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Full Text (PDF) Published OnlineFirst February 12, 2018; DOI: 10.1158/0008-5472.CAN-17-1861 Cancer Tumor Biology and Immunology Research A Distinct Oncogenerative Multinucleated Cancer Cell Serves as a Source of Stemness and Tumor Heterogeneity David Díaz-Carballo1, Sahitya Saka1, Jacqueline Klein1, Tobias Rennkamp1, Ali H. Acikelli1, Sascha Malak1, Holger Jastrow2, Gunther Wennemuth2, Clemens Tempfer3, Inge Schmitz4, Andrea Tannapfel4, and Dirk Strumberg1 Abstract The effects of anticancer treatments on cell heterogeneity and new mechanism used by tumor cells to invade surrounding tissues their proliferative potential play an important role in tumor and ensure life cycles. In contrast to the pregnant P1 cells with low persistence and metastasis. However, little is known about de- expression of stem cell markers despite their physiologic stem- polyploidization, cell fate, and physiologic stemness of the result- ness, the first offspring generations of daughter G1 cells expressed ing cell populations. Here, we describe a distinctive cell type high levels of ovarian cancer stem cell markers. Furthermore, termed "pregnant" P1 cells found within chemotherapy-refracto- both P1 and Gn cells overexpressed multiple human endogenous ry ovarian tumors, which generate and gestate daughter genera- retroviral envelope proteins. Moreover, programmed death- tion Gn cells intracytoplasmically. Release of Gn cells occurred by ligand 1 and the immunosuppressive domain of the retroviral ejection through crevices in the P1 cell membrane by body envelope proteins were also overexpressed in P1 cells, suggesting contractions or using a funiculus-like structure. These events effective protection against the host immune system. Together, characterized a not yet described mechanism of cell segregation. our data suggest that P1 oncogenerative cancer cells exhibit a not Maternal P1 cells were principally capable of surviving parturition yet described cell biological mechanism of persistence and trans- events and continued to breed and nurture Gn progenies. In mission of malignant cells in patients with advanced cancers. addition, P1 cells were competent to horizontally transmit off- Significance: P1 oncogenerative cell entities express low levels spring Gn cells into other specific proximal cells, injecting them to of CSC markers, which are characteristic of their histological receptor R1 cells via cell–cell tunneling. This process represents a origin. Cancer Res; 78(9); 2318–31. Ó2018 AACR. Introduction tion into pluripotent stem cells (iPSC) can be induced via Yama- naka's quadriga of transcription factors (2, 3). Embryonic stem cells (ESC) derive from the undifferentiated The source of tumor cell heterogeneity is still under debate inner mass of blastocysts. As pluripotent cells, they can differen- because the "cell of origin" has remained elusive. However, tiate into all derivatives of the three primary germ layers (1). Adult multiple conclusive lines of evidence suggest the existence of stem cells (ASC) are undifferentiated multipotent cells with the cancer stem cells (CSC) with characteristics that are normally capacity of self-renewal and generation of fully differentiated associated with ASCs, including the capacity for long-term self- daughter cells. They are virtually tissue resident, help maintain renewal and multipotency, which contributes to tumor cell het- cellular homeostasis, and express high levels of ABC transporters. erogeneity, a hallmark of stem cells (4, 5). Despite their localized ASCs are capable of cell transdifferentiation, that is, generating origin, CSCs can disseminate to distant sites. Another ASC-like differentiated cell types of other histologies. ASC transdifferentia- characteristic is the overexpression of ABC transporters and DNA repair mechanisms, which play a critical role in untreatable malig- nancies. Moreover, under therapeutic treatment conditions, differ- 1 Institute of Molecular Oncology and Experimental Therapeutics. Division of entiated cancer cells may change their phenotype and alter their Haematology and Oncology, Marienhospital Herne, Ruhr University Bochum, – Medical School, Herne, Germany. 2Institute of Anatomy, University of Duisburg- biology toward a more stem-like state to ensure survival (4 6). Essen, Medical School, Essen, Germany. 3Gynaecology and Obstetrics, Marien- A common phenomenon associated with cytostatic- and irra- hospital Herne, Ruhr University Bochum, Medical School, Herne, Germany. diation-induced cell heterogeneity is believed to be the emergence 4Institute of Pathology, Ruhr University Bochum, Medical School, Bochum, of multinucleated giant cell entities with CSC properties (7, 8). Germany. These cells can be generated via two different mechanisms: Note: Supplementary data for this article are available at Cancer Research (i) endoreplication coupled with karyokinesis - endomitosis Online (http://cancerres.aacrjournals.org/). (plasmodium formation); and (ii) syncytin-mediated cell–cell Corresponding Author: David Díaz-Carballo, Institute of Molecular Oncology fusion (syncytium formation). Endoreplication can be seen as a and Experimental Therapeutics, Marienhospital Herne, Ruhr University Bochum, deviant form of the normal mitotic cell cycle in which mitosis is Medical School, Dungelstr.€ 33, Herne 44623, Germany. Phone: 4923-2349- completely suppressed. Endomitosis is an abortive from of 91092; Fax: 4923-2349-91049; E-mail: mitosis that does not result in cell division but leads to [email protected] the formation of multinucleated giant cells (9, 10). Another doi: 10.1158/0008-5472.CAN-17-1861 multinucleated cell type arises from specificcell–cell fusion Ó2018 American Association for Cancer Research. events that are chieflymediatedbythefusogenicpropertiesof 2318 Cancer Res; 78(9) May 1, 2018 Downloaded from cancerres.aacrjournals.org on September 23, 2021. © 2018 American Association for Cancer Research. Published OnlineFirst February 12, 2018; DOI: 10.1158/0008-5472.CAN-17-1861 The Stemness Status of Oncogenerative P1 Cells envelope proteins from exogenous or endogenous retroviruses TransferMan 4r micromanipulator (Eppendorf) and washed in (HERV), that is, HERV-WE1 and HERV-FRD1.Cell–cell fusion 25 mL DMEM. Next, the cells were placed in approximately 25 mL via syncytins may generate both normal (syncytium tropho- on a dish lid, inverted onto the PBS-filled bottom chamber, and blasts during placental development) and pathologic forms, as cultured in 5% CO2, 95% humidity, 37 C until morula-like observed, for example, in high-grade Reed–Sternberg cells, spheres had formed. chemoresistant tumors or after viral infection, for example, with the syncytial respiratory virus (11, 12). Studies on the migration capacity of P1 and G1-Gn cells by Although the two mechanisms differ vastly at the physiologic Transwell migration assay fi level, the nal fate of many giant cells is the reverted multi- A Transwell migration assay was used to track and quantify the nucleation, which leads to the generation of daughter cells, thus migration of P1 and offspring cells. Tissue culture inserts with a promoting tumor initiation and development (8, 13). The translucent 8 mm PET-membrane (Sarstedt) precoated with col- theory of cellularization states that in multinucleated cells, the lagen types I/IV (Thermo Fisher Scientific) were used. A total of nuclei may have developed internal perinuclear membrane 2 Â 104 ovarian carcinoma cells from ascites were deposited on partitions facilitating the formation of new cells. This process the Transwell upper chamber, and DMEM containing 20% FBS has been described in Drosophila melanogaster embryos (14). was added as a chemoattractant to the lower chamber. After 24 However, to the best of our knowledge, the molecular mech- hours, cells were fixed with TCA 10% at 4C for one hour and anism behind this process has not been studied in detail in stained with SRB 0.4% in 1% acetic acid for one hour. Depending cancer cells. on the side of the membrane analyzed, the stained cells on the Here, we document a distinctive cell type termed "pregnant" P1 other side were removed mechanically. Migration was documen- cells found within chemotherapy-refractory ovarian tumors that ted using an inverted Nikon Eclipse TS100 microscope or generate daughter G1 cells intracytoplasmically by cellularization, quantified by immersing the membranes in Tris-HCl pH 10.5, which, upon gestation, are released into the immediate surround- measuring the dissolved proteins at 570 nm in a Tecan Infinite fi ings. Strikingly, P1 cells can inject G1 cells into speci c recipient M200 microtiter plate reader. Different P1/G1-Gn cell surface cells (R1) via cell–cell tunneling, which represents a horizontal structures like CXCR4, HERV-Fc1, HERV-KISD, and EpCAM were transmission of the entire genome between cells, resulting in new targeted using specific antibodies at 10 mg/mL for 24 hours to tetraploid cell entities. study their role in cell migration. P1 appears to be a distinctive tumor cell type with intriguing stem cell biology. Phenotypic characterization shows that P1 Differential expression of stem cell markers and immune express very low levels of CSC markers in spite of their stem cell checkpoints in P1 progenies as analyzed by qPCR biology (15). Interestingly, this is contrasted by the first genera- fi tion of progeny cells, which express a distinct signature of canon- Total RNA puri cation and cDNA synthesis. P1 progenies were ical CSC markers. Contrarily, P1 cells differentially produce more grown
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