Home LiteratureArticle Details
PMID: 15753302 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination.

De Santo C, Serafini P, Marigo I, Dolcetti L, Bolla M, Del Soldato P, Melani C, Guiducci C, Colombo MP, Iezzi M, Musiani P, Zanovello P, Bronte V

Abstract

Active suppression of tumor-specific T lymphocytes can limit the immune-mediated destruction of cancer cells. Of the various strategies used by tumors to counteract immune attacks, myeloid suppressors recruited by growing cancers are particularly efficient, often resulting in the induction of systemic T lymphocyte dysfunction. We have previously shown that the mechanism by which myeloid cells from tumor-bearing hosts block immune defense strategies involves two enzymes that metabolize L-arginine: arginase and nitric oxide (NO) synthase. NO-releasing aspirin is a classic aspirin molecule covalently linked to a NO donor group. NO aspirin does not possess direct antitumor activity. However, by interfering with the inhibitory enzymatic activities of myeloid cells, orally administered NO aspirin normalized the immune status of tumor-bearing hosts, increased the number and function of tumor-antigen-specific T lymphocytes, and enhanced the preventive and therapeutic effectiveness of the antitumor immunity elicited by cancer vaccination. Because cancer vaccines and NO aspirin are currently being investigated in independent phase I/II clinical trials, these findings offer a rationale to combine these treatments in subjects with advanced neoplastic diseases.

MeSH Terms
Animals Anti-Inflammatory Agents, Non-Steroidal/pharmacology Aspirin/analogs & derivatives,pharmacology Cancer Vaccines/pharmacology Carrier Proteins Immune System Diseases/drug therapy,immunology Lipocalins Mice Mice, Inbred BALB C Neoplasm Proteins Neoplasms/drug therapy,immunology,mortality Nitric Oxide Synthase/metabolism T-Lymphocytes/drug effects,immunology Time Factors
Chemicals
Anti-Inflammatory Agents, Non-Steroidal Cancer Vaccines Carrier Proteins Lipocalins Neoplasm Proteins Tinagl1 protein, mouse Nitric Oxide Synthase nitroaspirin Aspirin
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
De Santo Carmela
Department of Oncology and Surgical Sciences, Oncology Section, Padua University, 35128 Padua, Italy.
Serafini Paolo
Marigo Ilaria
Dolcetti Luigi
Bolla Manlio
Del Soldato Piero
Melani Cecilia
Guiducci Cristiana
Colombo Mario P
Iezzi Manuela
Musiani Piero
Zanovello Paola
Bronte Vincenzo
References (40)
40 references, click to expand
  1. M-1/M-2 macrophages and the Th1/Th2 paradigm.
    J Immunol. 2000 Jun 15;164(12):6166-73 PMID: 10843666
  2. Chronic treatment with nitric oxide-releasing aspirin reduces plasma low-density lipoprotein oxidation and oxidative stress, arterial oxidation-specific epitopes, and atherogenesis in hypercholesterolemic mice.
    Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12467-70 PMID: 12209007
  3. IL-1 beta converting enzyme is a target for nitric oxide-releasing aspirin: new insights in the antiinflammatory mechanism of nitric oxide-releasing nonsteroidal antiinflammatory drugs.
    J Immunol. 2000 Nov 1;165(9):5245-54 PMID: 11046058
  4. Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells.
    Blood. 2000 Dec 1;96(12):3838-46 PMID: 11090068
  5. IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice.
    J Immunol. 2003 Jan 1;170(1):270-8 PMID: 12496409
  6. Gastrointestinal safety of NO-aspirin (NCX-4016) in healthy human volunteers: a proof of concept endoscopic study.
    Gastroenterology. 2003 Mar;124(3):600-7 PMID: 12612897
  7. L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes.
    J Immunol. 2003 Aug 1;171(3):1232-9 PMID: 12874210
  8. All-trans-retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination.
    Cancer Res. 2003 Aug 1;63(15):4441-9 PMID: 12907617
  9. Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity.
    Blood. 2003 Sep 15;102(6):2138-45 PMID: 12750171
  10. Nitric oxide-donating aspirin inhibits beta-catenin/T cell factor (TCF) signaling in SW480 colon cancer cells by disrupting the nuclear beta-catenin-TCF association.
    Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12584-9 PMID: 14566053
  11. Leukocyte, rather than tumor-produced SPARC, determines stroma and collagen type IV deposition in mammary carcinoma.
    J Exp Med. 2003 Nov 17;198(10):1475-85 PMID: 14610043
  12. Growth inhibition of human colon cancer cells by nitric oxide (NO)-donating aspirin is associated with cyclooxygenase-2 induction and beta-catenin/T-cell factor signaling, nuclear factor-kappaB, and NO synthase 2 inhibition: implications for chemoprevention.
    Cancer Res. 2003 Nov 15;63(22):7613-8 PMID: 14633677
  13. Transforming growth factor-beta production and myeloid cells are an effector mechanism through which CD1d-restricted T cells block cytotoxic T lymphocyte-mediated tumor immunosurveillance: abrogation prevents tumor recurrence.
    J Exp Med. 2003 Dec 1;198(11):1741-52 PMID: 14657224
  14. Effective genetic vaccination with a widely shared endogenous retroviral tumor antigen requires CD40 stimulation during tumor rejection phase.
    J Immunol. 2003 Dec 15;171(12):6396-405 PMID: 14662838
  15. Derangement of immune responses by myeloid suppressor cells.
    Cancer Immunol Immunother. 2004 Feb;53(2):64-72 PMID: 14593498
  16. NO-donating aspirin inhibits intestinal carcinogenesis in Min (APC(Min/+)) mice.
    Biochem Biophys Res Commun. 2004 Jan 16;313(3):784-8 PMID: 14697260
  17. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species.
    J Immunol. 2004 Jan 15;172(2):989-99 PMID: 14707072
  18. Role of immature myeloid Gr-1+ cells in the development of antitumor immunity.
    Cancer Res. 2004 Feb 1;64(3):1130-9 PMID: 14871848
  19. Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses.
    Cancer Res. 2004 Aug 15;64(16):5839-49 PMID: 15313928
  20. Cancer immunotherapy: moving beyond current vaccines.
    Nat Med. 2004 Sep;10(9):909-15 PMID: 15340416
  21. TCR zeta-chain downregulation: curtailing an excessive inflammatory immune response.
    Nat Rev Immunol. 2004 Sep;4(9):675-87 PMID: 15343367
  22. Synergy between T-cell immunity and inhibition of paracrine stimulation causes tumor rejection.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6254-8 PMID: 7603979
  23. Effect of a new non-steroidal anti-inflammatory drug, nitroflurbiprofen, on the expression of inducible nitric oxide synthase in rat neutrophils.
    Br J Pharmacol. 1995 May;115(2):225-6 PMID: 7545516
  24. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages.
    Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6954-8 PMID: 9192673
  25. Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype.
    J Immunol. 1998 Jun 1;160(11):5347-54 PMID: 9605134
  26. Cyclooxygenase-independent chemoprevention with an aspirin derivative in a rat model of colonic adenocarcinoma.
    Life Sci. 1998;62(23):PL 367-73 PMID: 9627095
  27. Apoptotic death of CD8+ T lymphocytes after immunization: induction of a suppressive population of Mac-1+/Gr-1+ cells.
    J Immunol. 1998 Nov 15;161(10):5313-20 PMID: 9820504
  28. Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death.
    J Immunol. 1999 Mar 15;162(6):3356-66 PMID: 10092790
  29. Peroxynitrite: reactive, invasive and enigmatic.
    Curr Opin Chem Biol. 1999 Apr;3(2):226-35 PMID: 10226050
  30. Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation.
    J Immunol. 1999 May 15;162(10):5728-37 PMID: 10229805
  31. Enhanced anti-inflammatory effects of a nitric oxide-releasing derivative of mesalamine in rats.
    Gastroenterology. 1999 Sep;117(3):557-66 PMID: 10464131
  32. Immortalized myeloid suppressor cells trigger apoptosis in antigen-activated T lymphocytes.
    J Immunol. 2000 Dec 15;165(12):6723-30 PMID: 11120790
  33. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer.
    J Immunol. 2001 Jan 1;166(1):678-89 PMID: 11123353
  34. Therapeutic tumor immunity induced by polyimmunization with melanoma antigens gp100 and TRP-2.
    Cancer Res. 2001 Feb 1;61(3):859-63 PMID: 11221870
  35. Effects of nitric oxide-releasing aspirin versus aspirin on restenosis in hypercholesterolemic mice.
    Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2860-4 PMID: 11226331
  36. NKT cell-mediated repression of tumor immunosurveillance by IL-13 and the IL-4R-STAT6 pathway.
    Nat Immunol. 2000 Dec;1(6):515-20 PMID: 11101874
  37. Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism.
    J Immunol. 2002 Jan 15;168(2):689-95 PMID: 11777962
  38. Aspirin and salicylates inhibit the IL-4- and IL-13-induced activation of STAT6.
    J Immunol. 2002 Feb 1;168(3):1428-34 PMID: 11801685
  39. Potential cardioprotective actions of no-releasing aspirin.
    Nat Rev Drug Discov. 2002 May;1(5):375-82 PMID: 12120413
  40. DNA vaccination against rat her-2/Neu p185 more effectively inhibits carcinogenesis than transplantable carcinomas in transgenic BALB/c mice.
    J Immunol. 2000 Nov 1;165(9):5133-42 PMID: 11046045
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-03-15
Epub
2005-00-07
Pages
4185-90
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC554823
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com