Paraoxonase 1 activity in the sperm-rich portion of boar ejaculates is positively associated with sperm quality

Lucca, Matheus Schardong; Goularte, Karina Lemos; Rovani, Monique Tomazele; Schneider, Augusto; Gasperin, Bernardo Garziera; Lucia Júnior, Thomaz; Rossi, Carlos Augusto Rigon

doi:10.1590/1984-3143-AR2022-0039

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ORIGINAL ARTICLE • Anim. Reprod. 19 (3) • 2022 • https://doi.org/10.1590/1984-3143-AR2022-0039 copy

Paraoxonase 1 activity in the sperm-rich portion of boar ejaculates is positively associated with sperm quality

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Associations of the activity of the paraoxonase 1 (PON1) enzyme with boar sperm quality still needs to be characterized, since boar ejaculates present distinct portions with differences in sperm concentration and quality. This study evaluated PON1 activity in the serum, in the distinct portions of boar ejaculates and estimated correlations with sperm quality parameters. Ejaculates and blood samples were collected from six boars for three weeks (two per week per boar; n = 36). Serum and post-spermatic portion PON1 activities were positively correlated (P = 0.01) but were both uncorrelated with the PON1 activity in the sperm-rich portion and in the whole ejaculate (P > 0.05). Differences in PON1 activity among boars were only observed in the sperm-rich portion of the ejaculate (P < 0.05). The PON1 activity in the serum and in the post-spermatic portion was generally negatively correlated with parameters of spermatozoa kinetics (P < 0.05). In the sperm-rich portion, PON1 activity was positively correlated with sperm concentration (P < 0.0001), curvilinear distance and velocity (both P < 0.05) and DNA integrity (P < 0.05), but negatively correlated with straightness and linearity (P < 0.05). Thus, boar ejaculates with increased PON1 activity in the sperm-rich portion may present increased concentration and spermatozoa with acceptable curvilinear velocity and distance and DNA integrity, which suggests that PON1 activity may be a biomarker for potential fertility.

Keywords:
PON1; spermatozoa kinetics; membrane integrity; DNA integrity

Boars	Paraoxonase 1 activity (UI mL^-1)
Boars	Blood Serum	Post-spermatic portion	Sperm-rich portion	Whole ejaculate
1	6.0 ± 1.4	0.14 ± 0.40	3.1 ± 0.4^AB	1.9 ± 0.5
2	8.8 ± 1.0	1.36 ± 0.31	3.3 ± 0.3^A	2.1 ± 0.3
3	9.1 ± 0.9	1.09 ± 0.28	3.3 ± 0.3^A	2.2 ± 0.4
4	9.7 ± 0.9	0.63 ± 0.29	1.5 ± 0.3^BC	1.3 ± 0.4
5	9.7 ± 0.9	0.74 ± 0.28	1.6 ± 0.3^BC	1.2 ± 0.3
6	10.2 ± 1.1	0.86 ± 0.29	1.0 ± 0.3^C	1.2 ± 0.3
Total	9.2 ± 2.4	0.85 ± 0.72	2.2 ± 1.2	1.6 ± 0.9

Parameter	Boars
Parameter	1	2	3	4	5	6
Sperm concentration/mL (x 10⁹)	3.6 ± 1.2^AB	5.8 ± 0.9^A	5,4 ± 0.9^A	3.1 ± 0.9^AB	2.0 ± 0.9^B	1.5 ± 0.9^B
Total motility (%)	84.2 ± 6.6	80.6 ± 5.1	74.2 ± 4.6	80.4 ± 4.3	78.5 ± 4.5	73.9 ± 4.6
Progressive motility (%)	71.3 ± 8.1	66.9 ± 6.3	54.9 ± 5.7	62.8 ± 5.5	63.5 ± 5.6	52.1 ± 5.8
Distance average path (µm)	20.1 ± 1.6	23.1 ± 1.2	20.3 ± 1.1	19.8 ± 1.1	22.9 ± 1.1	18.8 ± 1.1
Distance in a curved line (µm)	38.3 ± 3.2	44.7 ± 2.4	40.5 ± 2.2	39.5 ± 2.2	43.7 ± 2.2	35.0 ± 2.2
Distance in a straight line (µm)	15.4 ± 1.0	15.6 ± 0.8	13.9 ± 0.7	14.0 ± 0.7	15.9 ± 0.7	14.2 ± 0.7
Average path velocity (µm/s)	42.6 ± 3.9	51.3 ± 3.0	44.3 ± 2.7	42.7 ± 2,6	49.9 ± 2,6	40.4 ± 3,1
Velocity in a curved line (µm/s)	81.1 ± 7.1	98.6 ± 5.4	87.6 ± 5.9	84.6 ± 5.7	94.8 ± 5.6	74.9 ± 5,8
Velocity in a straight line (µm/s)	32.7 ± 2.3	34.5 ± 1.7	30.1 ± 1.6	30.2 ± 1.4	34.7 ± 1.5	30.6 ± 1.6
Straightness (%)	75.9 ± 2.6	67.2 ± 2.0	68.4 ± 1.8	70.6 ± 1.9	69.8 ± 1.9	75.4 ± 1.9
Linearity (%)	39.9 ± 1.8	34.8 ± 1.4	34.2 ± 1.3	35,5 ± 1.3	36.5 ± 1.3	40.2 ± 1.3
Amplitude of lateral head displacement (%)	2.1 ± 0.3	3.3 ± 0.2	2.9 ± 0.2	2.7 ± 0.2	2.9 ± 0.2	2.4 ± 0.2
Beat cross frequency (%)	37.0 ± 1.1^A	33.2 ± 0.9^AB	31.8 ± 0.8^B	32.3 ± 0.8 ^B	33.5 ± 0.8^AB	31.9 ± 0.8^B
Wobble (%)	0.52 ± 0.02	0.51 ± 0.01	0.50 ± 0.01	0.50 ± 0.01	0.52 ± 0.01	0.53 ± 0.01

Parameter	Boars
Parameter	1	2	3	4	5	6
DNA integrity (%)	99.8 ± 6.2	95.4 ± 4.8	94.9 ± 4.4	90.7 ± 4.4	98.0 ± 4.2	94.1 ± 4.3
Acrosome integrity (%)	95.6 ± 1.0	86.4 ± 8.6	92.7 ± 7.8	84.6 ± 8.0	80.2 ± 7.9	84.2 ± 7.8
Membrane integrity (%)	89.1 ± 4.7	75.9 ± 3.6	90.7 ± 3.3	82.0 ± 3.2	81.1 ± 3.3	83.4 ± 3.0
Mitochondrial functionality (%)	89.7 ± 8.2	63.9 ± 6.3	86.4 ± 5.7	80.3 ± 5.6	71.2 ± 5.7	73.9 ± 5.8

Parameter	Mean ± SD^*	Paraoxonase 1 activity
Parameter	Mean ± SD^*	Blood Serum	Post-spermatic portion^†	Sperm-rich portion	Whole ejaculate
Total motility (%)	78.6 ± 10.6	-0.31 (P = 0.08)	-0.34 (P = 0.06)	0.11 (P = 0.53)	-0.14 (P = 0.43)
Progressive motility (%)	62.0 ± 14.0	-0.51 (P = 0.03)	-0.35 (P = 0.05)	0.11 (P = 0.59)	-0.26 (P = 0.14)
Distance average path (µm)	20.8 ± 3.0	-0.36 (P = 0.04)	-0.18 (P = 0.32)	0.28 (P = 0.11)	-0.10 (P = 0.58)
Distance in a curved line (µm)	40.3 ± 5.9	-0.24 (P = 0.18)	-0.11 (P = 0.55)	0.35 (P = 0.05)	-0.01 (P = 0.96)
Distance in a straight line (µm)	14.7 ± 1.7	-0.35 (P = 0.04)	-0.36 (P = 0.04)	0.12 (P = 0.49)	-0.27 (P = 0.13)
Average path velocity (µm/s)	45.2 ± 7.4	-0.39 (P = 0.03)	-0.16 (P = 0.36)	0.29 (P = 0.12)	-0.08 (P = 0.65)
Velocity in a curved line (µm/s)	87.0 ± 13.4	-0.29 (P = 0.10)	-0.10 (P = 0.59)	0.37 (P = 0.04)	-0.01 (P = 0.99)
Velocity in a straight line (µm/s)	32.2 ± 4.0	-0.42 (P = 0.02)	-0.34 (P = 0.06)	0.16 (P = 0.37)	-0.25 (P = 0.17)
Straightness (%)	71.0 ± 0.05	0.16 (P = 0.39)	-0.04 (P = 0.81)	-0.36 (P = 0.04)	-0.21 (P = 0.26)
Linearity (%)	37.0 ± 0.03	-0.12 (P = 0.56)	-0.28 (P = 0.12)	-0.37 (P = 0.04)	-0.32 (P = 0.08)
Amplitude of lateral head displacement (%)	2.7 ± 0.6	-0.24 (P = 0.19)	-0.02 (P = 0.91)	0.32 (P = 0.08)	-0.06 (P = 0.72)
Beat cross frequency (%)	32.9 ± 2.3	-0.34 (P = 0.06)	-0.11 (P = 0.56)	0.17 (P = 0.36)	-0.12 (P = 0.50)
Wobble (%)	0.5 ± 0.03	-0.29 (P = 0.11)	-0.29 (P = 0.11)	-0.17 (P = 0.35)	-0.21 (P = 0.24)

Parameter	Mean ± SD *	Paraoxonase 1 activity
Parameter	Mean ± SD *	Blood Serum	Post-spermatic portion	Sperm-rich portion	Whole ejaculate
DNA integrity (%)	95.4 ± 10.2	-0.37 (P = 0.04)	-0.19 (P = 0.29)	0.38 (P = 0.03)	0.06 (P = 0.76)
Acrosome integrity (%)	87.5 ± 18.7	-0.14 (P = 0.43)	-0.12 (P = 0.50)	0.18 (P = 0.32)	0.05 (P = 0.19)
Membrane integrity (%)	89.9 ± 10.6	-0.13 (P = 0.49)	-0.14 (P = 0.43)	0.15 (P = 0.39)	0.25 (P = 0.16)
Mitochondrial functionality (%)	77.7 ± 15.7	-0.07 (P = 0.71)	-0.20 (P = 0.27)	0.19 (P = 0.28)	0.24 (P = 0.18)

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[1] *Corresponding author: carlos.rossi.mv@gmail.com