Viewing a humorous film decreases IgE production by seminal B cells from patients with atopic eczema

Journal of Psychosomatic Research 66 (2009) 173 – 175

Viewing a humorous film decreases IgE production by seminal B cells from patients with atopic eczema Hajime Kimata⁎ Department of Allergy, Moriguchi-Keijinkai Hospital, Moriguchi, Osaka, Japan Received 7 September 2006; received in revised form 10 June 2008; accepted 11 June 2008

Abstract Objective: Sperms induced IgE production by seminal B cells from patients with atopic eczema via interaction of B cells with galectin-3 on sperms. We studied the effect of viewing a humorous film on IgE production by seminal B cells cultured with sperms. Methods: Twenty-four male patients with atopic eczema viewed a humorous film (Modern Times, featuring Charlie Chaplin). Just before and immediately after viewing, semen was collected, and seminal B cells and sperms were purified. Seminal B cells were cultured with sperms and IgE production was measured, while expression of galectin-3 on

sperms was assessed. Results: After viewing the humorous film, IgE production by B cells cultured with sperms was significantly decreased. Moreover, expression of galectin-3 on sperms was reduced. Conclusion: Viewing a humorous film reduced galectin-3 expression on sperms, which in turn decreased IgE production by seminal B cells cultured with sperms. These results indicate that viewing a humorous film may be helpful for the study and treatment of local IgE production and allergy in the reproductive tract. © 2009 Elsevier Inc. All rights reserved.

Keywords: Seminal B cells; IgE production; Galectin-3; Sperm; Atopic eczema; Viewing a humorous film; IL-6

Introduction Atopic eczema (AE) is a chronic inflammatory skin disease with enhanced IgE production. IgE production is modulated via IgE receptors (Fc epsilon receptor and galectin-3) on various cells [1,2]. IgE production was diminished by Th1 cytokine (IFN-γ, IL-12), while it was enhanced by Th2 cytokine (IL-4, IL-6, IL-10, IL-13) [3]. We previously reported that galectin-3 was expressed on sperms, and sperms increased IgE production by seminal B cells via interaction with galectin-3 with surface IgE on B cells from AE patients, but not from healthy subjects [4]. On the other hand, we and others have reported the various beneficial effects of viewing a humorous film on

⁎ Department of Allergy, Moriguchi-Keijinkai Hospital, 2-47-12, Yagumohigashimachi, Moriguchi, Osaka 570-0021, Japan. Tel.: +81 6 6906 9000; fax: +81 6 6906 9500. E-mail address: [email protected]. 0022-3999/08/$ – see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.jpsychores.2008.06.006

immune responses including (1) increase in natural killer activity in healthy subjects, (2) reduction of allergic skin wheal responses in AE patients, and (3) decrease in allergenspecific IgE production by peripheral blood B cells in AE patients [3,5,6]. Therefore, we hypothesize that viewing a humorous film may decrease IgE production by seminal B cells via interaction with sperms in AE patients. Methods Subjects After obtaining informed consent, 24 male patients with mild AE [scoring atopic dermatitis (SCORAD) index: mean 9, 95% CI 7–11] (mean age 30 years, range 24–36 years) were studied [7]. AE patients were treated with washing with povidone iodine and application of pinetar (Yoshida Pharmaceutical Co. Ltd., Tokyo, Japan) mixed with zinc oxide ointment, but without oral medication [3]. None of

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H. Kimata / Journal of Psychosomatic Research 66 (2009) 173–175

Table 1 Effect of viewing a humorous film on IgE production and galectin-3 expression Viewing a control film

Viewing a humorous film

Before viewing

Before viewing

After viewing

After viewing

(A) IgE production (ng/ml) by seminal B cells cultured with sperms 3.8 (0.5) 4.1 (0.6) 4.3 (0.6) 2.7 (0.3) ⁎ (B) Galectin-3 expression (ΔMFI) on sperms 36.5 (0.7) 37.2 (0.7) 36.9 (0.8)

21.2 (0.3) ⁎

(A) Seminal B cells and sperms were cultured before and after viewing a control film or a humorous film, and IgE production was measured. Values indicate means (S.E.M.) (N=24). (B) Gaelectin-3 expression on sperms was measured before and after viewing a control film or a humorous film. Values indicate means (S.E.M.) (N=24). ⁎ Significant decrease (P b.01) before viewing.

them had a sexually transmitted disease at the time of the study. They were randomly assigned to the study group after 5 days of sexual abstinence. Study design The study was conducted by crossover style. Twelve randomly assigned AE patients viewed an 87-min humorous film (Modern Times, featuring Charlie Chaplin), and after 2 weeks, they viewed an 87-min control nonhumorous film featuring weather information. On the other hand, another 12 AE patients first viewed the control film featuring weather information, and after 2 weeks, they viewed the same humorous video. Just before and immediately after viewing, semen was collected by masturbation. Motile sperm were obtained with the “swim-up” method [8]. Sperms were stained with biotinylated anti-galectin-3 mAb (Becton Dickinson, Mountain View, CA, USA), and cell surface expression of galectin-3 was analyzed as reported [1,2]. Semen was overlaid on Ficoll-Hypaque and centrifuged at 1500 rpm for 30 min. The interface was aspirated and mononuclear cells were collected. B cells were purified by sheep red blood cell rosetting and L-leucine methyl ester incubation methods [6]. Purified seminal B cells (2×104/0.2 ml per well) were cultured with sperms (2×105/0.2 ml per well) for 14 days, and IgE production was measured by ELISA [1,2]. In some experiments, seminal B cells obtained after viewing a control film (designated as “[control] seminal B cells”) or after viewing a humorous film (“[humorous] seminal B cells”) were either cocultured with sperms after viewing a control film ([control] sperms) or after a viewing a humorous film ([humorous] sperms) from different donors for 14 days, and IgE production was measured. [Control] seminal B cells or [humorous] seminal B cells (2×104/0.2 ml per well) were also co-cultured with [control] sperms or [humorous] sperms (2×105/0.2 ml per well) for 1 day, separated by panning, and thereafter seminal B cells alone (2×104/0.2 ml per well) were cultured. After 2 days, IL-6 production was measured by ELISA (R&D Systems) [3].

This study was approved by the Ethics Committee of Moriguchi-Keijinkai Hospital. Statistical analysis was performed with ANOVA. Results and discussion As shown in Table 1A, IgE production was significantly decreased in seminal B cells cultured with sperms after viewing a humorous film, but not after viewing a control film. IgE production by seminal B cells was induced via galectin-3 on sperms [3]. Thus, expression of galectin-3 on sperms was studied. As shown in Table 1B, expression of galectin-3 on sperms was significantly reduced after viewing a humorous film, but not after viewing a control film. These results suggest that decrease in IgE production was due to reduction of galectin-3 expression on sperms. However, it is possible that viewing a humorous film may affect seminal B cells, which in turn may decrease IgE production. To confirm this, seminal B cells were cocultured with sperms after viewing a control film or a humorous film. As shown in Table 2A, sperms obtained after viewing a humorous film decreased IgE production by seminal B cells whether they were obtained after viewing a control film or a humorous film. In contrast, sperms obtained after viewing a control film did not decrease IgE production by seminal B cells obtained after viewing a humorous film. Our previous study revealed that induction of IgE production by sperms was due to enhanced IL-6 production from seminal B cells [2]. As shown in Table 2B, preincubation of seminal B cells with sperms that were obtained after viewing a humorous film decreased IL-6

Table 2 Effect of viewing a humorous film on IgE and cytokine production in coculture (A)

IgE production (ng/ml)

[Control] seminal B cells+[control] sperms [Control] seminal B cells+[humorous] sperms [Humorous] seminal B cells+[humorous] sperms [Humorous] seminal B cells+[control] sperms

4.5 (0.6) 2.7 (0.2) ⁎ 2.5 (0.2) ⁎ 4.2 (0.5)

(B)

IL-6 production (pg/ml)

[Control] seminal B cells+[control] sperms [Control] seminal B cells+[humorous] sperms [Humorous] seminal B cells+[humorous] sperms [Humorous] seminal B cells+[control] sperms

29.5 (1.2) 17.9 (1.0) ⁎ 16.2 (0.9) ⁎ 29.1 (1.1)

(A) Seminal B cells obtained after viewing a control film ([control] seminal B cells) or a humorous film ([humorous] seminal B cells) were cocultured with sperms obtained after viewing a control film ([control] sperms) or a humorous film ([humorous] sperms), and IgE production was measured. Values indicate means (S.E.M.) (N=24). (B) [Control] or [humorous] seminal B cells were cocultured with [control] or [humorous] sperms for 1 day, washed, and then seminal B cells alone were cultured for 2 days, and IL-6 production was measured. Values indicate means (S.E.M.) (N=24). ⁎ Significant decrease (Pb.01) compared to cocultures of [control] seminal B cells+[control] sperms.

H. Kimata / Journal of Psychosomatic Research 66 (2009) 173–175

production by seminal B cells obtained after viewing a control film or a humorous film. In contrast, preincubation of seminal B cells with sperms that were obtained after viewing a control film failed to decrease IL-6 production by seminal B cells obtained after viewing a humorous film. Collectively, these results indicated that viewing a humorous film primarily affected sperms, which in turn decreased IgE production by seminal B cells. It was reported that stress reduced sperm numbers and motility [9]. Stress also modulated expression of receptors on various cells [10]. It was also reported that stress increased IgE production by skewing cytokine pattern toward Th2 type. That is, stress diminished Th1 cytokine production (IFN-γ, IL-12), while it enhanced Th2 cytokine production (IL-4, IL6, IL-10, IL-13) in blood or lymphocytes [11–13]. In contrast, reduction of stress decreased IgE production by skewing cytokine pattern toward Th1 type. That is, reduction of stress enhanced Th1 cytokine production, while it diminished Th2 cytokine production in blood or lymphocytes [6,12,14–16]. Therefore, it would be possible that viewing a humorous film may down-regulate galectin-3 expression on sperms, which in turn may diminish IL-6 production, resulting in decrease in IgE production by seminal B cells. Effects of reduction of stress on severity of AE (N=24) were also assessed. SCORAD index [mean (95 % CI)] at baseline, after viewing a humorous film, and after viewing a control film were 9 (7–11), 8 (6–10), and 9 (7–11), respectively. Although viewing a humorous film slightly improved severity of AE, this was not statistically significant (PN.05). However, it is tempting to speculate that skin symptoms may be improved if reduction of stress will be repeated by viewing a humorous film every day. This possibility is currently under investigation. Since allergy in reproductive tract is not unusual and fertilization is dependent on emotion, these results may be useful for the study of the effect of emotion on IgE production in the reproductive tract [17,18]. References [1] Sherr E, Macy E, Kimata H, Gilly M, Saxon A. Binding of the low affinity FceR on B cells suppress ongoing human IgE synthesis. J Immunol 1989;142:481–9.

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