A quantitative analysis of the sensory and sympathetic innervation of the mouse pancreas

Lindsay, Theodore H.; Halvorson, Kyle G.; Peters, Christopher M.; Ghilardi, Joseph R.; Kuskowski, Michael A.; Wong, Gilbert Y.; Mantyh, P.W.

doi:10.1016/j.neuroscience.2005.10.055

Cited by 70 publications

(48 citation statements)

References 44 publications

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“…Parasympathetic nerves, for instance, stimulate insulin secretion, whereas activation of sympathetic nerves inhibits insulin and stimulates glucagon secretion to elevate glucose levels in the circulation [2][3][4]. Histological studies reveal that islets are richly innervated by autonomic nerves, which enter the islets with the vasculature [5][6][7][8]. Despite these observations, to date, investigators still lack a detailed neurovascular anatomy of islets to understand the control mechanism, even in animals [9,10].…”

Section: Introductionmentioning

confidence: 99%

“…use of the immersion solution to reduce scattering as light travels in the specimen [18][19][20]) to allow for deeptissue microscopy. Here, in islet imaging, we employed the same penetrative 3-D microscopy with vessel painting (perfusion of blood vessels with fluorescent probes) [13,21] and islet histology [7,8,22,23] to provide a global and integral view of the islet sympathetic neurovascular complex.…”

Section: Introductionmentioning

confidence: 99%

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3-D imaging and illustration of the perfusive mouse islet sympathetic innervation and its remodelling in injury

Chiu

Hua

et al. 2012

Diabetologia

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Aims/hypothesis Sympathetic nerves influence islet hormone levels in the circulation. Insights into islet sympathetic innervation and its remodelling in diabetes may impact future therapeutics. However, standard immunohistochemistry and microtome-based microscopy cannot provide an integral view of the islet neurovascular complex. We prepared transparent islet specimens to investigate the spatial relationship between sympathetic nerves, blood vessels and islet cells in normal, streptozotocin-injected and non-obese diabetic mouse models. Methods Cardiac perfusion of fluorescent lectin was used to label pancreatic blood vessels. Tyrosine hydroxylase and nuclear staining were used to reveal islet sympathetic innervation and microstructure. Optical clearing (i.e. use of immersion solution to reduce scattering) was applied to enable 3-dimensional confocal microscopy of islets to visualise the sympathetic neurovascular complex in space. Results Unlike previously reported morphology, we observed perfusive intra-islet, perivascular sympathetic innervation, in addition to peri-islet contacts of sympathetic nerves with alpha cells and sympathetic fibres encircling the adjacent arterioles. The intra-islet axons became markedly prominent in streptozotocin-injected mice (2 weeks after injection). In non-obese diabetic mice, lymphocytic infiltration remodelled the peri-islet sympathetic axons in early insulitis. Conclusions/interpretation We have established an imaging approach to reveal the spatial features of mouse islet sympathetic innervation. The neurovascular complex and sympathetic nerve-alpha cell contact suggest that sympathetic nerves modulate islet hormone secretion through blood vessels, in addition to acting directly on alpha cells. In islet injuries, sympathetic nerves undergo different remodelling in response to different pathophysiological cues.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

3-D imaging and illustration of the perfusive mouse islet sympathetic innervation and its remodelling in injury

Chiu

Hua

et al. 2012

Diabetologia

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“…Moreover, in the Egyptian spiny mouse the numerous AChE-positive fibres and ganglia were found at the surface of the gland. In contrast, in laboratory mice the agglomerations of nerve cells were situated additionally in the vicinity of the bile duct (Gienc et al 1993;Lindsay et al 2006). Cholinergic fibres were observed in the interlobular connective tissue where they accompanied mostly blood vessels and the secretory ducts of the exocrine part of pancreas.…”

Section: Discussionmentioning

confidence: 99%

“…On the other hand, parasympathetic fibres are the branches of the vagus nerve. Autonomic fibres reach blood vessels, secretory ducts and pancreatic islets (Buijs et al 2001;Lindsay et. al.…”

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confidence: 99%

Autonomic Innervation of Pancreas in Egyptian Spiny Mouse (Acomys cahirinus, Desmarest)

et al. 2009

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The aim of the study was to obtain details of the morphology of the autonomic innervation of pancreas. Six adult Egyptian spiny mice (Acomys cahirinus, Desmarest) were studied for the presence and location of autonomic fibres and cells in the pancreas. The macromorphological investigations were performed using the thiocholine method adapted for this type of specimens. For processing tissues two histochemical techniques were used: thiocholine method on activity of AChE and the glyoxylic acid method for adrenergic structures.Cholinergic fibres and small autonomic ganglia were found among the secretory sections and along the pancreatic duct and both pancreaticoduodenal arteries, and its branches, reaching the Langerhans islets and forming around them a kind of net. From 24 to 40 AChE-positive ganglions in the whole exocrine part were observed. The highest density of cholinergic fibres was observed in the head of pancreas. Numerous adrenergic fibres that accompanied blood vessels as well as interlobular and intralobular ducts were found inside the exocrine parts of the pancreas. Neither adrenergic cells or adrenergic fibres were observed inside the pancreatic islets. Our results can be used in comparative anatomy studies of pancreas in mammals.

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“…Pancreatic innervation is being viewed with increasing interest with respect to pancreatic diseases, yet relatively little is known about pancreatic innervation during development and disease (Saravia and HomoDelarche 2003;Konturek et al 2003;Yi et al 2003;Rossi et al 2005;Lindsay et al 2006). Nonetheless, pancreatic nerves have recently been identified as a possible early target population in autoimmune diabetes, and there is increasing evidence that neuroendocrine remodeling does take place in the pancreatic islets of diabetic disease models (Persson-Sjogren et al 2005;Saravia and Homo-Delarche 2003;Winer et al 2003;Mei et al 2002).…”

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confidence: 99%

Pancreatic innervation in mouse development and β-cell regeneration

Burris

Hebrok

2007

Neuroscience

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Pancreatic innervation is being viewed with increasing interest with respect to pancreatic disease. At the same time, relatively little is currently known about innervation dynamics during development and disease. The present study employs confocal microscopy to analyze the growth and development of sympathetic and sensory neurons and astroglia during pancreatic organogenesis and maturation. Our research reveals that islet innervation is closely linked to the process of islet maturation-neural cell bodies undergo intrapancreatic migration/shuffling in tandem with endocrine cells, and close neuro-endocrine contacts are established quite early in pancreatic development. In addition, we have assayed the effects of large-scale β-cell loss and repopulation on the maintenance of islet innervation with respect to particular neuron types. We demonstrate that depletion of the β-cell population in the RIP-cmyc ER mouse line has cell-type-specific effects on postganglionic sympathetic neurons and pancreatic astroglia. This study contributes to a greater understanding of how cooperating physiological systems develop together and coordinate their functions, and also helps to elucidate how permutation of one organ system through stress or disease can specifically affect parallel systems in an organism.There are three neuron types-sympathetic, parasympathetic, and sensory-that innervate the pancreas, in addition to an astroglial population. The sympathetic and parasympathetic branches of the autonomic nervous system are involved in maintenance of blood glucose homeostasis in response to changing energy demands. Sympathetic neurons mediate the socalled "fight or flight" response through stress-induced neural activity. They inhibit insulin secretion and up-regulate glucagon release by respective β-and α-cell populations in the pancreatic islets of Langerhans, the net physiological result of which is to convert glycogen stores to blood glucose to meet immediate energy demands (Mundinger et al.2003). Through feeding-induced neural activity, parasympathetic neurons stimulate insulin secretion from insulin-producing β-cells to promote the removal of glucose from the blood into the liver for storage as glycogen, while repressing glucagon release (Benthem et al. 2001;Adeghate et al. 2000;Ahren 2000). Sensory neurons are involved in pain sensation; indeed, extreme pain is a well-documented concern in pancreatitis and pancreatic cancer patients (Wick et al. 2006a(Wick et al. , 2006b). The function of pancreatic astroglia, which encapsulate the islets of Langerhans, is not definitively known, although there is increasing evidence that astroglia are involved in synaptic transmission in the brain, and thus may be more involved in neuronal signaling than previously speculated (Halassa et al. 2007).*Correspondence to: Matthias Hebrok, UCSF Diabetes Center, 513 Parnassus Avenue, San Francisco, CA 94143 Email: mhebrok@diabetes.ucsf.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for pu...

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A quantitative analysis of the sensory and sympathetic innervation of the mouse pancreas

Cited by 70 publications

References 44 publications

3-D imaging and illustration of the perfusive mouse islet sympathetic innervation and its remodelling in injury

3-D imaging and illustration of the perfusive mouse islet sympathetic innervation and its remodelling in injury

Autonomic Innervation of Pancreas in Egyptian Spiny Mouse (Acomys cahirinus, Desmarest)

Pancreatic innervation in mouse development and β-cell regeneration

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