MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response

Weixin Wang, Meghan Corrigan-Cummins, Justin Hudson, Irina Maric, Olga Simakova, Sattva S. Neelapu, Larry W. Kwak, John Edward Janik, Barry Gause, Elaine S. Jaffe, Katherine R. Calvo

Research output: Contribution to journalArticle

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Abstract

Background MicroRNAs can play an important role in tumorigenesis through post-transcriptional regulation of gene expression, and are not well characterized in follicular lymphoma. Design and Methods MicroRNA profiles of enriched follicular lymphoma tumor cells from 16 patients were generated by assaying 851 human microRNAs. Tandem gene expression profiles were obtained for predicting microRNA targets. Results The expression of 133 microRNAs was significantly different (> 2-fold; P<0.05) between follicular lymphoma and follicular hyperplasia. Forty-four microRNAs in three groups generated a unique follicular lymphoma signature. Of these, ten microRNAs were increased (miR-193a-5p, - 193b*, -345, -513b, -574-3p, -584, -663, -1287, -1295, and -1471), 11 microRNAs were decreased (miR-17*, -30a, -33a, -106a*, -141, -202, -205, -222, -301b, -431*, and -570), and 23 microRNAs formed a group that was increased in most cases of follicular lymphoma but showed lower expression in a subset of cases (let-7a, let-7f, miR-7-1*, -9, -9*, -20a, -20b, -30b, -96, -98, -194, -195, -221*, -374a, -374b, -451, -454, -502-3p, -532-3p, -664*, -1274a, -1274b, and -1260). Higher expression of this last group was associated with improved response to chemotherapy. Gene expression analysis revealed increased expression of MAPK1, AKT1, PRKCE, IL4R and DROSHA and decreased expression of CDKN1A/p21, SOCS2, CHEK1, RAD51, KLF4, BLIMP1 and IRF4 in follicular lymphoma. Functional studies indicated that CDKN1A/p21 and SOCS2 expression is directly regulated by miR-20a/-20b and miR-194, respectively. Conclusions Follicular lymphoma is characterized by a unique microRNA signature, containing a subset of microRNAs whose expression correlate with response to chemotherapy. miR-20a/b and miR- 194 target CDKN1A and SOCS2 in follicular lymphoma, potentially contributing to tumor cell proliferation and survival.

Original languageEnglish (US)
Pages (from-to)586-594
Number of pages9
JournalHaematologica
Volume97
Issue number4
DOIs
StatePublished - Apr 1 2012

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Follicular Lymphoma
MicroRNAs
Cell Proliferation
Neoplasms
Drug Therapy
Gene Expression Regulation
Transcriptome
Hyperplasia
Cell Survival
Carcinogenesis

Keywords

  • Follicular lymphoma
  • Lymphomagenesis
  • MiRNA
  • Tumor response

ASJC Scopus subject areas

  • Hematology

Cite this

Wang, W., Corrigan-Cummins, M., Hudson, J., Maric, I., Simakova, O., Neelapu, S. S., ... Calvo, K. R. (2012). MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response. Haematologica, 97(4), 586-594. https://doi.org/10.3324/haematol.2011.048132

MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response. / Wang, Weixin; Corrigan-Cummins, Meghan; Hudson, Justin; Maric, Irina; Simakova, Olga; Neelapu, Sattva S.; Kwak, Larry W.; Janik, John Edward; Gause, Barry; Jaffe, Elaine S.; Calvo, Katherine R.

In: Haematologica, Vol. 97, No. 4, 01.04.2012, p. 586-594.

Research output: Contribution to journalArticle

Wang, W, Corrigan-Cummins, M, Hudson, J, Maric, I, Simakova, O, Neelapu, SS, Kwak, LW, Janik, JE, Gause, B, Jaffe, ES & Calvo, KR 2012, 'MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response', Haematologica, vol. 97, no. 4, pp. 586-594. https://doi.org/10.3324/haematol.2011.048132
Wang, Weixin ; Corrigan-Cummins, Meghan ; Hudson, Justin ; Maric, Irina ; Simakova, Olga ; Neelapu, Sattva S. ; Kwak, Larry W. ; Janik, John Edward ; Gause, Barry ; Jaffe, Elaine S. ; Calvo, Katherine R. / MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response. In: Haematologica. 2012 ; Vol. 97, No. 4. pp. 586-594.
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abstract = "Background MicroRNAs can play an important role in tumorigenesis through post-transcriptional regulation of gene expression, and are not well characterized in follicular lymphoma. Design and Methods MicroRNA profiles of enriched follicular lymphoma tumor cells from 16 patients were generated by assaying 851 human microRNAs. Tandem gene expression profiles were obtained for predicting microRNA targets. Results The expression of 133 microRNAs was significantly different (> 2-fold; P<0.05) between follicular lymphoma and follicular hyperplasia. Forty-four microRNAs in three groups generated a unique follicular lymphoma signature. Of these, ten microRNAs were increased (miR-193a-5p, - 193b*, -345, -513b, -574-3p, -584, -663, -1287, -1295, and -1471), 11 microRNAs were decreased (miR-17*, -30a, -33a, -106a*, -141, -202, -205, -222, -301b, -431*, and -570), and 23 microRNAs formed a group that was increased in most cases of follicular lymphoma but showed lower expression in a subset of cases (let-7a, let-7f, miR-7-1*, -9, -9*, -20a, -20b, -30b, -96, -98, -194, -195, -221*, -374a, -374b, -451, -454, -502-3p, -532-3p, -664*, -1274a, -1274b, and -1260). Higher expression of this last group was associated with improved response to chemotherapy. Gene expression analysis revealed increased expression of MAPK1, AKT1, PRKCE, IL4R and DROSHA and decreased expression of CDKN1A/p21, SOCS2, CHEK1, RAD51, KLF4, BLIMP1 and IRF4 in follicular lymphoma. Functional studies indicated that CDKN1A/p21 and SOCS2 expression is directly regulated by miR-20a/-20b and miR-194, respectively. Conclusions Follicular lymphoma is characterized by a unique microRNA signature, containing a subset of microRNAs whose expression correlate with response to chemotherapy. miR-20a/b and miR- 194 target CDKN1A and SOCS2 in follicular lymphoma, potentially contributing to tumor cell proliferation and survival.",
keywords = "Follicular lymphoma, Lymphomagenesis, MiRNA, Tumor response",
author = "Weixin Wang and Meghan Corrigan-Cummins and Justin Hudson and Irina Maric and Olga Simakova and Neelapu, {Sattva S.} and Kwak, {Larry W.} and Janik, {John Edward} and Barry Gause and Jaffe, {Elaine S.} and Calvo, {Katherine R.}",
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T1 - MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response

AU - Wang, Weixin

AU - Corrigan-Cummins, Meghan

AU - Hudson, Justin

AU - Maric, Irina

AU - Simakova, Olga

AU - Neelapu, Sattva S.

AU - Kwak, Larry W.

AU - Janik, John Edward

AU - Gause, Barry

AU - Jaffe, Elaine S.

AU - Calvo, Katherine R.

PY - 2012/4/1

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N2 - Background MicroRNAs can play an important role in tumorigenesis through post-transcriptional regulation of gene expression, and are not well characterized in follicular lymphoma. Design and Methods MicroRNA profiles of enriched follicular lymphoma tumor cells from 16 patients were generated by assaying 851 human microRNAs. Tandem gene expression profiles were obtained for predicting microRNA targets. Results The expression of 133 microRNAs was significantly different (> 2-fold; P<0.05) between follicular lymphoma and follicular hyperplasia. Forty-four microRNAs in three groups generated a unique follicular lymphoma signature. Of these, ten microRNAs were increased (miR-193a-5p, - 193b*, -345, -513b, -574-3p, -584, -663, -1287, -1295, and -1471), 11 microRNAs were decreased (miR-17*, -30a, -33a, -106a*, -141, -202, -205, -222, -301b, -431*, and -570), and 23 microRNAs formed a group that was increased in most cases of follicular lymphoma but showed lower expression in a subset of cases (let-7a, let-7f, miR-7-1*, -9, -9*, -20a, -20b, -30b, -96, -98, -194, -195, -221*, -374a, -374b, -451, -454, -502-3p, -532-3p, -664*, -1274a, -1274b, and -1260). Higher expression of this last group was associated with improved response to chemotherapy. Gene expression analysis revealed increased expression of MAPK1, AKT1, PRKCE, IL4R and DROSHA and decreased expression of CDKN1A/p21, SOCS2, CHEK1, RAD51, KLF4, BLIMP1 and IRF4 in follicular lymphoma. Functional studies indicated that CDKN1A/p21 and SOCS2 expression is directly regulated by miR-20a/-20b and miR-194, respectively. Conclusions Follicular lymphoma is characterized by a unique microRNA signature, containing a subset of microRNAs whose expression correlate with response to chemotherapy. miR-20a/b and miR- 194 target CDKN1A and SOCS2 in follicular lymphoma, potentially contributing to tumor cell proliferation and survival.

AB - Background MicroRNAs can play an important role in tumorigenesis through post-transcriptional regulation of gene expression, and are not well characterized in follicular lymphoma. Design and Methods MicroRNA profiles of enriched follicular lymphoma tumor cells from 16 patients were generated by assaying 851 human microRNAs. Tandem gene expression profiles were obtained for predicting microRNA targets. Results The expression of 133 microRNAs was significantly different (> 2-fold; P<0.05) between follicular lymphoma and follicular hyperplasia. Forty-four microRNAs in three groups generated a unique follicular lymphoma signature. Of these, ten microRNAs were increased (miR-193a-5p, - 193b*, -345, -513b, -574-3p, -584, -663, -1287, -1295, and -1471), 11 microRNAs were decreased (miR-17*, -30a, -33a, -106a*, -141, -202, -205, -222, -301b, -431*, and -570), and 23 microRNAs formed a group that was increased in most cases of follicular lymphoma but showed lower expression in a subset of cases (let-7a, let-7f, miR-7-1*, -9, -9*, -20a, -20b, -30b, -96, -98, -194, -195, -221*, -374a, -374b, -451, -454, -502-3p, -532-3p, -664*, -1274a, -1274b, and -1260). Higher expression of this last group was associated with improved response to chemotherapy. Gene expression analysis revealed increased expression of MAPK1, AKT1, PRKCE, IL4R and DROSHA and decreased expression of CDKN1A/p21, SOCS2, CHEK1, RAD51, KLF4, BLIMP1 and IRF4 in follicular lymphoma. Functional studies indicated that CDKN1A/p21 and SOCS2 expression is directly regulated by miR-20a/-20b and miR-194, respectively. Conclusions Follicular lymphoma is characterized by a unique microRNA signature, containing a subset of microRNAs whose expression correlate with response to chemotherapy. miR-20a/b and miR- 194 target CDKN1A and SOCS2 in follicular lymphoma, potentially contributing to tumor cell proliferation and survival.

KW - Follicular lymphoma

KW - Lymphomagenesis

KW - MiRNA

KW - Tumor response

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