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Polyethylene glycol fusion repair of severed rat sciatic nerves reestablishes axonal continuity and reorganizes sensory terminal fields in the spinal cord

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Neural Regeneration Research 2025年第7期20卷 2095-2107页

作者： Emily A.Hibbard Liwen Zhou Cathy Z.Yang Karthik Venkudusamy Yessenia Montoya Alexa Olivarez geo.ge d.bittner dale R.Sengelaub Program in Neuroscience Indiana UniversityBloomingtonINUSA department of Neuroscience University of Texas at AustinAustinTXUSA

Peripheral nerve injuries result in the rapid degeneration of distal nerve segments and immediate loss of motor and sensory functions;behavioral recovery is typically *** used a plasmalemmal fusogen,polyethylene glycol(PEG),to immediately fuse closely apposed open ends of severed proximal and distal axons in rat sciatic *** have previously reported that sciatic nerve axons repaired by PEG-fusion do not undergo Wallerian degeneration,and PEG-fused animals exhibit rapid(within 2–6 weeks)and extensive locomotor ***,our previous report showed that PEG-fusion of severed sciatic motor axons was non-specific,i.e.,spinal motoneurons in PEG-fused animals were found to project to appropriate as well as inappropriate target *** this study,we examined the consequences of PEG-fusion for sensory axons of the sciatic *** adult male and female rats(Sprague–dawley)received either a unilateral single cut or ablation injury to the sciatic nerve and subsequent repair with or without(Negative Control)the application of *** action potentials recorded immediately after PEG-fusion repair confirmed conduction across the injury *** success of PEG-fusion was confirmed through Sciatic Functional Index testing with PEG-fused animals showing improvement in locomotor function beginning at 35 days *** 2–42 days postoperatively,we anterogradely labeled sensory afferents from the dorsal aspect of the hindpaw following bilateral intradermal injection of wheat germ agglutinin conjugated horseradish ***-fusion repair reestablished axonal *** to unoperated animals,labeled sensory afferents ipsilateral to the injury in PEG-fused animals were found in the appropriate area of the dorsal horn,as well as inappropriate mediolateral and rostrocaudal ***,despite having intact peripheral nerves,similar reorganizations of labeled sensory afferents were also observed contralateral to the injury and repa

关键词： axotomy dorsal horn peripheral nerve injury plasticity polyethylene glycol(PEG) sciatic nerve sensory terminals wheat germ agglutinin horseradish peroxidase

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Polyethylene glycol has immunoprotective effects on sciatic allografts, but behavioral recovery and graft tolerance require neurorrhaphy and axonal fusion

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Neural Regeneration Research 2025年第4期20卷 1192-1206页

作者： Tyler A.Smith Liwen Zhou Cameron L.Ghergherehchi Michelle Mikesh Cathy Z.Yang Haley O.Tucker JuliAnne Allgood Jared S.Bushman geo.ge d.bittner department of Molecular Biosciences University of Texas at AustinAustinTXUSA department of Neuroscience University of Texas at AustinAustinTXUSA division of Pharmaceutical Sciences University of WyomingLaramieWYUSA

Behavioral recovery using(viable)peripheral nerve allografts to repair ablation-type(segmental-loss)peripheral nerve injuries is delayed or poor due to slow and inaccurate axonal ***,such peripheral nerve allografts undergo immunological rejection by the host immune *** contrast,peripheral nerve injuries repaired by polyethylene glycol fusion of peripheral nerve allografts exhibit excellent behavioral recovery within weeks,reduced immune responses,and many axons do not undergo Wallerian *** relative contribution of neurorrhaphy and polyethylene glycol-fusion of axons versus the effects of polyethylene glycol per se was unknown prior to this *** hypothesized that polyethylene glycol might have some immune-protective effects,but polyethylene glycol-fusion was necessary to prevent Wallerian degeneration and functional/behavioral *** examined how polyethylene glycol solutions per se affect functional and behavioral recovery and peripheral nerve allograft morphological and immunological responses in the absence of polyethylene glycol-induced axonal ***-type sciatic nerve injuries in outbred Sprague–dawley rats were repaired according to a modified protocol using the same solutions as polyethylene glycol-fused peripheral nerve allografts,but peripheral nerve allografts were loose-sutured(loose-sutured polyethylene glycol)with an intentional gap of 1–2 mm to prevent fusion by polyethylene glycol of peripheral nerve allograft axons with host *** to negative control peripheral nerve allografts not treated by polyethylene glycol and in contrast to polyethylene glycol-fused peripheral nerve allografts,animals with loose-sutured polyethylene glycol peripheral nerve allografts exhibited Wallerian degeneration for all axons and myelin degeneration by 7 days postoperatively and did not recover sciatic-mediated behavioral functions by 42 days *** morphological signs of rejection,such as col

关键词： allograft rejection axotomy macrophage myelin nerve repair polyethylene glycol(PEG) sciatic nerve T cell transplantation Wallerian degeneration

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Polyethylene glycol fusion repair of severed sciatic nerves accelerates recovery of nociceptive sensory perceptions in male and female rats of different strains

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Neural Regeneration Research 2025年第9期20卷 2667-2681页

作者： Liwen Zhou Karthik Venkudusamy Emily A.Hibbard Yessenia Montoya Alexa Olivarez Cathy Z.Yang Adelaide Leung Varun Gokhale Guhan Periyasamy Zeal Pathak dale R.Sengelaub geo.ge d.bittner department of Neuroscience University of TexasAustinTXUSA Program in Neuroscience Indiana UniversityBloomingtonINUSA department of Molecular Biosciences University of TexasAustinTXUSA

Successful polyethylene glycol fusion(PEG-fusion)of severed axons following peripheral nerve injuries for PEG-fused axons has been reported to:(1)rapidly restore electrophysiological continuity;(2)prevent distal Wallerian degeneration and maintain their myelin sheaths;(3)promote primarily motor,voluntary behavioral recoveries as assessed by the Sciatic Functional Index;and,(4)rapidly produce correct and incorrect connections in many possible combinations that produce rapid and extensive recovery of functional peripheral nervous system/central nervous system connections and reflex(e.g.,toe twitch)or voluntary *** preceding companion paper describes sensory terminal field reo rganization following PEG-fusion repair of sciatic nerve transections or ablations;howeve r,sensory behavioral recovery has not been explicitly explored following PEG-fusion *** the current study,we confirmed the success of PEG-fusion surgeries according to criteria(1-3)above and more extensively investigated whether PEG-fusion enhanced mechanical nociceptive recovery following sciatic transection in male and female outbred Sprague-dawley and inbred Lewis *** nociceptive responses were assessed by measuring withdrawal thresholds using von Frey filaments on the dorsal and midplantar regions of the *** von Frey filament tests were a more reliable method than plantar von Frey filament tests to assess mechanical nociceptive sensitivity following sciatic nerve *** withdrawal thresholds of the sciatic-mediated lateral dorsal region differed significantly across strain but not *** thresholds did not change significantly from baseline in chronic Unoperated and Sham-operated *** sciatic transection,all rats exhibited severe hyposensitivity to stimuli at the lateral dorsal region of the hindpaw ipsilateral to the ***,PEG-fused rats exhibited significantly earlier return to baseline withdrawal thresholds than Negative

关键词： autophagia axotomy collateral sprouting neuropathic pain peripheral nerve repair polyethylene glycol fusion(PEG-fusion) saphenous nerve sensory neurons sex and strain Wallerian degeneration

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Survival of rat sciatic nerve segments preserved in storage solutions ex vivo assessed by novel electrophysiological and morphological criteria

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Neural Regeneration Research 2023年第9期18卷 2082-2088页

作者： Liwen Zhou Monzer Alatrach Ted Zhao Paul Oliphint geo.ge d.bittner department of Neuroscience University of Texas at AustinAustinTXUSA

Most organ or tissue allografts with viable cells are sto red in solutions ex vivo for hours to seve ral *** allografts then require rapid host revascula rization upon transplantation to maintain donor-cell functions(e.g.,cardiac muscle contra ctions,hepatic secretions).In contrast,peripheral nerve allografts stored ex vivo do not require revascularization to act as scaffolds to guide outgrowth by host axons at 1-2 mm/d,likely aided by viable donor Schwann *** current storage solutions and protocols,axons in all these donor orga n/tissue/nerve transplants are expected to rapidly become non-viable due to Wallerian degeneration within ***,ex vivo storage solutions have not been assessed for preserving normal axonal functions,i.e.,conducting action potentials or maintaining myelin *** hypothesized that most or all organ storage solutions would maintain axonal *** examined several common organ/tissue storage solutions(University of Wisconsin Cold Storage Solution,Normosol-R,Normal Saline,and La ctated Ringe rs) for axonal viability in rat sciatic nerves ex vivo as assessed by maintaining:(1) conduction of artificially-induced compound action potentials;and(2) axonal and myelin morphology in a novel assay *** ten diffe rent storage solution conditions for peripheral nerves with viable axons(PNVAs) diffe red in their solution composition,osmolarity(250-318 mOsm),temperature(4℃ vs.25℃),and presence of *** action potentials and axonal morphology in PNVAs were best maintained for up to 9 days ex vivo in calcium-free hypotonic diluted(250 mOsm) Normosol-R(dNR) at 4℃.Surprisingly,compound action potentials were maintained for only 1-2 days in UW and NS at 4℃,a much shorter duration than PNVAs maintained in 4℃ dNR(9 days) or even in 25℃ dNR(5 days).Viable axons in peripheral nerve allografts are critical for successful polyethylene glycol(PEG)-fusion of viable proximal and distal ends of host axons with viable donor a

关键词： axonal morphometrics axonal viability calcium osmolarity peripheral nerve grafts peripheral nerve injury temperature tissue storage solutions tonicity Wallerian degeneration

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Repair and regeneration of peripheral nerve injuries that ablate branch points

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Neural Regeneration Research 2023年第12期18卷 2564-2568页

作者： JuliAnne E.Allgood geo.ge d.bittner Jared S.Bushman division of Pharmaceutical Sciences University of WyomingLaramieWYUSA department of Neuroscience The University of Texas at AustinAustinTXUSA

The peripheral nervous system has an extensive branching organization, and peripheral nerve injuries that ablate branch points present a complex challenge for clinical repair. Ablations of linear segments of the PNS have been extensively studied and routinely treated with autografts, acellular nerve allografts, conduits, wraps, and nerve transfers. In contrast, segmental-loss peripheral nerve injuries, in which one or more branch points are ablated so that there are three or more nerve endings, present additional complications that have not been rigorously studied or documented. This review discusses:(1) the branched anatomy of the peripheral nervous system,(2) case reports describing how peripheral nerve injuries with branched ablations have been surgically managed,(3) factors known to influence regeneration through branched nerve structures,(4) techniques and models of branched peripheral nerve injuries in animal models, and(5) conclusions regarding outcome measures and studies needed to improve understanding of regeneration through ablated branched structures of the peripheral nervous system.

关键词： allograft animal model branched injuries femoral nerve peripheral nerve injury peripheral nervous system regeneration repair sciatic nerve surgical repair

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Conundrums and confusions regarding how polyethylene glycol-fusion produces excellent behavioral recovery after peripheral nerve injuries

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Neural Regeneration Research 2018年第1期13卷 53-57页

作者： geo.ge d.bittner dale R.Sengelaub Cameron L.Ghergherehchi department of Neuroscience University of Texas at Austin department of Psychological and Brain Sciences Indiana University department of Molecular Biosciences University of Texas at Austin

Current Neuroscience dogma holds that transections or ablations of a segment of peripheral nerves produce：（1） Immediate loss of axonal continuity, sensory signaling, and motor control; （2） Wallerian rapid （1-3 days） degeneration of severed distal axons, muscle atrophy, and poor behavioral recovery after many months （if ever, after ablations） by slowly-regenerating （1 mm/d）, proximal-stump outgrowths that must specifically reinnervate denervated targets; （3） Poor acceptance of microsutured nerve allografts, even if tissue-matched and immune-suppressed. Repair of transections/ablations by neurorrhaphy and well-specified-sequences of PEG-fusion solutions （one containing polyethylene glycol, PEG） successfully address these problems. However, conundrums and confusions regarding unorthodox and dramatic results of PEG-fusion repair in animal model systems often lead to misunderstandings. For example, （1） Axonal continuity and signaling is re-established within minutes by non-specifically PEG-fusing （connecting） severed motor and sensory axons across each lesion site, but remarkable behavioral recovery to near-unoperated levels takes several weeks; （2） Many distal stumps of inappropriately-reconnected, PEG-fused axons do not ever （Wallerian） degenerate and continuously innervate muscle fibers that undergo much less atrophy than otherwise-denervated muscle fibers; （3） Host rats do not reject PEG-fused donor nerve allografts in a non-immuno-privileged environment with no tissue matching or immunosuppression; （4） PEG fuses apposed open axonal ends or seals each shut （thereby preventing PEG-fusion）, depending on the experimental protocol; （5） PEG-fusion protocols produce similar results in animal model systems and early human case studies. Hence, iconoclastic PEG-fusion data appropriately understood might provoke a re-thinking of some Neuroscience dogma and a paradigm shift in clinical treatment of peripheral nerve injuries.

关键词： axonal repair axotomy Wallerian degeneration polyethylene glycol allograft autograft nerve regeneration

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Methylene blue enhances polyethylene glycol-fusion repair of completely severed rat sciatic nerves

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Neural Regeneration Research 2021年第10期16卷 2056-2063页

作者： Cameron L.Ghergherehchi Jaimie T.Shores Joseph Alderete Erik K.Weitzel geo.ge d.bittner Institute for Cellular and Molecular Biology University of Texas at AustinAustinTXUSA department of Plastic and Reconstructive Surgery Johns Hopkins University School of MedicineBaltimoreMDUSA department of Surgery RESTOR LaboratorySan AntonioTXUSA department of Neuroscience University of Texas at AustinAustinTXUSA

Complete transection of peripheral mixed nerves immediately produces loss of sensory perception,muscle contractions and voluntary behavior mediated by the severed distal *** contrast to natural regeneration(~1 mm/d)of proximal axons that may eventually reinnervate denervated targets,re-innervation is restored within minutes by PEG-fusion that consists of neurorrhaphy and a sequence of well specified hypo-and isotonic calcium-free or calcium-containing solutions,the anti-oxidant methylene blue(MB)and the membrane fusogen polyethylene glycol(PEG).In this study,we examined the relative efficacy of PEG-fusion with no MB(0%),0.5%MB,or 1%MB on the recovery of voluntary behaviors by female Sprague-dawley rats with a complete mid-thigh severance of their sciatic nerve bathed in extracellular fluid or calcium-containing isotonic *** recovery of voluntary behaviors is the most relevant measure of success of any technique to repair peripheral nerve *** assessed recovery by the sciatic functional index,a commonly used measure of voluntary hindlimb behaviors following complete sciatic *** reported that both 1%MB and 0.5%MB in sterile distilled water in our PEG-fusion protocol with neurorrhaphy significantly increased the rate and extent of behavioral recovery compared to PEG plus neurorrhaphy ***,0.5%MB was as effective as 1%MB in voluntary behavioral recovery as assessed by the sciatic functional *** sterile 1%MB is no longer clinically available,we therefore recommend that 0.5%MB be included in upcoming human clinical trials to evaluate the safety and efficacy of *** animal procedures were approved by the University of Texas Institutional Animal Care and Use Committee(AUP-2019-00225)on September 9,2020.

关键词： axotomy methylene blue nerve repair neurorrhaphy peripheral nerve injury polyethylene glycol fusion sciatic nerve

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Functional and immunological peculiarities of peripheral nerve allografts

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Neural Regeneration Research 2022年第4期17卷 721-727页

作者： Kelly C.S.Roballo Jason P.Gigley Tyler A.Smith geo.ge d.bittner Jared S.Bushman School of Pharmacy University of WyomingLaramieWYUSA department of Molecular Biology University of WyomingLaramieWYUSA department of Molecular Biosciences University of Texas at AustinAustinTXUSA department of Neuroscience University of Texas at AustinAustinTXUSA

This review addresses the accumulating evidence that live(not decellularized)allogeneic peripheral nerves are functionally and immunologically peculiar in comparison with many other transplanted allogeneic *** is relevant because live peripheral nerve allografts are very effective at promoting recovery after segmental peripheral nerve injury via axonal regeneration and axon *** the immunological peculiarities of peripheral nerve allografts may also be of interest to the field of transplantation in *** topics are addressed:The first discusses peripheral nerve injury and the potential utility of peripheral nerve allografts for bridging segmental peripheral nerve defects via axon fusion and axon *** second reviews evidence that peripheral nerve allografts elicit a more gradual and less severe host immune response allowing for prolonged survival and function of allogeneic peripheral nerve cells and ***,potential mechanisms that may account for the immunological differences of peripheral nerve allografts are discussed.

关键词： allograft animal model immunology neuroimmunology peripheral nerve injury regeneration repair tissue regeneration tissue transplantation transplant

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Polyethylene glycol-fusion retards Wallerian degeneration and rapidly restores behaviors lost after nerve severance

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Neural Regeneration Research 2016年第2期11卷 217-219页

作者： geo.ge d.bittner Michelle Mikesh Cameron L.Ghergherehchi department of Neuroscience University of Texas at Austin

Some biological uses of polyethylene glycol（PEG）：The use of PEG as a membrane fusogen was first reported in 1976with the creation of cell hybrids,formed by suspending two cell lines in a 50%w/w solution of PEG in w... 详细信息

关键词： Figure PEG Polyethylene glycol-fusion retards Wallerian degeneration and rapidly restores behaviors lost after nerve severance

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Application and implications of polyethylene glycol-fusion as a novel technology to repair injured spinal cords

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Neural Regeneration Research 2015年第9期10卷 1406-1408页

作者： geo.ge d.bittner Kiran K.Rokkappanavar Jean d.Peduzzi department of Neuroscience University of Texas at Austin department of Biochemistry and Molecular Biology Wayne State University School of Medicine department of Anatomy & Cell Biology Department of Physical Medicine and Rehabilitation at Oakwood Wayne State University School of Medicine

Conventional vs. polyethylene glycol （PEG）-fusion tech- nologies to repair severed spinal axons： Most spinal cord injuries （SCIs） involve cutor crush-severance of spinal tract axons in the central nervous system （CNS）. Clinical out- comes after CNS axonal severance is very poor because proximal segments of CNS axons lack a suitable environment for outgrowth （Kakulas, 1999; Fitch and Silver, 2008; Rowland et al., 2008; Kwon et al., 2010） and therefore do not naturally regenerate （Ramon y Caial, 1928）. Current strategies to try to increase behavioral recovery after SCI are focused on en- hancing the environment for axonal outgrowth.

关键词： PEG Application and implications of polyethylene glycol-fusion as a novel technology to repair injured spinal cords

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