Primary cilia in stem cells and neural progenitors are regulated by neutral sphingomyelinase 2 and ceramide

Molecular Biology of the Cell

Volumn 25, Issue 11, 2014, Pages 1715-1729

  Hea, Qian ^a   Wang, Guanghu ^a   Wakade, Sushama ^a   Dasgupta, Somsankar ^a   Dinkins, Michael ^a   Konga, Ji Na ^a   Spassieva, Stefka D ^b   Bieberich, Erhard ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; CERAMIDE; HISTONE DEACETYLASE 6; PROTEIN KINASE C; SPHINGOMYELIN PHOSPHODIESTERASE; TUBULIN; AURKA PROTEIN, HUMAN; HDAC6 PROTEIN, HUMAN; HISTONE DEACETYLASE; SMPD3 PROTEIN, HUMAN;

ACETYLATION; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME SUBSTRATE; EUKARYOTIC FLAGELLUM; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STEM CELL; ANIMAL; CELL MEMBRANE; CYTOLOGY; CYTOSOL; DRUG EFFECTS; EMBRYONIC STEM CELL; ENZYMOLOGY; METABOLISM; MOUSE; ORGANOGENESIS; PLURIPOTENT STEM CELL; PROTEIN DEGRADATION; PROTEIN TRANSPORT; SPINDLE APPARATUS;

ACETYLATION; ANIMALS; AURORA KINASE A; CELL DIFFERENTIATION; CELL MEMBRANE; CERAMIDES; CILIA; CYTOSOL; EMBRYONIC STEM CELLS; ENZYME ACTIVATION; HISTONE DEACETYLASES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; NEURAL STEM CELLS; ORGANOGENESIS; PROTEIN KINASE C; PROTEIN TRANSPORT; PROTEOLYSIS; SPHINGOMYELIN PHOSPHODIESTERASE; SPINDLE APPARATUS; TUBULIN;

EID: 84901684237     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-12-0730     Document Type: Article

References (64)

1. Amador-Arjona A, Elliott J, Miller A, Ginbey A, Pazour GJ, Enikolopov G, Roberts AJ, Terskikh AV (2011). Primary cilia regulate proliferation of amplifying progenitors in adult hippocampus: implications for learning and memory. J Neurosci 31, 9933-9944.
2. Aubin I et al. (2005). A deletion in the gene encoding sphingomyelin phosphodiesterase 3 (Smpd3) results in osteogenesis and dentinogenesis imperfecta in the mouse. Nat Genet 37, 803-805. (Pubitemid 41077104)
3. Bieberich E, Kawaguchi T, Yu RK (2000). N-acylated serinol is a novel ceramide mimic inducing apoptosis in neuroblastoma cells. J Biol Chem 275, 177-181. (Pubitemid 30038969)
4. Bieberich E, MacKinnon S, Silva J, Noggle S, Condie BG (2003). Regulation of cell death in mitotic neural progenitor cells by asymmetric distribution of prostate apoptosis response 4 (PAR-4) and simultaneous elevation of endogenous ceramide. J Cell Biol 162, 469-479. (Pubitemid 36988555)
5. Bougie JK, Cai D, Hastings M, Farah CA, Chen S, Fan X, McCamphill PK, Glanzman DL, Sossin WS (2012). Serotonin-induced cleavage of the atypical protein kinase C Apl III in Aplysia. J Neurosci 32, 14630-14640.
6. Butler KV, Kalin J, Brochier C, Vistoli G, Langley B, Kozikowski AP (2010). Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J Am Chem Soc 132, 10842-10846.
7. Cao M, Li G, Pan J (2009). Regulation of cilia assembly, disassembly, and length by protein phosphorylation. Methods Cell Biol 94, 333-346.
8. Chalfant CE, Ogretmen B, Galadari S, Kroesen BJ, Pettus BJ, Hannun YA (2001). FAS activation induces dephosphorylation of SR proteins; dependence on the de novo generation of ceramide and activation of protein phosphatase 1. J Biol Chem 276, 44848-44855.
9. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L (2009). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27, 275-280.
10. Clarke CJ, Wu BX, Hannun YA (2011). The neutral sphingomyelinase family: identifying biochemical connections. Adv Enzyme Regul 51, 51-58.
11. Cowart LA, Okamoto Y, Lu X, Hannun YA (2006). Distinct roles for de novo versus hydrolytic pathways of sphingolipid biosynthesis in Saccharomyces cerevisiae. Biochem J 393, 733-740. (Pubitemid 43163813)
12. Cowart LA, Szulc Z, Bielawska A, Hannun YA (2002). Structural determinants of sphingolipid recognition by commercially available anti-ceramide antibodies. J Lipid Res 43, 2042-2048. (Pubitemid 35471070)
13. Desai K, Sullards MC, Allegood J, Wang E, Schmelz EM, Hartl M, Humpf HU, Liotta DC, Peng Q, Merrill AH Jr (2002). Fumonisins and fumonisin analogs as inhibitors of ceramide synthase and inducers of apoptosis. Biochim Biophys Acta 1585, 188-192. (Pubitemid 36096857)
14. Dhara SK, Hasneen K, Machacek DW, Boyd NL, Rao RR, Stice SL (2008). Human neural progenitor cells derived from embryonic stem cells in feeder-free cultures. Differentiation 76, 454-464. (Pubitemid 351725842)
15. Dhara SK, Stice SL (2008). Neural differentiation of human embryonic stem cells. J Cell Biochem 105, 633-640.
16. Dobierzewska A, Shi L, Karakashian AA, Nikolova-Karakashian MN (2012). Interleukin 1beta regulation of FoxO1 protein content and localization: evidence for a novel ceramide-dependent mechanism. J Biol Chem 287, 44749-44760.
17. Garin G, Abe J, Mohan A, Lu W, Yan C, Newby AC, Rhaman A, Berk BC (2007). Flow antagonizes TNF-alpha signaling in endothelial cells by inhibiting caspase-dependent PKC zeta processing. Circ Res 101, 97-105. (Pubitemid 47094628)
18. Gerdes JM, Davis EE, Katsanis N (2009). The vertebrate primary cilium in development, homeostasis, and disease. Cell 137, 32-45.
19. Govindarajan N, Rao P, Burkhardt S, Sananbenesi F, Schluter OM, Bradke F, Lu J, Fischer A (2013). Reducing HDAC6 ameliorates cognitive deficits in a mouse model for Alzheimer's disease. EMBO Mol Med 5, 52-63.
20. Gradilone SA, Radtke BN, Bogert PS, Huang BQ, Gajdos GB, Larusso NF (2013). HDAC6 inhibition restores ciliary expression and decreases tumor growth. Cancer Res 73, 2259-2270.
21. Han YG, Alvarez-Buylla A (2010). Role of primary cilia in brain development and cancer. Curr Opin Neurobiol 20, 58-67.
22. He Q, Wang G, Dasgupta S, Dinkins M, Zhu G, Bieberich E (2012). Characterization of an apical ceramide-enriched compartment regulating ciliogenesis. Mol Biol Cell 23, 3156-3166.
23. Hunkapiller J, Singla V, Seol A, Reiter JF (2011). The ciliogenic protein Oral-Facial-Digital 1 regulates the neuronal differentiation of embryonic stem cells. Stem Cells Dev 20, 831-841.
24. Kim DW, Hirth F (2009). Genetic mechanisms regulating stem cell self-renewal and differentiation in the central nervous system of Drosophila. Cell Adh Migr 3, 402-411.
25. Kiprilov EN et al. (2008). Human embryonic stem cells in culture possess primary cilia with hedgehog signaling machinery. J Cell Biol 180, 897-904. (Pubitemid 351398417)
26. Komatsu Y, Mishina Y (2013). Establishment of left-right asymmetry in vertebrate development: the node in mouse embryos. Cell Mol Life Sci 70, 4659-4666.
27. Krishnamurthy K, Dasgupta S, Bieberich E (2007a). Development and characterization of a novel anti-ceramide antibody. J Lipid Res 48, 968-975. (Pubitemid 46557902)
28. Krishnamurthy K, Wang G, Silva J, Condie BG, Bieberich E (2007b). Ceramide regulates atypical PKCz/l-mediated cell polarity in primitive ectoderm cells: a novel function of sphingolipids in morphogenesis. J Biol Chem 282, 3379-3390. (Pubitemid 47084368)
29. Krut O, Wiegmann K, Kashkar H, Yazdanpanah B, Kronke M (2006). Novel tumor necrosis factor-responsive mammalian neutral sphingomyelinase-3 is a C-tail-anchored protein. J Biol Chem 281, 13784-13793. (Pubitemid 43855294)
30. Lee CY, Andersen RO, Cabernard C, Manning L, Tran KD, Lanskey MJ, Bashirullah A, Doe CQ (2006). Drosophila Aurora-A kinase inhibits neuroblast self-renewal by regulating aPKC/Numb cortical polarity and spindle orientation. Genes Dev 20, 3464-3474. (Pubitemid 44969163)
31. Lee DF et al. (2012). Regulation of embryonic and induced pluripotency by aurora kinase-p53 signaling. Cell Stem Cell 11, 179-194.
32. Loktev AV, Zhang Q, Beck JS, Searby CC, Scheetz TE, Bazan JF, Slusarski DC, Sheffield VC, Jackson PK, Nachury MV (2008). A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev Cell 15, 854-865.
33. Marasas WF et al. (2004). Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr 134, 711-716. (Pubitemid 38456233)
34. Marchesini N, Luberto C, Hannun YA (2003). Biochemical properties of mammalian neutral sphingomyelinase 2 and its role in sphingolipid metabolism. J Biol Chem 278, 13775-13783. (Pubitemid 36799914)
35. Mizutani Y, Tamiya-Koizumi K, Nakamura N, Kobayashi M, Hirabayashi Y, Yoshida S (2001). Nuclear localization of neutral sphingomyelinase 1: biochemical and immunocytochemical analyses. J Cell Sci 114, 3727-3736. (Pubitemid 33041054)
36. Mori D, Yamada M, Mimori-Kiyosue Y, Shirai Y, Suzuki A, Ohno S, Saya H, Wynshaw-Boris A, Hirotsune S (2009). An essential role of the aPKC-Aurora A-NDEL1 pathway in neurite elongation by modulation of microtubule dynamics. Nat Cell Biol 11, 1057-1068.
37. Ogretmen B, Pettus BJ, Rossi MJ, Wood R, Usta J, Szulc Z, Bielawska A, Obeid LM, Hannun YA (2002). Biochemical mechanisms of the generation of endogenous long chain ceramide in response to exogenous short chain ceramide in the A549 human lung adenocarcinoma cell line. Role for endogenous ceramide in mediating the action of exogenous ceramide. J Biol Chem 277, 12960-12969. (Pubitemid 34952664)
38. Pan J, Snell W (2007). The primary cilium: keeper of the key to cell division. Cell 129, 1255-1257. (Pubitemid 46970712)
39. Persico A, Cervigni RI, Barretta ML, Corda D, Colanzi A (2010). Golgi partitioning controls mitotic entry through Aurora-A kinase. Mol Biol Cell 21, 3708-3721.
40. Pruett ST, Bushnev A, Hagedorn K, Adiga M, Haynes CA, Sullards MC, Liotta DC, Merrill AH Jr (2008). Biodiversity of sphingoid bases (" sphingosines") and related amino alcohols. J Lipid Res 49, 1621-1639.
41. Pugacheva EN, Jablonski SA, Hartman TR, Henske EP, Golemis EA (2007). HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129, 1351-1363. (Pubitemid 46962087)
42. Qin J, Berdyshev E, Poirer C, Schwartz NB, Dawson G (2012). Neutral sphingomyelinase 2 deficiency increases hyaluronan synthesis by up-regulation of hyaluronan synthase 2 through decreased ceramide production and activation of Akt. J Biol Chem 287, 13620-13632.
43. Reichert H (2011). Drosophila neural stem cells: cell cycle control of self-renewal, differentiation, and termination in brain development. Results Probl Cell Differ 53, 529-546.
44. Rohatgi R, Milenkovic L, Scott MP (2007). Patched1 regulates hedgehog signaling at the primary cilium. Science 317, 372-376. (Pubitemid 47106377)
45. Ruat M, Roudaut H, Ferent J, Traiffort E (2012). Hedgehog trafficking, cilia and brain functions. Differentiation 83, S97-104.
46. Satir P, Pedersen LB, Christensen ST (2010). The primary cilium at a glance. J Cell Sci 123, 499-503.
47. Sauane M et al. (2010). Ceramide plays a prominent role in MDA-7/IL-24-induced cancer-specific apoptosis. J Cell Physiol 222, 546-555.
48. Smith L, Chen L, Reyland ME, DeVries TA, Talanian RV, Omura S, Smith JB (2000). Activation of atypical protein kinase C zeta by caspase processing and degradation by the ubiquitin-proteasome system. J Biol Chem 275, 40620-40627. (Pubitemid 32064702)
49. Smith L, Smith JB (2002). Lack of constitutive activity of the free kinase domain of protein kinase C zeta. Dependence on transphosphorylation of the activation loop. J Biol Chem 277, 45866-45873. (Pubitemid 35417566)
50. Smith L, Wang Z, Smith JB (2003). Caspase processing activates atypical protein kinase C zeta by relieving autoinhibition and destabilizes the protein. Biochem J 375, 663-671. (Pubitemid 37433514)
51. Spassky N, Han YG, Aguilar A, Strehl L, Besse L, Laclef C, Ros MR, Garcia-Verdugo JM, Alvarez-Buylla A (2008). Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev Biol 317, 246-259.
52. Stoffel W, Jenke B, Holz B, Binczek E, Gunter RH, Knifka J, Koebke J, Niehoff A (2007). Neutral sphingomyelinase (SMPD3) deficiency causes a novel form of chondrodysplasia and dwarfism that is rescued by Col2A1-driven smpd3 transgene expression. Am J Pathol 171, 153-161. (Pubitemid 47339235)
53. Sultan I, Senkal CE, Ponnusamy S, Bielawski J, Szulc Z, Bielawska A, Hannun YA, Ogretmen B (2006). Regulation of the sphingosine-recycling pathway for ceramide generation by oxidative stress, and its role in controlling c-Myc/Max function. Biochem J 393, 513-521. (Pubitemid 43099090)
54. Swistowski A, Peng J, Liu Q, Mali P, Rao MS, Cheng L, Zeng X (2010). Efficient generation of functional dopaminergic neurons from human induced pluripotent stem cells under defined conditions. Stem Cells 28, 1893-1904.
55. Toughiri R, Li X, Du Q, Bieberich CJ (2013). Phosphorylation of NuMA by Aurora-A kinase in PC-3 prostate cancer cells affects proliferation, survival, and interphase NuMA localization. J Cell Biochem 114, 823-830.
56. Valenzuela-Fernandez A, Cabrero JR, Serrador JM, Sanchez-Madrid F (2008). HDAC6: a key regulator of cytoskeleton, cell migration and cell-cell interactions. Trends Cell Biol 18, 291-297.
57. Wang G, Krishnamurthy K, Bieberich E (2009a). Regulation of primary cilia formation by ceramide. J Lipid Res 50, 2103-2110.
58. Wang G, Krishnamurthy K, Chiang YW, Dasgupta S, Bieberich E (2008). Regulation of neural progenitor cell motility by ceramide and potential implications for mouse brain development. J Neurochem 106, 718-733.
59. Wang G, Krishnamurthy K, Umapathy NS, Verin AD, Bieberich E (2009b). The carboxyl-terminal domain of atypical protein kinase Czeta binds to ceramide and regulates junction formation in epithelial cells. J Biol Chem 284, 14469-14475.
60. Wang G, Silva J, Krishnamurthy K, Tran E, Condie BG, Bieberich E (2005). Direct binding to ceramide activates protein kinase Czeta before the formation of a pro-apoptotic complex with PAR-4 in differentiating stem cells. J Biol Chem 280, 26415-26424. (Pubitemid 41022238)
61. Wu BX, Clarke CJ, Hannun YA (2010a). Mammalian neutral sphingomyelinases: regulation and roles in cell signaling responses. Neuromol Med 12, 320-330.
62. Wu BX, Rajagopalan V, Roddy PL, Clarke CJ, Hannun YA (2010b). Identification and characterization of murine mitochondria-associated neutral sphingomyelinase (MA-nSMase), the mammalian sphingomyelin phosphodiesterase 5. J Biol Chem 285, 17993-18002.
63. Xiong Y, Zhao K, Wu J, Xu Z, Jin S, Zhang YQ (2013). HDAC6 mutations rescue human tau-induced microtubule defects in Drosophila. Proc Natl Acad Sci USA 110, 4604-4609.
64. Yamada M, Hirotsune S, Wynshaw-Boris A (2010). The essential role of LIS1, NDEL1 and Aurora-A in polarity formation and microtubule organization during neurogenesis. Cell Adh Migr 4, 180-184.