CoChat
Sign Up
Cited by 34Sarcoma Diagnosis and TreatmentCancer Cells and MetastasisCancer, Stress, Anesthesia, and Immune Response

Surgical Treatment of Osteosarcoma Induced Distant Pre‐Metastatic Niche in Lung to Facilitate the Colonization of Circulating Tumor Cells

Open access
Tang, Fan, Tie, Yan, Lan, Tian‐Xia, Yang, Jing‐Yun, Hong, Wei‐Qi, Chen, Si‐Yuan, Shi, Hou‐Hui, Li, Long‐Qing +5 more·2023·Advanced Science
DOI 10.1002/advs.202207518PMC PMC10558698
Open this paper in CoChat — free accountOpen PDF

Abstract

Recently, the major challenge in treating osteosarcoma patients is the metastatic disease, most commonly in the lungs. However, the underlying mechanism of recurrence and metastasis of osteosarcoma after surgical resection of primary tumor remains unclear. This study aims to investigate whether the pulmonary metastases characteristic of osteosarcoma is associated with surgical treatment and whether surgery contributes to the formation of pre‐metastatic niche in the distant lung tissue. In the current study, the authors observe the presence of circulating tumor cells in patients undergoing surgical resection of osteosarcoma which is correlated to tumor recurrence. The pulmonary infiltrations of neutrophils and Gr‐1 + myeloid cells are characterized to form a pre‐metastatic niche upon the exposure of circulating tumor cells after surgical resection. It is found that mitochondrial damage‐associated molecular patterns released from surgical resection contribute to the formation of pre‐metastatic niche in lung through IL‐1β secretion. This study reveals that surgical management for osteosarcoma, irrespective of the primary tumor, might promote the formation of postoperative pre‐metastatic niche in lung which is with important implications for developing rational therapies during peri‐operative period.

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 · 10.1002/advs.202207518

Cites

2 of 2 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?

  • M3-TAMs contribute to the metastasis and colonization of osteosarcoma cells in the lungs.

    “M3-TAMs contribute to the metastasis and colonization of osteosarcoma cells in the lungs [26], exacerbating the malignant progression of the tumor.”

    From Advances on immunotherapy for osteosarcoma (2024) · cites this paper as [26]

    The Discussion (page not provided) says that a surgery-induced lung niche facilitates the settlement of circulating osteosarcoma cells. It characterizes that niche by MDSC infiltration and mt-DAMP–induced IL-1β signaling, not by M3-TAMs. The specific attribution of a role to M3-TAMs is therefore unsupported. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

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: 54

  1. [1]a) W. H. Allum, S. P. Stenning, J. Bancewicz, P. I. Clark, R. E. Langley, J Clin Oncol 2009, 27, 5062; 19770374 b) R. Arriagada, A. Dunant, J. P. Pignon, B. Bergman, M. Chabowski, D. Grunenwald, M. Kozlowski, C. L. Péchoux, R. Pirker, M. I. Pinel, M. Tarayre, T. L. Chevalier, J Clin Oncol 2010, 28, 35. 19933916
  2. [2]S. Smeland, S. S. Bielack, J. Whelan, M. Bernstein, P. Hogendoorn, M. D. Krailo, R. Gorlick, K. A. Janeway, F. C. Ingleby, J. Anninga, I. Antal, C. Arndt, K. L. B. Brown, T. Butterfass‐Bahloul, G. Calaminus, M. Capra, C. Dhooge, M. Eriksson, A. M. Flanagan, G. Friedel, M. C. Gebhardt, H. Gelderblom, R. Goldsby, H. E. Grier, R. Grimer, D. S. Hawkins, S. Hecker‐Nolting, K. Sundby Hall, M. S. Isakoff, G. Jovic, et al., Eur J Cancer 2019, 109, 36. 30685685 PMC6506906
  3. [3]E. Thebault, S. Piperno‐Neumann, D. Tran, H. Pacquement, P. Marec‐Berard, C. Lervat, M. P. Castex, M. Cleirec, E. Bompas, J. P. Vannier, D. Plantaz, L. Saumet, C. Verite, O. Collard, C. Pluchart, C. Briandet, L. Monard, L. Brugieres, M. C. Le Deley, N. Gaspar, Cancers 2021, 1683, 10.3390/cancers13071683. PMC8038261 33918346 · DOI
  4. [4]L. Zhong, D. Liao, J. Li, W. Liu, J. Wang, C. Zeng, X. Wang, Z. Cao, R. Zhang, M. Li, K. Jiang, Y. X. Zeng, J. Sui, T. Kang, Signal Transduct Target Ther 2021, 6, 59. 33568623 PMC7876000
  5. [5]M. Nikanjam, S. Kato, R. Kurzrock, J. Hematol. Oncol. 2022, 15, 131. 36096847 PMC9465933
  6. [6]a) A. Chalopin, M. Tellez‐Gabriel, H. K. Brown, F. Vallette, M. F. Heymann, F. Gouin, D. Heymann, J Bone Oncol 2018, 12, 83; 30123735 PMC6092555 b) M. P. Johan, T. Kubo, T. Furuta, T. Sakuda, T. Sakaguchi, M. Nakanishi, M. Ochi, N. Adachi, J Orthop Res 2018, 36, 2562. 29637599
  7. [7]Y. Zhou, M. Han, J. Gao, J Control Release 2020, 325, 223. 32629136
  8. [8]a) Y. Liu, X. Cao, Cancer Cell 2016, 30, 668; 27846389 b) A. Deguchi, Y. Maru, Inflammation and Regeneration 2022, 42, 22. 35780158 PMC9250732
  9. [9]T. El Rayes, R. Catena, S. Lee, M. Stawowczyk, N. Joshi, C. Fischbach, C. A. Powell, A. J. Dannenberg, N. K. Altorki, D. Gao, V. Mittal, Proc. Natl. Acad. Sci. USA 2015, 112, 16000. 26668367 PMC4703007
  10. [10]a) K. L. Rock, J. J. Lai, H. Kono, Immunol Rev 2011, 243, 191; 21884177 PMC3170128 b) M. Huber‐Lang, J. D. Lambris, P. A. Ward, Nat. Immunol. 2018, 19, 327. 29507356 PMC6027646
  11. [11]A. Tiwari, Journal of clinical orthopaedics and trauma 2012, 3, 4. 25983449 PMC3872798
  12. [12]J. A. Krall, F. Reinhardt, O. A. Mercury, D. R. Pattabiraman, M. W. Brooks, M. Dougan, A. W. Lambert, B. Bierie, H. L. Ploegh, S. K. Dougan, R. A. Weinberg, Sci. Transl. Med. 2018, 10, 10.1126/scitranslmed.aan3464. PMC6364295 29643230 · DOI
  13. [13]S. Shalapour, M. Karin, J. Clin. Invest. 2015, 125, 3347. 26325032 PMC4588298
  14. [14]a) G. Shakhar, S. Ben‐Eliyahu, Annals of Surgical Oncology 2003, 10, 972; 14527919 b) F. Tang, Y. Tie, C. Tu, X. Wei, Clin. Transl. Med. 2020, 10, 199. 32508035 PMC7240866
  15. [15]J. Massagué, A. C. Obenauf, Nature 2016, 529, 298. 26791720 PMC5029466
  16. [16]a) N. Haga, A. Onagi, T. Koguchi, S. Hoshi, S. Ogawa, H. Akaihata, J. Hata, H. Hiraki, R. Honda, R. Tanji, K. Matsuoka, M. Kataoka, Y. Sato, K. Ishibashi, Y. Kojima, Annals of Surgical Oncology 2020, 27, 1272; 31832914 b) M. Tamminga, Clin Cancer Res 2020, 26, 1656. 31772122
  17. [17]K. W. Brudvik, L. T. Seeberg, H. Hugenschmidt, A. Renolen, C. B. Schirmer, C. Brunborg, B. A. Bjørnbeth, E. Borgen, B. Naume, A. Waage, G. Wiedswang, Annals of Surgical Oncology 2015, 22, 4029. 25801354
  18. [18]H. Peinado, H. Zhang, I. R. Matei, B. Costa‐Silva, A. Hoshino, G. Rodrigues, B. Psaila, R. N. Kaplan, J. F. Bromberg, Y. Kang, M. J. Bissell, T. R. Cox, A. J. Giaccia, J. T. Erler, S. Hiratsuka, C. M. Ghajar, D. Lyden, Nat Rev Cancer 2017, 17, 302. 28303905
  19. [19]M. R. Lewis, W. H. Cole, AMA Arch Surg 1958, 77, 621. 13582420
  20. [20]a) Z. Lu, J. Zou, S. Li, M. J. Topper, Y. Tao, H. Zhang, X. Jiao, W. Xie, X. Kong, M. Vaz, H. Li, Y. Cai, L. Xia, P. Huang, K. Rodgers, B. Lee, J. B. Riemer, C. P. Day, R. C. Yen, Y. Cui, Y. Wang, Y. Wang, W. Zhang, H. Easwaran, A. Hulbert, K. Kim, R. A. Juergens, S. C. Yang, R. J. Battafarano, E. L. Bush, et al., Nature 2020, 579, 284; 32103175 PMC8765085 b) F. Tang, Y. Tie, W. Hong, Y. Wei, C. Tu, X. Wei, Annals of Surgical Oncology 2020, 1, 4030. PMC7703739 33258011
  21. [21]R. Piranlioglu, E. Lee, M. Ouzounova, R. J. Bollag, A. H. Vinyard, A. S. Arbab, D. Marasco, M. Guzel, J. K. Cowell, M. Thangaraju, A. Chadli, K. A. Hassan, M. S. Wicha, E. Celis, H. Korkaya, Nat. Commun. 2019, 10, 1430. 30926774 PMC6441000
  22. [22]B. A. Smeester, N. J. Slipek, E. J. Pomeroy, K. Laoharawee, S. H. Osum, A. T. Larsson, K. B. Williams, N. Stratton, K. Yamamoto, J. J. Peterson, S. K. Rathe, L. J. Mills, W. A. Hudson, M. R. Crosby, M. Wang, E. P. Rahrmann, B. S. Moriarity, D. A. Largaespada, Bone 2020, 136, 115353. 32251854
  23. [23]J. M. Lord, M. J. Midwinter, Y. F. Chen, A. Belli, K. Brohi, E. J. Kovacs, L. Koenderman, P. Kubes, R. J. Lilford, Lancet 2014, 384, 1455. 25390327 PMC4729362
  24. [24]G. Y. Chen, G. Nuñez, Nat Rev Immunol 2010, 10, 826. 21088683 PMC3114424
  25. [25]X. Wei, B. Shao, Z. He, T. Ye, M. Luo, Y. Sang, X. Liang, W. Wang, S. Luo, S. Yang, S. Zhang, C. Gong, M. Gou, H. Deng, Y. Zhao, H. Yang, S. Deng, C. Zhao, L. Yang, Z. Qian, J. Li, X. Sun, J. Han, C. Jiang, M. Wu, Z. Zhang, Cell Res. 2015, 25, 237. 25613571 PMC4650577
  26. [26]a) D. Torre, G. Minoja, D. Maraggia, M. Chiaranda, R. Tambini, F. Speranza, M. Giola, Chest 1994, 105, 1241; 8162754 b) Y. Butt, A. Kurdowska, T. C. Allen, Arch Pathol 2016, 140, 345. 27028393
  27. [27]T. Brzoska, T. A. Luger, C. Maaser, C. Abels, M. Böhm, Endocr Rev 2008, 29, 581. 18612139
  28. [28]H. Patel, N. L. Marer, R. Q. Wharton, Z. A. Khan, R. Araia, C. Glover, M. M. Henry, T. G. Allen‐Mersh, Ann. Surg. 2002, 235, 226. 11807362 PMC1422418
  29. [29]M. M. Romsdahl, J Surg Res 1964, 4, 363. 14200440
  30. [30]L. Horváthová, V. Žárský, T. Pánek, R. Derelle, J. Pyrih, A. Motyčková, V. Klápšťová, M. Vinopalová, L. Marková, L. Voleman, V. Klimeš, M. Petrů, Z. Vaitová, I. Čepička, K. Hryzáková, K. Harant, M. W. Gray, M. Chami, I. Guilvout, O. Francetic, B. Franz Lang, Č. Vlček, A. D. Tsaousis, M. Eliáš, P. Doležal, Nat. Commun. 2021, 12, 2947. 34011950 PMC8134430
  31. [31]M. Marcatti, J. Saada, I. Okereke, C. E. Wade, S. H. Bossmann, M. Motamedi, B. Szczesny, Cells 2021, 10, 819. 33917426 PMC8067453
  32. [32]Q. Zhang, M. Raoof, Y. Chen, Y. Sumi, T. Sursal, W. Junger, K. Brohi, K. Itagaki, C. J. Hauser, Nature 2010, 464, 104. 20203610 PMC2843437
  33. [33]M. Hepokoski, J. Wang, K. Li, Y. Li, P. Gupta, T. Mai, A. Moshensky, M. Alotaibi, L. E. Crotty Alexander, A. Malhotra, P. Singh, American journal of physiology. Lung cellular and molecular physiology 2021, 320, L821. 33565357 PMC8174821
  34. [34]S. Sun, T. Sursal, Y. Adibnia, C. Zhao, Y. Zheng, H. Li, L. E. Otterbein, C. J. Hauser, K. Itagaki, PLoS One 2013, 8, e59989. 23527291 PMC3603956
  35. [35]L. S. Huang, Z. Hong, W. Wu, S. Xiong, M. Zhong, X. Gao, J. Rehman, A. B. Malik, Immunity 2020, 52, 475. 32164878 PMC7266657
  36. [36]a) A. Cheng, C. E. Vantucci, L. Krishnan, M. A. Ruehle, T. Kotanchek, L. B. Wood, K. Roy, R. E. Guldberg, Proc. Natl. Acad. Sci. USA 2021, 118, e2017889118; 33597299 PMC7923361 b) C. E. Vantucci, H. Ahn, T. Fulton, M. L. Schenker, P. Pradhan, L. B. Wood, R. E. Guldberg, K. Roy, N. J. Willett, Biomaterials 2021, 264, 120405. 33069135 PMC8117743
  37. [37]M. Rahman, S. Zhang, M. Chew, A. Ersson, B. Jeppsson, H. Thorlacius, Ann. Surg. 2009, 250, 783. 19806052
  38. [38]V. S. Pelly, A. Moeini, L. M. Roelofsen, E. Bonavita, C. R. Bell, C. Hutton, A. Blanco‐Gomez, A. Banyard, C. P. Bromley, E. Flanagan, S. C. Chiang, C. Jørgensen, T. N. Schumacher, D. S. Thommen, S. Zelenay, Cancer discovery 2021, 2602, 10.1158/2159-8290.cd-20-1815. 34031121 PMC7611767 · DOI
  39. [39]J. Xu, J. Guardado, R. Hoffman, H. Xu, R. Namas, Y. Vodovotz, L. Xu, M. Ramadan, J. Brown, H. R. Turnquist, T. R. Billiar, PLoS Med. 2017, 14, e1002365. 28742815 PMC5526517
  40. [40]S. L. Highfill, Y. Cui, A. J. Giles, J. P. Smith, H. Zhang, E. Morse, R. N. Kaplan, C. L. Mackall, Sci. Transl. Med. 2014, 6, 237ra67. PMC6980372 24848257
  41. [41]a) Z. Xie, B. Wu, Y. Liu, W. Ren, L. Tong, C. Xiang, A. Wei, Y. Gao, L. Zeng, H. Xie, W. Tang, Y. Hu, J. Med. Chem. 2020, 63, 1397; 31934767 b) D. Kokona, A. Ebneter, P. Escher, M. S. Zinkernagel, J Neuroinflammation 2018, 15, 340; 30541565 PMC6292111 c) C. Barca, A. J. Kiliaan, C. Foray, L. Wachsmuth, S. Hermann, C. Faber, M. Schaefers, M. Wiesmann, A. H. Jacobs, B. Zinnhardt, Society of Nuclear Medicine 2021, 446, 10.2967/jnumed.121.262279. PMC8978197 34168016 · DOI
  42. [42]Y. Sun, L. Yang, X. Hao, Y. Liu, J. Zhang, Z. Ning, Y. Shi, J. Hematol. Oncol. 2019, 12, 9. 30642372 PMC6332596
  43. [43]T. Fujiwara, M. A. Yakoub, A. Chandler, A. B. Christ, G. Yang, O. Ouerfelli, V. K. Rajasekhar, A. Yoshida, H. Kondo, T. Hata, H. Tazawa, Y. Dogan, M. A. S. Moore, T. Fujiwara, T. Ozaki, E. Purdue, J. H. Healey, Mol. Cancer Ther. 2021, 20, 1388. 34088832 PMC9336538
  44. [44]A. Weber, P. Wasiliew, M. Kracht, Sci. Signaling 2010, 3, cm2. 20086236
  45. [45]J. A. Meyerhardt, Q. Shi, C. S. Fuchs, J. Meyer, D. Niedzwiecki, T. Zemla, P. Kumthekar, K. A. Guthrie, F. Couture, P. Kuebler, J. C. Bendell, P. Kumar, D. Lewis, B. Tan, M. Bertagnolli, A. Grothey, H. S. Hochster, R. M. Goldberg, A. Venook, C. Blanke, E. M. O'Reilly, A. F. Shields, JAMA, J. Am. Med. Assoc. 2021, 325, 1277. PMC8025124 33821899
  46. [46]M. Xu, K. Hu, Y. Liu, Y. Huang, S. Liu, Y. Chen, D. Wang, S. Zhou, Q. Zhang, N. Mei, H. Lu, F. Li, X. Gao, J. Chen, Nat. Commun. 2021, 12, 3187. 34045459 PMC8160269
  47. [47]H. M. Hsiao, R. Fernandez, S. Tanaka, W. Li, J. H. Spahn, S. Chiu, M. Akbarpour, D. Ruiz‐Perez, Q. Wu, C. Turam, D. Scozzi, T. Takahashi, H. P. Luehmann, V. Puri, G. R. S. Budinger, A. S. Krupnick, A. V. Misharin, K. J. Lavine, Y. Liu, A. E. Gelman, A. Bharat, D. Kreisel, J. Clin. Invest. 2018, 128, 2833. 29781811 PMC6025976
  48. [48]S. Xiong, Z. Hong, L. S. Huang, Y. Tsukasaki, S. Nepal, A. Di, M. Zhong, W. Wu, Z. Ye, X. Gao, G. N. Rao, D. Mehta, J. Rehman, A. B. Malik, J. Clin. Invest. 2020, 130, 3684. 32298238 PMC7324198
  49. [49]B. M. Everett, J. G. MacFadyen, T. Thuren, P. Libby, R. J. Glynn, P. M. Ridker, J. Am. Coll. Cardiol. 2020, 76, 1660. 33004131
  50. [50]I. Kaplanov, Y. Carmi, R. Kornetsky, A. Shemesh, G. V. Shurin, M. R. Shurin, C. A. Dinarello, E. Voronov, R. N. Apte, Proc. Natl. Acad. Sci. USA 2019, 116, 1361. 30545915 PMC6347724
  51. [51]P. Xu, P. Zhang, Z. Sun, Y. Wang, J. Chen, C. Miao, Cancer Immunol. Immunother. 2015, 64, 1383. 26183035 PMC11028497
  52. [52]M. S. Kim, S. Y. Lee, T. R. Lee, W. H. Cho, W. S. Song, J. S. Koh, J. A. Lee, J. Y. Yoo, D. G. Jeon, Medical Oncology 2009, 20, 955. 19153123
  53. [53]M. S. Kim, W. H. Cho, W. S. Song, S. Y. Lee, D. G. Jeon, Clin. Orthop. Relat. Res. 2007, 463, 157. 17621233
  54. [54]a) M. Li, Y. Lu, Z. Long, M. Li, J. Kong, G. Chen, Z. Wang, J Bone Oncol 2019, 16, 100236; 31024791 PMC6475710 b) Y. Tang, Y. Lu, Y. Chen, L. Luo, L. Cai, B. Peng, W. Huang, H. Liao, L. Zhao, M. Pan, Journal of Experimental & cLinical Cancer Research: CR 2019, 38, 473. 31752959 PMC6873584

Cited by

Sorted by citations

Authors
Tang, F., Tie, Y., Lan, T., Yang, J., Hong, W., Chen, S., Shi, H., Li, L., Zeng, H., Min, L., Wei, Y., Tu, C., & Wei, X.
Affiliations
  • Sichuan University (CN)
  • Laboratory of Aging Research and Cancer Drug Target State Key Laboratory of Biotherapy National Clinical Research Center for Geriatrics West China Hospital Sichuan University No. 17, Block 3, Southern Renmin Road Chengdu Sichuan 610041 People's Republic of China
  • Department of Orthopedics Orthopedic Research Institute West China Hospital Sichuan University No. 17, Block 3, Southern Renmin Road Chengdu Sichuan 610041 People's Republic of China
ORCID
Venue
Advanced Science
Publisher
Wiley
Published
2023-08-16
Volume
10
Issue
28
Pages
e2207518-e2207518
ISSN
2198-3844 (ISSN-L)
DOI
10.1002/advs.202207518
PMC
PMC10558698
OpenAlex
W4385897339
Cited by
34
References
2
Citations by year
2026: 8 · 2025: 18 · 2024: 7 · 2023: 1
FWCI
6.24
Type
journal article
Language
en
Open access
Licence
Locations
  • Advanced Science (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Natural Science Foundation of China (82002847)
Topics
  • Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Sarcoma Diagnosis and Treatment
  • Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
  • Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
Keywords
osteosarcoma, pre-metastatic niche, lung metastasis, circulating tumor cells, surgical resection, tumor recurrence, neutrophils, mitochondrial damage-associated molecular patterns, IL-1β, perioperative therapy
MeSH terms
Adolescent, Adult, Bone Neoplasms, Female, Humans, Lung, Lung Neoplasms, Male, Neoplastic Cells, Circulating, Neoplasm Recurrence, Local, Osteosarcoma, Tumor Microenvironment

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