Search by lot number. A bioluminescent method to kinetically monitor viability in cell culture up to 72 hours. Quantifies cell proliferation based on ATP detection. A homogeneous method optimized to assess viability in 3D cell culture. Measures changes in membrane integrity.
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Password has been used too recently. Confirm New Password Passwords don't match. And what is the nature of the chemical messages neurons send and receive once the synaptic connections are made? This article will describe some major characteristics and effects of a protein called the nerve-growth factor NGF , which has made it possible to induce and analyze under highly favorable conditions some crucial steps in the differentiation of neurons, such as the growth and maturation of axons and the synthesis and release of neurotransmitters: the bearers of the chemical messages.
The discovery of NGF has also promoted an intensive search for other specific growth factors, leading to the isolation and characterization of a number of proteins with the ability to enhance the growth of different cell lines. The peripheral nervous system of vertebrate animals includes three kinds of nerve cells: sensory neurons, which transmit impulses from sensory receptor structures to the brain; motor neurons, which innervate the striated, or skeletal, muscles, and autonomic neurons, which regulate the functional activity of the circulatory system, the organs, the glands and the smooth muscles such as those of the intestine.
Autonomic neurons are of two kinds: sympathetic and parasympathetic. The sensory neurons and some of the sympathetic neurons are situated in chains of ganglia flanking the length of the spinal cord. Because these neurons are uniquely accessible to experimental manipulation much of the research on the development of the nervous system at the cellular level has focused on how the nerve fibers projecting from the sensory and sympathetic ganglia make connections with their corresponding target organs.
In the first half of this century the new science of experimental embryology seemed to offer the best way to study the intimate bond that interlocks the growth of the peripheral neurons and their target organs.
Ross G. Harrison of Yale University challenged the nervous system of the larva of amphibians to solve problems it would ordinarily never confront, such as providing nerves for limbs and organs grafted from other species. He wanted to see how sensory and sympathetic ganglia, sending out their nerve fibers to these peripheral "fields of innervation," would adjust to the different dimensions and configurations of the foreign organs.
Harrison's results demonstrated that the developing amphibian nervous system is remarkably flexible in adapting to such novel situations, even to the point of accelerating the growth of nerve fibers in a host species to keep pace with the faster-growing limb of a smaller donor species.
He concluded that the embryonic nervous system is highly receptive to influences exerted by the peripheral field. Such influences are not species-specific, however, since they can be evoked by organs or rudimentary limbs that have been transplanted from one species to another. Viktor Hamburger of Washington University extended Harrison's work but chose to study the chick embryo because its nervous system, although more complex than that of an amphibian, lends itself better to experimental analysis: its nerve centers are more clearly delineated and their strong affinity for silver stain enables the experimenter to visually examine the nerve structures more easily.
Hamburger grafted limb buds onto chick embryos at very early stages of development and observed how the modified peripheral field was innervated by sensory and sympathetic fibers. Unfortunately the responses were often so complex that they defied interpretation,. In , in an effort to get more straightforward results, Elmer D. Bueker of Georgetown University modified Hamburger's experimental approach.
He had the ingenious idea of replacing one limb bud of a chick embryo with a fragment of a bird or mammalian tumor. The tumor cells were all undifferentiated and hence provided a homogeneous peripheral field, in contrast to the cells of the normal limb bud, which were destined to differentiate into many types of tissue. Bueker's experiment was therefore expected to reveal how a homogeneous but fast-growing peripheral field would be innervated. Of three different tumors implanted in the body wall of three-day-old chick embryos only one, a mouse tumor of connective-tissue cells called sarcoma , grew vigorously and was invaded by nerve fibers growing out from adjacent sensory ganglia.
In embryos sacrificed after five days the sensory ganglia innervating the tumor were 33 percent larger than those innervating the normal limb bud on the opposite side of the embryo. At first these findings seemed to suggest that the size of a sensory ganglion depends on the size and rate of growth of its field of innervation.
According to this hypothesis the rapidly growing tumor provided a more favorable peripheral field for the innervating sensory fibers than the slowly growing limb bud did. A reexamination of Bueker's findings by our group at Washington University revealed new aspects of the phenomenon that obliged us to revise his conclusions.
We found not only that the growth of the sensory ganglia innervating the sarcoma tumors increased but also that the sympathetic ganglia increased enormously in volume, becoming five to six times larger than they were in control animals.
This increase in size of the sympathetic ganglia was considerably greater than that exhibited by the sensory ganglia. Together with the sensory fibers the sympathetic fibers branched all over the peripheral field provided by the tumor but did not form any synapses with the tumor cells. In addition, and indicating an even more striking departure from normality, the viscera of the embryos with the transplanted tumors were flooded with excessive numbers of sympathetic fibers long before the embryos of the control animals were even sparsely innervated.
The sympathetic fibers forced their way into large and small veins, impeding and sometimes completely obstructing the flow of blood. These extraordinary effects suggested that the overgrowth of the sympathetic ganglia was more than simply a response to the rapidly growing peripheral field of innervation provided by the tumor, as Bueker had proposed. Rather it seemed the tumor was releasing some chemical factor that was in turn inducing the remarkable growth of the sympathetic ganglia and the exuberant branching of their nerve fibers.
This hypothesis was tested by transplanting sarcoma tumors into the respiratory membranes of the chick egg, which are permeated with blood vessels from the embryo. The tumor and the developing chick embryo therefore shared the same blood supply, although they were not in direct contact.
We found that when the tumor was transplanted into the respiratory membranes, it elicited the same growth-promoting effects on the sympathetic ganglia as it did when it was implanted in the embryo itself, providing convincing proof that the tumor was releasing a soluble factor that was carried in the bloodstream to the embryo.
The next challenge was to identify the postulated nerve-growth factor being released by the tumor. For this purpose we needed a system much less complex than the developing embryo.
Tissue culture which in the early s had yet to become the universal biological tool it is today seemed to offer a useful alternative. We reasoned that if sarcoma was releasing a chemical factor with the ability to enhance nerve growth, the same effect should appear when an isolated sympathetic ganglion was incubated with the tumor in laboratory glassware. Sensory and sympathetic ganglia were dissected out of eight-day-old chick embryos and cultured in a semisolid medium in proximity to fragments of mouse sarcoma tumors.
Within 10 hours of incubation the isolated ganglion gave rise to a dense halo of nerve fibers, radiating out from the ex-plant like rays from the sun. Control ganglia cultured for the same length of time in the absence of the sarcoma cells displayed only a sparse and irregular outgrowth of nerve fibers. The discovery that the tumor could exert its growth-enhancing effects on an isolated ganglion in tissue culture was the turning point of the investigation.
Whereas our earlier experiments in developing chick embryos had required weeks of painstaking work, we could now in a few hours screen a large number of tissues, organic fluids and chemicals to determine if they were sources of the growth-promoting activity. Furthermore, it now became possible to attempt to isolate the nerve-growth factor from our simplified tissue-culture system.
Stanley Cohen, a biochemist, agreed to join our group at Washington University to undertake the task of identifying the active agent. Neurol Res. Intensive Care Med. Date I, Ohmoto T: Neural transplantation and trophic factors in Parkinson's disease: special reference to chromaffin cell grafting, NGF support from pretransected peripheral nerve, and encapsulated dopamine-secreting cell grafting. J Neurol. First clinical trials.
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Correspondence to Luigi Manni. LA conceived, drafted and reviewed the manuscript. MLR drafted and reviewed the manuscript. PB drafted and reviewed the manuscript. LM conceived, drafted and reviewed the manuscript. All authors read and approved the final manuscript. Reprints and Permissions. Aloe, L.
Nerve growth factor: from the early discoveries to the potential clinical use. J Transl Med 10, Download citation.
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Among the more useful processing strategies to fabricate nanofibers, electrospinning is one of the best known methods Greiner and Wendorff, Nanofibrous electrospun scaffolds offer a promising alternative to autologous grafting in peripheral nerve injuries, and have been extensively studied for neural tissue repair and regeneration Ghane et al.
There are several reasons for the great interest in electrospun constructs in neural tissue engineering: ease of manufacture, production using a variety of natural and synthetic polymers, structural similarity with the extracellular matrix, and tunable morphology and mechanical properties.
Of their various advantages, the ease of nanofiber functionalization is perhaps the most relevant, since biomolecules and drugs can easily be incorporated into electrospun scaffolds by means of several methods, including physical adsorption, blend electrospinning, coaxial electrospinning, and covalent immobilization.
The nanometer scale of the fibers provides an extremely high surface-to-volume ratio, and contributes to improving biological functionality and biomolecule delivery Ji et al. To tackle the problems related to the possible destabilization and denaturation of biomolecules such as growth factors when exposed to organic solvents in a traditional electrospinning process, variations in the technique, such as coaxial or emulsion electrospinning, have been employed to preserve the bioactivity of the incorporated biomolecules, thus enhancing the efficiency of incorporation, while controlling the release kinetics of the biomolecules at the same time.
A variety of natural and synthetic materials have been used to manufacture aligned structures for nerve regeneration, however only a few studies report significant results on the biomaterial-assisted delivery of NGF for in vivo applications.
In a detailed study recently published by Zhu et al. NGF was incorporated into the conduit following its manufacture, preventing the biomolecule from being negatively affected by the organic solvents used during the electrospinning process.
In vitro studies demonstrated that the conduits enhanced and attracted the longitudinal neurite growth of the dorsal root ganglion DRG neurons toward their high-concentration gradient side. In vivo , the conduits directed a stronger longitudinal attraction of axons and migration of Schwann cells in 15 mm rat sciatic nerve defects.
At 12 weeks, rats transplanted with the conduits showed satisfactory morphological and functional improvements in g-ratio and total number and area of myelinated nerve fibers, as well as sciatic function index, compound muscle action potentials, and muscle wet weight ratio, as compared to aligned conduits with uniform NGF distribution.
The performance of the NGF-gradient aligned conduits was similar to that of autografts, demonstrating the great potential of the proposed scaffolds in repairing peripheral nerve defects. More commonly, NGF is incorporated homogeneously into the nanofibers by means of coaxial or emulsion electrospinning. In the study by Kuihua et al. This approach permitted stabilization of the NGF during the electrospinning process, and contributed to a controlled sustained release of NGF.
A sustained release of biologically active NGF was observed, using ELISA and a PC12 cell-based bioassay, over a day time period, although the number of neurons was lower than the positive control. The core-shell fibrous conduits were then used as a bridge implanted across a mm defect in the sciatic nerve of rats. The outcome in terms of regenerated nerve at 12 weeks was evaluated by a combination of electrophysiological assessment, histochemistry, and electron microscopy, and the results, taken together, demonstrated that the NGF-aligned fibers promoted peripheral nerve regeneration significantly better than the same conduit without NGF, suggesting that the released NGF may effectively promote the regeneration of peripheral nerves.
In the study by Zhang et al. In vitro tests revealed that the scaffold was able maintain a stable structure for at least 4 months in buffered solution, with a degradation rate comparable to the nerve growth rate.
Good biocompatibility and good cell adhesion with PC 12 cells were demonstrated. In vivo evaluation also showed that the composite fibrous conduit was effective at bridging a 20 mm sciatic nerve gap in adult rats within 10 months, and electrical stimulation through the conduit promoted Schwann cell migration and axonal regrowth.
In addition to coaxial electrospinning, emulsion electrospinning can be also used to incorporate biomolecules while preserving their bioactivity, a method used to load recombinant human NGF into the core of emulsion electrospun PLLA nanofibers Xia and Lv, The resulting nanofibrous scaffold was then additionally loaded with recombinant human vascular endothelial growth factor VEGF on the surface to achieve a controlled dual-delivery of the biomolecules.
After demonstrating that the scaffold enhanced neural differentiation of iPSC-NCSC cells in vitro , it was implanted into a critical-size defect in a rat sciatic nerve model.
Footprint analysis, electrophysiological tests, and histological analysis revealed a significant improvement in neovascularization and nerve healing 3 months after surgery. The potential of electrospinning to prepare an aligned fiber matrix able to influence the directionality and growth of axons in the CNS was investigated in the study by Colello et al.
Upon implantation in a completely transected rat spinal cord, the composite matrices supplemented with NGF and ChABC promoted significant functional recovery. Examination of the conduits post-implantation revealed that electrospun aligned fibers induced a more robust cellular infiltration than random fibers.
A vascular network was also generated in these matrices, since electrospun fibers acted as a growth substrate for endothelial cells. The presence of axons within the implanted electrospun matrix demonstrated that the aligned composite fibers containing NGF are able to provide trophic support and directional guidance cues to regenerating axons following spinal cord injury.
In a very recent and exhaustive study, emulsion electrospinning was used to develop innovative microenvironment-responsive pH-responsive immunoregulatory electrospun fibers to promote nerve function Xi et al.
IL-4 plasmid-loaded liposomes pDNA were then grafted onto the surface of the electrospun fiber scaffolds. The resulting biomimetic scaffold responded directly to the acidic microenvironment at focal areas, followed by triggered release of the IL-4 plasmid-loaded liposomes within a few hours to suppress the release of inflammatory cytokines and promote the neural differentiation of mesenchymal stem cells in vitro.
A Sprague Dawley SD rat spinal hemisection model was used to investigate the in vivo performance on inflammation suppression, nerve regeneration and functional recovery. Once implanted into the rats with acute spinal cord injury, the scaffold showed sustained NGF release, achieved by the core-shell structure, and brought a significantly shifted immune subtype to down-regulate the acute inflammation response, reduce scar tissue formation, promote angiogenesis and neural differentiation at the injury site, and enhance functional recovery in vivo.
Overall, electrospinning-based technologies allow an extraordinary range of manufacturing opportunities for finely tuned design suitable for topical application. Moreover, several studies have also demonstrated that NGF bioactivity is not compromised by the electrospinning processing, making this technology suitable for applications in dermatology, but also neurosurgery and orthopedics.
While biomacromolecules offer promising and possibly fundamental pharmaceutical treatments for controlling and tacking diseases, their action is hampered by severe limitations in delivery.
This is due to chemical and physical instabilities, as well as difficulties in crossing physiological barriers, and to being accumulated and released over time at the correct site of action Duskey et al.
Conventional drug delivery strategies cannot address these limitations leading to the increase in the number of polymeric or lipidic nanomedicine NMed applications which have incredible potential for the medical field Germain et al. Regarding NGF delivery by means of nanomedicines, several attempts have been made to improve loading and delivery across the BBB by engineering various polymers with different BBB targeting ligands. One example was the use of a poly alkyl-cyanoacrylate polymer coated with polysorbate 80 to promote BBB crossing Kurakhmaeva et al.
This coating promoted the adsorption of apolipoproteins onto the nanoparticle NPs surface, and the contact of the NPs with the brain capillary endothelial cells which promoted endocytosis and the intracellular release of the drug. The effects of NGF-loaded NPs persisted for 7 and 21 days following a single injection of the neurotoxin proving to be one of the most promising NMed carriers by preventing the scavenging of the NGF by the cells of the reticuloendothelial system, prolonging circulation of these particles in the blood and increasing their concentration in cerebral vessels.
Acute amnesia in mice was induced by subcutaneous injection of scopolamine before training in the step-through passive avoidance reflex PAR test to determine effects on memory Kurakhmaeva et al.
In contrast, systemic administration of the NGF in solution did not induce any significant changes in the mental or cognitive activity of the animals after induction of these changes by scopolamine pretreatment. The biocompatibility of these nanocarriers and the bioactivity of NGF were confirmed in rat pheochromocytoma PC12 cells. Following modification of the particle surface with Apo E, the particles were able to cross the BBB and remained bioactive in terms of neurite outgrowth regulation.
High-density lipoprotein HDL -mimicking NPs is a natural NP consisting of a lipid core coated with apolipoproteins, and a phospholipid monolayer which plays a critical role in the transport of lipids, proteins, and nucleic acids via its interaction with target receptors.
In another approach Song et al. PLGA is one of the most successful polymers used in the development of drug delivery systems, offering excellent biocompatibility and biodegradability of NPs Tan et al. It underwent Ultrasound US -mediated destruction to deliver NGF, resulting in diminished histological injury, neuron loss and neuronal apoptosis, and increased BBB scores in a rat model of spinal cord injury.
Chitosan, another widely used biodegradable and biocompatible polymer was used by Razavi et al. The encapsulation efficiency of NGF in chitosan nanoparticles is These NMeds were evaluated for their differentiation potential of human adipose-derived stem cells h-ADSCs to Schwann-like cells as a source for treating various diseases such as peripheral nerve regeneration multiple sclerosis and diabetic neuropathy Razavi et al.
When the NGF was released from the NPs, it induced the differentiation and neurite outgrowth of these cells through intracellular pathways. The therapeutic benefit of n NGF for CNS repair following injury was evaluated in a mouse model of compression-induced acute spinal cord injury.
After 21 days, extensive ankle movements and occasional plantar stepping was observed, representing a significant functional recovery in locomotion. Besides these results, widely reviewed in the past literature Ruozi et al.
Regarding the choice of NMed, its design and production, a major concern, still hotly debated, regards two main aspects of nanoproduction. This erroneous view of the magic bullet led to many years of research without any real or concrete advances in the translatability of NMeds to a clinical setting. Therefore, it is pivotal, when approaching a NMed design to consider the future NMed as a single product together with the embedded drug. The second aspect, especially when considering biomacromolecules such as NGF, proteins or enzymes, relates to the stability of the biological drugs throughout the preparation procedure and during storage.
The greatest drawback concerns the requirements of nanoproduction such as stirring, heating, sonication, organic solvents, etc.
Failure to take these aspects into consideration when designing the NMed risks rendering the loaded drug ineffective, thus defeating its purpose. Nerve growth factor cell and gene therapy for the CNS, in particular to target cholinergic degeneration in AD, has been investigated in preclinical models and also tested in human studies Hosseini et al. Neuropathological analysis then aimed to establish whether AAV2 -NGF engaged the target cholinergic neurons of the basal forebrain.
Following a mean survival of 4. Given that AAV2-NGF did not directly engage the target cholinergic neurons, the authors cannot conclude that growth factor gene therapy is effective for AD Castle et al.
Results were gathered from a third dose cohort of patients with mild to moderate AD, receiving second-generation NGF-ECB implants with improved NGF secretion, in an open-label, phase Ib dose escalation study with a 6-month duration. The data derived from this patient cohort demonstrate the safety and tolerability of sustained NGF release by a second-generation NGF-ECB implant to the basal forebrain.
In the adult centers, the nerve paths are something fixed, ended, and immutable. Everything may die, nothing may be regenerated. It is for the science of the future to change, if possible, this harsh decree. NGF can now be produced using human recombinant technologies, and molecules which can limit adverse side-effects are available either as modified full-length proteins or as TrkA short peptides analogs. We also need to protect the molecule from protein degradation, and promote the crossing of blood-tissue barriers, in order to bring the appropriate molecule concentration to the appropriate place for the appropriate time.
The use of modern biomaterial technologies is an essential strategy for rapidly achieving this goal. Scaffolds obtained by different fabrication procedures, such as hydrogels and composite materials are providing significant indications about efficacy of NGF delivery in peripheral nerve, but also in other tissues repairs, as bone, while nanoparticle conjugation is regarded as a promising strategy also to overcome physiological barriers. However, in view of clinical translation, we also need to move forward in preclinical research, which, at the present, provides a puzzling and incomplete picture of biomaterial potentiality.
In particular, we need well-designed proof-of-concept studies for both safety and efficacy, thus including appropriate control groups and defined functional end-points in the efficacy studies, and the Good Laboratory Practice standard for safety studies.
Because of this, a more stringent interdisciplinary collaboration would be desirable, such as a more stringent editorial policy in both biomaterial and biomedical journals. All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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