Skip to main content

Ultrasound and Autism: How Disrupted Redox Homeostasis and Transient Membrane Porosity Confer Risk

  • Chapter
  • First Online:
Studies on Psychiatric Disorders

Abstract

Autism is a group of heterogenetic conditions, comprised of syndromic and nonsyndromic phenotypes. Its heterogeneity has challenged scientists for decades in the attempt to delimit its etiological origins. In this search, focus has fallen heavily on genetics, although a growing body of research suggests a large portion of cases may have a more complex etiology than genetics can explain. Therefore, greater attention is being paid to epigenetic effectors which may play roles in the development of autism. One such teratogen is prenatal ultrasound. In this chapter, we review the current modes of use and recent deregulations surrounding ultrasound, the primary and secondary bioeffects following exposure, its relevance to the development of the brain as well as to autism, the plasticity of the biological organism and how two separate effectors can lead to a common phenotype, and our hopes for future research in this area.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AP-1:

Activator protein 1

APC:

Activated protein C

ATP:

Adenosine triphosphate

cAMP:

Cyclic adenosine monophosphate

cGMP:

Cyclic guanosine monophosphate

CRE:

cAMP response element

CREB:

cAMP response element binding protein

CSF:

Cerebrospinal fluid

ERK:

Extracellular signal-regulated protein kinase

FDA:

United States Food and Drug Administration

FGF:

Fibroblast growth factor

GMP:

Guanosine monophosphate

GSK3β:

Glycogen synthase kinase 3β

HAT:

Histone acetyltransferases

HDAC:

Histone deacetylase

iNOS:

Irreducible nitric oxide synthase

JNK:

c-Jun N-terminal kinase

LAMP-1:

Lysosome-associated membrane glycoprotein 1

LEF:

Lymphoid enhancer factor

LRP:

Lipoprotein receptor-related protein

LTP:

Long-term potentiation

MAPK:

Mitogen-activated protein kinase

mTOR:

Mammalian target of rapamycin

NFκB:

Nuclear factor κB

NMDA:

N-methyl-D-aspartate

PIP2 :

Phosphatidylinositol (4,5)-bisphosphate

PIP3 :

Phosphatidylinositol (3,4,5)-trisphosphate

PKA:

Protein kinase A

PKC:

Protein kinase C

PTEN:

Phosphatase and tensin homologue

redox:

Reduction-oxidation

ROS:

Reactive oxygen species

TCF:

T cell factor

US:

Ultrasound

References

  • Abounader R, Reznik T, Colantuoni C, Martinez-Murillo F, Rosen EM, Laterra J (2004) Regulation of c-Met-dependent gene expression by PTEN. Oncogene 23:9173–9182

    CAS  PubMed  Google Scholar 

  • Adcock IM, Cosio B, Tsaprouni L, Barnes PJ, Ito K (2005) Redox regulation of histone deacetylases and glucocorticoid-mediated inhibition of the inflammatory response. Antioxid Redox Signal 7(1–2):144–152

    Article  CAS  PubMed  Google Scholar 

  • Ang ES Jr, Gluncic V, Duque A, Schafter ME, Rakic P (2006) Prenatal exposure to ultrasound waves impacts neuronal migration in mice. Proc Natl Acad Sci U S A 103(34):12903–12910

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Aylward EH, Minshew NJ, Field K, Sparks BF, Singh N (2002) Effects of age on brain volume and head circumference in autism. Neurology 59(2):175–183

    Article  CAS  PubMed  Google Scholar 

  • Bailey A, Luthert P, Dean A, Harding B, Janota I, Montgomery M, Rutter M, Lantos P (1998) A clinicopathological study of autism. Brain 121(Pt 5):889–905

    Article  PubMed  Google Scholar 

  • Banerjee D, Slack F (2002) Control of developmental timing by small temporal RNAs: a paradigm for RNA-mediated regulation of gene expression. Bioessays 24(2):119–129

    Article  CAS  PubMed  Google Scholar 

  • Barnett SB, Ter Haar GR, Ziskin MC, Rott HD, Duck FA, Maeda K (2000) International recommendations and guidelines for the safe use of diagnostic ultrasound in medicine. Ultrasound Med Biol 26(3):355–366

    Article  CAS  PubMed  Google Scholar 

  • Bennett MV, Zukin RS (2004) Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41(4):495–511

    Article  CAS  PubMed  Google Scholar 

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1(1):11–21

    Article  CAS  PubMed  Google Scholar 

  • Buhimschi IA, Kramer WB, Buhimschi CS, Thompson LP, Weiner CP (2000) Reduction-oxidation (redox) state regulation of matrix metalloproteinase activity in human fetal membranes. Am J Obstet Gynecol 182(2):458–464

    Article  CAS  PubMed  Google Scholar 

  • Campbell DL, Stamler JS, Strauss HC (1996) Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J Gen Physiol 108(4):277–293

    Article  CAS  PubMed  Google Scholar 

  • Campbell DB, Sutcliffe JS, Ebert PJ, Militerni R, Bravaccio C, Trillo S et al (2006) A genetic variant that disrupts MET transcription is associated with autism. Proc Natl Acad Sci U S A 103(45):16834–16839

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Campos LS, Leone DP, Relvas JB, Brakebusch C, Fässler R, Suter U, ffrench-Constant C (2004) β1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 131(14):3433–3444

    Article  CAS  PubMed  Google Scholar 

  • Casanova MF (2004) White matter volume increase and minicolumns in autism. Ann Neurol 56:453

    Article  PubMed  Google Scholar 

  • Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002) Minicolumnar pathology in autism. Neurology 58(3):428–432

    Article  PubMed  Google Scholar 

  • Chauhan A, Chauhan V, Brown WT, Cohen I (2004) Oxidative stress in autism: increased lipid peroxidation and reduced serum levels of ceruloplasmin and transferrin– the antioxidant proteins. Life Sci 75(21):2539–2549

    Article  CAS  PubMed  Google Scholar 

  • Cotterman R, Jin VX, Krig SR, Lemen JM, Wey A, Farnham PJ et al (2008) N-Myc regulates a widespread euchromatic program in the human genome partially independent of its role as a classical transcription factor. Cancer Res 68(23):9654–9662

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Deng CX, Sieling F, Pan H, Cui J (2004) Ultrasound-induced cell membrane porosity. Ultrasound Med Biol 30(4):519–526

    Article  PubMed  Google Scholar 

  • Dinno MA, Dyson M, Young SR, Mortimer AJ, Hart J, Crum LA (1989) The significance of membrane changes in the safe and effective use of therapeutic and diagnostic ultrasound. Phys Med Biol 34(11):1543–1552

    Article  CAS  PubMed  Google Scholar 

  • Doan N, Reher P, Meghji S, Harris M (1999) In vitro effects of therapeutic ultrasound on cell proliferation, protein synthesis, and cytokine production by human fibroblasts, osteoblasts, and monocytes. J Oral Maxillofac Surg 57(4):409–419

    Article  CAS  PubMed  Google Scholar 

  • Fiaschi T, Cozzi G, Raugei G, Formigli L, Ramponi G, Chiarugi P (2006) Redox regulation of beta-actin during integrin-mediated cell adhesion. J Biol Chem 281(32):22983–22991

    Article  CAS  PubMed  Google Scholar 

  • Funato Y, Michiue T, Asashima M, Miki H (2006) The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled. Nat Cell Biol 8(5):501–508

    Article  CAS  PubMed  Google Scholar 

  • Giles D, Hewitt D, Stewart A, Webb J (1956) Malignant disease in childhood and diagnostic radiation in utero. Lancet 1:447

    Google Scholar 

  • Götz M, Stricker SH (2006) Go with the flow: signaling from the ventricle directs neuroblast migration. Nat Neurosci 9(4):470–472

    Article  PubMed  Google Scholar 

  • Grether JK, Li SX, Yoshida CK, Croen LA (2010) Antenatal ultrasound and risk of autism spectrum disorders. J Autism Dev Disord 40(2):238–245

    Article  PubMed  Google Scholar 

  • Griendling KK, Ushio-Fukai M (1998) Redox control of vascular smooth muscle proliferation. J Lab Clin Med 132(1):9–15

    Article  CAS  PubMed  Google Scholar 

  • Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA et al (2001) Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294:2186–2189

    Article  CAS  PubMed  Google Scholar 

  • Guirao B, Meunier A, Mortaud S, Aquilar A, Corsi JM, Strehl L et al (2010) Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat Cell Biol 12(4):341–350

    Article  CAS  PubMed  Google Scholar 

  • Hatakeyama J, Bessho Y, Katoh K, Ookawara S, Fujioka M, Guillemot F et al (2004) Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development 131:5539–5550

    Article  CAS  PubMed  Google Scholar 

  • Ho SN (2006) Intracellular water homeostasis and the mammalian cellular osmotic stress response. J Cell Physiol 206(1):9–15

    Article  CAS  PubMed  Google Scholar 

  • Hogg N, Kalyanaraman B (1999) Nitric oxide and lipid peroxidation. Biochim Biophys Acta 1411(2–3):378–384

    Article  CAS  PubMed  Google Scholar 

  • Hormuzdi SG, Filippov MA, Mitropoulou G, Monyer H, Bruzzone R (2004) Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks. Biochim Biophys Acta 1662(1–2):113–137

    Article  CAS  PubMed  Google Scholar 

  • Hou CH, Lin J, Huang SC, Hou SM, Tang CH (2009) Ultrasound stimulates NF-κB activation and iNOS expression via the Ras/Raf/MEK/ERK signaling pathway in cultured preosteoblasts. J Cell Physiol 220:196–220

    Article  CAS  PubMed  Google Scholar 

  • Hsu HC, Fong YC, Chang CS, Hsu CJ, Hsu SF, Lin JG et al (2007) Ultrasound induces cyclooxygenase-2 expression through integrin, integrin-linked kinase, Akt, NF-κB and p300 pathway in human chondrocytes. Cell Signal 19(11):2317–2328

    Article  CAS  PubMed  Google Scholar 

  • James SJ, Melnyk S, Jernigan S, Cleves MA, Halstead CH, Wong DH et al (2006) Metabolic endophenotype and related genotypes are associated with oxidative stress in children with autism. Am J Med Genet 141B(8):947–956

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jana AK, Agarwal S, Chatterjee SN (1990) The induction of lipid peroxidation in liposomal membrane by ultrasound and the role of hydroxyl radicals. Radiat Res 124(1):7–14

    Article  CAS  PubMed  Google Scholar 

  • Juffermans LJ, Dijkmans PA, Musters RJ, Visser CA, Kamp O (2006) Transient permeabilization of cell membranes by ultrasound-exposed microbubbles is related to formation of hydrogen peroxide. Am J Physiol 291:H1595–1601

    Google Scholar 

  • Koshiyama K, Kodama T, Yano T, Fujikawa S (2006) Structural change in lipid bilayers and water penetration induced by shock waves: molecular dynamics simulations. Biophys J 91(6):198–205

    Article  Google Scholar 

  • Kumon RE, Aehle M, Sabens D, Parikh P, Kourennyi D, Deng CX (2007) Ultrasound-induced calcium oscillations and waves in Chinese hamster ovary cells in the presence of microbubbles. Biophys J 93(6):L29–L31

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lawrie A, Brisken AF, Franics SE, Wyllie D, Kiss-Toth E, Qwarnstrom EE et al (2003) Ultrasound-enhanced transgene expression in vascular cells is not dependent upon cavitation-induced free radicals. Ultrasound Med Biol 29(10):1453–1461

    Article  PubMed  Google Scholar 

  • Lei SZ, Pan ZH, Aggarwal SK, Chen HS, Hartman J, Sucher NJ, Lipton SA (1992) Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron 8(6):1087–1099

    Article  CAS  PubMed  Google Scholar 

  • Liebeskind D, Bases R, Koenigsberg M, Koss L, Raventos C (1981) Morphological changes in the surface characteristics of cultured cells after exposure to diagnostic ultrasound. Radiology 138:419–423

    Article  CAS  PubMed  Google Scholar 

  • MÃ¥rtensson M, Olsson M, Segall B, Fraser AG, Winter R, Brodin L-A (2009) High incidence of defective ultrasound transducers in use in routine clinical practice. Eur J Echocardiogr 10:389–394

    Article  PubMed  Google Scholar 

  • MÃ¥rtensson M, Olsson M, Brodin L-A (2010) Ultrasound transducer function: annual testing is not sufficient. Eur J Echocardiogr 11:801–805

    Article  PubMed  Google Scholar 

  • McBride KL, Varga EA, Pastore MT, Prior TW, Manickam K, Atkin JF et al (2010) Confirmation study of PTEN mutations among individuals with autism or developmental delays/mental retardation and macrocephaly. Autism Res 3(3):137–141

    Article  PubMed  Google Scholar 

  • McDonagh B, Tyther R, Sheehan D (2005) Carbonylation and glutathionylation of proteins in the blue mussel Mytilus edulis detected by proteomic analysis and Western blotting: actin as a target for oxidative stress. Aquat Toxicol 73(3):315–326

    Article  CAS  PubMed  Google Scholar 

  • Medina MA, del Castillo-Olivares A, Schweigerer L (1992) Plasma membrane redox activity correlates with N-myc expression in neuroblastoma cells. FEBS Lett 311(2):99–101

    Article  CAS  PubMed  Google Scholar 

  • Ming X, Stein TP, Brimacombe M, Johnson WG, Lambert GH, Wagner GC (2005) Increased secretion of a lipid peroxidation biomarker in autism. Prostaglandins Leukot Essent Fatty Acids 73(5):379–384

    Article  CAS  PubMed  Google Scholar 

  • Minkel JR (2010) Focus: how to open a hole in a cell. Phys Rev Focus 26:2

    Google Scholar 

  • Muller HJ (1927) Artificial transmutation of the gene. Science 66(1699):84–87

    Article  CAS  PubMed  Google Scholar 

  • Murata H, Ihara Y, Nakamura H, Yodoi J, Sumikawa K, Kondo T (2003) Glutaredoxin exerts an antiapoptotic effect by regulating the redox state of Akt. J Biol Chem 278(50):50226–50233

    Article  CAS  PubMed  Google Scholar 

  • Olkku A, Leskinen JJ, Lammi MJ, Hynynen K, Mahonen A (2010) Ultrasound-induced activation of Wnt signaling in human MG-63 osteoblastic cells. Bone 47(2):320–330

    Article  CAS  PubMed  Google Scholar 

  • Pébay A, Peshavariya H, Wong RCB, Dusting GJ (2011) Non-classical signalling mechanisms in stem cells. In: Atwood CS (ed) Embryonic stem cells: the hormonal regulation of pluripotency and embryogenesis. InTech, Rijeka, pp 317–336

    Google Scholar 

  • Pinto D, Pagnamenta AT, Klei L, Anney R, Merico D, Regan R et al (2010) Functional impact of global rare copy number variation in autism spectrum disorders. Nature 466(7304):368–372

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pohl P, Antonenko YN, Rosenfeld E (1993) Effect of ultrasound on the pH profiles in the unstirred layers near planar bilayer lipid membranes measured by microelectrodes. Biochim Biophys Acta 1152:155–160

    Article  CAS  PubMed  Google Scholar 

  • Rahman I, Marwick J, Kirkham P (2004) Redox modulation of chromatin remodeling: impact on histone acetylation and deacetylation, NF-κB and pro-inflammatory gene expression. Biochem Pharmacol 68:1255–1267

    Article  CAS  PubMed  Google Scholar 

  • Ranjan P, Anathy V, Burch PM, Weirather K, Lambeth JD, Heintz NH (2006) Redox-dependent expression of cyclin D1 and cell proliferation by Nox1 in mouse lung epithelia cells. Antioxid Redox Signal 8(9–10):1447–1459

    Article  CAS  PubMed  Google Scholar 

  • Rasalam AD, Hailey H, Williams JH, Moore SJ, Turnpenny PD, Lloyd DJ et al (2005) Characteristics of fetal anticonvulsant syndrome associated autistic disorder. Dev Med Child Neurol 47(8):551–555

    Article  CAS  PubMed  Google Scholar 

  • Reddy A, Caler EV, Andrews NW (2001) Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell 106(2):157–169

    Article  CAS  PubMed  Google Scholar 

  • Reher P, Doan N, Bradnock B, Meghji S, & Harris M (1999) Effect of ultrasound on the production of IL-8, basic FGF and VEGF. Cytokine 11:416–423

    Google Scholar 

  • Reher P, Harris M, Whiteman M, Hai HK, Meghji S (2002) Ultrasound stimulates nitric oxide and prostaglandin E2 production by human osteoblasts. Bone 31:236–241

    Article  CAS  PubMed  Google Scholar 

  • Riesz P, Kondo T (1992) Free radical formation induced by ultrasound and its biological implications. Free Radic Biol Med 13:247–270

    Article  CAS  PubMed  Google Scholar 

  • Roy S, Khanna S, Sen CK (2008) Redox regulation of the VEGF signaling pathway and tissue vascularization: hydrogen peroxide, the common link between physical exercise and cutaneous wound healing. Free Radic Biol Med 44(2):180–192

    Article  CAS  PubMed  Google Scholar 

  • Sanders SJ, Ercan-Sencicek AG, Hus V, Luo R, Murtha MT, Moreno-De-Luca D et al (2011) Multiple recurrent de novo CNVs, including duplications of the 7q11.23 Williams syndrome region, are strongly associated with autism. Neuron 70(5):863–885

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sarbassov DD, Sabatini DM (2005) Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex. J Biol Chem 280(47):39505–39509

    Article  CAS  PubMed  Google Scholar 

  • Schneider-Kolsky ME, Ayobi Z, Lombardo P, Brown D, Kedang B, Gibbs ME (2009) Ultrasound exposure of the foetal chick brain: effects on learning and memory. Int J Dev Neurosci 27:677–683

    Article  PubMed  Google Scholar 

  • Sheiner E, Shoham-Vardi I, Abramowicz JS (2007) What do clinical end users know regarding safety of ultrasound during pregnancy? J Ultrasound Med 26:319–325

    PubMed  Google Scholar 

  • Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N et al (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304(5675):1338–1340

    Article  CAS  PubMed  Google Scholar 

  • Shimshoni JA, Dalton EC, Jenkins A, Eyal S, Ewan K, Williams RS et al (2007) The effects of central nervous system-active valproic acid constitutional isomers, cyclopropyl analogs, and amide derivatives on neuronal growth cone behavior. Mol Pharmacol 71(3):884–892

    Article  CAS  PubMed  Google Scholar 

  • Siegel E, Goddard J, James AE Jr, Siegel EP (1979) Cellular attachment as a sensitive indicator of the effects of diagnostic ultrasound exposure on cultured human cells. Radiology 133:175–179

    Article  CAS  PubMed  Google Scholar 

  • Tervonen TA, Louivuori V, Sun X, Hokkanen ME, Kratochwil CF, Zebryk P, et al. (2009). Abberant differentiation of glutamatergic cells in neocortex of mouse model for fragile X syndrome. Neuro of Dis 33:250–259

    Google Scholar 

  • 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(10):e3511

    Article  PubMed Central  PubMed  Google Scholar 

  • Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160(1):1–40

    Article  CAS  PubMed  Google Scholar 

  • Way SW, McKenna J, Mietzsch U, Reith RM, Wu HCJ & Gambello MJ (2009) Loss of Tsc2 in radial glia models the brain pathology of tuberous sclerosis complex in the mouse. Hum Mol Genet 18:1252–1265

    Google Scholar 

  • Weeber EJ, Beffert U, Jones C, Christian JM, Forster E, Sweatt JD et al (2002) Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 277(42):39944–39952

    Article  CAS  PubMed  Google Scholar 

  • Wegiel J, Kuchna I, Nowicki K, Imaki H, Wegiel J, Marchi E et al (2010) The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol 119(6):755–770

    Article  PubMed Central  PubMed  Google Scholar 

  • West-Eberhard MJ (2005) Phenotypic accommodation: adaptive innovation due to developmental plasticity. J Exp Zool B Mol Dev Evol 304(6):618

    Google Scholar 

  • Williams EL, Casanova MF (2010) Autism or autisms? Finding the lowest common denominator. Bol Asoc Med P R 102(4):17–24

    PubMed  Google Scholar 

  • Williams EL, Casanova MF (2011) Above genetics: lessons from cerebral development in autism. Transl Neurosci 2(2):106–120

    Article  PubMed Central  PubMed  Google Scholar 

  • Wiltse J (2005) Mode of action: Inhibition of histone deacetylase, altering WNTdependent gene expression, and regulation of beta-catenin-developmental effects of valproic acid. CRC Critical Rev in Toxicol 35:727–738

    Google Scholar 

  • Windham GC, Zhang L, Gunier R, Croen LA, Grether JK (2006) Autism spectrum disorders in relation to distribution of hazardous air pollutants in the San Francisco Bay Area. Environ Health Perspect 114(9):1438–1444

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamamoto K, Takahashi T, Asahara T, Ohura N, Sokabe T, Kamiya A et al (2003) Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J Appl Physiol 95(5):2081–2088

    PubMed  Google Scholar 

  • Yang F, Gu N, Chen D, Xi X, Zhang D, Li Y et al (2008) Experimental study on cell self-sealing during sonoporation. J Control Release 131(3):205–210

    Article  CAS  PubMed  Google Scholar 

  • Young SR, Dyson M (1990a) The effect of therapeutic ultrasound on angiogenesis. Ultrasound Med Biol 16(3):261–269

    Article  CAS  PubMed  Google Scholar 

  • Young SR, Dyson M (1990b) Macrophage responsiveness to therapeutic ultrasound. Ultrasound Med Biol 16(8):809–816

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZJ, Huckle J, Francomano CA, Spencer RG (2003) The effects of pulsed low-intensity ultrasound on chondrocyte viability, proliferation, gene expression and matrix production. Ultrasound Med Biol 29(11):1645–1651

    Article  PubMed  Google Scholar 

  • Zhang X, Odom DT, Koo S-H, Conkright MD, Canettieri G, Best J et al (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci U S A 102(12):4459–4464

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhou X, Richon VM, Wang AH, Yang XJ, Rifkind RA, Marks PA (2000) Histone deacetylase 4 associates with extracellular signal-regulated kinases 1 and 2, and its cellular localization is regulated by oncogenic Ras. Proc Natl Acad Sci U S A 97(26):14329–14333

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu D, Tan KS, Zhang X, Sun AY, Sun GY, Lee JC (2005) Hydrogen peroxide alters membrane and cytoskeleton properties and increases intercellular connections in astrocytes. J Cell Sci 118(Pt 16):3695–3703

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emily L. Williams Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Williams, E.L., Casanova, M.F. (2015). Ultrasound and Autism: How Disrupted Redox Homeostasis and Transient Membrane Porosity Confer Risk. In: Dietrich-Muszalska, A., Chauhan, V., Grignon, S. (eds) Studies on Psychiatric Disorders. Oxidative Stress in Applied Basic Research and Clinical Practice. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-0440-2_18

Download citation

Publish with us

Policies and ethics