Germline-specific RNA helicase DDX4 forms cytoplasmic granules in cancer cells and promotes tumor growth
Cancer cells undergo major epigenetic alterations and transcriptomic changes, including ectopic expression of tissue- and cell-type-specific genes. Here, we show that the germline-specific RNA helicase DDX4 forms germ-granule-like cytoplasmic ribonucleoprotein granules in various human tumors, but n...
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| Published in: | Cell reports (Cambridge) Vol. 43; no. 7; p. 114430 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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23-07-2024
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| Abstract | Cancer cells undergo major epigenetic alterations and transcriptomic changes, including ectopic expression of tissue- and cell-type-specific genes. Here, we show that the germline-specific RNA helicase DDX4 forms germ-granule-like cytoplasmic ribonucleoprotein granules in various human tumors, but not in cultured cancer cells. These cancerous DDX4 complexes contain RNA-binding proteins and splicing regulators, including many known germ granule components. The deletion of DDX4 in cancer cells induces transcriptomic changes and affects the alternative splicing landscape of a number of genes involved in cancer growth and invasiveness, leading to compromised capability of DDX4-null cancer cells to form xenograft tumors in immunocompromised mice. Importantly, the occurrence of DDX4 granules is associated with poor survival in patients with head and neck squamous cell carcinoma and higher histological grade of prostate cancer. Taken together, these results show that the germ-granule-resembling cancerous DDX4 granules control gene expression and promote malignant and invasive properties of cancer cells.
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•Germ-granule-resembling DDX4 granules appear in different somatic malignancies•Deletion of DDX4 in cancer cells compromises tumor growth•DDX4 deletion affects the expression of genes associated with cancer invasiveness•DDX4 expression is associated with poor survival of cancer patients
Olotu et al. reveal the presence of cytoplasmic granules containing the germline-specific RNA helicase DDX4 in various human cancers. Using cultured cancer cells and a mouse xenograft model, they show that DDX4 is involved in the transcriptome regulation in cancer cells, and it promotes cancerous properties and tumor growth. |
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| AbstractList | Cancer cells undergo major epigenetic alterations and transcriptomic changes, including ectopic expression of tissue- and cell-type-specific genes. Here, we show that the germline-specific RNA helicase DDX4 forms germ-granule-like cytoplasmic ribonucleoprotein granules in various human tumors, but not in cultured cancer cells. These cancerous DDX4 complexes contain RNA-binding proteins and splicing regulators, including many known germ granule components. The deletion of DDX4 in cancer cells induces transcriptomic changes and affects the alternative splicing landscape of a number of genes involved in cancer growth and invasiveness, leading to compromised capability of DDX4-null cancer cells to form xenograft tumors in immunocompromised mice. Importantly, the occurrence of DDX4 granules is associated with poor survival in patients with head and neck squamous cell carcinoma and higher histological grade of prostate cancer. Taken together, these results show that the germ-granule-resembling cancerous DDX4 granules control gene expression and promote malignant and invasive properties of cancer cells. Cancer cells undergo major epigenetic alterations and transcriptomic changes, including ectopic expression of tissue- and cell-type-specific genes. Here, we show that the germline-specific RNA helicase DDX4 forms germ-granule-like cytoplasmic ribonucleoprotein granules in various human tumors, but not in cultured cancer cells. These cancerous DDX4 complexes contain RNA-binding proteins and splicing regulators, including many known germ granule components. The deletion of DDX4 in cancer cells induces transcriptomic changes and affects the alternative splicing landscape of a number of genes involved in cancer growth and invasiveness, leading to compromised capability of DDX4-null cancer cells to form xenograft tumors in immunocompromised mice. Importantly, the occurrence of DDX4 granules is associated with poor survival in patients with head and neck squamous cell carcinoma and higher histological grade of prostate cancer. Taken together, these results show that the germ-granule-resembling cancerous DDX4 granules control gene expression and promote malignant and invasive properties of cancer cells.Cancer cells undergo major epigenetic alterations and transcriptomic changes, including ectopic expression of tissue- and cell-type-specific genes. Here, we show that the germline-specific RNA helicase DDX4 forms germ-granule-like cytoplasmic ribonucleoprotein granules in various human tumors, but not in cultured cancer cells. These cancerous DDX4 complexes contain RNA-binding proteins and splicing regulators, including many known germ granule components. The deletion of DDX4 in cancer cells induces transcriptomic changes and affects the alternative splicing landscape of a number of genes involved in cancer growth and invasiveness, leading to compromised capability of DDX4-null cancer cells to form xenograft tumors in immunocompromised mice. Importantly, the occurrence of DDX4 granules is associated with poor survival in patients with head and neck squamous cell carcinoma and higher histological grade of prostate cancer. Taken together, these results show that the germ-granule-resembling cancerous DDX4 granules control gene expression and promote malignant and invasive properties of cancer cells. Cancer cells undergo major epigenetic alterations and transcriptomic changes, including ectopic expression of tissue- and cell-type-specific genes. Here, we show that the germline-specific RNA helicase DDX4 forms germ-granule-like cytoplasmic ribonucleoprotein granules in various human tumors, but not in cultured cancer cells. These cancerous DDX4 complexes contain RNA-binding proteins and splicing regulators, including many known germ granule components. The deletion of DDX4 in cancer cells induces transcriptomic changes and affects the alternative splicing landscape of a number of genes involved in cancer growth and invasiveness, leading to compromised capability of DDX4-null cancer cells to form xenograft tumors in immunocompromised mice. Importantly, the occurrence of DDX4 granules is associated with poor survival in patients with head and neck squamous cell carcinoma and higher histological grade of prostate cancer. Taken together, these results show that the germ-granule-resembling cancerous DDX4 granules control gene expression and promote malignant and invasive properties of cancer cells. [Display omitted] •Germ-granule-resembling DDX4 granules appear in different somatic malignancies•Deletion of DDX4 in cancer cells compromises tumor growth•DDX4 deletion affects the expression of genes associated with cancer invasiveness•DDX4 expression is associated with poor survival of cancer patients Olotu et al. reveal the presence of cytoplasmic granules containing the germline-specific RNA helicase DDX4 in various human cancers. Using cultured cancer cells and a mouse xenograft model, they show that DDX4 is involved in the transcriptome regulation in cancer cells, and it promotes cancerous properties and tumor growth. |
| ArticleNumber | 114430 |
| Author | Poutanen, Matti Lehtiniemi, Tiina Visakorpi, Tapio Bourgery, Matthieu Ma, Lin Mäkelä, Juho-Antti Vainio, Paula Laasanen, Sini Louramo, Elina Olotu, Opeyemi Sahlgren, Cecilia Koskenniemi, Anna-Riina Kotaja, Noora Laasanen, Samuli Westermarck, Jukka Ventelä, Sami Rivero-Müller, Adolfo Löyttyniemi, Eliisa Paramonov, Valeriy |
| Author_xml | – sequence: 1 givenname: Opeyemi surname: Olotu fullname: Olotu, Opeyemi organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 2 givenname: Anna-Riina surname: Koskenniemi fullname: Koskenniemi, Anna-Riina organization: Department of Pathology, Laboratory Division, Turku University Hospital and University of Turku, 20520 Turku, Finland – sequence: 3 givenname: Lin surname: Ma fullname: Ma, Lin organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 4 givenname: Valeriy surname: Paramonov fullname: Paramonov, Valeriy organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 5 givenname: Sini surname: Laasanen fullname: Laasanen, Sini organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 6 givenname: Elina surname: Louramo fullname: Louramo, Elina organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 7 givenname: Matthieu surname: Bourgery fullname: Bourgery, Matthieu organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 8 givenname: Tiina surname: Lehtiniemi fullname: Lehtiniemi, Tiina organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 9 givenname: Samuli surname: Laasanen fullname: Laasanen, Samuli organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 10 givenname: Adolfo surname: Rivero-Müller fullname: Rivero-Müller, Adolfo organization: Department of Biochemistry and Molecular Biology, Medical University of Lublin, 20-093 Lublin, Poland – sequence: 11 givenname: Eliisa surname: Löyttyniemi fullname: Löyttyniemi, Eliisa organization: Department of Biostatistics, University of Turku and Turku University Hospital, 20520 Turku, Finland – sequence: 12 givenname: Cecilia surname: Sahlgren fullname: Sahlgren, Cecilia organization: Faculty of Science and Engineering, Cell Biology, Åbo Akademi University, 20500 Turku, Finland – sequence: 13 givenname: Jukka surname: Westermarck fullname: Westermarck, Jukka organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 14 givenname: Sami surname: Ventelä fullname: Ventelä, Sami organization: Turku Bioscience, University of Turku and Åbo Akademi University, 20520 Turku, Finland – sequence: 15 givenname: Tapio surname: Visakorpi fullname: Visakorpi, Tapio organization: Faculty of Medicine and Health Technology, Tampere University and Tays Cancer Center, Tampere University Hospital, 33520 Tampere, Finland – sequence: 16 givenname: Matti surname: Poutanen fullname: Poutanen, Matti organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 17 givenname: Paula surname: Vainio fullname: Vainio, Paula organization: Department of Pathology, Laboratory Division, Turku University Hospital and University of Turku, 20520 Turku, Finland – sequence: 18 givenname: Juho-Antti surname: Mäkelä fullname: Mäkelä, Juho-Antti organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland – sequence: 19 givenname: Noora orcidid: 0000-0003-1503-9170 surname: Kotaja fullname: Kotaja, Noora email: noora.kotaja@utu.fi organization: Institute of Biomedicine, Integrative Physiology and Pharmacology Unit, University of Turku, 20520 Turku, Finland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38963760$$D View this record in MEDLINE/PubMed |
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| Keywords | RNA regulation DDX4 CP: Cancer RNP granules CP: Molecular biology tumor growth cancer-germline antigens cancer |
| Language | English |
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