Estradiol and progesterone differentially regulate formalin-induced nociception in ovariectomized female rats

Kuba, Tzipora; Wu, Hui-Bing K.; Nazarian, Arbi; Festa, Eugene D.; Barr, Gordon A.; Jenab, Shirzad; Inturrisi, Charles E.; Quiñones-Jenab, Vanya

doi:10.1016/j.yhbeh.2005.09.007

Cited by 79 publications

(57 citation statements)

References 64 publications

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“…Earlier studies in the goat revealed only minor sex differences in the responsiveness of TMJ nociceptive afferents despite significant sex differences in the biomechanical properties of the joint (Loughner et al 1997). In the formalin test for cutaneous pain, short-term (Kuba et al 2006) or long-term (Mannino et al 2007) E2 replacement in OvX rats significantly reduced formalin-induced flinching behavior in phase 2, whereas flinching during phase 1, thought to reflect peripheral sensitization, was not affected. Although P2X-positive neurons may represent only a fraction of the total number of TMJ afferents (Shinoda et al 2005), Western blot analysis revealed no significant group differences in P2X2 or P2X3 protein levels in trigeminal ganglion samples, suggesting that changes in receptor protein could not explain the effects of E2 on ATP-evoked TMJ unit activity.…”

Section: Mechanisms Of E2 Modulation Of Atp-evoked Activation Of Tmj mentioning

confidence: 80%

Differential Effects of Estradiol on Encoding Properties of TMJ Units in Laminae I and V at the Spinomedullary Junction in Female Rats

Tashiro¹,

Okamoto²,

Milam³

et al. 2007

Journal of Neurophysiology

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Tashiro A, Okamoto K, Milam SB, Bereiter DA. Differential effects of estradiol on encoding properties of TMJ units in laminae I and V at the spinomedullary junction in female rats. J Neurophysiol 98: 3242-3253, 2007. First published October 10, 2007 doi:10.1152/jn.00677.2007. To determine whether estrogen status modulated dorsal horn neural activity relevant to temporomandibular joint (TMJ) processing single units were recorded in superficial and deep laminae at the trigeminal subnucleus caudalis/upper cervical cord (Vc/C1-2) junction of ovariectomized (OvX) female rats under barbiturate anesthesia after 17␤-estradiol (E2) treatment for 2 days. E2 dose-dependently enhanced the response to intra-TMJ stimulation by adenosine triphosphate (ATP) of neurons classified as nociceptive specific (NS), but not wide dynamic range (WDR), in superficial laminae. ATP caused similar responses among NS and WDR neurons from deep laminae in all groups. By contrast, the cutaneous receptive field areas of WDR, but not NS, units in superficial and deep laminae were enlarged in high E2-treated (HE2) compared with low E2-treated (LE2) females. Units from untreated or vehicle-treated male rats displayed responses similar to those of LE2 females. TMJ units in superficial laminae from females were more likely to receive convergent cutaneous input and respond to jaw movement than males, independent of E2 treatment. Western blot analysis revealed similar levels of P2X2 and P2X3 receptor protein in Vc/C1-2 or trigeminal ganglion samples in all groups. Immunohistochemistry revealed dense terminal labeling for P2X3 receptors in superficial laminae and moderate labeling in deep laminae at the Vc/C1-2 junction. These data indicated a significant linkage between estrogen status and the magnitude of articular input evoked by ATP from TMJ neurons in the superficial laminae at the Vc/C1-2 junction, whereas estrogenic modulation of TMJ neurons in deep laminae affected only the convergent input from overlying facial skin.

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Section: Mechanisms Of E2 Modulation Of Atp-evoked Activation Of Tmj mentioning

confidence: 80%

Differential Effects of Estradiol on Encoding Properties of TMJ Units in Laminae I and V at the Spinomedullary Junction in Female Rats

Tashiro¹,

Okamoto²,

Milam³

et al. 2007

Journal of Neurophysiology

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“…Even though progesterone receptors have not been detected in the dorsal horn of the spinal cord (Kastrup et al, 1999), the possibility that progesterone also contributes to the effects of estrogen must be considered. Progesterone has indeed been shown to alter the nociceptive effects of estrogens (Drury and Gold, 1978;Kuba et al, 2006) at a spinal level (McCarthy et al, 1990;Medina et al, 1993;Ren et al, 2000) and to regulate nociception-related P2X3-receptor function in dorsal root ganglion neurons (Fan et al, 2011). Pregnancy-induced analgesia requires progesterone to become manifest so this analgesia is not seen in response to estrogens alone (Gintzler and Liu, 2001).…”

Section: Estrogen Receptor Neurons and The Endogenous Opioid Systemmentioning

confidence: 99%

Estrogenic influences in pain processing

Amandusson

Blomqvist

2013

Frontiers in Neuroendocrinology

111

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Gonadal hormones not only play a pivotal role in reproductive behavior and sexual differentiation, they also contribute to thermoregulation, feeding, memory, neuronal survival, and the perception of somatosensory stimuli. Numerous studies on both animals and human subjects have also demonstrated the potential effects of gonadal hormones, such as estrogens, on pain transmission. These effects most likely involve multiple neuroanatomical circuits as well as diverse neurochemical systems and they therefore need to be evaluated specifically to determine the localization and intrinsic characteristics of the neurons engaged. The aim of this review is to summarize the morphological as well as biochemical evidence in support for gonadal hormone modulation of nociceptive processing, with particular focus on estrogens and spinal cord mechanisms.

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“…Although animal studies showed that estradiol can attenuate pain (Gaumond et al, 2005;Kuba et al, 2006;Mannino et al, 2007) or has no effect (Mannino et al, 2005), there are also comparable animal studies that argue that estradiol exacerbates peripheral pain sensitization by decreasing mechanical threshold or increasing response to noxious stimuli administered to the colon and vagina (Bradshaw and Berkley, 2000;Evrard and Balthazart, 2004). Despite the controversy, we showed here that estradiol could exacerbate mechanical allodynia of inflamed TMJ in the ovariectomized rats, suggesting that rats with a higher level of plasma estradiol would be more sensitive to mechanical stimuli over the inflamed TMJ.…”

Section: Modulation Of Tmj Inflammatory Pain By Estradiolmentioning

confidence: 99%

17- -Estradiol Enhanced Allodynia of Inflammatory Temporomandibular Joint through Upregulation of Hippocampal TRPV1 in Ovariectomized Rats

Wu¹,

Bi²,

Kou³

et al. 2010

Journal of Neuroscience

105

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Temporomandibular disorders (TMDs) predominantly affect reproductive female patients, with pain the most frequent complaint. Although estrogens are believed to play important roles in TMD pain, the mechanism underlying modulation of TMD pain by estrogens remains largely unknown. Accumulating evidence implies that the hippocampus is involved in sexual dimorphism of pain sensitivity. In this study, we investigated the hippocampal TRPV1 (transient receptor potential vanilloid 1) expression in ovariectomized rats that received 17-␤-estradiol substitution and found that 17-␤-estradiol enhanced the mechanical allodynia of inflamed temporomandibular joint (TMJ) induced by complete Freund's adjuvant. Real-time PCR and immunoblotting demonstrated that TMJ inflammation significantly induced hippocampal TRPV1 expression compared with the control group but failed to induce it in the ovariectomized rats that received no estradiol replacement. In addition, estradiol potentiated TMJ inflammation-induced hippocampal TRPV1 expression in a dose-dependent manner in the ovariectomized rats. In contrast, TRPV1 transcription in amygdala, prefrontal cortex, and thalamus was not affected by TMJ inflammation and estradiol. Immunostaining showed TRPV1 localized in the processes and cytoplasm of pyramidal neurons in CA1-CA3 regions of the hippocampus. Moreover, intrahippocampal injection of TRPV1 antagonists capsazepine and 5Ј-iodoresiniferatoxin into the CA1 region of the hippocampus significantly attenuated allodynia of inflamed TMJ in both nonovariectomized and ovariectomized rats that received estradiol replacement. Our results suggested that hippocampal TRPV1 can modulate central pain processing and estradiol may contribute to the sexual dimorphism of TMD pain sensitivity through upregulation of TRPV1 expression in the hippocampus.

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Estradiol and progesterone differentially regulate formalin-induced nociception in ovariectomized female rats

Cited by 79 publications

References 64 publications

Differential Effects of Estradiol on Encoding Properties of TMJ Units in Laminae I and V at the Spinomedullary Junction in Female Rats

Differential Effects of Estradiol on Encoding Properties of TMJ Units in Laminae I and V at the Spinomedullary Junction in Female Rats

Estrogenic influences in pain processing

17- -Estradiol Enhanced Allodynia of Inflammatory Temporomandibular Joint through Upregulation of Hippocampal TRPV1 in Ovariectomized Rats

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