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Article: Photoacoustic Imaging as a Novel Non-Invasive Biomarker to Assess Intestinal Tissue Oxygenation and Motility in Neonatal Rats.

Weis, Victoria G / Cruz-Diaz, Nildris / Rauh, Jessica L / Ellison, Maryssa A / Yamaleyeva, Liliya M / Welch, Cherrie D / Zeller, Kristen A / Weis, Jared A

bioRxiv : the preprint server for biology

2023

Language	English
Publishing date	2023-06-27
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.06.27.545971
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Article ; Online: Photoacoustic Imaging as a Novel Non-invasive Biomarker to Assess Intestinal Tissue Oxygenation and Motility in Neonatal Rats.

Weis, Victoria G / Cruz-Diaz, Nildris / Rauh, Jessica L / Ellison, Maryssa A / Yamaleyeva, Liliya M / Welch, Cherrie D / Zeller, Kristen A / Weis, Jared A

Journal of pediatric surgery

2023 Volume 59, Issue 3, Page(s) 528–536

Abstract: Background: Within the premature infant intestine, oxygenation and motility play key physiological roles in healthy development and disease such as necrotizing enterocolitis. To date, there are limited techniques to reliably assess these physiological ... ...

Abstract	Background: Within the premature infant intestine, oxygenation and motility play key physiological roles in healthy development and disease such as necrotizing enterocolitis. To date, there are limited techniques to reliably assess these physiological functions that are also clinically feasible for critically ill infants. To address this clinical need, we hypothesized that photoacoustic imaging (PAI) can provide non-invasive assessment of intestinal tissue oxygenation and motility to characterize intestinal physiology and health. Methods: Ultrasound and photoacoustic images were acquired in 2-day and 4-day old neonatal rats. For PAI assessment of intestinal tissue oxygenation, an inspired gas challenge was performed using hypoxic, normoxic, and hyperoxic inspired oxygen (FiO2). For intestinal motility, oral administration of ICG contrast agent was used to compare control animals to an experimental model of loperamide-induced intestinal motility inhibition. Results: PAI demonstrated progressive increases in oxygen saturation (sO2) as FiO2 increased, while the pattern of oxygen localization remained relatively consistent in both 2-day and 4-day old neonatal rats. Analysis of intraluminal ICG contrast enhanced PAI images yielded a map of the motility index in control and loperamide treated rats. From PAI analysis, loperamide significantly inhibited intestinal motility, with a 32.6% decrease in intestinal motility index scores in 4-day old rats. Conclusion: These data establish the feasibility and application of PAI to non-invasively and quantitatively measure intestinal tissue oxygenation and motility. This proof-of-concept study is an important first step in developing and optimizing photoacoustic imaging to provide valuable insight into intestinal health and disease to improve the care of premature infants.
MeSH term(s)	Humans ; Infant, Newborn ; Rats ; Animals ; Animals, Newborn ; Photoacoustic Techniques/methods ; Loperamide ; Oxygen ; Intestines/diagnostic imaging ; Biomarkers
Chemical Substances	Loperamide (6X9OC3H4II) ; Oxygen (S88TT14065) ; Biomarkers
Language	English
Publishing date	2023-09-27
Publishing country	United States
Document type	Journal Article
ZDB-ID	80165-3
ISSN	1531-5037 ; 0022-3468
ISSN (online)	1531-5037
ISSN	0022-3468
DOI	10.1016/j.jpedsurg.2023.09.034
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Article: Photoacoustic Imaging for Non-Invasive Assessment of Physiological Biomarkers of Intestinal Injury in Experimental Necrotizing Enterocolitis.

Weis, Jared A / Rauh, Jessica L / Ellison, Maryssa A / Cruz-Diaz, Nildris / Yamaleyeva, Liliya M / Welch, Cherrie D / Zeller, Kristen A / Weis, Victoria G

bioRxiv : the preprint server for biology

2023

Abstract: Background: Necrotizing enterocolitis (NEC) is an often-lethal disease of the premature infants' intestinal tract that is exacerbated by significant difficulties in early and accurate diagnosis. In NEC disease, the intestine often exhibits hypoperfusion ...

Abstract	Background: Necrotizing enterocolitis (NEC) is an often-lethal disease of the premature infants' intestinal tract that is exacerbated by significant difficulties in early and accurate diagnosis. In NEC disease, the intestine often exhibits hypoperfusion and dysmotility, which contributes to advanced disease pathogenesis. However, these physiological features cannot be accurately and quantitively assessed within the current constraints of imaging modalities frequently used in the clinic (plain film X-ray and ultrasound). We have previously demonstrated the ability of photoacoustic imaging (PAI) to non-invasively and quantitively assess intestinal tissue oxygenation and motility in a healthy neonatal rat model. As a first-in-disease application, we evaluated NEC pathogenesis using PAI to assess intestinal health biomarkers in a preclinical neonatal rat experimental model of NEC. Methods: NEC was induced in neonatal rat pups from birth to 4 days old via hypertonic formula feeding, full-body hypoxic stress, and lipopolysaccharide administration to mimic bacterial colonization. Healthy breastfed (BF) controls and NEC rat pups were imaged at 2- and 4-days old. Intestinal tissue oxygen saturation was measured with PAI imaging for oxy- and deoxyhemoglobin levels. To measure intestinal motility, ultrasound and co-registered PAI cine recordings were used to capture intestinal peristalsis motion and contrast agent (indocyanine green) transit within the intestinal lumen. Additionally, both midplane two-dimensional and volumetric three-dimensional imaging acquisitions were assessed for oxygenation and motility. Results: NEC pups showed a significant decrease of intestinal tissue oxygenation as compared to healthy BF controls at both ages (2-days old: 55.90% +/- 3.77% vs 44.12% +/- 7.18%; 4-days old: 56.13% +/- 3.52% vs 38.86% +/- 8.33%). Intestinal motility, assessed using a computational intestinal deformation analysis, demonstrated a significant reduction in the intestinal motility index in both early (2-day) and established (4-day) NEC. Extensive NEC damage was confirmed with histology and dysmotility was confirmed by small intestinal transit assay. Conclusions: This study presents PAI as a successful emerging diagnostic imaging modality for both intestinal tissue oxygenation and intestinal motility disease hallmarks in a rat NEC model. PAI presents enormous significance and potential for fundamentally changing current clinical paradigms for detecting and monitoring intestinal pathologies in the premature infant.
Language	English
Publishing date	2023-10-23
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.10.20.563296
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Article ; Online: Clinical Correlates of Cholestasis in Preterm Infants with Surgical Necrotizing Enterocolitis.

Garg, Parvesh Mohan / Pittman, Isabella / Yi, Joe / Weis, Victoria G / Rodriguez, Ricardo Jorge / Ladd, Mitchell R / Rauh, Jessica L / McDonald, Anna Greene / Welch, Cherrie / Premkumar, Muralidhar Hebbur / Garg, Padma P / Maheshwari, Akhil

Newborn (Clarksville, Md.)

2023 Volume 2, Issue 3, Page(s) 191–197

Abstract: Background: We sought to investigate the clinical determinants and outcomes of cholestasis in preterm infants with surgical necrotizing enterocolitis (sNEC).: Methods: Retrospective comparison of clinical information in preterm infants who developed ... ...

Abstract	Background: We sought to investigate the clinical determinants and outcomes of cholestasis in preterm infants with surgical necrotizing enterocolitis (sNEC). Methods: Retrospective comparison of clinical information in preterm infants who developed cholestasis vs those who did not. Results: Sixty-two (62/91, 68.1%) infants with NEC developed cholestasis at any time following the onset of illness. Cholestasis was seen more frequently in those who had received ionotropic support at 24 hours following sNEC diagnosis (87.1% vs 58.6%; Conclusion: Cholestasis was seen in 68% of infants following surgical NEC. The most likely contributive factors are intestinal failure and subsequent PN dependence for longer periods. Our data suggest that identification and prevention of risk factors such as sepsis and surgical complications and early feeds following NEC surgery may improve outcomes.
Language	English
Publishing date	2023-09-26
Publishing country	United States
Document type	Journal Article
ISSN	2769-514X
ISSN (online)	2769-514X
DOI	10.5005/jp-journals-11002-0069
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Article ; Online: Human placental-derived stem cell therapy ameliorates experimental necrotizing enterocolitis.

Weis, Victoria G / Deal, Anna C / Mekkey, Gehad / Clouse, Cara / Gaffley, Michaela / Whitaker, Emily / Peeler, Cole B / Weis, Jared A / Schwartz, Marshall Z / Atala, Anthony

American journal of physiology. Gastrointestinal and liver physiology

2021 Volume 320, Issue 4, Page(s) G658–G674

Abstract: Necrotizing enterocolitis (NEC), a life-threatening intestinal disease, is becoming a larger proportionate cause of morbidity and mortality in premature infants. To date, therapeutic options remain elusive. Based on recent cell therapy studies, we ... ...

Abstract	Necrotizing enterocolitis (NEC), a life-threatening intestinal disease, is becoming a larger proportionate cause of morbidity and mortality in premature infants. To date, therapeutic options remain elusive. Based on recent cell therapy studies, we investigated the effect of a human placental-derived stem cell (hPSC) therapy on intestinal damage in an experimental NEC rat pup model. NEC was induced in newborn Sprague-Dawley rat pups for 4 days via formula feeding, hypoxia, and LPS. NEC pups received intraperitoneal (ip) injections of either saline or hPSC (NEC-hPSC) at 32 and 56 h into NEC induction. At 4 days, intestinal macroscopic and histological damage, epithelial cell composition, and inflammatory marker expression of the ileum were assessed. Breastfed (BF) littermates were used as controls. NEC pups developed significant bowel dilation and fragility in the ileum. Further, NEC induced loss of normal villi-crypt morphology, disruption of epithelial proliferation and apoptosis, and loss of critical progenitor/stem cell and Paneth cell populations in the crypt. hPSC treatment improved macroscopic intestinal health with reduced ileal dilation and fragility. Histologically, hPSC administration had a significant reparative effect on the villi-crypt morphology and epithelium. In addition to a trend of decreased inflammatory marker expression, hPSC-NEC pups had increased epithelial proliferation and decreased apoptosis when compared with NEC littermates. Further, the intestinal stem cell and crypt niche that include Paneth cells, SOX9
MeSH term(s)	Animals ; Animals, Newborn ; Apoptosis ; Cell Proliferation ; Cells, Cultured ; Cytokines/genetics ; Cytokines/metabolism ; Disease Models, Animal ; Enterocolitis, Necrotizing/genetics ; Enterocolitis, Necrotizing/metabolism ; Enterocolitis, Necrotizing/pathology ; Enterocolitis, Necrotizing/surgery ; Female ; Humans ; Ileum/metabolism ; Ileum/pathology ; Inflammation Mediators/metabolism ; Intestinal Mucosa/metabolism ; Intestinal Mucosa/pathology ; Paneth Cells/metabolism ; Paneth Cells/pathology ; Placenta/cytology ; Placenta/transplantation ; Pregnancy ; Rats, Sprague-Dawley ; Receptors, G-Protein-Coupled/metabolism ; SOX9 Transcription Factor ; Stem Cell Niche ; Stem Cell Transplantation ; Wound Healing ; Rats
Chemical Substances	Cytokines ; Inflammation Mediators ; Lgr5 protein, rat ; Receptors, G-Protein-Coupled ; SOX9 Transcription Factor ; Sox9 protein, rat
Language	English
Publishing date	2021-02-10
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	603840-2
ISSN	1522-1547 ; 0193-1857
ISSN (online)	1522-1547
ISSN	0193-1857
DOI	10.1152/ajpgi.00369.2020
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Article ; Online: Recruitment of Polarity Complexes and Tight Junction Proteins to the Site of Apical Bulk Endocytosis.

Engevik, Amy C / Krystofiak, Evan S / Kaji, Izumi / Meyer, Anne R / Weis, Victoria G / Goldstein, Anna / Coutts, Alexander W / Melkamu, Tamene / Saqui-Salces, Milena / Goldenring, James R

Cellular and molecular gastroenterology and hepatology

2021 Volume 12, Issue 1, Page(s) 59–80

Abstract: Background & aims: The molecular motor, Myosin Vb (MYO5B), is well documented for its role in trafficking cargo to the apical membrane of epithelial cells. Despite its involvement in regulating apical proteins, the role of MYO5B in cell polarity is less ...

Abstract	Background & aims: The molecular motor, Myosin Vb (MYO5B), is well documented for its role in trafficking cargo to the apical membrane of epithelial cells. Despite its involvement in regulating apical proteins, the role of MYO5B in cell polarity is less clear. Inactivating mutations in MYO5B result in microvillus inclusion disease (MVID), a disorder characterized by loss of key apical transporters and the presence of intracellular inclusions in enterocytes. We previously identified that inclusions in Myo5b knockout (KO) mice form from invagination of the apical brush border via apical bulk endocytosis. Herein, we sought to elucidate the role of polarity complexes and tight junction proteins during the formation of inclusions. Methods: Intestinal tissue from neonatal control and Myo5b KO littermates was analyzed by immunofluorescence to determine the localization of polarity complexes and tight junction proteins. Results: Proteins that make up the apical polarity complexes-Crumbs3 and Pars complexes-were associated with inclusions in Myo5b KO mice. In addition, tight junction proteins were observed to be concentrated over inclusions that were present at the apical membrane of Myo5b-deficient enterocytes in vivo and in vitro. Our mouse findings are complemented by immunostaining in a large animal swine model of MVID genetically engineered to express a human MVID-associated mutation that shows an accumulation of Claudin-2 over forming inclusions. The findings from our swine model of MVID suggest that a similar mechanism of tight junction accumulation occurs in patients with MVID. Conclusions: These data show that apical bulk endocytosis involves the altered localization of apical polarity proteins and tight junction proteins after loss of Myo5b.
MeSH term(s)	Animals ; Endocytosis ; Enterocytes/metabolism ; Intestinal Absorption ; Mice ; Mice, Knockout ; Myosin Type V/deficiency ; Myosin Type V/metabolism ; Tight Junction Proteins/genetics ; Tight Junction Proteins/metabolism
Chemical Substances	Myo5B protein, mouse ; Tight Junction Proteins ; Myosin Type V (EC 3.6.1.-)
Language	English
Publishing date	2021-02-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2819778-1
ISSN	2352-345X ; 2352-345X
ISSN (online)	2352-345X
ISSN	2352-345X
DOI	10.1016/j.jcmgh.2021.01.022
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Article ; Online: Current understanding of SPEM and its standing in the preneoplastic process.

Weis, Victoria G / Goldenring, James R

Gastric cancer : official journal of the International Gastric Cancer Association and the Japanese Gastric Cancer Association

2010 Volume 12, Issue 4, Page(s) 189–197

Abstract: Gastric cancer is the second leading cause of cancer-related death worldwide, but the details of gastric carcinogenesis remain unclear. In humans, two preneoplastic metaplasias are associated with the precancerous stomach: intestinal metaplasia and ... ...

Abstract	Gastric cancer is the second leading cause of cancer-related death worldwide, but the details of gastric carcinogenesis remain unclear. In humans, two preneoplastic metaplasias are associated with the precancerous stomach: intestinal metaplasia and spasmolytic polypeptide-expressing metaplasia (SPEM). While mouse models of Helicobacter sp. infection have not shown intestinal metaplasia, a number of mouse models lead to the evolution of SPEM. In this review, we summarize increasing data that indicates that SPEM arises in the setting of parietal cell loss, either following acute druginduced oxyntic atrophy or in chronic oxyntic atrophy associated with H. felis infection. Importantly, recent investigations support the origin of SPEM through transdifferentiation from mature chief cells following parietal cell loss. Novel biomarkers of SPEM, such as HE4, hold promise as specific markers of the metaplastic process distinct from normal gastric lineages. Staining with HE4 in humans and other studies in gerbils suggest that SPEM arises initially in the human stomach following parietal cell loss and then further evolves into intestinal metaplasia, likely in association with chronic inflammation. Further studies are needed to broaden our knowledge of metaplasia and early cancer-specific biomarkers that could give insights into both lineage derivation and preneoplasia detection.
MeSH term(s)	Animals ; Cell Transformation, Neoplastic ; Disease Models, Animal ; Gastric Mucosa/metabolism ; Gastric Mucosa/pathology ; Gerbillinae ; Humans ; Intercellular Signaling Peptides and Proteins ; Metaplasia/metabolism ; Metaplasia/pathology ; Mice ; Parietal Cells, Gastric/metabolism ; Peptides/metabolism ; Precancerous Conditions ; Stomach Neoplasms/etiology ; Stomach Neoplasms/pathology
Chemical Substances	Intercellular Signaling Peptides and Proteins ; Peptides ; spasmolytic polypeptide
Language	English
Publishing date	2010-01-05
Publishing country	Japan
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1463526-4
ISSN	1436-3305 ; 1436-3291
ISSN (online)	1436-3305
ISSN	1436-3291
DOI	10.1007/s10120-009-0527-6
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Article ; Online: Maturity and age influence chief cell ability to transdifferentiate into metaplasia.

Weis, Victoria G / Petersen, Christine P / Weis, Jared A / Meyer, Anne R / Choi, Eunyoung / Mills, Jason C / Goldenring, James R

American journal of physiology. Gastrointestinal and liver physiology

2016 Volume 312, Issue 1, Page(s) G67–G76

Abstract: The plasticity of gastric chief cells is exemplified by their ability to transdifferentiate into spasmolytic polypeptide-expressing metaplasia (SPEM) after parietal cell loss. We sought to determine if chief cell maturity is a limiting factor in the ... ...

Abstract	The plasticity of gastric chief cells is exemplified by their ability to transdifferentiate into spasmolytic polypeptide-expressing metaplasia (SPEM) after parietal cell loss. We sought to determine if chief cell maturity is a limiting factor in the capacity to transdifferentiate. Mist1 New & noteworthy: Previous investigations have indicated that spasmolytic polypeptide-expressing metaplasia (SPEM) in the stomach arises from transdifferentiation of chief cells. Nevertheless, the intrinsic properties of chief cells that influence transdifferentiation have been largely unknown. We now report that the ability to transdifferentiate into SPEM is impaired in chief cells that lack full functional maturation, and as chief cells age, they lose their ability to transdifferentiate. Thus chief cell plasticity is dependent on both cell age and maturation.
MeSH term(s)	Age Factors ; Animals ; Basic Helix-Loop-Helix Transcription Factors/genetics ; Basic Helix-Loop-Helix Transcription Factors/metabolism ; Cell Lineage/physiology ; Cell Proliferation/physiology ; Cell Transdifferentiation/physiology ; Chief Cells, Gastric/metabolism ; Chief Cells, Gastric/pathology ; Gastric Mucosa/metabolism ; Metaplasia/metabolism ; Metaplasia/pathology ; Mice ; Mice, Knockout ; Parietal Cells, Gastric/metabolism ; Parietal Cells, Gastric/pathology ; Peptides/metabolism ; Stomach/pathology
Chemical Substances	Basic Helix-Loop-Helix Transcription Factors ; Bhlha15 protein, mouse ; Peptides ; spasmolytic polypeptide
Language	English
Publishing date	2016-11-23
Publishing country	United States
Document type	Journal Article
ZDB-ID	603840-2
ISSN	1522-1547 ; 0193-1857
ISSN (online)	1522-1547
ISSN	0193-1857
DOI	10.1152/ajpgi.00326.2016
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Article ; Online: Apical Membrane Alterations in Non-intestinal Organs in Microvillus Inclusion Disease.

Schlegel, Cameron / Weis, Victoria G / Knowles, Byron C / Lapierre, Lynne A / Martin, Martin G / Dickman, Paul / Goldenring, James R / Shub, Mitchell D

Digestive diseases and sciences

2017 Volume 63, Issue 2, Page(s) 356–365

Abstract: Objectives: Microvillus inclusion disease (MVID) is a severe form of neonatal diarrhea, caused mainly by mutations in MYO5B. Inactivating mutations in MYO5B causes depolarization of enterocytes in the small intestine, which gives rise to chronic, ... ...

Abstract	Objectives: Microvillus inclusion disease (MVID) is a severe form of neonatal diarrhea, caused mainly by mutations in MYO5B. Inactivating mutations in MYO5B causes depolarization of enterocytes in the small intestine, which gives rise to chronic, unremitting secretory diarrhea. While the pathology of the small intestine in MVID patients is well described, little is known about extraintestinal effects of MYO5B mutation. Methods: We examined stomach, liver, pancreas, colon, and kidney in Navajo MVID patients, who share a single homozygous MYO5B-P660L (1979C>T p.Pro660Leu, exon 16). Sections were stained for markers of the apical membrane to assess polarized trafficking. Results: Navajo MVID patients showed notable changes in H/K-ATPase-containing tubulovesicle structure in the stomach parietal cells. Colonic mucosa was morphologically normal, but did show losses in apical ezrin and Syntaxin 3. Hepatocytes in the MVID patients displayed aberrant canalicular expression of the essential transporters MRP2 and BSEP. The pancreas showed small fragmented islets and a decrease in apical ezrin in pancreatic ducts. Kidney showed normal primary cilia. Conclusions: These findings indicate that the effects of the P660L mutation in MYO5B in Navajo MVID patients are not limited to the small intestine, but that certain tissues may be able to compensate functionally for alterations in apical trafficking.
MeSH term(s)	Cell Membrane/physiology ; Child ; Female ; Genetic Predisposition to Disease ; Humans ; Indians, North American ; Infant ; Infant, Newborn ; Kidney ; Malabsorption Syndromes/genetics ; Malabsorption Syndromes/metabolism ; Male ; Microvilli/genetics ; Microvilli/metabolism ; Microvilli/pathology ; Mucolipidoses/genetics ; Mucolipidoses/metabolism ; Mutation ; Myosin Heavy Chains/genetics ; Myosin Heavy Chains/metabolism ; Myosin Type V/genetics ; Myosin Type V/metabolism ; Pancreas ; Stomach
Chemical Substances	MYO5B protein, human ; Myosin Type V (EC 3.6.1.-) ; Myosin Heavy Chains (EC 3.6.4.1)
Language	English
Publishing date	2017-12-07
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	304250-9
ISSN	1573-2568 ; 0163-2116
ISSN (online)	1573-2568
ISSN	0163-2116
DOI	10.1007/s10620-017-4867-5
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Article: Current understanding of SPEM and its standing in the preneoplastic process

Weis, Victoria G / Goldenring, James R

Gastric cancer. 2009 Dec., v. 12, no. 4

2009

Abstract	Gastric cancer is the second leading cause of cancer-related death worldwide, but the details of gastric carcinogenesis remain unclear. In humans, two preneoplastic metaplasias are associated with the precancerous stomach: intestinal metaplasia and spasmolytic polypeptide-expressing metaplasia (SPEM). While mouse models of Helicobacter sp. infection have not shown intestinal metaplasia, a number of mouse models lead to the evolution of SPEM. In this review, we summarize increasing data that indicates that SPEM arises in the setting of parietal cell loss, either following acute druginduced oxyntic atrophy or in chronic oxyntic atrophy associated with H. felis infection. Importantly, recent investigations support the origin of SPEM through transdifferentiation from mature chief cells following parietal cell loss. Novel biomarkers of SPEM, such as HE4, hold promise as specific markers of the metaplastic process distinct from normal gastric lineages. Staining with HE4 in humans and other studies in gerbils suggest that SPEM arises initially in the human stomach following parietal cell loss and then further evolves into intestinal metaplasia, likely in association with chronic inflammation. Further studies are needed to broaden our knowledge of metaplasia and early cancer-specific biomarkers that could give insights into both lineage derivation and preneoplasia detection.
Keywords	metaplasia
Language	English
Dates of publication	2009-12
Size	p. 189-197.
Publisher	Springer Japan
Publishing place	Japan
Document type	Article
ZDB-ID	1463526-4
ISSN	1436-3291
ISSN	1436-3291
DOI	10.1007/s10120-009-0527-6
Database	NAL-Catalogue (AGRICOLA)

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