Molecular Mechanisms of p63-Mediated Squamous Cancer Pathogenesis

Moses, Michael A.; George, Andrea L.; Sakakibara, Nozomi; Mahmood, Kanwal; Ponnamperuma, Roshini M.; King, Kathryn E.; Weinberg, Wendy C.

doi:10.3390/ijms20143590

Molecular Mechanisms of p63-Mediated Squamous Cancer Pathogenesis

Journal Article · Mon Jul 01 00:00:00 EDT 2019 · International Journal of Molecular Sciences (Online)

DOI:https://doi.org/10.3390/ijms20143590· OSTI ID:1628384

Moses, Michael A. ^[1]; ^[2]; Sakakibara, Nozomi ^[2]; Mahmood, Kanwal ^[2]; Ponnamperuma, Roshini M. ^[2]; King, Kathryn E. ^[2]; Weinberg, Wendy C. ^[2]

U.S. Food and Drug Administration, Silver Spring, MD (United States). Laboratory of Molecular Oncology, Office of Biotechnology Products, Center for Drug Evaluation and Research; DOE/OSTI
U.S. Food and Drug Administration, Silver Spring, MD (United States). Laboratory of Molecular Oncology, Office of Biotechnology Products, Center for Drug Evaluation and Research

The p63 gene is a member of the p53/p63/p73 family of transcription factors and plays a critical role in development and homeostasis of squamous epithelium. p63 is transcribed as multiple isoforms; ΔNp63α, the predominant p63 isoform in stratified squamous epithelium, is localized to the basal cells and is overexpressed in squamous cell cancers of multiple organ sites, including skin, head and neck, and lung. Further, p63 is considered a stem cell marker, and within the epidermis, ΔNp63α directs lineage commitment. ΔNp63α has been implicated in numerous processes of skin biology that impact normal epidermal homeostasis and can contribute to squamous cancer pathogenesis by supporting proliferation and survival with roles in blocking terminal differentiation, apoptosis, and senescence, and influencing adhesion and migration. ΔNp63α overexpression may also influence the tissue microenvironment through remodeling of the extracellular matrix and vasculature, as well as by enhancing cytokine and chemokine secretion to recruit pro-inflammatory infiltrate. This review focuses on the role of ΔNp63α in normal epidermal biology and how dysregulation can contribute to cutaneous squamous cancer development, drawing from knowledge also gained by squamous cancers from other organ sites that share p63 overexpression as a defining feature.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: NCI/FDA Interagency Oncology Task Force (IOTF) Fellowship program; Research Participation Program at the Center for Drug Evaluation and Research; U.S. Food and Drug Administration; USDOE Office of Science (SC)

Grant/Contract Number:: SC0014664

OSTI ID:: 1628384

Journal Information:: International Journal of Molecular Sciences (Online), Journal Name: International Journal of Molecular Sciences (Online) Journal Issue: 14 Vol. 20; ISSN IJMCFK; ISSN 1422-0067

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

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p63 in Squamous Cell Carcinoma of the Skin: More Than a Stem Cell/Progenitor Marker Missero, Caterina; Antonini, Dario Journal of Investigative Dermatology, Vol. 137, Issue 2 https://doi.org/10.1016/j.jid.2016.10.032	journal	February 2017
PFKFB3, a Direct Target of p63, Is Required for Proliferation and Inhibits Differentiation in Epidermal Keratinocytes Hamanaka, Robert B.; Mutlu, Gökhan M. Journal of Investigative Dermatology, Vol. 137, Issue 6 https://doi.org/10.1016/j.jid.2016.12.020	journal	June 2017
TAp63 Prevents Premature Aging by Promoting Adult Stem Cell Maintenance Su, Xiaohua; Paris, Maryline; Gi, Young Jin Cell Stem Cell, Vol. 5, Issue 1 https://doi.org/10.1016/j.stem.2009.04.003	journal	July 2009
ΔNp63α Is an Oncogene that Targets Chromatin Remodeler Lsh to Drive Skin Stem Cell Proliferation and Tumorigenesis Keyes, William M.; Pecoraro, Matteo; Aranda, Victoria Cell Stem Cell, Vol. 8, Issue 2 https://doi.org/10.1016/j.stem.2010.12.009	journal	February 2011
p63 is a p53 homologue required for limb and epidermal morphogenesis Mills, Alea A.; Zheng, Binhai; Wang, Xiao-Jing Nature, Vol. 398, Issue 6729 https://doi.org/10.1038/19531	journal	April 1999
Conformational stability and activity of p73 require a second helix in the tetramerization domain Coutandin, D.; Löhr, F.; Niesen, F. H. Cell Death & Differentiation, Vol. 16, Issue 12 https://doi.org/10.1038/cdd.2009.139	journal	September 2009
iASPP/p63 autoregulatory feedback loop is required for the homeostasis of stratified epithelia: iASPP/p63 axis in skin stratification Chikh, Anissa; Matin, Rubeta N. H.; Senatore, Valentina The EMBO Journal, Vol. 30, Issue 20 https://doi.org/10.1038/emboj.2011.302	journal	September 2011
Transcriptional Repression of miR-34 Family Contributes to p63-Mediated Cell Cycle Progression in Epidermal Cells Antonini, Dario; Russo, Monia T.; De Rosa, Laura Journal of Investigative Dermatology, Vol. 130, Issue 5 https://doi.org/10.1038/jid.2009.438	journal	May 2010
SOX2 controls tumour initiation and cancer stem-cell functions in squamous-cell carcinoma Boumahdi, Soufiane; Driessens, Gregory; Lapouge, Gaelle Nature, Vol. 511, Issue 7508 https://doi.org/10.1038/nature13305	journal	June 2014
p63 regulates an adhesion programme and cell survival in epithelial cells Carroll, Danielle K.; Carroll, Jason S.; Leong, Chee-Onn Nature Cell Biology, Vol. 8, Issue 6 https://doi.org/10.1038/ncb1420	journal	May 2006
Emerging roles of proteases in tumour suppression López-Otín, Carlos; Matrisian, Lynn M. Nature Reviews Cancer, Vol. 7, Issue 10 https://doi.org/10.1038/nrc2228	journal	October 2007
ZNF185 is a p63 target gene critical for epidermal differentiation and squamous cell carcinoma development Smirnov, Artem; Lena, Anna Maria; Cappello, Angela Oncogene, Vol. 38, Issue 10 https://doi.org/10.1038/s41388-018-0509-4	journal	October 2018
Combining precision medicine and prophylaxis in oesophageal squamous cell carcinoma Baxter, Mark A.; Spender, Lindsay C.; Petty, Russell D. British Journal of Cancer, Vol. 123, Issue 11 https://doi.org/10.1038/s41416-020-01057-3	journal	September 2020
A genomic and epigenomic atlas of prostate cancer in Asian populations Li, Jing; Xu, Chuanliang; Lee, Hyung Joo Nature, Vol. 580, Issue 7801 https://doi.org/10.1038/s41586-020-2135-x	journal	March 2020
Delineation of the ADULT syndrome phenotype due to arginine 298 mutations of the p63 gene Rinne, Tuula; Spadoni, Emanuela; Kjaer, Klaus W. European Journal of Human Genetics, Vol. 14, Issue 8 https://doi.org/10.1038/sj.ejhg.5201640	journal	May 2006
A Functional Enhancer of Keratin14 Is a Direct Transcriptional Target of ΔNp63 Romano, Rose-Anne; Birkaya, Barbara; Sinha, Satrajit Journal of Investigative Dermatology, Vol. 127, Issue 5 https://doi.org/10.1038/sj.jid.5700652	journal	May 2007
p63α and ΔNp63α can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes Dohn, Michael; Zhang, Shungzhen; Chen, Xinbin Oncogene, Vol. 20, Issue 25 https://doi.org/10.1038/sj.onc.1204427	journal	May 2001
p63 identifies keratinocyte stem cells Pellegrini, G.; Dellambra, E.; Golisano, O. Proceedings of the National Academy of Sciences, Vol. 98, Issue 6 https://doi.org/10.1073/pnas.061032098	journal	March 2001
Repression of p63 and induction of EMT by mutant Ras in mammary epithelial cells Yoh, Kathryn E.; Regunath, Kausik; Guzman, Asja Proceedings of the National Academy of Sciences, Vol. 113, Issue 41 https://doi.org/10.1073/pnas.1613417113	journal	September 2016
ΔNp63-mediated regulation of hyaluronic acid metabolism and signaling supports HNSCC tumorigenesis Compagnone, Mirco; Gatti, Veronica; Presutti, Dario Proceedings of the National Academy of Sciences, Vol. 114, Issue 50 https://doi.org/10.1073/pnas.1711777114	journal	November 2017
Physical and Functional Interaction between p53 Mutants and Different Isoforms of p73 Strano, Sabrina; Munarriz, Eliana; Rossi, Mario Journal of Biological Chemistry, Vol. 275, Issue 38 https://doi.org/10.1074/jbc.M003360200	journal	July 2000
p63 Suppresses Non-epidermal Lineage Markers in a Bone Morphogenetic Protein-dependent Manner via Repression of Smad7 De Rosa, Laura; Antonini, Dario; Ferone, Giustina Journal of Biological Chemistry, Vol. 284, Issue 44 https://doi.org/10.1074/jbc.M109.049619	journal	August 2009
The p63 Protein Isoform ΔNp63α Modulates Y-box Binding Protein 1 in Its Subcellular Distribution and Regulation of Cell Survival and Motility Genes Di Costanzo, Antonella; Troiano, Annaelena; di Martino, Orsola Journal of Biological Chemistry, Vol. 287, Issue 36 https://doi.org/10.1074/jbc.M112.349951	journal	July 2012
The p63 Protein Isoform ΔNp63α Inhibits Epithelial-Mesenchymal Transition in Human Bladder Cancer Cells: ROLE OF MIR-205 Tran, Mai N.; Choi, Woonyoung; Wszolek, Matthew F. Journal of Biological Chemistry, Vol. 288, Issue 5 https://doi.org/10.1074/jbc.M112.408104	journal	December 2012
Physical Interaction with Human Tumor-derived p53 Mutants Inhibits p63 Activities Strano, Sabrina; Fontemaggi, Giulia; Costanzo, Antonio Journal of Biological Chemistry, Vol. 277, Issue 21 https://doi.org/10.1074/jbc.M201405200	journal	March 2002
p63α Mutations Lead to Aberrant Splicing of Keratinocyte Growth Factor Receptor in the Hay-Wells Syndrome Fomenkov, Alexey; Huang, Yi-Ping; Topaloglu, Ozlem Journal of Biological Chemistry, Vol. 278, Issue 26 https://doi.org/10.1074/jbc.M300746200	journal	April 2003
The Unique NH ₂ -terminally Deleted (ΔN) Residues, the P XX P Motif, and the PP X Y Motif Are Required for the Transcriptional Activity of the ΔN Variant of p63 Helton, E. Scott; Zhu, Jianhui; Chen, Xinbin Journal of Biological Chemistry, Vol. 281, Issue 5 https://doi.org/10.1074/jbc.M507964200	journal	November 2005
GPX2, a Direct Target of p63, Inhibits Oxidative Stress-induced Apoptosis in a p53-dependent Manner Yan, Wensheng; Chen, Xinbin Journal of Biological Chemistry, Vol. 281, Issue 12 https://doi.org/10.1074/jbc.M512655200	journal	January 2006
p63 regulates Satb1 to control tissue-specific chromatin remodeling during development of the epidermis Fessing, Michael Y.; Mardaryev, Andrei N.; Gdula, Michal R. Journal of Cell Biology, Vol. 194, Issue 6 https://doi.org/10.1083/jcb.201101148	journal	September 2011
p63 Induces CD4 ⁺ T-Cell Chemoattractant TARC/CCL17 in Human Epithelial Cells Kubo, Terufumi; Ichimiya, Shingo; Tonooka, Akiko Journal of Interferon & Cytokine Research, Vol. 28, Issue 12 https://doi.org/10.1089/jir.2008.0035	journal	December 2008
Hay-Wells syndrome is caused by heterozygous missense mutations in the SAM domain of p63 McGrath, J. A. Human Molecular Genetics, Vol. 10, Issue 3 https://doi.org/10.1093/hmg/10.3.221	journal	February 2001
p53 Family members p63 and p73 are SAM domain-containing proteins Thanos, Christopher D.; Bowie, James U. Protein Science, Vol. 8, Issue 8 https://doi.org/10.1110/ps.8.8.1708	journal	January 1999
SATB1 promotes tumor metastasis and invasiveness in oral squamous cell carcinoma Li, Y-C; Bu, L-L; Mao, L. Oral Diseases, Vol. 23, Issue 2 https://doi.org/10.1111/odi.12602	journal	November 2016
Integrative Analysis of Complex Cancer Genomics and Clinical Profiles Using the cBioPortal Gao, J.; Aksoy, B. A.; Dogrusoz, U. Science Signaling, Vol. 6, Issue 269 https://doi.org/10.1126/scisignal.2004088	journal	March 2013
Maintaining epithelial stemness with p63 Melino, Gerry; Memmi, Elisa Maria; Pelicci, Pier Giuseppe Science Signaling, Vol. 8, Issue 387 https://doi.org/10.1126/scisignal.aaa1033	journal	July 2015
Stxbp4 Regulates ΔNp63 Stability by Suppression of RACK1-Dependent Degradation Li, Yingchun; Peart, Melissa J.; Prives, Carol Molecular and Cellular Biology, Vol. 29, Issue 14 https://doi.org/10.1128/MCB.00449-09	journal	May 2009
A C-Terminal Inhibitory Domain Controls the Activity of p63 by an Intramolecular Mechanism Serber, Zach; Lai, Helen C.; Yang, Annie Molecular and Cellular Biology, Vol. 22, Issue 24 https://doi.org/10.1128/MCB.22.24.8601-8611.2002	journal	December 2002
Complex Transcriptional Effects of p63 Isoforms: Identification of Novel Activation and Repression Domains† Ghioni, Pamela; Bolognese, Fabrizio; Duijf, Pascal H. G. Molecular and Cellular Biology, Vol. 22, Issue 24 https://doi.org/10.1128/MCB.22.24.8659-8668.2002	journal	December 2002
Differential Recognition of Response Elements Determines Target Gene Specificity forp53 and p63 Osada, Motonobu; Park, Hannah Lui; Nagakawa, Yuichi Molecular and Cellular Biology, Vol. 25, Issue 14 https://doi.org/10.1128/MCB.25.14.6077-6089.2005	journal	July 2005
The p53 Homologue Np63 Interacts with the Nuclear Factor- B Pathway to Modulate Epithelial Cell Growth King, K. E.; Ponnamperuma, R. M.; Allen, C. Cancer Research, Vol. 68, Issue 13 https://doi.org/10.1158/0008-5472.CAN-07-6123	journal	July 2008
Np63 Versatilely Regulates a Broad NF- B Gene Program and Promotes Squamous Epithelial Proliferation, Migration, and Inflammation Yang, X.; Lu, H.; Yan, B. Cancer Research, Vol. 71, Issue 10 https://doi.org/10.1158/0008-5472.CAN-10-3445	journal	May 2011
Physical Association of HDAC1 and HDAC2 with p63 Mediates Transcriptional Repression and Tumor Maintenance in Squamous Cell Carcinoma Ramsey, M. R.; He, L.; Forster, N. Cancer Research, Vol. 71, Issue 13 https://doi.org/10.1158/0008-5472.CAN-11-0046	journal	April 2011
TNF- Promotes c-REL/ Np63 Interaction and TAp73 Dissociation from Key Genes That Mediate Growth Arrest and Apoptosis in Head and Neck Cancer Lu, H.; Yang, X.; Duggal, P. Cancer Research, Vol. 71, Issue 21 https://doi.org/10.1158/0008-5472.CAN-11-2460	journal	September 2011
Np63 Silences a miRNA Program to Aberrantly Initiate a Wound-Healing Program That Promotes TGF -Induced Metastasis Rodriguez Calleja, L.; Jacques, C.; Lamoureux, F. Cancer Research, Vol. 76, Issue 11 https://doi.org/10.1158/0008-5472.CAN-15-2317	journal	March 2016
Transglutaminase Interaction with α6/β4-Integrin Stimulates YAP1-Dependent ΔNp63α Stabilization and Leads to Enhanced Cancer Stem Cell Survival and Tumor Formation Fisher, Matthew L.; Kerr, Candace; Adhikary, Gautam Cancer Research, Vol. 76, Issue 24 https://doi.org/10.1158/0008-5472.CAN-16-2032	journal	October 2016
Genomic Analysis of Metastatic Cutaneous Squamous Cell Carcinoma Li, Y. Y.; Hanna, G. J.; Laga, A. C. Clinical Cancer Research, Vol. 21, Issue 6 https://doi.org/10.1158/1078-0432.CCR-14-1773	journal	January 2015
ΔNp63γ/SRC/Slug Signaling Axis Promotes Epithelial-to-Mesenchymal Transition in Squamous Cancers Srivastava, Kirtiman; Pickard, Adam; Craig, Stephanie G. Clinical Cancer Research, Vol. 24, Issue 16 https://doi.org/10.1158/1078-0432.CCR-17-3775	journal	May 2018
The cBio Cancer Genomics Portal: An Open Platform for Exploring Multidimensional Cancer Genomics Data: Figure 1. Cerami, Ethan; Gao, Jianjiong; Dogrusoz, Ugur Cancer Discovery, Vol. 2, Issue 5 https://doi.org/10.1158/2159-8290.CD-12-0095	journal	May 2012
A microRNA-dependent program controls p53-independent survival and chemosensitivity in human and murine squamous cell carcinoma Ory, Benjamin; Ramsey, Matthew R.; Wilson, Catherine Journal of Clinical Investigation, Vol. 121, Issue 2 https://doi.org/10.1172/JCI43897	journal	February 2011
FGFR2 signaling underlies p63 oncogenic function in squamous cell carcinoma Ramsey, Matthew R.; Wilson, Catherine; Ory, Benjamin Journal of Clinical Investigation, Vol. 123, Issue 8 https://doi.org/10.1172/JCI68899	journal	July 2013
SOX2 and p63 colocalize at genetic loci in squamous cell carcinomas Watanabe, Hideo; Ma, Qiuping; Peng, Shouyong Journal of Clinical Investigation, Vol. 124, Issue 4 https://doi.org/10.1172/JCI71545	journal	March 2014
ΔNp63-driven recruitment of myeloid-derived suppressor cells promotes metastasis in triple-negative breast cancer Kumar, Sushil; Wilkes, David W.; Samuel, Nina Journal of Clinical Investigation, Vol. 128, Issue 11 https://doi.org/10.1172/JCI99673	journal	September 2018
A crucial role for Fgfr2-IIIb signalling in epidermal development and hair follicle patterning Petiot, A. Development, Vol. 130, Issue 22 https://doi.org/10.1242/dev.00788	journal	November 2003
p63 regulates multiple signalling pathways required for ectodermal organogenesis and differentiation Laurikkala, J. Development, Vol. 133, Issue 8 https://doi.org/10.1242/dev.02325	journal	April 2006
Np63 knockout mice reveal its indispensable role as a master regulator of epithelial development and differentiation Romano, R. -A.; Smalley, K.; Magraw, C. Development, Vol. 139, Issue 4 https://doi.org/10.1242/dev.071191	journal	January 2012
p63 and Brg1 control developmentally regulated higher-order chromatin remodelling at the epidermal differentiation complex locus in epidermal progenitor cells Mardaryev, A. N.; Gdula, M. R.; Yarker, J. L. Development, Vol. 141, Issue 1 https://doi.org/10.1242/dev.103200	journal	December 2013
Δ Np63 knockout mice reveal its indispensable role as a master regulator of epithelial development and differentiation Romano, Rose-Anne; Smalley, Kirsten; Magraw, Caitlin Journal of Cell Science, Vol. 125, Issue 4 https://doi.org/10.1242/jcs.108647	journal	February 2012
Transcription factor p63 bookmarks and regulates dynamic enhancers during epidermal differentiation Kouwenhoven, Evelyn N.; Oti, Martin; Niehues, Hanna EMBO reports, Vol. 16, Issue 7 https://doi.org/10.15252/embr.201439941	journal	June 2015
ROCK ‐dependent phosphorylation of NUP 62 regulates p63 nuclear transport and squamous cell carcinoma proliferation Hazawa, Masaharu; Lin, De‐Chen; Kobayashi, Akiko EMBO reports, Vol. 19, Issue 1 https://doi.org/10.15252/embr.201744523	journal	December 2017
The genetics of cutaneous squamous cell carcinogenesis Campos, Manuel Antonio; Lopes, José Manuel; Soares, Paula European Journal of Dermatology, Vol. 28, Issue 5 https://doi.org/10.1684/ejd.2018.3403	journal	September 2018
TAp63 Prevents Premature Aging by Promoting Adult Stem Cell Maintenance Maryline, Paris,; Xiaohua, Su,; Satrajit, Sinha, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/fhc5-4r40	text	January 2009
ZNF185 is a p63 target gene critical for epidermal differentiation and squamous cell carcinoma development. Smirnov, Artem; Lena, Anna Maria; Cappello, Angela Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.32875	text	January 2019
Anti-Tumor Immunity in Head and Neck Cancer: Understanding the Evidence, How Tumors Escape and Immunotherapeutic Approaches Allen, Clint; Clavijo, Paul; Van Waes, Carter Cancers, Vol. 7, Issue 4 https://doi.org/10.3390/cancers7040900	journal	December 2015
p53 isoforms change p53 paradigm Bourdon, Jc Molecular & Cellular Oncology, Vol. 1, Issue 4 https://doi.org/10.4161/23723548.2014.969136	journal	December 2014
A miR-34a-SIRT6 axis in the squamous cell differentiation network Lefort, Karine; Brooks, Yang; Ostano, Paola Nature Publishing Group https://doi.org/10.5167/uzh-91706	text	January 2013
A novel ATAC-seq approach reveals lineage-specific reinforcement of the open chromatin landscape via cooperation between BAF and p63 Bao, Xiaomin; Rubin, Adam; Qu, Kun Figshare https://doi.org/10.6084/m9.figshare.c.3636329	collection	January 2015

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p63 Is a Promising Marker in the Diagnosis of Unusual Skin Cancer Smirnov, Artem; Anemona, Lucia; Novelli, Flavia International Journal of Molecular Sciences, Vol. 20, Issue 22 https://doi.org/10.3390/ijms20225781	journal	November 2019
Molecular Approach to Cutaneous Squamous Cell Carcinoma: From Pathways to Therapy Palazzo, Elisabetta; Morasso, Maria I.; Pincelli, Carlo International Journal of Molecular Sciences, Vol. 21, Issue 4 https://doi.org/10.3390/ijms21041211	journal	February 2020
Additional file 3 of SYT7 acts as an oncogene and a potential therapeutic target and was regulated by ΔNp63α in HNSCC Fu, You; Tian, Guocai; Zhang, Zhiyuan figshare https://doi.org/10.6084/m9.figshare.17305431	image	January 2021
Additional file 4 of SYT7 acts as an oncogene and a potential therapeutic target and was regulated by ΔNp63α in HNSCC Fu, You; Tian, Guocai; Zhang, Zhiyuan figshare https://doi.org/10.6084/m9.figshare.17305434.v1	image	January 2021
Additional file 5 of SYT7 acts as an oncogene and a potential therapeutic target and was regulated by ΔNp63α in HNSCC Fu, You; Tian, Guocai; Zhang, Zhiyuan figshare https://doi.org/10.6084/m9.figshare.17305440	image	January 2021
ΔNp63 transcript loss in bladder cancer constitutes an independent molecular predictor of TaT1 patients post-treatment relapse and progression Papadimitriou, Maria-Alexandra; Avgeris, Margaritis; Levis, Panagiotis K. Journal of Cancer Research and Clinical Oncology, Vol. 145, Issue 12 https://doi.org/10.1007/s00432-019-03028-5	journal	October 2019

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