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Published in: BMC Complementary Medicine and Therapies 1/2020

Open Access 01-12-2020 | Research article

Evaluation of immunomodulatory effects of Boswellia sacra essential oil on T-cells and dendritic cells

Authors: Alia M. Aldahlawi, Amani T. Alzahrani, Mohamed F. Elshal

Published in: BMC Complementary Medicine and Therapies | Issue 1/2020

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Abstract

Background

Boswellia sacra resin has been commonly used as analgesic, antimicrobial, and anti-inflammatory properties, which reflect its immunomodulatory activity. Dendritic cells (DCs) are specialized antigen-presenting cells (APCs) and sentinel cells that regulate the immune response. This study aims at investigating whether crude essential oil extracted from Boswellia sacra resin (BSEO), has a potential effect on the phenotype and functions of human monocyte-derived DCs.

Methods

Oil extract from the resin of Boswellia sacra was prepared by hydrodistillation using a custom made hydrodistiller. BSEO-mediated cell viability has been initially studied on human skin dermis cells (HSD) and DC precursors using quantitative and qualitative assays before applying on DCs. Human DCs were generated from differentiated peripheral blood monocytes cultured in media containing both GM-CSF and IL-4. DCs were exposed to 5 μg/mL or 10 μg/mL of BSEO in vitro. Morphological, phonotypical, and functional properties studied with microscopy, flow cytometry, and ELISA.

Results

Crude BSEO was found to interfere with the maturation and differentiation of DCs from precursor cells in the presence or absence of lipopolysaccharide (LPS). BSEO-treated DCs, cultured in the presence of LPS, reduced the ability of allogeneic T cells to proliferate compared to that co-cultured with LPS-stimulated DCs only. In addition, the endocytic capacity and secretion of IL-10 by DCs treated with BSEO was enhanced in comparison to LPS treated cells. Analysis of the chemical composition of BESO using GC-MS (Clarus 500 GC/MS, PerkinElmer, Shelton, CT) revealed the presence of compounds with several biological activities including antibacterial, antioxidant, and anti-inflammatory properties.

Conclusion

Results indicated that BSEO deviates the differentiation of monocytes into immature DCs. Furthermore, stimulation of immature DCs with BSEO was unable to generate full DC maturation. However, these findings may potentially be employed to generate DCs with tolerogenic properties that are able to induce tolerance in diseases with hypersensitivity, autoimmunity as well as transplantation.
Literature
1.
go back to reference Mannino G, Occhipinti A, Maffei ME. Quantitative Determination of 3-O-Acetyl-11-Keto-βBoswellic Acid (AKBA) and Other Boswellic Acids in Boswellia sacra Flueck (syn. B. carteri Birdw) and Boswellia serrata Roxb. Molecules. 2016;21(10):1329.PubMedCentralCrossRef Mannino G, Occhipinti A, Maffei ME. Quantitative Determination of 3-O-Acetyl-11-Keto-βBoswellic Acid (AKBA) and Other Boswellic Acids in Boswellia sacra Flueck (syn. B. carteri Birdw) and Boswellia serrata Roxb. Molecules. 2016;21(10):1329.PubMedCentralCrossRef
3.
go back to reference Roy S, Khanna S, Krishnaraju AV, Subbaraju GV, Yasmin T, Bagchi D, Sen CK. Regulation of vascular responses to inflammation: inducible matrix metalloproteinase-3 expression in human microvascular endothelial cells is sensitive to antiinflammatory Boswellia. Antioxid Redox Signal. 2006;8(3-4):653–60.PubMedCrossRef Roy S, Khanna S, Krishnaraju AV, Subbaraju GV, Yasmin T, Bagchi D, Sen CK. Regulation of vascular responses to inflammation: inducible matrix metalloproteinase-3 expression in human microvascular endothelial cells is sensitive to antiinflammatory Boswellia. Antioxid Redox Signal. 2006;8(3-4):653–60.PubMedCrossRef
4.
go back to reference Murthy KSR, Reddy MC, Rani SS, Pullaiah T. Bioactive principles and biological properties of essential oils of Burseraceae: a review. J Pharmacognosy Phytochemistry. 2016;5(2):247. Murthy KSR, Reddy MC, Rani SS, Pullaiah T. Bioactive principles and biological properties of essential oils of Burseraceae: a review. J Pharmacognosy Phytochemistry. 2016;5(2):247.
5.
go back to reference Guilliams M, Ginhoux F, Jakubzick C, Naik SH, Onai N, Schraml BU, Segura E, Tussiwand R, Yona S. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol. 2014;14(8):571–8.PubMedPubMedCentralCrossRef Guilliams M, Ginhoux F, Jakubzick C, Naik SH, Onai N, Schraml BU, Segura E, Tussiwand R, Yona S. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol. 2014;14(8):571–8.PubMedPubMedCentralCrossRef
6.
go back to reference Lam IV. In vitro generation of human monocyte-derived dendritic cells within 48 hours: lmu; 2012. Lam IV. In vitro generation of human monocyte-derived dendritic cells within 48 hours: lmu; 2012.
7.
go back to reference Sadhasivam S, Palanivel S, Ghosh S. Synergistic antimicrobial activity of Boswellia serrata Roxb. Ex Colebr.(Burseraceae) essential oil with various azoles against pathogens associated with skin, scalp and nail infections. Lett Appl Microbiol. 2016;63(6):495–501.PubMedCrossRef Sadhasivam S, Palanivel S, Ghosh S. Synergistic antimicrobial activity of Boswellia serrata Roxb. Ex Colebr.(Burseraceae) essential oil with various azoles against pathogens associated with skin, scalp and nail infections. Lett Appl Microbiol. 2016;63(6):495–501.PubMedCrossRef
8.
go back to reference Xia D, Lou W, Fung KM, Wolley CL, Suhail MM, Lin HK. Cancer Chemopreventive Effects of Boswellia sacra Gum Resin Hydrodistillates on Invasive Urothelial Cell Carcinoma: Report of a Case. Integr Cancer Ther. 2017;16(4):605–11.PubMedCrossRef Xia D, Lou W, Fung KM, Wolley CL, Suhail MM, Lin HK. Cancer Chemopreventive Effects of Boswellia sacra Gum Resin Hydrodistillates on Invasive Urothelial Cell Carcinoma: Report of a Case. Integr Cancer Ther. 2017;16(4):605–11.PubMedCrossRef
9.
go back to reference Kurokawa K, Ishii T, An W-W, Kanazawa Y, Ozawa M, Ichiyanagi T, Saito T, Nishihara E. Nakaya K. A heat-stable extract from mucuna stimulates the differentiation of bone marrow cells into dendritic cells and induces apoptosis in cancer cells. Nutr Cancer. 2011;63(1):100–8.PubMed Kurokawa K, Ishii T, An W-W, Kanazawa Y, Ozawa M, Ichiyanagi T, Saito T, Nishihara E. Nakaya K. A heat-stable extract from mucuna stimulates the differentiation of bone marrow cells into dendritic cells and induces apoptosis in cancer cells. Nutr Cancer. 2011;63(1):100–8.PubMed
10.
go back to reference Amirghofran Z, Ahmadi H, Karimi MH. Immunomodulatory activity of the water extract of Thymus vulgaris, Thymus daenensis, and Zataria multiflora on dendritic cells and T cells responses. J Immunoass Immunochem. 2012;33(4):388–402.CrossRef Amirghofran Z, Ahmadi H, Karimi MH. Immunomodulatory activity of the water extract of Thymus vulgaris, Thymus daenensis, and Zataria multiflora on dendritic cells and T cells responses. J Immunoass Immunochem. 2012;33(4):388–402.CrossRef
11.
go back to reference Li Y-R, Chen D-Y, Chu C-L, Li S, Chen Y-K, Wu C-L, Lin C-C. Naringenin inhibits dendritic cell maturation and has therapeutic effects in a murine model of collagen-induced arthritis. J Nutr Biochem. 2015;26(12):1467–78.PubMedCrossRef Li Y-R, Chen D-Y, Chu C-L, Li S, Chen Y-K, Wu C-L, Lin C-C. Naringenin inhibits dendritic cell maturation and has therapeutic effects in a murine model of collagen-induced arthritis. J Nutr Biochem. 2015;26(12):1467–78.PubMedCrossRef
12.
go back to reference An W-W, Kanazawa Y, Ozawa M, Nakaya K, Saito T, Tanaka A, Bradley WG. Dendritic cell differentiation and tumor cell apoptosis induced by components of a poly-phenylpropanoid polysaccharide complex. Anticancer Res. 2010;30(2):613–22.PubMed An W-W, Kanazawa Y, Ozawa M, Nakaya K, Saito T, Tanaka A, Bradley WG. Dendritic cell differentiation and tumor cell apoptosis induced by components of a poly-phenylpropanoid polysaccharide complex. Anticancer Res. 2010;30(2):613–22.PubMed
13.
go back to reference Nakaya K, Nabata Y, Ichiyanagi T, An WW. Stimulation of dendritic cell maturation and induction of apoptosis in leukemia cells by a heat-stable extract from azuki bean (Vigna angularis), a promising immunopotentiating food and dietary supplement for cancer prevention. Asian Pac J Cancer Prev. 2012;13(2):607–11.PubMedCrossRef Nakaya K, Nabata Y, Ichiyanagi T, An WW. Stimulation of dendritic cell maturation and induction of apoptosis in leukemia cells by a heat-stable extract from azuki bean (Vigna angularis), a promising immunopotentiating food and dietary supplement for cancer prevention. Asian Pac J Cancer Prev. 2012;13(2):607–11.PubMedCrossRef
14.
go back to reference Li J, Li J, Zhang F. The immunoregulatory effects of Chinese herbal medicine on the maturation and function of dendritic cells. J Ethnopharmacol. 2015;171:184–95.PubMedCrossRef Li J, Li J, Zhang F. The immunoregulatory effects of Chinese herbal medicine on the maturation and function of dendritic cells. J Ethnopharmacol. 2015;171:184–95.PubMedCrossRef
15.
go back to reference Suhail MM, Wu W, Cao A, Mondalek FG, Fung K-M, Shih P-T, Fang Y-T, Woolley C, Young G, Lin H-K. Boswellia sacra essential oil induces tumor cell-specific apoptosis and suppresses tumor aggressiveness in cultured human breast cancer cells. BMC Complement Altern Med. 2011;11(1):129.PubMedPubMedCentralCrossRef Suhail MM, Wu W, Cao A, Mondalek FG, Fung K-M, Shih P-T, Fang Y-T, Woolley C, Young G, Lin H-K. Boswellia sacra essential oil induces tumor cell-specific apoptosis and suppresses tumor aggressiveness in cultured human breast cancer cells. BMC Complement Altern Med. 2011;11(1):129.PubMedPubMedCentralCrossRef
16.
go back to reference Mahassni SH, Al-Reemi RM. Apoptosis and necrosis of human breast cancer cells by an aqueous extract of garden cress (Lepidium sativum) seeds. Saudi J Biol Sci. 2013;20(2):131–9.PubMedPubMedCentralCrossRef Mahassni SH, Al-Reemi RM. Apoptosis and necrosis of human breast cancer cells by an aqueous extract of garden cress (Lepidium sativum) seeds. Saudi J Biol Sci. 2013;20(2):131–9.PubMedPubMedCentralCrossRef
17.
go back to reference Romani N, Gruner S, Brang D, Kämpgen E, Lenz A, Trockenbacher B, Konwalinka G, Fritsch PO, Steinman RM, Schuler G. Proliferating dendritic cell progenitors in human blood. J Exp Med. 1994;180(1):83–93.PubMedCrossRef Romani N, Gruner S, Brang D, Kämpgen E, Lenz A, Trockenbacher B, Konwalinka G, Fritsch PO, Steinman RM, Schuler G. Proliferating dendritic cell progenitors in human blood. J Exp Med. 1994;180(1):83–93.PubMedCrossRef
18.
go back to reference Delles AM, Rittenhouse-Olson K, Morgan J, Oseroff AR. A simple method for the purification of human peripheral blood antigen presenting cells (dendritic cells, monocytes/macrophages, and B lymphocytes). Immunol Investig. 2002;31(3–4):233–45.CrossRef Delles AM, Rittenhouse-Olson K, Morgan J, Oseroff AR. A simple method for the purification of human peripheral blood antigen presenting cells (dendritic cells, monocytes/macrophages, and B lymphocytes). Immunol Investig. 2002;31(3–4):233–45.CrossRef
19.
go back to reference Romani N, Reider D, Heuer M, Ebner S, Kampgen E, Eibl B, Niederwieser D, Schuler G. Generation of mature dendritic cells from human blood. An improved method with special regard to clinical applicability. J Immunol Methods. 1996;196(2):137–51.PubMedCrossRef Romani N, Reider D, Heuer M, Ebner S, Kampgen E, Eibl B, Niederwieser D, Schuler G. Generation of mature dendritic cells from human blood. An improved method with special regard to clinical applicability. J Immunol Methods. 1996;196(2):137–51.PubMedCrossRef
20.
go back to reference Mohamed SA, Elshal MF, Kumosani TA, Aldahlawi AM, Basbrain TA, Alshehri FA, Choudhry H. L-asparaginase isolated from phaseolus vulgaris seeds exhibited potent anti-acute lymphoblastic leukemia effects in-vitro and low immunogenic properties in-vivo. Int J Environ Res Public Health. 2016;13(10):1008.PubMedCentralCrossRef Mohamed SA, Elshal MF, Kumosani TA, Aldahlawi AM, Basbrain TA, Alshehri FA, Choudhry H. L-asparaginase isolated from phaseolus vulgaris seeds exhibited potent anti-acute lymphoblastic leukemia effects in-vitro and low immunogenic properties in-vivo. Int J Environ Res Public Health. 2016;13(10):1008.PubMedCentralCrossRef
21.
go back to reference Egner W, McKenzie J, Smith S, Beard M, Hart D. Identification of potent mixed leukocyte reaction-stimulatory cells in human bone marrow. Putative differentiation stage of human blood dendritic cells. J Immunol. 1993;150(7):3043–53.PubMed Egner W, McKenzie J, Smith S, Beard M, Hart D. Identification of potent mixed leukocyte reaction-stimulatory cells in human bone marrow. Putative differentiation stage of human blood dendritic cells. J Immunol. 1993;150(7):3043–53.PubMed
22.
go back to reference Piemonti L, Monti P, Allavena P, Leone BE, Caputo A, Di Carlo V. Glucocorticoids increase the endocytic activity of human dendritic cells. Int Immunol. 1999;11(9):1519–26.PubMedCrossRef Piemonti L, Monti P, Allavena P, Leone BE, Caputo A, Di Carlo V. Glucocorticoids increase the endocytic activity of human dendritic cells. Int Immunol. 1999;11(9):1519–26.PubMedCrossRef
23.
go back to reference Koch F, Stanzl U, Jennewein P, Janke K, Heufler C, Kampgen E, Romani N, Schuler G. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J Exp Med. 1996;184(2):741–6.PubMedCrossRef Koch F, Stanzl U, Jennewein P, Janke K, Heufler C, Kampgen E, Romani N, Schuler G. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J Exp Med. 1996;184(2):741–6.PubMedCrossRef
24.
go back to reference Ni X, Suhail MM, Yang Q, Cao A, Fung K-M, Postier RG, Woolley C, Young G, Zhang J, Lin H-K. Frankincense essential oil prepared from hydrodistillation of Boswellia sacra gum resins induces human pancreatic cancer cell death in cultures and in a xenograft murine model. BMC Complement Altern Med. 2012;12(1):253.PubMedPubMedCentralCrossRef Ni X, Suhail MM, Yang Q, Cao A, Fung K-M, Postier RG, Woolley C, Young G, Zhang J, Lin H-K. Frankincense essential oil prepared from hydrodistillation of Boswellia sacra gum resins induces human pancreatic cancer cell death in cultures and in a xenograft murine model. BMC Complement Altern Med. 2012;12(1):253.PubMedPubMedCentralCrossRef
25.
go back to reference Basile AC, Sertie JA, Freitas PC, Zanini AC. Anti-inflammatory activity of oleoresin from Brazilian Copaifera. J Ethnopharmacol. 1988;22(1):101–9.PubMedCrossRef Basile AC, Sertie JA, Freitas PC, Zanini AC. Anti-inflammatory activity of oleoresin from Brazilian Copaifera. J Ethnopharmacol. 1988;22(1):101–9.PubMedCrossRef
26.
go back to reference Chen W, Lu Y, Wu J, Gao M, Wang A, Xu B. Beta-elemene inhibits melanoma growth and metastasis via suppressing vascular endothelial growth factor-mediated angiogenesis. Cancer Chemother Pharmacol. 2011;67(4):799–808.PubMedCrossRef Chen W, Lu Y, Wu J, Gao M, Wang A, Xu B. Beta-elemene inhibits melanoma growth and metastasis via suppressing vascular endothelial growth factor-mediated angiogenesis. Cancer Chemother Pharmacol. 2011;67(4):799–808.PubMedCrossRef
27.
go back to reference Picciolo G, Pallio G, Altavilla D, Vaccaro M, Oteri G, Irrera N, Squadrito F. beta-Caryophyllene Reduces the Inflammatory Phenotype of Periodontal Cells by Targeting CB2 Receptors. Biomedicines. 2020;8(6). Picciolo G, Pallio G, Altavilla D, Vaccaro M, Oteri G, Irrera N, Squadrito F. beta-Caryophyllene Reduces the Inflammatory Phenotype of Periodontal Cells by Targeting CB2 Receptors. Biomedicines. 2020;8(6).
28.
go back to reference Fidyt K, Fiedorowicz A, Strządała L, Szumny A. β-Caryophyllene and β-caryophyllene oxide—natural compounds of anticancer and analgesic properties. Cancer Med. 2016;5(10):3007–17.PubMedPubMedCentralCrossRef Fidyt K, Fiedorowicz A, Strządała L, Szumny A. β-Caryophyllene and β-caryophyllene oxide—natural compounds of anticancer and analgesic properties. Cancer Med. 2016;5(10):3007–17.PubMedPubMedCentralCrossRef
29.
go back to reference Hart PH, Brand C, Carson CF, Riley TV, Prager RH, Finlay-Jones JJ. Terpinen-4-ol, the main component of the essential oil of Melaleuca alternifolia (tea tree oil), suppresses inflammatory mediator production by activated human monocytes. Inflamm Res. 2000;49(11):619–26.PubMedCrossRef Hart PH, Brand C, Carson CF, Riley TV, Prager RH, Finlay-Jones JJ. Terpinen-4-ol, the main component of the essential oil of Melaleuca alternifolia (tea tree oil), suppresses inflammatory mediator production by activated human monocytes. Inflamm Res. 2000;49(11):619–26.PubMedCrossRef
30.
go back to reference George Kallivalappil G, Kuttan G. Evaluation of the anti-inflammatory and urotoxicity ameliorative effects of gamma-humulene containing active fraction of Emilia sonchifolia (L.) DC. Inflammopharmacology. 2019;27(2):409–20.PubMedCrossRef George Kallivalappil G, Kuttan G. Evaluation of the anti-inflammatory and urotoxicity ameliorative effects of gamma-humulene containing active fraction of Emilia sonchifolia (L.) DC. Inflammopharmacology. 2019;27(2):409–20.PubMedCrossRef
31.
go back to reference Rogerio AP, Andrade EL, Leite DF, Figueiredo CP, Calixto JB. Preventive and therapeutic anti-inflammatory properties of the sesquiterpene alpha-humulene in experimental airways allergic inflammation. Br J Pharmacol. 2009;158(4):1074–87.PubMedPubMedCentralCrossRef Rogerio AP, Andrade EL, Leite DF, Figueiredo CP, Calixto JB. Preventive and therapeutic anti-inflammatory properties of the sesquiterpene alpha-humulene in experimental airways allergic inflammation. Br J Pharmacol. 2009;158(4):1074–87.PubMedPubMedCentralCrossRef
32.
go back to reference Afoulous S, Ferhout H, Raoelison EG, Valentin A, Moukarzel B, Couderc F, Bouajila J. Chemical composition and anticancer, antiinflammatory, antioxidant and antimalarial activities of leaves essential oil of Cedrelopsis grevei. Food Chem Toxicol. 2013;56:352–62.PubMedCrossRef Afoulous S, Ferhout H, Raoelison EG, Valentin A, Moukarzel B, Couderc F, Bouajila J. Chemical composition and anticancer, antiinflammatory, antioxidant and antimalarial activities of leaves essential oil of Cedrelopsis grevei. Food Chem Toxicol. 2013;56:352–62.PubMedCrossRef
33.
go back to reference Chandra M, Prakash O, Kumar R, Bachheti RK, Bhushan B, Kumar M, Pant AK. β-Selinene-rich essential oils from the parts of Callicarpa macrophylla and their antioxidant and pharmacological activities. Medicines. 2017;4(3):52.PubMedCentralCrossRef Chandra M, Prakash O, Kumar R, Bachheti RK, Bhushan B, Kumar M, Pant AK. β-Selinene-rich essential oils from the parts of Callicarpa macrophylla and their antioxidant and pharmacological activities. Medicines. 2017;4(3):52.PubMedCentralCrossRef
34.
go back to reference Cane DE, Rawlings BJ, Yang CC. Isolation of (−)-gamma-cadinene and aristolochene from Aspergillus terreus. J Antibiot (Tokyo). 1987;40(9):1331–4.CrossRef Cane DE, Rawlings BJ, Yang CC. Isolation of (−)-gamma-cadinene and aristolochene from Aspergillus terreus. J Antibiot (Tokyo). 1987;40(9):1331–4.CrossRef
35.
go back to reference Boligon AA, Piana M, Brum TF, Froeder AL, Belke BV, Schwanz TG, Mario DN, Alves SH, Athayde ML. Scutia buxifolia Reissek essential oil: in vitro antioxidant and antimicrobial activities. An Acad Bras Cienc. 2014;86(3):1463–9.PubMedCrossRef Boligon AA, Piana M, Brum TF, Froeder AL, Belke BV, Schwanz TG, Mario DN, Alves SH, Athayde ML. Scutia buxifolia Reissek essential oil: in vitro antioxidant and antimicrobial activities. An Acad Bras Cienc. 2014;86(3):1463–9.PubMedCrossRef
36.
go back to reference Darwish RS, Hammoda HM, Ghareeb DA, Abdelhamid ASA, EM BELN, Harraz FM, Shawky E. Efficacy-directed discrimination of the essential oils of three Juniperus species based on their in-vitro antimicrobial and anti-inflammatory activities. J Ethnopharmacol. 2020;259:112971.PubMedCrossRef Darwish RS, Hammoda HM, Ghareeb DA, Abdelhamid ASA, EM BELN, Harraz FM, Shawky E. Efficacy-directed discrimination of the essential oils of three Juniperus species based on their in-vitro antimicrobial and anti-inflammatory activities. J Ethnopharmacol. 2020;259:112971.PubMedCrossRef
37.
go back to reference Yang H, Jung EM, Ahn C, Lee GS, Lee SY, Kim SH, Choi IG, Park MJ, Lee SS, Choi DH, et al. Elemol from Chamaecyparis obtusa ameliorates 2,4-dinitrochlorobenzene-induced atopic dermatitis. Int J Mol Med. 2015;36(2):463–72.PubMedCrossRef Yang H, Jung EM, Ahn C, Lee GS, Lee SY, Kim SH, Choi IG, Park MJ, Lee SS, Choi DH, et al. Elemol from Chamaecyparis obtusa ameliorates 2,4-dinitrochlorobenzene-induced atopic dermatitis. Int J Mol Med. 2015;36(2):463–72.PubMedCrossRef
38.
go back to reference Zhang K, Ge Z, Xue Z, Huang W, Mei M, Zhang Q, Li Y, Li W, Zhang Z, Zhang Z. Chrysin suppresses human CD14+ monocyte-derived dendritic cells and ameliorates experimental autoimmune encephalomyelitis. J Neuroimmunol. 2015;288:13–20.PubMedCrossRef Zhang K, Ge Z, Xue Z, Huang W, Mei M, Zhang Q, Li Y, Li W, Zhang Z, Zhang Z. Chrysin suppresses human CD14+ monocyte-derived dendritic cells and ameliorates experimental autoimmune encephalomyelitis. J Neuroimmunol. 2015;288:13–20.PubMedCrossRef
39.
go back to reference Shirley SA, Montpetit AJ, Lockey R, Mohapatra SS. Curcumin prevents human dendritic cell response to immune stimulants. Biochem Biophys Res Commun. 2008;374(3):431–6.PubMedPubMedCentralCrossRef Shirley SA, Montpetit AJ, Lockey R, Mohapatra SS. Curcumin prevents human dendritic cell response to immune stimulants. Biochem Biophys Res Commun. 2008;374(3):431–6.PubMedPubMedCentralCrossRef
40.
go back to reference Ribas A, Glaspy JA, Lee Y, Dissette VB, Seja E, Vu HT, Tchekmedyian NS, Oseguera D, Comin-Anduix B, Wargo JA. Role of dendritic cell phenotype, determinant spreading, and negative costimulatory blockade in dendritic cell-based melanoma immunotherapy. J Immunother. 2004;27(5):354–67.PubMedCrossRef Ribas A, Glaspy JA, Lee Y, Dissette VB, Seja E, Vu HT, Tchekmedyian NS, Oseguera D, Comin-Anduix B, Wargo JA. Role of dendritic cell phenotype, determinant spreading, and negative costimulatory blockade in dendritic cell-based melanoma immunotherapy. J Immunother. 2004;27(5):354–67.PubMedCrossRef
41.
go back to reference Tze LE, Horikawa K, Domaschenz H, Howard DR, Roots CM, Rigby RJ, Way DA, Ohmura-Hoshino M, Ishido S, Andoniou CE. CD83 increases MHC II and CD86 on dendritic cells by opposing IL-10–driven MARCH1-mediated ubiquitination and degradation. J Exp Med. 2011;208(1):149–65.PubMedPubMedCentralCrossRef Tze LE, Horikawa K, Domaschenz H, Howard DR, Roots CM, Rigby RJ, Way DA, Ohmura-Hoshino M, Ishido S, Andoniou CE. CD83 increases MHC II and CD86 on dendritic cells by opposing IL-10–driven MARCH1-mediated ubiquitination and degradation. J Exp Med. 2011;208(1):149–65.PubMedPubMedCentralCrossRef
42.
go back to reference Kruse M, Rosorius O, Krätzer F, Stelz G, Kuhnt C, Schuler G, Hauber J, Steinkasserer A. Mature dendritic cells infected with herpes simplex virus type 1 exhibit inhibited T-cell stimulatory capacity. J Virol. 2000;74(15):7127–36.PubMedPubMedCentralCrossRef Kruse M, Rosorius O, Krätzer F, Stelz G, Kuhnt C, Schuler G, Hauber J, Steinkasserer A. Mature dendritic cells infected with herpes simplex virus type 1 exhibit inhibited T-cell stimulatory capacity. J Virol. 2000;74(15):7127–36.PubMedPubMedCentralCrossRef
43.
go back to reference Prechtel AT, Turza NM, Theodoridis AA, Steinkasserer A. CD83 knockdown in monocyte-derived dendritic cells by small interfering RNA leads to a diminished T cell stimulation. J Immunol. 2007;178(9):5454–64.PubMedCrossRef Prechtel AT, Turza NM, Theodoridis AA, Steinkasserer A. CD83 knockdown in monocyte-derived dendritic cells by small interfering RNA leads to a diminished T cell stimulation. J Immunol. 2007;178(9):5454–64.PubMedCrossRef
44.
go back to reference Griffin MD, Lutz WH, Phan VA, Bachman LA, McKean DJ, Kumar R. Potent inhibition of dendritic cell differentiation and maturation by vitamin D analogs. Biochem Biophys Res Commun. 2000;270(3):701–8.PubMedCrossRef Griffin MD, Lutz WH, Phan VA, Bachman LA, McKean DJ, Kumar R. Potent inhibition of dendritic cell differentiation and maturation by vitamin D analogs. Biochem Biophys Res Commun. 2000;270(3):701–8.PubMedCrossRef
45.
go back to reference Piemonti L, Monti P, Sironi M, Fraticelli P, Leone BE, Dal Cin E, Allavena P, Di Carlo V. Vitamin D3 affects differentiation, maturation, and function of human monocyte-derived dendritic cells. J Immunol. 2000;164(9):4443–51.PubMedCrossRef Piemonti L, Monti P, Sironi M, Fraticelli P, Leone BE, Dal Cin E, Allavena P, Di Carlo V. Vitamin D3 affects differentiation, maturation, and function of human monocyte-derived dendritic cells. J Immunol. 2000;164(9):4443–51.PubMedCrossRef
46.
go back to reference Xing N, Maldonado ML, Bachman LA, McKean DJ, Kumar R, Griffin MD. Distinctive dendritic cell modulation by vitamin D 3 and glucocorticoid pathways. Biochem Biophys Res Commun. 2002;297(3):645–52.PubMedCrossRef Xing N, Maldonado ML, Bachman LA, McKean DJ, Kumar R, Griffin MD. Distinctive dendritic cell modulation by vitamin D 3 and glucocorticoid pathways. Biochem Biophys Res Commun. 2002;297(3):645–52.PubMedCrossRef
47.
go back to reference Kim G-Y, Kim K-H, Lee S-H, Yoon M-S, Lee H-J, Moon D-O, Lee C-M, Ahn S-C, Park YC, Park Y-M. Curcumin inhibits immunostimulatory function of dendritic cells: MAPKs and translocation of NF-κB as potential targets. J Immunol. 2005;174(12):8116–24.CrossRefPubMed Kim G-Y, Kim K-H, Lee S-H, Yoon M-S, Lee H-J, Moon D-O, Lee C-M, Ahn S-C, Park YC, Park Y-M. Curcumin inhibits immunostimulatory function of dendritic cells: MAPKs and translocation of NF-κB as potential targets. J Immunol. 2005;174(12):8116–24.CrossRefPubMed
48.
go back to reference May KF, Chen L, Zheng P, Liu Y. Anti-4-1BB monoclonal antibody enhances rejection of large tumor burden by promoting survival but not clonal expansion of tumor-specific CD8+ T cells. Cancer Res. 2002;62(12):3459–65.PubMed May KF, Chen L, Zheng P, Liu Y. Anti-4-1BB monoclonal antibody enhances rejection of large tumor burden by promoting survival but not clonal expansion of tumor-specific CD8+ T cells. Cancer Res. 2002;62(12):3459–65.PubMed
49.
go back to reference Bak SP, Barnkob MS, Bai A, Higham EM, Wittrup KD, Chen J. Differential requirement for CD70 and CD80/CD86 in dendritic cell-mediated activation of tumor-tolerized CD8 T cells. J Immunol. 2012;189(4):1708–16.PubMedCrossRef Bak SP, Barnkob MS, Bai A, Higham EM, Wittrup KD, Chen J. Differential requirement for CD70 and CD80/CD86 in dendritic cell-mediated activation of tumor-tolerized CD8 T cells. J Immunol. 2012;189(4):1708–16.PubMedCrossRef
50.
go back to reference Zheng Y, Manzotti CN, Liu M, Burke F, Mead KI, Sansom DM. CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. J Immunol. 2004;172(5):2778–84.PubMedCrossRef Zheng Y, Manzotti CN, Liu M, Burke F, Mead KI, Sansom DM. CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. J Immunol. 2004;172(5):2778–84.PubMedCrossRef
51.
go back to reference Xuan NT, Shumilina E, Nasir O, Bobbala D, Götz F, Lang F. Stimulation of mouse dendritic cells by gum Arabic. Cell Physiol Biochem. 2010;25(6):641–8.PubMedCrossRef Xuan NT, Shumilina E, Nasir O, Bobbala D, Götz F, Lang F. Stimulation of mouse dendritic cells by gum Arabic. Cell Physiol Biochem. 2010;25(6):641–8.PubMedCrossRef
52.
go back to reference Collins AV, Brodie DW, Gilbert RJ, Iaboni A, Manso-Sancho R, Walse B, Stuart DI, van der Merwe PA, Davis SJ. The interaction properties of costimulatory molecules revisited. Immunity. 2002;17(2):201–10.PubMedCrossRef Collins AV, Brodie DW, Gilbert RJ, Iaboni A, Manso-Sancho R, Walse B, Stuart DI, van der Merwe PA, Davis SJ. The interaction properties of costimulatory molecules revisited. Immunity. 2002;17(2):201–10.PubMedCrossRef
53.
go back to reference Gunn MD, Kyuwa S, Tam C, Kakiuchi T, Matsuzawa A, Williams LT, Nakano H. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J Exp Med. 1999;189(3):451–60.PubMedPubMedCentralCrossRef Gunn MD, Kyuwa S, Tam C, Kakiuchi T, Matsuzawa A, Williams LT, Nakano H. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J Exp Med. 1999;189(3):451–60.PubMedPubMedCentralCrossRef
54.
go back to reference Sanchez-Sanchez N, Riol-Blanco L, Rodriguez-Fernandez JL. The multiple personalities of the chemokine receptor CCR7 in dendritic cells. J Immunol. 2006;176(9):5153–9.PubMedCrossRef Sanchez-Sanchez N, Riol-Blanco L, Rodriguez-Fernandez JL. The multiple personalities of the chemokine receptor CCR7 in dendritic cells. J Immunol. 2006;176(9):5153–9.PubMedCrossRef
55.
go back to reference Randolph GJ, Angeli V, Swartz MA. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol. 2005;5(8):617–28.PubMedCrossRef Randolph GJ, Angeli V, Swartz MA. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol. 2005;5(8):617–28.PubMedCrossRef
56.
go back to reference Ohl L, Mohaupt M, Czeloth N, Hintzen G, Kiafard Z, Zwirner J, Blankenstein T, Henning G, Forster R. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity. 2004;21(2):279–88.PubMedCrossRef Ohl L, Mohaupt M, Czeloth N, Hintzen G, Kiafard Z, Zwirner J, Blankenstein T, Henning G, Forster R. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity. 2004;21(2):279–88.PubMedCrossRef
57.
go back to reference Motamedi M, Xu L, Elahi S. Correlation of transferrin receptor (CD71) with Ki67 expression on stimulated human and mouse T cells: the kinetics of expression of T cell activation markers. J Immunol Methods. 2016;437:43–52.PubMedCrossRef Motamedi M, Xu L, Elahi S. Correlation of transferrin receptor (CD71) with Ki67 expression on stimulated human and mouse T cells: the kinetics of expression of T cell activation markers. J Immunol Methods. 2016;437:43–52.PubMedCrossRef
58.
go back to reference Della Bella S, Gennaro M, Vaccari M, Ferraris C, Nicola S, Riva A, Clerici M, Greco M, Villa M. Altered maturation of peripheral blood dendritic cells in patients with breast cancer. Br J Cancer. 2003;89(8):1463–72.PubMedCrossRef Della Bella S, Gennaro M, Vaccari M, Ferraris C, Nicola S, Riva A, Clerici M, Greco M, Villa M. Altered maturation of peripheral blood dendritic cells in patients with breast cancer. Br J Cancer. 2003;89(8):1463–72.PubMedCrossRef
59.
go back to reference Zapala L, Drela N, Bil J, Nowis D, Basak GW, Lasek W. Optimization of activation requirements of immature mouse dendritic JAWSII cells for in vivo application. Oncol Rep. 2011;25(3):831–40.PubMed Zapala L, Drela N, Bil J, Nowis D, Basak GW, Lasek W. Optimization of activation requirements of immature mouse dendritic JAWSII cells for in vivo application. Oncol Rep. 2011;25(3):831–40.PubMed
60.
go back to reference Quah B, Ni K, O’Neill HC. In vitro hematopoiesis produces a distinct class of immature dendritic cells from spleen progenitors with limited T cell stimulation capacity. Int Immunol. 2004;16(4):567–77.PubMedCrossRef Quah B, Ni K, O’Neill HC. In vitro hematopoiesis produces a distinct class of immature dendritic cells from spleen progenitors with limited T cell stimulation capacity. Int Immunol. 2004;16(4):567–77.PubMedCrossRef
61.
go back to reference Sallusto F, Cella M, Danieli C, Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med. 1995;182(2):389–400.PubMedCrossRef Sallusto F, Cella M, Danieli C, Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med. 1995;182(2):389–400.PubMedCrossRef
62.
go back to reference Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. Induction of interleukin 10–producing, nonproliferating CD4+ T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med. 2000;192(9):1213–22.PubMedPubMedCentralCrossRef Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH. Induction of interleukin 10–producing, nonproliferating CD4+ T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med. 2000;192(9):1213–22.PubMedPubMedCentralCrossRef
63.
go back to reference Cassatella MA, Meda L, Bonora S, Ceska M, Constantin G. Interleukin 10 (IL-10) inhibits the release of proinflammatory cytokines from human polymorphonuclear leukocytes. Evidence for an autocrine role of tumor necrosis factor and IL-1 beta in mediating the production of IL-8 triggered by lipopolysaccharide. J Exp Med. 1993;178(6):2207–11.PubMedCrossRef Cassatella MA, Meda L, Bonora S, Ceska M, Constantin G. Interleukin 10 (IL-10) inhibits the release of proinflammatory cytokines from human polymorphonuclear leukocytes. Evidence for an autocrine role of tumor necrosis factor and IL-1 beta in mediating the production of IL-8 triggered by lipopolysaccharide. J Exp Med. 1993;178(6):2207–11.PubMedCrossRef
64.
go back to reference Mocellin S, Panelli MC, Wang E, Nagorsen D, Marincola FM. The dual role of IL-10. Trends Immunol. 2003;24(1):36–43.PubMedCrossRef Mocellin S, Panelli MC, Wang E, Nagorsen D, Marincola FM. The dual role of IL-10. Trends Immunol. 2003;24(1):36–43.PubMedCrossRef
65.
go back to reference Macatonia SE, Hosken NA, Litton M, Vieira P, Hsieh C-S, Culpepper JA, Wysocka M, Trinchieri G, Murphy KM, O'Garra A. Dendritic cells produce IL-12 and direct the development of Th1 cells from naive CD4+ T cells. J Immunol. 1995;154(10):5071–9.PubMed Macatonia SE, Hosken NA, Litton M, Vieira P, Hsieh C-S, Culpepper JA, Wysocka M, Trinchieri G, Murphy KM, O'Garra A. Dendritic cells produce IL-12 and direct the development of Th1 cells from naive CD4+ T cells. J Immunol. 1995;154(10):5071–9.PubMed
66.
go back to reference Watford WT, Moriguchi M, Morinobu A, O’Shea JJ. The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev. 2003;14(5):361–8.PubMedCrossRef Watford WT, Moriguchi M, Morinobu A, O’Shea JJ. The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev. 2003;14(5):361–8.PubMedCrossRef
67.
go back to reference Buelens C, Willems F, Delvaux A, Piérard G, Delville JP, Velu T, Goldman M. Interleukin-10 differentially regulates B7-1 (CD80) and B7-2 (CD86) expression on human peripheral blood dendritic cells. Eur J Immunol. 1995;25(9):2668–72.PubMedCrossRef Buelens C, Willems F, Delvaux A, Piérard G, Delville JP, Velu T, Goldman M. Interleukin-10 differentially regulates B7-1 (CD80) and B7-2 (CD86) expression on human peripheral blood dendritic cells. Eur J Immunol. 1995;25(9):2668–72.PubMedCrossRef
68.
go back to reference Kaliński P, Hilkens CM, Wierenga EA, Kapsenberg ML. T-cell priming by type-1and type-2 polarized dendritic cells: the concept of a third signal. Immunol Today. 1999;20(12):561–7.PubMedCrossRef Kaliński P, Hilkens CM, Wierenga EA, Kapsenberg ML. T-cell priming by type-1and type-2 polarized dendritic cells: the concept of a third signal. Immunol Today. 1999;20(12):561–7.PubMedCrossRef
69.
go back to reference Syrovets T, Büchele B, Krauss C, Laumonnier Y, Simmet T. Acetyl-boswellic acids inhibit lipopolysaccharide-mediated TNF-α induction in monocytes by direct interaction with IκB kinases. J Immunol. 2005;174(1):498–506.PubMedCrossRef Syrovets T, Büchele B, Krauss C, Laumonnier Y, Simmet T. Acetyl-boswellic acids inhibit lipopolysaccharide-mediated TNF-α induction in monocytes by direct interaction with IκB kinases. J Immunol. 2005;174(1):498–506.PubMedCrossRef
70.
go back to reference Al-Yasiry ARM, Kiczorowska B. Frankincense-therapeutic properties. Adv Hyg Exp Med Postepy Hig Med Dosw. 2016;70. Al-Yasiry ARM, Kiczorowska B. Frankincense-therapeutic properties. Adv Hyg Exp Med Postepy Hig Med Dosw. 2016;70.
71.
go back to reference Di Stefano V, Schillaci D, Cusimano MG, Rishan M, Rashan L. In vitro antimicrobial activity of frankincense oils from Boswellia sacra grown in different locations of the Dhofar region (Oman). Antibiotics. 2020;9(4):195.PubMedCentralCrossRef Di Stefano V, Schillaci D, Cusimano MG, Rishan M, Rashan L. In vitro antimicrobial activity of frankincense oils from Boswellia sacra grown in different locations of the Dhofar region (Oman). Antibiotics. 2020;9(4):195.PubMedCentralCrossRef
72.
go back to reference Schmiech M, Lang SJ, Werner K, Rashan LJ, Syrovets T, Simmet T. Comparative analysis of pentacyclic triterpenic acid compositions in oleogum resins of different Boswellia species and their in vitro cytotoxicity against treatment-resistant human breast cancer cells. Molecules. 2019;24(11):2153.PubMedCentralCrossRef Schmiech M, Lang SJ, Werner K, Rashan LJ, Syrovets T, Simmet T. Comparative analysis of pentacyclic triterpenic acid compositions in oleogum resins of different Boswellia species and their in vitro cytotoxicity against treatment-resistant human breast cancer cells. Molecules. 2019;24(11):2153.PubMedCentralCrossRef
73.
go back to reference Ammon HPT. Boswellic extracts and 11-keto-ß-boswellic acids prevent type 1 and type 2 diabetes mellitus by suppressing the expression of proinflammatory cytokines. Phytomedicine. 2019;63:153002.PubMedCrossRef Ammon HPT. Boswellic extracts and 11-keto-ß-boswellic acids prevent type 1 and type 2 diabetes mellitus by suppressing the expression of proinflammatory cytokines. Phytomedicine. 2019;63:153002.PubMedCrossRef
74.
go back to reference Yu G, Xiang W, Zhang T, Zeng L, Yang K, Li J. Effectiveness of Boswellia and Boswellia extract for osteoarthritis patients: a systematic review and meta-analysis. BMC Complement Med Ther. 2020;20(1):225.PubMedPubMedCentralCrossRef Yu G, Xiang W, Zhang T, Zeng L, Yang K, Li J. Effectiveness of Boswellia and Boswellia extract for osteoarthritis patients: a systematic review and meta-analysis. BMC Complement Med Ther. 2020;20(1):225.PubMedPubMedCentralCrossRef
75.
go back to reference Klauke A-L, Racz I, Pradier B, Markert A, Zimmer A, Gertsch J, Zimmer A. The cannabinoid CB2 receptor-selective phytocannabinoid beta-caryophyllene exerts analgesic effects in mouse models of inflammatory and neuropathic pain. Eur Neuropsychopharmacol. 2014;24(4):608–20.PubMedCrossRef Klauke A-L, Racz I, Pradier B, Markert A, Zimmer A, Gertsch J, Zimmer A. The cannabinoid CB2 receptor-selective phytocannabinoid beta-caryophyllene exerts analgesic effects in mouse models of inflammatory and neuropathic pain. Eur Neuropsychopharmacol. 2014;24(4):608–20.PubMedCrossRef
76.
go back to reference Ho CL, Liao PC, Wang EI, Su YC. Composition and antimicrobial activity of the leaf and twig oils of Litsea acutivena from Taiwan. Nat Prod Commun. 2011;6(11):1755–8.PubMed Ho CL, Liao PC, Wang EI, Su YC. Composition and antimicrobial activity of the leaf and twig oils of Litsea acutivena from Taiwan. Nat Prod Commun. 2011;6(11):1755–8.PubMed
77.
go back to reference Choi IY, Lim JH, Hwang S, Lee JC, Cho GS, Kim WK. Anti-ischemic and anti-inflammatory activity of (S)-cis-verbenol. Free Radic Res. 2010;44(5):541–51.PubMedCrossRef Choi IY, Lim JH, Hwang S, Lee JC, Cho GS, Kim WK. Anti-ischemic and anti-inflammatory activity of (S)-cis-verbenol. Free Radic Res. 2010;44(5):541–51.PubMedCrossRef
Metadata
Title
Evaluation of immunomodulatory effects of Boswellia sacra essential oil on T-cells and dendritic cells
Authors
Alia M. Aldahlawi
Amani T. Alzahrani
Mohamed F. Elshal
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2020
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-020-03146-5

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