Anti-apoptotic function of thymosin-β in developing chick spinal motoneurons

Biochemical and Biophysical Research Communications

Volumn 346, Issue 3, 2006, Pages 872-878

  Choi, So Yoen ^a   Kim, Dong Ki ^a   Eun, Bokkee ^b   Kim, Kyungjin ^b   Sun, Woong ^a   Kim, Hyun ^a  

^a Center for Environmental Toxico Genomics and Proteomics   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Chick embryo; Jun; Motoneuron; Programmed cell death; Thymosin

Indexed keywords

ACTIN; ISOPROTEIN; THYMOSIN; THYMOSIN BETA 15; THYMOSIN BETA10; THYMOSIN BETA4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROTECTION; CHICK; CHICK EMBRYO; CONTROLLED STUDY; ELECTROPORATION; GENE OVEREXPRESSION; IN VIVO STUDY; LIMB BUD; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPINAL CORD MOTONEURON; STATISTICAL SIGNIFICANCE;

ACTINS; ANIMALS; APOPTOSIS; CELL PROLIFERATION; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIMB BUD; MOTOR NEURONS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-JUN; RATS; SPINAL CORD; THYMOSIN;

SPONDIAS PURPUREA;

EID: 33745209636     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.05.207     Document Type: Article

References (41)

1. Koutrafouri V., Leondiadis L., Avgoustakis K., Livaniou E., Czarnecki J., Ithakissios D.S., and Evangelatos G.P. Effect of thymosin peptides on the chick chorioallantoic membrane angiogenesis model. Biochim. Biophys. Acta 1568 (2001) 60-66
2. Bock-Marquette I., Saxena A., White M.D., Dimaio J.M., and Srivastava D. Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 432 (2004) 466-472
3. Huff T., Otto A.M., Muller C.S., Meier M., and Hannappel E. Thymosin beta4 is released from human blood platelets and attached by factor XIIIa (transglutaminase) to fibrin and collagen. FASEB J. 16 (2002) 691-696
4. Malinda K.M., Sidhu G.S., Mani H., Banaudha K., Maheshwari R.K., Goldstein A.L., and Kleinman H.K. Thymosin beta4 accelerates wound healing. J. Invest. Dermatol. 113 (1999) 364-368
5. Yu F.X., Lin S.C., Morrison-Bogorad M., and Yin H.L. Effects of thymosin beta 4 and thymosin beta 10 on actin structures in living cells. Cell Motil. Cytoskeleton 27 (1994) 13-25
6. Chakravatri A., Zehr E.M., Zietman A.L., Shipley W.U., Goggins W.B., Finkelstein D.M., Young R.H., Chang E.L., and Wu C.L. Thymosin beta-15 predicts for distant failure in patients with clinically localized prostate cancer-results from a pilot study. Urology 55 (2000) 635-638
7. Dathe V., and Brand-Saberi B. Expression of thymosin beta4 during chick development. Anat. Embryol. (Berl.) 208 (2004) 27-32
8. Huff T., Muller C.S., Otto A.M., Netzker R., and Hannappel E. Beta-Thymosins, small acidic peptides with multiple functions. Int. J. Biochem. Cell Biol. 33 (2001) 205-220
9. Young J.D., Lawrence A.J., MacLean A.G., Leung B.P., McInnes I.B., Canas B., Pappin D.J., and Stevenson R.D. Thymosin beta 4 sulfoxide is an anti-inflammatory agent generated by monocytes in the presence of glucocorticoids. Nat. Med. 5 (1999) 1424-1427
10. Goodall G.J., Morgan J.I., and Horecker B.L. Thymosin beta 4 in cultured mammalian cell lines. Arch. Biochem. Biophys. 221 (1983) 598-601
11. Safer D., and Nachmias V.T. Beta thymosins as actin binding peptides. Bioessays 16 (1994) 590
12. Eadie J.S., Kim S.W., Allen P.G., Hutchinson L.M., Kantor J.D., and Zetter B.R. C-terminal variations in beta-thymosin family members specify functional differences in actin-binding properties. J. Cell. Biochem. 77 (2000) 277-287
13. Choe J., Sun W., Yoon S.Y., Rhyu I.J., Kim E.H., and Kim H. Effect of thymosin beta15 on the branching of developing neurons. Biochem. Biophys. Res. Commun. 331 (2005) 43-49
14. Roth L.W., Bormann P., Bonnet A., and Reinhard E. Beta-thymosin is required for axonal tract formation in developing zebrafish brain. Development 126 (1999) 1365-1374
15. Carpintero P., Anadon R., Diaz-Regueira S., and Gomez-Marquez J. Expression of thymosin beta4 messenger RNA in normal and kainate-treated rat forebrain. Neuroscience 90 (1999) 1433-1444
16. Vartiainen N., Pyykonen I., Hokfelt T., and Koistinaho J. Induction of thymosin beta(4) mRNA following focal brain ischemia. Neuroreport 7 (1996) 1613-1616
17. Sosne G., Siddiqi A., and Kurpakus-Wheater M. Thymosin-beta4 inhibits corneal epithelial cell apoptosis after ethanol exposure in vitro. Invest. Ophthalmol. Vis. Sci. 45 (2004) 1095-1100
18. Hamburger V. The stage series of the chick embryo. Dev. Dyn. 195 (1992) 273-275
19. Sun W., Gould T.W., Newbern J., Milligan C., Choi S.Y., Kim H., and Oppenheim R.W. Phosphorylation of c-Jun in avian and mammalian motoneurons in vivo during programmed cell death: an early reversible event in the apoptotic cascade. J. Neurosci. 25 (2005) 5595-5603
20. Caldero J., Prevette D., Mei X., Oakley R.A., Li L., Milligan C., Houenou L., Burek M., and Oppenheim R.W. Peripheral target regulation of the development and survival of spinal sensory and motor neurons in the chick embryo. J. Neurosci. 18 (1998) 356-370
21. Liu H.G., Hong G.X., Wang F.B., and Chen F. Motoneurotrophins derived from limb buds protect the motoneurons in anterior spinal cord after nerve injury and promote nerve regeneration. Brain Res. 800 (1998) 216-226
22. Llado J., Caldero J., Ribera J., Tarabal O., Oppenheim R.W., and Esquerda J.E. Opposing effects of excitatory amino acids on chick embryo spinal cord motoneurons: excitotoxic degeneration or prevention of programmed cell death. J. Neurosci. 19 (1999) 10803-10812
23. Ham J., Eilers A., Whitfield J., Neame S.J., and Shah B. c-Jun and the transcriptional control of neuronal apoptosis. Biochem. Pharmacol. 60 (2000) 1015-1021
24. Miller T.M., Moulder K.L., Knudson C.M., Creedon D.J., Deshmukh M., Korsmeyer S.J., and Johnson Jr. E.M. Bax deletion further orders the cell death pathway in cerebellar granule cells and suggests a caspase-independent pathway to cell death. J. Cell Biol. 139 (1997) 205-217
25. Dudek H., Datta S.R., Franke T.F., Birnbaum M.J., Yao R., Cooper G.M., Segal R.A., Kaplan D.R., and Greenberg M.E. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275 (1997) 661-665
26. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., and Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91 (1997) 231-241
27. Devineni N., Minamide L.S., Niu M., Safer D., Verma R., Bamburg J.R., and Nachmias V.T. A quantitative analysis of G-actin binding proteins and the G-actin pool in developing chick brain. Brain Res. 823 (1999) 129-140
28. Voisin P.J., Pardue S., and Morrison-Bogorad M. Developmental characterization of thymosin beta 4 and beta 10 expression in enriched neuronal cultures from rat cerebella. J. Neurochem. 64 (1995) 109-120
29. Gomez-Marquez J., and Anadon R. The beta-thymosins, small actin-binding peptides widely expressed in the developing and adult cerebellum. Cerebellum 1 (2002) 95-102
30. Anadon R., Rodriguez Moldes I., Carpintero P., Evangelatos G., Livianou E., Leondiadis L., Quintela I., Cervino M.C., and Gomez-Marquez J. Differential expression of thymosins beta(4) and beta(10) during rat cerebellum postnatal development. Brain Res. 894 (2001) 255-265
31. Carpintero P., Anadon R., and Gomez-Marquez J. Expression of the thymosin beta10 gene in normal and kainic acid-treated rat forebrain. Brain Res. Mol. Brain Res. 70 (1999) 141-146
32. Kerr J.F., Wyllie A.H., and Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26 (1972) 239-257
33. Yamazaki Y., Tsuruga M., Zhou D., Fujita Y., Shang X., Dang Y., Kawasaki K., and Oka S. Cytoskeletal disruption accelerates caspase-3 activation and alters the intracellular membrane reorganization in DNA damage-induced apoptosis. Exp. Cell Res. 259 (2000) 64-78
34. Cabado A.G., Leira F., Vieytes M.R., Vieites J.M., and Botana L.M. Cytoskeletal disruption is the key factor that triggers apoptosis in okadaic acid-treated neuroblastoma cells. Arch. Toxicol. 78 (2004) 74-85
35. Dahm L.M., and Landmesser L.T. The regulation of intramuscular nerve branching during normal development and following activity blockade. Dev. Biol. 130 (1988) 621-644
36. Oppenheim R.W., Caldero J., Cuitat D., Esquerda J., Ayala V., Prevette D., and Wang S. Rescue of developing spinal motoneurons from programmed cell death by the GABA(A) agonist muscimol acts by blockade of neuromuscular activity and increased intramuscular nerve branching. Mol. Cell. Neurosci. 22 (2003) 331-343
37. Goldstein A.L., Hannappel E., and Kleinman H.K. Thymosin beta4: actin-sequestering protein moonlights to repair injured tissues. Trends Mol. Med. 11 (2005) 421-429
38. Roth L.W., Bormann P., Wiederkehr C., and Reinhard E. Beta-thymosin, a modulator of the actin cytoskeleton is increased in regenerating retinal ganglion cells. Eur. J. Neurosci. 11 (1999) 3488-3498
39. Bao L., Loda M., Janmey P.A., Stewart R., Anand-Apte B., and Zetter B.R. Thymosin beta 15: a novel regulator of tumor cell motility upregulated in metastatic prostate cancer. Nat. Med. 2 (1996) 1322-1328
40. Philp D., Huff T., Gho Y.S., Hannappel E., and Kleinman H.K. The actin binding site on thymosin beta4 promotes angiogenesis. FASEB J. 17 (2003) 2103-2105
41. Mohring T., Kellmann M., Jurgens M., and Schrader M. Top-down identification of endogenous peptides up to 9 kDa in cerebrospinal fluid and brain tissue by nanoelectrospray quadrupole time-of-flight tandem mass spectrometry. J. Mass Spectrom. 40 (2005) 214-226