A locked, dimeric CXCL12 variant effectively inhibits pulmonary metastasis of CXCR4-expressing melanoma cells due to enhanced serum stability

Molecular Cancer Therapeutics

Volumn 11, Issue 11, 2012, Pages 2516-2525

  Takekoshi, Tomonori ^a   Ziarek, Joshua J ^a   Volkman, Brian F ^a   Hwang, Sam T ^a  

^a FROEDTERT MEMORIAL LUTHERAN HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CHEMOKINE RECEPTOR CXCR122; CHEMOKINE RECEPTOR CXCR4; DIPEPTIDYL PEPTIDASE IV; GELATINASE A; PLERIXAFOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CANCER INHIBITION; CANCER RESISTANCE; CONTROLLED STUDY; DRUG EFFICACY; ENZYMATIC DEGRADATION; FEMALE; GENE INACTIVATION; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; WESTERN BLOTTING;

ANIMALS; CALCIUM; CELL PROLIFERATION; CHEMOKINE CXCL12; DIPEPTIDYL PEPTIDASE 4; HETEROCYCLIC COMPOUNDS; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 2; MELANOMA; MICE; MICE, INBRED C57BL; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; RECEPTORS, CXCR4; SERUM;

EID: 84869226562     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-12-0494     Document Type: Article

References (38)

1. Ben-Baruch A. The multifaceted roles of chemokines in malignancy. Cancer Metastasis Rev 2006;25:357-71. (Pubitemid 44922355)
2. Sun X, Cheng G, Hao M, Zheng J, Zhou X, Zhang J, et al. CXCL12/CXCR4/CXCR7 chemokine axis and cancer progression. Cancer Metastasis Rev 2010;29:709-22.
3. Dell'Agnola C, Biragyn A. Clinical utilization of chemokines to combat cancer: the double-edged sword. Expert Rev Vaccines 2007;6:267-83. (Pubitemid 46607460)
4. Murakami T, Maki W, Cardones AR, Fang H, Tun Kyi A, Nestle FO, et al. Expression of CXC chemokine receptor-4 enhances the pulmonary metastatic potential of murine B16 melanoma cells. Cancer Res 2002;62:7328-34. (Pubitemid 36025256)
5. Cardones AR, Murakami T, Hwang ST. CXCR4 enhances adhesion of B16 tumor cells to endothelial cells in vitro and in vivo via beta(1) integrin. Cancer Res 2003;63:6751-7. (Pubitemid 37322955)
6. Drury LJ, Ziarek JJ, Gravel S, Veldkamp CT, Takekoshi T, Hwang ST, et al. Monomeric and dimeric CXCL12 inhibit metastasis through distinct CXCR4 interactions and signaling pathways. Proc Natl Acad Sci U S A 2011;108:17655-60.
7. Veldkamp CT, Peterson FC, Pelzek AJ, Volkman BF. The monomer-dimer equilibrium of stromal cell-derived factor-1 (CXCL 12) is altered by pH, phosphate, sulfate, and heparin. Protein Sci 2005;14:1071-81. (Pubitemid 40389378)
8. Veldkamp CT, Seibert C, Peterson FC, Volkman BF. Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12. Sci Signal 2008;1ra4:1-9.
9. Laguri C, Sadir R, Rueda P, Baleux F, Gans P, Arenzana-Seisdedos F, et al. The novel CXCL12gamma isoform encodes an unstructured cationic domain which regulates bioactivity and interaction with both glycosaminoglycans and CXCR4. PLoS ONE 2007;2:e1110.
10. McQuibban GA, Butler GS, Gong JH, Bendall L, Power C, Clark-Lewis I, et al. Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1. J Biol Chem 2001;276:43503-8.
11. Christopherson KW 2nd, Hangoc G, Broxmeyer HE. Cell surface peptidase CD26/dipeptidylpeptidase IV regulates CXCL12/stromal cell-derived factor-1 alpha-mediated chemotaxis of human cord blood CD34+ progenitor cells. J Immunol 2002;169:7000-8. (Pubitemid 36899288)
12. Tomihari M, Chung JS, Akiyoshi H, Cruz PD Jr, Ariizumi K. DC-HIL/glycoprotein nmb promotes growth of melanoma in mice by inhibiting the activation of tumor-reactive T cells. Cancer Res 2010;70:5778-87.
13. Wiley HE, Gonzalez EB, Maki W, Wu MT, Hwang ST. Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma. J Natl Cancer Inst 2001;93:1638-43. (Pubitemid 33094871)
14. Feng Y, Broder CC, Kennedy PE, Berger EA. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 1996;272:872-7. (Pubitemid 26154590)
15. De Clercq E. The AMD3100 story: the path to the discovery of a stem cell mobilizer (mozobil). Biochem Pharmacol 2009;77:1655-64.
16. D'Alterio C, Barbieri A, Portella L, Palma G, Polimeno M, Riccio A, et al. Inhibition of stromal CXCR4 impairs development of lung metastases. Cancer Immunol Immunother 2012. [Epub ahead of print].
17. Smith MC, Luker KE, Garbow JR, Prior JL, Jackson E, Piwnica-Worms D, et al. CXCR4 regulates growth of both primary and metastatic breast cancer. Cancer Res 2004;64:8604-12. (Pubitemid 39552073)
18. Davis DA, Singer KE, De La Luz Sierra M, Narazaki M, Yang F, Fales HM, et al. Identification of carboxypeptidase N as an enzyme responsible for C-terminal cleavage of stromal cell-derived factor-1alpha in the circulation. Blood 2005;105:4561-8. (Pubitemid 40807271)
19. Lambeir AM, Proost P, Durinx C, Bal G, Senten K, Augustyns K, et al. Kinetic investigation of chemokine truncation by CD26/dipeptidyl peptidase IV reveals a striking selectivity within the chemokine family. J Biol Chem 2001;276:29839-45.
20. Segers VF, Revin V, Wu W, Qiu H, Yan Z, Lee RT, et al. Protease-resistant stromal cell-derived factor-1 for the treatment of experimental peripheral artery disease. Circulation 2011;123:1306-15.
21. Ohtsuki T, Hosono O, Kobayashi H, Munakata Y, Souta A, Shioda T, et al. Negative regulation of the anti-human immunodeficiency virus and chemotactic activity of human stromal cell-derived factor 1alpha by CD26/dipeptidyl peptidase IV. FEBS Lett 1998;431:236-40. (Pubitemid 28334224)
22. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001;410:50-6. (Pubitemid 32225831)
23. Marechal R, Demetter P, Nagy N, Berton A, Decaestecker C, Polus M, et al. High expression of CXCR4 may predict poor survival in resected pancreatic adenocarcinoma. Br J Cancer 2009;100:1444-51.
24. Sekiya R, Kajiyama H, Sakai K, Umezu T, Mizuno M, Shibata K, et al. Expression of CXCR4 indicates poor prognosis in patients with clear cell carcinoma of the ovary. Hum Pathol 2012;43:904-10.
25. Hiratsuka S, Duda DG, Huang Y, Goel S, Sugiyama T, Nagasawa T, et al. C-X-C receptor type 4 promotes metastasis by activating p38 mitogen-activated protein kinase in myeloid differentiation antigen (gr-1)-positive cells. Proc Natl Acad Sci U S A 2011;108:302-7.
26. Brinckerhoff LH, Kalashnikov VV, Thompson LW, Yamshchikov GV, Pierce RA, Galavotti HS, et al. Terminal modifications inhibit proteolytic degradation of an immunogenic MART-1(27-35) peptide: implications for peptide vaccines. Int J Cancer 1999;83:326-34. (Pubitemid 29455755)
27. Mentlein R, Gallwitz B, Schmidt WE. Dipeptidyl-peptidase IV hydrolyses gastric inhibitory polypeptide, glucagon-like peptide-1(7-36)amide, peptide histidine methionine and is responsible for their degradation in human serum. Eur J Biochem 1993;214:829-35. (Pubitemid 23188160)
28. Bellmann-Sickert K, Beck-Sickinger AG. Palmitoylated SDF1alpha shows increased resistance against proteolytic degradation in liver homogenates. ChemMedChem 2011;6:193-200.
29. Kluskens LD, Nelemans SA, Rink R, de Vries L, Meter-Arkema A, Wang Y, et al. Angiotensin-(1-7) with thioether bridge: an angiotensin-converting enzyme-resistant, potent angiotensin-(1-7) analog. J Pharmacol Exp Ther 2009;328:849-54.
30. Baggiolini M, Dewald B, Moser B. Interleukin-8 and related chemotactic cytokines-CXC and CC chemokines. Adv Immunol 1994;55:97-179.
31. Van Zee KJ, Fischer E, Hawes AS, Hebert CA, Terrell TG, Baker JB, et al. Effects of intravenous IL-8 administration in nonhuman primates. J Immunol 1992;148:1746-52.
32. Crump MP, Gong JH, Loetscher P, Rajarathnam K, Amara A, Arenzana-Seisdedos F, et al. 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 1997;16:6996-7007. (Pubitemid 27520800)
33. Kanki S, Segers VF, Wu W, Kakkar R, Gannon J, Sys SU, et al. Stromal cell-derived factor-1 retention and cardioprotection for ischemic myocardium. Circ Heart Fail 2011;4:509-18.
34. Bartolome RA, Molina-Ortiz I, Samaniego R, Sanchez-Mateos P, Bustelo XR, Teixido J. Activation of Vav/Rho GTPase signaling by CXCL12 controls membrane-type matrix metalloproteinase-dependent melanoma cell invasion. Cancer Res 2006;66:248-58. (Pubitemid 43166031)
35. Delgado MB, Clark-Lewis I, Loetscher P, Langen H, Thelen M, Baggiolini M, et al. Rapid inactivation of stromal cell-derived factor-1 by cathepsin G associated with lymphocytes. Eur J Immunol 2001;31:699-707. (Pubitemid 32237105)
36. Valenzuela-Fernandez A, Planchenault T, Baleux F, Staropoli I, LeBarillec K, Leduc D, et al. Leukocyte elastase negatively regulates stromal cell-derived factor-1 (SDF-1)/CXCR4 binding and functions by amino-terminal processing of SDF-1 and CXCR4. J Biol Chem 2002;277:15677-89. (Pubitemid 34967841)
37. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002;2:161-74. (Pubitemid 37328786)
38. DiPersio JF, Uy GL, Yasothan U, Kirkpatrick P. Plerixafor. Nat Rev Drug Discov 2009;8:105-6.