An essential role for platelet-activating factor in activating mast cell migration following ultraviolet irradiation

Journal of Leukocyte Biology

Volumn 95, Issue 1, 2014, Pages 139-148

  Chacón Salinas, Rommel ^a,b   Chen, Limo ^a   Chávez Blanco, Alma D ^c   Limón Flores, Alberto Y ^a,b   Ma, Ying ^a   Ullrich, Stephen E ^a,d  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^c INSTITUTO NACIONAL DE CANCEROLOGÍA   (Mexico)

^d UNIVERSITY OF TEXAS   (United States)

Author keywords

Cell trafficking; Immune suppression; Inflammatory mediators; UV radiation

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; THROMBOCYTE ACTIVATING FACTOR;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL MIGRATION; CELL POPULATION; EXPOSURE; FEMALE; HYPOTHESIS; IMMUNOSUPPRESSIVE TREATMENT; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION DOSE; SKIN; ULTRAVIOLET B RADIATION; ULTRAVIOLET IRRADIATION; ULTRAVIOLET RADIATION; ANIMAL; CHEMOTAXIS; DRUG EFFECT; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INFLAMMATORY MEDIATORS; KNOCKOUT MOUSE; METABOLISM; RADIATION EXPOSURE;

CELL TRAFFICKING; IMMUNE SUPPRESSION; INFLAMMATORY MEDIATORS; UV RADIATION;

ANIMALS; CHEMOTAXIS; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; IMMUNOSUPPRESSION; MAST CELLS; MICE; MICE, KNOCKOUT; PLATELET ACTIVATING FACTOR; RECEPTORS, CXCR4; ULTRAVIOLET RAYS;

EID: 84897019482     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0811409     Document Type: Article

References (61)

1. Boscoe, F. P., Schymura, M. J. (2006) Solar ultraviolet-B exposure and cancer incidence and mortality in the United States, 1993-2002. BMC Cancer 6, 264-272.
2. Landi, M. T., Baccarelli, A., Tarone, R. E., Pesatori, A., Tucker, M. A., Hedayati, M., Grossman, L. (2002) DNA repair, dysplastic nevi, and sunlight sensitivity in the development of cutaneous malignant melanoma. J. Natl. Cancer Inst. 94, 94-101.
3. Wang, Y., Digiovanna, J. J., Stern, J. B., Hornyak, T. J., Raffeld, M., Khan, S. G., Oh, K. S., Hollander, M. C., Dennis, P. A., Kraemer, K. H. (2009) Evidence of ultraviolet type mutations in xeroderma pigmentosum melanomas. Proc. Natl. Acad. Sci. USA 106, 6279-6284.
4. Fisher, M. S., Kripke, M. L. (1982) Suppressor T lymphocytes control the development of primary skin cancers in ultraviolet-irradiated mice. Science 216, 1133-1134.
5. Yoshikawa, T., Rae, V., Bruins-Slot, W., Van den Berg, J. W., Taylor, J. R., Streilein, J. W. (1990) Susceptibility to effects of UVB radiation on induction of contact hypersensitivity as a risk factor for skin cancer in humans. J. Invest. Dermatol. 95, 530-536.
6. Vajdic, C. M., van Leeuwen, M. T., Webster, A. C., McCredie, M. R., Stewart, J. H., Chapman, J. R., Amin, J., McDonald, S. P., Grulich, A. E. (2009) Cutaneous melanoma is related to immune suppression in kidney transplant recipients. Cancer Epidemiol. Biomarkers Prev. 18, 2297-2303.
7. Kripke, M. L. (1974) Antigenicity of murine skin tumors induced by ultraviolet light. J. Natl. Cancer Inst. 53, 1333-1336.
8. Ullrich, S. E. (2005) Mechanisms underlying UV-induced immune suppression. Mutat. Res. 571, 185-205.
9. Chacon-Salinas, R., Limon-Flores, A. Y., Chavez-Blanco, A. D., Gonzalez-Estrada, A., Ullrich, S. E. (2011) Mast cell-derived IL-10 suppresses germinal center formation by affecting T follicular helper cell function. J. Immunol. 186, 25-31.
10. Loser, K., Mehling, A., Loeser, S., Apelt, J., Kuhn, A., Grabbe, S., Schwarz, T., Penninger, J. M., Beissert, S. (2007) Epidermal RANKL controls regulatory T-cell numbers via activation of dendritic cells. Nat. Med. 12, 1372-1379.
11. Schwarz, A., Noordegraaf, M., Maeda, A., Torii, K., Clausen, B. E., Schwarz, T. (2010) Langerhans cells are required for UVR-induced immunosuppression. J. Invest. Dermatol. 130, 1419-1427.
12. Fukunaga, A., Khaskhely, N. M., Ma, Y., Sreevidya, C. S., Taguchi, K., Nishigori, C., Ullrich, S. E. (2010) Langerhans cells serve as immunoregulatory cells by activating NKT cells. J. Immunol. 185, 4633-4640.
13. Hart, P. H., Grimbaldeston, M. A., Swift, G. J., Jaksic, A., Noonan, F. P., Finlay-Jones, J. J. (1998) Dermal mast cells determine susceptibility to ultraviolet B-induced systemic suppression of contact hypersensitivity responses in mice. J. Exp. Med. 187, 2045-2053.
14. Byrne, S. N., Limon-Flores, A. Y., Ullrich, S. E. (2008) Mast cell migration from the skin to the draining lymph nodes upon ultraviolet irradiation represents a key step in the induction of immune suppression. J. Immunol. 180, 4648-4655.
15. Galli, S. J., Kalesnikoff, J., Grimbaldeston, M. A., Piliponsky, A. M., Williams, C. M., Tsai, M. (2005) Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu. Rev. Immunol. 23, 749-786.
16. Kalesnikoff, J., Galli, S. J. (2008) New developments in mast cell biology. Nat. Immunol. 9, 1215-1223.
17. Alard, P., Kurimoto, I., Niizeki, H., Doherty, J. M., Streilein, J. W. (2001) Hapten-specific tolerance induced by acute, low-dose ultraviolet B radiation of skin requires mast cell degranulation. Eur. J. Immunol. 31, 1736-1746.
18. De Fabo, E. C., Noonan, F. P. (1983) Mechanism of immune suppression by ultraviolet irradiation in vivo. I. Evidence for the existence of a unique photoreceptor in skin and its role in photoimmunology. J. Exp. Med. 157, 84-98.
19. 2A receptor. Proc. Natl. Acad. Sci. USA 103, 17420-17425.
20. Gorman, S., Kuritzky, L. A., Judge, M. A., Dixon, K. M., McGlade, J. P., Mason, R. S., Finlay-Jones, J. J., Hart, P. H. (2007) Topically applied 1,25-dihydroxyvitamin D3 enhances the suppressive activity of CD4+CD25β cells in the draining lymph nodes. J. Immunol. 179, 6273-6283.
21. Walterscheid, J. P., Ullrich, S. E., Nghiem, D. X. (2002) Platelet-activating factor, a molecular sensor for cellular damage, activates systemic immune suppression. J. Exp. Med. 195, 171-179.
22. Wolf, P., Nghiem, D. X., Walterscheid, J. P., Byrne, S., Matsumura, Y., Matsumura, Y., Bucana, C., Ananthaswamy, H. N., Ullrich, S. E. (2006) Platelet-activating factor is crucial in psoralen and ultraviolet A-induced immune suppression, inflammation, and apoptosis. Am. J. Pathol. 169, 795-805.
23. Alappatt, C., Johnson, C. A., Clay, K. L., Travers, J. B. (2000) Acute keratinocyte damage stimulates platelet-activating factor production. Arch. Dermatol. Res. 292, 256-259.
24. Marathe, G. K., Johnson, C., Billings, S. D., Southall, M. D., Pei, Y., Spandau, D., Murphy, R. C., Zimmerman, G. A., McIntyre, T. M., Travers, J. B. (2005) Ultraviolet B radiation generates platelet-activating factor-like phospholipids underlying cutaneous damage. J. Biol. Chem. 280, 35448-35457.
25. Travers, J. B., Berry, D., Yao, Y., Yi, Q., Konger, R. L. (2010) Ultraviolet B radiation of human skin generates platelet-activating factor receptor agonists. Photochem. Photobiol. 86, 949-954.
26. Izumi, T., Shimizu, T. (1995) Platelet-activating factor receptor: gene expression and signal transduction. Biochim. Biophys. Acta 1259, 317-333.
27. Travers, J. B., Huff, J. C., Rola-Pleszczynski, M., Gelfand, E. W., Morelli, J. G., Murphy, R. C. (1995) Identification of functional platelet-activating factor receptors on human keratinocytes. J. Invest. Dermatol. 105, 816-823.
28. Zhang, Q., Yao, Y., Konger, R. L., Sinn, A. L., Cai, S., Pollok, K. E., Travers, J. B. (2008) UVB radiation-mediated inhibition of contact hypersensitivity reactions is dependent on the platelet-activating factor system. J. Invest. Dermatol. 128, 1780-1787.
29. Kajiwara, N., Sasaki, T., Bradding, P., Cruse, G., Sagara, H., Ohmori, K., Saito, H., Ra, C., Okayama, Y. (2010) Activation of human mast cells through the platelet-activating factor receptor. J. Allergy Clin. Immunol. 125, 1137. e6-1145. e6.
30. Fukunaga, A., Khaskhely, N. M., Sreevidya, C. S., Byrne, S. N., Ullrich, S. E. (2008) Dermal dendritic cells, and not Langerhans cells, play an essential role in inducing an immune response. J. Immunol. 180, 3057-3064.
31. Bussolati, B., Biancone, L., Cassoni, P., Russo, S., Rola-Pleszczynski, M., Montrucchio, G., Camussi, G. (2000) PAF produced by human breast cancer cells promotes migration and proliferation of tumor cells and neo-angiogenesis. Am. J. Pathol. 157, 1713-1725.
32. Moreno, S. E., Alves-Filho, J. C., Rios-Santos, F., Silva, J. S., Ferreira, S. H., Cunha, F. Q., Teixeira, M. M. (2006) Signaling via platelet-activating factor receptors accounts for the impairment of neutrophil migration in polymicrobial sepsis. J. Immunol. 177, 1264-1271.
33. Ishii, S., Shimizu, T. (2000) Platelet-activating factor (PAF) receptor and genetically engineered PAF receptor mutant mice. Prog. Lipid Res. 39, 41-82.
34. Grimbaldeston, M. A., Chen, C. C., Piliponsky, A. M., Tsai, M., Tam, S. Y., Galli, S. J. (2005) Mast cell-deficient W-sash c-kit mutant kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am. J. Pathol. 167, 835-848.
35. Nghiem, D. X., Walterscheid, J. P., Kazimi, N., Ullrich, S. E. (2002) Ultraviolet radiation-induced immunosuppression of delayed-type hypersensitivity in mice. Methods 28, 25-33.
36. Kuehn, H. S., Jung, M. Y., Beaven, M. A., Metcalfe, D. D., Gilfillan, A. M. (2011) Prostaglandin E2 activates and utilizes mTORC2 as a central signaling locus for the regulation of mast cell chemotaxis and mediator release. J. Biol. Chem. 286, 391-402.
37. Limon-Flores, A. Y., Chacon-Salinas, R., Ramos, G., Ullrich, S. E. (2009) Mast cells mediate the immune suppression induced by dermal exposure to JP-8 jet fuel. Toxicol. Sci. 112, 144-152.
38. Simon, H. U., Tsao, P. W., Siminovitch, K. A., Mills, G. B., Blaser, K. (1994) Functional platelet-activating factor receptors are expressed by monocytes and granulocytes but not by resting or activated T and B lymphocytes from normal individuals or patients with asthma. J. Immunol. 153, 364-377.
39. Marrache, A. M., Gobeil Jr., F., Bernier, S. G., Stankova, J., Rola-Pleszczynski, M., Choufani, S., Bkaily, G., Bourdeau, A., Sirois, M. G., Vazquez-Tello, A., Fan, L., Joyal, J. S., Filep, J. G., Varma, D. R., Ribeiro-Da-Silva, A., Chemtob, S. (2002) Proinflammatory gene induction by platelet-activating factor mediated via its cognate nuclear receptor. J. Immunol. 169, 6474-6481.
40. Katoh, H., Hosono, K., Ito, Y., Suzuki, T., Ogawa, Y., Kubo, H., Kamata, H., Mishima, T., Tamaki, H., Sakagami, H., Sugimoto, Y., Narumiya, S., Watanabe, M., Majima, M. (2010) COX-2 and prostaglandin EP3/EP4 signaling regulate the tumor stromal proangiogenic microenvironment via CXCL12-CXCR4 chemokine systems. Am. J. Pathol. 176, 1469-1483.
41. Niizeki, H., Alard, P., Streilein, J. W. (1997) Cutting edge: calcitonin gene-related peptide is necessary for ultraviolet B-impaired induction of contact hypersensitivity. J. Immunol. 159, 5183-5186.
42. Ullrich, S. E., Nghiem, D. X., Khaskina, P. (2007) Suppression of an established immune response by UVA-a critical role for mast cells. Photochem. Photobiol. 83, 1095-1100.
43. Sreevidya, C. S., Khaskhely, N. M., Fukunaga, A., Khaskina, P., Ullrich, S. E. (2008) Inhibition of photocarcinogenesis by platelet-activating factor or serotonin receptor antagonists. Cancer Res. 68, 3978-3984.
44. Melnikova, V. O., Mourad-Zeidan, A. A., Lev, D. C., Bar-Eli, M. (2006) Platelet-activating factor mediates MMP-2 expression and activation via phosphorylation of cAMP-response element-binding protein and contributes to melanoma metastasis. J. Biol. Chem. 281, 2911-2922.
45. Lefebvre, J. S., Marleau, S., Milot, V., Levesque, T., Picard, S., Flamand, N., Borgeat, P. (2010) Toll-like receptor ligands induce polymorphonuclear leukocyte migration: key roles for leukotriene B4 and platelet-activating factor. FASEB J. 24, 637-647.
46. Nilsson, G., Metcalfe, D. D., Taub, D. D. (2000) Demonstration that platelet-activating factor is capable of activating mast cells and inducing a chemotactic response. Immunology 99, 314-319.
47. Rastogi, P., White, M. C., Rickard, A., McHowat, J. (2008) Potential mechanism for recruitment and migration of CD133 positive cells to areas of vascular inflammation. Thromb. Res. 123, 258-266.
48. Fehlner-Gardiner, C. C., Uniyal, S., von Ballestrem, C. G., Chan, B. M. (1996) Differential utilization of VLA-4 (alpha 4 beta 1) and-5 (alpha 5 beta 1) integrins during the development of mouse bone marrow-derived mast cells. Differentiation 60, 317-325.
49. Marques, M., Pei, Y., Southall, M. D., Johnston, J. M., Arai, H., Aoki, J., Inoue, T., Seltmann, H., Zouboulis, C. C., Travers, J. B. (2002) Identification of platelet-activating factor acetylhydrolase II in human skin. J. Invest. Dermatol. 119, 913-919.
50. Liu, M., Zhu, H., Li, J., Garcia, C. C., Feng, W., Kirpotina, L. N., Hilmer, J., Tavares, L. P., Layton, A. W., Quinn, M. T., Bothner, B., Teixeira, M. M., Lei, B. (2012) Group A Streptococcus secreted esterase hydrolyzes platelet-activating factor to impede neutrophil recruitment and facilitate innate immune evasion. PLoS Pathog. 8, e1002624.
51. Liu, J., Chen, R., Marathe, G. K., Febbraio, M., Zou, W., McIntyre, T. M. (2011) Circulating platelet-activating factor is primarily cleared by transport, not intravascular hydrolysis, by lipoprotein-associated phospholipase A2/PAF acetylhydrolase. Circ. Res. 108, 469-477.
52. Prescott, S. M., Zimmerman, G. A., Stafforini, D. M., McIntyre, T. M. (2000) Platelet-activating factor and related lipid mediators. Annu. Rev. Biochem. 69, 419-445.
53. Pei, Y., Barber, L. A., Murphy, R. C., Johnson, C. A., Kelley, S. W., Dy, L. C., Fertel, R. H., Nguyen, T. M., Williams, D. A., Travers, J. B. (1998) Activation of the epidermal platelet-activating factor receptor results in cytokine and cyclooxygenase-2 biosynthesis. J. Immunol. 161, 1954-1961.
54. Rivas, J. M., Ullrich, S. E. (1992) Systemic suppression of delayed-type hypersensitivity by supernatants from UV-irradiated keratinocytes. An essential role for keratinocyte-derived IL-10. J. Immunol. 149, 3865-3871.
55. Beissert, S., Hosoi, J., Kühn, R., Rajewsky, K., Müller, W., Granstein, R. D. (1996) Impaired immunosuppressive response to ultraviolet radiation in interleukin-10-deficient mice. J. Invest. Dermatol. 107, 553-557.
56. Ramos, G., Limon-Flores, A. Y., Ullrich, S. E. (2007) Dermal exposure to jet fuel suppresses delayed-type hypersensitivity: a critical role for aromatic hydrocarbons. Toxicol. Sci. 100, 415-422.
57. Ullrich, S. E., Lyons, H. J. (2000) Mechanisms involved in the immunotoxicity induced by dermal application of JP-8 jet fuel. Toxicol. Sci. 58, 290-298.
58. Ramos, G., Kazimi, N., Nghiem, D. X., Walterscheid, J. P., Ullrich, S. E. (2004) Platelet activating factor receptor binding plays a critical role in jet fuel-induced immune suppression. Toxicol. Appl. Pharmacol. 195, 331-338.
59. Miller, A. C., Rashid, R. M., Elamin, E. M. (2007) The "T" in trauma: the helper T-cell response and the role of immunomodulation in trauma and burn patients. J. Trauma 63, 1407-1417.
60. Dudeck, A., Dudeck, J., Scholten, J., Petzold, A., Surianarayanan, S., Kohler, A., Peschke, K., Vohringer, D., Waskow, C., Krieg, T., Muller, W., Waisman, A., Hartmann, K., Gunzer, M., Roers, A. (2011) Mast cells are key promoters of contact allergy that mediate the adjuvant effects of haptens. Immunity 34, 973-984.
61. McLachlan, J. B., Shelburne, C. P., Hart, J. P., Pizzo, S. V., Goyal, R., Brooking-Dixon, R., Staats, H. F., Abraham, S. N. (2008) Mast cell activators: a new class of highly effective vaccine adjuvants. Nat. Med. 14, 536-541.