CoChat
Sign Up
Cited by 36Sarcoma Diagnosis and TreatmentBone Tumor Diagnosis and TreatmentsCancer Immunotherapy and Biomarkers

Identification of prognostic biomarkers associated with metastasis and immune infiltration in osteosarcoma

Open access
Yang, Bingsheng, Su, Zexin, Chen, Guoli, Zeng, Zhirui, Tan, Jianye, Wu, Guofeng, Zhu, Shuang, Lin, Lijun·2021·Oncology Letters
DOI 10.3892/ol.2021.12441PMC PMC7816295
Open this paper in CoChat — free account

Abstract

Osteosarcoma is the most common primary malignancy of the bones, and is associated with a high rate of metastasis and a poor prognosis. A tight association between the tumor microenvironment (TME) and osteosarcoma metastasis has been established. In the present study, the Estimation of STromal and Immune cells in MAlignant Tumor tissues using Expression data (ESTIMATE) algorithm was applied to calculate the immune and stromal scores of patients with osteosarcoma based on data from The Cancer Genome Atlas database. A metagene approach and deconvolution method were used to reveal distinct TME landscapes in patients with osteosarcoma. Bioinformatics analysis was used to identify differentially expressed genes (DEGs) associated with metastasis and immune infiltration in osteosarcoma, and a risk model was constructed using the DEGs with potential prognostic significance. Subsequently, gene set enrichment and Spearman's correlation analyses were used to delineate the biological processes associated with these prognostic biomarkers. Finally, immunohistochemical (IHC) analysis was performed to evaluate the expression levels of immune infiltrates and prognostic biomarkers in clinical osteosarcoma tissues. The results of the ESTIMATE demonstrated that patients with non‑metastatic osteosarcoma presented with higher immune/stromal scores and a more favorable prognosis compared with those with metastatic osteosarcoma. The TME landscapes in patients with osteosarcoma suggested that high levels of tumor‑infiltrating immune cells (TIICs) may suppress metastasis. Increased numbers of CD56bright natural killer cells, immature B cells, M1 macrophages and neutrophils, and lower levels of M2 macrophages were observed in the non‑metastatic tissues compared with those in the metastatic tissues. A total of 69 DEGs were identified to be associated with metastasis and immune infiltration in osteosarcoma. Of these, GATA3, LPAR5, EVI2B, RIAM and CFH exhibited prognostic potential and were highly expressed in non‑metastatic osteosarcoma tissues based on the IHC analysis results. These biomarkers were involved in various immune‑related biological processes and were positively associated with multiple TIICs and immune signatures. The risk model constructed using these prognostic biomarkers demonstrated high predictive accuracy for the prognosis of osteosarcoma. In conclusion, the present study proposed a five‑biomarker prognostic signature for the prediction of metastasis and immune infiltration in patients with osteosarcoma.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3892/ol.2021.12441

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Patients with non-metastasis showed higher immune scores and better prognosis compared with those with metastatic osteosarcoma.

    “The analysis of TME landscapes in osteosarcoma suggested that patients with non-metastasis showed higher immune scores and better prognosis compared with those with metastatic osteosarcoma.”

    From Advances on immunotherapy for osteosarcoma (2024) · cites this paper as [38]

  • High levels of tumor-infiltrating immune cells may suppress metastasis.

    “In addition, high levels of tumor-infiltrating immune cells may suppress metastasis [38].”

    From Advances on immunotherapy for osteosarcoma (2024) · cites this paper as [38]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 76

  1. [1]Ritter J Bielack SS Osteosarcoma Ann Oncol 21 Suppl 7 vii320 vii325 2010 10.1093/annonc/mdq276 20943636 · DOI
  2. [3]Huang L Huang Z Lin W Wang L Zhu X Chen X Yang S Lv C Salidroside suppresses the growth and invasion of human osteosarcoma cell lines MG63 and U2OS in vitro by inhibiting the JAK2/STAT3 signaling pathway Int J Oncol 54 1969 1980 2019 31081055 PMC6521935
  3. [4]Sergi C Zwerschke W Osteogenic sarcoma (osteosarcoma) in the elderly: Tumor delineation and predisposing conditions Exp Gerontol 43 1039 1043 2008 10.1016/j.exger.2008.09.009 18845233 · DOI
  4. [5]Jaffe N Osteosarcoma: Review of the past, impact on the future. The American experience Cancer Treat Res 152 239 262 2009 10.1007/978-1-4419-0284-9_12 20213394 · DOI
  5. [6]Miwa S Shirai T Yamamoto N Hayashi K Takeuchi A Igarashi K Tsuchiya H Current and emerging targets in immunotherapy for osteosarcoma J Oncol 2019 7035045 2019 10.1155/2019/7035045 30693030 PMC6332920 · DOI
  6. [7]Reed DR Hayashi M Wagner L Binitie O Steppan DA Brohl AS Shinohara ET Bridge JA Loeb DM Borinstein SC Isakoff MS Treatment pathway of bone sarcoma in children, adolescents, and young adults Cancer 123 2206 2218 2017 10.1002/cncr.30589 28323337 PMC5485018 · DOI
  7. [8]Reina-Campos M Moscat J Diaz-Meco M Metabolism shapes the tumor microenvironment Curr Opin Cell Biol 48 47 53 2017 10.1016/j.ceb.2017.05.006 28605656 PMC5650101 · DOI
  8. [9]Meurette O Mehlen P Notch signaling in the tumor microenvironment Cancer Cell 34 536 548 2018 10.1016/j.ccell.2018.07.009 30146333 · DOI
  9. [10]Chen JL Lucas JE Schroeder T Mori S Wu J Nevins J Dewhirst M West M Chi JT The genomic analysis of lactic acidosis and acidosis response in human cancers PLoS Genet 4 e1000293 2008 10.1371/journal.pgen.1000293 19057672 PMC2585811 · DOI
  10. [12]Mori K Rédini F Gouin F Cherrier B Heymann D Osteosarcoma: Current status of immunotherapy and future trends (Review) Oncol Rep 15 693 700 2006 16465432
  11. [13]Buddingh EP Kuijjer ML Duim RA Bürger H Agelopoulos K Myklebost O Serra M Mertens F Hogendoorn PC Lankester AC Cleton-Jansen AM Tumor-infiltrating macrophages are associated with metastasis suppression in high-grade osteosarcoma: A rationale for treatment with macrophage activating agents Clin Cancer Res 17 2110 2119 2011 10.1158/1078-0432.CCR-10-2047 21372215 · DOI · Paper page
  12. [14]Ratti C Botti L Cancila V Galvan S Torselli I Garofalo C Manara MC Bongiovanni L Valenti CF Burocchi A Trabectedin overrides osteosarcoma differentiative block and reprograms the tumor immune environment enabling effective combination with immune checkpoint inhibitors Clin Cancer Res 23 5149 5161 2017 10.1158/1078-0432.CCR-16-3186 28600479 · DOI
  13. [15]Kawano M Itonaga I Iwasaki T Tsumura H Enhancement of antitumor immunity by combining anti-cytotoxic T lymphocyte antigen-4 antibodies and cryotreated tumor lysate-pulsed dendritic cells in murine osteosarcoma Oncol Rep 29 1001 1006 2013 10.3892/or.2013.2224 23291864 · DOI · Paper page
  14. [16]Saraf AJ Fenger JM Roberts RD Osteosarcoma: Accelerating progress makes for a hopeful future Front Oncol 8 4 2018 10.3389/fonc.2018.00004 29435436 PMC5790793 · DOI
  15. [17]Wang Z Li B Ren Y Ye Z T-Cell-based immunotherapy for osteosarcoma: Challenges and opportunities Front Immunol 7 353 2016 10.3389/fimmu.2016.00353 27683579 PMC5021687 · DOI · Paper page
  16. [18]Miwa S Yamamoto N Hayashi K Takeuchi A Igarashi K Tsuchiya H Therapeutic targets for bone and soft-tissue sarcomas Int J Mol Sci 20 170 2019 10.3390/ijms20010170 PMC6337155 30621224 · DOI
  17. [19]Angelova M Charoentong P Hackl H Fischer ML Snajder R Krogsdam AM Waldner MJ Bindea G Mlecnik B Galon J Trajanoski Z Characterization of the immunophenotypes and antigenomes of colorectal cancers reveals distinct tumor escape mechanisms and novel targets for immunotherapy Genome Biol 16 64 2015 10.1186/s13059-015-0620-6 25853550 PMC4377852 · DOI
  18. [20]Li T Fan J Wang B Traugh N Chen Q Liu JS Li B Liu XS TIMER: A web server for comprehensive analysis of tumor-infiltrating immune cells Cancer Res 77 e108 e110 2017 10.1158/0008-5472.CAN-17-0307 29092952 PMC6042652 · DOI
  19. [21]Newman AM Liu CL Green MR Gentles AJ Feng W Xu Y Hoang CD Diehn M Alizadeh AA Robust enumeration of cell subsets from tissue expression profiles Nat Methods 12 453 457 2015 10.1038/nmeth.3337 25822800 PMC4739640 · DOI · Paper page
  20. [22]Xu Z Zhang Y Xu M Zheng X Lin M Pan J Ye C Deng Y Jiang C Lin Y Demethylation and overexpression of CSF2 are involved in immune response, chemotherapy resistance, and poor prognosis in colorectal cancer Onco Targets Ther 12 11255 11269 2019 10.2147/OTT.S216829 31908491 PMC6927609 · DOI
  21. [23]Pan JH Zhou H Cooper L Huang JL Zhu SB Zhao XX Ding H Pan YL Rong L LAYN is a prognostic biomarker and correlated with immune infiltrates in gastric and colon cancers Front Immunol 10 6 2019 10.3389/fimmu.2019.00006 30761122 PMC6362421 · DOI
  22. [24]Yang S Liu T Nan H Wang Y Chen H Zhang X Zhang Y Shen B Qian P Xu S Comprehensive analysis of prognostic immune-related genes in the tumor microenvironment of cutaneous melanoma J Cell Physiol 235 1025 1035 2020 10.1002/jcp.29018 31240705 · DOI
  23. [25]Shen Y Peng X Shen C Identification and validation of immune-related lncRNA prognostic signature for breast cancer Genomics 112 2640 2646 2020 10.1016/j.ygeno.2020.02.015 32087243 · DOI
  24. [26]Li R Qu H Wang S Wei J Zhang L Ma R Lu J Zhu J Zhong WD Jia Z GDCRNATools: An R/Bioconductor package for integrative analysis of lncRNA, miRNA and mRNA data in GDC Bioinformatics 34 2515 2517 2018 10.1093/bioinformatics/bty124 29509844 · DOI
  25. [28]Yoshihara K Shahmoradgoli M Martínez E Vegesna R Kim H Torres-Garcia W Treviño V Shen H Laird PW Levine DA Inferring tumour purity and stromal and immune cell admixture from expression data Nat Commun 4 2612 2013 10.1038/ncomms3612 24113773 PMC3826632 · DOI · Paper page
  26. [29]Hänzelmann S Castelo R Guinney J GSVA: Gene set variation analysis for microarray and RNA-seq data BMC Bioinformatics 14 7 2013 10.1186/1471-2105-14-7 23323831 PMC3618321 · DOI · Paper page
  27. [30]Therneau TM Grambsch PM Modeling Survival Data: Extending the Cox Model Springer New York, NY 2000 ISBN 0-387-98784-3 https://www.springer.com/gp/book/9780387987842# 10.1007/978-1-4757-3294-8 · DOI · Paper page
  28. [31]Ritchie ME Phipson B Wu D Hu Y Law CW Shi W Smyth GK limma powers differential expression analyses for RNA-sequencing and microarray studies Nucleic Acids Res 43 e47 2015 10.1093/nar/gkv007 25605792 PMC4402510 · DOI · Paper page
  29. [32]Yu G Wang LG Han Y He QY clusterProfiler: An R package for comparing biological themes among gene clusters OMICS 16 284 287 2012 10.1089/omi.2011.0118 22455463 PMC3339379 · DOI · Paper page
  30. [33]Shannon P Markiel A Ozier O Baliga NS Wang JT Ramage D Amin N Schwikowski B Ideker T Cytoscape: A software environment for integrated models of biomolecular interaction networks Genome Res 13 2498 2504 2003 10.1101/gr.1239303 14597658 PMC403769 · DOI · Paper page
  31. [34]Chin CH Chen SH Wu HH Ho CW Ko MT Lin CY cytoHubba: Identifying hub objects and sub-networks from complex interactome BMC Syst Biol 8 Suppl 4 S11 2014 10.1186/1752-0509-8-S4-S11 25521941 PMC4290687 · DOI
  32. [35]Friedman J Hastie T Tibshirani R Regularization paths for generalized linear models via coordinate descent J Stat Softw 33 1 22 2010 10.18637/jss.v033.i01 20808728 PMC2929880 · DOI · Paper page
  33. [37]Mootha VK Lindgren CM Eriksson KF Subramanian A Sihag S Lehar J Puigserver P Carlsson E Ridderstråle M Laurila E PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes Nat Genet 34 267 273 2003 10.1038/ng1180 12808457 · DOI · Paper page
  34. [38]Tang Z Li C Kang B Gao G Li C Zhang Z GEPIA: A web server for cancer and normal gene expression profiling and interactive analyses Nucleic Acids Res 45 W98 W102 2017 10.1093/nar/gkx247 28407145 PMC5570223 · DOI · Paper page
  35. [39]Ye Z Zeng Z Wang D Lei S Shen Y Chen Z Identification of key genes associated with the progression of intrahepatic cholangiocarcinoma using weighted gene co-expression network analysis Oncol Lett 20 483 494 2020 10.3892/ol.2020.11600 32565973 PMC7286119 · DOI
  36. [40]Tsukahara T Emori M Murata K Mizushima E Shibayama Y Kubo T Kanaseki T Hirohashi Y Yamashita T Sato N Torigoe T The future of immunotherapy for sarcoma Expert Opin Biol Ther 16 1049 1057 2016 10.1080/14712598.2016.1188075 27158940 · DOI
  37. [41]Wang SD Li HY Li BH Xie T Zhu T Sun LL Ren HY Ye ZM The role of CTLA-4 and PD-1 in anti-tumor immune response and their potential efficacy against osteosarcoma Int Immunopharmacol 38 81 89 2016 10.1016/j.intimp.2016.05.016 27258185 · DOI
  38. [43]Ehnman M Chaabane W Haglund F Tsagkozis P The tumor microenvironment of pediatric sarcoma: Mesenchymal mechanisms regulating cell migration and metastasis Curr Oncol Rep 21 90 2019 10.1007/s11912-019-0839-6 31418125 PMC6695368 · DOI
  39. [44]Zheng Y Wang G Chen R Hua Y Cai Z Mesenchymal stem cells in the osteosarcoma microenvironment: Their biological properties, influence on tumor growth, and therapeutic implications Stem Cell Res Ther 9 22 2018 10.1186/s13287-018-0780-x 29386041 PMC5793392 · DOI · Paper page
  40. [45]Scott MC Temiz NA Sarver AE LaRue RS Rathe SK Varshney J Wolf NK Moriarity BS O'Brien TD Spector LG Comparative transcriptome analysis quantifies immune cell transcript levels, metastatic progression, and survival in osteosarcoma Cancer Res 78 326 337 2018 10.1158/0008-5472.CAN-17-0576 29066513 PMC5935134 · DOI
  41. [46]Merchant MS Melchionda F Sinha M Khanna C Helman L Mackall CL Immune reconstitution prevents metastatic recurrence of murine osteosarcoma Cancer Immunol Immunother 56 1037 1046 2007 10.1007/s00262-006-0257-0 17149595 PMC11030906 · DOI
  42. [47]Merchant MS Bernstein D Amoako M Baird K Fleisher TA Morre M Steinberg SM Sabatino M Stroncek DF Venkatasan AM Adjuvant immunotherapy to improve outcome in high-risk pediatric sarcomas Clin Cancer Res 22 3182 3191 2016 10.1158/1078-0432.CCR-15-2550 26823601 PMC7831150 · DOI
  43. [48]Li X Gao Y Xu Z Zhang Z Zheng Y Qi F Identification of prognostic genes in adrenocortical carcinoma microenvironment based on bioinformatic methods Cancer Med 9 1161 1172 2020 10.1002/cam4.2774 31856409 PMC6997077 · DOI
  44. [49]Huang S Zhang B Fan W Zhao Q Yang L Xin W Fu D Identification of prognostic genes in the acute myeloid leukemia microenvironment Aging (Albany NY) 11 10557 10580 2019 10.18632/aging.102477 31740623 PMC6914404 · DOI
  45. [50]Schell TD Knowles BB Tevethia SS Sequential loss of cytotoxic T lymphocyte responses to simian virus 40 large T antigen epitopes in T antigen transgenic mice developing osteosarcomas Cancer Res 60 3002 3012 2000 10850449
  46. [51]Shen JK Cote GM Choy E Yang P Harmon D Schwab J Nielsen GP Chebib I Ferrone S Wang X Programmed cell death ligand 1 expression in osteosarcoma Cancer Immunol Res 2 690 698 2014 10.1158/2326-6066.CIR-13-0224 24866169 PMC4082476 · DOI
  47. [52]Lussier DM O'Neill L Nieves LM McAfee MS Holechek SA Collins AW Dickman P Jacobsen J Hingorani P Blattman JN Enhanced T-cell immunity to osteosarcoma through antibody blockade of PD-1/PD-L1 interactions J Immunother 38 96 106 2015 10.1097/CJI.0000000000000065 25751499 PMC6426450 · DOI · Paper page
  48. [53]Steinman RM Idoyaga J Features of the dendritic cell lineage Immunol Rev 234 5 17 2010 10.1111/j.0105-2896.2009.00888.x 20193008 · DOI
  49. [54]Yu Z Qian J Wu J Gao J Zhang M Allogeneic mRNA-based electrotransfection of autologous dendritic cells and specific antitumor effects against osteosarcoma in rats Med Oncol 29 3440 3448 2012 10.1007/s12032-012-0312-y 22843292 · DOI
  50. [55]Kawano M Tanaka K Itonaga I Iwasaki T Miyazaki M Ikeda S Tsumura H Dendritic cells combined with anti-GITR antibody produce antitumor effects in osteosarcoma Oncol Rep 34 1995 2001 2015 10.3892/or.2015.4161 26239052 · DOI · Paper page
  51. [56]Böttcher JP Bonavita E Chakravarty P Blees H Cabeza-Cabrerizo M Sammicheli S Rogers NC Sahai E Zelenay S Reis e Sousa C NK cells stimulate recruitment of cDC1 into the tumor microenvironment promoting cancer immune control Cell 172 1022 1037.e14 2018 10.1016/j.cell.2018.01.004 29429633 PMC5847168 · DOI · Paper page
  52. [57]Chang YH Connolly J Shimasaki N Mimura K Kono K Campana D A chimeric receptor with NKG2D specificity enhances natural killer cell activation and killing of tumor cells Cancer Res 73 1777 1786 2013 10.1158/0008-5472.CAN-12-3558 23302231 · DOI
  53. [58]Kiany S Huang G Kleinerman ES Effect of entinostat on NK cell-mediated cytotoxicity against osteosarcoma cells and osteosarcoma lung metastasis OncoImmunology 6 e1333214 2017 10.1080/2162402X.2017.1333214 28919994 PMC5593704 · DOI
  54. [59]Beauvillain C Delneste Y Scotet M Peres A Gascan H Guermonprez P Barnaba V Jeannin P Neutrophils efficiently cross-prime naive T cells in vivo Blood 110 2965 2973 2007 10.1182/blood-2006-12-063826 17562875 · DOI
  55. [60]Jablonska J Lang S Sionov RV Granot Z The regulation of pre-metastatic niche formation by neutrophils Oncotarget 8 112132 112144 2017 10.18632/oncotarget.22792 29340117 PMC5762385 · DOI
  56. [61]Zhao SJ Jiang YQ Xu NW Li Q Zhang Q Wang SY Li J Wang YH Zhang YL Jiang SH SPARCL1 suppresses osteosarcoma metastasis and recruits macrophages by activation of canonical WNT/β-catenin signaling through stabilization of the WNT-receptor complex Oncogene 37 1049 1061 2018 10.1038/onc.2017.403 29084211 PMC5851113 · DOI
  57. [62]Noy R Pollard JW Tumor-associated macrophages: From mechanisms to therapy Immunity 41 49 61 2014 10.1016/j.immuni.2014.09.021 25035953 PMC4137410 · DOI
  58. [63]Li R Shi Y Zhao S Shi T Zhang G NF-κB signaling and integrin-β1 inhibition attenuates osteosarcoma metastasis via increased cell apoptosis Int J Biol Macromol 123 1035 1043 2019 10.1016/j.ijbiomac.2018.11.003 30399378 · DOI
  59. [64]Shahi P Wang CY Chou J Hagerling C Gonzalez Velozo H Ruderisch A Yu Y Lai MD Werb Z GATA3 targets semaphorin 3B in mammary epithelial cells to suppress breast cancer progression and metastasis Oncogene 36 5567 5575 2017 10.1038/onc.2017.165 28581515 PMC5629104 · DOI
  60. [65]Si W Huang W Zheng Y Yang Y Liu X Shan L Zhou X Wang Y Su D Gao J Dysfunction of the reciprocal feedback loop between GATA3- and ZEB2-nucleated repression programs contributes to breast cancer metastasis Cancer Cell 27 822 836 2015 10.1016/j.ccell.2015.04.011 26028330 · DOI
  61. [66]Ma L Xue W Ma X GATA3 is downregulated in osteosarcoma and facilitates EMT as well as migration through regulation of slug Onco Targets Ther 11 7579 7589 2018 10.2147/OTT.S176534 30464506 PMC6214586 · DOI
  62. [67]Choi JW Herr DR Noguchi K Yung YC Lee CW Mutoh T Lin ME Teo ST Park KE Mosley AN Chun J LPA receptors: Subtypes and biological actions Annu Rev Pharmacol Toxicol 50 157 186 2010 10.1146/annurev.pharmtox.010909.105753 20055701 · DOI
  63. [68]Tsujiuchi T Araki M Hirane M Dong Y Fukushima N Lysophosphatidic acid receptors in cancer pathobiology Histol Histopathol 29 313 321 2014 24194373
  64. [69]Araki M Kitayoshi M Dong Y Hirane M Ozaki S Mori S Fukushima N Honoki K Tsujiuchi T Inhibitory effects of lysophosphatidic acid receptor-5 on cellular functions of sarcoma cells Growth Factors 32 117 122 2014 10.3109/08977194.2014.911294 24798396 · DOI
  65. [70]Dong Y Hirane M Araki M Fukushima N Honoki K Tsujiuchi T Lysophosphatidic acid receptor-5 negatively regulates cell motile and invasive activities of human sarcoma cell lines Mol Cell Biochem 393 17 22 2014 10.1007/s11010-014-2042-2 24676544 · DOI
  66. [71]Minami K Ueda N Ishimoto K Tsujiuchi T LPA5-mediated signaling induced by endothelial cells and anticancer drug regulates cellular functions of osteosarcoma cells Exp Cell Res 388 111813 2020 10.1016/j.yexcr.2020.111813 31904382 · DOI
  67. [72]Zjablovskaja P Kardosova M Danek P Angelisova P Benoukraf T Wurm AA Kalina T Sian S Balastik M Delwel R EVI2B is a C/EBPα target gene required for granulocytic differentiation and functionality of hematopoietic progenitors Cell Death Differ 24 705 716 2017 10.1038/cdd.2017.6 29991745 PMC6294764 · DOI
  68. [73]Matesanz-Isabel J Sintes J Llinàs L de Salort J Lázaro A Engel P New B-cell CD molecules Immunol Lett 134 104 112 2011 10.1016/j.imlet.2010.09.019 20933010 · DOI
  69. [74]Lafuente EM van Puijenbroek AA Krause M Carman CV Freeman GJ Berezovskaya A Constantine E Springer TA Gertler FB Boussiotis VA RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion Dev Cell 7 585 595 2004 10.1016/j.devcel.2004.07.021 15469846 · DOI
  70. [75]Patsoukis N Bardhan K Weaver JD Sari D Torres-Gomez A Li L Strauss L Lafuente EM Boussiotis VA The adaptor molecule RIAM integrates signaling events critical for integrin-mediated control of immune function and cancer progression Sci Signal 10 eaam8298 2017 10.1126/scisignal.aam8298 28831022 · DOI
  71. [76]Mace EM Monkley SJ Critchley DR Takei F A dual role for talin in NK cell cytotoxicity: Activation of LFA-1-mediated cell adhesion and polarization of NK cells J Immunol 182 948 956 2009 10.4049/jimmunol.182.2.948 19124737 · DOI
  72. [77]Meri T Amdahl H Lehtinen MJ Hyvärinen S McDowell JV Bhattacharjee A Meri S Marconi R Goldman A Jokiranta TS Microbes bind complement inhibitor factor H via a common site PLoS Pathog 9 e1003308 2013 10.1371/annotation/41169409-3260-4295-baf4-a1a4621a8e48 23637600 PMC3630169 · DOI
  73. [78]Bonavita E Gentile S Rubino M Maina V Papait R Kunderfranco P Greco C Feruglio F Molgora M Laface I PTX3 is an extrinsic oncosuppressor regulating complement-dependent inflammation in cancer Cell 160 700 714 2015 10.1016/j.cell.2015.01.004 25679762 · DOI
  74. [79]Corrales L Ajona D Rafail S Lasarte JJ Riezu-Boj JI Lambris JD Rouzaut A Pajares MJ Montuenga LM Pio R Anaphylatoxin C5a creates a favorable microenvironment for lung cancer progression J Immunol 189 4674 4683 2012 10.4049/jimmunol.1201654 23028051 PMC3478398 · DOI
  75. [80]Liu J Hoh J Loss of complement factor H in plasma increases endothelial cell migration J Cancer 8 2184 2190 2017 10.7150/jca.19452 28819420 PMC5560135 · DOI
  76. [81]Martin M Leffler J Smoląg KI Mytych J Björk A Chaves LD Alexander JJ Quigg RJ Blom AM Factor H uptake regulates intracellular C3 activation during apoptosis and decreases the inflammatory potential of nucleosomes Cell Death Differ 23 903 911 2016 10.1038/cdd.2015.164 26768663 PMC4832108 · DOI

Cited by

Sorted by citations

Authors
Yang, B., Su, Z., Chen, G., Zeng, Z., Tan, J., Wu, G., Zhu, S., & Lin, L.
Affiliations
  • Zhujiang Hospital (CN)
  • Southern Medical University (CN)
  • Putian University (CN)
  • Guiyang Medical University (CN)
Corresponding author
  • Zhu, Shuang
  • Lin, Lijun
ORCID
Venue
Oncology Letters
Publisher
Spandidos Publications
Published
2021-01-06
Volume
21
Issue
3
Pages
180-180
ISSN
  • 1792-1074 (ISSN-L)
  • 1792-1082
DOI
10.3892/ol.2021.12441
PMC
PMC7816295
OpenAlex
W3120376042
Cited by
36
References
4
Citations by year
2026: 2 · 2025: 6 · 2024: 6 · 2023: 9 · 2022: 5 · 2021: 8
FWCI
4.55
Type
journal article
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • Oncology Letters (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Sarcoma Diagnosis and Treatment
  • Health Sciences › Medicine › Rheumatology › Bone Tumor Diagnosis and Treatments
  • Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Keywords
osteosarcoma, metastasis, tumor immune infiltration, tumor microenvironment, prognostic factors, prognostic risk model, differentially expressed genes, tumor-infiltrating immune cells, natural killer cells, macrophage polarization, M2 macrophages, GATA3, LPAR5, RIAM, complement factor H

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review