Copy Number Gain of hsa-miR-569 at 3q26.2 Leads to Loss of TP53INP1 and Aggressiveness of Epithelial Cancers

Pradeep Chaluvally-Raghavan; Fan Zhang; Sunila Pradeep; Mark P. Hamilton; Xi Zhao; Rajesha Rupaimoole; Tyler Moss; Yiling Lu; Shuangxing Yu; Chad V. Pecot; Miriam R. Aure; Sylvain Peuget; Cristian Rodriguez-Aguayo; Hee Dong Han; Dong Zhang; Avinashnarayan Venkatanarayan; Marit Krohn; Vessela N. Kristensen; Mihai Gagea; Prahlad Ram; Wenbin Liu; Gabriel Lopez-Berestein; Philip L. Lorenzi; Anne Lise Børresen-Dale; Koei Chin; Joe Gray; Nelson J. Dusetti; Sean E. McGuire; Elsa R. Flores; Anil K. Sood; Gordon B. Mills

doi:10.1016/j.ccell.2014.10.010

Copy Number Gain of hsa-miR-569 at 3q26.2 Leads to Loss of TP53INP1 and Aggressiveness of Epithelial Cancers

Pradeep Chaluvally-Raghavan
, Fan Zhang
, Sunila Pradeep
, Mark P. Hamilton
, Xi Zhao
, Rajesha Rupaimoole
, Tyler Moss
, Yiling Lu
, Shuangxing Yu
, Chad V. Pecot
, Miriam R. Aure
, Sylvain Peuget
, Cristian Rodriguez-Aguayo
, Hee Dong Han
, Dong Zhang
, Avinashnarayan Venkatanarayan
, Marit Krohn
, Vessela N. Kristensen
, Mihai Gagea
, Prahlad Ram

Wenbin Liu, Gabriel Lopez-Berestein, Philip L. Lorenzi, Anne Lise Børresen-Dale, Koei Chin, Joe Gray, Nelson J. Dusetti, Sean E. McGuire, Elsa R. Flores, Anil K. Sood, Gordon B. Mills

Research output: Contribution to journal › Article › peer-review

50 Scopus citations

Abstract

Small noncoding miRNAs represent underexplored targets of genomic aberrations and emerging therapeutic targets. The 3q26.2 amplicon is among the most frequent genomic aberrations in multiple cancer lineages including ovarian and breast cancers. We demonstrate that hsa-miR-569 (hereafter designated as miR569), which is overexpressed in a subset of ovarian and breast cancers, at least in part due to the 3q26.2 amplicon, alters cell survival and proliferation. Downregulation of TP53INP1 expression by miR569 is required for the effects of miR569 on survival and proliferation. Targeting miR569 sensitizes ovarian and breast cancer cells overexpressing miR569 to cisplatin by increasing cell death both invitro and invivo. Thus targeting miR569 could potentially benefit patients with the 3q26.2 amplicon and subsequent miR569 elevation.

Original language	English (US)
Pages (from-to)	863-879
Number of pages	17
Journal	Cancer Cell
Volume	26
Issue number	6
DOIs	https://doi.org/10.1016/j.ccell.2014.10.010
State	Published - Dec 8 2014

Funding

G.B.M. is supported by NCI (2P50CA083639-11, 5P50CA058183-17, and 5R01CA123219-01), Stand up to Cancer/American Association of Cancer Research (SU2C-AACR-DT0209), and Komen Promise Grant (KG081694). P.C.R. is supported by Ann Schreiber Program for Excellence grant from Ovarian Cancer Research Fund and Scientific scholar award from Marsha Rivkin Center for Ovarian Cancer Research. J.W.G. is supported by NCI (P50CA58207 and U54CA112970). A.K.S. is supported by NCI (P50CA083639, P50CA098258, and U54CA151668). We thank Lydia W.T. Cheung for helpful insights. We acknowledge technical help from Nitin Puri and Varun Bagai, Ambion, Life Technologies, Austin, Texas for the RNAi studies. We thank Ronny Drapkin, Marian Novak, and Alison Karst for providing RNA extracted from normal fallopian tube samples. G.B.M. received sponsored research support from AstraZeneca, GlaxoSmithKline, Celgene, Exelixis, Roche, and Wyeth/Pfizer and has served as consultant to AstraZeneca, Celgene, Enzon, Hanall Bio, Novartis, Nuevolution, Symphogen, and Wyeth/Pfizer.

Funders	Funder number
Author National Institutes of Health National Institutes of Health National Institutes of Health National Institutes of Health The Bev Hartig Huntington's Disease Foundation National Institutes of Health
National Institute of Health-National Cancer Institute	5P50CA058183-17, P50CA083639, R01CA123219, U54CA151668, KG081694, P50CA098258, U54CA112970, SU2C-AACR-DT0209
Ovarian Cancer Research Fund
Marsha Rivkin Center for Ovarian Cancer Research	P50CA58207
GlaxoSmithKline
Roche
Celgene
Exelixis
AstraZeneca Schweiz

ASJC Scopus subject areas

Oncology
Cancer Research

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10.1016/j.ccell.2014.10.010

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Chaluvally-Raghavan, P., Zhang, F., Pradeep, S., Hamilton, M. P., Zhao, X., Rupaimoole, R., Moss, T., Lu, Y., Yu, S., Pecot, C. V., Aure, M. R., Peuget, S., Rodriguez-Aguayo, C., Han, H. D., Zhang, D., Venkatanarayan, A., Krohn, M., Kristensen, V. N., Gagea, M., ... Mills, G. B. (2014). Copy Number Gain of hsa-miR-569 at 3q26.2 Leads to Loss of TP53INP1 and Aggressiveness of Epithelial Cancers. Cancer Cell, 26(6), 863-879. https://doi.org/10.1016/j.ccell.2014.10.010

Chaluvally-Raghavan, P, Zhang, F, Pradeep, S, Hamilton, MP, Zhao, X, Rupaimoole, R, Moss, T, Lu, Y, Yu, S, Pecot, CV, Aure, MR, Peuget, S, Rodriguez-Aguayo, C, Han, HD, Zhang, D, Venkatanarayan, A, Krohn, M, Kristensen, VN, Gagea, M, Ram, P, Liu, W, Lopez-Berestein, G, Lorenzi, PL, Børresen-Dale, AL, Chin, K , Gray, J, Dusetti, NJ, McGuire, SE, Flores, ER, Sood, AK & Mills, GB 2014, 'Copy Number Gain of hsa-miR-569 at 3q26.2 Leads to Loss of TP53INP1 and Aggressiveness of Epithelial Cancers', Cancer Cell, vol. 26, no. 6, pp. 863-879. https://doi.org/10.1016/j.ccell.2014.10.010

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title = "Copy Number Gain of hsa-miR-569 at 3q26.2 Leads to Loss of TP53INP1 and Aggressiveness of Epithelial Cancers",

abstract = "Small noncoding miRNAs represent underexplored targets of genomic aberrations and emerging therapeutic targets. The 3q26.2 amplicon is among the most frequent genomic aberrations in multiple cancer lineages including ovarian and breast cancers. We demonstrate that hsa-miR-569 (hereafter designated as miR569), which is overexpressed in a subset of ovarian and breast cancers, at least in part due to the 3q26.2 amplicon, alters cell survival and proliferation. Downregulation of TP53INP1 expression by miR569 is required for the effects of miR569 on survival and proliferation. Targeting miR569 sensitizes ovarian and breast cancer cells overexpressing miR569 to cisplatin by increasing cell death both invitro and invivo. Thus targeting miR569 could potentially benefit patients with the 3q26.2 amplicon and subsequent miR569 elevation.",

author = "Pradeep Chaluvally-Raghavan and Fan Zhang and Sunila Pradeep and Hamilton, \{Mark P.\} and Xi Zhao and Rajesha Rupaimoole and Tyler Moss and Yiling Lu and Shuangxing Yu and Pecot, \{Chad V.\} and Aure, \{Miriam R.\} and Sylvain Peuget and Cristian Rodriguez-Aguayo and Han, \{Hee Dong\} and Dong Zhang and Avinashnarayan Venkatanarayan and Marit Krohn and Kristensen, \{Vessela N.\} and Mihai Gagea and Prahlad Ram and Wenbin Liu and Gabriel Lopez-Berestein and Lorenzi, \{Philip L.\} and B{\o}rresen-Dale, \{Anne Lise\} and Koei Chin and Joe Gray and Dusetti, \{Nelson J.\} and McGuire, \{Sean E.\} and Flores, \{Elsa R.\} and Sood, \{Anil K.\} and Mills, \{Gordon B.\}",

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doi = "10.1016/j.ccell.2014.10.010",

language = "English (US)",

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T1 - Copy Number Gain of hsa-miR-569 at 3q26.2 Leads to Loss of TP53INP1 and Aggressiveness of Epithelial Cancers

AU - Chaluvally-Raghavan, Pradeep

AU - Zhang, Fan

AU - Pradeep, Sunila

AU - Hamilton, Mark P.

AU - Zhao, Xi

AU - Rupaimoole, Rajesha

AU - Moss, Tyler

AU - Lu, Yiling

AU - Yu, Shuangxing

AU - Pecot, Chad V.

AU - Aure, Miriam R.

AU - Peuget, Sylvain

AU - Rodriguez-Aguayo, Cristian

AU - Han, Hee Dong

AU - Zhang, Dong

AU - Venkatanarayan, Avinashnarayan

AU - Krohn, Marit

AU - Kristensen, Vessela N.

AU - Gagea, Mihai

AU - Ram, Prahlad

AU - Liu, Wenbin

AU - Lopez-Berestein, Gabriel

AU - Lorenzi, Philip L.

AU - Børresen-Dale, Anne Lise

AU - Chin, Koei

AU - Gray, Joe

AU - Dusetti, Nelson J.

AU - McGuire, Sean E.

AU - Flores, Elsa R.

AU - Sood, Anil K.

AU - Mills, Gordon B.

PY - 2014/12/8

Y1 - 2014/12/8

N2 - Small noncoding miRNAs represent underexplored targets of genomic aberrations and emerging therapeutic targets. The 3q26.2 amplicon is among the most frequent genomic aberrations in multiple cancer lineages including ovarian and breast cancers. We demonstrate that hsa-miR-569 (hereafter designated as miR569), which is overexpressed in a subset of ovarian and breast cancers, at least in part due to the 3q26.2 amplicon, alters cell survival and proliferation. Downregulation of TP53INP1 expression by miR569 is required for the effects of miR569 on survival and proliferation. Targeting miR569 sensitizes ovarian and breast cancer cells overexpressing miR569 to cisplatin by increasing cell death both invitro and invivo. Thus targeting miR569 could potentially benefit patients with the 3q26.2 amplicon and subsequent miR569 elevation.

AB - Small noncoding miRNAs represent underexplored targets of genomic aberrations and emerging therapeutic targets. The 3q26.2 amplicon is among the most frequent genomic aberrations in multiple cancer lineages including ovarian and breast cancers. We demonstrate that hsa-miR-569 (hereafter designated as miR569), which is overexpressed in a subset of ovarian and breast cancers, at least in part due to the 3q26.2 amplicon, alters cell survival and proliferation. Downregulation of TP53INP1 expression by miR569 is required for the effects of miR569 on survival and proliferation. Targeting miR569 sensitizes ovarian and breast cancer cells overexpressing miR569 to cisplatin by increasing cell death both invitro and invivo. Thus targeting miR569 could potentially benefit patients with the 3q26.2 amplicon and subsequent miR569 elevation.

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Copy Number Gain of hsa-miR-569 at 3q26.2 Leads to Loss of TP53INP1 and Aggressiveness of Epithelial Cancers

Abstract

Funding

ASJC Scopus subject areas

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