The Influences of Omega-3 Polyunsaturated Fatty Acids on the Development of Skin Cancers
Abstract
:1. Introduction
2. Omega-3 Fatty Acids
3. Influence of Omega-3 Fatty Acids on Skin Cancers
3.1. Malignant Melanoma
3.2. Basal Cell Carcinoma and Omega-3 Fatty Acids
3.3. ATLL and Omega-3 Fatty Acids
3.4. Diffuse Large B-Cell Lymphoma and Omega-3 Fatty Acids
3.5. Cutaneous Squamous Cell Carcinoma (SCC)
4. Summary of the Effect of Omega-3 Fatty Acids against Each Skin Cancer
5. Epigenetic Modification by Omega-3 Fatty Acids
6. P53 and Omega-3 PUFAs
7. ERK Inhibition and Omega-3 PUFAs
8. Adhesion Molecule and Omega-3 PUFAs
9. Anti-Tumor Immunity and Omega-3 PUFAs
10. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Egawa, G.; Kabashima, K. Skin as a peripheral lymphoid organ: Revisiting the concept of skin-associated lymphoid tissues. J. Investig. Dermatol. 2011, 131, 2178–2185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kabashima, K.; Honda, T.; Ginhoux, F.; Egawa, G. The immunological anatomy of the skin. Nat. Rev. Immunol. 2019, 19, 19–30. [Google Scholar] [CrossRef] [PubMed]
- Dainichi, T.; Kitoh, A.; Otsuka, A.; Nakajima, S.; Nomura, T.; Kaplan, D.H.; Kabashima, K. The epithelial immune microenvironment (EIME) in atopic dermatitis and psoriasis. Nat. Immunol. 2018, 19, 1286–1298. [Google Scholar] [CrossRef]
- Vasseur, P.; Pohin, M.; Jégou, J.F.; Favot, L.; Venisse, N.; McHeik, J.; Morel, F.; Lecron, J.C.; Silvain, C. Liver fibrosis is associated with cutaneous inflammation in the imiquimod-induced murine model of psoriasiform dermatitis. Br. J. Dermatol. 2018, 179, 101–109. [Google Scholar] [CrossRef] [PubMed]
- Ren, F.; Zhang, M.; Zhang, C.; Sang, H. Psoriasis-Like Inflammation Induced Renal Dysfunction through the TLR/NF-κB Signal Pathway. Biomed. Res. Int. 2020, 2020, 3535264. [Google Scholar] [CrossRef] [Green Version]
- Sawada, Y.; Nakamura, M.; Tokura, Y. Generalized fixed drug eruption caused by pazufloxacin. Acta Derm.-Venereol. 2011, 91, 600–601. [Google Scholar] [CrossRef] [Green Version]
- Sawada, Y.; Honda, T.; Nakamizo, S.; Nakajima, S.; Nonomura, Y.; Otsuka, A.; Egawa, G.; Yoshimoto, T.; Nakamura, M.; Narumiya, S.; et al. Prostaglandin E(2) (PGE(2))-EP2 signaling negatively regulates murine atopic dermatitis-like skin inflammation by suppressing thymic stromal lymphopoietin expression. J. Allergy Clin. Immunol. 2019, 144, 1265–1273.e1269. [Google Scholar] [CrossRef] [Green Version]
- Ueharaguchi, Y.; Honda, T.; Kusuba, N.; Hanakawa, S.; Adachi, A.; Sawada, Y.; Otsuka, A.; Kitoh, A.; Dainichi, T.; Egawa, G.; et al. Thromboxane A(2) facilitates IL-17A production from Vγ4(+) γδ T cells and promotes psoriatic dermatitis in mice. J. Allergy Clin. Immunol. 2018, 142, 680–683.e2. [Google Scholar] [CrossRef] [Green Version]
- Sawada, Y.; Saito-Sasaki, N.; Mashima, E.; Nakamura, M. Daily Lifestyle and Inflammatory Skin Diseases. Int. J. Mol. Sci. 2021, 22, 5204. [Google Scholar] [CrossRef]
- Wada, A.; Sawada, Y.; Sugino, H.; Nakamura, M. Angioedema and Fatty Acids. Int. J. Mol. Sci. 2021, 22, 9000. [Google Scholar] [CrossRef]
- Sawada, Y.; Saito-Sasaki, N.; Nakamura, M. Omega 3 Fatty Acid and Skin Diseases. Front. Immunol. 2020, 11, 623052. [Google Scholar] [CrossRef]
- Saito-Sasaki, N.; Sawada, Y.; Mashima, E.; Yamaguchi, T.; Ohmori, S.; Yoshioka, H.; Haruyama, S.; Okada, E.; Nakamura, M. Maresin-1 suppresses imiquimod-induced skin inflammation by regulating IL-23 receptor expression. Sci. Rep. 2018, 8, 5522. [Google Scholar] [CrossRef]
- Sawada, Y.; Honda, T.; Nakamizo, S.; Otsuka, A.; Ogawa, N.; Kobayashi, Y.; Nakamura, M.; Kabashima, K. Resolvin E1 attenuates murine psoriatic dermatitis. Sci. Rep. 2018, 8, 11873. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sawada, Y.; Honda, T.; Hanakawa, S.; Nakamizo, S.; Murata, T.; Ueharaguchi-Tanada, Y.; Ono, S.; Amano, W.; Nakajima, S.; Egawa, G.; et al. Resolvin E1 inhibits dendritic cell migration in the skin and attenuates contact hypersensitivity responses. J. Exp. Med. 2015, 212, 1921–1930. [Google Scholar] [CrossRef] [Green Version]
- Sawada, Y.; Nakamura, M. Daily Lifestyle and Cutaneous Malignancies. Int. J. Mol. Sci. 2021, 22, 5227. [Google Scholar] [CrossRef]
- Nguyen, Q.V.; Malau-Aduli, B.S.; Cavalieri, J.; Malau-Aduli, A.E.O.; Nichols, P.D. Enhancing Omega-3 Long-Chain Polyunsaturated Fatty Acid Content of Dairy-Derived Foods for Human Consumption. Nutrients 2019, 11, 743. [Google Scholar] [CrossRef] [Green Version]
- Simopoulos, A.P. Omega-3 fatty acids in inflammation and autoimmune diseases. J. Am. Coll. Nutr. 2002, 21, 495–505. [Google Scholar] [CrossRef] [PubMed]
- Jenkins, R.W.; Fisher, D.E. Treatment of Advanced Melanoma in 2020 and Beyond. J. Investig. Dermatol. 2020, 141, 23–31. [Google Scholar] [CrossRef] [PubMed]
- Simiczyjew, A.; Dratkiewicz, E.; Mazurkiewicz, J.; Ziętek, M.; Matkowski, R.; Nowak, D. The Influence of Tumor Microenvironment on Immune Escape of Melanoma. Int. J. Mol. Sci. 2020, 21, 8359. [Google Scholar] [CrossRef]
- Chapman, P.B.; Hauschild, A.; Robert, C.; Haanen, J.B.; Ascierto, P.; Larkin, J.; Dummer, R.; Garbe, C.; Testori, A.; Maio, M.; et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med. 2011, 364, 2507–2516. [Google Scholar] [CrossRef] [Green Version]
- Peyssonnaux, C.; Eychène, A. The Raf/MEK/ERK pathway: New concepts of activation. Biol. Cell 2001, 93, 53–62. [Google Scholar] [CrossRef]
- Jung, T.; Haist, M.; Kuske, M.; Grabbe, S.; Bros, M. Immunomodulatory Properties of BRAF and MEK Inhibitors Used for Melanoma Therapy-Paradoxical ERK Activation and Beyond. Int. J. Mol. Sci. 2021, 22, 9890. [Google Scholar] [CrossRef] [PubMed]
- Hayward, N.K.; Wilmott, J.S.; Waddell, N.; Johansson, P.A.; Field, M.A.; Nones, K.; Patch, A.M.; Kakavand, H.; Alexandrov, L.B.; Burke, H.; et al. Whole-genome landscapes of major melanoma subtypes. Nature 2017, 545, 175–180. [Google Scholar] [CrossRef] [PubMed]
- Beadling, C.; Jacobson-Dunlop, E.; Hodi, F.S.; Le, C.; Warrick, A.; Patterson, J.; Town, A.; Harlow, A.; Cruz, F., 3rd; Azar, S.; et al. KIT gene mutations and copy number in melanoma subtypes. Clin. Cancer Res. 2008, 14, 6821–6828. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pires da Silva, I.; Ahmed, T.; Reijers, I.L.M.; Weppler, A.M.; Betof Warner, A.; Patrinely, J.R.; Serra-Bellver, P.; Allayous, C.; Mangana, J.; Nguyen, K.; et al. Ipilimumab alone or ipilimumab plus anti-PD-1 therapy in patients with metastatic melanoma resistant to anti-PD-(L)1 monotherapy: A multicentre, retrospective, cohort study. Lancet Oncol. 2021, 22, 836–847. [Google Scholar] [CrossRef]
- Yang, G.; Zhang, G.; Pittelkow, M.R.; Ramoni, M.; Tsao, H. Expression profiling of UVB response in melanocytes identifies a set of p53-target genes. J. Investig. Dermatol. 2006, 126, 2490–2506. [Google Scholar] [CrossRef] [Green Version]
- Donat-Vargas, C.; Berglund, M.; Glynn, A.; Wolk, A.; Åkesson, A. Dietary polychlorinated biphenyls, long-chain n-3 polyunsaturated fatty acids and incidence of malignant melanoma. Eur. J. Cancer 2017, 72, 137–143. [Google Scholar] [CrossRef]
- Wang, Y.; Li, L.; Jiang, W.; Yang, Z.; Zhang, Z. Synthesis and preliminary antitumor activity evaluation of a DHA and doxorubicin conjugate. Bioorganic Med. Chem. Lett. 2006, 16, 2974–2977. [Google Scholar] [CrossRef]
- Homsi, J.; Bedikian, A.Y.; Kim, K.B.; Papadopoulos, N.E.; Hwu, W.J.; Mahoney, S.L.; Hwu, P. Phase 2 open-label study of weekly docosahexaenoic acid-paclitaxel in cutaneous and mucosal metastatic melanoma patients. Melanoma Res. 2009, 19, 238–242. [Google Scholar] [CrossRef]
- Homsi, J.; Bedikian, A.Y.; Papadopoulos, N.E.; Kim, K.B.; Hwu, W.J.; Mahoney, S.L.; Hwu, P. Phase 2 open-label study of weekly docosahexaenoic acid-paclitaxel in patients with metastatic uveal melanoma. Melanoma Res. 2010, 20, 507–510. [Google Scholar] [CrossRef]
- Bedikian, A.Y.; DeConti, R.C.; Conry, R.; Agarwala, S.; Papadopoulos, N.; Kim, K.B.; Ernstoff, M. Phase 3 study of docosahexaenoic acid-paclitaxel versus dacarbazine in patients with metastatic malignant melanoma. Ann. Oncol. Off. J. Eur. Soc. Med. Oncol. 2011, 22, 787–793. [Google Scholar] [CrossRef] [PubMed]
- Tezabwala, B.U.; Bennett, M.; Grundy, S.M. Immunotoxicity of polyunsaturated fatty acids in serum-free medium. Immunopharmacol. Immunotoxicol. 1995, 17, 365–383. [Google Scholar] [CrossRef] [PubMed]
- Reich, R.; Royce, L.; Martin, G.R. Eicosapentaenoic acid reduces the invasive and metastatic activities of malignant tumor cells. Biochem. Biophys. Res. Commun. 1989, 160, 559–564. [Google Scholar] [CrossRef]
- Denkins, Y.; Kempf, D.; Ferniz, M.; Nileshwar, S.; Marchetti, D. Role of omega-3 polyunsaturated fatty acids on cyclooxygenase-2 metabolism in brain-metastatic melanoma. J. Lipid Res. 2005, 46, 1278–1284. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Serini, S.; Fasano, E.; Piccioni, E.; Monego, G.; Cittadini, A.R.; Celleno, L.; Ranelletti, F.O.; Calviello, G. DHA induces apoptosis and differentiation in human melanoma cells in vitro: Involvement of HuR-mediated COX-2 mRNA stabilization and β-catenin nuclear translocation. Carcinogenesis 2012, 33, 164–173. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Chen, C.Y.; Arita, M.; Kim, K.; Li, X.; Zhang, H.; Kang, J.X. An omega-3 polyunsaturated fatty acid derivative, 18-HEPE, protects against CXCR4-associated melanoma metastasis. Carcinogenesis 2018, 39, 1380–1388. [Google Scholar] [CrossRef]
- Serini, S.; Zinzi, A.; Vasconcelos, R.O.; Fasano, E.; Riillo, M.G.; Celleno, L.; Trombino, S.; Cassano, R.; Calviello, G. Role of β-catenin signaling in the anti-invasive effect of the omega-3 fatty acid DHA in human melanoma cells. J. Dermatol. Sci. 2016, 84, 149–159. [Google Scholar] [CrossRef]
- Tan, R.H.; Wang, F.; Fan, C.L.; Zhang, X.H.; Zhao, J.S.; Zhang, J.J.; Yang, Y.; Xi, Y.; Zou, Z.Q.; Bu, S.Z. Algal oil rich in n-3 polyunsaturated fatty acids suppresses B16F10 melanoma lung metastasis by autophagy induction. Food Funct. 2018, 9, 6179–6186. [Google Scholar] [CrossRef]
- Bachi, A.L.; Kim, F.J.; Nonogaki, S.; Carneiro, C.R.; Lopes, J.D.; Jasiulionis, M.G.; Correa, M. Leukotriene B4 creates a favorable microenvironment for murine melanoma growth. Mol. Cancer Res. 2009, 7, 1417–1424. [Google Scholar] [CrossRef] [Green Version]
- Puskás, L.G.; Fehér, L.Z.; Vizler, C.; Ayaydin, F.; Rásó, E.; Molnár, E.; Magyary, I.; Kanizsai, I.; Gyuris, M.; Madácsi, R.; et al. Polyunsaturated fatty acids synergize with lipid droplet binding thalidomide analogs to induce oxidative stress in cancer cells. Lipids Health Dis. 2010, 9, 56. [Google Scholar] [CrossRef] [Green Version]
- Zajdel, A.; Wilczok, A.; Chodurek, E.; Gruchlik, A.; Dzierzewicz, Z. Polyunsaturated fatty acids inhibit melanoma cell growth in vitro. Acta Pol. Pharm. 2013, 70, 365–369. [Google Scholar] [PubMed]
- Xia, S.; Lu, Y.; Wang, J.; He, C.; Hong, S.; Serhan, C.N.; Kang, J.X. Melanoma growth is reduced in fat-1 transgenic mice: Impact of omega-6/omega-3 essential fatty acids. Proc. Natl. Acad. Sci. USA 2006, 103, 12499–12504. [Google Scholar] [CrossRef] [Green Version]
- Almeida, E.B.; Silva, K.P.H.; Paixão, V.; Amaral, J.B.D.; Rossi, M.; Xavier-Navarro, R.A.; Barros, K.V.; Silveira, V.L.F.; Vieira, R.P.; Oliveira, L.V.F.; et al. A Mixture of Polyunsaturated Fatty Acids ω-3 and ω-6 Reduces Melanoma Growth by Inhibiting Inflammatory Mediators in the Murine Tumor Microenvironment. Int. J. Mol. Sci. 2019, 20, 3765. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Albino, A.P.; Juan, G.; Traganos, F.; Reinhart, L.; Connolly, J.; Rose, D.P.; Darzynkiewicz, Z. Cell cycle arrest and apoptosis of melanoma cells by docosahexaenoic acid: Association with decreased pRb phosphorylation. Cancer Res. 2000, 60, 4139–4145. [Google Scholar] [PubMed]
- Nehra, D.; Pan, A.H.; Le, H.D.; Fallon, E.M.; Carlson, S.J.; Kalish, B.T.; Puder, M. Docosahexaenoic acid, G protein-coupled receptors, and melanoma: Is G protein-coupled receptor 40 a potential therapeutic target? J. Surg. Res. 2014, 188, 451–458. [Google Scholar] [CrossRef] [Green Version]
- Vasconcelos, R.O.; Serini, S.; de Souza Votto, A.P.; Trindade, G.S.; Fanali, C.; Sgambato, A.; Calviello, G. Combination of ω-3 fatty acids and cisplatin as a potential alternative strategy for personalized therapy of metastatic melanoma: An in-vitro study. Melanoma Res. 2019, 29, 270–280. [Google Scholar] [CrossRef]
- Yang, C.J.; Kuo, C.T.; Wu, L.H.; Chen, M.C.; Pangilinan, C.R.; Phacharapiyangkul, N.; Liu, W.; Chen, Y.H.; Lee, C.H. Eicosapentaenoic acids enhance chemosensitivity through connexin 43 upregulation in murine melanoma models. Int. J. Med. Sci. 2019, 16, 636–643. [Google Scholar] [CrossRef] [Green Version]
- Baumgartner, M.; Sturlan, S.; Roth, E.; Wessner, B.; Bachleitner-Hofmann, T. Enhancement of arsenic trioxide-mediated apoptosis using docosahexaenoic acid in arsenic trioxide-resistant solid tumor cells. Int. J. Cancer 2004, 112, 707–712. [Google Scholar] [CrossRef]
- Salem, M.L.; Kishihara, K.; Abe, K.; Matsuzaki, G.; Nomoto, K. N-3 polyunsaturated fatty acids accentuate B16 melanoma growth and metastasis through suppression of tumoricidal function of T cells and macrophages. Anticancer Res. 2000, 20, 3195–3203. [Google Scholar]
- Sulciner, M.L.; Serhan, C.N.; Gilligan, M.M.; Mudge, D.K.; Chang, J.; Gartung, A.; Lehner, K.A.; Bielenberg, D.R.; Schmidt, B.; Dalli, J.; et al. Resolvins suppress tumor growth and enhance cancer therapy. J. Exp. Med. 2018, 215, 115–140. [Google Scholar] [CrossRef]
- Sekulic, A.; Migden, M.R.; Oro, A.E.; Dirix, L.; Lewis, K.D.; Hainsworth, J.D.; Solomon, J.A.; Yoo, S.; Arron, S.T.; Friedlander, P.A.; et al. Efficacy and safety of vismodegib in advanced basal-cell carcinoma. N. Engl. J. Med. 2012, 366, 2171–2179. [Google Scholar] [CrossRef] [Green Version]
- Zhang, H.; Ping, X.L.; Lee, P.K.; Wu, X.L.; Yao, Y.J.; Zhang, M.J.; Silvers, D.N.; Ratner, D.; Malhotra, R.; Peacocke, M.; et al. Role of P.PTCH and p53 genes in early-onset basal cell carcinoma. Am. J. Pathol. 2001, 158, 381–385. [Google Scholar] [CrossRef] [Green Version]
- Ouhtit, A.; Nakazawa, H.; Armstrong, B.K.; Kricker, A.; Tan, E.; Yamasaki, H.; English, D.R. UV-radiation-specific p53 mutation frequency in normal skin as a predictor of risk of basal cell carcinoma. J. Natl. Cancer Inst. 1998, 90, 523–531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agar, N.S.; Halliday, G.M.; Barnetson, R.S.; Ananthaswamy, H.N.; Wheeler, M.; Jones, A.M. The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: A role for UVA in human skin carcinogenesis. Proc. Natl. Acad. Sci. USA 2004, 101, 4954–4959. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wallingford, S.C.; Hughes, M.C.; Green, A.C.; van der Pols, J.C. Plasma omega-3 and omega-6 concentrations and risk of cutaneous basal and squamous cell carcinomas in Australian adults. Cancer Epidemiol. Prev. Biomark. 2013, 22, 1900–1905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seviiri, M.; Law, M.H.; Ong, J.S.; Gharahkhani, P.; Nyholt, D.R.; Olsen, C.M.; Whiteman, D.C.; MacGregor, S. Polyunsaturated Fatty Acid Levels and the Risk of Keratinocyte Cancer: A Mendelian Randomization Analysis. Cancer Epidemiol. Prev. Biomark. 2021, 30, 1591–1598. [Google Scholar] [CrossRef]
- Willemze, R.; Jaffe, E.S.; Burg, G.; Cerroni, L.; Berti, E.; Swerdlow, S.H.; Ralfkiaer, E.; Chimenti, S.; Diaz-Perez, J.L.; Duncan, L.M.; et al. WHO-EORTC classification for cutaneous lymphomas. Blood 2005, 105, 3768–3785. [Google Scholar] [CrossRef] [Green Version]
- Cook, L.B.; Fuji, S.; Hermine, O.; Bazarbachi, A.; Ramos, J.C.; Ratner, L.; Horwitz, S.; Fields, P.; Tanase, A.; Bumbea, H.; et al. Revised Adult T-Cell Leukemia-Lymphoma International Consensus Meeting Report. J. Clin. Oncol. 2019, 37, 677–687. [Google Scholar] [CrossRef]
- Sawada, Y.; Hino, R.; Hama, K.; Ohmori, S.; Fueki, H.; Yamada, S.; Fukamachi, S.; Tajiri, M.; Kubo, R.; Yoshioka, M.; et al. Type of skin eruption is an independent prognostic indicator for adult T-cell leukemia/lymphoma. Blood 2011, 117, 3961–3967. [Google Scholar] [CrossRef]
- Sawada, Y.; Shimauchi, T.; Yamaguchi, T.; Okura, R.; Hama-Yamamoto, K.; Fueki-Yoshioka, H.; Ohmori, S.; Yamada, S.; Yoshizawa, M.; Hiromasa, K.; et al. Combination of skin-directed therapy and oral etoposide for smoldering adult T-cell leukemia/lymphoma with skin involvement. Leuk. Lymphoma 2013, 54, 520–527. [Google Scholar] [CrossRef]
- Tokura, Y.; Sawada, Y.; Shimauchi, T. Skin manifestations of adult T-cell leukemia/lymphoma: Clinical, cytological and immunological features. J. Dermatol. 2014, 41, 19–25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamada, Y.; Tomonaga, M.; Fukuda, H.; Hanada, S.; Utsunomiya, A.; Tara, M.; Sano, M.; Ikeda, S.; Takatsuki, K.; Kozuru, M.; et al. A new G-CSF-supported combination chemotherapy, LSG15, for adult T-cell leukaemia-lymphoma: Japan Clinical Oncology Group Study 9303. Br. J. Haematol. 2001, 113, 375–382. [Google Scholar] [CrossRef]
- Tsukasaki, K.; Utsunomiya, A.; Fukuda, H.; Shibata, T.; Fukushima, T.; Takatsuka, Y.; Ikeda, S.; Masuda, M.; Nagoshi, H.; Ueda, R.; et al. VCAP-AMP-VECP compared with biweekly CHOP for adult T-cell leukemia-lymphoma: Japan Clinical Oncology Group Study JCOG9801. J. Clin. Oncol. 2007, 25, 5458–5464. [Google Scholar] [CrossRef] [PubMed]
- Stanchina, M.; Soong, D.; Zheng-Lin, B.; Watts, J.M.; Taylor, J. Advances in Acute Myeloid Leukemia: Recently Approved Therapies and Drugs in Development. Cancers 2020, 12, 3225. [Google Scholar] [CrossRef] [PubMed]
- Bladé, J.; Dimopoulos, M.; Rosiñol, L.; Rajkumar, S.V.; Kyle, R.A. Smoldering (asymptomatic) multiple myeloma: Current diagnostic criteria, new predictors of outcome, and follow-up recommendations. J. Clin. Oncol. 2010, 28, 690–697. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brown, M.; Bellon, M.; Nicot, C. Emodin and DHA potently increase arsenic trioxide interferon-alpha-induced cell death of HTLV-I-transformed cells by generation of reactive oxygen species and inhibition of Akt and AP-1. Blood 2007, 109, 1653–1659. [Google Scholar] [CrossRef]
- Crombie, J.L.; Armand, P. Diffuse Large B-Cell Lymphoma’s New Genomics: The Bridge and the Chasm. J. Clin. Oncol. 2020, 38, 3565–3574. [Google Scholar] [CrossRef] [PubMed]
- Charbonneau, B.; O’Connor, H.M.; Wang, A.H.; Liebow, M.; Thompson, C.A.; Fredericksen, Z.S.; Macon, W.R.; Slager, S.L.; Call, T.G.; Habermann, T.M.; et al. Trans fatty acid intake is associated with increased risk and n3 fatty acid intake with reduced risk of non-hodgkin lymphoma. J. Nutr. 2013, 143, 672–681. [Google Scholar] [CrossRef] [Green Version]
- Thanarajasingam, G.; Maurer, M.J.; Habermann, T.M.; Nowakowski, G.S.; Bennani, N.N.; Thompson, C.A.; Cerhan, J.R.; Witzig, T.E. Low Plasma Omega-3 Fatty Acid Levels May Predict Inferior Prognosis in Untreated Diffuse Large B-Cell Lymphoma: A New Modifiable Dietary Biomarker? Nutr. Cancer 2018, 70, 1088–1090. [Google Scholar] [CrossRef]
- Lomas, A.; Leonardi-Bee, J.; Bath-Hextall, F. A systematic review of worldwide incidence of nonmelanoma skin cancer. Br. J. Dermatol. 2012, 166, 1069–1080. [Google Scholar] [CrossRef]
- Corchado-Cobos, R.; García-Sancha, N.; González-Sarmiento, R.; Pérez-Losada, J.; Cañueto, J. Cutaneous Squamous Cell Carcinoma: From Biology to Therapy. Int. J. Mol. Sci. 2020, 21, 2956. [Google Scholar] [CrossRef] [PubMed]
- Burton, K.A.; Ashack, K.A.; Khachemoune, A. Cutaneous Squamous Cell Carcinoma: A Review of High-Risk and Metastatic Disease. Am. J. Clin. Dermatol. 2016, 17, 491–508. [Google Scholar] [CrossRef] [PubMed]
- Claveau, J.; Archambault, J.; Ernst, D.S.; Giacomantonio, C.; Limacher, J.J.; Murray, C.; Parent, F.; Zloty, D. Multidisciplinary management of locally advanced and metastatic cutaneous squamous cell carcinoma. Curr. Oncol. 2020, 27, e399–e407. [Google Scholar] [CrossRef] [PubMed]
- Elattar, T.M.; Lin, H.S. Comparison of the inhibitory effect of polyunsaturated fatty acids on prostaglandin synthesis I oral squamous carcinoma cells. Prostaglandins Leukot. Essent. Fat. Acids 1989, 38, 119–125. [Google Scholar] [CrossRef]
- Nikolakopoulou, Z.; Nteliopoulos, G.; Michael-Titus, A.T.; Parkinson, E.K. Omega-3 polyunsaturated fatty acids selectively inhibit growth in neoplastic oral keratinocytes by differentially activating ERK1/2. Carcinogenesis 2013, 34, 2716–2725. [Google Scholar] [CrossRef] [Green Version]
- Ye, Y.; Scheff, N.N.; Bernabé, D.; Salvo, E.; Ono, K.; Liu, C.; Veeramachaneni, R.; Viet, C.T.; Viet, D.T.; Dolan, J.C.; et al. Anti-cancer and analgesic effects of resolvin D2 in oral squamous cell carcinoma. Neuropharmacology 2018, 139, 182–193. [Google Scholar] [CrossRef]
- Palakurthi, S.S.; Flückiger, R.; Aktas, H.; Changolkar, A.K.; Shahsafaei, A.; Harneit, S.; Kilic, E.; Halperin, J.A. Inhibition of translation initiation mediates the anticancer effect of the n-3 polyunsaturated fatty acid eicosapentaenoic acid. Cancer Res. 2000, 60, 2919–2925. [Google Scholar]
- Wen, B.; Deutsch, E.; Opolon, P.; Auperin, A.; Frascogna, V.; Connault, E.; Bourhis, J. n-3 polyunsaturated fatty acids decrease mucosal/epidermal reactions and enhance antitumour effect of ionising radiation with inhibition of tumour angiogenesis. Br. J. Cancer 2003, 89, 1102–1107. [Google Scholar] [CrossRef] [Green Version]
- Weed, H.G.; Ferguson, M.L.; Gaff, R.L.; Hustead, D.S.; Nelson, J.L.; Voss, A.C. Lean body mass gain in patients with head and neck squamous cell cancer treated perioperatively with a protein- and energy-dense nutritional supplement containing eicosapentaenoic acid. Head Neck 2011, 33, 1027–1033. [Google Scholar] [CrossRef]
- Solís-Martínez, O.; Plasa-Carvalho, V.; Phillips-Sixtos, G.; Trujillo-Cabrera, Y.; Hernández-Cuellar, A.; Queipo-García, G.E.; Meaney-Mendiolea, E.; Ceballos-Reyes, G.M.; Fuchs-Tarlovsky, V. Effect of Eicosapentaenoic Acid on Body Composition and Inflammation Markers in Patients with Head and Neck Squamous Cell Cancer from a Public Hospital in Mexico. Nutr. Cancer 2018, 70, 663–670. [Google Scholar] [CrossRef]
- Kubota, H.; Hirai, T.; Yamauchi, A.; Ogo, A.; Matsumoto, H.; Ueno, T. Inhibitory Effect of Eicosapentaenoic Acid on the Migration of the Esophageal Squamous Cell Carcinoma Cell Line TE-1. Anticancer Res. 2020, 40, 5043–5048. [Google Scholar] [CrossRef] [PubMed]
- Sawada, Y.; Gallo, R.L. Role of Epigenetics in the Regulation of Immune Functions of the Skin. J. Investig. Dermatol. 2021, 141, 1157–1166. [Google Scholar] [CrossRef] [PubMed]
- Sawada, Y.; Nakatsuji, T.; Dokoshi, T.; Kulkarni, N.N.; Liggins, M.C.; Sen, G.; Gallo, R.L. Cutaneous innate immune tolerance is mediated by epigenetic control of MAP2K3 by HDAC8/9. Sci. Immunol. 2021, 6, eabe1935. [Google Scholar] [CrossRef]
- Sugino, H.; Sawada, Y.; Nakamura, M. IgA Vasculitis: Etiology, Treatment, Biomarkers and Epigenetic Changes. Int. J. Mol. Sci. 2021, 22, 7538. [Google Scholar] [CrossRef] [PubMed]
- Huang, Q.; Mo, M.; Zhong, Y.; Yang, Q.; Zhang, J.; Ye, X.; Zhang, L.; Cai, C. The Anticancer Role of Omega-3 Polyunsaturated Fatty Acids was Closely Associated with the Increase in Genomic DNA Hydroxymethylation. Anticancer Agents Med. Chem. 2019, 19, 330–336. [Google Scholar] [CrossRef]
- Kim, H.J.; Lee, M.; Lee, Y.B.; Yu, D.S. Investigation of Genetic Mutations in High-risk and Low-risk Basal Cell Carcinoma in a Non-Caucasian Population by Whole Exome Sequencing. Acta Derm. Venereol. 2021, 101, adv00458. [Google Scholar] [CrossRef]
- Li, L.; Li, F.; Xia, Y.; Yang, X.; Lv, Q.; Fang, F.; Wang, Q.; Bu, W.; Wang, Y.; Zhang, K.; et al. UVB induces cutaneous squamous cell carcinoma progression by de novo ID4 methylation via methylation regulating enzymes. EBioMedicine 2020, 57, 102835. [Google Scholar] [CrossRef]
- Collignon, E.; Canale, A.; Al Wardi, C.; Bizet, M.; Calonne, E.; Dedeurwaerder, S.; Garaud, S.; Naveaux, C.; Barham, W.; Wilson, A.; et al. Immunity drives TET1 regulation in cancer through NF-κB. Sci. Adv. 2018, 4, eaap7309. [Google Scholar] [CrossRef] [Green Version]
- Woollard, W.J.; Pullabhatla, V.; Lorenc, A.; Patel, V.M.; Butler, R.M.; Bayega, A.; Begum, N.; Bakr, F.; Dedhia, K.; Fisher, J.; et al. Candidate driver genes involved in genome maintenance and DNA repair in Sézary syndrome. Blood 2016, 127, 3387–3397. [Google Scholar] [CrossRef] [Green Version]
- Tsuzuki, T.; Kambe, T.; Shibata, A.; Kawakami, Y.; Nakagawa, K.; Miyazawa, T. Conjugated EPA activates mutant p53 via lipid peroxidation and induces p53-dependent apoptosis in DLD-1 colorectal adenocarcinoma human cells. Biochim. Biophys. Acta 2007, 1771, 20–30. [Google Scholar] [CrossRef]
- Kato, T.; Kolenic, N.; Pardini, R.S. Docosahexaenoic acid (DHA), a primary tumor suppressive omega-3 fatty acid, inhibits growth of colorectal cancer independent of p53 mutational status. Nutr. Cancer 2007, 58, 178–187. [Google Scholar] [CrossRef] [PubMed]
- Khan, N.A.; Nishimura, K.; Aires, V.; Yamashita, T.; Oaxaca-Castillo, D.; Kashiwagi, K.; Igarashi, K. Docosahexaenoic acid inhibits cancer cell growth via p27Kip1, CDK2, ERK1/ERK2, and retinoblastoma phosphorylation. J. Lipid Res. 2006, 47, 2306–2313. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, N.; Budhraja, A.; Cheng, S.; Liu, E.H.; Huang, C.; Chen, J.; Yang, Z.; Chen, D.; Zhang, Z.; Shi, X. Interruption of the MEK/ERK signaling cascade promotes dihydroartemisinin-induced apoptosis in vitro and in vivo. Apoptosis 2011, 16, 511–523. [Google Scholar] [CrossRef] [PubMed]
- Sun, H.; Hu, Y.; Gu, Z.; Owens, R.T.; Chen, Y.Q.; Edwards, I.J. Omega-3 fatty acids induce apoptosis in human breast cancer cells and mouse mammary tissue through syndecan-1 inhibition of the MEK-Erk pathway. Carcinogenesis 2011, 32, 1518–1524. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fenton, J.I.; McCaskey, S.J. Curcumin and docosahexaenoic acid block insulin-induced colon carcinoma cell proliferation. Prostaglandins Leukot. Essent. Fat. Acids 2013, 88, 219–226. [Google Scholar] [CrossRef]
- Mashima, E.; Sawada, Y.; Yamaguchi, T.; Yoshioka, H.; Ohmori, S.; Haruyama, S.; Yoshioka, M.; Okada, E.; Nakamura, M. A high expression of cell adhesion molecule 1 (CADM1) is an unfavorable prognostic factor in mycosis fungoides. Clin. Immunol. 2018, 193, 121–122. [Google Scholar] [CrossRef]
- Sawada, Y.; Mashima, E.; Saito-Sasaki, N.; Nakamura, M. The Role of Cell Adhesion Molecule 1 (CADM1) in Cutaneous Malignancies. Int. J. Mol. Sci. 2020, 21, 9732. [Google Scholar] [CrossRef]
- Saito-Sasaki, N.; Sawada, Y.; Okada, E.; Nakamura, M. Cell Adhesion Molecule 1 (CADM1) Is an Independent Prognostic Factor in Patients with Cutaneous Squamous Cell Carcinoma. Diagnostics 2021, 11, 830. [Google Scholar] [CrossRef]
- Pasqualini, M.E.; Heyd, V.L.; Manzo, P.; Eynard, A.R. Association between E-cadherin expression by human colon, bladder and breast cancer cells and the 13-HODE:15-HETE ratio. A possible role of their metastatic potential. Prostaglandins Leukot. Essent. Fat. Acids 2003, 68, 9–16. [Google Scholar] [CrossRef]
- Iwamoto, S.; Senzaki, H.; Kiyozuka, Y.; Ogura, E.; Takada, H.; Hioki, K.; Tsubura, A. Effects of fatty acids on liver metastasis of ACL-15 rat colon cancer cells. Nutr. Cancer 1998, 31, 143–150. [Google Scholar] [CrossRef]
- Mashima, E.; Inoue, A.; Sakuragi, Y.; Yamaguchi, T.; Sasaki, N.; Hara, Y.; Omoto, D.; Ohmori, S.; Haruyama, S.; Sawada, Y.; et al. Nivolumab in the treatment of malignant melanoma: Review of the literature. Onco Targets Ther. 2015, 8, 2045–2051. [Google Scholar] [CrossRef] [Green Version]
- Saito, R.; Sawada, Y.; Saito-Sasaki, N.; Yamamoto, K.; Yoshioka, H.; Ohmori, S.; Yoshioka, M.; Okada, E.; Nakamura, M. Profile fluctuation of peripheral blood in advanced melanoma patients treated with nivolumab. J. Dermatol. 2018, 45, 1452–1455. [Google Scholar] [CrossRef] [PubMed]
- Saito, R.; Sawada, Y.; Nakamura, M. Immune Profile Analysis in Peripheral Blood and Tumor in Patients with Malignant Melanoma. Int. J. Mol. Sci. 2021, 22, 1957. [Google Scholar] [CrossRef] [PubMed]
- Oda, T.; Sawada, Y.; Okada, E.; Yamaguchi, T.; Ohmori, S.; Haruyama, S.; Yoshioka, M.; Nakamura, M. Hypopituitarism and hypothyroidism following atrioventricular block during nivolumab treatment. J. Dermatol. 2017, 44, e144–e145. [Google Scholar] [CrossRef]
- Sato, S.; Sawada, Y.; Nakamura, M. STING Signaling and Skin Cancers. Cancers 2021, 13, 5603. [Google Scholar] [CrossRef]
- Carlsson, J.A.; Wold, A.E.; Sandberg, A.S.; Östman, S.M. The Polyunsaturated Fatty Acids Arachidonic Acid and Docosahexaenoic Acid Induce Mouse Dendritic Cells Maturation but Reduce T-Cell Responses In Vitro. PLoS ONE 2015, 10, e0143741. [Google Scholar] [CrossRef]
Skin Cancers | Detailed Action |
---|---|
Melanoma | Reduce the risk of melanoma by DHA/EPA intake [27] Enhance the sensitivity to chemotherapy by EPA and DHA [28,29,30,31,46,47,48]. Suppress tumor growth by linoleic acid, EPA, DHA [32,37,41,42,44,45]. Suppress tumor metastasis by EPA [33,37] Suppress tumor invasion by EPA and DHA [34,37] Enhance ROS production and P53 induction by DHA and EPA [40]. Suppress debris-stimulated cancer progression by RvD1, RvD2, or RvE1 [50] |
BCC | Reduce the risk of BCC by α-linolenic acid and linoleic [56]. |
ATLL | Synergistic effect on cell cycle arrest and cell death by the combination of DHA with chemotherapy [66]. |
DLBCL | Low intake of omega-3 fatty acids is associated with unfavorable survival [69]. |
SCC | Enhance the toxicity by DHA [75]. Reduce tumor size and cancer-derived cytokines/chemokines by RvD2 [76]. Suppress cell proliferation by EPA [77] Suppress tumor growth by the combination of Omega-3 PUFAs with ionizing radiation [78]. Suppress migration by EPA [81]. |
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Minokawa, Y.; Sawada, Y.; Nakamura, M. The Influences of Omega-3 Polyunsaturated Fatty Acids on the Development of Skin Cancers. Diagnostics 2021, 11, 2149. https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics11112149
Minokawa Y, Sawada Y, Nakamura M. The Influences of Omega-3 Polyunsaturated Fatty Acids on the Development of Skin Cancers. Diagnostics. 2021; 11(11):2149. https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics11112149
Chicago/Turabian StyleMinokawa, Yoko, Yu Sawada, and Motonobu Nakamura. 2021. "The Influences of Omega-3 Polyunsaturated Fatty Acids on the Development of Skin Cancers" Diagnostics 11, no. 11: 2149. https://0-doi-org.brum.beds.ac.uk/10.3390/diagnostics11112149