Enhanced cell migration and apoptosis resistance may underlie the association between high SERPINE1 expression and poor outcome in head and neck carcinoma patients

Oncotarget

Volumn 6, Issue 30, 2015, Pages 29016-29033

  Pavón, Miguel Angel ^a,b   Arroyo Solera, Irene ^a,b   Téllez Gabriel, Marta ^a,b   León, Xavier ^b,c   Virós, David ^d   López, Montserrat ^c   Gallardo, Alberto ^e   Céspedes, Maria Virtudes ^a,b   Casanova, Isolda ^a,b   López Pousa, Antonio ^b,c   Mangues, Maria Antonia ^c   Quer, Miquel ^c   Barnadas, Agustí ^c   Mangues, Ramón ^a,b  

^a BIOMEDICAL RESEARCH INSTITUTE SANT PAU IIB SANT PAU   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^d Servicio de Medicina Intensiva   (Spain)

^e HOSPITAL JOSEP TRUETA   (Spain)

Author keywords

AKT; Biomarker; HNSCC; Prognosis; SERPINE1

Indexed keywords

8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; CISPLATIN; MESSENGER RNA; PLASMINOGEN ACTIVATOR INHIBITOR 1; ANTINEOPLASTIC AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SERPINE1 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; ALCOHOL CONSUMPTION; APOPTOSIS; ARTICLE; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER SPECIFIC SURVIVAL; CELL MIGRATION; CELL PROLIFERATION; CHEMORADIOTHERAPY; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; DRUG RESISTANCE; FEMALE; GENE EXPRESSION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; LOCAL RECURRENCE FREE SURVIVAL; MAJOR CLINICAL STUDY; MALE; METASTASIS; OUTCOME ASSESSMENT; PATIENT RISK; PROGRESSION FREE SURVIVAL; PROSPECTIVE STUDY; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; RISK FACTOR; SQUAMOUS CELL CARCINOMA CELL LINE; WART VIRUS; CARCINOMA, SQUAMOUS CELL; CELL MOTION; DISEASE COURSE; DISEASE FREE SURVIVAL; DRUG EFFECTS; GENETIC DATABASE; GENETIC TRANSFECTION; GENETICS; HEAD AND NECK NEOPLASMS; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MORTALITY; PATHOLOGY; PROPORTIONAL HAZARDS MODEL; RADIATION RESPONSE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTOR; TREATMENT OUTCOME; TUMOR CELL LINE; TUMOR INVASION; UPREGULATION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BIOMARKERS, TUMOR; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CHEMORADIOTHERAPY; CISPLATIN; DATABASES, GENETIC; DISEASE PROGRESSION; DISEASE-FREE SURVIVAL; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; PHOSPHATIDYLINOSITOL 3-KINASE; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROPORTIONAL HAZARDS MODELS; PROSPECTIVE STUDIES; PROTO-ONCOGENE PROTEINS C-AKT; RETROSPECTIVE STUDIES; RISK FACTORS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TREATMENT OUTCOME; UP-REGULATION;

EID: 84945156332     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5032     Document Type: Article

References (64)

1. Leemans CR, Braakhuis BJ, Brakenhoff RH. The molecular biology of head and neck cancer. Nat Rev Cancer. 2011; 11:9-22.
2. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics. CA Cancer J Clin. 2014; 64:9-29.
3. Argiris A, Karamouzis MV, Raben D, Ferris RL. Head and neck cancer. Lancet. 2008; 371:1695-1709.
4. Leon X, Quer M, Diez S, Orus C, Lopez-Pousa A, Burgues J. Second neoplasm in patients with head and neck cancer. Head Neck. 1999; 21:204-210.
5. Braakhuis BJ, Brakenhoff RH, Leemans CR. Treatment choice for locally advanced head and neck cancers on the basis of risk factors: biological risk factors. Ann Oncol. 2012; 23:x173-177.
6. Lu P, Takai K, Weaver VM, Werb Z. Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol. 2011; 3.
7. Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci. 2010; 123:4195-4200.
8. Kwaan HC, McMahon B. The role of plasminogen-plasmin system in cancer. Cancer Treat Res. 2009; 148:43-66.
9. Ulisse S, Baldini E, Sorrenti S, D'Armiento M. The urokinase plasminogen activator system: a target for anti-cancer therapy. Curr Cancer Drug Targets. 2009; 9:32-71.
10. Mazar AP. Urokinase plasminogen activator receptor choreographs multiple ligand interactions: implications for tumor progression and therapy. Clin Cancer Res. 2008; 14:5649-5655.
11. Margheri F, Luciani C, Taddei ML, Giannoni E, Laurenzana A, Biagioni A, Chilla A, Chiarugi P, Fibbi G, Del Rosso M. The receptor for urokinase-plasminogen activator (uPAR) controls plasticity of cancer cell movement in mesenchymal and amoeboid migration style. Oncotarget. 2014; 5:1538-1553.
12. Duffy MJ, McGowan PM, Gallagher WM. Cancer invasion and metastasis: changing views. J Pathol. 2008; 214:283-293.
13. Harris L, Fritsche H, Mennel R, Norton L, Ravdin P, Taube S, Somerfield MR, Hayes DF, Bast RC Jr. American Society of Clinical Oncology update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol. 2007; 25:5287-5312.
14. Look MP, van Putten WL, Duffy MJ, Harbeck N, Christensen IJ, Thomssen C, Kates R, Spyratos F, Ferno M, Eppenberger-Castori S, Sweep CG, Ulm K, Peyrat JP, Martin PM, Magdelenat H, Brunner N, et al. Pooled analysis of prognostic impact of urokinase-type plasminogen activator and its inhibitor PAI-1 in 8377 breast cancer patients. J Natl Cancer Inst. 2002; 94:116-128.
15. Strojan P, Budihna M, Smid L, Vrhovec I, Skrk J. Urokinase-type plasminogen activator (uPA) and plasminogen activator inhibitor type 1 (PAI-1) in tissue and serum of head and neck squamous cell carcinoma patients. Eur J Cancer. 1998; 34:1193-1197.
16. Speleman L, Kerrebijn JD, Look MP, Meeuwis CA, Foekens JA, Berns EM. Prognostic value of plasminogen activator inhibitor-1 in head and neck squamous cell carcinoma. Head Neck. 2007; 29:341-350.
17. Lindberg P, Larsson A, Nielsen BS. Expression of plasminogen activator inhibitor-1, urokinase receptor and laminin gamma-2 chain is an early coordinated event in incipient oral squamous cell carcinoma. Int J Cancer. 2006; 118:2948-2956.
18. Huang CF, Yu GT, Wang WM, Liu B, Sun ZJ. Prognostic and predictive values of SPP1, PAI and caveolin-1 in patients with oral squamous cell carcinoma. Int J Clin Exp Pathol. 2014; 7:6032-6039.
19. Shi Z, Stack MS. Urinary-type plasminogen activator (uPA) and its receptor (uPAR) in squamous cell carcinoma of the oral cavity. Biochem J. 2007; 407:153-159.
20. Chin D, Boyle GM, Williams RM, Ferguson K, Pandeya N, Pedley J, Campbell CM, Theile DR, Parsons PG, Coman WB. Novel markers for poor prognosis in head and neck cancer. Int J Cancer. 2005; 113:789-797.
21. Chen YJ, Lin SC, Kao T, Chang CS, Hong PS, Shieh TM, Chang KW. Genome-wide profiling of oral squamous cell carcinoma. J Pathol. 2004; 204:326-332.
22. Liu CJ, Liu TY, Kuo LT, Cheng HW, Chu TH, Chang KW, Lin SC. Differential gene expression signature between primary and metastatic head and neck squamous cell carcinoma. J Pathol. 2008; 214:489-497.
23. Mendez E, Houck JR, Doody DR, Fan W, Lohavanichbutr P, Rue TC, Yueh B, Futran ND, Upton MP, Farwell DG, Heagerty PJ, Zhao LP, Schwartz SM, Chen C. A genetic expression profile associated with oral cancer identifies a group of patients at high risk of poor survival. Clin Cancer Res. 2009; 15:1353-1361.
24. Roepman P, Wessels LF, Kettelarij N, Kemmeren P, Miles AJ, Lijnzaad P, Tilanus MG, Koole R, Hordijk GJ, van der Vliet PC, Reinders MJ, Slootweg PJ, Holstege FC. An expression profile for diagnosis of lymph node metastases from primary head and neck squamous cell carcinomas. Nat Genet. 2005; 37:182-186.
25. Schmalbach CE, Chepeha DB, Giordano TJ, Rubin MA, Teknos TN, Bradford CR, Wolf GT, Kuick R, Misek DE, Trask DK, Hanash S. Molecular profiling and the identification of genes associated with metastatic oral cavity/pharynx squamous cell carcinoma. Arch Otolaryngol Head Neck Surg. 2004; 130:295-302.
26. Magnussen S, Rikardsen OG, Hadler-Olsen E, Uhlin-Hansen L, Steigen SE, Svineng G. Urokinase plasminogen activator receptor (uPAR) and plasminogen activator inhibitor-1 (PAI-1) are potential predictive biomarkers in early stage oral squamous cell carcinomas (OSCC). PLoS One. 2014; 9:e101895.
27. Dhanda J, Triantafyllou A, Liloglou T, Kalirai H, Lloyd B, Hanlon R, Shaw RJ, Sibson DR, Risk JM. SERPINE1 and SMA expression at the invasive front predict extracapsular spread and survival in oral squamous cell carcinoma. Br J Cancer. 2014.
28. Hundsdorfer B, Zeilhofer HF, Bock KP, Dettmar P, Schmitt M, Kolk A, Pautke C, Horch HH. Tumourassociated urokinase-type plasminogen activator (uPA) and its inhibitor PAI-1 in normal and neoplastic tissues of patients with squamous cell cancer of the oral cavity-clinical relevance and prognostic value. J Craniomaxillofac Surg. 2005; 33:191-196.
29. Nozaki S, Endo Y, Kawashiri S, Nakagawa K, Yamamoto E, Yonemura Y, Sasaki T. Immunohistochemical localization of a urokinase-type plasminogen activator system in squamous cell carcinoma of the oral cavity: association with mode of invasion and lymph node metastasis. Oral Oncol. 1998; 34:58-62.
30. Strojan P, Budihna M, Smid L, Vrhovec I, Skrk J. Urokinase-type plasminogen activator, plasminogen activator inhibitor type 1 and cathepsin D: analysis of their prognostic significance in squamous cell carcinoma of the head and neck. Anticancer Res. 2000; 20:3975-3981.
31. Rodrigo JP, Heideman DA, Garcia-Pedrero JM, Fresno MF, Brakenhoff RH, Diaz Molina JP, Snijders PJ, Hermsen MA. Time trends in the prevalence of HPV in oropharyngeal squamous cell carcinomas in northern Spain (1990-2009). Int J Cancer. 2014; 134:487-492.
32. Sakakibara T, Hibi K, Koike M, Fujiwara M, Kodera Y, Ito K, Nakao A. Plasminogen activator inhibitor-1 as a potential marker for the malignancy of colorectal cancer. Br J Cancer. 2005; 93:799-803.
33. Duffy MJ, Maguire TM, McDermott EW, O'Higgins N. Urokinase plasminogen activator: a prognostic marker in multiple types of cancer. J Surg Oncol. 1999; 71:130-135.
34. Harbeck N, Alt U, Berger U, Kruger A, Thomssen C, Janicke F, Hofler H, Kates RE, Schmitt M. Prognostic impact of proteolytic factors (urokinase-type plasminogen activator, plasminogen activator inhibitor 1, and cathepsins B, D, and L) in primary breast cancer reflects effects of adjuvant systemic therapy. Clin Cancer Res. 2001; 7:2757-2764.
35. Duffy MJ. Urokinase plasminogen activator and its inhibitor, PAI-1, as prognostic markers in breast cancer: from pilot to level 1 evidence studies. Clin Chem. 2002; 48:1194-1197.
36. Rotblat B, Grunewald TG, Leprivier G, Melino G, Knight RA. Anti-oxidative stress response genes: bioinformatic analysis of their expression and relevance in multiple cancers. Oncotarget. 2013; 4:2577-2590.
37. Langlois B, Saupe F, Rupp T, Arnold C, van der Heyden M, Orend G, Hussenet T. AngioMatrix, a signature of the tumor angiogenic switch-specific matrisome, correlates with poor prognosis for glioma and colorectal cancer patients. Oncotarget. 2014; 5:10529-10545.
38. Wilkins-Port CE, Ye Q, Mazurkiewicz JE, Higgins PJ. TGF-beta1 + EGF-initiated invasive potential in transformed human keratinocytes is coupled to a plasmin/MMP-10/MMP-1-dependent collagen remodeling axis: role for PAI-1. Cancer Res. 2009; 69:4081-4091.
39. Czekay RP, Wilkins-Port CE, Higgins SP, Freytag J, Overstreet JM, Klein RM, Higgins CE, Samarakoon R, Higgins PJ. PAI-1: An Integrator of Cell Signaling and Migration. Int J Cell Biol. 2011; 2011:562481.
40. Degryse B, Neels JG, Czekay RP, Aertgeerts K, Kamikubo Y, Loskutoff DJ. The low density lipoprotein receptor-related protein is a motogenic receptor for plasminogen activator inhibitor-1. J Biol Chem. 2004; 279:22595-22604.
41. Kamikubo Y, Neels JG, Degryse B. Vitronectin inhibits plasminogen activator inhibitor-1-induced signalling and chemotaxis by blocking plasminogen activator inhibitor-1 binding to the low-density lipoprotein receptor-related protein. Int J Biochem Cell Biol. 2009; 41:578-585.
42. Romer MU, Larsen L, Offenberg H, Brunner N, Lademann UA. Plasminogen activator inhibitor 1 protects fibrosarcoma cells from etoposide-induced apoptosis through activation of the PI3K/Akt cell survival pathway. Neoplasia. 2008; 10:1083-1091.
43. Kwaan HC, Wang J, Svoboda K, Declerck PJ. Plasminogen activator inhibitor 1 may promote tumour growth through inhibition of apoptosis. Br J Cancer. 2000; 82:1702-1708.
44. Wolff C, Malinowsky K, Berg D, Schragner K, Schuster T, Walch A, Bronger H, Hofler H, Becker KF. Signalling networks associated with urokinase-type plasminogen activator (uPA) and its inhibitor PAI-1 in breast cancer tissues: new insights from protein microarray analysis. J Pathol. 2011; 223:54-63.
45. Martin D, Abba MC, Molinolo AA, Vitale-Cross L, Wang Z, Zaida M, Delic NC, Samuels Y, Lyons JG, Gutkind JS. The head and neck cancer cell oncogenome: a platform for the development of precision molecular therapies. Oncotarget. 2014; 5:8906-8923.
46. Xue G, Hemmings BA. PKB/Akt-dependent regulation of cell motility. J Natl Cancer Inst. 2013; 105:393-404.
47. Fang H, Placencio VR, DeClerck YA. Protumorigenic activity of plasminogen activator inhibitor-1 through an antiapoptotic function. J Natl Cancer Inst. 2012; 104:1470-1484.
48. Ju X, Katiyar S, Wang C, Liu M, Jiao X, Li S, Zhou J, Turner J, Lisanti MP, Russell RG, Mueller SC, Ojeifo J, Chen WS, Hay N, Pestell RG. Akt1 governs breast cancer progression in vivo. Proc Natl Acad Sci U S A. 2007; 104:7438-7443.
49. Simone TM, Higgins CE, Czekay RP, Law BK, Higgins SP, Archambeault J, Kutz SM, Higgins PJ. SERPINE1: A Molecular Switch in the Proliferation-Migration Dichotomy in Wound-"Activated" Keratinocytes. Adv Wound Care (New Rochelle). 2014; 3:281-290.
50. Lamb R, Lisanti MP, Clarke RB, Landberg G. Co-ordination of cell cycle, migration and stem cell-like activity in breast cancer. Oncotarget. 2014; 5:7833-7842.
51. Shiwarski DJ, Shao C, Bill A, Kim J, Xiao D, Bertrand CA, Seethala RS, Sano D, Myers JN, Ha P, Grandis J, Gaither LA, Puthenveedu MA, Duvvuri U. To "Grow" or "Go": TMEM16A Expression as a Switch between Tumor Growth and Metastasis in SCCHN. Clin Cancer Res. 2014; 20:4673-4688.
52. Giese A, Bjerkvig R, Berens ME, Westphal M. Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol. 2003; 21:1624-1636.
53. Schultz C, Lemke N, Ge S, Golembieski WA, Rempel SA. Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res. 2002; 62:6270-6277.
54. Wang SD, Rath P, Lal B, Richard JP, Li Y, Goodwin CR, Laterra J, Xia S. EphB2 receptor controls proliferation/migration dichotomy of glioblastoma by interacting with focal adhesion kinase. Oncogene. 2012; 31:5132-5143.
55. Fedotov S, Iomin A. Migration and proliferation dichotomy in tumor-cell invasion. Phys Rev Lett. 2007; 98:118101.
56. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst. 2005; 97:1180-1184.
57. Pavon MA, Parreno M, Leon X, Sancho FJ, Cespedes MV, Casanova I, Lopez-Pousa A, Mangues MA, Quer M, Barnadas A, Mangues R. Ku70 predicts response and primary tumor recurrence after therapy in locally advanced head and neck cancer. Int J Cancer. 2008; 123:1068-1079.
58. Brenner JC, Graham MP, Kumar B, Saunders LM, Kupfer R, Lyons RH, Bradford CR, Carey TE. Genotyping of 73 UM-SCC head and neck squamous cell carcinoma cell lines. Head Neck. 2010; 32:417-426.
59. Zhao M, Sano D, Pickering CR, Jasser SA, Henderson YC, Clayman GL, Sturgis EM, Ow TJ, Lotan R, Carey TE, Sacks PG, Grandis JR, Sidransky D, Heldin NE, Myers JN. Assembly and initial characterization of a panel of 85 genomically validated cell lines from diverse head and neck tumor sites. Clin Cancer Res. 2011; 17:7248-7264.
60. Providence KM, Higgins SP, Mullen A, Battista A, Samarakoon R, Higgins CE, Wilkins-Port CE, Higgins PJ. SERPINE1 (PAI-1) is deposited into keratinocyte migration "trails" and required for optimal monolayer wound repair. Arch Dermatol Res. 2008; 300:303-310.
61. Rompani SB, Cepko CL. Retinal progenitor cells can produce restricted subsets of horizontal cells. Proc Natl Acad Sci U S A. 2008; 105:192-197.
62. Bosch R, Dieguez-Gonzalez R, Cespedes MV, Parreno M, Pavon MA, Granena A, Sierra J, Mangues R, Casanova I. A novel inhibitor of focal adhesion signaling induces caspaseindependent cell death in diffuse large B-cell lymphoma. Blood. 2011; 118:4411-4420.
63. Guerrero S, Casanova I, Farre L, Mazo A, Capella G, Mangues R. K-ras codon 12 mutation induces higher level of resistance to apoptosis and predisposition to anchorage-independent growth than codon 13 mutation or proto-oncogene overexpression. Cancer Res. 2000; 60:6750-6756.
64. Tellez-Gabriel M, Arroyo-Solera I, Leon X, Gallardo A, Lopez M, Cespedes MV, Casanova I, Lopez-Pousa A, Quer M, Mangues MA, Barnadas A, Mangues R, Pavon MA. High RAB5 expression is associated with good clinical outcome in patients with locally advanced head and neck squamous cell carcinoma. Cancer Med. 2013; 2:950-963.