Imaging in the era of molecular oncology

New technologies for imaging molecules, particularly optical technologies, are increasingly being used to understand the complexity, diversity and in vivo behaviour of cancers. 'Omic' approaches are providing comprehensive 'snapshots' of biological indicators, or biomarkers, of cancer, but imaging can take this information a step further, showing the activity of these markers in vivo and how their location changes over time. Advances in experimental and clinical imaging are likely to improve how cancer is understood at a systems level and, ultimately, should enable doctors not only to locate tumours but also to assess the activity of the biological processes within these tumours and to provide 'on the spot' treatment.

[1]  R. Wagner Icones Physiologicae : tabulae physiologiam et geneseos historiam illustrantes : 3 fasc = Erläuterungstafeln zur Physiologie und Entwickelungsgeschichte / , 1839 .

[2]  W. Röntgen,et al.  ON A NEW KIND OF RAYS. , 1896 .

[3]  G. Moore,et al.  The clinical use of fluorescein in neurosurgery; the localization of brain tumors. , 1948, Journal of neurosurgery.

[4]  F. Jöbsis Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. , 1977, Science.

[5]  B. Drexler,et al.  Diaphanography in the diagnosis of breast cancer. , 1985, Radiology.

[6]  H. Iishi,et al.  Diagnosis of gastric cancers with fluorescein‐labeled monoclonal antibodies to carcinoembryonic antigen , 1989, Lasers in surgery and medicine.

[7]  H. van den Bergh,et al.  Antibody–fluorescein conjugates for photoimmunodiagnosis of human colon carcinoma in nude mice , 1991, Cancer.

[8]  B. Chance,et al.  Optical method. , 1991, Annual review of biophysics and biophysical chemistry.

[9]  C. Heusser,et al.  Immunophotodiagnosis of colon carcinomas in patients injected with fluoresceinated chimeric antibodies against carcinoembryonic antigen. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[10]  G. Ogg,et al.  Ex Vivo Staining of Metastatic Lymph Nodes by Class I Major Histocompatibility Complex Tetramers Reveals High Numbers of Antigen-experienced Tumor-specific Cytolytic T Lymphocytes , 1998, The Journal of experimental medicine.

[11]  R. Weissleder,et al.  In vivo imaging of tumors with protease-activated near-infrared fluorescent probes , 1999, Nature Biotechnology.

[12]  P. Carmeliet,et al.  Angiogenesis in cancer and other diseases , 2000, Nature.

[13]  C. Contag,et al.  Use of reporter genes for optical measurements of neoplastic disease in vivo. , 2000, Neoplasia.

[14]  Henrique Veiga-Fernandes,et al.  Response of naïve and memory CD8+ T cells to antigen stimulation in vivo , 2000, Nature Immunology.

[15]  V. Ntziachristos,et al.  Concurrent MRI and diffuse optical tomography of breast after indocyanine green enhancement. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[16]  T. Mcclanahan,et al.  Involvement of chemokine receptors in breast cancer metastasis , 2001, Nature.

[17]  R. B. Campbell,et al.  In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy , 2001, Nature Medicine.

[18]  Ralph Weissleder,et al.  Magnetic relaxation switches capable of sensing molecular interactions , 2002, Nature Biotechnology.

[19]  S S Gambhir,et al.  Noninvasive quantitative imaging of protein–protein interactions in living subjects , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Thomas L. Chenevert,et al.  Noninvasive real-time imaging of apoptosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. Weissleder,et al.  Fluorescence molecular tomography resolves protease activity in vivo , 2002, Nature Medicine.

[22]  Ralph Weissleder,et al.  Detection of dysplastic intestinal adenomas using enzyme-sensing molecular beacons in mice. , 2002, Gastroenterology.

[23]  Ralph Weissleder,et al.  Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. , 2003, The New England journal of medicine.

[24]  T. Jovin,et al.  FRET imaging , 2003, Nature Biotechnology.

[25]  P. Choyke,et al.  Imaging of angiogenesis: from microscope to clinic , 2003, Nature Medicine.

[26]  Minutes,et al.  MOLECULAR IMAGING IN DRUG DISCOVERY AND DEVELOPMENT , 2003 .

[27]  T. Mihaljevic,et al.  Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping , 2004, Nature Biotechnology.

[28]  Ricky T. Tong,et al.  Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer , 2004, Nature Medicine.

[29]  Tayyaba Hasan,et al.  Flow Cytometry : A New Method for Enumerating Circulating Cancer Cells , 2004 .

[30]  Michel Bouvier,et al.  Real-time monitoring of ubiquitination in living cells by BRET , 2004, Nature Methods.

[31]  J. Ripoll,et al.  Visualization of antitumor treatment by means of fluorescence molecular tomography with an annexin V-Cy5.5 conjugate. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  D. Hanahan,et al.  Cathepsin cysteine proteases are effectors of invasive growth and angiogenesis during multistage tumorigenesis. , 2004, Cancer cell.

[33]  George Coukos,et al.  Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival , 2004, Nature Medicine.

[34]  Alison Stopeck,et al.  Circulating tumor cells, disease progression, and survival in metastatic breast cancer. , 2004, The New England journal of medicine.

[35]  A. Mackensen,et al.  Effector function of human tumor-specific CD8 T cells in melanoma lesions: a state of local functional tolerance. , 2004, Cancer research.

[36]  Sanjiv S. Gambhir,et al.  Molecular Imaging of Drug-Modulated Protein-Protein Interactions in Living Subjects , 2004, Cancer Research.

[37]  Napoleone Ferrara,et al.  Angiogenesis as a therapeutic target , 2005, Nature.

[38]  R. Weissleder,et al.  Tomographic fluorescence mapping of tumor targets. , 2005, Cancer research.

[39]  Vasilis Ntziachristos,et al.  Looking and listening to light: the evolution of whole-body photonic imaging , 2005, Nature Biotechnology.

[40]  R. Weissleder,et al.  Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-β signals in vivo , 2005 .

[41]  Vasilis Ntziachristos,et al.  Volumetric tomography of fluorescent proteins through small animals in vivo. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  E. Cocker,et al.  Fiber-optic fluorescence imaging , 2005, Nature Methods.

[43]  Paul Fockens,et al.  New imaging techniques at colonoscopy: tissue spectroscopy and narrow band imaging. , 2005, Gastrointestinal endoscopy clinics of North America.

[44]  B. Cravatt,et al.  Protein-reactive natural products. , 2005, Angewandte Chemie.

[45]  Hans Auler,et al.  Untersuchungen über die Rolle der Porphyrine bei geschwulstkranken Menschen und Tieren , 1942, Zeitschrift für Krebsforschung.

[46]  Vasilis Ntziachristos,et al.  Use of gene expression profiling to direct in vivo molecular imaging of lung cancer. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[47]  C. Halin,et al.  In vivo imaging of lymphocyte trafficking. , 2005, Annual review of cell and developmental biology.

[48]  R. Weissleder,et al.  Cell-specific targeting of nanoparticles by multivalent attachment of small molecules , 2005, Nature Biotechnology.

[49]  Wolfgang A Weber,et al.  Prediction of response to neoadjuvant chemotherapy by sequential F-18-fluorodeoxyglucose positron emission tomography in patients with advanced-stage ovarian cancer. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[50]  Dennis C. Sgroi,et al.  Stromal Fibroblasts Present in Invasive Human Breast Carcinomas Promote Tumor Growth and Angiogenesis through Elevated SDF-1/CXCL12 Secretion , 2005, Cell.

[51]  R. Jain Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy , 2005, Science.

[52]  Sanjiv S Gambhir,et al.  FDG-PET and beyond: molecular breast cancer imaging. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[53]  D. Piwnica-Worms,et al.  Spying on cancer: molecular imaging in vivo with genetically encoded reporters. , 2005, Cancer cell.

[54]  Conor L Evans,et al.  Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[55]  R. Tsien,et al.  The Fluorescent Toolbox for Assessing Protein Location and Function , 2006, Science.

[56]  R. Weissleder,et al.  Near infrared thoracoscopy of tumoral protease activity for improved detection of peripheral lung cancer , 2006, International journal of cancer.

[57]  F. Blankenberg,et al.  Radiolabeling of HYNIC–annexin V with technetium-99m for in vivo imaging of apoptosis , 2006, Nature Protocols.

[58]  Lihong V. Wang,et al.  Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging , 2006, Nature Biotechnology.

[59]  Ralph Weissleder,et al.  A macrophage-targeted theranostic nanoparticle for biomedical applications. , 2006, Small.

[60]  J. Bulte Intracellular endosomal magnetic labeling of cells. , 2006, Methods in molecular medicine.

[61]  Lai Guan Ng,et al.  Random migration precedes stable target cell interactions of tumor-infiltrating T cells , 2006, The Journal of experimental medicine.

[62]  J. Frank,et al.  Cellular magnetic resonance imaging: current status and future prospects , 2006, Expert review of medical devices.

[63]  Ralf Eberhardt,et al.  The Future of Bronchoscopy in Diagnosing, Staging and Treatment of Lung Cancer , 2006, Respiration.

[64]  Ralph Weissleder,et al.  Regulatory T cells reversibly suppress cytotoxic T cell function independent of effector differentiation. , 2006, Immunity.

[65]  John A. Evans,et al.  Comprehensive volumetric optical microscopy in vivo , 2006, Nature Medicine.

[66]  K. Brindle,et al.  Assessing responses to cancer therapy using molecular imaging. , 2006, Biochimica et biophysica acta.

[67]  Thierry Boon,et al.  Human T cell responses against melanoma. , 2006, Annual review of immunology.

[68]  P. Chattopadhyay,et al.  Live-cell assay to detect antigen-specific CD4+ T-cell responses by CD154 expression , 2006, Nature Protocols.

[69]  B. Bouma,et al.  Three-dimensional miniature endoscopy , 2006, Nature.

[70]  G. Feng,et al.  Next-Generation Optical Technologies for Illuminating Genetically Targeted Brain Circuits , 2006, The Journal of Neuroscience.

[71]  R. Weissleder,et al.  Labeling of immune cells for in vivo imaging using magnetofluorescent nanoparticles , 2006, Nature Protocols.

[72]  Ralph Weissleder,et al.  In vivo imaging of molecularly targeted phage. , 2006, Neoplasia.

[73]  R. Kiesslich,et al.  Technology Insight: confocal laser endoscopy for in vivo diagnosis of colorectal cancer , 2007, Nature Clinical Practice Oncology.

[74]  B. Ross,et al.  Noninvasive Molecular Imaging Sheds Light on the Synergy between 5-Fluorouracil and TRAIL/Apo2L for Cancer Therapy , 2007, Clinical Cancer Research.

[75]  Philip S Low,et al.  In vivo quantitation of rare circulating tumor cells by multiphoton intravital flow cytometry , 2007, Proceedings of the National Academy of Sciences.

[76]  Sebastian Amigorena,et al.  In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor , 2007, The Journal of experimental medicine.

[77]  F. Peale,et al.  Bv8 regulates myeloid-cell-dependent tumour angiogenesis , 2007, Nature.

[78]  T. Jacks,et al.  Restoration of p53 function leads to tumour regression in vivo , 2007, Nature.

[79]  Ross Tubo,et al.  Mesenchymal stem cells within tumour stroma promote breast cancer metastasis , 2007, Nature.

[80]  G. Evan,et al.  Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors , 2007, Nature Medicine.

[81]  Yarong Wang,et al.  Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. , 2007, Cancer research.

[82]  Charles P. Lin,et al.  Portable two-color in vivo flow cytometer for real-time detection of fluorescently-labeled circulating cells. , 2007, Journal of biomedical optics.

[83]  R. Weissleder,et al.  A Near-Infrared Cell Tracker Reagent for Multiscopic In Vivo Imaging and Quantification of Leukocyte Immune Responses , 2007, PloS one.

[84]  P. Choyke,et al.  Spectral Fluorescence Molecular Imaging of Lung Metastases Targeting HER2/neu , 2007, Clinical Cancer Research.

[85]  Wolfgang A Weber,et al.  PET to assess early metabolic response and to guide treatment of adenocarcinoma of the oesophagogastric junction: the MUNICON phase II trial. , 2007, The Lancet. Oncology.

[86]  Young L. Kim,et al.  Optical Markers in Duodenal Mucosa Predict the Presence of Pancreatic Cancer , 2007, Clinical Cancer Research.

[87]  B. Imperiali,et al.  Fluorogenic probes for monitoring peptide binding to class II MHC proteins in living cells. , 2007, Nature chemical biology.

[88]  F. Braet,et al.  Moving in the right direction—Nanoimaging in cancer cell motility and metastasis , 2007, Microscopy research and technique.

[89]  K. Gupta,et al.  Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer , 2007, Nature Medicine.

[90]  Michal Neeman,et al.  In vivo imaging of the systemic recruitment of fibroblasts to the angiogenic rim of ovarian carcinoma tumors. , 2007, Cancer research.

[91]  R. Weissleder,et al.  In vivo imaging of T cell delivery to tumors after adoptive transfer therapy , 2007, Proceedings of the National Academy of Sciences.

[92]  S. Digumarthy,et al.  Isolation of rare circulating tumour cells in cancer patients by microchip technology , 2007, Nature.

[93]  T. Jovin,et al.  Fluorescence imaging of amyloid formation in living cells by a functional, tetracysteine-tagged α-synuclein , 2007, Nature Methods.

[94]  Jan Grimm,et al.  A spatially and temporally restricted mouse model of soft tissue sarcoma , 2007, Nature Medicine.

[95]  John Condeelis,et al.  The cofilin pathway in breast cancer invasion and metastasis , 2007, Nature Reviews Cancer.

[96]  Kevin Brindle,et al.  New approaches for imaging tumour responses to treatment , 2008, Nature Reviews Cancer.

[97]  D. Carbone,et al.  Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. , 2008, Cancer cell.

[98]  R. DePinho,et al.  Targeted Nanoparticles for Imaging Incipient Pancreatic Ductal Adenocarcinoma , 2007, PLoS medicine.

[99]  Donhee Ham,et al.  Chip–NMR biosensor for detection and molecular analysis of cells , 2008, Nature Medicine.