Heterogeneous perivascular cell coverage affects breast cancer metastasis and response to chemotherapy

JCI Insight

Volumn 1, Issue 21, 2016, Pages

  Kim, Jiha ^a   de Sampaio, Pedro Correa ^a   Lundy, Donna Marie ^a   Peng, Qian ^a   Evans, Kurt W ^a   Sugimoto, Hikaru ^a   Gagea, Mihai ^a   Kienast, Yvonne ^b   do Amaral, Nayra Soares ^c   Rocha, Rafael Malagoli ^d   Eikesdal, Hans Petter ^e,f   Lønning, Per Eystein ^e,f   Meric Bernstam, Funda ^a   LeBleu, Valerie S ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b Roche Pharmaceutical Research and Early Development (pRED)   (Germany)

^c A C CAMARGO CANCER CENTER   (Brazil)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^e UNIVERSITY OF BERGEN   (Norway)

^f HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85021932495     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.90733     Document Type: Article

References (58)

1. Li YJ, et al. Perfusion heterogeneity in breast tumors for assessment of angiogenesis. J Ultrasound Med. 2013; 32(7):1145-1155.
2. Eberhard A, Kahlert S, Goede V, Hemmerlein B, Plate KH, Augustin HG. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: implications for antiangiogenic tumor therapies. Cancer Res. 2000; 60(5):1388-1393.
3. Cooke VG, et al. Pericyte depletion results in hypoxia-associated epithelial-to-mesenchymal transition and metastasis mediated by met signaling pathway. Cancer Cell. 2012; 21(1):66-81.
4. Smith MJ, Berger RW, Minhas K, Moorehead RA, Coomber BL. Heterogeneity of vascular and progenitor cell compartments in tumours from MMTV-PyVmT transgenic mice during mammary cancer progression. Int J Exp Pathol. 2011; 92(2):106-116.
5. Senchukova MA, Nikitenko NV, Tomchuk ON, Zaitsev NV, Stadnikov AA. Different types of tumor vessels in breast cancer: morphology and clinical value. Springerplus. 2015; 4:512.
6. Pepin F, et al. Gene-expression profiling of microdissected breast cancer microvasculature identifies distinct tumor vascular subtypes. Breast Cancer Res. 2012; 14(4):R120.
7. Armulik A, Genove G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell. 2011; 21(2):193-215.
8. Edelman DA, Jiang Y, Tyburski J, Wilson RF, Steffes C. Pericytes and their role in microvasculature homeostasis. J Surg Res. 2006; 135(2):305-311.
9. Gerhardt H, Semb H. Pericytes: gatekeepers in tumour cell metastasis?. J Mol Med. 2008; 86(2):135-144.
10. Meng MB, et al. Pericytes: a double-edged sword in cancer therapy. Future Oncol. 2015; 11(1):169-179.
11. Raza A, Franklin MJ, Dudek AZ. Pericytes and vessel maturation during tumor angiogenesis and metastasis. Am J Hematol. 2010; 85(8):593-598.
12. von Tell D, Armulik A, Betsholtz C. Pericytes and vascular stability. Exp Cell Res. 2006; 312(5):623-629.
13. Huang Y, Goel S, Duda DG, Fukumura D, Jain RK. Vascular normalization as an emerging strategy to enhance cancer immunotherapy. Cancer Res. 2013; 73(10):2943-2948.
14. Jain RK. A new target for tumor therapy. N Engl J Med. 2009; 360(25):2669-2671.
15. Kerbel RS, Viloria-Petit A, Klement G, Rak J. 'Accidental' anti-angiogenic drugs. Eur J Cancer. 2000; 36(10):1248-1257.
16. Keskin D, et al. Targeting vascular pericytes in hypoxic tumors increases lung metastasis via angiopoietin-2. Cell Rep. 2015; 10(7):1066-1081.
17. Xian X, et al. Pericytes limit tumor cell metastasis. J Clin Invest. 2006; 116(3):642-651.
18. Augustin HG, Koh GY, Thurston G, Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol. 2009; 10(3):165-177.
19. Eklund L, Saharinen P. Angiopoietin signaling in the vasculature. Exp Cell Res. 2013; 319(9):1271-1280.
20. Saharinen P, et al. Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat Cell Biol. 2008; 10(5):527-537.
21. Thomas M, Augustin HG. The role of the Angiopoietins in vascular morphogenesis. Angiogenesis. 2009; 12(2):125-137.
22. Scharpfenecker M, Fiedler U, Reiss Y, Augustin HG. The Tie-2 ligand angiopoietin-2 destabilizes quiescent endothelium through an internal autocrine loop mechanism. J Cell Sci. 2005; 118(pt 4):771-780.
23. Eikesdal HP, Knappskog S, Aas T, Lonning PE. TP53 status predicts long-term survival in locally advanced breast cancer after primary chemotherapy. Acta Oncol. 2014; 53(10):1347-1355.
24. Imanishi Y, et al. Angiopoietin-2 stimulates breast cancer metastasis through the α(5)β(1) integrin-mediated pathway. Cancer Res. 2007; 67(9):4254-4263.
25. Avraham HK, Jiang S, Fu Y, Nakshatri H, Ovadia H, Avraham S. Angiopoietin-2 mediates blood-brain barrier impairment and colonization of triple-negative breast cancer cells in brain. J Pathol. 2014; 232(3):369-381.
26. Rigamonti N, Kadioglu E, Keklikoglou I, Wyser Rmili C, Leow CC, De Palma M. Role of angiopoietin-2 in adaptive tumor resistance to VEGF signaling blockade. Cell Rep. 2014; 8(3):696-706.
27. Sfiligoi C, et al. Angiopoietin-2 expression in breast cancer correlates with lymph node invasion and short survival. Int J Cancer. 2003; 103(4):466-474.
28. Li P, He Q, Luo C, Qian L. Diagnostic and prognostic potential of serum angiopoietin-2 expression in human breast cancer. Int J Clin Exp Pathol. 2015; 8(1):660-664.
29. Holopainen T, et al. Effects of angiopoietin-2-blocking antibody on endothelial cell-cell junctions and lung metastasis. J Natl Cancer Inst. 2012; 104(6):461-475.
30. Imanishi Y, Hu B, Xiao G, Yao X, Cheng SY. Angiopoietin-2, an angiogenic regulator, promotes initial growth and survival of breast cancer metastases to the lung through the integrin-linked kinase (ILK)-AKT-B cell lymphoma 2 (Bcl-2) pathway. J Biol Chem. 2011; 286(33):29249-29260.
31. Srivastava K, et al. Postsurgical adjuvant tumor therapy by combining anti-angiopoietin-2 and metronomic chemotherapy limits metastatic growth. Cancer Cell. 2014; 26(6):880-895.
32. Tsutsui S, et al. Angiopoietin 2 expression in invasive ductal carcinoma of the breast: its relationship to the VEGF expression and microvessel density. Breast Cancer Res Treat. 2006; 98(3):261-266.
33. Gerald D, Chintharlapalli S, Augustin HG, Benjamin LE. Angiopoietin-2: an attractive target for improved antiangiogenic tumor therapy. Cancer Res. 2013; 73(6):1649-1657.
34. Mazzieri R, et al. Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell. 2011; 19(4):512-526.
35. Rigamonti N, De Palma M. A role for angiopoietin-2 in organ-specific metastasis. Cell Rep. 2013; 4(4):621-623.
36. Tolaney SM, et al. Role of vascular density and normalization in response to neoadjuvant bevacizumab and chemotherapy in breast cancer patients. Proc Natl Acad Sci U S A. 2015; 112(46):14325-14330.
37. Chrisanthar R, et al. CHEK2 mutations affecting kinase activity together with mutations in TP53 indicate a functional pathway associated with resistance to epirubicin in primary breast cancer. PLoS One. 2008; 3(8):e3062.
38. Chrisanthar R, et al. Predictive and prognostic impact of TP53 mutations and MDM2 promoter genotype in primary breast cancer patients treated with epirubicin or paclitaxel. PLoS One. 2011; 6(4):e19249.
39. Knappskog S, et al. Concomitant inactivation of the p53- and pRB- functional pathways predicts resistance to DNA damaging drugs in breast cancer in vivo. Mol Oncol. 2015; 9(8):1553-1564.
40. Thomas M, et al. A novel angiopoietin-2 selective fully human antibody with potent anti-tumoral and anti-angiogenic efficacy and superior side effect profile compared to Pan-Angiopoietin-1/-2 inhibitors. PLoS One. 2013; 8(2):e54923.
41. Gale NW, et al. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev Cell. 2002; 3(3):411-423.
42. Hansen TM, Singh H, Tahir TA, Brindle NP. Effects of angiopoietins-1 and -2 on the receptor tyrosine kinase Tie2 are differentially regulated at the endothelial cell surface. Cell Signal. 2010; 22(3):527-532.
43. Hegen A, Koidl S, Weindel K, Marme D, Augustin HG, Fiedler U. Expression of angiopoietin-2 in endothelial cells is controlled by positive and negative regulatory promoter elements. Arterioscler Thromb Vasc Biol. 2004; 24(10):1803-1809.
44. Fiedler U, et al. The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Paladebodies. Blood. 2004; 103(11):4150-4156.
45. Mackey JR, et al. Controlling angiogenesis in breast cancer: a systematic review of anti-angiogenic trials. Cancer Treat Rev. 2012; 38(6):673-688.
46. Sikov WM, et al. Impact of the addition of carboplatin and/or bevacizumab to neoadjuvant once-per-week paclitaxel followed by dose-dense doxorubicin and cyclophosphamide on pathologic complete response rates in stage II to III triple-negative breast cancer: CALGB 40603 (Alliance). J Clin Oncol. 2015; 33(1):13-21.
47. von Minckwitz G, et al. Neoadjuvant chemotherapy and bevacizumab for HER2-negative breast cancer. N Engl J Med. 2012; 366(4):299-309.
48. Bocci G, Di Paolo A, Danesi R. The pharmacological bases of the antiangiogenic activity of paclitaxel. Angiogenesis. 2013; 16(3):481-492.
49. Lee K, Qian DZ, Rey S, Wei H, Liu JO, Semenza GL. Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells. Proc Natl Acad Sci U S A. 2009; 106(7):2353-2358.
50. Tanaka T, Yamaguchi J, Shoji K, Nangaku M. Anthracycline inhibits recruitment of hypoxia-inducible transcription factors and suppresses tumor cell migration and cardiac angiogenic response in the host. J Biol Chem. 2012; 287(42):34866-34882.
51. Liu W, Shen SM, Zhao XY, Chen GQ. Targeted genes and interacting proteins of hypoxia inducible factor-1. Int J Biochem Mol Biol. 2012; 3(2):165-178.
52. Felcht M, et al. Angiopoietin-2 differentially regulates angiogenesis through TIE2 and integrin signaling. J Clin Invest. 2012; 122(6):1991-2005.
53. Hakanpaa L, et al. Endothelial destabilization by angiopoietin-2 via integrin β1 activation. Nat Commun. 2015; 6:5962.
54. Coffelt SB, et al. Angiopoietin 2 stimulates TIE2-expressing monocytes to suppress T cell activation and to promote regulatory T cell expansion. J Immunol. 2011; 186(7):4183-4190.
55. De Palma M, Naldini L. Angiopoietin-2 TIEs up macrophages in tumor angiogenesis. Clin Cancer Res. 2011; 17(16):5226-5232.
56. Coffelt SB, et al. Angiopoietin-2 regulates gene expression in TIE2-expressing monocytes and augments their inherent proangiogenic functions. Cancer Res. 2010; 70(13):5270-5280.
57. Wagenblast E, et al. A model of breast cancer heterogeneity reveals vascular mimicry as a driver of metastasis. Nature. 2015; 520(7547):358-362.
58. McAuliffe PF, et al. Ability to generate patient-derived breast cancer xenografts is enhanced in chemoresistant disease and predicts poor patient outcomes. PLoS One. 2015; 10(9):e0136851.