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Regulatory Roles of Mitochondrial Ribosome in Lung Diseases and Single Cell Biology

  • Linlin Zhang
  • William Wang
  • Bijun Zhu
  • Xiangdong WangEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1038)

Abstract

The mitochondria have the most vital processes in eukaryotic cells to produce ATP composed of polypeptides that are produced via ribosomes, as oxidative phosphorylation. Initially, studies regarding human mitochondrial ribosomes were performed in the model system, bovine mitochondrial ribosome, to investigate how ribosomes are biosynthesized and evolved as well as what their structure and function are. Advances in X-ray crystallography have led to dramatic progresses in structural studies of the ribosome. In recent years, there has been a growing interest in the properties of the mitochondrial ribosome. Although one of its main functions is the production of ATP, it was also linked to multiple diseases. A key area that remains unexplored and requires investigation and exploration is how mitochondrial ribosomal RNA (mt-rRNA) variations can affect the mitochondrial ribosomes in developing disease. This review summarizes the structure, elements, functions, and regulatory roles in associated diseases. With the continuous development of technology, studies on the mechanism of mitochondrial ribosome related diseases are crucial, in order to identify methods of prevention and treatment of these disorders.

Keywords

Mitochondria Ribosome Element Function Structure Diseases Single cell 

Notes

Acknowledgments

The work was supported by Zhongshan Distinguished Professor Grant (XDW), The National Nature Science Foundation of China (91230204, 81270099, 81320108001, 81270131, 81300010), The Shanghai Committee of Science and Technology (12JC1402200, 12431900207, 11410708600, 14431905100), Operation funding of Shanghai Institute of Clinical Bioinformatics, Ministry of Education for Academic Special Science and Research Foundation for PhD Education (20130071110043), and National Key Research and Development Program (2016YFC0902400, 2017YFSF090207).

References

  1. 1.
    Korostelev A, Noller HF. The ribosome in focus: new structures bring new insights. Trends Biochem Sci. 2007;32:434–41. [PubMed: 17764954]CrossRefPubMedGoogle Scholar
  2. 2.
    Kakkar P, Mehrotra S, Viswanathan PN. Influence of antioxidants on the peroxidative swelling of mitochondria in vitro. Cell Biol Toxicol. 1998;14:313–21. [PubMed: 9808359]CrossRefPubMedGoogle Scholar
  3. 3.
    Kikuchi S, Ninomiya T, Kohno T, Kojima T, Tatsumi H. Cobalt inhibits motility of axonal mitochondria and induces axonal degeneration in cultured dorsal root ganglion cells of rat. Cell Biol Toxicol. 2017. https://doi.org/10.1007/s10565-017-9402-0. [PubMed: 28656345]
  4. 4.
    Greber BJ, Ban N. Structure and function of the mitochondrial ribosome. Annu Rev Biochem. 2016;85:103–32. [PubMed: 27023846]CrossRefPubMedGoogle Scholar
  5. 5.
    Kaushal PS, Sharma MR, Agrawal RK. The 55S mammalian mitochondrial ribosome and its tRNA-exit region. Biochimie. 2015;114:119–26. [PubMed: 25797916]CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Cavdar KE, Ranasinghe A, Burkhart W, Blackburn K, Koc H, Moseley A, Spremulli LL. A new face on apoptosis: death-associated protein 3 and CDPD9 are mitochondrial ribosomal proteins. FEBS Lett. 2001;492:166–70. [PubMed: 11248257]CrossRefGoogle Scholar
  7. 7.
    De SD, YT T, Amunts A, Fontanesi F, Barrientos A. Mitochondrial ribosome assembly in health and disease. Cell Cycle. 2015;14:2226–50. [PubMed: 26030272]CrossRefGoogle Scholar
  8. 8.
    Pietromonaco SF, Denslow ND, O’Brien TW. Proteins of mammalian mitochondrial ribosomes. Biochimie. 1991;73:827–36. [PubMed: 1764527]CrossRefPubMedGoogle Scholar
  9. 9.
    Brown A, Amunts A, Bai XC, Sugimoto Y, Edwards PC, Murshudov G, Scheres SH, Ramakrishnan V. Structure of the large ribosomal subunit from human mitochondria. Science. 2014;346:718–22. [PubMed: 25278503]CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Rackham O, Filipovska A. Supernumerary proteins of mitochondrial ribosomes. Biochim Biophys Acta. 1840;2014:1227–32. [PubMed: 23958563]Google Scholar
  11. 11.
    Sharma MR, Booth TM, Simpson L, Maslov DA, Agrawal RK. Structure of a mitochondrial ribosome with minimal RNA. Proc Natl Acad Sci U S A. 2009;106:9637–42. [PubMed: 19497863]CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Maayah ZH, Abdelhamid G, El-Kadi AO. Development of cellular hypertrophy by 8-hydroxyeicosatetraenoic acid in the human ventricular cardiomyocyte, RL-14 cell line, is implicated by MAPK and NF-κB. Cell Biol Toxicol. 2015;31:241–59. [PubMed: 26493311]CrossRefPubMedGoogle Scholar
  13. 13.
    O’Brien TW. Properties of human mitochondrial ribosomes. IUBMB Life. 2003;55:505–13. [PubMed: 14658756]CrossRefPubMedGoogle Scholar
  14. 14.
    van der Sluis EO, Bauerschmitt H, Becker T, Mielke T, Frauenfeld J, Berninghausen O, Neupert W, Herrmann JM, Beckmann R. Parallel structural evolution of mitochondrial ribosomes and OXPHOS complexes. Genome Biol Evol. 2015;7:1235–51. [PubMed: 25861818]CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Kramer G, Boehringer D, Ban N, Bukau B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat Struct Mol Biol. 2009;16:589–97. [PubMed: 19491936]CrossRefPubMedGoogle Scholar
  16. 16.
    Ganta KK, Mandal A, Chaubey B. Depolarization of mitochondrial membrane potential is the initial event in non-nucleoside reverse transcriptase inhibitor efavirenz induced cytotoxicity. Cell Biol Toxicol. 2017;33:69–82. [PubMed: 27639578]CrossRefPubMedGoogle Scholar
  17. 17.
    Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, Agrawal RK. Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell. 2003;115:97–108. [PubMed: 14532006]CrossRefPubMedGoogle Scholar
  18. 18.
    Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF. Crystal structure of the ribosome at 5.5 A resolution. Science. 2001;292:883–96. [PubMed: 11283358]CrossRefPubMedGoogle Scholar
  19. 19.
    Gabashvili IS, Agrawal RK, Spahn CM, Grassucci R, Svergun D, Frank J, Penczek P. Solution structure of the E. coli 70S ribosome at 11.5 A resolution. Cell. 2000;100:537–49. [PubMed: 10721991]CrossRefPubMedGoogle Scholar
  20. 20.
    Mears JA, Cannone JJ, Stagg SM, Gutell RR, Agrawal RK, Harvey SC. Modeling a minimal ribosome based on comparative sequence analysis. J Mol Biol. 2002;321:215–34. [PubMed: 12144780]CrossRefPubMedGoogle Scholar
  21. 21.
    Zerin T, Kim JS, Gil HW, Song HY, Hong SY. Effects of formaldehyde on mitochondrial dysfunction and apoptosis in SK-N-SH neuroblastoma cells. Cell Biol Toxicol. 2015;31:261–72. [PubMed: 26728267]CrossRefPubMedGoogle Scholar
  22. 22.
    Zhu LZ, Hou YJ, Zhao M, Yang MF, XT F, Sun JY, XY F, Shao LR, Zhang HF, Fan CD. Caudatin induces caspase-dependent apoptosis in human glioma cells with involvement of mitochondrial dysfunction and reactive oxygen species generation. Cell Biol Toxicol. 2016;32:333–45. [PubMed: 27184666]CrossRefPubMedGoogle Scholar
  23. 23.
    Fenton TR, Gout IT. Functions and regulation of the 70kDa ribosomal S6 kinases. Int J Biochem Cell Biol. 2011;43:47–59. [PubMed: 20932932]CrossRefPubMedGoogle Scholar
  24. 24.
    Gómez-Sagasti MT, Becerril JM, Epelde L, Alkorta I, Garbisu C. Early gene expression in Pseudomonas fluorescents exposed to a polymetallic solution. Cell Biol Toxicol. 2015;31:39–81. [PubMed: 25754557]CrossRefPubMedGoogle Scholar
  25. 25.
    Zhou Y, Zhang S, Dai C, Tang S, Yang X, Li D, Zhao K, Xiao X. Quinocetone triggered ER stress-induced autophagy via ATF6/DAPK1-modulated mAtg9a trafficking. Cell Biol Toxicol. 2016;32:141–52. [PubMed: 27085326]CrossRefPubMedGoogle Scholar
  26. 26.
    Khamzina L, Veilleux A, Bergeron S, Marette A. Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-1inked insulin resistance. Endocrinology. 2005;146:1473–81. [PubMed: 15604215]CrossRefPubMedGoogle Scholar
  27. 27.
    Qiao LY, Zhande R, Jetton TL, Zhou G, Sun XJ. In vivo phosphorylation of insulin receptor substrate 1 at serine 789 by a novel serine kinase in insulin resistant rodents. J Biol Chem. 2002;277:26530–9. [PubMed: 12006586]CrossRefPubMedGoogle Scholar
  28. 28.
    Tandon P, Gallo CA, Khatri S, Barger JF, Yepiskoposyan H, Plas DR. Requirement for ribosomal protein S6 kinase 1 to mediate glycolysis and apoptosis resistance induced by Pten deficiency. Proc Natl Acad Sci U S A. 2011;108:2361–5. [PubMed: 21262837]CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Kaarniranta K, Tokarz P, Koskela A, Paterno J, Blasiak J. Autophagy regulates death of retinal pigment epithelium cells in age-related macular degeneration. Cell Biol Toxicol. 2017;33:113–28. [PubMed: 27900566]CrossRefPubMedGoogle Scholar
  30. 30.
    Seo JB, Jung SR, Hille B, Koh DS, Extracellular ATP. Protects pancreatic duct epithelial cells from alcohol-induced damage through P2Y1 receptor-cAMP signal pathway. Cell Biol Toxicol. 2016;32:229–47. [PubMed: 27197531]CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Hwahng SH, Ki SH, Bae EJ, Kim HE, Kim SG. Role of adenosine monophosphate-activated protein kinase-p70 ribosomal S6 kinase-l pathway in repression of liver X receptor-alpha-dependent lipogenie gene induction and hepatic steatosis by a novel class of dithiolethiones. Hepatology. 2009;49:1913–25. [PubMed: 19378344]CrossRefPubMedGoogle Scholar
  32. 32.
    Zhang K, Zheng W, Zheng H, Wang C, Wang M, Li T, Wang X, Zhang L, Xiao S, Fei C, Xue F. Identification of oxidative stress and responsive genes of HepG2 cells exposed to quinocetone, and compared with its metabolites. Cell Biol Toxicol. 2014;30:313–29. [PubMed: 25223261]CrossRefPubMedGoogle Scholar
  33. 33.
    Graifer D, Karpova G. Roles of ribosomal proteins in the functioning of translational machinery of eukaryotes. Biochimie. 2015;109:1–17. [PubMed: 25433209]CrossRefPubMedGoogle Scholar
  34. 34.
    Teng T, Mercer CA, Hexley P, Thomas G, Fumagalli S. Loss of tumor suppressor RPL5/RPL11 does not induce cell cycle arrest but impedes proliferation due to reduced ribosome content and translation capacity. Mol Cell Biol. 2013;33:4660–71. [PubMed: 24061479]CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Kim HJ, Maiti P, Barrientos A. Mitochondrial ribosomes in cancer. Semin Cancer Biol. 2017. https://doi.org/10.1016/j.semcancer.2017.04.004. [PubMed: 28445780]
  36. 36.
    Kim WH, Shen H, Jung DW, Williams DR. Some leopards can change their spots: potential repositioning of stem cell reprogramming compounds as anti-cancer agents. Cell Biol Toxicol. 2016;32:157–68. [PubMed: 27156576]CrossRefPubMedGoogle Scholar
  37. 37.
    Dejure FR, Royla N, Herold S, Kalb J, Walz S, Ade CP, Mastrobuoni G, Vanselow JT, Schlosser A, Wolf E, Kempa S, Eilers M. The MYC mRNA 3′-UTR couple RNA polymerase II function to glutamine and ribonucleotide levels. EMBO J. 2017;36:1854–68. [PubMed: 28408437]CrossRefPubMedGoogle Scholar
  38. 38.
    Huun J, Lønning PE, Knappskog S. Effects of concomitant inactivation of p53 and pRb on response to doxorubicin treatment in breast cancer cell lines. Cell Death Discov. 2017;3:17026. [PubMed: 28580174]CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Boesewetter DE, Collier JL, Kim AM, Riley MR. Alterations of A549 lung cell gene expression in response to biochemical toxins. Cell Biol Toxicol. 2006;22:101–18. [PubMed: 16528450]CrossRefPubMedGoogle Scholar
  40. 40.
    Draptchinskaia N, Gustavsson P, Andersson B, Pettersson M, Willig TN, Dianzani I, Ball S, Tchernia G, Klar J, Matsson H, et al. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet. 1999;21:169–75. [PubMed: 9988267]CrossRefPubMedGoogle Scholar
  41. 41.
    Martin JB, Mariana C, Marcelo GK. Nuclear PKCi-ECT2-Rac1 and ribosome biogenesis: a novel Axis in lung tumorigenesis. Cancer Cell. 2017;31:167–9. [PubMed: 28196591]CrossRefGoogle Scholar
  42. 42.
    Hellwig B, Madjar K, Edlund K, Marchan R, Cadenas C, Heimes AS, Almstedt K, Lebrecht A, Sicking I, Battista MJ, et al. Epsin family member 3 and ribosome-related genes are associated with late metastasis in estrogen receptor-positive breast cancer and long-term survival in non-small cell lung cancer using a genome-wide identification and validation strategy. PLoS One. 2016;11:e0167585. [PubMed: 27926932]CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Minghetti M, Drieschner C, Bramaz N, Schug H, Schirmer K. A fish intestinal epithelial barrier model established from the rainbow trout (Oncorhynchus mykiss) cell line. RTgutGC Cell Biol Toxicol. 2017. https://doi.org/10.1007/s10565-017-9385-x. [PubMed: 28251411]
  44. 44.
    Matthay MA, Ware LB, Zimmerman GA. The acute respiratory distress syndrome. J Clin Invest. 2012;122:2731–40. [PubMed: 22850883]CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Chen C, Shi L, Li Y, Wang X, Yang S. Disease-specific dynamic biomarkers selected by integrating inflammatory mediators with clinical informatics in ARDS patients with severe pneumonia. Cell Biol Toxicol. 2016;32:169–84. [PubMed: 27095254]CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Stevens T. Functional and molecular heterogeneity of pulmonary endothelial cells. Proc Am Thorac Soc. 2011;8:453–7. [PubMed: 22052919]CrossRefPubMedGoogle Scholar
  47. 47.
    Lee SJ, Smith A, Guo L, Alastalo TP, Li M, Sawada H, Liu X, Chen ZH, Ifedigbo E, Jin Y, et al. Autophagic protein LC3B confers resistance against hypoxia-induced pulmonary hypertension. Am J Respir Crit Care Med. 2011;183:649–58. [PubMed: 20889906]CrossRefPubMedGoogle Scholar
  48. 48.
    Lippai M, Szatmári Z. Autophagy-from molecular mechanisms to clinical relevance. Cell Biol Toxicol. 2017;33:145–68. [PubMed: 27957648]CrossRefPubMedGoogle Scholar
  49. 49.
    Nowak K, Ratajczak-Wrona W, Garley M, Jabłońska E. The effect of ethanol and N-nitrosodimethylamine on the iNOS-dependent NO production in human neutrophils. Role of NF-κB. Xenobiotica. 2017;30:1–8. [PubMed: 28608757]CrossRefGoogle Scholar
  50. 50.
    Mondrinos MJ, Zhang T, Sun S, Kennedy PA, King DJ, Wolfson MR, Knight LC, Scalia R, Kilpatrick LE. Pulmonary endothelial protein kinase C-delta (PKCδ) regulates neutrophil migration in acute lung inflammation. Am J Pathol. 2014;184:200–13. [PubMed: 24211111]CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Chu MP, Kriangkum J, Venner CP, Sandhu I, Hewitt J, Belch AR, Pilarski LM. Addressing heterogeneity of individual blood cancers: the need for single cell analysis. Cell Biol Toxicol. 2017;33:83–97. [PubMed: 27761761]CrossRefPubMedGoogle Scholar
  52. 52.
    Wang W, Gao D, Wang X. Can single-cell RNA sequencing crack the mystery of cells? Cell Biol Toxicol. 2017. https://doi.org/10.1007/s10565-017-9404-y. [PubMed: 28733864]
  53. 53.
    Phiboonchaiyanan PP, Busaranon K, Ninsontia C, Chanvorachote P. Benzophenone-3 increases metastasis potential in lung cancer cells via epithelial to mesenchymal transition. Cell Biol Toxicol. 2017;33:251–61. [PubMed: 27796700]CrossRefPubMedGoogle Scholar
  54. 54.
    Ellsworth DL, Blackburn HL, Shriver CD, Rabizadeh S, Soon-Shiong P, Ellsworth RE. Single-cell sequencing and tumorigenesis: improved understanding of tumor evolution and metastasis. Clin Transl Med. 2017;6:15. [PubMed: 28405930]CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Niu F, Wang DC, JP L, Wu W, Wang XD. Potentials of single-cell biology in identification and validation of disease biomarkers. J Cell Mol Med. 2016;20:1789–95. [PubMed: 27113384]CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Treutlein B, Brownfield DG, AR W, Neff NF, Mantalas GL, Espinoza FH, Desai TJ, Krasnow MA, Quake SR. Reconstructing lineage hierarchies of the distal lung epithelium using single cell RNA-seq. Nature. 2014;509:371–5. [PubMed: 24739965]CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Qian M, Wang DC, Chen H, Cheng Y. Detection of single cell heterogeneity in cancer. Semin Cell Dev Biol. 2017;64:143–9. [PubMed: 27619166]CrossRefPubMedGoogle Scholar
  58. 58.
    Ni X, Zhuo M, Su Z, Duan J, Gao Y, Wang Z, Zong C, Bai H, Chapman AR, Zhao J, et al. Reproducible copy number variation patterns among single circulating tumor cells of lung cancer patients. Proc Natl Acad Sci U S A. 2013;110:21083–8. [PubMed: 24324171]CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Wang W, Zhu B, Wang X. Dynamic phenotypes: illustrating a single-cell odyssey. Cell Biol Toxicol. 2017. https://doi.org/10.1007/s10565-017-9400-2. [PubMed: 28638956]
  60. 60.
    Wang W, Wang X. Single-cell CRISPR screening in drug resistance. Cell Biol Toxicol. 2017;33:207–10. [PubMed: 28474250]CrossRefPubMedGoogle Scholar
  61. 61.
    Wang Y, Navin NE. Advances and applications of single cell sequencing technologies. Mol Cell. 2015;58:598–609. [PubMed: 26000845]CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Matzov D, Bashan A, Yonath A. A bright future for antibiotics? Annu Rev Biochem. 2017;86:567–83. [PubMed: 28654325]CrossRefPubMedGoogle Scholar
  63. 63.
    Yan G, Yan X. Ribosomal proteomics: strategies, approaches, and perspectives. Biochimie. 2015;113:69–77. [PubMed: 25869001]CrossRefPubMedGoogle Scholar

Copyright information

© The Editor(s) (if applicable) and The Author(s) 2018 2017

Authors and Affiliations

  • Linlin Zhang
    • 1
  • William Wang
    • 1
  • Bijun Zhu
    • 1
  • Xiangdong Wang
    • 1
    Email author
  1. 1.Zhongshan Hospital Institute of Clinical ScienceFudan University, Shanghai Medical CollegeShanghaiChina

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