Analysis of site-specific histidine protonation in human prolactin

Biochemistry

Volumn 47, Issue 33, 2008, Pages 8638-8647

  Tettamanzi, M Cristina ^a   Keeler, Camille ^a   Meshack, Syrus ^a   Hodsdon, Michael E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL CULTURE; CHLORINE COMPOUNDS; DISSOCIATION; ENZYME ACTIVITY; EQUILIBRIUM CONSTANTS; FLOW INTERACTIONS; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTONATION; RATE CONSTANTS;

BIOPHYSICAL MECHANISM; COOPERATIVITY; CYTOKINE; DISSOCIATION RATE CONSTANT; EQUILIBRIUM DISSOCIATION CONSTANTS; EXTRACELLULAR DOMAINS; FUNCTIONAL PROPERTIES; HISTIDINE RESIDUES; INTERACTION BETWEEN RESIDUES; NMR SPECTROS COPY; PH-DEPENDENT; POTENTIAL MODELING; PROTEIN SURFACES; PROTON BINDINGS; PROTONATION REACTIONS; SITE-DIRECTED MUTAGENESIS; SITE-SPECIFIC;

BINDING SITES;

HISTIDINE; PROLACTIN;

ARTICLE; BINDING SITE; BIOLOGICAL MONITORING; BIOPHYSICAL EQUIPMENT; DENATURATION; DISSOCIATION CONSTANT; EQUILIBRIUM CONSTANT; HUMAN; MOLECULAR DYNAMICS; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON TRANSPORT; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS; STATISTICAL ANALYSIS; THERMODYNAMICS;

BINDING SITES; GENE EXPRESSION REGULATION; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; PROLACTIN; PROTEIN CONFORMATION; PROTEIN FOLDING; RECOMBINANT PROTEINS;

EID: 49749128750     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800444t     Document Type: Article

References (52)

1. Goffin, V., Binart, N., Touraine, P., and Kelly, P. A. (2002) Prolactin: The new biology of an old hormone. Annu. Rev. Physiol. 64, 47-67.
2. Wells, J. A., and de Vos, A. M. (1996) Hematopoietic receptor complexes. Annu. Rev. Biochem. 65, 609-634.
3. Ben-Jonathan, N., Mershon, J. L., Allen, D. L., and Steinmetz, R. W. (1996) Extrapituitary prolactin: Distribution, regulation, functions, and clinical aspects. Endocr. Rev. 17, 639-669.
4. Ben-Jonathan, N., Liby, K., McFarland, M., and Zinger, M. (2002) Prolactin as an autocrine/paracrine growth factor in human cancer. Trends Endocrinol. Metab. 13, 245-250.
5. Clevenger, C. V., Furth, P. A., Hankinson, S. E., and Schuler, L. A. (2003) The role of prolactin in mammary carcinoma. Endocr. Rev. 24, 1-27.
6. Goffin, V., Touraine, P., Pichard, C., Bernichtein, S., and Kelly, P. A. (1999) Should prolactin be reconsidered as a therapeutic target in human breast cancer? Mol. Cell. Endocrinol. 151, 79-87.
7. Leav, I., Merk, F. B., Lee, K. F., Loda, M., Mandoki, M., McNeal, J. E., and Ho, S. M. (1999) Prolactin receptor expression in the developing human prostate and in hyperplastic, dysplastic, and neoplastic lesions. Am. J. Pathol. 154, 863-870.
8. Xu, X., Kreye, E., Kuo, C. B., and Walker, A. M. (2001) A molecular mimic of phosphorylated prolactin markedly reduced tumor incidence and size when DU145 human prostate cancer cells were grown in nude mice. Cancer Res. 61, 6098-6104.
9. Bernichtein, S., Kinet, S., Jeay, S., Llovera, M., Madern, D., Martial, J. A., Kelly, P. A., and Goffin, V. (2001) S179D-human PRL, a pseudophosphorylated human PRL analog, is an agonist and not an antagonist. Endocrinology 142, 3950-3963.
10. Xu, X., Wu, W., Williams, V., Khong, A., Chen, Y. H., Deng, C., and Walker, A. M. (2003) Opposite effects of unmodified prolactin and a molecular mimic of phosphorylated prolactin on morphology and the expression of prostate specific genes in the normal rat prostate. Prostate 54, 25-33.
11. Ueda, E., Ozerdem, U., Chen, Y. H., Yao, M., Huang, K. T., Sun, H., Martins-Green, M., Bartolini, P., and Walker, A. M. (2006) A molecular mimic demonstrates that phosphorylated human prolactin is a potent anti-angiogenic hormone. Endocr.-Relat. Cancer 13, 95-111.
12. Maciejewski, P. M., Peterson, F. C., Anderson, P. J., and Brooks, C. L. (1995) Mutation of serine 90 to glutamic acid mimics phosphorylation of bovine prolactin. J. Biol. Chem. 270, 27661-27665.
13. Schenck, E. J., Canfield, J. M., and Brooks, C. L. (2003) Functional relationship of serine 90 phosphorylation and the surrounding putative salt bridge in bovine prolactin. Mol. Cell. Endocrinol. 204, 117-125.
14. Aranda, J., Rivera, J. C., Jeziorski, M. C., Riesgo-Escovar, J., Nava, G., Lopez-Barrera, F., Quiroz-Mercado, H., Berger, P., Martinez de la Escalera, G., and Clapp, C. (2005) Prolactins are natural inhibitors of angiogenesis in the retina. Invest. Ophthalmol. Visual Sci. 46, 2947-2953.
15. Piwnica, D., Touraine, P., Struman, I., Tabruyn, S., Bolbach, G., Clapp, C., Martial, J. A., Kelly, P. A., and Goffin, V. (2004) Cathepsin D processes human prolactin into multiple 16K-like N-terminal fragments: Study of their antiangiogenic properties and physiological relevance. Mol. Endocrinol. 18, 2522-2542.
16. Corbacho, A. M., Nava, G., Eiserich, J. P., Noris, G., Macotela, Y., Struman, I., Martinez de la Escalera, G., Freeman, B. A., and Clapp, C. (2000) Proteolytic cleavage confers nitric oxide synthase inducing activity upon prolactin. J. Biol. Chem. 275, 13183-13186.
17. Clapp, C., Martial, J. A., Guzman, R. C., Rentierdelrue, F., and Weiner, R. I. (1993) The 16-Kilodalton N-Terminal Fragment of Human Prolactin Is a Potent Inhibitor of Angiogenesis. Endocrinology 133, 1292-1299.
18. Keeler, C., Jablonski, E. M., Albert, Y. B., Taylor, B. D., Myszka, D. G., Clevenger, C. V., and Hodsdon, M. E. (2007) The kinetics of binding human prolactin, but not growth hormone, to the prolactin receptor vary over a physiologic pH range. Biochemistry 46, 2398-2410.
19. Dannies, P. S. (2002) Mechanisms for storage of prolactin and growth hormone in secretory granules. Mol. Genet. Metab. 76, 6-13.
20. 2+, and pH. Endocrinology 143, 1302-1309.
21. Hilfiker-Kleiner, D., Kaminski, K., Podewski, E., Bonda, T., Schaefer, A., Sliwa, K., Forster, O., Quint, A., Landmesser, U., Doerries, C., Luchtefeld, M., Poli, V., Schneider, M. D., Balligand, J. L., Desjardins, F., Ansari, A., Struman, I., Nguyen, N. Q., Zschemisch, N. H., Klein, G., Heusch, G., Schulz, R., Hilfiker, A., and Drexler, H. (2007) A cathepsin D-cleaved 16 kDa form of prolactin mediates postpartum cardiomyopathy. Cell 128, 589-600.
22. Leinwand, L. A. (2007) Molecular events underlying pregnancy-induced cardiomyopathy. Cell 128, 437-438.
23. Piwnica, D., Fernandez, I., Binart, N., Touraine, P., Kelly, P. A., and Goffin, V. (2006) A new mechanism for prolactin processing into 16K PRL by secreted cathepsin D. Mol. Endocrinol. 20, 3263-3278.
24. Clapp, C., Gonzalez, C., Macotela, Y., Aranda, J., Rivera, J. C., Garcia, C., Guzman, J., Zamorano, M., Vega, C., Martin, C., Jeziorski, M. C., and Martinez de la Escalera, G. (2006) Vasoinhibins: A family of N-terminal prolactin fragments that inhibit angiogenesis and vascular function. Front. Horm. Res. 35, 64-73.
25. Lkhider, M., Castino, R., Bouguyon, E., Isidore, C., and Ollivier-Bousquet, M. (2004) Cathepsin D released by lactating rat mammary epithelial cells is involved in prolactin cleavage under physiological conditions. J. Cell Sci. 117, 5155-5164.
26. Gerweck, L. E. (2000) The pH difference between tumor and normal tissue offers a tumor specific target for the treatment of cancer. Drug Resist. Updates 3, 49-50.
27. Brooks, D. J., Fresco, J. R., Lesk, A. M., and Singh, M. (2002) Evolution of amino acid frequencies in proteins over deep time: Inferred order of introduction of amino acids into the genetic code. Mol. Biol. Evol. 19, 1645-1655.
28. Jomain, J. B., Tallet, E., Broutin, I., Hoos, S., van, A. J., Ducruix, A., Kelly, P. A., Kragelund, B. B., England, P., and Goffin, V. (2007) Structural and thermodynamical bases for the design of pure prolactin receptor antagonists. X-ray structure of Del1-9G129R-hPRL. J. Biol. Chem. 282, 33118-33131.
29. Teilum, K., Hoch, J. C., Goffin, V., Kinet, S., Martial, J. A., and Kragelund, B. B. (2005) Solution structure of human prolactin. J. Mol. Biol. 351, 810-823.
30. Keeler, C., Dannies, P. S., and Hodsdon, M. E. (2003) The tertiary structure and backbone dynamics of human prolactin. J. Mol. Biol. 328, 1105-1121.
31. 15N-amino acids. J. Biomol. NMR 8, 184-192.
32. 15N-alanine-labeling of bovine trypsin. Application to the study of trypsin-inhibitor complexes and trypsinogen activation by NMR spectroscopy. Biochemistry 40, 6275-6283.
33. Pelton, J. G., Torchia, D. A., Meadow, N. D., and Roseman, S. (1993) Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated IIIGlc, a signal-transducing protein from Escherichia coli, using two-dimensional heteronuclear NMR techniques. Protein Sci. 2, 543-558.
34. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) Nmrpipe: A Multidimensional Spectral Processing System Based on Unix Pipes. J. Biomol. NMR 6, 277-293.
35. Kneller, D. G., and Goddard, T. D. (1997) SPARKY, University of California, San Francisco.
36. Cavanagh, J. (1996)Referencing. In Protein NMR Spectroscopy: Principles and Practice, pp 175-176, Academic Press, San Diego.
37. Gill, S. J., Richey, B., Bishop, G., and Wyman, J. (1985) Generalized binding phenomena in an allosteric macromolecule. Biophys. Chem. 21, 1-14.
38. 15N NMR spectroscopy of hydrogen-bonding interactions in the active site of serine proteases: Evidence for a moving histidine mechanism. Biochemistry 25, 7751-7759.
39. 13C NMR spectroscopy: Application to apo calmodulin. J. Am. Chem. Soc. 129, 15805-15813.
40. Chivers, P. T., Prehoda, K. E., Volkman, B. F., Kim, B. M., Markley, J. L., and Raines, R. T. (1997) Microscopic pKa values of Escherichia coli thioredoxin. Biochemistry 36, 14985-14991.
41. Gao, G., DeRose, E. F., Kirby, T. W., and London, R. E. (2006) NMR determination of lysine pKa values in the Pol λ lyase domain: Mechanistic implications. Biochemistry 45, 1785-1794.
42. Joshi, M. D., Hedberg, A., and McIntosh, L. P. (1997) Complete measurement of the pKa values of the carboxyl and imidazole groups in Bacillus circulans xylanase. Protein Sci. 6, 2667-2670.
43. Kesvatera, T., Jonsson, B., Thulin, E., and Linse, S. (1996) Measurement and modelling of sequence-specific pKa values of lysine residues in calbindin D9k. J. Mol. Biol. 259, 828-839.
44. Khare, D., Alexander, P., Antosiewicz, J., Bryan, P., Gilson, M., and Orban, J. (1997) pKa measurements from nuclear magnetic resonance for the B1 and B2 immunoglobulin G-binding domains of protein G: Comparison with calculated values for nuclear magnetic resonance and X-ray structures. Biochemistry 36, 3580-3589.
45. Lindman, S., Linse, S., Mulder, F. A., and Andre, I. (2006) Electrostatic contributions to residue-specific protonation equilibria and proton binding capacitance for a small protein. Biochemistry 45, 13993-14002.
46. 13C-NMR study of Bacillus circulans xylanase. Biochemistry 35, 9958-9966.
47. Oliveberg, M., Arcus, V. L., and Fersht, A. R. (1995) pKa values of carboxyl groups in the native and denatured states of barnase: The pKa values of the denatured state are on average 0.4 units lower than those of model compounds. Biochemistry 34, 9424-9433.
48. Schubert, M., Poon, D. K., Wicki, J., Tarling, C. A., Kwan, E. M., Nielsen, J. E., Withers, S. G., and McIntosh, L. P. (2007) Probing electrostatic interactions along the reaction pathway of a glycoside hydrolase: Histidine characterization by NMR spectroscopy. Biochemistry 46, 7383-7395.
49. Tan, Y. J., Oliveberg, M., Davis, B., and Fersht, A. R. (1995) Perturbed pKa-values in the denatured states of proteins. J. Mol. Biol. 254, 980-992.
50. Somers, W., Ultsch, M., DeVos, A. M., and Kossiakoff, A. A. (1994) The X-Ray Structure of a Growth-Hormone Prolactin Receptor Complex. Nature 372, 478-481.
51. Goffin, V., Shiverick, K. T., Kelly, P. A., and Martial, J. A. (1996) Sequence-function relationships within the expanding family of prolactin, growth hormone, placental lactogen, and related proteins in mammals. Endocr. Rev. 17, 385-410.
52. Richards, F. M. (1997) Protein stability: Still an unsolved problem. Cell. Mol. Life Sci. 53, 790-802.