NG2 proteoglycan-dependent recruitment of tumor macrophages promotes pericyteendothelial cell interactions required for brain tumor vascularization

OncoImmunology

Volumn 4, Issue 4, 2015, Pages

  Yotsumoto, Fusanori ^a,b   You, Weon Kyoo ^a,c   Cejudo Martin, Pilar ^a   Kucharova, Karolina ^a   Sakimura, Kenji ^d   Stallcup, William B ^a  

^a BURNHAM INSTITUTE   (United States)

^b FUKUOKA UNIVERSITY   (Japan)

^c Hanwha Corporation   (South Korea)

^d NIIGATA UNIVERSITY   (Japan)

Author keywords

Macrophage recruitment; NG2 proteoglycan; Pericyte endothelial cell interaction; Tumor microenvironment; Tumor vascularization

Indexed keywords

NERVE CELL ADHESION MOLECULE; NG2 PROTEOGLYCAN; PROTEOGLYCAN; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; BRAIN HYPOXIA; BRAIN PERICYTE; CELL ACTIVATION; CELL INTERACTION; CELL MOTILITY; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM CELL; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; TUMOR ASSOCIATED LEUKOCYTE; TUMOR BLOOD FLOW; TUMOR GROWTH; TUMOR VASCULARIZATION; TUMOR VOLUME;

EID: 84940768476     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2014.1001204     Document Type: Article

References (53)

1. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010; 141:39-51; PMID:20371344; http://dx. doi. org/10. 1016/j. cell. 2010. 03. 014
2. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014; 41:49-61; PMID:25035953; http://dx. doi. org/10. 1016/j. immuni. 2014. 06. 010
3. Coffelt SB, Hughes R, Lewis CE. Tumor-associated macrophages: effectors of angiogenesis and tumor progression. Biochim Biophys Acta 2009; 1796:11-8; PMID:19269310; http://dx. doi. org/10. 1016/j. bbcan. 2009. 02. 004
4. De Palma M, Naldini L. Tie2-expressing monocytes (TEMs): novel targets and vehicles of anticancer therapy? Biochim Biophys Acta 2009; 1796:5-10; PMID:19362584; http://dx. doi. org/10. 1016. /j. bbcan. 2009. 04. 001
5. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, Pollard JW. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol 2003; 163:2113-26; PMID:14578209; http:// dx. doi. org/10. 1016/S0002-9440(10)63568-7
6. Gibby K, You WK, Kadoya K, Helgadottir H, Young LJ, Ellies LG, Chang Y, Cardiff RD, Stallcup WB. Early vascular deficits are correlated with delayed mammary tumorigenesis in the MMTV-PyMT transgenic mouse following genetic ablation of the NG2 proteoglycan. Breast Cancer Res 2012; 14:R67; PMID:22531600; http://dx. doi. org/10. 1186/bcr3174
7. Coffelt SB, Lewis CE, Naldini L, Brown JM, Ferrara N, De Palma M. Elusive identities and overlapping phenotypes of proangiogenic myeloid cells in tumors. Am J Pathol 2010; 176:1564-76; PMID:20167863; http://dx. doi. org/10. 2353/ajpath. 2010. 090786
8. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, 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; 8:211-26; PMID:16169466; http://dx. doi. org/10. 1016/ j. ccr. 2005. 08. 002
9. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA, QianH, Xue XN, Pollard JW. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 2006; 66:11238-46; PMID:17114237; http://dx. doi. org/10. 1158/0008-5472. CAN-06-1278
10. Huang FJ, You WK, Bonaldo P, Seyfried TN, Pasquale EB, Stallcup WB. Pericyte deficiencies lead to aberrant tumor vascularizaton in the brain of the NG2 null mouse. Dev Biol 2010; 344:1035-46; PMID:20599895; http:// dx. doi. org/10. 1016/j. ydbio. 2010. 06. 023
11. You WK, Bonaldo P, Stallcup WB. Collagen VI ablation retards brain tumor progression due to deficits in assembly of the vascular basal lamina. Am J Pathol 2012; 180:1145-58; PMID:22200614; http://dx. doi. org/10. 1016/j. ajpath. 2011. 11. 006
12. You WK, Yotsumoto F, Sakimura K, Adams RH, StallcupWB. NG2 proteoglycan promotes tumor vascularization via integrin-dependent effects on pericyte function. Angiogenesis 2014; 17:61-76; PMID:23925489; http:// dx. doi. org/10. 1007/s10456-013-9378-1
13. Chang Y, She ZG, Sakimura K, Roberts A, Kucharova K, Rowitch DH, Stallcup WB. Ablation of NG2 proteoglycan leads to deficits in brown fat function and to adult onset obesity. PLoS One 2012; 7:e30637; PMID:22295099; http://dx. doi. org/10. 1371/journal. pone. 0030637
14. Luo Y, Radice GL. N-cadherin acts upstream of VEcadherin in controlling vascular morphogenesis. J Cell Biol 2005; 169:29-34; PMID:15809310; http://dx. doi. org/10. 1083/jcb. 200411127
15. Gerhardt H, Wolburg H, Redies C. N-cadherin mediates pericytic-endothelial interaction during brain angiogenesis in the chicken. Dev Dyn 2000; 218:472-9; PMID:10878612; http://dx. doi. org/10. 1002/1097-0177 (200007)218:3<472::AB-DVDY1008. 3. 0CO;2#
16. Armulik A, Abramsson A, Betsholtz C. Endothelial/ pericyte interactions. Circ Res 2005; 97:512-23; PMID:16166562; http://dx. doi. org/10. 1161/01. RES. 0000182903. 16652. d7
17. Plate KH, Risau W. Angiogenesis in malignant gliomas. Glia 1995; 15:339-47; PMID:8586468; http:// dx. doi. org/10. 1002/glia. 440150313
18. Roskelley CD, Bissell MJ. The dominance of the microenvironment in breast and ovarian cancer. Semin Cancer Biol 2002; 12:97-104; PMID:12027581; http://dx. doi. org/10. 1006/scbi. 2001. 0417
19. Rubin JB. Only in congenial soil: the microenvironment in brain tumorigenesis. Brain Pathol 2009; 19:144-9; PMID:19076779; http://dx. doi. org/ 10. 1111/j. 1750-3639. 2008. 00235. x
20. Wiseman BS, Werb Z. Stromal effects on mammary gland development and breast cancer. Science 2002; 296:1046-9; PMID:12004111; http://dx. doi. org/ 10. 1126/science. 1067431
21. Yuan L, Siegel M, Choi K, Khosla C, Miller CR, Jackson EN, Piwnica-Worms D, Rich KM. Transglutaminase 2 inhibitor, KCC009, disrupts fibronectin assembly in the extracellular matrix and sensitizes orthotopic glioblastomas to chemotherapy. Oncogene 2007; 26:2563-73; PMID:17099729; http://dx. doi. org/10. 1038/sj. onc. 1210048
22. Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012; 21:309-22; PMID:22439926; http://dx. doi. org/10. 1016/j. ccr. 2012. 02. 022
23. Ribatti D, Crivellato E. Immune cells and angiogenesis. J Cell Mol Med 2009; 13:2822-33; PMID:19538473; http://dx. doi. org/10. 1111/j. 1582-4934. 2009. 00810. x
24. Tigges U, Hyer EG, Scharf J, Stallcup WB. FGF2-dependent neovascularization of subcutaneous Matrigel plugs is initiated by bone marrow-derived pericytes and macrophages. Development 2008; 135:523-32; PMID:18171688; http://dx. doi. org/10. 1242/ dev. 002071
25. Stark K, Eckart A, Haidari S, Tirniceriu A, Lorenz M, von Bruhl ML, Gärtner F, Khandoga AG, Legate KR, Pless R et al. Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct' them with pattern-recognition and motility programs. Nat Immunol 2013; 14:41-51; PMID:23179077; http://dx. doi. org/10. 1038/ni. 2477
26. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003; 3:401-10; PMID:12778130; http://dx. doi. org/10. 1038/nrc1093
27. Monier-Gavelle F, Duband JL. Cross talk between adhesion molecules: control of N-cadherin activity by intracellular signals elicited by beta1 and beta3 integrins in migrating neural crest cells. J Cell Biol 1997; 137:1663-81; PMID:9199179; http://dx. doi. org/ 10. 1083/jcb. 137. 7. 1663
28. Arregui C, Pathre P, Lilien J, Balsamo J. The nonreceptor tyrosine kinase fer mediates cross-talk between Ncadherin and beta1-integrins. J Cell Biol 2000; 149:1263-74; PMID:10851023; http://dx. doi. org/ 10. 1083/jcb. 149. 6. 1263
29. Rymo SF, Gerhardt H, Wolfhagen Sand F, Lang R, Uv A, Betsholtz C. A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures. PLoS One 2011; 6: e15846; PMID:21264342; http://dx. doi. org/10. 1371/ journal. pone. 0015846
30. Bonde AK, Tischler V, Kumar S, Soltermann A, Schwendener RA. Intratumoral macrophages contribute to epithelial-mesenchymal transition in solid tumors. BMC cancer 2012; 12:35; PMID:22273460; http://dx. doi. org/10. 1186/1471-2407-12-35
31. Fan QM, Jing YY, Yu GF, Kou XR, Ye F, Gao L, Li R, Zhao QD, Yang Y, Lu ZH et al. Tumor-associated macrophages promote cancer stem cell-like properties via transforming growth factor-beta1-induced epithelial-mesenchymal transition in hepatocellular carcinoma. Cancer letters 2014; 352:160-8; PMID:24892648; http://dx. doi. org/10. 1016/j. canlet. 2014. 05. 008
32. Li F, Lan Y, Wang Y, Wang J, Yang G, Meng F, Han H, Meng A, Wang Y, Yang X. Endothelial Smad4 maintains cerebrovascular integrity by activating Ncadherin through cooperation with Notch. Developmental cell 2011; 20:291-302; PMID:21397841; http://dx. doi. org/10. 1016/j. devcel. 2011. 01. 011
33. Hutchings H, Ortega N, Plouet J. Extracellular matrixbound vascular endothelial growth factor promotes endothelial cell adhesion, migration, and survival through integrin ligation. FASEB J 2003; 17:1520-2; PMID:12709411; http://dx. doi. org/10. 1096/fj. 02-0691
34. Kucharova K, Chang Y, Boor A, Yong VW, Stallcup WB. Reduced inflammation accompanies diminished myelin damage and repair in the NG2 null mouse spinal cord. J Neuroinflammation 2011; 8:158; PMID:22078261; http://dx. doi. org/10. 1186/1742-2094-8-158
35. Jin H, Su J, Garmy-Susini B, Kleeman J, Varner J. Integrin alpha4beta1 promotes monocyte trafficking and angiogenesis in tumors. Cancer Res 2006; 66:2146-52; PMID:16489015; http://dx. doi. org/ 10. 1158/0008-5472. CAN-05-2704
36. Ulyanova T, Priestley GV, Banerjee ER, Papayannopoulou T. Unique and redundant roles of alpha4 and beta2 integrins in kinetics of recruitment of lymphoid vs myeloid cell subsets to the inflamed peritoneum revealed by studies of genetically deficient mice. Exp Hematol 2007; 35:1256-65; PMID:17553614; http:// dx. doi. org/10. 1016/j. exphem. 2007. 04. 015
37. Fukushi J, Makagiansar IT, Stallcup WB. NG2 proteoglycan promotes endothelial cell motility and angiogenesis via engagement of galectin-3 and alpha3beta1 integrin. Mol Biol Cell 2004; 15:3580-90; PMID:15181153; http://dx. doi. org/10. 1091/mbc. E04-03-0236
38. Chekenya M, Krakstad C, Svendsen A, Netland IA, Staalesen V, Tysnes BB, Selheim F, Wang J, Sakariassen PØ, Sandal T et al. The progenitor cell marker NG2/MPG promotes chemoresistance by activation of integrin-dependent PI3K/Akt signaling. Oncogene 2008; 27:5182-94; PMID:18469852; http://dx. doi. org/10. 1038/onc. 2008. 157
39. Makagiansar IT, Williams S, Mustelin T, Stallcup WB. Differential phosphorylation of NG2 proteoglycan by ERK and PKCalpha helps balance cell proliferation and migration. J Cell Biol 2007; 178:155-65; PMID:17591920; http://dx. doi. org/10. 1083/ jcb. 200612084
40. Forlow SB, White EJ, Barlow SC, Feldman SH, Lu H, Bagby GJ, Beaudet AL, Bullard DC, Ley K. Severe inflammatory defect and reduced viability in CD18 and E-selectin double-mutant mice. J Clin Invest 2000; 106:1457-66; PMID:11120753; http://dx. doi. org/ 10. 1172/JCI10555
41. Burg MA, Grako KA, Stallcup WB. Expression of the NG2 proteoglycan enhances the growth and metastatic properties of melanoma cells. J Cell Physiol 1998; 177:299-312; PMID:9766527; http://dx. doi. org/ 10. 1002/(SICI)1097-4652(199811)177:2<299::AIDJCP12> 3. 0. CO;2-5
42. Price MA, Colvin Wanshura LE, Yang J, Carlson J, Xiang B, Li G, Ferrone S, Dudek AZ, Turley EA, McCarthy JB. CSPG4, a potential therapeutic target, facilitates malignant progression of melanoma. Pigment Cell Melanoma Res 2011; 24:1148-57; PMID:22004131; http://dx. doi. org/10. 1111/j. 1755-148X. 2011. 00929. x
43. Wang J, Svendsen A, Kmiecik J, Immervoll H, Skaftnesmo KO, Planaguma J, Reed RK, Bjerkvig R, Miletic H, Enger PØ et al. Targeting the NG2/CSPG4 proteoglycan retards tumour growth and angiogenesis in preclinical models of GBM and melanoma. PLoS One 2011; 6:e23062; PMID:21829586; http://dx. doi. org/ 10. 1371/journal. pone. 0023062
44. Maciag PC, Seavey MM, Pan ZK, Ferrone S, Paterson Y. Cancer immunotherapy targeting the high molecular weight melanoma-associated antigen protein results in a broad antitumor response and reduction of pericytes in the tumor vasculature. Cancer Res 2008; 68:8066-75; PMID:18829565; http://dx. doi. org/10. 1158/0008-5472. CAN-08-0287
45. Al-Mayhani MT, Grenfell R, Narita M, Piccirillo S, Kenney-Herbert E, Fawcett JW, Collins VP, Ichimura K, Watts C. NG2 expression in glioblastoma identifies an actively proliferating population with an aggressive molecular signature. Neuro Oncol 2011; 13:830-45; PMID:21798846; http://dx. doi. org/10. 1093/neuonc/ nor088
46. Persson A, Englund E. Phagocytic properties in tumor astrocytes. Neuropathology 2012; 32:252-60; PMID:22098621; http://dx. doi. org/10. 1111/j. 1440-1789. 2011. 01266. x
47. Cattaruzza S, Nicolosi PA, Braghetta P, Pazzaglia L, Benassi MS, Picci P, Lacrima K, Zanocco D, Rizzo E, Stallcup WB et al. NG2/CSPG4-collagen type VI interplays putatively involved in the microenvironmental control of tumour engraftment and local expansion. J Mol Cell Biol 2013; 5:176-93; PMID:23559515; http://dx. doi. org/10. 1093/jmcb/mjt010
48. Smith FO, Rauch C, Williams DE, March CJ, Arthur D, Hilden J, Lampkin BC, Buckley JD, Buckley CV, Woods WG et al. The human homologue of rat NG2, a chondroitin sulfate proteoglycan, is not expressed on the cell surface of normal hematopoietic cells but is expressed by acute myeloid leukemia blasts from poorprognosis patients with abnormalities of chromosome band 11q23. Blood 1996; 87:1123-33; PMID:8562938
49. Wang X, Osada T, Wang Y, Yu L, Sakakura K, Katayama A, McCarthy JB, Brufsky A, Chivukula M, Khoury T et al. CSPG4 protein as a new target for the antibody-based immunotherapy of triple-negative breast cancer. J Natl Cancer Inst 2010; 102:1496-512; PMID:20852124; http://dx. doi. org/10. 1093/jnci/ djq343
50. Stallcup WB, Huang FJ. A role for the NG2 proteoglycan in glioma progression. Cell Adh Migr 2008; 2:192-201; PMID:19262111; http://dx. doi. org/10. 4161/ cam. 2. 3. 6279
51. Foo SS, Turner CJ, Adams S, Compagni A, Aubyn D, Kogata N, Lindblom P, Shani M, Zicha D, Adams RH. Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell 2006; 124:161-73; PMID:16413489; http://dx. doi. org/10. 1016/j. cell. 2005. 10. 034
52. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 1999; 8:265-77; PMID:10621974; http://dx. doi. org/ 10. 1023/A:1008942828960
53. Stockmann C, Doedens A, Weidemann A, Zhang N, Takeda N, Greenberg JI, Cheresh DA, Johnson RS. Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature 2008; 456:814-8; PMID:18997773; http://dx. doi. org/ 10. 1038/nature07445