Organ tropism in solid tumor metastasis: an updated review

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References

• 1. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Migrating cancer stem cells – an integrated concept of malignant tumour progression. Nat. Rev. Cancer 5(9), 744–749 (2005).
  Medline CASGoogle Scholar
• 2. Kim YH, Choi YW, Lee J, Soh EY, Kim JH, Park TJ. Senescent tumor cells lead the collective invasion in thyroid cancer. Nat. Commun. 8, 15208 (2017).
  MedlineGoogle Scholar
• 3. Fares J, Fares MY, Khachfe HH, Salhab HA, Fares Y. Molecular principles of metastasis: a hallmark of cancer revisited. Signal Transduct. Target. Ther. 5(1), 28 (2020).
  MedlineGoogle Scholar
• 4. Obradović MMS, Hamelin B, Manevski N et al. Glucocorticoids promote breast cancer metastasis. Nature 567(7749), 540–544 (2019).
  Medline CASGoogle Scholar
• 5. Guo F, Wang Y, Liu J, Mok SC, Xue F, Zhang W. CXCL12/CXCR4: a symbiotic bridge linking cancer cells and their stromal neighbors in oncogenic communication networks. Oncogene 35(7), 816–826 (2016).
  Medline CASGoogle Scholar
• 6. Birkbak NJ, McGranahan N. Cancer genome evolutionary trajectories in metastasis. Cancer Cell 37(1), 8–19 (2020).
  Medline CASGoogle Scholar
• 7. Tang Q, Su Z, Gu W, Rustgi AK. Mutant p53 on the path to metastasis. Trends Cancer 6(1), 62–73 (2020).
  MedlineGoogle Scholar
• 8. Baek AE, Yu YA, He S et al. The cholesterol metabolite 27 hydroxycholesterol facilitates breast cancer metastasis through its actions on immune cells. Nat. Commun. 8(1), 864 (2017).
  MedlineGoogle Scholar
• 9. Yu X, Chen L, Liu J et al. Immune modulation of liver sinusoidal endothelial cells by melittin nanoparticles suppresses liver metastasis. Nat. Commun. 10(1), 574 (2019).
  Medline CASGoogle Scholar
• 10. Leslie PL, Chao YL, Tsai YH et al. Histone deacetylase 11 inhibition promotes breast cancer metastasis from lymph nodes. Nat. Commun. 10(1), 4192 (2019).
  MedlineGoogle Scholar
• 11. Wang X, Liu R, Zhu W et al. UDP-glucose accelerates SNAI1 mRNA decay and impairs lung cancer metastasis. Nature 571(7763), 127–131 (2019).
  Medline CASGoogle Scholar
• 12. Lin B, Li Y, Wang T et al. CRMP2 is a therapeutic target that suppresses the aggressiveness of breast cancer cells by stabilizing RECK. Oncogene 39(37), 6024–6040 (2020).
  Medline CASGoogle Scholar
• 13. Follain G, Herrmann D, Harlepp S et al. Fluids and their mechanics in tumour transit: shaping metastasis. Nat. Rev. Cancer 20(2), 107–124 (2020).
  Medline CASGoogle Scholar
• 14. Zhang Z, Li J, Ou Y et al. CDK4/6 inhibition blocks cancer metastasis through a USP51–ZEB1-dependent deubiquitination mechanism. Signal Transduct. Target. Ther. 5(1), 25 (2020).
  Medline CASGoogle Scholar
• 15. Strilic B, Offermanns S. Intravascular survival and extravasation of tumor cells. Cancer Cell 32(3), 282–293 (2017).
  Medline CASGoogle Scholar
• 16. Anderson RL, Balasas T, Callaghan J et al. A framework for the development of effective anti-metastatic agents. Nat. Rev. Clin. Oncol. 16(3), 185–204 (2019).
  MedlineGoogle Scholar
• 17. Zhang W, Bado I, Wang H, Lo HC, Zhang XH. Bone metastasis: find your niche and fit in. Trends Cancer 5(2), 95–110 (2019).
  MedlineGoogle Scholar
• 18. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 8(2), 98–101 (1889).
  Google Scholar
• 19. Boire A, Brastianos PK, Garzia L, Valiente M. Brain metastasis. Nat. Rev. Cancer 20(1), 4–11 (2020).
  Medline CASGoogle Scholar
• 20. Achrol AS, Rennert RC, Anders C et al. Brain metastases. Nat. Rev. Dis. Primers 5(1), 5 (2019).
  MedlineGoogle Scholar
• 21. Tsao MN, Xu W, Wong RK et al. Whole brain radiotherapy for the treatment of newly diagnosed multiple brain metastases. Cochrane Database Syst. Rev. 1(1), CD003869 (2018).
  MedlineGoogle Scholar
• 22. Suh JH, Kotecha R, Chao ST, Ahluwalia MS, Sahgal A, Chang EL. Current approaches to the management of brain metastases. Nat. Rev. Clin. Oncol. 17(5), 279–299 (2020).
  MedlineGoogle Scholar
• 23. Sprowls SA, Arsiwala TA, Bumgarner JR et al. Improving CNS delivery to brain metastases by blood–tumor barrier disruption. Trends Cancer 5(8), 495–505 (2019).
  Medline CASGoogle Scholar
• 24. Mulvenna P, Nankivell M, Barton R et al. Dexamethasone and supportive care with or without whole brain radiotherapy in treating patients with non-small cell lung cancer with brain metastases unsuitable for resection or stereotactic radiotherapy (QUARTZ): results from a Phase 3, non-inferiority, randomised trial. Lancet 388(10055), 2004–2014 (2016).
  Medline CASGoogle Scholar
• 25. Altorki NK, Markowitz GJ, Gao D et al. The lung microenvironment: an important regulator of tumour growth and metastasis. Nat. Rev. Cancer 19(1), 9–31 (2019).
  Medline CASGoogle Scholar
• 26. Brown PD, Ballman KV, Cerhan JH et al. Postoperative stereotactic radiosurgery compared with whole brain radiotherapy for resected metastatic brain disease (NCCTG N107C/CEC·3): a multicentre, randomised, controlled, Phase 3 trial. Lancet Oncol. 18(8), 1049–1060 (2017).
  MedlineGoogle Scholar
• 27. Steeg PS, Camphausen KA, Smith QR. Brain metastases as preventive and therapeutic targets. Nat. Rev. Cancer 11(5), 352–363 (2011).
  Medline CASGoogle Scholar
• 28. Chung B, Esmaeili AA, Gopalakrishna-Pillai S et al. Human brain metastatic stroma attracts breast cancer cells via chemokines CXCL16 and CXCL12. NPJ Breast Cancer 3, 6 (2017).
  MedlineGoogle Scholar
• 29. Liu J, Li J, Li P et al. DLG5 suppresses breast cancer stem cell-like characteristics to restore tamoxifen sensitivity by inhibiting TAZ expression. J. Cell. Mol. Med. 23(1), 512–521 (2019).
  Medline CASGoogle Scholar
• 30. Zeng Q, Michael IP, Zhang P et al. Synaptic proximity enables NMDAR signalling to promote brain metastasis. Nature 573(7775), 526–531 (2019).
  Medline CASGoogle Scholar
• 31. Cheng G, Zhang Q, Pan J et al. Targeting lonidamine to mitochondria mitigates lung tumorigenesis and brain metastasis. Nat. Commun. 10(1), 2205 (2019).
  MedlineGoogle Scholar
• 32. Soffietti R, Ahluwalia M, Lin N, Rudà R. Management of brain metastases according to molecular subtypes. Nat. Rev. Neurol. 16(10), 557–574 (2020).
  Medline CASGoogle Scholar
• 33. Brown PD, Jaeckle K, Ballman KV et al. Effect of radiosurgery alone vs radiosurgery with whole brain radiation therapy on cognitive function in patients with 1 to 3 brain metastases: a randomized clinical trial. JAMA 316(4), 401–409 (2016).
  MedlineGoogle Scholar
• 34. O’Melia MJ, Lund AW, Thomas SN. The biophysics of lymphatic transport: engineering tools and immunological consequences. iScience 22, 28–43 (2019).
  MedlineGoogle Scholar
• 35. Naxerova K, Reiter JG, Brachtel E et al. Origins of lymphatic and distant metastases in human colorectal cancer. Science 357(6346), 55–60 (2017).
  Medline CASGoogle Scholar
• 36. Pelon F, Bourachot B, Kieffer Y et al. Cancer-associated fibroblast heterogeneity in axillary lymph nodes drives metastases in breast cancer through complementary mechanisms. Nat. Commun. 11(1), 404 (2020).
  Medline CASGoogle Scholar
• 37. Fukumura D, Kloepper J, Amoozgar Z, Duda DG, Jain RK. Enhancing cancer immunotherapy using antiangiogenics: opportunities and challenges. Nat. Rev. Clin. Oncol. 15(5), 325–340 (2018).
  Medline CASGoogle Scholar
• 38. Brown M, Assen FP, Leithner A et al. Lymph node blood vessels provide exit routes for metastatic tumor cell dissemination in mice. Science 359(6382), 1408–1411 (2018).
  Medline CASGoogle Scholar
• 39. Pereira ER, Kedrin D, Seano G et al. Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice. Science 359(6382), 1403–1407 (2018).
  Medline CASGoogle Scholar
• 40. Horton BL, Fessenden TB, Spranger S. Tissue site and the cancer immunity cycle. Trends Cancer 5(10), 593–603 (2019).
  Medline CASGoogle Scholar
• 41. Jalkanen S, Salmi M. Lymphatic endothelial cells of the lymph node. Nat. Rev. Immunol. 20(9), 566–578 (2020).
  Medline CASGoogle Scholar
• 42. Jain RK, Martin JD, Stylianopoulos T. The role of mechanical forces in tumor growth and therapy. Annu. Rev. Biomed. Eng. 16, 321–346 (2014).
  Medline CASGoogle Scholar
• 43. Mortezaee K. Hypoxia induces core-to-edge transition of progressive tumoral cells: a critical review on differential yet corroborative roles for HIF-1α and HIF-2α. Life Sci. 242, 117145 (2020). • Outlines a new concept in tumor resistance and progression: the hypoxia-inducible effect on the transition of tumor cells from the interior toward the invasive front of the tumor.
  Medline CASGoogle Scholar
• 44. Najafi M, Farhood B, Mortezaee K, Kharazinejad E, Majidpoor J, Ahadi R. Hypoxia in solid tumors: a key promoter of cancer stem cell (CSC) resistance. J. Cancer Res. Clin. Oncol. 146(1), 19–31 (2020). • Focuses on the mechanisms by which hypoxia acts for promoting cancer stem cell resistance in tumors of solid organs.
  MedlineGoogle Scholar
• 45. Wang L, Simons DL, Lu X et al. Breast cancer induces systemic immune changes on cytokine signaling in peripheral blood monocytes and lymphocytes. EBioMedicine 52, 102631 (2020).
  MedlineGoogle Scholar
• 46. Li C, Wang S, Xing Z et al. A ROR1–HER3–lncRNA signalling axis modulates the Hippo–YAP pathway to regulate bone metastasis. Nat. Cell Biol. 19(2), 106–119 (2017).
  Medline CASGoogle Scholar
• 47. Zuo H, Yang D, Yang Q, Tang H, Fu YX, Wan Y. Differential regulation of breast cancer bone metastasis by PARP1 and PARP2. Nat. Commun. 11(1), 1578 (2020).
  Medline CASGoogle Scholar
• 48. Buschhaus JM, Humphries BA, Eckley SS et al. Targeting disseminated estrogen-receptor-positive breast cancer cells in bone marrow. Oncogene 1–14 (2020).
  Google Scholar
• 49. Berish RB, Ali AN, Telmer PG, Ronald JA, Leong HS. Translational models of prostate cancer bone metastasis. Nat. Rev. Urol. 15(7), 403–421 (2018).
  Medline CASGoogle Scholar
• 50. Jiao S, Subudhi SK, Aparicio A et al. Differences in tumor microenvironment dictate T helper lineage polarization and response to immune checkpoint therapy. Cell 179(5), 1177–1190.e13 (2019).
  Medline CASGoogle Scholar
• 51. Romero-Moreno R, Curtis KJ, Coughlin TR et al. The CXCL5/CXCR2 axis is sufficient to promote breast cancer colonization during bone metastasis. Nat. Commun. 10(1), 4404 (2019).
  MedlineGoogle Scholar
• 52. Yang Z, Yue Z, Ma X, Xu Z. Calcium homeostasis: a potential vicious cycle of bone metastasis in breast cancers. Front. Oncol. 10, 293 (2020).
  MedlineGoogle Scholar
• 53. Lynch CC. Matrix metalloproteinases as master regulators of the vicious cycle of bone metastasis. Bone 48(1), 44–53 (2011).
  Medline CASGoogle Scholar
• 54. Teng S, Li YE, Yang M et al. Tissue-specific transcription reprogramming promotes liver metastasis of colorectal cancer. Cell Res. 30(1), 34–49 (2020).
  Medline CASGoogle Scholar
• 55. Scimeca M, Bonfiglio R, Urbano N, Schillaci O, Bonanno E. Adjuvant denosumab in early breast cancer. Lancet Oncol. 21(3), e122 (2020).
  MedlineGoogle Scholar
• 56. Wang S, Li GX, Tan CC et al. FOXF2 reprograms breast cancer cells into bone metastasis seeds. Nat. Commun. 10(1), 2707 (2019).
  MedlineGoogle Scholar
• 57. Colden M, Dar AA, Saini S et al. MicroRNA-466 inhibits tumor growth and bone metastasis in prostate cancer by direct regulation of osteogenic transcription factor RUNX2. Cell Death Dis. 8(1), e2572–e2572 (2018).
  Google Scholar
• 58. Ji Q, Zhou L, Sui H et al. Primary tumors release ITGBL1-rich extracellular vesicles to promote distal metastatic tumor growth through fibroblast-niche formation. Nat. Commun. 11(1), 1211 (2020).
  Medline CASGoogle Scholar
• 59. Valkenburg KC, de Groot AE, Pienta KJ. Targeting the tumour stroma to improve cancer therapy. Nat. Rev. Clin. Oncol. 15(6), 366–381 (2018).
  MedlineGoogle Scholar
• 60. Mortezaee K, Potes Y, Mirtavoos-Mahyari H et al. Boosting immune system against cancer by melatonin: a mechanistic viewpoint. Life Sci. 238, 116960 (2019).
  Medline CASGoogle Scholar
• 61. Mortezaee K, Parwaie W, Motevaseli E et al. Targets for improving tumor response to radiotherapy. Int. Immunopharmacol. 76, 105847 (2019).
  Medline CASGoogle Scholar
• 62. Coleman RE, Brown J, Holen I. Bone metastases. In: Abeloff's Clinical Oncology. 809–830. e3 (2020).
  Google Scholar
• 63. Croucher PI, McDonald MM, Martin TJ. Bone metastasis: the importance of the neighbourhood. Nat. Rev. Cancer 16(6), 373–386 (2016).
  Medline CASGoogle Scholar
• 64. Steeg PS. Targeting metastasis. Nat. Rev. Cancer 16(4), 201–218 (2016).
  Medline CASGoogle Scholar
• 65. Esposito M, Mondal N, Greco TM et al. Bone vascular niche E-selectin induces mesenchymal–epithelial transition and Wnt activation in cancer cells to promote bone metastasis. Nat. Cell Biol. 21(5), 627–639 (2019).
  Medline CASGoogle Scholar
• 66. Takahashi N, Chen HY, Harris IS et al. Cancer cells co-opt the neuronal redox-sensing channel TRPA1 to promote oxidative-stress tolerance. Cancer Cell 33(6), 985–1003.e7 (2018).
  Medline CASGoogle Scholar
• 67. Macedo F, Ladeira K, Pinho F et al. Bone metastases: an overview. Oncol. Rev. 11(1), 321 (2017).
  MedlineGoogle Scholar
• 68. Lee JW, Stone ML, Porrett PM et al. Hepatocytes direct the formation of a pro-metastatic niche in the liver. Nature 567(7747), 249–252 (2019).
  Medline CASGoogle Scholar
• 69. Yamaguchi N, Weinberg EM, Nguyen A et al. PCK1 and DHODH drive colorectal cancer liver metastatic colonization and nucleotide biosynthesis under hypoxia. bioRxiv 833186 (2019).
  Google Scholar
• 70. Chen RX, Chen X, Xia LP et al. N 6-methyladenosine modification of circNSUN2 facilitates cytoplasmic export and stabilizes HMGA2 to promote colorectal liver metastasis. Nat. Commun. 10(1), 4695 (2019).
  MedlineGoogle Scholar
• 71. Brodt P. Role of the microenvironment in liver metastasis: from pre-to prometastatic niches. Clin. Cancer Res. 22(24), 5971–5982 (2016).
  Medline CASGoogle Scholar
• 72. Hu M, Wang Y, Xu L et al. Relaxin gene delivery mitigates liver metastasis and synergizes with check point therapy. Nat. Commun. 10(1), 2993 (2019).
  MedlineGoogle Scholar
• 73. Liu Y, Crowe WN, Wang L et al. An inhalable nanoparticulate STING agonist synergizes with radiotherapy to confer long-term control of lung metastases. Nat. Commun. 10(1), 5108 (2019).
  Medline CASGoogle Scholar
• 74. Gui J, Zahedi F, Ortiz A et al. Activation of p38α stress-activated protein kinase drives the formation of the pre-metastatic niche in the lungs. Nat. Cancer 1, 603–619 (2020).
  MedlineGoogle Scholar
• 75. Aytes A, Giacobbe A, Mitrofanova A et al. NSD2 is a conserved driver of metastatic prostate cancer progression. Nat. Commun. 9(1), 5201 (2018).
  MedlineGoogle Scholar
• 76. Aras S, Zaidi MR. TAMeless traitors: macrophages in cancer progression and metastasis. Br. J. Cancer 117(11), 1583–1591 (2017).
  Medline CASGoogle Scholar
• 77. Mollinedo F. Neutrophil degranulation, plasticity, and cancer metastasis. Trends Immunol. 40(3), 228–242 (2019).
  Medline CASGoogle Scholar
• 78. Ghasemi A, De Palma M. Tweaking the DNA of myeloid cells curbs cancer spread. Nature 579(7798), 196–197 (2020).
  Medline CASGoogle Scholar
• 79. Garner H, de Visser KE. Immune crosstalk in cancer progression and metastatic spread: a complex conversation. Nat. Rev. Immunol. 20(8), 483–497 (2020).
  Medline CASGoogle Scholar
• 80. Liu T, Zhou L, Li D, Andl T, Zhang Y. Cancer-associated fibroblasts build and secure the tumor microenvironment. Front. Cell Dev. Biol. 7, 60 (2019).
  MedlineGoogle Scholar
• 81. Salmon H, Remark R, Gnjatic S, Merad M. Host tissue determinants of tumour immunity. Nat. Rev. Cancer 19(4), 215–227 (2019).
  Medline CASGoogle Scholar
• 82. Zeltz C, Primac I, Erusappan P, Alam J, Noel A, Gullberg D. Cancer-associated fibroblasts in desmoplastic tumors: emerging role of integrins. Semin. Cancer Biol. 62, 166–181 (2020).
  Medline CASGoogle Scholar
• 83. Najafi M, Mortezaee K, Majidpoor J. Stromal reprogramming: a target for tumor therapy. Life Sci. 239, 117049 (2019). • Focuses on the function of cancer-associated fibroblasts as the critical drivers of tumorigenesis, from initiation until progression toward metastasis.
  Medline CASGoogle Scholar
• 84. Liu Y, Cao X. Characteristics and significance of the pre-metastatic niche. Cancer Cell 30(5), 668–681 (2016).
  Medline CASGoogle Scholar
• 85. Liu XQ, Fourel L, Dalonneau F et al. Biomaterial-enabled delivery of SDF-1α at the ventral side of breast cancer cells reveals a crosstalk between cell receptors to promote the invasive phenotype. Biomaterials 127, 61–74 (2017).
  Medline CASGoogle Scholar
• 86. Mortezaee K. CXCL12/CXCR4 axis in the microenvironment of solid tumors: a critical mediator of metastasis. Life Sci. 249, 117534 (2020). • Outlines the importance of CXCL12/CXCR4 signaling in the promotion of metastasis.
  Medline CASGoogle Scholar
• 87. Egeblad M, Nakasone ES, Werb Z. Tumors as organs: complex tissues that interface with the entire organism. Dev. Cell 18(6), 884–901 (2010).
  Medline CASGoogle Scholar
• 88. Tan HX, Gong WZ, Zhou K et al. CXCR4/TGF-β1 mediated hepatic stellate cells differentiation into carcinoma-associated fibroblasts and promoted liver metastasis of colon cancer. Cancer Biol. Ther. 21(3), 258–268 (2020).
  Medline CASGoogle Scholar
• 89. Urosevic J, Blasco MT, Llorente A et al. ERK1/2 signaling induces upregulation of ANGPT2 and CXCR4 to mediate liver metastasis in colon cancer. Cancer Res. 80(21), 4668–4680 (2020).
  Medline CASGoogle Scholar
• 90. Chen IX, Chauhan VP, Posada J et al. Blocking CXCR4 alleviates desmoplasia, increases T-lymphocyte infiltration, and improves immunotherapy in metastatic breast cancer. Proc. Natl Acad. Sci. USA 116(10), 4558–4566 (2019).
  Medline CASGoogle Scholar
• 91. Zhang Q, Zhou N, Wang W, Zhou S. A novel autocrine CXCL14/ACKR2 axis: the achilles’ heel of cancer metastasis? Clin. Cancer Res. 25(12), 3476–3478 (2019).
  Medline CASGoogle Scholar
• 92. Inoue C, Miki Y, Saito R et al. PD-L1 induction by cancer-associated fibroblast-derived factors in lung adenocarcinoma cells. Cancers 11(9), 1257 (2019).
  CASGoogle Scholar
• 93. Gui Y, Aguilar-Mahecha A, Krzemien U et al. Metastatic breast carcinoma–associated fibroblasts have enhanced protumorigenic properties related to increased IGF2 expression. Clin. Cancer Res. 25(23), 7229–7242 (2019).
  Medline CASGoogle Scholar
• 94. Farhood B, Najafi M, Mortezaee K. Cancer-associated fibroblasts: secretions, interactions, and therapy. J. Cell. Biochem. 120(3), 2791–2800 (2019).
  Medline CASGoogle Scholar
• 95. Najafi M, Mortezaee K, Majidpoor J. Cancer stem cell (CSC) resistance drivers. Life Sci. 234, 116781 (2019) • Focuses on the adaptive mechanisms used by cancer stem cells for their growth in the primary and secondary areas.
  Medline CASGoogle Scholar
• 96. Li H, Zhang Q, Wu Q et al. Interleukin-22 secreted by cancer-associated fibroblasts regulates the proliferation and metastasis of lung cancer cells via the PI3K–Akt–mTOR signaling pathway. Am. J. Transl. Res. 11(7), 4077–4088 (2019).
  Medline CASGoogle Scholar
• 97. Wen S, Hou Y, Fu L et al. Cancer-associated fibroblast (CAF)-derived IL32 promotes breast cancer cell invasion and metastasis via integrin β3–p38 MAPK signalling. Cancer Lett. 442, 320–332 (2019).
  Medline CASGoogle Scholar
• 98. Zhou Q, Wu X, Wang X et al. The reciprocal interaction between tumor cells and activated fibroblasts mediated by TNF-α/IL-33/ST2L signaling promotes gastric cancer metastasis. Oncogene 39(7), 1414–1428 (2020).
  Medline CASGoogle Scholar
• 99. Li Q, Zhu CC, Ni B et al. Lysyl oxidase promotes liver metastasis of gastric cancer via facilitating the reciprocal interactions between tumor cells and cancer associated fibroblasts. EBioMedicine 49, 157–171 (2019).
  MedlineGoogle Scholar
• 100. Wu HJ, Hao M, Yeo SK, Guan JL. FAK signaling in cancer-associated fibroblasts promotes breast cancer cell migration and metastasis by exosomal miRNAs-mediated intercellular communication. Oncogene 39(12), 2539–2549 (2020).
  Medline CASGoogle Scholar
• 101. Ren J, Smid M, Iaria J et al. Cancer-associated fibroblast-derived gremlin 1 promotes breast cancer progression. Breast Cancer Res. 21(1), 109 (2019).
  MedlineGoogle Scholar
• 102. Yan Z, Ohuchida K, Fei S et al. Inhibition of ERK1/2 in cancer-associated pancreatic stellate cells suppresses cancer–stromal interaction and metastasis. J. Exp. Clin. Cancer Res. 38(1), 221 (2019).
  MedlineGoogle Scholar
• 103. Schuijs MJ, Png S, Richard AC et al. ILC2-driven innate immune checkpoint mechanism antagonizes NK cell antimetastatic function in the lung. Nat. Immunol. 21(9), 998–1009 (2020).
  Medline CASGoogle Scholar
• 104. Mortezaee K, Najafi M. Immune system in cancer radiotherapy: resistance mechanisms and therapy perspectives. Crit. Rev. Oncol. Hematol. 157, 103180 (2020).
  MedlineGoogle Scholar
• 105. Huntington ND, Cursons J, Rautela J. The cancer – natural killer cell immunity cycle. Nat. Rev. Cancer 20(8), 437–454 (2020).
  Medline CASGoogle Scholar
• 106. Chen EB, Zhou ZJ, Xiao K et al. The miR-561-5p/CX3CL1 signaling axis regulates pulmonary metastasis in hepatocellular carcinoma involving CX3CR1⁺ natural killer cells infiltration. Theranostics 9(16), 4779–4794 (2019).
  Medline CASGoogle Scholar
• 107. Lo HC, Xu Z, Kim IS et al. Resistance to natural killer cell immunosurveillance confers a selective advantage to polyclonal metastasis. Nat. Cancer 1, 709–722 (2020).
  Google Scholar
• 108. Nakamura K, Smyth MJ. Immunoediting of cancer metastasis by NK cells. Nat. Cancer 1, 670–671 (2020).
  Google Scholar
• 109. Chan IS, Knútsdóttir H, Ramakrishnan G et al. Cancer cells educate natural killer cells to a metastasis-promoting cell state. J. Cell Biol. 219(9), e202001134 (2020).
  Medline CASGoogle Scholar
• 110. Harmon C, Robinson MW, Hand F et al. Lactate-mediated acidification of tumor microenvironment induces apoptosis of liver-resident NK cells in colorectal liver metastasis. Cancer Immunol. Res. 7(2), 335–346 (2019).
  Medline CASGoogle Scholar
• 111. Smeda M, Przyborowski K, Stojak M, Chlopicki S. The endothelial barrier and cancer metastasis: does the protective facet of platelet function matter? Biochem. Pharmacol. 176, 113886 (2020).
  Medline CASGoogle Scholar
• 112. Mammadova-Bach E, Jesus Gil-Pulido, Edita Sarukhanyan et al. Platelet glycoprotein VI promotes metastasis through interaction with cancer cell-derived galectin-3. Blood 135(14), 1146–1160 (2020).
  MedlineGoogle Scholar
• 113. Zhuang M, Xin G, Wei Z et al. Dihydrodiosgenin inhibits endothelial cell-derived factor VIII and platelet-mediated hepatocellular carcinoma metastasis. Cancer Manag. Res. 11, 4871–4882 (2019).
  Medline CASGoogle Scholar
• 114. Gaertner F, Massberg S. Patrolling the vascular borders: platelets in immunity to infection and cancer. Nat. Rev. Immunol. 19(12), 747–776 (2019).
  Medline CASGoogle Scholar
• 115. Schlesinger M. Role of platelets and platelet receptors in cancer metastasis. J. Hematol. Oncol. 11(1), 125 (2018).
  Medline CASGoogle Scholar
• 116. Menter DG, Kopetz S, Hawk E et al. Platelet ‘first responders’ in wound response, cancer, and metastasis. Cancer Metastasis Rev. 36(2), 199–213 (2017).
  Medline CASGoogle Scholar
• 117. Zhang Y, Cedervall J, Hamidi A et al. Platelet-specific PDGFB ablation impairs tumor vessel integrity and promotes metastasis. Cancer Res. 80(16), 3345–3358 (2020).
  Medline CASGoogle Scholar
• 118. Xiong G, Chen J, Zhang G et al. Hsp47 promotes cancer metastasis by enhancing collagen-dependent cancer cell-platelet interaction. Proc. Natl Acad. Sci. USA 117(7), 3748–3758 (2020).
  Medline CASGoogle Scholar
• 119. Mortezaee K. Immune escape: a critical hallmark in solid tumors. Life Sci. 258, 118110 (2020). • Focuses on immune evasion mechanisms exploited by tumor cells to take a metastatic route.
  Medline CASGoogle Scholar
• 120. Dickson I. NETs promote liver metastasis via CCDC25. Nat. Rev. Gastroenterol. Hepatol. 17(8), 451–451 (2020).
  MedlineGoogle Scholar
• 121. Park J, Wysocki RW, Amoozgar Z et al. Cancer cells induce metastasis-supporting neutrophil extracellular DNA traps. Sci. Transl. Med. 8(361), 361ra138–361ra138 (2016).
  MedlineGoogle Scholar
• 122. Spicer JD, McDonald B, Cools-Lartigue JJ et al. Neutrophils promote liver metastasis via Mac-1-mediated interactions with circulating tumor cells. Cancer Res. 72(16), 3919–3927 (2012).
  Medline CASGoogle Scholar
• 123. Wculek SK, Malanchi I. Neutrophils support lung colonization of metastasis-initiating breast cancer cells. Nature 528(7582), 413–417 (2015).
  Medline CASGoogle Scholar
• 124. Huh SJ, Liang S, Sharma A, Dong C, Robertson GP. Transiently entrapped circulating tumor cells interact with neutrophils to facilitate lung metastasis development. Cancer Res. 70(14), 6071–6082 (2010).
  Medline CASGoogle Scholar
• 125. Li P, Lu M, Shi J et al. Dual roles of neutrophils in metastatic colonization are governed by the host NK cell status. Nat. Commun. 11(1), 4387 (2020).
  MedlineGoogle Scholar
• 126. Kang T, Zhu Q, Wei D et al. Nanoparticles coated with neutrophil membranes can effectively treat cancer metastasis. ACS Nano 11(2), 1397–1411 (2017).
  Medline CASGoogle Scholar
• 127. Rodrigues G, Hoshino A, Kenific CM et al. Tumour exosomal CEMIP protein promotes cancer cell colonization in brain metastasis. Nat. Cell Biol. 21(11), 1403–1412 (2019).
  Medline CASGoogle Scholar
• 128. Xu R, Rai A, Chen M, Suwakulsiri W, Greening DW, Simpson RJ. Extracellular vesicles in cancer – implications for future improvements in cancer care. Nat. Rev. Clin. Oncol. 15(10), 617–638 (2018).
  Medline CASGoogle Scholar
• 129. Zeng Z, Li Y, Pan Y et al. Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat. Commun. 9(1), 5395 (2018).
  Medline CASGoogle Scholar
• 130. Howe EN, Burnette MD, Justice ME et al. Rab11b-mediated integrin recycling promotes brain metastatic adaptation and outgrowth. Nat. Commun. 11(1), 3017 (2020).
  Medline CASGoogle Scholar
• 131. Mortezaee K, Najafi M, Farhood B, Ahmadi A, Shabeeb D, Musa AE. NF-κB targeting for overcoming tumor resistance and normal tissues toxicity. J. Cell. Physiol. 234(10), 17187–17204 (2019). • Provides an overview of the activity of NF-κB in resistance of tumors.
  Medline CASGoogle Scholar
• 132. Najafi M, Salehi E, Farhood B et al. Adjuvant chemotherapy with melatonin for targeting human cancers: a review. J. Cell. Physiol. 234(3), 2356–2372 (2019).
  Medline CASGoogle Scholar
• 133. Mortezaee K, Najafi M, Farhood B et al. Modulation of apoptosis by melatonin for improving cancer treatment efficiency: an updated review. Life Sci. 228, 228–241 (2019).
  Medline CASGoogle Scholar
• 134. Farhood B, Goradel NH, Mortezaee K et al. Melatonin as an adjuvant in radiotherapy for radioprotection and radiosensitization. Clin. Transl. Oncol. 21(3), 268–279 (2019).
  Medline CASGoogle Scholar
• 135. Seike T, Fujita K, Yamakawa Y et al. Interaction between lung cancer cells and astrocytes via specific inflammatory cytokines in the microenvironment of brain metastasis. Clin. Exp. Metastasis 28(1), 13–25 (2011).
  Medline CASGoogle Scholar
• 136. Mortezaee K. Redox tolerance and metabolic reprogramming in solid tumors. Cell Biol. Int. 45(2), 273–286 (2020). • Focuses over the two important adaptive mechanisms taken by tumor cells, important for their successful seeding in the secondary target organs.
  Google Scholar
• 137. Mortezaee K, Goradel NH, Amini P et al. NADPH oxidase as a target for modulation of radiation response; implications to carcinogenesis and radiotherapy. Curr. Mol. Pharmacol. 12(1), 50–60 (2019).
  Medline CASGoogle Scholar
• 138. Segar J, Shroff RT. Charging forward in locally advanced pancreatic cancer. Lancet Gastroenterol. Hepatol. 5(3), 234–236 (2020).
  MedlineGoogle Scholar
• 139. Giuliano AE, Ballman KV, McCall L et al. Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: the ACOSOG Z0011 (Alliance) randomized clinical trial. JAMA 318(10), 918–926 (2017).
  MedlineGoogle Scholar
• 140. Graham TA, Shibata D. Navigating the path to distant metastasis. Nat. Genet. 52(7), 642–643 (2020).
  Medline CASGoogle Scholar
• 141. Zhang C, Zhang L, Xu T et al. Mapping the spreading routes of lymphatic metastases in human colorectal cancer. Nat. Commun. 11(1), 1993 (2020).
  Medline CASGoogle Scholar
• 142. Reiter JG, Hung WT, Lee IH et al. Lymph node metastases develop through a wider evolutionary bottleneck than distant metastases. Nat. Genet. 52(7), 692–700 (2020).
  Medline CASGoogle Scholar
• 143. Milette S, Hashimoto M, Perrino S et al. Sexual dimorphism and the role of estrogen in the immune microenvironment of liver metastases. Nat. Commun. 10(1), 5745 (2019).
  Medline CASGoogle Scholar
• 144. Achinger-Kawecka J, Valdes-Mora F, Luu PL et al. Epigenetic reprogramming at estrogen-receptor binding sites alters 3D chromatin landscape in endocrine-resistant breast cancer. Nat. Commun. 11(1), 320 (2020).
  Medline CASGoogle Scholar
• 145. Contreras-Zárate MJ, Day NL, Ormond DR et al. Estradiol induces BDNF/TrkB signaling in triple-negative breast cancer to promote brain metastases. Oncogene 38(24), 4685–4699 (2019).
  Medline CASGoogle Scholar
• 146. Gomes AP, Ilter D, Low V et al. Dynamic incorporation of histone H3 variants into chromatin is essential for acquisition of aggressive traits and metastatic colonization. Cancer Cell 36(4), 402–417 (2019).
  Medline CASGoogle Scholar
• 147. Najafi M, Ahmadi A, Mortezaee K. Extracellular-signal-regulated kinase/mitogen-activated protein kinase signaling as a target for cancer therapy: an updated review. Cell Biol. Int. 43(11), 1206–1222 (2019).
  Medline CASGoogle Scholar
• 148. Ahmadi A, Najafi M, Farhood B, Mortezaee K. Transforming growth factor-β signaling: tumorigenesis and targeting for cancer therapy. J. Cell. Physiol. 234(8), 12173–12187 (2019).
  Medline CASGoogle Scholar
• 149. Boire A, Coffelt SB, Quezada SA, Vander Heiden MG, Weeraratna AT. Tumour dormancy and reawakening: opportunities and challenges. Trends Cancer 5(12), 762–765 (2019).
  MedlineGoogle Scholar
• 150. Rosel D, Fernandes M, Sanz-Moreno V, Brábek J. Migrastatics: redirecting R&D in solid cancer towards metastasis? Trends Cancer 5(12), 755–756 (2019).
  Medline CASGoogle Scholar
• 151. Tang X, Shi L, Xie N et al. SIRT7 antagonizes TGF-β signaling and inhibits breast cancer metastasis. Nat. Commun. 8(1), 318 (2017).
  MedlineGoogle Scholar
• 152. Gandalovičová A, Rosel D, Fernandes M et al. Migrastatics – anti-metastatic and anti-invasion drugs: promises and challenges. Trends Cancer 3(6), 391–406 (2017).
  Medline CASGoogle Scholar
• 153. Hoj JP, Mayro B, Pendergast AM. A TAZ–AXL–ABL2 feed-forward signaling axis promotes lung adenocarcinoma brain metastasis. Cell Rep. 29(11), 3421–3434.e8 (2019).
  Medline CASGoogle Scholar
• 154. Duruisseaux M. Lorlatinib: a new treatment option for ROS1-positive lung cancer. Lancet Oncol. 20(12), 1622–1623 (2019).
  MedlineGoogle Scholar
• 155. Zhuang X, Zhang H, Li X et al. Differential effects on lung and bone metastasis of breast cancer by Wnt signalling inhibitor DKK1. Nat. Cell Biol. 19(10), 1274–1285 (2017).
  Medline CASGoogle Scholar
• 156. Le A, Udupa S, Zhang C. The metabolic interplay between cancer and other diseases. Trends Cancer 5(12), 809–821 (2019).
  MedlineGoogle Scholar
• 157. Peck B, Schulze A. Lipid metabolism at the nexus of diet and tumor microenvironment. Trends Cancer 5(11), 693–703 (2019).
  Medline CASGoogle Scholar
• 158. Batlle E, Massagué J. Transforming growth factor-β signaling in immunity and cancer. Immunity 50(4), 924–940 (2019).
  Medline CASGoogle Scholar
• 159. Majidpoor J, Mortezaee K. Steps in metastasis: an updated review. Med. Oncol. 38(1), 3 (2021).
  MedlineGoogle Scholar
• 160. Mortezaee K. Enriched cancer stem cells, dense stroma, and cold immunity: Interrelated events in pancreatic cancer. J. Biochem. Mol. Toxicol. doi: 10.1002/jbt.22708 (2021) (Epub ahead of print).
  MedlineGoogle Scholar