纤毛/鞭毛内运输调控精子发生
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摘要
纤毛/鞭毛内运输机制(IFT)在纤毛/鞭毛形成中发挥非常保守的作用,精子尾部鞭毛轴丝的发育与纤毛形成类似,均由纤毛内运输调控。在所有哺乳动物细胞中,精子尾部含有的鞭毛最长,但目前极少有研究关注IFT在精子鞭毛形成中的作用及其机制。本文将讨论精子发生过程中IFT的作用及其在调控男性生殖健康中的重要性。
Intra flagellar transport(IFT) is an evolutionarily conserved mechanism thought to be essential for the assembly and maintenance of most eukaryotic cilia and flagella. Development of the sperm tail axoneme resembles the cilia formation, which is organized by intraflagellar transport(IFT). Of all mammalian cells, sperm have the longest motile cilia, but few studies are reported on the role of IFT in the formation of sperm flagella and the mechanisms of IFT in spermiogenesis. This article focuses on the role of IFT in spermatogenesis and the importance of IFT in male fertility.
Intra flagellar transport(IFT) is an evolutionarily conserved mechanism thought to be essential for the assembly and maintenance of most eukaryotic cilia and flagella. Development of the sperm tail axoneme resembles the cilia formation, which is organized by intraflagellar transport(IFT). Of all mammalian cells, sperm have the longest motile cilia, but few studies are reported on the role of IFT in the formation of sperm flagella and the mechanisms of IFT in spermiogenesis. This article focuses on the role of IFT in spermatogenesis and the importance of IFT in male fertility.
引文
[1] Keady BT, Samtani R, Tobita K, et al. IFT25 links the signal-dependent movement of Hedgehog components to intraflagellar transport. Dev Cell, 2012, 22(5): 940-951.
[2] Bhogaraju S, Taschner M, Morawetz M, et al. Crystal structure of the intraflagellar transport complex 25/27. EMBO J, 2011, 30(10): 1907-1918.
[3] Lechtreck KF. IFT-cargo interactions and protein transport in cilia. Trends Biochem Sci, 2015, 40(12): 765-778.
[4] Taschner M, Lorentzen E. The intraflagellar transport machinery. Cold Spring Harb Perspect Biol, 2016, 8(10). pii: a028092..
[5] Fan ZC, Behal RH, Geimer S, et al. Chlamydomonas IFT70/CrDYF-1 is a core component of IFT particle complex B and is required for flagellar assembly. Mol Biol Cell, 2010, 21(15): 2696-2706.
[6] Baldari CT, Rosenbaum J. Intraflagellar transport: It's not just for cilia any more. Curr Opin Cell Biol, 2010, 22(1): 75-80.
[7] Sedmak T, Wolfrum U. Intraflagellar transport molecules in ciliary and nonciliary cells of the retina. J Cell Biol, 2010, 189(1): 171-186.
[8] Follit JA, Xu F, Keady BT, et al. Characterization of mouse IFT complex B. Cell Motil Cytoskeleton, 2009, 66(8): 457-468.
[9] Follit JA, Tuft RA, Fogarty KE, et al. The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol Biol Cell, 2006, 17(9): 3781-3792.
[10] Pampliega O, Orhon I, Patel B, et al. Functional interaction between autophagy and ciliogenesis. Nature, 2013, 502(7470): 194-200.
[11] Ishikawa H, Marshall WF. Intraflagellar transport and ciliary dynamics. Cold Spring Harb Perspect Biol, 2017, 9(3). pii: a021998.
[12] Diniz MC, Pacheco AC, Farias KM, et al. The eukaryotic flagellum makes the day: Novel and unforeseen roles uncovered after post-genomics and proteomics data. Curr Protein Pept Sci, 2012, 13(6): 524-546.
[13] Avidor-Reiss T, Leroux MR. Shared and distinct mechanisms of compartmentalized and cytosolic ciliogenesis. Curr Biol, 2015, 25(23): R1143-R1150.
[14] Lechtreck KF, Van De Weghe JC, Harris JA, et al. Protein transport in growing and steady-state cilia. Traffic (Copenhagen, Denmark), 2017, 18(5): 277-286.
[15] Sloboda RD. Purification and localization of Iintraflagellar transport particles and polypeptides. Methods Mol Biol, 2016, 1365: 119-137.
[16] Cole DG. The intraflagellar transport machinery of Chlamydomonas reinhardtii. Traffic (Copenhagen, Denmark), 2003, 4(7): 435-442.
[17] Rosenbaum JL, Witman GB. Intraflagellar transport. Nat Rev Mol Cell Biol, 2002, 3(11): 813-825.
[18] Tull D, Vince JE, Callaghan JM, et al. SMP-1, a member of a new family of small myristoylated proteins in kinetoplastid parasites, is targeted to the flagellum membrane in Leishmania. Mol Biol Cell, 2004, 15(11): 4775-4786.
[19] Prevo B, Scholey JM, Peterman EJG. Intraflagellar transport: Mechanisms of motor action, cooperation, and cargo delivery. FEBS J, 2017, 284(18): 2905-2931.
[20] Kierszenbaum AL, Rivkin E, Tres LL, et al. GMAP210 and IFT88 are present in the spermatid golgi apparatus and participate in the development of the acrosome-acroplaxome complex, head-tail coupling apparatus and tail. Dev Dyn, 2011, 240(3): 723-736.
[21] du Plessis SS, Kashou AH, Benjamin DJ, et al. Proteomics: A subcellular look at spermatozoa. Reprod Biol Endocrinol, 2011, 9: 36.
[22] Kierszenbaum AL, Rivkin E, Tres LL. Cytoskeletal track selection during cargo transport in spermatids is relevant to male fertility. Spermatogenesis, 2011, 1(3): 221-230.
[23] Taschner M, Bhogaraju S, Lorentzen E. Architecture and function of IFT complex proteins in ciliogenesis. Differentiation, 2012, 83(2): S12-S22.
[24] Michael T, Fruzsina K, Philipp B, et al. Crystal structures of IFT70/52 and IFT52/46 provide insight into intraflagellar transport B core complex assembly. J Cell Biol, 2014, 207(2): 269-282.
[25] Taschner M, Mour?o A, Awasthi M, et al. Structural basis of outer dynein arm intraflagellar transport by the transport adaptor protein ODA16 and the intraflagellar transport protein IFT46. J Biolog Chem, 2017, 292(18): 7462-7473.
[26] Nishijima Y, Hagiya Y, Kubo T, et al. RABL2 interacts with the intraflagellar transport-B complex and CEP19 and participates in ciliary assembly. Mol Biol Cell, 2017, 28(12): 1652-1666.
[27] Scholey JM, Anderson KV. Intraflagellar transport and cilium-based signaling. Cell, 2006, 125(3): 439-442.
[28] Pan J, Snell W. The primary cilium: Keeper of the key to cell division. Cell, 2007, 129(7): 1255-1257.
[29] Wemmer KA, Marshall WF. Flagellar length control in chlamydomonas — paradigm for organelle size regulation. Int Rev cytol, 2007, 260: 175-212.
[30] Freitas MJ, Fardilha MJ. Intraflagellar protein 88 interactome analysis: A bioinformatics approach highlights its role in testis and sperm function. J Biophys Chem, 2014, 5(3): 99-106.
[31] Bhogaraju S, Engel BD, Lorentzen E. Intraflagellar transport complex structure and cargo interactions. Cilia, 2013, 2(1): 10.
[32] Engel BD, Ishikawa H, Wemmer KA, et al. The role of retrograde intraflagellar transport in flagellar assembly, maintenance, and function. J Cell Biol, 2012, 199(1): 151-167.
[33] Inaba K, Mizuno K. Sperm dysfunction and ciliopathy. Reprod Med Biol, 2016, 15(2): 77-94.
[34] Linck RW, Chemes H, Albertini DF. The axoneme: The propulsive engine of spermatozoa and cilia and associated ciliopathies leading to infertility. J Assist Reprod Genetics, 2016, 33(2): 141-156.
[35] Praveen K, Davis EE, Katsanis N. Unique among ciliopathies: Primary ciliary dyskinesia, a motile cilia disorder. F1000Prime Rep, 2015, 7: 36.
[36] Ko JY, Park JH. Mouse models of polycystic kidney disease induced by defects of ciliary proteins. BMB Rep, 2013, 46(2): 73-79.
[37] Jonassen JA, San Agustin J, Follit JA, et al. Deletion of IFT20 in the mouse kidney causes misorientation of the mitotic spindle and cystic kidney disease. J Cell Biol, 2008, 183(3): 377-384.
[38] Castaneda JM, Hua R, Miyata H, et al. TCTE1 is a conserved component of the dynein regulatory complex and is required for motility and metabolism in mouse spermatozoa. Pro Natl Acad Sci USA, 2017, 114(27): e5370-e5378.
[39] Swiderski RE, Yoko N, Mullins RF, et al. A mutation in the mouse ttc26 gene leads to impaired hedgehog signaling. PLoS Genetics, 2014, 10(10): e1004689.
[40] Bangs F, Anderson KV. Primary cilia and mammalian hedgehog signaling. Cold Spring Harb Perspect Biol, 2016, 9(5). pii: a028175.
[41] Ocbina PJ, Eggenschwiler JT, Ivan M, et al. Complex interactions between genes controlling trafficking in primary cilia. Nat Genetics, 2011, 43(6): 547-553.
[42] Lehti MS, Sironen A. Formation and function of the manchette and flagellum during spermatogenesis. Reproduction (Cambridge, England), 2016, 151(4): R43-R54.
[43] Lehti MS, Kotaja N, Sironen A. KIF3A is essential for sperm tail formation and manchette function. Mol Cell Endocrinol, 2013, 377(1-2): 44-55.
[44] Zhang Y, Ou Y, Cheng M, et al. KLC3 is involved in sperm tail midpiece formation and sperm function. Dev Biol, 2012, 366(2): 101-110.
[45] Yuan X, Garrett-Sinha LA, Sarkar D, et al. Deletion of IFT20 in early stage T lymphocyte differentiation inhibits the development of collagen-induced arthritis. Bone Res, 2014, 2: 14038.
[46] Sironen A, Uimari P, Iso-Touru T, et al. L1 insertion within SPEF2 gene is associated with increased litter size in the Finnish Yorkshire population. J Anim Breed Genetics, 2012, 129(2): 92-97.
[47] Follit JA, San Agustin JT, Xu F, et al. The Golgin GMAP210/TRIP11 anchors IFT20 to the Golgi complex. PLoS Genetics, 2008, 4(12): e1000315.
[48] Zhang Z, Li W, Zhang Y, et al. Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice. Mol Biol Cell, 2016, pii: mbc.E16-05-0318.
[49] Keady BT, Le YZ, Pazour GJ. IFT20 is required for opsin trafficking and photoreceptor outer segment development. Mol Biol Cell, 2011, 22(7): 921-930.
[50] Taulman PD, Haycraft CJ, Balkovetz DF, et al. Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol Biol Cell, 2001, 12(3): 589-599.
[51] San Agustin JT, Pazour GJ, Witman GB. Intraflagellar transport is essential for mammalian spermiogenesis but is absent in mature sperm. Mol Biol Cell, 2015, 26(24): 4358-4372.
[52] Kierszenbaum AL. Intramanchette transport (IMT): Managing the making of the spermatid head, centrosome, and tail. Mol Reprod Dev, 2002, 63(1): 1-4.
[53] Sironen A, Hansen J, Thomsen B, et al. Expression of SPEF2 during mouse spermatogenesis and identification of IFT20 as an interacting protein. Biol Reprod, 2010, 82(3): 580-590.
[54] Liu H, Li W, Zhang Y, et al. IFT25, an intraflagellar transporter protein dispensable for ciliogenesis in somatic cells, is essential for sperm flagella formation. Biol Reprod, 2017, 96(5): 993-1006.
[55] Loreng TD, Smith EF. The central apparatus of cilia and eukaryotic flagella. Cold Spring Harb Perspect Biol, 2017, 9(2). pii: a028118.
[56] Mitchell DR. Speculations on the evolution of 9+2 organelles and the role of central pair microtubules. Biol Cell, 2004, 96(9): 691-696.
[57] Eddy EM, Toshimori K, O'Brien DA. Fibrous sheath of mammalian spermatozoa. Microscopy research and technique, 2003, 61(1): 103-115.
[58] Eddy EM. The scaffold role of the fibrous sheath. Soc Reprod Fertil Suppl, 2007, 65: 45-62.
[59] Yang N, Li L, Eguether T, et al. Intraflagellar transport 27 is essential for hedgehog signaling but dispensable for ciliogenesis during hair follicle morphogenesis. Development (Cambridge, England), 2015, 142(16): 2860.
[60] Eguether T, San Agustin JT, Keady BT, et al. IFT27 links the BBSome to IFT for maintenance of the ciliary signaling compartment. Dev Cell, 2014, 31(3): 279-290.
[61] Zhang Y, Liu H, Li W, et al. Intraflagellar transporter protein (IFT27), an IFT25 binding partner, is essential for male fertility and spermiogenesis in mice. Dev Biol, 2017, 432(1): 125-139.
[62] Levental I, Veatch S. The Continuing Mystery of Lipid Rafts. J Mol Biol, 2016, 428(24 Pt A): 4749-4764.
[63] Zhang Y, Liu H, Li W, et al. Intraflagellar transporter protein 140 (IFT140), a component of IFT-A complex, is essential for male fertility and spermiogenesis in mice. Cytoskeleton (Hoboken, NJ), 2018, 75(2): 70-84.
[64] Hirano T, Katoh Y, Nakayama K. Intraflagellar transport-A complex mediates ciliary entry and retrograde trafficking of ciliary G protein-coupled receptors. Mol Biol Cell, 2017, 28(3): 429-439.
[2] Bhogaraju S, Taschner M, Morawetz M, et al. Crystal structure of the intraflagellar transport complex 25/27. EMBO J, 2011, 30(10): 1907-1918.
[3] Lechtreck KF. IFT-cargo interactions and protein transport in cilia. Trends Biochem Sci, 2015, 40(12): 765-778.
[4] Taschner M, Lorentzen E. The intraflagellar transport machinery. Cold Spring Harb Perspect Biol, 2016, 8(10). pii: a028092..
[5] Fan ZC, Behal RH, Geimer S, et al. Chlamydomonas IFT70/CrDYF-1 is a core component of IFT particle complex B and is required for flagellar assembly. Mol Biol Cell, 2010, 21(15): 2696-2706.
[6] Baldari CT, Rosenbaum J. Intraflagellar transport: It's not just for cilia any more. Curr Opin Cell Biol, 2010, 22(1): 75-80.
[7] Sedmak T, Wolfrum U. Intraflagellar transport molecules in ciliary and nonciliary cells of the retina. J Cell Biol, 2010, 189(1): 171-186.
[8] Follit JA, Xu F, Keady BT, et al. Characterization of mouse IFT complex B. Cell Motil Cytoskeleton, 2009, 66(8): 457-468.
[9] Follit JA, Tuft RA, Fogarty KE, et al. The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol Biol Cell, 2006, 17(9): 3781-3792.
[10] Pampliega O, Orhon I, Patel B, et al. Functional interaction between autophagy and ciliogenesis. Nature, 2013, 502(7470): 194-200.
[11] Ishikawa H, Marshall WF. Intraflagellar transport and ciliary dynamics. Cold Spring Harb Perspect Biol, 2017, 9(3). pii: a021998.
[12] Diniz MC, Pacheco AC, Farias KM, et al. The eukaryotic flagellum makes the day: Novel and unforeseen roles uncovered after post-genomics and proteomics data. Curr Protein Pept Sci, 2012, 13(6): 524-546.
[13] Avidor-Reiss T, Leroux MR. Shared and distinct mechanisms of compartmentalized and cytosolic ciliogenesis. Curr Biol, 2015, 25(23): R1143-R1150.
[14] Lechtreck KF, Van De Weghe JC, Harris JA, et al. Protein transport in growing and steady-state cilia. Traffic (Copenhagen, Denmark), 2017, 18(5): 277-286.
[15] Sloboda RD. Purification and localization of Iintraflagellar transport particles and polypeptides. Methods Mol Biol, 2016, 1365: 119-137.
[16] Cole DG. The intraflagellar transport machinery of Chlamydomonas reinhardtii. Traffic (Copenhagen, Denmark), 2003, 4(7): 435-442.
[17] Rosenbaum JL, Witman GB. Intraflagellar transport. Nat Rev Mol Cell Biol, 2002, 3(11): 813-825.
[18] Tull D, Vince JE, Callaghan JM, et al. SMP-1, a member of a new family of small myristoylated proteins in kinetoplastid parasites, is targeted to the flagellum membrane in Leishmania. Mol Biol Cell, 2004, 15(11): 4775-4786.
[19] Prevo B, Scholey JM, Peterman EJG. Intraflagellar transport: Mechanisms of motor action, cooperation, and cargo delivery. FEBS J, 2017, 284(18): 2905-2931.
[20] Kierszenbaum AL, Rivkin E, Tres LL, et al. GMAP210 and IFT88 are present in the spermatid golgi apparatus and participate in the development of the acrosome-acroplaxome complex, head-tail coupling apparatus and tail. Dev Dyn, 2011, 240(3): 723-736.
[21] du Plessis SS, Kashou AH, Benjamin DJ, et al. Proteomics: A subcellular look at spermatozoa. Reprod Biol Endocrinol, 2011, 9: 36.
[22] Kierszenbaum AL, Rivkin E, Tres LL. Cytoskeletal track selection during cargo transport in spermatids is relevant to male fertility. Spermatogenesis, 2011, 1(3): 221-230.
[23] Taschner M, Bhogaraju S, Lorentzen E. Architecture and function of IFT complex proteins in ciliogenesis. Differentiation, 2012, 83(2): S12-S22.
[24] Michael T, Fruzsina K, Philipp B, et al. Crystal structures of IFT70/52 and IFT52/46 provide insight into intraflagellar transport B core complex assembly. J Cell Biol, 2014, 207(2): 269-282.
[25] Taschner M, Mour?o A, Awasthi M, et al. Structural basis of outer dynein arm intraflagellar transport by the transport adaptor protein ODA16 and the intraflagellar transport protein IFT46. J Biolog Chem, 2017, 292(18): 7462-7473.
[26] Nishijima Y, Hagiya Y, Kubo T, et al. RABL2 interacts with the intraflagellar transport-B complex and CEP19 and participates in ciliary assembly. Mol Biol Cell, 2017, 28(12): 1652-1666.
[27] Scholey JM, Anderson KV. Intraflagellar transport and cilium-based signaling. Cell, 2006, 125(3): 439-442.
[28] Pan J, Snell W. The primary cilium: Keeper of the key to cell division. Cell, 2007, 129(7): 1255-1257.
[29] Wemmer KA, Marshall WF. Flagellar length control in chlamydomonas — paradigm for organelle size regulation. Int Rev cytol, 2007, 260: 175-212.
[30] Freitas MJ, Fardilha MJ. Intraflagellar protein 88 interactome analysis: A bioinformatics approach highlights its role in testis and sperm function. J Biophys Chem, 2014, 5(3): 99-106.
[31] Bhogaraju S, Engel BD, Lorentzen E. Intraflagellar transport complex structure and cargo interactions. Cilia, 2013, 2(1): 10.
[32] Engel BD, Ishikawa H, Wemmer KA, et al. The role of retrograde intraflagellar transport in flagellar assembly, maintenance, and function. J Cell Biol, 2012, 199(1): 151-167.
[33] Inaba K, Mizuno K. Sperm dysfunction and ciliopathy. Reprod Med Biol, 2016, 15(2): 77-94.
[34] Linck RW, Chemes H, Albertini DF. The axoneme: The propulsive engine of spermatozoa and cilia and associated ciliopathies leading to infertility. J Assist Reprod Genetics, 2016, 33(2): 141-156.
[35] Praveen K, Davis EE, Katsanis N. Unique among ciliopathies: Primary ciliary dyskinesia, a motile cilia disorder. F1000Prime Rep, 2015, 7: 36.
[36] Ko JY, Park JH. Mouse models of polycystic kidney disease induced by defects of ciliary proteins. BMB Rep, 2013, 46(2): 73-79.
[37] Jonassen JA, San Agustin J, Follit JA, et al. Deletion of IFT20 in the mouse kidney causes misorientation of the mitotic spindle and cystic kidney disease. J Cell Biol, 2008, 183(3): 377-384.
[38] Castaneda JM, Hua R, Miyata H, et al. TCTE1 is a conserved component of the dynein regulatory complex and is required for motility and metabolism in mouse spermatozoa. Pro Natl Acad Sci USA, 2017, 114(27): e5370-e5378.
[39] Swiderski RE, Yoko N, Mullins RF, et al. A mutation in the mouse ttc26 gene leads to impaired hedgehog signaling. PLoS Genetics, 2014, 10(10): e1004689.
[40] Bangs F, Anderson KV. Primary cilia and mammalian hedgehog signaling. Cold Spring Harb Perspect Biol, 2016, 9(5). pii: a028175.
[41] Ocbina PJ, Eggenschwiler JT, Ivan M, et al. Complex interactions between genes controlling trafficking in primary cilia. Nat Genetics, 2011, 43(6): 547-553.
[42] Lehti MS, Sironen A. Formation and function of the manchette and flagellum during spermatogenesis. Reproduction (Cambridge, England), 2016, 151(4): R43-R54.
[43] Lehti MS, Kotaja N, Sironen A. KIF3A is essential for sperm tail formation and manchette function. Mol Cell Endocrinol, 2013, 377(1-2): 44-55.
[44] Zhang Y, Ou Y, Cheng M, et al. KLC3 is involved in sperm tail midpiece formation and sperm function. Dev Biol, 2012, 366(2): 101-110.
[45] Yuan X, Garrett-Sinha LA, Sarkar D, et al. Deletion of IFT20 in early stage T lymphocyte differentiation inhibits the development of collagen-induced arthritis. Bone Res, 2014, 2: 14038.
[46] Sironen A, Uimari P, Iso-Touru T, et al. L1 insertion within SPEF2 gene is associated with increased litter size in the Finnish Yorkshire population. J Anim Breed Genetics, 2012, 129(2): 92-97.
[47] Follit JA, San Agustin JT, Xu F, et al. The Golgin GMAP210/TRIP11 anchors IFT20 to the Golgi complex. PLoS Genetics, 2008, 4(12): e1000315.
[48] Zhang Z, Li W, Zhang Y, et al. Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice. Mol Biol Cell, 2016, pii: mbc.E16-05-0318.
[49] Keady BT, Le YZ, Pazour GJ. IFT20 is required for opsin trafficking and photoreceptor outer segment development. Mol Biol Cell, 2011, 22(7): 921-930.
[50] Taulman PD, Haycraft CJ, Balkovetz DF, et al. Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol Biol Cell, 2001, 12(3): 589-599.
[51] San Agustin JT, Pazour GJ, Witman GB. Intraflagellar transport is essential for mammalian spermiogenesis but is absent in mature sperm. Mol Biol Cell, 2015, 26(24): 4358-4372.
[52] Kierszenbaum AL. Intramanchette transport (IMT): Managing the making of the spermatid head, centrosome, and tail. Mol Reprod Dev, 2002, 63(1): 1-4.
[53] Sironen A, Hansen J, Thomsen B, et al. Expression of SPEF2 during mouse spermatogenesis and identification of IFT20 as an interacting protein. Biol Reprod, 2010, 82(3): 580-590.
[54] Liu H, Li W, Zhang Y, et al. IFT25, an intraflagellar transporter protein dispensable for ciliogenesis in somatic cells, is essential for sperm flagella formation. Biol Reprod, 2017, 96(5): 993-1006.
[55] Loreng TD, Smith EF. The central apparatus of cilia and eukaryotic flagella. Cold Spring Harb Perspect Biol, 2017, 9(2). pii: a028118.
[56] Mitchell DR. Speculations on the evolution of 9+2 organelles and the role of central pair microtubules. Biol Cell, 2004, 96(9): 691-696.
[57] Eddy EM, Toshimori K, O'Brien DA. Fibrous sheath of mammalian spermatozoa. Microscopy research and technique, 2003, 61(1): 103-115.
[58] Eddy EM. The scaffold role of the fibrous sheath. Soc Reprod Fertil Suppl, 2007, 65: 45-62.
[59] Yang N, Li L, Eguether T, et al. Intraflagellar transport 27 is essential for hedgehog signaling but dispensable for ciliogenesis during hair follicle morphogenesis. Development (Cambridge, England), 2015, 142(16): 2860.
[60] Eguether T, San Agustin JT, Keady BT, et al. IFT27 links the BBSome to IFT for maintenance of the ciliary signaling compartment. Dev Cell, 2014, 31(3): 279-290.
[61] Zhang Y, Liu H, Li W, et al. Intraflagellar transporter protein (IFT27), an IFT25 binding partner, is essential for male fertility and spermiogenesis in mice. Dev Biol, 2017, 432(1): 125-139.
[62] Levental I, Veatch S. The Continuing Mystery of Lipid Rafts. J Mol Biol, 2016, 428(24 Pt A): 4749-4764.
[63] Zhang Y, Liu H, Li W, et al. Intraflagellar transporter protein 140 (IFT140), a component of IFT-A complex, is essential for male fertility and spermiogenesis in mice. Cytoskeleton (Hoboken, NJ), 2018, 75(2): 70-84.
[64] Hirano T, Katoh Y, Nakayama K. Intraflagellar transport-A complex mediates ciliary entry and retrograde trafficking of ciliary G protein-coupled receptors. Mol Biol Cell, 2017, 28(3): 429-439.