Home LiteratureArticle Details
PMID: 19293795 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Extracellular, cell-permeable survivin inhibits apoptosis while promoting proliferative and metastatic potential.

British journal of cancer ·Vol. 100 ·No. 7 ·2009-04-07 ·Pages 1073-86

Khan S, Aspe JR, Asumen MG, Almaguel F, Odumosu O, Acevedo-Martinez S, De Leon M, Langridge WH, Wall NR

Abstract

The tumour microenvironment is believed to be involved in development, growth, metastasis, and therapy resistance of many cancers. Here we show survivin, a member of the inhibitor of apoptosis protein (IAP) family, implicated in apoptosis inhibition and the regulation of mitosis in cancer cells, exists in a novel extracellular pool in tumour cells. Furthermore, we have constructed stable cell lines that provide the extracellular pool with either wild-type survivin (Surv-WT) or the previously described dominant-negative mutant survivin (Surv-T34A), which has proven pro-apoptotic effects in cancer cells but not in normal proliferating cells. Cancer cells grown in conditioned medium (CM) taken from Surv-WT cells absorbed survivin and experienced enhanced protection against genotoxic stresses. These cells also exhibited an increased replicative and metastatic potential, suggesting that survivin in the tumour microenvironment may be directly associated with malignant progression, further supporting survivin's function in tumourigenesis. Alternatively, cancer cells grown in CM taken from the Surv-T34A cells began to apoptose through a caspase-2- and caspase-9-dependent pathway that was further enhanced by the addition of other chemo- and radiotherapeutic modalities. Together our findings suggest a novel microenvironmental function for survivin in the control of cancer aggressiveness and spread, and should result in the genesis of additional cancer treatment modalities.

MeSH Terms
Apoptosis Cell Cycle Cell Line, Tumor Cell Proliferation Humans Inhibitor of Apoptosis Proteins Membrane Potential, Mitochondrial Microtubule-Associated Proteins/analysis,physiology Neoplasm Invasiveness Neoplasm Metastasis Neoplasms/pathology Survivin
Chemicals
BIRC5 protein, human Inhibitor of Apoptosis Proteins Microtubule-Associated Proteins Survivin
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Khan S
Division of Biochemistry and Microbiology, Department of Basic Sciences, Center for Health Disparities Research and Molecular Medicine, Loma Linda University, Loma Linda, CA 92350, USA.
Aspe J R
Asumen M G
Almaguel F
Odumosu O
Acevedo-Martinez S
De Leon M
Langridge W H R
Wall N R
References (43)
43 references, click to expand
  1. Coordinated histone modifications mediated by a CtBP co-repressor complex.
    Nature. 2003 Apr 17;422(6933):735-8 PMID: 12700765
  2. The universal character of the tumor-associated antigen survivin.
    Clin Cancer Res. 2007 Oct 15;13(20):5991-4 PMID: 17947459
  3. Bacterial and plant enterotoxin B subunit-autoantigen fusion proteins suppress diabetes insulitis.
    Mol Biotechnol. 2006 Jan;32(1):1-15 PMID: 16382177
  4. Expression of survivin in normal, hyperplastic, and neoplastic colonic mucosa.
    Hum Pathol. 2001 Jan;32(1):119-25 PMID: 11172305
  5. Survivin, a cancer target with an emerging role in normal adult tissues.
    Mol Cancer Ther. 2006 May;5(5):1087-98 PMID: 16731740
  6. Intracellular and surface distribution of monocyte tissue factor: application to intersubject variability.
    Arterioscler Thromb Vasc Biol. 2005 Jul;25(7):1493-8 PMID: 15860742
  7. Cancer gene therapy using a survivin mutant adenovirus.
    J Clin Invest. 2001 Oct;108(7):981-90 PMID: 11581299
  8. Capitalizing on the immunogenicity of dying tumor cells.
    Clin Cancer Res. 2008 Mar 15;14(6):1603-8 PMID: 18347160
  9. Balance between survivin, a key member of the apoptosis inhibitor family, and its specific antibodies determines erosivity in rheumatoid arthritis.
    Arthritis Res Ther. 2005;7(2):R349-58 PMID: 15743483
  10. Regulation of apoptosis at cell division by p34cdc2 phosphorylation of survivin.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13103-7 PMID: 11069302
  11. Inhibition of melanoma tumor growth in vivo by survivin targeting.
    Proc Natl Acad Sci U S A. 2001 Jan 16;98(2):635-40 PMID: 11149963
  12. Developmentally regulated expression of the novel cancer anti-apoptosis gene survivin in human and mouse differentiation.
    Am J Pathol. 1998 Jan;152(1):43-9 PMID: 9422522
  13. Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells.
    J Cell Biol. 1990 Apr;110(4):1427-38 PMID: 2324200
  14. Radiation-induced apoptosis of tumor cells is facilitated by inhibition of the interaction between Survivin and Smac/DIABLO.
    Cancer Lett. 2008 Jan 18;259(1):71-81 PMID: 17967504
  15. IAP family proteins--suppressors of apoptosis.
    Genes Dev. 1999 Feb 1;13(3):239-52 PMID: 9990849
  16. Preparation and characterization of monoclonal antibodies recognizing three distinct differentiation antigens (BL1, BL2, BL3) on human B lymphocytes.
    J Immunol. 1984 Aug;133(2):684-91 PMID: 6429242
  17. Control of apoptosis and mitotic spindle checkpoint by survivin.
    Nature. 1998 Dec 10;396(6711):580-4 PMID: 9859993
  18. JC-1, but not DiOC6(3) or rhodamine 123, is a reliable fluorescent probe to assess delta psi changes in intact cells: implications for studies on mitochondrial functionality during apoptosis.
    FEBS Lett. 1997 Jul 7;411(1):77-82 PMID: 9247146
  19. Mitochondrial survivin inhibits apoptosis and promotes tumorigenesis.
    J Clin Invest. 2004 Oct;114(8):1117-27 PMID: 15489959
  20. Cholera toxin entry into pig enterocytes occurs via a lipid raft- and clathrin-dependent mechanism.
    Biochemistry. 2005 Jan 25;44(3):873-82 PMID: 15654743
  21. Survivin exists in immunochemically distinct subcellular pools and is involved in spindle microtubule function.
    J Cell Sci. 2002 Feb 1;115(Pt 3):575-85 PMID: 11861764
  22. Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells: implications for microbial attachment and oral vaccine targeting.
    J Exp Med. 1996 Sep 1;184(3):1045-59 PMID: 9064322
  23. A functional comparison of CD34 + CD38- cells in cord blood and bone marrow.
    Blood. 1995 Nov 15;86(10):3745-53 PMID: 7579341
  24. Pleiotropic cell-division defects and apoptosis induced by interference with survivin function.
    Nat Cell Biol. 1999 Dec;1(8):461-6 PMID: 10587640
  25. Extracellular survivin up-regulates adhesion molecules on the surface of leukocytes changing their reactivity pattern.
    J Leukoc Biol. 2008 Jan;83(1):149-55 PMID: 17938276
  26. Suppression of survivin phosphorylation on Thr34 by flavopiridol enhances tumor cell apoptosis.
    Cancer Res. 2003 Jan 1;63(1):230-5 PMID: 12517802
  27. A novel antisense oligonucleotide targeting survivin expression induces apoptosis and sensitizes lung cancer cells to chemotherapy.
    Cancer Res. 2000 Jun 1;60(11):2805-9 PMID: 10850418
  28. Stimulation of the transepithelial flux of influenza HA vaccine by cholera toxin B subunit.
    Vaccine. 1992;10(2):101-6 PMID: 1539462
  29. Selective modulation of the endocytic uptake of ricin and fluid phase markers without alteration in transferrin endocytosis.
    J Biol Chem. 1990 Apr 15;265(11):6382-8 PMID: 1969411
  30. Spontaneous cytotoxic T-cell responses against survivin-derived MHC class I-restricted T-cell epitopes in situ as well as ex vivo in cancer patients.
    Cancer Res. 2001 Aug 15;61(16):5964-8 PMID: 11507035
  31. Drug resistance and the solid tumor microenvironment.
    J Natl Cancer Inst. 2007 Oct 3;99(19):1441-54 PMID: 17895480
  32. Survivin, versatile modulation of cell division and apoptosis in cancer.
    Oncogene. 2003 Nov 24;22(53):8581-9 PMID: 14634620
  33. The war on cancer.
    Lancet. 1996 May 18;347(9012):1377-81 PMID: 8637346
  34. Stromal reaction in cancer tissue: pathophysiologic significance of the expression of matrix-degrading enzymes in relation to matrix turnover and immune/inflammatory reactions.
    Pathol Int. 1998 Jan;48(1):1-9 PMID: 9589457
  35. The hallmarks of cancer.
    Cell. 2000 Jan 7;100(1):57-70 PMID: 10647931
  36. A complex with chromatin modifiers that occupies E2F- and Myc-responsive genes in G0 cells.
    Science. 2002 May 10;296(5570):1132-6 PMID: 12004135
  37. Baicalein induces cancer cell death and proliferation retardation by the inhibition of CDC2 kinase and survivin associated with opposite role of p38 mitogen-activated protein kinase and AKT.
    Mol Cancer Ther. 2007 Nov;6(11):3039-48 PMID: 18025287
  38. Rational design of shepherdin, a novel anticancer agent.
    Cancer Cell. 2005 May;7(5):457-68 PMID: 15894266
  39. Effects of survivin antagonists on growth of established tumors and B7-1 immunogene therapy.
    J Natl Cancer Inst. 2001 Oct 17;93(20):1541-52 PMID: 11604477
  40. The case for survivin as a regulator of microtubule dynamics and cell-death decisions.
    Curr Opin Cell Biol. 2006 Dec;18(6):609-15 PMID: 16934447
  41. A p34(cdc2) survival checkpoint in cancer.
    Cancer Cell. 2002 Jul;2(1):43-54 PMID: 12150824
  42. Survivin study: what is the next wave?
    J Cell Physiol. 2003 Oct;197(1):8-29 PMID: 12942537
  43. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma.
    Nat Med. 1997 Aug;3(8):917-21 PMID: 9256286
Article Info
Journal
British journal of cancer
Abbr.
Br J Cancer
ISSN
1532-1827
Published
2009-04-07
Epub
2009-00-17
Pages
1073-86
Language
English
Region
England
NLM ID
0370635
PMCID
PMC2669990
Subset
IM
Grants
NIMHD NIH HHS · P20 MD001632 · United States
NIMHD NIH HHS · P20 MD006988 · United States
NIMHD NIH HHS · 5 P20 MD 001632 · United States
NIGMS NIH HHS · R25 GM060507-01A1 · United States
NIGMS NIH HHS · R25 GM060507 · United States
NIMHD NIH HHS · P20 MD001632-010003 · United States
NIMHD NIH HHS · P20 MD001632-03 · United States
NIGMS NIH HHS · R25 GM060507-02 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com