大鼠脑缺血再灌注中电针治疗对Annexin A1的调节作用
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摘要
目的探讨Annexin A1在脑缺血再灌注损伤中的地位,电针治疗脑中风的作用机制与其的相关性。
方法将SD大鼠随机分成正常对照组、缺血再灌组、电针治疗组、DMSO对照组和TrkA抑制组五组,以线栓法建立大鼠大脑中动脉栓塞再灌注模型,电针穴位选择“水沟”、“承浆”穴。运用侧脑室注射特异性酪氨酸激酶抑制剂K252a抑制TrkA的作用,用免疫组化方法检测Annexin A1在大鼠海马组织中的表达变化以及核转位结果。
结果(1)在海马CA1区,脑缺血再灌组与正常对照组相比,Annexin A1的表达升高35.44%(P<0.05)。电针治疗组与脑缺血再灌组相比,Annexin A1的表达水平下降18.96%(P<0.05);在海马CA3区,脑缺血再灌组与正常对照组相比,Annexin A1的表达升高上升44.24%(P<0.05)。电针治疗组与脑缺血再灌组相比,Annexin A1的表达水平下降21.80%(P<0.05)。(2)抑制TrkA后进行电针治疗,在海马CA1区与DMSO组相比,K252a组Annexin A1的表达水平下降了12.20%(P<0.05),而在海马CA3区,K252a组Annexin A1的表达水平上升9.30%(P<0.05)。(3)在海马CA3区,脑缺血再灌组与正常对照组相比,Annexin A1在胞核上表达增加(P<0.05),电针治疗组与缺血再灌组相比降低了( P<0.05),在其他分组和分区中未见显著性差异。
结论:脑缺血再灌注后Annexin A1表达上调,电针治疗能够逆转Annexin A1表达,并且在海马CA3区通过TrkA途径来调整Annexin A1的作用。脑缺血再灌注后Annexin A1出现核转位现象,电针可以逆转Annexin A1的核转位。电针有可能通过调节Annexin A1的核转位来改变神经元的凋亡命运。
Objective: To explorer the role that Annexin A1 play in the brain ischemia reperfusion, and to observe the mechanism and the possible pathway that electroacupuncture therapy stroke.
Methods: S-D male rat was randomized into normal control group, ischemia reperfusion group, electroacupuncture treatment group, DMSO control group, TrkA inhibitor group. MACO model was established by thread embolism. SABC immunohistochemistry was applied to measure the expression change of Annexin A1 in the hippocampus tissue of rat brain. Anatomical points of Shuigou and Chengjiang were selected.K252a, a special tyrosine kinase inhibitor, was used by lateral cerebral ventricle injection to inhibit TrkA.
Result (1)In the CA1 region of hippocampus, the expression of Annexin A1 in the ischemia reperfusion group is higher 35.44% than that in the normal control group(P<0.05). The expression of Annexin A1 in the electroacupuncture therapy group is lower 18.96% than in the ischemia reperfusion group(P<0.05); In the CA3 region of hippocampus, the expression of Annexin A1 in the ischemia reperfusion group is higher 44.24% than that in the normal control group(P<0.05). The expression of Annexin A1 in the electroacupuncture therapy group is lower 21.80% than in the ischemia reperfusion group(P<0.05).(2)After TrkA inhibition, in the CA1 region of hippocampus, the expression of Annexin A1 in the K252a group is lower 12.20% than that in the DMSO group(P<0.05). However in the CA3 of hippocampus, the expression of Annexin A1 in the K252a group is higher 9.30% than that in the DMSO group (P<0.05). (3)In the CA3 region of hippocampus, the nuclear expression of Annexin A1 in the ischemia reperfusion group is higher than that in the normal control group(P<0.05) The nuclear expression of Annexin A1 in the electroacupuncture therapy group is lower than in the ischemia reperfusion group(P<0.05).
Conclusion: After brain ischemia reperfusion, Annexin A1 expression increase. Electroacupucture can decrease the expression of Annexin A1, electroacupuncture may play a role in the stroke through TrkA to regulate the anti- inflammation function of Annexin A1. And after brain ischemia reperfusion, the nuclear transloction ratio increase, electroacupuncture can reverse the phenomena. Electroacupuncture may alter the fate of neuron apoptosis through the regulation of nuclear transloction of Annexin A1.
方法将SD大鼠随机分成正常对照组、缺血再灌组、电针治疗组、DMSO对照组和TrkA抑制组五组,以线栓法建立大鼠大脑中动脉栓塞再灌注模型,电针穴位选择“水沟”、“承浆”穴。运用侧脑室注射特异性酪氨酸激酶抑制剂K252a抑制TrkA的作用,用免疫组化方法检测Annexin A1在大鼠海马组织中的表达变化以及核转位结果。
结果(1)在海马CA1区,脑缺血再灌组与正常对照组相比,Annexin A1的表达升高35.44%(P<0.05)。电针治疗组与脑缺血再灌组相比,Annexin A1的表达水平下降18.96%(P<0.05);在海马CA3区,脑缺血再灌组与正常对照组相比,Annexin A1的表达升高上升44.24%(P<0.05)。电针治疗组与脑缺血再灌组相比,Annexin A1的表达水平下降21.80%(P<0.05)。(2)抑制TrkA后进行电针治疗,在海马CA1区与DMSO组相比,K252a组Annexin A1的表达水平下降了12.20%(P<0.05),而在海马CA3区,K252a组Annexin A1的表达水平上升9.30%(P<0.05)。(3)在海马CA3区,脑缺血再灌组与正常对照组相比,Annexin A1在胞核上表达增加(P<0.05),电针治疗组与缺血再灌组相比降低了( P<0.05),在其他分组和分区中未见显著性差异。
结论:脑缺血再灌注后Annexin A1表达上调,电针治疗能够逆转Annexin A1表达,并且在海马CA3区通过TrkA途径来调整Annexin A1的作用。脑缺血再灌注后Annexin A1出现核转位现象,电针可以逆转Annexin A1的核转位。电针有可能通过调节Annexin A1的核转位来改变神经元的凋亡命运。
Objective: To explorer the role that Annexin A1 play in the brain ischemia reperfusion, and to observe the mechanism and the possible pathway that electroacupuncture therapy stroke.
Methods: S-D male rat was randomized into normal control group, ischemia reperfusion group, electroacupuncture treatment group, DMSO control group, TrkA inhibitor group. MACO model was established by thread embolism. SABC immunohistochemistry was applied to measure the expression change of Annexin A1 in the hippocampus tissue of rat brain. Anatomical points of Shuigou and Chengjiang were selected.K252a, a special tyrosine kinase inhibitor, was used by lateral cerebral ventricle injection to inhibit TrkA.
Result (1)In the CA1 region of hippocampus, the expression of Annexin A1 in the ischemia reperfusion group is higher 35.44% than that in the normal control group(P<0.05). The expression of Annexin A1 in the electroacupuncture therapy group is lower 18.96% than in the ischemia reperfusion group(P<0.05); In the CA3 region of hippocampus, the expression of Annexin A1 in the ischemia reperfusion group is higher 44.24% than that in the normal control group(P<0.05). The expression of Annexin A1 in the electroacupuncture therapy group is lower 21.80% than in the ischemia reperfusion group(P<0.05).(2)After TrkA inhibition, in the CA1 region of hippocampus, the expression of Annexin A1 in the K252a group is lower 12.20% than that in the DMSO group(P<0.05). However in the CA3 of hippocampus, the expression of Annexin A1 in the K252a group is higher 9.30% than that in the DMSO group (P<0.05). (3)In the CA3 region of hippocampus, the nuclear expression of Annexin A1 in the ischemia reperfusion group is higher than that in the normal control group(P<0.05) The nuclear expression of Annexin A1 in the electroacupuncture therapy group is lower than in the ischemia reperfusion group(P<0.05).
Conclusion: After brain ischemia reperfusion, Annexin A1 expression increase. Electroacupucture can decrease the expression of Annexin A1, electroacupuncture may play a role in the stroke through TrkA to regulate the anti- inflammation function of Annexin A1. And after brain ischemia reperfusion, the nuclear transloction ratio increase, electroacupuncture can reverse the phenomena. Electroacupuncture may alter the fate of neuron apoptosis through the regulation of nuclear transloction of Annexin A1.
引文
1. Gerke V, Moss SE: Annexins: from structure to function. Physiol Rev 2002, 82(2):331-371.
2. Rhee HJ, Kim GY, Huh JW, Kim SW, Na DS: Annexin I is a stress protein induced by heat, oxidative stress and a sulfhydryl-reactive agent. Eur J Biochem 2000, 267(11):3220-3225.
3. Ferlazzo V, D'Agostino P, Milano S, Caruso R, Feo S, Cillari E, Parente L: Anti-inflammatory effects of annexin-1: stimulation of IL-10 release and inhibition of nitric oxide synthesis. Int Immunopharmacol 2003, 3(10-11):1363-1369.
4. Angeles TS, Yang SX, Steffler C, Dionne CA: Kinetics of trkA tyrosine kinase activity and inhibition by K-252a. Arch Biochem Biophys 1998, 349(2):267-274.
5. Relton JK, Strijbos PJ, O'Shaughnessy CT, Carey F, Forder RA, Tilders FJ, Rothwell NJ: Lipocortin-1 is an endogenous inhibitor of ischemic damage in the rat brain. J Exp Med 1991, 174(2):305-310.
6. Rosengarth A, Luecke H: A calcium-driven conformational switch of the N-terminal and core domains of annexin A1. J Mol Biol 2003, 326(5):1317-1325.
7. Hwang IK, Lee KY, Yoo KY, Kim DS, Lee NS, Jeong YG, Kang TC, Han BH, Kim JS, Won MH: Tyrosine kinase A but not phosphacan/protein tyrosine phosphatase- zeta/beta immunoreactivity and protein level changes in neurons and astrocytes in the gerbil hippocampus proper after transient forebrain ischemia. Brain Res 2005, 1036(1-2):35-41.
8. Debret R, El Btaouri H, Duca L, Rahman I, Radke S, Haye B, Sallenave JM, Antonicelli F: Annexin A1 processing is associated with caspase-dependent apoptosis in BZR cells. FEBS Lett 2003, 546(2-3):195-202.
9. Dorovkov MV, Ryazanov AG: Phosphorylation of annexin I by TRPM7 channel-kinase. J Biol Chem 2004, 279(49):50643-50646.
10. Touyz RM, He Y, Montezano AC, Yao G, Chubanov V, Gudermann T, Callera GE: Differential regulation of transient receptor potential melastatin 6 and 7 cation channels by ANG II in vascular smooth muscle cells from spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 2006, 290(1):R73-78.
11. Zhao L, Shi J, Sun N, Tian S, Meng X, Liu X, Li L: Effect of electroacupuncture on TRPM7 mRNA expression after cerebral ischemia/reperfusion in rats via TrkA pathway. J Huazhong Univ Sci Technolog Med Sci 2005, 25(3):247-250.
12. Kim YS, Ko J, Kim IS, Jang SW, Sung HJ, Lee HJ, Lee SY, Kim Y, Na DS: PKCdelta-dependent cleavage and nuclear translocation of annexin A1 by phorbol
12-myristate 13-acetate. Eur J Biochem 2003, 270(20):4089-4094.
13. Ishido M: Overexpression of Bcl-2 inhibits nuclear localization of annexin I during tumor necrosis factor-alpha-mediated apoptosis in porcine renal LLC-PK1 cells. Regul Pept 2005, 124(1-3):45-51.
14.张京钟,施静,刘晓春,张静,关新民,王才源:电针对大鼠局灶性脑缺血后脑内Bax,Bcl-2表达的影响.中国组织化学与细胞化学杂志2001(01).
1 Gerke V, Moss SE. Annexins: from structure to function. Physiol Rev, 2002; 82(2):331-71.
2 Rescher U, Gerke V. Annexins--unique membrane binding proteins with diverse functions. J Cell Sci, 2004;117(Pt 13):2631-9.
3 Dorovkov MV, Ryazanov AG. Phosphorylation of annexin I by TRPM7 channel-kinase. J Biol Chem, 2004;279(49):50643-6.
4 Rosengarth A, Luecke H. A calcium-driven conformational switch of the N-terminal and core domains of annexin A1. J Mol Biol, 2003;326(5):1317-25.
5 Taylor AD, Cowell AM, Flower J, et al. Lipocortin 1 mediates an early inhibitory action of glucocorticoids on the secretion of ACTH by the rat anterior pituitary gland in vitro. Neuroendocrinology, 1993;58(4):430-9.
6 Fava RA, McKanna J, Cohen S. Lipocortin I (p35) is abundant in a restricted number of differentiated cell types in adult organs. J Cell Physiol, 1989;141(2):284-93.
7 Dreier R, Schmid KW, Gerke V, et al. Differential expression of annexins I, II and IV in human tissues: an immunohistochemical study. Histochem Cell Biol, 1998; 110(2):137-48.
8 Peers SH, Smillie F, Elderfield AJ, et al. Glucocorticoid-and non-glucocorticoid induction of lipocortins (annexins) 1 and 2 in rat peritoneal leucocytes in vivo. Br J Pharmacol, 1993;108(1):66-72.
9 Traverso V, Morris JF, Flower RJ, et al. Lipocortin 1 (annexin 1) in patches associated with the membrane of a lung adenocarcinoma cell line and in the cell cytoplasm. J Cell Sci, 1998;111 ( Pt 10):1405-18.
10 Perretti M, Christian H, Wheller SK, et al. Annexin I is stored within gelatinase granules of human neutrophil and mobilized on the cell surface upon adhesion but not phagocytosis. Cell Biol Int, 2000;24(3):163-74.
11 Perretti M, Croxtall JD, Wheller SK, et al. Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration. Nat Med, 1996;2(11):1259-62.
12 Oliani SM, Paul-Clark MJ, Christian HC, et al. Neutrophil interaction with inflamed postcapillary venule endothelium alters annexin 1 expression. Am J Pathol, 2001;158(2):603-15.
13 Vergnolle N, Comera C, Bueno L. Annexin 1 is overexpressed and specifically secreted during experimentally induced colitis in rats. Eur J Biochem, 1995;232(2):603-10.
14 Perretti M, Wheller SK, Flower RJ, et al. Modulation of cellular annexin I in human leukocytes infiltrating DTH skin reactions. J Leukoc Biol, 1999;65(5):583-9.
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22 Perretti M, Ingegnoli F, Wheller SK, et al. Annexin 1 modulates monocyte-endothelial cell interaction in vitro and cell migration in vivo in the human SCID mouse transplantation model. J Immunol, 2002;169(4):2085-92.
23 Alldridge LC, Harris HJ, Plevin R, et al. The annexin protein lipocortin 1 regulates the MAPK/ERK pathway. J Biol Chem, 1999;274(53):37620-8.
24 Sudlow AW, Carey F, Forder R, et al. The role of lipocortin-1 in dexamethasone-induced suppression of PGE2 and TNF alpha release from human peripheral blood mononuclear cells. Br J Pharmacol, 1996;117(7):1449-56.
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28 Gold R, Pepinsky RB, Zettl UK, et al. Lipocortin-1 (annexin-1) suppresses activation of autoimmune T cell lines in the Lewis rat. J Neuroimmunol, 1996;69(1-2):157-64.
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30 Goulding NJ, Ogbourn S, Pipitone N, et al. The inhibitory effect of dexamethasone on lymphocyte adhesion molecule expression and intercellular aggregation is not mediated by lipocortin 1. Clin Exp Immunol, 1999;118(3):376-83.
31 Raynal P, van Bergen en Henegouwen PM, Hullin F, et al. Morphological and biochemical evidence for partial nuclear localization of annexin 1 in endothelial cells.Biochem Biophys Res Commun, 1992;186(1):432-9.
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34 Solito E, Romero IA, Marullo S, et al. Annexin 1 binds to U937 monocytic cells and inhibits their adhesion to microvascular endothelium: involvement of the alpha 4 beta 1 integrin. J Immunol, 2000;165(3):1573-81.
35 Srikrishna G, Panneerselvam K, Westphal V, et al. Two proteins modulating transendothelial migration of leukocytes recognize novel carboxylated glycans on endothelial cells. J Immunol, 2001;166(7):4678-88.
36 Strausbaugh HJ, Rosen SD. A potential role for annexin 1 as a physiologic mediator of glucocorticoid-induced L-selectin shedding from myeloid cells. J Immunol, 2001;166(10):6294-300.
37 de Coupade C, Solito E, Levine JD. Dexamethasone enhances interaction of endogenous annexin 1 with L-selectin and triggers shedding of L-selectin in the monocytic cell line U-937. Br J Pharmacol, 2003;140(1):133-45.
38 Ferlazzo V, D'Agostino P, Milano S, et al. Anti-inflammatory effects of annexin-1: stimulation of IL-10 release and inhibition of nitric oxide synthesis. Int Immunopharmacol, 2003;3(10-11):1363-9.
39 Perretti M, Chiang N, La M, et al. Endogenous lipid- and peptide-derived anti-inflammatory pathways generated with glucocorticoid and aspirin treatment activate the lipoxin A4 receptor. Nat Med, 2002;8(11):1296-302.
40 Walther A, Riehemann K, Gerke V. A novel ligand of the formyl peptide receptor: annexin I regulates neutrophil extravasation by interacting with the FPR. Mol Cell, 2000;5(5):831-40.
41 Gavins FN, Yona S, Kamal AM, et al. Leukocyte antiadhesive actions of annexin 1: ALXR- and FPR-related anti-inflammatory mechanisms. Blood, 2003;101(10):4140-7.
42 Arur S, Uche UE, Rezaul K, et al. Annexin I is an endogenous ligand that mediates apoptotic cell engulfment. Dev Cell, 2003;4(4):587-98.
43 Ishido M. Overexpression of Bcl-2 inhibits nuclear localization of annexin I during tumor necrosis factor-alpha-mediated apoptosis in porcine renal LLC-PK1 cells. Regul Pept, 2005;124(1-3):45-51.
44 Kim YS, Ko J, Kim IS, et al. PKCdelta-dependent cleavage and nuclear translocation of annexin A1 by phorbol 12-myristate 13-acetate. Eur J Biochem, 2003;270(20):4089-94.
45 Litt MR, Jeremy RW, Weisman HF, et al. Neutrophil depletion limited to reperfusion reduces myocardial infarct size after 90 minutes of ischemia. Evidence for neutrophil-mediated reperfusion injury. Circulation, 1989;80(6):1816-27.
46 Poon BY, Ward CA, Cooper CB, et al. alpha(4)-integrin mediates neutrophil-induced free radical injury to cardiac myocytes. J Cell Biol, 2001;152(5):857-66.
47 D'Amico M, Di Filippo C, La M, et al. Lipocortin 1 reduces myocardial ischemia-reperfusion injury by affecting local leukocyte recruitment. FASEB J, 2000;14(13):1867-9.
48 Biffl WL, Moore EE. Splanchnic ischaemia/reperfusion and multiple organ failure. Br J Anaesth, 1996;77(1):59-70.
49 Cuzzocrea S, Tailor A, Zingarelli B, et al. Lipocortin 1 protects against splanchnic artery occlusion and reperfusion injury by affecting neutrophil migration. J Immunol, 1997;159(10):5089-97.
50 Relton JK, Rothwell NJ. Interleukin-1 receptor antagonist inhibits ischaemic and excitotoxic neuronal damage in the rat. Brain Res Bull, 1992;29(2):243-6.
2. Rhee HJ, Kim GY, Huh JW, Kim SW, Na DS: Annexin I is a stress protein induced by heat, oxidative stress and a sulfhydryl-reactive agent. Eur J Biochem 2000, 267(11):3220-3225.
3. Ferlazzo V, D'Agostino P, Milano S, Caruso R, Feo S, Cillari E, Parente L: Anti-inflammatory effects of annexin-1: stimulation of IL-10 release and inhibition of nitric oxide synthesis. Int Immunopharmacol 2003, 3(10-11):1363-1369.
4. Angeles TS, Yang SX, Steffler C, Dionne CA: Kinetics of trkA tyrosine kinase activity and inhibition by K-252a. Arch Biochem Biophys 1998, 349(2):267-274.
5. Relton JK, Strijbos PJ, O'Shaughnessy CT, Carey F, Forder RA, Tilders FJ, Rothwell NJ: Lipocortin-1 is an endogenous inhibitor of ischemic damage in the rat brain. J Exp Med 1991, 174(2):305-310.
6. Rosengarth A, Luecke H: A calcium-driven conformational switch of the N-terminal and core domains of annexin A1. J Mol Biol 2003, 326(5):1317-1325.
7. Hwang IK, Lee KY, Yoo KY, Kim DS, Lee NS, Jeong YG, Kang TC, Han BH, Kim JS, Won MH: Tyrosine kinase A but not phosphacan/protein tyrosine phosphatase- zeta/beta immunoreactivity and protein level changes in neurons and astrocytes in the gerbil hippocampus proper after transient forebrain ischemia. Brain Res 2005, 1036(1-2):35-41.
8. Debret R, El Btaouri H, Duca L, Rahman I, Radke S, Haye B, Sallenave JM, Antonicelli F: Annexin A1 processing is associated with caspase-dependent apoptosis in BZR cells. FEBS Lett 2003, 546(2-3):195-202.
9. Dorovkov MV, Ryazanov AG: Phosphorylation of annexin I by TRPM7 channel-kinase. J Biol Chem 2004, 279(49):50643-50646.
10. Touyz RM, He Y, Montezano AC, Yao G, Chubanov V, Gudermann T, Callera GE: Differential regulation of transient receptor potential melastatin 6 and 7 cation channels by ANG II in vascular smooth muscle cells from spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 2006, 290(1):R73-78.
11. Zhao L, Shi J, Sun N, Tian S, Meng X, Liu X, Li L: Effect of electroacupuncture on TRPM7 mRNA expression after cerebral ischemia/reperfusion in rats via TrkA pathway. J Huazhong Univ Sci Technolog Med Sci 2005, 25(3):247-250.
12. Kim YS, Ko J, Kim IS, Jang SW, Sung HJ, Lee HJ, Lee SY, Kim Y, Na DS: PKCdelta-dependent cleavage and nuclear translocation of annexin A1 by phorbol
12-myristate 13-acetate. Eur J Biochem 2003, 270(20):4089-4094.
13. Ishido M: Overexpression of Bcl-2 inhibits nuclear localization of annexin I during tumor necrosis factor-alpha-mediated apoptosis in porcine renal LLC-PK1 cells. Regul Pept 2005, 124(1-3):45-51.
14.张京钟,施静,刘晓春,张静,关新民,王才源:电针对大鼠局灶性脑缺血后脑内Bax,Bcl-2表达的影响.中国组织化学与细胞化学杂志2001(01).
1 Gerke V, Moss SE. Annexins: from structure to function. Physiol Rev, 2002; 82(2):331-71.
2 Rescher U, Gerke V. Annexins--unique membrane binding proteins with diverse functions. J Cell Sci, 2004;117(Pt 13):2631-9.
3 Dorovkov MV, Ryazanov AG. Phosphorylation of annexin I by TRPM7 channel-kinase. J Biol Chem, 2004;279(49):50643-6.
4 Rosengarth A, Luecke H. A calcium-driven conformational switch of the N-terminal and core domains of annexin A1. J Mol Biol, 2003;326(5):1317-25.
5 Taylor AD, Cowell AM, Flower J, et al. Lipocortin 1 mediates an early inhibitory action of glucocorticoids on the secretion of ACTH by the rat anterior pituitary gland in vitro. Neuroendocrinology, 1993;58(4):430-9.
6 Fava RA, McKanna J, Cohen S. Lipocortin I (p35) is abundant in a restricted number of differentiated cell types in adult organs. J Cell Physiol, 1989;141(2):284-93.
7 Dreier R, Schmid KW, Gerke V, et al. Differential expression of annexins I, II and IV in human tissues: an immunohistochemical study. Histochem Cell Biol, 1998; 110(2):137-48.
8 Peers SH, Smillie F, Elderfield AJ, et al. Glucocorticoid-and non-glucocorticoid induction of lipocortins (annexins) 1 and 2 in rat peritoneal leucocytes in vivo. Br J Pharmacol, 1993;108(1):66-72.
9 Traverso V, Morris JF, Flower RJ, et al. Lipocortin 1 (annexin 1) in patches associated with the membrane of a lung adenocarcinoma cell line and in the cell cytoplasm. J Cell Sci, 1998;111 ( Pt 10):1405-18.
10 Perretti M, Christian H, Wheller SK, et al. Annexin I is stored within gelatinase granules of human neutrophil and mobilized on the cell surface upon adhesion but not phagocytosis. Cell Biol Int, 2000;24(3):163-74.
11 Perretti M, Croxtall JD, Wheller SK, et al. Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration. Nat Med, 1996;2(11):1259-62.
12 Oliani SM, Paul-Clark MJ, Christian HC, et al. Neutrophil interaction with inflamed postcapillary venule endothelium alters annexin 1 expression. Am J Pathol, 2001;158(2):603-15.
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