Optimized Dose of Dendritic Cell-based Vaccination in Experimental Model of Tumor Using Artificial Neural Network
-
Zahra Mirsanei
,
Sima Habibi
,
Nasim Kheshtchin
,
Reza Mirzaei
,
Samaneh Arab
,
Bahareh Zand
,
Farhad Jadidi-Niaragh
,
Aida Safvati
,
Ehsan Sharif-Paghaleh
,
Abazar Arabameri
,
Davud Asemani
,
Jamshid Hajati
Abstract
Previous studies have demonstrated that maturation of dendritic cells (DCs) by pathogenic components through pathogen-associated molecular patterns (PAMPs) such as Listeria monocytogenes lysate (LML) or CpG DNA can improve cancer vaccination in experimental models. In this study, a mathematical model based on an artificial neural network (ANN) was used to predict several patterns and dosage of matured DC administration for improved vaccination. The ANN model predicted that repeated co-injection of tumor antigen (TA)-loaded DCs matured with CpG (CpG-DC) and LML (List-DC) results in improved antitumor immune response as well as a reduction of immunosuppression in the tumor microenvironment. In the present study, we evaluated the ANN prediction accuracy about DC-based cancer vaccines pattern in the treatment of Wehi164 fibrosarcoma cancer-bearing mice. Our results showed that the administration of the DC vaccine according to ANN predicted pattern, leads to a decrease in the rate of tumor growth and size and augments CTL effector function. Furthermore, gene expression analysis confirmed an augmented immune response in the tumor microenvironment. Experimentations justified the validity of the ANN model forecast in the tumor growth and novel optimal dosage that led to more effective treatment.
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3. Namdar A, Mirzaei R, Memarnejadian A, Boghosian R, Samadi M, Mirzaei HR, et al. Prophylactic DNA vaccine targeting Foxp3+ regulatory T cells depletes myeloid-derived suppressor cells and improves anti-melanoma immune responses in a murine model. Cancer Immunol Immunother 2018; 67(3):367-79.
4. Nourizadeh M, Masoumi F, Memarian A, Alimoghaddam K, Moazzeni SM, Yaghmaie M, et al. In vitro induction of potent tumor-specific cytotoxic T lymphocytes using TLR agonist-activated AML-DC. Target Oncol 2014; 9(3):225-37.
5. Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012; 12(4):265-77.6. Timmerman M, John M, Levy M, Ronald. Dendritic cell vaccines for cancer immunotherapy. Ann Rew Med 1999; 50(1):507-29.
7. Rosenberg SA. Progress in human tumour immunology and immunotherapy. Nature 2001; 411(6835):380-4.
8. Muraille E, Giannino R, Guirnalda P, Leiner I, Jung S, Pamer EG, et al. Distinct in vivo dendritic cell activation by live versus killed Listeria monocytogenes. Eur J Immunol 2005; 35(5):1463-71.
9. Krug A, Rothenfusser S, Selinger S, Bock C, Kerkmann M, Battiany J, et al. CpG-A oligonucleotides induce a monocyte-derived dendritic cell-like phenotype that preferentially activates CD8 T cells. The J Immunol 2003; 170(7):3468-77.10. Khamisabadi M, Arab S, Motamedi M, Khansari N, Moazzeni SM, Gheflati Z, et al. Listeria monocytogenes activated dendritic cell based vaccine for prevention of experimental tumor in mice. Iran J Immunol 2008; 5(1):36-44.
11. Arab S, Motamedi M, Khansari N, Moazzeni SM, et al. Dendritic cell maturation with CpG for tumor immunotherapy. Iran J Immunol 2006; 3(3):99-105.
12. Saei A, Boghozian R, Mirzaei R, Jamali A, Vaziri B, Hadjati J. Listeria monocytogenes protein fraction induces dendritic cells maturation and T helper 1 immune responses. Iran J Allergy Asthma Immunol 2014; 13(1):1-10.
13. Dolgin E. The mathematician versus the malignancy. Nat Med 2014; 20(5):460-3.
14. Bonin CRB, Fernandes GC, dos Santos RW, Lobosco M. Mathematical modeling based on ordinary differential equations: A promising approach to vaccinology. Hum Vaccin Immunother 2017; 13(2):484-9.
15. Linde J, Schulze S, Henkel SG, Guthke R. Data-and knowledge-based modeling of gene regulatory networks: an update. EXCLI J 2015; 14:346-78.
16. Debnath L. Nonlinear partial differential equations for scientists and engineers: Springer Science & Business Media; 2011.
17. Dreyfus G. Neural networks: methodology and applications: Springer Science & Business Media; 2005.
18. Falat L, Stanikova Z, Durisova M, Holkova B, Potkanova T. Application of neural network models in modelling economic time series with non-constant volatility. Procedia Economics and Finance. 2015;34:600-7.
19. Zamaniyan A, Joda F, Behroozsarand A, Ebrahimi H. Application of artificial neural networks (ANN) for modeling of industrial hydrogen plant. International Journal of Hydrogen Energy. 2013;38(15):6289-97.
20. Khan J, Wei JS, Ringner M, Saal LH, Ladanyi M, Westermann F, et al. Classification and diagnostic prediction of cancers using gene expression profiling and artificial neural networks. Nat Med 2001; 7(6):673-9.
21. Younis A, Ibrahim M, Kabuka M, John N. An artificial immune-activated neural network applied to brain 3D MRI segmentation. Journal of digital imaging. 2008 Oct 1;21(1):69-88..
22. Pourgholaminejad A, Jamali A, Samadi-Foroushani M, Amari A, Mirzaei R, Ansaripour B, et al. Reduced efficacy of multiple doses of CpG-matured dendritic cell tumor vaccine in an experimental model. Cell Immunol 2011; 271(2):360-4.
23. Mehrian M, Asemani D, Arabameri A, Pourgholaminejad A, Hadjati J. Modeling of tumor growth in dendritic cell-based immunotherapy using artificial neural networks. Comput Biol Chem 2014; 48:21-8.
24. Khan J, Wei JS, Ringner M, Saal LH, Ladanyi M, Westermann F, Berthold F, Schwab M, Antonescu CR, Peterson C, Meltzer PS. Classification and diagnostic prediction of cancers using gene expression profiling and artificial neural networks. Nature medicine. 2001 Jun;7(6):673
25. Nestle FO, Alijagic S, Gilliet M, et al. Vaccination of melanoma patients with peptide-or tumorlysate-pulsed dendritic cells. Nat Med 1998;4(3):328-32.
26. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992; 176(6):1693-702.
27. Inaba K, Inaba M, Naito M, Steinman R. Dendritic cell progenitors phagocytose particulates, including bacillus Calmette-Guerin organisms, and sensitize mice to mycobacterial antigens in vivo. J Exp Med 1993; 178(2):479-88.
28. Shafer-Weaver K, Sayers T, Strobl S, Derby E, Ulderich T, Baseler M, et al. The Granzyme B ELISPOT assay: an alternative to the 51 Cr-release assay for monitoring cell-mediated cytotoxicity. J Transl Med 2003; 1(1):14.
29. Kheshtchin N, Arab S, Ajami M, Mirzaei R, Ashourpour M, Mousavi N, et al. Inhibition of HIF-1α enhances anti-tumor effects of dendritic cell-based vaccination in a mouse model of breast cancer. Cancer Immunology, Immunotherapy. 2016;65(10):1159-67.
30. Jadidi-Niaragh F, Atyabi F, Rastegari A, Kheshtchin N, Arab S, Hassannia H, et al. CD73 specific siRNA loaded chitosan lactate nanoparticles potentiate the antitumor effect of a dendritic cell vaccine in 4T1 breast cancer bearing mice. J Control Release 2017; 246:46-59.
31. Terhune J, Berk E, Czerniecki BJ. Dendritic Cell-Induced Th1 and Th17 Cell Differentiation for Cancer Therapy. Vaccines (Basel) 2013; 1(4):527-49.
32. Macatonia SE, Hosken NA, Litton M, Vieira P, Hsieh C-S, Culpepper JA, et al. Dendritic cells produce IL-12 and direct the development of Th1 cells from naive CD4+ T cells. J Immunol 1995; 154(10):5071-9.
33. Heufler C, Koch F, Stanzl U, Topar G, Wysocka M, Trinchieri G, et al. Interleukin‐12 is produced by dendritic cells and mediates T helper 1 development as well as interferon‐γ production by T helper 1 cells. Eur J Immunol 1996; 26(3):659-68.
34. Wesa A, Galy A. Increased production of pro-inflammatory cytokines and enhanced T cell responses after activation of human dendritic cells with IL-1 and CD40 ligand. BMC Immunol 2002; 3(1):14.
35. Zenewicz LA, Shen H. Innate and adaptive immune responses to Listeria monocytogenes: a short overview. Microbes Infect 2007; 9(10):1208-15.
36. Kopp E, Medzhitov R. Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol 2003; 15(4):396-401.
37. Mancuso G, Gambuzza M, Midiri A, Biondo C, Papasergi S, Akira S, et al. Bacterial recognition by TLR7 in the lysosomes of conventional dendritic cells. Nat Immunol 2009; 10(6):587-94.
38. Krug A, Towarowski A, Britsch S, Rothenfusser S, Hornung V, Bals R, et al. Toll‐like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL‐12. Eur J Immunol 2001; 31(10):3026-37.
39. Marshall JD, Fearon K, Abbate C, Subramanian S, Yee P, Gregorio J, et al. Identification of a novel CpG DNA class and motif that optimally stimulate B cell and plasmacytoid dendritic cell functions. J Leukoc Biol 2003; 73(6):781-92.
40. Wilson S, Levy D. A mathematical model of the enhancement of tumor vaccine efficacy by immunotherapy. Bull Math Biol. 2012;74(7):1485-500.
41. Wilson S, Levy D. Functional Switching and Stability of Regulatory T Cells. Bull Math Biol 2013; 75(10):1891-911.
42. Vo M-C, Lee H-J, Kim J-S, Hoang M-D, Choi N-R, Rhee JH, et al. Dendritic cell vaccination with a toll-like receptor agonist derived from mycobacteria enhances anti-tumor immunity. Oncotarget. 2015;6(32):33781.
2. Mirzaei HR, Mirzaei H, Lee SY, Hadjati J, Till BG. Prospects for chimeric antigen receptor (CAR) γδ T cells: a potential game changer for adoptive T cell cancer immunotherapy. Cancer Lett 2016; 380(2):413-23.
3. Namdar A, Mirzaei R, Memarnejadian A, Boghosian R, Samadi M, Mirzaei HR, et al. Prophylactic DNA vaccine targeting Foxp3+ regulatory T cells depletes myeloid-derived suppressor cells and improves anti-melanoma immune responses in a murine model. Cancer Immunol Immunother 2018; 67(3):367-79.
4. Nourizadeh M, Masoumi F, Memarian A, Alimoghaddam K, Moazzeni SM, Yaghmaie M, et al. In vitro induction of potent tumor-specific cytotoxic T lymphocytes using TLR agonist-activated AML-DC. Target Oncol 2014; 9(3):225-37.
5. Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012; 12(4):265-77.6. Timmerman M, John M, Levy M, Ronald. Dendritic cell vaccines for cancer immunotherapy. Ann Rew Med 1999; 50(1):507-29.
7. Rosenberg SA. Progress in human tumour immunology and immunotherapy. Nature 2001; 411(6835):380-4.
8. Muraille E, Giannino R, Guirnalda P, Leiner I, Jung S, Pamer EG, et al. Distinct in vivo dendritic cell activation by live versus killed Listeria monocytogenes. Eur J Immunol 2005; 35(5):1463-71.
9. Krug A, Rothenfusser S, Selinger S, Bock C, Kerkmann M, Battiany J, et al. CpG-A oligonucleotides induce a monocyte-derived dendritic cell-like phenotype that preferentially activates CD8 T cells. The J Immunol 2003; 170(7):3468-77.10. Khamisabadi M, Arab S, Motamedi M, Khansari N, Moazzeni SM, Gheflati Z, et al. Listeria monocytogenes activated dendritic cell based vaccine for prevention of experimental tumor in mice. Iran J Immunol 2008; 5(1):36-44.
11. Arab S, Motamedi M, Khansari N, Moazzeni SM, et al. Dendritic cell maturation with CpG for tumor immunotherapy. Iran J Immunol 2006; 3(3):99-105.
12. Saei A, Boghozian R, Mirzaei R, Jamali A, Vaziri B, Hadjati J. Listeria monocytogenes protein fraction induces dendritic cells maturation and T helper 1 immune responses. Iran J Allergy Asthma Immunol 2014; 13(1):1-10.
13. Dolgin E. The mathematician versus the malignancy. Nat Med 2014; 20(5):460-3.
14. Bonin CRB, Fernandes GC, dos Santos RW, Lobosco M. Mathematical modeling based on ordinary differential equations: A promising approach to vaccinology. Hum Vaccin Immunother 2017; 13(2):484-9.
15. Linde J, Schulze S, Henkel SG, Guthke R. Data-and knowledge-based modeling of gene regulatory networks: an update. EXCLI J 2015; 14:346-78.
16. Debnath L. Nonlinear partial differential equations for scientists and engineers: Springer Science & Business Media; 2011.
17. Dreyfus G. Neural networks: methodology and applications: Springer Science & Business Media; 2005.
18. Falat L, Stanikova Z, Durisova M, Holkova B, Potkanova T. Application of neural network models in modelling economic time series with non-constant volatility. Procedia Economics and Finance. 2015;34:600-7.
19. Zamaniyan A, Joda F, Behroozsarand A, Ebrahimi H. Application of artificial neural networks (ANN) for modeling of industrial hydrogen plant. International Journal of Hydrogen Energy. 2013;38(15):6289-97.
20. Khan J, Wei JS, Ringner M, Saal LH, Ladanyi M, Westermann F, et al. Classification and diagnostic prediction of cancers using gene expression profiling and artificial neural networks. Nat Med 2001; 7(6):673-9.
21. Younis A, Ibrahim M, Kabuka M, John N. An artificial immune-activated neural network applied to brain 3D MRI segmentation. Journal of digital imaging. 2008 Oct 1;21(1):69-88..
22. Pourgholaminejad A, Jamali A, Samadi-Foroushani M, Amari A, Mirzaei R, Ansaripour B, et al. Reduced efficacy of multiple doses of CpG-matured dendritic cell tumor vaccine in an experimental model. Cell Immunol 2011; 271(2):360-4.
23. Mehrian M, Asemani D, Arabameri A, Pourgholaminejad A, Hadjati J. Modeling of tumor growth in dendritic cell-based immunotherapy using artificial neural networks. Comput Biol Chem 2014; 48:21-8.
24. Khan J, Wei JS, Ringner M, Saal LH, Ladanyi M, Westermann F, Berthold F, Schwab M, Antonescu CR, Peterson C, Meltzer PS. Classification and diagnostic prediction of cancers using gene expression profiling and artificial neural networks. Nature medicine. 2001 Jun;7(6):673
25. Nestle FO, Alijagic S, Gilliet M, et al. Vaccination of melanoma patients with peptide-or tumorlysate-pulsed dendritic cells. Nat Med 1998;4(3):328-32.
26. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992; 176(6):1693-702.
27. Inaba K, Inaba M, Naito M, Steinman R. Dendritic cell progenitors phagocytose particulates, including bacillus Calmette-Guerin organisms, and sensitize mice to mycobacterial antigens in vivo. J Exp Med 1993; 178(2):479-88.
28. Shafer-Weaver K, Sayers T, Strobl S, Derby E, Ulderich T, Baseler M, et al. The Granzyme B ELISPOT assay: an alternative to the 51 Cr-release assay for monitoring cell-mediated cytotoxicity. J Transl Med 2003; 1(1):14.
29. Kheshtchin N, Arab S, Ajami M, Mirzaei R, Ashourpour M, Mousavi N, et al. Inhibition of HIF-1α enhances anti-tumor effects of dendritic cell-based vaccination in a mouse model of breast cancer. Cancer Immunology, Immunotherapy. 2016;65(10):1159-67.
30. Jadidi-Niaragh F, Atyabi F, Rastegari A, Kheshtchin N, Arab S, Hassannia H, et al. CD73 specific siRNA loaded chitosan lactate nanoparticles potentiate the antitumor effect of a dendritic cell vaccine in 4T1 breast cancer bearing mice. J Control Release 2017; 246:46-59.
31. Terhune J, Berk E, Czerniecki BJ. Dendritic Cell-Induced Th1 and Th17 Cell Differentiation for Cancer Therapy. Vaccines (Basel) 2013; 1(4):527-49.
32. Macatonia SE, Hosken NA, Litton M, Vieira P, Hsieh C-S, Culpepper JA, et al. Dendritic cells produce IL-12 and direct the development of Th1 cells from naive CD4+ T cells. J Immunol 1995; 154(10):5071-9.
33. Heufler C, Koch F, Stanzl U, Topar G, Wysocka M, Trinchieri G, et al. Interleukin‐12 is produced by dendritic cells and mediates T helper 1 development as well as interferon‐γ production by T helper 1 cells. Eur J Immunol 1996; 26(3):659-68.
34. Wesa A, Galy A. Increased production of pro-inflammatory cytokines and enhanced T cell responses after activation of human dendritic cells with IL-1 and CD40 ligand. BMC Immunol 2002; 3(1):14.
35. Zenewicz LA, Shen H. Innate and adaptive immune responses to Listeria monocytogenes: a short overview. Microbes Infect 2007; 9(10):1208-15.
36. Kopp E, Medzhitov R. Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol 2003; 15(4):396-401.
37. Mancuso G, Gambuzza M, Midiri A, Biondo C, Papasergi S, Akira S, et al. Bacterial recognition by TLR7 in the lysosomes of conventional dendritic cells. Nat Immunol 2009; 10(6):587-94.
38. Krug A, Towarowski A, Britsch S, Rothenfusser S, Hornung V, Bals R, et al. Toll‐like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL‐12. Eur J Immunol 2001; 31(10):3026-37.
39. Marshall JD, Fearon K, Abbate C, Subramanian S, Yee P, Gregorio J, et al. Identification of a novel CpG DNA class and motif that optimally stimulate B cell and plasmacytoid dendritic cell functions. J Leukoc Biol 2003; 73(6):781-92.
40. Wilson S, Levy D. A mathematical model of the enhancement of tumor vaccine efficacy by immunotherapy. Bull Math Biol. 2012;74(7):1485-500.
41. Wilson S, Levy D. Functional Switching and Stability of Regulatory T Cells. Bull Math Biol 2013; 75(10):1891-911.
42. Vo M-C, Lee H-J, Kim J-S, Hoang M-D, Choi N-R, Rhee JH, et al. Dendritic cell vaccination with a toll-like receptor agonist derived from mycobacteria enhances anti-tumor immunity. Oncotarget. 2015;6(32):33781.
| Files | ||
| Issue | Vol 19, No 2 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v19i2.2770 | |
| PMID | 32372630 | |
| Keywords | ||
| Cancer Cancer vaccines Dendritic cells Listeria monocytogenes | ||
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How to Cite
1.
Mirsanei Z, Habibi S, Kheshtchin N, Mirzaei R, Arab S, Zand B, Jadidi-Niaragh F, Safvati A, Sharif-Paghaleh E, Arabameri A, Asemani D, Hajati J. Optimized Dose of Dendritic Cell-based Vaccination in Experimental Model of Tumor Using Artificial Neural Network. Iran J Allergy Asthma Immunol. 2020;19(2):172-182.
