Frequent CDKN2B/P15 and DAPK1 methylation in duodenal follicular lymphoma is related to duodenal reactive lymphoid hyperplasia
Duodenal type follicular lymphoma (DFL), a rare entity of follicular lymphoma (FL), is clinically indolent and is characterized by a low histological grade compared with nodal follicular lymphoma (NFL). Our previous reports revealed that DFL shares characteristics of both NFL and mucosa-associated l...
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| Published in | Journal of Clinical and Experimental Hematopathology Vol. 64; no. 2; pp. 129 - 137 |
|---|---|
| Main Authors | , , |
| Format | Journal Article |
| Language | English |
| Published |
Japan
The Japanese Society for Lymphoreticular Tissue Research
01.01.2024
JSLRT |
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| Online Access | Get full text |
| ISSN | 1346-4280 1880-9952 1880-9952 |
| DOI | 10.3960/jslrt.24020 |
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| Abstract | Duodenal type follicular lymphoma (DFL), a rare entity of follicular lymphoma (FL), is clinically indolent and is characterized by a low histological grade compared with nodal follicular lymphoma (NFL). Our previous reports revealed that DFL shares characteristics of both NFL and mucosa-associated lymphoid tissue (MALT) lymphoma in terms of clinical and biological aspects, suggesting its pathogenesis may involve antigenic stimulation. In contrast to NFL, the genomic methylation status of DFL is still challenging. Here, we determined the methylation profiles of DNAs from patients with DFL (n = 12), NFL (n = 10), duodenal reactive lymphoid hyperplasia (D-RLH) (n = 7), nodal reactive lymphoid hyperplasia (N-RLH) (n = 5), and duodenal samples from normal subjects (NDU) (n = 5) using methylation specific PCR of targets previously identified in MALT lymphoma (CDKN2B/P15, CDKN2A/P16, CDKN2C/P18, MGMT, hMLH-1, TP73, DAPK, HCAD). DAPK1 was frequently methylated in DFL (9/12; 75%), NFL (9/10; 90%), and D-RLH (5/7; 71%). CDKN2B/P15 sequences were methylated in six DFL samples and in only one NFL sample. Immunohistochemical analysis showed that p15 expression inversely correlated with methylation status. Genes encoding other cyclin-dependent kinase inhibitors (CDKN2A/P16, CDKN2C/P18) were not methylated in DFL samples. Methylation of the genes of interest was not detected in DNAs from D-RLH, except for DAPK1, and the difference in the extent of methylation between NDU and D-RLH was statistically significant (P = 0.013). Our results suggest that D-RLH serves as a reservoir for the development of DFL and that methylation of CDKN2B/P15 plays an important role in this process. |
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| AbstractList | Duodenal type follicular lymphoma (DFL), a rare entity of follicular lymphoma (FL), is clinically indolent and is characterized by a low histological grade compared with nodal follicular lymphoma (NFL). Our previous reports revealed that DFL shares characteristics of both NFL and mucosa-associated lymphoid tissue (MALT) lymphoma in terms of clinical and biological aspects, suggesting its pathogenesis may involve antigenic stimulation. In contrast to NFL, the genomic methylation status of DFL is still challenging. Here, we determined the methylation profiles of DNAs from patients with DFL (n = 12), NFL (n = 10), duodenal reactive lymphoid hyperplasia (D-RLH) (n = 7), nodal reactive lymphoid hyperplasia (N-RLH) (n = 5), and duodenal samples from normal subjects (NDU) (n = 5) using methylation specific PCR of targets previously identified in MALT lymphoma (CDKN2B/P15, CDKN2A/P16, CDKN2C/P18, MGMT, hMLH-1, TP73, DAPK, HCAD). DAPK1 was frequently methylated in DFL (9/12; 75%), NFL (9/10; 90%), and D-RLH (5/7; 71%). CDKN2B/P15 sequences were methylated in six DFL samples and in only one NFL sample. Immunohistochemical analysis showed that p15 expression inversely correlated with methylation status. Genes encoding other cyclin-dependen t kinase inhibitors (CDKN2A/P16, CDKN2C/P18) were not methylated in DFL samples. Methylation of the genes of interest was not detected in DNAs from D-RLH, except for DAPK1, and the difference in the extent of methylation between NDU and D-RLH was statistically significant (P = 0.013). Our results suggest that D-RLH serves as a reservoir for the development of DFL and that methylation of CDKN2B/P15 plays an important role in this process. Duodenal type follicular lymphoma (DFL), a rare entity of follicular lymphoma (FL), is clinically indolent and is characterized by a low histological grade compared with nodal follicular lymphoma (NFL). Our previous reports revealed that DFL shares characteristics of both NFL and mucosa-associated lymphoid tissue (MALT) lymphoma in terms of clinical and biological aspects, suggesting its pathogenesis may involve antigenic stimulation. In contrast to NFL, the genomic methylation status of DFL is still challenging. Here, we determined the methylation profiles of DNAs from patients with DFL (n = 12), NFL (n = 10), duodenal reactive lymphoid hyperplasia (D-RLH) (n = 7), nodal reactive lymphoid hyperplasia (N-RLH) (n = 5), and duodenal samples from normal subjects (NDU) (n = 5) using methylation specific PCR of targets previously identified in MALT lymphoma (CDKN2B/P15, CDKN2A/P16, CDKN2C/P18, MGMT, hMLH-1, TP73, DAPK, HCAD). DAPK1 was frequently methylated in DFL (9/12; 75%), NFL (9/10; 90%), and D-RLH (5/7; 71%). CDKN2B/P15 sequences were methylated in six DFL samples and in only one NFL sample. Immunohistochemical analysis showed that p15 expression inversely correlated with methylation status. Genes encoding other cyclin-dependent kinase inhibitors (CDKN2A/P16, CDKN2C/P18) were not methylated in DFL samples. Methylation of the genes of interest was not detected in DNAs from D-RLH, except for DAPK1, and the difference in the extent of methylation between NDU and D-RLH was statistically significant (P = 0.013). Our results suggest that D-RLH serves as a reservoir for the development of DFL and that methylation of CDKN2B/P15 plays an important role in this process. |
| ArticleNumber | 24020 |
| Author | Sato, Yasuharu Miyata-Takata, Tomoko Takata, Katsuyoshi |
| AuthorAffiliation | 1) Department of Cellular and Molecular Pathology , Niigata University Graduate School of Medicine , Niigata , Japan , 2) Department of Molecular Hematopathology , Okayama University Graduate School of Health Sciences , Okayama , Japan |
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| Cites_doi | 10.1126/science.8153634 10.1182/blood-2009-01-201731 10.3892/ijo_00000366 10.1309/LCGNV77J464LNFD6 10.1038/modpathol.2012.127 10.2353/ajpath.2010.090236 10.1101/gad.9.1.15 10.1111/j.1349-7006.2003.tb01357.x 10.1136/gut.52.5.641 10.1182/blood.V93.12.4347.412k31_4347_4353 10.1093/oxfordjournals.annonc.a058869 10.1038/sj.leu.2401009 10.1016/j.humpath.2013.03.002 10.1182/blood.V94.5.1773 10.1111/j.1349-7006.2011.01980.x 10.1111/cas.12392 10.1182/blood-2018-03-837252 10.1186/1476-4598-5-44 10.1073/pnas.1209620109 10.1038/modpathol.2009.51 10.1038/leu.2009.114 10.1111/cas.13031 |
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| Keywords | duodenal reactive hyperplasia DAPK1 CDKN2B/P15 methylation profile |
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| References | 14 Rohatiner A, d’Amore F, Coiffier B et al. Report on a workshop convened to discuss the pathological and staging classifications of gastrointestinal tract lymphoma. Ann Oncol. 1994; 5: 397-400. 23 Nakatsuka S, Takakuwa T, Tomita Y et al. Hypermethylation of death‐associated protein (DAP) kinase CpG island is frequent not only in B‐cell but also in T‐ and natural killer (NK)/T‐cell malignancies. Cancer Sci. 2003; 94: 87-91. 24 Rossi D, Capello D, Gloghini A et al. Aberrant promoter methylation of multiple genes throughout the clinico-pathologic spectrum of B-cell neoplasia. Haematologica. 2004; 89: 154-164. 3 Takata K, Sato Y, Nakamura N et al. Duodenal follicular lymphoma lacks AID but expresses BACH2 and has memory B-cell characteristics. Mod Pathol. 2013; 26: 22-31. 8 Kaneko Y, Sakurai S, Hironaka M et al. Distinct methylated profiles in Helicobacter pylori dependent and independent gastric MALT lymphomas. Gut. 2003; 52: 641-646. 10 Guo J, Burger M, Nimmrich I et al. Differential DNA methylation of gene promoters in small B-cell lymphomas. Am J Clin Pathol. 2005; 124: 430-439. 20 Baur AS, Shaw P, Burri N et al. Frequent methylation silencing of p15(INK4b) (MTS2) and p16(INK4a) (MTS1) in B-cell and T-cell lymphomas. Blood. 1999; 94: 1773-1781. 7 van Vollenhoven RF, Bieber MM, Powell MJ et al. VH4-34 encoded antibodies in systemic lupus erythematosus: a specific diagnostic marker that correlates with clinical disease characteristics. J Rheumatol. 1999; 26: 1727-1733. 9 O’Riain C, O’Shea DM, Yang Y et al. Array-based DNA methylation profiling in follicular lymphoma. Leukemia. 2009; 23: 1858-1866. 13 Ohnishi N, Takata K, Miyata-Takata T et al. CD10 down expression in follicular lymphoma correlates with gastrointestinal lesion involving the stomach and large intestine. Cancer Sci. 2016; 107: 1687-1695. 11 Kondo T, Oka T, Sato H et al. Accumulation of aberrant CpG hypermethylation by Helicobacter pylori infection promotes development and progression of gastric MALT lymphoma. Int J Oncol. 2009; 35: 547-557. 1 Takata K, Okada H, Ohmiya N et al. Primary gastrointestinal follicular lymphoma involving the duodenal second portion is a distinct entity: a multicenter, retrospective analysis in Japan. Cancer Sci. 2011; 102: 1532-1536. 15 Sato H, Oka T, Shinnou Y et al. Multi-step aberrant CpG island hyper-methylation is associated with the progression of adult T-cell leukemia/lymphoma. Am J Pathol. 2010; 176: 402-415. 6 Arons E, Suntum T, Stetler-Stevenson M, Kreitman RJ. VH4-34+ hairy cell leukemia, a new variant with poor prognosis despite standard therapy. Blood. 2009; 114: 4687-4695. 21 Deiss LP, Feinstein E, Berissi H, Cohen O, Kimchi A. Identification of a novel serine/threonine kinase and a novel 15-kD protein as potential mediators of the gamma interferon-induced cell death. Genes Dev. 1995; 9: 15-30. 16 Hayslip J, Montero A. Tumor suppressor gene methylation in follicular lymphoma: a comprehensive review. Mol Cancer. 2006; 5: 44. 12 Hayashi E, Takata K, Sato Y et al. Distinct morphologic, phenotypic, and clinical-course characteristics of indolent peripheral T-cell lymphoma. Hum Pathol. 2013; 44: 1927-1936. 22 Katzenellenbogen RA, Baylin SB, Herman JG. Hypermethylation of the DAP-kinase CpG island is a common alteration in B-cell malignancies. Blood. 1999; 93: 4347-4353. 17 Tompkins JD, Hall C, Chen VC et al. Epigenetic stability, adaptability, and reversibility in human embryonic stem cells. Proc Natl Acad Sci USA. 2012; 109: 12544-12549. 18 Kamb A, Gruis NA, Weaver-Feldhaus J et al. A cell cycle regulator potentially involved in genesis of many tumor types. Science. 1994; 264: 436-440. 4 Takata K, Tanino M, Ennishi D et al. Duodenal follicular lymphoma: comprehensive gene expression analysis with insights into pathogenesis. Cancer Sci. 2014; 105: 608-615. 5 Hellmuth JC, Louissaint A Jr, Szczepanowski M et al. Duodenal-type and nodal follicular lymphomas differ by their immune microenvironment rather than their mutation profiles. Blood. 2018; 132: 1695-1702. 2 Takata K, Sato Y, Nakamura N et al. Duodenal and nodal follicular lymphomas are distinct: the former lacks activation-induced cytidine deaminase and follicular dendritic cells despite ongoing somatic hypermutations. Mod Pathol. 2009; 22: 940-949. 19 Martinez-Delgado B, Robledo M, Arranz E et al. Hypermethylation of p15/ink4b/MTS2 gene is differentially implicated among non-Hodgkin’s lymphomas. Leukemia. 1998; 12: 937-941. 11 22 12 23 13 24 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 10 21 |
| References_xml | – reference: 7 van Vollenhoven RF, Bieber MM, Powell MJ et al. VH4-34 encoded antibodies in systemic lupus erythematosus: a specific diagnostic marker that correlates with clinical disease characteristics. J Rheumatol. 1999; 26: 1727-1733. – reference: 9 O’Riain C, O’Shea DM, Yang Y et al. Array-based DNA methylation profiling in follicular lymphoma. Leukemia. 2009; 23: 1858-1866. – reference: 8 Kaneko Y, Sakurai S, Hironaka M et al. Distinct methylated profiles in Helicobacter pylori dependent and independent gastric MALT lymphomas. Gut. 2003; 52: 641-646. – reference: 11 Kondo T, Oka T, Sato H et al. Accumulation of aberrant CpG hypermethylation by Helicobacter pylori infection promotes development and progression of gastric MALT lymphoma. Int J Oncol. 2009; 35: 547-557. – reference: 13 Ohnishi N, Takata K, Miyata-Takata T et al. CD10 down expression in follicular lymphoma correlates with gastrointestinal lesion involving the stomach and large intestine. Cancer Sci. 2016; 107: 1687-1695. – reference: 17 Tompkins JD, Hall C, Chen VC et al. Epigenetic stability, adaptability, and reversibility in human embryonic stem cells. Proc Natl Acad Sci USA. 2012; 109: 12544-12549. – reference: 23 Nakatsuka S, Takakuwa T, Tomita Y et al. Hypermethylation of death‐associated protein (DAP) kinase CpG island is frequent not only in B‐cell but also in T‐ and natural killer (NK)/T‐cell malignancies. Cancer Sci. 2003; 94: 87-91. – reference: 15 Sato H, Oka T, Shinnou Y et al. Multi-step aberrant CpG island hyper-methylation is associated with the progression of adult T-cell leukemia/lymphoma. Am J Pathol. 2010; 176: 402-415. – reference: 14 Rohatiner A, d’Amore F, Coiffier B et al. Report on a workshop convened to discuss the pathological and staging classifications of gastrointestinal tract lymphoma. Ann Oncol. 1994; 5: 397-400. – reference: 20 Baur AS, Shaw P, Burri N et al. Frequent methylation silencing of p15(INK4b) (MTS2) and p16(INK4a) (MTS1) in B-cell and T-cell lymphomas. Blood. 1999; 94: 1773-1781. – reference: 10 Guo J, Burger M, Nimmrich I et al. Differential DNA methylation of gene promoters in small B-cell lymphomas. Am J Clin Pathol. 2005; 124: 430-439. – reference: 24 Rossi D, Capello D, Gloghini A et al. Aberrant promoter methylation of multiple genes throughout the clinico-pathologic spectrum of B-cell neoplasia. Haematologica. 2004; 89: 154-164. – reference: 18 Kamb A, Gruis NA, Weaver-Feldhaus J et al. A cell cycle regulator potentially involved in genesis of many tumor types. Science. 1994; 264: 436-440. – reference: 6 Arons E, Suntum T, Stetler-Stevenson M, Kreitman RJ. VH4-34+ hairy cell leukemia, a new variant with poor prognosis despite standard therapy. Blood. 2009; 114: 4687-4695. – reference: 16 Hayslip J, Montero A. Tumor suppressor gene methylation in follicular lymphoma: a comprehensive review. Mol Cancer. 2006; 5: 44. – reference: 2 Takata K, Sato Y, Nakamura N et al. Duodenal and nodal follicular lymphomas are distinct: the former lacks activation-induced cytidine deaminase and follicular dendritic cells despite ongoing somatic hypermutations. Mod Pathol. 2009; 22: 940-949. – reference: 21 Deiss LP, Feinstein E, Berissi H, Cohen O, Kimchi A. Identification of a novel serine/threonine kinase and a novel 15-kD protein as potential mediators of the gamma interferon-induced cell death. Genes Dev. 1995; 9: 15-30. – reference: 5 Hellmuth JC, Louissaint A Jr, Szczepanowski M et al. Duodenal-type and nodal follicular lymphomas differ by their immune microenvironment rather than their mutation profiles. Blood. 2018; 132: 1695-1702. – reference: 1 Takata K, Okada H, Ohmiya N et al. Primary gastrointestinal follicular lymphoma involving the duodenal second portion is a distinct entity: a multicenter, retrospective analysis in Japan. Cancer Sci. 2011; 102: 1532-1536. – reference: 12 Hayashi E, Takata K, Sato Y et al. Distinct morphologic, phenotypic, and clinical-course characteristics of indolent peripheral T-cell lymphoma. Hum Pathol. 2013; 44: 1927-1936. – reference: 3 Takata K, Sato Y, Nakamura N et al. Duodenal follicular lymphoma lacks AID but expresses BACH2 and has memory B-cell characteristics. Mod Pathol. 2013; 26: 22-31. – reference: 22 Katzenellenbogen RA, Baylin SB, Herman JG. Hypermethylation of the DAP-kinase CpG island is a common alteration in B-cell malignancies. Blood. 1999; 93: 4347-4353. – reference: 4 Takata K, Tanino M, Ennishi D et al. Duodenal follicular lymphoma: comprehensive gene expression analysis with insights into pathogenesis. Cancer Sci. 2014; 105: 608-615. – reference: 19 Martinez-Delgado B, Robledo M, Arranz E et al. Hypermethylation of p15/ink4b/MTS2 gene is differentially implicated among non-Hodgkin’s lymphomas. Leukemia. 1998; 12: 937-941. – ident: 18 doi: 10.1126/science.8153634 – ident: 6 doi: 10.1182/blood-2009-01-201731 – ident: 11 doi: 10.3892/ijo_00000366 – ident: 10 doi: 10.1309/LCGNV77J464LNFD6 – ident: 3 doi: 10.1038/modpathol.2012.127 – ident: 15 doi: 10.2353/ajpath.2010.090236 – ident: 21 doi: 10.1101/gad.9.1.15 – ident: 23 doi: 10.1111/j.1349-7006.2003.tb01357.x – ident: 8 doi: 10.1136/gut.52.5.641 – ident: 22 doi: 10.1182/blood.V93.12.4347.412k31_4347_4353 – ident: 14 doi: 10.1093/oxfordjournals.annonc.a058869 – ident: 19 doi: 10.1038/sj.leu.2401009 – ident: 12 doi: 10.1016/j.humpath.2013.03.002 – ident: 20 doi: 10.1182/blood.V94.5.1773 – ident: 1 doi: 10.1111/j.1349-7006.2011.01980.x – ident: 4 doi: 10.1111/cas.12392 – ident: 5 doi: 10.1182/blood-2018-03-837252 – ident: 16 doi: 10.1186/1476-4598-5-44 – ident: 24 – ident: 7 – ident: 17 doi: 10.1073/pnas.1209620109 – ident: 2 doi: 10.1038/modpathol.2009.51 – ident: 9 doi: 10.1038/leu.2009.114 – ident: 13 doi: 10.1111/cas.13031 |
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| SubjectTerms | Adult Aged CDKN2B/P15 Cyclin-Dependent Kinase Inhibitor p15 - genetics Cyclin-Dependent Kinase Inhibitor p15 - metabolism DAPK1 Death-Associated Protein Kinases - genetics DNA Methylation Duodenal Neoplasms - genetics Duodenal Neoplasms - metabolism Duodenal Neoplasms - pathology duodenal reactive hyperplasia Female Humans Lymphoma, Follicular - genetics Lymphoma, Follicular - metabolism Lymphoma, Follicular - pathology Male methylation profile Middle Aged Original Pseudolymphoma - genetics Pseudolymphoma - pathology |
| Title | Frequent CDKN2B/P15 and DAPK1 methylation in duodenal follicular lymphoma is related to duodenal reactive lymphoid hyperplasia |
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