Effect of a C-end rule modification on antitumor activity of thymosin α1

Biochimie

Volumn 154, Issue , 2018, Pages 99-106

  Wang, Fanwen ^a   Xu, Caoying ^a   Peng, Renhao ^a   Li, Bin ^a   Shen, Xutong ^a   Zheng, Heng ^a   Lao, Xingzhen ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

Melanoma; Thymosin 1; Tumor homing; Tumor treatment

Indexed keywords

ALPHA INTEGRIN; B7 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; INTEGRIN ALPHA V BETA 3; INTERLEUKIN 2; MHC I PROTEIN; NEUROPILIN 1; PACLITAXEL; PROTEIN; THYMOSIN ALPHA1; TRIFLUOROETHANOL; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; THYMOSIN;

ANIMAL CELL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; B16-BL6 CELL LINE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ADHESION; CELL ADHESION ASSAY; CERVICAL SPINE DISLOCATION; CIRCULAR DICHROISM; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HISTOCHEMISTRY; HYDROGEN BOND; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; INTERNALIZATION; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TARGET CELL; TISSUE NECROSIS; TUMOR GROWTH; TUMOR VOLUME; TUMOR WEIGHT; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; MELANOMA; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; MELANOMA; MICE; THYMOSIN;

EID: 85051555472     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2018.08.001     Document Type: Article

References (69)

1. Ruoslahti, E., Rajotte, D., An address system in the vasculature of normal tissues and tumors. Annu. Rev. Immunol. 18 (2000), 813–827.
2. Pellinen, T., Arjonen, A., Vuoriluoto, K., Kallio, K., Fransen, J.A., Ivaska, J., Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins. J. Cell Biol. 173 (2006), 767–780.
3. Qin, X., Yan, M., Zhang, J., Wang, X., Shen, Z., Lv, Z., Li, Z., Wei, W., Chen, W., TGFbeta3-mediated induction of Periostin facilitates head and neck cancer growth and is associated with metastasis. Sci. Rep., 6, 2016, 20587.
4. Ruoslahti, E., The RGD story: a personal account. Matrix Biol. 22 (2003), 459–465.
5. Teesalu, T., Sugahara, K.N., Kotamraju, V.R., Ruoslahti, E., C-end rule peptides mediate neuropilin-1-dependent cell, vascular, and tissue penetration. Proc. Natl. Acad. Sci. U.S.A. 106 (2009), 16157–16162.
6. Acevedo, L.M., Barillas, S., Weis, S.M., Gothert, J.R., Cheresh, D.A., Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor. Blood 111 (2008), 2674–2680.
7. Jia, H., Bagherzadeh, A., Hartzoulakis, B., Jarvis, A., Lohr, M., Shaikh, S., Aqil, R., Cheng, L., Tickner, M., Esposito, D., Harris, R., Driscoll, P.C., Selwood, D.L., Zachary, I.C., Characterization of a bicyclic peptide neuropilin-1 (NP-1) antagonist (EG3287) reveals importance of vascular endothelial growth factor exon 8 for NP-1 binding and role of NP-1 in KDR signaling. J. Biol. Chem. 281 (2006), 13493–13502.
8. Soker, S., Takashima, S., Miao, H.Q., Neufeld, G., Klagsbrun, M., Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92 (1998), 735–745.
9. Xu, H.M., Yin, R., Chen, L., Siraj, S., Huang, X., Wang, M., Fang, H., Wang, Y., An RGD-modified endostatin-derived synthetic peptide shows antitumor activity in vivo. Bioconjugate Chem. 19 (2008), 1980–1986.
10. Lao, X.Z., Li, B., Liu, M., Chen, J., Gao, X.D., Zheng, H., Increased antitumor activity of tumor-specific peptide modified thymopentin. Biochimie 107 (2014), 277–285.
11. Curnis, F., Gasparri, A., Sacchi, A., Longhi, R., Corti, A., Coupling tumor necrosis factor-alpha with alphaV integrin ligands improves its antineoplastic activity. Canc. Res. 64 (2004), 565–571.
12. Nieberler, M., Reuning, U., Reichart, F., Notni, J., Wester, H.J., Schwaiger, M., Weinmuller, M., Rader, A., Steiger, K., Kessler, H., Exploring the role of RGD-recognizing integrins in cancer. Cancers, 9, 2017.
13. Wickham, T.J., Targeting adenovirus. Gene Ther. 7 (2000), 110–114.
14. Murphy, E.A., Majeti, B.K., Barnes, L.A., Makale, M., Weis, S.M., Lutu-Fuga, K., Wrasidlo, W., Cheresh, D.A., Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 9343–9348.
15. Garaci, E., Favalli, C., Pica, F., Vallebona, P.S., Palamara, A.T., Matteucci, C., Pierimarchi, P., Serafino, A., Mastino, A., Bistoni, F., Romani, L., Rasi, G., Thymosin alpha 1 - from bench to bedside. Ann Ny Acad Sci 1112 (2007), 225–234.
16. Goldstein, A.L., Goldsten, A.L., From lab to bedside: emerging clinical applications of thymosin alpha(1). Expet Opin. Biol. Ther. 9 (2009), 593–608.
17. Romani, L., Moretti, S., Fallarino, F., Bozza, S., Ruggeri, L., Casagrande, A., Aversa, F., Bistoni, F., Velardi, A., Garaci, E., Jack of all trades: thymosin alpha 1 and its pleiotropy. Thymosins in Health and Disease I 1269 (2012), 1–6.
18. Ciancio, A., Andreone, P., Kaiser, S., Mangia, A., Milella, M., Sola, R., Pol, S., Tsianos, E., De Rosa, A., Camerini, R., McBeath, R., Rizzetto, M., Thymosin alpha-1 with peginterferon alfa-2a/ribavirin for chronic hepatitis C not responsive to IFN/ribavirin: an adjuvant role?. J. Viral Hepat. 19:Suppl 1 (2012), 52–59.
19. Chien, R.N., Liaw, Y.F., Chen, T.C., Yeh, C.T., Sheen, I.S., Efficacy of thymosin alpha1 in patients with chronic hepatitis B: a randomized, controlled trial. Hepatology 27 (1998), 1383–1387.
20. You, J., Zhuang, L., Cheng, H.Y., Yan, S.M., Yu, L., Huang, J.H., Tang, B.Z., Huang, M.L., Ma, Y.L., Chongsuvivatwong, V., Sriplung, H., Geater, A., Qiao, Y.W., Wu, R.X., Efficacy of thymosin alpha-1 and interferon alpha in treatment of chronic viral hepatitis B: a randomized controlled study. World J. Gastroenterol. 12 (2006), 6715–6721.
21. Yang, Y.F., Zhao, W., Zhong, Y.D., Yang, Y.J., Shen, L., Zhang, N., Huang, P., Comparison of the efficacy of thymosin alpha-1 and interferon alpha in the treatment of chronic hepatitis B: a meta-analysis. Antivir. Res. 77 (2008), 136–141.
22. Romani, L., Oikonomou, V., Moretti, S., Iannitti, R.G., D'Adamo, M.C., Villella, V.R., Pariano, M., Sforna, L., Borghi, M., Bellet, M.M., Fallarino, F., Pallotta, M.T., Servillo, G., Ferrari, E., Puccetti, P., Kroemer, G., Pessia, M., Maiuri, L., Goldstein, A.L., Garaci, E., Thymosin alpha1 represents a potential potent single-molecule-based therapy for cystic fibrosis. Nat. Med. 23 (2017), 590–600.
23. Maio, M., Mackiewicz, A., Testori, A., Trefzer, U., Ferraresi, V., Jassem, J., Garbe, C., Lesimple, T., Guillot, B., Gascon, P., Gilde, K., Camerini, R., Cognetti, F., Large randomized study of thymosin alpha 1, interferon alfa, or both in combination with dacarbazine in patients with metastatic melanoma. J. Clin. Oncol. 28 (2010), 1780–1787.
24. Danielli, R., Fonsatti, E., Calabro, L., Di Giacomo, A.M., Maio, M., Thymosin alpha 1 in melanoma: from the clinical trial setting to the daily practice and beyond. Thymosins in Health and Disease Ii 1270, 2012, 8–12.
25. Romani, L., Bistoni, F., Gaziano, R., Bozza, S., Montagnoli, C., Perruccio, K., Pitzurra, L., Bellocchio, S., Velardi, A., Rasi, G., di Francesco, P., Garaci, E., Thymosin alpha 1 activates dendritic cells for antifungal Th1 resistance through Toll-like receptor signaling. Blood 103 (2004), 4232–4239.
26. Romani, L., Bistoni, F., Perruccio, K., Montagnoli, C., Gaziano, R., Bozza, S., Bonifazi, P., Bistoni, G., Rasi, G., Velardi, A., Fallarino, F., Garaci, E., Puccetti, P., Thymosin alpha 1 activates dendritic cell tryptophan catabolism and establishes a regulatory environment for balance of inflammation and tolerance. Blood 108 (2006), 2265–2274.
27. Chretien, P.B., Lipson, S.D., Makuch, R., Kenady, D.E., Cohen, M.H., Minna, J.D., Thymosin in cancer patients: in vitro effects and correlations with clinical response to thymosin immunotherapy. Canc. Treat Rep. 62 (1978), 1787–1790.
28. Schulof, R.S., Lloyd, M.J., Cleary, P.A., Palaszynski, S.R., Mai, D.A., Cox, J.W. Jr., Alabaster, O., Goldstein, A.L., A randomized trial to evaluate the immunorestorative properties of synthetic thymosin-alpha 1 in patients with lung cancer. J. Biol. Response Modif. 4 (1985), 147–158.
29. Garaci, E., Lopez, M., Bonsignore, G., Della Giulia, M., D'Aprile, M., Favalli, C., Rasi, G., Santini, S., Capomolla, E., Vici, P., et al. Sequential chemoimmunotherapy for advanced non-small cell lung cancer using cisplatin, etoposide, thymosin-alpha 1 and interferon-alpha 2a. Eur. J. Canc. 31A (1995), 2403–2405.
30. Salvati, F., Rasi, G., Portalone, L., Antilli, A., Garaci, E., Combined treatment with thymosin-alpha1 and low-dose interferon-alpha after ifosfamide in non-small cell lung cancer: a phase-II controlled trial. Anticancer Res. 16 (1996), 1001–1004.
31. Rasi, G., Terzoli, E., Izzo, F., Pierimarchi, P., Ranuzzi, M., Sinibaldi-Vallebona, P., Tuthill, C., Garaci, E., Combined treatment with thymosin-alpha1 and low dose interferon-alpha after dacarbazine in advanced melanoma. Melanoma Res. 10 (2000), 189–192.
32. King, R.S., Tuthill, C., Evaluation of thymosin alpha 1 in nonclinical models of the immune-suppressing indications melanoma and sepsis. Expet Opin. Biol. Ther. 15:Suppl 1 (2015), S41–S49.
33. Lao, X., Li, B., Liu, M., Shen, C., Yu, T., Gao, X., Zheng, H., A modified thymosin alpha 1 inhibits the growth of breast cancer both in vitro and in vivo: suppressment of cell proliferation, inducible cell apoptosis and enhancement of targeted anticancer effects. Apoptosis 20 (2015), 1307–1320.
34. Guo, Y., Chang, H., Li, J., Xu, X.Y., Shen, L., Yu, Z.B., Liu, W.C., Thymosin alpha 1 suppresses proliferation and induces apoptosis in breast cancer cells through PTEN-mediated inhibition of PI3K/Akt/mTOR signaling pathway. Apoptosis 20 (2015), 1109–1121.
35. Knutsen, A.P., Freeman, J.J., Mueller, K.R., Roodman, S.T., Bouhasin, J.D., Thymosin-alpha1 stimulates maturation of CD34+ stem cells into CD3+4+ cells in an in vitro thymic epithelia organ coculture model. Int. J. Immunopharm. 21 (1999), 15–26.
36. Wolf, G.T., Hudson, J., Peterson, K.A., Poore, J.A., McClatchey, K.D., Interleukin 2 receptor expression in patients with head and neck squamous carcinoma. Effects of thymosin alpha 1 in vitro. Arch. Otolaryngol. Head Neck Surg. 115 (1989), 1345–1349.
37. Giuliani, C., Napolitano, G., Mastino, A., Di Vincenzo, S., D'Agostini, C., Grelli, S., Bucci, I., Singer, D.S., Kohn, L.D., Monaco, F., Garaci, E., Favalli, C., Thymosin-alpha1 regulates MHC class I expression in FRTL-5 cells at transcriptional level. Eur. J. Immunol. 30 (2000), 778–786.
38. Grohmann, U., Fallarino, F., Puccetti, P., Tolerance, DCs and tryptophan: much ado about Ido. Trends Immunol. 24 (2003), 242–248.
39. Mellor, A.L., Munn, D.H., Ido expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4 (2004), 762–774.
40. Orabona, C., Puccetti, P., Vacca, C., Bicciato, S., Luchini, A., Fallarino, F., Bianchi, R., Velardi, E., Perruccio, K., Velardi, A., Bronte, V., Fioretti, M.C., Grohmann, U., Toward the identification of a tolerogenic signature in Ido-competent dendritic cells. Blood 107 (2006), 2846–2854.
41. Wang, F., Li, B., Fu, P., Li, Q., Zheng, H., Lao, X., Immunomodulatory and enhanced antitumor activity of a modified thymosin alpha1 in melanoma and lung cancer. Int. J. Pharm. (Amst.) 547 (2018), 611–620.
42. Li, J., Cheng, Y., Zhang, X., Zheng, L., Han, Z., Li, P., Xiao, Y., Zhang, Q., Wang, F., The in vivo immunomodulatory and synergistic anti-tumor activity of thymosin alpha1-thymopentin fusion peptide and its binding to TLR2. Canc. Lett. 337 (2013), 237–247.
43. Goldstein, A.L., Badamchian, M., Thymosins: chemistry and biological properties in health and disease. Expet Opin. Biol. Ther. 4 (2004), 559–573.
44. Nepravishta, R., Mandaliti, W., Eliseo, T., Sinibaldi Vallebona, P., Pica, F., Garaci, E., Paci, M., Thymosin alpha1 inserts N terminus into model membranes assuming a helical conformation. Expet Opin. Biol. Ther. 15:Suppl 1 (2015), S71–S81.
45. Mandaliti, W., Nepravishta, R., Pica, F., Vallebona, P.S., Garaci, E., Paci, M., Thymosin alpha1 interacts with hyaluronic acid electrostatically by its terminal sequence LKEKK. Molecules, 22, 2017.
46. Mandaliti, W., Nepravishta, R., Sinibaldi Vallebona, P., Pica, F., Garaci, E., Paci, M., Thymosin alpha1 interacts with exposed phosphatidylserine in membrane models and in cells and uses serum albumin as a Carrier. Biochemistry 55 (2016), 1462–1472.
47. Elizondo-Riojas, M.A., Chamow, S.M., Tuthill, C.W., Gorenstein, D.G., Volk, D.E., NMR structure of human thymosin alpha-1. Biochem. Bioph. Res. Co. 416 (2011), 356–361.
48. Xiong, J.P., Stehle, T., Zhang, R., Joachimiak, A., Frech, M., Goodman, S.L., Arnaout, M.A., Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand. Science 296 (2002), 151–155.
49. Chen, R., Li, L., Weng, Z., ZDOCK: an initial-stage protein-docking algorithm. Proteins 52 (2003), 80–87.
50. Jarvis, A., Allerston, C.K., Jia, H., Herzog, B., Garza-Garcia, A., Winfield, N., Ellard, K., Aqil, R., Lynch, R., Chapman, C., Hartzoulakis, B., Nally, J., Stewart, M., Cheng, L., Menon, M., Tickner, M., Djordjevic, S., Driscoll, P.C., Zachary, I., Selwood, D.L., Small molecule inhibitors of the neuropilin-1 vascular endothelial growth factor A (VEGF-A) interaction. J. Med. Chem. 53 (2010), 2215–2226.
51. Carraro, G., Naso, A., Montomoli, E., Gasparini, R., Camerini, R., Panatto, D., Tineo, M.C., De Giorgi, L., Piccirella, S., Khadang, B., Ceracchi, M., De Rosa, A., Thymosin-alpha 1 (Zadaxin (TM)) enhances the immunogenicity of an adjuvated pandemic H1N1v influenza vaccine (Focetria (TM)) in hennodialyzed patients: a pilot study. Vaccine 30 (2012), 1170–1180.
52. Volk, D.E., Tuthill, C.W., Elizondo-Riojas, M.A., Gorenstein, D.G., NMR structural studies of thymosin alpha 1 and beta-thymosins. Thymosins in Health and Disease Ii 1270, 2012, 73–78.
53. Garaci, E., Pica, F., Rasi, G., Favalli, C., Thymosin alpha 1 in the treatment of cancer: from basic research to clinical application. Int. J. Immunopharm. 22 (2000), 1067–1076.
54. Billich, A., Thymosin alpha1. SciClone pharmaceuticals. Curr. Opin. Invest. Drugs 3 (2002), 698–707.
55. Mandaliti, W., Nepravishta, R., Sinibaldi Vallebona, P., Pica, F., Garaci, E., Paci, M., New studies about the insertion mechanism of Thymosin alpha1 in negative regions of model membranes as starting point of the bioactivity. Amino Acids 48 (2016), 1231–1239.
56. Teesalu, T., Sugahara, K.N., Ruoslahti, E., Tumor-penetrating peptides. Front. Oncol., 3, 2013, 216.
57. Parker, M.W., Xu, P., Li, X.B., Vander Kooi, C.W., Structural basis for selective vascular endothelial growth factor-a (VEGF-A) binding to Neuropilin-1. J. Biol. Chem. 287 (2012), 11082–11089.
58. Roth, L., Agemy, L., Kotamraju, V.R., Braun, G., Teesalu, T., Sugahara, K.N., Hamzah, J., Ruoslahti, E., Transtumoral targeting enabled by a novel neuropilin-binding peptide. Oncogene 31 (2012), 3754–3763.
59. Jubb, A.M., Strickland, L.A., Liu, S.D., Mak, J., Schmidt, M., Koeppen, H., Neuropilin-1 expression in cancer and development. J. Pathol. 226 (2012), 50–60.
60. Garaci, E., Mastino, A., Pica, F., Favalli, C., Combination treatment using thymosin alpha 1 and interferon after cyclophosphamide is able to cure Lewis lung carcinoma in mice. Canc. Immunol. Immunother.: CII 32 (1990), 154–160.
61. Rasi, G., Silecchia, G., Sinibaldi-Vallebona, P., Spaziani, E., Pierimarchi, P., Sivilia, M., Tremiterra, S., Garaci, E., Anti-tumor effect of combined treatment with thymosin alpha 1 and interleukin-2 after 5-fluorouracil in liver metastases from colorectal cancer in rats. Int. J. Canc. 57 (1994), 701–705.
62. Feau, S., Arens, R., Togher, S., Schoenberger, S.P., Autocrine IL-2 is required for secondary population expansion of CD8(+) memory T cells. Nat. Immunol. 12 (2011), 908–913.
63. Matsuzaki, J., Tsuji, T., Luescher, I.F., Shiku, H., Mineno, J., Okamoto, S., Old, L.J., Shrikant, P., Gnjatic, S., Odunsi, K., Direct tumor recognition by a human CD4(+) T-cell subset potently mediates tumor growth inhibition and orchestrates anti-tumor immune responses. Sci. Rep., 5, 2015, 14896.
64. Bongiorno, E.K., Garcia, S.A., Sauma, S., Hooper, D.C., Type 1 immune mechanisms driven by the response to infection with attenuated rabies virus result in changes in the immune bias of the tumor microenvironment and necrosis of mouse GL261 brain tumors. J. Immunol. 198 (2017), 4513–4523.
65. Deligne, C., Metidji, A., Fridman, W.H., Teillaud, J.L., Anti-CD20 therapy induces a memory Th1 response through the IFN-gamma/IL-12 axis and prevents protumor regulatory T-cell expansion in mice. Leukemia 29 (2015), 947–957.
66. Braumuller, H., Wieder, T., Brenner, E., Assmann, S., Hahn, M., Alkhaled, M., Schilbach, K., Essmann, F., Kneilling, M., Griessinger, C., Ranta, F., Ullrich, S., Mocikat, R., Braungart, K., Mehra, T., Fehrenbacher, B., Berdel, J., Niessner, H., Meier, F., van den Broek, M., Haring, H.U., Handgretinger, R., Quintanilla-Martinez, L., Fend, F., Pesic, M., Bauer, J., Zender, L., Schaller, M., Schulze-Osthoff, K., Rocken, M., T-helper-1-cell cytokines drive cancer into senescence. Nature 494 (2013), 361–365.
67. Kammertoens, T., Friese, C., Arina, A., Idel, C., Briesemeister, D., Rothe, M., Ivanov, A., Szymborska, A., Patone, G., Kunz, S., Sommermeyer, D., Engels, B., Leisegang, M., Textor, A., Fehling, H.J., Fruttiger, M., Lohoff, M., Herrmann, A., Yu, H., Weichselbaum, R., Uckert, W., Hubner, N., Gerhardt, H., Beule, D., Schreiber, H., Blankenstein, T., Tumour ischaemia by interferon-gamma resembles physiological blood vessel regression. Nature 545 (2017), 98–102.
68. Franco, C.A., Jones, M.L., Bernabeu, M.O., Geudens, I., Mathivet, T., Rosa, A., Lopes, F.M., Lima, A.P., Ragab, A., Collins, R.T., Phng, L.K., Coveney, P.V., Gerhardt, H., Dynamic endothelial cell rearrangements drive developmental vessel regression. PLoS Biol., 13, 2015, e1002125.
69. Listopad, J.J., Kammertoens, T., Anders, K., Silkenstedt, B., Willimsky, G., Schmidt, K., Kuehl, A.A., Loddenkemper, C., Blankenstein, T., Fas expression by tumor stroma is required for cancer eradication. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 2276–2281.