Low 17beta-estradiol levels in Cnr1 knock-out mice affect spermatid chromatin remodeling by interfering with chromatin reorganization

Biology of Reproduction

Volumn 88, Issue 6, 2013, Pages

  Cacciola, Giovanna ^a   Chioccarelli, Teresa ^a   Altucci, Lucia ^a   Ledent, Catherine ^b   Mason, J Ian ^c   Fasano, Silvia ^a   Pierantoni, Riccardo ^a   Cobellis, Gilda ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cannabinoid receptor; Chromatin remodeling; DNA damage; Endocannabinoids; Epigenetic; Estrogens; FSH; GnRH; Gonadotropins; Hypothalamus; Spermatids; Spermatogenesis; Spermiogenesis; Testis

Indexed keywords

CANNABINOID 1 RECEPTOR; ESTRADIOL; FOLLITROPIN; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CNR1 GENE; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; ESTROGEN RELEASE; ESTROGEN SYNTHESIS; FOLLITROPIN RELEASE; GENE; KNOCKOUT MOUSE; MALE; MOUSE; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; SPERMATID;

CANNABINOID RECEPTOR; CHROMATIN REMODELING; DNA DAMAGE; ENDOCANNABINOIDS; EPIGENETIC; ESTROGENS; FSH; GNRH; GONADOTROPINS; HYPOTHALAMUS; SPERMATIDS; SPERMATOGENESIS; SPERMIOGENESIS; TESTIS;

ANIMALS; AROMATASE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; ESTRADIOL; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; GONADOTROPIN-RELEASING HORMONE; MALE; MICE; MICE, KNOCKOUT; PITUITARY GLAND; RECEPTOR, CANNABINOID, CB1; RECEPTORS, FSH; RECEPTORS, LHRH; SPERMATIDS; SPERMATOGENESIS; TESTIS;

EID: 84881582187     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.105726     Document Type: Article

References (73)

1. Miller D, Brinkworth M, Iles D. Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 2010; 139:287-301.
2. Irvine DS, Twigg JP, Gordon EL, Fulton N, Milne PA, Aitken RJ. DNA integrity in human spermatozoa: relationships with semen quality. J Androl 2000; 21:33-44.
3. Szczygiel MA, Ward WS. Combination of dithiothreitol and detergent treatment of spermatozoa causes paternal chromosomal damage. Biol Reprod 2002; 67:1532-1537.
4. Lewis SE, Agbaje IM. Using the alkaline comet assay in prognostic tests for male infertility and assisted reproductive technology outcomes. Mutagenesis 2008; 23:163-170.
5. Churikov D, Siino J, Svetlova M, Zhang K, Gineitis A, Morton Bradbury E, Zalensky A. Novel human testis-specific histone H2B encoded by the interrupted gene on the X chromosome. Genomics 2004; 84:745-56.
6. Battista N, Meccariello R, Cobellis G, Fasano S, Di Tommaso M, Pirazzi V, Konje JC, Pierantoni R, Maccarrone M. The role of endocannabinoids in gonadal function and fertility along the evolutionary axis. Mol Cell Endocrinol 2012; 355:1-14.
7. Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, Khochbin S. Establishment of male-specific epigenetic information. Gene 2005; 345: 139-153.
8. Gaucher J, Reynoird N, Montellier E, Boussouar F, Rousseaux S, Khochbin S. From meiosis to postmeiotic events: the secrets of histone disappearance. FEBS J 2010; 277:599-604.
9. Fuentes-Mascorro G, Serrano H, Rosado A. Sperm chromatin. Arch Androl 2000; 45:215-225.
10. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, Roloff TC, Beisel C, Schübeler D, Stadler MB, Peters AH. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 2010; 17:679-687.
11. Acone G, Trabucco E, Colacurci N, Cobellis L, Mackie K, Meccariello R, Cacciola G, Chioccarelli T, Fasano S, Pierantoni R, Cobellis G. Low type I cannabinoid receptor levels characterize placental villous in labouring delivery. Placenta 2009; 30:203-205.
12. Trabucco E, Acone G, Marenna A, Pierantoni R, Cacciola G, Chioccarelli T, Mackie K, Fasano S, Colacurci N, Meccariello R, Cobellis G, Cobellis L. Endocannabinoid system in first trimester placenta: low FAAH and high CB1 expression characterize spontaneous miscarriage. Placenta 2009; 30:516-522.
13. Pierantoni R, Cobellis G, Meccariello R, Cacciola G, Chianese R, Chioccarelli T, Fasano S. CB1 activity in male reproduction: mammalian and nonmammalian animal models. Vitam Horm 2009; 81:367-387.
14. Cacciola G, Chianese R, Chioccarelli T, Ciaramella V, Fasano S, Pierantoni R, Meccariello R, Cobellis G. Cannabinoids and Reproduction: A Lasting and Intriguing History. Pharmaceuticals 2010; 3:3275-3323.
15. Chioccarelli T, Cacciola G, Altucci L, Lewis SE, Simon L, Ricci G, Ledent C, Meccariello R, Fasano S, Pierantoni R, Cobellis G. Cannabinoid receptor 1 influences chromatin remodeling in mouse spermatids by affecting content of transition protein 2 mRNA and histone displacement. Endocrinology 2010; 151:5017-5029.
16. Meccariello R, Chianese R, Cacciola G, Cobellis G, Pierantoni R, Fasano S. Type-1 cannabinoid receptor expression in the frog, Rana esculenta, tissues: a possible involvement in the regulation of testicular activity. Mol Reprod Dev 2006; 73:551-558.
17. Meccariello R, Franzoni MF, Chianese R, Cottone E, Scarpa D, Donna D, Cobellis G, Guastalla A, Pierantoni R, Fasano S. Interplay between the endocannabinoid system and GnRH-I in the forebrain of the anuran amphibian Rana esculenta. Endocrinology 2008; 149:2149-2158.
18. Chianese R, Ciaramella V, Fasano S, Pierantoni R, Meccariello R. Anandamide modulates the expression of GnRH-II and GnRHRs in frog, Rana esculenta, diencephalon. Gen Comp Endocrinol 2011; 173:389-395.
19. Pertwee RG, Joe-Adigwe G, Hawksworth GM. Further evidence for the presence of cannabinoid CB1 receptors in mouse vas deferens. Eur J Pharmacol 1996; 296:169-172.
20. Cobellis G, Cacciola G, Scarpa D, Meccariello R, Chianese R, Franzoni MF, Mackie K, Pierantoni R, Fasano S. Endocannabinoid system in frog and rodent testis: type-1 cannabinoid receptor and fatty acid amide hydrolase activity in male germ cells. Biol Reprod 2006; 75:82-89.
21. Ricci G, Cacciola G, Altucci L, Meccariello R, Pierantoni R, Fasano S, Cobellis G. Endocannabinoid control of sperm motility: the role of epididymus. Gen Comp Endocrinol 2007; 153:320-322.
22. Cacciola G, Chioccarelli T, Ricci G, Meccariello R, Fasano S, Pierantoni R, Cobellis G. The endocannabinoid system in vertebrate male reproduction: a comparative overview. Mol Cell Endocrinol 2008; 286: S24-30.
23. Grimaldi P, Orlando P, Di Siena S, Lolicato F, Petrosino S, Bisogno T, Geremia R, De Petrocellis L, Di Marzo V. The endocannabinoid system and pivotal role of the CB2 receptor in mouse spermatogenesis. Proc Natl Acad Sci U S A 2009; 106:11131-11136.
24. Fasano S, Meccariello R, Cobellis G, Chianese R, Cacciola G, Chioccarelli T, Pierantoni R. The endocannabinoid system: an ancient signaling involved in the control of male fertility. Ann N Y Acad Sci 2009; 1163: 112-124.
25. Pierantoni R, Cobellis G, Meccariello R, Cacciola G, Chianese R, Chioccarelli T, Fasano S. Testicular gonadotropin-releasing hormone activity, progression of spermatogenesis, and sperm transport in vertebrates. Ann N Y Acad Sci 2009; 1163:279-291.
26. Cobellis G, Ricci G, Cacciola G, Orlando P, Petrosino S, Cascio MG, Bisogno T, De Petrocellis L, Chioccarelli T, Altucci L, Fasano S, Meccariello R, et al. A gradient of 2-arachidonoylglycerol regulates mouse epididymal sperm cell start-up. Biol Reprod 2010; 82:451-458.
27. Scorticati C, Fernández-Solari J, De Laurentiis A, Mohn C, Prestifilippo JP, Lasaga M, Seilicovich A, Billi S, Franchi A, McCann SM, Rettori V. The inhibitory effect of anandamide on luteinizing hormone-releasing hormone secretion is reversed by estrogen. Proc Natl Acad Sci U S A 2004; 101:11891-11896.
28. Maccarrone M, Cecconi S, Rossi G, Battista N, Pauselli R, Finazzi-Agro A. Anandamide activity and degradation are regulated by early postnatal aging and follicle-stimulating hormone in mouse Sertoli cells. Endocrinology 2003; 144:20-28.
29. Cacciola G, Chioccarelli T, Mackie K, Meccariello R, Ledent C, Fasano S, Pierantoni R, Cobellis G. Expression of type-1 cannabinoid receptor during rat postnatal testicular development: possible involvement in adult Leydig cell differentiation. Biol Reprod 2008; 79:758-765.
30. Wenger T, Ledent C, Csernus V, Gerendai I. The central cannabinoid receptor inactivation suppresses endocrine reproductive functions. Biochem Biophys Res Commun 2001; 284:363-368.
31. Chianese R, Chioccarelli T, Cacciola G, Ciaramella V, Fasano S, Pierantoni R, Meccariello R, Cobellis G. The contribution of lower vertebrate animal models in human reproduction research. Gen Comp Endocrinology 2011; 171:17-27.
32. Carrell DT, Emery BR, Hammoud S. Altered protamine expression and diminished spermatogenesis: what is the link. Hum Reprod Update 2007; 13:313-327.
33. Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, Bohme GA, Imperato A, Pedrazzini T, Roques BP, Vassart G, Fratta W, et al. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 1999; 283:401-404.
34. Cobellis G, Pierantoni R, Minucci S, Pernas-Alonso R, Meccariello R. Fasano S. c-fos activity in Rana esculenta testis: seasonal and estradiolinduced changes.Endocrinology 1999; 140:3238-3244.
35. Cobellis G, Meccariello R, Fienga G, Pierantoni R, Fasano S. Cytoplasmic and nuclear Fos protein forms regulate resumption of spermatogenesis in the frog, Rana esculenta. Endocrinology 2002; 143:163-170.
36. Pierantoni R, Cobellis G, Meccariello R, Fasano S. Evolutionary aspects of cellular communication in the vertebrate hypothalamo-hypophysiogonadal axis. Int Rev Cytol 2002; 218:69-141.
37. Cobellis G, Meccariello R, Pierantoni R, Fasano S. Intratesticular signals for progression of germ cell stages in vertebrates. Gen Comp Endocrinol 2003; 134:220-228.
38. Cobellis G, Lombardi M, Scarpa D, Izzo G, Fienga G, Meccariello R, Pierantoni R, Fasano S. Fra-1 activity in the frog, Rana esculenta, testis. Ann N Y Acad Sci 2005; 1040:264-268.
39. Cobellis G, Lombardi M, Scarpa D, Izzo G, Fienga G, Meccariello R, Pierantoni R, Fasano S. Fra1 activity in the frog, Rana esculenta, testis: a new potential role in sperm transport. Biol Reprod 2005; 72:1101-1108.
40. Cobellis G, Cacciola G, Chioccarelli T, Izzo G, Meccariello R, Pierantoni R, Fasano S. Estrogen regulation of the male reproductive tract in the frog, Rana esculenta: a role in Fra-1 activation in peritubular myoid cells and in sperm release. Gen Comp Endocrinol 2008; 155:838-846.
41. Ruwanpura SM, McLachlan RI, Meachem SJ. Hormonal regulation of male germ cell development. J Endocrinol 2010; 205:117-131.
42. Gill-Sharma MK, Choudhuri J, D'Souza S. Sperm chromatin protamination: an endocrine perspective. Protein Pept Lett 2011; 18:786-801.
43. Staub C, Rauch M, Ferrière F, Trépos M, Dorval-Coiffec I, Saunders PT, Cobellis G, Flouriot G, Saligaut C, Jégou B. Expression of estrogen receptor ESR1 and its 46-kDa variant in the gubernaculum testis. Biol Reprod 2005; 73:703-712.
44. Jones R. Sperm survival versus degradation in the mammalian epididymis: an hypothesis. Biol Reprod 2004; 71:1405-1411.
45. Carreau S, Bouraima-Lelong H, Delalande C. Estrogen, a female hormone involved in spermatogenesis. Adv Med Sci 2012; 57:31-36.
46. Shetty G, Krishnamurthy H, Krishnamurthy HN, Bhatnagar S, Moudgal RN. Effect of estrogen deprivation on the reproductive physiology of male and female primates. J Steroid Biochem Mol Biol 1997; 61:157-166.
47. Shetty G, Krishnamurthy H, Krishnamurthy HN, Bhatnagar AS, Moudgal NR. Effect of long-term treatment with aromatase inhibitor on testicular function of adult male bonnet monkeys (M. radiata). Steroids 1998; 63: 414-420.
48. Richthoff J, Spano M, Giwercman YL, Frohm B, Jepson K, Malm J, Elzanaty S, Stridsberg M, Giwercman A. The impact of testicular and accessory sex gland function on sperm chromatin integrity as assessed by the sperm chromatin structure assay (SCSA). Hum Reprod 2002; 17: 3162-3169.
49. Meeker JD, Singh NP, Hauser R. Serum concentrations of estradiol and free T4 are inversely correlated with sperm DNA damage in men from an infertility clinic. J Androl 2008; 29:379-388.
50. Doody KM, Carr BR, Rainey WE, Byrd W, Murry BA, Strickler RC, Thomas JL, Mason JI. 3b-Hydroxysteroid dehydrogenase/isomerase in the fetal zone and neocortex of the human fetal adrenal gland. Endocrinology 1990; 126:2487-2492.
51. Crispi S, Calogero RA, Santini M, Mellone P, Vincenzi B, Citro G, Vicidomini G, Fasano S, Meccariello R, Cobellis G, Menegozzo S, Pierantoni R, et al. Global gene expression profiling of human pleural mesotheliomas: identification of matrix metalloproteinase 14 (MMP-14) as potential tumour target. PLoS One 2009; 4:e7016.
52. Stygar D, Muravitskaya N, Eriksson B, Eriksson H, Sahlin L. Effects of SERM (selective estrogen receptor modulator) treatment on growth and proliferation in the rat uterus. Reprod Biol Endocrinol 2003; 1:40.
53. Franken DR, Franken CJ, de la Guerre H, de Villiers A. Normal sperm morphology and chromatin packaging: comparison between aniline blue and chromomycin A3 staining. Andrologia 1999; 31:361-366.
54. Evenson DP, Jost LK, Marshall D, Zinaman MJ, Clegg E, Purvis K, de Angelis P, Claussen OP. Utility of sperm chromatin structure assay as a diagnostic tool in the human fertility clinic. Hum Reprod 1999; 14: 1039-1049.
55. Carreau S, Hess RA. Oestrogens and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010; 365:1517-1535.
56. Ebling FJ, Brooks AN, Cronin AS, Ford H, Kerr JB. Estrogenic induction of spermatogenesis in the hypogonadal mouse. Endocrinology 2000; 141: 2861-2869.
57. Murphy LL, Muñoz RM, Adrian BA, Villanúa MA. Function of cannabinoid receptors in the neuroendocrine regulation of hormone secretion. Neurobiol Dis 1998; 5:432-446.
58. Gammon CM, Freeman GM Jr, Xie W, Petersen SL, Wetsel WC. Regulation of gonadotropin-releasing hormone secretion by cannabinoids. Endocrinology 2005; 146:4491-4499.
59. Farkas I, Kalló I, Deli L, Vida B, Hrabovszky E, Fekete C, Moenter SM, Watanabe M, Liposits Z. Retrograde endocannabinoid signaling reduces GABAergic synaptic transmission to gonadotropin-releasing hormone neurons. Endocrinology 2010; 151:5818-5829.
60. d'Anglemont de Tissigny X, Colledge WH. The role of kisspeptin signaling in reproduction. Physiology 2010; 25:207-217.
61. Lerrant Y, Kottler ML, Bergametti F, Moumni M, Blumberg-Tick J, Counis R. Expression of gonadotropin-releasing hormone (GnRH) receptor gene is altered by GnRH agonist desensitization in a manner similar to that of gonadotropin beta-subunit genes in normal and castrated rat pituitary. Endocrinology 1995; 136:2803-2808.
62. Nitta H, Bunick D, Hess RA, Janulis L, Newton SC, Millette CF, Osawa Y, Shizuta Y, Toda K, Bahr JM. Germ cells of the mouse testis express P450 aromatase. Endocrinology 1993; 132:1396-1401.
63. George JW, Dille EA, Heckert LL. Current concepts of follicle-stimulating hormone receptor gene regulation. Biol Reprod 2011; 84:7-17.
64. Bourguiba S, Genissel C, Lambard S, Bouraïma H, Carreau S. Regulation of aromatase gene expression in Leydig cells and germ cells. J Steroid Biochem Mol Biol 2003; 86:335-343.
65. Allan CM, Couse JF, Simanainen U, Spaliviero J, Jimenez M, Rodriguez K, Korach KS, Handelsman DJ. Estradiol induction of spermatogenesis is mediated via an estrogen receptor-falphag mechanism involving neuroendocrine activation of follicle-stimulating hormone secretion. Endocrinology 2010; 151:2800-2810.
66. Baines H, Nwagwu MO, Hastie GR, Wiles RA, Mayhew TM, Ebling FJ. Effects of estradiol and FSH on maturation of the testis in the hypogonadal (hpg) mouse. Reprod Biol Endocrinol 2008; 6:4.
67. Hrabovszky E, Steinhauser A, Barabás K, Shughrue PJ, Petersen SL, Merchenthaler I, Liposits Z. Estrogen receptor-beta immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2001; 142:3261-3264.
68. Harris HA. Estrogen receptor-beta: recent lessons from in vivo studies. Mol Endocrinol 2007; 21:1-13.
69. Zhao M, Shirley CR, Yu YE, Mohapatra B, Zhang Y, Unni E, Deng JM, Arango NA, Terry NH, Weil MM, Russell LD, Behringer RR, et al. Targeted disruption of the transition protein 2 gene affects sperm chromatin structure and reduces fertility in mice. Mol Cell Biol 2001; 21:7243-7255.
70. Aleem M, Padwal V, Choudhari J, Balasinor N, Parte P, Gill-Sharma MK. Estradiol affects androgen-binding protein expression and fertilizing ability of spermatozoa in adult male rats. Mol Cell Endocrinol 2006; 253:1-13.
71. Aravindan GR, Krishnamurthy H, Moudgal NR. Enhanced susceptibility of follicle-stimulating-hormone-deprived infertile bonnet monkey (Macaca radiata) spermatozoa to dithiothreitol-induced DNA decondensation in situ. J Androl 1997; 18:688-697.
72. Krishnamurthy H, Kumar KM, Joshi CV, Krishnamurthy HN, Moudgal RN, Sairam MR. Alterations in sperm characteristics of folliclestimulating hormone (FSH)-immunized men are similar to those of FSH-deprived infertile male bonnet monkeys. J Androl 2000; 21:316-327.
73. Ahmadi A, Ng SC. Fertilizing ability of DNA-damaged spermatozoa. J Exp Zool 1999; 284:696-704.