Dynamic changes in the cell membrane on three dimensional low coherent quantitative phase microscopy (3D LC-QPM) after treatment with the near infrared photoimmunotherapy

Near infrared photoimmunotherapy (NIR-PIT) is a newly developed cancer therapy that relies on the binding of a near-infrared antibody photoabsorber conjugate (APC) to a cancer cell. Subsequent exposure to NIR light selectively induces rapid necrotic cell death on target-expressing cells with minimal off-target effects. When treated with NIR-PIT, targeted cells become swollen, develop blebs and burst within minutes of light exposure. Detailed spatial and temporal morphological changes of the cellular membrane of targeted cells treated with NIR-PIT have not been fully explored with state-of-the-art microscopic methods. In this study, we investigated the morphologic and kinetic effects of PIT on two types of cells, a spindle-shaped 3T3/Her cell and a spheric-shaped MDA-MB468 cell, after NIR-PIT using three-dimensional low-coherent quantitative phase microscopy (3D LC-QPM). Adhesive cells treated with NIR-PIT demonstrated region-specific cell membrane rupture occurring first on the distal free edge of the cell near the site of adhesion, in a process that was independent of cell shape. The results show that the peripheral portions of the cell membrane near the site of adhesion are particularly vulnerable to the effects of NIR-PIT, likely because these sites exhibit higher baseline surface tension.

[1]  M. Bouvet,et al.  GFP labeling kinetics of triple-negative human breast cancer by a killer-reporter adenovirus in 3D Gelfoam® histoculture , 2017, In Vitro Cellular & Developmental Biology - Animal.

[2]  L. Zitvogel,et al.  Immunogenic cell death in cancer and infectious disease , 2016, Nature Reviews Immunology.

[3]  Peter L. Choyke,et al.  Immunogenic cancer cell death selectively induced by near infrared photoimmunotherapy initiates host tumor immunity , 2017, Oncotarget.

[4]  P. Choyke,et al.  Near infrared photoimmunotherapy of B‐cell lymphoma , 2016, Molecular oncology.

[5]  D. Speiser,et al.  Regulatory circuits of T cell function in cancer , 2016, Nature Reviews Immunology.

[6]  P. Choyke,et al.  Spatially selective depletion of tumor-associated regulatory T cells with near-infrared photoimmunotherapy , 2016, Science Translational Medicine.

[7]  P. Choyke,et al.  Alterations of filopodia by near infrared photoimmunotherapy: evaluation with 3D low-coherent quantitative phase microscopy. , 2016, Biomedical optics express.

[8]  P. Choyke,et al.  MR imaging biomarkers for evaluating therapeutic effects shortly after near infrared photoimmunotherapy , 2016, Oncotarget.

[9]  P. Choyke,et al.  Near Infrared Photoimmunotherapy Targeting EGFR Positive Triple Negative Breast Cancer: Optimizing the Conjugate-Light Regimen , 2015, PloS one.

[10]  M. Bouvet,et al.  Traditional Chinese medicine herbal mixture LQ arrests FUCCI-expressing HeLa cells in G0/G1 phase in 2D plastic, 2.5D Matrigel®, and 3D Gelfoam® culture visualized with FUCCI imaging , 2015, Oncotarget.

[11]  M. Bouvet,et al.  Cancer cells mimic in vivo spatial-temporal cell-cycle phase distribution and chemosensitivity in 3-dimensional Gelfoam® histoculture but not 2-dimensional culture as visualized with real-time FUCCI imaging , 2015, Cell cycle.

[12]  P. Choyke,et al.  Photoimmunotherapy of Gastric Cancer Peritoneal Carcinomatosis in a Mouse Model , 2014, PloS one.

[13]  N. Sugimoto,et al.  3‐Dimensional Tissue Is Formed From Cancer Cells In Vitro on Gelfoam®, But Not on MatrigelTM , 2014, Journal of cellular biochemistry.

[14]  I. Endo,et al.  Fluorescent proteins enhance UVC PDT of cancer cells. , 2012, Anticancer research.

[15]  Hisataka Kobayashi,et al.  Immediate in vivo target-specific cancer cell death after near infrared photoimmunotherapy , 2012, BMC Cancer.

[16]  R. Weichselbaum,et al.  A downside to apoptosis in cancer therapy? , 2011, Nature Medicine.

[17]  A. Jimeno,et al.  Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy , 2011, Nature Medicine.

[18]  Hisataka Kobayashi,et al.  Cancer Cell-Selective In Vivo Near Infrared Photoimmunotherapy Targeting Specific Membrane Molecules , 2011, Nature Medicine.

[19]  Yutaka Yamashita,et al.  Label-free imaging of intracellular motility by low-coherent quantitative phase microscopy. , 2011, Optics express.

[20]  M. Miwa,et al.  Low-coherent quantitative phase microscope for nanometer-scale measurement of living cells morphology. , 2008, Optics express.

[21]  L. Zitvogel,et al.  Molecular determinants of immunogenic cell death: surface exposure of calreticulin makes the difference , 2007, Journal of Molecular Medicine.

[22]  E. Manders,et al.  Controlled light-exposure microscopy reduces photobleaching and phototoxicity in fluorescence live-cell imaging , 2007, Nature Biotechnology.

[23]  L. Mahadevan,et al.  Non-equilibration of hydrostatic pressure in blebbing cells , 2005, Nature.

[24]  P. Mcneil,et al.  Plasma membrane disruption: repair, prevention, adaptation. , 2003, Annual review of cell and developmental biology.

[25]  Ram Dixit,et al.  Cell damage and reactive oxygen species production induced by fluorescence microscopy: effect on mitosis and guidelines for non-invasive fluorescence microscopy. , 2003, The Plant journal : for cell and molecular biology.

[26]  Erik Sahai,et al.  Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis , 2003, Nature Cell Biology.

[27]  R. Jain,et al.  Photodynamic therapy for cancer , 2003, Nature Reviews Cancer.

[28]  G. Snow,et al.  Basic principles, applications in oncology and improved selectivity of photodynamic therapy. , 2003, Anticancer research.

[29]  W. Bubb,et al.  Singlet Oxygen–mediated Protein Oxidation: Evidence for the Formation of Reactive Side Chain Peroxides on Tyrosine Residues ¶ , 2002, Photochemistry and photobiology.

[30]  C. Morris,et al.  Cell Surface Area Regulation and Membrane Tension , 2001, The Journal of Membrane Biology.

[31]  Jason C. Mills,et al.  Apoptotic Membrane Blebbing Is Regulated by Myosin Light Chain Phosphorylation , 1998, The Journal of cell biology.

[32]  C C Cunningham,et al.  Actin polymerization and intracellular solvent flow in cell surface blebbing , 1995, The Journal of cell biology.

[33]  G. Kroemer.  The pharmacology of T cell apoptosis. , 1995, Advances in immunology.

[34]  P. Janmey,et al.  Actin-binding protein requirement for cortical stability and efficient locomotion. , 1992, Science.