Skip to main content
Erschienen in: European Journal of Nutrition 3/2018

22.02.2017 | Original Contribution

Effects of Chlorella vulgaris on tumor growth in mammary tumor-bearing Balb/c mice: discussing association of an immune-suppressed protumor microenvironment with serum IFNγ and IgG decrease and spleen IgG potentiation

verfasst von: Ahad Khalilnezhad, Elham Mahmoudian, Nariman Mosaffa, Ali Anissian, Mohsen Rashidi, Davar Amani

Erschienen in: European Journal of Nutrition | Ausgabe 3/2018

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Chlorella vulgaris (CV) has exhibited immune-enhancing and protective activities against cancer and infections. However, there is an increasing concern about the use of Chlorella species in human, regarding its various molecules with antigenic features found in infectious microorganisms. Our goal was to investigate the impact of higher concentrations of CV on tumor growth in spontaneous mouse mammary tumor (SMMT) models.

Methods

Balb/c mice were daily given CV powder at doses of 0, 200, or 300 mg/kg for 42 days (CONTROL, CV200, and CV300 groups, respectively; n = 6/group). On day 14, the SMMT was inoculated. Tumor volume (TV) and body weight (BW) were monitored on 5-day intervals following tumor challenge. On day 43, blood, spleen, lungs, and tumor tissues were collected. Histopathological examinations on lungs and tumor tissues were performed following hematoxylin–eosin staining. Intratumor expression of 27 genes was assessed by real-time PCR. Total IgG, IFNγ, and IL-4 levels in serum and spleen culture supernatant were measured by ELISA.

Results

The TV/BW index showed significant increase in the CV200 group compared to the CONTROL (p = 0.047). The CV200 tumors exhibited more malignant phenotype, higher angiogenesis rate, and lower peritumoral neutrophil and macrophage-to-lymphocyte infiltration ratio compared to the CONTROL. Serum concentrations of IFNγ, IL-4, and IgG were declined, and the spleen IFNγ and IgG production was higher in the CV200 compared to the CONTROL. The IL-1β, IL-10, TGFβ1, FOXP3, HO-1, Gr1, CD11b, PCNA, LCN2, iNOS2, VEGFR2, CD31, and CD105L expressions were markedly increased in the CV200 tumors compared to the CONTROL (p = 0.001, 0.002, 0.006, 0.021, 0.004, 0.030, 0.016, 0.031, 0.025, 0.008, 0.014, 0.022, and 0.037, respectively). The changes in cytokine, IgG and gene expression values considerably correlated with tumor size, as well as with each other.

Conclusions

Our data provided evidence that C. vulgaris at a specific dose (200 mg/kg) promoted tumor growth in a mammary tumor model. This consequence might reflect an immune derangement in favor of developing a protumor microenvironment. However, this hypothesis needs to be further investigated in future.
Literatur
3.
Zurück zum Zitat Voisin MB, Buzoni-Gatel D, Bout D, Velge-Roussel F (2004) Both expansion of regulatory GR1 + CD11b + myeloid cells and anergy of T lymphocytes participate in hyporesponsiveness of the lung-associated immune system during acute toxoplasmosis. Infect Immun 72(9):5487–5492. doi:10.1128/IAI.72.9.5487-5492.2004 CrossRef Voisin MB, Buzoni-Gatel D, Bout D, Velge-Roussel F (2004) Both expansion of regulatory GR1 + CD11b + myeloid cells and anergy of T lymphocytes participate in hyporesponsiveness of the lung-associated immune system during acute toxoplasmosis. Infect Immun 72(9):5487–5492. doi:10.​1128/​IAI.​72.​9.​5487-5492.​2004 CrossRef
4.
Zurück zum Zitat Song X, Krelin Y, Dvorkin T, Bjorkdahl O, Segal S, Dinarello CA, Voronov E, Apte RN (2005) CD11b+/Gr-1 + immature myeloid cells mediate suppression of T cells in mice bearing tumors of IL-1beta-secreting cells. J Immunol 175(12):8200–8208. doi:10.4049/jimmunol.175.12.8200 CrossRef Song X, Krelin Y, Dvorkin T, Bjorkdahl O, Segal S, Dinarello CA, Voronov E, Apte RN (2005) CD11b+/Gr-1 + immature myeloid cells mediate suppression of T cells in mice bearing tumors of IL-1beta-secreting cells. J Immunol 175(12):8200–8208. doi:10.​4049/​jimmunol.​175.​12.​8200 CrossRef
5.
Zurück zum Zitat Wang H-M, Pan J-L, Chen C-Y, Chiu C-C, Yang M-H, Chang H-W, Chang J-S (2010) Identification of anti-lung cancer extract from Chlorella vulgaris C-C by antioxidant property using supercritical carbon dioxide extraction. Process Biochem 45(12):1865–1872. doi:10.1016/j.procbio.2010.05.023 CrossRef Wang H-M, Pan J-L, Chen C-Y, Chiu C-C, Yang M-H, Chang H-W, Chang J-S (2010) Identification of anti-lung cancer extract from Chlorella vulgaris C-C by antioxidant property using supercritical carbon dioxide extraction. Process Biochem 45(12):1865–1872. doi:10.​1016/​j.​procbio.​2010.​05.​023 CrossRef
6.
Zurück zum Zitat Queiroz Jde S, Barbosa CM, Rocha MC, Bincoletto C, Paredes-Gamero EJ, Queiroz ML, Palermo Neto J (2013) Chlorella vulgaris treatment ameliorates the suppressive effects of single and repeated stressors on hematopoiesis. Brain Behav Immun 29:39–50. doi:10.1016/j.bbi.2012.12.001 CrossRef Queiroz Jde S, Barbosa CM, Rocha MC, Bincoletto C, Paredes-Gamero EJ, Queiroz ML, Palermo Neto J (2013) Chlorella vulgaris treatment ameliorates the suppressive effects of single and repeated stressors on hematopoiesis. Brain Behav Immun 29:39–50. doi:10.​1016/​j.​bbi.​2012.​12.​001 CrossRef
7.
Zurück zum Zitat Kang H, Lee CH, Kim JR, Kwon JY, Seo SG, Han JG, Kim BG, Kim JE, Lee KW (2015) Chlorella vulgaris attenuates dermatophagoides farinae-induced atopic dermatitis-like symptoms in NC/Nga mice. Int J Mol Sci 16(9):21021–21034. doi:10.3390/ijms160921021 CrossRef Kang H, Lee CH, Kim JR, Kwon JY, Seo SG, Han JG, Kim BG, Kim JE, Lee KW (2015) Chlorella vulgaris attenuates dermatophagoides farinae-induced atopic dermatitis-like symptoms in NC/Nga mice. Int J Mol Sci 16(9):21021–21034. doi:10.​3390/​ijms160921021 CrossRef
8.
Zurück zum Zitat Vecina JF, Oliveira AG, Araujo TG, Baggio SR, Torello CO, Saad MJ, Queiroz ML (2014) Chlorella modulates insulin signaling pathway and prevents high-fat diet-induced insulin resistance in mice. Life Sci 95(1):45–52. doi:10.1016/j.lfs.2013.11.020 CrossRef Vecina JF, Oliveira AG, Araujo TG, Baggio SR, Torello CO, Saad MJ, Queiroz ML (2014) Chlorella modulates insulin signaling pathway and prevents high-fat diet-induced insulin resistance in mice. Life Sci 95(1):45–52. doi:10.​1016/​j.​lfs.​2013.​11.​020 CrossRef
9.
Zurück zum Zitat Justo GZ, Silva MR, Queiroz ML (2001) Effects of the green algae Chlorella vulgaris on the response of the host hematopoietic system to intraperitoneal ehrlich ascites tumor transplantation in mice. Immunopharmacol Immunotoxicol 23(1):119–132. doi:10.1081/IPH-100102573 CrossRef Justo GZ, Silva MR, Queiroz ML (2001) Effects of the green algae Chlorella vulgaris on the response of the host hematopoietic system to intraperitoneal ehrlich ascites tumor transplantation in mice. Immunopharmacol Immunotoxicol 23(1):119–132. doi:10.​1081/​IPH-100102573 CrossRef
11.
Zurück zum Zitat Souza Queiroz J, Marin Blasco I, Gagliano H, Daviu N, Gomez Roman A, Belda X, Carrasco J, Rocha MC, Palermo Neto J, Armario A (2016) Chlorella vulgaris reduces the impact of stress on hypothalamic-pituitary-adrenal axis and brain c-fos expression. Psychoneuroendocrinology 65:1–8. doi:10.1016/j.psyneuen.2015.12.002 CrossRef Souza Queiroz J, Marin Blasco I, Gagliano H, Daviu N, Gomez Roman A, Belda X, Carrasco J, Rocha MC, Palermo Neto J, Armario A (2016) Chlorella vulgaris reduces the impact of stress on hypothalamic-pituitary-adrenal axis and brain c-fos expression. Psychoneuroendocrinology 65:1–8. doi:10.​1016/​j.​psyneuen.​2015.​12.​002 CrossRef
12.
Zurück zum Zitat Kwak JH, Baek SH, Woo Y, Han JK, Kim BG, Kim OY, Lee JH (2012) Beneficial immunostimulatory effect of short-term Chlorella supplementation: enhancement of natural killer cell activity and early inflammatory response (randomized, double-blinded, placebo-controlled trial). Nutr J 11:53. doi:10.1186/1475-2891-11-53 CrossRef Kwak JH, Baek SH, Woo Y, Han JK, Kim BG, Kim OY, Lee JH (2012) Beneficial immunostimulatory effect of short-term Chlorella supplementation: enhancement of natural killer cell activity and early inflammatory response (randomized, double-blinded, placebo-controlled trial). Nutr J 11:53. doi:10.​1186/​1475-2891-11-53 CrossRef
14.
Zurück zum Zitat Noguchi N, Maruyama I, Yamada A (2014) The influence of chlorella and its hot water extract supplementation on quality of life in patients with breast cancer. Evid Based Complement Alternat Med 2014:704619. doi:10.1155/2014/704619 CrossRef Noguchi N, Maruyama I, Yamada A (2014) The influence of chlorella and its hot water extract supplementation on quality of life in patients with breast cancer. Evid Based Complement Alternat Med 2014:704619. doi:10.​1155/​2014/​704619 CrossRef
15.
Zurück zum Zitat Armstrong PB, Armstrong MT, Pardy RL, Child A, Wainwright N (2002) Immunohistochemical demonstration of a lipopolysaccharide in the cell wall of a eukaryote, the green alga, Chlorella. Biol Bull 203(2):203–204CrossRef Armstrong PB, Armstrong MT, Pardy RL, Child A, Wainwright N (2002) Immunohistochemical demonstration of a lipopolysaccharide in the cell wall of a eukaryote, the green alga, Chlorella. Biol Bull 203(2):203–204CrossRef
17.
Zurück zum Zitat Reyes Suarez E, Bugden SM, Kai FB, Kralovec JA, Noseda MD, Barrow CJ, Grindley TB (2008) First isolation and structural determination of cyclic beta-(1–>2)-glucans from an alga, Chlorella pyrenoidosa. Carbohydr Res 343(15):2623–2633. doi:10.1016/j.carres.2008.07.009 CrossRef Reyes Suarez E, Bugden SM, Kai FB, Kralovec JA, Noseda MD, Barrow CJ, Grindley TB (2008) First isolation and structural determination of cyclic beta-(1–>2)-glucans from an alga, Chlorella pyrenoidosa. Carbohydr Res 343(15):2623–2633. doi:10.​1016/​j.​carres.​2008.​07.​009 CrossRef
18.
Zurück zum Zitat Tabarsa M, Shin I-S, Lee JH, Surayot U, Park W, You S (2015) An immune-enhancing water-soluble α-glucan from Chlorella vulgaris and structural characteristics. Food Sci Biotechnol 24(6):1933–1941. doi:10.1007/s10068-015-0255-0 CrossRef Tabarsa M, Shin I-S, Lee JH, Surayot U, Park W, You S (2015) An immune-enhancing water-soluble α-glucan from Chlorella vulgaris and structural characteristics. Food Sci Biotechnol 24(6):1933–1941. doi:10.​1007/​s10068-015-0255-0 CrossRef
19.
Zurück zum Zitat Hasegawa T, Matsuguchi T, Noda K, Tanaka K, Kumamoto S, Shoyama Y, Yoshikai Y (2002) Toll-like receptor 2 is at least partly involved in the antitumor activity of glycoprotein from Chlorella vulgaris. Int Immunopharmacol 2(4):579–589 doi:10.1016/S1567-5769(02)00002-4 CrossRef Hasegawa T, Matsuguchi T, Noda K, Tanaka K, Kumamoto S, Shoyama Y, Yoshikai Y (2002) Toll-like receptor 2 is at least partly involved in the antitumor activity of glycoprotein from Chlorella vulgaris. Int Immunopharmacol 2(4):579–589 doi:10.​1016/​S1567-5769(02)00002-4 CrossRef
20.
Zurück zum Zitat Hsu HY, Jeyashoke N, Yeh CH, Song YJ, Hua KF, Chao LK (2010) Immunostimulatory bioactivity of algal polysaccharides from Chlorella pyrenoidosa activates macrophages via Toll-like receptor 4. J Agric Food Chem 58(2):927–936. doi:10.1021/jf902952z CrossRef Hsu HY, Jeyashoke N, Yeh CH, Song YJ, Hua KF, Chao LK (2010) Immunostimulatory bioactivity of algal polysaccharides from Chlorella pyrenoidosa activates macrophages via Toll-like receptor 4. J Agric Food Chem 58(2):927–936. doi:10.​1021/​jf902952z CrossRef
22.
Zurück zum Zitat Eroukhmanoff L, Oderup C, Ivars F (2009) T-cell tolerance induced by repeated antigen stimulation: selective loss of Foxp3- conventional CD4 T cells and induction of CD4 T-cell anergy. Eur J Immunol 39(4):1078–1087. doi:10.1002/eji.200838653 CrossRef Eroukhmanoff L, Oderup C, Ivars F (2009) T-cell tolerance induced by repeated antigen stimulation: selective loss of Foxp3- conventional CD4 T cells and induction of CD4 T-cell anergy. Eur J Immunol 39(4):1078–1087. doi:10.​1002/​eji.​200838653 CrossRef
23.
Zurück zum Zitat Noori S, Taghikhani M, Hassan ZM, Allameha A, Mostafaei A (2010) Tehranolide molecule modulates the immune response, reduce regulatory T cell and inhibits tumor growth in vivo. Mol Immunol 47(7–8):1579–1584. doi:10.1016/j.molimm.2010.01.007 CrossRef Noori S, Taghikhani M, Hassan ZM, Allameha A, Mostafaei A (2010) Tehranolide molecule modulates the immune response, reduce regulatory T cell and inhibits tumor growth in vivo. Mol Immunol 47(7–8):1579–1584. doi:10.​1016/​j.​molimm.​2010.​01.​007 CrossRef
24.
Zurück zum Zitat Kruisbeek AM (2001) Isolation of Mouse Mononuclear Cells. In: Coligan JE, Kruisbeek AM, Margulies DH, Shevach EM, Strober W (eds) Current protocols in immunology. Wiley, New York. doi:10.1002/0471142735.im0301s39 Kruisbeek AM (2001) Isolation of Mouse Mononuclear Cells. In: Coligan JE, Kruisbeek AM, Margulies DH, Shevach EM, Strober W (eds) Current protocols in immunology. Wiley, New York. doi:10.​1002/​0471142735.​im0301s39
25.
26.
Zurück zum Zitat Anderson P, Carrillo-Galvez AB, Garcia-Perez A, Cobo M, Martin F (2013) CD105 (endoglin)-negative murine mesenchymal stromal cells define a new multipotent subpopulation with distinct differentiation and immunomodulatory capacities. PLoS One 8(10):e76979. doi:10.1371/journal.pone.0076979 CrossRef Anderson P, Carrillo-Galvez AB, Garcia-Perez A, Cobo M, Martin F (2013) CD105 (endoglin)-negative murine mesenchymal stromal cells define a new multipotent subpopulation with distinct differentiation and immunomodulatory capacities. PLoS One 8(10):e76979. doi:10.​1371/​journal.​pone.​0076979 CrossRef
27.
Zurück zum Zitat Kim S-H, Hong J-H, Lee Y-C (2013) Ursolic acid, a potential PPARγ agonist, suppresses ovalbumin-induced airway inflammation and Penh by down-regulating IL-5, IL-13, and IL-17 in a mouse model of allergic asthma. Eur J Pharmacol 701(1–3):131–143. doi:10.1016/j.ejphar.2012.11.033 CrossRef Kim S-H, Hong J-H, Lee Y-C (2013) Ursolic acid, a potential PPARγ agonist, suppresses ovalbumin-induced airway inflammation and Penh by down-regulating IL-5, IL-13, and IL-17 in a mouse model of allergic asthma. Eur J Pharmacol 701(1–3):131–143. doi:10.​1016/​j.​ejphar.​2012.​11.​033 CrossRef
28.
Zurück zum Zitat Xiong W, Frasch SC, Thomas SM, Bratton DL, Henson PM (2013) Induction of TGF-beta1 synthesis by macrophages in response to apoptotic cells requires activation of the scavenger receptor CD36. PLoS One 8(8):e72772. doi:10.1371/journal.pone.0072772 CrossRef Xiong W, Frasch SC, Thomas SM, Bratton DL, Henson PM (2013) Induction of TGF-beta1 synthesis by macrophages in response to apoptotic cells requires activation of the scavenger receptor CD36. PLoS One 8(8):e72772. doi:10.​1371/​journal.​pone.​0072772 CrossRef
29.
30.
Zurück zum Zitat Patil K, Bellner L, Cullaro G, Gotlinger KH, Dunn MW, Schwartzman ML (2008) Heme oxygenase-1 induction attenuates corneal inflammation and accelerates wound healing after epithelial injury. Invest Ophthalmol Vis Sci 49(8):3379–3386. doi:10.1167/iovs.07-1515 CrossRef Patil K, Bellner L, Cullaro G, Gotlinger KH, Dunn MW, Schwartzman ML (2008) Heme oxygenase-1 induction attenuates corneal inflammation and accelerates wound healing after epithelial injury. Invest Ophthalmol Vis Sci 49(8):3379–3386. doi:10.​1167/​iovs.​07-1515 CrossRef
31.
Zurück zum Zitat Perez-Gomez E, Eleno N, Lopez-Novoa JM, Ramirez JR, Velasco B, Letarte M, Bernabeu C, Quintanilla M (2005) Characterization of murine S-endoglin isoform and its effects on tumor development. Oncogene 24(27):4450–4461 doi:10.1038/sj.onc.1208644 CrossRef Perez-Gomez E, Eleno N, Lopez-Novoa JM, Ramirez JR, Velasco B, Letarte M, Bernabeu C, Quintanilla M (2005) Characterization of murine S-endoglin isoform and its effects on tumor development. Oncogene 24(27):4450–4461 doi:10.​1038/​sj.​onc.​1208644 CrossRef
33.
Zurück zum Zitat Kubatka P, Kapinova A, Kruzliak P, Kello M, Vybohova D, Kajo K, Novak M, Chripkova M, Adamkov M, Pec M, Mojzis J, Bojkova B, Kassayova M, Stollarova N, Dobrota D (2015) Antineoplastic effects of Chlorella pyrenoidosa in the breast cancer model. Nutrition 31(4):560–569. doi:10.1016/j.nut.2014.08.010 CrossRef Kubatka P, Kapinova A, Kruzliak P, Kello M, Vybohova D, Kajo K, Novak M, Chripkova M, Adamkov M, Pec M, Mojzis J, Bojkova B, Kassayova M, Stollarova N, Dobrota D (2015) Antineoplastic effects of Chlorella pyrenoidosa in the breast cancer model. Nutrition 31(4):560–569. doi:10.​1016/​j.​nut.​2014.​08.​010 CrossRef
34.
35.
Zurück zum Zitat Fridman WH, Pages F, Sautes-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12(4):298–306. doi:10.1038/nrc3245 CrossRef Fridman WH, Pages F, Sautes-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12(4):298–306. doi:10.​1038/​nrc3245 CrossRef
36.
Zurück zum Zitat Du JW, Xu KY, Fang LY, Qi XL (2012) Interleukin-17, produced by lymphocytes, promotes tumor growth and angiogenesis in a mouse model of breast cancer. Mol Med Rep 6(5):1099–1102. doi:10.3892/mmr.2012.1036 CrossRef Du JW, Xu KY, Fang LY, Qi XL (2012) Interleukin-17, produced by lymphocytes, promotes tumor growth and angiogenesis in a mouse model of breast cancer. Mol Med Rep 6(5):1099–1102. doi:10.​3892/​mmr.​2012.​1036 CrossRef
38.
Zurück zum Zitat Esquivel-Velazquez M, Ostoa-Saloma P, Palacios-Arreola MI, Nava-Castro KE, Castro JI, Morales-Montor J (2015) The role of cytokines in breast cancer development and progression. J Interferon Cytokine Res 35(1):1–16. doi:10.1089/jir.2014.0026 CrossRef Esquivel-Velazquez M, Ostoa-Saloma P, Palacios-Arreola MI, Nava-Castro KE, Castro JI, Morales-Montor J (2015) The role of cytokines in breast cancer development and progression. J Interferon Cytokine Res 35(1):1–16. doi:10.​1089/​jir.​2014.​0026 CrossRef
39.
Zurück zum Zitat Tu S, Bhagat G, Cui G, Takaishi S, Kurt-Jones EA, Rickman B, Betz KS, Penz-Oesterreicher M, Bjorkdahl O, Fox JG, Wang TC (2008) Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell 14(5):408–419. doi:10.1016/j.ccr.2008.10.011 CrossRef Tu S, Bhagat G, Cui G, Takaishi S, Kurt-Jones EA, Rickman B, Betz KS, Penz-Oesterreicher M, Bjorkdahl O, Fox JG, Wang TC (2008) Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell 14(5):408–419. doi:10.​1016/​j.​ccr.​2008.​10.​011 CrossRef
44.
Zurück zum Zitat Paauwe M, Heijkants RC, Oudt CH, van Pelt GW, Cui C, Theuer CP, Hardwick JC, Sier CF, Hawinkels LJ (2016) Endoglin targeting inhibits tumor angiogenesis and metastatic spread in breast cancer. Oncogene 35(31):4069–4079. doi:10.1038/onc.2015.509 CrossRef Paauwe M, Heijkants RC, Oudt CH, van Pelt GW, Cui C, Theuer CP, Hardwick JC, Sier CF, Hawinkels LJ (2016) Endoglin targeting inhibits tumor angiogenesis and metastatic spread in breast cancer. Oncogene 35(31):4069–4079. doi:10.​1038/​onc.​2015.​509 CrossRef
45.
Zurück zum Zitat Turner N, Grose R (2010) Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 10(2):116–129CrossRef Turner N, Grose R (2010) Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 10(2):116–129CrossRef
46.
Zurück zum Zitat Kohrmann A, Kammerer U, Kapp M, Dietl J, Anacker J (2009) Expression of matrix metalloproteinases (MMPs) in primary human breast cancer and breast cancer cell lines: New findings and review of the literature. BMC Cancer 9:188. doi:10.1186/1471-2407-9-188 CrossRef Kohrmann A, Kammerer U, Kapp M, Dietl J, Anacker J (2009) Expression of matrix metalloproteinases (MMPs) in primary human breast cancer and breast cancer cell lines: New findings and review of the literature. BMC Cancer 9:188. doi:10.​1186/​1471-2407-9-188 CrossRef
47.
Zurück zum Zitat Fernandez CA, Yan L, Louis G, Yang J, Kutok JL, Moses MA (2005) The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin Cancer Res 11(15):5390–5395. doi:10.1158/1078-0432.CCR-04-2391 CrossRef Fernandez CA, Yan L, Louis G, Yang J, Kutok JL, Moses MA (2005) The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin Cancer Res 11(15):5390–5395. doi:10.​1158/​1078-0432.​CCR-04-2391 CrossRef
48.
Zurück zum Zitat Yang J, Bielenberg DR, Rodig SJ, Doiron R, Clifton MC, Kung AL, Strong RK, Zurakowski D, Moses MA (2009) Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci USA 106(10):3913–3918. doi:10.1073/pnas.0810617106 CrossRef Yang J, Bielenberg DR, Rodig SJ, Doiron R, Clifton MC, Kung AL, Strong RK, Zurakowski D, Moses MA (2009) Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci USA 106(10):3913–3918. doi:10.​1073/​pnas.​0810617106 CrossRef
49.
Zurück zum Zitat Oren B, Urosevic J, Mertens C, Mora J, Guiu M, Gomis RR, Weigert A, Schmid T, Grein S, Brune B, Jung M (2016) Tumour stroma-derived lipocalin-2 promotes breast cancer metastasis. J Pathol 239(3):274–285. doi:10.1002/path.4724 CrossRef Oren B, Urosevic J, Mertens C, Mora J, Guiu M, Gomis RR, Weigert A, Schmid T, Grein S, Brune B, Jung M (2016) Tumour stroma-derived lipocalin-2 promotes breast cancer metastasis. J Pathol 239(3):274–285. doi:10.​1002/​path.​4724 CrossRef
50.
Zurück zum Zitat Dillehay KL, Lu S, Dong Z (2014) Anti-tumor effects of a novel small molecule targeting PCNA chromatin association in prostate cancer. Mol Cancer Ther 13(12):2817–2826 doi:molcanther.0522.2014CrossRef Dillehay KL, Lu S, Dong Z (2014) Anti-tumor effects of a novel small molecule targeting PCNA chromatin association in prostate cancer. Mol Cancer Ther 13(12):2817–2826 doi:molcanther.0522.2014CrossRef
53.
Zurück zum Zitat Hemon P, Jean-Louis F, Ramgolam K, Brignone C, Viguier M, Bachelez H, Triebel F, Charron D, Aoudjit F, Al-Daccak R, Michel L (2011) MHC class II engagement by its ligand LAG-3 (CD223) contributes to melanoma resistance to apoptosis. J Immunol 186(9):5173–5183. doi:10.4049/jimmunol.1002050 CrossRef Hemon P, Jean-Louis F, Ramgolam K, Brignone C, Viguier M, Bachelez H, Triebel F, Charron D, Aoudjit F, Al-Daccak R, Michel L (2011) MHC class II engagement by its ligand LAG-3 (CD223) contributes to melanoma resistance to apoptosis. J Immunol 186(9):5173–5183. doi:10.​4049/​jimmunol.​1002050 CrossRef
54.
Zurück zum Zitat Bernabei P, Coccia EM, Rigamonti L, Bosticardo M, Forni G, Pestka S, Krause CD, Battistini A, Novelli F (2001) Interferon-gamma receptor 2 expression as the deciding factor in human T, B, and myeloid cell proliferation or death. J Leukoc Biol 70(6):950–960 Bernabei P, Coccia EM, Rigamonti L, Bosticardo M, Forni G, Pestka S, Krause CD, Battistini A, Novelli F (2001) Interferon-gamma receptor 2 expression as the deciding factor in human T, B, and myeloid cell proliferation or death. J Leukoc Biol 70(6):950–960
56.
Zurück zum Zitat Queiroz ML, da Rocha MC, Torello CO, de Souza Queiroz J, Bincoletto C, Morgano MA, Romano MR, Paredes-Gamero EJ, Barbosa CM, Calgarotto AK (2011) Chlorella vulgaris restores bone marrow cellularity and cytokine production in lead-exposed mice. Food Chem Toxicol 49(11):2934–2941. doi:10.1016/j.fct.2011.06.056 CrossRef Queiroz ML, da Rocha MC, Torello CO, de Souza Queiroz J, Bincoletto C, Morgano MA, Romano MR, Paredes-Gamero EJ, Barbosa CM, Calgarotto AK (2011) Chlorella vulgaris restores bone marrow cellularity and cytokine production in lead-exposed mice. Food Chem Toxicol 49(11):2934–2941. doi:10.​1016/​j.​fct.​2011.​06.​056 CrossRef
57.
Zurück zum Zitat Bunt SK, Clements VK, Hanson EM, Sinha P, Ostrand-Rosenberg S (2009) Inflammation enhances myeloid-derived suppressor cell cross-talk by signaling through Toll-like receptor 4. J Leukoc Biol 85(6):996–1004. doi:10.1189/jlb.0708446 CrossRef Bunt SK, Clements VK, Hanson EM, Sinha P, Ostrand-Rosenberg S (2009) Inflammation enhances myeloid-derived suppressor cell cross-talk by signaling through Toll-like receptor 4. J Leukoc Biol 85(6):996–1004. doi:10.​1189/​jlb.​0708446 CrossRef
58.
Zurück zum Zitat Khalilnezhad A, Mahmoudian E, Mosaffa N, Mohsenifar J, Amani D (2016) Spontaneous mouse mammary tumor cell lysates induce IgG production in spleen mononuclear cells of healthy and tumor-bearing mice. J Immunoassay Immunochem. doi:10.1080/15321819.2016.1266499 Khalilnezhad A, Mahmoudian E, Mosaffa N, Mohsenifar J, Amani D (2016) Spontaneous mouse mammary tumor cell lysates induce IgG production in spleen mononuclear cells of healthy and tumor-bearing mice. J Immunoassay Immunochem. doi:10.​1080/​15321819.​2016.​1266499
59.
Zurück zum Zitat MacSween JM, Eastwood SL (1980) Immunoglobulins associated with human tumours in vivo: IgG concentrations in eluates of colonic carcinomas. Br J Cancer 42(4):503–509CrossRef MacSween JM, Eastwood SL (1980) Immunoglobulins associated with human tumours in vivo: IgG concentrations in eluates of colonic carcinomas. Br J Cancer 42(4):503–509CrossRef
60.
Zurück zum Zitat Huber SA, Bigi G, Lucas ZJ (1980) Tumor-specific suppressor cells induced by immunization with spleen cells from tumor-bearing animals. Cancer Res 40(10):3477–3483 Huber SA, Bigi G, Lucas ZJ (1980) Tumor-specific suppressor cells induced by immunization with spleen cells from tumor-bearing animals. Cancer Res 40(10):3477–3483
61.
Zurück zum Zitat Toge T, Kameda A, Yamada H, Seto Y, Aratani K, Fujita T, Hattori T (1986) Role of the spleen on immunosuppression in esophageal and gastric cancer. The Japanese journal of surgery 16(5):330–335. doi:10.1007/bf02470555 CrossRef Toge T, Kameda A, Yamada H, Seto Y, Aratani K, Fujita T, Hattori T (1986) Role of the spleen on immunosuppression in esophageal and gastric cancer. The Japanese journal of surgery 16(5):330–335. doi:10.​1007/​bf02470555 CrossRef
62.
Zurück zum Zitat Nyhus JK, Wolford CC, Friece CR, Nelson MB, Sampsel JW, Barbera-Guillem E (2001) IgG-recognizing shed tumor-associated antigens can promote tumor invasion and metastasis. Cancer Immunol Immunother 50(7):361–372CrossRef Nyhus JK, Wolford CC, Friece CR, Nelson MB, Sampsel JW, Barbera-Guillem E (2001) IgG-recognizing shed tumor-associated antigens can promote tumor invasion and metastasis. Cancer Immunol Immunother 50(7):361–372CrossRef
63.
Zurück zum Zitat Barbera-Guillem E, Nyhus JK, Wolford CC, Friece CR, Sampsel JW (2002) Vascular endothelial growth factor secretion by tumor-infiltrating macrophages essentially supports tumor angiogenesis, and IgG immune complexes potentiate the process. Cancer Res 62(23):7042–7049 Barbera-Guillem E, Nyhus JK, Wolford CC, Friece CR, Sampsel JW (2002) Vascular endothelial growth factor secretion by tumor-infiltrating macrophages essentially supports tumor angiogenesis, and IgG immune complexes potentiate the process. Cancer Res 62(23):7042–7049
64.
Zurück zum Zitat Dong B, Dai G, Xu L, Zhang Y, Ling L, Sun L, Lv J (2014) Tumor cell lysate induces the immunosuppression and apoptosis of mouse immunocytes. Mol Med Rep 10 (6):2827–2834. doi:10.3892/mmr.2014.2606 CrossRef Dong B, Dai G, Xu L, Zhang Y, Ling L, Sun L, Lv J (2014) Tumor cell lysate induces the immunosuppression and apoptosis of mouse immunocytes. Mol Med Rep 10 (6):2827–2834. doi:10.​3892/​mmr.​2014.​2606 CrossRef
Metadaten
Titel
Effects of Chlorella vulgaris on tumor growth in mammary tumor-bearing Balb/c mice: discussing association of an immune-suppressed protumor microenvironment with serum IFNγ and IgG decrease and spleen IgG potentiation
verfasst von
Ahad Khalilnezhad
Elham Mahmoudian
Nariman Mosaffa
Ali Anissian
Mohsen Rashidi
Davar Amani
Publikationsdatum
22.02.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nutrition / Ausgabe 3/2018
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-017-1387-1

Weitere Artikel der Ausgabe 3/2018

European Journal of Nutrition 3/2018 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Notfall-TEP der Hüfte ist auch bei 90-Jährigen machbar

26.04.2024 Hüft-TEP Nachrichten

Ob bei einer Notfalloperation nach Schenkelhalsfraktur eine Hemiarthroplastik oder eine totale Endoprothese (TEP) eingebaut wird, sollte nicht allein vom Alter der Patientinnen und Patienten abhängen. Auch über 90-Jährige können von der TEP profitieren.

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Bei schweren Reaktionen auf Insektenstiche empfiehlt sich eine spezifische Immuntherapie

Insektenstiche sind bei Erwachsenen die häufigsten Auslöser einer Anaphylaxie. Einen wirksamen Schutz vor schweren anaphylaktischen Reaktionen bietet die allergenspezifische Immuntherapie. Jedoch kommt sie noch viel zu selten zum Einsatz.

Therapiestart mit Blutdrucksenkern erhöht Frakturrisiko

25.04.2024 Hypertonie Nachrichten

Beginnen ältere Männer im Pflegeheim eine Antihypertensiva-Therapie, dann ist die Frakturrate in den folgenden 30 Tagen mehr als verdoppelt. Besonders häufig stürzen Demenzkranke und Männer, die erstmals Blutdrucksenker nehmen. Dafür spricht eine Analyse unter US-Veteranen.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.