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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Emerging role of Hippo pathway in the regulation of hematopoiesis

  • Inyoung Kim (Department of Biochemistry, Chungnam National University) ;
  • Taeho Park (Aging Convergence Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Ji-Yoon Noh (Aging Convergence Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Wantae Kim (Department of Biochemistry, Chungnam National University)
  • Received : 2023.05.18
  • Accepted : 2023.07.28
  • Published : 2023.08.31
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Abstract

In various organisms, the Hippo signaling pathway has been identified as a master regulator of organ size determination and tissue homeostasis. The Hippo signaling coordinates embryonic development, tissue regeneration and differentiation, through regulating cell proliferation and survival. The YAP and TAZ (YAP/TAZ) act as core transducers of the Hippo pathway, and they are tightly and exquisitely regulated in response to various intrinsic and extrinsic stimuli. Abnormal regulation or genetic variation of the Hippo pathway causes a wide range of human diseases, including cancer. Recent studies have revealed that Hippo signaling plays a pivotal role in the immune system and cancer immunity. Due to pathophysiological importance, the emerging role of Hippo signaling in blood cell differentiation, known as hematopoiesis, is receiving much attention. A number of elegant studies using a genetically engineered mouse (GEM) model have shed light on the mechanistic and physiological insights into the Hippo pathway in the regulation of hematopoiesis. Here, we briefly review the function of Hippo signaling in the regulation of hematopoiesis and immune cell differentiation.

Keywords

Acknowledgement

This work was supported by research fund of Chungnam National University.

References

  1. Xu T, Wang W, Zhang S, Stewart RA and Yu W (1995) Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121, 1053-1063 https://doi.org/10.1242/dev.121.4.1053
  2. Hilman D and Gat U (2011) The evolutionary history of YAP and the hippo/YAP pathway. Mol Biol Evol 28, 2403-2417 https://doi.org/10.1093/molbev/msr065
  3. Justice RW, Zilian O, Woods DF, Noll M and Bryant PJ (1995) The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev 9, 534-546 https://doi.org/10.1101/gad.9.5.534
  4. Kim W and Jho EH (2018) The history and regulatory mechanism of the Hippo pathway. BMB Rep 51, 106-118 https://doi.org/10.5483/BMBRep.2018.51.3.022
  5. Zhao B, Li L, Tumaneng K, Wang CY and Guan KL (2010) A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF (beta-TRCP). Genes Dev 24, 72-85 https://doi.org/10.1101/gad.1843810
  6. Zhao B, Ye X, Yu J et al (2008) TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 22, 1962-1971 https://doi.org/10.1101/gad.1664408
  7. Wang D, He J, Huang B, Liu S, Zhu H and Xu T (2020) Emerging role of the Hippo pathway in autophagy. Cell Death Dis 11, 880
  8. Yamauchi T and Moroishi T (2019) Hippo pathway in mammalian adaptive immune system. Cells 8, 398
  9. Han Y (2019) Analysis of the role of the Hippo pathway in cancer. J Transl Med 17, 116
  10. Taha Z, Janse van Rensburg HJ and Yang X (2018) The hippo pathway: immunity and cancer. Cancers (Basel) 10, 94
  11. Zhao B, Tumaneng K and Guan KL (2011) The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat Cell Biol 13, 877-883 https://doi.org/10.1038/ncb2303
  12. Yu FX, Zhao B and Guan KL (2015) Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell 163, 811-828 https://doi.org/10.1016/j.cell.2015.10.044
  13. Allegra A, Pioggia G, Innao V, Musolino C and Gangemi S (2021) New insights into YES-associated protein signaling pathways in hematological malignancies: diagnostic and therapeutic challenges. Cancers (Basel) 13, 1981
  14. Cottini F, Hideshima T, Xu C et al (2014) Rescue of Hippo coactivator YAP1 triggers DNA damage-induced apoptosis in hematological cancers. Nat Med 20, 599-606 https://doi.org/10.1038/nm.3562
  15. Hu Y, Zhang Z, Kashiwagi M et al (2016) Superenhancer reprogramming drives a B-cell-epithelial transition and high-risk leukemia. Genes Dev 30, 1971-1990 https://doi.org/10.1101/gad.283762.116
  16. Davis AS, Viera AJ and Mead MD (2014) Leukemia: an overview for primary care. Am Fam Physician 89, 731-738
  17. Cacemiro MC, Berzoti-Coelho MG, Cominal JG, Burin SM and Castro FA (2017) Hippo pathway deregulation: implications in the pathogenesis of haematological malignancies. J Clin Pathol 70, 9-14 https://doi.org/10.1136/jclinpath-2016-204055
  18. Ramos A and Camargo FD (2012) The Hippo signaling pathway and stem cell biology. Trends Cell Biol 22, 339-346 https://doi.org/10.1016/j.tcb.2012.04.006
  19. Cheng H, Zheng Z and Cheng T (2020) New paradigms on hematopoietic stem cell differentiation. Protein Cell 11, 34-44 https://doi.org/10.1007/s13238-019-0633-0
  20. Dzierzak E and Philipsen S (2013) Erythropoiesis: development and differentiation. Cold Spring Harb Perspect Med 3, a011601
  21. Althoff MJ, Nayak RC, Hegde S et al (2020) Yap1-Scribble polarization is required for hematopoietic stem cell division and fate. Blood 136, 1824-1836 https://doi.org/10.1182/blood.2019004113
  22. Abdollahpour H, Appaswamy G, Kotlarz D et al (2012) The phenotype of human STK4 deficiency. Blood 119, 3450-3457 https://doi.org/10.1182/blood-2011-09-378158
  23. Marsola A, Simoes BP, Palma LC, Berzoti-Coelho MG, Burin SM and de Castro FA (2018) Expression of Hippo signaling pathway and Aurora kinase genes in chronic myeloid leukemia. Med Oncol 35, 26
  24. Morrison SJ, Uchida N and Weissman IL (1995) The biology of hematopoietic stem cells. Annu Rev Cell Dev Biol 11, 35-71 https://doi.org/10.1146/annurev.cb.11.110195.000343
  25. Orkin SH (2000) Diversification of haematopoietic stem cells to specific lineages. Nat Rev Genet 1, 57-64 https://doi.org/10.1038/35049577
  26. Pietras EM, Warr MR and Passegue E (2011) Cell cycle regulation in hematopoietic stem cells. J Cell Biol 195, 709-720 https://doi.org/10.1083/jcb.201102131
  27. Yang L, Bryder D, Adolfsson J et al (2005) Identification of Lin(-)Sca1(+)kit(+)CD34(+)Flt3- short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients. Blood 105, 2717-2723 https://doi.org/10.1182/blood-2004-06-2159
  28. Orkin SH and Zon LI (2008) Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132, 631-644 https://doi.org/10.1016/j.cell.2008.01.025
  29. Jansson L and Larsson J (2012) Normal hematopoietic stem cell function in mice with enforced expression of the Hippo signaling effector YAP1. PLoS One 7, e32013
  30. Donato E, Biagioni F, Bisso A, Caganova M, Amati B and Campaner S (2018) YAP and TAZ are dispensable for physiological and malignant haematopoiesis. Leukemia 32, 2037-2040 https://doi.org/10.1038/s41375-018-0111-3
  31. Goode DK, Obier N, Vijayabaskar MS et al (2016) Dynamic gene regulatory networks drive hematopoietic specification and differentiation. Dev Cell 36, 572-587 https://doi.org/10.1016/j.devcel.2016.01.024
  32. Adamo L, Naveiras O, Wenzel PL et al (2009) Biomechanical forces promote embryonic haematopoiesis. Nature 459, 1131-1135 https://doi.org/10.1038/nature08073
  33. Vining KH and Mooney DJ (2017) Mechanical forces direct stem cell behaviour in development and regeneration. Nat Rev Mol Cell Biol 18, 728-742 https://doi.org/10.1038/nrm.2017.108
  34. Seo J and Kim J (2018) Regulation of Hippo signaling by actin remodeling. BMB Rep 51, 151-156 https://doi.org/10.5483/BMBRep.2018.51.3.012
  35. Lundin V, Sugden WW, Theodore LN et al (2020) YAP regulates hematopoietic stem cell formation in response to the biomechanical forces of blood flow. Dev Cell 52, 446-460 e445
  36. Lee DH, Kim TS, Lee D and Lim DS (2018) Mammalian sterile 20 kinase 1 and 2 are important regulators of hematopoietic stem cells in stress condition. Sci Rep 8, 942
  37. Nejigane S, Takahashi S, Haramoto Y, Michiue T and Asashima M (2013) Hippo signaling components, Mst1 and Mst2, act as a switch between self-renewal and differentiation in Xenopus hematopoietic and endothelial progenitors. Int J Dev Biol 57, 407-414 https://doi.org/10.1387/ijdb.130010st
  38. Zhou X, Wang H, Li D, Song N, Yang F and Xu W (2022) MST1/2 inhibitor XMU-MP-1 alleviates the injury induced by ionizing radiation in haematopoietic and intestinal system. J Cell Mol Med 26, 1621-1628 https://doi.org/10.1111/jcmm.17203
  39. Zhang N, Bai H, David KK et al (2010) The Merlin/NF2 tumor suppressor functions through the YAP oncoprotein to regulate tissue homeostasis in mammals. Dev Cell 19, 27-38 https://doi.org/10.1016/j.devcel.2010.06.015
  40. Larsson J, Ohishi M, Garrison B et al (2008) Nf2/merlin regulates hematopoietic stem cell behavior by altering microenvironmental architecture. Cell Stem Cell 3, 221-227 https://doi.org/10.1016/j.stem.2008.06.005
  41. Blom B and Spits H (2006) Development of human lymphoid cells. Annu Rev Immunol 24, 287-320 https://doi.org/10.1146/annurev.immunol.24.021605.090612
  42. Ciofani M and Zuniga-Pflucker JC (2007) The thymus as an inductive site for T lymphopoiesis. Annu Rev Cell Dev Biol 23, 463-493 https://doi.org/10.1146/annurev.cellbio.23.090506.123547
  43. Germain RN (2002) T-cell development and the CD4-CD8 lineage decision. Nat Rev Immunol 2, 309-322 https://doi.org/10.1038/nri798
  44. Mou F, Praskova M, Xia F et al (2012) The Mst1 and Mst2 kinases control activation of rho family GTPases and thymic egress of mature thymocytes. J Exp Med 209, 741-759 https://doi.org/10.1084/jem.20111692
  45. Dong Y, Du X, Ye J et al (2009) A cell-intrinsic role for Mst1 in regulating thymocyte egress. J Immunol 183, 3865-3872 https://doi.org/10.4049/jimmunol.0900678
  46. Tang F, Gill J, Ficht X et al (2015) The kinases NDR1/2 act downstream of the Hippo homolog MST1 to mediate both egress of thymocytes from the thymus and lymphocyte motility. Sci Signal 8, ra100
  47. Katagiri K, Imamura M and Kinashi T (2006) Spatiotemporal regulation of the kinase Mst1 by binding protein RAPL is critical for lymphocyte polarity and adhesion. Nat Immunol 7, 919-928 https://doi.org/10.1038/ni1374
  48. Geng J, Yu S, Zhao H et al (2017) The transcriptional coactivator TAZ regulates reciprocal differentiation of T(H)17 cells and T(reg) cells. Nat Immunol 18, 800-812 https://doi.org/10.1038/ni.3748
  49. Li C, Bi Y, Li Y et al (2017) Dendritic cell MST1 inhibits Th17 differentiation. Nat Commun 8, 14275
  50. Du X, Shi H, Li J et al (2014) Mst1/Mst2 regulate development and function of regulatory T cells through modulation of Foxo1/Foxo3 stability in autoimmune disease. J Immunol 192, 1525-1535 https://doi.org/10.4049/jimmunol.1301060
  51. Du X, Wen J, Wang Y et al (2018) Hippo/Mst signalling couples metabolic state and immune function of CD8alpha(+) dendritic cells. Nature 558, 141-145 https://doi.org/10.1038/s41586-018-0177-0
  52. Alsufyani F, Mattoo H, Zhou D et al (2018) The Mst1 kinase is required for follicular B cell homing and B-1 B cell development. Front Immunol 9, 2393
  53. Branehog I, Ridell B, Swolin B and Weinfeld A (1975) Megakaryocyte quantifications in relation to thrombokinetics in primary thrombocythaemia and allied diseases. Scand J Haematol 15, 321-332 https://doi.org/10.1111/j.1600-0609.1975.tb01087.x
  54. Guo T, Wang X, Qu Y, Yin Y, Jing T and Zhang Q (2015) Megakaryopoiesis and platelet production: insight into hematopoietic stem cell proliferation and differentiation. Stem Cell Investig 2, 3
  55. Kaushansky K (2008) Historical review: megakaryopoiesis and thrombopoiesis. Blood 111, 981-986 https://doi.org/10.1182/blood-2007-05-088500
  56. Ganem NJ, Cornils H, Chiu SY et al (2014) Cytokinesis failure triggers hippo tumor suppressor pathway activation. Cell 158, 833-848 https://doi.org/10.1016/j.cell.2014.06.029
  57. Aylon Y, Michael D, Shmueli A, Yabuta N, Nojima H and Oren M (2006) A positive feedback loop between the p53 and Lats2 tumor suppressors prevents tetraploidization. Genes Dev 20, 2687-2700 https://doi.org/10.1101/gad.1447006
  58. Roy A, Lordier L, Pioche-Durieu C et al (2016) Uncoupling of the Hippo and Rho pathways allows megakaryocytes to escape the tetraploid checkpoint. Haematologica 101, 1469-1478 https://doi.org/10.3324/haematol.2016.149914
  59. Takeuchi K, Satoh M, Kuno H, Yoshida T, Kondo H and Takeuchi M (1998) Platelet-like particle formation in the human megakaryoblastic leukaemia cell lines, MEG-01 and MEG-01s. Br J Haematol 100, 436-444 https://doi.org/10.1046/j.1365-2141.1998.00576.x
  60. Lorthongpanich C, Jiamvoraphong N, Klaihmon P et al (2020) Effect of YAP/TAZ on megakaryocyte differentiation and platelet production. Biosci Rep 40, BSR20201780
  61. Lorthongpanich C, Jiamvoraphong N, Supraditaporn K, Klaihmon P, U-Pratya Y and Issaragrisil S (2017) The Hippo pathway regulates human megakaryocytic differentiation. Thromb Haemost 117, 116-126 https://doi.org/10.1160/TH16-07-0564
  62. Ruan B and Paulson RF (2022) Metabolic regulation of stress erythropoiesis, outstanding questions, and possible paradigms. Front Physiol 13, 1063294
  63. Baron MH, Vacaru A and Nieves J (2013) Erythroid development in the mammalian embryo. Blood Cells Mol Dis 51, 213-219 https://doi.org/10.1016/j.bcmd.2013.07.006
  64. Damkham N, Lorthongpanich C, Klaihmon P et al (2022) YAP and TAZ play a crucial role in human erythrocyte maturation and enucleation. Stem Cell Res Ther 13, 467
  65. Griffiths RE, Kupzig S, Cogan N et al (2012) Maturing reticulocytes internalize plasma membrane in glycophorin A-containing vesicles that fuse with autophagosomes before exocytosis. Blood 119, 6296-6306 https://doi.org/10.1182/blood-2011-09-376475
  66. Hao S, Matsui Y, Lai ZC and Paulson RF (2019) Yap1 promotes proliferation of transiently amplifying stress erythroid progenitors during erythroid regeneration. Exp Hematol 80, 42-54 e44
  67. Cowland JB and Borregaard N (2016) Granulopoiesis and granules of human neutrophils. Immunol Rev 273, 11-28 https://doi.org/10.1111/imr.12440
  68. Dancey JT, Deubelbeiss KA, Harker LA and Finch CA (1976) Neutrophil kinetics in man. J Clin Invest 58, 705-715 https://doi.org/10.1172/JCI108517
  69. Wynn TA, Chawla A and Pollard JW (2013) Macrophage biology in development, homeostasis and disease. Nature 496, 445-455 https://doi.org/10.1038/nature12034
  70. Wang S, Zhou L, Ling L et al (2020) The Crosstalk between Hippo-YAP pathway and innate immunity. Front Immunol 11, 323
  71. Buchon N, Silverman N and Cherry S (2014) Immunity in Drosophila melanogaster--from microbial recognition to whole-organism physiology. Nat Rev Immunol 14, 796-810 https://doi.org/10.1038/nri3763
  72. Banerjee U, Girard JR, Goins LM and Spratford CM (2019) Drosophila as a genetic model for hematopoiesis. Genetics 211, 367-417 https://doi.org/10.1534/genetics.118.300223
  73. Ferguson GB and Martinez-Agosto JA (2014) Yorkie and Scalloped signaling regulates Notch-dependent lineage specification during Drosophila hematopoiesis. Curr Biol 24, 2665-2672 https://doi.org/10.1016/j.cub.2014.09.081
  74. Nordin N, Fathrita Mohd Amir S, Rahimi Yusop M and Rozali Othman M (2015) Decolorization of C. I. reactive orange 4 and textile effluents by electrochemical oxidation technique using silver-carbon composite electrode. Acta Chim Slov 62, 642-651 https://doi.org/10.17344/acsi.2014.1264
  75. Milton CC, Grusche FA, Degoutin JL et al (2014) The Hippo pathway regulates hematopoiesis in Drosophila melanogaster. Curr Biol 24, 2673-2680 https://doi.org/10.1016/j.cub.2014.10.031
  76. Anderson AM, Bailetti AA, Rodkin E, De A and Bach EA (2017) A genetic screen reveals an unexpected role for yorkie signaling in JAK/STAT-dependent hematopoietic malignancies in Drosophila melanogaster. G3 (Bethesda) 7, 2427-2438 https://doi.org/10.1534/g3.117.044172
  77. Mo JS, Park HW and Guan KL (2014) The Hippo signaling pathway in stem cell biology and cancer. EMBO Rep 15, 642-656 https://doi.org/10.15252/embr.201438638
  78. Varelas X, Sakuma R, Samavarchi-Tehrani P et al (2008) TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat Cell Biol 10, 837-848 https://doi.org/10.1038/ncb1748
  79. Lian I, Kim J, Okazawa H et al (2010) The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev 24, 1106-1118 https://doi.org/10.1101/gad.1903310