uPAR-targeted optical imaging contrasts as theranostic agents for tumor margin detection

Theranostics

Volumn 4, Issue 1, 2014, Pages 106-118

  Yang, Lily ^a   Sajja, Hari Krishna ^a   Cao, Zehong ^a   Qian, Weiping ^a   Bender, Laura ^a   Marcus, Adam I ^a   Lipowska, Malgorzata ^a   Wood, William C ^a   Andrew Wang, Y ^b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OCEAN NANOTECH LLC   (United States)

Author keywords

And image guided surgery; Optical imaging; Theranostic nanoparticles; Tumor margin; UPAR

Indexed keywords

NANOPARTICLE; UROKINASE; UROKINASE RECEPTOR;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST TUMOR; CANCER DIAGNOSIS; CANCER PATIENT; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER STAGING; CONTRAST ENHANCEMENT; CONTROLLED STUDY; FEMALE; FLUORESCENCE IMAGING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMAGING SYSTEM; MOLECULAR IMAGING; MOUSE; NEAR INFRARED IMAGING SYSTEM; NONHUMAN; PANCREAS TUMOR; PRIMARY TUMOR; RADIODIAGNOSIS; RECEPTOR BINDING; TUMOR XENOGRAFT;

AND IMAGE-GUIDED SURGERY; OPTICAL IMAGING; THERANOSTIC NANOPARTICLES; TUMOR MARGIN; UPAR;

ANIMALS; CELL LINE, TUMOR; FEMALE; FLUORESCENT DYES; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICROSCOPY, FLUORESCENCE; NANOPARTICLES; OPTICAL IMAGING; PANCREATIC NEOPLASMS; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; RECOMBINANT PROTEINS; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84896739644     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.7409     Document Type: Article

References (60)

1. Balch GC, Mithani SK, Simpson JF, Kelley MC. Accuracy of intraoperative gross examination of surgical margin status in women undergoing partial mastectomy for breast malignancy. Am Surg. 2005;71(1): 22-7.
2. Abraham SC, Fox K, Fraker D, Solin L, Reynolds C. Sampling of grossly benign breast reexcisions: a multidisciplinary approach to assessing adequacy. Am J Surg Pathol. 1999;23(3): 316-22.
3. Sigal-Zafrani B, Lewis JS, Clough KB, et al. Histological margin assessment for breast ductal carcinoma in situ: precision and implications. Mod Pathol. 2004;17(1): 81-8.
4. Verbeke CS, Menon KV. Redefining resection margin status in pancreatic cancer. HPB. (Oxford) 2009;11(4): 282-9.
5. Howard TJ, Krug JE, Yu J, et al. A margin-negative R0 resection accomplished with minimal postoperative complications is the surgeon's contribution to long-term survival in pancreatic cancer. J Gastrointest Surg. 2006;10(10): 1338-45.
6. Lee J, Lee S, Bae Y. Multiple margin positivity of frozen section is an independent risk factor for local recurrence in breast-conserving surgery. J Breast Cancer. 2012;15(4): 420-6.
7. Jung W, Kang E, Kim SM, et al. Factors Associated with Re-excision after Breast-Conserving Surgery for Early-Stage Breast Cancer. J Breast Cancer. 2012;15(4): 412-9.
8. Chang DK, Johns AL, Merrett ND, et al. Margin clearance and outcome in resected pancreatic cancer. J Clin Oncol. 2009;27(17): 2855-62.
9. Kimbrough CW, St Hill CR, Martin RC, McMasters KM, Scoggins CR. Tumor-positive resection margins reflect an aggressive tumor biology in pancreatic cancer. J Surg Oncol. 2013;107(6): 602-7.
10. Neoptolemos JP, Stocken DD, Dunn JA, et al. Influence of resection margins on survival for patients with pancreatic cancer treated by adjuvant chemoradiation and/or chemotherapy in the ESPAC-1 randomized controlled trial. Ann Surg. 2001;234(6): 758-68.
11. Konstantinidis IT, Warshaw AL, Allen JN, et al. Pancreatic ductal adenocarcinoma: is there a survival difference for R1 resections versus locally advanced unresectable tumors? What is a "true" R0 resection? Ann Surg. 2013;257(4): 731-6.
12. Assersohn L, Powles TJ, Ashley S, et al. Local relapse in primary breast cancer patients with unexcised positive surgical margins after lumpectomy, radiotherapy and chemoendocrine therapy. Ann Oncol. 1999;10(12): 1451-5.
13. Bolger JC, Solon JG, Power C, Hill AD. Analysis of margin index as a method for predicting residual disease after breast-conserving surgery in a European cancer center. Ann Surg Oncol. 2012;19(1): 207-11.
14. Esposito I, Kleeff J, Bergmann F, et al. Most pancreatic cancer resections are R1 resections. Ann Surg Oncol. 2008;15(6): 1651-60.
15. Sahoo S, Lester SC. Pathology of breast carcinomas after neoadjuvant chemotherapy: an overview with recommendations on specimen processing and reporting. Arch Pathol Lab Med. 2009;133(4): 633-42.
16. Weissleder R, Tung CH, Mahmood U, Bogdanov A, Jr. In vivo imaging of tumors with protease-activated near-infrared fluorescent probes. Nat Biotechnol. 1999;17(4): 375-8.
17. Becker A, Hessenius C, Licha K, et al. Receptor-targeted optical imaging of tumors with near-infrared fluorescent ligands. Nat Biotechnol. 2001;19(4): 327-31.
18. Ye Y, Bloch S, Xu B, Achilefu S. Design, synthesis, and evaluation of near infrared fluorescent multimeric RGD peptides for targeting tumors. J Med Chem. 2006;49(7): 2268-75.
19. van Dam GM, Themelis G, Crane LM, et al. Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-alpha targeting: first in-human results. Nat Med. 2011;17(10): 1315-9.
20. Bradbury MS, Phillips E, Montero PH, et al. Clinically-translated silica nanoparticles as dual-modality cancer-targeted probes for image-guided surgery and interventions. Integr Biol (Camb). 2013;5(1): 74-86.
21. Keereweer S, Van Driel PB, Snoeks TJ, et al. Optical image-guided cancer surgery: challenges and limitations. Clin Cancer Res. 2013;19(14): 3745-54.
22. Vahrmeijer AL, Hutteman M, van der Vorst JR, van de Velde CJ, Frangioni JV. Image-guided cancer surgery using near-infrared fluorescence. Nat Rev Clin Oncol. 2013; Epub ahead of print. Doi: 10.1038/nrclinonc.2013.123.
23. Yang L, Mao H, Cao Z, et al. Molecular imaging of pancreatic cancer in an animal model using targeted multifunctional nanoparticles. Gastroenterology. 2009;136(5): 1514-25.
24. Nguyen QT, Olson ES, Aguilera TA, et al. Surgery with molecular fluorescence imaging using activatable cell-penetrating peptides decreases residual cancer and improves survival. Proc Natl Acad Sci U S A. 2010;107(9): 4317-22.
25. Kelly K, Alencar H, Funovics M, Mahmood U, Weissleder R. Detection of invasive colon cancer using a novel, targeted, library-derived fluorescent peptide. Cancer Res. 2004;64(17): 6247-51.
26. Ke S, Wen X, Gurfinkel M, et al. Near-infrared optical imaging of epidermal growth factor receptor in breast cancer xenografts. Cancer Res. 2003;63(22): 7870-5.
27. Yang L, Peng XH, Wang YA, et al. Receptor-targeted nanoparticles for in vivo imaging of breast cancer. Clin Cancer Res. 2009;15(14): 4722-32.
28. Yang L, Mao H, Wang YA, et al. Single chain epidermal growth factor receptor antibody conjugated nanoparticles for in vivo tumor targeting and imaging. Small. 2009;5(2): 235-43.
29. Cai W, Shin DW, Chen K, et al. Peptide-labeled near-infrared quantum dots for imaging tumor vasculature in living subjects. Nano Lett. 2006;6(4): 669-76.
30. Moore A, Medarova Z, Potthast A, Dai G. In vivo targeting of underglycosylated MUC-1 tumor antigen using a multimodal imaging probe. Cancer Res. 2004;64(5): 1821-7.
31. Blasi F, Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol. 2002;3(12): 932-43.
32. Hemsen A, Riethdorf L, Brunner N, et al. Comparative evaluation of urokinase-type plasminogen activator receptor expression in primary breast carcinomas and on metastatic tumor cells. Int J Cancer. 2003;107(6): 903-9.
33. He Y, Liu XD, Chen ZY, et al. Interaction between cancer cells and stromal fibroblasts is required for activation of the uPAR-uPA-MMP-2 cascade in pancreatic cancer metastasis. Clin Cancer Res. 2007;13(11): 3115-24.
34. Kjaergaard M, Hansen LV, Jacobsen B, Gardsvoll H, Ploug M. Structure and ligand interactions of the urokinase receptor (uPAR). Front Biosci. 2008;13: 5441-61.
35. Cantero D, Friess H, Deflorin J, et al. Enhanced expression of urokinase plasminogen activator and its receptor in pancreatic carcinoma. Br J Cancer. 1997;75(3): 388-95.
36. Solberg H, Ploug M, Hoyer-Hansen G, Nielsen BS, Lund LR. The murine receptor for urokinase-type plasminogen activator is primarily expressed in tissues actively undergoing remodeling. J Histochem Cytochem. 2001;49(2): 237-46.
37. Salden M, Splinter TA, Peters HA, et al. The urokinase-type plasminogen activator system in resected non-small-cell lung cancer. Rotterdam Oncology Thoracic Study Group. Annals of oncology : official journal of the European Society for Medical Oncology / ESMO. 2000;11(3): 327-32.
38. Kotzsch M, Bernt K, Friedrich K, et al. Prognostic relevance of tumour cell-associated uPAR expression in invasive ductal breast carcinoma. Histopathology. 2010;57(3): 461-71.
39. Nielsen BS, Rank F, Illemann M, Lund LR, Dano K. Stromal cells associated with early invasive foci in human mammary ductal carcinoma in situ coexpress urokinase and urokinase receptor. International journal of cancer. Journal international du cancer. 2007;120(10): 2086-95.
40. LeBeau AM, Duriseti S, Murphy ST, et al. Targeting uPAR with antagonistic recombinant human antibodies in aggressive breast cancer. Cancer Res. 2013;73(7): 2070-81.
41. Chen Y, Zheng B, Robbins DH, et al. Accurate discrimination of pancreatic ductal adenocarcinoma and chronic pancreatitis using multimarker expression data and samples obtained by minimally invasive fine needle aspiration. Int J Cancer. 2007;120(7): 1511-7.
42. Xue A, Scarlett CJ, Jackson CJ, Allen BJ, Smith RC. Prognostic significance of growth factors and the urokinase-type plasminogen activator system in pancreatic ductal adenocarcinoma. Pancreas. 2008;36(2): 160-7.
43. Pyke C, Graem N, Ralfkiaer E, et al. Receptor for urokinase is present in tumor-associated macrophages in ductal breast carcinoma. Cancer Res. 1993;53(8): 1911-5.
44. Hildenbrand R, Schaaf A. The urokinase-system in tumor tissue stroma of the breast and breast cancer cell invasion. Int J Oncol. 2009;34(1): 15-23.
45. Zhao Q, Jiang H, Cao Z, Yang L, Mao H, Lipowska M. A handheld fluorescence molecular tomography system for intraoperative optical imaging of tumor margins. Med Phys. 2011;38(11): 5873-8.
46. Zhou Z, Chen H, Lipowska M, et al. A dual-modal magnetic nanoparticle probe for preoperative and intraoperative mapping of sentinel lymph nodes by magnetic resonance and near infrared fluorescence imaging. J Biomater Appl. 2013;28(1): 100-11.
47. Miller FR, Santner SJ, Tait L, Dawson PJ. MCF10DCIS.com xenograft model of human comedo ductal carcinoma in situ. J Natl Cancer Inst. 2000;92(14): 1185-6.
48. Lin L, Gardsvoll H, Huai Q, Huang M, Ploug M. Structure-based engineering of species selectivity in the interaction between urokinase and its receptor: implication for preclinical cancer therapy. J Biol Chem. 2010;285(14): 10982-92.
49. Spivack B, Khanna MM, Tafra L, Juillard G, Giuliano AE. Margin status and local recurrence after breast-conserving surgery. Arch Surg. 1994;129(9): 952-6; discussion 56-7.
50. Weissleder R. Molecular imaging in cancer. Science. 2006;312(5777): 1168-71.
51. Holland JP, Normand G, Ruggiero A, Lewis JS, Grimm J. Intraoperative imaging of positron emission tomographic radiotracers using Cerenkov luminescence emissions. Mol Imaging. 2011;10(3): 177-86.
52. Ploug M. Structure-Driven Design of Radionuclide Tracers for Non-Invasive Imaging of uPAR and Targeted Radiotherapy. The Tale of a Synthetic Peptide Antagonist. Theranostics. 2013;3(7): 467-76.
53. Li Y, Wood N, Yellowlees D, Donnelly PK. Cell surface expression of urokinase receptor in normal mammary epithelial cells and breast cancer cell lines. Anticancer Res. 1999;19(2A): 1223-8.
54. Liu S, Bugge TH, Leppla SH. Targeting of tumor cells by cell surface urokinase plasminogen activator-dependent anthrax toxin. J Biol Chem. 2001;276(21): 17976-84.
55. de Virgilio M, Silvestris F. Urokinase receptor (uPAR) ligand based recombinant toxins for human cancer therapy. Curr Pharm Des. 2011;17(19): 1979-83.
56. Ploug M, Ostergaard S, Gardsvoll H, et al. Peptide-derived antagonists of the urokinase receptor. affinity maturation by combinatorial chemistry, identification of functional epitopes, and inhibitory effect on cancer cell intravasation. Biochemistry. 2001;40(40): 12157-68.
57. Berkenblit A, Matulonis UA, Kroener JF, et al. A6, a urokinase plasminogen activator (uPA)-derived peptide in patients with advanced gynecologic cancer: a phase I trial. Gynecologic oncology. 2005;99(1): 50-7.
58. O'Halloran TV, Ahn R, Hankins P, Swindell E, Mazar AP. The Many Spaces of uPAR: Delivery of Theranostic Agents and Nanobins to Multiple Tumor Compartments through a Single Target. Theranostics. 2013;3(7): 496-506.
59. Rosenblum MG, Kavanagh JJ, Burke TW, et al. Clinical pharmacology, metabolism, and tissue distribution of 90Y-labeled monoclonal antibody B72.3 after intraperitoneal administration. J Natl Cancer Inst. 1991;83(22): 1629-36.
60. Li ZB, Niu G, Wang H, et al. Imaging of urokinase-type plasminogen activator receptor expression using a 64Cu-labeled linear peptide antagonist by microPET. Clin Cancer Res. 2008;14(15): 4758-66.