Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-05T22:26:25.894Z Has data issue: false hasContentIssue false
  • English
  • Français

All-trans-retinoic acid and polyriboinosinoic : polyribocytidylic acid cooperate to elevate anti-tetanus immunoglobulin G and immunoglobulin M responses in vitamin A-deficient Lewis rats and Balb/c mice

Published online by Cambridge University Press:  28 February 2007

Kathleen L. DeCicco  and
A. Catharine Ross
Kathleen L. DeCicco
Affiliation:
The Graduate Program in Nutrition and, The Pennsylvania State University, University Park, Pennsylvania, PA 16802, USA
A. Catharine Ross*
Affiliation:
Department of Nutrition, The Pennsylvania State University, University Park, Pennsylvania, PA 16802, USA
*
*Corresponding author:Professor A. Catharine Ross, fax +1 814 865 4723, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Vitamin A (VA) deficiency compromises antibody responses to T-cell-dependent antigens such as tetanus toxoid, but this effect can be reversed through administration of retinol or retinoic acid (RA). To test whether RA and polyriboinosinioc : polyribocytidylic acid (PIC), a known inducer of several forms of interferon (IFN), can cooperate to increase specific immunoglobulin (Ig)G and IgM production during VA deficiency, rats and mice were made VA-deficient, immunized with TT and treated with all-trans-RA, PIC or their combination. VA-deficient rats produced low primary and secondary anti-tetanus IgG responses (VA-deficient controls v. VA-sufficient controls P < 0·001), although total IgG was slightly elevated when compared with VA-sufficient control rats. Although RA administered alone elevated antibody production during VA deficiency to control levels, RA combined with PIC synergistically enhanced these responses (RA and PIC group v. all other groups P < 0·0001). In contrast, Balb/c mice maintained on a VA-deficient diet and immunized in a similar fashion showed no impairment in antigen-specific IgG levels, but treatment with a combination of RA and PIC still evoked an additive enhancement in antigen-specific antibody production. Additionally, RA and PIC administration to VA-sufficient mice resulted in elevated antibody responses, suggesting that this combination should be evaluated further for its immuno-stimulatory effects.

Keywords

Vitamin ARetinoic acidPolyriboinosinic acidpolyribocytidylic acidInterferonAntibodies
Type
Symposium on ‘The molecular and cellular roles of nutrients in the immune system’
Information
Proceedings of the Nutrition Society , Volume 59 , Issue 4 , November 2000 , pp. 519 - 529
Copyright
Copyright © The Nutrition Society 2000

References

Abb, J & Deinhardt, F (1980) Effects of retinoic acid on the human lymphocyte response to mitogens. Experimental Cell Biology 48, 169–179.Google Scholar
Arora, D & Ross, AC (1994) Antibody response against tetanus toxoid is enhanced by lipopolysaccharide or tumor necrosis factor-alpha in vitamin A-sufficient and -deficient rats. American Journal of Clinical Nutrition 59, 922–928.CrossRefGoogle ScholarPubMed
Ballow, M, Wang, WP & Xiang, SN (1996) Modulation of B-cell immunoglobulin synthesis by retinoic acid. Clinical Immunology and Immunopathology 80, S73–S81.CrossRefGoogle ScholarPubMed
Beaton, GH, Martorell, R, Aronson, KJ, Edmonston, B, McCabe, G, Ross, AC & Harvey, B (1993) Effectiveness of Vitamin A Supplementation in the Control of Young Child Morbidity and Mortality in Developing Countries. ACC/SCN State-of-the-Art Series. Nutrition Policy Discussion Paper no. 13. Geneva: UN.Google Scholar
Bhatti, L & Sidell, N (1994) Transcriptional regulation by retinoic acid of interleukin-2α receptors in human B cells. Immunology 81, 273–279.Google Scholar
Bollag, W, Majewski, S & Jablonska, S (1994) Cancer combination chemotherapy with retinoids: experimental rationale. Leukemia 8, 1453–1457.Google ScholarPubMed
Coppenhaver, DH, Singh, IP, Sarzotti, M, Levy, HB & Baron, S (1995) Treatment of intracranial alphavirus infections in mice by a combination of specific antibodies and an interferon inducer. American Journal of Tropical Medicine and Hygiene 52, 34–40.CrossRefGoogle Scholar
Darnell, JE Jr, Kerr, IM & Stark, GR (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415–1420.CrossRefGoogle ScholarPubMed
DeCicco, KL, Zolfaghari, R, Li, N-Q, & Ross, AC (2000) Retinoic acid and polyriboinosinic acid:polyribocytidylic acid (PIC) act synergistically to enhance the antibody response to tetanus toxoid during vitamin A deficiency: possible involvement of interleukin (IL)-2 receptor beta, signal transducer and activator of transcription (STAT)-1, and interferon regulatory factor (IRF)-1. Journal of Infectious Diseases 182 Suppl. 1, (In the Press).Google Scholar
DeCicco, KL, Zolfaghari, R & Ross, AC (1999) Interleukin-2Rβ, IRF-1, and STAT-1 mRNA are reduced in vitamin A deficiency but recovered by treatment with retinoic acid (RA) and poly-I:C-L,C (PIC) in vivo. FASEB Journal 13, 674. 26 Abstr.Google Scholar
Dillehay, DL, Li, W, Kalin, J, Walia, AS & Lamon, EW (1987) In vitro effects of retinoids on murine thymus-dependent and thymus- independent mitogenesis. Cellular Immunology 107, 130–137.CrossRefGoogle ScholarPubMed
Dowling, JE & Wald, G (1960) The biological function of vitamin A acid. Proceedings of the National Academy of Sciences USA 46, 587–608.CrossRefGoogle ScholarPubMed
el Mansouri, S, Tod, M, Leclerq, M, Petitjean, O, Perret, G & Porthault, M (1995) Time- and dose-dependent kinetics of all-trans-retinoic acid in rats after oral or intravenous administration(s). Drug Metabolism and Disposition 23, 227–231.Google Scholar
Fawzi, WW, Chalmers, TC, Herrera, MG & Mosteller, F (1993) Vitamin A supplementation and child mortality. A meta-analysis. Journal of the American Medical Association 269, 898–903.CrossRefGoogle ScholarPubMed
Field, AK, Tytell, AA, Lampson, GP & Hilleman, MR (1967) Inducers of interferon and host resistance. II. Multistranded synthetic polynucleotide complexes. Proceedings of the National Academy of Sciences USA 58, 1004–1010.CrossRefGoogle ScholarPubMed
Gershwin, ME, Lentz, DR, Beach, RS & Hurley, LS (1984) Nutritional factors and autoimmunity: IV. Dietary vitamin A deprivation induces a selective increase in IgM autoantibodies and hypergammaglobulinemia in New Zealand black mice. Journal of Immunology 133, 222–226.CrossRefGoogle ScholarPubMed
Glasziou, PP & Mackerras, DEM (1993) Vitamin A supplementation in infection disease: a meta-analysis. British Medical Journal 306, 366–370.CrossRefGoogle ScholarPubMed
Gudas, LJ, Sporn, MB & Roberts, AB (1994) Cellular biology and biochemistry of the retinoids. In The Retinoids: Biology, Chemistry and Medicine, pp. 443–520 [Sporn, MB, Roberts, AB and Goodman, DS, editors]. New York: Raven Press.Google Scholar
Harada, H, Fujita, T, Miyamoto, M, Kimura, Y, Maruyama, M, Furia, A, Miyata, T & Taniguchi, T (1989) Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes. Cell 58, 729–739.CrossRefGoogle Scholar
Henderson, RH, Keja, J, Hayden, G, Galazka, A, Clements, J & Chan, C (1988) Immunizing the children of the world: Progress and prospects. Bulletin of the World Health Organization 66, 535–543.Google ScholarPubMed
Hilleman, MR (1970) Prospects for the use of double-stranded ribonucleic acid (Poly I:C) inducers in man. Journal of Infectious Diseases 121, 196–211.CrossRefGoogle ScholarPubMed
Himmelrich, H, Launois, P, Tacchini-Cottier, F & Louis, JA (1999) Some of the early events underlying Th2 cell maturation and susceptibility to Leishmania major infection in BALB/c mice. Biological Chemistry 380, 909–914.CrossRefGoogle ScholarPubMed
Kinoshita, M, Pasatiempo, AMG, Taylor, CE & Ross, AC (1991) Immunological memory to tetanus toxoid is established and maintained in the vitamin A-depleted rat. FASEB Journal 5, 2473–2481.Google Scholar
Kinoshita, M & Ross, AC (1993) Vitamin A status and immunoglobulin G subclasses in rats immunized with tetanus toxoid. FASEB Journal 7, 1277–1282.CrossRefGoogle ScholarPubMed
Lippman, SM, Gilsson, BS, Kavanagh, JJ, Lotan, R, Hong, WK, Paredes-Espinoza, M, Hittelman, WN, Holdener, EE & Krakoff, IH (1993) Retinoic acid and interferon combination studies in human cancer. European Journal of Cancer 29A, S9–S13.CrossRefGoogle Scholar
Lippman, SM, Lotan, R & Schleuniger, U (1997) Retinoid-interferon therapy of solid tumors. International Journal of Cancer 70, 481–483.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Majewski, S, Szmurlo, A, Marczak, M, Jablonska, S & Bollag, W (1994) Synergistic effect of retinoids and interferon α on tumor-induced angiogenesis: anti-angiogenic effect on HPV-harboring tumor-cell lines. International Journal of Cancer 57, 81–85.Google Scholar
Manetti, R, Annunziato, F, Tomasevic, L, Giannò, V, Parronchi, P, Romagnani, S & Maggi, E (1995) Polyinosinic acid : polycytidylic acid promotes T helper type 1 specific immune responses by stimulating macrophage production of interferon-α and interleukin-12. European Journal of Immunology 25, 2656–2660.CrossRefGoogle ScholarPubMed
Manetti, R, Gerosa, F, Giudizi, MG, Biagiotti, R, Parronchi, P, Piccinni, M-P, Sampognaro, S, Maggi, E, Romagnani, S & Trinchieri, G (1994) Interleukin 12 induces stable priming for interferon γ (IFN-γ) production during differentiation of human T helper (Th) cells and transient IFN-γ) production in established Th2 cell clones. Journal of Experimental Medicine 179, 1273–1283.CrossRefGoogle Scholar
Mangelsdorf, DJ, Thummel, C, Beato, M, Herrlich, P, Schutz, G, Umesono, K, Blumberg, B, Kastner, P, Mark, M, Chambon, P & Evans, RM (1995) The nuclear receptor superfamily: the second decade. Cell 83, 835–839.CrossRefGoogle ScholarPubMed
Marrack, P, Kappler, J & Mitchell, T (1999) Type I interferons keep activated T cells alive. Journal of Experimental Medicine 189, 521–529.CrossRefGoogle ScholarPubMed
Matikainen, S, Lehtonen, A, Sareneva, T, Julkunen, I (1998) Regulation of IRF and STAT gene expression by retinoic acid. Leukemia and Lymphoma 30, 63–71.CrossRefGoogle ScholarPubMed
Matikainen, S, Ronni, T, Lehtonen, A, Sareneva, T, Melén, K, Nordling, S, Levy, DE & Julkunen, I (1997) Retinoic acid induces signal transducer and activator of transcription (STAT) 1, STAT2, and p48 expression in myeloid leukemia cells and enhances their responsiveness to interferons. Cell Growth and Differentiation 8, 687–698.Google ScholarPubMed
Matikainen, S, Sareneva, T, Ronni, T, Lehtonen, A, Koskinen, PJ & Julkunen, I (1999) Interferon-α activates multiple STAT proteins and upregulates proliferation-associated IL-2Rα, c-myc, and pim-1 genes in human T cells. Blood 93, 1980–1991.Google Scholar
Mitchell, T, Kappler, J & Marrack, P (1999) Bystander virus infection prolongs activated T cell survival. Journal of Immunology 162, 4527–4535.CrossRefGoogle ScholarPubMed
Moore, DM, Kalvakolanu, DV, Lippman, SM, Kavanagh, JJ, Hong, WK, Borden, EC, Paredes-Espinoza, M & Krakoff, IH (1994) Retinoic acid and interferon in human cancer: mechanistic and clinical studies. Seminars in Hematology 31, 31–37.Google ScholarPubMed
Mosmann, TR & Coffman, RL (1989) Heterogeneity of cytokine secretion patterns and functions of helper T cells. Advances in Immunology 46, 111–147.CrossRefGoogle ScholarPubMed
Pasatiempo, AMG, Kinoshita, M & Ross, AC (1992) Co-immunization with lipopolysaccharide and pneumococcal polysaccharide (SSS-III) restores the antibody response to SSS-III in the vitamin A-deficient rat. FASEB Journal 6, A1659.Google Scholar
Pasatiempo, AMG, Kinoshita, M, Taylor, CE, & Ross, AC (1990) Antibody production in vitamin A-depleted rats is impaired after immunization with bacterial polysaccharide or protein antigens. FASEB Journal 4, 2518–2527.CrossRefGoogle ScholarPubMed
Pelicano, L, Li, FS, Schindler, C & Chelbi-Alix, MK (1997) Retinoic acid enhances the expression of interferon-induced proteins: evidence for multiple mechanisms of action. Oncogene 15, 2349–2359.CrossRefGoogle ScholarPubMed
Puri, SK, Dutta, GP, Levy, HB & Maheshwari, RK (1996) Poly IC-LC inhibits. Plasmodium cynomolgi B malaria infection in rhesus monkeys. Journal of Interferon Cytokine Research 16, 49–52.CrossRefGoogle Scholar
Reeves, PG, Nielsen, FH & Fahey, GC Jr (1993) AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. Journal of Nutrition 123, 1939–1951.CrossRefGoogle Scholar
Ross, AC (1990) Separation of fatty acid esters of retinol by high-performance liquid chromatography. Methods in Enzymology 189, 81–84.CrossRefGoogle ScholarPubMed
Ross, AC (1992) Vitamin A status: relationship to immunity and the antibody response. Proceedings of the Society for Experimental Biology and Medicine 200, 303–330.CrossRefGoogle ScholarPubMed
Ross, AC (1996) Vitamin A deficiency and retinoid repletion regulate the antibody response to bacterial antigens and the maintenance of natural killer cells. Clinical Immunology and Immunopathology 80, S36–S72.CrossRefGoogle ScholarPubMed
Ross, AC (2000 a) Vitamin A and retinoids. In Modern Nutrition in Health and Disease, 9th ed., pp. 305–327 [Shils, ME, Olson, JA, Shike, M and Ross, AC, editors]. Baltimore, MD: Williams Wilkins.Google Scholar
Ross, AC (2000 b) Vitamin A, retinoids and immune responses. In Vitamin A and Retinoids: An Update of Biological Aspects and Clinical Applications, pp. 83–95 [Livrea, MA, editor]. Basel: Birkhäuser Verlag.Google Scholar
Ross, AC & Hämmerling, UG (1994) Retinoids and the immune system. In The Retinoids: Biology, Chemistry and Medicine, pp. 521–544 [Sporn, MB, Roberts, AB and Goodman, DS, editors]. New York: Raven Press.Google Scholar
Schmidt, ME & Douglas, SD (1976) Effects of synthetic single- and multistranded polynucleotides on human monocyte IgG receptor activity in vitro. Proceedings of the Society for Experimental Biology and Medicine 151, 376–379.CrossRefGoogle ScholarPubMed
Semba, RD (1994) Vitamin A, immunity, and infection. Clinical and Infectious Diseases 19, 489–499.Google Scholar
Sen, GC & Ransohoff, RM (1993) Interferon-induced antiviral actions and their regulation. Advances in Virus Research 42, 57–102.Google Scholar
Sidell, N, Chang, B & Bhatti, L (1993) Up-regulation by retinoic acid of interleukin-2-receptor mRNA in human T lymphocytes. Cellular Immunology 146, 28–37.CrossRefGoogle ScholarPubMed
Smith, JE (1990) Preparation of vitamin A-deficient rats and mice. Methods in Enzymology 190, 229–236.CrossRefGoogle ScholarPubMed
Smith, SM, Levy, NL & Hayes, CE (1987) Impaired immunity in vitamin A deficient mice. Journal of Nutrition 117, 857–865.CrossRefGoogle ScholarPubMed
Sommer, A & , KP West, KP Jr (1996). Vitamin A Deficiency: Health, Survival, and Vision. New York: Oxford University Press Inc.Google Scholar
Su, L & David, M (1999) Inhibition of B cell receptor-mediated apoptosis by IFN. Journal of Immunology 162, 6317–6321.CrossRefGoogle ScholarPubMed
Valone, FH & Payan, DG (1985) Potentiation of mitogen-induced human T-lymphocyte activation by retinoic acid. Cancer Research 45, 4129–4131.Google ScholarPubMed
Wang, W & Ballow, M (1993) The effects of retinoic acid on in vitro immunoglobulin synthesis by cord blood and adult peripheral blood mononuclear cells. Cellular Immunology 148, 291–300.CrossRefGoogle ScholarPubMed
Weihua, X, Kolla, V & Kalvakolanu, DV (1997) Modulation of interferon action by retinoids – Induction of murine STAT1 gene expression by retinoic acid. Journal of Biological Chemistry 272, 9742–9748.CrossRefGoogle Scholar
Williams, BRG & Haque, SJ (1997) Interacting pathways of interferon signaling. Seminars in Oncology 24, S9–70–S9–77.Google ScholarPubMed
Wong, JP, Saravolac, EG, Sabuda, D, Levy, HB & Kende, M (1995) Prophylactic and therapeutic efficacies of Poly(ICLC) against respiratory influenza A virus infection in mice. Antimicrobial Agents and Chemotherapy 39, 2574–2576.CrossRefGoogle ScholarPubMed
Wuarin, L, Verity, MA & Sidell, N (1991) Effects of interferon-gamma and its interaction with retinoic acid on human neuroblastoma differentiation. International Journal of Cancer 48, 136–141.CrossRefGoogle ScholarPubMed