Mast Cells in the Mammalian Testis and Epididymis—Animal Models and Detection Methods
Abstract
:1. Introduction
2. Mast Cell Disorders
2.1. Allergies
2.2. Contribution of Mast Cells to the Pathology of the Mammalian Testis and Epididymis
3. Evolutionarily Conserved Mast Cells
4. Mast Cell Detection Methods in the Mammalian Testis and Epididymis
5. Mast Cells in Mammalian Testes and Epididymides
5.1. Rodents (Rat, Mouse, Hamster, Other)
5.2. Domestic (Sus scrofa domestica) and Wild Boar (Sus scrofa ferrus)
5.3. Non-Human Primates
6. Experimental Models Investigating Mast Cells in Mammalian Testes
6.1. Gonadal Effects of Medications
6.2. Mast Cell Antagonists
6.3. Experimental Autoimmune Orchitis (EAO)
6.4. Stress
6.5. Hormones
6.6. Genetically Altered Animals
6.7. Cryptorchidism
Animal | Strain | Experiment | Analysis | Result—MC | Result—ST | Result—Interstitium | Fertility * | Ref. |
---|---|---|---|---|---|---|---|---|
ALKYLATING AGENTS | ||||||||
RAT | Wistar | EDS daily PND 5–16 | PND 6–108 | MC in interstitium at PND 17–35 and increased number of MCs under the TA PND 17–108 | valuolae in SCs, thick basal lamina from PND 11; atrophic ST with no GCs or lumen from PND 28; no recovery after treatment | no LC from PND 11 | NA | [69] |
Sprague-Dawley | EDS single dose | 0–49 days after treatment | MCs in interstitium, max. 21 days after EDS | ST volume decrease: lowest 14 days after treatment; control levels 35 days after treatment | no LC on day 3 after EDS, recovered 50% by day 28 after EDS | NA | [65] | |
Sprague-Dawley | 1. EDS treatment ± testosterone implant 2. immunization against oxytocin | 3–10 weeks after treatment | 1. MCs in interstitium 21 and 70 days after EDS treatment 2. no MCs in interstitium after oxytocin administration | 1. 3–4× increased GC degeneration 2. 2× increased GC degeneration | 1. LC depletion | 1. transient subfertility in 50% | [66] | |
Sprague-Dawley | EDS ± testosterone | 3–41 days after treatment | MC increase in interstitium 21–41 days post-treatment (EDS); slower increase with testosterone | NA | LC depletion, initial macrophage increase (3–10 days), then depletion, prevented by testosterone | NA | [53] | |
Wistar | 1. hypophysectomy ± EDS (adult) OR GnRH antagonist (prepubertal); colchicine 2. GnRH antagonist | 1–30 days after treatment | 1. MC proliferation on day 20 by EDS, MC number increase 15–30 day (control) and 15–50 day in hypophysectomiy + EDS 2. prolif. and diff. MC PND 23–30 | NA | 1. mitosis-3rd and 18–22nd day 2. immature LC and mitotic figures increase, normal by 30th day | NA | [61] | |
Sprague Dawley | cyclophosphamide ± ZnO NP | after 4 weeks of treatment | MC number increase in interstitium; ZnO NP reduced (near normal MC number) | ZnO NP reduced ST and GC atrophy, separation of germinal epithelium from BM, tubular wall vacuolization, sperm abnormalities | wide interstitium, vascular congestion, acidophilic material, clusters of dark LC; ZnO NP reduced | NA | [57] | |
MOUSE | NMRI | cyclophosphamide ± EP for 35 days | after treatment | MC number increase in interstitium; EP reduced | germinal epithelium disarrangement and thickening; EP reduces | LC depletion; EP reduced | NA | [84] |
INFLAMMATION | ||||||||
RAT | Wistar and Sprague-Dawley | EAO (3 injections every 15 days) | 7–80 days after 1st injection | MC degranulation, number elevation after 80 days, 2× Sprague-Dawley and 5× Wistar | aspermatogenesis at day 80 | mononuclear cell infiltrate at day 80 | NA | [67] |
Wistar | EAO | 50 & 80 days after EAO | MC number and degranulation increase; MC in interstitium | almost complete loss of GC | granuloma formation; PAR2+ cell number increase | NA | [47] | |
Wistar | testis puncture Ø 3 mm (=EAO) followed by skin suture ± ketotifen | 1–30 days after treatment | ketotifen reduced MC number and degranulation increase in interstitium | GC depletion and ST fibrosis; ketotifen (does not prevent damage but) retains regenerative capacity | NA | [74] | ||
Wistar | EAO ± ketotifen | 56 days after first treatment | ketotifen reduced MC number increase | ketotifen reduced severity of histopathological testicular damage | ketotifen reduced testicular damage | NA | [117] | |
MOUSE | C57BL6/N or C57BL/6J | EAEO | 30–80 days after 1st immunisation | MC number increase in interstitium from low to high-grade EAEO | severe EAEO: ST diameter reduction, germ cell sloughing, SC-only tubules | macrophage and leukocyte number increase, fibrosis around ST | NA | [77] |
TORSION AND STRESS | ||||||||
RAT | Sprague–Dawley | torsion ± ketotifen | 30 days after treatment | ketotifen reduced increased MC numbers—contralateral testis | ketotifen reduced germinal epithelium sloughing, ST atrophy, walls fibrosis—contralateral testis | interstitial edema | NA | [117] |
Sprague-Dawley | torsion-detorsion ± VIP (2 or 4 h); prepubertal | after torsion | MC degranulation; VIP—protective effect (2 h); no MCs in interstitium | histological abnormalities; VIP reduced (2 h torsion) | histological abnormalities; VIP reduced (2 h torsion) | NA | [48] | |
Sprague-Dawley | torsion; contralateral testis analysis | 10, 30, and 80 days after torsion | maximum increase in MC number 30 days post-op | germinal epithelium sloughing (spermatocyte and spermatid apoptosis), ST atrophy, fibrosis, diameter, and Johnsen score decrease; possible reversibility | interstitial edema, T-lymphocyte, and macrophage number elevation | NA | [64] | |
MOUSE | dYY | torsion; contralateral testis analysis | 4–24 weeks after torsion | MC number increase in interstitium, maximum 8 weeks post-op | no histological changes | no histological changes | NA | [75] |
RAT | Wistar | 1. immobilisation cold stress 3h 3 days PND 15, 30, 45 ± VIP 2. β-endorphin + immobilisation PND 45 ± VIP | after treatment | 1. VIP reduced MC degranulation and maturation 2. VIP reduced MC degranulation and maturation | NA | 1. VIP prevented focal LC depletion | NA | [72] |
Wistar | torsion/detorsion ± hypothermia for 30 or 90′ prior to detorsion | 8 weeks after operation | torsion/detorsion significantly increased MC number | hypothermia increased Johansen score, reduced by torsion/detorsion | hypothermia ameliorated interstitial edema | NA | [120] | |
HORMONE TREATMENT | ||||||||
RAT | Wistar | EB on PND 1 | PND 45 and 90 | strong increase of MC number, interstitium at PND 45 | maturation arrest at the level of pachytene spermatocytes | increased proportion of interstitium (fibrosis and edema) | NA | [44] |
Wistar | 1. EB on PND 1 2. testosterone propionate on PND 1 | PND 45 | 1. MC number increase after estrogen in the testis 2. no effect | 1. impaired spermatogenesis | 1. immature interstitial cells | NA | [70] | |
Wistar | EB on PND 1 | PND 15–90 | MC in interstitium on PND 17, increase in number by PND 45 and mature by PND 90 | NA | mature LC from PND 90 | NA | [45] | |
Wistar | 1. EB treatment on PND 1 2. EDS (adult) | 1. PND 35–70 2. 5 days after treatment | 1. strong increase of MC number, interstitium at PND 35–70 testicular serotonin increase 2. no effect on MCs | NA | 1. LC depletion on PND 35; normal number on PND 70 2. LC absent | NA | [46] | |
ETHANOL | ||||||||
RAT | Wistar | ethanol and ethanol extract of Bauhinia forficata | 31 days after 1st treatment | decreased only the number of degranulated MCs | no effect | NA | NA | [68] |
UchB (Wistar) | ethanol 100 days | after treatment | no difference in MC number (testis); increase in total number of degranulated MCs (epidydimis) | NA | NA | NA | [49] | |
Wistar | ethanol 54 days | after treatment | no difference (testis); increase of MC number and degranulation (cauda & initial segment) | ethanol: mature spermatid number, mobile sperm count reduction; abnormal seminiferous tubule morphology | NA | NA | [51] | |
GENETIC ALTERATIONS | ||||||||
MOUSE | WT and transgenic AROM+ | AROM+ alteration | 4-, 9-, and 15- month-old | MC number increase in interstitium and during aging | spermatogenic disruption progression during aging (GC depletion to absence at 15 months) | LC hyperplasia and hypertrophy (4 months), giant multinucleated macrophage number progression; LC adenomas (9- and 15-month-old) | NA | [76] |
Mt-hAMH and C57BL/6 | Mt-hAMH alteration | 5-month-old | abundant MC in the interstitium | lower length of ST, vacuolization of Sertoli cells, loss of GC | LC depletion | infertility after 3 rounds of consecutive pairing | [125] | |
WT (C57BL/6) and RORα-deficient | RORα-deficiency alteration | 10–12-week-old | MC in the interstitium and within the seminiferous tubule near BM | ST diameter and germinal epithelium height decrease (GC apoptosis), basal membrane irregularities, hypospermatogenesis | LC vacuolization number reduction | NA | [78] | |
INFECTION | ||||||||
RAT | Wistar | C. trahomatis inoculation | 3–90 days after infection | MCs in inflammatory lesions of the epididymis 30 days after | germinal epithelium loss, spermatid giant cells after 7–70 days | interstitial fibrosis after 7–70 days | NA | [128] |
DEER MOUSE | Trypanosoma brucei infection | 0–10 weeks after infection | MC number increase in the interstitium | ST diameter decrease (loss of GC), increase with time | LC accumulation, mononuclear cell infiltration, increase with time | NA | [129] | |
CRYPTORCHIDISM | ||||||||
RAT | Wistar | experimental UDT (newborn) ± ketotifen, then peripubertal, pubertal, or adult bilateral orchidectomy | after orchidectomy | experimental UDT increased, and ketotifen decreased MC number in scrotal and abdominal testis | UDT: ST diameters decreased, ST basement membranes thickened, and spermatogenesis decreased—both testes; ketotifen prevented | interstitial fibrosis; ketotifen prevented | NA | [73] |
Sprague-Dawley | PND 15–17 unilateral cryptorchidism | 15 days after treatment | MC number increase in cryptorchid (higher) and scrotal (lower) testis | ST atrophy, diameter reduction, degenerative changes, GC disconnection from BM, BM thickening, destruction in tight junctions between SCs, SCs, and spermatogenic cells, decomposition of cytoplasmic bridges between spermatogenic cells | perivascular and interstitial fibrosis, edema, congestion, hemorrhage | NA | [127] | |
BOAR | domestic | cryptorchidism (unilateral and bilateral) | 9-month-old | abundant MCs in bilateral cryptorchid testes interstitium | NA | unilateral: fibrosis and LC degeneration in abdominal testis bilateral: advanced fibrosis, immature LC and LC degeneration | NA | [87] |
OTHER | ||||||||
RAT | Sprague-Dawley | topical histamine, ritanserin, ketanserin, histamine, and substance 48/80 | 30 min after treatment | MC degranulation after histamine and substance 48/80 (dose-dependant) | NA | NA | NA | [92] |
Wistar | acyclovir i.p. 15 consecutive days (3 doses) | 18 days after last treatment | increase of MC number in the testicular interstitium and peritubular area with higher doses | ST diameter, epithelial height (cell loss), tubular differentiation index, spermiogenesis index, repopulation index (higher dose) decrease | LC atrophy, connective tissue increase | lower pregnancy rate | [50] | |
Wistar | 1. Cl2MDP-lp injection PND 5, 10, 15, 20, 25 2. Cl2MDP ± hCG & hFSH PND 18 for 6 days | 1. PND 10–35 2. PND 27 | 1. MC in interstitium 10 and 15 days after treatment | NA | 1. short-term LC depletion after treatment PND 5–15 and long term LC depletion after treatment on PND 20–25 2. LC depletion, no changes after hCG and hFSH treatment | NA | [71] | |
Wistar | males with no mating experience and colony breeders analyzed at PND 40–170 | PND 40, 60, 90, 120 | serotonin + MC increase PND 40- 90; MC number at peak on PND 90 | NA | NA | NA | [97] | |
Sprague-Dawley | genistein ± DEHP in utero | PND 60, 120, 180 | genistein + DEHP: MC marker increase on PND 120 | genistein + DEHP: disruption in Sertoli cell function, different stage spermatogonia change | DEHP: LC number decrease PND 120 | NA | [56] |
7. Experimental Models Investigating Mast Cells in Mammalian Epididymides
8. Discussion
9. Conclusions
- Histological assessment, including toluidine blue stain, should always be included in studies analyzing testicular and epididymal mast cells, as a standard method that stains all mast cell subtypes, regardless of protein content.
- Depending on the effect and antibody used, a few fixation methods should be optimized at the beginning of the study due to the mast cell subtype specificity.
- When investigating animal models, whole testes should be used, including the tunica albuginea, for in most mammals, mast cells reside right underneath. When found in the interstitium, the seminiferous tubule wall thickness should be commented upon.
- With respect to practicality, domestic boars kept under non-variable conditions are proposed to resemble human testicular mast cell distribution better than rodents.
- No exclusively testis- or epididymis-specific mast cell markers have been found yet, although the characterization of other organ-specific mast cell markers is known.
- 3D in vitro models are promising, although they still need significant development in order to incorporate mast cells and the tunica albuginea, if possible. Further efforts need to be made to develop a suitable human-origin testicular cell line combination.
10. Materials and Methods
10.1. Samples
10.2. Immunohistochemistry
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Himelreich-Perić, M.; Katušić-Bojanac, A.; Hohšteter, M.; Sinčić, N.; Mužić-Radović, V.; Ježek, D. Mast Cells in the Mammalian Testis and Epididymis—Animal Models and Detection Methods. Int. J. Mol. Sci. 2022, 23, 2547. https://doi.org/10.3390/ijms23052547
Himelreich-Perić M, Katušić-Bojanac A, Hohšteter M, Sinčić N, Mužić-Radović V, Ježek D. Mast Cells in the Mammalian Testis and Epididymis—Animal Models and Detection Methods. International Journal of Molecular Sciences. 2022; 23(5):2547. https://doi.org/10.3390/ijms23052547
Chicago/Turabian StyleHimelreich-Perić, Marta, Ana Katušić-Bojanac, Marko Hohšteter, Nino Sinčić, Vedrana Mužić-Radović, and Davor Ježek. 2022. "Mast Cells in the Mammalian Testis and Epididymis—Animal Models and Detection Methods" International Journal of Molecular Sciences 23, no. 5: 2547. https://doi.org/10.3390/ijms23052547