Capacity of wild-type and chemokine-armed parvovirus H-1PV for inhibiting neo-angiogenesis

Virology

Volumn 447, Issue 1-2, 2013, Pages 221-232

  Lavie, Muriel ^a   Struyf, Sofie ^b   Stroh Dege, Alexandra ^a   Rommelaere, Jean ^a   Van Damme, Jo ^b   Dinsart, Christiane ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

Angiogenesis; Cancer therapy; Chemokine; Kaposi sarcoma; Parvovirus

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CXCR3; CXCL4 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; ONCOLYTIC H-1 PARVOVIRUS; ONCOLYTIC PARVOVIRUS; UNCLASSIFIED DRUG; VASCULOTROPIN; VIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL CULTURE; CELL IMMORTALIZATION; CELL KILLING; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG TARGETING; ENDOTHELIUM CELL; FEMALE; GENETIC TRANSDUCTION; H-1 PARVOVIRUS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOLYTIC VIROTHERAPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; TUMOR GROWTH; TUMOR VASCULARIZATION; UMBILICAL VEIN ENDOTHELIAL CELL; VIROGENESIS; WILD TYPE;

ANGIOGENESIS; CANCER THERAPY; CHEMOKINE; KAPOSI SARCOMA; PARVOVIRUS;

ANIMALS; BIOLOGICAL THERAPY; CELL SURVIVAL; CELLS, CULTURED; CHEMOKINES; ENDOTHELIAL CELLS; HUMANS; MICE; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PARVOVIRUS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 84885025161     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.09.019     Document Type: Article

References (91)

1. Abu El-Asrar A.M., Struyf S., Descamps F.J., Al-Obeidan S.A., Proost P., Van Damme J., Opdenakker G., Geboes K. Chemokines and gelatinases in the aqueous humor of patients with active uveitis. Am. J. Ophthalmol. 2004, 138(3):401-411.
2. Albini A., Paglieri I., Orengo G., Carlone S., Aluigi M.G., DeMarchi R., Matteucci C., Mantovani A., Carozzi F., Donini S., Benelli R. The beta-core fragment of human chorionic gonadotrophin inhibits growth of Kaposi's sarcoma-derived cells and a new immortalized Kaposi's sarcoma cell line. AIDS 1997, 11(6):713-721.
3. Angelova A.L., Aprahamian M., Balboni G., Delecluse H.J., Feederle R., Kiprianova I., Grekova S.P., Galabov A.S., Witzens-Harig M., Ho A.D., Rommelaere J., Raykov Z. Oncolytic rat parvovirus H-1PV, a candidate for the treatment of human lymphoma: in vitro and in vivo studies. Mol. Ther. 2009, 17(7):1164-1172.
4. Angiolillo A.L., Sgadari C., Taub D.D., Liao F., Farber J.M., Maheshwari S., Kleinman H.K., Reaman G.H., Tosato G. Human interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J. Exp. Med. 1995, 182(1):155-162.
5. Ball-Goodrich L.J., Leland S.E., Johnson E.A., Paturzo F.X., Jacoby R.O. Rat parvovirus type 1: the prototype for a new rodent parvovirus serogroup. J. Virol. 1998, 72(4):3289-3299.
6. Bergers G., Song S., Meyer-Morse N., Bergsland E., Hanahan D. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J. Clin. Invest. 2003, 111(9):1287-1295.
7. Bhat R., Dempe S., Dinsart C., Rommelaere J. Enhancement of NK cell antitumor responses using an oncolytic parvovirus. Int. J. Cancer 2011, 128(4):908-919.
8. Bodnar R.J., Yates C.C., Wells A. IP-10 blocks vascular endothelial growth factor-induced endothelial cell motility and tube formation via inhibition of calpain. Circ. Res. 2006, 98(5):617-625.
9. Brandenburger A., Legendre D., Avalosse B., Rommelaere J. NS-1 and NS-2 proteins may act synergistically in the cytopathogenicity of parvovirus MVMp. Virology 1990, 174(2):576-584.
10. Breitbach C.J., Arulanandam R., De Silva N., Thorne S.H., Patt R., Daneshmand M., Moon A., Ilkow C., Burke J., Hwang T.H., Heo J., Cho M., Chen H., Angarita F.A., Addison C., McCart J.A., Bell J.C., Kirn D.H. Oncolytic vaccinia virus disrupts tumor-associated vasculature in humans. Cancer Res. 2013, 73(4):1265-1275.
11. Breitbach C.J., Thorne S.H., Bell J.C., Kirn D.H. Targeted and armed oncolytic poxviruses for cancer: the lead example of JX-594. Curr. Pharmacol. Biotechnol. 2011, 13(9):1768-1772.
12. Brockhaus K., Plaza S., Pintel D.J., Rommelaere J., Salome N. Nonstructural proteins NS2 of minute virus of mice associate in vivo with 14-3-3 protein family members. J. Virol. 1996, 70(11):7527-7534.
13. Caillet-Fauquet P., Perros M., Brandenburger A., Spegelaere P., Rommelaere J. Programmed killing of human cells by means of an inducible clone of parvoviral genes encoding non-structural proteins. EMBO J. 1990, 9(9):2989-2995.
14. Chung A.S., Lee J., Ferrara N. Targeting the tumour vasculature: insights from physiological angiogenesis. Nat. Rev. Cancer 2010, 10(7):505-514.
15. Cole C.A., Nathanson N., Rivet H. Viral hemorrhagic encephalopathy of rats. II. Pathogenesis of central nervous system lesions. Am. J. Epidemiol. 1970, 91(3):339-350.
16. Cornali E., Zietz C., Benelli R., Weninger W., Masiello L., Breier G., Tschachler E., Albini A., Sturzl M. Vascular endothelial growth factor regulates angiogenesis and vascular permeability in Kaposi's sarcoma. Am. J. Pathol. 1996, 149(6):1851-1869.
17. Cornelis J.J., Spruyt N., Spegelaere P., Guetta E., Darawshi T., Cotmore S.F., Tal J., Rommelaere J. Sensitization of transformed rat fibroblasts to killing by parvovirus minute virus of mice correlates with an increase in viral gene expression. J. Virol. 1988, 62(9):3438-3444.
18. Cotmore S.F., D'Abramo A.M., Carbonell L.F., Bratton J., Tattersall P. The NS2 polypeptide of parvovirus MVM is required for capsid assembly in murine cells. Virology 1997, 231(2):267-280.
19. Cotmore S.F., Gottlieb R.L., Tattersall P. Replication initiator protein NS1 of the parvovirus minute virus of mice binds to modular divergent sites distributed throughout duplex viral DNA. J. Virol. 2007, 81(23):13015-13027.
20. Cotmore S.F., Tattersall P. Parvoviral host range and cell entry mechanisms. Adv. Virus Res. 2007, 70:183-232.
21. Dempe S., Lavie M., Struyf S., Bhat R., Verbeke H., Paschek S., Berghmans N., Geibig R., Rommelaere J., Van Damme J., Dinsart C. Antitumoral activity of parvovirus-mediated IL-2 and MCP-3/CCL7 delivery into human pancreatic cancer: implication of leucocyte recruitment. Cancer Immunol. Immunother. 2012, 61(11):2113-2123.
22. Dubrac A., Quemener C., Lacazette E., Lopez F., Zanibellato C., Wu W.G., Bikfalvi A., Prats H. Functional divergence between 2 chemokines is conferred by single amino acid change. Blood 2010, 116(22):4703-4711.
23. Ebos J.M., Kerbel R.S. Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat. Rev. Clin. Oncol. 2011, 8(4):210-221.
24. Ehlert J.E., Addison C.A., Burdick M.D., Kunkel S.L., Strieter R.M. Identification and partial characterization of a variant of human CXCR3 generated by posttranscriptional exon skipping. J. Immunol. 2004, 173(10):6234-6240.
25. Eisman R., Surrey S., Ramachandran B., Schwartz E., Poncz M. Structural and functional comparison of the genes for human platelet factor 4 and PF4alt. Blood 1990, 76(2):336-344.
26. Ellis L.M., Hicklin D.J. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat. Rev. Cancer 2008, 8(8):579-591.
27. Enderlin M., Kleinmann E.V., Struyf S., Buracchi C., Vecchi A., Kinscherf R., Kiessling F., Paschek S., Sozzani S., Rommelaere J., Cornelis J.J., Van Damme J., Dinsart C. TNF-alpha and the IFN-gamma-inducible protein 10 (IP-10/CXCL-10) delivered by parvoviral vectors act in synergy to induce antitumor effects in mouse glioblastoma. Cancer Gene Ther. 2009, 16(2):149-160.
28. Farber J.M. Mig and IP-10: CXC chemokines that target lymphocytes. J. Leukoc. Biol. 1997, 61(3):246-257.
29. Ferrara N. Pathways mediating VEGF-independent tumor angiogenesis. Cytokine Growth Factor Rev. 2010, 21(1):21-26.
30. Ferrara N., Alitalo K. Clinical applications of angiogenic growth factors and their inhibitors. Nat. Med. 1999, 5(12):1359-1364.
31. Geletneky K., Huesing J., Rommelaere J., Schlehofer J.R., Leuchs B., Dahm M., Krebs O., von Knebel Doeberitz M., Huber B., Hajda J. Phase I/IIa study of intratumoral/intracerebral or intravenous/intracerebral administration of Parvovirus H-1 (ParvOryx) in patients with progressive primary or recurrent glioblastoma multiforme: ParvOryx01 protocol. BMC Cancer 2012, 12:99.
32. Geletneky K., Kiprianova I., Ayache A., Koch R., Herrero Y.C.M., Deleu L., Sommer C., Thomas N., Rommelaere J., Schlehofer J.R. Regression of advanced rat and human gliomas by local or systemic treatment with oncolytic parvovirus H-1 in rat models. Neuro Oncol. 2010, 12(8):804-814.
33. Gengrinovitch S., Greenberg S.M., Cohen T., Gitay-Goren H., Rockwell P., Maione T.E., Levi B.Z., Neufeld G. Platelet factor-4 inhibits the mitogenic activity of VEGF121 and VEGF165 using several concurrent mechanisms. J. Biol. Chem. 1995, 270(25):15059-15065.
34. Gerwins P., Skoldenberg E., Claesson-Welsh L. Function of fibroblast growth factors and vascular endothelial growth factors and their receptors in angiogenesis. Crit. Rev. Oncol. Hematol. 2000, 34(3):185-194.
35. Giese N.A., Raykov Z., DeMartino L., Vecchi A., Sozzani S., Dinsart C., Cornelis J.J., Rommelaere J. Suppression of metastatic hemangiosarcoma by a parvovirus MVMp vector transducing the IP-10 chemokine into immunocompetent mice. Cancer Gene Ther. 2002, 9(5):432-442.
36. Giuliano S., Pages G. Mechanisms of resistance to anti-angiogenesis therapies. Biochimie 2013, 95(6):1110-1119.
37. Green C.J., Charles R.S., Edwards B.F., Johnson P.H. Identification and characterization of PF4varl, a human gene variant of platelet factor 4. Mol. Cell. Biol. 1989, 9(4):1445-1451.
38. Grekova S.P., Rommelaere J., Raykov Z. Parvoviruses-tools to fine-tune anticancer immune responses. Oncoimmunology 2012, 1(8):1417-1419.
39. Haag A., Menten P., Van Damme J., Dinsart C., Rommelaere J., Cornelis J.J. Highly efficient transduction and expression of cytokine genes in human tumor cells by means of autonomous parvovirus vectors; generation of antitumor responses in recipient mice. Hum. Gene Ther. 2000, 11(4):597-609.
40. Hoeben A., Landuyt B., Highley M.S., Wildiers H., Van Oosterom A.T., De Bruijn E.A. Vascular endothelial growth factor and angiogenesis. Pharmacol. Rev. 2004, 56(4):549-580.
41. Jacoby R.O., Ball-Goodrich L.J., Besselsen D.G., McKisic M.D., Riley L.K., Smith A.L. Rodent parvovirus infections. Lab. Anim. Sci. 1996, 46(4):370-380.
42. Jacoby R.O., Johnson E.A., Paturzo F.X., Ball-Goodrich L. Persistent rat virus infection in smooth muscle of euthymic and athymic rats. J. Virol. 2000, 74(24):11841-11848.
43. Jouan V., Canron X., Alemany M., Caen J.P., Quentin G., Plouet J., Bikfalvi A. Inhibition of in vitro angiogenesis by platelet factor-4-derived peptides and mechanism of action. Blood 1999, 94(3):984-993.
44. Kawada K., Hosogi H., Sonoshita M., Sakashita H., Manabe T., Shimahara Y., Sakai Y., Takabayashi A., Oshima M., Taketo M.M. Chemokine receptor CXCR3 promotes colon cancer metastasis to lymph nodes. Oncogene 2007, 26(32):4679-4688.
45. Keeley E.C., Mehrad B., Strieter R.M. Chemokines as mediators of tumor angiogenesis and neovascularization. Exp. Cell. Res. 2011, 317(5):685-690.
46. Keeley E.C., Mehrad B., Strieter R.M. CXC chemokines in cancer angiogenesis and metastases. Adv. Cancer Res. 2010, 106:91-111.
47. Kestler J., Neeb B., Struyf S., Van Damme J., Cotmore S.F., D'Abramo A., Tattersall P., Rommelaere J., Dinsart C., Cornelis J.J. cis requirements for the efficient production of recombinant DNA vectors based on autonomous parvoviruses. Hum. Gene Ther. 1999, 10(10):1619-1632.
48. Kirn D.H., Thorne S.H. Targeted and armed oncolytic poxviruses: a novel multi-mechanistic therapeutic class for cancer. Nat. Rev. Cancer 2009, 9(1):64-71.
49. Kottke T., Hall G., Pulido J., Diaz R.M., Thompson J., Chong H., Selby P., Coffey M., Pandha H., Chester J., Melcher A., Harrington K., Vile R. Antiangiogenic cancer therapy combined with oncolytic virotherapy leads to regression of established tumors in mice. J. Clin. Invest. 2010, 120(5):1551-1560.
50. Kowanetz M., Ferrara N. Vascular endothelial growth factor signaling pathways: therapeutic perspective. Clin. Cancer Res. 2006, 12(17):5018-5022.
51. Lasagni L., Francalanci M., Annunziato F., Lazzeri E., Giannini S., Cosmi L., Sagrinati C., Mazzinghi B., Orlando C., Maggi E., Marra F., Romagnani S., Serio M., Romagnani P. An alternatively spliced variant of CXCR3 mediates the inhibition of endothelial cell growth induced by IP-10, Mig, and I-TAC, and acts as functional receptor for platelet factor 4. J. Exp. Med. 2003, 197(11):1537-1549.
52. Li X., Rhode S.L. Mutation of lysine 405 to serine in the parvovirus H-1 NS1 abolishes its functions for viral DNA replication, late promoter trans activation, and cytotoxicity. J. Virol. 1990, 64(10):4654-4660.
53. Liu C., Luo D., Reynolds B.A., Meher G., Katritzky A.R., Lu B., Gerard C.J., Bhadha C.P., Harrison J.K. Chemokine receptor CXCR3 promotes growth of glioma. Carcinogenesis 2010, 32(2):129-137.
54. Liu M., Guo S., Stiles J.K. The emerging role of CXCL10 in cancer (Review). Oncol. Lett. 2011, 2(4):583-589.
55. Loetscher M., Gerber B., Loetscher P., Jones S.A., Piali L., Clark-Lewis I., Baggiolini M., Moser B. Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J. Exp. Med. 1996, 184(3):963-969.
56. Lorson C., Burger L.R., Mouw M., Pintel D.J. Efficient transactivation of the minute virus of mice P38 promoter requires upstream binding of NS1. J. Virol. 1996, 70(2):834-842.
57. Margolis G., Kilham L. Parvovirus infections, vascular endothelium, and hemorrhagic encephalopathy. Lab. Invest. 1970, 22(5):478-488.
58. Masood R., Cai J., Zheng T., Smith D.L., Naidu Y., Gill P.S. Vascular endothelial growth factor/vascular permeability factor is an autocrine growth factor for AIDS-Kaposi sarcoma. Proc. Nat. Acad. Sci. U.S.A. 1997, 94(3):979-984.
59. McKisic M.D., Macy J.D., Delano M.L., Jacoby R.O., Paturzo F.X., Smith A.L. Mouse parvovirus infection potentiates allogeneic skin graft rejection and induces syngeneic graft rejection. Transplantation 1998, 65(11):1436-1446.
60. Mesri E.A., Cesarman E., Boshoff C. Kaposi's sarcoma and its associated herpesvirus. Nat. Rev. Cancer 2010, 10(10):707-719.
61. Moehler M., Zeidler M., Schede J., Rommelaere J., Galle P.R., Cornelis J.J., Heike M. Oncolytic parvovirus H1 induces release of heat-shock protein HSP72 in susceptible human tumor cells but may not affect primary immune cells. Cancer Gene Ther. 2003, 10(6):477-480.
62. Moehler M.H., Zeidler M., Wilsberg V., Cornelis J.J., Woelfel T., Rommelaere J., Galle P.R., Heike M. Parvovirus H-1-induced tumor cell death enhances human immune response in vitro via increased phagocytosis, maturation, and cross-presentation by dendritic cells. Hum. Gene Ther. 2005, 16(8):996-1005.
63. Momoeda M., Wong S., Kawase M., Young N.S., Kajigaya S. A putative nucleoside triphosphate-binding domain in the nonstructural protein of B19 parvovirus is required for cytotoxicity. J. Virol. 1994, 68(12):8443-8446.
64. Mueller A., Meiser A., McDonagh E.M., Fox J.M., Petit S.J., Xanthou G., Williams T.J., Pease J.E. CXCL4-induced migration of activated T lymphocytes is mediated by the chemokine receptor CXCR3. J. Leukoc. Biol. 2008, 83(4):875-882.
65. Narvaiza I., Mazzolini G., Barajas M., Duarte M., Zaratiegui M., Qian C., Melero I., Prieto J. Intratumoral coinjection of two adenoviruses, one encoding the chemokine IFN-gamma-inducible protein-10 and another encoding IL-12, results in marked antitumoral synergy. J. Immunol. 2000, 164(6):3112-3122.
66. Nuesch J.P., Bar S., Rommelaere J. Viral proteins killing tumor cells: new weapons in the fight against cancer. Cancer Biol. Ther. 2008, 7(9):1374-1376.
67. Nuesch J.P., Lacroix J., Marchini A., Rommelaere J. Molecular pathways: rodent parvoviruses-mechanisms of oncolysis and prospects for clinical cancer treatment. Clin. Cancer Res. 2012, 18(13):3516-3523.
68. Pages G., Pouyssegur J. Transcriptional regulation of the vascular endothelial growth factor gene-a concert of activating factors. Cardiovasc. Res. 2005, 65(3):564-573.
69. Rommelaere J., Cornelis J.J. Antineoplastic activity of parvoviruses. J. Virol. Methods 1991, 33(3):233-251.
70. Rommelaere J., Geletneky K., Angelova A.L., Daeffler L., Dinsart C., Kiprianova I., Schlehofer J.R., Raykov Z. Oncolytic parvoviruses as cancer therapeutics. Cytokine Growth Factor Rev. 2010, 21(2-3):185-195.
71. Rosewicz S., Detjen K., Scholz A., von Marschall Z. Interferon-alpha: regulatory effects on cell cycle and angiogenesis. Neuroendocrinology 2004, 80(Suppl. 1):85-93.
72. Rubenstein J.L., Kim J., Ozawa T., Zhang M., Westphal M., Deen D.F., Shuman M.A. Anti-VEGF antibody treatment of glioblastoma prolongs survival but results in increased vascular cooption. Neoplasia 2000, 2(4):306-314.
73. Sato E., Fujimoto J., Toyoki H., Sakaguchi H., Alam S.M., Jahan I., Tamaya T. Expression of IP-10 related to angiogenesis in uterine cervical cancers. Br. J. Cancer 2007, 96(11):1735-1739.
74. Sieben M., Schafer P., Dinsart C., Galle P.R., Moehler M. Activation of the human immune system via toll-like receptors by the oncolytic parvovirus H-1. Int. J. Cancer 2012, 132(11):2548-2556.
75. Siegl G Biology and pathogenicity of autonomous parvoviruses. The Parvoviruses 1984, 297-362. Plenum Publishing Corp., New York. K.I. B. (Ed.).
76. Soda Y., Myskiw C., Rommel A., Verma I.M. Mechanisms of neovascularization and resistance to anti-angiogenic therapies in glioblastoma multiforme. J. Mol. Med. (Berlin) 2013, 91(4):439-448.
77. Sodhi A., Montaner S., Patel V., Zohar M., Bais C., Mesri E.A., Gutkind J.S. The Kaposi's sarcoma-associated herpes virus G protein-coupled receptor up-regulates vascular endothelial growth factor expression and secretion through mitogen-activated protein kinase and p38 pathways acting on hypoxia-inducible factor 1alpha. Cancer Res. 2000, 60(17):4873-4880.
78. Strieter R.M., Burdick M.D., Gomperts B.N., Belperio J.A., Keane M.P. CXC chemokines in angiogenesis. Cytokine Growth Factor Rev. 2005, 16(6):593-609.
79. Strieter R.M., Polverini P.J., Kunkel S.L., Arenberg D.A., Burdick M.D., Kasper J., Dzuiba J., Van Damme J., Walz A., Marriott D., et al. The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J. Biol. Chem. 1995, 270(45):27348-27357.
80. Struyf S., Burdick M.D., Peeters E., Van den Broeck K., Dillen C., Proost P., Van Damme J., Strieter R.M. Platelet factor-4 variant chemokine CXCL4L1 inhibits melanoma and lung carcinoma growth and metastasis by preventing angiogenesis. Cancer Res. 2007, 67(12):5940-5948.
81. Struyf S., Burdick M.D., Proost P., Van Damme J., Strieter R.M. Platelets release CXCL4L1, a nonallelic variant of the chemokine platelet factor-4/CXCL4 and potent inhibitor of angiogenesis. Circ. Res. 2004, 95(9):855-857.
82. Struyf S., Salogni L., Burdick M.D., Vandercappellen J., Gouwy M., Noppen S., Proost P., Opdenakker G., Parmentier M., Gerard C., Sozzani S., Strieter R.M., Van Damme J. Angiostatic and chemotactic activities of the CXC chemokine CXCL4L1 (platelet factor-4 variant) are mediated by CXCR3. Blood 2011, 117(2):480-488.
83. Tattersall P., Bratton J. Reciprocal productive and restrictive virus-cell interactions of immunosuppressive and prototype strains of minute virus of mice. J. Virol. 1983, 46(3):944-955.
84. Taub D.D., Lloyd A.R., Conlon K., Wang J.M., Ortaldo J.R., Harada A., Matsushima K., Kelvin D.J., Oppenheim J.J. Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells. J. Exp. Med. 1993, 177(6):1809-1814.
85. Vandercappellen J., Noppen S., Verbeke H., Put W., Conings R., Gouwy M., Schutyser E., Proost P., Sciot R., Geboes K., Opdenakker G., Van Damme J., Struyf S. Stimulation of angiostatic platelet factor-4 variant (CXCL4L1/PF-4var) versus inhibition of angiogenic granulocyte chemotactic protein-2 (CXCL6/GCP-2) in normal and tumoral mesenchymal cells. J. Leukoc. Biol. 2007, 82(6):1519-1530.
86. Vandercappellen J., Van Damme J., Struyf S. The role of the CXC chemokines platelet factor-4 (CXCL4/PF-4) and its variant (CXCL4L1/PF-4var) in inflammation, angiogenesis and cancer. Cytokine Growth Factor Rev. 2011, 22(1):1-18.
87. Wetzel K., Struyf S., Van Damme J., Kayser T., Vecchi A., Sozzani S., Rommelaere J., Cornelis J.J., Dinsart C. MCP-3 (CCL7) delivered by parvovirus MVMp reduces tumorigenicity of mouse melanoma cells through activation of T lymphocytes and NK cells. Int. J. Cancer 2007, 120(6):1364-1371.
88. Wrzesinski C., Tesfay L., Salome N., Jauniaux J.C., Rommelaere J., Cornelis J., Dinsart C. Chimeric and pseudotyped parvoviruses minimize the contamination of recombinant stocks with replication-competent viruses and identify a DNA sequence that restricts parvovirus H-1 in mouse cells. J. Virol. 2003, 77(6):3851-3858.
89. Wu Q., Dhir R., Wells A. Altered CXCR3 isoform expression regulates prostate cancer cell migration and invasion. Mol. Cancer 2012, 11:3.
90. Zadori Z., Szelei J., Tijssen P. SAT: a late NS protein of porcine parvovirus. J. Virol. 2005, 79(20):13129-13138.
91. Zipin-Roitman A., Meshel T., Sagi-Assif O., Shalmon B., Avivi C., Pfeffer R.M., Witz I.P., Ben-Baruch A. CXCL10 promotes invasion-related properties in human colorectal carcinoma cells. Cancer Res. 2007, 67(7):3396-3405.