Hydrogen Exchange Mass Spectrometry of Related Proteins with Divergent Sequences: A Comparative Study of HIV-1 Nef Allelic Variants

Journal of the American Society for Mass Spectrometry

Volumn 27, Issue 6, 2016, Pages 1048-1061

  Wales, Thomas E ^a   Poe, Jerrod A ^b   Emert Sedlak, Lori ^b   Morgan, Christopher R ^a,c   Smithgall, Thomas E ^b   Engen, John R ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c GENZYME CORPORATION   (United States)

Author keywords

Hck SH3; Protein conformation; Sequence conservation

Indexed keywords

DEUTERIUM; DISEASES; HYDROGEN; MASS SPECTROMETRY;

BIOLOGICAL FUNCTIONS; COMPARATIVE STUDIES; HCK SH3; HYDROGEN EXCHANGE; PROTEASE DIGESTION; PROTEIN CONFORMATION; SEQUENCE CONSERVATION; TERTIARY STRUCTURES;

PROTEINS;

ELI PROTEIN; G2E PROTEIN; HEMATOPOIETIC CELL KINASE; LTNP4 PROTEIN; NEF PROTEIN; NL4 3 PROTEIN; PROTEIN SH3; PROTEIN VARIANT; PROTEINASE; SF2 PROTEIN; UNCLASSIFIED DRUG; HYDROGEN; NEF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

AMINO ACID SEQUENCE; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; GENETIC VARIABILITY; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROGEN EXCHANGE MASS SPECTROMETRY; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; GENETICS; HUMAN; SRC HOMOLOGY DOMAIN;

AMINO ACID SEQUENCE; HIV-1; HUMANS; HYDROGEN; MASS SPECTROMETRY; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; PROTO-ONCOGENE PROTEINS C-HCK; SRC HOMOLOGY DOMAINS;

EID: 84971224753     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-016-1365-5     Document Type: Article

References (53)

1. Katta, V., Chait, B.T.: Conformational changes in proteins probed by hydrogen- exchange electrospray-ionization mass spectrometry. Rapid Commun. Mass Spectrom. 5, 214–217 (1991)
2. Wales, T.E., Engen, J.R.: Partial unfolding of diverse SH3 domains on a wide timescale. J. Mol. Biol. 357, 1592–1604 (2006)
3. Fang, J., Nevin, P., Kairys, V., Venclovas, C., Engen, J.R., Beuning, P.J.: Conformational analysis of processivity clamps in solution demonstrates that tertiary structure does not correlate with protein dynamics. Structure 22, 572–581 (2014)
4. Fackler, O.T., Baur, A.S.: Live and let die: Nef functions beyond HIV replication. Immunity 16, 493–497 (2002)
5. Greenway, A.L., Holloway, G., McPhee, D.A.: HIV-1 Nef: a critical factor in viral-induced pathogenesis. Adv. Pharmacol. 48, 299–343 (2000)
6. Joseph, A.M., Kumar, M., Mitra, D.: Nef: "necessary and enforcing factor" in HIV infection. Curr. HIV Res. 3, 87–94 (2005)
7. Cullen, B.R.: HIV-1 Nef protein: an invitation to a kill. Nat. Med. 5, 985–986 (1999)
8. Kestler, H.W.D., Ringler, D.J., Mori, K., Panicali, D.L., Sehgal, P.K., Daniel, M.D., Desrosiers, R.C.: Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65, 651–662 (1991)
9. Saksena, N.K., Wang, B., Dyer, W.B.: Biological and molecular mechanisms in progression and non-progression of HIV disease. AIDS Rev. 3, 133–144 (2001)
10. Rodes, B., Toro, C., Paxinos, E., Poveda, E., Martinez-Padial, M., Benito, J.M., Jimenez, V., Wrin, T., Bassani, S., Soriano, V.: Differences in disease progression in a cohort of long-term non-progressors after more than 16 years of HIV-1 infection. Aids 18, 1109–1116 (2004)
11. Crotti, A., Neri, F., Corti, D., Ghezzi, S., Heltai, S., Baur, A., Poli, G., Santagostino, E., Vicenzi, E.: Nef alleles from human immunodeficiency virus type 1-infected long-term nonprogressor hemophiliacs with or without late disease progression are defective in enhancing virus replication and CD4 down-regulation. J. Virol. 80, 10663–10674 (2006)
12. Tolstrup, M., Laursen, A.L., Gerstoft, J., Pedersen, F.S., Ostergaard, L., Duch, M.: Cysteine 138 mutation in HIV-1 Nef from patients with delayed disease progression. Sex. Health 3, 281–286 (2006)
13. Kirchhoff, F., Easterbrook, P.J., Douglas, N., Troop, M., Greenough, T.C., Weber, J., Carl, S., Sullivan, J.L., Daniels, R.S.: Sequence variations in human immunodeficiency virus type 1 Nef are associated with different stages of disease. J. Virol. 73, 5497–5508 (1999)
14. Carl, S., Greenough, T.C., Krumbiegel, M., Greenberg, M., Skowronski, J., Sullivan, J.L., Kirchhoff, F.: Modulation of different human immunodeficiency virus type 1 Nef functions during progression to AIDS. J. Virol. 75, 3657–3665 (2001)
15. Salvi, R., Garbuglia, A.R., Di Caro, A., Pulciani, S., Montella, F., Benedetto, A.: Grossly defective nef gene sequences in a human immunodeficiency virus type 1-seropositive long-term nonprogressor. J. Virol. 72, 3646–3657 (1998)
16. Deacon, N.J., Tsykin, A., Solomon, A., Smith, K., Ludford-Menting, M., Hooker, D.J., McPhee, D.A., Greenway, A.L., Ellett, A., Chatfield, C., Lawson, V.A., Crowe, S., Maerz, A., Sonza, S., Learmont, J., Sullivan, J.S., Cunningham, A., Dwyer, D., Dowton, D., Mills, J.: Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270, 988–991 (1995)
17. Hanna, Z., Kay, D.G., Rebai, N., Guimond, A., Jothy, S., Jolicoeur, P.: Nef harbors a major determinant of pathogenicity for an AIDS-like disease induced by HIV-1 in transgenic mice. Cell 95, 163–175 (1998)
18. Geyer, M., Fackler, O.T., Peterlin, B.M.: Structure–function relationships in HIV-1 Nef. EMBO Rep. 2, 580–585 (2001)
19. Kirchhoff, F., Schindler, M., Specht, A., Arhel, N., Munch, J.: Role of Nef in primate lentiviral immunopathogenesis. Cell. Mol. Life Sci. 65, 2621–2636 (2008)
20. Grzesiek, S., Bax, A., Clore, M., Gronenborn, A.M., Hu, J.-S., Kaufman, J., Palmer, I., Stahl, S.J., Wingfield, P.T.: The solution structure of HIV-1 Nef reveals an unexpected fold and permits delineation of the binding surface for the SH3 domain of Hck tyrosine protein kinase. Nat. Struct. Biol. 3, 340–345 (1996)
21. Lee, C.H., Saksela, K., Mirza, U.A., Chait, B.T., Kuriyan, J.: Crystal structure of the conserved core of HIV-1 Nef complexed with a Src family SH3 domain. Cell 85, 931–942 (1996)
22. Arold, S., Franken, P., Strub, M.P., Hoh, F., Benichou, S., Benarous, R., Dumas, C.: The crystal structure of HIV-1 Nef protein bound to the Fyn kinase SH3 domain suggests a role for this complex in altered T cell receptor signaling. Structure 5, 1361–1372 (1997)
23. Grzesiek, S., Bax, A., Hu, J.S., Kaufman, J., Palmer, I., Stahl, S.J., Tjandra, N., Wingfield, P.T.: Refined solution structure and backbone dynamics of HIV-1 Nef. Protein Sci. 6, 1248–1263 (1997)
24. Geyer, M., Munte, C.E., Schorr, J., Kellner, R., Kalbitzer, H.R.: Structure of the anchor-domain of myristoylated and non-myristoylated HIV-1 Nef protein. J. Mol. Biol. 289, 123–138 (1999)
25. Barnham, K.J., Monks, S.A., Hinds, M.G., Azad, A.A., Norton, R.S.: Solution structure of a polypeptide from the N terminus of the HIV protein Nef. Biochemistry 36, 5970–5980 (1997)
26. Geyer, M., Peterlin, B.M.: Domain assembly, surface accessibility, and sequence conservation in full length HIV-1 Nef. FEBS Lett. 496, 91–95 (2001)
27. Jia, X., Singh, R., Homann, S., Yang, H., Guatelli, J., Xiong, Y.: Structural basis of evasion of cellular adaptive immunity by HIV-1 Nef. Nat. Struct. Mol. Biol. 19, 701–706 (2012)
28. Ren, X., Park, S.Y., Bonifacino, J.S., Hurley, J.H.: How HIV-1 Nef hijacks the AP-2 clathrin adaptor to downregulate CD4. eLife 3, e01754 (2014)
29. Alvarado, J.J., Tarafdar, S., Yeh, J.I., Smithgall, T.E.: Interaction with the Src homology (SH3-SH2) region of the Src-family kinase Hck structures the HIV-1 Nef dimer for kinase activation and effector recruitment. J. Biol. Chem. 289, 28539–28553 (2014)
30. O'Neill, E., Kuo, L.S., Krisko, J.F., Tomchick, D.R., Garcia, J.V., Foster, J.L.: Dynamic evolution of the human immunodeficiency virus type 1 pathogenic factor. Nef. J. Virol. 80, 1311–1320 (2006)
31. Trible, R.P., Emert-Sedlak, L., Wales, T.E., Ayyavoo, V., Engen, J.R., Smithgall, T.E.: Allosteric loss-of-function mutations in HIV-1 Nef from a long-term non-progressor. J. Mol. Biol. 374, 121–129 (2007)
32. Wales, T.E., Engen, J.R.: Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom. Rev. 25, 158–170 (2006)
33. Narute, P.S., Smithgall, T.E.: Nef alleles from all major HIV-1 clades activate Src-family kinases and enhance HIV-1 replication in an inhibitor-sensitive manner. PLoS One 7, e32561 (2012)
34. Hochrein, J.M., Lerner, E.C., Schiavone, A.P., Smithgall, T.E., Engen, J.R.: An examination of dynamics crosstalk between SH2 and SH3 domains by hydrogen/deuterium exchange and mass spectrometry. Protein Sci. 15, 65–73 (2006)
35. Narute, P.S.: HIV-1 Nef-Src family kinase interaction: a novel target for the inhibition of HIV-1 pathogenesis. University of Pittsburgh: pp 175 (2012)
36. Moarefi, I., LaFevre-Bernt, M., Sicheri, F., Huse, M., Lee, C.H., Kuriyan, J., Miller, W.T.: Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature 385, 650–653 (1997)
37. Engen, J.R.: Analysis of unfolding and protein dynamics in the regulatory domains of hematopoietic cell kinase with hydrogen exchange and mass spectrometry. Doctoral Dissertation, Dept. of Chemistry. University of Nebraska-Lincoln, Lincoln (1999)
38. Mandell, J.G., Baerga-Ortiz, A., Akashi, S., Takio, K., Komives, E.A.: Solvent accessibility of the thrombin-thrombomodulin interface. J. Mol. Biol. 306, 575–589 (2001)
39. Zhang, Z., Smith, D.L.: Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation. Protein Sci. 2, 522–531 (1993)
40. Engen, J.R., Smithgall, T.E., Gmeiner, W.H., Smith, D.L.: Identification and localization of slow, natural, cooperative unfolding in the hematopoietic cell kinase SH3 domain by amide hydrogen exchange and mass spectrometry. Biochemistry 36, 14384–14391 (1997)
41. Engen, J.R., Wales, T.E., Chen, S., Marzluff, E.M., Hassell, K.M., Weis, D.D., Smithgall, T.E.: Partial cooperative unfolding in proteins as observed by hydrogen exchange mass spectrometry. Int. Rev. Phys. Chem. 32, 96–127 (2013)
42. Wales, T.E., Fadgen, K.E., Gerhardt, G.C., Engen, J.R.: High-speed and high-resolution UPLC separation at zero degrees Celsius. Anal. Chem. 80, 6815–6820 (2008)
43. Wang, L., Pan, H., Smith, D.L.: Hydrogen exchange-mass spectrometry: optimization of digestion conditions. Mol. Cell. Proteom. 1, 132–138 (2002)
44. Wu, Y., Kaveti, S., Engen, J.R.: Extensive deuterium back-exchange in certain immobilized pepsin columns used for H/D exchange mass spectrometry. Anal. Chem. 78, 1719–1723 (2006)
45. Hochrein, J.M., Wales, T.E., Lerner, E.C., Schiavone, A.P., Smithgall, T.E., Engen, J.R.: Conformational features of the full-length HIV and SIV Nef proteins determined by mass spectrometry. Biochemistry 45, 7733–7739 (2006)
46. Pene-Dumitrescu, T., Shu, S.T., Wales, T.E., Alvarado, J.J., Shi, H., Narute, P., Moroco, J.A., Yeh, J.I., Engen, J.R., Smithgall, T.E.: HIV-1 Nef interaction influences the ATP-binding site of the Src-family kinase. Hck. BMC Chem. Biol. 12, 1 (2012)
47. Hvidt, A., Linderstrom-Lang, K.: Exchange of hydrogen atoms in insulin with deuterium atoms in aqueous solutions. Biochim. Biophys. Acta 14, 574–575 (1954)
48. Choi, H.J., Smithgall, T.E.: Conserved residues in the HIV-1 Nef hydrophobic pocket are essential for recruitment and activation of the Hck tyrosine kinase. J. Mol. Biol. 343, 1255–1268 (2004)
49. Mayne, L.: Hydrogen exchange mass spectrometry. Methods Enzymol. 566, 335–356 (2016)
50. Bai, Y., Milne, J.S., Mayne, L., Englander, S.W.: Primary structure effects on peptide group hydrogen exchange. Proteins 17, 75–86 (1993)
51. Molday, R.S., Englander, S.W., Kallen, R.G.: Primary structure effects on peptide group hydrogen exchange. Biochemistry 11, 150–158 (1972)
52. Saksela, K., Cheng, G., Baltimore, D.: Proline-rich (PxxP) motifs in HIV-1 Nef bind to SH3 domains of a subset of Src kinases and are required for the enhanced growth of Nef+ viruses but not for down-regulation of CD4. EMBO J. 14, 484–491 (1995)
53. Sheff, J.G., Rey, M., Schriemer, D.C.: Peptide–column interactions and their influence on back exchange rates in hydrogen/deuterium exchange-MS. J. Am. Soc. Mass Spectrom. 24, 1006–1015 (2013)