Thymosin beta 4 mediates oligodendrocyte differentiation by upregulating p38 MAPK

GLIA

Volumn 60, Issue 12, 2012, Pages 1826-1838

  Santra, Manoranjan ^a   Chopp, Michael ^a,b   Zhang, Zheng Gang ^a   Lu, Mei ^c   Santra, Sutapa ^a   Nalani, Ankita ^a   Santra, Soumi ^a   Morris, Daniel C ^c  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

^c HENRY FORD HEALTH SYSTEM   (United States)

Author keywords

Actin binding proteins; N20.1 cells; Neruospheres; Subventricular zone

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELIN BASIC PROTEIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE 1; THYMOSIN BETA4;

ANIMAL CELL; APOPTOSIS; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; ENZYME PHOSPHORYLATION; LATERAL BRAIN VENTRICLE; MOLECULAR MECHANICS; MOUSE; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; MALE; MAP KINASE SIGNALING SYSTEM; MICE; OLIGODENDROGLIA; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RATS; STEM CELLS; THYMOSIN; UP-REGULATION;

EID: 84867656103     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22400     Document Type: Article

References (60)

1. Aguirre-Ghiso JA, Estrada Y, Liu D, Ossowski L. 2003. ERK(MAPK) activity as a determinant of tumor growth and dormancy; regulation by p38(SAPK). Cancer Res 63: 1684-1695.
2. Andrae J, Gallini R, Betsholtz C. 2008. Role of platelet-derived growth factors in physiology and medicine. Genes Dev 22: 1276-1312.
3. Baron W, Metz B, Bansal R, Hoekstra D, de Vries H. 2000. PDGF and FGF-2 signaling in oligodendrocyte progenitor cells: regulation of proliferation and differentiation by multiple intracellular signaling pathways. Mol Cell Neurosci 15: 314-329.
4. Bednarek R, Boncela J, Smolarczyk K, Cierniewska-Cieslak A, Wyroba E, Cierniewski CS. 2008. Ku80 as a novel receptor for thymosin beta4 that mediates its intracellular activity different from G-actin sequestering. J Biol Chem 283: 1534-1544.
5. Bock-Marquette I, Saxena A, White MD, Dimaio JM, Srivastava D. 2004. Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 432: 466-472.
6. Bulavin DV, Phillips C, Nannenga B, Timofeev O, Donehower LA, Anderson CW, Appella E, Fornace AJJr. 2004. Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nat Genet 36: 343-350.
7. Cargnello M, Roux PP. 2011. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 75: 50-83.
8. Cavaliere F, Urra O, Alberdi E, Matute C. 2012. Oligodendrocyte differentiation from adult multipotent stem cells is modulated by glutamate. Cell Death Dis 3: e268.
9. Chao JI, Yang JL. 2001. Opposite roles of ERK and p38 mitogen-activated protein kinases in cadmium-induced genotoxicity and mitotic arrest. Chem Res Toxicol 14: 1193-1202.
10. Chew LJ, Coley W, Cheng Y, Gallo V. 2010. Mechanisms of regulation of oligodendrocyte development by p38 mitogen-activated protein kinase. J Neurosci 30: 11011-11027.
11. Clark GJ, Westwick JK, Der CJ. 1997. p120 GAP modulates Ras activation of Jun kinases and transformation. J Biol Chem 272: 1677-1681.
12. Crockford D. 2007. Development of thymosin beta4 for treatment of patients with ischemic heart disease. Ann N Y Acad Sci 1112: 385-395.
13. Cuadrado A, Nebreda AR. 2010. Mechanisms and functions of p38 MAPK signalling. Biochem J 429: 403-417.
14. Davis RJ. 2000. Signal transduction by the JNK group of MAP kinases. Cell 103: 239-252.
15. Dell'Albani P, Kahn MA, Cole R, Condorelli DF, Giuffrida-Stella AM, de Vellis J. 1998. Oligodendroglial survival factors, PDGF-AA and CNTF, activate similar JAK/STAT signaling pathways. J Neurosci Res 54: 191-205.
16. Fragoso G, Haines JD, Roberston J, Pedraza L, Mushynski WE, Almazan G. 2007. p38 mitogen-activated protein kinase is required for central nervous system myelination. Glia 55: 1531-1541.
17. Franklin RJ. 2002. Why does remyelination fail in multiple sclerosis? Nat Rev Neurosci 3: 705-714.
18. Franklin RJ, Ffrench-Constant C. 2008. Remyelination in the CNS: From biology to therapy. Nat Rev Neurosci 9: 839-855.
19. Freeman KW, Bowman BR, Zetter BR. 2011. Regenerative protein thymosin beta-4 is a novel regulator of purinergic signaling. FASEB J 25: 907-915.
20. Goldstein AL, Hannappel E, Kleinman HK. 2005. Thymosin beta4: Actin-sequestering protein moonlights to repair injured tissues. Trends Mol Med 11: 421-429.
21. Goldstein AL, Hannappel E, Sosne G, Kleinman HK. 2012. Thymosin beta4: A multi-functional regenerative peptide. Basic properties and clinical applications. Expert Opin Biol Ther 12: 37-51.
22. Haines JD, Fragoso G, Hossain S, Mushynski WE, Almazan G. 2008. p38 Mitogen-activated protein kinase regulates myelination. J Mol Neurosci 35: 23-33.
23. Hermann A, Suess C, Fauser M, Kanzler S, Witt M, Fabel K, Schwarz J, Hoglinger GU, Storch A. 2009. Rostro-caudal gradual loss of cellular diversity within the periventricular regions of the ventricular system. Stem Cells 27: 928-941.
24. Ho JH, Chuang CH, Ho CY, Shih YR, Lee OK, Su Y. 2007. Internalization is essential for the antiapoptotic effects of exogenous thymosin beta-4 on human corneal epithelial cells. Invest Ophthalmol Vis Sci 48: 27-33.
25. Huff T, Rosorius O, Otto AM, Muller CS, Ballweber E, Hannappel E, Mannherz HG. 2004. Nuclear localisation of the G-actin sequestering peptide thymosin beta4. J Cell Sci 117(Pt 22): 5333-5341.
26. Hui L, Bakiri L, Mairhorfer A, Schweifer N, Haslinger C, Kenner L, Komnenovic V, Scheuch H, Beug H, Wagner EF. 2007. p38alpha suppresses normal and cancer cell proliferation by antagonizing the JNK-c-Jun pathway. Nat Genet 39: 741-749.
27. Jessen KR, Mirsky R. 2008. Negative regulation of myelination: relevance for development, injury, and demyelinating disease. Glia 56: 1552-1565.
28. Kim Y, Rice AE, Denu JM. 2003. Intramolecular dephosphorylation of ERK by MKP3. Biochemistry 42: 15197-151207.
29. Klinghoffer RA, Hamilton TG, Hoch R, Soriano P. 2002. An allelic series at the PDGFalphaR locus indicates unequal contributions of distinct signaling pathways during development. Dev Cell 2: 103-113.
30. Kyriakis JM, Avruch J. 2001. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81: 807-869.
31. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, Green D, McNulty D, Blumenthal MJ, Heys JR, Landvatter SW, Strickler JE, McLaughlin MM, Siemens IR, Fisher SM, Livi GP, White JR, Adams JL, Young PR. 1994. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372: 739-746.
32. Liu XS, Chopp M, Zhang RL, Hozeska-Solgot A, Gregg SC, Buller B, Lu M, Zhang ZG. 2009. Angiopoietin 2 mediates the differentiation and migration of neural progenitor cells in the subventricular zone after stroke. J Biol Chem 284: 22680-22689.
33. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
34. Malinda KM, Sidhu GS, Mani H, Banaudha K, Maheshwari RK, Goldstein AL, Kleinman HK. 1999. Thymosin beta4 accelerates wound healing. J Invest Dermatol 113: 364-368.
35. Maruyama M, Sudo T, Kasuya Y, Shiga T, Hu B, Osada H. 2000. Immunolocalization of p38 MAP kinase in mouse brain. Brain Res 887: 350-358.
36. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. 2006. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26: 7907-7918.
37. Mora CA, Baumann CA, Paino JE, Goldstein AL, Badamchian M. 1997. Biodistribution of synthetic thymosin beta 4 in the serum, urine, and major organs of mice. Int J Immunopharmacol 19: 1-8.
38. Morris DC, Chopp M, Zhang L, Lu M, Zhang ZG. 2010. Thymosin beta4 improves functional neurological outcome in a rat model of embolic stroke. Neuroscience 169: 674-682.
39. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Baron-Van Evercooren A. 2008. The role of SVZ-derived neural precursors in demyelinating diseases: From animal models to multiple sclerosis. J Neurol Sci 265: 26-31.
40. Nicolay DJ, Doucette JR, Nazarali AJ. 2007. Transcriptional control of oligodendrogenesis. Glia 55: 1287-1299.
41. Paez PM, Garcia CI, Davio C, Campagnoni AT, Soto EF, Pasquini JM. 2004. Apotransferrin promotes the differentiation of two oligodendroglial cell lines. Glia 46: 207-217.
42. Parkinson DB, Bhaskaran A, Arthur-Farraj P, Noon LA, Woodhoo A, Lloyd AC, Feltri ML, Wrabetz L, Behrens A, Mirsky R, Jesson KR. 2008. c-Jun is a negative regulator of myelination. J Cell Biol 181: 625-637.
43. Qi X, Tang J, Pramanik R, Schultz RM, Shirasawa S, Sasazuki T, Han J, Chen G. 2004. p38 MAPK activation selectively induces cell death in K-ras-mutated human colon cancer cells through regulation of vitamin D receptor. J Biol Chem 279: 22138-22144.
44. Roux PP, Blenis J. 2004. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68: 320-344.
45. Safer D, Elzinga M, Nachmias VT. 1991. Thymosin beta 4 and Fx, an actin-sequestering peptide, are indistinguishable. J Biol Chem 266: 4029-4032.
46. Sanai N, Alvarez-Buylla A, Berger MS. 2005. Neural stem cells and the origin of gliomas. N Engl J Med 353: 811-822.
47. Sanders MC, Goldstein AL, Wang YL. 1992. Thymosin beta 4 (Fx peptide) is a potent regulator of actin polymerization in living cells. Proc Natl Acad Sci U S A 89: 4678-4682.
48. Santra M, Katakowski M, Zhang RL, Zhang ZG, Meng H, Jiang F, Chopp M. 2006a. Protection of adult mouse progenitor cells and human glioma cells by de novo decorin expression in an oxygen- and glucose-deprived cell culture model system. J Cereb Blood Flow Metab 26: 1311-1322.
49. Santra M, Liu XS, Santra S, Zhang J, Zhang RL, Zhang ZG, Chopp M. 2006b. Ectopic expression of doublecortin protects adult rat progenitor cells and human glioma cells from severe oxygen and glucose deprivation. Neuroscience 142: 739-752.
50. Santra M, Zhang X, Santra S, Jiang F, Chopp M. 2006c. Ectopic doublecortin gene expression suppresses the malignant phenotype in glioblastoma cells. Cancer Res 66: 11726-11735.
51. Sim FJ, Zhao C, Penderis J, Franklin RJ. 2002. The age-related decrease in CNS remyelination efficiency is attributable to an impairment of both oligodendrocyte progenitor recruitment and differentiation. J Neurosci 22: 2451-2459.
52. Smart N, Risebro CA, Melville AA, Moses K, Schwartz RJ, Chien KR, Riley PR. 2007. Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 445: 177-182.
53. Sosne G, Qiu P, Kurpakus-Wheater M. 2007. Thymosin beta-4 and the eye: I can see clearly now the pain is gone. Ann N Y Acad Sci 1112: 114-122.
54. Tanaka K, Nogawa S, Suzuki S, Dembo T, Kosakai A. 2003. Upregulation of oligodendrocyte progenitor cells associated with restoration of mature oligodendrocytes and myelination in peri-infarct area in the rat brain. Brain Res 989: 172-179.
55. Westwick JK, Cox AD, Der CJ, Cobb MH, Hibi M, Karin M, Brenner DA. 1994. Oncogenic Ras activates c-Jun via a separate pathway from the activation of extracellular signal-regulated kinases. Proc Natl Acad Sci U S A 91: 6030-6034.
56. Xiong Y, Mahmood A, Meng Y, Zhang Y, Zhang ZG, Morris DC, Chopp M. 2010. Treatment of traumatic brain injury with thymosin beta(4) in rats. J Neurosurg 114: 102-115.
57. Zhang J, Zhang ZG, Morris D, Li Y, Roberts C, Elias SB, Chopp M. 2009. Neurological functional recovery after thymosin beta4 treatment in mice with experimental auto encephalomyelitis. Neuroscience 164: 1887-1893.
58. Zhang R, Zhang Z, Wang L, Wang Y, Gousev A, Zhang L, Ho KL, Morshead C, Chopp M. 2004. Activated neural stem cells contribute to stroke-induced neurogenesis and neuroblast migration toward the infarct boundary in adult rats. J Cereb Blood Flow Metab 24: 441-448.
59. Zhang ZG, Chopp M. 2009. Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol 8: 491-500.
60. Zhao Y, Qiu F, Xu S, Yu L, Fu G. 2011. Thymosin beta4 activates integrin-linked kinase and decreases endothelial progenitor cells apoptosis under serum deprivation. J Cell Physiol 226: 2798-2806.