Sequential gene profiling of basal cell carcinomas treated with imiquimod in a placebo-controlled study defines the requirements for tissue rejection

Genome Biology

Volumn 8, Issue 1, 2007, Pages

  Panelli, Monica C ^a   Stashower, Mitchell E ^b   Slade, Herbert B ^c   Smith, Kina ^a   Norwood, Christopher ^d   Abati, Andrea ^e   Fetsch, Patricia ^e   Filie, Armando ^e   Walters, Shelley Ann ^c   Astry, Calvin ^c   Aricó, Eleonora ^a   Zhao, Yingdong ^e   Selleri, Silvia ^a,f   Wang, Ena ^a   Marincola, Francesco M ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b The Clinical Skin Center of Northern Virginia   (United States)

^c 3M COMPANY   (United States)

^d WALTER REED ARMY MEDICAL CENTER   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; IMIQUIMOD; PLACEBO; RNA; AMINOQUINOLINE DERIVATIVE; ANTINEOPLASTIC AGENT; CD56 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; MESSENGER RNA;

ADAPTIVE IMMUNITY; ARTICLE; BASAL CELL CARCINOMA; CELLULAR IMMUNITY; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CREAM; DOSAGE SCHEDULE COMPARISON; DOUBLE BLIND PROCEDURE; DRUG DOSE REGIMEN; DRUG EFFICACY; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; INNATE IMMUNITY; PATIENT COMPLIANCE; PUNCH BIOPSY; RANDOMIZED CONTROLLED TRIAL; RNA HYBRIDIZATION; TUMOR IMMUNITY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; POLYMERASE CHAIN REACTION; TUMOR GENE;

AMINOQUINOLINES; ANTIGENS, CD56; ANTIGENS, CD8; ANTINEOPLASTIC AGENTS; CARCINOMA, BASAL CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, NEOPLASM; HUMANS; INTERFERON TYPE II; INTERFERON-ALPHA; PLACEBOS; POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 33847646901     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2007-8-1-r8     Document Type: Article

References (71)

1. Schulze HJ Cribier B Requena L Reifenberger J Ferrandiz C Garcia Diez A Tebbs V McRae S Imiquimod 5% cream for the treatment of superficial basal cell carcinoma: Results from a randomized vehicle-controlled phase III study in Europe. Br J Dermatol 2005 152 939-947 10.1111/ j.1365-2133.2005.06486.x 15888150
2. National Cancer Institute: Drug Information Summaries http://www.cancer.gov/clinicaltrials/developments/ newly-approved-treatments
3. Stockfleth E Trefzer U Garcia-Bartels C Wegner T Schmook T Sterry W The use of Toll-like receptor-7 agonist in the treatment of basal cell carcinoma: An overview. Br J Dermatol 2003 149 Suppl 66 53-56 10.1046/ j.0366-077X.2003.05626.x 14616352
4. Urosevic M Maier T Benninghoff B Slade H Burg G Dummer R Mechanisms unerlying imiquimod-induced regression of basal cell carcinoma in vivo. Arch Dermatol 2003 139 1325-1332 10.1001/archderm.139.10.1325 14568837
5. Stanley MA Imiquimod and the imidazoquinolones: Mechanism of action and therapeutic potential. Clin Exp Dermatol 2002 27 571-577 10.1046/ j.1365-2230.2002.01151.x 12464152
6. Naylor MF Crowson N Kuwahara R Teague K Garcia C Mackinnis C Haque R Odom C Jankey C Cornelison RL Treatment of lentigo maligna with topical imiquimod. Br J Dermatol 2003 149 Suppl 66 66-70 10.1046/ j.0366-077X.2003.05637.x 14616356
7. Ray CM Kluk M Grin CM Grant-Kels JM Successful treatment of malignant melanoma in situ with topical 5% imiquimod cream. Int J Dermatol 2005 44 428-434 10.1111/j.1365-4632.2005.02582.x 15869545
8. Hurwitz DJ Pincus L Kupper TS Imiquimod: A topically applied link between innate and acquired immunity. Arch Dermatol 2003 139 1347-1350 10.1001/archderm.139.10.1347 14568839
9. Majewski S Marczak M Mlynarczyk B Benninghoff B Jablonska S Imiquimod is a strong inhibitor of tumor cell-induced angiogenesis. Int J Dermatol 2005 44 14-19 10.1111/j.1365-4632.2004.02318.x 15663652
10. KEGG PATHWAY Database http://www.genome.ad.jp/kegg/pathway.html
11. Stroncek DF Basil C Nagorsen D Deola S Arico E Smith K Wang E Marincola FM Panelli MC Delayed polarization of mononuclear phagocyte transcriptional program by type I interferon isoforms. J Transl Med 2005 3 24 1187927 15953390 10.1186/1479-5876-3-24
12. KEGG: Toll-like Receptor Signaling Pathways http://www.genome.jp/ dbget-bin/www_bget?path:hSa04620
13. van Spriel AB Puls KL Sofi M Pouniotis D Hochrein H Orinska Z Knobeloch KP Plebanski M Wright MD A regulatory role for CD37 in T cell proliferation. J Immunol 2004 172 2953-2961 14978098
14. Jin P Wang E Provenzano M Deola S Selleri S Voiculescu S Stroncek DF Panelli MC Marincola FM Molecular signatures induced by interleukin-2 on peripheral blood mononuclear cells and T cell subsets. J Transl Med 2006 4 26 1557669 16805915 10.1186/1479-5876-4-26
15. Schluns KS Stoklasek T Lefrancois L The roles of interleukin-15 receptor alpha: Trans-presentation, receptor component, or both? Int J Biochem Cell Biol 2005 37 1567-1571 10.1016/j.biocel.2005.02.017 15896666
16. Zambricki E Shigeoka A Kishimoto H Sprent J Burakoff S Carpenter C Milford E McKay D Signaling T-cell survival and death by IL-2 and IL-15. Am J Transplant 2005 5 2623-2631 10.1111/j.1600-6143.2005.01075.x 16212621
17. Sanchez-Sanchez N Riol-Blanco L de la Rosa G Puig-Kroger A Garcia-Bordas J Martin D Longo N Cuadrado A Cabanas C Corbi AL et al. Chemokine receptor CCR7 induces intracellular signaling that inhibits apoptosis of mature dendritic cells. Blood 2004 104 619-625 10.1182/ blood-2003-11-3943 15059845
18. Fernandez N Renedo M Garcia-Rodriguez C Sanchez Crespo M Activation of monocytic cells through Fc gamma receptors induces the expression of macrophage-inflammatory protein (MIP)-1 alpha, MIP-1 beta, and RANTES. J Immunol 2002 169 3321-3328 12218153
19. Bade B Boettcher HE Lohrmann J Hink-Schauer C Bratke K Jenne DE Virchow JC Jr Luttmann W Differential expression of the granzymes A, K and M and perforin in human peripheral blood lymphocytes. Int Immunol 2005 17 1419-1428 10.1093/intimm/dxh320 16186162
20. Adrain C Murphy BM Martin SJ Molecular ordering of the caspase activation cascade initiated by the cytotoxic T lymphocyte/natural killer (CTL/NK) protease granzyme B. J Biol Chem 2005 280 4663-4673 10.1074/jbc.M410915200 15569669
21. Veugelers K Motyka B Frantz C Shostak I Sawchuk T Bleackley RC The granzyme B-serglycin complex from cytotoxic granules requires dynamin for endocytosis. Blood 2004 103 3845-3853 10.1182/blood-2003-06-2156 14739229
22. Brossard C Semichon M Trautmann A Bismuth G CD5 inhibits signaling at the immunological synapse without impairing its formation. J Immunol 2003 170 4623-4629 12707340
23. Choudhuri K Kearney A Bakker TR van der Merwe PA Immunology: How do T cells recognize antigen? Curr Biol 2005 15 R382-R385 10.1016/ j.cub.2005.05.001 15916940
24. Hahn WC Menu E Bothwell AL Sims PJ Bierer BE Overlapping but nonidentical binding sites on CD2 for CD58 and a second ligand CD59. Science 1992 256 1805-1807 10.1126/science.1377404 1377404
25. Badour K Zhang J Siminovitch KA The Wiskott-Aldrich syndrome protein: forging the link between actin and cell activation. Immunol Rev 2003 192 98-112 10.1034/j.1600-065X.2003.00031.x 12670398
26. Posselt AM Vincenti F Bedolli M Lantz M Roberts JP Hirose R CD69 expression on peripheral CD8 T cells correlates with acute rejection in renal transplant recipients. Transplantation 2003 76 190-195 10.1097/ 01.TP.0000073614.29680.A8 12865808
27. Lanier LL NK cell recognition. Annu Rev Immunol 2005 23 225-274 10.1146/ annurev.immunol.23.021704.115526 15771571
28. Wex T Buhling F Wex H Gunther D Malfertheiner P Weber E Bromme D Human cathepsin W, a cysteine protease predominantly expressed in NK cells, is mainly localized in the endoplasmic reticulum. J Immunol 2001 167 2172-2178 11490002
29. Fujii N Hiraki A Ikeda K Ohmura Y Nozaki I Shinagawa K Ishimaru F Kiura K Shimizu N Tanimoto M Harada M Expression of minor histocompatibility antigen, HA-1, in solid tumor cells. Transplantation 2002 73 1137-1141 10.1097/00007890-200204150-00022 11965046
30. Sullivan TP Dearaujo T Vincek V Berman B Evaluation of superficial basal cell carcinomas after treatment with imiquimod 5% cream or vehicle for apoptosis and lymphocyte phenotyping. Dermatol Surg 2003 29 1181-1186 10.1111/j.1524-4725.2003.29399.x 14725659
31. Iwasaki A Medzhitov R Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004 5 987-995 10.1038/ni1112 15454922
32. Hemmi H Kaisho T Takeuchi O Sato S Sanjo H Hoshino K Horiuchi T Tomizawa H Takeda K Akira S Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002 3 196-200 10.1038/ni758 11812998
33. Chan CW Crafton E Fan HN Flook J Yoshimura K Skarica M Brockstedt D Dubensky TW Stins MF Lanier LL Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nat Med 2006 12 207-213 10.1038/nm1352 16444266
34. Marincola FM Wang E Herlyn M Seliger B Ferrone S Tumors as elusive targets of T cell-directed immunotherapy. Trends Immunol 2003 24 335-342 10.1016/S1471-4906(03)00116-9 12810110
35. Bowen DG Walker CM Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 2005 436 946-952 10.1038/nature04079 16107834
36. Smith MW Yue ZN Korth MJ Do HA Boix L Fausto N Bruix J Carithers RL Jr Katze MG Hepatitis C virus and liver disease: Global transcriptional profiling and identification of potential markers. Hepatology 2003 38 1458-1467 14647057
37. Sarwal M Chua MS Kambham N Hsieh SC Satterwhite T Masek M Slavatierra O Jr Molecular heterogeneity in acute renal allograft rejection identified by DNA microarray profiling. N Engl J Med 2003 349 125-138 10.1056/ NEJMoa035588 12853585
38. Panelli MC Wang E Phan G Puhlman M Miller L Ohnmacht GA Klein H Marincola FM Genetic profiling of peripheral mononuclear cells and melanoma metastases in response to systemic interleukin-2 administration. Genome Biol 2002 3 RESEARCH0035 126240 12184809 10.1186/ gb-2002-3-7-research0035
39. Kim SH Han SY Azam T Yoon DY Dinarello CA Interleukin-32: A cytokine and inducer of TNFalpha. Immunity 2005 22 131-142 15664165
40. Hicks AM Riedlinger G Willingham MC Alexander-Miller MA von Kap-Herr C Pettenati MJ Sanders AM Weir HM Du W Kim J et al. Transferable anticancer innate immunity in spontaneous regression/complete resistance mice. Proc Natl Acad Sci USA 2006 103 7753-7758 1458507 16682640 10.1073/ pnas.0602382103
41. Wang E Miller LD Ohnmacht GA Liu ET Marincola FM High fidelity mRNA amplification for gene profiling. Nat Biotechnol 2000 18 457-459 10.1038/ 74546 10748532
42. Netea MG Azam T Ferwerda G Girardin SE Walsh M Park JS Abraham E Kim JM Yoon DY Dinarello CA Kim SH IL-32 synergizes with nucleotide oligomerization domain (NOD) 1 and NOD2 ligands for IL-1beta and IL-6 production through a caspase 1-dependent mechanism. Proc Natl Acad Sci USA 2005 102 16309-16314 1283464 16260731 10.1073/pnas.0508237102
43. Monsurro V Wang E Yamano Y Migueles SA Panelli MC Smith K Nagorsen D Connors M Jacobson S Marincola FM Quiescent phenotype of tumor-specific CD8+ T cells following immunization. Blood 2004 104 1970-1978 10.1182/ blood-2004-02-0525 15187028
44. Wang E Panelli MC Zavaglia K Mandruzzato S Hu N Taylor PR Seliger B Zanovello P Freedman RS Marincola FM Melanoma-restricted genes. J Transl Med 2004 2 34 527872 15488140 10.1186/1479-5876-2-34
45. Richwald GA Imiquimod. Drugs Today (Barc) 1999 35 497-511 12973395
46. Dahl MV Imiquimod: A cytokine inducer. J Am Acad Dermatol 2002 47 S205-S208 10.1067/mjd.2002.126586 12271278
47. Matzinger P Introduction to the series. Danger model of immunity. Scand J Immunol 2001 54 2-3 10.1046/j.1365-3083.2001.00973.x 11439141
48. Panelli MC Riker A Kammula U Wang E Lee KH Rosenberg SA Marincola FM Expansion of tumor-T cell pairs from fine needle aspirates of melanoma metastases. J Immunol 2000 164 495-504 10605047
49. Kammula US Marincola FM Rosenberg SA Real-time quantitative polymerase chain reaction assessment of immune reactivity in melanoma patients after tumor peptide vaccination. J Natl Cancer Inst 2000 92 1336-1344 10.1093/jnci/92.16.1336 10944556
50. Fuchs EJ Matzinger P Is cancer dangerous to the immune system? Semin Immunol 1996 8 271-280 10.1006/smim.1996.0035 8956455
51. Monsurro V Wang E Panelli MC Nagorsen D Jin P Katia Z Smith K Ngalame Y Even J Marincola FM Active-specific immunization against melanoma: Is the problem at the receiving end? Sem Cancer Biol 2003 13 473-480 10.1016/j.semcancer.2003.09.011
52. Marincola FM A balanced review of the status of T cell-based therapy against cancer. J Transl Med 2005 3 16 1090619 15831096 10.1186/ 1479-5876-3-16
53. Urosevic M Dummer R Conrad C Beyeler M Laine E Burg G Giliet M Disease-independent skin recruitment and activation of plasmacytoid predendritic cells following imiquimod treatment. J Natl Cancer Inst 2005 97 1143-1153 16077073
54. Torres A Storey L Anders M Miller RL Bulbulian BJ Jin J Raghavan S Lee J Slade HB Birmachu W Immune-mediated changes in actinic Keratosis following topical treatment with Imiquimod 5% cream. J Transl Med 2007 17257431
55. Rechtsteiner G Warger T Osterloh P Schild H Radsak MP Cutting edge: priming of CTL by transcutaneous peptide immunization with imiquimod. J Immunol 2005 174 2476-2480 15728450
56. Wenzel J Uerlich M Haller O Bieber T Tueting T Enhanced type I interferon signaling and recruitment of chemokine receptor CXCR3-expressing lymphocytes into the skin following treatment with the TLR7-agonist imiquimod. J Cutan Pathol 2005 32 257-262 10.1111/ j.0303-6987.2005.00297.x 15769273
57. Craft N Bruhn KW Nguyen BD Prins R Lin JW Liau LM Miller JF The TLR7 agonist imiquimod enhances the anti-melanoma effects of a recombinant Listeria monocytogenes vaccine. J Immunol 2005 175 1983-1990 16034143
58. Wang E Marincola FM Amplification of small quantities of mRNA for transcript analysis. In DNA arrays: A Molecular Cloning Manual Cold Springs Harbor, NY: Cold Spring Harbor Laboratory Press Bowtell D, Sambrook J 2002 204-213
59. Wang E RNA amplification for successful gene profiling analysis. J Transl Med 2005 3 28 1201175 16042807 10.1186/1479-5876-3-28
60. National Cancer Institute, Center for Cancer Research: MAdb GAL Files (Hs-CCDTM17 5 k-1px gal) http://nciarray.nci.nih.gov/gal_files/ gal_custom_current.shtml
61. Eisen MB Spellman PT Brown PO Botstein D Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998 95 14863-14868 24541 9843981 10.1073/pnas.95.25.14863
62. Ross DT Scherf U Eisen MB Perou CM Rees CA Spellman PT Iyer V Jeffrey SS van de Rijn M Waltham M et al. Systematic variation in gene expression patterns in human cancer cell lines. Nature Genetics 2000 24 227-235 10.1038/73432 10700174
63. DAVID Bioinformatics Resource 2006 http://david.abcc.ncifcrf.gov/
64. GeneCards Database http://www.genecards.org/index.shtml
65. COPE: Cytokines and Cells Online Pathfinder Encyclopedia http://www.copewithcytokines.de
66. Bioinformatic Harvester Database http://harvester.embl.de/harvester/P599/ P59901.htm
67. Biomedical Research Support Facilities, University of Pittsburgh http://www.pitt.edu/~rsup/OligoCalc.html
68. Livak KJ Schmittgen TD Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001 25 402-408 10.1006/meth.2001.1262 11846609
69. National Cancer Institute, Biometric Research Branch: BRB Array Tools http://linus.nci.nih.gov/BRB-ArrayTools.html
70. Simon R Lam A LI MC Ngan M Menenzes S Zhao Y Analysis of gene expression data using BRB-Array Tools. Cancer Informatics 2007 in press
71. NCBI: Gene Expression Omnibus (GEO) http://www.ncbi.nlm.nih.gov/geo/