Recombinant tissue plasminogen activator promotes, and progesterone attenuates, microglia/macrophage M1 polarization and recruitment of microglia after MCAO stroke in rats

Brain, Behavior, and Immunity

Volumn 49, Issue , 2015, Pages 267-279

  Won, Soonmi ^a   Lee, Jae Kyung ^b   Stein, Donald G ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

M1 M2 polarization; Macrophage; Microglia; MIP 1 ; Neuroinflammation; Progesterone; Recovery; Stroke; TPA

Indexed keywords

ALTEPLASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; PROGESTERONE; STROMELYSIN; TUMOR NECROSIS FACTOR ALPHA; ANTIINFLAMMATORY AGENT; RECOMBINANT PROTEIN; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ACTIVATION; CELL COUNT; CELL INFILTRATION; CELL MIGRATION; CELL POLARITY; CELL SHAPE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG MECHANISM; ENDOTHELIUM CELL; GENE EXPRESSION; MACROPHAGE; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REOXYGENATION; ANIMAL; CEREBRAL ARTERY DISEASE; CEREBROVASCULAR ACCIDENT; DISEASE MODEL; DRUG EFFECTS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL POLARITY; CHEMOKINE CCL3; DISEASE MODELS, ANIMAL; INFARCTION, MIDDLE CEREBRAL ARTERY; MACROPHAGES; MALE; MATRIX METALLOPROTEINASE 3; MICROGLIA; PROGESTERONE; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; STROKE; TISSUE PLASMINOGEN ACTIVATOR;

EID: 84940612919     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.06.007     Document Type: Article

References (65)

1. An J., Zhang C., Polavarapu R., Zhang X., Zhang X., Yepes M. Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein induce Akt phosphorylation in the ischemic brain. Blood 2008, 112(7):2787-2794.
2. Block M.L., Hong J.S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 2005, 76(2):77-98.
3. Bruce-Keller A.J., Barger S.W., Moss N.I., Pham J.T., Keller J.N., Nath A. Pro-inflammatory and pro-oxidant properties of the HIV protein Tat in a microglial cell line: attenuation by 17 beta-estradiol. J. Neurochem. 2001, 78(6):1315-1324.
4. Cao C., Lawrence D.A., Li Y., Von Arnim C.A., Herz J., Su E.J., Makarova A., Hyman B.T., Strickland D.K., Zhang L. Endocytic receptor LRP together with tPA and PAI-1 coordinates Mac-1-dependent macrophage migration. EMBO J. 2006, 25(9):1860-1870.
5. Cekic M., Johnson S.J., Bhatt V.H., Stein D.G. Progesterone treatment alters neurotrophin/proneurotrophin balance and receptor expression in rats with traumatic brain injury. Restor. Neurol. Neurosci. 2012, 28:1-12.
6. Cumming G. Understanding the New Statistics, Effect Sizes, Confidence Intervals and Meta Analysis 2012, Rutledge Press, London.
7. David S., Kroner A. Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 2011, 12(7):388-399.
8. Endres M. Statins and stroke. J. Cereb. Blood Flow Metab. 2005, 25(9):1093-1110.
9. Gelderblom M., Leypoldt F., Steinbach K., Behrens D., Choe C.U., Siler D.A., Arumugam T.V., Orthey E., Gerloff C., Tolosa E., Magnus T. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 2009, 40(5):1849-1857.
10. Godfrey K.R., Tanswell P., Bates R.A., Chappell M.J., Madden F.N. Nonlinear pharmacokinetics of tissue-type plasminogen activator in three animal species: a comparison of mathematical models. Biopharm. Drug Dispos. 1998, 19(2):131-140.
11. Grobmyer S.R., Kuo A., Orishimo M., Okada S.S., Cines D.B., Barnathan E.S. Determinants of binding and internalization of tissue-type plasminogen activator by human vascular smooth muscle and endothelial cells. J. Biol. Chem. 1993, 268(18):13291-13300.
12. Hu X., Li P., Guo Y., Wang H., Leak R.K., Chen S., Gao Y., Chen J. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 2012, 43(11):3063-3070.
13. I.M.S.Study Investigators Combined intravenous and intra-arterial recanalization for acute ischemic stroke: the Interventional Management of Stroke Study. Stroke 2004, 35(4):904-911.
14. Imai F., Suzuki H., Oda J., Ninomiya T., Ono K., Sano H., Sawada M. Neuroprotective effect of exogenous microglia in global brain ischemia. J. Cereb. Blood Flow Metab. 2007, 27(3):488-500.
15. Ishrat T., Sayeed I., Atif F., Stein D.G. Effects of progesterone administration on infarct volume and functional deficits following permanent focal cerebral ischemia in rats. Brain Res. 2009, 1257:94-101.
16. Ishrat T., Sayeed I., Atif F., Hua F., Stein D.G. Progesterone and allopregnanolone attenuate blood-brain barrier dysfunction following permanent focal ischemia by regulating the expression of matrix metalloproteinases. Exp. Neurol. 2010, 226(1):183-190.
17. Ishrat T., Sayeed I., Atif F., Hua F., Stein D.G. Progesterone is neuroprotective against ischemic brain injury through its effects on the phosphoinositide 3-kinase/protein kinase B signaling pathway. Neuroscience 2012, 210:442-450.
18. Jin R., Yang G., Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J. Leukoc. Biol. 2010, 87(5):779-789.
19. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 2009, 29(43):13435-13444.
20. Kim J.S., Gautam S.C., Chopp M., Zaloga C., Jones M.L., Ward P.A., Welch K.M. Expression of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 after focal cerebral ischemia in the rat. J. Neuroimmunol. 1995, 56(2):127-134.
21. Kim N.G., Lee H., Son E., Kwon O.Y., Park J.Y., Park J.H., Cho G.J., Choi W.S., Suk K. Hypoxic induction of caspase-11/caspase-1/interleukin-1beta in brain microglia. Brain Res. Mol. Brain Res. 2003, 114(2):107-114.
22. Kim J.Y., Kawabori M., Yenari M.A. Innate inflammatory responses in stroke: mechanisms and potential therapeutic targets. Curr. Med. Chem. 2014, 21(18):2076-2097.
23. Kohler E., Prentice D.A., Bates T.R., Hankey G.J., Claxton A., van Heerden J., Blacker D. Intravenous minocycline in acute stroke: a randomized, controlled pilot study and meta-analysis. Stroke 2013, 44(9):2493-2499.
24. Lalancette-Hebert M., Gowing G., Simard A., Weng Y.C., Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 2007, 27(10):2596-2605.
25. Lawrence T., Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 2011, 11(11):750-761.
26. Lee J.K., Tansey M.G. Microglia isolation from adult mouse brain. Methods Mol. Biol. 2013, 1041:17-23.
27. Lees K.R., Bluhmki E., von Kummer R., Brott T.G., Toni D., Grotta J.C., Albers G.W., Kaste M., Marler J.R., Hamilton S.A., Tilley B.C., Davis S.M., Donnan G.A., Hacke W., Allen K., Mau J., Meier D., del Zoppo G., De Silva D.A., Butcher K.S., Parsons M.W., Barber P.A., Levi C., Bladin C., Byrnes G. Time to treatment with intravenous alteplase and outcome in stroke: an updated pooled analysis of ECASS, ATLANTIS, NINDS, and EPITHET trials. Lancet 2010, 375(9727):1695-1703. ECASS, ATLANTIS, NINDS and EPITHET rt-PA Study Group.
28. Liesz A., Zhou W., Mracsko E., Karcher S., Bauer H., Schwarting S., Sun L., Bruder D., Stegemann S., Cerwenka A., Sommer C., Dalpke A.H., Veltkamp R. Inhibition of lymphocyte trafficking shields the brain against deleterious neuroinflammation after stroke. Brain 2011, 134(Pt 3):704-720.
29. Loane D.J., Byrnes K.R. Role of microglia in neurotrauma. Neurotherapeutics 2010, 7(4):366-377.
30. Luster A.D., Alon R., von Andrian U.H. Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 2005, 6(12):1182-1190.
31. Manicone A.M., McGuire J.K. Matrix metalloproteinases as modulators of inflammation. Semin. Cell Dev. Biol. 2008, 19(1):34-41.
32. Mikita J., Dubourdieu-Cassagno N., Deloire M.S., Vekris A., Biran M., Raffard G., Brochet B., Canron M.H., Franconi J.M., Boiziau C., Petry K.G. Altered M1/M2 activation patterns of monocytes in severe relapsing experimental rat model of multiple sclerosis. Amelioration of clinical status by M2 activated monocyte administration. Mult. Scler. 2011, 17(1):2-15.
33. Min K.J., Pyo H.K., Yang M.S., Ji K.A., Jou I., Joe E.H. Gangliosides activate microglia via protein kinase C and NADPH oxidase. Glia 2004, 48(3):197-206.
34. Minagar A., Shapshak P., Fujimura R., Ownby R., Heyes M., Eisdorfer C. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J. Neurol. Sci. 2002, 202(1-2):13-23.
35. Moretti A., Ferrari F., Villa R.F. Neuroprotection for ischaemic stroke: current status and challenges. Pharmacol. Ther. 2014.
36. Murray P.J., Wynn T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11(11):723-737.
37. Nagai N., De Mol M., Lijnen H.R., Carmeliet P., Collen D. Role of plasminogen system components in focal cerebral ischemic infarction: a gene targeting and gene transfer study in mice. Circulation 1999, 99(18):2440-2444.
38. Nicole O., Docagne F., Ali C., Margaill I., Carmeliet P., MacKenzie E.T., Vivien D., Buisson A. The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat. Med. 2001, 7(1):59-64.
39. Nimmo A.J., Vink R. Recent patents in CNS drug discovery: the management of inflammation in the central nervous system. Recent Pat. CNS Drug Discov. 2009, 4(2):86-95.
40. Nishi T., Maier C.M., Hayashi T., Saito A., Chan P.H. Superoxide dismutase 1 overexpression reduces MCP-1 and MIP-1 alpha expression after transient focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2005, 25(10):1312-1324.
41. Orth K., Willnow T., Herz J., Gething M.J., Sambrook J. Low density lipoprotein receptor-related protein is necessary for the internalization of both tissue-type plasminogen activator-inhibitor complexes and free tissue-type plasminogen activator. J. Biol. Chem. 1994, 269(33):21117-21122.
42. Pineda D., Ampurdanes C., Medina M.G., Serratosa J., Tusell J.M., Saura J., Planas A.M., Navarro P. Tissue plasminogen activator induces microglial inflammation via a noncatalytic molecular mechanism involving activation of mitogen-activated protein kinases and Akt signaling pathways and AnnexinA2 and Galectin-1 receptors. Glia 2012, 60(4):526-540.
43. Ponomarev E.D., Maresz K., Tan Y., Dittel B.N. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J. Neurosci. 2007, 27(40):10714-10721.
44. Riazi K., Galic M.A., Pittman Q.J. Contributions of peripheral inflammation to seizure susceptibility: cytokines and brain excitability. Epilepsy Res. 2010, 89(1):34-42.
45. Rossi B., Angiari S., Zenaro E., Budui S.L., Constantin G. Vascular inflammation in central nervous system diseases: adhesion receptors controlling leukocyte-endothelial interactions. J. Leukoc. Biol. 2011, 89(4):539-556.
46. Ruffell D., Mourkioti F., Gambardella A., Kirstetter P., Lopez R.G., Rosenthal N., Nerlov C. A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(41):17475-17480.
47. Saver J.L., Fonarow G.C., Smith E.E., Reeves M.J., Grau-Sepulveda M.V., Pan W., Olson D.M., Hernandez A.F., Peterson E.D., Schwamm L.H. Time to treatment with intravenous tissue plasminogen activator and outcome from acute ischemic stroke. JAMA 2013, 309(23):2480-2488.
48. Siao C.J., Tsirka S.E. Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. J. Neurosci. 2002, 22(9):3352-3358.
49. Siao C.J., Fernandez S.R., Tsirka S.E. Cell type-specific roles for tissue plasminogen activator released by neurons or microglia after excitotoxic injury. J. Neurosci. 2003, 23(8):3234-3242.
50. Skuljec J., Sun H., Pul R., Benardais K., Ragancokova D., Moharregh-Khiabani D., Kotsiari A., Trebst C., Stangel M. CCL5 induces a pro-inflammatory profile in microglia in vitro. Cell. Immunol. 2011, 270(2):164-171.
51. Suh H.S., Zhao M.L., Choi N., Belbin T.J., Brosnan C.F., Lee S.C. TLR3 and TLR4 are innate antiviral immune receptors in human microglia: role of IRF3 in modulating antiviral and inflammatory response in the CNS. Virology 2009, 392(2):246-259.
52. Suzuki Y., Nagai N., Umemura K., Collen D., Lijnen H.R. Stromelysin-1 (MMP-3) is critical for intracranial bleeding after t-PA treatment of stroke in mice. J. Thromb. Haemost. 2007, 5(8):1732-1739.
53. Wang Y.F., Tsirka S.E., Strickland S., Stieg P.E., Soriano S.G., Lipton S.A. Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat. Med. 1998, 4(2):228-231.
54. Wang H.K., Park U.J., Kim S.Y., Lee J.H., Kim S.U., Gwag B.J., Lee Y.B. Free radical production in CA1 neurons induces MIP-1alpha expression, microglia recruitment, and delayed neuronal death after transient forebrain ischemia. J. Neurosci. 2008, 28(7):1721-1727.
55. Wang G., Zhang J., Hu X., Zhang L., Mao L., Jiang X., Liou A.K., Leak R.K., Gao Y., Chen J. Microglia/macrophage polarization dynamics in white matter after traumatic brain injury. J. Cereb. Blood Flow Metab. 2013, 33(12):1864-1874.
56. Weber C., Koenen R.R. Fine-tuning leukocyte responses: towards a chemokine 'interactome'. Trends Immunol. 2006, 27(6):268-273.
57. Won S., Lee J.H., Wali B., Stein D.G., Sayeed I. Progesterone attenuates hemorrhagic transformation after delayed tPA treatment in an experimental model of stroke in rats: involvement of the VEGF-MMP pathway. J. Cereb. Blood Flow Metab. 2014, 34(1):72-80.
58. Woo M.S., Park J.S., Choi I.Y., Kim W.K., Kim H.S. Inhibition of MMP-3 or -9 suppresses lipopolysaccharide-induced expression of proinflammatory cytokines and iNOS in microglia. J. Neurochem. 2008, 106(2):770-780.
59. Wu F., Nicholson A.D., Haile W.B., Torre E., An J., Chen C., Lee A.K., Duong D.M., Dammer E.B., Seyfried N.T., Tong F.C., Votaw J.R., Yepes M. Tissue-type plasminogen activator mediates neuronal detection and adaptation to metabolic stress. J. Cereb. Blood Flow Metab. 2013, 33(11):1761-1769.
60. Wu F., Catano M., Echeverry R., Torre E., Haile W.B., An J., Chen C., Cheng L., Nicholson A., Tong F.C., Park J., Yepes M. Urokinase-type plasminogen activator promotes dendritic spine recovery and improves neurological outcome following ischemic stroke. J. Neurosci. 2014, 34(43):14219-14232.
61. Yepes M., Roussel B.D., Ali C., Vivien D. Tissue-type plasminogen activator in the ischemic brain: more than a thrombolytic. Trends Neurosci. 2009, 32(1):48-55.
62. Young A.M., Karri S.K., Ogilvy C.S. Exploring the use of estrogen & progesterone replacement therapy in subarachnoid hemorrhage. Curr. Drug Saf. 2012, 7(3):202-206.
63. Zaremba J., Ilkowski J., Losy J. Serial measurements of levels of the chemokines CCL2, CCL3 and CCL5 in serum of patients with acute ischaemic stroke. Folia Neuropathol. 2006, 44(4):282-289.
64. Zhang X., Polavarapu R., She H., Mao Z., Yepes M. Tissue-type plasminogen activator and the low-density lipoprotein receptor-related protein mediate cerebral ischemia-induced nuclear factor-kappaB pathway activation. Am. J. Pathol. 2007, 171(4):1281-1290.
65. Zhu H., Fan X., Yu Z., Liu J., Murata Y., Lu J., Zhao S., Hajjar K.A., Lo E.H., Wang X. Annexin A2 combined with low-dose tPA improves thrombolytic therapy in a rat model of focal embolic stroke. J. Cereb. Blood Flow Metab. 2010, 30(6):1137-1146.