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Pericytes Relationship with Cancer Stem Cells in the Colon

  • Pericytes (A Birbrair, Section Editor)
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Abstract

Purpose of Review

Stand out contribution of pericytes and cancer stem cells (CSC) to progression of colorectal cancer (CRC).

Recent Findings

Reported that CSC are responsible for the initiation and spread of the tumor; however, the microenvironment in the tumor plays a decisive role in prognosis; CSC and pericytes interaction are capable of contributing to neovascularization and promoting metastasis. We reviewed the contribution of cellular communication between pericytes, endothelial cells, and CSC with focus vascular remodeling, metastasis, angiogenesis, and vasculogenesis. Also, we were analyzed concise microRNAs and approved therapeutic target with the potential anti-angiogenic as treatment of CRC.

Summary

This work seeks to give an overview of pericytes in cancer and their role angiogenic with CSC in CRC.

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References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. Attwell D, Mishra A, Hall CN, O’Farrell FM, Dalkara T. What is a pericyte? J Cereb Blood Flow Metab. 2016;36(2):451–5.

    CAS  PubMed  Google Scholar 

  2. Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011;21:193–215.

    CAS  PubMed  Google Scholar 

  3. Birbrair A, Zhang T, Wang ZM, Messi ML, Mintz A, Delbono O. Pericytes at the intersection between tissue regeneration and pathology. Clin Sci. 2015;128(2):81–93.

    CAS  Google Scholar 

  4. Hellström M, Kalén M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development. 1999;126(14):3047–55.

    PubMed  Google Scholar 

  5. Ozerdem U, Stallcup WB. Early contribution of pericytes to angiogenic sprouting and tube formation. In: Angiogenesis. 2003. p. 241–9.

  6. Jiang T, Zhuang J, Duan H, Luo Y, Zeng Q, Fan K, et al. CD146 is a coreceptor for VEGFR-2 in tumor angiogenesis. Blood. 2012;120(11):2330–9.

    CAS  PubMed  Google Scholar 

  7. Berger M, Bergers G, Arnold B, Hämmerling GJ, Ganss R. Regulator of G-protein signaling-5 induction in pericytes coincides with active vessel remodeling during neovascularization. Blood. 2005;105(3):1094–101.

    CAS  PubMed  Google Scholar 

  8. Hughes S, Chan-Ling T. Characterization of smooth muscle cell and pericyte differentiation in the rat retina in vivo. Investig Ophthalmol Vis Sci. 2004;45(8):2795–806.

    Google Scholar 

  9. Yamazaki T, Mukouyama Y. Tissue specific origin, development, and pathological perspectives of pericytes. Front Cardiovasc Med. 2018;27:5.

    Google Scholar 

  10. Lo HW, Zhu H, Cao X, Aldrich A, Ali-Osman F. A novel splice variant of GLI1 that promotes glioblastoma cell migration and invasion. Cancer Res. 2009;69(17):6790–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Sena IFG, Borges IT, Lousado L, Azevedo PO, Andreotti JP, Almeida VM, et al. LepR+ cells dispute hegemony with Gli1+ cells in bone marrow fibrosis. Cell Cycle. 2017;16(21):2018–22.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Wu SP, Dong XR, Regan JN, Su C, Majesky MW. Tbx18 regulates development of the epicardium and coronary vessels. Dev Biol. 2013;383(2):307–20.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. •• Harrell CR, Simovic Markovic B, Fellabaum C, Arsenijevic A, Djonov V, Volarevic V. Molecular mechanisms underlying therapeutic potential of pericytes. J Biomed Sci. 2018;25. Excellent summarises the characteristics of pericytes.

  14. Payne LB, Zhao H, James CC, Darden J, McGuire D, Taylor S, et al. The pericyte microenvironment during vascular development. Microcirculation. 2019;26(8). Available from: https://onlinelibrary.wiley.com/doi/abs/10.1111/micc.12554. [cited 2020 Jan 21].

  15. Thomas HM, Cowin AJ, Mills SJ. The importance of pericytes in healing: wounds and other pathologies. Int J Mol Sci. 2017;18.

  16. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–11.

    CAS  PubMed  Google Scholar 

  17. Phi LTH, Sari IN, Yang YG, Lee SH, Jun N, Kim KS, et al. Cancer stem cells (CSCs) in drug resistance and their therapeutic implications in cancer treatment. Stem Cells Int. 2018;2018.

  18. Glumac PM, LeBeau AM. The role of CD133 in cancer: a concise review. Clin Transl Med. 2018;7(1).

  19. Fanali C, Lucchetti D, Farina M, Corbi M, Cufino V, Cittadini A, et al. Cancer stem cells in colorectal cancer from pathogenesis to therapy: controversies and perspectives. World J Gastroenterol. 2014;20(4):923–42.

    PubMed  PubMed Central  Google Scholar 

  20. Garza-Trevino EN, Rodriguez-Gonzalez MS, Delgado Gonzalez P, Alonso-Cruz YG, Alonso-Cruz YG, Soto-Dominguez A, et al. Remarkably higher efficacy and a wider safety window for nonfrontline over first-line drug combinations in the adenocarcinoma Colo 320DM cell line. J Buon. 22(5):1115–21. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29135091. [cited 2020 Feb 7].

  21. •• Nguyen LH, Goel A, Chung DC. Pathways of colorectal carcinogenesis. Gastroenterology. 2019. This paper summarises genetic changes associated with the development colorectal cancer.

  22. Cheng X, Xu X, Chen D, Zhao F, Wang W. Therapeutic potential of targeting the Wnt/β-catenin signaling pathway in colorectal cancer. Biomed Pharmacother. 2019;110:473–81. Available from: https://www.sciencedirect.com/science/article/pii/S0753332218355744?via%3Dihub. [cited 2019 Jun 1].

    CAS  PubMed  Google Scholar 

  23. Phelps RA, Chidester S, Dehghanizadeh S, Phelps J, Sandoval IT, Rai K, et al. A two-step model for colon adenoma initiation and progression caused by APC loss. Cell. 2009;137(4):623–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Armaghany T, Wilson JD, Chu Q, Mills G. Genetic alterations in colorectal cancer. Gastrointest Cancer Res. 2012;5:19–27.

  25. Pelullo M, Zema S, Nardozza F, Checquolo S, Screpanti I, Bellavia D. Wnt, Notch, and TGF-β pathways impinge on hedgehog signaling complexity: an open window on cancer. Front Genet. 2019;10.

  26. Cathomas G. PIK3CA in colorectal cancer. Vol. 4 Front Oncol; 2014.

  27. Vu T, Datta PK. Regulation of EMT in colorectal cancer: a culprit in metastasis, vol. 9: Cancers; 2017.

  28. Pedrosa L, Esposito F, Thomson TM, Maurel J. The tumor microenvironment in colorectal cancer therapy. Cancers. 2019;11.

  29. Yun JA, Kim SH, Hong HK, Yun SH, Kim HC, Chun HK, et al. Loss of E-cadherin expression is associated with a poor prognosis in stage III colorectal cancer. Oncology. 2014;86(5–6):318–28.

    CAS  PubMed  Google Scholar 

  30. Bocci F, Tripathi SC, Vilchez Mercedes SA, George JT, Casabar JP, Wong PK, et al. NRF2 activates a partial epithelial-mesenchymal transition and is maximally present in a hybrid epithelial/mesenchymal phenotype. Integr Biol (Camb). 2019;11(6):251–63.

    Google Scholar 

  31. Lu J, Shenoy AK. Epithelial-to-pericyte transition in cancer. Cancers. 2017;9.

  32. Manzat Saplacan RM, Balacescu L, Gherman C, Chira RI, Craiu A, Mircea PA, et al. The role of PDGFs and PDGFRs in colorectal cancer. 2017;2017.

  33. Garza Treviño EN, González PD, Valencia Salgado CI, Martinez GA. Effects of pericytes and colon cancer stem cells in the tumor microenvironment. Cancer Cell Int. 2019;19.

  34. Ribeiro AL, Okamoto OK. Combined effects of pericytes in the tumor microenvironment. Stem Cells Int. 2015;2015:1–8.

    Google Scholar 

  35. Chen Z, Xu XH, Hu J. Role of pericytes in angiogenesis: focus on cancer angiogenesis and anti-angiogenic therapy. Neoplasma. 2016;63:173–82.

  36. Jiang C, Huang YH, Lu JB, Yang YZ, Rao HL, Zhang B, et al. Perivascular cell coverage of intratumoral vasculature is a predictor for bevacizumab efficacy in metastatic colorectal cancer. Cancer Manag Res. 2018;10:3589–97.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Garza-Treviño EN, Said-Fernández SL, Martínez-Rodríguez HG. Understanding the colon cancer stem cells and perspectives on treatment. Cancer Cell Int. 2015;15(1):1–9.

    Google Scholar 

  38. Paiva AE, Lousado L, Guerra DAP, Azevedo PO, Sena IFG, Andreotti JP, et al. Pericytes in the premetastatic niche. Cancer Res. 2018;78(11):2779–86. Available from: http://cancerres.aacrjournals.org/lookup/doi/10.1158/0008-5472.CAN-17-3883.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Quintero-Fabián S, Arreola R, Becerril-Villanueva E, Torres-Romero JC, Arana-Argáez V, Lara-Riegos J, et al. Role of matrix metalloproteinases in angiogenesis and cancer. Front Oncol. 2019;9. Available from: https://www.frontiersin.org/article/10.3389/fonc.2019.01370/full.

  40. Chen Y, Song Y, Du W, Gong L, Chang H, Zou Z. Tumor-associated macrophages: an accomplice in solid tumor progression. J Biomed Sci. 2019;26.

  41. Zonneville J, Safina A, Truskinovsky AM, Arteaga CL, Bakin AV. TGF-β signaling promotes tumor vasculature by enhancing the pericyte-endothelium association. BMC Cancer. 2018;19, 18(1).

  42. Falcón BL, Hashizume H, Koumoutsakos P, Chou J, Bready JV, Coxon A, et al. Contrasting actions of selective inhibitors of angiopoietin-1 and angiopoietin-2 on the normalization of tumor blood vessels. Am J Pathol. 2009;175(5):2159–70.

    PubMed  PubMed Central  Google Scholar 

  43. Akwii RG, Sajib MS, Zahra FT, Mikelis CM. Role of angiopoietin-2 in vascular physiology and pathophysiology. Cells. 2019;8(5):471.

    CAS  PubMed Central  Google Scholar 

  44. •• McCarty MF, Somcio RJ, Stoeltzing O, Wey J, Fan F, Liu W, et al. Overexpression of PDGF-BB decreases colorectal and pancreatic cancer growth by increasing tumor pericyte content. J Clin Invest. 2007;117(8):2114–22. Expression of PDGF-BB rendering the tumor vasculature more resistant to angiogenic therapy.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Ribatti D. Tumor refractoriness to anti-VEGF therapy. Oncotarget. 2016;7:46668–77.

  46. Itatani Y, Kawada K, Sakai Y. Transforming growth factor-β signaling pathway in colorectal cancer and its tumor microenvironment. Int J Mol Sci. 2019;20.

  47. Calon A, Espinet E, Palomo-Ponce S, Tauriello DVF, Iglesias M, Céspedes MV, et al. Dependency of colorectal cancer on a TGF-β-driven program in stromal cells for metastasis initiation. Cancer Cell. 2012;22(5):571–84.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Tang YA, Chen Y feng, Bao Y, Mahara S, Yatim SMJM, Oguz G, et al. Hypoxic tumor microenvironment activates GLI2 via HIF-1α and TGF-β2 to promote chemoresistance in colorectal cancer. Proc Natl Acad Sci U S A 2018;115(26):E5990–E5999.

  49. Comunanza V, Bussolino F. Therapy for cancer: strategy of combining anti-angiogenic and target therapies. Front Cell Dev Biol. 2017;5.

  50. Pieterse Z, Sinha D, Kaur P. Pericytes in metastasis. In: Advances in experimental medicine and biology. New York: Springer; 2019. p. 125–35.

    Google Scholar 

  51. Hong Y, Fang F, Zhang Q. Circulating tumor cell clusters: what we know and what we expect (Review). Int J Oncol. 2016;49:2206–16.

  52. Teicher BA. CD248: a therapeutic target in cancer and fibrotic diseases. Oncotarget. 2019;10:993–1009.

  53. Kim B, Yoon J, Yoon SW, Park B. Onbaekwon suppresses colon cancer cell invasion by inhibiting expression of the CXC chemokine receptor 4. Integr Cancer Ther. 2017;16(2):244–51.

    PubMed  Google Scholar 

  54. Reymond N, D’Agua BB, Ridley AJ. Crossing the endothelial barrier during metastasis. Nat Rev Cancer. 2013;13:858–70.

  55. Platel V, Faure S, Corre I, Clere N. Endothelial-to-mesenchymal transition (EndoMT): roles in tumorigenesis, metastatic extravasation and therapy resistance. J Oncol. 2019;2019.

  56. Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell. 2011;20(5):576–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Schumacher D, Strilic B, Sivaraj KK, Wettschureck N, Offermanns S. Platelet-derived nucleotides promote tumor-cell transendothelial migration and metastasis via P2Y2 receptor. Cancer Cell. 2013;24(1):130–7.

    CAS  PubMed  Google Scholar 

  58. Massagué J, Obenauf AC. Metastatic colonization by circulating tumour cells. Nature. 2016;529:298–306.

  59. Murgai M, Ju W, Eason M, Kline J, Beury DW, Kaczanowska S, et al. KLF4-dependent perivascular cell plasticity mediates pre-metastatic niche formation and metastasis. Nat Med. 2017;23(10):1176–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Szade K, Gulati GS, Chan CKF, Kao KS, Miyanishi M, Marjon KD, et al. Where hematopoietic stem cells live: the bone marrow niche. Antioxid Redox Signal. 2018;29:191–204.

  61. •• Chiaverina G, di Blasio L, Monica V, Accardo M, Palmiero M, Peracino B, et al. Dynamic interplay between pericytes and endothelial cells during sprouting angiogenesis. Cells. 2019;8(9):1109. This paper using mouse models ex vivo for angiogenesis assay can studied interactions between ECs and pericytes and demostrate pericytes originate from mitotic events and can be recruited on the developing sprout by proliferation, migrate independently from endothelial cells, but also actively proliferate on the capillary-like structure.

    CAS  PubMed Central  Google Scholar 

  62. •• Li X, Li Y, Lu W, Chen M, Ye W, Zhang D. The tumor vessel targeting strategy: a double-edged sword in tumor metastasis. Cells. 2019;8(12):1602. Available from: https://www.mdpi.com/2073-4409/8/12/1602. [cited 2020 Jan 24]. This paper summarises contribution of angiogenesis to tumor metastasis.

    CAS  PubMed Central  Google Scholar 

  63. Barlow KD, Sanders AM, Soker S, Ergun S, Metheny-Barlow LJ. Pericytes on the tumor vasculature: Jekyll or hyde? Cancer Microenviron. 2013;6:1–17.

  64. •• Ziyad S, Iruela-Arispe ML. Molecular mechanisms of tumor angiogenesis. genes and cancer. 2011;2(12):1085–96. Excellent review highlighting the types of tumor vessels.

  65. Nagy JA, Dvorak HF. Heterogeneity of the tumor vasculature: the need for new tumor blood vessel type-specific targets. In: Clinical and experimental metastasis; 2012. p. 657–62.

    Google Scholar 

  66. •• Bendardaf R, El-Serafi A, Syrjänen K, Collan Y, Pyrhönen S. The effect of vascular endothelial growth factor-1 expression on survival of advanced colorectal cancer patients. Libyan J Med. 2017;12(1). Relation between expression of VEGF in biopsies, development of neovascularitation and metastasis.

  67. Chen WZ, Jiang JX, Yu XY, Xia WJ, Yu PX, Wang K, et al. Endothelial cells in colorectal cancer. World J Gastrointest Oncol. 2019;11:946–56.

  68. Shangguan W, Fan C, Chen X, Lu R, Liu Y, Li Y, et al. Endothelium originated from colorectal cancer stem cells constitute cancer blood vessels. Cancer Sci. 2017;108(7):1357–67.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Liu Z, Qi L, Li Y, Zhao X, Sun B. VEGFR2 regulates endothelial differentiation of colon cancer cells. BMC Cancer. 2017;30:17(1).

    Google Scholar 

  70. •• Fernández-Cortés M, Delgado-Bellido D, Javier OF. Vasculogenic mimicry: become an endothelial cell “But not so much.”. Front Oncol. 2019;9. Importance of tumor microenviroment in vascular mimicry acquisition and discribe terapeutic targets.

  71. Upile T, Jerjes W, Radhi H, Al-Khawalde M, Kafas P, Nouraei S, et al. Vascular mimicry in cultured head and neck tumour cell lines. Head Neck Oncol. 2011;3(1).

  72. Angara K, Borin TF, Arbab AS. Vascular Mimicry: a novel neovascularization mechanism driving anti-angiogenic therapy (AAT) resistance in glioblastoma. Transl Oncol. 2017;10:650–60.

  73. Ayala-Domínguez L, Olmedo-Nieva L, Muñoz-Bello JO, Contreras-Paredes A, Manzo-Merino J, Martínez-Ramírez I, et al. Mechanisms of vasculogenic mimicry in ovarian cancer. Front Oncol. 2019;9.

  74. Zhang Z, Imani S, Shasaltaneh MD, Hosseinifard H, Zou L, Fan Y, et al. The role of vascular mimicry as a biomarker in malignant melanoma: a systematic review and meta-analysis. BMC Cancer. 2019;19(1):1134. Available from: https://bmccancer.biomedcentral.com/articles/10.1186/s12885-019-6350-5.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Shen Y, Quan J, Wang M, Li S, Yang J, Lv M, et al. Tumor vasculogenic mimicry formation as an unfavorable prognostic indicator in patients with breast cancer. Oncotarget. 2017;8(34):56408–16.

    PubMed  PubMed Central  Google Scholar 

  76. Guo Q, Yuan Y, Jin Z, Xu T, Gao Y, Wei H, et al. Association between tumor vasculogenic mimicry and the poor prognosis of gastric cancer in China: an updated systematic review and meta-analysis. Biomed Res Int. 2016;2016.

  77. Li W, Ng JMK, Wong CC, Ng EKW, Yu J. Molecular alterations of cancer cell and tumour microenvironment in metastatic gastric cancer. Oncogene. 2018;37:4903–20.

  78. Donadon M, Lleo A, Di Tommaso L, Soldani C, Franceschini B, Roncalli M, et al. The shifting paradigm of prognostic factors of colorectal liver metastases: from tumor-centered to host immune-centered factors. Front Oncol. 2018;8.

  79. •• Cao Z, Bao M, Miele L, Sarkar FH, Wang Z, Zhou Q. Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer. 2013;49(18):3914–23. Vascular mimicry positive cancer patients show poor overall survival particulary in metastatic cancer.

    PubMed  Google Scholar 

  80. Ge H, Luo H. Overview of advances in vasculogenic mimicry – a potential target for tumor therapy. Cancer Manag Res. 2018;10:2429–37.

  81. •• Thijssen VLJL, Paulis YWJ, Nowak-Sliwinska P, Deumelandt KL, Hosaka K, Soetekouw PMMB, et al. Targeting PDGF-mediated recruitment of pericytes blocks vascular mimicry and tumor growth. J Pathol. 2018;246(4):447–58. Pericytes are important in vascular mimicry, facilitating sprouting, and structural support of the vascular-like networks.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Stratman AN, Davis GE. Endothelial cell-pericyte interactions stimulate basement membrane matrix assembly: influence on vascular tube remodeling, maturation, and stabilization. In: Microscopy and microanalysis. 2012. p. 68–80.

  83. Guyot M, Hilmi C, Ambrosetti D, Merlano M, Lo Nigro C, Durivault J, et al. Targeting the pro-angiogenic forms of VEGF or inhibiting their expression as anti-cancer strategies. Oncotarget. 2017;8(6):9174–88.

    PubMed  Google Scholar 

  84. Bin MM, Zaorsky NG, Deng L, Wang HH, Chao J, Zhao LJ, et al. Pericytes: a double-edged sword in cancer therapy. Future Oncol. 2015;11:169–79.

  85. Soheilifar MH, Grusch M, Neghab HK, Amini R, Maadi H, Saidijam M, et al. Angioregulatory microRNAs in colorectal cancer. Cancers. 2020;12.

  86. Chamorro-Jorganes A, Araldi E, Suárez Y. MicroRNAs as pharmacological targets in endothelial cell function and dysfunction. Pharmacol Res. 2013;75:15–27.

  87. Geevarghese A, Herman IM. Pericyte-endothelial crosstalk: implications and opportunities for advanced cellular therapies. Transl Res. 2014;163:296–306.

  88. Wang S, Olson EN. AngiomiRs-Key regulators of angiogenesis. Curr Opin Genet Dev. 2009;19:205–11.

  89. Takahashi RU, Miyazaki H, Ochiya T. The roles of microRNAs in breast cancer. Cancers. 2015;7:598–616.

  90. Qian X, Yu J, Yin Y, He J, Wang L, Li Q, et al. MicroRNA-143 inhibits tumor growth and angiogenesis and sensitizes chemosensitivity to oxaliplatin in colorectal cancers. Cell Cycle. 2013;12(9):1385–94.

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Baraniskin A, Buchberger B, Pox C, Graeven U, Holch JW, Schmiegel W, et al. Efficacy of bevacizumab in first-line treatment of metastatic colorectal cancer: a systematic review and meta-analysis. Eur J Cancer. 2019;106:37–44.

    CAS  PubMed  Google Scholar 

  92. Kanat O, Ertas H. Existing anti-angiogenic therapeutic strategies for patients with metastatic colorectal cancer progressing following first-line bevacizumab-based therapy. World J Clin Oncol. 2019;10(2):52–61. Available from: https://www.wjgnet.com/2218-4333/full/v10/i2/52.htm. [cited 2020 Jan 31].

    PubMed  PubMed Central  Google Scholar 

  93. Verdaguer H, Tabernero J, Macarulla T. Ramucirumab in metastatic colorectal cancer: evidence to date and place in therapy. Ther Adv Med Oncol. 2016;8:230–42.

  94. Wu C-P, Lusvarghi S, Wang J-C, Hsiao S-H, Huang Y-H, Hung T-H, et al. Avapritinib: a selective inhibitor of KIT and PDGFRα that reverses ABCB1 and ABCG2-mediated multidrug resistance in cancer cell lines. Mol Pharm. 2019;16(7):3040–52. Available from: https://pubs.acs.org/doi/10.1021/acs.molpharmaceut.9b00274. [cited 2020 Jan 31].

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Hoff PM, Hochhaus A, Pestalozzi BC, Tebbutt NC, Li J, Kim TW, et al. Cediranib plus FOLFOX/CAPOX versus placebo plus FOLFOX/CAPOX in patients with previously untreated metastatic colorectal cancer: a randomized, double-blind, phase III study (HORIZON II). J Clin Oncol. 2012;30(29):3596–603.

    CAS  PubMed  Google Scholar 

  96. Aljubran A, Elshenawy MA, Kandil M, Zahir MN, Shaheen A, Gad A, et al. Efficacy of regorafenib in metastatic colorectal cancer: a multi-institutional retrospective study. Clin Med Insights. 2019;13.

  97. Tapia Rico G, Price TJ. Atezolizumab for the treatment of colorectal cancer: the latest evidence and clinical potential. Expert Opin Biol Ther. 2018;18(4):449–57.

    CAS  PubMed  Google Scholar 

  98. Van Cutsem E, Yoshino T, Lenz HJ, Lonardi S, Falcone A, Limón ML, et al. Nintedanib for the treatment of patients with refractory metastatic colorectal cancer (LUME-Colon 1): a phase III, international, randomized, placebo-controlled study. Ann Oncol. 2018;29(9):1955–63.

    PubMed  PubMed Central  Google Scholar 

  99. Wang TF, Lockhart AC. Aflibercept in the treatment of metastatic colorectal cancer. Clin Med Insights. 2012;6:19–30.

  100. •• Hidalgo M, Martinez-Garcia M, Le Tourneau C, Massard C, Garralda E, Boni V, et al. First-in-human phase i study of single-agent vanucizumab, a first-in-class bispecific anti-angiopoietin-2/anti-vegf-a antibody, in adult patients with advanced solid tumors. Clin Cancer Res. 2018;24(7):1536–45. Vancizumab impact tumor vascularity, demonstrated encouraging antitumor activity.

    CAS  PubMed  Google Scholar 

  101. Andersen SE, Andersen IB, Jensen BV, Pfeiffer P, Ota T, Larsen JS. A systematic review of observational studies of trifluridine/tipiracil (TAS-102) for metastatic colorectal cancer. Acta Oncol (Madr). 2019;58(8):1149–57.

    CAS  Google Scholar 

  102. Smith KM, Desai J. Nivolumab for the treatment of colorectal cancer. Expert Rev Anticancer Ther. 2018;18(7):611–8.

    CAS  PubMed  Google Scholar 

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Garza Treviño, E.N., Delgado-Gonzalez, P., Valencia Salgado, C.I. et al. Pericytes Relationship with Cancer Stem Cells in the Colon. Curr. Tissue Microenviron. Rep. 1, 187–198 (2020). https://doi.org/10.1007/s43152-020-00015-8

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