Vein wrapping facilitates basic fibroblast growth factor‐induced heme oxygenase‐1 expression following chronic nerve constriction injury

The clinical efficacy of autologous vein wrapping for recurrent compressive neuropathy has been demonstrated; however, the underlying mechanisms of this technique remain unclear. Rats were divided into chronic constriction injury (CCI) and CCI + vein wrapping (CCI + VW) groups. Mechanical allodynia was evaluated using von Frey filaments. To identify the neuroprotective factors released from veins, basic fibroblast growth factor (bFGF) mRNA expression in veins was compared to that in the sciatic nerve. The response of heme oxygenase‐1 (HO‐1) expression to vein wrapping was evaluated by RT‐PCR and enzyme‐linked immunosorbent assays. The effects of exogenous bFGF on HO‐1 expression were evaluated using a sciatic nerve cell culture. Vein wrapping significantly increased the withdraw threshold levels compared to the untreated CCI group. bFGF mRNA expression in veins was higher than that in untreated sciatic nerves. HO‐1 mRNA expression was induced at higher levels in sciatic nerve cells in the presence of exogenous bFGF compared to untreated control cells. HO‐1 mRNA and protein expression in the sciatic nerve were also higher in the CCI + VW group compared with the CCI group. Our results suggest that vein‐derived bFGF contributes to the therapeutic benefit of vein wrapping through the induction of HO‐1 in the sciatic nerve. Vein wrapping is a useful technique for reducing neuropathic pain. Further understanding of the neurotrophic factors released from veins may help to optimize current procedures for treating recurrent compressive neuropathy and traumatic peripheral nerve injury, and lead to the development of new therapeutic methods using recombinant neurotrophic factors. © 2017 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 36:898–905, 2018.

[1]  Y. Isobe,et al.  Oriented collagen tubes combined with basic fibroblast growth factor promote peripheral nerve regeneration in a 15 mm sciatic nerve defect rat model. , 2017, Journal of biomedical materials research. Part A.

[2]  Keisuke Sato,et al.  Epalrestat Upregulates Heme Oxygenase-1, Superoxide Dismutase, and Catalase in Cells of the Nervous System. , 2016, Biological & pharmaceutical bulletin.

[3]  Mireia Carcolé,et al.  The Induction of Heme Oxygenase 1 Decreases Painful Diabetic Neuropathy and Enhances the Antinociceptive Effects of Morphine in Diabetic Mice , 2016, PloS one.

[4]  Hongyu Zhang,et al.  The Role of bFGF in the Excessive Activation of Astrocytes Is Related to the Inhibition of TLR4/NFκB Signals , 2015, International journal of molecular sciences.

[5]  A. Lloyd,et al.  Macrophage-Induced Blood Vessels Guide Schwann Cell-Mediated Regeneration of Peripheral Nerves , 2015, Cell.

[6]  GuoLin Wang,et al.  H2Treatment Attenuated Pain Behavior and Cytokine Release Through the HO-1/CO Pathway in a Rat Model of Neuropathic Pain , 2015, Inflammation.

[7]  M. Hamdy,et al.  Functional and electrophysiological outcome after autogenous vein wrapping of primary repaired ulnar nerves , 2014, Microsurgery.

[8]  S. Ohtori,et al.  Vein wrapping for chronic nerve constriction injury in a rat model: study showing increases in VEGF and HGF production and prevention of pain-associated behaviors and nerve damage. , 2014, The Journal of bone and joint surgery. American volume.

[9]  N. N. Pathak,et al.  Atorvastatin attenuates neuropathic pain in rat neuropathy model by down-regulating oxidative damage at peripheral, spinal and supraspinal levels , 2014, Neurochemistry International.

[10]  R. Motterlini,et al.  Treatment with Carbon Monoxide-releasing Molecules and an HO-1 Inducer Enhances the Effects and Expression of µ-Opioid Receptors during Neuropathic Pain , 2013, Anesthesiology.

[11]  M. Siemionow,et al.  Techniques and materials for enhancement of peripheral nerve regeneration: A literature review , 2013, Microsurgery.

[12]  Gemma Gou,et al.  Effects of treatment with a carbon monoxide-releasing molecule and a heme oxygenase 1 inducer in the antinociceptive effects of morphine in different models of acute and chronic pain in mice , 2013, Psychopharmacology.

[13]  S. Ohtori,et al.  Differences Between Tumor Necrosis Factor–&agr; Receptors Types 1 and 2 in the Modulation of Spinal Glial Cell Activation and Mechanical Allodynia in a Rat Sciatic Nerve Injury Model , 2013, Spine.

[14]  R. Foresti,et al.  Emerging concepts on the anti-inflammatory actions of carbon monoxide-releasing molecules (CO-RMs) , 2012, Medical gas research.

[15]  L. Richard,et al.  Endoneurial Fibroblast-Like Cells , 2012, Journal of neuropathology and experimental neurology.

[16]  S. Mulgrew,et al.  Further Evidence for Treatment of Recalcitrant Neuropathy of the Upper Limb With Autologous Vein Wrapping , 2012, Annals of plastic surgery.

[17]  R. Motterlini,et al.  Carbon Monoxide Reduces Neuropathic Pain and Spinal Microglial Activation by Inhibiting Nitric Oxide Synthesis in Mice , 2012, PloS one.

[18]  D. Sotereanos,et al.  Vein wrapping at cubital tunnel for ulnar nerve problems. , 2010, Journal of shoulder and elbow surgery.

[19]  A. I. Rojo,et al.  Heme oxygenase-1 induction modulates microsomal prostaglandin E synthase-1 expression and prostaglandin E(2) production in osteoarthritic chondrocytes. , 2009, Biochemical pharmacology.

[20]  V. R. Prakash,et al.  Role of oxidative stress in pathophysiology of peripheral neuropathy and modulation by N‐acetyl‐l‐cysteine in rats , 2006, European journal of pain.

[21]  L. Joosten,et al.  Influence of heme oxygenase 1 modulation on the progression of murine collagen-induced arthritis. , 2005, Arthritis and rheumatism.

[22]  J. Thompson,et al.  Fibroblast Growth Factor-1 Induces Heme Oxygenase-1 via Nuclear Factor Erythroid 2-related Factor 2 (Nrf2) in Spinal Cord Astrocytes CONSEQUENCES FOR MOTOR NEURON SURVIVAL* , 2005 .

[23]  Y. Olsson,et al.  Mast cells in normal and sectioned peripheral nerve , 1965, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[24]  Jianwei Hou,et al.  Acceleration effect of basic fibroblast growth factor on the regeneration of peripheral nerve through a 15-mm gap. , 2003, Journal of biomedical materials research. Part A.

[25]  N. Weidner,et al.  Purification of Schwann cells by selection of p75 low affinity nerve growth factor receptor expressing cells from adult peripheral nerve , 2003, Journal of Neuroscience Methods.

[26]  D. Sotereanos,et al.  Neovascularization and other histopathologic findings in an autogenous saphenous vein wrap used for recalcitrant carpal tunnel syndrome: a case report. , 2003, The Journal of hand surgery.

[27]  Masahiko Takano,et al.  Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone‐marrow stromal cells , 2001, The European journal of neuroscience.

[28]  L. Schon,et al.  Surgical Treatment of Chronic Lower Extremity Neuropathic Pain , 2001, Clinical orthopaedics and related research.

[29]  M. Hirata,et al.  Heme oxygenase1 (HSP‐32) is induced in myelin‐phagocytosing Schwann cells of injured sciatic nerves in the rat , 2000, The European journal of neuroscience.

[30]  L. Schon,et al.  Peripheral Nerve Vein Wrapping For Intractable Lower Extremity Pain , 2000, Foot & ankle international.

[31]  D. Sotereanos,et al.  Recalcitrant post-surgical neuropathy of the ulnar nerve at the elbow: treatment with autogenous saphenous vein wrapping. , 2000, Journal of reconstructive microsurgery.

[32]  G. Lundborg,et al.  A Role of Migratory Schwann Cells in a Conditioning Effect of Peripheral Nerve Regeneration , 1999, Experimental Neurology.

[33]  L. Schon,et al.  Histopathologic Findings in Autogenous Saphenous Vein Graft Wrapping for Recurrent Tarsal Tunnel Syndrome: A Case Report , 1998, Foot & ankle international.

[34]  M. Tohyama,et al.  Growth factors prevent changes in Bcl-2 and Bax expression and neuronal apoptosis induced by nitric oxide , 1998, Cell Death and Differentiation.

[35]  A. Mizoguchi,et al.  Basic Fibroblast Growth Factor Promotes Extension of Regenerating Axons of Peripheral Nerve. In Vivo Experiments Using a Schwann Cell Basal Lamina Tube Model , 1997, Journal of neurocytology.

[36]  A. Cucina,et al.  bFGF release is dependent on flow conditions in experimental vein grafts. , 1995, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[37]  J. Herndon,et al.  Vein‐graft wrapping for the treatment of recurrent compression of the median nerve , 1995, Microsurgery.

[38]  T. Yaksh,et al.  Quantitative assessment of tactile allodynia in the rat paw , 1994, Journal of Neuroscience Methods.

[39]  M. Reidy,et al.  Basic fibroblast growth factor: its role in the control of smooth muscle cell migration. , 1993, The American journal of pathology.

[40]  E. Edelman,et al.  Perivascular and intravenous administration of basic fibroblast growth factor: vascular and solid organ deposition. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[41]  P. Stroobant,et al.  Platelet-derived growth factors and fibroblast growth factors are mitogens for rat Schwann cells , 1990, The Journal of cell biology.

[42]  D. Rifkin,et al.  Recent developments in the cell biology of basic fibroblast growth factor , 1989, The Journal of cell biology.

[43]  Gary J. Bennett,et al.  A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man , 1988, Pain.

[44]  W. Dixon,et al.  Efficient analysis of experimental observations. , 1980, Annual review of pharmacology and toxicology.

[45]  Thomas Pk,et al.  The connective tissue of peripheral nerve: an electron microscope study. , 1963 .

[46]  P. Thomas,et al.  The connective tissue of peripheral nerve: an electron microscope study. , 1963, Journal of anatomy.