DOI: 10.1182/blood.v92.9.3172. Gene Transfer in Dendritic Cells, Induced by Oral DNA Vaccination With Salmonellatyphimurium, Results in Protective Immunity Against a Murine Fibrosarcoma

Gene Transfer in Dendritic Cells, Induced by Oral DNA Vaccination With Salmonellatyphimurium, Results in Protective Immunity Against a Murine Fibrosarcoma

10.1182/blood.v92.9.3172

Crossref journal-article

American Society of Hematology

Blood (234)

Abstract

AbstractA live attenuated AroA− auxotrophic mutant ofSalmonella typhimurium (SL7207) has been used as carrier for the pCMVβ vector that contains the β-galactosidase (β-gal) gene under the control of the immediate early promoter ofCytomegalovirus (CMV). We tested whether orally administered bacterial carrier could enter and deliver the transgene to antigen-presenting cells (APCs) through the natural enteric route of infection and whether β-gal expression could generate a protective response against an aggressive murine fibrosarcoma transduced with the β-gal gene (F1.A11) that behaves operationally as a tumor-associated antigen. After three courses, at 15-day intervals, mice developed both cell-mediated and systemic humoral responses to β-gal. Mice vaccinated with the Salmonella harboring pCMVβ, but not with plasmid-less carrier, showed resistance to a challenge with F1.A11 cells. These experiments suggest that Salmonella-based DNA immunization allows us to specifically target antigen expression in vivo to APCs. To prove that the transgene is actually expressed by APCs as a function of an eukaryotic promoter, the green fluorescent protein (GFP) was placed under the control of either the eukariotic CMV or a prokaryotic promoter. Using cytofluorometric analysis, GFP was detected only in splenocytes of mice receiving a Salmonella carrier harboring GFP under the CMV promoter. These results indicate that transgene expression occurs because of a Salmonella-mediated gene transfer to eukaryotic cells. Finally, approximately 19% of the splenocytes expressed GFP. Among them, F4/80+ macrophages and CD11cbright dendritic cells (DCs) were scored as positive for GFP expression. Extensive work has been performed trying to optimize the way to transfect DCs, ex vivo, with genes coding for relevant antigens. We show here, for the first time, that DCs can be directly and specifically transduced in vivo such to induce DNA vaccination against tumors.© 1998 by The American Society of Hematology.

Bibliography

Paglia, P., Medina, E., Arioli, I., Guzman, C. A., & Colombo, M. P. (1998). Gene Transfer in Dendritic Cells, Induced by Oral DNA Vaccination With Salmonellatyphimurium, Results in Protective Immunity Against a Murine Fibrosarcoma. Blood, 92(9), 3172â3176.

Authors 5

Paola Paglia (first)
Eva Medina (additional)
Ivano Arioli (additional)
Carlos A. Guzman (additional)
Mario P. Colombo (additional)

References 27 Referenced 111

10.1001/jama.1997.03540360065034 / JAMA / Recommendations for follow-up care of individuals with an inherited predisposition to cancer. by Burke (1997)
{'key': '2020021216241614600_B2', 'first-page': '101', 'article-title': 'Listeria monocytogenes, a promising vaccine carrier to evoke cellular immune responses', 'volume-title': 'Recombinant Gram-positive bacteria vehicles for mucosal immunization, Intelligence Unit Series.', 'author': 'Chakraborty', 'year': '1997'} / Recombinant Gram-positive bacteria vehicles for mucosal immunization, Intelligence Unit Series. / Listeria monocytogenes, a promising vaccine carrier to evoke cellular immune responses by Chakraborty (1997)
10.1038/32588 / Nature / Dendritic cells and the control of immunity. by Bancherau (1998)
10.1146/annurev.immunol.15.1.617 / Annu Rev Immunol / DNA Vaccines. by Donnelly (1997)
10.1016/S1074-7613(95)80001-8 / Immunity / Manipulation of the immune response to a plasmid-encoded viral antigen by coinoculation with plasmids expressing cytokines. by Xiang (1995)
10.1084/jem.184.4.1555 / J Exp Med / Gene vaccination with naked plasmid DNA: Mechanism of CTL priming. by Corr (1996)
10.1073/pnas.93.16.8578 / Proc Natl Acad Sci USA / Induction of cytotoxic T-lymphocytes by intramuscular immunization with plasmid DNA is facilitated by bone-marrow-derived cells. by Doe (1996)
10.1016/S0264-410X(96)00252-6 / Vaccine / Attenuated bacteria as DNA delivery vehicle for DNA-mediated immunization. by Sizemore (1997)
{'key': '2020021216241614600_B9', 'first-page': '1207', 'article-title': 'Gene transfer from bacteria to mammalian cells.', 'volume': '318', 'author': 'Courvalin', 'year': '1995', 'journal-title': 'Life Sci'} / Life Sci / Gene transfer from bacteria to mammalian cells. by Courvalin (1995)
10.1038/nbt0298-181 / Nat Biotech / Delivery of antigen-encoding plasmid DNA into the cytosol of macrophages by attenuated suicide Listeria monocytogenes. by Dietrich (1998)
10.1016/S0092-8674(00)80465-1 / Cell / Oral somatic transgene vaccination using attenuated S. typhimurium. by Darji (1997)
10.1002/eji.1830270637 / Eur J Immunol / The defined attenuated Listeria monocytogenes Δmpl2 mutant is an effective oral vaccine carrier to trigger long lasting immune response against a mouse fibrosarcoma. by Paglia (1997)
10.1084/jem.183.1.317 / J Exp Med / Murine dendritic cells loaded in vitro with soluble protein prime cytotoxic T lymphocytes against tumor antigen in vivo. by Paglia (1996)
10.1016/S0378-1119(97)00197-2 / Gene / Green fluorescent protein-based reporter systems for genetic analysis of bacteria including monocopy applications. by Suarez (1997)
10.4049/jimmunol.156.1.238 / J Immunol / Cytokine enhancement of DNA immunization leads to effective treatment of established pulmonary metastases. by Irvine (1996)
{'key': '2020021216241614600_B16', 'first-page': '4776', 'article-title': 'Regression of established tumors in mice mediated by the oral administration of a recombinant Listeria monocytogenes.', 'volume': '55', 'author': 'Pan', 'year': '1995', 'journal-title': 'Cancer Res'} / Cancer Res / Regression of established tumors in mice mediated by the oral administration of a recombinant Listeria monocytogenes. by Pan (1995)
10.1146/annurev.iy.12.040194.005015 / Annu Rev Immunol / Tolerance, danger, and the extended family. by Matzinger (1994)
10.1128/IAI.66.6.2401-2409.1998 / Infect Immun / Bacterial perturbation of cytokine network. by Wilson (1998)
10.1126/science.7513904 / Science / Role of bone-marrow-derived cells in presenting MHC class I-restricted tumor antigens. by Huang (1994)
10.1084/jem.171.2.377 / J Exp Med / Class I-restricted processing and presentation of exogenous cell-associated antigen in vivo. by Carbone (1990)
10.1038/nm1096-1122 / Nat Med / DNA-based immunization by in vivo transfection of dendritic cells. by Condon (1996)
10.1126/science.273.5273.352 / Science / Immunostimulatory sequences necessary for effective intradermal gene immunization. by Sato (1996)
10.1038/nm0996-1038 / Nat Med / DNA immunization induces protective immunity against B-cell lymphoma. by Syrengelas (1996)
{'key': '2020021216241614600_B24', 'first-page': '114', 'article-title': 'Pharmacological enhancement of in vivo foreign gene expression in muscle.', 'volume': '1', 'author': 'Danko', 'year': '1994', 'journal-title': 'Gene Ther'} / Gene Ther / Pharmacological enhancement of in vivo foreign gene expression in muscle. by Danko (1994)
10.1126/science.276.5313.718 / Science / Exploitation of mammalian host cell functions by bacterial pathogens. by Finlay (1997)
10.1038/nm0595-471 / Nat Med / A recombinant Listeria monocytogenes vaccine expressing a model tumor antigen protects mice against lethal tumor challenge and causes regression of established tumors. by Pan (1995)
10.1084/jem.186.8.1183 / J Exp Med / Dendritic cells as adjuvants for immune-mediated resistance to tumors. by Schuler (1997)

Dates

Type	When
Created	5 years, 10 months ago (Oct. 14, 2019, 7:25 a.m.)
Deposited	1 year, 11 months ago (Sept. 21, 2023, 12:52 p.m.)
Indexed	1 week, 5 days ago (Aug. 20, 2025, 8:32 a.m.)
Issued	26 years, 10 months ago (Nov. 1, 1998)
Published	26 years, 10 months ago (Nov. 1, 1998)
Published Print	26 years, 10 months ago (Nov. 1, 1998)

Funders 0

None

BibTeX

@article{Paglia_1998, title={Gene Transfer in Dendritic Cells, Induced by Oral DNA Vaccination With Salmonellatyphimurium, Results in Protective Immunity Against a Murine Fibrosarcoma}, volume={92}, ISSN={0006-4971}, url={http://dx.doi.org/10.1182/blood.v92.9.3172}, DOI={10.1182/blood.v92.9.3172}, number={9}, journal={Blood}, publisher={American Society of Hematology}, author={Paglia, Paola and Medina, Eva and Arioli, Ivano and Guzman, Carlos A. and Colombo, Mario P.}, year={1998}, month=nov, pages={3172–3176} }

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      "year": "1998",
      "journal-title": "Nature"
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      "author": "Donnelly",
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      "journal-title": "Annu Rev Immunol"
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      "doi-asserted-by": "crossref",
      "first-page": "129",
      "DOI": "10.1016/S1074-7613(95)80001-8",
      "article-title": "Manipulation of the immune response to a plasmid-encoded viral antigen by coinoculation with plasmids expressing cytokines.",
      "volume": "2",
      "author": "Xiang",
      "year": "1995",
      "journal-title": "Immunity"
    },
    {
      "key": "2020021216241614600_B6",
      "doi-asserted-by": "crossref",
      "first-page": "1555",
      "DOI": "10.1084/jem.184.4.1555",
      "article-title": "Gene vaccination with naked plasmid DNA: Mechanism of CTL priming.",
      "volume": "184",
      "author": "Corr",
      "year": "1996",
      "journal-title": "J Exp Med"
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      "doi-asserted-by": "crossref",
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      "volume": "93",
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      "first-page": "804",
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      "author": "Sizemore",
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      "date-parts": [
        [
          1998,
          11,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1182/blood.V92.9.3172",
  "relation": {},
  "ISSN": [
    "1528-0020",
    "0006-4971"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1998,
        11,
        1
      ]
    ]
  }
}