Nature of T lymphocyte recognition of macrophage-associated antigens. V. Contribution of individual peptide residues of human fibrinopeptide B to T lymphocyte responses

We present a novel super-resolution fluorescence lifetime microscopy technique called generalized stepwise optical saturation (GSOS) that generalizes and extends the concept of the recently demonstrated stepwise optical saturation (SOS) super-resolution microscopy [Biomed. Opt. Express 9, 1613 (2018)29675306]. The theoretical basis of GSOS is developed based on exploring the dynamics of a two-level fluorophore model and using perturbation theory. We show that although both SOS and GSOS utilize the linear combination of M raw images to increase the imaging resolution by a factor of M, SOS is a special and the simplest case of GSOS. The super-resolution capability is demonstrated with theoretical analysis and numerical simulations for GSOS with sinusoidal and pulse-train modulations. Using GSOS with pulse-train modulation, super-resolution and fluorescence lifetime imaging microscopy (FLIM) images can be obtained simultaneously. The super-resolution FLIM capability is experimentally demonstrated with a cell sample on a custom-built two-photon frequency-domain (FD) FLIM system based on radio frequency analog signal processing. To our knowledge, this is the first implementation of super-resolution imaging in FD-FLIM.

[1]  S. Hell,et al.  Simultaneous multi-lifetime multi-color STED imaging for colocalization analyses. , 2011, Optics express.

[2]  Hans C. Gerritsen,et al.  Fluorescence Lifetime Imaging in Scanning Microscopy , 2006 .

[3]  R. Roeder,et al.  Super-resolution fluorescence microscopy by stepwise optical saturation. , 2018, Biomedical optics express.

[4]  J. Gamble,et al.  Role of major histocompatibility complex gene products in delayed-type hypersensitivity. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[5]  E. Shevach.  The function of macrophages in antigen recognition by guinea pig T lymphocytes. III. Genetic analysis of the antigens mediating macrophage-T lymphocyte interaction. , 1976, Journal of immunology.

[6]  H. Gerritsen,et al.  Multiple Time-Gate Module for Fluorescence Lifetime Imaging , 2001 .

[7]  A. Rosenthal.  Determinant Selection and Macrophage Function in Genetic Control of the Immune Response , 1978, Immunological reviews.

[8]  S. Hell.  Far-Field Optical Nanoscopy , 2007, Science.

[9]  M. Gustafsson.  Nonlinear structured-illumination microscopy: wide-field fluorescence imaging with theoretically unlimited resolution. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Lippincott-Schwartz,et al.  Imaging Intracellular Fluorescent Proteins at Nanometer Resolution , 2006, Science.

[11]  S. Schlossman,et al.  Antigen recognition: the specificity of an isolated T lymphocyte population. , 1977, Journal of immunology.

[12]  M. Stulbarg,et al.  The specificity of antigen-induced thymidine-2-14C incorporation into lymph node cells frrom sensitized animals. , 1968, Journal of immunology.

[13]  B. Benacerraf,et al.  STIMULATION OF ANTIBODY RESPONSES IN VITRO BY ANTIGEN-BEARING SYNGENEIC AND ALLOGENEIC MACROPHAGES , 1976 .

[14]  Andreas Volkmer,et al.  Molecular photobleaching kinetics of Rhodamine 6G by one- and two-photon induced confocal fluorescence microscopy. , 2005, Chemphyschem : a European journal of chemical physics and physical chemistry.

[15]  W. Webb,et al.  Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm , 1996 .

[16]  Emily A. Smith,et al.  Supercontinuum stimulated emission depletion fluorescence lifetime imaging. , 2012, The journal of physical chemistry. B.

[17]  M. Mycek,et al.  Fluorescence lifetime imaging microscopy. , 2007, Methods in cell biology.

[18]  M. Neil,et al.  Mapping Molecular Function to Biological Nanostructure: Combining Structured Illumination Microscopy with Fluorescence Lifetime Imaging (SIM + FLIM) , 2017 .

[19]  Ales Benda,et al.  Optical saturation as a versatile tool to enhance resolution in confocal microscopy. , 2009, Biophysical journal.

[20]  R. Day,et al.  Investigating protein-protein interactions in living cells using fluorescence lifetime imaging microscopy , 2011, Nature Protocols.

[21]  R. Zucker,et al.  Quality assessment of confocal microscopy slide based systems: Performance , 2006, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[22]  Stephan R. Kurtz.  Mixers as Phase Detectors , 2001 .

[23]  Yi Zheng,et al.  Two-Photon Intravital Fluorescence Lifetime Imaging of the Kidney Reveals Cell-Type Specific Metabolic Signatures. , 2017, Journal of the American Society of Nephrology : JASN.

[24]  J. Sprent,et al.  Restricted helper function of F1 hybrid T cells positively selected to heterologous erythrocytes in irradiated parental strain mice. II. Evidence for restrictions affecting helper cell induction and T-B collaboration, both mapping to the K-end of the H-2 complex , 1978, The Journal of experimental medicine.

[25]  K. Carlsson,et al.  Theoretical investigation of the signal-to-noise ratio in fluorescence lifetime imaging. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[26]  N. Tamai,et al.  Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy. , 2007, Analytical chemistry.

[27]  R. Seeger,et al.  SYNERGISTIC INTERACTION OF MACROPHAGES AND LYMPHOCYTES IN ANTIGEN-INDUCED TRANSFORMATION OF LYMPHOCYTES , 1970, The Journal of experimental medicine.

[28]  Yide Zhang,et al.  Super-sensitivity multiphoton frequency-domain fluorescence lifetime imaging microscopy. , 2016, Optics express.

[29]  Patrick Fay,et al.  Saturation-compensated measurements for fluorescence lifetime imaging microscopy. , 2017, Optics letters.

[30]  Børge Hamre,et al.  Testing Fluorescence Lifetime Standards using Two-Photon Excitation and Time-Domain Instrumentation: Rhodamine B, Coumarin 6 and Lucifer Yellow , 2014, Journal of Fluorescence.

[31]  D. Rosenstreich,et al.  Peritoneal Exudate Lymphocyte II. In Vitro Lymphocyte Proliferation Induced by Brief Exposure to Antigen , 1973 .

[32]  S. Hell,et al.  Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. , 1994, Optics letters.

[33]  J. Waldron,et al.  Antigen-induced proliferation of guinea pig lymphocytes in vitro: obligatory role of macrophages in the recognition of antigen by immune T-lymphocytes. , 1973, Journal of immunology.

[34]  E. Shevach,et al.  The Role of Ia Antigens in T Cell Activation , 1977, Immunological reviews.

[35]  Michael J Rust,et al.  Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) , 2006, Nature Methods.

[36]  W. Paul,et al.  Interaction Between Antigen‐Presenting Cells and Primed T Lymphocytes , 1978, Immunological reviews.

[37]  Satoshi Kawata,et al.  High-resolution confocal microscopy by saturated excitation of fluorescence. , 2007, Physical review letters.

[38]  M. Neil,et al.  Stimulated emission depletion microscopy with a supercontinuum source and fluorescence lifetime imaging. , 2008, Optics letters.