#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Sexual behaviour in a murine model of mucopolysaccharidosis type I (MPS I)


Autoři: Ana Barbosa Mendes aff001;  Cinthia Castro do Nascimento aff001;  Vânia D’Almeida aff001
Působiště autorů: Department of Psychobiology, Universidade Federal de São Paulo, São Paulo, SP, Brazil aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0220429

Souhrn

Mucopolysaccharidosis Type I (MPS I) is a rare genetic lysosomal storage disease caused by a mutation of IDUA gene. IDUA codes for α-L-iduronidase (IDUA), a lysosomal hydrolase that degrades glycosaminoglycans (GAGs): heparan sulphate and dermatan sulphate. GAGs are structural and signalling molecules that have a crucial role in controlling a variety of cell functions and their interaction with the extracellular matrix. Because of GAG’s widespread action in cellular metabolism, MPS I is a progressive and disabling multisystemic disorder. Nowadays, the therapies available allowed patients to reach the adult life and the consequences of the disease in their reproductive system are mostly unknown. We aimed to investigate whether IDUA disruption influences sexual behaviour and sexual steroid production in male and female MPS I mice. We used 3 and 6-month-old male and 3-month-old female Idua+/_ and Idua-/- mice to evaluate typical rodent copulatory behaviours. In males we observed the frequency and latency of mounts, intromissions and ejaculations. In females, we evaluated the lordosis quotient. We also analysed the locomotor capacity of mice in the open field test, since mobility is essential for copulatory behaviour. We also quantified steroidal hormonal levels in plasmatic samples. We detected an increase in the latencies of intromissions in Idua-/- males when compared to Idua+/_. However, the number of intromissions was not statistically different between groups. No parameter of female sexual behaviour was statistically different between control and knockout females. In both sexes, we detected diminished mobility in Idua-/- mice. Plasma hormone levels did not differ between Idua+/_ and Idua-/- mice, both in males and females. Although the motor disability predicted to MPS I animals, we concluded that in the considered time point of MPS I progression studied, mice are able to perform sexual behaviour.

Klíčová slova:

Cognitive impairment – Copulation – Lysosomes – Mice – Progesterone – Steroid hormones – Testosterone – Ejaculation


Zdroje

1. Neufeld EF, Muenzer J. The Mucopolysaccharidoses. In: Scriver CR, Sly WS, Childs B, Beaudet AL, Valle D, Kinzler KW VB, editors. The metabolic & molecular bases of inherited disease. New York: McGraw-Hill;2001. pp. 3421–3452.

2. Clarke LA. The mucopolysaccharidoses: a success of molecular medicine. Expert Rev Mol Med. 2008;1: 1–18.

3. Muenzer J, Wraith JE, Clarke LA. Mucopolysaccharidosis I: Management and treatment guidelines. Pediatrics. 2009;123: 12–29.

4. Kakkis ED. Enzyme-replacement therapy in mucopolysaccharidosis I. N Engl J Med. 2001;344(3): 182–188. doi: 10.1056/NEJM200101183440304 11172140

5. Hendriksz CJ, Moss GM, Wraith JE. Pregnancy in a patient with mucopolysaccharidosis type IH homozygous for the W402X mutation. J Inherit Metab Dis]. 2004;27(5): 685–686.

6. Remérand G, Merlin E, Froissart R, Brugnon F, Kanold J, Janny L, et al. Four successful pregnancies in a patient with mucopolysaccharidosis type I treated by allogeneic bone marrow transplantation. J Inherit Metab Dis. 2009;Suppl 1: S111–S113.

7. Castorina M, Antuzzi D, Richards SM, Cox GF, Xue Y. Successful pregnancy and breastfeeding in a woman with mucopolysaccharidosis type I while receiving laronidase enzyme replacement therapy. Clin Exp Obstet Gynecol. 2015;42(1): 108–113. 25864295

8. Staropoli JF, Haliw L, Biswas S, Garrett L, Hölter SM, Becker L et al. Large-Scale Phenotyping of an Accurate Genetic Mouse Model of JNCL Identifies Novel Early Pathology Outside the Central Nervous System. Plos One. 2012;7(6): e38310. doi: 10.1371/journal.pone.0038310 22701626

9. Butler A, He X., Gordon RE, Wu H, Gatt S, Schuchman EH. Reproductive Pathology and Sperm Physiology in Acid Sphingomyelinase-Deficient Mice. Am J Pathol. 2002;161(3): 1061–1075. doi: 10.1016/S0002-9440(10)64267-8 12213735

10. Fan JUN, Akabane H, Graham SN, Richardson LL, Zhu G. Sperm Defects in Mice Lacking a Functional Niemann–Pick C1 Protein. Mol Reprod Dev. 2006;1291: 1284–1291.

11. Luddi A, Strazza M, Carbone M, Moretti E, Costantino-ceccarini E. Galactosylceramidase deficiency causes sperm abnormalities in the mouse model of globoid cell leukodystrophy. Exp Cell Res. 2005;304: 59–68. doi: 10.1016/j.yexcr.2004.10.034 15707574

12. Xu H, Kongmanas K, Kadunganattil S, Smith CE, Rupar T, Goto-Inoue N, Hermo L, Faull KF, Tanphaichitr N. Arylsulfatase A deficiency causes seminolipid accumulation and a lysosomal storage disorder in Sertoli cells. J Lipid Res. 2011;52: 2187–2197. doi: 10.1194/jlr.M019661 21965315

13. Yildiz Y, Matern H, Thompson B, Allegood JC, Warren RL, Ramirez DM, Hammer RE, Hamra FK, Matern S, Russell DW. Mutation of β -glucosidase 2 causes glycolipid storage disease and impaired male fertility. J Clin Invest. 2006;116(11): 2985–2994. doi: 10.1172/JCI29224 17080196

14. Adamali I, Somani IH, Trasler JM, Hermo L. II. Characterization and Development of the Regional and Cellular-Specific Abnormalities in the Epididymis of Mice with Hexosaminidase A Deficiency. J Androl. 1999 20(6): 803–824. 10591619

15. McGlynn R, Dobrenis K, Walkley SU. Differential subcellular localization of cholesterol, gangliosides, and glycosaminoglycans in murine models of mucopolysaccharide storage disorders. J Comp Neurol. 2004;480(4): 415–426. doi: 10.1002/cne.20355 15558784

16. Walkley SU. Secondary accumulation of gangliosides in lysosomal storage disorders. Semin Cell Dev Biol. 2004;15(4): 433–444. doi: 10.1016/j.semcdb.2004.03.002 15207833

17. Chung S, Ma X, Liu Y, Lee D, Tittiger M, Ponder KP. Effect of neonatal administration of a retroviral vector expressing α-l-iduronidase upon lysosomal storage in brain and other organs in mucopolysaccharidosis I mice. Molecular Genetics and Metabolism. 2007;90(2): 181–192. doi: 10.1016/j.ymgme.2006.08.001 16979922

18. Do Nascimento CC, Aguiar Junior O, D’ Almeida V. Analysis of male reproductive parameters in a murine model of mucopolysaccharidosis type I (MPS I). Int J Clin Exp Pathol. 2014;7(6): 3488–3497. 25031781

19. Do Nascimento CC, Aguiar O, Viana GM, D’Almeida V. Evidence that glycosaminoglycan storage and collagen deposition in the cauda epididymis does not impair sperm viability in the Mucopolysaccharidosis type I mouse model. Reproduction, Fertil. Dev. Forthcoming.

20. Milazzo J, Bironneau A, Vannier J, Liard-zmuda A., Macé B. Precocious initiation of spermatogenesis in a 19-month-old boy with Hurler syndrome. Basic Clin Androl. 2014 24(8): 1–7.

21. Soper BW, Pung AW, Vogler CA, Grubb JH, Sly WS, Barker JE. Enzyme replacement therapy improves reproductive performance in mucopolysaccharidosis type VII mice but does not prevent postnatal losses. Pediatric Research. 1999;45(2): 180–186. doi: 10.1203/00006450-199902000-00004 10022587

22. Baldo G, Mayer FQ, Martinelli B, Dilda A, Meyer F, Ponder KP, et al. Evidence of a progressive motor dysfunction in Mucopolysaccharidosis type I mice. Behav Brain Res. 2012;233(1): 169–175. doi: 10.1016/j.bbr.2012.04.051 22580166

23. Ohmi K, Greenberg DS, Rajavel KS, Ryazantsev S, Li HH, Neufeld EF. Activated microglia in cortex of mouse models of mucopolysaccharidoses I and IIIB. PNAS. 2003;100(4): 1902–1907. doi: 10.1073/pnas.252784899 12576554

24. Kikusui T. Analysis of Male Aggressive and Sexual Behavior in Mice. Methods Mol Biol. 2013;1068: 307–318. doi: 10.1007/978-1-62703-619-1_23 24014372

25. Brock O, Baum MJ, Bakker J. The Development of Female Sexual Behavior Requires Prepubertal Estradiol. Journal of Neuroscience. 2011;31(15): 5574–5578. doi: 10.1523/JNEUROSCI.0209-11.2011 21490197

26. Chinen CC, Faria RR, Frussa-filho R. Characterization of the Rapid-Onset Type of Behavioral Sensitization to Amphetamine in Mice: Role of Drug–Environment Conditioning, Neuropsychopharmacology. 2006;31: 151–159. doi: 10.1038/sj.npp.1300789 15956986

27. Sampaio LO, Markus RP, Nader HB. The effect of sexual hormones on the sulfated glycosaminoglycan pattern of male genital accessory organs. Arch Biochem Biophys. 1985;240(1): 470–477. doi: 10.1016/0003-9861(85)90052-9 4015112

28. Grunert G, Fernández S, Tchernitchin AN. Methods for the evaluation of responses to estrogen in individual cell types or regions of the uterus. Hormone Research. 1984;19(4): 253–262. doi: 10.1159/000179895 6204915

29. Sato E. Intraovarian control of selective follicular growth and induction of oocyte maturation in mammals. Proc Jpn Acad Ser B Phys Biol Sci. 2015;91(3): 76–91. doi: 10.2183/pjab.91.76 25765010

30. Hull EM, Wood RI, McKenna KE. Neurobiology of male sexual behavior. In: Neill JD. (Ed.), Physiology of Reproduction. New York: Elsevier;2006. pp. 1729–1824.

31. Wood RI, Newman SW. Integration of chemosensory and hormonal cues is essential for mating in the male Syrian hamster. J. Neurosci. 1995;15: 7261–7269. doi: 10.1523/JNEUROSCI.15-11-07261.1995 7472480

32. Lamprea MR, Cardenas FP, Setem J, Morato S. Thigmotactic responses in an open-field. Braz J Med Biol Res. 2008;41(2): 135–140. doi: 10.1590/s0100-879x2008000200010 18297193

33. Xie C, Richardson JA, Turley SD, Dietschy JM. Cholesterol substrate pools and steroid hormone levels are normal in the face of mutational inactivation of NPC1 protein. J Lipid Res. 2006;7(5): 953–963.

34. Durdiakova J, Ostatnikova D, Celec P. Testosterone and its metabolites modulators of brain functions. Acta Neurobiologiae Experimentalis (Wars). 2011;71(4): 434–454.

35. Arteaga-Silva M, Rodríguez-Dorantes M, Baig S, Morales-Montor J. Effects of castration and hormone replacement on male sexual behavior and pattern of expression in the brain of sex-steroid receptors in BALB/c AnN mice. Comp Biochem Physiol A Mol Integr Physiol. 2007;147(3): 607–615. doi: 10.1016/j.cbpa.2006.11.013 17292648

36. Hull EM, Domingues JM. Sexual behavior in male rodents. Horm behav. 2007;51(1): 45–55.

37. Matsumoto T, Honda S, Harada N. Alteration in sex-specific behaviors in male mice lacking the aromatase gene. Neuroendocrinology. 2003;77(6): 416–424. doi: 10.1159/000071313 12845227

38. Estep DQ, Lanier DL, Dewsbury DA. Copulatory behavior and nest building behavior of wild house mice (Mus musculus). Anim Learn Behav. 1975;3(4): 329–336. doi: 10.3758/bf03213455 1228022

39. Baldo G, Mayer FQ, Martinelli BZ, de Carvalho TG, Meyer FS, de Oliveira PG et al. Enzyme replacement therapy started at birth improves outcome in difficult-to-treat oorgans organs in mucopolysaccharidosis I mice. Mol Genet Metab. 2013;109(1): 33–40. doi: 10.1016/j.ymgme.2013.03.005 23562162


Článek vyšel v časopise

PLOS One


2019 Číslo 12
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#