1932

Abstract

Visualizing and modulating molecular and cellular processes occurring deep within living organisms is fundamental to our study of basic biology and disease. Currently, the most sophisticated tools available to dynamically monitor and control cellular events rely on light-responsive proteins, which are difficult to use outside of optically transparent model systems, cultured cells, or surgically accessed regions owing to strong scattering of light by biological tissue. In contrast, ultrasound is a widely used medical imaging and therapeutic modality that enables the observation and perturbation of internal anatomy and physiology but has historically had limited ability to monitor and control specific cellular processes. Recent advances are beginning to address this limitation through the development of biomolecular tools that allow ultrasound to connect directly to cellular functions such as gene expression. Driven by the discovery and engineering of new contrast agents, reporter genes, and bioswitches, the nascent field of biomolecular ultrasound carries a wave of exciting opportunities.

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2018-06-07
2024-04-16
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Literature Cited

  1. 1.  Szabo TL 2004. Diagnostic Ultrasound Imaging: Inside Out Cambridge, MA: Academic
  2. 2.  Azhari H 2010. Basics of Biomedical Ultrasound for Engineers Hoboken, NJ: John Wiley & Sons
  3. 3.  Cobbold RS 2006. Foundations of Biomedical Ultrasound Oxford, UK: Oxford Univ. Press
  4. 4.  Liang H-D, Noble JA, Wells PNT 2011. Recent advances in biomedical ultrasonic imaging techniques. Interface Focus 1:475–76
    [Google Scholar]
  5. 5.  Powers J, Kremkau F 2011. Medical ultrasound systems. Interface Focus 1:477–89
    [Google Scholar]
  6. 6.  Foster FS, Pavlin CJ, Harasiewicz KA, Christopher DA, Turnbull DH 2000. Advances in ultrasound biomicroscopy. Ultrasound Med. Biol. 26:1–27
    [Google Scholar]
  7. 7.  Evans DH, Jensen JA, Nielsen MB 2011. Ultrasonic colour Doppler imaging. Interface Focus 1:490–502
    [Google Scholar]
  8. 8.  Rubin JM, Bude RO, Carson PL, Bree RL, Adler RS 1994. Power Doppler US: a potentially useful alternative to mean frequency-based color Doppler US. Radiology 190:853–56
    [Google Scholar]
  9. 9.  Ferrara K, Pollard R, Borden M 2007. Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annu. Rev. Biomed. Eng. 9:415–47
    [Google Scholar]
  10. 10.  Paefgen V, Doleschel D, Kiessling F 2015. Evolution of contrast agents for ultrasound imaging and ultrasound-mediated drug delivery. Front. Pharmacol. 6:197
    [Google Scholar]
  11. 11.  Unnikrishnan S, Klibanov AL 2012. Microbubbles as ultrasound contrast agents for molecular imaging: preparation and application. Am. J. Roentgenol. 199:292–99
    [Google Scholar]
  12. 12.  Frinking PJA, Bouakaz A, Kirkhorn J, Ten Cate FJ, de Jong N 2000. Ultrasound contrast imaging: current and new potential methods. Ultrasound Med. Biol. 26:965–75
    [Google Scholar]
  13. 13.  Mor-Avi V, Caiani EG, Collins KA, Korcarz CE, Bednarz JE, Lang RM 2001. Combined assessment of myocardial perfusion and regional left ventricular function by analysis of contrast-enhanced power modulation images. Circulation 104:352–57
    [Google Scholar]
  14. 14.  Simpson DH, Chin CT, Burns PN 1999. Pulse inversion Doppler: a new method for detecting nonlinear echoes from microbubble contrast agents. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 46:372–82
    [Google Scholar]
  15. 15.  Tanter M, Fink M 2014. Ultrafast imaging in biomedical ultrasound. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 61:102–19
    [Google Scholar]
  16. 16.  Mace E, Montaldo G, Osmanski BF, Cohen I, Fink M, Tanter M 2013. Functional ultrasound imaging of the brain: theory and basic principles. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60:492–506
    [Google Scholar]
  17. 17.  Mace E, Montaldo G, Cohen I, Baulac M, Fink M, Tanter M 2011. Functional ultrasound imaging of the brain. Nat. Methods 8:662–64
    [Google Scholar]
  18. 18.  Errico C, Pierre J, Pezet S, Desailly Y, Lenkei Z et al. 2015. Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging. Nature 527:499–502
    [Google Scholar]
  19. 19.  Lin F, Shelton SE, Espíndola D, Rojas JD, Pinton G, Dayton PA 2017. 3-D ultrasound localization microscopy for identifying microvascular morphology features of tumor angiogenesis at a resolution beyond the diffraction limit of conventional ultrasound. Theranostics 7:196–204
    [Google Scholar]
  20. 20.  Hynynen K, Darkazanli A, Unger E, Schenck JF 1993. MRI-guided noninvasive ultrasound surgery. Med. Phys. 20:107–15
    [Google Scholar]
  21. 21.  Hynynen K, Clement GT, McDannold N, Vykhodtseva N, King R et al. 2004. 500-Element ultrasound phased array system for noninvasive focal surgery of the brain: a preliminary rabbit study with ex vivo human skulls. Magn. Reson. Med. 52:100–7
    [Google Scholar]
  22. 22.  O'Brien WD 2007. Ultrasound-biophysics mechanisms. Prog. Biophys. Mol. Biol. 93:212–55
    [Google Scholar]
  23. 23.  Sarvazyan AP, Rudenko OV, Nyborg WL 2010. Biomedical applications of radiation force of ultrasound: historical roots and physical basis. Ultrasound Med. Biol. 36:1379–94
    [Google Scholar]
  24. 24.  Coussios CC, Roy RA 2008. Applications of acoustics and cavitation to noninvasive therapy and drug delivery. Annu. Rev. Fluid Mech. 40:395–420
    [Google Scholar]
  25. 25.  Jolesz FA, Hynynen K, McDannold N, Tempany C 2005. MR imaging-controlled focused ultrasound ablation: a noninvasive image-guided surgery. Magn. Reson. Imaging Clin. N. Am. 13:545–60
    [Google Scholar]
  26. 26.  Hesley GK, Gorny KR, Woodrum DA 2013. MR-guided focused ultrasound for the treatment of uterine fibroids. Cardiovasc. Interv. Radiol. 36:5–13
    [Google Scholar]
  27. 27.  Uchida T, Nakano M, Hongo S, Shoji S, Nagata Y et al. 2012. High-intensity focused ultrasound therapy for prostate cancer. Int. J. Urol. 19:187–201
    [Google Scholar]
  28. 28.  Illing RO, Kennedy JE, Wu F, ter Haar GR, Protheroe AS et al. 2005. The safety and feasibility of extracorporeal high-intensity focused ultrasound (HIFU) for the treatment of liver and kidney tumours in a Western population. Br. J. Cancer 93:890–95
    [Google Scholar]
  29. 29.  Carpentier A, Canney M, Vignot A, Reina V, Beccaria K et al. 2016. Clinical trial of blood-brain barrier disruption by pulsed ultrasound. Sci. Transl. Med. 8:343re2
    [Google Scholar]
  30. 30.  Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA 2001. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 220:640–46
    [Google Scholar]
  31. 31.  Machet L, Boucaud A 2002. Phonophoresis: efficiency, mechanisms and skin tolerance. Int. J. Pharm. 243:1–15
    [Google Scholar]
  32. 32.  Bader KB, Bouchoux G, Holland CK 2016. Sonothrombolysis. Adv. Exp. Med. Biol. 880:339–62
    [Google Scholar]
  33. 33.  Mason T, Lorimer J 2002. Applied Sonochemistry Weinheim, Ger: Wiley-VCH Verlag
  34. 34.  Brand S, Weiss EC, Lemor RM, Kolios MC 2008. High frequency ultrasound tissue characterization and acoustic microscopy of intracellular changes. Ultrasound Med. Biol. 34:1396–407
    [Google Scholar]
  35. 35.  Shapiro MG, Goodwill PW, Neogy A, Yin M, Foster FS et al. 2014. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat. Nanotechnol. 9:311–16
    [Google Scholar]
  36. 36.  Bowen C, Jensen T 1965. Blue-green algae: fine structure of the gas vacuoles. Science 147:1460–62
    [Google Scholar]
  37. 37.  Klebahn H 1895. Gasvakuolen, ein Bastendteil der Zellen der wasserblutenbildenden Phycochromaceen. Flora 80:241–82
    [Google Scholar]
  38. 38.  Walsby A 1994. Gas vesicles. Microbiol. Rev. 58:94–144
    [Google Scholar]
  39. 39.  Pfeifer F 2012. Distribution, formation and regulation of gas vesicles. Nat. Rev. Microbiol. 10:705–15
    [Google Scholar]
  40. 40.  Ezzeldin HM, Klauda JB, Solares SD 2012. Modeling of the major gas vesicle protein, GvpA: from protein sequence to vesicle wall structure. J. Struct. Biol. 179:18–28
    [Google Scholar]
  41. 41.  Walsby AA, Revsbech NP, Grieffel DH 1992. The gas permeability coefficient of the cyanobacterial gas vesicle wall. J. Gen. Microbiol. 138:837–45
    [Google Scholar]
  42. 42.  Lakshmanan A, Lu GJ, Farhadi A, Nety SP, Kunth M et al. 2017. Preparation of biogenic gas vesicle nanostructures for use as contrast agents for ultrasound and MRI. Nat. Protoc. 12:2050
    [Google Scholar]
  43. 43.  Lakshmanan A, Farhadi A, Nety SP, Lee-Gosselin A, Bourdeau RW et al. 2016. Molecular engineering of acoustic protein nanostructures. ACS Nano 10:7314–22
    [Google Scholar]
  44. 44.  Cherin E, Melis JM, Bourdeau RW, Yin M, Kochmann DM et al. Acoustic behavior of Halobacterium salinarum gas vesicles in the high-frequency range: experiments and modeling. Ultrasound Med. Biol. 43:1016–30
    [Google Scholar]
  45. 45.  Maresca D, Lakshmanan A, Lee-Gosselin A, Melis JM, Ni Y-L et al. 2017. Nonlinear ultrasound imaging of nanoscale acoustic biomolecules. Appl. Phys. Lett. 110:073704
    [Google Scholar]
  46. 46.  Bourdeau RW, Lee-Gosselin A, Lakshmanan A, Farhadi A, Kumar SR et al. 2018. Acoustic reporter genes for non-invasive imaging of microbes in mammalian hosts. Nature 553:86–90
    [Google Scholar]
  47. 47.  Stuart ES, Morshed F, Sremac M, DasSarma S 2004. Cassette-based presentation of SIV epitopes with recombinant gas vesicles from halophilic archaea. J. Biotechnol. 114:225–37
    [Google Scholar]
  48. 48.  Offner S, Wanner G, Pfeifer F 1996. Functional studies of the gvpACNO operon of Halobacterium salinarium reveal that the GvpC protein shapes gas vesicles. J. Bacteriol. 178:2071–78
    [Google Scholar]
  49. 49.  Offner S, Ziese U, Wanner G, Typke D, Pfeifer F 1998. Structural characteristics of halobacterial gas vesicles. Microbiology 144:1331–42
    [Google Scholar]
  50. 50.  Strunk T, Hamacher K, Hoffgaard F, Engelhardt H, Zillig MD et al. 2011. Structural model of the gas vesicle protein GvpA and analysis of GvpA mutants in vivo. . Mol. Microbiol. 81:56–68
    [Google Scholar]
  51. 51.  Li N, Cannon MC 1998. Gas vesicle genes identified in Bacillus megaterium and functional expression in Escherichia coli. . J. Bacteriol. 180:2450–58
    [Google Scholar]
  52. 52.  Bartelle BB, Berrios-Otero CA, Rodriguez JJ, Friedland AE, Aristizábal O, Turnbull DH 2012. Novel genetic approach for in vivo vascular imaging in mice. Circ. Res. 110:938–47
    [Google Scholar]
  53. 53.  Olson ES, Orozco J, Wu Z, Malone CD, Yi B et al. 2013. Toward in vivo detection of hydrogen peroxide with ultrasound molecular imaging. Biomaterials 34:8918–24
    [Google Scholar]
  54. 54.  Malone CD, Yeh Y, Esener S, Mattrey R, Hoyt K 2016. Ultrasound characterization of oxygen contrast agents produced during the reaction of hydrogen peroxide with catalase-loaded nanoparticles. Proc. Ultrason. Symp., Tours, Fr.1–4 New York: IEEE Int.
    [Google Scholar]
  55. 55.  Sheeran PS, Luois SH, Mullin LB, Matsunaga TO, Dayton PA 2012. Design of ultrasonically-activatable nanoparticles using low boiling point perfluorocarbons. Biomaterials 33:3262–69
    [Google Scholar]
  56. 56.  Leung TK, Rajendran MY, Monfries C, Hall C, Lim L 1990. The human heat-shock protein family. Expression of a novel heat-inducible HSP70 (HSP70B') and isolation of its cDNA and genomic DNA. Biochem. J. 267:125–32
    [Google Scholar]
  57. 57.  Dhaka A, Viswanath V, Patapoutian A 2006. TRP ion channels and temperature sensation. Annu. Rev. Neurosci. 29:135–61
    [Google Scholar]
  58. 58.  Hoynes-O'Connor A, Hinman K, Kirchner L, Moon TS 2015. De novo design of heat-repressible RNA thermosensors in E. coli. Nucleic Acids Res 43:6166–79
    [Google Scholar]
  59. 59.  Valdez-Cruz NA, Caspeta L, Pérez NO, Ramírez OT, Trujillo-Roldán MA 2010. Production of recombinant proteins in E. coli by the heat inducible expression system based on the phage lambda pL and/or pR promoters. Microb. Cell Fact. 9:18
    [Google Scholar]
  60. 60.  Hurme R, Berndt KD, Normark SJ, Rhen M 1997. A proteinaceous gene regulatory thermometer in Salmonella. . Cell 90:55–64
    [Google Scholar]
  61. 61.  Madio DP, van Gelderen P, DesPres D, Olson AW, de Zwart JA et al. 1998. On the feasibility of MRI-guided focused ultrasound for local induction of gene expression. J. Magnet. Reson. Imaging 8:101–4
    [Google Scholar]
  62. 62.  Braiden V, Ohtsuru A, Kawashita Y, Miki F, Sawada T et al. 2000. Eradication of breast cancer xenografts by hyperthermic suicide gene therapy under the control of the heat shock protein promoter. Hum. Gene Ther. 11:2453–63
    [Google Scholar]
  63. 63.  Xiong X, Sun Y, Sattiraju A, Jung Y, Mintz A et al. 2015. Remote spatiotemporally controlled and biologically selective permeabilization of blood-brain barrier. J. Control. Release 217:113–20
    [Google Scholar]
  64. 64.  Deckers R, Quesson B, Arsaut J, Eimer S, Couillaud F, Moonen CT 2009. Image-guided, noninvasive, spatiotemporal control of gene expression. PNAS 106:1175–80
    [Google Scholar]
  65. 65.  Guilhon E, Voisin P, de Zwart JA, Quesson B, Salomir R et al. 2003. Spatial and temporal control of transgene expression in vivo using a heat-sensitive promoter and MRI-guided focused ultrasound. J. Gene Med. 5:333–42
    [Google Scholar]
  66. 66.  Anckar J, Sistonen L 2011. Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu. Rev. Biochem. 80:1089–115
    [Google Scholar]
  67. 67.  Batulan Z, Shinder GA, Minotti S, He BP, Doroudchi MM et al. 2003. High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. J. Neurosci. 23:5789–98
    [Google Scholar]
  68. 68.  Oehler R, Pusch E, Zellner M, Dungel P, Hergovics N et al. 2001. Cell type-specific variations in the induction of hsp70 in human leukocytes by feverlike whole body hyperthermia. Cell Stress Chaperones 6:306–15
    [Google Scholar]
  69. 69.  de Marco A, Vigh L, Diamant S, Goloubinoff P 2005. Native folding of aggregation-prone recombinant proteins in Escherichia coli by osmolytes, plasmid- or benzyl alcohol–overexpressed molecular chaperones. Cell Stress Chaperones 10:329–39
    [Google Scholar]
  70. 70.  Zhao K, Liu M, Burgess RR 2005. The global transcriptional response of Escherichia coli to induced σ32 protein involves σ32 regulon activation followed by inactivation and degradation of σ32in vivo. . J. Biol. Chem. 280:17758–68
    [Google Scholar]
  71. 71.  Piraner DI, Abedi MH, Moser BA, Lee-Gosselin A, Shapiro MG 2017. Tunable thermal bioswitches for in vivo control of microbial therapeutics. Nat. Chem. Biol. 13:75–80
    [Google Scholar]
  72. 72.  Stanley SA, Sauer J, Kane RS, Dordick JS, Friedman JM 2015. Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nat. Med. 21:92–98
    [Google Scholar]
  73. 73.  Huang H, Delikanli S, Zeng H, Ferkey DM, Pralle A 2010. Remote control of ion channels and neurons through magnetic-field heating of nanoparticles. Nat. Nano 5:602–6
    [Google Scholar]
  74. 74.  Chen R, Romero G, Christiansen MG, Mohr A, Anikeeva P 2015. Wireless magnetothermal deep brain stimulation. Science 347:1477–80
    [Google Scholar]
  75. 75.  Yoo S, Kim R, Park J-H, Nam Y 2016. Electro-optical neural platform integrated with nanoplasmonic inhibition interface. ACS Nano 10:4274–81
    [Google Scholar]
  76. 76.  Carvalho-de-Souza JL, Treger JS, Dang B, Kent SBH, Pepperberg DR, Bezanilla F 2015. Photosensitivity of neurons enabled by cell-targeted gold nanoparticles. Neuron 86:207–17
    [Google Scholar]
  77. 77.  Heureaux J, Chen D, Murray VL, Deng CX, Liu AP 2014. Activation of a bacterial mechanosensitive channel in mammalian cells by cytoskeletal stress. Cell. Mol. Bioeng. 7:307–19
    [Google Scholar]
  78. 78.  Ibsen S, Tong A, Schutt C, Esener S, Chalasani SH 2015. Sonogenetics is a non-invasive approach to activating neurons in Caenorhabditis elegans. . Nat. Commun. 6:8264
    [Google Scholar]
  79. 79.  Pan Y, Yoon S, Sun J, Huang Z, Lee C et al. 2018. Mechanogenetics for the remote and noninvasive control of cancer immunotherapy. PNAS 115:992–97
    [Google Scholar]
  80. 80.  Kubanek J, Shi J, Marsh J, Chen D, Deng C, Cui J 2016. Ultrasound modulates ion channel currents. Sci. Rep. 6:24170
    [Google Scholar]
  81. 81.  Prieto ML, Firouzi K, Khuri-Yakub BT, Maduke M 2017. Activation of Piezo1 but not Nav1.2 channels by ultrasound at 43 MHz. bioRxiv preprint. https://doi.org/10.1101/136994
    [Crossref]
  82. 82.  Fry FJ, Ades HW, Fry WJ 1958. Production of reversible changes in the central nervous system by ultrasound. Science 127:83–84
    [Google Scholar]
  83. 83.  Tyler WJ, Tufail Y, Finsterwald M, Tauchmann ML, Olson EJ, Majestic C 2008. Remote excitation of neuronal circuits using low-intensity, low-frequency ultrasound. PLOS ONE 3:e3511
    [Google Scholar]
  84. 84.  Tufail Y, Matyushov A, Baldwin N, Tauchmann ML, Georges J et al. 2010. Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron 66:681–94
    [Google Scholar]
  85. 85.  Naor O, Krupa S, Shoham S 2016. Ultrasonic neuromodulation. J. Neural Eng. 13:031003
    [Google Scholar]
  86. 86.  Dalecki D 2004. Mechanical bioeffects of ultrasound. Annu. Rev. Biomed. Eng. 6:229–48
    [Google Scholar]
  87. 87.  Mehic E, Xu JM, Caler CJ, Coulson NK, Moritz CT, Mourad PD 2014. Increased anatomical specificity of neuromodulation via modulated focused ultrasound. PLOS ONE 9:e86939
    [Google Scholar]
  88. 88.  Yang PS, Kim H, Lee W, Bohlke M, Park S et al. 2012. Transcranial focused ultrasound to the thalamus is associated with reduced extracellular GABA levels in rats. Neuropsychobiology 65:153–60
    [Google Scholar]
  89. 89.  Bystritsky A, Korb AS, Douglas PK, Cohen MS, Melega WP et al. 2011. A review of low-intensity focused ultrasound pulsation. Brain Stimul 4:125–36
    [Google Scholar]
  90. 90.  Deffieux T, Younan Y, Wattiez N, Tanter M, Pouget P, Aubry JF 2013. Low-intensity focused ultrasound modulates monkey visuomotor behavior. Curr. Biol. 23:2430–33
    [Google Scholar]
  91. 91.  Legon W, Sato TF, Opitz A, Mueller J, Barbour A et al. 2014. Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans. Nat. Neurosci. 17:322–29
    [Google Scholar]
  92. 92.  Lee W, Kim H, Jung Y, Song IU, Chung YA, Yoo SS 2015. Image-guided transcranial focused ultrasound stimulates human primary somatosensory cortex. Sci. Rep. 5:8743
    [Google Scholar]
  93. 93.  Sato T, Shapiro MG, Tsao DY 2018. Ultrasonic neuromodulation causes widespread cortical activation via an indirect auditory mechanism. bioRxiv preprint. https://doi.org/10.1101/234211
    [Crossref]
  94. 94.  Guo H, Hamilton M, Offutt SJ, Gloeckner CD, Li T, et al. 2018. Ultrasound produces extensive brain activation via a cochlear pathway. bioRxiv preprint. https://doi.org/10.1101/233189
    [Crossref]
  95. 95.  Legon W, Rowlands A, Opitz A, Sato TF, Tyler WJ 2012. Pulsed ultrasound differentially stimulates somatosensory circuits in humans as indicated by EEG and FMRI. PLOS ONE 7:e51177
    [Google Scholar]
  96. 96.  Pumphrey RJ 1950. Upper limit of frequency for human hearing. Nature 166:571
    [Google Scholar]
  97. 97.  Tyler WJ 2011. Noninvasive neuromodulation with ultrasound? A continuum mechanics hypothesis. Neuroscientist 17:25–36
    [Google Scholar]
  98. 98.  Prieto ML, Omer O, Khuri-Yakub BT, Maduke MC 2013. Dynamic response of model lipid membranes to ultrasonic radiation force. PLOS ONE 8:e77115
    [Google Scholar]
  99. 99.  Plaksin M, Shoham S, Kimmel E 2014. Intramembrane cavitation as a predictive bio-piezoelectric mechanism for ultrasonic brain stimulation. Phys. Rev. X 4:011004
    [Google Scholar]
  100. 100.  Marmottant P, Hilgenfeldt S 2003. Controlled vesicle deformation and lysis by single oscillating bubbles. Nature 423:153–56
    [Google Scholar]
  101. 101.  Prentice P, Cuschieri A, Dholakia K, Prausnitz M, Campbell P 2005. Membrane disruption by optically controlled microbubble cavitation. Nat. Phys. 1:107–10
    [Google Scholar]
  102. 102.  Kotopoulis S, Dimcevski G, Gilja OH, Hoem D, Postema M 2013. Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study. Med. Phys. 40:072902
    [Google Scholar]
  103. 103.  Sirsi SR, Borden MA 2012. Advances in ultrasound mediated gene therapy using microbubble contrast agents. Theranostics 2:1208–22
    [Google Scholar]
  104. 104.  Choi JJ, Pernot M, Small SA, Konofagou EE 2007. Noninvasive, transcranial and localized opening of the blood-brain barrier using focused ultrasound in mice. Ultrasound Med. Biol. 33:95–104
    [Google Scholar]
  105. 105.  Hosseinkhah N, Hynynen K 2012. A three-dimensional model of an ultrasound contrast agent gas bubble and its mechanical effects on microvessels. Phys. Med. Biol. 57:785–808
    [Google Scholar]
  106. 106.  Tung YS, Vlachos F, Feshitan JA, Borden MA, Konofagou EE 2011. The mechanism of interaction between focused ultrasound and microbubbles in blood-brain barrier opening in mice. J. Acoust. Soc. Am. 130:3059–67
    [Google Scholar]
  107. 107.  Samiotaki G, Acosta C, Wang S, Konofagou EE 2015. Enhanced delivery and bioactivity of the neurturin neurotrophic factor through focused ultrasound-mediated blood–brain barrier opening in vivo. . J. Cereb. Blood Flow Metab. 35:611–22
    [Google Scholar]
  108. 108.  Thevenot E, Jordao JF, O'Reilly MA, Markham K, Weng YQ et al. 2012. Targeted delivery of self-complementary adeno-associated virus serotype 9 to the brain, using magnetic resonance imaging-guided focused ultrasound. Hum. Gene Ther. 23:1144–55
    [Google Scholar]
  109. 109.  McDannold N, Vykhodtseva N, Hynynen K 2008. Blood-brain barrier disruption induced by focused ultrasound and circulating preformed microbubbles appears to be characterized by the mechanical index. Ultrasound Med. Biol. 34:834–40
    [Google Scholar]
  110. 110.  Poon C, McMahon D, Hynynen K 2017. Noninvasive and targeted delivery of therapeutics to the brain using focused ultrasound. Neuropharmacology 120:20–37
    [Google Scholar]
  111. 111.  Downs ME, Buch A, Sierra C, Karakatsani ME, Teichert T et al. 2015. Long-term safety of repeated blood-brain barrier opening via focused ultrasound with microbubbles in non-human primates performing a cognitive task. PLOS ONE 10:e0125911
    [Google Scholar]
  112. 112.  Chen H, Konofagou EE 2014. The size of blood-brain barrier opening induced by focused ultrasound is dictated by the acoustic pressure. J. Cereb. Blood Flow Metab. 34:1197–204
    [Google Scholar]
  113. 113.  Song KH, Fan AC, Hinkle JJ, Newman J, Borden MA, Harvey BK 2017. Microbubble gas volume: a unifying dose parameter in blood-brain barrier opening by focused ultrasound. Theranostics 7:144–52
    [Google Scholar]
  114. 114.  O'Reilly MA, Hynynen K 2012. Blood-brain barrier: real-time feedback-controlled focused ultrasound disruption by using an acoustic emissions-based controller. Radiology 263:96–106
    [Google Scholar]
  115. 115.  Szablowski JO, Lue B, Lee-Gosselin A, Malounda D, Shapiro MG 2018. Acoustically targeted chemogenetics for noninvasive control of neural circuits. bioRxiv preprint. https://doi.org/10.1101/241406
    [Crossref]
  116. 116.  Sternson SM, Roth BL 2014. Chemogenetic tools to interrogate brain functions. Annu. Rev. Neurosci. 37:387–407
    [Google Scholar]
  117. 117.  Keeler AM, ElMallah MK, Flotte TR 2017. Gene therapy 2017: progress and future directions. Clin. Transl. Sci. 10:242–48
    [Google Scholar]
  118. 118.  Laurell T, Petersson F, Nilsson A 2007. Chip integrated strategies for acoustic separation and manipulation of cells and particles. Chem. Soc. Rev. 36:492–506
    [Google Scholar]
  119. 119.  Evander M, Nilsson J 2012. Acoustofluidics 20: applications in acoustic trapping. Lab Chip 12:4667–76
    [Google Scholar]
  120. 120.  Dyson M, Woodward B, Pond JB 1971. Flow of red blood cells stopped by ultrasound. Nature 232:572–73
    [Google Scholar]
  121. 121.  Galanzha EI, Viegas MG, Malinsky TI, Melerzanov AV, Juratli MA et al. 2016. In vivo acoustic and photoacoustic focusing of circulating cells. Sci. Rep. 6:21531
    [Google Scholar]
  122. 122.  Barkholt Muller P, Barnkob R, Herring Jensen MJ, Bruus H 2012. A numerical study of microparticle acoustophoresis driven by acoustic radiation forces and streaming-induced drag forces. Lab Chip 12:4617–27
    [Google Scholar]
  123. 123.  Barnkob R, Augustsson P, Laurell T, Bruus H 2012. Acoustic radiation- and streaming-induced microparticle velocities determined by microparticle image velocimetry in an ultrasound symmetry plane. Phys. Rev. E 86:056307
    [Google Scholar]
  124. 124.  Antfolk M, Muller PB, Augustsson P, Bruus H, Laurell T 2014. Focusing of sub-micrometer particles and bacteria enabled by two-dimensional acoustophoresis. Lab Chip 14:2791–99
    [Google Scholar]
  125. 125.  Mao Z, Li P, Wu M, Bachman H, Mesyngier N et al. 2017. Enriching nanoparticles via acoustofluidics. ACS Nano 11:603–12
    [Google Scholar]
  126. 126.  Wang LV, Hu S 2012. Photoacoustic tomography: in vivo imaging from organelles to organs. Science 335:1458–62
    [Google Scholar]
  127. 127.  Beard P 2011. Biomedical photoacoustic imaging. Interface Focus 1:602–31
    [Google Scholar]
  128. 128.  Yao J, Wang L, Yang J-M, Maslov KI, Wong TTW et al. 2015. High-speed label-free functional photoacoustic microscopy of mouse brain in action. Nat. Methods 12:407–10
    [Google Scholar]
  129. 129.  Staley J, Grogan P, Samadi AK, Cui H, Cohen MS, Yang X 2010. Growth of melanoma brain tumors monitored by photoacoustic microscopy. J. Biomed. Opt. 15:040510
    [Google Scholar]
  130. 130.  Zhang HF, Maslov K, Sivaramakrishnan M, Stoica G, Wang LV 2007. Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy. Appl. Phys. Lett. 90:053901
    [Google Scholar]
  131. 131.  Jathoul AP, Laufer J, Ogunlade O, Treeby B, Cox B et al. 2015. Deep in vivo photoacoustic imaging of mammalian tissues using a tyrosinase-based genetic reporter. Nat. Photonics 9:239–46
    [Google Scholar]
  132. 132.  Weber J, Beard PC, Bohndiek SE 2016. Contrast agents for molecular photoacoustic imaging. Nat. Methods 13:639–50
    [Google Scholar]
  133. 133.  Cai X, Li L, Krumholz A, Guo Z, Erpelding TN et al. 2012. Multi-scale molecular photoacoustic tomography of gene expression. PLOS ONE 7:e43999
    [Google Scholar]
  134. 134.  Yao J, Kaberniuk AA, Li L, Shcherbakova DM, Zhang R et al. 2016. Multi-scale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe. Nat. Methods 13:67–73
    [Google Scholar]
  135. 135.  Yaqoob Z, Psaltis D, Feld MS, Yang C 2008. Optical phase conjugation for turbidity suppression in biological samples. Nat. Photonics 2:110–15
    [Google Scholar]
  136. 136.  McDowell EJ, Cui M, Vellekoop IM, Senekerimyan V, Yaqoob Z, Yang C 2010. Turbidity suppression from the ballistic to the diffusive regime in biological tissues using optical phase conjugation. J. Biomed. Opt. 15:025004–11
    [Google Scholar]
  137. 137.  Vellekoop IM, van Putten EG, Lagendijk A, Mosk AP 2008. Demixing light paths inside disordered metamaterials. Opt. Express 16:67–80
    [Google Scholar]
  138. 138.  Mahan G, Engler W, Tiemann J, Uzgiris E 1998. Ultrasonic tagging of light: theory. PNAS 95:14015–19
    [Google Scholar]
  139. 139.  Xu X, Liu H, Wang LV 2011. Time-reversed ultrasonically encoded optical focusing into scattering media. Nat. Photonics 5:154–57
    [Google Scholar]
  140. 140.  Wang YM, Judkewitz B, DiMarzio CA, Yang C 2012. Deep-tissue focal fluorescence imaging with digitally time-reversed ultrasound-encoded light. Nat. Commun. 3:928
    [Google Scholar]
  141. 141.  Judkewitz B, Wang YM, Horstmeyer R, Mathy A, Yang C 2013. Speckle-scale focusing in the diffusive regime with time reversal of variance-encoded light (TROVE). Nat. Photonics 7:300–5
    [Google Scholar]
  142. 142.  Shapiro MG, Ramirez RM, Sperling LJ, Sun G, Sun J et al. 2014. Genetically encoded reporters for hyperpolarized xenon magnetic resonance imaging. Nat. Chem. 6:629–34
    [Google Scholar]
  143. 143.  Lu GJ, Farhadi A, Szablowski JO, Lee-Gosselin A, Barnes SR et al. 2018. Acoustically modulated magnetic resonance imaging of gas-filled protein nanostructures. Nat. Mater. In press. https://doi.org/10.1038/s41563-018-0023-7
    [Crossref]
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