S100A11, an Dual Mediator for Growth Regulation of Human Keratinocytes

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2007 Nov 6

PMID 17978094

Citations 50

Authors

Masakiyo Sakaguchi

Hiroyuki Sonegawa

Hitoshi Murata

Midori Kitazoe

Jun-Ichiro Futami

Ken Kataoka

Hidenori Yamada

Nam-Ho Huh

Affiliations

Soon will be listed here.

Abstract

We previously revealed a novel signal pathway involving S100A11 for inhibition of the growth of normal human keratinocytes (NHK) caused by high Ca(++) or transforming growth factor beta. Exposure to either agent resulted in transfer of S100A11 to nuclei, where it induced p21(WAF1). In contrast, S100A11 has been shown to be overexpressed in many human cancers. To address this apparent discrepancy, we analyzed possible new functions of S100A11, and we provide herein evidence that 1) S100A11 is actively secreted by NHK; 2) extracellular S100A11 acts on NHK to enhance the production of epidermal growth factor family proteins, resulting in growth stimulation; 3) receptor for advanced glycation end products, nuclear factor-kappaB, Akt, and cAMP response element-binding protein are involved in the S100A11-triggered signal transduction; and 4) production and secretion of S100A11 are markedly enhanced in human squamous cancer cells. These findings indicate that S100A11 plays a dual role in growth regulation of epithelial cells.

Citing Articles

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References

Xu D, Kyriakis J . Phosphatidylinositol 3'-kinase-dependent activation of renal mesangial cell Ki-Ras and ERK by advanced glycation end products. J Biol Chem. 2003; 278(41):39349-55. DOI: 10.1074/jbc.M302771200. View

Marenholz I, Heizmann C, Fritz G . S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun. 2004; 322(4):1111-22. DOI: 10.1016/j.bbrc.2004.07.096. View

Lugering N, Stoll R, Kucharzik T, Schmid K, Rohlmann G, Burmeister G . Immunohistochemical distribution and serum levels of the Ca(2+)-binding proteins MRP8, MRP14 and their heterodimeric form MRP8/14 in Crohn's disease. Digestion. 1995; 56(5):406-14. DOI: 10.1159/000201267. View

Hofmann M, Drury S, Fu C, Qu W, Taguchi A, Lu Y . RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 1999; 97(7):889-901. DOI: 10.1016/s0092-8674(00)80801-6. View

Oue N, Hamai Y, Mitani Y, Matsumura S, Oshimo Y, Aung P . Gene expression profile of gastric carcinoma: identification of genes and tags potentially involved in invasion, metastasis, and carcinogenesis by serial analysis of gene expression. Cancer Res. 2004; 64(7):2397-405. DOI: 10.1158/0008-5472.can-03-3514. View

Ryckman C, Vandal K, Rouleau P, Talbot M, Tessier P . Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J Immunol. 2003; 170(6):3233-42. DOI: 10.4049/jimmunol.170.6.3233. View

Schaefer K, Brachwitz K, Wai D, Braun Y, Diallo R, Korsching E . Expression profiling of t(12;22) positive clear cell sarcoma of soft tissue cell lines reveals characteristic up-regulation of potential new marker genes including ERBB3. Cancer Res. 2004; 64(10):3395-405. DOI: 10.1158/0008-5472.CAN-03-0809. View

Sarkadi B, Price E, Boucher R, Germann U, Scarborough G . Expression of the human multidrug resistance cDNA in insect cells generates a high activity drug-stimulated membrane ATPase. J Biol Chem. 1992; 267(7):4854-8. View

Gupta G, Nguyen D, Chiang A, Bos P, Kim J, Nadal C . Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature. 2007; 446(7137):765-70. DOI: 10.1038/nature05760. View

10.

Bogumil T, Rieckmann P, Kubuschok B, FELGENHAUER K, Bruck W . Serum levels of macrophage-derived protein MRP-8/14 are elevated in active multiple sclerosis. Neurosci Lett. 1998; 247(2-3):195-7. DOI: 10.1016/s0304-3940(98)00263-8. View

11.

Foell D, Frosch M, Sorg C, Roth J . Phagocyte-specific calcium-binding S100 proteins as clinical laboratory markers of inflammation. Clin Chim Acta. 2004; 344(1-2):37-51. DOI: 10.1016/j.cccn.2004.02.023. View

12.

Todoroki H, Kobayashi R, Watanabe M, Minami H, Hidaka H . Purification, characterization, and partial sequence analysis of a newly identified EF-hand type 13-kDa Ca(2+)-binding protein from smooth muscle and non-muscle tissues. J Biol Chem. 1991; 266(28):18668-73. View

13.

Arumugam T, Simeone D, Schmidt A, Logsdon C . S100P stimulates cell proliferation and survival via receptor for activated glycation end products (RAGE). J Biol Chem. 2003; 279(7):5059-65. DOI: 10.1074/jbc.M310124200. View

14.

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. DOI: 10.1016/s1357-2725(01)00046-2. View

15.

Liao H, Wu J, Kuhn E, Chin W, Chang B, Jones M . Use of mass spectrometry to identify protein biomarkers of disease severity in the synovial fluid and serum of patients with rheumatoid arthritis. Arthritis Rheum. 2004; 50(12):3792-803. DOI: 10.1002/art.20720. View

16.

Huttunen H, 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. DOI: 10.1074/jbc.274.28.19919. View

17.

Mailliard W, Haigler H, Schlaepfer D . Calcium-dependent binding of S100C to the N-terminal domain of annexin I. J Biol Chem. 1996; 271(2):719-25. DOI: 10.1074/jbc.271.2.719. View

18.

Kuruto R, Nozawa R, Takeishi K, Arai K, Yokota T, Takasaki Y . Myeloid calcium binding proteins: expression in the differentiated HL-60 cells and detection in sera of patients with connective tissue diseases. J Biochem. 1990; 108(4):650-3. DOI: 10.1093/oxfordjournals.jbchem.a123257. View

19.

Ehlermann P, Eggers K, Bierhaus A, Most P, Weichenhan D, Greten J . Increased proinflammatory endothelial response to S100A8/A9 after preactivation through advanced glycation end products. Cardiovasc Diabetol. 2006; 5:6. PMC: 1475836. DOI: 10.1186/1475-2840-5-6. View

20.

Heizmann C, Fritz G, Schafer B . S100 proteins: structure, functions and pathology. Front Biosci. 2002; 7:d1356-68. DOI: 10.2741/A846. View