S100A8/A9 stimulates keratinocyte proliferation in the development of squamous cell carcinoma of the skin via the receptor for advanced glycation-end products

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Iotzova Weiss, Guergana ^a   Dziunycz, Piotr J ^a   Freiberger, Sandra N ^a   Läuchli, Severin ^a   Hafner, Jürg ^a   Vogl, Thomas ^b   French, Lars E ^a   Hofbauer, Günther F L ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; CALGRANULIN A; CALGRANULIN B; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; AGER PROTEIN, HUMAN;

ARTICLE; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EPIDERMIS; GRAFT RECIPIENT; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENCE; IMMUNOSUPPRESSIVE TREATMENT; KERATINOCYTE; SKIN CARCINOGENESIS; SKIN CARCINOMA; TRANSCRIPTION REGULATION; UPREGULATION; CELL MOTION; CELL TRANSFORMATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKIN TUMOR; SQUAMOUS CELL CARCINOMA;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; CALGRANULIN A; CALGRANULIN B; CARCINOMA, SQUAMOUS CELL; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; KERATINOCYTES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKIN NEOPLASMS;

EID: 84926226232     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120971     Document Type: Article

References (66)

1. Euvrard S, Kanitakis J, Claudy A. Skin cancers after organ transplantation. N Engl J Med. 2003; 348 (17):1681-91. PMID: 12711744
2. Ackerman AB, Mones JM. Solar (actinic) keratosis is squamous cell carcinoma. Br J Dermatol. 2006; 155(1):9-22. PMID: 16792746
3. Fuchs A, Marmur E. The kinetics of skin cancer: progression of actinic keratosis to squamous cell carcinoma. Dermatol Surg. 2007; 33(9):1099-101. PMID: 17760601
4. Muhleisen B, Petrov I, Gachter T, Kurrer M, Scharer L, Dummer R, et al. Progression of cutaneous squamous cell carcinoma in immunosuppressed patients is associated with reduced CD123+ and FOXP3+ cells in the perineoplastic inflammatory infiltrate. Histopathology. 2009; 55(1):67-76. doi: 10.1111/j.1365-2559.2009.03324.x PMID: 19614769
5. Kosmidis M, Dziunycz P, Suarez-Farinas M, Muhleisen B, Scharer L, Lauchli S, et al. Immunosuppression affects CD4+ mRNA expression and induces Th2 dominance in the microenvironment of cutaneous squamous cell carcinoma in organ transplant recipients. J Immunother. 2010; 33(5):538-46. doi: 10.1097/CJI.0b013e3181cc2615 PMID: 20463594
6. Hofbauer GF, Bavinck JN, Euvrard S. Organ transplantation and skin cancer: basic problems and new perspectives. Exp Dermatol. 2010.
7. Tan TT, Coussens LM. Humoral immunity, inflammation and cancer. Curr Opin Immunol. 2007; 19 (2):209-16. PMID: 17276050
8. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006; 6(1):24-37. PMID: 16397525
9. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002; 420(6917):860-7. PMID: 12490959
10. Mueller MM. Inflammation in epithelial skin tumours: old stories and new ideas. Eur J Cancer. 2006; 42 (6):735-44. PMID: 16527478
11. Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, Pan YC, et al. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem. 1992; 267(21):14998-5004. PMID: 1378843
12. Miyata T, Hori O, Zhang J, Yan SD, Ferran L, Iida Y, et al. The receptor for advanced glycation end products (RAGE) is a central mediator of the interaction of AGE-beta2microglobulin with human mononuclear phagocytes via an oxidant-sensitive pathway. Implications for the pathogenesis of dialysis-related amyloidosis. J Clin Invest. 1996; 98(5):1088-94. PMID: 8787669
13. Shinohara M, Thornalley PJ, Giardino I, Beisswenger P, Thorpe SR, Onorato J, et al. Overexpression of glyoxalase-I in bovine endothelial cells inhibits intracellular advanced glycation endproduct formation and prevents hyperglycemia-induced increases in macromolecular endocytosis. J Clin Invest. 1998; 101(5):1142-7. PMID: 9486985
14. Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T, Arnold B, et al. Understanding RAGE, the receptor for advanced glycation end products. J Mol Med. 2005; 83(11):876-86. PMID: 16133426
15. Gebhardt C, Riehl A, Durchdewald M, Nemeth J, Furstenberger G, Muller-Decker K, et al. RAGE signaling sustains inflammation and promotes tumor development. J Exp Med. 2008; 205(2):275-85. doi: 10.1084/jem.20070679 PMID: 18208974
16. Schmidt AM, Yan SD, Yan SF, Stern DM. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest. 2001; 108(7):949-55. PMID: 11581294
17. Xu XC, Abuduhadeer X, Zhang WB, Li T, Gao H, Wang YH. Knockdown of RAGE inhibits growth and invasion of gastric cancer cells. European journal of histochemistry: EJH. 2013; 57(4):e36. doi: 10.4081/ejh.2013.e36 PMID: 24441189
18. Leibold JS, Riehl A, Hettinger J, Durben M, Hess J, Angel P. Keratinocyte-specific deletion of the receptor RAGE modulates the kinetics of skin inflammation in vivo. The Journal of investigative dermatology. 2013; 133(10):2400-6. doi: 10.1038/jid.2013.185 PMID: 23594597
19. Ghavami S, Rashedi I, Dattilo BM, Eshraghi M, Chazin WJ, Hashemi M, et al. S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J Leukoc Biol. 2008; 83(6):1484-92. doi: 10.1189/jlb.0607397 PMID: 18339893
20. Huttunen HJ, Fages C, Rauvala H. Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-kappaB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J Biol Chem. 1999; 274(28):19919-24. PMID: 10391939
21. Stern D, Yan SD, Yan SF, Schmidt AM. Receptor for advanced glycation endproducts: a multiligand receptor magnifying cell stress in diverse pathologic settings. Adv Drug Deliv Rev. 2002; 54(12):1615-25. PMID: 12453678
22. Taguchi A, Blood DC, del Toro G, Canet A, Lee DC, Qu W, et al. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature. 2000; 405(6784):354-60. PMID: 10830965
23. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 1999; 97(7):889-901. PMID: 10399917
24. Bjork P, Bjork A, Vogl T, Stenstrom M, Liberg D, Olsson A, et al. Identification of human S100A9 as a novel target for treatment of autoimmune disease via binding to quinoline-3-carboxamides. PLoS Biol. 2009; 7(4):e97. doi: 10.1371/journal.pbio.1000097 PMID: 19402754
25. McNeill E, Hogg N. S100A9 has a protective role in inflammation-induced skin carcinogenesis. International journal of cancer Journal international du cancer. 2014.
26. Bando M, Zou X, Hiroshima Y, Kataoka M, Ross KF, Shinohara Y, et al. Mechanism of interleukin-1alpha transcriptional regulation of S100A9 in a human epidermal keratinocyte cell line. Biochimica et biophysica acta. 2013; 1829(9):954-62. doi: 10.1016/j.bbagrm.2013.03.010 PMID: 23563247
27. Schonthaler HB, Guinea-Viniegra J, Wculek SK, Ruppen I, Ximenez-Embun P, Guio-Carrion A, et al. S100A8-S100A9 protein complex mediates psoriasis by regulating the expression of complement factor C3. Immunity. 2013; 39(6):1171-81. doi: 10.1016/j.immuni.2013.11.011 PMID: 24332034
28. Choi DK, Li ZJ, Chang IK, Yeo MK, Kim JM, Sohn KC, et al. Clinicopathological roles of S100A8 and S100A9 in cutaneous squamous cell carcinoma in vivo and in vitro. Archives of dermatological research. 2014.
29. Donato R. Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochimica et biophysica acta. 1999; 1450(3):191-231. PMID: 10395934
30. Kerkhoff C, Klempt M, Sorg C. Novel insights into structure and function of MRP8 (S100A8) and MRP14 (S100A9). Biochimica et biophysica acta. 1998; 1448(2):200-11. PMID: 9920411
31. Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nature medicine. 2007; 13(9):1042-9. PMID: 17767165
32. Kerkhoff C, Voss A, Scholzen TE, Averill MM, Zanker KS, Bornfeldt KE. Novel insights into the role of S100A8/A9 in skin biology. Exp Dermatol. 2012; 21(11):822-6. doi: 10.1111/j.1600-0625.2012.01571.x PMID: 22882537
33. Rammes A, Roth J, Goebeler M, Klempt M, Hartmann M, Sorg C. Myeloid-related protein (MRP) 8 and MRP14, calcium-binding proteins of the S100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J Biol Chem. 1997; 272(14):9496-502. PMID: 9083090
34. Foell D, Wittkowski H, Vogl T, Roth J. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol. 2007; 81(1):28-37. PMID: 16943388
35. Hermani A, De Servi B, Medunjanin S, Tessier PA, Mayer D. S100A8 and S100A9 activate MAP kinase and NF-kappaB signaling pathways and trigger translocation of RAGE in human prostate cancer cells. Exp Cell Res. 2006; 312(2):184-97. PMID: 16297907
36. Sunahori K, Yamamura M, Yamana J, Takasugi K, Kawashima M, Yamamoto H, et al. The S100A8/A9 heterodimer amplifies proinflammatory cytokine production by macrophages via activation of nuclear factor kappa B and p38 mitogen-activated protein kinase in rheumatoid arthritis. Arthritis Res Ther. 2006; 8(3):R69. PMID: 16613612
37. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol. 2001; 33(7):637-68. PMID: 11390274
38. Foell D, Seeliger S, Vogl T, Koch HG, Maschek H, Harms E, et al. Expression of S100A12 (EN-RAGE) in cystic fibrosis. Thorax. 2003; 58(7):613-7. PMID: 12832680
39. Gebhardt C, Nemeth J, Angel P, Hess J. S100A8 and S100A9 in inflammation and cancer. Biochem Pharmacol. 2006; 72(11):1622-31. PMID: 16846592
40. Arai K, Takano S, Teratani T, Ito Y, Yamada T, Nozawa R. S100A8 and S100A9 overexpression is associated with poor pathological parameters in invasive ductal carcinoma of the breast. Curr Cancer Drug Targets. 2008; 8(4):243-52. PMID: 18537548
41. Turovskaya O, Foell D, Sinha P, Vogl T, Newlin R, Nayak J, et al. RAGE, carboxylated glycans and S100A8/A9 play essential roles in colitis-associated carcinogenesis. Carcinogenesis. 2008; 29 (10):2035-43. doi: 10.1093/carcin/bgn188 PMID: 18689872
42. Shen J, Abel EL, Riggs PK, Repass J, Hensley SC, Schroeder LJ, et al. Proteomic and pathway analyses reveal a network of inflammatory genes associated with differences in skin tumor promotion susceptibility in DBA/2 and C57BL/6 mice. Carcinogenesis. 2012; 33(11):2208-19. doi: 10.1093/carcin/bgs213 PMID: 22782996
43. Djerbi N, Dziunycz PJ, Reinhardt D, Iotzova-Weiss G, Hafner J, Lauchli S, et al. Influence of cyclosporin and prednisolone on RAGE, S100A8/A9, and NFkappaB expression in human keratinocytes. JAMA dermatology. 2013; 149(2):236-7. doi: 10.1001/jamadermatol.2013.836 PMID: 23426492
44. Lagasse E, Clerc RG. Cloning and expression of two human genes encoding calcium-binding proteins that are regulated during myeloid differentiation. Mol Cell Biol. 1988; 8(6):2402-10. PMID: 3405210
45. Murao S, Collart F, Huberman E. A protein complex expressed during terminal differentiation of monomyelocytic cells is an inhibitor of cell growth. Cell Growth Differ. 1990; 1(10):447-54. PMID: 2278876
46. Rugtveit J, Haraldsen G, Hogasen AK, Bakka A, Brandtzaeg P, Scott H. Respiratory burst of intestinal macrophages in inflammatory bowel disease is mainly caused by CD14+L1+ monocyte derived cells. Gut. 1995; 37(3):367-73. PMID: 7590432
47. Haider AS, Peters SB, Kaporis H, Cardinale I, Fei J, Ott J, et al. Genomic analysis defines a cancerspecific gene expression signature for human squamous cell carcinoma and distinguishes malignant hyperproliferation from benign hyperplasia. The Journal of investigative dermatology. 2006; 126 (4):869-81. PMID: 16470182
48. Mitsui H, Suarez-Farinas M, Gulati N, Shah KR, Cannizzaro MV, Coats I, et al. Gene expression profiling of the leading edge of cutaneous squamous cell carcinoma: IL-24-driven MMP-7. The Journal of investigative dermatology. 2014; 134(5):1418-27. doi: 10.1038/jid.2013.494 PMID: 24270662
49. Ghavami S, Eshragi M, Ande SR, Chazin WJ, Klonisch T, Halayko AJ, et al. S100A8/A9 induces autophagy and apoptosis via ROS-mediated cross-talk between mitochondria and lysosomes that involves BNIP3. Cell Res. 2009.
50. Ghavami S, Kerkhoff C, Chazin WJ, Kadkhoda K, Xiao W, Zuse A, et al. S100A8/9 induces cell death via a novel, RAGE-independent pathway that involves selective release of Smac/DIABLO and Omi/HtrA2. Biochimica et biophysica acta. 2008; 1783(2):297-311. PMID: 18060880
51. Nukui T, Ehama R, Sakaguchi M, Sonegawa H, Katagiri C, Hibino T, et al. S100A8/A9, a key mediator for positive feedback growth stimulation of normal human keratinocytes. J Cell Biochem. 2008; 104 (2):453-64. PMID: 18044712
52. Ichikawa M, Williams R, Wang L, Vogl T, Srikrishna G. S100A8/A9 activate key genes and pathways in colon tumor progression. Mol Cancer Res. 2011; 9(2):133-48. doi: 10.1158/1541-7786.MCR-10-0394 PMID: 21228116
53. Junttila MR, Li SP, Westermarck J. Phosphatase-mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. FASEB J. 2008; 22(4):954-65. PMID: 18039929
54. Eue I, Sorg C. Arachidonic acid specifically regulates binding of S100A8/9, a heterodimer complex of the S100 class of calcium binding proteins, to human microvascular endothelial cells. Atherosclerosis. 2001; 154(2):505-8. PMID: 11263412
55. Kerkhoff C, Vogl T, Nacken W, Sopalla C, Sorg C. Zinc binding reverses the calcium-induced arachidonic acid-binding capacity of the S100A8/A9 protein complex. FEBS Lett. 1999; 460(1):134-8. PMID: 10571075
56. Vandal K, Rouleau P, Boivin A, Ryckman C, Talbot M, Tessier PA. Blockade of S100A8 and S100A9 suppresses neutrophil migration in response to lipopolysaccharide. J Immunol. 2003; 171(5):2602-9. PMID: 12928412
57. van Lent PL, Grevers L, Blom AB, Sloetjes A, Mort JS, Vogl T, et al. Myeloid-related proteins S100A8/ S100A9 regulate joint inflammation and cartilage destruction during antigen-induced arthritis. Annals of the rheumatic diseases. 2008; 67(12):1750-8. PMID: 18055478
58. Qin F, Song Y, Li Z, Zhao L, Zhang Y, Geng L. S100A8/A9 Induces Apoptosis and Inhibits Metastasis of CasKi Human Cervical Cancer Cells. Pathol Oncol Res. 2009.
59. Bluth MJ, Zaba LC, Moussai D, Suarez-Farinas M, Kaporis H, Fan L, et al. Myeloid dendritic cells from human cutaneous squamous cell carcinoma are poor stimulators of T-cell proliferation. The Journal of investigative dermatology. 2009; 129(10):2451-62. doi: 10.1038/jid.2009.96 PMID: 19387481
60. Brooks YS, Ostano P, Jo SH, Dai J, Getsios S, Dziunycz P, et al. Multifactorial ERbeta and NOTCH1 control of squamous differentiation and cancer. J Clin Invest. 2014; 124(5):2260-76. doi: 10.1172/JCI72718 PMID: 24743148
61. Dziunycz PJ, Lefort K, Wu X, Freiberger SN, Neu J, Djerbi N, et al. The oncogene ATF3 is potentiated by cyclosporine A and ultraviolet light A. The Journal of investigative dermatology. 2014; 134(7):1998-2004. doi: 10.1038/jid.2014.77 PMID: 24509533
62. Restivo G, Nguyen BC, Dziunycz P, Ristorcelli E, Ryan RJ, Ozuysal OY, et al. IRF6 is a mediator of Notch pro-differentiation and tumour suppressive function in keratinocytes. The EMBO journal. 2011; 30(22):4571-85. doi: 10.1038/emboj.2011.325 PMID: 21909072
63. Dziunycz P, Hofbauer GF. Immune phenotype of peripheral blood cells and skin squamous cell carcinoma in organ transplant recipients. Expert review of clinical immunology. 2010; 6(3):359-62. doi: 10.1586/eci.10.21 PMID: 20441422
64. Wu X, Nguyen BC, Dziunycz P, Chang S, Brooks Y, Lefort K, et al. Opposing roles for calcineurin and ATF3 in squamous skin cancer. Nature. 2010; 465(7296):368-72. doi: 10.1038/nature08996 PMID: 20485437
65. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3(6):1101-8. PMID: 18546601
66. Hunter MJ, Chazin WJ. High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factor-related proteins 8 and 14. J Biol Chem. 1998; 273(20):12427-35. PMID: 9575199