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Abdulrahman Seid Ahmed, M., Omer, N., M. Suliman, A., & Ellaithi, M. (2021). Expression of Cyclin D1 in Oral Squamous Cell Carcinoma. Sudan Journal of Medical Sciences (SJMS), 16(4), 558–566. https://doi.org/10.18502/sjms.v16i4.9953
https://doi.org/10.18502/sjms.v16i4.9953
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authors
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Malak Abdulrahman Seid Ahmed
Malak Abdulrahman Seid Ahmed
Faculty of Medical Laboratory sciences, Al-Neelain University, Khartoum, Sudan
-
Nazik Omer
Nazik Omer
Department of oral and maxillofacial surgery, division of oral Pathology, Faculty of Dentistry, University of Khartoum, Sudan
-
Ahmed M. Suliman
Ahmed M. Suliman
Department of oral and maxillofacial surgery, division of oral Pathology, Faculty of Dentistry, University of Khartoum, Sudan
-
Mona Ellaithi
Mona Ellaithi
Faculty of Medical Laboratory sciences, Al-Neelain University, Khartoum, Sudan
Published Date
- Dec 31, 2021
Expression of Cyclin D1 in Oral Squamous Cell Carcinoma
Abstract
Background: Cyclin D1 expression regulates normal cell cycle. Its deregulation or overexpression may cause disruption in the normal cell cycle control and lead to cancer progression. In this study, we aimed to study the expression of cyclin D1 in oral squamous cell carcinoma (OSCC) and find its association with the different grades of oral tumors, if any.
Methods: This cross-sectional study included 40 formalin-fixed paraffin-embedded tissue blocks specimens of OSCC with variable grades. The expression of cyclin D1 was evaluated through immunohistochemical (IHC) staining.
Results: There were 9 female and 31 male samples, with a male-to-female ratio of 3.4:1. The age ranged between 25 and 90 years with an average age of 65.5 years. Twenty-five (62.5%) samples were diagnosed as well-differentiated squamous cell carcinoma (WDSCC) and fifteen (37.5%) as poorly differentiated squamous cell carcinoma (PDSCC). No cases of moderately differentiated squamous carcinoma were included in the study. The expression of cyclin D1 was detected in the cases of WDSCC and a lesser expression was seen in the PDSCC with a P-value of 0.0003, OR 1581 and 95% CI (29.8239 to 83810.7113).
Conclusion: Cyclin D1 is expressed in OSCC and stronger expression was detected in WDSCC.
Keywords:
Cyclin D1, oral squamous cell carcinoma (OSCC), Toombak, Sudanese oral cancer, immunohistochemistry
References
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[25] Marocchio, L. S., Lima, J., Sperandio, F. F., et al. (2010). Oral squamous cell carcinoma: an analysis of 1,564 cases showing advances in early detection. Journal of Oral Science, vol. 52, no. 2, pp. 267–273.
[26] Sarkaria, J. N. and Harari, P. M. (1994). Oral tongue cancer in young adults less than 40 years of age: rationale for aggressive therapy. Head & Neck, vol. 16, no. 2, pp. 107–111.
[27] Chitapanarux, I., Lorvidhaya, V., Sittitrai, P., et al. (2006). Oral cavity cancers at a young age: analysis of patient, tumor and treatment characteristics in Chiang Mai University Hospital. Oral Oncology, vol. 42, no. 1, pp. 83–88.
[28] Llewellyn, C., Johnson, N. W., and Warnakulasuriya, K. (2004). Risk factors for oral cancer in newly diagnosed patients aged 45 years and younger: a case–control study in Southern England. Journal of Oral Pathology & Medicine, vol. 33, no. 9, pp. 525–532.
[29] Al-Jaber, A., Al-Nasser, L., and El-Metwally, A. (2016). Epidemiology of oral cancer in Arab countries. Saudi Medical Journal, vol. 37, no. 3, pp. 249–255.
[30] Elbeshir, E., Abeen, H., Idris, A., et al. (1989). Snuff dipping and oral cancer in Sudan: a retrospective study. British Journal of Oral and Maxillofacial Surgery, vol. 27, no. 3, pp. 243–248.
[31] Idris, A., Ahmed, H., Mukhtar, B., et al. (1995). Descriptive epidemiology of oral neoplasms in sudan 1970–1985 and the role of toombak. International Journal of Cancer, vol. 61, no. 2, pp. 155–158.
[32] Ahmed, H. G. (2013). Aetiology of oral cancer in the Sudan. Journal of Oral & Maxillofacial Research, vol. 4, no. 2, p. e3.
[33] Osman, T. A., Satti, A. A., Bøe, O. E., et al. (2010). Pattern of malignant tumors registered at a referral oral and maxillofacial hospital in Sudan during 2006 and 2007. Journal of Cancer Research and Therapeutics, vol. 6, no. 4, pp. 473–477.
[34] Pednekar, M. S., Gupta, P. C., Yeole, B. B., et al. (2011). Association of tobacco habits, including bidi smoking, with overall and site-specific cancer incidence: results from the Mumbai cohort study. Cancer Causes & Control, vol. 22, no. 6, pp. 859–868.
[35] IARC Working Group on the Evaluation of Carcinogenic Risks to Humans Personal habits and indoor combustions. (2012). Volume 100E: a review of human carcinogens. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, vol. 100, Pt. E, pp. 1–538.
[36] Idris, A. M., Prokopczyk, B., and Hoffmann, D. (1994). Toombak: a major risk factor for cancer of the oral cavity in Sudan. Preventive Medicine, vol. 23, no. 6, pp. 832–839.
[37] Idris, A. M., Ibrahim, S. O., Vasstrand, E. N., et al. (1998). The Swedish snus and the Sudanese toombak: are they different? Oral Oncology, vol. 34, no. 6, pp. 558–566;
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[39] Montero, P. H. and Patel, S. G. (2015). Cancer of the oral cavity. Surgical Oncology Clinics of North America, vol. 24, no. 3, pp. 491–508.
[40] Choudhary, A., Kesarwani, P., Gaikwad, P., et al. (2016). Expression of cyclin D1 in oral squamous cell carcinoma and its correlation with histological differentiation: an immunohistochemical study. Journal of Indian Academy of Oral Medicine and Radiology, vol. 28, no. 2, pp. 140–144.
[41] Lam, K. Y., Irene, O. L., Yuen, A. P., et al. (2000). Cyclin D1 expression in oral squamous cell carcinomas: clinicopathological relevance and correlation with p53 expression. Journal of Oral Pathology & Medicine, vol. 29, no. 4, pp. 167–172.
[42] Angadi, P. V. and Krishnapillai, R. (2007). Cyclin D1 expression in oral squamous cell carcinoma and verrucous carcinoma: correlation with histological differentiation. Oral Surgery, Oral Medicine, Oral Pathology, and Oral Radiology, vol. 103, no. 3, pp. 30–35.
[43] Wu, M., Putti, T. C., and Bhuiya, T. A. (2002). Comparative study in the expression of p53, EGFR, TGF- alpha, and cyclin D1 in verrucous carcinoma, verrucous hyperplasia and squamous cell carcinoma of head and neck region. Applied Immunohistochemistry & Molecular Morphology, vol. 10, no. 4, pp. 351–356.
[44] Saawarn, S., Astekar, M., Saawarn, N., et al. (2012). Cyclin D1 expression and its correlation with histopathological differentiation in oral squamous cell carcinoma. Scientific World Journal, vol. 2012, p. 978327.
[45] Montalto, F. I. and De Amicis, F. (2020). Cyclin D1 in cancer: a molecular connection for cell cycle control, adhesion and invasion in tumor and stroma. Cells, vol. 9, no. 12, p. 2648.
[46] Perisanidis, C., Perisanidis, B., and Wrba, F. (2012). Evaluation of immunohistochemical expression of p53, p21, p27, cyclin D1, and Ki67 in oral and oropharyngeal squamous cell carcinoma. Journal of Oral Pathology & Medicine, vol. 41, no. 1, pp. 40–46.
[47] Smith, B. (2001). SGLCD. Molecular marker expression in oral and oropharyngeal squamous cell carcinoma. The Archives of Otolaryngology – Head & Neck Surgery, vol. 127, no. 7, pp. 780–785.
[48] Michalides, R., van Veelen, N. M., Kristel, P. M., et al. (1997). Overexpression of cyclin D1 indicates a poor prognosis in squamous cell carcinoma of the head and neck. The Archives of Otolaryngology – Head & Neck Surgery, vol. 123, no. 5, pp. 497–502.
[49] Rasamny, J. J., Allak, A., and Krook, K. A. (2012). Cyclin D1 and FADD as biomarkers in head and neck squamous cell carcinoma. Otolaryngology–Head and Neck Surgery, vol. 146, no. 6, pp. 923–931.
[50] Faraji, F., Schubert, A. D., Kagohara, L. T., et al. (2018) The genome-wide molecular landscape of HPV-driven and HPV-negative head and neck squamous cell carcinoma. In B. Burtness and E. Golemis (Eds.), Molecular determinants of head and neck cancer. Current Cancer Research. Cham: Humana Press.
[51] Hermida-Prado, F., Menéndez, S. T., Albornoz-Afanasiev, P., et al. (2018). Distinctive expression and amplification of genes at 11q13 in relation to HPV status with impact on survival in head and neck cancer patients. Journal of Clinical Medicine, vol. 7, no. 12, p. 501.
[52] van Kempen, P. M., Noorlag, R., Braunius, W. W., et al. (2015). Clinical relevance of copy number profiling in oral and oropharyngeal squamous cell carcinoma. Cancer Medicine, vol. 4, no. 10, pp. 1525–1535.
[53] Mohamed, F. E., Aldayem, L. N., Hemaida, M. A., et al. (2021). Molecular detection of human papillomavirus-16 among Sudanese patients diagnosed with squamous cell carcinoma and salivary gland carcinoma. BMC Research Notes, vol. 14, no. 1, p. 56.
[2] Casimiro, M. C., Crosariol, M., Loro, E., et al. (2012). Cyclins and cell cycle control in cancer and disease. Genes & Cancer, vol. 3, no. 11–12, pp. 649–657.
[3] Motokura, T. and Arnold, A. (1993). Cyclin D and oncogenesis. Current Opinion in Genetics and Development, vol. 3, no. 1, pp. 5–10.
[4] Weinstat-Saslow, D., Merino, M. J., Manrow, R. E., et al. (1995). Overexpression of cyclin D mRNA distinguishes invasive and in situ breast carcinomas from non-malignant lesions. Nature Medicine, vol. 1, no. 12, pp. 1257–1260.
[5] Hall, M. and Peters, G. (1996). Genetic alterations of cyclins, cyclin-dependent kinases, and Cdk inhibitors in human cancer. Advances in Cancer Research, vol. 68, pp. 67–108.
[6] Gillett, C., Smith, P., Gregory, W., et al. (1996). Cyclin D1 and prognosis in human breast cancer. International Journal of Cancer, vol. 69, no. 2, pp. 92–99.
[7] Sutherland, R. L. and Musgrove, E. A. (2002). Cyclin D1 and mammary carcinoma: new insights from transgenic mouse models. Breast Cancer Research, vol. 4, no. 1, pp. 14–17.
[8] Vermeulen, K., Van Bockstaele, D. R., and Berneman, Z. N. (2003). The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Proliferation, vol. 36, no. 3, pp. 131–149.
[9] Knudsen, K. E., Diehl, J. A., Haiman, C. A., et al. (2006). Cyclin D1: polymorphism, aberrant splicing and cancer risk. Oncogene, vol. 25, no. 11, pp. 1620–1628.
[10] Yamamoto, M., Tamakawa, S., Yoshie, M., et al. (2006). Neoplastic hepatocyte growth associated with cyclin D1 redistribution from the cytoplasm to the nucleus in mouse hepatocarcinogenesis. Molecular Carcinogenesis, vol. 45, no. 12, pp. 901–913.
[11] Miyamoto, R., Uzawa, N., Nagaoka, S., et al. (2003). Prognostic significance of cyclin D1 amplification and overexpression in oral squamous cell carcinoma. Oral Oncology, vol. 39, no. 6, pp. 610–618.
[12] Das, S. N., Khare, P., Singh, M. K., et al. (2011). Correlation of cyclin D1 expression with aggressive DNA pattern in patients with tobacco-related intraoral squamous cell carcinoma. Indian Journal of Medical Research, vol. 133, no. 4, pp. 381–386.
[13] Shenoy, A. M. (2011). Cyclin D1 over expression as a prognostic factor in patients with tobacco‑related intraoral squamous cell carcinoma. Indian Journal of Medical Research, vol. 133, no. 4, pp. 364–365.
[14] Swaminathan, U., Joshua, E., Umadevi, K., et al. (2012). Expression of p53 and Cyclin D1 in oral squamous cell carcinoma and normal mucosa: an immunohistochemical study. Journal of Oral and Maxillofacial Pathology, vol. 16, no. 2, pp. 172–177.
[15] Lin, R. J., Lubpairee, T., Liu, K. Y., et al. (2013). Cyclin D1 overexpression is associated with poor prognosis in oropharyngeal cancer. Journal of Otolaryngology – Head & Neck Surgery, vol. 42, no. 1, pp. 1–7.
[16] Bancroft, J. D., Layton, C., and Suvarna, S. K. (2013). Bancrofts Theory and Practice of Histological Techniques (7th ed.). Churchill Livingstone: Elsevier.
[17] Todd, R., Hinds, P. W., Munger, K., et al. (2002). Cell cycle dysregulation in oral cancer. Critical Reviews in Oral Biology & Medicine, vol. 13, no. 1, pp. 51–61.
[18] Fu, M., Wang, C., Li, Z., et al. (2004). Minireview: Cyclin D1: normal and abnormal functions. Endocrinology, vol. 145, no. 12, pp. 5439–5447.
[19] Assoian, R. K. and Klein, E. A. (2008). Growth control by intracellular tension and extracellular stiffness. Trends in Cell Biology, vol. 18, no. 7, pp. 347–352.
[20] Donnellen, R. and Chetty, R. (1998). Cyclin D1 and human neoplasia. Journal of Clinical Pathology, vol. 51, no. 1, pp. 1–7.
[21] Alao, J. P. (2007). The regulation of cyclin D1 degradation: roles in cancer development and the potential for therapeutic invention. Molecular Cancer, vol. 6, no. 1, p. 24.
[22] Shiboski, C. H., Schmidt, B. L., and Jordan, R. C. (2007). Racial disparity in stage at diagnosis and survival among adults with oral cancer in the US. Community Dentistry and Oral Epidemiology, vol. 35, no. 3, pp. 233–240.
[23] Zini, A., Czerninski, R., and Sgan-Cohen, H. D. (2010). Oral cancer over four decades: epidemiology, trends, histology, and survival by anatomical sites. Journal of Oral Pathology & Medicine, vol. 39, no. 4, pp. 299–305.
[24] Johnson, N. W., Jayasekara, P., and Amarasinghe, A. A. (2011). Squamous cell carcinoma and precursor lesions of the oral cavity: epidemiology and aetiology. Periodontology 2000, vol. 57, no. 1, pp. 19–37.
[25] Marocchio, L. S., Lima, J., Sperandio, F. F., et al. (2010). Oral squamous cell carcinoma: an analysis of 1,564 cases showing advances in early detection. Journal of Oral Science, vol. 52, no. 2, pp. 267–273.
[26] Sarkaria, J. N. and Harari, P. M. (1994). Oral tongue cancer in young adults less than 40 years of age: rationale for aggressive therapy. Head & Neck, vol. 16, no. 2, pp. 107–111.
[27] Chitapanarux, I., Lorvidhaya, V., Sittitrai, P., et al. (2006). Oral cavity cancers at a young age: analysis of patient, tumor and treatment characteristics in Chiang Mai University Hospital. Oral Oncology, vol. 42, no. 1, pp. 83–88.
[28] Llewellyn, C., Johnson, N. W., and Warnakulasuriya, K. (2004). Risk factors for oral cancer in newly diagnosed patients aged 45 years and younger: a case–control study in Southern England. Journal of Oral Pathology & Medicine, vol. 33, no. 9, pp. 525–532.
[29] Al-Jaber, A., Al-Nasser, L., and El-Metwally, A. (2016). Epidemiology of oral cancer in Arab countries. Saudi Medical Journal, vol. 37, no. 3, pp. 249–255.
[30] Elbeshir, E., Abeen, H., Idris, A., et al. (1989). Snuff dipping and oral cancer in Sudan: a retrospective study. British Journal of Oral and Maxillofacial Surgery, vol. 27, no. 3, pp. 243–248.
[31] Idris, A., Ahmed, H., Mukhtar, B., et al. (1995). Descriptive epidemiology of oral neoplasms in sudan 1970–1985 and the role of toombak. International Journal of Cancer, vol. 61, no. 2, pp. 155–158.
[32] Ahmed, H. G. (2013). Aetiology of oral cancer in the Sudan. Journal of Oral & Maxillofacial Research, vol. 4, no. 2, p. e3.
[33] Osman, T. A., Satti, A. A., Bøe, O. E., et al. (2010). Pattern of malignant tumors registered at a referral oral and maxillofacial hospital in Sudan during 2006 and 2007. Journal of Cancer Research and Therapeutics, vol. 6, no. 4, pp. 473–477.
[34] Pednekar, M. S., Gupta, P. C., Yeole, B. B., et al. (2011). Association of tobacco habits, including bidi smoking, with overall and site-specific cancer incidence: results from the Mumbai cohort study. Cancer Causes & Control, vol. 22, no. 6, pp. 859–868.
[35] IARC Working Group on the Evaluation of Carcinogenic Risks to Humans Personal habits and indoor combustions. (2012). Volume 100E: a review of human carcinogens. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, vol. 100, Pt. E, pp. 1–538.
[36] Idris, A. M., Prokopczyk, B., and Hoffmann, D. (1994). Toombak: a major risk factor for cancer of the oral cavity in Sudan. Preventive Medicine, vol. 23, no. 6, pp. 832–839.
[37] Idris, A. M., Ibrahim, S. O., Vasstrand, E. N., et al. (1998). The Swedish snus and the Sudanese toombak: are they different? Oral Oncology, vol. 34, no. 6, pp. 558–566;
[38] Odell, E. W., Jani, P., Sherriff, M., et al. (1994). The prognostic value of individual histologic grading parameters in small lingual squamous cell carcinomas. The importance of the pattern of invasion. Cancer, vol. 74, no. 3, pp. 789–794.
[39] Montero, P. H. and Patel, S. G. (2015). Cancer of the oral cavity. Surgical Oncology Clinics of North America, vol. 24, no. 3, pp. 491–508.
[40] Choudhary, A., Kesarwani, P., Gaikwad, P., et al. (2016). Expression of cyclin D1 in oral squamous cell carcinoma and its correlation with histological differentiation: an immunohistochemical study. Journal of Indian Academy of Oral Medicine and Radiology, vol. 28, no. 2, pp. 140–144.
[41] Lam, K. Y., Irene, O. L., Yuen, A. P., et al. (2000). Cyclin D1 expression in oral squamous cell carcinomas: clinicopathological relevance and correlation with p53 expression. Journal of Oral Pathology & Medicine, vol. 29, no. 4, pp. 167–172.
[42] Angadi, P. V. and Krishnapillai, R. (2007). Cyclin D1 expression in oral squamous cell carcinoma and verrucous carcinoma: correlation with histological differentiation. Oral Surgery, Oral Medicine, Oral Pathology, and Oral Radiology, vol. 103, no. 3, pp. 30–35.
[43] Wu, M., Putti, T. C., and Bhuiya, T. A. (2002). Comparative study in the expression of p53, EGFR, TGF- alpha, and cyclin D1 in verrucous carcinoma, verrucous hyperplasia and squamous cell carcinoma of head and neck region. Applied Immunohistochemistry & Molecular Morphology, vol. 10, no. 4, pp. 351–356.
[44] Saawarn, S., Astekar, M., Saawarn, N., et al. (2012). Cyclin D1 expression and its correlation with histopathological differentiation in oral squamous cell carcinoma. Scientific World Journal, vol. 2012, p. 978327.
[45] Montalto, F. I. and De Amicis, F. (2020). Cyclin D1 in cancer: a molecular connection for cell cycle control, adhesion and invasion in tumor and stroma. Cells, vol. 9, no. 12, p. 2648.
[46] Perisanidis, C., Perisanidis, B., and Wrba, F. (2012). Evaluation of immunohistochemical expression of p53, p21, p27, cyclin D1, and Ki67 in oral and oropharyngeal squamous cell carcinoma. Journal of Oral Pathology & Medicine, vol. 41, no. 1, pp. 40–46.
[47] Smith, B. (2001). SGLCD. Molecular marker expression in oral and oropharyngeal squamous cell carcinoma. The Archives of Otolaryngology – Head & Neck Surgery, vol. 127, no. 7, pp. 780–785.
[48] Michalides, R., van Veelen, N. M., Kristel, P. M., et al. (1997). Overexpression of cyclin D1 indicates a poor prognosis in squamous cell carcinoma of the head and neck. The Archives of Otolaryngology – Head & Neck Surgery, vol. 123, no. 5, pp. 497–502.
[49] Rasamny, J. J., Allak, A., and Krook, K. A. (2012). Cyclin D1 and FADD as biomarkers in head and neck squamous cell carcinoma. Otolaryngology–Head and Neck Surgery, vol. 146, no. 6, pp. 923–931.
[50] Faraji, F., Schubert, A. D., Kagohara, L. T., et al. (2018) The genome-wide molecular landscape of HPV-driven and HPV-negative head and neck squamous cell carcinoma. In B. Burtness and E. Golemis (Eds.), Molecular determinants of head and neck cancer. Current Cancer Research. Cham: Humana Press.
[51] Hermida-Prado, F., Menéndez, S. T., Albornoz-Afanasiev, P., et al. (2018). Distinctive expression and amplification of genes at 11q13 in relation to HPV status with impact on survival in head and neck cancer patients. Journal of Clinical Medicine, vol. 7, no. 12, p. 501.
[52] van Kempen, P. M., Noorlag, R., Braunius, W. W., et al. (2015). Clinical relevance of copy number profiling in oral and oropharyngeal squamous cell carcinoma. Cancer Medicine, vol. 4, no. 10, pp. 1525–1535.
[53] Mohamed, F. E., Aldayem, L. N., Hemaida, M. A., et al. (2021). Molecular detection of human papillomavirus-16 among Sudanese patients diagnosed with squamous cell carcinoma and salivary gland carcinoma. BMC Research Notes, vol. 14, no. 1, p. 56.