed] [Google Scholar]
- 58. Mizgerd JP, Meek BB, Kutkoski GJ, Bullard DC, Beaudet AL, Doerschuk CM (1996) Selectins and neutrophil traffic: margination and Streptococcus Pneumoniae‐induced emigration in murine lungs. J Exp Med 184: 639–645. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59. Munoz FM, Hawkins EP, Bullard DC, Beaudet AL, Kaplan SL (1997) Host defense against systemic infection with Streptococcus pneumoniae is impaired in E‐, P‐, and E‐/P‐selectin‐deficient mice. J Clin Invest 100: 2099–2106. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60. Muller WA, Weigl SA, Deng X, Phillips DM (1993) PECAM‐1 is required for transendothelial migration of leukocytes. J Exp Med 178: 449–460. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61. Mulligan MS, Desrochers PE, Chinnaiyan AM, Gibbs DF, Varani J, Johnson KJ, Weiss SJ (1993) In vivo suppression of immune complex‐induced alveolitis by secretory leukoproteinase inhibitor and tissue inhibitor of metallo‐proteinases 2. Proc Natl Acad Sci USA 90: 11523–11527. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62. Mulligan MS, Miyasaka M, Tamatani T, Jones ML, Ward PA (1994) Requirements for L‐selectin in neutrophil‐mediated lung injury in rats. J Immunol 152: 832–840. [PubMed] [Google Scholar]
- 63. Mulligan MS, Vaporciyan AA, Miyasaka M, Tamatani T, Ward PA (1993) Tumor necrosis factor alpha regulates in vivo intrapulmonary expression of ICAM‐1. Am J Pathol 142: 1739–1749. [PMC free article] [PubMed] [Google Scholar]
- 64. Mulligan MS, Warner RL, Foreback JL, Shanley TP, Ward PA (1997) Protective effects of IL‐4, IL‐10, IL‐12, and IL‐13 in IgG immune complex‐induced lung injury: role of endogenous IL‐12. J Immunol 159: 3483–3489. [PubMed] [Google Scholar]
- 65. Okada Y, Copeland BR, Mori E, Tung M‐M, Thomas WS, del Zoppo GJ (1994) P‐selectin and intercellular adhesion molecule‐1 expression after focal brain ischemia and reperfusion. Stroke 25: 201–211. [DOI] [PubMed] [Google Scholar]
- 66. Olofsson AM, Arfors KE, Ranezani L, Wolitzky B, Butcher EC, Von Andrian UH (1994) E‐selectin mediates leukocyte rolling in interleukin‐1‐treated rabbit mesentery venules. Blood 84: 2749–2758. [PubMed] [Google Scholar]
- 67. Ostrovsky L, King AJ, Bond S, Mitchell D, Niu X‐F, Kubes P (1998) A juxtacrine mechanism for neutrophil adhesion on platelets involves platelet‐activating factor and a selectin‐dependent activation process. Blood 91: 3028–3036. [PubMed] [Google Scholar]
- 68. Ostrovsky L, Woodman RC, Payne D, Teoh D, Kubes P (1997) Antithrombin III prevents and rapidly reverses leukocyte recruitment in ischemia/reperfusion. Circulation 96: 2302–2310. [DOI] [PubMed] [Google Scholar]
- 69. Patel KD (1998) Eosinophil tethering to interleukin‐4‐activated endothelial cells requires both P‐selectin and vascular cell adhesion molecule‐1. Blood 92: 3904–3911. [PubMed] [Google Scholar]
- 70. Patel KD, Zimmerman GA, Prescott SM, McEver RP, McIntyre TM (1991) Oxygen radicals induce human endothelial cells to express GMP‐140 and bind neutrophils. J Cell Biol 112: 749–759. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 71. Pizcueta P, Luscinskas FW (1994) Monoclonal antibody blockade of L‐selectin inhibits mononuclear leukocyte recruitment to inflammatory sites in vivo . Am J Pathol 145: 461–469. [PMC free article] [PubMed] [Google Scholar]
- 72. Prestigiacomo CJ, Kim SC, Connolly ES, Jr. , Liao H, Yan SF, Pinsky DJ (1999) CD18‐mediated neutrophil recruitment contributes to the pathogenesis of reperfused but not nonreperfused stroke. Stroke 30: 1110–1117. [DOI] [PubMed] [Google Scholar]
- 73. Ramamoorthy C, Sharar SR, Harlan JM, Tedder TF, Winn RK (1996) Blocking L‐selectin function attenuates reperfusion injury following hemorrhagic shock in rabbits. Am J Physiol 271: H1871–H1877. [DOI] [PubMed] [Google Scholar]
- 74. Reinhardt PH, Kubes P (1998) Differential leukocyte recruitment from whole blood via endothelial adhesion molecules under shear conditions. Blood 92: 4691–4699. [PubMed] [Google Scholar]
- 75. Robinson SD, Frenette PS, Rayburn H, Cummiskey M, Ullman‐Cullere M, Wagner DD, Hynes RO (1999) Multiple, targeted deficiencies in selectins reveal a predominant role for P‐selectin in leukocyte recruitment. Proc Natl Acad Sci USA 96: 11452–11457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76. Schmid‐Schonbein GW, Usami S, Skalak R, Chien S (1980) The interaction of leukocytes and erythrocytes in capillary and postcapillary vessels. Microvasc Res 19: 45–70. [DOI] [PubMed] [Google Scholar]
- 77. Shanley TP, Schmal H, Friedl HP, Jones ML, Ward PA (1995) Regulatory effects of intrinsic IL‐10 in IgG immune complex‐induced lung injury. J Immunol 154: 3454–3460. [PubMed] [Google Scholar]
- 78. Smyth SS, Joneckis CC, Parise LV (1993) Regulation of vascular integrins. Blood 81: 2827–2843. [PubMed] [Google Scholar]
- 79. Soriano SG, Coxon A, Wang YF, Frosch MP, Lipton SA, Hickey PR, Mayadas TN (1999) Mice deficient in Mac‐1 (CD11b/CD18) are less susceptible to cerebral ischemia/reperfusion injury. Stroke 30: 134–139. [DOI] [PubMed] [Google Scholar]
- 80. Spertini O, Luscinskas FW, Kansas GS, Munro JM, Griffin JD, Gimbrone MA Jr., Tedder TF (1991) Leukocyte adhesion molecule‐1 (LAM‐1, L‐Selectin) interacts with an inducible endothelial cell ligand to support leukocyte adhesion. J Immunol 147: 2565–2573. [PubMed] [Google Scholar]
- 81. Springer TA (1995) Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu Rev Physiol 57: 827–872. [DOI] [PubMed] [Google Scholar]
- 82. Sriramarao P, Von Andrian UH, Butcher EC, Bourdon MA, Broide DH (1994) L‐selectin and very late antigen‐4 integrin promote eosinophil rolling at physiological shear rates in vivo . J Immunol 153: 4238–4246. [PubMed] [Google Scholar]
- 83. Tang T, Frenette PS, Hynes RO, Wagner DD, Mayadas TN (1996) Cytokine‐induced meningitis is dramatically attenuated in mice deficient in endothelial selectins. J Clin Invest 97: 2485–2490. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 84. Tedder TF, Steeber DA, Pizcuetta P (1995) L‐selectin‐deficient mice have impaired leukocyte recruitment into inflammatory sites. J Exp Med 181: 2259–2264. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 85. Watson SR, Fennie C, Lasky LA (1991) Neutrophil influx into an inflammatory site inhibited by a soluble homing receptor‐IgG chimaera. Nature 349: 164–167. [DOI] [PubMed] [Google Scholar]
- 86. Weber C, Springer TA (1997) Neutrophil accumulation on activated, surface‐adherent platelets in flow is mediated by interaction of Mac‐1 with fibrinogen bound to alphallbbeta3 and stimulated by platelet‐activating factor. J Clin Invest 100: 2085–2093. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 87. Weber JR, Angstwurm K, Rosenkranz T, Lindauer U, Burger W, Einhaupl KM, Dirnagl U (1997) Histamine (H1) receptor antagonist inhibits leukocyte rolling in pial vessels in the early phase of bacterial meningitis in rats. Neurosci Lett 226: 17–20. [DOI] [PubMed] [Google Scholar]
- 88. Weyrich AS, Ma X‐L, Lefer DJ, Albertine KH, Lefer AM (1993) In vivo neutralization of P‐selectin protects feline heart and endothelium in myocardial ischemia and reperfusion injury. J Clin Invest 91: 2620–2629. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 89. Wong J, Johnston B, Lee SS, Bullard DC, Smith CW, Beaudet AL, Kubes P (1997) A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J Clin Invest 99: 2782–2790. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 90. Xu J, Grewal IS, Geba GP, Flavell RA (1996) Impaired primary T cell responses in L‐selectin‐deficient mice. J Exp Med 183: 589–598. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 91. Yong T, Zheng MQ, Linthicum DS (1997) Local histamine release increases leukocyte rolling in the cerebral microcirculation of the mouse. Brain Injury 11: 765–774. [DOI] [PubMed] [Google Scholar]
- 92. Zhang RL, Chopp M, Li Y, Zaloga C, Jiang N, Jones ML, Miyasaka M, Ward PA (1994) Anti‐ICAM‐1 antibody reduces ischemic cell damage after transient middle cerebral artery occlusion in the rat. Neurology 44: 1747–1751. [DOI] [PubMed] [Google Scholar]
- 93. Zimmerman BJ, Paulson JC, Arrhenius TS, Gaeta FCA, Granger DN (1994) Thrombin receptor peptide‐mediated leukocyte rolling in rat mesenteric venules: roles of P‐selectin and sialyl Lewis X. Am J Physiol 267: H1049–H1053. [DOI] [PubMed] [Google Scholar]