IEO model: A novel concept describing the complete metastatic process in the liver microenvironment (Review)
- Authors:
- Lu Wang
- Yinan Sun
- Minxiao Yi
- Weiheng Zhao
- Xianglin Yuan
-
Affiliations: Department of Oncology, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430030, P.R. China, Division of Cardiology, Department of Internal Medicine, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei 430030, P.R. China - Published online on: April 10, 2020 https://doi.org/10.3892/ol.2020.11525
- Pages: 3627-3633
This article is mentioned in:
Abstract
![]() |
![]() |
Denève E, Riethdorf S, Ramos J, Nocca D, Coffy A, Daurès JP, Maudelonde T, Fabre JM, Pantel K and Alix-Panabières C: Capture of viable circulating tumor cells in the liver of colorectal cancer patients. Clin Chem. 59:1384–1392. 2013. View Article : Google Scholar : PubMed/NCBI | |
Obenauf AC and Massaguè J: Surviving at a distance: Organ specific metastasis. Trends Cancer. 1:76–91. 2015. View Article : Google Scholar : PubMed/NCBI | |
Hu Z, Ding J, Ma Z, Sun R, Seoane JA, Scott Shaffer J, Suarez CJ, Berghoff AS, Cremolini C, Falcone A, et al: Quantitative evidence for early metastatic seeding in colorectal cancer. Nat Genet. 51:1113–1122. 2019. View Article : Google Scholar : PubMed/NCBI | |
Massaguè J and Obenauf AC: Metastatic colonization by circulating tumor cells. Nature. 529:298–306. 2016. View Article : Google Scholar : PubMed/NCBI | |
Van den Eynden GG, Majeed AW, Illemann M, Vermeulen PB, Bird NC, Høyer-Hansen G, Eefsen RL, Reynolds AR and Brodt P: The multifaceted role of the microenvironment in liver metastasis: Biology and clinical implications. Cancer Res. 73:2031–2043. 2013. View Article : Google Scholar : PubMed/NCBI | |
Guo Y, Ji X, Liu J, Fan D, Zhou Q, Chen C, Wang W, Wang G, Wang H, Yuan W, et al: Effects of exosomes on pre-metastatic niche formation in tumors. Mol Cancer. 18:392019. View Article : Google Scholar : PubMed/NCBI | |
Li Destri G, Castaing M, Ferlito F, Minutolo V, Di Cataldo A and Puleo S: Rare hepatic metastases of colorectal cancer in livers with symptomatic HBV and HCV hepatitis. Ann Ital Chir. 84:323–327. 2013.PubMed/NCBI | |
Qiu HB, Zhang LY, Zeng ZL, Wang ZQ, Luo HY, Keshari RP, Zhou ZW and Xu RH: HBV infection decreases risk of liver metastasis in patients with colorectal cancer: A cohort study. World J Gastroenterol. 17:804–808. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kondo T, Okabayashi K, Hasegawa H, Tsuruta M, Shigeta K and Kitagawa Y: The impact of hepatic fibrosis on the incidence of liver metastasis from colorectal cancer. Br J Cancer. 115:34–39. 2016. View Article : Google Scholar : PubMed/NCBI | |
Chiou WY, Chang CM, Tseng KC, Hung SK, Lin HY, Chen YC, Su YC, Tseng CW, Tsai SJ, Lee MS and Li CY: Effect of liver cirrhosis on metastasis in colorectal cancer patients: A nationwide population-based cohort study. Jpn J Clin Oncol. 45:160–168. 2015. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Ding X, Nan L, Wang Y, Wang J, Yan Z, Zhang W, Sun J, Zhu W, Ni B, et al: Investigation of the roles of exosomes in colorectal cancer liver metastasis. Oncol Rep. 33:2445–2453. 2015. View Article : Google Scholar : PubMed/NCBI | |
Gordon-Weeks AN, Lim SY, Yuzhalin AE, Jones K, Markelc B, Kim KJ, Buzzelli JN, Fokas E, Cao Y, Smart S and Muschel R: Neutrophils promote hepatic metastasis growth through fibroblast growth factor 2-dependent angiogenesis in mice. Hepatology. 65:1920–1935. 2017. View Article : Google Scholar : PubMed/NCBI | |
Mendonsa AM, VanSaun MN, Ustione A, Piston DW, Fingleton BM and Gorden DL: Host and tumor derived MMP13 regulate extravasation and establishment of colorectal metastases in the liver. Mol Cancer. 14:492015. View Article : Google Scholar : PubMed/NCBI | |
Cai B, Liao K, Song XQ, Wei WY, Zhuang Y and Zhang S: Patients with chronically diseased livers have lower incidence of colorectal liver metastases: A meta-analysis. PLoS One. 9:e1086182014. View Article : Google Scholar : PubMed/NCBI | |
Song E, Chen J, Ouyang N, Wang M, Exton MS and Heemann U: Kupffer cells of cirrhotic rat livers sensitize colon cancer cells to Fas mediated apoptosis. Br J Cancer. 84:1265–1271. 2001. View Article : Google Scholar : PubMed/NCBI | |
Seitz G: Why are metastases in cirrhotic livers so rare? Ultraschall Med. 10:123–126. 1989.(In German). View Article : Google Scholar : PubMed/NCBI | |
Seymour K and Charnley RM: Evidence that metastasis is less common in cirrhotic than normal liver: A systematic review of post-mortem case-control studies. Br J Surg. 86:1237–1242. 1999. View Article : Google Scholar : PubMed/NCBI | |
Lee JW, Stone ML, Porrett PM, Thomas SK, Komar CA, Li JH, Delman D, Graham K, Gladney WL, Hua X, et al: Hepatocytes direct the formation of a pro-metastatic niche in the liver. Nature. 567:249–252. 2019. View Article : Google Scholar : PubMed/NCBI | |
Utsunomiya T, Saitsu H, Saku M, Yoshida K, Matsumata T, Shimada M and Sugimachi K: Rare occurrence of colorectal cancer metastasis in livers infected with hepatitis B or C virus. Am J Surg. 177:279–281. 1999. View Article : Google Scholar : PubMed/NCBI | |
Qian HG, Zhang J, Leng JH, Zhou GQ, Wu JH, Tian XY, Yang Y and Hao CY: Association of hepatitis B virus infection and cirrhosis with liver metastasis in colorectal cancer. Zhonghua Wei Chang Wai Ke Za Zhi. 13:202–204. 2010.(In Chinese). PubMed/NCBI | |
Song E, Chen J, Ou Q and Su F: Rare occurrence of metastatic colorectal cancers in livers with replicative hepatitis B infection. Am J Surg. 181:529–533. 2001. View Article : Google Scholar : PubMed/NCBI | |
Zeng ZS, Sun Y, Shu WP and Guillem JG: Tissue inhibitor of metalloproteinase-3 is a basement membrane-associated protein that is significantly decreased in human colorectal cancer. Dis Colon Rectum. 44:1290–1296. 2001. View Article : Google Scholar : PubMed/NCBI | |
Cheng L, Geng L, Dai B, Zheng T, Fu J, Qiao L, Cai W, Wang Y and Yang J: Repression of let-7a cluster prevents adhesion of colorectal cancer cells by enforcing a mesenchymal phenotype in presence of liver inflammation. Cell Death Dis. 9:4892018. View Article : Google Scholar : PubMed/NCBI | |
Uetsuji S, Yamamura M, Yamamichi K, Okuda Y, Takada H and Hioki K: Absence of colorectal cancer metastasis to the cirrhotic liver. Am J Surg. 164:176–177. 1992. View Article : Google Scholar : PubMed/NCBI | |
Wu JF and Chang MH: Natural history of chronic hepatitis B virus infection from infancy to adult life-the mechanism of inflammation triggering and long-term impacts. J Biomed Sci. 22:922015. View Article : Google Scholar : PubMed/NCBI | |
Tordjmann T, Soulie A, Guettier C, Schmidt M, Berthou C, Beaugrand M and Sasportes M: Perforin and granzyme B lytic protein expression during chronic viral and autoimmune hepatitis. Liver. 18:391–397. 1998. View Article : Google Scholar : PubMed/NCBI | |
Lara-Pezzi E, Majano PL, Gómez-Gonzalo M, García-Monzón C, Moreno-Otero R, Levrero M and López-Cabrera M: The hepatitis B virus X protein up-regulates tumor necrosis factor alpha gene expression in hepatocytes. Hepatology. 28:1013–1021. 1998. View Article : Google Scholar : PubMed/NCBI | |
McVicker B, Tuma DJ, Lazure KE, Thomas P and Casey CA: Alcohol, carcinoembryonic antigen processing and colorectal liver metastases. Adv Exp Med Biol. 815:295–311. 2015. View Article : Google Scholar : PubMed/NCBI | |
Maeda M, Nagawa H, Maeda T, Koike H and Kasai H: Alcohol consumption enhances liver metastasis in colorectal carcinoma patients. Cancer. 83:1483–1488. 1998. View Article : Google Scholar : PubMed/NCBI | |
Dong H, Tang J, Li LH, Ge J, Chen X, Ding J, Men HT, Luo WX, Du Y, Li C, et al: Serum carbohydrate antigen 19-9 as an indicator of liver metastasis in colorectal carcinoma cases. Asian Pac J Cancer Prev. 14:909–913. 2013. View Article : Google Scholar : PubMed/NCBI | |
Karube H, Masuda H, Hayashi S, Ishii Y and Nemoto N: Fatty liver suppressed the angiogenesis in liver metastatic lesions. Hepatogastroenterology. 47:1541–1545. 2000.PubMed/NCBI | |
Pancione M, Giordano G, Remo A, Febbraro A, Sabatino L, Manfrin E, Ceccarelli M and Colantuoni V: Immune escape mechanisms in colorectal cancer pathogenesis and liver metastasis. J Immunol Res. 2014:6868792014. View Article : Google Scholar : PubMed/NCBI | |
Alderton GK: Metastasis. Exosomes drive premetastatic niche formation. Nat Rev Cancer. 12:4472012. View Article : Google Scholar : PubMed/NCBI | |
Kosaka N, Iguchi H, Hagiwara K, Yoshioka Y, Takeshita F and Ochiya T: Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J Biol Chem. 288:10849–10859. 2013. View Article : Google Scholar : PubMed/NCBI | |
Théry C, Ostrowski M and Segura E: Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 9:581–593. 2009. View Article : Google Scholar : PubMed/NCBI | |
Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ and Lötvall JO: Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 9:654–672. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bang C and Thum T: Exosomes: New players in cell-cell communication. Int J Biochem Cell Biol. 44:2060–2064. 2012. View Article : Google Scholar : PubMed/NCBI | |
Hood JL, Pan H, Lanza GM and Wickline SA; Consortium for Translational Research in Advanced Imaging and Nanomedicine (C-TRAIN), : Paracrine induction of endothelium by tumor exosomes. Lab Invest. 89:1317–1328. 2009. View Article : Google Scholar : PubMed/NCBI | |
Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO and Skog J: Tumor microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun. 2:1802011. View Article : Google Scholar : PubMed/NCBI | |
Aliotta JM, Pereira M, Johnson KW, de Paz N, Dooner MS, Puente N, Ayala C, Brilliant K, Berz D, Lee D, et al: Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription. Exp Hematol. 38:233–245. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S, et al: Tumor exosome integrins determine organotropic metastasis. Nature. 527:329–335. 2015. View Article : Google Scholar : PubMed/NCBI | |
Labelle M, Begum S and Hynes RO: Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Res. 20:579–560. 2011. | |
Houg DS and Bijlsma MF: The hepatic pre-metastatic niche in pancreatic ductal adenocarcinoma. Mol Cancer. 17:952018. View Article : Google Scholar : PubMed/NCBI | |
Hambardzumyan D, Becher OJ, Rosenblum MK, Pandolfi PP, Manova-Todorova K and Holland EC: PI3K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev. 22:436–448. 2008. View Article : Google Scholar : PubMed/NCBI | |
Cao ZW, Ding BS, Guo PP, Lee SB, Butler JM, Casey SC, Simons M, Tam W, Felsher DW, Shido K, et al: Angiocrine factors deployed by tumor vascular niche induce B cell lymphoma invasiveness and chemoresistance. Cancer Res. 25:350–365. 2014. | |
Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, et al: VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 438:820–827. 2005. View Article : Google Scholar : PubMed/NCBI | |
McAllister SS and Weinberg RA: The tumor-induced systemic environment as a critical regulator of cancer progression and metastasis. Nat Cell Biol. 16:717–727. 2014. View Article : Google Scholar : PubMed/NCBI | |
Tabariés S, Dupuy F, Dong Z, Monast A, Annis MG, Spicer J, Ferri LE, Omeroglu A, Basik M, Amir E, et al: Claudin-2 promotes breast cancer liver metastasis by facilitating tumor cell interactions with hepatocytes. Mol Cell Biol. 32:2979–2991. 2012. View Article : Google Scholar : PubMed/NCBI | |
Aird WC: Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circ Res. 100:174–190. 2007. View Article : Google Scholar : PubMed/NCBI | |
Nguyen DX, Bos PD and Massagué J: Metastasis: From dissemination to organ-specific colonization. Nat Rev Cancer. 9:274–284. 2009. View Article : Google Scholar : PubMed/NCBI | |
Budczies J, von Winterfeld M, Klauschen F, Bockmayr M, Lennerz JK, Denkert C, Wolf T, Warth A, Dietel M, Anagnostopoulos I, et al: The landscape of metastatic progression patterns across major human cancers. Oncotarget. 6:570–583. 2015. View Article : Google Scholar : PubMed/NCBI | |
Eyles J, Puaux AL, Wang X, Toh B, Prakash C, Hong M, Tan TG, Zheng L, Ong LC, Jin Y, et al: Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J Clin Invest. 120:2030–2039. 2010. View Article : Google Scholar : PubMed/NCBI | |
Chen WS, Wei SJ, Liu JM, Hsiao M, Kou-Lin J and Yang WK: Tumor invasiveness and liver metastasis of colon cancer cells correlated with cyclooxygenase-2 (COX-2) expression and inhibited by a COX-2-selective inhibitor, etodolac. Int J Cancer. 91:894–899. 2001. View Article : Google Scholar : PubMed/NCBI | |
Wang D, Sun H, Wei J, Cen B and DuBois RN: CXCL1 is critical for premetastatic niche formation and metastasis in colorectal cancer. Cancer Res. 77:3655–3665. 2017. View Article : Google Scholar : PubMed/NCBI | |
Murdoch C, Muthana M, Coffelt SB and Lewis CE: The role of myeloid cells in the promotion of tumor angiogenesis. Nat Rev Cancer. 8:618–631. 2008. View Article : Google Scholar : PubMed/NCBI | |
Flavell RA, Sanjabi S, Wrzesinski SH and Licona-Limón P: The polarization of immune cells in the tumor environment by TGFbeta. Nat Rev Immunol. 10:554–567. 2010. View Article : Google Scholar : PubMed/NCBI | |
Luzzi KJ, MacDonald IC, Schmidt EE, Kerkvliet N, Morris VL, Chambers AF and Groom AC: Multistep nature of metastatic inefficiency: Dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am J Pathol. 153:865–873. 1998. View Article : Google Scholar : PubMed/NCBI | |
Brodt P: Role of the microenvironment in liver metastasis: From pre- to prometastatic niches. Clin Cancer Res. 22:5971–5982. 2016. View Article : Google Scholar : PubMed/NCBI | |
Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS and Albelda SM: Polarization of tumor-associated neutrophil phenotype by TGF-beta: ‘N1’ versus ‘N2’ TAN. Cancer Res. 16:183–194. 2009. | |
Steele CW, Karim SA, Leach JDG, Bailey P, Upstill-Goddard R, Rishi L, Foth M, Bryson S, McDaid K, Wilson Z, et al: CXCR2 inhibition profoundly suppresses metastases and augments immunotherapy in pancreatic ductal adenocarcinoma. Cancer Res. 29:832–845. 2016. | |
Hirai H, Fujishita T, Kurimoto K, Miyachi H, Kitano S, Inamoto S, Itatani Y, Saitou M, Maekawa T and Taketo MM: CCR1-mediated accumulation of myeloid cells in the liver microenvironment promoting mouse colon cancer metastasis. Clin Exp Metastasis. 31:977–989. 2014. View Article : Google Scholar : PubMed/NCBI | |
Elpek KG, Cremasco V, Shen H, Harvey CJ, Wucherpfennig KW, Goldstein DR, Monach PA and Turley SJ: The tumor microenvironment shapes lineage, transcriptional, and functional diversity of infiltrating myeloid cells. Cancer Immunol Res. 2:655–667. 2014. View Article : Google Scholar : PubMed/NCBI | |
Yuan H, Li ZM, Shao J, Ji WX, Xia W and Lu S: FGF2/FGFR1 regulates autophagy in FGFR1-amplified non-small cell lung cancer cells. J Exp Clin Cancer Res. 36:722017. View Article : Google Scholar : PubMed/NCBI | |
Presta M, Andrés G, Leali D, Dell'Era P and Ronca R: Inflammatory cells and chemokines sustain FGF2-induced angiogenesis. Eur Cytokine Netw. 20:39–50. 2009. View Article : Google Scholar : PubMed/NCBI | |
Shibutani M, Maeda K, Nagahara H, Fukuoka T, Matsutani S, Kashiwagi S, Tanaka H, Hirakawa K and Ohira M: A comparison of the local immune status between the primary and metastatic tumor in colorectal cancer: A retrospective study. BMC Cancer. 18:3712018. View Article : Google Scholar : PubMed/NCBI | |
Le DT, Durham JN, Smith KN, Wang H, Bartlett BR, Aulakh LK, Lu S, Kemberling H, Wilt C, Luber BS, et al: Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science. 357:409–413. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhou G, Noordam L, Sprengers D, Doukas M, Boor PPC, van Beek AA, Erkens R, Mancham S, Grünhagen D, Menon AG, et al: Blockade of LAG3 enhances responses of tumor-infiltrating T cells in mismatch repair-proficient liver metastases of colorectal cancer. Oncoimmunology. 7:e14483322018. View Article : Google Scholar : PubMed/NCBI | |
Tauriello DVF, Palomo-Ponce S, Stork D, Berenguer-Llergo A, Badia-Ramentol J, Iglesias M, Sevillano M, Ibiza S, Cañellas A, Hernando-Momblona X, et al: TGFβ drives immune evasion in genetically reconstituted colon cancer metastasis. Nature. 554:538–543. 2018. View Article : Google Scholar : PubMed/NCBI | |
Vermeulen PB, Colpaert C, Salgado R, Royers R, Hellemans H, Van Den Heuvel E, Goovaerts G, Dirix LY and Van Marck E: Liver metastases from colorectal adenocarcinomas grow in three patterns with different angiogenesis and desmoplasia. J Pathol. 195:336–342. 2001. View Article : Google Scholar : PubMed/NCBI | |
Bugyik E, Szabó V, Dezső K, Rókusz A, Szücs A, Nagy P, Tóvári J, László V, Döme B and Paku S: Role of (myo)fibroblasts in the development of vascular and connective tissue structure of the C38 colorectal cancer in mice. Cancer Commun (Lond). 38:462018. View Article : Google Scholar : PubMed/NCBI | |
Padmanaban V, Krol I, Suhail Y, Szczerba BM, Aceto N, Bader JS and Ewald AJ: E-cadherin is required for metastasis in multiple models of breast cancer. Nature. 573:439–444. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wang HH, McIntosh AR, Hasinoff BB, Rector ES, Ahmed N, Nance DM and Orr FW: B16 melanoma cell arrest in the mouse liver induces nitric oxide release and sinusoidal cytotoxicity: A natural hepatic defense against metastasis. Cancer Res. 60:5862–5869. 2000.PubMed/NCBI | |
Yanagida H, Kaibori M, Yoshida H, Habara K, Yamada M, Kamiyama Y and Okumura T: Hepatic ischemia/reperfusion upregulates the susceptibility of hepatocytes to confer the induction of inducible nitric oxide synthase gene expression. Shock. 26:162–168. 2006. View Article : Google Scholar : PubMed/NCBI | |
Braet F, Nagatsuma K, Saito M, Soon L, Wisse E and Matsuura T: The hepatic sinusoidal endothelial lining and colorectal liver metastases. World J Gastroenterol. 13:821–825. 2007. View Article : Google Scholar : PubMed/NCBI |