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Recent advancements in biomedical research have underscored the importance of noninvasive cellular manipulation techniques. Sonogenetics, a method that uses genetic engineering to produce ultrasound-sensitive proteins in target cells, is gaining prominence along with optogenetics, electrogenetics, and magnetogenetics. Upon stimulation with ultrasound, these proteins trigger a cascade of cellular activities and functions. Unlike traditional ultrasound modalities, sonogenetics offers enhanced spatial selectivity, improving precision and safety in disease treatment. This technology broadens the scope of non-surgical interventions across a wide range of clinical research and therapeutic applications, including neuromodulation, oncologic treatments, stem cell therapy, and beyond. Although current literature predominantly emphasizes ultrasonic neuromodulation, this review offers a comprehensive exploration of sonogenetics. We discuss ultrasound properties, the specific ultrasound-sensitive proteins employed in sonogenetics, and the technique’s potential in managing conditions such as neurological disorders, cancer, and ophthalmic diseases, and in stem cell therapies. Our objective is to stimulate fresh perspectives for further research in this promising field.
Maresca D, Lakshmanan A, Abedi M, et al. Biomolecular ultrasound and sonogenetics. Annu Rev Chem Biomol Eng. 2018;9:229–252.
Jiang X, Savchenko O, Li Y, et al. A review of low-intensity pulsed ultrasound for therapeutic applications. IEEE Trans Biomed Eng. 2019;66(10):2704–2718.
Yu K, Niu X, Krook-Magnuson E, He B. Intrinsic functional neuron-type selectivity of transcranial focused ultrasound neuromodulation. Nat Commun. 2021;12(1):2519.
Tufail Y, Matyushov A, Baldwin N, et al. Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron. 2010;66(5):681–694.
Baute Penry V, Cartwright MS. Neuromuscular ultrasound for peripheral neuropathies. Semin Neurol. 2019;39(5):542–548.
Zou J, Yi S, Niu L, et al. Neuroprotective effect of ultrasound neuromodulation on kainic acid-induced epilepsy in mice. IEEE Trans Ultrason Ferroelectrics Freq Control. 2021;68(9):3006–3016.
Moosa S, Martínez-Fernández R, Elias WJ, Del Alamo M, Eisenberg HM, Fishman PS. The role of high-intensity focused ultrasound as a symptomatic treatment for Parkinson’s disease. Mov Disord. 2019;34(9):1243–1251.
Shimokawa H, Shindo T, Ishiki A, et al. A pilot study of whole-brain low-intensity pulsed ultrasound therapy for early stage of Alzheimer’s disease (LIPUS-AD): a randomized, double-blind, placebo-controlled trial. Tohoku J Exp Med. 2022;258(3):167–175.
Tramontin NDS, Silveira PCL, Tietbohl LTW, Pereira BDC, Simon K, Muller AP. Effects of low-intensity transcranial pulsed ultrasound treatment in a model of Alzheimer’s disease. Ultrasound Med Biol. 2021;47(9):2646–2656.
Li X, Yang H, Yan J, Wang X, Li X, Yuan Y. Low-intensity pulsed ultrasound stimulation modulates the nonlinear dynamics of local field potentials in temporal lobe epilepsy. Front Neurosci. 2019;13:287.
Ebadi S, Henschke N, Forogh B, et al. Therapeutic ultrasound for chronic low back pain. Cochrane Database Syst Rev. 2020;7(7):CD009169.
Xia P, Shen S, Lin Q, et al. Low-intensity pulsed ultrasound treatment at an early osteoarthritis stage protects rabbit cartilage from damage via the integrin/focal adhesion kinase/mitogen-activated protein kinase signaling pathway. J Ultrasound Med. 2015;34(11):1991–1999.
Lue T, Tan Y, Guo Y, et al. Low-intensity pulsed ultrasound stimulates proliferation of stem/progenitor cells: what we need to know to translate basic science research into clinical applications. Asian J Androl. 2021;23(6):602.
Kusuyama J, Bandow K, Shamoto M, Kakimoto K, Ohnishi T, Matsuguchi T. Low intensity pulsed ultrasound (LIPUS) influences the multilineage differentiation of mesenchymal stem and progenitor cell lines through ROCK-Cot/Tpl2-MEK-ERK signaling pathway. J Biol Chem. 2014;289(15):10330–10344.
Li H, Zhou J, Zhu M, et al. Low-intensity pulsed ultrasound promotes the formation of periodontal ligament stem cell sheets and ectopic periodontal tissue regeneration. J Biomed Mater Res. 2021;109(7):1101–1112.
Abrunhosa VM, Soares CP, Batista Possidonio AC, et al. Induction of skeletal muscle differentiation in vitro by therapeutic ultrasound. Ultrasound Med Biol. 2014;40(3):504–512.
Chan YS, Hsu KY, Kuo CH, et al. Using low-intensity pulsed ultrasound to improve muscle healing after laceration injury: an in vitro and in vivo study. Ultrasound Med Biol. 2010;36(5):743–751.
Sato M, Motoyoshi M, Shinoda M, Iwata K, Shimizu N. Low-intensity pulsed ultrasound accelerates nerve regeneration following inferior alveolar nerve transection in rats. Eur J Oral Sci. 2016;124(3):246–250.
Xia B, Chen G, Zou Y, Yang L, Pan J, Lv Y. Low-intensity pulsed ultrasound combination with induced pluripotent stem cells-derived neural crest stem cells and growth differentiation factor 5 promotes sciatic nerve regeneration and functional recovery. J Tissue Eng Regen Med. 2019;13(4):625–636.
Liu T, Choi MH, Zhu J, et al. Sonogenetics: recent advances and future directions. Brain Stimul. 2022;15(5):1308–1317.
Azadeh SS, Lordifard P, Soheilifar MH, Esmaeeli Djavid G, Keshmiri Neghab H. Ultrasound and sonogenetics: a new perspective for controlling cells with sound. Iran J Pharm Res (IJPR). 2021;20(3):151–160.
Wang S, Meng W, Ren Z, et al. Ultrasonic neuromodulation and sonogenetics: a new era for neural modulation. Front Physiol. 2020;11:787.
Brier MI, Dordick JS. Remote activation of cellular signaling. Science. 2020;368(6494):936–937.
Rabut C, Yoo S, Hurt RC, et al. Ultrasound technologies for imaging and modulating neural activity. Neuron. 2020;108(1):93–110.
di Biase L, Falato E, Di Lazzaro V. Transcranial focused ultrasound (tFUS) and transcranial unfocused ultrasound (tUS) neuromodulation: from theoretical principles to stimulation practices. Front Neurol. 2019;10:549.
Dalecki D. Mechanical bioeffects of ultrasound. Annu Rev Biomed Eng. 2004;6:229–248.
Bachu VS, Kedda J, Suk I, Green JJ, Tyler B. High-intensity focused ultrasound: a review of mechanisms and clinical applications. Ann Biomed Eng. 2021;49(9):1975–1991.
Izadifar Z, Babyn P, Chapman D. Mechanical and biological effects of ultrasound: a review of present knowledge. Ultrasound Med Biol. 2017;43(6):1085–1104.
Palermo G, Pinto F, Totaro A, et al. High-intensity focused ultrasound in prostate cancer: today’s outcomes and tomorrow’s perspectives. Scand J Urol. 2013;47(3):179–187.
Zhu L, Altman MB, Laszlo A, et al. Ultrasound hyperthermia technology for radiosensitization. Ultrasound Med Biol. 2019;45(5):1025–1043.
Yang Y, Pacia CP, Ye D, et al. Sonothermogenetics for noninvasive and cell-type specific deep brain neuromodulation. Brain Stimul. 2021;14(4):790–800.
Sun T, Samiotaki G, Wang S, Acosta C, Chen CC, Konofagou EE. Acoustic cavitation-based monitoring of the reversibility and permeability of ultrasound-induced blood-brain barrier opening. Phys Med Biol. 2015;60(23):9079–9094.
Korstjens CM, van der Rijt RH, Albers GH, Semeins CM, Klein-Nulend J. Low-intensity pulsed ultrasound affects human articular chondrocytes in vitro. Med Biol Eng Comput. 2008;46(12):1263–1270.
Kobayashi Y, Sakai D, Iwashina T, Iwabuchi S, Mochida J. Low-intensity pulsed ultrasound stimulates cell proliferation, proteoglycan synthesis and expression of growth factor-related genes in human nucleus pulposus cell line. ECM. 2009;17:11–22.
Yao H, Zhang L, Yan S, et al. Low-intensity pulsed ultrasound/nanomechanical force generators enhance osteogenesis of BMSCs through microfilaments and TRPM7. J Nanobiotechnol. 2022;20(1):378.
Kubanek J, Shi J, Marsh J, Chen D, Deng C, Cui J. Ultrasound modulates ion channel currents. Sci Rep. 2016;6:24170.
Ibsen S, Tong A, Schutt C, Esener S, Chalasani SH. Sonogenetics is a non-invasive approach to activating neurons in Caenorhabditis elegans. Nat Commun. 2015;6:8264.
Qiu X, Müller U. Sensing sound: cellular specializations and molecular force sensors. Neuron. 2022;110(22):3667–3687.
Kloda A, Martinac B. Mechanosensitive channels of bacteria and Archaea share a common ancestral origin. Eur Biophys J. 2002;31(1):14–25.
Boulos RA. Antimicrobial dyes and mechanosensitive channels. Antonie Leeuwenhoek. 2013;104(2):155–167.
Haswell ES, Phillips R, Rees DC. Mechanosensitive channels: what can they do and how do they do it? Structure. 2011;19(10):1356–1369.
Sukharev SI, Blount P, Martinac B, Blattner FR, Kung C. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature. 1994;368(6468):265–268.
Sukharev SI, Schroeder MJ, McCaslin DR. Stoichiometry of the large conductance bacterial mechanosensitive channel of E. coli. A biochemical study. J Membr Biol. 1999;171(3):183–193.
Oakley AJ, Martinac B, Wilce MC. Structure and function of the bacterial mechanosensitive channel of large conductance. Protein Sci. 1999;8(10):1915–1921.
Spencer RH, Chang G, Rees DC. ’Feeling the pressure’: structural insights into a gated mechanosensitive channel. Curr Opin Struct Biol. 1999;9(4):448–454.
Maurer JA, Dougherty DA. Generation and evaluation of a large mutational library from the Escherichia coli mechanosensitive channel of large conductance, MscL: implications for channel gating and evolutionary design. J Biol Chem. 2003;278(23):21076–21082.
Walton TA, Idigo CA, Herrera N, Rees DC. MscL: channeling membrane tension. Pflügers Archiv. 2015;467(1):15–25.
Park KH, Berrier C, Martinac B, Ghazi A. Purification and functional reconstitution of N- and C-halves of the MscL channel. Biophys J. 2004;86(4):2129–2136.
Koçer A, Walko M, Meijberg W, Feringa BL. A light-actuated nanovalve derived from a channel protein. Science. 2005;309(5735):755–758.
Bartlett JL, Levin G, Blount P. An in vivo assay identifies changes in residue accessibility on mechanosensitive channel gating. Proc Natl Acad Sci U S A. 2004;101(27):10161–10165.
Koçer A, Walko M, Bulten E, Halza E, Feringa BL, Meijberg W. Rationally designed chemical modulators convert a bacterial channel protein into a pH-sensory valve. Angew Chem Int Ed Engl. 2006;45(19):3126–3130.
Nakayama Y, Mustapić M, Ebrahimian H, et al. Magnetic nanoparticles for "smart liposomes". Eur Biophys J. 2015;44(8):647–654.
Teng J, Loukin S, Anishkin A, Kung C. The force-from-lipid (FFL) principle of mechanosensitivity, at large and in elements. Pflügers Archiv. 2015;467(1):27–37.
Nomura T, Cranfield CG, Deplazes E, et al. Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. Proc Natl Acad Sci U S A. 2012;109(22):8770–8775.
Babakhanian M, Yang L, Nowroozi B, et al. Effects of low intensity focused ultrasound on liposomes containing channel proteins. Sci Rep. 2018;8(1):17250.
Soloperto A, Boccaccio A, Contestabile A, et al. Mechano-sensitization of mammalian neuronal networks through expression of the bacterial large-conductance mechanosensitive ion channel. J Cell Sci. 2018;131(5):jcs210393.
Xian Q, Qiu Z, Murugappan S, et al. Modulation of deep neural circuits with sonogenetics. Proc Natl Acad Sci U S A. 2023;120(22):e2220575120.
Heureaux J, Chen D, Murray VL, Deng CX, Liu AP. Activation of a bacterial mechanosensitive channel in mammalian cells by cytoskeletal stress. Cell Mol Bioeng. 2014;7(3):307–319.
Qiu Z, Kala S, Guo J, et al. Targeted neurostimulation in mouse brains with non-invasive ultrasound. Cell Rep. 2021;34(1):108595.
Ye J, Tang S, Meng L, et al. Ultrasonic control of neural activity through activation of the mechanosensitive channel MscL. Nano Lett. 2018;18(7):4148–4155.
Nilius B, Voets T. TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Arch - Eur J Physiol.. 2005;451(1):1–10.
Christensen AP, Corey DP. TRP channels in mechanosensation: direct or indirect activation? Nat Rev Neurosci. 2007;8(7):510–521.
Li H. TRP channel classification. Adv Exp Med Biol. 2017;976:1–8.
Startek JB, Boonen B, Talavera K, Meseguer V. TRP channels as sensors of chemically-induced changes in cell membrane mechanical properties. Int J Mol Sci. 2019;20(2):371.
Liu C, Montell C. Forcing open TRP channels: mechanical gating as a unifying activation mechanism. Biochem Biophys Res Commun. 2015;460(1):22–25.
Gualdani R, Gailly P, Yuan JH, et al. A TRPM7 mutation linked to familial trigeminal neuralgia: omega current and hyperexcitability of trigeminal ganglion neurons. Proc Natl Acad Sci U S A. 2022;119(38):e2119630119.
Bagnell AM, Sumner CJ, McCray BA. TRPV4: a trigger of pathological RhoA activation in neurological disease. Bioessays. 2022;44(6):e2100288.
Wu J, Ryskamp D, Birnbaumer L, Bezprozvanny I. Inhibition of TRPC1-dependent store-operated calcium entry improves synaptic stability and motor performance in a mouse model of Huntington’s disease. J Huntingtons Dis. 2018;7(1):35–50.
Woudenberg-Vrenken TE, Bindels RJ, Hoenderop JG. The role of transient receptor potential channels in kidney disease. Nat Rev Nephrol. 2009;5(8):441–449.
Wu G, He M, Yin X, et al. The pan-cancer landscape of crosstalk between TRP family and tumour microenvironment relevant to prognosis and immunotherapy response. Front Immunol. 2022;13:837665.
Ma L, Liu X, Liu Q, Jin S, Chang H, Liu H. The roles of transient receptor potential ion channels in pathologies of glaucoma. Front Physiol. 2022;13:806786.
Khanahmad H, Mirbod SM, Karimi F, et al. Pathological mechanisms induced by TRPM2 ion channels activation in renal ischemia-reperfusion injury. Mol Biol Rep. 2022;49(11):11071–11079.
Wang L, Chang JH, Buckley AF, Spurney RF. Knockout of TRPC6 promotes insulin resistance and exacerbates glomerular injury in Akita mice. Kidney Int. 2019;95(2):321–332.
Lin BL, Matera D, Doerner JF, et al. In vivo selective inhibition of TRPC6 by antagonist BI 749327 ameliorates fibrosis and dysfunction in cardiac and renal disease. Proc Natl Acad Sci U S A. 2019;116(20):10156–10161.
Dhaka A, Viswanath V, Patapoutian A. Trp ion channels and temperature sensation. Annu Rev Neurosci. 2006;29:135–161.
Caterina MJ. Vanilloid receptors take a TRP beyond the sensory afferent. Pain. 2003;105(1–2):5–9.
Tominaga M, Caterina MJ, Malmberg AB, et al. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 1998;21(3):531–543.
Huang H, Delikanli S, Zeng H, Ferkey DM, Pralle A. Remote control of ion channels and neurons through magnetic-field heating of nanoparticles. Nat Nanotechnol. 2010;5(8):602–606.
Xu K, Yang Y, Hu Z, et al. TRPV1-mediated sonogenetic neuromodulation of motor cortex in freely moving mice. J Neural Eng. 2023;20(1):016055.
Trost C, Bergs C, Himmerkus N, Flockerzi V. The transient receptor potential, TRP4, cation channel is a novel member of the family of calmodulin binding proteins. Biochem J. 2001;355(Pt 3):663–670.
Kang L, Gao J, Schafer WR, Xie Z, Shawn Xu XZ. C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron. 2010;67(3):381–391.
Duque M, Lee-Kubli CA, Tufail Y, et al. Sonogenetic control of mammalian cells using exogenous Transient Receptor Potential A1 channels. Nat Commun. 2022;13(1):600.
Oh SJ, Lee JM, Kim HB, et al. Ultrasonic neuromodulation via astrocytic TRPA1. Curr Biol. 2019;29(20):3386–3401.e8.
Zhang Y, Chen K, Sloan SA, et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci. 2014;34(36):11929–11947.
Yoo S, Mittelstein DR, Hurt RC, Lacroix J, Shapiro MG. Focused ultrasound excites cortical neurons via mechanosensitive calcium accumulation and ion channel amplification. Nat Commun. 2022;13(1):493.
Fang XZ, Zhou T, Xu JQ, et al. Structure, kinetic properties and biological function of mechanosensitive Piezo channels. Cell Biosci. 2021;11(1):13.
Xu X, Liu S, Liu H, et al. Piezo channels: awesome mechanosensitive structures in cellular mechanotransduction and their role in bone. Int J Mol Sci. 2021;22(12):6429.
Coste B, Mathur J, Schmidt M, et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science. 2010;330(6000):55–60.
Zhao Q, Wu K, Geng J, et al. Ion permeation and mechanotransduction mechanisms of mechanosensitive Piezo channels. Neuron. 2016;89(6):1248–1263.
Gao Q, Cooper PR, Walmsley AD, Scheven BA. Role of Piezo channels in ultrasound-stimulated dental stem cells. J Endod. 2017;43(7):1130–1136.
Qiu Z, Guo J, Kala S, et al. The mechanosensitive ion channel Piezo1 significantly mediates in vitro ultrasonic stimulation of neurons. iScience. 2019;21:448–457.
Zhu J, Xian Q, Hou X, et al. The mechanosensitive ion channel Piezo1 contributes to ultrasound neuromodulation. Proc Natl Acad Sci U S A. 2023;120(18):e2300291120.
Shen X, Song Z, Xu E, Zhou J, Yan F. Sensitization of nerve cells to ultrasound stimulation through Piezo1-targeted microbubbles. Ultrason Sonochem. 2021;73:105494.
Murthy SE, Dubin AE, Patapoutian A. Piezos thrive under pressure: mechanically activated ion channels in health and disease. Nat Rev Mol Cell Biol. 2017;18(12):771–783.
Hoffman BU, Baba Y, Lee SA, Tong CK, Konofagou EE, Lumpkin EA. Focused ultrasound excites action potentials in mammalian peripheral neurons in part through the mechanically gated ion channel PIEZO2. Proc Natl Acad Sci U S A. 2022;119(21):e2115821119.
Li J, Liu S, Song C, et al. PIEZO2 mediates ultrasonic hearing via cochlear outer hair cells in mice. Proc Natl Acad Sci U S A. 2021;118(28):e2101207118.
Smith PA. K+ channels in primary afferents and their role in nerve injury-induced pain. Front Cell Neurosci. 2020;14:566418.
Borsotto M, Veyssiere J, Moha Ou Maati H, Devader C, Mazella J, Heurteaux C. Targeting two-pore domain K+ channels TREK-1 and TASK-3 for the treatment of depression: a new therapeutic concept. Br J Pharmacol. 2015;172(3):771–784.
Cadaveira-Mosquera A, Ribeiro SJ, Reboreda A, Pérez M, Lamas JA. Activation of TREK currents by the neuroprotective agent riluzole in mouse sympathetic neurons. J Neurosci. 2011;31(4):1375–1385.
González W, Valdebenito B, Caballero J, et al. K₂p channels in plants and animals. Pflügers Archiv. 2015;467(5):1091–1104.
Ketchum KA, Joiner WJ, Sellers AJ, Kaczmarek LK, Goldstein SA. A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature. 1995;376(6542):690–695.
Brohawn SG, Su Z, MacKinnon R. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels. Proc Natl Acad Sci U S A. 2014;111(9):3614–3619.
Brohawn SG, Campbell EB, MacKinnon R. Physical mechanism for gating and mechanosensitivity of the human TRAAK K+ channel. Nature. 2014;516(7529):126–130.
Brohawn SG, Wang W, Handler A, Campbell EB, Schwarz JR, MacKinnon R. The mechanosensitive ion channel TRAAK is localized to the mammalian node of Ranvier. Elife. 2019;8:e50403.
Sorum B, Rietmeijer RA, Gopakumar K, Adesnik H, Brohawn SG. Ultrasound activates mechanosensitive TRAAK K+ channels through the lipid membrane. Proc Natl Acad Sci U S A. 2021;118(6):e2006980118.
Belyantseva IA, Adler HJ, Curi R, Frolenkov GI, Kachar B. Expression and localization of prestin and the sugar transporter GLUT-5 during development of electromotility in cochlear outer hair cells. J Neurosci. 2000;20(24):RC116.
Zheng J, Shen W, He DZ, Long KB, Madison LD, Dallos P. Prestin is the motor protein of cochlear outer hair cells. Nature. 2000;405(6783):149–155.
Dallos P, Wu X, Cheatham MA, et al. Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Neuron. 2008;58(3):333–339.
Liberman MC, Gao J, He DZZ, Wu X, Jia S, Zuo J. Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature. 2002;419(6904):300–304.
Ge J, Elferich J, Dehghani-Ghahnaviyeh S, et al. Molecular mechanism of prestin electromotive signal amplification. Cell. 2021;184(18):4669–4679.e13.
Kamar RI, Organ-Darling LE, Raphael RM. Membrane cholesterol strongly influences confined diffusion of prestin. Biophys J. 2012;103(8):1627–1636.
Santos-Sacchi J, Shen W, Zheng J, Dallos P. Effects of membrane potential and tension on prestin, the outer hair cell lateral membrane motor protein. J Physiol. 2001;531(Pt 3):661–666.
Rossiter SJ, Zhang S, Liu Y. Prestin and high frequency hearing in mammals. Commun Integr Biol. 2011;4(2):236–239.
Liu Z, Qi FY, Zhou X, Ren HQ, Shi P. Parallel sites implicate functional convergence of the hearing gene prestin among echolocating mammals. Mol Biol Evol. 2014;31(9):2415–2424.
Li YY, Liu Z, Qi FY, Zhou X, Shi P. Functional effects of a retained ancestral polymorphism in prestin. Mol Biol Evol. 2017;34(1):88–92.
Huang YS, Fan CH, Hsu N, et al. Sonogenetic modulation of cellular activities using an engineered auditory-sensing protein. Nano Lett. 2020;20(2):1089–1100.
Huang YS, Fan CH, Yang WT, Yeh CK, Lin YC. Sonogenetic modulation of cellular activities in mammalian cells. Methods Mol Biol. 2021;2312:109–124.
ter Haar G. Intervention and therapy. Ultrasound Med Biol. 2000;26(Suppl 1):S51-S54.
Xin Z, Lin G, Lei H, Lue TF, Guo Y. Clinical applications of low-intensity pulsed ultrasound and its potential role in urology. Transl Androl Urol. 2016;5(2):255–266.
Kim T, Park C, Chhatbar PY, et al. Effect of low intensity transcranial ultrasound stimulation on neuromodulation in animals and humans: an updated systematic review. Front Neurosci. 2021;15:620863.
Beisteiner R, Lozano AM. Transcranial ultrasound innovations ready for broad clinical application. Adv Sci. 2020;7(23):2002026.
Wang P, Zhang J, Yu J, Smith C, Feng W. Brain modulatory effects by low-intensity transcranial ultrasound stimulation (TUS): a systematic review on both animal and human studies. Front Neurosci. 2019;13:696.
Yoo SS, Bystritsky A, Lee JH, et al. Focused ultrasound modulates region-specific brain activity. Neuroimage. 2011;56(3):1267–1275.
Zhang T, Pan N, Wang Y, Liu C, Hu S. Transcranial focused ultrasound neuromodulation: a review of the excitatory and inhibitory effects on brain activity in human and animals. Front Hum Neurosci. 2021;15:749162.
Lin WT, Chen RC, Lu WW, Liu SH, Yang FY. Protective effects of low-intensity pulsed ultrasound on aluminum-induced cerebral damage in Alzheimer’s disease rat model. Sci Rep. 2015;5:9671.
Lee W, Kim H, Jung Y, Song IU, Chung YA, Yoo SS. Image-guided transcranial focused ultrasound stimulates human primary somatosensory cortex. Sci Rep. 2015;5:8743.
Liao YH, Chen MX, Chen SC, et al. Effects of noninvasive low-intensity focus ultrasound neuromodulation on spinal cord neurocircuits in vivo. Evid Based Complement Alternat Med. 2021;2021:8534466.
Alavi Tamaddoni H, Duryea AP, Vlaisavljevich E, Xu Z, Hall TL. Acoustic methods for increasing the cavitation initiation pressure threshold. IEEE Trans Ultrason Ferroelectrics Freq Control. 2018;65(11):2012–2019.
Lin Y, Lin L, Cheng M, et al. Effect of acoustic parameters on the cavitation behavior of SonoVue microbubbles induced by pulsed ultrasound. Ultrason Sonochem. 2017;35:176–184.
Tung YS, Vlachos F, Feshitan JA, Borden MA, Konofagou EE. The mechanism of interaction between focused ultrasound and microbubbles in blood-brain barrier opening in mice. J Acoust Soc Am. 2011;130(5):3059–3067.
Chen H, Kreider W, Brayman AA, Bailey MR, Matula TJ. Blood vessel deformations on microsecond time scales by ultrasonic cavitation. Phys Rev Lett. 2011;106(3):034301.
Ahmadi F, McLoughlin IV, Chauhan S, ter-Haar G. Bio-effects and safety of low-intensity, low-frequency ultrasonic exposure. Prog Biophys Mol Biol. 2012;108(3):119–138.
Legon W, Ai L, Bansal P, Mueller JK. Neuromodulation with single-element transcranial focused ultrasound in human thalamus. Hum Brain Mapp. 2018;39(5):1995–2006.
King RL, Brown JR, Newsome WT, Pauly KB. Effective parameters for ultrasound-induced in vivo neurostimulation. Ultrasound Med Biol. 2013;39(2):312–331.
Foley JL, Little JW, Vaezy S. Image-guided high-intensity focused ultrasound for conduction block of peripheral nerves. Ann Biomed Eng. 2007;35(1):109–119.
Foster FS, Mehi J, Lukacs M, et al. A new 15-50 MHz array-based micro-ultrasound scanner for preclinical imaging. Ultrasound Med Biol. 2009;35(10):1700–1708.
Kim H, Chiu A, Lee SD, Fischer K, Yoo SS. Focused ultrasound-mediated non-invasive brain stimulation: examination of sonication parameters. Brain Stimul. 2014;7(5):748–756.
Kubanek J, Shukla P, Das A, Baccus SA, Goodman MB. Ultrasound elicits behavioral responses through mechanical effects on neurons and ion channels in a simple nervous system. J Neurosci. 2018;38(12):3081–3091.
Magaram U, Weiss C, Vasan A, Reddy KC, Friend J, Chalasani SH. Two pathways are required for ultrasound-evoked behavioral changes in Caenorhabditis elegans. PLoS One. 2022;17(5):e0267698.
Prieto ML, Firouzi K, Khuri-Yakub BT, Maduke M. Activation of Piezo1 but not NaV1.2 channels by ultrasound at 43 MHz. Ultrasound Med Biol. 2018;44(6):1217–1232.
Pan Y, Yoon S, Sun J, et al. Mechanogenetics for the remote and noninvasive control of cancer immunotherapy. Proc Natl Acad Sci U S A. 2018;115(5):992–997.
Wu CY, Fan CH, Chiu NH, Ho YJ, Lin YC, Yeh CK. Targeted delivery of engineered auditory sensing protein for ultrasound neuromodulation in the brain. Theranostics. 2020;10(8):3546–3561.
Knafo S, Wyart C. Optogenetic neuromodulation: new tools for monitoring and breaking neural circuits. Ann Phys Rehabil Med. 2015;58(4):259–264.
Ndode-Ekane XE, Immonen R, Hämäläinen E, et al. MRI-guided electrode implantation for chronic intracerebral recordings in a rat model of post-traumatic epilepsy-challenges and gains. Biomedicines. 2022;10(9):2295.
Fan CH, Wei KC, Chiu NH, et al. Sonogenetic-based neuromodulation for the amelioration of Parkinson’s disease. Nano Lett. 2021;21(14):5967–5976.
Singh A, Tijore A, Margadant F, et al. Enhanced tumor cell killing by ultrasound after microtubule depolymerization. Bioeng Transl Med. 2021;6(3):e10233.
Song Y, Chen J, Zhang C, et al. Mechanosensitive channel Piezo1 induces cell apoptosis in pancreatic cancer by ultrasound with microbubbles. iScience. 2022;25(2):103733.
Wang T, Wang H, Pang G, et al. A logic AND-gated sonogene nanosystem for precisely regulating the apoptosis of tumor cells. ACS Appl Mater Interfaces. 2020;12(51):56692–56700.
Wu Y, Liu Y, Huang Z, et al. Control of the activity of CAR-T cells within tumours via focused ultrasound. Nat Biomed Eng. 2021;5(11):1336–1347.
Sakai D, Tomita H, Maeda A. Optogenetic therapy for visual restoration. Int J Mol Sci. 2022;23(23):15041.
Macé E, Caplette R, Marre O, et al. Targeting channelrhodopsin-2 to ON-bipolar cells with vitreally administered AAV restores ON and OFF visual responses in blind mice. Mol Ther. 2015;23(1):7–16.
Busskamp V, Duebel J, Balya D, et al. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science. 2010;329(5990):413–417.
Beauchamp MS, Oswalt D, Sun P, et al. Dynamic stimulation of visual cortex produces form vision in sighted and blind humans. Cell. 2020;181(4):774–783.e5.
Blaize K, Arcizet F, Gesnik M, et al. Functional ultrasound imaging of deep visual cortex in awake nonhuman primates. Proc Natl Acad Sci U S A. 2020;117(25):14453–14463.
Provansal M, Marazova K, Sahel JA, Picaud S. Vision restoration by optogenetic therapy and developments toward sonogenetic therapy. Transl Vis Sci Technol. 2022;11(1):18.
Cadoni S, Demené C, Alcala I, et al. Ectopic expression of a mechanosensitive channel confers spatiotemporal resolution to ultrasound stimulations of neurons for visual restoration. Nat Nanotechnol. 2023;18(6):667–676.
Costa V, Carina V, Fontana S, et al. Osteogenic commitment and differentiation of human mesenchymal stem cells by low-intensity pulsed ultrasound stimulation. J Cell Physiol. 2018;233(2):1558–1573.
Li F, Liu Y, Cai Y, et al. Ultrasound irradiation combined with hepatocyte growth factor accelerate the hepatic differentiation of human bone marrow mesenchymal stem cells. Ultrasound Med Biol. 2018;44(5):1044–1052.
Song BW, Park JH, Kim B, et al. A combinational therapy of articular cartilage defects: rapid and effective regeneration by using low-intensity focused ultrasound after adipose tissue-derived stem cell transplantation. Tissue Eng Regen Med. 2020;17(3):313–322.
Moghaddam ZH, Mokhtari-Dizaji M, Movahedin M. Effect of acoustic cavitation on mouse spermatogonial stem cells: colonization and viability. J Ultrasound Med. 2021;40(5):999–1010.
Mohaqiq M, Movahedin M, Mokhtari Dizaji M, Mazaheri Z. Upregulation of integrin-α6 and integrin-β1 gene expressions in mouse spermatogonial stem cells after continues and pulsed low intensity ultrasound stimulation. Cell J. 2018;19(4):634–639.
Lv Y, Zhao P, Chen G, Sha Y, Yang L. Effects of low-intensity pulsed ultrasound on cell viability, proliferation and neural differentiation of induced pluripotent stem cells-derived neural crest stem cells. Biotechnol Lett. 2013;35(12):2201–2212.
Xia B, Zou Y, Xu Z, Lv Y. Gene expression profiling analysis of the effects of low-intensity pulsed ultrasound on induced pluripotent stem cell-derived neural crest stem cells. Biotechnol Appl Biochem. 2017;64(6):927–937.
Xu P, Gul-Uludag H, Ang WT, et al. Low-intensity pulsed ultrasound-mediated stimulation of hematopoietic stem/progenitor cell viability, proliferation and differentiation in vitro. Biotechnol Lett. 2012;34(10):1965–1973.
Liu B, Chen W, Jiang J, et al. Treatment effect of low-intensity pulsed ultrasound on benzene- and cyclophosphamide-induced aplastic Anemia in rabbits. Phys Ther. 2019;99(11):1443–1452.
Hu R, Yang ZY, Li YH, Zhou Z. LIPUS promotes endothelial differentiation and angiogenesis of periodontal ligament stem cells by activating Piezo1. Int J Stem Cells. 2022;15(4):372–383.
Liu S, Jiang C, Hu J, Chen H, Han B, Xia S. Low-intensity pulsed ultrasound enhanced adipose-derived stem cell-mediated angiogenesis in the treatment of diabetic erectile dysfunction through the piezo-ERK-VEGF axis. Stem Cell Int. 2022;2022:6202842.
Wu JY, Yeager K, Tavakol DN, et al. Directed differentiation of human iPSCs into mesenchymal lineages by optogenetic control of TGF-β signaling. Cell Rep. 2023;42(5):112509.
Choi J, Shin E, Lee J, et al. Light-stimulated insulin secretion from pancreatic islet-like organoids derived from human pluripotent stem cells. Mol Ther. 2023;31(5):1480–1495.
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