Program Project Grant (P01): UPR/ ISR in Cancer
NIH Grant # P01-CA165997
Principal Investigator:
- Costas Koumenis, PhD, University of Pennsylvania
Project Overview:
The overall goal of this Program is to investigate the role of the Unfolded Protein Response (UPR) signaling pathway in tumor homeostasis and tumor progression. Rapidly proliferating cancer cells must thrive in amicroenvironment wherein metabolic nutrients such as glucose, oxygen and growth factors become limitingas tumor volume expands beyond the established vascularity of the tissue. The UPR functions as a sensorof the availability of key cellular nutrients, such as glucose and oxygen, that are critically important for tumorgrowth and progression. The UPR and specifically the PERK kinase, has recently been shown to facilitateoncogene-mediated tumor progression, suggesting that the UPR may also respond to bioenergeticchallenges triggered by aberrant oncogene-dependent signaling. The overall hypothesis being interrogatedby this Program Project is that the UPR and more specifically, the PERK kinase, functions as a sensor oftumor cell autonomous and non-autonomous bioenergetic stress; the ensuing activation of PERK catalyticfunction promotes tumor cell adaptation to this stress and thereby facilitates tumor progression. To test thishypothesis, three synergistic projects have been developed. Project 1 will evaluate mechanisms whereby amicro-RNA balances PERK-dependent pro-survival and pro-apoptotic functions. Key preliminary datasuggest that miR-211 is a novel regulator of the pro-apoptotic factor, CHOP, and functions to temporallyregulate CHOP expression. Project 2 will interrogate the function of PERK as a first response regulator of c-Myc-dependent bioenergetic and proteotoxic stress. Through its capacity to temper protein translation,PERK moderates cellular response to c-Myc thereby ensuring that bioenergetic capacity matches oncogenicdemand resulting in tumor growth rather than apoptosis. Project 3 will test the hypothesis that tumor cellsactivate the UPR, and, perhaps, more broadly the Integrated Stress Response (ISR) due to oncogeneactivation or oxygen and/or nutritional deficit, and thereby acquire the ability to escape the anti-proliferativeand pro-apoptotic effects of Type 1 interferons, IFNa/p. Through the synergistic functions of this Program,we will ascertain how PERK balances growth with apoptosis (Projects 1 and 2), how PERK responds toenvironmental challenge (Projects 1 and 3) and how tumor cells utilize PERK and the UPR to adapt tooncogene-triggered bioenergetic stress (Projects 1-2-3). All three projects will make extensive use ofscientific Core B (Metabolomics/ Genomics) and have already established a working, highly collaborativerelationship. It is our supposition that findings stemming from work proposed herein will provide a foundationfor the design of novel anti-cancer treatment strategies targeting this pathway.
Project 1: Micro-RNA-dependent signaling by the UPR
- J. Alan Diehl, PhD, Medical University of South Carolina (Leader)
- Je-Hyun Yoon, PhD, Medical University of South Carolina (Co-Investigator)
Project 2: The UPR effector ATF4 in metabolic reprogramming and survival during Myc-induced tumorigenesis
- Costas Koumenis, PhD, University of Pennsylvania (Leader)
- Davide Ruggero, PhD, University of California, San Fransisco (Co-Investigator, Project 2)
Project 3: Integrated Stress and Interferon Responses
- Serge Y. Fuchs, MD, PhD, University of Pennsylvania (Leader)
Core A: Administrative Core
- Costas Koumenis, PhD, University of Pennsylvania (Director)
- Andrea Rycroft, University of Pennsylvania (Project Coordinator)
Core B: Metabolomics/Genomics
- Aalim Weljie, PhD, University of Pennsylvania (Core Director)
- Paul Wang, PhD, University of Pennsylvania (Co-Investigator)
External Advisory Board:
- Amato J. Giaccia, PhD, Stanford University
- Linda Hendershot, PhD, St. Jude Children's Research Hospital
- Steven McMahon, PhD, Thomas Jefferson University
- Dmitry Gabrilovich, MD, PhD, The Wistar Institute
Publications
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Gui J, Katlinski KV, Koumenis C, Diehl JA, Fuchs SY. The PKR-Like Endoplasmic Reticulum Kinase Promotes the Dissemination of Myc-Induced Leukemic Cells. Mol Cancer Res. 2019 Mar 22. PMID: 30902831
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Ortiz A, Gui J, Zahedi F, Yu P, Cho C, Bhattacharya S, Carbone CJ, Yu Q, Katlinski KV, Katlinskaya YV, Handa S, Haas V, Volk SW, Brice AK, Wals K, Matheson NJ, Antrobus R, Ludwig S, Whiteside TL, Sander C, Tarhini AA, Kirkwood JM, Lehner PJ, Guo W, Rui H, Minn AJ, Koumenis C, Diehl JA, Fuchs SY. An Interferon-Driven Oxysterol-Based Defense against Tumor-Derived Extracellular Vesicles. Cancer Cell. 2019 Jan 14;35(1):33-45.e6. doi: 10.1016/j.ccell.2018.12.001. PubMed PMID: 30645975; PubMed Central PMCID: PMC6336114
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Tameire, F., Verginadis, I., Leli, MN., Polte C., Dr. Conn S.C., Ojha, R., Salas C., Chinga F., Monroy M.A., Fu X., Wang P., Kossenkov A., Dr. Ye J., Amaravadi R., Ignatova Z., Fuchs S.Y., Diehl J.A., Ruggero, D. and Koumenis C. ATF4 couples MYC-dependent translational activity to bioenergetic demands during tumor progression. Nat. Cell Biol., in press.
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Nguyen HG, Conn CS, Kye Y, Xue L, Forester CM, Cowen JE, Hsieh AC, Cunningham JT, Truillet C, Tamiere F, Evans MK, Evans CP, Yang JC, Hann B, Koumenis C, Walter P, Carroll PR, Ruggero D. Development of stress response therapy targeting aggressive prostate cancer. Sci Transl. Med. 2018 May; 10(439). PMID: 29720449. PMCID: PMC6045425
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Bu Y, Yoshida A, Chitnis N, Altman BJ, Tameire F, Oran A, Gennaro V, Armeson KE, McMahon SB, Wertheim GB, Dang CV, Ruggero D, Koumenis C, Fuchs SY, Diehl JA. A PERK-miR-211 axis suppresses circadian regulators and protein synthesis to promote cancer cell survival. Nat Cell Biol. 2018 Jan;20(1):104-115. doi: 10.1038/s41556-017-0006-y. Epub 2017 Dec 11. PubMed PMID: 29230015; PubMed Central PMCID: PMC5741512.
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Brady LK, Wang H, Radens CB, Bi Y, Radovich M, Maity A, Ivan A, Ivan M, Barash Y, Koumenis C. Transcriptome analysis of hypoxic cancer cells uncovers intron retention in EIF2B5 as a mechanism to inhibit translation. PLoS Biol., 2017 Sept 29; 15(9). PMID: 28961236. PMCID: PMC5636171.
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McQuiston AS and Diehl JA. Recent Insights into PERK-Dependent Signaling from the Endoplasmic Reticulum. F1000 Faculty Reviews. 2017 Oct 27; 6: 1897. PMID: 29152224. PMCID: PMC5667976.
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Katlinski KV, Gui J, Katlinskaya YV, Ortiz A, Chakraborty R, Bhattacharya S, Carbone CJ, Beiting DP, Girondo MA, Peck AR, Puré E, Chatterji P, Rustgi AK, Diehl JA, Koumenis C, Rui H, Fuchs SY. Inactivation of Interferon Receptor Promotes the Establishment of Immune Privileged Tumor Microenvironment. Cancer Cell. 2017 Feb 13;31(2):194-207. PubMed PMID: 28196594; PubMed Central PMCID: PMC5313042.
- Zhao B, Bhattacharya S, Yu Q, Fuchs SY. Expression of the IFNAR1 chain of type 1 interferon receptor in benign cells protects against progression of acute leukemia. Leuk Lymphoma. 2017 May 15:1-7. PubMed PMID: 28503979.
- Zhang KJ, Yin XF, Yang YQ, Li HL, Xu YN, Chen LY, Liu XJ, Yuan SJ, Fang XL, Xiao J, Wu S, Xu HN, Chu L, Katlinski KV, Katlinskaya YV, Guo RB, Wei GW, Wang DC, Liu XY, Fuchs SY. A Potent In Vivo Antitumor Efficacy of Novel Recombinant Type I Interferon. Clin Cancer Res. 2017 Apr 15;23(8):2038-2049. PubMed PMID: 27683179; PubMed Central PMCID: PMC5373932.
- Hong F, Liu B, Wu BX, Morreall J, Roth B, Davies C, Sun S, Diehl JA, Li Z. CNPY2 is a key initiator of the PERK-CHOP pathway of the unfolded protein response. Nat Struct Mol Biol. 2017 Oct; 24(10): 834-839. PMID: 28869608. PMCID: PMC6102046.
- Ortiz A, Fuchs SY. Anti-metastatic functions of type 1 interferons: Foundation for the adjuvant therapy of cancer. Cytokine. 2017 Jan;89:4-11. Review. PubMed PMID: 26822709. PubMed Central PMCID: PMC4959969.
- Pytel D, Gao Y, Mackiewicz K, Katlinskaya YV, Staschke KA, Paredes MC, Yoshida A, Qie S, Zhang G, Chajewski OS, Wu L, Majsterek I, Herlyn M, Fuchs SY, Diehl JA. PERK Is a Haploinsufficient Tumor Suppressor: Gene Dose Determines Tumor-Suppressive Versus Tumor Promoting Properties of PERK in Melanoma. PLoS Genet. 2016 Dec 15;12(12):e1006518. PubMed PMID: 27977682; PubMed Central PMCID: PMC5207760.
- Gui J, Gober M, Yang X, Katlinski KV, Marshall CM, Sharma M, Werth VP, Baker DP, Rui H, Seykora JT, Fuchs SY. Therapeutic Elimination of the Type 1 Interferon Receptor for Treating Psoriatic Skin Inflammation. J Invest Dermatol. 2016 Oct;136(10):1990-2002. PubMed PMID: 27369778; PubMed Central PMCID: PMC5035634.
- Bu Y, Diehl JA. PERK Integrates Oncogenic Signaling and Cell Survival During Cancer Development. J Cell Physiol. 2016 Oct;231(10):2088-96. Review. PubMed PMID: 26864318; PubMed Central PMCID: PMC4912452.
- Bu Y, Diehl JA. Stressing Out Melanoma with an anti-GRP78 compound. Pigment Cell Melanoma Res. 2016 Sep;29(5):490-1. PubMed PMID: 27302845; PubMed Central PMCID: PMC5448159
- Katlinskaya YV, Katlinski KV, Yu Q, Ortiz A, Beiting DP, Brice A, Davar D, Sanders C, Kirkwood JM, Rui H, Xu X, Koumenis C, Diehl JA, Fuchs SY. Suppression of Type I Interferon Signaling Overcomes Oncogene-Induced Senescence and Mediates Melanoma Development and Progression. Cell Rep. 2016 Apr 5;15(1):171-80. PubMed PMID: 27052162; PubMed Central PMCID: PMC4826807.
- Xu Z, Bu Y, Chitnis N, Koumenis C, Fuchs SY, Diehl JA. miR-216b regulation of c-Jun mediates GADD153/CHOP-dependent apoptosis. Nat Commun. 2016 May 13;7:11422. PubMed PMID: 27173017; PubMed Central PMCID: PMC4869177.
- Davar D, Fuchs SY, Kirkwood JM. BRAF Inhibitors and IFNα: Plus, Minus, or Indeterminate? J Natl Cancer Inst. 2016 Feb 5;108(7). pii: djv432. PubMed PMID: 26851801.
- Katlinskaya YV, Katlinski KV, Lasri A, Li N, Beiting DP, Durham AC, Yang T, Pikarsky E, Lengner CJ, Johnson FB, Ben-Neriah Y, Fuchs SY. Type I Interferons Control Proliferation and Function of the Intestinal Epithelium. Mol Cell Biol. 2016 Jan 25;36(7):1124-35. PubMed PMID: 26811327; PubMed Central PMCID: PMC4800802.
- Xia C, Vijayan M, Pritzl CJ, Fuchs SY, McDermott AB, Hahm B. Hemagglutinin of Influenza A Virus Antagonizes Type I Interferon (IFN) Responses by Inducing Degradation of Type I IFN Receptor 1. J Virol. 2015 Dec 16;90(5):2403-17. PubMed PMID: 26676772; PubMed Central PMCID: PMC4810695.
- Yu Q, Zhao B, Gui J, Katlinski KV, Brice A, Gao Y, Li C, Kushner JA, Koumenis C, Diehl JA, Fuchs SY. Type I interferons mediate pancreatic toxicities of PERK inhibition. Proc Natl Acad Sci U S A. 2015 Dec 15;112(50):15420-5. PubMed PMID: 26627716; PubMed Central PMCID: PMC4687574.
- Katlinskaya YV, Carbone CJ, Yu Q, Fuchs SY. Type 1 interferons contribute to the clearance of senescent cell. Cancer Biol Ther. 2015;16(8):1214-9. PubMed PMID: 26046815; PubMed Central PMCID: PMC4622626.
- Tameire F, Verginadis II, Koumenis C. Cell intrinsic and extrinsic activators of the unfolded protein response in cancer: Mechanisms and targets for therapy. Semin Cancer Biol. 2015 Aug;33:3-15. Review. PubMed PMID: 25920797; PubMed Central PMCID: PMC4523493.
- Dey S, Sayers CM, Verginadis II, Lehman SL, Cheng Y, Cerniglia GJ, Tuttle SW, Feldman MD, Zhang PJ, Fuchs SY, Diehl JA, Koumenis C. ATF4-dependent induction of heme oxygenase 1 prevents anoikis and promotes metastasis. J Clin Invest. 2015 Jul 1;125(7):2592-608. doi: 10.1172/JCI78031. Epub 2015 May 26. PubMed PMID: 26011642; PubMed Central PMCID: PMC4563676.
- Yu Q, Katlinskaya YV, Carbone CJ, Zhao B, Katlinski KV, Zheng H, Guha M, Li N, Chen Q, Yang T, Lengner CJ, Greenberg RA, Johnson FB, Fuchs SY. DNA-Damage-Induced Type I Interferon Promotes Senescence and Inhibits Stem Cell Function.Cell Rep. 2015 May 5;11(5):785-97. PubMed PMID: 25921537; PubMed Central PMCID: PMC4426031.
- Yu Q, Carbone CJ, Katlinskaya YV, Zheng H, Zheng K, Luo M, Wang PJ, Greenberg RA, Fuchs SY. Type I interferon controls propagation of long interspersed element-1. J Biol Chem. 2015 Apr 17;290(16):10191-9. PubMed PMID: 25716322; PubMed Central PMCID: PMC4400334.
- Maas NL, Diehl JA. Molecular pathways: the PERKs and pitfalls of targeting the unfolded protein response in cancer. Clin Cancer Res. 2015 Feb 15;21(4):675-9. PubMed PMID: 25182515; PubMed Central PMCID: PMC4334714.
- Bhattacharya S, Katlinski KV, Reichert M, Takano S, Brice A, Zhao B, Yu Q, Zheng H, Carbone CJ, Katlinskaya YV, Leu NA, McCorkell KA, Srinivasan S, Girondo M, Rui H, May MJ, Avadhani NG, Rustgi AK, Fuchs SY. Triggering ubiquitination of IFNAR1 protects tissues from inflammatory injury. EMBO Mol Med. 2014 Mar;6(3):384-97.PubMed PMID: 24480543; PubMed Central PMCID: PMC3958312.