Small-animal SPECT/CT imaging of cancer xenografts and pulmonary fibrosis using a 99mTc-labeled integrin αvβ6-targeting cyclic peptide with improved in vivo stability

Hao Líu1, Liquan Gao1, Xinhe Yu1, Liang Zhong2, Jiyun Shi3, Bing Jia1, Nan Li4, Zhaofei Liu1, Fan Wang3
1Medical Isotopes Research Center and Department of Radiation Medicine, School of Basic Medical Sciences, Peking University Health Science Center, Beijing, 100191, China
2Medical and Healthy Analytical Center, Peking University, Beijing 100191, China
3Key Laboratory of Protein and Peptide Pharmaceuticals, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
4Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Nuclear Medicine, Peking University Cancer Hospital & Institute, Beijing 100142, China

Tóm tắt

Từ khóa


Tài liệu tham khảo

Agarwal SK (2014) Integrins and cadherins as therapeutic targets in fibrosis. Front Pharmacol 5:131

Ambrosini V, Zompatori M, De Luca F, Antonia D, Allegri V, Nanni C, Malvi D, Tonveronachi E, Fasano L, Fabbri M, Fanti S (2010) 68Ga-DOTANOC PET/CT allows somatostatin receptor imaging in idiopathic pulmonary fibrosis: preliminary results. J Nucl Med 51:1950–1955

Bates RC (2005) Colorectal cancer progression: integrin alphavbeta6 and the epithelial-mesenchymal transition (EMT). Cell Cycle 4:1350–1352

Bates RC, Mercurio AM (2005) The epithelial-mesenchymal transition (EMT) and colorectal cancer progression. Cancer Biol Ther 4:365–370

Besser D, Muller B, Kleinwachter P, Greiner G, Seyfarth L, Steinmetzer T, Arad O, Reissmann S (2000) Synthesis and characterization of octapeptide somatostatin analogues with backbone cyclization: comparison of different strategies, biological activities and enzymatic stabilities. J Prakt Chem 342:537–545

Bogdanowich-Knipp SJ, Chakrabarti S, Williams TD, Dillman RK, Siahaan TJ (1999a) Solution stability of linear vs. cyclic RGD peptides. J Pept Res 53:530–541

Bogdanowich-Knipp SJ, Jois DS, Siahaan TJ (1999b) The effect of conformation on the solution stability of linear vs. cyclic RGD peptides. J Pept Res 53:523–529

Breuss JM, Gillett N, Lu L, Sheppard D, Pytela R (1993) Restricted distribution of integrin beta6 mRNA in primate epithelial tissues. J Histochem Cytochem 41:1521–1527

Cai Y, Zhu L, Zhang F, Niu G, Lee S, Kimura S, Chen X (2013) Noninvasive monitoring of pulmonary fibrosis by targeting matrix metalloproteinases (MMPs). Mol Pharm 10:2237–2247

Cantor DI, Cheruku HR, Nice EC, Baker MS (2015) Integrin alphavbeta6 sets the stage for colorectal cancer metastasis. Cancer Metastasis Rev 34:715–734

Desgrosellier JS, Cheresh DA (2010) Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 10:9–22

Dong C, Liu Z, Wang F (2015) Radioligand saturation binding for quantitative analysis of ligand-receptor interactions. Biophys Rep 1:148–155

Elayadi AN, Samli KN, Prudkin L, Liu YH, Bian A, Xie XJ, Wistuba II, Roth JA, McGuire MJ, Brown KC (2007) A peptide selected by biopanning identifies the integrin alphavbeta6 as a prognostic biomarker for nonsmall cell lung cancer. Cancer Res 67:5889–5895

Gilon C, Halle D, Chorev M, Selinger Z, Byk G (1991) Backbone cyclization: a new method for conferring conformational constraint on peptides. Biopolymers 31:745–750

Gribbin J, Hubbard RB, Le Jeune I, Smith CJ, West J, Tata LJ (2006) Incidence and mortality of idiopathic pulmonary fibrosis and sarcoidosis in the UK. Thorax 61:980–985

Hackel BJ, Kimura RH, Miao Z, Liu H, Sathirachinda A, Cheng Z, Chin FT, Gambhir SS (2013) 18F-fluorobenzoate-labeled cystine knot peptides for PET imaging of integrin alphavbeta6. J Nucl Med 54:1101–1105

Hausner SH, DiCara D, Marik J, Marshall JF, Sutcliffe JL (2007) Use of a peptide derived from foot-and-mouth disease virus for the noninvasive imaging of human cancer: generation and evaluation of 4-[18F]fluorobenzoyl A20FMDV2 for in vivo imaging of integrin alphavbeta6 expression with positron emission tomography. Cancer Res 67:7833–7840

Hausner SH, Marik J, Gagnon MK, Sutcliffe JL (2008) In vivo positron emission tomography (PET) imaging with an alphavbeta6 specific peptide radiolabeled using 18F-”click” chemistry: evaluation and comparison with the corresponding 4-[18F]fluorobenzoyl- and 2-[18F]fluoropropionyl-peptides. J Med Chem 51:5901–5904

Hausner SH, Abbey CK, Bold RJ, Gagnon MK, Marik J, Marshall JF, Stanecki CE, Sutcliffe JL (2009a) Targeted in vivo imaging of integrin alphavbeta6 with an improved radiotracer and its relevance in a pancreatic tumor model. Cancer Res 69:5843–5850

Hausner SH, Kukis DL, Gagnon MK, Stanecki CE, Ferdani R, Marshall JF, Anderson CJ, Sutcliffe JL (2009b) Evaluation of [64Cu]Cu-DOTA and [64Cu]Cu-CB-TE2A chelates for targeted positron emission tomography with an alphavbeta6-specific peptide. Mol Imaging 8:111–121

Hausner SH, Carpenter RD, Bauer N, Sutcliffe JL (2013) Evaluation of an integrin alphavbeta6-specific peptide labeled with [18F]fluorine by copper-free, strain-promoted click chemistry. Nucl Med Biol 40:233–239

Horan GS, Wood S, Ona V, Li DJ, Lukashev ME, Weinreb PH, Simon KJ, Hahm K, Allaire NE, Rinaldi NJ, Goyal J, Feghali-Bostwick CA, Matteson EL, O’Hara C, Lafyatis R, Davis GS, Huang X, Sheppard D, Violette SM (2008) Partial inhibition of integrin alphavbeta6 prevents pulmonary fibrosis without exacerbating inflammation. Am J Respir Crit Care Med 177:56–65

Hu LY, Bauer N, Knight LM, Li Z, Liu S, Anderson CJ, Conti PS, Sutcliffe JL (2014) Characterization and evaluation of 64Cu-labeled A20FMDV2 conjugates for imaging the integrin alphavbeta 6. Mol Imaging Biol 16:567–577

Jia B, Shi J, Yang Z, Xu B, Liu Z, Zhao H, Liu S, Wang F (2006) 99mTc-labeled cyclic RGDfK dimer: initial evaluation for SPECT imaging of glioma integrin alphavbeta3 expression. Bioconjug Chem 17:1069–1076

John AE, Luckett JC, Tatler AL, Awais RO, Desai A, Habgood A, Ludbrook S, Blanchard AD, Perkins AC, Jenkins RG, Marshall JF (2013) Preclinical SPECT/CT imaging of alphavbeta6 integrins for molecular stratification of idiopathic pulmonary fibrosis. J Nucl Med 54:2146–2152

Kimura RH, Teed R, Hackel BJ, Pysz MA, Chuang CZ, Sathirachinda A, Willmann JK, Gambhir SS (2012) Pharmacokinetically stabilized cystine knot peptides that bind alphavbeta6 integrin with single-digit nanomolar affinities for detection of pancreatic cancer. Clin Cancer Res 18:839–849

Lee JS, Heo J, Libbrecht L, Chu IS, Kaposi-Novak P, Calvisi DF, Mikaelyan A, Roberts LR, Demetris AJ, Sun Z, Nevens F, Roskams T, Thorgeirsson SS (2006) A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 12:410–416

Li F, Song Z, Li Q, Wu J, Wang J, Xie C, Tu C, Wang J, Huang X, Lu W (2011) Molecular imaging of hepatic stellate cell activity by visualization of hepatic integrin alphavbeta3 expression with SPECT in rat. Hepatology 54:1020–1030

Liu Z, Jin C, Yu Z, Zhang J, Liu Y, Zhao H, Jia B, Wang F (2010) Radioimmunotherapy of human colon cancer xenografts with 131I-labeled anti-CEA monoclonal antibody. Bioconjug Chem 21:314–318

Liu H, Wu Y, Wang F, Liu Z (2014a) Molecular imaging of integrin alphavbeta6 expression in living subjects. Am J Nucl Med Mol Imaging 4:333–345

Liu Z, Liu H, Ma T, Sun X, Shi J, Jia B, Sun Y, Zhan J, Zhang H, Zhu Z, Wang F (2014b) Integrin alphavbeta6-targeted SPECT imaging for pancreatic cancer detection. J Nucl Med 55:989–994

Man YK, DiCara D, Chan N, Vessillier S, Mather SJ, Rowe ML, Howard MJ, Marshall JF, Nissim A (2013) Structural guided scaffold phage display libraries as a source of bio-therapeutics. PLoS ONE 8:e70452

Navaratnam V, Fleming KM, West J, Smith CJ, Jenkins RG, Fogarty A, Hubbard RB (2011) The rising incidence of idiopathic pulmonary fibrosis in the U.K. Thorax 66:462–467

Nothelfer EM, Zitzmann-Kolbe S, Garcia-Boy R, Kramer S, Herold-Mende C, Altmann A, Eisenhut M, Mier W, Haberkorn U (2009) Identification and characterization of a peptide with affinity to head and neck cancer. J Nucl Med 50:426–434

Pakkala M, Hekim C, Soininen P, Leinonen J, Koistinen H, Weisell J, Stenman UH, Vepsalainen J, Narvanen A (2007) Activity and stability of human kallikrein-2-specific linear and cyclic peptide inhibitors. J Pept Sci 13:348–353

Patsenker E, Popov Y, Stickel F, Jonczyk A, Goodman SL, Schuppan D (2008) Inhibition of integrin alphavbeta6 on cholangiocytes blocks transforming growth factor-beta activation and retards biliary fibrosis progression. Gastroenterology 135:660–670

Peng ZW, Ikenaga N, Liu SB, Sverdlov DY, Vaid KA, Dixit R, Weinreb PH, Violette S, Sheppard D, Schuppan D, Popov Y (2016) Integrin alphavbeta6 critically regulates hepatic progenitor cell function and promotes ductular reaction, fibrosis, and tumorigenesis. Hepatology 63:217–232

Pi L, Robinson PM, Jorgensen M, Oh SH, Brown AR, Weinreb PH, Trinh TL, Yianni P, Liu C, Leask A, Violette SM, Scott EW, Schultz GS, Petersen BE (2015) Connective tissue growth factor and integrin alphavbeta6: a new pair of regulators critical for ductular reaction and biliary fibrosis in mice. Hepatology 61:678–691

Puthawala K, Hadjiangelis N, Jacoby SC, Bayongan E, Zhao Z, Yang Z, Devitt ML, Horan GS, Weinreb PH, Lukashev ME, Violette SM, Grant KS, Colarossi C, Formenti SC, Munger JS (2008) Inhibition of integrin alphavbeta6, an activator of latent transforming growth factor-beta, prevents radiation-induced lung fibrosis. Am J Respir Crit Care Med 177:82–90

Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, Colby TV, Cordier JF, Flaherty KR, Lasky JA, Lynch DA, Ryu JH, Swigris JJ, Wells AU, Ancochea J, Bouros D, Carvalho C, Costabel U, Ebina M, Hansell DM, Johkoh T, Kim DS, King TE Jr., Kondoh Y, Myers J, Müller NL, Nicholson AG, Richeldi L, Selman M, Dudden RF, Griss BS, Protzko SL, Schünemann HJ; ATS/ERS/JRS/ALAT Committee on Idiopathic Pulmonary Fibrosis (2011) An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 183:788–824

Roxin A, Zheng G (2012) Flexible or fixed: a comparative review of linear and cyclic cancer-targeting peptides. Future Med Chem 4:1601–1618

Saha A, Ellison D, Thomas GJ, Vallath S, Mather SJ, Hart IR, Marshall JF (2010) High-resolution in vivo imaging of breast cancer by targeting the pro-invasive integrin alphavbeta6. J Pathol 222:52–63

Saini G, Porte J, Weinreb PH, Violette SM, Wallace WA, McKeever TM, Jenkins G (2015) alphavbeta6 integrin may be a potential prognostic biomarker in interstitial lung disease. Eur Respir J 46:486–494

Satpati D, Hausner SH, Bauer N, Sutcliffe JL (2014) Cerenkov luminescence imaging of alphav beta6 integrin expressing tumors using (90) Y-labeled peptides. J Labelled Comp Radiopharm 57:558–565

Shi J, Wang F, Liu S (2016) Radiolabeled cyclic RGD peptides as radiotracers for tumor imaging. Biophys Rep 2:1–20

Singh AN, McGuire MJ, Li S, Hao G, Kumar A, Sun X, Brown KC (2014) Dimerization of a phage-display selected peptide for imaging of alphavbeta6- integrin: two approaches to the multivalent effect. Theranostics 4:745–760

Ueda M, Fukushima T, Ogawa K, Kimura H, Ono M, Yamaguchi T, Ikehara Y, Saji H (2014) Synthesis and evaluation of a radioiodinated peptide probe targeting alphavbeta6 integrin for the detection of pancreatic ductal adenocarcinoma. Biochem Biophys Res Commun 445:661–666

Utz JP, Ryu JH, Douglas WW, Hartman TE, Tazelaar HD, Myers JL, Allen MS, Schroeder DR (2001) High short-term mortality following lung biopsy for usual interstitial pneumonia. Eur Respir J 17:175–179

Wells AU (2013) Managing diagnostic procedures in idiopathic pulmonary fibrosis. Eur Respir Rev 22:158–162

Win T, Lambrou T, Hutton BF, Kayani I, Screaton NJ, Porter JC, Maher TM, Endozo R, Shortman RI, Lukey P, Groves AM (2012) 18F-Fluorodeoxyglucose positron emission tomography pulmonary imaging in idiopathic pulmonary fibrosis is reproducible: implications for future clinical trials. Eur J Nucl Med Mol Imaging 39:521–528

Xu MY, Porte J, Knox AJ, Weinreb PH, Maher TM, Violette SM, McAnulty RJ, Sheppard D, Jenkins G (2009) Lysophosphatidic acid induces alphavbeta6 integrin-mediated TGF-beta activation via the LPA2 receptor and the small G protein G alpha(q). Am J Pathol 174:1264–1279

Yang GY, Guo S, Dong CY, Wang XQ, Hu BY, Liu YF, Chen YW, Niu J, Dong JH (2015) Integrin alphavbeta6 sustains and promotes tumor invasive growth in colon cancer progression. World J Gastroenterol 21:7457–7467

Yu X, Wu Y, Liu H, Gao L, Sun X, Zhang C, Shi J, Zhao H, Jia B, Liu Z, Wang F (2016) Small-animal SPECT/CT of the progression and recovery of rat liver fibrosis by using an integrin alphavbeta3-targeting radiotracer. Radiology 279:502–512

Zhu X, Li J, Hong Y, Kimura RH, Ma X, Liu H, Qin C, Hu X, Hayes TR, Benny P, Gambhir SS, Cheng Z (2014) 99mTc-labeled cystine knot peptide targeting integrin alphavbeta6 for tumor SPECT imaging. Mol Pharm 11:1208–1217