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Article: Orchestrating Resilience: How Neuropilin-2 and Macrophages Contribute to Cardiothoracic Disease.

Dhupar, Rajeev / Powers, Amy A / Eisenberg, Seth H / Gemmill, Robert M / Bardawil, Charles E / Udoh, Hannah M / Cubitt, Andrea / Nangle, Leslie A / Soloff, Adam C

Journal of clinical medicine

2024 Volume 13, Issue 5

Abstract: Immunity has evolved to balance the destructive nature of inflammation with wound healing to overcome trauma, infection, environmental insults, and rogue malignant cells. The inflammatory response is marked by overlapping phases of initiation, resolution, ...

Abstract	Immunity has evolved to balance the destructive nature of inflammation with wound healing to overcome trauma, infection, environmental insults, and rogue malignant cells. The inflammatory response is marked by overlapping phases of initiation, resolution, and post-resolution remodeling. However, the disruption of these events can lead to prolonged tissue damage and organ dysfunction, resulting long-term disease states. Macrophages are the archetypic phagocytes present within all tissues and are important contributors to these processes. Pleiotropic and highly plastic in their responses, macrophages support tissue homeostasis, repair, and regeneration, all while balancing immunologic self-tolerance with the clearance of noxious stimuli, pathogens, and malignant threats. Neuropilin-2 (Nrp2), a promiscuous co-receptor for growth factors, semaphorins, and integrins, has increasingly been recognized for its unique role in tissue homeostasis and immune regulation. Notably, recent studies have begun to elucidate the role of Nrp2 in both non-hematopoietic cells and macrophages with cardiothoracic disease. Herein, we describe the unique role of Nrp2 in diseases of the heart and lung, with an emphasis on Nrp2 in macrophages, and explore the potential to target Nrp2 as a therapeutic intervention.
Language	English
Publishing date	2024-03-01
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2662592-1
ISSN	2077-0383
ISSN	2077-0383
DOI	10.3390/jcm13051446
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Article ; Online: A triad of NRP2, DLX and p53 proteins in lung cancer metastasis.

Drabkin, Harry A / Starkova, Julia / Gemmill, Robert M

Oncotarget

2017 Volume 8, Issue 57, Page(s) 96464–96465

Language	English
Publishing date	2017-11-14
Publishing country	United States
Document type	Editorial
ZDB-ID	2560162-3
ISSN	1949-2553 ; 1949-2553
ISSN (online)	1949-2553
ISSN	1949-2553
DOI	10.18632/oncotarget.22097
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Article: Epigenetic Regulation of the Epithelial to Mesenchymal Transition in Lung Cancer.

Roche, Joëlle / Gemmill, Robert M / Drabkin, Harry A

Cancers

2017 Volume 9, Issue 7

Abstract: Lung cancer is the leading cause of cancer deaths worldwide. It is an aggressive and devastating cancer because of metastasis triggered by enhanced migration and invasion, and resistance to cytotoxic chemotherapy. The epithelial to mesenchymal transition ...

Abstract	Lung cancer is the leading cause of cancer deaths worldwide. It is an aggressive and devastating cancer because of metastasis triggered by enhanced migration and invasion, and resistance to cytotoxic chemotherapy. The epithelial to mesenchymal transition (EMT) is a fundamental developmental process that is reactivated in wound healing and a variety of diseases including cancer where it promotes migration/invasion and metastasis, resistance to treatment, and generation and maintenance of cancer stem cells. The induction of EMT is associated with reprogramming of the epigenome. This review focuses on major mechanisms of epigenetic regulation mainly in lung cancer with recent data on EZH2 (enhancer of zeste 2 polycomb repressive complex 2 subunit ), the catalytic subunit of the PRC2 (Polycomb Group PcG), that behaves as an oncogene in lung cancer associated with gene repression, non-coding RNAs and the epitranscriptome.
Language	English
Publishing date	2017-06-24
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2527080-1
ISSN	2072-6694
ISSN	2072-6694
DOI	10.3390/cancers9070072
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Article ; Online: Cholesterol and the development of clear-cell renal carcinoma.

Drabkin, Harry A / Gemmill, Robert M

Current opinion in pharmacology

2012 Volume 12, Issue 6, Page(s) 742–750

Abstract: The majority of kidney cancers are clear-cell carcinomas (ccRCC), characterized by the accumulation of cholesterol, cholesterol esters, other neutral lipids and glycogen. Rather than being a passive bystander, the clear-cell phenotype is suggested to be ... ...

Abstract	The majority of kidney cancers are clear-cell carcinomas (ccRCC), characterized by the accumulation of cholesterol, cholesterol esters, other neutral lipids and glycogen. Rather than being a passive bystander, the clear-cell phenotype is suggested to be a biomarker of deregulated cholesterol and lipid biosynthesis, which plays an important role in development of the disease. One clue to this relationship has come from the elucidation of the hereditary kidney cancer gene, TRC8, which functions partly to degrade key regulators of endogenous cholesterol and lipid biosynthesis. In addition, deregulation of the mevalonate pathway has been shown to play a key role in cellular transformation and invasion. These findings are supported by considerable epidemiologic data linking obesity and the deregulation of lipid biosynthesis to ccRCC.
MeSH term(s)	Animals ; Carcinoma, Renal Cell/etiology ; Carcinoma, Renal Cell/genetics ; Carcinoma, Renal Cell/pathology ; Cholesterol/metabolism ; Cholesterol Esters/metabolism ; Glycogen/metabolism ; Humans ; Kidney Neoplasms/etiology ; Kidney Neoplasms/genetics ; Kidney Neoplasms/pathology ; Lipids/biosynthesis ; Mevalonic Acid/metabolism ; Obesity/complications ; Receptors, Cell Surface/genetics
Chemical Substances	Cholesterol Esters ; Lipids ; RNF139 protein, human ; Receptors, Cell Surface ; Glycogen (9005-79-2) ; Cholesterol (97C5T2UQ7J) ; Mevalonic Acid (S5UOB36OCZ)
Language	English
Publishing date	2012-12
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2037057-X
ISSN	1471-4973 ; 1471-4892
ISSN (online)	1471-4973
ISSN	1471-4892
DOI	10.1016/j.coph.2012.08.002
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Article ; Online: Isoforms of Neuropilin-2 Denote Unique Tumor-Associated Macrophages in Breast Cancer.

Dhupar, Rajeev / Jones, Katherine E / Powers, Amy A / Eisenberg, Seth H / Ding, Kai / Chen, Fangyuan / Nasarre, Cecile / Cen, Zhanpeng / Gong, Yi-Nan / LaRue, Amanda C / Yeh, Elizabeth S / Luketich, James D / Lee, Adrian V / Oesterreich, Steffi / Lotze, Michael T / Gemmill, Robert M / Soloff, Adam C

Frontiers in immunology

2022 Volume 13, Page(s) 830169

Abstract: Tumor-associated macrophages (TAMs) exert profound influence over breast cancer progression, promoting immunosuppression, angiogenesis, and metastasis. Neuropilin-2 (NRP2), consisting of the NRP2a and NRP2b isoforms, is a co-receptor for heparin-binding ... ...

Abstract	Tumor-associated macrophages (TAMs) exert profound influence over breast cancer progression, promoting immunosuppression, angiogenesis, and metastasis. Neuropilin-2 (NRP2), consisting of the NRP2a and NRP2b isoforms, is a co-receptor for heparin-binding growth factors including VEGF-C and Class 3 Semaphorins. Selective upregulation in response to environmental stimuli and independent signaling pathways endow the NRP2 isoforms with unique functionality, with NRP2b promoting increased Akt signaling
MeSH term(s)	Animals ; Breast Neoplasms/pathology ; Female ; Humans ; Mice ; Neuropilin-1/genetics ; Neuropilin-2/genetics ; Neuropilin-2/metabolism ; Protein Isoforms ; Tumor-Associated Macrophages
Chemical Substances	Neuropilin-2 ; Protein Isoforms ; Neuropilin-1 (144713-63-3)
Language	English
Publishing date	2022-04-27
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2022.830169
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Article: The emerging role of class-3 semaphorins and their neuropilin receptors in oncology.

Nasarre, Patrick / Gemmill, Robert M / Drabkin, Harry A

OncoTargets and therapy

2014 Volume 7, Page(s) 1663–1687

Abstract: The semaphorins, discovered over 20 years ago, are a large family of secreted or transmembrane and glycophosphatidylinositol -anchored proteins initially identified as axon guidance molecules crucial for the development of the nervous system. It has now ... ...

Abstract	The semaphorins, discovered over 20 years ago, are a large family of secreted or transmembrane and glycophosphatidylinositol -anchored proteins initially identified as axon guidance molecules crucial for the development of the nervous system. It has now been established that they also play important roles in organ development and function, especially involving the immune, respiratory, and cardiovascular systems, and in pathological disorders, including cancer. During tumor progression, semaphorins can have both pro- and anti-tumor functions, and this has created complexities in our understanding of these systems. Semaphorins may affect tumor growth and metastases by directly targeting tumor cells, as well as indirectly by interacting with and influencing cells from the micro-environment and vasculature. Mechanistically, semaphorins, through binding to their receptors, neuropilins and plexins, affect pathways involved in cell adhesion, migration, invasion, proliferation, and survival. Importantly, neuropilins also act as co-receptors for several growth factors and enhance their signaling activities, while class 3 semaphorins may interfere with this. In this review, we focus on the secreted class 3 semaphorins and their neuropilin co-receptors in cancer, including aspects of their signaling that may be clinically relevant.
Language	English
Publishing date	2014-09-24
Publishing country	New Zealand
Document type	Journal Article ; Review
ZDB-ID	2495130-4
ISSN	1178-6930
ISSN	1178-6930
DOI	10.2147/OTT.S37744
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Article ; Online: Notes on the biology and distribution of the tribe Agallissini in North America (Coleoptera: Cerambycidae: Cerambycinae).

Austin, Thomas / Heffern, Daniel / Gemmill, Robert / Raber, Brian / Quinn, Mike

Zootaxa

2018 Volume 4457, Issue 3, Page(s) 444–454

Abstract: New distributional records, new larval host records, various collecting notes, and observations are reported for the North American species of the tribe Agallissini LeConte, 1873 (Coleoptera: Cerambycidae: Cerambycinae): Agallissus lepturoides (Duponchel ...

Abstract	New distributional records, new larval host records, various collecting notes, and observations are reported for the North American species of the tribe Agallissini LeConte, 1873 (Coleoptera: Cerambycidae: Cerambycinae): Agallissus lepturoides (Duponchel Chevrolat, 1841), Osmopleura chamaeropis (Horn, 1893), and Zagymnus clerinus (LeConte, 1873). The species are illustrated and distribution maps are provided.
MeSH term(s)	Animals ; Coleoptera ; North America
Language	English
Publishing date	2018-08-09
Publishing country	New Zealand
Document type	Journal Article
ISSN	1175-5334
ISSN (online)	1175-5334
DOI	10.11646/zootaxa.4457.3.6
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Article ; Online: Obesity, cholesterol, and clear-cell renal cell carcinoma (RCC).

Drabkin, Harry A / Gemmill, Robert M

Advances in cancer research

2010 Volume 107, Page(s) 39–56

Abstract: Multiple epidemiologic studies have linked the development of renal cancer to obesity. In this chapter, we begin with a review of selected population studies, followed by recent mechanistic discoveries that further link lipid deregulation to the RCC ... ...

Abstract	Multiple epidemiologic studies have linked the development of renal cancer to obesity. In this chapter, we begin with a review of selected population studies, followed by recent mechanistic discoveries that further link lipid deregulation to the RCC development. The upregulation of leptin and downregulation of adiponectin pathways in obesity fit well with our molecular understanding of RCC pathogenesis. In addition, two forms of hereditary RCC involve proteins, Folliculin and TRC8, that are positioned to coordinately regulate lipid and protein biosynthesis. Both of these biosynthetic pathways have important downstream consequences on HIF-1/2alpha levels and angiogenesis, key aspects in the disease pathogenesis. The role of lipid biology and its interface with protein translation regulation represents a new dimension in RCC research with potential therapeutic implications.
MeSH term(s)	Adiponectin/metabolism ; Basic Helix-Loop-Helix Transcription Factors/genetics ; Basic Helix-Loop-Helix Transcription Factors/metabolism ; Carcinoma, Renal Cell/etiology ; Carcinoma, Renal Cell/genetics ; Carcinoma, Renal Cell/metabolism ; Carrier Proteins/genetics ; Carrier Proteins/metabolism ; Cholesterol/metabolism ; Estrone/metabolism ; Humans ; Hypoxia-Inducible Factor 1, alpha Subunit/genetics ; Hypoxia-Inducible Factor 1, alpha Subunit/metabolism ; Kidney Neoplasms/etiology ; Kidney Neoplasms/genetics ; Kidney Neoplasms/metabolism ; Leptin/metabolism ; Lipids/biosynthesis ; Lipids/genetics ; Neoplastic Syndromes, Hereditary/epidemiology ; Neoplastic Syndromes, Hereditary/genetics ; Neoplastic Syndromes, Hereditary/metabolism ; Obesity/complications ; Obesity/metabolism ; Receptors, Cell Surface/genetics ; Receptors, Cell Surface/metabolism ; Sterol Regulatory Element Binding Proteins/metabolism
Chemical Substances	Adiponectin ; Basic Helix-Loop-Helix Transcription Factors ; Carrier Proteins ; HIF1A protein, human ; Hypoxia-Inducible Factor 1, alpha Subunit ; Leptin ; Lipids ; RNF139 protein, human ; Receptors, Cell Surface ; Sterol Regulatory Element Binding Proteins ; VBP1 protein, human ; endothelial PAS domain-containing protein 1 ; Estrone (2DI9HA706A) ; Cholesterol (97C5T2UQ7J)
Language	English
Publishing date	2010
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	127-2
ISSN	2162-5557 ; 0065-230X
ISSN (online)	2162-5557
ISSN	0065-230X
DOI	10.1016/S0065-230X(10)07002-8
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Article ; Online: Neuropilin-2b facilitates resistance to tyrosine kinase inhibitors in non-small cell lung cancer.

Dimou, Anastasios / Nasarre, Cecile / Peterson, Yuri K / Pagano, Rose / Gooz, Monika / Nasarre, Patrick / Drabkin, Harry A / Armeson, Kent E / Gibney, Barry C / Gemmill, Robert M / Denlinger, Chadrick E

The Journal of thoracic and cardiovascular surgery

2020 Volume 162, Issue 2, Page(s) 463–473

Abstract: Objective: Innate and acquired resistance is the principle factor limiting the efficacy of tyrosine kinase inhibitors in lung cancer. We have observed a dramatic upregulation of the cell surface co-receptor neuropilin-2b in lung cancers clinically ... ...

Abstract	Objective: Innate and acquired resistance is the principle factor limiting the efficacy of tyrosine kinase inhibitors in lung cancer. We have observed a dramatic upregulation of the cell surface co-receptor neuropilin-2b in lung cancers clinically treated with tyrosine kinase inhibitors correlating with acquired resistance. We hypothesize that neuropilin-2b plays a functional role in acquired tyrosine kinase inhibitor resistance. Methods: Non-small cell lung cancer proliferation and survival were determined during chronic tyrosine kinase inhibitor exposure in the presence or absence of neuropilin-2b knock-down. Interactions of neuropilin-2a and neuropilin-2b isoforms with PTEN and GSK3β were assessed by immunoprecipitation. Neuropilin-2a and neuropilin-2b mutants deleted for their cytoplasmic domains were used to identify regions responsible for neuropilin-2b-GSK3β interaction. Because GSK3β is known to phosphorylate and degrade PTEN, phospho-PTEN and total PTEN levels were assessed after transfection of neuropilin-2a and neuropilin-2b wild-type and mutant constructs. Results: Non-small cell lung cancer cells chronically treated with gefitinib or osimertinib developed drug resistance and exhibited logarithmic growth in the presence of endothelial growth factor receptor tyrosine kinase inhibitors. However, neuropilin-2b knockdown cells remained sensitive to gefitinib. Likewise, neuropilin-2b knockdown suppressed and neuropilin-2a knockdown enhanced cellular migration. Acquired drug resistance and cell migration correlated with neuropilin-2b-dependent AKT activation with the intermediate step of GSK3β-dependent PTEN degradation. A specific binding site for GSK3β on the cytoplasmic domain of neuropilin-2b was identified with truncated protein constructs and computer modeling. Conclusions: Neuropilin-2b facilitates non-small cell lung cancer resistance to tyrosine kinase inhibitors, and this biological effect relates to AKT activation. Neuropilin-2b GSK3β interactions appear to be essential for PTEN degradation and AKT activation in lung cancer cells. Disruption of the neuropilin-2b GSK3β interaction may represent a novel treatment strategy to preserve sensitivity to tyrosine kinase inhibitors in non-small cell lung cancer.
MeSH term(s)	A549 Cells ; Acrylamides/pharmacology ; Aniline Compounds/pharmacology ; Antineoplastic Agents/pharmacology ; Carcinoma, Non-Small-Cell Lung/drug therapy ; Carcinoma, Non-Small-Cell Lung/enzymology ; Carcinoma, Non-Small-Cell Lung/genetics ; Carcinoma, Non-Small-Cell Lung/pathology ; Cell Movement/drug effects ; Cell Proliferation/drug effects ; Drug Resistance, Neoplasm ; Enzyme Activation ; Gefitinib/pharmacology ; Glycogen Synthase Kinase 3 beta/metabolism ; Humans ; Lung Neoplasms/drug therapy ; Lung Neoplasms/enzymology ; Lung Neoplasms/genetics ; Lung Neoplasms/pathology ; Neoplasm Invasiveness ; Neuropilin-2/genetics ; Neuropilin-2/metabolism ; PTEN Phosphohydrolase/metabolism ; Phosphorylation ; Protein Kinase Inhibitors/pharmacology ; Proteolysis ; Proto-Oncogene Proteins c-akt/metabolism
Chemical Substances	Acrylamides ; Aniline Compounds ; Antineoplastic Agents ; Neuropilin-2 ; Protein Kinase Inhibitors ; neuropilin-2, human ; osimertinib (3C06JJ0Z2O) ; GSK3B protein, human (EC 2.7.11.1) ; Glycogen Synthase Kinase 3 beta (EC 2.7.11.1) ; Proto-Oncogene Proteins c-akt (EC 2.7.11.1) ; PTEN Phosphohydrolase (EC 3.1.3.67) ; PTEN protein, human (EC 3.1.3.67) ; Gefitinib (S65743JHBS)
Language	English
Publishing date	2020-05-25
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	3104-5
ISSN	1097-685X ; 0022-5223
ISSN (online)	1097-685X
ISSN	0022-5223
DOI	10.1016/j.jtcvs.2020.03.166
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Article: CD47 is a direct target of SNAI1 and ZEB1 and its blockade activates the phagocytosis of breast cancer cells undergoing EMT.

Noman, Muhammad Zaeem / Van Moer, Kris / Marani, Vanessa / Gemmill, Robert M / Tranchevent, Léon-Charles / Azuaje, Francisco / Muller, Arnaud / Chouaib, Salem / Thiery, Jean Paul / Berchem, Guy / Janji, Bassam

Oncoimmunology

2018 Volume 7, Issue 4, Page(s) e1345415

Abstract: We report that CD47 was upregulated in different EMT-activated human breast cancer cells versus epithelial MCF7 cells. Overexpression of SNAI1 or ZEB1 in epithelial MCF7 cells activated EMT and upregulated CD47 while siRNA-mediated targeting of SNAI1 or ... ...

Abstract	We report that CD47 was upregulated in different EMT-activated human breast cancer cells versus epithelial MCF7 cells. Overexpression of SNAI1 or ZEB1 in epithelial MCF7 cells activated EMT and upregulated CD47 while siRNA-mediated targeting of SNAI1 or ZEB1 in mesenchymal MDA-MB-231 cells reversed EMT and strongly decreased CD47. Mechanistically, SNAI1 and ZEB1 upregulated CD47 by binding directly to E-boxes in the human CD47 promoter. TCGA and METABRIC data sets from breast cancer patients revealed that CD47 correlated with SNAI1 and Vimentin. At functional level, different EMT-activated breast cancer cells were less efficiently phagocytosed by macrophages vs. MCF7 cells. The phagocytosis of EMT-activated cells was rescued by using CD47 blocking antibody or by genetic targeting of SNAI1, ZEB1 or CD47. These results provide a rationale for an innovative preclinical combination immunotherapy based on PD-1/PD-L1 and CD47 blockade along with EMT inhibitors in patients with highly aggressive, mesenchymal, and metastatic breast cancer.
Language	English
Publishing date	2018-02-15
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	2645309-5
ISSN	2162-402X ; 2162-4011
ISSN (online)	2162-402X
ISSN	2162-4011
DOI	10.1080/2162402X.2017.1345415
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