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Monomeric structure of the cardioprotective chemokine SDF-1/CXCL12

  1. Christopher T. Veldkamp,
  2. Joshua J. Ziarek,
  3. Jidong Su,
  4. Harihar Basnet,
  5. Richard Lennertz,
  6. Joshua J. Weiner,
  7. Francis C. Peterson,
  8. John E. Baker,
  9. Brian F. Volkman*

Article first published online: 20 MAY 2009

DOI: 10.1002/pro.167

Issue

Protein Science

Protein Science

Volume 18, Issue 7, pages 1359–1369, July 2009

Additional Information

How to Cite

Veldkamp, C. T., Ziarek, J. J., Su, J., Basnet, H., Lennertz, R., Weiner, J. J., Peterson, F. C., Baker, J. E. and Volkman, B. F. (2009), Monomeric structure of the cardioprotective chemokine SDF-1/CXCL12. Protein Science, 18: 1359–1369. doi: 10.1002/pro.167

Author Information

  1. Department of Biochemistry, Medical College of Wisconsin, Milwaukee, Wisconsin 53226

*Department of Biochemistry, Medical College of Wisconsin, 8701 Watertown Plank Road, Milwaukee, WI 53226

Publication History

  1. Issue published online: 23 JUN 2009
  2. Article first published online: 20 MAY 2009
  3. Accepted manuscript online: 20 MAY 2009 12:00AM EST
  4. Manuscript Accepted: 7 MAY 2009
  5. Manuscript Received: 22 MAR 2009

Funded by

  • NIH. Grant Number: R01 AI058072
  • SpinOdyssey American Cancer Society Postdoctoral Fellowship
  • State of Wisconsin Breast Cancer Research Tax Check Off Grant

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References

  • 1
    Baggiolini M (2001) Chemokines in pathology and medicine. J Intern Med 250: 91–104.
  • 2
    Fernandez EJ, Lolis E (2002) Structure, function, and inhibition of chemokines. Annu Rev Pharmacol Toxicol 42: 469–499.
  • 3
    Rossi D, Zlotnik A (2000) The biology of chemokines and their receptors. Annu Rev Immunol 18: 217–242.
  • 4
    Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T (1996) Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382: 635–638.
  • 5
    Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T. (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393: 591–594.
  • 6
    Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR (1998) Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393: 595–599.
  • 7
    Bleul CC, Farzan M, Choe H, Parolin C, Clark-Lewis I, Sodroski J, Springer TA (1996) The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382: 829–833.
  • 8
    Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272: 872–877.
  • 9
    D'Souza MP, Harden VA (1996) Chemokines and HIV-1 second receptors. Confluence of two fields generates optimism in AIDS research. Nat Med 2: 1293–1300.
  • 10
    D'Souza MP, Cairns JS, Plaeger SF (2000) Current evidence and future directions for targeting HIV entry: therapeutic and prophylactic strategies. JAMA 284: 215–222.
  • 11
    Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verastequi E, Zlotnik A (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410: 50–56.
  • 12
    Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, Giordano FJ (2004) Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110: 3300–3305.
  • 13
    Hu X, Dai S, Wu WJ, Tan W, Zhu X, Mu J, Guo Y, Bolli R, Rokosh G (2007) Stromal cell derived factor-1 alpha confers protection against myocardial ischemia/reperfusion injury: role of the cardiac stromal cell derived factor-1 alpha CXCR4 axis. Circulation 116: 654–663.
  • 14
    Saxena A, Fish JE, White MD, Yu S, Smyth JW, Shaw RM, DiMaio JM, Srivastava D (2008) Stromal cell-derived factor-1alpha is cardioprotective after myocardial infarction. Circulation 117: 2224–2231.
  • 15
    Segers VF, Tokunou T, Higgins LJ, MacGillivray C, Gannon J, Lee RT (2007) Local delivery of protease-resistant stromal cell derived factor-1 for stem cell recruitment after myocardial infarction. Circulation 116: 1683–1692.
  • 16
    Sasaki T, Fukazawa R, Ogawa S, Kanno S, Nitta T, Ochi M, Shimizu K (2007) Stromal cell-derived factor-1alpha improves infarcted heart function through angiogenesis in mice. Pediatr Int 49: 966–971.
  • 17
    Koch KC, Schaefer WM, Liehn EA, Rammos C, Mueller D, Schroeder J, Dimassi T, Stopinski T, Weber C (2006) Effect of catheter-based transendocardial delivery of stromal cell-derived factor 1alpha on left ventricular function and perfusion in a porcine model of myocardial infarction. Basic Res Cardiol 101: 69–77.
  • 18
    Zhang G, Nakamura Y, Wang X, Hu Q, Suggs LJ, Zhang J (2007) Controlled release of stromal cell-derived factor-1 alpha in situ increases c-kit+ cell homing to the infarcted heart. Tissue Eng 13: 2063–2071.
  • 19
    Penn MS, Zhang M, Deglurkar I, Topol EJ (2004) Role of stem cell homing in myocardial regeneration. Int J Cardiol 95 (Suppl 1): S23–S25.
  • 20
    Yamaguchi J, Kusano KF, Masuo O, Kawamoto A, Silver M, Murasawa S, Bosch-Marce M, Masuda H, Losordo DW, Isner JM, Asahara T (2003) Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107: 1322–1328.
  • 21
    Hattori K, Heissig B, Tashiro K, Honjo T, Tateno M, Shieh JH, Hackett NR, Quitoriano MS, Crystal RG, Rafii S, Moore MA (2001) Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 97: 3354–3360.
  • 22
    Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, Rafii S (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109: 625–637.
  • 23
    Dealwis C, Fernandez EJ, Thompson DA, Simon RJ, Siani MA, Lolis E (1998) Crystal structure of chemically synthesized [N33A] stromal cell-derived factor 1alpha, a potent ligand for the HIV-1 “fusin” coreceptor. Proc Natl Acad Sci USA 95: 6941–6946.
  • 24
    Ohnishi Y, Senda T, Nandhagopal N, Sugimoto K, Shioda T, Nagal Y, Mitsui Y (2000) Crystal structure of recombinant native SDF-1alpha with additional mutagenesis studies: an attempt at a more comprehensive interpretation of accumulated structure-activity relationship data. J Interferon Cytokine Res 20: 691–700.
  • 25
    Ryu EK, Kim TG, Kwon TH, Jung ID, Ryu D, Park YM, Kim J, Ahn KH, Ban C (2007) Crystal structure of recombinant human stromal cell-derived factor-1alpha. Proteins 67: 1193–1197.
  • 26
    Veldkamp CT, Peterson FC, Pelzek AJ, Volkman BF (2005) The monomer-dimer equilibrium of stromal cell-derived factor-1 (CXCL 12) is altered by pH, phosphate, sulfate, and heparin. Protein Sci 14: 1071–1081.
  • 27
    Veldkamp CT, Seibert C, Peterson FC, De la Cruz NB, Haugner JC, III, Basnet H, Sakmar TP, Volkman BF (2008) Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12. Sci Signal 1: ra4.
  • 28
    Veldkamp CT, Seibert C, Peterson FC, Sakmar TP, Volkman BF (2006) Recognition of a CXCR4 sulfotyrosine by the chemokine stromal cell-derived factor-1alpha (SDF-1alpha/CXCL12). J Mol Biol 359: 1400–1409.
  • 29
    Crump MP, Gong JH, Loetscher P, Rajarathnam K, Amara A, Arenzana-Seisdedos F, Virelizier JL, Baggiolini M, Sykes BD, Clark-Lewis I (1997) Solution structure and basis for functional activity of stromal cell-derived factor-1; dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J 16: 6996–7007.
  • 30
    Ohnishi Y, Senda T, Nandhagopal N, Sugimoto K, Shioda T, Nagal Y, Mitsui Y (2000) Crystal structure of recombinant native SDF-1alpha with additional mutagenesis studies: an attempt at a more comprehensive interpretation of accumulated structure-activity relationship data. J Interferon Cytokine Res 20: 691–700.
  • 31
    Dealwis C, Fernandez EJ, Thompson DA, Simon RJ, Siani MA, Lolis E (1998) Crystal structure of chemically synthesized [N33A] stromal cell-derived factor 1alpha, a potent ligand for the HIV-1 “fusin” coreceptor. Proc Natl Acad Sci USA 95: 6941–6946.
  • 32
    Gozansky EK, Louis JM, Caffrey M, Clore GM (2005) Mapping the binding of the N-terminal extracellular tail of the CXCR4 receptor to stromal cell-derived factor-1alpha. J Mol Biol 345: 651–658.
  • 33
    Baryshnikova OK, Sykes BD (2006) Backbone dynamics of SDF-1alpha determined by NMR: interpretation in the presence of monomer-dimer equilibrium. Protein Sci 15: 2568–2578.
  • 34
    Tjandra N, Bax A (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278: 1111–1114.
  • 35
    Tjandra N, Omichinski JG, Gronenborn AM, Clore GM, Bax A (1997) Use of dipolar 1H-15N and 1H-13C couplings in the structure determination of magnetically oriented macromolecules in solution. Nat Struct Biol 4: 732–738.
  • 36
    Ottiger M, Bax A (1998) Characterization of magnetically oriented phospholipid micelles for measurement of dipolar couplings in macromolecules. J Biomol NMR 12: 361–372.
  • 37
    Fleming K, Matthews S (2004) Media for studies of partially aligned states. Methods Mol Biol 278: 79–88.
  • 38
    Rajarathnam K, Sykes BD, Kay CM, Dewald B, Geiser T, Baggiolini M, Clark-Lewis I (1994) Neutrophil activation by monomeric interleukin-8. Science 264: 90–92.
  • 39
    Allen SJ, Crown SE, Handel TM (2007) Chemokine: receptor structure, interactions, and antagonism. Annu Rev Immunol 25: 787–820.
  • 40
    Hoogewerf AJ, Kuschert GS, Proudfoot AE, Borlat F, Clark-Lewis I, Power CA, Wells TN (1997) Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 36: 13570–13578.
  • 41
    Campanella GS, Grimm J, Manice LA, Colvin RA, Medoff BD, Wojtkiewicz GR, Weissleder R, Luster AD (2006) Oligomerization of CXCL10 is necessary for endothelial cell presentation and in vivo activity. J Immunol 177: 6991–6998.
  • 42
    Proudfoot AE, Handel TM, Johnson Z, Lau EK, LiWang P, Clark-Lewis I, Borlat F, Wells TN, Kosco-Vilbois MH (2003) Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc Natl Acad Sci USA 100: 1885–1890.
  • 43
    Handel TM, Johnson Z, Rodrigues DH, Dos Santos AC, Cirillo R, Muzio V, Riva S, Mack M, Deruaz M, Borlat F, Vitte PA, Wells TN, Teixeira MM, Reoudfoot AE (2008) An engineered monomer of CCL2 has anti-inflammatory properties emphasizing the importance of oligomerization for chemokine activity in vivo. J Leukoc Biol 84: 1101–1108.
  • 44
    Johnson Z, Kosco-Vilbois MH, Herren S, Cirillo R, Muzio V, Zaratin P, Carbonatto M, Mack M, Smailbegovic A, Rose M, Lever R, Page C, Wells TN, Proudfoot AE. (2004) Interference with heparin binding and oligomerization creates a novel anti-inflammatory strategy targeting the chemokine system. J Immunol 173: 5776–5785.
  • 45
    Veldkamp CT, Peterson FC, Hayes PL, Mattmiller JE, Haugner JC, III, de la Cruz N, Volkman BF (2007) On-column refolding of recombinant chemokines for NMR studies and biological assays. Protein Expr Purif 52: 202–209.
  • 46
    Baker JE, Curry BD, Olinger GN, Gross GJ (1997) Increased tolerance of the chronically hypoxic immature heart to ischemia. Contribution of the KATP channel. Circulation 95: 1278–1285.
  • 47
    Baker JE, Konorev EA, Gross GJ, Chilian WM, Jacob HJ (2000) Resistance to myocardial ischemia in five rat strains: is there a genetic component of cardioprotection? Am J Physiol Heart Circ Physiol 278: H1395–H1400.
  • 48
    Sudmeier JL, Ash EL, Gunther UL, Luo X, Bullock PA, Bachovchin WW (1996) HCN, a triple-resonance NMR technique for selective observation of histidine and tryptophan side chains in 13C/15N-labeled proteins. J Magn Reson B 113: 236–247.
  • 49
    Markley JL, Ulrich EL, Westler WM, Volkman BF (2003) Macromolecular structure determination by NMR spectroscopy. Methods Biochem Anal 44: 89–113.
  • 50
    Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289–302.
  • 51
    Herrmann T, Guntert P, Wuthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319: 209–227.
  • 52
    Linge JP, Williams MA, Spronk CA, Bonvin AM, Nilges M (2003) Refinement of protein structures in explicit solvent. Proteins 50: 496–506.
  • 53
    Altieri AS, Hinton DP, Byrd RA (1995) Association of biomolecular systems via pulsed field gradient NMR self-diffusion measurements. J Am Chem Soc 117: 7566–7567.
  • 54
    Uedaira H, Uedaira H (1970) Translational frictional coefficients of molecules in aqueous solution. J Phys Chem 74: 2211–2214.
  • 55
    Ottiger M, Delaglio F, Bax A (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J Magn Reson 131: 373–378.
  • 56
    Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277–293.
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