Endogenous tissue plasminogen activator mediates bone marrow stromal cell-induced neurite remodeling after stroke in mice

Stroke

Volumn 42, Issue 2, 2011, Pages 459-464

  Shen, Li Hong ^a   Xin, Hongqi ^a   Li, Yi ^a   Zhang, Rui Lan ^a   Cui, Yisheng ^a   Zhang, Li ^a   Lu, Mei ^a   Zhang, Zheng Gang ^a   Chopp, Michael ^a,b  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

Author keywords

bone marrow stromal cells; functional recovery; neurite remodeling; stroke; tissue plasminogen activator

Indexed keywords

CASEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; PHOSPHATE BUFFERED SALINE; SYNAPTOPHYSIN; TISSUE PLASMINOGEN ACTIVATOR; VON WILLEBRAND FACTOR;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; BRAIN CORTEX; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE SEVERITY; ENZYME ACTIVITY; ENZYME LOCALIZATION; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE FIBER GROWTH; NERVE REGENERATION; NEUROLOGIC EXAMINATION; NONHUMAN; PRIORITY JOURNAL; STROKE; STROMA CELL; ZYMOGRAPHY;

ANIMALS; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURITES; RECOVERY OF FUNCTION; STROKE; STROMAL CELLS; TISSUE PLASMINOGEN ACTIVATOR;

EID: 79251637340     PISSN: 00392499     EISSN: None     Source Type: Journal    
DOI: 10.1161/STROKEAHA.110.593863     Document Type: Article

References (55)

1. Vassalli JD, Sappino AP, Belin D. The plasminogen activator/plasmin system. J Clin Invest. 1991;88:1067-1072.
2. Huber K. Plasminogen activator inhibitor type-1 (part one): basic mechanisms, regulation, and role for thromboembolic disease. J Thromb Thrombolysis. 2001;11:183-193.
3. Samson AL, Medcalf RL. Tissue-type plasminogen activator: a multifaceted modulator of neurotransmission and synaptic plasticity. Neuron. 2006;50:673-678.
4. Tsirka SE, Rogove AD, Bugge TH, Degen JL, Strickland S. An extracellular proteolytic cascade promotes neuronal degeneration in the mouse hippocampus. J Neurosci. 1997;17:543-552.
5. Xin H, Li Y, Shen LH, Liu X, Wang X, Zhang J, Pourabdollah-Nejad DS, Zhang C, Zhang L, Jiang H, Zhang ZG, Chopp M. Increasing tpa activity in astrocytes induced by multipotent mesenchymal stromal cells facilitate neurite outgrowth after stroke in the mouse. PLoS One. 5:e9027.
6. Seeds NW, Basham ME, Haffke SP. Neuronal migration is retarded in mice lacking the tissue plasminogen activator gene. Proc Natl Acad Sci USA. 1999;96:14118-14123.
7. Centonze D, Napolitano M, Saulle E, Gubellini P, Picconi B, Martorana A, Pisani A, Gulino A, Bernardi G, Calabresi P. Tissue plasminogen activator is required for corticostriatal long-term potentiation. Eur J Neurosci. 2002;16:713-721. (Pubitemid 35471841)
8. Mataga N, Nagai N, Hensch TK. Permissive proteolytic activity for visual cortical plasticity. Proc Natl Acad Sci USA. 2002;99:7717-7721.
9. Akassoglou K, Kombrinck KW, Degen JL, Strickland S. Tissue plasminogen activator-mediated fibrinolysis protects against axonal degeneration and demyelination after sciatic nerve injury. J Cell Biol. 2000;149: 1157-1166.
10. Siconolfi LB, Seeds NW. Induction of the plasminogen activator system accompanies peripheral nerve regeneration after sciatic nerve crush. J Neurosci. 2001;21:4336-4347.
11. Krystosek A, Seeds NW. Peripheral neurons and Schwann cells secrete plasminogen activator. J Cell Biol. 1984;98:773-776.
12. Sumi Y, Dent MA, Owen DE, Seeley PJ, Morris RJ. The expression of tissue and urokinase-type plasminogen activators in neural development suggests different modes of proteolytic involvement in neuronal growth. Development. 1992;116:625-637.
13. Siconolfi LB, Seeds NW. Mice lacking tPA, uPA, or plasminogen genes showed delayed functional recovery after sciatic nerve crush. J Neurosci. 2001;21:4348-4355.
14. Li Y, Chen J, Zhang CL, Wang L, Lu D, Katakowski M, Gao Q, Shen LH, Zhang J, Lu M, Chopp M. Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia. 2005;49: 407-417. (Pubitemid 40222918)
15. Liu Z, Li Y, Qu R, Shen L, Gao Q, Zhang X, Lu M, Savant-Bhonsale S, Borneman J, Chopp M. Axonal sprouting into the denervated spinal cord and synaptic and postsynaptic protein expression in the spinal cord after transplantation of bone marrow stromal cell in stroke rats. Brain Res. 2007;1149:172-180.
16. Shen LH, Li Y, Chen J, Cui Y, Zhang C, Kapke A, Lu M, Savant-Bhonsale S, Chopp M. One-year follow-up after bone marrow stromal cell treatment in middle-aged female rats with stroke. Stroke. 2007;38: 2150-2156.
17. Liu Z, Li Y, Zhang ZG, Cui X, Cui Y, Lu M, Savant-Bhonsale S, Chopp M. Bone marrow stromal cells enhance inter-and intracortical axonal connections after ischemic stroke in adult rats. J Cereb Blood Flow Metab. 2010;30:1288-1295.
18. Liu Z, Zhang RL, Li Y, Cui Y, Chopp M. Remodeling of the corticospinal innervation and spontaneous behavioral recovery after ischemic stroke in adult mice. Stroke. 2009;40:2546-2551.
19. Chen J, Zhang C, Jiang H, Li Y, Zhang L, Robin A, Katakowski M, Lu M, Chopp M. Atorvastatin induction of VEGF and BDNF promotes brain plasticity after stroke in mice. J Cereb Blood Flow Metab. 2005;25: 281-290.
20. Swanson RA, Morton MT, Tsao-Wu G, Savalos RA, Davidson C, Sharp FR. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab. 1990;10:290-293.
21. Cui X, Chen J, Zacharek A, Li Y, Roberts C, Kapke A, Savant-Bhonsale S, Chopp M. Nitric oxide donor upregulation of stromal cell-derived factor-1/chemokine (CXC motif) receptor 4 enhances bone marrow stromal cell migration into ischemic brain after stroke. Stem Cells. 2007; 25:2777-2785.
22. Sheehan D, Hrapchak B. Theory and practice of histotechnology. St. Louis, MO: CV Mosby Co; 1980.
23. SAS Institute SAS/STAT 9.1 User's Guide. Cary, NC: SAS Institute;, 2004.
24. Ujike H, Takaki M, Kodama M, Kuroda S. Gene expression related to synaptogenesis, neuritogenesis, and MAP kinase in behavioral sensitization to psychostimulants. Ann N Y Acad Sci. 2002;965:55-67.
25. Lawrence DA, Strandberg L, Ericson J, Ny T. Structure-function studies of the SERPIN plasminogen activator inhibitor type 1. Analysis of chimeric strained loop mutants. J Biol Chem. 1990;265:20293-20301.
26. Dezawa M, Hoshino M, Nabeshima Y, Ide C. Marrow stromal cells: implications in health and disease in the nervous system. Curr Mol Med. 2005;5:723-732.
27. Li Y, Chopp M, Chen J, Wang L, Gautam SC, Xu YX, Zhang Z. Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J Cereb Blood Flow Metab. 2000;20:1311-1319.
28. Stroemer RP, Kent TA, Hulsebosch CE. Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke. 1995;26:2135-2144.
29. Neuhuber B, Timothy Himes B, Shumsky JS, Gallo G, Fischer I. Axon growth and recovery of function supported by human bone marrow stromal cells in the injured spinal cord exhibit donor variations. Brain Res. 2005;1035:73-85.
30. Kim JA, Tran ND, Li Z, Yang F, Zhou W, Fisher MJ. Brain endothelial hemostasis regulation by pericytes. J Cereb Blood Flow Metab. 2006;26: 209-217.
31. Schreiber SS, Tan Z, Sun N, Wang L, Zlokovic BV. Immunohistochemical localization of tissue plasminogen activator in vascular endothelium of stroke-prone regions of the rat brain. Neurosurgery. 1998;43: 909-913.
32. Yepes M, Lawrence DA. Neuroserpin: a selective inhibitor of tissue-type plasminogen activator in the central nervous system. Thromb Haemost. 2004;91:457-464. (Pubitemid 38396867)
33. Seeds NW, Basham ME, Ferguson JE. Absence of tissue plasminogen activator gene or activity impairs mouse cerebellar motor learning. J Neurosci. 2003;23:7368-7375.
34. Krystosek A, Seeds NW. Plasminogen activator release at the neuronal growth cone. Science. 1981;213:1532-1534.
35. Polavarapu R, Gongora MC, Yi H, Ranganthan S, Lawrence DA, Strickland D, Yepes M. Tissue-type plasminogen activator-mediated shedding of astrocytic low-density lipoprotein receptor-related protein increases the permeability of the neurovascular unit. Blood. 2007;109: 3270-3278.
36. Park L, Gallo EF, Anrather J, Wang G, Norris EH, Paul J, Strickland S, Iadecola C. Key role of tissue plasminogen activator in neurovascular coupling. Proc Natl Acad Sci USA. 2008;105:1073-1078.
37. Zhao G, Reynolds JN, Flavin MP. Temporal profile of tissue plasminogen activator (tPA) and inhibitor expression after transient focal cerebral ischemia. Neuroreport. 2003;14:1689-1692.
38. Nagai N, De Mol M, Lijnen HR, 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: 2440-2444.
39. Ning M, Furie KL, Koroshetz WJ, Lee H, Barron M, Lederer M, Wang X, Zhu M, Sorensen AG, Lo EH, Kelly PJ. Association between tPA therapy and raised early matrix metalloproteinase-9 in acute stroke. Neurology. 2006;66:1550-1555.
40. Tsuji K, Aoki T, Tejima E, Arai K, Lee SR, Atochin DN, Huang PL, Wang X, Montaner J, Lo EH. Tissue plasminogen activator promotes matrix metalloproteinase-9 upregulation after focal cerebral ischemia. Stroke. 2005;36:1954-1959.
41. Hu K, Yang J, Tanaka S, Gonias SL, Mars WM, Liu Y. Tissue-type plasminogen activator acts as a cytokine that triggers intracellular signal transduction and induces matrix metalloproteinase-9 gene expression. J Biol Chem. 2006;281:2120-2127.
42. Kang SS, Kook JH, Hwang S, Park SH, Nam SC, Kim JK. Inhibition of matrix metalloproteinase-9 attenuated neural progenitor cell migration after photothrombotic ischemia. Brain Res. 2008;1228:20-26.
43. Wang L, Zhang ZG, Zhang RL, Gregg SR, Hozeska-Solgot A, LeTourneau Y, Wang Y, Chopp M. Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J Neurosci. 2006;26:5996-6003.
44. Lu L, Tonchev AB, Kaplamadzhiev DB, Boneva NB, Mori Y, Sahara S, Ma D, Nakaya MA, Kikuchi M, Yamashima T. Expression of matrix metalloproteinases in the neurogenic niche of the adult monkey hippocampus after ischemia. Hippocampus. 2008;18:1074-1084.
45. Barkho BZ, Munoz AE, Li X, Li L, Cunningham LA, Zhao X. Endogenous matrix metalloproteinase (MMP)-3 and MMP-9 promote the differentiation and migration of adult neural progenitor cells in response to chemokines. Stem Cells. 2008;26:3139-3149.
46. Kim DH, Lilliehook C, Roides B, Chen Z, Chang M, Mobashery S, Goldman SA. Testosterone-induced matrix metalloproteinase activation is a checkpoint for neuronal addition to the adult songbird brain. J Neurosci. 2008;28:208-216.
47. Gutiérrez-Fernández A, Gingles NA, Bai H, Castellino FJ, Parmer RJ, Miles LA. Plasminogen enhances neuritogenesis on laminin-1. J Neurosci. 2009;29:12393-12400.
48. Bruno MA, Cuello AC. Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade. Proc Natl Acad Sci USA. 2006;103: 6735-6740.
49. Mou X, Peterson CB, Prosser RA. Tissue-type plasminogen activatorplasmin-bdnf modulate glutamate-induced phase-shifts of the mouse suprachiasmatic circadian clock in vitro. Eur J Neurosci. 2009;30: 1451-1460.
50. Gray K, Ellis V. Activation of pro-BDNF by the pericellular serine protease plasmin. FEBS Lett. 2008;582:907-910.
51. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B. Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science. 2004;306: 487-491.
52. Nagappan G, Zaitsev E, Senatorov VV Jr, Yang J, Hempstead BL, Lu B. Control of extracellular cleavage of proBDNF by high frequency neuronal activity. Proc Natl Acad Sci USA. 2009;106:1267-1272.
53. Yamazaki M, Chiba K, Mohri T. Fundamental role of nitric oxide in neuritogenesis of PC12h cells. Br J Pharmacol. 2005;146:662-669.
54. Kucharewicz I, Kowal K, Buczko W, Bodzenta-Łukaszyk A. The plasmin system in airway remodeling. Thromb Res. 2003;112:1-7.
55. Barker PA. Whither proBDNF? Nat Neurosci. 2009;12:105-106.