New model of macrophage acquisition of the lymphatic endothelial phenotype

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Hall, Kelly L ^a   Volk Draper, Lisa D ^a   Flister, Michael J ^a   Ran, Sophia ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; ALPHA9 INTEGRIN; CD11B ANTIGEN; CELL MARKER; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; NOTCH1 RECEPTOR; PODOPLANIN; PROTEIN F4 80; PROTEIN LY6C; PROTEIN LYVE 1; TRANSCRIPTION FACTOR C MAF; UNCLASSIFIED DRUG; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 3; GREEN FLUORESCENT PROTEIN; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CELL CULTURE; CELL DIFFERENTIATION; CELL INFILTRATION; CELL POPULATION; CELL TYPE; CONTROLLED STUDY; DIAPHRAGM; ENDOTHELIAL PROGENITOR CELL; FEMALE; GENE CONTROL; GENE EXPRESSION; INFLAMMATORY LYMPHANGIOGENESIS; INTRACELLULAR SIGNALING; LYMPH VESSEL; LYMPHANGIOGENESIS; LYMPHATIC ENDOTHELIAL PROGENITOR CELL; MACROPHAGE; MACROPHAGE ACTIVATION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PERITONITIS; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL LINE; CYTOLOGY; ENDOTHELIUM CELL; INFLAMMATION; LYMPHATIC SYSTEM; METABOLISM; PHOSPHORYLATION;

MUS;

ANIMALS; ANTIGENS, CD11B; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; ENDOTHELIAL CELLS; GREEN FLUORESCENT PROTEINS; INFLAMMATION; LIPOPOLYSACCHARIDES; LYMPHATIC SYSTEM; MACROPHAGES; MICE; MICE, INBRED BALB C; NF-KAPPA B; PHENOTYPE; PHOSPHORYLATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84857728639     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031794     Document Type: Article

References (64)

1. Shin WS, Rockson SG, (2008) Animal models for the molecular and mechanistic study of lymphatic biology and disease. Ann N Y Acad Sci 1131: 50-74.
2. Olszewski WL, (2003) The lymphatic system in body homeostasis: physiological conditions. Lymphat Res Biol 1: 11-21.
3. Tso P, Pitts V, Granger DN, (1985) Role of lymph flow in intestinal chylomicron transport. Am J Physiol 249: G21-G28.
4. Johnson LA, Jackson DG, (2008) Cell traffic and the lymphatic endothelium. Ann N Y Acad Sci 1131: 119-133.
5. Mouta C, Heroult M, (2003) Inflammatory triggers of lymphangiogenesis. Lymphat Res Biol 1: 201-218.
6. Ran S, Volk L, Hall K, Flister MJ, (2009) Lymphangiogenesis and lymphatic metastasis in breast cancer. Pathophysiology 17: 229-251.
7. Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, et al. (2001) Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7: 192-198.
8. Baluk P, Tammela T, Ator E, Lyubynska N, Achen MG, et al. (2005) Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J Clin Invest 115: 247-257.
9. Ganta VC, Cromer W, Mills GL, Traylor J, Jennings M, et al. (2010) Angiopoietin-2 in experimental colitis. Inflamm Bowel Dis 16: 1029-1039.
10. Henno A, Blacher S, Lambert C, Colige A, Seidel L, et al. (2009) Altered expression of angiogenesis and lymphangiogenesis markers in the uninvolved skin of plaque-type psoriasis. Br J Dermatol 160: 581-590.
11. Kang S, Lee SP, Kim KE, Kim HZ, Memet S, et al. (2009) Toll-like receptor 4 in lymphatic endothelial cells contributes to LPS-induced lymphangiogenesis by chemotactic recruitment of macrophages. Blood 113: 2605-2613.
12. Zhang Q, Lu Y, Proulx ST, Guo R, Yao Z, et al. (2007) Increased lymphangiogenesis in joints of mice with inflammatory arthritis. Arthritis Res Ther 9: R118.
13. Maruyama K, Asai J, Ii M, Thorne T, Losordo DW, et al. (2007) Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing. Am J Pathol 170: 1178-1191.
14. Paavonen K, Puolakkainen P, Jussila L, Jahkola T, Alitalo K, (2000) Vascular endothelial growth factor receptor-3 in lymphangiogenesis in wound healing. Am J Pathol 156: 1499-1504.
15. Veikkola T, Jussila L, Makinen T, Karpanen T, Jeltsch M, et al. (2001) Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J 20: 1223-1231.
16. Makinen T, Veikkola T, Mustjoki S, Karpanen T, Catimel B, et al. (2001) Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J 20: 4762-4773.
17. Flister MJ, Wilber A, Hall KL, Iwata C, Miyazono K, et al. (2010) Inflammation induces lymphangiogenesis through up-regulation of VEGFR-3 mediated by NF-kappaB and Prox1. Blood 115: 418-429.
18. Wigle JT, Oliver G, (1999) Prox1 function is required for the development of the murine lymphatic system. Cell 98: 769-778.
19. Pytowski B, Goldman J, Persaud K, Wu Y, Witte L, et al. (2005) Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J Natl Cancer Inst 97: 14-21.
20. Roberts N, Kloos B, Cassella M, Podgrabinska S, Persaud K, et al. (2006) Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2. Cancer Res 66: 2650-2657.
21. Achen MG, Jeltsch M, Kukk E, Makinen T, Vitali A, et al. (1998) Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci U S A 95: 548-553.
22. Ristimaki A, Narko K, Enholm B, Joukov V, Alitalo K, (1998) Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J Biol Chem 273: 8413-8418.
23. Trompezinski S, Berthier-Vergnes O, Denis A, Schmitt D, Viac J, (2004) Comparative expression of vascular endothelial growth factor family members, VEGF-B,-C and-D, by normal human keratinocytes and fibroblasts. Exp Dermatol 13: 98-105.
24. Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, et al. (2004) VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 113: 1040-1050.
25. Iwata C, Kano MR, Komuro A, Oka M, Kiyono K, et al. (2007) Inhibition of cyclooxygenase-2 suppresses lymph node metastasis via reduction of lymphangiogenesis. Cancer Res 67: 10181-10189.
26. Srinivasan RS, Dillard ME, Lagutin OV, Lin FJ, Tsai S, et al. (2007) Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev 21: 2422-2432.
27. Jiang S, Bailey AS, Goldman DC, Swain JR, Wong MH, et al. (2008) Hematopoietic stem cells contribute to lymphatic endothelium. PLoS ONE 3: e3812.
28. Zumsteg A, Baeriswyl V, Imaizumi N, Schwendener R, Ruegg C, et al. (2009) Myeloid cells contribute to tumor lymphangiogenesis. PLoS ONE 4: e7067.
29. Kerjaschki D, Huttary N, Raab I, Regele H, Bojarski-Nagy K, et al. (2006) Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat Med 12: 230-234.
30. Religa P, Cao R, Bjorndahl M, Zhou Z, Zhu Z, et al. (2005) Presence of bone marrow-derived circulating progenitor endothelial cells in the newly formed lymphatic vessels. Blood 106: 4184-4190.
31. Lee JY, Park C, Cho YP, Lee E, Kim H, et al. (2010) Podoplanin-expressing cells derived from bone marrow play a crucial role in postnatal lymphatic neovascularization. Circulation 122: 1413-1425.
32. Buttler K, Ezaki T, Wilting J, (2008) Proliferating mesodermal cells in murine embryos exhibiting macrophage and lymphendothelial characteristics. BMC Dev Biol 8: 43.
33. Maruyama K, Ii M, Cursiefen C, Jackson DG, Keino H, et al. (2005) Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest 115: 2363-2372.
34. Suzuki H, Watabe T, Kato M, Miyazawa K, Miyazono K, (2005) Roles of vascular endothelial growth factor receptor 3 signaling in differentiation of mouse embryonic stem cell-derived vascular progenitor cells into endothelial cells. Blood 105: 2372-2379.
35. Conrad C, Niess H, Huss R, Huber S, von Luettichau I, et al. (2009) Multipotent mesenchymal stem cells acquire a lymphendothelial phenotype and enhance lymphatic regeneration in vivo. Circulation 119: 281-289.
36. Cimato T, Beers J, Ding S, Ma M, McCoy JP, et al. (2009) Neuropilin-1 identifies endothelial precursors in human and murine embryonic stem cells before CD34 expression. Circulation 119: 2170-2178.
37. Skobe M, Hamberg LM, Hawighorst T, Schirner M, Wolf GL, et al. (2001) Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma. Am J Pathol 159: 893-903.
38. Saaristo A, Tammela T, Farkkila A, Karkkainen M, Suominen E, et al. (2006) Vascular endothelial growth factor-C accelerates diabetic wound healing. Am J Pathol 169: 1080-1087.
39. Kim KE, Koh YJ, Jeon BH, Jang C, Han J, et al. (2009) Role of CD11b+ macrophages in intraperitoneal lipopolysaccharide-induced aberrant lymphangiogenesis and lymphatic function in the diaphragm. Am J Pathol 175: 1733-1745.
40. Young PP, Ardestani S, Li B, (2010) Myeloid cells in cancer progression: unique subtypes and their roles in tumor growth, vascularity, and host immune suppression. Cancer Microenviron 4: 1-11.
41. Gordon S, Taylor PR, (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953-964.
42. Ralph P, Nakoinz I, (1977) Antibody-dependent killing of erythrocyte and tumor targets by macrophage-related cell lines: enhancement by PPD and LPS. J Immunol 119: 950-954.
43. Flister MJ, Volk LD, Ran S, (2011) Characterization of Prox1 and VEGFR-3 expression and lymphatic phenotype in normal organs of mice lacking p50 subunit of NF-kappaB. Microcirculation 18: 85-101.
44. Jeon BH, Jang C, Han J, Kataru RP, Piao L, et al. (2008) Profound but dysfunctional lymphangiogenesis via vascular endothelial growth factor ligands from CD11b+ macrophages in advanced ovarian cancer. Cancer Res 68: 1100-1109.
45. Watari K, Nakao S, Fotovati A, Basaki Y, Hosoi F, et al. (2008) Role of macrophages in inflammatory lymphangiogenesis: Enhanced production of vascular endothelial growth factor C and D through NF-kappaB activation. Biochem Biophys Res Commun 377: 826-831.
46. Makinen T, Jussila L, Veikkola T, Karpanen T, Kettunen MI, et al. (2001) Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat Med 7: 199-205.
47. Salven P, Mustjoki S, Alitalo R, Alitalo K, Rafii S, (2003) VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells. Blood 101: 168-172.
48. Bogos K, Renyi-Vamos F, Dobos J, Kenessey I, Tovari J, et al. (2009) High VEGFR-3-positive circulating lymphatic/vascular endothelial progenitor cell level is associated with poor prognosis in human small cell lung cancer. Clin Cancer Res 15: 1741-1746.
49. Hosking B, Francois M, Wilhelm D, Orsenigo F, Caprini A, et al. (2009) Sox7 and Sox17 are strain-specific modifiers of the lymphangiogenic defects caused by Sox18 dysfunction in mice. Development 136: 2385-2391.
50. Francois M, Caprini A, Hosking B, Orsenigo F, Wilhelm D, et al. (2008) Sox18 induces development of the lymphatic vasculature in mice. Nature 456: 643-647.
51. Shawber CJ, Funahashi Y, Francisco E, Vorontchikhina M, Kitamura Y, et al. (2007) Notch alters VEGF responsiveness in human and murine endothelial cells by direct regulation of VEGFR-3 expression. J Clin Invest 117: 3369-3382.
52. Srinivasan RS, Geng X, Yang Y, Wang Y, Mukatira S, et al. (2010) The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev 24: 696-707.
53. Lin FJ, Chen X, Qin J, Hong YK, Tsai MJ, et al. (2010) Direct transcriptional regulation of neuropilin-2 by COUP-TFII modulates multiple steps in murine lymphatic vessel development. J Clin Invest 120: 1694-1707.
54. Banerji S, Ni J, Wang SX, Clasper S, Su J, et al. (1999) LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 144: 789-801.
55. Schacht V, Ramirez MI, Hong YK, Hirakawa S, Feng D, et al. (2003) T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J 22: 3546-3556.
56. Vlahakis NE, Young BA, Atakilit A, Sheppard D, (2005) The lymphangiogenic vascular endothelial growth factors VEGF-C and-D are ligands for the integrin alpha9beta1. J Biol Chem 280: 4544-4552.
57. De Palma M, Venneri MA, Galli R, Sergi SL, Politi LS, et al. (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8: 211-226.
58. Coffelt SB, Tal AO, Scholz A, De Palma M, Patel S, et al. (2010) Angiopoietin-2 Regulates Gene Expression in TIE2-Expressing Monocytes and Augments Their Inherent Proangiogenic Functions. Cancer Res 70: 5270-5280.
59. Pucci F, Venneri MA, Biziato D, Nonis A, Moi D, et al. (2009) A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood "resident" monocytes, and embryonic macrophages suggests common functions and developmental relationships. Blood 114: 901-914.
60. Klagsbrun M, Eichmann A, (2005) A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Factor Rev 16: 535-548.
61. Kono T, Kubo H, Shimazu C, Ueda Y, Takahashi M, et al. (2006) Differentiation of lymphatic endothelial cells from embryonic stem cells on OP9 stromal cells. Arterioscler Thromb Vasc Biol 26: 2070-2076.
62. Hartley JW, Evans LH, Green KY, Naghashfar Z, Macias AR, et al. (2008) Expression of infectious murine leukemia viruses by RAW264.7 cells, a potential complication for studies with a widely used mouse macrophage cell line. Retrovirology 5: 1.
63. Natarajan M, Lin KM, Hsueh RC, Sternweis PC, Ranganathan R, (2006) A global analysis of cross-talk in a mammalian cellular signalling network. Nat Cell Biol 8: 571-580.
64. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.