Thymosin β4 improves functional neurological outcome in a rat model of embolic stroke

Neuroscience

Volumn 169, Issue 2, 2010, Pages 674-682

  Morris, D C ^a   Chopp, M ^b,c   Zhang, L ^b   Lu, M ^d   Zhang, Z G ^b  

^a HENRY FORD HEALTH SYSTEM   (United States)

^b HENRY FORD HOSPITAL   (United States)

^c OAKLAND UNIVERSITY   (United States)

^d HENRY FORD HEALTH SCIENCES CENTER   (United States)

Author keywords

Axonal remodeling; Oligodendrocyte; Rat; Stroke; Thymosin; Thymosin beta4

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; PROTEIN ANTIBODY; PROTEOCHONDROITIN SULFATE; THYMOSIN BETA4; ANTIGEN; ASCL1 PROTEIN, RAT; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CHONDROITIN SULFATE PROTEOGLYCAN 4; PROTEOGLYCAN; THYMOSIN; THYMOSIN BETA(4);

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN EMBOLISM; BRAIN FUNCTION; CELL COUNT; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; FUNCTIONAL ASSESSMENT; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROGNOSIS; RAT; REMYELINIZATION; ANIMAL; BIOSYNTHESIS; CEREBRAL ARTERY DISEASE; CORPUS CALLOSUM; CORPUS STRIATUM; METABOLISM; MYELIN SHEATH; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; STEM CELL; VASCULARIZATION; WISTAR RAT;

ANIMALS; ANTIGENS; AXONS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL PROLIFERATION; CORPUS CALLOSUM; CORPUS STRIATUM; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MYELIN SHEATH; NEURONS; OLIGODENDROGLIA; PROTEOGLYCANS; RATS; RATS, WISTAR; STEM CELLS; THYMOSIN;

EID: 77954574668     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.05.017     Document Type: Article

References (45)

1. Aguirre A., Dupree J.L., Mangin J.M., Gallo V. A functional role for EGFR signaling in myelination and remyelination. Nat Neurosci 2007, 10:990-1002.
2. Aguirre A., Gallo V. Reduced EGFR signaling in progenitor cells of the adult subventricular zone attenuates oligodendrogenesis after demyelination. Neuron Glia Biol 2007, 3:209-220.
3. Arvidsson A., Collin T., Kirik D., Kokaia Z., Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002, 8:963-970.
4. Bock-Marquette I., Saxena A., White M.D., Dimaio J.M., Srivastava D. Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 2004, 432:466-472.
5. Prioritizing interventions to improve rates of thrombolysis for ischemic stroke. Neurology 2005, 64:654-659. California Acute Stroke Pilot Registry (CASPR) Investigators.
6. Carpintero P., Anadon R., Diaz-Regueira S., Gomez-Marquez J. Expression of thymosin beta4 messenger RNA in normal and kainate-treated rat forebrain. Neuroscience 1999, 90:1433-1444.
7. Cenci M.A., Whishaw I.Q., Schallert T. Animal models of neurological deficits: how relevant is the rat?. Nat Rev Neurosci 2002, 3:574-579.
8. Chen J., Zacharek A., Li A., Zhang C., Ding J., Roberts C., Lu M., Kapke A., Chopp M. Vascular endothelial growth factor mediates atorvastatin-induced mammalian achaete-scute homologue-1 gene expression and neuronal differentiation after stroke in retired breeder rats. Neuroscience 2006, 141:737-744.
9. Chen J., Zacharek A., Li Y., Li A., Wang L., Katakowski M., Roberts C., Lu M., Chopp M. N-cadherin mediates nitric oxide-induced neurogenesis in young and retired breeder neurospheres. Neuroscience 2006, 140:377-388.
10. Chen J., Zhang Z.G., Li Y., Wang Y., Wang L., Jiang H., Zhang C., Lu M., Katakowski M., Feldkamp C.S., Chopp M. Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 2003, 53:743-751.
11. Dewar D., Underhill S.M., Goldberg M.P. Oligodendrocytes and ischemic brain injury. J Cereb Blood Flow Metab 2003, 23:263-274.
12. Ding G., Jiang Q., Li L., Zhang L., Gang Zhang Z., Ledbetter K.A., Ewing J.R., Li Q., Chopp M. Detection of BBB disruption and hemorrhage by Gd-DTPA enhanced MRI after embolic stroke in rat. Brain Res 2006, 1114:195-203.
13. Franklin R.J., Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008, 9:839-855.
14. Goldstein A.L., Hannappel E., Kleinman H.K. Thymosin beta4: actin-sequestering protein moonlights to repair injured tissues. Trends Mol Med 2005, 11:421-429.
15. Goldstein A.L., Slater F.D., White A. Preparation, assay, and partial purification of a thymic lymphocytopoietic factor (thymosin). Proc Natl Acad Sci U S A 1966, 56:1010-1017.
16. Gomez-Marquez J., Anadon R. The beta-thymosins, small actin-binding peptides widely expressed in the developing and adult cerebellum. Cerebellum 2002, 1:95-102.
17. Gregersen R., Christensen T., Lehrmann E., Diemer N.H., Finsen B. Focal cerebral ischemia induces increased myelin basic protein and growth-associated protein-43 gene transcription in peri-infarct areas in the rat brain. Exp Brain Res 2001, 138:384-392.
18. Guarnera G., De Rosa A., Camerini R. Thymosin beta-4 and venous ulcers: clinical remarks on a European prospective, randomized study on safety, tolerability, and enhancement on healing. Ann N Y Acad Sci 2007, 1112:407-412.
19. Hacke W., Kaste M., Bluhmki E., Brozman M., Davalos A., Guidetti D., Larrue V., Lees K.R., Medeghri Z., Machnig T., Schneider D., von Kummer R., Wahlgren N., Toni D. Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008, 359:1317-1329.
20. Hinkel R., El-Aouni C., Olson T., Horstkotte J., Mayer S., Muller S., Willhauck M., Spitzweg C., Gildehaus F.J., Munzing W., Hannappel E., Bock-Marquette I., DiMaio J.M., Hatzopoulos A.K., Boekstegers P., Kupatt C. Thymosin beta4 is an essential paracrine factor of embryonic endothelial progenitor cell-mediated cardioprotection. Circulation 2008, 117:2232-2240.
21. Horner P.J., Power A.E., Kempermann G., Kuhn H.G., Palmer T.D., Winkler J., Thal L.J., Gage F.H. Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 2000, 20:2218-2228.
22. Huff T., Rosorius O., Otto A.M., Muller C.S., Ballweber E., Hannappel E., Mannherz H.G. Nuclear localisation of the G-actin sequestering peptide thymosin beta4. J Cell Sci 2004, 117:5333-5341.
23. Ivkovic S., Canoll P., Goldman J.E. Constitutive EGFR signaling in oligodendrocyte progenitors leads to diffuse hyperplasia in postnatal white matter. J Neurosci 2008, 28:914-922.
24. Kleindorfer D., Xu Y., Moomaw C.J., Khatri P., Adeoye O., Hornung R. US geographic distribution of rt-PA utilization by hospital for acute ischemic stroke. Stroke 2009, 40:3580-3584.
25. Kleindorfer D.O., Broderick J.P., Khoury J., Flaherty M.L., Woo D., Alwell K., Moomaw C.J., Pancioli A., Jauch E., Miller R., Kissela B.M. Emergency department arrival times after acute ischemic stroke during the 1990s. Neurocrit Care 2007, 7:31-35.
26. Lu D., Mahmood A., Qu C., Goussev A., Schallert T., Chopp M. Erythropoietin enhances neurogenesis and restores spatial memory in rats after traumatic brain injury. J Neurotrauma 2005, 22:1011-1017.
27. Malinda K.M., Goldstein A.L., Kleinman H.K. Thymosin beta 4 stimulates directional migration of human umbilical vein endothelial cells. FASEB J 1997, 11:474-481.
28. Malinda K.M., Sidhu G.S., Mani H., Banaudha K., Maheshwari R.K., Goldstein A.L., Kleinman H.K. Thymosin beta4 accelerates wound healing. J Invest Dermatol 1999, 113:364-368.
29. Mora C.A., Baumann C.A., Paino J.E., Goldstein A.L., Badamchian M. Biodistribution of synthetic thymosin beta 4 in the serum, urine, and major organs of mice. Int J Immunopharmacol 1997, 19:1-8.
30. Pantoni L., Garcia J.H., Gutierrez J.A. Cerebral white matter is highly vulnerable to ischemia. Stroke 1996, 27:1641-1646. discussion 1647.
31. Sapp E., Kegel K.B., Aronin N., Hashikawa T., Uchiyama Y., Tohyama K., Bhide P.G., Vonsattel J.P., DiFiglia M. Early and progressive accumulation of reactive microglia in the Huntington disease brain. J Neuropathol Exp Neurol 2001, 60:161-172.
32. Shen L.H., Li Y., Chen J., Zhang J., Vanguri P., Borneman J., Chopp M. Intracarotid transplantation of bone marrow stromal cells increases axon-myelin remodeling after stroke. Neuroscience 2006, 137:393-399.
33. Sim F.J., Zhao C., Penderis J., Franklin R.J. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J Neurosci 2002, 22:2451-2459.
34. Smart N., Risebro C.A., Melville A.A., Moses K., Schwartz R.J., Chien K.R., Riley P.R. Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 2007, 445:177-182.
35. Sosne G., Hafeez S., Greenberry A.L., Kurpakus-Wheater M. Thymosin beta4 promotes human conjunctival epithelial cell migration. Curr Eye Res 2002, 24:268-273.
36. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med 1995, 333:1581-1587. The NINDS rt-PA Stroke Study Group.
37. van Kesteren R.E., Carter C., Dissel H.M., van Minnen J., Gouwenberg Y., Syed N.I., Spencer G.E., Smit A.B. Local synthesis of actin-binding protein beta-thymosin regulates neurite outgrowth. J Neurosci 2006, 26:152-157.
38. Vartiainen N., Pyykonen I., Hokfelt T., Koistinaho J. Induction of thymosin beta(4) mRNA following focal brain ischemia. Neuroreport 1996, 7:1613-1616.
39. Wang L., Zhang Z., Wang Y., Zhang R., Chopp M. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004, 35:1732-1737.
40. Yang H., Cheng X., Yao Q., Li J., Ju G. The promotive effects of thymosin beta4 on neuronal survival and neurite outgrowth by upregulating L1 expression. Neurochem Res 2008, 33:2269-2280.
41. Zhang R., Wang Y., Zhang L., Zhang Z., Tsang W., Lu M., Chopp M. Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 2002, 33:2675-2680.
42. Zhang R., Zhang Z., Wang L., Wang Y., Gousev A., Zhang L., Ho K.L., Morshead C., Chopp M. Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 2004, 24:441-448.
43. Zhang R.L., Zhang Z., Zhang L., Wang Y., Zhang C., Chopp M. Delayed treatment with sildenafil enhances neurogenesis and improves functional recovery in aged rats after focal cerebral ischemia. J Neurosci Res 2006, 83:1213-1219.
44. Zhang Z., Zhang R.L., Jiang Q., Raman S.B., Cantwell L., Chopp M. A new rat model of thrombotic focal cerebral ischemia. J Cereb Blood Flow Metab 1997, 17:123-135.
45. Zhang Z.G., Zhang L., Tsang W., Soltanian-Zadeh H., Morris D., Zhang R., Goussev A., Powers C., Yeich T., Chopp M. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J Cereb Blood Flow Metab 2002, 22:379-392.