Heterogeneity of tumor endothelial cells and drug delivery

Advanced Drug Delivery Reviews

Volumn 99, Issue , 2016, Pages 140-147

  Hida, Kyoko ^a   Maishi, Nako ^a   Sakurai, Yu ^a   Hida, Yasuhiro ^b   Harashima, Hideyoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Angiogenesis; Anti angiogenic therapy; Drug delivery; Heterogeneity; MEND; Metastasis; Tumor; Tumor endothelial cell

Indexed keywords

BLOOD VESSELS; DRUG DELIVERY; DRUG THERAPY; TUMORS;

ANGIOGENESIS; ANTI-ANGIOGENIC THERAPY; HETEROGENEITY; MEND; METASTASIS;

ENDOTHELIAL CELLS;

VASCULOTROPIN; ANTINEOPLASTIC AGENT;

ANTIANGIOGENIC THERAPY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG PENETRATION; DRUG RESISTANCE; DRUG RETENTION; DRUG SAFETY; DRUG TARGETING; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; NEOVASCULARIZATION (PATHOLOGY); PERSONALIZED MEDICINE; PRIORITY JOURNAL; REVIEW; TUMOR CELL; TUMOR ENDOTHELIAL CELL; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ANIMAL; BLOOD VESSEL; DRUG EFFECTS; HUMAN; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PATHOLOGY; PROCEDURES;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOOD VESSELS; DRUG DELIVERY SYSTEMS; DRUG RESISTANCE, NEOPLASM; ENDOTHELIAL CELLS; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84953208688     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2015.11.008     Document Type: Review

References (78)

1. Folkman J. Angiogenesis: an organizing principle for drug discovery?. Nat. Rev. Drug Discov. 2007, 6:273-286.
2. Johnson D.H., Fehrenbacher L., Novotny W.F., Herbst R.S., Nemunaitis J.J., Jablons D.M., Langer C.J., DeVore R.F., Gaudreault J., Damico L.A., Holmgren E., Kabbinavar F. Randomized phase II trial comparing bevacizumab plus carboplatin and paclitaxel with carboplatin and paclitaxel alone in previously untreated locally advanced or metastatic non-small-cell lung cancer. J. Clin. Oncol. 2004, 22:2184-2191.
3. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 1971, 285:1182-1186.
4. Fidler I.J. Regulation of neoplastic angiogenesis. J. Natl. Cancer Inst. Monogr. 2001, 10-14.
5. McDonald D.M., Baluk P. Significance of blood vessel leakiness in cancer. Cancer Res. 2002, 62:5381-5385.
6. McDonald D.M., Choyke P.L. Imaging of angiogenesis: from microscope to clinic. Nat. Med. 2003, 9:713-725.
7. Akino T., Hida K., Hida Y., Tsuchiya K., Freedman D., Muraki C., Ohga N., Matsuda K., Akiyama K., Harabayashi T., Shinohara N., Nonomura K., Klagsbrun M., Shindoh M. Cytogenetic abnormalities of tumor-associated endothelial cells in human malignant tumors. Am. J. Pathol. 2009, 175:2657-2667.
8. Amin D.N., Hida K., Bielenberg D.R., Klagsbrun M. Tumor endothelial cells express epidermal growth factor receptor (EGFR) but not ErbB3 and are responsive to EGF and to EGFR kinase inhibitors. Cancer Res. 2006, 66:2173-2180.
9. Hida K., Hida Y., Amin D.N., Flint A.F., Panigrahy D., Morton C.C., Klagsbrun M. Tumor-associated endothelial cells with cytogenetic abnormalities. Cancer Res. 2004, 64:8249-8255.
10. Hida K., Hida Y., Shindoh M. Understanding tumor endothelial cell abnormalities to develop ideal anti-angiogenic therapies. Cancer Sci. 2008, 99:459-466.
11. Kurosu T., Ohga N., Hida Y., Maishi N., Akiyama K., Kakuguchi W., Kuroshima T., Kondo M., Akino T., Totsuka Y., Shindoh M., Higashino F., Hida K. HuR keeps an angiogenic switch on by stabilising mRNA of VEGF and COX-2 in tumour endothelium. Br. J. Cancer 2011, 104:819-829.
12. Matsuda K., Ohga N., Hida Y., Muraki C., Tsuchiya K., Kurosu T., Akino T., Shih S.C., Totsuka Y., Klagsbrun M., Shindoh M., Hida K. Isolated tumor endothelial cells maintain specific character during long-term culture. Biochem. Biophys. Res. Commun. 2010, 394:947-954.
13. Ohga N., Hida K., Hida Y., Muraki C., Tsuchiya K., Matsuda K., Ohiro Y., Totsuka Y., Shindoh M. Inhibitory effects of epigallocatechin-3 gallate, a polyphenol in green tea, on tumor-associated endothelial cells and endothelial progenitor cells. Cancer Sci. 2009, 100:1963-1970.
14. Tsuchiya K., Hida K., Hida Y., Muraki C., Ohga N., Akino T., Kondo T., Miseki T., Nakagawa K., Shindoh M., Harabayashi T., Shinohara N., Nonomura K., Kobayashi M. Adrenomedullin antagonist suppresses tumor formation in renal cell carcinoma through inhibitory effects on tumor endothelial cells and endothelial progenitor mobilization. Int. J. Oncol. 2010, 36:1379-1386.
15. Adya R., Tan B.K., Punn A., Chen J., Randeva H.S. Visfatin induces human endothelial VEGF and MMP-2/9 production via MAPK and PI3K/Akt signalling pathways: novel insights into visfatin-induced angiogenesis. Cardiovasc. Res. 2008, 78:356-365.
16. Ohga N., Ishikawa S., Maishi N., Akiyama K., Hida Y., Kawamoto T., Sadamoto Y., Osawa T., Yamamoto K., Kondoh M., Ohmura H., Shinohara N., Nonomura K., Shindoh M., Hida K. Heterogeneity of tumor endothelial cells: comparison between tumor endothelial cells isolated from high- and low-metastatic tumors. Am. J. Pathol. 2012, 180:1294-1307.
17. Kibria G., Hatakeyama H., Ohga N., Hida K., Harashima H. The effect of liposomal size on the targeted delivery of doxorubicin to integrin alphavbeta3-expressing tumor endothelial cells. Biomaterials 2013, 34:5617-5627.
18. Sakurai Y., Hatakeyama H., Sato Y., Hyodo M., Akita H., Ohga N., Hida K., Harashima H. RNAi-mediated gene knockdown and anti-angiogenic therapy of RCCs using a cyclic RGD-modified liposomal-siRNA system. J. Control. Release 2014, 173:110-118.
19. Folkman J., Kerbel R. Role of angiogenesis in tumor growth and metastasis clinical translation of angiogenesis inhibitors. Semin. Oncol. 2002, 29:15-18.
20. Casanovas O., Hicklin D.J., Bergers G., Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005, 8:299-309.
21. Keedy V.L., Sandler A.B. Inhibition of angiogenesis in the treatment of non-small cell lung cancer. Cancer Sci. 2007, 98:1825-1830.
22. Kindler H.L., Friberg G., Singh D.A., Locker G., Nattam S., Kozloff M., Taber D.A., Karrison T., Dachman A., Stadler W.M., Vokes E.E. Phase II trial of bevacizumab plus gemcitabine in patients with advanced pancreatic cancer. J. Clin. Oncol. 2005, 23:8033-8040.
23. Saif M.W., Elfiky A., Salem R.R. Gastrointestinal perforation due to bevacizumab in colorectal cancer. Ann. Surg. Oncol. 2007, 14:1860-1869.
24. Kane R.C., Farrell A.T., Saber H., Tang S., Williams G., Jee J.M., Liang C., Booth B., Chidambaram N., Morse D., Sridhara R., Garvey P., Justice R., Pazdur R. Sorafenib for the treatment of advanced renal cell carcinoma. Clin. Cancer Res. 2006, 12:7271-7278.
25. Escudier B., Eisen T., Stadler W.M., Szczylik C., Oudard S., Siebels M., Negrier S., Chevreau C., Solska E., Desai A.A., Rolland F., Demkow T., Hutson T.E., Gore M., Freeman S., Schwartz B., Shan M., Simantov R., Bukowski R.M., Group T.S. Sorafenib in advanced clear-cell renal-cell carcinoma. N. Engl. J. Med. 2007, 356:125-134.
26. Garcia A.A., Hirte H., Fleming G., Yang D., Tsao-Wei D.D., Roman L., Groshen S., Swenson S., Markland F., Gandara D., Scudder S., Morgan R., Chen H., Lenz H.J., Oza A.M. Phase II clinical trial of bevacizumab and low-dose metronomic oral cyclophosphamide in recurrent ovarian cancer: a trial of the California, Chicago, and Princess Margaret Hospital phase II consortia. J. Clin. Oncol. 2008, 26:76-82.
27. Hashizume H., Baluk P., Morikawa S., McLean J.W., Thurston G., Roberge S., Jain R.K., McDonald D.M. Openings between defective endothelial cells explain tumor vessel leakiness. Am. J. Pathol. 2000, 156:1363-1380.
28. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 2003, 3:422-433.
29. Baluk P., Hashizume H., McDonald D.M. Cellular abnormalities of blood vessels as targets in cancer. Curr. Opin. Genet. Dev. 2005, 15:102-111.
30. Jain R.K. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005, 307:58-62.
31. Chang Y.S., di Tomaso E., McDonald D.M., Jones R., Jain R.K., Munn L.L. Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:14608-14613.
32. Matsumura Y., Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 1986, 46:6387-6392.
33. Fang J., Nakamura H., Maeda H. The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev. 2011, 63:136-151.
34. Paez-Ribes M., Allen E., Hudock J., Takeda T., Okuyama H., Vinals F., Inoue M., Bergers G., Hanahan D., Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009, 15:220-231.
35. Croix B.St, Rago C., Velculescu V., Traverso G., Romans K.E., Montgomery E., Lal A., Riggins G.J., Lengauer C., Vogelstein B., Kinzler K.W. Genes expressed in human tumor endothelium. Science 2000, 289:1197-1202.
36. Arbiser J.L., Raab G., Rohan R.M., Paul S., Hirschi K., Flynn E., Price E.R., Fisher D.E., Cohen C., Klagsbrun M. Isolation of mouse stromal cells associated with a human tumor using differential diphtheria toxin sensitivity. Am. J. Pathol. 1999, 155:723-729.
37. Seaman S., Stevens J., Yang M.Y., Logsdon D., Graff-Cherry C., Croix B.St Genes that distinguish physiological and pathological angiogenesis. Cancer Cell 2007, 11:539-554.
38. Hida K., Klagsbrun M. A new perspective on tumor endothelial cells: unexpected chromosome and centrosome abnormalities. Cancer Res. 2005, 65:2507-2510.
39. Bussolati B., Deambrosis I., Russo S., Deregibus M.C., Camussi G. Altered angiogenesis and survival in human tumor-derived endothelial cells. Faseb J. 2003, 17:1159-1161.
40. Xiong Y.Q., Sun H.C., Zhang W., Zhu X.D., Zhuang P.Y., Zhang J.B., Wang L., Wu W.Z., Qin L.X., Tang Z.Y. Human hepatocellular carcinoma tumor-derived endothelial cells manifest increased angiogenesis capability and drug resistance compared with normal endothelial cells. Clin. Cancer Res. 2009, 15:4838-4846.
41. Akiyama K., Ohga N., Hida Y., Kawamoto T., Sadamoto Y., Ishikawa S., Maishi N., Akino T., Kondoh M., Matsuda A., Inoue N., Shindoh M., Hida K. Tumor endothelial cells acquire drug resistance by MDR1 up-regulation via VEGF signaling in tumor microenvironment. Am. J. Pathol. 2012, 180:1283-1293.
42. Dudley A.C., Khan Z.A., Shih S.C., Kang S.Y., Zwaans B.M., Bischoff J., Klagsbrun M. Calcification of multipotent prostate tumor endothelium. Cancer Cell 2008, 14:201-211.
43. Molema G. Heterogeneity in endothelial responsiveness to cytokines, molecular causes, and pharmacological consequences. Semin. Thromb. Hemost. 2010, 36:246-264.
44. Langenkamp E., Molema G. Microvascular endothelial cell heterogeneity: general concepts and pharmacological consequences for anti-angiogenic therapy of cancer. Cell Tissue Res. 2009, 335:205-222.
45. Nagy J.A., Dvorak H.F. Heterogeneity of the tumor vasculature: the need for new tumor blood vessel type-specific targets. Clin. Exp. Metastasis 2012, 29:657-662.
46. Bussolati B., Assenzio B., Deregibus M.C., Camussi G. The proangiogenic phenotype of human tumor-derived endothelial cells depends on thrombospondin-1 downregulation via phosphatidylinositol 3-kinase/Akt pathway. J. Mol. Med. (Berl) 2006, 84:852-863.
47. Duensing S., Munger K. Human papillomaviruses and centrosome duplication errors: modeling the origins of genomic instability. Oncogene 2002, 21:6241-6248.
48. de Groot J.F., Fuller G., Kumar A.J., Piao Y., Eterovic K., Ji Y., Conrad C.A. Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro-Oncology 2010, 12:233-242.
49. Sato Y. Persistent vascular normalization as an alternative goal of anti-angiogenic cancer therapy. Cancer Sci. 2011, 102:1253-1256.
50. Helfrich I., Scheffrahn I., Bartling S., Weis J., von Felbert V., Middleton M., Kato M., Ergun S., Schadendorf D. Resistance to antiangiogenic therapy is directed by vascular phenotype, vessel stabilization, and maturation in malignant melanoma. J. Exp. Med. 2010, 207:491-503.
51. Taylor S.M., Nevis K.R., Park H.L., Rogers G.C., Rogers S.L., Cook J.G., Bautch V.L. Angiogenic factor signaling regulates centrosome duplication in endothelial cells of developing blood vessels. Blood 2010, 116:3108-3117.
52. Gao D., Nolan D., McDonnell K., Vahdat L., Benezra R., Altorki N., Mittal V. Bone marrow-derived endothelial progenitor cells contribute to the angiogenic switch in tumor growth and metastatic progression. Biochim. Biophys. Acta 2009, 1796:33-40.
53. Ricci-Vitiani L., Pallini R., Biffoni M., Todaro M., Invernici G., Cenci T., Maira G., Parati E.A., Stassi G., Larocca L.M., De Maria R. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010, 468:824-828.
54. Wang R., Chadalavada K., Wilshire J., Kowalik U., Hovinga K.E., Geber A., Fligelman B., Leversha M., Brennan C., Tabar V. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 2010, 468:829-833.
55. Cheng L., Huang Z., Zhou W., Wu Q., Donnola S., Liu J.K., Fang X., Sloan A.E., Mao Y., Lathia J.D., Min W., McLendon R.E., Rich J.N., Bao S. Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 2013, 153:139-152.
56. Streubel B., Chott A., Huber D., Exner M., Jager U., Wagner O., Schwarzinger I. Lymphoma-specific genetic aberrations in microvascular endothelial cells in B-cell lymphomas. N. Engl. J. Med. 2004, 351:250-259.
57. van Beijnum J.R., Dings R.P., van der Linden E., Zwaans B.M., Ramaekers F.C., Mayo K.H., Griffioen A.W. Gene expression of tumor angiogenesis dissected: specific targeting of colon cancer angiogenic vasculature. Blood 2006, 108:2339-2348.
58. Fonsato V., Buttiglieri S., Deregibus M.C., Puntorieri V., Bussolati B., Camussi G. Expression of Pax2 in human renal tumor-derived endothelial cells sustains apoptosis resistance and angiogenesis. Am. J. Pathol. 2006, 168:706-713.
59. Lu C., Bonome T., Li Y., Kamat A.A., Han L.Y., Schmandt R., Coleman R.L., Gershenson D.M., Jaffe R.B., Birrer M.J., Sood A.K. Gene alterations identified by expression profiling in tumor-associated endothelial cells from invasive ovarian carcinoma. Cancer Res. 2007, 67:1757-1768.
60. Buckanovich R.J., Sasaroli D., O'Brien-Jenkins A., Botbyl J., Hammond R., Katsaros D., Sandaltzopoulos R., Liotta L.A., Gimotty P.A., Coukos G. Tumor vascular proteins as biomarkers in ovarian cancer. J. Clin. Oncol. 2007, 25:852-861.
61. Muraki C., Ohga N., Hida Y., Nishihara H., Kato Y., Tsuchiya K., Matsuda K., Totsuka Y., Shindoh M., Hida K. Cyclooxygenase-2 inhibition causes antiangiogenic effects on tumor endothelial and vascular progenitor cells. Int. J. Cancer 2012, 130:59-70.
62. Yamamoto K., Ohga N., Hida Y., Maishi N., Kawamoto T., Kitayama K., Akiyama K., Osawa T., Kondoh M., Matsuda K., Onodera Y., Fujie M., Kaga K., Hirano S., Shinohara N., Shindoh M., Hida K. Biglycan is a specific marker and an autocrine angiogenic factor of tumour endothelial cells. Br. J. Cancer 2012, 106:1214-1223.
63. Maishi N., Ohga N., Hida Y., Akiyama K., Kitayama K., Osawa T., Onodera Y., Shinohara N., Nonomura K., Shindoh M., Hida K. CXCR7: a novel tumor endothelial marker in renal cell carcinoma. Pathol. Int. 2012, 62:309-317.
64. Osawa T., Ohga N., Akiyama K., Hida Y., Kitayama K., Kawamoto T., Yamamoto K., Maishi N., Kondoh M., Onodera Y., Fujie M., Shinohara N., Nonomura K., Shindoh M., Hida K. Lysyl oxidase secreted by tumour endothelial cells promotes angiogenesis and metastasis. Br. J. Cancer 2013, 109:2237-2247.
65. Osawa T., Ohga N., Hida Y., Kitayama K., Akiyama K., Onodera Y., Fujie M., Shinohara N., Shindoh M., Nonomura K., Hida K. Prostacyclin receptor in tumor endothelial cells promotes angiogenesis in an autocrine manner. Cancer Sci. 2012, 103:1038-1044.
66. Alam M.T., Nagao-Kitamoto H., Ohga N., Akiyama K., Maishi N., Kawamoto T., Shinohara N., Taketomi A., Shindoh M., Hida Y., Hida K. Suprabasin as a novel tumor endothelial cell marker. Cancer Sci. 2014, 105:1533-1540.
67. Otsubo T., Hida Y., Ohga N., Sato H., Kai T., Matsuki Y., Takasu H., Akiyama K., Maishi N., Kawamoto T., Shinohara N., Nonomura K., Hida K. Identification of novel targets for antiangiogenic therapy by comparing the gene expressions of tumor and normal endothelial cells. Cancer Sci. 2014, 105:560-567.
68. Zhuang X., Herbert J.M., Lodhia P., Bradford J., Turner A.M., Newby P.M., Thickett D., Naidu U., Blakey D., Barry S., Cross D.A., Bicknell R. Identification of novel vascular targets in lung cancer. Br. J. Cancer 2015, 112:485-494.
69. Pasqualini R., Koivunen E., Kain R., Lahdenranta J., Sakamoto M., Stryhn A., Ashmun R.A., Shapiro L.H., Arap W., Ruoslahti E. Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res. 2000, 60:722-727.
70. Pastorino F., Brignole C., Marimpietri D., Cilli M., Gambini C., Ribatti D., Longhi R., Allen T.M., Corti A., Ponzoni M. Vascular damage and anti-angiogenic effects of tumor vessel-targeted liposomal chemotherapy. Cancer Res. 2003, 63:7400-7409.
71. Arap W., Pasqualini R., Ruoslahti E. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 1998, 279:377-380.
72. Kogure K., Akita H., Yamada Y., Harashima H. Multifunctional envelope-type nano device (MEND) as a non-viral gene delivery system. Adv. Drug Deliv. Rev. 2008, 60:559-571.
73. Hatakeyama H., Akita H., Harashima H. A multifunctional envelope type nano device (MEND) for gene delivery to tumours based on the EPR effect: a strategy for overcoming the PEG dilemma. Adv. Drug Deliv. Rev. 2011, 63:152-160.
74. Sato Y., Hatakeyama H., Sakurai Y., Hyodo M., Akita H., Harashima H. A pH-sensitive cationic lipid facilitates the delivery of liposomal siRNA and gene silencing activity in vitro and in vivo. J. Control. Release 2012, 163:267-276.
75. Whitehead K.A., Langer R., Anderson D.G. Knocking down barriers: advances in siRNA delivery. Nat. Rev. Drug Discov. 2009, 8:129-138.
76. Allport J.R., Shinde Patil V.R., Weissleder R. Murine neuronal progenitor cells are preferentially recruited to tumor vasculature via alpha4-integrin and SDF-1alpha-dependent mechanisms. Cancer Biol. Ther. 2004, 3(9):838-844. PMID: 15254391.
77. Akiyama K., Ohga N., Maishi N., Hida Y., Kitayama K., Kawamoto T., Osawa T., Suzuki Y., Shinohara N., Nonomura K., Shindoh M., Hida K. The F-prostaglandin receptor is a novel marker for tumor endothelial cells in renal cell carcinoma. Pathol. Int. 2013, 63(1):37-44.
78. Akiyama K., Maishi N., Ohga N., Hida Y., Ohba Y., Alam M.T., Kawamoto T., Ohmura H., Yamada K., Torii C., Shindoh M., Hida K. Inhibition of multidrug transporter in tumor endothelial cells enhances antiangiogenic effects of low-dose metronomic paclitaxel. Am. J. Pathol. 2015, 185(2):572-580.