The Hallmarks of Circulating Hybrid Cells.
Cellular fusion
Hallmarks of cancer
Macrophage
Metastasis
Neoplastic-immune cell hybrid
Tumor
Journal
Results and problems in cell differentiation
ISSN: 0080-1844
Titre abrégé: Results Probl Cell Differ
Pays: Germany
ID NLM: 0173555
Informations de publication
Date de publication:
2024
2024
Historique:
medline:
27
11
2023
pubmed:
24
11
2023
entrez:
23
11
2023
Statut:
ppublish
Résumé
While tumor metastases represent the primary driver of cancer-related mortality, our understanding of the mechanisms that underlie metastatic initiation and progression remains incomplete. Recent work identified a novel tumor-macrophage hybrid cell population, generated through the fusion between neoplastic and immune cells. These hybrid cells are detected in primary tumor tissue, peripheral blood, and in metastatic sites. In-depth analyses of hybrid cell biology indicate that they can exploit phenotypic properties of both parental tumor and immune cells, in order to intravasate into circulation, evade the immune response, and seed tumors at distant sites. Thus, it has become increasingly evident that the development and dissemination of tumor-immune hybrid cells play an intricate and fundamental role in the metastatic cascade and can provide invaluable information regarding tumor characteristics and patient prognostication. In this chapter, we review the current understanding of this novel hybrid cell population, the specific hallmarks of cancer that these cells exploit to promote cancer progression and metastasis, and discuss exciting new frontiers that remain to be explored.
Identifiants
pubmed: 37996690
doi: 10.1007/978-3-031-37936-9_21
doi:
Types de publication
Review
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
467-485Informations de copyright
© 2024. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Aichel O (1911) Über Zellverschmelzung mit qualitativ abnormer Chromosomenverteilung als Ursache der Geschwulstbildung, vol 13. W. Engelmann, Leipzig
Allan AL, Vantyghem SA, Tuck AB, Chambers AF, Chin-Yee IH, Keeney M (2005) Detection and quantification of circulating tumor cells in mouse models of human breast cancer using immunomagnetic enrichment and multiparameter flow cytometry. Cytometry A 65(1):4–14. https://doi.org/10.1002/cyto.a.20132
doi: 10.1002/cyto.a.20132
pubmed: 15810015
Avilès D, Jami J, Rousset JP, Ritz E (1977) Tumor x host cell hybrids in the mouse: chromosomes from the normal cell parent maintained in malignant hybrid tumors. J Natl Cancer Inst 58(5):1391–1399. https://doi.org/10.1093/jnci/58.5.1391
doi: 10.1093/jnci/58.5.1391
pubmed: 853528
Ben-David U, Amon A (2020) Context is everything: aneuploidy in cancer. Nat Rev Genet 21(1):44–62. https://doi.org/10.1038/s41576-019-0171-x
doi: 10.1038/s41576-019-0171-x
pubmed: 31548659
Boveri T (2008) Concerning the origin of malignant tumours by Theodor Boveri. Translated and annotated by Henry Harris. J Cell Sci 121 Suppl 1:1–84. https://doi.org/10.1242/jcs.025742
doi: 10.1242/jcs.025742
pubmed: 18089652
Cancer Statistics Center (2020) American Cancer Society. http://cancerstatisticscenter.cancer.org . Accessed 1 Dec 2022
Cao MF, Chen L, Dang WQ, Zhang XC, Zhang X, Shi Y, Yao XH, Li Q, Zhu J, Lin Y, Liu S, Chen Q, Cui YH, Zhang X, Bian XW (2019) Hybrids by tumor-associated macrophages × glioblastoma cells entail nuclear reprogramming and glioblastoma invasion. Cancer Lett 442:445–452. https://doi.org/10.1016/j.canlet.2018.11.016
Casanova-Acebes M, Dalla E, Leader AM, LeBerichel J, Nikolic J, Morales BM, Brown M, Chang C, Troncoso L, Chen ST, Sastre-Perona A, Park MD, Tabachnikova A, Dhainaut M, Hamon P, Maier B, Sawai CM, Agulló-Pascual E, Schober M, Brown BD, Reizis B, Marron T, Kenigsberg E, Moussion C, Benaroch P, Aguirre-Ghiso JA, Merad M (2021) Tissue-resident macrophages provide a pro-tumorigenic niche to early NSCLC cells. Nature 595(7868):578–584. https://doi.org/10.1038/s41586-021-03651-8
doi: 10.1038/s41586-021-03651-8
pubmed: 34135508
pmcid: 8923521
Chakraborty AK, Sodi S, Rachkovsky M, Kolesnikova N, Platt JT, Bolognia JL, Pawelek JM (2000) A spontaneous murine melanoma lung metastasis comprised of host x tumor hybrids. Cancer Res 60(9):2512–2519
pubmed: 10811133
Chakraborty A, Lazova R, Davies S, Bäckvall H, Ponten F, Brash D, Pawelek J (2004) Donor DNA in a renal cell carcinoma metastasis from a bone marrow transplant recipient. Bone Marrow Transplant 34(2):183–186. https://doi.org/10.1038/sj.bmt.1704547
doi: 10.1038/sj.bmt.1704547
pubmed: 15195072
Clawson GA, Kimchi E, Patrick SD, Xin P, Harouaka R, Zheng S, Berg A, Schell T, Staveley-O’Carroll KF, Neves RI, Mosca PJ, Thiboutot D (2012) Circulating tumor cells in melanoma patients. PLoS One 7(7):e41052. https://doi.org/10.1371/journal.pone.0041052
doi: 10.1371/journal.pone.0041052
pubmed: 22829910
pmcid: 3400630
Clawson GA, Matters GL, Xin P, Imamura-Kawasawa Y, Du Z, Thiboutot DM, Helm KF, Neves RI, Abraham T (2015) Macrophage-tumor cell fusions from peripheral blood of melanoma patients. PLoS One 10(8):e0134320. https://doi.org/10.1371/journal.pone.0134320
doi: 10.1371/journal.pone.0134320
pubmed: 26267609
pmcid: 4534457
Davies PS, Powell AE, Swain JR, Wong MH (2009) Inflammation and proliferation act together to mediate intestinal cell fusion. PLoS One 4(8):e6530. https://doi.org/10.1371/journal.pone.0006530
doi: 10.1371/journal.pone.0006530
pubmed: 19657387
pmcid: 2716548
DeNardo DG, Andreu P, Coussens LM (2010) Interactions between lymphocytes and myeloid cells regulate pro- versus anti-tumor immunity. Cancer Metastasis Rev 29(2):309–316. https://doi.org/10.1007/s10555-010-9223-6
doi: 10.1007/s10555-010-9223-6
pubmed: 20405169
pmcid: 2865635
de Visser KE, Coussens LM (2006) The inflammatory tumor microenvironment and its impact on cancer development. Contrib Microbiol 13:118–137. https://doi.org/10.1159/000092969
doi: 10.1159/000092969
pubmed: 16627962
de Wit S, Zeune LL, Hiltermann TJN, Groen HJM, Dalum GV, Terstappen L (2018) Classification of cells in CTC-enriched samples by advanced image analysis. Cancers (Basel) 10(10). https://doi.org/10.3390/cancers10100377
Dietz MS, Sutton TL, Walker BS, Gast CE, Zarour L, Sengupta SK, Swain JR, Eng J, Parappilly M, Limbach K, Sattler A, Burlingame E, Chin Y, Gower A, Mira JLM, Sapre A, Chiu YJ, Clayburgh DR, Pommier SJ, Cetnar JP, Fischer JM, Jaboin JJ, Pommier RF, Sheppard BC, Tsikitis VL, Skalet AH, Mayo SC, Lopez CD, Gray JW, Mills GB, Mitri Z, Chang YH, Chin K, Wong MH (2021) Relevance of circulating hybrid cells as a non-invasive biomarker for myriad solid tumors. Sci Rep 11(1):13630. https://doi.org/10.1038/s41598-021-93053-7
doi: 10.1038/s41598-021-93053-7
pubmed: 34211050
pmcid: 8249418
Ding J, Jin W, Chen C, Shao Z, Wu J (2012) Tumor associated macrophage × cancer cell hybrids may acquire cancer stem cell properties in breast cancer. PLoS One 7(7):e41942. https://doi.org/10.1371/journal.pone.0041942
Duelli D, Lazebnik Y (2003) Cell fusion: a hidden enemy? Cancer Cell 3(5):445–448. https://doi.org/10.1016/s1535-6108(03)00114-4
doi: 10.1016/s1535-6108(03)00114-4
pubmed: 12781362
Durmus NG, Tekin HC, Guven S, Sridhar K, Arslan Yildiz A, Calibasi G, Ghiran I, Davis RW, Steinmetz LM, Demirci U (2015) Magnetic levitation of single cells. Proc Natl Acad Sci U S A 112(28):E3661–E3668. https://doi.org/10.1073/pnas.1509250112
doi: 10.1073/pnas.1509250112
pubmed: 26124131
pmcid: 4507238
Fortuna MB, Dewey MJ, Furmanski P (1989) Cell fusion in tumor development and progression: occurrence of cell fusion in primary methylcholanthrene-induced tumorigenesis. Int J Cancer 44(4):731–737. https://doi.org/10.1002/ijc.2910440430
doi: 10.1002/ijc.2910440430
pubmed: 2793245
Fortuna MB, Dewey MJ, Furmanski P (1990) Enhanced lung colonization and tumorigenicity of fused cells isolated from primary MCA tumors. Cancer Lett 55(2):109–114. https://doi.org/10.1016/0304-3835(90)90019-t
doi: 10.1016/0304-3835(90)90019-t
pubmed: 2265408
Friedl P, Wolf K (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3(5):362–374. https://doi.org/10.1038/nrc1075
doi: 10.1038/nrc1075
pubmed: 12724734
Gast CE, Silk AD, Zarour L, Riegler L, Burkhart JG, Gustafson KT, Parappilly MS, Roh-Johnson M, Goodman JR, Olson B, Schmidt M, Swain JR, Davies PS, Shasthri V, Iizuka S, Flynn P, Watson S, Korkola J, Courtneidge SA, Fischer JM, Jaboin J, Billingsley KG, Lopez CD, Burchard J, Gray J, Coussens LM, Sheppard BC, Wong MH (2018) Cell fusion potentiates tumor heterogeneity and reveals circulating hybrid cells that correlate with stage and survival. Sci Adv 4(9):eaat7828. https://doi.org/10.1126/sciadv.aat7828
doi: 10.1126/sciadv.aat7828
pubmed: 30214939
pmcid: 6135550
Goldenberg DM (1968) [On the progression of malignity: a hypothesis]. Klin Wochenschr 46(16):898–899. https://doi.org/10.1007/bf01746251
Goldenberg DM, Bhan RD, Pavia RA (1971) In vivo human-hamster somatic cell fusion indicated by glucose 6-phosphate dehydrogenase and lactate dehydrogenase profiles. Cancer Res 31(8):1148–1152
pubmed: 5095979
Goldenberg DM, Pavia RA, Tsao MC (1974) In vivo hybridisation of human tumour and normal hamster cells. Nature 250(5468):649–651. https://doi.org/10.1038/250649a0
doi: 10.1038/250649a0
pubmed: 4859359
Goldenberg DM, Rooney RJ, Loo M, Liu D, Chang CH (2014) In-vivo fusion of human cancer and hamster stromal cells permanently transduces and transcribes human DNA. PLoS One 9(9):e107927. https://doi.org/10.1371/journal.pone.0107927
doi: 10.1371/journal.pone.0107927
pubmed: 25259521
pmcid: 4178054
Gupta GP, Massagué J (2006) Cancer metastasis: building a framework. Cell 127(4):679–695. https://doi.org/10.1016/j.cell.2006.11.001
doi: 10.1016/j.cell.2006.11.001
pubmed: 17110329
Hanahan D (2022) Hallmarks of cancer: new dimensions. Cancer Discov 12(1):31–46. https://doi.org/10.1158/2159-8290.Cd-21-1059
doi: 10.1158/2159-8290.Cd-21-1059
pubmed: 35022204
Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100(1):57–70. https://doi.org/10.1016/s0092-8674(00)81683-9
doi: 10.1016/s0092-8674(00)81683-9
pubmed: 10647931
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674. https://doi.org/10.1016/j.cell.2011.02.013
doi: 10.1016/j.cell.2011.02.013
pubmed: 21376230
Hass R, von der Ohe J, Dittmar T (2021) Hybrid formation and fusion of cancer cells in vitro and in vivo. Cancers (Basel) 13(17). https://doi.org/10.3390/cancers13174496
Jiang E, Yan T, Xu Z, Shang Z (2019) Tumor microenvironment and cell fusion. Biomed Res Int 2019:5013592. https://doi.org/10.1155/2019/5013592
doi: 10.1155/2019/5013592
pubmed: 31380426
pmcid: 6657644
Johansson CB, Youssef S, Koleckar K, Holbrook C, Doyonnas R, Corbel SY, Steinman L, Rossi FM, Blau HM (2008) Extensive fusion of haematopoietic cells with Purkinje neurons in response to chronic inflammation. Nat Cell Biol 10(5):575–583. https://doi.org/10.1038/ncb1720
doi: 10.1038/ncb1720
pubmed: 18425116
pmcid: 4230437
Kerbel RS, Lagarde AE, Dennis JW, Donaghue TP (1983) Spontaneous fusion in vivo between normal host and tumor cells: possible contribution to tumor progression and metastasis studied with a lectin-resistant mutant tumor. Mol Cell Biol 3(4):523–538. https://doi.org/10.1128/mcb.3.4.523-538.1983
doi: 10.1128/mcb.3.4.523-538.1983
pubmed: 6687920
pmcid: 368568
LaBerge GS, Duvall E, Grasmick Z, Haedicke K, Pawelek J (2017) A melanoma lymph node metastasis with a donor-patient hybrid genome following bone marrow transplantation: a second case of leucocyte-tumor cell hybridization in cancer metastasis. PLoS One 12(2):e0168581. https://doi.org/10.1371/journal.pone.0168581
doi: 10.1371/journal.pone.0168581
pubmed: 28146572
pmcid: 5287451
LaBerge GS, Duvall E, Haedicke K, Pawelek J (2019) Leukocyte
LaBerge G, Duvall E, Grasmick Z, Haedicke K, Galan A, Pawelek J (2021) A melanoma patient with macrophage-cancer cell hybrids in the primary tumor, a lymph node metastasis and a brain metastasis. Cancer Genet 256-257:162–164. https://doi.org/10.1016/j.cancergen.2021.05.009
doi: 10.1016/j.cancergen.2021.05.009
pubmed: 34166887
Larsson LI (2010) Cell fusions: regulation and control. Springer, Dordrecht
Lazova R, LaBerge GS, Duvall E, Spoelstra N, Klump V, Sznol M, Cooper D, Spritz RA, Chang JT, Pawelek JM (2013) A melanoma brain metastasis with a donor-patient hybrid genome following bone marrow transplantation: first evidence for fusion in human cancer. PLoS One 8(6):e66731. https://doi.org/10.1371/journal.pone.0066731
doi: 10.1371/journal.pone.0066731
pubmed: 23840523
pmcid: 3694119
Leopold Wager CM, Wormley FL Jr (2014) Classical versus alternative macrophage activation: the Ying and the Yang in host defense against pulmonary fungal infections. Mucosal Immunol 7(5):1023–1035. https://doi.org/10.1038/mi.2014.65
doi: 10.1038/mi.2014.65
pubmed: 25073676
Li W, Ma H, Zhang J, Zhu L, Wang C, Yang Y (2017) Unraveling the roles of CD44/CD24 and ALDH1 as cancer stem cell markers in tumorigenesis and metastasis. Sci Rep 7(1):13856. https://doi.org/10.1038/s41598-017-14364-2
doi: 10.1038/s41598-017-14364-2
pubmed: 29062075
pmcid: 5653849
Li H, Meng QH, Noh H, Somaiah N, Torres KE, Xia X, Batth IS, Joseph CP, Liu M, Wang R, Li S (2018) Cell-surface vimentin-positive macrophage-like circulating tumor cells as a novel biomarker of metastatic gastrointestinal stromal tumors. Oncoimmunology 7(5):e1420450. https://doi.org/10.1080/2162402x.2017.1420450
doi: 10.1080/2162402x.2017.1420450
pubmed: 29721368
pmcid: 5927484
Liang K, Yaman S, Patel RK, Parappilly MS, Walker BS, Wong MH, Durmus NG (2022) Magnetic levitation and sorting of neoplastic circulating cell hybrids. bioRxiv. https://doi.org/10.1101/2022.11.03.515127
Lin EY, Pollard JW (2004) Macrophages: modulators of breast cancer progression. Novartis Found Symp 256:158–168. Discussion 168–172, 259–169
doi: 10.1002/0470856734.ch12
pubmed: 15027489
Lin D, Shen L, Luo M, Zhang K, Li J, Yang Q, Zhu F, Zhou D, Zheng S, Chen Y, Zhou J (2021) Circulating tumor cells: biology and clinical significance. Signal Transduct Target Ther 6(1). https://doi.org/10.1038/s41392-021-00817-8
Liu Q, Liao Q, Zhao Y (2016) Myeloid-derived suppressor cells (MDSC) facilitate distant metastasis of malignancies by shielding circulating tumor cells (CTC) from immune surveillance. Med Hypotheses 87:34–39. https://doi.org/10.1016/j.mehy.2015.12.007
doi: 10.1016/j.mehy.2015.12.007
pubmed: 26826638
Lu X, Kang Y (2009) Efficient acquisition of dual metastasis organotropism to bone and lung through stable spontaneous fusion between MDA-MB-231 variants. Proc Natl Acad Sci U S A 106(23):9385–9390. https://doi.org/10.1073/pnas.0900108106
doi: 10.1073/pnas.0900108106
pubmed: 19458257
pmcid: 2695061
Malyshev I, Malyshev Y (2015) Current concept and update of the macrophage plasticity concept: intracellular mechanisms of reprogramming and M3 macrophage “switch” phenotype. Biomed Res Int 2015:341308. https://doi.org/10.1155/2015/341308
doi: 10.1155/2015/341308
pubmed: 26366410
pmcid: 4561113
Manjunath Y, Mitchem JB, Suvilesh KN, Avella DM, Kimchi ET, Staveley-O’Carroll KF, Deroche CB, Pantel K, Li G, Kaifi JT (2020) Circulating giant tumor-macrophage fusion cells are independent prognosticators in patients with NSCLC. J Thorac Oncol 15(9):1460–1471. https://doi.org/10.1016/j.jtho.2020.04.034
doi: 10.1016/j.jtho.2020.04.034
pubmed: 32416323
Mantovani A, Marchesi F, Malesci A, Laghi L, Allavena P (2017) Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol 14(7):399–416. https://doi.org/10.1038/nrclinonc.2016.217
doi: 10.1038/nrclinonc.2016.217
pubmed: 28117416
pmcid: 5480600
Mekler LB (1971) [Hybridization of transformed cells with lymphocytes as 1 of the probable causes of the progression leading to the development of metastatic malignant cells]. Vestn Akad Med Nauk SSSR 26(8):80–89
Melzer C, Ohe JV, Hass R (2020) Altered tumor plasticity after different cancer cell fusions with MSC. Int J Mol Sci 21(21). https://doi.org/10.3390/ijms21218347
Melzer C, Ohe JV, Luo T, Hass R (2021) Spontaneous fusion of MSC with breast cancer cells can generate tumor dormancy. Int J Mol Sci 22(11). https://doi.org/10.3390/ijms22115930
Mohme M, Riethdorf S, Pantel K (2017) Circulating and disseminated tumour cells—mechanisms of immune surveillance and escape. Nat Rev Clin Oncol 14(3):155–167. https://doi.org/10.1038/nrclinonc.2016.144
doi: 10.1038/nrclinonc.2016.144
pubmed: 27644321
Mohr M, Tosun S, Arnold WH, Edenhofer F, Zänker KS, Dittmar T (2015) Quantification of cell fusion events human breast cancer cells and breast epithelial cells using a Cre-LoxP-based double fluorescence reporter system. Cell Mol Life Sci 72(19):3769–3782. https://doi.org/10.1007/s00018-015-1910-6
doi: 10.1007/s00018-015-1910-6
pubmed: 25900663
Nel I, Jehn U, Gauler T, Hoffmann AC (2014) Individual profiling of circulating tumor cell composition in patients with non-small cell lung cancer receiving platinum based treatment. Transl Lung Cancer Res 3(2):100–106. https://doi.org/10.3978/j.issn.2218-6751.2014.03.05
doi: 10.3978/j.issn.2218-6751.2014.03.05
pubmed: 25806288
pmcid: 4367657
Neubert NJ, Schmittnaegel M, Bordry N, Nassiri S, Wald N, Martignier C, Tillé L, Homicsko K, Damsky W, Maby-El Hajjami H, Klaman I, Danenberg E, Ioannidou K, Kandalaft L, Coukos G, Hoves S, Ries CH, Fuertes Marraco SA, Foukas PG, De Palma M, Speiser DE (2018) T cell-induced CSF1 promotes melanoma resistance to PD1 blockade. Sci Transl Med 10(436). https://doi.org/10.1126/scitranslmed.aan3311
Noy R, Pollard JW (2014) Tumor-associated macrophages: from mechanisms to therapy. Immunity 41(1):49–61. https://doi.org/10.1016/j.immuni.2014.06.010
doi: 10.1016/j.immuni.2014.06.010
pubmed: 25035953
pmcid: 4137410
Nygren JM, Liuba K, Breitbach M, Stott S, Thorén L, Roell W, Geisen C, Sasse P, Kirik D, Björklund A, Nerlov C, Fleischmann BK, Jovinge S, Jacobsen SE (2008) Myeloid and lymphoid contribution to non-haematopoietic lineages through irradiation-induced heterotypic cell fusion. Nat Cell Biol 10(5):584–592. https://doi.org/10.1038/ncb1721
doi: 10.1038/ncb1721
pubmed: 18425115
Parappilly MS, Chin Y, Whalen RM, Anderson AN, Robinson TS, Strgar L, Sutton TL, Conley P, Klocke C, Gibbs SL, Chang YH, Wu G, Wong MH, Skalet AH (2022) Circulating neoplastic-immune hybrid cells predict metastatic progression in uveal melanoma. Cancers (Basel) 14(19). https://doi.org/10.3390/cancers14194617
Park MD, Silvin A, Ginhoux F, Merad M (2022) Macrophages in health and disease. Cell 185(23):4259–4279. https://doi.org/10.1016/j.cell.2022.10.007
doi: 10.1016/j.cell.2022.10.007
pubmed: 36368305
pmcid: 9908006
Parker KH, Beury DW, Ostrand-Rosenberg S (2015) Myeloid-derived suppressor cells: critical cells driving immune suppression in the tumor microenvironment. Adv Cancer Res 128:95–139. https://doi.org/10.1016/bs.acr.2015.04.002
doi: 10.1016/bs.acr.2015.04.002
pubmed: 26216631
pmcid: 4662416
Pawelek JM (2005) Tumour-cell fusion as a source of myeloid traits in cancer. Lancet Oncol 6(12):988–993. https://doi.org/10.1016/s1470-2045(05)70466-6
doi: 10.1016/s1470-2045(05)70466-6
pubmed: 16321767
Pawelek JM (2007) Viewing malignant melanoma cells as macrophage-tumor hybrids. Cell Adh Migr 1(1):2–6
doi: 10.4161/cam.3841
pubmed: 19262091
pmcid: 2633673
Pawelek JM, Chakraborty AK (2008a) The cancer cell—leukocyte fusion theory of metastasis. Adv Cancer Res 101:397–444. https://doi.org/10.1016/s0065-230x(08)00410-7
doi: 10.1016/s0065-230x(08)00410-7
pubmed: 19055949
Pawelek JM, Chakraborty AK (2008b) Fusion of tumour cells with bone marrow-derived cells: a unifying explanation for metastasis. Nat Rev Cancer 8(5):377–386. https://doi.org/10.1038/nrc2371
doi: 10.1038/nrc2371
pubmed: 18385683
Peinado H, Marin F, Cubillo E, Stark HJ, Fusenig N, Nieto MA, Cano A (2004) Snail and E47 repressors of E-cadherin induce distinct invasive and angiogenic properties in vivo. J Cell Sci 117(Pt 13):2827–2839. https://doi.org/10.1242/jcs.01145
doi: 10.1242/jcs.01145
pubmed: 15169839
Powell AE, Anderson EC, Davies PS, Silk AD, Pelz C, Impey S, Wong MH (2011) Fusion between Intestinal epithelial cells and macrophages in a cancer context results in nuclear reprogramming. Cancer Res 71(4):1497–1505. https://doi.org/10.1158/0008-5472.Can-10-3223
doi: 10.1158/0008-5472.Can-10-3223
pubmed: 21303980
pmcid: 3079548
Puluca N, Durmus NG, Lee S, Belbachir N, Galdos FX, Ogut MG, Gupta R, Hirano KI, Krane M, Lange R, Wu JC, Wu SM, Demirci U (2020) Levitating cells to sort the fit and the fat. Adv Biosyst 4(6):e1900300. https://doi.org/10.1002/adbi.201900300
doi: 10.1002/adbi.201900300
pubmed: 32352239
Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141(1):39–51. https://doi.org/10.1016/j.cell.2010.03.014
doi: 10.1016/j.cell.2010.03.014
pubmed: 20371344
pmcid: 4994190
Rizvi AZ, Swain JR, Davies PS, Bailey AS, Decker AD, Willenbring H, Grompe M, Fleming WH, Wong MH (2006) Bone marrow-derived cells fuse with normal and transformed intestinal stem cells. Proc Natl Acad Sci U S A 103(16):6321–6325. https://doi.org/10.1073/pnas.0508593103
doi: 10.1073/pnas.0508593103
pubmed: 16606845
pmcid: 1435365
Senger DR, Perruzzi CA, Feder J, Dvorak HF (1986) A highly conserved vascular permeability factor secreted by a variety of human and rodent tumor cell lines. Cancer Res 46(11):5629–5632
pubmed: 3756910
Silk AD, Gast CE, Davies PS, Fakhari FD, Vanderbeek GE, Mori M, Wong MH (2013) Fusion between hematopoietic and epithelial cells in adult human intestine. PLoS One 8(1):e55572. https://doi.org/10.1371/journal.pone.0055572
doi: 10.1371/journal.pone.0055572
pubmed: 23383228
pmcid: 3559593
Skokos EA, Charokopos A, Khan K, Wanjala J, Kyriakides TR (2011) Lack of TNF-α-induced MMP-9 production and abnormal E-cadherin redistribution associated with compromised fusion in MCP-1-null macrophages. Am J Pathol 178(5):2311–2321. https://doi.org/10.1016/j.ajpath.2011.01.045
doi: 10.1016/j.ajpath.2011.01.045
pubmed: 21514443
pmcid: 3081180
Stramer B, Mayor R (2017) Mechanisms and in vivo functions of contact inhibition of locomotion. Nat Rev Mol Cell Biol 18(1):43–55. https://doi.org/10.1038/nrm.2016.118
doi: 10.1038/nrm.2016.118
pubmed: 27677859
Sutton TL, Walker BS, Wong MH (2019) Circulating hybrid cells join the fray of circulating cellular biomarkers. Cell Mol Gastroenterol Hepatol 8(4):595–607. https://doi.org/10.1016/j.jcmgh.2019.07.002
doi: 10.1016/j.jcmgh.2019.07.002
pubmed: 31319228
pmcid: 6889578
Sutton TL, Patel RK, Anderson AN, Bowden SG, Whalen R, Giske NR, Wong MH (2022) Circulating cells with macrophage-like characteristics in cancer: the importance of circulating neoplastic-immune hybrid cells in cancer. Cancers (Basel) 14(16). https://doi.org/10.3390/cancers14163871
Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, Hartwell K, Onder TT, Gupta PB, Evans KW, Hollier BG, Ram PT, Lander ES, Rosen JM, Weinberg RA, Mani SA (2010) Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci U S A 107(35):15449–15454. https://doi.org/10.1073/pnas.1004900107
doi: 10.1073/pnas.1004900107
pubmed: 20713713
pmcid: 2932589
Tocchio A, Durmus NG, Sridhar K, Mani V, Coskun B, El Assal R, Demirci U (2018) Magnetically guided self-assembly and coding of 3D living architectures. Adv Mater 30(4). https://doi.org/10.1002/adma.201705034
Toyoshima K, Hayashi A, Kashiwagi M, Hayashi N, Iwatsuki M, Ishimoto T, Baba Y, Baba H, Ohta Y (2015) Analysis of circulating tumor cells derived from advanced gastric cancer. Int J Cancer 137(4):991–998. https://doi.org/10.1002/ijc.29455
doi: 10.1002/ijc.29455
pubmed: 25622566
Vande Woude GF, Klein G (2009) Advances in cancer research. Elsevier, San Diego
Virchow R (1863) Cellular pathology as based upon physiological and pathological histology. Dover, New York
doi: 10.5962/bhl.title.32770
Walker BS, Sutton TL, Zarour L, Hunter JG, Wood SG, Tsikitis VL, Herzig DO, Lopez CD, Chen EY, Mayo SC, Wong MH (2021) Circulating hybrid cells: a novel liquid biomarker of treatment response in gastrointestinal cancers. Ann Surg Oncol 28(13):8567–8578. https://doi.org/10.1245/s10434-021-10379-2
doi: 10.1245/s10434-021-10379-2
pubmed: 34365557
pmcid: 8995146
Wang HF, Xiang W, Xue BZ, Wang YH, Yi DY, Jiang XB, Zhao HY, Fu P (2021) Cell fusion in cancer hallmarks: Current research status and future indications. Oncol Lett 22(1):530. https://doi.org/10.3892/ol.2021.12791
doi: 10.3892/ol.2021.12791
pubmed: 34055095
pmcid: 8138896
Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, Graf T, Pollard JW, Segall J, Condeelis J (2004) A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 64(19):7022–7029. https://doi.org/10.1158/0008-5472.Can-04-1449
doi: 10.1158/0008-5472.Can-04-1449
pubmed: 15466195
Yilmaz Y, Lazova R, Qumsiyeh M, Cooper D, Pawelek J (2005) Donor Y chromosome in renal carcinoma cells of a female BMT recipient: visualization of putative BMT-tumor hybrids by FISH. Bone Marrow Transplant 35(10):1021–1024. https://doi.org/10.1038/sj.bmt.1704939
doi: 10.1038/sj.bmt.1704939
pubmed: 15778726
Zhang Y, Wang F, Ning N, Chen Q, Yang Z, Guo Y, Xu D, Zhang D, Zhan T, Cui W (2015) Patterns of circulating tumor cells identified by CEP8, CK and CD45 in pancreatic cancer. Int J Cancer 136(5):1228–1233. https://doi.org/10.1002/ijc.29070
doi: 10.1002/ijc.29070
pubmed: 25042121