Multiplexed single-molecule force spectroscopy for dissecting biophysical regulation of membrane receptors functions on live cells

Chenyi An; Wei Chen

doi:10.52601/bpr.2021.210022

Volume 7 Issue 5

Oct. 2021

Turn off MathJax

Article Contents

Article Navigation > Biophysics Reports > 2021 > 7(5): 377-383

Chenyi An, Wei Chen. Multiplexed single-molecule force spectroscopy for dissecting biophysical regulation of membrane receptors functions on live cells[J]. Biophysics Reports, 2021, 7(5): 377-383. doi: 10.52601/bpr.2021.210022

Citation:

Chenyi An, Wei Chen. Multiplexed single-molecule force spectroscopy for dissecting biophysical regulation of membrane receptors functions on live cells[J]. Biophysics Reports, 2021, 7(5): 377-383. doi: 10.52601/bpr.2021.210022

Citation:

PDF (1300 KB)

Multiplexed single-molecule force spectroscopy for dissecting biophysical regulation of membrane receptors functions on live cells

doi: 10.52601/bpr.2021.210022

Chenyi An¹,
Wei Chen^{1, 2, 3
,
,}

1.
Department of Cell Biology and Department of Cardiology of the Second Affiliated Hospital, Zhejiang University School of Medicine, Zhejiang University, Hangzhou 310058, China
2.
Key Laboratory for Biomedical Engineering of Ministry of Education and State Key Laboratory for Modern Optical Instrumentation, Zhejiang University, Hangzhou 310058, China
3.
Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, Zhejiang University, Hangzhou 310058, China

Funds: This work was supported by grants from the National Basic Research Program of China (2015CB910800 and 2017ZX10203205), the National Science Foundation of China (31522021 and 31971237), the Fundamental Research Funds for the Central Universities (2015XZZX004-32), and China Postdoctoral Science Foundation (2020M681834).

More Information

Corresponding author: jackweichen@zju.edu.cn (W. Chen)
Received Date: 26 June 2021
Accepted Date: 21 July 2021
Publish Date: 31 October 2021

Abstract

Abstract

Complex physical cues including two-dimensional membrane environment, dynamic mechanical force, and bioelectric activity inevitably affect membrane receptor functions. Multiplexed single-molecule force spectroscopy (SMFS) techniques with the capability of live-cell measurements are essential to systemically dissect receptor’s functions under complex biophysical regulation. In this review, we summarize recent progress of live-cell based SMFS techniques and specifically focus on the progress of SMFS on the biomembrane force probe with enhanced mechanical stability and multiplexed capability of fluorescence imaging. We further suggest the necessity of developing multiplexed SMFS techniques with simultaneous bioelectric regulation capability to investigate membrane potential regulated membrane receptor functions. These state-of-art multiplexed SMFS techniques will dissect membrane receptors functions in a systematic biophysical angle, resolving the biochemical, biomechanical and bioelectrical regulatory mechanisms in physiologically relevant conditions.
- Multiplexed SMFS techniques,
- Membrane receptor,
- Biophysical regulation,
- Live cell

FullText(HTML)

References(52)

References

[1]	An C, Hu W, Gao J, Ju B-F, Obeidy P, Zhao YC, Tu X, Fang W, Ju LA, Chen W (2020) Ultra-stable biomembrane force probe for accurately determining slow dissociation kinetics of PD-1 blockade antibodies on single living cells. Nano Lett 20: 5133−5140 doi: 10.1021/acs.nanolett.0c01360
[2]	Arlauckas SP, Garris CS, Kohler RH, Kitaoka M, Cuccarese MF, Yang KS, Miller MA, Carlson JC, Freeman GJ, Anthony RM, Weissleder R, Pittet MJ (2017) In vivo imaging reveals a tumor-associated macrophage-mediated resistance pathway in anti-PD-1 therapy. Sci Transl Med 9: eaal3604. https://doi.org/10.1126/scitranslmed.aal3604
[3]	Bashour KT, Gondarenko A, Chen H, Shen K, Liu X, Huse M, Hone JC, Kam LC (2014) CD28 and CD3 have complementary roles in T-cell traction forces. Proc Natl Acad Sci USA 111: 2241−2246 doi: 10.1073/pnas.1315606111
[4]	Brazin KN, Mallis RJ, Boeszoermenyi A, Feng Y, Yoshizawa A, Reche PA, Kaur P, Bi K, Hussey, R E, Duke-Cohan JS, Song L, Wagner G, Arthanari H, Lang MJ, Reinherz EL (2018) The T cell antigen receptor α transmembrane domain coordinates triggering through regulation of bilayer immersion and CD3 subunit associations. Immunity 49: 1−13 doi: 10.1016/j.immuni.2018.06.014
[5]	Brinkmann U, Kontermann RE (2021) Bispecific antibodies. Science 372: 916−917 doi: 10.1126/science.abg1209
[6]	Chang F, Minc N (2014) Electrochemical control of cell and tissue polarity. Annu Rev Cell Dev Bi 30: 317−336 doi: 10.1146/annurev-cellbio-100913-013357
[7]	Chen W, Evans EA, McEver RP, Zhu C (2008) Monitoring receptor-ligand interactions between surfaces by thermal fluctuations. Biophys J 94: 694−701 doi: 10.1529/biophysj.107.117895
[8]	Chen W, Lou J, Evans EA, Zhu C (2012) Observing force-regulated conformational changes and ligand dissociation from a single integrin on cells. J Cell Biol 199: 497−512 doi: 10.1083/jcb.201201091
[9]	Chen W, Lou J, Zhu C (2010) Forcing switch from short- to intermediate- and long-lived states of the αA domain generates LFA-1/ICAM-1 catch bonds. J Biol Chem 285: 35967−35978 doi: 10.1074/jbc.M110.155770
[10]	Chen W, Zhu C (2013) Mechanical regulation of T-cell functions. Immunol Rev 256: 160−176 doi: 10.1111/imr.12122
[11]	De Gast GC, Haagen I-A, Van Houten AA, Klein SC, Duits AJ, De Weger RA, Vroom TM, Clark MR, Phillips J, Van Dijk AJG, De Lau WBM, Bast BJEG (1995) CD8 T cell activation after intravenous administration of CD3×CD19 bispecific antibody in patients with non-Hodgkin lymphoma. Cancer Immunol Immunother 40: 390−396 doi: 10.1007/BF01525390
[12]	De Vlaminck I, Henighan T, Van Loenhout MTJ, Pfeiffer I, Huijts J, Kerssemakers JWK, Katan AJ, Van Langen-Suurling A, Van Der Drift E, Wyman C, Dekker C (2011) Highly parallel magnetic tweezers by targeted DNA tethering. Nano Lett 11: 5489−5493 doi: 10.1021/nl203299e
[13]	Del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheets MP (2009) Stretching single talin rod molecules activates vinculin binding. Science 323: 638−641 doi: 10.1126/science.1162912
[14]	Drent E, Poels R, Ruiter R, Van Der Donk NWCJ, Zweegman S, Yuan H, De Bruijn J, Sadelain M, Lokhorst HM, Groen RWJ, Mutis T, Themeli M (2019) Combined CD28 and 4-1BB costimulation potentiates affinity-tuned chimeric antigen receptor-engineered T cells. Clin Cancer Res 25: 4014−4025 doi: 10.1158/1078-0432.CCR-18-2559
[15]	Feng Y, Brazin KN, Kobayashi E, Mallis RJ, Reinherz EL, Lang MJ (2017) Mechanosensing drives acuity of αβ T-cell recognition. Proc Natl Acad Sci USA 114: E8204−E8213 doi: 10.1073/pnas.1703559114
[16]	Ghorashian S, Kramer AM, Onuoha S, Wright G, Bartram J, Richardson R, Albon SJ, Casanovas-Company J, Castro F, Popova B, Villanueva K, Yeung Jenny, Vetharoy W, Guvenel A, Wawrzyniecka PA, Mekkaoui L, Cheung GW-K, Pinner D, Chu J, Lucchini G, Silva J, Ciocarlie O, Lazareva A, Inglott S, Gilmour KC, Ahsan G, Ferrari M, Manzoor S, Champion K, Brooks T, Lopes A, Hackshaw A, Farzaneh F, Chiesa R, Rao K, Bonney D, Samarasinghe S, Coulden N, Vora A, Veys P, Hough R, Wynn R, Pule MA (2019) Enhanced CAR T cell expansion and prolonged persistence in pediatric patients with ALL treated with a low-affinity CD19 CAR. Nat Med 25: 1408−1414 doi: 10.1038/s41591-019-0549-5
[17]	Guo Q, He Y, Lu HP (2015) Interrogating the activities of conformational deformed enzyme by single-molecule fluorescence-magnetic tweezers microscopy. Proc Natl Acad Sci USA 112: 13904−13909 doi: 10.1073/pnas.1506405112
[18]	Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflug Arch Eur J Phy 391: 85−100 doi: 10.1007/BF00656997
[19]	He Y, Lu M, Cao J, Lu HP (2012) Manipulating protein conformations by single-molecule AFM-FRET nanoscopy. ACS Nano 6: 1221−1229 doi: 10.1021/nn2038669
[20]	Hong J, Ge C, Jothikumar P, Yuan Z, Liu B, Bai K, Li K, Rittase W, Shinzawa M, Zhang Y, Palin A, Love P, Yu X, Salaita K, Evavold BD, Singer A, Zhu C (2018) A TCR mechanotransduction signaling loop induces negative selection in the thymus. Nat Immunol 19: 1379−1390 doi: 10.1038/s41590-018-0259-z
[21]	Hu KH, Butte MJ (2016) T cell activation requires force generation. J Cell Biol 213: 535−542 doi: 10.1083/jcb.201511053
[22]	Hu W, Zhang Y, Sun X, Zhang T, Xu L, Xie H, Li Z, Liu W, Lou J, Chen W (2019) FcγRIIB-I232T polymorphic change allosterically suppresses ligand binding. Elife 8: e46689. https://doi.org/10.7554/eLife.46689
[23]	Huang J, Zarnitsyna VI, Liu B, Edwards LJ, Jiang N, Evavold BD, Zhu C (2010) The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464: 932−936 doi: 10.1038/nature08944
[24]	Johnson KC, Thomas WE (2018) How do we know when single-molecule force spectroscopy really tests single bonds? Biophys J 114: 2032−2039 doi: 10.1016/j.bpj.2018.04.002
[25]	Ju L, Chen Y, Xue L, Du X, Zhu C (2016) Cooperative unfolding of distinctive mechanoreceptor domains transduces force into signals. Elife 5: e15447. https://doi.org/10.7554/eLife.15447
[26]	June CH, O'Connor RS, Kawalekar OU, Ghassemi S, Milone MC (2018) CAR T cell immunotherapy for human cancer. Science 359: 1361−1365 doi: 10.1126/science.aar6711
[27]	Kim ST, Takeuchi K, Sun Z-YJ, Touma M, Castro CE, Fahmy A, Lang MJ, Wagner G, Reinherz EL (2009) The αβ T cell receptor is an anisotropic mechanosensor. J Biol Chem 284: 31028−31037 doi: 10.1074/jbc.M109.052712
[28]	Kong F, Li Z, Parks WM, Dumbauld DW, Garcia AJ, Mould AP, Humphries MJ, Zhu C (2013) Cyclic mechanical reinforcement of integrin-ligand interactions. Mol Cell 49: 1060−1068 doi: 10.1016/j.molcel.2013.01.015
[29]	Labrijn AF, Janmaat ML, Reichert JM, Parren PWHI (2019) Bispecific antibodies: a mechanistic review of the pipeline. Nat Rev Drug Discov 18: 585−608 doi: 10.1038/s41573-019-0028-1
[30]	Levin M (2021) Bioelectric signaling: reprogrammable circuits underlying embryogenesis, regeneration, and cancer. Cell 184: 1971−1989 doi: 10.1016/j.cell.2021.02.034
[31]	Li R, Ma C, Cai H, Chen W (2020) The CAR T-cell mechanoimmunology at a glance. Adv Sci 7: 2002628. https://doi.org/10.1002/advs.202002628
[32]	Liu B, Chen W, Evavold BD, Zhu C (2014) Accumulation of dynamic catch bonds between TCR and agonist peptide-MHC triggers T cell signaling. Cell 157: 357−368 doi: 10.1016/j.cell.2014.02.053
[33]	Liu B, Chen W, Natarajan K, Li Z, Margulies DH, Zhu C (2015a) The cellular environment regulates in situ kinetics of T-cell receptor interaction with peptide major histocompatibility complex. Eur J Immunol 45: 2099−2110 doi: 10.1002/eji.201445358
[34]	Liu B, Chen W, Zhu C (2015b) Molecular force spectroscopy on cells. Annu Rev Phys Chem 66: 427−451 doi: 10.1146/annurev-physchem-040214-121742
[35]	Ma L, Cai Y, Li Y, Jiao J, Wu Z, O'Shaughnessy B, Camilli PD, Karatekin E, Zhang Y (2017) Single-molecule force spectroscopy of protein-membrane interactions. Elife 6: e30493. https://doi.org/10.7554/eLife.30493
[36]	Malmqvist M (1993) Surface plasmon resonance for detection and measurement of antibody-antigen affinity and kinetics. Curr Opin Immunol 5: 282−286 doi: 10.1016/0952-7915(93)90019-O
[37]	Neuman KC, Nagy A (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat Methods 5: 491−505 doi: 10.1038/nmeth.1218
[38]	Pardoll DM (2012) The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12: 252−264 doi: 10.1038/nrc3239
[39]	Porter DL, Levine BL, Kalos M, Bagg A, June CH (2016) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365: 725−733
[40]	Ribeck H, Saleh OA (2008) Multiplexed single-molecule measurements with magnetic tweezers. Rev Sci Instrum 79: 094301. https://doi.org/10.1063/1.2981687
[41]	Rossy J, Laufer JM, Legler DF (2018) Role of mechanotransduction and tension in T cell function. Front Immunol 9: 2638. https://doi.org/10.3389/fimmu.2018.02638
[42]	Shi X, Bi Y, Yang W, Guo X, Jiang Y, Wan C, Li L, Bai Y, Guo J, Wang Y, Chen X, Wu B, Sun H, Liu W, Wang J, Xu C (2013) Ca²⁺ regulates T-cell receptor activation by modulating the charge property of lipids. Nature 493: 111−115 doi: 10.1038/nature11699
[43]	Springer TA, Dustin ML (2012) Integrin inside-out signaling and the immunological synapse. Curr Opin Cell Biol 24: 107−115 doi: 10.1016/j.ceb.2011.10.004
[44]	Struckmeier J, Wahl R, Leuschner M, Nunes J, Janovjak H, Geisler U, Hofmann G, Jähnke T, Daniel JM (2008) Fully automated single-molecule force spectroscopy for screening applications. Nanotechnology 19: 384020. https://doi.org/10.1088/0957-4484/19/38/384020
[45]	Swamy M, Beck-Garcia K, Beck-Garcia E, Hartl FA, Morath A, Yousefi OS, Dopfer EP, Molnár E, Schulze AK, Blanco R, Borroto A, Martın-Blanco N, Alarcon B, Höfer T, Minguet S, Schamel WWA (2016) A cholesterol-based allostery model of T cell receptor phosphorylation. Immunity 44: 1091−1101 doi: 10.1016/j.immuni.2016.04.011
[46]	Wang X, Ha T (2013) Defining single molecular forces required to activate integrin and notch signaling. Science 340: 991−994 doi: 10.1126/science.1231041
[47]	Wu P, Zhang T, Liu B, Fei P, Cui L, Qin R, Zhu H, Yao D, Martinez RJ, Hu W, An C, Zhang Y, Liu J, Shi J, Fan J, Yin W, Sun J, Zhou C, Zeng X, Xu C, Wang J, Evavold BD, Zhu C, Chen W, Lou J (2019) Mechano-regulation of peptide-MHC class I conformations determines TCR antigen recognition. Mol Cell 73: 1−13 doi: 10.1016/j.molcel.2018.12.012
[48]	Yang M, Brackenbury WJ (2013) Membrane potential and cancer progression. Front Physiol 4: 185. https://doi.org/10.3389/fphys.2013.00185
[49]	Zhang T, Hu W, Chen W (2021) Plasma membrane integrates biophysical and biochemical regulation to trigger immune receptor functions. Front Immunol 12: 613185. https://doi.org/10.3389/fimmu.2021.613185
[50]	Zhou Y, Wong C-O, Cho K-J, Van Der Hoeven D, Liang H, Thakur DP, Luo J, Babic M, Zinsmaier KE, Zhu MX, Hu H, Venkatachalam K, Hancock JF (2015) Membrane potential modulates plasma membrane phospholipid dynamics and K-Ras signaling. Science 349: 873−876 doi: 10.1126/science.aaa5619
[51]	Zhu C, Chen W, Lou J, Rittase W, Li K (2019) Mechanosensing through immunoreceptors. Nat Immunol 10: 1269−1278
[52]	Zimmerman B, Kelly B, McMillan BJ, Seegar TCM, Dror RO, Kruse AC (2016) Crystal structure of a full-length human tetraspanin reveals a cholesterol-binding pocket. Cell 167: 1041−1051 doi: 10.1016/j.cell.2016.09.056