Tushar D. Bhagat

Tushar D. Bhagat, Ph.D.

  • Research Assistant Professor, Department of Oncology (Medical Oncology)

Area of research

  • A) Epigenetics of tumor microenvironment B] Stress Reduction Programs at Einstein: 1) 3-week Stress Reduction Program using mindfulness & 2) Mindfulness Based Stress Reduction (MBSR) 8-week course

Email

Location

  • Albert Einstein College of Medicine Jack and Pearl Resnick Campus 1300 Morris Park Avenue Bronx, NY 10461

Lab of Tushar D. Bhagat

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Research Profiles

Research Profiles

Research Profiles

Professional Interests

 

 

1]

Pancreatic Cancer-Associated Fibroblast formation is regulated by epigenetic reprogramming through lactate (eLife 2019)

2]

Epigenetically Aberrant Stroma in MDS Propagates Disease via Wnt/β-Catenin Activation (JBC 2017)

3]

Notch Pathway Is Activated via Genetic and Epigenetic Alterations and Is a Therapeutic Target in Clear Cell Renal Cancer (Cancer Research, 2017)

4]

Hypomethylation of noncoding DNA regions and overexpression of the long noncoding RNA, AFAP1-AS1, in Barrett's esophagus & esophageal adenocarcinoma, (Gastroenterology, 2012)

5]

Scientifically evaluated (Clinical-trial tested) Online Stress Reduction Programs for Einstein-Montefiore community.

 

 

 

1]

Pancreatic Cancer-associated Fibroblast formation is regulated by epigenetic reprogramming through lactate:

 

Pancreatic ductal adenocarcinoma (PDAC) is known to be influenced by fibrosis due to stromal cell proliferation. However, the molecular mechanism of cancer associated fibroblasts (CAFs) formation is not clear. Through the genome wide epigenetic analysis of CAFs obtained from patients and through in vitro conditioning, we found that there is a loss of cytosine methylation across the genome that led to overexpression of inflammatory cytokines such as CXCR4. The cancer cells demonstrated increased invasiveness when co-cultured with CAFs that was reversed via the inhibition of CXCR4. The lactate produced by cancer cells seemed to result in mesenchymal stem cells (MSCs) showing increase in alpha-ketoglutarate (aKG) within them. aKG facilitated the increase in hydroxymethylation and decrease in methylation via the TET enzymes while the MSCs transformed into CAFs in vitro. Mice co-injected with cancer cells and TET deficient MSCs demonstrated decreased tumor growth. Therefore PDAC exhibits epigenetic reprograming during CAF transformation that is associated with increased lactate from the tumor cells.

 

2]

Epigenetically Aberrant Stroma in MDS Propagates Disease via Wnt/β-Catenin Activation:

 

Other researchers have explored how the microenvironment within bone marrow influences lymphoma and other forms of malignant hematopoiesis – cancers derived from blood cells. But this paper is the first to explore how the epigenetics (DNA methylation) in that microenvironment (stroma) influences advancement to leukemia. Our results define previously unknown epigenetic changes in the bone marrow stroma that lead to the progression of pre-cancerous myelodysplastic syndrome (MDS) into acute myeloid leukemia (AML). Specifically, we focused on the poorly understood role of bone marrow stroma cells in regulating clinical responses to a set of DNA-regulators known as DNA methyltransferase inhibitors (DNMTi). A major finding of this study was that the cyticines in the DNA of these stroma from untreated MDS patients were aberrantly hypermethylated (too much methylation) in the regions of the DNA that are rich in cytosine-guanine (CG) nucleotides that are sites of epigenetic regulation. But the stroma from MDS patients that were treated with the DNA methyltransferase inhibitor 5-azacytidine (a drug used in the clinic for MDS treatment) did not show the aberrant methylation pattern and these stroma supported healthy development of red blood cells ( a major issue with MDS patients). The aberrant methylation in MDS patients suppress a negative regulator of Wnt/β-Catenin signaling pathway, FRZB, which leads to hyper activation of this pathway leading to progression to leukemia. Significance: Growing the bone marrow stromal cells from MDS patient bone marrow itself is a significant technical feat in scientific research, something that is very difficult to do, let alone studying these stromal cells. This study furthers the understanding the development and progression of MDS to leukemia due to the support from the ‘healthy’ bone marrow stromal cells and how that mutually cooperative interaction can be intercepted by a DNMTi drugs.

 

3]

Notch Pathway Is Activated via Genetic and Epigenetic Alterations and Is a Therapeutic Target in Clear Cell Renal Cancer

 

Clear cell renal cell carcinoma (CCRCC) is an incurable form of kidney cancer once it is in an advanced stage. One of the causes of kidney cancer is activation of the NOTCH pathway (as shown in patients cancer tissue gene expression analysis). This pathway is activated genetically because of deletion of the VHL gene leading to hyperproliferation of kidney tubule cells. Additionally the epigenetic mechanism that triggers JAGGED2 is via loss of methylation of H3Kme1 gene region, which leads to the overactivation of the NOTCH pathway.  In other words, JAGGED2 sets off the chain reaction along the NOTCH pathway that leads to development of CCCRCC. Current therapies do not allow for selective re-methylation, so our therapeutic response is limited to attempts at directly inhibiting the hyperactivated JAGGED2. We showed that the existing γ-secretase inhibitor LY3039478 could be applied in such manner to inhibit the NOTCH pathway in order to arrest the progression of renal cancer. SIGNIFICANCE: This study shows the cause of kidney cancer to be NOTCH pathway activation. Demonstrates the genetic and epigenetic mechanism of the activation and therefore provides a therapeutic target (γ-secretase) and proposes an effective drug LY3039478 already in clinical trial for treatment of CCRCC.

 

4]

Hypomethylation of noncoding DNA regions and overexpression of the long noncoding RNA, AFAP1-AS1, in Barrett's esophagus and esophageal adenocarcinoma:

 

Normally, RNA’s function is gene translation, but this paper showed how one of RNA's secondary or additional roles in gene expression regulation in cancer development works. While the existence of this additional function was already documented, its mechanism was not understood. This paper showed that the mechanism is methylation. Reductions in methylation of a long non coding (lncRNA) AFAP-AS1 in both pre-cancerous Barrett's esophagus (BE) and esophageal adenocarcinoma (EAC), in their coding and noncoding regions of the genome was seen in patient biopsies. While dysregulation of noncoding RNAs is known to occur during carcinogenesis, it has never been studied in the transition from BE to EAC. Using high-resolution methylome and transcriptome analysis, we showed that RNA AFAP1-AS1 is overexpressed in BE and EAC compared to normal esophageal tissue facilitates cancer-related biologic functions of EAC cells including their increased proliferation, cell migration and invasion. Significance: Currently the available therapeutic outcomes for EAC patients are very grim while current treatment regimens are relatively ineffective, as EAC cannot be detected early enough. When EAC is diagnosed it is already spread and metastasized and therefore very difficult to treat. This study will help Doctors to use AFAP1-AS1 expression and methylation patternas a biomarker for EAC and therefore help in the early detection and better treatment of EAC.

 

5]

Scientifically evaluated (Clinical-trial tested) Online Stress Reduction Programs for Einstein-Montefiore community.

 

MBSR is a scientifically & medically (through clinical trials) tested 8-week program that combines techniques such as mindfulness meditation, yoga, and interpersonal relational activities. Besides helping us connect with ourselves & others better, it has been proven to be helpful in improving immune and cognitive function; reducing stress, anxiety, depression, chronic pain and alleviating multiple other health conditions. Over 40 years of research on MBSR has shown how it can empower an individual to develop/strengthen the ability to manage several other physical and mental challenges thereby increasing well-being and happiness in life.

 

Course structure (two types of courses)

 

A] 3-week Course: Stress Reduction by Mindfulness

 

‣An Program based on MBSR

‣ Pre-requisite: Requires Introductory Session Attendance

‣ Format: Online on ZOOM (total time: ~17 hrs worth with home practice)

‣ Duration: Three weeks, 2.5 hr sessions each with 2 course cycle options.

Course Cycle 1: Tuesdays, June 23rd, 30th, & July7th 7:00-9:30 pm

Course Cycle 2: Thursdays, June 25th,  July 2nd, & 9th 7:00-9:30 pm

‣ Daily practice: ~30 mins simple daily home practice between the sessions

‣ Support: Contact Facilitator during course via texts, emails & phone calls.

‣ Join an introductory session by signing-up here

 

B] Actual 8-week MBSR complete Course

 

‣ Format: Online on zoom (total time: ~44 hrs worth with home practice)

‣Weekly 2.5 hour interactive and didactic group class

‣Duration: 8-weeks, 2.5 hr sessions each with 2 course cycle options.

Course Cycle 1: Tuesdays, June 23rd to August 11th 7:00-9:30 pm

Course Cycle 2: Thursdays, June 25th to August 13th 7:00-9:30 pm

‣30-60 min simple daily assignments

‣ Support: Contact Facilitator during course via texts, emails & phone calls.

‣ Join an introductory session by signing-up heres

 

Selected Publications

 

  1. Bhagat TD, Ahrens DV, Dawlaty M, Zou Y, Baddour J, Achreja A, Zhao H, Yang L, Patel B, Kang C, Choudhary G, Gordon-Mitchell S, Aluri S, Bhattacharyya S, Sahu S, Yu Y, Bartenstein M, Giricz O, Suzuki M, Sohal D, Gupta S, Guerrero PA, Batra S, Goggins M, Steidl U, Greally J, Agarwal B, Pradhan K, Banerjee D, Nagrath D, Maitra A, Verma A. “Lactate-mediated epigenetic reprogramming regulates formation of human pancreatic cancer-associated fibroblasts.” eLife 2019 (manuscript accepted)
  2. Bhagat TD, Chen S, Bartenstein M, Barlowe AT, Von Ahrens D, Choudhary GS, Tivnan P, Amin E, Marcondes AM, Sanders MA, Hoogenboezem RM, Kambhampati S, Ramachandra N, Mantzaris I, Sukrithan V, Laurence R, Lopez R, Bhagat P, Giricz O, Sohal D, Wickrema A, Yeung C, Gritsman K, Aplan P, Hochedlinger K, Yu Y, Pradhan K, Zhang J, Greally JM, Mukherjee S, Pellagatti A, Boultwood J, Will B, Steidl U, Raaijmakers MHGP, Deeg HJ, Kharas MG, Verma A. 2017, “Epigenetically Aberrant Stroma in MDS Propagates Disease via Wnt/β-Catenin Activation.” Cancer Res.  77(18):4846-4857.
  3. Bhagat TD, Zou Y, Huang S, Park J, Palmer MB, Hu C, Li W, Shenoy N, Giricz O, Choudhary G, Yu Y, Ko YA, Izquierdo MC, Park ASD, Vallumsetla N, Laurence R, Lopez R, Suzuki M, Pullman J, Kaner J, Gartrell B, Hakimi AA, Greally JM, Patel B, Benhadji K, Pradhan K, Verma A, Susztak K. (2017) “Notch Pathway Is Activated via Genetic and Epigenetic Alterations and Is a Therapeutic Target in Clear Cell Renal Cancer.” J Biol Chem. 292(3): 837–846.
  4. Bhagat TD*, Zhou L*, Sokol L*, Kessel R, Caceres G, Gundabolu K, Tamari R, Gordon S, Mantzaris I, Jodlowski T, Yu Y, Jing X, Polineni R, Bhatia K, Pellagatti A, Boultwood J, Kambhampati S, Steidl U, Stein C, Ju W, Liu G, Kenny P, List A, Bitzer M, Verma A. (2013) “miR-21 mediates hematopoietic suppression in MDS by activating TGF-β signaling” Blood. 121(15):2875-81 (*joint first author)
  5. Wu W*, Bhagat TD*, Yang X, Song JH, Cheng Y, Agarwal R, Abraham JM, Ibrahim S, Bartenstein M, Hussain Z, Suzuki M, Yu Y, Chen W, Eng C, Greally J, Verma A, Meltzer SJ. (2013) “Hypomethylation of noncoding DNA regions and overexpression of the long noncoding RNA, AFAP1-AS1, in Barrett's esophagus and esophageal adenocarcinoma.”  Gastroenterology. 144(5):956-966. (*Joint first author)
  6. Sridharan A, Schinke CD, Georgiev G, Silva Ferreira MD, Victor Thiruthuvanathan V, MacArthur I, Bhagat TD, Choudhary G, Alluri S, Chen J, Pradhan K, Xia Y, Panjikaran M, Sims G, Bhagat CK, Bender R, Keeler L, Graber A, Heuck C, Fletcher FA, Alapat D, Weinhold N, Johnson SK, Wickrema A, Barlogie B, Morgan GJ, Steidl UG, Will B, Verma A. Stem Cell Mutations Can be Detected in Myeloma Patients Years before Onset of Secondary Leukemias. Blood Advances 2019 (manuscript accepted)
  7. Bowler TG, Pradhan K, Kong Y, Bartenstein M, Morrone KA, Sridharan A, Kessel RM, Shastri A, Giricz O1, Bhagat TD, Gordon-Mitchell S, Rohanizadegan M, Hooda L, Datt I, Przychodzen BP, Parmar S, Maqbool S, Maciejewski JP, Steidl U, Greally JM, Verma A. (2019) “Misidentification of MLL3 and other mutations in cancer due to highly homologous genomic regions.” Leukemia Lymphoma. 2019 Jul 10:1-6. doi: 10.1080/10428194.2019.1630620. [Epub ahead of print]
  8. Smith MA, Choudhary GS, Pellagatti A, Choi K, Bolanos LC, Bhagat TD, Gordon-Mitchell S, Von Ahrens D, Pradhan K, Steeples V, Kim S, Steidl U, Walter M, Fraser IDC, Kulkarni A, Salomonis N, Komurov K, Boultwood J, Verma A, Starczynowski DT. (2019) “U2AF1 mutations induce oncogenic IRAK4 isoforms and activate innate immune pathways in myeloid malignancies.”  Nat Cell Biol. 21(5):640-650.
  9. Sundaravel S, Kuo W-L, Jeong J, Choudhary G, Gordon-Mitchell S, Liu H, Bhagat T, McGraw K, Gurbuxani S, List A, Verma A, Wickrema A. (2019) “Loss of function of DOCK4 in myelodysplastic syndromes stem cells are restored by inhibitors of DOCK4 signaling networks.” Clinical Cancer Research. (Accepted Jun 2019)
  10. Jeong JJ, Gu X, Nie J, Sundaravel S, Liu H, Kuo WL, Bhagat TD, Pradhan K, Cao J, Nischal S, McGraw KL, Bhattacharyya S, Bishop MR, Artz A, Thirman MJ, Moliterno A, Ji P, Levine RL, Godley LA, Steidl U, Bieker J, List AF, Sauntharajah Y, He C, Verma A, Wickrema A. (2019) “Cytokine regulated phosphorylation and activation of TET2 by JAK2 in hematopoiesis.” Cancer Discov. pii: CD-18-1138.
  11. Shenoy N, Bhagat TD, Cheville J, Lohse C, Bhattacharyya S, Tischer A, Machha V, Gordon-Mitchell S, Choudhary G, Wong LF, Gross L, Ressigue E, Leibovich B, Boorjian SA, Steidl U, Wu X, Pradhan K, Gartrell B, Agarwal B, Pagliaro L, Suzuki M, Greally JM, Rakheja D, Thompson RH, Susztak K, Witzig T, Zou Y, Verma A. (2019) “Ascorbic acid-induced TET activation mitigates adverse hydroxymethylcytosine loss in renal cell carcinoma.” J Clin Invest. 130:1612-1625.
  12. Shastri A, Choudhary G, Teixeira M, Gordon-Mitchell S, Ramachandra N, Bernard L, Bhattacharyya S, Lopez R, Pradhan K, Giricz O, Ravipati G, Wong LF, Cole S, Bhagat TD, Feld J, Dhar Y, Bartenstein M, Thiruthuvanathan VJ, Wickrema A, Ye BH, Frank DA, Pellagatti A, Boultwood J, Zhou T, Kim Y, MacLeod AR, Epling-Burnette PK, Ye M, McCoon P, Woessner R, Steidl U, Will B, Verma A. (2018) “Antisense STAT3 inhibitor decreases viability of myelodysplastic and leukemic stem cells.” J Clin Invest. 128(12):5479-5488.
  13. Von Ahrens D, Bhagat TD, Nagrath D, Maitra A, Verma A. (2017) “The role of stromal cancer-associated fibroblasts in pancreatic cancer.” J Hematol Oncol. 10(1):76
  14. Giricz O, Mo Y, Dahlman KB, Cotto-Rios XM, Vardabasso C, Nguyen H, Matusow B, Bartenstein M, Polishchuk V, Johnson DB, Bhagat TD, Shellooe R, Burton E, Tsai J, Zhang C, Habets G, Greally JM, Yu Y, Kenny PA, Fields GB, Pradhan K, Stanley ER, Bernstein E, Bollag G, Gavathiotis E, West BL, Sosman JA, Verma AK. (2018) “The RUNX1/IL-34/CSF-1R axis is an autocrinally regulated modulator of resistance to BRAF-V600E inhibition in melanoma.” JCI Insight. 3(14): e120422
  15. Saleiro D, Mehrotra S, Kroczynska B, Beauchamp EM, Lisowski P, Majchrzak-Kita B, Bhagat TD, Stein BL, McMahon B, Altman JK, Kosciuczuk EM, Baker DP, Jie C, Jafari N, Thompson CB, Levine RL, Fish EN, Verma AK, Leonidas C. Platanias LC. (2016) “Central Role of ULK1 in Type I Interferon Signaling.” Cell Rep. 11(4): 605–617
  16. Shenoy N, Bhagat T, Nieves E, Stenson M, Lawson J, Choudhary GS, Habermann T, Nowakowski G, Singh R, Wu X, Verma A, Witzig TE. (2017) “Upregulation of TET activity with ascorbic acid induces epigenetic modulation of lymphoma cells.” Blood Cancer J. 7(7): e587
  17. Shah UA, Chung EY, Giricz O, Pradhan K, Kataoka K, Gordon-Mitchell S, Bhagat TD, Mai Y, Wei Y, Ishida E, Choudhary GS, Joseph A, Rice R, Gitego N, Parrish C, Bartenstein M, Goel S, Mantzaris I, Shastri A, Derman O, Binder A, Gritsman K, Kornblum N, Braunschweig I, Bhagat C, Hall J, Graber A, Ratner L, Wang Y, Ogawa S, Verma A, Ye BH, Janakiram M. (2018) “North American ATLL has a distinct mutational and transcriptional profile and responds to epigenetic therapies.” Blood. blood-2018-01-824607
  18. Bhattacharyya S, Pradhan K, Campbell N, Mazdo J, Vasantkumar A, Maqbool S, Bhagat TD, Gupta S, Suzuki M, Yu Y, Greally JM, Steidl U, Bradner J, Dawlaty M, Godley L, Maitra A, Verma A. (2017) “Altered hydroxymethylation is seen at regulatory regions in pancreatic cancer and regulates oncogenic pathways.” Genome Research. 27(11): 1830–1842
  19. Bachegowda L, Morrone K, Winski SL, Mantzaris I, Bartenstein M, Ramachandra N, Giricz O, Sukrithan V, Nwankwo G, Shahnaz S, Bhagat T, Bhattacharyya S, Assal A, Shastri A, Gordon-Mitchell S, Pellagatti A, Boultwood J, Schinke C, Yu Y, Guha C, Rizzi J, Garrus J, Brown S, Wollenberg L, Hogeland G, Wright D, Munson M, Rodriguez M, Gross S, Chantry D, Zou Y, Platanias L, Burgess LE, Pradhan K, Steidl U, Verma A. (2017) “Pexmetinib: a novel dual inhibitor of Tie-2 and p38 MAPK with efficacy in preclinical models of myelodysplastic syndromes and acute myeloid leukemia.” Cancer Research. 76(16): 4841–4849
  20. Sundaravel S, Duggan R, Bhagat T, Ebenezer DL, Liu H, Yu Y, Bartenstein M, Unnikrishnan M, Karmakar S, Liu T-C, Torregroza I, Quenon T, Anastasi J, McGraw KL, Pellagatti A, Boultwood J, Yajnik V, Artz A, Le Beau MM, Steidl U, List AF, Evans T, Verma A, and Wickrema A. (2015) “Reduced DOCK4 expression leads to erythroid dysplasia in myelodysplastic syndromes.”  PNAS 112 (46) E6359-E6368Schinke C, Giricz O, Li W, Shastri A, Gordon SAK, Barreyro L, Bhagat T, Bhattacharyya S, Ramachandra N, Bartenstein M, Pellagatti A, Boultwood J, Wickrema A, Yu Y, Will B, Wei S, Steidl U, Verma A. (2015) “IL8-CXCR2 pathway inhibition as a therapeutic strategy against MDS and AML stem cells.” Blood. 125(20) 3144-3152
  21. Caescu CI, Guo X, Tesfa L, Bhagat TD, Verma A, Zheng D, Stanley ER. (2015) “Colony stimulating factor-1 receptor signaling networks inhibit mouse macrophage inflammatory responses by induction of microRNA-21.” Blood. 125(8) E1-13
  22. Hu CY, Mohtat D, Yu Y, Ko YA, Shenoy N, Bhattacharya S, Izquierdo MC, Park AS, Giricz O, Vallumsetla N, Gundabolu K, Ware K, Bhagat TD, Suzuki M, Pullman J, Liu XS, Greally JM, Susztak K, Verma A. (2014) “Kidney cancer is characterized by aberrant methylation of tissue-specific enhancers that are prognostic for overall survival.”Clin Cancer Res. 20(16):4349-60
  23. Mariani CJ, Vasanthakumar A, Madzo J, Yesilkanal A, Bhagat T, Yu Y, Bhattacharyya S, Wenger RH, Cohn SL, Nanduri J, Verma A, Prabhakar NR, Godley LA. (2014) “TET1-mediated hydroxymethylation facilitates hypoxic gene induction in neuroblastoma.” Cell Rep. 7(5):1343-52
  24. Tamari R, Schinke C, Bhagat T, Roth M, Braunschweig I, Will B, Steidl U, Verma A. (2014) “Eltrombopag can overcome the anti-megakaryopoietic effects of lenalidomide without increasing proliferation of the malignant myelodysplastic syndrome/acute myelogenous leukemia clone.” Leuk Lymphoma. 55(12):2901-6
  25. Bartholdy B, Christopeit M, Will B, Mo Y, Barreyro L, Yu Y, Bhagat TD, Okoye-Okafor UC, Todorova TI, Greally JM, Levine RL, Melnick A, Verma A, Steidl U. (2014) “HSC commitment-associated epigenetic signature is prognostic in acute myeloid leukemia.” J Clin Invest. 124(3):1158-67
  26. Bajpai M, Kessel R, Bhagat T, Nischal S, Yu Y, Verma A, Das KM. (2013) “High Resolution Integrative Analysis Reveals Widespread Genetic and Epigenetic Changes After Chronic In-Vitro Acid and Bile Exposure in Barrett's Epithelium Cells.” Genes Chromosomes and Cancer. 52(12) 1123-1132
  27. Yang X, Song JH, Cheng Y, Wu W, Bhagat T, Yu Y, Abraham JM, Ibrahim S, Ravich W, Roland BC, Khashab M, Singh VK, Shin EJ, Yang X, Verma AK, Meltzer SJ, Mori Y. (2013) “Long non-coding RNA HNF1A-AS1 regulates proliferation and migration in oesophageal adenocarcinoma cells.” Gut. Sep 2. ;63(6):881-90
  28. Bhattacharyya S, Yu Y, Suzuki M, Campbell N, Mazdo J, Vasanthakumar A, Bhagat TD, Nischal S, Christopeit M, Parekh S, Steidl U, Godley L, Maitra A, Greally JM, Verma A. (2013) “Genome-wide hydroxymethylation tested using the HELP-GT assay shows redistribution in cancer.” Nucleic Acids Res. 41(16):e157
  29. Heuck CJ, Mehta J, Bhagat T, Gundabolu K, Yu Y, Khan S, Chrysofakis G, Schinke C, Tariman J, Vickrey E, Pulliam N, Nischal S, Zhou L, Bhattacharyya S, Meagher R, Hu C, Maqbool S, Suzuki M, Parekh S, Reu F, Steidl U, Greally J, Verma A, Singhal SB. (2013) “Myeloma is characterized by stage-specific alterations in DNA methylation that occur early during myelomagenesis.” J Immunol. 190(6):2966-75
  30. Will B, Vogler TO, Bartholdy B, Garrett-Bakelman F, Mayer J, Barreyro L, Pandolfi A, Todorova TI, Okoye-Okafor UC, Stanley RF, Bhagat TD, Verma A, Figueroa ME, Melnick A, Roth M, Steidl U. (2013). “Satb1 regulates the self-renewal of hematopoietic stem cells by promoting quiescence and repressing differentiation commitment.” Nat Immunol. 14(5):437-45
  31. Nischal S, Bhattacharyya S, Christopeit M, Yu Y, Zhou L, Bhagat TD, Sohal D, Will B, Mo Y, Suzuki M, Pardanani A, McDevitt M, Maciejewski JP, Melnick AM, Greally JM, Steidl U, Moliterno A, Verma A. (2013) “Methylome profiling reveals distinct alterations in phenotypic and mutational subgroups of myeloproliferative neoplasms.”Cancer Res. 73(3):1076-85.
  32. Yu Y, Mo Y, Ebenezer D, Bhattacharyya S, Liu H, Sundaravel S, Giricz O, Wontakal S, Cartier J, Caces B, Artz A, Nischal S, Bhagat T, Bathon K, Maqbool S, Gligich O, Suzuki M, Steidl U, Godley L, Skoultchi A, Greally J, Wickrema A, Verma A. (2013) “High resolution methylome analysis reveals widespread functional hypomethylation during adult human erythropoiesis.” J Biol. Chem. 288(13):8805-14.
  33. Khan H, Vale C, Bhagat T, Verma A. (2013) “Role of DNA methylation in the pathogenesis and treatment of myelodysplastic syndromes.” Semin. Hematol. 50(1):16-37
  34. Will B, Zhou L, Vogler TO, Ben-Neriah S, Schinke C, Tamari R, Yu Y, Bhagat TD, Bhattacharyya S, Barreyro L, Heuck C, Mo Y, Parekh S, McMahon C, Pellagatti A, Boultwood J, Montagna C, Silverman L, Maciejewski J, Greally JM, Ye BH, List AF, Steidl C, Steidl U, Verma A. (2012) “Stem and progenitor cells in myelodysplastic syndromes show aberrant stage-specific expansion and harbor genetic and epigenetic alterations.”Blood. 120(10):2076-86.
  35. Barta SK, Zou Y, Schindler J, Shenoy N, Bhagat TD, Steidl U, Verma A. (2012) “Synergy of sequential administration of a deglycosylated ricin A chain-containing combined anti-CD19 and anti-CD22 immunotoxin (Combotox) and cytarabine in a murine model of advanced acute lymphoblastic leukemia.” Leuk Lymphoma. 53(10): 1999-2003.
  36. Agarwal A, Polineni R, Hussein Z, Vigoda I, Bhagat TD, Bhattacharyya S, Maitra A, Verma A. (2012) “Role of epigenetic alterations in the pathogenesis of Barrett's esophagus and esophageal adenocarcinoma.” Int J Clin Exp Pathol. 5(5): 382-96.
  37. Shenoy N, Kessel R, Bhagat TD, Bhattacharyya S, Yu Y, McMahon C, Verma A. (2012) “Alterations in the ribosomal machinery in cancer and hematologic disorders.” J Hematol Oncol. Jun 18;5:32.
  38. Alvarez H, Opalinska J, Zhou L, Sohal D, Fazzari MJ, Yu Y, Montagna C, Montgomery EA, Canto M, Dunbar KB, Wang J, Roa JC, Mo Y, Bhagat T, Ramesh KH, Cannizzaro L, Mollenhauer J, Thompson RF, Suzuki M, Meltzer SJ, Melnick A, Greally JM, Maitra A, Verma A. (2011). "Widespread hypomethylation occurs early and synergizes with gene amplification during esophageal carcinogenesis." PLoS Genet 7(3): e1001356
  39. Zhou L, Opalinska J, Sohal D, Yu Y, Mo Y, Bhagat T, Abdel-Wahab O, Fazzari M, Figueroa M, Alencar C, Zhang J, Kambhampati S, Parmar S, Nischal S, Hueck C, Suzuki M, Freidman E, Pellagatti A, Boultwood J, Steidl U, Sauthararajah Y, Yajnik V, McMahon C, Gore SD, Platanias LC, Levine R, Melnick A, Wickrema A, Greally JM, Verma A. (2011). "Aberrant epigenetic and genetic marks are seen in myelodysplastic leukocytes and reveal Dock4 as a candidate pathogenic gene on chromosome 7q." J Biol Chem 286(28): 25211-25223.
  40. Zhou L, McMahon C, Bhagat T, Alencar C, Yu Y, Fazzari M, Sohal D, Heuck C, Gundabolu K, Ng C, Mo Y, Shen W, Wickrema A, Kong G, Friedman E, Sokol L, Mantzaris I, Pellagatti A, Boultwood J, Platanias LC, Steidl U, Yan L, Yingling JM, Lahn MM, List A, Bitzer M, Verma A. (2011). "Reduced SMAD7 leads to overactivation of TGF- β signaling in MDS that can be reversed by a specific inhibitor of TGF- β receptor I kinase." Cancer Res 71(3): 955-963.
  41. Schinke C, Goel S, Bhagat TD, Zhou L, Mo Y, Gallagher R, Kabalka GW, Platanias LC, Verma A, Das B. (2010). "Design and synthesis of novel derivatives of all-trans retinoic acid demonstrate the combined importance of acid moiety and conjugated double bonds in its binding to PML-RAR-alpha oncogene in acute promyelocytic leukemia." Leuk Lymphoma 51(6): 1108-1114.
  42. Einstein F, Thompson RF, Bhagat TD, Fazzari MJ, Verma A, Barzilai N, Greally JM. (2010). "Cytosine methylation dysregulation in neonates following intrauterine growth restriction." PLoS ONE 5(1): e8887.
  43. Zhou L, Nguyen AN, Sohal D, Ying Ma J, Pahanish P, Gundabolu K, Hayman J, Chubak A, Mo Y, Bhagat TD, Das B, Kapoun AM, Navas TA, Parmar S, Kambhampati S, Pellagatti A, Braunchweig I, Zhang Y, Wickrema A, Medicherla S, Boultwood J, Platanias LC, Higgins LS, List AF, Bitzer M, Verma A (2008). "Inhibition of the TGF- β receptor I kinase promotes hematopoiesis in MDS." Blood 112(8): 3434-3443.
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