Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content

FASEB Journal

Volumn 27, Issue 10, 2013, Pages 4226-4243

  Fullston, Tod ^a   Teague, E Maria C Ohlsson ^a   Palmer, Nicole O ^a   Deblasio, Miles J ^a   Mitchell, Megan ^a   Corbett, Mark ^a   Print, Cristin G ^b   Owens, Julie A ^a   Lane, Michelle ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c Repromed   (Australia)

Author keywords

DNA damage; Epigenetic alteration; Methylation; Nongenetic transmission; ROS

Indexed keywords

CELL DNA; DLT28D2 PROTEIN; FATTY ACID; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HIGH MOBILITY GROUP B1 PROTEIN; INSULIN; LEPTIN; LRRTM3 PROTEIN; MESSENGER RNA; MICRORNA; PROTEIN; SMARCE1 PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; REACTIVE OXYGEN METABOLITE; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DISEASE TRANSMISSION; DNA DAMAGE; DNA METHYLATION; EMBRYO DEVELOPMENT; FATTY ACID BLOOD LEVEL; GERM CELL; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; IMPAIRED GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; LIPID DIET; MALE; MALE FERTILITY; MATING; METABOLIC DISORDER; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OBESITY; ORGAN WEIGHT; PATERNAL OBESITY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RETROPERITONEAL FAT; SPERM; TESTIS; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; C57BL MOUSE; ENERGY METABOLISM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GLUCOSE TOLERANCE TEST; INSULIN RESISTANCE; METABOLISM; PHYSIOLOGY; SEX DIFFERENCE; SPERMATOZOON;

MUS;

ANIMALS; ENERGY METABOLISM; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE TOLERANCE TEST; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; OBESITY; REACTIVE OXYGEN SPECIES; SEX FACTORS; SPERMATOZOA; TESTIS; TRANSCRIPTOME;

EID: 84885151895     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-224048     Document Type: Article

References (87)

1. Begg, S., Vos, T., Barker, B., Stevenson, C, Stanley, L., and Lopez, A. D. (2007) The Burden of Disease and Injury in Australia 2003, Australian Institute of Health and Welfare, Canberra, Australia
2. Nguyen, D. M., and El-Serag, H. B. (2010) The epidemiology of obesity. Gastroenterol. Clin. North Am. 39, 1-7
3. Fall, C. H. (2011) Evidence for the intra-uterine programming of adiposity in later life. Ann. Hum. Biol. 38, 410-428
4. Dunn, G. A, and Bale, T. L. (2009) Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 150, 4999-5009
5. Dunn, G. A, and Bale, T. L. (2011) Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152, 2228-2236
6. Ng, S. F., Lin, R. C., Laybutt, D. R., Barres, R., Owens, J. A, and Morris, M. J. (2010) Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467, 963-966
7. Youngson, N. A, and Whitelaw, E. (2011) The effects of acquired paternal obesity on the next generation. Asian J. Androl. 13, 195-196
8. Danielzik, S., Langnase, K., Mast, M., Spethmann, C., and Muller, M. J. (2002) Impact of parental BMI on the manifestation of overweight 5-7-year old children. Eur. J. Nutr. 41, 132-138
9. Li, L., Law, C., Lo Conte, R., and Power, C. (2009) Intergenerational influences on childhood body mass index: the effect of parental body mass index trajectories. Am. J. Clin. Nutr. 89, 551-557
10. Whitaker, K. L., Jarvis, M. J., Beeken, R. J., Boniface, D., and Wardle, J. (2010) Comparing maternal and paternal intergenerational transmission of obesity risk in a large population-based sample. Am. J. Clin. Nutr. 91, 1560-1567
11. Freeman, E., Fletcher, R., Collins, C. E., Morgan, P. J., and Callister, R. (2012). Preventing and treating childhood obesity: time to target fathers. Int. J. Obes. (Lond.) 36, 12-15
12. Krawetz, S. A. (2005) Paternal contribution: new insights and future challenges. Nat. Rev. Genet. 6, 633-642
13. Bhat, G. K., Sea, T. L., Olatinwo, M. O., Simorangkir, D., Ford, B. D., and Mann, D. R. (2006) Influence of a leptin deficiency on testicular morphology, germ cell apoptosis, and expression levels of apoptosis-related genes in the mouse. J. Androl. 27, 302-310
14. Ghanayem, B. I., Bai, R., Kissling, G. E., Travlos, G., and Hoffler, U. (2010) Diet-induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity. Biol. Reprod. 82, 96-104
15. Palmer, N. O., Fullston, T., Mitchell, M., Setchell, B. P., and Lane, M. (2011). SIRT6 in mouse spermatogenesis is modulated by diet induced obesity. Reprod. Feritil. Dev. 23, 929-939
16. Jensen, T. K., Andersson, A. M., Jorgensen, N., Andersen, A. G., Petersen, J. H., and Skakkebaek, N. E. (2004) Body mass index in relation to semen quality and reproductive hormones among 1, 558 Danish men. Fertil. Steril. 82, 863-870
17. Fejes, I., Koloszar, S., Szollosi, J., Zavaczki, Z., and Pal, A. (2005) Is semen quality affected by male body fat distribution? Andrologia 37, 155-159
18. Magnusdottir, E. V., Thorsteinsson, T., Thorsteinsdottir, S., Heimisdottir, M., and Olafsdottir, K. (2005) Persistent organochlorines, sedentary occupation, obesity and human male subfertility. Hum. Reprod. 20, 208-215
19. Kort, H. I., Massey, J. B., Elsner, C. W., Mitchell-Leef, D., Witt, M. A., and Roudebush, W. E. (2006) Impact of body mass index values on sperm quantity and quality. J. Androl. 27, 450-452
20. Hammoud, A. O., Wilde, N., Gibson, M., Parks, A., and Meikle, A. W. (2008) Male obesity and alteration in sperm parameters. Fertil. Steril. 90, 2222-2225
21. Bakos, H. W., Henshaw, R. C., Mitchell, M., and Lane, M. (2011) Paternal body mass index is associated with decreased blastocyst development and reduced live birth rates following assisted reproductive technology. Fertil. Steril. 95, 1700-1704
22. Chavarro, J. E., Toth, T. L., Wright, D. L., Meeker, J. D., and Hauser, R. (2010) Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic. Fertil. Steril. 93, 2222-2231
23. MacDonald, A. A., Herbison, G. P., Showell, M., and Farquhar, C. M. (2010) The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis. Hum. Reprod. Update 16, 293-311
24. Tunc, O., Bakos, H. W., and Tremellen, K. (2011) Impact of body mass index on seminal oxidative stress. Andrologia 43, 121-128
25. Ostermeier, G. C., Goodrich, R. J., Moldenhauer, J. S., Diamond, M. P., and Krawetz, S. A. (2005) A suite of novel human spermatozoal RNAs. J. Androl. 26, 70-74
26. Van der Heijden, G. W., Derijck, A. A., Ramos, L., Giele, M., and De Boer, P. (2006) Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Dev. Biol. 298, 458-469
27. Lin, C. C., Wang, J. D., Hsieh, G. Y., Chang, Y. Y., and Chen, P. C. (2008) Increased risk of death with congenital anomalies in the offspring of male semiconductor workers. Int. J. Occup. Environ. Health 14, 112-116
28. Yauk, C., Polyzos, A., Rowan-Carroll, A., Somers, C. M., Van Schooten, F. J., Berndt, M. L., Pogribny, I. P., Koturbash, I., Williams, A., Douglas, G. R., and Kovalchuk, O. (2008) Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc. Natl. Acad. Sci. U. S. A. 105, 605-610
29. Grandjean, V., Gounon, P., Wagner, N., Martin, L., Bernex, F., Cuzin, F., and Rassoulzadegan, M. (2009) The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development 136, 3647-3655
30. Hammoud, S. S., Nix, D. A., Zhang, H., Purwar, J., and Cairns, B. R. (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478
31. Rassoulzadegan, M., and Cuzin, F. (2010) The making of an organ: RNA mediated developmental controls in mice. Organogenesis 6, 33-36
32. Ward, W. S. (2010) Function of sperm chromatin structural elements in fertilization and development. Mol. Hum. Reprod. 16, 30-36
33. El Hajj, N., Zechner, U., Schneider, E., Tresch, A., Hahn, T., Schorsch, M., and Haaf, T. (2011) Methylation status of imprinted genes and repetitive elements in sperm DNA from infertile males. Sex Dev. 5, 60-69
34. Liu, W. M., Pang, R. T., Chiu, P. C., Wong, B. P., Lee, K. F., and Yeung, W. S. (2012) Sperm-borne microRNA-34c is required for the first cleavage division in mouse. Proc. Natl. Acad. Sci. U. S. A. 109, 490-494
35. Marczylo, E. L., Amoako, A. A., Konje, J. C., Gant, T. W., and Marczylo, T. H. (2012) Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 7, 432-439
36. Guerrero-Bosagna, C., Settles, M., Lucker, B., and Skinner, M. K. (2010). Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 5
37. Bakos, H. W., Mitchell, M., Setchell, B. P., and Lane, M. (2011). The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int. J. Androl. 34, 402-410
38. Fullston, T., Palmer, N. O., Owens, J. A., Mitchell, M., and Lane, M. (2012) Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum. Reprod. 27, 1391-1400
39. Mitchell, M., Bakos, H. W., and Lane, M. (2011) Paternal diet-induced obesity impairs embryo development and implantation in the mouse. Fertil. Steril. 95, 1349-1353
40. Adiga, S. K., Upadhya, D., Kalthur, G., Bola Sadashiva, S. R., and Kumar, P. (2010) Transgenerational changes in somatic and germ line genetic integrity of first-generation offspring derived from the DNA damaged sperm. Fertil. Steril. 93, 2486-2490
41. De Blasio, M. J., Dodic, M., Jefferies, A. J., Moritz, K. M., and Owens, J. A. (2007) Maternal exposure to dexamethasone or cortisol in early pregnancy differentially alters insulin secretion and glucose homeostasis in adult male sheep offspring. Am. J. Physiol. Endocrinol. Metab. 293, E75-E82
42. Nasr-Esfahani, M. H., Aitken, J. R., and Johnson, M. H. (1990) Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109, 501-507
43. Lane, M., Maybach, J. M., and Gardner, D. K. (2002) Addition of ascorbate during cryopreservation stimulates subsequent embryo development. Hum. Reprod. 17, 2686-2693
44. Bakos, H. W., Mitchell, M., Setchell, B. P., and Lane, M. (2010). The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int. J. Androl. 34, 402-410
45. Irizarry, R. A., Bolstad, B. M., Collin, F., Cope, L. M., and Speed, T. P. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15
46. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., Hornik, K., Hothorn, T., Huber, W., Iacus, S., Irizarry, R., Leisch, F., Li, C., Maechler, M., Rossini, A. J., Sawitzki, G., Smith, C., Smyth, G., Tierney, L., Yang, J. Y., and Zhang, J. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80
47. Tunc, O., and Tremellen, K. (2009) Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J. Assist. Reprod. Genet. 26, 537-544
48. Gong, Z., and Muzumdar, R. H. (2012) Pancreatic function, type 2 diabetes, and metabolism in aging. Int. J. Endocrinol. 320482
49. Santulli, G., Lombardi, A., Sorriento, D., Anastasio, A., Formisano, P., Beguinot, F., Trimarco, B., Miele, C., and Iaccarino, G. (2012) Age-related impairment in insulin release: the essential role of beta (2)-adrenergic receptor. Diabetes 61, 692-701
50. Ogus, S., Ke, Y., Qiu, J., Wang, B., and Chehab, F. F. (2003) Hyperleptinemia precipitates diet-induced obesity in transgenic mice overexpressing leptin. Endocrinology 144, 2865-2869
51. Sun, K., Kusminski, C. M., and Scherer, P. E. (2011) Adipose tissue remodeling and obesity. J. Clin. Invest. 121, 2094-2101
52. Howie, G. J., Sloboda, D. M., Kamal, T., and Vickers, M. H. (2009). Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J. Physiol. 587, 905-915
53. Dunn, G. A., Morgan, C. P., and Bale, T. L. (2011) Sexspecificity in transgenerational epigenetic programming. Horm. Behav. 59, 290-295
54. Ostermeier, G. C., Miller, D., Huntriss, J. D., Diamond, M. P., and Krawetz, S. A. (2004) Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429, 154
55. Rassoulzadegan, M., Grandjean, V., Gounon, P., Vincent, S., and Cuzin, F. (2006) RNA-mediated non-Mendelian inheritance of an epigenetic change in the mouse. Nature 441, 469-474
56. Wagner, K. D., Wagner, N., Ghanbarian, H., Grandjean, V., Cuzin, F., and Rassoulzadegan, M. (2008) RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev. Cell 14, 962-969
57. Chong, M. M., Zhang, G., Cheloufi, S., Neubert, T. A., and Littman, D. R. (2010) Canonical and alternate functions of the microRNA biogenesis machinery. Genes Dev. 24, 1951-1960
58. Suh, N., Baehner, L., Moltzahn, F., Melton, C., Chen, J., and Blelloch, R. (2010) MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr. Biol. 20, 271-277
59. Smith, Z. D., Chan, M. M., Mikkelsen, T. S., Gu, H., Regev, A., and Meissner, A. (2012) A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339-344
60. Abu-Halima, M., Hammadeh, M., Schmitt, J., Leidinger, P., Meese, E., and Backes, C. (2013). Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertil. Steril. 99, 1249-1255
61. Morey, J. S., Ryan, J. C., and Van Dolah, F. M. (2006) Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol. Proced. Online 8, 175-193
62. Chen, Y., Gelfond, J. A., McManus, L. M., and Shireman, P. K. (2009) Reproducibility of quantitative RT-PCR array in miRNA expression profiling and comparison with microarray analysis. BMC Genomics 10, 407
63. Git, A., Dvinge, H., Salmon-Divon, M., Osborne, M., Hadfield, J., Bertone, P., and Caldas, C. (2010) Systematic comparison of microarray profiling, real-time PCR, and nextgeneration sequencing technologies for measuring differential microRNA expression. RNA 16, 991-1006
64. Pradervand, S., Weber, J., Lemoine, F., Consales, F., Dupasquier, M., Thomas, J., Richter, H., Kaessmann, H., Beaudoing, E., Hagenbüchle, O., and Harshman, K. (2010) Concordance among digital gene expression, microarrays, and qPCR when measuring differential expression of microRNAs. BioTechniques 48, 219-222
65. Palmer, N. O., Bakos, H. W., Owens, J. A., Setchell, B. P., and Lane, M. (2012) Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am. J. Physiol. Endocrinol. Metab. 302, E768-E780
66. Leibel, N. I., Baumann, E. E., Kocherginsky, M., and Rosenfield, R. L. (2006) Relationship of adolescent polycystic ovary syndrome to parental metabolic syndrome. J. Clin. Endocrinol. Metab. 91, 1275-1283
67. Grandjean, V., and Rassoulzadegan, M. (2009) Epigenetic inheritance of the sperm: an unexpected role of RNA. Gynecol. Obstet. Fertil. 37, 558-561
68. Yamauchi, Y., Shaman, J. A., and Ward, W. S. (2011) Nongenetic contributions of the sperm nucleus to embryonic development. Asian J. Androl. 13, 31-35
69. Piovan, C., Palmieri, D., Di Leva, G., Braccioli, L., Nuovo, G., Tortoreto, M., Sasso, M., Plantamura, I., Triulzi, T., Taccioli C, Tagliabue, E., Iorio, M. V., and Croce, C. M. (2012) Oncosuppressive role of p53-induced miR-205 in triple negative breast Cancer Mol. Oncol. 6, 458-472
70. Ma, J., Flemr, M., Stein, P., Berninger, P., Zavolan, M., Svoboda, P., and Schultz, R. M. (2010) MicroRNA activity is suppressed in mouse oocytes. Curr. Biol. 20, 265-270
71. Wang, Y., Medvid, R., Melton, C., Jaenisch, R., and Blelloch, R. (2007) DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat. Genet. 39, 380-385
72. Ning, H., Huang, Y. C., Banie, L., Hung, S., Li, L. C., Lue, T. F., and Lin, C. S. (2009) MicroRNA regulation of neuron-like differentiation of adipose tissue-derived stem cells. Differentiation 78, 253-259
73. Bedzhov, I., Liszewska, E., Kanzler, B., and Stemmler, M. P. (2012). Igf1r signaling is indispensable for preimplantation development and is activated via a novel function of E-cadherin. PLoS Genet. 8, e1002609
74. Mansfield, J. H., Harfe, B. D., Nissen, R., Obenauer, J., Chaudhuri, A., Farzan-Kashani, R., Zuker, M., Pasquinelli, A. E., Ruvkun, G., Sharp, P. A., Tabin, C. J., and McManus, M. T. (2004) MicroRNA-responsive 'sensor' transgenes uncover Hoxlike and other developmentally regulated patterns of vertebrate microRNA expression. Nat. Genet 36, 1079-1083
75. Yekta, S., Shih, I. H., and Bartel, D. P. (2004) MicroRNA-directed cleavage of HOXB8 mRNA. Science 304, 594-596
76. Hornstein, E., Mansfield, J. H., Yekta, S., Hu, J. K., McManus, M. T., Baskerville, S., Bartel, D. P., and Tabin, C. J. (2005) The microRNA miR-196 acts upstream of Hoxb8 and Shh in limb development. Nature 438, 671-674
77. Iimura, T., and Pourquie, O. (2007) Hox genes in time and space during vertebrate body formation. Dev. Growth Differ. 49, 265-275
78. Tripurani, S. K., Lee, K. B., Wee, G., Smith, G. W., and Yao, J. (2011) MicroRNA-196a regulates bovine newborn ovary homeobox gene (NOBOX) expression during early embryogenesis. BMC Dev. Biol. 11, 25
79. Madison-Villar, M. J., and Michalak, P. (2011) Misexpression of testicular microRNA in sterile Xenopus hybrids points to tetrapod-specific microRNAs associated with male fertility. J. Mol. Evol. 73, 316-324
80. Hulf, T., Sibbritt, T., Wiklund, E. D., Patterson, K., Stirzaker, C., Qu, W., Nair, S., Horvath, L. G., Armstrong, N. J., Kench, J. G., Sutherland, R. L., and Clark, S. J. (2013). Epigenetic-induced repression of microRNA-205 is associated with MED1 activation and a poorer prognosis in localized prostate cancer. Oncogene 32, 2891-2899
81. Palmer, N. O., Fullston, T., Mitchell, M., Setchell, B. P., and Lane, M. (2011) SIRT6 in mouse spermatogenesis is modulated by diet-induced obesity. Reprod. Fertil. Dev. 23, 929-939
82. Das, S., Bryan, K., Buckley, P. G., Piskareva, O., Foley, N., Ryan, J., Lynch, J., Creevey, L., Fay, J., Prenter, S., Koster, J., Van Sluis, P., Versteeg, R., Eggert, A., Schulte, J. H., Schramm, A, Mestdagh, P., Vandesompele, J., Speleman, F., and Stallings, R. L. (2013). Modulation of neuroblastoma disease pathogenesis by an extensive network of epigenetically regulated microRNAs. Oncogene 32, 2927-2936
83. Tanic, M., Zajac, M., Gomez-Lopez, G., Benitez, J., and Martinez-Delgado, B. (2012) Integration of BRCA1-mediated miRNA and mRNA profiles reveals microRNA regulation of TRAF2 and NF-kB pathway. Breast Cancer Res. Treat. 134, 41-51
84. Dar, A. A., Majid, S., De Semir, D., Nosrati, M., and Kashani-Sabet, M. (2011) miRNA-205 suppresses melanoma cell proliferation and induces senescence via regulation of E2F1 protein. J. Biol. Chem. 286, 16606-16614
85. Lin, T., Chao, C., Saito, S., Mazur, S. J., Appella, E., and Xu, Y (2005) p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat. Cell Biol. 7, 165-171
86. Abd El Naby, W. S., Hagos, T. H., Hossain, M. M., Salilew-Wondim, D., Rings, F., Cinar, M. U., Tholen, E., Looft, C, Schellander, K., Hoelker, M., and Tesfaye, D. (2013). Expression analysis of regulatory microRNAs in bovine cumulus oocyte complex and preimplantation embryos. Zygote 21, 31-51
87. Carone, B. R., Fauquier, L., Habib, N., Shea, J. M., Li, R., Bock, C., Li, C, Gu, H., Zamore, P. D., Meissner, A., Weng, Z., Hofmann, H. A., Friedman, N., and Rando, O. J. (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143, 1084-1096