Periodic Arrangement of Lipopolysaccharides Nanostructures Accelerates and Enhances the Maturation Processes of Dendritic Cells

Liu, Yang; Wang, Kang-Hsin; Chen, Huan-Yuan; Li, Jie-Ren; Laurence, Ted A.; Ly, Sonny; Liu, Fu-Tong; Liu, Gang-Yu

doi:10.1021/acsanm.7b00254

Title: Periodic Arrangement of Lipopolysaccharides Nanostructures Accelerates and Enhances the Maturation Processes of Dendritic Cells

Journal Article · 28 January 2018 · ACS Applied Nano Materials

DOI: https://doi.org/10.1021/acsanm.7b00254 · OSTI ID:1560109

Liu, Yang ^[1]; Wang, Kang-Hsin ^[2]; Chen, Huan-Yuan ^[3]; Li, Jie-Ren ^[1]; Laurence, Ted A. ^[4]; Ly, Sonny ^[4]; Liu, Fu-Tong ^[5];

^[1]

Univ. of California, Davis, CA (United States). Dept. of Chemistry
Univ. of California, Davis, CA (United States). Dept. of Chemistry and Dept. of Dermatology, School of Medicine
Univ. of California, Davis, CA (United States). Dept. of Dermatology, School of Medicine; Academia Sinica, Taipei, (Taiwan). Inst. of Biomedical Sciences
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Univ. of California, Sacramento, CA (United States). Dept. of Dermatology, School of Medicine; Academia Sinica, Taipei, (Taiwan). Inst. of Biomedical Sciences

This work reports an important application of nanomaterials consisting of biological ligands, such as lipopolysaccharides (LPS) nanostructures. Upon immobilization onto surfaces as periodic arrays of nanostructures, these surface-bound LPS nanostructures significantly impacted the maturation process of bone marrow derived dendritic cells (BMDCs): accelerating the maturation process in comparison to other means of ligand presentations such as LPS solution and monolayers on surfaces. In some cases, LPS nanostructures led to a new maturation phenotype in vitro characterized by hyper-dendritized morphology. This level of maturation enhancement was observed for the first time in vitro. Possible mechanisms leading to the acceleration and enhancement of BMDC maturation were also discussed. This work demonstrates an important concept: surface-bound nanostructures of ligands provide a new and powerful cue for regulating cellular signaling processes. The fact that primary cells’ signaling processes, such as BMDC maturation, can be altered suggests a new means for programming dendritic cells for immune therapy.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1560109

Report Number(s):: LLNL--JRNL-779339; 970006

Journal Information:: ACS Applied Nano Materials, Journal Name: ACS Applied Nano Materials Journal Issue: 2 Vol. 1; ISSN 2574-0970

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (68)

A NTIGEN P RESENTATION AND T C ELL S TIMULATION BY D ENDRITIC C ELLS Guermonprez, Pierre; Valladeau, Jenny; Zitvogel, Laurence Annual Review of Immunology, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.immunol.20.100301.064828	journal	April 2002
Modulation of Cell Adhesion Complexes by Surface Protein Patterns Pesen, Devrim; Haviland, David B. ACS Applied Materials & Interfaces, Vol. 1, Issue 3 https://doi.org/10.1021/am800264h	journal	January 2009
Particle Lithography Enables Fabrication of Multicomponent Nanostructures Lin, Wei-feng; Swartz, Logan A.; Li, Jie-Ren The Journal of Physical Chemistry C, Vol. 117, Issue 44 https://doi.org/10.1021/jp406239d	journal	October 2013
Harnessing Dendritic Cells for Tumor Antigen Presentation Nierkens, Stefan; Janssen, Edith M. Cancers, Vol. 3, Issue 2 https://doi.org/10.3390/cancers3022195	journal	April 2011
Host Defense Mechanisms Triggered by Microbial Lipoproteins Through Toll-Like Receptors Brightbill, H. D. Science, Vol. 285, Issue 5428 https://doi.org/10.1126/science.285.5428.732	journal	July 1999
Dendritic cells and the control of immunity Banchereau, Jacques; Steinman, Ralph M. Nature, Vol. 392, Issue 6673 https://doi.org/10.1038/32588	journal	March 1998
Mast Cell Activation on Patterned Lipid Bilayers of Subcellular Dimensions ^† Orth, Reid N.; Wu, Min; Holowka, David A. Langmuir, Vol. 19, Issue 5 https://doi.org/10.1021/la026314c	journal	March 2003
Comparison of immature and mature bone marrow-derived dendritic cells by atomic force microscopy Xing, Feiyue; Wang, Jiongkun; Hu, Mingqian Nanoscale Research Letters, Vol. 6, Issue 1 https://doi.org/10.1186/1556-276X-6-455	journal	July 2011
Antifouling Coatings: Recent Developments in the Design of Surfaces That Prevent Fouling by Proteins, Bacteria, and Marine Organisms Banerjee, Indrani; Pangule, Ravindra C.; Kane, Ravi S. Advanced Materials, Vol. 23, Issue 6, p. 690-718 https://doi.org/10.1002/adma.201001215	journal	September 2010
Engineered Nanostructures of Haptens Lead to Unexpected Formation of Membrane Nanotubes Connecting Rat Basophilic Leukemia Cells Li, Jie-Ren; Ross, Shailise S.; Liu, Yang ACS Nano, Vol. 9, Issue 7 https://doi.org/10.1021/acsnano.5b02270	journal	June 2015
The nature of activatory and tolerogenic dendritic cell-derived signal II Bakdash, Ghaith; Sittig, Simone P.; Dijk, Tjeerd van Frontiers in Immunology, Vol. 4 https://doi.org/10.3389/fimmu.2013.00053	journal	January 2013
Immunobiology of Dendritic Cells Banchereau, Jacques; Briere, Francine; Caux, Christophe Annual Review of Immunology, Vol. 18, Issue 1 https://doi.org/10.1146/annurev.immunol.18.1.767	journal	April 2000
The Origin and Mechanism of the Allograft Reaction Lafferty, K. J.; Woolnough, J. Immunological Reviews, Vol. 35, Issue 1 https://doi.org/10.1111/j.1600-065X.1977.tb00241.x	journal	June 1977
Combined Effects of Substrate Topography and Stiffness on Endothelial Cytokine and Chemokine Secretion Jeon, Hyeona; Tsui, Jonathan H.; Jang, Sue Im ACS Applied Materials & Interfaces, Vol. 7, Issue 8 https://doi.org/10.1021/acsami.5b00554	journal	February 2015
HIV‐1 Nef triggers Vav‐mediated signaling pathway leading to functional and morphological differentiation of dendritic cells Quaranta, Maria Giovanna; Mattioli, Benedetta; Spadaro, Francesca The FASEB Journal, Vol. 17, Issue 14 https://doi.org/10.1096/fj.03-0272com	journal	September 2003
Mannan derivatives induce phenotypic and functional maturation of mouse dendritic cells Sheng, Kuo-Ching; Pouniotis, Dodie S.; Wright, Mark D. Immunology, Vol. 118, Issue 3 https://doi.org/10.1111/j.1365-2567.2006.02384.x	journal	July 2006
Positioning protein molecules on surfaces: A nanoengineering approach to supramolecular chemistry Liu, G. -Y.; Amro, N. A. Proceedings of the National Academy of Sciences, Vol. 99, Issue 8 https://doi.org/10.1073/pnas.072695699	journal	April 2002
Costimulatory Molecules on Immunogenic Versus Tolerogenic Human Dendritic Cells Hubo, Mario; Trinschek, Bettina; Kryczanowsky, Fanny Frontiers in Immunology, Vol. 4 https://doi.org/10.3389/fimmu.2013.00082	journal	January 2013
Engineered Nanostructures of Antigen Provide an Effective Means for Regulating Mast Cell Activation Deng, Zhao; Weng, I-Chun; Li, Jie-Ren ACS Nano, Vol. 5, Issue 11 https://doi.org/10.1021/nn202510n	journal	October 2011
Antigen presentation by Langerhans cells Igyártó, Botond Z.; Kaplan, Daniel H. Current Opinion in Immunology, Vol. 25, Issue 1 https://doi.org/10.1016/j.coi.2012.11.007	journal	February 2013
Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. De Smedt, T.; Pajak, B.; Muraille, E. Journal of Experimental Medicine, Vol. 184, Issue 4 https://doi.org/10.1084/jem.184.4.1413	journal	October 1996
Comparison of hexamethyldisilazane and critical point drying treatments for SEM analysis of anaerobic biofilms and granular sludge Araujo, J. C. Journal of Electron Microscopy, Vol. 52, Issue 4 https://doi.org/10.1093/jmicro/52.4.429	journal	September 2003
Toll-like receptor signalling Akira, Shizuo; Takeda, Kiyoshi Nature Reviews Immunology, Vol. 4, Issue 7 https://doi.org/10.1038/nri1391	journal	July 2004
Nanopillar Surface Topology Promotes Cardiomyocyte Differentiation through Cofilin-Mediated Cytoskeleton Rearrangement Seo, Ha-Rim; Joo, Hyung Joon; Kim, Dae Hwan ACS Applied Materials & Interfaces, Vol. 9, Issue 20 https://doi.org/10.1021/acsami.7b01555	journal	May 2017
Requirement of Rac1 and Rac2 Expression by Mature Dendritic Cells for T Cell Priming Benvenuti, F. Science, Vol. 305, Issue 5687 https://doi.org/10.1126/science.1099159	journal	August 2004
Detection of CD28/CD86 co-stimulatory molecules and surface properties of T and dendritic cells: An AFM study: CD28 and CD86 molecules appeared to be expressed as 100-200 nm nanoclusters Huang, Xun; Guo, He; Wang, Chuang Scanning, Vol. 38, Issue 4 https://doi.org/10.1002/sca.21279	journal	October 2015
Targeted Disruption of the MyD88 Gene Results in Loss of IL-1- and IL-18-Mediated Function Adachi, Osamu; Kawai, Taro; Takeda, Kiyoshi Immunity, Vol. 9, Issue 1 https://doi.org/10.1016/S1074-7613(00)80596-8	journal	July 1998
Structural Insights into the Assembly of Large Oligomeric Signalosomes in the Toll-Like Receptor-Interleukin-1 Receptor Superfamily Ferrao, R.; Li, J.; Bergamin, E. Science Signaling, Vol. 5, Issue 226 https://doi.org/10.1126/scisignal.2003124	journal	May 2012
Calcium ions induce collapse of charged O-side chains of lipopolysaccharides from Pseudomonas aeruginosa Schneck, Emanuel; Papp-Szabo, Erzsebet; Quinn, Bonnie E. Journal of The Royal Society Interface, Vol. 6, Issue suppl_5 https://doi.org/10.1098/rsif.2009.0190.focus	journal	July 2009
Effects of 3-dimensional culture conditions (collagen-chitosan nano-scaffolds) on maturation of dendritic cells and their capacity to interact with T-lymphocytes Daneshmandi, Saeed; Dibazar, Shaghayegh Pishkhan; Fateh, Shirin Journal of Immunotoxicology, Vol. 13, Issue 2 https://doi.org/10.3109/1547691X.2015.1045636	journal	May 2015
Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity Wilson, Nicholas S.; Behrens, Georg M. N.; Lundie, Rachel J. Nature Immunology, Vol. 7, Issue 2 https://doi.org/10.1038/ni1300	journal	January 2006
Regulation of antigen uptake, migration, and lifespan of dendritic cell by Toll-like receptors Zanoni, Ivan; Granucci, Francesca Journal of Molecular Medicine, Vol. 88, Issue 9 https://doi.org/10.1007/s00109-010-0638-x	journal	June 2010
Helical assembly in the MyD88–IRAK4–IRAK2 complex in TLR/IL-1R signalling Lin, Su-Chang; Lo, Yu-Chih; Wu, Hao Nature, Vol. 465, Issue 7300 https://doi.org/10.1038/nature09121	journal	May 2010
Cell-type and Donor-specific Transcriptional Responses to Interferon-α Schlaak, Joerg F.; Hilkens, Catharien M. U.; Costa-Pereira, Ana P. Journal of Biological Chemistry, Vol. 277, Issue 51 https://doi.org/10.1074/jbc.M205571200	journal	December 2002
Dendritic Cells in Cancer Immunotherapy Fong, Lawrence; Engleman, Edgar G. Annual Review of Immunology, Vol. 18, Issue 1 https://doi.org/10.1146/annurev.immunol.18.1.245	journal	April 2000
Phenotype and polarization of autologous T cells by biomaterial-treated dendritic cells: Phenotype and Polarization of Autologous T Cells Park, Jaehyung; Gerber, Michael H.; Babensee, Julia E. Journal of Biomedical Materials Research Part A, Vol. 103, Issue 1 https://doi.org/10.1002/jbm.a.35150	journal	March 2014
Engineering the Spatial Selectivity of Surfaces at the Nanoscale Using Particle Lithography Combined with Vapor Deposition of Organosilanes Li, Jie-Ren; Lusker, Kathie L.; Yu, Jing-Jiang ACS Nano, Vol. 3, Issue 7 https://doi.org/10.1021/nn9004796	journal	June 2009
Engineering Cell Instructive Materials To Control Cell Fate and Functions through Material Cues and Surface Patterning Ventre, Maurizio; Netti, Paolo A. ACS Applied Materials & Interfaces, Vol. 8, Issue 24 https://doi.org/10.1021/acsami.5b08658	journal	January 2016
Innate immune recognition: mechanisms and pathways: Innate immune recognition Medzhitov, Ruslan; Janeway, CharleS. Jr Immunological Reviews, Vol. 173, Issue 1 https://doi.org/10.1034/j.1600-065X.2000.917309.x	journal	February 2000
Synergy between TLR2 and TLR4: A safety mechanism Beutler, E.; Gelbart, T.; West, C. Blood Cells, Molecules, and Diseases, Vol. 27, Issue 4 https://doi.org/10.1006/bcmd.2001.0441	journal	July 2001
An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow Lutz, Manfred B.; Kukutsch, Nicole; Ogilvie, Alexandra L. J. Journal of Immunological Methods, Vol. 223, Issue 1 https://doi.org/10.1016/S0022-1759(98)00204-X	journal	February 1999
Bioinspired Zwitterionic Surface Coatings with Robust Photostability and Fouling Resistance Huang, Chun-Jen; Chu, Sz-Hau; Wang, Lin-Chuan ACS Applied Materials & Interfaces, Vol. 7, Issue 42 https://doi.org/10.1021/acsami.5b08418	journal	October 2015
Characterization of methylene diphenyl diisocyanate-haptenated human serum albumin and hemoglobin Mhike, Morgen; Chipinda, Itai; Hettick, Justin M. Analytical Biochemistry, Vol. 440, Issue 2 https://doi.org/10.1016/j.ab.2013.05.022	journal	September 2013
Conditioning of Cardiovascular Tissue Using a Noncontact Magnetic Stretch Bioreactor with Embedded Magnetic Nanoparticles Hogan, Matthew; Chen, Yi-Ting; Kolhatkar, Arati G. ACS Biomaterials Science & Engineering, Vol. 2, Issue 9 https://doi.org/10.1021/acsbiomaterials.6b00375	journal	August 2016
T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases Mempel, Thorsten R.; Henrickson, Sarah E.; von Andrian, Ulrich H. Nature, Vol. 427, Issue 6970 https://doi.org/10.1038/nature02238	journal	January 2004
Cancer immunotherapy comes of age Mellman, Ira; Coukos, George; Dranoff, Glenn Nature, Vol. 480, Issue 7378 https://doi.org/10.1038/nature10673	journal	December 2011
GSTO1-1 modulates metabolism in macrophages activated through the LPS and TLR4 pathway Menon, Deepthi; Coll, Rebecca; O'Neill, Luke A. J. Journal of Cell Science, Vol. 128, Issue 10 https://doi.org/10.1242/jcs.167858	journal	May 2015
TLR4, Ethanol, and Lipid Rafts: A New Mechanism of Ethanol Action with Implications for other Receptor-Mediated Effects Szabo, Gyongyi; Dolganiuc, Angela; Dai, Qun The Journal of Immunology, Vol. 178, Issue 3 https://doi.org/10.4049/jimmunol.178.3.1243	journal	January 2007
T OLL -L IKE R ECEPTORS Takeda, Kiyoshi; Kaisho, Tsuneyasu; Akira, Shizuo Annual Review of Immunology, Vol. 21, Issue 1 https://doi.org/10.1146/annurev.immunol.21.120601.141126	journal	April 2003
T cell repertoire scanning is promoted by dynamic dendritic cell behavior and random T cell motility in the lymph node Miller, M. J.; Hejazi, A. S.; Wei, S. H. Proceedings of the National Academy of Sciences, Vol. 101, Issue 4 https://doi.org/10.1073/pnas.0306407101	journal	January 2004
Comprehensive Analysis of the Effect of Electron Irradiation on Oligo(ethylene glycol) Terminated Self-Assembled Monolayers Applicable for Specific and Nonspecific Patterning of Proteins Jeyachandran, Yekkoni Lakshmanan; Zharnikov, Michael The Journal of Physical Chemistry C, Vol. 116, Issue 28 https://doi.org/10.1021/jp303764h	journal	July 2012
DNA Loading and Release Using Custom-Tailored Poly( l -lysine) Surfaces Shakiba, Amin; Patil, Sagar L.; Zenasni, Oussama ACS Applied Materials & Interfaces, Vol. 9, Issue 28 https://doi.org/10.1021/acsami.7b05024	journal	July 2017
A Supra-monolayer Nanopattern for Organic Nanoparticle Array Deposition Wang, Sunxi; Sobczynski, Daniel J.; Jahanian, Pedram ACS Applied Materials & Interfaces, Vol. 5, Issue 7 https://doi.org/10.1021/am400181w	journal	March 2013
Dendritic Cells Mellman, Ira; Steinman, Ralph M. Cell, Vol. 106, Issue 3 https://doi.org/10.1016/S0092-8674(01)00449-4	journal	August 2001
High state of order of isolated bacterial lipopolysaccharide and its possible contribution to the permeation barrier property of the outer membrane Labischinski, H.; Barnickel, G.; Bradaczek, H. Journal of Bacteriology, Vol. 162, Issue 1 https://doi.org/10.1128/JB.162.1.9-20.1985	journal	April 1985
CTLA-4 Control over Foxp3+ Regulatory T Cell Function Wing, K.; Onishi, Y.; Prieto-Martin, P. Science, Vol. 322, Issue 5899 https://doi.org/10.1126/science.1160062	journal	October 2008
Control of Regulatory T Cells and Airway Tolerance by Lung Macrophages and Dendritic Cells Duan, Wei; Croft, Michael Annals of the American Thoracic Society, Vol. 11, Issue Supplement 5 https://doi.org/10.1513/AnnalsATS.201401-028AW	journal	December 2014
Campylobacter jejuni Lipooligosaccharides Modulate Dendritic Cell-Mediated T Cell Polarization in a Sialic Acid Linkage-Dependent Manner Bax, Marieke; Kuijf, Mark L.; Heikema, Astrid P. Infection and Immunity, Vol. 79, Issue 7 https://doi.org/10.1128/IAI.00009-11	journal	April 2011
Monocyte-derived DC maturation strategies and related pathways: a transcriptional view Castiello, Luciano; Sabatino, Marianna; Jin, Ping Cancer Immunology, Immunotherapy, Vol. 60, Issue 4 https://doi.org/10.1007/s00262-010-0954-6	journal	January 2011
Determination of critical micelle concentrations and aggregation numbers by fluorescence correlation spectroscopy: Aggregation of a lipopolysaccharide Yu, Lanlan; Tan, Minyi; Ho, Bow Analytica Chimica Acta, Vol. 556, Issue 1 https://doi.org/10.1016/j.aca.2005.09.008	journal	January 2006
Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. Cella, M.; Scheidegger, D.; Palmer-Lehmann, K. Journal of Experimental Medicine, Vol. 184, Issue 2 https://doi.org/10.1084/jem.184.2.747	journal	August 1996
Nanopattern Gradients for Cell Studies Fabricated Using Hole-Mask Colloidal Lithography Bøggild, Thea; Runager, Kasper; Sutherland, Duncan S. ACS Applied Materials & Interfaces, Vol. 8, Issue 24 https://doi.org/10.1021/acsami.5b08315	journal	June 2016
A Pivotal Role of Rho GTPase in the Regulation of Morphology and Function of Dendritic Cells Kobayashi, Michihiro; Azuma, Eiichi; Ido, Masaru The Journal of Immunology, Vol. 167, Issue 7 https://doi.org/10.4049/jimmunol.167.7.3585	journal	October 2001
Actin Dynamics Regulates Dendritic Cell-Mediated Transfer of HIV-1 to T Cells Ménager, Mickaël M.; Littman, Dan R. Cell, Vol. 164, Issue 4 https://doi.org/10.1016/j.cell.2015.12.036	journal	February 2016
TNF ligands and receptors - a matter of life and death: TNF ligands/receptors signalling and pharmacology MacEwan, David J. British Journal of Pharmacology, Vol. 135, Issue 4 https://doi.org/10.1038/sj.bjp.0704549	journal	February 2002
The structural basis of lipopolysaccharide recognition by the TLR4–MD-2 complex Park, Beom Seok; Song, Dong Hyun; Kim, Ho Min Nature, Vol. 458, Issue 7242 https://doi.org/10.1038/nature07830	journal	March 2009
CD40L Induces Functional Tunneling Nanotube Networks Exclusively in Dendritic Cells Programmed by Mediators of Type 1 Immunity Zaccard, Colleen R.; Watkins, Simon C.; Kalinski, Pawel The Journal of Immunology, Vol. 194, Issue 3 https://doi.org/10.4049/jimmunol.1401832	journal	December 2014
The electron's spin and molecular chirality – how are they related and how do they affect life processes? Michaeli, Karen; Kantor-Uriel, Nirit; Naaman, Ron Chemical Society Reviews, Vol. 45, Issue 23 https://doi.org/10.1039/C6CS00369A	journal	January 2016

Cited By (2)

Tunneling nanotubes mediate the expression of senescence markers in mesenchymal stem/stromal cell spheroids: TNTs mediate senescence in MSC spheroids Whitehead, Jacklyn; Zhang, Jiali; Harvestine, Jenna N. STEM CELLS, Vol. 38, Issue 1 https://doi.org/10.1002/stem.3056	journal	August 2019
Single Dose of a Polyanhydride Particle-Based Vaccine Generates Potent Antigen-Specific Antitumor Immune Responses Wafa, Emad I.; Geary, Sean M.; Ross, Kathleen A. Journal of Pharmacology and Experimental Therapeutics, Vol. 370, Issue 3 https://doi.org/10.1124/jpet.118.252809	journal	October 2018

Similar Records

CXCR4 engagement promotes dendritic cell survival and maturation

Journal Article · 2007 · Biochemical and Biophysical Research Communications · OSTI ID:21032915

Kabashima, Kenji; Sugita, Kazunari; Shiraishi, Noriko; +3 more

Staphylococcal enterotoxin C2 stimulated the maturation of bone marrow derived dendritic cells via TLR-NFκB signaling pathway

Journal Article · 2018 · Experimental Cell Research · OSTI ID:23082654

Yao, Songyuan; Xu, Mingkai; Li, Yansheng; +4 more

ATP/P2X7-NLRP3 axis of dendritic cells participates in the regulation of airway inflammation and hyper-responsiveness in asthma by mediating HMGB1 expression and secretion

Journal Article · 2018 · Experimental Cell Research · OSTI ID:23082400

Li, Ruiting; Wang, Jing; Li, Ruifang; +7 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Periodic Arrangement of Lipopolysaccharides Nanostructures Accelerates and Enhances the Maturation Processes of Dendritic Cells

Citation Formats

References (68)

Cited By (2)

Similar Records

Related Subjects