Use of ribosome-inactivating proteins from Sambucus for the construction of immunotoxins and conjugates for cancer therapy

Toxins

Volumn 3, Issue 4, 2011, Pages 420-441

  Ferreras, José M ^a   Citores, Lucía ^a   Iglesias, Rosario ^a   Jiménez, Pilar ^b   Girbés, Tomás ^b  

^a UNIVERSITY OF VALLADOLID   (Spain)

^b UNIVERSITY OF VALLADOLID   (Spain)

Author keywords

Endoglin (CD105); Immunotoxin; Ribosome inactivating proteins; Sambucus; Transferrin

Indexed keywords

ABRIN; EBULIN 1; IMMUNOTOXIN; LECTIN; LECTIN NIGRIN B CONJUGATE; NIGRIN B; RIBOSOME INACTIVATING PROTEIN 1; RIBOSOME INACTIVATING PROTEIN 2; RICIN; RUFOCROMOMYCIN; TRANSFERRIN; TRANSFERRIN EBULIN 1 CONJUGATE; TRANSFERRIN NIGRIN B CONJUGATE; UNCLASSIFIED DRUG; VOLKENSIN; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; EBULIN L; EBULIN L TRANSFERRIN CONJUGATE; ENDOGLIN ANTIBODY EBULIN L CONJUGATE; ENDOGLIN ANTIBODY NIGRIN B CONJUGATE; NIGRIN B TRANSFERRIN CONJUGATE; PLANT TOXIN;

ANTINEOPLASTIC ACTIVITY; CANCER THERAPY; DRUG CONJUGATION; DRUG CYTOTOXICITY; HUMAN; IC 50; INTERNALIZATION; NONHUMAN; PHYLOGENY; PROTEIN ISOLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; SAMBUCUS; BINDING AFFINITY; CANCER CHEMOTHERAPY; CELL VIABILITY; DOSE RESPONSE; DRUG EFFICACY; DRUG MECHANISM; DRUG MEGADOSE; DRUG STRUCTURE; ENDOCYTOSIS; ENZYME ACTIVITY; INTRACELLULAR SIGNALING; PLANT GENE; PROTEIN SYNTHESIS INHIBITION; PROTEIN TARGETING; RIBOSOME INACTIVATING PROTEIN 2 GENE; TOXICITY TESTING;

ANIMALIA; SAMBUCUS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; CELL SURVIVAL; HELA CELLS; HUMANS; IMMUNOTOXINS; LETHAL DOSE 50; MODELS, MOLECULAR; NEOPLASMS; PROTEIN CONFORMATION; RIBOSOME INACTIVATING PROTEINS, TYPE 2; SAMBUCUS;

EID: 79955636245     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins3050420     Document Type: Review

References (122)

1. Barbieri, L.; Battelli, M.G.; Stirpe, F. Ribosome-inactivating proteins from plants. Biochim. Biophys. Acta 1993, 1154, 237-282.
2. Girbes, T.; Ferreras, J.M.; Arias, F.J.; Stirpe, F. Description, distribution, activity and phylogenetic relationship of ribosome-inactivating proteins in plants, fungi and bacteria. Mini Rev. Med. Chem. 2004, 4, 461-476.
3. Stirpe, F. Ribosome-inactivating proteins. Toxicon 2004, 44, 371-383.
4. Hartley, M.R.; Lord, J.M. Cytotoxic ribosome-inactivating lectins from plants. Biochim. Biophys. Acta 2004, 1701, 1-14.
5. Obrig, T.G. Escherichia coli Shiga Toxin Mechanisms of Action in Renal Disease. Toxins 2010, 2, 2769-2794.
6. Brigotti, M.; Rambelli, F.; Zamboni, M.; Montanaro, L.; Sperti, S. Effect of alpha-sarcin and ribosome-inactivating proteins on the interaction of elongation factors with ribosomes. Biochem. J. 1989, 257, 723-727.
7. Barbieri, L.; Ferreras, J.M.; Barraco, A.; Ricci, P.; Stirpe, F. Some ribosome-inactivating proteins depurinate ribosomal RNA at multiple sites. Biochem. J. 1992, 286, 1-4.
8. Iglesias, R.; Arias, F.J.; Rojo, M.A.; Escarmis, C.; Ferreras, J.M.; Girbes, T. Molecular action of the type 1 ribosome-inactivating protein saporin 5 on Vicia sativa ribosomes. FEBS Lett. 1993, 325, 291-294.
9. Girbes, T.; deTorre, C.; Iglesias, R.; Ferreras, J.M.; Mendez, E. RIP for viruses. Nature 1996, 379, 777-778.
10. Barbieri, L.; Gorini, P.; Valbonesi, P.; Castiglioni, P.; Stirpe, F. Unexpected activity of saporins. Nature 1994, 372, 624.
11. Barbieri, L.; Ciani, M.; Girbes, T.; Liu, W.Y.; van Damme, E.J.; Peumans, W.J.; Stirpe, F. Enzymatic activity of toxic and non-toxic type 2 ribosome-inactivating proteins. FEBS Lett. 2004, 563, 219-222.
12. Shih, N.; McDonald, K.; Jackman, A.; Girbés, T.; Iglesias, R. Bifunctional plant defence enzymes with chitinase and ribosome inactivating activities from Trichosanthes kirilowii cell cultures. Plant Sci. 1997, 130, 145-150.
13. Huang, P.L.; Chen, H.C.; Kung, H.F.; Huang, P.L.; Huang, P.; Huang, H.I.; Lee-Huang, S. Anti-HIV plant proteins catalyze topological changes of DNA into inactive forms. Biofactors 1992, 4, 37-41.
14. Lee-Huang, S.; Huang, P.L.; Huang, P.L.; Bourinbaiar, A.S.; Chen, H.C.; Kung, H.F. Inhibition of the integrase of human immunodeficiency virus (HIV) type 1 by anti-HIV plant proteins MAP30 and GAP31. Proc. Natl. Acad. Sci. USA 1995, 92, 8818-8822.
15. Li, X.D.; Chen, W.F.; Liu, W.Y.; Wang, G.H. Large-scale preparation of two new ribosome-inactivating proteins-cinnamomin and camphorin from the seeds of Cinnamomum camphora. Protein Expr. Purif. 1997, 10, 27-31.
16. Ruggiero, A.; Chambery, A.; Di Maro, A.; Mastroianni, A.; Parente, A.; Berisio, R. Crystallization and preliminary X-ray diffraction analysis of PD-L1, a highly glycosylated ribosome inactivating protein with DNase activity. Protein Pept. Lett. 2007, 14, 407-409.
17. Lombard, S.; Helmy, M.E.; Pieroni, G. Lipolytic activity of ricin from Ricinus sanguineus and Ricinus communis on neutral lipids. Biochem. J. 2001, 358, 773-781.
18. Morlon-Guyot, J.; Helmy, M.; Lombard-Frasca, S.; Pignol, D.; Pieroni, G.; Beaumelle, B. Identification of the ricin lipase site and implication in cytotoxicity. J. Biol. Chem. 2003, 278, 17006-17011.
19. Stirpe, F.; Barbieri, L.; Gorini, P.; Valbonesi, P.; Bolognesi, A.; Polito, L. Activities associated with the presence of ribosome-inactivating proteins increase in senescent and stressed leaves. FEBS Lett. 1996, 382, 309-312.
20. Stirpe, F.; Barbieri, L.; Abbondanza, A.; Falasca, A.I.; Brown, A.N.; Sandvig, K.; Olsnes, S.; Pihl, A. Properties of volkensin, a toxic lectin from Adenia volkensii. J. Biol. Chem. 1985, 260, 14589-14595.
21. Citores, L.; Ferreras, J.M.; Iglesias, R.; Carbajales, M.L.; Arias, F.J.; Jimenez, P.; Rojo, M.A.; Girbes, T. Molecular mechanism of inhibition of mammalian protein synthesis by some four-chain agglutinins. Proposal of an extended classification of plant ribosome-inactivating proteins (rRNA N-glycosidases). FEBS Lett. 1993, 329, 59-62.
22. Olsnes, S.; Saltvedt, E.; Pihl, A. Isolation and comparison of galactose-binding lectins from Abrus precatorius and Ricinus communis. J. Biol. Chem. 1974, 249, 803-810.
23. Roberts, L.M.; Lamb, F.I.; Pappin, D.J.; Lord, J.M. The primary sequence of Ricinus communis agglutinin. Comparison with ricin. J. Biol. Chem. 1985, 260, 15682-15686.
24. Girbes, T.; Citores, L.; Ferreras, J.M.; Rojo, M.A.; Iglesias, R.; Munoz, R.; Arias, F.J.; Calonge, M.; Garcia, J.R.; Mendez, E. Isolation and partial characterization of nigrin b, a non-toxic novel type 2 ribosome-inactivating protein from the bark of Sambucus nigra L. Plant Mol. Biol. 1993, 22, 1181-1186.
25. Girbes, T.; Citores, L.; Iglesias, R.; Ferreras, J.M.; Munoz, R.; Rojo, M.A.; Arias, F.J.; Garcia, J.R.; Mendez, E.; Calonge, M. Ebulin 1, a nontoxic novel type 2 ribosome-inactivating protein from Sambucus ebulus L. leaves. J. Biol. Chem. 1993, 268, 18195-18199.
26. Citores, L.; deBenito, F.M.; Iglesias, R.; Ferreras, J.M.; Jimenez, P.; Argueso, P.; Farias, G.; Mendez, E.; Girbes, T. Isolation and characterization of a new non-toxic two-chain ribosome-inactivating protein from fruits of elder (Sambucus nigra L). J. Exp. Bot. 1996, 47, 1577-1585.
27. Citores, L.; Iglesias, R.; Munoz, R.; Ferreras, J.M.; Jimenez, P.; Girbes, T. Elderberry (Sambucus nigra L.) seed proteins inhibit protein synthesis and display strong immunoreactivity with rabbit polyclonal antibodies raised against the type 2 ribosome-inactivating protein nigrin b. J. Exp. Bot. 1994, 45, 513-516.
28. Girbes, T.; Citores, L.; de Benito, F.M.; Inglesias, R.; Ferreras, J.M. A non-toxic two-chain ribosome-inactivating protein co-exists with a structure-related monomeric lectin (SNA III) in elder (Sambucus nigra) fruits. Biochem. J. 1996, 315, 343.
29. Citores, L.; de Benito, F.M.; Iglesias, R.; Ferreras, J.M.; Argueso, P.; Jimenez, P.; Testera, A.; Camafeita, E.; Mendez, E.; Girbes, T. Characterization of a new non-toxic two-chain ribosome-inactivating protein and a structurally-related lectin from rhizomes of dwarf elder (Sambucus ebulus L.). Cell. Mol. Biol. (Noisy-le-Grand) 1997, 43, 485-499.
30. Citores, L.; de Benito, F.M.; Iglesias, R.; Miguel, F.J.; Argueso, P.; Jimenez, P.; Mendez, E.; Girbes, T. Presence of polymerized and free forms of the non-toxic type 2 ribosome-inactivating protein ebulin and a structurally related new homodimeric lectin in fruits of Sambucus ebulus L. Planta 1998, 204, 310-319.
31. de Benito, F.M.; Citores, L.; Iglesias, R.; Ferreras, J.M.; Camafeita, E.; Mendez, E.; Girbes, T. Isolation and partial characterization of a novel and uncommon two-chain 64-kDa ribosome-inactivating protein from the bark of elder (Sambucus nigra L.). FEBS Lett. 1997, 413, 85-91.
32. Rojo, M.A.; Yato, M.; Ishii-Minami, N.; Minami, E.; Kaku, H.; Citores, L.; Girbes, T.; Shibuya, N. Isolation, cDNA cloning, biological properties, and carbohydrate binding specificity of sieboldin-b, a type II ribosome-inactivating protein from the bark of japanese elderberry (Sambucus sieboldiana). Arch. Biochem. Biophys. 1997, 340, 185-194.
33. de Benito, F.M.; Citores, L.; Iglesias, R.; Ferreras, J.M.; Soriano, F.; Arias, J.; Mendez, E.; Girbes, T. Ebulitins: A new family of type 1 ribosome-inactivating proteins (rRNA N-glycosidases) from leaves of Sambucus ebulus L. that coexist with the type 2 ribosome-inactivating protein ebulin 1. FEBS Lett. 1995, 360, 299-302.
34. de Benito, F.M.; Iglesias, R.; Ferreras, J.M.; Citores, L.; Camafeita, E.; Mendez, E.; Girbes, T. Constitutive and inducible type 1 ribosome-inactivating proteins (RIPs) in elderberry (Sambucus nigra L.). FEBS Lett. 1998, 428, 75-79.
35. van Damme, E.J.; Barre, A.; Rouge, P.; Van, L.F.; Peumans, W.J. Isolation and molecular cloning of a novel type 2 ribosome-inactivating protein with an inactive B chain from elderberry (Sambucus nigra) bark. J. Biol. Chem. 1997, 272, 8353-8360.
36. van Damme, E.J.; Roy, S.; Barre, A.; Citores, L.; Mostafapous, K.; Rouge, P.; Van, L.F.; Girbes, T.; Goldstein, I.J.; Peumans, W.J. Elderberry (Sambucus nigra) bark contains two structurally different Neu5Ac(alpha2,6)Gal/GalNAc-binding type 2 ribosome-inactivating proteins. Eur. J. Biochem. 1997, 245, 648-655.
37. Ferreras, J.M.; Citores, L.; Iglesias, R.; Jiménez, P.; Girbés, T. Sambucus Ribosome-Inactivating Proteins and Lectins. In Toxic Plant Proteins, Plant Cell Monographs; Lord, J.M., Hartley, M.R., Eds.; Springer-Verlag: Berlin, Germany, 2010; Volume 18, pp. 107-131.
38. Ferreras, J.M.; Citores, L.; de Benito, F.M.; Arias, F.J.; Rojo, M.A.; Munoz R.; Iglesias, R.; Girbes, T. Ribosome-inactivating proteins and lectins from Sambucus. Curr. Top. Phytochem. 2000, 3, 113-128.
39. Rojo, M.A.; Citores, L.; Jimenez, P.; Ferreras, J.M.; Arias, F.J.; Mendez, E.; Girbes, T. Isolation and characterization of a new D-galactose-binding lectin from Sambucus racemosa L. Protein Pept. Lett. 2003, 10, 287-293.
40. Iglesias, R.; Citores, L.; Ferreras, J.M.; Perez, Y.; Jimenez, P.; Gayoso, M.J.; Olsnes, S.; Tamburino, R.; Di Maro, A.; Parente, A.; Girbes, T. Sialic acid-binding dwarf elder four-chain lectin displays nucleic acid N-glycosidase activity. Biochimie 2010, 92, 71-80.
41. van Damme, E.J.; Barre, A.; Rouge, P.; van, L.F.; Peumans, W.J. The NeuAc(alpha-2,6)-Gal/GalNAc-binding lectin from elderberry (Sambucus nigra) bark, a type-2 ribosome-inactivating protein with an unusual specificity and structure. Eur. J. Biochem. 1996, 235, 128-137.
42. Peumans, W.J.; Roy, S.; Barre, A.; Rouge, P.; van, L.F.; van Damme, E.J. Elderberry (Sambucus nigra) contains truncated Neu5Ac(alpha-2,6)Gal/GalNAc-binding type 2 ribosome-inactivating proteins. FEBS Lett. 1998, 425, 35-39.
43. Karpova, I.S.; Koretska, N.V.; Palchykovska, L.G.; Negrutska, V.V. Lectins from Sambucus nigra L. inflorescences: Isolation and investigation of biological activity using procaryotic test-systems. Ukr. Biokhim. Zh. 2007, 79, 145-152.
44. Kaku, H.; Tanaka, Y.; Tazaki, K.; Minami, E.; Mizuno, H.; Shibuya, N. Sialylated oligosaccharide-specific plant lectin from Japanese elderberry (Sambucus sieboldiana) bark tissue has a homologous structure to type II ribosome-inactivating proteins, ricin and abrin. cDNA cloning and molecular modeling study. J. Biol. Chem. 1996, 271, 1480-1485.
45. Citores, L.; Rojo, M.A.; Jimenez, P.; Ferreras, J.M.; Iglesias, R.; Aranguez, I.; Girbes, T. Transient occurrence of an ebulin-related D-galactose-lectin in shoots of Sambucus ebulus L. Phytochemistry 2008, 69, 857-864.
46. Kaku, H.; Peumans, W.J.; Goldstein, I.J. Isolation and characterization of a second lectin (SNA-II) present in elderberry (Sambucus nigra L.) bark. Arch. Biochem. Biophys. 1990, 277, 255-262.
47. van Damme, E.J.; Roy, S.; Barre, A.; Rouge, P.; van, L.F.; Peumans, W.J. The major elderberry (Sambucus nigra) fruit protein is a lectin derived from a truncated type 2 ribosome-inactivating protein. Plant J. 1997, 12, 1251-1260.
48. Peumans, W.J.; Kellens, J.T.; Allen, A.K.; van Damme, E.J. Isolation and characterization of a seed lectin from elderberry (Sambucus nigra L.) and its relationship to the bark lectins. Carbohydr. Res. 1991, 213, 7-17.
49. Rojo, M.A.; Kaku, H.; Ishii-Minami, N.; Minami, E.; Yato, M.; Hisajima, S.; Yamaguchi, T.; Shibuya, N. Characterization and cDNA cloning of monomeric lectins that correspond to the B-chain of a type 2 ribosome-inactivating protein from the bark of japanese elderberry (Sambucus sieboldiana). J. Biochem. 2004, 135, 509-516.
50. Rojo, M.A.; Citores, L.; Arias, F.J.; Ferreras, J.M.; Jimenez, P.; Girbes, T. cDNA molecular cloning and seasonal accumulation of an ebulin l-related dimeric lectin of dwarf elder (Sambucus ebulus L) leaves. Int. J. Biochem. Cell. Biol. 2003, 35, 1061-1065.
51. van Damme, E.J.; Barre, A.; Rouge, P.; Van, L.F.; Peumans, W.J. Characterization and molecular cloning of Sambucus nigra agglutinin V (nigrin b), a GalNAc-specific type-2 ribosome-inactivating protein from the bark of elderberry (Sambucus nigra). Eur. J. Biochem. 1996, 237, 505-513.
52. Pascal, J.M.; Day, P.J.; Monzingo, A.F.; Ernst, S.R.; Robertus, J.D.; Iglesias, R.; Perez, Y.; Ferreras, J.M.; Citores, L.; Girbes, T. 2.8-A crystal structure of a nontoxic type-II ribosome-inactivating protein, ebulin l. Proteins 2001, 43, 319-326.
53. Shibuya, N.; Goldstein, I.J.; Broekaert, W.F.; Nsimba-Lubaki, M.; Peeters, B.; Peumans, W.J. The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(alpha 2-6)Gal/GalNAc sequence. J. Biol. Chem. 1987, 262, 1596-1601.
54. Citores, L.; Munoz, R.; de Benito, F.M.; Iglesias, R.; Ferreras, J.M.; Girbes, T. Differential sensitivity of HELA cells to the type 2 ribosome-inactivating proteins ebulin l, nigrin b and nigrin f as compared with ricin. Cell. Mol. Biol. (Noisy-le-Grand) 1996, 42, 473-476.
55. Battelli, M.G.; Citores, L.; Buonamici, L.; Ferreras, J.M.; de Benito, F.M.; Stirpe, F.; Girbes, T. Toxicity and cytotoxicity of nigrin b, a two-chain ribosome-inactivating protein from Sambucus nigra: Comparison with ricin. Arch. Toxicol. 1997, 71, 360-364.
56. Gayoso, M.J.; Munoz, R.; Arias, Y.; Villar, R.; Rojo, M.A.; Jimenez, P.; Ferreras, J.M.; Aranguez, I.; Girbes, T. Specific dose-dependent damage of Lieberkuhn crypts promoted by large doses of type 2 ribosome-inactivating protein nigrin b intravenous injection to mice. Toxicol. Appl. Pharmacol. 2005, 207, 138-146.
57. Stirpe, F.; Barbieri, L. Ribosome-inactivating proteins up to date. FEBS Lett. 1986, 195, 1-8.
58. Citores, L.; Munoz, R.; Rojo, M.A.; Jimenez, P.; Ferreras, J.M.; Girbes, T. Evidence for distinct cellular internalization pathways of ricin and nigrin b. Cell. Mol. Biol. (Noisy-le-Grand) 2003, 49, OL461-OL465.
59. Battelli, M.G.; Musiani, S.; Buonamici, L.; Santi, S.; Riccio, M.; Maraldi, N.M.; Girbes, T.; Stirpe, F. Interaction of volkensin with HeLa cells: Binding, uptake, intracellular localization, degradation and exocytosis. Cell Mol. Life Sci. 2004, 61, 1975-1984.
60. Lord, J.M.; Roberts, L.M.; Lencer, W.I. Entry of protein toxins into mammalian cells by crossing the endoplasmic reticulum membrane: Co-opting basic mechanisms of endoplasmic reticulum-associated degradation. Curr. Top. Microbiol. Immunol. 2005, 300, 149-168.
61. Spooner, R.A.; Hart, P.J.; Cook, J.P.; Pietroni, P.; Rogon, C.; Hohfeld, J.; Roberts, L.M.; Lord, J.M. Cytosolic chaperones influence the fate of a toxin dislocated from the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 2008, 105, 17408-17413.
62. Mayerhofer, P.U.; Cook, J.P.; Wahlman, J.; Pinheiro, T.T.; Moore, K.A.; Lord, J.M.; Johnson, A.E.; Roberts, L.M. Ricin A chain insertion into endoplasmic reticulum membranes is triggered by a temperature increase to 37 °C. J. Biol. Chem. 2009, 284, 10232-10242.
63. Pastan, I.; Hassan, R.; FitzGerald, D.J.; Kreitman, R.J. Immunotoxin treatment of cancer. Annu. Rev. Med. 2007, 58, 221-237.
64. Wong, L.; Suh, D.Y.; Frankel, A.E. Toxin conjugate therapy of cancer. Semin. Oncol. 2005, 32, 591-595.
65. Bolognesi, A.; Polito, L. Immunotoxins and other conjugates: Pre-clinical studies. Mini. Rev. Med. Chem. 2004, 4, 563-583.
66. Potala, S.; Sahoo, S.K.; Verma, R.S. Targeted therapy of cancer using diphtheria toxin-derived immunotoxins. Drug Discov. Today 2008, 13, 807-815.
67. Frankel, A.E.; Kreitman, R.J.; Sausville, E.A. Targeted toxins. Clin. Cancer Res. 2000, 6, 326-334.
68. Cheung, M.C.; Revers, L.; Perampalam, S.; Wei, X.; Kiarash, R.; Green, D.E.; bdul-Wahid, A.; Gariepy, J. An evolved ribosome-inactivating protein targets and kills human melanoma cells in vitro and in vivo. Mol. Cancer 2010, 9, 28.
69. Rosenblum, M. Immunotoxins and toxin constructs in the treatment of leukemia and lymphoma. Adv. Pharmacol. 2004, 51, 209-228.
70. Fracasso, G.; Bellisola, G.; Castelletti, D.; Tridente, G.; Colombatti, M. Immunotoxins and other conjugates: Preparation and general characteristics. Mini Rev. Med. Chem. 2004, 4, 545-562.
71. Frankel, A.E.; Neville, D.M.; Bugge, T.A.; Kreitman, R.J.; Leppla, S.H. Immunotoxin therapy of hematologic malignancies. Semin. Oncol. 2003, 30, 545-557.
72. Vitetta, E.S. Immunotoxins and vascular leak syndrome. Cancer J. 2000, 6, S218-S224.
73. Pai-Scherf, L.H.; Villa, J.; Pearson, D.; Watson, T.; Liu, E.; Willingham, M.C.; Pastan, I. Hepatotoxicity in cancer patients receiving erb-38, a recombinant immunotoxin that targets the erbB2 receptor. Clin. Cancer Res. 1999, 5, 2311-2315.
74. Kreitman, R.J. Immunotoxins for targeted cancer therapy. AAPS J. 2006, 8, E532-E551.
75. Kreitman, R.J.; Pastan, I. Immunotoxins in the treatment of hematologic malignancies. Curr. Drug Targets 2006, 7, 1301-1311.
76. Lord, J.M.; Roberts, L.M.; Robertus, J.D. Ricin: Structure, mode of action, and some current applications. FASEB J. 1994, 8, 201-208.
77. Lambert, J.M.; Goldmacher, V.S.; Collinson, A.R.; Nadler, L.M.; Blattler, W.A. An immunotoxin prepared with blocked ricin: A natural plant toxin adapted for therapeutic use. Cancer Res. 1991, 51, 6236-6242.
78. Grossbard, M.L.; Fidias, P.; Kinsella, J.; O'Toole, J.; Lambert, J.M.; Blattler, W.A.; Esseltine, D.; Braman, G.; Nadler, L.M.; Anderson, K.C. Anti-B4-blocked ricin: A phase II trial of 7 day continuous infusion in patients with multiple myeloma. Br. J. Haematol. 1998, 102, 509-515.
79. Recht, L.; Torres, C.O.; Smith, T.W.; Raso, V.; Griffin, T.W. Transferrin receptor in normal and neoplastic brain tissue: Implications for brain-tumor immunotherapy. J. Neurosurg. 1990, 72, 941-945.
80. Trowbridge, I.S.; Domingo, D.L. Anti-transferrin receptor monoclonal antibody and toxin-antibody conjugates affect growth of human tumour cells. Nature 1981, 294, 171-173.
81. Qian, Z.M.; Li, H.; Sun, H.; Ho, K. Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway. Pharmacol. Rev. 2002, 54, 561-587.
82. Hagihara, N.; Walbridge, S.; Olson, A.W.; Oldfield, E.H.; Youle, R.J. Vascular protection by chloroquine during brain tumor therapy with Tf-CRM107. Cancer Res. 2000, 60, 230-234.
83. Shinohara, H.; Fan, D.; Ozawa, S.; Yano, S.; Van, A.M.; Viner, J.L.; Beers, R.; Pastan, I.; Fidler, I.J. Site-specific expression of transferrin receptor by human colon cancer cells directly correlates with eradication by antitransferrin recombinant immunotoxin. Int. J. Oncol. 2000, 17, 643-651.
84. Hall, W.A. Targeted toxin therapy for malignant astrocytoma. Neurosurgery 2000, 46, 544-551.
85. Singh, M. Transferrin as a targeting ligand for liposomes and anticancer drugs. Curr. Pharm. Des. 1999, 5, 443-451.
86. Citores, L.; Ferreras, J.M.; Munoz, R.; Benitez, J.; Jimenez, P.; Girbes, T. Targeting cancer cells with transferrin conjugates containing the non-toxic type 2 ribosome-inactivating proteins nigrin b or ebulin l. Cancer Lett. 2002, 184, 29-35.
87. Hall, W.A.; Godal, A.; Juell, S.; Fodstad, O. In vitro efficacy of transferrin-toxin conjugates against glioblastoma multiforme. J. Neurosurg. 1992, 76, 838-844.
88. Recht, L.D.; Raso, V.; Davis, R.; Salmonsen, R. Immunotoxin sensitivity of Chinese hamster ovary cells expressing human transferrin receptors with differing internalization rates. Cancer Immunol. Immunother. 1996, 42, 357-361.
89. Ippoliti, R.; Lendaro, E.; D'Agostino, I.; Fiani, M.L.; Guidarini, D.; Vestri, S.; Benedetti, P.A.; Brunori, M. A chimeric saporin-transferrin conjugate compared to ricin toxin: Role of the carrier in intracellular transport and toxicity. FASEB J. 1995, 9, 1220-1225.
90. Munoz, R.; Arias, Y.; Ferreras, J.M.; Jimenez, P.; Rojo, M.A.; Girbes, T. Sensitivity of cancer cell lines to the novel non-toxic type 2 ribosome-inactivating protein nigrin b. Cancer Lett. 2001, 167, 163-169.
91. Munoz, R.; Arias, Y.; Ferreras, J.M.; Rojo, M.A.; Gayoso, M.J.; Nocito, M.; Benitez, J.; Jimenez, P.; Bernabeu, C.; Girbes, T. Targeting a marker of the tumour neovasculature using a novel anti-human CD105-immunotoxin containing the non-toxic type 2 ribosome-inactivating protein nigrin b. Cancer Lett. 2007, 256, 73-80.
92. Benitez, J.; Ferreras, J.M.; Munoz, R.; Arias, Y.; Iglesias, R.; Cordoba-Diaz, M.; del Villar, R.; Girbes, T. Cytotoxicity of an ebulin l-anti-human CD105 immunotoxin on mouse fibroblasts (L929) and rat myoblasts (L6E9) cells expressing human CD105. Med. Chem. 2005, 1, 65-70.
93. Folkman, J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1995, 1, 27-31.
94. Folkman, J. Angiogenesis. Annu. Rev Med. 2006, 57, 1-18.
95. Hanahan, D.; Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996, 86, 353-364.
96. Nussenbaum, F.; Herman, I.M. Tumor angiogenesis: Insights and innovations. J. Oncol. 2010, 2010, 132641.
97. Jain, R.K. Vascular and interstitial barriers to delivery of therapeutic agents in tumors. Cancer Metastasis Rev. 1990, 9, 253-266.
98. Heldin, C.H.; Rubin, K.; Pietras, K.; Ostman, A. High interstitial fluid pressure-an obstacle in cancer therapy. Nat. Rev. Cancer 2004, 4, 806-813.
99. Fonsatti, E.; Nicolay, H.J.; Altomonte, M.; Covre, A.; Maio, M. Targeting cancer vasculature via endoglin/CD105: A novel antibody-based diagnostic and therapeutic strategy in solid tumours. Cardiovasc. Res. 2010, 86, 12-19.
100. Novak, K. Angiogenesis inhibitors revised and revived at AACR. American Association for Cancer Research. Nat. Med. 2002, 8, 427.
101. von Mehren, M.; Adams, G.P.; Weiner, L.M. Monoclonal antibody therapy for cancer. Annu. Rev. Med. 2003, 54, 343-369.
102. Tabata, M.; Kondo, M.; Haruta, Y.; Seon, B.K. Antiangiogenic radioimmunotherapy of human solid tumors in SCID mice using (125)I-labeled anti-endoglin monoclonal antibodies. Int. J. Cancer 1999, 82, 737-742.
103. Maio, M.; Altomonte, M.; Fonsatti, E. Is it the primetime for endoglin (CD105) in the clinical setting? Cardiovasc. Res. 2006, 69, 781-783.
104. Duff, S.E.; Li, C.; Garland, J.M.; Kumar, S. CD105 is important for angiogenesis: Evidence and potential applications. FASEB J. 2003, 17, 984-992.
105. Bodey, B.; Bodey, B., Jr.; Siegel, S.E.; Kaiser, H.E. Immunocytochemical detection of endoglin is indicative of angiogenesis in malignant melanoma. Anticancer Res. 1998, 18, 2701-2710.
106. Li, C.; Guo, B.; Bernabeu, C.; Kumar, S. Angiogenesis in breast cancer: The role of transforming growth factor beta and CD105. Microsc. Res. Tech. 2001, 52, 437-449.
107. Fonsatti, E.; Altomonte, M.; Nicotra, M.R.; Natali, P.G.; Maio, M. Endoglin (CD105): A powerful therapeutic target on tumor-associated angiogenetic blood vessels. Oncogene 2003, 22, 6557-6563.
108. Zijlmans, H.J.; Fleuren, G.J.; Hazelbag, S.; Sier, C.F.; Dreef, E.J.; Kenter, G.G.; Gorter, A. Expression of endoglin (CD105) in cervical cancer. Br. J. Cancer 2009, 100, 1617-1626.
109. Kuiper, P.; Hawinkels, L.J.; de Jonge-Muller, E.S.; Biemond, I.; Lamers, C.B.; Verspaget, H.W. Angiogenic markers endoglin and vascular endothelial growth factor in gastroenteropancreatic neuroendocrine tumors. World J. Gastroenterol. 2011, 17, 219-225.
110. Fonsatti, E.; Jekunen, A.P.; Kairemo, K.J.; Coral, S.; Snellman, M.; Nicotra, M.R.; Natali, P.G.; Altomonte, M.; Maio, M. Endoglin is a suitable target for efficient imaging of solid tumors: In vivo evidence in a canine mammary carcinoma model. Clin. Cancer Res. 2000, 6, 2037-2043.
111. Bredow, S.; Lewin, M.; Hofmann, B.; Marecos, E.; Weissleder, R. Imaging of tumour neovasculature by targeting the TGF-beta binding receptor endoglin. Eur. J. Cancer 2000, 36, 675-681.
112. Li, C.; Guo, B.; Wilson, P.B.; Stewart, A.; Byrne, G.; Bundred, N.; Kumar, S. Plasma levels of soluble CD105 correlate with metastasis in patients with breast cancer. Int. J. Cancer 2000, 89, 122-126.
113. Burrows, F.J.; Derbyshire, E.J.; Tazzari, P.L.; Amlot, P.; Gazdar, A.F.; King, S.W.; Letarte, M.; Vitetta, E.S.; Thorpe, P.E. Up-regulation of endoglin on vascular endothelial cells in human solid tumors: Implications for diagnosis and therapy. Clin. Cancer Res. 1995, 1, 1623-1634.
114. Marioni, G.; Ottaviano, G.; Giacomelli, L.; Staffieri, C.; Casarotti-Todeschini, S.; Bonandini, E.; Staffieri, A.; Blandamura, S. CD105-assessed micro-vessel density is associated with malignancy recurrence in laryngeal squamous cell carcinoma. Eur. J. Surg. Oncol. 2006, 32, 1149-1153.
115. Matsuno, F.; Haruta, Y.; Kondo, M.; Tsai, H.; Barcos, M.; Seon, B.K. Induction of lasting complete regression of preformed distinct solid tumors by targeting the tumor vasculature using two new anti-endoglin monoclonal antibodies. Clin. Cancer Res. 1999, 5, 371-382.
116. Maier, J.A.; Delia, D.; Thorpe, P.E.; Gasparini, G. In vitro inhibition of endothelial cell growth by the antiangiogenic drug AGM-1470 (TNP-470) and the anti-endoglin antibody TEC-11. Anticancer Drugs 1997, 8, 238-244.
117. Raab, U.; Velasco, B.; Lastres, P.; Letamendia, A.; Cales, C.; Langa, C.; Tapia, E.; Lopez-Bote, J.P.; Paez, E.; Bernabeu, C. Expression of normal and truncated forms of human endoglin. Biochem. J. 1999, 339, 579-588.
118. Benitez, J.; Rojo, M.A.; Munoz R.; Ferreras, J.M.; Jimenez, P.; Girbes T. Design and cytotoxicity analysis of a conjugate containing the new D-galactose-binding lectin SELld and the non-toxic type 2 ribosome-inactivating protein nigrin b. Lett. Drug Des. Discov. 2004, 1, 35-44.
119. Bolognesi, A.; Tazzari, P.L.; Olivieri, F.; Polito, L.; Falini, B.; Stirpe, F. Induction of apoptosis by ribosome-inactivating proteins and related immunotoxins. Int. J. Cancer 1996, 68, 349-355.
120. Szatrowski, T.P.; Dodge, R.K.; Reynolds, C.; Westbrook, C.A.; Frankel, S.R.; Sklar, J.; Stewart, C.C.; Hurd, D.D.; Kolitz, J.E.; Velez-Garcia, E.; et al. Lineage specific treatment of adult patients with acute lymphoblastic leukemia in first remission with anti-B4-blocked ricin or high-dose cytarabine: Cancer and Leukemia Group B Study 9311. Cancer 2003, 97, 1471-1480.
121. Lavelle, E.; Grant, G.; Pfüller, U.; Girbes, T.; Jimenez, P.; Pusztai, A.; Leavy, O.; Mills, K.H.G.; O'Hagan, D.T. Mucosal Immunogenicity and Adjuvanticity of Plant Lectins. Immunology 2000, 52, 415.
122. Baluna, R.; Coleman, E.; Jones, C.; Ghetie, V.; Vitetta, E.S. The effect of a monoclonal antibody coupled to ricin A chain-derived peptides on endothelial cells in vitro: Insights into toxin-mediated vascular damage. Exp. Cell Res. 2000, 258, 417-424.