Peptidoglycan from Staphylococcus aureus has an anti-apoptotic effect in HaCaT keratinocytes mediated by the production of the cellular inhibitor of apoptosis protein-2

Microbiology and Immunology

Volumn 58, Issue 2, 2014, Pages 87-95

  Vázquez Sánchez, Ernesto Antonio ^a   Rodríguez Romero, Magdalena ^a   Sánchez Torres, Luvia Enid ^a   Rodríguez Martínez, Sandra ^a   Cancino Diaz, Juan Carlos ^a   Rodríguez Cortes, Octavio ^b   García López, Eduardo Stalin ^c   Cancino Diaz, Mario Eugenio ^a  

^a National School Biological Sciences National Polytechnic Institute   (Mexico)

^b Department of Immunology   (Mexico)

^c Juárez Hospital of Mexico   (Mexico)

Author keywords

Apoptosis; Cellular inhibitor of apoptosis protein 2; Keratinocytes; Peptidoglycan

Indexed keywords

APOPTOSIS; CELLULAR INHIBITOR OF APOPTOSIS PROTEIN-2; KERATINOCYTES; PEPTIDOGLYCAN;

ANTIMICROBIAL CATIONIC PEPTIDES; APOPTOSIS; CELL LINE; GENE EXPRESSION; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; INTERLEUKIN-8; KERATINOCYTES; PEPTIDOGLYCAN; STAPHYLOCOCCUS AUREUS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84894095288     PISSN: 03855600     EISSN: 13480421     Source Type: Journal    
DOI: 10.1111/1348-0421.12126     Document Type: Article

References (41)

1. Williams R.E. (1967) Staphylococcus aureus as commensal and pathogen. Pathol Microbiol (Basel) 30: 932-45.
2. Kennedy-Crispin M., Billick E., Mitsui H., Gulati N., Fujita H., Gilleaudeau P., Sullivan-Whalen M., Johnson-Huang L.M., Suárez-Fariñas M., Krueger J.G. (2011) Human keratinocytes response to injury upregulates CCL20 and other genes linking innate and adaptive immunity. J Invest Dermatol 132: 105-13.
3. Voorhees T., Chang J., Yao Y., Kaplan M.H., Chang C.H., Travers J.B. (2011) Dendritic cells produce inflammatory cytokines in response to bacterial products from Staphylococcus aureus-infected atopic dermatitis lesions. Cell Immunol 267: 17-22.
4. Holland D.B., Bojar R.A., Farrar M.D., Holland K.T. (2009) Differential innate immune responses of a living skin equivalent model colonized by Staphylococcus epidermidis or Staphylococcus aureus. FEMS Microbiol Lett 290: 149-55.
5. Kawai K., Shimura H., Minagawa M., Ito A., Tomiyama K., Ito M. (2002) Expression of functional Toll-like receptor 2 on human epidermal keratinocytes. J Dermatol Sci 30: 185-94.
6. Flacher V., Bouschbacher M., Verronèse E., Massacrier C., Sisirak V., Berthier-Vergnes O., de Saint-Vis B., Caux C., Dezutter-Dambuyant C., Lebecque S., Valladeau J. (2006) Human Langerhans cells express a specific TLR profile and differentially respond to viruses and gram-positive bacteria. J Immunol 177: 7959-67.
7. Matsubara M., Harada D., Manabe H., Hasegawa K. (2004) Staphylococcus aureus peptidoglycan stimulates granulocyte macrophage colony-stimulating factor production from human epidermal keratinocytes via mitogen-activated protein kinases. FEBS Lett 566: 195-200.
8. Niebuhr M., Baumert K., Werfel T. (2010) TLR-2-mediated cytokine and chemokine secretion in human keratinocytes. Exp Dermatol 19: 873-7.
9. Olaru F., Jensen L.E. (2010) Staphylococcus aureus stimulates neutrophil targeting chemokine expression in keratinocytes through an autocrine IL-1alpha signaling loop. J Invest Dermatol 130: 1866-7.
10. Tohyama M., Sayama K., Komatsuzawa H., Hanakawa Y., Shirakata Y., Dai X., Yang L., Tokumaru S., Nagai H., Hirakawa S., Sugai M., Hashimoto K. (2007) CXCL16 is a novel mediator of the innate immunity of epidermal keratinocytes. Int Immunol 19: 1095-102.
11. Kobayashi M., Yoshiki R., Sakabe J., Kabashima K., Nakamura M., Tokura Y. (2009) Expression of Toll-like receptor 2, NOD2 and dectin-1 and stimulatory effects of their ligands and histamine in normal human keratinocytes. Br J Dermatol 160: 297-304.
12. Köllisch G., Kalali B.N., Voelcker V., Wallich R., Behrendt H., Ring J., Bauer S., Jakob T., Mempel M., Ollert M. (2005) Various members of the Toll-like receptor family contribute to the innate immune response of human epidermal keratinocytes. Immunology 114: 531-4.
13. Matsui K., Nishikawa A. (2013) Peptidoglycan-induced T helper 2 immune response in mice involves interleukin-10 secretion from Langerhans cells. Microbiol Immunol 57: 130-8.
14. Kim J.M., Lee J.Y., Kim Y.J. (2008) Inhibition of apoptosis in Bacteroides fragilis enterotoxin-stimulated intestinal epithelial cells through the induction of c-IAP-2. Eur J Immunol 38: 2190-9.
15. Liu J., Enomoto S., Lancto C.A., Abrahamsen M.S., Rutherford M.S. (2008) Inhibition of apoptosis in Cryptosporidium parvum-infected intestinal epithelial cells is dependent on survivin. Infect Immun 76: 3784-92.
16. Follows S.A., Murlidharan J., Massari P., Wetzler L.M., Genco C.A. (2009) Neisseria gonorrhoeae infection protects human endocervical epithelial cells from apoptosis via expression of host antiapoptotic proteins. Infect Immun 77: 3602-10.
17. Li Z., Chen J., Chan K.W., Qiao L., Wong B.C. (2011) A possible role of cIAP2 in Helicobacter pylori-associated gastric cancer. Cancer Lett 313: 192-200.
18. Karatsaidis A., Hayashi K., Schreurs O., Helgeland K., Schenck K. (2007) Survival signalling in keratinocytes of erythematous oral lichen planus. J Oral Pathol Med 36: 215-22.
19. Tovar-Castillo L.E., Cancino-Diaz J.C., Garcia-Vazquez F., Cancino-Gomez F.G., Leon-Dorantes G., Blancas-Gonzalez F., Jimenez-Zamudio L., Garcia-Latorre E., Cancino-Diaz M.E. (2007) Under-expression of VHL and over-expression of HDAC1, HIF-1alpha, LL37 and IAP-2 in affected skin biopsies of patients with psoriasis. Inter J Dermatol 46: 239-46.
20. Rodríguez-Martínez S., Cancino-Diaz J.C., Vargas-Zuñiga M., Cancino-Diaz M.E. (2008) LL37 regulates the over-expression of VEGF and c-IAP2 in human keratinocytes. Inter J Dermatol 47: 457-62.
21. Ruíz-González V., Cancino-Diaz J.C., Rodríguez-Martínez S., Cancino-Diaz M.E. (2009) Keratinocytes treated with peptidoglycan from Staphylococcus aureus produce VEGF, and its expression is amplified by the subsequent production of IL-13. Inter J Dermatol 48: 846-54.
22. Kränke B.B. (2005) Staphylococcal toxins in patients with psoriasis, atopic dermatitis, and erythroderma, and in healthy control subjects. J Am Acad Dermatol 53: 67-72.
23. Sun Y., Ottosson A., Pervaiz S., Fadeel B. (2003) Smac-mediated sensitization of human B lymphoma cells to staurosporine- and lactacystin-triggered apoptosis is apoptosome-dependent. Leukemia 21: 1035-43.
24. Fukui A., Ohta K., Nishi H., Shigeishi H., Tobiume K., Takechi M., Kamata N. (2013) Interleukin-8 and CXCL10 expression in oral keratinocytes and fibroblasts via Toll-like receptors. Microbiol Immunol 57: 198-206.
25. Nickoloff B.J., Qin J.Z., Nestle F.O. (2007) Immunopathogenesis of psoriasis. Clin Rev Allergy Immunol 33: 45-6.
26. Brook I., Frazier E.H., Yeager J.K. (1999) Microbiology of infected pustular psoriasis lesions. Int J Dermatol 38: 579-81.
27. Noble W.C. (1998) Skin bacteriology and the role of Staphylococcus aureus in infection. Br J Dermatol 139: 9-12.
28. Yarwood J.M., Leung D.Y., Schlievert P.M. (2000) Evidence for the involvement of bacterial superantigens in psoriasis, atopic dermatitis, and Kawasaki syndrome. FEMS Microbiol Lett 192: 1-7.
29. Baker B.S., Laman J.D., Powles A., van der Fits L., Voerman J.S., Melief M.J., Fry L. (2006) Peptidoglycan and peptidoglycan-specific Th1 cells in psoriatic skin lesions. J Pathol 209: 174-81.
30. Bonifati C., Carducci M., Cordiali F.P., Trento E., Sacerdoti G., Fazio M., Ameglio F. (1994) Correlated increases of tumour necrosis factor-alpha, interleukin-6 and granulocyte monocyte-colony stimulating factor levels in suction blister fluids and sera of psoriatic patients-relationships with disease severity. Clin Exp Dermatol 19: 383-7.
31. Chamorro C.I., Weber G., Grönberg A., Pivarcsi A., Ståhle M. (2008) The human antimicrobial peptide LL-37 suppresses apoptosis in keratinocytes. J Invest Dermatol 129: 937-44.
32. Shimizu D., Peters J.H., Vallboehmer D., Kuramochi H., Uchida K., Schneider S., Chandrasoma P.T., Danenberg K.D., Demeester T.R., Danenberg P.V. (2004) Cyclooxygenase-2 (COX-2) mediated anti-apoptosis may occur via Bcl-2 in the progression of Barrett's esophagus to adenocarcinoma. J Clin Oncol 22: 9529.
33. Dynek J.N., Vucic D. (2013) Antagonists of IAP proteins as cancer therapeutics. Cancer Lett 332: 206-14.
34. Cui X., Imaizumi T., Yoshida H., Tanji K., Matsumiya T., Satoh K. (2000) Lipopolysaccharide induces the expression of cellular inhibitor of apoptosis protein-2 in human macrophages. Biochem Biophys Acta 1524: 178-82.
35. Conte D., Holcik M., Lefebvre C.A., Lacasse E., Picketts D.J., Wright K.E., Korneluk R.G. (2006) Inhibitor of apoptosis protein cIAP2 is essential for lipopolysaccharide-induced macrophage survival. Mol Cell Biol 26: 699-708.
36. Friboulet L., Gourzones C., Tsao S.W., Morel Y., Paturel C., Témam S., Uzan C., Busson P. (2010) Poly(I:C) induces intense expression of c-IAP2 and cooperates with an IAP inhibitor in induction of apoptosis in cancer cells. BMC Cancer 10: 327.
37. Zhang L., Pelech S., Uitto V.J. (2004) Bacterial GroEL-like heat shock protein 60 protects epithelial cells from stress-induced death through activation of ERK and inhibition of caspase-3. Exp Cell Res 292: 231-40.
38. Weatherhead S.C., Farr P.M., Jamieson D., Hallinan J.S., Lloyd J.J., Wipat A., Reynolds N.J. (2011) Keratinocyte apoptosis in epidermal remodeling and clearance of psoriasis induced by UV radiation. J Invest Dermatol 131: 1916-2.
39. Luanpitpong S., Nimmannit U., Chanvorachote P., Leonard S.S., Pongrakhananon V., Wang L., Rojanasakul Y. (2011) Hydroxyl radical mediates cisplatin-induced apoptosis in human hair follicle dermal papilla cells and keratinocytes through Bcl-2-dependent mechanism. Apoptosis 16: 769-82.
40. Friboulet L., Pioche-Durieu C., Rodriguez S., Valent A., Souquère S., Ripoche H., Khabir A., Tsao S.W., Bosq J., Lo K.W., Busson P. (2008) Recurrent overexpression of c-IAP2 in EBV-associated nasopharyngeal carcinomas: critical role in resistance to Toll-like receptor 3-mediated apoptosis. Neoplasia 10: 1183-94.
41. Yuan Z., Syrkin G., Adem A., Geha R., Pastoriza J., Vrikshajanani C., Smith T., Quinn T.J., Alemu G., Cho H., Barrett C.J., Arap W., Pasqualini R., Libutti S.K. (2013) Blockade of inhibitors of apoptosis (IAPs) in combination with tumor-targeted delivery of tumor necrosis factor-α leads to synergistic antitumor activity. Cancer Gene Ther 20: 46-5.