Telomeric G-quadruplex-forming DNA fragments induce TLR9-mediated and LL-37-regulated invasion in breast cancer cells in vitro
Toll-like receptor 9 (TLR9) is a cellular DNA-receptor widely expressed in cancers. We previously showed that synthetic and self-derived DNA fragments induce TLR9-mediated breast cancer cell invasion in vitro. We investigated here the invasive effects of two nuclease-resistant DNA fragments, a 9-mer...
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Published in | Breast cancer research and treatment Vol. 155; no. 2; pp. 261 - 271 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
New York
Springer US
01.01.2016
Springer Springer Nature B.V |
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Abstract | Toll-like receptor 9 (TLR9) is a cellular DNA-receptor widely expressed in cancers. We previously showed that synthetic and self-derived DNA fragments induce TLR9-mediated breast cancer cell invasion in vitro. We investigated here the invasive effects of two nuclease-resistant DNA fragments, a 9-mer hairpin, and a G-quadruplex DNA based on the human telomere sequence, both having native phosphodiester backbone. Cellular uptake of DNAs was investigated with immunofluorescence, invasion was studied with Matrigel-assays, and mRNA and protein expression were studied with qPCR and Western blotting and protease activity with zymograms. TLR9 expression was suppressed through siRNA. Although both DNAs induced TLR9-mediated changes in pro-invasive mRNA expression, only the telomeric G-quadruplex DNA significantly increased cellular invasion. This was inhibited with GM6001 and aprotinin, suggesting MMP- and serine protease mediation. Furthermore, complexing with LL-37, a cathelicidin-peptide present in breast cancers, increased 9-mer hairpin and G-quadruplex DNA uptake into the cancer cells. However, DNA/LL-37 complexes decreased invasion, as compared with DNA-treatment alone. Invasion studies were conducted also with DNA fragments isolated from neoadjuvant chemotherapy-treated breast tumors. Also such DNA induced breast cancer cell invasion in vitro. As with the synthetic DNAs, this invasive effect was reduced by complexing the neoadjuvant tumor-derived DNAs with LL-37. We conclude that 9-mer hairpin and G-quadruplex DNA fragments are nuclease-resistant DNA structures that can act as invasion-inducing TLR9 ligands. Their cellular uptake and the invasive effects are regulated via LL-37. Although such structures may be present in chemotherapy-treated tumors, the clinical significance of this finding requires further studying. |
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AbstractList | Toll-like receptor 9 (TLR9) is a cellular DNA-receptor widely expressed in cancers. We previously showed that synthetic and self-derived DNA fragments induce TLR9-mediated breast cancer cell invasion in vitro. We investigated here the invasive effects of two nuclease-resistant DNA fragments, a 9-mer hairpin, and a G-quadruplex DNA based on the human telomere sequence, both having native phosphodiester backbone. Cellular uptake of DNAs was investigated with immunofluorescence, invasion was studied with Matrigel-assays, and mRNA and protein expression were studied with qPCR and Western blotting and protease activity with zymograms. TLR9 expression was suppressed through siRNA. Although both DNAs induced TLR9-mediated changes in pro-invasive mRNA expression, only the telomeric G-quadruplex DNA significantly increased cellular invasion. This was inhibited with GM6001 and aprotinin, suggesting MMP- and serine protease mediation. Furthermore, complexing with LL-37, a cathelicidin-peptide present in breast cancers, increased 9-mer hairpin and G-quadruplex DNA uptake into the cancer cells. However, DNA/LL-37 complexes decreased invasion, as compared with DNA-treatment alone. Invasion studies were conducted also with DNA fragments isolated from neoadjuvant chemotherapy-treated breast tumors. Also such DNA induced breast cancer cell invasion in vitro. As with the synthetic DNAs, this invasive effect was reduced by complexing the neoadjuvant tumor-derived DNAs with LL-37. We conclude that 9-mer hairpin and G-quadruplex DNA fragments are nuclease-resistant DNA structures that can act as invasion-inducing TLR9 ligands. Their cellular uptake and the invasive effects are regulated via LL-37. Although such structures may be present in chemotherapy-treated tumors, the clinical significance of this finding requires further studying. |
Audience | Academic |
Author | Kauppila, Joonas H. Jukkola-Vuorinen, Arja Graves, David E. Sandholm, Jouko A. Lehenkari, Petri P. Selander, Katri S. Tuomela, Johanna M. Kaakinen, Mika Hayden, Katherine L. Haapasaari, Kirsi-Maria Harris, Kevin W. |
Author_xml | – sequence: 1 givenname: Johanna M. surname: Tuomela fullname: Tuomela, Johanna M. organization: Division of Hematology-Oncology, Department of Medicine, University of Alabama at Birmingham, Comprehensive Cancer Center, University of Alabama at Birmingham, Department of Cell Biology and Anatomy, Institute of Biomedicine, University of Turku – sequence: 2 givenname: Jouko A. surname: Sandholm fullname: Sandholm, Jouko A. organization: Division of Hematology-Oncology, Department of Medicine, University of Alabama at Birmingham, Comprehensive Cancer Center, University of Alabama at Birmingham, Turku Centre for Biotechnology, University of Turku and Åbo Akademi University – sequence: 3 givenname: Mika surname: Kaakinen fullname: Kaakinen, Mika organization: Department of Anatomy and Cell Biology, University of Oulu, Oulu Center for Cell–Matrix Research, Faculty of Biochemistry and Molecular Medicine, Biocenter Oulu, University of Oulu – sequence: 4 givenname: Katherine L. surname: Hayden fullname: Hayden, Katherine L. organization: Department of Chemistry, University of Alabama at Birmingham – sequence: 5 givenname: Kirsi-Maria surname: Haapasaari fullname: Haapasaari, Kirsi-Maria organization: Department of Pathology, University of Oulu – sequence: 6 givenname: Arja surname: Jukkola-Vuorinen fullname: Jukkola-Vuorinen, Arja organization: Department of Oncology, University Hospital of Oulu – sequence: 7 givenname: Joonas H. surname: Kauppila fullname: Kauppila, Joonas H. organization: Department of Anatomy and Cell Biology, University of Oulu, Department of Pathology, University of Oulu, Department of Surgery, Oulu University Hospital – sequence: 8 givenname: Petri P. surname: Lehenkari fullname: Lehenkari, Petri P. organization: Department of Anatomy and Cell Biology, University of Oulu, Department of Pathology, University of Oulu, Department of Surgery, Oulu University Hospital – sequence: 9 givenname: Kevin W. surname: Harris fullname: Harris, Kevin W. organization: Division of Hematology-Oncology, Department of Medicine, University of Alabama at Birmingham, Comprehensive Cancer Center, University of Alabama at Birmingham, Birmingham Veterans Affairs Medical Center, Birmingham – sequence: 10 givenname: David E. surname: Graves fullname: Graves, David E. organization: Comprehensive Cancer Center, University of Alabama at Birmingham, Department of Chemistry, University of Alabama at Birmingham – sequence: 11 givenname: Katri S. surname: Selander fullname: Selander, Katri S. email: Katriselander@uabmc.edu organization: Division of Hematology-Oncology, Department of Medicine, University of Alabama at Birmingham, Comprehensive Cancer Center, University of Alabama at Birmingham, Department of Pathology, Lapland Central Hospital, Department of Chemistry, UAB |
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Keywords | 9-mer hairpin DNA LL-37 Toll-like receptor 9 Invasion Telomeric G-quadruplex DNA |
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70 G Schreiber (3683_CR26) 1985; 13 CY Chiang (3683_CR46) 2012; 11 JM Ilvesaro (3683_CR24) 2008; 6 H Fernando (3683_CR34) 2009; 37 N Chaudary (3683_CR39) 2006; 26 S Sandgren (3683_CR29) 2004; 279 R Ramirez (3683_CR47) 2003; 278 B Schmausser (3683_CR8) 2004; 136 JH Kauppila (3683_CR41) 2014; 5 H Ronkainen (3683_CR10) 2011; 30 Z Cao (3683_CR31) 2006; 78 JL Huppert (3683_CR35) 2007; 35 M Mempel (3683_CR44) 2003; 121 A Jukkola-Vuorinen (3683_CR19) 2009; 1 R Kulkarni (3683_CR11) 2011; 343 A Hidmark (3683_CR4) 2012 S Akira (3683_CR1) 2003; 85 SB Coffelt (3683_CR37) 2009; 7 A Trieu (3683_CR52) 2006; 26 J Korvala (3683_CR18) 2014; 43 A Marshak-Rothstein (3683_CR40) 2007; 25 G Weber (3683_CR51) 2009; 11 JM Silva (3683_CR48) 1999; 59 3683_CR49 J Eddy (3683_CR36) 2008; 36 AM Krieg (3683_CR43) 2012; 22 JH Kauppila (3683_CR16) 2011; 59 B Schmausser (3683_CR13) 2005; 295 MA Merrell (3683_CR15) 2006; 4 S Yoshizawa (3683_CR30) 1994; 22 D Droemann (3683_CR14) 2005; 6 JD Heilborn (3683_CR50) 2005; 114 J Tuomela (3683_CR21) 2012; 135 |
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publication-title: J Invest Dermatol doi: 10.1111/j.1523-1747.2003.12630.x contributor: fullname: M Mempel – volume: 13 start-page: 7663 issue: 21 year: 1985 ident: 3683_CR26 publication-title: Nucleic Acids Res doi: 10.1093/nar/13.21.7663 contributor: fullname: G Schreiber – volume: 122 start-page: 1030 issue: 5 year: 2008 ident: 3683_CR38 publication-title: Int J Cancer doi: 10.1002/ijc.23186 contributor: fullname: SB Coffelt |
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Snippet | Toll-like receptor 9 (TLR9) is a cellular DNA-receptor widely expressed in cancers. We previously showed that synthetic and self-derived DNA fragments induce... |
SourceID | proquest gale crossref pubmed springer |
SourceType | Aggregation Database Index Database Publisher |
StartPage | 261 |
SubjectTerms | Antimicrobial Cationic Peptides - genetics Breast cancer Breast Neoplasms - genetics Breast Neoplasms - pathology Cancer cells Cancer genetics Cancer research Cancer therapies Cell adhesion & migration Cell Line, Tumor Chemotherapy Deoxyribonucleic acid DNA DNA Fragmentation DNA, Neoplasm - genetics Female G-Quadruplexes Genetic research Humans Ligands Medicine Medicine & Public Health Neoplasm Invasiveness - genetics Neoplasm Invasiveness - pathology Oncology Preclinical Study Proteases Protein expression RNA RNA, Messenger - genetics Telomere - genetics Toll-Like Receptor 9 - genetics |
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Title | Telomeric G-quadruplex-forming DNA fragments induce TLR9-mediated and LL-37-regulated invasion in breast cancer cells in vitro |
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