微流控芯片技术在细胞黏附研究中的优势与应用前景
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摘要
背景:细胞黏附性质影响细胞的迁移、增殖、分化,对于细胞分离和富集、组织工程、临床疾病研究及应用均有极其重要的意义。微流控芯片具有小型化、集成化、高通量、低能耗、分析快速等特性,在细胞黏附研究中具有独特的优势。目的:总结并讨论微流控芯片技术在细胞黏附研究中应用的最新进展。方法:由第一作者检索2008至2018年PubMed数据库和百链云数据库,纳入与微流控技术、细胞黏附等相关的文献,并进行系统整理、归纳总结和分析。结果与结论:共检索到文献238篇,按照纳入和排除标准筛选后,共纳入53篇文献,通过阅读、总结和分析文献发现:微流控芯片平台为进行体外基于细胞黏附研究提供了新的可能性,其具有更高的通量,并且能精确控制生物、物理、化学因素构建体内细胞微环境,调控一系列细胞行为,包括细胞黏附、迁移、生长、增殖和分化及细胞与细胞、细胞与基质的相互作用等。微流控芯片技术在动态监测细胞黏附过程、定量检测细胞黏附力、分离和富集稀有细胞、筛选生物医学材料及研究细胞黏附相关疾病等方面具有广阔的应用前景。
BACKGROUND: Cell adhesion affects cell migration, proliferation, and differentiation. It is of extremely vital significance for cell separation and enrichment, tissue engineering and clinical disease research. Microfluidic chips have unique advantages in cell adhesion studies such as miniaturization, integration, high throughput,low energy consumption, and rapid analysis.OBJECTIVE: To summarize and discuss the latest advances of microfluidic chip technology in cell adhesion research.METHODS: The first author performed a data retrieval of PubMed and Bailianyun databases to search the articles published during2008-2018 and addressing cell adhesion and microfluidic chip technology and reviewed the literatures systematically.RESULTS AND CONCLUSION: A total of 238 articles were retrieved and 53 articles were included in the final analysis according to the inclusion and exclusion criteria. These articles were read, summarized and analyzed. Results showed that the microfluidic chip platform provides new possibilities for in vitro studies of cell adhesion because it exhibits higher throughput, enables precise control of the biological,physical, and chemical factors involved in the construction of in vivo cellular microenvironment, and regulates a series of cellular behaviors including cell adhesion, migration, growth, proliferation, differentiation, cell-cell interactions, and cell-matrix interactions. Microfluidic chip technology has broad application prospects in the dynamic monitoring of cell adhesion process, quantitative measurement of cell adhesion,isolation and enrichment of rare cells, screening of biomedical materials, and research on cell adhesion-related diseases.
BACKGROUND: Cell adhesion affects cell migration, proliferation, and differentiation. It is of extremely vital significance for cell separation and enrichment, tissue engineering and clinical disease research. Microfluidic chips have unique advantages in cell adhesion studies such as miniaturization, integration, high throughput,low energy consumption, and rapid analysis.OBJECTIVE: To summarize and discuss the latest advances of microfluidic chip technology in cell adhesion research.METHODS: The first author performed a data retrieval of PubMed and Bailianyun databases to search the articles published during2008-2018 and addressing cell adhesion and microfluidic chip technology and reviewed the literatures systematically.RESULTS AND CONCLUSION: A total of 238 articles were retrieved and 53 articles were included in the final analysis according to the inclusion and exclusion criteria. These articles were read, summarized and analyzed. Results showed that the microfluidic chip platform provides new possibilities for in vitro studies of cell adhesion because it exhibits higher throughput, enables precise control of the biological,physical, and chemical factors involved in the construction of in vivo cellular microenvironment, and regulates a series of cellular behaviors including cell adhesion, migration, growth, proliferation, differentiation, cell-cell interactions, and cell-matrix interactions. Microfluidic chip technology has broad application prospects in the dynamic monitoring of cell adhesion process, quantitative measurement of cell adhesion,isolation and enrichment of rare cells, screening of biomedical materials, and research on cell adhesion-related diseases.
引文
[1]Khalili AA,Ahmad MR.A Review of Cell Adhesion Studies for Biomedical and Biological Applications.Int J Mol Sci.2015;16(8):18149-18184.
[2]Kunutsor SK,Bakker SJ,Dullaart RP.Soluble Vascular Cell Adhesion Molecules May be Protective of Future Cardiovascular Disease Risk:Findings from the PREVENDProspective Cohort Study.J Atheroscler Thromb.2017;24(8):804-818.3589
[3]Garrido-Urbani S,Vonlaufen A,Stalin J,et al.Junctional adhesion molecule C(JAM-C)dimerization aids cancer cell migration and metastasis.Biochimica Et Biophysica Acta.2018;1865(4):638-649.
[4]Dimitriadis GK,Kaur J,Adya R,et al.Chemerin induces endothelial cell inflammation:activation of nuclear factor-kappa beta and monocyte-endothelial adhesion.Oncotarget.2018;9(24):16678-16690.
[5]Guevara-Pantoja PE,Jim??Nez-Vald??S RJ,Garc?-A-Cordero JL,et al.Pressure-actuated monolithic acrylic microfluidic valves and pumps.Lab Chip.2018;18(4):662-669.
[6]Cui X,Liu Y,Hu D,et al.A fluorescent microbead-based microfluidic immunoassay chip for immune cell cytokine secretion quantification.Lab Chip.2018;18(3);522-531.
[7]Chen C,Townsend AD,Hayter EA,et al.Insert-based microfluidics for 3D cell culture with analysis.Anal Bioanal Chem.2018;410(22):1-11.
[8]Wang W,Li L,Ding M,et al.A Microfluidic Hydrogel Chip with Orthogonal Dual Gradients of Matrix Stiffness and Oxygen for Cytotoxicity Test.Biochip J.2018;12(2):1-10.
[9]Honarmandi P,Lee H,Lang MJ,et al.A microfluidic system with optical laser tweezers to study mechanotransduction and focal adhesion recruitment.Lab Chip.2011;11(4):684-694.
[10]Thompson TJ,Han B.Analysis of adhesion kinetics of cancer cells on inflamed endothelium using a microfluidic platform.Biomicrofluidics.2018;12(4):042215.
[11]Tu L,Li X,Bian S,et al.Label-free and real-time monitoring of single cell attachment on template-stripped plasmonic nano-holes.Sci Rep.2017;7(1):1-11.
[12]Hoffmann M,Tserpes K,Moutsompegka E,et al.Determination of adhesion strength of pre-bond contaminated composite-tometal bonded joints by centrifuge tests.Compos B Eng.2018;147:114-121.
[13]Kim H,Yamagishi A,Imaizumi M,et al.Quantitative measurements of intercellular adhesion between a macrophage and cancer cells using a cup-attached AFM chip.Colloids Surf B Biointerfaces.2017;155:366-372.
[14]Hogan B,Babataheri A,Hwang Y,et al.Characterizing Cell Adhesion by Using Micropipette Aspiration.Biophys J.2015;109(2):209-219.
[15]Jing P,Liu Y,Keeler EG,et al.Optical tweezers system for live stem cell organization at the single-cell level.Biomed Opt Express.2018;9(2):771-779.
[16]Fuhrmann A,Engler AJ.The cytoskeleton regulates cell attachment strength.Biophys J.2015;109(1):57-65.
[17]Kim HW,Han S,Kim W,et al.Modulating wall shear stress gradient via equilateral triangular channel for in situ cellular adhesion assay.Biomicrofluidics.2016;10(5):11-25.
[18]Li Y,Gao A,Yu L.Monitoring of TGF-β1-Induced Human Lung Adenocarcinoma A549 Cells Epithelial-Mesenchymal Transformation Process by Measuring Cell Adhesion Force with a Microfluidic Device.Appl Biochem Biotechnol.2016;178(1):114-125.
[19]Lu L,Zheng GX,Yang YS,et al.Measurement of Giardia lamblia,adhesion force using an integrated microfluidic assay.Anal Bioanal Chem.2017;409(5):1-9.
[20]Christ KV,Williamson KB,Masters KS,et al.Measurement of single-cell adhesion strength using a microfluidic assay.Biomed Microdevices.2010;12(3):443-455.
[21]Mao S,Zhang W,Huang Q,et al.In Situ Scatheless Cell Detachment Reveals Correlation between Adhesion Strength and Viability at Single-Cell Resolution.Angew Chem Int Ed Engl.2017;57(1):236-240.
[22]Mao S,Zhang Q,Li H,et al.Adhesion analysis of single circulating tumor cells on a base layer of endothelial cells using open microfluidics.Chem Sci.2018;9:7694-7699.
[23]Cheng Z,Wu X,Cheng J,et al.Microfluidic fluorescenceactivated cell sorting(μFACS)chip with integrated piezoelectric actuators for low-cost mammalian cell enrichment.Microfluid Nanofluidics.2017;21(1):9-19.
[24]Kwak B,Lee J,Lee D,et al.Selective isolation of magnetic nanoparticle-mediated heterogeneity subpopulation of circulating tumor cells using magnetic gradient based microfluidic system.Biosens Bioelectron.2017;88:153-158.
[25]Pang L,Shen S,Ma C,et al.Deformability and size-based cancer cell separation using an integrated microfluidic device.Analyst.2015;140(21):7335-7346.
[26]Ali H,Park CW.Numerical study on the complete blood cell sorting using particle tracing and dielectrophoresis in a microfluidic device.Korea-Aust Rheol J.2016;28(4):327-339.
[27]Ung L,Mutafopulos K,Spink P,et al.Enhanced Surface Acoustic Wave Cell Sorting by 3D microfluidic chip design.Lab Chip.2017;17(23):4059-4069.
[28]Singh A,Singh A,Suri S,et al.Adhesion strength-based,label-free isolation of human pluripotent stem cells.Nat Methods.2013;10(5):438-444.
[29]桑维维,常亚男,李娟.微流控芯片对乳腺癌细胞mda-mb-231的捕获及再培养研究[J].中国生物工程杂志,2015,35(6):46-53.
[30]Zhang Y,Wu M,Han X,et al.High-throughput,label-free isolation of cancer stem cells based on cell adhesion capacity.Angew Chem Int Ed Engl.2015;54(37):10838-10842.
[31]Chen W,Allen SG,Reka AK,et al.Nanoroughened adhesion-based capture of circulating tumor cells with heterogeneous expression and metastatic characteristics.BMC Cancer.2016;16:614-625.
[32]Dasanna AK,Schwarz US.Adhesion-based sorting of blood cells:an adhesive dynamics simulation study.Soft Matter.2018;14(44):9061-9070.
[33]Ermis M,Antmen E,Hasirci V.Micro and Nanofabrication methods to control cell-substrate interactions and cell behavior:A review from the tissue engineering perspective.Bioact Mater.2018;3(3):355-369.
[34]Francesco R,Simone B,Federica F,et al.A micron-scale surface topography design reducing cell adhesion to implanted materials.Sci Rep.2018;8(1):10887-10899.
[35]Zahran R,Rosales LJI,Rodríguez Valverde MA,et al.Effect of Hydrofluoric Acid Etching Time on Titanium Topography,Chemistry,Wettability,and Cell Adhesion.PLoS One.2016;11(11):e0165296.
[36]余劭婷,秦金桥,关国平,等.丝素纤维表面改性提高细胞黏附性能[J].生物医学工程学进展,2016,37(3):144-149.
[37]Tang Z,Akiyama Y,Itoga K,et al.Shear stress-dependent cell detachment from temperature-responsive cell culture surfaces in a microfluidic device.Biomaterials.2012;33(30):7405-7411.
[38]Hampe A,Li Z,Sethi S,et al.A Microfluidic Platform to Study Astrocyte Adhesion on Nanoporous Gold Thin Films.Nanomaterials.2018;8(7):452-463.
[39]Li P,Yu H,Liu N,et al.Visible Light Induced Electropolymerization of Suspended Hydrogel Bioscaffolds in a Microfluidic Chip.Biomater Sci.2018;6(6):1371-1378.
[40]Stamp ME,J?tten AM,Kudella PW,et al.Exploring the Limits of Cell Adhesion under Shear Stress within Physiological Conditions and beyond on a Chip.Diagnostics.2016;6(4):38-52.
[41]Gong X,Yao J,He H,et al.Combination of flow and micropattern alignment affecting flow-resistant endothelial cell adhesion.J Mech Behav Biomed Mater.2017;74:11-20.
[42]Vanessa K,Christoph G,Ivannikov D,et al.vasQchip:A Novel Microfluidic,Artificial Blood Vessel Scaffold for Vascularized3D Tissues.Adv MaterTechnol.2018;3(4):1700246.
[43]Sharmistha N,Kumar PA,Viswanathan K,et al.Controlled shear flow directs osteogenesis on UHMWPE based hybrid nano-biocomposites in custom designed PMMA microfluidic device.ACS Appl Bio Mater.2018;1(2):414-435.
[44]秦建华,张敏,于浩,等.人体器官芯片[J].中国科学院院刊,2017,32(12):18-26.
[45]Ahn S,Ardo?a HAM,Lind JU,et al.Mussel-inspired 3D fiber scaffolds for heart-on-a-chip toxicity studies of engineered nanomaterials.Anal Bioanal Chem.2018;410(24):6141-6154.
[46]Khazali AS,Clark AM,Wells A.A Pathway to Personalizing Therapy for Metastases Using Liver-on-a-Chip Platforms.Stem Cell Rev.2017;13(3):364-380.
[47]Humayun M,Chow CW,Ewk Y.Microfluidic lung airway-on-a-chip with arrayable suspended gels for studying epithelial and smooth muscle cell interactions.Lab Chip.2018;18(9):1298-1309.
[48]Wilmer MJ,Ng CP,Lanz HL,et al.Kidney-on-a-Chip Technology for Drug-Induced Nephrotoxicity Screening.Trends Biotechnol.2016;34(2):156-170.
[49]Jalili-Firoozinezhad S,Prantil-Baun R,Jiang A,et al.Modeling radiation injury-induced cell death and countermeasure drug responses in a human Gut-on-a-Chip.Cell Death Dis.2018;9(2):223-236.
[50]Kucukal E,Little JA,Gurkan UA.Shear dependent red blood cell adhesion in microscale flow.Integr Biol.2018;10(4):194-206.
[51]Kim M,Alapan Y,Adhikari A,et al.Hypoxia enhanced adhesion of red blood cells in microscale flow.Microcirculation.2017;24(5):e12374.
[52]Shea DJ,Li YW,Stebe KJ,et al.E-selectin-mediated rolling facilitates pancreatic cancer cell adhesion to hyaluronic acid.FASEB J.2017;31(11):5078-5086.
[53]Antoniellis Silveira AA,Dominical VM,Morelli Vital D,et al.Attenuation of TNF-induced neutrophil adhesion by simvastatin is associated with the inhibition of Rho-GTPase activity,p50 activity and morphological changes.Int Immunopharmacol.2018;58:160-165.
[2]Kunutsor SK,Bakker SJ,Dullaart RP.Soluble Vascular Cell Adhesion Molecules May be Protective of Future Cardiovascular Disease Risk:Findings from the PREVENDProspective Cohort Study.J Atheroscler Thromb.2017;24(8):804-818.3589
[3]Garrido-Urbani S,Vonlaufen A,Stalin J,et al.Junctional adhesion molecule C(JAM-C)dimerization aids cancer cell migration and metastasis.Biochimica Et Biophysica Acta.2018;1865(4):638-649.
[4]Dimitriadis GK,Kaur J,Adya R,et al.Chemerin induces endothelial cell inflammation:activation of nuclear factor-kappa beta and monocyte-endothelial adhesion.Oncotarget.2018;9(24):16678-16690.
[5]Guevara-Pantoja PE,Jim??Nez-Vald??S RJ,Garc?-A-Cordero JL,et al.Pressure-actuated monolithic acrylic microfluidic valves and pumps.Lab Chip.2018;18(4):662-669.
[6]Cui X,Liu Y,Hu D,et al.A fluorescent microbead-based microfluidic immunoassay chip for immune cell cytokine secretion quantification.Lab Chip.2018;18(3);522-531.
[7]Chen C,Townsend AD,Hayter EA,et al.Insert-based microfluidics for 3D cell culture with analysis.Anal Bioanal Chem.2018;410(22):1-11.
[8]Wang W,Li L,Ding M,et al.A Microfluidic Hydrogel Chip with Orthogonal Dual Gradients of Matrix Stiffness and Oxygen for Cytotoxicity Test.Biochip J.2018;12(2):1-10.
[9]Honarmandi P,Lee H,Lang MJ,et al.A microfluidic system with optical laser tweezers to study mechanotransduction and focal adhesion recruitment.Lab Chip.2011;11(4):684-694.
[10]Thompson TJ,Han B.Analysis of adhesion kinetics of cancer cells on inflamed endothelium using a microfluidic platform.Biomicrofluidics.2018;12(4):042215.
[11]Tu L,Li X,Bian S,et al.Label-free and real-time monitoring of single cell attachment on template-stripped plasmonic nano-holes.Sci Rep.2017;7(1):1-11.
[12]Hoffmann M,Tserpes K,Moutsompegka E,et al.Determination of adhesion strength of pre-bond contaminated composite-tometal bonded joints by centrifuge tests.Compos B Eng.2018;147:114-121.
[13]Kim H,Yamagishi A,Imaizumi M,et al.Quantitative measurements of intercellular adhesion between a macrophage and cancer cells using a cup-attached AFM chip.Colloids Surf B Biointerfaces.2017;155:366-372.
[14]Hogan B,Babataheri A,Hwang Y,et al.Characterizing Cell Adhesion by Using Micropipette Aspiration.Biophys J.2015;109(2):209-219.
[15]Jing P,Liu Y,Keeler EG,et al.Optical tweezers system for live stem cell organization at the single-cell level.Biomed Opt Express.2018;9(2):771-779.
[16]Fuhrmann A,Engler AJ.The cytoskeleton regulates cell attachment strength.Biophys J.2015;109(1):57-65.
[17]Kim HW,Han S,Kim W,et al.Modulating wall shear stress gradient via equilateral triangular channel for in situ cellular adhesion assay.Biomicrofluidics.2016;10(5):11-25.
[18]Li Y,Gao A,Yu L.Monitoring of TGF-β1-Induced Human Lung Adenocarcinoma A549 Cells Epithelial-Mesenchymal Transformation Process by Measuring Cell Adhesion Force with a Microfluidic Device.Appl Biochem Biotechnol.2016;178(1):114-125.
[19]Lu L,Zheng GX,Yang YS,et al.Measurement of Giardia lamblia,adhesion force using an integrated microfluidic assay.Anal Bioanal Chem.2017;409(5):1-9.
[20]Christ KV,Williamson KB,Masters KS,et al.Measurement of single-cell adhesion strength using a microfluidic assay.Biomed Microdevices.2010;12(3):443-455.
[21]Mao S,Zhang W,Huang Q,et al.In Situ Scatheless Cell Detachment Reveals Correlation between Adhesion Strength and Viability at Single-Cell Resolution.Angew Chem Int Ed Engl.2017;57(1):236-240.
[22]Mao S,Zhang Q,Li H,et al.Adhesion analysis of single circulating tumor cells on a base layer of endothelial cells using open microfluidics.Chem Sci.2018;9:7694-7699.
[23]Cheng Z,Wu X,Cheng J,et al.Microfluidic fluorescenceactivated cell sorting(μFACS)chip with integrated piezoelectric actuators for low-cost mammalian cell enrichment.Microfluid Nanofluidics.2017;21(1):9-19.
[24]Kwak B,Lee J,Lee D,et al.Selective isolation of magnetic nanoparticle-mediated heterogeneity subpopulation of circulating tumor cells using magnetic gradient based microfluidic system.Biosens Bioelectron.2017;88:153-158.
[25]Pang L,Shen S,Ma C,et al.Deformability and size-based cancer cell separation using an integrated microfluidic device.Analyst.2015;140(21):7335-7346.
[26]Ali H,Park CW.Numerical study on the complete blood cell sorting using particle tracing and dielectrophoresis in a microfluidic device.Korea-Aust Rheol J.2016;28(4):327-339.
[27]Ung L,Mutafopulos K,Spink P,et al.Enhanced Surface Acoustic Wave Cell Sorting by 3D microfluidic chip design.Lab Chip.2017;17(23):4059-4069.
[28]Singh A,Singh A,Suri S,et al.Adhesion strength-based,label-free isolation of human pluripotent stem cells.Nat Methods.2013;10(5):438-444.
[29]桑维维,常亚男,李娟.微流控芯片对乳腺癌细胞mda-mb-231的捕获及再培养研究[J].中国生物工程杂志,2015,35(6):46-53.
[30]Zhang Y,Wu M,Han X,et al.High-throughput,label-free isolation of cancer stem cells based on cell adhesion capacity.Angew Chem Int Ed Engl.2015;54(37):10838-10842.
[31]Chen W,Allen SG,Reka AK,et al.Nanoroughened adhesion-based capture of circulating tumor cells with heterogeneous expression and metastatic characteristics.BMC Cancer.2016;16:614-625.
[32]Dasanna AK,Schwarz US.Adhesion-based sorting of blood cells:an adhesive dynamics simulation study.Soft Matter.2018;14(44):9061-9070.
[33]Ermis M,Antmen E,Hasirci V.Micro and Nanofabrication methods to control cell-substrate interactions and cell behavior:A review from the tissue engineering perspective.Bioact Mater.2018;3(3):355-369.
[34]Francesco R,Simone B,Federica F,et al.A micron-scale surface topography design reducing cell adhesion to implanted materials.Sci Rep.2018;8(1):10887-10899.
[35]Zahran R,Rosales LJI,Rodríguez Valverde MA,et al.Effect of Hydrofluoric Acid Etching Time on Titanium Topography,Chemistry,Wettability,and Cell Adhesion.PLoS One.2016;11(11):e0165296.
[36]余劭婷,秦金桥,关国平,等.丝素纤维表面改性提高细胞黏附性能[J].生物医学工程学进展,2016,37(3):144-149.
[37]Tang Z,Akiyama Y,Itoga K,et al.Shear stress-dependent cell detachment from temperature-responsive cell culture surfaces in a microfluidic device.Biomaterials.2012;33(30):7405-7411.
[38]Hampe A,Li Z,Sethi S,et al.A Microfluidic Platform to Study Astrocyte Adhesion on Nanoporous Gold Thin Films.Nanomaterials.2018;8(7):452-463.
[39]Li P,Yu H,Liu N,et al.Visible Light Induced Electropolymerization of Suspended Hydrogel Bioscaffolds in a Microfluidic Chip.Biomater Sci.2018;6(6):1371-1378.
[40]Stamp ME,J?tten AM,Kudella PW,et al.Exploring the Limits of Cell Adhesion under Shear Stress within Physiological Conditions and beyond on a Chip.Diagnostics.2016;6(4):38-52.
[41]Gong X,Yao J,He H,et al.Combination of flow and micropattern alignment affecting flow-resistant endothelial cell adhesion.J Mech Behav Biomed Mater.2017;74:11-20.
[42]Vanessa K,Christoph G,Ivannikov D,et al.vasQchip:A Novel Microfluidic,Artificial Blood Vessel Scaffold for Vascularized3D Tissues.Adv MaterTechnol.2018;3(4):1700246.
[43]Sharmistha N,Kumar PA,Viswanathan K,et al.Controlled shear flow directs osteogenesis on UHMWPE based hybrid nano-biocomposites in custom designed PMMA microfluidic device.ACS Appl Bio Mater.2018;1(2):414-435.
[44]秦建华,张敏,于浩,等.人体器官芯片[J].中国科学院院刊,2017,32(12):18-26.
[45]Ahn S,Ardo?a HAM,Lind JU,et al.Mussel-inspired 3D fiber scaffolds for heart-on-a-chip toxicity studies of engineered nanomaterials.Anal Bioanal Chem.2018;410(24):6141-6154.
[46]Khazali AS,Clark AM,Wells A.A Pathway to Personalizing Therapy for Metastases Using Liver-on-a-Chip Platforms.Stem Cell Rev.2017;13(3):364-380.
[47]Humayun M,Chow CW,Ewk Y.Microfluidic lung airway-on-a-chip with arrayable suspended gels for studying epithelial and smooth muscle cell interactions.Lab Chip.2018;18(9):1298-1309.
[48]Wilmer MJ,Ng CP,Lanz HL,et al.Kidney-on-a-Chip Technology for Drug-Induced Nephrotoxicity Screening.Trends Biotechnol.2016;34(2):156-170.
[49]Jalili-Firoozinezhad S,Prantil-Baun R,Jiang A,et al.Modeling radiation injury-induced cell death and countermeasure drug responses in a human Gut-on-a-Chip.Cell Death Dis.2018;9(2):223-236.
[50]Kucukal E,Little JA,Gurkan UA.Shear dependent red blood cell adhesion in microscale flow.Integr Biol.2018;10(4):194-206.
[51]Kim M,Alapan Y,Adhikari A,et al.Hypoxia enhanced adhesion of red blood cells in microscale flow.Microcirculation.2017;24(5):e12374.
[52]Shea DJ,Li YW,Stebe KJ,et al.E-selectin-mediated rolling facilitates pancreatic cancer cell adhesion to hyaluronic acid.FASEB J.2017;31(11):5078-5086.
[53]Antoniellis Silveira AA,Dominical VM,Morelli Vital D,et al.Attenuation of TNF-induced neutrophil adhesion by simvastatin is associated with the inhibition of Rho-GTPase activity,p50 activity and morphological changes.Int Immunopharmacol.2018;58:160-165.