Bubree Subramanian, PhD
Our lab focuses on understanding the molecular mechanisms that regulate anti-tumor immune response in cancers. Currently we are investing the following topics in our laboratory.
- Tumor derived extracellular vesicles and anti-tumor immunity in colorectal cancer
- Atypical chemokine receptor 4 (ACKR4) in anti-tumor Iimmunity in colorectal cancer
- MicroRNAs mediate host-microbiome interactions in colorectal cancer progression
- Regulation of host immune response in osteosarcoma
Cancer Biology, Cancer immunology, MicroRNAs mediated gene regulation in development and disease
Awards & Recognition
- Visiting Professor, University of Erlangen-Nuremberg, Germany
- American Cancer Society Research Scholar Award, USA
- Carlson Faculty Award, University of Minnesota/Karolinska Institute Faculty collaboration program
- Norwegian Centennial Chair Faculty Award for visiting professorship to University of Oslo, Norway
- Senior research fellowship from University Grants Commission, New Delhi, India
- Merit scholarship from Department of Biotechnology, New Delhi, India
- Member of American Association for Cancer Research (AACR), USA
- Member American Society of Exosomes and Microvesicles, (ASEMV) USA
- Member, Connective Tissue Oncology Society (CTOS), USA
- Member, American Pancreatic Association (APA), USA
- Member of the Human Genome Organization (HUGO), UK
- Life member, Society of Biological Chemists, India
Associate Professor, Basic and Translational Research, Department of Surgery
Faculty, MS and PhD Programs in Pharmacology
PhD, Centre for Cellular and Molecular Biology, Jawaharlal Nehru University, India (Molecular and Cellular Biology)
M.S., Tamil Nadu Agriculture University, India (Biotechnology)
B.S., Tamil Nadu Agriculture University, India (Agriculture)
Post graduate diploma, Patents Law, National Academy of Legal Studies & Research, India; Postdoctoral Associate, Stanford University, Department of Pathology
MicroRNA mediated gene regulation in human sarcomas
Gene expression profiles - developing novel diagnostic markers and identification of therapeutic targets in sarcomas and other cancers.
1. Tumor derived extracellular vesicles and anti-tumor immunity in colorectal cancer.
Colorectal cancer (CRC) remains the third most common cause of cancer-related deaths in the U.S. The majority (~85%) of CRC tumors are non-immunogenic, i.e. they lack a significant number of infiltrating T cells, and are typically unresponsive to the immune-checkpoint inhibitor based therapies that have dramatically changed the way we treat many cancer patients. T cells isolated from non-immunogenic, microsatellite stable (MSS) CRC have lower levels of the CD28 protein, which provides a co-stimulatory signal required for T cell activation, trafficking, proliferation, differentiation and cytotoxic activity. We are testing the following hypothesis that extracellular vesicles (EVs) containing immunosuppressive microRNAs secreted by CRC cells suppress host T cell activity locally and in tumor draining lymph nodes, resulting in a deficient immune response that allows for increased tumor progression and growth. Results from this study will fundamentally advance our knowledge of how cancer cells modulate and suppress the immune response, provide novel targets, and form the basis for a new anti-cancer therapeutic strategy.
2. Atypical Chemokine Receptor 4 (ACKR4) in anti-tumor immunity in colorectal cancer
Several chemokines and cytokines are implicated in CRC immune response. One of the under examined features of CRC is the regulation of anti-tumor immunity by atypical chemokine receptor 4 (ACKR4) expression. This receptor, is involved in the internalization and degradation of multiple chemokines, such as chemokine (C-C motif) ligand 19 (CCL19) and CCL21, thereby modulating the CC-chemokine receptor 7 (CCR7)/CCL19/CCL21 chemotaxis and its downstream immune responses. We are testing the hypothesize that ACKR4 positively affects immune regulation in CRC and confers antitumor immunity by modulating CCR7/CCL19/CCL21 chemotaxis.The results from this pilot study will establish the clinical significance of ACKR4 expression levels to immune response in colorectal cancer. As an outcome, it will fundamentally advance our knowledge of how anti-tumor immunity was generated and regulated in CRC, and provide novel targets for CRC immunotherapies.
3. MicroRNAs mediate host-microbiome interactions in colorectal cancer progression
The current standard of care for colorectal cancer (CRC) involves chemotherapies developed more than 50 years ago. Although the 5-year survival rate has been rising over the past few decades, it is still low at about 65%. And most of the improvement in survival is due to increased screening, which has identified more cases of CRC in earlier stages. In the past decade, with the advancement of high-throughput “omics” technologies, it has become clear that the microbiome plays an essential role in driving the pathogenesis of CRC; however, the mechanisms that underlie host-microbiome interactions in CRC have yet to be elucidated. Part of the reason is the complex interplay between the colon epithelium, the microbiome, and the immune system. Previous publications have elucidated how the microbiome could affect miRNA expression in CRC, but how CRC could affect the microbiome is not yet understood, even though host genetics is known to shape the microbiome. In light of these evidence, we are testing the hypothesis that a positive feedback loop exists in CRC in which preexisting dysbiosis initially drives the expression of certain miRNAs in the colon epithelium, which are then released into the colon lumen and in turn affect the composition of the gut microbiome, leading to additional dysbiosis. Results from this study will elucidate the underlying mechanisms of host-microbiome interactions in CRC and will provide insights into the development of novel treatment strategies.
4. Regulation of host immune response in osteosarcoma
Osteosarcoma (OS) is the most common primary bone malignancy, accounting for ~2% of childhood cancers. The relative 5-year survival rate for patients <30 years is ~60%, for patients with metastatic OS the rate drops to <20% - rates that have not changed over the last three decades. There is a critical need to develop novel therapeutic strategies for OS. Immunotherapy is dramatically changing how we treat patients with cancer, however, it is only effective when immune cells are actively recognize and fight the cancer. Our previous work provided evidence that OS tumors show differing levels of immune cell infiltration, and that low levels of immune cell gene expression are strongly associated with metastasis and poor patient survival. We have identified a set of microRNAs whose expression also correlates with poor survival. Our central hypothesis is that lack of a robust immune response and disruption of miRNA-mediated signaling networks are two key factors contributing to OS progression, response to therapy, and patient survival outcomes. We have mRNA and microRNA sequence data for 55 human OS tumors, 20 of which will be further tested using histochemistry to reveal which tumors have active immune cell infiltration. This project will validate our novel expression-based method for identifying patients who have an active anti-tumor immune response, and are thus most likely to benefit from adjuvant immunotherapy. Our integrated expression analysis should validate novel therapeutic targets and advance our understanding of OS pathobiology, particularly the molecular mechanisms used by tumors to suppress the host immune system. These results are expected to have a positive translational impact as this knowledge will aid in the identification of novel therapeutic targets and inform future treatment and detection strategies, thereby improving the overall survival of osteosarcoma patients.
95. Scott MC, Temiz NA, Sarver AE, LaRue, RS Rathe SK, Varshney J, Wolf NK, Moriarity BS, Spector LG, Modiano JF, Largaespada DA, Subramanian S, Sarver AL. Comparative transcriptome analysis quantifies immune cell transcript levels, metastatic progression and survival in osteosarcoma. Cancer Research 2018, 78: 326-337
94. Zhao X, Subramanian S. Intrinsic resistance of solid tumors to immune checkpoint blockade therapy. Cancer Research 2017 77: 817-822
93. Zhao X, Subramanian S. Oncogenic pathways that affect the antitumor immune response and immune checkpoint blockade therapy. Pharmacology and Therapeutics 2017 181:76-84.
92. Yuan C, Burns M, Subramanian S*, Blekhman R. Interaction between host microRNAs and the gut microbiota in colorectal cancer. mSystems (in press)
91. Deshpande DA, Guedes AGP, Graeff R, Dogan S, Subramanian S, Walseth TF, Kannan MS. CD38/cADPR signaling pathway in airway disease: Regulatory mechanisms. Mediators of Inflammation (in press)
90. Audre M, Zhao X, Subramanian S. Genotypic and phenotypic signatures to predict immune checkpoint blockade therapy response in colorectal cancer patients. Translational Res. (in press)
89. Thayanithy V, O'Hare P, Wong P, Zhao X, Steer CJ, Subramanian S, Lou E. A transwell assay that excludes exosomes for assessment of tunneling nanotube-mediated intercellular communication. Cell Communication and Signaling 2017 15:46.
88. Lou E, Gholami S, Romin Y, Thayanithy V, Fujisawa S, Desir S, Steer C, Subramanian S, Fong Y, Manova K, Moore M. Imaging tunneling membrane tubes elucidates cell communication in tumors. Trends in Cancer 2017 10:678-685.
87. Zhao X, Li L, Starr T, Subramanian S. Tumor location impacts immune response mouse models of colon cancer. Oncotarget 2017 8:54775-54787
86. Shu J, Li L, Sarver A, Varshney J, Spector L, Largaespada D, Steer C and Subramanian S. Imprinting defects at human 14q32 locus alters gene expression and is associated with the pathobiology of osteosarcoma. Oncotarget 2016 doi: 10.18632/oncotarget.6965.
85. Lou E, O'Hare P, Subramanian S, Steer CJ. Lost in Translation:Applying 2D intercellular communication via tunneling nanotubes in cell culture to the 3D environment of cancer biology. FEBS J 2017 284: 699-707
84. Nair A, Niu N, Tang X, Kocher J, Subramanian S* Kalari K. Circular RNAs and their associations with Breast Cancer subtype. Oncotarget 2016 DOI: 10.18632/oncotarget.13134 *Co-corresponding author
83. Sarver A and Subramanian S. Imprinting defects in osteosarcoma: DNA- and chromatin-modifying drugs hold promise to osteosarcoma therapy. Epigenomics 2016 7:885-888
82. Deshpande AD, Guedes AGP, Lund FE, Subramanian S, Walseth TF, Kannan MS. CD38 in the pathogenesis of allergic airway disease: potential therapeutic targets. Pharmacology and Therapeutics 2017 172: 116-126
81. Scott MC, Tomiyasu H, Garbe JR, Cornax I, Amaya C, O’Sullivan GM, Subramanian S, Bryan B, Modiano JF. Heterotypic models of osteosarcomarecapitulate tumor Heterogeneity and biological behavior. Disease Models Mechanisms 2016 9: 1435-1444. (Selected as an Editor’s Choice lead article of the issue)
80. Dixit A, Sarver A, Yuan Z, George J, Barlass U, Cheema C, Sareen A, Banerjee S, Dudeja V, Dawra R, Subramanian S, Saluja A. Comprehensive analysis of microRNA signature of mouse pancreatic acini identifies over-expression of miR-21-3p in acute pancreatitis. Am J Physiol - Gastrointestinal and Liver Physiology 2016 311: G974–G980.
79. Desir S, Dickson E, Vogel R, Thayanithy V, Wong P, Teoh D, Geller M, Steer C, Subramanian S, Lou E Tunneling nanotube conduits mediate direct cell-to-cell communication in ovarian cancer: implications for emergence of chemoresistance. Oncotarget 2016 doi: 10.18632/oncotarget.9504.
78. Dileepan M, Sarver A, Panettieri R, Subramanian S, Kannan M. MicroRNA mediated chemokine responses in human airway smooth muscle cells. PLoS One 2016 11(3):e0150842
77. Yan Y, Hanse EA, Stedman K, Benson JM, Lowman XH, Subramanian S, Kelekar A. ATRA upregulates tumor suppressor phosphatase PHLPP2 via C/EBP-b mediated repression of the miR17~92 cluster in AML. Cell Death and Diff 2016 7:1232-1242.
76. Varshney J, Scott MC, Largaespada DA, Subramanian S. Understanding Osteosarcoma Pathobiology: From Bench to Kennel to Bedside. Veterinary Sciences 2015 3: 3, 1-15
75. Sarver AE, Li L, Kartha RV, Subramanian S. MicroRNAs in the malignant transformation process. Adv Exp Med Biol. 2015; 889:1-21
74. Scott MC, SarverAL, TomiyasuH, EttenJV, Varshney J, SubramanianS, Modiano JF. Aberrant Retinoblastoma (RB)-E2F Transcriptional Regulation Defines Molecular Phenotypes of Osteosarcoma. J Bio Chem 2015 290:28072-28083
73. Murphy SJ, Hart SN, Halling GC, Johnson SH, Drucker T, Lima JF, Rohakhtar FR, Harris F, Kosari F, Subramanian S, Petersen GM, Kipp BR, McWilliams RR, Couch FJ and Vasmatzis G. Integrated genomic analysis of pancreatic ductal adenocarcinomas and impact on the SMAD4 and FHIT genes. Cancer Research 2016 76:749-761
72. Silva M, Hernandez ME, Rojas F, Li L, Subramanian S, Wilson MJ. MicroRNA miR-182 cluster mediated modulation of RECK without changes in cell surface membrane type-1 matrix metalloproteinase. Am J Cancer Research 2015 9: 2918-2928
71. Sarver A, Li L, Subramanian S.MicroRNA miR-183 functions as a potential oncogene by targeting EGR1 and promoting tumor cell migration. Cancer Research 2010, 70: 9570-9580.
70. Rojas F, Hernandez ME, Silva M, Li L, Subramanian S, Wilson MJ, Liu P. The Oncogenic Response to miR-335 is associated with cell surface expression of membrane-type 1 matrix metalloproteinase (MT1-MMP) activity. PLoS One 2015, 10:e0132026
69. Deshpande DA, Dileepan M, Walseth TA, Subramanian S and Kannan MS. MicroRNA regulation of airway smooth muscle phenotype: relevance to asthma. Drug Disc Res. 2015 76: 286–295
68. Sarver A and Subramanian S. Are microRNAs the answer to colorectal cancer’s big questions. J Clin Exp Pathol 2015 5:242
67. Varshney J and Subramanian S. MicroRNAs as potential target in human bone and soft tissue sarcoma therapeutics. Front Mol Biosci 2015 2: 31
66. Sarver AE, Sarver AL, Thayanithy V, Subramanian S. Identification, by systematic RNA sequencing, of novel candidate biomarkers and therapeutic targets in human soft tissue tumors. Lab Invest 2015 95: 1077-1088
65. Sarver AE, Subramanian S. MicroRNAs in the pathobiology of sarcomas. Lab Invest 2015 95:987-994
64. Oliveira A, Beyer G, Chugh R, Skube S, Majumder K, Banerjee S, Sangwan V, Dawra R, Subramanian S, Saluja A, and Dudeja A. Triptolide abrogates growth of colon cancer and induces cell cycle arrest by inhibiting transcriptional activation of E2F. Lab Invest 2015 95: 648-659
63. Guedes AGP, Deshpande DA, Dileepan M, Walseth TF, Panettieri RA, Subramanian S and Kannan MS. CD38 and Airway hyperresponsiveness: Studies on human airway smooth muscle cells and mouse models. Can J Physiol Pharm 2015 93: 145-153
62. Li L, Sarver A, Rohini K, Hajeri P, French A, Thibodeau S, Steer C, Subramanian S. Sequential expression of miR-182 and miR-503 cooperatively targets FBXW7 contributing to the malignant transformation of colon adenoma to adenocarcinoma. J Pathol 2014 234: 488-501 (Cover page article)
61. Dileepan M, Jude JA, Rao SP, Panettieri RA, Subramanian S, Walseth TF and Kannan MS. MicroRNA-708 regulates CD38 expression through signaling pathways JNK MAPKinase and PTEN/AKT in human airway smooth muscle cells. Respir Res. 2014 15:107
60. Thayanithy V, Dickson EL, Steer C, Subramanian S, Lou E, Tumor-stromal cross-talk: Direct cell-to-cell transfer of oncogenic microRNAs via tunneling nanotubes. Transl Res 2014 164: 359-365
59. Thayanithy V, Babatunde V, Dickson, EL, Wong P, Oh S, Ke X, Barlas A, Fujisawa S, Romin Y, Moreira AL, Downey RJ, Steer CJ, Subramanian S, Lou E. Tumor exosomes induce tunneling nanotubes in lipid raft-enriched regions of human mesothelioma cells. Exp Cell Res, 2014, 323: 178-188
58. Kartha RV and Subramanian S. Competing Endogenous RNAs (ceRNAs): New Entrants to the Intricacies of Gene Regulation. Front Genet 2014 30;5:8 (Invited inaugural article as an Associate Editor)
57. Varshney J and Subramanian S. Small is the new big- interplay of microRNAs in cancer. Current Science 2014 107: 803-814
56. Khatri R and Subramanian S. MicroRNA-135b and its circuitry networks as potential therapeutic targets in colon cancer. Front Oncol 2013, 3:268
55.Lou E, Subramanian S, Steer C. Pancreatic Cancer: Modulation of KRAS, MicroRNAs and Intercellular Communication in the Setting of Tumor Heterogeneity. Pancreas 2013,42: 1218-1226
54. Bannerjee S, Thayanithy V, Sangwan V, MacKenzie T, Saluja A, Subramanian S. Minnelide induces cell death and reduces tumor burden in orthotopic mice models of osteosarcoma. Cancer Letters 2013 335: 412-420
53.MacKenzie T, Mujumdar N, Banerjee S, Sangwan V, Sarver A, Vickers S, Subramanian S, Saluja A. Triptolide Induces the Expression of miR-142-3p, a Negative Regulator of heat shock protein 70 and pancreatic cancer cell proliferation. Molecular Cancer Ther 2013, 12:1266-1275
52. Sarver A, Thayanithy V, Scott M, Cleton AM, Hogendoorn P, Modiano J, Subramanian S. Integrative and comparative genomic analyses of human and canine osteosarcoma reveal the prognostic significance of 14q32 locus microRNAs. Orph J Rare Diseases 2013 8: 7
51. Charbonneau B, Vogel R, Manivel C, Rizzardi A, Schmechel S, Ognjanovic S, Subramanian S, Largaespada D, Weigel B. Expression of FGFR3 and FGFR4 and clinical risk factors associated with progression-free survival in synovial sarcoma. Human Pathology 2013,44:1918-1926
50. Sunderbose K Kartha RV, Subramanian S. MicroRNAs as biomarkers in cancer. Diagnostics.2013 3: 84-104
49. Raghu R, Liu CT, Mong-Hsun T, Xiaojia T, Krishna K, Subramanian S, Lee-Yan S. Transcriptome analysis of garlic induced hepatoprotection against alcoholic fatty liver. J Agri Food Chem. 201260:11104-11119
48. Shu J, Xia Z, Li L, Liang ET, Slipek N, Shen D, Foo J, Subramanian S, Steer C. Dose-dependent differential mRNA target selection and regulation by let-7a-7f and miR-17-92 cluster microRNAs. RNA Biol 2012 9:1275-1287
47. Angstadt AY, Thayanithy V, Subramanian S, Modiano JF, and Breen M. A genome-wide approach to comparative oncology: High-resolution oligonucleotide aCGH of canine and human osteosarcoma pinpoints shared microaberrations. Cancer Genetics 2012 205:572-587
46. Sarver A, Subramanian S. Competitive endogenous RNA Database. Bioinformation 2012 8(15): 731-733.
45.Thayanithy V, Park C, Sarver A, Kartha RV, Korpela DM, Graef AJ, Steer CJ, Modiano JF, Subramanian S. Combinatorial treatment of DNA and chromatin-modifying drugs cause cell death in human and canine osteosarcoma cell lines. PLOS One 2012 7(9): e43720.
44. Jude J, Dileepan M, Subramanian S, Solway J, Panettieri R, Walseth T, Kannan MS. MicroRNA miR-140-3p regulation of TNF-?-induced CD38 expression in human airway smooth muscle cells. Am J of Physiol 2012303:460-468
43. Subramanian S and Kartha RV. MicroRNA mediated gene regulations in human sarcomas. Cell Mol Life Sci 2012 69: 3571-3585
42. Lou E, Fujisawa S, Barlas A, Romin Y, Manova-Todorova K, Moore M and Subramanian S. Tunneling nanotubes: A new paradigm for studying intercellular communication and therapeutics in cancer. Commun Integer Biol 2012 5: 399–403 (Cover page article)
41. Steer CJ and Subramanian S. Circulating microRNAs as Biomarkers: A New Frontier in Diagnostics. Liver Transplantation 2012 18:265-269 (Cover page article)
40. Li L, Sarver A, Alamgir S, and Subramanian S.Downregulation of microRNAs miR-1, -206 and -29 stabilizes PAX3 and CCND2 expression in rhabdomyosarcoma. Lab Invest 2012 92:571-83
39. Thyanithy V, Sarver A, Kartha R, Park CW, Scott MC, AngstadtA, Breen M, Steer CJ, Modiano J, and Subramanian S. Perturbation in 14q32 miRNAs-MYC-miR-17~92 gene network contributes to osteosarcoma. Bone 2012 50:171-181
38. Shu J, Kren BT, Xia Z, Wong PY, Li L, Hanse EA, Min MM, Li B, Albrecht JH, Zeng Y, Subramanian S, and Steer CJ. Genome-wide microRNA downregulation as a negative feedback mechanism in the early phases of liver regeneration. Hepatology 2011 54:609-619
37. Oberg AL, French AJ, Sarver AL, Subramanian S, Morlan BW, Riska SM, Borralho PM, Cunningham JM, Boardman LA, Wang L, Smyrk TC, Asmann Y, Steer CJ, Thibodeau SN. MicroRNA expression in colon polyps provides evidence for a multi-hit model of colon cancer. PLoS One 2011 6(6): e20465
36. Scott MC, Sarver AL, Gavin K, Thayanithy V, Getzy DM, Newman RA, Cutter GR, Lindblad-Toh K, Kisseberth WC, Hunter LE, Subramanian S, Breen M, Modiano JF. Molecular subtypes of osteosarcoma identified by reducing tumor heterogeneity through an innovative comparative approach. Bone 2011 54:609-619
35. Mills AM, Beck AH, Montgomery K, Zhu SX, Espinosa I, Lee CH, Subramanian S, Fletcher C, van de Rijn M, West RB. Expression of subtype-specific Group 1 leiomyosarcoma markers in a wide variety of sarcomas by gene expression analysis and immunohistochemistry. Am J Surg Pathol 2011 35:583-589
34. Beckman JD, Chen C, Nguyen J, Thayanithy V, Subramanian S, Steer CJ, Vercellotti GM. Regulation of Heme-Oxygenase-1 protein expression by miR-377 in combination with miR-217. J Biol Chem 2011 286: 3194-3202
33. Shu J, Kren BT, Xia Z, Wong PY, Li L, Hanse EA, Min MM, Li B, Albrecht JH, Zeng Y, Subramanian S, Steer CJ. Genome-wide microRNA downregulation as a negative feedback mechanism in the early phases of liver regeneration. Hepatology 2011 54:609-619
32. Park C, Zeng Y, Zhang X, Subramanian S and Steer CJ.MicroRNAs identified in highly purified nuclei from HCT116 colon cancer cells. RNA Biology 2010 7:(5)
31. Sarver A, Phalak R, Thayanithy V, Subramanian S.S-MED: Sarcoma microRNA Expression Database. Lab Invest 2010 90: 753-761
30. Subramanian S*, Thayanithy V, West RB, Lee CH, Beck AH,Zhu S, Downs-Kelly E, Montgomery K, Goldblum JR,Hogendoorn PCW, Corless CL, Oliveira AM, Dry SM, Nielsen TO, Rubin BP, Fletcher JA, Fletcher CDM, van de Rijn M. Genome-wide transcriptome analyses reveals p53 inactivation mediated loss of miR-34a expression in malignant peripheral nerve sheath tumors. J Pathol 2010 220: 58-70 *Corresponding author, selected as hot topic and highlighted in J Pathol.Virtual Issue Number 1, April 2010
29. Subramanian S and Steer CJ. MicroRNA as gatekeepers of apoptosis. J Cell Physiol 2010 223: 289-298 (cover page article and discussed in the highlight section)
28. Kartha RV and Subramanian S. MicroRNAs in cardiovascular diseases: Biology and potential clinical applications. J Cardiovasc Tran Res 2010 3: 256-270
27. WangL, Tang H, Thayanithy T, Subramanian S, Oberg AL, Cunningham JM, Cerhan JR, Steer CJ, Thibodeau SN. Gene networks and microRNAs implicated in aggressive prostate cancer. Cancer Research 2009 69:9490-9497
26. Lee CH, Subramanian S, Beck AH, Espinosa I, Senz J, Zhu S, Huntsman D, van de Rijn M, Gilks C. MicroRNA profiling of BRCA1/2 mutation-carrying and non-mutation carrying high-grade serous carcinomas of ovary. PLoS One 2009 4(10):e7314
25. SarverAL, FrenchA, Borralho PM, Thayanithy V, Silverstein K, Morlan B, Oberg A, Cunningham J, Subramanian S, Wang L, Rodrigues C, Thibodeau SN, Steer CJ.Human colon cancer profiles show differential microRNA expression depending on mismatch repair status and are characteristic of undifferentiated proliferative states. BMC Cancer 2009 9:401
24. Wang L, Oberg AL, Asmann YW, Sicotte H, McDonnell SK, Riska SM, Liu W, Steer CJ, Subramanian S, Cunningham JM, Cerhan JR and Thibodeau SN. Genome-wide transcriptional profiling reveals microRNA-correlated genes and pathways in human lymphoblastoid cell lines.PLoS One 2009 4 (6): e5878
23. Hu Z, Fan C, Livasy C, He X, Oh DS, Ewend MG, Carey LA, Subramanian S, West R, Ikpatt F, Olopade OI, van de Rijn M, Perou CM. A compact VEGF signature associated with distant metastases and poor outcomes. BMC Medicine 2009 Mar 16;7:9
22. ClarkeB, TinkerAV, Lee C, Subramanian S, van de RijnM, TurbinD, Cadungog MG, HuntsmanD, CoukosG, GilksCB Intraepithelial T cells and Prognosis in Ovarian Carcinoma: Novel Associations with Stage, Tumor Type and BRCA1 Loss.Mod Pathol 2009 22:393-402
21. Subramanian S, Lui WO, Lee CH, Espinosa E, Nielsen T, Heinrich M, Corless C, Fire A, and van de Rijn M. MicroRNA expression signature of human soft tissue tumors. Oncogene 2008 27; 2015-2026
20. Lubieniecka JM, de Bruijn D, Su L,van Dijk A, Subramanian S, van de Rijn M, Poulin N, van Kessel A, Nielsen TO. Histone deacetylase inhibitors reverse SS18-SSX mediated polycomb silencing of the tumor suppressor EGR1 in synovial sarcoma. Cancer Research 2008 68: 4303-4310
19. Lee C, Espinosa I, Jensen K, Subramanian S, Zhu S, Varma S, Montgomery K, Nielsen TO, van de Rijn M and West R. Gene expression profiling identifies p63 as a diagnostic marker for giant cell tumor of the bone. Modern Pathology 2008 21:531-539
18. Lee C, Espinosa I, Vrijaldenhoven S, Subramanian S, Montgomery K, Zhu S, Poulin N, Nielsen T, West R, Gilks B, van de Rijn M. Prognostic significance of macrophage marker in leiomyosarcomas. Clinical Caner Research 2008 14; 1423-1430
17. Espinosa I, Lee C, Kim M, Rouse B, Subramanian S, Montgomery K, Corless CL, Heinrich MC, Smith KS, et al. A novel monoclonal antibody against DOG1 is a sensitive and specific marker for gastrointestinal stromal tumors. Am J Surg Path 2008 32; 210-218
16. Terry J, Saito T, Subramanian S, Ruttan C, Antonescu CR, Goldblum JR, Downs-Kelly E, Corless CL, Rubin BP, van de Rijn M, Ladanyi M, and Nielsen TO. TLE1 as a diagnostic immunohistochemical marker for synovial sarcoma emerging from gene expression profiling studies. Am J Surg Path 2007 31: 240-246
15. West RB, Rubin BP, Miller M, Subramanian S, Kaygusuz G, Montgomery K, Luca AD, Gilks B, Nielsen TO, Huntsman D and van de Rijn M. CSF1-COL6A3 gene fusion is present in a minority of tumor cells in tenosynovial giant cell tumor and pigment villonodular synovitis.Proc Natl Acad Sci USA 2006 103:690-695
14. Subramanian S, West RB, Marinelli RJ, Nielsen TO, Rubin BP, Goldblum JR, Patel RM, Zhu S, Montgomery K, Ng TL, Corless CL, Heinrich MC, and van de Rijn M. Gene Expression Profile of Extraskeletal Myxoid Chondrosarcoma. J Pathol 2005 206:433-444
13. Suresh A, Shah V, Rani DS, Singh BN, Uma G, Subramanian S, Kumar S and Singh L. A mouse gene encoding a novel member of the WD family of proteins is highly conserved and predominantly expressed in testis (wdr13). Mol Reprod Dev 2005 72: 299-310
12. West RB, Nuyten DSA, Subramanian S, Corless CL, Rubin BP, Montgomery K, Zhu SX, Nielsen TO, Patel R, Goldblum JR, Brown PO, van de Vijver M, van de Rijn M. Stromal Expression Signatures Predict Outcome in Breast Carcinoma. PLoS Biology 2005 3:3187
11. Subramanian S, West RB, Corless CL, Ou W, Rubin BP, Chu K, Leung SY, Yuen ST, Zhu S, Hernandez-Boussard T, Montgomery KD, Nielsen TO, Patel RM, Goldblum JR, Heinrich MC, Fletcher JA and van de Rijn M. Gastrointestinal Stromal Tumors (GISTs) with KIT and PDGFRA mutations have distinct gene expression profiles. Oncogene 2004 23: 7780-7790
10. West RB, Corless CL, Chen X, Rubin BP, Subramanian S, Montgomery KD, Zhu S, Ball CA, Nielsen TO, Patel R, Goldblum JR, Brown PO, Heinrich MC and van de Rijn M. The Novel Marker, DOG1, is expressed ubiquitously in Gastrointestinal Stromal Tumors irrespective of KIT or PDGFRA mutation status. Am J Pathol 2004 165: 107-113
9. Sabarinadh Ch, Subramanian S and Mishra RK. Extreme conservation of non-repetitive non-coding regions near HoxD complex of vertebrates. BMC Genomics 2004 5:75
8. Subramanian S, Mishra RK and Singh L Genome-wide analysis of microsatellite repeats in human: Abundance and their density in specific genomic regions Genome Biology 2004 4:R13
7. Subramanian S, Mishra RK and Singh L.Genome-wide analysis of Bkm sequences (GATA repeats): Predominant association with sex chromosomes and potential role in higher order chromatin organization and function.Bioinformatics 2003 19: 681-685
6. Subramanian S, Madugula VM, George R, Mishra RK, Pandit MW, Chanderashekar S Kumar and Singh L. Triplet repeats analysis in human genome: Abundance, distribution and association with genes and other genomic regions. Bioinformatics 2003 19: 549-552
5. Subramanian S, Madugula VM, George R Satish Kumar C, Pandit MW and Singh L. SSRD: A simple sequence repeat database for human genome. Comparative and Functional Genomic 20034: 342-345
4. Thangaraj K, Subramanian S, and Singh L. A unique case of deletion and duplication in the long arm of the Y chromosome in an individual with ambiguous genitalia.Am J Med Genet 2003 116: 205-207
3.Singh BN, Suresh A, Uma G, Subramanian S, Sultana MS, Goel S, Kumar S and Singh L.A highly conserved human gene encoding a novel member of WD-repeat family of proteins (WDR13). Genomics 2003 81: 315-328
2. Thangaraj K, Gupta NJ, Pavini K, Reddy AG, Subramanian S, Rani DS, Ghosh B, Chakravarty B and Singh L. Y-chromosome deletion in Azoospermic Men in India. J Andrology 2003 24: 588-597
1. Subramanian S, Madgula VM, George R, Mishra RK, Pandit MW, Kumar CS, Singh L MRD: a microsatellite repeats database for prokaryotic and eukaryotic genomes. Genome Biology. 2002; 3, 12