The neovasculature homing motif NGR: More than meets the eye

Blood

Volumn 112, Issue 7, 2008, Pages 2628-2635

  Corti, Angelo ^a   Curnis, Flavio ^a   Arap, Wadih ^b   Pasqualini, Renata ^b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPEPTIDASE; ARGININE; ASPARAGINE; CISPLATIN; DOXORUBICIN; FIBRONECTIN; GEMCITABINE; GLYCINE; INTEGRIN; ISOASPARTIC ACID; MELPHALAN; MICROSOMAL AMINOPEPTIDASE; PACLITAXEL; PLASMID VECTOR; PROTEIN NGR; RECOMBINANT GAMMA INTERFERON; SYNTHETIC PEPTIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN; NGR PEPTIDE; OLIGOPEPTIDE;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; DEAMINATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; ENDOTHELIUM CELL; HUMAN; LOW DRUG DOSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; CHEMISTRY; METABOLISM; REVIEW;

AMINO ACID MOTIFS; ANIMALS; CELL ADHESION; DRUG DELIVERY SYSTEMS; HUMANS; INTEGRINS; NEOVASCULARIZATION, PATHOLOGIC; OLIGOPEPTIDES;

EID: 53449088574     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-04-150862     Document Type: Article

References (87)

1. Arap W, Kolonin MG; Trepel M, et al. Steps toward mapping the human vasculature by phage display. Nat Med. 2002;8:121-127.
2. Pasqualini R, Ruoslahti E. Organ targeting in vivo using phage display peptide libraries. Nature. 1996;380:364-366.
3. ArapW, Pasqualini R. Ruoslahti E. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science. 1998;279:377-380.
4. Curnis F, Longhi R, Crippa L, et al. Spontaneous formation of L-isoaspartate and gain of function in fibronectin. J Biol Chem. 2006;281:36466-36476.
5. Koivunen E, Gay DA, Ruoslahti E. Selection of peptides binding to the alpha 5 beta 1 integrin from phage display library. J Biol Chem. 1993; 268:20205-20210.
6. Koivunen E, Wang B. Ruoslahti E. Isolation of a highly specific ligand for the alpha 5 beta 1 integrin from a phage display library. J Cell Biol. 1994;124:373-380.
7. Kornblihtt AR, Umezawa K. Vibe-Pedersen K. Baralle FE. Primary structure of human fibronectin: differential splicing may generate at least 10 polypeptides from a single gene. EMBOJ 1985;4:1755-1759.
8. Healy JM, Murayama O, MaedaT et al. Peptide ligands for integrin alpha v beta 3 selected from random phage display libraries. Biochemistry. 1995;34:3948-3955.
9. Pasqualini R, Koivunen E, Ruoslahti E. Alpha v integrins as receptors for tumor targeting by circulating ligands [see comments]. Nat Biotechnol. 1997;15:542-546.
10. Pasqualini R, Koivunen E, Kain R. et al. Aminopeptidase N is a receptor for tumor-homing peptides and atargetfor inhibiting angiogenesis. Cancer Res. 2000:60:722-727.
11. Luan Y Xu W. The structure and main functions of aminopeptidase N. Curr Med Chem. 2007;14: 639-647.
12. Riemann D. KehlenA. Langner J. CD13-notjust a marker in leukemia typing. Immunol Today. 1999;20:83-88.
13. Razak K, Newland AC. The significance of aminopeptidases and haematopoietic cell differentiation. Blood Rev. 1992;6:243-250.
14. Curnis F. Arrigoni G. Sacchi A, et al. Differential binding of drugs containing the NGR motif to CD 13 isoforms in tumor vessels, epithelia, and myeloid cells. Cancer Res. 2002;62:867-874.
15. BuehlerA, van Zandvoort MA, Stelt BJ, et al. cNGR: a novel homing sequence for GD13/APN targeted molecular imaging of murine cardiac angiogenesis in vivo. ArteriosclerThromb Vase Biol. 2006;26:2681-2687.
16. Lahdenranta J, Sidman RL Pasqualini R, Arap W. Treatment of hypoxia-induced retinopathy with targeted proapoptotic peptidomimetic in a mouse model of disease. FASEB J 2007;21:3272-3278.
17. Taylor A. Aminopeptidases: structure and function. FASEB J 1993;7:290-298.
18. Shipp MA. Look AT. Hematopoietic differentiation antigens that are membrane-associated enzymes: cutting is the key. Blood. 1993;82:1052-1070.
19. Dixon J, Kaklamanis L. Turley H. et al. Expression of aminopeptidase-n (CD 13) in normal tissues and malignant neoplasms of epithelial and lymphoid origin. J Clin Pathol. 1994;47:43-47.
20. Chen H, Kinzer CA, Paul WE. p161, a murine membrane protein expressed on mast cells and some macrophages, is mouse CD13/aminopeptidase N. J Immunol. 1996;157:2593-2600.
21. Drexler HG. Classification of acute myeloid leukemias-a comparison of FAB and immunophenotyping. Leukemia. 1987;1:697-705.
22. Ozawa MG, Zurita AJ, Dias-Neto E, et al. Beyond receptor expression levels: the relevance of target accessibility in ligand-directed pharmacodelivery systems. Trends Cardiovasc Med. 2008;18: 126-133.
23. Look AT, Ashmun RA, Shapiro LH, Peiper SC. Human myeloid plasma membrane glycoprotein CD13 (gp150) is identical to aminopeptidase N. J Clin Invest. 1989;83:1299-1307.
24. Look AT Peiper SC, Rebentisch MB, et al. Transfer and expression of the gene encoding a human myeloid membrane antigen (gp150). J Clin Invest. 1985;75:569-579.
25. O'Connell PJ, Gerkis V. d'Apice AJ. Variable O-glycosylation of CD13 (aminopeptidase N). J Biol Chem. 1991;266:4593-4597.
26. Xu Y, Wellner D, Scheinberg DA. Cryptic and regulatory epitopes in CD13/aminopeptidase N. Exp Hematol. 1997;25:521-529.
27. Yang E, Shim JS, Woo HJ, Kim KW, Kwon HJ. Aminopeptidase N/CD13 induces angiogenesis through interaction with a pro-angiogenic protein, galectin-3. Biochem Biophys Res Commun. 2007;363:336-341.
28. Pastorino F, Brignole C, Di Paolo D, et al. Targeting liposomal chemotherapy via both tumor cellspecific and tumor vasculature-specific ligands potentiates therapeutic efficacy. Cancer Res. 2006;66:10073-10082.
29. Pastorino F, Brignole C, Marimpietri D, et al. Vascular damage and anti-angiogenic effects of tumor vessel-targeted liposomal chemotherapy. Cancer Res. 2003;63:7400-7409.
30. Garde SV, Forte AJ, Ge M, et al. Binding and internalization of NGR-peptide-targeted liposomal doxorubicin (TVT-DOX) in CD13-expressing cells and its antitumor effects. Anticancer Drugs. 2007; 18:1189-1200.
31. Ellerby HM, Arap W, Ellerby LM, et al. Anti-cancer activity of targeted pro-apoptotic peptides. Nat Med. 1999;5:1032-1038.
32. Curnis F, Sacchi A, Borgna L, et al. Enhancement of tumor necrosis factor alpha antitumor immunotherapeutic properties by targeted delivery to aminopeptidase N (CD13). Nat Biotechnol. 2000;18: 1185-1190.
33. Corti A. Strategies for improving the antineoplastic activity of TN F by tumor targeting. Methods Mol Med. 2004;98:247-264.
34. Curnis F, Sacchi A, Corti A. Improving chemotherapeutic drug penetration in tumors by vascular targeting and barrier alteration. J Clin Invest. 2002;110:475-482.
35. Sacchi A, Gasparri A, Curnis F, Bellone M, Corti A. Crucial role for interferon-gamma in the synergism between tumor vasculature-targeted tumor necrosis factor alpha (NGR-TNF)and doxorubicin. Cancer Res. 2004;64:7150-7155.
36. Zarovni N. Monaco L, Corti A. Inhibition of tumor growth by intramuscular injection of cDNA encoding tumor necrosis factor alpha coupled to NGR and RGD tumor-homing peptides. Hum Gene Ther. 2004;15:373-382.
37. Sacchi A. Gasparri A, Gallo-Stampino C, et al. Synergistic antitumor activity of cisplatin, paclitaxel, and gemcitabine with tumor vasculaturetargeted tumor necrosis factor-alpha. Clin Cancer Res. 2006;12:175-182.
38. Corti A, Ponzoni M. Tumor vascular targeting with tumor necrosis factor alpha and chemotherapeutic drugs. Ann N Y Acad Sci. 2004;1028:104-112.
39. Gleave ME, Elhilali M, Fradet Y, et al. Interferon gamma-1 b compared with placebo in metastatic renal-cell carcinoma. Canadian Urologic Oncology Group. N Engl J Med. 1998:338: 1265-1271.
40. Curnis F, Gasparri A, Sacchi A, et al. Targeted delivery of I FN-gamma to tumor vessels uncouples anti-tumor from counter-regulatory mechanisms. Cancer Res. 2005;65:2906-2913.
41. Meng J, Yan Z, Wu J, et al. High-yield expression, purification and characterization of tumor-targeted IFN-alpha2a. Cytotherapy. 2007;9:60-68.
42. YokoyamaY, Ramakrishnan S. Addition of an aminopeptidase N-binding sequence to human endostatin improves inhibition of ovarian carcinoma growth. Cancer. 2005;104:321-331.
43. Meng J, Ma N, Yan Z, Han W, Zhang Y NGR enhanced the anti-angiogenic activity of tum-5. J Biochem (Tokyo) 2006:140:299-304.
44. Grifman M, Trepel M, Speece P, et al. Incorporation of tumor-targeting peptides into recombinant adeno-associated virus capsids. Mol Ther. 2001; 3:964-975.
45. Liu L, Anderson WF, Beart RW, Gordon EM, Hall FL. Incorporation of tumor vasculature targeting motifs into moloney murine leukemia virus env escort proteins enhances retrovirus binding and transduction of human endothelial cells. J Virol. 2000;74:5320-5328.
46. Moffatt S. Wiehle S, Cristiano RJ. Tumor-specific gene delivery mediated by a novel peptidepolyethylenimine-DNA polyplex targeting aminopeptidase N/CD13. Hum Gene Ther. 2005; 16:57-67.
47. Moffatt S, Cristiano RJ. Uptake characteristics of NGR-coupled stealth PEI/pDNA nanoparticles loaded with PLGA-PEG-PLGA tri-block copolymer for targeted delivery to human monocytederived dendritic cells. Int J Pharm. 2006;321: 143-154.
48. Holle L, Song W, Hicks L, et al. In vitro targeted killing of human endothelial cells by co-incubation of human serum and NGR peptide conjugated human albumin protein bearing alpha (1-3) galactose epitopes. Oncol Rep. 2004;11: 613-616.
49. Zhang Z, Harada H, Tanabe K, et al. Aminopeptidase N/CD13 targeting fluorescent probes: synthesis and application to tumor cell imaging. Peptides. 2005;26:2182-2187.
50. Dirksen A, Langereis S, de Waal BF, et al. Design and synthesis of a bimodal target-specific contrast agent for angiogenesis. Org Lett. 2004;6: 4857-4860.
51. von Wallbrunn A, Waldeck J, Holtke C, et al. In vivo optical imaging of CD13/APN-expression in tumor xenografts. J Biomed Opt. 2008;13:011007.
52. Curnis F, Gasparri A, Sacchi A, et al. Targeted delivery of I FNgamma to tumor vessels uncouples antitumor from counterregulatory mechanisms. Cancer Res. 2005:65:2906-2913.
53. Mizuguchi H, Koizumi N, Hosono T, et al. A simplified system for constructing recombinant adenoviral vectors containing heterologous peptides in the HI loop of their fiber knob. Gene Ther. 2001;8: 730-735.
54. Koivunen E, Wang B, Ruoslahti E. Isolation of a highly specific ligand for the alpha 5 beta 1 integrin from a phage display library. J Cell Biol. 1994:124:373-380.
55. Koivunen E, Wang B, Ruoslahti E. Phage libraries displaying cyclic peptides with different ring sizes: ligand specificities of the RGD-directed integrins. Bio/Technology. 1995:13:265-270.
56. Colombo G, Curnis F, De Mori GM, et al. Structure-activity relationships of linear and cyclic peptides containing the NGR tumor-homing motif. J Biol Chem. 2002;277:47891-47897.
57. Majhen D, Gabrilovac J, Eloit M, Richardson J, Ambriovic-Ristov A. Disulfide bond formation in NGR fiber-modified adenovirus is essential for retargeting to aminopeptidase N. Biochem Biophys Res Commun. 2006;348:278-287.
58. FuzeryAK. Mihala N. Szabo P. et al. Solution state conformation and degradation of cyclopeptides containing an NGR motif. J Pept Sci. 2005; 11:53-59.
59. Di Matteo P. Curnis F, Longhi R, et al. Immunogenic and structural properties of the Asn-Gly-Arg (NGR) tumor neovasculature-homing motif. Mol Immunol. 2006;43:1509-1518.
60. Bairoch A, Apweiler R. The Swiss-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acid Res. 2000;28:45-48.
61. Pankov R, Yamada KM. Fibronectin at a glance. J Cell Sci. 2002;115:3861-3863.
62. Matsas R, Stephenson SL, Hryszko J, Kenny AJ, Turner AJ. The metabolism of neuropeptides. Phase separation of synaptic membrane preparations with Triton X-114 reveals the presence of aminopeptidase N. Biochem J 1985;231:445-449.
63. Hoffmann T, Faust J, Neubert K, Ansorge S. Dipeptidyl peptidase IV (CD 26) and aminopeptidase N (CD 13) catalyzed hydrolysis of cytokines and peptides with N-terminal cytokine sequences. FEBS Lett. 1993;336:61-64.
64. van Hensbergen Y, Broxterman HJ, Elderkamp YW, et al. A doxorubicin-CNGRC-peptide conjugate with prodrug properties. Biochem Pharmacol. 2002;63:897-908.
65. Saiki I, Fujii H, Yoneda J, et al. Role of aminopeptidase N (CD13) in tumor-cell invasion and extracellular matrix degradation. Int J Cancer. 1993; 54:137-143.
66. Menrad A, Speicher D, Wacker J, Herlyn M. Biochemical and functional characterization of aminopeptidase N expressed by human melanoma cells. Cancer Res. 1993;53:1450-1455.
67. Bhagwat SV, Lahdenranta J, Giordano R, et al. CD13/APN is activated by angiogenic signals and is essential for capillary tube formation. Blood. 2001;97:652-659.
68. Rangel R, Sun Y, Guzman-Rojas L, et al. Impaired angiogenesis in aminopeptidase N-null mice. Proc Natl Acad Sci U S A. 2007; 104:4588-4593.
69. Fukasawa K, Fujii H, Saitoh Y, et al. Aminopeptidase N (APN/CD13) is selectively expressed in vascular endothelial cells and plays multiple roles in angiogenesis. Cancer Lett. 2006;243:135-143.
70. Petrovic N. Schacke W, Gahagan JR, et al. CD13/APN regulates endothelial invasion and filopodia formation. Blood. 2007;110:142-150.
71. Santos AN, Langner J, Herrmann M, Riemann D. Aminopeptidase N/CD13 is directly linked to signal transduction pathways in monocytes. Cell Immunol. 2000;201:22-32.
72. Olsen J, Cowell GM, Konigshofer E, et al. Complete amino acid sequence of human intestinal aminopeptidase N as deduced from cloned cDNA. FEBS Lett. 1988;238:307-314.
73. Asokan A, Hamra JB, Govindasamy L, Agbandje-McKenna M, Samulski RJ. Adeno-associated virus type 2 contains an integrin alpha5beta1 binding domain essential for viral cell entry. J Virol. 2006;80:8961-8969.
74. Reissner KJ, Aswad DW. Deamidation and isoaspartate formation in proteins: unwanted alterations or surreptitious signals? Cell Mol Life Sci. 2003;60:1281-1295.
75. Robinson NE, Robinson AB. Amide molecular clocks in drosophila proteins: potential regulators of aging and other processes. Mech Ageing Dev. 2004;125:259-267.
76. Lanthier J, Desrosiers RR. Protein L-isoaspartyl methyltransterase repairs abnormal aspartyl residues accumulated in vivo in type-l collagen and restores cell migration. Exp Cell Res. 2004:293: 96-105.
77. Spitaleri A, Mari S, Curnis F, et al. Structural basis for the interaction of isoDGR with the RGD-binding site of avbeta 3 integrin. J Biol Chem. 2008; May 13 [Epub ahead of print].
78. Pussell BA, Peake PW, Brown MA, Charlesworth JA. Human fibronectin metabolism. J Clin Invest. 1985:76:143-148.
79. Humphries MJ, Obara M, Olden K, Yamada KM. Role of fibronectin in adhesion, migration, and metastasis. Cancer Invest. 1989:7:373-393.
80. Wierzbicka-Patynowski I, Schwarzbauer JE. The ins and outs of fibronectin matrix assembly. J Cell Sci. 2003:116:3269-3276.
81. Takahashi S, Leiss M, Moser M, et al. The RGD motif in fibronectin is essential for development but dispensable for fibril assembly. J Cell Biol. 2007;178:167-178.
82. Brooks PC. Silletti S. von SchalschaTL, Friedlander M, Cheresh DA. Disruption of angiogenesis by PEX, a non catalytic metalloproteinase fragment with integrin binding activity. Cell. 1998; 92:391-400.
83. Tarui T, Miles LA, Takada Y. Specific interaction of angiostatin with integrin alpha(v)beta(3) in endothelial cells. J Biol Chem. 2001;276:39562- 39568.
84. Rehn M, VeikkolaT, Kukk-Valdre E, et al. Interaction of endostatin with integrins implicated in angiogenesis. Proc Natl Acad Sci U S A. 2001;98: 1024-1029.
85. Weber DJ, McFadden PN. Detection and characterization of a protein isoaspartyl methyltransterase which becomes trapped in the extracellular space during blood vessel injury. J Protein Chem. 1997;16:257-267.
86. Weber DJ, McFadden PN. Injury-induced enzymatic methylation of aging collagen in the extracellular matrix of blood vessels. J Protein Chem. 1997;16:269-281.
87. Obenauer JC, Cantley LC, Yaffe MB. Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 2003;31:3635-3641.