A novel population of local pericyte precursor cells in tumor stroma that require Notch signaling for differentiation

Microvascular Research

Volumn 101, Issue , 2015, Pages 38-47

  Patenaude, Alexandre ^a   Woerher, Stefan ^a   Umlandt, Patricia ^a   Wong, Fred ^a   Ibrahim, Rawa ^a   Kyle, Alastair ^a   Unger, Sandy ^a   Fuller, Megan ^a   Parker, Jeremy ^a   Minchinton, Andrew ^a   Eaves, Connie J ^a,b   Karsan, Aly ^a,b  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ATAXIN 1; CD146 ANTIGEN; CD31 ANTIGEN; CD45 ANTIGEN; GAMMA SECRETASE; HERMES ANTIGEN; JAGGED1; MICROSOMAL AMINOPEPTIDASE; NOTCH RECEPTOR; THY 1 ANTIGEN; TIE 1 RECEPTOR; ATXN1 PROTEIN, HUMAN; ATXN1 PROTEIN, MOUSE; MCAM PROTEIN, HUMAN; MCAM PROTEIN, MOUSE; PTPRC PROTEIN, HUMAN; PTPRC PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CANCER STEM CELL; CELL DIFFERENTIATION; CELL MATURATION; COCULTURE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOTHELIUM CELL; EX VIVO STUDY; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STROMA CELL; TUMOR CELL; TUMOR MICROENVIRONMENT; TUMOR STROMA; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CANCER TRANSPLANTATION; CYTOLOGY; EXPERIMENTAL MELANOMA; FLOW CYTOMETRY; LEWIS CARCINOMA; MESENCHYMAL STROMA CELL; METABOLISM; NEOPLASM; STEM CELL; TRANSGENIC MOUSE; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; ANTIGENS, CD146; ANTIGENS, CD31; ANTIGENS, CD45; ATAXIN-1; BONE MARROW TRANSPLANTATION; CARCINOMA, LEWIS LUNG; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; FLOW CYTOMETRY; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MELANOMA, EXPERIMENTAL; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; NEOPLASMS; PERICYTES; RECEPTOR, TIE-1; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84938903705     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2015.05.004     Document Type: Article

References (38)

1. Abramsson A., Berlin O., Papayan H., Paulin D., Shani M., Betsholtz C. Analysis of mural cell recruitment to tumor vessels. Circulation 2002, 105:112-117.
2. Armulik A., Genove G., Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises, Dev. Cell 2011, 21:193-215.
3. Baker J.H., Lam J., Kyle A.H., Sy J., Oliver T., Co S.J., Dragowska W.H., Ramsay E., Anantha M., Ruth T.J., Adam M.J., Yung A., Kozlowski P., Minchinton A.I., Ng S.S., Bally M.B., Yapp D.T. Irinophore C, a novel nanoformulation of irinotecan, alters tumor vascular function and enhances the distribution of 5-fluorouracil and doxorubicin. Clin. Cancer Res. 2008, 14:7260-7271.
4. Benedito R., Roca C., Sorensen I., Adams S., Gossler A., Fruttiger M., Adams R.H. The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 2009, 137:1124-1135.
5. Benz C., Copley M.R., Kent D.G., Wohrer S., Cortes A., Aghaeepour N., Ma E., Mader H., Rowe K., Day C., Treloar D., Brinkman R.R., Eaves C.J. Hematopoietic stem cell subtypes expand differentially during development and display distinct lymphopoietic programs. Cell Stem Cell 2012, 10:273-283.
6. Cappellari O., Benedetti S., Innocenzi A., Tedesco F.S., Moreno-Fortuny A., Ugarte G., Lampugnani M.G., Messina G., Cossu G. Dll4 and PDGF-BB Convert Committed Skeletal Myoblasts to Pericytes without Erasing Their Myogenic Memory, Dev. Cell 2013, 24:586-599.
7. Chang L., Noseda M., Higginson M., Ly M., Patenaude A., Fuller M., Kyle A.H., Minchinton A.I., Puri M.C., Dumont D.J., Karsan A. Differentiation of vascular smooth muscle cells from local precursors during embryonic and adult arteriogenesis requires Notch signaling. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6993-6998.
8. Chang A.C., Fu Y., Garside V.C., Niessen K., Chang L., Fuller M., Setiadi A., Smrz J., Kyle A., Minchinton A., Marra M., Hoodless P.A., Karsan A. Notch Initiates the Endothelial-to-Mesenchymal Transition in the Atrioventricular Canal through Autocrine Activation of Soluble Guanylyl Cyclase, Dev. Cell 2012, 21:288-300.
9. Crisan M., Yap S., Casteilla L., Chen C.W., Corselli M., Park T.S., Andriolo G., Sun B., Zheng B., Zhang L., Norotte C., Teng P.N., Traas J., Schugar R., Deasy B.M., Badylak S., Buhring H.J., Giacobino J.P., Lazzari L., Huard J., Peault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3:301-313.
10. De Bock K., Cauwenberghs S., Carmeliet P. Vessel abnormalization: another hallmark of cancer? Molecular mechanisms and therapeutic implications. Curr. Opin. Genes Dev. 2011, 21:73-79.
11. De Palma M., Venneri M.A., Galli R., Sergi Sergi L., Politi L.S., Sampaolesi M., Naldini L. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005, 8:211-226.
12. Dhar K., Dhar G., Majumder M., Haque I., Mehta S., Van Veldhuizen P.J., Banerjee S.K., Banerjee S. Tumor cell-derived PDGF-B potentiates mouse mesenchymal stem cells-pericytes transition and recruitment through an interaction with NRP-1, Mol. Cancer 2010, 9:209.
13. Domenga V., Fardoux P., Lacombe P., Monet M., Maciazek J., Krebs L.T., Klonjkowski B., Berrou E., Mericskay M., Li Z., Tournier-Lasserve E., Gridley T., Joutel A. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 2004, 18:2730-2735.
14. Du R., Lu K.V., Petritsch C., Liu P., Ganss R., Passegue E., Song H., Vandenberg S., Johnson R.S., Werb Z., Bergers G. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008, 13:206-220.
15. Dufraine J., Funahashi Y., Kitajewski J. Notch signaling regulates tumor angiogenesis by diverse mechanisms. Oncogene 2008, 27:5132-5137.
16. Eilken H.M., Adams R.H. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 2010, 22:617-625.
17. Gridley T. Notch signaling in the vasculature. Curr. Top. Dev. Biol. 2010, 92:277-309.
18. High F.A., Lu M.M., Pear W.S., Loomes K.M., Kaestner K.H., Epstein J.A. Endothelial expression of the Notch ligand Jagged1 is required for vascular smooth muscle development. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1955-1959.
19. Kalluri R., Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer 2006, 6:392-401.
20. Kopan R., Ilagan M.X. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009, 137:216-233.
21. Larrivee B., Niessen K., Pollet I., Corbel S.Y., Long M., Rossi F.M., Olive P.L., Karsan A. Minimal contribution of marrow-derived endothelial precursors to tumor vasculature. J. Immunol. 2005, 175:2890-2899.
22. Liu H., Kennard S., Lilly B. NOTCH3 expression is induced in mural cells through an autoregulatory loop that requires endothelial-expressed JAGGED1. Circ. Res. 2009, 104:466-475.
23. Liu H., Zhang W., Kennard S., Caldwell R.B., Lilly B. Notch3 is critical for proper angiogenesis and mural cell investment. Circ. Res. 2010, 107:860-870.
24. Liu J., Sato C., Cerletti M., Wagers A. Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr. Top. Dev. Biol. 2010, 92:367-409.
25. Morikawa S., Baluk P., Kaidoh T., Haskell A., Jain R.K., McDonald D.M. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 2002, 160:985-1000.
26. Noseda M., McLean G., Niessen K., Chang L., Pollet I., Montpetit R., Shahidi R., Dorovini-Zis K., Li L., Beckstead B., Durand R.E., Hoodless P.A., Karsan A. Notch activation results in phenotypic and functional changes consistent with endothelial-to-mesenchymal transformation. Circ. Res. 2004, 94:910-917.
27. O'Keeffe M.B., Devlin A.H., Burns A.J., Gardiner T.A., Logan I.D., Hirst D.G., McKeown S.R. Investigation of pericytes, hypoxia, and vascularity in bladder tumors: association with clinical outcomes. Oncol. Res. 2008, 17:93-101.
28. Patel N.S., Dobbie M.S., Rochester M., Steers G., Poulsom R., Le Monnier K., Cranston D.W., Li J.L., Harris A.L. Up-regulation of endothelial delta-like 4 expression correlates with vessel maturation in bladder cancer. Clin. Cancer Res. 2006, 12:4836-4844.
29. Rajantie I., Ilmonen M., Alminaite A., Ozerdem U., Alitalo K., Salven P. Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood 2004, 104:2084-2086.
30. Roca C., Adams R.H. Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 2007, 21:2511-2524.
31. Sainson R.C., Harris A.L. Regulation of angiogenesis by homotypic and heterotypic notch signalling in endothelial cells and pericytes: from basic research to potential therapies. Angiogenesis 2008, 11:41-51.
32. Schadler K.L., Zweidler-McKay P.A., Guan H., Kleinerman E.S. Delta-like ligand 4 plays a critical role in pericyte/vascular smooth muscle cell formation during vasculogenesis and tumor vessel expansion in Ewing's sarcoma. Clin. Cancer Res. 2010, 16:848-856.
33. Song S., Ewald A.J., Stallcup W., Werb Z., Bergers G. PDGFRbeta+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat. Cell Biol. 2005, 7:870-879.
34. Stefansson I.M., Salvesen H.B., Akslen L.A. Vascular proliferation is important for clinical progress of endometrial cancer. Cancer Res. 2006, 66:3303-3309.
35. Stewart K.S., Zhou Z., Zweidler-McKay P., Kleinerman E.S. Delta-like ligand 4-Notch signaling regulates bone marrow-derived pericyte/vascular smooth muscle cell formation. Blood 2011, 117:719-726.
36. Weis S.M., Cheresh D.A. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat. Med. 2011, 17:1359-1370.
37. Wu X., Zou Y., Zhou Q., Huang L., Gong H., Sun A., Tateno K., Katsube K., Radtke F., Ge J., Minamino T., Komuro I. Role of Jagged1 in arterial lesions after vascular injury. Arterioscler. Thromb. Vasc. Biol. 2011, 31:2000-2006.
38. Yonenaga Y., Mori A., Onodera H., Yasuda S., Oe H., Fujimoto A., Tachibana T., Imamura M. Absence of smooth muscle actin-positive pericyte coverage of tumor vessels correlates with hematogenous metastasis and prognosis of colorectal cancer patients. Oncology 2005, 69:159-166.