Predicting the site of distant metastases in breast cancer

Автор: Grigoryeva E.S., Ivanyuk E.E., Choinzonov E.L., Cherdyntseva N.V.

Журнал: Сибирский онкологический журнал @siboncoj

Рубрика: Обзоры

Статья в выпуске: 1 т.22, 2023 года.

Бесплатный доступ

Background. Distant organ tumor dissemination is a major cause of breast cancer-related deaths. Breast cancer can metastasize to several organs, and the most frequent metastatic sites include the bones, lungs and liver. There is a question what factors can influence the direction of spread of tumor cells to a particular organ. Material and Methods. We summarized the data available in the world literature on methods for prediction of the localization of distant metastases in breast cancer patients. Results. We divided the factors associated with the localization of distant metastases into two main groups: clinicopathological parameters of breast cancer patients and molecular features of tumor microenvironment and tumor cells (primary tumor and circulating tumor cells) or its derivates - exosomes. From our point of view, the most powerful clinicopathological factor predicting the distant metastasis site is a molecular subtype of primary tumor. We can conclude that luminal (HR+/HER2-) tumors are often characterized by single metastases and bones are the most common metastatic site, while TNBC and HER2-enriched tumors often metastasize to multiple sites, most commonly brain and liver. However, several authors did not reveal these associations in their studies. It likely indicates the existence of other factors that significantly affect the organotropism of metastasis. Numerous studies demonstrate the association of different molecules expressed on tumor cells with organotropic metastasis. However, these data are very fragmentary and rather contradictory. Conclusion. The found associations are common to all participants of metastatic cascade, but remains unclear which factors are essential and crucial in determining the direction of metastasis.

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Breast cancer, hematogenous metastasis, prognostic predictors

Короткий адрес: https://sciup.org/140297839

IDR: 140297839   |   DOI: 10.21294/1814-4861-2023-22-1-151-158

Список литературы Predicting the site of distant metastases in breast cancer

  • Riggio A.I., Varley K.E., Welm A.L. The lingering mysteries of metastatic recurrence in breast cancer. Br J Cancer. 2021; 124(1): 13-26. https://doi.org/10.1038/s41416-020-01161-4.
  • Gomis R.R., Gawrzak S. Tumor cell dormancy. Mol Oncol. 2017; 11(1): 62-78. https://doi.org/10.1016/j.molonc.2016.09.009.
  • Malmgren J., Hurlbert M., Atwood M., Kaplan H.G. Examination of a paradox: recurrent metastatic breast cancer incidence decline without improved distant disease survival: 1990-2011. Breast Cancer Res Treat. 2019; 174(2): 505-14. https://doi.org/10.1007/s10549-018-05090-y.
  • Holleczek B., Stegmaier C., Radosa J.C., Solomayer E.F., Brenner H. Risk of loco-regional recurrence and distant metastases of patients with invasive breast cancer up to ten years after diagnosis - results from a registry-based study from Germany. BMC Cancer. 2019; 19(1): 520. https://doi.org/10.1186/s12885-019-5710-5.
  • Xiao W., Zheng S., Yang A., Zhang X., Zou Y., Tang H., Xie X. Breast cancer subtypes and the risk of distant metastasis at initial diagnosis: a population-based study. Cancer Manag Res. 2018; 10: 5329-38. https://doi.org/10.2147/CMAR.S176763.
  • Molnár I.A., Molnár B.Á., Vízkeleti L., Fekete K., Tamás J., Deák P., Szundi C., Székely B., Moldvay J., Vári-Kakas S., Szász M.A., Ács B., Kulka J., Tőkés A.M. Breast carcinoma subtypes show different patterns of metastatic behavior. Virchows Arch. 2017; 470(3): 275-83. https://doi.org/10.1007/s00428-017-2065-7.
  • Kunikullaya S.U., Poddar J., Sharma A.D., Patel S. Pattern of distant metastasis in molecular subtypes of carcinoma breast: An institutional study. Indian J Cancer. 2017; 54(1): 327-32. https://doi.org/10.4103/ijc.IJC_177_17.
  • Soni A., Ren Z., Hameed O., Chanda D., Morgan C.J., Siegal G.P., Wei S. Breast cancer subtypes predispose the site of distant metastases. Am J Clin Pathol. 2015; 143(4): 471-8. https://doi.org/10.1309/AJCPYO5FSV3UPEXS.
  • Diessner J., Wischnewsky M., Stüber T., Stein R., Krockenberger M., Häusler S., Janni W., Kreienberg R., Blettner M., Schwentner L., Wöckel A., Bartmann C. Evaluation of clinical parameters influencing the development of bone metastasis in breast cancer. BMC Cancer. 2016; 16: 307. https://doi.org/10.1186/s12885-016-2345-7.
  • Boutros C., Mazouni C., Lerebours F., Stevens D., Lei X., GonzalezAngulo A.M., Delaloge S. A preoperative nomogram to predict the risk of synchronous distant metastases at diagnosis of primary breast cancer. Br J Cancer. 2015; 112: 992-7. https://doi.org/10.1038/bjc.2015.34.
  • Ali B., Mubarik F., Zahid N., Sattar A.K. Clinicopathologic Features Predictive of Distant Metastasis in Patients Diagnosed With Invasive Breast Cancer. JCO Glob Oncol. 2020; 6: 1346-51. https://doi.org/10.1200/GO.20.00257.
  • Sopik V., Narod S.A. The relationship between tumour size, nodal status and distant metastases: on the origins of breast cancer. Breast Cancer Res Treat. 2018; 170(3): 647-56. https://doi.org/10.1007/s10549-018-4796-9.
  • Park H., Chang S.K., Kim J.Y., Lee B.M., Shin H.S. Risk factors for distant metastasis as a primary site of treatment failure in early-stage breast cancer. Chonnam Med J. 2014; 50(3): 96-101. https://doi.org/10.4068/cmj.2014.50.3.96.
  • Min Y., Liu X., Hu D., Chen H., Chen J., Xiang K., Yin G., Han Y., Feng Y., Luo H. Risk Factors, Prognostic Factors, and Nomogram for Distant Metastasis in Breast Cancer Patients Without Lymph Node Metastasis. Front Endocrinol (Lausanne). 2021; 12. https://doi.org/10.3389/fendo.2021.771226.
  • Yao Y., Chu Y., Xu B., Hu Q., Song Q. Risk factors for distant metastasis of patients with primary triple-negative breast cancer. Biosci Rep. 2019; 39(6). https://doi.org/10.1042/BSR20190288.
  • Chen M.T., Sun H.F., Zhao Y., Fu W.Y., Yang L.P., Gao S.P., Li L.D., Jiang H.L., Jin W. Comparison of patterns and prognosis among distant metastatic breast cancer patients by age groups: a SEER population-based analysis. Sci Rep. 2017; 7(1): 9254. https://doi.org/10.1038/s41598-017-10166-8.
  • Colzani E., Johansson A.L., Liljegren A., Foukakis T., Clements M., Adolfsson J., Hall P., Czene K. Time-dependent risk of developing dis- tant metastasis in breast cancer patients according to treatment, age and tumour characteristics. Br J Cancer. 2014; 110(5): 1378-84. https://doi.org/10.1038/bjc.2014.5.
  • Frank S., Carton M., Dubot C., Campone M., Pistilli B., Dalenc F., Mailliez A., Levy C., D’Hondt V., Debled M., Vermeulin T., Coudert B., Perrin C., Gonçalves A., Uwer L., Ferrero J.M., Eymard J.C., Petit T., Mouret-Reynier M.A., Patsouris A., Guesmia T., Bachelot T., Robain M., Cottu P. Impact of age at diagnosis of metastatic breast cancer on overall survival in the real-life ESME metastatic breast cancer cohort. Breast. 2020; 52: 50-7. https://doi.org/10.1016/j.breast.2020.04.009.
  • Purushotham A., Shamil E., Cariati M., Agbaje O., Muhidin A., Gillett C., Mera A., Sivanadiyan K., Harries M., Sullivan R., Pinder S.E., Garmo H., Holmberg L. Age at diagnosis and distant metastasis in breast cancer--a surprising inverse relationship. Eur J Cancer. 2014; 50(10): 1697-705. https://doi.org/10.1016/j.ejca.2014.04.002.
  • Hoshino A., Costa-Silva B., Shen T.L., Rodrigues G., Hashimoto A., Tesic Mark M., Molina H., Kohsaka S., Di Giannatale A., Ceder S., Singh S., Williams C., Soplop N., Uryu K., Pharmer L., King T., Bojmar L., Davies A.E., Ararso Y., Zhang T., Zhang H., Hernandez J., Weiss J.M., Dumont-Cole V.D., Kramer K., Wexler L.H., Narendran A., Schwartz G.K., Healey J.H., Sandstrom P., Labori K.J., Kure E.H., Grandgenett P.M., Hollingsworth M.A., de Sousa M., Kaur S., Jain M., Mallya K., Batra S.K., Jarnagin W.R., Brady M.S., Fodstad O., Muller V., Pantel K., Minn A.J., Bissell M.J., Garcia B.A., Kang Y., Rajasekhar V.K., Ghajar C.M., Matei I., Peinado H., Bromberg J., Lyden D. Tumour exosome integrins determine organotropic metastasis. Nature. 2015; 527(7578): 329-35. https://doi.org/10.1038/nature15756.
  • Sihto H., Lundin J., Lundin M., Lehtimäki T., Ristimäki A., Holli K., Sailas L., Kataja V., Turpeenniemi-Hujanen T., Isola J., Heikkilä P., Joensuu H. Breast cancer biological subtypes and protein expression pre- dict for the preferential distant metastasis sites: a nationwide cohort study. Breast Cancer Res. 2011; 13(5): R87. https://doi.org/10.1186/bcr2944.
  • McFarlane S., Coulter J.A., Tibbits P., O’Grady A., McFarlane C., Montgomery N., Hill A., McCarthy H.O., Young L.S., Kay E.W., Isacke C.M., Waugh D.J. CD44 increases the efficiency of distant metastasis of breast cancer. Oncotarget. 2015; 6(13): 11465-76. https://doi.org/10.18632/oncotar-get.3410.
  • Leontovich A.A., Jalalirad M., Salisbury J.L., Mills L., Haddox C., Schroeder M., Tuma A., Guicciardi M.E., Zammataro L., Gambino M.W., Amato A., Di Leonardo A., McCubrey J., Lange C.A., Liu M., Haddad T., Goetz M., Boughey J., Sarkaria J., Wang L., Ingle J.N., Galanis E., D’Assoro A.B. NOTCH3 expression is linked to breast cancer seeding and distant metastasis. Breast Cancer Res. 2018; 20(1): 105. https://doi.org/10.1186/s13058-018-1020-0.
  • Oshi M., Katsuta E., Yan L., Ebos J.M.L., Rashid O.M., Matsuy- ama R., Endo I., Takabe K. A Novel 4-Gene Score to Predict Survival, Distant Metastasis and Response to Neoadjuvant Therapy in Breast Cancer. Cancers (Basel). 2020; 12(5): 1148. https://doi.org/10.3390/cancers12051148.
  • Chen G.Y., Cheng J.C., Chen Y.F., Yang J.C., Hsu F.M. Circulating Exosomal Integrin β3 Is Associated with Intracranial Failure and Survival in Lung Cancer Patients Receiving Cranial Irradiation for Brain Metastases: A Prospective Observational Study. Cancers (Basel). 2021; 13(3): 380. https://doi.org/10.3390/cancers13030380.
  • Luo T., Huang J., Wu C., Huang Q., Zhong H., Qiu G., Liu Y., Liu J., Tang W. Cancer Exosome-derived Integrin α6 and Integrin β4 Promote Lung Metastasis of Colorectal Cancer. Research Square. 2020. https://doi.org/10.21203/rs.3.rs-91600/v1.
  • Zhang H., Deng T., Liu R., Bai M., Zhou L., Wang X., Li S., Wang X., Yang H., Li J., Ning T., Huang D., Li H., Zhang L., Ying G., Ba Y. Exosome- delivered EGFR regulates liver microenvironment to promote gastric can- cer liver metastasis. Nat Commun. 2017; 8. https://doi.org/10.1038/ncomms15016.
  • Costa-Silva B., Aiello N.M., Ocean A.J., Singh S., Zhang H., Thakur B.K., Becker A., Hoshino A., Mark M.T., Molina H., Xiang J., Zhang T., Theilen T.M., García-Santos G., Williams C., Ararso Y., Huang Y., Rodrigues G., Shen T.L., Labori K.J., Lothe I.M., Kure E.H., Hernandez J., Doussot A., Ebbesen S.H., Grandgenett P.M., Hollingsworth M.A., Jain M., Mallya K., Batra S.K., Jarnagin W.R., Schwartz R.E., Matei I., Peinado H., Stanger B.Z., Bromberg J., Lyden D. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015; 17(6): 816-26. https://doi.org/10.1038/ncb3169.
  • Sun J., Lu Z., Fu W., Lu K., Gu X., Xu F., Dai J., Yang Y., Jiang J. Exosome-Derived ADAM17 Promotes Liver Metastasis in Colorectal Cancer. Front Pharmacol. 2021; 12: 734351. https://doi.org/10.3389/fphar.2021.734351.
  • Zhang C., Wang X.Y., Zhang P., He T.C., Han J.H., Zhang R., Lin J., Fan J., Lu L., Zhu W.W., Jia H.L., Zhang J.B., Chen J.H. Cancer- derived exosomal HSPC111 promotes colorectal cancer liver metastasis by reprogramming lipid metabolism in cancer-associated fibroblasts. Cell Death Dis. 2022; 13(1): 57. https://doi.org/10.1038/s41419-022-04506-4.PM.
  • Tayoun T., Faugeroux V., Oulhen M., Aberlenc A., Pawlikowska P., Farace F. CTC-Derived Models: A Window into the Seeding Capacity of Circulating Tumor Cells (CTCs). Cells. 2019; 8(10): 1145. https://doi.org/10.3390/cells8101145.
  • Dianat-Moghadam H., Azizi M., Eslami-S Z., Cortés-Hernán- dez L.E., Heidarifard M., Nouri M., Alix-Panabières C. The Role of Circulating Tumor Cells in the Metastatic Cascade: Biology, Technical Challenges, and Clinical Relevance. Cancers (Basel). 2020; 12(4): 867. https://doi.org/10.3390/cancers12040867.
  • Chen Q., Zhang X.H., Massagué J. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell. 2011; 20(4): 538-49. https://doi.org/10.1016/j.ccr.2011.08.025.
  • McGowan P.M., Simedrea C., Ribot E.J., Foster P.J., Palmieri D., Steeg P.S., Allan A.L., Chambers A.F. Notch1 inhibition alters the CD44hi/ CD24lo population and reduces the formation of brain metastases from breast cancer. Mol Cancer Res. 2011; 9(7): 834-44. https://doi.org/10.1158/1541-7786.MCR-10-0457.
  • Zhong Y., Shen S., Zhou Y., Mao F., Lin Y., Guan J., Xu Y., Zhang S., Liu X., Sun Q. NOTCH1 is a poor prognostic factor for breast cancer and is associated with breast cancer stem cells. Onco Targets Ther. 2016; 9: 6865-71. https://doi.org/10.2147/OTT.S109606.
  • Miao K., Lei J.H., Valecha M.V., Zhang A., Xu J., Wang L., Lyu X., Chen S., Miao Z., Zhang X., Su S.M., Shao F., Rajendran B.K., Bao J., Zeng J., Sun H., Chen P., Tan K., Chen Q., Wong K.H., Xu X., Deng C.X. NOTCH1 activation compensates BRCA1 deficiency and promotes triple- negative breast cancer formation. Nat Commun. 2020; 11(1): 3256. https://doi.org/10.1038/s41467-020-16936-9.
  • Study Of MK-0752 In Combination With Tamoxifen Or Letrozole to Treat Early Stage Breast Cancer (MK-0752) [Internet]. ClinicalTrials. gov Identifier: NCT00756717. URL: https://www.clinicaltrials.gov [cited 2021].
  • Zhang L., Ridgway L.D., Wetzel M.D., Ngo J., Yin W., Kumar D., Goodman J.C., Groves M.D., Marchetti D. The identification and charac- terization of breast cancer CTCs competent for brain metastasis. Sci Transl Med. 2013; 5(180): 180ra48. https://doi.org/10.1126/scitranslmed.3005109. Erratum in: Sci Transl Med. 2013; 5(189): 189er5.
  • Klotz R., Thomas A., Teng T., Han S.M., Iriondo O., Li L., Re- strepo-Vassalli S., Wang A., Izadian N., MacKay M., Moon B.S., Liu K.J., Ganesan S.K., Lee G., Kang D.S., Walmsley C.S., Pinto C., Press M.F., Lu W., Lu J., Juric D., Bardia A., Hicks J., Salhia B., Attenello F., Smith A.D., Yu M. Circulating Tumor Cells Exhibit Metastatic Tropism and Reveal Brain Metastasis Drivers. Cancer Discov. 2020; 10(1): 86-103. https://doi.org/10.1158/2159-8290.CD-19-0384.
  • Clements M.E., Johnson R.W. PREX1 drives spontaneous bone dissemination of ER+ breast cancer cells. Oncogene. 2020; 39(6): 1318-34. https://doi.org/10.1038/s41388-019-1064-3.
  • Chen W., Hoffmann A.D., Liu H., Liu X. Organotropism: new in- sights into molecular mechanisms of breast cancer metastasis. NPJ Precis Oncol. 2018; 2(1): 4. https://doi.org/10.1038/s41698-018-0047-0.
  • Gil-Bernabé A.M., Ferjancic S., Tlalka M., Zhao L., Allen P.D., Im J.H., Watson K., Hill S.A., Amirkhosravi A., Francis J.L., Pollard J.W., Ruf W., Muschel R.J. Recruitment of monocytes/macrophages by tissue factor-mediated coagulation is essential for metastatic cell survival and premetastatic niche establishment in mice. Blood. 2012; 119(13): 3164-75. https://doi.org/10.1182/blood-2011-08-376426.
  • Najmeh S., Cools-Lartigue J., Rayes R.F., Gowing S., Vourtzoumis P., Bourdeau F., Giannias B., Berube J., Rousseau S., Ferri L.E., Spicer J.D. Neutrophil extracellular traps sequester circulating tumor cells via β1- integrin mediated interactions. Int J Cancer. 2017; 140(10): 2321-30. https://doi.org/10.1002/ijc.30635.
  • Cools-Lartigue J., Spicer J., McDonald B., Gowing S., Chow S., Giannias B., Bourdeau F., Kubes P., Ferri L. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J Clin Invest. 2013; 123(8): 3446-58. https://doi.org/10.1172/JCI67484.
  • Albrengues J., Shields M.A., Ng D., Park C.G., Ambrico A., Poindexter M.E., Upadhyay P., Uyeminami D.L., Pommier A., Küttner V., Bružas E., Maiorino L., Bautista C., Carmona E.M., Gimotty P.A., Fearon D.T., Chang K., Lyons S.K., Pinkerton K.E., Trotman L.C., Goldberg M.S., Yeh J.T., Egeblad M. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science. 2018; 361(6409). https://doi.org/10.1126/science.aao4227.
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