Cross-talk between mitochondrial fusion and the Hippo pathway in controlling cell proliferation during Drosophila development

Genetics

Volumn 203, Issue 4, 2016, Pages 1777-1788

  Deng, Qiannan ^a,b,c   Guo, Ting ^a,b,c   Zhou, Xiu ^c,e   Xi, Yongmei ^a,b,d   Yang, Xiaohang ^a,b,d   Ge, Wanzhong ^a,b,d  

^a Zhejiang University School of Medicine   (China)

^b Zhejiang University   (China)

^c ZHEJIANG UNIVERSITY   (China)

^d ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^e SICHUAN UNIVERSITY   (China)

Author keywords

Cell proliferation; ChChd3; Hippo pathway; Mitochondria

Indexed keywords

BETA GALACTOSIDASE; CELL MEMBRANE PROTEIN; COILED COIL HELIX COILED COIL HELIX DOMAIN CONTAINING 3 PROTEIN; MARF PROTEIN; MESSENGER RNA; MITOCHONDRIAL PROTEIN; OPA1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; CHCHD3 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; HPO PROTEIN, DROSOPHILA; MEMBRANE PROTEIN; MFN2 PROTEIN, DROSOPHILA; NUCLEAR PROTEIN; OPA1 PROTEIN, DROSOPHILA; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; TRANSACTIVATOR PROTEIN; YORKIE PROTEIN, DROSOPHILA;

ARTICLE; CELL FRACTIONATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE ACTIVATION; HIPPO PATHWAY; HOMOZYGOSITY; INNER MEMBRANE; INSECT DEVELOPMENT; LOSS OF FUNCTION MUTATION; MITOCHONDRION; MOLECULAR INTERACTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TISSUE GROWTH; UPREGULATION; ANIMAL; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE;

ANIMALS; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEOSTASIS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANES; NUCLEAR PROTEINS; OXIDATIVE STRESS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS;

EID: 84981505079     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.186445     Document Type: Article

References (38)

1. Boland, M. L., A. H. Chourasia, and K. F. Macleod, 2013 Mitochondrial dysfunction in cancer. Front. Oncol. 3: 292.
2. Chan, D. C., 2006 Mitochondria: dynamic organelles in disease, aging, and development. Cell 125: 1241–1252.
3. Chan, D. C., 2012 Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 46: 265–287.
4. Darshi, M., V. L. Mendiola, M. R. Mackey, A. N. Murphy, A. Koller et al., 2011 ChChd3, an inner mitochondrial membrane protein, is essential for maintaining crista integrity and mitochondrial function. J. Biol. Chem. 286: 2918–2932.
5. Dorn, 2nd, G. W., C. F. Clark, W. H. Eschenbacher, M. Y. Kang, J. T. Engelhard et al., 2011 MARF and Opa1 control mitochondrial and cardiac function in Drosophila. Circ. Res. 108: 12–17.
6. Gaspar, P., and N. Tapon, 2014 Sensing the local environment: actin architecture and Hippo signalling. Curr. Opin. Cell Biol. 31: 74–83.
7. Halder, G., and R. L. Johnson, 2011 Hippo signaling: growth control and beyond. Development 138: 9–22.
8. Harvey, K. F., C. M. Pfleger, and I. K. Hariharan, 2003 The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114: 457–467.
9. Harvey, K. F., X. Zhang, and D. M. Thomas, 2013 The Hippo pathway and human cancer. Nat. Rev. Cancer 13: 246–257.
10. Huang, J., S. Wu, J. Barrera, K. Matthews, and D. Pan, 2005 The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122: 421–434.
11. Irvine, K. D., and K. F. Harvey, 2015 Control of Organ Growth by Patterning and Hippo Signaling in Drosophila. Cold Spring Harb. Perspect. Biol. 7: pii: a019224.
12. Itoh, K., K. Nakamura, M. Iijima, and H. Sesaki, 2013 Mitochondrial dynamics in neurodegeneration. Trends Cell Biol. 23: 64– 71.
13. Kasahara, A., and L. Scorrano, 2014 Mitochondria: from cell death executioners to regulators of cell differentiation. Trends Cell Biol. 24: 761–770.
14. Kashatus, J. A., A. Nascimento, L. J. Myers, A. Sher, F. L. Byrne et al., 2015 Erk2 phosphorylation of Drp1 promotes mitochondrial fission and MAPK-driven tumor growth. Mol. Cell 57: 537–551.
15. Mandal, S., P. Guptan, E. Owusu-Ansah, and U. Banerjee, 2005 Mitochondrial regulation of cell cycle progression during development as revealed by the tenured mutation in Drosophila. Dev. Cell 9: 843–854.
16. Martin-Blanco, E., A. Gampel, J. Ring, K. Virdee, N. Kirov et al., 1998 puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 12: 557–570.
17. Mishra, P., and D. C. Chan, 2014 Mitochondrial dynamics and inheritance during cell division, development and disease. Nat. Rev. Mol. Cell Biol. 15: 634–646.
18. Mitra, K., 2013 Mitochondrial fission-fusion as an emerging key regulator of cell proliferation and differentiation. BioEssays 35: 955–964.
19. Nagaraj, R., S. Gururaja-Rao, K. T. Jones, M. Slattery, N. Negre et al., 2012 Control of mitochondrial structure and function by the Yorkie/YAP oncogenic pathway. Genes Dev. 26: 2027–2037.
20. Nunnari, J., and A. Suomalainen, 2012 Mitochondria: in sickness and in health. Cell 148: 1145–1159.
21. Ohsawa, S., Y. Sato, M. Enomoto, M. Nakamura, A. Betsumiya et al., 2012 Mitochondrial defect drives non-autonomous tumour progression through Hippo signalling in Drosophila. Nature 490: 547–551.
22. Owusu-Ansah, E., A. Yavari, S. Mandal, and U. Banerjee, 2008 Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nat. Genet. 40: 356–361.
23. Pan, D., 2010 The hippo signaling pathway in development and cancer. Dev. Cell 19: 491–505.
24. Pantalacci, S., N. Tapon, and P. Leopold, 2003 The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat. Cell Biol. 5: 921–927.
25. Plouffe, S. W., A. W. Hong, and K. L. Guan, 2015 Disease implications of the Hippo/YAP pathway. Trends Mol. Med. 21: 212– 222.
26. Ren, F., L. Zhang, and J. Jiang, 2010 Hippo signaling regulates Yorkie nuclear localization and activity through 14–3-3 dependent and independent mechanisms. Dev. Biol. 337: 303–312.
27. Sandoval, H., C. K. Yao, K. Chen, M. Jaiswal, T. Donti et al., 2014 Mitochondrial fusion but not fission regulates larval growth and synaptic development through steroid hormone production. eLife 3: e03558.
28. Schauble, S., C. C. King, M. Darshi, A. Koller, K. Shah et al., 2007 Identification of ChChd3 as a novel substrate of the cAMP-dependent protein kinase (PKA) using an analog-sensitive catalytic subunit. J. Biol. Chem. 282: 14952–14959.
29. Schroeder, M. C., and G. Halder, 2012 Regulation of the Hippo pathway by cell architecture and mechanical signals. Semin. Cell Dev. Biol. 23: 803–811.
30. Serasinghe, M. N., S. Y. Wieder, T. T. Renault, R. Elkholi, J. J. Asciolla et al., 2015 Mitochondrial division is requisite to RAS-induced transformation and targeted by oncogenic MAPK pathway inhibitors. Mol. Cell 57: 521–536.
31. Sing, A., Y. Tsatskis, L. Fabian, I. Hester, R. Rosenfeld et al., 2014 The atypical cadherin fat directly regulates mitochondrial function and metabolic state. Cell 158: 1293–1308.
32. Sykiotis, G. P., and D. Bohmann, 2008 Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev. Cell 14: 76–85.
33. Udan, R. S., M. Kango-Singh, R. Nolo, C. Tao, and G. Halder, 2003 Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat. Cell Biol. 5: 914–920.
34. van der Bliek, A. M., Q. Shen, and S. Kawajiri, 2013 Mechanisms of mitochondrial fission and fusion. Cold Spring Harb. Perspect. Biol. 5: pii: a011072.
35. Wu, S., J. Huang, J. Dong, and D. Pan, 2003 hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114: 445–456.
36. Xu, T., W. Wang, S. Zhang, R. A. Stewart, and W. Yu, 1995 Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121: 1053–1063.
37. Yarosh, W., J. Monserrate, J. J. Tong, S. Tse, P. K. Le et al., 2008 The molecular mechanisms of OPA1-mediated optic atrophy in Drosophila model and prospects for antioxidant treatment. PLoS Genet. 4: e6.
38. Yu, F. X., and K. L. Guan, 2013 The Hippo pathway: regulators and regulations. Genes Dev. 27: 355–371.