Clinical significance and novel mechanism of action of kallikrein 6 in glioblastoma

Neuro-Oncology

Volumn 15, Issue 3, 2013, Pages 305-318

  Drucker, Kristen L ^a   Paulsen, Alex R ^a   Giannini, Caterina ^a   Decker, Paul A ^a   Blaber, Sachiko I ^b   Blaber, Michael ^b   Uhm, Joon H ^a   O'Neill, Brian P ^a   Jenkins, Robert B ^a   Scarisbrick, Isobel A ^a  

^a MAYO CLINIC   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

Author keywords

apoptosis; glioma; grade IV; malignancy; temozolomide

Indexed keywords

CISPLATIN; KALLIKREIN 6; PROTEINASE ACTIVATED RECEPTOR 1; RECOMBINANT ENZYME; RECOMBINANT KALLIKREIN 6; RNA; STAUROSPORINE; TEMOZOLOMIDE; THROMBIN RECEPTOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; ASTROCYTOMA CELL; CANCER CHEMOTHERAPY; CANCER GRADING; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER RESISTANCE; CANCER SURVIVAL; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENDER; GLIOBLASTOMA; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; IN VITRO STUDY; MULTIMODALITY CANCER THERAPY; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SCORING SYSTEM;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL PROLIFERATION; CISPLATIN; ENZYME INHIBITORS; GLIOBLASTOMA; HUMANS; KALLIKREINS; NEOPLASM GRADING; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STAUROSPORINE; SURVIVAL RATE; TUMOR CELLS, CULTURED;

EID: 84874520373     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nos313     Document Type: Article

References (62)

1. Adamson C, Kanu OO, Mehta AI, et al. Glioblastoma multiforme: a review of where we have been and where we are going. Expert Opin Investig Drugs. 2009;18(8):1061-1083.
2. Phillips HS, Kharbanda S, Chen R, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell. 2006;9(3):157-173. (Pubitemid 43357943)
3. Gravendeel LA, Kouwenhoven MC, Gevaert O, et al. Intrinsic gene expression profiles of gliomas are a better predictor of survival than histology. Cancer Res. 2009;69(23):9065-9072.
4. Colman H, Zhang L, Sulman EP, et al. A multigene predictor of outcome in glioblastoma. Neuro Oncol. 2010;12(1):49-57.
5. Lundwall A, Clauss A, Olsson AY. Evolution of kallikrein-related peptidases in mammals and identification of a genetic locus encoding potential regulatory inhibitors. Biol Chem. 2006;387(3):243-249.
6. Sotiropoulou G, Pampalakis G, Diamandis EP. Functional roles of human kallikrein-related peptidases. J Biol Chem. 2009;284(48):32989-32994.
7. Emami N, Diamandis EP. Utility of kallikrein-related peptidases (KLKs) as cancer biomarkers. Clin Chem. 2008;54(10):1600-1607.
8. Zhu X, Albertsen PC, Andriole GL, Roobol MJ, Schroder FH, Vickers AJ. Risk-based prostate cancer screening. Eur Urol. 2011;61(4):652-661.
9. Diamandis EP, Scorilas A, Fracchioli S, et al. Human kallikrein 6 (hK6): a new potential serum biomarker for diagnosis and prognosis of ovarian carcinoma. J Clin Oncol. 2003;21(6):1035-1043. (Pubitemid 46594132)
10. Luo LY, Soosaipillai A, Grass L, Diamandis EP. Characterization of human kallikreins 6 and 10 in ascites fluid from ovarian cancer patients. Tumour Biol. 2006;27(5):227-234. (Pubitemid 44260247)
11. Shan SJ, Scorilas A, Katsaros D, Diamandis EP. Transcriptional upregulation of human tissue kallikrein 6 in ovarian cancer: clinical and mechanistic aspects. Br J Cancer. 2007;96(2):362-372. (Pubitemid 46160644)
12. Bayani J, Marrano P, Graham C, et al. Genomic instability and copynumber heterogeneity of chromosome 19q, including the kallikrein locus, in ovarian carcinomas. Mol Oncol. 2011;5(1):48-60.
13. Nathalie HV, Chris P, Serge G, et al. High kallikrein-related peptidase 6 in non-small cell lung cancer cells: an indicator of tumor proliferation and poor prognosis. J Cell Mol Med. 2009.
14. Kim JJ, Kim JT, Yoon HR, et al. Upregulation and secretion of kallikreinrelated peptidase 6 (KLK6) in gastric cancer. Tumour Biol. 2012.
15. Kim JT, Song EY, Chung KS, et al. Up-regulation and clinical significance of serine protease kallikrein 6 in colon cancer. Cancer. 2011;117(12):2608- 2619.
16. Petraki C, Dubinski W, Scorilas A, et al. Evaluation and prognostic significance of human tissue kallikrein-related peptidase 6 (KLK6) in colorectal cancer. Pathol Res Pract. 2012;208(2):104-108.
17. Cairncross G, Jenkins R. Gliomas with 1p/19q codeletion: a.k.a. oligodendroglioma. Cancer J. 2008;14(6):352-357.
18. Cairncross G, Berkey B, Shaw E, et al. Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: Intergroup Radiation Therapy Oncology Group Trial 9402. J Clin Oncol. 2006;24(18):2707-2714. (Pubitemid 46630566)
19. Burton EC, Lamborn KR, Feuerstein BG, et al. Genetic aberrations defined by comparative genomic hybridization distinguish long-term from typical survivors of glioblastoma. Cancer Res. 2002;62(21): 6205-6210. (Pubitemid 35244472)
20. Vogazianou AP, Chan R, Backlund LM, et al. Distinct patterns of 1p and 19q alterations identify subtypes of human gliomas that have different prognoses. Neuro Oncol. 2010.
21. Yousef GM, Borgono CA, White NM, et al. In silico analysis of the human kallikrein gene 6. Tumour Biol. 2004;25(5-6):282-289. (Pubitemid 40082332)
22. Strojnik T, Kavalar R, Zajc I, Diamandis EP, Oikonomopoulou K, Lah TT. Prognostic impact of CD68 and kallikrein 6 in human glioma. Anticancer Res. 2009;29(8):3269-3279.
23. Talieri M, Zoma M, Devetzi M, Scorilas A, Ardavanis A. Kallikrein-related peptidase 6 (KLK6) gene expression in intracranial tumors. Tumour Biol. 2012.
24. Scarisbrick IA, Asakura K, Blaber S, et al. Preferential expression of myelencephalon specific protease by oligodendrocytes of the adult rat spinal cord white matter. Glia. 2000;30:219-230. (Pubitemid 30259662)
25. Scarisbrick IA, Isackson PJ, Ciric B, Windebank AJ, Rodriguez M. MSP, a trypsin-like serine protease, is abundantly expressed in the human nervous system. J Comp Neurol. 2001;431(3):347-361. (Pubitemid 32115299)
26. Scarisbrick IA, Blaber SI, Lucchinetti CF, Genain CP, Blaber M, Rodriguez M. Activity of a newly identified serine protease in CNS demyelination. Brain. 2002;125(Pt 6):1283-1296. (Pubitemid 34587138)
27. Scarisbrick IA, Radulovic M, Larson N, et al. Kallikrein 6 is a novel molecular trigger of reactive astrogliosis. Biol Chem. 2012;393:355-367.
28. Therneau TM, Grambsch PM. Modeling Survival Data: Extending the Cox Model. New York: Springer; 2000.
29. Drucker KL, Kitange GJ, Kollmeyer TM, et al. Characterization and gene expression profiling in glioma cell lines with deletion of chromosome 19 before and after microcell-mediated restoration of normal human chromosome Genes Chromosomes Cancer. 2009;48(10):854-864.
30. Scarisbrick IA, Blaber SI, Tingling JT, Rodriguez M, Blaber M, Christophi GP. Potential scope of action of tissue kallikreins in CNS immunemediated disease. J Neuroimmunol. 2006;178(1-2):167-176. (Pubitemid 44307340)
31. Scarisbrick IA, Epstein B, Cloud BA, et al. Functional role of kallikrein 6 in regulating immune cell survival. PLoS One. 2011;6(3):e18376.
32. Bernett MJ, Blaber SI, Scarisbrick IA, Dhanarajan P, Thompson SM, Blaber M. Crystal structure and biochemical characterization of human kallikrein 6 reveals that a trypsin-like kallikrein is expressed in the central nervous system. J Biol Chem. 2002;277(27):24562-24570. (Pubitemid 34951983)
33. Blaber SI, Scarisbrick IA, Bernett MJ, et al. Enzymatic properties of rat myelencephalon-specific protease. Biochemistry. 2002;41(4): 1165-1173. (Pubitemid 34083769)
34. Stupp R, Dietrich PY, Ostermann Kraljevic S, et al. Promising survival for patients with newly diagnosed glioblastoma multiforme treated with concomitant radiation plus temozolomide followed by adjuvant temozolomide. J Clin Oncol. 2002;20(5):1375-1382. (Pubitemid 34177445)
35. Beier D, Rohrl S, Pillai DR, et al. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res. 2008;68(14): 5706-5715.
36. Gill JS, Windebank AJ. Cisplatin-induced apoptosis in rat dorsal root ganglion neurons is associated with attempted entry into the cell cycle. J Clin Invest. 1998;101(12):2842-2850. (Pubitemid 28294593)
37. Liu C, Sarkaria JN, Petell CA, et al. Combination of measles virus virotherapy and radiation therapy has synergistic activity in the treatment of glioblastoma multiforme. Clin Cancer Res. 2007;13(23):7155-7165. (Pubitemid 350276902)
38. Combs SE, Zipp L, Rieken S, et al. In vitro evaluation of photon and carbon ion radiotherapy in combination with chemotherapy in glioblastoma cells. Radiat Oncol. 2012;7:9.
39. Cao X, Zhu H, Ali-Osman F, Lo HW. EGFR and EGFRvIII undergo stressand EGFR kinase inhibitor-induced mitochondrial translocalization: a potential mechanism of EGFR-driven antagonism of apoptosis. Mol Cancer. 2011;10:26.
40. Eischen CM, Kottke TJ, Martins LM, et al. Comparison of apoptosis in wild-type and Fas-resistant cells: chemotherapy-induced apoptosis is not dependent on Fas/Fas ligand interactions. Blood. 1997;90(3):935-943. (Pubitemid 27314125)
41. Kaufmann SH, Desnoyers S, Ottaviano Y, Davidson NE, Poirier GG. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 1993;53(17):3976-3985. (Pubitemid 23267698)
42. Zhao W, Kridel S, Thorburn A, et al. Fatty acid synthase: a novel target for antiglioma therapy. Br J Cancer. 2006;95(7):869-878. (Pubitemid 44498103)
43. Fuh B, Sobo M, Cen L, et al. LLL-3 inhibits STAT3 activity, suppresses glioblastoma cell growth and prolongs survival in a mouse glioblastoma model. Br J Cancer. 2009;100(1):106-112.
44. Oikonomopoulou K, Hansen KK, Saifeddine M, et al. Proteinase-activated receptors, targets for kallikrein signaling. J Biol Chem. 2006;281(43):32095- 32112. (Pubitemid 46036764)
45. Vandell AG, Larson N, Laxmikanthan G, et al. Protease-activated receptor dependent and independent signaling by kallikreins 1 and 6 in CNS neuron and astroglial cell lines. J Neurochem. 2008; 107(3):855-870.
46. Tatebe H, Watanabe Y, Kasai T, et al. Extracellular neurosin degrades alpha-synuclein in cultured cells. Neurosci Res. 2010;67(4): 341-346.
47. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987-996. (Pubitemid 40349501)
48. Nakada M, Okada Y, Yamashita J. The role of matrix metalloproteinases in glioma invasion. Front Biosci. 2003;8:e261-e269.
49. Adams MN, Ramachandran R, Yau MK, et al. Structure, function and pathophysiology of protease activated receptors. Pharmacol Ther. 2011;130:248-282.
50. Zhang Y, Zhan H, Xu W, et al. Upregulation of matrix metalloproteinase-1 and proteinase-activated receptor-1 promotes the progression of human gliomas. Pathol Res Pract. 2011;207(1): 24-29.
51. Angelo PF, Lima AR, Alves FM, et al. Substrate specificity of human kallikrein 6: salt and glycosaminoglycan activation effects. J Biol Chem. 2006;281(6):3116-3126. (Pubitemid 43845921)
52. Tantivejkul K, Loberg RD, Mawocha SC, et al. PAR1-mediated NFkappaB activation promotes survival of prostate cancer cells through a Bcl-xL-dependent mechanism. J Cell Biochem. 2005;96(3):641-652. (Pubitemid 41504661)
53. Yang E, Boire A, Agarwal A, et al. Blockade of PAR1 signaling with cellpenetrating pepducins inhibits Akt survival pathways in breast cancer cells and suppresses tumor survival and metastasis. Cancer Res. 2009;69(15):6223-6231.
54. Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009;32(12):638-647.
55. Ghosh MC, Grass L, Soosaipillai A, Sotiropoulou G, Diamandis EP. Human kallikrein 6 degrades extracellular matrix proteins and may enhance the metastatic potential of tumour cells. Tumour Biol. 2004;25(4):193-199. (Pubitemid 39551746)
56. Henkhaus RS, Gerner EW, Ignatenko NA. Kallikrein 6 is a mediator of K-RAS-dependent migration of colon carcinoma cells. Biol Chem. 2008;389(6):757-764. (Pubitemid 352009420)
57. Prezas P, Arlt MJ, Viktorov P, et al. Overexpression of the human tissue kallikrein genes KLK4, 5, 6, and 7 increases the malignant phenotype of ovarian cancer cells. Biol Chem. 2006;387(6):807-811. (Pubitemid 43964805)
58. Pampalakis G, Prosnikli E, Agalioti T, Vlahou A, Zoumpourlis V, Sotiropoulou G. A tumor-protective role for human kallikrein-related peptidase 6 in breast cancer mediated by inhibition of epithelialto-mesenchymal transition. Cancer Res. 2009;69(9):3779-3787.
59. Krenzer S, Peterziel H, Mauch C, et al. Expression and function of the kallikrein-related peptidase 6 in the human melanoma microenvironment. J Invest Dermatol. 2011;131(11):2281-2288.
60. Bergmann S, Junker K, Henklein P, Hollenberg MD, Settmacher U, Kaufmann R. PAR-type thrombin receptors in renal carcinoma cells: PAR1-mediated EGFR activation promotes cell migration. Oncol Rep. 2006;15(4):889-893.
61. Arora P, Cuevas BD, Russo A, Johnson GL, Trejo J. Persistent transactivation of EGFR and ErbB2/HER2 by protease-activated receptor-1 promotes breast carcinoma cell invasion. Oncogene. 2008;27(32): 4434-4445.
62. Shi X, Gangadharan B, Brass LF, Ruf W, Mueller BM. Protease-activated receptors (PAR1 and PAR2) contribute to tumor cell motility and metastasis. Mol Cancer Res. 2004;2(7):395-402. (Pubitemid 39031073)