Upregulation of phosphorylated HSP27, PRDX2, GRP75, GRP78 and GRP94 in acquired middle ear cholesteatoma growth

International Journal of Molecular Sciences

Volumn 14, Issue 7, 2013, Pages 14439-14459

  Ho, Kuen Yao ^a,b   Yeh, Tai Sheng ^c   Huang, Han Hsiang ^c   Hung, Kuo Feng ^c   Chai, Chee Yin ^a,b   Chen, Wan Tzu ^a   Tsai, Shih Meng ^b   Chang, Ning Chia ^a   Chien, Chen Yu ^a   Wang, Hsun Mo ^d   Wu, Yu Jen ^c  

^a KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c MEIHO UNIVERSITY   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Cholesteatoma; Grp75; Grp78; Grp94; Hsp27; Prdx2

Indexed keywords

GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; HEAT SHOCK PROTEIN 27; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; PEROXIREDOXIN 2; RAS PROTEIN;

ADULT; AGED; ARTICLE; CELL PROLIFERATION; CHOLESTEATOMA; CLINICAL ARTICLE; CONTROLLED STUDY; EPITHELIUM; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; KERATINOCYTE; MALE; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TWO DIMENSIONAL ELECTROPHORESIS; UPREGULATION; WESTERN BLOTTING;

ADOLESCENT; ADULT; CHOLESTEATOMA, MIDDLE EAR; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; HEAT-SHOCK PROTEINS; HSP27 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MALE; MEMBRANE PROTEINS; MIDDLE AGED; PEROXIREDOXINS; PHOSPHORYLATION; SKIN; TANDEM MASS SPECTROMETRY; UP-REGULATION; YOUNG ADULT;

EID: 84880085898     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140714439     Document Type: Article

References (66)

1. Kuczkowski, J.; Sakowicz-Burkiewicz, M.; Izycka-Świeszewska, E.; Mikaszewski, B.; Pawelczyk, T. Expression of tumor necrosis factor-α, interleukin-1α, interleukin-6 and interleukin-10 in chronic otitis media with bone osteolysis. ORL J. Otorhinolaryngol. Relat. Spec. 2011, 73, 93-99.
2. Haruyam, T.; Furukawa, M.; Kusunoki, T.; Onoda, J.; Ikeda, K. Expression of IL-17 and its role in bone destruction in human middle ear cholesteatoma. ORL J. Otorhinolaryngol. Relat. Spec. 2010, 72, 325-331.
3. Kuczkowski, J.; Sakowicz-Burkiewicz, M.; Izycka-Świeszewska, E. Expression of the receptor activator for nuclear factor-κB ligand and osteoprotegerin in chronic otitis media. Am. J. Otolaryngol. 2010, 31, 404-409.
4. Juhn, S.K.; Jung, M.K.; Hoffman, M.D.; Drew, B.R.; Preciado, D.A.; Sausen, N.J.; Jung, T.T.; Kim, B.H.; Park, S.Y.; Lin, J. et al. The role of inflammatory mediators in the pathogenesis of otitis media and sequelae. Clin. Exp. Otorhinolaryngol. 2008, 1, 117-138.
5. Nason, R.; Jung, J.Y.; Chole, R.A. Lipopolysaccharide-induced osteoclastogenesis from mononuclear precursors: A mechanism for osteolysis in chronic otitis. J. Assoc. Res. Otolaryngol. 2009, 10, 151-160.
6. Hilton, C.W.; Ondrey, F.G.; Wuertz, B.R.; Levine, S.C. Interleukin-8 production in response to tumor necrosis factor-alpha by cholesteatoma keratinocytes in cell culture. Laryngoscope 2011, 121, 372-374.
7. Helgaland, T.; Engelen, B.; Olsnes, C.; Aarstad, H.J.; Vassbotn, F.S. In vitro cholesteatoma growth and secretion of cytokines. Acta Otolaryngol. 2010, 130, 815-819.
8. Greenberg, J.S.; Manolidis, S. High incidence of complications encountered in chronic otitis media surgery in a U.S. metropolitan public hospital. Otolaryngol. Head Neck Surg. 2001, 125, 623-627.
9. Bagger-Sjoback, D.; Phelps, P.D. Cholesteatoma with extension to the cochlea. Am. J. Otol. 1985, 6, 338-343.
10. Chi, H.P.; Ho, K.Y.; Chai, C.Y.; Ta, C.F.; Wang, L.F.; Lee, K.W.; Kuo, W.R.; Wu, S.C.; Tsai, S.M. Epidermal growth factor expression in middle ear cholesteatoma. Kaohsiung J. Med. Sci. 2004, 20, 6-11.
11. Raynov, A.M.; Choung, Y.H.; Park, H.Y.; Choi, S.J.; Park, K. Establishment and characterization of an in vitro model for cholesteatoma. Clin. Exp. Otorhinolaryngol. 2008, 1, 86-91.
12. Marenda, S.A.; Aufdemorte, T.B. Localization of cytokines in cholesteatoma tissue. Otolaryngol. Head Neck Surg. 1995, 112, 359-368.
13. Yoshikawa, M.; Kojima, H.; Wada, K.; Tsukidate, T.; Okada, N.; Saito, H.; Moriyama, H. Identification of specific gene expression profiles in fibroblasts derived from middle ear cholesteatoma. Arch. Otolaryngol. Head Neck Surg. 2006, 132, 734-742.
14. Raffa, S.; Leone, L.; Scrofani, C.; Monini, S.; Torrisi, M.R.; Barbara, M. Cholesteatoma-associated fibroblasts modulate epithelial growth and differentiation through KGF/FGF7 secretion. Histochem. Cell. Biol. 2012, 138, 251-269.
15. Yamamoto-Fukuda, T.; Aoki, D.; Hishikawa, Y.; Kobayashi, T.; Takahashi, H.; Koji, T. Possible involvement of keratinocyte growth factor and its receptor in enhanced epithelial-cell proliferation and acquired recurrence of middle-ear cholesteatoma. Lab. Invest. 2003, 83, 123-136.
16. Huisman, M.A.; De Heer, E.; Grote, J.J. Survival signaling and terminal differentiation in cholesteatoma epithelium. Acta OtoLaryngol. 2007, 127, 424-429.
17. Liu, C.I.; Chen, C.C.; Chen, J.C.; Su, J.H.; Huang, H.H.; Chen, J.Y.; Wu, Y.J. Proteomic analysis of anti-tumor effects of 11-dehydrosinulariolide on CAL-27 cells. Mar. Drugs 2011, 9, 1254-1272.
18. Su, T.R.; Lin, J.J.; Chiu, C.C.; Chen, J.Y.F.; Su, J.H.; Cheng, Z.J.; Hwang, W.I.; Huang, H.H.; Wu, Y.J. Proteomic investigation of anti-tumor activities exerted by sinularin against A2058 melanoma cells. Electrophoresis 2012, 33, 1139-1152.
19. Kim, J.L.; Jung, H.H. Proteomic analysis of cholesteatoma. Acta OtoLaryngol. 2004, 124, 783-788.
20. Shieh, T.J.; Ho, K.Y.; Kuo, W.R.; Chai, C.Y.; Lin, C.S.; Juan, K.H. Evaluation of proliferative activity in middle ear cholesteatoma using proliferating cell nuclear antigen. Kaohsiung J. Med. Sci 1999, 15, 468-474.
21. Yasuda, E.; Kumada, T.; Takai, S.; Ishisaki, A.; Noda, T.; Matsushima-Nishiwaki, R.; Yoshimi, N.; Kato, K.; Toyoda, H.; Kaneoka, Y. et al. Attenuated phosphorylation of heat shock protein 27 correlates with tumor progression in patients with hepatocellular carcinoma. Biochem. Biophys. Res. Commun 2005, 337, 337-342.
22. Yuan, J.; Rozengurt, E. PKD, PKD2, and p38 MAPK mediate Hsp27 serine-82 phosphorylation induced by neurotensin in pancreatic cancer PANC-1 cells. J. Cell. Biochem. 2008, 103, 648-662.
23. Huisman, M.A.; De Heer, E.; Grote, J.J. Sustained extracellular signal-regulated kinase1/2 mitogen-activated protein kinase signalling is related to increased p21 expression in cholesteatoma epithelium. Acta Otolaryngol. 2005, 125, 134-140.
24. Tavaria, M.; Gabriele, T.; Kola, I.; Anderson, R.L. A hitchhiker's guide to the human Hsp70 family. Cell. Stress Chaperones 1996, 1, 23-28.
25. Morano, K.A. New tricks for an old dog: The evolving world of Hsp70. Ann. N. Y. Acad. Sci. 2007, 1113, 1-14.
26. Shinoda, H.; Huang, C.C. Heat shock proteins in middle ear cholesteatoma. Otolaryngol. Head Neck Surg. 1996, 114, 77-83.
27. Lee, A.S. The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 2005, 35, 373-381.
28. Lee, A.S. The glucose-regulated proteins: Stress induction and clinical applications. Trends Biochem. Sci. 2001, 26, 504-510.
29. Hughes, C.S.; Shen, J.W.; Subjeck, J.R. Resistance to etoposide induced by three glucose-regulated stresses in Chinese hamster ovary cells. Cancer Res. 1989, 49, 4452-4454.
30. Jamora, C.; Dennert, G.; Lee, A.S. Inhibition of tumor progression by suppression of stress protein GRP78/BiP induction in fibrosarcoma B/C10ME. Proc. Natl. Acad. Sci. USA 1996, 93, 7690-7694.
31. Song, M.S.; Park, Y.K.; Lee, J.H.; Park, K. Induction of Glucose-regulated Protein 78 by Chronic Hypoxia in Human Gastric Tumor Cells through a Protein Kinase C-ε/ERK/AP-1 Signaling Cascade. Cancer Res. 2001, 61, 8322-8330.
32. Voisine, C.; Craig, E.A.; Zufall, N.; von Ahsen, O.; Pfanner, N.; Voos, W. The protein import motor of mitochondria: Unfolding and trapping of preproteins are distinct and separable functions of matrix Hsp70. Cell 1999, 97, 565-574.
33. Ma, Z.; Izumi, H.; Kanai, M.; Kabuyama, Y.; Ahn, N.G.; Fukasawa, K. Mortalin controls centrosome duplication via modulating centrosomal localization of p53. Oncogene 2006, 25, 5377-5390.
34. Lim, J.H.; Martin, F.; Guiard, B.; Pfanner, N.; Voos, W. The mitochondrial Hsp70-dependent import system actively unfolds preproteins and shortens the lag phase of translocation. EMBO J. 2001, 20, 941-950.
35. Sacht, G.; Brigelius-Flohe, R.; Kiess, M.; Sztajer, H.; Flohe, L. ATP-sensitive association of mortalin with the IL-1 receptor type I. Biofactors 1999, 9, 49-60.
36. Takano, S.; Wadhwa, R.; Mitsui, Y.; Kaul, S.C. Identification and characterization of molecular interactions between glucose-regulated proteins (GRPs) mortalin/GRP75/peptide-binding protein 74 (PBP74) and GRP94. Biochem. J. 2001, 357, 393-398.
37. Wadhwa, R.; Yaguchi, T.; Hasan, M.K.; Taira, K.; Kaul, S.C. Mortalin-MPD (mevalonate pyrophosphate decarboxylase) interactions and their role in control of cellular proliferation. Biochem. Biophys. Res. Commun. 2003, 302, 735-742.
38. Mizukoshi, E.; Suzuki, M.; Misono, T.; Loupatov, A.; Munekata, E.; Kaul, S.C.; Wadhwa, R.; Imamura, T. Cell-cycle dependent tyrosine phosphorylation on mortalin regulates its interaction with fibroblast growth factor-1. Biochem. Biophys. Res. Commun. 2001, 280, 1203-1209.
39. Yaguchi, T.; Aida, S.; Kaul, S.C.; Wadhwa, R. Involvement of mortalin in cellular senescence from the perspective of its mitochondrial import, chaperone, and oxidative stress management functions. Ann. N. Y. Acad. Sci. 2007, 1100, 306-311.
40. Wadhwa, R.; Takano, S.; Taira, K.; Kaul, S.C. Reduction in mortalin level by its antisense expression causes senescence-like growth arrest in human immortalized cells. J. Gene Med. 2004, 6, 439-444.
41. Langer, R.; Feith, M.; Siewert, J.R.; Wester, H.J.; Hoefler, H. Expression and clinical significance of glucose regulated proteins GRP78 (BiP) and GRP94 (GP96) in human adenocarcinomas of the esophagus. BMC Cancer 2008, 8, doi:10.1186/1471-2407-8-70.
42. Zheng, H.C.; Takahashi, H.; Li, X.H.; Hara, T.; Masuda, S.; Guan, Y.F.; Takano, Y. Overexpression of GRP78 and GRP94 are markers for aggressive behavior and poor prognosis in gastric carcinomas. Hum. Pathol. 2008, 39, 1042-1049.
43. Fu, Y.; Lee, A.S. Glucose regulated proteins in cancer progression, drug resistance and immunotherapy. Cancer Biol. Ther. 2006, 5, 741-744.
44. Kubota, K.; Lee, D.H.; Tsuchiya, M.; Young, C.S.; Everett, E.T.; Martinez-Mier, E.A.; Snead, M.L.; Nguyen, L.; Urano, F.; Bartlett, J.D. Fluoride induces endoplasmic reticulum stress in ameloblasts responsible for dental enamel formation. J. Biol. Chem. 2005, 280, 23194-23202.
45. Garrido, C.; Brunet, M.; Didelot, C.; Zermati, Y.; Schmitt, E.; Kroemer, G. Heat shock proteins 27 and 70: Anti-apoptotic proteins with tumorigenic properties. Cell. Cycle 2006, 5, 2592-2601.
46. Bruey, J.M.; Paul, C.; Fromentin, A.; Hilpert, S.; Arrigo, A.P.; Solary, E.; Garrido, C. Differential regulation of HSP27 oligomerization in tumor cells grown in vitro and in vivo. Oncogene 2000, 19, 4855-4863.
47. Wang, A.; Liu, X.; Sheng, S.; Ye, H.; Peng, T.; Shi, F.; Crowe, D.L.; Zhou, X. Dysregulation of heat shock protein 27 expression in oral tongue squamous cell carcinoma. BMC Cancer 2009, 9, doi:10.1186/1471-2407-9-167.
48. Xu, L.; Chen, S.; Bergan, R.C. MAPKAPK2 and HSP27 are downstream effectors of p38 MAP kinase-mediated matrix metalloproteinase type 2 activation and cell invasion in human prostate cancer. Oncogene 2006, 25, 2987-2998.
49. Kostenko, S.; Moens, U. Heat shock protein 27 phosphorylation: Kinases, phosphatases, functions and pathology. Cell. Mol. Life Sci. 2009, 66, 3289-3307.
50. Gibbs, S.; Silva Pinto, A.N.; Murli, S.; Huber, M.; Hohl, D.; Ponec, M. Epidermal growth factor and keratinocyte growth factor differentially regulate epidermal migration, growth, and differentiation. Wound Repair Regen. 2000, 8, 192-203.
51. Shirakata, Y. Regulation of epidermal keratinocytes by growth factors. J. Dermatol. Sci. 2010, 59, 73-80.
52. Niwa, M.; Hotta, K.; Hara, A.; Hirade, K.; Ito, H.; Kato, K.; Kozawa, O. TNF-α decreases hsp 27 in human blood mononuclear cells: Involvement of protein kinase c. Life Sci. 2006, 80, 181-186.
53. Sudhoff, H.; Dazert, S.; Gonzales, A.M.; Borkowski, G.; Park, S.Y.; Baird, A.; Hildmann, H.; Ryan, A.F. Angiogenesis and angiogenic growth factors in middle ear cholesteatoma. Otol. Neurotol. 2000, 21, 793-798.
54. Evans, I.M.; Britton, G.; Zachary, I.C. Vascular endothelial growth factor induces heat shock protein (HSP) 27 serine 82 phosphorylation and endothelial tubulogenesis via protein kinase D and independent of p38 kinase. Cell Signal. 2008, 20, 1375-1384.
55. Schluter, H.; Apweiler, R.; Holzhutter, H.G.; Jungblut, P.R. Finding one's way in proteomics: A protein species nomenclature. Chem. Cent. J. 2009, 3, doi:10.1186/1752-153X-3-11.
56. Huang, C.C.; Chen, C.T.; Huang, T.S.; Shinoda, H. Mediation of signal transduction in keratinocytes of human middle ear cholesteatoma by ras protein. Eur. Arch. Otorhinolaryngol. 1996, 253, 385-389.
57. Wong, J.W.; Shi, B.; Farboud, B.; McClaren, M.; Shibamoto, T.; Cross, C.E.; Isseroff, R.R. Ultraviolet B-mediated phosphorylation of the small heat shock protein HSP27 in human keratinocytes. J. Investig. Dermatol. 2000, 115, 427-434.
58. Robitaille, H.; Simard-Bisson, C.; Larouche, D.; Tanguay, R.M.; Blouin, R.; Germain, L. The small heat-shock protein Hsp27 undergoes ERK-dependent phosphorylation and redistribution to the cytoskeleton in response to dual leucine zipper-bearing kinase expression. J. Invest. Dermatol. 2010, 130, 74-85.
59. Mitev, V.; Miteva, L. Signal transduction in keratinocytes. Exp. Dermatol. 1999, 8, 96-108.
60. Rozengurt, E. Protein kinase D signaling: Multiple biological functions in health and disease. Physiology (Bethesda) 2011, 26, 23-33.
61. Valyi-Nagy, I.; Jensen, P.J.; Albelda, S.M.; Rodeck, U. Cytokine-induced expression of transforming growth factor-alpha and the epidermal growth factor receptor in neonatal skin explants. J. Invest. Dermatol. 1992, 99, 350-356.
62. Saunders, N.A.; Jetten, A.M. Control of growth regulatory and differentiation-specific genes in human epidermal keratinocytes by interferon gamma. Antagonism by retinoic acid and transforming growth factor beta 1. J. Biol. Chem. 1994, 269, 2016-2022.
63. Yun, S.J.; Seo, J.J.; Chae, J.Y.; Lee, S.C. Peroxiredoxin I and II are up-regulated during differentiation of epidermal keratinocytes. Arch. Dermatol. Res. 2005, 296, 555-559.
64. Myers, E.N.; Park, K.; Chun, Y.; Lee, D.; Hwang, S. Signal transduction pathway in human middle ear cholesteatoma. Otolaryngol. Head Neck Surg. 1999, 120, 899-904.
65. Ryu, J.; Park, S.G.; Park, B.C.; Choe, M.; Lee, K.S.; Cho, J.W. Proteomic analysis of psoriatic skin tissue for identification of differentially expressed proteins: Up-regulation of GSTP1, SFN and PRDX2 in psoriatic skin. Int. J. Mol. Med. 2011, 28, 785-792.
66. Wu, Y.J.; Chen, H.M.; Wu, T.T.; Wu, J.S.; Chu, R.M.; Juang, R.H. Preparation of monoclonal antibody bank against whole water-soluble proteins from rapid-growing bamboo shoots. Proteomics 2006, 6, 5898-5902.