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Article ; Online: The 3D's of Neural Phenotypes in Oral Cancer: Distance, Diameter, and Density.

D'Silva, Nisha J / Perez-Pacheco, Cindy / Schmitd, Ligia B

Advanced biology

2022 Volume 7, Issue 2, Page(s) e2200188

Abstract: Squamous cell carcinoma of the oral cavity (OSCC) is the most common type of head and neck cancer; survival is poor, and response to treatment varies. Metastasis or recurrence in the regional lymph nodes is associated with poor survival. Consequently, ... ...

Abstract	Squamous cell carcinoma of the oral cavity (OSCC) is the most common type of head and neck cancer; survival is poor, and response to treatment varies. Metastasis or recurrence in the regional lymph nodes is associated with poor survival. Consequently, overt or occult spread to the lymph nodes is used to identify patients who will receive adjuvant radiation therapy. Perineural invasion and the diameter of nerves exhibiting perineural invasion have also been suggested to be of prognostic significance. The explosion of interest in cancer neuroscience in the last two decades has led to novel biological insights into interactions between nerves and tumor cells. However, the criteria for defining perineural invasion have lagged behind current knowledge. It is important to re-evaluate the concept of perineural invasion and identify other neural phenotypes in OSCC that can impact treatment selection and prognosis. In addition to perineural invasion, neural phenotypes that are of potential relevance to tumor progression include nerve-tumor distance, nerve diameter, and nerve density. This manuscript discusses the translational significance of recent mechanistic studies on the progression of oral cancer.
MeSH term(s)	Humans ; Neoplasm Invasiveness ; Mouth Neoplasms ; Prognosis ; Head and Neck Neoplasms ; Lymph Nodes/pathology
Language	English
Publishing date	2022-11-14
Publishing country	Germany
Document type	Journal Article ; Review ; Research Support, N.I.H., Extramural
ISSN	2701-0198
ISSN (online)	2701-0198
DOI	10.1002/adbi.202200188
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Article ; Online: Nerve density in cancer: Less is better.

Schmitd, Ligia B / Perez-Pacheco, Cindy / D'Silva, Nisha J

FASEB bioAdvances

2021 Volume 3, Issue 10, Page(s) 773–786

Abstract: The density of nerves in cancer is emerging as a relevant clinical parameter for patient survival. Nerves in the tumor microenvironment have been associated with poor survival and recurrence, particularly if involved in perineural invasion. However, ... ...

Abstract	The density of nerves in cancer is emerging as a relevant clinical parameter for patient survival. Nerves in the tumor microenvironment have been associated with poor survival and recurrence, particularly if involved in perineural invasion. However, usually only a few nerves inside a tumor are affected by perineural invasion, while most nerves are not. Mechanistic studies have shown nerve-secreted factors promote tumor growth and invasion thereby making tumors more aggressive. Therefore, the overall number of nerves in the tumor microenvironment should be more representative of the nerve-tumor biological interaction than perineural invasion. This review summarizes the available clinical information about nerve density as a measure of clinical outcome in cancer and explores the mechanisms underlying nerve density in cancer, specifically, neurogenesis, axonogenesis, and neurotropism.
Language	English
Publishing date	2021-07-11
Publishing country	United States
Document type	Journal Article ; Review
ISSN	2573-9832
ISSN (online)	2573-9832
DOI	10.1096/fba.2021-00046
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Article: The chick chorioallantoic membrane In Vivo model to assess perineural invasion in head and neck cancer

Schmitd, Ligia B / Banerjee, Rajat / D’Silva, Nisha J / Liu, Min / Scanlon, Christina S

Journal of visualized experiments. 2019 June 21, , no. 148

2019

Abstract: Perineural invasion is a phenotype in which cancer surrounds or invades the nerves. It is associated with poor clinical outcome for head and neck squamous cell carcinoma and other cancers. Mechanistic studies have shown that the molecular crosstalk ... ...

Abstract	Perineural invasion is a phenotype in which cancer surrounds or invades the nerves. It is associated with poor clinical outcome for head and neck squamous cell carcinoma and other cancers. Mechanistic studies have shown that the molecular crosstalk between nerves and tumor cells occurs prior to physical interaction. There are only a few in vivo models to study perineural invasion, especially to investigate early progression, before physical nerve-tumor interactions occur. The chick chorioallantoic membrane model has been used to study cancer invasion, because the basement membrane of the chorionic epithelium mimics that of human epithelial tissue. Here we repurposed the chick chorioallantoic membrane model to investigate perineural invasion, grafting rat dorsal root ganglia and human head and neck squamous cell carcinoma cells onto the chorionic epithelium. We have demonstrated how this model can be useful to evaluate the ability of cancer cells to invade neural tissue in vivo.
Keywords	basement membrane ; chicks ; chorioallantoic membrane ; ganglia ; head ; head and neck neoplasms ; humans ; models ; neck ; neoplasm cells ; nerve tissue ; phenotype ; rats ; squamous cell carcinoma
Language	English
Dates of publication	2019-0621
Size	p. e59296.
Publishing place	Journal of Visualized Experiments
Document type	Article
ISSN	1940-087X
DOI	10.3791/59296
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: The Chick Chorioallantoic Membrane In Vivo Model to Assess Perineural Invasion in Head and Neck Cancer.

Schmitd, Ligia B / Liu, Min / Scanlon, Christina S / Banerjee, Rajat / D'Silva, Nisha J

Journal of visualized experiments : JoVE

2019 , Issue 148

Abstract	Perineural invasion is a phenotype in which cancer surrounds or invades the nerves. It is associated with poor clinical outcome for head and neck squamous cell carcinoma and other cancers. Mechanistic studies have shown that the molecular crosstalk between nerves and tumor cells occurs prior to physical interaction. There are only a few in vivo models to study perineural invasion, especially to investigate early progression, before physical nerve-tumor interactions occur. The chick chorioallantoic membrane model has been used to study cancer invasion, because the basement membrane of the chorionic epithelium mimics that of human epithelial tissue. Here we repurposed the chick chorioallantoic membrane model to investigate perineural invasion, grafting rat dorsal root ganglia and human head and neck squamous cell carcinoma cells onto the chorionic epithelium. We have demonstrated how this model can be useful to evaluate the ability of cancer cells to invade neural tissue in vivo.
MeSH term(s)	Animals ; Cell Line, Tumor ; Chick Embryo ; Chorioallantoic Membrane/pathology ; Disease Models, Animal ; Ganglia, Spinal/pathology ; Head and Neck Neoplasms/pathology ; Humans ; Neoplasm Invasiveness ; Rats
Language	English
Publishing date	2019-06-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Video-Audio Media
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/59296
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Article: Sarm1 is not necessary for activation of neuron-intrinsic growth programs yet required for the Schwann cell repair response and peripheral nerve regeneration.

bioRxiv : the preprint server for biology

2024

Abstract: Upon peripheral nervous system (PNS) injury, severed axons undergo rapid SARM1-dependent Wallerian degeneration (WD). In mammals, the role of SARM1 in PNS regeneration, however, is unknown. Here we demonstrate ... ...

Abstract	Upon peripheral nervous system (PNS) injury, severed axons undergo rapid SARM1-dependent Wallerian degeneration (WD). In mammals, the role of SARM1 in PNS regeneration, however, is unknown. Here we demonstrate that
Language	English
Publishing date	2024-04-17
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.04.583374
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Article ; Online: Increased Nerve Density Adversely Affects Outcome in Oral Cancer.

Perez-Pacheco, Cindy / Schmitd, Ligia B / Furgal, Allison / Bellile, Emily L / Liu, Min / Fattah, Aya / Gonzalez-Maldonado, Laura / Unsworth, Shelby P / Wong, Sunny Y / Rozek, Laura S / Rao, Arvind / Wolf, Gregory T / Taylor, Jeremy M G / Casper, Keith / Mierzwa, Michelle / D'Silva, Nisha J

Clinical cancer research : an official journal of the American Association for Cancer Research

2023 Volume 29, Issue 13, Page(s) 2501–2512

Abstract: Purpose: Perineural invasion (PNI) in oral cavity squamous cell carcinoma (OSCC) is associated with poor survival. Because of the risk of recurrence, patients with PNI receive additional therapies after surgical resection. Mechanistic studies have shown ...

Abstract	Purpose: Perineural invasion (PNI) in oral cavity squamous cell carcinoma (OSCC) is associated with poor survival. Because of the risk of recurrence, patients with PNI receive additional therapies after surgical resection. Mechanistic studies have shown that nerves in the tumor microenvironment promote aggressive tumor growth. Therefore, in this study, we evaluated whether nerve density (ND) influences tumor growth and patient survival. Moreover, we assessed the reliability of artificial intelligence (AI) in evaluating ND. Experimental design: To investigate whether increased ND in OSCC influences patient outcome, we performed survival analyses. Tissue sections of OSCC from 142 patients were stained with hematoxylin and eosin and IHC stains to detect nerves and tumor. ND within the tumor bulk and in the adjacent 2 mm was quantified; normalized ND (NND; bulk ND/adjacent ND) was calculated. The impact of ND on tumor growth was evaluated in chick chorioallantoic-dorsal root ganglia (CAM-DRG) and murine surgical denervation models. Cancer cells were grafted and tumor size quantified. Automated nerve detection, applying the Halo AI platform, was compared with manual assessment. Results: Disease-specific survival decreased with higher intratumoral ND and NND in tongue SCC. Moreover, NND was associated with worst pattern-of-invasion and PNI. Increasing the number of DRG, in the CAM-DRG model, increased tumor size. Reduction of ND by denervation in a murine model decreased tumor growth. Automated and manual detection of nerves showed high concordance, with an F1 score of 0.977. Conclusions: High ND enhances tumor growth, and NND is an important prognostic factor that could influence treatment selection for aggressive OSCC. See related commentary by Hondermarck and Jiang, p. 2342.
MeSH term(s)	Humans ; Animals ; Mice ; Artificial Intelligence ; Reproducibility of Results ; Neoplasm Invasiveness ; Mouth Neoplasms/pathology ; Carcinoma, Squamous Cell/pathology ; Squamous Cell Carcinoma of Head and Neck ; Head and Neck Neoplasms ; Tumor Microenvironment
Language	English
Publishing date	2023-04-11
Publishing country	United States
Document type	Research Support, N.I.H., Extramural ; Journal Article ; Research Support, Non-U.S. Gov't ; Comment
ZDB-ID	1225457-5
ISSN	1557-3265 ; 1078-0432
ISSN (online)	1557-3265
ISSN	1078-0432
DOI	10.1158/1078-0432.CCR-22-3496
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Zs.A 4223: Show issues

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Article ; Online: Spatial and Transcriptomic Analysis of Perineural Invasion in Oral Cancer.

Schmitd, Ligia B / Perez-Pacheco, Cindy / Bellile, Emily L / Wu, Weisheng / Casper, Keith / Mierzwa, Michelle / Rozek, Laura S / Wolf, Gregory T / Taylor, Jeremy M G / D'Silva, Nisha J

Clinical cancer research : an official journal of the American Association for Cancer Research

2022 Volume 28, Issue 16, Page(s) 3557–3572

Abstract: Purpose: Perineural invasion (PNI), a common occurrence in oral squamous cell carcinomas, is associated with poor survival. Consequently, these tumors are treated aggressively. However, diagnostic criteria of PNI vary and its role as an independent ... ...

Abstract	Purpose: Perineural invasion (PNI), a common occurrence in oral squamous cell carcinomas, is associated with poor survival. Consequently, these tumors are treated aggressively. However, diagnostic criteria of PNI vary and its role as an independent predictor of prognosis has not been established. To address these knowledge gaps, we investigated spatial and transcriptomic profiles of PNI-positive and PNI-negative nerves. Experimental design: Tissue sections from 142 patients were stained with S100 and cytokeratin antibodies. Nerves were identified in two distinct areas: tumor bulk and margin. Nerve diameter and nerve-to-tumor distance were assessed; survival analyses were performed. Spatial transcriptomic analysis of nerves at varying distances from tumor was performed with NanoString GeoMx Digital Spatial Profiler Transcriptomic Atlas. Results: PNI is an independent predictor of poor prognosis among patients with metastasis-free lymph nodes. Patients with close nerve-tumor distance have poor outcomes even if diagnosed as PNI negative using current criteria. Patients with large nerve(s) in the tumor bulk survive poorly, suggesting that even PNI-negative nerves facilitate tumor progression. Diagnostic criteria were supported by spatial transcriptomic analyses of >18,000 genes; nerves in proximity to cancer exhibit stress and growth response changes that diminish with increasing nerve-tumor distance. These findings were validated in vitro and in human tissue. Conclusions: This is the first study in human cancer with high-throughput gene expression analysis in nerves with striking correlations between transcriptomic profile and clinical outcomes. Our work illuminates nerve-cancer interactions suggesting that cancer-induced injury modulates neuritogenesis, and supports reclassification of PNI based on nerve-tumor distance rather than current subjective criteria.
MeSH term(s)	Head and Neck Neoplasms/pathology ; Humans ; Keratins ; Mouth Neoplasms/genetics ; Mouth Neoplasms/pathology ; Neoplasm Invasiveness/genetics ; Neoplasm Invasiveness/pathology ; Neoplasm Staging ; Peripheral Nerves/pathology ; Prognosis ; Retrospective Studies ; Transcriptome
Chemical Substances	Keratins (68238-35-7)
Language	English
Publishing date	2022-07-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	1225457-5
ISSN	1557-3265 ; 1078-0432
ISSN (online)	1557-3265
ISSN	1078-0432
DOI	10.1158/1078-0432.CCR-21-4543
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Article ; Online: Phosphorylation of TRIP13 at Y56 induces radiation resistance but sensitizes head and neck cancer to cetuximab.

Banerjee, Rajat / Liu, Min / Bellile, Emily / Schmitd, Ligia B / Goto, Mitsuo / Hutchinson, Marsha-Kay N D / Singh, Priyanka / Zhang, Shuang / Damodaran, Dilna P V / Nyati, Mukesh K / Spector, Matthew E / Ward, Brent / Wolf, Gregory / Casper, Keith / Mierzwa, Michelle / D'Silva, Nisha J

Molecular therapy : the journal of the American Society of Gene Therapy

2021 Volume 30, Issue 1, Page(s) 468–484

Abstract: Radiation therapy, a mainstay of treatment for head and neck cancer, is not always curative due to the development of treatment resistance; additionally, multi-institutional trials have questioned the efficacy of concurrent radiation with cetuximab, the ... ...

Abstract	Radiation therapy, a mainstay of treatment for head and neck cancer, is not always curative due to the development of treatment resistance; additionally, multi-institutional trials have questioned the efficacy of concurrent radiation with cetuximab, the epidermal growth factor receptor (EGFR) inhibitor. We unraveled a mechanism for radiation resistance; that is, radiation induces EGFR, which phosphorylates TRIP13 (thyroid hormone receptor interactor 13) on tyrosine 56. Phosphorylated (phospho-)TRIP13 promotes non-homologous end joining (NHEJ) repair to induce radiation resistance. NHEJ is the main repair pathway for radiation-induced DNA damage. Tumors expressing high TRIP13 do not respond to radiation but are sensitive to cetuximab or cetuximab combined with radiation. Suppression of phosphorylation of TRIP13 at Y56 abrogates these effects. These findings show that EGFR-mediated phosphorylation of TRIP13 at Y56 is a vital mechanism of radiation resistance. Notably, TRIP13-pY56 could be used to predict the response to radiation or cetuximab and could be explored as an actionable target.
MeSH term(s)	ATPases Associated with Diverse Cellular Activities/metabolism ; Cell Cycle Proteins/metabolism ; Cell Line, Tumor ; Cetuximab/metabolism ; Cetuximab/pharmacology ; DNA End-Joining Repair ; Head and Neck Neoplasms/drug therapy ; Head and Neck Neoplasms/genetics ; Head and Neck Neoplasms/radiotherapy ; Humans ; Phosphorylation
Chemical Substances	Cell Cycle Proteins ; ATPases Associated with Diverse Cellular Activities (EC 3.6.4.-) ; TRIP13 protein, human (EC 3.6.4.-) ; Cetuximab (PQX0D8J21J)
Language	English
Publishing date	2021-06-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2010592-7
ISSN	1525-0024 ; 1525-0016
ISSN (online)	1525-0024
ISSN	1525-0016
DOI	10.1016/j.ymthe.2021.06.009
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Zs.A 5640: Show issues

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Article ; Online: Redefining Perineural Invasion: Integration of Biology With Clinical Outcome.

Schmitd, Ligia B / Beesley, Lauren J / Russo, Nickole / Bellile, Emily L / Inglehart, Ronald C / Liu, Min / Romanowicz, Genevieve / Wolf, Gregory T / Taylor, Jeremy M G / D'Silva, Nisha J

Neoplasia (New York, N.Y.)

2018 Volume 20, Issue 7, Page(s) 657–667

Abstract: A diagnosis of perineural invasion (PNI), defined as cancer within or surrounding at least 33% of the nerve, leads to selection of aggressive treatment in squamous cell carcinoma (SCC). Recent mechanistic studies show that cancer and nerves interact ... ...

Abstract	A diagnosis of perineural invasion (PNI), defined as cancer within or surrounding at least 33% of the nerve, leads to selection of aggressive treatment in squamous cell carcinoma (SCC). Recent mechanistic studies show that cancer and nerves interact prior to physical contact. The purpose of this study was to explore cancer-nerve interactions relative to clinical outcome. Biopsy specimens from 71 patients with oral cavity SCC were stained with hematoxylin and eosin and immunohistochemical (IHC; cytokeratin, S100, GAP43, Tuj1) stains. Using current criteria, PNI detection was increased with IHC. Overall survival (OS) tended to be poor for patients with PNI (P = .098). OS was significantly lower for patients with minimum tumor-nerve distance smaller than 5 μm (P = .011). The estimated relative death rate decreased as the nerve-tumor distance increased; there was a gradual drop off in death rate from distance equal to zero that stabilized around 500 μm. In PNI-negative patients, nerve diameter was significantly related to OS (HR 2.88, 95%CI[1.11,7.49]). Among PNI-negative nerves, larger nerve-tumor distance and smaller nerve diameter were significantly related to better OS, even when adjusting for T-stage and age (HR 0.82, 95% CI[0.72,0.92]; HR 1.27, 95% CI[1.00,1.62], respectively). GAP43, a marker for neuronal outgrowth, stained less than Tuj1 in nerves at greater distances from tumor (OR 0.76, 95% CI[0.73,0.79]); more GAP43 staining was associated with PNI. Findings from a small group of patients suggest that nerve parameters other than presence of PNI can influence outcome and that current criteria of PNI need to be re-evaluated to integrate recent biological discoveries.
MeSH term(s)	Aged ; Carcinoma, Squamous Cell/metabolism ; Carcinoma, Squamous Cell/mortality ; Carcinoma, Squamous Cell/pathology ; Disease Progression ; Female ; Humans ; Kaplan-Meier Estimate ; Male ; Middle Aged ; Neoplasm Grading ; Neoplasm Invasiveness ; Neoplasm Staging ; Neoplasms, Nerve Tissue/metabolism ; Neoplasms, Nerve Tissue/secondary ; Odds Ratio ; Proportional Hazards Models ; Recurrence
Language	English
Publishing date	2018-05-23
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1483840-0
ISSN	1476-5586 ; 1522-8002
ISSN (online)	1476-5586
ISSN	1522-8002
DOI	10.1016/j.neo.2018.04.005
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Zs.A 5203: Show issues

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Article ; Online: Squamous cell carcinoma subverts adjacent histologically normal epithelium to promote lateral invasion.

Singh, Priyanka / Banerjee, Rajat / Piao, Songlin / Costa de Medeiros, Marcell / Bellile, Emily / Liu, Min / Damodaran Puthiya Veettil, Dilna / Schmitd, Ligia B / Russo, Nickole / Danella, Erika / Inglehart, Ronald C / Pineault, Kyriel M / Wellik, Deneen M / Wolf, Greg / D'Silva, Nisha J

The Journal of experimental medicine

2017 Volume 218, Issue 6

Abstract: Recurrent and new tumors, attributed in part to lateral invasion, are frequent in squamous cell carcinomas and lead to poor survival. We identified a mechanism by which cancer subverts adjacent histologically normal epithelium to enable small clusters of ...

Abstract	Recurrent and new tumors, attributed in part to lateral invasion, are frequent in squamous cell carcinomas and lead to poor survival. We identified a mechanism by which cancer subverts adjacent histologically normal epithelium to enable small clusters of cancer cells to burrow undetected under adjacent histologically normal epithelium. We show that suppression of DMBT1 within cancer promotes aggressive invasion and metastasis in vivo and is associated with metastasis in patients. Cancer cells via TGFβ1 and TNFα also suppress DMBT1 in adjacent histologically normal epithelium, thereby subverting it to promote invasion of a small population of tumor cells. The sufficiency of DMBT1 in this process is demonstrated by significantly higher satellite tumor nests in Dmbt1-/- compared with wild-type mice. Moreover, in patients, invasion of small tumor nests under adjacent histologically normal epithelium is associated with increased risk for recurrence and shorter disease-free survival. This study demonstrates a crucial role of adjacent histologically normal epithelium in invasion and its important role in the tumor microenvironment and opens new possibilities for therapeutic strategies that reduce tumor recurrence.
MeSH term(s)	Animals ; Calcium-Binding Proteins/metabolism ; Carcinoma, Squamous Cell/metabolism ; Carcinoma, Squamous Cell/pathology ; Cell Line, Tumor ; Disease-Free Survival ; Epithelium/metabolism ; Epithelium/pathology ; Humans ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Neoplasm Invasiveness/pathology ; Neoplasm Recurrence, Local/metabolism ; Neoplasm Recurrence, Local/pathology ; Tumor Microenvironment/physiology
Chemical Substances	Calcium-Binding Proteins
Language	English
Publishing date	2017-10-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20200944
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