Chapter 25 Interactions of IGF-II with the IGF2R/Cation-Independent Mannose-6-Phosphate Receptor. Mechanism and Biological Outcomes

Vitamins and Hormones

Volumn 80, Issue C, 2009, Pages 699-719

  Brown, J ^a   Jones, E Y ^a   Forbes, B E ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Binding surface; Cancer; Insulin like growth factor; Mannose 6 phosphate; Receptor; Structure

Indexed keywords

SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR;

CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; PROTEIN BINDING; PROTEIN CONFORMATION; REVIEW;

HUMANS; INSULIN-LIKE GROWTH FACTOR II; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTOR, IGF TYPE 2;

EID: 61349170301     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0083-6729(08)00625-0     Document Type: Review

References (86)

1. Bach L.A., Hsieh S., Sakano K., Fujiwara H., Perdue J.F., and Rechler M.M. Binding of mutants of human insulin-like growth factor II to insulin-like growth factor binding proteins 1-6. J. Biol. Chem. 268 (1993) 9246-9254
2. Blanchard F., Raher S., Duplomb L., Vusio P., Pitard V., Taupin J.L., Moreau J.F., Hoflack B., Minvielle S., Jacques Y., and Godard A. The mannose 6-phosphate/insulin-like growth factor II receptor is a nanomolar affinity receptor for glycosylated human leukemia inhibitory factor. J. Biol. Chem. 273 (1998) 20886-20893
3. Blanchard F., Duplomb L., Raher S., Vusio P., Hoflack B., Jacques Y., and Godard A. Mannose 6-phosphate/insulin-like growth factor II receptor mediates internalization and degradation of leukemia inhibitory factor but not signal transduction. J. Biol. Chem. 274 (1999) 24685-24693
4. Braulke T. Type-2 IGF receptor: A multi-ligand binding protein. Horm. Metab. Res. 31 (1999) 242-246
5. Brown J., Esnouf R.M., Jones M.A., Linnell J., Harlos K., Hassan A.B., and Jones E.Y. Structure of a functional IGF2R fragment determined from the anomalous scattering of sulfur. EMBO J. 21 (2002) 1054-1062
6. Brown J., Delaine C., Zaccheo O.J., Siebold C., Gilbert R.J., van Boxel G., Denley A., Wallace J.C., Hassan A.B., Forbes B.E., and Jones E.Y. Structure and functional analysis of the IGF-II/IGF2R interaction. EMBO J. 27 (2008) 265-276
7. Byrd J.C., Devi G.R., de Souza A.T., Jirtle R.L., and MacDonald R.G. Disruption of ligand binding to the insulin-like growth factor II/mannose 6-phosphate receptor by cancer-associated missense mutations. J. Biol. Chem. 274 (1999) 24408-24416
8. Byrd J.C., Park J.H., Schaffer B.S., Garmroudi F., and MacDonald R.G. Dimerization of the insulin-like growth factor II/mannose 6-phosphate receptor. J. Biol. Chem. 275 (2000) 18647-18656
9. Clairmont K.B., and Czech M.P. Chicken and Xenopus mannose 6-phosphate receptors fail to bind insulin-like growth factor II. J. Biol. Chem. 264 (1989) 16390-16392
10. Clairmont K.B., and Czech M.P. Extracellular release as the major degradative pathway of the insulin-like growth factor II/mannose 6-phosphate receptor. J. Biol. Chem. 266 (1991) 12131-12134
11. Costello M., Baxter R.C., and Scott C.D. Regulation of soluble insulin-like growth factor II/mannose 6-phosphate receptor in human serum: Measurement by enzyme-linked immunosorbent assay. J. Clin. Endocrinol. Metab. 84 (1999) 611-617
12. Dahms N.M., and Hancock M.K. P-type lectins. Biochim. Biophys. Acta 19 (2002) 2-3
13. Dahms N.M., Rose P.A., Molkentin J.D., Zhang Y., and Brzycki M.A. The bovine mannose 6-phosphate/insulin-like growth factor II receptor. The role of arginine residues in mannose 6-phosphate binding. J. Biol. Chem. 268 (1993) 5457-5463
14. Dahms N.M., Wick D.A., and Brzycki-Wessell M.A. The bovine mannose 6-phosphate/insulin-like growth factor II receptor. Localization of the insulin-like growth factor II binding site to domains 5-11. J. Biol. Chem. 269 (1994) 3802-3809
15. De Souza A.T., Hankins G.R., Washington M.K., Orton T.C., and Jirtle R.L. M6P/IGF2R gene is mutated in human hepatocellular carcinomas with loss of heterozygosity. Nat. Genet. 11 (1995) 447-449
16. Delaine C., Alvino C.L., McNeil K.A., Mulhern T.D., Gauguin L., De Meyts P., Jones E.Y., Brown J., Wallace J.C., and Forbes B.E. A novel binding site for the human insulin-like growth factor-II (IGF-II)/mannose 6-phosphate receptor on IGF-II. J. Biol. Chem. 282 (2007) 18886-18894
17. Denley A., Wallace J.C., Cosgrove L.J., and Forbes B.E. The insulin receptor isoform exon 11- (IR-A) in cancer and other diseases: A review. Horm. Metab. Res. 35 (2003) 778-785
18. Dennis P.A., and Rifkin D.B. Cellular activation of latent transforming growth factor beta requires binding to the cation-independent mannose 6-phosphate/insulin-like growth factor type II receptor. Proc. Natl. Acad. Sci. USA 88 (1991) 580-584
19. Devi G.R., Byrd J.C., Slentz D.H., and MacDonald R.G. An insulin-like growth factor II (IGF-II) affinity-enhancing domain localized within extracytoplasmic repeat 13 of the IGF-II/mannose 6-phosphate receptor. Mol. Endocrinol. 12 (1998) 1661-1672
20. Devi G.R., De Souza A.T., Byrd J.C., Jirtle R.L., and MacDonald R.G. Altered ligand binding by insulin-like growth factor II/mannose 6-phosphate receptors bearing missense mutations in human cancers. Cancer Res. 59 (1999) 4314-4319
21. Forbes B.E., McNeil K.A., Scott C.D., Surinya K.H., Cosgrove L.J., and Wallace J.C. Contribution of residues A54 and L55 of the human insulin-like growth factor-II (IGF-II) A domain to Type 2 IGF receptor binding specificity. Growth Factors 19 (2001) 163-173
22. Gallicchio M.A., Kaun C., Wojta J., Binder B., and Bach L.A. Urokinase type plasminogen activator receptor is involved in insulin-like growth factor-induced migration of rhabdomyosarcoma cells in vitro. J. Cell. Physiol. 197 (2003) 131-138
23. Garmroudi F., Devi G., Slentz D.H., Schaffer B.S., and MacDonald R.G. Truncated forms of the insulin-like growth factor II (IGF-II)/mannose 6-phosphate receptor encompassing the IGF-II binding site: Characterization of a point mutation that abolishes IGF-II binding. Mol. Endocrinol. 10 (1996) 642-651
24. Ghosh P., Dahms N.M., and Kornfeld S. Mannose 6-phosphate receptors: New twists in the tale. Nat. Rev. Mol. Cell Biol. 4 (2003) 202-212
25. Gicquel C., and Le Bouc Y. Hormonal regulation of fetal growth. Horm. Res. 3 (2006) 28-33
26. Godar S., Horejsi V., Weidle U.H., Binder B.R., Hansmann C., and Stockinger H. M6P/IGFII-receptor complexes urokinase receptor and plasminogen for activation of transforming growth factor-beta1. Eur. J. Immunol. 29 (1999) 1004-1013
27. Hancock M.K., Haskins D.J., Sun G., and Dahms N.M. Identification of residues essential for carbohydrate recognition by the insulin-like growth factor II/mannose 6-phosphate receptor. J. Biol. Chem. 277 (2002) 11255-11264
28. Hawkes C., and Kar S. The insulin-like growth factor-II/mannose-6-phosphate receptor: Structure, distribution and function in the central nervous system. Brain Res. Brain Res. Rev. 44 (2004) 117-140
29. Hebert E. Mannose-6-phosphate/insulin-like growth factor II receptor expression and tumor development. Biosci. Rep. 26 (2006) 7-17
30. Hu C.K., McCall S., Madden J., Huang H., Clough R., Jirtle R.L., and Anscher M.S. Loss of heterozygosity of M6P/IGF2R gene is an early event in the development of prostate cancer. Prostate Cancer Prostatic Dis. 9 (2006) 62-67
31. Huang Z., Wen Y., Shandilya R., Marks J.R., Berchuck A., and Murphy S.K. High throughput detection of M6P/IGF2R intronic hypermethylation and LOH in ovarian cancer. Nucleic Acids Res. 34 (2006) 555-563
32. Ikezu T., Okamoto T., Giambarella U., Yokota T., and Nishimoto I. In vivo coupling of insulin-like growth factor II/mannose 6-phosphate receptor to heteromeric G proteins. Distinct roles of cytoplasmic domains and signal sequestration by the receptor. J. Biol. Chem. 270 (1995) 29224-29228
33. Jadot M., Canfield W.M., Gregory W., and Kornfeld S. Characterization of the signal for rapid internalization of the bovine mannose 6-phosphate/insulin-like growth factor-II receptor. J. Biol. Chem. 267 (1992) 11069-11077
34. Jang H.S., Kang K.M., Choi B.O., Chai G.Y., Hong S.C., Ha W.S., and Jirtle R.L. Clinical significance of loss of heterozygosity for M6P/IGF2R in patients with primary hepatocellular carcinoma. World J. Gastroenterol. 14 (2008) 1394-1398
35. Kaku K., Osada H., Seki K., and Sekiya S. Insulin-like growth factor 2 (IGF2) and IGF2 receptor gene variants are associated with fetal growth. Acta Paediatr. 96 (2007) 363-367
36. Kang J.X., Li Y., and Leaf A. Mannose-6-phosphate/insulin-like growth factor-II receptor is a receptor for retinoic acid. Proc. Natl. Acad. Sci. USA 94 (1997) 13671-13676
37. Kang J.X., Bell J., Leaf A., Beard R.L., and Chandraratna R.A. Retinoic acid alters the intracellular trafficking of the mannose-6-phosphate/insulin-like growth factor II receptor and lysosomal enzymes. Proc. Natl. Acad. Sci. USA 95 (1998) 13687-13691
38. Kiess W., Thomas C.L., Greenstein L.A., Lee L., Sklar M.M., Rechler M.M., Sahagian G.G., and Nissley S.P. Insulin-like growth factor-II (IGF-II) inhibits both the cellular uptake of beta-galactosidase and the binding of beta-galactosidase to purified IGF-II/mannose 6-phosphate receptor. J. Biol. Chem. 264 (1989) 4710-4714
39. Killian J.K., Byrd J.C., Jirtle J.V., Munday B.L., Stoskopf M.K., MacDonald R.G., and Jirtle R.L. M6P/IGF2R imprinting evolution in mammals. Mol. Cell 5 (2000) 707-716
40. Killian J.K., Oka Y., Jang H.S., Fu X., Waterland R.A., Sohda T., Sakaguchi S., and Jirtle R.L. Mannose 6-phosphate/insulin-like growth factor 2 receptor (M6P/IGF2R) variants in American and Japanese populations. Hum. Mutat. 18 (2001) 25-31
41. Korner C., Nurnberg B., Uhde M., and Braulke T. Mannose 6-phosphate/insulin-like growth factor II receptor fails to interact with G-proteins. Analysis of mutant cytoplasmic receptor domains. J. Biol. Chem. 270 (1995) 287-295
42. Koster A., von Figura K., and Pohlmann R. Mistargeting of lysosomal enzymes in M(r) 46,000 mannose 6-phosphate receptor-deficient mice is compensated by carbohydrate-specific endocytotic receptors. Eur. J. Biochem. 224 (1994) 685-689
43. Kreiling J.L., Byrd J.C., Deisz R.J., Mizukami I.F., Todd III R.F., and MacDonald R.G. Binding of urokinase-type plasminogen activator receptor (uPAR) to the mannose 6-phosphate/insulin-like growth factor II receptor: Contrasting interactions of full-length and soluble forms of uPAR. J. Biol. Chem. 278 (2003) 20628-20637
44. Kreiling J.L., Byrd J.C., and MacDonald R.G. Domain interactions of the mannose 6-phosphate/insulin-like growth factor II receptor. J. Biol. Chem. 280 (2005) 21067-21077
45. Lau M.M., Stewart C.E., Liu Z., Bhatt H., Rotwein P., and Stewart C.L. Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev. 8 (1994) 2953-2963
46. Lee J.S., Weiss J., Martin J.L., and Scott C.D. Increased expression of the mannose 6-phosphate/insulin-like growth factor-II receptor in breast cancer cells alters tumorigenic properties in vitro and in vivo. Int. J. Cancer 107 (2003) 564-570
47. Leivonen S.K., and Kahari V.M. Transforming growth factor-beta signaling in cancer invasion and metastasis. Int. J. Cancer 121 (2007) 2119-2124
48. Leksa V., Godar S., Cebecauer M., Hilgert I., Breuss J., Weidle U.H., Horejsi V., Binder B.R., and Stockinger H. The N terminus of mannose 6-phosphate/insulin-like growth factor 2 receptor in regulation of fibrinolysis and cell migration. J. Biol. Chem. 277 (2002) 40575-40582
49. Leksa V., Godar S., Schiller H.B., Fuertbauer E., Muhammad A., Slezakova K., Horejsi V., Steinlein P., Weidle U.H., Binder B.R., and Stockinger H. TGF-beta-induced apoptosis in endothelial cells mediated by M6P/IGFII-R and mini-plasminogen. J. Cell Sci. 118 (2005) 4577-4586
50. Linnell J., Groeger G., and Hassan A.B. Real time kinetics of insulin-like growth factor II (IGF-II) interaction with the IGF-II/mannose 6-phosphate receptor: The effects of domain 13 and pH. J. Biol. Chem. 276 (2001) 23986-23991
51. Lobel P., Dahms N.M., and Kornfeld S. Cloning and sequence analysis of the cation-independent mannose 6-phosphate receptor. J. Biol. Chem. 263 (1988) 2563-2570
52. Ludwig T., Eggenschwiler J., Fisher P., D'Ercole A.J., Davenport M.L., and Efstratiadis A. Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev. Biol. 177 (1996) 517-535
53. MacDonald R.G. Mannose-6-phosphate enhances cross-linking efficiency between insulin-like growth factor-II (IGF-II) and IGF-II/mannose-6-phosphate receptors in membranes. Endocrinology 128 (1991) 413-421
54. McKinnon T., Chakraborty C., Gleeson L.M., Chidiac P., and Lala P.K. Stimulation of human extravillous trophoblast migration by IGF-II is mediated by IGF type 2 receptor involving inhibitory G protein(s) and phosphorylation of MAPK. J. Clin. Endocrinol. Metab. 86 (2001) 3665-3674
55. Minniti C.P., Kohn E.C., Grubb J.H., Sly W.S., Oh Y., Muller H.L., Rosenfeld R.G., and Helman L.J. The insulin-like growth factor II (IGF-II)/mannose 6-phosphate receptor mediates IGF-II-induced motility in human rhabdomyosarcoma cells. J. Biol. Chem. 267 (1992) 9000-9004
56. Mohamed M.M., and Sloane B.F. Cysteine cathepsins: Multifunctional enzymes in cancer. Nat. Rev. Cancer 6 (2006) 764-775
57. Monk D., Arnaud P., Apostolidou S., Hills F.A., Kelsey G., Stanier P., Feil R., and Moore G.E. Limited evolutionary conservation of imprinting in the human placenta. Proc. Natl. Acad. Sci. USA 103 (2006) 6623-6628
58. Motyka B., Korbutt G., Pinkoski M.J., Heibein J.A., Caputo A., Hobman M., Barry M., Shostak I., Sawchuk T., Holmes C.F., Gauldie J., and Bleackley R.C. Mannose 6-phosphate/insulin-like growth factor II receptor is a death receptor for granzyme B during cytotoxic T cell-induced apoptosis. Cell 103 (2000) 491-500
59. Nykjaer A., Christensen E.I., Vorum H., Hager H., Petersen C.M., Roigaard H., Min H.Y., Vilhardt F., Moller L.B., Kornfeld S., and Gliemann J. Mannose 6-phosphate/insulin-like growth factor-II receptor targets the urokinase receptor to lysosomes via a novel binding interaction. J. Cell Biol. 141 (1998) 815-828
60. O'Gorman D.B., Weiss J., Hettiaratchi A., Firth S.M., and Scott C.D. Insulin-like growth factor-II/mannose 6-phosphate receptor overexpression reduces growth of choriocarcinoma cells in vitro and in vivo. Endocrinology 143 (2002) 4287-4294
61. Olson L.J., Zhang J., Dahms N.M., and Kim J.J. Twists and turns of the cation-dependent mannose 6-phosphate receptor. Ligand-bound versus ligand-free receptor. J. Biol. Chem. 277 (2002) 10156-10161
62. Olson L.J., Dahms N.M., and Kim J.J. The N-terminal carbohydrate recognition site of the cation-independent mannose 6-phosphate receptor. J. Biol. Chem. 279 (2004) 34000-34009
63. Olson L.J., Yammani R.D., Dahms N.M., and Kim J.J. Structure of uPAR, plasminogen, and sugar-binding sites of the 300 kDa mannose 6-phosphate receptor. EMBO J. 23 (2004) 2019-2028
64. Petry C.J., Ong K.K., Wingate D.L., Brown J., Scott C.D., Jones E.Y., Pembrey M.E., and Dunger D.B. Genetic variation in the type 2 insulin-like growth factor receptor gene and disparity in childhood height. Growth Horm. IGF Res. 15 (2005) 363-368
65. Prince S.N., Foulstone E.J., Zaccheo O.J., Williams C., and Hassan A.B. Functional evaluation of novel soluble insulin-like growth factor (IGF)-II-specific ligand traps based on modified domain 11 of the human IGF2 receptor. Mol. Cancer Ther. 6 (2007) 607-617
66. Reddy S.T., Chai W., Childs R.A., Page J.D., Feizi T., and Dahms N.M. Identification of a low affinity mannose 6-phosphate-binding site in domain 5 of the cation-independent mannose 6-phosphate receptor. J. Biol. Chem. 279 (2004) 38658-38667
67. Roberts D.L., Weix D.J., Dahms N.M., and Kim J.J. Molecular basis of lysosomal enzyme recognition: Three-dimensional structure of the cation-dependent mannose 6-phosphate receptor. Cell 93 (1998) 639-648
68. Roche P., Brown J., Denley A., Forbes B.E., Wallace J.C., Jones E.Y., and Esnouf R.M. Computational model for the IGF-II/IGF2r complex that is predictive of mutational and surface plasmon resonance data. Proteins 64 (2006) 758-768
69. Sakano K., Enjoh T., Numata F., Fujiwara H., Marumoto Y., Higashihashi N., Sato Y., Perdue J.F., and Fujita-Yamaguchi Y. The design, expression, and characterization of human insulin-like growth factor II (IGF-II) mutants specific for either the IGF-II/cation-independent mannose 6-phosphate receptor or IGF-I receptor. J. Biol. Chem. 266 (1991) 20626-20635
70. Savage S.A., Woodson K., Walk E., Modi W., Liao J., Douglass C., Hoover R.N., and Chanock S.J. Analysis of genes critical for growth regulation identifies insulin-like growth factor 2 receptor variations with possible functional significance as risk factors for osteosarcoma. Cancer Epidemiol. Biomarkers Prev. 16 (2007) 1667-1674
71. Schmidt B., Kiecke-Siemsen C., Waheed A., Braulke T., and von Figura K. Localization of the insulin-like growth factor II binding site to amino acids 1508-1566 in repeat 11 of the mannose 6-phosphate/insulin-like growth factor II receptor. J. Biol. Chem. 270 (1995) 14975-14982
72. Scott C.D., and Firth S.M. The role of the M6P/IGF-II receptor in cancer: Tumor suppression or garbage disposal?. Horm. Metab. Res. 36 (2004) 261-271
73. Sitar T., Popowicz G.M., Siwanowicz I., Huber R., and Holak T.A. Structural basis for the inhibition of insulin-like growth factors by insulin-like growth factor-binding proteins. Proc. Natl. Acad. Sci. USA 103 (2006) 13028-13033
74. Souza R.F., Appel R., Yin J., Wang S., Smolinski K.N., Abraham J.M., Zou T.T., Shi Y.Q., Lei J., Cottrell J., Cymes K., Biden K., et al. Microsatellite instability in the insulin-like growth factor II receptor gene in gastrointestinal tumours. Nat. Genet. 14 (1996) 255-257
75. Tong P.Y., Tollefsen S.E., and Kornfeld S. The cation-independent mannose 6-phosphate receptor binds insulin-like growth factor II. J. Biol. Chem. 263 (1988) 2585-2588
76. Wang Z.Q., Fung M.R., Barlow D.P., and Wagner E.F. Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature 372 (1994) 464-467
77. Westlund B., Dahms N.M., and Kornfeld S. The bovine mannose 6-phosphate/insulin-like growth factor II receptor. Localization of mannose 6-phosphate binding sites to domains 1-3 and 7-11 of the extracytoplasmic region. J. Biol. Chem. 266 (1991) 23233-23239
78. Williams C., Rezgui D., Prince S.N., Zaccheo O.J., Foulstone E.J., Forbes B.E., Norton R.S., Crosby J., Hassan A.B., and Crump M.P. Structural insights into the interaction of insulin-like growth factor 2 with IGF2R domain 11. Structure 15 (2007) 1065-1078
79. Wylie A.A., Murphy S.K., Orton T.C., and Jirtle R.L. Novel imprinted DLK1/GTL2 domain on human chromosome 14 contains motifs that mimic those implicated in IGF2/H19 regulation. Genome Res. 10 (2000) 1711-1718
80. Xu Y., Papageorgiou A., and Polychronakos C. Developmental regulation of the soluble form of insulin-like growth factor-II/mannose 6-phosphate receptor in human serum and amniotic fluid. J. Clin. Endocrinol. Metab. 83 (1998) 437-442
81. Yandell C.A., Dunbar A.J., Wheldrake J.F., and Upton Z. The kangaroo cation-independent mannose 6-phosphate receptor binds insulin-like growth factor II with low affinity. J. Biol. Chem. 274 (1999) 27076-27082
82. Yandell C.A., Francis G.L., Wheldrake J.F., and Upton Z. Kangaroo IGF-II is structurally and functionally similar to the human. J. Endocrinol. 161 (1999) 445-453
83. York S.J., Arneson L.S., Gregory W.T., Dahms N.M., and Kornfeld S. The rate of internalization of the mannose 6-phosphate/insulin-like growth factor II receptor is enhanced by multivalent ligand binding. J. Biol. Chem. 274 (1999) 1164-1171
84. Young L.E., Fernandes K., McEvoy T.G., Butterwith S.C., Gutierrez C.G., Carolan C., Broadbent P.J., Robinson J.J., Wilmut I., and Sinclair K.D. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27 (2001) 153-154
85. Zaccheo O.J., Prince S.N., Miller D.M., Williams C., Kemp C.F., Brown J., Jones E.Y., Catto L.E., Crump M.P., and Hassan A.B. Kinetics of insulin-like growth factor II (IGF-II) interaction with domain 11 of the human IGF-II/mannose 6-phosphate receptor: Function of CD and AB loop solvent-exposed residues. J. Mol. Biol. 359 (2006) 403-421
86. Zaina S., and Squire S. The soluble type 2 insulin-like growth factor (IGF-II) receptor reduces organ size by IGF-II-mediated and IGF-II-independent mechanisms. J. Biol. Chem. 273 (1998) 28610-28616