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Article: Machine-Learning Identifies a Strategy for Differentiation Therapy in Solid Tumors.

Sinha, Saptarshi / Alcantara, Joshua / Perry, Kevin / Castillo, Vanessa / Espinoza, Celia R / Taheri, Sahar / Vidales, Eleadah / Tindle, Courtney / Adel, Adel / Amirfakhri, Siamak / Sawires, Joseph R / Yang, Jerry / Bouvet, Michael / Sahoo, Debashis / Ghosh, Pradipta

bioRxiv : the preprint server for biology

2024

Abstract: Background: Although differentiation therapy can cure some hematologic malignancies, its curative potential remains unrealized in solid tumors. This is because conventional computational approaches succumb to the thunderous noise of inter-/intratumoral ... ...

Abstract	Background: Although differentiation therapy can cure some hematologic malignancies, its curative potential remains unrealized in solid tumors. This is because conventional computational approaches succumb to the thunderous noise of inter-/intratumoral heterogeneity. Using colorectal cancers (CRCs) as an example, here we outline a machine learning(ML)-based approach to track, differentiate, and selectively target cancer stem cells (CSCs). Methods: A transcriptomic network was built and validated using healthy colon and CRC tissues in diverse gene expression datasets (~5,000 human and >300 mouse samples). Therapeutic targets and perturbation strategies were prioritized using ML, with the goal of reinstating the expression of a transcriptional identifier of the differentiated colonocyte, CDX2, whose loss in poorly differentiated (CSC-enriched) CRCs doubles the risk of relapse/death. The top candidate target was then engaged with a clinical-grade drug and tested on 3 models: CRC lines in vitro, xenografts in mice, and in a prospective cohort of healthy (n = 3) and CRC (n = 23) patient-derived organoids (PDOs). Results: The drug shifts the network predictably, induces CDX2 and crypt differentiation, and shows cytotoxicity in all 3 models, with a high degree of selectivity towards all CDX2-negative cell lines, xenotransplants, and PDOs. The potential for effective pairing of therapeutic efficacy (IC50) and biomarker (CDX2-low state) is confirmed in PDOs using multivariate analyses. A 50-gene signature of therapeutic response is derived and tested on 9 independent cohorts (~1700 CRCs), revealing the impact of CDX2-reinstatement therapy could translate into a ~50% reduction in the risk of mortality/recurrence. Conclusions: Findings not only validate the precision of the ML approach in targeting CSCs, and objectively assess its impact on clinical outcome, but also exemplify the use of ML in yielding clinical directive information for enhancing personalized medicine.
Language	English
Publishing date	2024-01-17
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.09.13.557628
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Article ; Online: Functional assays with human patient-derived enteroid monolayers to assess the human gut barrier.

Sayed, Ibrahim M / Tindle, Courtney / Fonseca, Ayden G / Ghosh, Pradipta / Das, Soumita

STAR protocols

2021 Volume 2, Issue 3, Page(s) 100680

Abstract: Here, we describe the use of polarized patient enteroid-derived monolayers (EDMs) to assess the impact of e-cigarettes on the human gut barrier. These EDMs can be adapted to culture in a 96-well plate for high-throughput screening. We model the effect of ...

Abstract	Here, we describe the use of polarized patient enteroid-derived monolayers (EDMs) to assess the impact of e-cigarettes on the human gut barrier. These EDMs can be adapted to culture in a 96-well plate for high-throughput screening. We model the effect of e-cigarettes by combining pathogens, enteroids, and e-cigarette vapor-infused media and assess gut barrier integrity, bacterial internalization, and inflammatory response of the gut epithelium. This protocol can be used to assess the effects of e-cigarette components on gut functions. For complete details on the use and execution of this protocol, please refer to Sharma et al. (2021).
MeSH term(s)	Cell Culture Techniques/methods ; Epithelium ; High-Throughput Screening Assays/methods ; Humans ; Intestinal Mucosa/drug effects ; Intestinal Mucosa/microbiology ; Intestine, Small/cytology ; Models, Biological ; Organoids/cytology ; Organoids/metabolism ; Primary Cell Culture/methods ; Vaping/adverse effects
Language	English
Publishing date	2021-07-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	2666-1667
ISSN (online)	2666-1667
DOI	10.1016/j.xpro.2021.100680
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Functional assays with human patient-derived enteroid monolayers to assess the human gut barrier

Ibrahim M. Sayed / Courtney Tindle / Ayden G. Fonseca / Pradipta Ghosh / Soumita Das

STAR Protocols, Vol 2, Iss 3, Pp 100680- (2021)

2021

Abstract: Summary: Here, we describe the use of polarized patient enteroid-derived monolayers (EDMs) to assess the impact of e-cigarettes on the human gut barrier. These EDMs can be adapted to culture in a 96-well plate for high-throughput screening. We model the ... ...

Abstract	Summary: Here, we describe the use of polarized patient enteroid-derived monolayers (EDMs) to assess the impact of e-cigarettes on the human gut barrier. These EDMs can be adapted to culture in a 96-well plate for high-throughput screening. We model the effect of e-cigarettes by combining pathogens, enteroids, and e-cigarette vapor-infused media and assess gut barrier integrity, bacterial internalization, and inflammatory response of the gut epithelium. This protocol can be used to assess the effects of e-cigarette components on gut functions.For complete details on the use and execution of this protocol, please refer to Sharma et al. (2021).
Keywords	Cell Biology ; Cell culture ; High Throughput Screening ; Immunology ; Microbiology ; Stem Cells ; Science (General) ; Q1-390
Language	English
Publishing date	2021-09-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: SPT6 loss permits the transdifferentiation of keratinocytes into an intestinal fate that resembles Barrett's metaplasia.

Vo, Daniella T / Fuller, MacKenzie R / Tindle, Courtney / Anandachar, Mahitha Shree / Das, Soumita / Sahoo, Debashis / Ghosh, Pradipta

iScience

2021 Volume 24, Issue 10, Page(s) 103121

Abstract: Transient depletion of the transcription elongation factor SPT6 in the keratinocyte has been recently shown to inhibit epidermal differentiation and stratification; instead, they transdifferentiate into a gut-like lineage. We show here that this ... ...

Abstract	Transient depletion of the transcription elongation factor SPT6 in the keratinocyte has been recently shown to inhibit epidermal differentiation and stratification; instead, they transdifferentiate into a gut-like lineage. We show here that this phenomenon of transdifferentiation recapitulates Barrett's metaplasia, the only human pathophysiologic condition in which a stratified squamous epithelium that is injured due to chronic acid reflux is trans-committed into an intestinal fate. The evidence we present here not only lend support to the notion that the keratinocytes are potentially the cell of origin of Barrett's metaplasia but also provide mechanistic insights linking transient acid exposure, downregulation of SPT6, stalled transcription of the master regulator of epidermal fate TP63, loss of epidermal fate, and metaplastic progression. Because Barrett's metaplasia in the esophagus is a pre-neoplastic condition with no preclinical human models, these findings have a profound impact on the modeling Barrett's metaplasia-in-a-dish.
Language	English
Publishing date	2021-09-11
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2021.103121
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Article: A Living Organoid Biobank of Crohn's Disease Patients Reveals Molecular Subtypes for Personalized Therapeutics.

bioRxiv : the preprint server for biology

2023

Language	English
Publishing date	2023-03-13
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.03.11.532245
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Article: COVID-19 lung disease shares driver AT2 cytopathic features with Idiopathic pulmonary fibrosis.

Sinha, Saptarshi / Castillo, Vanessa / Espinoza, Celia R / Tindle, Courtney / Fonseca, Ayden G / Dan, Jennifer M / Katkar, Gajanan D / Das, Soumita / Sahoo, Debashis / Ghosh, Pradipta

bioRxiv : the preprint server for biology

2022

Abstract: Background: In the aftermath of Covid-19, some patients develop a fibrotic lung disease, i.e., : Method: Using an AI-guided approach, we analyzed > 1000 human lung transcriptomic datasets associated with various lung conditions using two viral ... ...

Abstract	Background: In the aftermath of Covid-19, some patients develop a fibrotic lung disease, i.e., Method: Using an AI-guided approach, we analyzed > 1000 human lung transcriptomic datasets associated with various lung conditions using two viral pandemic signatures (ViP and sViP) and one covid lung-derived signature. Upon identifying similarities between COVID-19 and idiopathic pulmonary fibrosis (IPF), we subsequently dissected the basis for such similarity from molecular, cytopathic, and immunologic perspectives using a panel of IPF-specific gene signatures, alongside signatures of alveolar type II (AT2) cytopathies and of prognostic monocyte-driven processes that are known drivers of IPF. Transcriptome-derived findings were used to construct protein-protein interaction (PPI) network to identify the major triggers of AT2 dysfunction. Key findings were validated in hamster and human adult lung organoid (ALO) pre-clinical models of COVID-19 using immunohistochemistry and qPCR. Findings: COVID-19 resembles IPF at a fundamental level; it recapitulates the gene expression patterns (ViP and IPF signatures), cytokine storm (IL15-centric), and the AT2 cytopathic changes, e.g., injury, DNA damage, arrest in a transient, damage-induced progenitor state, and senescence-associated secretory phenotype (SASP). These immunocytopathic features were induced in pre-clinical COVID models (ALO and hamster) and reversed with effective anti-CoV-2 therapeutics in hamsters. PPI-network analyses pinpointed ER stress as one of the shared early triggers of both diseases, and IHC studies validated the same in the lungs of deceased subjects with COVID-19 and SARS-CoV-2-challenged hamster lungs. Lungs from Interpretation: Like IPF, COVID-19 may be driven by injury-induced ER stress that culminates into progenitor state arrest and SASP in AT2 cells. The ViP signatures in monocytes may be key determinants of prognosis. The insights, signatures, disease models identified here are likely to spur the development of therapies for patients with IPF and other fibrotic interstitial lung diseases. Funding: This work was supported by the National Institutes for Health grants R01-GM138385 and AI155696 and funding from the Tobacco-Related disease Research Program (R01RG3780). One sentence summary: Severe COVID-19 triggers cellular processes seen in fibrosing Interstitial Lung Disease. Research in context: Evidence before this study:
Language	English
Publishing date	2022-07-18
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.11.28.470269
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Article ; Online: SPT6 loss permits the transdifferentiation of keratinocytes into an intestinal fate that resembles Barrett’s metaplasia

Daniella T. Vo / MacKenzie R. Fuller / Courtney Tindle / Mahitha Shree Anandachar / Soumita Das / Debashis Sahoo / Pradipta Ghosh

iScience, Vol 24, Iss 10, Pp 103121- (2021)

2021

Abstract: Summary: Transient depletion of the transcription elongation factor SPT6 in the keratinocyte has been recently shown to inhibit epidermal differentiation and stratification; instead, they transdifferentiate into a gut-like lineage. We show here that this ...

Abstract	Summary: Transient depletion of the transcription elongation factor SPT6 in the keratinocyte has been recently shown to inhibit epidermal differentiation and stratification; instead, they transdifferentiate into a gut-like lineage. We show here that this phenomenon of transdifferentiation recapitulates Barrett’s metaplasia, the only human pathophysiologic condition in which a stratified squamous epithelium that is injured due to chronic acid reflux is trans-committed into an intestinal fate. The evidence we present here not only lend support to the notion that the keratinocytes are potentially the cell of origin of Barrett’s metaplasia but also provide mechanistic insights linking transient acid exposure, downregulation of SPT6, stalled transcription of the master regulator of epidermal fate TP63, loss of epidermal fate, and metaplastic progression. Because Barrett’s metaplasia in the esophagus is a pre-neoplastic condition with no preclinical human models, these findings have a profound impact on the modeling Barrett’s metaplasia-in-a-dish.
Keywords	Molecular biology ; Cell biology ; Bioinformatics ; Science ; Q
Language	English
Publishing date	2021-10-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: COVID-19 lung disease shares driver AT2 cytopathic features with Idiopathic pulmonary fibrosis.

Sinha, Saptarshi / Castillo, Vanessa / Espinoza, Celia R / Tindle, Courtney / Fonseca, Ayden G / Dan, Jennifer M / Katkar, Gajanan D / Das, Soumita / Sahoo, Debashis / Ghosh, Pradipta

EBioMedicine

2022 Volume 82, Page(s) 104185

Abstract: Background: In the aftermath of Covid-19, some patients develop a fibrotic lung disease, i.e., post-COVID-19 lung disease (PCLD), for which we currently lack insights into pathogenesis, disease models, or treatment options.: Methods: Using an AI- ... ...

Abstract	Background: In the aftermath of Covid-19, some patients develop a fibrotic lung disease, i.e., post-COVID-19 lung disease (PCLD), for which we currently lack insights into pathogenesis, disease models, or treatment options. Methods: Using an AI-guided approach, we analyzed > 1000 human lung transcriptomic datasets associated with various lung conditions using two viral pandemic signatures (ViP and sViP) and one covid lung-derived signature. Upon identifying similarities between COVID-19 and idiopathic pulmonary fibrosis (IPF), we subsequently dissected the basis for such similarity from molecular, cytopathic, and immunologic perspectives using a panel of IPF-specific gene signatures, alongside signatures of alveolar type II (AT2) cytopathies and of prognostic monocyte-driven processes that are known drivers of IPF. Transcriptome-derived findings were used to construct protein-protein interaction (PPI) network to identify the major triggers of AT2 dysfunction. Key findings were validated in hamster and human adult lung organoid (ALO) pre-clinical models of COVID-19 using immunohistochemistry and qPCR. Findings: COVID-19 resembles IPF at a fundamental level; it recapitulates the gene expression patterns (ViP and IPF signatures), cytokine storm (IL15-centric), and the AT2 cytopathic changes, e.g., injury, DNA damage, arrest in a transient, damage-induced progenitor state, and senescence-associated secretory phenotype (SASP). These immunocytopathic features were induced in pre-clinical COVID models (ALO and hamster) and reversed with effective anti-CoV-2 therapeutics in hamsters. PPI-network analyses pinpointed ER stress as one of the shared early triggers of both diseases, and IHC studies validated the same in the lungs of deceased subjects with COVID-19 and SARS-CoV-2-challenged hamster lungs. Lungs from tg-mice, in which ER stress is induced specifically in the AT2 cells, faithfully recapitulate the host immune response and alveolar cytopathic changes that are induced by SARS-CoV-2. Interpretation: Like IPF, COVID-19 may be driven by injury-induced ER stress that culminates into progenitor state arrest and SASP in AT2 cells. The ViP signatures in monocytes may be key determinants of prognosis. The insights, signatures, disease models identified here are likely to spur the development of therapies for patients with IPF and other fibrotic interstitial lung diseases. Funding: This work was supported by the National Institutes for Health grants R01- GM138385 and AI155696 and funding from the Tobacco-Related disease Research Program (R01RG3780).
MeSH term(s)	Adult ; Animals ; COVID-19 ; Cytokine Release Syndrome ; Humans ; Idiopathic Pulmonary Fibrosis/genetics ; Idiopathic Pulmonary Fibrosis/metabolism ; Lung/pathology ; Mice ; SARS-CoV-2
Language	English
Publishing date	2022-07-20
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	2851331-9
ISSN	2352-3964
ISSN (online)	2352-3964
DOI	10.1016/j.ebiom.2022.104185
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Article ; Online: Anticancer pan-ErbB inhibitors reduce inflammation and tissue injury and exert broad-spectrum antiviral effects.

Saul, Sirle / Karim, Marwah / Ghita, Luca / Huang, Pei-Tzu / Chiu, Winston / Durán, Verónica / Lo, Chieh-Wen / Kumar, Sathish / Bhalla, Nishank / Leyssen, Pieter / Alem, Farhang / Boghdeh, Niloufar A / Tran, Do Hn / Cohen, Courtney A / Brown, Jacquelyn A / Huie, Kathleen E / Tindle, Courtney / Sibai, Mamdouh / Ye, Chengjin /

Khalil, Ahmed Magdy / Chiem, Kevin / Martinez-Sobrido, Luis / Dye, John M / Pinsky, Benjamin A / Ghosh, Pradipta / Das, Soumita / Solow-Cordero, David E / Jin, Jing / Wikswo, John P / Jochmans, Dirk / Neyts, Johan / De Jonghe, Steven / Narayanan, Aarthi / Einav, Shirit

The Journal of clinical investigation

2023 Volume 133, Issue 19

Abstract: Targeting host factors exploited by multiple viruses could offer broad-spectrum solutions for pandemic preparedness. Seventeen candidates targeting diverse functions emerged in a screen of 4,413 compounds for SARS-CoV-2 inhibitors. We demonstrated that ... ...

Abstract	Targeting host factors exploited by multiple viruses could offer broad-spectrum solutions for pandemic preparedness. Seventeen candidates targeting diverse functions emerged in a screen of 4,413 compounds for SARS-CoV-2 inhibitors. We demonstrated that lapatinib and other approved inhibitors of the ErbB family of receptor tyrosine kinases suppress replication of SARS-CoV-2, Venezuelan equine encephalitis virus (VEEV), and other emerging viruses with a high barrier to resistance. Lapatinib suppressed SARS-CoV-2 entry and later stages of the viral life cycle and showed synergistic effect with the direct-acting antiviral nirmatrelvir. We discovered that ErbB1, ErbB2, and ErbB4 bind SARS-CoV-2 S1 protein and regulate viral and ACE2 internalization, and they are required for VEEV infection. In human lung organoids, lapatinib protected from SARS-CoV-2-induced activation of ErbB-regulated pathways implicated in non-infectious lung injury, proinflammatory cytokine production, and epithelial barrier injury. Lapatinib suppressed VEEV replication, cytokine production, and disruption of blood-brain barrier integrity in microfluidics-based human neurovascular units, and reduced mortality in a lethal infection murine model. We validated lapatinib-mediated inhibition of ErbB activity as an important mechanism of antiviral action. These findings reveal regulation of viral replication, inflammation, and tissue injury via ErbBs and establish a proof of principle for a repurposed, ErbB-targeted approach to combat emerging viruses.
MeSH term(s)	Animals ; Humans ; Mice ; Antiviral Agents/pharmacology ; COVID-19 ; Cytokines ; Hepatitis C, Chronic ; Inflammation/drug therapy ; Lapatinib/pharmacology ; SARS-CoV-2
Chemical Substances	Antiviral Agents ; Cytokines ; Lapatinib (0VUA21238F)
Language	English
Publishing date	2023-10-02
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	3067-3
ISSN	1558-8238 ; 0021-9738
ISSN (online)	1558-8238
ISSN	0021-9738
DOI	10.1172/JCI169510
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Article: Anticancer pan-ErbB inhibitors reduce inflammation and tissue injury and exert broad-spectrum antiviral effects.

Khalil, Ahmed Magdy / Martinez-Sobrido, Luis / Dye, John M / Pinsky, Benjamin A / Ghosh, Pradipta / Das, Soumita / Solow-Cordero, David E / Jin, Jing / Wikswo, John P / Jochmans, Dirk / Neyts, Johan / Jonghe, Steven De / Narayanan, Aarthi / Einav, Shirit

bioRxiv : the preprint server for biology

2023

Abstract	Targeting host factors exploited by multiple viruses could offer broad-spectrum solutions for pandemic preparedness. Seventeen candidates targeting diverse functions emerged in a screen of 4,413 compounds for SARS-CoV-2 inhibitors. We demonstrated that lapatinib and other approved inhibitors of the ErbB family receptor tyrosine kinases suppress replication of SARS-CoV-2, Venezuelan equine encephalitis virus (VEEV), and other emerging viruses with a high barrier to resistance. Lapatinib suppressed SARS-CoV-2 entry and later stages of the viral life cycle and showed synergistic effect with the direct-acting antiviral nirmatrelvir. We discovered that ErbB1, 2 and 4 bind SARS-CoV-2 S1 protein and regulate viral and ACE2 internalization, and they are required for VEEV infection. In human lung organoids, lapatinib protected from SARS-CoV-2-induced activation of ErbB-regulated pathways implicated in non-infectious lung injury, pro-inflammatory cytokine production, and epithelial barrier injury. Lapatinib suppressed VEEV replication, cytokine production and disruption of the blood-brain barrier integrity in microfluidic-based human neurovascular units, and reduced mortality in a lethal infection murine model. We validated lapatinib-mediated inhibition of ErbB activity as an important mechanism of antiviral action. These findings reveal regulation of viral replication, inflammation, and tissue injury via ErbBs and establish a proof-of-principle for a repurposed, ErbB-targeted approach to combat emerging viruses.
Language	English
Publishing date	2023-05-10
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.05.15.444128
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