The effect of cigarette smoke on fertilization and pre-implantation development: Assessment using animal models, clinical data, and stem cells

Biological Research

Volumn 44, Issue 2, 2011, Pages 189-194

  Talbot, Prue ^a   Lin, Sabrina ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cigarette smoke; Embryos; Fertilization; IVF; Stem cells; Toxicology

Indexed keywords

ANIMALIA;

EID: 80052065330     PISSN: 07169760     EISSN: 07176287     Source Type: Journal    
DOI: 10.4067/S0716-97602011000200011     Document Type: Article

References (71)

1. BENOWITZ N L (2008) Clinical pharmacology of nicotine: implications for understanding, preventing, and treating tobacco addiction. Clin Pharmacol Ther 83, 531-41.
2. BUESEN R, GENSCHOW E, SLAWIK B, VISAN A, SPIELMANN H, LUCH A, SEILER A (2009) Embryonic Stem Cell Test Remastered: Comparison between the Validated EST and the New Molecular FACS-EST for Assessing Developmental Toxicity In Vitro. Toxicol Sci 108, 389-400.
3. CASTLES A, ADAMS E K, MELVIN C L, KELSCH C, BOULTON M L (1999) Effects of smoking during pregnancy. Five meta-analyses. Am J Prev Med 16, 208-15.
4. CHAPIN R, AUGUSTINE-RAUCH K, BEYER B, DASTON G, FINNELL R, FLYNN T, HUNTER S, MIRKES P, O'SHEA K S, PIERSMA A, SANDLER D, VANPARYS P, VAN MAELE-FABRY G (2008) State of the art in developmental toxicity screening methods and a way forward: a meeting report addressing embryonic stem cells, whole embryo culture, and zebrafi sh. Birth Defects Res B Dev Reprod Toxicol 83, 446-56.
5. CHEN L, ZHANG H, POWERS R W, RUSSELL P T, LARSEN W J (1996) Covalent linkage between proteins of the inter-a-inhibitor family and hyaluronic acid is mediated by a factor produced by granulosa cells. J Biol Chem 27, 19409-19414.
6. COOPER A R, MOLEY K H (2008) Maternal tobacco use and its preimplantation effects on fertility: more reasons to stop smoking. Semin Reprod Med 26, 204-12.
7. CROXATTO H B, VILLALÓN M (1994) Oocyte Transport. In Cambridge Reviews in Human Reproduction: The Oocyte (ed. J. G. Grudzinskas, T. Chard, J. L. Simpson and J. Yovich), pp. 253-276. Cambridge University Press, Cambridge.
8. DÁVILA J C, CEZAR G G, THIEDE M, STROM S, MIKI T, TROSKO J (2004) Use and application of stem cells in toxicology. Toxicol Sci 79, 214-23.
9. DETMAR J, RABAGLINO T, TANIUCHI Y, OH J, ACTON B M, BENITO A, NÚÑEZ G, JURISICOVA A (2006) Embryonic loss due to exposure to polycyclic aromatic hydrocarbons is mediated by Bax. Apoptosis 11, 1413-25.
10. DICARLANTONIO G, TALBOT P (1999) Inhalation of mainstream and sidestream cigarette smoke retards embryo transport and slows muscle contraction in oviducts of hamsters (Mesocricetus auratus). Biol Reprod 61, 651-6.
11. DIFRANZA J R, ALIGNE C A, WEITZMAN M (2004) Prenatal and postnatal environmental tobacco smoke exposure and children's health. Pediatrics 113, 1007-15.
12. DWYER J B, BROIDE R S, LESLIE F M (2008) Nicotine and brain development. Birth Defects Res C Embryo Today 84, 30-44.
13. EL MULLA K F, KOHN F M, EL BEHEIRY A H, SCHILL W B (1995) The effect of smoking and varicocele on human sperm acrosin activity and acrosome reaction. Hum Reprod 10, 3190-4.
14. EPA (1992) EPA Report/600/6-90/006F: Respiratory health effects of passive smoking: lung cancer and other disorders, Washington, DC.
15. EPA C (2005) Proposed identifi cation of environmental tobacco smoke as a toxic air contaminant. Part B: Health Effects. California Environmental Protection Agency, Office of Environmental Health Hazard Assessment, Sacramento.
16. ESPOSITO E R, HORN K H, GREENE R M, PISANO M M (2008) An animal model of cigarette smoke-induced in utero growth retardation. Toxicology 246, 193-202.
17. FULOP C, SZANTO S, MUKHOPADHYAY D, BARDOS T, KAMATH R V, RUGG M S, DAY A J, SALUSTRI A, HASCALL V C, GLANT T T, MIKECZ K (2003) Impaired cumulus mucifi cation and female sterility in tumor necrosis factor-induced protein-6 defi cient mice. Development 130, 2253-61.
18. GIESEKE C, TALBOT P (2005) Cigarette smoke inhibits hamster oocyte pickup by increasing adhesion between the oocyte cumulus complex and oviductal cilia. Biol Reprod 73, 443-51.
19. GOEL P, RADOTRA A, SINGH I, AGGARWAL A, DUA D (2004) Effects of passive smoking on outcome in pregnancy. J Postgrad Med 50, 12-6.
20. HANDLER A, DAVIS F, FERRE C, YEKO T (1989). The relationship of smoking and ectopic pregnancy. Am J Public Health 79, 1239-42.
21. HEGAARD H K, KJAERGAARD H, MOLLER L F, WACHMANN H, OTTESEN B (2006). The effect of environmental tobacco smoke during pregnancy on birth weight. Acta Obstet Gynecol Scand 85, 675-81.
22. HOFFMANN D, DJORDJEVIC M V, HOFFMANN I (1997) The changing cigarette. Preventive Medicine 26, 437-434.
23. HUNG P H, BAUMBER J, MEYERS S A, VANDEVOORT C A (2007) Effects of environmental tobacco smoke in vitro on rhesus monkey sperm function. Reprod Toxicol 23, 499-506.
24. JENKINS R A, GUERIN M R, TOMKINS B A (2000) Mainstream and sidestream cigarette smoke. In Chemistry of Environmental Tobacco Smoke: Composition and Measurement, pp. 49-75. CRC Press, Boca Raton.
25. JI L, MELKONIAN G, RIVELES K, TALBOT P (2002) Identification of pyridine compounds in cigarette smoke solution that inhibit growth of the chick chorioallantoic membrane. Toxicol Sci 69, 217-25.
26. KHARRAZI M, DELORENZE G N, KAUFMAN F L, ESKENAZI B, BERNERT J T, JR GRAHAM S, PEARL M, PIRKLE J (2004) Environmental tobacco smoke and pregnancy outcome. Epidemiology 15, 660-70.
27. KNOLL M, TALBOT P (1998) Cigarette smoke inhibits oocyte cumulus complex pick-up by the oviduct independent of ciliary beat frequency. Reproductive Toxicology 12, 57-68.
28. LAM X, GIESEKE C, KNOLL M, TALBOT P (2000) Assay and importance of adhesive interaction between hamster (Mesocricetus auratus) oocytecumulus complexes and the oviductal epithelium. Biol Reprod 62, 579-88.
29. LIN S, TRAN V, TALBOT P (2009) Comparison of Toxicity of Smoke From Traditional and Harm Reduction Cigarettes Using Embryonic Stem Cells as a Novel Model for Pre-Implantation Development. Human Reproduction 24, 386-397.
30. MAGERS T, TALBOT P, DICARLANTONIO G, KNOLL M, DEMERS D, TSAI I, HOODBHOY T (1995). Cigarette smoke inhalation affects the reproductive system of female hamsters. Reprod Toxicol 9, 513-25.
31. MAHI-BROWN C A, YANAGIMACHI R (1983) Parameters infl uencing ovum pickup by oviductal fi mbria in the golden hamster. Gam Res 8, 1-10.
32. MARITZ G S (2008) Nicotine and lung development. Birth Defects Res C Embryo Today 84, 45-53.
33. MARTIN G R (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 78, 7634-8.
34. MELKONIAN G, ECKELHOEFER H, WU M, WANG Y, TONG C, RIVELES K, P T (2003) Growth and angiogenesis are inhibited in vivo in developing tissues by pyrazine and its derivatives. Toxicological Sciences 75, 393-401.
35. MLYNARCIKOVA A, SCSUKOVA S, VRSANSKA S, NAGYOVA E, FICKOVA M, KOLENA J (2004) Inhibitory effect of cadmium and tobacco alkaloids on expansion of porcine oocyte-cumulus complexes. Cent Eur J Public Health 12 Suppl, S62-4.
36. NERI A, MARCUS S L (1972) Effect of nicotine on the motility of the oviducts in the Rhesus monkey: a preliminary report. J Reproduction Fertility 31, 91-.
37. NORWOOD J T, ANDERSON R G W (1980) Evidence that adhesive sites on the tips of oviduct cilia membranes are required for ovum pickup in situ. Biol Reprod 23, 788-791.
38. RICHARDS J S (2005) Ovulation: new factors that prepare the oocyte for fertilization. Mol Cell Endocrinol 234, 75-9.
39. RIVELES K, IV M, AREY J, TALBOT P (2003) Pyridines in cigarette smoke inhibit hamster oviductal functioning in picomolar doses. Reprod Toxicol 17, 191-202.
40. RIVELES K, ROZA R, AREY J, TALBOT P (2004) Pyrazine derivatives in cigarette smoke inhibit hamster oviductal functioning. Reprod Biol Endocrinol 2, 23.
41. RIVELES K, ROZA R, TALBOT P (2005) Phenols, quinolines, indoles, benzene, and 2-cyclopenten-1-ones are oviductal toxicants in cigarette smoke. Toxicol Sci 86, 141-51.
42. ROGERS J M (2008) Tobacco and pregnancy: overview of exposures and effects. Birth Defects Res C Embryo Today 84, 1-15.
43. SARAIYA M, BERG C J, KENDRICK J S, STRAUSS L T, ATRACH H K, AHN Y W (1998) Cigarette smoking as a risk factor for ectopic pregnancy. Am J Obstet Gynecol 178, 493-498.
44. SEILER, A, VISAN A, BUESEN R, GENSCHOW E, SPIELMANN H (2004) Improvement of an in vitro stem cell assay for developmental toxicity: the use of molecular endpoints in the embryonic stem cell test. Reprod Toxicol 18, 231-40.
45. SHILOH H, LAHAV-BARATZ S, KOIFMAN M, ISHAI D, BIDDER D, WEINER-MEGANZI Z, DIRNFELD M (2004) The impact of cigarette smoking on zona pellucida thickness of oocytes and embryos prior to transfer into the uterine cavity. Hum Reprod 19, 157-9.
46. SHIVERICK K T, SALAFIA C (1999) Cigarette smoking and pregnancy I: ovarian, uterine and placental effects. Placenta 20, 265-72.
47. SINKO I, MOROCZ M, ZADORI J, KOKAVSZKY K, RASKO I (2005) Effect of cigarette smoking on DNA damage of human cumulus cells analyzed by comet assay. Reprod Toxicol 20, 65-71.
48. SOARES S R, MELO M A (2008) Cigarette smoking and reproductive function. Curr Opin Obstet Gynecol 20, 281-91.
49. STILLMAN R J, ROSENBERG M J, SACHS B P (1986) Smoking and Reproduction. Fertil and Sterility 46, 545-566.
50. SWARTZ W J, MATTISON D R (1985) Benzo(a)pyrene inhibits ovulation in C57BL/6N mice. Anat Rec 212, 268-276.
51. TALBOT P (1983) Intrafollicular pressure promotes partial evacuation of the antrum during hamster ovulation in vitro. J Exp Zool 226, 129-35.
52. TALBOT P, DICARLANTONIO G, ZAO P, PENKALA J, HAIMO LT (1985) Motile cells lacking hyaluronidase can penetrate the hamster oocyte cumulus complex. Dev Biol 108, 387-98.
53. TALBOT P, GIESKE C, KNOLL M (1999) Oocyte pickup by the mammalian oviduct. Mol Biol Cell 10, 5-8.
54. TALBOT P, RIVELES K (2005) Smoking and reproduction: the oviduct as a target of cigarette smoke. Reprod Biol Endocrinol 3, 52.
55. TALBOT P, SHUR B, MYLES D (2003) Cell adhesion and fertilization: steps in oocyte transport, sperm-zona pellucida interactions, and sperm-egg fusion. Biology of Reproduction 68, 1-9.
56. THOMSON JA, ITSKOVITZ-ELDOR J, SHAPIRO SS, WAKNITZ MA, SWIERGIEL JJ, MARSHALL VS, JONES JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-7.
57. USDHHS (2001) Women and smoking: a report of the surgeon general. United States Department of Health and Human Services, Centers for Disease Control and Prevention, Offi ce on Smoking and Health, Atlanta.
58. USDHHS (2006) The health consequences of involuntary exposure to tobacco smoke: a reprt of the surgeon general. United States Department of Health and Human Services, Centers for Disease Control and Prevention, Offi ce on Smoking and Human Health, Atlanta.
59. VAN VOORHIS B J, SYROP C H, HAMMITT D G, DUNN M S, SNYDER G D (1992) Effects of smoking on ovulation induction for assisted reproductive techniques. Fertil Steril 58, 981-5.
60. VILORIA T, RUBIO M C, RODRIGO L, CALDERÓN G, MERCADER A, MATEU E, MESEGUER M, REMOHI J, PELLICER A (2005) Smoking habits of parents and male: female ratio in spermatozoa and preimplantation embryos. Hum Reprod 20, 2517-22.
61. VRSANSKA S, NAGYOVA E, MLYNARCIKOVA A, FICKOVA M, KOLENA J (2003) Components of cigarette smoke inhibit expansion of oocytecumulus complexes from porcine follicles. Physiol Res 52, 383-7.
62. WAYLEN A L, METWALLY M, JONES G L, WILKINSON A J, LEDGER W L (2009) Effects of cigarette smoking upon clinical outcomes of assisted reproduction: a meta-analysis. Hum Reprod Update 15, 31-44.
63. WINDHAM G C, HOPKINS B, FENSTER L, SWAN S H (2000) Prenatal active or passive tobacco smoke exposure and the risk of preterm delivery or low birth weight. Epidemiology 11, 427-33.
64. YAMAMOTO Y, ISOYAMA E, SOFIKITIS N, MIYAGAWA I (1998) Effects of smoking on testicular function and fertilizing potential in rats. Urol Res 26, 45-8.
65. YANAGIMACHI R (1984) Fertilization in mammals. Tokai J Exp Clin Med 9, 81-5.
66. ZDRAVKOVIC T, GENBACEV O, LAROCQUE N, MCMASTER M, FISHER S (2008) Human embryonic stem cells as a model system for studying the effects of smoke exposure on the embryo. Reprod Toxicol.
67. ZHANG H, GUO D, WANG L, ZHAO Y, CHENG Y, QIAO Z (2005) Effect of nicotine on Oct-4 and Rex-1 expression of mouse embryonic stem cells. Reprod Toxicol 19, 473-8.
68. ZHAO Z, REECE E A (2005) Nicotine-induced embryonic malformations mediated by apoptosis from increasing intracellular calcium and oxidative stress. Birth Defects Res B Dev Reprod Toxicol 74, 383-91.
69. ZHOU R, ZHOU Y, LI S, HAUG A (2000) Effect of environmental tobacco smoke on intracellular free calcium of boar sperm incubated in seminal plasma. Toxicol Lett 114, 135-41.
70. ZHUO L, YONEDA M, ZHAO M, YINGSUNG W, YOSHIDA N, KITAGAWA Y, KAWAMURA K, SUZUKI T, KIMATA K (2001) Defect in SHAPhyaluronan complex causes severe female infertility. A study by inactivation of the bikunin gene in mice. J Biol Chem 276, 7693-6.
71. ZUR NIEDEN N I, KEMPKA G, AHR H J (2004) Molecular multiple endpoint embryonic stem cell test--a possible approach to test for the teratogenic potential of compounds. Toxicol Appl Pharmacol 194, 257-69.