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Research Article

Long Noncoding RNA JHDM1D-AS1 Promotes Tumor Growth by Regulating Angiogenesis in Response to Nutrient Starvation

Ayano Kondo, Aya Nonaka, Teppei Shimamura, Shogo Yamamoto, Tetsuo Yoshida, Tatsuhiko Kodama, Hiroyuki Aburatani, Tsuyoshi Osawa
Ayano Kondo
aDivision of Genome Science, RCAST, The University of Tokyo, Tokyo, Japan
bInnovative Technology Laboratories, Kyowa Hakko Kirin Co., Ltd., Tokyo, Japan
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Aya Nonaka
aDivision of Genome Science, RCAST, The University of Tokyo, Tokyo, Japan
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Teppei Shimamura
cDepartment of Systems Biology, Graduate School of Medicine, Nagoya University, Nagoya, Japan
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Shogo Yamamoto
aDivision of Genome Science, RCAST, The University of Tokyo, Tokyo, Japan
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Tetsuo Yoshida
dTranslational Research Unit, Kyowa Hakko Kirin Co., Ltd., Shizuoka, Japan
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Tatsuhiko Kodama
eLaboratory for Systems Biology and Medicine, RCAST, The University of Tokyo, Tokyo, Japan
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Hiroyuki Aburatani
aDivision of Genome Science, RCAST, The University of Tokyo, Tokyo, Japan
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Tsuyoshi Osawa
eLaboratory for Systems Biology and Medicine, RCAST, The University of Tokyo, Tokyo, Japan
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DOI: 10.1128/MCB.00125-17
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ABSTRACT

Long noncoding RNAs play a pivotal role in tumor progression, but their role in cancer cells in the nutrient-starved tumor microenvironment remains unknown. Here, we show that a nutrient starvation-responsive long noncoding RNA, JHDM1D antisense 1 (JHDM1D-AS1), promotes tumorigenesis by regulating angiogenesis in response to nutrient starvation. Expression of JHDM1D-AS1 was increased in cancer cells. In addition, expression of JHDM1D-AS1 was increased in clinical tumor samples compared to that in normal tissue. Stable expression of JHDM1D-AS1 in human pancreatic cancer (PANC-1 and AsPC-1) cells promoted cell growth in vitro. Remarkably, these JHDM1D-AS1-expressing cells showed a significant increase in tumor growth in vivo that was associated with increased formation of CD31+ blood vessels and elevated infiltration of CD11b+ macrophage lineage cells into tumor tissues. Genome-wide analysis of tumor xenografts revealed that expression of genes for tumor-derived angiogenic factors such as hHGF and hFGF1 concomitant with host-derived inflammation-responsive genes such as mMmp3, mMmp9, mS100a8, and mS100a9 was increased in tumor xenografts of JHDM1D-AS1-expressing pancreatic cancer cells, leading to a poor prognosis. Our results provide evidence that increased JHDM1D-AS1 expression under nutrient starvation accelerates tumor growth by upregulating angiogenesis, thus laying the foundation for improved therapeutic strategies.

FOOTNOTES

    • Received 21 March 2017.
    • Returned for modification 10 April 2017.
    • Accepted 16 June 2017.
    • Accepted manuscript posted online 26 June 2017.
  • Supplemental material for this article may be found at https://doi.org/10.1128/MCB.00125-17 .

  • Copyright © 2017 Kondo et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license .

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Long Noncoding RNA JHDM1D-AS1 Promotes Tumor Growth by Regulating Angiogenesis in Response to Nutrient Starvation
Ayano Kondo, Aya Nonaka, Teppei Shimamura, Shogo Yamamoto, Tetsuo Yoshida, Tatsuhiko Kodama, Hiroyuki Aburatani, Tsuyoshi Osawa
Molecular and Cellular Biology Aug 2017, 37 (18) e00125-17; DOI: 10.1128/MCB.00125-17

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Long Noncoding RNA JHDM1D-AS1 Promotes Tumor Growth by Regulating Angiogenesis in Response to Nutrient Starvation
Ayano Kondo, Aya Nonaka, Teppei Shimamura, Shogo Yamamoto, Tetsuo Yoshida, Tatsuhiko Kodama, Hiroyuki Aburatani, Tsuyoshi Osawa
Molecular and Cellular Biology Aug 2017, 37 (18) e00125-17; DOI: 10.1128/MCB.00125-17
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KEYWORDS

Carcinogenesis
Gene Expression Regulation, Neoplastic
Neoplasms
Neovascularization, Pathologic
Starvation
angiogenesis
cancer
epigenetics
long noncoding RNA
nutrient starvation
tumor microenvironment

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