Applications of atomic force microscopy in immunology
Jiping Li1, Yuying Liu2,3, Yidong Yuan1,4, Bo Huang2,3,5()
1. Beijing Smartchip Microelectronics Technology Company Limited, Beijing 100192, China 2. Department of Immunology & National Key Laboratory of Medical Molecular Biology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, School of Basic Medicine Peking Union Medical College, Beijing 100005, China 3. Clinical Immunology Center, Chinese Academy of Medical Sciences, Beijing 100005, China 4. School of Microelectronics, Tianjin University, Tianjin 300072, China 5. Department of Biochemistry & Molecular Biology, Tongji Medical College, Huazhong University of Science & Technology, Wuhan 430030, China
Cellular mechanics, a major regulating factor of cellular architecture and biological functions, responds to intrinsic stresses and extrinsic forces exerted by other cells and the extracellular matrix in the microenvironment. Cellular mechanics also acts as a fundamental mediator in complicated immune responses, such as cell migration, immune cell activation, and pathogen clearance. The principle of atomic force microscopy (AFM) and its three running modes are introduced for the mechanical characterization of living cells. The peak force tapping mode provides the most delicate and desirable virtues to collect high-resolution images of morphology and force curves. For a concrete description of AFM capabilities, three AFM applications are discussed. These applications include the dynamic progress of a neutrophil-extracellular-trap release by neutrophils, the immunological functions of macrophages, and the membrane pore formation mediated by perforin, streptolysin O, gasdermin D, or membrane attack complex.
CJ Miller, LA Davidson. The interplay between cell signalling and mechanics in developmental processes. Nat Rev Genet 2013; 14(10): 733–744 https://doi.org/10.1038/nrg3513
pmid: 24045690
HJ Butt, B Cappella, M Kappl. Force measurements with the atomic force microscope: technique, interpretation and applications. Surf Sci Rep 2005; 59(1–6): 1–152 https://doi.org/10.1016/j.surfrep.2005.08.003
5
KC Chang, YW Chiang, CH Yang, JW Liou. Atomic force microscopy in biology and biomedicine. Tzu Chi Medical J 2012; 24(4): 162–169 https://doi.org/10.1016/j.tcmj.2012.08.002
6
U Maver, T Velnar, M Gaberšček, O Planinšek, M Finšgar. Recent progressive use of atomic force microscopy in biomedical applications. Trends Analyt Chem 2016; 80: 96–111 https://doi.org/10.1016/j.trac.2016.03.014
7
Y Wu, J Cai, L Cheng, Y Xu, Z Lin, C Wang, Y Chen. Atomic force microscope tracking observation of Chinese hamster ovary cell mitosis. Micron 2006; 37(2): 139–145 https://doi.org/10.1016/j.micron.2005.08.007
pmid: 16239112
GE Atilla-Gokcumen, E Muro, J Relat-Goberna, S Sasse, A Bedigian, ML Coughlin, S Garcia-Manyes, US Eggert. Dividing cells regulate their lipid composition and localization. Cell 2014; 156(3): 428–439 https://doi.org/10.1016/j.cell.2013.12.015
pmid: 24462247
10
E Moeendarbary, AR Harris. Cell mechanics: principles, practices, and prospects. Wiley Interdiscip Rev Syst Biol Med 2014; 6(5): 371–388 https://doi.org/10.1002/wsbm.1275
pmid: 25269160
F Braet, DJ Taatjes, E Wisse. Probing the unseen structure and function of liver cells through atomic force microscopy. Semin Cell Dev Biol 2018; 73: 13–30 https://doi.org/10.1016/j.semcdb.2017.07.001
pmid: 28688930
13
F Calvo, N Ege, A Grande-Garcia, S Hooper, RP Jenkins, SI Chaudhry, K Harrington, P Williamson, E Moeendarbary, G Charras, E Sahai. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol 2013; 15(6): 637–646 https://doi.org/10.1038/ncb2756
pmid: 23708000
14
N Wang, M Zhang, Y Chang, N Niu, Y Guan, M Ye, C Li, J Tang. Directly observing alterations of morphology and mechanical properties of living cancer cells with atomic force microscopy. Talanta 2019; 191: 461–468 https://doi.org/10.1016/j.talanta.2018.09.008
pmid: 30262086
15
J Alcaraz, J Otero, I Jorba, D Navajas. Bidirectional mechanobiology between cells and their local extracellular matrix probed by atomic force microscopy. Semin Cell Dev Biol 2018; 73: 71–81 https://doi.org/10.1016/j.semcdb.2017.07.020
pmid: 28743639
A Elosegui-Artola, I Andreu, AEM Beedle, A Lezamiz, M Uroz, AJ Kosmalska, R Oria, JZ Kechagia, P Rico-Lastres, AL Le Roux, CM Shanahan, X Trepat, D Navajas, S Garcia-Manyes, P Roca-Cusachs. Force triggers YAP nuclear entry by regulating transport across nuclear pores. Cell 2017; 171(6): 1397–1410.e14 https://doi.org/10.1016/j.cell.2017.10.008
pmid: 29107331
M Krieg, AR Dunn, MB Goodman. Mechanical control of the sense of touch by β-spectrin. Nat Cell Biol 2014; 16(3): 224–233 https://doi.org/10.1038/ncb2915
pmid: 24561618
20
S El-Kirat-Chatel, YF Dufrêne. Nanoscale imaging of the Candida-macrophage interaction using correlated fluorescence-atomic force microscopy. ACS Nano 2012; 6(12): 10792–10799 https://doi.org/10.1021/nn304116f
pmid: 23146149
21
SV Pageon, MA Govendir, D Kempe, M Biro. Mechanoimmunology: molecular-scale forces govern immune cell functions. Mol Biol Cell 2018; 29(16): 1919–1926 https://doi.org/10.1091/mbc.E18-02-0120
pmid: 30088799
YB Kim, YH Ahn, JH Jung, YJ Lee, JH Lee, JL Kang. Programming of macrophages by UV-irradiated apoptotic cancer cells inhibits cancer progression and lung metastasis. Cell Mol Immunol 2019; 16(11): 851–867 https://doi.org/10.1038/s41423-019-0209-1
pmid: 30842627
24
CH Liu, H Liu, B Ge. Innate immunity in tuberculosis: host defense vs pathogen evasion. Cell Mol Immunol 2017; 14(12): 963–975 https://doi.org/10.1038/cmi.2017.88
pmid: 28890547
25
Y Li, Y Li, X Cao, X Jin, T Jin. Pattern recognition receptors in zebrafish provide functional and evolutionary insight into innate immune signaling pathways. Cell Mol Immunol 2017; 14(1): 80–89 https://doi.org/10.1038/cmi.2016.50
pmid: 27721456
26
JZ Kechagia, J Ivaska, P Roca-Cusachs. Integrins as biomechanical sensors of the microenvironment. Nat Rev Mol Cell Biol 2019; 20(8): 457–473 https://doi.org/10.1038/s41580-019-0134-2
pmid: 31182865
27
BH Hosseini, I Louban, D Djandji, GH Wabnitz, J Deeg, N Bulbuc, Y Samstag, M Gunzer, JP Spatz, GJ Hämmerling. Immune synapse formation determines interaction forces between T cells and antigen-presenting cells measured by atomic force microscopy. Proc Natl Acad Sci USA 2009; 106(42): 17852–17857 https://doi.org/10.1073/pnas.0905384106
pmid: 19822763
28
C Leung, AW Hodel, AJ Brennan, N Lukoyanova, S Tran, CM House, SC Kondos, JC Whisstock, MA Dunstone, JA Trapani, I Voskoboinik, HR Saibil, BW Hoogenboom. Real-time visualization of perforin nanopore assembly. Nat Nanotechnol 2017; 12(5): 467–473 https://doi.org/10.1038/nnano.2016.303
pmid: 28166206
29
Y Liu, T Zhang, Y Zhou, J Li, X Liang, N Zhou, J Lv, J Xie, F Cheng, Y Fang, Y Gao, N Wang, B Huang. Visualization of perforin/gasdermin/complement-formed pores in real cell membranes using atomic force microscopy. Cell Mol Immunol 2019; 16(6): 611–620 https://doi.org/10.1038/s41423-018-0165-1
pmid: 30283066
30
DE Discher, DJ Mooney, PW Zandstra. Growth factors, matrices, and forces combine and control stem cells. Science 2009; 324(5935): 1673–1677 https://doi.org/10.1126/science.1171643
pmid: 19556500
31
PH Wu, DRB Aroush, A Asnacios, WC Chen, ME Dokukin, BL Doss, P Durand-Smet, A Ekpenyong, J Guck, NV Guz, PA Janmey, JSH Lee, NM Moore, A Ott, YC Poh, R Ros, M Sander, I Sokolov, JR Staunton, N Wang, G Whyte, D Wirtz. A comparison of methods to assess cell mechanical properties. Nat Methods 2018; 15(7): 491–498 https://doi.org/10.1038/s41592-018-0015-1
pmid: 29915189
32
M Li, D Dang, L Liu, N Xi, Y Wang. Atomic force microscopy in characterizing cell mechanics for biomedical applications: a review. IEEE Trans Nanobioscience 2017; 16(6): 523–540 https://doi.org/10.1109/TNB.2017.2714462
pmid: 28613180
33
Y Zhang, F Wei, YC Poh, Q Jia, J Chen, J Chen, J Luo, W Yao, W Zhou, W Huang, F Yang, Y Zhang, N Wang. Interfacing 3D magnetic twisting cytometry with confocal fluorescence microscopy to image force responses in living cells. Nat Protoc 2017; 12(7): 1437–1450 https://doi.org/10.1038/nprot.2017.042
pmid: 28686583
34
L Sborgi, S Rühl, E Mulvihill, J Pipercevic, R Heilig, H Stahlberg, CJ Farady, DJ Müller, P Broz, S Hiller. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J 2016; 35(16): 1766–1778 https://doi.org/10.15252/embj.201694696
pmid: 27418190
35
M Pilling, P Gardner. Fundamental developments in infrared spectroscopic imaging for biomedical applications. Chem Soc Rev 2016; 45(7): 1935–1957
36
S Cazaux, A Sadoun, M Biarnes-Pelicot, M Martinez, S Obeid, P Bongrand, L Limozin, PH Puech. Synchronizing atomic force microscopy force mode and fluorescence microscopy in real time for immune cell stimulation and activation studies. Ultramicroscopy 2016; 160: 168–181 https://doi.org/10.1016/j.ultramic.2015.10.014
pmid: 26521163
37
B Knoops, S Becker, MA Poncin, J Glibert, S Derclaye, A Clippe, D Alsteens. Specific interactions measured by AFM on living cells between peroxiredoxin-5 and TLR4: relevance for mechanisms of innate immunity. Cell Chem Biol 2018; 25(5): 550–559.e3 https://doi.org/10.1016/j.chembiol.2018.02.006
pmid: 29551349
38
TA Camesano, Y Liu, M Datta. Measuring bacterial adhesion at environmental interfaces with single-cell and single-molecule techniques. Adv Water Resour 2007; 30(6–7): 1470–1491 https://doi.org/10.1016/j.advwatres.2006.05.023
39
MS Rana, HR Pota, IR Petersen. Performance of sinusoidal scanning with MPC in AFM imaging. IEEE/ASME Trans Mechatron 2015; 20(1): 73–83 https://doi.org/10.1109/TMECH.2013.2295112
40
MS Rana, HR Pota, IR Petersen. Spiral scanning with improved control for faster imaging of AFM. IEEE Trans NanoTechnol 2014; 13(3): 541–550 https://doi.org/10.1109/TNANO.2014.2309653
41
T Arildsen, CS Oxvig, PS Pedersen, J Ostergaard, T Larsen. Reconstruction algorithms in undersampled AFM imaging. IEEE J Sel Top Signal Process 2016; 10(1): 31–46 https://doi.org/10.1109/JSTSP.2015.2500363
42
C Heu, A Berquand, C Elie-Caille, L Nicod. Glyphosate-induced stiffening of HaCaT keratinocytes, a Peak Force Tapping study on living cells. J Struct Biol 2012; 178(1): 1–7 https://doi.org/10.1016/j.jsb.2012.02.007
pmid: 22369932
SM Salapaka, A Ramamoorthy, MV Salapaka. AFM imaging?Reliable or not?: validation and verification of images in atomic force microscopy. Control Systems IEEE 2013; 33(6): 106–118 https://doi.org/10.1109/MCS.2013.2279475
45
DA Smith, C Robinson, J Kirkham, J Zhang, ML Wallwork. Chemical force spectroscopy and imaging. Rev Anal Chem 2001; 20(1): 1–26 https://doi.org/10.1515/REVAC.2001.20.1.1
46
X Zhang, EP Wojcikiewicz, VT Moy. Dynamic adhesion of T lymphocytes to endothelial cells revealed by atomic force microscopy. Exp Biol Med (Maywood) 2006; 231(8): 1306–1312 https://doi.org/10.1177/153537020623100804
pmid: 16946399
47
ME Drew, AR Konicek, P Jaroenapibal, RW Carpick, Y Yamakoshi. Nanocrystalline diamond AFM tips for chemical force spectroscopy: fabrication and photochemical functionalization. J Mater Chem B Mater Biol Med 2012; 22(25): 12682–12688
48
Hyonchol K, Hideo A, Toshiya O and ATsushi I. Quantification of cell adhesion interactions by AFM: effects of LPS/PMA on the adhesion of C6 glioma cell to collagen type I. Appl Surf Sci 2002; 188(3–4): 493–498 https://doi.org/10.1016/S0169-4332(01)00978-3
E Neubert, D Meyer, F Rocca, G Günay, A Kwaczala-Tessmann, J Grandke, S Senger-Sander, C Geisler, A Egner, MP Schön, L Erpenbeck, S Kruss. Chromatin swelling drives neutrophil extracellular trap release. Nat Commun 2018; 9(1): 3767 https://doi.org/10.1038/s41467-018-06263-5
pmid: 30218080
A Diz-Muñoz, DA Fletcher, OD Weiner. Use the force: membrane tension as an organizer of cell shape and motility. Trends Cell Biol 2013; 23(2): 47–53 https://doi.org/10.1016/j.tcb.2012.09.006
pmid: 23122885
54
I Maridonneau-Parini. Control of macrophage 3D migration: a therapeutic challenge to limit tissue infiltration. Immunol Rev 2014; 262(1): 216–231 https://doi.org/10.1111/imr.12214
pmid: 25319337
A Labernadie, A Bouissou, P Delobelle, S Balor, R Voituriez, A Proag, I Fourquaux, C Thibault, C Vieu, R Poincloux, GM Charrière, I Maridonneau-Parini. Protrusion force microscopy reveals oscillatory force generation and mechanosensing activity of human macrophage podosomes. Nat Commun 2014; 5(1): 5343 https://doi.org/10.1038/ncomms6343
pmid: 25385672
57
ST Souza, LC Agra, CEA Santos, E Barreto, JM Hickmann, EJS Fonseca. Macrophage adhesion on fibronectin evokes an increase in the elastic property of the cell membrane and cytoskeleton: an atomic force microscopy study. Eur Biophys J 2014; 43(12): 573–579 https://doi.org/10.1007/s00249-014-0988-3
pmid: 25326725
58
A Labernadie, C Thibault, C Vieu, I Maridonneau-Parini, GM Charrière. Dynamics of podosome stiffness revealed by atomic force microscopy. Proc Natl Acad Sci USA 2010; 107(49): 21016–21021 https://doi.org/10.1073/pnas.1007835107
pmid: 21081699
59
B Lowin, M Hahne, C Mattmann, J Tschopp. Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways. Nature 1994; 370(6491): 650–652 https://doi.org/10.1038/370650a0
pmid: 7520535
60
D Kägi, F Vignaux, B Ledermann, K Bürki, V Depraetere, S Nagata, H Hengartner, P Golstein. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994; 265(5171): 528–530 https://doi.org/10.1126/science.7518614
pmid: 7518614
61
D Kägi, B Ledermann, K Bürki, P Seiler, B Odermatt, KJ Olsen, ER Podack, RM Zinkernagel, H Hengartner. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 1994; 369(6475): 31–37 https://doi.org/10.1038/369031a0
pmid: 8164737
62
K Baran, M Dunstone, J Chia, A Ciccone, KA Browne, CJP Clarke, N Lukoyanova, H Saibil, JC Whisstock, I Voskoboinik, JA Trapani. The molecular basis for perforin oligomerization and transmembrane pore assembly. Immunity 2009; 30(5): 684–695 https://doi.org/10.1016/j.immuni.2009.03.016
pmid: 19446473
63
J Ding, K Wang, W Liu, Y She, Q Sun, J Shi, H Sun, DC Wang, F Shao. Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 2016; 535(7610): 111–116 https://doi.org/10.1038/nature18590
pmid: 27281216
64
S Mukherjee, H Zheng, MG Derebe, KM Callenberg, CL Partch, D Rollins, DC Propheter, J Rizo, M Grabe, QX Jiang, LV Hooper. Antibacterial membrane attack by a pore-forming intestinal C-type lectin. Nature 2014; 505(7481): 103–107 https://doi.org/10.1038/nature12729
pmid: 24256734
65
R Newton, M Delguste, M Koehler, AC Dumitru, PR Laskowski, DJ Müller, D Alsteens. Combining confocal and atomic force microscopy to quantify single-virus binding to mammalian cell surfaces. Nat Protoc 2017; 12(11): 2275–2292 https://doi.org/10.1038/nprot.2017.112
pmid: 28981124
66
RH Law, N Lukoyanova, I Voskoboinik, TT Caradoc-Davies, K Baran, MA Dunstone, ME D’Angelo, EV Orlova, F Coulibaly, S Verschoor, KA Browne, A Ciccone, MJ Kuiper, PI Bird, JA Trapani, HR Saibil, JC Whisstock. The structural basis for membrane binding and pore formation by lymphocyte perforin. Nature 2010; 468(7322): 447–451 https://doi.org/10.1038/nature09518
pmid: 21037563
K Newton, KE Wickliffe, A Maltzman, DL Dugger, A Strasser, VC Pham, JR Lill, M Roose-Girma, S Warming, M Solon, H Ngu, JD Webster, VM Dixit. RIPK1 inhibits ZBP1-driven necroptosis during development. Nature 2016; 540(7631): 129–133 https://doi.org/10.1038/nature20559
pmid: 27819682
69
P Eaton, CP do Amaral, SCP Couto, MS Oliveira, AG Vasconcelos, TKS Borges, SAS Kückelhaus, JRSA Leite, MI Muniz-Junqueira. Atomic force microscopy is a potent technique to study eosinophil activation. Front Physiol 2019; 10: 1261 https://doi.org/10.3389/fphys.2019.01261
pmid: 31632296
70
X Shen, H Gu, P Ma, Z Luo, M Li, Y Hu, K Cai. Minocycline-incorporated multilayers on titanium substrates for simultaneous regulation of MSCs and macrophages. Mater Sci Eng C 2019; 102: 696–707 https://doi.org/10.1016/j.msec.2019.04.074
pmid: 31147042
71
J Pi, H Cai, F Yang, H Jin, J Liu, P Yang, J Cai. Atomic force microscopy based investigations of anti-inflammatory effects in lipopolysaccharide-stimulated macrophages. Anal Bioanal Chem 2016; 408(1): 165–176 https://doi.org/10.1007/s00216-015-9091-6
pmid: 26476923