Expression of VEGF Receptors on Endothelial Cells in Mouse Skeletal Muscle

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Imoukhuede, Princess I ^a   Popel, Aleksander S ^b  

^a University of Illinois at Urbana Champaign   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; PHYCOERYTHRIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CELL HETEROGENEITY; CELL ISOLATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EX VIVO STUDY; FEMALE; FIBROBLAST; FLUORESCENCE ANALYSIS; GASTROCNEMIUS MUSCLE; HINDLIMB; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE;

3T3 CELLS; ANIMALS; CALIBRATION; ENDOTHELIAL CELLS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICROCIRCULATION; MUSCLE, SKELETAL; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

MUS;

EID: 84866309317     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044791     Document Type: Article

References (120)

1. Semenza GL, (2004) O2-regulated gene expression: transcriptional control of cardiorespiratory physiology by HIF-1. J Appl Physiol 96: 1173-1177.
2. Hiratsuka S, Maru Y, Okada A, Seiki M, Noda T, et al. (2001) Involvement of Flt-1 Tyrosine Kinase (Vascular Endothelial Growth Factor Receptor-1) in Pathological Angiogenesis. Cancer Res 61: 1207-1213.
3. Dunk C, Ahmed A, (2001) Vascular Endothelial Growth Factor Receptor-2-Mediated Mitogenesis Is Negatively Regulated by Vascular Endothelial Growth Factor Receptor-1 in Tumor Epithelial Cells. Am J Pathol 158: 265-273.
4. Meyer RD, Mohammadi M, Rahimi N, (2006) A Single Amino Acid Substitution in the Activation Loop Defines the Decoy Characteristic of VEGFR-1/FLT-1. Journal of Biological Chemistry 281: 867-875.
5. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M, (1998) Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proceedings of the National Academy of Sciences of the United States of America 95: 9349-9354.
6. Qutub AA, Mac Gabhann F, Karagiannis ED, Vempati P, Popel AS, (2009) Multiscale models of angiogenesis. IEEE Eng Med Biol Mag 28: 14-31.
7. Mac Gabhann F, Qutub AA, Annex BH, Popel AS, (2010) Systems biology of pro-angiogenic therapies targeting the VEGF system. Wiley Interdisciplinary Reviews: Systems Biology and Medicine 2: 694-707.
8. Wu FT, Stefanini MO, Mac Gabhann F, Popel AS, (2009) Modeling of growth factor-receptor systems from molecular-level protein interaction networks to whole-body compartment models. Methods Enzymol 467: 461-497.
9. Stefanini M, Wu F, Mac Gabhann F, Popel A, (2008) A compartment model of VEGF distribution in blood, healthy and diseased tissues. BMC Systems Biology 2: 77.
10. Stefanini MO, Wu FTH, Mac Gabhann F, Popel AS, (2009) The Presence of VEGF Receptors on the Luminal Surface of Endothelial Cells Affects VEGF Distribution and VEGF Signaling. PLoS Comput Biol 5: e1000622.
11. Mac Gabhann F, Popel AS, (2007) Dimerization of VEGF receptors and implications for signal transduction: A computational study. Biophysical Chemistry 128: 125-139.
12. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH, (1994) Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem 269: 26988-26995.
13. Vaisman N, Gospodarowicz D, Neufeld G, (1990) Characterization of the receptors for vascular endothelial growth factor. J Biol Chem 265: 19461-19466.
14. Prahst C, Heroult M, Lanahan AA, Uziel N, Kessler O, et al. (2008) Neuropilin-1-VEGFR-2 complexing requires the PDZ-binding domain of neuropilin-1. J Biol Chem 283: 25110-25114.
15. Gitay-Goren H, Soker S, Vlodavsky I, Neufeld G, (1992) The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules. Journal of Biological Chemistry 267: 6093-6098.
16. Chen J-H, Wang X-C, Kan M, Sato JD, (2001) Effect of FGF-1 and FGF-2 on VEGF Binding to Human Umbilical Vein Endothelial Cells. Cell Biology International 25: 257-260.
17. Imoukhuede PI, Popel AS, (2011) Quantification and cell-to-cell variation of vascular endothelial growth factor receptors. Experimental Cell Research 317: 955-965.
18. Aronowski J, Labiche L, (2003) Perspectives on reperfusion-induced damage in rodent models of experimental focal ischemia and role of gamma-protein kinase C. ILAR journal. 44: 105-109.
19. Chalothorn D, Clayton JA, Zhang H, Pomp D, Faber JE, (2007) Collateral density, remodeling, and VEGF-A expression differ widely between mouse strains. Physiol Genomics 30: 179-191.
20. Helisch A, Wagner S, Khan N, Drinane M, Wolfram S, et al. (2006) Impact of Mouse Strain Differences in Innate Hindlimb Collateral Vasculature. Arteriosclerosis, Thrombosis, and Vascular Biology 26: 520-526.
21. Dokun AO, Keum S, Hazarika S, Li Y, Lamonte GM, et al. (2008) A Quantitative Trait Locus (LSq-1) on Mouse Chromosome 7 Is Linked to the Absence of Tissue Loss After Surgical Hindlimb Ischemia. Circulation 117: 1207-1215.
22. Sugimori H, Yao H, Ooboshi H, Ibayashi S, Iida M, (2004) Krypton laser-induced photothrombotic distal middle cerebral artery occlusion without craniectomy in mice. Brain Research Protocols 13: 189-196.
23. Majid A, He YY, Gidday JM, Kaplan SS, Gonzales ER, et al. (2000) Differences in vulnerability to permanent focal cerebral ischemia among 3 common mouse strains. Stroke 31: 2707-2714.
24. Barone FC, Knudsen DJ, Nelson AH, Feuerstein GZ, Willette RN, (1993) Mouse Strain Differences in Susceptibility to Cerebral Ischemia Are Related to Cerebral Vascular Anatomy. J Cereb Blood Flow Metab 13: 683-692.
25. Mac Gabhann F, Peirce SM, (2010) Collateral Capillary Arterialization following Arteriolar Ligation in Murine Skeletal Muscle. Microcirculation 17: 333-347.
26. Scholz D, Ziegelhoeffer T, Helisch A, Wagner S, Friedrich C, et al. (2002) Contribution of Arteriogenesis and Angiogenesis to Postocclusive Hindlimb Perfusion in Mice. Journal of Molecular and Cellular Cardiology 34: 775-787.
27. Fukino K, Sata M, Seko Y, Hirata Y, Nagai R, (2003) Genetic background influences therapeutic effectiveness of VEGF. Biochemical and Biophysical Research Communications 310: 143-147.
28. Cherwek DH, Hopkins MB, Thompson MJ, Annex BH, Taylor DA, (2000) Fiber type-specific differential expression of angiogenic factors in response to chronic hindlimb ischemia. Am J Physiol Heart Circ Physiol 279: H932-938.
29. Annex BH, Torgan CE, Lin P, Taylor DA, Thompson MA, et al. (1998) Induction and maintenance of increased VEGF protein by chronic motor nerve stimulation in skeletal muscle. Am J Physiol Heart Circ Physiol 274: H860-867.
30. Lloyd PG, Prior BM, Yang HT, Terjung RL, (2003) Angiogenic growth factor expression in rat skeletal muscle in response to exercise training. Am J Physiol Heart Circ Physiol 284: H1668-1678.
31. Elowitz MB, Levine AJ, Siggia ED, Swain PS, (2002) Stochastic Gene Expression in a Single Cell. Science 297: 1183-1186.
32. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S, (2006) Stochastic mRNA synthesis in mammalian cells. Plos Biology 4: 1707-1719.
33. Raj A, van Oudenaarden A, (2008) Nature, Nurture, or Chance: Stochastic Gene Expression and Its Consequences. Cell 135: 216-226.
34. Janes KA, Wang C-C, Holmberg KJ, Cabral K, Brugge JS, (2010) Identifying single-cell molecular programs by stochastic profiling. Nat Meth 7: 311-317.
35. Niepel M, Spencer SL, Sorger PK, (2009) Non-genetic cell-to-cell variability and the consequences for pharmacology. Current Opinion in Chemical Biology 13: 556-561.
36. McKinney-Freeman SL, Jackson KA, Camargo FD, Ferrari G, Mavilio F, et al. (2002) Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proceedings of the National Academy of Sciences of the United States of America 99: 1341-1346.
37. Majka SM, Jackson KA, Kienstra KA, Majesky MW, Goodell MA, et al. (2003) Distinct progenitor populations in skeletal muscle are bone marrow derived and exhibit different cell fates during vascular regeneration. J Clin Invest 111: 71-79.
38. van BeijnumJR, Rousch M, Castermans K, van der Linden E, Griffioen AW, (2008) Isolation of endothelial cells from fresh tissues. Nat Protocols 3: 1085-1091.
39. Nielsen JS, McNagny KM, (2009) CD34 is a Key Regulator of Hematopoietic Stem Cell Trafficking to Bone Marrow and Mast Cell Progenitor Trafficking in the Periphery. Microcirculation 16: 487-496.
40. Nielsen JS, McNagny KM, (2008) Novel functions of the CD34 family. Journal of Cell Science 121: 3683-3692.
41. Lili W, Fatima A, Adolfas KG, Robert FV, Gerald EM, (2006) Comparison of fluorescein and phycoerythrin conjugates for quantifying CD20 expression on normal and leukemic B-cells. Cytometry Part B: Clinical Cytometry 70B: 410-415.
42. Kulwinder KP, Edward TJ, Sujata BI, (2001) Performance evaluation of quantiBRITE phycoerythrin beads. Cytometry 45: 250-258.
43. Gero B, Ferdinand H, Ruth K, (1994) Flow cytometric detection and quantitation of the epidermal growth factor receptor in comparison to Scatchard analysis in human bladder carcinoma cell lines. Cytometry 17: 75-83.
44. Rose NL, Palcic MM, Shapiro AMJ, Lakey JRT, (2003) An evaluation of the activation of endogenous pancreatic enzymes during human islet isolations. Transplantation Proceedings 35: 2455-2457.
45. Villaschi S, Nicosia RF, (1994) Paracrine interactions between fibroblasts and endothelial cells in a serum-free coculture model. Modulation of angiogenesis and collagen gel contraction. Laboratory Investigation 71: 291-299.
46. Jeong JH, Chan V, Cha C, Zorlutuna P, Dyck C, et al. (2011) "Living" Microvascular Stamp for Patterning of Functional Neovessels; Orchestrated Control of Matrix Property and Geometry. Advanced Materials 24: 58-63.
47. D'Agostino RB, Belanger A, D'Agostino RB Jr, (1990) A Suggestion for Using Powerful and Informative Tests of Normality. The American Statistician 44: 316-321.
48. DeCarlo LT, (1997) On the Meaning and Use of Kurtosis. Psychological Methods 2: 292-307.
49. Balanda KP, MacGillivray HL, (1988) Kurtosis: A Critical Review. The American Statistician 42: 111-119.
50. Zhang Z, Neiva K, Lingen M, Ellis L, Nor J (2010) VEGF-dependent tumor angiogenesis requires inverse and reciprocal regulation of VEGFR1 and VEGFR2. Cell Death and Differentiation: 499-512.
51. Li S, Lao J, Chen BPC, Li Y-s, Zhao Y, et al. (2002) Genomic analysis of smooth muscle cells in three-dimensional collagen matrix. The FASEB Journal.
52. Grayson WL, Ma T, Bunnell B, (2004) Human Mesenchymal Stem Cells Tissue Development in 3D PET Matrices. Biotechnology progress 20: 905-912.
53. Cukierman E, Pankov R, Stevens DR, Yamada KM, (2001) Taking Cell-Matrix Adhesions to the Third Dimension. Science 294: 1708-1712.
54. Smalley KSM, (2006) Life ins't flat: Taking cancer biology to the next dimension. In vitro cellular developmental biologyAnimal 42: 242.
55. Davis GE, Stratman AN, Sacharidou A, Koh W (2011) Chapter Three- Molecular Basis for Endothelial Lumen Formation and Tubulogenesis During Vasculogenesis and Angiogenic Sprouting. International Review of Cell and Molecular Biology: Academic Press. 101-165.
56. Birgersdotter A, Sandberg R, Ernberg I, (2005) Gene expression perturbation in vitroâ€"A growing case for three-dimensional (3D) culture systems. 3D Cultures in Cancer Biology 15: 405-412.
57. Hynes RO, (1999) Cell adhesion: old and new questions. Trends in Genetics 15: M33-M37.
58. Clare H, (2011) Hetheridge (2011) Uses of the in vitro endothelial-fibroblast organotypic co-culture assay in angiogenesis research. Biochemical Society Transactions 39: 1597.
59. Bishop ET, (1999) An in vitro model of angiogenesis: basic features. Angiogenesis 3: 335.
60. Bobik A, Campbell JH, (1993) Vascular derived growth factors: cell biology, pathophysiology, and pharmacology. Pharmacological reviews 45: 1-42.
61. Nicosia RF, Nicosia SV, Smith M, (1994) Vascular endothelial growth factor, platelet-derived growth factor, and insulin-like growth factor-1 promote rat aortic angiogenesis in vitro. The American Journal of Pathology 145: 1023-1029.
62. Dewey CF, Bussolari SR, Gimbrone MA, PF D, (1981) The dynamic response of vascular endothelial cells to fluid shear stress. Journal of Biomechanical Engineering 103: 177.
63. Cukierman E, Pankov R, Yamada KM, (2002) Cell interactions with three-dimensional matrices. Current opinion in cell biology 14: 633-640.
64. Takahashi T, Shibuya M, (1997) The 230 kDa mature form of KDR/Flk-1 (VEGF receptor-2) activates the PLC-γ pathway and partially induces mitotic signals in NIH3T3 fibroblasts. Oncogene 14: 2079.
65. Sawano A, Takahashi T, Yamaguchi S, Aonuma M, Shibuya M, (1996) Flt-1 but not KDR/Flk-1 tyrosine kinase is a receptor for placenta growth factor, which is related to vascular endothelial growth factor. Cell Growth Differ 7: 213-221.
66. Seetharam L, Gotoh N, Maru Y, Neufeld G, Yamaguchi S, et al. (1995) A unique signal transduction from FLT tyrosine kinase, a receptor for vascular endothelial growth factor VEGF. Oncogene 10: 135-147.
67. Jin X, Ge X, Zhu D-l, Yan C, Chu Y-F, et al. (2007) Expression and function of vascular endothelial growth factor receptors (Flt-1 and Flk-1) in vascular adventitial fibroblasts. Journal of Molecular and Cellular Cardiology 43: 292-300.
68. Berthaut A, Mirshahi P, Benabbou N, Azzazene D, Bordu C, et al. (2009) Vascular endothelial growth factor receptor-1 (VEGFR-1) expression in human corneal fibroblast decreased with age. Mol Vis 15: 1997-2007.
69. Sawano A, Iwai S, Sakurai Y, Ito M, Shitara K, et al. (2001) Flt-1, vascular endothelial growth factor receptor 1, is a novel cell surface marker for the lineage of monocyte-macrophages in humans. Blood 97: 785-791.
70. Shibuya M, (2006) Vascular endothelial growth factor receptor-1 (VEGFR-1/Flt-1): a dual regulator for angiogenesis. Angiogenesis 9: 225-230.
71. Clauss M, Gerlach M, Gerlach H, Brett J, Wang F, et al. (1990) Vascular permeability factor: a tumor-derived polypeptide that induces endothelial cell and monocyte procoagulant activity, and promotes monocyte migration. The Journal of Experimental Medicine 172: 1535-1545.
72. Ferrara N, Gerber H-P, LeCouter J, (2003) The biology of VEGF and its receptors. Nat Med 9: 669-676.
73. Olsson A-K, Dimberg A, Kreuger J, Claesson-Welsh L, (2006) VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 7: 359-371.
74. Kearney JB, Kappas NC, Ellerstrom C, DiPaola FW, Bautch VL, (2004) The VEGF receptor flt-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis. Blood 103: 4527-4535.
75. Gampel A, Moss L, Jones MC, Brunton V, Norman JC, et al. (2006) VEGF regulates the mobilization of VEGFR2/KDR from an intracellular endothelial storage compartment. Blood 108: 2624-2631.
76. Ewan LC, Jopling HM, Jia H, Mittar S, Bagherzadeh A, et al. (2006) Intrinsic Tyrosine Kinase Activity is Required for Vascular Endothelial Growth Factor Receptor 2 Ubiquitination, Sorting and Degradation in Endothelial Cells. Traffic 7: 1270-1282.
77. Mittar S, Ulyatt C, Howell GJ, Bruns AF, Zachary I, et al. (2009) VEGFR1 receptor tyrosine kinase localization to the Golgi apparatus is calcium-dependent. Experimental Cell Research 315: 877-889.
78. Jopling HM, Howell GJ, Gamper N, Ponnambalam S, (2011) The VEGFR2 receptor tyrosine kinase undergoes constitutive endosome-to-plasma membrane recycling. Biochemical and Biophysical Research Communications 410: 170-176.
79. Jopling HM, Odell AF, Hooper NM, Zachary IC, Walker JH, et al. (2009) Rab GTPase Regulation of VEGFR2 Trafficking and Signaling in Endothelial Cells. Arteriosclerosis, Thrombosis, and Vascular Biology 29: 1119-1124.
80. Lampugnani MG, Orsenigo F, Gagliani MC, Tacchetti C, Dejana E, (2006) Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. The Journal of Cell Biology 174: 593-604.
81. Bhattacharya R, Kang-Decker N, Hughes DA, Mukherjee P, Shah V, et al. (2005) Regulatory role of dynamin-2 in VEGFR-2/KDR-mediated endothelial signaling. The FASEB Journal 19: 1692-1694.
82. Jones MC, Caswell PT, Moran-Jones K, Roberts M, Barry ST, et al. (2009) VEGFR1 (Flt1) Regulates Rab4 Recycling to Control Fibronectin Polymerization and Endothelial Vessel Branching. Traffic 10: 754-766.
83. Bruns A, Bao L, Walker J, Ponnambalam S, (2009) VEGF-A-stimulated signalling in endothelial cells via a dual receptor tyrosine kinase system is dependent on co-ordinated trafficking and proteolysis. Biochemical Society Transactions 37: 1193-1197.
84. Rush JS, Quinalty LM, Engelman L, Sherry DM, Ceresa BP, (2012) Endosomal Accumulation of the Activated Epidermal Growth Factor Receptor (EGFR) Induces Apoptosis. Journal of Biological Chemistry 287: 712-722.
85. Sorkin A, von Zastrow M, (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10: 609-622.
86. Sorkin A, von Zastrow M, (2002) Signal transduction and endocytosis: close encounters of many kinds. Nat Rev Mol Cell Biol 3: 600-614.
87. Nilsson I, Bahram F, Li X, Gualandi L, Koch S, et al. (2010) VEGF receptor 2/-3 heterodimers detected in situ by proximity ligation on angiogenic sprouts. EMBO J 29: 1377-1388.
88. Neagoe PE, Lemieux C, Sirois MG, (2005) Vascular endothelial growth factor (VEGF)-A165-induced prostacyclin synthesis requires the activation of VEGF receptor-1 and-2 heterodimer. Journal of Biological Chemistry 280: 9904-9912.
89. Huang K, Andersson C, Roomans GM, Ito N, Claesson-Welsh L, (2001) Signaling properties of VEGF receptor-1 and-2 homo- and heterodimers. The International Journal of Biochemistry & Cell Biology 33: 315-324.
90. Cao Y (2009) Positive and Negative Modulation of Angiogenesis by VEGFR1 Ligands. Sci Signal 2: re1-.
91. Hudlicka O, (1985) Development and adaptability of microvasculature in skeletal muscle. J Exp Biol 115: 215-228.
92. Murakami S, Fujino H, Takeda I, Momota R, Kumagishi K, et al. (2010) Comparison of capillary architecture between slow and fast muscles in rats using a confocal laser scanning microscope. Acta Med Okayama 64: 11-18.
93. Pilpel Y, Castrillo JI, Oliver SG (2011) Noise in Biological Systems: Pros, Cons, and Mechanisms of Control Yeast Systems Biology: Humana Press. 407-425.
94. Bentley K, Gerhardt H, Bates PA, (2008) Agent-based simulation of notch-mediated tip cell selection in angiogenic sprout initialisation. Journal of Theoretical Biology 250: 25-36.
95. Bentley K, Mariggi G, Gerhardt H, Bates PA, (2009) Tipping the Balance: Robustness of Tip Cell Selection, Migration and Fusion in Angiogenesis. PLoS Comput Biol 5: e1000549.
96. Stefanini MO, Wu FTH, Mac Gabhann F, Popel AS, (2010) Increase of plasma VEGF after intravenous administration of bevacizumab is predicted by a pharmacokinetic model. Cancer Research 70: 9886-9894.
97. Finley S, Engel-Stefanini M, Imoukhuede PI, Popel A, (2011) Pharmacokinetics and pharmacodynamics of VEGF-neutralizing antibodies. BMC Systems Biology 5: 193.
98. Wu FTH, Stefanini MO, Mac Gabhann F, Kontos CD, Annex BH, et al. (2009) Computational kinetic model of VEGF trapping by soluble VEGF receptor-1: effects of transendothelial and lymphatic macromolecular transport. Physiological Genomics 38: 29-41.
99. Wu FTH, Stefanini MO, Gabhann FM, Kontos CD, Annex BH, et al. (2010) VEGF and soluble VEGF receptor-1 (sFlt-1) distributions in peripheral arterial disease: an in silico model. American Journal of Physiology- Heart and Circulatory Physiology 298: H2174-H2191.
100. Wu FTH, Stefanini MO, Mac Gabhann F, Popel AS, (2009) A Compartment Model of VEGF Distribution in Humans in the Presence of Soluble VEGF Receptor-1 Acting as a Ligand Trap. PLoS ONE 4: e5108.
101. Mac Gabhann F, Ji J, Popel A, (2007) Multi-scale Computational Models of Pro-angiogenic Treatments in Peripheral Arterial Disease. Annals of Biomedical Engineering 35: 982-994.
102. Gevertz JL, Torquato S, (2006) Modeling the effects of vasculature evolution on early brain tumor growth. Journal of Theoretical Biology 243: 517-531.
103. Bauer AL, Jackson TL, Jiang Y, (2007) A Cell-Based Model Exhibiting Branching and Anastomosis during Tumor-Induced Angiogenesis. Biophysical Journal 92: 3105-3121.
104. Peirce SM, (2008) Computational and Mathematical Modeling of Angiogenesis. Microcirculation 15: 739-751.
105. Liu P, Ying Y-s, Anderson RGW, (1997) Platelet-derived growth factor activates mitogen-activated protein kinase in isolated caveolae. Proceedings of the National Academy of Sciences 94: 13666-13670.
106. Mitsuda T, Furukawa K, Fukumoto S, Miyazaki H, Urano T, et al. (2002) Overexpression of Ganglioside GM1 Results in the Dispersion of Platelet-derived Growth Factor Receptor from Glycolipid-enriched Microdomains and in the Suppression of Cell Growth Signals. Journal of Biological Chemistry 277: 11239-11246.
107. Miljan EA, Bremer EG (2002) Regulation of Growth Factor Receptors by Gangliosides. Sci STKE 2002: re15-.
108. Raghu H, Sodadasu P, Malla R, Gondi C, Estes N, et al. (2010) Localization of uPAR and MMP-9 in lipid rafts is critical for migration, invasion and angiogenesis in human breast cancer cells. BMC Cancer 10: 647.
109. Chu CL, Buczek-Thomas JA, Nugent MA, (2004) Heparan sulphate proteoglycans modulate fibroblast growth factor-2 binding through a lipid raft-mediated mechanism. Biochem J 379: 331-341.
110. Lajoie P, Goetz JG, Dennis JW, Nabi IR, (2009) Lattices, rafts, and scaffolds: domain regulation of receptor signaling at the plasma membrane. The Journal of Cell Biology 185: 381-385.
111. Sonveaux P, Martinive P, DeWever J, Batova Z, Daneau G, et al. (2004) Caveolin-1 Expression Is Critical for Vascular Endothelial Growth Factor-Induced Ischemic Hindlimb Collateralization and Nitric Oxide-Mediated Angiogenesis. Circulation Research 95: 154-161.
112. Casalou C, Costa A, Carvalho T, Gomes AL, Zhu Z, et al. (2011) Cholesterol Regulates VEGFR-1 (FLT-1) Expression and Signaling in Acute Leukemia Cells. Molecular Cancer Research 9: 215-224.
113. Labrecque L, Royal I, Surprenant DS, Patterson C, Gingras D, et al. (2003) Regulation of Vascular Endothelial Growth Factor Receptor-2 Activity by Caveolin-1 and Plasma Membrane Cholesterol. Molecular Biology of the Cell 14: 334-347.
114. Bernatchez PN, Acevedo L, Fernandez-Hernando C, Murata T, Chalouni C, et al. (2007) Myoferlin Regulates Vascular Endothelial Growth Factor Receptor-2 Stability and Function. Journal of Biological Chemistry 282: 30745-30753.
115. Sundberg C, Friman T, Hecht LE, Kuhl C, Solomon KR, (2009) Two Different PDGF β-Receptor Cohorts in Human Pericytes Mediate Distinct Biological Endpoints. The American Journal of Pathology 175: 171-189.
116. Zajchowski LD, Robbins SM, (2002) Lipid rafts and little caves. European Journal of Biochemistry 269: 737-752.
117. Simons K, Toomre D, (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31-39.
118. Edidin M, (2003) The State of Lipid Rafts: From Model Membranes to Cells. Annual Review of Biophysics and Biomolecular Structure 32: 257-283.
119. Quinn PJ, (2010) A lipid matrix model of membrane raft structure. Progress in Lipid Research 49: 390-406.
120. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, et al. (2012) Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing. New England Journal of Medicine 366: 883-892.