Functional evolution of IGF2:IGF2R domain 11 binding generates novel structural interactions and a specific IGF2 antagonist

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 20, 2016, Pages E2766-E2775

  Frago, Susana ^a   Nicholls, Ryan D ^b   Strickland, Madeleine ^b   Hughes, Jennifer ^a   Williams, Christopher ^b   Garner, Lee ^a   Surakhy, Mirvat ^a   Maclean, Rory ^a   Rezgui, Dellel ^a   Prince, Stuart N ^a   Zaccheo, Oliver J ^a   Ebner, Daniel ^c   Sanegre, Sabina ^a   Yu, Sheng ^d   Buffa, Francesca M ^d   Crump, Matthew P ^b   Bassim Hassan, Andrew ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Binding kinetics; Biological therapy; Growth factor receptor; Insulin like growth factor 2; Protein evolution

Indexed keywords

FC FUSION PROTEIN; HYBRID PROTEIN; PROTEIN INHIBITOR; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR; UNCLASSIFIED DRUG; IGF2 PROTEIN, HUMAN; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; ENZYME MECHANISM; GENE MUTATION; IN VIVO STUDY; MOLECULAR EVOLUTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; RIGIDITY; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; SURFACE PROPERTY; YEAST; ADULT; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DIRECTED MOLECULAR EVOLUTION; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; PICHIA; PROTEIN DOMAIN; TUMOR CELL LINE; X RAY CRYSTALLOGRAPHY;

ADULT; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CELL LINE, TUMOR; CRYSTALLOGRAPHY, X-RAY; DIRECTED MOLECULAR EVOLUTION; HUMANS; INSULIN-LIKE GROWTH FACTOR II; MODELS, MOLECULAR; PICHIA; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTOR, IGF TYPE 2;

EID: 84969786305     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1513023113     Document Type: Article

References (59)

1. Harms MJ, Thornton JW (2013) Evolutionary biochemistry: Revealing the historical and physical causes of protein properties. Nat Rev Genet 14(8):559-571.
2. Williams C, et al. (2012) An exon splice enhancer primes IGF2:IGF2R binding site structure and function evolution. Science 338(6111):1209-1213.
3. Ghosh P, Dahms NM, Kornfeld S (2003) Mannose 6-phosphate receptors: New twists in the tale. Nat Rev Mol Cell Biol 4(3):202-212.
4. Linnell J, Groeger G, Hassan AB (2001) 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(26):23986-23991.
5. Morgan DO, et al. (1987) Insulin-like growth factor II receptor as a multifunctional binding protein. Nature 329(6137):301-307.
6. Wilkins JF, Haig D (2003) What good is genomic imprinting: The function of parentspecific gene expression. Nat Rev Genet 4(5):359-368.
7. Hughes J, Frago S, Bühnemann C, Carter EJ, Hassan AB (2013) Maternal transmission of a humanised Igf2r allele results in an Igf2 dependent hypomorphic and non-viable growth phenotype. PLoS One 8(2):e57270.
8. Lau MM, et al. (1994) Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev 8(24):2953-2963.
9. Wang ZQ, Fung MR, Barlow DP, Wagner EF (1994) Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature 372(6505):464-467.
10. Wylie AA, et al. (2003) Tissue-specific inactivation of murine M6P/IGF2R. Am J Pathol 162(1):321-328.
11. De Souza AT, Hankins GR, Washington MK, Orton TC, Jirtle RL (1995) M6P/IGF2R gene is mutated in human hepatocellular carcinomas with loss of heterozygosity. Nat Genet 11(4):447-449.
12. Hankins GR, et al. (1996) M6P/IGF2 receptor: A candidate breast tumor suppressor gene. Oncogene 12(9):2003-2009.
13. Harper J, et al. (2006) Soluble IGF2 receptor rescues Apc(Min/+) intestinal adenoma progression induced by Igf2 loss of imprinting. Cancer Res 66(4):1940-1948.
14. Prince SN, Foulstone EJ, Zaccheo OJ, Williams C, Hassan AB (2007) 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(2):607-617.
15. Surinya KH, et al. (2008) An investigation of the ligand binding properties and negative cooperativity of soluble insulin-like growth factor receptors. J Biol Chem 283(9): 5355-5363.
16. Delaine C, et al. (2007) 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(26):18886-18894.
17. Bach LA, Headey SJ, Norton RS (2005) IGF-binding proteins: The pieces are falling into place. Trends Endocrinol Metab 16(5):228-234.
18. Greenall SA, et al. (2013) Biochemical characterization of individual human glycosylated proinsulin-like growth factor (IGF)-II and big-IGF-II isoforms associated with cancer. J Biol Chem 288(1):59-68.
19. Zaina S, Squire S (1998) 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(44):28610-28616.
20. Yee D (2012) Insulin-like growth factor receptor inhibitors: Baby or the bathwater? J Natl Cancer Inst 104(13):975-981.
21. Brown J, et al. (2008) Structure and functional analysis of the IGF-II/IGF2R interaction. EMBO J 27(1):265-276.
22. Zaccheo OJ, et al. (2006) 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(2):403-421.
23. Canfield WM, Kornfeld S (1989) The chicken liver cation-independent mannose 6-phosphate receptor lacks the high affinity binding site for insulin-like growth factor II. J Biol Chem 264(13):7100-7103.
24. Clairmont KB, Czech MP (1989) Chicken and Xenopus mannose 6-phosphate receptors fail to bind insulin-like growth factor II. J Biol Chem 264(28):16390-16392.
25. Yandell CA, Dunbar AJ, Wheldrake JF, Upton Z (1999) The kangaroo cationindependent mannose 6-phosphate receptor binds insulin-like growth factor II with low affinity. J Biol Chem 274(38):27076-27082.
26. Bloom JD, Arnold FH (2009) In the light of directed evolution: Pathways of adaptive protein evolution. Proc Natl Acad Sci USA 106(Suppl 1):9995-10000.
27. Levin KB, et al. (2009) Following evolutionary paths to protein-protein interactions with high affinity and selectivity. Nat Struct Mol Biol 16(10):1049-1055.
28. Yuen CM, Liu DR (2007) Dissecting protein structure and function using directed evolution. Nat Methods 4(12):995-997.
29. Mergler M, Wolf K, Zimmermann M (2004) Development of a bisphenol A-adsorbing yeast by surface display of the Kluyveromyces yellow enzyme on Pichia pastoris. Appl Microbiol Biotechnol 63(4):418-421.
30. Williams C, et al. (2007) Structural insights into the interaction of insulin-like growth factor 2 with IGF2R domain 11. Structure 15(9):1065-1078.
31. Tinoco I, Sauer K, Wang JC (1978) Physical Chemistry: Prinicples and Applications in Biological Sciences (Prentice-Hall, Englewood Cliffs, NJ).
32. Dougherty DA (2007) Cation-pi interactions involving aromatic amino acids. J Nutr 137(6, Suppl 1):1504S-1508S, discussion 1516S-1517S.
33. Gallivan JP, Dougherty DA (1999) Cation-pi interactions in structural biology. Proc Natl Acad Sci USA 96(17):9459-9464.
34. Duguay SJ, et al. (1998) Post-translational processing of the insulin-like growth factor-2 precursor. Analysis of O-glycosylation and endoproteolysis. J Biol Chem 273(29): 18443-18451.
35. Bühnemann C, et al. (2014) Quantification of the heterogeneity of prognostic cellular biomarkers in Ewing sarcoma using automated image and random survival forest analysis. PLoS One 9(9):e107105.
36. Kastritis PL, Rodrigues JP, Folkers GE, Boelens R, Bonvin AM (2014) Proteins feel more than they see: Fine-tuning of binding affinity by properties of the non-interacting surface. J Mol Biol 426(14):2632-2652.
37. Škrlec K, Štrukelj B, Berlec A (2015) Non-immunoglobulin scaffolds: A focus on their targets. Trends Biotechnol 33(7):408-418.
38. Harms MJ, Thornton JW (2014) Historical contingency and its biophysical basis in glucocorticoid receptor evolution. Nature 512(7513):203-207.
39. Brouwer-Visser J, Huang GS (2015) IGF2 signaling and regulation in cancer. Cytokine Growth Factor Rev 26(3):371-377.
40. Chess A (2012) Mechanisms and consequences of widespread random monoallelic expression. Nat Rev Genet 13(6):421-428.
41. Gaudet F, et al. (2003) Induction of tumors in mice by genomic hypomethylation. Science 300(5618):489-492.
42. Lui JC, Baron J (2013) Evidence that Igf2 down-regulation in postnatal tissues and upregulation in malignancies is driven by transcription factor E2f3. Proc Natl Acad Sci USA 110(15):6181-6186.
43. Miyamoto S, et al. (2007) Matrix metalloproteinase-7 triggers the matricrine action of insulin-like growth factor-II via proteinase activity on insulin-like growth factor binding protein 2 in the extracellular matrix. Cancer Sci 98(5):685-691.
44. Seshagiri S, et al. (2012) Recurrent R-spondin fusions in colon cancer. Nature 488(7413):660-664.
45. Sun Y, et al. (2006) IGF2 is critical for tumorigenesis by synovial sarcoma oncoprotein SYT-SSX1. Oncogene 25(7):1042-1052.
46. Vidal SJ, et al. (2015) A targetable GATA2-IGF2 axis confers aggressiveness in lethal prostate cancer. Cancer Cell 27(2):223-239.
47. Yee D (2015) A tale of two receptors: Insulin and insulin-like growth factor signaling in cancer. Clin Cancer Res 21(4):667-669.
48. Haluska P, et al. (2014) Phase I dose-escalation study of MEDI-573, a bispecific, antiligand monoclonal antibody against IGFI and IGFII, in patients with advanced solid tumors. Clin Cancer Res 20(18):4747-4757.
49. Mireuta M, Birman E, Barmash M, Pollak M (2014) Quantification of binding of IGF-1 to BI 836845, a candidate therapeutic antibody against IGF-1 and IGF-2, and effects of this antibody on IGF-1:IGFBP-3 complexes in vitro and in male C57BL/6 mice. Endocrinology 155(3):703-715.
50. Gao J, et al. (2011) Dual IGF-I/II-neutralizing antibody MEDI-573 potently inhibits IGF signaling and tumor growth. Cancer Res 71(3):1029-1040.
51. Chen W, Feng Y, Zhao Q, Zhu Z, Dimitrov DS (2012) Human monoclonal antibodies targeting nonoverlapping epitopes on insulin-like growth factor II as a novel type of candidate cancer therapeutics. Mol Cancer Ther 11(7):1400-1410.
52. Dransfield DT, et al. (2010) A human monoclonal antibody against insulin-like growth factor-II blocks the growth of human hepatocellular carcinoma cell lines in vitro and in vivo. Mol Cancer Ther 9(6):1809-1819.
53. Forsten KE, Lauffenburger DA (1992) Interrupting autocrine ligand-receptor binding: Comparison between receptor blockers and ligand decoys. Biophys J 63(3):857-861.
54. Isoyama S, et al. (2015) Basal expression of insulin-like growth factor 1 receptor determines intrinsic resistance of cancer cells to a phosphatidylinositol 3-kinase inhibitor ZSTK474. Cancer Sci 106(2):171-178.
55. Flanigan SA, et al. (2013) Overcoming IGF1R/IR resistance through inhibition of MEK signaling in colorectal cancer models. Clin Cancer Res 19(22):6219-6229.
56. Guix M, et al. (2008) Acquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteins. J Clin Invest 118(7):2609-2619.
57. Fukuda I, et al. (2006) Clinical features of insulin-like growth factor-II producing nonislet-cell tumor hypoglycemia. Growth Horm IGF Res 16(4):211-216.
58. Rikhof B, et al. (2009) Insulin-like growth factors and insulin-like growth factorbinding proteins in relation to disease status and incidence of hypoglycaemia in patients with a gastrointestinal stromal tumour. Ann Oncol 20(9):1582-1588.
59. Wu S, Letchworth GJ (2004) High efficiency transformation by electroporation of Pichia pastoris pretreated with lithium acetate and dithiothreitol. Biotechniques 36(1):152-154.