logo

SCIENCE CHINA Life Sciences, Volume 59 , Issue 3 : 299-311(2016) https://doi.org/10.1007/s11427-015-4986-1

Platelet-mediated adhesion facilitates leukocyte sequestration in hypoxia-reoxygenated microvessels

More info
  • ReceivedAug 30, 2015
  • AcceptedSep 24, 2015
  • PublishedJan 15, 2016

Abstract


Funded by

Natural Science Foundation of Beijing City(7092093)


Acknowledgment

Acknowledgements This work was supported by the Natural Science Foundation of Beijing City (7092093).


Open access

Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and source are credited


Interest statement

Compliance and ethics The author(s) declare that they have no conflict of interest.


References

[1] Alcaide P., Newton G., Auerbach S., Sehrawat S., Mayadas T.N., Golan D.E., Yacono P., Vincent P., Kowalczyk A., Luscinskas F.W.. p120-Catenin regulates leukocyte transmigration through an effect on VE-cadherin phosphorylation. Blood, 2008, 112: 2770-2779 CrossRef PubMed Google Scholar

[2] Carvalho-Tavares J., Hickey M.J., Hutchison J., Michaud J., Sutcliffe I.T., Kubes P.. A role for platelets and endothelial selectins in tumor necrosis factor-α–induced leukocyte recruitment in the brain microvasculature. Circ Res, 2000, 87: 1141-1148 CrossRef PubMed Google Scholar

[3] Coito A.J.. Leukocyte transmigration across endothelial and extracellular matrix protein barriers in liver ischemia/reperfusion injury. Curr Opin Organ Transplant, 2011, 16: 34-40 CrossRef PubMed Google Scholar

[4] Coltel N., Combes V., Hunt N., Grau G.. Cerebral malaria - A neurovascular pathology with many riddles still to be solved. CNR, 2004, 1: 91-110 CrossRef Google Scholar

[5] Compston A., Coles A.. Multiple sclerosis. Lancet, 2008, 372: 1502-1517 CrossRef Google Scholar

[6] Martins P.A.C., van Gils J.M., Mol A., Hordijk P.L., Zwaginga J.J.. Platelet binding to monocytes increases the adhesive properties of monocytes by up-regulating the expression and functionality of β1 and β2 integrins. J Leukocyte Biol, 2006, 79: 499-507 CrossRef PubMed Google Scholar

[7] Diacovo T.G., Puri K.D., Warnock R.A., Springer T.A., von Andrian U.H.. Platelet-mediated lymphocyte delivery to high endothelial venules. Science, 1996a, 273: 252-255 CrossRef PubMed ADS Google Scholar

[8] Diacovo, T.G., Roth, S.J., Buccola, J.M., Bainton, D.F., and Springer, T.A. (1996b). Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the beta 2-integrin CD11b/CD18. Blood 88, 146–157. Google Scholar

[9] Dixon D.A., Tolley N.D., Bemis-Standoli K., Martinez M.L., Weyrich A.S., Morrow J.D., Prescott S.M., Zimmerman G.A.. Expression of COX-2 in platelet-monocyte interactions occurs via combinatorial regulation involving adhesion and cytokine signaling. J Clin Investigation, 2006, 116: 2727-2738 CrossRef Google Scholar

[10] Duilio C., Ambrosio G., Kuppusamy P., DiPaula A., Becker L.C., Zweier J.L.. Neutrophils are primary source of O2 radicals during reperfusion after prolonged myocardial ischemia. Am J Physiol-Heart Circulatory Physiol, 2001, 280: H2649-H2657 CrossRef PubMed Google Scholar

[11] Dulkanchainun T.S., Goss J.A., Imagawa D.K., Shaw G.D., Anselmo D.M., Kaldas F., Wang T., Zhao D., Busuttil A.A., Kato H., et al. Reduction of hepatic ischemia/reperfusion injury by a soluble P-selectin glycoprotein ligand-1. Ann Surgery, 1998, 227: 832-840 CrossRef PubMed Google Scholar

[12] Francischetti I., Moreno J.B., Scholz M., Yoshida W.B.. Os leucócitos e a resposta inflamatória na lesão de isquemia-reperfusão. Rev Bras Cir Cardiovasc, 2010, 25: 575-584 CrossRef PubMed Google Scholar

[13] Garcia-Criado, F.J., Toledo-Pereyra, L.H., Lopez-Neblina, F., Phillips, M.L., Paez-Rollys, A., and Misawa, K. (1995). Role of P-selectin in total hepatic ischemia and reperfusion. J Am Coll Surg 181, 327–334. Google Scholar

[14] Grau, G.E., Tacchini-Cottier, F., Vesin, C., Milon, G., Lou, J.N., Piguet, P.F., and Juillard, P. (1993). TNF-induced microvascular pathology: active role for platelets and importance of the LFA-1/ICAM-1 interaction. Eur Cytokine Netw 4, 415–419. Google Scholar

[15] Huo Y., Schober A., Forlow S.B., Smith D.F., Hyman M.C., Jung S., Littman D.R., Weber C., Ley K.. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat Med, 2003, 9: 61-67 CrossRef PubMed Google Scholar

[16] Kaul S.. The “no reflow” phenomenon following acute myocardial infarction: Mechanisms and treatment options. J Cardiology, 2014, 64: 77-85 CrossRef PubMed Google Scholar

[17] Kuijper, P.H., Gallardo Torres, H.I., van der Linden, J.A., Lammers, J.W., Sixma, J.J., Koenderman, L., and Zwaginga, J.J. (1996). Platelet-dependent primary hemostasis promotes selectin- and integrin-mediated neutrophil adhesion to damaged endothelium under flow conditions. Blood 87, 3271–3281. Google Scholar

[18] Lehr H.A.. Microcirculatory dysfunction induced by cigarette smoking. Microcirculation, 2000, 7: 367-384 CrossRef Google Scholar

[19] Lou, J., Donati, Y.R., Juillard, P., Giroud, C., Vesin, C., Mili, N., and Grau, G.E. (1997). Platelets play an important role in TNF-induced microvascular endothelial cell pathology. Am J Pathol 151, 1397–1405. Google Scholar

[20] Lou J.N., Mili N., Decrind C., Donati Y., Kossodo S., Spiliopoulos A., Ricou B., Suter P.M., Morel D.R., Morel P., et al. An improved method for isolation of microvascular endothelial cells from normal and inflamed human lung. In Vitro CellDevBiol-anim, 1998, 34: 529-536 CrossRef PubMed Google Scholar

[21] Maroszynska, I., and Fiedor, P. (2000). Leukocytes and endothelium interaction as rate limiting step in the inflammatory response and a key factor in the ischemia-reperfusion injury. Ann Transplant 5, 5–11. Google Scholar

[22] May A.E., Langer H., Seizer P., Bigalke B., Lindemann S., Gawaz M.. Platelet-leukocyte interactions in inflammation and atherothrombosis. Semin Thromb Hemost, 2007, 33: 123-127 CrossRef PubMed Google Scholar

[23] Mehta S.R., Bassand J.P., Chrolavicius S., Diaz R., Fox K.A.A., Granger C.B., Jolly S., Rupprecht H.J., Widimsky P., Yusuf S.. Design and rationale of CURRENT-OASIS 7: A randomized, 2 × 2 factorial trial evaluating optimal dosing strategies for clopidogrel and aspirin in patients with ST and non–ST-elevation acute coronary syndromes managed with an early invasive strategy. Am Heart J, 2008, 156: 1080-1088.e1 CrossRef PubMed Google Scholar

[24] Muller W.A.. Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol Mech Dis, 2011, 6: 323-344 CrossRef PubMed Google Scholar

[25] Muller W.A.. Getting leukocytes to the site of inflammation. Vet Pathol, 2013, 50: 7-22 CrossRef PubMed Google Scholar

[26] Niccoli G., Spaziani C., Marino M., Pontecorvo M.L., Cosentino N., Bacà M., Porto I., Leone A.M., Crea F.. Effect of chronic Aspirin therapy on angiographic thrombotic burden in patients admitted for a first ST-elevation myocardial infarction. Am J Cardiology, 2010, 105: 587-591 CrossRef PubMed Google Scholar

[27] Pai S., Qin J., Cavanagh L., Mitchell A., El-Assaad F., Jain R., Combes V., Hunt N.H., Grau G.E.R., Weninger W., et al. Real-time imaging reveals the dynamics of leukocyte behaviour during experimental cerebral malaria pathogenesis. PLoS Pathog, 2014, 10: e1004236 CrossRef PubMed Google Scholar

[28] Pak S., Kondo T., Nakano Y., Murata S., Fukunaga K., Oda T., Sasaki R., Ohkohchi N.. Platelet adhesion in the sinusoid caused hepatic injury by neutrophils after hepatic ischemia reperfusion. Platelets, 2010, 21: 282-288 CrossRef PubMed Google Scholar

[29] Piccardoni P., Sideri R., Manarini S., Piccoli A., Martelli N., de Gaetano G., Cerletti C., Evangelista V.. Platelet/polymorphonuclear leukocyte adhesion: a new role for SRC kinases in Mac-1 adhesive function triggered by P-selectin. Blood, 2001, 98: 108-116 CrossRef PubMed Google Scholar

[30] Ritter L.S., Stempel K.M., Coull B.M., McDonagh P.F.. Leukocyte-platelet aggregates in rat peripheral blood after ischemic stroke and reperfusion. Biol Res Nursing, 2005, 6: 281-288 CrossRef PubMed Google Scholar

[31] Ruggeri Z.M., Mendolicchio G.L.. Adhesion mechanisms in platelet function. Circ Res, 2007, 100: 1673-1685 CrossRef PubMed Google Scholar

[32] Ruggeri Z.M., Orje J.N., Habermann R., Federici A.B., Reininger A.J.. Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood, 2006, 108: 1903-1910 CrossRef PubMed Google Scholar

[33] Salmon P., Oberholzer J., Occhiodoro T., Morel P., Lou J., Trono D.. Reversible immortalization of human primary cells by lentivector-mediated transfer of specific genes. Mol Ther, 2000, 2: 404-414 CrossRef PubMed Google Scholar

[34] Shaw S.K., Ma S., Kim M.B., Rao R.M., Hartman C.U., Froio R.M., Yang L., Jones T., Liu Y., Nusrat A., et al. Coordinated redistribution of leukocyte LFA-1 and endothelial cell ICAM-1 accompany neutrophil transmigration. J Exp Med, 2004, 200: 1571-1580 CrossRef PubMed Google Scholar

[35] Sindram D., Porte R.J., Hoffman M.R., Bentley R.C., Clavien P.A.. Synergism between platelets and leukocytes in inducing endothelial cell apoptosis in the cold ischemic rat liver: a Kupffer cell-mediated injury. FASEB J, 2001, 15: 1230-1232 CrossRef PubMed Google Scholar

[36] Sternlicht M.D., Werb Z.. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol, 2001, 17: 463-516 CrossRef Google Scholar

[37] Tsuchihashi S., Fondevila C., Shaw G.D., Lorenz M., Marquette K., Benard S., Shen X.D., Ke B., Busuttil R.W., Kupiec-Weglinski J.W.. Molecular characterization of rat leukocyte P-selectin glycoprotein ligand-1 and effect of its blockade: protection from ischemia-reperfusion injury in liver transplantation. J Immunol, 2006, 176: 616-624 CrossRef Google Scholar

[38] Weyrich A.S., Elstad M.R., McEver R.P., McIntyre T.M., Moore K.L., Morrissey J.H., Prescott S.M., Zimmerman G.A.. Activated platelets signal chemokine synthesis by human monocytes.. J Clin Invest, 1996, 97: 1525-1534 CrossRef PubMed Google Scholar

[39] Wojcik J.D., Van Horn D.L., Webber A.J., Johnson S.A.. Mechanism whereby platelets support the endothelium. Transfusion, 1969, 9: 324-336 CrossRef PubMed Google Scholar

[40] Wong J., Johnston B., Lee S.S., Bullard D.C., Smith C.W., Beaudet A.L., Kubes P.. A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature.. J Clin Invest, 1997, 99: 2782-2790 CrossRef PubMed Google Scholar

[41] Wu L.Q., Zhang W.J., Niu J.X., Ye L.Y., Yang Z.H., Grau G.E., Lou J.N.. Phenotypic and functional differences between human liver cancer endothelial cells and liver sinusoidal endothelial cells. J Vasc Res, 2008, 45: 78-86 CrossRef PubMed Google Scholar

[42] Yang H., Majno P., Morel P., Toso C., Triponez F., Oberholzer J., Mentha G., Lou J.. Prostaglandin E1 protects human liver sinusoidal endothelial cell from apoptosis induced by hypoxia reoxygenation. Microvascular Res, 2002, 64: 94-103 CrossRef PubMed Google Scholar

[43] Yang L., Kowalski J.R., Zhan X., Thomas S.M., Luscinskas F.W.. Endothelial cell cortactin phosphorylation by Src contributes to polymorphonuclear leukocyte transmigration in vitro. Circ Res, 2006, 98: 394-402 CrossRef PubMed Google Scholar

[44] Zabel B.A., Rott A., Butcher E.C.. Leukocyte chemoattractant receptors in human disease pathogenesis. Annu Rev Pathol Mech Dis, 2015, 10: 51-81 CrossRef PubMed Google Scholar

[45] Zhang, B.H., Zhang, W.J., Lou, J.N., and Li, C.H. (2010a). Morphologic and functional characteristics of the immortalized human liver sinusoidal endothelial cell line. Zhonghua Wai Ke Za Zhi 48, 48–52. Google Scholar

[46] Zhang W., Feng J., Zhou R., Ye L., Liu H., Peng L., Lou J., Li C.. Tanshinone IIA protects the human blood–brain barrier model from leukocyte-associated hypoxia-reoxygenation injury. Eur J Pharmacol, 2010b, 648: 146-152 CrossRef PubMed Google Scholar

  • Figure 1

    The effects of platelets on leukocyte adhesion to ECs after hypoxia-reoxygenation (H-R). A, Observation of the adhesion of BCECF-labeled- leukocytes to human brain endothelial cells (HBECs), human lung endothelial cells (HLECs) and liver sinusoidal endothelial cells (LSECs) under a fluorescence microscope (×100; green fluorescence denoted leukocytes and PLT indicated platelet). B, The fluorescence intensity of the adherent leukocytes (**, P<0.01, the H-R group versus the resting group; ##, P<0.01, the H-R (PLT) group versus the H-R group; n=3). C, The effects of the adhesion molecule blockade on the adhesion of leukocytes to ECs without platelets after H-R (**, P<0.01, the antibody group versus the IgG group; n=3). D, The effects of the adhesion molecule blockade on the adhesion of leukocytes to ECs with platelet pre-incubation after H-R (**, P<0.01, the antibody group versus the IgG group; n=3).

  • Figure 2

    The platelet adhesion to LSECs or leukocytes after H-R. A, The adhesion of BCECF-labeled-platelets to a confluent LSEC monolayer observed by a fluorescence microscope (×100; green fluorescence denoted platelets). B, The fluorescence intensity of the adherent platelets (**, P<0.01 compared with the resting group; n=3). C, The flow cytometry analysis of the adherent BCECF-labeled platelets to leukocytes after H-R. The leukocytes without platelet incubation were employed as a negative control. D, The mean fluorescence intensity of the adherent BCECF- labeled platelets to leukocytes after H-R (**,P<0.01 compared with the resting group; n=3). E, The effects of the adhesion molecule blockade on the adhesion of platelets to LSECs after H-R (**, P<0.01, the antibody group versus the IgG group; n=3). F, The effects of the adhesion molecule blockade on the adhesion of platelets to leukocytes after H-R (**, P<0.01, the antibody group versus the IgG group; n=3).

  • Figure 3

    The morphological evidences for leukocyte adhesion to ECs. A, Observation of the leukocyte adhesion to LSEC under a laser scanning confocal microscope after H-R (×1,800). The platelets were labeled with CM-DiI (red) and the leukocytes were labeled with BCECF (green). B, Quantification of the adherent leukocytes to a single LSEC (**, P<0.01 compared with the H-R group; n=5). C, Ratio of the direct adherent leukocytes to the total adherent leukocytes (**, P< 0.01 compared with the H-R group; n=5). D, The transmission electron microscope images of the leukocyte adhesion to LSEC after H-R (×8,000).

  • Figure 4

    The effects of platelets on leukocyte TEM after H-R. A, Observation of the transmigrated leukocytes through the endothelial cell layer under a fluorescence microscope (×100; green fluorescence denoted leukocytes). B, Quantification of the fluorescence intensity of the transmigrated leukocytes (**, P<0.01, the H-R group versus the resting group; ##, P<0.01, the H-R (PLT) group versus the H-R group; n=3). C, The effects of the adhesion molecule blockade on leukocyte TEM without platelets after H-R (*, P<0.05; **, P<0.01, the antibody group versus the IgG group; n=3). D, The effects of the adhesion molecule blockade on leukocyte TEM with platelet pre-incubation after H-R (*, P<0.05; **, P<0.01, the antibody group versus the IgG group; n=3).

  • Figure 5

    The effects of platelets on leukocyte adhesion and TEM in ischemic-reperfused vessels in vivo. The leukocytes were labeled with green fluorescent dye BCECF, and the platelets were labeled with red fluorescent dye CM-DiI. The H-R-treated leukocytes incubated with or without platelets were injected into the jejunal artery after one of its branches suffered ischemia for 30 min. A, In the acute model (10 min after the transfusion), the leukocyte or platelet distribution was demonstrated by green or red fluorescence in the normoxia or ischemia-reperfused area (n=10). B, In the subacute model (12 h after the transfusion), the leukocyte or platelet distribution was demonstrated by green or red fluorescence in the normoxia or ischemia-reperfused area (n=10).

  • Figure 6

    A schematic diagram of the influence of platelets on leukocyte TEM and sequestration. Under the H-R condition without platelets, the leukocytes adhered to ECs and subsequently transmigrated through the endothelium. Under the H-R condition with platelets, the leukocyte adhesion was enhanced, but the leukocyte TEM was suppressed, leading to leukocyte sequestration in hypoxia-reoxygenated microvessels.

qqqq

Contact and support