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Applications of AFM Cellular and Molecular Biophysical Detection in Clinical Lymphoma Rituximab Treatment

Chapter
Part of the Springer Theses book series (Springer Theses)

Abstract

Biomedical applications of AFM single-cell and single-molecule detection on lymphoma rituximab targeted therapy were investigated. At the single-cell level, the morphological and mechanical changes on single lymphoma cells during the three killing mechanisms (PCD, ADCC, CDC) of rituximab were revealed. Primary cancerous cells and effector cells from the bone marrow of clinical lymphoma patients were identified by the cell surface specific biomarker fluorescence recognition. At the single-molecule level, two types of molecular interactions (CD20-rituximab, FcR-rituximab) involved in rituximab’s mechanisms were measured and correlated with the clinical rituximab therapeutic outcomes, showing the close links between molecular properties and rituximab efficacies.

References

  1. 1.
    Li M, Liu L, Xi N et al (2011) Imaging and measuring the rituximab-induced changes of mechanical properties in B-lymphoma cells using atomic force microscopy. Biochem Biophys Res Commun 404:689–694CrossRefGoogle Scholar
  2. 2.
    Li M, Liu L, Xi N et al (2012) Drug-induced changes of topography and elasticity in living B lymphoma cells based on atomic force microscopy. Acta Phys Chim Sin 28:1502–1508Google Scholar
  3. 3.
    Li M, Liu L, Xi N et al (2016) Applications of atomic force microscopy in exploring drug actions in lymphoma-targeted therapy at the nanoscale. Bionanoscience 6:22–32ADSCrossRefGoogle Scholar
  4. 4.
    Hu M, Wang J, Zhao H et al (2009) Nanostructure and nanomechanics analysis of lymphocyte using AFM: from resting, activated to apoptosis. J Biomech 42:1513–1519CrossRefGoogle Scholar
  5. 5.
    Cai X, Yang X, Cai J et al (2010) Atomic force microscope-related study membrane-associated cytotoxicity in human pterygium fibroblasts induced by mitomycin C. J Phys Chem B 114:3833–3839CrossRefGoogle Scholar
  6. 6.
    Beers SA, Chan CHT, French RR et al (2010) CD20 as a target for therapeutic type I and II monoclonal antibodies. Semin Hematol 47:107–114CrossRefGoogle Scholar
  7. 7.
    El-Kirat-Chatel S, Dufrene YF (2012) Nanoscale imaging of the candida-macrophage interaction using correlated fluorescence-atomic force microscopy. ACS Nano 6:10792–10799Google Scholar
  8. 8.
    May RC, Machesky LM (2001) Phagocytosis and the actin cytoskeleton. J Cell Sci 114:1061–1077Google Scholar
  9. 9.
    McEarchern JA, Oflazoglu E, Francisco L et al (2007) Engineered anti-CD70 antibody with multiple effector functions exhibits in vitro and in vivo antitumor activities. Blood 109:1185–1192CrossRefGoogle Scholar
  10. 10.
    Beers SA, French RR, Chan HTC et al (2010) Antigenic modulation limits the efficacy of anti-CD20 antibodies: implications for antibody selection. Blood 115:5191–5201CrossRefGoogle Scholar
  11. 11.
    Chen YY, Wu CC, Hsu JL et al (2009) Surface rigidity change of Escherichia coli after filamentous bacteriophage infection. Langmuir 25:4607–4614CrossRefGoogle Scholar
  12. 12.
    Ohnesorge FM, Horber JKH, Haberle W et al (1997) AFM review study on pox viruses and living cells. Biophys J 73:2183–2194CrossRefGoogle Scholar
  13. 13.
    Mogilner A, Keren K (2009) The shape of motile cells. Curr Biol 19:R762–R771CrossRefGoogle Scholar
  14. 14.
    Keren K, Pincus Z, Allen GM et al (2008) Mechanism of shape determination in motile cells. Nature 453:475–480ADSCrossRefGoogle Scholar
  15. 15.
    Pham T, Mero P, Booth JW (2011) Dynamic of macrophage trogocytosis of rituximab-coated B cells. Plos One 6:e14498ADSCrossRefGoogle Scholar
  16. 16.
    Pollard TD (2003) The cytoskeleton, cellular motility and the reductionist agenda. Nature 422:741–745ADSCrossRefGoogle Scholar
  17. 17.
    Kagiwada H, Nakamura C, Kihara T et al (2010) The mechanical properties of a cell, as determined by its actin cytoskeleton, are important for nanoneedle insertion into a living cell. Cytoskeleton 67:496–503CrossRefGoogle Scholar
  18. 18.
    Greenberg S, Grinstein S (2002) Phagocytosis and innate immunity. Curr Opin Immunol 14:136–145CrossRefGoogle Scholar
  19. 19.
    Li M, Liu L, Xi N et al (2014) Nanoscale imaging and morphological analysis of Fc receptor-mediated macrophage phagocytosis against cancer cells. Langmuir 30:1609–1621CrossRefGoogle Scholar
  20. 20.
    Manches O, Lui G, Chaperot L et al (2003) In vitro mechanisms of action of rituximab on primary non-Hodgkin lymphomas. Blood 101:949–954CrossRefGoogle Scholar
  21. 21.
    Adams GP, Weiner LM (2005) Monoclonal antibody therapy of cancer. Nat Biotechnol 23:1147–1157CrossRefGoogle Scholar
  22. 22.
    Manches O, Lui G, Chaperot L et al (2003) In vitro mechanisms of action of rituximab on primary non-Hodgkin lymphomas. Blood 101:949–954CrossRefGoogle Scholar
  23. 23.
    Shan D, Ledbetter JA, Press OW (1998) Apoptosis of malignant human B cells by ligation of CD20 with monoclonal antibodies. Blood 91:1644–1652Google Scholar
  24. 24.
    Li M, Liu L, Xi N et al (2015) Quantitative analysis of drug-induced complement-mediated cytotoxic effect on single tumor cells using atomic force microscopy and fluorescence microscopy. IEEE Trans Nanobiosci 14:84–94CrossRefGoogle Scholar
  25. 25.
    Tegla CA, Cudrici C, Patel S et al (2011) Membrane attack by complement: the assembly and biology of terminal complement complexes. Immunol Res 51:45–60CrossRefGoogle Scholar
  26. 26.
    Weiland MH, Qian Y, Sodetz JM (2014) Membrane pore formation by human complement: functional importance of the transmembrane β-hairpin (TMH) segments of C8α and C9. Mol Immunol 57:310–316CrossRefGoogle Scholar
  27. 27.
    Tschopp J, Podack ER, Muller-Eberhard HJ (1982) Ultrastructure of the membrane attack complex of complement: detection of the tetramolecular C9-polymerizing complex C5b-8. Proc Natl Acad Sci USA 79:7474–7478ADSCrossRefGoogle Scholar
  28. 28.
    Cuerrier CM, Lebel R, Grandbois M (2007) Single cell transfection using plasmid decorated AFM probes. Biochem Biophys Res Commun 355:632–636CrossRefGoogle Scholar
  29. 29.
    Vakarelski IU, Brown SC, Higashitani K et al (2007) Penetration of living cell membranes with fortified carbon nanotube tips. Langmuir 23:10893–10896CrossRefGoogle Scholar
  30. 30.
    Lam WA, Rosenbluth MJ, Fletcher DA (2007) Chemotherapy exposure increases leukemia cell stiffness. Blood 109:3505–3508CrossRefGoogle Scholar
  31. 31.
    Fletcher DA, Mullins RD (2010) Cell mechanics and the cytoskeleton. Nature 463:485–492ADSCrossRefGoogle Scholar
  32. 32.
    Lombardi ML, Lammerding J (2010) Altered mechanical properties of the nucleus in disease. Methods Cell Biol 98:121–141CrossRefGoogle Scholar
  33. 33.
    Yamada KM, Cukierman E (2007) Modeling tissue morphogenesis and cancer in 3D. Cell 130:601–610CrossRefGoogle Scholar
  34. 34.
    Li M, Xiao X, Liu L et al (2013) Atomic force microscopy study of the antigen-antibody binding force on patient cancer cells based on ROR1 fluorescence recognition. J Mol Recognit 26:432–438CrossRefGoogle Scholar
  35. 35.
    Humburg MA, Collins FS (2010) The path to personalized medicine. N Engl J Med 363:301–304CrossRefGoogle Scholar
  36. 36.
    Li M, Xiao X, Liu L et al (2013) Nanoscale mapping and organization analysis of target proteins on cancer cells from B-cell lymphoma patients. Exp Cell Res 319:2812–2821CrossRefGoogle Scholar
  37. 37.
    Baskar S, Kwong K, Hofer T et al (2008) Unique cell surface expression of receptor tyrosine kinase ROR1 in human B-cell chronic lymphocytic leukemia. Clin Cancer Res 14:396–404CrossRefGoogle Scholar
  38. 38.
    Fukuda T, Chen L, Endo T et al (2008) Antisera induced by infusions of autologous Ad-CD154-leukemia B cells identify ROR1 as an oncofetal antigen and receptor for Wnt5a. Proc Natl Acad Sci USA 105:3047–3052ADSCrossRefGoogle Scholar
  39. 39.
    Uhrmacher S, Schmidt C, Erdfelder F et al (2011) Use of the receptor tyrosine kinase-orphan receptor 1(ROR1) as a diagnostic tool in chronic lymphocytic leukemia (CLL). Leuk Res 35:1360–1366CrossRefGoogle Scholar
  40. 40.
    Barna G, Mihalik R, Timar B et al (2011) ROR1 expression is not a unique marker of CLL. Hematol Oncol 29:17–21CrossRefGoogle Scholar
  41. 41.
    Bicocca VT, Chang BH, Masouleh BK et al (2012) Crosstalk between ROR1 and the pre-B cell receptor promotes survival of t (1;19) acute lymphoblastic leukemia. Cancer Cell 22:656–667CrossRefGoogle Scholar
  42. 42.
    Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70CrossRefGoogle Scholar
  43. 43.
    Hinterdorfer P, Dufrene YF (2006) Detection and localization of single molecular recognition events using atomic force microscopy. Nat Methods 3:347–355CrossRefGoogle Scholar
  44. 44.
    Lee CK, Wang YM, Huang LS et al (2007) Atomic force microscopy: determining of unbinding force, off rate and energy barrier for protein-ligand interaction. Micron 38:446–461CrossRefGoogle Scholar
  45. 45.
    Sanchez SA, Tricerri MA, Gratton E (2012) Laurden generalized polarization fluctuations measures membrane packing micro-heterogeneity in vivo. Proc Natl Acad Sci USA 109:7314–7319ADSCrossRefGoogle Scholar
  46. 46.
    Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50ADSCrossRefGoogle Scholar
  47. 47.
    Casuso I, Khao J, Chami M et al (2012) Characterization of the motion of membrane proteins using high-speed atomic force microscopy. Nat Nanotechnol 7:525–529ADSCrossRefGoogle Scholar
  48. 48.
    McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodeling. Nature 438:590–596ADSCrossRefGoogle Scholar
  49. 49.
    Dufrene YF, Evans E, Engel A et al (2011) Five challenges to bringing single-molecule force spectroscopy into living cells. Nat Methods 8:123–127CrossRefGoogle Scholar
  50. 50.
    Nimmerjahn F, Ravetch JV (2008) Fc receptors as regulators of immune response. Nat Rev Immunol 8:34–47CrossRefGoogle Scholar
  51. 51.
    Nimmerjahn F, Ravetch JV (2006) Fc receptors: old friends and new family members. Immunity 24:19–28CrossRefGoogle Scholar
  52. 52.
    Weiner LM, Murray JC, Shuprine CW (2012) Antibody-based immunotherapy of cancer. Cell 148:1081–1084CrossRefGoogle Scholar
  53. 53.
    Pham T, Mero P, Booth JW (2011) Dynamics of macrophage trogocytosis of rituximab-coated B cells. PLoS ONE 6:e14498ADSCrossRefGoogle Scholar
  54. 54.
    Shi X, Xu L, Yu J et al (2009) Study of inhibition effect of Herceptin on interaction between Heregulin and ErbB receptors HER3/HER2 by single-molecule force spectroscopy. Exp Cell Res 315:2847–2855CrossRefGoogle Scholar
  55. 55.
    Bell GI (1978) Models for the specific adhesion of cells to cells. Science 200:618–627ADSCrossRefGoogle Scholar
  56. 56.
    Evans E, Ritchie K (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72:1541–1555CrossRefGoogle Scholar
  57. 57.
    Medalsy ID, Muller DJ (2013) Nanomechanical properties of proteins and membranes depend on loading rate and electrostatic interactions. ACS Nano 7:2642–2650CrossRefGoogle Scholar
  58. 58.
    Zhang X, Shi X, Xu L et al (2013) Atomic force microscopy study of the effect of HER2 antibody on EGF mediated ErbB ligand-receptor interaction. Nanomedicine 9:627–635CrossRefGoogle Scholar
  59. 59.
    Jaron-Mendelson M, Yossef R, Appel MY et al (2012) Dimerization of NKp46 receptor is essential for NKp46-mediated lysis: characterization of the dimerization site by epitope mapping. J Immunol 188:6165–6174CrossRefGoogle Scholar
  60. 60.
    Mselle TF, Howell AL, Ghosh M et al (2009) Human uterine natural killer cells but not blood natural killer cells inhibit human immunodeficiency virus type 1 infection by secretion of CXCL12. J Virol 83:11188–11195CrossRefGoogle Scholar
  61. 61.
    Silva MRG, Hoffman R, Srour EF et al (1994) Generation of human natural killer cells from immature progenitors does not require marrow stromal cells. Blood 84:841–846Google Scholar
  62. 62.
    Santo JPD, Vosshenrich CAJ (2006) Bone marrow versus thymic pathways of natural killer cell development. Immunol Rev 214:35–46CrossRefGoogle Scholar
  63. 63.
    Li M, Liu L, Xi N et al (2013) Imaging and measuring the biophysical properties of Fc gamma receptors on single macrophages using atomic force microscopy. Biochem Biophys Res Commun 438:709–714CrossRefGoogle Scholar
  64. 64.
    Li M, Xiao X, Zhang W et al (2014) AFM analysis of the multiple types of molecular interactions involved in rituximab lymphma therapy on patient tumor cells and NK cells. Cell Immunol 290:233–244CrossRefGoogle Scholar
  65. 65.
    Li M, Xiao X, Zhang W et al (2014) Nanoscale distribution of CD20 on B-cell lymphoma tumour cells and its potential role in the clinical efficacy of rituximab. J Microsc 254:19–30CrossRefGoogle Scholar
  66. 66.
    Tan L, Lin P, Chisti MM et al (2013) Real time analysis of binding between rituxima (anti-CD20 antibody) and B lymphoma cells. Anal Chem 85:8543–8551CrossRefGoogle Scholar
  67. 67.
    Smith MR (2003) Rituximab (monoclonal anti-CD20 antibody): mechanisms of action and resistance. Oncogene 22:7359–7368CrossRefGoogle Scholar
  68. 68.
    Silverman GJ, Weisman S (2003) Rituximab therapy and autoimmune disorders: prospects for anti-B cell therapy. Arthritis Rheum 48:1484–1492CrossRefGoogle Scholar
  69. 69.
    Galon J, Robertson MW, Galinha A et al (1997) Affinity of the interaction between Fc gamma receptor type III (FcγRIII) and monomeric human IgG subclasses role of FcγRIII glycosylation. Eur J Immunol 27:1928–1932CrossRefGoogle Scholar
  70. 70.
    Bruhns P, Iannascoli B, England P et al (2009) Specificity and affinity of human Fcγ receptors and their polymorphic variants for human IgG subclasses. Blood 113:3716–3725CrossRefGoogle Scholar
  71. 71.
    Maloney DG (2012) Anti-CD20 antibody therapy for B-cell lymphomas. N Engl J Med 366:2008–2016CrossRefGoogle Scholar
  72. 72.
    Fernandez-Segura E, Garcia JM, Lopez-Escamez JA et al (1994) Surface expression and distribution of Fc receptor III (CD16 molecule) on human natural killer cells and polymorphonuclear neutrophils. Microsc Res Tech 28:277–285CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Robotics, Shenyang Institute of AutomationChinese Academy of SciencesShenyangChina

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