Fol. Biol. 2019, 65, 170-180

https://doi.org/10.14712/fb2019065040170

Role of the TAp63 Isoform in Recurrent Nasal Polyps

A. Terrinoni1, R. Palombo1, C. Pitolli1, S. Caporali2, R. De Berardinis3, S. Ciccarone3, A. Lanzillotta3, S. Mauramati4, G. Porta5, M. Minieri1, G. Melino1, Sergio Bernardini1, Ernesto Bruno3

1Department of Experimental Medicine, University of Rome Tor Vergata, Rome, Italy
2Department of Industrial Engineering, University of Rome Tor Vergata, Rome, Italy
3Department of Clinical Sciences and Translational Medicine, University of Rome Tor Vergata, Rome, Italy
4University of Pavia, Italy and Department of Otorhinolaryngology, University of Pavia, Foundation IRCCS Policlinico “San Matteo”, Pavia, Italy
5Department of Medicine and Surgery, University of Insubria, Varese, Italy

Received May 2019
Accepted June 2019

References

1. Akhtar, S., Ikram, M., Azam, I., Dahri, T. (2010) Factors associated with recurrent nasal polyps: a tertiary care experience. J. Pak. Med. Assoc. 60, 102-104.
2. Albu, S., Tomescu, E., Mexca, Z., Nistor, S., Necula, S., Cozlean, A. (2004) Recurrence rates in endonasal surgery for polyposis. Acta Otorhinolaryngol. Belg. 58, 79-86.
3. Arason, A. J., Jonsdottir, H. R., Halldorsson, S., Benediktsdottir, B. E., Bergthorsson, J. T., Ingthorsson, S., Baldursson, O., Sinha, S., Gudjonsson, T., Magnusson, M. K. (2014) ΔNp63 has a role in maintaining epithelial integrity in airway epithelium. PLoS One 9, e88683. <https://doi.org/10.1371/journal.pone.0088683>
4. Bachert, C., Mannent, L., Naclerio, R. M., Mullol, J., Ferguson, B. J., Gevaert, P., Hellings, P., Jiao, L., Wang, L., Evans, R. R., Pirozzi, G., Graham, N. M., Swanson, B., Hamilton, J. D., Radin, A., Gandhi, N. A., Stahl, N., Yancopoulos, G. D., Sutherland, E. R. (2016) Effect of subcutaneous dupilumab on nasal polyp burden in patients with chronic sinusitis and nasal polyposis: a randomized clinical trial. JAMA 315, 469-479. <https://doi.org/10.1001/jama.2015.19330>
5. Bhattacharyya, N. (2007) Influence of polyps on outcomes after endoscopic sinus surgery. Laryngoscope 117, 1834-1838. <https://doi.org/10.1097/MLG.0b013e3180caa19d>
6. Bruno, E., Mohamed, E. I., Alessandrini, M., Russo, S., Schiaroli, S., De Lorenzo, A., Di Girolamo, A. (2002) Longterm follow-up of cellular proliferation as a predictive index for the relapse of nasal polyposis. Am. J. Rhinol. 16, 237-241. <https://doi.org/10.1177/194589240201600501>
7. Bruno, E., Bonmassar, E., Di Girolamo, S., Adamo, R., Alessandrini, M., Ottaviani, F., Rosati, F., Franzese, O. (2004) Evaluation of telomerase activity in nasal polyps. Am. J. Rhinol. 18, 197-201. <https://doi.org/10.1177/194589240401800403>
8. Candi, E., Rufini, A., Terrinoni, A., Dinsdale, D., Ranalli, M., Paradisi, A., De Laurenzi, V., Spagnoli, L. G., Catani, M. V., Ramadan, S., Knight, R. A., Melino, G. (2006a) Differential roles of p63 isoforms in epidermal development: selective genetic complementation in p63 null mice. Cell Death Differ. 13, 1037-1047. <https://doi.org/10.1038/sj.cdd.4401926>
9. Candi, E., Terrinoni, A., Rufini, A., Chikh, A., Lena, A. M.;,Suzuki, Y., Sayan, B. S., Knight, R. A., Melino, G. (2006b) p63 is upstream of IKK α in epidermal development. J. Cell Sci. 119, 4617-4622. <https://doi.org/10.1242/jcs.03265>
10. Candi, E., Dinsdale, D., Rufini, A., Salomoni, P., Knight, R. A., Mueller, M., Krammer, P. H., Melino, G. (2007) TAp63 and ΔNp63 in cancer and epidermal development. Cell Cycle 6, 274-285. <https://doi.org/10.4161/cc.6.3.3797>
11. Carroll, D. K., Carroll, J. S., Leong, C. O., Cheng, F., Brown, M., Mills, A. A., Brugge, J. S., Ellisen, L. W. (2006) p63 regulates an adhesion programme and cell survival in epithelial cells. Nat. Cell Biol. 8, 551-561. <https://doi.org/10.1038/ncb1420>
12. Cerami, E., Gao, J., Dogrusoz, U., Gross, B. E., Sumer, S. O., Aksoy, B. A., Jacobsen, A., Byrne, C. J., Heuer, M. L., Larsson, E., Antipin, Y., Reva, B., Goldberg, A. P., Sander, C., Schultz, N. (2012) The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2, 401-404. <https://doi.org/10.1158/2159-8290.CD-12-0095>
13. Compagnone, M., Gatti, V., Presutti, D., Ruberti, G., Fierro, C., Markert, E. K., Vousden, K. H., Zhou, H., Mauriello, A., Anemone, L., Bongiorno-Borbone, L., Melino, G., Peschiaroli, A. (2017) ΔNp63-mediated regulation of hyaluronic acid metabolism and signaling supports HNSCC tumorigenesis. Proc. Natl. Acad. Sci. USA 114, 13254-13259. <https://doi.org/10.1073/pnas.1711777114>
14. Dennis, S. K., Lam, K., Luong, A. (2016) A review of classification schemes for chronic rhinosinusitis with nasal polyposis endotypes. Laryngoscope Investig. Otolaryngol. 1, 130-134.
15. DeYoung, M. P., Johannessen, C. M., Leong, C. O., Faquin, W., Rocco, J. W., Ellisen, L. W. (2006) Tumor-specific p73 up-regulation mediates p63 dependence in squamous cell carcinoma. Cancer Res. 66, 9362-9368. <https://doi.org/10.1158/0008-5472.CAN-06-1619>
16. Divekar, R., Hagan, J., Rank, M., Park, M., Volcheck, G., O’Brien, E., Meeusen, J., Kita, H., Butterfield, J. (2016) Diagnostic utility of urinary LTE4 in asthma, allergic rhinitis, chronic rhinosinusitis, nasal polyps, and aspirin sensitivity. J. Allergy Clin. Immunol. Pract. 4, 665-670. <https://doi.org/10.1016/j.jaip.2016.03.004>
17. Dohn, M., Zhang, S., Chen, X. (2001) p63α and ΔNp63α can induce cell cycle arrest and apoptosis and differentially regulate p53 target genes. Oncogene 20, 3193-3205. <https://doi.org/10.1038/sj.onc.1204427>
18. Fokkens, W. J., Lund, V. J., Mullol, J., Bachert, C., Alobid, I., Baroody, F., Cohen, N., Cervin, A., Douglas, R., Gevaert, P., Georgalas, C., Goossens, H., Harvey, R., Hellings, P., Hopkins, C., Jones, N., Joos, G., Kalogjera, L., Kern, B., Kowalski, M., Price, D., Riechelmann, H., Schlosser, R., Senior, B., Thomas, M., Toskala, E., Voegels, R., Wang de, Y., Wormald, P. J. (2012a) European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology 50, 1-12. <https://doi.org/10.4193/Rhino12.000>
19. Fokkens, W. J., Lund, V. J., Mullol, J., Bachert, C., Alobid, I., Baroody, F., Cohen, N., Cervin, A., Douglas, R., Gevaert, P., Georgalas, C., Goossens, H., Harvey, R., Hellings, P., Hopkins, C., Jones, N., Joos, G., Kalogjera, L., Kern, B., Kowalski, M., Price, D., Riechelmann, H., Schlosser, R., Senior, B., Thomas, M., Toskala, E., Voegels, R., Wang de, Y., Wormald, P. J. (2012b) European position paper on rhinosinusitis and nasal polyps 2012. Rhinol. Suppl. 3, preceding table of contents, 1-298.
20. Gao, J., Aksoy, B. A., Dogrusoz, U., Dresdner, G., Gross, B., Sumer, S. O., Sun, Y., Jacobsen, A., Sinha, R., Larsson, E., Cerami, E., Sander, C., Schultz, N. (2013) Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci. Signal. 6, pl1. <https://doi.org/10.1126/scisignal.2004088>
21. Gevaert, P., Van Bruaene, N., Cattaert, T., Van Steen, K., Van Zele, T., Acke, F., De Ruyck, N., Blomme, K., Sousa, A. R.;,Marshall, R. P., Bachert, C. (2011) Mepolizumab, a humanized anti-IL-5 mAb, as a treatment option for severe nasal polyposis. J. Allergy Clin. Immunol. 128, 989-995 e981-988. <https://doi.org/10.1016/j.jaci.2011.07.056>
22. Gevaert, P., Calus, L., Van Zele, T., Blomme, K., De Ruyck, N., Bauters, W., Hellings, P., Brusselle, G., De Bacquer, D., van Cauwenberge, P., Bachert, C. (2013) Omalizumab is effective in allergic and nonallergic patients with nasal polyps and asthma. J. Allergy Clin. Immunol. 131, 110-116 e111. <https://doi.org/10.1016/j.jaci.2012.07.047>
23. Giacobbe, A., Bongiorno-Borbone, L., Bernassola, F., Terrinoni, A., Markert, E. K., Levine, A. J., Feng, Z., Agostini, M., Zolla, L., Agro, A. F., Notterman, D. A., Melino, G., Peschiaroli, A. (2013) p63 regulates glutaminase 2 expression. Cell Cycle 12, 1395-1405.
24. Gonfloni, S., Di Tella, L., Caldarola, S., Cannata, S. M., Klinger, F. G., Di Bartolomeo, C., Mattei, M., Candi, E., De Felici, M., Melino, G., Cesareni, G. (2009) Inhibition of the c-Abl-TAp63 pathway protects mouse oocytes from chemotherapy-induced death. Nat. Med. 15, 1179-1185. <https://doi.org/10.1038/nm.2033>
25. Hackett, T. L., Warner, S. M., Stefanowicz, D., Shaheen, F., Pechkovsky, D. V., Murray, L. A., Argentieri, R., Kicic, A., Stick, S. M., Bai, T. R., Knight, D. A. (2009) Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-β 1. Am. J. Respir. Crit. Care Med. 180, 122-133. <https://doi.org/10.1164/rccm.200811-1730OC>
26. Hibi, K., Trink, B., Patturajan, M., Westra, W. H., Caballero, O. L., Hill, D. E., Ratovitski, E. A., Jen, J., Sidransky, D. (2000) AIS is an oncogene amplified in squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 97, 5462-5467. <https://doi.org/10.1073/pnas.97.10.5462>
27. Kaneko, Y., Kohno, T., Kakuki, T., Takano, K. I., Ogasawara, N., Miyata, R., Kikuchi, S., Konno, T., Ohkuni, T., Yajima, R., Kakiuchi, A., Yokota, S. I., Himi, T., Kojima, T. (2017) The role of transcriptional factor p63 in regulation of epithelial barrier and ciliogenesis of human nasal epithelial cells. Sci. Rep. 7, 10935. <https://doi.org/10.1038/s41598-017-11481-w>
28. Koennecke, M., Klimek, L., Mullol, J., Gevaert, P., Wollenberg, B. (2018) Subtyping of polyposis nasi: phenotypes, endotypes and comorbidities. Allergol. J. Int. 27, 56-65. <https://doi.org/10.1007/s40629-017-0048-5>
29. Kojima, T., Go, M., Takano, K., Kurose, M., Ohkuni, T., Koizumi, J., Kamekura, R., Ogasawara, N., Masaki, T., Fuchimoto, J., Obata, K., Hirakawa, S., Nomura, K., Keira, T., Miyata, R., Fujii, N., Tsutsumi, H., Himi, T., Sawada, N. (2013) Regulation of tight junctions in upper airway epithelium. Biomed. Res. Int. 2013, 947072.
30. Langdon, C., Mullol, J. (2016) Nasal polyps in patients with asthma: prevalence, impact, and management challenges. J. Asthma Allergy 9, 45-53.
31. Li, C. W., Shi, L., Zhang, K. K., Li, T. Y., Lin, Z. B., Lim, M. K., McKeon, F., Xian, W., Wang de, Y. (2011) Role of p63/ p73 in epithelial remodeling and their response to steroid treatment in nasal polyposis. J. Allergy Clin. Immunol. 127, 765-772 e761-762. <https://doi.org/10.1016/j.jaci.2010.12.011>
32. Lund, V. J., Flood, J., Sykes, A. P., Richards, D. H. (1998) Effect of fluticasone in severe polyposis. Arch. Otolaryngol. Head Neck Surg. 124, 513-518. <https://doi.org/10.1001/archotol.124.5.513>
33. Massion, P. P., Taflan, P. M., Jamshedur Rahman, S. M., Yildiz, P., Shyr, Y., Edgerton, M. E., Westfall, M. D., Roberts, J. R., Pietenpol, J. A., Carbone, D. P., Gonzalez, A. L. (2003) Significance of p63 amplification and overexpression in lung cancer development and prognosis. Cancer Res. 63, 7113-7121.
34. Melino, G.. Lu, X.. Gasco, M., Crook, T., Knight, R. A. (2003) Functional regulation of p73 and p63: development and cancer. Trends Biochem. Sci. 28, 663-670. <https://doi.org/10.1016/j.tibs.2003.10.004>
35. Mills, A. A., Zheng, B., Wang, X. J., Vogel, H., Roop, D. R., Bradley, A. (1999) p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398, 708-713. <https://doi.org/10.1038/19531>
36. Mills, A. A. (2006) p63: oncogene or tumor suppressor? Curr. Opin. Genet. Dev. 16, 38-44. <https://doi.org/10.1016/j.gde.2005.12.001>
37. Nickoloff, B. J., Qin, J. Z., Chaturvedi, V., Denning, M. F., Bonish, B., Miele, L. (2002) Jagged-1 mediated activation of notch signaling induces complete maturation of human keratinocytes through NF-κB and PPARγ. Cell Death Differ. 9, 842-855. <https://doi.org/10.1038/sj.cdd.4401036>
38. Palombo, R., Porta, G., Bruno, E., Provero, P., Serra, V., Neduri, K., Viziano, A., Alessandrini, M., Micarelli, A., Ottaviani, F., Melino, G., Terrinoni, A. (2015) OTX2 regulates the expression of TAp63 leading to macular and cochlear neuroepithelium development. Aging (Albany NY) 7, 928-936. <https://doi.org/10.18632/aging.100839>
39. Palombo, R., Savini, I., Avigliano, L., Madonna, S., Cavani, A., Albanesi, C., Mauriello, A., Melino, G., Terrinoni, A. (2016) Luteolin-7-glucoside inhibits IL-22/STAT3 pathway, reducing proliferation, acanthosis, and inflammation in keratinocytes and in mouse psoriatic model. Cell Death Dis. 7, e2344. <https://doi.org/10.1038/cddis.2016.201>
40. Pirrone, C., Chiaravalli, A. M., Marando, A., Conti, A., Rainero, A., Pistochini, A., Lo Curto, F., Pasquali, F., Castelnuovo, P., Capella, C., Porta, G. (2017) OTX1 and OTX2 as possible molecular markers of sinonasal carcinomas and olfactory neuroblastomas. Eur. J. Histochem. 61, 2730.
41. Romano, R. A., Smalley, K., Magraw, C., Serna, V. A., Kurita, T., Raghavan, S., Sinha, S. (2012) ΔNp63 knockout mice reveal its indispensable role as a master regulator of epithelial development and differentiation. Development 139, 772-782. <https://doi.org/10.1242/dev.071191>
42. Rouleau, M., Medawar, A., Hamon, L., Shivtiel, S., Wolchinsky, Z., Zhou, H., De Rosa, L., Candi, E., de la Forest Divonne, S., Mikkola, M. L., van Bokhoven, H., Missero, C., Melino, G., Puceat, M., Aberdam, D. (2011) TAp63 is important for cardiac differentiation of embryonic stem cells and heart development. Stem Cells 29, 1672-1683. <https://doi.org/10.1002/stem.723>
43. Rudmik, L., Schlosser, R. J., Smith, T. L., Soler, Z. M. (2012) Impact of topical nasal steroid therapy on symptoms of nasal polyposis: a meta-analysis. Laryngoscope 122, 1431-1437. <https://doi.org/10.1002/lary.23259>
44. Schleimer, R. P. (2017) Immunopathogenesis of chronic rhinosinusitis and nasal polyposis. Annu. Rev. Pathol. 12, 331-357. <https://doi.org/10.1146/annurev-pathol-052016-100401>
45. Sniezek, J. C., Matheny, K. E., Westfall, M. D., Pietenpol, J. A. (2004) Dominant negative p63 isoform expression in head and neck squamous cell carcinoma. Laryngoscope 114, 2063-2072. <https://doi.org/10.1097/01.mlg.0000149437.35855.4b>
46. Soyka, M. B., Wawrzyniak, P., Eiwegger, T., Holzmann, D., Treis, A., Wanke, K., Kast, J. I., Akdis, C. A. (2012) Defective epithelial barrier in chronic rhinosinusitis: the regulation of tight junctions by IFN-γ and IL-4. J. Allergy Clin. Immunol. 130, 1087-1096 e1010. <https://doi.org/10.1016/j.jaci.2012.05.052>
47. Steinke, J. W., Borish, L. (2015) Factors driving the aspirin exacerbated respiratory disease phenotype. Am. J. Rhinol. Allergy 29, 35-40. <https://doi.org/10.2500/ajra.2015.29.4123>
48. Stevens, W. W., Peters, A. T., Suh, L., Norton, J. E., Kern, R. C., Conley, D. B., Chandra, R. K., Tan, B. K., Grammer, L. C., Harris, K. E., Carter, R. G., Kato, A., Urbanek, M., Schleimer, R. P., Hulse, K. E. (2015) A retrospective, crosssectional study reveals that women with CRSwNP have more severe disease than men. Immun. Inflamm. Dis. 3, 14-22. <https://doi.org/10.1002/iid3.46>
49. Stevens, W. W., Schleimer, R. P., Kern, R. C. (2016) Chronic rhinosinusitis with nasal polyps. J. Allergy Clin. Immunol. Pract. 4, 565-572. <https://doi.org/10.1016/j.jaip.2016.04.012>
50. Suh, E. K., Yang, A., Kettenbach, A., Bamberger, C., Michaelis, A. H., Zhu, Z., Elvin, J. A., Bronson, R. T., Crum, C. P., McKeon, F. (2006) p63 protects the female germ line during meiotic arrest. Nature 444, 624-628. <https://doi.org/10.1038/nature05337>
51. Terrinoni, A., Pagani, I. S., Zucchi, I., Chiaravalli, A. M., Serra, V., Rovera, F., Sirchia, S., Dionigi, G., Miozzo, M., Frattini, A., Ferrari, A., Capella, C., Pasquali, F., Curto, F. L., Albertini, A., Melino, G., Porta, G. (2011) OTX1 expression in breast cancer is regulated by p53. Oncogene 30, 3096-3103. <https://doi.org/10.1038/onc.2011.31>
52. Terrinoni, A., Serra, V., Bruno, E., Strasser, A., Valente, E., Flores, E. R., van Bokhoven, H., Lu, X., Knight, R. A., Melino, G. (2013) Role of p63 and the Notch pathway in cochlea development and sensorineural deafness. Proc. Natl. Acad. Sci. USA 110, 7300-7305. <https://doi.org/10.1073/pnas.1214498110>
53. Terrinoni, A., Didona, B., Caporali, S., Chillemi, G., Lo Surdo, A., Paradisi, M., Annichiarico-Petruzzelli, M., Candi, E., Bernardini, S., Melino, G. (2018) Role of the keratin 1 and keratin 10 tails in the pathogenesis of ichthyosis hystrix of Curth Macklin. PLoS One 13, e0195792. <https://doi.org/10.1371/journal.pone.0195792>
54. Tomassen, P., Vandeplas, G., Van Zele, T., Cardell, L. O., Arebro, J., Olze, H., Forster-Ruhrmann, U., Kowalski, M. L., Olszewska-Ziaber, A., Holtappels, G., De Ruyck, N., Wang, X., Van Drunen, C., Mullol, J., Hellings, P., Hox, V., Toskala, E., Scadding, G., Lund, V., Zhang, L., Fokkens, W., Bachert, C. (2016) Inflammatory endotypes of chronic rhinosinusitis based on cluster analysis of biomarkers. J. Allergy Clin. Immunol. 137, 1449-1456 e1444. <https://doi.org/10.1016/j.jaci.2015.12.1324>
55. Warner, S. M., Hackett, T. L., Shaheen, F., Hallstrand, T. S., Kicic, A., Stick, S. M., Knight, D. A. (2013) Transcription factor p63 regulates key genes and wound repair in human airway epithelial basal cells. Am. J. Respir. Cell Mol. Biol. 49, 978-988. <https://doi.org/10.1165/rcmb.2012-0447OC>
56. Wawrzyniak, P., Wawrzyniak, M., Wanke, K., Sokolowska, M., Bendelja, K., Ruckert, B., Globinska, A., Jakiela, B., Kast, J. I., Idzko, M., Akdis, M., Sanak, M., Akdis, C. A. (2017) Regulation of bronchial epithelial barrier integrity by type 2 cytokines and histone deacetylases in asthmatic patients. J. Allergy Clin. Immunol. 139, 93-103. <https://doi.org/10.1016/j.jaci.2016.03.050>
57. Wu, G., Nomoto, S., Hoque, M. O., Dracheva, T., Osada, M., Lee, C. C., Dong, S. M., Guo, Z., Benoit, N., Cohen, Y., Rechthand, P., Califano, J., Moon, C. S., Ratovitski, E., Jen, J., Sidransky, D., Trink, B. (2003) ΔNp63α and TAp63α regulate transcription of genes with distinct biological functions in cancer and development. Cancer Res. 63, 2351-2357.
58. Yang, A., Kaghad, M., Wang, Y., Gillett, E., Fleming, M. D., Dotsch, V., Andrews, N. C., Caput, D., McKeon, F. (1998) p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol. Cell 2, 305-316. <https://doi.org/10.1016/S1097-2765(00)80275-0>
59. Yang, A., Schweitzer, R., Sun, D., Kaghad, M., Walker, N., Bronson, R. T., Tabin, C., Sharpe, A., Caput, D., Crum, C., McKeon, F. (1999) p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398, 714-718. <https://doi.org/10.1038/19539>
60. Young, J., Frenkiel, S., Tewfik, M. A., Mouadeb, D. A. (2007) Long-term outcome analysis of endoscopic sinus surgery for chronic sinusitis. Am. J. Rhinol. 21, 743-747. <https://doi.org/10.2500/ajr.2007.21.3108>
61. Zangen, R., Ratovitski, E., Sidransky, D. (2005) ΔNp63α levels correlate with clinical tumor response to cisplatin. Cell Cycle 4, 1313-1315. <https://doi.org/10.4161/cc.4.10.2066>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Submissions

Archive