Oxidative stress and oocyte quality: ethiopathogenic mechanisms of minimal/mild endometriosis-related infertility

Cell and Tissue Research

Volumn 364, Issue 1, 2016, Pages

  Da Broi, Michele Gomes ^a   Navarro, Paula Andrea ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Early endometriosis; Follicular microenvironment; Infertility; Oocyte quality; Oxidative stress

Indexed keywords

CUMULUS CELL; DISEASE ASSOCIATION; ENDOMETRIOSIS; FEMALE GENITAL TRACT PARAMETERS; FEMALE INFERTILITY; HUMAN; NONHUMAN; OOCYTE MATURATION; OOCYTE QUALITY; OVARY FOLLICLE FLUID; OXIDATIVE STRESS; PATHOGENESIS; PERITONEAL FLUID; PRIORITY JOURNAL; REVIEW; SERUM; ANIMAL; FEMALE; METABOLISM; OOCYTE; PATHOLOGY;

ANIMALS; ENDOMETRIOSIS; FEMALE; HUMANS; INFERTILITY, FEMALE; OOCYTES; OXIDATIVE STRESS;

EID: 84950302486     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-015-2339-9     Document Type: Review

References (69)

1. Agarwal A, Saleh RA, Bedaiwy MA (2003) Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79:829–843
2. Agarwal A, Gupta S, Sharma RK (2005) Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 3:28
3. Akande VA, Hunt LP, Cahill DJ, Jenkins JM (2004) Differences in time to natural conception between women with unexplained infertility and infertile women with minor endometriosis. Hum Reprod 19:96–103
4. Albertini DF (1992) Cytoplasmic microtubular dynamics and chromatin organization during mammalian oogenesis and oocyte maturation. Mutat Res 296:57–68
5. Al-Fadhli R, Kelly SM, Tulandi T, Tanr SL (2006) Effects of different stages of endometriosis on the outcome of in vitro fertilization. J Obstet Gynaecol Can 28:888–891
6. Alpay Z, Saed GM, Diamond MP (2006) Female infertility and free radicals: potential role in adhesions and endometriosis. J Soc Gynecol Investig 13:390–398
7. Appasamy M, Jauniaux E, Serhal P, Al-Qahtani A, Groome NP, Muttukrishna S (2008) Evaluation of the relationship between follicular fluid oxidative stress, ovarian hormones, and response to gonadotropin stimulation. Fertil Steril 89:912–921
8. Attaran M, Pasqualotto E, Falcone T, Goldberg JM, Miller KF, Agarwal A, Sharma RK (2000) The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int J Fertil Womens Med 45:314–320
9. Augoulea A, Alexandrou A, Creatsa M, Vrachnis N, Lambrinoudaki I (2012) Pathogenesis of endometriosis: the role of genetics, inflammation and oxidative stress. Arch Gynecol Obstet 286:99–103
10. Barcelos ID, Vieira RC, Ferreira EM, Martins WP, Ferriani RA, Navarro PA (2009) Comparative analysis of the spindle and chromosome configurations of in vitro-matured oocytes from patients with endometriosis and from control subjects: a pilot study. Fertil Steril 92:1749–1752
11. Barcelos ID, Donabella FC, Ribas CP, Meola J, Ferriani RA, Paz CC de, Navarro PA (2015) Down-regulation of the CYP19A1 gene in cumulus cells of infertile women with endometriosis. Reprod Biomed Online 30:532–541
12. Bellelis P, Dias JA Jr, Podgaec S, Gonzales M, Baracat EC, Abrao MS (2010) Epidemiological and clinical aspects of pelvic endometriosis—a case series. Rev Assoc Med Bras 56:467–471
13. Bergqvist A, D’Hooghe T (2002) Mini symposium on pathogenesis of endometriosis and treatment of endometriosis-associated subfertility. Introduction: the endometriosis enigma. Hum Reprod Update 8:79–83
14. Brizek CL, Schlaff S, Pellegrini VA, Frank JB, Worrilow KC (1995) Increased incidence of aberrant morphological phenotypes in human embryogenesis—an association with endometriosis. J Assist Reprod Genet 12:106–112
15. Campos Petean C, Ferriani RA, Reis RM dos, Moura MD de, Jordao AA Jr, Navarro PA (2008) Lipid peroxidation and vitamin E in serum and follicular fluid of infertile women with peritoneal endometriosis submitted to controlled ovarian hyperstimulation: a pilot study. Fertil Steril 90:2080–2085
16. Carvalho LF, Samadder AN, Agarwal A, Fernandes LF, Abrao MS (2012) Oxidative stress biomarkers in patients with endometriosis: systematic review. Arch Gynecol Obstet 286:1033–1040
17. Da Broi MG, Andrade AZ, Rodrigues JK, Paz CCP, Jordão AA, Navarro PA (2013) Total antioxidant capacity (TAC) levels in follicular fluid of infertile patients undergoing ICSI: a possible predictor of clinical pregnancy. IFFS/ASRM Conjoint Meeting. Fertil Steril 100:S425
18. Da Broi MG, Albuquerque FO, Andrade AZ de, Cardoso RL, Jordão AA Jr, Navarro PA (2014a) Systemic and follicular oxidative stress in infertile women with endometriosis undergoing controlled ovarian stimulation for ICSI: is there a role in the ethiopathogenesis of infertility? Fertil Steril 102:e79
19. Da Broi MG, Malvezzi H, Paz CC, Ferriani RA, Navarro PA (2014b) Follicular fluid from infertile women with mild endometriosis may compromise the meiotic spindles of bovine metaphase II oocytes. Hum Reprod 29:315–323
20. Da Broi MG, Rodrigues JK, Andrade AZ, Giorgi VSI, Jordão AA, Navarro P (2014c) Systemic and follicular oxidative stress in infertile women with minimal/mild endometriosis undergoing controlled ovarian stimulation for ICSI: is there a role in the etiopathogenesis of infertility? JBRA Assist Reprod 18:117
21. De Santis L, Cino I, Rabellotti E, Calzi F, Persico P, Borini A, Coticchio G (2005) Polar body morphology and spindle imaging as predictors of oocyte quality. Reprod Biomed Online 11:36–42
22. Donabela F, Barcelos I, Pavdovan C, Meola J, Ferriani RA, Navarro P (2011) PTGS2 gene expression (COX2) in cummulus oophorus cells of endometriosis and control infertile patients submitted to ICSI. ASRM 67th Annual Meeting. Fertil Steril 96: S236–S237
23. Eichenlaub-Ritter U, Shen Y, Tinneberg HR (2002) Manipulation of the oocyte: possible damage to the spindle apparatus. Reprod Biomed Online 5:117–124
24. Eppig JJ, Wigglesworth K, Pendola FL (2002) The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A 99:2890–2894
25. Ferreira EM, Vireque AA, Adona PR, Meirelles FV, Ferriani RA, Navarro PA (2009) Cytoplasmic maturation of bovine oocytes: structural and biochemical modifications and acquisition of developmental competence. Theriogenology 71:836–848
26. Ferriani RA, Barcelos I, Donabela F, Ribas C, Meola J, Navarro PA (2013) Lower expression of the gene CYP19A1 in cumulus oophorus cells from infertile women with minimal and mild endometriosis may be involved in the infertility related to this disease. 5th International IVI Congress, Seville, Spain. http://comtecmed.com/ivi/2013/Uploads/Editor/abstract_41.pdf
27. Garcia-Velasco JA, Arici A (1999) Is the endometrium or oocyte/embryo affected in endometriosis? Hum Reprod 14(Suppl 2):77–89
28. Garrido N, Navarro J, Remohi J, Simon C, Pellicer A (2000) Follicular hormonal environment and embryo quality in women with endometriosis. Hum Reprod Update 6:67–74
29. Giorgi VS, Da Broi MG, Paz CC, Ferriani RA, Navarro PA (2015) N-acetyl-cysteine and L-carnitine prevent meiotic oocyte damage induced by follicular fluid from infertile women with mild endometriosis. Reprod Sci (in press)
30. Giudice LC, Kao LC (2004) Endometriosis. Lancet 364:1789–1799
31. Gnoth C, Godehardt D, Godehardt E, Frank-Herrmann P, Freundl G (2003) Time to pregnancy: results of the German prospective study and impact on the management of infertility. Hum Reprod 18:1959–1966
32. Gupta S, Agarwal A, Krajcir N, Alvarez JG (2006) Role of oxidative stress in endometriosis. Reprod Biomed Online 13:126–134
33. Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A (2008) Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril 90:247–257
34. Halliwell B (1994) Free radicals, antioxidants, and human disease: curiosity, cause, or consequence? Lancet 344:721–724
35. Hamel M, Dufort I, Robert C, Gravel C, Leveille MC, Leader A, Sirard MA (2008) Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod 23:1118–1127
36. Haouzi D, Hamamah S (2009) Pertinence of apoptosis markers for the improvement of in vitro fertilization (IVF). Curr Med Chem 16:1905–1916
37. 2 and ageing on spindles and chromosomes in mouse oocytes from pre-antral follicle culture. Hum Reprod 16:737–748
38. Hughes EG, Fedorkow DM, Collins JA (1993) A quantitative overview of controlled trials in endometriosis-associated infertility. Fertil Steril 59:963–970
39. Jackson LW, Schisterman EF, Dey-Rao R, Browne R, Armstrong D (2005) Oxidative stress and endometriosis. Hum Reprod 20:2014–2020
40. Jianini BTGM, Giorgi VSI, Malvezzi H, Da Broi MG, Paz CCP da, Navarro PAAS (2014) Peritoneal fluid from infertile women with minimal/mild endometriosis may compromise the spindle of metaphase II bovine oocytes. 8th Annual Congress of the SBRA. JBRA Assist Reprod 18:117–118
41. Kim NH, Chung HM, Cha KY, Chung KS (1998) Microtubule and microfilament organization in maturing human oocytes. Hum Reprod 13:2217–2222
42. Kumbak B, Kahraman S, Karlikaya G, Lacin S, Guney A (2008) In vitro fertilization in normoresponder patients with endometriomas: comparison with basal simple ovarian cysts. Gynecol Obstet Invest 65:212–216
43. Liu L, Trimarchi JR, Navarro P, Blasco MA, Keefe DL (2003) Oxidative stress contributes to arsenic-induced telomere attrition, chromosome instability, and apoptosis. J Biol Chem 278:31998–32004
44. Ma CH, Yan LY, Qiao J, Sha W, Li L, Chen Y, Sun QY (2010) Effects of tumor necrosis factor-alpha on porcine oocyte meiosis progression, spindle organization, and chromosome alignment. Fertil Steril 93:920–926
45. Mandelbaum J, Anastasiou O, Levy R, Guerin JF, Larouziere V de, Antoine JM (2004) Effects of cryopreservation on the meiotic spindle of human oocytes. Eur J Obstet Gynecol Reprod Biol 113 (Suppl 1):S17–S23
46. Mansour G, Abdelrazik H, Sharma RK, Radwan E, Falcone T, Agarwal A (2009) L-carnitine supplementation reduces oocyte cytoskeleton damage and embryo apoptosis induced by incubation in peritoneal fluid from patients with endometriosis. Fertil Steril 91:2079–2086
47. Marcoux S, Maheux R, Berube S (1997) Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian Collaborative Group on Endometriosis. N Engl J Med 337:217–222
48. Mullen SF, Agca Y, Broermann DC, Jenkins CL, Johnson CA, Critser JK (2004) The effect of osmotic stress on the metaphase II spindle of human oocytes, and the relevance to cryopreservation. Hum Reprod 19:1148–1154
49. Murphy AA, Santanam N, Morales AJ, Parthasarathy S (1998) Lysophosphatidyl choline, a chemotactic factor for monocytes/T-lymphocytes is elevated in endometriosis. J Clin Endocrinol Metab 83:2110–2113
50. Navarro PA, Liu L, Keefe DL (2004) In vivo effects of arsenite on meiosis, preimplantation development, and apoptosis in the mouse. Biol Reprod 70:980–985
51. Navarro PA, Liu L, Ferriani RA, Keefe DL (2006) Arsenite induces aberrations in meiosis that can be prevented by coadministration of N-acetylcysteine in mice. Fertil Steril 85 (Suppl 1):1187–1194
52. Navarro PA, Malvezzi H, Da Broi MG, Rosa e Silva JC, Vireque AA, Meola J (2013) The peritoneal fluid of infertile women with and without minimal/mild endometriosis reduces the expression of genes GSR and CAT in bovine oocytes. 5th International IVI Congress, Seville, Spain. http://comtecmed.com/ivi/2013/Uploads/Editor/abstract_88.pdf
53. Ngo C, Chereau C, Nicco C, Weill B, Chapron C, Batteux F (2009) Reactive oxygen species controls endometriosis progression. Am J Pathol 175:225–234
54. Parazzini F (1999) Ablation of lesions or no treatment in minimal-mild endometriosis in infertile women: a randomized trial. Gruppo Italiano per lo Studio dell’Endometriosi. Hum Reprod 14:1332–1334
55. Pasqualotto EB, Agarwal A, Sharma RK, Izzo VM, Pinotti JA, Joshi NJ, Rose BI (2004) Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril 81:973–976
56. Pellicer A, Oliveira N, Ruiz A, Remohi J, Simon C (1995) Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod 10 (Suppl 2):91–97
57. Practice Committee of the ASRM (2012) Endometriosis and infertility: a committee opinion. Fertil Steril 98:591–598
58. Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, Dekel N (2011) Reactive oxygen species are indispensable in ovulation. Proc Natl Acad Sci U S A 108:1462–1467
59. Signorile PG, Baldi A (2010) Endometriosis: new concepts in the pathogenesis. Int J Biochem Cell Biol 42:778–780
60. Simon C, Gutierrez A, Vidal A, de los Santos MJ, Tarin JJ, Remohi J, Pellicer A (1994) Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod 9:725–729
61. Singh N, Lata K, Naha M, Malhotra N, Tiwari A, Vanamail P (2014) Effect of endometriosis on implantation rates when compared to tubal factor in fresh non donor in vitro fertilization cycles. J Hum Reprod Sci 7:143–147
62. Sung L, Mukherjee T, Takeshige T, Bustillo M, Copperman AB (1997) Endometriosis is not detrimental to embryo implantation in oocyte recipients. J Assist Reprod Genet 14:152–156
63. Szczepanska M, Kozlik J, Skrzypczak J, Mikolajczyk M (2003) Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril 79:1288–1293
64. Tanghe S, Van Soom A, Nauwynck H, Coryn M, Kruif A de (2002) Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 61:414–424
65. Tesfaye D, Ghanem N, Carter F, Fair T, Sirard MA, Hoelker M, Schellander K, Lonergan P (2009) Gene expression profile of cumulus cells derived from cumulus-oocyte complexes matured either in vivo or in vitro. Reprod Fertil Dev 21:451–461
66. Van Blerkom J, Davis P (2001) Differential effects of repeated ovarian stimulation on cytoplasmic and spindle organization in metaphase II mouse oocytes matured in vivo and in vitro. Hum Reprod 16:757–764
67. Van Langendonckt A, Casanas-Roux F, Donnez J (2002) Oxidative stress and peritoneal endometriosis. Fertil Steril 77:861–870
68. Volarcik K, Sheean L, Goldfarb J, Woods L, Abdul-Karim FW, Hunt P (1998) The meiotic competence of in-vitro matured human oocytes is influenced by donor age: evidence that folliculogenesis is compromised in the reproductively aged ovary. Hum Reprod 13:154–160
69. Wang WH, Keefe DL (2002) Prediction of chromosome misalignment among in vitro matured human oocytes by spindle imaging with the PolScope. Fertil Steril 78:1077–1081