Program Official

Principal Investigator

Michael A.
Hollingsworth
Awardee Organization

University Of Nebraska Medical Center
United States

Fiscal Year
2023
Activity Code
U01
Early Stage Investigator Grants (ESI)
Not Applicable
Project End Date

Pancreatic Cancer Detection Consortium

This proposal to continue in the Pancreatic Cancer Detection Consortium will further build and enhance our biospecimen resource that collects longitudinal blood samples on patients at risk of developing pancreatic cancer and unique tissue resources that include rare pancreatic premalignant lesions. We propose to continue and enhance our discovery and validation of blood-based and imaging-based biomarkers that have the potential to detect and differentiate the earliest possible stages of pancreatic lesions that are likely to progress to cancer. This proposal proceeds from an ongoing effort that was initiated 3.5 years ago in which we have enrolled approximately 469 patients with known germline mutations or with significant inherited risk of unknown etiology (more than 2 affected with no defined mutations) for pancreatic cancer. We prospectively collect biological specimens (100 mL blood) and detailed clinical data every six months from an at-risk cohort that represents the target population envisioned for clinical application of biomarkers with potential to detect pancreatic cancer. In addition to patients with inherited risk, we will continue to collect longitudinal samples on groups of patients with increased risk of pancreatic cancer: those with pancreatic cystic neoplasms or chronic pancreatitis, and new onset diabetes (NOD). We also propose three biomarker research specific aims that have grown out of progress during the previous grant award. One aim will build upon our previous results with mucin type biomarkers and related glycoproteins by examining the potential of a set of additional biomarkers to improve detection cancer prior to clinical diagnosis in the earliest stages of disease progression. A second aim will examine the capacity of newly identified antibodies to CEACAM6 to identify earliest lesions in the pancreas by immunohistochemistry and state of the art imaging modalities. A third aim will determine the performance characteristics of a panel of exosome-based biomarkers detecting early pancreatic cancer and differentiating benign cystic lesions from those that progress to cancer.

Publications

  • Froeling FEM, Swamynathan MM, Deschênes A, Chio IIC, Brosnan E, Yao MA, Alagesan P, Lucito M, Li J, Chang AY, Trotman LC, Belleau P, Park Y, Rogoff HA, Watson JD, Tuveson DA. Bioactivation of Napabucasin Triggers Reactive Oxygen Species-Mediated Cancer Cell Death. Clinical cancer research : an official journal of the American Association for Cancer Research. 2019 Dec 1;25(23):7162-7174. Epub 2019 Sep 16. PMID: 31527169
  • Yoo HB, Moon JW, Kim HR, Lee HS, Miyabayashi K, Park CH, Ge S, Zhang A, Tae YK, Sub Y, Park HW, Gee HY, Notta F, Tuveson DA, Bang S, Kim MY, Roe JS. A TEAD2-Driven Endothelial-Like Program Shapes Basal-Like Differentiation and Metastasis of Pancreatic Cancer. Gastroenterology. 2023 Jul;165(1):133-148.e17. Epub 2023 Mar 11. PMID: 36907523
  • Nimmakayala RK, Ogunleye AO, Parte S, Krishna Kumar N, Raut P, Varadharaj V, Perumal NK, Nallasamy P, Rauth S, Cox JL, Lele SM, Batra SK, Ponnusamy MP. PAF1 cooperates with YAP1 in metaplastic ducts to promote pancreatic cancer. Cell death & disease. 2022 Oct 1;13(10):839. PMID: 36180487
  • Gautam SK, Kumar S, Dam V, Ghersi D, Jain M, Batra SK. MUCIN-4 (MUC4) is a novel tumor antigen in pancreatic cancer immunotherapy. Seminars in immunology. 2020 Feb;47:101391. Epub 2020 Jan 14. PMID: 31952903
  • Cannon A, Thompson C, Hall BR, Jain M, Kumar S, Batra SK. Desmoplasia in pancreatic ductal adenocarcinoma: insight into pathological function and therapeutic potential. Genes & cancer. 2018 Mar;9(3-4):78-86. PMID: 30108679
  • Neesse A, Bauer CA, Öhlund D, Lauth M, Buchholz M, Michl P, Tuveson DA, Gress TM. Stromal biology and therapy in pancreatic cancer: ready for clinical translation? Gut. 2019 Jan;68(1):159-171. Epub 2018 Sep 3. PMID: 30177543
  • Dwivedi NV, Datta S, El-Kersh K, Sadikot RT, Ganti AK, Batra SK, Jain M. GPCRs and fibroblast heterogeneity in fibroblast-associated diseases. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2023 Aug;37(8):e23101. PMID: 37486603
  • Kisling SG, Natarajan G, Pothuraju R, Shah A, Batra SK, Kaur S. Implications of prognosis-associated genes in pancreatic tumor metastasis: lessons from global studies in bioinformatics. Cancer metastasis reviews. 2021 Sep;40(3):721-738. Epub 2021 Sep 30. PMID: 34591244
  • Bhatia R, Thompson C, Ganguly K, Singh S, Batra SK, Kumar S. Alcohol and Smoking Mediated Modulations in Adaptive Immunity in Pancreatitis. Cells. 2020 Aug 11;9. (8). PMID: 32796685
  • Wang G, Biswas AK, Ma W, Kandpal M, Coker C, Grandgenett PM, Hollingsworth MA, Jain R, Tanji K, Lόpez-Pintado S, Borczuk A, Hebert D, Jenkitkasemwong S, Hojyo S, Davuluri RV, Knutson MD, Fukada T, Acharyya S. Metastatic cancers promote cachexia through ZIP14 upregulation in skeletal muscle. Nature medicine. 2018 Jun;24(6):770-781. Epub 2018 Jun 6. PMID: 29875463
  • Nallasamy P, Nimmakayala RK, Karmakar S, Leon F, Seshacharyulu P, Lakshmanan I, Rachagani S, Mallya K, Zhang C, Ly QP, Myers MS, Josh L, Grabow CE, Gautam SK, Kumar S, Lele SM, Jain M, Batra SK, Ponnusamy MP. Pancreatic Tumor Microenvironment Factor Promotes Cancer Stemness via SPP1-CD44 Axis. Gastroenterology. 2021 Dec;161(6):1998-2013.e7. Epub 2021 Aug 19. PMID: 34418441
  • Asao T, Tobias GC, Lucotti S, Jones DR, Matei I, Lyden D. Extracellular vesicles and particles as mediators of long-range communication in cancer: connecting biological function to clinical applications. Extracellular vesicles and circulating nucleic acids. 2023 Sep;4(3):461-485. Epub 2023 Aug 16. PMID: 38707985
  • Steele NG, Biffi G, Kemp SB, Zhang Y, Drouillard D, Syu L, Hao Y, Oni TE, Brosnan E, Elyada E, Doshi A, Hansma C, Espinoza C, Abbas A, The S, Irizarry-Negron V, Halbrook CJ, Franks NE, Hoffman MT, Brown K, Carpenter ES, Nwosu ZC, Johnson C, Lima F, Anderson MA, Park Y, Crawford HC, Lyssiotis CA, Frankel TL, Rao A, Bednar F, Dlugosz AA, Preall JB, Tuveson DA, Allen BL, Pasca di Magliano M. Inhibition of Hedgehog Signaling Alters Fibroblast Composition in Pancreatic Cancer. Clinical cancer research : an official journal of the American Association for Cancer Research. 2021 Apr 1;27(7):2023-2037. Epub 2021 Jan 25. PMID: 33495315
  • Carmicheal J, Hayashi C, Huang X, Liu L, Lu Y, Krasnoslobodtsev A, Lushnikov A, Kshirsagar PG, Patel A, Jain M, Lyubchenko YL, Lu Y, Batra SK, Kaur S. Label-free characterization of exosome via surface enhanced Raman spectroscopy for the early detection of pancreatic cancer. Nanomedicine : nanotechnology, biology, and medicine. 2019 Feb;16:88-96. Epub 2018 Dec 11. PMID: 30550805
  • Hoshino A, Kim HS, Bojmar L, Gyan KE, Cioffi M, Hernandez J, Zambirinis CP, Rodrigues G, Molina H, Heissel S, Mark MT, Steiner L, Benito-Martin A, Lucotti S, Di Giannatale A, Offer K, Nakajima M, Williams C, Nogués L, Pelissier Vatter FA, Hashimoto A, Davies AE, Freitas D, Kenific CM, Ararso Y, Buehring W, Lauritzen P, Ogitani Y, Sugiura K, Takahashi N, Alečković M, Bailey KA, Jolissant JS, Wang H, Harris A, Schaeffer LM, García-Santos G, Posner Z, Balachandran VP, Khakoo Y, Raju GP, Scherz A, Sagi I, Scherz-Shouval R, Yarden Y, Oren M, Malladi M, Petriccione M, De Braganca KC, Donzelli M, Fischer C, Vitolano S, Wright GP, Ganshaw L, Marrano M, Ahmed A, DeStefano J, Danzer E, Roehrl MHA, Lacayo NJ, Vincent TC, Weiser MR, Brady MS, Meyers PA, Wexler LH, Ambati SR, Chou AJ, Slotkin EK, Modak S, Roberts SS, Basu EM, Diolaiti D, Krantz BA, Cardoso F, Simpson AL, Berger M, Rudin CM, Simeone DM, Jain M, Ghajar CM, Batra SK, Stanger BZ, Bui J, Brown KA, Rajasekhar VK, Healey JH, de Sousa M, Kramer K, Sheth S, Baisch J, Pascual V, Heaton TE, La Quaglia MP, Pisapia DJ, Schwartz R, Zhang H, Liu Y, Shukla A, Blavier L, DeClerck YA, LaBarge M, Bissell MJ, Caffrey TC, Grandgenett PM, Hollingsworth MA, Bromberg J, Costa-Silva B, Peinado H, Kang Y, Garcia BA, O'Reilly EM, Kelsen D, Trippett TM, Jones DR, Matei IR, Jarnagin WR, Lyden D. Extracellular Vesicle and Particle Biomarkers Define Multiple Human Cancers. Cell. 2020 Aug 20;182(4):1044-1061.e18. Epub 2020 Aug 13. PMID: 32795414
  • Shin SC, Thomas D, Radhakrishnan P, Hollingsworth MA. Invasive phenotype induced by low extracellular pH requires mitochondria dependent metabolic flexibility. Biochemical and biophysical research communications. 2020 Feb 18. Epub 2020 Feb 18. PMID: 32081432
  • Miyabayashi K, Baker LA, Deschênes A, Traub B, Caligiuri G, Plenker D, Alagesan B, Belleau P, Li S, Kendall J, Jang GH, Kawaguchi RK, Somerville TDD, Tiriac H, Hwang CI, Burkhart RA, Roberts NJ, Wood LD, Hruban RH, Gillis J, Krasnitz A, Vakoc CR, Wigler M, Notta F, Gallinger S, Park Y, Tuveson DA. Intraductal Transplantation Models of Human Pancreatic Ductal Adenocarcinoma Reveal Progressive Transition of Molecular Subtypes. Cancer discovery. 2020 Oct;10(10):1566-1589. Epub 2020 Jul 23. PMID: 32703770
  • Xu PC, You M, Yu SY, Luan Y, Eldani M, Caffrey TC, Grandgenett PM, O'Connell KA, Shukla SK, Kattamuri C, Hollingsworth MA, Singh PK, Thompson TB, Chung S, Kim SY. Visceral adipose tissue remodeling in pancreatic ductal adenocarcinoma cachexia: the role of activin A signaling. Scientific reports. 2022 Jan 31;12(1):1659. PMID: 35102236
  • Karmakar S, Rauth S, Nallasamy P, Perumal N, Nimmakayala RK, Leon F, Gupta R, Barkeer S, Venkata RC, Raman V, Rachagani S, Ponnusamy MP, Batra SK. RNA Polymerase II-Associated Factor 1 Regulates Stem Cell Features of Pancreatic Cancer Cells, Independently of the PAF1 Complex, via Interactions With PHF5A and DDX3. Gastroenterology. 2020 Nov;159(5):1898-1915.e6. Epub 2020 Aug 8. PMID: 32781084
  • Lucotti S, Kenific CM, Zhang H, Lyden D. Extracellular vesicles and particles impact the systemic landscape of cancer. The EMBO journal. 2022 Sep 15;41(18):e109288. Epub 2022 Sep 2. PMID: 36052513
  • Napoleon JV, Sagar S, Kubica SP, Boghean L, Kour S, King HM, Sonawane YA, Crawford AJ, Gautam N, Kizhake S, Bialk PA, Kmiec E, Mallareddy JR, Patil PP, Rana S, Singh S, Prahlad J, Grandgenett PM, Borgstahl GEO, Ghosal G, Alnouti Y, Hollingsworth MA, Radhakrishnan P, Natarajan A. Small-molecule IKKβ activation modulator (IKAM) targets MAP3K1 and inhibits pancreatic tumor growth. Proceedings of the National Academy of Sciences of the United States of America. 2022 May 3;119(18):e2115071119. Epub 2022 Apr 27. PMID: 35476515
  • Biffi G, Tuveson DA. Diversity and Biology of Cancer-Associated Fibroblasts. Physiological reviews. 2021 Jan 1;101(1):147-176. Epub 2020 May 28. PMID: 32466724
  • Gautam SK, Khan P, Natarajan G, Atri P, Aithal A, Ganti AK, Batra SK, Nasser MW, Jain M. Mucins as Potential Biomarkers for Early Detection of Cancer. Cancers. 2023 Mar 7;15. (6). PMID: 36980526
  • Humpton TJ, Alagesan B, DeNicola GM, Lu D, Yordanov GN, Leonhardt CS, Yao MA, Alagesan P, Zaatari MN, Park Y, Skepper JN, Macleod KF, Perez-Mancera PA, Murphy MP, Evan GI, Vousden KH, Tuveson DA. Oncogenic KRAS Induces NIX-Mediated Mitophagy to Promote Pancreatic Cancer. Cancer discovery. 2019 Sep;9(9):1268-1287. Epub 2019 Jul 1. PMID: 31263025
  • Rauth S, Ganguly K, Atri P, Parte S, Nimmakayala RK, Varadharaj V, Nallasamy P, Vengoji R, Ogunleye AO, Lakshmanan I, Chirravuri R, Bessho M, Cox JL, Foster JM, Talmon GA, Bessho T, Ganti AK, Batra SK, Ponnusamy MP. Elevated PAF1-RAD52 axis confers chemoresistance to human cancers. Cell reports. 2023 Feb 28;42(2):112043. Epub 2023 Jan 28. PMID: 36709426
  • Vance K, Alitinok A, Winfree S, Jensen-Smith H, Swanson BJ, Grandgenett PM, Klute KA, Crichton DJ, Hollingsworth MA. Machine learning analyses of highly-multiplexed immunofluorescence identifies distinct tumor and stromal cell populations in primary pancreatic tumors. Cancer biomarkers : section A of Disease markers. 2022;33(2):219-235. PMID: 35213363
  • Mundry CS, Eberle KC, Singh PK, Hollingsworth MA, Mehla K. Local and systemic immunosuppression in pancreatic cancer: Targeting the stalwarts in tumor's arsenal. Biochimica et biophysica acta. Reviews on cancer. 2020 Aug;1874(1):188387. Epub 2020 Jun 21. PMID: 32579889
  • Bhatia R, Thompson CM, Clement EJ, Ganguly K, Cox JL, Rauth S, Siddiqui JA, Mashiana SS, Jain M, Wyatt TA, Mashiana HS, Singh S, Woods NT, Kharbanda KK, Batra SK, Kumar S. Malondialdehyde-Acetaldehyde Extracellular Matrix Protein Adducts Attenuate Unfolded Protein Response During Alcohol and Smoking-Induced Pancreatitis. Gastroenterology. 2022 Oct;163(4):1064-1078.e10. Epub 2022 Jul 3. PMID: 35788346
  • Amor C, Fernández-Maestre I, Chowdhury S, Ho YJ, Nadella S, Graham C, Carrasco SE, Nnuji-John E, Feucht J, Hinterleitner C, Barthet VJA, Boyer JA, Mezzadra R, Wereski MG, Tuveson DA, Levine RL, Jones LW, Sadelain M, Lowe SW. Prophylactic and long-lasting efficacy of senolytic CAR T cells against age-related metabolic dysfunction. Nature aging. 2024 Mar;4(3):336-349. Epub 2024 Jan 24. PMID: 38267706
  • Bhatia R, Siddiqui JA, Ganguly K, Thompson CM, Cannon A, Aithal A, Perumal N, Maurya SK, Li X, Cox JL, Gurumurthy CB, Rachagani S, Jain M, Nasser MW, Batra SK, Kumar S. Muc4 loss mitigates epidermal growth factor receptor activity essential for PDAC tumorigenesis. Oncogene. 2023 Mar;42(10):759-770. Epub 2023 Jan 9. PMID: 36624189
  • Baker LA, Tiriac H, Tuveson DA. Generation and Culture of Human Pancreatic Ductal Adenocarcinoma Organoids from Resected Tumor Specimens. Methods in molecular biology (Clifton, N.J.). 2019;1882:97-115. PMID: 30378047
  • Baker LA, Tuveson DA. Generation and Culture of Tumor and Metastatic Organoids from Murine Models of Pancreatic Ductal Adenocarcinoma. Methods in molecular biology (Clifton, N.J.). 2019;1882:117-133. PMID: 30378048
  • Caffrey T, Sagar S, Thomas D, Lewallen ME, Hollingsworth MA, Radhakrishnan P. The glycoprotein mucin-1 negatively regulates GalNAc transferase 5 expression in pancreatic cancer. FEBS letters. 2019 Oct;593(19):2751-2761. Epub 2019 Jul 21. PMID: 31283009
  • Aithal A, Rauth S, Kshirsagar P, Shah A, Lakshmanan I, Junker WM, Jain M, Ponnusamy MP, Batra SK. MUC16 as a novel target for cancer therapy. Expert opinion on therapeutic targets. 2018 Aug;22(8):675-686. Epub 2018 Jul 26. PMID: 29999426
  • Zhang H, Freitas D, Kim HS, Fabijanic K, Li Z, Chen H, Mark MT, Molina H, Martin AB, Bojmar L, Fang J, Rampersaud S, Hoshino A, Matei I, Kenific CM, Nakajima M, Mutvei AP, Sansone P, Buehring W, Wang H, Jimenez JP, Cohen-Gould L, Paknejad N, Brendel M, Manova-Todorova K, Magalhães A, Ferreira JA, Osório H, Silva AM, Massey A, Cubillos-Ruiz JR, Galletti G, Giannakakou P, Cuervo AM, Blenis J, Schwartz R, Brady MS, Peinado H, Bromberg J, Matsui H, Reis CA, Lyden D. Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation. Nature cell biology. 2018 Mar;20(3):332-343. Epub 2018 Feb 19. PMID: 29459780
  • Nimmakayala RK, Rauth S, Chirravuri Venkata R, Marimuthu S, Nallasamy P, Vengoji R, Lele SM, Rachagani S, Mallya K, Malafa MP, Ponnusamy MP, Batra SK. PGC1α-Mediated Metabolic Reprogramming Drives the Stemness of Pancreatic Precursor Lesions. Clinical cancer research : an official journal of the American Association for Cancer Research. 2021 Oct 1;27(19):5415-5429. PMID: 34172498
  • Pelissier Vatter FA, Cioffi M, Hanna SJ, Castarede I, Caielli S, Pascual V, Matei I, Lyden D. Extracellular vesicle- and particle-mediated communication shapes innate and adaptive immune responses. The Journal of experimental medicine. 2021 Aug 2;218. (8). Epub 2021 Jun 28. PMID: 34180950
  • Gautam SK, Basu S, Aithal A, Dwivedi NV, Gulati M, Jain M. Regulation of pancreatic cancer therapy resistance by chemokines. Seminars in cancer biology. 2022 Nov;86(Pt 2):69-80. Epub 2022 Sep 2. PMID: 36064086
  • Elyada E, Bolisetty M, Laise P, Flynn WF, Courtois ET, Burkhart RA, Teinor JA, Belleau P, Biffi G, Lucito MS, Sivajothi S, Armstrong TD, Engle DD, Yu KH, Hao Y, Wolfgang CL, Park Y, Preall J, Jaffee EM, Califano A, Robson P, Tuveson DA. Cross-Species Single-Cell Analysis of Pancreatic Ductal Adenocarcinoma Reveals Antigen-Presenting Cancer-Associated Fibroblasts. Cancer discovery. 2019 Aug;9(8):1102-1123. Epub 2019 Jun 13. PMID: 31197017
  • Engle DD, Tiriac H, Rivera KD, Pommier A, Whalen S, Oni TE, Alagesan B, Lee EJ, Yao MA, Lucito MS, Spielman B, Da Silva B, Schoepfer C, Wright K, Creighton B, Afinowicz L, Yu KH, Grützmann R, Aust D, Gimotty PA, Pollard KS, Hruban RH, Goggins MG, Pilarsky C, Park Y, Pappin DJ, Hollingsworth MA, Tuveson DA. The glycan CA19-9 promotes pancreatitis and pancreatic cancer in mice. Science (New York, N.Y.). 2019 Jun 21;364(6446):1156-1162. PMID: 31221853
  • Liu Y, Kaur S, Huang Y, Fahrmann JF, Rinaudo JA, Hanash SM, Batra SK, Singhi AD, Brand RE, Maitra A, Haab BB. Biomarkers and Strategy to Detect Preinvasive and Early Pancreatic Cancer: State of the Field and the Impact of the EDRN. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2020 Dec;29(12):2513-2523. Epub 2020 Jun 12. PMID: 32532830
  • Tiriac H, Plenker D, Baker LA, Tuveson DA. Organoid models for translational pancreatic cancer research. Current opinion in genetics & development. 2019 Feb;54:7-11. Epub 2019 Mar 4. PMID: 30844513
  • Kehrberg RJ, Bhyravbhatla N, Batra SK, Kumar S. Epigenetic regulation of cancer-associated fibroblast heterogeneity. Biochimica et biophysica acta. Reviews on cancer. 2023 May;1878(3):188901. Epub 2023 Apr 28. PMID: 37120098
  • Cannon A, Thompson CM, Maurer HC, Atri P, Bhatia R, West S, Ghersi D, Olive KP, Kumar S, Batra SK. CXCR3 and Cognate Ligands are Associated with Immune Cell Alteration and Aggressiveness of Pancreatic Ductal Adenocarcinoma. Clinical cancer research : an official journal of the American Association for Cancer Research. 2020 Nov 15;26(22):6051-6063. Epub 2020 Sep 1. PMID: 32873571
  • Belleau P, Deschênes A, Chambwe N, Tuveson DA, Krasnitz A. Genetic Ancestry Inference from Cancer-Derived Molecular Data across Genomic and Transcriptomic Platforms. Cancer research. 2023 Jan 4;83(1):49-58. PMID: 36351074
  • Barkeer S, Chugh S, Karmakar S, Kaushik G, Rauth S, Rachagani S, Batra SK, Ponnusamy MP. Novel role of O-glycosyltransferases GALNT3 and B3GNT3 in the self-renewal of pancreatic cancer stem cells. BMC cancer. 2018 Nov 22;18(1):1157. PMID: 30466404
  • Tuveson D, Clevers H. Cancer modeling meets human organoid technology. Science (New York, N.Y.). 2019 Jun 7;364(6444):952-955. PMID: 31171691
  • Dalal V, Carmicheal J, Dhaliwal A, Jain M, Kaur S, Batra SK. Radiomics in stratification of pancreatic cystic lesions: Machine learning in action. Cancer letters. 2020 Jan 28;469:228-237. Epub 2019 Oct 17. PMID: 31629933
  • Tian C, Öhlund D, Rickelt S, Lidström T, Huang Y, Hao L, Zhao RT, Franklin O, Bhatia SN, Tuveson DA, Hynes RO. Cancer Cell-Derived Matrisome Proteins Promote Metastasis in Pancreatic Ductal Adenocarcinoma. Cancer research. 2020 Apr 1;80(7):1461-1474. Epub 2020 Feb 6. PMID: 32029550
  • Bhatia R, Bhyravbhatla N, Kisling A, Li X, Batra SK, Kumar S. Cytokines chattering in pancreatic ductal adenocarcinoma tumor microenvironment. Seminars in cancer biology. 2022 Nov;86(Pt 2):499-510. Epub 2022 Mar 26. PMID: 35346801
  • Nimmakayala RK, Batra SK, Ponnusamy MP. Unraveling the journey of cancer stem cells from origin to metastasis. Biochimica et biophysica acta. Reviews on cancer. 2019 Jan;1871(1):50-63. Epub 2018 Nov 9. PMID: 30419314
  • Ganguly K, Shah A, Atri P, Rauth S, Ponnusamy MP, Kumar S, Batra SK. Chemokine-mucinome interplay in shaping the heterogeneous tumor microenvironment of pancreatic cancer. Seminars in cancer biology. 2022 Nov;86(Pt 2):511-520. Epub 2022 Mar 26. PMID: 35346803
  • Xu J, Roe JS, Lee E, Tonelli C, Ji KY, Younis OW, Somervile TDD, Yao M, Milazzo JP, Tiriac H, Kolarzyk AM, Lee E, Grem JL, Lazenby AJ, Grunkemeyer JA, Hollingsworth MA, Grandgenett PM, Borowsky AD, Park Y, Vakoc CR, Tuveson DA, Hwang CI. Engrailed-1 Promotes Pancreatic Cancer Metastasis. Advanced science (Weinheim, Baden-Wurttemberg, Germany). 2024 Feb;11(6):e2308537. Epub 2023 Dec 18. PMID: 38110836
  • Chugh S, Barkeer S, Rachagani S, Nimmakayala RK, Perumal N, Pothuraju R, Atri P, Mahapatra S, Thapa I, Talmon GA, Smith LM, Yu X, Neelamegham S, Fu J, Xia L, Ponnusamy MP, Batra SK. Disruption of C1galt1 Gene Promotes Development and Metastasis of Pancreatic Adenocarcinomas in Mice. Gastroenterology. 2018 Nov;155(5):1608-1624. Epub 2018 Aug 4. PMID: 30086262
  • Rauth S, Karmakar S, Shah A, Seshacharyulu P, Nimmakayala RK, Ganguly K, Bhatia R, Muniyan S, Kumar S, Dutta S, Lin C, Datta K, Batra SK, Ponnusamy MP. SUMO Modification of PAF1/PD2 Enables PML Interaction and Promotes Radiation Resistance in Pancreatic Ductal Adenocarcinoma. Molecular and cellular biology. 2021 Nov 22;41(12):e0013521. Epub 2021 Sep 27. PMID: 34570619
  • Shi Y, Gao W, Lytle NK, Huang P, Yuan X, Dann AM, Ridinger-Saison M, DelGiorno KE, Antal CE, Liang G, Atkins AR, Erikson G, Sun H, Meisenhelder J, Terenziani E, Woo G, Fang L, Santisakultarm TP, Manor U, Xu R, Becerra CR, Borazanci E, Von Hoff DD, Grandgenett PM, Hollingsworth MA, Leblanc M, Umetsu SE, Collisson EA, Scadeng M, Lowy AM, Donahue TR, Reya T, Downes M, Evans RM, Wahl GM, Pawson T, Tian R, Hunter T. Targeting LIF-mediated paracrine interaction for pancreatic cancer therapy and monitoring. Nature. 2019 May;569(7754):131-135. Epub 2019 Apr 17. PMID: 30996350
  • Jahan R, Ganguly K, Smith LM, Atri P, Carmicheal J, Sheinin Y, Rachagani S, Natarajan G, Brand RE, Macha MA, Grandgenett PM, Kaur S, Batra SK. Trefoil factor(s) and CA19.9: A promising panel for early detection of pancreatic cancer. EBioMedicine. 2019 Apr;42:375-385. Epub 2019 Apr 5. PMID: 30956167
  • Ponz-Sarvise M, Corbo V, Tiriac H, Engle DD, Frese KK, Oni TE, Hwang CI, Öhlund D, Chio IIC, Baker LA, Filippini D, Wright K, Bapiro TE, Huang P, Smith P, Yu KH, Jodrell DI, Park Y, Tuveson DA. Identification of Resistance Pathways Specific to Malignancy Using Organoid Models of Pancreatic Cancer. Clinical cancer research : an official journal of the American Association for Cancer Research. 2019 Nov 15;25(22):6742-6755. Epub 2019 Sep 6. PMID: 31492749
  • Saxena S, Molczyk C, Purohit A, Ehrhorn E, Goel P, Prajapati DR, Atri P, Kaur S, Grandgenett PM, Hollingsworth MA, Batra SK, Singh RK. Differential expression profile of CXC-receptor-2 ligands as potential biomarkers in pancreatic ductal adenocarcinoma. American journal of cancer research. 2022 Jan 15;12(1):68-90. eCollection 2022. PMID: 35141005
  • Tonelli C, Yordanov GN, Hao Y, Deschênes A, Hinds J, Belleau P, Klingbeil O, Brosnan E, Doshi A, Park Y, Hruban RH, Vakoc CR, Dobin A, Preall J, Tuveson DA. A mucus production programme promotes classical pancreatic ductal adenocarcinoma. Gut. 2024 May 10;73(6):941-954. PMID: 38262672
  • Siddiqui JA, Pothuraju R, Jain M, Batra SK, Nasser MW. Advances in cancer cachexia: Intersection between affected organs, mediators, and pharmacological interventions. Biochimica et biophysica acta. Reviews on cancer. 2020 Apr;1873(2):188359. Epub 2020 Mar 25. PMID: 32222610
  • Lenkiewicz E, Malasi S, Hogenson TL, Flores LF, Barham W, Phillips WJ, Roesler AS, Chambers KR, Rajbhandari N, Hayashi A, Antal CE, Downes M, Grandgenett PM, Hollingsworth MA, Cridebring D, Xiong Y, Lee JH, Ye Z, Yan H, Hernandez MC, Leiting JL, Evans RM, Ordog T, Truty MJ, Borad MJ, Reya T, Von Hoff DD, Fernandez-Zapico ME, Barrett MT. Genomic and Epigenomic Landscaping Defines New Therapeutic Targets for Adenosquamous Carcinoma of the Pancreas. Cancer research. 2020 Oct 15;80(20):4324-4334. Epub 2020 Sep 14. PMID: 32928922
  • Marimuthu S, Rauth S, Ganguly K, Zhang C, Lakshmanan I, Batra SK, Ponnusamy MP. Mucins reprogram stemness, metabolism and promote chemoresistance during cancer progression. Cancer metastasis reviews. 2021 Jun;40(2):575-588. Epub 2021 Apr 4. PMID: 33813658
  • Ogunleye AO, Nimmakayala RK, Batra SK, Ponnusamy MP. Metabolic Rewiring and Stemness: A Critical Attribute of Pancreatic Cancer Progression. Stem cells (Dayton, Ohio). 2023 May 15;41(5):417-430. PMID: 36869789
  • Demyan L, Habowski AN, Plenker D, King DA, Standring OJ, Tsang C, St Surin L, Rishi A, Crawford JM, Boyd J, Pasha SA, Patel H, Galluzzo Z, Metz C, Gregersen PK, Fox S, Valente C, Abadali S, Matadial-Ragoo S, DePeralta DK, Deutsch GB, Herman JM, Talamini MA, Tuveson DA, Weiss MJ. Pancreatic Cancer Patient-derived Organoids Can Predict Response to Neoadjuvant Chemotherapy. Annals of surgery. 2022 Sep 1;276(3):450-462. Epub 2022 Jun 27. PMID: 35972511
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  • Dasgupta A, Shukla SK, Vernucci E, King RJ, Abrego J, Mulder SE, Mullen NJ, Graves G, Buettner K, Thakur R, Murthy D, Attri KS, Wang D, Chaika NV, Pacheco CG, Rai I, Engle DD, Grandgenett PM, Punsoni M, Reames BN, Teoh-Fitzgerald M, Oberley-Deegan R, Yu F, Klute KA, Hollingsworth MA, Zimmerman MC, Mehla K, Sadoshima J, Tuveson DA, Singh PK. SIRT1-NOX4 signaling axis regulates cancer cachexia. The Journal of experimental medicine. 2020 Jul 6;217. (7). PMID: 32441762
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  • Gupta R, Leon F, Rauth S, Batra SK, Ponnusamy MP. A Systematic Review on the Implications of O-linked Glycan Branching and Truncating Enzymes on Cancer Progression and Metastasis. Cells. 2020 Feb 14;9. (2). PMID: 32075174
  • Carmicheal J, Atri P, Sharma S, Kumar S, Chirravuri Venkata R, Kulkarni P, Salgia R, Ghersi D, Kaur S, Batra SK. Presence and structure-activity relationship of intrinsically disordered regions across mucins. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2020 Feb;34(2):1939-1957. Epub 2020 Jan 5. PMID: 31908009
  • Carmicheal J, Patel A, Dalal V, Atri P, Dhaliwal AS, Wittel UA, Malafa MP, Talmon G, Swanson BJ, Singh S, Jain M, Kaur S, Batra SK. Elevating pancreatic cystic lesion stratification: Current and future pancreatic cancer biomarker(s). Biochimica et biophysica acta. Reviews on cancer. 2020 Jan;1873(1):188318. Epub 2019 Oct 30. PMID: 31676330
  • Nallasamy P, Nimmakayala RK, Parte S, Are AC, Batra SK, Ponnusamy MP. Tumor microenvironment enriches the stemness features: the architectural event of therapy resistance and metastasis. Molecular cancer. 2022 Dec 22;21(1):225. PMID: 36550571
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  • Thomas D, Sagar S, Liu X, Lee HR, Grunkemeyer JA, Grandgenett PM, Caffrey T, O'Connell KA, Swanson B, Marcos-Silva L, Steentoft C, Wandall HH, Maurer HC, Peng XL, Yeh JJ, Qiu F, Yu F, Madiyalakan R, Olive KP, Mandel U, Clausen H, Hollingsworth MA, Radhakrishnan P. Isoforms of MUC16 activate oncogenic signaling through EGF receptors to enhance the progression of pancreatic cancer. Molecular therapy : the journal of the American Society of Gene Therapy. 2021 Apr 7;29(4):1557-1571. Epub 2020 Dec 25. PMID: 33359791
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  • Oni TE, Biffi G, Baker LA, Hao Y, Tonelli C, Somerville TDD, Deschênes A, Belleau P, Hwang CI, Sánchez-Rivera FJ, Cox H, Brosnan E, Doshi A, Lumia RP, Khaledi K, Park Y, Trotman LC, Lowe SW, Krasnitz A, Vakoc CR, Tuveson DA. SOAT1 promotes mevalonate pathway dependency in pancreatic cancer. The Journal of experimental medicine. 2020 Sep 7;217. (9). PMID: 32633781
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