Research Article
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Expression and prognostic value of ING3 in advanced laryngeal squamous cell carcinoma

Year 2023, Volume: 9 Issue: 3, 517 - 528, 04.05.2023
https://doi.org/10.18621/eurj.1108404

Abstract

Objectives: Laryngeal squamous cell carcinomas (LSCC) is one of the most common aggressive neoplasms of the head and neck region. There is a significant need for identification of successful and accurate prognostic markers to better estimate the clinical outcomes for LSCC patients. In this study, we aimed at analyzing the differential expressions of inhibitor growth (ING) family members and to evaluate the prognostic values of deregulated ING genes in LSCC.


Methods:
We investigated the relative expressions of ING genes in laryngeal tumor-normal tissue pairs in the mRNA level using quantitative real-time polymerase chain reaction and relative expression of ING3 in the protein level using Western Blot analysis.


Results:
The rate of genetic alterations of ING3 was relatively higher in head and neck cancer including LSCC. ING3 expression was significantly upregulated in LSCC tissue samples in both mRNA and protein level. Higher expression of ING3 was also correlated with poor disease-free survival of patients with head and neck cancer.


Conclusions:
Our findings assigned an oncogenic feature for ING3 in laryngeal cancer with a significant upregulation detected in advanced cases and suggested a vital prognostic potential for ING3.

Supporting Institution

The Scientific Research Projects of Ataturk University

Project Number

TCD-2020-7724

References

  • 1. Genden EM, Ferlito A, Silver CE, Jacobson AS, Werner JA, Suarez C, et al. Evolution of the management of laryngeal cancer. Oral Oncol 2007;43:431-9.
  • 2. Yang C, Gao S, Zhang H, Xu L, Liu J, Wang M, et al. CD47 is a potential target for the treatment of laryngeal squamous cell carcinoma. Cell Physiol Biochem 2016;40:126-36.
  • 3. Vassileiou A, Vlastarakos PV, Kandiloros D, Delicha E, Ferekidis E, Tzagaroulakis A, et al. Laryngeal cancer: smoking is not the only risk factor. B-ENT 2012;8:273-8.
  • 4. Groome PA, O'Sullivan B, Irish JC, Rothwell DM, Schulze K, Warde PR, et al. Management and outcome differences in supraglottic cancer between Ontario, Canada, and the Surveillance, Epidemiology, and End Results areas of the United States. J Clin Oncol 2003;21:496-505.
  • 5. Luo J, Wu J, Lv K, Li K, Wu J, Wen Y, et al. Analysis of postsurgical health-related quality of life and quality of voice of patients with laryngeal carcinoma. Medicine (Baltimore) 2016;95:e2363.
  • 6. Liu Y, Su Z, Li G, Yu C, Ren S, Huang D, et al. Increased expression of metadherin protein predicts worse disease-free and overall survival in laryngeal squamous cell carcinoma. Int J Cancer 2013;133:671-9.
  • 7. Almadori G, Bussu F, Paludettii G. Predictive factors of neck metastases in laryngeal squamous cell carcinoma. Towards an integrated clinico-molecular classification. Acta Otorhinolaryngol Ital 2006;26:326-34.
  • 8. Zhang X, Xu LS, Wang ZQ, Wang KS, Li N, Cheng ZH, et al. ING4 induces G2/M cell cycle arrest and enhances the chemosensitivity to DNA-damage agents in HepG2 cells. FEBS Lett 2004;570:7-12.
  • 9. He GH, Helbing CC, Wagner MJ, Sensen CW, Riabowol K. Phylogenetic analysis of the ING family of PHD finger proteins. Mol Biol Evol 2005;22:104-16.
  • 10. Coles AH, Jones SN. The ING gene family in the regulation of cell growth and tumorigenesis. J Cell Physiol 2009;218:45-57.
  • 11. Soliman MA, Riabowol K. After a decade of study-ING, a PHD for a versatile family of proteins. Trends Biochem Sci 2007;32:509-19.
  • 12. Campos EI, Chin MY, Kuo WH, Li G. Biological functions of the ING family tumor suppressors. Cell Mol Life Sci 2004;61:2597-613.
  • 13. Dantas A, Al Shueili B, Yang Y, Nabbi A, Fink D, Riabowol K. Biological Functions of the ING Proteins. Cancers (Basel) 2019;11:1817.
  • 14. Gou WF, Yang XF, Shen DF, Zhao S, Sun HZ, Luo JS, et al. Immunohistochemical profile of ING3 protein in normal and cancerous tissues. Oncol Lett 2017;13:1631-6.
  • 15. Almami A, Hegazy SA, Nabbi A, Alshalalfa M, Salman A, Abou-Ouf H, et al. ING3 is associated with increased cell invasion and lethal outcome in ERG-negative prostate cancer patients. Tumour Biol 2016;37:9731-8.
  • 16. Smolle E, Fink-Neuboeck N, Lindenmann J, Smolle-Juettner F, Pichler M. The biological and clinical relevance of inhibitor of growth (ING) genes in non-small cell lung cancer. Cancers (Basel) 2019;11:1118.
  • 17. Du Y, Cheng Y, Su G. The essential role of tumor suppressor gene ING4 in various human cancers and non-neoplastic disorders. Biosci Rep 2019;39:BCR20180773.
  • 18. Gournay M, Paineau M, Archambeau J, Pedeux R. Regulat-INGs in tumors and diseases: Focus on ncRNAs. Cancer Lett 2019;447:66-74.
  • 19. Li X, Kikuchi K, Takano Y. ING genes work as tumor suppressor genes in the carcinogenesis of head and neck squamous cell carcinoma. J Oncol 2011;2011:963614.
  • 20. Yang C, Gao J, Yan N, Wu B, Ren Y, Li H, et al. Propofol inhibits the growth and survival of gastric cancer cells in vitro through the upregulation of ING3. Oncol Rep 2017;37:587-93.
  • 21. Gou WF, Sun HZ, Zhao S, Niu ZF, Mao XY, Takano Y, et al. Downregulated inhibitor of growth 3 (ING3) expression during colorectal carcinogenesis. Indian J Med Res 2014;139:561-7.
  • 22. Fink D, Yau T, Nabbi A, Wagner B, Wagner C, Hu SM, et al. Loss of Ing3 expression results in growth retardation and embryonic death. Cancers (Basel) 2019;12:180.
  • 23. Nagashima M, Shiseki M, Pedeux RM, Okamura S, Kitahama-Shiseki M, Miura K, et al. A novel PHD-finger motif protein, p47ING3, modulates p53-mediated transcription, cell cycle control, and apoptosis. Oncogene 2003;22:343-50.
  • 24. Gunduz M, Beder LB, Gunduz E, Nagatsuka H, Fukushima K, Pehlivan D, et al. Downregulation of ING3 mRNA expression predicts poor prognosis in head and neck cancer. Cancer Sci 2008;99:531-8.
  • 25. Lu M, Chen F, Wang Q, Wang K, Pan Q, Zhang X. Downregulation of inhibitor of growth 3 is correlated with tumorigenesis and progression of hepatocellular carcinoma. Oncol Lett 2012;4:47-52.
  • 26. Nabbi A, McClurg UL, Thalappilly S, Almami A, Mobahat M, Bismar TA, et al. ING3 promotes prostate cancer growth by activating the androgen receptor. BMC Med 2017;15:103.
  • 27. Ngollo M, Lebert A, Daures M, Judes G, Rifai K, Dubois L, et al. Global analysis of H3K27me3 as an epigenetic marker in prostate cancer progression. BMC Cancer 2017;17:261.
  • 28. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012;2:401-4.
  • 29. Chandrashekar DS, Bashel B, Balasubramanya SAH, Creighton C, Ponce-Rodriguez I, Chakravarthi BVSK, et al. UALCAN: a portal for facilitating tumor subgroup gene expression and survival analyses. Neoplasia 2017;19:649-58.
  • 30. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004;6:1-6.
  • 31. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, et al. STRING 8--a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 2009;37(Database issue):D412-6.
  • 32. Obid R, Redlich M, Tomeh C. The Treatment of Laryngeal Cancer. Oral Maxillofac Surg Clin North Am 2019;31:1-11.
  • 33. Vossen DM, Verhagen CVM, Verheij M, Wessels LFA, Vens C, van den Brekel MWM. Comparative genomic analysis of oral versus laryngeal and pharyngeal cancer. Oral Oncol 2018;81:35-44.
  • 34. Shiga K, Ogawa T, Katagiri K, Yoshida F, Tateda M, Matsuura K, et al. Differences between oral cancer and cancers of the pharynx and larynx on a molecular level. Oncol Lett 2012;3:238-43.
  • 35. Yuan H, Jiang H, Wang Y, Dong Y. Increased expression of lncRNA FTH1P3 predicts a poor prognosis and promotes aggressive phenotypes of laryngeal squamous cell carcinoma. Biosci Rep 2019;39:BSR20181644.
  • 36. Prabhu RS, Hanasoge S, Magliocca KR, Hall WA, Chen SA, Higgins KA, et al. Lymph node ratio influence on risk of head and neck cancer locoregional recurrence after initial surgical resection: implications for adjuvant therapy. Head Neck 2015;37:777-82.
  • 37. Ludwig S, Klitzsch A, Baniahmad A. The ING tumor suppressors in cellular senescence and chromatin. Cell Biosci 2011;1:25.
  • 38. Zhang R, Jin J, Shi J, Hou Y. INGs are potential drug targets for cancer. J Cancer Res Clin Oncol 2017;143:189-97.
  • 39. Nabbi A, Almami A, Thakur S, Suzuki K, Boland D, Bismar TA, et al. ING3 protein expression profiling in normal human tissues suggest its role in cellular growth and self-renewal. Eur J Cell Biol 2015;94:214-22.
  • 40. Wang J, Liu Z, Feng X, Gao S, Xu S, Liu P. Tumor suppressor gene ING3 induces cardiomyocyte hypertrophy via inhibition of AMPK and activation of p38 MAPK signaling. Arch Biochem Biophys 2014;562:22-30.
  • 41. Mouche A, Archambeau J, Ricordel C, Chaillot L, Bigot N, Guillaudeux T, et al. ING3 is required for ATM signaling and DNA repair in response to DNA double strand breaks. Cell Death Differ 2019;26:2344-57.
  • 42. McClurg UL, Nabbi A, Ricordel C, Korolchuk S, McCracken S, Heer R, et al. Human ex vivo prostate tissue model system identifies ING3 as an oncoprotein. Br J Cancer 2018;118:713-26.
  • 43. Bismar TA, Alshalalfa M, Petersen LF, Teng LH, Gerke T, Bakkar A, et al. Interrogation of ERG gene rearrangements in prostate cancer identifies a prognostic 10-gene signature with relevant implication to patients' clinical outcome. BJU Int 2014;113:309-19.
  • 44. Gunduz M, Ouchida M, Fukushima K, Ito S, Jitsumori Y, Nakashima T, et al. Allelic loss and reduced expression of the ING3, a candidate tumor suppressor gene at 7q31, in human head and neck cancers. Oncogene 2002;21:4462-70.
  • 45. Zhou R, Rotte A, Li G, Chen X, Chen G, Bhandaru M. Nuclear localization of ING3 is required to suppress melanoma cell migration, invasion and angiogenesis. Biochem Biophys Res Commun 2020;527:418-24.
  • 46. Li X, Zhang Q, Zhang M, Luo Y, Fu Y. Downregulation of nuclear ING3 expression and translocalization to cytoplasm promotes tumorigenesis and progression in head and neck squamous cell carcinoma (HNSCC). Histol Histopathol 2020;35:681-90.
  • 47. Kumamoto K, Fujita K, Kurotani R, Saito M, Unoki M, Hagiwara N, et al. ING2 is upregulated in colon cancer and increases invasion by enhanced MMP13 expression. Int J Cancer 2009;125:1306-15.
  • 48. Wang Y, Alla V, Goody D, gupta SK, Spitschak A, Wolkenhauer O, et al. Epigenetic factor EPC1 is a master regulator of DNA damage response by interacting with E2F1 to silence death and activate metastasis-related gene signatures. Nucleic Acids Res 2016;44:117-33.
  • 49. Loesch K, Galaviz S, Hamoui Z, Clanton R, Akabani G, Deveau M, et al. Functional genomics screening utilizing mutant mouse embryonic stem cells identifies novel radiation-response genes. PLoS One 2015;10:e0120534.
  • 50. Huang X, Spencer GJ, Lynch JT, Ciceri F, Somerville TD, Somervaille TC. Enhancers of Polycomb EPC1 and EPC2 sustain the oncogenic potential of MLL leukemia stem cells. Leukemia 2014;28:1081-91.
  • 51. Nara M, Teshima K, Watanabe A, Ito M, Iwamoto K, Kitabayashi A, et al. Bortezomib reduces the tumorigenicity of multiple myeloma via downregulation of upregulated targets in clonogenic side population cells. PLoS One 2013;8:e56954.
  • 52. Borkosky SS, Gunduz M, Nagatsuka H, Beder LB, Gunduz E, Sheikh Ali MAL, et al. Frequent deletion of ING2 locus at 4q35.1 associates with advanced tumor stage in head and neck squamous cell carcinoma. J Cancer Res Clin Oncol 2009;135:703-13.
  • 53. Tallen G, Kaiser I, Krabbe S, Lass U, Hartmann C, Henze G, et al. No ING1 mutations in human brain tumours but reduced expression in high malignancy grades of astrocytoma. Int J Cancer 2004;109:476-9.
  • 54. Takahashi M, Ozaki T, Todo S, Nakagawara A. Decreased expression of the candidate tumor suppressor gene ING1 is associated with poor prognosis in advanced neuroblastomas. Oncol Rep 2004;12:811-6.
  • 55. Chen Y, Huang Y, Hou P, Zhang Z, Zhang Y, Wang W, et al. ING4 suppresses tumor angiogenesis and functions as a prognostic marker in human colorectal cancer. Oncotarget 2016;7:79017-31.
  • 56. Liu Y, Yu L, Wang Y, Zhang Y, Zhang G. Expression of tumor suppressor gene ING4 in ovarian carcinoma is correlated with microvessel density. J Cancer Res Clin Oncol 2012;138:647-55.
  • 57. You Q, Wang XS, Fu SB, Jin XM. Downregulated expression of inhibitor of growth 4 (ING4) in advanced colorectal cancers: a non-randomized experimental study. Pathol Oncol Res 2011;17:473-7.
Year 2023, Volume: 9 Issue: 3, 517 - 528, 04.05.2023
https://doi.org/10.18621/eurj.1108404

Abstract

Project Number

TCD-2020-7724

References

  • 1. Genden EM, Ferlito A, Silver CE, Jacobson AS, Werner JA, Suarez C, et al. Evolution of the management of laryngeal cancer. Oral Oncol 2007;43:431-9.
  • 2. Yang C, Gao S, Zhang H, Xu L, Liu J, Wang M, et al. CD47 is a potential target for the treatment of laryngeal squamous cell carcinoma. Cell Physiol Biochem 2016;40:126-36.
  • 3. Vassileiou A, Vlastarakos PV, Kandiloros D, Delicha E, Ferekidis E, Tzagaroulakis A, et al. Laryngeal cancer: smoking is not the only risk factor. B-ENT 2012;8:273-8.
  • 4. Groome PA, O'Sullivan B, Irish JC, Rothwell DM, Schulze K, Warde PR, et al. Management and outcome differences in supraglottic cancer between Ontario, Canada, and the Surveillance, Epidemiology, and End Results areas of the United States. J Clin Oncol 2003;21:496-505.
  • 5. Luo J, Wu J, Lv K, Li K, Wu J, Wen Y, et al. Analysis of postsurgical health-related quality of life and quality of voice of patients with laryngeal carcinoma. Medicine (Baltimore) 2016;95:e2363.
  • 6. Liu Y, Su Z, Li G, Yu C, Ren S, Huang D, et al. Increased expression of metadherin protein predicts worse disease-free and overall survival in laryngeal squamous cell carcinoma. Int J Cancer 2013;133:671-9.
  • 7. Almadori G, Bussu F, Paludettii G. Predictive factors of neck metastases in laryngeal squamous cell carcinoma. Towards an integrated clinico-molecular classification. Acta Otorhinolaryngol Ital 2006;26:326-34.
  • 8. Zhang X, Xu LS, Wang ZQ, Wang KS, Li N, Cheng ZH, et al. ING4 induces G2/M cell cycle arrest and enhances the chemosensitivity to DNA-damage agents in HepG2 cells. FEBS Lett 2004;570:7-12.
  • 9. He GH, Helbing CC, Wagner MJ, Sensen CW, Riabowol K. Phylogenetic analysis of the ING family of PHD finger proteins. Mol Biol Evol 2005;22:104-16.
  • 10. Coles AH, Jones SN. The ING gene family in the regulation of cell growth and tumorigenesis. J Cell Physiol 2009;218:45-57.
  • 11. Soliman MA, Riabowol K. After a decade of study-ING, a PHD for a versatile family of proteins. Trends Biochem Sci 2007;32:509-19.
  • 12. Campos EI, Chin MY, Kuo WH, Li G. Biological functions of the ING family tumor suppressors. Cell Mol Life Sci 2004;61:2597-613.
  • 13. Dantas A, Al Shueili B, Yang Y, Nabbi A, Fink D, Riabowol K. Biological Functions of the ING Proteins. Cancers (Basel) 2019;11:1817.
  • 14. Gou WF, Yang XF, Shen DF, Zhao S, Sun HZ, Luo JS, et al. Immunohistochemical profile of ING3 protein in normal and cancerous tissues. Oncol Lett 2017;13:1631-6.
  • 15. Almami A, Hegazy SA, Nabbi A, Alshalalfa M, Salman A, Abou-Ouf H, et al. ING3 is associated with increased cell invasion and lethal outcome in ERG-negative prostate cancer patients. Tumour Biol 2016;37:9731-8.
  • 16. Smolle E, Fink-Neuboeck N, Lindenmann J, Smolle-Juettner F, Pichler M. The biological and clinical relevance of inhibitor of growth (ING) genes in non-small cell lung cancer. Cancers (Basel) 2019;11:1118.
  • 17. Du Y, Cheng Y, Su G. The essential role of tumor suppressor gene ING4 in various human cancers and non-neoplastic disorders. Biosci Rep 2019;39:BCR20180773.
  • 18. Gournay M, Paineau M, Archambeau J, Pedeux R. Regulat-INGs in tumors and diseases: Focus on ncRNAs. Cancer Lett 2019;447:66-74.
  • 19. Li X, Kikuchi K, Takano Y. ING genes work as tumor suppressor genes in the carcinogenesis of head and neck squamous cell carcinoma. J Oncol 2011;2011:963614.
  • 20. Yang C, Gao J, Yan N, Wu B, Ren Y, Li H, et al. Propofol inhibits the growth and survival of gastric cancer cells in vitro through the upregulation of ING3. Oncol Rep 2017;37:587-93.
  • 21. Gou WF, Sun HZ, Zhao S, Niu ZF, Mao XY, Takano Y, et al. Downregulated inhibitor of growth 3 (ING3) expression during colorectal carcinogenesis. Indian J Med Res 2014;139:561-7.
  • 22. Fink D, Yau T, Nabbi A, Wagner B, Wagner C, Hu SM, et al. Loss of Ing3 expression results in growth retardation and embryonic death. Cancers (Basel) 2019;12:180.
  • 23. Nagashima M, Shiseki M, Pedeux RM, Okamura S, Kitahama-Shiseki M, Miura K, et al. A novel PHD-finger motif protein, p47ING3, modulates p53-mediated transcription, cell cycle control, and apoptosis. Oncogene 2003;22:343-50.
  • 24. Gunduz M, Beder LB, Gunduz E, Nagatsuka H, Fukushima K, Pehlivan D, et al. Downregulation of ING3 mRNA expression predicts poor prognosis in head and neck cancer. Cancer Sci 2008;99:531-8.
  • 25. Lu M, Chen F, Wang Q, Wang K, Pan Q, Zhang X. Downregulation of inhibitor of growth 3 is correlated with tumorigenesis and progression of hepatocellular carcinoma. Oncol Lett 2012;4:47-52.
  • 26. Nabbi A, McClurg UL, Thalappilly S, Almami A, Mobahat M, Bismar TA, et al. ING3 promotes prostate cancer growth by activating the androgen receptor. BMC Med 2017;15:103.
  • 27. Ngollo M, Lebert A, Daures M, Judes G, Rifai K, Dubois L, et al. Global analysis of H3K27me3 as an epigenetic marker in prostate cancer progression. BMC Cancer 2017;17:261.
  • 28. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012;2:401-4.
  • 29. Chandrashekar DS, Bashel B, Balasubramanya SAH, Creighton C, Ponce-Rodriguez I, Chakravarthi BVSK, et al. UALCAN: a portal for facilitating tumor subgroup gene expression and survival analyses. Neoplasia 2017;19:649-58.
  • 30. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004;6:1-6.
  • 31. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, et al. STRING 8--a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 2009;37(Database issue):D412-6.
  • 32. Obid R, Redlich M, Tomeh C. The Treatment of Laryngeal Cancer. Oral Maxillofac Surg Clin North Am 2019;31:1-11.
  • 33. Vossen DM, Verhagen CVM, Verheij M, Wessels LFA, Vens C, van den Brekel MWM. Comparative genomic analysis of oral versus laryngeal and pharyngeal cancer. Oral Oncol 2018;81:35-44.
  • 34. Shiga K, Ogawa T, Katagiri K, Yoshida F, Tateda M, Matsuura K, et al. Differences between oral cancer and cancers of the pharynx and larynx on a molecular level. Oncol Lett 2012;3:238-43.
  • 35. Yuan H, Jiang H, Wang Y, Dong Y. Increased expression of lncRNA FTH1P3 predicts a poor prognosis and promotes aggressive phenotypes of laryngeal squamous cell carcinoma. Biosci Rep 2019;39:BSR20181644.
  • 36. Prabhu RS, Hanasoge S, Magliocca KR, Hall WA, Chen SA, Higgins KA, et al. Lymph node ratio influence on risk of head and neck cancer locoregional recurrence after initial surgical resection: implications for adjuvant therapy. Head Neck 2015;37:777-82.
  • 37. Ludwig S, Klitzsch A, Baniahmad A. The ING tumor suppressors in cellular senescence and chromatin. Cell Biosci 2011;1:25.
  • 38. Zhang R, Jin J, Shi J, Hou Y. INGs are potential drug targets for cancer. J Cancer Res Clin Oncol 2017;143:189-97.
  • 39. Nabbi A, Almami A, Thakur S, Suzuki K, Boland D, Bismar TA, et al. ING3 protein expression profiling in normal human tissues suggest its role in cellular growth and self-renewal. Eur J Cell Biol 2015;94:214-22.
  • 40. Wang J, Liu Z, Feng X, Gao S, Xu S, Liu P. Tumor suppressor gene ING3 induces cardiomyocyte hypertrophy via inhibition of AMPK and activation of p38 MAPK signaling. Arch Biochem Biophys 2014;562:22-30.
  • 41. Mouche A, Archambeau J, Ricordel C, Chaillot L, Bigot N, Guillaudeux T, et al. ING3 is required for ATM signaling and DNA repair in response to DNA double strand breaks. Cell Death Differ 2019;26:2344-57.
  • 42. McClurg UL, Nabbi A, Ricordel C, Korolchuk S, McCracken S, Heer R, et al. Human ex vivo prostate tissue model system identifies ING3 as an oncoprotein. Br J Cancer 2018;118:713-26.
  • 43. Bismar TA, Alshalalfa M, Petersen LF, Teng LH, Gerke T, Bakkar A, et al. Interrogation of ERG gene rearrangements in prostate cancer identifies a prognostic 10-gene signature with relevant implication to patients' clinical outcome. BJU Int 2014;113:309-19.
  • 44. Gunduz M, Ouchida M, Fukushima K, Ito S, Jitsumori Y, Nakashima T, et al. Allelic loss and reduced expression of the ING3, a candidate tumor suppressor gene at 7q31, in human head and neck cancers. Oncogene 2002;21:4462-70.
  • 45. Zhou R, Rotte A, Li G, Chen X, Chen G, Bhandaru M. Nuclear localization of ING3 is required to suppress melanoma cell migration, invasion and angiogenesis. Biochem Biophys Res Commun 2020;527:418-24.
  • 46. Li X, Zhang Q, Zhang M, Luo Y, Fu Y. Downregulation of nuclear ING3 expression and translocalization to cytoplasm promotes tumorigenesis and progression in head and neck squamous cell carcinoma (HNSCC). Histol Histopathol 2020;35:681-90.
  • 47. Kumamoto K, Fujita K, Kurotani R, Saito M, Unoki M, Hagiwara N, et al. ING2 is upregulated in colon cancer and increases invasion by enhanced MMP13 expression. Int J Cancer 2009;125:1306-15.
  • 48. Wang Y, Alla V, Goody D, gupta SK, Spitschak A, Wolkenhauer O, et al. Epigenetic factor EPC1 is a master regulator of DNA damage response by interacting with E2F1 to silence death and activate metastasis-related gene signatures. Nucleic Acids Res 2016;44:117-33.
  • 49. Loesch K, Galaviz S, Hamoui Z, Clanton R, Akabani G, Deveau M, et al. Functional genomics screening utilizing mutant mouse embryonic stem cells identifies novel radiation-response genes. PLoS One 2015;10:e0120534.
  • 50. Huang X, Spencer GJ, Lynch JT, Ciceri F, Somerville TD, Somervaille TC. Enhancers of Polycomb EPC1 and EPC2 sustain the oncogenic potential of MLL leukemia stem cells. Leukemia 2014;28:1081-91.
  • 51. Nara M, Teshima K, Watanabe A, Ito M, Iwamoto K, Kitabayashi A, et al. Bortezomib reduces the tumorigenicity of multiple myeloma via downregulation of upregulated targets in clonogenic side population cells. PLoS One 2013;8:e56954.
  • 52. Borkosky SS, Gunduz M, Nagatsuka H, Beder LB, Gunduz E, Sheikh Ali MAL, et al. Frequent deletion of ING2 locus at 4q35.1 associates with advanced tumor stage in head and neck squamous cell carcinoma. J Cancer Res Clin Oncol 2009;135:703-13.
  • 53. Tallen G, Kaiser I, Krabbe S, Lass U, Hartmann C, Henze G, et al. No ING1 mutations in human brain tumours but reduced expression in high malignancy grades of astrocytoma. Int J Cancer 2004;109:476-9.
  • 54. Takahashi M, Ozaki T, Todo S, Nakagawara A. Decreased expression of the candidate tumor suppressor gene ING1 is associated with poor prognosis in advanced neuroblastomas. Oncol Rep 2004;12:811-6.
  • 55. Chen Y, Huang Y, Hou P, Zhang Z, Zhang Y, Wang W, et al. ING4 suppresses tumor angiogenesis and functions as a prognostic marker in human colorectal cancer. Oncotarget 2016;7:79017-31.
  • 56. Liu Y, Yu L, Wang Y, Zhang Y, Zhang G. Expression of tumor suppressor gene ING4 in ovarian carcinoma is correlated with microvessel density. J Cancer Res Clin Oncol 2012;138:647-55.
  • 57. You Q, Wang XS, Fu SB, Jin XM. Downregulated expression of inhibitor of growth 4 (ING4) in advanced colorectal cancers: a non-randomized experimental study. Pathol Oncol Res 2011;17:473-7.
There are 57 citations in total.

Details

Primary Language English
Subjects Biochemistry and Cell Biology (Other), Otorhinolaryngology
Journal Section Original Articles
Authors

Neslişah Barlak 0000-0002-4811-9372

Gülnur Kuşdemir 0000-0002-4188-5031

Rasim Gumus 0000-0002-9208-8729

Abdulkadir Şahin 0000-0002-8426-792X

Betül Gündoğdu 0000-0002-3786-3286

Ömer Faruk Karatas 0000-0002-0379-2088

Arzu Tatar 0000-0002-4486-2695

Project Number TCD-2020-7724
Publication Date May 4, 2023
Submission Date May 11, 2022
Acceptance Date September 15, 2022
Published in Issue Year 2023 Volume: 9 Issue: 3

Cite

AMA Barlak N, Kuşdemir G, Gumus R, Şahin A, Gündoğdu B, Karatas ÖF, Tatar A. Expression and prognostic value of ING3 in advanced laryngeal squamous cell carcinoma. Eur Res J. May 2023;9(3):517-528. doi:10.18621/eurj.1108404

e-ISSN: 2149-3189 


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