Mechanisms of Metastasis in Colorectal Cancer and Metastatic Organotropism: Hematogenous versus Peritoneal Spread
E. Pretzsch
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorF. Bösch
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorJ. Neumann
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Institute of Pathology, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorP. Ganschow
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorA. Bazhin
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorM. Guba
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorJ. Werner
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorCorresponding Author
M. Angele
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorE. Pretzsch
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorF. Bösch
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorJ. Neumann
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Institute of Pathology, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorP. Ganschow
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorA. Bazhin
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorM. Guba
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorJ. Werner
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorCorresponding Author
M. Angele
Department of General, Visceral, and Transplant Surgery, Ludwig-Maximilians-University Munich, Munich, Germany uni-muenchen.de
Search for more papers by this authorAbstract
Metastasis is the major cause of death in patients with colorectal carcinoma (CRC). The most common sites of metastasis are the liver and the peritoneum. Peritoneal carcinomatosis is often considered the end stage of the disease after the tumor has spread to the liver. However, almost half of CRC patients with peritoneal carcinomatosis do not present with liver metastasis. This brings up the question of whether peritoneal spread can still be considered as the end stage of a metastasized CRC or whether it should just be interpreted as a site of metastasis alternative to the liver. This review tries to discuss this question and summarize the current status of literature on potential characteristics in tumor biology in the primary tumor, i.e., factors (transcription factors and direct and indirect E-cadherin repressors) and pathways (WNT, TGF-β, and RAS) modulating EMT, regulation of EMT on a posttranscriptional and posttranslational level (miRNAs), and angiogenesis. In addition to tumor-specific characteristics, factors in the tumor microenvironment, immunological markers, ways of transport of tumor cells, and adhesion molecules appear to differ between hematogenous and peritoneal spread. Factors such as integrins and exosomal integrins, cancer stem cell phenotype, and miRNA expression appear to contribute in determining the metastatic route. We went through each step of the metastasis process comparing hematogenous to peritoneal spread. We identified differences with respect to organotropism, epithelial-mesenchymal transition, angiogenesis and inflammation, and tumor microenvironment which will be further elucidated in this review. A better understanding of the underlying mechanisms and contributing factors of metastasis development in CRC has huge relevance as it is the foundation to help find specific targets for treatment of CRC.
Conflicts of Interest
The authors declare that they have no conflicts of interest.
References
- 1 Ferlay J., Shin H.-R., Bray F., Forman D., Mathers C., and Parkin D. M., Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008, International Journal of Cancer. (2010) 127, no. 12, 2893–2917, https://doi.org/10.1002/ijc.25516, 2-s2.0-78049485263.
- 2 Cook A. D., Single R., and McCahill L. E., Surgical resection of primary tumors in patients who present with stage IV colorectal cancer: an analysis of surveillance, epidemiology, and end results data, 1988 to 2000, Annals of Surgical Oncology. (2005) 12, no. 8, 637–645, https://doi.org/10.1245/ASO.2005.06.012, 2-s2.0-23744473728.
- 3 Desch C. E., Benson A. B., Somerfield M. R. et al., Colorectal cancer surveillance: 2005 update of an American society of clinical oncology practice guideline, Journal of Clinical Oncology. (2005) 23, no. 33, 8512–8519, https://doi.org/10.1200/JCO.2005.04.0063, 2-s2.0-33644696421.
- 4 Segelman J., Granath F., Holm T., MacHado M., Mahteme H., and Martling A., Incidence, prevalence and risk factors for peritoneal carcinomatosis from colorectal cancer, British Journal of Surgery. (2012) 99, no. 5, 699–705, https://doi.org/10.1002/bjs.8679, 2-s2.0-84859590873.
- 5 van Gestel Y. R. B. M., Thomassen I., Lemmens V. E. P. P. et al., Metachronous peritoneal carcinomatosis after curative treatment of colorectal cancer, European Journal of Surgical Oncology (EJSO). (2014) 40, no. 8, 963–969, https://doi.org/10.1016/j.ejso.2013.10.001, 2-s2.0-84903880600.
- 6 Thomassen I., Van Gestel Y. R., Lemmens V. E., and De Hingh I. H., Incidence, prognosis, and treatment options for patients with synchronous peritoneal carcinomatosis and liver metastases from colorectal origin, Diseases of the Colon and Rectum. (2013) 56, no. 12, 1373–1380, https://doi.org/10.1097/DCR.0b013e3182a62d9d, 2-s2.0-84888329362.
- 7 Hoshino A., Costa-Silva B., Shen T.-L. et al., Tumour exosome integrins determine organotropic metastasis, Nature. (2015) 527, no. 7578, 329–335, https://doi.org/10.1038/nature15756, 2-s2.0-84947723880.
- 8 Mann K. M., Ward J. M., Yew C. C. K. et al., Sleeping Beauty mutagenesis reveals cooperating mutations and pathways in pancreatic adenocarcinoma, Proceedings of the National Academy of Sciences. (2012) 109, no. 16, 5934–5941, https://doi.org/10.1073/pnas.1202490109, 2-s2.0-84859947197.
- 9 Reichert M., Bakir B., Moreira L. et al., Regulation of epithelial plasticity determines metastatic organotropism in pancreatic cancer, Developmental Cell. (2018) 45, no. 6, 696–711, https://doi.org/10.1016/j.devcel.2018.05.025, 2-s2.0-85048174090.
- 10 Benedicto A., Marquez J., Herrero A., Olaso E., Kolaczkowska E., and Arteta B., Decreased expression of the β2 integrin on tumor cells is associated with a reduction in liver metastasis of colorectal cancer in mice, BMC Cancer. (2017) 17, no. 1, 1–17, https://doi.org/10.1186/s12885-017-3823-2, 2-s2.0-85037375798.
- 11 Chen W., Hoffmann A. D., Liu H., and Liu X., Organotropism: new insights into molecular mechanisms of breast cancer metastasis, NPJ Precision Oncology. (2018) 2, no. 1, https://doi.org/10.1038/s41698-018-0047-0.
- 12 Stessels F., Van Den Eynden G., Van Der Auwera I. et al., Breast adenocarcinoma liver metastases, in contrast to colorectal cancer liver metastases, display a non-angiogenic growth pattern that preserves the stroma and lacks hypoxia, British Journal of Cancer. (2004) 90, no. 7, 1429–1436, https://doi.org/10.1038/sj.bjc.6601727, 2-s2.0-2342584137.
- 13 Neumann J., Löhrs L., Albertsmeier M. et al., Cancer stem cell markers are associated with distant hematogenous liver metastases but not with peritoneal carcinomatosis in colorectal cancer, Cancer Investigation. (2015) 33, no. 8, 354–360, https://doi.org/10.3109/07357907.2015.1047507, 2-s2.0-84942986896.
- 14 Nagata H., Ishihara S., Kishikawa J. et al., CD133 expression predicts post-operative recurrence in patients with colon cancer with peritoneal metastasis, International Journal of Oncology. (2018) 52, 721–732, https://doi.org/10.3892/ijo.2018.4240, 2-s2.0-85041576641.
- 15 Fujino S. and Miyoshi N., Oct4 gene expression in primary colorectal cancer promotes liver metastasis, Stem Cells International. (2019) 2019, 1–10, https://doi.org/10.1155/2019/7896524.
- 16 Mohamed S. Y., Kaf R. M., Ahmed M. M., Elwan A., Ashour H. R., and Ibrahim A., The prognostic value of cancer stem cell markers (Notch1, ALDH1, and CD44) in primary colorectal carcinoma, Journal of Gastrointestinal Cancer. (2018) 8, 1–14.
- 17 Zhou Y., Xia L., Wang H. et al., Cancer stem cells in progression of colorectal cancer, Oncotarget. (2018) 9, no. 70, 33403–33415, https://doi.org/10.18632/oncotarget.23607, 2-s2.0-85053053921.
- 18 Paschos K. A., Majeed A. W., and Bird N. C., Natural history of hepatic metastases from colorectal cancer-pathobiological pathways with clinical significance, World Journal of Gastroenterology. (2014) 20, no. 14, 3719–3737, https://doi.org/10.3748/wjg.v20.i14.3719, 2-s2.0-84898417231.
- 19 Cao H., Xu E., Liu H., Wan L., and Lai M., Epithelial-mesenchymal transition in colorectal cancer metastasis: a system review, Pathology-Research and Practice. (2015) 211, no. 8, 557–569, https://doi.org/10.1016/j.prp.2015.05.010, 2-s2.0-84983094062.
- 20 Van Roy F., Beyond E-cadherin: roles of other cadherin superfamily members in cancer, Nature Reviews Cancer. (2014) 14, no. 2, 121–134, https://doi.org/10.1038/nrc3647, 2-s2.0-84894520335.
- 21 Peña C., García J. M., Silva J. et al., E-cadherin and vitamin D receptor regulation by SNAIL and ZEB1 in colon cancer: clinicopathological correlations, Human Molecular Genetics. (2005) 14, no. 22, 3361–3370, https://doi.org/10.1093/hmg/ddi366, 2-s2.0-27944447368.
- 22 Batlle E., Sancho E., Francí C. et al., The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumour cells, Nature Cell Biology. (2000) 2, 84–89, https://doi.org/10.1038/35000034, 2-s2.0-0033789680.
- 23 Cano A., Pérez-moreno M. A., Rodrigo I. et al., The transcription factor Snail controls epithelial—mesenchymal transitions by repressing E-cadherin expression, Nature Cell Biology. (2000) 2, 76–83, https://doi.org/10.1038/35000025, 2-s2.0-0033784843.
- 24 Comijn J., Berx G., Vermassen P. et al., The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion, Molecular Cell. (2001) 7, no. 6, 1267–1278, https://doi.org/10.1016/s1097-2765(01)00260-x, 2-s2.0-0034964418.
- 25 Yang J., Mani S. A., Donaher J. L. et al., Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis, Cell. (2004) 117, no. 7, 927–939, https://doi.org/10.1016/j.cell.2004.06.006, 2-s2.0-2942707848.
- 26 Pe M. A., Locascio A., Rodrigo I. et al., A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions, Journal of Biological Chemistry. (2001) 276, no. 29, 27424–27431, https://doi.org/10.1074/jbc.M100827200, 2-s2.0-0035920152.
- 27
Wakeman J. A.,
Sarkar D.,
Shields B., and
Davies M. L., BRACHYURY confers cancer stem cell characteristics on colorectal cancer cells, International Journal of Cancer. (2012) 337, no. 2, 328–337, https://doi.org/10.1002/ijc.26029, 2-s2.0-83655201491.
10.1002/ijc.26029 Google Scholar
- 28 Kilic N., Feldhaus S., Kilic E. et al., Brachyury expression predicts poor prognosis at early stages of colorectal cancer, European Journal of Cancer. (2011) 47, no. 7, 1080–1085, https://doi.org/10.1016/j.ejca.2010.11.015, 2-s2.0-79953690193.
- 29 Jackstadt R., Röh S., Neumann J. et al., AP4 is a mediator of epithelial-mesenchymal transition and metastasis in colorectal cancer, The Journal of Experimental Medicine. (2013) 210, no. 7, 1331–1350, https://doi.org/10.1084/jem.20120812, 2-s2.0-84880682384.
- 30 Watanabe T., Kobunai T., Yamamoto Y. et al., Gene expression of mesenchyme forkhead 1 (FOXC2) significantly correlates with the degree of lymph node metastasis in colorectal cancer, International Surgery. (2011) 96, no. 3, 207–216, https://doi.org/10.9738/1399.1, 2-s2.0-84862963456.
- 31 Sanchez-Tillo E., de Barrios O., Siles L., Cuatrecasas M., Castells A., and Postigo A., -catenin/TCF4 complex induces the epithelial-to-mesenchymal transition (EMT)-activator ZEB1 to regulate tumor invasiveness, Proceedings of the National Academy of Sciences. (2011) 108, no. 48, 19204–19209, https://doi.org/10.1073/pnas.1108977108, 2-s2.0-82755198488.
- 32 Han X., Fang X., Lou X. et al., Silencing SOX2 induced mesenchymal-epithelial transition and its expression predicts liver and lymph node metastasis of CRC patients, PLoS One. (2012) 7, no. 8, e41335, https://doi.org/10.1371/journal.pone.0041335, 2-s2.0-84865106429.
- 33 Dai X., Ge J., Wang X., Qian X., Zhang C., and Li X., OCT4 regulates epithelial-mesenchymal transition and its knockdown inhibits colorectal cancer cell migration and invasion, Oncology Reports. (2013) 29, no. 1, 155–160, https://doi.org/10.3892/or.2012.2086, 2-s2.0-84872832415.
- 34 Meng H.-M., Zheng P., Wang X.-Y. et al., Over-expression of Nanog predicts tumor progression and poor prognosis in colorectal cancer, Cancer Biology and Therapy. (2010) 9, no. 4, 295–302, https://doi.org/10.4161/cbt.9.4.10666, 2-s2.0-77953553879.
- 35 Lu M.-H., Huang C.-C., Pan M.-R., Chen H.-H., and Hung W.-C., Prospero homeobox 1 promotes epithelial-mesenchymal transition in colon cancer cells by inhibiting e-cadherin via miR-9, Clinical Cancer Research. (2012) 18, no. 23, 6416–6425, https://doi.org/10.1158/1078-0432.CCR-12-0832, 2-s2.0-84870360174.
- 36 Ono H., Imoto I., Kozaki K. et al., SIX1 promotes epithelial-mesenchymal transition in colorectal cancer through ZEB1 activation, Oncogene. (2012) 31, no. 47, 4923–4934, https://doi.org/10.1038/onc.2011.646, 2-s2.0-84870055922.
- 37 Takahashi Y., Sawada G., Kurashige J. et al., Paired related homoeobox 1, a new EMT inducer, is involved in metastasis and poor prognosis in colorectal cancer, British Journal of Cancer. (2013) 109, no. 2, 307–311, https://doi.org/10.1038/bjc.2013.339, 2-s2.0-84881107710.
- 38 Belton A., Gabrovsky A., Bae Y. K. et al., HMGA1 induces intestinal polyposis in transgenic mice and drives tumor progression and stem cell properties in colon cancer cells, PLoS One. (2012) 7, no. 1, e30034, https://doi.org/10.1371/journal.pone.0030034, 2-s2.0-84856055494.
- 39 Diesch J., Sanij E., Gilan O. et al., Widespread FRA1-dependent control of mesenchymal transdifferentiation programs in colorectal cancer cells, PLoS One. (2014) 9, no. 3, e88950, https://doi.org/10.1371/journal.pone.0088950, 2-s2.0-84899114827.
- 40 Go T., Bandre E., Cejas P. et al., TWIST1 overexpression is associated with nodal invasion and male sex in primary colorectal cancer, Annals of Surgical Oncology. (2008) 16, no. 1, 78–87, https://doi.org/10.1245/s10434-008-0166-x, 2-s2.0-58549100103.
- 41
Okada T.,
Suehiro Y.,
Ueno K.,
Mitomori S.,
Kaneko S., and
Nishioka M., TWIST1 hypermethylation is observed frequently in colorectal tumors and its overexpression is associated with unfavorable outcomes in patients with colorectal cancer, Genes, Chromosom Cancer. (2010) 462, 452–462, https://doi.org/10.1002/gcc.20755, 2-s2.0-77950680545.
10.1002/gcc.20755 Google Scholar
- 42 Toiyama Y., Yasuda H., Saigusa S. et al., Increased expression of slug and vimentin as novel predictive biomarkers for lymph node metastasis and poor prognosis in colorectal cancer, Carcinogenesis. (2013) 34, no. 11, 2548–2557, https://doi.org/10.1093/carcin/bgt282, 2-s2.0-84886996188.
- 43 Velez-Delvalle C., Marsch-Moreno M., Castro-Muñozledo F., Galván-Mendoza I. J., and Kuri-Harcuch W., Epithelial cell migration requires the interaction between the vimentin and keratin intermediate filaments, Scientific Reports. (2016) 6, no. 1, 1–10, https://doi.org/10.1038/srep24389, 2-s2.0-84969756448.
- 44 Novellasdemunt L., Antas P., and Li V. S. W., Targeting Wnt signaling in colorectal cancer. A review in the theme: cell signaling: proteins, pathways and mechanisms, American Journal of Physiology-Cell Physiology. (2015) 309, no. 8, C511–C521, https://doi.org/10.1152/ajpcell.00117.2015, 2-s2.0-84945181246.
- 45 Vincan E. and Barker N., The upstream components of the Wnt signalling pathway in the dynamic EMT and MET associated with colorectal cancer progression, Clinical and Experimental Metastasis. (2008) 25, no. 6, 657–663, https://doi.org/10.1007/s10585-008-9156-4, 2-s2.0-47549098136.
- 46 Markowitz S., Wang J., Myeroff L. et al., Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability, Science. (1995) 268, 1336–1339, https://doi.org/10.1126/science.7761852, 2-s2.0-0029066689.
- 47 Markowitz S. D. and Bertagnolli M. M., Molecular basis of colorectal cancer, New England Journal of Medicine. (2009) 361, no. 25, 2449–2460, https://doi.org/10.1056/nejmra0804588, 2-s2.0-72449176846.
- 48 Hata A. and Chen Y.-G., TGF-β signaling from receptors to smads, Cold Spring Harbor Perspectives in Biology. (2016) 8, no. 9, https://doi.org/10.1101/cshperspect.a022061, 2-s2.0-84986210662.
- 49 Brown K. A., Pietenpol J. A., and Moses H. L., A tale of two proteins: differential roles and regulation of Smad2 and Smad3 in TGF-β signaling, Journal of Cellular Biochemistry. (2007) 101, no. 1, 9–33, https://doi.org/10.1002/jcb.21255, 2-s2.0-34247539528.
- 50 Zhao S., Venkatasubbarao K., Lazor J. W. et al., Inhibition of STAT3Tyr705 phosphorylation by Smad4 suppresses transforming growth factor -mediated invasion and metastasis in pancreatic cancer cells, Cancer Research. (2008) 68, no. 11, 4221–4228, https://doi.org/10.1158/0008-5472.CAN-07-5123, 2-s2.0-49249095430.
- 51 Xiong H., Hong J., Du W. et al., Roles of STAT3 and ZEB1 proteins in E-cadherin down-regulation and human colorectal cancer epithelial-mesenchymal transition, Journal of Biological Chemistry. (2012) 287, no. 8, 5819–5832, https://doi.org/10.1074/jbc.M111.295964, 2-s2.0-84863115473.
- 52 Reinacher-schick A., Baldus S. E., Romdhana B. et al., Loss of Smad4 correlates with loss of the invasion suppressor E-cadherin in advanced colorectal carcinomas, The Journal of Pathology. (2004) 202, no. 4, 412–420, https://doi.org/10.1002/path.1516, 2-s2.0-11144358223.
- 53 Ahmad R., Kumar B., Chen Z. et al., Loss of claudin-3 expression induces IL6/gp130/Stat3 signaling to promote colon cancer malignancy by hyperactivating Wnt/β-catenin signaling, Oncogene. (2017) 36, no. 47, 6592–6604, https://doi.org/10.1038/onc.2017.259, 2-s2.0-85035030283.
- 54 Mi L., Zhu F., Yang X. et al., The metastatic suppressor NDRG1 inhibits EMT, migration and invasion through interaction and promotion of caveolin-1 ubiquitylation in human colorectal cancer cells, Oncogene. (2017) 36, no. 30, 4323–4335, https://doi.org/10.1038/onc.2017.74, 2-s2.0-85016116740.
- 55 Jin R., Liu W., Menezes S. et al., The metastasis suppressor NDRG1 modulates the phosphorylation and nuclear translocation of -catenin through mechanisms involving FRAT1 and PAK4, Journal of Cell Science. (2014) 127, no. 14, 3116–3130, https://doi.org/10.1242/jcs.147835, 2-s2.0-84904350451.
- 56 Kovacevic Z., Menezes S. V., Sahni S. et al., The metastasis suppressor, N-MYC downstream-regulated gene-1 (NDRG1), down-regulates the ErbB family of receptors to inhibit downstream oncogenic signaling pathways, Journal of Biological Chemistry. (2016) 291, no. 3, 1029–1052, https://doi.org/10.1074/jbc.M115.689653, 2-s2.0-84954504741.
- 57 Sahni S., Bae D.-H., Lane D. J. R. et al., The metastasis suppressor, N-myc Downstream-regulated gene 1 (NDRG1), inhibits stress-induced autophagy in cancer cells, Journal of Biological Chemistry. (2014) 289, no. 14, 9692–9709, https://doi.org/10.1074/jbc.M113.529511, 2-s2.0-84898065350.
- 58 Kovacevic Z. and Richardson D. R., The metastasis suppressor, Ndrg-1: a new ally in the fight against cancer, Carcinogenesis. (2006) 27, no. 12, 2355–2366, https://doi.org/10.1093/carcin/bgl146, 2-s2.0-33845358660.
- 59 Mao Z., Sun J., Feng B. et al., The metastasis suppressor, N-myc downregulated gene 1 (NDRG1), is a prognostic biomarker for human colorectal cancer, PLoS One. (2013) 8, no. 7, e68206, https://doi.org/10.1371/journal.pone.0068206, 2-s2.0-84879979807.
- 60 Suman S., Kurisetty V., Das T. P. et al., Activation of AKT signaling promotes epithelial-mesenchymal transition and tumor growth in colorectal cancer cells, Molecular Carcinogenesis. (2014) 53, no. S1, E151–E160, https://doi.org/10.1002/mc.22076, 2-s2.0-84894445272.
- 61 Katoh M. and Katoh M., Cross-talk of WNT and FGF signaling pathways at GSK3ß to regulate ß-catenin and SNAIL signaling cascades, Cancer Biology and Therapy. (2006) 5, no. 9, 1059–1064, https://doi.org/10.4161/cbt.5.9.3151, 2-s2.0-33751073938.
- 62 Shimokawa T., Furukawa Y., Sakai M., Li M., Miwa N., and Lin Y., Advances in brief involvement of the FGF18 gene in colorectal carcinogenesis , as a novel downstream target of the  -catenin/T-cell factor complex 1, Cancer Research. (2003) 6116–6120.
- 63 Weis S. M. and Cheresh D. A., Tumor angiogenesis: molecular pathways and therapeutic targets, Nature Medicine. (2011) 17, no. 11, 1359–1370, https://doi.org/10.1038/nm.2537, 2-s2.0-81255188940.
- 64 Li J., Ji Z., Qiao C., Qi Y., and Shi W., Overexpression of ADAM9 promotes colon cancer cells invasion, Journal of Investigative Surgery. (2013) 26, no. 3, 127–133, https://doi.org/10.3109/08941939.2012.728682.
- 65 Mazzocca A., Coppari R., De Franco R. et al., A secreted form of ADAM9 promotes carcinoma invasion through tumor-stromal interactions, Cancer Research. (2005) 65, no. 11, 4728–4738, https://doi.org/10.1158/0008-5472.CAN-04-4449, 2-s2.0-19644367756.
- 66 Dong Y., Wu Z., He M. et al., ADAM9 mediates the interleukin-6-induced Epithelial-Mesenchymal transition and metastasis through ROS production in hepatoma cells, Cancer Letters. (2018) 421, 1–14, https://doi.org/10.1016/j.canlet.2018.02.010, 2-s2.0-85042218835.
- 67 Lin C.-Y., Chen H.-J., Huang C.-C. et al., ADAM9 promotes lung cancer metastases to brain by a plasminogen activator-based pathway, Cancer Research. (2014) 74, no. 18, 5229–5243, https://doi.org/10.1158/0008-5472.CAN-13-2995, 2-s2.0-84907486062.
- 68 Scherl-Mostageer M., Sommergruber W., Abseher R., Hauptmann R., Ambros P., and Schweifer N., Identification of a novel gene, CDCP1, overexpressed in human colorectal cancer, Oncogene. (2001) 20, no. 32, 4402–4408, https://doi.org/10.1038/sj.onc.1204566, 2-s2.0-0035913186.
- 69 Heublein S., Albertsmeier M., Pfeifer D. et al., Association of differential miRNA expression with hepatic vs. peritoneal metastatic spread in colorectal cancer, BMC Cancer. (2018) 18, no. 1, 1–10, https://doi.org/10.1186/s12885-018-4043-0, 2-s2.0-85042532045.
- 70 Ling M., Liu C., Liang S., and Kang X., miR-200c inhibits invasion and migration in human colon cancer cells SW480/620 by targeting ZEB1, Clinical and Experimental Metastasis. (2012) 29, no. 5, 457–469, https://doi.org/10.1007/s10585-012-9463-7, 2-s2.0-84862325783.
- 71 Gregory P. A., Bert A. G., Paterson E. L. et al., The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1, Nature Cell Biology. (2008) 10, no. 5, 593–601, https://doi.org/10.1038/ncb1722, 2-s2.0-43049103824.
- 72 Chang C.-J., Chao C.-H., Xia W. et al., p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs, Nature Cell Biology. (2011) 13, no. 3, 317–323, https://doi.org/10.1038/ncb2173, 2-s2.0-79952283482.
- 73 Hur K., Toiyama Y., Takahashi M. et al., MicroRNA-200c modulates epithelial-to-mesenchymal transition (EMT) in human colorectal cancer metastasis, Gut. (2014) 62, no. 9, 1315–1326, https://doi.org/10.1136/gutjnl-2011-301846, 2-s2.0-84881551103.
- 74 Siemens H., Neumann J., Jackstadt R. et al., Detection of miR-34a promoter methylation in combination with elevated expression of c-met and -catenin predicts distant metastasis of colon cancer, Clinical Cancer Research. (2013) 19, no. 3, 710–720, https://doi.org/10.1158/1078-0432.CCR-12-1703, 2-s2.0-84873373140.
- 75 Ma W., Liu B., Li J. et al., MicroRNA-302c represses epithelial-mesenchymal transition and metastasis by targeting transcription factor AP-4 in colorectal cancer, Biomedicine and Pharmacotherapy. (2018) 105, 670–676, https://doi.org/10.1016/J.BIOPHA.2018.06.025, 2-s2.0-85048265180.
- 76 Shi L., Jackstadt R., Siemens H., Li H., Kirchner T., and Hermeking H., P53-induced miR-15a/16-1 and AP4 form a double-negative feedback loop to regulate epithelial-mesenchymal transition and metastasis in colorectal cancer, Cancer Research. (2014) 74, no. 2, 532–542, https://doi.org/10.1158/0008-5472.CAN-13-2203, 2-s2.0-84892923276.
- 77 Meng Q., Chen Y., Lian B., Shang Y., and Yang H., miR-218 promotes apoptosis of SW1417 human colon cancer cells by targeting c-FLIP, Oncology Reports. (2018) 40, no. 2, 916–922, https://doi.org/10.3892/or.2018.6460, 2-s2.0-85048959316.
- 78 Asangani I. A., Rasheed S. A. K., Nikolova D. A. et al., MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer, Oncogene. (2008) 27, no. 15, 2128–2136, https://doi.org/10.1038/sj.onc.1210856, 2-s2.0-41749113108.
- 79 Yang M.-H., Yu J., Chen N. et al., Elevated microRNA-31 expression regulates colorectal cancer progression by repressing its target gene SATB2, PLoS One. (2013) 8, no. 12, e85353, https://doi.org/10.1371/journal.pone.0085353, 2-s2.0-84893631835.
- 80 Dimova I., Popivanov G., and Djonov V., Angiogenesis in cancer-general pathways and their therapeutic implications, Journal of BUON. (2014) 19, no. 1, 15–21, https://doi.org/10.7892/boris.83821.
- 81 Semenza G. L., Signal transduction to hypoxia-inducible factor 1, Biochemical Pharmacology. (2002) 64, no. 5-6, 993–998, https://doi.org/10.1016/S0006-2952(02)01168-1, 2-s2.0-0036710591.
- 82 Mariani F., Sena P., and Roncucci L., Inflammatory pathways in the early steps of colorectal cancer development, World Journal of Gastroenterology. (2014) 20, no. 29, 9716–9731, https://doi.org/10.3748/wjg.v20.i29.9716, 2-s2.0-84905828174.
- 83 Ferrara N. and Davis-Smyth T., The biology of vascular endothelial growth factor, Endocrine Reviews. (1997) 18, no. 1, 4–25, https://doi.org/10.1210/er.18.1.4.
- 84 Maishi N. and Hida K., Tumor endothelial cells accelerate tumor metastasis, Cancer Science. (2017) 108, no. 10, 1921–1926, https://doi.org/10.1111/cas.13336, 2-s2.0-85030158304.
- 85 Peña M. M. O., IL-33 promotes growth and liver metastasis of colorectal cancer in mice by remodeling the tumor microenvironment and inducing angiogenesis, Molecular Carcinogenesis. (2017) 56, no. 1, 272–287, https://doi.org/10.1002/mc.22491, 2-s2.0-85002369621.
- 86 Albini A., Bruno A., Noonan D. M., and Mortara L., Contribution to tumor angiogenesis from innate immune cells within the tumor microenvironment: implications for immunotherapy, Frontiers in Immunology. (2018) 9, https://doi.org/10.3389/fimmu.2018.00527, 2-s2.0-85045005911.
- 87 Wei W., Mok S. C., Oliva E., Kim S.-h., Mohapatra G., and Birrer M. J., FGF18 as a prognostic and therapeutic biomarker in ovarian cancer, Journal of Clinical Investigation. (2013) 123, no. 10, 4435–4448, https://doi.org/10.1172/JCI70625, 2-s2.0-84885056979.
- 88 Zhu W., Gliddon B. L., Jarman K. E. et al., CIB1 contributes to oncogenic signalling by Ras via modulating the subcellular localisation of sphingosine kinase 1, Oncogene. (2017) 36, no. 18, 2619–2627, https://doi.org/10.1038/onc.2016.428, 2-s2.0-85004154221.
- 89 Armacki M., Joodi G., Nimmagadda S. C. et al., A novel splice variant of calcium and integrin-binding protein 1 mediates protein kinase D2-stimulated tumour growth by regulating angiogenesis, Oncogene. (2014) 33, no. 9, 1167–1180, https://doi.org/10.1038/onc.2013.43, 2-s2.0-84896689604.
- 90 Puca R. and Nardinocchi L., Regulation of vascular endothelial growth factor expression by homeodomain-interacting protein kinase-2, Journal of Experimental and Clinical Cancer Research. (2008) 27, no. 22, 1–10, https://doi.org/10.1186/1756-9966-27-22, 2-s2.0-52949128032.
- 91 Aiello N. M., Bajor D. L., Norgard R. J. et al., Metastatic progression is associated with dynamic changes in the local microenvironment, Nature Communications. (2016) 7, no. 1, 1–9, https://doi.org/10.1038/ncomms12819, 2-s2.0-84987786814.
- 92 Rhim A. D., Oberstein P. E., Thomas D. H. et al., Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma, Cancer Cell. (2014) 25, no. 6, 735–747, https://doi.org/10.1016/j.ccr.2014.04.021, 2-s2.0-84902435628.
- 93
Huang Z. and
Feng Y., Exosomes derived from hypoxic colorectal cancer cells promote angiogenesis through Wnt4-induced β-catenin signaling in endothelial cells, Oncology Research Featuring Preclinical and Clinical Cancer Therapeutics. (2017) 25, no. 5, 651–661, https://doi.org/10.3727/096504016x14752792816791, 2-s2.0-85019682359.
10.3727/096504016X14752792816791 Google Scholar
- 94 Takeda A., Stoeltzing O., Ahmad S. A. et al., Role of angiogenesis in the development and growth of liver metastasis, Annals of Surgical Oncology. (2002) 9, no. 7, 610–616, https://doi.org/10.1007/bf02574475.
- 95 Kaplan R. N., Riba R. D., Zacharoulis S. et al., VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche, Nature. (2005) 438, no. 7069, 820–827, https://doi.org/10.1038/nature04186, 2-s2.0-28644432204.
- 96 Kaplan R. N., Rafii S., and Lyden D., Preparing the “soil”: the premetastatic niche, Cancer Research. (2006) 66, no. 23, 11089–11093, https://doi.org/10.1158/0008-5472.CAN-06-2407, 2-s2.0-33845811455.
- 97 Wal G. E. V. D., Gouw A. S. H., Moorlag H. E., and Bulthuis M. L. C., Angiogenesis in synchronous and metachronous colorectal liver metastases: the liver as a permissive soil, Annals of Surgery. (2012) 255, no. 1, 86–94, https://doi.org/10.1097/SLA.0b013e318238346a, 2-s2.0-84155163058.
- 98 Lemoine L., Sugarbaker P., and Van Der Speeten K., Pathophysiology of colorectal peritoneal carcinomatosis: role of the peritoneum, World Journal of Gastroenterology. (2016) 22, no. 34, 7692–7707, https://doi.org/10.3748/wjg.v22.i34.7692, 2-s2.0-84988566175.
- 99
George S. K.,
Theofilos P.,
Susan E. E.,
Richard K.,
Robert H. R., and
Eleftherios P. D., Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue, Molecular Cancer Research. (2015) 10, no. 11, 1403–1418, https://doi.org/10.1158/1541-7786.MCR-12-0307.Cancer-Associated.
10.1158/1541-7786.MCR-12-0307.Cancer-Associated Google Scholar
- 100 Mikuła-Pietrasik J., Uruski P., Tykarski A., and Książek K., The peritoneal “soil” for a cancerous “seed”: a comprehensive review of the pathogenesis of intraperitoneal cancer metastases, Cellular and Molecular Life Sciences. (2018) 75, no. 3, 509–525, https://doi.org/10.1007/s00018-017-2663-1, 2-s2.0-85030092770.
- 101 Marcuello M., Mayol X., Felipe-Fumero E. et al., Modulation of the colon cancer cell phenotype by pro-inflammatory macrophages: a preclinical model of surgery-associated inflammation and tumor recurrence, PLoS One. (2018) 13, no. 2, e0192958, https://doi.org/10.1371/journal.pone.0192958, 2-s2.0-85042453029.
- 102 Li Y., Wang L., Pappan L., Galliher-Beckley A., and Shi J., IL-1β promotes stemness and invasiveness of colon cancer cells through Zeb1 activation, Molecular Cancer. (2012) 11, no. 1, https://doi.org/10.1186/1476-4598-11-87, 2-s2.0-84869875206.
- 103 Calon A., Espinet E., Palomo-Ponce S. et al., Dependency of colorectal cancer on a TGF-β-driven program in stromal cells for metastasis initiation, Cancer Cell. (2012) 22, no. 5, 571–584, https://doi.org/10.1016/j.ccr.2012.08.013, 2-s2.0-84869021181.
- 104 Rokavec M., Öner M. G., Li H. et al., IL-6R/STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis, Journal of Clinical Investigation. (2014) 124, no. 4, 1853–1867, https://doi.org/10.1172/JCI73531DS1.
- 105 Brighenti E., Calabrese C., Liguori G. et al., Interleukin 6 downregulates p53 expression and activity by stimulating ribosome biogenesis: a new pathway connecting inflammation to cancer, Oncogene. (2014) 33, no. 35, 4396–4406, https://doi.org/10.1038/onc.2014.1, 2-s2.0-85027946414.
- 106 Cheng X.-S., Li Y.-F., Tan J. et al., CCL20 and CXCL8 synergize to promote progression and poor survival outcome in patients with colorectal cancer by collaborative induction of the epithelial-mesenchymal transition, Cancer Letters. (2014) 348, no. 1-2, 77–87, https://doi.org/10.1016/j.canlet.2014.03.008, 2-s2.0-84900500082.
- 107 Bates R. C., DeLeo M. J., and Mercurio A. M., The epithelial-mesenchymal transition of colon carcinoma involves expression of IL-8 and CXCR-1-mediated chemotaxis, Experimental Cell Research. (2004) 299, no. 2, 315–324, https://doi.org/10.1016/j.yexcr.2004.05.033, 2-s2.0-4444319419.
- 108 Wang H., Wang H.-S., Zhou B.-H. et al., Epithelial-mesenchymal transition (EMT) induced by TNF-α requires AKT/GSK-3β-Mediated stabilization of snail in colorectal cancer, PLoS One. (2013) 8, no. 2, e56664, https://doi.org/10.1371/journal.pone.0056664, 2-s2.0-84874217880.
- 109 Itatani Y., Kawada K., Fujishita T. et al., Loss of SMAD4 from colorectal cancer cells promotes CCL15 expression to recruit CCR1+ myeloid cells and facilitate liver metastasis, Gastroenterology. (2013) 145, no. 5, 1064–1075, https://doi.org/10.1053/j.gastro.2013.07.033, 2-s2.0-84886789666.
- 110 Kojima M., Higuchi Y., Yokota M. et al., Human subperitoneal fibroblast and cancer cell interaction creates microenvironment that enhances tumor progression and metastasis, PLoS One. (2014) 9, no. 2, e88018, https://doi.org/10.1371/journal.pone.0088018, 2-s2.0-84895088632.
- 111 Kitayama J., Emoto S., Yamaguchi H., Ishigami H., and Watanabe T., CD90(+) mesothelial-like cells in peritoneal fluid promote peritoneal metastasis by forming a tumor permissive microenvironment, PLoS One. (2014) 9, no. 1, e86516, https://doi.org/10.1371/journal.pone.0086516, 2-s2.0-84907020981.
- 112 Zhang Y., Nowicka A., Solley T. N. et al., Stromal cells derived from visceral and obese adipose tissue promote growth of ovarian cancers, PLoS One. (2015) 10, no. 8, e0136361, https://doi.org/10.1371/journal.pone.0136361, 2-s2.0-84943339748.
- 113 Sluiter N., de Cuba E., Kwakman R., Kazemier G., Meijer G., and te Velde E. A., Adhesion molecules in peritoneal dissemination: function, prognostic relevance and therapeutic options, Clinical and Experimental Metastasis. (2016) 33, no. 5, 401–416, https://doi.org/10.1007/s10585-016-9791-0, 2-s2.0-84963679488.
- 114 De Cuba E. M. V., Kwakman R., Van Egmond M. et al., Understanding molecular mechanisms in peritoneal dissemination of colorectal cancer, Virchows Archiv. (2012) 461, no. 3, 231–243, https://doi.org/10.1007/s00428-012-1287-y, 2-s2.0-84867399679.
- 115 Lambert A. W., Pattabiraman D. R., and Weinberg R. A., Emerging biological principles of metastasis, Cell. (2017) 168, no. 4, 670–691, https://doi.org/10.1016/j.cell.2016.11.037, 2-s2.0-85012054684.
- 116 Sakamoto M., Takamura M., Ino Y., Miura A., Genda T., and Hirohashi S., Involvement of c-src in carcinoma cell motility and metastasis, Japanese Journal of Cancer Research. (2001) 92, no. 9, 941–946, https://doi.org/10.1111/j.1349-7006.2001.tb01184.x, 2-s2.0-0034796912.
- 117 Sasaki S., Ueda M., Iguchi T. et al., DDR2 expression is associated with a high frequency of peritoneal dissemination and poor prognosis in colorectal cancer, Anticancer Research. (2017) 37, no. 5, 2587–2591, https://doi.org/10.21873/anticanres.11603, 2-s2.0-85019054973.