Sex-related difference in collateral sprouting of nociceptive axons after peripheral nerve injury in the rat

Alkayed, 1998, Gender-linked brain injury in experimental stroke, Stroke, 29, 159, 10.1161/01.STR.29.1.159 Bajrović, 2002, Interneuronal signalling is involved in induction of collateral sprouting of nociceptive axons, Neuroscience, 111, 587, 10.1016/S0306-4522(01)00588-7 Bajrović, 1998, Extent of nociceptive dermatomes in adult rats is not primarily maintained by axonal competition, Exp. Neurol., 150, 115, 10.1006/exnr.1997.6734 Behse, 1974, Endoneurial space and its constituents in the sural nerve of patients with neuropathy, Brain, 97, 773, 10.1093/brain/97.1.773 Brown, 1981, Motor nerve sprouting, Annu. Rev. Neurosci., 4, 17, 10.1146/annurev.ne.04.030181.000313 Coyle, 1995, Female rats are more susceptible to the development of neuropathic pain using the partial sciatic nerve ligation (PSNL) model, Neurosci. Lett., 186, 135, 10.1016/0304-3940(95)11304-F Decosterd, 2000, Spared nerve injury, Pain, 87, 149, 10.1016/S0304-3959(00)00276-1 Delcroix, 1997, Diabetes and axotomy-induced deficits in retrograde axonal transport of nerve growth factor correlate with decreased levels of p75LNTR protein in lumbar dorsal root ganglia, Brain Res. Mol. Brain Res., 51, 82, 10.1016/S0169-328X(97)00215-5 Devor, 1979, Two modes of cutaneous reinnervation following peripheral nerve injury, J. Comp. Neurol., 185, 211, 10.1002/cne.901850113 Diamond, 1987, Evidence that endogenous nerve growth factor is responsible for collateral sprouting, but not the regeneration, of nociceptive axons in adult rats, Proc. Natl. Acad. Sci. USA, 84, 6596, 10.1073/pnas.84.18.6596 Diamond, 1992, Regulation of the sensory innervation of skin, 309 Diamond, 1992, Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat, J. Neurosci., 12, 1454, 10.1523/JNEUROSCI.12-04-01454.1992 Doubleday, 1992, The role of nerve growth factor in collateral reinnervation by cutaneous C-fibres in the rat, Brain Res., 593, 179, 10.1016/0006-8993(92)91306-Y Gallo, 1997, The TrkA receptor mediates growth cone turning toward a localized source of nerve growth factor, J. Neurosci., 17, 5445, 10.1523/JNEUROSCI.17-14-05445.1997 Garcia-Segura, 2001, Neuroprotection by estradiol, Prog. Neurobiol., 63, 29, 10.1016/S0301-0082(00)00025-3 Gibbels, 1989, Morphometry of unmyelinated nerve fibers, Clin. Neuropathol., 8, 179 Groswasser, 1998, Female TBI patients recover better than males, Brain Inj., 12, 805, 10.1080/026990598122197 Hall, 1991, Sex differences in postischemic neuronal necrosis in gerbils, J. Cereb. Blood Flow Metab., 11, 292, 10.1038/jcbfm.1991.61 Hellweg, 1994, Axonal transport of endogenous nerve growth factor (NGF) and NGF receptor in experimental diabetic neuropathy, Exp. Neurol., 130, 24, 10.1006/exnr.1994.1181 Inbal, 1980, Autotomy following nerve injury, Pain, 9, 327, 10.1016/0304-3959(80)90047-0 Jackson, 1983, Failure of intact cutaneous mechanosensory axons to sprout functional collaterals in skin of adult rabbits, Brain Res., 273, 277, 10.1016/0006-8993(83)90851-X Jones, 1993, Gonadal steroids and neuronal regeneration, Adv. Neurol., 59, 227 Jones, 1993, Recovery from facial paralysis following crush injury of the facial nerve in hamsters, Exp. Neurol., 121, 133, 10.1006/exnr.1993.1079 Jones, 1994, Androgenic enhancement of motor neuron regeneration, Ann. NY Acad. Sci., 743, 141, 10.1111/j.1749-6632.1994.tb55791.x Jones, 2001, Neuroprotective effects of gonadal steroids on regenerating peripheral motoneurons, Brain Res. Rev., 37, 372, 10.1016/S0165-0173(01)00107-2 Jung-Testas, 1993, Stimulation of rat Schwann cell proliferation by estradiol, Dev. Brain Res., 72, 282, 10.1016/0165-3806(93)90194-F Jung-Testas, 1996, Demonstration of progesterone receptors in rat Schwann cells, J. Steroid Biochem. Mol. Biol., 58, 77, 10.1016/0960-0760(96)00009-X Kanje, 2000, Collateral sprouting from sensory and motor axons into an end to side attached nerve segment, NeuroReport, 11, 2455, 10.1097/00001756-200008030-00023 Kennedy, 1984, Collateral reinnervation of sweat glands, Ann. Neurol., 5, 73, 10.1002/ana.410150114 Kertesz, 1989, Sex equality in intrahemispheric language organization, Brain Lang., 37, 401, 10.1016/0093-934X(89)90027-8 Kimura, 1992, Sex differences in the brain, Sci. Am., 267, 118, 10.1038/scientificamerican0992-118 Kingery, 1989, The development of chronic mechanical hyperalgesia, autotomy and collateral sprouting following sciatic nerve section in rat, Pain, 38, 321, 10.1016/0304-3959(89)90219-4 Kinnman, 1987, Collateral sprouting of sensory axons in the hairy skin of the trunk, Brain Res., 414, 385, 10.1016/0006-8993(87)90021-7 Kinnman, 1992, Collateral reinnervation and expansive regenerative reinnervation by sensory axons into “foreign” denervated skin, Exp. Brain Res., 91, 61, 10.1007/BF00230013 Koenig, 1995, Progesterone synthesis and myelin formation by Schwann cells, Science, 268, 1500, 10.1126/science.7770777 Kovac̆ic̆, 1999, Recovery of cutaneous pain sensitivity after end-to-side nerve repair in the rat, J. Neurosurg., 91, 857, 10.3171/jns.1999.91.5.0857 Kujawa, 1991, Testosterone differentially regulates the regenerative properties of injured hamster facial motoneurons, J. Neurosci., 11, 3898, 10.1523/JNEUROSCI.11-12-03898.1991 Kujawa, 1993, Testosterone regulation of the regenerative properties of injured rat sciatic motor neurons, J. Neurosci. Res., 15, 268, 10.1002/jnr.490350306 Kume-Kick, 1994, Sex hormones affect muscle contractility and motor functional recovery following peroneal nerve crush, Exp. Neurol., 128, 115, 10.1006/exnr.1994.1118 Li, 1996, Gender influences the magnitude of the inflammatory response within embolic cerebral infarcts in young rats, Stroke, 27, 498, 10.1161/01.STR.27.3.498 Liu, 1999, Motor functional and morphological findings following end-to-side neurorrhaphy in the rat model, J. Orthop. Res., 17, 293, 10.1002/jor.1100170220 Liuzzi, 1999, Long-term estrogen replacement coordinately decreases trkA and beta-PPT mRNA levels in dorsal root ganglion neurons, Exp. Neurol., 155, 260, 10.1006/exnr.1998.6999 Loy, 1980, Sexual dimorphism in extent of axonal sprouting in rat hippocampus, Science, 208, 1282, 10.1126/science.7375941 Lundborg, 1994, Can sensory and motor collateral sprouting be induced from intact peripheral nerve by end to side anastomosis?, J. Hand Surg. (Br.), 19, 277, 10.1016/0266-7681(94)90069-8 Magnaghi, 1999, Po gene expression is modulated by androgens in the sciatic nerve of adult male rats, Mol. Brain Res., 70, 36, 10.1016/S0169-328X(99)00124-2 Markus, 1984, Spread of saphenous somatotopic projection map in spinal cord and hypersensitivity of the foot after chronic sciatic denervation in adult rat, Brain Res., 296, 27, 10.1016/0006-8993(84)90508-0 Matsumoto, 1999, Schwann cells can induce collateral sprouting from intact axons, J. Reconstr. Microsurg., 15, 281, 10.1055/s-2007-1000102 Mearow, 1995, Anti-NGF treatment blocks the upregulation of NGF receptor mRNA expression associated with collateral sprouting of rat dorsal root ganglion neurons, Neurosci. Lett., 184, 55, 10.1016/0304-3940(94)11167-H Mearow, 1994, Expression of NGF receptor and GAP-43 mRNA in DRG neurons during collateral sprouting and regeneration of dorsal cutaneous nerves, J. Neurobiol., 25, 127, 10.1002/neu.480250205 Nixon, 1984, Impulse activity evokes precocious sprouting of nociceptive nerves into denervated skin, Somatosens. Res., 2, 97, 10.1080/07367244.1984.11800553 Ochoa, 1978, Recognition of unmyelinated fiber disease, Muscle Nerve, 1, 375, 10.1002/mus.880010506 Ochoa, 1969, The normal sural nerve in man. I. Ultrastructure and numbers of fibres and cells, Acta Neuropathol., 13, 197, 10.1007/BF00690642 Owen, 1989, A role for nerve growth factor in collateral reinnervation from sensory nerves in the guinea pig, Brain Res., 476, 248, 10.1016/0006-8993(89)91245-6 Papka, 1997, Localization of estrogen receptor protein and estrogen receptor messenger RNA in peripheral autonomic and sensory neurons, Neuroscience, 79, 1153, 10.1016/S0306-4522(97)00076-6 Pertens, 1999, Intraspinal and behavioral consequences of nerve growth factor-induced nociceptive sprouting and nerve growth factor-induced hyperalgesia compared in adult rats, J. Comp. Neurol., 410, 73, 10.1002/(SICI)1096-9861(19990719)410:1<73::AID-CNE7>3.0.CO;2-3 Peyronnard, 1982, Motor and sensory neurons of the rat sural nerve, Muscle Nerve, 5, 654, 10.1002/mus.880050811 Pizzamiglio, 1985, Evidence for sex differences in brain organization in recovery in aphasia, Brain Lang., 25, 213, 10.1016/0093-934X(85)90081-1 Rabin, 1985, Autotomy following limb denervation, Pain, 21, 105, 10.1016/0304-3959(85)90280-5 Roof, 1993, Gender influences outcome of brain injury, Brain Res., 607, 333, 10.1016/0006-8993(93)91526-X Roof, 2000, Gender differences in acute CNS trauma and stroke, J. Neurotrauma, 17, 367, 10.1089/neu.2000.17.367 Shaywitz, 1995, Sex differences in the functional organization of the brain for language, Nature, 373, 607, 10.1038/373607a0 Sohrabji, 1994, Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory, J. Neurosci., 14, 459, 10.1523/JNEUROSCI.14-02-00459.1994 Stein, 2001, Brain damage, sex hormones and recovery, Trends Neurosci., 24, 386, 10.1016/S0166-2236(00)01821-X Subbarao, 1981, Reflex sympathetic dystrophy syndrome of the upper extremity, Arch. Phys. Med. Rehabil., 62, 549 Svenningsen, 1999, Estrogen and progesterone stimulate Schwann cell proliferation in a sex- and age-dependent manner, J. Neurosci. Res., 57, 124, 10.1002/(SICI)1097-4547(19990701)57:1<124::AID-JNR13>3.0.CO;2-P Swett, 1991, Sensory neurons of the rat sciatic nerve, Exp. Neurol., 114, 82, 10.1016/0014-4886(91)90087-S Tanzer, 1997, Gonadal steroid regulation of hamster facial nerve regeneration, Exp. Neurol., 146, 258, 10.1006/exnr.1997.6529 Tham, 1998, Motor collateral sprouting through an end-to-side nerve repair, J. Hand Surg. (Am.), 23, 844, 10.1016/S0363-5023(98)80161-5 Veldman, 1993, Signs and symptoms of reflex sympathetic dystrophy, Lancet, 342, 1012, 10.1016/0140-6736(93)92877-V Viterbo, 1992, Latero-terminal neurorraphy without removal of the epineural sheath, Rev. Paul. Med., 110, 267 Wall, 1979, Autotomy following peripheral nerve lesions, Pain, 7, 103, 10.1016/0304-3959(79)90002-2 Weddell, 1941, The local extension of nerve fibers into denervated areas of skin, J. Neurol. Psychol., 4, 206, 10.1136/jnnp.4.3-4.206 Young, 1940, Fibrin suture of peripheral nerves, Lancet, 2, 126, 10.1016/S0140-6736(01)07978-8 Yu, 1989, Survival of motoneurons following axotomy is enhanced by lactation or by progesterone treatment, Brain Res., 491, 379, 10.1016/0006-8993(89)90075-9 Zhang, 1998, Effects of gender and estradiol treatment on focal brain ischemia, Brain Res., 784, 321, 10.1016/S0006-8993(97)00502-7 Zhang, 1999, Evaluation of collateral sprouting after end-to-side nerve coaptation using a fluorescent double-labeling technique, Microsurgery, 19, 281, 10.1002/(SICI)1098-2752(1999)19:6<281::AID-MICR5>3.0.CO;2-D Zhao, 1997, Nerve regeneration after terminolateral neurorrhaphy, J. Rec. Microsurg., 13, 31, 10.1055/s-2008-1063938