Riding shotgun: A dual role for the epidermal growth factor-Cripto/FRL-1/ Cryptic protein cripto in nodal trafficking

Traffic

Volumn 10, Issue 7, 2009, Pages 783-791

  Constam, Daniel B ^a  

^a EPFL   (Switzerland)

Author keywords

Clathrin independent endocytosis; Degradation; Flotillin; Multivesicular endosomes; Precursor processing; Proprotein convertases; Signal duration; Smad anchor for receptor activation; Transforming growth factor b

Indexed keywords

ACTIVIN RECEPTOR 1; ACTIVIN RECEPTOR 2; EPIDERMAL GROWTH FACTOR; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; PROTEIN CRIPTO; PROTEIN NODAL; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG;

CELL MEMBRANE TRANSPORT; CELL SPECIFICITY; CELL SURFACE; CONCENTRATION RESPONSE; EMBRYO DEVELOPMENT; ENDOCYTOSIS; ENDOSOME; HUMAN; INTERNALIZATION; LYSOSOME; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; XENOPUS; ZEBRA FISH;

ANIMALS; ENDOCYTOSIS; ENDOSOMES; EPIDERMAL GROWTH FACTOR; HOMEODOMAIN PROTEINS; HUMANS; LYSOSOMES; MEMBRANE PROTEINS; NODAL PROTEIN; PROTEIN PRECURSORS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSCRIPTION FACTORS; XENOPUS PROTEINS; ZEBRAFISH PROTEINS;

EID: 67249117804     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.00874.x     Document Type: Review

References (83)

1. Conlon FL, Lyons KM, Takaesu N, Barth KS, Kispert A, Herrmann B, Robertson EJ. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development. 1994; 120: 1919-28.
2. Zhou X, Sasaki H, Lowe L, Hogan BLM, Kuehn MR. Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature 1993; 361: 543-547.
3. Shen MM. Nodal signaling: Developmental roles and regulation. Development 2007 Mar; 134: 1023-1034.
4. Camus A, Perea-Gomez A, Moreau A, Collignon J. Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo. Dev Biol 2006; 295: 743-755.
5. Mesnard D, Guzman-Ayala M, Constam DB. Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 2006; 133: 2497-2505.
6. Brennan J, Lu CC, Norris DP, Rodriguez TA, Beddington RS, Robertson EJ. Nodal signalling in the epiblast patterns the early mouse embryo. Nature 2001; 411: 965-969.
7. James D, Levine AJ, Besser D, Hemmati-Brivanlou A. TGFβ/activin/ nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 2005; 132: 1273-1282.
8. Ogawa K, Saito A, Matsui H, Suzuki H, Ohtsuka S, Shimosato D, Morishita Y, Watabe T, Niwa H, Miyazono K. Activin-Nodal signaling is involved in propagation of mouse embryonic stem cells. J Cell Sci. 2007 Jan 1; 120 (Pt 1): 55-65.
9. Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, Vallier L. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature. 2007 Jul 12; 448 (7150): 191-5.
10. Ang SL, Constam DB. A gene network establishing polarity in the early mouse embryo. Semin Cell Dev Biol 2004; 15: 555-561.
11. Shiratori H, Hamada H. The left-right axis in the mouse: From origin to morphology. Development 2006; 133: 2095-2104.
12. Gritsman K, Zhang J, Cheng S, Heckscher E, Talbot WS, Schier AF. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 1999; 97: 121-132.
13. Shen MM, Schier AF. The EGF-CFC gene family in vertebrate development. Trends Genet 2000; 16: 303-309.
14. Beck S, Le Good JA, Guzman M, Haim NB, Roy K, Beermann F, Constam DB. Extraembryonic proteases regulate Nodal signalling during gastrulation. Nat Cell Biol. 2002; 4: 981-5.
15. Eimon PM, Harland RM. Effects of heterodimerization and proteolytic processing on Derriere and Nodal activity: Implications for mesoderm induction in Xenopus. Development 2002; 129: 3089-4103.
16. BenHaim N, Lu C, Pescatore L, Mesnard D, Bischofberger M, Naef F, Robertson EJ, Guzman M, Constam DB. The Nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev Cell. 2006; 11: 1-11.
17. Hagos EG, Dougan ST. Time-dependent patterning of the mesoderm and endoderm by Nodal signals in zebrafish. BMC Dev Biol 2007; 7: 22.
18. Jullien J, Gurdon J. Morphogen gradient interpretation by a regulated trafficking step during ligand-receptor transduction. Genes Dev 2005; 19: 2682-2694.
19. Le Good JA, Joubin K, Giraldez AJ, Ben-Haim N, Beck S, Chen Y, Schier AF, Constam DB. Nodal stability determines signaling range. Curr Biol. 2005; 15: 1-20.
20. van der Goot FG, Gruenberg J. Intra-endosomal membrane traffic. Trends Cell Biol 2006; 16: 514-521.
21. Woodman PG, Futter CE. Multivesicular bodies: Co-ordinated progression to maturity. Curr Opin Cell Biol 2008; 20: 408-414.
22. Malerod L, Stuffers S, Brech A, Stenmark H. Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 2007; 8: 1617-1629.
23. Progida C, Malerod L, Stuffers S, Brech A, Bucci C, Stenmark H. RILP is required for the proper morphology and function of late endosomes. J Cell Sci 2007; 120: 3729-3737.
24. Pons V, Luyet PP, Morel E, Abrami L, van der Goot FG, Parton RG, Gruenberg J. Hrs and SNX3 Functions in Sorting and Membrane Invagination within Multivesicular Bodies. PLoS Biol. 2008 Sep 2; 6 (9): E214.
25. Theos AC, Truschel ST, Tenza D, Hurbain I, Harper DC, Berson JF, Thomas PC, Raposo G, Marks MS. A lumenal domain-dependent pathway for sorting to intralumenal vesicles of multivesicular endosomes involved in organelle morphogenesis. Dev Cell. 2006 Mar; 10 (3): 343-54.
26. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007; 8: 603-612.
27. Lang DM, Lommel S, Jung M, Ankerhold R, Petrausch B, Laessing U, Wiechers MF, Plattner H, Stuermer CA. Identification of reggie-1 and reggie-2 as plasmamembrane-associated proteins which cocluster with activated GPI-anchored cell adhesion molecules in non-caveolar micropatches in neurons. J Neurobiol. 1998 Dec; 37 (4): 502-23.
28. Stuermer CA, Lang DM, Kirsch F, Wiechers M, Deininger SO, Plattner H. Glycosylphosphatidyl inositol-anchored proteins and fyn kinase assemble in noncaveolar plasma membrane microdomains defined by reggie-1 and -2. Mol Biol Cell 2001;12: 3031-3045.
29. Glebov OO, Bright NA, Nichols BJ. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 2006; 8: 46-54.
30. Payne CK, Jones SA, Chen C, Zhuang X. Internalization and trafficking of cell surface proteoglycans and proteoglycan-binding ligands. Traffic 2007; 8: 389-401.
31. Morrow IC, Rea S, Martin S, Prior IA, Prohaska R, Hancock JF, James DE, Parton RG. Flotillin-1/reggie-2 traffics to surface raft domains via a novel golgi-independent pathway. Identification of a novel membrane targeting domain and a role for palmitoylation. J Biol Chem. 2002 Dec 13; 277 (50): 48834-41.
32. Neumann-Giesen C, Falkenbach B, Beicht P, Claasen S, Luers G, Stuermer CA, Herzog V, Tikkanen R. Membrane and raft association of reggie-1/ flotillin-2: Role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem J. 2004 Mar 1; 378 (Pt 2): 509-18.
33. Frick M, Bright NA, Riento K, Bray A, Merrified C, Nichols BJ. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol 2007; 17: 1151-1156.
34. Katanaev VL, Solis GP, Hausmann G, Buestorf S, Katanayeva N, Schrock Y, Stuermer CA, Basler K. Reggie-1/flotillin-2 promotes secretion of the long-range signalling forms of Wingless and Hedgehog in Drosophila. Embo J. 2008 Feb 6; 27 (3): 509-21.
35. Sotgia F, Razani B, Bonuccelli G, Schubert W, Battista M, Lee H, Capozza F, Schubert AL, Minetti C, Buckley JT, Lisanti MP. Intracellular retention of glycosylphosphatidyl inositol-linked proteins in caveolin-deficient cells. Mol Cell Biol. 2002 Jun; 22 (11): 3905-26.
36. Blouin CM, Le Lay S, Lasnier F, Dugail I, Hajduch E. Regulated association of caveolins to lipid droplets during differentiation of 3T3-L1 adipocytes. Biochem Biophys Res Commun 2008; 376: 331-335.
37. Frank PG, Pavlides S, Cheung MW, Daumer K, Lisanti MP. Role of caveolin-1 in the regulation of lipoprotein metabolism. Am J Physiol Cell Physiol 2008; 295: C242-C248.
38. Massague J, Kelly B. Internalization of transforming growth factor-beta and its receptor in BALB/c 3T3 fibroblasts. J Cell Physiol 1986; 128: 216-222.
39. Anders RA, Arline SL, Dore JJ, Leof EB. Distinct endocytic responses of heteromeric and homomeric transforming growth factor beta receptors. Mol Biol Cell 1997; 8: 2133-2143.
40. Garamszegi N, Dore JJ Jr., Penheiter SG, Edens M, Yao D, Leof EB. Transforming growth factor beta receptor signaling and endocytosis are linked through a COOH terminal activation motif in the type I receptor. Mol Biol Cell 2001; 12: 2881-2893.
41. Anders RA, Dore JJ Jr., Arline SL, Garamszegi N, Leof EB. Differential requirement for type I and type II transforming growth factor beta receptor kinase activity in ligand-mediated receptor endocytosis. J Biol Chem 1998; 273: 23118-23125.
42. Chen W, Kirkbride KC, How T, Nelson CD, Mo J, Frederick JP, Wang X-F, Lefkowitz RJ, Blobe GC. β-Arrestin 2 Mediates Endocytosis of Type III TGF-{beta} Receptor and Down-Regulation of Its Signaling. Science. 2003 September 5, 2003; 301 (5638): 1394-7.
43. Tsukazaki T, Chiang TA, Davison AF, Attisano L, Wrana JL. SARA, a FYVE domain protein that recruits Smad2 to the TGF beta receptor. Cell 1998; 95: 779-791.
44. Hayes S, Chawla A, Corvera S. TGF beta receptor internalization into EEA1-enriched early endosomes: Role in signaling to Smad2. J Cell Biol 2002; 158: 1239-1249.
45. Penheiter SG, Mitchell H, Garamszegi N, Edens M, Dore JJ Jr., Leof EB. Internalization-dependent and -independent requirements for transforming growth factor beta receptor signaling via the Smad pathway. Mol Cell Biol 2002; 22: 4750-4759.
46. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 2003; 5: 410-421.
47. Razani B, Zhang XL, Bitzer M, von Gersdorff G, Bottinger EP, Lisanti MP. Caveolin-1 regulates transforming growth factor (TGF)-beta/SMAD signaling through an interaction with the TGF-beta type I receptor. J Biol Chem 2001; 276: 6727-6738.
48. Le Saux CJ, Teeters K, Miyasato SK, Hoffmann PR, Bollt O, Douet V, Shohet RV, Broide DH, Tam EK. Down-regulation of caveolin-1, an inhibitor of transforming growth factor-beta signaling, in acute allergen-induced airway remodeling. J Biol Chem. 2008 Feb 29; 283 (9): 5760-8.
49. Vilar JM, Jansen R, Sander C. Signal processing in the TGF-beta superfamily ligand-receptor network. PLoS Comput Biol 2006; 2: E3.
50. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 2008; 15: 209-219.
51. Yamamoto H, Sakane H, Michiue T, Kikuchi A. Wnt3a and Dkk1 regulate distinct internalization pathways of LRP6 to tune the activation of beta-catenin signaling. Dev Cell 2008; 15: 37-48.
52. Panopoulou E, Gillooly DJ, Wrana JL, Zerial M, Stenmark H, Murphy C, Fotsis T. Early endosomal regulation of Smad-dependent signaling in endothelial cells. J Biol Chem. 2002; 277 (20): 18046-52.
53. Zhou Y, Scolavino S, Funderburk SF, Ficociello LF, Zhang X, Klibanski A. Receptor internalization-independent activation of Smad2 in activin signaling. Mol Endocrinol 2004; 18: 1818-1826.
54. Lu Z, Murray JT, Luo W, Li H, Wu X, Xu H, Backer JM, Chen YG. Transforming growth factor beta activates Smad2 in the absence of receptor endocytosis. J Biol Chem. 2002; 277 (33): 29363-8.
55. Yeo C-Y, Whitman M. Nodal Signals to Smads through Cripto-Dependent and Cripto-Independent Mechanisms. Mol Cell 2001; 7: 949-957.
56. Reissmann E, Jornvall H, Blokzijl A, Andersson O, Chang C, Minchiotti G, Persico MG, Ibanez CF, Brivanlou AH. The orphan receptor ALK7 and the Activin receptor ALK4 mediate signaling by Nodal proteins during vertebrate development. Genes Dev. 2001;15 (15): 2010-22.
57. Yan YT, Liu JJ, Luo Y, Chaosu E, Haltiwanger RS, Abate-Shen C, Shen MM. Dual roles of Cripto as a ligand and coreceptor in the nodal signaling pathway. Mol Cell Biol. 2002; 22 (13): 4439-49.
58. Blanchet M-H, Le Good JA, Mesnard D, Oorschot V, Baflast S, Minchiotti G, Klumperman J, Constam DB. Cripto recruits Furin and PACE4 and controls Nodal trafficking during proteolytic maturation. EMBO J. 2008; 27: 2580-91.
59. Chen C, Shen MM. Two modes by which Lefty proteins inhibit nodal signaling. Curr Biol 2004; 14: 618-624.
60. Blanchet M-H, Le Good JA, Oorschot V, Baflast S, Minchiotti G, Klumperman J, Constam DB. Cripto localizes Nodal at the limiting membrane of early endosomes. Sci Signal. 2008; 1 (45): Ra13.
61. Hikasa H, Sokol SY. The involvement of Frodo in TCF-dependent signaling and neural tissue development. Development 2004; 131: 4725-4734.
62. Waxman JS. Regulation of the early expression patterns of the zebrafish Dishevelled-interacting proteins Dapper1 and Dapper2. Dev Dyn 2005; 233: 194-200.
63. Waxman JS, Hocking AM, Stoick CL, Moon RT. Zebrafish Dapper1 and Dapper2 play distinct roles in Wnt-mediated developmental processes. Development 2004; 131: 5909-5921.
64. Zhang L, Zhou H, Su Y, Sun Z, Zhang H, Zhang Y, Ning Y, Chen YG, Meng A. Zebrafish Dpr2 inhibits mesoderm induction by promoting degradation of nodal receptors. Science. 2004 Oct 1; 306 (5693): 114-7.
65. Zhang L, Gao X, Wen J, Ning Y, Chen YG. Dapper 1 antagonizes Wnt signaling by promoting dishevelled degradation. J Biol Chem 2006; 281: 8607-8612.
66. Meng F, Cheng X, Yang L, Hou N, Yang X, Meng A. Accelerated re-epithelialization in Dpr2-deficient mice is associated with enhanced response to TGF beta signaling. J Cell Sci 2008; 121: 2904-2912.
67. Piek E, Van Dinther M, Parks WT, Sallee JM, Bottinger EP, Roberts AB, Ten Dijke P. RLP, a novel Ras-like protein, is an immediate-early transforming growth factor-beta (TGF-beta) target gene that negatively regulates transcriptional activity induced by TGF-beta. Biochem J. 2004 Oct 1; 383 (Pt 1): 187-99.
68. Pezeron G, Lambert G, Dickmeis T, Strahle U, Rosa FM, Mourrain P. Rasl11b knock down in zebrafish suppresses one-eyed-pinhead mutant phenotype. PLoS ONE 2008; 3: E1434.
69. Choi SC, Kim GH, Lee SJ, Park E, Yeo CY, Han JK. Regulation of activin/ nodal signaling by Rap2-directed receptor trafficking. Dev Cell 2008; 15: 49-61.
70. Mitchell H, Choudhury A, Pagano RE, Leof EB. Ligand-dependent and -independent transforming growth factor-beta receptor recycling regulated by clathrin-mediated endocytosis and Rab11. Mol Biol Cell 2004; 15: 4166-4178.
71. Martello G, Zacchigna L, Inui M, Montagner M, Adorno M, Mamidi A, Morsut L, Soligo S, Tran U, Dupont S, Cordenonsi M, Wessely O, Piccolo S. MicroRNA control of Nodal signalling. Nature. 2007 Sep 13; 449 (7159): 183-8.
72. Dyson S, Gurdon JB. The interpretation of position in a morphogen gradient as revealed by occupancy of activin receptors. Cell 1998; 93: 557-568.
73. Bokel C, Schwabedissen A, Entchev E, Renaud O, Gonzalez-Gaitan M. SARA endosomes and the maintenance of Dpp signaling levels across mitosis. Science 2006; 314: 1135-1139.
74. Sharma P, Sabharanjak S, Mayor S. Endocytosis of lipid rafts: An identity crisis. Semin Cell Dev Biol 2002; 13: 205-214.
75. Naslavsky N, Weigert R, Donaldson JG. Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol Biol Cell 2003; 14: 417-431.
76. Naslavsky N, Weigert R, Donaldson JG. Characterization of a nonclathrin endocytic pathway: Membrane cargo and lipid requirements. Mol Biol Cell 2004; 15: 3542-3552.
77. Kalia M, Kumari S, Chadda R, Hill MM, Parton RG, Mayor S. Arf6-independent GPI-anchored protein-enriched early endosomal compartments fuse with sorting endosomes via a Rab5/ phosphatidylinositol-3′-kinase-dependent machinery. Mol Biol Cell 2006; 17: 3689-3704.
78. Fujimoto T. GPI-anchored proteins, glycosphingolipids, and sphingomyelin are sequestered to caveolae only after crosslinking. J Histochem Cytochem 1996; 44: 929-941.
79. Fivaz M, Vilbois F, Thurnheer S, Pasquali C, Abrami L, Bickel PE, Parton RG, van der Goot FG. Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J. 2002; 21 (15): 3989-4000.
80. Sharma P, Varma R, Sarasij RC, Ira, Gousset K, Krishnamoorthy G, Rao M, Mayor S. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell. 2004 Feb 20; 116 (4): 577-89.
81. Legler DF, Doucey MA, Schneider P, Chapatte L, Bender FC, Bron C. Differential insertion of GPI-anchored GFPs into lipid rafts of live cells. FASEB J 2005; 19: 73-75.
82. Sabharanjak S, Sharma P, Parton RG, Mayor S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2002; 2: 411-423.
83. Kumari S, Mayor S. ARF1 is directly involved in dynamin-independent endocytosis. Nat Cell Biol 2008; 10: 30-41.