Protein S drives oral squamous cell carcinoma tumorigenicity through regulation of AXL

Oncotarget

Volumn 8, Issue 8, 2017, Pages 13986-14002

  Abboud Jarrous, Ghada ^a   Priya, Shivam ^a   Maimon, Avi ^a   Fischman, Stuart ^a   Cohen Elisha, Mayan ^a   Czerninski, Rakefet ^a   Burstyn Cohen, Tal ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

AXL; OSCC; PROS1; Protein S; Squamous cell carcinoma

Indexed keywords

AXL PROTEIN; PROTEIN S; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; R 428; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; AXL RECEPTOR TYROSINE KINASE; ONCOPROTEIN; PLASMA PROTEIN; PROS1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENICITY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; PROTEIN EXPRESSION; TUMOR DIFFERENTIATION; TUMOR GROWTH; ANIMAL; CELL MOTION; GENE EXPRESSION REGULATION; GENE SILENCING; HEAD AND NECK TUMOR; METABOLISM; MOUTH TUMOR; NONOBESE DIABETIC MOUSE; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SCID MOUSE; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; BLOOD PROTEINS; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HEAD AND NECK NEOPLASMS; HETEROGRAFTS; HUMANS; MICE; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; MOUTH NEOPLASMS; PROTO-ONCOGENE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 85013443434     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.14753     Document Type: Article

References (56)

1. Graham DK, DeRyckere D, Davies KD, Earp HS. The TAM family: phosphatidylserine-sensing receptor tyrosine kinases gone awry in cancer. Nature reviews Cancer. 2014; 14:769-785
2. von Mässenhausen A, Sanders C, Thewes B, Deng M, Queisser A, Vogel W, Kristiansen G, Duensing S, Schröck A, Bootz F, Brossart P, Kirfel J, Heasley L, Brägelmann J, Perner S. MERTK as a novel therapeutic target in head and neck cancer. Oncotarget. 2016; 7:32678-32694. doi: 10.18632/oncotarget.8724
3. Giles KM, Kalinowski FC, Candy PA, Epis MR, Zhang PM, Redfern AD, Stuart LM, Goodall GJ, Leedman PJ. Axl mediates acquired resistance of head and neck cancer cells to the epidermal growth factor receptor inhibitor erlotinib. Mol Cancer Ther. 2013; 12:2541-2558
4. Lee C-H, Yen C-Y, Liu S-Y, Chen C-K, Chiang C-F, Shiah S-G, Chen P-H, Shieh Y-S. Axl Is a Prognostic Marker in Oral Squamous Cell Carcinoma. Ann Surg Oncol. 2011; 19:500-508
5. Brand TM, Iida M, Stein AP, Corrigan KL, Braverman CM, Coan JP, Pearson HE, Bahrar H, Fowler TL, Bednarz BP, Saha S, Yang D, Gill PS, Lingen MW, Saloura V, Villaflor VM, et al. AXL Is a Logical Molecular Target in Head and Neck Squamous Cell Carcinoma. American Association for Cancer Research. 2015; 21:2601-2612
6. Elkabets M, Pazarentzos E, Juric D, Sheng Q, Pelossof RA, Brook S, Benzaken AO, Rodon J, Morse N, Yan JJ, Liu M, Das R, Chen Y, Tam A, Wang H, Liang J, et al. AXL mediates resistance to PI3Kalpha inhibition by activating the EGFR/PKC/mTOR axis in head and neck and esophageal squamous cell carcinomas. Cancer Cell. 2015; 27:533-546
7. Zhang Z, Lee JC, Lin L, Olivas V, Au V, LaFramboise T, Abdel-Rahman M, Wang X, Levine AD, Rho JK, Choi YJ, Choi C-M, Kim S-W, Jang SJ, Park YS, Kim WS, et al. Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat Genet. 2012; 44:852-860
8. Meyer AS, Miller MA, Gertler FB, Lauffenburger DA. The Receptor AXL Diversifies EGFR Signaling and Limits the Response to EGFR-Targeted Inhibitors in Triple-Negative Breast Cancer Cells. Science Signaling. 2013; 6:ra66-ra66
9. Stitt TN, Conn G, Gore M, Lai C, Bruno J, Radziejewski C, Mattsson K, Fisher J, Gies DR, Jones PF, Masiakowski P, Ryan TA, Tobkes NJ, Chen DH, DiStefano PS, Long GL, et al. The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell. 1995; 80:661-670
10. Lew ED, Oh J, Burrola PG, Lax I, Zagórska A, Través PG, Schelssinger J, Lemke G. Differential TAM receptorligand-phospholipid interactions delimit differential TAM bioactivities. Elife. 2014. doi: 10.7554/eLife.03385
11. Burstyn-Cohen T, Lew ED, Traves PG, Burrola PG, Hash JC, Lemke G. Genetic dissection of TAM receptor-ligand interaction in retinal pigment epithelial cell phagocytosis. Neuron. 2012; 76:1123-1132
12. Rothlin CV, Ghosh S, Zuniga EI, Oldstone MB, Lemke G. TAM Receptors Are Pleiotropic Inhibitors of the Innate Immune Response. Cell. 2007; 131:1124-1136
13. Laurance S, Lemarié CA, Blostein MD. Growth Arrest-Specific Gene 6 (gas6) and Vascular Hemostasis. Advances in Nutrition. 2012; 3:196-203
14. Lemke G. Biology of the TAM receptors. Cold Spring Harb Perspect Biol. 2013; 5:a009076
15. Carrera Silva EA, Chan PY, Joannas L, Errasti AE, Gagliani N, Bosurgi L, Jabbour M, Perry A, Smith-Chakmakova F, Mucida D, Cheroutre H, Burstyn-Cohen T, Leighton JA, Lemke G, Ghosh S, Rothlin CV. T cell-derived protein S engages TAM receptor signaling in dendritic cells to control the magnitude of the immune response. Immunity. 2013; 39:160-170
16. Burstyn-Cohen T, Heeb MJ, Lemke G. Lack of Protein S in mice causes embryonic lethal coagulopathy and vascular dysgenesis. J Clin Invest. 2009; 119:2942-2953
17. Hutterer M, Knyazev P, Abate A, Reschke M, Maier H, Stefanova N, Knyazeva T, Barbieri V, Reindl M, Muigg A, Kostron H, Stockhammer G, Ullrich A. Axl and Growth Arrest-Specific Gene 6 Are Frequently Overexpressed in Human Gliomas and Predict Poor Prognosis in Patients with Glioblastoma Multiforme. Clinical Cancer Research. 2008; 14:130-138
18. Sun W, Fujimoto J, Tamaya T. Coexpression of Gas6/Axl in human ovarian cancers. Oncology. 2004; 66:450-457
19. Loges S, Schmidt T, Tjwa M, van Geyte K, Lievens D, Lutgens E, Vanhoutte D, Borgel D, Plaisance S, Hoylaerts M, Luttun A, Dewerchin M, Jonckx B, Carmeliet P. Malignant cells fuel tumor growth by educating infiltrating leukocytes to produce the mitogen Gas6. Blood. 2010; 115:2264-2273
20. Schlegel J, Sambade MJ, Sather S, Moschos SJ, Tan AC, Winges A, DeRyckere D, Carson CC, Trembath DG, Tentler JJ, Eckhardt SG, Kuan PF, Hamilton RL, Duncan LM, Miller CR, Nikolaishvili-Feinberg N, et al. MERTK receptor tyrosine kinase is a therapeutic target in melanoma. J Clin Invest. 2013; 123:2257-2267
21. Zhang Y-X, Knyazev PG, Cheburkin YV, Sharma K, Knyazev YP, Orfi L, Szabadkai I, Daub H, Kéri G, Ullrich A. AXL Is a Potential Target for Therapeutic Intervention in Breast Cancer Progression. Cancer research. 2008; 68:1905-1915
22. O'Donnell RK, Kupferman M, Wei SJ, Singhal S, Weber R, O'Malley B, Jr., Cheng Y, Putt M, Feldman M, Ziober B, Muschel RJ. Gene expression signature predicts lymphatic metastasis in squamous cell carcinoma of the oral cavity. Oncogene. 2004; 24:1244-1251
23. Nishikawa Y, Miyazaki T, Nakashiro K, Yamagata H, Isokane M, Goda H, Tanaka H, Oka R, Hamakawa H. Human FAT1 cadherin controls cell migration and invasion of oral squamous cell carcinoma through the localization of beta-catenin. Oncol Rep. 2011; 26:587-592
24. Anneroth G, Hansen LS. A methodologic study of histologic classification and grading of malignancy in oral squamous cell carcinoma. Scand J Dent Res. 1984; 92:448-468
25. Zhong L-P, Chen W-T, Zhang C-P, Zhang Z-Y. Increased CK19 expression correlated with pathologic differentiation grade and prognosis in oral squamous cell carcinoma patients. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology. 2007; 104:377-384
26. Nanda KDS, Ranganathan K, Devi U, Joshua E. Increased expression of CK8 and CK18 in leukoplakia, oral submucous fibrosis, and oral squamous cell carcinoma: An immunohistochemistry study. Oral Surg Oral Med Oral Pathol Oral Radiol. 2012; 113:245-253
27. Kaufmann O, Fietze E, Mengs J, Dietel M. Value of p63 and Cytokeratin 5/6 as Immunohistochemical Markers for the Differential Diagnosis of Poorly Differentiated and Undifferentiated Carcinomas. American Journal of Clinical Pathology. 2001; 116:823-830
28. Fillies T, Werkmeister R, Packeisen J, Brandt B, Morin P, Weingart D, Joos U, Buerger H. Cytokeratin 8/18 expression indicates a poor prognosis in squamous cell carcinomas of the oral cavity. BMC Cancer. 2006; 6:1-8
29. Fillies T, Jogschies M, Kleinheinz J, Brandt B, Joos U, Buerger H. Cytokeratin alteration in oral leukoplakia and oral squamous cell carcinoma. Oncol Rep. 2007; 18:639-643
30. Holland SJ, Pan A, Franci C, Hu Y, Chang B, Li W, Duan M, Torneros A, Yu J, Heckrodt TJ, Zhang J, Ding P, Apatira A, Chua J, Brandt R, Pine P, et al. R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer. Cancer Res. 2010; 70:1544
31. Brand TM, Iida M, Stein AP, Corrigan KL, Braverman CM, Luthar N, Toulany M, Gill PS, Salgia R, Kimple RJ, Wheeler DL. AXL Mediates Resistance to Cetuximab Therapy. Cancer research. 2014; 74:5152-5164
32. Oda D, Dale BA, Bourekis G. Human oral epithelial cell culture. II. Keratin expression in fetal and adult gingival cells. In Vitro Cell Dev Biol. 1990; 26:596-603
33. Moll R, Divo M, Langbein L. The human keratins: biology and pathology. Histochemistry and Cell Biology. 2008; 129:705-733
34. Axelrod H, Pienta KJ. Axl as a mediator of cellular growth and survival. Oncotarget. 2014; 5:8818-8852. doi: 10.18632/oncotarget.2422
35. Li Y, Ye X, Tan C, Hongo JA, Zha J, Liu J, Kallop D, Ludlam MJ, Pei L. Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis. Oncogene. 2009; 28:3442-3455
36. Verma A, Warner SL, Vankayalapati H, Bearss DJ, Sharma S. Targeting Axl and Mer kinases in cancer. Mol Cancer Ther. 2011; 10:1763-1773
37. Korshunov VA. Axl-dependent signalling: a clinical update. Clin Sci (Lond). 2012; 122:361-368
38. Asiedu MK, Beauchamp-Perez FD, Ingle JN, Behrens MD, Radisky DC, Knutson KL. AXL induces epithelial-tomesenchymal transition and regulates the function of breast cancer stem cells. Oncogene. 2014; 33:1316-1324
39. Ben-Batalla I, Schultze A, Wroblewski M, Erdmann R, Heuser M, Waizenegger JS, Riecken K, Binder M, Schewe D, Sawall S, Witzke V, Cubas-Cordova M, Janning M, Wellbrock J, Fehse B, Hagel C, et al. Axl, a prognostic and therapeutic target in acute myeloid leukemia mediates paracrine crosstalk of leukemia cells with bone marrow stroma. Blood. 2013; 122:2443-2452
40. Wu X, Liu X, Koul S, Lee CY, Zhang Z, Halmos B. AXL kinase as a novel target for cancer therapy. Oncotarget. 2014; 5: 9546-9563. doi: 10.18632/oncotarget.2542
41. Sheridan C. First Axl inhibitor enters clinical trials. Nat Biotechnol. 2013; 31:775-776
42. Nagata K, Ohashi K, Nakano T, Arita H, Zong C, Hanafusa H, Mizuno K. Identification of the product of growth arrest-specific gene 6 as a common ligand for Axl, Sky, and Mer receptor tyrosine kinases. J Biol Chem. 1996; 271:30022-30027
43. Rankin EB, Fuh KC, Castellini L, Viswanathan K, Finger EC, Diep AN, LaGory EL, Kariolis MS, Chan A, Lindgren D, Axelson H, Miao YR, Krieg AJ, Giaccia AJ. Direct regulation of GAS6/AXL signaling by HIF promotes renal metastasis through SRC and MET. Proceedings of the National Academy of Sciences. 2014; 111:13373-13378
44. Hattori S, Kikuchi E, Kosaka T, Miyazaki Y, Tanaka N, Miyajima A, Mikami S, Oya M. Relationship Between Increased Expression of the Axl/Gas6 Signal Cascade and Prognosis of Patients with Upper Tract Urothelial Carcinoma. Ann Surg Oncol. 2016; 23:663-670
45. Rea K, Pinciroli P, Sensi M, Alciato F, Bisaro B, Lozneanu L, Raspagliesi F, Centritto F, Cabodi S, Defilippi P, Avanzi GC, Canevari S, Tomassetti A. Novel Axl-driven signaling pathway and molecular signature characterize highgrade ovarian cancer patients with poor clinical outcome. Oncotarget. 2015; 13:30859-30875. doi: 10.18632/oncotarget.5087
46. Lee C-H, Liu S-Y, Chou K-C, Yeh C-T, Shiah S-G, Huang R-Y, Cheng J-C, Yen C-Y, Shieh Y-S. Tumor-Associated Macrophages Promote Oral Cancer Progression Through Activation of the Axl Signaling Pathway. Ann Surg Oncol. 2014; 21:1031-1037
47. Valverde P. Effects of Gas6 and hydrogen peroxide in Axl ubiquitination and downregulation. Biochemical and Biophysical Research Communications. 2005; 333:180-185
48. Konishi A, Aizawa T, Mohan A, Korshunov VA, Berk BC. Hydrogen Peroxide Activates the Gas6-Axl Pathway in Vascular Smooth Muscle Cells. J Biol Chem. 2004; 279:28766-28770
49. Bellosta P, Costa M, Lin DA, Basilico C. The receptor tyrosine kinase ARK mediates cell aggregation by homophilic binding. Molecular and Cellular Biology. 1995; 15:614-625
50. Fridell YW, Jin Y, Quilliam LA, Burchert A, McCloskey P, Spizz G, Varnum B, Der C, Liu ET. Differential activation of the Ras/extracellular-signal-regulated protein kinase pathway is responsible for the biological consequences induced by the Axl receptor tyrosine kinase. Molecular and Cellular Biology. 1996; 16:135-145
51. O'Bryan JP, Frye RA, Cogswell PC, Neubauer A, Kitch B, Prokop C, Espinosa R, Le Beau MM, Earp HS, Liu ET. axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Molecular and Cellular Biology. 1991; 11:5016-5031
52. Tsou W-I, Nguyen K-QN, Calarese DA, Garforth SJ, Antes AL, Smirnov SV, Almo SC, Birge RB, Kotenko SV. Receptor Tyrosine Kinases, TYRO3, AXL, and MER, Demonstrate Distinct Patterns and Complex Regulation of Ligand-induced Activation. Journal of Biological Chemistry. 2014; 289:25750-25763
53. Mudduluru G, Ceppi P, Kumarswamy R, Scagliotti GV, Papotti M, Allgayer H. Regulation of Axl receptor tyrosine kinase expression by miR-34a and miR-199a/b in solid cancer. Oncogene. 2011; 30:2888-2899
54. Jamali Z, Asl Aminabadi N, Attaran R, Pournagiazar F, Ghertasi Oskouei S, Ahmadpour F. MicroRNAs as prognostic molecular signatures in human head and neck squamous cell carcinoma: A systematic review and metaanalysis. Oral Oncol. 2015; 51:321-331
55. Salloum-Asfar S, Arroyo AB, Teruel-Montoya R, Garcia-Barbera N, Roldan V, Vicente V, Martinez C, Gonzalez-Conejero R. MiRNA-Based Regulation of Hemostatic Factors through Hepatic Nuclear Factor-4 Alpha. PLoS One. 2016; 11:e0154751
56. Bauer T, Zagórska A, Jurkin J, Yasmin N, Köffel R, Richter S, Gesslbauer B, Lemke G, Strobl H. Identification of Axl as a downstream effector of TGF-β1 during Langerhans cell differentiation and epidermal homeostasis. The Journal of Experimental Medicine. 2012; 209:2033-2047