Identification of the amniotic fluid insulin-like growth factor binding protein-1 phosphorylation sites and propensity to proteolysis of the isoforms

FEBS Journal

Volumn 276, Issue 20, 2009, Pages 6033-6046

  Dolcini, Lorenzo ^a   Sala, Alberto ^a   Campagnoli, Monica ^a   Labò, Sara ^a   Valli, Maurizia ^a   Visai, Livia ^a   Minchiotti, Lorenzo ^a   Monaco, Hugo L ^b   Galliano, Monica ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

Author keywords

IGFBP; Insulin like growth factor binding protein 1; Mass spectrometry; Phosphorylation; Proteolysis

Indexed keywords

CHYMOTRYPSIN; GLUTAMIC ACID; ISOPROTEIN; PROLINE; PROTEINASE; SERINE; SOMATOMEDIN BINDING PROTEIN 1; THREONINE; TRYPSIN;

AMINO ACID SEQUENCE; AMNION FLUID; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HUMAN; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; STAPHYLOCOCCUS AUREUS; TANDEM MASS SPECTROMETRY;

AMNIOTIC FLUID; BINDING SITES; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, ION EXCHANGE; CHROMATOGRAPHY, LIQUID; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 1; PHOSPHORYLATION; PREGNANCY; PROTEIN ISOFORMS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TANDEM MASS SPECTROMETRY;

STAPHYLOCOCCUS AUREUS;

EID: 70349504395     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07318.x     Document Type: Article

References (46)

1. Jones JI Clemmons DR (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 16, 3 34.
2. Firth SM Baxter RC (2002) Cellular actions of the insulin growth factor binding proteins. Endocr Rev 23, 824 854.
3. Baxter RC (2000) Insulin-like growth factor (IGF-) binding proteins: interactions with IGFs and intrinsic bioactivities. Am J Physiol Endocrinol Metab 278, 967 976.
4. Kiepe D, Van der Paas A, Ciarmatori S, Ständker L, Schütt B, Hoeflich A, Hügel U, Oh J Tönshoff B (2008) Defined carboxy-terminal fragments of insulin-like growth factor binding protein-2 exert similar mitogenic activity on cultured rat growth plate chondrocytes as IGF-I. Endocrinology 149, 4901 4911.
5. Leu JI George DL (2007) Hepatic IGFBP1 is a prosurvival factor that binds to BAK, protects the liver from apoptosis, and antagonizes the proapoptotic actions of p53 at mitochondria. Genes Dev 21, 3095 3109.
6. Lang CH, Vary TC Frost RA (2003) Acute in vivo elevation of insulin-like growth factor (IGF) binding protein-1 decreases plasma free IGF-I and muscle protein synthesis. Endocrinology 144, 3922 3933.
7. Westwood M (1999) Role of insulin-like growth factor binding protein 1 in human pregnancy. Rev Reprod 4, 160 167.
8. Gibson JM, Aplin JD, White A Westwood M (2001) Regulation of IGF bioavailability in pregnancy. Mol Hum Reprod 7, 79 87.
9. Fowler DJ, Nicolaides KH Miell JP (2000) Insulin-like growth factor binding protein-1 (IGFBP-1): a multifunctional role in the human female reproductive tract. Hum Reprod 6, 495 504.
10. Tisi DK, Liu XJ, Wykes LJ, Skinner CD Koski KG (2005) Insulin-like growth factor II and binding proteins 1 and 3 from second trimester human amniotic fluid are associated with infant birth weight. J Nutr 135, 1667 1672.
11. Irving JA Lala PK (1995) Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGF-beta, IGF-II, and IGFBP-1. Exp Cell Res 217, 419 427.
12. Jones JI, Gockerman A, Busby WH Jr., Wright G Clemmons DR (1993) Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha 5 beta 1 integrin by means of its Arg-Gly-Asp sequence. Proc Natl Acad Sci USA 90, 10553 10557.
13. Gockerman A, Prevette T, Jones JI Clemmons DR (1995) Insulin-like growth factor (IGF)-binding proteins inhibit the smooth muscle cell migration responses to IGF-I and IGF-II. Endocrinology 136, 4168 4173.
14. Gleeson LM, Chakraborty C, McKinnon T Lala PK (2001) Insulin-like growth factor-binding protein 1 stimulates human trophoblast migration by signaling through alpha 5 beta 1 integrin via mitogen-activated protein kinase pathway. J Clin Endocrinol Metab 86, 2484 2493.
15. Huang ST, Vo KC, Lyell DJ, Faessen GH, Tulac S, Tibshirani R, Giaccia AJ Giudice LC (2004) Developmental response to hypoxia. FASEB J 18, 1348 1365.
16. Kajimura S, Aida K Duan C (2005) Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proc Natl Acad Sci USA 102, 1240 1245.
17. Sitar T, Popowiicz GM, Siwanowicz I, Huber R Holak TA (2006) Structural basis for the inhibition of insulin-like growth factors by insulin-like growth factor-binding proteins. Proc Natl Acad Sci USA 103, 13028 13033.
18. Westwood M, Gibson J, Davies AJ, Young RJ White A (1994) The phosphorylation pattern of insulin-like growth factor-binding protein-1 in normal plasma is different from that in amniotic fluid and changes during pregnancy. J Clin Endocrinol Metab 79, 1735 1741.
19. Weber MM, Spöttl G, Gössl C Engelhardt D (1999) Characterization of human insulin-like growth factor-binding proteins by two-dimensional polyacrylamide gel electrophoresis and Western ligand blot analysis. J Clin Endocrinol Metab 84, 1679 1684.
20. Gianazza E, Wait R, Begum S, Eberini I, Campagnoli M, Labò S Galliano M (2007) Mapping the 5-50 fraction of human amniotic fluid by 2-DE and ESI-MS. Proteomics Clin Appl 1, 167 175.
21. Jones JI, D'Ercole JA, Camacho-Hubner C Clemmons DR (1991) Phosphorylation of insulin-like growth factor (IGF)-binding protein 1 in cell culture and in vivo: effects on affinity for IGF-I. Proc Natl Acad Sci USA 88, 7481 7485.
22. Jones JI, Busby WH Jr., Wright G, Smith CE, Kimack NM Clemmons DR (1993) Identification of the sites of phosphorylation in insulin-like growth factor binding protein-1. Regulation of its affinity by phosphorylation of serine 101. J Biol Chem 268, 1125 1131.
23. Seferovic MD, Ali R, Kamei H, Liu S, Khosravi JM, Nazarian S, Han VK, Duan C Gupta MB (2009) Hypoxia and leucine deprivation induce human insulin-like growth factor binding protein-1 hyperphosphorylation and increase its biological activity. Endocrinology 159, 220 231.
24. Nissum M, Abuhehab M, Sukop U, Khosravi JM, Wildgruber R, Eckerskorn C, Han VKM Gupta MB (2009) Functional and complementary phosphorylation state attributes of human insulin-like growth factor binding protein-1 (IGFBP-1) isoforms resolved by free flow electrophoresis. Mol Cell Proteomics 8, 1424 1435.
25. Bankowski E, Sobolewski K, Palka J Jaworski S (2004) Decreased expression of the insulin-like growth factor-I-binding protein-1 (IGFBP-1) phosphoisoform in pre-eclamptic Wharton's jelly and its role in the regulation of collagen biosynthesis. Clin Chem Lab Med 42, 175 181.
26. Loukovaara M, Leinonen P, Teramo K, Nurminen E, Andersson S Rutanen EM (2005) Effect of maternal diabetes on phosphorylation of insulin-like growth factor binding protein-1 in cord serum. Diabet Med 22, 434 439.
27. Coppock HA, White A, Aplin JD Westwood M (2004) Matrix metalloprotease-3 and -9 proteolyze insulin-like growth factor-binding protein-1. Biol Reprod 71, 438 443.
28. Brandt K, Wang J, Lundell K, Ståhlberg M, Horn HV, Ehrenborg E, Hall K, Jörnvall H Lewitt M (2009) IGFBP-1 protease activity and IGFBP-1 fragments in a patient with multiple myeloma. Growth Horm IGF Res doi :.
29. Rechsteiner M Rogers SW (1996) PEST sequences and regulation by proteolysis. Trends Biochem Sci 21, 267 271.
30. Sala A, Capaldi S, Campagnoli M, Faggion B, Labò S, Perduca M, Romano A, Carrizo ME, Valli M, Visai L et al. (2005) Structure and properties of the C-terminal domain of insulin-like growth factor-binding protein-1 isolated from human amniotic fluid. J Biol Chem 280, 29812 29819.
31. Blom N, Gammeltoft S Brunak S (1999) Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294, 1351 1362.
32. Gibson BW Cohen P (1990) Liquid secondary ion mass spectrometry of phosphorylated and sulfated peptides and proteins. Methods Enzymol 193, 480 501.
33. Kim J, Camp DG II. Smith RD (2004) Improved detection of multi-phosphorylated peptides in the presence of phosphoric acid in liquid chromatography/mass spectrometry. J Mass Spectrom 39, 208 215.
34. Salih E (2005) Phosphoproteomics by mass spectrometry and classical protein chemistry approaches. Mass Spectrom Rev 24, 828 846.
35. Frost RA Tseng L (1991) Insulin-like growth factor-binding protein-1 is phosphorylated by cultured human endometrial stromal cells and multiple protein kinases in vitro. J Biol Chem 266, 18082 18088. (Pubitemid 21908050)
36. Temporini C, Dolcini L, Abee A, Calleri E, Galliano M, Caccialanza G Massolini G (2008) Development of an integrated chromatographic system for on-line digestion and characterization of phosphorylated proteins. J Chromatogr A 1183, 65 75.
37. Kabir-Salmani M, Shimizu Y, Sakai K Iwashita M (2005) Posttranslational modifications of decidual IGFBP-1 by steroid hormones in vitro. Mol Hum Reprod 11, 667 671.
38. Irwin JC, Fuentes LD, Dsupin BA Giudice LC (1993) Insulin-like growth factor regulation of human endometrial stromal cell function: coordinate effects on insulin-like growth factor binding protein-1, cell proliferation and prolactin secretion. Regul Pept 48, 165 177.
39. Bunn CR Fowlkes JR (2003) Insulin-like growth factor binding protein proteolysis. Trends Endocrinol Metab 14, 176 181.
40. Nakamura M, Miyamoto S, Maeda H, Ishii G, Hasebe T, Chiba T, Asaka M Ochiai A (2005) Matrix metalloproteinase-7 degrades all insulin-like growth factor binding proteins and facilitates insulin-like growth factor bioavailability. Biochem Biophys Res Commun 333, 1011 1016.
41. Binoux M, Lalou C, Lassarre C Segovia B (1994) Regulation of IGF bioavailability by IGFBP proteases. In The insulin-like growth factors and their regulatory proteins (Baxter RC, Gluckman PD Rosenfeld RG eds pp. 217 226. Elsevier Science, Amsterdam.
42. Graham ME, Kilby DM, Firth SM, Robinson PJ Baxter RC (2007) The in vivo phosphorylation and glycosylation of human insulin-like growth factor binding protein-5. Mol Cell Proteomics 6, 1392 1405.
43. Hoech WG Mukku VR (1994) Identification of the major sites of phosphorylation in IGF binding protein-3. J Cell Biochem 56, 262 273.
44. Zhang Z Marshall AG (1998) A universal algorithm for fast and automated charge state deconvolution of electrospray mass-to-charge ratio spectra. J Am Soc Mass Spectrom 9, 225 233.
45. Clauser KR, Baker PR Burlingame AL (1999) Role of accurate mass measurement (±10 ppm) in protein identification strategies employing MS or MS/MS and database searching. Anal Chem 71, 2871 2882.
46. Morodomi T, Ogata Y, Sasaguri Y, Morimatsu M Nagase H (1992) Purification and characterization of matrix metalloproteinase 9 from U937 monocytic leukaemia and HT1080 fibrosarcoma cells. Biochem J 285, 603 611.