Advanced search
Publication Cover
Expert Opinion on Therapeutic Targets Volume 12, 2008 - Issue 6
Submit an article Journal homepage
260
Views
20
CrossRef citations to date
0
Altmetric
Review

Src inhibitors in breast cancer therapy

Stephen Hiscox RCUK Academic Fellow Cardiff University, Welsh School of Pharmacy, Redwood Building, King Edward VII Avenue, Cardiff, CF10 3XF, UK +029 20 870306; +029 20 875152; [email protected]
, PhD &
Robert I Nicholson Director Cardiff University, Tenovus Centre for Cancer Research, Redwood Building, King Edward VII Avenue, Cardiff, Wales, CF10 3NB, UK
, PhD
Pages 757-767 | Published online: 15 May 2008

Bibliography

  • Brugge JS, Erikson RL, Purchio AF, et al. Identification of a transformation-specific antigen induced by an avian sarcoma virus. Nature 1977;269(5626):346-8
  • Purchio AF, Erikson E, Brugge JS, Erikson RL. Identification of a polypeptide encoded by the avian sarcoma virus src gene. Proc Natl Acad Sci USA 1978;75(3):1567-71
  • Stehelin D, Varmus HE, Bishop JM, Vogt PK. DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA. Nature 1976;260(5547):170-3
  • Thomas SM, Brugge JS. Cellular functions regulated by Src family kinases. Ann Rev Cell Dev Biol 1997;13:513-609
  • Baumgartner M, Radziwill G, Lorger M, et al. c-Src-mediated epithelial cell migration and invasion regulated by PDZ binding site. Mol Cell Biol 2008;28(2):642-55
  • McGarrigle D, Huang XY. GPCRs signaling directly through Src-family kinases. Sci STKE 2007;2007(392):pe35. Published online 26 June 2007, doi:10.1126/stke.3922007pe35
  • Biscardi JS, Ishizawar RC, Silva CM, Parsons SJ. Tyrosine kinase signalling in breast cancer: epidermal growth factor receptor and c-Src interactions in breast cancer. Breast Cancer Res 2000;2(3):203-10
  • Irby RB, Yeatman TJ. Role of Src expression and activation in human cancer. Oncogene 2000;19(49):5636-42
  • Huveneers S, Van Den Bout I, Sonneveld P, et al. Integrin αvβ3 controls activity and oncogenic potential of primed c-Src. Cancer Res 2007;67(6):2693-700
  • Galliher AJ, Schiemann WP. β3 integrin and Src facilitate transforming growth factor-β mediated induction of epithelial-mesenchymal transition in mammary epithelial cells. Breast Cancer Res 2006;8(4):R42. Published online 19 July 2006, doi:10.1186/bcr1524
  • Migliaccio A, Castoria G, Auricchio F. Src-dependent signalling pathway regulation by sex-steroid hormones: therapeutic implications. Int J Biochem Cell Biol 2007;39(7-8):1343-8
  • Migliaccio A, DI Domenico M, Castoria G, et al. Steroid receptor regulation of epidermal growth factor signaling through Src in breast and prostate cancer cells: steroid antagonist action. Cancer Res 2005;65(22):10585-93
  • Silva CM. Role of STATs as downstream signal transducers in Src family kinase-mediated tumorigenesis. Oncogene 2004;23(48):8017-23
  • Brunton VG, Avizienyte E, Fincham VJ, et al. Identification of Src-specific phosphorylation site on focal adhesion kinase: dissection of the role of Src SH2 and catalytic functions and their consequences for tumor cell behavior. Cancer Res 2005;65(4):1335-42
  • Cowell LN, Graham JD, Bouton AH, et al. Tamoxifen treatment promotes phosphorylation of the adhesion molecules, p130Cas/BCAR1, FAK and Src, via an adhesion-dependent pathway. Oncogene 2006;25(58):7597-607
  • Frame MC. Src in cancer: deregulation and consequences for cell behaviour. Biochim Biophys Acta 2002;1602(2):114-30
  • Verbeek BS, Vroom TM, Adriaansen-Slot SS, et al. c-Src protein expression is increased in human breast cancer. An immunohistochemical and biochemical analysis. J Pathol 1996;180(4):383-8
  • Reissig D, Clement J, Sanger J, et al. Elevated activity and expression of Src-family kinases in human breast carcinoma tissue versus matched non-tumor tissue. J Cancer Res Clin Oncol 2001;127(4):226-30
  • Ottenhoff-Kalff AE, Rijksen G, Van Beurden EA, et al. Characterization of protein tyrosine kinases from human breast cancer: involvement of the c-src oncogene product. Cancer Res 1992;52(17):4773-8
  • Irby RB, Mao W, Coppola D, et al. Activating SRC mutation in a subset of advanced human colon cancers. Nat Genet 1999;21(2):187-90
  • Sugimura M, Kobayashi K, Sagae S, et al. Mutation of the SRC gene in endometrial carcinoma. Jpn J Cancer Res 2000;91(4):395-8
  • Wang NM, Yeh KT, Tsai CH, et al. No evidence of correlation between mutation at codon 531 of src and the risk of colon cancer in Chinese. Cancer Lett 2000;150(2):201-4
  • Laghi L, Bianchi P, Orbetegli O, et al. Lack of mutation at codon 531 of SRC in advanced colorectal cancers from Italian patients. Br J Cancer 2001;84(2):196-8
  • Bild AH, Yao G, Chang JT, et al. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 2006;439(7074):353-7
  • Luttrell DK, Lee A, Lansing TJ, et al. Involvement of pp60c-src with two major signaling pathways in human breast cancer. Proc Natl Acad Sci USA 1994;91(1):83-7
  • Muthuswamy SK, Muller WJ. Activation of Src family kinases in Neu-induced mammary tumors correlates with their association with distinct sets of tyrosine phosphorylated proteins in vivo. Oncogene 1995;11(9):1801-10
  • Ishizawar RC, Miyake T, Parsons SJ. c-Src modulates ErbB2 and ErbB3 heterocomplex formation and function. Oncogene 2007;26(24):3503-10
  • Ishizawar R, Parsons SJ. c-Src and cooperating partners in human cancer. Cancer Cell 2004;6(3):209-14
  • Li Y, Ren J, Yu W, et al. The epidermal growth factor receptor regulates interaction of the human DF3/MUC1 carcinoma antigen with c-Src and β-catenin. J Biol Chem 2001;276(38):35239-42
  • Singh R, Bandyopadhyay D. MUC1: a target molecule for cancer therapy. Cancer Biol Ther 2007;6(4):481-6
  • Yang E, Hu XF, Xing PX. Advances of MUC1 as a target for breast cancer immunotherapy. Histol Histopathol 2007;22(8):905-22
  • Egan C, Pang A, Durda D, et al. Activation of Src in human breast tumor cell lines: elevated levels of phosphotyrosine phosphatase activity that preferentially recognizes the Src carboxy terminal negative regulatory tyrosine 530. Oncogene 1999;18(5):1227-37
  • Bjorge JD, Pang A, Fujita DJ. Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J Biol Chem 2000;275(52):41439-46
  • Tonks NK, Muthuswamy SK. A brake becomes an accelerator: PTP1B–a new therapeutic target for breast cancer. Cancer Cell 2007;11(3):214-6
  • Webster MA, Cardiff RD, Muller WJ. Induction of mammary epithelial hyperplasias and mammary tumors in transgenic mice expressing a murine mammary tumor virus/activated c-src fusion gene. Proc Natl Acad Sci USA 1995;92(17):7849-53
  • Guy CT, Muthuswamy SK, Cardiff RD, et al. Activation of the c-Src tyrosine kinase is required for the induction of mammary tumors in transgenic mice. Genes Dev 1994;8(1):23-32
  • Nicholson RI, Gee JM, Harper ME. EGFR and cancer prognosis. Eur J Cancer 2001;37(Suppl 4):S9-15
  • Summy JM, Gallick GE. Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev 2003;22(4):337-58
  • Maa MC, Leu TH, Mccarley DJ, et al. Potentiation of epidermal growth factor receptor-mediated oncogenesis by c-Src: implications for the etiology of multiple human cancers. Proc Natl Acad Sci USA 1995;92(15):6981-5
  • Wilson LK, Luttrell DK, Parsons JT, Parsons SJ. pp60c-src tyrosine kinase, myristylation, and modulatory domains are required for enhanced mitogenic responsiveness to epidermal growth factor seen in cells overexpressing c-src. Mol Cell Biol 1989;9(4):1536-44
  • Roche S, Fumagalli S, Courtneidge SA. Requirement for Src family protein tyrosine kinases in G2 for fibroblast cell division. Science 1995;269(5230):1567-9
  • Boerner JL, Biscardi JS, Silva CM, Parsons SJ. Transactivating agonists of the EGF receptor require Tyr 845 phosphorylation for induction of DNA synthesis. Mol Carcinog 2005;44(4):262-73
  • Belsches-Jablonski AP, Biscardi JS, Peavy DR, et al. Src family kinases and HER2 interactions in human breast cancer cell growth and survival. Oncogene 2001;20(12):1465-75
  • Sam MR, Elliott BE, Mueller CR. A novel activating role of SRC and STAT3 on HGF transcription in human breast cancer cells. Mol Cancer 2007;6(1):69
  • Lengyel E, Prechtel D, Resau JH, et al. C-Met overexpression in node-positive breast cancer identifies patients with poor clinical outcome independent of Her2/neu. Int J Cancer 2005;113(4):678-82
  • Lindemann K, Resau J, Nahrig J, et al. Differential expression of c-Met, its ligand HGF/SF and HER2/neu in DCIS and adjacent normal breast tissue. Histopathology 2007;51(1):54-62
  • Visvader JE, Lindeman GJ. Transcriptional regulators in mammary gland development and cancer. Int J Biochem Cell Biol 2003;35(7):1034-51
  • Migliaccio A, Di Domenico M, Castoria G, et al. Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J 1996;15(6):1292-300
  • Migliaccio A, Piccolo D, Castoria G, et al. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J 1998;17(7):2008-18
  • Silva CM, Shupnik MA. Integration of steroid and growth factor pathways in breast cancer: focus on signal transducers and activators of transcription and their potential role in resistance. Mol Endocrinol 2007;21(7):1499-512
  • Acconcia F, Kumar R. Signaling regulation of genomic and nongenomic functions of estrogen receptors. Cancer Lett 2006;238(1):1-14
  • Simoncini T, Hafezi-Moghadam A, Brazil DP, et al. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 2000;407(6803):538-41
  • Hitosugi T, Sasaki K, Sato M, et al. Epidermal growth factor directs sex-specific steroid signaling through Src activation. J Biol Chem 2007;282(14):10697-706
  • Castoria G, Barone MV, Di Domenico M, et al. Non-transcriptional action of oestradiol and progestin triggers DNA synthesis. EMBO J 1999;18(9):2500-10
  • Migliaccio A, Castoria G, Di Domenico M, et al. Steroid-induced androgen receptor-oestradiol receptor β-Src complex triggers prostate cancer cell proliferation. EMBO J 2000;19(20):5406-17
  • Levin ER, Pietras RJ. Estrogen receptors outside the nucleus in breast cancer. Breast Cancer Res Treat 2008;108(3):351-61
  • Pedram A, Razandi M, Levin ER. Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol 2006;20(9):1996-2009
  • Wong CW, Mcnally C, Nickbarg E, et al. Estrogen receptor-interacting protein that modulates its nongenomic activity-crosstalk with Src/Erk phosphorylation cascade. Proc Natl Acad Sci USA 2002;99(23):14783-8
  • Varricchio L, Migliaccio A, Castoria G, et al. Inhibition of estradiol receptor/Src association and cell growth by an estradiol receptor α tyrosine-phosphorylated peptide. Mol Cancer Res 2007;5(11):1213-1
  • Auricchio F, Migliaccio A, Castoria G. Sex-steroid hormones and EGF signalling in breast and prostate cancer cells: Targeting the association of Src with steroid receptors. Steroids 2008
  • Levin ER. Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol Endocrinol 2003;17(3):309-17
  • Arpino G, Wiechmann L, Osborne CK, Schiff R. Cross-talk between the estrogen receptor and the HER tyrosine kinase receptor family: molecular mechanism and clinical implications for endocrine therapy resistance. Endocr Rev 2008;29(2):217-33
  • Massarweh S, Schiff R. Resistance to endocrine therapy in breast cancer: exploiting estrogen receptor/growth factor signaling crosstalk. Endocr Relat Cancer 2006;13(Suppl 1):S15-24
  • Razandi M, Pedram A, Park ST, Levin ER. Proximal events in signaling by plasma membrane estrogen receptors. J Biol Chem 2003;278(4):2701-12
  • Chu I, Arnaout A, Loiseau S, et al. Src promotes estrogen-dependent estrogen receptor α proteolysis in human breast cancer. J Clin Invest 2007;117(8):2205-15
  • Zheng X, Resnick RJ, Shalloway D. Apoptosis of estrogen-receptor negative breast cancer and colon cancer cell lines by PTPα and src RNAi. Int J Cancer 2008;122(9):1999-2007
  • Fincham VJ, Frame MC. The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility. EMBO J 1998;17(1):81-92
  • Hiscox S, Jordan NJ, Morgan L, et al. Src kinase promotes adhesion-independent activation of FAK and enhances cellular migration in tamoxifen-resistant breast cancer cells. Clin Exp Metastasis 2007;24(3):157-67
  • Planas-Silva MD, Bruggeman RD, Grenko RT, et al. Role of c-Src and focal adhesion kinase in progression and metastasis of estrogen receptor-positive breast cancer. Biochem Biophys Res Commun 2006;341(1):73-81
  • Cortes-Reynosa P, Robledo T, Macias-Silva M, et al. Src kinase regulates metalloproteinase-9 secretion induced by type IV collagen in MCF-7 human breast cancer cells. Matrix Biol 2007
  • Zou JX, Liu Y, Pasquale EB, Ruoslahti E. Activated SRC oncogene phosphorylates R-ras and suppresses integrin activity. J Biol Chem 2002;277(3):1824-7
  • Datta A, Huber F, Boettiger D. Phosphorylation of β3 integrin controls ligand binding strength. J Biol Chem 2002;277(6):3943-9
  • Chang JH, Gill S, Settleman J, Parsons SJ. c-Src regulates the simultaneous rearrangement of actin cytoskeleton, p190RhoGAP, and p120RasGAP following epidermal growth factor stimulation. J Cell Biol 1995;130(2):355-68
  • Skoudy A, Llosas MD, Garcia De Herreros A. Intestinal HT-29 cells with dysfunction of E-cadherin show increased pp60src activity and tyrosine phosphorylation of p120-catenin. Biochem J 1996;317(Pt 1):279-84
  • Takeda H, Nagafuchi A, Yonemura S, et al. V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and β catenin is not required for the shift. J Cell Biol 1995;131(6 Pt 2):1839-47
  • Nam JS, Ino Y, Sakamoto M, Hirohashi S. Src family kinase inhibitor PP2 restores the E-cadherin/catenin cell adhesion system in human cancer cells and reduces cancer metastasis. Clin Cancer Res 2002;8(7):2430-6
  • Elliott BE, Meens JA, Sengupta SK, et al. The membrane cytoskeletal crosslinker ezrin is required for metastasis of breast carcinoma cells. Breast Cancer Res 2005;7(3):R365-73
  • Hall CL, Lange LA, Prober DA, et al. pp60(c-src) is required for cell locomotion regulated by the hyaluronan receptor RHAMM. Oncogene 1996;13(10):2213-24
  • Hiscox S, Morgan L, Green TP, et al. Elevated Src activity promotes cellular invasion and motility in tamoxifen resistant breast cancer cells. Breast Cancer Res Treat 2006;97(3):263-74
  • Gonzalez L, Agullo-Ortuno MT, Garcia-Martinez JM, et al. Role of c-Src in human MCF7 breast cancer cell tumorigenesis. J Biol Chem 2006;281(30):20851-64
  • Cortesio CL, Chan KT, Perrin BJ, et al. Calpain 2 and PTP1B function in a novel pathway with Src to regulate invadopodia dynamics and breast cancer cell invasion. J Cell Biol 2008;180(5):957-71
  • Guarino M, Rubino B, Ballabio G. The role of epithelial-mesenchymal transition in cancer pathology. Pathology 2007;39(3):305-18
  • Strizzi L, Bianco C, Normanno N, et al. Epithelial mesenchymal transition is a characteristic of hyperplasias and tumors in mammary gland from MMTV-Cripto-1 transgenic mice. J Cell Physiol 2004;201(2):266-76
  • Planas-Silva MD, Waltz PK. Estrogen promotes reversible epithelial-to-mesenchymal-like transition and collective motility in MCF-7 breast cancer cells. J Steroid Biochem Mol Biol 2007;104(1-2):11-21
  • Mitra SK, Mikolon D, Molina JE, et al. Intrinsic FAK activity and Y925 phosphorylation facilitate an angiogenic switch in tumors. Oncogene 2006;25(44):5969-84
  • Zetser A, Bashenko Y, Edovitsky E, et al. Heparanase induces vascular endothelial growth factor expression: correlation with p38 phosphorylation levels and Src activation. Cancer Res 2006;66(3):1455-63
  • Niu G, Wright KL, Huang M, et al. Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene 2002;21(13):2000-8
  • Altmann E, Widler L, Missbach M. N(7)-substituted-5-aryl-pyrrolo[2,3-d]pyrimidines represent a versatile class of potent inhibitors of the tyrosine kinase c-Src. Mini Rev Med Chem 2002;2(3):201-8
  • Altmann E, Missbach M, Green J, et al. 7-Pyrrolidinyl- and 7-piperidinyl-5-aryl-pyrrolo[2,3-d]pyrimidines - potent inhibitors of the tyrosine kinase c-Src. Bioorg Med Chem Lett 2001;11(6):853-6
  • Roskoski R Jr. Src protein-tyrosine kinase structure and regulation. Biochem Biophys Res Commun 2004;324(4):1155-64
  • Shakespeare WC, Bohacek RS, Azimioara MD, et al. Structure-based design of novel bicyclic nonpeptide inhibitors for the src SH2 domain. J Med Chem 2000;43(21):3815-9
  • Sharma SV, Oneyama C, Yamashita Y, et al. UCS15A, a non-kinase inhibitor of Src signal transduction. Oncogene 2001;20(17):2068-79
  • Oneyama C, Nakano H, Sharma SV. UCS15A, a novel small molecule, SH3 domain-mediated protein-protein interaction blocking drug. Oncogene 2002;21(13):2037-50
  • Shakespeare WC, Metcalf CA 3RD, Wang Y, et al. Novel bone-targeted Src tyrosine kinase inhibitor drug discovery. Curr Opin Drug Discov Devel 2003;6(5):729-41
  • Violette SM, Guan W, Bartlett C, et al. Bone-targeted Src SH2 inhibitors block Src cellular activity and osteoclast-mediated resorption. Bone 2001;28(1):54-64
  • Beliakoff J, Whitesell L. Hsp90: an emerging target for breast cancer therapy. Anticancer Drugs 2004;15(7):651-62
  • Bishop SC, Burlison JA, Blagg BS. Hsp90: a novel target for the disruption of multiple signaling cascades. Curr Cancer Drug Targets 2007;7(4):369-88
  • Schnur RC, Corman ML, Gallaschun RJ, et al. Inhibition of the oncogene product p185erbB-2 in vitro and in vivo by geldanamycin and dihydrogeldanamycin derivatives. J Med Chem 1995;38(19):3806-12
  • Lombardo LJ, Lee FY, Chen P, et al. Discovery of N-(2-chloro-6-methyl- phenyl)-2-(6-(4-(2-hydroxyethyl)- piperazin-1-yl)-2-methylpyrimidin-4- ylamino)thiazole-5-carboxamide (BMS-354825), a dual Src/Abl kinase inhibitor with potent antitumor activity in preclinical assays. J Med Chem 2004;47(27):6658-61
  • Finn RS, Dering J, Ginther C, et al. Dasatinib, an orally active small molecule inhibitor of both the src and abl kinases, selectively inhibits growth of basal-type/“triple-negative” breast cancer cell lines growing in vitro. Breast Cancer Res Treat 2007;105(3):319-26
  • Huang F, Reeves K, Han X, et al. Identification of candidate molecular markers predicting sensitivity in solid tumors to dasatinib: rationale for patient selection. Cancer Res 2007;67(5):2226-38
  • Jallal H, Valentino ML, Chen G, et al. A Src/Abl kinase inhibitor, SKI-606, blocks breast cancer invasion, growth, and metastasis in vitro and in vivo. Cancer Res 2007;67(4):1580-8
  • Herynk MH, Beyer AR, Cui Y, et al. Cooperative action of tamoxifen and c-Src inhibition in preventing the growth of estrogen receptor-positive human breast cancer cells. Mol Cancer Ther 2006;5(12):3023-31
  • Summy JM, Gallick GE. Treatment for advanced tumors: SRC reclaims center stage. Clin Cancer Res 2006;12(5):1398-401
  • Lowell CA, Soriano P. Knockouts of Src-family kinases: stiff bones, wimpy T cells, and bad memories. Genes Dev 1996;10(15):1845-57
  • Hortobagyi GN. Trastuzumab in the treatment of breast cancer. N Engl J Med 2005;353(16):1734-6
  • Dizdar O, Dede DS, Bulut N, Altundag K. Dasatinib may also inhibit c-Kit in triple negative breast cancer cell lines. Breast Cancer Res Treat 2008;107(2):303
  • Harputluoglu H, Dizdar O, Altundag K. Potential targeted therapy options in the management of basal cell subtype of breast carcinoma. Hum Pathol 2007;38(12):1869; author reply 1870
  • Anders CK, Acharya CR, Hsu DS, et al. Age-specific differences in oncogenic pathway deregulation seen in human breast tumors. PLoS One 2008;3(1):e1373
  • Linke R, Dempke W. Management of imatinib-resistant CML patients. Onkologie 2007;30(11):574-80
  • O'hare T, Eide CA, Deininger MW. Bcr-Abl kinase domain mutations and the unsettled problem of Bcr-AblT315I: looking into the future of controlling drug resistance in chronic myeloid leukemia. Clin Lymphoma Myeloma 2007;7(Suppl 3):S120-30
  • Hitosugi T, Sato M, Sasaki K, Umezawa Y. Lipid raft specific knockdown of SRC family kinase activity inhibits cell adhesion and cell cycle progression of breast cancer cells. Cancer Res 2007;67(17):8139-48
  • Kamath JR, Liu R, Enstrom AM, et al. Development and characterization of potent and specific peptide inhibitors of p60c-src protein tyrosine kinase using pseudosubstrate-based inhibitor design approach. J Pept Res 2003;62(6):260-8
  • Reynolds AB, Roesel DJ, Kanner SB, Parsons JT. Transformation-specific tyrosine phosphorylation of a novel cellular protein in chicken cells expressing oncogenic variants of the avian cellular src gene. Mol Cell Biol 1989;9(2):629-38
  • Hiscox S, Morgan L, Green T, Nicholson RI. Src as a therapeutic target in anti-hormone/anti-growth factor-resistant breast cancer. Endocr Relat Cancer 2006;13(Suppl 1):S53-9
  • Hiscox S, Green TP, Jordan NJ, et al. Combination therapy using AZD0530 and tamoxifen prevents anti-hormone resistance in breast cancer cells. Breast Can Res Treat 2006;100:S246

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.