Honors & Awards

  • Life Science National eligibility test (NET) award, Council of Scientific and Industrial Research (CSIR) Govt. of India (Jun 2011)
  • National Senior Research PhD Fellowship, Council of Scientific and Industrial Research (CSIR)- University grants commission (UGC) (Jan 2015-Dec 2016)
  • National Junior Research PhD fellowship, Council of Scientific and Industrial Research (CSIR)- University grants commission (UGC) (Jan 2012-Dec 2014)
  • All-India Graduate Aptitude Test in Engineering -GATE Fellowship in Biotechnology, Indian Institute of Science (IISc) (April 2011)
  • BCIL (Biotech Consortium India Limited) Industrial training Fellowship, Department of Biotechnology (DBT), Govt. of India (2010)
  • Contingency grant for MSc. dissertation at HCG Hospitals Bangalore, Department of Biotechnology, Govt. of India (2010)
  • DBT Fellowship for MSc Biotechnology, Department of Biotechnology (DBT), Govt. of India (2008-2010)

Professional Education

  • Doctor of Philosophy, Institute of Bioinformatics, Bangalore, India (2017)
  • Master of Science, University Of Mysore (2011)
  • Bachelor of Science, Bangalore University (2008)

Stanford Advisors

All Publications

  • Detection, survival and infectious potential of Mycobacterium tuberculosis in the environment: a review of the evidence and epidemiological implications EUROPEAN RESPIRATORY JOURNAL Martinez, L., Verma, R., Croda, J., Horsburgh, C., Walter, K. S., Degner, N., Middelkoop, K., Koch, A., Hermans, S., Warner, D. F., Wood, R., Cobelens, F., Andrews, J. R. 2019; 53 (6)
  • Whole Genome Sequencing of Mycobacterium tuberculosis Clinical Isolates From India Reveals Genetic Heterogeneity and Region-Specific Variations That Might Affect Drug Susceptibility FRONTIERS IN MICROBIOLOGY Advani, J., Verma, R., Chatterjee, O., Pachouri, P., Upadhyay, P., Singh, R., Yadav, J., Naaz, F., Ravikumar, R., Buggi, S., Suar, M., Gupta, U. D., Pandey, A., Chauhan, D. S., Tripathy, S., Gowda, H., Prasad, T. 2019; 10
  • Integrated Multi-Omic Analysis of Mycobacterium tuberculosis H37Ra Redefines Virulence Attributes. Frontiers in microbiology Pinto, S. M., Verma, R., Advani, J., Chatterjee, O., Patil, A. H., Kapoor, S., Subbannayya, Y., Raja, R., Gandotra, S., Prasad, T. S. 2018; 9: 1314


    H37Ra is a virulence attenuated strain of Mycobacterium tuberculosis widely employed as a model to investigate virulence mechanisms. Comparative high-throughput studies have earlier correlated its avirulence to the presence of specific mutations or absence of certain proteins. However, a recent sequencing study of H37Ra, has disproved several genomic differences earlier reported to be associated with virulence. This warrants further investigations on the H37Ra proteome as well. In this study, we carried out an integrated analysis of the genome, transcriptome, and proteome of H37Ra. In addition to confirming single nucleotide variations (SNVs) and insertion-deletions that were reported earlier, our study provides novel insights into the mutation spectrum in the promoter regions of 7 genes. We also provide transcriptional and proteomic evidence for 3,900 genes representing ~80% of the total predicted gene count including 408 proteins that have not been identified previously. We identified 9 genes whose coding potential was hitherto reported to be absent in H37Ra. These include 2 putative virulence factors belonging to ESAT-6 like family of proteins. Furthermore, proteogenomic analysis enabled us to identify 63 novel proteins coding genes and correct 25 existing gene models in H37Ra genome. A majority of these were found to be conserved in the virulent strain H37Rv as well as in other mycobacterial species suggesting that the differences in the virulent and avirulent strains of M. tuberculosis are not entirely dependent on the expression of certain proteins or their absence but may possibly be ascertained to functional changes.

    View details for DOI 10.3389/fmicb.2018.01314

    View details for PubMedID 29971057

    View details for PubMedCentralID PMC6018540

  • Data on whole genome sequencing of extrapulmonary tuberculosis clinical isolates from India. Data on whole genome sequencing of extrapulmonary tuberculosis clinical isolates from India. Advani, J., Sharma.K, Verma, R., Chatterjee O, Solanki HS, Pandey.A., Gowda.H., Prasad. TSK 2018
  • Rise of Clinical Microbial Proteogenomics: A Multiomics Approach to Nontuberculous Mycobacterium-The Case of Mycobacterium abscessus UC22. Rise of Clinical Microbial Proteogenomics: A Multiomics Approach to Nontuberculous Mycobacterium-The Case of Mycobacterium abscessus UC22. Advani, J., Verma, R., Chatterjee O, Gowda H, Prasad TSK, et al 2018

    View details for DOI 10.1089/omi.2018.0116

  • Quantitative Proteomic and Phosphoproteomic Analysis of H37Ra and H37Rv Strains of Mycobacterium tuberculosis JOURNAL OF PROTEOME RESEARCH Verma, R., Pinto, S. M., Patil, A. H., Advani, J., Subba, P., Kumar, M., Sharma, J., Dey, G., Ravikumar, R., Buggi, S., Satishchandra, P., Sharma, K., Suar, M., Tripathy, S. P., Chauhan, D. S., Gowda, H., Pandey, A., Gandotra, S., Prasad, T. S. 2017; 16 (4): 1632-1645


    Mycobacterium tuberculosis, the causative agent of tuberculosis, accounts for 1.5 million human deaths annually worldwide. Despite efforts to eradicate tuberculosis, it still remains a deadly disease. The two best characterized strains of M. tuberculosis, virulent H37Rv and avirulent H37Ra, provide a unique platform to investigate biochemical and signaling pathways associated with pathogenicity. To delineate the biomolecular dynamics that may account for pathogenicity and attenuation of virulence in M. tuberculosis, we compared the proteome and phosphoproteome profiles of H37Rv and H37Ra strains. Quantitative phosphoproteomic analysis was performed using high-resolution Fourier transform mass spectrometry. Analysis of exponential and stationary phases of these strains resulted in identification and quantitation of 2709 proteins along with 512 phosphorylation sites derived from 257 proteins. In addition to confirming the presence of previously described M. tuberculosis phosphorylated proteins, we identified 265 novel phosphorylation sites. Quantitative proteomic analysis revealed more than five-fold upregulation of proteins belonging to virulence associated type VII bacterial secretion system in H37Rv when compared to those in H37Ra. We also identified 84 proteins, which exhibited changes in phosphorylation levels between the virulent and avirulent strains. Bioinformatics analysis of the proteins altered in their level of expression or phosphorylation revealed enrichment of pathways involved in fatty acid biosynthesis and two-component regulatory system. Our data provides a resource for further exploration of functional differences at molecular level between H37Rv and H37Ra, which will ultimately explain the molecular underpinnings that determine virulence in tuberculosis.

    View details for DOI 10.1021/acs.jproteome.6b00983

    View details for Web of Science ID 000398985700023

    View details for PubMedID 28241730

  • Whole Genome Sequencing of Mycobacterium tuberculosis Isolates From Extrapulmonary Sites. Omics : a journal of integrative biology Sharma, K., Verma, R., Advani, J., Chatterjee, O., Solanki, H. S., Sharma, A., Varma, S., Modi, M., Ray, P., Mukherjee, K. K., Sharma, M., Dhillion, M. S., Suar, M., Chatterjee, A., Pandey, A., Prasad, T. S., Gowda, H. 2017; 21 (7): 413–25


    Tuberculosis (TB) remains one of the leading causes of morbidity and mortality worldwide. Extrapulmonary tuberculosis (EPTB) constitutes around 15-20% of TB cases in immunocompetent individuals. Extrapulmonary sites that are affected by TB include bones, lymph nodes, meningitis, pleura, and genitourinary tract. Whole genome sequencing has emerged as a powerful tool to map genetic diversity among Mycobacterium tuberculosis (MTB) isolates and identify the genomic signatures associated with drug resistance, pathogenesis, and disease transmission. Several pulmonary isolates of MTB have been sequenced over the years. However, availability of whole genome sequences of MTB isolates from extrapulmonary sites is limited. Some studies suggest that genetic variations in MTB might contribute to disease presentation in extrapulmonary sites. This can be addressed if whole genome sequence data from large number of extrapulmonary isolates becomes available. In this study, we have performed whole genome sequencing of five MTB clinical isolates derived from EPTB sites using next-generation sequencing platform. We identified 1434 nonsynonymous single nucleotide variations (SNVs), 143 insertions and 105 deletions. This includes 279 SNVs that were not reported before in publicly available datasets. We found several mutations that are known to confer resistance to drugs. All the five isolates belonged to East-African-Indian lineage (lineage 3). We identified 9 putative prophage DNA integrations and 14 predicted clustered regularly interspaced short palindromic repeats (CRISPR) in MTB genome. Our analysis indicates that more work is needed to map the genetic diversity of MTB. Whole genome sequencing in conjunction with comprehensive drug susceptibility testing can reveal clinically relevant mutations associated with drug resistance.

    View details for DOI 10.1089/omi.2017.0070

    View details for PubMedID 28692415

  • Integrating transcriptomic and proteomic data for accurate assembly and annotation of genomes GENOME RESEARCH Prasad, T. S., Mohanty, A. K., Kumar, M., Sreenivasamurthy, S. K., Dey, G., Nirujogi, R. S., Pinto, S. M., Madugundu, A. K., Pati, A. H., Advani, J., Manda, S. S., Gupta, M. K., Dwivedi, S. B., Kelkar, D. S., Hall, B., Jiang, X., Peery, A., Rajagopalan, P., Yelamanchi, S. D., Solanki, H. S., Raja, R., Sathe, G. J., Chavan, S., Verma, R., Patel, K. M., Jain, A. P., Syed, N., Datta, K. K., Khan, A. A., Dammalli, M., Jayaram, S., Radhakrishnan, A., Mitchell, C. J., Na, C., Kumar, N., Sinnis, P., Sharakhov, I. V., Wang, C., Gowda, H., Tu, Z., Kumar, A., Pandey, A. 2017; 27 (1): 133-144


    Complementing genome sequence with deep transcriptome and proteome data could enable more accurate assembly and annotation of newly sequenced genomes. Here, we provide a proof-of-concept of an integrated approach for analysis of the genome and proteome of Anopheles stephensi, which is one of the most important vectors of the malaria parasite. To achieve broad coverage of genes, we carried out transcriptome sequencing and deep proteome profiling of multiple anatomically distinct sites. Based on transcriptomic data alone, we identified and corrected 535 events of incomplete genome assembly involving 1196 scaffolds and 868 protein-coding gene models. This proteogenomic approach enabled us to add 365 genes that were missed during genome annotation and identify 917 gene correction events through discovery of 151 novel exons, 297 protein extensions, 231 exon extensions, 192 novel protein start sites, 19 novel translational frames, 28 events of joining of exons, and 76 events of joining of adjacent genes as a single gene. Incorporation of proteomic evidence allowed us to change the designation of more than 87 predicted "noncoding RNAs" to conventional mRNAs coded by protein-coding genes. Importantly, extension of the newly corrected genome assemblies and gene models to 15 other newly assembled Anopheline genomes led to the discovery of a large number of apparent discrepancies in assembly and annotation of these genomes. Our data provide a framework for how future genome sequencing efforts should incorporate transcriptomic and proteomic analysis in combination with simultaneous manual curation to achieve near complete assembly and accurate annotation of genomes.

    View details for DOI 10.1101/gr.201368.115

    View details for Web of Science ID 000391906500012

    View details for PubMedID 28003436

    View details for PubMedCentralID PMC5204337

  • A network map of Interleukin-10 signaling pathway JOURNAL OF CELL COMMUNICATION AND SIGNALING Verma, R., Balakrishnan, L., Sharma, K., Khan, A. A., Advani, J., Gowda, H., Tripathy, S. P., Suar, M., Pandey, A., Gandotra, S., Prasad, T. S., Shankar, S. 2016; 10 (1): 61-67


    Interleukin-10 (IL-10) is an anti-inflammatory cytokine with important immunoregulatory functions. It is primarily secreted by antigen-presenting cells such as activated T-cells, monocytes, B-cells and macrophages. In biologically functional form, it exists as a homodimer that binds to tetrameric heterodimer IL-10 receptor and induces downstream signaling. IL-10 is associated with survival, proliferation and anti-apoptotic activities of various cancers such as Burkitt lymphoma, non-Hodgkins lymphoma and non-small scell lung cancer. In addition, it plays a central role in survival and persistence of intracellular pathogens such as Leishmania donovani, Mycobacterium tuberculosis and Trypanosoma cruzi inside the host. The signaling mechanisms of IL-10 cytokine are not well explored and a well annotated pathway map has been lacking. To this end, we developed a pathway resource by manually annotating the IL-10 induced signaling molecules derived from literature. The reactions were categorized under molecular associations, activation/inhibition, catalysis, transport and gene regulation. In all, 37 molecules and 76 reactions were annotated. The IL-10 signaling pathway can be freely accessed through NetPath, a resource of signal transduction pathways previously developed by our group.

    View details for DOI 10.1007/s12079-015-0302-x

    View details for Web of Science ID 000377699100008

    View details for PubMedID 26253919

    View details for PubMedCentralID PMC4850137

  • A network map of BDNF/TRKB and BDNF/p75NTR signaling system. Journal of cell communication and signaling Sandhya, V. K., Raju, R., Verma, R., Advani, J., Sharma, R., Radhakrishnan, A., Nanjappa, V., Narayana, J., Somani, B. L., Mukherjee, K. K., Pandey, A., Christopher, R., Prasad, T. S. 2013; 7 (4): 301-307

    View details for DOI 10.1007/s12079-013-0200-z

    View details for PubMedID 23606317

    View details for PubMedCentralID PMC3889250

  • A multilectin affinity approach for comparative glycoprotein profiling of rheumatoid arthritis and spondyloarthropathy. Clinical proteomics Bhattacharjee, M., Sharma, R., Goel, R., Balakrishnan, L., Renuse, S., Advani, J., Gupta, S. T., Verma, R., Pinto, S. M., Sekhar, N. R., Nair, B., Prasad, T. S., Harsha, H. C., Jois, R., Shankar, S., Pandey, A. 2013; 10 (1): 11-?


    Arthritis refers to inflammation of joints and includes common disorders such as rheumatoid arthritis (RA) and spondyloarthropathies (SpAs). These diseases differ mainly in terms of their clinical manifestations and the underlying pathogenesis. Glycoproteins in synovial fluid might reflect the disease activity status in the joints affected by arthritis; yet they have not been systematically studied previously. Although markers have been described for assisting in the diagnosis of RA, there are currently no known biomarkers for SpA.We sought to determine the relative abundance of glycoproteins in RA and SpA by lectin affinity chromatography coupled to iTRAQ labeling and LC-MS/MS analysis. We also used ELISA to validate the overexpression of VCAM-1, one of the candidate proteins identified in this study, in synovial fluid from RA patients.We identified proteins that were previously reported to be overexpressed in RA including metalloproteinase inhibitor 1 (TIMP1), myeloperoxidase (MPO) and several S100 proteins. In addition, we discovered several novel candidates that were overexpressed in SpA including Apolipoproteins C-II and C-III and the SUN domain-containing protein 3 (SUN3). Novel molecules found overexpressed in RA included extracellular matrix protein 1 (ECM1) and lumican (LUM). We validated one of the candidate biomarkers, vascular cell adhesion molecule 1 (VCAM1), in 20 RA and SpA samples using ELISA and confirmed its overexpression in RA (p-value <0.01). Our quantitative glycoproteomic approach to study arthritic disorders should open up new avenues for additional proteomics-based discovery studies in rheumatological disorders.

    View details for DOI 10.1186/1559-0275-10-11

    View details for PubMedID 24010407

    View details for PubMedCentralID PMC3846907

  • Proteomic analysis of purified protein derivative of Mycobacterium tuberculosis. Clinical proteomics Prasad, T. S., Verma, R., Kumar, S., Nirujogi, R. S., Sathe, G. J., Madugundu, A. K., Sharma, J., Puttamallesh, V. N., Ganjiwale, A., Myneedu, V. P., Chatterjee, A., Pandey, A., Harsha, H., Narayana, J. 2013; 10 (1): 8-?


    Purified protein derivative (PPD) has been used for more than half a century as an antigen for the diagnosis of tuberculosis infection based on delayed type hypersensitivity. Although designated as "purified," in reality, the composition of PPD is highly complex and remains ill-defined. In this report, high resolution mass spectrometry was applied to understand the complexity of its constituent components. A comparative proteomic analysis of various PPD preparations and their functional characterization is likely to help in short-listing the relevant antigens required to prepare a less complex and more potent reagent for diagnostic purposes.Proteomic analysis of Connaught Tuberculin 68 (PPD-CT68), a tuberculin preparation generated from M. tuberculosis, was carried out in this study. PPD-CT68 is the protein component of a commercially available tuberculin preparation, Tubersol, which is used for tuberculin skin testing. Using a high resolution LTQ-Orbitrap Velos mass spectrometer, we identified 265 different proteins. The identified proteins were compared with those identified from PPD M. bovis, PPD M. avium and PPD-S2 from previous mass spectrometry-based studies. In all, 142 proteins were found to be shared between PPD-CT68 and PPD-S2 preparations. Out of the 354 proteins from M. tuberculosis-derived PPDs (i.e. proteins in either PPD-CT68 or PPD-S2), 37 proteins were found to be shared with M. avium PPD and 80 were shared with M. bovis PPD. Alignment of PPD-CT68 proteins with proteins encoded by 24 lung infecting bacteria revealed a number of similar proteins (206 bacterial proteins shared epitopes with 47 PPD-CT68 proteins), which could potentially be involved in causing cross-reactivity. The data have been deposited to the ProteomeXchange with identifier PXD000377.Proteomic and bioinformatics analysis of different PPD preparations revealed commonly and differentially represented proteins. This information could help in delineating the relevant antigens represented in various PPDs, which could further lead to development of a lesser complex and better defined skin test antigen with a higher specificity and sensitivity.

    View details for DOI 10.1186/1559-0275-10-8

    View details for PubMedID 23870090

    View details for PubMedCentralID PMC3729367