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Neurochemical Research

, Volume 32, Issue 12, pp 2203–2209 | Cite as

Emerging Role of Combination of All-trans Retinoic Acid and Interferon-gamma as Chemoimmunotherapy in the Management of Human Glioblastoma

  • Azizul Haque
  • Naren L. Banik
  • Swapan K. Ray
Original Paper

Abstract

Glioblastoma is the most malignant and common type of brain tumor with devastating outcome. Because current treatment modalities are mostly ineffective in controlling and curing glioblastoma, new and innovative therapeutic strategies must be developed. This article describes recent advances in chemoimmunotherapy, which is combination of chemotherapy and immunotherapy, against glioblastoma. We provide an overview of available treatment options for glioblastomas, gaps in our knowledge of immune recognition of these malignant tumors, and chemotherapeutic and immunotherapeutic agents that need to be further explored for designing novel chemoimmunotherapeutic strategy for the management of human glioblastomas. Our recent study demonstrated that combination of the chemotherapeutic agent all-trans retinoic acid (ATRA) and the immunotherapeutic agent interferon-gamma (IFN-γ) could concurrently induce differentiation, apoptotic death, and immune components in two different human glioblastoma cell lines. We propose that combination of ATRA and IFN-γ can become an efficacious chemoimmunotherapy for the treatment of human glioblastoma.

Keywords

Apoptosis ATRA Chemoimmunotherapy Cross-presentation Gamma interferon-inducible lysosomal thiolreductase Glioblastoma IFN-γ Invariant chain 

Notes

Acknowledgments

This work was supported in part by the grants from Leukemia and Lymphoma Society, American Cancer Society, Department of Defence, and American Lung Association (to A.H.), and also National Institutes of Health (to N.L.B and S.K.R.).

References

  1. 1.
    Boudreau CR, Yang I, Liau LM (2005) Gliomas: advances in molecular analysis and characterization. Surg Neurol 64:286–294PubMedCrossRefGoogle Scholar
  2. 2.
    Palanichamy K, Erkkinen M, Chakravarti A (2006) Predictive and prognostic markers in human glioblastomas. Curr Treat Options Oncol 7:490–504PubMedCrossRefGoogle Scholar
  3. 3.
    Wong ML, Kaye AH, Hovens CM (2007) Targeting malignant glioma survival signalling to improve clinical outcomes. J Clin Neurosci 14:301–308PubMedCrossRefGoogle Scholar
  4. 4.
    Hsieh JC, Lesniak MS (2005) Surgical management of high-grade gliomas. Expert Rev Neurother 5:S33–S39PubMedCrossRefGoogle Scholar
  5. 5.
    Paganelli G, Bartolomei M, Grana C, Ferrari M, Rocca P, Chinol M (2006) Radioimmunotherapy of brain tumor. Neurol Res 28:518–522PubMedCrossRefGoogle Scholar
  6. 6.
    Nieder C, Grosu AL, Astner S, Molls M (2005) Treatment of unresectable glioblastoma multiforme. Anticancer Res 25:4605–4610PubMedGoogle Scholar
  7. 7.
    Nieder C, Adam M, Molls M, Grosu AL (2006) Therapeutic options for recurrent high-grade glioma in adult patients: recent advances. Crit Rev Oncol Hematol 60:181–193PubMedCrossRefGoogle Scholar
  8. 8.
    Robins HI, Chang S, Butowski N, Mehta M (2007) Therapeutic advances for glioblastoma multiforme: current status and future prospects. Curr Oncol Rep 9:66–70PubMedCrossRefGoogle Scholar
  9. 9.
    Ng SS, Gao Y, Chau DH, Li GH, Lai LH, Huang PT, Huang CF, Huang JJ, Chen YC, Kung HF, Lin MC (2007) A novel glioblastoma cancer gene therapy using AAV-mediated long-term expression of human TERT C-terminal polypeptide. Cancer Gene Ther 14:561–572PubMedCrossRefGoogle Scholar
  10. 10.
    Fan X, Salford LG, Widegren B (2007) Glioma stem cells: evidence and limitation. Semin Cancer Biol 17:214–218PubMedCrossRefGoogle Scholar
  11. 11.
    Nikanjam M, Blakely EA, Bjornstad KA, Shu X, Budinger TF, Forte TM (2007) Synthetic nano-low density lipoprotein as targeted drug delivery vehicle for glioblastoma multiforme. Int J Pharm 328:86–94PubMedCrossRefGoogle Scholar
  12. 12.
    Tang J, Flomenberg P, Harshyne L, Kenyon L, Andrews DW (2005) Glioblastoma patients exhibit circulating tumor-specific CD8+ T cells. Clin Cancer Res 11:5292–9529PubMedCrossRefGoogle Scholar
  13. 13.
    Carpentier AF, Meng Y (2006) Recent advances in immunotherapy for human glioma. Curr Opin Oncol 18:631–636PubMedCrossRefGoogle Scholar
  14. 14.
    Kahlon KS, Brown C, Cooper LJ, Raubitschek A, Forman SJ, Jensen MC (2004) Specific recognition and killing of glioblastoma multiforme by interleukin 13-zetakine redirected cytolytic T cells. Cancer Res 64:9160–9166PubMedCrossRefGoogle Scholar
  15. 15.
    Yamanaka R, Abe T, Yajima N, Tsuchiya N, Homma J, Kobayashi T, Narita M, Takahashi M, Tanaka R (2003) Vaccination of recurrent glioma patients with tumour lysate-pulsed dendritic cells elicits immune responses: results of a clinical phase I/II trial. Br J Cancer 89:1172–1179PubMedCrossRefGoogle Scholar
  16. 16.
    Yu JS, Liu G, Ying H, Yong WH, Black KL, Wheeler CJ (2004) Vaccination with tumor lysate-pulsed dendritic cells elicits antigen-specific, cytotoxic T-cells in patients with malignant glioma. Cancer Res 64:4973–4979PubMedCrossRefGoogle Scholar
  17. 17.
    van der Bruggen P, Van den Eynde BJ (2006) Processing and presentation of tumor antigens and vaccination strategies. Curr Opin Immunol 18:98–104PubMedCrossRefGoogle Scholar
  18. 18.
    Thompson JA, Dissanayake SK, Ksander BR, Knutson KL, Disis ML, Ostrand-Rosenberg S (2006) Tumor cells transduced with the MHC class II Transactivator and CD80 activate tumor-specific CD4+ T cells whether or not they are silenced for invariant chain. Cancer Res 66:1147–1154PubMedCrossRefGoogle Scholar
  19. 19.
    Schiltz PM, Gomez GG, Read SB, Kulprathipanja NV, Kruse CA (2002) Effects of IFN-γ and interleukin-1β on major histocompatibility complex antigen and intercellular adhesion molecule-1 expression by 9L gliosarcoma: relevance to its cytolysis by alloreactive cytotoxic T lymphocytes. J Interferon Cytokine Res 22:1209–1216PubMedCrossRefGoogle Scholar
  20. 20.
    Gomez GG, Kruse CA (2006) Mechanisms of malignant glioma immune resistance and sources of immunosuppression. Gene Ther Mol Biol 10:133–146PubMedGoogle Scholar
  21. 21.
    Gattoni A, Parlato A, Vangieri B, Bresciani M, Derna R (2006) Interferon-gamma: biologic functions and HCV therapy (type I/II) (1 of 2 parts). Clin Ter 157:377–386PubMedGoogle Scholar
  22. 22.
    Haque A, Das A, Hajiaghamohseni LM, Younger A, Banik NL, Ray SK (2006) Induction of apoptosis and immune response by all-trans retinoic acid plus interferon-gamma in human glioblastoma T98G and U87MG cells. Cancer Immunol Immunother 56:615–625PubMedCrossRefGoogle Scholar
  23. 23.
    Tao Y, Yang Y, Wang W (2006) Effect of all-trans-retinoic acid on the differentiation, maturation and functions of dendritic cells derived from cord blood monocytes. FEMS Immunol Med Microbiol 47:444–450PubMedCrossRefGoogle Scholar
  24. 24.
    Mathew JS, Sharma RP (2000) Effect of all-trans-retinoic acid on cytokine production in a murine macrophage cell line. Int J Immunopharmacol 22:693–706PubMedCrossRefGoogle Scholar
  25. 25.
    Wang KC, Cheng AL, Chuang SE, Hsu HC, Su IJ (2000) Retinoic acid-induced apoptotic pathway in T-cell lymphoma: Identification of four groups of genes with differential biological functions. Exp Hematol 28:1441–1450PubMedCrossRefGoogle Scholar
  26. 26.
    Pohl J, LaFace D, Sands JF (1993) Transcription of retinoic acid receptor genes in transgenic mice increases CD8 T-cell subset. Mol Biol Rep 17:135–142PubMedCrossRefGoogle Scholar
  27. 27.
    Westervelt P, Pollock JL, Oldfather KM, Walter MJ, Ma MK, Williams A, DiPersio JF, Ley TJ (2002) Adaptive immunity cooperates with liposomal all-trans-retinoic acid (ATRA) to facilitate long-term molecular remissions in mice with acute promyelocytic leukemia. Proc Natl Acad Sci USA 99:9468–9473PubMedCrossRefGoogle Scholar
  28. 28.
    Luo XM, Ross AC (2005) Physiological and receptor-selective retinoids modulate interferon gamma signaling by increasing the expression, nuclear localization, and functional activity of interferon regulatory factor-1. J Biol Chem 280:36228–36236PubMedCrossRefGoogle Scholar
  29. 29.
    Aoudjit F, Bosse M, Stratowa C, Voraberger G, Audette M (1994) Regulation of intercellular adhesion molecule-1 expression by retinoic acid: analysis of the 5’ regulatory region of the gene. Int J Cancer 58:543–549PubMedCrossRefGoogle Scholar
  30. 30.
    Matloubian M, Concepcion RJ, Ahmed R (1994) CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. J Virol 68:8056–8063PubMedGoogle Scholar
  31. 31.
    Mautner J, Jaffee EM, Pardoll DM (2005) Tumor-specific CD4+ T cells from a patient with renal cell carcinoma recognize diverse shared antigens. Int J Cancer 115:752–759PubMedCrossRefGoogle Scholar
  32. 32.
    Kusmartsev S, Cheng F, Yu B, Nefedova Y, Sotomayor E, Lush R, Gabrilovich D (2003) All-trans retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination. Cancer Res 63:4441–4449PubMedGoogle Scholar
  33. 33.
    Mirza N, Fishman M, Fricke I, Dunn M, Neuger AM, Frost TJ, Lush RM, Antonia S, Gabrilovich DI (2006) All-trans retinoic acid improves differentiation of myeloid cells and immune response in cancer patients. Cancer Res 66:9299–9307PubMedCrossRefGoogle Scholar
  34. 34.
    Mocellin S, Wang E, Marincola FM (2001) Cytokines and immune response in the tumor microenvironment. J Immunother 24:392–407CrossRefGoogle Scholar
  35. 35.
    Sinha P, Clements VK, Miller S, Ostrand-Rosenberg S (2005) Tumor immunity: a balancing act between T cell activation, macrophage activation and tumor-induced immune suppression. Cancer Immunol Immunother 54:1137–1142PubMedCrossRefGoogle Scholar
  36. 36.
    Haque MA, Li P, Jackson SK, Zarour HM, Hawes JW, Phan UT, Maric M, Cresswell P, Blum JS (2002) Absence of gamma-interferon-inducible lysosomal thiol reductase in melanomas disrupts T cell recognition of select immunodominant epitopes. J Exp Med 195:1267–1277PubMedCrossRefGoogle Scholar
  37. 37.
    Facoetti A, Nano R, Zelini P, Morbini P, Benericetti E, Ceroni M, Campoli M, Ferrone S (2005) Human leukocyte antigen and antigen processing machinery component defects in astrocytic tumors. Clin Cancer Res 11:8304–8311PubMedCrossRefGoogle Scholar
  38. 38.
    O’Donnell PW, Haque A, Klemsz MJ, Kaplan MH, Blum JS (2004) Induction of the antigen processing enzyme IFN-gamma-inducible lysosomal thiol reductase in melanoma cells is STAT1-dependent but CIITA-independent. J Immunol 173:731–735PubMedGoogle Scholar
  39. 39.
    Maccalli C, Li YF, El-Gamil M, Rosenberg SA, Robbins PF (2003) Identification of a colorectal tumor-associated antigen (COA-1) recognized by CD4+ T lymphocytes. Cancer Res 63:6735–6743PubMedGoogle Scholar
  40. 40.
    Zehbe I, Hohn H, Pilch H, Neukirch C, Freitag K, Maeurer MJ (2005) Differential MHC class II component expression in HPV-positive cervical cancer cells: implication for immune surveillance. Int J Cancer 117:807–815PubMedCrossRefGoogle Scholar
  41. 41.
    Rangel LB, Agarwal R, Sherman-Baust CA, Mello-Coelho V, Pizer ES, Ji H, Taub DD, Morin PJ (2004) Anomalous expression of the HLA-DR α and β chains in ovarian and other cancers. Cancer Biol Ther 3:1021–1027PubMedCrossRefGoogle Scholar
  42. 42.
    Haque A, Blum JS (2005) New insights in antigen processing and epitope selection: development of novel immunotherapeutic strategies for cancer, autoimmunity and infectious diseases. J Biol Regul Homeost Agents 19:93–104PubMedGoogle Scholar
  43. 43.
    Hatano M, Eguchi J, Tatsumi T, Kuwashima N, Dusak JE, Kinch MS, Pollack IF, Hamilton RL, Storkus WJ, Okada H (2005) EphA2 as a glioma-associated antigen: a novel target for glioma vaccines. Neoplasia 7:717–722PubMedCrossRefGoogle Scholar
  44. 44.
    Nutt CL, Betensky RA, Brower MA, Batchelor TT, Louis DN, Stemmer-Rachamimov AO (2005) YKL-40 is a differential diagnostic marker for histologic subtypes of high-grade gliomas. Clin Cancer Res 11:2258–2264PubMedCrossRefGoogle Scholar
  45. 45.
    Akasaki Y, Liu G, Chung NH, Ehtesham M, Black KL, Yu JS (2004) Induction of a CD4+ T regulatory type 1 response by cyclooxygenase-2-overexpressing glioma. J Immunol 173:4352–4359PubMedGoogle Scholar
  46. 46.
    Cetin N, Dienel G, Gokden M (2005) CD117 expression in glial tumors. J Neurooncol 75:195–202PubMedCrossRefGoogle Scholar
  47. 47.
    Pallasch CP, Struss AK, Munnia A, Konig J, Steudel WI, Fischer U, Meese E (2005) Autoantibodies against GLEA2 and PHF3 in glioblastoma: tumor-associated autoantibodies correlated with prolonged survival. Int J Cancer 117:456–459PubMedCrossRefGoogle Scholar
  48. 48.
    Liu G, Ying H, Zeng G, Wheeler CJ, Black KL, Yu JS (2004) HER-2, gp100, and MAGE-1 are expressed in human glioblastoma and recognized by cytotoxic T cells. Cancer Res 64:4980–4986PubMedCrossRefGoogle Scholar
  49. 49.
    Dissanayake SK, Thompson JA, Bosch JJ, Clements VK, Chen PW, Ksander BR, Ostrand-Rosenberg S (2004) Activation of tumor-specific CD4+ T lymphocytes by major histocompatibility complex class II tumor cell vaccines: a novel cell-based immunotherapy. Cancer Res 64:1867–1874PubMedCrossRefGoogle Scholar
  50. 50.
    Haque MA, Hawes JW, Blum JS (2001) Cysteinylation of an MHC class II ligand: importance endocytosis and reductive processing in T cell recognition. J Immunol 166:4543–4551PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Azizul Haque
    • 1
    • 2
    • 3
  • Naren L. Banik
    • 1
    • 3
    • 4
  • Swapan K. Ray
    • 1
    • 3
    • 4
  1. 1.Department of Microbiology and ImmunologyMedical University of South CarolinaCharlestonUSA
  2. 2.Children’s Research InstituteMedical University of South CarolinaCharlestonUSA
  3. 3.Hollings Cancer CenterMedical University of South CarolinaCharlestonUSA
  4. 4.Department of NeurosciencesMedical University of South CarolinaCharlestonUSA

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