S100A8/A9 (Calprotectin) Negatively Regulates G2/M Cell Cycle Progression and Growth of Squamous Cell Carcinoma

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Khammanivong, Ali ^a   Wang, Chengxing ^a   Sorenson, Brent S ^a   Ross, Karen F ^a   Herzberg, Mark C ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN; CHECKPOINT KINASE 1; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; SHORT HAIRPIN RNA; THREONINE; TYROSINE;

ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CARCINOGENESIS; CARCINOMA CELL; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GENE SILENCING; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MITOSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

CALGRANULIN A; CALGRANULIN B; CARCINOMA, SQUAMOUS CELL; CELL DIVISION; CELL LINE, TUMOR; CELL PROLIFERATION; G2 PHASE; G2 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HUMANS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN PHOSPHATASE 2; SIGNAL TRANSDUCTION;

EID: 84879938648     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069395     Document Type: Article

References (66)

1. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
2. Ross KF, Herzberg MC, (2001) Calprotectin expression by gingival epithelial cells. Infect Immun 69: 3248-3254.
3. Hitomi J, Kimura T, Kusumi E, Nakagawa S, Kuwabara S, et al. (1998) Novel S100 proteins in human esophageal epithelial cells: CAAF1 expression is associated with cell growth arrest. Arch Histol Cytol 61: 163-178.
4. Itou H, Yao M, Fujita I, Watanabe N, Suzuki M, et al. (2002) The crystal structure of human MRP14 (S100A9), a Ca(2+)-dependent regulator protein in inflammatory process. J Mol Biol 316: 265-276.
5. Hessian PA, Fisher L, (2001) The heterodimeric complex of MRP-8 (S100A8) and MRP-14 (S100A9). Antibody recognition, epitope definition and the implications for structure. Eur J Biochem 268: 353-363.
6. Hsu K, Champaiboon C, Guenther BD, Sorenson BS, Khammanivong A, et al. (2009) Anti-Infective Protective Properties of S100 Calgranulins. Antiinflamm Antiallergy Agents Med Chem 8: 290-305.
7. Gebhardt C, Breitenbach U, Tuckermann JP, Dittrich BT, Richter KH, et al. (2002) Calgranulins S100A8 and S100A9 are negatively regulated by glucocorticoids in a c-Fos-dependent manner and overexpressed throughout skin carcinogenesis. Oncogene 21: 4266-4276.
8. Hermani A, De Servi B, Medunjanin S, Tessier PA, Mayer D, (2006) S100A8 and S100A9 activate MAP kinase and NF-kappaB signaling pathways and trigger translocation of RAGE in human prostate cancer cells. Exp Cell Res 312: 184-197.
9. Gebhardt C, Nemeth J, Angel P, Hess J, (2006) S100A8 and S100A9 in inflammation and cancer. Biochem Pharmacol 72: 1622-1631.
10. Ehrchen JM, Sunderkotter C, Foell D, Vogl T, Roth J, (2009) The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J Leukoc Biol 86: 557-566.
11. Turovskaya O, Foell D, Sinha P, Vogl T, Newlin R, et al. (2008) RAGE, carboxylated glycans and S100A8/A9 play essential roles in colitis-associated carcinogenesis. Carcinogenesis 29: 2035-2043.
12. Arai K, Takano S, Teratani T, Ito Y, Yamada T, et al. (2008) S100A8 and S100A9 overexpression is associated with poor pathological parameters in invasive ductal carcinoma of the breast. Curr Cancer Drug Targets 8: 243-252.
13. Moon A, Yong HY, Song JI, Cukovic D, Salagrama S, et al. (2008) Global gene expression profiling unveils S100A8/A9 as candidate markers in H-ras-mediated human breast epithelial cell invasion. Mol Cancer Res 6: 1544-1553.
14. Ito Y, Arai K, Nozawa R, Yoshida H, Hirokawa M, et al. (2009) S100A8 and S100A9 expression is a crucial factor for dedifferentiation in thyroid carcinoma. Anticancer Res 29: 4157-4161.
15. Nemeth J, Stein I, Haag D, Riehl A, Longerich T, et al. (2009) S100A8 and S100A9 are novel nuclear factor kappa B target genes during malignant progression of murine and human liver carcinogenesis. Hepatology 50: 1251-1262.
16. Yong HY, Moon A, (2007) Roles of calcium-binding proteins, S100A8 and S100A9, in invasive phenotype of human gastric cancer cells. Arch Pharm Res 30: 75-81.
17. Odegaard E, Davidson B, Elgaaen BV, Fagerhol MK, Engh V, et al. (2008) Circulating calprotectin in ovarian carcinomas and borderline tumors of the ovary. Am J Obstet Gynecol 198: 418 e411-417.
18. Yao R, Lopez-Beltran A, Maclennan GT, Montironi R, Eble JN, et al. (2007) Expression of S100 protein family members in the pathogenesis of bladder tumors. Anticancer Res 27: 3051-3058.
19. Arai K, Teratani T, Nozawa R, Yamada T, (2001) Immunohistochemical investigation of S100A9 expression in pulmonary adenocarcinoma: S100A9 expression is associated with tumor differentiation. Oncol Rep 8: 591-596.
20. Melle C, Ernst G, Schimmel B, Bleul A, Koscielny S, et al. (2004) A technical triade for proteomic identification and characterization of cancer biomarkers. Cancer Res 64: 4099-4104.
21. Gonzalez HE, Gujrati M, Frederick M, Henderson Y, Arumugam J, et al. (2003) Identification of 9 genes differentially expressed in head and neck squamous cell carcinoma. Arch Otolaryngol Head Neck Surg 129: 754-759.
22. Fung LF, Lo AK, Yuen PW, Liu Y, Wang XH, et al. (2000) Differential gene expression in nasopharyngeal carcinoma cells. Life Sci 67: 923-936.
23. Kong JP, Ding F, Zhou CN, Wang XQ, Miao XP, et al. (2004) Loss of myeloid-related proteins 8 and myeloid-related proteins 14 expression in human esophageal squamous cell carcinoma correlates with poor differentiation. World J Gastroenterol 10: 1093-1097.
24. Wang J, Cai Y, Xu H, Zhao J, Xu X, et al. (2004) Expression of MRP14 gene is frequently down-regulated in Chinese human esophageal cancer. Cell Res 14: 46-53.
25. Tugizov S, Berline J, Herrera R, Penaranda ME, Nakagawa M, et al. (2005) Inhibition of human papillomavirus type 16 E7 phosphorylation by the S100 MRP-8/14 protein complex. J Virol 79: 1099-1112.
26. Coleman N, Stanley MA, (1994) Expression of the myelomonocytic antigens CD36 and L1 by keratinocytes in squamous intraepithelial lesions of the cervix. Hum Pathol 25: 73-79.
27. Forester CM, Maddox J, Louis JV, Goris J, Virshup DM, (2007) Control of mitotic exit by PP2A regulation of Cdc25C and Cdk1. Proceedings of the National Academy of Sciences of the United States of America 104: 19867-19872.
28. Margolis SS, Perry JA, Forester CM, Nutt LK, Guo Y, et al. (2006) Role for the PP2A/B56delta phosphatase in regulating 14-3-3 release from Cdc25 to control mitosis. Cell 127: 759-773.
29. Guenin S, Schwartz L, Morvan D, Steyaert JM, Poignet A, et al. (2008) PP2A activity is controlled by methylation and regulates oncoprotein expression in melanoma cells: a mechanism which participates in growth inhibition induced by chloroethylnitrosourea treatment. Int J Oncol 32: 49-57.
30. Glatter T, Wepf A, Aebersold R, Gstaiger M, (2009) An integrated workflow for charting the human interaction proteome: insights into the PP2A system. Mol Syst Biol 5: 237.
31. Driemel O, Murzik U, Escher N, Melle C, Bleul A, et al. (2007) Protein profiling of oral brush biopsies: S100A8 and S100A9 can differentiate between normal, premalignant, and tumor cells. Proteomics Clin Appl 1: 486-493.
32. Roesch Ely M, Nees M, Karsai S, Magele I, Bogumil R, et al. (2005) Transcript and proteome analysis reveals reduced expression of calgranulins in head and neck squamous cell carcinoma. Eur J Cell Biol 84: 431-444.
33. Soni DV, Sramkoski RM, Lam M, Stefan T, Jacobberger JW, (2008) Cyclin B1 is rate limiting but not essential for mitotic entry and progression in mammalian somatic cells. Cell Cycle 7: 1285-1300.
34. Perrotti D, Neviani P, (2008) Protein phosphatase 2A (PP2A), a drugable tumor suppressor in Ph1(+) leukemias. Cancer Metastasis Rev 27: 159-168.
35. Champaiboon C, Sappington KJ, Guenther BD, Ross KF, Herzberg MC, (2009) Calprotectin S100A9 calcium-binding loops I and II are essential for keratinocyte resistance to bacterial invasion. J Biol Chem 284: 7078-7090.
36. Agarwal C, Singh RP, Dhanalakshmi S, Tyagi AK, Tecklenburg M, et al. (2003) Silibinin upregulates the expression of cyclin-dependent kinase inhibitors and causes cell cycle arrest and apoptosis in human colon carcinoma HT-29 cells. Oncogene 22: 8271-8282.
37. Taylor WR, Stark GR, (2001) Regulation of the G2/M transition by p53. Oncogene 20: 1803-1815.
38. Peng CY, Graves PR, Thoma RS, Wu Z, Shaw AS, et al. (1997) Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277: 1501-1505.
39. Peng CY, Graves PR, Ogg S, Thoma RS, Byrnes MJ 3rd, et al. (1998) C-TAK1 protein kinase phosphorylates human Cdc25C on serine 216 and promotes 14-3-3 protein binding. Cell Growth Differ 9: 197-208.
40. Graves PR, Lovly CM, Uy GL, Piwnica-Worms H, (2001) Localization of human Cdc25C is regulated both by nuclear export and 14-3-3 protein binding. Oncogene 20: 1839-1851.
41. Ozen M, Ittmann M, (2005) Increased expression and activity of CDC25C phosphatase and an alternatively spliced variant in prostate cancer. Clin Cancer Res 11: 4701-4706.
42. Shiromizu T, Goto H, Tomono Y, Bartek J, Totsukawa G, et al. (2006) Regulation of mitotic function of Chk1 through phosphorylation at novel sites by cyclin-dependent kinase 1 (Cdk1). Genes Cells 11: 477-485.
43. Franckhauser C, Mamaeva D, Heron-Milhavet L, Fernandez A, Lamb NJ, (2010) Distinct pools of cdc25C are phosphorylated on specific TP sites and differentially localized in human mitotic cells. PLoS One 5: e11798.
44. Bulavin DV, Higashimoto Y, Demidenko ZN, Meek S, Graves P, et al. (2003) Dual phosphorylation controls Cdc25 phosphatases and mitotic entry. Nat Cell Biol 5: 545-551.
45. Yang J, Wu LJ, Tashino S, Onodera S, Ikejima T, (2010) Protein tyrosine kinase pathway-derived ROS/NO productions contribute to G2/M cell cycle arrest in evodiamine-treated human cervix carcinoma HeLa cells. Free Radic Res 44: 792-802.
46. Maalouf M, Alphonse G, Colliaux A, Beuve M, Trajkovic-Bodennec S, et al. (2009) Different mechanisms of cell death in radiosensitive and radioresistant p53 mutated head and neck squamous cell carcinoma cell lines exposed to carbon ions and x-rays. Int J Radiat Oncol Biol Phys 74: 200-209.
47. Wang XM, Li J, Feng XC, Wang Q, Guan DY, et al. (2008) Involvement of the role of Chk1 in lithium-induced G2/M phase cell cycle arrest in hepatocellular carcinoma cells. J Cell Biochem 104: 1181-1191.
48. Voss A, Bode G, Sopalla C, Benedyk M, Varga G, et al. (2011) Expression of S100A8/A9 in HaCaT keratinocytes alters the rate of cell proliferation and differentiation. FEBS Lett 585: 440-446.
49. Qin F, Song Y, Li Z, Zhao L, Zhang Y, et al. (2010) S100A8/A9 induces apoptosis and inhibits metastasis of CasKi human cervical cancer cells. Pathol Oncol Res 16: 353-360.
50. Nukui T, Ehama R, Sakaguchi M, Sonegawa H, Katagiri C, et al. (2008) S100A8/A9, a key mediator for positive feedback growth stimulation of normal human keratinocytes. J Cell Biochem 104: 453-464.
51. Ghavami S, Rashedi I, Dattilo BM, Eshraghi M, Chazin WJ, et al. (2008) S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J Leukoc Biol 83: 1484-1492.
52. Ghavami S, Kerkhoff C, Chazin WJ, Kadkhoda K, Xiao W, et al. (2008) S100A8/9 induces cell death via a novel, RAGE-independent pathway that involves selective release of Smac/DIABLO and Omi/HtrA2. Biochim Biophys Acta 1783: 297-311.
53. Chen J, Martin BL, Brautigan DL, (1992) Regulation of protein serine-threonine phosphatase type-2A by tyrosine phosphorylation. Science 257: 1261-1264.
54. Xiong Y, Jing XP, Zhou XW, Wang XL, Yang Y, et al. (2013) Zinc induces protein phosphatase 2A inactivation and tau hyperphosphorylation through Src dependent PP2A (tyrosine 307) phosphorylation. Neurobiol Aging 34: 745-756.
55. Pitre A, Davis N, Paul M, Orr AW, Skalli O, (2012) Synemin promotes AKT-dependent glioblastoma cell proliferation by antagonizing PP2A. Mol Biol Cell 23: 1243-1253.
56. Hofstetter CP, Burkhardt JK, Shin BJ, Gursel DB, Mubita L, et al. (2012) Protein phosphatase 2A mediates dormancy of glioblastoma multiforme-derived tumor stem-like cells during hypoxia. PLoS One 7: e30059.
57. Zhou XZ, Kops O, Werner A, Lu PJ, Shen M, et al. (2000) Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell 6: 873-883.
58. Rupniak HT, Rowlatt C, Lane EB, Steele JG, Trejdosiewicz LK, et al. (1985) Characteristics of four new human cell lines derived from squamous cell carcinomas of the head and neck. J Natl Cancer Inst 75: 621-635.
59. Eicher SA, Clayman GL, Liu TJ, Shillitoe EJ, Storthz KA, et al. (1996) Evaluation of topical gene therapy for head and neck squamous cell carcinoma in an organotypic model. Clin Cancer Res 2: 1659-1664.
60. Lee Y, Yang X, Huang Y, Fan H, Zhang Q, et al. (2010) Network modeling identifies molecular functions targeted by miR-204 to suppress head and neck tumor metastasis. PLoS Comput Biol 6: e1000730.
61. Kumar P, Gao Q, Ning Y, Wang Z, Krebsbach PH, et al. (2008) Arsenic trioxide enhances the therapeutic efficacy of radiation treatment of oral squamous carcinoma while protecting bone. Mol Cancer Ther 7: 2060-2069.
62. Worsham MJ, Chen KM, Meduri V, Nygren AO, Errami A, et al. (2006) Epigenetic events of disease progression in head and neck squamous cell carcinoma. Arch Otolaryngol Head Neck Surg 132: 668-677.
63. Nisapakultorn K, Ross KF, Herzberg MC, (2001) Calprotectin expression in vitro by oral epithelial cells confers resistance to infection by Porphyromonas gingivalis. Infect Immun 69: 4242-4247.
64. Sorenson BS, Khammanivong A, Guenther BD, Ross KF, Herzberg MC, (2012) IL-1 receptor regulates S100A8/A9-dependent keratinocyte resistance to bacterial invasion. Mucosal Immunol 5: 66-75.
65. Krutzik PO, Nolan GP, (2003) Intracellular phospho-protein staining techniques for flow cytometry: monitoring single cell signaling events. Cytometry A 55: 61-70.
66. Perry JA, Kornbluth S, (2007) Cdc25 and Wee1: analogous opposites? Cell division 2: 12.