Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지

Oxidative Stress Induced Damage to Paternal Genome and Impact of Meditation and Yoga - Can it Reduce Incidence of Childhood Cancer?

  • Dada, Rima (Department of Anatomy, Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences) ;
  • Kumar, Shiv Basant (Laboratory for Molecular Reproduction and Genetics) ;
  • Chawla, Bhavna (Ocular Oncology & Pediatric Ophthalmology Service, Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences) ;
  • Bisht, Shilpa (Laboratory for Molecular Reproduction and Genetics) ;
  • Khan, Saima (Laboratory for Molecular Reproduction and Genetics)
  • Published : 2016.09.01
⟨ Previous Next ⟩

Abstract

Background: Sperm DNA damage is underlying aetiology of poor implantation and pregnancy rates but also affects health of offspring and may also result in denovo mutations in germ line and post fertilization. This may result in complex diseases, polygenic disorders and childhood cancers. Childhood cancer like retinoblastoma (RB) is more prevalent in developing countries and the incidence of RB has increased more than three fold in India in the last decade. Recent studies have documented increased incidence of cancers in children born to fathers who consume alcohol in excess and tobacco or who were conceived by assisted conception. The aetiology of childhood cancer and increased disease burden in these children is lin ked to oxidative stress (OS) and oxidative DNA damage( ODD) in sperm of their fathers. Though several antioxidants are in use to combat oxidative stress, the effect of majority of these formulations on DNA is not known. Yoga and meditation cause significant decline in OS and ODD and aid in regulating OS levels such that reactive oxygen speues meditated signal transduction, gene expression and several other physiological functions are not disrupted. Thus, this study aimed to analyze sperm ODD as a possible etiological factor in childhood cancer and role of simple life style interventions like yoga and meditation in significantly decreasing seminal oxidative stress and oxidative DNA damage and thereby decreasing incidence of childhood cancers. Materials and Methods: A total of 131 fathers of children with RB (non-familial sporadic heritable) and 50 controls (fathers of healthy children) were recruited at a tertiary center in India. Sperm parameters as per WHO 2010 guidelines and reactive oxygen species (ROS), DNA fragmentation index (DFI), 8-hydroxy-2'-deoxy guanosine (8-OHdG) and telomere length were estimated at day 0, and after 3 and 6 months of intervention. We also examined the compliance with yoga and meditation practice and smoking status at each follow-up. Results: The seminal mean ROS levels (p<0.05), sperm DFI (p<0.001), 8-OHdG (p<0.01) levels were significantly higher in fathers of children with RB, as compared to controls and the relative mean telomere length in the sperm was shorter. Levels of ROS were significantly reduced in tobacco users (p<0.05) as well as in alcoholics (p<0.05) after intervention. DFI reduced significantly (p<0.05) after 6 months of yoga and meditation practice in all groups. The levels of oxidative DNA damage marker 8-OHdG were reduced significantly after 3 months (p<0.05) and 6 months (p<0.05) of practice. Conclusions: Our results suggest that OS and ODD DNA may contribute to the development of childhood cancer. This may be due to accumulation of oxidized mutagenic base 8OHdG, and elevated MDA levels which results in MDA dimers which are also mutagenic, aberrant methylation pattern, altered gene expression which affect cell proliferation and survival through activation of transcription factors. Increased mt DNA mutations and aberrant repair of mt and nuclear DNA due to highly truncatred DNA repair mechanisms all contribute to sperm genome hypermutability and persistant oxidative DNA damage. Oxidative stress is also associated with genome wide hypomethylation, telomere shortening and mitochondrial dysfunction leading to genome hypermutability and instability. To the best of our knowledge, this is the first study to report decline in OS and ODD and improvement in sperm DNA integrity following adoption of meditation and yoga based life style modification.This may reduce disease burden in next generation and reduce incidence of childhood cancers.

Keywords

References

  1. Aitken RJ, Baker MA, De Iuliis GN, et al (2010a). New insights into sperm physiology and pathology. Handb Exp Pharmacol, 16, 99-115.
  2. Aitken RJ, De Iuliis GN (2010b). On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod, 16, 3-13. https://doi.org/10.1093/molehr/gap059
  3. Aitken RJ, Smith TB, Jobling MS, et al (2014a). Oxidative stress and male reproductive health. Asian J Androl, 16, 31-8. https://doi.org/10.4103/1008-682X.122203
  4. Allen M, Dietz M, Blair KS, et al (2012). Cognitive-affective neural plasticity following active-controlled mindfulness intervention. J Neurosc, 32, 15601-10. https://doi.org/10.1523/JNEUROSCI.2957-12.2012
  5. Begg CB (1991). Statistics Medicine, 10, 1887-95. https://doi.org/10.1002/sim.4780101205
  6. Bock BC, Fava JL, Gaskins R, et al (2012). Yoga as a complementary treatment for smoking cessation in women. J Womens Health (Larchmt), 21, 240-48. https://doi.org/10.1089/jwh.2011.2963
  7. Bock BC, Rosen RK, Fava JL, et al (2014). Testing the efficacy of yoga as a complementary therapy for smoking cessation: design and methods of the breath easy trial. Contemporary clinical trials, 38, 321-32. https://doi.org/10.1016/j.cct.2014.06.003
  8. Bunin GR, Tseng M, Li Y, et al (2012). Parental diet and risk of retinoblastoma resulting from new germline RB1 mutation. Environ Mol Mutagen, 53, 451-61. https://doi.org/10.1002/em.21705
  9. Businelle MS, Lam CY, Kendzor DE, et al (2013). Alcohol consumption and urges to smoke among women during a smoking cessation attempt. Exp Clin Psychopharmacol, 21, 29-37. https://doi.org/10.1037/a0031009
  10. Callaway E (2012). Fathers bequeath more mutations as they age. Nature, 488, 439 https://doi.org/10.1038/488439a
  11. Cawthon RM (2009). Telomere length measurement by a novel monochrome multiplex quantitative PCR method. Nucleic Acids Res, 37, 21. https://doi.org/10.1093/nar/gkn1027
  12. Clara GM, Jaime G, Rosa R (2012). Types, causes, detection and repair of DNA fragmentation in animal and human sperm cells. Int J Mol Sci, 13, 14026-52. https://doi.org/10.3390/ijms131114026
  13. Cremers HP, Mercken L, Oenema A, et al (2012). A web-based computer-tailored smoking prevention programme for primary school children: intervention design and study protocol. BMC Publ Health, 12, 277. https://doi.org/10.1186/1471-2458-12-277
  14. Dada R, Kumar SB, Tolahunase M, et al (2015). Yoga and meditation as a therapeutic intervention in oxidative stress and oxidative DNA damage to paternal genome. J Yoga Phys Ther, 5, 4.
  15. Dada T, Faiq MA, Mohanty K, et al (2016). Effect of yoga and meditation based intervention on intraocular pressure, quality of life, oxidative stress and gene expression pattern in primary open angle glaucoma: a randomized controlled. association of research on vision and ophthalmology (ARVO). 2016. ARVO 2016 Annual Meeting Abstracts.
  16. Davis JM, Mills DM, Stankevitz KA, et al (2013). Pilotrandomized trial on mindfulness training for smokers in young adult binge drinkers. BMC Complement Altern Med, 13, 215. https://doi.org/10.1186/1472-6882-13-215
  17. Evenson DP, Jost LK, Marshall D, et al (1999). Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod, 14, 1039-49. https://doi.org/10.1093/humrep/14.4.1039
  18. Farb NAS, Segal ZV, Mayberg H, et al (2007). Attending to the present: mindfulness meditation reveals distinct neural modes of self-reference. Soc Cogn Affect Neurosci, 2, 313-22. https://doi.org/10.1093/scan/nsm030
  19. Fiore MC, Jaen CR, Baker TB, et al (2008). Treating tobacco use and dependence: 2008 update. rockville, md: u.s. department of health and human services, U.S. Public Health Service; 2008.
  20. Forster P, Hohoff C, Dunkelmann B, et al (2015). Elevated germline mutation rate in teenage fathers. Proc R Soc B, 282, 20142898. https://doi.org/10.1098/rspb.2014.2898
  21. Guz J, Gackowski D, Foksinski M, et al (2013). Comparison of oxidative stress/DNA damage in semen and blood of fertile and infertile men. PLoS One, 8, 68490. https://doi.org/10.1371/journal.pone.0068490
  22. Hargreave M, Jensen A, Toender A, et al (2013). Fertility treatment and childhood cancer risk: a systematic metaanalysis. Fertil Steril, 100, 150-61 https://doi.org/10.1016/j.fertnstert.2013.03.017
  23. Hoffmann D, Hoffmann I, El-Bayoumy K (2001). The less harmful cigarette: a controversial issue. A tribute to Ernst L. Wynder. Chem Res Toxicol, 14, 767-90. https://doi.org/10.1021/tx000260u
  24. Jones KT (2008). Meiosis in oocytes: predisposition to aneuploidy and its increased incidence with age. Human Reproduction Update, 14,143-58. https://doi.org/10.1093/humupd/dmm043
  25. Khasky AD, Smith JC (1999). Stress, relaxation states and creativity. Percept Mot Skills, 88, 409-16. https://doi.org/10.2466/pms.1999.88.2.409
  26. Kishlay K , Deepika D, Amar S , et al (2012). Predictive value of DNA integrity analysis in idiopathic recurrent pregnancy loss following spontaneous conception. J Assist Reprod Genet, 29, 861-67. https://doi.org/10.1007/s10815-012-9801-3
  27. Kong A, Frigge ML, Masson G, et al (2012). Rate of de novo mutations and theimportance of father's age to disease risk. Nature, 488, 471-5. https://doi.org/10.1038/nature11396
  28. Kravitz AV, Tomasi D, LeBlanc KH, et al (2015). Corticostriatal circuits: Novel therapeutic targets for substance use disorders. Brain Res, 2, 83-8.
  29. Kumar K, Deka D, Singh A, Chattopadhyay P, Dada R (2012). Expression pattern of PRM2, HSP90 and WNT5A in male partners of couples experiencing idiopathic recurrent miscarriages. J Genet, 91, 363-6. https://doi.org/10.1007/s12041-012-0200-4
  30. Kumar SB, Chawla B, Bisht S, et al (2015). Tobacco use increases oxidative dna damage in sperm - possible etiology of childhood cancer. Asian Pac J Cancer Prev, 16, 6967-72. https://doi.org/10.7314/APJCP.2015.16.16.6967
  31. Kumar SB, Rashmi Y, Raj Kumar Y, et al (2015). Telomerase activity and cellular aging might be positively modified by a yoga-based lifestyle intervention. J Altern Complement Med, 21, 370-72. https://doi.org/10.1089/acm.2014.0298
  32. Lappas M, Hiden U, Desoye G, et al (2011). The role of oxidative stress in the pathophysiology of gestational diabetes mellitus. Antioxid Redox Signal, 15, 3061-100. https://doi.org/10.1089/ars.2010.3765
  33. Lee WC and Hsiao CK (1996). Alternative summary indices for the receiver operating characteristic curve. Epidemiol, 7, 605-11. https://doi.org/10.1097/00001648-199611000-00007
  34. Liu RZ, Gao JC, Zhang HG, et al (2010). Seminal plasma zinc level may be associated with the effect of cigarette smoking on sperm parameters. J Int Med Res, 38, 923-8. https://doi.org/10.1177/147323001003800318
  35. Lopes S, Jurisicova A, Sun JG, et al (1998). Sperm deoxyribonucleic acid fragmentation is increased in poorquality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril, 69, 528-32 https://doi.org/10.1016/S0015-0282(97)00536-0
  36. Malathi A, Damodaran A (1999). Stress due to exams in medical students- role of yoga. Indian J Physiol Pharmacol, 43, 218-24.
  37. Mishra SS, Kumar R, Malhotra N, et al (2013). Expression of PARP1 in primary infertility patients and correlation with DNA fragmentation index a pilot study. J Anat Soc India, 62, 98-104. https://doi.org/10.1016/j.jasi.2013.12.005
  38. Mishra SS, Kumar R, Malhotra N, et al (2016). Mild oxidative stress is beneficial for sperm telomere length maintenance. World J Methodol, 6, 163-70. https://doi.org/10.5662/wjm.v6.i2.163
  39. Mittal D, Yadav RK, Sihota R, et al (2015). Impact of meditation and yoga based intervention on quality of life and stress markers in glaucoma patients: a prospective randomized controlled study. Int Glaucoma Review, 16, 237.
  40. Mohanty K, Faiq MA, Dada R, et al (2016). Yoga and meditation based intervention alters global genome expression profile in primary open angle glaucoma (POAG): Role in oxidative stress management. JISANH, 3: Special Issue for Paris Redox.
  41. Moizs M, Bajzik G, Lelovics Z, et al (2013). First result of differentiated communication-to smokers and non-smokersin order to increase the voluntary participation rate in lung screening. BMC Public Health, 13, 914. https://doi.org/10.1186/1471-2458-13-914
  42. Pham-Huy LA, He H and Pham-Huy C (2008). Free radicals, antioxidants in disease and health. Int J Biomedical Sci, 4, 89-96.
  43. Purkayastha A, Sharma N, Pathak A, et al (2016). An extremely rare case of metastatic retinoblastoma of parotids presenting as a massive swelling in a child. Translational Pediatrics, 5, 90-4. https://doi.org/10.21037/tp.2016.02.01
  44. Shamsi MB, Venkatesh S, Kumar R (2010). Antioxidant levels in blood and seminal plasma and their impact on sperm parameters in infertile men. Indian J Biochem Biophys, 47, 38-43.
  45. Tolahunase M, Bisht S, Sagar R, et al (2016). Effect of yoga on quality of life and seminal quality in male infertility patients with major depressive disorder (mdd) (2016) Randomized controlled trial. Paper presented at: 41st American Society of Andrology Annual Meeting; New Orleans, Louisiana.
  46. Thilagavathi J, Kumar M, Mishra SS (2013a). Analysis of sperm telomere length in men with idiopathic infertility. Arch Gynecol Obstet, 287, 803-7. https://doi.org/10.1007/s00404-012-2632-8
  47. Thilagavathi J, Mishra SS, Kumar M (2013b) Analysis of telomere length in couples experiencing idiopathic recurrent pregnancy loss. J Assist Reprod Genet, 30, 793-8. https://doi.org/10.1007/s10815-013-9993-1
  48. Tremellen K.(2008)Oxidative stress and male infertility-a clinical perspective. Human Reproduct Update, 14, 243-58. https://doi.org/10.1093/humupd/dmn004
  49. U.S. Department of Health and Human Services: Reducing tobacco use: a report of the surgeon general. Atlanta, GA: U.S. department of health and human services, centers for disease control and prevention, national center for chronic disease prevention and health promotion, office on smoking and health; 2000.
  50. Venkatesh S, Deecaraman M, Kumar R, et al (2009). Sperm DNA damage & oxidative stress in recurrent spontaneous abortion (RSA). Indian J Med Res, 129, 127-37.
  51. Venkatesh S, Singh A, Shamsi MB, et al (2011). Clinical significance of sperm DNA damage threshold value in the assessment of male infertility. Reprod Sci, 18, 1005-13. https://doi.org/10.1177/1933719111401662
  52. Von Stetina JR, Orr-Weaver T L. (2011). Developmental Control of Oocyte Maturation and Egg Activation in Metazoan Models. Cold Spring Harbor Perspectives Biology, 3, 5553 https://doi.org/10.1101/cshperspect.a005553
  53. Ward E, DeSantis C, Robbins A, et al (2014). Childhood and adolescent cancer statistics. CA Cancer J Clin, 64, 83-103. https://doi.org/10.3322/caac.21219
  54. Wiener-Megnazi Z, Auslender R, Dirnfeld M (2012). Advanced paternal age and reproductive outcome. Asian J Androl, 14, 69-76. https://doi.org/10.1038/aja.2011.69
  55. World Health Organization (1997). Tobacco or Health: A Global Status Report. Geneva:WHO, 10-48.
  56. Yadav RK, Magan D, Mehta N, et al (2012). Efficacy of a shortterm yoga-based lifestyle intervention in reducing stress and inflammation: preliminary results. J Altern Complement Med, 18, 662-7. https://doi.org/10.1089/acm.2011.0265
  57. Zara S (2005). The Guide to Community Preventive Services. New York, NY: Oxford University Press.