Immunohistochemical expression and neurochemical phenotypes of huntingtin-associated protein 1 in the myenteric plexus of mouse gastrointestinal tract

Tarif, Abu Md Mamun; Islam, Nabiul; Jahan, Mir Rubayet; Yanai, Akie; Nozaki, Kanako; Masumoto, Kouji; Shinoda, Koh

doi:10.1007/s00441-021-03542-4

Cited by 11 publications

(9 citation statements)

References 92 publications

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“…Moreover, confocal immunofluorescent analysis of TT and HeLa cells confirms that CGRP were in TT cells but not in HeLa cells. The specificity of both CGRP‐antibodies used in this study was additionally confirmed by virtually identical staining patterns in the GI tract (more specifically in the stomach) of previous reports using other antibodies ( Peninsula Laboratories : Hibberd et al., 2022; Smolilo et al., 2020; Spencer et al., 2016, Sigma‐Aldrich : Tarif et al., 2021). The staining was shown to be reduced or completely abolished by preadsorption with CGRP from Peninsula (Domeneghini et al., 2004).…”

Section: Methodssupporting

confidence: 83%

“…Mouse +/− + /− + /− (+/+ Tarif) +/− (+/+ Tarif) (Furness et al, 2004;Matsumoto et al, 2014;Mongardi Fantaguzzi et al, 2009;Qu et al, 2008;Spencer et al, 2018Spencer et al, , 2016Spencer et al, , 2014Spencer et al, 2020;Tan et al, 2008;Tarif et al, 2021) Rat +/− +/− +/+ (Furness et al, 2001;Hayakawa et al, 2009;Ladic & Buchan, 1998;Mitsui, 2009;Mózsik et al, 2005;Rosenfeld et al, 1983;Su et al, 1987) Hamster +/− + /+ + /+ + /+ (Shochina et al, 1997;Toole et al, 1999 (Furness et al, 1991;Serzysko et al, 2021;Sternini et al, 1992) Lamb +/+ (Chiocchetti et al, 2006;Mazzoni et al, 2010) Pig +/+ +/+ +/+ (Makowska & Gonkowski, 2019;Palus et al, 2018;Poonyachoti et al, 2002) Human +/− + /− (+/+ Timmermans)…”

Section: Stomach Small Intestine Large Intestine Referencesmentioning

confidence: 99%

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Organization and morphology of calcitonin gene‐related peptide‐immunoreactive axons in the whole mouse stomach

Ma,

Nguyen,

Madas

et al. 2023

J of Comparative Neurology

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Nociceptive afferent axons innervate the stomach and send signals to the brain and spinal cord. Peripheral nociceptive afferents can be detected with a variety of markers (e.g., substance P [SP] and calcitonin gene‐related peptide [CGRP]). We recently examined the topographical organization and morphology of SP‐immunoreactive (SP‐IR) axons in the whole mouse stomach muscular layer. However, the distribution and morphological structure of CGRP‐IR axons remain unclear. We used immunohistochemistry labeling and applied a combination of imaging techniques, including confocal and Zeiss Imager M2 microscopy, Neurolucida 360 tracing, and integration of axon tracing data into a 3D stomach scaffold to characterize CGRP‐IR axons and terminals in the whole mouse stomach muscular layers. We found that: (1) CGRP‐IR axons formed extensive terminal networks in both ventral and dorsal stomachs. (2) CGRP‐IR axons densely innervated the blood vessels. (3) CGRP‐IR axons ran in parallel with the longitudinal and circular muscles. Some axons ran at angles through the muscular layers. (4) They also formed varicose terminal contacts with individual myenteric ganglion neurons. (5) CGRP‐IR occurred in DiI‐labeled gastric‐projecting neurons in the dorsal root and vagal nodose ganglia, indicating CGRP‐IR axons were visceral afferent axons. (6) CGRP‐IR axons did not colocalize with tyrosine hydroxylase or vesicular acetylcholine transporter axons in the stomach, indicating CGRP‐IR axons were not visceral efferent axons. (7) CGRP‐IR axons were traced and integrated into a 3D stomach scaffold. For the first time, we provided a topographical distribution map of CGRP‐IR axon innervation of the whole stomach muscular layers at the cellular/axonal/varicosity scale.

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Section: Methodssupporting

confidence: 83%

Section: Stomach Small Intestine Large Intestine Referencesmentioning

confidence: 99%

Organization and morphology of calcitonin gene‐related peptide‐immunoreactive axons in the whole mouse stomach

Ma,

Nguyen,

Madas

et al. 2023

J of Comparative Neurology

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“…An additional smaller population of vagal afferents also contribute some CGRP nerve fibers to the upper gastrointestinal tract (Zhong et al., 2008). The CGRP‐expressing nerve fibers in mouse stomach and esophagus may be exclusively extrinsic (Sharrad et al., 2015; Tarif et al., 2021).…”

Section: Introductionmentioning

confidence: 99%

Quantification of CGRP‐immunoreactive myenteric neurons in mouse colon

Hibberd

Yew

Dodds

et al. 2022

J of Comparative Neurology

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Quantitative data of biological systems provide valuable baseline information for understanding pathology, experimental perturbations, and computational modeling. In mouse colon, calcitonin gene‐related peptide (CGRP) is expressed by myenteric neurons with multiaxonal (Dogiel type II) morphology, characteristic of intrinsic primary afferent neurons (IPANs). Analogous neurons in other species and gut regions represent 5–35% of myenteric neurons. We aimed to quantify proportions of CGRP‐immunopositive (CGRP+) myenteric neurons. Colchicine‐treated wholemount preparations of proximal, mid, and distal colon were labeled for HuC/D, CGRP, nitric oxide synthase (NOS), and peripherin (Per). The pan‐neuronal markers (Hu+/Per+) co‐labeled 94% of neurons. Hu+/Per– neurons comprised ∼6%, but Hu‐/Per+ cells were rare. Thus, quantification was based on Hu+ myenteric neurons (8576 total; 1225 ± 239 per animal, n = 7). CGRP+ cell bodies were significantly larger than the average of all Hu+ neurons (329 ± 13 vs. 261 ± 12 μm2, p < .0001). CGRP+ neurons comprised 19% ± 3% of myenteric neurons without significant regional variation. NOS+ neurons comprised 42% ± 2% of myenteric neurons overall, representing a lower proportion in proximal colon, compared to mid and distal colon (38% ± 2%, 44% ± 2%, and 44% ± 3%, respectively). Peripherin immunolabeling revealed cell body and axonal morphology in some myenteric neurons. Whether all CGRP+ neurons were multiaxonal could not be addressed using peripherin immunolabeling. However, of 118 putatively multiaxonal neurons first identified based on peripherin immunoreactivity, all were CGRP+ (n = 4). In conclusion, CGRP+ myenteric neurons in mouse colon were comprehensively quantified, occurring within a range expected of a putative IPAN marker. All Per+ multiaxonal neurons, characteristic of Dogiel type II/IPAN morphology, were CGRP+.

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“…In addition to central nervous system (CNS), HAP1 is also present in the enteric nervous system (ENS) ( Tarif and Islam, 2021 ; Tarif et al, 2022 ) that is embedded in the wall of the gastrointestinal tract and contains polarized neural circuits responsible for controlling a wide variety of gastrointestinal functions ( Furness et al, 2014 ). The ENS, sharing many features with the brain, can act as a potential portal for pathogenesis of NDs and is also a neurodegenerative target ( Chalazonitis and Rao, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

“…The ENS, sharing many features with the brain, can act as a potential portal for pathogenesis of NDs and is also a neurodegenerative target ( Chalazonitis and Rao, 2018 ). HAP1 is abundantly expressed in excitatory and inhibitory motor neurons of myenteric plexuses, and secretomotor and vasodilator neurons of submucosal plexuses ( Tarif and Islam, 2021 ; Tarif et al, 2022 ). The fact suggests that HAP1-associated intracellular trafficking plays an important role in these neurons of ENS.…”

Section: Introductionmentioning

confidence: 99%

Huntingtin-associated protein 1-associated intracellular trafficking in neurodegenerative diseases

Chen

et al. 2023

Front. Aging Neurosci.

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Huntingtin-associated protein 1 (HAP1), the first identified HTT-binding partner, is highly expressed in the central nervous system, and has been found to associated with neurological diseases. Mounting evidence suggests that HAP1 functions as a component of cargo-motor molecules to bind various proteins and participates in intracellular trafficking. It is known that the failure of intracellular transport is a key contributor to the progression of neurodegenerative disorders (NDs) including Alzheimer’s disease (AD), Huntington’s disease (HD), Parkinson’s disease (PD), amyotrophic lateral sclerosis (ALS), spinal and bulbar muscular atrophy (SBMA) and spinocerebellar ataxia (SCA). The link between HAP1 and various NDs is supported by growing evidence. This review aims to provide a comprehensive overview of the intracellular trafficking function of HAP1 and its involvement in NDs.

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Immunohistochemical expression and neurochemical phenotypes of huntingtin-associated protein 1 in the myenteric plexus of mouse gastrointestinal tract

Cited by 11 publications

References 92 publications

Organization and morphology of calcitonin gene‐related peptide‐immunoreactive axons in the whole mouse stomach

Organization and morphology of calcitonin gene‐related peptide‐immunoreactive axons in the whole mouse stomach

Quantification of CGRP‐immunoreactive myenteric neurons in mouse colon

Huntingtin-associated protein 1-associated intracellular trafficking in neurodegenerative diseases

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