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Journal of Immunology Research
Volume 2017, Article ID 9212134, 10 pages
https://doi.org/10.1155/2017/9212134
Research Article

Inflammatory Cytokine Pattern Is Sex-Dependent in Mouse Cutaneous Melanoma Experimental Model

1Immunology Department, “Victor Babes” National Institute of Pathology, 99-101 Spl. Independentei, 050096 Bucharest, Romania
2Faculty of Biology, University of Bucharest, 91-95 Spl. Independentei, 76201 Bucharest, Romania
3Colentina University Hospital, 19-21 Stefan cel Mare Blv., 020125 Bucharest, Romania
4“Carol Davila” University of Pharmacy and Medicine, 37 Dionisie Lupu Street, 020021 Bucharest, Romania

Correspondence should be addressed to Monica Neagu; moc.liamg@acinom.ugaen

Received 21 July 2017; Revised 9 October 2017; Accepted 22 October 2017; Published 26 November 2017

Academic Editor: Nejat K. Egilmez

Copyright © 2017 Mihaela Surcel et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Neagu, C. Constantin, and C. Tanase, “Immune-related biomarkers for diagnosis/prognosis and therapy monitoring of cutaneous melanoma,” Expert Review of Molecular Diagnostics, vol. 10, no. 7, pp. 897–919, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. E. A. Grimm, “Immunology comes full circle in melanoma while specific immunity is unleashed to eliminate metastatic disease, inflammatory products of innate immunity promote resistance,” Critical Reviews in Oncogenesis, vol. 21, no. 1-2, pp. 57–63, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Bulman, M. Neagu, and C. Constantin, “Immunomics in skin cancer - improvement in diagnosis, prognosis and therapy monitoring,” Current Proteomics, vol. 10, no. 3, pp. 202–217, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Mantovani, P. Allavena, A. Sica, and F. Balkwill, “Cancer-related inflammation,” Nature, vol. 454, no. 7203, pp. 436–444, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Neagu, C. Constantin, and C. Longo, “Chemokines in the melanoma metastasis biomarkers portrait,” Journal of Immunoassay and Immunochemistry, vol. 36, no. 6, pp. 559–566, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. T. DiChiara, Cancer Chemotherapy for Melanoma: Dacarbazine A Patient’s Guide to Cancer Chemotherapy with Dacarbazine, 2009, http://skincancer.about.com/od/treatmentoptions/a/melanoma_chemo.htm.
  7. A. Y. Bedikian, M. Millward, H. Pehamberger et al., “Bcl-2 antisense (oblimersen sodium) plus dacarbazine in patients with advanced melanoma: the oblimersen melanoma study group,” Journal of Clinical Oncology, vol. 24, no. 29, pp. 4738–4745, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Hahka-Kemppinen, T. Muhonen, L. Kangas, and S. Pyrhönen, “Chemosensitivity of human melanoma metastases in mouse subrenal capsule assay-can it predict tumour response to combined cytostatic plus interferon therapy in metastatic melanoma?” Melanoma Research, vol. 6, no. 3, pp. 215–221, 1996. View at Publisher · View at Google Scholar · View at Scopus
  9. D. C. Lev, A. Onn, V. O. Melinkova et al., “Exposure of melanoma cells to dacarbazine results in enhanced tumour growth and metastasis in vivo,” Journal of Clinical Oncology, vol. 22, no. 11, pp. 2092–2100, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. W. W. Overwijk and N. P. Restifo, “B16 as a mouse model for human melanoma,” Current Protocols in Immunology, vol. 39, no. 20.1, pp. 20.1.1–20.1.29, 2001. View at Publisher · View at Google Scholar
  11. Committee for the Update of the guide for the care and use of laboratory animals and National Research Council, Guide for the Care and Use of Laboratory Animals, The National Academies Press, Washington, DC, USA, Eighth edition, 2010.
  12. I. K. Egorov, “Mouse models of efficient and inefficient anti-tumour immunity, with emphasis on minimal residual disease and tumour escape,” Cancer Immunology Immunotherapy, vol. 55, no. 1, pp. 1–22, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Winter, N. K. van den Engel, D. Rüttinger et al., “Therapeutic T cells induce tumor-directed chemotaxis of innate immune cells through tumor-specific secretion of chemokines and stimulation of B16BL6 melanoma to secrete chemokines,” Journal of Translational Medicine, vol. 5, p. 56, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Coelho de Sá and C. F. Neto, “Inflammasomes and dermatology,” Anais Brasileiros de Dermatologia, vol. 91, no. 5, pp. 566–578, 2016. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Neagu, C. Constantin, and S. Zurac, “Immune parameters in prognosis and therapy monitoring of cutaneous melanoma patients: experience, role and limitations,” BioMed Research International, vol. 2013, Article ID 107940, 13 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Okamoto, W. Liu, Y. Luo et al., “Constitutively active inflammasome in human melanoma cells mediating autoinflammation via caspase-1 processing and secretion of interleukin-1β,” Journal of Biological Chemistry, vol. 285, no. 9, pp. 6477–6488, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Mashiah, S. Brenner, Y. Pessach, V. Barak, and J. Schachter, “Differences in cytokine levels in melanoma patients with and without redness (Brenner sign),” Anticancer Research, vol. 29, no. 5, pp. 1793–1796, 2009. View at Google Scholar
  18. V. von Felbert, F. Córdoba, J. Weissenberger et al., “Interleukin-6 gene ablation in a transgenic mouse model of malignant skin melanoma,” The American Journal of Pathology, vol. 166, no. 3, pp. 831–841, 2005. View at Publisher · View at Google Scholar
  19. A. Tuccitto, M. Tazzari, V. Beretta et al., “Immunomodulatory factors control the fate of melanoma tumor initiating cells,” Stem Cells, vol. 34, no. 10, pp. 2449–2460, 2016. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Lodin, M. Lekander, J. Syk, K. Alving, P. Petrovic, and A. Andreasson, “Longitudinal co-variations between inflammatory cytokines, lung function and patient reported outcomes in patients with asthma,” PLoS One, vol. 12, no. 9, article e0185019, 2017. View at Publisher · View at Google Scholar
  21. R. J. Giblin, E. J. Bennett, G. R. Zosky, and R. M. Dwyer, “The impact of sex and 25(OH)D deficiency on metabolic function in mice,” Nutrients, vol. 9, no. 9, 2017. View at Publisher · View at Google Scholar
  22. C. D. Ene, A. E. Anghel, M. Neagu, and I. Nicolae, “25-OH vitamin D and interleukin-8: emerging biomarkers in cutaneous melanoma development and progression,” Mediators of Inflammation, vol. 2015, Article ID 904876, 8 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  23. I. Nieto-Vazquez, S. Fernández-Veledo, C. de Alvaro, and M. Lorenzo, “Dual role of interleukin-6 in regulating insulin sensitivity in murine skeletal muscle,” Diabetes, vol. 57, no. 12, pp. 3211–3221, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Sahoo, Y. M. Jung, H. K. Kwon et al., “A novel splicing variant of mouse interleukin (IL)-24 antagonizes IL-24-induced apoptosis,” Journal of Biological Chemistry, vol. 283, no. 43, pp. 28860–28872, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. P. B. Fisher, D. Sarkar, I. V. Lebedeva et al., “Melanoma differentiation associated gene-7/interleukin-24 (mda-7/IL-24): novel gene therapeutic for metastatic melanoma,” Toxicology and Applied Pharmacology, vol. 224, no. 3, pp. 300–307, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. I. H. Chan, V. Wu, S. McCauley, E. A. Grimm, and J. B. Mumm, “IL-10: expanding the immune oncology horizon,” Receptors & Clinical Investigations, vol. 2, no. 4, p. 1041, 2015. View at Publisher · View at Google Scholar
  27. G. Benedek, J. Zhang, H. Nguyen et al., “Novel feedback loop between M2 macrophages/microglia and regulatory B cells in estrogen-protected EAE mice,” Journal of Neuroimmunology, vol. 305, pp. 59–67, 2017. View at Publisher · View at Google Scholar
  28. C. M. Díaz-Montero, S. El Naggar, A. Al Khami et al., “Priming of naive CD8+ T cells in the presence of IL-12 selectively enhances the survival of CD8+CD62Lhi cells and results in superior anti-tumor activity in a tolerogenic murine model,” Cancer Immunology, Immunotherapy, vol. 57, no. 4, pp. 563–572, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. T. M. Fan, D. M. Kranz, and E. J. Roy, “Enhancing antitumor immunity: combining IL-12 with TGFβ1 antagonism,” Journal of immunotherapy, vol. 30, no. 5, pp. 479–489, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. K. M. Mirjačić Martinović, N. L. Babović, R. R. Džodić, V. B. Jurišić, A. Z. Ninković, and G. M. Konjević, “Beneficial in-vitro effects of interleukin-2, interleukin-12, and their combination on functional and receptor characteristics of natural killer cells in metastatic melanoma patients with normal serum lactate dehydrogenase levels,” Melanoma Research, vol. 26, no. 6, pp. 551–564, 2016. View at Publisher · View at Google Scholar · View at Scopus
  31. S. L. Klein and K. L. Flanagan, “Sex differences in immune responses,” Nature Reviews Immunology, vol. 16, no. 10, pp. 626–638, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. J. L. Hood, “Melanoma exosome induction of endothelial cell GM-CSF in pre-metastatic lymph nodes may result in different M1 and M2 macrophage mediated angiogenic processes,” Medical Hypotheses, vol. 94, pp. 118–122, 2016. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Laffont, C. Seillet, and J. C. Guéry, “Estrogen receptor-dependent regulation of dendritic cell development and function,” Frontiers in Immunolology, vol. 8, p. 108, 2017. View at Publisher · View at Google Scholar
  34. M. W. Roomi, T. Kalinovsky, A. Niedzwiecki, and M. Rath, “Modulation of MMP-2 and -9 secretion by cytokines, inducers and inhibitors in human melanoma A-2058 cells,” Oncology Reports, vol. 37, no. 6, pp. 3681–3687, 2017. View at Publisher · View at Google Scholar
  35. Z. R. Yurkovetsky, J. M. Kirkwood, H. D. Edington et al., “Multiplex analysis of serum cytokines in melanoma patients treated with interferon-α2b,” Clinical Cancer Research, vol. 13, no. 8, pp. 2422–2428, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Shetty, G. M. Beasley, S. Sparks et al., “Plasma cytokine analysis in patients with advanced extremity melanoma undergoing isolated limb infusion,” Annals of Surgical Oncology, vol. 20, no. 4, pp. 1128–1135, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Everhardt Queen, M. Moerdyk-Schauwecker, L. M. McKee, L. J. Leamy, and Y. M. Huet, “Differential expression of inflammatory cytokines and stress genes in male and female mice in response to a lipopolysaccharide challenge,” PLoS One, vol. 11, no. 4, article e0152289, 2016. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Y. Fang, K. Izumi, K. P. Lai et al., “Infiltrating macrophages promote prostate tumorigenesis via modulating androgen receptor-mediated CCL4–STAT3 signaling,” Cancer Research, vol. 73, no. 18, pp. 5633–5646, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. J. E. Laiseca, M. F. Ladelfa, J. Cotignola et al., “Functional interaction between co-expressed MAGE-A proteins,” PLoS One, vol. 12, no. 5, article e0178370, 2017. View at Publisher · View at Google Scholar
  40. G. D. Rădăvoi, C. Pricop, V. Jinga et al., “A comprehensive analysis of genome-wide association studies to identify prostate cancer susceptibility loci for the Romanian population,” Romanian Journal of Morphology and Embryology, vol. 57, no. 2, pp. 467–475, 2016. View at Google Scholar
  41. M. Koga, H. Kai, K. Egami et al., “Mutant MCP-1 therapy inhibits tumor angiogenesis and growth of malignant melanoma in mice,” Biochemical and Biophysical Research Communications, vol. 365, no. 2, pp. 279–284, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. C. E. Redon, J. S. Dickey, A. J. Nakamura et al., “Tumors induce complex DNA damage in distant proliferative tissues in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 42, pp. 17992–17997, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Iannone, L. Miele, P. Maiolino, A. Pinto, and S. Morello, “Blockade of A2b adenosine receptor reduces tumor growth and immune suppression mediated by myeloid-derived suppressor cells in a mouse model of melanoma,” Neoplasia, vol. 15, no. 12, pp. 1400–1409, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Stubelius, A. Andersson, U. Islander, and H. Carlsten, “Ovarian hormones in innate inflammation,” Immunobiology, vol. 222, no. 8-9, pp. 878–883, 2017. View at Publisher · View at Google Scholar
  45. O. Kodet, L. Lacina, E. Krejčí et al., “Melanoma cells influence the differentiation pattern of human epidermal keratinocytes,” Molecular Cancer, vol. 14, no. 1, p. 1, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Neagu and C. Constantin, New insights in cutaneous melanoma immune-therapy — tackling immune-suppression and specific anti-tumoral response, M. Murph, Ed., Chapter 9 in “Melanoma”, InTech, Croatia, 2015. View at Publisher · View at Google Scholar
  47. H. Winter, N. K. van den Engel, D. Rüttinger et al., “Therapeutic T cells induce tumor-directed chemotaxis of innate immune cells through tumor-specific secretion of chemokines and stimulation of B16BL6 melanoma to secrete chemokines,” Journal of Translational Medicine, vol. 5, no. 1, p. 56, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Tiesset, H. Bernard, N. Bartke et al., “(n-3) long-chain PUFA differentially affect resistance to Pseudomonas aeruginosa infection of male and female cftr−/− mice,” The Journal of Nutrition, vol. 141, no. 6, pp. 1101–1107, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Neagu, C. Constantin, D. Martin, L. Albulescu, N. Iacob, and D. Ighigeanu, “Whole body microwave irradiation for improved dacarbazine therapeutical action in cutaneous melanoma mouse model,” Radiology Research and Practice, vol. 2013, Article ID 414816, 10 pages, 2013. View at Publisher · View at Google Scholar
  50. M. Neagu, C. Constantin, G. Manda Gina, and M. Irina, “Biomarkers of metastatic melanoma,” Biomarkers in Medicine, vol. 3, no. 1, pp. 71–89, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Bulman, D. McCarthy, M. Neagu, and C. Constantin, “Surface-enhanced laser desorption/ionization mass spectrometry for biomarker discovery in cutaneous melanoma,” Current Proteomics, vol. 14, no. 2, pp. 100–111, 2017. View at Publisher · View at Google Scholar
  52. B. Marinescu, G. Isvoranu, L. Anghelache, and F. Cionca, “Hematology references for three laboratory mice strains,” Roumanian Archives of Microbiology and Immunology, vol. 73, no. 1-2, pp. 30–34, 2014. View at Google Scholar
  53. M. Lupu, A. Caruntu, C. Caruntu et al., “Neuroendocrine factors: the missing link in non-melanoma skin cancer (review),” Oncology Reports, vol. 38, no. 3, pp. 1327–1340, 2017. View at Publisher · View at Google Scholar
  54. C. Caruntu, D. Boda, C. Constantin, A. Caruntu, and M. Neagu, “Catecholamines increase in vitro proliferation of murine B16F10 melanoma cells,” Acta Endocrinologica (Buc), vol. 10, no. 4, pp. 545–558, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. C. Caruntu, A. Mirica, A. E. Roca et al., “The role of estrogens and estrogen receptors in melanoma development and progression,” Acta Endocrinologica (Buc), vol. 12, no. 2, pp. 234–241, 2016. View at Publisher · View at Google Scholar