Advanced search
Publication Cover
Molecular and Cellular Biology Volume 21, 2001 - Issue 4
Submit an article Journal homepage
19
Views
80
CrossRef citations to date
0
Altmetric
Cell Growth and Development

p21Cip1 and p27Kip1Regulate Cell Cycle Reentry after Hypoxic Stress but Are Not Necessary for Hypoxia-Induced Arrest

Susannah L. GreenCenter for Clinical Sciences Research, Department of Radiation Oncology, Stanford University, Stanford, California94303-5152
,
Rachel A. FreibergCenter for Clinical Sciences Research, Department of Radiation Oncology, Stanford University, Stanford, California94303-5152
&
Amato J. GiacciaCenter for Clinical Sciences Research, Department of Radiation Oncology, Stanford University, Stanford, California94303-5152Correspondence[email protected]
Pages 1196-1206 | Received 15 Jun 2000, Accepted 06 Nov 2000, Published online: 28 Mar 2023

Citations (80)

Keep up to date with the latest research on this topic with citation updates for this article.

Subscribe to citation updates

Read on this site (11)

Michal W. Luczak, Casey Krawic & Anatoly Zhitkovich. (2021) NAD+ metabolism controls growth inhibition by HIF1 in normoxia and determines differential sensitivity of normal and cancer cells. Cell Cycle 20:18, pages 1812-1827.
Read now
Monika Löffler, Elizabeth A. Carrey & Wolfgang Knecht. (2020) The pathway to pyrimidines: The essential focus on dihydroorotate dehydrogenase, the mitochondrial enzyme coupled to the respiratory chain. Nucleosides, Nucleotides & Nucleic Acids 39:10-12, pages 1281-1305.
Read now
Mariam Abaza & Yunus A Luqmani. (2013) The influence of pH and hypoxia on tumor metastasis. Expert Review of Anticancer Therapy 13:10, pages 1229-1242.
Read now
Peter Ebbesen, Erik O. Pettersen, Thomas A. Gorr, Gerhard Jobst, Kaye Williams, Jochen Kieninger, Roland H. Wenger, Silvia Pastorekova, Ludwig Dubois, Philippe Lambin, Brad G. Wouters, Twan Van Den Beucken, Claudiu T. Supuran, Lorenz Poellinger, Peter Ratcliffe, Arvydas Kanopka, Agnes Görlach, Max Gasmann, Adrian L. Harris, Patrick Maxwell & Andrea Scozzafava. (2009) Taking advantage of tumor cell adaptations to hypoxia for developing new tumor markers and treatment strategies. Journal of Enzyme Inhibition and Medicinal Chemistry 24:sup1, pages 1-39.
Read now
Zuzana Bencokova, Muriel R. Kaufmann, Isabel M. Pires, Philip S. Lecane, Amato J. Giaccia & Ester M. Hammond. (2009) ATM Activation and Signaling under Hypoxic Conditions. Molecular and Cellular Biology 29:2, pages 526-537.
Read now
Tomás Alarcón, Markus R. Owen, Helen M. Byrne & Philip K. Maini. (2006) Multiscale modelling of tumour growth and therapy: the influence of vessel normalisation on chemotherapy. Computational and Mathematical Methods in Medicine 7:2-3, pages 85-119.
Read now
Rachel A. Freiberg, Ester M. Hammond, Mary Jo Dorie, Scott M. Welford & Amato J. Giaccia. (2006) DNA Damage during Reoxygenation Elicits a Chk2-Dependent Checkpoint Response. Molecular and Cellular Biology 26:5, pages 1598-1609.
Read now
Fiona A. Mack, Jagruti H. Patel, Mangatt P. Biju, Volker H. Haase & M. Celeste Simon. (2005) Decreased Growth of Vhl−− Fibrosarcomas Is Associated with Elevated Levels of Cyclin Kinase Inhibitors p21 and p27. Molecular and Cellular Biology 25:11, pages 4565-4578.
Read now
Lawrence B. Gardner, Feng Li, Xuejie Yang & Chi V. Dang. (2003) Anoxic Fibroblasts Activate a Replication Checkpoint That Is Bypassed By E1a. Molecular and Cellular Biology 23:24, pages 9032-9045.
Read now
Nobuhito Goda, Heather E. Ryan, Bahram Khadivi, Wayne McNulty, Robert C. Rickert & Randall S. Johnson. (2003) Hypoxia-Inducible Factor 1α Is Essential for Cell Cycle Arrest during Hypoxia. Molecular and Cellular Biology 23:1, pages 359-369.
Read now
Ester M. Hammond, Nicholas C. Denko, Mary Jo Dorie, Robert T. Abraham & Amato J. Giaccia. (2002) Hypoxia Links ATR and p53 through Replication Arrest. Molecular and Cellular Biology 22:6, pages 1834-1843.
Read now

Articles from other publishers (69)

Huan Deng, Yamei Chen, Peijing Li, Qingqing Hang, Peng Zhang, Ying Jin & Ming Chen. (2023) PI3K/AKT/mTOR pathway, hypoxia, and glucose metabolism: Potential targets to overcome radioresistance in small cell lung cancer. Cancer Pathogenesis and Therapy 1:1, pages 56-66.
Crossref
Mehtap Kilic Eren. 2023. Hypoxia in Cancer: Significance and Impact on Cancer Therapy. Hypoxia in Cancer: Significance and Impact on Cancer Therapy 89 117 .
Tian Huan, Hongbo Li & Bin Tang. (2022) Radiotherapy plus CAR-T cell therapy to date: A note for cautions optimism?. Frontiers in Immunology 13.
Crossref
Cheng Wang, Changxi Qi, Mingchao Liu, Lumei Wang, Guodong Cheng, Liping Li, Yuxiao Xing, Xiaona Zhao & Jianzhu Liu. (2021) Protective effects of agrimonolide on hypoxia‐induced H9c2 cell injury by maintaining mitochondrial homeostasis. Journal of Cellular Biochemistry 123:2, pages 306-321.
Crossref
Rajnish Kumar Singh, Yonggang Pei, Dipayan Bose, Zachary L Lamplugh, Kunfeng Sun, Yan Yuan, Paul Lieberman, Jianxin You & Erle S Robertson. (2021) KSHV-encoded vCyclin can modulate HIF1α levels to promote DNA replication in hypoxia. eLife 10.
Crossref
Stig Linder. 2021. Clinical Bioenergetics. Clinical Bioenergetics 547 564 .
Yinrui Lei, Tao Chen, Yeyi Li, Man Shang, Yan Zhang, Yuepeng Jin, Qiujing Yu, Fang Guo & Ting Wang. (2020) O-GlcNAcylation of PFKFB3 is required for tumor cell proliferation under hypoxia. Oncogenesis 9:2.
Crossref
Jonatas Rafael de Oliveira, Samira Esteves Afonso Camargo & Luciane Dias de Oliveira. (2019) Rosmarinus officinalis L. (rosemary) as therapeutic and prophylactic agent. Journal of Biomedical Science 26:1.
Crossref
Eva-Leonne Göttgens, Johan Bussink, Katarzyna B. Leszczynska, Hans Peters, Paul N. Span & Ester M. Hammond. (2019) Inhibition of CDK4/CDK6 Enhances Radiosensitivity of HPV Negative Head and Neck Squamous Cell Carcinomas. International Journal of Radiation Oncology*Biology*Physics 105:3, pages 548-558.
Crossref
Chengyu Li, Zhaojun Liu, Jiaqi Zhou, Xueqin Meng, Shuo Liu, Weijian Li, Xue Zhang, Jilong Zhou, Wang Yao, Chao Dong, Yan Cao, Rongyang Li, Baobao Chen, Aiwen Jiang, Yi Jiang, Caibo Ning, Fang Zhao, Yinghui Wei, Shao-chen Sun, Jingli Tao, Wangjun Wu, Ming Shen & Honglin Liu. (2019) Insulin-like growth factor-I prevents hypoxia-inducible factor-1 alpha-dependent G1/S arrest by activating cyclin E/cyclin-dependent kinase2 via the phoshatidylinositol-3 kinase/AKT/forkhead box O1/Cdkn1b pathway in porcine granulosa cells†. Biology of Reproduction.
Crossref
Hak Rae Lee, Faith Leslie & Samira M. Azarin. (2018) A facile in vitro platform to study cancer cell dormancy under hypoxic microenvironments using CoCl2. Journal of Biological Engineering 12:1.
Crossref
Xiaoya Ma, Huabing Zhang, Xiang Xue & Yatrik M. Shah. (2017) Hypoxia-inducible factor 2α (HIF-2α) promotes colon cancer growth by potentiating Yes-associated protein 1 (YAP1) activity. Journal of Biological Chemistry 292:41, pages 17046-17056.
Crossref
Noushin Nabavi, Kevin L. Bennewith, Andrew Churg, Yuzhuo Wang, Colin C. Collins & Luciano Mutti. (2017) Switching off malignant mesothelioma: exploiting the hypoxic microenvironment. Genes & Cancer 7:11-12, pages 340-354.
Crossref
Rahul Agrawal, Tina P. Dale, Mohammed A. Al-Zubaidi, Prit Benny Malgulwar, Nicholas R. Forsyth & Ritu Kulshreshtha. (2016) Pluripotent and Multipotent Stem Cells Display Distinct Hypoxic miRNA Expression Profiles. PLOS ONE 11:10, pages e0164976.
Crossref
Sanjay Kumar & Meenal Vaidya. (2016) Hypoxia inhibits mesenchymal stem cell proliferation through HIF1α-dependent regulation of P27. Molecular and Cellular Biochemistry 415:1-2, pages 29-38.
Crossref
Heidi Högel, Petra Miikkulainen, Lucia Bino & Panu M. Jaakkola. (2015) Hypoxia inducible prolyl hydroxylase PHD3 maintains carcinoma cell growth by decreasing the stability of p27. Molecular Cancer 14:1.
Crossref
S. Sathya, S. Sudhagar & B.S. Lakshmi. (2015) Estrogen suppresses breast cancer proliferation through GPER / p38 MAPK axis during hypoxia. Molecular and Cellular Endocrinology 417, pages 200-210.
Crossref
Kirti Bhatt, Qingqing Wei, Navjotsingh Pabla, Guie Dong, Qing-Sheng Mi, Mingyu Liang, Changlin Mei & Zheng Dong. (2015) MicroRNA-687 Induced by Hypoxia-Inducible Factor-1 Targets Phosphatase and Tensin Homolog in Renal Ischemia-Reperfusion Injury. Journal of the American Society of Nephrology 26:7, pages 1588-1596.
Crossref
P. Guerrero & T. Alarcón. (2015) Stochastic Multiscale Models of Cell Population Dynamics: Asymptotic and Numerical Methods. Mathematical Modelling of Natural Phenomena 10:1, pages 64-93.
Crossref
Anne LeZachary E. Stine, Christopher NguyenJunaid AfzalPeng SunMax HamakerNicholas M. SiegelArvin M. GouwByung-hak KangShu-Han YuRory L. Cochran, Kurt A. Sailor, Hongjun Song & Chi V. Dang. (2014) Tumorigenicity of hypoxic respiring cancer cells revealed by a hypoxia–cell cycle dual reporter. Proceedings of the National Academy of Sciences 111:34, pages 12486-12491.
Crossref
B. Bedessem & A. Stéphanou. (2014) A mathematical model of HiF-1-mediated response to hypoxia on the G1/S transition. Mathematical Biosciences 248, pages 31-39.
Crossref
L Martin, M Rainey, C Santocanale & L B Gardner. (2011) Hypoxic activation of ATR and the suppression of the initiation of DNA replication through cdc6 degradation. Oncogene 31:36, pages 4076-4084.
Crossref
James P. Bridges, Sui Lin, Machiko Ikegami & John M. Shannon. (2012) Conditional hypoxia inducible factor-1α induction in embryonic pulmonary epithelium impairs maturation and augments lymphangiogenesis. Developmental Biology 362:1, pages 24-41.
Crossref
Can Tan, Li-Yang Zhang, Hong Chen, Ling Xiao, Xian-Peng Liu & Jian-Xiang Zhang. (2011) Overexpression of the human ubiquitin E3 ligase CUL4A alleviates hypoxia–reoxygenation injury in pheochromocytoma (PC12) cells. Biochemical and Biophysical Research Communications 416:3-4, pages 403-408.
Crossref
Jiangli Dou, Pan Ma, Chuannan Xiong, Chengyu Tan & Yuguang Du. (2011) Induction of apoptosis in human acute leukemia HL-60 cells by oligochitosan through extrinsic and intrinsic pathway. Carbohydrate Polymers 86:1, pages 19-24.
Crossref
Malini S. Pillai, S. Sapna & K. Shivakumar. (2011) p38 MAPK regulates G1-S transition in hypoxic cardiac fibroblasts. The International Journal of Biochemistry & Cell Biology 43:6, pages 919-927.
Crossref
Scott M. Welford & Amato J. Giaccia. (2011) Hypoxia and Senescence: The Impact of Oxygenation on Tumor Suppression. Molecular Cancer Research 9:5, pages 538-544.
Crossref
Ester M. Hammond, Monica Olcina & Amato J. Giaccia. 2011. Molecular Determinants of Radiation Response. Molecular Determinants of Radiation Response 127 141 .
Vinita A. Hajeri, Brent A. Little, Mary L. Ladage & Pamela A. Padilla. (2010) NPP-16/Nup50 Function and CDK-1 Inactivation Are Associated with Anoxia-induced Prophase Arrest in Caenorhabditis elegans. Molecular Biology of the Cell 21:5, pages 712-724.
Crossref
Isabel M. Pires, Zuzana Bencokova, Manuela Milani, Lisa K. Folkes, Ji-Liang Li, Mike R. Stratford, Adrian L. Harris & Ester M. Hammond. (2010) Effects of Acute versus Chronic Hypoxia on DNA Damage Responses and Genomic Instability. Cancer Research 70:3, pages 925-935.
Crossref
Lesley QuintosIn Ae LeeHyo Jung KimJi-Sun LimJia ParkMi-Kyung Sung, Young Rok SeoJong-Sang Kim. (2010) Significance of p27 kip1 as potential biomarker for intracellular oxidative status . Nutrition Research and Practice 4:5, pages 351.
Crossref
Young-Kwon Park & Hyunsung Park. (2010) Prevention of CCAAT/Enhancer-binding Protein β DNA Binding by Hypoxia during Adipogenesis. Journal of Biological Chemistry 285:5, pages 3289-3299.
Crossref
Xin Huang, Lianghao Ding, Kevin L. Bennewith, Ricky T. Tong, Scott M. Welford, K. Kian Ang, Michael Story, Quynh-Thu Le & Amato J. Giaccia. (2009) Hypoxia-Inducible mir-210 Regulates Normoxic Gene Expression Involved in Tumor Initiation. Molecular Cell 35:6, pages 856-867.
Crossref
Aylin Sar, Dragana Ponjevic, Monica Nguyen, Adrian Harold Box & Douglas James Demetrick. (2009) Identification and characterization of demethylase JMJD1A as a gene upregulated in the human cellular response to hypoxia. Cell and Tissue Research 337:2, pages 223-234.
Crossref
Mathew L Coleman & Peter J Ratcliffe. (2009) Angiogenesis: escape from hypoxia. Nature Medicine 15:5, pages 491-493.
Crossref
Myungmi Oh, Takeshi Tanaka, Masato Kobayashi, Takako Furukawa, Tetsuya Mori, Takashi Kudo, Shigeharu Fujieda & Yasuhisa Fujibayashi. (2009) Radio-copper-labeled Cu-ATSM: an indicator of quiescent but clonogenic cells under mild hypoxia in a Lewis lung carcinoma model. Nuclear Medicine and Biology 36:4, pages 419-426.
Crossref
Marzia Scortegagna, Rebecca J. Martin, Raleigh D. Kladney, Robert G. Neumann & Jeffrey M. Arbeit. (2009) Hypoxia-Inducible Factor-1α Suppresses Squamous Carcinogenic Progression and Epithelial-Mesenchymal Transition. Cancer Research 69:6, pages 2638-2646.
Crossref
Adrian Harold BoxCarol YuenDragana PonjevicGordon H. FickDouglas James Demetrick. (2008) Signaling and apoptosis differences between severe hypoxia and desferoxamine treatment of human epithelial cells. Biochemistry and Cell Biology 86:5, pages 425-436.
Crossref
Ji-Hong Lim, Yoon-Mi Lee, Yang-Sook Chun & Jong-Wan Park. (2008) Reactive oxygen species-mediated cyclin D1 degradation mediates tumor growth retardation in hypoxia, independently of p21 cip1 and hypoxia-inducible factor . Cancer Science, pages ???-???.
Crossref
Regina M. Young, Shang-Jui Wang, John D. Gordan, Xinjun Ji, Stephen A. Liebhaber & M. Celeste Simon. (2008) Hypoxia-mediated Selective mRNA Translation by an Internal Ribosome Entry Site-independent Mechanism. Journal of Biological Chemistry 283:24, pages 16309-16319.
Crossref
Julie Basu Ray, Sara Arab, Yupu Deng, Peter Liu, Linda Penn, David W. Courtman & Michael E. Ward. (2008) Oxygen regulation of arterial smooth muscle cell proliferation and survival. American Journal of Physiology-Heart and Circulatory Physiology 294:2, pages H839-H852.
Crossref
Chi V. Dang, Jung-whan Kim, Ping Gao & Jason Yustein. (2008) The interplay between MYC and HIF in cancer. Nature Reviews Cancer 8:1, pages 51-56.
Crossref
N Horrée, EH Gort, P van der Groep, APM Heintz, M Vooijs & PJ van Diest. (2008) Hypoxia-inducible factor 1α is essential for hypoxic p27 induction in endometrioid endometrial carcinoma. The Journal of Pathology 214:1, pages 38-45.
Crossref
Ranjit S. Bindra, Meredith E. Crosby & Peter M. Glazer. (2007) Regulation of DNA repair in hypoxic cancer cells. Cancer and Metastasis Reviews 26:2, pages 249-260.
Crossref
An Wouters, Bea Pauwels, Filip Lardon & Jan B. Vermorken. (2007) Review: Implications of In Vitro Research on the Effect of Radiotherapy and Chemotherapy Under Hypoxic Conditions. The Oncologist 12:6, pages 690-712.
Crossref
Amber Buescher Johnson & Michelle Craig Barton. (2007) Hypoxia-induced and stress-specific changes in chromatin structure and function. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 618:1-2, pages 149-162.
Crossref
John D. Gordan, Jessica A. Bertout, Cheng-Jun Hu, J. Alan Diehl & M. Celeste Simon. (2007) HIF-2α Promotes Hypoxic Cell Proliferation by Enhancing c-Myc Transcriptional Activity. Cancer Cell 11:4, pages 335-347.
Crossref
HELEN M. BYRNE, MARKUS R. OWEN, TOMAS ALARCON, JAMES MURPHY & PHILIP K. MAINI. (2011) MODELLING THE RESPONSE OF VASCULAR TUMOURS TO CHEMOTHERAPY: A MULTISCALE APPROACH. Mathematical Models and Methods in Applied Sciences 16:supp01, pages 1219-1241.
Crossref
Ester M. Hammond, Rachel A. Freiberg & Amato J. Giaccia. (2006) The roles of Chk 1 and Chk 2 in hypoxia and reoxygenation. Cancer Letters 238:2, pages 161-167.
Crossref
Lunyin Yu, Deborah A. Quinn, Hari G. Garg & Charles A. Hales. (2006) Gene expression of cyclin-dependent kinase inhibitors and effect of heparin on their expression in mice with hypoxia-induced pulmonary hypertension. Biochemical and Biophysical Research Communications 345:4, pages 1565-1572.
Crossref
Rob Cairns, Ioanna Papandreou & Nicholas Denko. (2006) Overcoming Physiologic Barriers to Cancer Treatment by Molecularly Targeting the Tumor Microenvironment. Molecular Cancer Research 4:2, pages 61-70.
Crossref
Barbara Bedogni, Scott M. Welford, David S. Cassarino, Brian J. Nickoloff, Amato J. Giaccia & Marianne Broome Powell. (2005) The hypoxic microenvironment of the skin contributes to Akt-mediated melanocyte transformation. Cancer Cell 8:6, pages 443-454.
Crossref
N. Aravindan, M. T. Williams, B. J. C. J. Riedel & A. D. Shaw. (2005) Transcriptional responses of rat skeletal muscle following hypoxia-reoxygenation and near ischaemia-reperfusion. Acta Physiologica Scandinavica 183:4, pages 367-377.
Crossref
Andreja Budde, Nicole Schneiderhan-Marra, Gabriele Petersen & Bernhard Brüne. (2005) Retinoblastoma susceptibility gene product pRB activates hypoxia-inducible factor-1 (HIF-1). Oncogene 24:10, pages 1802-1808.
Crossref
Ioanna Papandreou, Ashley Powell, Ai Lin Lim & Nicholas Denko. (2005) Cellular reaction to hypoxia: sensing and responding to an adverse environment. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 569:1-2, pages 87-100.
Crossref
Ranjit S. Bindra & Peter M. Glazer. (2005) Genetic instability and the tumor microenvironment: towards the concept of microenvironment-induced mutagenesis. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 569:1-2, pages 75-85.
Crossref
Michael Murphy, J. Andrew Carlson, Martin P. Keough, Kevin P. Claffey, Sabina Signoretti & Massimo Loda. (2004) Hypoxia regulation of the cell cycle in malignant melanoma: putative role for the cyclin-dependent kinase inhibitor p27 Kip1 . Journal of Cutaneous Pathology 31:7, pages 477-482.
Crossref
Ester M. Hammond & Amato J. Giaccia. (2004) The role of ATM and ATR in the cellular response to hypoxia and re-oxygenation. DNA Repair 3:8-9, pages 1117-1122.
Crossref
Charles S. Powell, Marcienne M. Wright & Robert M. Jackson. (2004) p38 mapk and MEK1/2 inhibition contribute to cellular oxidant injury after hypoxia . American Journal of Physiology-Lung Cellular and Molecular Physiology 286:4, pages L826-L833.
Crossref
William H. Stotz, Dechun Li & Roger A. Johns. (2004) Exogenous Nitric Oxide Upregulates p21<sup>waf1/cip1</sup> in Pulmonary Microvascular Smooth Muscle Cells. Journal of Vascular Research 41:3, pages 211-219.
Crossref
M.Christiane Brahimi-Horn & Jacques Pouysségur. 2004. 157 213 .
Jörg Hänze, Bastian G Eul, Rajkumar Savai, Stefanie Krick, Parag Goyal, Friedrich Grimminger, Werner Seeger & Frank Rose. (2003) RNA interference for HIF-1α inhibits its downstream signalling and affects cellular proliferation. Biochemical and Biophysical Research Communications 312:3, pages 571-577.
Crossref
Gang Wang, Richard Reisdorph, Robert E. Clark, Robin Miskimins, Ronald Lindahl & W. Keith Miskimins. (2003) Cyclin dependent kinase inhibitor p27Kip1 is upregulated by hypoxia via an ARNT dependent pathway. Journal of Cellular Biochemistry 90:3, pages 548-560.
Crossref
Nobuhito Goda, Sara J. Dozier & Randall S. Johnson. (2003) HIF-1 in Cell Cycle Regulation, Apoptosis, and Tumor Progression. Antioxidants & Redox Signaling 5:4, pages 467-473.
Crossref
Aoife M Shannon, David J Bouchier-Hayes, Claire M Condron & Deirdre Toomey. (2003) Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treatment Reviews 29:4, pages 297-307.
Crossref
R. M. Douglas & G. G. Haddad. (2003) Invited Review: Effect of oxygen deprivation on cell cycle activity: a profile of delay and arrest. Journal of Applied Physiology 94:5, pages 2068-2083.
Crossref
T.I. Goonewardene, H.M. Sowter & A.L. Harris. (2002) Hypoxia-induced pathways in breast cancer. Microscopy Research and Technique 59:1, pages 41-48.
Crossref
Adrian L. Harris. (2002) Hypoxia — a key regulatory factor in tumour growth. Nature Reviews Cancer 2:1, pages 38-47.
Crossref
Pamela A. Padilla & Mark B. Roth. (2001) Oxygen deprivation causes suspended animation in the zebrafish embryo. Proceedings of the National Academy of Sciences 98:13, pages 7331-7335.
Crossref

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.