Identification and characterization of stromal-like cells with CD207
Cell lines
Cellular model
Histiocytoses
In vitro study
Langerhans cell histiocytosis
Rare disorders
Journal
BMC cancer
ISSN: 1471-2407
Titre abrégé: BMC Cancer
Pays: England
ID NLM: 100967800
Informations de publication
Date de publication:
12 Feb 2024
12 Feb 2024
Historique:
received:
08
05
2023
accepted:
28
12
2023
medline:
12
2
2024
pubmed:
12
2
2024
entrez:
11
2
2024
Statut:
epublish
Résumé
Histiocytoses are rare disorders manifested by increased proliferation of pathogenic myeloid cells sharing histological features with macrophages or dendritic cells and accumulating in various organs, i.a., bone and skin. Pre-clinical in vitro models that could be used to determine molecular pathways of the disease are limited, hence research on histiocytoses is challenging. The current study compares cytophysiological features of progenitor, stromal-like cells derived from histiocytic lesions (sl-pHCs) of three pediatric patients with different histiocytoses types and outcomes. The characterized cells may find potential applications in drug testing. Molecular phenotype of the cells, i.e. expression of CD1a and CD207 (langerin), was determined using flow cytometry. Cytogenetic analysis included GTG-banded metaphases and microarray (aCGH) evaluation. Furthermore, the morphology and ultrastructure of cells were evaluated using a confocal and scanning electron microscope. The microphotographs from the confocal imaging were used to reconstruct the mitochondrial network and its morphology. Basic cytophysiological parameters, such as viability, mitochondrial activity, and proliferation, were analyzed using multiple cellular assays, including Annexin V/7-AAD staining, mitopotential analysis, BrdU test, clonogenicity analysis, and distribution of cells within the cell cycle. Biomarkers potentially associated with histiocytoses progression were determined using RT-qPCR at mRNA, miRNA and lncRNA levels. Intracellular accumulation of histiocytosis-specific proteins was detected with Western blot. Cytotoxicyty and IC50 of vemurafenib and trametinib were determined with MTS assay. Obtained cellular models, i.e. RAB-1, HAN-1, and CHR-1, are heterogenic in terms of molecular phenotype and morphology. The cells express CD1a/CD207 markers characteristic for dendritic cells, but also show intracellular accumulation of markers characteristic for cells of mesenchymal origin, i.e. vimentin (VIM) and osteopontin (OPN). In subsequent cultures, cells remain viable and metabolically active, and the mitochondrial network is well developed, with some distinctive morphotypes noted in each cell line. Cell-specific transcriptome profile was noted, providing information on potential new biomarkers (non-coding RNAs) with diagnostic and prognostic features. The cells showed different sensitivity to vemurafenib and trametinib. Obtained and characterized cellular models of stromal-like cells derived from histiocytic lesions can be used for studies on histiocytosis biology and drug testing.
Sections du résumé
BACKGROUND
BACKGROUND
Histiocytoses are rare disorders manifested by increased proliferation of pathogenic myeloid cells sharing histological features with macrophages or dendritic cells and accumulating in various organs, i.a., bone and skin. Pre-clinical in vitro models that could be used to determine molecular pathways of the disease are limited, hence research on histiocytoses is challenging. The current study compares cytophysiological features of progenitor, stromal-like cells derived from histiocytic lesions (sl-pHCs) of three pediatric patients with different histiocytoses types and outcomes. The characterized cells may find potential applications in drug testing.
METHODS
METHODS
Molecular phenotype of the cells, i.e. expression of CD1a and CD207 (langerin), was determined using flow cytometry. Cytogenetic analysis included GTG-banded metaphases and microarray (aCGH) evaluation. Furthermore, the morphology and ultrastructure of cells were evaluated using a confocal and scanning electron microscope. The microphotographs from the confocal imaging were used to reconstruct the mitochondrial network and its morphology. Basic cytophysiological parameters, such as viability, mitochondrial activity, and proliferation, were analyzed using multiple cellular assays, including Annexin V/7-AAD staining, mitopotential analysis, BrdU test, clonogenicity analysis, and distribution of cells within the cell cycle. Biomarkers potentially associated with histiocytoses progression were determined using RT-qPCR at mRNA, miRNA and lncRNA levels. Intracellular accumulation of histiocytosis-specific proteins was detected with Western blot. Cytotoxicyty and IC50 of vemurafenib and trametinib were determined with MTS assay.
RESULTS
RESULTS
Obtained cellular models, i.e. RAB-1, HAN-1, and CHR-1, are heterogenic in terms of molecular phenotype and morphology. The cells express CD1a/CD207 markers characteristic for dendritic cells, but also show intracellular accumulation of markers characteristic for cells of mesenchymal origin, i.e. vimentin (VIM) and osteopontin (OPN). In subsequent cultures, cells remain viable and metabolically active, and the mitochondrial network is well developed, with some distinctive morphotypes noted in each cell line. Cell-specific transcriptome profile was noted, providing information on potential new biomarkers (non-coding RNAs) with diagnostic and prognostic features. The cells showed different sensitivity to vemurafenib and trametinib.
CONCLUSION
CONCLUSIONS
Obtained and characterized cellular models of stromal-like cells derived from histiocytic lesions can be used for studies on histiocytosis biology and drug testing.
Identifiants
pubmed: 38342891
doi: 10.1186/s12885-023-11807-0
pii: 10.1186/s12885-023-11807-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
105Subventions
Organisme : Agencja Badań Medycznych
ID : 2019/ABM/01/00016-00
Organisme : Agencja Badań Medycznych
ID : 2019/ABM/01/00016-00
Organisme : Agencja Badań Medycznych
ID : 2019/ABM/01/00016-00
Organisme : Agencja Badań Medycznych
ID : 2019/ABM/01/00016-00
Organisme : Agencja Badań Medycznych
ID : 2019/ABM/01/00016-00
Organisme : Agencja Badań Medycznych
ID : 2019/ABM/01/00016-00
Informations de copyright
© 2024. The Author(s).
Références
Emile J-F, Cohen-Aubart F, Collin M, Fraitag S, Idbaih A, Abdel-Wahab O, Rollins BJ, Donadieu J, Haroche J. Histiocytosis. Lancet. 2021;398:157–70. https://doi.org/10.1016/S0140-6736(21)00311-1 .
pubmed: 33901419
pmcid: 9364113
doi: 10.1016/S0140-6736(21)00311-1
McClain KL, Bigenwald C, Collin M, Haroche J, Marsh RA, Merad M, Picarsic J, Ribeiro KB, Allen CE. Histiocytic disorders. Nat Rev Dis Primers. 2021;7:73. https://doi.org/10.1038/s41572-021-00307-9 .
pubmed: 34620874
pmcid: 10031765
doi: 10.1038/s41572-021-00307-9
Emile J-F, Abla O, Fraitag S, Horne A, Haroche J, Donadieu J, Requena-Caballero L, Jordan MB, Abdel-Wahab O, Allen CE, et al. Revised classification of histiocytoses and neoplasms of the macrophage-dendritic cell lineages. Blood. 2016;127:2672–81. https://doi.org/10.1182/blood-2016-01-690636 .
pubmed: 26966089
pmcid: 5161007
doi: 10.1182/blood-2016-01-690636
Egan C, Jaffe ES. Non-neoplastic histiocytic and dendritic cell disorders in lymph nodes. Semin Diagn Pathol. 2018;35:20–33. https://doi.org/10.1053/j.semdp.2017.11.002 .
pubmed: 29150219
doi: 10.1053/j.semdp.2017.11.002
Huynh KN, Nguyen BD. Histiocytosis and neoplasms of macrophage-dendritic cell lineages: multimodality imaging with emphasis on PET/CT. Radiographics. 2021;41:576–94. https://doi.org/10.1148/rg.2021200096 .
pubmed: 33606566
doi: 10.1148/rg.2021200096
Gogusev J, Telvi L, Murakami I, Lepelletier Y, Nezelof C, Stojkoski A, Glorion C, Jaubert F. DOR-1, A novel CD10+ stromal cell line derived from progressive Langerhans cell histiocytosis of bone. Pediatr Blood Cancer. 2005;44:128–37. https://doi.org/10.1002/pbc.20090 .
pubmed: 15390308
doi: 10.1002/pbc.20090
Murakami I, Gogusev J, Jaubert F, Matsushita M, Hayashi K, Miura I, Tanaka T, Oka T, Yoshino T. Establishment of a Langerhans cell histiocytosis lesion cell line with dermal dendritic cell characteristics. Oncol Rep. 2015;33:171–8. https://doi.org/10.3892/or.2014.3567 .
pubmed: 25351656
doi: 10.3892/or.2014.3567
Smieszek A, Marcinkowska K, Pielok A, Sikora M, Valihrach L, Carnevale E, Marycz K. Obesity affects the proliferative potential of equine endometrial progenitor cells and modulates their molecular phenotype associated with mitochondrial metabolism. Cells. 2022;11:1437. https://doi.org/10.3390/cells11091437 .
pubmed: 35563743
pmcid: 9100746
doi: 10.3390/cells11091437
Sikora M, Marcinkowska K, Marycz K, Wiglusz RJ, Śmieszek A. The potential selective cytotoxicity of poly (L- Lactic Acid)-based scaffolds functionalized with nanohydroxyapatite and europium (III) ions toward osteosarcoma cells. Materials (Basel). 2019;12:3779. https://doi.org/10.3390/ma12223779 .
pubmed: 31752084
doi: 10.3390/ma12223779
Sikora M, Śmieszek A, Marycz K. Bone marrow stromal cells (BMSCs CD45- /CD44+ /CD73+ /CD90+ ) isolated from osteoporotic mice SAM/P6 as a novel model for osteoporosis investigation. J Cell Mol Med. 2021;25:6634–51. https://doi.org/10.1111/jcmm.16667 .
pubmed: 34075722
pmcid: 8278098
doi: 10.1111/jcmm.16667
Heuer GG, Skorupa AF, Prasad Alur RK, Jiang K, Wolfe JH. Accumulation of abnormal amounts of glycosaminoglycans in murine mucopolysaccharidosis type VII neural progenitor cells does not alter the growth rate or efficiency of differentiation into neurons. Mol Cell Neurosci. 2001;17:167–78. https://doi.org/10.1006/mcne.2000.0917 .
pubmed: 11161477
doi: 10.1006/mcne.2000.0917
Doubling Time - Online computing with 2 points. https://www.doubling-time.com/compute.php .
Smieszek A, Kornicka K, Szłapka-Kosarzewska J, Androvic P, Valihrach L, Langerova L, Rohlova E, Kubista M, Marycz K. Metformin increases proliferative activity and viability of multipotent stromal stem cells isolated from adipose tissue derived from horses with equine metabolic syndrome. Cells. 2019;8:80. https://doi.org/10.3390/cells8020080 .
pubmed: 30678275
pmcid: 6406832
doi: 10.3390/cells8020080
Kalmer M, Pannen K, Lemanzyk R, Wirths C, Baumeister J, Maurer A, Kricheldorf K, Schifflers J, Gezer D, Isfort S, et al. Clonogenic assays improve determination of variant allele frequency of driver mutations in myeloproliferative neoplasms. Ann Hematol. 2022;101:2655–63. https://doi.org/10.1007/s00277-022-05000-9 .
pubmed: 36269400
pmcid: 9646600
doi: 10.1007/s00277-022-05000-9
Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156–9. https://doi.org/10.1006/abio.1987.9999 .
pubmed: 2440339
doi: 10.1006/abio.1987.9999
AAT Bioquest, Inc. (2023, February 18). Quest Graph
Xiao Y, van Halteren AGS, Lei X, Borst J, Steenwijk E, de Wit T, Grabowska J, Voogd R, Kemps P, Picarsic J, et al. Bone marrow-derived myeloid progenitors as driver mutation carriers in high- and low-risk Langerhans cell histiocytosis. Blood. 2020;136:2188–99. https://doi.org/10.1182/blood.2020005209 .
pubmed: 32750121
doi: 10.1182/blood.2020005209
Allen CE, Li L, Peters TL, Leung H-CE, Yu A, Man T-K, Gurusiddappa S, Phillips MT, Hicks MJ, Gaikwad A, et al. Cell-specific gene expression in Langerhans cell histiocytosis lesions reveals a distinct profile compared with epidermal Langerhans cells. J Immunol. 2010;184:4557–67. https://doi.org/10.4049/jimmunol.0902336 .
pubmed: 20220088
doi: 10.4049/jimmunol.0902336
Gulati N, Allen CE. Langerhans cell histiocytosis: Version 2021. Hematol Oncol. 2021;39(Suppl 1):15–23. https://doi.org/10.1002/hon.2857 .
pubmed: 34105821
pmcid: 9150752
doi: 10.1002/hon.2857
Betts DR, Leibundgut KE, Feldges A, Plüss HJ, Niggli FK. Cytogenetic abnormalities in Langerhans cell histiocytosis. Br J Cancer. 1998;77:552–555.
Goyal G, Tazi A, Go RS, Rech KL, Picarsic JL, Vassallo R, Young JR, Cox CW, Van Laar J, Hermiston ML, et al. International expert consensus recommendations for the diagnosis and treatment of Langerhans cell histiocytosis in adults. Blood. 2022;139:2601–21. https://doi.org/10.1182/blood.2021014343 .
pubmed: 35271698
doi: 10.1182/blood.2021014343
Caux C, Dezutter-Dambuyant C, Schmitt D, Banchereau J. GM-CSF and TNF-alpha cooperate in the generation of dendritic Langerhans cells. Nature. 1992;360:258–61. https://doi.org/10.1038/360258a0 .
pubmed: 1279441
doi: 10.1038/360258a0
Strobl H, Riedl E, Scheinecker C, Bello-Fernandez C, Pickl WF, Rappersberger K, Majdic O, Knapp W. TGF-beta 1 promotes in vitro development of dendritic cells from CD34+ hemopoietic progenitors. J Immunol. 1996;157:1499–507.
pubmed: 8759731
doi: 10.4049/jimmunol.157.4.1499
Yasmin N, Bauer T, Modak M, Wagner K, Schuster C, Köffel R, Seyerl M, Stöckl J, Elbe-Bürger A, Graf D, et al. Identification of bone morphogenetic protein 7 (BMP7) as an instructive factor for human epidermal Langerhans cell differentiation. J Exp Med. 2013;210:2597–610. https://doi.org/10.1084/jem.20130275 .
pubmed: 24190429
pmcid: 3832935
doi: 10.1084/jem.20130275
Bigley V, McGovern N, Milne P, Dickinson R, Pagan S, Cookson S, Haniffa M, Collin M. Langerin-expressing dendritic cells in human tissues are related to CD1c+ dendritic cells and distinct from Langerhans cells and CD141high XCR1+ dendritic cells. J Leukoc Biol. 2015;97:627–34. https://doi.org/10.1189/jlb.1HI0714-351R .
pubmed: 25516751
doi: 10.1189/jlb.1HI0714-351R
Mitchell J, Kannourakis G. Does CD1a expression influence T cell function in patients with langerhans cell histiocytosis? Front Immunol. 2021;12:773598.
pubmed: 34956202
pmcid: 8702800
doi: 10.3389/fimmu.2021.773598
Andersen WK, Knowles DM, Silvers DN. CD1 (OKT6)-positive juvenile xanthogranuloma. OKT6 is not specific for Langerhans cell histiocytosis (histiocytosis X). J Am Acad Dermatol. 1992;26:850–4. https://doi.org/10.1016/0190-9622(92)70120-5 .
pubmed: 1613148
doi: 10.1016/0190-9622(92)70120-5
Lie E, Jedrych J, Sweren R, Kerns ML. Generalized indeterminate cell histiocytosis successfully treated with methotrexate. JAAD Case Rep. 2022;25:93–6. https://doi.org/10.1016/j.jdcr.2022.05.027 .
pubmed: 35799682
pmcid: 9253551
doi: 10.1016/j.jdcr.2022.05.027
Kvedaraite E, Milne P, Khalilnezhad A, Chevrier M, Sethi R, Lee HK, Hagey DW, von Bahr Greenwood T, Mouratidou N, Jädersten M, et al. Notch-dependent cooperativity between myeloid lineages promotes Langerhans cell histiocytosis pathology. Sci Immunol. 2022;7:eadd3330. https://doi.org/10.1126/sciimmunol.add3330 .
pubmed: 36525505
pmcid: 7614120
doi: 10.1126/sciimmunol.add3330
Al-Maghrabi J. Vimentin immunoexpression is associated with higher tumor grade, metastasis, and shorter survival in colorectal cancer. Int J Clin Exp Pathol. 2020;13:493–500.
pubmed: 32269687
pmcid: 7137029
Madabhavi I, Patel A, Modi G, Anand A, Panchal H, Parikh S. Interdigitating dendritic cell tumor: a rare case report with review of literature. J Cancer Res Ther. 2018;14:690–3. https://doi.org/10.4103/0973-1482.183189 .
pubmed: 29893342
doi: 10.4103/0973-1482.183189
Therrien A, El Haffaf Z, Wartelle-Bladou C, Côté-Daigneault J, Nguyen BN. Langerhans cell histiocytosis presenting as Crohn’s disease: a case report. Int J Colorectal Dis. 2018;33:1501–4. https://doi.org/10.1007/s00384-018-3066-y .
pubmed: 29737419
doi: 10.1007/s00384-018-3066-y
Luz FB, Gaspar TAP, Kalil-Gaspar N, Ramos-e-Silva M. Multicentric reticulohistiocytosis. J Eur Acad Dermatol Venereol. 2001;15:524–31. https://doi.org/10.1046/j.1468-3083.2001.00362.x .
pubmed: 11843211
doi: 10.1046/j.1468-3083.2001.00362.x
Butti R, Kumar TVS, Nimma R, Banerjee P, Kundu IG, Kundu GC. Osteopontin signaling in shaping tumor microenvironment conducive to malignant progression. Adv Exp Med Biol. 2021;1329:419–41. https://doi.org/10.1007/978-3-030-73119-9_20 .
pubmed: 34664250
doi: 10.1007/978-3-030-73119-9_20
Del Prete A, Scutera S, Sozzani S, Musso T. Role of osteopontin in dendritic cell shaping of immune responses. Cytokine Growth Factor Rev. 2019;50:19–28. https://doi.org/10.1016/j.cytogfr.2019.05.004 .
pubmed: 31126876
doi: 10.1016/j.cytogfr.2019.05.004
Tan Y, Zhao L, Yang Y-G, Liu W. The role of osteopontin in tumor progression through tumor-associated macrophages. Front Oncol. 2022;12: 953283. https://doi.org/10.3389/fonc.2022.953283 .
pubmed: 35898884
pmcid: 9309262
doi: 10.3389/fonc.2022.953283
Zhao H, Chen Q, Alam A, Cui J, Suen KC, Soo AP, Eguchi S, Gu J, Ma D. The role of osteopontin in the progression of solid organ tumour. Cell Death Dis. 2018;9:1–15. https://doi.org/10.1038/s41419-018-0391-6 .
doi: 10.1038/s41419-018-0391-6
Zhao Y, Huang C. The role of osteopontin in the development and metastasis of melanoma. Melanoma Res. 2021;31:283–9. https://doi.org/10.1097/CMR.0000000000000753 .
pubmed: 34039941
doi: 10.1097/CMR.0000000000000753
Yoo J, Jung JH, Kang SJ, Kang CS. Expression of matrix metalloproteinase-9 correlates with poor prognosis in human malignant fibrous histiocytoma. Cancer Res Treat. 2004;36:384–8. https://doi.org/10.4143/crt.2004.36.6.384 .
pubmed: 20368833
pmcid: 2843884
doi: 10.4143/crt.2004.36.6.384
Salemi R, Falzone L, Madonna G, Polesel J, Cinà D, Mallardo D, Ascierto PA, Libra M, Candido S. MMP-9 as a candidate marker of response to BRAF inhibitors in melanoma patients with BRAFV600E mutation detected in circulating-free DNA. Front Pharmacol. 2018;9:856. https://doi.org/10.3389/fphar.2018.00856 .
pubmed: 30154717
pmcid: 6102751
doi: 10.3389/fphar.2018.00856
Burgos M, Cavero-Redondo I, Álvarez-Bueno C, Galán-Moya EM, Pandiella A, Amir E, Ocaña A. Prognostic value of the immune target CEACAM6 in cancer: a meta-analysis. Ther Adv Med Oncol. 2022;14:17588359211072620. https://doi.org/10.1177/17588359211072621 .
pubmed: 35082925
pmcid: 8785271
doi: 10.1177/17588359211072621
Redd L, Schmelz M, Burack WR, Cook JR, Day AW, Rimsza L. Langerhans cell histiocytosis shows distinct cytoplasmic expression of major histocompatibility class II antigens. J Hematop. 2016;9:107–12. https://doi.org/10.1007/s12308-016-0272-9 .
pubmed: 30338008
doi: 10.1007/s12308-016-0272-9
Cavalli G, Dagna L, Biavasco R, Villa A, Doglioni C, Ferrero E, Ferrarini M. Erdheim-Chester disease: an in vivo human model of Mϕ activation at the crossroad between chronic inflammation and cancer. J Leukoc Biol. 2020;108:591–9. https://doi.org/10.1002/JLB.3MR0120-203RR .
pubmed: 32056262
doi: 10.1002/JLB.3MR0120-203RR
Grau-Vorster M, Laitinen A, Nystedt J, Vives J. HLA-DR expression in clinical-grade bone marrow-derived multipotent mesenchymal stromal cells: a two-site study. Stem Cell Res Ther. 2019;10:164. https://doi.org/10.1186/s13287-019-1279-9 .
pubmed: 31196185
pmcid: 6567533
doi: 10.1186/s13287-019-1279-9
van Megen KM, van ’t Wout EJT, Lages Motta J, Dekker B, Nikolic T, Roep BO. Activated mesenchymal stromal cells process and present antigens regulating adaptive immunity. Front Immunol. 2019;10:694. https://doi.org/10.3389/fimmu.2019.00694 .
Polchert D, Sobinsky J, Douglas G, Kidd M, Moadsiri A, Reina E, Genrich K, Mehrotra S, Setty S, Smith B, et al. IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur J Immunol. 2008;38:1745–55. https://doi.org/10.1002/eji.200738129 .
pubmed: 18493986
pmcid: 3021120
doi: 10.1002/eji.200738129
Müller L, Tunger A, Wobus M, von Bonin M, Towers R, Bornhäuser M, Dazzi F, Wehner R, Schmitz M. Immunomodulatory properties of mesenchymal stromal cells: an update. Front Cell Dev Biol. 2021;9:637725. https://doi.org/10.3389/fcell.2021.637725 .
pubmed: 33634139
pmcid: 7900158
doi: 10.3389/fcell.2021.637725
Scheid AD, Beadnell TC, Welch DR. Roles of mitochondria in the hallmarks of metastasis. Br J Cancer. 2021;124:124–35. https://doi.org/10.1038/s41416-020-01125-8 .
pubmed: 33144695
doi: 10.1038/s41416-020-01125-8
Liu Y, Sun Y, Guo Y, Shi X, Chen X, Feng W, Wu L-L, Zhang J, Yu S, Wang Y, et al. An overview: the diversified role of mitochondria in cancer metabolism. Int J Biol Sci. 2023;19:897–915. https://doi.org/10.7150/ijbs.81609 .
pubmed: 36778129
pmcid: 9910000
doi: 10.7150/ijbs.81609
Grieco JP, Allen ME, Perry JB, Wang Y, Song Y, Rohani A, Compton SLE, Smyth JW, Swami NS, Brown DA, et al. Progression-mediated changes in mitochondrial morphology promotes adaptation to hypoxic peritoneal conditions in serous ovarian cancer. Front Oncol. 2021;10:60011. https://doi.org/10.3389/fonc.2020.600113
doi: 10.3389/fonc.2020.600113
Tomková V, Sandoval-Acuña C, Torrealba N, Truksa J. Mitochondrial fragmentation, elevated mitochondrial superoxide and respiratory supercomplexes disassembly is connected with the tamoxifen-resistant phenotype of breast cancer cells. Free Radic Biol Med. 2019;143:510–21. https://doi.org/10.1016/j.freeradbiomed.2019.09.004 .
pubmed: 31494243
doi: 10.1016/j.freeradbiomed.2019.09.004
Ma Y, Wang L, Jia R. The role of mitochondrial dynamics in human cancers. Am J Cancer Res. 2020;10:1278–93.
pubmed: 32509379
pmcid: 7269774
Boulton DP, Caino MC. Mitochondrial fission and fusion in tumor progression to metastasis. Front Cell Dev Biol. 2022;10:849962. https://doi.org/10.3389/fcell.2022.849962 .
pubmed: 35356277
pmcid: 8959575
doi: 10.3389/fcell.2022.849962
Tanwar DK, Parker DJ, Gupta P, Spurlock B, Alvarez RD, Basu MK, Mitra K. Crosstalk between the mitochondrial fission protein, Drp1, and the cell cycle is identified across various cancer types and can impact survival of epithelial ovarian cancer patients. Oncotarget. 2016;7:60021–37. https://doi.org/10.18632/oncotarget.11047 .
pubmed: 27509055
pmcid: 5312366
doi: 10.18632/oncotarget.11047
Bleiberg H, Galand P. In vitro autoradiographic determination of cell kinetic parameters in adenocarcinomas and adjacent healthy mucosa of the human colon and rectum. Cancer Res. 1976;36:325–8.
pubmed: 1260740
Yano S, Miwa S, Mii S, Hiroshima Y, Uehara F, Yamamoto M, Kishimoto H, Tazawa H, Bouvet M, Fujiwara T, et al. Invading cancer cells are predominantly in G0/G1 resulting in chemoresistance demonstrated by real-time FUCCI imaging. Cell Cycle. 2014;13:953–60. https://doi.org/10.4161/cc.27818 .
pubmed: 24552821
pmcid: 3984318
doi: 10.4161/cc.27818
Greenberg A, Simon I. S phase duration is determined by local rate and global organization of replication. Biology (Basel). 2022;11:718. https://doi.org/10.3390/biology11050718 .
pubmed: 35625446
doi: 10.3390/biology11050718
Mitra K, Wunder C, Roysam B, Lin G, Lippincott-Schwartz J. A hyperfused mitochondrial state achieved at G1–S regulates cyclin E buildup and entry into S phase. Proc Natl Acad Sci. 2009;106:11960–5. https://doi.org/10.1073/pnas.0904875106 .
pubmed: 19617534
pmcid: 2710990
doi: 10.1073/pnas.0904875106
Azizidoost S, Nasrolahi A, Ghaedrahmati F, Kempisty B, Mozdziak P, Radoszkiewicz K, Farzaneh M. The pathogenic roles of lncRNA-Taurine upregulated 1 (TUG1) in colorectal cancer. Cancer Cell Int. 2022;22:335. https://doi.org/10.1186/s12935-022-02745-1 .
pubmed: 36333703
pmcid: 9636703
doi: 10.1186/s12935-022-02745-1
Hsieh PF, Yu CC, Chu PM, Hsieh PL. Long Non-Coding RNA MEG3 in Cellular Stemness. Int J Mol Sci. 2021;22:5348. https://doi.org/10.3390/ijms22105348 .
pubmed: 34069546
pmcid: 8161278
doi: 10.3390/ijms22105348
Yao Q, Yang J, Liu T, Zhang J, Zheng Y. Long noncoding RNA MALAT1 promotes the stemness of esophageal squamous cell carcinoma by enhancing YAP transcriptional activity. FEBS Open Bio. 2019;9:1392–402. https://doi.org/10.1002/2211-5463.12676 .
pubmed: 31116509
pmcid: 6668371
doi: 10.1002/2211-5463.12676
Koyama S, Tsuchiya H, Amisaki M, Sakaguchi H, Honjo S, Fujiwara Y, Shiota G. NEAT1 is required for the expression of the liver cancer stem cell marker CD44. Int J Mol Sci. 2020;21:1927. https://doi.org/10.3390/ijms21061927 .
pubmed: 32168951
pmcid: 7139689
doi: 10.3390/ijms21061927
Wang M, Gu J, Zhang X, Yang J, Zhang X, Fang X. Long non-coding RNA DANCR in cancer: roles, mechanisms, and implications. Front Cell Dev Biol. 2021;9:753706. https://doi.org/10.3389/fcell.2021.753706 .
pubmed: 34722539
pmcid: 8554091
doi: 10.3389/fcell.2021.753706
Khales SA, Mozaffari-Jovin S, Geerts D, Abbaszadegan MR. TWIST1 activates cancer stem cell marker genes to promote epithelial-mesenchymal transition and tumorigenesis in esophageal squamous cell carcinoma. BMC Cancer. 2022;22:1272. https://doi.org/10.1186/s12885-022-10252-9 .
pubmed: 36474162
pmcid: 9724315
doi: 10.1186/s12885-022-10252-9
Huang K, Tang Y. SChLAP1 promotes prostate cancer development through interacting with EZH2 to mediate promoter methylation modification of multiple miRNAs of chromosome 5 with a DNMT3a-feedback loop. Cell Death Dis. 2021;12:1–16. https://doi.org/10.1038/s41419-021-03455-8 .
doi: 10.1038/s41419-021-03455-8
Kidd SG, Carm KT, Bogaard M, Olsen LG, Bakken AC, Løvf M, Lothe RA, Axcrona K, Axcrona U, Skotheim RI. High expression of SCHLAP1 in primary prostate cancer is an independent predictor of biochemical recurrence, despite substantial heterogeneity. Neoplasia. 2021;23:634–41. https://doi.org/10.1016/j.neo.2021.05.012 .
pubmed: 34107378
pmcid: 8192444
doi: 10.1016/j.neo.2021.05.012
Liang Y, Zhang D, Zheng T, Yang G, Wang J, Meng F, Liu Y, Zhang G, Zhang L, Han J, et al. lncRNA-SOX2OT promotes hepatocellular carcinoma invasion and metastasis through miR-122-5p-mediated activation of PKM2. Oncogenesis. 2020;9:1–12. https://doi.org/10.1038/s41389-020-0242-z .
doi: 10.1038/s41389-020-0242-z