Folliculogenesis, inheritance, and mitochondrial diseases: a review article

authors:

avatar Akram Alizadeh , avatar Raheleh Naserian Moghadam , avatar Samira Sistani , avatar Raghayeh Hosseini Kia , avatar Sajad Oubari , avatar Farhad Obari , *


how to cite: Alizadeh A, Naserian Moghadam R, Sistani S, Hosseini Kia R, Oubari S, et al. Folliculogenesis, inheritance, and mitochondrial diseases: a review article. koomesh. 2023;25(6):e152855. 

Abstract

Introduction: Oocyte mitochondria are unique organs that are established from the basal population in the primordial bud. Oocytes are formed in the mammalian ovary after birth, during folliculogenesis, and have a fundamental role in energy production and cellular processes, including metabolism and signal transduction. Each mitochondrion contains 5-10 copies of the mitochondrial genome, therefore each cell contains several hundreds to thousands of mitochondrial genomes. In most organisms, including humans, the father's mitochondria, which enter the ovule through the sperm, are never transmitted to the children, so the inheritance pattern of the mitochondrial genome has a maternal pattern. Materials and Methods: Related articles from WILY ONLINE LIBRARY, ISI Web of Science, Link Springer, ScienceDirect, and Pubmed databases from 1963 to 2022 in which inheritance patterns, maternal inheritance, mitochondria, and mitochondrial diseases were searched and studied. Results: The findings indicate that the removal of paternal mitochondria and mechanisms related to ubiquinone, proteasome, and autophagy cause the destruction of paternal mitochondria and prevent the transfer of the mitochondrial genome. Mitochondrial diseases are mitochondrial changes in adult tissues and the resulting differences in clinical manifestations, so the mediating mechanisms in the relationship between genetic variation and human diseases are still a mystery, mainly due to problems in modeling. Conclusion: Mitochondrial diseases caused by mutation of the mitochondrial genome in the maternal pattern caused by mutations in mitochondria are seen in MELAS, MERRF, NARP syndromes, Leigh, oligosymptomatic syndromes, diabetes mellitus, cardiomyopathy, myoglobinuria, and sensory-neural deafness. Therefore, the recognition of this mutation can be the target of gene therapy in the future.

References

  • 1.

    Pepling ME, Spradling AC. Female mouse germ cells form synchronously dividing cysts. Development 1998; 125: 3323-3328.

  • 2.

    Collado-Fernandez E, Picton HM, Re D. Metabolism throughout follicle and oocyte development in mammals. Int J Dev Biol 2012; 56: 799-808.

  • 3.

    Findlay JK, Hutt KJ, Hickey M, Anderson RA. How is the number of primordial follicles in the ovarian reserve established? Biol Reprod 2015; 1: 93-97.

  • 4.

    Wear HM, McPike MJ, Watanabe KH. From primordial germ cells to primordial follicles: A review and visual representation of early ovarian development in mice. J Ovarian Res 2016; 9: 1-11.

  • 5.

    Pepling ME. Follicular assembly: Mechanisms of action. Reproduction. 2012; 139: 143-149.

  • 6.

    Jamnongjit M, Hammes SR. Oocyte maturation: The coming of age of a germ cell. Semin Reprod Med 2005; 23: 234-241.

  • 7.

    Baker TG. A quantitative and cytological study of germ cells in human varies. Proc R Soc London Ser B, Biol Sci 1963; 158: 417-433.

  • 8.

    Karimi S, Alizadeh A, Tabibi N, Ghasemi S. Increase the efficiency of MKN45 cell line to CD44 editing by CRISPR-Cas9: a hypothesis about P53 suppression in Gene editing. J Appl Biotechnol Rep 2022; 9: 453-457. (Persian).

  • 9.

    Van Blerkom J. Mitochondria in human oogenesis and preimplantation embryogenesis: Engines of metabolism, ionic regulation and developmental competence. Reproduction 2004; 128: 269-280.

  • 10.

    Zhang X, Wu XQ, Lu S, Guo YL, Ma X. Deficit of mitochondria-derived ATP during oxidative stress impairs mouseMII oocyte spindles. Cell Res 2006; 841: 16-850.

  • 11.

    Arab S, Alizadeh A, Asgharzade S. Tumor-resident adenosine-producing mesenchymal stem cells as a potential target for cancer treatment. Clin Experiment Med 2021; 21: 205-213. (Persian).

  • 12.

    Barzilai A, Yamamoto KI. DNA damage responses to oxidative stress. DNA Repair (Amst) 2004; 3: 1109-1115.

  • 13.

    Shakeri R, Kheirollahi A, Davoodi J. Apaf-1: Regulation and function in cell death. Biochimie 2017; 135: 111-125.

  • 14.

    Ghara AR, Ghadi FE, Hossaini SH, Alizadeh A, Mirmahmoudi R. Antioxidant and antidiabetic effect of capparis decidua edgew (Forssk.) extract on liver and pancreas of streptozotocin-induced diabetic rats. J Appl Biotechnol Rep 2021; 8: 76-82. (Persian).

  • 15.

    Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A. Mitochondrial functionality in reproduction: From gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update 2009; 15: 553-572.

  • 16.

    Chiaratti MR, Garcia BM, Carvalho KF, Macabelli CH, da Silva Ribeiro FK, Zangirolamo AF, et al. Oocyte mitochondria: Role on fertility and disease transmission. Anim Reprod 2018; 15: 231-238.

  • 17.

    Ramalho-Santos J, Amaral S. Mitochondria and mammalian reproduction. Mol Cell Endocrinol 2013; 379: 74-84.

  • 18.

    Bradley J, Swann K. Mitochondria and lipid metabolism in mammalian oocytes and early embryos. Int J Dev Biol 2019; 63: 93-103.

  • 19.

    Kidder GM, Mhawi AA. Gap junctions and ovarian folliculogenesis. Reproduction 2002; 123: 613-620.

  • 20.

    Dumollard R, Carroll J, Duchen MR, Campbell K, Swann K.Mitochondrial function and redox state in mammalian embryos. Semin Cell Dev Biol 2009; 20: 346-353.

  • 21.

    Brinster RL, Harstad H. Energy metabolism in primordial germ cells of the mouse. Exp Cell Res 1977; 109: 111-117.

  • 22.

    Cinco R, Digman MA, Gratton E, Luderer U. Spatial characterization of bioenergetics and metabolism of primordial to Preovulatory follicles in whole ex vivo murine ovary. Biol Reprod 2016; 95: 129-129.

  • 23.

    Dumollard R, Campbell K, Halet G, Carroll J, Swann K. Regulation of cytosolic and mitochondrial ATP levels in mouse eggs and zygotes. Dev Biol 2008; 316: 431-440.

  • 24.

    Dunning KR, Akison LK, Russell DL, Norman RJ, Robker RL. Increased Beta-oxidation and improved oocyte developmental competence in response to L-carnitine during ovarian in vitro follicle development in mice. Biol Reprod 2011; 85: 548-555.

  • 25.

    Dunning KR, Cashman K, Russell DL, Thompson JG, Norman RJ, Robker RL. Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Biol Reprod 2010; 83: 909-918.

  • 26.

    Malott KF, Luderer U. Toxicant effects on mammalian oocyct mitochondria. Biol Reprod 2021; 104: 784-793.

  • 27.

    Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 2011; 11: 797-813.

  • 28.

    Wang LY, Wang DH, Zou XY, Xu CM. Mitochondrial functions on oocytes and preimplantation embryos. J Zhejiang Univ Sci B 2009; 10: 483-492.

  • 29.

    Al-Zubaidi U, Liu J, Cinar O, Robker RL, Adhikari D, Carroll J. The spatio-temporal dynamics of mitochondrial membrane potential during oocyte maturation. Mol Hum Reprod 2019; 25: 695-705.

  • 30.

    Cotterill M, Harris SE, Fernandez EC, Lu J, Huntriss JD, Campbell BK, Picton HM. The activity and copy number of mitochondrial DNA in ovine oocytes throughout oogenesis in vivo and during oocyte maturation in vitro. Mol Hum Reprod 2013; 19: 444-450.

  • 31.

    Roth Z. Symposium review: Reduction in oocyte developmental competence by stress is associated with alterations in mitochondrial function. J Dairy Sci 2018; 101: 3642-3654.

  • 32.

    Hosseinikia R, Nikbakht MR, Moghadam AA, Tajehmiri A, Hosseinikia M, Oubari F, et al. Molecular and cellular interactions of allogenic and autologus mesenchymal stem cells with innate and acquired immunity and their role in regenerative medicine. Int J Hematol Oncol Stem Cell Res 2017; 11: 63.

  • 33.

    Nachvak SM, Hosseinikia M, Abdollahzad H, Pasdar Y, Oubari F, Hosseinikia R, Shabanpur M. Pattern of kebab intake as a potential carcinogenic risk factor in adult of Kermanshah , Iran: 2015. Int J Hematol Oncol Stem Cell Res 2018; 12: 23. (Persian).

  • 34.

    Hosseinikia M, Oubari F, Hosseinkia R, Tabeshfar Z, Salehi MG, Mousavian Z, et al. Quercetin supplementation in non-alcoholic fatty liver disease A randomized, double-blind, placebo-controlled clinical trial. Nutr Food Sci 2020; 50: 1279-1293. (Persian)##https://doi.org/10.1108/NFS-10-2019-0321.

  • 35.

    Pasdar Y, Oubari F, Nikougoftar Zarif M, Abbasi M, Pourmahmoudi A, Hosseinikia M. Effects of quercetin supplementation on hematological parameters in non-alcoholic fatty liver disease: a randomized, double-blind, placebo-controlled pilot study. Clin Nutr Res 2020; 9: 11-19.

  • 36.

    Abbasi E, Vafaei SA, Naseri N, Darini A, Azandaryani M, Kian Ara F, Mirzaei F. Protective effects of cerium oxide nanoparticles in non-alcoholic fatty liver disease (NAFLD) and carbon tetrachloride-induced liver damage in rats: Study on intestine and liver. Metabol Open 2021; 12: 100151. (Persian).

  • 37.

    Nikbakht MR, Nikougoftar Zarif M, Oubari F, Mansouri K, Hosseinikia R, Hosseinikia M, Tajeh miri A. Mesenchymal stem cells transplantation: immunobiology, therapeutic applications and challenges- review article. SJKU 2015; 20: 113-139. (Persian).

  • 38.

    Morvati S. Inheritance in mitochondrial genome and related diseases. Sci J Med Organiz Islamic Repub Iran 2010; 3: 314-325. (Persian).

  • 39.

    Schapira AH. Mitochondrial disease. Lancet 2006; 368: 70-82.

  • 40.

    Taanman JW, Muddle JR, Muntau AC. Mitochondrial DNA depletion can be prevented by dGMP and dAMP supplementation in a resting culture of deoxyguanosine kinase-deficient fi broblasts. Hum Mol Genet 2003; 12: 1839-1845.

  • 41.

    Morovvati S, Modarresi M, Habibi G, Kiarudi Y, Karami A, Peyvandi AA. Sequence analysis of mitochondrial DNA hypervariable regions: an approach to personal identification. Arch Med Res 2007; 38: 345-349.

  • 42.

    Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G. Ubiquitin tag for sperm mitochondria. Nature 1999; 402: 371-372.

  • 43.

    Sutovsky P, Van Leyen K, McCauley T, Day BN, Sutovsky M. Degradation of paternal mitochondria after fertilization: implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance. Reprod Biomed Online 2004; 8: 24-33.

  • 44.

    St John J, Sakkas D, Dimitriadi K, Barnes A, Maclin V, Ramey J, et al. Failure of elimination of paternal mitochondrial DNA in abnormal embryos. Lancet 2000; 355: 200.

  • 45.

    Nussbaum RL, McInnes RR, Willard HF. Thompson and Thompson Genetics in Medicine. 7th ed. Philadelphia: Saunders Elsevier. 2007; 381-387.##https://doi.org/10.1016/B978-1-4160-3080-5.50020-1.

  • 46.

    Poulton J, Morten KJ, Weber K, Brown GK, Bindoff L. "Are duplications of mitochondrial DNA characteristic of Kearns-Sayre syndrome?". Hum Mol Genet 1994; 3: 947-951.

  • 47.

    Chinnery PF, Howell N, Lightowlers RN, Turnbull DM. MELAS and MERRF. The relationship between maternal mutation load and the frequency of clinically aff ected off spring. Brain 1998; 121: 1889-1894.

  • 48.

    Holt IJ, Harding AE, Morgan-Hughes JA. Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature 1988; 331: 717-719.

  • 49.

    Servidei S. Mitochondrial encephalomyopathies: gene mutation. Neuromuscul Disord 2004; 14: 107-116.

  • 50.

    Majamaa K, Moilanen JS, Uimonen S, Remes AM, Salmela PI, Krpp M, et al. Epidemiology of A3243G, the mutation for mitochondrial encephalomyopathy, lactic acidosis, and strokelike episodes: prevalence of the mutation in an adult population. Am J Hum Genet 1998; 63: 447-454.

  • 51.

    Morovvati S, Nakagawa M, Sato Y, Hamada K, Higuchi I, Osame M. Phenotypes and mitochondrial DNA substitutions in families with A3243G mutation. Acta Neurol Scand. 2002 Aug; 106(2): 104-8.

  • 52.

    McFarland R, Schaefer AM, Gardner JL, Lynn S, Hayes CM, Barron MJ, et al. Familial myopathy: new insights into the T14709C mitochondrial tRNA mutation. Ann Neurol 2004; 55: 478-484.

  • 53.

    Cock HR, Cooper J, Schapira A. Nuclear complementation in Leber's hereditary optic neuropathy. Neurology 1995; 45: 294.

  • 54.

    Man PY, Griffi ths PG, Brown DT, Howell N, Turnbull DM, Chinnery PF. The epidemiology of Leber hereditary optic neuropathy in the North East of England. Am J Hum Genet 2003; 72: 333-339.

  • 55.

    Rak M, Tetaud E, Duvezin-Caubet S, Ezkurdia N, Bietenhader M, Rytka J, di Rago JP. "A yeast model of the neurogenic ataxia retinitis pigmentosa (NARP) T8993G mutation in the mitochondrial ATP synthase-6 gene". J Biol Chem 2007; 282: 34039-34047.

  • 56.

    Parfait B, de Lonlay P, von Kleist-Retzow JC, Cormier-Daire V, Chrtien D, Rtig A, et al. The neurogenic weakness, ataxia and retinitis pigmentosa (NARP) syndrome mtDNA mutation (T8993G) triggers muscle ATPase deficiency and hypocitrullinaemia. Eur J Pediatr1999; 158: 55-58.

  • 57.

    "Leigh syndrome". Genetics Home Reference. National Institute of Health. 23 September 2013. Retrieved 16 October 2013.

  • 58.

    Tranchant C, Anheim M. Movement disorders in mitochondrial diseases. Revue Neurologique 2016.

  • 59.

    Puschmann A. New genes causing hereditary parkinson's disease or parkinsonism. Curr Neurol Neuros Rep 2017; 17: 66.

  • 60.

    Quadri M, Mandemakers W, Grochowska MM, Masius R, Geut H, Fabrizio E, et al. LRP10 genetic variants in familial Parkinson's disease and dementia with Lewy bodies: a genome-wide linkage and sequencing study. The Lancet Neurol 2018; 17: 597-608.

  • 61.

    Chen Y, Cen Z, Zheng X, Pan Q, Chen X, Zhu L, et al. LRP10 in autosomal-dominant Parkinson's disease. Movement Disord 2019; 34: 912-916.

  • 62.

    Stoker TB, Torsney KM, Barker RA. Pathological mechanisms and clinical aspects of GBA1 mutation-associated Parkinson's disease. In Stoker TB, Greenland JC (eds.). Parkinson's Disease: Pathogenesis and clinical aspects. Brisbane.

  • 63.

    Davie CA. A review of Parkinson's disease. Br Med Bull 2008; 86: 109-127.

  • 64.

    Kalia LV, Lang AE. Parkinson's disease. Lancet 2015; 386: 896-912.

  • 65.

    Stumvoll M, Gan-Or Z, Dion PA, Rouleau GA. Genetic perspective on the role of the autophagy-lysosome pathway in Parkinson disease. Autophagy 2015; 11: 1443-1457.

  • 66.

    Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 2004; 429: 417-423.

  • 67.

    Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, et al. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 2005; 308: 1909-1911.

  • 68.

    Lauri A, Pompilio G, Capogrossi MC. Capogrossi. The mitochondrial genome in aging and senescence. Ageing Res Rev 2014; 18: 1-15.

  • 69.

    Brandon M, Baldi PA, Wallace DC. Mitochondrial mutations in cancer. Oncogene 2006; 25: 4647-4662.

  • 70.

    Petros JA, Baumann AK, Ruiz-Pesini E, Amin MB, Sun CQ, Hall J, et al. mtDNA mutations increase tumorigenicity in prostatecancer. Proc Natl Acad Sci USA 2005; 102: 719-724.

  • 71.

    Nakamura M, Nakano S, Goto Y, et al. A novel point mutation in the mitochondrial tRNA(Ser(UCN)) gene detected in a family with MERRF/MELAS overlap syndrome. Biochem Biophys Res Commun 1995; 214: 86-93.

  • 72.

    Mancuso M, Filosto M, Mootha VK, Rocchi A, Pistolesi S, Murri L, et al. A novel mitochondrial tRNAPhe mutation causes MERRF syndrome. Neurology 2004; 62: 2119-2121.

  • 73.

    Millar N, Newman N. Walsh & Hoyt's clinical neuro-ophthalmology, The Essentials (5th ed). 1999.

  • 74.

    Houshmand M, Panahi MS, Hosseini BN, Dorraj GH, Tabassi AR. Investigation on mtDNA deletions and twinkle gene mutation (G1423C) in Iranian patients with chronic progressive external opthalmoplagia. Neurol India 2006; 54: 182-185.

  • 75.

    Zeviani M, Di Donauto S. Mitochondrial disorders. Brain 2004; 127: 2153-2172.

  • 76.

    Copeland WC. Inherited mitochondrial diseases of DNA replication. Ann Rev Medi 2008; 59: 131-146.

  • 77.

    Van Goethem G, Dermaut B, Lfgren A, Martin JJ, Van Broeckhoven C. Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nature Genetics 2001; 28: 211-212.

  • 78.

    Pearson HA, Lobel JS, Kocoshis SA, Naiman JL, Windmiller J, Lammi AT, et al. A new syndrome of refractory sideroblastic anemia with vacuolization of marrow precursors and exocrine pancreatic dysfunction. J Pediatric 1979; 95: 976-984.

  • 79.

    Rotig A, Colonna M, Bonnefont JP, Blanche S, Fischer A, Saudubray JM, Munnich A. Mitochondrial DNA deletion in Pearson's marrow/pancreas syndrome. Lancet 1989; 1: 902-903.