Trade-offs between male fertility reduction and selected growth factors or the klotho response in a lipopolysaccharide-dependent mouse model |
Solek, Przemyslaw
(Department of Biotechnology, Institute of Biology and Biotechnology, Collegium Scientarium Naturalium, University of Rzeszow)
Mytych, Jennifer (Department of Biotechnology, Institute of Biology and Biotechnology, Collegium Scientarium Naturalium, University of Rzeszow) Sujkowska, Ewelina (Department of Biotechnology, Institute of Biology and Biotechnology, Collegium Scientarium Naturalium, University of Rzeszow) Grzegorczyk, Magdalena (Department of Biotechnology, Institute of Biology and Biotechnology, Collegium Scientarium Naturalium, University of Rzeszow) Jasiewicz, Patrycja (Department of Biotechnology, Institute of Biology and Biotechnology, Collegium Scientarium Naturalium, University of Rzeszow) Sowa‑Kucma, Magdalena (Department of Human Physiology, Institute of Medical Sciences, Medical College of Rzeszow University) Stachowicz, Katarzyna (Department of Neurobiology, Maj Institute of Pharmacology Polish Academy of Sciences) Koziorowski, Marek (Department of Biotechnology, Institute of Biology and Biotechnology, Collegium Scientarium Naturalium, University of Rzeszow) Tabecka‑Lonczynska, Anna (Department of Biotechnology, Institute of Biology and Biotechnology, Collegium Scientarium Naturalium, University of Rzeszow) |
1 | Stachowicz K (2019) Behavioral consequences of co-administration of MTEP and the COX-2 inhibitor NS398 in mice. Part 1. Behav Brain Res 370:111961. https://doi.org/10.1016/j.bbr.2019.111961 DOI |
2 | Evans-Hoeker EA, Eisenberg E, Diamond MP, Legro RS, Alvero R, Coutifaris C, Casson PR, Christman GM, Hansen KR, Zhang H, Santoro N, Steiner AZ (2018) Major depression, antidepressant use, and male and female fertility. Fertil Steril 109:879-887. https://doi.org/10.1016/j.fertnstert.2018.01.029 DOI |
3 | Yan YC, Sun YP, Zhang ML (1998) Testis epidermal growth factor and spermatogenesis. Arch Androl 40:133-146. https://doi.org//10.3109//01485019808987936 DOI |
4 | Tse MC, Vong QP, Cheng CH, Chan KM (2002) PCR-cloning and gene expression studies in common carp (Cyprinus carpio) insulin-like growth factor-II. Biochim Biophys Acta 1575:63-74. https://doi.org/10.1016//s0167-4781(02)00244-0 DOI |
5 | Lim K, Groen A, Molostvov G, Lu T, Lilley KS, Snead D, James S, Wilkinson IB, Ting S, Hsiao LL, Hiemstra TF, Zehnder D (2015) alpha-Klotho Expression in Human Tissues. J Clin Endocrinol Metab 100:E1308-E1318. https://doi.org/10.1210/jc.2015-1800 DOI |
6 | Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T, Ohyama Y, Kurabayashi M, Kaname T, Kume E, Iwasaki H, Iida A, Shiraki-Iida T, Nishikawa S, Nagai R, Nabeshima YI (1997) Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390:45-51. https://doi.org/10.1038/36285 DOI |
7 | Marciniak M, Chruscicka B, Lech T, Burnat G, Pilc A (2016) Expression of group III metabotropic glutamate receptors in the reproductive system of male mice. Reprod Fertil Dev 28:369-374. https://doi.org/10.1071//RD14132 DOI |
8 | Romanelli F, Valenca M, Conte D, Isidori A, Negro-Vilar A (1995) Arachidonic acid and its metabolites effects on testosterone production by rat Leydig cells. J Endocrinol Invest 18:186-193. https://doi.org/10.1007//BF03347801 DOI |
9 | Wang Y, Sun Z (2009) Current understanding of klotho. Ageing Res Rev 8:43-51. https://doi.org/10.1016/j. arr. 2008. 10. 002 DOI |
10 | Li SA, Watanabe M, Yamada H, Nagai A, Kinuta M, Takei K (2004) Immunohistochemical localization of Klotho protein in brain, kidney, and reproductive organs of mice. Cell Struct Funct 29:91-99. https://doi.org/10.1247//csf.29.91 DOI |
11 | Painsipp E, Kofer MJ, Sinner F, Holzer P (2011) Prolonged depression-like behavior caused by immune challenge: influence of mouse strain and social environment. PLoS ONE 6:e20719. https://doi.org/10.1371//journal.pone.0020719 DOI |
12 | Martin SA, Dantzer R, Kelley KW, Woods JA (2014) Voluntary wheel running does not affect lipopolysaccharide-induced depressive-like behavior in young adult and aged mice. Neuro-ImmunoModulation 21:52-63. https://doi.org/10.1159//000356144 DOI |
13 | Korpelainen EI, Karkkainen MJ, Tenhunen A, Lakso M, Rauvala H, Vierula M, Parvinen M, Alitalo K (1998) Overexpression of VEGF in testis and epididymis causes infertility in transgenic mice: evidence for nonendothelial targets for VEGF. J Cell Biol 143:1705-1712. https://doi.org/10.1083//jcb.143.6.1705 DOI |
14 | Nakamura M, Kobayashi T, Chang XT, Nagahama Y (1998) Gonadal sex differentiation in teleost fish. J Exp Zool 281:362-372. https://doi.org/10.1002//(SICI)1097-010X(19980 801)281:5<362::AID-JEZ3>3.0.CO;2-M DOI |
15 | Stachowicz K, Bobula B, Tokarski K (2020) NS398, a cyclooxygenase-2 inhibitor, reverses memory performance disrupted by imipramine in C57Bl/6J mice. Brain Res 1734:146741. https://doi.org//10.1016/j.brainres.2020.146741 DOI |
16 | Maranesi M, Zerani M, Leonardi L, Pistilli A, Arruda-Alencar J, Stabile AM, Rende M, Castellini C, Petrucci L, Parillo F, Moura A, Boiti C (2015) Gene expression and localization of NGF and its cognate receptors NTRK1 and NGFR in the sex organs of male rabbits. Reprod Domest Anim 50:918-925. https://doi.org/10.1111//rda.12609 DOI |
17 | Wang SM, Han C, Bahk WM, Lee SJ, Patkar AA, Masand PS, Pae CU (2018) Addressing the side effects of contemporary antidepressant drugs: a comprehensive review. Chonnam Med J 54:101-112. https://doi.org/10.4068//cmj.2018.54.2.101 DOI |
18 | Casilla-Lennon MM, Meltzer-Brody S, Steiner AZ (2016) The effect of antidepressants on fertility. Am J Obserics Gynecol 215:314.e311-315. https://doi.org/10.1016/j.fertnstert.2014.12.023 DOI |
19 | Tanrikut C, Schlegel PN (2007) Antidepressant-associated changes in semen parameters. Urology 69:185-187. https://doi.org//10.1016/j.urology.2006.10.034 DOI |
20 | Schmidt JA, de Avila JM, McLean DJ (2007) Analysis of gene expression in bovine testis tissue prior to ectopic testis tissue xenografting and during the grafting period. Biol Reprod 76:1071-1080. https://doi.org/10.1095//biolreprod.106.058222 DOI |
21 | Reinecke M, Collet C (1998) The phylogeny of the insulin-like growth factors. Int Rev Cytol 183:1-94. https://doi.org/10.1016/S0074-7696(08)60142-4 DOI |
22 | Lupu F, Terwilliger JD, Lee K, Segre GV, Efstratiadis A (2001) Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev Biol 229:141-162. https://doi.org/10.1006//dbio.2000.9975 DOI |
23 | Pomierny-Chamiolo L, Poleszak E, Pilc A, Nowak G (2010) NMDA but not AMPA glutamatergic receptors are involved in the antidepressant-like activity of MTEP during the forced swim test in mice. Poland Pharmacol Rep 62:1186-1190. https://doi.org//10.1016//S1734-1140(10)70381-9 DOI |
24 | Palucha-Moniewiera A, Wieronska JM, Branski P, Burnat G, Chruscicka B, Pilc A (2013) Is the mGlu5 receptor a possible target for new antidepressant drugs? Pharmacol Rep 65:1506-1511. https://doi.org/10.1016//s1734-1140(13)71511-1 DOI |
25 | Tabecka-Lonczynska A, Mytych J, Solek P, Kowalewski MP, Koziorowski M (2019) Seasonal expression of insulin-like growth factor 1 (IGF-1), its receptor IGF-1R and klotho in testis and epididymis of the European bison (Bison bonasus, Linnaeus 1758). Theriogenology 126:199-205. https://doi.org/10.1016/j.theriogenology.2018.12.016 DOI |
26 | Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219:983-985. https://doi.org/10.1126//science.6823562 DOI |
27 | Perrot V, Moiseeva EB, Gozes Y, Chan SJ, Funkenstein B (2000) Insulin-like growth factor receptors and their ligands in gonads of a hermaphroditic species, the gilthead seabream (Sparus aurata): expression and cellular localization. Biol Reprod 63:229-241. https://doi.org/10.1095//biolreprod63.1.229 DOI |
28 | Lui WY, Lee WM, Cheng CY (2003) TGF-betas: their role in testicular function and Sertoli cell tight junction dynamics. Int J Androl 26:147-160. https://doi.org/10.1046/j.1365-2605.2003.00410.x DOI |
29 | Wang X, Liang Y, Wang J, Wang M (2013) Effect of NS-398, a cyclooxygenase-2 selective inhibitor, on the cytotoxicity of cytotoxic T lymphocytes to ovarian carcinoma cells. Tumour Biol 34:1517-1522. https://doi.org/10.1007//s13277-013-0677-3 DOI |
30 | Muller N, Schwarz MJ (2008) COX-2 inhibition in schizophrenia and major depression. Curr Pharm Des 14:1452-1465. https://doi.org//10.2174//138161208784480243 DOI |
31 | Palaniyappan L, Insole L, Ferrier N (2009) Combining antidepressants: a review of evidence. Adv Psychiatr Treat 15:90-99. https://doi.org//10.1192//apt.bp.107.004820 DOI |
32 | Wang X, Walsh LP, Reinhart AJ, Stocco DM (2000) The role of arachidonic acid in steroidogenesis and steroidogenic acute regulatory (StAR) gene and protein expression. J Biol Chem 275:20204-20209. https://doi.org/10.1074//jbc.M003113200 DOI |
33 | Imai M, Ishikawa K, Matsukawa N, Kida I, Ohta J, Ikushima M, Chihara Y, Rui X, Rakugi H, Ogihara T (2004) Klotho protein activates the PKC pathway in the kidney and testis and suppresses 25-hydroxyvitamin D3 1alpha-hydroxylase gene expression. Endocrine 25:229-234. https://doi.org/10.1385//ENDO:25:3:229 DOI |
34 | Hendrick V, Gitlin M, Althshuler L, Korenman S (2000) Antidepressant medications, mood and male fertility. Psychoneuroendocrinology 25:37-51. https://doi.org/10.1016//S0306-4530(99)00038-4 DOI |
35 | Nalbandian A, Dettin L, Dym M, Ravindranath N (2003) Expression of vascular endothelial growth factor receptors during male germ cell differentiation in the mouse. Biol Reprod 69:985-994. https://doi.org/10.1095//biolreprod.102.013581 DOI |
36 | Hendrick V, Gitlin M, Altshuler L, Korenman S (2000) Antidepressant medications, mood and male fertility. Psychoneuroendocrinology 25:37-51. https://doi.org/10.1016//s0306-4530(99)00038-4 DOI |
37 | Agrawal R, Jacobs H, Payne N, Conway G (2002) Concentration of vascular endothelial growth factor released by cultured human luteinized granulosa cells is higher in women with polycystic ovaries than in women with normal ovaries. Fertil Steril 78:1164-1169. https://doi.org/10.1016//S0015-0282(02) 04242-5 DOI |
38 | Griffeth RJ, Bianda V, Nef S (2014) The emerging role of insulinlike growth factors in testis development and function. Basic Clin Androl 24:12. https://doi.org/10.1186//2051-4190-24-12 DOI |
39 | Moraga PF, Llanos MN, Ronco AM (1997) Arachidonic acid release from rat Leydig cells depends on the presence of luteinizing hormone/human chorionic gonadotrophin receptors. J Endocrinol 154:201-209. https://doi.org/10.1677//joe.0.1540201 DOI |
40 | Wang X, Dyson MT, Jo Y, Stocco DM (2003) Inhibition of cyclooxygenase-2 activity enhances steroidogenesis and steroidogenic acute regulatory gene expression in MA-10 mouse Leydig cells. Endocrinology 144:3368-3375. https://doi.org/10.1210//en.2002-0081 DOI |
41 | Marks DM, Shah MJ, Patkar AA, Masand PS, Park GY, Pae CU (2009) Serotonin-norepinephrine reuptake inhibitors for pain control: premise and promise. Curr Neuropharmacol 7:331-336. https://doi.org/10.2174//157015909790031201 DOI |
42 | Radhakrishnan B, Oke BO, Papadopoulos V, DiAugustine RP, Suarez-Quian CA (1992) Characterization of epidermal growth factor in mouse testis. Endocrinology 131:3091-3099. https://doi.org//10.1210//endo.131.6.1446643 DOI |
43 | Brown LF, Yeo KT, Berse B, Morgentaler A, Dvorak HF, Rosen S (1995) Vascular permeability factor (vascular endothelial growth factor) is strongly expressed in the normal male genital tract and is present in substantial quantities in semen. J Urol 154:576-579. https://doi.org/10.1016//S0022-5347(01)67114-3 DOI |
44 | Olofsson B, Korpelainen E, Pepper MS, Mandriota SJ, Aase K, Kumar V, Gunji Y, Jeltsch MM, Shibuya M, Alitalo K, Eriksson U (1998) Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc Natl Acad Sci USA 95:11709-11714. https://doi.org/10.1073//pnas.95.20.11709 DOI |
45 | Luo H, Kimura K, Aoki M, Hirako M (2002) Vascular endothelial growth factor (VEGF) promotes the early development of bovine embryo in the presence of cumulus cells. J Vet Med Sci 64:967-971. https://doi.org/10.1292//jvms.64.967 DOI |
46 | Obermair A, Obruca A, Pohl M, Kaider A, Vales A, Leodolter S, Wojta J, Feichtinger W (1999) Vascular endothelial growth factor and its receptors in male fertility. Fertil Steril 72:269-275. https://doi.org//10.1016//s0015-0282(99)00234-4 DOI |
47 | Vinas J, Piferrer F (2008) Stage-specific gene expression during fish spermatogenesis as determined by laser-capture microdissection and quantitative-PCR in sea bass (Dicentrarchus labrax) gonads. Biol Reprod 79:738-747. https://doi.org/10.1095//biolreprod.108.069708 DOI |
48 | Greene MW, Chen TT (1997) Temporal expression pattern of insulin-like growth factor mRNA during embryonic development in a teleost, rainbow trout (Onchorynchus mykiss). Mol Mar Biol Biotechnol 6:144-151 (PMID: 9200841) |
49 | Gonzalez CR, Matzkin ME, Frungieri MB, Terradas C, Ponzio R, Puigdomenech E, Levalle O, Calandra RS, Gonzalez-Calvar SI (2010) Expression of the TGF-beta1 system in human testicular pathologies. Reprod Biol Endocrinol 8:148. https://doi.org//10.1186//1477-7827-8-148 DOI |
50 | Haigh JJ (2008) Role of VEGF in organogenesis. Organogenesis 4:247-256. https://doi.org/10.4161//org.4.4.7415 DOI |
51 | Kassab M, Abd-Elmaksoud A, Ali MA (2007) Localization of the epidermal growth factor (EGF) and epidermal growth factor receptor (EGFR) in the bovine testis. J Mol Histol 38:207-214. https://doi.org/10.1007//s10735-007-9089-2 DOI |
52 | He J, Dong C, You R, Zhu Z, Lv L, Smith GW (2009) Localization of epidermal growth factor (EGF) and its receptor (EGFR) during postnatal testis development in the alpaca (Lama pacos). Anim Reprod Sci 116:155-161. https://doi.org/10.1016/j.anireprosci.2009.01.002 DOI |
53 | Pan Y, Cui Y, Yu S, Zhang Q, Fan J, Abdul Rasheed B, Yang K (2014) The expression of epidermal growth factor (EGF) and its receptor (EGFR) during post-natal testes development in the yak. Reprod Domest Anim 49:970-976. https://doi.org/10.1111//rda.12416 DOI |
54 | Wong RW, Kwan RW, Mak PH, Mak KK, Sham MH, Chan SY (2000) Overexpression of epidermal growth factor induced hypospermatogenesis in transgenic mice. J Biol Chem 275:18297-18301. https://doi.org/10.1074//jbc.M001965200 DOI |
55 | Leone F, Lofaro D, Gigliotti P, Perri A, Vizza D, Toteda G, Lupinacci S, Armentano F, Papalia T, Bonofiglio R (2014) Soluble Klotho levels in adult renal transplant recipients are modulated by recombinant human erythropoietin. J Nephrol 27:577-585. https://doi.org//10.1007//s40620-014-0089-5 DOI |
56 | Sawada J, Itakura A, Tanaka A, Furusaka T, Matsuda H (2000) Nerve growth factor functions as a chemoattractant for mast cells through both mitogen-activated protein kinase and phosphatidylinositol 3-kinase signaling pathways. Blood 95:2052-2058. https://doi.org/10.1182//blood.V95.6.2052 DOI |
57 | Ayson FG, de Jesus EG, Moriyama S, Hyodo S, Funkenstein B, Gertler A, Kawauchi H (2002) Differential expression of insulin-like growth factor I and II mRNAs during embryogenesis and early larval development in rabbitfish, Siganus guttatus. Gen Comp Endocrinol 126:165-174. https://doi.org/10.1006/gcen.2002.7788 DOI |
58 | Shiraishi K, Matsuyama H (2012) Local expression of epidermal growth factor-like growth factors in human testis and its role in spermatogenesis. J Androl 33:66-73. https://doi.org/10.2164//jandrol.110.011981 DOI |
59 | Koh N, Fujimori T, Nishiguchi S, Tamori A, Shiomi S, Nakatani T, Sugimura K, Kishimoto T, Kinoshita S, Kuroki T, Nabeshima Y (2001) Severely reduced production of klotho in human chronic renal failure kidney. Biochem Biophys Res Commun 280:1015-1020. https://doi.org/10.1006//bbrc.2000.4226 DOI |
60 | Chang WY, Kulp SK, Sugimoto Y, Canatan H, Shidaifat F, Inpanbutr N, Lin YC (1996) Detection of keratinocyte growth factor (KGF) messenger ribonucleic acid and immunolocalization of KGF in the canine testis. Endocrine 5:247-255. https://doi.org/10.1007//BF02739057 DOI |
61 | Skaper SD (2017) Nerve growth factor: a neuroimmune crosstalk mediator for all seasons. Immunology 151:1-15. https://doi.org/10.1111//imm.12717 DOI |
62 | Cupp AS, Kim GH, Skinner MK (2000) Expression and action of neurotropin-3 and nerve growth factor in embryonic and early postnatal rat testis development. Biol Reprod 63:1617-1628. https://doi.org/10.1095//biolreprod63.6.1617 DOI |
63 | Wang H, Dong Y, Chen W, Hei J, Dong C (2011) Expression and localization of nerve growth factor (NGF) in the testis of alpaca (llama pacos). Folia Histochem Cytobiol 49:55-61. https://doi.org//10.5603//FHC.2011.0009 DOI |
![]() |