Hypoxic regulation of the PERK/ATF4/LAMP3-arm of the unfolded protein response in head and neck squamous cell carcinoma

Head and Neck

Volumn 37, Issue 6, 2015, Pages 896-905

  Nagelkerke, Anika ^a   Sweep, Fred C G J ^a   Stegeman, Hanneke ^a   Grénman, Reidar ^b   Kaanders, Johannes H A M ^a   Bussink, Johan ^a   Span, Paul N ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

endoplasmic reticulum stress; head and neck squamous cell carcinoma (HNSCC); hypoxia; lysosome associated membrane protein 3 (LAMP3); unfolded protein response (UPR)

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CARBONATE DEHYDRATASE IX; DENDRITIC CELL LYSOSOME ASSOCIATED MEMBRANE PROTEIN; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PHOSPHOTRANSFERASE; PKR LIKE ENDOPLASMIC RETICULUM KINASE; UNCLASSIFIED DRUG; LAMP3 PROTEIN, HUMAN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; PERK KINASE; PROTEIN KINASE R; TUMOR PROTEIN;

ARTICLE; CANCER GENETICS; CANCER PROGNOSIS; CANCER SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; DISTANT METASTASIS; ENDOPLASMIC RETICULUM STRESS; FEMALE; FOLLOW UP; GENE EXPRESSION REGULATION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOHISTOCHEMISTRY; MALE; METASTASIS FREE SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR BIOPSY; TUMOR XENOGRAFT; UNFOLDED PROTEIN RESPONSE; ADULT; AGED; ANIMAL; CELL HYPOXIA; CELL SURVIVAL; COHORT ANALYSIS; COMPARATIVE STUDY; GENETICS; HEAD AND NECK TUMOR; METABOLISM; MIDDLE AGED; MORTALITY; POLYMERASE CHAIN REACTION; PROCEDURES; PROGNOSIS; SQUAMOUS CELL CARCINOMA; SURVIVAL RATE; TUMOR CELL LINE; VERY ELDERLY; WESTERN BLOTTING; XENOGRAFT;

ACTIVATING TRANSCRIPTION FACTOR 4; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL HYPOXIA; CELL LINE, TUMOR; CELL SURVIVAL; COHORT STUDIES; EIF-2 KINASE; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAD AND NECK NEOPLASMS; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MALE; MIDDLE AGED; NEOPLASM PROTEINS; POLYMERASE CHAIN REACTION; PROGNOSIS; SURVIVAL RATE;

EID: 84929948619     PISSN: 10433074     EISSN: 10970347     Source Type: Journal    
DOI: 10.1002/hed.23693     Document Type: Article

References (42)

1. Brown JM,. Evidence for acutely hypoxic cells in mouse tumours, and a possible mechanism of reoxygenation. Br J Radiol 1979; 52: 650-656.
2. Thomlinson RH, Gray LH,. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br J Cancer 1955; 9: 539-549.
3. Rademakers SE, Span PN, Kaanders JH, Sweep FC, van der Kogel AJ, Bussink J,. Molecular aspects of tumour hypoxia. Mol Oncol 2008; 2: 41-53.
4. Brizel DM, Scully SP, Harrelson JM, et al., Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res 1996; 56: 941-943.
5. Brizel DM, Sibley GS, Prosnitz LR, Scher RL, Dewhirst MW,. Tumor hypoxia adversely affects the prognosis of carcinoma of the head and neck. Int J Radiat Oncol Biol Phys 1997; 38: 285-289.
6. Fyles AW, Milosevic M, Wong R, et al., Oxygenation predicts radiation response and survival in patients with cervix cancer. Radiother Oncol 1998; 48: 149-156.
7. Hockel M, Schlenger K, Aral B, Mitze M, Schaffer U, Vaupel P,. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res 1996; 56: 4509-4515.
8. Nordsmark M, Overgaard M, Overgaard J,. Pretreatment oxygenation predicts radiation response in advanced squamous cell carcinoma of the head and neck. Radiother Oncol 1996; 41: 31-39.
9. Sundfor K, Lyng H, Rofstad EK,. Tumour hypoxia and vascular density as predictors of metastasis in squamous cell carcinoma of the uterine cervix. Br J Cancer 1998; 78: 822-827.
10. Janssens GO, Rademakers SE, Terhaard CH, et al., Accelerated radiotherapy with carbogen and nicotinamide for laryngeal cancer: results of a phase III randomized trial. J Clin Oncol 2012; 30: 1777-1783.
11. Kaanders JH, Wijffels KI, Marres HA, et al., Pimonidazole binding and tumor vascularity predict for treatment outcome in head and neck cancer. Cancer Res 2002; 62: 7066-7074.
12. Vaupel P, Thews O, Hoeckel M,. Treatment resistance of solid tumors: role of hypoxia and anemia. Med Oncol 2001; 18: 243-259.
13. Hockel M, Vaupel P,. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 2001; 93: 266-276.
14. Sutherland RM,. Tumor hypoxia and gene expression-implications for malignant progression and therapy. Acta Oncol 1998; 37: 567-574.
15. Harris AL,. Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2002; 2: 38-47.
16. Feldman DE, Chauhan V, Koong AC,. The unfolded protein response: a novel component of the hypoxic stress response in tumors. Mol Cancer Res 2005; 3: 597-605.
17. Koumenis C, Wouters BG,. "Translating" tumor hypoxia: unfolded protein response (UPR)-dependent and UPR-independent pathways. Mol Cancer Res 2006; 4: 423-436.
18. Rouschop KM, van den Beucken T, Dubois L, et al., The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J Clin Invest 2010; 120: 127-141.
19. Wouters BG, Koritzinsky M,. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 2008; 8: 851-864.
20. Koumenis C, Naczki C, Koritzinsky M, et al., Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 2002; 22: 7405-7416.
21. Blais JD, Filipenko V, Bi M, et al., Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol Cell Biol 2004; 24: 7469-7482.
22. Ameri K, Lewis CE, Raida M, Sowter H, Hai T, Harris AL,. Anoxic induction of ATF-4 through HIF-1-independent pathways of protein stabilization in human cancer cells. Blood 2004; 103: 1876-1882.
23. Rzymski T, Milani M, Pike L, et al., Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene 2010; 29: 4424-4435.
24. Mujcic H, Rzymski T, Rouschop KM, et al., Hypoxic activation of the unfolded protein response (UPR) induces expression of the metastasis-associated gene LAMP3. Radiother Oncol 2009; 92: 450-459.
25. Kanao H, Enomoto T, Kimura T, et al., Overexpression of LAMP3/TSC403/DC-LAMP promotes metastasis in uterine cervical cancer. Cancer Res 2005; 65: 8640-8645.
26. Nagelkerke A, Mujcic H, Bussink J, et al., Hypoxic regulation and prognostic value of LAMP3 expression in breast cancer. Cancer 2011; 117: 3670-3681.
27. Mujcic H, Nagelkerke A, Rouschop KM, et al., Hypoxic activation of the PERK/eIF2alpha arm of the unfolded protein response promotes metastasis through induction of LAMP3. Clin Cancer Res 2013; 19: 6126-6137.
28. Nagelkerke A, Bussink J, Mujcic H, et al., Hypoxia stimulates migration of breast cancer cells via the PERK/ATF4/LAMP3-arm of the unfolded protein response. Breast Cancer Res 2013; 15: R2.
29. Nagelkerke A, Bussink J, van der Kogel AJ, Sweep FC, Span PN,. The PERK/ATF4/LAMP3-arm of the unfolded protein response affects radioresistance by interfering with the DNA damage response. Radiother Oncol 2013; 108: 415-421.
30. Nagelkerke A, Sieuwerts AM, Bussink J, et al., LAMP3 is involved in tamoxifen resistance in breast cancer through modulation of autophagy. Endocr Relat Cancer 2014; 21: 101-112.
31. Hoogsteen IJ, Lok J, Marres HA, et al., Hypoxia in larynx carcinomas assessed by pimonidazole binding and the value of CA-IX and vascularity as surrogate markers of hypoxia. Eur J Cancer 2009; 45: 2906-2914.
32. Nijkamp MM, Hoogsteen IJ, Span PN, et al., Spatial relationship of phosphorylated epidermal growth factor receptor and activated AKT in head and neck squamous cell carcinoma. Radiother Oncol 2011; 101: 165-170.
33. Troost EG, Laverman P, Philippens ME, et al., Correlation of [18F]FMISO autoradiography and pimonidazole [corrected] immunohistochemistry in human head and neck carcinoma xenografts. Eur J Nucl Med Mol Imaging 2008; 35: 1803-1811.
34. Stegeman H, Kaanders JH, Wheeler DL, et al., Activation of AKT by hypoxia: a potential target for hypoxic tumors of the head and neck. BMC Cancer 2012; 12: 463.
35. de Kok JB, Roelofs RW, Giesendorf BA, et al., Normalization of gene expression measurements in tumor tissues: comparison of 13 endogenous control genes. Lab Invest 2005; 85: 154-159.
36. Nagelkerke A, Mujcic H, Wouters B, Span PN,. 18S is an appropriate housekeeping gene for in vitro hypoxia experiments. Br J Cancer 2010; 103: 590; author reply 591-592.
37. de Haro C, Mendez R, Santoyo J,. The eIF-2alpha kinases and the control of protein synthesis. FASEB J 1996; 10: 1378-1387.
38. Kaufman RJ,. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 1999; 13: 1211-1233.
39. Bi M, Naczki C, Koritzinsky M, et al., ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J 2005; 24: 3470-3481.
40. Blais JD, Addison CL, Edge R, et al., Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress. Mol Cell Biol 2006; 26: 9517-9532.
41. Mazure NM, Pouyssegur J,. Hypoxia-induced autophagy: cell death or cell survival? Curr Opin Cell Biol 2010; 22: 177-180.
42. Lee AH, Iwakoshi NN, Glimcher LH,. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003; 23: 7448-7459.