1932

Abstract

Many biochemical systems are spatially heterogeneous and exhibit nonlinear behaviors, such as state switching in response to small changes in the local concentration of diffusible molecules. Systems as varied as blood clotting, intracellular calcium signaling, and tissue inflammation are all heavily influenced by the balance of rates of reaction and mass transport phenomena including flow and diffusion. Transport of signaling molecules is also affected by geometry and chemoselective confinement via matrix binding. In this review, we use a phenomenon referred to as patchy switching to illustrate the interplay of nonlinearities, transport phenomena, and spatial effects. Patchy switching describes a change in the state of a network when the local concentration of a diffusible molecule surpasses a critical threshold. Using patchy switching as an example, we describe conceptual tools from nonlinear dynamics and chemical engineering that make testable predictions and provide a unifying description of the myriad possible experimental observations. We describe experimental microfluidic and biochemical tools emerging to test conceptual predictions by controlling transport phenomena and spatial distribution of diffusible signals, and we highlight the unmet need for in vivo tools.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-060815-014207
2017-06-20
2024-10-04
Loading full text...

Full text loading...

/deliver/fulltext/biochem/86/1/annurev-biochem-060815-014207.html?itemId=/content/journals/10.1146/annurev-biochem-060815-014207&mimeType=html&fmt=ahah

Literature Cited

  1. Tayalia P, Mooney DJ. 1.  2009. Controlled growth factor delivery for tissue engineering. Adv. Mater. 21:3269–85 [Google Scholar]
  2. Ehrbar M, Zeisberger SM, Raeber GP, Hubbell JA, Schnell C, Zisch AH. 2.  2008. The role of actively released fibrin-conjugated VEGF for VEGF receptor 2 gene activation and the enhancement of angiogenesis. Biomaterials 29:1720–29 [Google Scholar]
  3. Lee K, Silva EA, Mooney DJ. 3.  2011. Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. J. R. Soc. Interface 8:153–70 [Google Scholar]
  4. Martino MM, Hubbell JA. 4.  2010. The 12th-14th type III repeats of fibronectin function as a highly promiscuous growth factor-binding domain. FASEB J 24:4711–21 [Google Scholar]
  5. Dowd CJ, Cooney CL, Nugent MA. 5.  1999. Heparan sulfate mediates bFGF transport through basement membrane by diffusion with rapid reversible binding. J. Biol. Chem. 274:5236–44 [Google Scholar]
  6. Tyson JJ, Chen KC, Novak B. 6.  2003. Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr. Opin. Cell Biol. 15:221–31 [Google Scholar]
  7. Pickup M, Novitskiy S, Moses HL. 7.  2013. The roles of TGFβ in the tumour microenvironment. Nat. Rev. Cancer 13:788–99 [Google Scholar]
  8. Åström KJ, Murray R. 8.  2003. Feedback Systems: An Introduction for Scientists and Engineers Princeton, NJ: Princeton Univ. Press [Google Scholar]
  9. Phillips R, Kondev J, Theriot J. 9.  2008. Physical Biology of the Cell New York: Garland Science [Google Scholar]
  10. Fogelson AL, Neeves KB. 10.  2015. Fluid mechanics of blood clot formation. Annu. Rev. Fluid Mech. 47:377–403 [Google Scholar]
  11. Jesty J, Beltrami E. 11.  2005. Positive feedbacks of coagulation: their role in threshold regulation. Arterioscler. Thromb. Vasc. Biol. 25:2463–69 [Google Scholar]
  12. Mann KG, Brummel K, Butenas S. 12.  2003. What is all that thrombin for?. J. Thromb. Haemost. 1:1504–14 [Google Scholar]
  13. Rana K, Neeves KB. 13.  2016. Blood flow and mass transfer regulation of coagulation. Blood Rev 30:357–68 [Google Scholar]
  14. Epstein IR, Showalter K. 14.  1996. Nonlinear chemical dynamics: oscillations, patterns, and chaos. J. Phys. Chem. 100:13132–47 [Google Scholar]
  15. Turing AM. 15.  1952. The chemical basis of morphogenesis. Philos. Trans. R. Soc. B 237:37–72 [Google Scholar]
  16. Luss D, Sheintuch M. 16.  2005. Spatiotemporal patterns in catalytic systems. Catal. Today 105:254–74 [Google Scholar]
  17. Holmes EE, Lewis MA, Banks JE, Veit RR. 17.  1994. Partial differential equations in ecology: spatial interactions and population dynamics. Ecology 75:17–29 [Google Scholar]
  18. Okubo A, Levin SA. 18.  2001. Diffusion and Ecological Problems: Modern Perspectives New York: Springer [Google Scholar]
  19. Saltzman WM, Olbricht WL. 19.  2002. Building drug delivery into tissue engineering design. Nat. Rev. Drug Discov. 1:177–86 [Google Scholar]
  20. Bissell MJ, Hines WC. 20.  2011. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 17:320–29 [Google Scholar]
  21. Lu P, Weaver VM, Werb Z. 21.  2012. The extracellular matrix: a dynamic niche in cancer progression. J. Cell Biol. 196:395–406 [Google Scholar]
  22. Przybyla LM, Voldman J. 22.  2012. Attenuation of extrinsic signaling reveals the importance of matrix remodeling on maintenance of embryonic stem cell self-renewal. PNAS 109:835–40 [Google Scholar]
  23. Epstein IR. 23.  1995. The consequences of imperfect mixing in autocatalytic chemical and biological systems. Nature 374:321–27 [Google Scholar]
  24. Runyon MK, Kastrup CJ, Johnson-Kerner BL, Ha TG, Ismagilov RF. 24.  2008. Effects of shear rate on propagation of blood clotting determined using microfluidics and numerical simulations. J. Am. Chem. Soc. 130:3458–64 [Google Scholar]
  25. Kastrup CJ, Runyon MK, Shen F, Ismagilov RF. 25.  2006. Modular chemical mechanism predicts spatiotemporal dynamics of initiation in the complex network of hemostasis. PNAS 103:15747–52 [Google Scholar]
  26. Pompano RR, Li HW, Ismagilov RF. 26.  2008. Rate of mixing controls rate and outcome of autocatalytic processes: theory and microfluidic experiments with chemical reactions and blood coagulation. Biophys. J. 95:1531–43 [Google Scholar]
  27. Choi YY, Chung BG, Lee DH, Khademhosseini A, Kim JH, Lee SH. 27.  2010. Controlled-size embryoid body formation in concave microwell arrays. Biomaterials 31:4296–303 [Google Scholar]
  28. Bhatia SN, Balis UJ, Yarmush ML, Toner M. 28.  1999. Effect of cell–cell interactions in preservation of cellular phenotype: cocultivation of hepatocytes and nonparenchymal cells. FASEB J 13:1883–900 [Google Scholar]
  29. Xia Y, Whitesides GM. 29.  1998. Soft lithography. Annu. Rev. Mater. Sci. 28:153–84 [Google Scholar]
  30. Giovannucci DR, Bruce JIE, Straub SV, Arreola J, Sneyd J. 30.  et al. 2002. Cytosolic Ca2+ and Ca2+-activated Cl current dynamics: insights from two functionally distinct mouse exocrine cells. J. Physiol. 540:469–84 [Google Scholar]
  31. Chen Y-H, Peng C-C, Tung Y-C. 31.  2015. Flip channel: a microfluidic device for uniform-sized embryoid body formation and differentiation. Biomicrofluidics 9:054111 [Google Scholar]
  32. Przybyla LM, Theunissen TW, Jaenisch R, Voldman J. 32.  2013. Matrix remodeling maintains ESC self-renewal by activating Stat3. Stem Cells 31:1097–106 [Google Scholar]
  33. Kloxin AM, Kasko AM, Salinas CN, Anseth KS. 33.  2009. Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science 324:59–63 [Google Scholar]
  34. Tan CP, Seo BR, Brooks DJ, Chandler EM, Craighead HG, Fischbach C. 34.  2009. Parylene peel-off arrays to probe the role of cell–cell interactions in tumour angiogenesis. Integr. Biol. 1:587–94 [Google Scholar]
  35. Li CY, Wood DK, Hsu CM, Bhatia SN. 35.  2011. DNA-templated assembly of droplet-derived PEG microtissues. Lab Chip 11:2967–75 [Google Scholar]
  36. Robertus J, Browne WR, Feringa BL. 36.  2010. Dynamic control over cell adhesive properties using molecular-based surface engineering strategies. Chem. Soc. Rev. 39:354–78 [Google Scholar]
  37. Wu LY, Di Carlo D, Lee LP. 37  2008. Microfluidic self-assembly of tumor spheroids for anticancer drug discovery. Biomed. Microdevices 10:197–202 [Google Scholar]
  38. Yarmush ML, King KR. 38.  2009. Living-cell microarrays. Annu. Rev. Biomed. Eng 11:235–57 [Google Scholar]
  39. Zervantonakis IK, Kothapalli CR, Chung S, Sudo R, Kamm RD. 39.  2011. Microfluidic devices for studying heterotypic cell-cell interactions and tissue specimen cultures under controlled microenvironments. Biomicrofluidics 5:14 [Google Scholar]
  40. Lee GH, Lee JS, Wang X, Hoon Lee S. 40.  2016. Bottom-up engineering of well-defined 3D microtissues using microplatforms and biomedical applications. Adv. Healthc. Mater. 5:56–74 [Google Scholar]
  41. Albrecht DR, Underhill GH, Wassermann TB, Sah RL, Bhatia SN. 41.  2006. Probing the role of multicellular organization in three-dimensional microenvironments. Nat. Methods 3:369–75 [Google Scholar]
  42. Gu L, Mooney DJ. 42.  2016. Biomaterials and emerging anticancer therapeutics: engineering the microenvironment. Nat. Rev. Cancer 16:56–66 [Google Scholar]
  43. Murphy SV, Atala A. 43.  2014. 3D bioprinting of tissues and organs. Nat. Biotech. 32:773–85 [Google Scholar]
  44. Woolfson DN, Mahmoud ZN. 44.  2010. More than just bare scaffolds: towards multi-component and decorated fibrous biomaterials. Chem. Soc. Rev. 39:3464–79 [Google Scholar]
  45. Yin X, Mead BE, Safaee H, Langer R, Karp JM, Levy O. 45.  2016. Engineering stem cell organoids. Cell Stem Cell 18:25–38 [Google Scholar]
  46. Hwang YS, Chung BG, Ortmann D, Hattori N, Moeller HC, Khademhosseini A. 46.  2009. Microwell-mediated control of embryoid body size regulates embryonic stem cell fate via differential expression of WNT5a and WNT11. PNAS 106:16978–83 [Google Scholar]
  47. Lee LH, Peerani R, Ungrin M, Joshi C, Kumacheva E, Zandstra PW. 47.  2009. Micropatterning of human embryonic stem cells dissects the mesoderm and endoderm lineages. Stem Cell Res 2:155–62 [Google Scholar]
  48. Peerani R, Zandstra PW. 48.  2010. Enabling stem cell therapies through synthetic stem cell-niche engineering. J. Clin. Invest. 120:60–70 [Google Scholar]
  49. Sung KE, Yang N, Pehlke C, Keely PJ, Eliceiri KW. 49.  et al. 2011. Transition to invasion in breast cancer: A microfluidic in vitro model enables examination of spatial and temporal effects. Integr. Biol. 3:439–50 [Google Scholar]
  50. Chen D, Du WB, Liu Y, Liu WS, Kuznetsov A. 50.  et al. 2008. The chemistrode: a droplet-based microfluidic device for stimulation and recording with high temporal, spatial, and chemical resolution. PNAS 105:16843–48 [Google Scholar]
  51. Kaigala GV, Lovchik RD, Drechsler U, Delamarche E. 51.  2011. A vertical microfluidic probe. Langmuir 27:5686–93 [Google Scholar]
  52. Saha-Shah A, Green CM, Abraham DH, Baker LA. 52.  2016. Segmented flow sampling with push–pull theta pipettes. Analyst 141:1958–65 [Google Scholar]
  53. Ross AE, Belanger MC, Woodroof JF, Pompano RR. 53.  2017. Spatially resolved microfluidic stimulation of lymphoid tissue ex vivo. Analyst 142:649–59 [Google Scholar]
  54. Chang TC, Mikheev AM, Huynh W, Monnat RJ, Rostomily RC, Folch A. 54.  2014. Parallel microfluidic chemosensitivity testing on individual slice cultures. Lab Chip 14:4540–51 [Google Scholar]
  55. Huang Y, Williams JC, Johnson SM. 55.  2012. Brain slice on a chip: opportunities and challenges of applying microfluidic technology to intact tissues. Lab Chip 12:2103–17 [Google Scholar]
  56. Mohammed JS, Caicedo HH, Fall CP, Eddington DT. 56.  2008. Microfluidic add-on for standard electrophysiology chambers. Lab Chip 8:1048–55 [Google Scholar]
  57. Queval A, Ghattamaneni NR, Perrault CM, Gill R, Mirzaei M. 57.  et al. 2010. Chamber and microfluidic probe for microperfusion of organotypic brain slices. Lab Chip 10:326–34 [Google Scholar]
  58. Tang YT, Kim J, Lopez-Valdes HE, Brennan KC, Ju YS. 58.  2011. Development and characterization of a microfluidic chamber incorporating fluid ports with active suction for localized chemical stimulation of brain slices. Lab Chip 11:2247–54 [Google Scholar]
  59. Yi Y, Park J, Lim J, Lee CJ, Lee S-H. 59.  2015. Central nervous system and its disease models on a chip. Trends Biotechnol 33:762–76 [Google Scholar]
  60. Campenot RB. 60.  1977. Local control of neurite development by nerve growth factor. PNAS 74:4516–19 [Google Scholar]
  61. Tang YT, Mendez JM, Theriot JJ, Sawant PM, Lopez-Valdes HE. 61.  et al. 2014. Minimum conditions for the induction of cortical spreading depression in brain slices. J. Neurophysiol. 112:2572–79 [Google Scholar]
  62. Good MC, Zalatan JG, Lim WA. 62.  2011. Scaffold proteins: hubs for controlling the flow of cellular information. Science 332:680–86 [Google Scholar]
  63. Chen C-C, Wang L, Plikus MV, Jiang TX, Murray PJ. 63.  et al. 2015. Organ-level quorum sensing directs regeneration in hair stem cell populations. Cell 161:277–90 [Google Scholar]
  64. Kastrup CJ, Boedicker JQ, Pomerantsev AP, Moayeri M, Bian Y. 64.  et al. 2008. Spatial localization of bacteria controls coagulation of human blood by ‘quorum acting.’. Nat. Chem. Biol 4:742–50 [Google Scholar]
  65. Hui EE, Bhatia SN. 65.  2007. Micromechanical control of cell–cell interactions. PNAS 104:5722–26 [Google Scholar]
  66. Rosenthal A, Macdonald A, Voldman J. 66.  2007. Cell patterning chip for controlling the stem cell microenvironment. Biomaterials 28:3208–16 [Google Scholar]
  67. Lee WH, Ngernsutivorakul T, Mabrouk OS, Wong J-MT, Dugan CE. 67.  et al. 2016. Microfabrication and in vivo performance of a microdialysis probe with embedded membrane. Anal. Chem. 88:1230–37 [Google Scholar]
  68. Slaney TR, Nie J, Hershey ND, Thwar PK, Linderman J. 68.  et al. 2011. Push-pull perfusion sampling with segmented flow for high temporal and spatial resolution in vivo chemical monitoring. Anal. Chem. 83:5207–13 [Google Scholar]
  69. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S. 69.  et al. 2003. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:113–17 [Google Scholar]
  70. Kastrup CJ, Nahrendorf M, Figueiredo JL, Lee H, Kambhampati S. 70.  et al. 2012. Painting blood vessels and atherosclerotic plaques with an adhesive drug depot. PNAS 109:21444–49 [Google Scholar]
  71. Kolambkar YM, Dupont KM, Boerckel JD, Huebsch N, Mooney DJ. 71.  et al. 2011. An alginate-based hybrid system for growth factor delivery in the functional repair of large bone defects. Biomaterials 32:65–74 [Google Scholar]
  72. Mitragotri S, Burke PA, Langer R. 72.  2014. Overcoming the challenges in administering biopharmaceuticals: formulation and delivery strategies. Nat. Rev. Drug Discov. 13:655–72 [Google Scholar]
  73. Patterson J, Martino MM, Hubbell JA. 73.  2010. Biomimetic materials in tissue engineering. Mater. Today 13:14–22 [Google Scholar]
  74. Schoellhammer CM, Schroeder A, Maa R, Lauwers GY, Swiston A. 74.  et al. 2015. Ultrasound-mediated gastrointestinal drug delivery. Sci. Transl. Med. 7:310ra168 [Google Scholar]
  75. Borselli C, Storrie H, Benesch-Lee F, Shvartsman D, Cezar C. 75.  et al. 2010. Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. PNAS 107:3287–92 [Google Scholar]
  76. Furie B, Furie BC. 76.  2012. Formation of the clot. Thromb. Res. 130:Suppl. 1S44–46 [Google Scholar]
  77. Tischer D, Weiner OD. 77.  2014. Illuminating cell signalling with optogenetic tools. Nat. Rev. Mol. Cell Biol. 15:551–58 [Google Scholar]
  78. Peinado H, Lavotshkin S, Lyden D. 78.  2011. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin. Cancer Biol. 21:139–46 [Google Scholar]
  79. Dargan SL, Schwaller B, Parker I. 79.  2004. Spatiotemporal patterning of IP3-mediated Ca2+ signals in Xenopus oocytes by Ca2+-binding proteins. J. Physiol. 556:447–61 [Google Scholar]
  80. Ivanciu L, Stalker TJ. 80.  2015. Spatiotemporal regulation of coagulation and platelet activation during the hemostatic response in vivo. J. Thromb. Haemost. 13:1949–59 [Google Scholar]
  81. Griffith LG, Swartz MA. 81.  2006. Capturing complex 3D tissue physiology in vitro. Nat. Rev. Mol. Cell Biol. 7:211–24 [Google Scholar]
  82. Proudfoot AEI. 82.  2006. The biological relevance of chemokine–proteoglycan interactions. Biochem. Soc. Trans. 34:422–26 [Google Scholar]
  83. Swartz MA, Fleury ME. 83.  2007. Interstitial flow and its effects in soft tissues. Annu. Rev. Biomed. Eng 9:229–56 [Google Scholar]
  84. Magzoub M, Jin S, Verkman AS. 84.  2008. Enhanced macromolecule diffusion deep in tumors after enzymatic digestion of extracellular matrix collagen and its associated proteoglycan decorin. FASEB J 22:276–84 [Google Scholar]
  85. Kim J, Cao L, Shvartsman D, Silva EA, Mooney DJ. 85.  2011. Targeted delivery of nanoparticles to ischemic muscle for imaging and therapeutic angiogenesis. Nano Lett 11:694–700 [Google Scholar]
  86. Dityatev A, Seidenbecher CI, Schachner M. 86.  2010. Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci 33:503–12 [Google Scholar]
  87. Sykova E, Nicholson C. 87.  2008. Diffusion in brain extracellular space. Physiol. Rev. 88:1277–340 [Google Scholar]
  88. Chauhan VP, Lanning RM, Diop-Frimpong B, Mok W, Brown EB. 88.  et al. 2009. Multiscale measurements distinguish cellular and interstitial hindrances to diffusion in vivo. Biophys. J. 97:330–36 [Google Scholar]
  89. Netti PA, Berk DA, Swartz MA, Grodzinsky AJ, Jain RK. 89.  2000. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 60:2497–503 [Google Scholar]
  90. Khanvilkar K, Donovan MD, Flanagan DR. 90.  2001. Drug transfer through mucus. Adv. Drug Deliv. Rev. 48:173–93 [Google Scholar]
  91. Stewart PS. 91.  2003. Diffusion in biofilms. J. Bacteriol. 185:1485–91 [Google Scholar]
  92. Ward KW. 92.  2008. A review of the foreign-body response to subcutaneously-implanted devices: The role of macrophages and cytokines in biofouling and fibrosis. J. Diabetes Sci. Technol. 2:768–77 [Google Scholar]
  93. Sachlos E, Auguste DT. 93.  2008. Embryoid body morphology influences diffusive transport of inductive biochemicals: a strategy for stem cell differentiation. Biomaterials 29:4471–80 [Google Scholar]
  94. Hynes RO. 94.  2009. The extracellular matrix: not just pretty fibrils. Science 326:1216–19 [Google Scholar]
  95. Francavilla C, Papetti M, Rigbolt KT, Pedersen AK, Sigurdsson JO. 95.  et al. 2016. Multilayered proteomics reveals molecular switches dictating ligand-dependent EGFR trafficking. Nat. Struct. Mol. Biol. 23:608–18 [Google Scholar]
  96. Dona E, Barry JD, Valentin G, Quirin C, Khmelinskii A. 96.  et al. 2013. Directional tissue migration through a self-generated chemokine gradient. Nature 503:285–89 [Google Scholar]
  97. Dai E, Liu LY, Wang H, McIvor D, Sun YM. 97.  et al. 2010. Inhibition of chemokine-glycosaminoglycan interactions in donor tissue reduces mouse allograft vasculopathy and transplant rejection. PLOS ONE 5:e10510 [Google Scholar]
  98. Proudfoot AEI, Handel TM, Johnson Z, Lau EK, LiWang P. 98.  et al. 2003. Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. PNAS 100:1885–90 [Google Scholar]
  99. Brown JM, Xia J, Zhuang B, Cho KS, Rogers CJ. 99.  et al. 2012. A sulfated carbohydrate epitope inhibits axon regeneration after injury. PNAS 109:4768–73 [Google Scholar]
  100. Custodio CA, Reis RL, Mano JF. 100.  2014. Engineering biomolecular microenvironments for cell instructive biomaterials. Adv. Healthc. Mater. 3:797–810 [Google Scholar]
  101. Martino MM, Tortelli F, Mochizuki M, Traub S, Ben-David D. 101.  et al. 2011. Engineering the growth factor microenvironment with fibronectin domains to promote wound and bone tissue healing. Sci. Transl. Med. 3:100ra89 [Google Scholar]
  102. Das RK, Zouani OF. 102.  2014. A review of the effects of the cell environment physicochemical nanoarchitecture on stem cell commitment. Biomaterials 35:5278–93 [Google Scholar]
  103. Wong AP, Perez-Castillejos R, Christopher Love J, Whitesides GM. 103.  2008. Partitioning microfluidic channels with hydrogel to construct tunable 3-D cellular microenvironments. Biomaterials 29:1853–61 [Google Scholar]
  104. Tien J, Nelson CM. 104.  2014. Microstructured extracellular matrices in tissue engineering and development: an update. Ann. Biomed. Eng 42:1413–23 [Google Scholar]
  105. Chen S, Lee LP. 105.  2010. Non-invasive microfluidic gap junction assay. Integr. Biol. 2:130–38 [Google Scholar]
  106. Chan V, Novakowski SK, Law S, Klein-Bosgoed C, Kastrup CJ. 106.  2015. Controlled transcription of exogenous mRNA in platelets using protocells. Angew. Chem. Int. Ed. Engl. 54:13590–93 [Google Scholar]
  107. Lizana L, Bauer B, Orwar O. 107.  2008. Controlling the rates of biochemical reactions and signaling networks by shape and volume changes. PNAS 105:4099–104 [Google Scholar]
  108. Gorris HH, Walt DR. 108.  2010. Analytical chemistry on the femtoliter scale. Angew. Chem. Int. Ed. Engl. 49:3880–95 [Google Scholar]
  109. Vincent ME, Liu WS, Haney EB, Ismagilov RF. 109.  2010. Microfluidic stochastic confinement enhances analysis of rare cells by isolating cells and creating high density environments for control of diffusible signals. Chem. Soc. Rev. 39:974–84 [Google Scholar]
  110. Weitz M, Mückl A, Kapsner K, Berg R, Meyer A, Simmel FC. 110.  2014. Communication and computation by bacteria compartmentalized within microemulsion droplets. J. Am. Chem. Soc. 136:72–75 [Google Scholar]
  111. Boedicker JQ, Vincent ME, Ismagilov RF. 111.  2009. Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew. Chem. Int. Ed. Engl. 48:5908–11 [Google Scholar]
  112. Connell JL, Wessel AK, Parsek MR, Ellington AD, Whiteley M, Shear JB. 112.  2010. Probing prokaryotic social behaviors with bacterial “lobster traps.”. mBio 1:e00202–10 [Google Scholar]
  113. Carnes EC, Lopez DM, Donegan NP, Cheung A, Gresham H. 113.  et al. 2010. Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nat. Chem. Biol. 6:41–45 [Google Scholar]
  114. Hagen SJ, Son M, Weiss JT, Young JH. 114.  2010. Bacterium in a box: sensing of quorum and environment by the LuxI/LuxR gene regulatory circuit. J. Biol. Phys. 36:317–27 [Google Scholar]
  115. Luthuli BB, Purdy GE, Balagadde FK. 115.  2015. Confinement-induced drug-tolerance in mycobacteria mediated by an efflux mechanism. PLOS ONE 10:e0136231 [Google Scholar]
  116. Yu HM, Meyvantsson I, Shkel IA, Beebe DJ. 116.  2005. Diffusion dependent cell behavior in microenvironments. Lab Chip 5:1089–95 [Google Scholar]
  117. Tschumperlin DJ, Dai G, Maly IV, Kikuchi T, Laiho LH. 117.  et al. 2004. Mechanotransduction through growth-factor shedding into the extracellular space. Nature 429:83–86 [Google Scholar]
  118. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG. 118.  et al. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469:415–18 [Google Scholar]
  119. Magliozzi R, Howell O, Vora A, Serafini B, Nicholas R. 119.  et al. 2007. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain 130:1089–104 [Google Scholar]
  120. Park S, Wolanin PM, Yuzbashyan EA, Silberzan P, Stock JB, Austin RH. 120.  2003. Motion to form a quorum. Science 301:188 [Google Scholar]
  121. Ribbe J, Maier B. 121.  2016. Density-dependent differentiation of bacteria in spatially structured open systems. Biophys. J. 110:1648–60 [Google Scholar]
  122. Shen F, Pompano RR, Kastrup CJ, Ismagilov RF. 122.  2009. Confinement regulates complex biochemical networks: initiation of blood clotting by “diffusion acting.”. Biophys. J. 97:2137–45 [Google Scholar]
  123. Hathcock JJ. 123.  2006. Flow effects on coagulation and thrombosis. Arterioscler. Thromb. Vasc. Biol. 26:1729–37 [Google Scholar]
  124. Wyffels K, Kaanders J, Rijken P, Bussink J, van den Hoogen FJA. 124.  et al. 2000. Vascular architecture and hypoxic profiles in human head and neck squamous cell carcinomas. Br. J. Cancer 83:674–83 [Google Scholar]
  125. Kuo JS, Chiu DT. 125.  2011. Controlling mass transport in microfluidic devices. Annu. Rev. Anal. Chem. 4:275–96 [Google Scholar]
  126. Okorie UM, Denney WS, Chatterjee MS, Neeves KB, Diamond SL. 126.  2008. Determination of surface tissue factor thresholds that trigger coagulation at venous and arterial shear rates: amplification of 100 fM circulating tissue factor requires flow. Blood 111:3507–13 [Google Scholar]
  127. Shen F, Kastrup CJ, Liu Y, Ismagilov RF. 127.  2008. Threshold response of initiation of blood coagulation by tissue factor in patterned microfluidic capillaries is controlled by shear rate. Arterioscler. Thromb. Vasc. Biol. 28:2035–41 [Google Scholar]
  128. Alonzo LF, Moya ML, Shirure VS, George SC. 128.  2015. Microfluidic device to control interstitial flow-mediated homotypic and heterotypic cellular communication. Lab Chip 15:3521–29 [Google Scholar]
  129. Choi NW, Cabodi M, Held B, Gleghorn JP, Bonassar LJ, Stroock AD. 129.  2007. Microfluidic scaffolds for tissue engineering. Nat. Mater. 6:908–15 [Google Scholar]
  130. Bonvin C, Overney J, Shieh AC, Dixon JB, Swartz MA. 130.  2010. A multichamber fluidic device for 3D cultures under interstitial flow with live imaging: development, characterization, and applications. Biotechnol. Bioeng. 105:982–91 [Google Scholar]
  131. Baylis JR, Yeon JH, Thomson MH, Kazerooni A, Wang X. 131.  et al. 2015. Self-propelled particles that transport cargo through flowing blood and halt hemorrhage. Sci. Adv. 1:e1500379 [Google Scholar]
  132. Gao W, Dong R, Thamphiwatana S, Li J, Gao W. 132.  et al. 2015. Artificial micromotors in the mouse's stomach: a step toward in vivo use of synthetic motors. ACS Nano 9:117–23 [Google Scholar]
  133. Srivastava SK, Medina-Sanchez M, Koch B, Schmidt OG. 133.  2016. Medibots: dual-action biogenic microdaggers for single-cell surgery and drug release. Adv. Mater. 28:832–37 [Google Scholar]
  134. Schmitz ML, Weber A, Roxlau T, Gaestel M, Kracht M. 134.  2011. Signal integration, crosstalk mechanisms and networks in the function of inflammatory cytokines. Biochim. Biophys. Acta Mol. Cell Res. 1813:2165–75 [Google Scholar]
  135. Vaday GG, Lider O. 135.  2000. Extracellular matrix moieties, cytokines, and enzymes: dynamic effects on immune cell behavior and inflammation. J. Leukoc. Biol. 67:149–59 [Google Scholar]
  136. Lassmann H. 136.  2011. Review: the architecture of inflammatory demyelinating lesions: implications for studies on pathogenesis. Neuropathol. Appl. Neurobiol. 37:698–710 [Google Scholar]
  137. Gao HM, Hong JS. 137.  2008. Why neurodegenerative diseases are progressive: Uncontrolled inflammation drives disease progression. Trends Immunol 29:357–65 [Google Scholar]
  138. Akassoglou K, Adams RA, Bauer J, Mercado P, Tseveleki V. 138.  et al. 2004. Fibrin depletion decreases inflammation and delays the onset of demyelination in a tumor necrosis factor transgenic mouse model for multiple sclerosis. PNAS 101:6698–703 [Google Scholar]
  139. Marik C, Felts PA, Bauer J, Lassmann H, Smith KJ. 139.  2007. Lesion genesis in a subset of patients with multiple sclerosis: a role for innate immunity?. Brain 130:2800–15 [Google Scholar]
  140. van der Valk P, Amor S. 140.  2009. Preactive lesions in multiple sclerosis. Curr. Opin. Neurol. 22:207–13 [Google Scholar]
  141. Bhatia SN, Ingber DE. 141.  2014. Microfluidic organs-on-chips. Nat. Biotech. 32:760–72 [Google Scholar]
  142. Choi CK, Breckenridge MT, Chen CS. 142.  2010. Engineered materials and the cellular microenvironment: a strengthening interface between cell biology and bioengineering. Trends Cell Biol 20:705–14 [Google Scholar]
  143. Wang M, Hershey ND, Mabrouk OS, Kennedy RT. 143.  2011. Collection, storage, and electrophoretic analysis of nanoliter microdialysis samples collected from awake animals in vivo. Anal. Bioanal. Chem. 400:2013–23 [Google Scholar]
  144. Cepeda DE, Hains L, Li D, Bull J, Lentz SI, Kennedy RT. 144.  2015. Experimental evaluation and computational modeling of tissue damage from low-flow push–pull perfusion sampling in vivo. J. Neurosci. Methods 242:97–105 [Google Scholar]
  145. Bucher ES, Wightman RM. 145.  2015. Electrochemical analysis of neurotransmitters. Annu. Rev. Anal. Chem. 8:239–61 [Google Scholar]
  146. Andersson U, Tracey KJ. 146.  2012. Neural reflexes in inflammation and immunity. J. Exp. Med. 209:1057–68 [Google Scholar]
  147. Germain RN, Robey EA, Cahalan MD. 147.  2012. A decade of imaging cellular motility and interaction dynamics in the immune system. Science 336:1676–81 [Google Scholar]
  148. Reynolds F, Kelly KA. 148.  2011. Techniques for molecular imaging probe design. Mol. Imaging 10:407–19 [Google Scholar]
  149. Porterfield WB, Prescher JA. 149.  2015. Tools for visualizing cell–cell ‘interactomes.’. Curr. Opin. Chem. Biol 24:121–30 [Google Scholar]
  150. Shapiro MG, Goodwill PW, Neogy A, Yin M, Foster FS. 150.  et al. 2014. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat. Nanotechnol. 9:311–16 [Google Scholar]
  151. Shapiro MG, Ramirez RM, Sperling LJ, Sun G, Sun J. 151.  et al. 2014. Genetically encoded reporters for hyperpolarized xenon magnetic resonance imaging. Nat. Chem. 6:629–34 [Google Scholar]
  152. Crosetto N, Bienko M, van Oudenaarden A. 152.  2015. Spatially resolved transcriptomics and beyond. Nat. Rev. Genet. 16:57–66 [Google Scholar]
  153. Miesenbock G. 153.  2009. The optogenetic catechism. Science 326:395–99 [Google Scholar]
  154. Ryu KA, Stutts L, Tom JK, Mancini RJ, Esser-Kahn AP. 154.  2014. Stimulation of innate immune cells by light-activated TLR7/8 agonists. J. Am. Chem. Soc. 136:10823–25 [Google Scholar]
  155. Bansal A, Zhang Y. 155.  2014. Photocontrolled nanoparticle delivery systems for biomedical applications. Acc. Chem. Res. 47:3052–60 [Google Scholar]
  156. Aryal M, Arvanitis CD, Alexander PM, McDannold N. 156.  2014. Ultrasound-mediated blood–brain barrier disruption for targeted drug delivery in the central nervous system. Adv. Drug Deliv. Rev. 72:94–109 [Google Scholar]
  157. Jeong J-W, McCall JG, Shin G, Zhang Y, Al-Hasani R. 157.  et al. 2015. Wireless optofluidic systems for programmable in vivo pharmacology and optogenetics. Cell 162:662–74 [Google Scholar]
  158. Purwada A, Jaiswal MK, Ahn H, Nojima T, Kitamura D. 158.  et al. 2015. Ex vivo engineered immune organoids for controlled germinal center reactions. Biomaterials 63:24–34 [Google Scholar]
  159. Singh A, Peppas NA. 159.  2014. Hydrogels and scaffolds for immunomodulation. Adv. Mater. 26:6530–41 [Google Scholar]
  160. Farra R, Sheppard NF Jr., McCabe L, Neer RM, Anderson JM. 160.  et al. 2012. First-in-human testing of a wirelessly controlled drug delivery microchip. Sci. Transl. Med. 4:122ra21 [Google Scholar]
  161. Chang A, Smith MC, Yin XH, Fox RJ, Staugaitis SM, Trapp BD. 161.  2008. Neurogenesis in the chronic lesions of multiple sclerosis. Brain 131:2366–75 [Google Scholar]
/content/journals/10.1146/annurev-biochem-060815-014207
Loading
/content/journals/10.1146/annurev-biochem-060815-014207
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error