Compartmentalizing proximal FGFR1 signaling in ovine placental artery endothelial cell caveolae

Biology of Reproduction

Volumn 87, Issue 2, 2012, Pages

  Feng, Lin ^a   Zhang, Hong Hai ^a   Wang, Wen ^a   Zheng, Jing ^b   Chen, Dong Bao ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Caveolae; Caveolin 1; Frs2 ; Placental endothelial cells; Proximal FGF2 FGFR1 signaling

Indexed keywords

CAVEOLIN 1; CHOLESTEROL; FIBROBLAST GROWTH FACTOR RECEPTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR 2; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; METHYL BETA CYCLODEXTRIN; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAVEOLA; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; FETOPLACENTAL UNIT; NONHUMAN; PLACENTA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; ARTERIES; CAVEOLAE; CELLS, CULTURED; ENDOTHELIAL CELLS; FEMALE; FIBROBLAST GROWTH FACTOR 2; GRB2 ADAPTOR PROTEIN; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PLACENTA; PREGNANCY; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SHEEP; SIGNAL TRANSDUCTION;

OVIS;

EID: 84869439503     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.100750     Document Type: Article

References (43)

1. Beenken A, Mohammadi M. The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discov 2009; 8:235-253.
2. Johnson DE, Williams LT. Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 1993; 60:1-41.
3. Kouhara H, Hadari YR, Spivak-Kroizman T, Schilling J, Bar-Sagi D, Lax I, Schlessinger J. A lipid-anchored Grb2-binding protein that links FGFreceptor activation to the Ras/MAPK signaling pathway. Cell 1997; 89: 693-702.
4. Hadari YR, Gotoh N, Kouhara H, Lax I, Schlessinger J. Critical role for the docking-protein FRS2 alpha in FGF receptor-mediated signal transduction pathways. Proc Natl Acad Sci U S A 2001; 98:8578-8583.
5. Gotoh N. Regulation of growth factor signaling by FRS2 family docking/ scaffold adaptor proteins. Cancer Sci 2008; 99:1319-1325.
6. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG, King F, Roberts T, Ratnofsky S, Lechleider RJ, et al. SH2 domains recognize specific phosphopeptide sequences. Cell 1993; 72:767-778.
7. Hadari YR, Kouhara H, Lax I, Schlessinger J. Binding of Shp2 tyrosine phosphatase to FRS2 is essential for fibroblast growth factor-induced PC12 cell differentiation. Mol Cell Biol 1998; 18:3966-3973.
8. Lamothe B, Yamada M, Schaeper U, Birchmeier W, Lax I, Schlessinger J. The docking protein Gab1 is an essential component of an indirect mechanism for fibroblast growth factor stimulation of the phosphatidylinositol 3-kinase/Akt antiapoptotic pathway. Mol Cell Biol 2004; 24: 5657-5666.
9. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2000; 103: 211-225.
10. Schlessinger J. Common and distinct elements in cellular signaling via EGF and FGF receptors. Science 2004; 306:1506-1507.
11. Hunter T. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 1995; 80:225-236.
12. Mattoon DR, Lamothe B, Lax I, Schlessinger J. The docking protein Gab1 is the primary mediator of EGF-stimulated activation of the PI-3K/Akt cell survival pathway. BMC Biol 2004; 2:24.
13. Ong SH, Hadari YR, Gotoh N, Guy GR, Schlessinger J, Lax I. Stimulation of phosphatidylinositol 3-kinase by fibroblast growth factor receptors is mediated by coordinated recruitment of multiple docking proteins. Proc Natl Acad Sci U S A 2001; 98:6074-6079.
14. Bruns RR, Palade GE. Studies on blood capillaries. II. Transport of ferritin molecules across the wall of muscle capillaries. J Cell Biol 1968; 37: 277-299.
15. Bruns RR, Palade GE. Studies on blood capillaries. I. General organization of blood capillaries in muscle. J Cell Biol 1968; 37:244-276.
16. Palade GE, Bruns RR. Structural modulations of plasmalemmal vesicles. J Cell Biol 1968; 37:633-649.
17. de Laurentiis A, Donovan L, Arcaro A. Lipid rafts and caveolae in signaling by growth factor receptors. Open Biochem J 2007; 1:12-32.
18. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 1992; 68:673-682.
19. Predescu D, Palade GE. Plasmalemmal vesicles represent the large pore system of continuous microvascular endothelium. Am J Physiol 1993; 265:H725-H733.
20. Minshall RD, Tiruppathi C, Vogel SM, Malik AB. Vesicle formation and trafficking in endothelial cells and regulation of endothelial barrier function. Histochem Cell Biol 2002; 117:105-112.
21. Glenney JR Jr., Soppet D. Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc Natl Acad Sci U S A 1992; 89:10517-10521.
22. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 genedisrupted mice. Science 2001; 293:2449-2452.
23. Okamoto T, Schlegel A, Scherer PE, Lisanti MP. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes"at the plasma membrane. J Biol Chem 1998; 273:5419-5422.
24. Isshiki M, Ando J, Yamamoto K, Fujita T, Ying Y, Anderson RG. Sites of Ca(2{thorn}) wave initiation move with caveolae to the trailing edge of migrating cells. J Cell Sci 2002; 115:475-484.
25. Isshiki M, Ying YS, Fujita T, Anderson RG. A molecular sensor detects signal transduction from caveolae in living cells. J Biol Chem 2002; 277: 43389-43398.
26. Biswas SB, Hammond RW, Anderson LD. Fibroblast growth factors from bovine pituitary and human placenta and their functions in the maturation of porcine granulosa cells in vitro. Endocrinology 1988; 123:559-566.
27. Arany E, Hill DJ. Fibroblast growth factor-2 and fibroblast growth factor receptor-1 mRNA expression and peptide localization in placentae from normal and diabetic pregnancies. Placenta 1998; 19:133-142.
28. Borowicz PP, Arnold DR, Johnson ML, Grazul-Bilska AT, Redmer DA, Reynolds LP. Placental growth throughout the last two thirds of pregnancy in sheep: vascular development and angiogenic factor expression. Biol Reprod 2007; 76:259-267.
29. Pfarrer C, Weise S, Berisha B, Schams D, Leiser R, Hoffmann B, Schuler G. Fibroblast growth factor (FGF)-1, FGF2, FGF7 and FGF receptors are uniformly expressed in trophoblast giant cells during restricted trophoblast invasion in cows. Placenta 2006; 27:758-770.
30. Cooke FN, Pennington KA, Yang Q, Ealy AD. Several fibroblast growth factors are expressed during pre-attachment bovine conceptus development and regulate interferon-tau expression from trophectoderm. Reproduction 2009; 137:259-269.
31. Zheng J, Vagnoni KE, Bird IM, Magness RR. Expression of basic fibroblast growth factor, endothelial mitogenic activity, and angiotensin II type-1 receptors in the ovine placenta during the third trimester of pregnancy. Biol Reprod 1997; 56:1189-1197.
32. Zheng J, Bird IM, Melsaether AN, Magness RR. Activation of the mitogen-activated protein kinase cascade is necessary but not sufficient for basic fibroblast growth factor- and epidermal growth factor-stimulated expression of endothelial nitric oxide synthase in ovine fetoplacental artery endothelial cells. Endocrinology 1999; 140:1399-1407.
33. Feng L, Liao WX, Luo Q, Zhang HH, Wang W, Zheng J, Chen DB. Caveolin-1 orchestrates fibroblast growth factor 2 signaling control of angiogenesis in placental artery endothelial cell caveolae. J Cell Physiol 2012; 227:2480-2491.
34. Davy A, Feuerstein C, Robbins SM. Signaling within a caveolae-like membrane microdomain in human neuroblastoma cells in response to fibroblast growth factor. J Neurochem 2000; 74:676-683.
35. Ridyard MS, Robbins SM. Fibroblast growth factor-2-induced signaling through lipid raft-associated fibroblast growth factor receptor substrate 2 (FRS2). J Biol Chem 2003; 278:13803-13809.
36. Liao WX, Feng L, Zhang H, Zheng J, Moore TR, Chen DB. Compartmentalizing VEGF-induced ERK2/1 signaling in placental artery endothelial cell caveolae: a paradoxical role of caveolin-1 in placental angiogenesis in vitro. Mol Endocrinol 2009; 23:1428-1444.
37. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, Lisanti MP. Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and cofractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 1996; 271:15160-15165.
38. Couet J, Li S, Okamoto T, Ikezu T, Lisanti MP. Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 1997; 272:6525-6533.
39. Parpal S, Karlsson M, Thorn H, Stralfors P. Cholesterol depletion disrupts caveolae and insulin receptor signaling for metabolic control via insulin receptor substrate-1, but not for mitogen-activated protein kinase control. J Biol Chem 2001; 276:9670-9678.
40. Lu F, Ogawa R, Nguyen DT, Chen B, Guo D, Helm DL, Zhan Q, Murphy GF, Orgill DP. Microdeformation of three-dimensional cultured fibroblastsinduces gene expression and morphological changes. Ann Plast Surg 2011; 66:296-300.
41. Sims-Lucas S, Cusack B, Eswarakumar VP, Zhang J, Wang F, Bates CM. Independent roles of Fgfr2 and Frs2alpha in ureteric epithelium. Development 2011; 138:1275-1280.
42. Boardman PE, Sanz-Ezquerro J, Overton IM, Burt DW, Bosch E, Fong WT, Tickle C, Brown WR, Wilson SA, Hubbard SJ. A comprehensive collection of chicken cDNAs. Curr Biol 2002; 12:1965-1969.
43. Lisanti MP, Scherer PE, Vidugiriene J, Tang Z, Hermanowski-Vosatka A, Tu YH, Cook RF, Sargiacomo M. Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J Cell Biol 1994; 126:111-126