The β-thymosins: Intracellular and extracellular activities of a versatile actin binding protein family

Cell Motility and the Cytoskeleton

Volumn 66, Issue 10, 2009, Pages 839-851

  Mannherz, Hans Georg ^a,b   Hannappel, Ewald ^c  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Actin; ADF cofilin; Beta thymosins; Formins; WH2 domain

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; BETA THYMOSIN; BETA4 THYMOSIN; COFILIN; G ACTIN; MONOMER; THYMOSIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; AMINO TERMINAL SEQUENCE; ANGIOGENESIS; CELL ACTIVATION; COMPLEX FORMATION; CONFERENCE PAPER; CYTOPLASM; CYTOSKELETON; DYNAMICS; EUKARYOTIC CELL; HAIR GROWTH; HEART PROTECTION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; MOLECULAR WEIGHT; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FAMILY; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY; THYMUS; WOUND HEALING;

ACTINS; AMINO ACID SEQUENCE; CYTOSKELETON; MICROFILAMENTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; THYMOSIN;

EUKARYOTA;

EID: 70349413077     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20371     Document Type: Conference Paper

References (93)

1. Aguda AH, Xue B, Irobi E, Préat T, Robinson RC. 2006. The structural basis of actin interaction with multiple WH2/beta-thymosin motif-containing proteins. Structure 14:469-476. (Pubitemid 43363480)
2. Andrianantoandro E, Pollard TD. 2006. Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24:13-23. (Pubitemid 44466682)
3. Au JK, Olivares AO, Henn A, Cao W, Safer D, De La Cruz EM. 2008. Widely distributed residues in thymosin β4 are critical for actin binding. Biochemistry 47:4181-4188.
4. Badamchian M, Damavandy AA, Damavandy H, Wadhwa S, Katz B, Goldstein AL. 2007. Identification and quantification of thymosin β4 in human saliva and tears. Ann N Y Acad Sci 1112:458-465. (Pubitemid 47598681)
5. Ballweber E, Hannappel E, Niggemeyer B, Mannherz HG. 1994. Induction of the repolymerization of actin from the actin: thymosin β4 complex by calcium, phalloidin, free ends of filamentous actin, skeletal muscle subfragment 1 and chicken intestinal myosin I. Eur J Biochem 223:419-426. (Pubitemid 24244188)
6. 4 on actin by competition with Gactin binding proteins indicates negative cooperativity between binding sites located on subdomains 1 and 2 of actin. Biochem J 327:787-793.
7. Ballweber E, Giehl C, Hannappel E, Huff T, Jockusch BM, Mannherz HG. 1998. Plant profilin induces actin polymerisation from actin: Thymosin complexes and competes directly with β-thymosins and with negative co-operativity with DNase I for binding to actin. FEBS Lett 425:251-255. (Pubitemid 28178901)
8. Ballweber E, Hannappel E, Huff T, Stephan H, Haener M, Taschner N, Stoffler D, Aebi U, Mannherz HG. 2002. Polymerisation of chemically cross-linked actin: Thymosin β4 complex to filamentous actin: Alteration in helical parameters and visualisation of thymosin β4 binding on F-actin. J Mol Biol 315:613-625. (Pubitemid 34729313)
9. Bao L, Loda M, Janmey PA, Stewart R, Anand-Apte B, Zeiter BR. 1996. Thymosin beta-15: A novel regulator of tumor cell motility upregulated in metastatic prostate cancer. Nat Med 2:1322-1328. (Pubitemid 26401734)
10. Bednarek R, Boncela J, Smolarcyk K, Cierniewska-Cieslak A, Wyroba E, Cierniewski CS. 2007. Ku80 as a novel receptor for thymosin β4 that mediates its intracellular activity different from G actin sequestering. J Biol Chem 283:1534-1544.
11. Birbach A. 2008. Profilin, a multi-modal regulator of neuronal plasticity. Bioessays 30:994-1002.
12. Bock-Marquette I, Saxena A, White MD, DiMaio JM, Srivastava D. 2004. Thymosin b4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature 432:466-472. (Pubitemid 39576522)
13. Boquet I, Boujemaa R, Carlier MF, Préat T. 2000. Ciboulot regulates actin assembly during Drosophila brain metamorphosis. Cell 102:797-808.
14. 4 and protein in human wound fluid after abdominal surgery. Ann N Y Acad Sci 1112:418-424.
15. Brieger A, Plotz G, Zeuzam S, Trojan J. 2007. Thymosin beta 4 expression and nuclear transport are regulated by hMLH1. Biochem Biophys Res Commun 364:731-736. (Pubitemid 350103693)
16. Califano D, Monaco C, Santelli G, Giuliano A, Veronese ML, Berlingieri MT, de Franciscis V, Berger N, Trapasso F, Santoro M. 1998. Thymosin beta-10 gene overexpression correlated with the highly malignant neoplastic phenotype of transformed thyroid cells in vivo and in vitro. Cancer Res 58:823-828. (Pubitemid 28099498)
17. Carlier MF, Pantaloni D. 1994. Actin assembly in response to extracellular signals: Role of capping proteins, thymosin beta-4 and profilin. Semin Cell Biol 5:183-191. (Pubitemid 124003284)
18. Carlier M-F, Jean C, Rieger K, Lenfant M, Pantaloni D. 1993. Modulation of the interaction between G-actin and thymosin β4 by the ATP/ADP ratio: Possible implication in the regulation of actin dynamics. Proc Natl Acad Sci USA 90:5034-5038. (Pubitemid 23182970)
19. Carlier MF, Didry D, Erk I, Lepault J, Van Troys ML, Vandekerckhove J, Perelroizen I, Yin H, Doi Y, Pantaloni D. 1996. Tbeta 4 is not a simple G-actin sequestering protein and interacts with F-actin at high concentration. J Biol Chem 271:9231-9239. (Pubitemid 26137324)
20. Cassimeris L, Safer D, Nachmias VT, Zigmond SH. 1992. Thymosin β4 sequesters the majority of G-actin in resting human polymorphonuclear leukocytes. J Cell Biol 119:1261-1270.
21. Cha HJ, Jeong MJ, Kleinman HK. 2003. Role of thymosin beta4 in tumor metastasis and angiogenesis. J Natl Cancer Inst 95: 1674-1680. (Pubitemid 37509076)
22. Chakravatri A, Zehr EM, Zietman AL, Shipley WU, Goggins WB, Finkelstein DM, Young RH, Chang EL, Wu CL. 2000. Thymosin beta-15 predicts for distant failure in patients with clinically localized prostate cancer-results from a pilot study. Urology 55:635-638.
23. Chaudhary A. 1998. Probing the phosphoinositide 4, 5-bisphosphate binding site of human profilin I. Chem Biol 5:273-281. (Pubitemid 28259742)
24. Chhabra ES, Higgs HN. 2007. The many faces of actin: Matching assembly factors with cellular structures. Nat Cell Biol 9: 1110-1119.
25. Cohen MV, Downey JM. 2008. Adenosine: Trigger and mediator of cardioprotection. Basic Res Cardiol 103:203-215.
26. Condeelis J. 2001. How is actin polymerization nucleated in vivo? Trends Cell Biol 11:288-293.
27. Dominguez R. 2007. The β-thymosin/WH2 fold. Multifunctionality and structure. Ann N Y Acad Sci 1112:86-94.
28. Etienne-Manneville S, Hall A. 2002. Rho GTPases in cell biology. Nature 420:629-635.
29. Galea CA, Pagala VR, Obenauer JC, Park CG, Slaughter CA, Kriwacki RW. 2006. Proteomic studies of the intrinsically unstructured mammalian proteome. J Proteome Res 10:2839-2848.
30. Goldschmidt-Clermont PJ, Kim JW, Machesky LM, Rhee SG, Pollard TD. 1991. Regulation of phospholipase C-gamma 1 by profilin and tyrosine phosphorylation. Science 251:1231-1233. (Pubitemid 21926219)
31. Goldschmidt-Clermont PJ, Kim JW, Machesky LM, Rhee 1992. The control actin nucleotide exchange by thymsoin β4 and profilin. A potential regulatory mechanism for actin polymerisation in cells. Mol Biol Cell 3:1015-1024.
32. 4: Actin sequestering protein moonlights to repair injured tissues. Trends Mol Med 11:421-429.
33. Golla R, Philp N, Safer D, Chintapalli J, Hoffman R, Collins L, Nachmias VT. 1997. Co-ordinate regulation of the cytoskeleton in 3T3 cells overexpressing thymosin-β4. Cell Motil Cytoskeleton 38:187-200. (Pubitemid 27430424)
34. Hall AK. 1991. Differential expression of thymosin genes in human tumors and in the developing human kidney. Int J Cancer 48:672-677.
35. Hannappel E, van Kampen M. 1987. Determination of thymosin beta 4 in human blood cells and serum. J Chromatogr 397:279-285. (Pubitemid 17109698)
36. Hannappel E, Huff T. 2003. The thymosins, Prothymosin a, parathymosin, and β-thymosins: structure and function. Vitam Horm 66:257-296. (Pubitemid 137640819)
37. Hasko G, Linden J, Cronstein B, Pacher P. 2008. Adenosine receptors: Therapeutic aspects for inflammatory and immune diseases. Nat Rev Drug Discov 7:759-770.
38. Hertzog M, van Heijenoort C, Didry D, Gaudier M, Coutant J, Gigant B, Didelot G, Préat T, Knossow M, Guittet E, Carlier MF. 2004. The beta-thymosin/WH2 domain; Structural basis for the switch from inhibition to promotion of actin assembly. Cell 117:611-623. (Pubitemid 38692527)
39. Huff T, Müller CSG, Otto AM, Netzker R, Hannappel E. 2001. β-Thymosins, small acidic peptides with multiple functions. Int J Biochem Cell Biol 33:205-220. (Pubitemid 32304390)
40. Huff T, Otto AM, Müller CS, Meier M, Hannappel E. 2002. Thymosin β4 is released from human blood platelets and attached by factor XIIIa (transglutaminase) to fibrin and collagen. FASEB J 16:691-696. (Pubitemid 34465433)
41. Huff T, Rosorius O, Otto AM, Müller CSG, Ballweber E, Hannappel E, Mannherz HG. 2004. Nuclear localisation of the Gactin sequestering peptide thymosin β4. J Cell Sci 117:5333-5341. (Pubitemid 39562495)
42. Huff T, Müller CS, Hannappel E. 2007. Thymosin beta4 is not always the main beta-thymosin in mammalian platelets. Ann N Y Acad Sci 1112:451-457. (Pubitemid 47598667)
43. Inzitari R, Cabras T, Pisano E, Fanali C, Manconi B, Scarano E, Fiorita A, Paludetti G, Manni A, Nemolato S, Faa G, Castagnola M, Messana I. 2009. HPLC-ESI-MS analysis of oral human fluids reveals that gingival crevicular fluid is the main source of oral thymosins beta(4) and beta(10). J Sep Sci 32:57-63.
44. Irobi E, Aguda AH, Larsson M, Guerin C, Yin HL, Burtnick LD, Blanchoin L, Robinson RC. 2004. Structural basis of actin sequestration by thymosin-beta4: Implications for WH2 proteins. EMBO J 23:3599-3608. (Pubitemid 39336282)
45. Junot C, Nicolet L, Ezan E, Gonzales MF, Menard J, Azizi M. 1999. Effect of angiotensin-converting enzyme inhibition on plasma, urine, and tissue concentrations of hemoregulatory peptide acetyl-Ser-Asp-Lys-Pro in rats. J Pharmacol Exp Ther 291: 982-987.
46. Kabsch W, Mannherz HG, Pai E, Suck D, Holmes KC. 1990. The atomic structure of actin:DNase I complex. Nature 347:37-44.
47. Kobayashi T, Okada F, Fujii N, Tomita N, Ito S, Tazawa H, Aoyama T, Choi SK, Shibata T, Fujita H. 2002. Thymosin beta-4 regulates motility and metastasis of malignant mouse fibrosarcoma cells. Am J Pathol 160:869-882. (Pubitemid 34224577)
48. Koerner C, Guan T, Gerace L, Cingolani G. 2003. Synergy of silent and hot spot mutations in importin β reveals a dynamic mechanism for recognition of a nuclear localization signal. J Biol Chem 278:16216-16221. (Pubitemid 36799745)
49. Kovar DR, Pollard TD. 2004. Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc Natl Acad Sci USA 101:14725-14730.
50. Lai FPL, Szczodrak M, Block J, Faix J, Breitsprecher D, Mannherz HG, Stradal TE, Dunn GA, Small JV, Rottner K. 2008. Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J 27:982-992.
51. Lassing I, Lindberg U. 1985. Specific interaction between phosphatidylinositol 4,5-bisphosphate and profilactin. Nature 314:472-474. (Pubitemid 15145594)
52. Lassing I, Lindberg U. 1998. Evidence that the phosphatidylinositol cycle is linked to cell motility. Exp Cell Res 174:1-15.
53. MacLaughlin PJ, Gooch J, Mannherz HG, Weeds AG. 1993. Atomic structure of gelsolin segment 1 in complex with actin and the mechanism of filament severing. Nature 364:685-692. (Pubitemid 23273120)
54. 4 preferentially into the fibrin (ogen) aC-domains. Biochemistry 43:10748-10756.
55. Mannherz HG, Ballweber E, Galla M, Villard S, Granier C, Steegborn C, Schmidtmann A, Jaquet K, Pope B, Weeds AG. 2007. Mapping the ADF/cofilin binding site on monomeric actin by competitive cross-linking and peptide array: Evidence for a second binding site on monomeric actin. J Mol Biol 366:745-755. (Pubitemid 46175883)
56. Mannherz HG, Dansranjavin T, Gremm D, Mazur A, Sokoll A, Hannappel E, Jockusch B. 2008. Thymosin beta 4 inhibits ADF/ cofilin stimulated F-actin cycling and cell migration: Reversal by the FH2-domain of mDia1. Eur J Cell Biol 87(Suppl. 58):23-23
57. Metzler WJ. 1994. Identification of the poly-L-proline binding site on human profilin. J Biol Chem 269:4620-4625. (Pubitemid 24237834)
58. Mockrin SC, Korn ED. 1980. Acanthamoeba profilin interacts with Gactin to increase the rate of exchange of actin-bound adenosine 5′-triphosphate. Biochemistry 19:5359-5362.
59. Nachmias VT, Cassimeris L, Golla R, Safer D. 1993. Thymosin beta 4 (T beta 4) in activated platelets. Eur J Cell Biol 61:314-320.
60. Naylor PH, McClure JE, Spangelo BL, Low TL, Goldstein AL. 1984. Immunochemical studies on thymosin: Radioimmunoassay of thymosin β 4. Immunopharmacology 7:9-16.
61. Nolen BJ, Littlefield RS, Pollard TD. 2004. Crystal structures of actinrelated protein 2/3 complex with bound ATP or ADP. Proc Natl Acad Sci USA 101:15627-15632.
62. Paunola E, Mattila PK, Lappalainen P. 2002.WH2 domain: A small versatile adaptor for actin monomers. FEBS Lett 57:231-232. (Pubitemid 34242984)
63. Pantaloni D, Carlier M-F. 1993. How profilin promotes actin filament assembly in the presence of thymosin beta 4. Cell 75:1007-1014. (Pubitemid 24014557)
64. Plavina T, Hincapie M, Wakshull E, Subramanyam M, Hancock WS. 2008. Increased plasma concentrations of cytoskeletal and Ca2+-binding proteins and their peptides in psoriasis patients. Clin Chem 54:1805-1814.
65. Pollard TD, Weeds AG. 1984. The rate constant for ATP hydrolysis by polymerized actin. FEBS Lett 170:94-98.
66. Pollard TD, Cooper JA. 1986. Actin and actin-binding proteins: A critical evaluation of mechanisms and functions. Annu Rev Biochem 55:987-1035.
67. Pollard TD, Borisy GG. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453-465.
68. Quinlan ME, Heuser JE, Kerkhoff E, Mullins RD. 2005. Drosophila Spire is an actin nucleation factor. Nature 433:382-388. (Pubitemid 40203312)
69. Romer S, Le Clainche C, Didry D, Egile C, Pantaloni D, Carlier M-F. 2004. Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119:419-429. (Pubitemid 39423843)
70. Roy P, Rajfur Z, Jones D, Marriot G, Loew L, Jacobson K. 2001. Local photorelease of caged thymosin β4 in locomoting keratocytes causes cell turning. J Cell Biol 153:1035-1047. (Pubitemid 34289242)
71. Safer D, Golla R, Nachmias VT. 1990. Isolation of a 5-kDa actinsequestering peptide from human blood platelets. Proc Natl Acad Sci USA 87:2536-2540. (Pubitemid 20141773)
72. Safer D, Elzinga M, Nachmias VT. 1991. Thymosin beta-4 and Fxan actin-sequestering peptide, are indistinguishable. J Biol Chem 266:4029-4032. (Pubitemid 21909312)
73. Safer D, Sosnick TR, Elzinga M. 1997. Thymosin β4 binds actin in an extended conformation and contacts both the barbed and pointed ends. Biochemistry 36:5806-5816. (Pubitemid 27214932)
74. Sanger JM, Golla R, Safer D, Choi JK, Yu KR, Sanger JW, Nachmias VT. 1995. Increasing intracellular concentrations of thymosin beta 4 in PtK2 cells: Effects on stress fibers, cytokinesis, and cell spreading. Cell Motil Cytoskeleton 31:307-322.
75. Schutt CE, Myslik JC, Rozycki MD, Goonesekere NC, Lindberg U. 1993. The structure of crystalline profilin-β-actin. Nature 365:810-816.
76. Sosne G, Christopherson PL, Barrett RP, Fridman R. 2005. Thymosin β4 modulates corneal matrix metalloproteinase levels and polymorphonuclear cell infiltration after alkali injury. Invest Ophthalmol Vis Sci 46:2388-2395. (Pubitemid 43119484)
77. Sosne G, Albeiruti AR, Hollis B, Siddiqi A, Ellenberg D, Kurpakus- Wheater M. 2006. Thymosin β4 inhibits benzalkonium chloride- mediated apoptosis in corneal and conjunctival epithelial cells in vitro. Exp Eye Res 83:502-507. (Pubitemid 44183802)
78. Sosne G, Qiu P, Christopherson PL, Wheater MK. 2007. Thymosin β4 suppression of corneal NFkB: A potential anti-inflammatory pathway. Exp Eye Res 84:663-669. (Pubitemid 46420439)
79. Sugase K, Dyson HJ, Wright PE. 2007. Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447:1021-1025. (Pubitemid 46975749)
80. Sun HQ, Lin HL. 2007. The β-thymosin enigma. Ann N Y Acad Sci 1112:45-55.
81. Sun H-Q, Kwiatkowska K, Yin HL. 1996. Beta-thymosins are not simple actin monomer buffering proteins. J Biol Chem 271:9223-9230.
82. Tardif M, Huang S, Redmond T, Safer D, Pring M, Zigmond SH. 1995. Actin polymerization induced by GTP gamma S in permeabilized neutrophils is induced and maintained by free barbed ends. J Biol Chem 270:28075-28083.
83. Vancompernolle K, Vandekerckhove J, Bubb MR, Korn ED. 1991. The interfaces of actin and Acanthamoeba actobindin. Identification of a new actin-binding motif. J Biol Chem. 266:15427-15431.
84. Weber A. 1999. Actin binding proteins that change extent and rate of actin monomer-polymer distribution by different mechanisms. Mol Cell Biochem 190:67-74.
85. Weber A, Nachmias VT, Pennise CR, Pring M, Safer D. 1992. Interaction of thymosin β4 with muscle and platelet actin: Implications for actin sequestration in resting platelets. Biochemistry 31:6179-6185.
86. Wegner A. 1976. Head to tail polymerization of actin. J Mol Biol 108:139-150.
87. Witke W. 2004. The role of profilin complexes in cell motility and other cellular processes. Trends Cell Biol 14:461-469. (Pubitemid 39092704)
88. Wodnar-Filipowicz AW, Horecker BL. 1983. In vitro synthesis of thymosin β 4 encoded by rat spleen mRNA. Proc Natl Acad Sci USA 80:1811-1815.
89. Wodnar-Filipowicz A, Gubler U, Furuichi Y, Richardson M, Nowoswiat EF, Poonian MS, Horecker BL. 1984. Cloning and sequence analysis of cDNA for rat spleen thymosin β4. Proc Natl Acad Sci USA 81:2295-2297. (Pubitemid 14148248)
90. Yarmola EG, Parikh S, Bubb MR. 2001. Formation and implications of a ternary complex of profilin, thymosin beta 4, and actin. J Biol Chem 276:45555-45563. (Pubitemid 37370788)
91. Yu FX, Lin SC, Morrison-Bogorad M, Atkinson MAL, Yin HL. 1993. Thymosin beta-10 and Thymosin beta-4 are both actin monomer sequestering proteins. J Biol Chem 268:502-509. (Pubitemid 23021350)
92. Yu FX, Lin SC, Morrison-Bogorad M, Yin HL. 1994. Effects of thymosin beta-4 and thymosin beta-10 on actin structures in living cells. Cell Motil Cytoskeleton 27:13-25. (Pubitemid 24036377)
93. Zarbock J, Oschkinat H, Hannappel E, Kalbacher H, Voelter W, Holak TA. 1990. Solution conformation of thymosin beta 4: A nuclear magnetic resonance and simulated annealing study. Biochemistry 29:7814-7821. (Pubitemid 20281227)