Introduction of an N-terminal peptide of S100C/A11 into human cells induces apoptotic cell death

Journal of Molecular Medicine

Volumn 82, Issue 9, 2004, Pages 612-620

  Makino, Eiichi ^a,b   Sakaguchi, Masakiyo ^b   Iwatsuki, Keiji ^b   Huh, Nam Ho ^b  

^a KAWASAKI MEDICAL SCHOOL   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

Author keywords

Apoptosis; Human cancer; P21 WAF1 CIP1; Peptide; S100C A11

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; CALCIUM BINDING PROTEIN; CASPASE; PROTEIN P21; PROTEIN S 100; PROTEIN S100C; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; CELL DEATH; CELL KILLING; CYTOTOXICITY; DNA SYNTHESIS INHIBITION; ENZYME ACTIVITY; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; KERATINIZATION; PEPTIDE ANALYSIS; PROTEIN DOMAIN; PROTEIN FAMILY; PULSED FIELD GEL ELECTROPHORESIS; TISSUE SPECIFICITY;

AMINO ACID SEQUENCE; APOPTOSIS; CARCINOMA; CARCINOMA, SQUAMOUS CELL; CELL CYCLE PROTEINS; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA REPLICATION; DRUG DESIGN; GENE EXPRESSION REGULATION; GENE PRODUCTS, TAT; HUMANS; MELANOMA; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; S100 PROTEINS;

EID: 4744355870     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-004-0560-1     Document Type: Article

References (47)

1. Heizmann CW, Fritz G, Schafer BW (2002) S100 proteins: structure, functions and pathology. Front Biosci 7:d1356-d1368
2. Donato R (1999) Functional roles of S100 proteins, calcium-binding proteins of the EF-hand type. Biochim Biophys Acta 1450:191-231
3. Makino T, Takaishi M, Morohashi M, Huh NH (2001) Hornerin, a novel profilaggrin-like protein and differentiation-specific marker isolated from mouse skin. J Biol Chem 276:47445-47452
4. Ilg EC, Schafer BW, Heizmann CW (1996) Expression pattern of S100 calcium-binding proteins in human tumors. Int J Cancer 68:325-332
5. Maelandsmo GM, Florenes VA, Mellingsaeter T, Hovig E, Kerbel RS, Fodstad O (1997) Differential expression patterns of S100A2, S100A4 and S100A6 during progression of human malignant melanoma. Int J Cancer 74:464-469
6. Nagy N, Brenner C, Markadieu N, Chaboteaux C, Camby I, Schafer BW, Pochet R, Heizmann CW, Salmon I, Kiss R, Decaestecker C (2001) S100A2, a putative tumor suppressor gene, regulates in vitro squamous cell carcinoma migration. Lab Invest 81:599-612
7. Komatsu K, Murata K, Kameyama M, Ayaki M, Mukai M, Ishiguro S, Miyoshi J, Tatsuta M, Inoue M, Nakamura H (2002) Expression of S100A6 and S100A4 in matched samples of human colorectal mucosa, primary colorectal adenocarcinomas and liver metastases. Oncology 63:192-200
8. El-Rifai W, Moskaluk CA, Abdrabbo MK, Harper J, Yoshida C, Riggins GJ, Frierson HF Jr, Powell SM (2002) Gastric cancers overexpress S100A calcium-binding proteins. Cancer Res 62:6823-6826
9. Hernan R, Fasheh R, Calabrese C, Frank AJ, Maclean KH, Allard D, Barraclough R, Gilbertson RJ (2003) ERBB2 up-regulates S100A4 and several other prometastatic genes in medulloblastoma. Cancer Res 63:140-148
10. Sherbet GV, Lakshmi MS (1998) S100A4 (MTS1) calcium binding protein in cancer growth, invasion and metastasis. Anticancer Res 18:2415-2421
11. Lloyd BH, Platt-Higgins A, Rudland PS, Barraclough R (1998) Human S100A4 (p9Ka) induces the metastatic phenotype upon benign tumour cells. Oncogene 17:465-473
12. Bjornland K, Winberg JO, Odegaard OT, Hovig E, Loennechen T, Aasen AO, Fodstad O, Maelandsmo GM (1999) S100A4 involvement in metastasis: deregulation of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases in osteosarcoma cells transfected with an anti-S100A4 ribozyme. Cancer Res 59:4702-4708
13. Takenaga K, Nakamura Y, Sakiyama S (1997) Expression of antisense RNA to S100A4 gene encoding an S100-related calcium-binding protein suppresses metastatic potential of high-metastatic Lewis lung carcinoma cells. Oncogene 14:331-337
14. Ambartsumian N, Klingelhofer J, Grigorian M, Christensen C, Kriajevska M, Tulchinsky E, Georgiev G, Berezin V, Bock E, Rygaard J, Cao R, Cao Y, Lukanidin E (2001) The metastasis-associated Mtsl (S100A4) protein could act as an angiogenic factor. Oncogene 20:4685-4695
15. Boni R, Heizmann CW, Doguoglu A, Ilg EC, Schafer BW, Dummer R, Burg G (1997) Ca (2+)-binding proteins S100A6 and S100B in primary cutaneous melanoma. J Cutan Pathol 24:76-80
16. Hauschild A, Engel G, Brenner W, Glaser R, Monig H, Henze E, Christophers E (1999) S100B protein detection in serum is a significant prognostic factor in metastatic melanoma. Oncology 56:338-344
17. Millward TA, Heizmann CW, Schafer BW, Hemmings BA (1998) Calcium regulation of Ndr protein kinase mediated by S100 calcium-binding proteins. EMBO J 17:5913-5922
18. Liu D, Rudland PS, Sibson DR, Platt-Higgins A, Barraclough R (2000) Expression of calcium-binding protein S100A2 in breast lesions. Br J Cancer 83:1473-1479
19. Feng G, Xu X, Youssef EM, Lotan R (2001) Diminished expression of S100A2, a putative tumor suppressor, at early stage of human lung carcinogenesis. Cancer Res 61:7999-8004
20. Boni R, Burg G, Doguoglu A, Ilg EC, Schafer BW, Muller B, Heizmann CW (1997) Immunohistochemical localization of the Ca2+ binding S100 proteins in normal human skin and melanocytic lesions. Br J Dermatol 137:39-43
21. Todoroki H, Kobayashi R, Watanabe M, Minami H, Hidaka H (1991) 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 266:18668-18673
22. Sakaguchi M, Miyazaki M, Inoue Y, Tsuji T, Kouchi H, Tanaka T, Yamada H, Namba M (2000) Relationship between contact inhibition and intranuclear S100C of normal human fibroblasts. J Cell Biol 149:1193-1206
23. Mailliard WS, Haigler HT, Schlaepfer DD (1996) Calcium-dependent binding of S100C to the N-terminal domain of annexin I. J Biol Chem 271:719-725
24. Sakaguchi M, Miyazaki M, Takaishi M, Sakaguchi Y, Makino E, Kataoka N, Yamada H, Namba M, Huh NH (2003) S100C/ All is a key mediator of Ca2+-induced growth inhibition of human epidermal keratinocytes. J Cell Biol 163:825-835
25. Gartel AL, Serfas MS, Tyner AL (1996) p21-negative regulator of the cell cycle. Proc Soc Exp Biol Med 213:138-149
26. Schwartz GK (2002) CDK inhibitors: cell cycle arrest versus apoptosis. Cell Cycle 1:122-123
27. Han Z, Wei W, Dunaway S, Darnowski JW, Calabresi P, Sedivy J, Hendrickson EA, Balan KV, Pantazis P, Wyche JH (2002) Role of p21 in apoptosis and senescence of human colon cancer cells treated with camptothecin. J Biol Chem 277:17154-17160
28. Detjen KM, Murphy D, Welzel M, Farwig K, Wiedenmann B, Rosewicz S (2003) Downregulation of p21 (waf/cip-1) mediates apoptosis of human hepatocellular carcinoma cells in response to interferon-gamma. Exp Cell Res 282:78-89
29. Kwon YH, Jovanovic A, Serfas MS, Tyner AL (2003) The Cdk inhibitor p21 is required for necrosis but it inhibits apoptosis following toxin-induced liver injury. J Biol Chem (epub ahead of print)
30. Waldman T, Lengauer C, Kinzler KW, Vogelstein B (1996) Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature 381:713-716
31. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, Fusenig NE (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J Cell Biol 106:761-771
32. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285:1569-1572
33. van Engeland M, Nieland LJ, Ramaekers FC, Schutte B, Reutelingsperger CP (1998) Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31:1-9
34. St John LS, Sauter ER, Herlyn M, Litwin S, Adler-Storthz K (2000) Endogenous p53 gene status predicts the response of human squamous cell carcinomas to wild-type p53. Cancer Gene Ther 7:749-756
35. Katsuda K, Kataoka M, Uno F, Murakami T, Kondo T, Roth JA, Tanaka N, Fujiwara T (2002) Activation of caspase-3 and cleavage of Rb are associated with p16-mediated apoptosis in human non-small cell lung cancer cells. Oncogene 21:2108-2113
36. Janicke RU, Sprengart ML, Wati MR, Porter AG (1998) Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273:9357-9360
37. Ruemmele FM, Dionne S, Qureshi I, Sarma DS, Levy E, Seidman EG (1999) Butyrate mediates Caco-2 cell apoptosis via up-regulation of pro-apoptotic BAK and inducing caspase-3 mediated cleavage of poly-(ADP-ribose) polymerase (PARP). Cell Death Differ 6:729-735
38. Cande C, Cohen I, Daugas E, Ravagnan L, Larochette N, Zamzami N, Kroemer G (2002) Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria. Biochimie 84:215-222
39. Larochette N, Decaudin D, Jacotot E, Brenner C, Marzo I, Susin SA, Zamzami N, Xie Z, Reed J, Kroemer G (1999) Arsenite induces apoptosis via a direct effect on the mitochondrial permeability transition pore. Exp Cell Res 249:413-421
40. Fonfria E, Dare E, Benelli M, Sunol C, Ceccatelli S (2002) Translocation of apoptosis-inducing factor in cerebellar granule cells exposed to neurotoxic agents inducing oxidative stress. Eur J Neurosci 16:2013-2016
41. Mittelman JM, Gudkov AV (1999) Generation of p53 suppressor peptide from the fragment of p53 protein. Somat Cell Mol Genet 25:115-128
42. Kanovsky M, Raffo A, Drew L, Rosal R, Do T, Friedman FK, Rubinstein P, Visser J, Robinson R, Brandt-Rauf PW, Michl J, Fine RL, Pincus MR (2001) Peptides from the amino terminal mdm-2-binding domain of p53, designed from conformational analysis, are selectively cytotoxic to transformed cells. Proc Natl Acad Sci U S A 98:12438-12443
43. Do TN, Rosal RV, Drew L, Raffo AJ, Michl J, Pincus MR, Friedman FK, Petrylak DP, Cassai N, Szmulewicz J, Sidhu G, Fine RL, Brandt-Rauf PW (2003) Preferential induction of necrosis in human breast cancer cells by a p53 peptide derived from the MDM 2 binding site. Oncogene 22:1431-1444
44. Li Y, Rosal RV, Brandt-Rauf PW, Fine RL (2002) Correlation between hydrophobic properties and efficiency of carrier-mediated membrane transduction and apoptosis of a p53 C-terminal peptide. Biochem Biophys Res Commun 298:439-449
45. Giorello L, Clerico L, Pescarolo MP, Vikhanskaya F, Salmona M, Colella G, Bruno S, Mancuso T, Bagnasco L, Russo P, Parodi S (1998) Inhibition of cancer cell growth and c-Myc transcriptional activity by a c-Myc helix 1-type peptide fused to an internalization sequence. Cancer Res 58:3654-3659
46. Poulaki V, Mitsiades CS, Joussen AM, Lappas A, Kirchhof B, Mitsiades N (2002) Constitutive nuclear factor-kappaB activity is crucial for human retinoblastoma cell viability. Am J Pathol 161:2229-2240
47. Thomas RP, Farrow BJ, Kim S, May MJ, Hellmich MR, Evers BM (2002) Selective targeting of the nuclear factor-kappaB pathway enhances tumor necrosis factor-related apoptosis-inducing ligand-mediated pancreatic cancer cell death. Surgery 132:127-134