Expression of ezrin protein and phosphorylated ezrin in pelvic endometriotic lesions

Peloggia, Alessandra; Andres, Marina Paula; Abrão, Mauricio Simões

doi:10.1016/j.clinsp.2022.100074

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Original articles • Clinics 77 • 2022 • https://doi.org/10.1016/j.clinsp.2022.100074 copy

Expression of ezrin protein and phosphorylated ezrin in pelvic endometriotic lesions

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Objective:

To evaluate the expression of Ezrin and Phosphorylated Ezrin (Phospho-Ezrin) in endometriosis lesions and its relation to the menstrual cycle phase, stage of endometriosis, histological classification, and clinical symptoms.

Material and methods:

The authors conducted a retrospective study, with endometriotic lesions collected from women with endometriosis (n = 57) who underwent laparoscopy from 2017 to 2018. The expression of Ezrin and Phosphorylated Ezrin proteins was analyzed by immunohistochemistry.

Results:

All the endometriotic lesions contained immunostaining for Ezrin in the glands. Phosphorylated Ezrin was expressed in the stroma of all endometriotic lesions. There was no difference in the Ezrin and Phosphorylated Ezrin’s expression in the retrocervical, ovarian, superficial, and intestinal lesions in the same patient. Dysmenor-rhea, dyspareunia, acyclic pain, infertility, and dysuria were similar in the three groups of Ezrin staining. There was an inversely proportional relationship between severe dyschezia and Ezrin’s intensity, being 66.7% of Ezrin 1 (weak intensity), 36.7 Ezrin 2 (moderate intensity), and 10.0% of Ezrin 3 (p = 0.013). Regarding Phospho-Ezrin there wasn’t a significant difference between all the analyzed variables. Histological classification and menstrual cycle phase had also no significant difference between Ezrin and Phospho-Ezrin immunostaining.

Conclusion:

Ezrin protein and Phospho-Ezrin can be considered important markers to elucidate the mechanisms related to migration and attachment of endometriotic lesions. It is still unclear if Ezrin and Phospho-Ezrin are a cause or consequence of endometriosis. Further studies comparing different types of lesions and eutopic endometrium are necessary to elucidate the role of these proteins in the pathogenesis of endometriosis.

HIGHLIGHTS

The implantation of endometrial cells in the pelvic cavity has been related to some factors such as a receptive environment that allows the implantation and proliferation of these cells.
Several studies have shown the participation of the Ezrin protein in the process of invasion of malignant cells.
The expression of Ezrin and its activated form was observed in endometriotic lesions providing great evidence that these proteins can play an important role in the migration and attachment of endometriotic lesions.

Characteristics	Ezrin			p
Characteristics	1	2	3	p
Age (years)	38.0±4.2	36.2±6.0	35.4±4.4	0.540^a a ANOVA.
BMI (kg/m²)	22.1±1.7	24.1±6.0	23.4±3.0	0.522^b b Kruskal-Wallis Test.
Phase of the menstrual cycle				0.282^c c Fischer’s Exact Test.
Proliferative	2 (8.7)	10 (43.5)	11 (47.8)
Secretory	5 (14.7)	20 (58.8)	9 (26.5)
ASRM Stage				0.921^c c Fischer’s Exact Test.
I	0 (0)	2 (6.7)	2 (10.0)
II	2 (28.6)	10 (33.3)	8 (40.0)
III	2 (28.6)	6 (20.0)	2 (10.0)
IV	3 (42.9)	12 (40.0)	8 (40.0)
Dysmenorrhea (VAS)				0.556^c c Fischer’s Exact Test.
< 7	1 (16.7)	10 (33.3)	4 (20.0)
≥ 7	5 (83.3)	20 (66.7)	16 (80.0)
Dyspareunia (VAS)				0.703^c c Fischer’s Exact Test.
< 7	5 (83.3)	21 (70.0)	13 (65.0)
≥ 7	1 (16.7)	9 (30.0)	7 (35.0)
Acyclic pain (VAS)				0.195^c c Fischer’s Exact Test.
< 7	4 (66.0)	24 (80.0)	11 (55.0)
≥ 7	2 (33.3)	6 (20.0)	9 (45.0)
Cyclic Dyschezia (VAS)				0.013^c c Fischer’s Exact Test.
< 7	2 (33.3)	19 (63.3)	18 (90.0)
≥ 7	4 (66.7)	11 (36.7)	2 (10.0)
Cyclic dysuria (VAS)				0.088^c c Fischer’s Exact Test.
< 7	5 (83.3)	30 (100)	19 (95.0)
≥ 7	1 (16.7)	0 (0)	1 (5.0)
Infertility				0.240^c c Fischer’s Exact Test.
No	0 (0)	7 (29.2)	2 (11.8)
Yes	6 (100)	17 (70.8)	15 (88.2)

Characteristics	Phospho-Ezrin			p
Characteristics	1	2	3	p
Age (years)	39.4 ± 3.8	35.5 ± 5.4	35.0 ± 3.6	0.895^a a ANOVA.
BMI (kg/m²)	23.2 ± 2.3	23.8 ± 5.3	23.0 ± 1.0
Phase of the menstrual cycle
Proliferative	3 (33.3)	20 (44.4)	0 (0)	0.103^b b Kruskal-Wallis Test.
Secretory	6 (66.7)	25 (55.6)	3 (100)
ASRM Stage				0.828^c c Fischer’s Exact Test.
I	0 (0)	4 (8.9)	0 (0)
II	5 (55.6)	14 (31.1)	1 (33.3)
III	1 (11.1)	9 (20.0)	0 (0)
IV	3 (33.3)	18 (40.0)	2 (66.7)
Dysmenorrhea (VAS)				0.193^c c Fischer’s Exact Test.
< 7	4 (50.0)	10 (22.2)	1 (33.3)
≥ 7	4 (50.0)	35 (77.8)	2 (66.7)
Dyspareunia (VAS)				0.538^c c Fischer’s Exact Test.
< 7	7 (87.5)	30 (66.7)	2 (66.7)
≥ 7	1 (12.5)	15 (33.3)	1 (33.3)
Acyclic pain (VAS)				0.732^c c Fischer’s Exact Test.
< 7	6 (75.0)	30 (66.7)	3 (100)
≥ 7	2 (25.0)	15 (33.3)	0 (0)
Cyclic dyschezia (VAS)				0.633^c c Fischer’s Exact Test.
< 7	5 (62.5)	31 (68.9)	3 (100)
≥ 7	3 (37.5)	14 (31.1)	0 (0)
Cyclic dysuria (VAS)				0.100^c c Fischer’s Exact Test.
< 7	8 (100)	43 (95.6)	3 (100)
≥ 7	0 (0)	2 (4.4)	0 (0)
Infertility				0.822^c c Fischer’s Exact Test.
No	1 (11.8)	8 (22.9)	0 (0)
Yes	8 (88.9)	27 (77.1)	3 (100)

Histological type	Ezrin 1		Ezrin 2		Ezrin 3		p
Histological type	n	%	n	%	n	%	p
Deep retrocervical							0.906^a a Fischer’s exact test.
Estromal pure	0	0.0%	1	100.0%	0	0.0%
Glandular differentiated	1	50.0%	1	50.0%	0	0.0%
Glandular mixed	4	13.3%	14	46.7%	12	40.0%
Glandular undifferentiated	1	10.0%	5	50.0%	4	40.0%
Deep intestinal							0.771^a a Fischer’s exact test.
Estromal pure	0	0	0	0	0	0
Glandular differentiated	1	20.0%	2	40.0%	2	40.0%
Glandular mixed	3	14.3%	13	61.9%	5	23.8%
Glandular undifferentiated	0	0.0%	3	50.0%	3	50.0%
Superficial lesion							0.077^a a Fischer’s exact test.
Estromal pure	0	0	0	0	0	0
Glandular differentiated	1	100.0%	0	0.0%	0	0.0%
Glandular mixed	3	23.1%	5	38.5%	5	38.5%
Glandular undifferentiated	1	4.8%	10	47.6%	10	47.6%
Ovarian lesion							0.156^a a Fischer’s exact test.
Estromal pure	0	0	0	0	0	0
Glandular differentiated	1	33.3%	0	0.0%	2	66.7%
Glandular mixed	0	0	0	0	0	0
Glandular undifferentiated	1	20.0%	2	40.0%	2	40.0%

Histological type	Phospho-Ezrin 1		Phospho-Ezrin 2		Phospho-Ezrin 3		p
Histological type	n	%	n	%	n	%	p
Deep retrocervical							0.846^a a Fischer’s Exact test.
Estromal pure	0	0.0	1	100.0	0	0.0
Glandular differentiated	0	0.0	2	100.0	0	0.0
Glandular mixed	4	13.3	24	80.0	2	6.7
Glandular undifferentiated	2	20.0	7	70.0	1	10.0
Deep intestinal							0.257^a a Fischer’s Exact test.
Estromal pure	0	0.0	0	0.0	0	0.0
Glandular differentiated	0	0.0	5	100.0	0	0.0
Glandular mixed	5	23.8	13	61.9	3	14.3
Glandular undifferentiated	0	0.0	6	100.0	0	0.0
Superficial lesion							0.919^a a Fischer’s Exact test.
Estromal pure	0	0.0	0	0.0	0	0.0
Glandular differentiated	0	0.0	1	100.0	0	0.0
Glandular mixed	2	15.4	10	76.9	1	7.7
Glandular undifferentiated	4	19.0	17	81.0	0	0.0
Ovarian lesion							0.501^a a Fischer’s Exact test.
Estromal pure	0	0.0	0	0.0	0	0.0
Glandular differentiated	0	0.0	3	100.0	0	0.0
Glandular mixed	0	0.0	0	0.0	0	0.0
Glandular undifferentiated	1	20.0	3	60.0	1	20.0

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[1] * Corresponding author. E-mail address: msabrao@mac.com (M.S. Abrão).