Long Noncoding RNA Ceruloplasmin Promotes Cancer Growth by Altering Glycolysis

Rajesha Rupaimoole; Jaehyuk Lee; Monika Haemmerle; Hui Ling; Rebecca A. Previs; Sunila Pradeep; Sherry Y. Wu; Cristina Ivan; Manuela Ferracin; Jennifer B. Dennison; Niki M.Zacharias Millward; Archana S. Nagaraja; Kshipra M. Gharpure; Michael McGuire; Nidhin Sam; Guillermo N. Armaiz-Pena; Nouara C. Sadaoui; Cristian Rodriguez-Aguayo; George A. Calin; Ronny I. Drapkin; Jeffery Kovacs; Gordon B. Mills; Wei Zhang; Gabriel Lopez-Berestein; Pratip K. Bhattacharya; Anil K. Sood

doi:10.1016/j.celrep.2015.11.047

Long Noncoding RNA Ceruloplasmin Promotes Cancer Growth by Altering Glycolysis

Rajesha Rupaimoole, Jaehyuk Lee, Monika Haemmerle, Hui Ling, Rebecca A. Previs, Sunila Pradeep, Sherry Y. Wu, Cristina Ivan, Manuela Ferracin, Jennifer B. Dennison, Niki M.Zacharias Millward, Archana S. Nagaraja, Kshipra M. Gharpure, Michael McGuire, Nidhin Sam, Guillermo N. Armaiz-Pena, Nouara C. Sadaoui, Cristian Rodriguez-Aguayo, George A. Calin, Ronny I. DrapkinJeffery Kovacs, Gordon B. Mills, Wei Zhang, Gabriel Lopez-Berestein, Pratip K. Bhattacharya, Anil K. Sood

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96 Scopus citations

Abstract

Long noncoding RNAs (lncRNAs) significantly influence the development and regulation of genome expression in cells. Here, we demonstrate the role of lncRNA ceruloplasmin (NRCP) in cancer metabolism and elucidate functional effects leading to increased tumor progression. NRCP was highly upregulated in ovarian tumors, and knockdown of NRCP resulted in significantly increased apoptosis, decreased cell proliferation, and decreased glycolysis compared with control cancer cells. In an orthotopic mouse model of ovarian cancer, siNRCP delivered via a liposomal carrier significantly reduced tumor growth compared with control treatment. We identified NRCP as an intermediate binding partner between STAT1 and RNA polymerase II, leading to increased expression of downstream target genes such as glucose-6-phosphate isomerase. Collectively, we report a previously unrecognized role of the lncRNA NRCP in modulating cancer metabolism. As demonstrated, DOPC nanoparticle-incorporated siRNA-mediated silencing of this lncRNA in vivo provides therapeutic avenue toward modulating lncRNAs in cancer.

Original language	English (US)
Pages (from-to)	2395-2402
Number of pages	8
Journal	Cell Reports
Volume	13
Issue number	11
DOIs	https://doi.org/10.1016/j.celrep.2015.11.047
State	Published - Dec 22 2015
Externally published	Yes

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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Rupaimoole, R., Lee, J., Haemmerle, M., Ling, H., Previs, R. A., Pradeep, S., Wu, S. Y., Ivan, C., Ferracin, M., Dennison, J. B., Millward, N. M. Z., Nagaraja, A. S., Gharpure, K. M., McGuire, M., Sam, N., Armaiz-Pena, G. N., Sadaoui, N. C., Rodriguez-Aguayo, C., Calin, G. A., ... Sood, A. K. (2015). Long Noncoding RNA Ceruloplasmin Promotes Cancer Growth by Altering Glycolysis. Cell Reports, 13(11), 2395-2402. https://doi.org/10.1016/j.celrep.2015.11.047

Rupaimoole, R, Lee, J, Haemmerle, M, Ling, H, Previs, RA, Pradeep, S, Wu, SY, Ivan, C, Ferracin, M, Dennison, JB, Millward, NMZ, Nagaraja, AS, Gharpure, KM, McGuire, M, Sam, N, Armaiz-Pena, GN, Sadaoui, NC, Rodriguez-Aguayo, C, Calin, GA, Drapkin, RI, Kovacs, J, Mills, GB, Zhang, W, Lopez-Berestein, G, Bhattacharya, PK & Sood, AK 2015, 'Long Noncoding RNA Ceruloplasmin Promotes Cancer Growth by Altering Glycolysis', Cell Reports, vol. 13, no. 11, pp. 2395-2402. https://doi.org/10.1016/j.celrep.2015.11.047

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title = "Long Noncoding RNA Ceruloplasmin Promotes Cancer Growth by Altering Glycolysis",

abstract = "Long noncoding RNAs (lncRNAs) significantly influence the development and regulation of genome expression in cells. Here, we demonstrate the role of lncRNA ceruloplasmin (NRCP) in cancer metabolism and elucidate functional effects leading to increased tumor progression. NRCP was highly upregulated in ovarian tumors, and knockdown of NRCP resulted in significantly increased apoptosis, decreased cell proliferation, and decreased glycolysis compared with control cancer cells. In an orthotopic mouse model of ovarian cancer, siNRCP delivered via a liposomal carrier significantly reduced tumor growth compared with control treatment. We identified NRCP as an intermediate binding partner between STAT1 and RNA polymerase II, leading to increased expression of downstream target genes such as glucose-6-phosphate isomerase. Collectively, we report a previously unrecognized role of the lncRNA NRCP in modulating cancer metabolism. As demonstrated, DOPC nanoparticle-incorporated siRNA-mediated silencing of this lncRNA in vivo provides therapeutic avenue toward modulating lncRNAs in cancer.",

author = "Rajesha Rupaimoole and Jaehyuk Lee and Monika Haemmerle and Hui Ling and Previs, {Rebecca A.} and Sunila Pradeep and Wu, {Sherry Y.} and Cristina Ivan and Manuela Ferracin and Dennison, {Jennifer B.} and Millward, {Niki M.Zacharias} and Nagaraja, {Archana S.} and Gharpure, {Kshipra M.} and Michael McGuire and Nidhin Sam and Armaiz-Pena, {Guillermo N.} and Sadaoui, {Nouara C.} and Cristian Rodriguez-Aguayo and Calin, {George A.} and Drapkin, {Ronny I.} and Jeffery Kovacs and Mills, {Gordon B.} and Wei Zhang and Gabriel Lopez-Berestein and Bhattacharya, {Pratip K.} and Sood, {Anil K.}",

note = "Publisher Copyright: {\textcopyright} 2015 The Authors.",

year = "2015",

month = dec,

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doi = "10.1016/j.celrep.2015.11.047",

language = "English (US)",

volume = "13",

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T1 - Long Noncoding RNA Ceruloplasmin Promotes Cancer Growth by Altering Glycolysis

AU - Rupaimoole, Rajesha

AU - Lee, Jaehyuk

AU - Haemmerle, Monika

AU - Ling, Hui

AU - Previs, Rebecca A.

AU - Pradeep, Sunila

AU - Wu, Sherry Y.

AU - Ivan, Cristina

AU - Ferracin, Manuela

AU - Dennison, Jennifer B.

AU - Millward, Niki M.Zacharias

AU - Nagaraja, Archana S.

AU - Gharpure, Kshipra M.

AU - McGuire, Michael

AU - Sam, Nidhin

AU - Armaiz-Pena, Guillermo N.

AU - Sadaoui, Nouara C.

AU - Rodriguez-Aguayo, Cristian

AU - Calin, George A.

AU - Drapkin, Ronny I.

AU - Kovacs, Jeffery

AU - Mills, Gordon B.

AU - Zhang, Wei

AU - Lopez-Berestein, Gabriel

AU - Bhattacharya, Pratip K.

AU - Sood, Anil K.

PY - 2015/12/22

Y1 - 2015/12/22

N2 - Long noncoding RNAs (lncRNAs) significantly influence the development and regulation of genome expression in cells. Here, we demonstrate the role of lncRNA ceruloplasmin (NRCP) in cancer metabolism and elucidate functional effects leading to increased tumor progression. NRCP was highly upregulated in ovarian tumors, and knockdown of NRCP resulted in significantly increased apoptosis, decreased cell proliferation, and decreased glycolysis compared with control cancer cells. In an orthotopic mouse model of ovarian cancer, siNRCP delivered via a liposomal carrier significantly reduced tumor growth compared with control treatment. We identified NRCP as an intermediate binding partner between STAT1 and RNA polymerase II, leading to increased expression of downstream target genes such as glucose-6-phosphate isomerase. Collectively, we report a previously unrecognized role of the lncRNA NRCP in modulating cancer metabolism. As demonstrated, DOPC nanoparticle-incorporated siRNA-mediated silencing of this lncRNA in vivo provides therapeutic avenue toward modulating lncRNAs in cancer.

AB - Long noncoding RNAs (lncRNAs) significantly influence the development and regulation of genome expression in cells. Here, we demonstrate the role of lncRNA ceruloplasmin (NRCP) in cancer metabolism and elucidate functional effects leading to increased tumor progression. NRCP was highly upregulated in ovarian tumors, and knockdown of NRCP resulted in significantly increased apoptosis, decreased cell proliferation, and decreased glycolysis compared with control cancer cells. In an orthotopic mouse model of ovarian cancer, siNRCP delivered via a liposomal carrier significantly reduced tumor growth compared with control treatment. We identified NRCP as an intermediate binding partner between STAT1 and RNA polymerase II, leading to increased expression of downstream target genes such as glucose-6-phosphate isomerase. Collectively, we report a previously unrecognized role of the lncRNA NRCP in modulating cancer metabolism. As demonstrated, DOPC nanoparticle-incorporated siRNA-mediated silencing of this lncRNA in vivo provides therapeutic avenue toward modulating lncRNAs in cancer.

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ER -

Long Noncoding RNA Ceruloplasmin Promotes Cancer Growth by Altering Glycolysis

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