Advanced search
Publication Cover
Expert Review of Cardiovascular Therapy Volume 3, 2005 - Issue 1
Submit an article Journal homepage
18
Views
3
CrossRef citations to date
0
Altmetric
Review

Genetic maneuvers to ameliorate ventricular function in heart failure: therapeutic potential and future implications

Fariya Bukhari University of Arizona, Department of Medicine, Tucson, AZ 85721, USA. [email protected]
,
Thomas MacGillivray Massachusetts General Hospital, Cardiac Surgery Division, Boston, MA 02114, USA
,
Federica del Monte Massachusetts General Hospital, Cardiovascular Research Center, 149 13th Street, CNY-4, Charlestown, MA 02129, USA
&
Roger J Hajjar Massachusetts General Hospital, Cardiovascular Research Center, 149 13th Street, CNY-4, Charlestown, MA 02129, USA. [email protected]
Pages 85-97 | Published online: 10 Jan 2014

References

  • del Monte F, Kizana E, Tabchy A, Hajjar RJ. Targeted gene transfer in heart failure: implications for novel gene identification. Curr. Opin. Mol. Ther.6(4), 381–394 (2004).
  • Hajjar RJ, Huq F, Matsui T, Rosenzweig A. Genetic editing of dysfunctional myocardium. Med. Clin. North Am.87(2), 553–567 (2003).
  • Baumgartner I, Pieczek A, Manor O et al. Constitutive expression of phVEGF165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation97(12), 1114–1123 (1998).
  • Lee RJ, Springer ML, Blanco-Bose WE, Shaw R, Ursell PC, Blau HM. VEGF gene delivery to myocardium: deleterious effects of unregulated expression. Circulation102(8), 898–901 (2000).
  • Iwata A, Sai S, Nitta Y et al. Liposome-mediated gene transfection of endothelial nitric oxide synthase reduces endothelial activation and leukocyte infiltration in transplanted hearts. Circulation103(22), 2753–2759 (2001).
  • Lawrie A, Brisken AF, Francis SE et al. Ultrasound enhances reporter gene expression after transfection of vascular cells in vitro. Circulation99(20), 2617–2620 (1999).
  • Hart SL, Arancibia-Carcamo CV, Wolfert MA et al. Lipid-mediated enhancement of transfection by a nonviral integrin-targeting vector. Hum. Gene Ther.9(4), 575–585 (2000).
  • Parkes R, Meng QH, Siapati KE, McEwan JR, Hart SL. High efficiency transfection of porcine vascular cells in vitro with a synthetic vector system. J. Gene Med.4(3), 292–299 (1998).
  • Huard J, Lochmuller H, Acsadi G, Jani A, Massie B, Karpati G. The route of administration is a major determinant of the transduction efficiency of rat tissues by adenoviral recombinants. Gene Ther.2(2), 107–115 (1995).
  • Hiltunen MO, Turunen MP, Turunen AM et al. Biodistribution of adenoviral vector to nontarget tissues after local in vivo gene transfer to arterial wall using intravascular and periadventitial gene delivery methods. Fed. Am. Soc. Exp. Biol. J.14(14), 2230–2236 (2000).
  • Wen S, Schneider DB, Driscoll RM, Vassalli G, Sassani AB, Dichek DA. Second-generation adenoviral vectors do not prevent rapid loss of transgene expression and vector DNA from the arterial wall. Arterioscler. Thromb. Vasc. Biol.20(6), 1452–1458 (2000).
  • Fleury S, Driscoll R, Simeoni E et al. Helper-dependent adenovirus vectors devoid of all viral genes cause less myocardial inflammation compared with first-generation adenovirus vectors. Basic Res. Cardiol.4, 247–256 (2004).
  • Oka K, Pastore L, Kim IH et al. Long-term stable correction of low-density lipoprotein receptor-deficient mice with a helper-dependent adenoviral vector expressing the very low-density lipoprotein receptor. Circulation103(9), 1274–1281 (2001).
  • Havenga MJ, Lemckert AA, Ophorst OJ et al. Exploiting the natural diversity in adenovirus tropism for therapy and prevention of disease. J. Virol.76(9), 4612–4620 (2003).
  • Zhang LQ, Mei YF, Wadell G. Human adenovirus serotypes 4 and 11 show higher binding affinity and infectivity for endothelial and carcinoma cell lines than serotype 5. J. Gen. Virol.84(Pt 3), 687–695 (2002).
  • Arap W, Kolonin MG, Trepel M et al. Steps toward mapping the human vasculature by phage display. Nature Med.8(2), 121–127 (2002).
  • Hay CM, De Leon H, Jafari JD et al. Enhanced gene transfer to rabbit jugular veins by an adenovirus containing a cyclic RGD motif in the HI loop of the fiber knob. J. Vasc. Res.38(4), 315–323 (2000).
  • Reynolds PN, Zinn KR, Gavrilyuk VD et al. A targetable, injectable adenoviral vector for selective gene delivery to pulmonary endothelium in vivo. Mol. Ther.2(6), 562–578 (1999).
  • Harari OA, Wickham TJ, Stocker CJ et al. Targeting an adenoviral gene vector to cytokine-activated vascular endothelium via E-selectin. Gene Ther.6(5), 801–807 (2003).
  • Vassalli G, Bueler H, Dudler J, von Segesser LK, Kappenberger L. Adeno-associated virus (AAV) vectors achieve prolonged transgene expression in mouse myocardium and arteries in vivo: a comparative study with adenovirus vectors. Int. J. Cardiol.90(2–3), 229–238 (2001).
  • Girod A, Ried M, Wobus C et al. Genetic capsid modifications allow efficient retargeting of adeno-associated virus Type 2. Nature Med.5(12), 1438 (1999).
  • Nicklin SA, Von Seggern DJ, Work LM et al. Ablating adenovirus Type 5 fiber-CAR binding and HI loop insertion of the SIGYPLP peptide generate an endothelial cell-selective adenovirus. Mol. Ther.4(6), 534–542 (2001).
  • Bonci D, Cittadini A, Latronico MV et al. ‘Advanced’ generation lentiviruses as efficient vectors for cardiomyocyte gene transduction in vitro and in vivo. Gene Ther.10(8), 630–636 (2003).
  • Emani SM, Shah AS, Bowman MK et al. Catheter-based intracoronary myocardial adenoviral gene delivery: importance of intraluminal seal and infusion flow rate. Mol. Ther.8(2), 306–313 (2003).
  • Marshall DJ, Palasis M, Lepore JJ, Leiden JM. Biocompatibility of cardiovascular gene delivery catheters with adenovirus vectors: an important determinant of the efficiency of cardiovascular gene transfer. Mol. Ther.1(5 Pt 1), 423–429 (2000).
  • Raake P, von Degenfeld G, Hinkel R et al. Myocardial gene transfer by selective pressure-regulated retroinfusion of coronary veins: comparison with surgical and percutaneous intramyocardial gene delivery. J. Am. Coll. Cardiol.44(5), 1124–1129 (2004).
  • Grossman PM, Han Z, Palasis M, Barry JJ, Lederman RJ. Incomplete retention after direct myocardial injection. Cath. Cardiovasc. Interv.55(3), 392–397 (2002).
  • Fromes Y, Salmon A, Wang X et al. Gene delivery to the myocardium by intrapericardial injection. Gene. Ther.6(4), 683–688 (1999).
  • Jones JM, Wilson KH, Koch WJ, Milano CA. Adenoviral gene transfer to the heart during cardiopulmonary bypass: effect of myocardial protection technique on transgene expression. Eur. J. Cardiothorac. Surg.21(5), 847–852 (2002).
  • Bridges CR, Burkman JM, Malekan R et al. Global cardiac-specific transgene expression using cardiopulmonary bypass with cardiac isolation. Ann. Thorac. Surg.73(6), 1939–1946 (2002).
  • Nykanen AI, Krebs R, Saaristo A et al. Angiopoietin-1 protects against the development of cardiac allograft arteriosclerosis. 107(9), 1308–1314 (2003).
  • Hata JA, Williams ML, Koch WJ. Genetic manipulation of myocardial β-adrenergic receptor activation and desensitization. J. Mol. Cell. Cardiol.37(1), 11–12 (2004).
  • Barki-Harrington L, Perrino C, Rockman HA. Network integration of the adrenergic system in cardiac hypertrophy. Cardiovasc. Res.63(3), 391–402 (2004).
  • Chandrasekar B, Marelli-Berg FM, Tone M, Bysani S, Prabhu SD, Murray DR. β-adrenergic stimulation induces interleukin-18 expression via β2-AR, PI3K, Akt, IKK, and NF-κB. Biochem. Biophys. Res. Commun.319(2), 304–311 (2004).
  • Thompson RB, Rungwerth K, Koch WJ. Gene therapy for heart failure. Ann. Med.36(Suppl. 1), 106–115 (2004).
  • Tevaearai HT, Eckhart AD, Walton GB, Keys JR, Wilson K, Koch WJ. Myocardial gene transfer and overexpression of β2-adrenergic receptors potentiates the functional recovery of unloaded failing hearts. Circulation106(1), 124–129 (2002).
  • Cross HR, Steenbergen C, Lefkowitz RJ, Koch WJ, Murphy E. Overexpression of the cardiac β(2)-adrenergic receptor and expression of a β-adrenergic receptor kinase-1 (βARK1) inhibitor both increase myocardial contractility but have differential effects on susceptibility to ischemic injury. Circ. Res.85(11), 1077–1084 (1999).
  • Du XJ, Autelitano DJ, Dilley RJ, Wang B, Dart AM, Woodcock EA. β(2)-adrenergic receptor overexpression exacerbates development of heart failure after aortic stenosis. Circulation101(1), 71–77 (2000).
  • Schluter KD. β2-adrenergic receptor overexpression exacerbates development of heart failure after aortic stenosis. Circulation103(2), E11 (2001).
  • Tang T, Gao MH, Roth DM, Guo T, Hammond HK. Adenyl cyclase Type VI corrects cardiac sarcoplasmic eticulum calcium uptake defects in cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. (1999).
  • Engelhardt S, Hein L, Wiesmann F, Lohse MJ. Progressive hypertrophy and heart failure in β1-adrenergic receptor transgenic mice. Proc. Natl Acad. Sci. USA96(12), 7059–7064 (2001).
  • Jahns R, Boivin V, Hein L et al. Direct evidence for a β1-adrenergic receptor-directed autoimmune attack as a cause of idiopathic dilated cardiomyopathy. J. Clin. Invest.113(10), 1419–1429 (1999).
  • Akhter SA, Eckhart AD, Rockman HA, Shotwell K, Lefkowitz RJ, Koch WJ. In vivo inhibition of elevated myocardial β-adrenergic receptor kinase activity in hybrid transgenic mice restores normal β-adrenergic signaling and function. Circulation100(6), 648–653 (2004).
  • Harding VB, Jones LR, Lefkowitz RJ, Koch WJ, Rockman HA. Cardiac β-ARK1 inhibition prolongs survival and augments β-blocker therapy in a mouse model of severe heart failure. Proc. Natl Acad. Sci. USA98(10), 5809–5814 (2001).
  • Eckhart AD, Fentzke RC, Lepore J et al. Inhibition of βARK1 restores impaired biochemical β-adrenergic receptor responsiveness but does not rescue CREB(A133)-induced cardiomyopathy. J. Mol. Cell. Cardiol.34(6), 669–677 (2002).
  • Lai NC, Roth DM, Gao MH et al. Intracoronary adenovirus encoding adenyl cyclase VI increases left ventricular function in heart failure. Circulation110(3), 330–336 (2004).
  • Odley A, Hahn HS, Lynch RA et al. Regulation of cardiac contractility by Rab4-modulated α2-adrenergic receptor recycling. Proc. Natl Acad. Sci. USA101(18), 7082–7087 (2004).
  • Williams ML, Hata JA, Schroder J et al. Targeted β-adrenergic receptor kinase (βARK1) inhibition by gene transfer in failing human hearts. Circulation109(13), 1590–1593 (2004).
  • Khoynezhad A, Jalali Z, Tortolani AJ. Apoptosis: pathophysiology and therapeutic implications for the cardiac surgeon. Ann. Thorac. Surg.78(3), 1109–1118 (2004).
  • Moe GW, Marin-Garcia J, Konig A, Goldenthal M, Lu X, Feng Q. In vivo tumor necrosis factor-α inhibition ameliorates cardiac mitochondrial dysfunction, oxidative stress and apoptosis in experimental heart failure. Am. J. Physiol. Heart Circ. Physiol.287(4), H1813–H1820 (2004).
  • Henriksen PA, Newby DE. Therapeutic inhibition of tumor necrosis factor-α in patients with heart failure: cooling an inflamed heart. Heart89(1), 14–18 (2003).
  • Mital S, Barbone A, Addonizio LJ et al. Endogenous endothelium-derived nitric oxide inhibits myocardial caspase activity: implications for treatment of end stage heart failure. J. Heart Lung Transplant.21(5), 576–585 (2002).
  • Date T, Luo Z, Yamakawa M et al. Myocardial expression of baculoviral p35 alleviates doxorubicin-induced cardiomyopathy in rats. Hum. Gene Ther.14(10), 947–957 (2003).
  • Yang W, Guastella J, Huang JC et al. MX1013, a dipeptide caspase inhibitor with potent in vivo antiapoptotic activity. Br. J. Pharmacol.140(2), 402–412 (2003).
  • Agata J, Chao L, Chao J. Kallikrein gene delivery improves cardiac reserve and attenuates remodeling after myocardial infarction. Hypertension40(5), 653–659 (2002).
  • Suzuki K, Kostin S, Person V, Elsasser A, Schaper J. Time course of the apoptotic cascade and effects of caspase inhibitors in adult rat ventricular cardiomyocytes. J. Mol. Cell. Cardiol.33(5), 983–994 (2001).
  • Welch S, Plank D, Witt S et al. Cardiac-specific IGF-1 expression attenuates dilated cardiomyopathy in tropomodulin-overexpressing transgenic mice. Circ. Res.90(6), 641–648 (2002).
  • Su EJ, Cioffi CL, Stefansson S et al. Gene therapy vector-mediated expression of insulin-like growth factors protects cardiomyocytes from apoptosis and enhances neovascularization. Am. J. Physiol. Heart Circ. Physiol.284(4), H1429–H1440 (2003).
  • Ogata Y, Takahashi M, Ueno S et al. Anti-apoptotic effect of endothelin-1 in rat cardiomyocytes in vitro. Hypertension41(5), 1156–1163 (2003).
  • Oie E, Clausen OP, Yndestad A, Grogaard HK, Attramadal H, OIje E. Endothelin receptor antagonism attenuates cardiomyocyte apoptosis after induction of ischemia in rats. Scand. Cardiovasc. J.36(2), 108–116 (2002). Erratum: Scand. Cardiovasc. J.36(4), 255 (2002).
  • Shiomi T, Tsutsui H, Matsusaka H et al. Overexpression of glutathione peroxidase prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation109(4), 544–549 (2004).
  • Chatterjee S, Stewart AS, Bish LT et al. Viral gene transfer of the antiapoptotic factor Bcl-2 protects against chronic postischemic heart failure. Circulation106(12 Suppl. 1), I212–I217 (2002).
  • Okumura S, Takagi G, Kawabe J et al. Disruption of type 5 adenyl cyclase gene preserves cardiac function against pressure overload. Proc. Natl Acad. Sci. USA100(17), 9986–9990 (2003).
  • Kuwahara K, Saito Y, Kishimoto I et al. Cardiotrophin-1 phosphorylates Akt and BAD, and prolongs cell survival via a PI3K-dependent pathway in cardiac myocytes. J. Mol. Cell. Cardiol.32(8), 1385–1394 (2000).
  • Taniyama Y, Walsh K. Elevated myocardial Akt signaling ameliorates doxorubicin-induced congestive heart failure and promotes heart growth. J. Mol. Cell. Cardiol.34(10), 1241–1247 (2002).
  • Shiraishi I, Melendez J, Ahn Y et al. Nuclear targeting of Akt enhances kinase activity and survival of cardiomyocytes. Circ. Res.94(7), 884–891 (2004).
  • Condorelli G, Drusco A, Stassi G et al. Akt induces enhanced myocardial contractility and cell size in vivo in transgenic mice. Proc. Natl Acad. Sci. USA99(19), 12333–12338 (2002).
  • Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia–reperfusion injury in mouse heart. Circulation101(6), 660–667 (2000).
  • Hayashidani S, Tsutsui H, Shiomi T et al. Antimonocyte chemoattractant protein-1 gene therapy attenuates left ventricular remodeling and failure after experimental myocardial infarction. Circulation108(17), 2134–2140 (2003).
  • Russell RR 3rd, Li J, Coven DL et al. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J. Clin. Invest.114(4), 495–503 (2004).
  • Shilkrut M, Yaniv G, Asleh R, Levy AP, Larisch S, Binah O. Tyrosine kinases inhibitors block Fas-mediated deleterious effects in normoxic and hypoxic ventricular myocytes. J. Mol. Cell. Cardiol.35(10), 1229–1240 (2003).
  • Kawamura T, Hasegawa K, Morimoto T et al. Expression of p300 protects cardiac myocytes from apoptosis in vivo. Biochem. Biophys. Res. Commun.315(3), 733–738 (2004).
  • Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc. Natl Acad. Sci. USA99(20), 12825–12830 (2002).
  • Sugioka R, Shimizu S, Funatsu T et al. BH4-domain peptide from Bcl-xL exerts antiapoptotic activity in vivo. Oncogene22(52), 8432–8440 (2003).
  • Zou Y, Zhu W, Sakamoto M et al. Heat shock transcription factor 1 protects cardiomyocytes from ischemia/reperfusion injury. Circulation108(24), 3024–3030 (2003).
  • Jones WK, Brown M, Ren X, He S, McGuinness M. NF-κB as an integrator of diverse signaling pathways: the heart of myocardial signaling? Cardiovasc. Toxicol.3(3), 229–254 (2003).
  • Dawn B, Xuan YT, Marian M et al. Cardiac-specific abrogation of NF-κB activation in mice by transdominant expression of a mutant I κBα. J. Mol. Cell. Cardiol.33(1), 161–173 (2001).
  • Wehrens XH, Marks AR. Novel therapeutic approaches for heart failure by normalizing calcium cycling. Nature Rev. Drug Discov.3(7), 565–573 (2004).
  • Miyamoto MI, del Monte F, Schmidt U et al. Adenoviral gene transfer of SERCA2a improves left-ventricular function in aortic-banded rats in transition to heart failure. Proc. Natl Acad. Sci. USA97(2), 793–798 (2000).
  • del Monte F, Harding SE, Schmidt U et al. Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation100(23), 2308–2311 (1999).
  • Terracciano CM, Hajjar RJ, Harding SE. Overexpression of SERCA2a accelerates repolarisation in rabbit ventricular myocytes. Cell. Calcium31(6), 299–305 (2002).
  • del Monte F, Harding SE, Dec GW, Gwathmey JK, Hajjar RJ. Targeting phospholamban by gene transfer in human heart failure. Circulation105(8), 904–907 (2002).
  • del Monte F, Williams E, Lebeche D et al. Improvement in survival and cardiac metabolism after gene transfer of sarcoplasmic reticulum Ca2+-ATPase in a rat model of heart failure. Circulation104(12), 1424–1429 (2001).
  • Chen Y, Escoubet B, Prunier F et al. Constitutive cardiac overexpression of sarcoplasmic/endoplasmic reticulum Ca2+-ATPase delays myocardial failure after myocardial infarction in rats at a cost of increased acute arrhythmias. Circulation109(15), 1898–903 (2004).
  • Davia K, Bernobich E, Ranu HK et al. SERCA2A overexpression decreases the incidence of after contractions in adult rabbit ventricular myocytes. J. Mol. Cell. Cardiol.33(5), 1005–1015 (2001).
  • del Monte F, Lebeche D, Guerrero JL et al. Abrogation of ventricular arrhythmias in a model of ischemia and reperfusion by targeting myocardial calcium cycling. Proc. Natl Acad. Sci. USA101(15), 5622–5627 (2004).
  • Wehrens XH, Lehnart SE, Reiken SR et al. Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin 2. Science304(5668), 292–296 (2004).
  • Yano M, Kobayashi S, Kohno M et al. FKBP12.6-mediated stabilization of calcium-release channel (ryanodine receptor) as a novel therapeutic strategy against heart failure. Circulation107(3), 477–484 (2003).
  • Kohno M, Yano M, Kobayashi S et al. A new cardioprotective agent, JTV519, improves defective channel gating of ryanodine receptor in heart failure. Am. J. Physiol. Heart Circ. Physiol.284(3), H1035–H1042 (2002).
  • Suarez J, Belke DD, Gloss B et al. In vivo adenoviral transfer of sorcin reverses cardiac contractile abnormalities of diabetic cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol.286(1), H68–H75 (2004).
  • Seidler T, Miller SL, Loughrey CM et al. Effects of adenovirus-mediated sorcin overexpression on excitation-contraction coupling in isolated rabbit cardiomyocytes. Circ. Res.93(2), 132–139 (2003).
  • Carr AN, Schmidt AG, Suzuki Y et al. Type 1 phosphatase, a negative regulator of cardiac function. Mol. Cell. Biol.22(12), 4124–4135 (2002).
  • Huq F, Lebeche D, Iyer V, Liao R, Hajjar RJ. Gene transfer of parvalbumin improves diastolic dysfunction in senescent myocytes. Circulation109(22), 2780–2785 (2003).
  • Wahr PA, Michele DE, Metzger JM. Parvalbumin gene transfer corrects diastolic dysfunction in diseased cardiac myocytes. Proc. Natl Acad. Sci. USA96(21), 11982–11985 (1999).
  • Hirsch JC, Borton AR, Albayya FP, Russell MW, Ohye RG, Metzger JM. Comparative analysis of parvalbumin and SERCA2a cardiac myocyte gene transfer in a large animal model of diastolic dysfunction. Am. J. Physiol. Heart Circ. Physiol.286(6), H2314–H2321 (2004).
  • Wehrens XH, Lehnart SE, Reiken SR, Marks AR. Ca2+/calmodulin-dependent protein kinase II phosphorylation regulates the cardiac ryanodine receptor.Circ. Res.94(6), E61–E70 (2004).
  • Asahi M, Otsu K, Nakayama H et al. Cardiac-specific overexpression of sarcolipin inhibits sarco(endo)plasmic reticulum Ca2+ ATPase (SERCA2a) activity and impairs cardiac function in mice. Proc. Natl Acad. Sci. USA101(25), 9199–9204 (2004).
  • Asahi M, Nakayama H, Tada M, Otsu K. Regulation of sarco(endo)plasmic reticulum Ca2+ adenosine triphosphatase by phospholamban and sarcolipin: implication for cardiac hypertrophy and failure. Trends Cardiovasc. Med.13(4), 152–157 (2003).
  • Matsuno Y, Iwata H, Umeda Y et al. Nonviral gene gun mediated transfer into the beating heart. J. Am. Soc. Art. Int. Organs49(6), 641–644 (2003).
  • Chen IY, Wu JC, Min JJ et al. Micro-positron emission tomography imaging of cardiac gene expression in rats using bicistronic adenoviral vector-mediated gene delivery. Circulation109(11), 1415–1420 (2004).
  • Barbash IM, Leor J, Feinberg MS et al. Interventional magnetic resonance imaging for guiding gene and cell transfer in the heart. Heart90(1), 87–91 (2004).
  • Bekeredjian R, Chen S, Frenkel PA, Grayburn PA, Shohet RV. Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation108(8), 1022–1026 (2003).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.