An inhibitor of cyclin-dependent kinases suppresses TLR signaling and increases the susceptibility of cancer patients to herpes viridae

Cell Cycle

Volumn 10, Issue 1, 2011, Pages 118-126

  Zoubir, Mustapha ^a,b,c   Flament, Caroline ^a,b,c   Gdoura, Abdelaziz ^b,c   Bahleda, Rastilav ^b,c   Litvinova, Elena ^a,b,c   Soumelis, Vassili ^d,e   Conforti, Rosa ^a,b,c   Viaud, Sophie ^a,b,c   Soria, Jean Charles ^b,c   Kroemer, Guido ^b,f,g,h   Zitvogel, Laurence ^a,b,c   Chaput, Nathalie ^a,b  

^a INSERM   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d PSL RESEARCH UNIVERSITY   (France)

^e INSTITUT CURIE   (France)

^f CENTRE DE RECHERCHE DES CORDELIERS   (France)

^g HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^h UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Cancer; CDK inhibitors; Dendritic cells; Herpes; TLR

Indexed keywords

CYCLIN DEPENDENT KINASE 2 INHIBITOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; PHA 793887; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; [N [6,6 DIMETHYL 5 [(1 METHYLPIPERIDIN 4 YL)CARBONYL] 2,4,5,6 TETRAHYDROPYRROLO[3,4 C]PYRAZOL 3 YL] 3 METHYLBUTANAMIDE];

ADULT; ADVANCED CANCER; AGED; ARTICLE; CANCER PATIENT; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DRUG DOSE ESCALATION; EUROPE; FEMALE; HERPES SIMPLEX; HERPES VIRUS; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; MALE; NATURAL KILLER CELL; PAPULOVESICULAR RASH; PHASE 1 CLINICAL TRIAL; SIDE EFFECT; VIRUS REPLICATION;

HERPES; HERPESVIRIDAE;

EID: 78650813167     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.1.14445     Document Type: Article

References (62)

1. Malumbres M, Barbacid M. Cell cycle, CDKs and cancer: A changing paradigm. Nat Rev Cancer 2009; 9:153-66.
2. Malumbres M, Barbacid M. To cycle or not to cycle: a critical decision in cancer. Nat Rev Cancer 2001; 1:222-31.
3. Malumbres M, Barbacid M. Mammalian cyclin-dependent kinases. Trends Biochem Sci 2005; 30:630-41.
4. Ortega S, Malumbres M, Barbacid M. Cyclin D-dependent kinases, INK4 inhibitors and cancer. Biochim Biophys Acta 2002; 1602:73-87.
5. Aleem E, Kiyokawa H, Kaldis P. Cdc2-cyclin E complexes regulate the G1/S phase transition. Nat Cell Biol 2005; 7:831-6.
6. Martin A, Odajima J, Hunt SL, Dubus P, Ortega S, Malumbres M, et al. Cdk2 is dispensable for cell cycle inhibition and tumor suppression mediated by p27(Kip1) and p21(Cip1). Cancer Cell 2005; 7:591-8.
7. Malumbres M, Pevarello P, Barbacid M, Bischoff JR. CDK inhibitors in cancer therapy: What is next? Trends Pharmacol Sci 2008; 29:16-21.
8. Shapiro GI. Cyclin-dependent kinase pathways as targets for cancer treatment. J Clin Oncol 2006; 24:1770-83.
9. Malumbres M, Sotillo R, Santamaria D, Galan J, Cerezo A, Ortega S, et al. Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Cell 2004; 118:493-504. (Pubitemid 39485668)
10. Larochelle S, Merrick KA, Terret ME, Wohlbold L, Barboza NM, Zhang C, et al. Requirements for Cdk7 in the assembly of Cdk1/cyclin B and activation of Cdk2 revealed by chemical genetics in human cells. Mol Cell 2007; 25:839-50. (Pubitemid 46442792)
11. Li CJ, Vassilev A, DePamphilis ML. Role for Cdk1 (Cdc2)/cyclin A in preventing the mammalian origin recognition complex's largest subunit (Orc1) from binding to chromatin during mitosis. Mol Cell Biol 2004; 24:5875-86. (Pubitemid 38787972)
12. Brasca MG, Albanese C, Alzani R, Amici R, Avanzi N, Ballinari D, et al. Optimization of 6,6-dimethyl pyrrolo[3,4-c]pyrazoles: Identification of PHA-793887, a potent CDK inhibitor suitable for intravenous dosing. Bioorganic & medicinal chemistry 18:1844-53.
13. Massard C, Soria J, Anthoney D, Proctor A, Scaburri A, Pacciarini M, et al. A first in man, dose-escalation study of PHA-793887 administered as a 1 hour IV infusion on days 1, 8 and 15 of a 4 week cycle in patients with advanced/metastatic solid tumors. Companion paper.
14. Advani SJ, Weichselbaum RR, Roizman B. The role of cdc2 in the expression of herpes simplex virus genes. Proc Natl Acad Sci USA 2000; 97:10996-1001.
15. Hossain A, Holt T, Ciacci-Zanella J, Jones C. Analysis of cyclin-dependent kinase activity after herpes simplex virus type 2 infection. J Gen Virol 1997; 78:3341-8.
16. Schang LM. Cyclin-dependent kinases as cellular targets for antiviral drugs. J Antimicrob Chemother 2002; 50:779-92.
17. Schang LM. The cell cycle, cyclin-dependent kinases and viral infections: new horizons and unexpected connections. Prog Cell Cycle Res 2003; 5:103-24.
18. Schang LM, Bantly A, Knockaert M, Shaheen F, Meijer L, Malim MH, et al. Pharmacological cyclin-dependent kinase inhibitors inhibit replication of wild-type and drug-resistant strains of herpes simplex virus and human immunodeficiency virus type 1 by targeting cellular, not viral, proteins. J Virol 2002; 76:7874-82.
19. Schang LM, Bantly A, Schaffer PA. Explant-induced reactivation of herpes simplex virus occurs in neurons expressing nuclear cdk2 and cdk4. J Virol 2002; 76:7724-35.
20. Schang LM, Phillips J, Schaffer PA. Requirement for cellular cyclin-dependent kinases in herpes simplex virus replication and transcription. J Virol 1998; 72:5626-37.
21. Schang LM, Rosenberg A, Schaffer PA. Roscovitine, a specific inhibitor of cellular cyclin-dependent kinases, inhibits herpes simplex virus DNA synthesis in the presence of viral early proteins. J Virol 2000; 74:2107-20.
22. Hazeki K, Nigorikawa K, Hazeki O. Role of phosphoinositide 3-kinase in innate immunity. Biol Pharm Bull 2007; 30:1617-23.
23. Jiang A, Bloom O, Ono S, Cui W, Unternaehrer J, Jiang S, et al. Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 2007; 27:610-24. (Pubitemid 47615505)
24. Martin M, Rehani K, Jope RS, Michalek SM. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat Immunol 2005; 6:777-84. (Pubitemid 43090463)
25. Ohtani M, Nagai S, Kondo S, Mizuno S, Nakamura K, Tanabe M, et al. Mammalian target of rapamycin and glycogen synthase kinase 3 differentially regulate lipopolysaccharide-induced interleukin-12 production in dendritic cells. Blood 2008; 112:635-43.
26. Rehani K, Wang H, Garcia CA, Kinane DF, Martin M. Toll-like receptor-mediated production of IL-1Ra is negatively regulated by GSK3 via the MAPK ERK1/2. J Immunol 2009; 182:547-53.
27. Tachado SD, Li X, Swan K, Patel N, Koziel H. Constitutive activation of phosphatidylinositol-3-kinase signaling pathway downregulates TLR4-mediated tumor necrosis factor-alpha release in alveolar macrophages from asymptomatic HIV-positive persons in vitro. J Biol Chem 2008; 283:33191-8.
28. Wang H, Garcia CA, Rehani K, Cekic C, Alard P, Kinane DF, et al. IFNbeta production by TLR4-stimulated innate immune cells is negatively regulated by GSK3beta. J Immunol 2008; 181:6797-802.
29. Alzani R, Pedrini O, Albanese C, Ceruti R, Casolaro A, Patton V, et al. Therapeutic efficacy of the pan-cdk inhibitor PHA-793887 in vitro and in vivo in engraftment and high-burden leukemia models. Exp Hematol 2010; 38:259-69.
30. Kawai T, Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. International immunology 2009; 21:317-37.
31. Davey GM, Wojtasiak M, Proietto AI, Carbone FR, Heath WR, Bedoui S. Cutting edge: priming of CD8 T cell immunity to herpes simplex virus type 1 requires cognate TLR3 expression in vivo. J Immunol 184:2243-6.
32. Hochrein H, Schlatter B, O'Keeffe M, Wagner C, Schmitz F, Schiemann M, et al. Herpes simplex virus type-1 induces IFNalpha production via Toll-like receptor 9-dependent and -independent pathways. Proc Natl Acad Sci USA 2004; 101:11416-21.
33. Sato A, Linehan MM, Iwasaki A. Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc Natl Acad Sci USA 2006; 103:17343-8.
34. Sorensen LN, Reinert LS, Malmgaard L, Bartholdy C, Thomsen AR, Paludan SR. TLR2 and TLR9 synergistically control herpes simplex virus infection in the brain. J Immunol 2008; 181:8604-12.
35. Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, Suter M, et al. Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med 1999; 5:405-11.
36. Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 2007; 26:503-17.
37. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, et al. Induced recruitment of NK cells to lymph nodes provides IFNgamma for T(H)1 priming. Nat Immunol 2004; 5:1260-5.
38. Koelle DM, Corey L. Recent progress in herpes simplex virus immunobiology and vaccine research. Clinical microbiology reviews 2003; 16:96-113.
39. Nandakumar S, Woolard SN, Yuan D, Rouse BT, Kumaraguru U. Natural killer cells as novel helpers in anti-herpes simplex virus immune response. J Virol 2008; 82:10820-31. (Pubitemid 352691159)
40. Pereira RA, Scalzo A, Simmons A. Cutting edge: a NK complex-linked locus governs acute versus latent herpes simplex virus infection of neurons. J Immunol 2001; 166:5869-73.
41. Grubor-Bauk B, Simmons A, Mayrhofer G, Speck PG. Impaired clearance of herpes simplex virus type 1 from mice lacking CD1d or NKT cells expressing the semi-variant Valpha 14-Jalpha281 TCR. J Immunol 2003; 170:1430-4.
42. Mikloska Z, Sanna PP, Cunningham AL. Neutralizing antibodies inhibit axonal spread of herpes simplex virus type 1 to epidermal cells in vitro. J Virol 1999; 73:5934-44.
43. Chen YT, Wang YH, Cheng YY, Hung SL. Direct binding of herpes simplex virus type 1 virions to complement C3. Viral Immunol 2003; 16:347-55.
44. Verschoor A, Brockman MA, Gadjeva M, Knipe DM, Carroll MC. Myeloid C3 determines induction of humoral responses to peripheral herpes simplex virus infection. J Immunol 2003; 171:5363-71.
45. + T cells are selectively activated and retained in latently infected sensory ganglia. Immunity 2003; 18:593-603.
46. Mueller SN, Jones CM, Smith CM, Heath WR, Carbone FR. Rapid cytotoxic T lymphocyte activation occurs in the draining lymph nodes after cutaneous herpes simplex virus infection as a result of early antigen presentation and not the presence of virus. J Exp Med 2002; 195:651-6.
47. + T cells can clear established lytic infections from skin and nerves and can partially limit the early spread of virus after cutaneous inoculation. J Immunol 2004; 172:392-7.
48. Vollstedt S, Franchini M, Hefti HP, Odermatt B, O'Keeffe M, Alber G, et al. Flt3 ligand-treated neonatal mice have increased innate immunity against intracellular pathogens and efficiently control virus infections. J Exp Med 2003; 197:575-84.
49. Mark KE, Wald A, Magaret AS, Selke S, Olin L, Huang ML, et al. Rapidly cleared episodes of herpes simplex virus reactivation in immunocompetent adults. J Infect Dis 2008; 198:1141-9.
50. Lund J, Sato A, Akira S, Medzhitov R, Iwasaki A. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J Exp Med 2003; 198:513-20.
51. Diebold SS, Montoya M, Unger H, Alexopoulou L, Roy P, Haswell LE, et al. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 2003; 424:324-8.
52. Novak N, Peng WM. Dancing with the enemy: The interplay of herpes simplex virus with dendritic cells. Clin Exp Immunol 2005; 142:405-10. (Pubitemid 41719834)
53. Reske A, Pollara G, Krummenacher C, Katz DR, Chain BM. Glycoprotein-dependent and TLR2-independent innate immune recognition of herpes simplex virus-1 by dendritic cells. J Immunol 2008; 180:7525-36.
54. + dendritic cells. Nat Immunol 2009; 10:488-95.
55. Zhang SY, Jouanguy E, Ugolini S, Smahi A, Elain G, Romero P, et al. TLR3 deficiency in patients with herpes simplex encephalitis. Science (New York, NY) 2007; 317:1522-7.
56. Monick MM, Mallampalli RK, Carter AB, Flaherty DM, McCoy D, Robeff PK, et al. Ceramide regulates lipopolysaccharide-induced phosphatidylinositol-3-kinase and Akt activity in human alveolar macrophages. J Immunol 2001; 167:5977-85.
57. Fukao T, Tanabe M, Terauchi Y, Ota T, Matsuda S, Asano T, et al. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat Immunol 2002; 3:875-81.
58. Martin M, Schifferle RE, Cuesta N, Vogel SN, Katz J, Michalek SM. Role of the phosphatidylinositol 3 kinase-Akt pathway in the regulation of IL-10 and IL-12 by Porphyromonas gingivalis lipopolysaccharide. J Immunol 2003; 171:717-25.
59. Hu X, Paik PK, Chen J, Yarilina A, Kockeritz L, Lu TT, et al. IFNgamma suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1 proteins. Immunity 2006; 24:563-74.
60. Hasan UA, Trinchieri G, Vlach J. Toll-like receptor signaling stimulates cell cycle entry and progression in fibroblasts. J Biol Chem 2005; 280:20620-7.
61. Hasan UA, Caux C, Perrot I, Doffin AC, Menetrier-Caux C, Trinchieri G, et al. Cell proliferation and survival induced by Toll-like receptors is antagonized by type I IFNs. Proc Natl Acad Sci USA 2007; 104:8047-52.
62. Xu L, Wang C, Wen Z, Yao X, Liu Z, Li Q, et al. Selective upregulation of CDK2 is critical for TLR9 signaling stimulated proliferation of human lung cancer cell. Immunol Lett 2010; 127:93-9.